Responsive Document: CREW: Department of Agriculture: Regarding Pesticides: 8/1/2014

Control Number: 7112161
COLONY COLLAPSE DISORDER

2010 ANNUAL PROGRESS REPORT
CCD Steering Committee

June 2011
Mention of trade names or commercial products in this report is solely for the purpose of
providing specific information and does not imply recommendation or endorsement by the U.S.
Department of Agriculture.
This publication reports research involving pesticides. It does not contain recommendations for
their use, nor does it imply that uses discussed here have been registered. All uses of pesticides
must be registered by appropriate State and/or Federal agencies before they can be
recommended.
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Cover: Adult honey bee on a flower. Photo courtesy of David Cappaert, Michigan State
University, Bugwood.org.
CCD Steering Committee Members
USDA Agricultural Research Service (co-chair)

Kevin Hackett
USDA National Institute of Food and Agriculture (co-chair)
Mary Purcell-Miramontes
USDA Animal and Plant Health Inspection Service
Robyn Rose
Colin Stewart
Alan Dowdy
USDA National Agricultural Statistics Service
Bruce Boess
USDA Natural Resources Conservation Service
Doug Holy
USDA Office of Pest Management Policy
Sheryl Kunickis
David Epstein
Environmental Protection Agency
Tom Steeger
Tom Moriarty
Allen Vaughan
Executive Summary
Mandated by section 7204(h)(4) of the Food Conservation and Energy Act, Pub. Law
No. 110-246, the 2008 Farm Bill, this third annual report of research progress during 2010
on Honey Bee Colony Collapse Disorder (CCD) represents the work of a large number of
scientists from 8 Federal agencies, 2 State departments of agriculture, 22 universities, and
several private research efforts.
In response to the unexplained losses of U.S. honey bee colonies now known as Colony Collapse
Disorder (CCD), USDAs Agricultural Research Service (ARS) and National Institute of Food
and Agriculture (NIFA) led a collaborative effort to define an approach for responding to CCD,
resulting in the CCD Action Plan, in July 2007. Other Federal agencies e.g., the Animal and
Plant Health Inspection Service (APHIS), the Natural Resources Conservation Service, and the
Environmental Protection Agencys (EPAs) Office of Pesticide Programs have been members
of the CCD Steering Committee for many years; this year, USDAs Office of Pest Management
Policy and the National Agricultural Statistics Service have joined the Steering Committee.
Many universities and organizations (i.e., Federal, State, and private) were also involved in
developing this plan and are carrying out work that addresses the CCD problem.
Annual surveys clearly show that overall colony losses continue to be as high as 30 percent or
more since CCD began to be reported. Beekeepers cannot economically sustain such high levels
of losses indefinitely. Although a number of factors have been associated with CCD and
pollinator declines in general, no single factor or specific combination of factors has been
identified as a cause. Factors associated with declines include disease/parasites, nutrition,
pesticides, bee management practices, habitat fragmentation, and agricultural practices.
Reducing the incidence of CCD and pollinator declines will likely require managing multiple
factors simultaneously. Overall losses to managed pollinators were about 33 percent. Relative
to the overall losses, CCD contributed approximately 8 percent in recent national surveys.
However, losses to individual beekeepers attributed to CCD may vary significantly by size of the
beekeeping operation. Therefore, this statistic is just a rough estimate.
To help ensure more robust pollinator health, the CCD Steering Committee is facilitating the
development of science-based best management strategies that integrate current research results
associated with CCD incidence and pollinator decline in general. As part of these efforts, the
CCD Steering Committee member agencies are working together to examine ways to mitigate
impacts on pollinator health. This effort requires coordination across different Federal partners
(USDA, Department of Interior, and EPA), States, and stakeholders to ensure a sustained effort
that effectively integrates management options.
The CCD Steering Committee believes that it is necessary for scientists, beekeepers, and growers
to reconvene in the next year to revisit approaches and research, which are now needed to
counter honey bee decline, taking into account information developed during the past 3 years and
to revise the 2007 Action Plan to reflect the current state of knowledge. A range of stakeholders
will be engaged to develop strategies for managing factors associated with diminished pollinator
health and not focus exclusively on CCD.
Research is ongoing in the four topic areas outlined in the CCD Action Plan, but the studies
encompass factors involved in bee losses in general, not just due to CCD. The four areas are (1)
survey and sample data collection, (2) analysis of existing samples, (3) research to identify
factors affecting honey bee health, including attempts to recreate CCD symptomology, and
(4) mitigation and management preventive measures. Progress in each of the four topic areas
is highlighted below.
Topic I: Survey and Sample Data Collection. Surveys continue to provide evidence of
high honey bee losses due to CCD and declines in pollinator health. Correlated with
these high levels of losses, research has shown that weak colonies had overall increased
pathogen levels and showed evidence of pesticide residues, although no pattern of
specific pathogens or pesticides was indicated. Colonies in comparatively good health
also contained a wide range of pesticide residues. To understand the potential role of
pesticides in pollinator declines, representatives of the CCD Steering Committee
(APHIS, ARS, and EPA) participated in a Society of Environmental Toxicology and
Chemistry global Pellston conference. The purpose was to develop a risk assessment
process for honey bees and non-Apis bees and to identify the exposure and effects data
needed to inform that process.
Topic II: Analysis of Existing Samples. Previously, viruses and other pathogens and
parasites were found to be present at greater levels in CCD colonies than in non-CCD
colonies. The extent to which pesticides are associated with CCD remains uncertain, and
additional research is necessary. Studies in 2010 revealed several new viruses and other
pathogens affecting honey bees. Further studies are needed to determine if these new
pathogens are involved in CCD-affected hives.
Topic III: Research to Identify Factors Affecting Honey Bee Health, Including
Attempts to Recreate CCD Symptomology. CCD was initially characterized by the rapid
loss of adult worker bees from the colony, lack of dead worker bees, and delayed
invasion of hive pests. Although additional studies are needed, researchers have recently
observed that Varroa mite and other pathogens such as Nosema may be contributing
factors to CCD. In addition, the Varroa mite and other pathogens occur at levels that are
typically considered below economic thresholds. Researchers continue their efforts to
document whether there are correlations between the presence of Varroa mites, diverse
pathogens, and pesticides, which appear to impact overall colony health. In addition,
apiaries surrounded by intensively farmed landscapes were found to be associated with
higher colony losses in the spring.
Topic IV: Mitigation and Management Preventive Measures. Two national multiyear
projects, the ARS Area-wide Project on Honey Bee Health and a NIFA-funded
Coordinated Agricultural Project (CAP), are continuing to make progress in developing
managements strategies to combat bee losses. A new CAP project funded by NIFA, the
Bee Informed Partnership (http://beeinformed.org), has begun to examine bee
management practices and facilitate communication of successful practices between
beekeepers. The eXtension Community of Practice (www.extension.org/bee health) is
also disseminating information on honey bee health and management practices.
Colony Collapse Disorder (CCD)

Annual Progress Report
This report is the third annual report prepared in response to section 7204(h)(4) of the
2008 Farm Bill, which directed the Secretary of Agriculture to
submit to the Committee on Agriculture of the House of Representatives and the
Committee on Agriculture, Nutrition, and Forestry of the Senate an annual report
describing the progress made by the Department of Agriculture in
(A) Investigating the cause or causes of honey bee colony collapse; and
(B) Finding appropriate strategies to reduce colony loss.
Background and Highlights of Research
After the large-scale, unexplained losses of managed U.S. honey bee (Apis mellifera L.) colonies
during the winter of 20062007, investigators identified a set of symptoms that were termed
Colony Collapse Disorder (CCD). In response to this problem, Federal and State government,
university, and private researchers, led by USDAs Agricultural Research Service (ARS) and
National Institute of Food and Agriculture (NIFA), mobilized to define an approach to CCD, an
effort resulting in formation of the CCD Steering Committee and publication of the CCD Action
Plan in July 2007. Over the past several years, the CCD Steering Committee has included
representatives from USDA (Animal and Plant Health Inspection Service (APHIS), NIFA, ARS,
and Natural Resources Conservation Service [NRCS]) and the Environmental Protection
Agencys (EPA) Office of Pesticide Programs. This year, USDAs Office of Pest Management
Policy (OPMP) and National Agricultural Statistics Service (NASS) joined the Steering
Committee. Many organizations, public and private, in addition to those represented on the CCD
Steering Committee, are involved in the work to address the CCD problem.
During the past 3 years, numerous causes for CCD have been proposed and examined. There
have been many associations identified throughout the course of research; however, the strength
of these associations has varied considerably, and it has become increasingly clear that no single
factor alone is responsible for the malady.
Researchers continue to document elevated pathogen levels in CCD-affected bees, although no
single pathogen or group of pathogens has been definitively linked to CCD. In addition, studies
that examined colonies for the presence of known honey bee parasites, such as the Varroa mite
(Varroa destructor), tracheal mite (Acarapis woodi), and the fungal gut parasite Nosema spp.,
have not found that any of these parasites by themselves occurred at sufficient levels or pattern to
explain CCD.
During the past year, several independent studies have shown that bees are exposed to a wide
range of pesticides and that some of these pesticides at high concentrations interact with other
pesticides, honey bee parasites, or viruses in ways that significantly increase individual bee
mortality. Further studies are needed to ascertain whether these greater-than-additive effects
occur at environmentally relevant pesticide concentrations. In addition, studies have shown that
exposure to pesticides can result in effects on bee behavior. However, further studies on
individual bees are needed to better understand colony-level effects. The pesticides detected
with the greatest frequency and quantities are those used by beekeepers to control mites.
Conversely, bees exposed to the pesticide coumaphos, which is used by beekeepers to treat
Varroa mites, appear to have lower levels of CCD, suggesting that reducing infestation of
Varroa mites could directly or indirectly reduce incidence of CCD. Results from other longterm monitoring projects also suggest that the fungicide chlorothalonil has been associated with a
newly identified condition in the hive named entombed pollen, which is associated with
premature bee mortality. However, it is not yet known whether the presence of chlorothalonil
within honeybee comb is exclusively associated with entombed pollen. Other factors not yet
determined may also have a role. Taken together, these studies illustrate support for the
hypothesis that CCD is a result of many different factors, factors that may work independently or
in combination.
Because CCD is a complex phenomenon, developing effective solutions to the problem will
depend on considerable research commitment. The current coordinated research response is
dedicated to resolving the CCD issue, as well as improving overall pollinator health. NIFAs
Coordinated Agricultural Project (CAP) and ARS Area-wide Project on Honey Bee Health are
ongoing efforts that have taken broad, regional approaches to solving pollinator losses. Funding
from ARS and NIFA, with additional contributions by a number of other sources, including the
National Honey Board, the Almond Board of California, Burts Bees, Haagen-Dazs, the North
American Pollinator Protection Campaign, Project Apis m. (PAm), and the Foundation for the
Preservation of Honey Bees, has supported a variety of new studies and attracted new expertise
to bee health issues. Results from these research efforts are being published, and a new
eXtension bee-health Web site (www.extension.org/bee health) has been assembled to provide
reliable research-based information to beekeepers and the general public.
In an effort to address the multiple factors associated with pollinator declines, the CCD Action
Plan is organized under four topic areas: (1) Survey and sample data collection, (2) analysis of
existing samples, (3) research to identify factors affecting honey bee health, including attempts
to recreate CCD symptomology, and (4) mitigation and management preventive measures.
Summaries of research under each of the four topic areas are presented below. More detailed
accounts of progress on each of the research projects can be found in Appendix 1.
Topic I: Survey and Sample Data Collection
Surveys of beekeepers throughout the United States were jointly conducted for the fourth
consecutive year by the Apiary Inspectors of America and ARS. Total losses (not limited to
CCD) for winter 20102011 were 30 percent, which was in the same range as previous surveys
performed between 2007 and 2009. Most beekeepers indicated that this level of loss was
economically unsustainable for beekeeping operations. Large-scale commercial beekeepers
indicated that losses were due to several contributing factors, including poor queens, Varroa
mite, pesticides, and CCD.
Preliminary results from systematic surveys of experimental apiaries in seven States managed by
NIFA-funded CAP researchers reported that the leading causes of overall losses included
intensive agricultural use of the surrounding landscape, pesticide exposure, and Varroa mite and
diseases. Surveys conducted in Canada and Europe showed that Varroa mite and pathogens
were consistently the leading factors correlated with declines.
USDAs APHIS expanded its survey of beekeepers from 13 to 34 States to detect exotic pests
and diseases of honey bees. The survey conducted thus far has not detected Apis ceranae, the
Slow Paralysis Virus that has been reported in Australia, or the parasitic mite Tropilaelaps,
which commonly is found in Asia on several species of honey bees; so these pests have likely
not invaded the United States. Nosema ceranae, which is a microsporidial pathogen recently
introduced into the United States, was the only species of Nosema detected in this recent APHIS
survey. This species has been tentatively linked in some studies as contributing to CCD in the
United States.
Members of the CCD steering committee (EPA and USDAs APHIS and ARS) participated in a
global Society of Environmental Toxicology and Chemistry (SETAC) Pellston 1 workshop in
January 2011. The global Pellston conference is an important beginning in developing improved
approaches for characterizing potential sublethal impact of pesticides on individual bees and on
colonies, as well as to identify the data needed to inform the risk assessment process. The
SETAC conference also examined the adequacy of tests performed with Apis mellifera to serve
as a model to predict effects on other non-Apis pollinators.
Topic II: Analysis of Existing Samples
As reported in the 2010 Progress Report www.ars.usda.gov/is/br/ccd/ccdprogressreport2010.pdf,
a large survey revealed that levels of pesticides in wax and pollen were similar in both CCD and
healthy colonies. Further analysis showed that levels of the varroacide coumaphos were higher
in healthy control colonies relative to CCD colonies. These preliminary data suggest several
possibilities that need to be examined with more detailed, hypothesis-driven experiments.
Molecular studies by scientists at the University of Illinois seem to support the hypothesis that
exposure to coumaphos may have some beneficial effect on ability of bees to resist pathogens.
They found that honey bee genes express enzymes that can detoxify harmful compounds in
honey and propolis.
In addition, this year the ARS Pollinating Insect Research Laboratory in Logan, Utah, analyzed
existing samples of managed solitary bees used for pollinating crops. These bees were evaluated
to determine whether they were infected by any of the viruses associated with CCD in honey
bees. Some of these honey bee viruses were found in both alfalfa leaf-cutting bees and alkali
bees, with infection rates that ranged from 3 to 34 percent of the population.
The first Pellston Conference was held in 1977 to address the needs and means for assessing the hazards of
chemicals to aquatic life. Since then, many conferences have been held to evaluate current and prospective
environmental issues. Each has focused on a relevant environmental topic, and the proceedings of each have been
published as a peer-reviewed or informal report. These documents have been widely distributed and are valued by
environmental scientists, engineers, regulators, and managers because of their technical basis and their
comprehensive, state-of-the-science reviews. The first four Pellston conferences were initiated before SETAC was
effectively functioning. Beginning with the 1982 conference, however, SETAC has been the primary organizer, and
SETAC members (on a volunteer basis) have been instrumental in planning, conducting, and disseminating
conference results. Taken from: http://www.setac.org/node/104.
Pennsylvania State University extension specialists are working with the USDA Agricultural
Marketing Services National Science Laboratory in North Carolina to analyze wax, pollen, and
brood samples for the presence of pesticides for beekeepers who suspect colony losses associated
with exposure to pesticides. The Foundation for the Preservation of Honey Bees and Project
Apis m. (PAm) are contributing funds to cover half of the cost of the pesticide analysis.
Information from samples is being stored in a centralized database that beekeepers and
researchers can access. At this time, the database is not accessible to the general public.
EPA is collating beekill incident information provided through a variety of sources to document
whether particular pesticides are associated with the losses. While pesticide manufacturers
(registrants) are required to report incident data directly to the EPA, the Agency also relies on
reports from State and local governments and the public to populate its incident database. EPA
has increased the number of options available to the public for reporting beekill incidents directly
to the Agency.
Topic III: Research to Identify Factors Affecting Honey Bee Health, Including Attempts to
Recreate CCD Symptomology
Numerous research efforts jointly supported by ARS and NIFA continue to investigate factors
that may play a role in causing CCD, either alone and/or in combination. Factors include
diseases (parasites and pathogens), pesticides, poor nutrition, beekeeping practices, and to a
lesser extent, other pests such as the small hive beetle.
Possible Mortality Factors and Their Interactions. Researchers at Pennsylvania State
University conducted laboratory bioassays with specific levels of pesticides to measure a variety
of effects on bees. They found synergistic interactions on bee larvae between a crop fungicide
and a miticide used by beekeepers for Varroa control. This means that the bees suffered more
serious effects when exposed to more than one pesticide at the same time and that bee
management practices may be affecting colony health. Further studies using pesticide dosages
equivalent to those actually used in the field (environmentally relevant concentrations) need to
be conducted to show if the laboratory study reflects what actually occurs in the environment.
The researchers also found that larval and adult honey bees had different sensitivities to
pesticides. A fungicide that was very toxic to bee larvae did not kill adult honey bees. These
studies utilized exposure methods that represent the worst case scenario and do not necessarily
reflect how larval bees may actually be exposed through consumption of brood food. Additional
studies demonstrated that common inert ingredients used in pesticides had a high toxicity in
honey bee larvae, although the extent to which these inerts would be present under actual field
conditions is yet to be determined. These preliminary studies suggest that fungicides, inert
ingredients, and pesticide interactions may have crucial impacts on development and survival of
honey bees, depending on the extent to which the inert may be present under the conditions of
actual use.
Previously, scientists at the University of NebraskaLincoln documented the harmful synergistic
effects of certain miticides and fungicide combinations on honey bee health in laboratory studies
(Johnson, et al. 2010). Although further testing needs to occur at environmentally relevant
concentrations, these scientists recommend that beekeepers be cautious about applying these
pesticides in combination. Beekeepers should particularly avoid applying miticides when honey
bees are placed in orchards or other crop settings where exposure to fungicides is likely. Studies
are underway to assess the effects of exposure to simultaneously applied miticides and
fungicides at environmentally relevant concentrations on brood survival, weight gain, and queen
performance.
As previously reported, Israeli acute paralysis virus (IAPV) was found to be associated with
CCD and could be an important CCD indicator. Following up on this finding, ARS scientists
studied the role of Varroa mite in IAPV transmission among honey bees. Because mites feed
and move between adult bees and brood, they have the potential to act as a vector to transmit
pathogens from infected bees to healthy bees, and they have been reported to be associated with
viral disease outbreaks in the field. Research results demonstrated that Varroa mite is a
biological vector of IAPV by supporting replication of the virus and transmitting IAPV among
honey bees. Therefore, controlling Varroa mite might be an important way to reduce the spread
of IAPV in bee hives and could be a strategy for reducing bee decline.
Bumble Bee Decline. Some bumble bee species also have experienced drastic population
declines, even to the point of extinction. This brings into question whether CCD is solely a
honey bee issue or part of a more general problem among bees of many kinds. This past year, a
North American Bumble Bee Conservation Planning meeting was organized for the first time
(November 2010) to bring together researchers, government agency representatives,
conservation organizations, beekeepers, and growers to discuss the recent declines in bumble
bees and identify needs related to bumble bee conservation. The meeting was facilitated by a
representative from the International Union for the Conservation of Nature (IUCN) and resulted
in the formation of a bumble bee specialist group to advise IUCN on bumble bee issues. This
group is preparing a report of its findings.
Immune System Effects. Another study conducted by ARS scientists resulted in a somewhat
counterintuitive conclusion, a finding that temperature-stressed bees were more resistant to
infection by pathogens than nonstressed bees. Using alfalfa leafcutting bees (Megachile
rotundata) as a model, experiments determined that bees exhibit a heightened biological
response to temperature stress that has many similarities to the immune response. Thus, if bees
were stressed by higher temperatures before a pathogen started to invade, infection levels were
lower. The study hypothesized that the pathogen invaded nonstressed bees more readily, as these
bees did not have time to activate their immune response before the pathogen was able to
become established and disable some of the honey bees immune functions.
Topic IV: Mitigation and Management Preventive Measures

Trilateral Discussions to Prevent Invasive Pathogens. To meet the need for a stronger
regulatory framework for controlling the accidental introduction of exotic bee pathogens, APHIS
and ARS initiated trilateral discussions between Mexico, Canada, and the United States through
the North American Plant Protection Organization (NAPPO), with the goal of developing
coordinated guidelines for the regulation and importation of pollen. The importation of pollen as
a source of food for bees is currently not allowed in the United States and Canada, but it is
allowed in Mexico. However, the importation of pollen for human consumption (regulated in the
United States by the Food and Drug Administration) is allowed in all three countries, which
could provide a pathway for the introduction of new pathogens. The NAPPO technical advisory
group is also trying to determine whether mitigation measures such as radiation or ozone are
feasible. APHIS is working to amend its regulations to allow pollen importation for bee feed
under permit with the appropriate safeguards.
Best Management Practices (BMP) Guide. To assist beekeepers and growers relying on
pollinators, a Best Management Practices Guide for Beekeepers Pollinating Californias
Agricultural Crops (www.beeccdcap.uga.edu/documents/bmpcalagr.html) was developed by
members of the NIFA-CAP team. The Guide was published in the American Bee Journal and in
the trade magazine Bee Culture, two of the most widely read beekeeping publications in North
America. The article offers guidance to beekeepers and almond growers in seven areas:
nutrition, Varroa mite control, Nosema control, management of hive equipment, colony
management, business management, and guidance to almond growers renting bees.
Genomics Tools to Manage Varroa Mites. A genome draft sequence was published for the
Varroa mite, revealing potential weak points in mite biology (defensive proteins and proteins
used in chemical mitigation) and candidates for novel controls such as RNA interference
(RNAi). In fact, the publication of mite candidate genes in genomic databases led to worldwide
control studies for this parasite using RNAi technology. Microbes also identified in this study
have been screened across bees and mites as possible controls for Varroa.
Varroa-Resistant Bees for Commercial Use. ARS scientists tested Russian honey bees and
bees containing a Varroa-resistant trait (Varroa-sensitive hygiene [VSH]) for productivity in two
largescale field tests using two different migratory beekeeping routes. Two years of testing
during commercial pollination of almonds, apples, blueberries, and cranberries, with
overwintering in Louisiana, showed the Varroa-resistant stocks to be as large and productive as
control stocks at each pollination site. A 1-year test involving almond pollination and Midwest
honey production, with overwintering in Californias Central Valley, again showed Russian and
VSH bees to have adequate colony size, survivability, and honey production. The results suggest
these Varroa-resistant bees are well suited for commercial pollination services and honey
production.
EPAs Expediting of Reviews for Section 18. EPA is working with State liaison agencies to
provide beekeepers with appropriate tools to control bee colony pests such as Varroa mites. The
Agency is working closely with USDAs ARS and OPMP to expedite reviews of Emergency
Exemption requests (under section 18 of the Federal Insecticide, Fungicide and Rodenticide Act;
FIFRA), Special Local Needs Registrations (under section 24c of FIFRA), and full registrations
(under section 3 of FIFRA) of miticides.
Blue Orchard Bees for Almond Pollination. This past year, three workshops were conducted
by collaborating scientists with the California Farm Advisors and ARS to train almond producers
and blue orchard bee (Osmia lignaria) producers on methods for raising this bee and for using it
effectively as an almond pollinator. Research also continues to seek the best way to integrate
bee hives for the most cost-effective and complete pollination. Field trials were established this
year in a joint collaboration between ARS and almond producers in California.
Bumble Bee Rearing and Investigations of Bumble Bee-Honey Bee Disease Transmission.
Research continued toward developing mass rearing methods for bumble bee colonies using
native western bumble bees (Bombus occidentalis). Eastern U.S. species are thought to carry
diseases that may affect wild bumble bee populations in the Western United States, so
commercially available species are needed for Western farmers.
Pollinator studies have also focused on exploring the use of bumble bees as pollinators and
seeking to determine the relationship between bumble bee and honey bee pests and diseases.
Studies have revealed that bumble bees are affected by IAPV and other viruses and parasites that
affect the honey bee. These findings may have potential implications for the role of these factors
in bee decline and may assist researchers to develop an understanding of, and ultimately
controlling, bee parasites.
Enhancing Pollinator Forage. The Natural Resources Conservation Service has continued to
encourage private landowners to establish or enhance pollinator forage by providing appropriate
flowering plants from early spring through late fall.
The Appendix provides more results and findings from the past year of CCD research, listed
within the framework of the CCD Action Plan.
APPENDIX: Accomplishments by Action Plan Component

Pesticides have been identified as one of the factors that potentially contribute to CCD and to
diminished pollinator health. The EPAs Office of Pesticide Programs (OPP), which is tasked
with regulating pesticides, has been taking several actions to enhance the tools used to regulate
pesticide products.
Global Workshop on Pesticide Risk Assessment for Pollinators, January 2011.
Representatives of the U.S. Department of Agriculture (USDA), including ARS and APHIS, and
EPAs OPP served as panelists in a Society of Environmental Toxicology and Chemistry
(SETAC) global Pellston Workshop on Pesticide Risk Assessment for Pollinators. Workshop
participants totaling 48 from 5 continents were tasked with advancing the current state of the
science of pesticide risk assessment by more thoroughly vetting quantitative and qualitative
measures of exposure and effects on individual bees and at the colony level. The SETAC
Workshop aimed to synthesize global understanding of exposure and effects measurements and
work toward a common/harmonized global process for evaluating and quantitatively
characterizing risk to insect pollinators from exposure to pesticides. The SETAC Workshop
focused on four major topics to
1. Design/identify testing protocols to provide an understanding of potential exposure to
bees (including daily ingestion rates) from pesticide residues in pollen, and nectar, as
well as from exposure through other routes of direct and indirect exposure;
2. Design/identify testing protocols to measure effects of pesticides to developing brood
and adult honey bees at both the individual and colony level;
3. Propose a tiered approach for characterizing the potential risk of pesticides to
pollinators; and
4. Explore the applicability of testing protocols, used for honey bees (Apis bees), to
measure effects of pesticides and pesticide risk to native (non-Apis) insect pollinators.
SETAC will publish an overview (synopsis) of the Workshop online in summer 2011, and the
full proceedings of the workshop will be published by SETAC in early 2012.
EPA has committed to developing a quantitative process for evaluating the potential risks of
pesticides to insect pollinators for use in regulating pesticide products. EPA will examine the
conclusions of the SETAC workshop and will utilize its Scientific Advisory Panel (SAP) to
publicly vet a proposed process in summer 2012.
Coordination with International Partners. Efforts, such as those by EPA, have been underway
to coordinate elements of science and policy with international partners such as the Organization
for Economic Co-operation and Development (OECD) to better understand the potential role of
pesticide use in bee declines. The OECD Working Group on Pesticides has established the
Pesticide Effects on Insect Pollinator (PEIP) Expert Group that has developed a series of
activities 2 (http://www.oecd.org/dataoecd/19/27/45275778.pdf) on pollinator testing, research,
2
OECD 2010. Environmental Directorate Joint Meeting on the Chemicals Committee and the Working Party on Chemicals,
Pesticides and Biotechnology (ENV/JM/MONO(2010)24 Series on Pesticides No. 52 OECD Survey on Pollinator Testing,
Research, Mitigation and Information Management: Survey Results http://www.oecd.org/dataoecd/19/27/45275778.pdf.
A-2
mitigation, and information management related to insect pollinator declines. The PEIP is
currently working on four activities: (i) establishing means for efficient communication of
pollinator incidents among regulatory authorities; (ii) developing pollinator testing requirements;
(iii) sharing information aimed to mitigate potential risk of pesticides to pollinators; and (iv)
developing a pollinator research clearinghouse. As a first step, questionnaires related to these
topics were distributed to OECD member countries. Responses to these questionnaires will be
used to develop tools to facilitate timely sharing and understanding of available information.
PROJECT CONTACTS
Tom Steeger (Steeger.Thomas@epa.gov)
Tom Moriarty (Moriarty.Thomas@epamail.epa.gov)
Goal 1: Determine the extent of CCD in the United States.
1. Definition of CCD: Refine CCD symptomology to determine what CCD is and what it is
not.
and
2. Develop and conduct an expanded, systematic, nationwide, epidemiological survey, based on
existing models.
Accomplishments
U.S. Bee Loss Survey. ARS, in collaboration with the Apiary Inspectors of America, conducted
a nationwide bee loss survey for the fourth consecutive year. Participation this year was at an
all-time high, in part due to survey availability online. Results indicated a trend similar to
previous years with this past fall-winter losses at 34.4 percent, consistent with the 33 percent
average loss rate of past surveys. CCD-like symptoms continued to be identified by beekeepers
as being observed in some colony losses, with 80 percent of commercial beekeepers reporting
these symptoms. U.S. beekeepers continue to have elevated colony losses that include CCD in
the fall and winter, which does not include the loss of colonies in the spring and summer; over
time, these losses are a major economic drain on beekeepers.
PROJECT CONTACTS
Dennis vanEngelsdorp (dennis.vanengelsdorp@gmail.com)
Jeff Pettis (jeff.pettis@ars.usda.gov)
Improved Field Collection and Shipping Methods for Bee Diagnoses. A novel shipping
method for live worker bees was developed and proven in field and laboratory analyses. This
method improves on prior strategies in cost to shippers (often beekeepers) and in the ability to
deliver material suitable for RNA analysis. It is now the method of choice for forensic analyses,
including for the USDA-APHIS and USDA-ARS National Bee Survey.
A-3
PROJECT CONTACTS
Dennis vanEngelsdorp (dennis.vanengelsdorp@gmail.com
Judy Chen (judy.chen@ars.usda.gov)
Jay Evans (jay.evans@ars.usda.gov)
Tool Development for Tracking and Understanding CCD. BRL scientists improved current
methods to (1) collect field samples of honey bee populations and ship them for genetic analyses,
(2) stabilize and extract RNA, (3) conduct high-throughput genetic screens for viruses and other
pests, (4) collect embryos from established colonies, and
(5) carry out controlled experiments on adult bees using sterile cups. These methods are being
used in national surveys in the United States in order to establish cell lines and other genetic
techniques, and in attempts to combine possible causes of CCD (pathogens and pesticides) in an
attempt to determine interactive effects.
PROJECT CONTACTS
Goal 2: Determine current status of honey bee colony production and health.
1. Develop a long-term annual APHIS survey on the overall health status of U.S. honey bees.
Accomplishment
USDA-APHIS Bee Pest Survey: APHIS, in collaboration with ARS and 13 States, completed a
limited pest and disease survey to look for exotic pests. The survey showed that no exotic
Tropilaelaps mites, Slow Paralysis Virus, or Apis ceranae bees were detected in the 349 samples
representing 2,700 colonies across the United States. Nosema ceranae was the only species of
Nosema detected, and no tracheal mites were detected, although they have been common in the
United States in past years. The survey results are available online at the APHIS Bee Health site.
The national survey expanded to include 34 States this year.
PROJECT CONTACTS
Robyn Rose (robyn.rose@aphis.usda.gov)
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Goal 1: Identify and characterize pathogens associated with CCD.
1. Analyze samples using
High-throughput sequencing for pathogen detection in individual colonies.
Microarray analysis and quantitative gene expression studies to determine stressor or
pathogen effects on bee gene expression.
Integrated Virus Detection System (IVDS) for identifying pathogens by particle size.
and
2. Isolate, purify, and quantify microbes associated with CCD.
Accomplishments
New Viruses Discovered in Large Migratory Bee Operation. Scientists at the University of
CalifornianSan Francisco conducted a study of a large-scale migratory beekeeping operation
that transported bees from South Dakota to Mississippi and California in 2010. Using
comprehensive molecular detection methods, including a custom microarray, quantitative
polymerase chain reaction (qPCR), and ultra-deep sequencing, the researchers uncovered the
seasonal incidence and abundance of several viruses, the microsporidian Nosema sp., Crithidia
mellificae, and several bacteria that are well-known bee pathogens. In addition, they discovered
four novel RNA viruses, two of which were the most abundantly observed components of honey
bee pathogens. One virus, the newly named Lake Sinai virus strain 2 (LSV2), predominated.
Funding: Project Apis m., Howard Hughes Medical Institute, Genentech Graduate Student
Fellowship, A.P. Giannini Foundation Medical Research Fellowship, and
UC-Daviss Hagen-Dazs Postdoctoral Fellowship in Honey Bee Biology.
PROJECT CONTACT
Joe Derisi (joe@derisilab.ucsf.edu)
Presence of Chronic Bee Paralysis Virus in the United States. Chronic bee paralysis virus
(CBPV) is a disease agent that causes characteristic paralysis symptoms in adult honey bees
and could lead to host and colony mortality. Using developed molecular diagnostic tools, ARS
scientists presented the first evidence of CBPV infection in honey bees in the United States. The
study yielded important information on the incidence of CBPV infection in the U.S. population
of adult honey bees and demonstrated the phylogenetic relationships of U.S. strains of CBPV
with isolates of CBPV from the different geographical regions of the world, thereby increasing
our understanding of virus diversity in the United States.
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PROJECT CONTACTS
Bumble Bees and Israeli Acute Paralysis Virus (IAPV) and Deformed Wing Virus (DWV)
Studied. Researchers found that IAPV infects bumble bees and reduces colony life span.
Bumble bees dying from IAPV infections returned to the colony to die inside the hive, unlike
honey bees, which died outside the hive. Bumble bees, however, also exhibited the same
paralytic-like seizures as observed in honey bees.
Funding: USDA-NIFA.
PROJECT CONTACTS
Anne Averill (aaverill@ent.umass.edu)
Lee Solter (lsolter@illinois.edu)
Frank Drummond (frank.drummond@umit.maine.edu)
A New Bee Fungus Found in Association with Solitary Bees. A new fungus that is closely
related to the fungal pathogen that causes chalkbrood (Ascosphaera apis) was found in the pollen
stores and nesting materials of alfalfa leafcutting bees, M. rotundata, in Canada and the western
United States. The new fungus was named A. subglobosa. This new species, closely related to
A. atra and A. duoformis, is distinct from other Ascosphaera species by its evanescent spore
balls, globose to subglobose spores, and unique nuclear ribosomal DNA ITS sequence.
Discoveries such as this non-pathogenic Ascosphaera are assisting in elucidating the evolution of
microbes to the pathogenic state, and could help us better understand the sudden arrival of new
bee pathogens.
Funding: USDA-ARS and University of Copenhagen.
PROJECT CONTACT
Rosalind James (rosalind.james@ars.usda.gov)
Characterizing Chalkbrood Strains in Honey Bees. The pathogenic fungus A. apis, which
causes chalkbrood disease, is ubiquitous in honey bee populations. The draft genome assembly
of this pathogen was used to search for DNA markers adequate to identify different strains and
populations of this pathogen. DNA primers were designed for five different markers and tested
against a panel of closely related fungal species. These markers were compared for 12 distinct
isolates of the pathogen. Use of three of the most variable markers had the same detection power
as use of all five markers.
PROJECT CONTACT
A-6
Non-Apis Bee Pathogens Identified and Characterized. University scientists have been
studying several parasites associated with bumble bees (i.e., Crithidia bombi; a protozoan
parasite of bumble bees), Nosema bombi, and the tracheal mite in order to determine their
transmission patterns, occurrence and distribution, and origin. Although the protozoan was
found in commercial bumble bees, it does not seem to be transmitted from wild bumble bees to
managed honey bees in the area of Massachusetts investigated. Results from these studies will
assist in understanding and ultimately controlling bee parasites.
Funding: USDA-NIFA.
PROJECT CONTACTS
Anne Averill (aaverill@ent.umass.edu)
Goal 2: Identify and characterize pests associated with CCD.
1. Use standard sampling methods to analyze samples for tracheal and Varroa mites and
Nosema species.
Accomplishment
Interactions between Pests, Pathogens, and Pesticides Being Investigated. With funding
from the NIFA Coordinated Agricultural Project, scientists are examining the potential
interactive effects of pests, pathogens, and pesticides in seven States across the United States.
After the first 2-year trial, preliminary results indicate that surrounding landscape, pesticide
exposure, parasites, and diseases were significant factors in explaining overall colony losses, and
not losses due to CCD alone. As the percentage of intensive agriculture in the landscape
surrounding an apiary site increased, it was found that colony losses in the spring also increased.
This might be due to decreased flower resources, but it also could be related to increased
pesticide exposure. Additional research is needed to resolve this uncertainty. It was observed
that as pesticide-contaminated pollen brought back to the hive increased, the queen replacement
due to supercedure also increased, suggesting a potential mechanism for overall colony losses.
However, the laboratory also found that colony losses during the spring and summer buildup
season were due to the parasitic Varroa mite, Nosema disease, and IAPV. Overwintering colony
losses were found to be a function of Varroa levels and IAPV in colonies. Although further
studies are needed to make firm conclusions, these results suggest that CCD might be a
combination of Varroa, Nosema, and viral disease. In addition, these results corroborate the
findings of previously published genomic and proteomic analyses suggesting Varroa and viral
associations for CCD. The relationship between pesticide exposure to bees and queen
supercedure suggests that pesticides also could play a role in weakening colonies that ultimately
might lead to losses.
Funding: USDA-NIFA.
A-7
PROJECT CONTACTS
Nancy Ostiguy (nxo3@psu.edu)
Katherine Aronstein (kate.aronstein@ars.usda.gov)
Steve Sheppard (shepp@wsu.edu)
Kirk Visscher (visscher@ucr.edu)
Marla Spivak (spiva001@umn.edu)
Jamie Ellis (jdellis@ufl.edu)
John Adamczyk (john.adamczyk@ars.usda.gov)
Steve Cook (steve.cook@ars.usda.gov)
Goal 3: Identify pesticides or environmental contaminants associated with CCD.
1. Examine wax, pollen, honey, and adult bee samples for pesticides and environmental
contaminants.
Accomplishments
Collecting and Assessing Pesticide-Related Bee Kill Incidents. In its role in regulating
pesticides, EPA requires data to document the potential effects of pesticides on honey bees at the
level of the individual organism and at the colony level, depending on the outcome of lower tier
tests and other scientifically relevant information. EPA also collects and assesses data on
ecological (bee kill) incidents associated with the use of pesticides. Incidents are typically
reported to State Lead Agencies (SLAs; consisting primarily of State departments of agriculture)
within each of the 50 States, where formal investigations are conducted to determine whether
specific pesticides may have been associated with the incidents. Incident reports may also be
reported to pesticide registrants who may also conduct investigations. Only the pesticide
registrants are required by law to report incidents to EPA; States that investigate incident reports
may or may not relay the results of those investigations to EPA. Incident reports received
through this process are recorded in a database (i.e., the Ecological Incident Information System
[EIIS]) maintained by OPP.
In addition to this formal process for reporting and investigating incidents, incidents may also be
reported by the public through the National Pesticide Information Center (NPIC) Web site
(http://npic.orst.edu/reportprob.html#env), maintained by Oregon State University under an
assistance agreement with EPA. Bee kill incident reports may also be submitted directly to EPA
via e-mail using the beekill@epa.gov address that is available on EPAs pollinator Web site
(http://www.epa.gov/opp00001/ecosystem/pollinator/science.html) or by contacting the Agency
directly by phone. Incident reports that are not investigated, however, may not contain sufficient
information to support risk assessments that rely on these data as a line of evidence for whether a
chemical can impact non-target species such as honey bees. Detailed information (such as
pesticide use information, residue data, number of bees/colonies lost, time over which the
incident took place, and colony health/management) enables risk assessors to better evaluate
whether a particular pesticide can be reasonably linked to a bee kill incident.
A-8
PROJECT CONTACTS
Pesticide Variability Analyzed in Stationary Hive Study. Scientists supported by NIFAs
Coordinated Agricultural Project analyzed pesticide residues in stationary bee hives and
identified a variety of different chemicals and their metabolites in hives. During the past 2 years
(20092010), these researchers have been monitoring pesticides in pollen collected by foraging
honey bees at the apiaries set up for the stationary hive survey in both rural and urban
environments. The amount of pesticides observed varies with time and location. On average,
each sample has had residues of four pesticides. A total of 45 different pesticide compounds or
metabolites have been observed during the past 2 years including insecticides, fungicides, and
herbicides.
Funding: USDA-NIFA.
PROJECT CONTACTS
Brian Eitzer (Brian.Eitzer@ct.gov)
Steve Cook (steve.cook@ars.usda.gov)
Kirk Visscher (visscher@ucr.edu)
Pesticide Exposure to Bees Documented in 1100 Samples Across the United States.
Scientists from Pennsylvania State University and ARS continue to document both unintentional
and intentional exposure of honey bees to pesticide residues in hive products, especially
beebread and beeswax. Samples were collected from migratory beekeepers in 23 States and one
province in Canada. These samples included bees that were collected during beekill incidents.
Honey bees and possibly other pollinators were exposed to a large number (and often high
levels) of pesticides, as suggested by an average of 6.2 pesticides per pollen sample and up to
31 pesticides in a single sample. More than 1,100 samples of bee products were analyzed to
date, with 130 different pesticides and metabolites detected from North American apiary samples
alone. The frequency and quantity of pesticides detected varied considerably, and most of the
samples were close to the level of quantification for their respective pesticides. Particularly
noteworthy is the fungicide chlorothalonil, which was found in the majority of samples analyzed.
Almost all comb and foundation wax was contaminated with miticides used to control parasitic
mites of honey bees and other pesticides, averaging 8 detections with a high of 39 per sample;
however, again the quantity of pesticides detected varied considerably. Although no single
pesticide was shown to be responsible, the additive and synergistic effects of multiple pesticide
exposures are believed to be contributing factors in declining honey bee health, but further
studies are needed to better support this hypothesis. Potential pesticide interactions with other
stressors including Varroa, IAPV, and Nosema, and its role in CCD require further study. In the
future, researchers will focus on impacts of multiple pesticide residues in bee food via
synergistic interactions that can act at sublethal levels on key pollinator behaviors/physiology
A-9
including memory and learning, and on immune function. Results of these studies were
published (Mullin et al., 2010 PLoS ONE 5: 1-19e9754).
Funding: USDA-NIFA, Pennsylvania State University, and National Honey Board.
PROJECT CONTACTS
Chris Mullin (CAMullin@psu.edu)
James L. Frazier (jff2@psu.edu)
Maryann Frazier (mxt15@psu.edu)
Dennis vanEngelsdorp (Dennis.Vanengelsdorp@gmail.com)
Cost-sharing Program for Pesticide Analysis of Honey Bee Colony Matrices (Honey, Wax,
Pollen, Bees, Brood, etc.). Based on recent evidence of frequent pesticide detections in wax,
pollen, and brood, beekeepers have expressed an interest in having samples from their own
colonies/apiaries tested for pesticides. A fund has been established to assist beekeepers by
paying half of the cost of the pesticide analysis. Analysis is being performed by the USDA AMS
National Science Laboratory in Gastonia, North Carolina, and the information generated from
individual samples becomes part of a large, centralized database maintained at Pennsylvania
State University. At this time, the database is not accessible to the general public.
Funding: Foundation for the Preservation of Honey Bees and Project Apis m. (PAm).
PROJECT CONTACT
Maryann Frazier, Pennsylvania State University (mxt15@psu.edu)
Reduction of Honey Bees Pollinating Nine Crops. In 2009 and 2010, researchers assessed
changes in nine colonies on each of nine field crops by counting foragers exiting colonies during
the pollination period for each crop. Researchers also conducted pesticide analyses on samples
of dead and dying bees around hive entrances, returning foragers, crop flowers, trapped pollen,
and corn flowers located near a cotton crop. Colony levels were significantly reduced in hives
pollinating cotton, corn, and alfalfa, while hives placed in apples, pumpkins, almonds, melons,
blueberries, and wild flowers (for honey production) increased or remained fairly consistent. A
total of 52 pesticide residues was detected in samples collected across the 9 crops. Pesticide
residues were not detected on the target crops (those crops in which the bees were rented for
pollination) but were found in trapped pollen in hives or on dead and dying bees in the vicinity of
the hives. It is difficult to say with certainty where the residues came from, but bees were
possibly visiting other crops or plants treated with the pesticides found in trapped pollen or on
the dead and dying bees. Since honey bees require diverse sources of pollen, the establishment
of flowering, pesticide-free plants near bee-pollinated crops could help mitigate exposure to
pesticides.
Funding: National Honey Board and USDA-NIFA.
A-10
PROJECT CONTACTS
Chris Mullin (CAMullin@psu.edu)
James L. Frazier (jff2@psu.edu)
Movement of Imidacloprid in Trees Explored. APHIS has used soil and trunk injection of
imidacloprid to treat hardwood trees in controlling the invasive Asian long- horned beetle. There
is the potential for movement of the pesticide into pollen and nectar of treated trees. APHIS is
collaborating with ARS to monitor the movement of imidacloprid into pollen and nectar and to
evaluate the potential effects on honey bees and other non-target species over a 3-year period.
Low levels of imidacloprid were found in flowers and pollen during the initial 3 years of this
study. There were greater amounts of imidacloprid found in pollen from soil-injected than trunkinjected trees, and male flowers had higher amounts than female flowers. However, little of the
imadicloprid found in flowers was from pollen, and no metabolites of imidacloprid were found
in pollen. Although there were instances where sublethal levels of imidacloprid to honey bees
were found in pollen from treated trees, this pollen is probably diluted and mixed with other
pollen in the hive, thus reducing potential exposure to sublethal doses.
This study has been extended for 3 years to further monitor for and quantify imidacloprid residue
levels in flowers, pollen, nectar, and leaves; determine the impact of residues on honey bee
health; and compare results of soil- and trunk-injected trees.
Funding: USDA-APHIS and USDA-ARS.
PROJECT CONTACTS
Robyn Rose (Robyn.I.Rose@aphis.usda.gov)
Ongoing Research
Stationary Apiary Health Parameters Comparisons. In the NIFA Coordinated Agricultural
Project (CAP), scientists assessed the presence and quantity of tracheal and Varroa mites,
viruses, Nosema in bees and pesticides in wax, as well as quantity of pollen, queen health
parameters, and brood and adult bee populations, evaluating possible linkages between
pest/pathogen/pesticide presence and colony survivorship. Data show high variability among
virus presence, and evaluations continue to identify possible linkages. There was also a high
variability in the pesticide load in the pollen brought back to the hives.
Funding: USDA-NIFA.
PROJECT CONTACTS
Brian Eitzer (Brian.Eitzer@ct.gov)
A-11
Goal 4: Determine bee physiological response to toxins, pesticides, or pathogens and develop
analytical tools to assess bee health.
1. Compare genes expressed in response to specific pathogens or pesticides with those
expressed in bees from CCD colonies,
and
2. Develop the use of molecular markers to determine the physiological status of bees and as
indicators of bee health.
Accomplishments
Residue Analysis Yields Clues to Potential Fate of Pesticides. EPA OPPs Analytical
Chemistry Laboratory in Fort Meade, Maryland, provides residue analysis of neonicotinoid
pesticides in honey bee colonies in support of research being conducted by USDA in conjunction
with the University of Maryland. These studies are informing EPAs understanding of the
potential exposure of honey bees to pesticide (neonicotinoid) residues in pollen and nectar. In
addition, these studies have provided information on the potential effects of imidacloprid on
honey bee colonies following prolonged exposure to the compound in diets (pesticide-spiked bee
bread). In support of pesticide residue analyses, EPAs Analytical Chemistry Laboratory has
refined analytical techniques used for measuring residues of imidacloprid and its degradates and
has increased the detection limits for these residues. These new methods have been published in
the open literature.
Funding: EPA.
PROJECT CONTACTS
Methods Developed to Detect Virus Replication in Honey Bees. The assessment of virus
effects on bee colony health requires not only the detection of viruses in bees and bee colonies
but also the indication of virus replication in the host. Scientists at the University of
Massachusetts have developed a simple, real-time polymerase chain reaction (PCR) based assay
to detect the most active stage of virus replicationproduction of a material known as negative
strand, replicative intermediateand determined that 5080 percent of the virus-positive bees
had these intermediates. These results indicate that actual virus infection rates were much lower
than previously understood.
Funding: USDA-NIFA.
PROJECT CONTACT
John P. Burand (jburand@microbio.umass.edu)
A-12
Gene-expression Analyses Using Candidate Immune- and Stress-response Genes. Gene

expression analyses with parallel bee gene sets and pathogen genes have revealed changes in the
set of expressed bee genes that could relate to the cause(s) of collapsing colonies, including a
massive shift in the abundances of gene transcripts related to protein translation. These
experiments were complemented by high-throughput sequencing of millions of honey bee RNAs
for bees challenged by the American foulbrood bacterium (Paenibacillus larvae) and bees from
CCD and control colonies.
Funding: USDA-ARS.
PROJECT CONTACTS
Scott Cornmann (scott.cornmann@ars.usda.gov)
Genes Associated with Nosema Infection Determined by Microarrays. In 2010, we verified
the status of bees infected with Nosema using DNA and microarray approaches. Microarray
analyses revealed that Nosema infection alters host metabolic pathways regulating nutrition and
behavioral maturation as expected, but Nosema infection surprisingly does not appear to
significantly alter immune gene expression in midgut and fat body tissues up to 7 days postinfection. We will continue to examine impacts of infection by characterizing gene expression in
immune-related tissues up to 2 weeks post-infection in bees infected with Nosema. These
studies will identify host response to Nosema infection and may lead to downstream applications
in commercial management.
Funding: USDA-ARS and USDA-NIFA.
PROJECT CONTACTS
Christina Grozinger (cmgrozinger@psu.edu)
Diagnostic Tools Developed for High-Throughput Detection and Monitoring of Honey Bee
Diseases. ARS scientists developed a new diagnostic tool for detection of Nosema infection in
field honey bee samples. This highly specific, sensitive test, based on an antigen capture assay
that detects Nosema spore wall protein, is capable of detecting Nosema antibodies. Researchers
are pursuing leads to transfer this technology to private industry. These findings have been
accepted for publication in the Journal of Apicultural Research.
Following the development of a reliable field diagnostic tool, ARS scientists are now using the
same antibody-based approach to develop a high-throughput laboratory test (enzyme-linked
immunosorbent assay; ELISA) for Nosema detection in bees. In response to increased incidence
of fungal diseases in bee colonies, ARS scientists developed a simple DNA-based method for
detection of chalkbrood fungal disease in bee brood. This test will allow detection of the fungus
prior to clinical signs of the disease. Although chalkbrood disease is usually not a primary
concern for the beekeepers, it has recently become more prevalent. Research indicates that high
levels of stress as a result of intense management of the environment may affect bee immune
responses, making them more vulnerable to what were once considered benign diseases.
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PROJECT CONTACTS
A-14
Topic III: Research to Identify Factors Affecting Honey Bee Health, Including Attempts to
Recreate CCD Symptomology
Goal 1: Confirm or eliminate potential environmental stressors as contributing causes of
CCD.
1. Test effects (lethal and sublethal) of neonicotinoids and other pesticides used for crop
protection.
Various research results indicate the presence of a range of pesticides and their degradates in
honey bee colonies; however, no research or survey information has linked the incidence of CCD
to pesticides. This is consistent with the multi-factorial hypothesis being pursued by the CCD
Steering Committee. To the extent that pesticides are demonstrated to be directly impacting
honey bee survival, growth and/or reproduction, EPA is prepared to mitigate these effects to the
extent possible under the law.
As discussed earlier, EPA is also working with its international partners through OECD to
identify high-quality research on the potential effects of pesticides on pollinator health,
particularly as it relates to CCD.
EPA is continuing its efforts to collaborate with researchers in both government and nongovernment institutions regarding the data that can potentially inform EPAs regulatory decisionmaking. EPA scientists have also served as ad hoc reviewers of research proposals related to the
potential effects of pesticides on insect pollinators submitted to USDA for funding.
PROJECT CONTACTS
Accomplishments
Lethal and Sublethal Effects of Insecticides on Non-Apis Bees Elucidated. Using totally
enclosed field cage systems, University of Massachusetts scientists assessed the impact of
imidacloprid in flowering low bush blueberry on commercial bumble bees (Bombus impatiens).
After bloom ended, the bees were released to forage on surrounding plants for the remainder of
the spring and summer. Results suggest that imidacloprid reduced brood (immature bees) at the
end of bloom but did not seem to affect the survival of adult workers.
Funding: USDA-NIFA.
PROJECT CONTACT
Persistence of the Effect of the Insecticide Novaluron on Bee Reproduction. In a study on
alfalfa leafcutting bees in field cages, an ARS scientist evaluated the persistence of toxicity of
the insecticide novaluron. The effect of female bee exposure to novaluron-treated alfalfa was
found to persist for at least 2 weeks post-spray; the effect was not adult mortality, but instead,
A-15
mortality in the eggs laid by exposed adult females. Egg mortality was higher in cages with
treated alfalfa compared to cages with untreated alfalfa. The effect diminished over time but
remained higher than control mortality throughout the study.
PROJECT CONTACTS
Theresa Pitts-Singer (theresa.pitts singer@ars.usda.gov)
James Barbour (jbarbour@uidaho.edu)
Synergistic and Sublethal Impacts of Pesticides Determined on Honey Bee Larvae.
The levels of pesticides detected within the hive have increasingly raised concerns about bee
health and development under chronic exposure to pesticides. Scientists at Pennsylvania State
University have used a modified in vitro larval rearing technique to assess the survival of honey
bee larvae during a 6-day exposure to sublethal doses of four of the most frequently found
pesticides in bee pollen. A Toxicity Probabilistic model was developed to determine relative
toxicity of a single pesticide to honey bee larvae, which estimates pesticide toxicity as a function
of the magnitude of toxicant exposure and a bees sensitivity to a toxicant. Modeling results
demonstrate that honey bee larvae and adults have different sensitivity to pesticides, and
chlorothalonil, a fungicide which is considered non-toxic to bees on an acute exposure basis and
is applied during bloom, has the highest relative toxicity to bee larvae compared to adult bees
among the pesticides tested: fluvalinate, coumaphos, and chlorpyrifos. In addition, a method for
assessing mixture toxicity was developed. Synergistic interactions were found between the
fungicide chlorothalonil and the miticide fluvalinate at concentrations 34 ppm and 3 ppm,
respectively, increasing larval mortality at day 4, approximately 7 times greater than the
expected toxicity for mixtures with only concentration addition effect. However, when
decreasing the concentration for fluvalinate and chlorothalonil by 10 fold, the mixture displayed
antagonistic interaction. Chlorothalonil and coumaphos in mixtures at sublethal doses also
displayed synergistic toxicity 5 times greater than the expected mortality if there is no
interaction. The other binary mixtures, including fluvalinate and coumaphos, fluvalinate and
chlorpyrifos, and coumaphos and chlorpyrifos, showed an additive effect. For three-component
mixtures, only one significant reduction in larval mortality was found when adding coumaphos
into the mixture of fluvalinate and chlorothalonil. Adding 34 ppm chlorothalonil into the threecomponent mixture of fluvalinate, coumaphos, and chlorpyrifos, the four-component mixture
showed an additive effect. Moreover, considering pesticide formulations, the researchers
demonstrated high toxicity of a common inert ingredient N-methylpyrrolidone (NMP) to honey
bee larvae; NMP can kill all the reared larvae during the first day. This study suggests that
fungicides, inert ingredients, and pesticide interactions may have crucial impacts on development
and survival of honey bee larvae. However, it is uncertain as to the extent that formulation inerts
remain with their active ingredients, and additional research is needed to resolve this uncertainty.
Funding: USDA-NIFA.
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PROJECT CONTACTS
James L. Frazier (JFrazier@psu.edu)
Chris Mullin (oy9@psu.edu)
2. Test the effects of current miticides used in hives on worker bee longevity and colony health.
Accomplishments
Interactive and Sublethal Effects of In-hive Miticides Evaluated. Scientists at the University
of NebraskaLincoln have been studying the synergistic effects of various varroacides and
fungicides on honey bee health, testing for lethal and sublethal effects. Research indicated that
combinations of varroacides that are detoxified by the cytochrome P450 system
(e.g., the miticides tau-fluvalinate, coumaphos, and fenproximate) tend to be significantly more
toxic when applied in combination. A similar interaction occurred when bees were exposed
concurrently to a cytochrome P450-inhibiting fungicide and a varroacide that was metabolized
by P450s. Normally these varroacides are well tolerated by honey bees, but pre-treatment with a
P450-inhibiting fungicide greatly increases mortality in bees by a synergistic ratio of nearly
2000 in the most extreme case. While this interaction was found using fungicide doses
substantially higher than would likely occur through consumption of fungicide-contaminated
pollen (Mullin et al., 2010, PLoS ONE 5: e9754), the potency of this interaction raises concerns
about lethal and sublethal effects that may be occurring at field-relevant doses. The results
suggest that honey bees should not be treated with more than one P450-detoxified varroacide
concurrently or sequentially because varroacides are known to accumulate in beeswax. They
also suggest that beekeepers should avoid applying P450-detoxified varroacides when honey
bees are placed in orchards or other crop settings where exposure to P450-inhibiting fungicides is
likely. Additional studies are needed to resolve this uncertainty. These results may be useful for
incorporation into a bee health management plan. Additional studies are needed to determine the
range of bee exposure to fungicides and varroacides in the field and how these concentrations
affect the bees.
Funding: USDA-NIFA.
PROJECT CONTACT
Marion Ellis (mellis3@unl.edu)
Further Studies on Sublethal Effects of In-hive Miticides. Previously, scientists at the
University of NebraskaLincoln documented the harmful synergistic effects of certain varroacide
and fungicide combinations on honey bee health in laboratory studies (Johnson, et al., 2010).
Their results suggest that beekeepers should avoid applying these varroacides in combination.
Beekeepers should also avoid applying these varroacides when honey bees are placed in orchards
or other crop settings where exposure to prochloraz is likely. Studies are underway to assess the
effects of exposure to simultaneously applied field-relevant doses of miticides and fungicides on
brood survival, weight gain, and queen performance.
Funding: USDA-NIFA.
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PROJECT CONTACT
Certain Varroacides Could Actually Lower Bee Susceptibility to CCD.
Pennsylvania State University and ARS researchers conducted a classification and regression
tree (CART) analysis to better understand the relative importance of different risk variables in
explaining CCD (van Engelsdorp et al., 2010). Fifty-five variables, which included various
pathogens, pesticides, and pests, were used to construct the models. Six of the 19 variables
having the greatest discriminatory value were pesticide levels. Notably, coumaphos (a miticide
commonly used by beekeepers) levels in brood had the highest discriminatory value and were
highest in control (healthy) colonies. This suggests that higher levels of coumaphos could help
colonies fight off CCD. This result must be interpreted with caution, however, because Varroa
mite levels were similar in both CCD and non-CCD (control colonies). Follow-up studies are
necessary to quantify Varroa infestations at different time intervals to give more conclusive
results.
Funding: National Honey Board; USDA-ARS; North Carolina Agriculture Foundation; North
Carolina Department of Agriculture and Consumer Services; USDA-NIFA; and University of
Liege, Belgium.
PROJECT CONTACTS
Jim Frazier (jff2@psu.edu)
3. Test the effects of antibiotics (especially new ones such as Tylosin) on the increase in
pathogens (e.g., Nosema ceranae) and the overall viability of bees over winter.
See Topic IV, Goal 5.
4. Test effects of supplemental protein and carbohydrate (e.g., high fructose corn syrup
[HFCS]) feedings on bee health.
See Topic IV, Goal 1, Objective 1.
5. Test effects of availability and quality of natural food sources on bee health as affected by
climatic factors (e.g., drought).
and
6. Test effects of management practices (e.g., nutrition and migratory stresses) on bee health.
These objectives are being done as part of the work on migratory beekeeping and the Areawide project. See Topic IV, Goals 1 and 6.
A-18
Goal 2: Confirm or eliminate potential pathogens as contributing causes of CCD.

1. Test pathogenicity of the following CCD-associated microbes against honey bees and nonApis bees:
Viruses
Fungi (chalk brood; stonebrood)
Microsporidia (Nosema)
Bacteria
Trypanosomes and other microbes
Accomplishments
Differential Susceptibility of Bees to IAPV. Honey bee workers of different ages were found
to be differentially susceptible to IAPV infection. Newly emerged adult bees were highly
susceptible to infection by IAPV, with median mortality occurring at 46 hours post emergence.
The susceptibility declines as bees age, with 5- to 6-day-old bees exhibiting 40 percent mortality
at 80 hours. Bees parasitized as pupae (with normal wings) by Varroa are approximately twice
as susceptible to IAPV infections as non-parasitized bees.
Funding: USDA-NIFA.
PROJECT CONTACT
Diana Cox-Foster (dxc12@psu.edu)
Honey Bee Viruses Found in Non-Apis Bees Essential to Alfalfa Seed Industry. A survey of
alfalfa leafcutting bees (ALCB) (Megachile rotundata) and alkali bees (Nomia melanderi) from
Utah and Washington State, and subsequent molecular analysis for seven different RNA viruses,
revealed the presence of deformed wing virus (DWV), Israeli acute paralysis virus (IAPV), black
queen cell virus (BQCV), and sac brood virus (SBV). Further, when IAPV was fed to virus-free
ALCB larvae, the viral infection disrupted adult diapause, with IAPV-infected bees having a
significantly greater percentage emerging as second-generation adults as compared to the control
treatment. IAPV infection also significantly reduced the ALCB adult survivorship in both males
and females when acquired in newly emerged adults. IAPV was confirmed to be replicating in
both the adult and larval stages, and the infection was confined to the gut in larvae.
Funding: USDA-ARS, USDA-NIFA, and Pennsylvania Department of Agriculture.
PROJECT CONTACTS
Diana Cox Foster (dxc12@psu.edu)
A-19
Goal 3: Confirm or eliminate pests as contributing causes of CCD.

1. Test the effects of Varroa mites on bee health and robustness, particularly overwintering
effects and association with CCD in early spring.
See Topic III, Goal 4.
2. Determine the importance of Varroa as a vector of viruses associated with CCD or as a
general immunosuppressive agent on the colony itself.
Accomplishment
Varroa Mites and Virus (IAPV) Transmission. IAPV was identified to be strongly associated
with CCD and is considered to be a significant marker for CCD. Because mites feed and move
between adult bees and brood, they have the potential to act as a vector to transmit pathogens
from infected bees to healthy bees and have been reported to be associated with viral disease
outbreaks in the field. Research results demonstrated that Varroa mite is a biological vector of
the virus by supporting replication of IAPV and transmitting IAPV among honey bees. The
results also showed that the mite-virus association could possibly reduce host immunity and
therefore promote elevated levels of virus replication. This study sheds light on the
epidemiology of IAPV infection in honey bees and adds additional importance to the control of
Varroa mites.
PROJECT CONTACTS
Also see Topic III, Goal 4.
Goal 4: Determine what factors (or interactions between factors) are most important in their
contribution to CCD. This includes environmental factors
(e.g., temperature, humidity, and chemical exposure), pathogens and parasites, and bee
genetics and breeding.
Accomplishments
Synergism Found Between Pesticides on Honey Bee Homing Behavior. Researchers at
Michigan State University determined that the distance of bee search flights and the length of
time homing memories are retained by bees. An assay was developed to determine the effects of
pesticides on the memories of foraging bees. In this study, bees were first released 0.8 km from
the hive, and the bees returning to the hive were counted (homing rate). Those bees that were
released the first time were recaptured and re-released 1.8 km away from the hive. Bees returned
home equally well from the first release site (0.8 km). However, when the returning bees were
re-released 1.8 km away from the hive, bees that were treated with a combination of fluvalinate
and imidacloprid showed a significant reduction in their homing rate. Further, their homing rate
was not affected when either pesticide was used alone. These results suggest that these two
A-20
pesticides have a synergistic effect on honey bee learning and/or memory. These results shed
light on a possible effect of CCD on bees, because foragers are having trouble finding their way
home.
Funding: Michigan State University, Australia National University, and USDA-NIFA.
PROJECT CONTACT
Zachary Huang (bees@msu.edu)
Synergistic Effects of Pesticide Exposure on Pathogen Growth and Bee Health Discovered.
There has been significant concern about possible interactive effects of various pesticides and
pathogens on bees. When bees were exposed to the gut parasite Nosema and the insecticide
imidacloprid, researchers found evidence of an interactive effect on honey bee health. Worker
bees exhibited up to a fourfold increase in Nosema levels when they originated from colonies
that had been fed imidacloprid, indicating a subtle sublethal interaction between pesticides and
pathogens. The same fourfold increase was exhibited in bees exposed to 2.5 ppb or 20 ppb
imidacloprid. Also, while the individual bees contained higher spore loads, the colonies from
which they were derived did not exhibit elevated Nosema loads. This research has been
submitted for publication, and similar findings have recently been published from a study in
France in Environmental Microbiology 2009.
Funding: USDA-ARS and North American Pollinator Protection Campaign (NAPPC).
PROJECT CONTACTS
Galen Dively (Galen@umd.edu)
Interactions Among the Microsporidia Nosema apis and Nosema ceranae, the Viruses
IAPV, DWV, BQCV, and Rearing Temperature. Development, virulence, infectivity (IC50),
spore production, temperature effects, and direct competition in the same host were evaluated for
N. ceranae and N. apis. No significant difference in virulence between the two species was
detected, but IC50 studies demonstrated that a 5x higher dosage of N. ceranae is needed for
infection. Host mortality at different temperatures was not significantly different for the two
pathogens. N. ceranae produced slightly more spores than N. apis over the infection period
when 200 the infective dosage was fed. When individual bees were inoculated with both
Nosema species to produce mixed infections, N. apis produced more spores. When viruses
(DWV, IAPV, and BQCV) were combined with microsporidia at different temperatures,
mortality trended higher but was not significantly different from mortality due to the
microsporidia alone. There was no difference in spore production by N. apis and N. ceranae
when mixed with viruses. Mortality of virus and Nosema combinations was highest at low and
high rearing temperatures, no matter the combination (and including controls), so rearing
temperature was the mortality factor, not mixes of virus and Nosema.
Funding: USDA-NIFA and USDA-ARS.
A-21
PROJECT CONTACTS
Association of Miticides With Adult Bee Susceptibility to Nosema. A significant relationship
between pesticide residue exposure (in brood comb) and adult susceptibility to infection with
Nosema ceranae was detected in a common hive environment study in 2010. The three most
frequently observed pesticides were miticides used to control Varroa mite in brood comb. That
is, adult honey bees that were reared in high pesticide residue comb (taken from existing
commercial beekeeping operations) were significantly more likely to become infected with
Nosema ceranae than those reared in low residue comb, suggesting a detrimental sublethal effect
of pesticide exposure on the immune system. These findings were reported at several beekeeper
local, regional, and national meetings. A manuscript was submitted to the Journal of
Invertebrate Pathology. A follow-up large-scale field study was initiated in 2010 and will be
completed in 2011.
Funding: USDA-NIFA-CAP; the State Beekeeper Associations of Washington, Oregon, Idaho,
and California; and Project Apis m.
PROJECT CONTACT
Interaction Between Pesticides and Bee Viruses Found. Pennsylvania State University
researchers found that consumption of sublethal levels of certain pesticides elevates viral titers in
infected bees and appears to alter the immune responses of the bees. In cage studies, nurse or
house bees were fed sugar solutions containing pesticides (myclobutanil, acetamiprid,
fluvalinate, or chlorothalonil) at dosages previously determined to be sublethal. These dosages
approximated lower concentrations found in incoming pollen. The titers of several picorna-like
viruses (deformed wing virus, black queen cell virus, and IAPV) were found to be elevated by
one or several of the pesticides. The expression of several immune-related genes was altered by
the pesticide exposure as compared to untreated bees that were also immune challenged. The
identity of the viruses was confirmed via genome sequencing.
Funding: Pennsylvania Department of Agriculture.
PROJECT CONTACT
Diana Cox-Foster (dxc12@psu.edu)
A-22
Interactions of Israeli Acute Paralysis Virus (IAPV) and Deformed Wing Virus (DWV) on
Honey Bee Health Examined. In a Cooperative Agricultural Project between ARS and the
University of Illinois, scientists examined the interactions among IAPV, DWV, pesticides, and
Nosema. Results showed that IAPV-infected bees exhibited 90100 percent early
(35 days post-infection) mortality rates and paralytic-like seizures before death. Behavioral
changes included increased brood feedings and release of Nasanov pheromones, which draw
bees back to the hive and are associated with worker recruitment to the hive or food and water
sources. These results implicate the virus as being associated with both mortality and behavioral
changes, which are possible links to CCD. The behavioral changes, in particular, deserve further
investigation since CCD might be a consequence of such changes.
Studies also showed that bees exposed to neonicotinoid insecticides and fungicides at sublethal
levels had impaired immune systems and increased levels of the viruses noted above. Because
CCD might be a result of such interactions and damaged bee immunity, further studies are
planned to examine immune responses and determine the mechanisms underlying these
interactions.
Research is also characterizing levels of Nosema ceranae and Nosema apis to determine possible
interactions and synergies with the viruses above.
PROJECT CONTACTS
Effect of Varroa Mites and Varroa-Transmitted Viruses on Nutritional and Health Status
of Honey Bees. The main goal of this study (20102011) is to understand how mite infestation
and mite-transmitted diseases affect immune competence and the nutritional status of managed
honey bees. Preliminary results demonstrated that Varroa infestation has a major impact on the
performance of individual honey bee health as well as on colony-level effects, including
significant losses in weight in pupae and newly emerged adults infested with mites. Importantly,
Varroa infestation affected the nutritional status of bees. The amount of available sugar,
especially glucose, was depressed in Varroa-infested individuals, and this effect was
significantly greater for adult bees than pupae. Interestingly, Varroa-infested bees were able to
maintain their protein content, including protein content per unit weight in newly emerged bees
bearing Varroa relative to controls. Consistent with the small effect of Varroa infestation on bee
protein nutrition, the total free amino acid content did not vary significantly with treatment. The
dominant amino acids in all samples (including all three life stages, and Varroa-infested vs.
un-infested) were serine and proline. Preliminary results indicating that Varroa-infested pupae
have reduced content of the key sulfur amino acid methionine are being investigated further, as
are other metabolites. Additional efforts are focused on monitoring the level of viral infection
and immune responses in Varroa-infested versus control bees using a DNA-based approach.
A-23
PROJECT CONTACTS
Angela E. Douglas (aes326@cornell.edu)
Viral Diseases and Varroa Mites Linked to Colony Losses. Since 2008, ARS scientists in
Weslaco, Texas, have collaborated with university scientists to determine key factors
(e.g., parasites, diseases, and pesticides) contributing to honey bee colony losses in apiaries
across the United States. First-year data from this Coordinated Agricultural Project indicate that
Varroa mite infestation and viral diseases contribute strongly to colony losses.
PROJECT CONTACT
Temperature Found to Affect Honey Bee Susceptibility to Fungi. Stonebrood and chalk
brood are two fungal diseases of honey bees. Stonebrood is caused by a non-specialist fungal
pathogen (Aspergillus flavus) that affects many animals to varying degrees. Chalkbrood is
caused by a highly specialized pathogen of bees (i.e., Ascosphaera apis). When these fungal
pathogens were fed to honey bees, stonebrood appeared to be more virulent than chalkbrood.
However, when recently infected larvae were exposed to a 24 h cooling period (a cold stress),
mortality from chalkbrood increased, whereas bees tended to recover from stonebrood. These
results raise interesting questions about temperature stress and honey bee immune responses to
pathogens with different degrees of specialization.
PROJECT CONTACTS
Svjeltlana Vojvodic (svo@life.ku.dk)
Temperature Stress Found to Increase Immune Response in Bees. Both high and low
temperatures increased the expression of immune response genes in the alfalfa leafcutting bee.
Genes associated with pathogen recognition and trypsin-like serine proteases were most highly
expressed at the lowest rearing temperature (20C), while prophenoloxidase, melanization,
immune response signalling pathways, effectors, and reactive oxygen species were most highly
expressed at the warmest temperature (35C). The chalkbrood pathogen was found to affect
some non-immunity host functions, particularly protein synthesis, differently at different
temperatures, with the lowest rates of protein synthesis occurring at 30C, a temperature where
protein synthesis is high in healthy insects. If a temperature stress occurs before the pathogen
has infected, it appears to elicit an immune response in the host, and this early response can
prevent infection from occurring.
Funding: USDA-ARS.
A-24
PROJECT CONTACTS
Johan Hu (junhuan.xu@usu.edu)
Ongoing Research
Varroa Mite and Nosema Species Being Sequenced. ARS scientists in Beltsville, Maryland,
have finished sequencing, annotating, and publishing the Nosema ceranae genome and have
sequenced Nosema apis. Also, with industry support, ARS initiated a genome project on Varroa
destructor, the primary honey bee parasite, as part of a worldwide consortium. Further analysis
of these results will allow researchers to identify genes implicated in virulence, viral disease, and
chemical resistance and to develop new strategies to control their impact on bees.
PROJECT CONTACTS
A-25
Topic IV: Mitigation and Management Preventive Measures

Goal 1: Develop best management practices for honey bees.
1. Develop best management practices for migratory beekeeping.
Accomplishments
Best Management Practices (BMPs) Published. USDA-NIFAs Coordinated Agricultural
Project (CAP) has published a Best Management Practices Guide for Honey Bee Health in the
American Bee Journal and Bee Culture, which are two trade publications read by most
beekeepers. The BMP guide is also available on the CAP projects extension Web site,
http://www.extension.org/pages/33379/best-management-practices-bmps-for-beekeeperspollinating-californias-agricultural-crops. The BMP publication is the result of a collaborative
effort involving CAP-funded scientists and Project Apis m., a beekeeper and almond grower
foundation. For more information on the eXtension site, see Goal 7.
Funding: USDA-NIFA and Project Apis m.
PROJECT CONTACTS
John Skinner (jskinner@utk.edu)
Keith Delaplane (ksd@uga.edu)
Brood Pheromone Shown to Improve Colony Strength. ARS scientists in Weslaco, Texas,
are testing a new brood pheromone device in honey bee colonies to improve the health of honey
bees, as well as to improve crop pollination. In a cooperative agreement with Contech, Inc.
(formerly PheroTech International Inc.), ARS carried out field trials showing that treated
colonies experienced increases in pollen collection and population.
Funding: USDA-ARS and Contech, Inc.
PROJECT CONTACT
Effects of Supplemental Protein Feeding on Colony Growth Assessed. Cranberry pollination
is extremely stressful to honey bees, providing minimal nutrition for the amount of work
performed. ARS scientists studied whether supplemental feeding with the MegaBee protein
supplement during cranberry pollination could reduce colony losses and improve colony
population growth. Results showed that colonies fed the protein supplement grew more than
those that were not fed, indicating that even a relatively small addition of supplemental protein to
colonies during cranberry pollination improves their growth and survival.
A-26
PROJECT CONTACTS
Gloria DeGrandi-Hoffman (Gloria.Hoffman@ars.usda.gov)
Gordon Wardell (GordyAW@aol.com)
Effects of Protein Supplements on Worker Physiology and Immune Response Examined.
To evaluate the potential benefits of nutritional supplements on bee health, ARS scientists
compared protein levels, endocrine development, and immune response in adult worker bees fed
protein, pollen, and high fructose corn syrup supplements. Results showed that protein and
pollen supplements produced similarly positive effects, but bees fed high fructose corn syrup had
significantly reduced immune responses. This study will help beekeepers improve management
strategies for their bees.
Funding: USDA-ARS.
PROJECT CONTACTS
Winter Feeding and Its Improvement of Colony Size and Survival. This work started in the
fall of 2006 and has continued to date. The Weslaco laboratory has shown that colonies being
prepared for almond pollination in California show dramatic improvement when fed
continuously from September through late January. Cooperating beekeepers and others have
stated that they consider this work to have caused a total change in how they manage their
colonies for almond pollination. Projects completed include interaction of feeding and Nosema
infection; interaction of feeding and Varroa parasitism; optimum time of feeding; evaluation of
commercially available pollen substitutes/supplements; interaction of nutrition, Nosema, and
Varroa; and mountainside wintering (cool, windy conditions reduce winter flight and the need
for food); and the food efficiency (bees per pound of diet consumed) of four strains of bees.
During feeding trials, some unanticipated findings came to light: a) colonies that went queenless did not attempt supercedure or emergency queen cell construction (the duration of queen
survival was correlated with the level of Varroa parasitism and to a lesser degree, the level of
Nosema infection); b) colonies whose Varroa levels were above 150 mites (natural mite drop
onto a sticky board during 3 days) in October had few colonies achieve almond pollination grade
regardless of mite treatment or feeding in the fall-winter; c) treating colonies with fumagillin
appears to have a short (about 2 months) negative impact on colonies. However, untreated
infected colonies showed extremely poor performance after 14 months. This highlights the need
to control even fairly moderate infections (500,000 spores/bee) of N. ceranae in some areas.
Funding: USDA-ARS.
PROJECT CONTACTS
Frank Eischen (frank.eischen@ars.usda.gov)
A-27
Honey Compound Could Enhance Bee Tolerance to Pesticide. Honey was found to contain a
compound called pinocembrin, which is likely derived from propolis, and which acts as a
powerful inducer of the enzymes that metabolize tau-fluvalinate. These results suggest that bee
consumption of honey may serve a hitherto unrecognized role in honey bee health in the context
of pesticide tolerance.
PROJECT CONTACT
May R. Berenbaum (maybe@illinois.edu)
Plant Resin Identified to Improve Bee Resistance to Fungal Toxins. Honey bees and their
resource-rich nests are hosts to a wide range of fungi, including species that produce toxic
substances called mycotoxins, which workers detoxify using gut enzymes. In bioassay
experiments, bees that consumed extracts of propolis, a complex mixture of plant resins collected
by bees and used as a general caulking material in the hive, had an enhanced capacity to detoxify
mycotoxins. These results suggest that the enzymes involved in mycotoxin detoxification are
enhanced by ingestion of propolis, which may serve a role in honey bee health.
PROJECT CONTACT
May R. Berenbaum (maybe@illinois.edu)
Malnutrition, Beneficial Microbes, and Nutritional Needs of Honey Bees. Scientists at ARS
in Tucson, Arizona, believe that malnutrition is a major cause of colony losses. However,
malnutrition, especially in its early stages, is difficult to diagnose. To remedy this, these ARS
scientists are identifying biomarkers associated with the nutritional state of the bees.
Researchers found that bees emitted volatile compounds when adult workers and larval bees
were malnourished. Emissions of these compounds increase in bees experiencing acute
malnutrition. Identifying these chemical cues will enable ARS to evaluate how contemporary
beekeeping and pollination practice, as well as environmental contamination, affects the
nutritional state of a colony and its vulnerability to disease and decline.
Researchers at ARS in Tucson have uncovered key bacterial communities needed by bees for
food processing and digestion. When scientists fed colonies pollen contaminated with
fungicides, less than 30 percent reared new queens, suggesting that key nutrients needed to raise
queens might be missing. Colonies that cannot successfully replace their queens cannot survive
and thus contribute to the colony losses experienced by U.S. beekeepers.
Supplemental feeding can have deleterious effects on colonies if used for prolonged periods.
ARS researchers showed that colonies fed supplemental protein produced higher numbers of
brood but did not supply them complete nutrition. The lowered protein levels in workers
shortened their lifespan and eventually reduced brood rearing, causing the colony to decline and
the hives to perish. Additional studies found that during the winter, colonies fed sugar syrup
made with sucrose produced more brood in spring compared with colonies fed high fructose corn
syrup. These researchers are advising beekeepers that feeding colonies exclusively on high
fructose corn syrup during winter or floral dearth periods can negatively impact colony strength
required for pollination.
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Funding: USDA-ARS.
PROJECT CONTACT
2. Develop best management practices for pest and pathogen control.
Accomplishments
High Ozone Concentrations Being Developed As a Fumigant for Beehive Equipment. In
2010, a mid-size ozone fumigation chamber was set up and field tested in Florida using honey
bee supers and comb from beekeepers. Ozone fumigant killed 100 percent of the insect pests
(small hive beetles and various wax moths), and pathogen loads were reduced. Pesticide
residues were not effectively eliminated because comb wax protected the chemicals from
degradation. Although the combs smelled unpleasant after treatment, no toxic compounds were
formed, and the bees readily accepted ozone-treated comb in the colony. Treating comb also did
not appear to affect the attractiveness to greater wax moth.
Funding: USDA-ARS, Florida Department of Plant Industries, and USDA-NIFA.
PROJECT CONTACT
Rosalind James (Rosalind.James@ars.usda.gov)
HopGuard, a New Natural Product for Varroa Mite Control. Beekeepers need new
methods to control Varroa because currently registered products are inconsistent in their
effectiveness, harmful to brood, contaminate wax combs used in hives, or no longer control the
mite because it is resistant. Under a Cooperative Research and Development Agreement
(CRADA) with J.I. Haas, Inc., a product was developed (HopGuard) that incorporates the beta
plant acids (BPA) that are byproducts of hops processing for the beer brewing industry.
Prototypes of the product were tested in commercial colonies and in packages of bees used to
start new colonies. HopGuard was highly effective in reducing mite populations. The product
did not harm queens, adult bees, or brood, and it did not contaminate honey or the wax comb. A
Section 18 emergency registration was issued by EPA and HopGuard, and is now in
commercial production.
Funding: CRADA between USDA-ARS and J.I. Haas, Inc.
PROJECT CONTACT
A-29
Controlling the Key Parasite Varroa destructor Through Application of Genomics. A

genome draft sequence was published for the Varroa mite, revealing potential weak points in
mite biology (defensive proteins and proteins used in chemical mitigation) and candidates for
novel controls such as RNA interference (RNAi). In fact, the publication in genomic databases
of mite candidate genes allowed the worldwide initiation of RNAi efforts for this parasite,
ending in late 2010, with the first successful demonstration of RNAi activity in Varroa.
Microbes identified in this screen have also been screened across bees and mites as plausible
controls for Varroa.
Funding: USDA-ARS.
PROJECT CONTACTS
Chemicals Associated With Mite Control Identified. ARS scientists at Gainesville, Florida,
have discovered several chemicals that are produced in large amounts by drone and worker
brood during the cell capping process but not by queen larvae, which affect the searching
behavior of the Varroa mite. ARS has filed a provisional patent on the use of these compounds
for control of the Varroa mite and is working with private industry to develop control programs
using the attractants.
Funding: USDA-ARS.
PROJECT CONTACT
Peter Teal (Peter.Teal@ars.usda.gov)
New Lures and Traps for Control of Small Hive Beetle (SHB) and Prevention of Invasion
by Beetles Related to SHB. Working with scientists at the Department of Entomology and
Nematology, University of Florida, ARS Gainesville scientists found that chemicals from
bumble bee colonies were attractive to SHB. The beetle showed no preference for the honey
bees over the bumble bees.
ARS scientists in Gainesville have developed a highly effective lure for the SHB based on
chemicals produced by ripe fruit. The attractant has outperformed currently used attractants for
the pests.
Also, scientists in Gainesville have developed a light-based attractant-trap system for capture of
small hive beetle adults and larvae in honey houses. Tests show that the trap captures at least
80 percent of all wandering larvae.
These scientists also documented that the SHB reproduces as well on ripe fruit as it does in
honey bee colonies. This finding, as well as the fact that beetles are more strongly attracted to
odors from fruit like pears and cantaloupe, demonstrates that the pest is very capable of surviving
in the absence of managed bee hives and provides important information for developing
strategies to mitigate beetle invasion of hives.
A-30
Scientists at Gainesville, working with scientists from the International Center for Insect
Physiology and Ecology in Nairobi, Kenya, have also identified a new beetle pest of honey bee
colonies in Africa and have discovered that the beetle is attracted to lures currently in use to
monitor for the SHB. These discoveries are important because we can now monitor for this pest
at ports of entry into the United States and thereby know if and when the new beetle invades the
United States.
Funding: USDA-ARS.
PROJECT CONTACT
Peter Teal (Peter.Teal@ars.usda.gov)
Major Bee Pathogen Sequenced. Recently, ARS scientists in Weslaco, Texas, finished
sequencing one of the major honey bee pathogens, Ascosphaera apis, the causative agent of
chalkbrood disease. Research focuses on discovering genes involved in the invasion and
pathogenesis of the bee host. This information will lead to the development of novel disease
control methods.
Funding: USDA-ARS.
PROJECT CONTACT
Chalkbrood Disease and Implementations to Host Pathogenesis. ARS scientists analyzed
responses of the honey bee fungal pathogen Ascosphaera apis during host pathogenesis using
high-throughput sequencing. Data analysis captured a significant number of differentially
expressed genes that may be related to fungal reproduction, host invasion, and stress responses.
This study may provide new insights into the mechanisms of host invasion and progression of
chalkbrood disease and presents a unique opportunity to improve our understanding of the highly
complex nature of host-pathogen interactions.
Funding: USDA-ARS.
PROJECT CONTACTS
Anna Bennett (akb39@hoyamail.georgtown.edu)
3. Establish guidelines for floral gardens to maintain stronger honey bees.
and
4. Develop best management practices for pesticide use.
A-31
Accomplishment
Progress Toward Best Management Practices for Pesticide Use. EPA is working with a
broad range of stakeholders through the Pesticide Program Dialogue Committee (PPDC), a
stakeholder group chartered under the Federal Advisory Committee Act, to explore and develop
additional ways of mitigating the potential effects of pesticides on bees. Broad stakeholder input
will best ensure success of best management practices (BMPs) that may involve not only
beekeepers, but also growers and pesticide applicators. Additional mitigation measures under
consideration include both improved label language and encouraging
communication/cooperation between growers/applicators and beekeepers.
EPA has been working through its regional offices and with State Lead Agencies to engage local
stakeholders in dialogue to understand successful grower-beekeeper interactions on a local scale.
Understanding successes at the local level may serve as a basis to expand or transplant local
successes to other State or national programs. Programs like Driftwatch
(http://driftwatch.agriculture.purdue.edu/index.html) are being examined as a means of
identifying the location of vulnerable crops like honey bee colonies (apiaries) through national
registries that would enable growers/applicators to be aware of such vulnerable areas in advance
of pesticide applications and communicate pesticide application options with the beekeepers
before they occur.
As discussed earlier, EPA is also working with its OECD international partners to develop a
compendium of mitigation measures that various countries have used around the world to
mitigate the potential risks of pesticides to insect pollinators.
PROJECT CONTACTS
Goal 2: Develop best management practices for non-Apis bees to provide alternative
pollinators for crops, gardens, and natural areas.
1. Develop best management practices for pest and pathogen control in non-Apis bees.
and
2. Establish guidelines for maintaining stronger populations of non-Apis bees in agricultural
systems, home gardens, and wild lands.
Accomplishments
Blue Orchard Bee Workshops Delivered to Almond Production Community. ARS
scientists with California Cooperative Extension personnel organized and delivered workshops
(2009 and 2010) to provide information on the blue orchard bee and its use for almond
pollination. Workshops were designed to facilitate networking among the almond production
community interested in using blue orchard bees as almond pollinators along with, or instead of,
A-32
honey bees. Guidance on managing blue orchard bees for almonds is now available to promote
its use and reduce pressure on the sole use of honey bees.
Funding: USDA-ARS and University of CaliforniaDavis.
PROJECT CONTACTS
James Cane (jim.cane@ars.usda.gov)
Theresa Pitts-Singer (theresa.pitts-singer@ars.usda.gov)
Carolyn Pickel (cxpickel@ucdavis.edu)
Efficiency of Alfalfa Leafcutting Bees Affected by Stocking Density and Floral Resource
Abundance. The alfalfa leafcutting bee (M. rotundata) is commonly used to pollinate alfalfa for
seed production in the United States and Canada, but maintaining healthy stocks of these bees is
hampered by disease, parasites, predators, and unexplained mortality of eggs and small larvae.
An ARS researcher has shown that typical U.S. alfalfa leafcutting bee stocking densities for
alfalfa pollination are unnecessarily high, decreasing the number of bees that remain at the
commercial site, decreasing bee pollination efficiency, and reducing the number of healthy
offspring produced. The amount of alfalfa bloom in fields also affects the number of bees that
remain onsite and the number of offspring that can be produced. This research provides
information for optimizing stocking density in light of available floral resources.
Funding: USDA-ARS.
PROJECT CONTACT
Delaying Novaluron Applications Decreases Negative Effects. Novaluron (Rimon) is a
relatively new insecticide that is an insect growth regulator, labeled for lygus control in alfalfa
fields during bloom. Some alfalfa leafcutting beekeepers have complained about poor bee
returns in fields where novaluron was used, and laboratory trials have shown this pesticide to be
toxic to larvae and eggs. Field experiments were conducted in 2010 to evaluate the effect of the
timing of novaluron (Rimon 0.83 EC) spray applications on alfalfa leafcutting bee reproduction.
Spray timing was found to have no impact on the mean number of nest cells produced by the end
of the season. However, the percentage of pollen balls (bees that died as eggs or young larvae)
was lower, and the percentage of live larvae higher, on unsprayed (control) plots and plots
treated with Rimon late, as compared to plots treated during early and mid-bloom. These
results indicate that Rimon has a reduced impact on overall production of healthy alfalfa
leafcutting bees when applications are delayed until the late bloom period.
Funding: USDA-ARS, USDA-NIFA, and Chemtura.
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PROJECT CONTACTS
James Barbour (jbarbour@uidho.edu)
Nesting Methods Successfully Established for Four Bumble Bee Species. Bumble bees are
important pollinators of commercial greenhouse crops, but they are difficult to raise in captivity.
Because it is particularly difficult to get queens to establish new nests in captivity, three nest
establishment methods were tested on four species of bumble bees. The results show that some
techniques greatly increase the success rate (by fourfold) in some species in comparison to other
techniques. By targeting the proper rearing techniques to a given species, bumble bee producers
and researchers will be able to save time and resources when producing these bees in culture.
Funding: USDA-ARS.
PROJECT CONTACT
James Strange (james.strange@ars.usda.gov)
Wildland Fire Shown to Increase Wild Pollinators. Controlled burns constitute one method
used to manage fuel loads in natural areas, but the effects on pollinators remain unknown. The
fates of wild bee communities following wildfire were largely unknown but are critical to
anticipating pollination services during large post-fire rangeland restoration projects. Using a
new suite of sampling protocols, researchers systematically sampled bee floral guilds over time
after large burns, sampling from sites inside and outside the burned areas. Plant communities
were also characterized. Where rangeland plant communities were in good shape before
burning, the diversity of the native bee communities returned the following year. Over several
years, the native wildflowers likewise recovered. Initial seeding in restoration projects should
include plants that are broadly attractive to local native bees to sustain these bees until the native
plant communities can reestablish, since that re-establishment can take several years.
Funding: USDA-ARS, DOI-BLM, and USDA-FS.
PROJECT CONTACT
James Cane (jim.cane@ars.usda.gov)
Goal 3: Maintain bees with resistance to parasites and pathogens.
1. Identify traits associated with resistance to parasites and pathogens.
Accomplishments
USDA Varroa-Resistant Honey Bees Found Well Suited For Commercial Pollination in
Two Trials. ARS scientists tested Russian honey bees and bees containing a Varroa-resistant
trait (Varroa-sensitive hygiene [VSH]) for size and productivity in two large-scale field tests
comprising two different migratory routes. Two years of testing during commercial pollination
of almonds, apples, blueberries, and cranberries, with overwintering in Louisiana, showed the
USDA Varroa-resistant stocks to be as large and productive as control stocks at each pollination
A-34
site. One year of a test involving almond pollination and Midwest honey production, with
overwintering in Californias Central Valley, again showed Russian and VSH bees to have
adequate colony size, survivability, and honey production. These results suggest that Varroaresistant bees are well-suited for commercial pollination.
Funding: USDA-ARS.
PROJECT CONTACTS
Tom Rinderer (Tom.Rinderer@ars.usda.gov)
Bob Danka (Bob.Danka@ars.usda.gov)
Improved Management Strategies For Russian Honey Bees Developed. ARS scientists at
Baton Rouge, Louisiana, have evaluated management procedures to improve Russian honey bees
for early season pollination of almonds. Extensive tests found that feeding regimes (and
secondarily, hive size) affect colony populations. Colonies fed pollen substitute dwindled less in
winter than those not fed. Feeding pollen substitute with natural pollen added was much better
than feeding just pollen substitute. Feeding protein as patties was better than feeding it in plastic
comb within the brood nest. Feeding sucrose syrup at a slow rate continuously from autumn to
mid-winter simultaneously with protein increased colony size. Russian colonies grew more in
8-frame hives than in 10-frame hives, but hive size was less important than feeding protein.
Housing colonies in black hives did not improve colony population over colonies in white hives.
These findings collectively show that Russian honey bees can be managed in the southern United
States to produce colonies that are more than sufficient to rent for almond pollination in
February.
Funding: USDA-ARS.
PROJECT CONTACTS
Ongoing Research
Identifying Genes that Confer Resistance to Varroa Mites. Two separate projects were
undertaken, and genes were mapped to chromosomal regions that influence each of the two
behavioral traits that have been shown to be important for suppressing mite populations:
Varroa-sensitive hygiene (VSH) and mite-grooming behavior. Several chromosomal regions
were identified for each trait. The genes in these regions are being analyzed and considered for
follow-up experiments to confirm their role in conferring resistance to Varroa so that they can be
targeted with marker-assisted selection to pyramid multiple resistance genes in commercial
stocks.
A-35
PROJECT CONTACTS
Greg Hunt (ghunt@purdue.edu)
Miguel Arechavaleta-Velasco (are@servidor.unam.mx)
Thomas Webster (thomas.webster@kysu.edu)
Also see Goal 4, Objective 1: Identifying genes that confer resistance to Varroa and pathogens,
and genes that respond to biotic challenges.
2. Introduce resistance traits into bee stocks favored by the industry.
Accomplishments
Breeding for Hygienic Behavior. University of Minnesota researchers and extension specialists
are evaluating commercial honey bee stocks for the level of hygienic behavior, a trait that is
associated with the bees resistance to the Varroa mite. A pilot certification program will be
initiated for the hygienic trait. A Tech Transfer team is forming in California to assist bee
breeders with stock selection for hygienic behavior and to reduce chemical use in breeder
colonies. It is envisioned that this team will serve as a model for the Nation in producing local,
regionally adapted queens that are resistant to mites.
Funding: National Honey Board and California Almond Board.
PROJECT CONTACT
Commercialization of Varroa-resistant Honey Bees Selected for Pollination Performance.
Varroa mites are a major cause of colony losses throughout the United States. Bees with
Varroa-sensitive hygiene (VSH), which have good resistance to Varroa mites, were tested by
researchers for two seasons in a commercial migratory beekeeping operation. Bee colonies were
created from VSH queens that were out-crossed, i.e., matings were not controlled, a method used
by most large-scale beekeepers. Bee colonies were shipped nationwide for pollination of four
crops and for late-summer honey production. VSH colonies performed well in terms of survival,
populations, and resistance to Varroa mites. The best surviving VSH bee colonies from each
year were propagated to form a VSH breeding population that had enhanced genetics for both
mite resistance and behavior related to crop pollination. These bees are now being marketed by
a Cooperative Research and Development Agreement partner, Glenn Apiaries, and the use of
their germplasm should improve adoption of mite-resistant bees by commercial beekeepers that
pollinate crops.
Funding: USDA-ARS.
A-36
PROJECT CONTACTS
Ongoing Work
Genetic Techniques Used to Improve Bee Breeding. The University of Tennessee has
replaced half its bee stock with varieties resistant to Varroa mites (either the Varroa-Sensitive
Hygiene [VSH] strain or with hybrids raised from VSH queens). Equipment and apiary
expansion is underway to conduct bee breeding demonstration workshops in 2011 and 2012.
Workshop materials will be obtained or developed for inclusion on eXtension.org for use in any
bee breeding workshop. These efforts will increase the use of robust bee stocks.
Funding: USDA-NIFA.
PROJECT CONTACTS
Nick Calderone (nwc4@cornell.edu)
Greg Hunt (ghunt@purdue.edu)
Thomas Webster (thomas.webster@kysu.edu)
Michael Wilson (mwilso14@utk.edu)
3. Use genomic technologies and germplasm preservation to maintain quantities of desirable
honey bee germplasm.
Accomplishments
Honey Bee Germplasm Importations to Improve Genetic Variation in United States.
Honey bee semen was collected from locations in Italy and the Republic of Georgia in 2010 and
returned to the United States under a USDA-APHIS quarantine permit to Washington State
University. The fresh semen was used to inseminate queens produced from existing U.S.
commercial strains of honey bees and overwintered in Washington and California (collaboration
with University of CaliforniaDavis). This genetic material is being incorporated into existing
U.S, honey bee strains to increase sex allele diversity and reduce inbreeding effects. Genetic
material derived from the Italian importations (20082010) will be released to the commercial
bee breeding industry in 2011.
Funding: Washington and California State Beekeeping Associations and
USDA-NIFA-AFRI-CAP.
PROJECT CONTACT
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Cryopreservation of Honey Bee Germplasm. In 2010, the Washington State University

research team also developed a practical methodology for maintaining honey bee germplasm
(semen) by cooling samples at temperatures below the freezing point. Using this new method,
researchers there produced three successive generations of honey bee queens from cryopreserved
(i.e., frozen at liquid nitrogen temperatures) semen in 2010. This demonstration marked the
turning point for a new era of germplasm preservation/conservation in honey bees, as it will now
be possible to establish genetic repositories for the honey bee. Future germplasm collections
(2011 and beyond) will include cryopreservation of a portion of the semen for subsequent use. A
manuscript for publication in a peer-reviewed journal was prepared and submitted on this topic.
Funding: Washington and California State Beekeeping Associations and
USDA-NIFA-AFRI-CAP.
PROJECT CONTACT
4. Transition to mite- and pathogen-resistant honey bee stocks.
Accomplishments
Groundwork Established for a Sustainable Market for Genetically Improved Queens.
Researchers are working to train beekeepers in stock selection (e.g., VSH bees) and breeding
techniques, as well as management and testing practices to reduce impact from pests, pathogens,
and chemicals. Specifically, scientists are teaching a 2-day Queen Rearing Short Course every
summer at the University of Minnesota to assist bee breeders. This course combines lecture and
hands-on field work.
In 2008 and 2009, researchers conducted onsite visits with 17 queen producers in northern
California. These operations produce at least half of the commercially available queens in the
Nation and thus have major impact on honey bee genetics and improvement nationally.
Scientists demonstrated how to test their stock for hygienic behavior and how to test their
colonies for Nosema, and they provided best management practices, including reducing chemical
inputs into their breeding stocks.
Washington State University and University of California at Davis researchers have imported
selected stock for two Carniolan and Italian bees for breeding purposes. In the future, the team
will bring in a third subspecies favored by beekeepers, the Caucasian.
Over the 2-year study, two things became evident: (1) bee breeders are very competent and
produce high-quality, well-mated queens to supply beekeepers throughout the Nation; (2)
breeding for pathogenic resistance is highly complex, while maintaining productive
characteristics and pollination efficiency requires professional assistance to help bee breeders
improve stock selection, enhance genetic diversity, and perform disease diagnostics.
Funding: USDA-NIFA.
A-38
PROJECT CONTACTS
Increased Transfer of the VSH Mite-Resistance Technology to Foster Breeding of Bees
with Improved Mite Resistance. Bees with the trait of Varroa-sensitive hygiene (VSH) have
strong resistance to Varroa mites. VSH breeder queens are available through an ARS
partnership with a commercial queen breeder. Semen from VSH bees now is directly available
from ARS for incorporation into existing bee stocks. Research showed that commercially
available VSH queens that are mated to non-VSH drones have acceptable mite resistance. Tests
are ongoing in Hawaii to determine the value of VSH in mitigating Varroa damage in a tropical
environment that is the base of a large queen production industry. Two workshops were given in
2010 at regional and national beekeeping meetings to teach breeders how to test, select, and
breed for the trait. Together, these efforts should encourage incorporation of VSH-based mite
resistance into diverse bee stocks and thus support beekeeping sustainability.
Funding: USDA-ARS.
PROJECT CONTACTS
Also see Topic IV, Goal 3, Objective 2.
Goal 4: Develop ways to manage mite resistance to miticides and create alternatives.
1. Develop resistance management programs that provide beekeepers with tools for mite
management.
Accomplishment
EPA Expediting Reviews for Section 18. EPA is working with State Lead Agencies to provide
beekeepers with appropriate tools to control bee colony pests such as Varroa mites. The Agency
is working closely with USDA ARS and the Office of Pest Management Policy (OPMP) to
expedite reviews of Emergency Exemption requests (under section 18 of the Federal Insecticide,
Fungicide and Rodenticide Act [FIFRA]), Special Local Needs Registrations
(under section 24c of FIFRA), and full registrations (under section 3 of FIFRA) of miticides.
PROJECT CONTACTS
2. Develop new methods of managing parasites and pathogens.
See Type IV, Goal 3.
A-39
Goal 5: Improve the regulatory framework to better protect against the introduction of new
pathogens, pests, and parasites of bees to meet World Trade Organization (WTO) and
International Committee of the World Organization for Animal Health (OIE) requirements
for the importation and exportation of honey bees.
1. Develop new molecular detection systems that can be used to detect pathogens, pests, and
parasites in introduced bee stocks and bee products used in beekeeping.
and
2. Explore opportunities to change regulations based on new molecular detection systems. For
example, if a virus is shown to be pathogenic and reliable new detection methods are found,
then movement of virus-contaminate bee stocks may be regulated by bodies such as OIE.
Accomplishments
New Molecular Assay for Resistant Bacterial Strains Developed. ARS identified the
mechanism of resistance of the bacterial honey bee pathogen (for American foulbrood) to the
antibiotics oxytetracycline (OTC) and developed a new molecular assay for detecting
OTC-resistant bacterial strains in bee samples. This new identification method is now available
for regulatory officials who are considering ways of preventing the spread of resistant bacterial
strains in bee shipments.
Funding: USDA-ARS.
PROJECT CONTACT
Guidelines for Bee Imports Developed. The North American Plant Protection Organization
completed recommendations to coordinate regulation and importations of non-Apis bees between
Mexico, Canada, and the United States. Initial guidelines were developed for the safe
importation of bees to avoid the accidental release of bee pathogens and parasites and to avoid
the introduction of bee species that may cause a loss of native bees.
PROJECT CONTACTS
Colin Stewart (Colin.Stewart@aphis.usda.gov)
Rosalind R. James (Rjames@biology.usu.du)
3. Establish processes for periodic monitoring of the U.S. honey bee population to determine
whether specific pests are present.
A-40
Accomplishment
Pilot Survey for Bee Diseases, Parasites, and Pests. APHIS, in collaboration with ARS,
conducted a pilot survey in 2009 in Florida, California, and Hawaii to validate sampling
protocols used to determine which diseases/parasites/pests of honey bees are and are not present
in the United States. A limited national survey of 13 States was conducted in 2010. A report of
these results can be found at
http://www.aphis.usda.gov/plant health/plant pest info/honey bees/downloads/2010-2011Limited Survey Report.pdf. A national survey is being conducted in 2011 in 34 States. The
exotic pests Tropilaelaps mites, Apis ceranae, and Slow Paralysis Virus have not been found
during this survey. Therefore, the United States is not allowing importations from countries
known to have these pests (e.g., Australia and Southeast Asia).
PROJECT CONTACTS
Robyn Rose (Robyn.I.Rose@aphis.usda.gov)
Goal 6: Demonstrate improved colony health by integrating research-derived knowledge and
tactics into an Area-wide Project.
1. Test and verify management approaches for mite control, improved diet, improved bee stock,
and changes in migratory practice.
and
2. Transfer technology for early spring bee availability for pollination.
Accomplishment
Area-wide Project Initiated. ARS is continuing an Area-wide Project on Honey Bee Health
across multiple ARS locations (Tucson, Arizona; Beltsville, Maryland; Weslaco, Texas; and
Baton Rouge, Louisiana). The project has several aspects, including documenting the impact of
migration on bee colonies, examining the effects of supplemental feeding on colony health,
developing more resistant bee lines and improved methods for their management, and
developing better control methods for honey bee pests. Ultimately, the project aims to develop a
set of best management practices for migratory beekeepers to reduce stress on their bee colonies,
thereby enabling bees to ward off threats. Specific results of these individual research projects
are described elsewhere in this report.
Funding: USDA-ARS.
A-41
PROJECT CONTACTS
John Adamczyk (John.Adamczyk@ars.usda.gov)
Frank Eischen (Feischen@weslaco.ars.usda.gov)
Also see Topic III, and Topic IV, Goal 1.
Goal 7: Transmit or disseminate science-based information to manage bees.
1. Develop, maintain, and preserve a secure Web-based site for scientific collaboration
(SharePoint).
and
2. Develop, maintain, and update a Web-based public Internet site (e.g., eXtension or PIPE;
Pest Information Platform for Extension)
Accomplishments
eXtension Progress
The eXtension.org Community of Practice (CoP) continues to disseminate Web-based

information on bee health (http://www.extension.org/bee_health). Currently, the Bee
Health CoP has over 100 contributors with expertise in bee research and extension.
There are approximately 400 pages of content on this Web site. A few examples
include (1) The Best Management Practices For Beekeepers Pollinating Californias
Agricultural Crops, (2) Varroa-Sensitive Hygiene and Mite Reproduction, and (3)
American Bee Research Conference proceedings with videos of scientific
presentations. An average of 11,000 page views per month was recorded during a
12-week period in 2010. Also, the CoP features an Ask an Expert tool that allows
the public to ask bee health professionals questions regarding concerns about bees.
Users can upload pictures to facilitate better disease and pest identification. To date,
about 500 questions about bees were successfully answered by the experts.
A new team of 27 bee research and extension specialists has organized around the
CoP to expand on surveys of honey bee losses (such as the winter loss survey) and
sampling projects (such as the California Bee Breeders stock improvement effort). A
new Web site was created, which solicits survey participation and provides
information about their efforts (http://beeinformed.org/). A blog page was also
created to foster informal discussions about bee-related topics between project
cooperators and the public (http://beeinformed.org/blog).
A-42
Other ongoing Web-related outreach tools include email campaigns, articles in

beekeeping journals with an online presence (e.g., Bee Culture and American Bee
Journal), and results from research by NIFAs Managed Pollinator CAP team
(http://www.beeccdcap.uga.edu).

PROJECT CONTACTS
Keith Delaplane (Ksd@uga.edu)
John A. Skinner (Jskinner@utk.edu)
Zachary Huang (Huang@msu.edu)
Greg Hunt (GHunt@purdue.edu)
May Berenbaum (Maybe@uiuc.edu)
Social Media Outreach Initiated. Researchers are pursuing additional outreach opportunities
using social networking sites and public Web pages. Honey bee health is featured on a YouTube
page (http://www.youtube.com/beehealth), and researchers are now implementing pages on
Facebook, Twitter, Second Life, and Wikipedia, and beekeeper Web forums such as
www.beesource.com.
Funding: USDA-NIFA.
PROJECT CONTACTS
John A. Skinner (Jskinner@utk.edu)
Keith Delaplane (Ksd@uga.edu)
A-43
Control
Number:
7270983
Control
Number:
7270986
Control
Number:
7428462
From:
Subject:
Date Sent:
Date Received:
Joe Harman (b) (6)

ge alfalfa
12/16/2010 06:30:33 CST
12/16/2010 06:32:41 CST
>
Ban GE alfalfa. The risk of damage to other crops is too great.
Joe and Evy Harman

Owners/Innkeepers
Frederick House
28 North New St.
Staunton, VA 24401
<http://www.frederickhouse.com> www.frederickhouse.com
(b) (6)
800-334-5575
(b) (6)
In the face of severely declining bee colonies nationally with beekeepers reporting record
losses this year it would not be responsible to continue to allow these threatening
compounds to be used so broadly. Independent scientists and commercial beekeepers attribute
dramatic bee die-offs to a combination of factors, but exposure to neonicotinoids is a key
contributor. We are asking you as Chief Executive to direct the EPA to follow the EU and EFSA
lead and recognize the risks are unacceptably high. Pollination services provided by honey bees
and the other even less-studied wild bees are far too important for agriculture, gardens and
wild plants to treat them in a non-precautionary manner. Many thousands of beekeeper
livelihoods, and indeed the future viability of commercial beekeeping and the crops relying on
these pollination services, are potentially in jeopardy. Experts have identified the potential for
domino effects of cascading inadequate crop pollination due to shortage of viable pollinators.
This could rapidly evolve into devastating, perhaps irreversible, losses to farmers, consumers
and the economy as a whole, which relies on domestically-produced bee-pollinated food and
fiber crops.
In recent statements about the EUs decision, EPA officials highlighted a recent USDA report,
the Report on the National Stakeholders Conference on Honey Bee Health - National Honey Bee
Health Stakeholder Conference Steering Committee. Unlike the peer-reviewed, scientific EFSA
report, the USDA report was not peer-reviewed; it derived from a meeting of numerous
stakeholders including many non-scientists. It is dated and not comprehensive. Further, there
was not consensus among the stakeholders on the statements in the final report.
We would like to bring your attention to recent acknowledgments of key facts by EPA officials,
made in public statements at recent meetings, in media statements, in EPA documents and
other venues:
They acknowledged EPAs enforcement guidance for neonicotinoid use was inadequate.
They acknowledged EPAs bee kill incident reporting system was inadequate.
They have stated the labels on neonicotinoid products are inadequate to mitigate
adverse environmental effects, specifically to avoid seed dust-mediated mortality to
honey bees and other beneficial insects in or near corn fields.
They recognize the current corn planting machinery poses significant dust-off risks and
needs changing, while also recognizing that such changes will likely take many years and
stating that EPA lacks authority to mandate machinery changes.
They acknowledge that bee health and populations, and crop pollination, are in a nearcrisis state based on several synergistic factors including insecticide use.
They indicated the agency has not consulted with the U.S. Fish and Wildlife Service on
potential effects on threatened or endangered species under Sec. 7 of the Endangered
Species Act for the neonicotinoid insecticides.
Despite the above, EPA has refused to exercise its regulatory power to address the one factor it
could address tomorrow the major contribution of these insecticide to bee declines and
instead has pointed to land use decisions, crop planting choices by farmers, pathogens, bee
nutrition and other factors over which EPA has no authority. Indeed, no other Federal agency
2
has the power to help stem bee declines by addressing any of those synergistic factors within a
reasonable timeframe.
We would like to further highlight a broader threat: water contamination by imidacloprid,
clothianidin, thiamethoxam and the other compounds, the effect of which is to sterilize much
of the invertebrate food chain, threatening insects, fish, amphibians and other taxa, including,
but not limited to, aquatic and insectivorous birds. Recently, the American Bird Conservancy
(ABC) released a report, The Impact of the Nations Most Widely Used Insecticides on Birds,
researched by an internationally-recognized avian toxicologist, Pierre Mineau, who examined
the key EPA risk assessment documents and found numerous failures in the agencys approvals.
The report showed high direct and indirect mortality risks to a broad suite of birds, as well as to
aquatic invertebrates and ecosystems generally. It found that the observed acute threats from
water contamination by EPA-approved neonicotinoids may be totally unprecedented in the
history of pesticide registration. It also stated: EPA has not been heeding the warnings of its
own toxicologists. Dr. Mineau examined the approved product labels and found them
inadequate, stating regulators are clearly mistaken in believing that exposure to treated seed
can be minimized by label statements or adherence to good agricultural practices. The report
describes EPAs analysis as scientifically unsound. It urges the agency to suspend use of these
products and to ban neonicotinoid seed treatments altogether.
The leeway for your Administration to somehow disregard the ABC report was drastically
reduced by the peer-reviewed publication in PLOS ONE on May 1 of this year of a major Dutch
study, Macro-Invertebrate Decline in Surface Water Polluted with Imidacloprid. This multi-year,
comprehensive, field study states (emphasis added):
While a large amount of evidence exists from laboratory single species and
mesocosm experiments, our study is the first large scale research based on
multiple years of actual field monitoring data that shows that neonicotinoid
insecticide pollution occurring in surface water has a strong negative effect on
aquatic invertebrate life, with potentially far-reaching consequences for the
food chain and ecosystem functions.
In short, we could face a second Silent Spring above and beyond the threats to managed and
wild pollinators. Unfortunately, EPAs planned deadline of completing its Registration Reviews
for the major neonicotinoids by 2018 is far too slow in view of their potentially calamitous risks.
We trust you do not want to preside over this pending crisis. Directing EPA to follow the EUs
lead would be a first step but even more protective measures are needed, including a minimum
two-year suspension for all outdoor uses of neonicotinoid insecticides pending resolution of
their risks.
Thank you for your consideration of this urgent appeal. We look forward to your response.*
Sincerely,
George H. Fenwick
American Bird Conservancy
Jay Feldman
Beyond Pesticides
Patty Clary
Californians for Alternatives to Toxics
Michael Green
Center for Environmental Health
Andrew Kimbrell
Center for Food Safety
Jamie Rappaport Clark

Defenders of Wildlife
Wenonah Hauter
Food & Water Watch
Erich Pica
Friends of the Earth
Kim Leval
Northwest Coalition for Alternatives to Pesticides
Judy Hatcher
Pesticide Action Network North America
Michael Brune
Sierra Club
Scott Hoffman Black

The Xerces Society
CC:
Tom Vilsack, Secretary of Agriculture

Sally Jewell, Secretary of the Interior
Nancy Sutley, Chair, Council on Environmental Quality
Bob Perciasepe, Acting Administrator, EPA
*To reply to the signers please contact: Ms. Larissa Walker, Policy & Campaign Coordinator
Center for Food Safety, 660 Pennsylvania Ave. SE, Suite 302, Washington, DC 20003
email: lwalker@centerforfoodsafety.org; tel: 202.547.9359; fax: 202.547.9429
From:
To:
Cc:
Subject:
Date:
Attachments:
Kunickis, Sheryl
Miller, Renee
Epstein, David
Statement for Bee Health Report
Tuesday, March 19, 2013 8:09:09 AM
Honey Bee Conference Report 3 19 13 FINAL for clearance (2).docx
Renee,
Thanks for your assistance with getting this cleared. It should be a relatively simple process as
most of the key people in the agencies tapped to clear this document were instrumental in drafting
and/ or reviewing the early and final drafts! I have crafted the statement you requested and it
follows. Also, please use the file that is attached as I made one minor edit. Let me know if you
have questions.
The goal of the conference was for officials from USDA and EPA to receive
input from scientists, state governments, non-governmental organizations,
industry and other stakeholders as they consider future actions to
promote health and mitigate risks to North Americas managed honey
bees. The meeting had four aims:
Synthesize the state of knowledge regarding CCD
Synthesize the current state of knowledge regarding each of the

factors affecting honey bee health
Arthropod pests and pathogens
Nutrition
Pesticides
Bee biology, genetics, and breeding
Discuss and identify priority topics for research and Best Management
Practices (BMPs) to be considered by the CCD Steering Committee for
action
That said, this report is the proceedings of this conference not a USDA
policy document and was drafted over the last several months by
members of the CCD Steering Committee that participated in the

conference. Much of the content cannot be changed as it must reflect what
was heard or stated at the meeting. Finally, the following disclaimer is
included:
This is a report presenting the proceedings of a stakeholder conference

organized and conducted by members of the National Honey Bee Health
Stakeholder Conference Steering Committee on October 15-17, 2012 in
Alexandria, VA. The views expressed in this report are those of the
presenters and participants and do not necessarily represent the policies
or positions of the Department of Agriculture (USDA), the Environmental
Protection Agency (EPA), or the United States Government (USG).
The content of this document will be used to update the CCD Action Plan
and will help guide future research efforts.
Cheers,
Sheryl
Sheryl H. Kunickis, Ph.D.

Director
1400 Independence Ave., SW
Room 3871-South Building, MS-0314
Washington, D.C. 20250-0314
(202) 720-5375 Office

(b) (6)
sheryl.kunickis@ars.usda.gov
http://www.ars.usda.gov/opmp
From:
To:
Cc:
Subject:
Date:
Attachments:
Johansen, Erik (AGR)

mverdercarlos@cdpr.ca.gov; Epstein, David
Clock-Rust, Mary
WSDA bee protection pamphlet
Thursday, September 26, 2013 3:02:55 PM
image001.png
image002.png
image003.png
image004.png
image005.png
388-Ten Ways To Protect Bees From Pesticides.pdf
Hi Marylou and Dave,
I have attached a pdf copy of the WSDA bee protection pamphlet that was mentioned during the
Labeling Subgroup conference call yesterday, and a link to the WSDA news release
(http://agr.wa.gov/News/2013/13-27.aspx).
The pamphlet is intended to provide information on protecting bees from pesticides applied to
ornamental plants, and is primarily intended for homeowners. The pamphlet has specific
information regarding foliar and systemic uses of the nitroguanidine neonicotinoids on ornamental
plants.
Feel free to share the pamphlet with the Labeling Subgroup, if you feel it would be useful.
Take care,
Erik W. Johansen
Special Pesticide RegistrationProgram Coordinator
Phone: (360) 902-2078
Fax: (360) 902-2093
E-mail: ejohansen@agr.wa.gov
WSDA web site: http://agr.wa.gov/
LogoFinal-Color-NoText
WSDA is now on
or you can subscribe or unsubscribe to WSDA News Clips
From:
To:
Subject:
Date:
Attachments:
Kunickis, Sheryl
"terry@cornerpostrealestate.com"
USDA Response - Email regarding Honeybee Health Concerns
Wednesday, December 04, 2013 2:31:53 PM
image001.jpg
Dear Ms. Mendicino,

Thank you for your email to Secretary Vilsack dated November 21, 2013. I have
been asked to follow up with you on his behalf.
We share your concerns regarding honeybees, and many good scientists here at the
USDA and at Universities across the United States are hard at work finding solutions.
Unfortunately, the solutions to reversing bee declines are far more complicated than
banning pesticides. Honeybee health is also affected by a range of problems, from
poor nutrition due to decreased availability of forage plants to infestations by
parasites and diseases. Annual surveys of the beekeepers that tend to the bees
indicate that poor controls for the parasitic mite, Varroa, is the leading cause of
overwintering colony losses. There is no consensus among the US scientific
community that banning pesticides, alone, would solve the problem of bee declines.
The European Commission has, indeed, adopted a proposal to restrict the use of
three pesticides belonging to the neonicotinoid pesticide family for a period of two
years for certain uses on bee attractive plants and cereals. The restrictions began on
December 1, 2013, so it is far too early to make any claims that EU bee numbers
are positively responding to an action not yet taken.
The Environmental Protection Agency (EPA), the agency of the Federal government
that regulates pesticide use, is not currently banning nor severely restricting the use
of neonicotinoid pesticides. Neonicotinoid pesticides are currently being re-evaluated
through registration review, the EPA's periodic re-evaluation of registered pesticides
to ensure they meet current health and safety standards. The EPA bases its pesticide
regulatory decisions on the entire body of scientific literature. Based on currently
available data, the EPA's scientific conclusions are similar to those expressed by the
European Food Safety Authority (EFSA) with regard to the potential for acute effects
and uncertainty about chronic risk. However, the EFSA report does not address risk
management, which, under U.S. Federal law, is a key component of the EPA's
pesticide regulatory scheme.
Agricultural producers in the US work diligently and with great care to provide food
security for our nation. The availability of an abundant, affordable supply of food to
an ever-expanding US population that has grown three-fold in the past century,
alone, is an amazing accomplishment in a world where hunger and malnutrition
affect nearly one billion people. No doubt you would agree that a brighter future
includes both healthy bees and a well-fed human population. We make risk-benefit
decisions every day. For example, we know that more than thirty thousand people
per year die in car accidents, yet we use that knowledge to build better and safer
cars, and most of continue to drive daily. We balance the risk with the benefits. The
same approach is needed in the use of pesticides in producing our food and fiber.
The predominance of farmers do not wantonly and carelessly misuse pesticides, but
are continuously trained through land-grant universities in every state of the nation
in best management practices that promote limited, timely, and accurate pesticide
use and application. As a result, we have the safe and abundant food supply as
mentioned earlier.
Thank you for your concerns about honeybees expressed in your message. Be
assured that we take this issue very seriously and are making every effort to find
solutions.
Sheryl Kunickis

Director
(202) 720-5375 Office

(b) (6)
Cell
sheryl.kunickis@osec.usda.gov
From:
To:
Subject:
Date:
Attachments:
Kunickis, Sheryl
Epstein, David; Rogers, Ted; Chin, Teung; Fajardo, Julius - ARS; Coble, Harold
Sulfoxaflor...
Monday, December 09, 2013 10:24:07 AM
image001.jpg
BEE GROUPS SUE OVER PESTICIDE APPROVAL: Pollinator protection groups are
challenging EPA's May 6 approval of the neonicotinoid pesticide sulfoxaflor, which the
groups allege is "very highly toxic" to honey bees. In a 50-page complaint filed Friday in the
U.S. Court of Appeals for the Ninth Circuit, the groups, led by the Pollinator Stewardship
Council, argue that the Dow AgroSciences chemical has been found to have the potential to
pose a risk to bees, and that EPA erred by dropping its requirements for additional field
testing of the pesticide prior to granting it a full registration. "The record shows that EPA
improperly and artificially constrained its risk-benefit analysis, narrowly considering only
sulfoxaflor's purported benefits ... EPA failed entirely to account for the devastating impact
that sulfoxaflor will have both on the beekeeping industry and on the multitude of important
crops that must be pollinated by bees if they are to bear fruit or seed," the groups allege.
The complaint is available here: http://bit.ly/18dyq9E

Director
(202) 720-5375 Office

(b) (6)
Cell
sheryl.kunickis@osec.usda.gov NEW!
From:
To:
Subject:
Date:
Attachments:
Kunickis, Sheryl
Bartuska, Ann - OSEC; Ramaswamy, Sonny; Rexroad, Caird; Hackett, Kevin; Pettis, Jeff; Wilcox, Caren - OSEC;
Gibson, Loureatha - OSEC; Epstein, David
Review of CFS report by some land grant scientists re: Neonics
Monday, April 14, 2014 12:35:32 PM
Neonicotinoids Midsouth Perspective.pdf
Good Afternoon,
Please see a quick overview of thoughts on the presentation and the document that was
presented to many of us by the Center for Food Safety three weeks ago. (b) (5)
Bottom line: (b) (5)
Thanks,
Sheryl
From: Jeffrey Gore [mailto:JGore@drec.msstate.edu]

Sent: Saturday, April 12, 2014 1:17 PM
To: Scott D Stewart
Cc: Epstein, David; Darrell D Hensley
Subject: Re: FW: Neonics
David,
Attached is a report from the Center for Food Safety and a response that I wrote with review and minor
editing from my colleagues in the Mid-South. Our plan is to use this as a framework to write an article to be
published in the American Entomologist or some other venue. Feel free to contact me if you have any
questions or need additional information.
Jeff
Jeff Gore
Delta Research and Extension Center
Mississippi State University
P.O. Box 197

82 Stoneville Rd.
Stoneville, MS 38776
Blog: http://www.mississippi-crops.com
Phone: (662)686-3252
Cell: (b) (6)
>>> "Stewart, Scott D" <sdstewart@utk.edu> 4/11/2014 3:19 PM >>>
Jeff,
Maybe you should forward your well-prepared response to the recent anti-neonic article to David
Epstein. Ive copied him in with a link to my much more brief article. Someone needs to call foul!
http://news.utcrops.com/2014/04/how-valuable-are-insecticide-seed-treatments/
Scott
Scott D. Stewart, Professor and IPM Coordinator

The University of Tennessee
West TN Research & Education Center
605 Airways Blvd
Jackson, TN 38301
Phone: 731-425-4709
Fax: 731-425-4709
Email: sdstewart@utk.edu
Web: http://www.UTcrops.com
Neonicotinoid Seed Treatments and their Use in IPM Programs in the Mid-South
Jeff Gore, jgore@drec.msstate.edu
Mississippi State University, Delta Research and Extension Center, Stoneville, MS
Don Cook
Mississippi State University, Delta Research and Extension Center, Stoneville, MS
Angus Catchot
Mississippi State University Extension Service, Starkville, MS
Scott Stewart
University of Tennessee, Western TN Research and Extension Center, Jackson, TN
Gus Lorenz
University of Arkansas Extension Service, Lonoke, AR
David Kerns
LSU AgCenter, Macon Ridge Research Station, Winnsboro, LA
Value of Neonicotinoid Seed Treatments in the Mid-South
Farming is a business, period! More importantly, farming is one of the most risky businesses in
the world, with respect to economics. In the current environment, farmers invest hundreds of
thousands if not millions of dollars at planting and do not see a return on that investment until
harvest, several months later. In the meantime, more can go wrong between planting and harvest
than can go right, and farmers are walking a fine line between planting a crop the following
season and being out of business. The notion that a farmer would spend additional money on a
production practice that does not provide an economic return is foolish. Currently, seed costs are
at an all time high, mainly due to elite cultivars and technology fees associated with transgenic
traits (herbicide and insecticide resistance). Additionally, herbicide resistant weed species have
made early season management more difficult and costly compared to a decade ago. As a result,
farmers have reduced seed rates to minimum levels to offset some of the costs associated with
planting. In general, in-season risk can be reduced with an earlier planting date. Numerous
studies have shown that early production systems in soybean and cotton produce higher yields
and incur lower risk from drought and pests than later plantings in the Mid-South (Heatherly
1999, Adams et al. 2013). However, earlier plantings do not come without their share of risks.
Early spring conditions are often cool and damp in the Mid-South and can change from optimal
to sub-optimal within a 24 hour period. As a result, seedling emergence and plant growth and
development are often delayed, and the crop becomes more susceptible to insect and disease
pests. Insecticides and fungicides applied as seed treatments are an important component of crop
production to minimize the risk of stand losses from these pests, especially with early plantings
when pest populations and weather conditions are difficult to predict.
In cotton, thrips are an annual pest that can significantly delay maturity and reduce yields. Their
impact in cotton is often more dramatic in earlier plantings compared to later plantings. Thrips
are also a pest of soybean, but their impact on soybean growth and development is minor.
However, numerous other insect pests can impact soybean during the seedling stage. These
include threecornered alfalfa hopper, bean leaf beetle, and various soil insects. Soil insects such
as wireworms and white grubs are probably the most yield limiting insects in seedling soybean in
the Mid-South because of the widespread adoption of soil conservation programs. Many
growers in the Mid-South prepare their land during the late summer and early fall after the
previous crop has been harvested. Those fields host a wide range of winter annual plants that
support various soil inhabiting insects throughout the winter and early spring. Those winter
annual weeds are allowed to grow and prosper in fields to prevent soil erosion. The growers
apply a "burndown" herbicide 3 to 4 weeks before planting and plant into a stale seedbed. Lack
of tillage during the spring allows the majority of the soil insects to survive and damage the
crops planted into those fields when the crop seeds germinate and emerge. As a result,
insecticide seed treatments are an integral component of integrated pest management programs
for most crops in the Mid-South.
An experiment was recently conducted over a three year period at three locations in Mississippi
to investigate the impact of planting date, soybean maturity group, and insecticide seed treatment
on soybean yield and economics. The project was funded entirely by soybean checkoff dollars
through the Mississippi Soybean Promotion Board. The treatments included three planting dates
(mid-April, mid-May, and mid-June), five maturity groups (MG III, early MG IV, late MG IV,
early MG V, and late MG V), and two seed treatments (fungicide only and fungicide +
thiamethoxam). At all locations, the insecticide seed treatment resulted in yields significantly
higher than the fungicide only treatment (Table 1) when averaged across all planting dates and
maturity groups with an average yield advantage of 2.4 bushels per acre across all locations
(Buehring et al. in review). It is also important to point out that the yield advantage was
significant regardless of the overall yield potential of the site. Low yield environments
benefitted equally to average and high yield environments.
Table 1. Soybean yield response to seed treatments, averaged over soybean maturity
groups, planting dates, Verona, Stoneville and Starkville, MS.
Verona
Starkville
Stoneville
Seed treatment
------------------------Yield (bu/acre)------------------Mean
1
Apron
47.0 b
26.5 b
61.9 b
45.1
Apron +
Cruiser
50.3 a
28.3 a
64.0 a
47.5
1
Within a column, numbers with the same letters are not significantly different at the 5%
probability level.
More importantly, the use of an insecticide seed treatment resulted in a net economic return at all
locations regardless of the market price used ($8/bu - $12/bu). Returns ranged from $1.40 per
acre to $26.60 per acre when averaged across all other factors (Table 2). It is important to note
that the market price received by growers in Mississippi over the last few years has been greater
than $10.00/bu, and in many cases exceeds $12.00/bu.
Table 2. Apron + Cruiser seed treatment yield increase and returns above Cruiser seed
treatment cost at a selected soybean market prices.
Market
Price $/bu
8
10
12
Verona
Starkville
Stoneville
Avg.
------------Apron + Cruiser bu/acre increase------------------------3.3
1.8
2.1
2.4
---------Returns $/acre above Apron + Cruiser treatment cost ($13/A)--13.40
1.40
3.80
6.30
20.00
5.00
8.00
11.00
26.60
8.60
12.20
15.80
Given the high input costs associated with soybean production in the Mid-South, these values
could mean the difference between a net economic return for the grower and a net economic loss.
Although insecticide seed treatments do provide a certain level of "insurance" for early season
establishment and growth of soybean seedlings, the yield benefits and economic returns from
these treatments in the Mid-South demonstrate their importance in soybean IPM.
The results from field corn are even more pronounced in the Mid-South region. Because of the
relatively low planting populations and high soil insect pressure, stand loss due to the soil insect
complex is common in the region. This is especially true in areas where the sugarcane beetle
occurs. The soil insect complex is difficult to control in general and virtually impossible to
control with foliar insecticides. Often visual symptoms of soil insect injury to field corn are not
immediately apparent, and several weeks may pass before the full extent of the damage can be
evaluated and replant decisions made. If replanting is required, the optimum planting window
for corn has usually passed and yield potential declines substantially for plantings beyond the
optimum window. Herbicides used in corn are often applied early and are not compatible with
replanting of other crops suited for the Mid-South region, so late replants from stand loss pose a
risk most farmers cannot bear. Insecticide seed treatments greatly reduce the risk from the soil
insect complex in field corn in the Mid-South. The only alternatives to neonicotinoid seed
treatments are in-furrow applications of granular or liquid broad spectrum organophosphate and
pyrethroid insecticides.
In cotton, Cook et al. (2011) provided a review of thrips biology, crop injury, crop maturity, and
yield impacts. They cited numerous studies that showed both yield increases and no yield
response from thrips management in cotton. However, the authors cited research from Virginia
(Herbert 2002) where yield increases averaged 339 lbs lint/A from thrips management. More
recently, yield increases of 431 and 547 lb lint/A were observed in North Carolina and Virginia,
respectively (Herbert et al. 2007) where aldicarb and seed treatments with imidacloprid were
used. Similar results have not been published, but have been reported from the Mid-South (see
http://www.utcrops.com/MultiState/Trials/2011/Cotton%20Thrips%20Regional%20Thrips.pdf).
In general, thrips are considered a difficult pest to manage with foliar applied insecticides and
multiple applications are needed with foliar sprays of broad spectrum insecticides to obtain
satisfactory control. Because of this, thrips have been considered an annual pest of cotton in the
Mid-South and some at-planting control option is always recommended.
Alternatives to Neonicotinoid Seed Treatments
Very few alternatives are available for early season insect control in cotton, soybeans, and corn
in the Mid-South. The alternatives include granular or liquid insecticides that are applied in-
furrow or banded over the open seed furrow. The alternative insecticides include
organophosphates, carbamates, pyrethroids, and neonicotinoids (sprayed in-furrow). More
importantly, these insecticides are applied at much higher rates when used in this manner
compared with seed treatments. For example, one viable option to control the soil insect
complex in corn and soybean includes chlorpyrifos (Lorsban) applied at 1.0 lb ai/A. In contrast,
the maximum use rate for thiamethoxam applied as a seed treatment (Cruiser) in corn and
soybean is 0.165 and 0.083 lb ai/A, respectively. This equates to an approximately 6 and 12-fold
reduction in the total amount of active ingredient applied on a per acre basis when seed
treatments are used. Similarly, imidacloprid is applied at approximately 0.04 lb ai/A when
applied as a seed treatment in cotton. When imidacloprid is applied as an in-furrow spray
(Admire Pro), it can be applied at a maximum use rate of 0.33 lb ai/A, an 8.25-fold increase. If
thrips are controlled with foliar sprays in cotton, the maximum amount of active ingredient
applied per acre can easily exceed 0.5 lb. Also, use of the neonicotinoids as seed treatments has
been considered less likely to flare secondary pests compared to foliar sprays. Two-spotted
spider mite has become an important early season pest of cotton in many areas of the Mid-South.
This pest is generally maintained below economic densities by the actions of natural enemies.
Foliar applications of broad spectrum insecticides such as acephate or dicrotophos (the most
commonly used insecticides for foliar thrips control) will disrupt the natural enemy complex and
allow spider mites to become established and threaten economic losses.
Seed Treatments as a Component of IPM in the Mid-South
As stated previously, early season insect pests are considered an important limiting factor to
economic crop production in the Mid-South. Insect pests can delay maturity and cause
significant yield reductions in most crops grown in the Mid-South. Management of these insects
is complicated by the fact that many of them are not easily or economically controlled with foliar
insecticide applications based on an economic threshold. In the Mid-South, the soil insect
complex is difficult to predict prior to planting. Also, there are no foliar options available to
effectively manage these pests. Therefore, the use of an at-planting insecticide is recommended
in most crops in the Mid-South. Neonicotinoid seed treatments have been the product of choice
for about the last decade because of their low use rates on a per acre basis, ease of use, reduced
exposure to workers and handlers, and reduced impact to natural enemies. Neonicotinoid seed
treatments are not innocuous and can impact natural enemy populations; however, their impact is
much less than other at-planting options and foliar sprays. Because of these reasons and because
early season insect pests are an annual economic problem in the Mid-South, neonicotinoid seed
treatments are generally considered an integral component of IPM in most crops including
cotton, corn, soybean, peanut, wheat, grain sorghum, and rice.
Rebuttal to: Heavy Costs: Weighing the Value of Neonicotinoid Insecticides in Agriculture
The paper titled "Heavy Costs: Weighing the Value of Neonicotinoid Insecticides in Agriculture"
published by the Center for Food Safety is limited in scope. In their paper, the authors state "It
appears EPA has overvalued the 'insurance' neonicotinoids offer against non-existent or
insignificant pest pressures in many contexts." The information used to draw these conclusions
is based almost exclusively on information from the midwestern and northeastern U.S. where
they do not always see an economic benefit. In the southern U.S., and almost certainly in other
warmer climates, insect pests are an annual yield limiting problem that impact profitable crop
production in most crops. As a result, the conclusions drawn in this paper do not represent the
entire U.S.
The authors of this paper reviewed 19 manuscripts published in refereed journals and based their
conclusions off of those findings. The focus of this rebuttal will be on those papers that report
neonicotinoid seed treatment use on crops that are grown in the Mid-South (corn, soybean, and
wheat).
Corn
Cox et al. (2007):
This study was conducted in New York. The primary target was the soil insect complex. The
authors state that "The experimental site was plowed and harrow-cultipacked a couple of days
before planting in both years." Most of the soil insect complex that infests corn seedlings have
long life cycles and are generally in the field at the time of planting. Any type of cultivation
within a few days of planting will destroy a large percentage of the soil insect complex and most
entomologists and pest managers would not expect to see much of a benefit from at-planting
insecticides in this situation. In many areas of the country, USDA-NRCS programs promote
conservation tillage to minimize soil loss and runoff from crop fields. In conservation tillage
fields, the soil pest complex will be more robust than that observed with conventional tillage and
the results would be much more dramatic and consistent. Despite tillage before planting, the
authors state "The results of this study indicate that growers can safely use clothianidin seed
treatments where soil insect damage is expected."
Jordan et al. (2012):
This study was conducted in Virginia. The primary target of this study was white grubs and
wireworms. The white grub population consisted of primarily Japanese beetle in year 1 and
Asiatic garden beetle in years 2 and 3. The wireworm population consisted of primarily
Conoderus spp. in years 1 and 2. Overall, wireworm densities were low in year 3. The authors
state that "The results of our study showed a direct relationship between fall white grub soil
density, spring density, and subsequent stand and yield loss in corn." The authors also suggest
that pest species complex may have impacted the differences they observed between years. As a
side note, all of the fields used in this study were in corn fields following soybean. Results may
have been more dramatic in corn fields following corn production the previous year.
Petzold-Maxwell et al. (2013):
This study was conducted in Iowa, Illinois, and Nebraska. The primary targets were Diabrotica
spp. that included the western corn rootworm and northern corn rootworm, two species that do
not occur in most areas of the Mid-South. The authors compared Poncho 1250 (clothianidin) to
Aztec and Bt corn hybrids. Based on figure 1, the insects evaluated did not appear to cause a
level of injury that would reduce yields. This is based on the fact that significant differences
were observed in root injury on non-Bt corn, but no differences in yield were observed. The
authors state that Cruiser 250 was used in the control treatment to manage other insect pests.
This is a major flaw in the experimental design, because the insecticides are not being evaluated
over the full spectrum of pests that may have been present.
Wilde et al. (2007):

This study was conducted in Kansas. The targets included several different soil and foliar pests.
Damage from white grubs was significantly reduced. Also, significant yield losses were
observed in the control plots where wireworms were present. Chinch bugs were also controlled
and a significant yield benefit was observed. The authors suggest that Poncho and Cruiser have
"great promise for growers dealing with a variety of early-season soil inhabiting and foliar
pests."
Soybean
Cox et al. (2008):
This study was conducted in New York. The experimental site was chisel-plowed (deep tillage)
the day before the first planting date and then disked-harrowed on the day of planting at each
planting date. This would have eliminated numerous soil insect pests that may have impacted
soybean growth and development. Results may be completely different when planting into a
stale seedbed. The authors also state that this study was only conducted at 1 site in 2 years and
acknowledge that more research is needed under more diverse conditions. This is a very limited
study to use to draw broad conclusions and the results are not representative of the majority of
soybean growing regions.
Cox and Cherney (2011):
This study was conducted in New York at 3 locations over a 2 year period. Fifty percent of the
trials had a significant yield benefit from the use of a seed treatment. The authors converted
yields to a percentage. This is meaningless without knowing what the actual yields were. If
average yield was 20 bushels per acre, a 4% yield increase is probably not economical.
However, if average yield was 60 bushels per acre, then a 4% yield increase would probably be
economical. The authors also state that based on the seeding rate by seed treatment interaction
for partial returns, that growers can attain maximum partial profit at seeding rates of almost
50,000 fewer seeds per hectare. This is an important finding given the high costs of seed.
Esker and Conley (2012):
This study was conducted in Wisconsin. The authors state at the beginning of the conclusions
that "Results from this study indicated that seed treatments can be a cost effective component of
soybean production although several factors must be considered, in particular environment and
cultivar." In this study, the response of the economic return was highly dependent on grain sale
price. The highest price that the authors used for their analysis ($0.44/kg) would equate to about
$12.00/bushel, which is about the price growers receive in the Mid-South. In some years, the
price can greatly exceed this value. As a result, the actual probability of breaking even is
probably closer to the higher end of the range that the authors give and what is cited in the
Center for Food Safety article.
Johnson et al. (2009):
This study was conducted in Iowa, Michigan, and Minnesota evaluating the use of see treatments
against soybean aphid. The only year that soybean aphid had a significant impact on yields was
in 2005, the year that the seed treatment was not evaluated. This biased the economic analysis in
this study. The data for 2005 will make the IPM and prophylactic treatments look better than the
seed treatment when averaged across all 3 years of the study. In all cases, the seed treatment had
fewer aphid days than the IPM and control treatments. This is despite the fact that the authors
state that the seed treatment is gone before the aphids show up. If this is truly the case, how
could the seed treatment have fewer aphid days than the IPM and control treatments? In
Michigan, the seed treatment and prophylactic treatment yielded higher than the control and IPM
programs.
McCornack and Ragsdale (2006):
This study was conducted in Minnesota with soybean aphid as the primary target. In all cases,
yield was numerically greater in the in the thiamethoxam treatment compared to the control.
There is no indication of how the data were analyzed in this paper. The analysis was broken out
by year, but a combined analysis may have provided significant differences based on the trends.
Magalhaes et al. (2009):
This study was conducted in Nebraska against soybean aphid. The authors of the Center for
Food Safety state that higher aphid populations may overwhelm seed treatments, but
thiamethoxam held aphid populations below the economic threshold. Only imidacloprid was
overwhelmed by aphids. No yields were reported in this study.
Ohnesorg et al. (2009):
This study was conducted in Iowa against soybean aphid. In this study, thiamethoxam provided
similar yields to that observed with foliar sprays, but had less impact on natural enemies. Yields
do not correlate well with aphid days suggesting that other insect pests may have been present.
For instance, the number of aphid days was significantly lower in the 50 g thiamethoxam
treatment than the 100 g thiamethoxam treatment. However, yields were greater in the 100 g
treatment compared to the 50 g treatment.
Reisig et al. (2012):
This study was conducted in North Carolina and Virginia with thrips as the target pest. The
authors state "In contrast to the mid-South, where a variety of insect pests are present in seedling
soybean, the predominant insect pest of soybean in NC and VA is thrips." They also stated "The
presence of other seedling pests may justify the continued use of neonicotinoid seed treatments
in the mid-South."
Seagraves and Lundgren (2012):
This study was conducted in South Dakota against thrips and soybean aphid. The study was
conducted over a 2 year period at 1 location.
Tinsley et al. (2012):
This study was conducted in Illinois against soybean aphid. The data in this experiment were not
analyzed properly. It was analyzed as a factorial experiment, but every level of Factor B
(insecticide treatment) was not included at every level of Factor A (Soybean Line). Therefore
the interaction between soybean line and insecticide treatment is meaningless. No meaningful
conclusions can be drawn from this experiment as it is presented.
Wheat
Wilde eta al. (2001):
This study was conducted in Kansas and the primary targets included greenbug and Russian
wheat aphid, as well as, Hessian fly. Imidacloprid and thiamethoxam provided outstanding early
season control of both species at all rates. Control of late season populations was less consistent,
but the highest rates reduced damage. Seed treatments also provided good early season control
of Hessian fly. The authors concluded that seed treatments could be most useful in several
situations. These included when a fall infestation is likely or if an insect problem is a chronic
pest in a given area.
Royer et al. (2005):
This study was conducted in Oklahoma. Imidacloprid provided a significant yield benefit in
most situations. Low rates provided significant yield protection and the most economic benefit.
It also significantly reduced the incidence of barley yellow dwarf virus at all rates on all
varieties. Profits were higher for all imidacloprid rates where BYDV occurred. The authors
state "seed treated with imidacloprid has many environmentally and economically desirable
qualities (e.g. low application rate, minimal worker exposure hazard, prevention of virus disease
to the crop). If deployed prudently, an insecticide seed treatment offers a sensible tool to use in
an IPM program."
Conclusions
Research from all areas of the U.S. demonstrates the importance of neonicotinoid seed
treatments in many situations. The document from the Center for Food Safety highlighted
refereed publications to support the conclusion that neonicotinoid seed treatments do not provide
an economic benefit for producers. The current review of those papers suggests that
neonicotinoid seed treatments can provide an economic benefit for growers in the regions where
the research was conducted. Interpretation of selected manuscripts without considering all of the
underlying factors that can influence the outcome can be dangerous. The papers reviewed
represent a very small subset of all of the research on neonicotinoid seed treatments over the last
20 years and does not adequately represent the value of those treatments across the U.S. In the
Mid-South, neonicotinoid seed treatments are recommended by University Research and
Extension Specialists in multiple crops. Most of that research may not be published in refereed
journals, but it should not be discounted. In the Mid-South, research on the efficacy and value of
neonicotinoid seed treatments has been conducted since they were released and continue to be
studied today. The figure below shows a summary of six years of trials conducted across the
Mid-South (AR, MS, LA, TN, and MO) to evaluate the benefits of insecticide seed treatments.
A total of 103 replicated trials indicates that there is an 80% probability that growers will receive
a net economic benefit from the use of insecticide seed treatments in soybean. The yield
advantage from using an insecticide seed treatment averaged 3.3 bushels per acre across all trials.
Cox, WJ, E Shields, and JH Cherney. 2007. The effect of clothianidin seed treatments on corn
growth following soybean. Crop Science, 47:2482-2485.
Cox, WJ, E Shields, and JH Cherney. 2008. Planting date and seed treatment effects on soybean
in the northeastern United States. Agronomy Journal, 100(6): 1662-1665.
Cox, WJ and JH Cherney. 2011. Location, variety, and seeding rate interactions with soybean
seed-applied insecticides/fungicides. Agronomy Journal, 103(5):1366-1371.
Esker, PD and SP Conley. 2012. Probability of yield response and breaking even for soybean
seed treatments. Crop Science, 52:351-359.
Heatherly, L. G. 1999. Early soybean production system, pp 103-118. In L. G. Heatherly and H.
F. Hodges [eds.], Soybean production in the Midsouth. CRC Press, New York.
Herbert, D. A. 2002. Yield protection strategies for thrips in Virginia cotton. In P. Dugger and
D. A. Richter (eds.), Proceedings 2002 Beltwide Cotton Conferences, National Cotton Council,
Memphis, TN.
Herbert, D. A., Jr., J. Bacheler, S. Malone, and D. Mott. 2007. Thrips control options in
Virginia/North Carolina: overview, insights, and updates. In S. Boyd, M. Huffman, D. Richter,
and B. Robertson (eds.), Proceedings 2007 Beltwide Cotton Conferences, National Cotton
Council, Memphis, TN.
Johnson, KD, ME ONeal, DW Ragsdale, CD Difonzo, SM Swinton, PM Dixon, BD Potter, EW
Hodgson, and AC Costamagna. 2009. Probability of cost-effective managementof soybean aphid
(Hemiptera: Aphididae) in North America. Journal of Economic Entomology, 102(6): 21012108.
Jordan, TA, RR Youngman, CL Laub, S Tiwari, TP Kuhar, TK Balderson, DM Moore, and M
Saphir. 2012. Fall soil sampling method for predicting spring infestation of white grubs
(Coleoptera: Scarabaeidae) in corn and the benefits of clothianidin seed treatment in Virginia.
Crop Protection, 39: 57-62.
McCornack, BP and DW Ragsdale. 2006. Efficacy of thiamethoxam to suppress soybean aphid
populations in Minnesota soybean. Crop Management, 5(1).
Magalhaes, LC, TE Hunt, and BD Siegfried. 2009. Efficacy of neonicotinoid seed treatments to
reduce soybean aphid populations under field and controlled conditions in Nebraska. Journal of
Economic Entomology, 102(1): 187-195.
Ohnesorg, WJ, KD Johnson, and ME ONeal. 2009. Impact of reduced-risk insecticides on
soybean aphid and associated natural enemies. Journal of Economic Entomology, 102(5): 18161826.
Petzold-Maxwell, JL, LJ Meinke, ME Gray, RE Estes, and AJ Gassmann. 2013. Effect of Bt

maize and soil insecticides on yield, injury, and rootworm survival: implications for resistance
management. Journal of Economic Entomology, 106(5): 1941-1951.
Pynenburg, GM, PH Sikkema, DE Robinson, and CL Gillard. 2011a. The interaction of annual
weed and white mold management systems for dry bean production in Canada. Canadian
Journal of Plant Science, 91: 587-598.
Pynenburg, GM, PH Sikkema, and CL Gillard. 2011b. Agronomic and economic assessment of
intensive pest management of dry bean (Phaseolus vulgaris). Crop Protection, 30: 340-348.
Reisig, DD, DA Herbert, and S Malone. 2012. Impact of neonicotinoid seed treatments on thrips
and soybean yield in Virginia and North Carolina. Journal of Economic Entomology, 105(3):
884-889.
Royer, TA, KL Giles, T Nyamanzi, RM Hunger, EG Krenzer, NC Elliott, SD Kindler, and M
Payton. 2005. Economic evaluation of the effects of planting date and application rate of
imidacloprid for management of cereal aphids and barley yellow dwarf in winter wheat. Journals
of Economic Entomology, 98(1): 95-102.
Seagraves, MP and JG Lundgren. 2012. Effects of neonicotinoid seed treatments on soybean
aphid and its natural enemies. Journal of Pest Science, 85:125-132.
Soroka, JJ, LF Grenkow, and RB Irvine. 2008. Impact of decreasing ratios of insecticide-treated
seed on flea beetle feeding levels and canola seed yields. Journal of Economic Entomology,
101(6): 1811-1820.
Tinsley, NA, KL Steffey, RE Estes, JR Heeren, ME Gray, and BW Diers. 2012. Field-level
effects of preventative management tactics on soybean aphids (Aphis glycines Matsumara) and
their predators. Journal of Applied Entomology, 136: 361-371.
Wilde, GE, RJ Whitworth, M Claassen, and RA Shufran. 2001. Seed treatment for control of
wheat insects and its effect on yield. Journal of Agricultural and Urban Entomology, 18(1): 111.
Wilde, G, K Roozeboom, A Ahmad, M Claassen, B Gordon, W Heer, L Maddux, V Martin, P
Evans, K Kofoid, J Long, A Schlegel, and M Witt. 2007. Seed treatment effects on early season
pests of corn and corn growth and yield in the absence of agricultural pests. Journal of
Agricultural and Urban Entomology, 24(4): 177-193.
From:
To:
Subject:

Request from the Thurston County Commissioners to Restrict the Ornamental Use of Neonicotinoids to Protect
Bees
Monday, April 29, 2013 7:39:21 PM
image001.png
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2013 Thurston County Letter to WSDA - Restrictions on Neonicotinoids to Protect Honey Bees.pdf
Date:
Attachments:
Hi Marylou and David,
WSDA has Received a Request from the Thurston County Commissioners to Restrict the Ornamental
Use of Neonicotinoids to Protect Bees. Do either of you mind if I share this with the PPDC Labeling
subgroup as an FYI?
Take care,
Erik W. Johansen
Phone: (360) 902-2078
Fax: (360) 902-2093
WSDA is now on
COUNTY COMMISSIONERS
Cathy Wolfe
District One
Sandra Romero
District Two
Karen Valenzuela
District Three
BOARD OF COUNTY COMMISSIONERS

April 8, 2013
Don Hover
Director, WSDA
1111 Washington Street SE, 2nd Floor
PO Box 42560
Olympia, WA 98504-2560
Dear Mr. Hover,

We are writing to express our concerns regarding the Olympia Beekeepers Associations
substantial bee colony loss in 2012.
We share the beekeepers deep concern and belief that immediate action on a local level is
appropriate and necessary. Based on the science and action recommendations contained in the
report of the Xerces Society for Invertebrate Conservation Are Neonicotinoids Killing Bees?, the
Olympia Beekeepers Association has requested our assistance in implementing a restriction on
the purchase, sale, distribution and application of the neonicotinoid class of insecticides for
ornamental use to persons or entities with a valid WSDA pesticide applicator license. This class
of insecticide includes but is not limited to imidacloprid, clothianidin and thiamethoxan. This
will have no known impact on commercial agricultural use, as farmers are already required to
hold a valid applicators license to apply restricted use pesticides, nor on pet and other animal
applications of neonicotinoid-containing products.
Entomologists generally admit that honeybee colony collapse disorder involves many factors
including mites, viruses, poor nutrition, and exposure to a diverse array of pesticides and other
chemicals but the science also clearly demonstrates the sub-lethal effects of long-term
exposure to neonicotinoids on the ability of honeybees to forage and communicate. Even when
exposed to relatively low concentrations of these insecticides, honeybee workers can become
confused and disoriented, delaying or impairing their ability to return to their hive. Besides these
behavioral effects, chronic exposure to low doses of neonicotinoids can also reduce breeding
success, decrease metabolic efficiency, and reduce disease resistance. Because there is a great
deal of concern over the rapid decline of insect pollinators, both domesticated and wild, and
because the health of honeybee colonies is important for our state food security and economy, we
hope to take a precautionary approach with home ornamental use of neonicotinoid-containing
products, so as to minimize chronic exposure of honeybees to this class of compounds.
Building #1, Room 269, 2000 Lakeridge Drive SW, Olympia, Washington 98502-6045 (360) 786-5440
TDD (360) 754-2933
From:
To:
Subject:
Date:
Attachments:
Iain Kelly
Epstein, David
Recent Publications on Neonicotinoids
Monday, April 30, 2012 11:02:38 PM
BCS Statement on Henry et al 2012 final 2012 04 01-a.pdf
BCS Statement on Whitehorn et al. 2012 final 2012 04 01-a.pdf
BCS Statement on Pettis et al. 2012 CM 2012 01 20-final.pdf
BCS Statement on Tapparo et al 2012 03 25-CM final.pdf
BCS Statement on Krupke et al 2012-02-21 Final U S .pdf
BCS Statement on Lu et al 2012 final 2012 04 10.pdf
David, at the CLA Spring Conference, I said we were reviewing the recent studies on neonicotinoids.
Attached dare our considerations of them. Would appreciate any comments you have.
We also discussed your upcoming October meeting. Could you send me a draft agenda?
Many Thanks,
Regards, Iain
________________________________________
Iain Kelly
Bayer CropScience LP
Bee Health Team Lead
RESEARCH TRIANGLE PARK
Phone: +1 919-549-2552
Mobile: (b) (6)
E-mail: iain kelly@bayer.com
Web: http://www.bayer.com
The information contained in this e-mail is for the exclusive use of the intended recipient(s) and may be confidential, proprietary,
and/or legally privileged. Inadvertent disclosure of this message does not constitute a waiver of any privilege. If you receive this
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delete this e-mail and all copies and notify the sender. Thank you.
For alternate languages please go to http://bayerdisclaimer.bayerweb.com
Notes on the study of WHITEHORN et al. (2012)

http://www.sciencemag.org/content/early/recent / 29 March 2012 / 10.1126/science.1215025
Neonicotinoids pesticide reduces bumblebee colony growth and queen production

Penelope R. WHITEHORN1, Stephanie OCONNOR1, Felix L. WACKERS2 & Dave GOULSON1.
1School Natural Sciences, University of Stirling, Stirling, FK9 4LA, UK.
2Lancaster University, LEC, Lancaster, LA1 4YQ, UK
This is an interesting study that evaluated effects on bumble bee colony development from exposure
to Imidacloprid-contaminated diet. Replicate colonies of Bombus terrestris were fed with pollen and
nectar for two weeks under laboratory conditions. The colonies received ad libitum pollen and sugar
water; in the control group, sugar water and pollen were uncontaminated, in the treatment groups,
sugar water and pollen were spiked with 6 and 0.7 ppb or with 12 and 1.4 ppb Imidacloprid,
respectively. After two weeks of exposure in the laboratory, colonies were placed at a field location
remote from intensive pesticide use to forage freely and consume natural pollen and nectar for a
period of 6 additional weeks. The weight of the colonies was assessed each week and the number of
individual drones, workers, new queens, pupae and empty cells was assessed at the termination of
the study. All the colonies of all treatment groups developed and produced queens; weight
development was comparable between treatment and control during the exposure time (first two
weeks). From week 3 onwards, however, the control colonies gained more cumulative weight and
produced significantly more queens than the treatment colonies. Queen production in bumble bee
colonies can depend on colony size, with larger colonies producing more queens than small colonies,
so the authors conclude that the exposed colonies grew less than the control colonies due to effects of
Imidacloprid sublethal exposure, and therefore produced fewer queens.
Comments from the BCS Perspective:
1. The test design applied by WHITEHORN et al. (2012) is not validated; therefore it is not clear
whether the results presented would be reproducible at all. Experience with ecotoxicological study
designs for bees has shown that study validation is essential to assure generating scientifically
sound results.
2. The reported lower colony weight of treatment colonies compared to control colonies is basically
just a difference between different experimental groups; although there may be a statistically
significant difference in this endpoint, there is no evidence at all that this represents an adverse
effect, or, respectively, a biologically significant effect. In honey bees, for instance, hive weight
gain is predominantly determined by the quantity of nectar stores in the hive, which can be very
different between individual colonies even when set up at the same location under the same
environmental conditions, without indicating differences in colony vitality. Although bumblebees
do not have as extensive nectar stores a honeybees (as the authors note), B. terrestris does
indeed store nectar (see e.g. DORNHAUS & CHITTKA 2004, 2005), moreover a nest consists of many
other components (nesting material, pollen stores etc.) that influence its weight, so that the colony
weight parameter would not be very significant to deduce an adverse effect to the organisms of
the colony.
3. The number of workers per colony (i.e. the colony strength) at study termination was not
significantly different among the different treatment groups. Therefore the argument of the authors
that even a small drop in colony size may bring [the colony] below the threshold for queen
production is not very logical, as colony size is defined by number of individuals in the colony and
not by nest weight. In any case, there are no data available in the scientific literature that show
that queen production of a bumblebee colony is dependent on nest weight.
4. The differences in weight gain of colonies can have several causes, and this parameter is highly
variable. In a previous publication (GOULSON et al. 2002), one of the authors shows that changes
in weight of bumblebee nests situated in three different habitat types differs significantly
depending on their location and the associated available resources, but can also be influenced by
the presence of a parasite (Aphonimia socialia) in the colonies with lower weight gain. In the study
of WHITEHORN et al. (2012), no exact description of such alternative parameters that might likewise
influence colony weight development. One particularity that shows how variable this parameter
can be is the comparison of the values of net cumulative weight gain between the colonies used in
the previous study (GOULSON et al. 2002) and the current study: the hives that had the weakest
development gained around 400 g within 4 weeks in the older publication, whereas in the current
study the colonies that developed most strongly gained only 200 g within the same time span. This
variability in the endpoint of weight gain highlights again that the test design is not established and
validated, and drawing conclusions on the development of bumblebee colonies under the
influence of sublethal exposure concentrations of Neonicotinoids on the basis of the findings
presented here is very problematic.
5. How many new queens are produced by a bumblebee colony in one years cycle is a parameter
that is so far unpredictable and governed by processes and factors that are poorly understood
(DUCHATEAU et al. 2004, GOULSON 2006). Although the size of the colony, normally expressed as
the number of workers, may have an impact on when the production of queens is triggered in a
colony, it is not the only factor. For example, a study comparing the production of new queens and
drones between several colonies reared at different times shows that one of the main factors
affecting the production on new queens is the hibernation conditions of the founder queen
(DUCHATEU et al. 2004). In the study under discussion here, there is no mention of these factors,
and it is not clear at which point in the development cycle of the colonies the exposure took place.
Therefore it is quite possible that factors other than pesticide exposure, that were not assessed
and not taken into consideration, influenced the outcome of the study regarding the queen
production endpoint.
6. The authors indicate that they chose the low test concentrations (6 ppb in pollen and 0.7 ppb in
nectar) because this is the level found in oil-seed rape, however the reference they cited in
support (BONMATIN et al. 2003) did not include any original research measurements of residue
levels in oil-seed rape nectar and pollen, but instead reported the levels of 4.4 to 7.6 ppb in pollen
and 0.6 to 0.8 ppb in nectar that were determined in an unpublished study by SCOTT-DUPREE &
SPIVAK (2001). These data, which came from just two experimental test plots, are not broadly
representative of what bees encounter under conditions of commercial use. They represent high
end, rather than typical field concentrations. Residues of Imidacloprid in nectar and pollen of seedtreated crops like sunflower or oilseed rape are in most cases significantly lower, as outlined in
SCHMUCK et al. (2004) and MAUS et al. (2003) where a much higher number of residue data points
were evaluated: In sunflower crops, the Imidacloprid residue levels in nectar and pollen were in
all but one sample below the LOD of 1.5 ppb. Only one out of 18 analysed samples showed a
higher residue level of 1.6 ppb. In rape, residue levels between < 1.5 and 5 ppb were recorded in
the nectar and pollen samples. Only in one out of 15 analysed samples, a higher residue level was
detected (7.8 ppb in a pollen sample).
7. Furthermore, a continuous exposure to a contaminated diet over two weeks in a no-choice
scenario in the laboratory will in any case lead to exaggerated exposure conditions that are not
comparable to a situation as prevailing in the field.
Under realistic conditions, a bumblebee
colony, even when exposed to a highly attractive, seed-treated crop, would not source its
complete nectar and pollen supply exclusively from this culture over two full weeks.
Additional
food sources would be exploited as well (especially by bumblebees which only have a weakly
pronounced individual fixation or preference for certain types of flowers, and which do not
communicate with their nestmates to attract them to a certain type of flower). This would lead to a
significant dilution of residues in the colonys food stores. This is even true for a scenario as
outlined by WHITEHORN et al. (2012) where in a 10 x 20 km patch of land 100% of the area is in a 1
km radius of oilseed rape fields.
8. The authors indicate that no field studies have examined of the impact of Imidacloprid soilsystemic treatments to bumble bee colonies in the field. This is incorrect. TASEI et al. (2001) and
GELS & POTTER (2002) reported no effects on bumble bees for use of Imidacloprid as a sunflower
seed treatment and application to lawns containing clover, respectively, when the compound was
applied according to label directions. Foliar deposits applications not followed by irrigation (a
violation of the product label) were in contrast found to be hazardous to bumblebees by GELS &
POTTER (2002).
9. The authors suggest that based on their results the use of neonicotinoids may be having
considerable negative impact on wild bumblebee populations across the developed world. This is
a highly speculative statement. The authors do not adequately discuss the uncertainties inherent
in extrapolation of their study results, a main one being whether the exposure levels they tested
are representative of what bumble bees experience in real field scenarios. A critical assumption
they are making is that nectar concentrations that bumble bees are exposed to in the real world
are 6 ppb or greater since they did not test any lower concentrations. This assumption is based
on limited field data from one small-plot field study that did even include bumble bees. Other field
studies have found clearly lower levels of neonicotinoids in nectar and pollen of seed-treated
crops when evaluating a more extended pool of data (e.g. MAUS et al. 2003, SCHMUCK et al. 2004,
CUTLER & SCOTT-DUPREE, 2007).
10. Finally, there are several statements in the paper that are simply untrue or incorrect in the given
context. These include:
In the context of reviewing past bee studies of neonicotinoids, the authors state is unclear
what impact this exposure [to Neonicotinoids] has on bee colonies under field conditions.
In reality, it is quite clear that effects are not observed in the field. There are a plenty of
field studies available that investigate exactly this question and conclude no adverse
effects by exposure under realistic conditions (e.g. SCHMUCK & KEPPLER 2003, MAUS et al.
2003, SCHMUCK et al. 2004, CUTLER & SCOTT-DUPREE, 2007, NGUYEN et al. 2009, and
many more). That all these field data were largely ignored shows that the authors cited
quite selectively from the available literature.
The reference to 140 different crops treated with Imidacloprid suggests that the authors
apparently mix up seed treatment and spray treatments; the majority of these crops are
treated with spray formulations. Any spray application of Imidacloprid is prescribed to be
conducted out of the flowering period of the crop, so that an exposure of bees and
bumblebees can be a-priori be excluded when the application is done correctly.
The mention of pollen residue levels of Neonicotinoids (here: Clothianidin) up to 88 g/kg

refers to a recent publication of KRUPKE et al. (2012). This unique finding from one sample
is an extreme outlier in comparison to the many hundreds of pollen samples that have
been reported for the same compound in other studies (e.g. SCHMUCK & KEPPLER 2003,
LIEBIG et al. 2008 and BCS unpublished data). Therefore, the origin of the high residue
level in the aforementioned sample must be considered unclear and cannot necessarily be
attributed to systemic residues from seed treatment.
Conclusions
In conclusion it can be stated that the results presented by WHITEHORN et al. (2012) originate from a
study conducted under artificial conditions that may have resulted in higher exposures to Imidacloprid
than are likely to occur at real crop fields, and that the observed effects, besides being of questionable
reproducibility, may not necessarily be attributable to exposure to Imidacloprid. The conclusions drawn
by the authors are both speculative and at odds with the results of previous studies. The overall
weight of the currently available evidence does not support the authors conclusion that exposure to
Neonicotinoids under realistic field conditions may be causing widespread harm to bumblebee
populations.
References
BONMATIN, J.M., I. MOINEAU, R. CHARVET, C. FLECHE, M.E. COLIN & E.R. BENGSCH (2003): A LC/APCIMS/MS method for analysis of imidacloprid in soils, in plants, and in pollens. Analytical Chemistry
75: 2027-2033
CUTLER, G.C. & C. SCOTT-DUPREE (2007): Exposure to Clothianidin Seed-Treated Canola Has No
Long-Term Impact on Honey Bees. - Journal of Economic Entomology. 100: 765772
DORNHAUS, A. & L. CHITTKA (2004): Information flow and regulation of foraging activity in bumble bees
(Bombus spp.). - Apidologie 35: 183192
DORNHAUS, A. & L. CHITTKA (2005): Bumble bees (Bombus terrestris) store both food and information
in honeypots. - Behavioral Ecology, doi:10.1093/beheco/ari040: 661-666
DUCHATEAU, M.J., H.H.W. VELTHUIS, & J.J. BOOMSMA (2004): Sex ratio variation in the bumblebee
Bombus terrestris. - Behavioral Ecology 15: 7182
GOULSON, D. (2006): Bumblebees Their Behaviour and Ecology. Oxford University Press: 235 pp.
GOULSON, D., W.O.H. HUGHES, L.C. DERWENT & J.C. STOUT ( 2002): Colony growth of the bumblebee,
Bombus terrestris, in improved and conventional agricultural and suburban habitats. - Oecologia 130:
267273
LIEBiG, G., Th. KUSTERMANN & D. DE CRAIGHER (2008): Bee monitoring during and after the 2008
maize flowering season in the Rhine Valley (English translation of the German original report). Landesanstalt fr Bienenkunde, University of Hohenheim, Germany, December 2008: 37 pp.
SCOTT-DUPREE C. D. & M.S. SPIVAk (2001):- The impact of Gaucho and TI-435 seed-treated Canola on
honey bees, Apis mellifera L..- Unpublished Study Report 110405, April 11. 2001, University of
Guelph/University of Minnesota.
Dr. Maria Teresa ALMANZA, Dr. David L. FISCHER, Dr. Christian MAUS, 2012-04-01
Statement on the findings of the study:

TAPPARO et al. (2012): Assessment of the Environmental Exposure of Honeybees to Particulate
Matter Containing Neonicotinoid Insecticides Coming from Corn Coated Seeds
Authors: A. TAPPARO, D. MARTON, C. GIORIO, A. ZANELL, L. SOLDA, M. MARZARO, L. VIVAN, & V. GIROLAMI.
University of Padova, Padova, Italy
Environmental Science and Technology, DOI: 10.1021/es2035152
Contents of the publication

TAPPARO et al. (2012) report on results of field experiments that measured emissions of particulate matter
containing neonicotinoid insecticides from the sowing of dressed maize seeds and resulting potential
exposure levels for honey bees. Various types of treated corn seeds were sown into a test field using two
different types of pneumatic planters and the amount of total particulate matter and active ingredient
emitted into the air and deposited at various distances away from the planter or downwind edge of the
field were determined. The experiments were run with and without downward deflectors mounted on
planters air exhaust outlet. Two different types of experiments were performed: mobile sowing and
static sowing. In the mobile sowing experiments, the planters moved across the field as in normal maize
sowing practice. In static sowing experiments, the planter remained in a fixed place but processed seeds
as would normally occur during mobile planting. The seeds tested were commercial products of Pioneer
Hi-bred that were marketed in 2008, 2009 and 2010. All of these seed batches had Heubach dustmeter
measures of <3 g per 100 kg seed.
Insecticide concentrations in samples of exhausted air at the outlet of the air fan ranged from 3.39 to 12.0
mg/m3 and the mass of insecticide a.i. released per ha planted ranged from 0.43 to 1.53 g. The
percentage of the insecticide a.i. present on the seeds that was emitted in the planter air exhaust ranged
from 0.52 to 1.85%. Some differences were noted between different batches of seeds, for example
between Poncho 1250 seeds from 2009 and 2010. However, the authors indicate that all seed samples
emitted significant quantities of insecticide-laden particulate matter.
As part of the static sowing experiments, sugar syrup feeders and honey bee hives were placed so that
bees would fly directly through the air exhaust of the planter, and become powdered with any emitted
dust. After the static planter had been allowed to operate for 1 hour, individual bees that had flown
across the field were captured and subject to chemical analysis to determine the mass of insecticide on
their body. Likewise caged bees were placed for 30 s at distances of 1.00, 2.25, 4.50, 6.75 and 9.00
meters from the airflow emitted by the planter and then analyzed for insecticide load. The concentrations
measured in these individual bee samples were highly variable. The bees flying across the field had
insecticide loads ranging from 78 to >1000 ng/bee, and the caged bees had similarly high residue loads,
with a tendency for the exposure level to decrease with distance away from the air outlet. For comparison,
the authors cite the contact LD50 values for imidacloprid, clothianidin and thiamethoxam of 18, 22 and 30
ng/bee that were reported by IWASA et al. (2004) and suggest their measured residue levels were well
above the lethal level. The authors do not mention that these values are for bees dosed with a liquid
droplet of the a.i. using acetone as a carrier, and that penetration across the insect cuticle and the
resulting LD50 may differ greatly for a chemical applied as a dust.
Use of the deflectors greatly reduced the mass of particulate matter and insecticide sampled downwind
from the planter, but did not have a dramatic effect on the contact dose to individual bees that flew across
the field or were caged near the planter in the static sowing experiments.
The authors conclude that particulate matter released by drilling machines during sowing of maize seeds
coated with neonicotinoid insecticides represents a significant mechanism of environmental diffusion of
these insecticides. Bees flying over the sowing field and approaching the emission cloud of the drilling
machine can efficiently intercept the suspended particles being directly contaminated with an elevated
dose of insecticide, significantly higher than contact LD50 values. These exposures therefore represent a
concern for both apiculture and crop production based on bee pollination.
Comments from the BCS perspective
The publication of TAPPARO et al. (2012) is one out of several articles published by this group of authors
and to fully appreciate the significance of their data, it is necessary to also read their other papers (e.g.,
MARZARO et al. 2009, GIROLAMI et al. 2012). In prior studies, the authors investigated the possibility that
honey bees get into contact with lethal doses of neonicotinoid insecticides when they visit flowering plants
where deposition of abraded seed dust has occurred or by ingestion of guttation or dew droplets of the
same flowering plants. However, they found the concentrations and bee doses resulting from foraging on
such plants for pollen and nectar of flowers or for dew drops and guttation fluids were not high enough to
cause mortality. Drift of abraded seed dust to adjacent blooming plants could not explain the bee kill
events observed in Italy and which seemed to be associated with the planting of neonicotinoid-treated
maize seeds. Consequently, a new hypothesis was formulated, that bees obtain lethal doses by flying
through the dust cloud created during planting activities. The reasoning behind this hypothesis is
debatable. The authors state that exposure of bees from residues on vegetation surrounding drilled areas
cannot be the key route of exposure because residue levels of neonicotinoids found in such vegetation is
comparably low. Other authors (e.g. PISTORIUS et al. (2009), however, describe from the incident in the
Upper Rhine Valley in Germany symptoms that clearly hint to effects caused by contaminated nectar or
pollen that was stored in the affected hives. Therefore it appears questionable in how far the initial
hypothesis of the authors was correct.
In order to test the hypothesis that the acquisition of dust inflight is a significant source of bee
contamination, the authors designed and conducted new experiments. TAPPARO et al. (2012) present
planter emission data and individual bee exposure levels, however other papers present more clearly the
toxic responses of honey bees to these exposures (e.g., see MAZARO et al. 2009 and GIROLAMI et al.
2012). Upon reading these other studies, it becomes clear that bee deaths generally did not occur unless
the powdered bees were captured, brought into the laboratory and kept in conditions of high (>95%)
humidity. As stated by MARZARO et al. (2009): A clear indication that bees were killed by powdering, only
if held in high humidity, emerged. They did observe some individual bees killed in the field, but the level
of mortality under typical field conditions was low. Air humidity values of > 95% are, at least under climatic
conditions as prevailing in maize growing regions of the temperate zones, unusual; likewise, they are
higher than humidities commonly prevailing in bee hives (see e.g. ELLIS 2008).
The experiments of this research team demonstrate that abraded dust from neonicotinoid-treated maize
seeds is intrinsically very toxicity to honey bees, and bee deaths can occur under artificial scenarios set up
by the investigators. However, under normal agricultural and apicultural conditions, the sowing of
neonicotinoid treated seeds did not pose a serious risk.
That abraded dust from insecticide-treated maize seeds is highly toxic to honey bees was already well
known. Use of advanced seed coatings have been shown to significantly reduce abrasion of the a.i. from
maize seeds. Modification of planter exhaust systems to direct airflow downward toward the soil has been
shown to be very effective at reducing off-site drift. Ongoing product stewardship efforts continue to limit
this and other routes of potential exposure to bees. The occurrence of bee poisoning events are now rare,
and it is important to remember that even when such events have occurred, they have generally involved
a small proportion of the bees in a colony and had no long-lasting effect. Even in the case of the 2008
incident in southern Germany in which an extraordinarily high level of seed dust was released due to
improper coating of the treated seeds and over 12,000 bee colonies were affected, nearly all of these
colonies recovered (PISTORIUS et al. 2009). There is no scientific justification for suggesting, as do
TAPPARO et al. (2012), that abraded dust released during planting of neonicotinoid-treated maize seeds
represents a possible cause of declining bee populations or colony collapse disorder, is of concern for
crop production based on bee pollination, or is a widespread ecological problem requiring a rethinking of
agricultural policies. The work of this research team demonstrates that lethal exposure of honey bees to
abraded seed dust is only likely to occur under very specific and unusual conditions, and provides a basis
for further targeted efforts to limit the possibility of such occurrences. A more reasoned interpretation of
this and other recent papers on the same subject (e.g., KRUPKE et al., 2012) is that the problem of toxic
exposure of bees to corn seed dust is limited in scope, and likely correctable with improved seed
coatings/lubricants and planter modifications.
Correction of Technical Errors or Misleading Statements about Risk:

Several statements made in the paper are incorrect or highly misleading.
In the Introduction section it is stated:
the environmental releases of substances with recognized toxic and ecotoxic effects, such as
neonicotinoid insecticides that have been associated with the worldwide crisis of honeybee colonies
Several studies have investigated whether pesticides, amongst them neonicotinoids, are a significant
causative factor behind the decline of honeybee colonies. In the EFSA Scientific Report Bee Mortality
and Bee Surveillance in Europe (HENDRIKX et al. 2009) it is pointed out that no involvement of pesticides
has been proven for colony losses or CCD, and that High concentrations of pesticides have rarely been
identified in relation to colony losses in USA and Europe. In a survey of the French AFSSA (2009b),
pesticides were not among the key factors that were identified to be responsible for bee mortality; there
was no evidence found for a significant involvement of pesticides in the observed bee declines. In an
article published in Science, RATNIEKS & CARRECK (2010) point out that pests and diseases are the key
factors behind bee decline, and that pesticides are unlikely to have caused bee losses as they were
observed in the 1990s in France. These are just three examples of many examples that demonstrate that
the scientific community does, with a few exceptions, not associate honeybee colony decline with
pesticides.
In the Introduction section, it is further stated:
In the past decade honeybee colonies throughout the world have been subject to rapid losses in the
order of 40%, in particular in Southern Europe.
According to POTTS et al. (2010), the number of honeybee colonies in Mediterranean Europe has
increased by 13.3% during the last years. On a global level, numbers of colonies are likewise growing
rather than decreasing according to AIZEN & HARDER (2009). Therefore the figure of 40% losses may refer
to episodic events in certain countries or regions, but does not reflect a global trend nor even a regional
trend for Southern Europe.
In the Introduction section, TAPPARO et al. (2012) go on to state:

This phenomenon, also named colony collapse disorder, represents a worldwide crisis with effects both
on crop production and on ecosystems.
Colony Collapse Disorder is a phenomenon characterized by rather specific symptoms which is more or
less restricted to USA; bee decline or mortality reported from other countries and regions is usually not
associated with CCD-typical symptoms and in so far fundamentally different (see for instance HENDRIKX et
al. 2009,
VAN
ENGELSDORP et al. 2009,
VAN
ENGELSDORP & MEIXNER 2010). The authors are here mixing
up different phenomena. Moreover, it is a myth that the observed bee decline is globally affecting
agricultural crop production (e.g. AIZEN et al. 2008, AIZEN & HARDER 2009). There are no scientific data
that substantiate the assumption that bee decline so far factually affects agriculture.
In the Introduction section, TAPPARO et al. (2012) state:
In Italy and Europe, corn sowing from mid-March to May was often accompanied by a rapid
disappearance of foraging bees. [] a close relationship was observed between the deaths of bees and
the use of pneumatic drilling machines.
Apart from Italy, bee losses associated with maize drilling were only observed in Austria at a very low
level, and in Germany at one and in Slovenia at two episodic events. From other European countries such
observations have according to our knowledge never been made (see BARNETT et al. 2007, SEEFELD
2006, 2008, THOMPSON & THORBAHN 2009). In France, no cases of mortality caused by drilling of maize
seeds treated with neonicotinoids have been found during extensive multi-year monitoring efforts (AFSSA
2007, 2009a).
In the Results and Discussion section, it is stated:
Germany before the ban of neonicotinoids- and Austrian and Slovenian beekeepers continued to report
extended losses of bee colonies in spring in conjunction with corn sowing.
In Germany and Slovenia, bee mortality associated with maize drilling was only reported in one or two,
respectively, individual incidents. In Austria, only very few cases of increased mortality were reported.
Colony losses associated with maize drilling have only very rarely been reported even in the scopes of the
few incidents referred to in these countries (PISTORIUS et al. 2009, GIRSCH & MOOSBECKHOFER 2011,
MAROLT et al. 2011, SEEFELD 2006, 2008, THOMPSON & THORBAHN 2009).
In the section on Analytical Methods for Single-Bee Analysis after Field Exposure, it is stated:
Short-term mortality and the characteristic symptoms of neonicotinoid neurotoxicity []
Symptoms seen in bees that had been killed by neonicotinoids are not specific to this class of compounds
(or not even specific to pesticide intoxication at all), so there is no way to diagnose neonicotinoid
intoxication by means of externally visible symptoms found in dead bees.
Conclusion
TAPPARO et al. (2012) present results of field experiments that demonstrate that honey bees that fly
through the air exhaust of pneumatic corn planters can become contaminated with abraded dust from
insecticide-treated maize seeds and this can sometimes result in the death of individual bees. However,
their research results and the available records of field incidents suggest that the problem of toxic
exposure of bees to corn seed dust is limited in scope, and continues to be minimized with improved seed
coatings/lubricants, planter modifications and product stewardship measures. This phenomenon has not
been scientifically linked to, and is not suspected by mainstream scientists to be the cause of colony
collapse disorder or widespread honey bee colony losses.
References
AFSSA (2007) : Afssa-saisine n 2007-SA-0393 dossier li n2007-3845-Cruiser 20 dec 2007. Avis de

l'Agence franaise de scurit sanitaire des aliments relatif aux conclusions de l'valuation de la
prparation Cruiser concernant le risque long-terme pour les colonies d'abeilles. 9 pp.
AFSSA (2009a) : Afssa-dossier n2009-1235-Cruiser 350 1 dec 2009. - Avis de l'Agence franaise de
scurit sanitaire des aliments relatif une demande d'autorisation de mise sur le march de la
prparation Cruiser 350 base de thiamthoxam de la socit Syngenta Agro SAS 31pp.
AFSSA (2009b): Weakening, collapse and mortality of bee colonies.: 222 pp.
AIZEN, M.A., L.A. GARIBALDI, S.A. CUNNINGHAM & A.M. KLEIN (2008): Long-Term Global Trends in Crop
Yield and Production Reveal No Current Pollination Shortage but Increasing Pollinator Dependency. Current Biology 18, 15721575
AIZEN, M.A. & L. HARDER (2009): The truth about the disappearing honeybees. New Scientist 2731: 3 pp.
BARNETT, E.A. A.J. CHARLTON & M.R. FLETCHER (2007) Incidents of bee poisoning with pesticides in the
United Kingdom, 19942003. - Pest Management Science 63:10511057
ELLIS, M.B. (2008): Homoeostasis Humidity and Water Relations in Honeybee Colonies (Apis mellifera).Dissertation, University of Pretoria, South Africa: 126 pp.
GIROLAMI, V., M. MARZARO, L. VIVAN, L. MAZZON, M. GREATTI., C. GIORIO, D. MARTON & A. TAPPARO (2011):
Fatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implication.
Journal of Applied Entomology. -. doi: 10.1111/j.1439-0418.2011.01648.x
GIRSCH, L. & R. MOOSBECKHOFER (2011): Untersuchungen zum Auftreten von Bienenverlusten in Maisund Rapsanbaugebieten sterreichs und mglicher Zusammenhnge mit Bienenkrankheiten und dem
Einsatz
von
Pflanzenschutzmitteln
(Projekt-Akronym:
MELISSA).
Vierter
Zwischenbericht.
https://www.dafne.at/prod/dafne_plus_common/attachment_download/daf1759bdaa879
85a4b448c3807dfcc7/MELISSA_Vierter_Zwischenbericht_14_09_2011.pdf: 44 pp.
HENDRIKX, P., M.-P. CHAUZAT, M. DEBIN, P. NEUMANN, I. FRIES, W. RITTER, M. BROWN, F. MUTINELLI, Y. LE
CONTE & A. GREGORC (2009): Scientific Report Submitted to EFSA : Bee Mortality and Bee Surveillance in
Europe: 217 pp.
KRUPKE, C.H., G.J. HUNT, B. EITZER, G. ANDINO & K. GIVEN (2012): Multiple routes of pesticide exposure
for honey bees living near agricultural fields. PLoS ONE 7(1): e29268. doi.10.1371/journal.pone.0029268
MAROLT, P., Z. LOTREK & S.D. MILANOVI (2011): Report on bee declines in the Mura Region and other
parts of Slovenia in the period from 17 April to 30 May 2011. Media Release, Republic of Slovenia,
Ministry of Agriculture, Forestry and Food, Inspectorate of the RS for Agriculture, Forestry and Food.
17.06.2011: 12 pp.
MARZARO, M., L. VIVAN, , A. TARGA, L. MAZZON, N. MORI, M. GREATTI, E. PETRUCCO TOFFOLO, A. DI
BERNARDO, C. GIORIO, D. MARTON, A. TAPPARO & V. GIROLAMI (2011): Lethal aerial powdering of honey
bees with neonicotinoids from fragments of maize seed coat. - Bulletin of Insectology 64: 118125.
PISTORIUS, J., G. BISCHOFF U. HEIMBACH, & M. STHLER (2009): Bee poisoning incidents in Germany in
spring 2008 caused by abrasion of active subtances from treated seeds during sowing of maize. - Julius
Khn-Archiv 423: 118-126.
POTTS, S.G., S.P.M. ROBERTS, R. DEAN, G. MARRIS, M.A. BROWN, R. JONES, P. NEUMANN & J. SETTELE
(2010): Declines of managed honey bees and beekeepers in Europe. Journal of Apicultural Research
49: 15-22
RATNIEKS, F.L.W. & N.L. CARRECK (2010): Clarity on Honey Bee Collapse? - Science 327: 151-152
SEEFELD, F. (2006): Chemical detection of damage to honey bees caused by pesticides. - Nachrichtenblatt
des Deutschen Pflanzenschutzdienstes, 58: 5966
SEEFELD, F. (2008): Chemische Untersuchungen zur Aufklrung von Schadensfllen an Honigbienen
durch Pflanzenschutzmittel im Zeitraum 1985 bis 2006. - Mitteilungen aus dem Julius Khn-Institut 418: 1150
TAPPARO, A., D. MARTON, C. GIORIO, A. ZANELLA, L. SOLDA, M. MARZARO, L. VIVAN, & V. GIROLAMI (2012):
Assessment of the Environmental Exposure of Honeybees to Particulate Matter Containing Neonicotinoid
Insecticides Coming from Corn Coated Seeds.
Environmental Science and Technology. -, doi:
10.1021/es2035152
THOMPSON, H.M. & D. THORBAHN (2009): Review of honeybee pesticide poisoning incidents in Europe
evaluation of the hazard quotient approach for risk assessment. - Julius-Khn-Archiv 423: 103-108
VAN ENGELSDORP, D., J.D. EVANS, C. SAEGERMAN, Ch. MULLINS, E. HAUBRUGE, B.K. NGUYEN, M. FRAZIER, J.
FRAZIER, D. COX-FOSTER, Y. CHEN, R. UNDERWOOD, D. TARPY & J.S. PETTIS (2009): Colony Collapse
Disorder: A Descriptive Study. PLoS ONE 4: doi:10.1371/journal.pone.0006481
VAN ENGELSDORP, D. & M.D. MEIXNER (2010): A historical review of managed honey bee populations in
Europe and the United States and the factors that may affect them. - Journal of Invertebrate Pathology
103: S80S95
Dr. David L FISCHER, Dr. Andrew CHAPPLE, Dr. Iain KELLY, Dr. Lubos VRBKA & Dr. Christian MAUS
2012-03-25
PETTIS et al. (2012): Pesticide Exposure in Honey Bees Results in Increased Levels
of the Gut Pathogen Nosema
Naturwissenschaften, DOI 10.1007/s00114-011-0881-1

In the recently issued publication of PETTIS et al. (2012), interactions between chronic, sublethal exposure
of honeybee colonies to Imidacloprid, and the infection of individual honeybees with the fungal gut
parasite Nosema are investigated.
Three treatment groups were set up in the study, each consisting of ten bee hives. On group was fed with
artificial diet containing 20 ppb Imidacloprid, the second with 5 ppb Imidacloprid, and the third remained
untreated as control group. Exposure time was 10 weeks. After 5 weeks, brood combs were removed, and
newly emerged young bees were infested with Nosema spores (ca. 330,000 spores per bee). Mortality of
the infested bees was recorded, and after 12 days, Nosema spore level was determined for each
individual bee. In a second trial, bees that emerged from combs taken out of exposed colonies after 8
weeks were infested with two different doses of Nosema spores (ca. 330,000 and 33,000 per bee) in the
same experimental setup.
In none of the experiments, an increased mortality rate was observed in any treatment group, mortality
always remained below 20%. In the first trial, bees from colonies chronically exposed to Imidacloprid had
higher Nosema spore counts (both treatment groups ca. 700,000 spores/bee) than bees from the control
group (ca. 200,000 spores/bee). In the second trial, initial dosage of bees with spores had no effect on the
eventual infestation level, but bees from control colonies had lower levels than bees from Imidaclopridexposed colonies. However, there was no dose-response relationship in spore counts, and differences
between treatment and control were less pronounced than in the first trial (control: ca. 1,000,000
spores/bee; 5 ppb: ca. 1,750,000 spores/bee; 20 ppb: ca. 1,500,000 spores/bee). At the end of the trials,
eight of the thirty experimental colonies were found infested with Nosema (by means of natural infection),
but there was no correlation between frequency and severity of infestation, and Imidacloprid exposure:
three control colonies (avg. spore counts 4,300,000 spores/bee), three colonies of the 5 ppb group (avg.
spore count 2,900,000 spores/be), and two colonies of the 20 ppb group (avg. spore count 500,000
spores/bee) showed Nosema infestations.
From the reported findings, the authors conclude an interaction between sub-lethal exposure to
Imidacloprid at the colony level and Nosema spore production in individual bees, and postulate that
sublethal exposure of honeybee colonies to pesticides may cause adverse effects by making them more
susceptible to pathogens, that have so far been overlooked in the pesticide risk assessment.

The study of PETTIS et al. (2012) appears technically well conducted and well reported. It is common
sense that multiple stressors may interact with each other, and that an organism exposed to a certain
stressor may be more susceptible of the effects of other stressors. In so far, the reported results as such
do not appear implausible. Nevertheless, there are some aspects to consider when drawing conclusions
from the results of the study.
Although the exposure to Imidacloprid took place under field conditions with entire bee colonies, the
Nosema infestation and exposure part of the study was conducted under artificial laboratory
conditions with individual worker bees out of the context of the colony and its complex interactions and
compensation mechanisms. In such an artificial laboratory environment, bees may react quite different
from a situation under realistic field conditions. There were already many cases where a sublethal
stressor was shown to induce certain effects in the laboratory, which could then, however, not be
recovered under field conditions, or where sublethal effects that were seen in the laboratory proved
not to be biologically relevant under realistic conditions. Therefore, the results of the study referred to
here do not provide a proof of an adverse effect to bee colonies by the exposure to sublethal doses of
a neonicotinoid (although this is implied in the paper), but at the utmost indicates an intrinsic effect
potential. There is no evidence that this could cause a hazard to bee colonies under realistic
conditions.
This is further supported by the observations of PETTIS et al. (2012) regarding the study colonies that
remained in the field and were the source for the combs for emergence of the bees for the laboratory
part of the study. There was not only no positive correlation between Imidacloprid exposure and
natural Nosema infection in terms of number of infested colonies, but the infested control colonies had
by far the highest infestation levels, followed by the colonies exposed to low Imidacloprid
concentrations, and the lowest spore counts were recorded in the colonies exposed to the highest
pesticide concentration. This once more underlines the fact that field conditions are fundamentally
different from what we can test in the laboratory, and that laboratory data can not be 1 : 1 extrapolated
to the field.
The endpoints measured in the reported study, like Nosema infestation are complex and influenced by
plenty of partly unknown factors; no standards have been defined so far, and little is known about the
intrinsic variability of the endpoints. This is for instance mirrored by the fact that in the first experiment
the infestation with 330,000 spores/bee consistently resulted in a spore level of 700,000 spores/bee,
whereas in the second trial the infestation with just 1/10th of the spores lead to final spore levels of
more than 2,000,000/bee, with similar levels in bees originally infested with 330,000 spores/bee. This
complete lack of a dose-response relationship underlines the high intrinsic variability of the endpoint
and makes it extremely different to distinguish true correlations from erratic findings.
Before concluding on any consistent and relevant synergistic effect, the reproducibility of the reported
findings has to be demonstrated. Findings of a higher sensitivity of honeybees exposed to sublethal
concentrations of Imidacloprid to Nosema infestation has also been reported in another laboratory
study (ALAUX et al. 2009), but a third study from the Bee Institute of Celle/Germany, did not find
interactions between sublethal exposure to Imidacloprid and a challenge with Nosema infestation
(WEHLING et al. 2006, 2009). Likewise, the observation of PETTIS et al. (2012) that individual bees from
the treatment groups exposed to Imidacloprid were more severely infested with Nosema than the
control groups are in contradiction with the conclusion of ALAUX et al. (2009) that Imidacloprid may
have a slight suppressing effect to Nosema (yet this seems to be confirmed again by the field colony
data from PETTIS et al. 2012). These inconsistencies clearly point at the fact that for testing of
sublethal effects and of multiple stressor effects to honeybees there are no fully technically mature
and validated test designs available so that it is not surprising that study results may be inconsistent
and not reproducible.
Another point that should be emphasized is the fact that in none of the treatment groups there was
any increased mortality observed. This demonstrates that vitality of bees originating from colonies
chronically exposed to Imidacloprid at levels up to 20 ppb is not negatively affected, even not under
aggravated conditions like an artificial infestation with Nosema. This confirms the established chronic
field NOAEC for Imidacloprid at 20 ppb.
Finally, the hypothesis that sublethal exposure to pesticides makes bees more susceptible to diseases
or parasites under field condition is contradicted by the findings of several field monitoring projects
where the occurrence of pathogens is surveyed as well as the exposure to pesticides under realistic
field conditions (e.g.
VAN
ENGELSDORP et al. 2009, CHAUZAT et al. 2010a, b, GENERSCH et al. 2010,
HIGES et al. 2010). None of the mentioned studies makes mention of any correlation between
infestation with certain pathogens and the exposure to pesticide residues, or between findings of
pesticide residues and increased colony mortality, as it would have to be expected if the hypothesis
would be true. The fact that no correlation between pesticide exposure and honeybee colony mortality
is found does obviously not support the hypothesis of PETTIS et al. (2012) that interactions between
pesticides and pathogens might be a major contributor to increased mortality of honey bee colonies
worldwide, and their concern that there might in terms of this be major gaps in the existing testing and
risk assessment procedures for pesticides and their effects to honey bees.
In summary, it can be stated that the study of PETTIS et al. (2012) does not convincingly substantiate the
assumption of any adverse effects of the exposure of honeybees to sublethal doses of Imidacloprid in
combination with other stressors like diseases or pathogens under realistic exposure conditions in the
field.
References
ALAUX, C., J.L. BRUNET, C. DUSSAUBAT C, F. MONDET F, S. TCHAMITCHAN, M. COUSIN, J. BRILLARD, A. BALDY,
L.P. BELZUNCES & Y. LE CONTE (2010): Interactions between Nosema microspores and a
neonicotinoid weaken honeybees (Apis mellifera). - Environmental Microbiology 12:774782
CHAUZAT, M.P., P. CARPENTIER, F. MADEC, S. BOUGEARD, N. COUGOULE, P. DRAJNUDEL, M.C. CLMENT, M.
AUBERT & J.P. FAUCON (2010a) : The role of infectious agents and parasites in the health of honey
bee colonies in France. - Journal of Apicultural Research 49: 31-39
CHAUZAT, M.P., A.C. MARTEL, S. ZEGGANE, P. DRAJNUDEL, F. SCHURR, M.C. CLMENT, M. RIBIRE-CHABERT,
M. AUBERT & .P. FAUCON (2010b): A case control study and a survey of mortalities of honey bee
colonies (Apis mellifera) in France during the winter of 2005-06. - Journal of Apicultural Research
49: 40-51
GENERSCH, E., W.
VON DER
OHE, H. KAATZ, A. SCHROEDER, Ch. OTTEN, R. BCHLER, S. BERG, W. RITTER,
W. MHLEN, S. GISDER, M. MEIXNER, G. LIEBIG & P. ROSENKRANZ (2010a): The German bee
monitoring project: a long term study to understand periodically high winter losses of honey bee
colonies. - Apidologie 41: 332-352
HIGES, M., R. MARTIN-HERNNDEZ, A. MARTNEZ-SALVADOR, E. GARRIDO-BAILN, A.V. GONZLEZ-PORTO, A.
MEANA, J.L. BERNAL, J.
DE
NOZAL & J. BERNAL (2010): A preliminary study of the epidemiological
factors related to honey bee colony loss in Spain. - Environmental Microbiology Reports 2: 243250
PETTIS, J.S., D.
VAN
ENGELSDORP, J. JOHNSON & G. DIVELY (2012): Pesticide exposure in honey bees
results in increased levels of the gut pathogen Nosema. Naturwissenschaften, DOI

10.1007/s00114-011-0881-1
VAN ENGELSDORP D., J.D. EVANS, C. SAEGERMAN, Ch. MULLIN, E. HAUBRUGE, B.K. NGUYEN, M. FRAZIER, D.
COX-FOSTER, Y. CHEN, R. UNDERWOOD, D.R. TARPY & J.S. PETTIS (2009): Colony Collapse Disorder:
A Descriptive Study. PLoS ONE 4(8): e6481. doi:10.1371/journal.pone.0006481
WEHLING, M., W. VON DER OHE, D. BRASSE & R. FORSTER (2006): Intoxication of honeybees Interactions
of plant protection products and other factors. Proceedings of the Second European Conference
of Apidology, EurBee, Prague (Czech Republic), 10.-16. September, 2006: 79
WEHLING, M., W.
VON DER
OHE, D. BRASSE & R. FORSTER (2009): Colony losses interactions of plant
protection products and other factors. Julius Khn-Archiv: 423: 153-154
Dr. Christian MAUS, 2012-01-27

LU et al. (2012): In situ replication of honey bee colony collapse disorder
Authors: Ch. LU, K.M. W ARCHOL & R.A. CALLAHAN

Harvard School of Public Health, Boston/USA
Worchester County Beekeepers Association, Massachusetts/USA
Bulletin of Insectology 65 (1)
In their publication In situ replication of honey bee colony collapse disorder, LU et al. (2012) describe a
trial in which they claim they have replicated inducing symptoms of Colony Collapse Disorder (CCD) by
chronically exposing bee colonies to high-fructose corn syrup (HFCS) contaminated with Imidacloprid, and
bring forward a new hypothesis about the origin of CCD. The authors hypothesize that CCD is caused by
Imidacloprid residues originating from seed treatment in corn in HFCS which is used to feed honeybee
colonies. In order to verify this hypothesis, they set up the following trial design: In each of four different
apiaries, five commercial colonies were set up, four were fed with HFCS containing Imidacloprid at
different concentrations, the fifth received uncontaminated HFCS and served as control colony. The
colonies of the treatment groups were first exposed to a lower Imidacloprid concentration for 4 weeks,
followed by a higher exposure concentration for subsequent 9 weeks. The exposure concentrations of the
different treatment groups were 0.1 + 20 g/kg, 1.1 + 40 g/kg, 5.3 + 200 g/kg, and 10.5 + 400 g/kg.
Treatments were repeated weekly between July and September 2010. In this period, hives were assessed
weekly, with bi-weekly brood assessments. Further weekly hive assessments followed in the time period
between December 2010 and March 2011. At the end of the assessment period all colonies of the two
higher treatment group and the 20 g/kg treatment group, three out of four colonies of the 40 g/kg group,
and two out of four colonies of the control group were found dead. From this observation, the authors
conclude that the observed mortality, which they attribute to exposure to Imidacloprid, demonstrate that
Imidacloprid residues in HFCS are a plausible mechanism to explain CCD.

It is obvious that the study design applied by LU et al. (2012) suffers from many flaws, with regard to the
set-up of the trial as well as regarding the context in which it was conducted. Moreover, many of the
conclusions drawn from the findings are highly questionable. In the following, the most critical points are
listed and discussed.
Trial Design Replication. In ecotoxicological bee testing, especially when entire honeybee colonies are
subject of the test, the choice of a suitable design is of key importance for obtaining scientifically solid
results. An important aspect of this is an appropriate replication, especially since a bee colony is a highly
complex meta-organism, a fact which entails a significant natural variability in almost all testing endpoints
that may be measured in such a study. The numbers of replicates that are needed to appropriately
address a certain endpoint depend largely on the complexity and intrinsic variability of the endpoint to be
measured. For a relatively simple endpoint like mortality or foraging activity, relatively low replicate
numbers like three or four, as normally used in semi-field tests, are commonly considered appropriate.
However, this cannot be applied to the study under discussion here. One of the most complex endpoints
one could think of is overwintering success and overwintering mortality of bee colonies an endpoint that
depicts the upshot of a long, complex process that is influenced by numerous, partly interdependent
variables and factors, many of which are not even known to us. To address this kind of endpoint with a
relatively low number of replicates, as LU et al. (2012) did, (only four hives per treatment group!) seems
hardly appropriate. Therefore it is questionable in how far their design is at all capable of detecting
significant differences between different experimental groups in the endpoint overwintering mortality. The
authors seem to be aware of this as they call this weakness of their study design an apparent deficiency.
It remains the question then: why do they nevertheless draw conclusions from a test conducted under an
obviously flawed design? In this context, it is likewise notable that the authors apparently did not conduct a
statistical analysis of their colony mortality data, as would be expected in a solid scientific study.
In addition to the low numbers of colonies of the individual treatment groups that actually do not allow
drawing conclusions from the outcome of the study, similarly the dose-response relationship in colony
mortality that the authors claim to see, is rather doubtful: in the 20 g/kg exposure group, mortality set in
earlier than in the 40 g/kg as well as in the 200 g/kg treatment group, and reached higher levels than in
the 40 g/kg group. This is not consistent with the assumption of a dose-response relationship. Likewise,
the authors state that they have found that the initial brood rearing corresponded to imidacloprid doses
two weeks after the initial imidacloprid dosing, however, it is inversely related to imidacloprid dosages at
the end of dosing regime, however, they then admit that the decrease [of brood cells during the
observation period] is independent of different Imidacloprid doses applied to the hives. According to the
graph sown in Figure 1, there is no obvious or significant dose-response relationship in the abundance of
brood cells at all values fluctuate, as typical for this endpoint, over time, with sometimes the control
group, sometimes a treatment group (in particular the 20 g/kg and the 40 g/kg groups) having highest
abundances of brood cells. Towards the end of the season, brood abundance decreases in all treatment
groups, which is a natural phenomenon related to the generation cycle of a bee colony. During this period,
measurements of brood abundance will anyway lead to erratic figures, so there is no sense in making
comparisons between observations on the development of this endpoint in different treatment groups
during this time of the year.
Another point that raises some doubt that the test design as used by LU et al. (2012) would be capable of
reliably detecting treatment effects and yielding anything else but erratic results, is the following: there is
no doubt that dietary Imidacloprid concentrations of 400 or even of 200 g/kg are hazardous to bees,
especially when chronically administered to a colony. When a colony is exposed to such concentrations
over many weeks, one should expect that there would be effects of this visible. In so far it is surprising that
apparently no such effects were seen at all during all the exposure period, and that first signs of
treatment-related colony mortality only set in 13 weeks after exposure. This suggests that the test design
was not sufficiently sensitive to detect any treatment-related effects, and the distribution of the observed
mortality over the different treatment groups was just erratic.
Exposure of Bee Colonies to Neonicotinoids. In a sound scientific approach, it would have been the
logical procedure to first gather information about the nature of a realistic exposure scenario, before
simulating this scenario in a trial. In the given case, this would have meant evaluating what residue levels
of Imidacloprid would normally be present in HFCS, and then defining the exposure levels to be tested in a
study on the basis of these realistic exposure levels. However, apparently the authors had no information
available about potential residue levels in HFCS, and instead of determining a realistic exposure scenario
by conducting residue analyses in commercially available HFCS samples, they based the exposure levels
tested in their study on pure guesses which are completely unsubstantiated. They argue that the
maximum residue level of Imidacloprid in corn as set by US EPA is 50 g/kg. As there is no maximum
residue level set for HFCS, they arbitrarily assume that residue levels in HFCS are the ten-fold maximum
tolerated level for corn grain, from which HFCS is processed. First, deducing an anticipated, common
environmental exposure concentration from a maximum tolerated residue level is absurd and not in
compliance with any scientifically sound principle. Second, a ten-fold extrapolation factor for a product
which is even not processed in a concentration process (see below) is by no means justified (analogy: this
would be like assuming that each pedestrian walking on the sidewalk along a street with a 100 km/h
speed limit would move there with a speed of 1000 km/h the speed limit is basically valid for cars, so
other entities may move at much higher speeds, even though common sense suggests that they would
not do so).
Another point which is very questionable related to the authors assumption that there were significant
Imidacloprid residues in HFCS refers to the following consideration: if their assumption was true that there
is widespread occurrence of residue levels of Neonicotinoids in HFCS, why did they then not analyze the
HFCS they used for Neonicotinoid residue levels just to determine these levels, and why did they then
have to spike it with Imidacloprid at all if their hypothesis was correct, then residues of the compound
would already have been in there, and spiking it again would have been double dosing. Then, if there
would be significant residue levels of Imidacloprid in commercially available HFCS, why did the authors
then find no residues in their analysis of the blank sample fed to their control hives (Table 2)? Implicitly,
the authors seem to suggest that a problem with Imidacloprid residues in HFCS must have been in
particular in older batches produced in 2005/06, as they point out that they were not able to obtain HFCS
manufactured during this years, so they used food-grade HFCS fortified with different levels of
Imidacloprid, mimicking the levels that are assumed to have been present in the older HFCS. This
approach is lacking any logical coherence if a significant residue level of Imidacloprid was present in
HFCS in 2005/06, but no more nowadays, how can the incidences of CCD symptoms that are still
reported in more recent years, be attributed to Imidacloprid residues in HFCS? Moreover, the authors give
no explanation why in the framework of their hypothesis Imidacloprid residues in HFCS should have been
different between 2005/06 and nowadays.
Then, even if there were Imidacloprid residues in HFCS as the authors hypothesize, the exposure
scenario as tested would not be realistic: in apicultural practice, no bee colony would be fed with HFCS all
season long. In so far, exposure conditions as applied here would be strongly exaggerated in any case.
Whatever assumptions about residues of Neonicotinoids may be present in HFCS might have been made
by the authors, it seems, in contrast to their hypotheses, to be a matter of fact that HFCS contains no
Neonicotinoid residues at all. In 2009, USDA analyzed 12 HFCS samples of different origins for pesticide
residues; these residue analyses screened for ca. 200 active ingredients; the detection limit for
Imidacloprid was 1 g/kg. No residues of Imidacloprid or other Neonicotinoids were found (Roger
Simonds, USDA Agrimarketing Service, Gastonia, North Carolina, personal communication). Therefore, it
seems very unlikely that residues of Imidacloprid or other Neonicotinoids are prevalent in HFCS.
That no Imidacloprid residues are found in HFCS that is produced from seed-treated corn is not surprising
when considering the process in which this commodity is usually produced: Corn grain is converted to
corn syrup with several production steps. First, the grain is wet milled to produce corn starch. The starch is
taken through three separate enzymatic conversions to break the starch into oligosaccharides, then to
hydrolyze the oligosaccharides to glucose, and finally to isomerize the glucose to a glucose/fructose
mixture. The raw corn syrup is then purified with activated carbon. Even if Imidacloprid residues that might
potentially be present in the grains would not be degraded in the maceration process, they would
ultimately be removed from the syrup by final activated carbon purification. Moreover, there is no step in
this production process in which Imidacloprid could be concentrated. Therefore, even if there would be
residues in HFCS, they would be lower rather than higher than those that might be found in corn grain.
Another point to justify the tested concentrations that the authors are bringing forward is a reference to a
paper of GIROLAMI et al. (2009) who found Imidacloprid residue levels of 47 mg/kg in guttation liquid from
seedlings of Imidacloprid seed-treated maize plants. It is not in any way reasonable to compare residue
levels in xylem liquid of young seedlings (this is where guttation fluid originates from) with residue levels in
processed products originating from fruits from mature plants in which the substance used for seed
treatment has been massively diluted and degraded. Moreover, it has been convincingly demonstrated
that guttation liquid is not normally used by bee colonies as relevant water source (KEPPLER et al. 2010,
PISTORIUS et al. in press), and even in cases where individual bees might be picking up guttation fluid, this
would not lead to a long-term exposure of the colonies as it was in the design of the study of LU et al.
(2012). The authors state then that the finding of the loss of honey bee hives at the levels as low as 20
g/kg of imidacloprid in HFCS raises the question of whether there is a no observed- adverse-effect-level
of imidacloprid (and most likely of other neonicotinoids as well) for honey bees. This statement is
erroneous: A NOAEC for Imidacloprid has been established in numerous honeybee studies under fieldrelevant conditions (see for instance MAUS et al. 2003, SCHMUCK et al. 2005). That the authors were not
able to determine a NOAEC in their study may on one hand be related to the fact that the described
experiment was probably not capable of establishing a robust NOEC for the endpoint overwintering
mortality due to flaws of the design (see above). On the other hand, the authors tested, compared to
environmental exposure levels, excessively high dietary concentrations: even the lowest exposure level
tested (20 g/kg) is by far higher than the residue levels that are normally found in nectar and pollen of
seed-treated crops (see for instance MAUS et al. 2003, SCHMUCK et al. 2005), and the highest
concentrations tested by LU et al. (2012) were hundred-fold and more overdosed compared to typical
environmental concentrations.. The authors argue that the bees of the test colonies would have reduced
the concentration of Imidacloprid in their food supply by diluting the offered HFCS with nectar collected
from nearby floral resources, but to reach realistic exposure levels, even the lowest test concentration
would have to be diluted by a factor of four to ten, which is, under consideration of the season when
exposure took place (end of July to end of September when natural food sources for bees tend to be
scarce), highly unlikely. A chronic dietary exposure to residue levels as high as 20 g/kg, as tested in the
study under discussion here is therefore a scenario that would not occur under realistic agricultural
conditions. Interestingly, in an earlier study on overwintering success of bee colonies exposed to
Imidacloprid (FAUCON et al. 2005), where environmentally more relevant residue levels (0.5 and 5 g/kg)
were tested with more appropriate replicate numbers (8 to 9 per treatment group), no adverse effects to
the exposed hives were found.
Another debatable point regarding the dosing regimes applied in the study under discussion here is why
the authors first applied low exposure concentrations between 0.1 and 10.5 g/kg which, at least the lower
concentrations, may come close to what a bee colony may be exposed to in the field, but then after a few
weeks switched to at least partly dramatically exaggerated rates. There seems no be no reasonable
rationale behind this, and the authors likewise do not justify this unusual dosing regime.
Correlations between colony mortality and the use of Neonicotinoids. The authors claim that the first
significant occurrence of CCD in US in 2006/07 was correlated with the introduction of neonicotinoid
insecticides as seed treatment in corn in 2004/05. This, again, is a statement which is based on several
misconceptions and errors: 1.) Imidacloprid as a seed treatment in corn was brought on the market in US
in 2000, and was first used there during the planting season 2001. 2.) Imidacloprid seed treatment in corn
was initially only applied on a very limited acreage in US, and after two years on the market, it was hardly
used any more, being replaced by other products. During the years 2004 to 2011, the percentage of US
corn acres treated with Imidacloprid has been less than one-half of one percent (BCS, unpublished data).
Therefore it is ridiculous to assume that after market introduction of Imidacloprid in corn, Imidacloprid
residues might have been prevalent in HFCS produced in US, and the claimed correlation is completely
unsubstantiated.
If there would exist a causative link between the use of Neonicotinoids and honeybee colony mortality,
one should see a correlation between use of Neonicotinoids and exposure of bees to Neonicotinoids on
one hand, and colony losses on the other hand. However, this is not the case at all. On the contrary, CCD
occurrence and other colony losses that have been observed at large scales are not correlated with
exposure of honey bee colonies to Neonicotinoids (VAN ENGELSDORP et al. 2009, DELAPLANE 2012) or to
exposure of colonies to Neonicotinoid-treated crops (e.g. OTTEN 2003a, b, CHARRIRE & NEUMANN 2010).
Linkage of Neonicotinoid exposure to declining bee colony health and elevated colony losses has not
been found in any of the recent regional multifactorial studies of declining bee health (VAN ENGELSDORP et
al. 2009, 2010a, ROGERS & KEMP 2004, NGUYEN et al. 2009, CHAUZAT et al. 2009, GENERSCH et al. 2010).
As another example, no unusual colony losses are reported from Australia, where a lot of Neonicotinoid
seed treatment is applied (but no Varroa mites are present) (NEUMANN & CARRECK 2010). Moreover, in
recent scientific reviews of the evidence for whether Neonicotinoid pesticides play a causal role in bee
declines (BLACQUIERE et al. 2012, CRESSWELL et al. 2012), the conclusion reached is there is no evidence
that they do. Finally, if increased colony mortality would in fact be caused by Neonicotinoid-contaminated
HFCS, how could then the observed colony losses in regions where HFCS is or has not been not
commonly used to feed bee colonies (like Europe, Asia) be explained?
Symptoms of mortality. The authors claim to have induced CCD in their study. However, the symptoms
described do not seem to support this claim. In late December 2010, all colonies were found alive, but the
ones exposed to higher levels of Imidacloprid appeared weaker with smaller bee clusters inside the
hives (apparently just an estimate), and dead bees were found in front of the hives. Then subsequently,
more and more colonies died after these signs of weakening. The dead hives were remarkably empty,
just food stores with honey and pollen were left in the combs. VAN ENGELSDORP et al. (2009) describe in
detail the symptoms used to define colonies as suffering from CCD. Symptoms include (1) the apparent
rapid loss of adult worker bees from affected colonies as evidenced by weak or dead colonies with excess
brood populations relative to adult bee populations, (2) a noticeable lack of dead worker bees both within
and surrounding the affected hives, (3) the delayed invasion of hives pests (e.g. small hive beetles and
wax moths), and kleptoparasitism (stealing food) from neighboring honey bee colonies. Other authors
(summarized by HENDRIKX et al. 2009) add that CCD is furthermore characterized by a sudden
disappearance of worker bees during the beekeeping season, and by evidence of recent brood (young
larvae, seemingly healthy queen). Almost none of these symptoms was observed in connection with the
colony mortality described by LU et al. (2012): the disappearance and the collapse of the affected colonies
did apparently not set in spontaneously, but was preceded by a weakening of the colonies; moreover,
dead bees were found in front of the hive, which would by definition not be the case in incidences of CCD,
but which is normal for overwintering colonies. There is no mention of the presence of a surviving queen in
the affected hives, but it can be implied that the authors would have recorded the presence of a lonesome
queen in the remarkably empty hives. Moreover, there is no information provided about the presence of
bee brood, but since the observation were made during winter time, it can be assumed that there was no
brood. Thus, what the authors have seen was colony mortality, but certainly not CCD.
Potential causes of mortality. The authors claim that The loss of imidacloprid-treated hives in this study
is also highly unlikely due to pathogen infection since the presence of neither Nosema nor a large number
of Varroa mites was observed in hives during the summer and fall seasons., and they conclude that
Since all hives were considered healthy as they went into fall season, those pathogens posed very little
threat to the health of honey bee hives. They substantiate this by an Apistan (active ingredient: TauFluvalinate) and Fumagillin B treatment against Varroa and Nosema that had been conducted in October.
Apparently, however, the health status of the colonies and the presence or absence of parasites was not
accurately checked with appropriate methods (or, if so, the results of this health analysis, like Varroa
counts or Nosema spore counts, are not documented), and it appears that hives were simply declared
healthy by the authors based on the lack of obvious signs of disease or parasite infestation seen by visual
inspection. However, the absence of conspicuous signs of diseases and parasites in late summer is by no
means conclusive evidence that the hives were not infested at all. Many beekeepers who have lost their
hives over winter due to Varroosis or other diseases would have considered them healthy when visually
inspecting them in late summer or fall. Likewise, just the fact that a treatment against a certain parasite
has been conducted does unfortunately by no means guarantee that the treatment was successful and
that the treated hive was and has remained parasite-free later on, especially when the treatment was
conducted with an inappropriate timing (see below), and with an active ingredient that might be not
efficient, if possible resistance has not been checked. For instance, according to OTTEN (2005), German
apiaries which had been treated with Apistan had losses as high as 43% over the winter of 2002/03. As
the authors likewise do not provide any data about diagnosis of diseases or parasites in the colonies that
died over the winter, it is very possible that the observed mortality was caused by Varroa or other
parasites or diseases which are commonly recognized to be the main factor behind colony overwintering
mortality.
Hive management. In the publication of LU et al. (2012) there are some details described about the
handling of the study colonies that give rise to the assumption that they have been improperly managed.
For instance, Varroa treatment with Apistan was conducted in October, which is much too late in the
season to be fully effective. Moreover, the applied product is not effective against mites in many areas of
the US. It is very possible that these management practices have contributed to the overall high colony
mortality observed in this study. Another point to mention is that the hives were apparently opened once a
week for assessments, even during the winter months at low temperatures. This is certainly not beneficial
for colony health and may likewise have weakened them. In this context it is notable that hive
management is in fact an important factor causing colony losses VAN ENGELSDORP et al. (2010b) even
rank it higher than CCD as a factor causing colony mortality.
Errors. Finally, there are several statements in the paper that are simply untrue or incorrect in the given
context. These include:
The abrupt emergence of colony collapse disorder (CCD) in the United States during 2006-2007, and
other countries later has raised the concern of losing this important perennial pollinator globally. - Largescale losses are not new to the beekeeping industry. Many of the symptoms similar to those related to
CCD have been described before. The first published record of this disorder appeared already in 1869.
Subsequently losses were described in Colorado in 1891 and 1896 where large clusters disappeared or
dwindled to tiny clusters with queens in May, hence the name May disease (UNDERWOOD & VAN
ENGELSDORP 2007). Then, CCD is not a common, global phenomenon, but specific to USA; in Europe, for
instance, colony losses with CCD symptoms are exceptional (see for instance HENDRIKX et al. 2009, VAN
ENGELSDORP et al. 2009, VAN ENGELSDORP & MEIXNER 2010). Even in the USA, many professional
apiarists have never seen a single case of CCD. The vast majority of colony losses in the US are not from
CCD (see e.g. VAN ENGELSDORP et al. 2010b).
Although some losses of honey bees from healthy and well managed hives during the winter months
have always been part of apiculture (for instance, in the New England area, winter losses of honey bee
hives are typically 15-30%), never in the history of the beekeeping industry has the loss of honey bee
hives occurred in such magnitude and over such a widely distributed geographic area. Sadly enough,
beekeepers are not facing only some losses and certainly not limited to the New England area.
According to NEUMANN & CARRECK (2010) elevated colony losses have recently been reported from e.g.
Europe (CRAILSHEIM et al., 2009), the USA (VAN ENGELSDORP et al., 2009; 2010) and the Middle East
(HADDAD et al., 2009, SOROKER et al., 2009) but only rarely from South America and virtually not at all
from Africa and Australia. The scientists cited above linked this to the fact that colonies of African honey
bees and Africanized honey bees in South America survive without Varroa treatment, whilst the mite has
not yet introduced into Australia. Furthermore, bee colony losses are clearly not a new phenomenon, they
just gained more attention: VAN ENGELSDORP & MEIXNER (2010) examined the historical records and
showed that extensive losses are not unusual. Already almost a century ago, in 1906, beekeepers on the
Isle of Wight (England), noticed that many of their honey bee colonies were dying, with numerous bees
crawling from the hive unable to fly. Older records report massive bee colony losses without obvious
disease symptoms from Australia in 1872 (BEUHNE 1910).
Winter losses of honey bee hives usually occur because honey bees run out of or cannot access food, or
the cluster becomes too small to generate sufficient heat. Starvation is one of the potential causes of
overwintering mortality, however, clearly not the only or even not the most predominant one. Factors
involved in overwintering mortality are for instance listed by VAN ENGELSDORP et al. (2010b) and by
BRODSCHNEIDER et al. (2010).
Commercial beekeepers appear to be affected by CCD at a disproportional rate According to van

ENGELSDORP et al. (2010b), professional beekeepers record on average less pronounced losses
compared to small apiaries.
To explain that mortality only set in several months after exposure to the treatment, the authors
hypothesize that winter bees were in their larval stage exposed to Imidacloprid, and therefore may have
been sublethally affected by this as adults. As an evidence for this kind of phenomenon, they cite the
publication of MEDRZYCKI et al. (2010). However, this paper describes different sensitivities of bees that
were reared at different temperatures to an insecticide, and not a reduced vitality of bees that were reared
exposed to a pesticide. In so far, this study is not of relevance in the given context.
Conclusions
The study presented by Lu et al. (2012) has been conducted according to a faulty design that was based
on numerous incorrect to unsupportable assumptions which are totally inconsistent with a sound scientific
approach. The results are accordingly insignificant for any risk assessment, moreover the authors interpret
them in a very questionable way. The study provides no evidence at all that the exposure of honeybee
colonies to Neonicotinoids under realistic conditions might have any adverse effect.
References
BEUHNE, R. (1910): Bee mortality. - Journal of the Department of Agriculture of Victoria, Australia 8: 149151
BLACQUIRE, T., G. SMAGGHE, C.A.M. VAN GESTEL & V. MOMMAERTS (2012): Neonicotinoids in bees: a
review on concentrations, side-effects and risk assessment. Ecotoxicology: DOI 10.1007/s10646-0120863-x
BRODSCHNEIDER, R., R. MOOSBECKHOFER & K. CRAILSHEIM (2010). Surveys as a tool to record winter losses
of honey bee colonies: a two year case study in Austria and South Tyrol. - Journal of Apicultural Research
49: 23-30
CHARRIRE, J.D. & P. NEUMANN (2010): Survey to estimate winter losses in Switzerland. Journal of
Apicultural Research 49: 132-133
CRAILSHEIM, K., R. BRODSCHNEIDER& P. NEUMANN (2009): The COLOSS puzzle: filling in the gaps. - In:
Proceedings of the 4th COLOSS Conference, 3-4 March 2009. Zagreb, Croatia: 46-47.
CHAUZAT, M.P., P. CARPENTIER, A.C. MARTEL, S. BOUGEARD, N. COUGOULE, Ph. PORTA, J. LACHAIZE, F.
MADEC, M. AUBERT & J.P. FAUCON (2009) : Influence of Pesticide Residues on Honey Bee (Hymenoptera:
Apidae) Colony Health in France. - Environmental Entomology 38: 514-523
CRESSWELL, J.E., N. DESNEUX & D. vaN ENGELSDORP (2012): Dietary traces of Neonicotinoid pesticides as
a cause of population declines in honey bees: an evaluation by Hills epidemiological criteria. - Pest
Management Science: doi: 10.1002/ps.3290.
DELAPLANE, K. (2012): Managed Pollinator Coordiated Agricultural Project Highlights and Emerging
Trends. - Bee Culture 12: 24-25.
GENERSCH, E., W. von DER OHE, H. KAATZ, A. SCHROEDER, Ch. OTTEN, R. Bchler, S. BERG, W. RITTER,
W. MHLEN, S. GISDER, M. MEIXNER, G. LIEBIG & P. ROSENKRANZ (2010): The German bee monitoring
project: a long term study to understand periodically high winter losses of honey bee colonies. - Apidologie
41: 332-352
FAUCON, J.P., C. AURIERES, P. DRAJNUDEL, L. MATHIEU, M. RIBIRE, A.C. MARTEL, S. ZEGGANE, M.P.
CHAUZAT & M.F.A. AUBERT (2005): Experimental study on the toxicity of imidacloprid given in syrup to
honey bee (Apis mellifera) colonies. - Pest Management Science 61:111125
10
GIROLAMI, V., M. MAZZON, A. SQUARTINI, N. MORI, M. MAZARO, A. DI BERNARDO, M. GREATTI, G. GIORIO &
A. TAPPARO (2009): Translocation of neonicotinoid insecticides from coated seeds to seedling guttation
drops: a novel way of intoxication for bees - Journal of Economic Entomology 102: 1808-1815.
HADDAD, N., A. BATAENEH, I. ALBABA, D. OBEID & S. ABDULRAHMAN (2009): Status of colony losses in
the Middle East. - In: Proceedings of the 41st Apimondia Congress, Mointpellier, France:.36
HENDRIKX, P., M.-P. CHAUZAT, M. DEBIN, P. NEUMANN, I. FRIES, W. RITTER, M. BROWN, F. MUTINELLI, Y. LE
CONTE & A. GREGORC (2009): Scientific Report Submitted to EFSA : Bee Mortality and Bee Surveillance in
Europe.: 217 pp.
KEPPLER, J., R. BECKER, R. SPATZ & F. DEchet (2010): Systemische insektizide Beizmittel Auftreten und
Relevanz von Guttation fr die Entwicklung von Honigbienenkolonien - Julius-Khn-Archiv 428: 133
MAUS, Ch., G. CUR & R. SCHMUCK (2003): Safety of imidacloprid seed dressings to honey bees: a
comprehensive overview of compilation of the current state of knowledge. - Bulletin of Insectology 56: 5157.
NEUMANN, P. & N.L. CARRECK (2010): Honey bee colony losses. - Journal of Apicultural Research 49: 1-6
MEDRZYCKI, P., F. SGOLASTRA, L. BORTOLOTTI, G. BOGO, S. TOSI, E. PADOVANI, C. PORRINI & A.G. SABATINI
(2010): Influence of brood rearing temperature on honey bee development and susceptibility to poisoning
by pesticides - Journal of Apicultural Research 49: 52-59.
NGUYEN, B.K., C. SAEGERMAN, G. PIRARD, J. MIGNON, J. W IDART, B. THIRONET, F.J. VERHEGGEN, D.

BREKVENS, E. DE PAUW & E. HAUBRUGE (2009): Does Imidacloprid Seed Treated Maize Have an Impact on
Honey Bee Mortality? Journal of Economic Entomology. 102: 616-623
OTTEN, Ch. (2003a): Das Vlkersterben: Daten und Fakten. Deutsches Bienen Journal 8/2003: 312-314
OTTEN, Ch. (2003b): Daten und Fakten zu den Vlkerverlusten. ADIZ 8/2003: 6-8
11
OTTEN, Ch. (2005): Bee Colony Mortality in Germany: Data and Facts. - In: FORSTER, R., E. BODE & D.
BRASSE (eds.): Das Bienensterben im Winter 2002/2003 in Deutschland Zum Stand der
wissenschaftlichen Erkenntnisse. Bundesamt fr Verbraucherschutz und Lebensmittelsicherheit (BVL),
Braunschweig: 9-15
PISTORIUS, J., T. BROBYN, P. CAMPBELL, R. FORSTER, J.A. LORSCH, F. MAROLLEAU, Ch. MAUS, J. LCKMANN,
H. SUZUKI, K. W ALLNER & R. BECKER (in press): Assessment of risks to honey bees posed by guttation.
Julius-Khn-Archiv
ROGERS, R.E.L., & J.R. KEMP (2004): Assessing Bee Health in the Maritimes: A survey of pesticide
residues in honey bee, Apis mellifera, colonies. Final Report, PEI Adapt Council Project Number 319.02.
October 15th, 2004
SCHMUCK, R., R. SCHNING & R. SUR (2005): Studies on the Effects of Plant Protection Products
Containing Imidacloprid on the Honeybee, Apis mellifera L. In: FORSTER, R., E. BODE & D. BRASSE (eds.):
Das Bienensterben im Winter 2002/2003 in Deutschland Zum Stand der wissenschaftlichen
Erkenntnisse. Bundesamt fr Verbraucherschutz und Lebensmittelsicherheit (BVL), Braunschweig: 68-92
SOROKER, V., A. HETZRONI, B. YACOBSON, H. VOET, S. SLABEZKI, H. EFRAT, & N. CHEJANOVSKY

(2009): Colony losses in Israel: incidence of viral infection and beehive populations. - In: Proceedings of
the 41st Apimondia Congress, Mointpellier, France: 38
VAN ENGELSDORP, D., J.D. EVANS, C. SAEGERMAN, Ch. MULLINS, E. HAUBRUGE, B.K. NGUYEN, M. FRAZIER, J.
FRAZIER, D. COX-FOSTER, Y. CHEN, R. UNDERWOOD, D. TARPY & J.S. PETTIS (2009): Colony Collapse
Disorder: A Descriptive Study. PLoS ONE 4: doi:10.1371/journal.pone.0006481
VAN ENGELSDORP, D. & M.D. MEIXNER (2010): A historical review of managed honey bee populations in
Europe and the United States and the factors that may affect them. - Journal of Invertebrate Pathology
103: S80S95
VAN ENGLESDORP, D., N. SPEYBROECK, J.D. EVANS, B.K. NGUYEN, Ch. MULLINS, M. FRAZIER, D. COXFOSTER, Y. CHEN, D. TARPY, E. HAUBRUGE, J.S. PETTIS & C. SAEGERMAN (2010a): Weighing Risk Factors
12
Associated with Bee Colony Collapse Disorder by Classification and Regression Tree Analysis. - Journal
of Economic Entomology 103:1517-1523.
VAN ENGELSDORP,
D., J. HAYES Jr., R.M. UNDERWOOD & J.S. PETTIS (2010b): A survey of honey bee colony
losses in the United States, fall 2008 to spring 2009. - Journal of Apicultural Research 49: 7-14
UNDERWOOD, R.M. & D. VAN ENGELSDORP (2007): Colony Collapse Disorder: Have We Seen This Before? Bee Culture 35:138
Dr. Ch. MAUS, A. SCHRMANN, DR. D. FISCHER, DR. D. ROGERS, DR. I. KELLY, 2012-04-10
13
Bayer CropScience Statement on the Findings of the Study:
KRUPKE et al. (2012): Multiple Routes of Pesticide Exposure for Honey Bees
Living Near Agricultural Fields
PLoS ONE 7 (1) 1-8

The publication of KRUPKE et al. (2012) reports the findings of a study on potential routs of exposures
for honeybees to pesticides, especially to Neonicotinoids, conducted in a corn-growing region in USA
in 2010. The study was initiated in response to reports of bee kills at Indiana apiaries in spring of 2010
which coincided with the corn planting period in the area and which were believed to be related to
neonicotinoid seed treatment products.
In the first part of the study, one half of the study field of a ca. 2.1 ha was sown with corn seeds
treated with Clothianidin at a dressing rate of 1.25 mg a.s./kernel with a vacuum-pneumatic drilling
machine, the other half with untreated corn seeds. Commercial bee hives were set up within and
around the field. Samples for analysis of neonicotinoids were taken from the soils of fields around the
study field, from waste talc in the planter that was added to the seeds before drilling, from pollen of
treated and untreated corn plants on the study field, and from pollen loads of forager bees returning to
the study hives. Additional test plots were drilled using the same planter in 2011 with commerciallyobtained corn seeds treated with various rates of Thiamethoxam or Clothianidin and additional
samples of the waste talc were collected. Key analytical findings are depicted in the below table:
Matrix
Clothianidin [ppb]
Thiamethoxam [ppb]
2.1 - 9.6
n.d.
4,900,000 - 15,030,000
68,000 - 13,240,000
3.9
1.7
Pollen loads collected before drilling of the

study plot
n.d. - 88
n.d. - 7.4
Pollen loads collected after drilling of the

study plot
n.d. - 12
n.d
Soil of surrounding fields

Talc from the planter
Maize pollen from treated plants (study plot)
n.d. = not detected
In the second part of the study, samples were taken from an apiary in Indiana where in 2011 increased
bee mortality was reported that was coinciding with the corn planting season. Sample were taken from
weeds growing close to corn fields in the surroundings, from dead and from live bees found near the
hives of the apiary, as well as from recently stored pollen and nectar taken from the apiarys hives.
Key analytical findings are depicted in the below table:

Matrix
Clothianidin [ppb]
Thiamethoxam [ppb]
3.8-13.3
n.d.
Healthy bees
n.d.
n.d.
Pollen in hive (sick)
10.7
20.4
Pollen in hive (healthy)
2.9
6.2
Weeds near study field

n.d. = not detected
1.1-9.4
n.d.-2.9
Dead bees
These findings are claimed to give evidence about different exposure routes for honeybees to
neonicotinoids originating from seed treatment products, which are basically exposure to soil dust from
previously treated fields that contains neonicotinoid residues, exposure to abraded dust from the seed
treatment emitted during the drilling process, and exposure to systemic residues in nectar and pollen
of treated crops (or succeeding crops/weeds on treated fields). By these multiple pathways of
exposure, bee colonies in areas where neonicotinoid seed treatment is applied would then be exposed
throughout the growing season.

The publication of KRUPKE et al. (2012) presents some data on potential exposure routes to
neonicotinoid seed treatment products; basically none of these are fundamentally new, all have
already been suggested and investigated in previous publications or studies (PISTORIUS et al. 2009;
NIKOLAKIS et al. 2009; HERBST et al. 2010; MARZARO et al. 2011). The presented figures are largely
consistent with the data on those exposure routes that already had been collected in previous studies.
However, there are some points in particular related to the interpretation of the data surveyed that
require clarification or comment:
Soil dust as exposure route: One of the discussed potential routes of exposure is via dust from soils
that contain neonicotinoid residues from previous croppings. There may indeed be neonicotinoid
residues in soils that were planted with seed-treated crops, but these are very low. The highest
Clothianidin residue soil level found in this study was 9.6 ppb.
Using EPAs contact LD50 for
Clothianidin of 0.0439 g/bee, a bee would have to be exposed to 4.6 g of soil dust, which is
equivalent to 46 times its body weight. Clearly, soil dust containing residue levels reported by Krupke
et al. is not a toxicologically significant exposure route for honeybees.
Waste talc samples from planters: It is well known that abraded dust from neonicotinoid seed
treatment products can contain intrinsically highly toxic insecticide concentrations, which is
consequently also true for talcum added to the treated seeds in the planter. This was confirmed in the
study of KRUPKE et al. (2012). However, while their results suggest high intrinsic toxicity of these
dusts, they do not allow inferences to be made about the risk potential for bees, as they do not give
any information about the exposure levels of bees to dusts emitted by corn planters and deposited on
bee attractive flowers. The measurements they reported were made on the waste material left in the
planter after drilling, rather than on the dust emitted from it during drilling.
This waste material
contained broken off pieces of the seeds and seed coatings in addition to talc (Brian Eitzer, personal
communication). Because these samples were of material that dropped out of the planter exhaust
airstream, they likely contained coarser, heavier particles than the dust emitted by the planters. The
insecticide concentration of this coarse material may not be representative of that of the dust emitted
from the planter. Of more relevance to the assessment of exposure of honey bees to planter-emitted
dust would be samples of dust deposition on flowers from areas immediately adjacent and downwind
from the planted field. KRUPKE et al. (2012) did not evaluate this, although they did collect and analyze
whole dandelion flowers that were growing near recently planted cornfields during their investigation of
a 2011 bee kill event. These samples contained only very low levels of neonicotinoids. While of
questionable relevance to assessing bee exposure to abraded seed dust released during planting, the
high concentrations in the waste talc reported by KRUPKE et al. (2012) do suggest that farmers should
take care not to blow waste material on to blooming crops or weeds when cleaning out planting
equipment.
Systemic residues in maize pollen: Figures displayed are consistent with previous findings from
comprehensive field residue studies (SCHMUCK & KEPPLER 2003, unpublished data). The residue levels
are not of concern since they are well below the established colony field no-observed-effect
concentration of 20 ppb. However, one point should be highlighted: in the pollen sample from
Clothianidin-treated maize, both Clothianidin and Thiamethoxam were found. As Thiamethoxam is
degraded to Clothianidin, but not vice versa, this is not possible and suggests that either samples were
contaminated or mixed up.
Residues in pollen loads: Residues in pollen loads that forager bees carried to the study hives were
very variable and inconsistent. At planting and immediately following planting residues were low and
below a level of concern. Anomalously, there were some higher residues immediately prior to planting.
There was no correlation between the amount of corn pollen, as a percentage of total pollen, in a
sample and the residue level of neonicotinoids. Therefore it is clear that the residues in this matrix
that were found pre-planting are not related to the seed treatment on the study field, and most likely
result from an unknown source of contamination.
Synergistic effects: The co-occurrence of certain fungicides and neonicotinoids in bee-collected

pollen is pointed out by the authors, and they bring up concerns about potential synergistic effects
between both types of compounds under reference to IWASA et al. (2004). It should however be noted
that IWASA et al. report about synergistic effect potentials between fungicides and cyano-substituted
neonicotinoids (e.g. Acetamiprid, Thiacloprid), and found no significant synergistic effects between
fungicides and nitro-substituted neonicotinoids (e.g. Imidacloprid, Thiamethoxam, Clothianidin). These
two classes of neonicotinoids behave fundamentally different in this respect.
Synergistic effects
between fungicides and nitro-substituted neonicotinoids have according to our knowledge never been
documented in scientific research.
Lack of Observable Adverse Effects in the 2010 Field Experiment: The 2010 field experiment
appears to have been designed to simulate conditions thought to be responsible for the bee kill
incident at the Purdue apiaries earlier that year. Four honey bee colonies were placed around the
perimeter of a test plot that was then planted with seeds with maximum Clothianidin treatment rate,
and four additional colonies were placed around an adjacent test plot which was planted with
untreated seeds. The paper did not mention whether any adverse effects were observed in these
colonies seemingly placed in harms way. These colonies were visited daily for purposes of collecting
samples from pollen traps and it seems reasonable to assume that if significant numbers of dead or
dying bees were present, this would have been observed. In a recent phone conversation with BCS
scientists, Christian Krupke confirmed that no unusual mortalities or signs of pesticide intoxication
were observed at these colonies.
Investigation of 2011 bee mortalities: From the analytical results depicted, it appears possible that
the surveyed bee colonies had been exposed to a neonicotinoid seed treatment product. Residue
levels of Clothianidin found in dead bees are comparable to findings after a Clothianidin incident in
Germany in 2008. Findings of Clothianidin and of Thiamethoxam in in-hive matrices and on weeds
from the surroundings suggest that Thiamethoxam was the compound they were exposed to. There
was no Thiamethoxam found in dead bees, but this may be explained by its relatively fast metabolic
conversion to Clothianidin in bees. In-hive samples were taken from two hives of the apiary, one sick
and one healthy. Both terms were defined on the basis of presence or absence of dead bees found
in front of the hive, which considering the complexity of a bee colony is a quite insufficient criterion.
Residues of Thiamethoxam and Clothianidin were found in both the healthy and the sick hive, but
at somewhat higher levels in the sick colonies. However, as the sample size was very small (just two
colonies!) there is no way of doing a scientifically sound correlation between the health status of the
colonies and the residue levels found. In summary, the data presented basically demonstrate that bee
hives from the sampled apiary were exposed to a neonicotinoid, most probably Thiamethoxam. That
individual exposed worker bees have been killed is not unlikely.
Nonetheless, no effect to the
observed colonies was documented. The available evidence does not identify a route of exposure, as
the residue levels in the in-hive pollen and the flowers from adjacent fields are not sufficiently high to
result in bee mortality. Coincidence of the mortalities with planting season and spatial proximity with
typically seed-treated crops support the plausibility of an assumption that dust from seed treatment
was the route of exposure, but information regarding the circumstances and conditions that resulted in
the exposure (e.g. seed treatment quality, planter types and equipment, agricultural practice, tillage
system) are lacking. Therefore, based on the presented data, it is not possible to fully evaluate the
incident, nor to exclude for example the possibility that the incident was caused by inappropriate
practices related to handling or sowing treated seeds.
Reports of pesticide bee kill incidents associated with corn planting in the US Midwest have been
extremely infrequent, suggesting that this is not a common route of exposure in this type of
environment, and is being effectively avoided. In other environments, effective measures have been
developed and implemented to minimize exposure (see e.g. NIKOLAKIS et al. 2009, HERBST et al. 2010,
EUROPEAN COMMISSION 2010). If the appropriate measures are correctly applied, exposure should be
kept at a minimum such that the intrinsic toxicity of dusts should play a minor role in the evaluation of a
potential risk. The KRUPKE et al. (2012) study may have identified another agriculture management
practice in need of attention, namely the proper clean up and disposal of waste talc after planting. The
two bee kill incidents reported KRUPKE et al. (2012) appeared to be of minor severity, with no indication
of any colony deaths. The Purdue University colonies affected in 2010 all reportedly recovered to
normal strength within a few weeks (Greg Hunt, personal communication). The 2011 incident appears
to have been similar, although details were not given in the paper.
While these incidents are
regrettable, they in no way suggest that use of neonicotinoid insecticides as a corn seed treatment
play any role at all in the high annual colony loss rates or Colony Collapse Disorder syndrome that
some US Beekeepers have reported in recent years. Bayer CropScience is unaware of even a single
bee colony loss in the United States that can be reasonably attributed to the use of Clothianidin,
Imidacloprid or any other neonicotinoid as a corn seed treatment.
Correction of Technical Errors or Misleading Statements about Risk: Several statements made
in the paper are incorrect or highly misleading. First, it was stated that some of the pollen sample
concentrations exceeded the oral LD50.
There was one pollen sample with a total neonicotinoid
concentration of 95.4 ppb (88 ppb clothianidin + 7.4 ppb thiamethoxam). For a nurse bee weighing
100 mg and consuming 6.5 mg of pollen with a concentration of 95.4 ppb would result in a dose of
0.62 ng, which is far below the LD50. Consumption of the pollen with the average concentration
reported for bee-collected pollen would result in daily ingestion of only 2% of the LD50.
Second, a related statement made in the paper was A bee will consume 65 mg of pollen during the
10 day period it spends as a nurse bee, therefore a concentration of 20 ng/g (ppb) in pollen would
correspond to a dose of 1.3 ng (65 mg x 20 ng/g) or almost 50% of the oral LD50 of ca. 2.8 ng/bee.
This statement is accurate, but it is highly misleading to compare the dose ingested over 10 days to an
acute oral LD50. Bees rapidly metabolize and excrete neonicotinoids so that non-toxic concentrations
do not build up over multiple days to become toxic concentrations.
The correct approach is to
compare the dose ingested per day with the LD50 (and even this will overestimate the real risk).
In
this case, the daily dose 0.13 ng/bee/d represents <5% of the LD50. A chronic (10-day) feeding study
with young adult honey bees established a no-observed-effect level of 0.38 ng/bee/d for clothianidin.
Thus, the scenario Krupke et al. hypothesized clearly poses a minimal risk.
Finally, it was stated that pollen contaminated with levels of neonicotinoids similar to those shown in
our results has been known to impair pollinator health. Three citations were given in support. The first
is a study that evaluated changes in the frequency of the proboscis extension reflex of individual
honey bees in a highly artificial laboratory assay. The relevance of changes in this endpoint to the
health of bee colonies in the field has not been demonstrated. The second citation is a review article
that cites the first study and presents no original data. The third citation refers to sublethal effects
related to the foraging activity of bumblebees in laboratory or greenhouse study setups. The data
presented are certainly of scientific interest, but it is not possible to deduce from them any general
statement about an impairment of pollinator health.
Conclusion: In summary, it can be stated that the study of KRUPKE et al. (2012) does not provide any
fundamentally new evidence about honeybee exposure to neonicotinoid seed treatment products. The
exposure levels reported in soil, pollen and nectar are generally consistent with previous research and
were not high enough to represent a significant risk for honey bees. Higher concentrations found in
waste talc collected from inside pneumatic equipment post-planting represent an intrinsic hazard to
honey bees, however actual exposure of bees to this material was not demonstrated and would
appear to be preventable. The paper reports some information documenting the occurrence of two
minor bee kill incidents that were coincident with planting of treated corn seeds that may have been
caused by neonicotinoid exposure. However, the available information is insufficient to determine the
route of exposure.
In their field experiment, low exposure levels and no adverse effects were
observed for bee colonies placed in harms way around the perimeter of a field as it was planted with
treated corn seeds. Overall, the publication represents an interesting case study, but it does not
provide any significant new insights into exposure of honeybees to neonicotinoid insecticides.
References:
EUROPEAN COMMISSION (2010):
Commission Directive 2010/21/EU of 12 March 2010
amending
Annex I to Council Directive 91/414/EEC as regards the specific provisions relating to clothianidin,
thiamethoxam, fipronil and Imidacloprid. - Official Journal of the European Union L 65/27-L65/30
HERBST, A., D. RAUTMANN, H.J. OSTEROTH, H.J. W EHMANN & H. GANZELMEIER (2010): Drift of seed
dressing chemicals during the sowing of maize. Aspects of Applied Biology 99: 265-269
IWASA, T., N. MOTOYAMA, J.T. AMBROSE & R.M. ROE (2004): Mechanism for the differential toxicity of
neonicotinoid insecticides in the honey bee, Apis mellifera. - Crop Protection 23: 371378
KRUPKE, Ch.H., G.J. HUNT, B.D. EITZER, G. ANDINO & K. GIVEN (2012): Multiple Routes of Pesticide
Exposure for Honey Bees Living Near Agricultural Fields. - PLoS ONE 7: 1-8
MARZARO M., L. VIVAN, A. TARGA, L. MAZZON, N. MORI, M. GREATTI, E. PETRUCCO TOFFOLO, A. DI
BERNARDO, C. GIORIO, D. MARTON, A. TAPPARO, V. GIROLAMI (2011): Lethal aerial powdering of
honey bees with neonicotinoids from fragments of maize seed coat. Bulletin of Insectology 64 (1):
119-126
NIKOLAKIS, A., A. CHAPPLE, R. FRIESSLEBEN, P. NEUMANN, Th. SCHAD, R. SCHMUCK, H.F. SCHNIER, H.J.
SCHNORBACH, R. SCHNING & Ch. MAUS (2009): An effective risk management approach to prevent
bee damage due to the emission of abraded seed treatment particles during sowing of seeds
treated with bee toxic insecticides. - Julius-Khn-Archiv 423: 132-148
PISTORIUS J., BISCHOFF G., HEIMBACH U., STHLER M. (2009): Bee poisoning incidents in Germany in
spring 2008 causedby abrasion of active substance from treated seeds duringsowing of maize.Julius Khn Archiv, 423: 118-126.
SCHMUCK, R. & J. KEPPLER (2003): Clothianidin Ecotoxicological profile and risk assessment. Pflanzenschutz-Nachrichten Bayer 56: 26-58
Christian MAUS, David FISCHER, Iain KELLY & Dick ROGERS
2 T.W. Alexander Drive
Research Triangle Park, NC 27709
February 21, 2012
Notes on Study of HENRY et al. (2012)

http://www.sciencemag.org/content/early/recent / 29 March 2012 /
10.1126/science.1215039
Title: A Common Pesticide Decreases Foraging Success and Survival in Honey

Bees
Authors: Mickal HENRY1*, Maxime BEGUIN2, Fabrice REQUIER3,4, Orianne
ROLLIN1,5, Jean- Franois ODOUX4, Pierrick AUPINEL4, Jean APTEL1, Sylvie
TCHAMITCHIAN1, Axel DECOURTYE5
1
INRA, UR406 Abeilles et Environnement, F-84914 Avignon, France.
Association pour le dveloppement de lapiculture provenale (ADAPI), F-13626
Aix-en-Provence, France.
3
Centre dEtudes Biologiques de Chiz, CNRS, UPR1934, F-79360 Beauvoir-
sur-Niort, France.
4
INRA, UE1255, UE Entomologie, F-17700 Surgres, France.
ACTA, UMT PrADE, UR 406 Abeilles et Environnement, F-84914 Avignon,
France.
This is an interesting study which employed the use of radio frequency

identification (RFID)
tags on honey bees to study whether exposure to the
Neonicotinoid insecticide Thiamethoxam (manufactured by Syngenta) impairs the

ability of forager bees to return to the hive and if so, whether this is likely to have
consequences for the long-term survival of the colony. The study is presented in
the context of colony collapse disorder, a phenomenon in which adult honey
bees rapidly disappear from their colony leaving behind apparently healthy queen
and abundant brood and food stores, and other types of colony losses as
currently observed in many regions of the world. Some have hypothesized that
the disappearance of the adult bees and eventual collapse of colonies may be a
result of sublethal toxicity of Neonicotinoid pesticides since various laboratory

assays are claimed to show these compounds impair memory and learning of
honey bees at sublethal levels. HENRY et al. (2012) evaluated whether acute
dietary exposure to a non-lethal dose of Thiamethoxam causes homing failure
(inability of foraging bees to return to their hive) and indirectly whether this could
lead to colony failure (hive depopulation). Homing failure rates were determined
by direct experimentation. Pollen forager bees were captured as they returned to
their hive, held for several hours and after a period of feeding and fasting
administered a dose of 1.34 ng Thiamethoxam in 20 L of 50% sugar solution
containing 0.067 ng Thiamethoxam/L. The bees were then released 1 km away
from the hive. Test subjects were marked with radio frequency identification tags
that permitted automated recording of when these bees returned to the hive.
Bees not returning to the hive were assumed to have died and the mortality from
homing failure and background causes (determined in control bees) were then
inputted into a population model to predict the long term consequences of the
pesticide-induced homing failure on the hive colony dynamics.
Comments from the BCS Perspective
1. Actually, the study setup described by the authors is just measuring homing
behavior, and not survival or mortality by homing failure. Worker bee mortality
and population dynamics in a colony is a very complex natural process which
is influenced by many factors, and the natural turnover (i.e. mortality) rate of a
full-sized colony is up to 2,000 bees per day (IMDORF et al. 1996). Worker
bees that die in terms of this turnover tend to leave their hive before by
instinct as a behavioral pattern related to colony hygiene. Therefore, it is an
unjustified interpretation to a-priori equate differences in numbers of worker
bees returning (which does not necessarily constitute an adverse effect on
colony level) to a colony with mortality by homing failure.
2. The dose level tested was described as being commonly encountered by

foraging bees in real field situations, but justification for this is not well
explained and appears to be based on faulty reasoning. The concentration of
the dosing solution was 67 g/L, which is about 56 ppb when one converts it
to a wt/wt measurement (50% sucrose solution has a density of roughly 1.2
mg/L). This concentration is much greater than the 1-5 ppb levels that have
typically been reported in nectar produced by plants grown from
Neonicotinoid-treated seeds; even maximum residue levels of Neonicotinoids
found in nectar or pollen of seed-treated crops are by far lower than the
concentration applied here. HENRY et al. (2012) apparently set their dosing
concentrations to produce the maximum cumulative dose bees may ingest
over an entire day of feeding, and then administered this dose at once in a
single meal. For a Neonicotinoid, which is rapidly metabolized by honey bees,
the dose bees can tolerate over an entire day of feeding is much greater than
what they can tolerate if ingested as a single meal. An analogous situation
would occur if instead of taking 2 pills of a medication every 4 hours for a total
of 12 per 24 hours, as is directed by the product label, a person were to take
12 pills at one time. The single dose ingested would be 6 times greater than
the maximum recommended. HENRY et al. (2012) have done essentially the
same thing. The single dose they administered was >20 times the single dose
forager bees obtain when they feed on nectar of flowers of crops grown from
Thiamethoxam treated seeds: A report by the French authorities (ANSES
2010) estimated the concentration of Thiamethoxam present in nectar of oilseed rape flowers to be slightly less than 2 ppb. Nectar forager bees have a
limit of about 30 mg they ingest in a single foraging bout. Even if one
assumes all of this nectar was consumed as food (rather than brought back to
the hive for purposes of making honey), the dose the bee would ingest from
30 mg of nectar with a concentration of 2 ppb (=ng/g) is 0.06 ng. This
therefore would appear to represent a worst-case estimate of the acute oral
dose that is field relevant. HENRY et al. (2012) gave their bees a dose of 1.34
ng, which is 22 times greater than 0.06 ng. It should likewise be emphasized
that an acute dose of 1.34 ng Thiamethoxam/bee as administered here may

already have caused a certain level of mortality as it is relatively close to LD50
figures established for some Neonicotinoids. It may have been a sublethal
dose level, but it was still a very high dose level. It is improper to claim the
exposure scenario as described by HENRY et al. (2012) is representative of
what bees commonly encounter at real world agricultural sites.
3. Rather than try to calculate the worst-case acute oral dose level bees could
experience in the field, as was done above, HENRY et al. (2012) used the data
of RORTAIS et al. (2007) to estimate the possible cumulative daily dose for a
forager bee. In other words, they sought to give as a single dose the total
amount of toxicant taken in over an entire day of feeding. Many substances
are toxic when an entire daily intake is administered as a single dose. Even
water may be fatal if a person is forced to drink too much at once. Referring
back to the medication example, would anyone not expect side effects if a
person took 12 pills at once, instead of 2 every 4 hours? HENRY et al. (2012)
did not explain the details of how they came up with a target dose level of 1
ng/bee. But clearly, this is not a field relevant exposure level. And the fact that
their dosing solution turned out upon chemical analysis to be 134% of
nominal is also concerning. This is not reasonably close to the nominal
amountusually regulatory authorities consider 80-120% of nominal to be
reasonable. The reported level (134%) is clearly outside the norm of typical
measurement error in preparation of dose levels.
4. The test design applied by HENRY et al. (2012) is not validated; therefore it is
not clear whether the results presented would be reproducible at all.
Experience with honeybee study designs has shown that study validation is
essential to assure generating scientifically sound results. Likewise, the
population model applied seems not to be validated, at least not for honeybee
population dynamics. Population development of a bee colony is a highly
complex thing and we are far away from having fully understood its
mechanisms and interdependencies. For instance, recent research results
suggest that the individual lifespan of worker bees may be influenced by the
abundance of brood in the colony (e.g. LIEBIG et al. 2012). Such effects that
might effectively compensate losses of forager bees are not considered in the
applied population model.
5. A few months ago, the study of SCHNEIDER et al. (2012) was published that
had a similar purpose and design as the experiments described by HENRY et
al. (2012) Using RFID technology, foraging and homing behavior of
honeybees exposed to sublethal levels of Imidacloprid and Clothianidin was
tested. In contrast to HENRY et al. (2012), SCHNEIDER et al. (2012) tested a set
of different exposure concentrations of their test substances (0.15 to 6 ng/bee
Imidacloprid and 0.05 to 2 ng/bee Clothianidin), among them concentrations
that really may correspond to field-relevant exposure scenarios. They
concluded that at field-relevant doses for nectar and pollen no adverse effect
was observed for either substance. It is highly likely that HENRY et al. (2012)
would have come to the same conclusion for their test substance
Thiamethoxam, if they would have followed Schneider et al.s scientifically
sound approach to test a range of concentrations that also include fieldrelevant dose rates. Interestingly, HENRY et al. (2012) mention the work of
SCHNEIDER et al. (2012) in their reference list, but do not refer to it in more
detail in their discussion, as would be expected given that both studies deal
with the same methods and with compounds of the same class of chemicals.
6. In the study of HENRY et al. (2012), there were, as in most studies so far
conducted on sublethal effects, only individual bees tested out of the context
of the colony. It has been frequently seen that worker bees when sub-lethally
exposed to a pesticide react completely differently compared to when a whole
colony is exposed to the same compound, or that sublethal effects that were
seen in the laboratory on individual bees could not be recovered under field
conditions in bee colonies exposed to the respective concentrations of the
compound; this has for instance been shown for the proboscis extension
reflex test (MAUS et al. 2003; THOMPSON & MAUS 2007; other example in
PETTIS et al. 2012). Therefore, an extrapolation from findings on individual
bees exposed under artificial designs to colony effects under field conditions
is generally difficult to make, if not even impossible.
7. If exposure of honeybee colonies to sublethal levels of Neonicotinoids under
field conditions would in fact lead to a loss of forager bees and eventually a
depopulation of the hives, as the authors hypothesize, this should also
become evident in field studies where hives are exposed to treated crops.
However,
more
than
30
field
studies
have
been
conducted
with
Neonicotinoids and this kind of effect has never been observed (see for
instance MAUS et al. 2003, SCHMUCK et al. 2005, SCHMUCK & KEPPLER 2003).
8. There is no field evidence linking hive depopulations to sublethal exposures
to Neonicotinoids. On the contrary, CCD occurrence and other colony losses
that have been observed at large scales are not correlated with exposure of
honey bee colonies to Neonicotinoids (VAN ENGELSDORP et al. 2009,
DELAPLANE 2012) or to exposure of colonies to Neonicotinoid-treated crops
(e.g. OTTEN 2003a, b, CHARRIRE & NEUMANN 2010). Linkage of Neonicotinoid
exposure to declining bee colony health and elevated colony losses has NOT
been found in any of the recent regional multifactorial studies of declining bee
health (VAN ENGELSDORP et al. 2009, 2010, ROGERS & KEMP 2004, NGUYEN et
al. 2009, CHAUZAT et al. 2009, GENERSCH et al. 2010). Finally, in recent
scientific reviews of the evidence for whether Neonicotinoid pesticides plays a
causal role in bee declines (BLACQUIERE et al. 2012, CRESSWELL et al. 2012),
the conclusion reached is there is no evidence that they do.
9. There are several statements in the paper that are simply untrue or incorrect
in the given context. These include:
a. CCD is not a common phenomenon of the Northern hemisphere as
initially stated in the article, but specific to USA; in Europe, for
instance, colony losses with CCD symptoms are exceptional (see for
instance HENDRIKX et al. 2009,
VAN
ENGELSDORP et al. 2009,
VAN
ENGELSDORP & MEIXNER 2010). Even in the USA, many professional

apiarists have never seen a single case of CCD. The vast majority of
colony losses in the US are not from CCD.
b.
Neonicotinoids are not especially liable to provoke [] behavioral

trouble. There have indeed been several studies in which sublethal
doses of Neonicotinoids were tested on bees, and behavioral
differences were found between treated and untreated individuals.
However, in no case it has been shown that these differences indeed
would constitute adverse effects and would thus have to be classified
as behavioral troubles.
Conclusion: The study demonstrates that sublethal, but nevertheless very high
and non-field relevant exposure levels of Thiamethoxam have an effect on
homing behavior of forager bees. It does not provide significant new insights into
risk assessments for Neonicotinoids. The results are NOT evidence that
Neonicotinoids are involved in CCD or otherwise elevated colony losses.
References:
ANSES (2010): Avis de l'Agence nationale de scurit sanitaire de lalimentation,
de lenvironnement et du travail relatif une demande d'autorisation de mise sur
le march de la prparation CRUISER OSR base de thiamthoxam, fludioxonil
et mtalaxyl-M de la socit SYNGENTA AGRO SAS. - ANSES dossier n
2007-3336 CRUISER OSR: 27 pp.
BLACQUIRE, T., G. SMAGGHE, C.A.M.
VAN
GESTEL & V. MOMMAERTS (2012):
Neonicotinoids in bees: a review on concentrations, side-effects and risk

assessment. Ecotoxicology: DOI 10.1007/s10646-012-0863-x
CHARRIRE, J.D. & P. NEUMANN (2010): Survey to estimate winter losses in

Switzerland. Journal of Apicultural Research 49: 132-133
CRESSWELL, J.E., N. DESNEUX & D.
VAN
ENGELSDORP (2012): Dietary traces of
Neonicotinoid pesticides as a cause of population declines in honey bees: an

evaluation by Hills epidemiological criteria. - Pest Management Science: doi:
10.1002/ps.3290.
DELEPLANE, K. (2012): Managed Pollinator Coordiated Agricultural Project

Highlights and Emerging Trends. - Bee Culture 12:24-25.
GENERSCH, E., W. VON DER OHE, H. KAATZ, A. SCHROEDER, CH. OTTEN, R.

BCHLER, S. BERG, W. RITTER, W. MHLEN, S. GISDER, M. MEIXNER, G. LIEBIG & P.
ROSENKRANZ (2010): The German bee monitoring project: a long term study to
understand periodically high winter losses of honey bee colonies. - Apidologie
41: 332-352
HENDRIKX, P., M.-P. CHAUZAT, M. DEBIN, P. NEUMANN, I. FRIES, W. RITTER, M.

BROWN, F. MUTINELLI, Y. LE CONTE & A. GREGORC (2009): Scientific Report
Submitted to EFSA : Bee Mortality and Bee Surveillance in Europe: 217 pp.
IMDORF, A., M. RICKLI & P. FLURI (1996): Massenwechsel des Bienenvolkes.Schweizerisches Zentrum fr Bienenforschung Liebefeld, Bern: 48 pp.
LIEBIG, G., P. AUMEIER & O. BOCKING.( 2012): The loss of bees an important and
puzzling parameter in population dynamics of honey bee colonies. Symposium
Abstracts, Annual Meetings of the Working Group of the German Bee Institutes,
Bonn, March 27th to 29th, 2012: 20,
MAUS, Ch., G. CUR & R. SCHMUCK (2003):
Safety of imidacloprid seed
dressings to honey bees: a comprehensive overview of compilation of the current

state of knowledge. - Bulletin of Insectology 56: 51-57.
NGUYEN, B.K., C. SAEGERMAN, G. PIRARD, J. MIGNON, J. WIDART, B. THIRONET, F.J.

VERHEGGEN, D. BREKVENS, E. DE PAUW & E. HAUBRUGE (2009): Does Imidacloprid
Seed Treated Maize Have an Impact on Honey Bee Mortality? Journal of
Economic Entomology. 102: 616-623
OTTEN, Ch. (2003a): Das Vlkersterben: Daten und Fakten. Deutsches Bienen
Journal 8/2003: 312-314
OTTEN, Ch. (2003b): Daten und Fakten zu den Vlkerverlusten. ADIZ 8/2003:
6-8
PETTIS, J.S., D.
VAN
ENGELSDORP, J. JOHNSON & G. DIVELY (2012): Pesticide
exposure in honey bees results in increased levels of the gut pathogen Nosema.
Naturwissenschaften, DOI 10.1007/s00114-011-0881-1
ROGERS, R.E.L., & J.R. KEMP (2004): Assessing Bee Health in the Maritimes: A
survey of pesticide residues in honey bee, Apis mellifera, colonies. Final Report,
PEI Adapt Council Project Number 319.02. October 15th, 2004
RORTAIS, A., G. ARNOLD, M.P. HALM & F. TOUFFET-BRIENS (2007): Modes of

honeybee
exposure
to
systemic
insecticides:
Estimated
amounts
of
contaminated pollen and nectar consumed by different categories of bees.

Apidologie 36: 71-83
SCHMUCK, R. & J. KEPPLER (2003): Clothianidin Ecotoxicological profile and risk

assessment. Bayer-Pflanzenschutznachrichten 56: 26-58
SCHMUCK, R., R. SCHNING & R. SUR (2005): Studies on the Effects of Plant
Protection Products Containing Imidacloprid on the Honeybee, Apis mellifera L.
In: FORSTER, R., E. BODE & D. BRASSE (eds.): Das Bienensterben im Winter
2002/2003 in Deutschland Zum Stand der wissenschaftlichen Erkenntnisse.

Bundesamt
fr
Verbraucherschutz
und
Lebensmittelsicherheit
(BVL),
Braunschweig: 68-92
THOMPSON, H.M. & Ch. MAUS ( 2007): The relevance of sublethal effects in honey
bee testing for pesticide risk assessment. Pest Management Science 63:1058
1061
VAN ENGELSDORP, D., J.D. EVANS, C. SAEGERMAN, Ch. MULLINS, E. HAUBRUGE,

B.K. NGUYEN, M. FRAZIER, J. FRAZIER, D. COX-FOSTER, Y. CHEN, R. UNDERWOOD,
D. TARPY & J.S. PETTIS (2009): Colony Collapse Disorder: A Descriptive Study.
PLoS ONE 4: doi:10.1371/journal.pone.0006481
VAN ENGLESDORP, D., N. SPEYBROECK, J.D. EVANS, B.K. NGUYEN, Ch. MULLINS, M.
FRAZIER, D. COX-FOSTER, Y. CHEN, D. TARPY, E. HAUBRUGE, J.S. PETTIS & C.
SAEGERMAN (2010): Weighing Risk Factors Associated with Bee Colony Collapse
Disorder by Classification and Regression Tree Analysis. - Journal of Economic
Entomology 103:1517-1523.
VAN ENGELSDORP, D. & M.D. MEIXNER (2010): A historical review of managed

honey bee populations in Europe and the United States and the factors that may
affect them. - Journal of Invertebrate Pathology 103: S80S95
Dr. David L. FISCHER & Dr. Christian MAUS, 2012-04-01
From:
To:
Subject:
Date:
Epstein, David
"Cristi Palmer"
RE: Varroa summit
Tuesday, April 08, 2014 12:16:00 PM
Cristi,
Call anytime today, I am in the office until 3:30pm.
Dave
David Epstein, Ph.D.
Senior Entomologist, USDA Office of Pest Management Policy
1400 Independence Ave SW
Room 3871 - South Bldg., Mail Stop 0314
Washington, DC 20250-0314
Office: (202) 720-9877

Work Mobile: (b) (6)
Personal Mobile: (b) (6)
email: david.epstein@ars.usda.gov
From: Cristi Palmer [mailto:palmer@AESOP.Rutgers.edu]

Sent: Tuesday, April 08, 2014 10:56 AM
To: Epstein, David
Cc: 'Keith Dorschner'; 'Michael Braverman'
Subject: RE: Varroa summit
HI Dave,
I am working with a group of ornamental horticulture entomologists and bee entomologists who are
interested in addressing some perceived knowledge gaps for pollinator safety. (b) (5)
(b) (5)
When would be a
good time for me to call you to talk about this potential research pathway and how it might
complement other research endeavors?
Take care,
Cristi
From: Epstein, David [mailto:David.Epstein@ARS.USDA.GOV]

To: Keith Dorschner
Cc: Cristi Palmer
Subject: RE: Varroa summit
Hi Keith and Cristi,

Always open to discussions on pollinators its what I do.
Dave
Senior Entomologist, USDA Office of Pest Management Policy
Office: (202) 720-9877
Work Mobile:(b) (6)
From: Keith Dorschner [mailto:dorschner@AESOP.Rutgers.edu]

To: Epstein, David
Cc: Cristi Palmer
Subject: Varroa summit
Hi Dave,
I was wondering about the summary of this meeting and access to the presentations. No pressure!
Also, I copy Cristi Palmer, the IR4 Ornamental Hort program manager. Cristi would like to discuss
with you pollinator safety and ornamental plants.
Hope all is well,
Keith
This electronic message contains information generated by the USDA solely for the intended
recipients. Any unauthorized interception of this message or the use or disclosure of the
information it contains may violate the law and subject the violator to civil or criminal
penalties. If you believe you have received this message in error, please notify the sender and
delete the email immediately.
From:
To:
Subject:
Date:
Epstein, David
rmcallister@croplifeamerica.org
RE: US EPA notified USDA-OPMP re: Oregon
Friday, June 28, 2013 6:21:00 PM
Ray,
There was no post. The email, below was sent to the IPM Centers and was distributed from there. The
safety info came straight from an EPA manual.
David
From:<Epstein>, David <David.Epstein@ARS.USDA.GOV>
Date:Friday, June 28, 2013 8:26 AM
Subject:FW: ACTION: Outreach needed
IPM Colleagues,
(b) (5)
With agricultural production in full swing all across the country, OPMP requests your assistance through
outreach and education to remind all users of pesticides of the importance of following the label. This
helps to ensure good pest management while protecting wildlife, their habitat, and the environment. It
is especially important that urban gardeners and homeowners, who may not be as familiar with the
content of the label, have access to this important information. We are requesting your assistance in
communicating this information to your communities. Information could include the following:
Use of any pesticide in any way that is not consistent with label directions and precautions is
illegal. It may also be ineffective and dangerous. The basic steps in reducing pesticide risks are:
Choose the form of pesticide best suited to your target site and the pest you want to control:
o First, identify the problem correctly and then, choose the least-toxic pesticide that will
achieve the results you want and be the least toxic to you and the environment.
o When the words broad-spectrum appear on the label, this means the product is effective
against a broad range of pests. If the label says selective, the product is effective against
one or a few pests.
o Read the label before buying the pesticide, read the label before mixing or using the
pesticide each time, and read the label before storing or disposing of the pesticide.
Determining the right amount to purchase and use: do not assume that using more pesticide
than the label recommends will do a better job. It wont.
Find the signal wordeither Danger, Warning, or Caution on the pesticide label. The signal
word tells you how poisonous the product is to humans.
Choose the form of pesticide (aerosol, dust, bait, or other) best suited to your target site and the
pest you want to control. Certain formulations work better for some pests and/or some target
areas than others
Using the product safely and correctly:
o Never apply pesticides outdoors on a windy day (winds higher than 10 mph)
o Wear protective clothing, dont smoke or eat

o Mix and apply only the amount you need
o Watch for negative effects on wildlife (birds, butterflies, and bees) in and near treated
areas. If you see any unusual behavior, stop using that pesticide, and contact EPAs
Pesticide Incident Response Officer
Store and dispose of pesticides properly.
o Follow all storage instructions on the pesticide label.
o Always store pesticides in their original containers, complete with labels that list
ingredients, directions for use, and first aid steps in case of accidental poisoning.
State and local laws regarding pesticide disposal may be stricter than the federal requirements on the
label. Be sure to check with your state or local solid waste agency before disposing of your pesticide
containers.
From:
To:
Subject:
Date:
Epstein, David
jean.reimers@bayer.com
RE: Update on Calypso cancellations
Tuesday, February 04, 2014 9:39:31 PM
Agreed. I'll have to check with my sources.

Sent from my Android phone using TouchDown (www.nitrodesk.com)
-----Original Message----From: Jean Reimers [jean.reimers@bayer.com]
Received: Tuesday, 04 Feb 2014, 11:16am
To: Epstein, David [David.Epstein@ARS.USDA.GOV]
Subject: Re: Update on Calypso cancellations
Lucky you. We are supposed to get more ice here tonight.

I checked on Calypso and it is registered on pome fruits, stone fruits and peppers;
so I don't understand the concerns of the walnut growers. I suggest we wait and
see if any more concerns are raised but for now it seems to be quiet. Agree?
Sent from my iPad
On Feb 4, 2014, at 10:36 AM, "Epstein, David" <David.Epstein@ARS.USDA.GOV>
wrote:
No ice here in FL. Visiting my parents.
Received: Tuesday, 04 Feb 2014, 8:20am
To: Epstein, David [David.Epstein@ARS.USDA.GOV]
Subject: RE: Update on Calypso cancellations
Thanks for the clarification. I will pass this along and see if we are hearing anything from
them. Be careful on the ice tonight and tomorrow. Sounds like were going to get
another winter storm.
Jean Reimers
Director, Government Relations
Bayer CropScience
701 Pennsylvania Avenue, NW
Suite 720
Washington, DC 20004
Tel: 202-756-3779
Fax: 202-628-6622
Mobile:(b) (6)
E-Mail: jean reimers@bayer.com
Please visit our anniversary website:

Bayer: 150 Years Science For A Better Life

Sent: Monday, February 03, 2014 8:02 PM
To: Jean Reimers
Subject: RE: Update on Calypso cancellations
Jean,
Primary concerns came from walnut growers.

David
Received: Monday, 03 Feb 2014, 10:18am
To: Kunickis, Sheryl [Sheryl.Kunickis@ARS.USDA.GOV]; Epstein, David
[David.Epstein@ARS.USDA.GOV]
CC: jvroom@croplifeamerica.org [jvroom@croplifeamerica.org]; Barbara Glenn
(BGlenn@croplifeamerica.org) [BGlenn@croplifeamerica.org]
Subject: Update on Calypso cancellations
Following our recent phone call, (b) (5)
(b) (5)
(b) (5)
(b) (5)
Hope this answers the remaining questions. Please let me know if you need
additional information.
Jean Reimers
Bayer CropScience
Suite 720
Tel: 202-756-3779
Fax: 202-628-6622
Mobile: (b) (6)

The information contained in this e-mail is for the exclusive use of the intended recipient(s) and may be confidential,
proprietary, and/or legally privileged. Inadvertent disclosure of this message does not constitute a waiver of any
privilege. If you receive this message in error, please do not directly or indirectly use, print, copy, forward, or
disclose any part of this message. Please also delete this e-mail and all copies and notify the sender. Thank you.
This electronic message contains information generated by the USDA solely for
the intended recipients. Any unauthorized interception of this message or the use
or disclosure of the information it contains may violate the law and subject the
violator to civil or criminal penalties. If you believe you have received this
message in error, please notify the sender and delete the email immediately.
From:
To:
Subject:
Date:
Attachments:
Epstein, David
"Moriarty.Thomas@epamail.epa.gov"; Johansen, Erik (AGR); mverdercarlos@cdpr.ca.gov
RE: Statements used by EPA to protect pollinators from exposure to pesticides
Tuesday, January 15, 2013 7:59:00 AM
image001.gif
Tom,
(b) (5)
Please keep us posted

on your discussions with Tom, Meredith and management.
Dave
From: Moriarty.Thomas@epamail.epa.gov [mailto:Moriarty.Thomas@epamail.epa.gov]

Sent: Tuesday, January 15, 2013 7:48 AM
To: Johansen, Erik (AGR); mverdercarlos@cdpr.ca.gov; Epstein, David
Subject: Re: Statements used by EPA to protect pollinators from exposure to pesticides
Eric, Marylou, David,
(b) (5)
(b) (5)
(b) (5)
Thoughts?
tom m
"Johansen, Erik (AGR)" ---01/14/2013 08:23:52 PM---Hi Marylou and David, I think that our
conversation on January 4 regarding the terms "foraging" and
From: "Johansen, Er k (AGR)" <EJohansen@agr.wa.gov>
To: "mverdercarlos@cdpr.ca.gov" <mverdercarlos@cdpr.ca.gov>, "David.Epstein@ARS.USDA.GOV"
<David.Epstein@ARS.USDA.GOV>
Cc: John Scott <John.Scott@ag.state.co.us>, Cindy Baker-Smith <CindyS@amvac-chemical.com>, Iain Kelly <iain.kelly@bayer.com>,
Steve Coy (b) (6)
>, Joel <jnelsen@cacitrusmutual.com>, "dparker@cotton.org" <dparker@cotton.org>, Ray
McAllister <RMcAllister@croplifeamerica.org>, Connie Hart <connie.hart@hc-sc.gc.ca>, "joseph.bagdon@ma.usda.gov"
<joseph.bagdon@ma.usda.gov>, "Willett@nwhort.org" <Willett@nwhort.org>, "skegley@pesticideresearch.com"
<skegley@pesticideresearch.com>, Rick Smith <beezmans@roadrunner.com>, "ScottSchertz@schertzaerial.com"
<ScottSchertz@schertzaerial.com>, (b) (6)
, "John Abbott" <john.abbott@syngenta.com>,
(b) (6)
"Tim.McPherson@usa.dupont.com" <Tim.McPherson@usa.dupont.com>, "Julie.Schlekau@valent.com" <Julie.Schlekau@valent.com>,
Mary Clock-Rust/DC/USEPA/US@EPA, Thomas Moriarty/DC/USEPA/US@EPA
Date: 01/14/2013 08:23 PM
Subject: Statements used by EPA to protect pollinators from exposure to pesticides

(b) (5)
Take care,
Erik W. Johansen
Phone: (360) 902-2078
Fax: (360) 902-2093
WSDA is on Facebook and Twitter
From:
To:
Cc:
Subject:
Date:
Attachments:
Epstein, David
"Laura Phelps"; Pettis, Jeff
"Iain Kelly"
RE: spiromesifen and bee label language
Tuesday, January 24, 2012 3:29:00 PM
image001.jpg
Hi Laura,
Jeff and I met this afternoon to discuss the pollinators/labeling issues. Since Iain is coming by on
Thursday, I will update him then on our discussion.
Regards,
David
Entomologist, USDA Office of Pest Management Policy
Office: (202) 720-9877
Mobile: (b) (6)
From: Laura Phelps [mailto:laura.phelps@bayer.com]

Sent: Friday, January 20, 2012 3:04 PM
To: Epstein, David; Pettis, Jeff
Subject: RE: spiromesifen and bee label language
Dear David, and Jeff,

Thank you so much for meeting with us the other week to discuss bee language. I am writing to see
what you latest thoughts on the issue might be. I know you discussed several things to possible do
including consulting with other USDAers, growers, and bee keepers. I believe there was even mention
of a survey. Please let us know if there is anything we can do to assist.
Thanks,
Laura
Sent: Tuesday, December 27, 2011 10:23 AM
To: Laura Phelps; Pettis, Jeff; Clive Halder; Iain Kelly
Ms. Phelps,
I can be available January 6 th 9-11 am; 1-3pm or January 10 th 9-11am. I will be at a conference Jan
11-15, and unavailable to conference call during this time.
Regards,
David

Office: (202) 720-9877
Mobile: (b) (6)

Sent: Tuesday, December 27, 2011 10:07 AM
To: Epstein, David; Pettis, Jeff; Clive Halder; Iain Kelly
Dr. Epstein,
Thanks so much. We would like to set up a conference call and web ex.
Let me know if any of the following dates might work for you-
January 6 th 9-11 am; 1-3pm

January 10 th 9-11am
January 12 th 1-3pm
January 13 th 1-3pm
Dr. Pettis- I assume you are on the east coast. Please let me know if this is not the case.
Laura Phelps
Regulatory Affairs, Insecticides
Bayer CropScience
2 T. W. Alexander Drive
RTP, NC 27709
office: 919-549-2302
mobil:919-352-8075
email: laura.phelps@bayer.com

Sent: Monday, December 19, 2011 10:32 AM
To: Laura Phelps
Ms. Phelps,
Thank you for the table. It was not shared with us when Ian, Dave and Dick came to meet with us at
OPMP. Id be glad to conference call with you and Dr. Pettis on this topic. Let me know what dates
and times you are suggesting.
Regards,
David

Office: (202) 720-9877
Mobile: (b) (6)

Sent: Monday, December 19, 2011 10:11 AM
To: Pettis, Jeff; Epstein, David
Subject: spiromesifen and bee label language
Hello Dr. Pettis and Dr. Epstein,

I am writing this letter to follow up on our (BayerCropScience) wish to consult with
you on bee language for the spirotetramat insecticide label. We were given your names
from Tom Steeger at EPA as good contacts to help develop mitigation criteria for different
crops. You recently met with Ian Kelly and Dave Fischer from Bayer and they hopefully
shared with you a table we are in the process of developing. We have presented this table
to EPA and would also like to have USDA input as well.
This current effort is geared for the spiromesifen label but our hopes are that the same
proposals can be used for different labels. For this compound we believe the majority of
the crops may not need mitigation language because they are either not attractive to bees,
bees are not used for pollination, or it is minor acreage. We need, however, to make sure
our crop specific research and assumptions are corroborated with the appropriate
governmental agencies. The General Hazard Statement reads as follows: This product is
toxic to bee larvae. See the "Directions for Use" section of this label for specific crop
application instructions that minimize potential risk to bee larvae. For specified crops the
use directions will read: Apply in evening or at night. For the majority of the crops however
we propose no mitigation language. We would like to discuss this.
The ultimate goal for the table is a tailored set of measures developed for a variety of
crops that can be consistently implemented. Our aim is to allow farmers to maximize the
potential of their existing cropland as well as best protect the entire lifespan of pollinators.
Please take a look at the draft attachment and then perhaps we could have a conference
call to further discuss.
Description: Laura
Laura Phelps
Regulatory Affairs, Insecticides
Bayer CropScience
2 T. W. Alexander Drive
RTP, NC 27709
office: 919-549-2302
mobil:(b) (6)
email: laura.phelps@bayer.com
From:
To:
Cc:
Subject:
Date:
Epstein, David
"iain.kelly@bayer.com"; Kunickis, Sheryl
"peg.cherny@bayer.com"; "jean.reimers@bayer.com"
Re: Slides from Bayer Meeting
Thursday, January 12, 2012 5:09:12 PM
Yes, sounds good.
From: Iain Kelly [mailto:iain.kelly@bayer.com]

Sent: Thursday, January 12, 2012 12:30 PM
To: Kunickis, Sheryl; Epstein, David
Cc: Peg Cherny <peg.cherny@bayer.com>; Jean Reimers <jean.reimers@bayer.com>
Subject: RE: Slides from Bayer Meeting
Great. Does 1.30 2.30 work for both you and David then?
Iain
From: Kunickis, Sheryl [mailto:Sheryl.Kunickis@ARS.USDA.GOV]

To: Iain Kelly; Epstein, David
Cc: Peg Cherny; Jean Reimers
1-4pm. Conflicts were morning and I eliminated an all day meeting.

To: Epstein, David; Kunickis, Sheryl
Sheryl it looked like you may have afternoon conflicts. Does anytime in the afternoon work for you?
Iain

To: Iain Kelly; Kunickis, Sheryl
Yes, afternoon is possible.

Thanks David, we have to be over at EPA by 10.30 does the afternoon work at all?
Iain

To: Iain Kelly; Kunickis, Sheryl
Iain,
Im interested in hearing the update. I have a meeting scheduled for 8:30-9:30 on 1/26. 10- 11
would work for me.
Regards,

Office: (202) 720-9877
Mobile:(b) (6)
Fax: (202) 720-3191

Sent: Wednesday, January 11, 2012 4:03 PM
Sheryl and David,
At our meeting in December on Pollinators/bees, we touched very briefly on seed treatment. Our
commercial and technology experts on seed treatment are giving Steve Bradbury and his OPP staff an
update on advances in seed treatment on the 26 th January. If you are interested we would be happy to
provide the same update to you. Ideally first thing in the morning of Jan 26 th (say between 9-10) or
just after lunch (1-2 or 2-3) would work best.
Could you please let me know if you would be interested and if any of the proposed timings would
work..
(David left you a vmail about it too).
Many Thanks,
Iain
________________________________________
Iain Kelly
Coordinator U.S. Bee Health Issues
Phone: +1 919-549-2552
Mobile: (b) (6)

From:
To:
Bcc:
Subject:
Date:
Epstein, David
"Dan Botts"
Kunickis, Sheryl
RE: Revised draft -- Neonoc project information for meeting with EPA
Dan,
Ill be there for the pre-meeting.
David
From: Dan Botts [mailto:Daniel.Botts@ffva.com]

To: hwbr@citrusrdf.org; mrgrs@ufl.edu; ben@unclematts.com; Tom Turpen; steve.olson@bayer.com;
john.taylor@syngenta.com; Smith, Jeffrey; eruckert@mwe.com; Dennis.Howard@freshfromflorida.com;
john.abbott@syngenta.com; Epstein, David
Cc: Don Brady; Richard Keigwin; bradbury.steven@epa.gov; Mike Aerts; Lucy Nieves
Subject: Revised draft -- Neonoc project information for meeting with EPA
To All:
This is the 2nd revised draft of the document to be used to guide the discussions with EPA on
Thursday. We will revise and extend based as necessary based on discussion Thursday morning at
the pre-meeting at McDermott, Wills & Emery in DC. Feel free to call or raise concerns prior to the
meeting. I am traveling and will have periodic connection to my email but will only be able to
respond in the evenings. For anyone interested in participating in the pre-meeting via conference
call, we will use (866) 453-5550, participant pin number 8020599. We will probably be able to
accommodate teleconferencing at the EPA at the same number.
I arrive in DC around 9:30 tomorrow evening and will be staying at the Marriott Crystal gateway in
Crystal City. The pre-meeting will be held at 600 13 th street, NW, Washington, DC starting at 10:00
am. we will head over to EPA around 2:45 to be able to clear security in time for the 3:30 meeting
at EPA. The meeting is scheduled for 3:30 - 5:00 pm.
Please let me know if you are going to attend the pre meeting so I can arrange for lunch.
Dan
Daniel A. Botts
Vice President, Industry Resources

Florida Fruit & Vegetable Association
Mailing Address:
P. O. Box 948153
Maitland, Florida 32794-8153
Street Address:
800 Trafalgar Court, Suite 200
Maitland, Florida 32751
(T): (321) 214-5200
(F): (321) 214-0210
(C): (b) (6)
From:
To:
Subject:
Date:
Attachments:
Epstein, David
"Iain Kelly"
RE: Recent Publications on Neonicotinoids
Tuesday, May 01, 2012 7:18:00 AM
Proposed Agenda 4 24 12.docx
Iain,
Ill read through the statements and get back to you. The conference agenda is attached.
David

Sent: Monday, April 30, 2012 11:02 PM
To: Epstein, David
Subject: Recent Publications on Neonicotinoids
David, at the CLA Spring Conference, I said we were reviewing the recent studies on neonicotinoids.
Attached dare our considerations of them. Would appreciate any comments you have.
We also discussed your upcoming October meeting. Could you send me a draft agenda?
Many Thanks,
Regards, Iain
________________________________________
Iain Kelly
Bee Health Team Lead
Phone: +1 919-549-2552
Mobile: (b) (6)
Draft Agenda:
National Stakeholders Conference on Honey Bee Health
Date: Scheduled for October 15-17, 2012.

Attendees: 150 attendees including: research scientists from federal and academic
laboratories, federal and state policy makers, and stakeholders from agricultural,
beekeeping, industry and NGO communities.
Venue: Sheraton Suites Old Town Alexandria, 801 North St. Asaph Street, Alexandria,
VA 22314
Conference Steering Committee: David Epstein, USDA-ARS-OPMP;
Tom Moriarty and Tom Steeger, USEPA; Kevin Hackett, USDA-ARS; Robyn Rose,
USDA-APHIS; Doug Holy, USDA-NRCS
Structure
Day 1
Plenary session
8:30AM 8:40AM: Welcome (David Epstein)
8:40AM 9:30AM: Keynote Speaker: Overview of the state of our pollinators,
and the role of the conference and participants
keynote speaker: May Berenbaum
9:30AM-10:40AM: Stakeholder Opening Comments
Presenters: Darren Cox, Beekeeper Representative to EPA
Pollinator Program Dialogue Committee; Dan Botts, Minor Crop
Farm Alliance; Gabrielle Ludwig, Almond Board of California; Dr.
Barbra Glenn, VP, Science and Regulatory Affairs, Crop Life
America; Laurie Davies Adams, Executive Director, North
American Pollinator Protection Campaign; Christi Heintz, Apis m
10:40AM 11:00AM: Break
Topic Presentations:
11:00AM 11:30AM: Current State of Knowledge of CCD and its Relation to

Honey Bee Health
Lead presenters: Jeff Pettis; Dennis vanEnglesdorp

11:30AM 12:00AM: Current State of Knowledge of Nutrition and Best
Management Practices
Lead presenters: Gloria De-Grandi-Hoffman; Nancy Moran
12:00PM 1:30PM:
Lunch
1:30AM 2:00PM: Current State of Knowledge of Pathogens and Best

Lead presenters: Dianna Cox-Foster; Jay Evans
2:00PM 2:30PM: Current State of Knowledge of Arthropod Pests and Best
Lead presenters: Dennis Van Englesdorf
2:30PM 3:00PM: State of Knowledge of Pesticides and BMPs
Lead presenters: Jim Frazier; Reed Johnson
3:00PM 3:30PM: Break
3:30PM 4:00PM: Current State of Knowledge of Bee Genetics, Breeding
and Best Management Practices
Lead presenters: Marla Spivak, Steve Shepperd
4:00PM 4:30PM: Current State of Knowledge of Bee Biology (MOVE UP IN
SCHEDULE??)
Lead presenters: Gene Robinson, Jay Evans
5:00PM 7:00PM: Mixer
Day 2
8:00AM 10:00AM: Break-Out Sessions
-
Nutrition and Best Management Practices
Pathogens and Arthropod Pests & Best Management Practices
Pesticides and Best Management Practices
Bee Genetics, Breeding, Biology and Best Management

Practices
10:20AM - 12:00PM: Break-Out Sessions

-
Nutrition and Best Management Practices
Pathogens and Arthropod Pests & Best Management Practices
Pesticides and Best Management Practices
Bee Genetics, Breeding and Best Management Practices
12:00PM 1:30PM: Lunch

1:30PM 3:10PM: Conference participants reconvene in general session
Workgroup Reports to the Whole:
1:30 2:15: Nutrition
2:15 3:00: Pests
Workgroup Reports to the Whole:
3:20 4:15: Pesticides
4:15 - 5:00: Bee Genetics, Breeding, Biology
Day 3
9:00AM 12:00PM: CCD Steering Committee meeting with research leaders to
revise CCD Action Plan
From:
To:
Cc:
Subject:
Date:
CHRISTIANSEN, JESSICA (AG/1000)

Epstein, David; "lda@pollinator.org"; "wbuhler@ncsu.edu"; JENKINS, DANIEL J (AG/1920); Kunickis, Sheryl;
"tva@pollinator.org"; "joseph.wisk@basf.com"
"clock-rust.mary@epa.gov"; Moriarty.Thomas@epamail.epa.gov; Pettis, Jeff
RE: Pollinator Summit:BMPs subgrp
Friday, January 25, 2013 5:33:05 PM
Hi all,
Ive captured some talking points toward our draft agenda we discussed yesterday. Please let me
know if you have any edits, additions, corrections, and I will send a final version to the larger steering
team ahead of Mondays call. I will also verbally present some more detail around the below on
Mondays call.
Something else to consider is socializing this summit with some key bee industry folks, to gain
alignment and keep building upon communications from such events as the October Bee Health
Stakeholder meetings. Just a thought to discuss with the larger team.
Thanks and have a wonderful weekend!

Jessie
P.S. I still sound like a dying bull frogbut a bit better so am hopeful to have a somewhat normal
voice back by Monday J
BMP section draft agenda:

Review of Best Management Practices / Stewardship tools
o Agricultural pesticide application
Seed Treatment BMPs
Propose to have Lisa Nichols present on the joint CLA/ASTA Seed
Treatment Stewardship Guide document
Spray Drift BMPs
Reaching out to the CLA Spray Drift team to inquire about a
presenter to cover the other non-seed treatment pesticide
application types
o Bee Industry BMPs
Jeff Pettis to present on mitigation of bee exposure to pesticides in and
outside of the hive
o Ensure there is an emphasis on how the various tools are interconnected across
multiple audiences (ag industry, bee industry, growers, regulators, academics, etc.)
Communication / Outreach / Education

o Creating a sustainable communication network is critical; that crosses and connects
various industries, growers, regulators, and special interest partners
There will be a lot of focus in this section on the actionable items (i.e.
education / outreach strategies; how to measure success behavioral
changes, not just passing along documents) with the BMP / educational
tools that are currently, or soon to be, available
o Wayne Buhler will present and we are reaching out to NAPCC (Laurie Adams or anther
representative) as well to present (possibly other presenters too!)
Review of pesticidestewardship.org and other similar resources

To: 'lda@pollinator.org'; 'wbuhler@ncsu.edu'; JENKINS, DANIEL J [AG/1920]; Kunickis, Sheryl;
'tva@pollinator.org'; 'joseph.wisk@basf.com'; CHRISTIANSEN, JESSICA [AG/1000]
Cc: 'clock-rust.mary@epa.gov'; Moriarty.Thomas@epamail.epa.gov; Pettis, Jeff
Subject: RE: Pollinator Summit:BMPs subgrp
I spoke with Jeff Pettis, he is willing to present BMPs for mitigating bee exposure to pesticides in
and outside of the hive.
Regards,
David
Office: (202) 720-9877
Mobile: (b) (6)
From: Epstein, David

Sent: Wednesday, January 23, 2013 11:15 AM
To: 'lda@pollinator.org'; 'wbuhler@ncsu.edu'; 'daniel.j.jenkins@monsanto.com'; Kunickis, Sheryl;
'tva@pollinator.org'; 'joseph.wisk@basf.com'; 'CHRISTIANSEN, JESSICA (AG/1000)'
Cc: 'clock-rust.mary@epa.gov'
Subject: Pollinator Summit:BMPs subgrp teleconference Thursday 24th 2pm: Teleconference phone
number 888-858-2144; access code 9514507
Hello All,
We will teleconference tomorrow, Thursday, Jan 24 at 2pm. I did not hear back from all of you
through the Doodle poll, but time necessitates scheduling based on those that did respond.
Teleconference phone number 888-858-2144; access code 9514507
Regards,


Office: (202) 720-9877
Mobile:(b) (6)
Fax: (202) 720-3191

To: 'lda@pollinator.org'; 'wbuhler@ncsu.edu'; 'daniel.j.jenkins@monsanto.com'; Kunickis, Sheryl;
'tva@pollinator.org'; 'joseph.wisk@basf.com'
Cc: clock-rust.mary@epa.gov
Subject: FW: Pollinator Summit: Steering Committee Next Steps
Folks,
Following up on last Fridays teleconference, I volunteered to organize a 2nd teleconference for this
week among those who agreed to work in the BMP sub-group, in advance of the next meeting of
the whole group on Monday the 28th. Please use the following url to a Doodle poll to choose a
date and time for the conference.
http://www.doodle.com/5znszx5v4x5hr22i
Regards,
David
Office: (202) 720-9877
Mobile:(b) (6)
From: Clock-Rust.Mary@epamail.epa.gov [mailto:Clock-Rust.Mary@epamail.epa.gov]

Sent: Saturday, January 19, 2013 8:19 AM
To: Clock-Rust.Mary@epamail.epa.gov
Subject: Re: Pollinator Summit: Steering Committee Next Steps
Hi Again, Just wanted to send this email list for the people and groups.
Cheers, Mary
Name
Laurie Adams
Wayne Buhler
David Epstein
SubGroup
BMP
BMP
BMP
Email
lda@pollinator.org
wbuhler@ncsu.edu
david.epstein@ars.usda.gov
Clive Halder
Dan Jenkins
Sheryl Kunickis
Andrew Lavigne
Janis McFarland
Lisa Nichols
Warren Richardson
Tom Van Arsdall
Joseph Wisk
Dust
BMP
BMP
Seed
Seed
Seed
Seed
BMP
BMP
Treatment
Treatment
Treatment
Treatment
clive.halder@bayer.com
daniel.j.jenkins@monsanto.com
Sheryl.Kunickis@ARS.USDA.GOV
alavigne@amseed.org
janis.mcfarland@syngenta.com
lnichols@amseed.org
warren.richardson@pioneer.com
tva@pollinator.org
joseph.wisk@basf.com
Mary Clock-Rust
US EPA, Office of Pesticide Programs
Phone: 703.308.2718
email: clock-rust.mary@epa.gov
Visit: http://www.epa.gov/pesticides/
-----Mary Clock-Rust/DC/USEPA/US wrote: ----To: clive.halder@bayer.com, tva@pollinator.org, warren.richardson@pioneer.com,
joseph.wisk@basf.com, richard_aucoin@hc-sc.gc.ca, daniel.j.jenkins@monsanto.com,
alavigne@amseed.org, wbuhler@ncsu.edu, Sheryl.kunickis@ars.usda.gov,
Connie.Hart@hc-sc.gc.ca, lda@pollinator.org, janis.mcfarland@syngenta.com,
Mary.Mitchell@hc-sc.gc.ca, lnichols@amseed.org, Jamie Green/R7/USEPA/US@EPA, Josh
Svaty/R7/USEPA/US@EPA, Lois Rossi/DC/USEPA/US@EPA, Donald
Brady/DC/USEPA/US@EPA, Anita Pease/DC/USEPA/US@EPA, Richard
Keigwin/DC/USEPA/US@EPA, Thomas Moriarty/DC/USEPA/US@EPA, Tracy
Lantz/DC/USEPA/US@EPA, Robert Mcnally/DC/USEPA/US@EPA
From: Mary Clock-Rust/DC/USEPA/US
Date: 01/18/2013 05:11PM
Subject: Pollinator Summit: Steering Committee Next Steps
Hi Everyone,
Thanks for your participation in the call today.
Here is how I understand the groups breaking down and the sub-bullets:
Seed Treatment Group
Preparation of Seed for treatment
Coatings and formulations
Application processes following treatment
Members:
Andrew Lavigne
Janis McFarland
Warren Richardson
Dust Group
Talc replacement
Equipment manufacturing design changes
Midwest study (NAPPC?) to investigate exposures during plantings
Member(s):
Clive Halder
BMPs Group
Intended Audience, Communication, availability of BMPs
BMPs related to work in pesticide application, for beekeeping and broader health
of bees
Education, other possible sub topics?
Members:
Wayne Buhler
Dan Jenkins
Dave Epstein
Joe Wisk
Laurie Adams
Please make an effort to meet or call your group next week (January 22-25) to clarify
and expand or edit subtopics and sub-bullets under each theme area. Please email Mary
with your thoughts and findings by Friday January 25.
Our next conference call will be January 28, at 12 noon EDT. We will use the same callin number: 1-866-299-3188. Code: 703-305-0392.
If you have any questions, please email or call me.
Thanks and have a great weekend.
Mary Clock-Rust
Phone: 703.308.2718
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From:
To:
Cc:
Subject:
Date:
Hackett, Kevin
Sonny Ramaswamy; Pettis, Jeff; Purcell, Mary; Kunickis, Sheryl; Epstein, David; Woteki, Catherine - OSEC;
Bartuska, Ann - OSEC; Fitzner, Michael; Broussard, Meryl C
Adamczyk, John; Scott, Roy
RE: Neonics and honey bee
Thursday, February 13, 2014 9:57:02 AM
This was modified from a message from John Adamczyk, who is lead on a one-year funded project with
the authors of the report:
We now have cooperative agreements with Gus et al. The data Gus and others show was funded by the
soybean promotion board and possibly from the National Cotton Council.
The have collected more data from plant structures, but lacked funding to run more samples for
neonicotinoid pesticide analysis. They have some funding from us to get more samples processed from
samples in the freezer and for some additional studies in the spring. We also will provide the bees and
expertise now to try and see what effects these low levels have on bee health. That is what they are
lacking.
Seed companies for years have said that neonics are not found in cotton pollen, so this data is not that
novel, but does provide some empirical data from non-industry sources.
Kevin
Kevin J. Hackett, Ph.D.
Senior National Program Leader
USDA/Agricultural Research Service
5601 Sunnyside Ave, 4-2222
Beltsville, MD 20705-5139
301-504-4680 (office)
301-504-6191 (fax)
Kevin.Hackett@ars.usda.gov
-----Original Message----From: Sonny Ramaswamy [mailto:bugswamy@icloud.com]
Sent: Wednesday, February 12, 2014 7:47 PM
To: Hackett, Kevin; Pettis, Jeff; Purcell, Mary; Kunickis, Sheryl; Epstein, David; Woteki, Catherine OSEC; Bartuska, Ann - OSEC; Fitzner, Michael; Broussard, Meryl C
Subject: Neonics and honey bee
Interesting finding.
http://entomologytoday.org/2014/02/06/neonicotinoids-barely-found-in-pollen-of-seed-treated-plants/
-Ciao,
Sonny
From:
To:
Subject:
Date:
Epstein, David
Pettis, Jeff; Kunickis, Sheryl
RE: Neonicotinoid Seed Treatment discussion and Its Impacts
Monday, July 16, 2012 7:08:00 AM
Jeff,
Sheryl and I will be attending the ISU event, as we will be in IA and NE that week for field trips to
cornfields and an atrazine watershed. Let me know what you decide.
Dave
From: Pettis, Jeff

Sent: Sunday, July 15, 2012 8:39 AM
Subject: RE: Neonicotinoid Seed Treatment discussion and Its Impacts
Sheryl,
I agree it looks like not all of us need to attend. Were you and David to be in the area (or at least
travelling) during that period? For me it would be a special overnight trip but I could do it.
Let me know what you think about your plans (you and David)and I may or may not attend.
Jeff
From: Kunickis, Sheryl
Sent: Tuesday, July 10, 2012 4:58 PM
Subject: Fw: Neonicotinoid Seed Treatment discussion and Its Impacts
David and Jeff,

This is the invitation to the pollinator meeting at ISU. It appears to be more of a "pollinator-related"
meeting... Not totally certain of the need for all to attend. Thoughts?
Sheryl
From: Wintersteen, Wendy [AEX S] [mailto:wwinters@iastate.edu]
Sent: Tuesday, July 10, 2012 02:58 PM
Subject: Neonicotinoid Seed Treatment discussion and Its Impacts
Iowa State University's College of Agriculture and Life Sciences and the Iowa Department of
Agriculture and Land Stewardship are hosting a discussion of neonicotinoid seed treatments
and potential impacts on beneficial insects.Dr. Steve Bradbury, Director, Office of Pesticide
Programs at the U.S. Environmental Protection Agency, will participate in the discussion.
Stakeholders representing farmers, seed companies, pesticide companies and formulators,
bee keepers, equipment manufacturers and state and federal agencies have been invited to
participate.
The format for this session will be informal. We hope to learn about what different groups
are doing to understand and address potential dust drift and collectively explore practical,
innovative opportunities for minimizing dust drift potential.
The session will be held on Thursday, July 26, from 10 a.m. to 3 p.m. at the ISU Memorial
Union's Gallery Room.A light lunch will be served.Parking is available for a fee in the
Memorial Union Parking Ramp. The following map link may be helpful for directions to the
Memorial Union, the Parking Ramp, and the Iowa State University campus:
http://www.fpm.iastate.edu/maps/default.asp?
zoom=3&xcenter=1779&ycenter=2410&background=map&xshow=1780&yshow=2410
If you are available to attend, please RVSP by Friday, July 20, by emailing or calling Trina
Zimmer attrina@iastate.eduor 515-294-2518.If you have any questions, please call us.
Sincerely,
Wendy Wintersteen, Dean Bill Northey, Secretary

College of Agriculture and Iowa Department of Agriculture and
Life Sciences Land Stewardship
Iowa State University
From:
To:
Cc:
Subject:
Date:
Attachments:
Iain Kelly
Epstein, David
David Fischer; Robyn Kneen
RE: Meeting with OPMP
BCS Position.pdf
David,
Looking forward to tomorrow. Robyn Kneen and David Fischer and I will be there.
Do I phone you when we get through security?
I also attach a position paper that was submitted to the European Commission by Bayer CropScience.
We can discuss more tomorrow.
Kind Regards, Iain
-----Original Message----From: Epstein, David [mailto:David.Epstein@ARS.USDA.GOV]
Sent: Thursday, January 24, 2013 10:30 AM
To: Iain Kelly
Subject: RE: Meeting with OPMP
Iain,
We're on for Wed at 10. I'll send a meeting invite, shortly.
David
-----Original Message----From: Iain Kelly [mailto:iain.kelly@bayer.com]
Sent: Thursday, January 24, 2013 8:02 AM
To: Epstein, David
Subject: Meeting with OPMP
David
My colleagues are available on the Morning of 30th January. 10 til 12 would work best for us if you are
available.
Iain
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Monheim, 2013-01-25
Bayer CropScience Comments on EFSA Conclusions on the Bee Risk

Assessment of Imidacloprid and Clothianidin
Content:
1. Executive Summary
2. Review of the EFSA Report
3. Country level activity not assessed in EFSA Reports
o Stewardship Measures
o Member State Monitoring Projects
4. Outlook and recommendations
5. Appendix
1. Executive Summary
Bayer CropScience does not believe that the new EFSA reports alter the quality and validity of the
existing risk assessments and the underlying data set for imidacloprid and clothianidin.
We have generated extensive safety data for our neonicotinoid-containing crop protection products.
These have been reviewed and approved by the competent EU and Member State authorities
reflecting the agro-environmental conditions in the respective member states.
The absence of any unacceptable risk by these products has been further demonstrated by
monitoring data under more recent practical use conditions from all over Europe.
There have been significant stewardship improvements implemented over the last 5 years.
Unfortunately risk mitigation measures were not considered in the EFSA reports, likewise EFSA
omitted comprehensive data sets and evidence available to them in their assessment.
Strict regulations for the approval of crop protection products have been put in force by competent
authorities on EU and member state level. However, the EFSA reports are based on only recently
published scientific opinion and guidance documents for risk assessment as well as for seed
treatment. Both guidance documents have not yet been discussed by the competent authorities and
are not yet in force.
The unfavorable risk conclusion of EFSA is not based on new information but just on the fact that
more conservative, but not yet validated, criteria have been applied. Furthermore, numerous studies
conducted under relevant field conditions in different member states were not considered in the
EFSA evaluation.
With the evaluation principles as applied here, such a risk would be concluded for any kind of plant
protection product.
Bayer CropScience has always been proactively working on closing data gaps and continues to be
open to constructive dialogue with the competent authorities, on all relevant points relating to the
safety of our products. We are convinced that our seed treatment uses, if applied according to the
label instructions, do not pose an unacceptable risk to bee colonies and are committed to the
continuous development and implementation of stewardship measures.
Page 2 of 13
2. Review of the EFSA Report

2.1 Bayer CropScience has generated extensive safety data for its neonicotinoid products
The EFSA Peer Review builds primarily on data which have been submitted in the context of
member state registrations of plant protection products. Our product data have been reviewed and
approved by the competent EU and Member State authorities reflecting the agro-environmental
conditions in the respective member states.
However, further relevant information is available at Member State level which complements the
registration data and is particularly related to seed abrasion dust and guttation. This information as
well as country-specific mitigation measures or label languages was not considered in the EFSA risk
evaluation. Furthermore, only selected publications have been taken into account for the risk
assessment, while others, such as those as provided by MS Germany to the PPR meeting in
November have not been used.
For many uses, EFSA identified data gaps even though data and/or reasoned cases had been
provided by the notifier which adequately addressed honeybee concerns. This discrepancy is
related to the applied data selection methodology which left any of the higher tier studies out of
consideration due to evaluation uncertainties (no approved methodology, conditions not
representative for the whole of the European Union). EFSA did not consider the series of higher
tier studies conducted under realistic agro-environmental field conditions in various European
member states. The risks identified are therefore solely based on their overly conservative
screening of tier 1 risk assessments. As a result, the large number of data gaps proposed by EFSA
is misleading and their conclusions prone to mis-interpretation.
2.2 EFSA Report relies on unvalidated risk assessment scheme

The risk assessment that has been applied by EFSA in their evaluation is based on the recently
published EFSA Scientific Opinion on the science behind the development of a risk assessment of
plant protection products on bees (EFSA Journal 2012; 10(5):2668) from which the new EFSA
Draft Guidance Document on bee testing and risk assessment (draft published September 2012)
has been developed. Also, elements from the not yet implemented new Seed Treatment Guidance
Document are applied.
Both guidance documents are still in the stage of peer review not yet finalized.
Accordingly, EFSA has applied a non-validated draft risk assessment scheme, which amounts to a
screening step designed to identify if a proposed plant protection product use has the potential to
pose a risk, and not to determine the significance or acceptability of such risks. As EFSA itself
commented in the Peer Review Response it is not appropriate for EFSA to indicate whether the
risks identified should be regarded as acceptable or not acceptable.
The lack of validation was also emphasized by member states during the short peer review process.
Since EFSA has applied new assessment criteria, inconsistencies between previous evaluations at
European and Member State level were both inevitable and unavoidable.
Page 3 of 13
During the commenting phase of this guidance document as proposed by EFSA, was estimated that
data gaps would exist for 96% of all plant protection products (herbicides, fungicides, insecticides
and plant growth regulators). Therefore the vast majority of products used in European food
production these products would be regarded by EFSA, applying the logic of the current evaluation,
as Risk Identified.
In summary, the risk conclusion of EFSA is not based on new information but on the fact that more
conservative, not yet validated, criteria have been applied. As a consequence, the EFSA
conclusion differs significantly from the risk evaluations performed at Member State level on the
basis of established and validated criteria which concluded an acceptable risk for authorized uses.
2.3 Long term studies conclude no risk in crops attractive or not attractive to bees
Bayer CropScience is convinced that the available very comprehensive database qualifies for a
weight-of-evidence approach, which is common practice for risk evaluations and which makes best
use of all available information. A weight-of-evidence approach has previously been applied at
Member State level and resulted in the conclusion of acceptable risks putting laboratory data into
context.
Bee attractive crops

Nectar- and pollen-rich plants are particularly important when considering risk assessment for seed
treatment due to their bee attractiveness. The sustainabilityof the use in oilseed rape for honey bees
has been confirmed in Europe where this crop is predominantly the winter variety. A multi-year
extensive monitoring programme performed in Germany (with about 1.4 Mio ha winter oil seed rape
in 2012 [www.ufop.de]) has also not identified any concerns related to neonicotinoids (Genersch et
al, 2010; Apidologie, 41(3), 332-352).
However, EFSA considered only tier 1 risk data which explains their conclusion of a risk to
honeybees from exposure to systemic residues in pollen and nectar of bee attractive crops, for
example oil seed rape. Furthermore, the risk conclusion is based on the assumption that
honeybees are exposed at all times to the highest single residue value ever recorded across all
studies, multiplied by a further correction factor. Under real conditions, foraging honeybees do not
exclusively consume freshly collected nectar but usually consume already processed nectar with
higher sugar concentration before leaving the hives (Visscher et al. J. Ins. Physiol 42, 1089-1094
(1996). This consumption behaviorresults in significantly lower dose rates as those calculated by
EFSA.
The discrepancy between such conservative tier 1 risk conclusions and facts from practical use is
demonstrated by the success of Bayer CropSciences spring oil-seed rape (canola) seed production
business in Canada. As the major breeder of these seeds, our business is dependent on crop
pollination and requires the use of many thousands of honey bee colonies each year. Every single
one of the fields used for seed production are sown from seeds treated with neonicotinoids for crop
Page 4 of 13
protection and no incidents of bee colony impact have ever been recorded since introduction of
neonicotinoids a decade ago1. In fact, the number of bee hives in Alberta, where most of the canola
is bred, increased from 148,000 in 1992 to over 274,000 in 2011.
Crops not attractive to bees

For crops not or less attractive to bees, the risk assessment should be carried outwith the same
vigor, but focused on other routes of exposure, such as abrasion dust and guttation. Although no
methodology is yet agreed, the methods are being refined based on experience obtained over
recent years and more information is becoming available to define and assess the potential risk. A
large number of studies have been performed by regulatory authorities and industry.
All available information referring to guttation confirms the acceptability of the risk for honey-bee
colonies and for beekeeping activities (see Pistorius et al. (2012): Assessment of Risks to Honey
Bees Posed by Guttation. Julius Khn-Archiv 437: 199 ff.).
The requirement to address guttation has only recently been included into the data requirements in
the new European plant protection regulation 1107/2009, which come into force from January 2016
for plant protection products. Bayer CropScience is committed to the development of appropriate
methodologies and to finalize studies and the associated risk assessments to fulfill this timetable.
In recent years, significant progress has been made in enhancing the quality of seed treatment to
reduce the occurrence of dust abrasion. The implementation of technical modifications to sowing
equipment, such as the use of deflectors, has further substantially reduced the risk posed by seed
treatment dust during the sowing operation. Additional improvements regarding the coating quality,
for example, are also expected within the next 1-2 years. Therefore, by the time the exposure to
abraded dust during sowing of treated seeds becomes a legally binding assessment criteria, which it
currently is not, assessment methodologies and relevant data sets should be established.
2.4 Conclusion
Numerous studies generated under realistic field conditions consistently show that neonicotinoid
seed treatment uses do not pose an unacceptable risk to honeybees. Member State authorizations
of our products are based on these field studies and appropriate risk mitigation measures, yet were
unfortunately omitted in the EFSA evaluation. Furthermore a novel, not yet validated risk
assessment approach has been applied.
Bayer CropScience is convinced about the safety of our products and that the existing data and
overall evidence allows a scientifically robust risk assessment.
Consequently, Bayer CropScience is fully committed to work with all competent authorities and
stakeholders to continue to validate appropriate methodologies and to improve and refine risk
assessment for honeybees.
1The
Statistics and Data Development Branch of Alberta Agriculture and Rural Development
Page 5 of 13
3. Country level activity not assessed in EFSA Reviews

3.1 Stewardship Measures
Seed treatments are one of the most environmentally friendly ways of applying an insecticide. In
recent years significant progress has been made in enhancing the quality of seed treatment from
the naked seed to the seed in the soil. Across the supply chain from industry right through to
farmers and professional contractors, we are all committed to the safe use of seed treatment
and handling of treated seed and are actively deploying stewardship measures to reduce the
impact on the environment to the minimum. The key measures in this regard are listed below:
a) Seed treatment from naked seed to coated seed
Significant efforts, including in-depth training, have been made to improve the
knowledge of the professionals doing the seed treatment using professional treatment
equipment.
The adherence of coating onto seeds has been significantly improved by removing dust
particles before treatment and thereby prevents dust particles being coated with active
substances.
The recipes for the components and the processes during seed treatment has been
optimized for adherence and resistance to abrasion.
The entire seed treatment process has to be carefully monitored and quality criteria have to be
established. A certification system should be with an independent auditing as described below.
A key criteria for seed quality is the abrasion resistance of treated seed, that is measured by
Heubach values and agreed both by European Seeds Association (ESA and the European Seed
Treatment Manufacturers. They ensure that treated seeds meet the established dust references
values which equal or improve on all Member State legal minimums (see Appendix 5.2).
The "European Seed Treatment Assurance (ESTA) scheme has been set up by ESA to assure that
seed treatment processes and treated seeds meet the requirements defined by legislators and
industry. The whole process from seed cleaning to final Heubach values of treated seed is
monitored and audited by an independent body (see Appendix 5.1 for further details).
The scheme is a trademark protected initiative and combines several elements that guarantee
professional, high quality seed treatment applications.
Page 6 of 13
This ESTA scheme builds on the good work initiated by the Seed Treatment Industry
Stewardship Steering Committee (STISSC). STISSC is a seed treatment industry stewardship
task force (current members: BASF, Bayer CropScience, Makhteshim, Syngenta), initiated in 2009
to implement stewardship measures for seed treatment in Europe.
Examples of ESTA accreditation include the dust control program (Plan qualit poussire) in France
and the SeedGuard certification for seed treatment plants in use in Germany.
b) Drilling Planting of the treated seed in the soil

There are many ways of planting the seed, differing in technical complexity:
- Vacuum-pneumatic seed separation (negative air pressure)
- Pneumatic seed separation using air streams (compressed air, positive air pressure)
- Mechanical seed separation (without air assistance)
Vacuum-pneumatic drills are very effective in delivering precise seed spacing, but result in more
dust dispersion. By adding specific deflectors to these drills a reduction of 90% dispersion is
achieved by directing the dust to the ground.
Deflector retro-fitting on already existing vacuum-pneumatic drills has been promoted by STISSC
(see point 3 below) since 2009, and 40,000 units have been installed since then. It is anticipated
that this will equate to a > 70% market coverage in Europeby 2014.The percentage is constantly
increasing, as leading manufacturers of vacuum-pneumatic sowing machines are now routinely
equipping their newly sold machines since 2012 with appropriate deflectors. A new ISO norm for
minimizing the effects of fan exhaust from pneumatic drilling systems is being rolled out by the
manufacturer association (ISO/TC 23/SC 3, implementation 2015), aspart of a continual drive for
best practice in drilling technology.
c) Putting theory into Good Practise

In order to emphasize the Good Practise imperative for
treated seed to end users huge efforts have been made to
train farmers and professional contractors in this area.
Furthermore, an EU-wide seed labelling initiative has been
rolled-out by ESA, supported by STISSC companies.
From sowing season 2011 onwards labels (which are
available in all 26 EU languages) have been attached to seed
bags, initially with corn and oilseed rape with the aim to
extend to all crops immediately. More information can be
found under www.euroseeds.org/esta.
Bayer CropScience has already provided 8,1 million safe use labels to its customers in 2012 and
will extend this to all crops.
Page 7 of 13
Significant progress has been made in enhancing the quality of the entire seed business.
As a company with an in-house expertise in all of the processes from seed to seed treatment to
seed handling and beyond, Bayer CropScience is in a unique position in our ability to drive
improvements through the entire chain.
We have been researching this area for many years and continue to look for improvements in
product formulation and the development of new and improved coating agents.
Across the supply chain from industry right through to farmers and professional contractors, we are
committed to the safe use of seed treatment and are actively deploying stewardship measures to
continuously improve the safety of this technology.
Page 8 of 13
3.2 Member State Monitoring Projects

The European Commission requested the European Food Safety Authority (EFSA) to assess the
risk for bees in the light of new scientific and technical knowledge and monitoring data based on
Article 21 of Regulation (EC) No. 1107/2009.
Since it is explicitly mentioned, it is surprising that monitoring datawere not considered during the
scientific review, and we are of the opinion that the EFSA review in its current form is not complete.
Evidence concerning the safety of plant protection products that comes from monitoring approaches
is particularly important since potential effects of the products under investigation are there
surveyed under realistic field conditions as resulting from uses underagronomic practice. In contrast
to laboratory or other lower-tier results, monitoring data have the advantage that they provide insight
into what happens in reality and do not require any extrapolation approaches which may bring in
uncertainties to the assessment.
In summary, regarding potential effects of neonicotinoids to bees, monitoring data from countries
across Europe provide a clear picture of sustainable use, even when the individual data sets may
have their limitations or shortcomings:
Incidents with neonicotinoids are, very low in number, and are invariable associated
withoccasional off-label uses; it is worthy of note, that neonicotinoids are considerably less
involved in bee incidents than many other classes of insecticidal compounds, including
pyrethroids and carbamates (see e.g. Thompson & Thorbahn 2009).
With the exception of a few cases of bee mortality that were caused by exposure of bees to
dust from seed treatment products and in which apparently poor seed treatment
qualitieshave been involved, only very few cases of intoxications of bees with neonicotinoids
are recorded in those countries where passive monitoring systems are existing.
Wherever active monitoring has been conducted that investigates factual or potential
exposure to neonicotinoids as a potential causal factor behind bee mortality, no correlations
have been found between colony losses and the exposure to neonicotinoids.
Thus, monitoring data from all over Europe clearly confirm that the use of neonicotinoid seed
treatment products under practical use conditions and if applied according to the label instructions
does not pose an unacceptable risk to bee colonies.
The table below (see Attachment page 13) presents an overview of European monitoring data
available to us, including that from projects that have not been taken into consideration by EFSA.
Page 9 of 13
4.
Outlook and recommendations
Bayer CropScience is ready to work with the European Commission and Member States in order to
take the necessary steps to address the outcome of the EFSA reports.
We have been proactively working on closing data gaps and continue to be open to constructive
dialogue with the competent regulatory authorities, in order to discuss all relevant points relating to
the safety of our products.
We are continuously improving stewardship measures of all our products and are ready to
significantly increase risk management measures to demonstrate safe use of our products.
The extensive stewardship measures that have been established in the field and are being
constantly improved throughout the seed treatment chain should hereby be taken into account
Monitoring has recently been recommended as an appropriate tool to determine the realistic
exposure of bees to neonicotinoid seed treatment products. Monitoring data from all over Europe
clearly confirm that the use of these products under practical use conditions does not pose an
unacceptable risk to bee colonies. These comprehensive data sets should be taken into account.
We recommend that by enforcing the Commission Directive 2010/21/EU this existing evidence
should be further increased with more monitoring activities addressing realistic use conditions.
Overall, it should be acknowledged, that bee health is a complex issue. The 2009 EFSA project
Bee mortality and bee surveillance in Europe suggested that there are many factors involved in the
causes of the decline in the bee population. Among those that have been considered the Varroa
mite is by far the most threatening factor for bee decline. Clearlyother bee diseases and pests, as
well as agricultural and beekeeping management practises may also contribute to honey bee health.
The various stakeholders involved have undertaken many actions to gain a better understanding of
the multiple factors that influence bee health and measures to improve it. Suchon-going actions
must be continued and where necessary reinforced, based on an appropriate assessment of the
possible risks for animal and human health and also risks for the environment.
Bayer CropScience is fully committed to contribute to these improvements and to taking a range of
actions, as outlined before.
However, it should be emphasised that such actions can only be successful if all interested
stakeholders take part in a constructive and transparent manner.
Page 10 of 13
5. Appendix:
5.1.
ESTA Scheme
The "European Seed Treatment Assurance (ESTA) scheme is a trademark protected ESA initiative and
combines several elements that guarantee professional, high quality seed treatment applications:
- a quality assurance charter (ESTA Standard) which provides the base for an independent
certification of treatment sites by accredited auditors
- a guidance for auditors (ESTA Checklist) to promote and simplify the harmonised use and
interpretation of the standard
- ESTA Governance
- defined maximum dust reference values
- a uniform testing protocol for these Heubach testing method
- recommendations for safe use labelling of treated seed and information to be supplied to users
consisting of a multilingual leaflet and individual safe use pictograms.
ESTA covers the following processes:
Page 11 of 13
5.2. Heubach dust reference values
Seed batches that exceed the Heubach reference dust value have to be reworked and will not be
released on the market.
Page 12 of 13
From:
To:
Cc:
Subject:
Date:
Epstein, David
rmcallister@croplifeamerica.org
Kunickis, Sheryl; Iain Kelly; Brinkmeyer, Ray; Barbara Glenn
RE: Meet with CLA Pollinator Issue Management Team?
Wednesday, October 31, 2012 1:52:00 PM
Ray,
Sheryl and I are scheduled for a meeting with EPA on ESA proximity analysis from 9-noon,
tomorrow. Sheryl will attend that meeting and I will instead come join you at CLA at 9AM to discuss
pollinators with your management team. See you at 9.
Regards,
David
Office: (202) 720-9877
Mobile:(b) (6)
From: Ray McAllister [mailto:RMcAllister@croplifeamerica.org]

Sent: Wednesday, October 31, 2012 1:33 PM
To: Epstein, David
Cc: Kunickis, Sheryl; Iain Kelly; Brinkmeyer, Ray; Barbara Glenn
Subject: Meet with CLA Pollinator Issue Management Team?
David:
I understand you have talked with both Iain Kelly and Ray Brinkmeyer today. We are interested in
having you and Sheryl meet with our Pollinator Issue Management Team for an hour or so tomorrow
(Thursday November 1), between 9 a.m. and noon (at your convenience), to review the outcome and
next steps for the Honeybee Health Conference, and subsequent USDA-EPA collaboration on
pollinator health issues. We realize this is very short notice, but want to take advantage of the
opportunity if you are available. Most of our members will be on the phone for the meeting (and you
are welcome to call in), but if you can come to our offices, we can get a few of the in-town folks
together.
Our offices are in a state of controlled disarray caused by major renovations in progress, but we can
still find a smaller conference room to accommodate us.
Ray S. McAllister, PhD
Senior Director, Regulatory Policy
CropLife America
202-872-3874 (office)
(b) (6)
(cell)
ray@croplife.us
This e-mail message may contain privileged and/or confidential information, and is intended to be received only by persons entitled to
receive such information. If you have received this e-mail in error, please notify the sender immediately. Please delete it and all
attachments from any servers, hard drives or any other media. Other use of this e-mail by you is strictly prohibited.
All e-mails and attachments sent and received are subject to monitoring, reading and archival by CropLife America and RISE. The
recipient of this e-mail is solely respons ble for checking for the presence of "Viruses" or other "Malware". CropLife America and RISE
accepts no liability for any damage caused by any such code transmitted by or accompanying this e-mail or any attachment.
From:
To:
Subject:
Date:
Epstein, David
"Steeger, Thomas"
RE: Literature Review
Monday, March 31, 2014 1:11:00 PM
Tom,
Yes, I will be in CA, and yes, conversations re involving IPM centers has been a discussion point of
both the Coordinating Committee (Im on it) and the farm management practices working group in
the intervening conference calls since the last meeting in Dec. I also suggested to the Coordinating
Committee that at least one rep from the State Apiarists, State lead agencies, and from PSEPs be
involved. Trying to cover all of the bases. All input is welcome.
Dave
From: Steeger, Thomas [mailto:Steeger.Thomas@epa.gov]

Sent: Monday, March 31, 2014 1:00 PM
To: Epstein, David
Subject: RE: Literature Review
Daveit my understanding that you will be attending the Keystone Coalition meetings in-person
this week. One thing that does not seem to have been touched on in the discussions is the potential
role that the Coalition might play in coordinating discussions between regional IPM Centers, state
apiary inspectors and beekeepers/growers. The IPM centers likely represent a sufficiently regionspecific presence that they may be able to contour spatially specific plans to meet specific crop
production needs. Thoughts?
Tom

Sent: Monday, March 31, 2014 11:52 AM
To: Steeger, Thomas
Subject: RE: Literature Review
Tom,
I have not forgotten about this report, just very busy. I did download and review the 19 papers the
CFS reviewed for this report, (b) (5)
doing a full lit search and will get an accounting to you as soon as I can.
dave
From: Steeger, Thomas [mailto:Steeger.Thomas@epa.gov]

Sent: Tuesday, March 25, 2014 8:04 AM
To: Epstein, David
Subject: Literature Review
Greetings Dave,
I would be interested in learning your perspective on the attached "literature review" by the
Center for Food Safety examining the benefits associated with the use of neonicotinoids.
Tom
From:
To:
Cc:
Subject:
Date:
Epstein, David
Purcell, Mary; Hackett, Kevin
Kunickis, Sheryl
RE: Invitation to participate in 2013 CLA/RISE Spring Conference
Wednesday, February 20, 2013 9:55:00 AM
Mary,
Let me discuss this with Sheryl. I have no experience with the clearance process at USDA to predict
when the report will be cleared. My EFSA presentation consisted of a collection of bullet points
pulled from the draft report. I am confident we can pull together a presentation for Sonny from
what we have.
Dave
From: Purcell, Mary

Sent: Wednesday, February 20, 2013 9:48 AM
To: Epstein, David; Hackett, Kevin
Subject: FW: Invitation to participate in 2013 CLA/RISE Spring Conference
Dave and Kevin,

See email thread below. (b) (5)
Dave, could we give him your presentation (was it written

down?) I could take your presentation and distill it down into talking points for him.
Mary Purcell-Miramontes, Ph. D.
Dr. Mary Purcell-Miramontes

National Program Leader
USDA-NIFA
Institute of Food Production and Sustainability
800 9 th street, SW, Room 3438
Washington DC 20024
Voice (202) 401-5168
Fax (202) 401-6488
Agency website: http://www.nifa.usda.gov
Investing In Science | Securing Our Future
For notification of future NIFA RFAs released on www.grants.gov:
Register at http://www.grants.gov/search/subscribeAdvanced.do
Be sure to use the correct CFDA Number; AFRI= 10.310 ; SBIR = 10.212; Higher Education Challenge Grants
="10.217"
CFDA numbers for other programs are on the NIFA website
From: Ramaswamy, Sonny

Sent: Wednesday, February 20, 2013 9:21 AM
To: Purcell, Mary
Cc: Fitzner, Michael; Sheely, Deborah; Lucas-Brown, Donita; Martin, Jennifer
Subject: Fwd: Invitation to participate in 2013 CLA/RISE Spring Conference
Mary. Would you be able to arm me with the report and talking points? Maybe reach out to
Epstein, Hackett, et al?
If possible a couple weeks before you, Jenny and I can get together and brainstorm.
Thanks.
-
Sonny Ramaswamy, Director
National Institute of Food and Agriculture
United States Department of Agriculture
Begin forwarded message:
From: Barbara Glenn <BGlenn@croplifeamerica.org>
Date: February 19, 2013, 3:26:24 PM EST
To: "Ramaswamy, Sonny (sonny@nifa.usda.gov)" <sonny@nifa.usda.gov>
Cc: Barbara Glenn <BGlenn@croplifeamerica.org>, Melanie Rogers
<MRogers@croplifeamerica.org>
Sonny,
Melanie will contact Danita today or early tomorrow.
The invitation to speak is during the session focusing on pollinator issues to be held on
April 18 at 1:30 3:15 pm. Other panelists include Dick Rogers, Bayer CropScience,
Mace Vaughn Xerces Society, and Zac Browning, Browning Honey Company. Mace is
invited to moderate.
Sonny, we would love for you to share the results of the USDA EPA Stakeholder
Conference report. The research direction is of critical importance to CLA. Our
pollinator issue management team has met with Kevin, Jeff and Mary Miramontes
Purcell, but we thought that you would best summarize the nuggets for the future
direction, getting past the old CCD Steering Committees work.
Again, Melanie will talk to Danita. We have receptions on both evenings so would love
to see you at one of these as well. I would recommend the one on April 18 at 5:30 pm
after you speak.
Thank you for considering the invitation! Lets keep talking.
Regards,
Barb
Barbara P. Glenn, Ph.D.

Senior Vice President, Science and Regulatory Affairs
CropLife America
1156 15th St. NW
desk (202) 833 4474
cell (b) (6)
fax (202) 463 0474

bglenn@croplifeamerica.org
www.croplifeamerica.org
From: Melanie Rogers

Sent: Tuesday, February 19, 2013 9:20 AM
To: Barbara Glenn
Regards,
Melanie A. Rogers
Administrative Assistant, Science and Regulatory Affairs
CropLife America
From: Ramaswamy, Sonny [mailto:sonny@nifa.usda.gov]
Sent: Thursday, February 14, 2013 8:01 PM
To: Barbara Glenn
Cc: Melanie Rogers; Lucas-Brown, Donita; Barbara Glenn
Subject: Re: Invitation to participate in 2013 CLA/RISE Spring Conference
Barbara. I'm confused. Is the pollinator session on April 17 or 18?
Also shouldn't you invite Kevin Hackett or Jeff Pettis to do the honey bee lecture? They
have better experiences than I.
-Sonny Ramaswamy
USDA-NIFA
On Feb 14, 2013, at 6:52 PM, "Barbara Glenn" <BGlenn@croplifeamerica.org> wrote:

Sonny,
Great! It would be super to see you at our kick off session regarding
conservation and the networking reception on April 17.
By way of clarification, we are inviting you to speak on USDA pollinator

research priorities stemming from the National Stakeholder Conference.
We expect that the report will be final by that time. The session is on
Thursday April 18 in Crystal City. We have a dynamic pollinator session
and this is a hot topic for growers , industry, and agencies.
We know that as an entomologist you have unique expertise in these

issues and would look forward to getting you involved in a discussion -/
believe one speaker is a bee keeper leader and one from Xcerces Society.
Thank you for letting us know if you can speak April 17!
Barb
Sent from my iPhone
On Feb 13, 2013, at 1:26 PM, "Ramaswamy, Sonny"
<sonny@nifa.usda.gov> wrote:
Hi Barbara. Thanks for the kind invitation for a very
interesting program.
I will try to attend the plenary session and the reception

starting at 4:00 pm on April 17.
See you then, if not before.
Thanks, again.
--
Sonny Ramaswamy
Director, National Institute of Food and Agriculture
United States Department of Agriculture
305-A, Jamie L. Whitten Building
1400 Independence Ave, SW
E:sonny@nifa.usda.gov
T: 202-720-4423
F: 202-720-8987
I:http://www.nifa.usda.gov
From: Barbara Glen <bglenn@croplifeamerica.org>

Date: Tuesday, February 12, 2013 4:11 PM
To: "Ramaswamy, Sonny" <sonny@nifa.usda.gov>
Cc: Melanie Rogers <MRogers@croplifeamerica.org>
Subject: Invitation to participate in 2013 CLA/RISE Spring
Conference
Good afternoon,
Attached please find a formal invitation to participate in

our pollinator session at our annual CropLife
America/RISE Spring Conference. Our conference
always provides the latest information on crop
protection and specialty pesticides, so we look forward
to including you on the program.
Additional information can be found on our website

here. Thank you for considering our invitation to
participate!
Barb
Barbara P. Glenn, Ph.D.

Senior Vice President, Science and Regulatory Affairs
CropLife America
1156 15th St. NW
desk (202) 833 4474
cell(b) (6)
fax (202) 463 0474

bglenn@croplifeamerica.org
This e-mail message may contain privileged and/or confidential information, and
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Please delete it and all attachments from any servers, hard drives or any other
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All e-mails and attachments sent and received are subject to monitoring, reading and archival by
CropLife America and RISE. The recipient of this e-mail is solely respons ble for checking for the
presence of "Viruses" or other "Malware". CropLife America and RISE accepts no liability for any
damage caused by any such code transmitted by or accompanying this e-mail or any attachment.
This e-mail message may contain privileged and/or confidential information, and is intended to be received only by
persons entitled to receive such information. If you have received this e-mail in error, please notify the sender
immediately. Please delete it and all attachments from any servers, hard drives or any other media. Other use of
this e-mail by you is strictly prohibited.
All e-mails and attachments sent and received are subject to monitoring, reading and archival by CropLife America
and RISE. The recipient of this e-mail is solely responsible for checking for the presence of "Viruses" or other
"Malware". CropLife America and RISE accepts no liability for any damage caused by any such code transmitted by
or accompanying this e-mail or any attachment.
From:
To:
Subject:
Date:
Epstein, David
Coble, Harold; Fowler, Dianne; Kunickis, Sheryl; Rogers, Ted; Schechtman, Michael; Chin, Teung F. - APHIS
RE: Honeybees and neonicotinoids
Harold,
There are discrete bits of research information connecting declines in bee health with use of
neonicotinoid insecticides, but none of these researchers make the leap that the press does
that this means pesticides are the cause of CCD. The current consensus of the scientific
community is that pesticides are one factor associated with CCD, particularly where the
colony has been weakened by pests, poor nutrition and/or predators/pathogens.
The particular research cited in the article you sent identifies problems associated with a
particular application method for the insecticides clothianidin and thiamethoxam. I know one
of the researchers involved in the study, and he is a good scientist. The same application
method for clothianidin, cited in this report, was associated with a bee kill in Germany last
year. I believe that Bayer is now treating seed with these insecticides prior to planting to
mitigate concerns with exposure to bees. The USDAs Jeff Pettis also published research
identifying concerns with sub-lethal effects of clothianidin on bees a couple of years back,
and other research has also connected neonicotinoids with erratic navigational abilities of
foraging bees.
Just met this morning with Don Brady, Director of EPA EFED on this very topic at a meeting
of the National Cotton Council. He indicated that EPA is watching the development of the
science on neonics and bees closely, but sees no current scientific evidence that would
argue for more than mitigation tactics at this time.
David
From: Coble, Harold
To: Coble, Harold; Epstein, David; Fowler, Dianne; Kunickis, Sheryl; Rogers, Ted; Schechtman, Michael;
Chin, Teung F. - APHIS
Subject: FW: Honeybees and neonicotinoids
David,
What do you think about this?
From: Harold Coble [mailto:hdcoble@ncsu.edu]

To: Coble, Harold
Subject: Fwd: Honeybees and neonicotinoids
---------- Forwarded message ---------From: Robert Bellinger <BBLLNGR@clemson.edu>

Date: Tue, Jan 17, 2012 at 9:59 AM
Subject: Honeybees and neonicotinoids
To: Robert Bellinger <BBLLNGR@clemson.edu>
Cc: Joseph Krausz <JKRAUSZ@clemson.edu>
All,
FYI. Serious issue. Imidacloprid has also been implicated here. I got this particular item from
Dr. Joe Krauz, SC DPR.
Bob Bellinger
================================================
Robert G. (Bob) Bellinger, Ph.D.
Professor of Entomology & Extension Pesticide Coordinator;
Director, Pesticide Information Program;
Extension Pesticide Safety Education Program Coordinator;
Pest Management Information Program Coordinator;
Extension Entomologist, Specialist for Stored Grain Insect Management; Pasture & Forage Insects; Forest Insects
Teaching areas: IPM; Turfgrass Insects; Forest Insect Management; Agricultural Entomology; Insecticides
Entomology
Rm 107 Long Hall
340315, Clemson University
Clemson, SC 29634-0310
e-mail: bbllngr@clemson.edu
Voice: 864-656-5042, 3111
Fax: 864-656-0274
http://www.clemson.edu/extension/pest ed/ - Clemson Pesticide Information Program

http://www.clemson.edu/cafls/departments/esps/entomology/index.html - Clemson Entomology
http://www.clemson.edu/cafls/departments/esps/faculty_staff/entomology/bellinger.html- Bellinger Faculty Page
-Harold D. Coble, Ph.D.

Agronomist
USDA/ARS/OA
Office of Pest Management Policy
1730 Varsity Drive, Suite 110
Raleigh, NC 27606
Voice: (919) 513-0494
Fax: (919) 513-1114
email: hdcoble@ncsu.edu
From:
To:
Cc:
Subject:
Date:
Epstein, David
Pettis, Jeff; Hackett, Kevin; Serratosa, Jordi (FDA)
"Mary.Purcell@usda.gov"
RE: Honey bees docs and collaboration draft proposal
Wednesday, January 30, 2013 8:10:00 AM
Jeff,
The agenda for the meeting, 9am-11am, is below. I will be attending in person. I can check with Dr.
Serratosa if a conference line has been set up.
Dave
Draft the agenda for pollinators activities for a meeting between OPP and EFSA's
task force on pollinators nextFeb 7th 2013.
A. White paper : Risk Assessment framework.The document will be circulated
probably next week by Don Brady . Point should coverexchangeof viewsand the
implications for the Risk assessments in FDA and EFSA in case of divergent
opinions.
B.USDA proceedings report of the last Stakeholder meeting: The Steering
Committee for CCD (USDA/ARS / EPA) will finalize a position paper on
research priorities based on the last National Stakeholder meeting
conclusions.Kevin Hocket (chairman of the scientific Steering group) & /Don Brady
could be presenting the document.
C EFSA briefing about the next scientific opinion (global report) for May 2013
:Briefing from EFSAon the a global report to be presented in for May 2013 with
the support of the Task force on honey bees -
D. OECD Activities by FDA and EFSA in the working group - Pesticide Effects on
Insect Pollinators-
Exchange of views of the current activities for betterunderstanding andcooperation
D. Neonicotinoids Update of the activities and future steps in EFSA and EPA (Don
Brady and Richard Keigwin)
From: Pettis, Jeff

Sent: Tuesday, January 29, 2013 2:57 PM
To: Hackett, Kevin; Serratosa, Jordi (FDA)
Cc: 'Mary.Purcell@usda.gov'; Epstein, David
Subject: RE: Honey bees docs and collaboration draft proposal
Kevin,
I did not have this on my agenda but would like to call in and participate.
Can I get the call-in information when available?
Thanks,
Dr. Jeff Pettis

Research Leader
USDA-ARS Bee Research Laboratory
Bldg. 306 BARC-E
Beltsville, MD 20705 USA
E-mail jeff.pettis@ars.usda.gov
Phone 301 504-7299
Fax 301 504-8736
From: Hackett, Kevin

To: Serratosa, Jordi (FDA)
Cc: 'Mary.Purcell@usda.gov'; Epstein, David; Pettis, Jeff
Hi Jordi. Yes.
Jeff: Are you attending?
Kevin

301-504-4680 (office)
301-504-6191 (fax)
From: Serratosa, Jordi * [mailto:Jordi.Serratosa@fda.hhs.gov]

Sent: Monday, January 28, 2013 5:56 PM
To: Hackett, Kevin
Cc: 'Mary.Purcell@usda.gov'; Epstein, David
Dear Kevin
We are preparing the final agenda for the tele-conference next 7 Feb. Are you willing to be in cc ?
David has already confirmed . Is some other attendant from ARS ?
Best regards
Jordi
From: Hackett, Kevin [mailto:Kevin.Hackett@ARS.USDA.GOV]

To: Serratosa, Jordi *; Epstein, David
Cc: 'Mary.Purcell@usda.gov'
Hi Jordi,
David took the lead in putting together the meeting and the report. He should be the person
representing USDA on the call. I might also be able to participate by teleconference.
David: Are you available to present the results?
I have copied Mary, who is Co-chair of the CCD Steering Committee.
Kevin

301-504-4680 (office)
301-504-6191 (fax)

To: Hackett, Kevin; Epstein, David
Dear Kevin and David

We are planning a tele- meeting next 7 February at 9.00 am on Pollinators between
EPA (Don Braddy) and EFSA colleagues (task force pollinators. The draft agenda is
included below . Point number 2 of the agenda was to give an overview of the last
stakeholder meeting (giving for granted that the notes are available).
Are you interested to participate ? could you share before the 7 February the notes of
the last stakeholder meeting and the main conclusions ?
With my best wishes for 2013 !
Jordi
Draft the agenda for pollinators activities for a meeting between OPP and EFSA's
task force on pollinators nextFeb 7th 2013.
A. White paper : Risk Assessment framework.The document will be circulated

probably next week by Don Brady . Point should coverexchangeof viewsand the
implications for the Risk assessments in FDA and EFSA in case of divergent
opinions.
B.USDA proceedings report of the last Stakeholder meeting : The Steering
Committee for CCD (USDA/ARS / EPA) will finalize a position paper on
research priorities based on the last National Stakeholder meeting
conclusions.Kevin Hocket (chairman of the scientific Steering group) & /Don Brady
could be presenting the document.
C EFSA briefing about the next scientific opinion (global report) for May 2013
:Briefing from EFSAon the a global report to be presented in for May 2013 with
the support of the Task force on honey bees -
D. OECD Activities by FDA and EFSA in the working group - Pesticide Effects on
Insect Pollinators-
Exchange of views of the current activities for betterunderstanding andcooperation
D. Neonicotinoids Update of the activities and future steps in EFSA and EPA (Don
Brady and Richard Keigwin)
Dr. Jordi Serratosa
European Food Safety Authority "Liaison officer" at FDA
White Oak, Building 31 room 3438
10903 New Hampshire Avenue,
Silver Spring MD USA 20993
Tel 301 -79 68 387
Fax 301- 595 50 63
FDA e mail Jordi.Serratosa@fda.hhs.gov
EFSA e mail Jordi.Serratosa@efsa.europa.eu
From: Hackett, Kevin [mailto:Kevin.Hackett@ARS.USDA.GOV]

Sent: Tuesday, November 27, 2012 2:59 PM
To: Serratosa, Jordi *
Cc: Epstein, David
Jordi,
Thank you for sharing the report. You are quite a way ahead of us.
We are still working on our report from the meeting and have a meeting to discuss our report next
Monday. David is chairing that meeting, so he may want to comment.
I am not available Thursday for a call. Thanks for inviting me.
Kevin

301-504-4680 (office)
301-504-6191 (fax)
Sent: Tuesday, November 27, 2012 2:50 PM
To: Hackett, Kevin
Dear Kevin
Please find enclosed the report "inventory of EFSA activities on bees
http://www.efsa.europa.eu/en/press/news/121120a.htm.
I wonder if you have already finish the research priorities on pollinators ? . On Thursday
there will be a Public session on Pollinator protection organized by EPA and after the
meeting I have planned to will meet Don Braddy in Arlington to discuss a possible meeting
with EFSA on pollinators and future activities.
Would you like to be included in case we have a teleconference ?
Is there anything new to share ?
Best regards
Jordi
_____________________________________________
a, Jordi *
tober 19, 2012 5:30 PM
ett@ars.usda.gov
ney bees docs and collaboration draft proposal
<< File: Honey bee background doc EFSA tasks 2012-13 .pdf >> << File: Mission report Nat Stak
mtg Honey Bee Health 15-16 Oct 2012 Final .doc >>
Dear Kevin
It was a pleasure to talk to you this week at the pollinators meeting. As agreed I send you two docs
for your information. (b) (5)
(b) (5)
(b) (5)
Did I forget some intermediate steps ?

I was thinking to whom I should address this proposal or you can refine and distribute.
My contact lines in EPA are Steve Bradbury and Brady, in ARS I give for granted you are the contact
and Sheryl . Furthermore I could share it with FDA colleagues in CVM and FSIS could be interested
for the national residue monitoring plan (including bee diseases/vet med and residues in honey).
Looking forward your comments on the follow up
I wish you an excellent week end !
Jordi
Dr. Jordi Serratosa

European Food Safety Authority "Liaison officer" at FDA
White Oak, Building 31 room 3438
10903 New Hampshire Avenue,
Silver Spring MD USA 20993
Tel 301 -79 68 387
Fax 301- 595 50 63
FDA e mail Jordi.Serratosa@fda.hhs.gov
EFSA e mail Jordi.Serratosa@efsa.europa.eu
From:
To:
Subject:
Date:
Epstein, David
Kunickis, Sheryl
RE: Follow-up to discussion last week on neonic benefits project and presentation
Monday, April 14, 2014 11:11:00 AM
No idea. John asked me who with USDA may have knowledge regarding economic impacts
associated with the use of neonic treated seed, and I replied that we could check with ERS to see if
it was a question anyone had addressed.

Sent: Monday, April 14, 2014 10:32 AM
To: Epstein, David
Subject: RE: Follow-up to discussion last week on neonic benefits project and presentation
Who from ERS should be invited? I have been talking with Keigwin and will send the
invitation.

To: john.abbott@syngenta.com
Cc: Kunickis, Sheryl
Subject: RE: Follow-up to discussion last week on neonic benefits project and presentation
John,
I will discuss the ERS question with Dr. Kunickis and get back to you.
David
From: john.abbott@syngenta.com [mailto:john.abbott@syngenta.com]

To: Epstein, David; jbaron@AESOP.Rutgers.edu; Kunickis, Sheryl
Cc: Dan.Fay@valent.com; jamin.huang@bayer.com
Subject: Follow-up to discussion last week on neonic benefits project and presentation
David and Jerry,

Good to see you last week. Per our discussion last week (Sheryl, sorry we did not have a chance to
discuss this directly), a meeting date and time with EPA for AgInformatics to present the results of
their benefits assessment for the neonicotinoid insecticides has been set for April 30 th from 3-5. I
had suggested that I would contact you about having a similar meeting once this meeting was set
with EPA, PMRA and CDPR. However, EPA has suggested including you in the meeting they have
organized, which AgInformatics and the registrants support. I am sending this email just as a heads
up and they will be contacting you directly. Russell Wassem in PRD is organizing this meeting for
EPA.
David,
You indicated that it might be beneficial to have someone from ERS participate with the economic
aspects of this project. I would appreciate it if you could assist EPA with a contact.

Please let me know if you have any questions.
Regards,
John
This message may contain confidential information. If you are not the designated recipient, please notify the sender immediately, and
delete the original and any copies. Any use of the message by you is prohibited.
From:
To:
Cc:
Subject:
Date:
Epstein, David
"Charles Allen"; Mark Matocha
Kerns, David L.
RE: EPA and neonicotinoid seed treatments
Thursday, April 17, 2014 7:29:00 AM
Thank you, Charles. Much appreciated.
From: Charles Allen [mailto:ctallen@ag.tamu.edu]

Sent: Wednesday, April 16, 2014 7:32 PM
To: Mark Matocha; Epstein, David
Cc: Kerns, David L.
Subject: FW: EPA and neonicotinoid seed treatments
Mark and David Epstein,

(b) (5)
Charles Allen
Extension Entomology Program Leader/Assoc. Dept. Head
Professor and Statewide IPM Coordinator
Texas A&M AgriLife Research and Extension Center
7887 Highway 87 N
San Angelo, TX 76901
Phone: (325) 653-4576

Cell: (b) (6)
e-mail: ctallen@ag.tamu.edu
From: Kerns, David L. [mailto:DKerns@agcenter.lsu.edu]

Sent: Wednesday, April 16, 2014 2:27 PM
To: Charles Allen
Subject: RE: EPA and neonicotinoid seed treatments

Charles,
I dug up some AMT and Beltwide information I put together. There is a little more but I have run
out of time.
You can send it to the appropriate people, I do not have Marks email.
Best regards
David
David Kerns
Jack Hamilton Regents Chair in Cotton Production
LSU AgCenter Macon Ridge
212 A Macon Ridge Rd
Winnsboro, LA 71295
Phone: 318-435-2157
FAX: 318-435-2133
Cell: (b) (6)
From: Charles Allen [mailto:ctallen@ag.tamu.edu]

To: Kerns, David L.
Subject: FW: EPA and neonicotinoid seed treatments
David,
You may want to respond to this request. Do you have a thrips damage summary for High Plains
Cotton you could send Mark Matocha and David Epstein?
Charles Allen
Extension Entomology Program Leader/Assoc. Dept. Head
Professor and Statewide IPM Coordinator
Texas A&M AgriLife Research and Extension Center
7887 Highway 87 N
San Angelo, TX 76901
Phone: (325) 653-4576

Cell: (b) (6)
e-mail: ctallen@ag.tamu.edu
From: Mark Matocha

To: Raul Villanueva; Allen Knutson; Charles Allen; Pat Porter
Cc: Roy Parker
Subject: EPA and neonicotinoid seed treatments
Gentlemen,
(b) (5)
If you have data that supports efficacy of neonic seed treatments, published or otherwise, please
send it to (cc me):
David Epstein
USDA office of Pest Management Policy
David.Epstein@ars.usda.gov
David has to complete his response to EPA this week so if possible send any data you might have as
soon as possible. Sorry for the short notice but I was only made aware of this Friday afternoon.
Thanks,
Mark A. Matocha, PhD.

Assistant Professor and Extension Specialist
Texas A&M AgriLife Extension Service
115 Agronomy Field Lab
College Station, TX 77843-2488
979-845-3789
979-458-2777 (fax)
From:
To:
Subject:
Date:
Attachments:
Epstein, David
Kunickis, Sheryl
RE: CONFIDENTIAL: EPA action on labels to address bees
Wednesday, August 14, 2013 7:17:29 PM
image001.jpg
Made it to PSU.
-----Original Message----From: Kunickis, Sheryl [Sheryl.Kunickis@ARS.USDA.GOV]
Received: Wednesday, 14 Aug 2013, 4:47pm
To: MacMillan, Anne - OSEC [Anne.MacMillan@osec.usda.gov]; Harden, Krysta - OSEC
[Krysta.Harden@osec.usda.gov]; McFarland, Lilia - OSEC [Lilia.McFarland@osec.usda.gov];
McFarland, Lilia (OSEC) [lilia.mcfarland2@usda.gov]; Woteki, Catherine - OSEC
[Catherine.Woteki@osec.usda.gov]; Bartuska, Ann - OSEC [Ann.Bartuska@osec.usda.gov];
Ramaswamy, Sonny [sonny@nifa.usda.gov]; Knipling, Edward [Edward.Knipling@ARS.USDA.GOV];
Rexroad, Caird [Caird.Rexroad@ARS.USDA.GOV]
CC: Epstein, David [David.Epstein@ARS.USDA.GOV]; Pettis, Jeff [Jeff.Pettis@ARS.USDA.GOV];
Hackett, Kevin [Kevin.Hackett@ARS.USDA.GOV]
Subject: CONFIDENTIAL: EPA action on labels to address bees
(b) (5)
These pesticides are high benefit pesticides for the agricultural community. The hope is this
action will slow/stop the banning of these products by States.
FYI USDA scientists reviewed and commented on the draft label language.
Please let me know if there are questions.

Sheryl

Director
(202) 720-5375 Office

(b) (6)
Cell
From:
To:
Cc:
Subject:
Date:
Attachments:
Epstein, David
Mary Jo Tomalewski; Kunickis, Sheryl
Jean Reimers; Barbara Glenn; jvroom@croplifeamerica.org
RE: Conference Call Request
image001.jpg
I can be available either day and time
From: Mary Jo Tomalewski [mailto:mjtomalewski@croplifeamerica.org]

Cc: Jean Reimers; Barbara Glenn; jvroom@croplifeamerica.org
Subject: Conference Call Request
Sheryl and David,
I have been asked to schedule a conference call with you, Jean Reimers (Bayer) and Dr. Barb Glenn
(CLA), to discuss the impact of neonic label requirements by EPA.
Jean and Barb are both available at the following times:

Thursday, January 23, 4 or 4:30p
Friday, January 24, after 10a
The call will last between 45 and 60 minutes. Please let me know if these times would work for
you. I will then send an Outlook appointment with call-in information.
Thank you for your assistance.
Best regards,
MJ
Mary Jo Tomalewski
Executive Assistant to the President & CEO
CropLife America
1156 15th Street, NW
Suite 400
Direct Dial (202) 872-3849
Main Switchboard (202) 296-1585
Mobile (b) (6)
Fax (202) 349-1268
Email mjtomalewski@croplifeamerica.org
Web www.croplifeamerica.org
world in your hands
How can I serve you today?
This e-mail message may contain privileged and/or confidential information, and is intended to be received only by persons entitled to
receive such information. If you have received this e-mail in error, please notify the sender immediately. Please delete it and all
attachments from any servers, hard drives or any other media. Other use of this e-mail by you is strictly prohibited.
All e-mails and attachments sent and received are subject to monitoring, reading and archival by CropLife America and RISE. The
recipient of this e-mail is solely respons ble for checking for the presence of "Viruses" or other "Malware". CropLife America and RISE
accepts no liability for any damage caused by any such code transmitted by or accompanying this e-mail or any attachment.
From:
To:
Cc:
Subject:
Date:
Laws, Meredith
Andy Jensen; Rossi, Lois
Epstein, David
RE: bees, potatoes
Dear Dr. Jensen,
Thank you for your inquiry. At this time EPA does not have a list of crops or plants that are attractive
to bees. Its my understanding that a list is being developed by USDA. You may wish to contact Dr.
David Epstein at USDAs Office of Pest Management Policy. Ive copied him on this email. He may be
able to advise you.
Sincerely,
Meredith
Meredith Laws
Chief, Insecticide-Rodenticide Branch
Registration Division
Office of Pesticide Programs
(703) 308-7038
www.epa.gov/pesticides
From: Andy Jensen [mailto:ajensen@potatoes.com]

To: Rossi, Lois; Laws, Meredith
Subject: bees, potatoes
Ms. Rossi and Laws,
I work in research management for the potato industry in the Northwest. We have been concerned
about the future of neonicotinoids in potatoes. I have been asked to find the answer to a specific
question: Does the EPA have a list of crops or plants that are considered to be attractive to
pollinators? Or conversely, a list of crops NOT attractive to pollinators? We know that potato
flowers are rarely visited by bees, but wonder whether scientific documentation of this would be
important. Any existing opinions or lists from EPA regarding crops attractive to bees would
therefore be valuable.
Regards,
Andy
Andy Jensen, Ph.D.

Manager, Northwest Potato Research Consortium
4032 N Ballantyne Ln.
Eagle, ID 83616
Home Office: 208-939-9965

Cell: (b) (6)
Web: www.nwpotatoresearch.com
From:
To:
Subject:
Date:
Epstein, David
Kunickis, Sheryl
RE: Bee news
Thursday, March 20, 2014 1:58:00 PM
Wow! More than .5 million signatures!!!

Sent: Thursday, March 20, 2014 1:39 PM
To: Epstein, David
Subject: Bee news
Advocates' petitions seek ban of chemicals linked to bee deaths

Amanda Peterka, E&E reporter
Published: Thursday, March 20, 2014
This story was updated at 1:27 p.m. EDT.
Bee advocates today delivered more than half a million signatures to U.S. EPA Administrator Gina
McCarthy urging her agency to suspend the use of an insecticide linked to pollinator deaths.
About 25 advocates from several different organizations, many dressed in yellow-and-black-striped
costumes, posed in front of EPA's entrance this morning before heading in to deliver the signatures.
The event marked the one-year anniversary of a lawsuit filed by the Center for Food Safety and four
beekeepers against the agency over registration of the insecticide.
"We'd like EPA to suspend them until they're proven safe and protect pollinators," Larissa Walker,
policy and campaign coordinator at the Center for Food Safety, said outside EPA's headquarters. "We
feel like right now EPA is failing to do its job."
The groups delivering the petitions included Friends of the Earth, Pesticide Action Network North
America, Beyond Pesticides and Food Democracy Now.
Populations of honeybees and other pollinators have declined precipitously in recent years due to a
phenomenon known as colony collapse disorder. EPA and the Department of Agriculture last year
found that pesticides were a factor in colony collapse disorder, although the departments also cited
genetics, habitat loss, poor nutrition and disease (Greenwire, May 2, 2013).
CropLife America, which represents agribusiness interests, says there's no demonstrated link to bee
die-offs when neonicotinoid-based insecticides are used properly and that it is monitoring the use of
the chemicals.
But environmentalists are seeking a complete ban on the products until additional reviews are
completed. They allege that EPA rushed the neonicotinoids to market without proper review and has
not done enough to incorporate new findings.
The European Union has already banned neonicotinoids in an effort to save pollinators.
"Pollinator protection is one of EPA's highest priorities and we will review their petition," the agency
said in a statement. "EPA is working to protect bees and other pollinators from pesticide risks with a
diverse group of stakeholders to better [understand] factors associated with declining pollinator health."
Last August, EPA unveiled a new label for products containing certain neonicotinoids that includes
information on pollinator exposure and spray drift (E&ENews PM, Aug. 15, 2013).
Jim Doan, a beekeeper from New York and a plaintiff in the lawsuit against EPA, said in a statement
that the bee industry is at risk of collapsing without intervention by the government.
"Convening conferences and changing pesticides labels is lip service and window dressing to the issue,
but has no substance," he said.
From:
To:
Subject:
Date:
Jean Reimers
Iain Kelly; Epstein, David; Kunickis, Sheryl
RE: Bayer Statement on Calypso
David and Sheryl I have also passed on your questions and we are gathering the information. We
will get back to you on Monday.
Hope you have a good weekend and stay warm.
Jean Reimers
Bayer CropScience
Suite 720
Tel: 202-756-3779
Fax: 202-628-6622
Mobile: (b) (6)

From: Iain Kelly

To: Epstein, David (David.Epstein@ARS.USDA.GOV); Sheryl kunickis@ars.usda.gov
Cc: Jean Reimers
Subject: Bayer Statement on Calypso
David, Sheryl,
Understand you got a chance to discuss Calypso further with CLA and Jean today. Please see our
standby statement below. If I can send you any further information let me know. As discussed with
David we will keep you informed of any critical decisions we make in our products going forward so that
there are no surprises.
Best regards,
Iain
Standby Statement
Bayer CropScience has notified the Environmental Protection Agency (EPA) of its decision to
voluntarily cancel the registration of Calypso insecticide. This decision was based solely on an
examination of the products future registration study requirements, for which an economically
viable business case could no longer be supported. The decision to exit this business had nothing to
do with bee health. In fact, the performance profile of Calypso made its use particularly well-suited
to horticultural crops dependent on insect pollinators.
________________________________________
Iain Kelly, Ph.D.
Bee Health Issues Manager

Phone: +1 919-549-2552
Mobile: (b) (6)
From:
To:
Subject:
Date:
Attachments:
Epstein, David
Myers, Clayton
RE: Australian Overview Report regarding Neonicotinoid and the Health of Honey Bees in Australia
Monday, March 03, 2014 8:44:00 AM
image001.png
Thanks, I had not yet seen it.
From: Myers, Clayton [mailto:Myers.Clayton@epa.gov]

To: Epstein, David
Subject: FW: Australian Overview Report regarding Neonicotinoid and the Health of Honey Bees in
Australia
Im presuming youve already seen this, but thought I would forward just in case . . . .
From: Laws, Meredith

Sent: Friday, February 28, 2014 9:16 AM
To: Myers, Clayton
Subject: FW: Australian Overview Report regarding Neonicotinoid and the Health of Honey Bees in
Australia
HI Clayton I thought you might be interested in this report.
Meredith
From: Amy McCaskill [mailto:amy.mccaskill@bayer.com]

Sent: Thursday, February 27, 2014 4:35 PM
To: Laws, Meredith
Cc: Steeger, Thomas; Moriarty, Thomas
Subject: Australian Overview Report regarding Neonicotinoid and the Health of Honey Bees in Australia
Dear Ms. Laws,
I am a new Federal Registrations manager at Bayer CropScience reporting to Clive Halder. I am also
a member of our North American Bee Health Core Team. As pollinator protection is one of our core
product stewardship concerns, I am looking forward to working with you and your colleagues in the
future on these matters.
We wanted to bring to your attention an overview report that was developed by The Australian
Pesticides and Veterinary Medicine Authority and released on 19 February 2014. It is a broad
overview of the issues relating to honeybee health in Australia, however, there is a particular focus on
the use of neonicotinoid insecticides. We believe it is an objective and thorough overview of this topic.
I have attached it here and will also send a copy through the front desk.
Best Regards/Met vriendelijke groeten/Mit freundlichen Gren/Cordialement/Saludos Cordiales,
Amy McCaskill
Federal Regulatory Affairs
2 TW Alexander Drive
RTP, NC 27709
Phone: 919-549-2297
Mobile:(b) (6)
Fax: 919-549-2514
E-mail: amy.mccaskill@bayer.com
Web: http://www.bayercropscience.com
From:
To:
Subject:
Date:
Attachments:
Marylou Verder-Carlos
Epstein, David
PPDC-Request for Input
Friday, April 27, 2012 5:29:05 PM
Draft Proposal for PollinatorProtection Statements EWJ 03-25-2012.pdf
Comparison of pollinator protection statements 04-20-2012.pdf
Statements Table.pdf
David, here is the draft of what I am planning on sending Mary.

-------------------------------------------------------------------------Hello Mary,
(b) (5)
Another issue that needs to be addressed is there are definite practices that can impact crops that need
pollination and those crops that do not need pollination. Both of those groups of crops though will be
visited by bees or other pollinators. It may be very helpful then for the labeling language to be more
crop group specific (e.g. honey-producing, non-honey producing, or, citrus, trees and nuts, etc).
Lastly, we feel that improvement of the labeling language is not the only thing that needs to be done.
Protection of the pollinators has be done in concert with best management practices, outreach and
training and enforcement. Of course, with out consistent labeling language, enforcement will also be
very challenging.
-----------------------------------------------------------------------Let me know what you think, and please revise as need be. Thank you!
Marylou
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
From:
To:
Cc:
Subject:
Date:
Attachments:

Marylou Verder-Carlos; Epstein, David
John Scott; jcranney@calcitrusquality.org; dparker@cotton.org; rmcallister@croplifeamerica.org;
cbakersmith@gowanco.com; Bagdon, Joseph - NRCS, Amherst, MA; skegley@pesticideresearch.com;
schertz@schertzaerial.com; (b) (6)
timothy.wilson@syngenta.com; julie.schlekau@valent.com;
Mary Clock-Rust
Draft proposal for pollinator protection statements
Thursday, March 29, 2012 4:46:15 PM
Draft Proposal for Pollinator Protection Statements EWJ 03-25-2012.pdf
Hi Marylou and Dave,
I am sending you and the rest of the labeling subgroup a copy of the most recent version
(3/25/2012) of my draft proposal for pollinator protection statements. The primary changes were:
(b) (5)
Since I wrote this version of the draft proposal, there have been several emails among members in
the labeling subgroup regarding various suggestions or concerns with proposed labeling statements.
At this time I have not incorporated any of these comments, since I felt it might be helpful to see if
the revisions have resolved any of the concerns that were raised at the last subgroup conference
call. Unfortunately, I was unable to participate in the workgroup conference call this morning.
Take care,
Erik W. Johansen
Phone: (360) 902-2078
Fax: (360) 902-2093
WSDA is on Facebook and Twitter
(b) (5)
(b) (5)
(b) (5)
From:
To:
Cc:
Subject:
Date:
Attachments:
Clock-Rust, Mary
Clock-Rust, Mary; LDA@pollinator.org; john.abbott@syngenta.com; (b) (6)
;
aaverill@ent.umass.edu; Bagdon, Joseph - NRCS, Amherst, MA; CindyS@amvac-chemical.com;
lori@agbusinessresources.com; djb134@psu.edu; rbireley@cdpr.ca.gov; sblack@xerces.org;
sbrettha@illinois.edu; rsbrinkmeyer@dow.com; z browning@msn.com; wayne buhler@ncsu.edu;
acode@pesticide.org;(b) (6)
;(b) (6)
;
(b) (6)
Frank Drummond@umit.maine.edu; mduke@pestworld.org; peter.egan@osd.mil; Epstein, David;
jgray@state.nd.us;(b) (6)
t; nharriott@beyondpesticides.org; Connie.Hart@hc-sc.gc.ca;
christi@projectapism.org; Holy, Doug - NRCS, Rosslyn, VA; Rise, David; Anthony.M.Jadczak@maine.gov;
allan.james@midvalleyag.com; erik.janus@monsanto.com; ejohansen@agr.wa.gov;
skegley@pesticideresearch.com; iain.kelly@bayer.com; VJKramer@dow.com; gludwig@almondboard.com;
rmcallister@croplifeamerica.org; Tim.McPherson@usa.dupont.com; CAMullin@psu.edu; Joel Nelsen;
knye@michfb.com; cpalmer@abcbirds.org; dparker@cotton.org; Pettis, Jeff; lphelps@manainc.com;
markrisley@unitedsuppliers.com; ROWEB@Michigan.Gov; jsass@nrdc.org; julie.schlekau@valent.com;
john.scott@ag.state.co.us; mseetin@usapple.org; beezmans@roadrunner.com; tom@vanarsdall.com;
; mace@xerces.org; mverdercarlos@cdpr.ca.gov;
(b) (6)
lwalker@centerforfoodsafety.org; willett@nwhort.org; joseph.wisk@basf.com; danw@ndgga.com; Keigwin,
Richard; Brady, Donald; Pease, Anita; Moriarty, Thomas; Steeger, Thomas; Laws, Meredith; aimee@xerces.org;
Scott Schertz; Thomas, James (JD)
Winfield, Sarah
PPDC Pollinator Workgroup Session-Tomorrow-Thursday Dec 5
Wednesday, December 04, 2013 4:32:39 PM
Outline Slides for PPWG Presentation to PPDC 12-5-13.pptx
Hello PPDC Pollinator Protection Workgroup,
I hope that you had a nice Thanksgiving Holiday.
As you know, the full PPDC meeting (webinar) is tomorrow and Friday. The session pertaining to the
Pollinator Protection Workgroup takes place at 1:45 EDT until 3:15 EDT. I hope you can join the
webinar. See the PPDC website for details on the agenda and webinar instructions.
http://www.epa.gov/pesticides/ppdc/
The slides for the workgroup session are attached. If you have any questions before the session,
feel free to email me in the morning. The only workgroup members expected to speak are David
Epstein (Labeling SG) and Wayne Buhler (Education and Training SG). There may be some questions
for others, however, so I hope you will all participate.
Following the session, we can expect feedback from the full PPDC. I look forward to continue
working with you all.
Thank you for all of your hard work, patience and persistence on these important issues.
Cheers,
Mary
Mary Clock-Rust
Biologist
Environmental Fate and Effects Division
U.S. Environmental Protection Agency
703-308-2718
clock-rust.mary@epa.gov
(Email sent 11/21/13 follows)
Dear PPDC Pollinator Protection Workgroup,
I am attaching the draft agenda for the full PPDC meeting taking place December 5+6. The
Pollinator Protection Workgroup is scheduled to present to the full PPDC on December 5 (Thursday)
at 1:45 PM until 3:15 PM (EDT). As we mentioned in the call today, the PPDC meeting will be
conducted as a webinar. By following the instructions attached, you should be able to see
presentations and hear speakers talking through your computers speakers. If you are simply
listening to the PPDC meeting and viewing the slides being presented and you have computer
speakers, you should not need to call in. If your computer does not have speakers, then you can
access the audio by calling into the teleconference line at the top of the agenda.
For Subgroup Chairs who will be speaking only: The expectation is that the subgroup chairs will
present to the full PPDC during the time slot on December 5. For those that will be speaking, they
should call into the teleconference line and also be logged into the webinar. It is important that you
mute and unmute your phone as you speak or listen. Use #6 to mute and *6 to unmute when you
are speaking. Do not attempt to speak through your computer microphone.
For those of you on the very short call today, please accept my apologies for not introducing those
EPA staff that were present in the room here: Mary clock-Rust, Donald Brady, Anita Pease and
Thomas Moriarty.
Also, early next week I will be sending a list of accomplishments that the group has worked on since
it began (in 2011). The accomplishments will make up the content of the presentation to the full
PPDC as well as the groups overall recommendations.
If you have any questions, please let me know.
Cheers,
Mary
Mary Clock-Rust
Biologist
Environmental Fate and Effects Division
703-308-2718
clock-rust.mary@epa.gov
What is Bloom?
Beekeepers: Anytime a flower is open to bees for pollen and nectar.
Geography, topography, weather affect bloom timing bloom times for the
same crop can vary between regions within a state.
In CA Citrus, defined as 10% -90% of orchard in bloom; determined by
stakeholders including growers, beekeepers, pesticide applicators and the CAC
in the citrus district of where the groves are located
Concerns:
Crops with different cultivars planted together or in close proximity that
bloom at different times
Weed bloom
Extended Bloom: tomatoes, cucurbits, etc.
Extra-floral nectaries NOT a flower; require different language on a
pesticide label cotton has season-long nectar-producing parts of plants
Beekeepers: Pesticide notification rarely results in bee hive movement - is a
means of opening the line of communication between the beekeeper and
pesticide applicator
Growers: want balanced approach that enables the producer to protect his
crop/economic livelihood, while not creating undo stress on managed bees
SLAS: a label needs a stated, specific time period to be enforceable
Issues that Need to be Addressed for Using Bloom as a Reference

on a Pesticide Label
1) Any prohibition time (time before bloom during which a product cannot
be used) must be based on a robust risk assessment for an active
ingredient.
2)Need additional discussions regarding crops (e.g., cotton, tomato) that
have nectar-producing parts, pollen shedding, or are indeterminate
bloomers
3)Need broader discussions with SLAs regarding the enforceability of using
bloom in label language
4)Need to further discuss looking at the CA Citrus program as a model for
other crops, i.e., mechanisms and processes that would allow for
authoritative, local level implementation of the term bloom
Allows flexibility - specific to a commodity for a specific region
This type of flexibility does not seem possible at the level of the federal
label
Currently no state program which ensures that managed bees will not
be present in any treatment area
Proposal to PPDC is that use of bloom on a pesticide label may work,
however the Labeling Subgroup needs to address several issues related to
the use of the term bloom in order to preserve local flexibility while
providing enforceable protection for pollinators.
From:
To:
Subject:
Date:
Attachments:
Clock-Rust.Mary@epamail.epa.gov
clive.halder@bayer.com; tva@pollinator.org; warren.richardson@pioneer.com; joseph.wisk@basf.com;
daniel.j.jenkins@monsanto.com; alavigne@amseed.org; wbuhler@ncsu.edu; Kunickis, Sheryl; Epstein, David;
Connie.Hart@hc-sc.gc.ca; LDA@pollinator.org; janis.mcfarland@syngenta.com; Mary.Mitchell@hc-sc.gc.ca;
lnichols@amseed.org; jessica.christiansen@monsanto.com; Svaty.Josh@epamail.epa.gov;
Rossi.Lois@epamail.epa.gov; Brady.Donald@epamail.epa.gov; Pease.Anita@epamail.epa.gov;
Keigwin.Richard@epamail.epa.gov; Moriarty.Thomas@epamail.epa.gov; Lantz.Tracy@epamail.epa.gov;
Mcnally.Robert@epamail.epa.gov; Laws.Meredith@epamail.epa.gov; Steeger.Thomas@epamail.epa.gov
Pollinator Summit: Notes from Call on 2.7.13
Monday, February 11, 2013 11:11:10 AM
Preliminary Agenda Pollinator Summit.docx
Hello,
I have attempted to put together a proposed agenda for the Summit with time frames for the
various agenda items. Please see attached and let me know if you have any comments.
Action Items:
Please look at the draft/proposed agenda with speakers and timelines.
Are the speakers names correct, including spelling? Please add any needed
affiliations or other information.
Add sub-bullets for detail on the presentations if possible.
Please comment on the proposed time slots for each presentation. Is there enough
time, too much time?
For the BMP theme, is there a better title for this segment, aside from simply BMPs?
Also, Jessi and others, please give me titles of presentations and time needed for each.
Group Leads, please send Mary the following: 1) Number of people from each theme
group will be attending (so we can reserve seats for everyone)? 2) Speaker names; 3)
Send any comments and changes on the proposed agenda.
Our next call is this Wednesday, from 3:30 PM-4:30 PM. The call-in number is 1866-299-3188. Code: 703-308-2718.
Thanks!
Mary
Mary Clock-Rust
US EPA, Office of Pesticide Programs (See
Summit.docx)
Phone: 703.308.2718
attached file: Preliminary Agenda Pollinator
Notes from Steering Committee Call 2/7/13

Action Items:
Please look at the draft/proposed agenda with speakers and timelines.
Are the speakers names correct, including spelling? Please add any needed
affiliations or other information.
Add sub-bullets for detail on the presentations if possible.
Please comment on the proposed time slots for each presentation. Is there enough
time, too much time?
For the BMP theme, is there a better title for this segment, aside from simply
BMPs? Also, Jessi and others, please give me titles of presentations and time
needed for each.
Group Leads, please send Mary the following: 1) Number of people from each
theme group will be attending (so we can reserve seats for everyone)? 2) Speaker
names; 3) Send any comments and changes on the proposed agenda.
Our next call is this Wednesday, February 13, from 3:30 PM-4:30 PM. The callin number is 1-866-299-3188. Code: 703-308-2718.
Pollinator Summit Agenda
March 5, 2013
Potomac Yard South, 1st Floor Conference Center
(Draft 2/11/13)
Presenters in italics following topic.
9:00 9:30 AM
Introduction (30 min)
Purpose, tone and expectations of summit Steve Bradbury - 10 min
The Overall Value of Seed Treatments Ray Knake - 10 min
The Value of Seed Treatments to Growers - Jay Lynch from ISU - 10 min
9:30-11:00 AM
Dust Group (90 min)
9:30-10:00 AM Talc replacement Clive Halder/Bayer- 30 min
10:00 -10:20 AM Equipment manufacturing design changes- Nick
Tindall/American Equipment Manufacturers 20 min
(Break 10:20-10:30 AM)
10:30 11:00 AM Midwest Dust StudyLaurie Adams-Pollinator Partnership
????Ray Kendrick talk during this session.
11:00 AM - 1:30 PM
Seed Treatment Group (90 min)
11:00-11:15 AM Preparation of Seed for treatment Pioneer/ Monsanto-15 min
11:15-11:45 AM Formulation Technology Innovation and Improvements- Dr.
Palle Pedersen - Syngenta Seed Care Institute -30 min
11:45 12:00 PM Seed Applied Additives, Coatings, including new polymer
technologies Mike McFatrick, Becker-Underwood-15 min
(Lunch 12:00-1:00 PM)
1:00 1:30 PM Advances in technology - Seed Treatment application technology

commercial & downstream ie: Flow Meters, Seed Wheels, On-Demand, ISO
certified production facilities- Speaker not identified yet / Panel? -30 min.
1:30 4:00 PM
Communication/Education/BMPs Group(2 hours)
General Review of Best Management Practices / Stewardship tools: BMP's for

pesticide use at the agricultural site, and in the hive.
BMPs for agricultural pesticide application
Seed Treatment BMPs
Joint CLA/ASTA Seed Treatment Stewardship Guide document-Lisa Nichols
Bee Industry BMPs
BMPs around mitigation of bee exposure to pesticides in and outside of the hive-Jeff
Pettis
Ensure there is an emphasis on how the various tools are interconnected across
multiple audiences (ag industry, bee industry, growers, regulators, academics, etc.)
(2:30 2:45 PM Break)
Communication / Outreach / Education
Creating a sustainable communication network is critical; that crosses and connects
various industries, growers, beekeepers, seed treaters, regulators, and special interest
partners
Actionable items (i.e. education / outreach strategies; how to measure success
behavioral changes) with the BMP / educational tools that are currently, or soon to be,
available
Review of BMP website-pesticidestewardship.org and other similar resources
Wayne Buhler
4:00 -4:45 PM Wrap-Up
4:00 -4:15 PM Lessons learned, next steps, progress, future opportunity for
collaboration- Steve Bradbury 30 min.
4:15 4:45 PM Questions and Answers Panel? 30 min.
From:
To:
Subject:
Date:
Attachments:
Clock-Rust.Mary@epamail.epa.gov
clive.halder@bayer.com; tva@pollinator.org; warren.richardson@pioneer.com; joseph.wisk@basf.com;
richard aucoin@hc-sc.gc.ca; daniel.j.jenkins@monsanto.com; alavigne@amseed.org; wbuhler@ncsu.edu;
Kunickis, Sheryl; Epstein, David; Connie.Hart@hc-sc.gc.ca; lda@pollinator.org; janis.mcfarland@syngenta.com;
Mary.Mitchell@hc-sc.gc.ca; lnichols@amseed.org; jessica.christiansen@monsanto.com;
Green.Jamie@epamail.epa.gov; Svaty.Josh@epamail.epa.gov; Rossi.Lois@epamail.epa.gov;
Brady.Donald@epamail.epa.gov; Pease.Anita@epamail.epa.gov; Keigwin.Richard@epamail.epa.gov;
Moriarty.Thomas@epamail.epa.gov; Lantz.Tracy@epamail.epa.gov; Mcnally.Robert@epamail.epa.gov
Pollinator Summit: Notes from Call 1-18-13
First Meeting January 18, 2013 Pollinator Summit Steering Committee.docx
Hello,
Attached please find the notes from last week's first call with the Pollinator Summit steering committee.
As far as next steps, we agreed that each group would brainstorm to clarify and expand or edit the
sub-topics and sub-bullets under each theme area and be prepared to discuss these next Monday
when we have our next call, 12-1 PM, EDT. The call in number will be the same: 1-866-299-3188,
Code 703-305-0392.
If you have any questions, please let me know.
(See attached file: First Meeting January 18, 2013 Pollinator Summit Steering
Committee.docx)
Thanks!
Mary
Mary Clock-Rust
Phone: 703.308.2718
Pollinator Summit Steering Committee

Notes from First Meeting
January 18, 2013
Attendees: Steve Bradbury, Donald Brady, Lois Rossi, Anita Pease, Richard Keigwin, Tracy
Lantz, Thomas Moriarty, Robert McNally, Wayne Buhler, Clive Halder, Dan Jenkins, David
Epstein, Janis McFarland, Mary Mitchell, Warren Richardson, Laurie Adams, Joseph Wisk, Lisa
Nichols, Pat McCain, Jessica Christiansen, Mary Clock-Rust.
Steve Bradbury explained the concept of the summit. The summit is designed to be EPA
hosting/providing the forum to find efficiencies and partnerships among stakeholders that
have different perspectives, resources, and interests but that share common objective-to
protect pollinators; efforts that the broader public should know about.
Donald Brady said part of the idea for the summit is to highlight the tangible efforts being
made in these three areas of pollinator protection-Dust, Seed Treatment and BMPs. The
one-day meeting will be hosted by EPA and EPA will facilitate a discussion around the
current efforts and to focus on ongoing work. The summit will be a collaborative
opportunity to exchange ideas and have conversations around the work being done.
The summit will be:
A platform which EPA provides to facilitate discussion and information on current
activities by a diverse group of stakeholders to address overall pollinator health.
An opportunity for stakeholders to understand ongoing work and identify areas of
additional collaboration for current and future actions.
EPA will invite stakeholders to:
present summaries of the work they are doing and plan to do, in order to understand and
reduce potential exposure or risk from pesticide products, and
look for opportunities for collaboration to build long-term changes that are protective of
agriculture and honey bees.
There was some discussion and clarifying questions about the different theme areas, how
the day will go, and the proposed agenda. Thoughts shared included plenary session,
short presentations in each of the three areas, breakout sessions and then wrap up/next
steps.
Laurie Adams suggested each theme area identify three main points that they want to
convey and to structure succinct presentations around those.
Lois suggested grouping people around the three theme areas, identifying subtopics and
presenters. SC members volunteered for one of the three different theme areas that will
be the focus of the summit (dust, seed treatment, BMPs).
Warren Richardson asked that we use the remaining time to further explore each of the
theme areas.
The group identified the following subtopics and members:
Seed Treatment Group Subtopics:
Preparation of Seed for treatment
Coatings and formulations
Application processes following treatment
Members: Andrew Lavigne, Janis McFarland, Warren Richardson
Dust Group Subtopics:
Talc replacement
Equipment manufacturing design changes
Midwest study (NAPPC?) to investigate exposures during plantings
Members: Clive Halder, ??
BMPs Group Subtopics:
Intended Audience, Communication, availability of BMPs
BMPs related to work in pesticide application, for beekeeping and broader health of
bees
Education, other possible sub topics?
Members: Wayne Buhler, Dan Jenkins, Dave Epstein, Joe Wisk, Laurie Adams, Tom Van
Arsdall, Jessica Christiansen
Next Steps:
o Each subgroup should organize a call for brainstorming over the next week
(January 22-25) to clarify and expand or edit subtopics and sub-bullets under each
theme area. Email Mary with your thoughts and findings by Friday January 25.
o Our next conference call will be January 28, at 12 noon EDT. We will use the
same call-in number: 1-866-299-3188. Code: 703-305-0392.
From:
To:
Subject:
Date:
Epstein, David
Kunickis, Sheryl
Pollinator Issues
Monday, May 14, 2012 4:15:00 PM
Sheryl,
Not sure this is what you wanted. In attempting to put this issue on paper, I realized that
explanations are necessary for the uninitiated for it to make any sense, so there is more explanatory
discussion then originally intended.
As regards current pollinator issues, the current consensus of the scientific community is that
declines in domesticated, managed honey bee populations are resulting from a combination of
factors, including nutrition, pathogens/parasites, pesticides and biology/genetics/breeding, acting
individually and in combination with one another. The Federal Colony Collapse Disorder (CCD)
Steering Committee has recommended that the focus on CCD should include general honey bee
health, as CCD is accounting for a relatively small percentage of the overall national losses of
managed honey bee colonies.
There have been several peer-reviewed scientific papers published this year showing concerns with
the use of pesticides, and in particular, a class of insecticides referred to as neonicotinoids, and
honey bee health. These papers get reported in the media and draw high scrutiny to pesticide use as
a sole cause of declines in honey bee health and (CCD). The USEPA is informed in its risk assessment
of pesticides and resulting regulatory action regarding pollinator protection through a series of
workshops known as SETAC-Pellston (Society of Environmental Toxicology and Chemistry),
developed by a steering committee comprised of members from government, business, academic,
and nongovernmental organizations interested in advancing the science to understand the effect of
pesticides on non-target insects. To date, SETAC-Pellston has not recommended regulatory action
on pesticides for pollinator protection.
The USEPA Office of Pesticide Programs Pesticide Program Dialogue Committee (PPDC), formed a
Pollinator Protection Workgroup at its April 2011 meeting, consisting of four subgroups: labeling,
best management practices, communication/education/training, and enforcement. There have been
very deliberate discussions within each subgroup on actions that could be taken to further pollinator
protection while the science of pesticide effects on pollinators evolves. The following bulleted list
were recommendations from the labeling subgroup at the May 3-4 PPDC meeting:
Environmental Hazard Statements are not consistent and difficult to understand. Simplify
language (e.g. eliminate potentially toxic , highly toxic and replace with toxic)
Develop a labeling interpretation manual for clarity
Provide simple label statements on pesticides residual toxicity
Consider revisions to the Label Review Manual
Solicit input from state lead agencies (SLAs) before finalizing label revisions labels must be
enforceable
Various label issues overlap with BMPs, communication/education/training and enforcement

subgroups
In addition to the bullet points, above, the discussions within the labeling subgroup have included
the following:
Consideration risk-assessment based, crop specific labeling
- crops requiring commercially contracted pollination services (<1% all cropland)
- research/surveys into crop attractiveness to pollinators; crops with historical records of bee
kills
- crops valued for honey production
- determinate vs indeterminate blooming crops
- attractiveness of crops with extra-floral nectarines
- attractiveness and management of flowering weeds within farmlands
Systemic vs. non-systemic pesticides and residual activity
All above is simply to inform EPA, and no regulatory action has been proposed to date.
Regards,
David
Office: (202) 720-9877
Mobile:(b) (6)
From:
To:
Cc:
Subject:
Date:
Attachments:
Importance:
Serratosa, Jordi *
richardson.rochelle@epa.gov; Brady.Donald@epamail.epa.gov; RORTAIS Agnes; SZENTES Csaba; AUTERI
Domenica; Mary Mitchell; "Mary.Purcell@usda.gov"; connie.hart@hc-sc.gc.ca;
Steeger.Thomas@epamail.epa.gov; Richard Keigwin; Epstein, David; Hackett, Kevin; Pettis, Jeff; Stutsman,
Martin J; Liang, Charlotte; Oriani, Julia A; Friedlander, Lynn G; Smith, Emily (CVM-ONADE); RSchoen@nas.edu;
Kornele, Michelle; Obrien, Anna; Regmi, Prajwal; Volker, Brent; Schoen, Robin
MESNAOUI Mariama; LIEM Djien; DELUYKER Hubert; ROBINSON Tobin; Prater, Donald; Corrigan, Dara; Smith,
Merton; Zink, Donald; Scheid, Jon F; AZZALI Anna; Klurfeld, David; Oria, Maria; Burnsteel, Cindy
Pollinator
Wednesday, January 30, 2013 5:47:03 PM
Status of Pollinators in NAmerica.pdf
Horizontal mandate on bees signed.pdf
Mandate Colloquium signed.pdf
FINAL REPORT SEPTEMBER FIFRA SAP POLLINATOR MEETING PDF COPY.pdf
Outline for Report 2.doc
Agenda Pollinators Feb 7th .doc
High
On behalf of EFSA and EPA ,
Find enclosed the invitation and the agenda for the next cluster meeting on Pollinators scheduled for
the next Feb. 7th. Please inform me if there are changes in the attendants or the contents. Rochelle
Richardson will share the telephone number to connect with the teleconference and the pass code.
E mail missing : Marguerita Conti (Canada)
Looking forward to meet
Best , Jordi
Cluster meeting on Pollinators EPA/EFSA/PMRA

7 February 2013 (Thursday)
9.00-11.00 am ET Arlington VA/US-15.00-17.00 pm Parma IT
______________________________________________________________
Coordination of the telephone call and pass code to be sent later to all participants by
Rochelle Richardson richardson.rochelle@epa.gov Tel 703-308-6860
__________________________________________________________________________________
Attendants :
US EPA: Don Brady , Tom Steeger, Richard Keigwin

EFSA: Agns Rortais, Csaba Szentes , Domenica Auteri
Canada: PMRA Mary Mitchell, Connie Hart , Marguerita Conti
USDA/ARS: David Epstein, Kevin J. Hackett; Jeff Pettis, Mary Purcel
FDA//CFSAN : Marty Stutsman , Charlotte Liang;
FDA / CVM Julia Oriani , Lynn Friedlander , Emily Smith, Michelle Kornele.
Anna OBrien, Prajwal Regmi, Brent Volker.
NAS Robin Schoen (to be confirmed)
Welcome and introduction of the participants

1. 9.00 am To be confirmed: EPA Steve Bradbury (or Don Brady), EFSA Catherine GeslainLaneele (or Jordi), PH Canada Richard Aucoin (or Mary Mitchell) ) (5 )
2. 09.05 am . White paper SAP Pollinator meeting (final report) : EPA short presentation and
Exchange of views, (Implications for the Risk assessments in case of divergent opinions).
EPA/PMRA/: Tom Steeger will present this joint project /Connie Hart PMRA Rep
(20)
Status of Pollinators in North America

http://www.nap.edu/catalog/11761.html
Status of
Pollinators
in north
america
Committee on the Status of Pollinators in North America
Board on Life Sciences

Board on Agriculture and Natural Resources
Division on Earth and Life Studies
Copyright National Academy of Sciences. All rights reserved.

THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001

NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the
councils of the National Academy of Sciences, the National Academy of Engineering,
and the Institute of Medicine. The members of the committee responsible for the
report were chosen for their special competences and with regard for appropriate
balance.
This study was supported by the U.S. Department of Agriculture, Agricultural
Research Service (USDA-ARS) under Award No. 59-0790-3-201 and the U.S. Geological Survey (USGS) under Grant Agreement No. 03HQGR0131. The content of
this publication does not necessarily reflect the views or policies of the USDA-ARS
or USGS, nor does mention of trade names, commercial products or organizations
imply endorsement by the U.S. Government.
International Standard Book Number-13: 978-0-309-10289-6 (Book)
International Standard Book Number-10: 0-309-10289-8 (Book)
International Standard Book Number-13: 978-0-309-66381-6 (PDF)
International Standard Book Number-10: 0-309-66381-4 (PDF)
Library of Congress Control Number: 2006940682
Additional copies of this report are available from the National Academies Press, 500
Fifth Street, NW, Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202)
334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu.
Copyright 2007 by the National Academy of Sciences. All rights reserved.
Printed in the United States of America.
Cover: Design by Van Nguyen. Photo credits clockwise from top left: hummingbird
by W. May; sphinx moth by W. May; bat by Merlin D. Tuttle, Bat Conservation
International, reprinted with permission; bee by David Inouye, University of
Maryland, College Park.

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government, the public, and the scientific and engineering communities. The Council
is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph
J. Cicerone and Dr. Wm. Wulf are chair and vice chair, respectively, of the National
Research Council.
www.national-academies.org


COMMITTEE ON STATUS OF POLLINATORS

IN NORTH AMERICA
MAY BERENBAUM (Chair), University of Illinois, Urbana-Champaign
PETER BERNHARDT, St. Louis University, Missouri
STEPHEN BUCHMANN, University of Arizona, Tucson
NICHOLAS W. CALDERONE, Cornell University, Ithaca, New York
PAUL GOLDSTEIN, Florida Museum of Natural History, Gainesville
DAVID W. INOUYE, University of Maryland, College Park
PETER KEVAN, University of Guelph, Ontario, Canada
CLAIRE KREMEN, University of California, Berkeley
RODRIGO A. MEDELLN, Universidad Nacional Autonoma de Mexico,
Mexico City
TAYLOR RICKETTS, World Wildlife Fund, Washington, D.C.
GENE E. ROBINSON, University of Illinois, Urbana-Champaign
ALLISON A. SNOW, Ohio State University, Columbus
SCOTT M. SWINTON, Michigan State University, East Lansing
LEONARD B. THIEN, Tulane University, New Orleans, Louisiana
F. CHRISTIAN THOMPSON, Systematic Entomology Laboratory,
U.S.Department of Agriculture, Washington, D.C.
Staff
EVONNE P.Y. TANG, Study Director
FRANCES E. SHARPLES, Director, Board on Life Sciences
ROBIN A. SCHOEN, Director, Board on Agriculture and Natural
Resources
PEGGY TSAI, Associate Program Officer
KAREN IMHOF, Administrative Assistant
KATE KELLY, Editor
PAULA WHITACRE, Editor

BOARD ON LIFE SCIENCES

KEITH YAMAMOTO (Chair), University of California, San Francisco
ANN M. ARVIN, Stanford University School of Medicine, Stanford,
California
JEFFREY L. BENNETZEN, University of Georgia, Athens
RUTH BERKELMAN, Emory University, Atlanta, Georgia
DEBORAH BLUM, University of Wisconsin, Madison
R. ALTA CHARO, University of Wisconsin, Madison
JEFFREY L. DANGL, University of North Carolina, Chapel Hill
PAUL R. EHRLICH, Stanford University, Stanford, California
MARK D. FITZSIMMONS, John D. and Catherine T. MacArthur
Foundation, Chicago, Illinois
JO HANDELSMAN, University of Wisconsin, Madison
ED HARLOW, Harvard Medical School, Boston, Massachusetts
KENNETH H. KELLER, University of Minnesota, Minneapolis
RANDALL MURCH, Virginia Polytechnic Institute and State University,
Alexandria
GREGORY A. PETSKO, Brandeis University, Waltham, Massachusetts
MURIEL E. POSTON, Skidmore College, Saratoga Springs, New York
JAMES REICHMAN, University of California, Santa Barbara
MARC T. TESSIER-LAVIGNE, Genentech, Inc., South San Francisco,
California
JAMES TIEDJE, Michigan State University, East Lansing
TERRY L. YATES, University of New Mexico, Albuquerque
Staff
FRANCES E. SHARPLES, Director
KERRY A. BRENNER, Senior Program Officer
ANN H. REID, Senior Program Officer
MARILEE K. SHELTON-DAVENPORT, Senior Program Officer
EVONNE P.Y. TANG, Senior Program Officer
ROBERT T. YUAN, Senior Program Officer
ADAM P. FAGEN, Program Officer
ANNA FARRAR, Financial Associate
ANNE F. JURKOWSKI, Senior Program Assistant
TOVA G. JACOBOVITS, Senior Program Assistant
vi

BOARD ON AGRICULTURE AND NATURAL RESOURCES

W. REG GOMES (Chair), University of California, Oakland
SANDRA J. BARTHOLMEY, University of Illinois, Chicago
ROGER N. BEACHY, Donald Danforth Plant Science Center, St. Louis,
Missouri
H. H. CHENG, University of Minnesota, St. Paul
BRUCE L. GARDNER, University of Maryland, College Park
JEAN HALLORAN, Consumer Policy Institute/Consumers Union,
Yonkers, New York
HANS R. HERREN, Millennium Institute, Arlington, Virginia
KIRK C. KLASING, University of California, Davis
BRIAN W. MCBRIDE, University of Guelph, Ontario, Canada
TERRY L. MEDLEY, E. I. duPont de Nemours & Co., Wilmington,
Delaware
ROBERT PAARLBERG, Wellesley College, Watertown, Massachusetts
ALICE N. PELL, Cornell University, Ithaca, New York
BOBBY PHILLS, Florida A&M University, Tallahassee
SONYA B. SALAMON, University of Illinois, Urbana-Champaign
HAL SALWASSER, Oregon State University, Corvallis
PEDRO A. SANCHEZ, The Earth Institute at Columbia University,
Palisades, New York
B. L. TURNER, II, Clark University, Worcester, Massachusetts
LAURIAN UNNEVEHR, University of Illinois, Urbana-Champaign
JAW-KAI WANG, University of Hawaii, Honolulu
TILAHUN D. YILMA, University of California, Davis
Staff
ROBIN A. SCHOEN, Director
AUSTIN J. LEWIS, Program Officer
MICHAEL MA, Program Officer
PEGGY TSAI, Associate Program Officer
RUTH S. ARIETI, Senior Project Assistant
KAREN L. IMHOF, Administrative Assistant
vii


Preface
The magnitude and direction of all manner of anthropogenic global environmental change have lately come to dominate the national conversation:
at the movies, on the Internet, and in the press. Entering the term environmental crisis on Google generates close to 52 million hits, and the debate is
raging over the validity of various projections of consequences and diverse
proposals for remediation. Of the multitude of ways humans could be harming the planet, however, one that has largely been ignored is the pollinator
crisisthe perceived global decline in the number and viability of animal
species that facilitate reproduction of flowering plants, the overwhelming
majority of plants in terrestrial communities. In her hugely influential book
Silent Spring published more than 40 years ago, Rachel Carson recognized
the central role of pollinators. They are the proverbial birds and the bees,
along with many other insect species and even a handful of mammals, that
maintain human health and terrestrial biodiversity. Carson painted a bleak
picture of a world with fruitless falls. In the intervening decades, reports
have quietly accumulated from virtually every continent of shortages or
extinction of pollinators of various descriptions.
Ironically, despite its apparent lack of marquee appeal, pollinator decline is one form of global change that actually does have credible potential to alter the shape and structure of the terrestrial world. Over the past
decade, the public has begun to take notice and ask whether a pollinator
crisis is brewing and, if so, what can be done to avert it. The National Research Council, in keeping with its charter to provide independent, objective
analysis and advice on scientific matters of national importance, took on
this issue at the request of the U.S. Department of Agriculture and the U.S.
ix

PREFACE
Geological Survey and commissioned a study; overseeing the study process

were the Board on Agriculture and Natural Resources and the Board on
Life Sciences.
Because the efforts of pollination are so pervasive ecologically and
economically, the committee charged with assessing the status of pollinators required representation of a breadth of interests and abilities. The 15
members came from across the United States, Canada, and Mexico, and
their expertise encompasses ecology, population biology, ethology, genetics, evolutionary biology, botany, entomology, systematics, agricultural
economics, apiculture, and conservation biology (Appendix A). The committee devoted more than a year to examining literature, meeting with the
experts who are most familiar with the lives of pollinators, and meeting
with people whose livelihoods depend on pollinator activities. Evonne Tang,
Senior Program Officer for the Board of Life Sciences, labored brilliantly
and tirelessly to arrange meetings, secure information, make contacts, and
reconcile and edit numerous versions of the report. Fran Sharples, Director
of the Board on Life Sciences, was generous with administrative, scientific,
and moral support. From the Board on Agriculture and Natural Resources,
Robin Schoen, director; Karen Imhof, administrative assistant; and Peggy
Tsai, research associate, provided invaluable guidance, organizational effort,
and logistical assistance in support of the project
It seems particularly appropriate that a study examining the health and
well-being of the premier ecological mutualism on the planet should result
from mutual respect and cooperation among a group of dedicated scholars.
That the conclusions reached by the committee and presented in this report
will inspire a rash of Hollywood disaster films is extremely unlikelytidal
waves, floods, fires, and explosions still remain inherently more cinematic
than just about anything involving flowers, birds, bees, and butterfliesbut
it is to be hoped that the recommendations will inspire discussion and action nonetheless.
May Berenbaum
Chair, Committee on the Status of
Pollinators in North America

Acknowledgments
This report is a product of the cooperation and contributions of many

people. The members of the committee thank all of the speakers who attended its first committee meeting on July 6, 2005, the workshop on October 1819, 2005, and the third committee meeting on January 14, 2006 and
others who provided information and input. (Appendix B presents a list of
presentations to the committee.)
This report has been reviewed in draft form by persons chosen for their
diverse perspectives and technical expertise in accordance with procedures
approved by the National Research Councils Report Review Committee.
The purpose of this independent review is to provide candid and critical
comments that will assist the institution in making its published report as
sound as possible and to ensure that the report meets institutional standards
of objectivity, evidence, and responsiveness to the study charge. The review
comments and draft manuscript remain confidential to protect the integrity
of the deliberative process. We wish to thank the following for their review
of this report:

Deane Bowers, University of Colorado, Boulder

Susan Mazer, University of California, Santa Barbara
Robert Page, Arizona State University
Peter Raven, Missouri Botanical Garden
Malcolm Sanford (retired), University of Florida
Marla Spivak, University of Minnesota
James Thomson, University of Toronto
Nickolas Waser, University of California, Riverside
xi

xii

ACKNOWLEDGMENTS
Don Wilson, U.S. Fish and Wildlife Service

Ada Wossink, North Carolina State University
Although the reviewers listed above provided constructive comments

and suggestions, they were not asked to endorse the conclusions or recommendations, nor did they see the final draft of the report before its release.
The review of this report was overseen by Drs. Frederic L. Gould and Mary
Jane Osborn. Appointed by the National Research Council, Drs. Gould
and Osborn were responsible for making certain that an independent examination of this report was carried out in accordance with institutional
procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the author
committee and the institution.

Contents
SUMMARY
ROLE AND IMPORTANCE OF POLLINATORS

Pollinators in Natural and Agricultural Ecosystems, 16
Population Management, 18
Value of Pollination, 22
State of Knowledge, 25
History of Concern, 26
Charge to the Committee, 33
13
STATUS OF POLLINATORS
Pollinators and the Concept of Decline, 34
Population Trends, 35
Conclusions, 73
34
3 C
AUSES OF POLLINATOR DECLINES AND
POTENTIAL THREATS

Decline in Actively Managed Pollinators, 75

Decline in Natural or Wild Pollinators, 87

Conclusions, 103
4 E
FFECTS OF VARIATIONS IN POLLINATOR
POPULATIONS ON POLLINATION SERVICES

Pollinators in Agriculture, 104
xiii
75
104

xiv

CONTENTS
Pollinators in Natural Areas, 119

Conclusions, 129
5 MONITORING POLLINATOR POPULATIONS

AND SERVICES

Review and Assessment of Current Monitoring Programs, 131

Requirements for Adequate Monitoring of Pollinators and
Pollination Function, 140

Conclusions, 153
6 STRATEGIES FOR MAINTAINING POLLINATORS
AND POLLINATION SERVICES

Maintaining Commercial Pollinators, 156

Maintaining Wild Pollinators, 171

Maintaining Pollination Services, 185

Public Policy and Pollinator Populations, 190

Adaptive Management and Pollinator Monitoring, 194

Conclusions, 194
131
155
7 FINDINGS AND RECOMMENDATIONS

Managed Pollinators, 197

Wild Pollinators, 201
196
GLOSSARY
208
REFERENCES
215
APPENDIXES
A
B
C
D
E
F
G
H
I
Committee Biographies
Presentations to the Committee
Recently Extinct Insects from Around the World
Endangered Insects in the Continental United States
Bee Species in Decline in North America
Meetings and Conferences on Pollinator Issues 19792006
Methods for Analyzing Status of Pollinators
Xerces Society Red List of Pollinating Insects of North America
Annual Bee Variability of Bee Abundances
275
282
285
287
289
290
293
298
307

Summary
This report of the National Research Councils Committee on the Status

of Pollinators in North America is an assessment of pollinating animals in
the United States, Canada, and Mexico. To prepare this report, the committee compiled and analyzed the published literature; consulted numerous
experts from academia, industry, and nongovernmental organizations;
and drew from its members extensive expertise. The extent to which the
committee could discuss different pollinator species in different regions
depended largely on the availability of data, as the amount and quality of
evidence vary widely for different animal groups. For most North American
pollinator species, long-term population data are lacking and knowledge
of their basic ecology is incomplete. These information deficiencies make
definitive assessments of North American pollinator status exceedingly
difficult. This lack stands in contrast to the study of pollinators in Europe,
where status has been the subject of systematic investigation for some time,
and where declines and extinctions have been definitively documented.
Notwithstanding these gaps, the committee found sufficient evidence to
determine the status of a range of both managed and unmanaged pollinators in North America.
IMPORTANCE OF POLLINATORS
About three-quarters of the more than 240,000 species of the worlds
flowering plants rely on pollinatorsinsects, birds, bats, and other animalsto various degrees to carry pollen from the male to the female parts
of flowers for reproduction. Pollinators are vital to agriculture because most


STATUS OF POLLINATORS IN NORTH AMERICA
fruit, vegetable, seed crops and other crops that provide fiber, drugs, and
fuel are pollinated by animals. Bee-pollinated forage and hay crops, such
as alfalfa and clover, also are used to feed the animals that supply meat and
dairy products. Animal-pollinated crops generally provide relatively higher
income to growers than do crops pollinated in other ways.
Over and above its direct economic value to humans, pollination by
animals provides essential maintenance of the structure and function of
a wide range of natural communities in North America, and it enhances
aesthetic, recreational, and cultural aspects of human activity. In view of
that economic and ecological importance, this report assesses the status of
pollinators in North America, identifies species for which there is evidence
of decline, analyzes the putative causes of those declines, and discusses their
potential consequences. The committees statement of task is provided in
Box S-1.
The first section of this summary addresses the status, causes of decline, consequences of decline, monitoring needs of managed pollinators,
potential steps for managed pollinators conservation and restoration, and
the committees recommendations (some in abbreviated form). The second
section covers the same topics for wild pollinators. Detailed recommendations are provided in Chapter 7.
BOX S-1
Statement of Task:
Committee on the Status of Pollinators in North America
The National Research Councils Committee on the Status of Pollinators
in North America was charged to address the following questions:
To what degree, if any, are pollinators experiencing serious
decline?
Where decline can be established by available data, what are its
causes?
What are the potential consequences of decline in agricultural and
natural ecosystems?
What research and monitoring are needed to improve
information?
What conservation or restoration steps can be taken to prevent,
slow, or reverse decline?

SUMMARY
MANAGED POLLINATORS
Status
Findings: Long-term population trends for the honey bee, the most important managed pollinator, are demonstrably downward. Similar data are not
available for other managed pollinators, such as alfalfa leafcutting bees and
bumble bees.
Among the various pollinator groups, evidence for decline in North
America is most compelling for the honey bee, Apis mellifera. Honey bees
enable the production of no fewer than 90 commercially grown crops, and
beekeeping is a large commercial industry that leases honey bee colonies for
pollination services across the continent.
Since 1947, the U.S. Department of Agricultures (USDAs) National
Agricultural Statistics Service (NASS) has tracked honey bee colonies managed by beekeepers in the United States. Statistics demonstrate declines
in 19471972 and 19891996, and a recent drop in 2005. Reports from
industry journals suggest higher rates of winter kill in honey bee colonies
since the advent of the parasitic mite Varroa destructor in the 1980s, causing
temporary shortages of healthy honey bee colonies (for early season almond
pollination) that are not captured by the NASS data. However, putting those
declines into context is complicated by the peculiarities of NASS data collection. Because its annual survey focuses on honey production and pollinating
colonies are not monitored unless they also produce honey, there are limits
on the extent to which those data can be extrapolated to inform population
estimates. NASS methods result in undercounting because the annual survey
group consists of beekeepers with five or more hives; there is no mechanism
to count hobbyist beekeepers who might nevertheless contribute to the supply of honey-producing or pollinating colonies. Moreover, because surveys
do not consider that some honey-producing colonies travelthey are leased
in different regions of the country for different seasonsthese colonies can
be counted more than once.
NASS also conducts a 5-year census of agriculture survey that counts
all honey bee colonies just once, but definitional differences make the data
incompatible with data from the annual honey survey. Yet another complicating factor is that no surveys account for colony health or for intrayear
volatility in colony numbers. (Colonies that die early in the year, when they
are critically needed for pollination, can be replaced by purchasing packages
of bees or splitting surviving colonies later in the year.) Finally, there is an
additional complication for assessing the supply of honey bee pollinators in
North America. U.S. data collection does not match what is done in Canada
or Mexico. Canadian data are collected on all honey bee colonies, whether
they are kept for pollination, for honey production, or both. Mexico has

only recently begun a survey programdata collection began in 1990and

its collection methods were not available to the committee.
Recommendation: Improved information gathering for the beekeeping
industry is critical, and the NASS should modify its data collection methodologies. The committee specifically recommends that NASS:
Refine its assessment of honey bee abundance, specifically by collecting data annually, eliminating double-counting, recording pollination
services, and monitoring winter losses.
Collect commercial honey bee pollination data, including crops pollinated and leasing fees, from beekeepers and from crop growers.
Coordinate and reconcile data collection on honey bee colonies
throughout North America. NASS should make its annual survey definitions
compatible with its 5-year census of agriculture. The United States should
work with Canada and Mexico through the North American Free Trade
Agreements Commission for Environmental Cooperation and the Trilateral
Committee for Wildlife and Ecosystem Conservation and Management to
adopt common methodologies.
Causes of Decline
Findings: Introduced parasites and pathogens clearly have harmed some
managed pollinators, most notably honey bees.
Introduced parasites, particularly Varroa destructor, the varroa mite,
clearly have contributed to reductions in managed and unmanaged honey
bees. In early 2005, for the first time since 1922, pollinating honey bees were
imported from outside North America, a change made possible by a regulatory alteration to the terms of the Honeybee Act of 1922. The imports were
permitted in part because of a shortage of honey bee colonies for almond
pollination in California. Bee importation, however, can carry the risk of
pest and parasite introduction. There is evidence that other factors also
contribute to current and potential future declines, among them antibioticresistant pathogens (American foulbrood); pesticide-resistant mites; and the
encroachment of Africanized honey bees, particularly in the southeastern
United States, a major regional source of honey bees sold or leased in the
rest of the country.
Recommendation: The Animal and Plant Health Inspection Service (APHIS)
should ensure that its regulations prohibit introduction of new pests and
parasites along with imported bees, and Congress should extend the Honey
bee Act of 1922 in principle to other managed pollinator species.

SUMMARY
Recommendation: Through research at the Agricultural Research Service

(ARS) and competitive grant programs, USDA should not only continue but
also expand its efforts to:
Encourage innovative approaches to protecting honey bee health
by
developing sustainable pest and resistance management programs for varroa mites, including identifying additional leasttoxic alternative pesticides and nonchemical cultural bee
management practices.
Improve genetic stocks of honey bees by
refining methods for breeding, selecting, maintaining, and
improving stocks with disease and pest resistance, moderated
temperament, and improved honey production;
refining methods for producing high-quality queen production
from selected stocks including controlling mating to ensure
expression of desired traits in colonies;
expanding current efforts in germplasm preservation, including cryopreservation;
developing methods for the maintenance of European stocks
in areas of Africanization;
developing a third-party certification program to ensure the
quality and effectiveness of commercial queens; and
identifying genetic and genomic markers as a support to
breeding programs (Chapter 6).
Although honey bees are the most important managed pollinators,
other managed non-Apis species also require attention. The development of
management protocols for wild species and the management of agricultural
landscapes to sustain wild pollinator populations can create alternatives to
honey bees as pollinator demands rise and shortages become likely.
Recommendation: The USDA-ARS should:
Create research entomology positions in its fruit and vegetable laboratories in geographically diverse regions of the United States to develop
new non-Apis pollinators and establish protocols for management. These
activities should augment work in the Bee Biology and Systematics Laboratory in Logan, Utah, which currently serves as a focal point for non-Apis
research.

Develop and implement bombiculture disease management programs to prevent pathogen spillover to wild populations.
Address pathogen problems in culturing alfalfa leafcutter bees
(megachileculture) to improve pollinator efficacy and sustainability.
Conduct research on landscape and farm management as related
to pollinators, and provide guidance on pollinator-friendly management
practices.
Recommendation: Private-sector funding mechanisms for honey bee health
and technology transfer from government research facilities should be created and enhanced to meet pollination needs. Industry checkoff programs,
for example, could add honey bee pollination services to the existing crop
commodity and honey programs. This private-sector effort could complement federally funded basic research efforts and promote translational
research.
Consequences of Decline
Findings: Managed pollinator decline and rising cost of pest control could
increase pollinator rental fees.
Among the most conspicuous, demonstrable consequences of changing pollinator status is the rising cost of pest control in bee husbandry that
has attended mite infestations of managed populations. Honey bee rental
fees rise because of increasing demand attributable to growth in almond
production and because of seasonal instability in honey bee populations.
Notwithstanding, alternative managed pollinator species are not being
widely utilized. And despite evidence of their efficacy as crop pollinators,
wild species are not being effectively utilized.
Monitoring
Findings: As noted, improved information gathering for the beekeeping
industry is critical, and the NASS should modify its data collection methodologies. In addition, the potential for the development of new management
protocols to increase the use of wild pollinator species for agriculture should
be explored to create alternatives to honey bees as commercial pollinator
demands rise and shortages become likely.
Domestication
of bumble bees for commercial propagation.

research is the process of applying ideas, insights, and discoveries generated
through basic scientific inquiry to industrial, agricultural, and medical uses.
Translational

SUMMARY
Recommendation: USDA should establish discovery surveys for crop pollinators throughout the range of crops in North America to identify the
contributions of wild species to agricultural pollination.
Conservation and Restoration
Findings: Research in genetics and genomics has facilitated the development
and maintenance of mite- and pathogen-resistant stocks of honey bees.
However, these technologies have not been widely adopted, and there is a
pressing need for translational research to synthesize commercially viable
practices from the results of basic research.
As noted, USDAs intramural research and competitive grant programs
should expand efforts to use state-of-the-art scientific knowledge to encourage innovative and commercially viable approaches to protecting honey bee
health.
WILD POLLINATORS
Status
Findings: There is evidence of decline in the abundance of some pollinators,
but the strength of this evidence varies among taxa. Long-term population
trends for several wild bee species (notably bumble bees) and some butterflies, bats, and hummingbirds are demonstrably downward. For most pollinator species, however, the paucity of long-term population data and the
incomplete knowledge of even basic taxonomy and ecology make definitive
assessment of status exceedingly difficult.
Most other insect pollinators in natural and agricultural systems are not
well characterized, taxonomically or ecologically, in part because of the lack
of monitoring programs and in part because of a shortage of taxonomists.
Overall, the paucity of long-term data prevents the documentation of population trends for almost all pollinator species. Although suggestive evidence
of decline, extirpation, or extinction exists for some species, documentation
of population changes is available for very few.
Notwithstanding the deficiencies in the data, there is clear evidence of
decline in the numbers of some vertebrate and invertebrate pollinators. In
parts of their ranges, the declines of several vertebrate pollinator species,
particularly bats, are evidenced by conservation program monitoring. Longterm studies by individual investigators and regional Heritage Programs also
provide evidence for declineslocal and globalamong wild bumble bee
species and in some butterflies. Some pollinator species have been added to
endangered species lists.

Recommendation: To address the taxonomic impediment to assessing pollinator status, USDA-ARS should expand basic research on the systematics
of pollinators and on the development of rapid identification tools.
Causes of Decline
Findings: The causes of decline among wild pollinators vary by species but
are generally difficult to assign definitively. Pathogens that have spilled over
from commercially produced bumble bees for greenhouse pollination appear
to have contributed to declines in some native bumble bees. Other factors
for which there is convincing evidence include habitat degradation and loss,
particularly for some bats, bees, and butterflies.
Definitive causes of decline or factors that contribute to decline in species with demonstrable changes in population status could be assigned in
only a few cases. A major cause of decline in native bumble bees appears
to be recently introduced nonnative protozoan parasites, including Nosema
bombi and Crithidia bombi, probably from commercial bumble bees imported from Europe for greenhouse pollination. The bees frequently harbor
pathogens and their escape from greenhouses can lead to infections in native
species. Disease, notably chalkbrood (caused by the fungal pathogen Ascosphaera aggregata), also has harmed populations of Megachile rotundata,
the alfalfa leafcutter bee, in the United States. In some species, competition
with exotic pollinators (including Apis mellifera) has led to population
declines.
Declines in many pollinator groups are associated with habitat loss,
fragmentation, and deterioration, although in the United States data are,
in most cases, inadequate to demonstrate causation unambiguously. One
exception is the decline in bat populations that is attributed to the destruction of cave roosts.
There is evidence that other factors contribute to the documented declines among other pollinators. Changes in phenological synchrony and in
distributions of pollinators and plants resulting from global climate change
could lead to a decline in interactions between flowers and pollinators.
Disruption of migratory routes is evident in hummingbirds, nectar-feeding
bats, and some butterflies.
Recommendation: To prevent pathogen spillover to wild populations,
APHIS should require that any commercially produced bumble bee colony
shipped within the United States be certified as disease-free.

SUMMARY
Findings: The consequences of pollinator decline in nonagricultural systems
are more difficult to define, but one important result could be an increased
vulnerability of some plant species to extinction.
Few plant species rely on a single pollinator. Pollen limitation of seed set
is common in wild plants, but its population consequences are not clear. In
the event of declining pollinator populations, some plant populations that
are dependent on affected pollinators for reproduction could become more
vulnerable to an extinction vortexthe interacting demographic and genetic
factors that progressively reduce small populations. Therefore, the effects of
pollinator decline on rare plant species or on those with small populations
also should be given special attention.
Recommendation: The U.S. Geological Survey, the Fish and Wildlife Service,
and other agencies responsible for natural resource protection should establish discovery surveys for pollinators of rare, threatened, and endangered
plant species.
Monitoring
Findings: Long-term, systematic monitoring is necessary for unambiguous
documentation of trends in species abundance and richness. Such monitoring allows detection of relationships between changes in pollinator communities and the putative causes of change. Those relationships must be
understood to assist in developing plans to mitigate harm or to manage
species sustainably.
Pollinator-monitoring programs in Europe (for example, the Survey of
Wild Bees in Belgium and France and the European Unions Assessing LargeScale Risks for Biodiversity with Tested Methods project) have effectively
documented declines in pollinator abundance, but there is no comparable
U.S. program. The lack of historical baselines to compare with contemporary survey data makes it difficult to assess pollinator status or to determine
the causes of documented declines.
Recommendation: The federal government should establish a network of
long-term pollinator-monitoring projects that use standardized protocols
and joint data-gathering interpretation in collaboration with Canada and
Mexico. A rapid, one-time assessment of the current status of wild pollinators in North America to establish a baseline for long-term monitoring is a
laudable initial goal.

10
Components of this two-part assessment and monitoring program should

include re-surveys of areas well sampled in the past and mining of museum
collections and the literature for historical data that correspond to areas of
continuous, high-intensity sampling. The assessment should also include
monitoring of pollinator status and function that integrates the work of
professional scientists and citizen-scientists to maximize the depth and
breadth of effort.
The selection of study species should correspond to the strength of
evidence for decline. In view of collective evidence of population declines
and possible extinctions, bees provide a logical initial focus. Lepidoptera
constitute another group for which a compelling need for monitoring exists,
given recent extinctions and the classifications of some species as endangered
or threatened.
Findings: Effective conservation or restoration of pollinator populations
requires comprehensive knowledge of their biology, which is currently
insufficient to inform the design of sustainable management and maintenance programs. However, many simple and relatively inexpensive practices
for pollinator conservation are available. Land managers and landowners, including farmers and homeowners, should be encouraged to adopt
pollinator-friendly practices, many of which incur little expense. However, widespread adoption of these practices is unlikely unless there is a
general appreciation of the ecological and economic benefits of pollinators.
Hence, public outreach is key to pollinator protection, conservation, and
restoration.
Recommendation: Because of the importance of pollination as an ecosystem
service in both agricultural and natural ecosystems, the National Science
Foundation and USDA should recognize pollination as a cross-cutting theme
in their competitive grant programs. Representative areas where research
is needed include identification of causes and consequences of pollinator
decline, ecology, restoration, conservation, and management of pollinators
and pollination services, and establishment of Small Business Innovation
Research programs to promote technology transfer to address the health
and sustainability of commercially managed pollinators.
Notwithstanding deficiencies in understanding of wild-pollinator biology, viable, pollinator-friendly land management practices (such as planting native plants to enhance pollinator habitat) are known and available,
although not yet widely adopted. Farmers and ranchers can be offered
economic incentives to adopt such practices.

11
SUMMARY
Recommendation: Economic incentives should be expanded for pollinator

conservation.
State-level Natural Resources Conservation Service (NRCS) offices
should provide lists of scientifically tested and approved pollinator-friendly
practices to farmers participating in USDA cost share programs (the Wildlife Habitat Incentives Program and the Environmental Quality Incentives
Program), land retirement programs (the Conservation Reserve Program
[CRP] and the Conservation Reserve Enhancement Program), and production stewardship programs (the Conservation Security Program).
CRP should explicitly incorporate pollinator habitat in the
environmental-benefits index used to evaluate land parcel proposals and
incorporate the value of pollinator habitat development into its determination of the stewardship tiers for federal payments.
USDA cost-sharing, land retirement, and production stewardship
programs should be available to producers of all commoditiesfruits, nuts,
and vegetablesthat depend on pollinators.
The NRCS should target new hiring of personnel whose expertise is
in biological sciences, especially ecology and natural-area management.
Landowners other than farmers and rancherssuch as homeowners
and businessesalso could contribute to the conservation of pollinators by planting wildflowers to provide floral resources for resident and
migratory adult pollinators and by providing nesting sites for females.
People who do not own or manage land also can help by participating in
monitoring programs. Critical to the success of citizen-scientist programs,
however, is effective public outreach to raise awareness of pollinators ecological and economic contributions and to encourage public participation
in conservation.
Recommendation: As part of their outreach, federal granting agencies
should make an effort to enhance pollinator awareness in the broader community through citizen-scientist monitoring programs, teacher education,
and K12 and general public education efforts that center on pollination.
Recommendation: Professional societies (Ecological Society of America,
Entomological Society of America, American Association of Professional
Apiculturists, Botanical Society of America) and nongovernmental organizations (North American Pollinator Protection Campaign, Xerces Society
for Invertebrate Conservation) should collaborate with landowners and the
public to increase awareness of the importance of pollinators and to publicize simple activities the public can do to promote and sustain pollinator
abundance and diversity.

12
Although the object of the Endangered Species Act of 1973 (ESA) is to

protect endangered species and their habitats, many endangered pollinators
are not recognized as candidate species for two reasons. First, Congress
directed that listing of species requires a scientific determination of a species continued existence as threatened or endangered, but data on many
pollinators are sketchy. Second, a 1981 congressional revision of the ESA
specifically exempted any species of the Class Insecta determined by the
Secretary to constitute a pest whose protection under the provisions of this
Act would present an overwhelming and overriding risk to man. Some
caterpillars and carpenter bees, for example, can cause economic damage.
Thus, it might be difficult to present sufficient evidence to list them.
Recommendation: Congress should not consider any ESA amendment that
would create additional barriers to listing pollinator species as endangered.

1
Role and Importance of Pollinators
The angiospermsflowering plants that produce seeds often enclosed

within an edible fruitare among the planets most successful life forms.
More than 250,000 species of flowering plants have been described, and
an equivalent number could await discovery (Davies et al., 2004). At the
base of most terrestrial and many aquatic food webs, the angiosperms are
the principal providers of nutrients and resources to most other organisms,
and they provide multidimensional structure for the majority of terrestrial
and freshwater ecosystems. Humans derive food, fiber, drugs, and fuel,
either directly or indirectly from angiosperms. Moreover, angiosperms have
enhanced aesthetic, recreational, and cultural pursuits since before recorded
history.
Reproductive systems of angiosperms vary greatly among species
(Box 1-1), but two processes are necessary for sexual reproduction in all angiosperms: pollinationthe transfer of pollen from the anthers of a stamen
to the stigma of a pistiland fertilizationthe fusion of the sperm nuclei
from pollen with the egg nucleus in the ovary to produce an embryo. Some
plants self-pollinate, that is, pollen transfer occurs within the same flower
or among the flowers on a single plant, usually because the anthers touch
the adjacent stigma. The majority of flowering plants, however, depend on
the transfer of pollen from other individuals (cross-pollination).
Although some species rely on abiotic forces, including wind and water,
for pollen transfer, more than three-fourths of the planets angiosperms rely
on over 200,000 species of animal pollinators to various extents to meet
their reproductive needs. Fossil records show that angiosperms underwent
a remarkable diversification between 130 million and 90 million years ago
13

14
BOX 1-1
Barriers to Self-Fertilization

Flowers can be staminate (bearing only male reproductive organs), pistillate (bearing only female reproductive organs), or perfect (bearing male and
female reproductive organs). Individual plants can be monoecious (bearing
staminate and pistillate flowers), dioecious (staminate and pistillate flowers
borne on separate plants), or even trioecious (staminate, pistillate, and perfect flowers borne on separate plants). Within dioecy, various conditions can
be found in different species; gynodioecy, for example, is the term applied
to the breeding system of species in which individuals bear either female or
hermaphrodite flowers (Richards, 1997). Almost three-quarters of all plant
species produce perfect flowers. Approximately 5 percent are dioecious, and
slightly more than 5 percent are monoecious (Molnar, 2004).

Pollination can occur within the flowers of a single plant, among different
flowers of a single plant, and among flowers of different plants. A plant that is
self-fertile and self-pollinating is called autogamous if pollination and fertilization take place within the same flower. A plant is geitonogamous if pollination
and fertilization take place between flowers of the same plant, whereas a plant
that is cross-pollinated and cross-fertilized is xenogamous. It is common for
plants to receive mixtures of self and outcross (nonself) pollen grains, especially if the male and female parts are in the same flower (Plate 1a perfect
or hermaphrodite flower).

Perpetual self-fertilization could be problematic for plants because of the
many potential genetic complications associated with inbreeding (Charlesworth and Charlesworth, 1987). Accordingly, adaptations that reduce the likelihood of selfing exist in many taxa. Dioecy and monoecy promote outcrossing,
and that they achieved ecological dominance 100 million to 70 million years
ago (Davies et al., 2004). Chief among the many explanations offered for
their spectacular ascendancy is the development of mutualistic associations
with animals for the dispersal of pollen (Baker and Hurd, 1968; Faegri and
van der Pijl, 1979; Labandeira et al., 1994; Stebbins, 1950, 1974) and seeds
(Herrera, 1989; Kevan, 1984; van der Pijl, 1982). Mutualistic associations
with animals provide mobility of gametes to otherwise predominantly sessile
terrestrial plants, which allows for greater genetic variation in plants as well
as access to a wider range of ecological opportunities through seed dispersal.
For flowering plants, use of an animal partner to transport pollen increases
the area in which potential mates can be found and promotes outcrossing,
the merger of gametes from genetically distinct individuals. Increasing genetic variability through recombination associated with outcrossing is key

role and importance of pollinators
15
although monoecious plants can receive self-pollen from male flowers on the
same plant. Many monoecious species produce male and female flowers at
different times, and the probability of selfing is reduced. Similarly, in plants
with hermaphrodite flowers, self-pollination within flowers is avoided when the
male and female floral parts mature at different times. In some species, the
chance of self-pollination is reduced because the male and female parts of
the same flowers are separated. In a subset of those species, the male and
female parts of the flower move closer together as the flower ages, allowing
self-pollination as a last resort before the flower is too old to set fruit.

As a further deterrent to selfing, many flowering plant species are selfincompatiblethat is, pollen that is deposited on a stigma within the same
flower (or another flower on the same plant) is unable to achieve fertilization.
Self-incompatibility is controlled in complex and variable ways, and it involves
the interplay of incompatibility alleles (of which there may be many) and
their effects in the two parent plants (Matton et al., 1994). The effectiveness
of self-incompatibility mechanisms ranges from absolute to weak, and the
mechanisms for blocking self-fertilization can break down as a result of aging
or external factors, especially heat.

Breaking those barriers down ensures sexual reproduction (seed set and
fruit set) even when cross-pollination is not possible. It is important to note,
however, that despite the ubiquity of outbreeding, many species persist exclusively and successfully with self-pollinating and self-fertile flowers. Moreover,
some self-fertile plants that can self-pollinate (including some legumes) are
of agricultural importance. They can establish themselves in nonindigenous
areas where their natural pollinators are absent. The nature and evolutionary biology of plant-breeding systems are presented in detail by Richards
(1997).
to allowing organisms to adapt to spatially and temporally variable environments (Box 1-1). Genetic variability in plant populations could help to
facilitate the evolution of resistance to pathogens and herbivores.
After fertilization is complete, the production of fruit ensues. A flowers
ovary may contain a single ovule and produce a fruit that bears only a single
seed (as in the almond, avocado, coconut, plum, or cherry), or it may contain hundreds of ovules and produce a fruit bearing hundreds of seeds (as
in the tomato, kiwi fruit, cucumber, watermelon, or squash). Because each
seed results from the union of a sperm cell from a pollen grain and an egg
cell, some plants require many hundreds of pollen grains to fertilize all of
the available egg cells. If a flower receives an inadequate number of pollen
grains, some of the egg cells will not be fertilized and accordingly seeds will
not develop. Economic consequences of such incomplete fertilization include

16
production of undersized or misshapen fruit that, for a market crop, has less
value. Adequate pollination often requires that individual flowers be visited
by many pollinators or that one to several pollinators make multiple trips
to the same flower.
Some fruits of economic importance are seedless by design. They are
generally the product of selective breeding or genetic manipulation that
would not be sustainable in nature (Schery, 1972). Seedless bananas, for
example, are the products of sterile triploid plants arising either spontaneously or as a result of hybridization of diploid and tetraploid individuals
and are propagated vegetatively. Parthenocarpic fruits, such as clementines
(seedless tangerines), are those in which fruits develop in the absence of successful fertilization; fertilization could fail because these self-incompatible
cultivars are grown in monoculture orchards. Seedless grapes, in contrast,
are stenospermocarpic; fertilization takes place, but the resulting fruit is
seedless because the immature embryo fails to develop (Schery, 1972).
POLLINATORS IN NATURAL
AND AGRICULTURAL ECOSYSTEMS
In view of the fact that pollinator-plant interactions encompass almost
400,000 species, the precise nature of the relationship between plant and
pollinator varies enormously. Although some animals visit flowers for nectar
or pollen, not all flower visitors bring about pollination. Effective pollinators often have behavioral and anatomical traits that greatly increase the
efficiency and accuracy of pollen delivery (Barth, 1991; Faegri and van
der Pijl, 1979; Proctor et al., 1996). In general, pollination is a mutually
beneficial interaction; pollinating animals receive some form of nutritional
reward for visitation and pollen delivery. Pollen itself can be a reward,
serving as the primary food resource for most larval bees and as an important source of protein for some flies, butterflies, birds, and bats (Roulston
and Cane, 2000). Other plants provide nectar, oils, resins, fragrances,
pheromone precursors, and other resources to induce visitation and pollen
delivery (Barth, 1991; Buchmann, 1987; Dafni et al., 2005; Roulston and
Cane, 2000; Roulston et al., 2000).
Plants and pollinators vary in their degree of interdependence. Some
plant species depend primarily on a single species or genus of pollinator,
which in turn has restricted sources of pollen or nectar. An example of a
closely dependent association is the relationship between plants in the genus
Yucca (Agavaceae) and their pollinators, the aptly named yucca moths of the
genus Tegeticula (reviewed in Pellmyr, 2003). In this mutualism, estimated
to be more than 40 million years old, the adult yucca moth is the primary
pollinator of yucca and the developing yucca seeds the main nutritive source
for the caterpillar. The female moths have unique structures, called tentacles,

17
which are used to collect and compact comparatively large quantities of

pollen (up to 10 percent of the moths weight) from yucca flowers. After
gathering a pollen mass, the moth flies off and visits another flower, in
which she lays eggs. Then, in a distinctive series of stereotyped behaviors,
she places part of the pollen load directly on the stigma surface to achieve
pollination and subsequent fertilization, thereby guaranteeing a food source
for her offspring.
Such specialized relationships, however, are the exception in plantpollinator interactions. In many cases, if not most, associations are highly
opportunistic. Over a 2-year period, for example, at least 45 species of
insects in 5 orders were observed to visit Geranium thunbergii flowers in
a natural population; of these, 11 species in 3 orders served as principal
pollinators (Kandori, 2002). Principal pollinators of a particular species
can vary spatially as well as temporally; the alpine sky pilot, Polemonium
viscosum, is pollinated primarily by bumble bees at high elevations and by
flies at low elevations in its native Rocky Mountain range (Galen et al.,
1987). Humans have understood the agricultural importance of pollinationthat plants require pollen transfer to produce fruits and set seedfor
at least 3,500 years. However, the idea that seeds result ultimately from the
deposition of pollen grains on stigmatic surfaces was not clearly articulated
until the 17th century (Camerarius, 1694) and even then was slow to gain
acceptance. The systematist Carolus Linnaeus, for example, identified the
sexual organs of plants as important components of his classification system,
to the disapprobation of the 18th centurys religious establishment.
The idea that animals play a role in cross-pollination, the transfer of
pollen from one individual to another, was not clearly articulated until
close to a century later (Klreuter, 1761; Sprengel, 1793). Joseph Gottlieb
Klreuter, a professor of natural history at the University of Karlsruhe,
Germany, demonstrated that insect visitation was a prerequisite for seed
production in several economically important fruits, vegetables, and ornamental flowers and put his knowledge to practical use by developing technique for artificial fertilization and conducting the first cross-hybridization
of two plant species (Mayr, 1986; Sinnott, 1946).
The great insights and practical achievements of Klreuter and Sprengel
failed for the most part to inspire their contemporaries, but a half-century
later their work had a profound influence on the thinking of another biologistCharles Darwin. The publication of The Origin of Species by Means
of Natural Selection or The Preservation of Favoured Races in the Struggle
for Life (The Origin of Species, in short) in 1859 ushered in a new era of experimental pollination biology. In his preface, Darwin described the process
of coadaptation, which is what allows living organisms to serve as selective
agents in the same manner as abiotic forces and specifically mentioned pollination as an example.

18
Darwins extensive writings on plant-pollinator relationships, not only

in The Origin of Species but also in The Various Contrivances by which
British and Foreign Orchids are Fertilised by Insects and the Good Effects
of Intercrossing in 1862 and other subsequent publications, summarized an
extensive literature and described his own meticulous experiments, thereby
providing compelling evidence of the significance of pollination in the lives
of plants. Demonstration of the evolutionary mechanism to account for
the reciprocally adaptive relationship between plants and their pollinators
provided the impetus for an explosion of interest in pollination biology
(Delpino, 18681875; Knuth, 1906, 1908, 1912; Mller, 1869; Mller and
Delpino, 1869) that laid the foundation for agricultural applications and
for contemporary experimental studies.
POPULATION MANAGEMENT
Active Management
Recognition of the mechanisms of biotic pollination led to important
agricultural innovation, with extensive economic consequences (Box 1-2);
management of pollinator species allowed for enhanced crop productivity
and for commercialization (and export) of numerous crop plants. In North
America, only a handful of pollinator species are actively managedthat
is, they are semidomesticated, produced in large quantities, and bought
and sold commercially. Of these, Apis mellifera L., the western honey bee,
is the premier actively managed pollinator worldwide, highly valued for its
activity as a pollinator and for its production of wax and honey (Delaplane
and Mayer, 2000; Free, 1993; Kearns et al., 1998; McGregor, 1976).
Native to Eurasia, the honey bee has been hunted for its honey and
wax for at least 6,000 years (Crane, 1983, 1990) and records of semidomestication and hive management date back to ancient Egypt (Crane,
1999). A. mellifera rapidly became the primary pollinator for modern agri
culture, and managed colonies were transported around the world, first
arriving in North America with European colonists in the 1600s (Sheppard,
1989a). Modern apiculture in North America dates to 1862, when L. L.
Langstroth, a Philadelphia minister who kept bees as a hobby, exploited
the concept of bee space to construct movable-frame, top-bar hives that
allowed beekeepers to harvest honey, manipulate their colonies, and increase
efficiency without harming the bees (Langstroth, 1862). Langstroths invention resulted in the large-scale commercial beekeeping and honey industry
that exists today.
Honey bees pollinate more than 100 commercially grown crops in
North America (Delaplane and Mayer, 2000; Free, 1993; Kearns et al.,
1998; McGregor, 1976). In the United States, about 135,000 beekeepers

19
manage 2.4 million colonies of honey bees. Most beekeepers (about 94

percent) are hobbyists with 25 colonies or fewer. Another 5 percent are
called sideliners, each managing 25300 colonies. Only about 1 percent are
commercial beekeepers and they generally manage between 300 and 60,000
colonies each to provide most of the nations pollination services (D. Weaver,
The American Beekeeping Federation, presentation to the committee on
October 19, 2005).
Beekeepers in the United States have formed hundreds of local associations and two national trade organizations. The American Beekeeping Federation (ABF) has about 1200 members (ABF, 2005), and the American Honey
Producers Association (AHPA) has about 500 members (S. Park, AHPA,
personal communication, June 12, 2006). The Eastern Apicultural Society,
Heartland Apicultural Association, and the Western Apicultural Society meet
annually and provide extensive educational opportunities for beekeepers.
Many beekeepers, however, do not belong to any formal organization.
Other species of pollinators for which active management systems have
been developed include several species of bumble bees (Bombus), mainly
for pollination of greenhouse tomatoes (de Ruijter, 1997; Hughes, 1996;
Kevan, et al., 1991; Macfarlane et al., 1994; Plowright, 1996; van Heemert
et al., 1990), and leafcutting bees (Megachile rotundata) (Bohart, 1972a;
Frank, 2003), which pollinate most of the alfalfa in parts of the arid Pacific
Northwest (R. Bitner, presentation to the committee, January 14, 2006).
To a lesser extent, alkali bees (Nomia melanderi) (Bohart, 1972a) also are
managed for alfalfa pollination (Stephen, 2003).
Mason bees, including the Japanese horn-faced bee, Osmia cornifrons,
are managed to some extent, mainly for pollination of apple orchards in
the eastern United States (Batra, 1982; Bohart, 1972b), although they are
used extensively in Japan for pollinating the entire apple crop. Several native Osmia species, notably O. lignaria, are used to pollinate apples in the
northwestern United States (Bosch and Kemp, 2002) and in eastern Canada
(Sheffield, 2006) and to pollinate cherries (Bosch and Kemp, 1999, 2000,
2001). Methods for cultivating this species are well developed (Griffin,
1993; Torchio, 2003).
Literature on the culture and management of many alternative pollinators is available (Batra, 1994a,b; Bosch and Kemp, 2001; Free, 1970;
Kevan et al., 1990; Shepherd et al., 2003; Torchio, 1990, 2003). For some
crops, bumble bees, megachilids, and other native bees are more efficient
pollinators than are honey bees (Cane, 2002; Javorek et al., 2002; Maeta
and Kitamura, 1981; Tepedino, 1997) and Osmia species serve as alternative pollinators for almonds (Bosch and Kemp, 2000; Torchio, 2003), red
raspberries and blackberries (Cane, 2005), pears (Maeta et al., 1993), blueberries (MacKenzie et al., 1997; Stubbs and Drummond, 1997a,b; Stubbs
et al., 1997), and sweet clover (Richards, 2003).

20
BOX 1-2
What Is Pollination Worth?

Pollination has value in two very different senses. Its intrinsic value or
essential worth is conceptual, so it cannot be measured easily. The economic
value of pollination is its worth for human ends, as determined through exchanges of goods or services (NRC, 2005).

The aggregate economic value of pollination services is the difference between what consumers are willing to pay (demand) and what it costs producers to provide those services (supply). Consumers willingness to pay comes
not only from direct use of pollination (for example, eating fruits of pollinated
blossoms or enjoying the aesthetics of butterflies visiting garden flowers), but
also from appreciation for the existence of pollinators and their services to
future generations. Where markets do not exist (as for pollination services
provided by wild pollinators), it is difficult to estimate economic value, although
environmental economists have developed methods of approximation (NRC,
2005). Where markets exist (as for agricultural crop pollination), economic
values can be estimated for discrete changes in supply and demand.

For the case of commercial honey bee pollination services, the consumers are the crop growers and the producers are the beekeepers. The demand
curve that describes the number of honey bee colonies the growers are willing
to rent at different prices for pollination is derived from what individual growers expect to earn from yield gains attributable to pollination; their demand
depends on expected crop prices, expected yield gains, and the costs of
available alternative means of pollination. Because growers raise different
crops under different conditions, some are willing to pay more than others.
An almond grower whose production is worth $2,000 per acre will be willing
to pay more than will a grower of apples for cider that is worth less than $500
per acre. The supply curve that describes how many honey bee colonies individual beekeepers are willing to rent out depends on the beekeepers costs
of production and what they can earn from alternative uses of their bees.
Beekeeping also differs in costs and earning opportunities. A beekeeper who
must transport bees a long distance will have higher costs than will one who
An improved understanding of the mechanics of pollination and of its

active management led to the commercialization and worldwide expansion
of many crops, hitherto an impossibility. Common figs (Ficus carica) and
Smyrna figs in California are a case in point. California, second only to
Turkey in fig production, has 18,357 acres in fig production that was worth
nearly $10 million in 1998 (Farrar, 1999). Ficus species are primarily pollinated by agaonid fig wasps in highly species-specific associations (Bronstein,
1988; Machado et al., 2005). Fig production did not become established in

21
is close to an orchard that needs pollination. More details on supply and demand effects and an example relating to almond pollination are presented in
Chapter 4.

Three basic methods have been used to estimate the value of commercial
honey bee pollination services (Table 1-1). The first is simply to equate the
value of services with the amount paid for them (Rucker et al., 2005). The
approach does not capture potential consumer willingness to pay, nor does
it account for beekeepers production costs. The second approach also is the
most common. This method is to estimate the value of pollination services
by taking the total value (market price multiplied by quantity) of a crop and
multiplying that value by a coefficient for the crops estimated dependence on
commercial pollination (Levin, 1983; Morse and Calderone, 2000; Robinson et
al., 1989b). That approach captures consumer willingness to pay, but fails to
subtract beekeepers production costs. It attributes all crop value to pollination
and ignores other inputs required to produce the crop. Neither of the first two
methods considers that a shift in honey bee supply (for example, because of
a new disease or pest) could raise crop prices and thus alter grower demand
for pollination services (Kevan and Phillips, 2001). Southwick and Southwick
(1992) attempted to capture that effect by estimating the price elasticities of
demand for U.S. agricultural crops.

Even where markets exist and price effects are considered, it is impossible to make reliable estimates of the total value of an ecosystem service
such as pollination. The market value of pollination supply shifts can be reliably
estimated only for relatively small perturbations from values that have been
observed in the past. Even the threat of a complete loss of pollination services
would induce some people to pay extraordinarily high prices to prevent a total
loss of the service. Others, however, would do without. Such price-quantity relationships fall well outside prior experience. For pollination services provided
by wild pollinators where markets do not exist, current estimates of nonmarket
value are fraught with limiting assumptions. The economic value of extreme
deviations, such as losing all pollination services, cannot be soundly estimated
(Heal, 2000). If calculable, the economic value of keeping pollination services
would be very high, similar to their intrinsic value.
California until fig wasps were imported in the 1890s for pollination and
growers learned to identify the proper species for pollination and determine
overwintering requirements to synchronize wasp life cycles with the plants
(McGregor, 1976; Swingle, 1908).
Although pollinators are in most cases managed for crop pollination,
there are examples of pollinator management to achieve other goals. Hobby
beekeepers often keep bees primarily for honey production or for personal
satisfaction rather than for pollination. Honey bees have been recruited

22
for delivery of various biological control agents to protect field and greenhouse-grown crops against fungal pathogens and pests (Kevan et al., 2005).
Bees are used to deliver Bacillus subtilis to blueberry flowers to suppress
Monilinia vaccinicorymbosi, or mummy berry disease, a devastating fungus
(Dedej et al., 2004). They also have been used to deliver Trichoderma harzianum 1295-22, a commercially produced agent for control of the pathogenic fungus Botrytis cinerea on strawberries (Kovach et al., 2000). There
is a continuing effort to investigate the potential of honey bees as biological
monitors for environmental contaminants (Bromenshenk et al., 1995) and
land mines (Bromenshenk et al., 2003).
Passive Management
In addition to active management, pollinators can also be managed passivelythat is, their activities can be manipulated by altering environmental
conditions to promote their diversity and population growth or to influence
particular behavior (Shepherd et al., 2003; Vaughn et al., 2004). Passive
management includes farming to promote the growth of floral resources,
providing artificial nest materials and nest sites, and protecting nesting
habitat. All of these practices are designed to increase the diversity of the
pollinator community and the abundances of particular species (Kevan et
al., 1990; Kremen and Chaplin, in press).
VALUE OF POLLINATION
Pollination as a biotic process has both commercial and ecological
value. In the context of agriculture, pollination provides a wide range of
benefits to a broad diversity of commodities across North America. In some
cases, production of the commodity itself results directly from the act of
pollination (for example, fruit production). In other cases, although pollination does not result in production of the commodity itself, the process
contributes to crop propagation (for example, production of seeds used to
grow a root crop such as carrots) or quality (for example, size of tomatoes
has been linked to repeated pollination). There are indirect benefits as well,
through food-chain relationships. Alfalfa seed, a bee-pollinated crop with
an annual value of $109 million (direct effect), is used to produce hay for
livestock forage that is valued at $4.6 billion per year (indirect effect) (Morse
and Calderone, 2000). Although these indirect effects tend to exaggerate the
economic value of pollination, they have been used in several widely cited
studies (see Table 1-1).
The annual value of honey bee pollination to U.S. agriculture has been
variously estimated at $150 million (Rucker et al., 2005), $1.65.7 billion
(Southwick and Southwick, 1992), $9 billion (Robinson et al., 1989a),

23
TABLE 1-1 Value of U.S. Agricultural Production Attributable to Honey

Bee Pollination: Comparison of Studies
Study
Reference
Year
Total
Value
($ billion)
Direct
Crop
Value
($ billion)
Indirect
Crop
Valuea
($ billion)
Animal
Value
($ billion)
Levin, 1983
1980
19.0
5.9
6.0
7.2
Robinson
et al.,
1989a,b
Southwick
and
Southwick,
1992b
Morse and
Calderone,
2000
Rucker et al.,
2005
1985
9.7
6.1
3.6
1986
5.7
5.7
1996
1998
14.6
7.8
6.7
0.15
2004
0.15
Notes
Author
attributes 10%
of cattle value to
bees via alfalfa
hay
Value based on
price elasticity
of supply change
Value is
pollination fees
paid
aCrops
that receive indirect benefits include alfalfa hay, asparagus, broccoli, carrot,
cauliflower, celery, onion, and sugar beet.
bEstimate for no replacement of bees; no price effects.
$14.6 billion (Morse and Calderone, 2000), and $18.9 billion (Levin, 1983).
The annual benefit of honey bee pollination in Canada has been estimated
at $443 million by Scott-Dupree and colleagues (1995). More recent data
are shown on the website of the Canadian Honey Council (http://www.
honeycouncil.ca/users/folder.asp). The lowest U.S. figure is an estimate of
the annual value of pollination fees actually paid by farmers (Rucker et al.,
2005)a value that does not capture the higher fees that farmers would be
willing to pay to ensure good pollination. Table 1-1 compares studies that
include estimates of such willingness to pay for pollination services and it
provides a breakdown of total reported values as direct benefits to crops,
indirect benefits to crops, and indirect benefits to livestock. The value of
direct benefits to crops clusters in the range of $5 billion to $10 billion (the
higher end adjusted to 2005 dollars). Values reported by Morse and Calderone (2000) and by Levin (1983) include indirect benefits of the honey bee
pollination required for seed production in alfalfa hay, asparagus, broccoli,
carrot, cauliflower, celery, onion, and sugar beet. Levin (1983) included 10

24
percent of the value of cattle and dairy production that he attributed to

alfalfa hay whose seed requires bee pollination. Attributing the full market
value of such indirect effects to pollination exaggerates the economic value
of pollination services, because indirect products like alfalfa hay or cattle
require many production inputs besides alfalfa seed. Even the alfalfa seed
made possible by pollination requires that farmers provide other costly production inputs. These and other limitations of estimating economic values
are discussed in Box 1-2. Given the estimates currently available, consistent
comparisons can be made across those economic values based on the direct
effects of pollinators.
The contributions of A. mellifera are not unique: Alfalfa leafcutting
bees and bumble bees also pollinate crops. An estimated $2 billion to $3
billion value in annual crop pollination can be attributed to the activities of
native bees and other insects (Losey and Vaughn, 2006; Prescott-Allen and
Prescott-Allen, 1986; Southwick and Southwick, 1992).
Some vertebrates also operate as pollinators of ecologically and economically important plants. Tropical trees of the family Bombacaceae,
which includes species used for timber, silk cotton, balsa wood, and other
products, rely primarily on bats for pollination (Bawa, 1990; Watson and
Dallwitz, 1992). Many columnar cacti and agaves, which are important
sources of alcoholic beverages (tequila, mescal) and other products (sisal
fibers), also depend on bats and birds for pollination (Arizaga and Ezcurra,
2002; Arizaga et al., 2002; Fleming et al., 2001a,b; Grant and Grant, 1979;
Rocha et al., 2005; Valiente-Banuet et al., 1996; but see also Slauson, 2000,
2001). Globally, pollinators are fundamentally important for the production
of roughly 30 percent of the human diet and most fibers (cotton and flax),
edible oils, alcoholic beverages, nutraceuticals, and medicines created from
plants (Buchmann and Nabhan, 1996; McGregor, 1976; Roubik, 1995).
Estimating the value of pollinators and pollination in natural ecosystems and predicting the consequences of their losses are considerably more
challenging than estimating their economic value in agriculture. Such estimates are complicated by both the number of species involved (globally,
more than 400,000) and the relative paucity of information available for
most of those species. For example, in their effort to calculate the economic
value of ecological services provided by insects, Losey and Vaughan (2006)
did not attempt to place a dollar value on the contributions of pollinators
to maintenance of natural plant communities, although it is reasonable to
assume that a significant proportion of plants in uncultivated terrestrial
communities rely upon pollinators. These plants, in turn, contribute to
many ecosystem services of value to humans, such as water filtration, carbon
sequestration, and flood and erosion control (Daily et al., 1997). An added
complication is that insect pollinators may contribute ecosystem services
other than pollination in their larval stages. The value of these services is

25
equally difficult to calculate, particularly without a complete understanding

of all aspects of pollinators life histories.
Dobson et al. (2006), however, developed a system for assessing the
susceptibility of different ecosystem services to species loss. According to
this system, which takes into consideration trophic level interactions, redundancies, and competition, ecosystem services are classified into Types A
through E, with Type A services at one extreme identified as those in which
species losses are mostly compensated for by co-occurring species and Type
E services identified as the most brittle services; for these services, small
changes in species biodiversity result in large changes in the provisioning of
ecosystem services. In Type C, an intermediate response, a linear decline in
ecosystem service is expected with each species loss. In this system, pollination is considered a Type C or E service for most ecosystems, with species
losses having significant impacts on trophic stability. Indeed, pollination
is the only mutualistic association singled out by Dobson et al. (2006) for
assessment.
STATE OF KNOWLEDGE
The study of pollinator-plant interactions is a thriving, albeit small, area
of inquiry. There are no professional societies dedicated to this pursuit, and
publications in the field appear in a wide range of journals. A search of the
Ovid serials database with the keyword pollination yields 6906 publications for the period 19902005, with the numbers steadily increasing from
2000 onward (see also Figure 1-1 in Kearns and Inouye, 1993). Although
several universities alone or in partnership with state agencies offer classes on
bees and beekeeping (for example, http://www.masterbeekeeper.org/masterbeekeeper.htm, http://www.ento.vt.edu/~fell/apiculture/summer/summerb.
htm, http://www.life.uiuc.edu/entomology/bee-course.html, http://www.
news.cornell.edu/Chronicle/00/5.11.00/bee-course.html, http://neipmc.org/
ipm_news_popover.cfm?id=821), courses in pollination biology are rare, although it often is included as a topic in seminars on plant-insect interactions
(University of Southern Mississippi, Auburn University, Mesa State College,
University of Toronto, Canada). Classes in pollination biology have been
taught in recent years at the University of Arizona, University of California
(Davis and Berkeley), University of Maryland, University of Texas at Austin, St. Louis University, Humboldt State University, and California State
University at Fullerton. In Canada, pollination biology courses have been
recently offered at the University of Guelph, Ontario, and at the University
of Manitoba. In Puerto Rico, a course is offered at the Departamento de
Qumica y Biologa (http://mail.udlap.mx/~cvergara/EcolPol/EcolPol.html).
Many pollination biologists, conservationists, and land managers benefit
from an annual 10-day class (the Bee Course, now in its ninth year, http://

26
research.amnh.org/invertzoo/beecourse) on the systematics and biology of

bees native to the southwestern United States and Mexico that is presented
by the American Museum of Natural History-Southwestern Research Station at Portal, Arizona. In 2006, the McGuire Center for Lepidoptera &
Biodiversity in Gainesville, Florida, announced plans to offer a course on
natural history and identification, captive propagation, host plant care
and needs, field/lab research techniques, permitting/recovery planning
basics, population monitoring, habitat restoration, butterfly exhibitry, education and outreach, partnership building, and the like (http://www.aza.
org/prodev/ButterflyCon/).
Despite the widely held assumption that the birds and the bees in its
literal sense is a concept that is familiar even to schoolchildren, incorporation of pollination biology into primary and even secondary science curricula is far from routine. There are no specific references, for example, to
pollination biology or pollinators in the National Academy of Sciences own
set of science education standards (NRC, 1996) or in the benchmarks for
scientific literacy published by the American Association for the Advancement of Science (AAAS, 1994).
HISTORY OF CONCERN
Concerns about the status of pollinators in North America over the last
quarter-century have arisen in two different contexts. The agricultural community has voiced concerns over fluctuations in the health and availability
of A. mellifera, the principal managed pollinator in the United States, and
associated impacts on crop production, whereas the ecological community
has noted declines worldwide as part of a larger effort addressing biodiversity losses and associated impacts on ecosystem services.
Managed Pollinators
Although the U.S. Department of Agricultures (USDAs) National Agricultural Statistics Service (NASS) reported that 4.2 million colonies of honey
bees were managed by beekeepers in the United States in 1981, the detection of the parasitic honey bee mites Acarapis woodi Rennie and Varroa
destructor (formerly V. jacobsoni Oud; see Anderson and Trueman, 2000)
in the United States in 1984 (Anonymous, 1987; Delfinado-Baker, 1984)
and in 1987 (Delfinado-Baker 1988), respectively, ushered in an era that has
been marked by fluctuations in colony numbers that is overlaid by a general downward trend (Chapter 2). Although A. woodi was very damaging
immediately after its introduction, North American honey bee populations
exhibited some resistance (Chapter 3) and, after several years, deaths from
that parasite appeared to decline. However, the actual contribution of this

27
parasite to changes in honey bee colony numbers was never clearly established. Today, the primary concern among beekeepers is the varroa mite,
which continues to cause major losses of managed hives (Caron and Hubner,
2001; Finley et al., 1996; Lumkin, 2005). Infection with V. destructor is
fatal to most honey bee colonies of European ancestry (Beetsma, 1994;
DeJong, 1990; DeJong et al., 1984; Matheson, 1994; Morse and Gonalves,
1979). The high rate of mortality is the combined result of several factors,
including low levels of natural resistance to mites in the honey bee population; inadequate stock development and production facilities; widespread
use of pesticides, which helps to maintain mite-susceptible genotypes in
the honey bee population; and widespread pesticide resistance in the mite
population.
Few honey bee breeding programs (artificial selection) have successfully
consolidated low levels of existing mite resistance into strains with significant levels of mite resistance (Harbo and Harris, 1999a). Although these
strains hold promise for mite management, they are slowly being integrated
into beekeepers management programs (Chapter 6; Sheppard, 2006).
Honey bees have been widely regarded as having suffered under the
weight of those stresses. NASSs 2005 estimate of 2.41 million honey bee
colonies in the United States is a 28 percent decline from the pre-mite 1981
numbers, after correction for a 1985 change in NASS methodology (Chapter 2). Also, parasitic mites had, by all accounts, an even more serious and
negative effect on the population of feral honey bee colonies (Hoopingarner,
1991; Kraus and Page, 1995; Loper, 1995, 1996, 1997).
These losses occurred as demand for agricultural pollination services
was increasing dramatically, particularly for crops that depend completely
on pollinators. The almond-growing business presents a compelling example
(Figure 1-1). Over the 25 years between 1980 and 2005, U.S. almond acreage increased by nearly 70 percent. Approximately 1.4 million bee colonies
are needed to pollinate 550,000 acres of almonds in California, and in 2005
a shortage of colonies led to imports of colonies from Australia (Flottum,
2005). According to forecasts of the California Almond Board (cited in
Sumner and Boriss, 2006), almond growing will expand to 850,000 acres
by 2012, eventually requiring the services of 2.12 million colonies of pollinators. Other pollinator-dependent crops include squash (Figure 1-2) and
muskmelon (cantaloupe) (Figure 1-3); domestic production of these crops
has nearly doubled over the past two decades.
The growth in demand for crop pollination is not restricted to field
crops. Although USDA does not collect data on acreage of greenhouse tomatoes, other sources suggest a recent large increase. Total greenhouse crop
In
1985, NASS stopped counting beekeeping operations with fewer than five colonies. The
result was an estimated reduction of 0.86 million in the number of colonies meeting its count
criterion (Muth et al., 2003, p. 498).

28
900
Bearing Acreage (1,000 acres)
800
700
600
500
400
300
1980
1985
1990
1995
2000
2005
2010
Historical data from USDA Economic Research Service.

Data from a presentation by the Almond Board Bee Task Force (Heintz, 2005).
FIGURE 1-1 Bearing acreage of U.S. almond trees in 19802010. Almost all almonds
are grown in California.
acreage increased by 40 percent between 1996 and 1999 (Dodson et al.,

2002). In Mississippi, the number of commercial growers went from 15 in
1988 to about 130 in 2006 (Mississippi State University Extension Service,
2006; Snyder, 2006). The top 15 states in greenhouse tomato production
had almost 600 acres in cultivation in 1999 (Snyder, 1999); in 2002, the
total was about 750 acres (Dodson et al., 2002). Greenhouse tomatoes require pollination that is now accomplished mainly by managed colonies of
bumble bees (Chapter 3). The growth in production suggests the demand
for those bees will increase as well.
Wild Pollinators
Concerns about pollinator status are in at least one way unique in
discussions of threats to biodiversity in general, in that such concerns are
often directly and explicitly linked to concerns about the status of another
group of organismsthe mutualistic flowering plant partners of pollinators. Over the past quarter-century, declines in wild pollinator populations

29
of various descriptions have been reported in Europe, Asia, Central and

South America, Africa, and Australia (Allen-Wardell et al., 1998; Biesmeijer
et al., 2006; Donaldson, 2002; Kearns et al., 1998; Oldroyd and Wongsiri,
2006; de Ruijter, 2002). By contrast, few pollinator species are monitored
in North America. Declines in bat populations have been so dramatic that
two of the three U.S. speciesthe lesser long-nosed bat (Leptonycteris
curasoae) and the Mexican long-nosed bat (L. nivalis)are now listed as
endangered under the terms of the U.S. Endangered Species Act. All three
species are listed on the federal list of species at risk of extinction in Mexico
(SEMARNAT, 2002). Around the world, almost half of the insect extinctions documented have involved flower-visiting species (Appendix C). The
first insect to be listed as officially endangered in the United States (Appendix D) was the Schaus swallowtail, Papilio aristodemus, a flower-visiting
species and a presumed pollinator. Flower-visiting Lepidoptera, many of
which are actual or potential pollinators, currently dominate the list of
endangered species: 17 species of butterfly and 3 species of moth constitute
more than half of all insect species listed as endangered (http://ecos.fws.
gov/servlet/TESSWebpage) (Appendix D). Evidence for population decline
1000
Millions of Pounds of Squash
900
800
700
600
500
400
300
1980
1985
1990
1995
2000
2005
FIGURE 1-2 U.S. squash production, 19802005. Available evidence shows that
squash plants must be pollinated by insects, and that honey bees are the chief
pollinators (McGregor, 1976). Source: USDA-NASS.

30
24000
Millions of Pounds Harvested
22000
20000
18000
16000
14000
12000
10000
8000
1960
1970
1980
1990
2000
FIGURE 1-3 U.S. muskmelon production, 19602006. Flowers must be pollinated

to produce cantaloupes. Source: USDA Economic Research Service.
(Appendix E) and local population extinction of other pollinators has begun

to accumulate (Kremen et al., 2002a; Larsen et al., 2005).
Comprehensive recognition of the value of ecosystem services provided by pollinators (Daily et al., 1997; Kremen et al., 2002a, Kremen and
13n
Chaplin, in press) is relatively recent and quantitative studies on pollinator populations in North America are few in number. Among the possible
causes suggested for declines in wild pollinator numbers are fragmentation,
degradation and loss of habitat, nontarget effects of agricultural pesticides,
competition from invasive species, and introduced diseases (Johansen, 1977;
Kearns et al., 1998; Kevan, 1974, 1975a, 1999, 2001; Kremen and Ricketts,
2000; Morandin et al., 2005; Rathcke and Jules, 1993).
Efforts to Address Concern
The concept of a pollinator crisislocalized extinctions and possibly
a global decline in the number and viability of pollinating species contributing to trophic collapse (sensu Dobson et al. 2006)began to gain recognition as a critical issue in the early 1990s. Major losses in managed honey
bee colonies led to concern in the United States about this critical pollinator
(Watanabe, 1994). The publication of The Forgotten Pollinators (Buchmann
and Nabhan, 1996), which extended the concern to nonmanaged species

31
and placed the issue within the greater context of biodiversity decline, galvanized the ecological community. Buchmann and Nabhans book concluded
with a call for a U.S. national policy on pollination and pollinators. Subsequent emphasis of pollination as a fundamental ecosystem service (Daily
et al., 1997) led to an explosion of interest in the international policy arena
(Allen-Wardell et al., 1998; Costanza et al., 1997; Eardley et al., 2006).
Among the first international efforts to address concern specifically
about the status of pollinators was a proposal by the government of Brazil
at the second meeting of the Subsidiary Body on Scientific, Technical and
Technological Advice (SBSTTA) of the Convention on Biodiversity, which
convened in Montreal, Quebec, September 26, 1996 (Appendix F). The
purpose was to establish a program in agricultural biodiversity, which includes an international pollinator conservation initiative (Campanhola
et al., 1998). Subsequently, the Third Conference of the Parties (COP3) to
the Convention on Biodiversity (CBD), which met in Buenos Aires, Argentina, November 415, 1996, drafted Decision III.11, Conservation and
Sustainable Use of Agricultural Biodiversity, identifying pollinators as a
priority group for case studies. That, in turn, led to an International
Workshop on Conservation and Sustainable Use of Pollinators in Agriculture, which placed an emphasis on bees, when it met in So Paulo, Brazil,
in October 1998. The workshop report, Pollinating Bees: The Conservation
Link Between Agriculture and Nature. Proceedings of the Workshop on
the Conservation and Sustainable Use of Pollinators in Agriculture, with
Emphasis on Bees (Kevan and Imperatriz Fonseca, 2002), included the So
Paolo Declaration on Pollinators, which proposed the establishment of
an International Pollinator Conservation Initiative (Dias et al., 1999). An
early response to that call was made at the first meeting of the Systematics
Society of Southern Africa, which founded the African Pollinator Initiative
in January 1999.
The So Paolo proposal was ultimately presented by the Brazilian government to the SBSTTA at its fifth meeting and, at COP5the fifth meeting
of the Conference of the Partiesthe International Initiative for the Conservation and Sustainable Use of Pollinators was created. That initiative was
to promote international cooperation with several goals:
Monitor pollinator decline, its causes, and its impact on pollination
services.
Address the lack of taxonomic information on pollinators.
Assess the economic value of pollination and the economic impact
of the decline of pollination services.
Promote the conservation and the restoration and sustainable
use of pollinator diversity in agriculture and related ecosystems (CBD,
2005, p. 2).

32
The United Nations Food and Agriculture Organization was invited to

coordinate the initiative among the participating nations and agencies and
to devise a plan that was based on the recommendations in the So Paulo
Declaration on Pollinators. In April 2002, the International Pollinator Initiative was approved at the sixth meeting of the Conference of the Parties,
which was convened in the Netherlands (www.biodiv.org/doc/meetings/
sbstta/sbstta-07/official/sbstta-07-09-add1-en.doc). In March 2006, at the
United Nations Convention on Biodiversity, Conference of the Parties,
general meeting 8 in Curitiba, Brazil, the publication, Pollinators and Pollination: A Resource Book for Policy and Practice (Eardley et al., 2006),
was heralded.
Between 1995 and 1999, the tri-national (United States, Canada,
Mexico) Forgotten Pollinators (FP) Campaign was co-founded and directed
by Gary Nabhan and Stephen Buchmann at the Arizona-Sonora Desert
Museum in Tucson, Arizona. During its later years, the FP Campaign
shifted its emphasis to focus on migratory pollinators (bats, hummingbirds,
white-winged doves, monarch butterflies) in the United States and Mexico.
In 1999, the North American Pollinator Protection Campaign (NAPPC)
was launched by the Coevolution Institute in San Francisco, California, in
collaboration with the National Fish and Wildlife Foundation. NAPPC is a
tri-national public-private partnership of more than 100 organizations and
agencies that promote pollinator awareness, policies, educational outreach,
research, and conservation. Also in 1999, USDA and the U.S. Geological
Survey (USGS) sponsored a joint meeting in Logan, Utah (Tepedino and
Ginsberg, 2000), to explore the issue of pollinator decline. In November
1999, the USDA Agricultural Research Service (ARS) convened a workshop to obtain stakeholder input from state departments of agriculture,
universities, pesticide companies, beekeepers, and extension agents on
research priorities for the Bees and Pollination Component of the Crop
Production National Program Writing Teams. These teams were formed
at each of the workshops and consisted of ARS scientists and members of
the ARS National Program Staff. The first function of each was to identify
problem area topics for inclusion in the National Program Action Plan.
Subsequently, individual team members were assigned as principal authors
for each area identified. Writing teams and individual writers used input
from the workshops, their own knowledge, and input from other ARS scientists and cooperators to identify research goals and activities to develop
this action plan (http://www.ars.usda.gov/research/programs/programs.
htm?np_code=305&docid=883).
Also in 1999, the National Science Foundation (NSF) funded a meeting at the National Center for Ecological Analysis and Synthesis (NCEAS)
on pollinator decline, the proceedings of which were published in 2001
(http://www.ecologyandsociety.org/vol5/iss1/art1/) in the journal Conserva-

33
tion Ecology (now Ecology and Society). NSF also provided funds in fiscal
years 20052007 for a series of NCEAS workshops to determine how to
restore pollinators and pollination function in degraded landscapes. Other
federal agencies with an interest in pollinator status include the U.S. Fish
and Wildlife Services Division of Environmental Quality, which maintains
a pollinator website (http://www.fws.gov/contaminants/Issues/Pollinators.
cfm) that has statements on pollinator decline. The USGS National Biological Information Infrastructure, a collaborative program designed to provide
access to data on natural resources within U.S. borders, also has a pollinator
decline program (http://www.nbii.gov).
CHARGE TO THE COMMITTEE
In 2002, NAPPC approached the National Research Council with a
request for a study to review the literature on pollinating animals in North
America. With funding provided by USDA, USGS, and The National Academies, the National Research Councils Board on Life Sciences and Board
on Agriculture and Natural Resources jointly convened an ad hoc committee to document the status of pollinating animals in North America. The
questions to be addressed included whether, and to what degree, pollinators
are experiencing serious decline; in cases where decline can be established
by available data, what its causes are; and what the potential consequences
of decline might be in both agricultural and natural ecosystems. The study
committee was tasked to make recommendations on research and monitoring needs to provide improved information and on any conservation or
restoration steps that could prevent, slow, or reverse potential decline. The
committee also was asked to compile and analyze the published literature,
determine the current state of knowledge on pollinator status, identify
knowledge gaps, and establish priorities for addressing these gaps.
To address its charge, the committee assessed the status of pollinators
in the United States, Canada, and Mexico between the Atlantic and Pacific
Oceans (Chapter 2) and some of the causes of decline in pollinator populations (Chapter 3). However, the extent to which the committee could discuss
each species in different regions depended largely on the availability of data.
The proportion of the report devoted to honey bees reflects the amount of
knowledge and data available for this species. In contrast, the proportion
of the report devoted to wild pollinators reflects the sparse data and our incomplete knowledge on those groups despite their critical role in ecosystem
functioning. The later chapters of the report discuss the potential impact of
pollinator decline in agriculture and natural areas (Chapter 4) and suggest
ways to monitor, conserve, and restore managed and unmanaged pollinators
(Chapters 5 and 6).

2
Status of Pollinators
A definitive assessment of the status of pollinator populations in North

America will hinge on the quality and availability of data from a variety of
well-corroborated sources, and such information is not available for every
taxon. Because of their economic importance, actively managed pollinators
are more likely than are wild pollinators to be closely and systematically
monitored. But even when standardized data are available, interpretation
of patterns of population change can be difficult. Ascertaining a pattern of
decline in wild pollinator species involves consideration of a broader range
of sources of information, including historical accounts, natural history
collections, recently published observations, and comparative analyses. For
some species, population data that are sufficient to inform an assessment of
pollinator status simply do not exist.
POLLINATORS AND THE CONCEPT OF DECLINE
Identifying population declines, particularly for insects, is problematic
primarily because, for many species, there are no historical data on absolute
abundance. Historical accounts (for example, Jones and Kimball, 1943)
often described abundance not quantitatively but qualitativelya species
might be called common, uncommon, or rareso the information
is difficult to interpret or compare. There are, however, numerous reports
of declines of pollinating insects that have been documented according the
strict criteria of federal or state law or regulations or by nongovernmental
organizations. A case in point is the Massachusetts Endangered Species
Act (MESA; 321 CMR 8:00), which requires demonstration of habitat
34

35
threat and population decline before an animal or plant can be listed as

endangered, threatened, or of special concernterms that themselves are
suggestive of particular patterns of population change. However, different jurisdictions can define terms differently, and that causes difficulty for
comparative studies of decline or endangerment. Some species also have
inherently small populations and restricted ranges, and their relative rarity
might not be the result of declining population.
In determining whether pollinator populations are declining, it is important to acknowledge the distinction between a decline and a shortage.
An economically driven shortage of pollinators that occurs as a result of
increased demand could be entirely independent of the condition of pollinator populations. In this report, the term decline is applied to populations
for which the number of individuals is decreasing over time; shortage
means that the supply of pollinators or their services is insufficient to meet
demand. The status of pollinator populations and assemblages can be assessed in many ways, both direct and indirect (see Appendix G for examples
of methods for analyzing pollinator status).
POPULATION TRENDS
Insect Pollinators
Although more than 750,000 insect species have been described
(Grimaldi and Engel, 2005), possibly as many as 30 million more await
discovery and formal description (Erwin, 1982; Stork, 1988, 1996; see also
May, 1999, and Erwin, 2004). Insects comprise the most diverse assemblage
of terrestrial animals, including within their ranks some of the most economically important pollinators and the dominant pollinators in a variety
of natural systems. In some communities, insects pollinate as many as 93
percent of the flowering plants (Bawa, 1974, 1990; Kato, 2000). Unfortunately, the available taxonomic expertise does not exist to document fully
the Earths insect biodiversity (Box 2-1); it is a virtual certainty that many
insect pollinators have yet to be discovered and identified. Notwithstanding
the existence of taxonomic impediments, a substantial body of information
is available on pollinator population trends. The quality of this information,
however, varies with taxon as, accordingly, do conclusions about the status
of pollinators in these groups.
Ants, Bees, and Wasps (Order Hymenoptera)
The order Hymenoptera is a diverse and economically important group
of approximately 125,000 described species comprising plant-feeding sawflies, parasitic and nonparasitic wasps, ants, and bees (Zayed and Packer,

36
BOX 2-1
Diversity and the Taxonomic Impediment

Insects account for more than half of the estimated 1,586,800 species that
have been formally described by scientists (Grimaldi and Engel, 2005). The
most current estimates of species undescribed or unknown to science range
from 10 million to 30 million (Grimaldi and Engel, 2005; Stork, 1988, 1996);
and many of the most species-rich groups are among the least thoroughly
characterized. Because of a lack of available expertise, it is often impossible
to identify (or determine) specimens.

Taxonomy and its applied interface, identification, are fundamental to
continuing the study and conservation of organisms. As knowledge of living
systems grows more comprehensive, the scientific community demands more
from taxonomy than simply identifying which species to avoid and which are
edible or otherwise useful. That the rate at which species are becoming extinct
appears to exceed the rate at which new species are described (Hambler
and Speight, 1996) poses not merely an academic problem but a daunting
challenge to understand biodiversity with economic potential before it disappears. The problem applies to the study of plant-pollinator interactions in North
America as some pollinating insects, particularly beetles and flies, are yet to
be discovered and described.

The Global Taxonomic Initiative is attempting to reduce the bottleneck in
taxonomic research resources in the face of what has been called the greatest
extinction crisis in roughly 60 million years (J.A. Thomas et al., 2004). Under
2005). The order includes within its ranks the principal managed pollinators of the world, bees in the genera Apis, Bombus, Megachile, Osmia, and
Melipona, as well as numerous unmanaged species of bees (Box 2-2) and
wasps that represent a variety of families.
Honey Bees (Apis mellifera)
Nearly 17,000 species of bees have been formally described, and as
many as 30,000 are estimated worldwide (Michener, 2000; T. Griswold,
U.S. Department of Agriculture [USDA] Bee Biology and Systematics Laboratory, presentation to the committee, October 18, 2005). Although other
species are often more efficient pollinators than are honey bees on a flowerby-flower basis, honey bees are, for many reasons, the pollinator of choice
for most North American crops. A. mellifera is highly suitable as a commercial pollinator because of its biology (Hoopingarner and Waller, 1992;

37
the leadership and authority of the Convention on Biological Diversity, the

initiative has two aims: (1) to increase the efficiency of biological systematics,
and (2) to bolster the number of practicing, professional systematists. Critical to the development of greater understanding is a supply of professional
taxonomists, usually university-trained scientists with doctorates in their
disciplines.

The taxonomic impediment is far from an insoluble problem. The Consortium for the Barcode of Life is an international initiative to develop DNA
barcoding as a global standard for identifying specimens. DNA barcoding uses
a short gene sequence from a specific region of a genome as an identifying
marker for a species (http://barcoding.si.edu). DNA barcoding promises to
provide a rapid and inexpensive means of identifying specimens by matching
barcode sequences with those of taxonomically validated vouchers. In the
United States, steps to ameliorate the shortage of professionals include the
highly successful program of the National Science Foundation (NSF) Partnerships for Enhancing Expertise in Taxonomy, which supports taxonomic
research and training (Rodman and Cody, 2003). Assembling the Tree of
Lifeanother NSF effortinvolves advanced molecular and optical technology, readily disseminated Web-based initiatives, and increasingly advanced
analytical software. Whether the federal govenment will continue to support
and expand such programs is an open question. Hence, the first challenges
to solving the taxonomic impediment in North America and globally are to
assess available resources and identify the support and resources needed to
reduce or eliminate taxonomic impediments.
Winston, 1987). In contrast to most other species of bees that have annual
nests founded by individual, overwintered females each spring, honey bee
colonies are perennial. Honey bee populations range between 10,000 and
30,000 individual worker bees, even at their nadir in late winter and early
spring. Thus, honey bee colonies are able to muster large numbers of pollinators when they are needed for late winter and early spring blooms, as
well as throughout the rest of the growing season. As a generalist, the honey
bee can pollinate many agricultural crops, including almond and blueberry.
Because it forages over long distances (up to 14 km from its nest), it is
useful in expansive monocultures where wild bees of other species with
more limited foraging ranges are restricted to field margins. In addition,
honey bees exhibit sophisticated communication, which increases foraging
efficiency, and floral constancy; individuals repeatedly visit a single plant
species during each foraging trip and can recruit nestmates to flowers of
that species (von Frisch, 1967). Thus, honey bees behavior increases the

38
BOX 2-2
Sociality and Bee Pollination

Of the nearly 17,000 described species of bees (Michener 2000), the
vast majority are solitary. Each female makes her own nest and cares for her
own offspring. Among the species of pollinators that are actively managed,
Megachile rotundata, Nomia melanderi, Osmia cornifrons, and Osmia lignaria
all exhibit this solitary lifestyle.

The other species of bees that are actively managed for pollination in
North America, Apis mellifera and various species of Bombus, are eusocial.
Eusociality is defined by three traits: (1) cooperative care of young by members of the same colony; (2) reproductive division of labor, with more or less
sterile individuals (workers) working on behalf of fecund colony members
(queens); and (3) an overlap of at least two generations of adults in the same
colony (Michener, 1969; Wilson, 1971).

Eusociality is the most extreme form of social organization in the animal
kingdom (Wilson, 1971). It is relatively rare, limited to termites (order Isoptera),
several groups of Hymenoptera (all ant species and several lineages of bees
and wasps), and a few species of aphids, thrips, beetles, shrimp, and mammals
(Crespi and Yanega, 1995; Sherman et al., 1995). Eusociality plays a prominent role in pollinator behavior, especially in the case of the honey bee.

Division of labor for reproduction lies at the heart of eusociality. Hymenoptera display the haplodiploid mode of sex determination; fertilized diploid
eggs develop into females and unfertilized haploid eggs develop into males.
Females can develop into either queens or workers. Queens specialize in
reproduction, laying up to several thousand worker eggs per day. Workers
engage in little if any personal reproduction, and perform all tasks related to
colony maintenance and growth, including foraging.

Eusocial species are divided into two groups: primitively eusocial and
advanced eusocial. In most primitively eusocial species, colonies have annual life cycles and populations are relatively small, typically a few dozen to
a few hundred individuals. There are no morphological differences between
queens and workers, but there can be differences in physiology and size.
Division of labor for reproduction is achieved by a dominance hierarchy that
is established and maintained by direct behavioral mechanisms, including
pushing, biting, and physical prevention of egg laying. Aggression is a common occurrence in a primitively eusocial colony. Bumble bee species exhibit
a primitively eusocial lifestyle.

In advanced eusocial species, colonies are typically perennial and populations number in the thousands to even millions of individuals. Queens and
workers are distinguished by striking morphological differences. In advanced
eusocial species, queen inhibition of worker reproduction is achieved by
chemical communicationqueen pheromonesrather than by direct physical
aggression. In advanced eusocial species, the fate of an individualqueen

or workeris determined before adulthood, and there is far less dominancerelated aggression among individuals than in other animal societies. This sets
the stage for natural selection, acting on the phenotypes of colonies, to fashion systems of division of labor among groups of highly specialized workers
and intricate forms of communication to integrate their activities. Honey bees
exhibit an advanced eusocial lifestyle.

Several aspects of eusociality contribute to the value of the honey bee
as a commercial pollinator: (1) Perennial colonies result in large forces of
foraging worker bees, especially early in the growing season, when pollination is required for many crops. Noneusocial species, with annual population
cycles, have far smaller populations early in the growing season. (2) Foraging
in honey bee colonies is based on division of labor. There is an age-related
division of labor among worker honey bees, which is based on a process of
behavioral maturation (Robinson, 1992). After working in the hive for 2 to 3
weeks, worker honey bees specialize in foraging for the remainder of their
4- to 7-week adult life. They take about 10 foraging trips per day and log up
to 800 km over the course of their foraging career (Winston, 1987). Workers
become more efficient at foraging with experience (Dukas and Visscher,
1994), which likely increases their efficacy as pollinators. (3) Foraging in honey
bee colonies also is enhanced by communication. Foragers communicate
the location of particularly rewarding food sources by means of the famous
dance language, elucidated by Nobel laureate Karl von Frisch (1967), the
only nonprimate symbolic language. Honey bees are thus able to rapidly and
effectively direct their foraging force toward a particular field or orchard in
bloom. This can enhance pollination by mobilizing a large group of foragers
during what is sometimes a relatively short window of opportunity. Pollination often is constrained temporally by floral phenology or adverse weather
conditions that limit bee flight (Delaplane and Mayer, 2000). Other traits that
enhance the value of A. mellifera as a pollinator are described in the section
entitled Honey Bees (Apis mellifera) in this chapter.

Other species of bees display levels of sociality that are intermediate
between solitary and eusocial. Communal species nest in aggregations
but do not display any of the three defining traits of eusociality. Megachile
rotundata nests in aggregation, which facilitates their use as an actively managed pollinator. Quasisocial species display cooperative brood care, but no
reproductive castes or generational overlap. Semisocial species display
cooperative brood care and reproductive castes, but no generational overlap.
Some species exhibit different levels of sociality during different phases of the
colony lifecycle. A bumble bee colony, for example, is established by a single
individual, acting in a solitary manner. When the first brood emerges and
assumes responsibility for all colony activities except egg laying, the colony
then becomes primitively eusocial. Bumble bee colonies are most valuable
for pollination during the eusocial phase, when they have an active group of
worker foragers.
39

41
Acarapis woodi (first detected in 1984) and to the Varroa destructor mite
(first detected in 1987) (Chapter 3). The precipitous drop between 1985 and
1986 also is attributable to a change in NASS survey methods that could
represent a statistical artifact. After not collecting data from 1982 to 1985
(official data were based on estimates only), NASS changed its surveys to
exclude beekeepers who had fewer than five colonies.
Assuming that estimates of honey bee pollination activity in agricultural
crops would be improved by more accurate information on total commercial
honey bee colony numbers, the U.S. data have four limitations, most of them
linked to the NASS focus on honey production. First, the surveys count only
honey bee colonies from which commercial honey is harvested; those that
exclusively provide pollination services are not counted. Second, the same
hives can be counted in several states if commercial honey is harvested in
more than one state. Third, annual data are no longer collected on the number of colonies held by beekeepers who own fewer than five hives. Finally,
no data are collected on colony health, a factor that has become more important since the parasitic mite invasions of the 1980s (Chapter 3). NASS
also surveys beekeeping operations every 5 years for its census of agriculture
(USDA-NASS, 2004a). The 2002 census included all honey bee colonies and
reported them in the county where the owner of the colonies largest value
of agricultural products was raised or produced (USDA-NASS, 2004a),
thus addressing the first three limitations above. However, the agricultural
census data are taken less frequently and the variable definitions are incompatible with the annual honey survey data.
In contrast to the declines in the United States, Canada had important
periods of growth in honey bee colony numbers between 1955 and 1986 and
from 1996 to 2005 (Figure 2-2) (Statistics Canada, raw data and 2006). As
in the United States, there was a decline after the period of mite invasions in
the late 1980s, and the Canada-U.S. border was closed to the importation
of live bees in 1987 to prevent the spread of mites from the United States
to Canada (Saskatchewan Agriculture and Food, 2004). Statistics Canada
collects data on honey bees kept for pollination and on those that produce
honey (Statistics Canada, 2006), but there are some inconsistencies in data
collection practices across provinces.
Honey bee colony data from Mexico, available only for 19902003,
show a decline in the total from 2.1 million colonies to 1.7 million colonies
between 1990 and 1997 (SIAP, 2005). With minor fluctuations, colony
numbers remained stable at 1.7 million during 19972003. Mexican honey
production data are available for a longer period, 19802002, but those
data do not show any clear trend. Honey production in the principal states
of Yucatn, Campeche, Veracruz, Jalisco, Guerrero, and Quintana Roo
has fluctuated from 42,000 to 75,000 metric tons, leveling off at 57,000
59,000 metric tons in 20002004 (Ortega-Rivas and Ochoa-Bautista,

43
feral hivesrevealed 75 percent of these colonies no longer existed, and all

surviving colonies were infested with varroa. The proximity of these feral
colonies relative to commercial apiaries led Kraus and Page (1995) to suggest that the mites moved from commercial to feral colonies. Other than
these studies, the committee is not aware of other surveys of feral honey bee
colonies in North America.
Bumble Bees (Bombus spp.)
Approximately 239 bumble bee species are known worldwide (Williams,
1998), 49 of them in the United States. The 41 species in Canada are also
all found in the United States. Twenty species are known in Mexico, nine of
them also present in the contiguous United States (R.W. Thorp, University
of California, Davis, presentation to the committee, January 14, 2006; personal communication, March 2006). Some species of bumble bees (Bombus
impatiens and B. occidentalis) have been managed primarily for pollinating
greenhouse tomatoes (Dogterom et al., 1998). In contrast with managed
honey bee colonies (Apis mellifera) in the United States and Canadafor
which agricultural monitoring agencies often have long-term records of
honey bee colonies (Figure 2-1)data on managed bumble bee colonies are
not collected in the United States, Canada, or Mexico.
Native bumble bees pollinate wild flowers and serve as alternative or
complementary pollinators for some crops, such as watermelon and cucumber (Stanghellini et al., 1996a,b). Although many native bumble bee species
in the United States were once common, entomologists and naturalists have
been noting declines and regional absences of some species within the past
decade. The Xerces Society for Invertebrate Conservation has placed four
bumble bee species (Appendix H) on its Red List of at-risk pollinator insects
of North America (Shepherd et al., 2005).
Bombus (Bombus) franklini (Frison, 1921), the Franklin bumble bee,
is (or was) an endemic species with the most restricted geographic range of
any bumble bee in North America and possibly the world (Williams, 1998).
Its range, known at one time to span from southwest Oregon to northwest
California, encompasses a distance of 241 km north to south and 112 km
east to west. Within that area, B. franklini could be found at elevations from
162 m in the north to above 2,340 m in the southern portion of its historic
range. B. frankilini is thought to have become extinct recently in its native
range of the U.S. Pacific Northwest (Buchmann and Ascher, 2005; Shepherd
et al., 2003, 2005). Thorp (2003, 2005) first began to notice and document
a precipitous decline in B. franklini at numerous localities in 1988. Extensive
searching by R.W. Thorp and his colleagues over the last 4 years has failed to
re-locate B. franklini populations or individuals across that region (Thorp,
2003). B. franklini is now treated as a species of concern or a special

44
status species by the U.S. Fish and Wildlife Service, the California Natural
History Data Base, and the Oregon Natural Heritage Information Center.
It also appears on the Xerces Society Red List (Appendix H; Shepherd et
al., 2005).
B. occidentalis, at one time commonly observed in central California,
began in the late 1990s to disappear from most of its known geographic
range. Thorp (2003, 2005) conducted extensive searches for B. occidentalis
and reported that it is now extremely rare in habitats where it was formerly
common. The species is still present in some parts of its range, such as the
Colorado Rocky Mountains; it is still relatively common near the Rocky
Mountain Biological Laboratory as of 2006 (D. Inouye, University of Maryland, personal observation, 2006).
B. affinis apparently disappeared from northern New York state about
1998 and from southern New York before 2004 (Day, in preparation; J.
Ascher, American Museum of Natural History, personal communication,
March 2006). John Ascher of the American Museum of Natural History reports that B. affinis was common on the Cornell University campus between
1996 and 1998, but that he and other entomology students and faculty have
not observed it since 2001. Despite collecting more than 1,200 bumble bees
in the Black Rock Forest of New York during 2003, Giles and Ascher (2006)
failed to find any specimens of B. affinis.
Because there is no long-term monitoring or corresponding baseline
data for bumble bees or other species of wild non-Apis bees in the United
States, Canada, or Mexico, the population status of bumble bees cannot
be determined definitively in North America. The United Kingdom, in contrast, has a long and well-established tradition of monitoring by scientists
and naturalists. Extensive standardized monitoring protocols are followed
across a grid system covering the entire United Kingdom. The Bees, Wasps
and Ants Recording Society was established in 1978 expressly to allow
anyone of any age or experience with an interest in aculeates (ants, bees,
and stinging wasps) to contribute to a recording scheme designed to obtain
proper, well coordinated data on the distribution and habitats of many
species in order to support conservation programmes, ecological research,
and to promote effective conservation strategies on a national basis
(http://www.searchnbn.net/organisation/organisation.jsp?orgKey=222). The
ALARM project (Assessing Large Scale Risks for Biodiversity with Tested
Methods) was established in 2004 with the objective of assessing changes
in the richness, abundance, and distribution of pollinators across Europe
(Box 2-3). This project and several other studies show that decline in species
richness, frequency, and distribution of bees is evident (Box-2-4; Goulson et
al., 2005; Westrich 1989, 1996) if these parameters are carefully monitored
or observed. Records of species richness, frequency, and distribution of bees
in North America are few in number.

BOX 2-3
The ALARM Project
Changes in Bee and Flower Fly Richness, Abundance, and
Distribution Documented

In 2004, the ALARM project (Assessing Large Scale Risks for
Biodiversity with Tested Methods) was initiated and funded as part of
the United Nations Food and Agriculture Organization. Details of the
program are presented in Chapter 5, but one component relevant to this
discussion is the effort to quantify distribution shifts in keystone pollinator groups across Europe. ALARM researchers conducted an extensive
before-and-after 1980 repeat survey of native bees and flower flies in
the United Kingdom and the Netherlands (Biesmeijer et al., 2006). Each
country was divided into 10 x 10 km grid cells and species richness and
abundance were analyzed on the basis of more than 500,000 authenticated records. A landscape-level rarefaction analysis (Colwell et al., 2004;
Krebs, 1999; Magurran, 2004) was conducted from the United Kingdom
and Netherlands data sets and analyzed with EstimateS 7.5 software
(Colwell, 2005).

The results of these first comprehensive national surveys of pollinators show widespread decline of bees and syrphid flies. Species richness
of bees declined in about 40 percent and 60 percent of the grid cells in
the United Kingdom and the Netherlands, respectively. In the United
Kingdom, 18 percent of the grid cells showed increases and 45 percent
had the same species richness. The national data from the two countries
allowed researchers to ask whether individual pollinator species were
changing in distribution and abundance. Of the 229 bee species assessed
in the United Kingdom and the 201 species assessed in the Netherlands,
more showed declines in abundance from before to after 1980 (based
on the total number of times each species was recorded across all grid
cells in which they were present in those two periods) than stayed stable
or decreased. In the Netherlands, the number of species that showed
area loss (range contraction) was substantially higher than the number
that showed area gain (range expansion), with an overall significant decrease in occupancy. In contrast, no clear trends in range changes were
observed in the United Kingdom. When abundance and range changes
were considered together, there were statistically significant declines in
native bees in the United Kingdom and the Netherlands (Biesmeijer et
al., 2006). The findings are consistent with studies of status for butterflies
(Asher et al., 2001; J.A. Thomas et al., 2004), for bumble bees (Rasmont
et al., 2006), and for native European bees (Banaszak and Kosior, unpublished data; Srospataki et al., 2005).
SOURCE: Biesmeijer et al., 2006.
45

46
BOX 2-4
European Bee Surveys and Population Declines

A United Nations Food and Agriculture Organization report, The Survey
of Wild Bees (Hymenoptera, Apoidea) in Belgium and France (Rasmont et al.,
2006), presents evidence of pollinator declines among diverse taxa of bees
native to those countries during the past 30 years. The Belgian Mons and
Gembloux government laboratories published their first report on native bees
of Belgium and France in 1980 (Leclercq et al., 1980), listing 13 species of
the superfamily Apoidea at risk in Belgium, Luxembourg, and northern France.
A subsequent report (Rasmont and Mersch, 1988) presented information on
the faunistic drift of Belgian bumble bee species; that report cites the first red
list of threatened insects in the Belgian fauna. The 1988 report was updated
and revised in 1993 (Rasmont et al., 1993) to include general findings about
the entire Belgian bee fauna of more than 300 species. After 1993, research
teams at the two Belgian laboratories expanded their bee survey efforts to
other areas and countries, including France (Pauly, 1999; Rasmont and Adamski, 1995; Rasmont and Gaspar, 2002; Rasmont et al., 1995), Morocco
(Rasmont and Barbier, 2003), Turkey (Rasmont and Flagothier, 1996), and
even Madagascar (Pauly et al., 2001). Rasmont and his colleagues have
prepared biogeographic, faunistic surveys and taxonomic revisions of bee
genera at continental scales (Andrenidae: Patiny, 1998; Patiny and Gaspar,
2000; Anthophoridae: Terzo and Rasmont, 2004; Melittidae: Michez et al.,
2004a,b; Terzo and Ortiz-Sanchez, 2004).

To date, 360 species of bees have been reported in Belgium; of these,
330 species of solitary bees (Apoidea) were documented as occurring within
Belgium between 1900 and 1992 (Rasmont et. al., 2006). In that period, 91
species (25.2 percent) were decreasing in abundance, 145 (40.2 percent)
remained relatively stable, 39 (10.8 percent) had expanded their ranges,
and 85 species (23.5 percent) were placed in an undetermined situation as
rare species. These data were collected from more than 48,000 records and
79,765 specimens. Results from the study published by Rasmont and colleagues (2006) confirmed that 13 of the same species were decreasing as
had been reported by Leclercq et al. (1980). Rasmont and colleagues (2006)
also reported a sharp contraction in most cleptoparasitic (cuckoo bee) species
and hypothesized that their bee host species had declined. The report also
discussed a decline among mason bees (Osmia spp.) that use snail shells
as nesting substrates. The same observation had been reported earlier by
Westrich (1990). With respect to the overall pattern of change, Rasmont and
colleagues (2006) state:

In an untouched wild bee fauna, the isolated regression of a longtongued species could probably be ecologically compensated for by
the spontaneous substitution of competing species. However, in the
present situation, it is the whole guild that is threatened. Therefore,
we may fear that the linked regression of all species will not allow
a spontaneous replacement. It is likely that the density and the
diversity of these pollinators fall under the population level needed
to insure the pollination requirement of many agricultural and horticultural productions. Moreover, the regression of key species would
lead to the disappearance of great parts of the wild flora.

Rasmont and colleagues (2006) make a special case to discuss the plight
of bumble bees in Europe. They reported a continental decline in abundance
in several bumble bee species. The most dramatic case was for Bombus
cullumanus (Kirby). At the start of the 20th century, B. cullumanus was seen
as far north as southern Sweden and was abundant in northern Germany,
the Netherlands, and England. It had been observed in large cities, such as
Brussels and Paris, since the 1950s. By the 1990s, it had disappeared from
most of its former range. Today, it can be found only in a few dozen localities
in the West and East Pyrnes and in western portions of the Massif Central
mountains, and it is now rare wherever it is found (Rasmont et al., 1993).
The authors reported that other bumble beesB. confusus Schenck, B.
distinguendus Morawitz, and B. sylvarum (L.), all long-tongued species associated with leguminous floral hostsalso experienced contractions within
their respective ranges. A few, however, have actually expanded their ranges.
B. semenoviellus (Skorikov), originally known from Moscow, can be now found
in northern Germany and is expected to colonize the Netherlands and Belgium
in the next few years.

Another formerly common, now rare, species is the leafcutting bee
Megachile parietina (Goeffroy) (= Chalicodoma muraia Retzius) in France.
Toward the end of the 19th century, when Jean-Henri Fabre was writing his
famed Souvenirs Entomologiques, this leafcutting bee was common enough
to be considered a pest in buildings. It has become rare throughout France,
for unknown reasons (Rasmont and Barbier, 2003). M. parietina is a visitor
to legume flowers, so its population decline could be symptomatic of a larger
problem among native leguminous plants and their pollinators in France and
Belgium. A rare carpenter bee, Xylocopa cantabrita Lepeletier, was formally
known only from a few localities in France and Spain. Terzo and Rasmont
(2004) relocated that rare bee during recent faunal surveys.
47

48
Mexican Stingless Bees (Melipona and Trigona)

Stingless bees, species in the tribe Meliponini, comprise about 400 species found in neotropical and paleotropical forests (Roubik, 1989). These
social bees form long-lived colonies, make and store honey, and are important pollinators of forest trees and crops. For millenia, ancient and modern
Mayan peoples of southernmost Mexico and neighboring countries have
kept the meliponine bees of their tropical forest environments in hollow log
hives (jobones) in or near villages. Stingless bees have supplied the Maya
with honey for food and for medicine and with beeswax as a sealant and
art material (Crane, 1999).
Mayan beekeepers have traditionally searched for stingless bee colonies in the low tropical forests of the Yucatn, traveling several kilometers
from their villages to locate wild colonies of Melipona and Trigona. Today,
beekeepers must travel even farther into smaller patches of remnant forests
of large-diameter trees (used by stingless bees for nesting cavities) to find
Melipona colonies (Villanueva, personal communication, March 2006).
In the past, bee houses with traditional log hives contained dozens or
hundreds of colonies, and beekeepers knew how to divide and reproduce
colonies (Villanueva-Gutierrez et al., 2005). It is now uncommon to find a
beekeeping operation with more than five colonies of Melipona in villages
near Felipe Carillo Puerto, Quintana Roo (Vilanueva-Gutierrez and Roubik,
personal communication, March 2006).
Ancient Mayan beekeeping is disappearing because of habitat fragmentation and intensive apiculture. A recent survey (Villanueva-Gutierrez et al.,
2005) documented that 93 percent of the managed Melipona and Trigona
stingless bee colonies in the Yucatn Peninsula have been lost during the
past quarter-century (Table 2-1). Hurricanes in the past two decades have
also decimated feral and managed colonies of Yucatecan stingless bees.
Villanueva-Gutierrez and colleagues predict there will be no managed colonies of Melipona and Trigona in Yucatecan Mayan lands by 2008 unless
action is taken to maintain the bee colonies (Villanueva-Gutierrez et al.,
2005).
Sixteen species of gentle native bees are found within the Yucatn
Peninsula, where they pollinate forest trees, Mayan dooryard gardens, and
milpa agricultural lands. There are no studies on population trends of feral
meliponines, although Brquez (2003) examined the distributional limits
of meliponines in northwestern Mexico. They are not present in the United
States or Canada.
Orchid Bees (Euglossa, Eufriesea, Exaerete, Eulaema)
Orchid bees (family Apidae, tribe Euglossini) constitute a natural group
of approximately 250 brilliant metallic-green, blue, and red species from

49
TABLE 2-1 Number of Melipona Hives That Beekeepers from the

Mayan Zone (near Felipe Carillo Puerto, Quintana Roo, Mexico) Have
Kept During the Past 54 Years
Name of Mayan
Community
Name of Beekeepers
or Institutions
Chan Santa Cruz

Chan Santa Cruz
Chanc de Repente
Chanc de Repente
Chanc de Repente
Chuny
Felipe Carrillo Puerto
Delfino Naal
Nemesio Pot
Bernardo Pea
Anastasio Perez
Eduardo Yam
Patricio Canul
Instituto Nacional
Indigenista
Santiago Pat
Fernando Yam
Francisco Cim
Jun Mena
Celestino Camal
Ponciano Tun
Margarito Tuz
Bernab Kantn
Humberto Ku Cauichl
Francisco HuiCab
Doroteo Pech
Jos Pott
Pedro Cahun Uh
Isidro Pea Tuz
Modesto Chuc
Isaas Cahuich
Rancho San Martn
Miztequilla
Miztequilla
Naranjal
Naranjal
Nueva Lora
Nuevo Israel
Palmas
Presidente Jurez
San Hermenegildo
Santa Mara
Seor
Seor
Tihosuco
Tuzic
X hazil
X hazil
Yo Actn
Totals
Number of
Hives Kept
Between 1950
and End of 1981
Unknown
Unknown
42
Unknown
Unknown
45
0
Unknown
40
25
26
Unknown
Unknown
220
Unknown
60
50
22
Unknown
Unknown
200
10
15
Unknown
Likely >1000
Number of
Hives Kept
at End of
1990
Number of
Hives Kept
at End of
2003
8
12
25
10
5
30
40
2
8
8
0
0
8
11
6
19
15
12
7
6
5
16
40
37
18
6
5
40
7
10
10
389
2
8
3
6
2
0
0
4
0
7
0
0
15
8
0
0
4
96
SOURCE: Villanueva-Gutierrez et al., 2005.
the neotropical forests of Mexico south into Central and South America
(Cameron, 2004; Michener, 2000; Roubik and Hanson, 2004). Although
an errant Eulaema male was discovered in the United Status (Minckley and
Reyes, 1996), orchid bees live in neotropical forests and can be found in
Sonora and Sinaloa (Alamos region) and farther south, including the rainforests of Quintana Roo, Mexico. Euglossines historically have comprised
up to 25 percent of the total bee fauna in many intact neotropical forests,
and they are thought to be excellent indicators of disturbance (Roubik and
Hanson, 2004; Roubik, personal communication, March 2006). Within
intact forests, however, euglossine populations are extremely stable, and
some species might even be increasing (Roubik, 2001).

50
TABLE 2-2 Examples of Bees in North America and Some of the Plants
They Visit and Pollinate
Common Name
Scientific Name
Alkali bee
Blueberry bee
Carpenter bee
Digger bee
Nomia melanderi
Habropoda laboriosa
Xylocopa spp.
Andrena, Colletes, and
Melissodes spp.
Megachile rotundata
Osmia lignaria
Peponapis pruinosa
other Peponapis and
Xenoglossa spp.
Eumegachile pugnata
Alfalfa leafcutting bee

Blue Orchard bee (a mason bee)
Squash and gourd bee
Sunflower bee
Examples of Crop Plants

Pollinated
Alfalfa, clover, mint
Blueberry
Passion flower, eggplant, pepper
Cotton, fruit trees
Alfalfa
Almond, apple, sweet cherry
Squash, pumpkin, gourds
Sunflower
Other Bees
Other than honey bees and bumble bees, more than 3,500 species of
solitary bees pollinate crops and wild plants in North America. Examples
of native bee pollinators include alkali bees, squash bees, and leafcutting
bees (Table 2-2). A number of native bee species are rare and have narrow
geographic ranges or have not been collected for many decades. The Xerces
Society Red List for bees is presented in Appendix H, Table H-2.
Ants
All 11,844 named ant species are eusocial, ecologically important insects
(Agosti and Johnson, 2005; Hlldobler and Wilson, 1990, 1994; Wilson and
Hlldobler, 2005). Common in most plant communities, ants visit plants
and collect sugars. Interactions with flowering plants involve mutualisms
that include dispersing seeds, visiting extra-floral nectarines, serving as
guards against seed predators or herbivores, and in some cases pollinating flowers (Beattie, 1985; Boucher, 1985; Bronstein, 1944a,b; Bronstein
and McKey, 1998; Buckley, 1982; Huxley and Cutler, 1991; Janzen, 1985;
Rico-Gray and Oliveira, 2006; Thompson, 1982, 1994, 2005; Wilson and
Hlldobler, 2005). Although ants are collectively involved in thousands
of interactions with plants and are commonly observed on flowers, they
pollinate few species (about 20) of angiosperms (Table 2-2; Beattie, 1985;
Peakall et al., 1991; Rico-Gray and Oliveira, 2006; Thien and Rico-Gray,
2004). Nevertheless, many ant-plant mutualisms other than pollination
greatly increase the reproductive success of plants and ants.
The 20 flowering plants (18 genera, 9 families) pollinated by ants
(Table 2-3) occur in a variety of habitats throughout the world. Of the

51
TABLE 2-3 Plant Species in North America

Pollinated by Ants
Species
Caryophyllaceae
Arenaria tetraquetra
Gypsophyla
Paronychia pulvinata
Crassulaceae
Diamorpha smalli
Brassicaceae
Lobularia maritime
Euphorbiaceae
Euphorbia cyparissias
Orchidaceae
Mirabilis nyctaginea
Epipactis palustris
Maxillaria parviflora
Polygonaceae
Eriogonum pelinophilum
Polygonum cascadense
Orthocarpus pusillus
References
Gmez et al., 1996
Gmez et al. 1996
Puterbaugh, 1998
Gomez et al., 1996; Wyatt, 1981;
Wyatt and Stoneburner, 1981;
Gmez, 2000
Schurch et al., 2000
Cruden, 1973
Brantjes, 1981; Nilsson, 1978
Singer, 2003
Bowlin et al., 1993
Hickman, 1974
Kincaid, 1963
16 subfamilies of ants, the Ponerinae, Myrmicinae, Formicidae, and

Dolichoderinae (Grimaldi and Engel, 2005; Wilson and Hlldobler, 2005)
are commonly involved in plant interactions (more than 33 genera; antagonistic and mutualistic) (Rico-Gray and Oliveira, 2006).
There are no databases that monitor fluctuations in ant populations.
Recent studies, however, have documented population shifts of groups
of organisms that include ants (Christian, 2001; Forys and Allen, 2005;
Haugaasen et al., 2003; Morrison, 2002; Richardson et al., 1996; Roberts
et al., 2000; Torres and Snelling, 1997). Currently, the Conservation International Tropical Ecology, Assessment, and Monitoring project (http://www.
teaminitiative.org) tracks litter and ant diversity in Costa Rica (Agosti et
al., 2000; J.T. Longino, Evergreen State College, personal communication,
October 2005). An excellent source of information on ant databases in
general is http://antbase.org, a website maintained jointly by the American
Museum of Natural History and the Ohio State University.
Wasps
Most of the approximately 100,000 described wasp species worldwide
are carnivorous, preying on other insects. Many others are parasites, laying their eggs on or inside immature insects or other living hosts. The large

52
digger wasp family (Sphecidae) contains approximately 9,550 species,

most of which are carnivorous, seeking out insect prey to provision their
larval cells (http://www.calacademy.org/research/entomology/Entomology_
Resources/Hymenoptera/sphecidae/Number_of_Species.htm). Although
sphecids are not always hairy or good pollen vectors, many adults that visit
flowers to search for nectar might serve as pollinators. Similarly, some species within the large spider wasp family (Pompilidae) seek out flowers for
nectar. Their spiny legs pick up and transport the specialized pollinia of milkweed plants (Asclepias spp.) and they can be effective pollinators (Kephart
and Theiss, 2003). One group of large wasps that has adopted a flowervisiting, pollen-collecting, larval-provisioning lifestyle includes the subfamily
Masarinae within the family Vespidae. Two genera (Pseudomasaris, with 14
species limited to the western United States, and Euparagia with 6 species)
are found in the United States. Euparagia species visit Eriogonum blossoms
for nectar, but provision nests with paralyzed weevil prey items. Unlike bees,
Pseudomasaris wasps actively harvest pollen and nectar and then provision their underground brood cells with pollen or nectar instead of live or
paralyzed arthropod prey (spiders, pompilid wasps, weevils). Many masarid
species have elongate mouthparts that are specialized for extracting nectar
from long tubular blossoms. In the southwestern United States, species of
Pseudomasaris are oligolectic (their pollen foraging is restricted to particular genera or to a single genus within a plant family), and they provision
their nests with pollen and nectar largely from flowers of plants within the
families Hydrophyllaceae, Polygonaceae, and Scrophulariaceae. They are
principal pollinators of species of beardstongue (Penstemon spp.), including
the endangered P. grahamii (http://www.epa.gov/fedrgstr/EPASPECIES/
2006/January/Day19/e363.htm), Phacelia, Hydrophyllum, and Eriodictyon.
Pseudomasarines are important to the ecology of these wildflowers, and they
play ecosystem service roles in the southwestern United States and Mexico.
Within the southwestern United States, several masarid species are restricted
to highly localized habitats or have not been collected in decades (Richards,
1963, 1966). Pseudomasaris micheneri is known only from the Inyo Mountains of Inyo County, California (Westgard Pass), and only from collections
made during the 1930s and 1940s. It has not been collected since then.
Pseudomasaris macneilli is known from only two locations in northern California (Trinity Alps) and one location in Utah. Those collections were made
during 1951 and 1961. Similarly, Pseudomasaris macswaini has a localized
distribution and could be at risk (Richards, 1963, 1966). Further exploration and collection in known habitats when Phacelia and other floral hosts
are in bloom will be necessary to determine the current status of masarine
populations in North America.
An example of pollinator-plant interdependence involves the so-called
fig wasps. The term fig wasp has been broadly applied to many plant-

53
feeding chalcid wasps (Chalcidoidea) that have mutualistic relationships

in inflorescences (synconia) of fig trees (Ficus, Moraceae). There could be
several hundred such species, although many are still undescribed (Weiblen,
2002). Formerly, these wasps were all placed within the family Agaonidae.
Molecular studies and DNA sequences indicate that the five families containing fig wasps (Agaonidae, Eurytomidae, Pteromalidae, Ormyridae, and
Torymidae and the subfamilies Epichrysomallinae and the Sycophaginae)
are not closely related (Campbell et al., 2000; Machado et al., 1996;
Rasplus et al., 1998). The Sycoecinae, Otitesellinae, and Sycorctinae have
been placed in the Pteromalidae, which leaves only the truly fig-pollinating
wasps in the Agaonidae. Forty-seven genera, comprising approximately
800 species worldwide of fig-loving wasps are recognized as pollinators of
Ficus species. There are 21 species of Ficus in Mexico, two in the United
States (Florida), and none in Canada. Unlike most flowering plants, which
can be pollinated by a guild of pollinators and floral visitors, each Ficus
species typically is primarily pollinated by one, or sometimes two, species
of agaonid fig wasps (Weiblen, 2002). Some wasps associated with figs, but
not typically thought of as pollinators, can enter through fig ostiolessmall
openings in the fruitto effect pollination (Jousselin et al., 2001).
Originally native to western Asia and the Mediterranean, the edible fig
(Ficus carica) is the only species cultivated commercially for fruit production. In the United States, California dominates, with 98 percent of U.S.
fig production (60,000 tons), although according to the USDA Economic
Research Service (ERS), figs are grown commercially in at least 14 states
(USDA-ERS, 2004).
Twenty-one species of Ficus are indigenous to Mexico; none of these
tropical species can survive unaided in Canada. Two native Ficus species
are known in the continental United States, occurring naturally in southern
Florida (F. aurea and F. citrifolia). Only five species of agaonid fig wasp are
known from Mexico, although unreported species could occur there (Noyes,
1998; Rasplus et al., 1988; J.Y. Rasplus, personal communication, January
2006). Despite the importance of fig wasps to pollination of Ficus, there are
no published studies documenting population trends in this group.
Beetles (Order Coleoptera)
With about 350,000 described species, beetles (Coleoptera) constitute
the largest insect order (Grimaldi and Engel, 2005). Beetles often are ignored
as pollinators because both the larvae and the adults of so many species destroy the reproductive organs of wild and domesticated seed plants (Borror
et al., 1989). However, beetle pollination is believed to have contributed to
the pollination of different lineages of flowering plants for over 120 million
years (Bernhardt, 1999, 2000) as shown by the preponderance of beetle pol-

54
lination in surviving species of basal (magnoliid) angiosperms (Bernhardt

and Thien, 1987) and in reconstructions of flower and beetle fossils (insects
that belonged to still extant lineages associated with pollen consumption).
In a review of the international scientific literature published between
1906 and 1999, Bernhardt (2000) reported that 34 families (representing
some 170 discrete species) of flowering plant contain at least one species
pollinated primarily by beetles. Another 79 generalist species distributed
within 22 families of flowering plants are pollinated by beetles with other
animals, including flies, bees, and birds. Pollinating beetles come from at
least 27 families within the order. Beetle behavior on flowers varies according to insect species and sex, and some effect pollination while searching
for edible rewards (nectar, pollen, starchy food bodies).
The number of pollinating beetle species cannot be estimatedanother
result of the acknowledged taxonomic impediment (Box 2-1). Knowledge of
known beetle species as effective pollinators of U.S. and Canadian vegetation continues to lag behind information about native bees, bats, and birds
in the two countries. An estimated 52 U.S. and Canadian plant species are
pollinated by beetles (Table 2-4). However, similar estimates are not available in Mexico, and the role of North American flower-visiting beetles as
pollinators has yet to be assessed.
Beetle pollination is usually associated with tropical latitudes (reviewed
by Bernhardt, 2000). The extent of beetle pollination within the flora of the
United States, Canada, and northern Mexico is open to speculation; few
studies confirm that beetles contact both receptive pistil tips and pollenshedding anthers while they forage or find mates (Table 2-3). The role of
beetles as pollinators of temperate, North American flora differs by plant
geography so that the role a beetle species plays in pollination of temperate, North American flora could change with the distribution of the plant
species. In the Southeast, most yellow pond lilies (Nuphar) are pollinated
by the chrysomelid beetle, Donacia crassipes (Schneider et al, 1977). As
this genus of water lily has expanded its distribution northwards (it also
has been introduced into European water ways), it is pollinated by insects
in other orders (Herring, 2003; Lippok and Renner, 1997; Renner and
Johanson, 1995).
There are no beetle-pollinated crops in Canada or the United States, unless the recent attempts to domesticate and commercialize fruit production
in American species of paw paw (Asimina spp.; Norman and Clayton, 1986)
are considered. Most Annona spp. sold as custard apples, sugar apples,
or soursops are beetle pollinated (Gottsberger, 1989a,b), as is Myristica
fragrans (Armstrong, 1986), the source of the commercial sister species,
nutmeg and mace.
In the United States and Canada, beetle pollination is economically
important in the context of significant numbers of annual and bulbous or-

55
TABLE 2-4 An Illustrative List of Indigenous Beetle-Pollinated Plants

of Canada and the United States (Common Names of Plants are in
Parentheses)
Other
Pollinators
Plant Genus
Taxa of Pollinating Beetles
Asimina (paw
paws, 8)
Euphoria sepulchralis
Trichius spp.
Trichotinius lunulatus
T. piger
T. rufobrunneus
Typocerus zebra
Calopterus truncatus
Bombus, flies
Kral, 1960; Norman

and Clayton, 1986
Staphylinid
beetles
Grant, 1950
Acanthoscelides sp.
Acmaeodera sp.
Anastranglia sp.
Anthaxia sp.
Anthremus sp.
Brachysomida sp.
Cryptorhorpalum sp.
Diabrotica sp.
Emmenotarsus sp.
Eschatocrepis sp.
Eutrichopterus sp.
Hippodomia sp.
Judolia sp.
Listrus sp.
Mordella sp.
Mordellistena sp.
Nemognatha sp.
Tricochrous sp.
Trichodes sp.
Trichochrous sp.
Bees, flies, and

moths
Dilley, 2000
Calycanthus
(W. spice
bush, 1)
Calochortus
(mariposa
lilies, 26)
Ipomopsis
(gilia, 1)
Linanthus
(linanthus, 1)
Trichochrous sp.
References
Grant and Grant, 1965

Grant and Grant, 1965
continued

56
TABLE 2-4 Continued

Other
Pollinators
Plant Genus
Taxa of Pollinating Beetles
Magnolia
(magnolias,
10)
Bees
Acmaeodera pulchella
Aleochara lata
A. sp.
Allecula punctulata
Amaspis rufa
Arthromacra aenea
Collops tricolor
Copidita thoracica
Conotelus sp.
Derelomus bicolor
Diabrotica duodecimpunctata
Epuraea ovata
E. duryi
Gaurotes cyanipennis
Goes debilis
Gyrophaena sp.
Leptaura sp.
Macrodactylos angustatus
Mordella discoidea
M. melaena
M. octopunctata
M. sp.
Nitidula sp.
Ophistomis bicolor
Phyllopaga fervida
Prionomerus calceatus
Satira gagatina
Sitophilus oryzae
Strangalina luteicornis
Staphylinus sp.
Trichiotinus innulatus
T. piger
T. trinotata
Typoceros zebra
Donacia crassipes
Bees, flies
Nuphar (yellow
pond lilies, 3)
Saururus
(lizards tail,
1)
Xerophyllum
(bear grass, 1)
Trichiotinus spp.
Anastrangalia laetifica
Cosmosalia chrysocoma
Epicauta sp.
Leptaura propinqua
Trichodes ornatus
Total Plant Species
Total Pollinating Beetles Identified to Species
Bees, flies,
wasp, and
wind
Flies
References
Thien, 1974
Lippok and Renner,

1997;
Schneider et al., 1977
Thien et al., 1999
Vance et al., 2004
52
36

57
namental flowersgarden favorites on hybrids and cultivars derived from

wild species native to the Mediterranean basin and southern Africa, whose
ancestors are beetle pollinated (Dafni et al., 1990; Goldblatt et al., 1998). At
least 4 species in the genus Amphicoma and the 26 monkey beetle species in
9 genera (Anisochelus, Anisonyx, Heterochelis, Khoina, Lepisia, Lepithix,
Pachynema, Peritichia, and Scelophysa) may be involved in pollinating
the St. Brigid or poppy anemone (Anenome coronaria), orange buttercup
(Ranunculus asiaticus), red tulip (Tulipa agenensis), corn poppy (Papaver
rhoeas), and the more recently marketed peacock moraeas (Moraea), ixias
(Ixia) and romuleas (Romulea). The committee is not aware of any studies
on population trends of pollinating beetles.
Flies (Order Diptera)
The true flies (order Diptera) are among the most diverse of the insects,
with more than 150,000 species described (Thompson, 2006). Flies are
ancientthe oldest fossils are known to have come from the Permian (250
million years ago), and flies might have been the first pollinators (Labandeira, 1998). The group, however, underwent its greatest diversification
along with flowering plants from the late Cretaceous onward. Higher flies
(suborder Cyclorrhapha) are the result of this radiation and now account for
about two-thirds of the extant Diptera (Grimaldi and Engel, 2005). Extant
flies are classified into 153 families and 148,416 species, with 124 families
and 24,219 species found in Canada, Mexico, and the continental United
States (Thompson, 2006).
The state of taxonomic knowledge for higher categories (families and
genera) is summarized in the Manual of Nearctic Diptera (McAlpine et al.,
1981, 1989). The last assessment of the Nearctic Diptera fauna was done in
1988 (Thompson, 1990) and, according to the results, about two-thirds of
all the flies known to occur in America north of Mexico have been named.
Unfortunately, fewer than 1 percent of these flies are treated comprehensively in monographs, and fewer than one-quarter of the species have been
thoroughly revised. No field guides exist exclusively for flies, and only one
digital key has been developed (Carroll et al., 2005). The assessment also
noted a decline in specialists in the ranks of graduate teachers at universities
and among museum curators.
Most higher flies are flower visitors and many have been documented as
pollinators. All of the worlds floristic provinces contain at least one plant
species pollinated primarily or exclusively by flies, and fly pollination is regarded as second only to bee pollination in the evolution of flowering-plant
diversity (reviewed by Larson et al., 2001). Flies as flower visitors (anthophiles) and pollinators have been reviewed by Larson and colleagues (2001).
Following from their work (and table) and combined with the number of

58
species for each group identified as containing pollinators, it is possible to

estimate that 17,460 species in North America are flower visitors and likely
pollinators (Table 2-5).
Some fly species forage actively in cool, wet climates, so fly pollination
could dominate among the flora of the Arctic tundra and the montane-alpine
zones of North America (Kearns, 1990; Kevan, 1972). Research published
within the past 15 years demonstrates that fly pollination dominates in plant
species that are characterized by small flowers that bloom under shade and
in seasonally moist habitats. Cacao (Theobroma cacao, from which chocolate is obtained) is the best-known example (Young, 1994), but others are
in the Iridaceae (Goldblatt et al., 2005) and Saxifragaceae (Goldblatt et al.,
2004).
In association with bees, flies appear to contribute to the pollination of
several fruit and vegetable crops (Free, 1970), but cacao is the only domesticated plant of major economic significance pollinated exclusively by flies
(tropical midges). Cacao is a tropical shrub that cannot be grown in Canada
or in most of the United States, but it has been commercially and culturally
important to Mexico since the days of the Aztec Empire (Young, 1994).
The dominant pollinators of beargrass (Xerophyllum tenax), a montane
herb native to the American Pacific Northwest, consist of more than 20
species of flower fly. Licensed collection of beargrass leaves occurs annually
for exportation to Europe for the floral craft trade. Harvesters in the Pacific
Northwest were paid over $11.5 million for beargrass in 1989 (Schlosser
et al., 1991). A number of garden and potted plants are derived from flypollinated species, including birthwort (Aristolochia), starfish flower (Stapelia), tuberous aroids including the jack-in-the-pulpits (Araceae), and the
ancestors of some hybrid gladioli (Gladiolus; Bernhardt and Thien, 1987;
Goldblatt and Manning, 1999; Proctor et al., 1996). No flies have been truly
managed, but some flower flies (Syrphidae, genera Eristalis, Syritta; Jarlan
et al., 1997) have been used to pollinate crops in greenhouses.
Knowledge of the distribution and population sizes of North American
flies is virtually nonexistent. Although the few published monographs and
revisions usually contain summary statements of material examined and,
frequently, distribution maps, there are no publicly available databases
of substantive specimen data. Similarly, there could be just one long-term
program to collect population data for flies, using a Malaise trap at the
Rocky Mountain Biological Laboratory in Crested Butte, Colorado. In Europe, however, some groups of flies are actively studied by citizen-scientists.
Flower flies (Syrphidae) are very popular with citizen-scientists; syrphids,
for example, have been included in the ALARM project (Box 2-2 and
Chapter 6).
Population trends cannot be determined without population data
for North American flies, although in Europe the ALARM project has

59
TABLE 2-5 Total Number of Identified Diptera Species and the

Estimated Number of Diptera Species That Are Pollinators
Taxon
Number of
Species
Estimated
Number of
Canada,
Level of
Mexico, or U.S. Taxonomic
Pollinators
Knowledge
Syrphidae
Bombyliidae
Culicidae
Bibionidae
Cecidomyiidae
Ceratopogonidae
Psychodidae
Chironomidae
Tabanidae
Rhagionidae
Athericidae
Stratiomyidae
Asilidae
Apioceridae
Therevidae
Mydidae
Acroceridae
Nemestrinidae
Empididae
Dolichopodidae
Phoridae
Drosophilidae
Lauxaniidae
Chloropidae
Scathophagidae
Anthomyiidae
Muscidae
Fanniidae
Sarcophagidae
Calliphoridae
Tachinidae
Bolitophilidae
Diadocidiidae
Ditomyiidae
Keroplatidae
Lygistorrhinidae
Mycetophilidae
Rangomaramidae
Sciaridae
5872
5009
3517
743
5831
5525
2801
6722
4295
676
120
2669
7166
165
1057
452
395
255
4839
6742
3655
3863
1844
2841
291
1887
4932
295
3015
1487
9470
54
25
78
837
27
3891
5
2093
1001
1095
289
111
1250
671
172
1126
472
118
6
469
1286
89
167
90
68
10
903
1459
443
321
172
320
153
709
774
119
484
124
2005
20
3
9
88
1
685
0
178
Level of
Ecological
Knowledge
Medium
Medium
High
Medium
Medium
Medium
Low
Low
High
Medium
Medium
Medium
Medium
High
High
High
High
High
Medium
Medium
Low
High
Low
Low
Medium
High
Medium
High
Medium
Medium
Low
Medium
Medium
High
Medium
High
Medium
Medium
Low
High
Low
Medium
Medium
Low
Medium
High
Medium
Medium
Medium
Medium
High
High
High
High
High
Medium
Medium
Low
High
Low
Low
Medium
High
Medium
High
Medium
Medium
Low
Low
Low
Low
Low
Low
Low
Medium
Low
NOTE: Documented population trends are not available for all taxa except for Syrphidae.

60
documented shifts and declines for several flower fly species in the United
Kingdom and the Netherlands (Box 2-3; Biesmeijer et al., 2006). One
North American species, the Delhi Sands flower-loving fly (Rhaphiomidas
terminatus abdominalis; Kingsley, 1996), has been placed on the U.S. Endangered Species List.
Butterflies and Moths (Order Lepidoptera)
With approximately 150,000 species described worldwide (Grimaldi
and Engel, 2005), Lepidoptera are among the most species-rich orders of
insects, as measured by formally described and documented species. The
Lepidoptera include many of the most easily recognized insects, and they
are relevant to understanding pollination systems and their origins.
As with most herbivorous insects, butterflies and moths interact with
plants during both larval and adult stages, the latter of which are those usually involved in pollination. Although some of the best-studied examples of
plant-insect mutualisms involve moths and butterflies (Heliconius butterfly,
Boggs et al., 1981; Estrada and Jiggins, 2002; yucca moth, Pellmyr et al.,
1996; Powell, 1992), obligatory mutualisms are exceptional in Lepidoptera.
Although many flowering plants rely primarily on butterflies or moths, most
Lepidoptera visit a wide variety of nectar sources. Although lepidopteran
pollinators largely are generalists and often transfer only small amounts
of pollen, they tend to move longer distances to visit flowers of the same
species than do other pollinating insects, such as bees, and thus are important in maintaining gene flow within and among populations (Herrera,
1987, 2000).
The earliest documented North American extinctions of insects involved
Lepidoptera (the xerces blue, Glaucopsyche xerces), and the Lepidoptera
were the bellwethers of the earliest observations of invertebrate species
decline in North America (Tilden, 1956). At least some of these extinctions
occurred before any information on pollinating capacity of these butterflies
was obtained. Butterflies and moths account for a high number of species
currently regarded as threatened or endangered in various North American
regions and tracked by various state heritage programs (http://www.natureserve.org). Numerous butterfly species are protected under the terms of the
Endangered Species Act (Chapter 1) and by state legislation.
Massachusetts, for example, lists 48 Lepidoptera speciesnearly half
of the invertebrates on its listas endangered, threatened, or of special
concern under MESA (http://www.mass.gov/dfwele/dfw/nhesp/nhrare.htm).
Most, if not all, of those butterflies and moths have declined significantly in
the past 100 years. MESA also lists 10 beetles, 31 dragonflies and damselflies, 8 crustaceans, 7 mussels, 7 snails, and 4 other invertebrates. The large
proportion of Lepidoptera listed could be more a reflection of the generally

61
greater knowledge about them than their larger propensity toward decline
(May et al., 1996). Although threatened species legislation varies from state
to state, similar trends are widely recognized by scientific and academic
communities.
Butterflies
Butterflies and moths often have precise habitat and life history requirements. As is the case for most herbivorous insects, the majority of Lepidoptera generally specialize on three or fewer host plant families for larvae
(Bernays and Graham 1988; Farrell and Mitter, 1993; Mitter and Farrell,
1993; Powell et al., 1998). Yet there are significant information gaps about
the extent to which plantseconomically important and otherwiserely
exclusively on particular lepidopteran species for pollination. Although
butterfly larvae tend to be host-specific for food, their activities as adult
pollinators are likely to be general. There are notable exceptions; the wild
carnation Dianthus carthusianorum in Europe, for example, appears to be
specialized for butterfly pollination and is visited by five butterfly species,
of which two, due to visitation frequency, are principal pollinators (Bloch
et al., 2006).
The bay checkerspot butterfly, Euphydryas editha bayensis (Nymphalidae), pollinates native plants in North America. Variation in population
size of this butterfly has been meticulously documented. It has been the
focus of regular census efforts in the Jasper Ridge Biological Preserve near
Palo Alto, California, for more than 40 years (Ehrlich and Hanski, 2004),
and local population extinctions have been documented for 1991 and
1998 (McLaughlin et al., 2002). Although it is known from other localities
(there is a large population in Morgan Hills and a small population near
Redwood City), the bay checkerspot was designated as threatened in 1987
and included on the Federal Endangered Species List. It was almost certainly
more extensively distributed before the invasion of its habitat by Eurasian
grasses (McLaughlin et al., 2002). Local population extinctions of the sort
observed for the bay checkerspot have also been documented in the Rhone
Valley of Switzerland for Satyrus ferulae, which has disappeared from 31
of 62 sites, and Melanargia galathea, which has disappeared from 29 of 67
sites, since 1970 (Bloch et al., 2006).
The monarch butterfly, Danaus plexippus, pollinates many milkweed
and other plant species. It has been the subject of intense interest, in part because of its dramatic ecology (sequestering cardenolides from asclepiaceous
host plants and serving as the central model in an extensive mimicry system)
and migratory behavior (Halpern, 2001). The Fourth of July butterfly count
(known as 4JC in short), an annual monitoring effort undertaken by a broad
cross-section of amateurs and professionals, provides insight about fluctua-

62
tions in monarch populations (Swengel, 1990). Swengel (1995) described

population fluctuations.
From 1977 to 1986, the mean number of monarchs per hour in eastern North
America varied significantly in only one of nine pairs of consecutive years. From
1986 to 1994, eastern monarchs varied significantly in five of eight year-pairs,
with a nearly equal number of increases and decreases. However, the amount
of variation within each year-pair was similar for 19771986 and 19861994
(median difference ca. a factor of 2). Although the Atlantic and midwestern
subregions of the eastern population covaried in four of eight year-pairs from
19861994, differences between the two subregions sometimes damped fluctuations in the eastern population overall. Data from independent transect surveys
in Wisconsin for 19901994 agreed with the direction of fluctuations in Wisconsin 4JCs. In 4JCs from 19871994 in the Pacific coastal states, monarchs
varied less than the eastern population, with a significant increase in 1989 and
significant decrease in 1988. However, a nonsignificant decline of an order of
magnitude occurred in 1993, and a considerable but smaller increase occurred
in 1994. Fluctuations in monarch abundance in eastern North America during 19771994 often, but not always, coincided with years affected by major
widespread perturbations of typical weather such as the El Nino-Southern
Oscillation, major volcanic eruptions, droughts and floods.
Since Swengels study, other groups have collected data on monarch populations in various locations, and they also have reported fluctuating numbers
from year to year (Gibbs et al., 2006; O. Taylor, University of Kansas,
presentation to the committee, October 18, 2005).
Results from another Fourth of July Butterfly Count, carried out since
1977 by Arthur M. Shapiro (University of California, Davis), provide
information about the variations in populations of 36 butterfly species in
the Sacramento Valley. During the 29-year study, 39,614 butterflies were
counted; the number of species observed each year ranged from 17 to 30 and
the number of inviduals from 618 to 2613. The site is a partly channelized
perennial stream, its floodplain, and adjacent levees, and it is surrounded
by agricultural lands. The results from Shapiros annual census have been
used in a recent analysis (OBrien et al., in review) to investigate the usefulness of different statistical methods for identifying trends in overall species
diversity and in the probability of the presence of individual species. Species
diversity declined 38 percent over the study period. Although the decline
was detectable by the 13th year, it did not become statistically significant
until the 23rd year of the study. Of the 23 species analyzed, 8 have declined
significantly and 11 more show a negative (statistically nonsignificant)
trend. Neither abundance nor diversity was significantly correlated with
any weather patterns examined, although the weather at the study site has
warmed significantly over the past 30 years. Thus, the cause of the decline

63
is still unknown, but species that overwinter as eggs or larvae were more
likely to decline than those that overwinter as pupae or adults. Most of
the species reported as declining also are declining regionally. The results
published by OBrien and colleagues (in review) point out the importance
of systematic, long-term monitoring. Because of statistical limitations, the
dramatic decline in species numbers reported in the study would have gone
undocumented in a census that lasted less than 22 years.
Moths
Moths are underappreciated as pollinators because most of their pollinating activity takes place at night. They are known to pollinate a diverse suite of plants, ranging from cacti (Clark-Tapia and Molina-Freaner,
2004) to orchids (Little et al., 2005) to trees (Lin and Bernardello, 1999).
Some moth species have specialized morphological features, such as long
proboscides, and behavior that make them excellent pollinators of some
plants (Barth, 1985; Proctor et al., 1996). Some plants, such as various
species of Yucca (Thompson, 1994), are icons of specialized pollination
biology. Yucca moths (Tegeticula and Pronuba spp.) are highly specialized pollinators of Yucca spp. within desert and chaparral habitats of the
United States and Mexico. The adult yucca moth does not feed, but it uses
specially modified palps (tentacles) to gather up a ball of pollen that it
places on a receptive floral stigma, ensuring the production of the seeds
that larvae eat (Bogler et al., 1995; Faegri and van der Pijl, 1979; Pellmyr
et al., 1996; Proctor et al., 1996). Similarly, Gaura and Calylophus species
(Clinebell et al., 2004) and the senita cactus (Pachycereus schottii; Fleming
and Holland, 1998) are in plant-specific moth pollinator systems that have
been intensively studied.
Although a variety of moths are known to be pollinators, the families
Geometridae (geometer moths), Noctuidae (owlet moths), and Sphingidae
(sphinx moths) are among the best studied. The Sphingidae (Gregory, 1963
1964) and the highly diverse Noctuidae are among the most efficient of the
lepidopteran pollinators. Within the deserts of the southwestern United
States and Mexico, large fast-flying hawkmoths or sphingids (Sphingidae)
are coadapted pollinators of night-blooming Datura spp. (Solanaceae)
and night-blooming cacti in the genus Peniocereus (Raguso et al., 2003).
At least 106 species in the temperate North American flora are known to
be visited by sphinx moths, including many from the Onagraceae (Grant,
1985). Migratory noctuids feed on the floral nectar of many species of plants
(Kevan and Kendall, 1997). Geometrids have been recorded as pollinators
of orchids (Thien and Utech, 1970) among other species. There are no data
on population trends of moth species.

64
Thrips (Order Thysanoptera)

The thrips (Thysanoptera) are slender, small insects (generally no more
than one millimeter long), arranged into nine families of living species distributed worldwide, largely in the tropics and temperate regions, with a few
species in Arctic regions (Lewis, 1997; Mound, 1997). Checklists of adult
thrips have been produced by Stannard (1957, 1968) for North America.
Thrips feed on a variety of plant tissues, including pollen, fungal mycelia, and spores, and they also are predatory (Grimaldi and Engel, 2005;
Kirk, 1993, 1997). When they feed on pollen, thrips puncture the coat and
drain the grains (Kirk, 1984, 1985, 1997). Grimaldi and Engel (2005) note
that pollen feeding evolved several times in thrips; they are so numerous on
flowers that they can be effective pollinators of a wide variety of plants in
nature and agriculture (Ananthakrishnan, 1993; Endress, 1994; Kirk, 1988;
Lewis, 1973, 1997; Terry, 1997). Generally, however, they are regarded
as minor or secondary pollinators (Kirk, 1997; Lewis, 1973, 1997; Terry,
2001).
As minor pollinators, thrips also pollinate such agricultural plants as
beets, beans, onions, and cacao (Kirk, 1997; Lewis, 1973). Although thrips
can pollinate plants in the absence of other pollinators, their importance in
open-pollinated crops depends on whether other insects pollinate the flowers first (Kirk, 1997). Thrips can enter unopened buds (Mackie and Smith,
1935), but the peak number of thrips can occur after peak visits by other
insects (Kirk, 1984). The grooming behavior of thrips contributes to both
self- and cross-pollination in plants (Kirk, 1997). As thrips arrange the
fringe hairs before and after flight, pollen grains are shed from their bodies
(Kirk, 1997). The stigma is prominent in many flowers and because it is used
by thrips for take-off and landing, the pollinator thus places pollen directly
on the stigma (Kirk, 1997).
Populations of thrips on crops grown in greenhouses and shade houses
depend on breeding within the crop (Kirk, 1997). For example, young
chrysanthemum plants are rooted from older plants, and when adult female
Frankliniella occidentalis (western flower thrips) oviposit in apical leaves,
growers can inadvertently raise their own pest populations and transport
them to other sites in the cuttings (Kirk, 1997). The flower trade is responsible for the worldwide distribution of that thrips species, as well as others
(Table 6.2 of Kirk, 1997).
In part because of their size and their more frequent role as herbivorous
plant pests and disease vectors (Ullman et al. 1997), North American thrips
have not generally been the focus of concern about population decline; no
thrips species is currently protected under the provisions of the Endangered
Species Act (ESA). Because of restrictions on ESA, it is unlikely that any
species that has had an adverse economic impact on a crop species would

65
be eligible for listing, even if it could be shown that thrips provide essential
pollination services (Chapter 6).
Mammalian Pollinators
Bats
Estimates of the number of bat-pollinated plants species in the Americas range from 600 (Neuweiler, 2000) to 1,000 species (Winter and von
Helversen, 2001). Most bat-pollinated flowers have intense scents that are
different from those pollinated by other animals (von Helversen and Winter,
2003). Sulphur-based compounds are more common in bat-pollinated species than they are in other pollination systems (von Helversen et al., 2000).
Given that the scents are produced in many phylogenetically unrelated species of plants, they are likely the result of long coevolutionary associations
(Knudsen et al., 1993).
The color of bat-pollinated flowers is normally inconspicuous, from
whitish to green or brown. The color reflectance of the flower itself probably would not be a strong attractant for bats, because most bats are
considered color-blind (Jacobs, 1992), although some species might see
some color (von Helversen and Winter, 2003). Ultraviolet clues in several
bat-pollinated flowers (notably on columnar cacti) prompted studies of bats
ability to detect ultraviolet radiation. Von Helversen and Winter (2003)
reported that Glossophaga soricina is highly sensitive to ultraviolet light.
Other characteristics of bat-pollinated flowers include an outward-facing
position at the edge or away from the plants foliage, thereby facilitating the
bats access. Most bat-pollinated flowers are large, with sturdy petals and
exposed stamens and pistil. They generally open at night, and many open
only for a single night. The protein content in the nectar of bat-pollinated
flowers is greater than it is in flowers pollinated by insects, and those plants
generally have more nectar (Neuweiler, 2000). Plant families recognized
for their many bat-pollinated species include Agavaceae, Bignoniaceae,
Bombacaceae, Cactaceae, Caesalpiniaceae, Chrysobalanaceae, Convolvulaceae, Cucurbitaceae, Fabaceae, Malvaceae, Marcgraviaceae, Mimosaceae,
Musaceae, Pandanaceae, and Tiliaceae (Neuweiler, 2000), although as many
as 27 plant families in the New World have bat-pollinated species (Vogel,
1969). Most of those groups are tropical, and the number of bat-pollinated
species increases as latitude decreases (Heithaus, 1982; von Helversen and
Winter, 2003).
There are at least 12 species of pollinating bats in North America,
including southern Mexico (Baker et al., 2003; Ceballos et al., 1997;
Medelln et al., 1997). The most prominently recognizedby virtue of
their conservation statusare the three long-distance migratory species: the

66
lesser long-nosed bat (Leptonycteris curasoae), the Mexican long-nosed bat

(L. nivalis), and the hog-nosed bat (Choeronycteris mexicana). Few population data are available for pollinating bats in North America, given that
populations are difficult to survey, few people are qualified to survey them,
and few people study them. Most population data take the form of isolated
reports that indicate local trends in abundance rather than precise estimates
of population size. Information on both species of Leptonycteris (Ceballos et
al., 1997; Fleming, 2004; Fleming and Nassar, 2002; Fleming et al., 2001a;
Galindo et al., 2004; Moreno-Valdez et al., 2004; Stoner et al., 2003) covers
regions of western, northwestern, and central Mexico and the researchers
have presented data on population dynamics that cover only relatively short
periods. An effort to monitor and assess the status of L. curasoae is being
centralized by the Arizona Game and Fish Department (http://www.azgfd.
gov/w_c/edits/documents/Leptcuye.fi.pdf), and the Program for Conservation of Mexican Bats has been compiling information on this and other
species for several years (Medelln, 2003; Medelln et al., 2004).
Pollinating bats can be divided into two behaviorally functional groups:
species restricted to the tropical regions of southern Mexico (Glossophaga,
Hylonycteris, Choeroniscus, Anoura, Lichonycteris, Musonycteris) and
those that migrate, moving from central and southern Mexico to northern
Mexico and the southern United States (Ceballos and Oliva, 2005; Reid,
1997). All pollinating bats provide important services for many species of
North American plants. Many species of columnar cacti, species of Agave,
trees in the family Bombacaceae, and many other plants rely heavily on
bats to carry out sexual reproduction. Agaves are economically important
throughout Mexico, but particularly in western regions where they are
used for the production of tequila. Tequila production does not, however,
depend on pollination by bats. By virtue of their common asexual mode of
reproduction, agaves are planted from shoots associated with adult plants,
and their flowering is prevented by premature harvest. Nevertheless, bats
could be necessary to promote genetic diversity for the long-term viability
of commercially grown agaves (Arizaga et al., 2002; Dalton, 2005; Rocha
et al., 2005; Valenzuela-Zapata and Nabhan, 2004).
Some other economically important plants linked to bat pollination
are the balsa tree (Bombacaceae: Ochroma pyramidale), ceiba (Ceiba
pentandra), and many columnar cacti whose fruits are used and commercialized fresh or dried, or processed into jams, jellies, and candies
(Neobuxbaumia spp., Pachycereus spp., and others) (Bawa, 1990; Watson
and Dallwitz, 1992). Ecologically important plants, such as the cardon
(Pachycereus pringlei), saguaro (Carnegiea gigantea), and other columnar
cacti, vary in their reliance on bats (Fleming et al., 2001b; Grant and Grant,
1979; Valiente-Banuet et al., 1996). Some populations of these cacti are frequently pollinated by white-winged doves (Zenaida asiatica), several species

67
of hummingbirds, sphingid moths, bees, or beetles (Fleming et al., 2001b;

Grant and Grant, 1979; Valiente-Banuet et al., 1996) on the day after their
nocturnal anther dehiscence.
The genus Glossophaga has four North American species, all present in
tropical Mexico. Three of them have wider distribution, extending into Central and South America, and one, G. morenoi, is endemic to the dry tropical
forest of western Mexico. Two species, G. commissarissi and G. soricina,
are widespread and common and do not seem to face any threat; the other
two tend to be locally rare (Ceballos and Oliva, 2005; Reid, 1997). No
population estimates or trends have been obtained, but neither is considered
to be facing conservation threats by the Mexican government and neither
appears on the International Union for the Conservation of Nature and
Natural Resources/The World Conservation Union Red List of threatened
species (http://www.iucnredlist.org/).
Leptonycteris curasoae and L. nivalis are migratory species considered
threatened in Mexico and endangered in the United States. Their listing in
the United States was prompted by surveys in some known roosts that indicated severe declines (U.S. Fish and Wildlife Service, 1988, 1994; Wilson
et al., 1985), although subsequent studies suggested that the declines might
not have been as severe as originally thought (Cockrum and Petryszyn,
1991). In Mexico, the species was listed as threatened when some winter
maternity roosts (the species has a summer and a winter reproductive pulse)
were found severely depleted; much of its original habitat in western and
central Mexico has been destroyed for tourism and agricultural development (SEMARNAT, 2002). The Program for Conservation of Mexican Bats
has monitored between 7 and 20 roosts per year, documenting population
stability or growth, and noting temporary declines in some years (Medelln,
2003; Medelln et al., 2004).
Another migratory species listed as threatened in Mexico, but not in the
United States, is the hog-nosed bat, Choeronycteris mexicana (SEMARNAT,
2002). Although there are no reliable population estimates, since 1906,
fewer than 1,500 individuals have been documented throughout the species
range (Cryan and Bogan, 2003). In contrast with the long-nosed bats, this
species roosts in small numbers, typically about 12 bats per roost. Because
roosts tend to be scattered widely over landscapes, surveys are difficult
(Arroyo-Cabrales et al., 1987; Cryan and Bogan, 2003; Tuttle, 2000).
Two of the four North American Glossophaga species are very abundant (Ceballos and Oliva, 2005; Reid, 1997), and there is no evidence of
decline. Although the one species endemic to Mexico appears to be less
common, there are no population estimates that permit a firm assessment
of status.
The banana bat (Musonycteris harrisoni), a rare species that appears to
be highly specialized, as evidenced by its extremely long snout and tongue,

68
is endemic to western Mexico, from Jalisco to Oaxaca. Fewer than 70 individuals have ever been observed, and only 3 roosts with 3 individuals or
fewer have been reported (Tllez and Ortega, 1999). The species is considered threatened by the Mexican federal government (SEMARNAT, 2002).
The tailless bat (Anoura geoffroyi) is widespread in the southern half of
Mexico and occurs frequently at medium elevations1,0002,500 m above
sea leveland also, rarely, at lower elevations. Although this species is not
very common, it is not thought to be facing any threats (Ceballos and Oliva,
2005; Reid, 1997). No population estimates are available.
Three well-recognized pollinator species, Hylonycteris underwoodi,
Choeroniscus godmani, and Lichonycteris obscura, tend to be rare. The
former two have a wide distribution over the southern half of Mexico; the
third is known only from the state of Chiapas south to South America. No
population estimates or trends are detectable through peer-reviewed literature. The three species are associated with primary tropical forests, both
dry and wet (Ceballos and Oliva, 2005; Reid, 1997), and none is on the
Mexican list of species at risk of extinction.
Three migratory bat species are considered threatened or endangered by
the Mexican (SEMARNAT, 2002) and U.S. (U.S. Fish and Wildlife Service,
1988) federal governments. Conservation and recovery programs have been
initiated and the bat populations are being monitored; surveys in recent
years in several colonies suggest that the populations of at least two (L.
nivalis and L. curasoae) of these three species in the genus Leptonycteris
are stable. However, taking those species off the threatened or endangered
species list may be premature. More local evidence is required before a firm
conclusion can be drawn (Medelln, 2003; Medelln et al., 2004). Other
pollinating bats might not be in decline, but those associated with primary
habitats have long been considered rare, and their biology and importance
are virtually unknown.
Nonflying Mammalian Pollinators
Among nonflying mammals, at least two species of opossum (Caluromys derbianus and Didelphis marsupialis; Tschapka and von Helversen,
1999) visit the flowers of Marcgravia in Central America. Coatis (Nasua
nasua; Mora et al., 1999) and kinkajous (Potos flavus; Kays, 1999) have
been documented as consistent flower visitors and potential or realized
pollinators of various trees, including Ochroma, Pseudobombax, Tetrathylacium, and others. Janson et al. (1981) suggested that several primates
(including the spider monkey, Ateles), opossums, and procyonids could be
pollinators of several tree species in the rainforests, although at least the spider monkey has been shown to damage virtually all flowers it visits, apparently substantially decreasing fruit set (Riba-Hernandez and Stoner, 2005).

69
These mammals habitats span southern Mexico to central Mexico and

from the northern coatis range to southwestern United States. Opossums
can also be found in southern Canada. The woolly opossum (Caluromys
derbianus) is considered under special protection, and two of its subspecies
are considered endangered. An endemic species of coati is threatened, and
the kinkajou is under special protection (SEMARNAT, 2002). Pollination
by nonflying mammals is reported more often for other continents (Carthew
and Goldingay 1997; Goldingay et al. 1991).
Avian Pollinators
Pollination by birds is well known and recognized in North America,
largely because of hummingbirds (Faegri and van der Pijl, 1966). Population
data for avian pollinators are available from a variety of sources, including
the North American Breeding Bird Survey (BBS) (see http://www.mbr-pwrc.
usgs.gov/bbs/genintro.html for a history of this effort), which is now coordinated through the U.S. Geological Survey (USGS) Patuxent Wildlife
Research Center. Bird banding data collected by individuals or at bird banding stations are compiled by the North American Bird Banding Laboratory,
(http://www.pwrc.usgs.gov/bbl/) which also is part of the Patuxent Wildlife
Research Center. Some summary BBS statistics are available from a USGS
website (Sauer et al., 2005); some results are presented here. Cautious interpretation is necessary, however, because at least for hummingbirds, the
BBS methodology is less than ideal.
Hummingbirds
Eighteen hummingbird species are known in the United States, 9 are
known from Canada (although some of these are rare visitors from Mexico;
Sibley, 2000), and 63 are known from Mexico. Most hummingbirds do not
sing (even though they vocalize in aggressive interactions), so they can be
more difficult to detect. Males and females can occupy different habitats,
and males are polygynousthat is, they mate with more than one female
in a breeding season.
Although a few species overwinter in the United States, most migrate
southward, depending on migration corridors or nectar corridors (Nabhan
et al., 2004). It can be difficult to assess hummingbird populations because
some surveys (such as the Christmas Bird Counts) are conducted when
individuals might have left for wintering grounds. There is evidence that
a high percentage of rufous hummingbirds (Selasphorus rufus) lose body
weight during migration, requiring longer stopover times if floral resources
are scarce (Russell et al., 1994).
The relationship between hummingbirds and the flowers they visit

70
is well studied (Arizmendi and Ornelas, 1990; Calder, 2004; Grant and
Grant, 1967), and hummingbirds are important pollinators in much of
North America. Although hummingbirds visit a wide variety of flowers,
many hummingbird-pollinated flowers share some general characteristics. The flowers tend to be tubular, brightly colored (red, orange, bright
yellow), and relatively odorless, and their nectar is often more diluted than
that of bee-pollinated flowers (Baker, 1975; Pyke and Waser, 1981) but
could contain higher levels of sucrose (Baker et al., 1998). Hummingbirds
display variation in bill shape and length (Stiles and Skutch, 1989), and
some studies indicate that all hummingbirds can extract nectar from longtubed, wide-opening flowers, but that only long-billed hummingbirds do
so from long-tubed, narrow-opening flowers (Temeles et al., 2002). The
list of species of plants that are visited and pollinated by hummingbirds is
extensive (Bertin, 1982; Grant and Grant, 1968), and it encompasses plants
in many families: Acanthaceae, Asteraceae, Bromeliaceae, Campanulaceae,
Ericaceae, Fabaceae, Gentianaceae, Heliconiaceae, Loranthaceae, Malvaceae,
Onagraceae, Polemoniaceae, Rubiaceae, Zingiberaceae, and many others
(Knudsen et al., 2004; McDade and Weeks, 2004).
Although hummingbirds might be minor as pollinators of agricultural
crops (cacti; Griffith, 2004), many species of wildflowers have coevolved
with hummingbirds and exhibit morphological, phenological, or other traits
that facilitate interaction (Fenster et al., 2004). Data from BBS with a high
credibility index (at least 14 samples in the long term, of moderate precision,
and of moderate abundance on routes) are available for 8 hummingbird species. Data cited below come from the BBS website (http://www.mbr-pwrc.
usgs.gov/bbs/bbs.html).
In the states where the credibility index is high (such as North Carolina, Oklahoma, and West Virginia), the trend (percentage change per year)
shown for the ruby-throated hummingbird (Archilochus colubris) from
1966 to 2005 is positive. Overall, trends in the United States (2.5 percent per
year) and Canada (2.5 percent per year) are positive (http://www.mbr-pwrc.
usgs.gov/cgi-bin/atlasa99.pl?04280&1&05). For the black-chinned hummingbird (Archilochus alexandri), for one site (Edwards Plateau) for
which the credibility index is high, the trend from 1966 to 2005 is positive
(1.2 percent per year). Overall, the trend for A. alexandri is positive in the
United States (1.6 percent per year), and negative in Canada (3.2 percent
per year). For Annas hummingbird (Calypte anna), in the states where the
credibility index is high, the trend from 1966 to 2005 is positive; the data
set includes California, a state with a few regionsCalifornia, Southern
California grasslands, foothills, and Fish and Wildlife Service Region 1.
Overall, the trend is positive (1.2 percent per year) in the United States.
For the broad-tailed hummingbird (Selasphorus platycercus), in the states
where the credibility index is high, the trend from 1966 to 2005 is mixed;

71
it is slightly negative in Colorado and slightly positive in New Mexico.

Overall, the trend is slightly negative (0.2 percent per year) in the United
States. Calder et al. (1983) reported that, over a 10-year period at the Rocky
Mountain Biological Laboratory, the population of S. platycercus appeared
to be declining, although nest counts of breeding females remained fairly
constant. In the years since that study, the population has remained variable, but with no discernable long-term trend (D. Inouye, University of
Maryland, and Rocky Mountain Biological Laboratory, Colorado, personal
observation). For the rufous hummingbird (Selasphorus rufus), in Oregon
and Washington, the two states where the credibility index is high, the trend
from 1966 to 2005 is negative. Overall, trends in the United States (2.0
percent per year) and Canada (2.1 percent per year) are negative. An interesting development over the past decade is that rufous hummingbirds are
commonly found in the eastern United States, where they previously were
thought to be absent.
The status of several species, because of a lack of information, is more
difficult to determine. For the Costa hummingbird (Calypte costae), there
are no states where the credibility index is high, but the trend from 1966 to
2005 is positive for one state with a few regionsthe Great Basin deserts
and Mexican highlands. Overall, the trend is positive (0.5 percent per
year) in the United States. Similarly, for the calliope hummingbird (Stellula
calliope), there are no states where the credibility index is high, but the
trend from 1966 to 2005 is positive in Idaho and Wyoming and negative in
California, Montana, Oregon, and Washington. Overall, the trend is negative (0.9 percent per year) for the United States and slightly positive (0.8
percent per year) for Canada. There is no statistically significant detectable
trend. Finally, for the Allen hummingbird (Selasphorus sasin) there are no
states with a high credibility index, but in the southern Pacific rainforest
regionthe only region with a high indexthe trend from 1966 to 2005
is negative (1.2 percent per year) but edging upward over the past several
years. Overall, the trend for S. sasin in the United States is negative (2.0
percent per year). This species is on the Audubon Society Watch List because
of its very restricted range in the United States. There are two subspecies,
identified primarily through their distribution (mainland or the Channel
Islands off the coast of Southern California), and although the subspecies
with the wider range (coastal Mexico to Oregon) appears to be in decline,
the other appears to be spreading.
Unfortunately, there do not appear to be any long-term data about
population trends of species of hummingbirds that are distributed in Mexico
exclusively. Although these species could be under pressure from habitat
alteration and fragmentation, there is no equivalent of the BBS data and no
systematic banding efforts that the committee could discover.

72
Nonhummingbird Avian Pollinators

Although not typically thought of as pollinators, at least one dove
species, the white-winged dove (Zenaida asiatica), is an important pollinator of saguaro and possibly other cacti (Fleming, 2000). The population
trend for that species is slightly negative from 1966 to 2005 in Arizona,
the Sonoran Desert, and the Mexican highlands. Overall, in the United
States and in the survey area, the trend is positive (1.6 percent per year).
A few other nonhummingbird avian species also pollinate North American
plants, and there is evidence that they also affect flower morphology. The
genus Erythrina (Fabaceae), a pantropical leguminous small tree, shows
two distinct flower and nectar types: hummingbird-pollinated species have
upright inflorescences with tubular, radially arranged flowers and nectar
that has relatively high concentrations of sugar. The species pollinated by
passerine birds (including swallows) have horizontal inflorescences held
upright, with the flowers arranged radially along the axis, the narrow
standard petal folded to form a pseudotube, and relatively dilute nectar
(Bruneau, 1997). Several species have been identified: verdins (pollinating
ocotillo, Fouquieria splendens; Waser, 1979), oriole (Icterus spp.: Etcheverry
and Aleman, 2005; Toledo and Hernandez, 1979), parrot (Aratinga),
woodpecker (Centurus), tityra (Tityra), warbler (Dendroica), wren (Campylorhyncus), jay (Psilorhinus), vireo (Vireo), blackbird (Dives), grackle
(Cassidix), oropensola (Psarocolius), honeycreeper (Cyanerpes), tanager
(Thraupis, Piranga), euphonia (Euphonia), mockingbird (Mimus), thrasher
(Toxostoma), and finch (Carpodacus) visit flowers of a diverse array of species including Bernoullia, Ceiba, Tabebuia, Spathodea, and Agave (Ornelas
et al., 2002; Toledo, 1977).
Some bird species of these genera are on the Mexican federal list of endangered species: six vireo species are under special protection, two species
are threatened, and one is endangered. Three orioles and two oropendolas
are under special protection; two parrots of the genus Aratinga are under
special protection, two more are threatened, and one subspecies of one
threatened species is considered endangered. Two species of warbler are
threatened, and one wren species is under special protection, one is threatened, and one is endangered. Two euphonias are under special protection,
one thrasher is endangered, and two subspecies of finch are endangered
(SEMARNAT, 2002).
Information Needs
As the number of individual hummingbird banders in the United States
has grown, so has the amount of information about the birds abundance
and migration paths. Additional data might have been collected at some

73
long-term bird banding stations or by long-term individual banders that

could add to the incomplete data for hummingbirds. Long-term monitoring
of bird-pollinated plants also could provide useful information on the stability of the ecosystem services they provide, particularly if plants pollinated
solely by the birds are chosen.
CONCLUSIONS
Despite the paucity of long-term data, collectively there is reliable evidence that some North American pollinator species have become extinct or
locally extirpated, or have exhibited decreases in population size (Table 2-6).
At least two bumble bee species could face imminent extinction, and several
other pollinators have declined significantly (honey bees and U.S. and Mexi-
TABLE 2-6 Illustrative Examples of Pollinators in North America for

Which Evidence of Decline Is Available
Common Name
Species Name
Location
Species for Which Quantitative Data Are Available

Honey bee
Honey bee
Franklins bumble bee
Western bumble bee
Bumble bee
Bay checkerspot butterfly
Long-nosed bat
Long-nosed bat
Rufous hummingbird
Allens hummingbird
Hymenoptera
Apis mellifera
A. mellifera
Bombus franklini
B. occidentalis
B. affinis
Lepidoptera
Euphydryas editha bayensis
Chiroptera
Leptonycteris curasoae
L. nivalis
Apodiformes
Selasphorus rufus
S. sasin
United States
Mexico
Pacific Northwest of the
United States
Central California
New York
Palo Alto, California and
other localities
United States and Mexico
United States and Mexico
United States and Canada
United States
Species for Which Quantitative Data Are Not Available

Stingless bees
Pollen wasps
Pollen wasps
Hog-nosed bat
Banana bat
Hymenoptera
Melipona spp.
Trigona spp.
Pseudomasaris micheneri
P. macswaini
Chiroptera
Choeronycteris mexicana
Musonycteris harrisoni
Southern Mexico
Inyo County, California
Mexico
Mexico

74
can pollinating bats), although many have populations that are stable or
perhaps even increasing, as are a few of the hummingbird species. It should
be noted that there is no evidence of population decline for some species
merely because their populations have not been monitored over time. Overall, whether there is a pollinator crisis is difficult to ascertain inasmuch
as there is no definition of crisis that is universally accepted; however, if
decline is defined as a systematic decrease in population size over time,
then there is evidence that some pollinators in North America representing
a diversity of taxa are, in fact, in decline. It is accordingly important to ascertain the causes and the consequences of those declines as a step toward
informed decision making about action to be taken and what would most
likely ensure successful reversal.

3
Causes of Pollinator Declines
and Potential Threats
It is difficult to determine whether North American pollinator species

are declining, and no less challenging is determining the causes of putative
declines or local extirpations. Many explanations have been invoked to account for declines in pollinator populations in North America, including,
among others, exposure to pathogens, parasites, and pesticides; habitat
fragmentation and loss; climate change; market forces; intra- and interspecific competition with native and invasive species; and genetic alterations.
Careful evaluation of the literature allows some causes to be assigned, but
explanations are ambiguous or elusive for other species losses.
DECLINE IN ACTIVELY MANAGED POLLINATORS
Honey Bees (Apis mellifera L.)
The best evidence of specific pollinator decline is seen in the western
honey bee, Apis mellifera L., the primary commercial pollinator of agricultural crops in North America and the most widely used, actively managed
pollinator in the world (Delaplane and Mayer, 2000; Kearnes et al., 1998;
McGregor, 1976). The population losses among honey bees are elucidated
in a large body of literature on honey bee pests, parasites, and pathogens
(Morse and Flottum, 1997), most notably on the parasitic mites Varroa
destructor (varroa mite) and Acarapis woodi Rennie (tracheal mite), the
pathogen Paenibacillus larvae (American foulbrood, [AFB]), and the invasive Africanized honey bee.
75

76
Parasitic Mites
Varroa Mite (Varroa destructor)
The supply of healthy and affordable honey bee colonies for crop pollination clearly has been threatened by the arrival of parasitic mites Varroa
destructor and Acarapis woodi. Since 1981just before the arrival of A.
woodistocks of honey bee colonies in the United States have declined by
39 percent (Figure 2-1; USDA-NASS, 1995, 1999, 2005, 2006). Parasitism
by mites of honey bees is a relatively recent problem in North America. A
19801982 survey of samples from 4,400 apiaries in the United States and
Canada revealed no evidence of mite infestation (Shimanuki et al., 1983).
The varroa mite was first reported in the United States in 1987 (Anonymous,
1987) and within a decade it had become established throughout the United
States.
Varroa destructor (Anderson and Trueman, 2000) has caused dramatic
declines in honey bee abundance in North America and throughout the
world (DeJong, 1990; DeJong et al., 1982a; Sammataro et al., 2000). The
varroa mite is an obligate external parasite of A. mellifera and Apis cerana
(eastern honey bee) that was first described as V. jacobsoni (Oudemans,
1904) in Java. It exists there in a stable and sustainable association with
A. cerana, its native host (Rath, 1999). In eastern honey bee colonies, female varroa mites reproduce almost exclusively on male (drone) larvae or
pupae (Koeniger et al., 1983), so they do not affect the population size of
the female worker force. The biology of A. cerana, including its relationship
with the varroa mite, is discussed by Kevan et al. (1996) and by Oldroyd
and Wongsiri (2006).
The association of V. destructor with the western honey bee, A. mellifera, reportedly began in the 1950s (Matheson, 1995) when the mites
moved into honey bee colonies brought into the home range of A. cerana.
Subsequently, the varroa mite has established a nearly cosmopolitan distribution with respect to its new host, and Australia is now the only mite-free
continent (Matheson, 1995). It is not known how this parasite entered the
United States.
In A. mellifera, female varroa mites reproduce on both worker and male
larvae. Infestation of honey bee colonies of European origin (the source of
most A. mellifera introduced to North America) is fatal if untreated, and
colony mortality usually occurs 6 months to 2 years after the initial infestation (DeJong, 1990).
Newly emerged adult worker bees parasitized as pupae exhibit a range
of symptoms: substantial loss of adult weight (DeJong et al., 1982a,b; Engels
and Schatton, 1986), reduced concentrations of serum proteins (Engels and
Schatton, 1986), impaired development of (brood food-producing) hypopharyngeal glands (Schneider and Drescher, 1987), severe deformations of

CAUSES OF POLLINATOR DECLINES AND POTENTIAL THREATS
77
the wings (Akratanakul and Burgett, 1975), and reduced longevity (DeJong
and DeJong, 1983).
Varroa parasitism of A. mellifera drones also can affect the ability of
the queen to obtain adequate supplies of healthy sperm during mating.
Parasitism has been associated with reduced sperm quality (Collins and Pettis, 2001) and with decreases in adult weight, size of seminal vesicles, and
mucus. Effects of parasitism on male behavior include a decline in the frequency of flight (Schneider, 1986) and decreased flight performance, sperm
production, and mating efficiency (Bubalo et al., 2005; Duay et al., 2002).
Varroa parasitism of honey bees is associated with viral pathogens, and
some damage attributed to varroa mites is actually viral in origin (Allen and
Ball, 1996). Although some viral diseases of honey bees are associated with
varroa infestations (Kevan et al., 2006; Oldroyd and Wongsiri, 2006), which
negative effects are exclusively attributable to direct actions of the mites or
to their associated pathogens is unknown (Chen et al., 2005). Parasitic mite
syndrome is used to describe colonies that exhibit a constellation of symptoms, including the presence of diseased adult and immature bees, adults
with deformed wings, and crawling bees at hive entrances (Shimanuki et al.,
1994). Once this syndrome is apparent, the colony begins a rapid decline
in adult worker population and viable replacement brood. It dies, typically
within 36 weeks of the onset of symptoms.
The rate at which the varroa mite population increases in a honey bee
colony depends in part on the rate at which individual mites reproduce
(Fries et al., 1994). Some stocks of honey bees, such as neotropical Africanized honey bees (see section on Invasive Species in this chapter), are less
susceptible to varroa mites than are other stocks, apparently because they
have slightly faster developmental times, thus depriving the mites of the time
necessary for successful reproduction (Camazine, 1986).
Twenty years after its introduction to the United States, V. destructor
continues to devastate honey bee populations. High losses have been reported
locally (Burgett, 1994; Loper, 1995) and nationally. During the winter of
19951996, northern U.S. beekeepers experienced their largest losses in
history; in some states, 30 to 80 percent of colonies were lost (Finley et
al., 1996). Similar losses were observed in the winters of 20002001 and
20042005 (Caron and Hubner, 2001; Lumkin, 2005). Data on colony losses
are derived from informal surveys of beekeepers, and the exact causes of
colony deaths have not been established. However, except for the large loss
of honey bee colonies in the 1940s from the bacterial disease, AFB, losses on
this scale were never reported before the detection of parasitic mites (Finley et
al., 1996). These honey bee losses have occurred despite the industrys heavy
reliance on pesticides to control mite populations. Pesticide resistance has
become widespread (Elzen et al., 1998, 1999d) and many beekeepers are no
longer able to use the few registered pesticides for varroa control.

78
New miticides formulated from natural products (Calderone, 2000;

Calderone and Nasr, 1999; Calderone and Spivak, 1995; Calderone et al.,
1997) and fungal pathogens Hirsutella thompsonii and Metarhizium anisopliae have shown promise, but problems with temperature sensitivity and
treatment methods remain unresolved (Kanga et al., 2003a,b).
Operating costs for beekeepers have increased because of varroa mite
infestations (Kemp, 2000); expenses include those for pesticide treatment
(material and labor) and to replace colonies killed by the mites. Replacing
colonies also requires additional labor and, because the new colonies are
smaller, they produce less honey the first year than healthy colonies that
have successfully wintered (Morse, 1994). The bee industry badly needs
improved methods for managing varroa mites, including methods of breeding for resistance in hosts (Chapter 6).
Tracheal Mite (Acarapis woodi)
The tracheal mite Acarapis woodi is an internal parasite of A. mellifera.
Initially identified in the United Kingdom in 1921 (Imms, 1921; Rennie,
1921), tracheal mites were first detected in the United States in 1984 in
Texas, where they most likely entered into the country on swarms of bees
from Mexico (Eischen et al., 1990; Hall and Eischen, 1991; Pettis et al.,
1987). At first, tracheal mites caused serious damage to colonies in the
United States (Eischen, 1987; Eischen et al., 1989; Frazier et al., 1994;
Otis, 1990; Sammataro et al., 2000; Scott-Dupree and Otis, 1991), but attention to tracheal mites has diminished as beekeepers struggle to manage
the more problematic varroa mite. Perhaps this is also related to findings of
heritable variation in honey bees for resistance to tracheal mites (Gary et al.,
1990; Nasr et al., 2001; Page and Gary, 1990). Several chemical treatments
have been identified to control tracheal mites (Calderone and Shimanuki,
1995; Clark, 1990; Delaplane, 1992; Wilson and Collins, 1993; Wilson et
al., 1989, 1990). The current status of the tracheal mite and its impact on
honey bees are unknown.
Pathogens
Paenibacillus larvae (formerly Bacillus larvae: White, 1920) is the
most serious honey bee pathogen. It causes AFB, a disease of larval honey
bees. AFB is highly virulent and easily spread among colonies as a result
of beekeeper activity and bee behavior, and it is generally fatal if untreated
(Shimanuki, 1997). During the first half of the 20th century, AFB was the
most serious threat to beekeeping, and it caused tremendous loss of colonies,
amounting to hundreds of thousands in the 1940s (Barrett, 1955). The incidence of AFB was reduced dramatically by the introduction of antibiotics

79
and by state apiary inspection programs that required the burning of infected hives (Barrett, 1955).
Sulfathiozole (Hasemans and Childers, 1944) was the first effective
chemotherapeutic agent used to control AFB, but its use was discontinued in
the United States because of concerns with residues in honey (Lodesani and
Costa, 2005). Gochnauer (1951) reported good control with oxytetracycline
(Terramycin) and was a mainstay in AFB prevention until the 1990s
(Wilson, 1970; Wilson et al., 1973). However, AFB is troublesome because
its spores are refractory to antibiotics (Shimanuki, 1997) and can persist
on contaminated equipment for more than 80 years. Treatment of colonies
with active cases of AFB eliminates disease symptoms, but withdrawal of
antibiotics is generally followed by disease recurrence (Allipi et al., 1999).
Even when infected colonies are treated with antibiotics, there is still a
major threat to nearby healthy colonies because the infected colonies can
serve as reservoirs of infective spores. Consequently, the use of oxytetracycline is recommended as a preventive rather than as a treatment for active
cases. Most states still require that colonies with active cases of AFB be
destroyed and the equipment be burned or buried (Ratnieks, 1992).
Resistance to the antibiotics used against AFB was not observed in the
United States until about 1994 (Shimanuki and Knox, 1994), but it has become widespread, and AFB is now a resurgent threat to the industry (Cox
et al., 2005; Evans, 2003). Tylosin tartrate (Tylan) is an effective control
agent (Alippi et al., 1999; Elzen et al., 2002; Hitchcock et al., 1970) that
recently received Food and Drug Administration approval (FDA-CVM
Update, October 20, 2005). However, a single chemical treatment is only a
short-term solution, as has demonstrably been the case with treatment for
varroa mites.
Pesticides
The application of pesticides, especially insecticides used to control
crop pests, kills or weakens thousands of honey bee colonies in the United
States each year (Johansen and Mayer, 1990). Local bee kills have occurred
sporadically for decades and likely have not contributed significantly to the
recent national decline in colony populations (Chapter 2). Most pesticidecaused bee kills are the result of accidents, careless application, or failure
to adhere to label recommendations and warnings (Johansen and Mayer,
1990).
A few examples illustrate the nature of the problem: mosquito control
programs have resulted in major losses of honey bees in Canada and the
United States (Dixon and Fingler, 1982, 1984). In Manitoba, efforts to
combat serious outbreaks of western equine encephalitis by controlling its
mosquito vectors resulted in colony losses that amounted to $850,000 in

80
1983 (Dixon and Fingler, 1984). In California, between 1966 and 1979,
before the emergence of the varroa mite, insecticides caused the death of
more than 1 million coloniesaccounting for 47 percent of bee colony
deaths in that periodcausing a 10 percent decrease in population (NRCC,
1981, Table 6, p. 83).
Recent trends in North America and many other parts of the world are
toward reducing the use of pesticides in agriculture and forestry, to mitigate
problems associated with pesticide applications, and adopting such practices
as restricting spraying to times when pollinators are not foraging (Adey et
al., 1986; Johansen and Mayer, 1990). In a lawsuit against the State of Minnesota and the International Paper Company (the landowners), beekeepers
alleged that the landowners sprayed carbaryl insecticide (Sevin XLR Plus)
to control cottonwood leaf beetles (Chrysomela scripta) despite the knowledge that the tree plantations were within the foraging range of beekeepers
apiaries. Although the case was disposed by the Minnesota District Court,
the Supreme Court reversed the District Courts decision (http://www.beyondpesticides.org/news/daily_news_archive/2005/03_10_05.htm). The State
of Minnesota settled out of court with a $335,000 payment to beekeepers
(Anonymous, 2005; Schell, 2005).
Sublethal effects of pesticides on bee foraging behavior have been reported (Pham-Delegue et al., 2002). For example, there have been reports in
Europe that exposure to Gaucho (imidacloprid) impairs the navigational
and foraging abilities of honey bees. These results have not been obtained
in all studies (Pham-Delegue et al., 2002), and the effect of imidacloprid on
honey bees is controversial. However, other pesticides have been shown to
impair bee behavior, so the threat of sublethal effects of pesticides on bee
foraging behavior is real.
The negative impact of pesticides on managed honey bee colonies suggests that feral bee populations could be similarly affected by pesticides,
but there are no studies on the latter subject to the committees knowledge.
Feral honey bees have not been studied intensively (see Chapter 2). Pesticides
can potentially harm many bee species and even eliminate some pollinator
populations in ecosystems. However, bee populations seem to recover once
pesticide application ceases (for example, Kevan et al., 1997) unless the
populations are eliminated over a very large area.
Transgenic Crops
Transgenic crops were developed in part to reduce the unintended effects of pesticides. However, the deployment of crop plants genetically engineered to express insecticidal proteins in pollen raised questions about direct
effects on nontarget species, including some pollinators (Losey et al., 1999).
For honey bees, the concerns involved the potential lethality of insecticidal

81
transgenic proteins, the sublethal effects of these proteins on insect behavior,

physiology, and reproduction and the economic effects of transgenic pollen
as a contaminant of honey. Malone and Pham-Delgue (2001) reviewed the
small literature on this topic and concluded that, in some cases, there are
negative but sublethal effects attributable to consumption of transgenic pollens. These effects varied with the identity of the transgene and the amount
of its expression but in no case have any effects of transgenic crops on honey
bee populations been documented.
Invasive Species
Africanized Honey Bees
The Africanized honey bee is a hybrid of the African race, A. mellifera
scutellata, intentionally introduced to Brazil in the early 1950s (Winston,
1992), and European races of A. mellifera introduced with European colonists in the 1600s (Sheppard, 1989a,b). The Africanized honey bee gained
some measure of notoriety because it is more defensive than most European
races of honey bee; when disturbed, colonies of Africanized honey bees
respond more aggressively and with more rapid and prolonged stinging
behavior (Winston, 1992). The spread of the Africanized honey bee from
South to North America is one of historys most spectacular examples of
biological invasion (Roubik, 1989; Schneider et al., 2004). Several traits
have facilitated the establishment of Africanized honey bees: their colonies
grow faster than do those of the European honey bees, and there are genetic incompatibilities in hybrids that favor loss of European traits; African
drones exhibit mating advantages; Africanized bees have a greater ability to
establish nests in a broader variety of locations; and they exhibit more nest
usurpation behavior than do European bees (Schneider et al., 2004). The
influx of Africanized bees into the United States began several years after
resident honey bee populations had experienced sharp declines (Chapter 2);
Africanization of U.S. bees was not a cause of those declines.
Africanized honey bees were first detected in the United States in Hidalgo, Texas, in 1990 (Hunter et al., 1993). They have spread throughout
the Southwest, parts of California, and most recently (National Plant Board,
2005), parts of the Southeast including Florida (Figure 3-1). Africanized
honey bees have not spread into Canada because the border between the
two countries has been closed to transport of honey bees since tracheal mites
were detected in the United States (see Chapter 2). If the border were to reopen to allow imports of packaged bees and queens from the United States,
there would be potential for Africanized bees to be imported to Canada.
Although the Brazilian (DeJong, 1996; Goncalves et al., 1991) and
Mexican (Guzman-Novoa and Page, 1994a, 1999) bee industries eventually

83
have adjusted well to Africanized honey bees, beekeeping in Mexico and

Brazil differs in many fundamental ways from that in the United States and
Canada, and experiences with Africanized bees in those countries might not
serve as useful models for the rest of the hemisphere.
The presence of Africanized bees throughout the southern and southeastern United States could exacerbate losses of European honey bee colonies documented in Chapter 2 (Winston, 1992). Africanized bees reproduce
(swarm) more often than do European bees (Danka and Rinderer, 1986;
Winston, 1979; Winston et al., 1981), which has two important consequences. First, colonies are weakened as a result, and weaker colonies do not
pollinate as efficiently as stronger colonies (Winston, 1987). Second, swarms
of honey bees often settle in places near humans, posing an increased health
hazard.
Colonization by Africanized honey bees might make it more difficult
to obtain replacement queens and packages from desirable stocks. As Africanized honey bees move northward, farther into California, and eastward
into the southeastern United States, they will enter the principal queen- and
package-producing regions (northern California, Georgia, Alabama, Louisiana, Mississippi, Florida) and wintering areas for migratory beekeepers
(Florida, Louisiana, South Carolina, Texas), who move their colonies as
crops come into bloom. Each year, the bee packaging industry supplies at
least a million queens and packages of bees (Schiff and Sheppard, 1995,
1996) for replacement of colonies that succumb to winter stress, mites, or
the rigors of migratory beekeeping. About half of the queens are produced
in the western United States and half in the southeastern United States.
Africanized honey bees will also encroach on prime agricultural regions
such as the almond orchards in California. Africanized honey bees are less
desirable than European honey bees as commercial pollinators because they
forage over relatively short distances (Danka et al., 1993) so they are not
appropriate for some crops. They also are more likely to abandon their
colonies altogether when food is scarce (Danka et al., 1987; Winston et al.,
1979, 1983), and shortages of nectar can occur when honey bee colonies
are used at high densities to pollinate orchards or fields. Most important,
Africanized honey bees aggressive behavior contributes to increased liability
costs and regulations banning the movement of bees into or through certain
areas (Danka et al., 1987). Beekeepers are almost entirely dependent on the
goodwill of rural property owners to find locations for their apiaries.
Predictions about the eventual distribution of Africanized honey bees
in the United States vary. Some researchers suggest Africanized bees will
become established across all the southern states (Dietz and Vergara, 1995;
Rinderer, 1986; Taylor, 1977). Africanized bees are not likely to survive in
the interior portions of the United States, but partially Africanized colonies
(European or Africanized queens mated to one or more Africanized drones)

84
could (Dietz and Vergara, 1995). The seasonal movement of packages,

queens, and beekeepers servicing crops both within and outside areas with
Africanized honey bees could contribute to an increase in range, even if
temporary in some locales.
Small Hive Beetle (Aethina tumida)
Native to South Africa (Lundie, 1940), the small hive beetle (Aethina
tumida) was detected in the United States in 1998 (Thomas, 1998), but how
it arrived is not known. Adults and larvae eat pollen, honey, and brood, in
the process damaging colonies and beekeeping equipment (Thomas, 1998).
They especially damage combs of unextracted honey stored in honey houses
(Hood, 2004a); the larvae burrow through the combs and defecate in them,
causing the honey to ferment and leak from the combs (Headings, 2000).
The small hive beetle is found throughout the eastern United States,
although it is considered an economically important pest only along the
southeastern coast (Hood, 2004b). In northern states, it is a manageable
pest of honey houses that is not associated with colony losses (Neumann and
Elzen, 2004). Whether it becomes a more noxious pest could depend on its
capacity to expand its range; its ultimate distribution in the United States
could be affected partly by soil conditions (Ellis et al., 2004a). Whether it
will remain manageable is an open question as well. Chemical controls are
available (Elzen et al., 1999b), and biological control agents show promise
(Ellis et al., 2004b; Richards et al., 2005). Racial variation in the response
of honey bees to A. tumida infestation (Elzen et al., 2001) suggests that
selection for resistance to this pest, like selection for resistance to AFB and
varroa mites, is possible.
Bumble Bees (Bombus spp.)
Starting in the early 1990s, companies in Europe (Banda and Paxton
1991), Israel, and Canada (Kevan et al., 1991) developed commercial insectary techniques for mass-rearing bumble bees year-round to pollinate
tomatoes, sweet peppers, and several other greenhouse crops (Banda and
Paxton, 1991; Kevan et al., 1991). In the United States and Canada, Bombus
impatiens and B. occidentalis have been the main species used commercially,
although B. occidentalis has not been reared by Koppert since 1998 (M.
Tacolla, Koppert Biological Systems, Inc., personal communication, March
2006), and the other company is closing its rearing program soon (R. Ward,
Biobest Canada Ltd., personal communication, June 2006). Because bumble
bees are reared and deployed for pollination at high densitiesas many as
23,000 individuals per greenhouse (Morandin et al., 2001)they are particularly vulnerable to pathogens and parasites.

85
Parasites
Bumble bees suffer from infestation by several parasites, notably the
protozoans Nosema bombi and Crithidia bombi and the tracheal mite
Locustacris buchneri (Imhoof and Schmid-Hempel, 1999; Shykoff and
Schmid-Hempel, 1991). The two protozoan parasites often occur together
in European bumble bees. Although C. bombi is suggested not to be native
to North America (its natural host is the European B. terrestris), it has been
found in B. impatiens and B. occidentalis in North America, likely because
the three species were reared together in the same insectary facilities in Europe (Colla et. al, 2006; Thorp, 2003; Winter et al., 2006) during the years
when queens collected in North America were sent to Europe to establish
colonies and then returned to North America. Presumably, cross-infected
bees returned to North America for pollination of greenhouse crops also foraged outside the greenhouses and infected wild bees (Colla et al., 2006).
A new threat to bumble bees is deformed wing virus, originally a disease
of honey bees, that has been found in B. terrestris in European commercial
breeding operations and in a feral colony of B. pascuorum in Germany
(Genersch et al., 2006). The frequency of this disease in honey bees is increasing because of oral transmission and transmission by varroa mites; in bumble
bees, transmission appears to be exclusively oral. Discovery of this virus in
bumble bees raises questions about transmission and cross-infectivity among
bumble bees and between bumble bees and honey bees, as well as the potential risks of commercial trafficking in bumble bees (R. Thorp, University of
California, Davis, personal communication, April 2006).
There is growing evidence of the proliferation of exotic pathogens and
parasites in populations of commercially reared bumble bees in the United
States and Canada (Colla et al., 2006). Bumble bees used in greenhouse
pollination frequently harbor high levels of different pathogens (Colla et
al., 2006), and infected colonies exhibit reduced survival and reproduction
and diminished foraging efficiency (Brown et al., 2003; Fisher and Pomeroy,
1989; Gegear et al., 2005; Husband and Sinha, 1970; Macfarlane et al.,
1995; Otterstatter et al., 2005). Nosema bombi is globally associated with
bumble bees, and its ubiquity in managed colonies presents a palpable risk
to wild bumble bee populations in North America (Flanders et al., 2003;
Thorp et al., 2003).
Pesticides
The damage to honey bees inflicted by insecticides suggests that similar
problems occur for other managed and unmanaged bee species (Helson et al.,
1994; Johansen and Mayer, 1990; Torchio, 1973). Nontarget effects, however, particularly in unmanaged populations, tend to be poorly documented,

86
so the scope of the problem is unclear. The few comparative studies give evidence that pesticide toxicities are not necessarily predictive of the hazards to
other bee species (Johansen and Mayer, 1990; Kevan and Plowright, 1995;
NRCC, 1981). Like honey bees, bumble bees can be exposed to pesticides
while foraging (Gels et al., 2002; Tasei et al., 2001). Ground-nesting bumble
bees, however, are uniquely susceptible to pesticides applied to turf or lawns
for grub control (Gels et al., 2002). Effects can be sublethal (Belzunces et
al., 2001; Tasei et al., 1994); for example, imidacloprid (Morandin et al.,
2005) and clothianidin (Franklin et al., 2004) can hamper foraging and
pollinating. Morandin and Winston (2003), however, reported no effects
of the transgenic (insecticidal) proteins Cry1ac or chitinase.
Because almost all bumble bee deaths caused by pesticide exposure
are unreported, determining their implications for bumble bee population
declines is difficult, if not impossible. Thompson (2001) suggested that nontarget exposures can disproportionately affect bumble bee numbers if they
occur early in the season when queens are still foraging and when colonies
are very small (Thompson, 2001). During studies on the environmental
effects of fenitrothion on pollination and bumble bees in New Brunswick,
Canada, Plowright and his colleagues (1978) noted severe bumble bee
population reductions that were evidenced in changed foraging behavior of
surviving colonies. Foraging trip times declined because there was less competition with congeners for floral resources and the bumble bee populations
rebounded quickly (reviewed in Kevan and Plowright, 1995).
Alfalfa Leafcutting Bees (Megachile rotundata F.)
Alfalfa (= lucerne) is a major forage crop grown for free-ranging livestock and as hay for livestock feed. In the United States, about 25 million
acres (about 10 million hectares) of alfalfa are planted annually, and the
crop has an estimated value of more than $5 billion (Flanders and Radcliff,
2000). The primary pollinator is the introduced alfalfa leafcutting bee Megachile rotundata F. Management techniques for this solitary bee are well developed (Peterson et al., 1992; Stephen, 2003); however, chalkbrood disease
nearly destroyed the production of leafcutting bees in the United States.
Chalkbrood is a fungal disease caused by Ascosphaera aggregata Skou
(Goettel et al., 1997; Vandenberg and Stephen, 1983). Larvae contract
chalkbrood by ingesting pollen contaminated with fungal spores. After
germinating in the midgut, the fungus infiltrates the hemocoel and mycelia
proliferate, turning the body chalk-white (Vandenberg and Stephen, 1983).
The disease was first noted in Nevada in 1973 and has since spread to most
areas in western North America (Stephen et al., 1981), where total bee
mortality rates can exceed 60 percent.
Because chalkbrood disease is less common in Canada, most leafcutting

87
bee production in North America is in British Columbia, Saskatchewan,

Alberta, and Manitoba. Although some seed growers in the United States
can replace bee stocks in a good year, a loss of 50 percent or more is typical. Consequently, large numbers of alfalfa leafcutting bees are imported
from Canada each year (R. Bitners presentation to the committee, January
14, 2006). Canadian beekeepers produce large numbers of healthy bees,
perhaps because of increased resistance to chalkbrood in Canadian stocks
(Vandenberg, 1991). But if chalkbrood disease becomes endemic in Canada,
leafcutting bee production could be jeopardized (Peterson et al., 1992). Efforts to select for resistant stocks of M. rotundata in the United States have
been unsuccessful (Stephen and Fichter, 1990a,b). Although recent records
are difficult to find, there have been losses of alfalfa leafcutting bees caused
by pesticides in the western United States (Johansen, 1977). In Manitoba,
law protects alfalfa leafcutting bees from pesticide applications (Tang et
al., 2005).
Alkali Bee (Nomia melanderi Cockerell)
The alkali bee, Nomia melanderi Cockerell, is the worlds only intensively managed ground-nesting bee. In regions of the western United States,
particularly in southeastern Washington and formerly in several other areas
(among them, Lovelock, Nevada), alfalfa seed growers construct large subirrigated nest sites with salt-crusted surfaces for this bee. Densities of 400
nests per square meter over a hectare or more can be obtained with this
gregarious bee (Bohart, 1970, 1972a; Fronk, 1963).
Alkalli bee mortality can be caused by a variety of vertebrate and invertebrate predators, microbial pathogens, inadvertent pesticide exposure
(especially aerial applications of pesticide for rangeland grasshoppers), vehicular traffic (which can kill bees crossing roads near their nest sites), and
nest site flooding. Economic factors, however, were primarily responsible
for declines in North American populations. Low prices for alfalfa leafcutting bees led growers to abandon the maintenance of nesting sites, leading
to a decrease from peak populations of more than 400,000 nesting females
per site to a few thousand per site in Touchet Valley, Washington. Prices of
leafcutting bees have risen recently, as have prices of alfalfa, leading to an
increase in the cultivation of alkali bees (Stephen, 2003).
DECLINE IN NATURAL OR WILD POLLINATORS
Pathogen Spillover
Nosema bombi could be the most important factor responsible for the
extinction of Bombus franklini (Thorp et al., 2003), perhaps via patho-

88
gen spillover (Colla et al., 2006; Box 3-1), which can occur when heavily
infected, domestic hosts interact with closely related wild populations.
Commercially produced bumble bees used for greenhouse pollination often have extensive pathogen infections that can spread to wild bees when
the commercial bees escape from greenhouses and interact with their wild
BOX 3-1
Unintended Consequences of Greenhouse Pollination
and Native Pollinators

When commercial growers began to grow tomatoes in greenhouses,
they realized that good fruit set required pollination (Velthuis, 2002). Tomato flowers have poricidal anthers that are typically pollinated by buzz
pollinationthe vibration of the wing muscles of large bees that land on
flowers to collect pollen. Different techniques were investigated to achieve
pollination mechanically: blowers were installed to move pollen around,
overhead wires used as trellises were struck or shaken, and hand-held
electric vibrators were used to shake individual flowers. Introducing bees
into greenhouses proved the most economical strategy. Although some
pollination can be accomplished by honey bees, bumble bees are much
more efficient. In the 1980s, large-scale bumble bee rearing operations
began in Europe for use by growers of greenhouse tomatoes and other
crops.

Two unintended consequences have resulted from this commercially
successful effort. First, because greenhouses are not generally airtight
and sometimes are not screened, bumble bees escape and establish in
areas of the world where they are not native. The effects have not yet
been widely studied, but they are likely to include competition with native bees. Second, the commercial rearing and export of bees has also
resulted in transport of bumble bee parasites and diseases, possibly
causing the apparent local extinction of B. occidentalis from the west
coast of the United States in recent years and the disappearance of B.
franklini from its relatively small range in the area along the Oregon and
Washington border.

Because there are no large-scale monitoring operations for bumble
bee distribution and abundance, it is difficult to determine the consequences of introducing bees and their diseases. Internal tracheal mites
of European origin have been found in wild bumble bees in Japan, and
Nosema bombi, a microsporidian parasite of bumble bees, has been
found in colonies imported from Europe (Colla et al., 2006; Thorp et al.,
2003).

89
counterparts at nearby flowers. In Canada and elsewhere, foraging bumble

bees can escape from greenhouses and survive; Whittington and colleagues
(2004) reported that as much as 73 percent of the pollen carried by Bombus
foragers in greenhouses comes from native plants and weeds growing outside, and the European species B. terrestris is now established in Japan after
its introduction for greenhouse pollination (Matsumura et al., 2004). Managed, greenhouse-reared bumble bees are likely to come in contact with wild
Bombus species. If extinction of B. franklini was caused by pathogen spillover, this species has the unfortunate distinction of providing the first known
example of this phenomenon in wild invertebrates; pathogen spillover has
been reported in vertebrates and plants (Power and Mitchell, 2004).
Interspecific Competition in Bees
Pollinators have been introduced from one part of the world to another
for at least three centuries, resulting in the establishment of one species
(Apis mellifera) and several species of another genus (Bombus) on most
continents. Many other introduced species have become established in
the United States and Canada (Table 3-1). The major damage caused by
introduced species includes competition with native pollinators for floral
resources and nest sites (Barthell and Thorp, 1995; Barthell et al., 1998;
Thorp et al., 2000; Box 3-2), inadvertent introduction of natural enemies
(Butz-Huryn, 1997; Dupont et al., 2004; Kato et al., 1999; Paton et al.,
1992, 1996; Roubik, 1978), especially pathogens that can escape into wild
populations of native pollinators, enhanced pollination of exotic weeds and
furthering their spread by increasing seed set (Barthell et al., 2001; Goulson
and Derwent, 2004), and disruption of the pollination of native plants via
deposition of heterospecific pollen on the stigma.
The extent to which introduced species disrupt native communities
remains equivocal (Goulson, 2003a; Schaffer et al., 1983). Schaffer and colleagues monitored agave blossoms in Arizona before, during, and after the
introduction of genetically marked honey bees (Schaffer et al., 1983). They
reported that honey bees lowered the available amount of Agave pollen and
nectar, and their introduction led to shifts in the numbers of foraging native
bumble bees and nectar-feeding ants. Short-term effects of interspecific competition have been documented, including beneficial effects to plants (Dick,
2001), but long-term population effects have not been documented.
Honey bees are highly polylectic (they collect pollen from many unrelated plants) and because even a few colonies can collect hundreds of
kilograms of nectar and dozens of kilograms of pollen annually (Buchmann,
1996), they can lower the available amount of nectar and pollen in diverse
natural plant communities (Paton, 1990, 1993, 1996). The flower-visiting
behavior of native flower visitorssuch as bees, hummingbirds, ants, and

90
TABLE 3-1 Exotic Bee Species Now Established in the United States and
Canada (Polylectic Species Collect Pollen from Many Unrelated Plants)
Scientific Name
Introduction
Dates
ANDRENIDAE
Andrena wilkella (Kirby)
Accidental
17001800s
APIDAEa
Apis mellifera L.
Apis mellifera scutellata Lepeletier
Anthophora plumipes (Pallas)
Ceratina cobaltina Cressonb
Ceratina dalltoreana Friese
Centris eisenii Foxc
Introduced
Introduced
Introduced
Accidental
Accidental
Accidental
1620s
1950s
1980s
1970s
1940s
1990s
Xylocopa tabaniformis parkinsonae Cockerelld
Accidental
1980s
COLLETIDAE
Hylaeus bisinuatus Forster
Hylaeus hyalinatus Smith
Hylaeus punctatus Brulle
Accidental
Accidental
Accidental
19901910
1990s
1980s
MEGACHILIDAE
Anthidium manicatum L.
Anthidium oblongatum (Illiger)
Chelostoma campanularum (Kirby)
Chelostoma fuliginosum (Panzer)
Hoplitis anthocopoides (Schenck)
Lithurgus chrysurus Fonscoloombe
Megachile apicalis (Spinola)
Accidental
Accidental
Accidental
Accidental
Accidental
Accidental
Accidental
1960s
1990s
1960s
1960s
1960s
1970s
1930s
Accidental
Accidental
Accidental
Accidental
1940s
17001800s
19201945
1990s
Osmia coerulescens (L.)
Accidental
1800s
Osmia cornifrons (Radoszkowski)

Osmia cornuta (Latreille)
Introduced
Introduced
1960s
1980s
Megachile concinna Smith

Megachile lanata (F.)
Megachile rotundata (F.)
Megachile sculpturalis Smith
aCeratina (Pithitis) smaragdula (F.) was deliberately introduced to California and Florida,
but failed to establish (Daly et al., 1971).
bThe neotropical bee Ceratina cobaltina Cresson has been collected sporadically in Texas
since 1978 and may be adventive (J. Neff, Central States Melittological Institute, Austin, Texas,
personal communication, October 2005).
cThe centridine Centris eisenii has been collected at horticultural plantings of Callaeum
macropterum (its floral oil host plant) from Nogales to Tucson, Arizona, since the 1990s, and
is likely adventive and established in southern Arizona (S. Buchmann, unpublished data).

91
Distribution
Floral Host
Reference
Northeastern United States,

eastern Canada
Polylectic
Malloch, 1918
Global, except polar regions

Southern United States, California
Maryland
Texas
California
Southern Arizona (Nogales,
Tucson)
Texas (Austin only)
Polylectic
Polylectic
Polylectic
Polylectic
Polylectic
Callaeum macroptera,
Lycium spp.
Polylectic
Smith, 1977
Winston, 1992
Batra, 1994a, 2003
Neff, personal communication
Daly, 1966
Buchmann and Snelling,
personal communication
Neff, personal communication
Transcontinental
New York
California
Polylectic
Polylectic
Polylectic
Snelling, 1970
Ascher, 2001
Snelling, 1983
New York, Connecticut, Ontario

Mid-Atlantic States
New York
New York
New York, Virginia
New Jersey (now locally extinct?)
Eastern United States, Washington,
Oregon, California
Transcontinental
Florida
Transcontinental
Eastern United States
Polylectic
Polylectic
Campanula
Campanula
Echium
Centaurea
Polylectic
Jaycox, 1967
Hoebeke and Wheeler, 1999
Eickwort, 1980
Eickwort, 1980
Eickwort, 1980
Roberts, 1978
Stephen and Torchio, 1961
Asteraceae
Polylectic
Fabaceae
Polylectic
Butler and Wargo, 1963

Mitchell, 1962
Stephen and Torchio, 1961
Mangum and Brooks, 1997;
Batra, 1998
Rust, 1974
Northeastern and northwestern

United States, parts of Canada
adjacent to the United States
Transcontinental, patchy
Limited local U.S. releases
Fabaceae
Rosaceae
Rosaceae
Batra, 1998
Torchio and Asensio, 1985;
Torchio et al., 1987
dThe larger carpenter bee (Xylocopa tabaniformis parkinsonae) is now a permanent resident
of the city limits of Austin, Texas, likely having been accidentally introduced (an anthropogenic
range extension) in firewood, which may also have been the case with Ceratina cobaltina.
SOURCE: Adapted with permission from Cane (2003).

92
BOX 3-2
Competition Between Managed and Wild Pollinators

If a plant community is close to its carrying capacity for pollinators,
introduction of additional pollinators by moving in managed colonies
of honey bees or other bees, or the introduction of more native bees,
presents the potential for increasing competition for floral resources. This
potential for competition has been a concern for areas where honey bees
are not native but have been introduced or proposed for introduction, and
also for areas (Australia) where bumble bees are not native but have
been proposed for introduction. In a literature review in 1997, Butz-Huryn
concluded that the presence of honey bees, however, alters the foraging
behavior and abundance of some native fauna on flowers, but no studies
have shown detrimental impacts of honey bees on population abundances of any native animals or plants. More recently, in a combination of
observational and experimental studies, Thomson (2006) found that niche
overlap between honey and bumble bees reached levels as high as 80 to
90 percent during times of resource scarcity, but only in 1 of 7 months of
observation was there a significant negative relationship between them.
In an experimental study, however, the mean numbers of bumble bee
foragers observed on a given transect increased significantly with greater
distance from introduced honey bee colonies. Of the three measures
(niche overlap, correlations in abundances, and effects of experimental
introductions) that Thomson considered, only the experimental data on
forager abundances accurately estimated competitive effects on colony
reproductive success.

These studies suggest that it may not be easy to detect competition
between pollinators, even if it is affecting reproductive success. If feral
honey bee colonies increase again in North America, for example if disease-resistant strains are developed, there may be subtle, unintended,
but significant effects on native bees that use the same floral resources.
If this alters visitation and pollination rates of native plants, there may be
consequences for their populations as well.
waspsshifted after the experimental introduction of honey bees to a chaparral area in southern Arizona (Schaffer et al., 1979, 1983).
An experimental study in California examined the effects of competition
with Apis mellifera on colony foraging behavior and reproductive success of
a native eusocial bee, B. occidentalis (Thomson, 2004). Bumble bee colonies
in competition with honey bees experienced increased nectar scarcity and
had lowered rates of larval production. Thus, A. mellifera can competitively
suppress a native bee species that is a known important pollinator. The

93
competitive effects of introduced pollinators depend on phenology (seasonal

timing), abundance, and overlap in resource use. Competition among bees is
likely because some bumble bee species have proboscides (tongues) that
are the same length as the proboscis of A. mellifera (Inouye, 1977); proboscis length determines in part the range of plants that can be used as nectar
sources (Harder, 1982, 1983, 1986; Stang et al., 2006). After Africanized
bees were experimentally introduced into a community of neotropical stingless bees, native bee numbers declined, as did their use of floral resources
(Roubik, 1978, 1980; Roubik and Wolda, 2001).
In addition to competitively suppressing native bees, exotic bees can
affect ecosystem function by virtue of their foraging habits. Many exotic
species demonstrate a preference for visiting the flowers of weedy plants on
disturbed sites (Goulson, 2003a; Roubik, 1983; Thorp, 1996) and accordingly can be less likely to pollinate native plant species. Effects of introduced
Africanized honey bees on populations of native stingless bees in Central
America have been reported by Roubik (1978, 1980). Those studies indicate
that the potential of a nonnative pollinator species to affect native populations must be considered before introduction.
Habitat Losses for Insect Pollinators
Habitat alteration, fragmentation, and loss pose major problems for
populations of many organisms, and pollinator populations are no exception (Kearns and Inouye, 1997; Kevan, 2001; Kevan et al., 1990). Bees
and other insect pollinators require nesting sites (suitable soil, dead wood,
abandoned mouse nests, burrows) and floral resources (nectar and pollen) to
persist. These environmental resources are at risk through disruption caused
by row-crop agriculture, grazing, and fragmentation of habitat into patches
too small to support diverse communities of pollinators (Kearns et al., 1998;
Kevan, 1999, 2001; Kevan et al., 1990). Changes in agriculture, caused by
large plantings of monocultures, loss of field margins, abandonment of crop
rotation involving legumes (which have been replaced by fertilizers), and
lower diversity of weeds in fields and pastures (caused by herbicide use) are
all detrimental to pollinator populations (Goulson, 2003b; Kevan, 1999;
Kevan et al., 1990). The loss of flower-rich grasslands, and in particular the
long-tubed flowers in the Fabaceae, seems to underlie the decline of at least
three previously common bumble bee species in England (Goulson et al.,
2005). Grazing can disrupt ground-nesting bees, affect availability of water
(for nest construction) and nectar, and decrease the diversity and abundance
of floral resources (Gess and Gess, 1993; Vinson et al., 1993). Fragmentation makes it more difficult for pollinators to maintain metapopulation
structures, decreasing the availability of corridors and source populations
for recolonization. Bumble bees seem particularly susceptible to such effects,

94
and more than half of the species in the United Kingdom are either already
extinct or could face extinction in the next few decades (Goulson, 2003c).
The apparent loss of two species in the United States in the past few years
suggests that North American bumble bees are similarly imperiled as a result of the combined effects of numerous anthropogenic factors, including
habitat loss, degradation, conversion, pesticide use, pollution, and pathogen
spillover from commercial bumble bee cultures (Thorp, 2003, 2005).
The urbanization of many pollinator habitats also can have unintended,
detrimental consequences. Pollinator populations can be reduced by exposure to city lights and other artificial light sources, including bug zappers
(Frick and Tallamy, 1996), and by traffic on roadways (McKenna et al.,
2001). Some researchers, however, report positive effects of urban or suburban growth on selected bee species when floral resources and nest sites
are available (Cane et al., 2006; Frankie et al., 2005).
A decline in habitat quality can occur even if the overall diversity of
vegetation is static or increases; floral composition is key to determining
suitability. Rasmont and colleagues (2006) suggested that the loss of predominantly longer-tongued bee taxa in Belgium and France is the result of
a loss of floral resources, especially plants with long corollas (Fabaceae, Lamiaceae, Scrophulariaceae, Boraginaceae). They also concluded that anthropogenic disturbancesexcessive mowing of embankments, road sides, and
public areascould have led to the loss of floral hosts and their specialized
bee pollinators. They further hypothesized that decreases in native, solitary,
ground-nesting bees could have been caused by afforestation and the negative effects of poisoning or the sublethal effects of exposure to insecticides,
fungicides, and herbicides. Afforestation occurred on chalky dry grasslands
(prime bee habitats), especially in the Namur province, where habitats have
been converted to pine plantations or housing. Bees and other pollinators
can survive in urban or suburban settings if nesting sites are available and if
there is appropriate floral diversity to provide nectar and pollen throughout
the growing season (Cane et al., 2006; Frankie et al., 2005).
Invasive Plant Species and Bees
The literature on biological control is rife with accounts of accidental or
even deliberate introduction of plants that have become noxious weeds. In
North America, exotic grasses accidentally introduced or grown as livestock
fodder are spreading rapidly (DAntonio and Vitousek, 1992; Larson et al.,
2001; Zavaleta et al., 2001). Exotic grasses, such as red brome (Bromus
madritensis) and buffel grass (Cenchrus ciliaris) in the southwestern United
States and northern Mexico, are rapidly choking out other plants, decreasing nectar and pollen-producing wildflowers, and providing fuel for intense
wildfires. Because buffel grass and other highly invasive grasses cover bare

95
ground, they provide optimal nesting sites for ground-nesting solitary bees
(Buchmann, 1996), but such benefits could be outweighed by elevated risks
of wildfires and by reductions in available forage species (Asner et al., 2004;
Daehler, 2003).
Bee Genetics and Diploid Males: An Extinction Vortex?
Like the entire order of Hymenoptera, bees exhibit haplodiploidy, in
which males develop from unfertilized eggs while females are derived from
fertilized eggs. The genetic basis of sex determination in haplodiploid species appears to be diverse (Bull, 1983; Cook, 1993). In some hymenopteran
insects, including bees, a complementary sex-determining mechanism is
present (Cook, 1993). Females develop when the alleles at the sex determining locus are different (heterozygous). Unfertilized eggs develop into males
because they are hemizygous at this locus. And diploid males, which are
not viable, arise when the alleles at the sex-determining locus are the same
(homozygous). The gene for complementary sex determination (csd) has
recently been identified in honey bees (Beye et al., 2003), providing strong
molecular support for understanding complementary sex determination.
A recent theoretical analysis suggests that complementary sex determination could be a risk factor for the decline, and even extinction, of bee
pollinators (Zayed and Packer, 2005). Zayed and Packer (2005) developed
a stochastic mathematical model that predicts that if population sizes decrease (because of other intrinsic or extrinsic factors, such as those discussed
above), the frequency of diploid males will increase because of inbreeding
and the loss of heterozygosity at the csd locus. According to this model,
the increase in diploid males leads to inbreeding depression, reducing the
effective breeding size of a population and decreasing the production of
females, thus further depressing populations. Thus, under some conditions,
single-locus complementary sex determination can create substantial genetic
load.
Support for the extinction vortex hypothesis currently is limited.
Zayed and Packer (2001) estimated the frequency of diploid drones could
be as high as 50 percent in small populations of the primitively eusocial
bee Halictus poeyi in central and south Florida, much higher than earlier estimates by Kukuk (1989) of 2 to 14 percent. Hedrick et al. (2006)
suggested that the deleterious effects of low variation at the csd locus in
Hymenoptera might be stronger than for self-incompatibility genes or Major
Histocompatability Complex genes; these loci are generally thought to be
particularly important in the population dynamics of plants and vertebrates,
respectively. The extinction vortex hypothesis is noteworthy because prior to
its development, haplodiploid organisms were thought to be relatively less
sensitive to genetic factors that can cause population declines, such as the

96
founder effect (the effect of establishing a new population by a small number

of individuals, carrying only a small fraction of the original populations
genetic variation), the Allee effect (the positive effect of population density
on population growth rate), genetic drift, and deleterious mutations (Hartl
and Clark, 1997) because deleterious alleles have a higher probability of
being purged in haploid males. But the extinction vortex hypothesis predicts
that haplodiploid species with particularly small populations, and thus
fewer alleles at csd, are particularly at risk (Hedrick et al., 2006). Solitary
Hymenoptera have lower fecundity and population sizes than do eusocial
species. This novel hypothesis in pollination conservation genetics deserves
serious examination (Zayed and Packer, 2005).
Transgenic Crops and Butterflies
Concerns about transgenic crops and nontarget species have been studied most extensively for butterflies, with a particular focus on the influence
of Bt corn. Initial genetic transformations of corn (Zea mays) used Bacillus thuringiensis (Bt) endotoxins, specifically Cry1ab, Cry1ac, or Cry9c, for
control of the European corn borer, Ostrinia nubilalis (Minorsky, 2001).
Before the 1996 release of Bt corn, most industry testing focused on nontarget predators and the honey bee, all of which are taxa not expected to
be affected by the Lepidoptera-specific toxins (Malone and Pham-Delgue,
2001; OCallaghan et al., 2005). By 1999, more than 20 million acres (9.6
million hectares) of Bt corn had been planted in the United Statesmore
than 20 percent of all corn acreage (NRC, 2000)and concerns over consequences to nontarget organisms had increased.
In a small-scale laboratory bioassay, Losey and colleagues (1999)
demonstrated that larvae of the monarch butterfly (Danaus plexippus)
experienced substantial mortality after ingesting Bt corn pollen. Partly
because of the iconic nature of the monarch butterflyits striking appearance and thousand-mile migration to a narrow range of overwintering sites
led to its designation as the state insect in Alabama, Idaho, Illinois, Texas,
West Virginia, and Minnesota (http://www.adver-net.com/states.html)the
discovery of the potential for damage caused by Bt corn led to widespread
public alarm (Berenbaum, 2001). The dramatic increase in acreage of
transgenic corn between 1996 and 2000 notwithstanding, no documentation of declines in monarch populations, either in the midwestern United
States, where much of the nations transgenic corn was planted, or in the
overwintering sites was reported (see Chapter 2). The implications of the
work of Losey and colleagues (1999) were questioned for natural populations (Shelton and Rousch, 1999).
Concern in the scientific community and among the public at large
prompted multiple studies to estimate risks associated with monarch butter

97
fly exposure to corn pollen and to quantify the effects of pollen ingestion
(Hellmich et al., 2001; Oberhauser et al., 2001; Pleasants et al., 2001;
Sears et al., 2001; Stanley-Horn et al., 2001; Zangerl et al., 2001). Collectively, the work showed that the asclepiaceous host plants of D. plexippus
are found in cornfields throughout much of eastern North America, so
D. plexippus is in fact potentially vulnerable to the consequences of exposure to Bt corn pollen. Despite the proximity of monarchs to transgenic
corn pollen, however, the risks of adverse effects are low. A combination of
factors provides protection: selection for particular genetic transformations
of corn (Hellmich et al., 2001; Zangerl et al., 2001), caterpillar behavior
(Anderson et al., 2005), lack of pollen persistence (Pleasants et al., 2001),
and phenological displacement (Bartholomew and Yeargan, 2001). Sears
and colleagues (2001) conducted a risk assessment on the basis of available
laboratory and field data and they concluded that an adoption rate of the
demonstrably less harmful Bt corn transformations of 80 percent of the
total corn crop would place only 0.05 percent of the monarch population
at risk. This estimated risk is substantially lower than the risk presented by
pesticides conventionally used for control of European corn borer (StanleyHorn et al., 2001).
Although the public focus on nontarget effects of genetically modified
corn originated with the report on monarchs (Losey et al., 1999), other
studies have estimated negligible nontarget effects for a few other Lepidoptera: Papilio polyxenes, the black swallowtail (Wraight et al., 2000), and
Euchaetes egle, the milkweed tussock caterpillar (Jesse and Obrycki, 2002).
Laboratory and field studies of Bt corn on other continents (Li et al., 2005)
also failed to demonstrate damage to a nontarget lepidopteran, Antheraea
pernyi, which is used as a natural silk source (Li et al., 2005).
Transgenic crops could pose secondary reasons for concern for pollinators, in the form of genetically modified, herbicide-tolerant (GMHT)
crops. Weeds in agricultural monocultures can be important host plants for
lepidopteran pollinators (milkweed for monarch butterflies; Oberhauser
et al., 2001) and nectar or pollen resources for a variety of pollinator species. They can provide resources for more of the growing season than does
the crop, and they attract pollinators that the crop does not (for example,
long-tubed corollas for long-tongued pollinators). Evidence for this effect
is provided by the British Farmscale Study, a 5-year project that assessed
the effects of farm management of GMHT crops on farmland biodiversity
relative to conventional agriculture. Heard and colleagues (2003) reported
that weed populations were reduced in most (but not all) fields of GMHT
crops, and Haughton and co-workers (2003) reported reduced abundances
of butterflies in transgenic beet and spring canola fields and smaller numbers
of bees in transgenic beet fields compared with non-GMHT crops. In field
margins, butterfly numbers were lower by 24 percent adjacent to transgenic

98
spring canola (Roy et al., 2003). In general, pollinator numbers reflected

nectar source abundance (Hawes et al., 2003). Whether the reduced abundances in the field could lead to reduced pollinator populations over time
would depend on the proportion of GMHT crops within the foraging ranges
of these insects. Moreover, it is not known whether those findings are applicable to agroecosystems outside of Britain.
Habitat Destruction and Bats
Bats face important extinction threats (Chapter 2). Mickleburgh and
colleagues (2002) reported that 11 bat species have become extinct in the
past 400 years, 65 are either critically endangered or endangered, and 177
more are vulnerable to extinction, according to the criteria of the World
Conservation Union (Mickleburgh et al., 2002). The 242 bat species represent about 24 percent of the worlds total number of bat species, a proportion that is consistent with the 25 percent of the mammals of the world
considered at risk of extinction (IUCN, 1996).
The loss of bat populations is mostly the result of habitat destruction,
especially of roosting sites in caves. About half of Mexicos 140 bat species
(Arita, 1993; Medelln et al., 1997) and half of the United States 45 species
(Pierson, 1998) roost in caves. Among nectar-feeding bats (12 species in
Mexico and the United States), only two do not use caves as roosts (Arita,
1993). The others, including the three migratory species with seasonal
ranges in the United States, rely on caves to some extent. Bats spend more
than half of their time roosting in caves (Kunz, 1982) and they attain high
numbers in cave environments (Tuttle, 2000), so the destruction of caves
is a significant threat to bats (Medelln, 2003). Severe declines of cave bat
populations have been documented in Mexico and elsewhere (Hutson et al.,
2001; Medelln, 2003; Moreno, 1997).
The most common causes for the destruction of cave-dwelling bat populations involve misguided attempts to control the vampire bat (Desmodus
rotundus), vandalism such as setting fires in caves, disturbance during critical times such as birth peaks, and persecution of such mythical creatures
as the chupacabras (Arita and Santos-del-Prado, 1999; Medelln, 2003).
These causes are linked to a lack of understanding of the bats ecological
purposes and economic benefits (Medelln et al., 2004).
Habitat destruction also threatens migratory pollinivorous bats. Species
that migrate seasonally (Arita and Santos-del-Prado, 1999; Medelln et al.,
2004; Wilkinson and Fleming, 1996) need a nectar trail or corridor along
their migratory route (Allen-Wardell et al., 1998; Buchmann and Nabhan,
Mythical
creature said to inhabit part of the Americas (particularly in Puerto Rico) and to
attack and drink blood of livestock.

99
1996; Fleming et al., 1993; Nabhan et al., 2004) that is continuous and
sufficiently conserved to provide the bats with resources. Natural habitats
have been destroyed or fragmented along the migratory corridors of western Mexico and other areas (Valiente-Banuet, 2002), but it is not known
whether the destruction is damaging bat populations.
Some nectar-feeding bats are habitat specialists that could depend
largely on the availability of intact dry tropical forest for survival (Quesada
et al., 2003). That group includes nectarivorous bats with restricted distributions, such as the Mexican banana bat (Musonycteris harrisoni) and the
Moreno long-tongued bat (Glossophaga morenoi). The bats inhabit the dry
tropical forest of western Mexico, a region that has experienced considerable deforestation and fragmentation (Trejo and Dirzo, 2000). Declines in
their populations could affect the reproductive biology of their food plants
(Quesada et al., 2003).
Habitat Changes and Hummingbirds
Most studies of threats to landbirds have focused on nonhummingbird
species (for example, Rappole and McDonald, 1994; Robbins et al., 1989),
partly because no hummingbird is included on the U.S. Endangered Species
Act list. Migratory bird species (including some pollinating species) show
declines that have been linked to deforestation and forest fragmentation in
the tropical wintering ranges of those species (Robbins et al., 1989). The
Audubon Societys WatchList (http://www.audubon.org/bird/watch/) has
six species of hummingbird identified by Partners in Flight at the national
level as moderately high or moderate priority: the Allen (Selasphorus sasin),
buff-bellied (Amazilia yucatanensis), calliope (Stellula calliope), Costa
(Calypte costae), lucifer (Calothorax lucifer), and rufous (Selasphorus rufus)
hummingbirds. Threats listed for the six species on the WatchList include
habitat destruction that results from human encroachment (urbanization,
agriculture, conversion of grasslands for cattle ranching). Another important identified threat is the replacement of native plants by invasive species
that are unproductive for hummingbirds.
Calder (2004) identified the destruction of stopover habitatconsidered
critical to migrationalong the migratory corridors as a cause of population
decline. He also identified habitat destruction attributable to the invasion of
African exotic buffel grass, which could damage Sonoran Desert vegetation
(Burquez and Martnez-Yrzar, 1997). Abnormal weather, primarily cold
winters or drought along desert migratory corridors, also could pose an
important threat to hummingbirds (Calder, 2004). After one particularly
cold winter (19571958), Bailey and Niedrach (1965) reported that less
than one-fourth of the 1957 population of broad-tailed hummingbirds reap-

100
peared in 1958 and 1959. After another unusually cold winter in 1995, the
population declined by an estimated 57 percent (Calder, 2004).
At least 7 (5 threatened, 2 endangered) of the 23 hummingbird species
are shown on the Mexican list of species at risk of extinction (SEMARNAT, 2002). These seven species were Campylopterus excellens, Lophornis
brachylopha, Thalurania ridgwayi, Hylocharis xanthusii, Eupherusa
cyanophrys, Amazilia viridifrons, and Eupherusa poliocerca (Ornelas,
2000). All face similar threats: they have restricted distributions (all seven
are endemic to small areas in the south, west, or northwest of Mexico) and
all have experienced severe habitat destruction or fragmentation caused by
conversion of grasslands to use for cattle ranching or agriculture. Urban or
suburban domestic cats that are allowed outside have been implicated in
mortality of ruby-throated hummingbirds, a species of conservation concern
in some parts of its range (Lepczyk et al., 2004).
One threat is associated only with the (primarily Mexican) lucifer hummingbird: trade in individuals in past decades (although confirmation is
lacking) (http://audubon2.org/webapp/watchlist/viewSpecies.jsp?id=127),
which is likely to have affected several other species. It is not known whether
the hummingbird trade continues to be a factor of concern.
Climate Change
Global, regional, and local climate changes can alter or disrupt plantpollinator relationships. Included in the global climate change forecast are
shifts in temperature and precipitation, concentrations of carbon dioxide
(CO2) and ozone, and ultraviolet light levels. All are important to plant
growth and flowering, and those changes could alter plant and pollinator
phenology and distribution along altitudinal and latitudinal gradients, generate changes in plant and pollinator mutualisms and community compositions, and cause local extinctions.
There is evidence that the latitudinal and altitudinal ranges of some
plants and pollinators have changed in the past 30 years, presumably in
response to global warming (Walther, 2004). For example, some butterflies
in Britain and North America have expanded ranges north (Crozier, 2003;
Hill et al., 1999; Parmesan et al., 1999), and others in Montana (Lesica and
McCune, 2004), Spain (Wilson et al., 2005), and Norway (Klanderud and
Birks, 2003) have contracted ranges at lower altitudes and latitudes.
An increase in atmospheric CO2 could alter production of nectar
(reviewed by Davis, 2003). Typically, elevated CO2 concentrations alter
nectar volume and secretion rate, sometimes negatively and sometimes
positively, but not sugar concentration or composition (for example, Lake
and Hughes, 1999). Increases in CO2 could benefit at least one species of

101
melon (Cucumis melo). Average nectar volumes per flower were significantly
higher, sometimes by as much as 100 percent (Dag and Eisikowitch, 2000),
in greenhouses enriched with CO2. No comparable greenhouse or field
studies seem to have addressed the potential for CO2 enrichment to affect
pollen production.
Elevated intensities of ultraviolet-B radiation (UV-B; wavelengths between 280 and 320 nanometers) result from diminished concentrations of
atmospheric ozone and can delay flowering and diminish lifetime flower
production in some plants. Sampson and Cane (1999) reported idiosyncratic
responses in flowering phenology and flower production in two annual
plants, traits that could affect plant competition for pollinator services,
and plant and pollinator reproductive success. Stephanou and colleagues
(2000) reported that UV-B increased nectary size in another species, which
apparently resulted in an observed increase in pollination, but no differences
were reported in honey bee foraging behavior on brassicaceous nectar plants
exposed to and protected from UV-B (Collins et al., 1997).
In the Washington, D.C. area, Abu-Asab and colleagues (2001) reported that 89 plant species had advanced flowering time by an average of
4.5 days (although 11 species showed later flowering times). Primack and
colleagues (2004) used herbarium specimens of the same individual plants
in the Arnold Arboretum in Boston, Massachusetts, to compare flowering
times from 1885 to 2002. Plants flowered 8 days earlier from 1980 to 2002
than they did from 1900 to 1920. Flowering by agricultural species also is
influenced by global warming: a 40-year study of white clover (Trifolium
repens) revealed that flowering has advanced by 7.5 days per decade since
1978 (Williams and Abberton, 2004).
Several studies demonstrate that pollinator phenology can be influenced
by changing global temperatures. The first appearance of most British butterflies has advanced in the past two decades; peak appearance also occurs
earlier, and multibrooded species exhibit longer flight periods (Roy and
Sparks, 2000). Forister and Shapiro (2003) documented a similar change
in California butterflies. The mean date of first flight trended toward earlier dates for 16 species (70 percent of the fauna studied), and the trend
was statistically significant for 4 of them (average shift of 24 days). Seven
species showed trends toward later appearance that were not statistically
significant. Some Spanish butterflies (8 of 19 species studied from 1988 to
2002) also showed significant advances in mean flight dates (Stefanescu
et al., 2003).
If the phenology of flowering and pollinator activities does not change
synchronously, there is the potential for disruption of coordinated interactions. Plants might flower before or after the period of seasonal activity of
their pollinators and different groups of pollinators might respond differ-

102
ently to a change in temperature. A record-early spring in Japan resulted in

drastic decreases in seed set of two species normally pollinated by bees, but
not in two others pollinated by flies (Kudo et al., 2004). A long-term study
of life cycles of Mediterranean plants and animals showed that the phenology of plant leafing out, flowering, and fruiting changed at different rates,
and all were different from changes recorded for butterfly emergence and
the arrival of migratory birds (Peuelas et al., 2002). The authors suggested
that these changes could alter ecosystem structure and function. Migrating
pollinators (for example, hummingbirds that overwinter in Mexico and reproduce in the United States) depend on corridors with flowers that bloom
at the appropriate times during spring and fall migrations. If the timing of
the migration does not coincide with flowering, the plants could suffer a
loss of pollinators and the pollinators could face energetically expensive
migratory flights with no opportunity to forage and replenish metabolic
fuel along the way.
Thus, the evidence indicates that plants and their pollinators could
respond differentially to climate change. Depending on the degree of variations in their responses, the consequences of climate change could range
from subtle to dramatic. Alterations in nectar abundance or concentration
could change the foraging behavior of pollinators, increasing or decreasing pollination of one flower by another of the same plant (geitonogamy);
changing the quantities of pollen collected or deposited or the distances
that pollen is transportedall can have significant effects on plant mating
systems and genetic parameters. Changes in floral abundance could in turn
influence the abundance and distribution of pollinators. The loss of synchrony that could result from differential responses in phenology of plants
and pollinators could be important and possibly result in the loss of some
historical mutualisms or the creation of new ones. It appears that this area of
research warrants more attention, in view of the potential for climate change
to disrupt plant-pollinator interactions significantly in the future.
The combined effects of climate change and other environmental
changes (such as habitat fragmentation) have not been assessed for most
pollination systems, but Warren and colleagues (2001) reported that 34 of
46 British butterfly species that might be expected to respond positively to
climate warming at their northern climatic range margins in fact declined,
as negative consequences of habitat loss outweighed the positive responses
to climate warming over the past 30 years. Although half of the habitat generalists that also were mobile species increased their distributions, the other
generalists and 89 percent of the habitat specialists declined in distribution,
suggesting that the diversity of pollinators could decline substantially in
the face of the combined pressures of climate change and habitat loss. The
potent combination of environmental changes could cause substantial harm
to many plant-pollinator interactions.

103
CONCLUSIONS
Just as different species of pollinators differ in the degree to which their
diversity and populations have declined, the causes that underlie decline
vary widely. Some mortality is particularly important in a narrow range of
pollinators; in managed pollination systems, there is clear evidence of reductions in pollinator numbers caused by introduced parasites and pathogens.
The evidence indicates that these agents of mortality also could operate in
wild pollinator declines. Other causes of mortality affect a cross-section
of pollinators (albeit to different extents); habitat degradation and habitat
loss, in their many manifestations, have contributed to declines in many
vertebrate and invertebrate pollinators.

4
Effects of Variations in Pollinator
Populations on Pollination Services
Because pollinators provide essential ecosystem services in agricultural

and natural areas, it is valuable to determine whether pollination services are
threatened by their declining populations. Many plant species rely on pollinators for sexual reproduction, but whether a global pollination crisis is
jeopardizing food supplies or wild biodiversity has been debated (Buchmann
and Nabhan, 1996; Ghazoul, 2005a,b; Potts et al., 2005; Steffan-Dewenter
et al., 2005). Chapter 2 noted that a pollinator shortage exists when the
demand for pollination services exceeds available pollinator capacity. Shortages can be exacerbated by pollinator declines, but they can arise even when
pollinator populations are stable or increasing over time. Some shortages,
for example, those caused by the high seasonal demands of the California
almond industry for honey bee colonies (for example, Norton, 2005), can
be moderated by market forces, like the economics of supply and demand.
In contrast, chronic and continuing pollinator declines could threaten the
basic ecosystem services that many people take for granted. In the study of
consequences for pollination and ecosystem services, it is useful to distinguish between transient pollinator shortages and declines.
POLLINATORS IN AGRICULTURE
Food Security and Nutrition
An evaluation of experimental evidence for pollination requirements
of 107 globally traded fruit and vegetable crops (representing 40 percent
of global plant-based food production) by Klein et al. (2007) shows that
104

VARIATIONS IN POPULATIONS ON POLLINATION SERVICES
105
animal pollination improves production in 75 percent of the crops studied.

Most cultivars of another 10 percent of the crops require animal pollination.
Another 8.5 percent of the crops do not benefit from animal pollination
and its role in production of the remaining 6.5 percent crops is not known.
Many crops, howevernotably the staple grains that form the foundation
of most human diets (rice, wheat, maize, sorghums, millets, rye, barley)are
self-pollinating or pollinated by the wind. Together, species that do not
rely on pollinators account for most of the worlds food supply by weight
(FAO, 2005).
Pollinator declines, therefore, do not fundamentally threaten the worlds
caloric supplies. However, fruits and vegetables, which add diversity to the
human diet and provide essential nutrients, tend to depend heavily on pollinators (Prescott-Allen and Prescott-Allen, 1990; Roubik, 1995). Seven of the
nine crops that provide at least 50 percent of the vitamin C available to the
human diet globally depend partially or entirely on animal pollination for
the production of fruits or seeds (oranges, cabbages, green peppers, tomatoes, melons, tangerines, watermelon) (FAO, 2005; Free, 1993; McGregor,
1976; USDA-NASS, 2006b).
Animal-pollinated crops also tend to have greater economic value than
do crops that are not animal-pollinated, and they provide relatively more
income to farmers per unit of land (USDA-NASS, 2006b). Moreover, several
oilseed crops depend on pollinators, and bee pollination is required to produce the seeds of major forage and hay crops, such as alfalfa and clover,
that feed the animals that supply meat and dairy products. Thus, despite the
fact that they do not provide the bulk of the human diet, animal-pollinated
plants contribute importantly to the quality of the human diet. Although
estimates of the proportion of the human diet that is attributable to animal
pollination are occasionally attempted and frequently cited (for example,
McGregors 1976 estimate that one-third of the human diet can be traced
directly or indirectly to animal pollination), the proportion likely varies
among countries and regions and depends on dietary preferences, seasonal
availability, cultural practices, and economic status of consumers.
Major Crops
Plant species grown as agricultural commodities display a wide variety
of breeding systems. Some readily self-pollinate; others are dioecious, monoecious, or self-incompatible and require animal pollination (Free, 1993;
McGregor, 1976; Table 4-1). Dependence on pollinators also varies greatly
among crops. In the United States, about 130 agricultural crops benefit from
insect pollination (McGregor 1976; see examples in Table 4-1). Most North
American crops can produce some fruits and seeds without animal pollination, but pollination often increases their value through higher yields or im-

106
TABLE 4-1 Value of Common Crops That Require or Benefit from Insect
Pollination
Commodity
Bearing
Acres
Production
Unit
Utilized Production
(thousand units)
Value of
Utilized Production
($ thousand U.S.)
Apple
Blueberry, cultivated
Blueberry, wild
Cranberry
Cherry, sweet
Cucumber, fresh
Melon, cantaloupe
Melon, watermelon
Nut, almond
Peach
Pear
Squash, all
395,000
41,720
NA
39,600
73,940
58,600
86,000
149,600
550,000
145,530
64,150
50,700
Ton
Ton
Ton
Ton
Ton
Hundredweight
Hundredweight
Hundredweight
Ton
Ton
Ton
Hundredweight
4,261.6
94.4
40.2
309.2
246.8
55,000.0
22,107.0
38,208.0
833.3
1,205.1
922.5
7,685.0
1,783,952
221,610
28,540
208,025
344,471
187,391
371,721
342,918
1,600,144
454,532
270,385
197,020
SOURCE: Data from NASS Non-citrus Fruits and Nuts 2003 Summary.
proved quality (Klein et al., 2007). Coffee self-pollinates, but yields increase
as a result of pollinator visits (Klein et al., 2003a,b,c; Ricketts et al., 2004;
Roubik, 2002). A few U.S. cropsmelons, cucurbit squashes, almond, and
most pome fruitsare completely dependent on animal pollination to set
fruit. Crops with many-seeded fruits, such as watermelon, pumpkin, and
kiwi, have hundreds of ovules so they require many pollen grains per stigma.
Thus, they are more susceptible to pollinator shortages than are those with
few seeds per fruit (Free, 1993; Stanghellini et al., 1997).
In a detailed 1976 report, Insect Pollination of Cultivated Crop Plants,
published by the U.S. Departmnent of Agriculture, McGregor (p. iv) noted
that the pollination of plants, essential in the perpetuation of most species,
is so unobtrusively accomplished that it is often overlooked. Although
pollinators are critical to many agroecosystems, their importance varies
not only among crop species but even among varieties of the same crop.
In addition, wild-pollinator abundances can fluctuate dramatically among
locations and over time (Kremen et al., 2002b; Price et al., 2005). Reliable
data on the specific contributions of pollinators to crop yields are often lacking, and obtaining this information requires large-scale, long-term studies.
Listed in Table 4-1 are the relative area and value of several major crops
known to benefit from pollinators. Because managed honey bees are often
used to pollinate them, the extent to which managed and unmanaged pollinators provide adequate pollination service for optimal yields remains for
the most part undetermined.

107
Managed and Wild Crop Pollinators

Crop plants in North America are pollinated by many wild or managed
native species of animals, in addition to managed colonies of introduced
honey bees (Apis mellifera). The wild species include native bees, feral honey
bees, other insects, birds, and bats (Free, 1993; Chapter 2). For some crops,
one or more wild species could be more efficient than honey bees, although
honey bees also might contribute to pollination (Free, 1993). Blueberry,
cranberry, and kiwi are buzz-pollinateda visiting bee vibrates its body
to sonicate the pollen grains out of the flowers anthers. Bumble bees (Bombus spp.) and some other native bees are much more efficient blueberry pollinators than are honey bees because they buzz-pollinate (Buchman, 1983;
Cane and Payne, 1990; Javorek et al., 2002; MacKenzie, 1997; MacKenzie
et al., 1996), whereas honey bees cannot. However, honey bees are used
to pollinate wild blueberries because apiculture is well developed. Even in
crops that are routinely pollinated by managed honey bees, wild pollinators
also can contribute pollination services. Watermelon growers in California
use managed honey bees, but their crops also receive substantial pollination
from a diverse community of native bees (Kremen et al., 2002a).
The adequacy of pollination services provided by managed and wild
pollinators, including feral honey bees, can vary widely and is poorly documented for many crops (Free, 1993). Greenleaf and Kremen (2006b) studied
field-grown tomatoes for which growers did not import honey bee colonies.
They found that native bees (such as Anthophora spp. and Bombus spp.)
were buzz-pollinating the crops. Although wild species are either known or
likely to be important pollinators in many crop systems, the relative contributions of different groups of pollinators to crop yields are rarely defined.
With such a paucity of relevant research, it is useful to review evidence
from a sample of well-studied crops to evaluate the availability and importance of wild pollinators. For these exemplars, pollinator shortages often
can be overcome by providing sufficient numbers of managed pollinators,
especially honey bees, although in a few cases the crop production depends
completely on specific pollinators (for example, midges or bats).
Watermelon
Watermelon (Citrullus lanatus) is grown in several parts of the United
States and Mexico. U.S. production in 2005 was worth $410 million (USDANASS, 2006b). Because watermelon has separate male and female flowers,
animal pollination is critical. Watermelon pollination requirements are high:
5001,000 pollen grains must be deposited on stigmas to produce marketable fruits (Adlerz, 1966; McGregor, 1976), so the plant relies on multiple
insect visits to each female flower for successful pollination (Stanghellini et
al., 1997). In most areas of cultivation within North America, pollination

108
is provided by managed honey bees and a diverse set of native bee species
(Kremen et al., 2002a).
In the central valley of California, Kremen and colleagues (2002a)
measured pollination at 14 watermelon farms that differed in degree of
isolation from natural habitat. At farms near natural habitat, the native bee
community was sufficient to provide adequate pollination. At farms far from
natural habitat, however, average pollen deposition by native bees alone
was insufficient. The inadequacy was the result of a reduction in overall
pollinator abundance and of local extinction of the most efficient pollinators
(Kremen et al., 2004; Larsen et al., 2005).
Blueberry
Blueberries (Vaccinium spp.) grow in several Canadian provinces and in
several U.S. states. High-bush blueberries are actively cultivated; low-bush
blueberries are harvested from semicultivated wild plants. In the United
States, about 44,000 acres (17,800 hectares) of high-bush blueberries are
planted to produce a crop worth more than $275 million annually (USDANASS, 2006b). Like many other species in their family, blueberries are
buzz-pollinated, primarily by bumble bees (Buchmann, 1983; Free, 1993).
Introduced honey bees do not buzz-pollinate, so high-bush blueberries
depend largely on native wild bees for pollination (Buchmann, 1983; Free,
1993; MacKenzie, 1997; MacKenzie et al., 1996).
Several research groups have investigated the dependence of blueberry
production on wild bees. Cane and Payne (1988), for example, listed four
species of wild bumble bee (Bombus spp.) and the anthophorine Habropoda
laboriosa that buzz-pollinate high-bush blueberry fields in Alabama and
Georgia. Honey bees from colonies at field borders were found to carry
little or no blueberry pollen. In New Brunswick, Canada, pesticide applications in nearby forests were followed by devastating reductions in native
populations of bumble bees, andrenid bees, and halictid bees, which might
have contributed to a severe drop in low-bush blueberry production (Kevan,
1975b). When a less harmful insecticide was introduced, native bees appeared to recover (Kevan et al., 1997), and production returned to normal
(Kevan and Plowright, 1995). These findings highlight both the dependence
of the crop on wild pollinators and the interconnectedness of contiguous
natural and cultivated habitats.
Sunflower
Sunflowers are grown throughout the world for oil and confection seed,
and in 2005, 2.7 million acres were under production in North America,
mostly in the United States (FAO, 2005). Sunflower, Helianthus annuus,

109
is a widely distributed native plant in North America, visited by many of

its native pollinator species, including some bee species that specialize on
sunflower pollen (for example, Svastra obliqua). Unlike the sunflower, many
crops are grown outside their native ranges and therefore are visited by
novel pollinators. The sunflower head consists of many individual florets,
each of which passes first through a male stage and then a female stage
(Free, 1993). Although the plant is self-compatible, bees often increase
sunflower seed set by moving pollen from male-stage florets to female-stage
florets within the same flower head and through cross-pollination between
individual plants (Greenleaf, 2005; Greenleaf and Kremen, 2006b). Most
sunflower varieties are sold as hybrid seeds, which require cross-pollination
between pollen-producing lines and those that lack pollen. The hybrid sunflower seed production industry is worth $26 million annually in the United
States (Greenleaf, 2005), and more than 90 percent of seed production occurs in northern California (Lilleboe, 2000).
Several studies have documented improvements in sunflower seed production as a result of insect pollination, although the degree of improvement
varies among cultivars. For example, seed set on flower heads increased
from 1 to 35 percent when bees provided self-pollination, transferring
pollen among florets; when bees moved pollen between florets on different
sunflower heads, seed set increased to 63 percent (Free, 1993). Although
managed honey bee hives are stocked in hybrid sunflower fields in the United
States, non-Apis bees also pollinate hybrid sunflowers and might do so far
more efficiently than honey bees (DeGrandi-Hoffman and Watkins, 2000;
Greenleaf, 2005; Parker, 1981). Non-Apis bee interactions with honey bees
increase the pollination efficiency on hybrid sunflower by as much as five
times, by disturbing them as they forage on florets and causing them to
move among plants more often and cross-pollinate plants more effectively
(Greenleaf, 2005). From those findings, Greenleaf (2005) calculated that the
direct pollination provided by wild bees nationally to the hybrid sunflower
seed industry was worth $1.9 million, the interspecific interaction between
wild and honey bees was worth $10.4 million, and the direct contribution of
honey bees was worth $13.8 million. Both proximity to natural habitat and
crop rotation practices affect the amount of sunflower pollination provided
by wild bees (Greenleaf, 2005; Greenleaf and Kremen, 2006b).
Canola
Canola is Canadas fourth largest crop in terms of area under cultivation, and annual exports are currently worth more than $2 billion Canadian (Morandin and Winston, 2005). The two species in the mustard
family grown to produce canola oil, Brassica napus and B. rapa, differ in
dependence on pollinators. B. napus is self-compatible, but some cultivars

110
produce better yield with cross-pollination (Kevan and Eisikowitch, 1990).

In contrast, B. rapa is self-incompatible and therefore requires pollinators
for seed set. Although managed honey bees are used, many native species
also pollinate canola crops (Morandin and Winston, 2005).
Morandin and Winston (2005) studied pollination of self-incompatible
canola in Alberta, Canada, and compared results from fields with different
management regimes. They reported that farms with more wild bees also
showed smaller pollination deficits, which were defined as the extent to
which yields were depressed because of insufficient pollination. The farms
with the fewest bees were those planted in genetically modified, herbicideresistant plants. Because those fields were treated heavily with herbicides,
they had a lower diversity and abundance of flowering weeds, which could
account for their reduced capacity to support wild bees. Using those results,
Morandin and Winston (2006) calculated that profits lost by retiring up to
30 percent of the field area from production would be more than offset by
increased yield that would result from better pollination by the more diverse
and abundant pollinators found in fields within 750 meters of uncultivated
areas.
Coffee
Coffee (Coffea arabica and C. robusta) is grown extensively in Mexico
and is one of the developing worlds most valuable export commodities.
Worldwide, 11 million hectares are planted in coffee, and the industry
employs 25 million people (OBrien and Kinnaird, 2003). C. arabica, the
species thought to produce the highest-quality coffee, self-pollinates, but
yields increase 15 to 50 percent when flowers are visited by bees (for example, Free, 1993; Klein et al., 2003b; Roubik, 2002). Despite that, few
coffee farmers recognize pollination as an issue for their crops (Ricketts et
al., unpublished data).
Several recent studies have investigated the importance of wild bees to
coffee production. Ricketts and colleagues (Ricketts, 2004; Ricketts et al.,
2004) reported that in Costa Rica a diverse community of wild bees pollinates coffee. The pollinators were mainly wild Africanized honey bees and
10 species of social stingless bee (tribe Meliponini). The species depend on
forest habitat for nest sites and food resources but flew into nearby coffee
fields when they were in flower. Coffee fields near forest patches received
more visits by a more diverse set of bees and had 20 percent higher yields
than did fields more than 1 km away from a forest. Klein and colleagues
(Klein et al., 2002, 2003c) also noted a diverse community of wild coffee
pollinators in Indonesia. They reported that coffee yields increased with
increased diversity of pollinators and that pollinator diversity increased near
forest remnants and in less intensive farms managed with a more diverse

111
canopy of shade trees. Although these studies were performed outside North
America, their findings are informative for coffee production in Mexico.
Cacao
Chocolate is made from the seeds of the cacao tree (Theobroma cacao),
which is native to the western Amazon basin, but now grown in many
humid tropical regions, including Mexico (Clay, 2004). Cacao trees can be
either self-compatible or self-incompatible, but even self-compatible trees
require insect visits to move pollen from anthers to stigmas and pollinate the
flowers. Honey bees do not appear to be effective pollenators (Free, 1993).
Although the identity of the principal pollinators of cacao eluded growers
and scientists for many years, midges in the family Ceratopogonidae have
been identified as the most important group (Free, 1993; Young, 1985).
Many other wild insects also have been observed visiting cacao (bees in
the subfamilies Halictinae, Meliponinae), but their pollinating efficiency is
either low or undetermined (for example, Young, 1981, 1985).
There is substantial evidence that farm management practices influence
the amount and quality of habitat for midges within and around cacao
farms and therefore can affect yields (Free, 1993). Midges prefer shady,
moist conditions; their eggs are laid and larvae develop in rotting wood and
leaves on the ground (Free, 1993). Young (1982, 1986) showed that adding
pieces of rotting wood to the leaf litter within cacao plantations increased
the abundance of several midge species and that cacao plants near shade
trees or rotting material often had more fruits than did trees that were
farther away.
Agave
Tequilaone of several alcoholic beverages derived from agaveis produced exclusively from Agave tequilana var. azul in select regions of Mexico.
Tequila revenues were close to $1 billion in exports and domestic sales in
2000 (Tequila Aficionado, 2001), and in 1998, Mexico had about 100,000
hectares (about 250,000 acres) containing roughly 200 million plants
(Ramrez, 1998). After 1989, and at least until 2002, the tequila industry
faced major agave shortages caused by several diseases that affected about
30 percent of the plants at different stages of development (Jimnez-Hidalgo
et al., 2004; Larrea-Reynoso, 1998; Valenzuela-Zapata, 1994).
Although many species of agave, including A. tequilana, are naturally
pollinated by bats and other animals (Arizaga et al., 2002; Rocha et al.,
2005), the industry uses only asexually reproduced plants to replenish the
producing population. This practice has prevented outcrossing of individuals
and resulted in loss of genetic diversity compared to other agaves (Dalton,

112
2005). Recent studies have suggested links between the disease outbreaks to
this reduction of genetic diversity (Valenzuela-Zapata and Nabhan, 2004),
and producers are supporting research to find solutions (Dalton, 2005). The
tequila industry very likely would benefit if genetic diversity were maintained and used in various combinations in the fields. Monocultures with
little genetic variation are susceptible to pests and diseases.
Other Crops
Ecologists have investigated a variety of crops, both in North America
and elsewhere, to determine the degree of pollination services provided
by wild bees. Some studies demonstrate extensive pollination by wild pollinators (Roubik, 1993, 1995), whereas others find little support for this
assertion (reviewed in Free, 1993; Klein et al., 2007). Additional studies on
pollination of muskmelon (cantaloupe), almond, and tomato in California,
New Jersey, and elsewhere are under way (Greenleaf and Kremen, 2006a;
Kremen, unpublished data; Williams and Kremen, unpublished data; Winfree et al., 2006). The growing body of research will contribute to elucidating the degree to which wild pollinators benefit agricultural production and,
more important, the circumstances and management regimes that affect
pollination of crops by unmanaged wild pollinators.
Alleviating Pollinator Shortages
Traditional farmers and plant breeders have developed new cultivars
that depend less on pollinators. Cultivated hybrid sunflowers (Helianthus
annuus) self-pollinate even though their insect-pollinated wild ancestors
are self-incompatible (Heiser, 1954). In the early 1900s, strawberries were
developed with hermaphrodite flowers to improve fruit set (McGregor,
1976), although they still benefit from pollinators. Similarly, flowers of wild
tomatoes and some heirloom tomato varieties must be visited by bumble
bees to set fruit. Most cultivated tomatoes can self-pollinate if they are
jostled mechanically (McGregor, 1976), but greenhouse tomatoes typically
are buzz-pollinated by managed bumble bees (Box 3-1). In field production,
some varieties of tomatoes also produce more and larger fruits if they are
visited by bees (Greenleaf and Kremen, 2006a).
Bananas and some varieties of pineapple, grape, citrus, cucumber, and
persimmon can produce fruit without sexual fertilization, a process known
as parthenocarpy. Parthenocarpic fruit production solves problems associated with insufficient numbers of pollinators by bypassing them altogether.
Parthenocarpy can be induced with the use of plant hormones and genetic
modification (Gorguet et al., 2005; Pagnotta, 1999; Rotino et al., 1997).
Mainland and Eck (1968) induced fruit production in blueberries with

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applications of auxin, gibberellin, and kinin, and Hayata and colleagues

(1995) and Maroto and colleagues (2005) used plant regulators to induce
parthenocarpic fruit production in watermelons. In a report that detailed
parthenocarpy induced by genetic modification, Acciarri and colleagues
(2002) reported improved fruit production in eggplant using the DefH9iaaM auxin-synthesizing gene. Donzella and colleagues (2000) reported the
same results. Mezzetti and colleagues (2002a,b, 2004) used the DefH9-iaaM
gene to induce parthenocarpic fruit production in strawberry and raspberry
cultivars. Barg and colleagues (2001) reported successful production of
parthenocarpy in tomato cultivars by use of a chimeric transgene. Conventional and molecular techniques have been used to produce parthenocarpic
cultivars of citrus (Koltunow et al., 2000). The development of additional
parthenocarpic varieties through traditional breeding or recombinant DNA
techniques could expand the number of crops that do not require pollination by animal vectors. Nonetheless, pollinators contribute to maintenance
of plant genetic diversity (see Agave example above) and are important for
breeding programs (such as hybrid or other seed production).
In some cases, the problem of insufficient cross-pollination can be addressed by better planting designs. For example, apples are self-incompatible
and require cross-pollination not only between individuals but also between
cultivars, and movements of honey bees from tree to tree are limited. Using
genetic markers, Kron and colleagues (2001a,b) demonstrated that intercultivar pollen movement by pollinating honey bees in orchards of dwarf
apple was limited to about four neighboring trees. Thus, plantings with too
many rows of the same cultivar produced lower yields. In such a situation,
the efforts of the pollinators (and the money spent by grower) are wasted,
and in essence a pollinator shortage is created unnecessarily. Moreover,
Kron and colleagues (2001a,b) noted that the pollen of some apple cultivars is more vigorous than is that of others. Planting arrangements can be
designed to increase the efficiency of available pollinators. Another method
of alleviating pollinator shortages is to protect and enhance the habitats of
wild pollinators. Strategies for improving pollinator habitats in and around
agricultural areas are discussed in Chapter 6.
Economic and Financial Consequences of Pollinator Shifts
Honey bees are responsible for the greatest percentage of agricultural
pollinator activity in North America, and they constitute the greatest percentage of the commercial pollination market. Commercial beekeepers, who
account for an estimated 99 percent of all reported pollination rentals in
North America (Burgett, 2004), earn their income from pollination fees and
honey sales. Honey revenues averaged $143 million annually from 1986 to
2005 (USDA-NASS, 1995, 1999, 2004b, 2005), and reached record highs

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in 20022003 (USDA-NASS, 2005). Although pollination fee data are not

reported nationally, the total has been estimated at $150 million: $75 per
hive for each of the 2 million hives in commercial hands (Rucker et al.,
2005).
Commercial beekeepers divide their honey bees time between crops
that contribute to pollination income and crops that yield marketable honey.
Honey production is high for alfalfa, clover, and vetch crops. Almonds,
however, which create North Americas greatest demands for managed
honey bees, do not provide commercially competitive honey. Pollination
fees tend to be higher for crops that need pollination, but produce poor
honey. Burgett and colleagues (2004) reported average pollination fees
for honey crops (vetch seed, crimson clover seed, red clover seed, radish
seed, blueberry) between 1987 and 2002 ranged from $2.67 to $23.29 per
colony, in 2002 dollars. By contrast, fees for nonhoney crops (cucumber,
pear, sweet cherry, squash, apple, cranberry, almond) were higher: $25.21
to $38.24. Rucker and colleagues (2005) reported that honey production
and pollination services tend to compete for beekeepers services and higher
honey prices are associated with higher fees for pollination.
The largest concentrations of honey bee colonies are maintained in four
regions: the Dakotas and the northwestern tier states, where large areas
of vetch and clover produce high-quality honey; California, with almond,
fruit, and melon crops; Florida, with orange blossom as the major March
and April crop and with winter vegetables and small fruits; and Texas, with
winter vegetables (USDA-NASS, 2006). The mobility of commercial bee
colonies on tractor trailers creates three major south-to-north pollination
routes: West Coast, Midwest, and East Coast.
The economic consequences of pollinator shortages in agriculture hinge
on six determining factors: a specific need for animal pollination, a crop
yield gain contributed by the pollinator, the crop price, the cost of pollination services, the value of marketed byproducts (such as honey), and the
availability of alternative means of pollination.
Predicting the direct, short-run economic consequences of population
declines in honey beesthe principal managed pollinator speciesis not
straightforward. Microeconomic theory predicts two effects; both increase
pollination fees. The first is a rise in cost of producing and maintaining commercial bees. This increase reduces the quantity of pollinators that can be
supplied at any price (leftward shift in the supply curve, illustrated in Figure
4-1). The second is an increase in demand for commercial honey bee pollination caused by decreases in feral bee colonies and native pollinator numbers
or by an increase in acreage or floral density of pollinator-dependent crops
(rightward shift in the demand curve, Figure 4-1).
The economic effects of a decrease in abundance of insect pollinator are
likely to be greatest for crops that rely heavily on insect pollination. Morse

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BOX 4-1
Pollination Fees for California Almonds

The California almond industry is contending with record high prices for
rentals of honey bee colonies. Average fees jumped from $35 per colony in
the late 1990s to $75 in 2005 (Burgett, 2005; Burgett et al., 2004) (Figure 4-2),
and fees can go as high as $150 per colony (http://beesource.com/pov/
traynor/bcnov2005.htm). Given that the U.S. commercial honey bee population remained fairly stable (on a year-to-year basis) between 1996 and 2004
(USDA-NASS, 1999, 2004a, 2005), the increased cost cannot be attributed
solely to honey bee decline.

Three other factors are also responsible for the higher pollination fees.
First, California almond acreage expanded more than 35 percent (from
405,000 to 550,000 acres) between 1991 and 2004, during which time varroa
mites infestations were widely detected (Pollack and Perez, 2005). The current bearing acreage in almonds requires 1.4 million colonies for pollination
during the February flowering period (Heinz, 2005), and that figure constitutes
more than 60 percent of the U.S. supply of commercial honey bees. Second,
honey bee colonies have experienced significant winter mortality that is attributable to varroa mite infestation that leads to seasonal colony shortages
each February because beekeepers have not had time to rejuvenate colonies.
Third, the price of honey has been relatively high since 2002. Almond nectar
is bitter, so beekeepers who market honey avoid almonds as forage plants.
Indeed, honey traditionally competes with pollination for the beekeepers business: when honey prices go up, pollination rental fees climb as well (Rucker
et al., 2005).

How high can almond pollination fees go? Recent almond plantings mean
that bearing acreage will continue to rise. Given that almonds are almost
and reduced agricultural employment would have negative multiplier effects

in the reduction of spending on other goods and services.
The prices of pollination byproducts and the availability of alternative
means of pollination also should be considered. A decline in managed honey
bee populations should trigger a rise in the price of honey. And the rising
cost of pollination and the income lost as a result of lower crop yields should
trigger research and development of alternative means of pollination.
Evidence suggests that some of the hypothesized economic effects of
pollinator decline have, in fact, occurred in the United States since the mid1980s when tracheal and varroa mites began to spread. Statistical regression analysis of annual pollination fee data from Washington and Oregon
shows that honey bee colony rental fees for pear, cherry, and apple rose by
$4.40$5.30 (in 2002 dollars) after 1991, when the varroa mite was widely

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higher pollination fees that eventually would be seen in higher prices at the
supermarket.
Over the long term, the indirect effects of honey bee shortages will depend on how markets and technology respond. If the pollination markets
adjust to a new, higher price equilibrium, then higher costs could undermine
the profitability of crop production in marginal areas. Increased food prices
also are possible, although whether they occur would depend on competition from fruit, nut, and vegetable producers outside North America.
POLLINATORS IN NATURAL AREAS
Pollinator Limitation of Seed Production
As with agricultural systems, pollinator limitation in natural plant
populations occurs through a variety of mechanisms that decrease pollinator
abundance below that required by plants for full reproduction, and pollinator shortages are expected to depress fruit and seed set in local plants. Low
seed set can be caused by other factors as well, including severe weather,
inadequate concentrations of soil nutrients, disease, damage caused by herbivores, partial sterility, or shortages of neighboring plants with compatible
pollen. Thus, in plant populations where reproduction is low or appears to
be declining, explanations other than inadequate pollination should first
be ruled out (Figure 4-4). It is difficult to study the efficacy of pollination
services because it is usually impossible to augment native pollinator populations artificially in controlled experiments (Thompson, 2001). Therefore,
many studies rely on indirect evidence, such as correlations between pollinator abundance and seed set or the effects of hand-pollination treatments
on seed set (Box 4-2).
In the most extreme examples of pollinator limitation, seed set fails
because a plants primary pollinators are extinct or in precipitous decline.
The best known cases in the United States involve endemic Hawaiian plant
species that depend on pollinating birds or moths that are now extinct
on one or more islands (Nabhan and Buchmann, 1996); some of them
are maintained only by hand pollination. Two species of native lobeliads,
Brighamia insignis and B. rockii (Shepherd et al., 2003), are examples whose
principal sphingid moth pollinator is believed to be extinct (Kearns et al.,
1998). In other cases, broadly applied insecticides have killed some native
pollinators, resulting in low seed production in two species of wild plant
(Thomson et al., 1985).
A more subtle form of pollinator limitation occurs when a plant species
loses its pollinators to competition with other plants that have overlapping
flowering seasons and share the same habitat (Kephart, 2005). Pollinators
often prefer one plant species over another because of differences in floral

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BOX 4-2
Pollen Supplementation Experiments

Seed production is influenced by the supply of resources available
to the plant for producing reproductive structures as well as by the availability of compatible pollen for siring seeds. A common way to test for
pollen-limited fecundity (seed set) is to carry out pollen supplementation
experiments (Ashman et al., 2004). The flowers of one set of plants are
hand-pollinated with ample amounts of compatible pollen, and their seed
set is compared with that of flowers on naturally pollinated control plants
(Kearns and Inouye, 1993; Thompson, 2001). Thorough hand-pollination
of all of a plants flowers throughout its lifetime can aid in differentiating
between resource limitation and pollen limitation (Zimmerman and Pyke,
1988) in that resource limitation might prevent plants from producing fruits
in successive years even when there is no shortage of pollination.

Hand-pollination is impractical, however, in long-lived or many-flowered species like shrubs and trees. If only a fraction of the plants flowers
are hand-pollinated, a separate set of control flowers should be used to
determine whether artificially high seed set from hand-pollinated flowers
causes artificially low seed set on the remaining, naturally pollinated
flowers. Such an outcome could result because resources that are used
early in the growing season are not available for later fruit set (Knight et
al., 2005a; Stephenson, 1981).

Similarly, to avoid overestimating the extent of pollen limitation,
investigators should determine whether artificially high fecundity in one
year is followed by lower fecundity or reduced vegetative growth in the
next year, as occurred in moth-pollinated cranefly orchids (Tipularia
discolor) in Maryland (Snow and Whigham, 1989). Pollen supplementation experiments should be carried out in several populations, including
small, isolated populations, to account for temporal and spatial variation
in pollinator service. Some studies probably over- or underestimate the
extent of pollen limitation, but meta-analyses of pollen supplementation
experiments can correct for many of these shortcomings (Knight et al.,
2006). Careful experimentation can reveal the relative contributions of
resource limitation and pollen limitation within a single species (Asikainen
and Mutikainen, 2005; Campbell and Halama, 1993).
Because several mechanisms can account for low fecundity (Figure 4-4),
it is useful to distinguish between two types of pollen-related constraints on
seed production: pollinator limitation (insufficient pollinator service) and
pollen limitation (insufficient delivery of compatible pollen to receptive stigmas; see Thompson, 2001). Low numbers of pollinators often cause pollen

122
limitation of seed production, but not all examples of pollen limitation result
from low numbers of pollinators. For example, pollen limitation can occur
in self-incompatible species that are highly clonal (Duncan et al., 2004), in
populations without compatible mating types (Demauro, 1993), or during
mass flowering (Vance et al., 2004) even when pollinators are common
because too little outcross pollen is delivered to receptive stigmas. Methods
for quantifying pollen limitation of seed set are described in Box 4-2. Plant
populations that experience chronic and increasingly severe symptoms of
pollen limitation are prime candidates for further study to determine whether low fecundity can be attributed to declining pollinator populations.
Several recent reviews indicate that pollen-limited fecundity is widespread in natural populations and can be severe (Burd, 1994; Knight et al.,
2006; Larson and Barrett, 2000). Burd (1994) reported that 62 percent of
258 species exhibited pollen limitation at some sites and times, and Ashman
and colleagues (2004) found evidence for pollen limitation in 62 of 85 cases
in which hand-pollination was carried out on whole plants. In agreement
with previous surveys, Knight and colleagues (2005a) reported that pollen
limitation was more common in self-incompatible species than in selfcompatible ones, and plants with fewer pollinator species were more likely
to be pollen-limited than were those with many. Vamosi and colleagues
(2006) reported a strong positive correlation between plant species richness
and pollen limitation on a global scale, but there was no clear explanation
for this association. The investigators hypothesized that competition for
pollinators is more prevalent in species-rich communities, but they were
unable to determine whether competition for pollinators is a natural and
long-standing phenomenon or whether lower fecundity is a consequence of
recent declines in pollinator populations.
In general, little is known about whether pollen limitation of seed set
in wild plants has become more chronic or more severe on a large scale in
recent decades. In any given species, the ratio of flowering plants to foraging
pollinators can vary greatly during the flowering season, among locations,
and over time (Fenster and Dudash, 2001), so it is difficult to identify all
but the most drastic pollinator shortages. Despite that, well-planned pollen
supplementation experiments can provide useful tests for pollinator service.
They also are more manageable than tracking pollinator population trends
directly or attempting to correlate variations in pollinator abundance with
plant fecundity. Pollen supplementation experiments provide information
about the immediate consequences of pollinator shortages, especially when
studies include flower-bagging treatments that completely exclude pollinators. Conservation biologists use hand-pollination to determine whether
insufficient pollination might contribute to the decline of threatened and endangered species, although that often is not the case (Bigger, 1999; Johnson
et al., 2004; Rasmussen and Kollmann, 2004). Long-term monitoring of

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pollen-limited fecundity (Chapter 5) is a prerequisite for securing compelling

evidence of the functional consequences of pollinator declines.
Direct and Indirect Effects of Pollinator Shifts
Specialization and Redundancy in Plant-Pollinator Interactions
Pollination is typically a mutualistic relationship, and disrupting it can
have immediate and significant consequencesat least for the partners
directly involvedalthough the consequences might not be easily or immediately discerned. Janzen (1974) and Kevan (1974) suggested that loss of
mutualisms could be an insidious process that might go unnoticed but that
eventually would have major consequences for the integrity of an ecosystem. The complex nature of many plant-pollinator relationships, which can
involve many links among species, could mean that the loss of component
species would eventually elicit a sequence of plant or pollinator extinctions
(Memmot et al., 2004; Olesen and Jain, 1994; Rathcke and Jules, 1993).
Few studies have investigated how the breakdown of mutualistic pollination relationships might contribute to the decline of endangered plants
(Robertson et al., 1999), but there are examples of the extinction of the
primary pollinators of some species (Cox and Elmqvist, 2000; Ladley and
Kelly, 1995; Robertson et al., 1999; Weller, 1994). Memmot et al. (2004)
used records of flowers and pollinators to simulate the consequences of progressive pollinator extinction by removing pollinator species and observing
which plants were left without pollinators as a result. In the simulations, the
proportion of plants visited by pollinators declined differentially depending
on whether pollinators are removed at random, systematically from least
specialized (generalist) to most specialized, or systematically from most specialized to least specialized. The percentage of plants visited decreases more
or less linearly if generalist pollinators are removed first. If the pollinators
are removed in random order or in the order from least to most specialized,
the percentage of plants visited decreases in a steadily accelerating pattern.
These results suggest that loss of generalist pollinators pose the biggest
threat to pollination systems (Memmott et al., 2004).
Pollen limitation of fruit or seed set can serve as a useful indication of
pollinator decline. However, although many researchers have demonstrated
apparent pollen limitation, few have investigated its effects on the demographics of plant species (but see Johnson et al., 2004; Ward and Johnson,
2005). The decline or loss of specialist pollinators would appear to be an
obvious case in which to find consequences for conservation. Steiner and
Whitehead (1996) identified a case in which the floral form of a South African shrub (Ixianthes retzioides) suggested that a large oil-collecting bee was
the coevolved pollinator, although no such bee could be found in the popula-

124
tions examined. The minimal seed set that occurs in the populations appears
to be the result of visits by pollen-collecting bees. There are other cases in
which the loss of a coevolved pollinator appears to have been ameliorated
by the arrival of introduced species that visit and pollinate the flowers. For
example, in Hawaii the Japanese white-eye Zosterops japonicus has taken
over the role of extinct or rare native birds in pollinating at least two plant
species (Cox, 1983; Lammers et al., 1987). Plants with long, curved corollas, which might have depended on pollinators with matching mouthparts,
have had unusually high extinction rates on Pacific islands; these losses have
been accompanied (or preceded) by extinctions of their pollinating birds
(Pimm et al., 1994).
Although few North American plant species rely on a small number
of pollinator species for seed production, many plants depend heavily on
specific floral visitors, such as bumble bees, for effective pollination. Plants
have evolved suites of floral traits that attract and reward pollinators and
pollinators can be classified into functional groups based on the types of
flowers they pollinate (reviewed by Fenster et al., 2004).
To explore the extent of specialization for pollinators, Fenster and
colleagues (2004) examined visitation data for 278 animal-pollinated
plant species in Illinois that had been studied almost 80 years earlier by
Robertson (1929). Recognizing that not all floral visitors are effective as
pollinators, Fensters group reported that 75 percent of the plant species
were visited mainly by species in only one or two of nine functional groups
(long-tongued bees, short-tongued bees, other Hymenoptera, Diptera, Coleoptera, Lepidoptera, Hemiptera, Neuroptera, and birds). In contrast, Waser
and colleagues (1996) examined Robertsons (1929) records and noted that
91 percent of 375 native plant taxa reported in that study had been visited
by more than one pollinator species. These reviews suggest that flowers of
many plant species are visited by generalist pollinators as well as by pollinators in particular functional groups (Tudor et al., 2004).
If pollinator declines occur differentially in different taxonomic groups,
rather than across all categories of major pollinators equally and simultaneously, the consequences for plant reproduction depend on the degree of
redundancy in pollinator communities and on changes in the composition
of pollinator communities. Redundancy has been described for a variety of
plant-pollinator relationships; angiosperms in general could thus be buffered against losses of individual pollinator species (Waser and Ollerton,
2006). Most pollinators visit a variety of plants, and many plants are attractive to a range of pollinators (Memmott, 1999; Memmott et al., 2004).
Because most pollinators are not completely constant to particular flowers,
plant-pollinator interactions represent a complex web. Redundancy is one
characteristic of community-level analysis of plant-pollinator relationships
in general (Memmott, 1999).

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The importance of redundancy among co-occurring pollinators is apparent in the variation in floral availability among locations, over time (for
example, Saavedra et al., 2003), and among pollinators. The redundancy of
services is a safety net for the long-term survival of plants and pollinators
alike. Sharing of pollinators also can facilitate interactions among plants
(Moeller, 2004). An example of the dynamic nature of pollinator communities involves the creosote bush, Larrea tridentata, a plant visited and
pollinated by many specialist bees in the southwestern United States and
Mexico. There are few long-term studies of bee abundance and diversity,
but one investigation in undisturbed sites revealed that only a minority of
abundant bee species was typically persistent, even after 20 years (Cane
et al., 2006). Most of the bee species in the Larrea pollinator guild were
uncommon, geographically sporadic, and temporally unpredictable (Cane
et al., 2006). Williams and colleagues (2001) surveyed published studies
and reported that bee faunas are typically locally diverse, highly variable in
space and time, and often rich in rare species. These attributes of pollinator
guilds indicate that intense long-term sampling among sites is necessary to
differentiate the changes that are attributable to specific impacts of pollinator declines from the natural dynamics of populations and communities.
These attributes also suggest that a metapopulation model that accounts
for local disappearance and reintroduction of insect populations may be
typical of many pollinator species. Because plant-pollinator interactions are
highly connected and plant and pollinator populations can shift in time and
space, conserving mutualisms might require a better understanding of their
population dynamics and interactions.
Pollinator Declines, Plant Demography, and Genetics
The degree to which declining pollinator abundance affects plant population dynamics depends on several factors (Harris and Johnson, 2004), as
illustrated in Figure 4-4. First, a decline in pollinators will not necessarily
result in lower seed production (step 1, Figure 4-4). The prevalence of
pollen-limited fecundity (Knight et al., 2006) suggests that low seed set or
fruit production could be exacerbated by declining pollinator populations,
but that might not be the case if alternative pollinators are present or if the
plant is autogamous (self-pollinating) when pollinators are absent. Even
when seed set remains high, though, increased rates of selfing could lead
to poor seed quality because of inbreeding depression (Charlesworth and
Charlesworth, 1987). In species that typically outcross, the survival and
reproduction of selfed progeny are often lower than they are for outcrossed
progeny (Dudash, 1990). Plants with mixed mating systems could be forced
to increase reliance on selfing instead of outcrossing for seed production
(Goodwillie, 2000).

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The second condition that must be met for population-level responses to

pollinator declines is for lower seed production to translate into lower seedling establishment (step 2, Figure 4-4). If seedling establishment is limited by
some factor other than seed production, such as dispersal, seed predation,
germination microsites, or high seedling mortality, then reduced fecundity
might not affect seedling recruitment. Few studies have demonstrated that
plant population size is seed-limited (Brys et al., 2004; Juenger and Bergelson, 2000). Empirical study of seed limitation is challenging. Vast numbers
of seeds never reach a suitable site for seedling establishment, which is often
patchy and episodic, and the effects of small but chronic decreases in plant
fecundity on seedling populations could be difficult to measure in the field.
Therefore, plant population ecologists often rely on population modeling
based on empirically derived transition probabilities to predict the effects
of reduced or enhanced fecundity on seedling establishment (Miriti et al.,
2001).
The third condition that must be met for population-level responses to
pollinator declines is for decreased seedling establishment to cause decreases
in the number of mature plants. As with seedlings, the survival of young
plants to sexual maturity can be strongly limited by competition, herbivory,
extreme weather, human activity, and numerous other factors. Population
modeling is useful for determining how this stage of the plants life history
affects the number of mature plants. Drastic reductions in recruitment could
be detectable in natural populations, and small, undetectable effects of declining fecundity could be insignificant or important. If the plants are longlived perennials, it might be many years for the loss of pollinator services to
become apparent in the population structure. Many wild plant populations
already are declining because of habitat loss, competition with invasive
species, overgrazing by livestock or deer, and other factors (Ellstrand and
Elam, 1993); more information is needed to ascertain whether declining
pollinators could induce or exacerbate the loss of plant populations. Such
a decline in wild plant populations because of pollination deficits might be
in progress, but there is a dearth of published evidence for its occurrence in
North America during recent decades.
If all the consequences of declining pollinator populations in fact occur
(which seems unlikely), plant populations could become more vulnerable to
an extinction vortex. The extinction vortex refers to the interacting factors
that serve to reduce small populations progressively because of the increased
risk of demographic and genetic consequences of small population size,
including genetic erosion, inbreeding depression, decreased reproductive
success, and greater susceptibility to catastrophes and random variations
in environmental parameters (Kearns et al., 1998). One demographic risk
is the Allee effect (inverse density dependence at low densities), which has

127
been demonstrated experimentally in plant populations (Groom, 1998;

Hackney and McGraw, 2001) and observed in nature (Lamont et al., 1993).
If there are no compensatory mechanisms for pollinator loss, and if reduced
seed production from pollinator loss is directly reflected in smaller plant
populations, these populations could enter an extinction vortex (Bond,
1994). Only careful research can disclose the necessary information about
breeding systems, specificity and redundancy of pollinators, and plant life
histories that will allow accurate prediction of the consequences of pollinator declines or losses.
At the other end of the spectrum, pollinator populations could increase
and have a positive effect on plant abundance. One such case involves banyan trees, introduced ornamental fig species (especially Ficus benghalensis,
F. altissima, and F. microcarpa) that became invasive pests in southern
Florida subsequent to the inadvertent introduction about 25 years ago of
the nonnative wasps that pollinate them (Nadel et al., 1992).
Indirect Effects of Pollinator Declines
There is a possibility that a cascade of ecological consequences could
follow from the loss (or change in abundance) of roots, stems, leaves, flowers, fruits, and seedsall of which can be resources for herbivores (including seed predators)produced by plants. A broad range of herbivores and
frugivores is supported by such resources, as are parasites and parasitoids
of those species. Decreases in seeds, nuts, and fruits could be damaging
to many species of insects, birds, and mammals, even if plant populations
do not exhibit declines. More severe effects are expected if populations of
mature plants become scarcer. For example, trophic cascades and the loss
of shelter and nesting sites associated with plant species decline could cause
reductions in bird populations. An example of how pollination itself can be
part of a trophic cascade is provided by a study of the effects of fish as predators of dragonfly larvae in Florida (Knight et al., 2005b). Adult dragonflies
are predators of some pollinators, so plants near ponds with dragonflyeating fish receive more pollinator visits and are less pollen-limited than
are those near fish-free ponds. This example suggests that pollinators are
an important food resource for insectivorous predators.
Economic and Financial Consequences
Major shifts in natural pollinator populations could have economic
repercussions either directlyin their appeal to nature lovers and collectorsor indirectly in their effects on the plants they pollinate. Some pollinators are appreciated aesthetically; butterflies and hummingbirds are

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prime examples. That the honey bee is the state insect of 17 states and
that various butterflies are state insects in 23 additional states (http://www.
netstate.com/states/tables/state_insects.htm) is an indication of the visibility of pollinating species and the value placed on them. Apart from their
intrinsic value, pollinators generate economic benefit through tourism. In
20002001, about 250,000 tourists visited the monarch butterfly reserve
in west-central Mexico (Barkin, 2003). Colorado, Florida, Costa Rica, and
Brazil host butterfly and bird tours (http://wingsbirds.com/birdsand.htm),
although no estimates are readily available on total tourist expenditures at
these sites.
Apart from ecotourism, at least one study shows evidence of park visitors expressed willingness to pay to protect endangered butterfly species (of
Boloria aquilonaris in Germany; Degenhardt and Gronemann, 1998). The
existence of various pollinator conservation groups also provides evidence
of peoples willingness to pay to ensure the survival of endangered butterflies and birds. Examples include the British and Dutch Butterfly Conservation organizations (http://www.butterfly-conservation.org/ and http://www.
vlinderstichting.nl/), the American Butterfly Conservation Initiative (http://
www.butterflyrecovery.org/), the Xerces Society (www.xerces.org), and the
Hummingbird Society (http://www.hummingbirdsociety.org/).
The loss of major groups of pollinators in natural areas could trigger
changes in abundance or community composition, or even the loss of plant
species that depend on pollinators for sexual propagation. The economic
value of such losses stems from two sources. The first is the combination of
existence, bequest, and cultural values that some people would be willing
to pay to ensure species survival, enjoyment, or use by future generations.
Also important are the aesthetic benefits or cultural satisfaction of watching
pollinators at work. This broad category of value applies not only to the
pollinator species, but also to plant species that depend on them for reproduction and to animal species that depend on associated fruits and seeds
for food. No studies appear to have estimated willingness to pay to prevent
such wild species losses that would attend pollinator decline.
The second source of economic value is the value of losing the potential opportunity to generate future income, for example by commercial
pharmaceutical discoveries that could have come from a species that will
be lost. The bioprospecting literature has attempted to estimate the value
of conserving biodiversity hotspots. Published results ascribe low values to
land conservation, except in areas with very high biodiversity, because the
probability of finding commercially exploitable species is low (Rausser and
Small, 2000; Simpson et al., 1996). Theoretical valuations from models of
complex species interaction offer less definitive results (Simpson, 2002) but
give no guidance for small-scale biodiversity loss attributable to pollinator shifts. Extrapolating from these findings, the likely value of the small

129
number of plant species that might be lost as a result of reproductive failure

that is caused by a loss of pollinators is likely to be small. Finally, some
economically important wild species (for example, ginseng) that suffer from
pollinator limitation also are severely threatened by other stressors, such as
overharvesting and deer grazing (McGraw and Furedi, 2005). In such cases,
species demise is only partially attributable to pollinator limitation.
CONCLUSIONS
Severe shortages of pollinators could cause many common food crops
to become more expensive and perhaps less available, but there is no strong
evidence for a current pollination crisis in agricultural production in North
America. Most animal-pollinated crops can be serviced by honey bees, and
farmers are accustomed to paying more for these services when necessary.
Chronic pollinator shortages should lead to market adjustments and other
innovations, although the demand for supplemental pollination has been
strong recently, especially among Californias almond growers. Importing managed pollinators from other countries or regions can lead to the
introduction and spread of pathogens and unwanted bee species (Chapter
3). Therefore, it is prudent to sustain wild-pollinator populations as a
means of buffering current and future shortages of managed pollinators of
agricultural crops. In some cases, farmers could find that promoting wild
pollinators that can supplement or substitute for managed pollinators could
provide greater yields than will complete dependence on rented honey bee
colonies (for example, Greenleaf, 2005). Intensive agricultural practices and
pesticide use can reduce wild-pollinator diversity and abundance (for example, Kevan, 1975b; Kremen et al., 2002b; Larsen et al., 2005). Strategies
for promoting abundance of wild pollinators are presented in Chapter 6.
In natural areas, the consequences of pollinator shifts on ecosystem
services and possible solutions to these problems are varied and complex.
Relatively few plant species rely on a single pollinator species or even on a
single category of pollinators for reproduction. Because of the redundancy
of most plant-pollinator communities, the ecological consequences of losing
a small number of pollinator species could be limited. However, the loss
of pollinator species reduces the redundancy of pollinator services in the
ecosystem, and thus its resiliency, so that further losses of pollinator species
would likely have more severe consequences for the ecosystem.
Plant communities in which massive pollinator declines are reported, for
example because of persistent pesticide use or extensive habitat degradation,
merit careful study of ramifying consequences for biodiversity. The ecological consequences of widespread pollinator declines could be substantial, but
they could be difficult to detect because seed production varies dramatically
in response to many biotic and abiotic factors (Figure 4-4). Moreover, the

130
effects of sustained declines in seed production on the size and abundance

of plant populations could be subtle, slow processes that are real and overlooked by short-term studies. There is little available evidence to suggest that
recent pollinator declines in North America have resulted in smaller populations of wild plants, possibly because the challenges of obtaining evidence
are formidable. More research is needed to assess ecological consequences
of current and future pollinator declines.

5
Monitoring Pollinator
Populations and Services
Given that information on the status of pollinators and pollination

services is far from complete, it is important to establish standardized,
wide-scale, long-term protocols for monitoring pollinator populations and
pollination services so that future changes can be assessed and appropriate
actions taken. Existing monitoring efforts, in place for commercial honey
bees and for some wild bee, butterfly, bird, and bat pollinators, provide a
starting point. However, all extant programs need to be improved and an
overarching framework will be useful for establishing cost-effective and
feasible monitoring programs for a broader range of commercial and wild
pollinators and pollination services in North America.
REVIEW AND ASSESSMENT OF
CURRENT MONITORING PROGRAMS
Commercial Honey Bee Colonies
The National Agricultural Statistics Service (NASS) generates agricultural production statistics through the use of annual surveys of producers
of agricultural products in each state. NASS offices continuously update
producer lists, which are solicited from a variety of sources including commodity and grower groups. Beekeeping is one of the industry groups monitored by NASS. NASS reports on beekeeping operations through its annual
honey report and its 5-yearly agricultural census.
The NASS Annual Honey Report of beekeeping commodities includes
131

132
national statistics on the price of honey (per pound) by color and marketing
channel, and the following commodity statistics for each state:
The number of honey-producing colonies.
The average honey yield per colony.
Total honey production.
The average price per pound paid to beekeepers.
Total value of honey production.
Stocks of honey held by producers (not including stocks held by
producers under the commodity loan program).
Data from states with few beekeeping operationsConnecticut, Delaware,
Maryland, Massachusetts, New Hampshire, Oklahoma, Rhode Island, and
South Carolinaare pooled to maintain confidentiality. Colony counts
reported by NASS in its Annual Honey Report are based on beekeepers
with more than five colonies and on honey-producing colonies only. Colony
counts include all honey-producing colonies in a state and may count colonies more than once if they produce honey in more than one state (migratory
beekeeping).
The 5-yearly Census of Agriculture uses different counting procedures
than the Annual Honey Report. The most recent 2002 census (USDA-NASS,
2004a) counted all bee colonies, and counted them only in the county
where the owner of the colonies largest value of agricultural products was
raised or produced (USDA-NASS, 2004a, Appendix A, p. A-8). The census
reports inventories and sales of colonies of bees, and honey produced, both
nationally and by state.
The data reported suffer from a number of ambiguities. Restricting reported counts to honey-producing colonies results in an underestimate of the
number of colonies; although NASS collects data in its annual survey form
Bee and Honey Inquiry on the total number of colonies, they report on
only the honey-producing colonies. According to the most recent agricultural
census, for example, 30 percent of the nations 17,357 beekeeping operations
did not produce honey in 2002 (USDA-NASS, 2004a, Table 2.19, p. 378).
Yet counting colonies in each state in which they produce honey results in an
overestimate of the number of colonies. The magnitude of these two countervailing errors is undetermined. Restricting colony counts to beekeepers
with more than five colonies also results in an underestimate of the number
of colonies nationwide. This undercount may involve as many as 100,000
400,000 colonies, assuming 100,000 hobbyist beekeepers with 14 colonies
each (Chapter 1). Although, the colonies of most hobbyists are unlikely to
find their way into the commercial pollination marketplace, they may contribute substantially to pollination for small grower operations, backyard
gardens and urban landscapes, and wild (native and weedy) plants.

MONITORING POLLINATOR POPULATIONS AND SERVICES
133
NASS statistics also do not include an assessment of pollination-relevant

characteristics such as colony quality (strength, presence of parasites or
pathogens), number of colonies lost over the winter (trade journal reports
of winter losses are largely anecdotal), number of colonies rented for pollination, pollination rental fees, crops pollinated, and the numbers of queens
and packages produced. At present, NASS statistics provide data only from
beekeepers; such information from growers as rental price paid or the ease
of obtaining the appropriate pollination service would provide a useful
comparison with data collected from beekeepers to allow for an assessment
of demand and shortages.
Wild Pollinators
Bees
Repeat Surveys
Several contemporary investigators have visited historical field sites
where earlier pollinator surveys, particularly of native bees, had been conducted to determine if landscape changes during intervening years had resulted in changes in bee guild composition or losses of species from the area.
Carlinville, Illinois, was sampled from 1884 to 1916 by Robertson (1929),
who collected 214 bee species on over 400 plant species. Of the 214 species,
157 were found on only 24 of the plant species sampled. Approximately
three-quarters of a century later (19701972), Marlin and LaBerge (2001)
repeated that survey in Carlinville, concentrating their sampling effort on
the 24 plant species that provided the bulk of the bee species reported by
Robertson (1929). They collected 140 species of bees representing 82 percent of the species found by Robertson (as well as 14 species not recorded on
those plants in the earlier survey). The relatively high degree of similarity in
the bee community, despite the passage of 75 years and extensive landscape
changes, was not the anticipated result. The authors suggested that patches
of diverse habitats embedded within the agricultural matrix (for example,
rural grasslands, forests, and open woods) have maintained bee diversity
over time despite major changes in land use patterns.
Kevan and his colleagues have been analyzing data for pollinator diversity and abundance (Kevan et al., 1997) on New Brunswick blueberry
fields for a period of about 8 years and find that the Srensen, and other
indices, of similarity between years but on the same fields are typically low
(about 0.2) (unpublished). Turnock et al. (in preparation) have analyzed
8-year-long patterns of abundance in bumble bees in Manitoba, and noted
changes by orders of magnitude from one year to the next. Javorek has some
longer term studies ongoing in New Brunswick and Nova Scotia (Javorek
et al., 2002). Sheffield (2006) has compared the data of Brittain (1933)

134
with his own and found that by and large, the diversity of bees that visit
apple blossoms has not changed. Roubik studied euglossine bees at chemical baits for 20 years in Panama and reviewed other monitoring studies of
bees conducted in California and in Central and South America (Roubik
2001). The euglossine bee guild in Panama showed no detectable overall
change in species richness over 20 years, but interannual variability in bee
abundances, both at the community and species level, was high (414 fold,
respectively). He concluded that surveys must include a minimum of four
sampling years to detect statistically significant trends in bee populations
(Roubik, 2001).
New Monitoring Programs
Several of the most comprehensive and extensive long-term monitoring
programs for bees have been established outside temperate North America
(for example, Europe, Box 5-1). In recent years, however, several notable
programs have been initiated for monitoring North American bee species.
Since 2002, James Cane (U.S. Department of Agricultures Bee Biology
and Systematics Laboratory in Logan, Utah) has coordinated a network
of professional scientists collecting data on the diversity and abundance of
bees at native and cultivated squash and gourd plants in Canada, the United
States, and Mexico using standardized observation and sampling techniques
(http://www.ars.usda.gov/Research/docs.htm?docid=12040). This effort is
designed to establish baseline data and assess changes in cultivated squash
and gourd bee guild populations over time and under different land management practices.
Butterflies
As with bees, many of the longest and most comprehensive monitoring
programs for butterflies are conducted outside the United States, either in
the New World tropics (for example, the 35-year program in the Atlantic
Forest region, Brown and Freitas, 2000) or the 30-year Butterfly Monitoring
Scheme in the United Kingdom (Roy et al., 2001). However, several U.S.
butterfly species have been studied and their populations censused for decades by individual investigators. Perhaps best known are the long-standing
studies of Paul Ehrlich and colleagues of Euphydryas editha bayensis, the
Bay checkerspot butterfly. This species was regularly censused in Stanford
Universitys Jasper Ridge Biological Preserve near Palo Alto, California,
for almost 40 years (Ehrlich and Hanski, 2004; Chapter 2). Among the
insights gained from this long-term study are the prevalence of local extinctions (even of federally protected species), the importance of topographic
heterogeneity to allow populations to weather extreme droughts and floods,

135
and the need for nearby populations to provide migrants for recolonizing
habitat patches following local extinctions. These insights apply not only
to Euphydryas editha bayensis populations, but also to many other pollinator species that require habitat heterogeneity (particularly the ones that
exist in subdivided populations because of habitat fragmentation). Habitat
heterogeneity accommodates the different habitat requirements of larvae
and adults and allows the insects to respond adaptively to intraannual and
interannual weather variations.
Another notable butterfly monitoring effort, also in California, has been
conducted near Davis, California. Arthur Shapiro and colleagues (University of California at Davis) conducted an annual census of butterflies from
Willow Slough, California, for over 29 years. Examination of census records
of over 39,000 individuals representing 36 species for trends in faunal diversity and in the probability of presence of individual species (Chapter 2
and OBrien et al., forthcoming) revealed a statistically significant decline
of 38 percent in overall species diversity. That long-term studies are needed
to detect declines is evidenced by the fact that for 22 years the measured
decline in observed richness did not achieve statistical significance.
The annual fall migration of the monarch butterfly, Danaus plexippus,
has been monitored according to a standardized protocol by Lincoln Brower
and colleagues on an annual basis from the peninsular town of Cape May,
New Jresey, from 1991 to 2004 (Walton et al., 2005). The 13-year survey
revealed substantial annual fluctuations in the numbers of migrating butterflies, with a 13-year low recorded in 2004. Across the 13-year period,
numbers of monarchs counted per season varied 35-fold. In general, years
of above-average abundance tend to be followed immediately by years of
below-average abundance, a pattern that, again, emphasizes the value of
multiyear long-term monitoring in order to avoid drawing inappropriate
conclusions about pollinator status.
North American Butterfly Association
The North American Butterfly Association (NABA, http://www.naba.
org) has about 5,000 members and is the largest group of individuals in
North America (Canada, United States, and Mexico) interested in butter
flies. The Xerces Society for the Invertebrate Conservation and subsequently NABA have conducted the annual Fourth of July Butterfly Counts
across North America since 1975 (http://biology.usgs.gov/s+t/noframe/
f070.htm; http://www.naba.org/counts.html). Results are posted on the
Internet (http://www.naba.org/pubs/countpub.html) along with a checklist
of North American butterflies (http://www.naba.org/ftp/check2com.pdf).
For example, in 2004, a total of 467 counts were held in 48 U.S. states, 4
Canadian provinces, and 1 Mexican state. Each count represents compila-

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BOX 5-1
A Model Monitoring Program for Pollinators from Europe
(ALARM)a

An extensive and innovative European Union (EU) scientific program
for long-term monitoring of bees and other pollinators has begun within the
multicountry framework of conservation farming practices. The Assessing
Large-Scale Risks for Biodiversity with Tested Methods project (ALARM;
http://www.alarmproject.net) started in 2004. ALARM is a consortium of 54
partners from academic institutions representing 26 countries, including 19
EU countries (Austria, Belgium, Czech Republic, Denmark, Estonia, Finland,
France, Greece, Ireland, Italy, Lithuania, the Netherlands, Poland, Portugal,
Romania, Slovenia, Spain, Sweden, and the United Kingdom), and Bulgaria,
Romania, Israel, Switzerland, and three International Cooperation states.
From 2004 to 2009, 16.7 million euros are budgeted for the project. ALARM
aims to quantify the environmental risks to biodiversity, including pollinators,
with standardized and repeatable sampling methodologies. ALARM has five
modules: pollinator loss, climate change, invasive species, environmental
chemicals, and socioeconomics. The pollinator module objectives are to
(1) quantify distribution shifts in keystone pollinator groups across Europe;
(2) measure the economic and biodiversity risks associated with the loss
of pollination services in agricultural and natural habitats; (3) determine the
relative importance of drivers of pollinator loss; (4) develop predictive models
for pollinator loss and consequent risks to habitat, humans, and wildlife; and
(5) create and maintain a knowledge database to underpin the sustainable
conservation and management of pollinator species across Europe.

ALARM researchers have just concluded an extensive analysis of beforeand-after data from 1980 repeat surveys of native bees and flower flies (family
tions of all butterflies observed at sites within a 15-mile-diameter circle by

teams of citizen-scientist observers in a 1-day period. Comparisons of the
NABA count results across years have proved useful in elucidating effects
of habitat and weather changes on North American butterflies (Kocher and
Williams, 2000).
Monarch Watch
Monarch Watch (http://www.monarchwatch.org/) is a University of
Kansas Entomology Program founded in 1992 and dedicated to education,
conservation, and research on monarch butterflies in North America. It
engages citizen-scientists in large-scale research projects designed to reveal

137
Syrphidae) in the United Kingdom and the Netherlands (Biesmeijer et al.,

2006; see Box 2-2 in Chapter 2). ALARM is also undertaking many repeat
historical observations of EU pollinators by resampling previously well-studied
locations. The aim is to fill current knowledge gaps with point estimates
of changes across Europe in regions where large national data sets are
unavailable.

The ALARM group is developing and testing standardized and repeatable
methods for sampling pollinators in six European countries using 48 natural
and agricultural sites. Methods tested in parallel include trap nests for bees,
water-filled pan traps, netting at flowers along fixed transects, and counts at
fixed observation plots. The final ALARM standardized methods toolkit is
planned to be ready for distribution to other researchers by 2007. The ALARM
project provides a model for a monitoring program that could be replicated in
North America. North America contains many of the same biomes (tundra,
boreal forest, temperate deciduous and coniferous forests, prairies or steppes,
Mediterranean scrub) as Europe, with a few additions (desert, subtropical,
and tropical forests). A monitoring project in North America could be more
complex ecologically but a lot simpler administratively than the European program, which involves 26 countries. Canada already has an existing Ecological
Monitoring and Assessment Network (http://www.eman-rese.ca/eman/program/about.html), which is a cooperative partnership of federal, provincial,
and municipal governments; academic institutions; aboriginal communities
and organizations; industry; environmental nongovernmental organizations;
volunteer community groups; elementary and secondary schools; and other
groups and individuals involved in ecological monitoring.
aPresentation
2005.
to the committee by S. Potts, University of Reading, on October 19,
valuable information about monarch butterfly biology and their annual

migration to and from overwintering sites in the state of Michoacan west
of Mexico City. Participants tag 30,000100,000 butterflies each year during the fall migration, with a recovery rate of tagged butterflies in Mexico
of 0.6 to 1.8 percent per year (which is considered high given the distance
the monarch butterflies travel, the hazards of the migration, and the overall
population size). This is one of the largest mark and recapture programs in
operation. All tag recoveries are posted online (http://www.monarchwatch.
org/tagmig/recoveries.htm). An estimated 100,000 people participate in
Monarch Watch each year, including students from over 2,000 schools,
and nature centers and other organizations in Canada, the United States,
and Mexico. A conservation initiative known as Monarch Waystations

138
(http://www.monarchwatch.org/ws/) has encouraged the creation and registration of over 600 monarch habitats (with host and nectar plants) located
at schools, nature centers, zoos, private homes, and businesses. Monarch
Watch serves as a model for how to maintain a long-term outreach program
that engages the public in scientific endeavors and conservation relevant to
pollinators (Rogg et al., 1999; Taylor, 2000). Other citizen-scientist programs for Lepidoptera could benefit from adopting their tagging methods
and incentives for study and reporting.
Birds
A number of different programs monitor hummingbird populations,
but the results they provide are often inconsistent, in part due to different
temporal and spatial scales of study as well as different methodologies used.
The Breeding Bird Surveys (http://www.mbr-pwrc.usgs.gov/bbs/bbs.html)
provide data and trends for many bird species, including eight humming
birds. In the 105-year database of Audubon Societys Christmas Bird
Counts (CBC; http://audubon2.org/birds/cbc/hr/graph.html), no species of
hummingbird appears to be declining. However, December is not a good
time of year to census migratory species of hummingbirds in Canada (none
recorded) and their abundance is quite low in the United States at that time
because they are in Mexico. The data for nonmigratory Annas hummingbird are highly variable (probably reflecting in part growth of participation
in the CBC) but show no indication of decline. Although the eBird citizen
science project of the Cornell Laboratory of Ornithology does not yet provide population monitoring data, it is working toward this goal. In Mexico,
a country-wide effort to document birds was launched in 2005, AverAves
(http://www.ebird.org/aVerAves/). Despite existence of multiple programs,
many species, including those that are endangered or threatened, are not
monitored at all. For example, of the 45 endangered species, only a small
number have ever been or are currently being monitored (Sibley, 2000).
In addition to these large-scale, long-term monitoring programs, several
individual investigators have carried out long-term monitoring of rufous (Selasphorus rufus) and broad-tailed (Selasphorus platycercus) hummingbirds
for decades in the western United States, Canada, and northern Mexico.
These monitoring programs have elucidated details of the migratory patterns and population and breeding structure that would otherwise probably not have been discovered. For example, Calder (1987, 1992; Banks
and Calder, 1989) found that the broad-tailed hummingbird is subdivided
into two populations: one that migrates to spend the summer in the United
States, breeding from May through July and molting in midwinter, and a
resident population that remains in Mexico year-round, molting in May
and June and breeding from September through December (Calder and

139
Calder, 1992). In contrast, in the rufous hummingbird, all individuals

migrate north in the early spring across the Pacific coastal states and then
diverge into two breeding groups: one in the Pacific Northwest and one in
the northern Rockies. Additional studies restricted to local populations have
been useful in elucidating ecology and natural history, but could potentially
better inform management action if conducted at a larger scale. E. Santana
(University of Guadalajara, Mexico, personal communication, December
2005) has monitored the abundance of several hummingbird species in the
Manantlan Biosphere Reserve of western Mexico for 18 years and found
nonuniform interannual changes between species, which suggest differential
responses among species to habitat and other changes. Another regional
study (Schondube et al., 2004) conducted between 1995 and 2001 indicated
that the number of rufous hummingbirds has remained relatively stable in
western Mexico.
Although bird populations are monitored, the monitoring is not necessarily conducted at the most informative spatial or temporal scales. Data on
seasonal, spatial, and numerical fluctuations on hummingbirds and other
flower-visiting birds could be collected across the three countries in North
America. The United States can play a role in promoting collaborative
efforts to monitor population trends, biological factors, and pollination
services by those species under standardized protocols.
Bats
The monitoring of pollinating bats to date has been limited to two of
the four threatened and endangered species. In fact, the inclusion of two
migratory nectar-feeding species on the U.S. Endangered Species List (as
endangered) and the Mexican list of species at risk (as threatened, both
species) stimulated the monitoring and study of the lesser long-nosed bat
(Leptonycteris curasoae) and the Mexican long-nosed bat (L. nivalis) (Medelln, 2003; Medelln et al., 2004). The intermittent monitoring so far has
allowed a preliminary understanding of the status, ecology, and movements
of migratory pollinating bats. These species continue to be monitored by
the Program for Conservation of Mexican Bats (Medelln et al., 2004). In
Arizona, a monitoring effort by the Arizona Game and Fish Department
(2006) continues to produce important information (Krebbs et al., 2005).
For example, simultaneous visits to all known roosts of the lesser long-nosed
bat in Arizona and northern Sonora have been conducted for the past few
years. The simultaneous counts constitute one of the most robust ongoing
efforts to assess the status and population dynamics of this species. Bats
congregate in their roosts so that counting them in roosts provides an accurate assessment of a large proportion of their total population.
Because of their habit of roosting in caves, identifying ecologically sig-

140
nificant caves for ongoing standardized monitoring is essential for assessing

the status of bat populations. Documenting population size and evidence
of reproduction is the most important priority, but dates of arrival at and
departure from the roosts, diet composition, and other data are important to
acquire in order to understand conservation needs (Medelln, 2003). Given
the long-distance, international movements of those species, only monitoring at large scales of multiple colonies across the species summer and winter
ranges will provide the needed information. International collaborative efforts in monitoring and conservation practices are therefore critical for the
benefit of those primarily migratory species.
REQUIREMENTS FOR ADEQUATE MONITORING OF
POLLINATORS AND POLLINATION FUNCTION
Commercial Pollinators
An accurate assessment of commercially managed pollinator status
and function is a fundamental antecedent to a rational decision-making
process aimed at recommending allocation of private and public resources
for management of commercial pollinator species. An accurate assessment
requires an unambiguous determination of the number and type of commercial pollinating units available, the quality of those pollinating units
(for example, health and strength), assessments of annual and seasonal
losses, pollination fees or purchase prices, and the crops that are pollinated
with each species. Complete and accurate data will permit statistical trend
analyses of commercial pollinator status and function, and such analyses
can provide stakeholders with a rational basis for action.
Specifically, monitoring activities could include an array of pollinationspecific characteristics. Questions could be directed to both suppliers of
pollination services (for example, solitary bee operations and bumble bee
companies), and consumers of pollination services (for example, crop growers). Questions for suppliers could include queries regarding the number of
pollination units rented or sold for pollination (by crop); in the case of honey
bees, the number of times a colony was rented in a year; and rental fees or
selling prices charged for pollinating units. For honey bees, data should be
segregated according to the crop being pollinated. Data on annual colony
losses and colony losses during the previous winter should also be collected.
Questions for growers could include queries on whether pollination services
were purchased during the previous seasons, the species involved (honey
bees, bumble bees, solitary bees), the number of units purchased or rented,
the price or rental fee paid, the crop grown, and some measure of the difficulty in obtaining the desired pollination services.
NASS is already collecting some pollination-specific data, but surveys

141
could be adjusted to acquire the information mentioned above. Moreover,

monitoring methods could be adjusted to eliminate current ambiguities in
the honey data report and data collection could be modified to include tracking of winter losses of honey bee colonies. Such information can provide
a measure of volatility in colony numbers that is not captured by current
methods.
Wild Pollinator Populations
Little is known about the status of most wild pollinators in North
America, especially for wild populations of native bees, the dominant pollinators of flowering plants on wild or unmanaged lands (Chapter 3); in
particular, there is seldom a historical baseline to which modern data can
be compared. Two sampling strategies could be employed to compensate
for the absence of relevant baseline data. First, existing historical data
could be used in conjunction with recent survey data to conduct focused
assessments of the status of pollinators in certain regions of North America.
For example, given a set of bee species collected from a specific locality
in Connecticut between 1900 and 1930, a re-survey can be conducted to
determine how many of those species can still be detected (see Box 2-3;
Biesmeijer et al., 2006). Second, a long-term annual monitoring program
could be initiated expressly to establish a baseline for evaluating status of
pollinators at different times in the future. Such monitoring, in contrast to
an assessment that provides a snapshot in time, can both illuminate trends
in species abundance and allow detection of relationships between changes
in community composition and putative environmental causes of change
(Kevan et al., 1997; Kremen, 1992; Kremen et al., 1993). Understanding
such relationships is crucial for developing plans to mitigate environmental
change and to manage for species persistence (Walters and Holling, 1990).
Although such programs are difficult to set up and maintain, the European
ALARM project (Box 5-1) provides an inspirational example of a pollinator
monitoring program across many countries.
In addition to assessing and monitoring pollinator populations and
communities, monitoring pollination function over time is important. The
relationship between the presence, absence, or abundance of a given pollinator species and the pollination service that a particular plant species
receives is complex (Bond, 1995; Memmott et al., 2004; Morris, 2003).
Relationships between plants and their pollinators are most commonly
generalized; that is, most plant species have several to many pollinating
species as visitors, and most pollinator species visit and pollinate many
different plant species (Chapter 2). In addition, asymmetric specialization,
whereby specialist mutualists can interact with more generalized partners,
appears to be common in pollinator-plant networks (Vzquez and Aizen,

144
least well-studied groups of pollinators (Proctor et al., 1996), wild bees

could be a top priority for coordinated assessment. Lepidoptera, especially
butterflies, have been utilized as a key indicator group for insects (for example, Fleishman et al., 2005) and their visibility, familiarity, and ecological
importance argue for focusing monitoring efforts on this group initially,
and then expanding to include others. That said, many of the monitoring
techniques proposed here allow simultaneous collection of observations
and samples of a wide range of flower-visiting species. Such data could be
collected and archived even if time and resources do not allow processing
and analysis immediately.
Assessment Program
Assessment programs will provide information about the status of a
wide variety of pollinators in North America. The ALARM project showed
that a before-and-after comparison based on past and recent surveys could
reveal range contractions in many pollinator species (Biesmeijer et al., 2006;
Box 2-3). The results suggest that concerns about pollinator status are
warranted. Using that project as a guide, an assessment program in North
America could include three activities:
Conduct intensive field surveys to collect, curate, and identify insect
pollinators, repeated over at least 34-year periods (because of year-toyear variability in populations and species composition; see Chapter 3), in
regions where significant historical records (late 1800s to early 1900s for
many localities in eastern North America; 1950s1970s for more recently
surveyed localities in western North America) are known to exist for pollinators (Table 5-1). Current species presence can be compared with historical records to determine the number of species that still occur in these
geographic areas (Biesmeijer et al., 2006; Marlin and LaBerge, 2001).
Capture historical data from museum collections (Anderson et al.,
2002; Biesmeijer et al., 2006; Graham et al., 2004) for selected localities
where intensive field surveys are currently being carried out for comparison
of records. (See Table 5-2 for locations and sampling dates of recent or
ongoing surveys.)
Monitor populations of selected pollinator species that are rare or
suspected to be in decline (for example, Bombus spp., Chapter 2), using
contemporary genetic or demographic techniques. For example, for bees,
recent studies suggest that measuring the proportion of diploid males (Chapter 3) may be a simple, but effective, genetic technique to determine whether
populations have experienced significant decline and are at enhanced risk for
the future (Roubik, 2003, Zayed and Packer, 2005; Zayed et al., 2004).

145
TABLE 5-1 Examples of Areas Appropriate for Repeat Survey of U.S.

Pollinator Populations (Localities, Some of Which Have Been or Are
Being Re-surveyed, Contain Substantial Collections of Bees and Other
Flower-Loving Insects)
Locality
County
State
Collection
Period
Collection
Method
Portal
Antioch Dunes
Mt. Diablo
Surprise Canyon
Altadena, La Crescenta
Tanbark Flat
Hastings Preserve
Sagehen Creek, Hobart
Mills
18 mi W Blythe
Boyd Deep Canyon Desert
Research Center
Idyllwild, Keen Camp
Palm Springs, Whitewater
Canyon
Riverside
The Gavilan
Morongo Valley
Twentynine Palms
Victorville, Apple Valley
Borrego Valley
Putah Creek and Canyon
Moldenke transect,
northern California
Boulder
Rocky Mountain Biological
Laboratory
Miami and vicinity
Moscow
Carlinville
Chicago and vicinity
Lawrence
Plummers Island
Mount Desert and vicinity
E.S. George Reserve
Hattiesburg
Raleigh
Fargo
Mesilla
Rodeo
Albany Pinebush Reserve
Ithaca and vicinity
Cochise
Contra Costa
Contra Costa
Inyo
Los Angeles
Los Angeles
Monterrey
Nevada
AZ
CA
CA
CA
CA
CA
CA
CA
19501970
19301960
19301950
19501970
1930
1950
19301940
19301960
Net
Net
Net
Net
Net
Net
Net
Net
Riverside
Riverside
CA
CA
19501970
19401970
Net
Net
Riverside
Riverside
CA
CA
19201940
19301960
Net
Net
Riverside
Riverside
San Bernardino
San Bernardino
San Bernardino
San Diego
Yolo
CA
CA
CA
CA
CA
CA
CA
CA
19301950
19301950
19301960
19301960
19301960
19301960
19501960
19601970
Net
Net
Net
Net
Net
Net
Net
Net
Boulder
Gunnison
CO
CO
19301940
19751980s
Net
Net
FL
ID
IL
IL
KS
MD
ME
MI
MS
NC
ND
NM
NM
NY
NY
1930
19301960
18901920
19201930
19301960
Net
Net
Net
Net
Net
Net
Net
Net
Net
Net
Net
Net
Net
Net
Net
Latah
Macoupin
Douglas
Montgomery
Hancock
Livingston
Forrest
Wake
Cass
Hidalgo
Albany
Tompins
19101950
1970
1940
19201950
19101950
Early 1900s
19501970
18801950
continued

146
TABLE 5-1 Continued

Locality
County
State
Collection
Period
Collection
Method
Brooklyn (Flatbush,
Prospect Park,
Floyd Bennett Field)
Gardiners Island
Corvallis
Curlew Valley
Cache Valley
Milwaukee
Laramie
Kings
NY
1890
Net
Suffolk
Benton
Box Elder, Oneida
Cache, Franklin
Milwaukee
Albany
NY
OR
UT, ID
UT, ID
WI
WY
1910
19201960
19601970
19402000
19001930
1970
Net
Net
Net, Malaise
Net, pan, Malaise
Net
Net
SOURCE: J. Asher, American Museum of Natural History, and T. Griswold, USDA, personal
communication, October, 2005; Procter, 1946.
Monitoring Pollinator Communities and Pollination Function

A useful monitoring program must employ standardized, tested, repeatable methodology applied with sufficient spatial and temporal replication
to ensure confidence and allow interpretation of time trends in the resulting data. Describing the many factors that must be taken into account in
designing a monitoring program is beyond the scope of this report, but
such factors are discussed by Elzinga et al. (2001) and Potts et al. (2005).
Monitoring programs can be designed to assess specific techniques to guide
management, or they can be designed to track trends over time to assess the
changing status of species or ecosystems (Kevan et al., 1997; Kremen et al.,
1993). The latter type of program is most appropriate for monitoring both
pollinator communities and pollination function across large geographic
regions such as North America.
Monitoring insect populations and their function as pollinators presents
certain challenges. Many species can be identified only by a professional
taxonomist or are not yet described so that the taxonomic impediment
(Box 2-1) can be a significant obstacle (Kremen et al. 1993; OToole, 2002).
In addition, insect populations tend to experience large interannual or interseasonal changes in abundance (Roubik, 2001; Wolda, 1988), making detection of temporal trends difficult. Insect communities often include many rare
species (Magurran, 1988) and rare species are inherently less amenable to
monitoring with confidence across space and time. Complicating the process
of evaluating insect communities is that variation in composition can be
extremely high, even in samples from nearby areas of the same habitat type,
or at the same site across time (Williams et al., 2001). Thus, any monitoring
program focusing on insect pollinators must address both the taxonomic
impediment and the challenge of collecting data with sufficient spatial and
temporal resolution to allow trend detection.
UT
CA
San Rafael Desert

Death Valley National
Park
Pinnacles National
Monument
NM
White Sands Missile

Range
20032005
19992000
20012002
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Digitized
10,000
3,000
5,000
23,021
6,783
99,156
67,617
25,196
12,218
7,065
Records
>250
125
>200
223
647
598
398
333
270
Species
SB
SB, U.S.
Army
SB, U.S.
Army
TG
TG
OM,
TG
TG
OM,
TG
TG
TG
Data
Ownera
Pan
Net, pan
Pan
Net, pan
Net, pan
Net
Net, pan
Net, pan
Net
Net, pan
Collection
Method
Time
Monthly
Monthly
Monthly
Biweekly
Biweekly
Biweekly
Biweekly
Biweekly
Standard
Interval
Plot
aData owner: TG: T. Griswold, USDA-ARS; OM: O. Messinger, USDA-ARS; SB: S. Buchmann, University of Arizona, Tucson.
SOURCE: T. Griswold, USDA-ARS, personal communication, October 2005.
FL
AZ
Avalon Plantation
Yuma Proving Ground
20042006
UT
CA
20032004
UT
Grand StaircaseEscalante National

Monument
Dugway Proving
Grounds
Yosemite National Park
1998,
20042005
20002003,
2005
NV
19791993
19931995,
19992000
19961999
Collection
Period
Clark County
CA
State
Location
Biweekly on
dunes
Trail segments
systematically
sampled
Identifications
not complete
Identifications
not completed
for 2005
Identifications
not completed
for 2005
Identifications
not complete
Notes
TABLE 5-2 Examples of Modern Inventory Areas for Bee Pollinators (Corresponding Museum Data Could Be
Captured for the Listed Localities to Compare Between Historical and Modern Records and Provide a Status
Assessment)


147

148
A cost-effective approach to addressing the two kinds of obstacles to

monitoring insect pollinators might be to involve both professional scientists and citizen-scientists in the effort (Lepczyk, 2005). The professional
science component provides the scientific rigor and detail needed for robust
assessments of biodiversity response to changes in management practices
(Bednarek and Hart, 2005; Noss, 1990). The citizen-scientist component
may then increase the temporal and spatial breadth of studies that can be
conducted at minimal cost, but at a sacrifice of some quality in the data
(Table 5-3). Studies conducted by citizen-scientists could be carried out at
low taxonomic resolution (for example, bumble bee, flower fly rather
than identifications at the genus or species level), thereby circumventing the
difficulty in identifying most pollinating insects caught in field studies to
the species level. Careful integration of citizen-scientist efforts with professional efforts (for example, calibrating the data collected by citizen-scientists
against that from the professional scientist programsee below) is necessary
to optimize the utility of the resulting data. An important added advantage
to including citizen-scientists is that it builds appreciation and understand-
TABLE 5-3 Pollinator Long-Term Monitoring Program: Comparison of

Professional and Citizen-Scientist Monitoring Programs
Number of sites
Type of sites
Taxonomic
resolution
Temporal
resolution
Pollinator
status
measurement
Pollinator
function
measurement
Goals
Benefits, costs,
and caveats
Professional
Citizen-Scientist
50100
Gradients of disturbance and sites
shared with citizen-scientist
program
High: genus and species
Many
Many, of interest to citizens
High: monthly, biweekly, or daily
Low: operational taxonomic units

such as bumble bee, sweat bee,
flower fly
Low: often annual
Species richness, relative

abundance, identity (specimens)
Counts of operational taxonomic

units (observations)
Pollen limitation for plants

with varied breeding systems,
including species studied by
citizen-scientists
Higher resolution of data along
land use change gradients
Calibration of citizen-scientists
data
Provides high-quality data but at
high cost
Fruit or seed set for self-incompatible

plants; bulbil counts on agaves in
Mexico
Data from more sites than
professionals could survey alone
Public involvement in pollinator
monitoring, conservation
Provides large quantity of data
at low cost but must be tested,
calibrated

149
ing of pollinators among stakeholders (for example, Condon, 1995; Kevan,

1975a). Examples of successful citizen-scientist monitoring programs that
have yielded scientifically valid monitoring data with potential to assist in
conservation and management of various species include the Tucson Bird
Count (Turner, 2003; Turner et al., 2004), the Breeding Bird Survey (Mineau
et al., 2005; Vance et al., 2003), and the House Finch Disease Survey (http://
www.birds.cornell.edu/hofi/) of the Cornell Ornithological Laboratory (Altizer et al., 2004; Dhondt et al., 2005).
Professional Science Programs
The professional science program could be designed with two goals in
mind: (1) to obtain an intensive, detailed data set to use in determining the
long-term effect of land use change (the dominant force enhancing extinction rates and altering ecosystem processes; Millennium Ecosystem Assessment, 2005) on pollinator communities and pollination function, and (2) to
obtain targeted data for a small number of sites with the goal of calibrating
the data from the citizen-scientist programs to make the data from those
programs more useful.
To assess the influence of land use change on pollinator communities, the professional scientist monitoring program could also monitor
sites across an existing land use gradient, from relatively pristine natural
habitats to extensively anthropogenically altered habitats. Studies across
environmental gradients provide immediate information about the effects
of land use change. They trade spatial coverage for (see also Greenleaf and
Kremen, 2006a,b) time coverage by providing an estimate of the correlation
between the accumulated environmental characteristics associated with different degrees of land use change and the community or functional characteristics. For example, Kremen et al. (2002b) found that the intensification
of agriculture in California, from small-scale organic farms near natural
habitats to large-scale conventional farms isolated from natural habitats,
greatly reduced the diversity and abundance of wild pollinators at watermelon and other crops, and hence the services provided. In the intensively
farmed region, many common species known from historical records have
disappeared (Kremen et al., 2002b; Larsen et al., 2005). Thus a snapshot
study can provide a useful amount of information about the local status of
pollinator species (see also Kevan, 1975a; Kevan et al., 1997; Scott-Dupree
and Winston, 1987).
Land use change is dynamic; for example, in the United States, European colonization was accompanied by extensive conversion of forested
lands to agriculture, but those trends have since been replaced by afforestation (Caspersen et al., 2000; Lepers et al., 2005). In some regions, both
forested and agricultural areas are being converted to urban or ex-urban

150
areas (Brown et al., 2005). The different land uses are likely to have radically different effects on pollinator communities (for examples, see Cane
et al., 2006; Chacoff and Aizen, 2006; Frankie et al., 2005; Klein et al.,
2002; Kremen et al., 2004; Ricketts, 2004; Winfree et al., 2006), and thus
on pollination function (Herrera, 2000; Larsen et al., 2005; Memmott et
al., 2004). Grixti and Packer emphasized in their paper (2006) that pollinator assemblages change with successional advances in vegetation, even in
urbanized locations. Both community composition and function could be
monitored over time along land use gradients.
To calibrate the data obtained from the citizen-scientist program, the
professional scientist program would need to involve data collection at a
much higher spatial, temporal, and taxonomic resolution in selected areas
that overlap with the citizen-scientist program (for example, at urban gardens
in the northeastern United States, and on vegetable farms in Californiasee
below). Data for the most part could be specimen-based. Specimens can
be identified to species by professional taxonomists in combination with
trained para-taxonomists (as in the INBioInstituto Nacional de Biodiversidadprogram in Costa RicaJanzen, 2004; and the All Taxa Biodiversity
Inventory in the Great Smoky Mountains, http://www.dlia.org/index.shtml).
Such data can be analyzed to determine the degree of association between the citizen-scientist data and the professional scientist data (see also
Bhattacharjee, 2005; Danielsen et al., 2005; Gaidet-Drapier et al., 2006).
Citizen-Scientist Programs
A proposed citizen-scientist program could use simple measures of
pollinator abundance (such as the number of bees observed at flowers) and
pollination function (such as seeds set within fruits or flower-to-fruit ratios
on target plants) that could be correctly implemented by nonscientists with
minimal training. Inexpensive identification guides could be made available
following the online model of Discover Life (http://www.discoverlife.
org/) developed by John Pickering at the University of Georgia, Athens,
or Frogwatch (run jointly by the National Wildlife Federation and USGS,
http://www.nwf.org/frogwatchUSA/).
Programs could be designed and coordinated by scientists, possibly
working in public-private partnerships (as is the case with Frogwatch), but
implemented by citizens, educators, and students. Such a program could be
carried out over a large number of localities, in places that people frequently
visit and care about (such as urban gardens and accessible nature reserves).
Data can be collected at a relatively coarse temporal and taxonomic resolution, with the goal of long-term annual monitoring of common species
and easily recognizable guilds (for example, bumble bees, carpenter bees,
and flower flies). Simple, easily implemented observational techniques and

151
measurements are ideal for this enterprise (for examples, see Methods section below). Use of websites for data entry and to view data is desirable
because it allows participants to gain immediate feedback about their work
and enhances their motivation (see http://www.tucsonbirds.org/results/ and
http://www.eman-rese.ca/eman/datamanage.html for examples). Many excellent examples of existing citizen-scientist monitoring programs provide
models (for example, Frogwatch, Monarch Watch, Tucson Bird Count,
Illinois Butterfly Monitoring Network, http://www.bfly.org/, Canadas Ecological Monitoring and Assessment Network, and others).
Methods
Monitoring Pollinator Status
The professional scientist program could use a combination of specimenbased and observation methods to monitor species abundance (Potts et al.,
2005), whereas observational methods are best suited to citizen-scientist
programs. Many methods are available for collecting pollinator specimens
(Potts et al., 2005), and archiving voucher specimens in a recognized museum collection is a requirement for identification of many species, especially
insects. Methods include netting visitors at flowers or trapping pollinators
in pan traps, trap nests, or Malaise traps. Netting visitors at flowers is an
active sampling method that requires training, and results from this method
vary greatly depending on the skill of the netter. All of the other methods
are termed passive sampling methods; these do not require great skill and
are therefore less subject to inter-investigator biases, but trap placement and
collection must be conducted in a highly standardized manner, both within
and between sites. Investigators conducting surveys utilize a combination of
methods, because a single method is rarely suitable for capturing all species
present (Cane et al., 2000; Potts et al., 2005). A standardized protocol developed in North America for sampling bees and other pollinators includes
both active and passive sampling methods and is listed at http://online.sfsu.
edu/~beeplot/pdfs/Bee%20Plot%202003.pdf. For the passive, pan-trap
sampling methods, some testing has been conducted to determine the effects
of bowl color emission spectrum, bowl size, bowl spacing, type of soap utilized in water, and length of time operated. These tests suggest that yellow,
blue, and white UV-emitting bowls are the most effective for trapping pollinators, and that bowls should be spaced at least 5 m from each other for
maximum efficiency. Dish-washing detergent should be used in the water to
break surface tension. The size of bowl used for sampling duration did not
affect the number of pollinators caught (http://online.sfsu.edu/~beeplot/).
Other standardized protocols involving these and other methods are currently being tested in Europe by the ALARM project (see Box 5-1).

152
Pollinator communities and populations can also be monitored through

visual observation (Potts et al., 2005). Identifying insect pollinators to species on the wing is difficult and requires extensive training in most cases.
Thus, monitoring programs relying on visual observation will necessarily
be conducted at a coarse taxonomic resolution, except in rare cases involving extremely familiar and exceptionally recognizable species such as Apis
mellifera or Danaus plexippus. Such resolution may be appropriate with
a minimum level of training for a citizen-scientist monitoring program for
pollinators. Citizen-scientist monitoring programs have also been developed
for birds and bats in Mexico and for birds in the United States (for example,
Breeding Bird Survey, http://www.pwrc.usgs.gov/bbs/).
To standardize sampling, both visual observation and specimen sampling must be conducted only under specified weather conditions (sun, cloud
cover, temperature, wind) and time of day or season, in predetermined
sampling units of time (for example, a given number of minutes per sample,
and samples per site per day) and space (transects or plots) to achieve equal
sampling effort between sites (Dafni et al., 2005).
Monitoring Pollination Function
A standard method for monitoring pollination function, well suited
to the professional scientist program, is to measure pollen limitation
(Box 4-2) and in doing so determine whether focal plants become more or
less pollen-limited over time or with land-use intensification. Pollen limitation is measured by comparing reproduction on flowers that are experimentally cross-pollinated (by hand-pollinating the flower with pollen from
another individual) against control flowers on the same plant and on an
adjacent, companion plant that are pollinated under ambient (open) conditions (Dafni et al., 2005; Kearns and Inouye, 1993; Box 4-2). Use of potted
plants placed in different environments minimizes differences in plants due
to nutrition, genetics, and other variables.
A simpler method that could be used by citizen-scientists is to monitor
a self-incompatible, pollinator-dependent plant over time and assess fruit
or seed set. Accessible techniques for assessing breeding systems are available in Bernhardt and Edens (2004) and Dafni et al. (2005). Monitoring of
pollination function in this manner over time, or along land use gradients,
provides a valuable companion data set to that gathered on pollinator
abundance trends.
Alternative methods for monitoring pollination function may exist for
specific plants and their pollinators. For example, in the deserts of Mexico
and the southwestern United States, monitoring of bulbil production by
agaves may provide a simple but effective measure of ecosystem pollination
services provided by vertebrate organisms, usually bats. Agaves can repro-

153
TABLE 5-4 Areas for Monitoring Pollination Function Using Agave

Bulbil Production
Area
Region or State
Country
Caon de Santa Elenaa

Central Mexican Highlandsb
Chiricahua Mountainsa
Chisos Mountainsa
Cumbres de Monterrey National Parka
Hatchet and Animas Mountainsa
Maderas del Carmena
Sierra Madre Occidentala
Sierra Madre Occidentala
Tehuacn Valleyc
Trans-Mexican Volcanic Beltb
Northwestern Chihuahua
Hidalgo, Puebla, Tlaxcala
Southeastern Arizona
Big Bend National Park, Texas
Central Nuevo Len
Southwestern New Mexico
Northwestern Coahuila
Northeastern Sonora
Northwestern Chihuahua
Southern Puebla
Morelos, Michoacan, Jalisco,
Colima
Mexico
Mexico
United States
United States
Mexico
United States
Mexico
Mexico
Mexico
Mexico
Mexico
aArea
bAgaves
vegetation dominated by agaves.

locally abundant.
cAgaves dominate vegetation in the southernmost stretch.
duce vegetatively by producing shoots and rhizomes, or sexually by producing seed-bearing fruits in the stalk after successful pollination (Arizaga
and Ezcurra, 1995, 2002), but when pollinators fail to appear, agaves may
produce aerial bulbils in the flowering stalk (Arizaga and Ezcurra, 1995). In
the Tehuacan Desert of central Mexico, about 5 percent of the plants were
never pollinated and instead produced bulbils (Arizaga and Ezcurra, 2002).
Monitoring the frequency of bulbil production in selected areas (Table 5-4)
may provide a direct indicator of pollinator availability or pollinator service
to agaves.
CONCLUSIONS
Current monitoring systems for commercial pollinators, chiefly Apis
mellifera, exist, but these fail to report or capture all of the necessary data
to monitor pollinator status and function. In particular, new questionnaires
directed at both the beekeepers and growers need to be developed to capture
information on pollination by agricultural commodity. Several monitoring
programs also exist for specific taxa or functional groups of pollinators, but
many of these programs are either run by individual scientists, and are therefore limited in scale and not sustainable over the long term, or by citizenscientist groups, and are therefore limited in precision and repeatability.
For pollinators, the ALARM project of the EU provides an excellent
model for monitoring and includes development and testing of monitoring
methods. In addition, some excellent models exist for a variety of taxa that

154
couple professional and citizen-scientist collection efforts. The combination

of professional and citizen-scientist collection efforts extends the potential
for data accumulation, although testing and calibration are needed to assure data quality and validity. A monitoring program could be developed
for long-term assessment of pollinator status and function using both
professional and citizen-science elements. To address the enormous spatial
and temporal variability in pollinator populations as well as the taxonomic
impediment, calibration systems could be developed to determine the degree
of correspondence between data collected by professional scientists at a fine
taxonomic resolution, and data collected by citizen-scientists at a coarser
resolution. If valid calibrations can be developed and data quality can be
assured, use of both types of data sets is likely to provide more information
germane to evaluating pollinator status in time and space at a relatively
low cost.
Legacy data (specimens archived in museums) could be captured digitally and utilized (more extensively than has been done to date) to provide
a baseline for assessing the status of pollinators in North America today.
Areas where substantial legacy data exist should be re-surveyed; areas where
contemporary surveys are ongoing should be targeted for digital capture of
historical specimen data.

6
Strategies for Maintaining Pollinators
and Pollination Services
Although information on the status of most pollinators is incomplete,

much can be done to maintain commercial and wild pollinator populations
and to prevent future shortages of pollination services. The sustainability of
the European or western honey bee (Apis mellifera), the principal managed
pollinator in North America, could be buttressed through the development
and adoption of parasite- and pathogen-resistant stocks of bees. Several
developments could help the bee industry reach this goal: use of modern molecular techniques for identifying superior Apis stocks, effective methods for
the preservation of honey bee germplasm, a suitable infrastructure for maintenance and use of resistant stocks, and adoption of practices by commercial
queen producers and beekeepers that are consistent with these goals.
The development of mite- and pathogen-resistant stocks, however, is
a long-term solution, one that will require extensive collaboration among
researchers, extension personnel, and the queen-and-package industry. In
the meantime, beekeepers require immediate relief. Other pest management
strategies include programs that mitigate the effects of pesticide resistance
in mite populations and cultural and other nonchemical techniques for disease management in commercial hives. Management techniques also must
be implemented to reduce the impact of Africanized honey bees, which
have begun to colonize areas of the United States critical to the beekeeping
industry. The development of methods that support the commercialization
of non-Apis pollinator species is also a high priority.
For wild, unmanaged pollinators, the most important goals involve
conservation and restoration of habitat. Many pollinators can survive in
small habitat patches and use the resources in natural areas, wildlands,
155

156
and even human-dominated areas including appropriately managed farms,

urban parks, and golf courses. Small changes could produce substantial
benefits, but basic information on the resource requirements of a wider variety of pollinator species is needed to improve habitat management. Also,
economic and policy incentives would encourage the stewards of a wide
range of urban and rural areas to adopt pollinator-friendly practices and
also to encourage information exchange and outreach. The most effective
and sustainable route to stability in pollination services is to identify and
implement practices that promote the availability of diverse commercial
and wild pollinators.
MAINTAINING COMMERCIAL POLLINATORS
Apis mellifera: Problems and Solutions
The beekeeping industry is at a critical juncture as it faces a suite of
challenges that defy easy solution. The parasitic honey bee mite Varroa destructor, now ubiquitous in North America, is the single greatest threat to a
sustainable supply of healthy and affordable honey bee colonies worldwide
(DeJong, 1990; DeJong et al., 1982a, 1984). Major wintertime losses of
honey bees in the United States every few years since 1993 (Burgett, 1994;
Caron and Hubner, 2001; Finly et al., 1996; Lumkin, 2005) are almost
certainly attributable to varroa mite infestation, which was exacerbated by
the evolution of resistance to standard miticides. The tracheal mite Acarapis
woodi also contributes to the periodic catastrophic winter losses, but reliable data on its prevalence in North America are not available. There are
effective treatments for management of tracheal mites, including trachealmite-resistant stocks of bees (Chapter 3). Problems with tracheal mites,
to the extent that they exist, can most likely be ameliorated by improved
detection and control among beekeepers.
Another serious challenge to the beekeeping industry is the Africanized
honey bee, which has colonized several regions of the United States that
are important to the commercial queen-and-package bee industry (northern
California and the southeastern United States). The bees also migrate with
beekeepers to hospitable wintering grounds. Because the Africanized bees
have several traits that are undesirable for beekeeping (Chapter 3), it is
imperative that the genotype be prevented from coming to predominance
in the United States and Canada. The bees presence in the southeastan
important area of queen-and-package production for the rest of the United
States and a primary wintering ground for beekeepers (Chapter 3)makes
this objective paramount.

STRATEGIES FOR MAINTAINING POLLINATORS AND SERVICES
157
Resistant Honey Bee Breeding

A long-term solution to the problems of parasitic mites and honey
bee pathogens is the development of resistant stocks of bees. Several traits
associated with varroa mite resistance are heritable (that is, available for
selection) (Camazine, 1986; Camazine and Morse, 1988; DeJong, 1996;
Harbo, 1992, 1993; Harbo and Harris, 1999a,b; Harbo and Hoopingarner,
1995; Harbo et al., 1997; Moritz, 1985; Moritz and Hanel, 1984; Rinderer
et al., 2003). Similarly, tracheal mite resistance is a heritable trait (Gary et
al., 1990; Page and Gary, 1990). A varroa-resistant stock of honey bees
was developed at the U.S. Department of Agriculture (USDA) Agricultural
Research Service (ARS) honey bee research laboratory in Baton Rouge,
Louisiana (Harbo and Harris, 1999a), and is available commercially as
SMR (suppressing mite reproduction) or SMART stock.
Related efforts also have focused on identifying honey bee populations
with a long history of exposure to V. destructor as a potential source of resistant stock (Rinderer et al., 1999, 2001, 2003). ARS began to import bees
from the Primorsky region in far-eastern Russia beginning in the early 1990s
(Rinderer et al., 2005). The Russian bees were quarantined on an island off
the coast of Louisiana, and they have been subject to further selection. The
Russian bees exhibit a high degree of varroa mite resistance (Rinderer et al.,
2003, and references therein), and they are now available commercially.
Resistance to American foulbrood and other bee pathogens was shown
to be heritable in the 1930s (Park, 1936). Although other traits contribute
to foulbrood resistance (Spivak and Gilliam, 1998a,b), the principal mechanism is hygienic behavior (Rothenbuhler, 1964). Stocks that exhibit hygienic
behavior have been developed at least three times since the 1930s (Park et
al., 1937, 1939; Rothenbuhler, 1964; Spivak and Reuter, 2001). Hygienic
behavior also could operate in mite resistance (Boecking et al., 2000; Harbo
and Harris, 2005; Spivak and Rueter, 2001), and the University of Minnesota has developed hygienic stocks that are available commercially.
Another challenge to the bee industry is the synthesis of results from federal and academic research into sustainable commercial queen-and-package
operations. There are well-developed methods for quantifying resistance to
mites and pathogens (Harbo and Harris, 1999a; Harbo et al., 1997; Spivak
and Downey, 1998; Spivak and Gilliam, 1998a,b) and for breeding and
maintaining resistant stocks (Harris et al., 2002; Page and Laidlaw, 1982a,b;
Page et al., 1983, 1985). Perusal of trade journals reveals beekeepers interest in mite-resistant stocks of bees and the low availability of such stock:
Several suppliers advertise Russian, SMR, or hygienic bee stocks, but there
are no data on the number or quality of queens available. It is not clear why
resistant stocks have not yet been widely adopted (Sheppard, 2006), but it
is possible that the impediments include the difficulty of maintaining inbred

158
lines, the negative consequences of selecting one trait over others that are
commercially important (Page and Laidlaw, 1992), and the time and effort
involved in replacing queens (Laidlaw, 1992).
Of particular importance is the lack of locally adapted stocks. Typically,
although not universally, southern queen producers use stocks that perform
well in the warmer south but that might not do well in the north, where
winters are more severe. This is especially problematic for stocks that are
affected by tracheal mites or diseases such as chalkbrood, both of which
affect bees more in the cooler, damper regions of the north (Flores et al.,
1996). Establishing locally adapted populations of bees is difficult because
more than 500,000 queens are shipped each year throughout the country
from southern production sites (Schiff and Sheppard, 1995, 1996).
Instrumental insemination (Laidlaw, 1992) is ideal for bee-breeding
programs (development and maintenance), although it is more costly than
is natural mating. Moreover, the honey bee mating behavior presents a
challenge to the development and maintenance of selected lines of honey
bees. Honey bee queens are naturally polyandrous (Winston 1987), mating
with 717 drones on 15 mating flights, usually within the second week of
life. Queens and drones fly to discrete spaces in drone congregation areas,
located some distance above the ground and away from their nests. Mating
takes place as the queen flies through one or more drone congregation areas,
where the sources of drones are uncontrolled. It is not clear whether some
percentage of mating with a specific desired stock is necessary to ensure
a mite- or pathogen-resistant colony (Box 6-1) and likely depends on the
genetic mechanisms involved (dominance, additive, epistasis).
Most commercial queen producers probably do not use resistant stocks,
and most queens shipped throughout the United States apparently still come
from susceptible stocks of bees. Susceptible queens also produce drones that
flood local mating areas, so it is difficult to establish a sustainable resistant
population.
Genetic Solutions to Problems with Mites and Pathogens
Genomics and germplasm preservation could be used to facilitate the
development and maintenance of selected honey bee stocks. The traditional
breeding process could be augmented through the use of genetic markers
(expressed sequence tags and quantitative trait loci) for desirable traits.
Markers already have been identified for defensive behavior (Hunt et al.,
1998) and for hygienic behavior (Lapidge et al., 2002), and more research
could facilitate development of commercially viable selected stocks of honey
bees. The recent sequencing of the honey bee genome by the Baylor College
of Medicine (The Honeybee Genome Sequencing Consortium, 2006) and

BOX 6-1
Development and Maintenance of Selected Stocks:
Controlled Mating

The development and maintenance of selected stocks and breeder
queens require controlled mating, generally through instrumental insemination (Laidlaw, 1992). Breeder queens (selected queens inseminated
with semen from selected drones) are transferred or sold to commercial
queen producers who use them to produce large numbers of production
queens for sale to beekeepers. The parentage of the production queens
is controlled through the use of breeder queens. Before a production
queen is sold to a beekeeper, it is first mated to several drones, and the
mating of production queens is invariably natural. Because commercial
queen producers cannot completely control the sources of the drones that
mate with their production queens (Laidlaw and Page, 1998), the queens
often mate with drones from unselected stocks of local wild bees or from
colonies belonging to other beekeepers. Thus, production queens will
often produce hybrid workers that do not exhibit the desired traits or that
do not exhibit those traits to the desired extent, depending on the genetic
basis of the variation under selection (for example, dominance, additive,
epistasis).

The percentage of matings that must occur with a specific desired
stock to ensure a mite or pathogen resistance in a colony is not known
and could depend on the trait. Some work suggests that open-mated
queens from selected stocks can produce colonies with usefulbut
incompletemite resistance (Harbo and Harris, 2001; see also Spivak
and Reuter, 1998, and Spivak et al., 1995, for response to American foulbrood), but another report suggests that both male and female parents
should be from selected stocks (Harris and Rinderer, 2004).

Although instrumental insemination is currently complicated for use
in commercial queen production, there are other options for controlling
commercial matingdrone saturation and isolation (Laidlaw and Page,
1998). The former achieves varying degrees of controlled natural mating
by stocking mating areas with large numbers of drone source colonies
from the desired selected source (Hellmich, 1986, 1991; Hellmich et al.,
1988). The latter uses isolated mating yards to control mating. The opportunity to employ isolation is limited because a separation of several
kilometers from other sources of drones is required.
159

160
related developments in honey bee genomics (Robinson et al., 2005) provide

outstanding resources for these efforts.
Maintaining selected stocks of honey bees is difficult because of the
generally uncontrolled mating behavior of queens and because queens have
relatively short and unpredictable lives of 13 years (Seeley, 1985). Given
the ephemeral nature of honey bee stocks, honey bee germplasm (sperm,
eggs, embryos) is an ideal candidate for preservation, which would allow
stakeholders an economical way to maintain large quantities of desirable
germplasm from a nearly unlimited number of sources. The benefit seen in
the increased access to resources would well justify the investment required to
identify or develop the germplasm. This work would fit within the mission of
the USDA National Animal Germplasm Program (http://www.ars-grin.gov/
animal/), which coordinates and supports the cryopreservation of U.S. animal
genetic resources (Blackburn, 2002). Preservation of honey bee germplasm
has been attempted, so far with limited success (Collins, 2000, 2004).
Transition to Resistant Stocks
Converting the current U.S. honey bee population to one that is resistant
to parasites and pathogens is an enormous challenge that would require
unprecedented cooperation among queen producers and consumers, federal and university research facilities and extension programs, and, most
important, beekeepers. A successful transition would require improved
identification methods, including the use of genetic markers in mass screening for desirable traits; new stocks that are viable in several regions; an
industry infrastructure that maintains superior stocks; and a mechanism for
third-party certification of new product lines. Certification of breeder stock,
mating technology, production methods and facilities, and commercially
produced bees and queens would be necessary.
Managing Miticide Resistance
Pesticide resistance has become the major problem for the management
of parasitic mites. Populations of V. destructor that exhibit resistance to
fluvalinate (Baxter et al., 1998; Elzen et al., 1998, 1999a,b,c,d; Hillesheim
et al., 1996; Macedo et al., 2002), coumaphos (Elzen and Westervelt, 2002;
Milani and Della Vedova, 1996; Pettis et al., 2004), or amitraz (Elzen et al.,
1999c, 2000) are widespread.
Resistance management programs would provide beekeepers with a
significant tool for mite management. Such programs could be built around
results from several areas of research, including projects on the mechanisms
and management of resistance to various pesticides (Gerson et al. 1991; Ting
et al. 2003; Wang et al. 2002; Wu et al. 2003), the identification of genetic

161
correlations among resistance mechanisms, determination of the fitness

consequences of pesticide resistance, and determination of optimal intervals
for pesticide rotation (Hall et al. 2004).
The industry also could benefit from the development of synergists to
inhibit enzyme-based resistance in mite populations, thereby restoring the
effectiveness of existing miticides. And the identification of new, less toxic
pesticide compounds derived from natural products would provide beekeepers with still more options. In particular, the work should focus on improving the efficiency and reliability of such commercial products as Mite-Away
II and other soft chemicals (Apiguard and Api-Life VAR).
The design of resistance management programs could follow up results
from research projects outlined above. Although there are no comprehensive
programs for beekeepers, there is considerable literature that could be used
as a starting point for research on pests of bees (see Batabyal and Nijkamp,
2005; Benting et al., 2004; Comins, 1986; Elzen et al., 1999b; Georghiou,
1980; Green et al., 1990; Hall et al., 2004; MacDonald et al., 2003; Phillips et al., 1989; Thompson, 2003; Walker-Simmons, 2003; Williamson et
al., 2003).
The tracheal mite has dropped into relative obscurity over the past decade, overshadowed by problems with varroa mites. The current effects of
tracheal mites on honey bee populations are not known. Fortunately, several
remedies are available for control of tracheal mites, including grease patties (made from vegetable shortening and granulated or powdered sugar)
(Baxter et al., 2000; Calderone and Shimanuki, 1995; Liu and Nasr, 1993;
Wilson et al., 1989), formic acid (Baxter et al., 2000; Feldlaufer et al., 1997;
Hoppe et al., 1989), and menthol (Baxter et al., 2000; Duff and Furgala,
1993; Wilson et al., 1989, 1990). Amitraz, although not currently marketed,
also can be effective against tracheal mites under some circumstances (Duff
and Furgala, 1993; Wilson and Collins, 1993). Treatment results have been
mixed (Duff and Furgala, 1993; Scott-Dupree and Otis, 1992), and honey
bee populations have evolved resistance to tracheal mites (Gary et al., 1990;
Page and Gary, 1990), an attribute that likely has contributed to a reduction
in concern about this pest.
There is an additional economic benefit to deploying mite-resistant
bees and reducing pesticide useover and above the savings realized from
eliminating the need to purchase chemical pesticides. The use of resistant
stocks allows beekeepers to eliminate pesticide use, and some beekeepers
could potentially sell their products at a premium (NRC, 2000).
Other Methods of Managing Parasites and Pathogens
Nonchemical control methodssuch as cultural methods or biological
controloffer many advantages for beekeepers. Combined with third-party

162
certification of honey (as pesticide-free or organic, for instance), those

methods expand the beekeepers options in the marketplace, enabling them
to take advantage of the more lucrative trade in natural foods. Among the
cultural methods for mite control, drone brood removal, which exploits
mite preference for drone brood, can be effective albeit labor-intensive
(Calderone, 2005). The Beltsville screen insert, a piece of wire mesh inserted
35 cm between a hives bottom and its bottom board, traps the mites that
typically fall to the bottom of the hive as bees groom to rid themselves of
mites. The insert prevents the mites from climbing back up to reinfest the
bees. The screen insert has yielded mixed and generally disappointing results
(Ellis et al., 2001; Harbo and Harris, 2004; Pettis and Shimanuki, 1999;
Rinderer et al., 2003), but it could become an effective management tool
if it were combined with pesticides that have a rapid knockdown effect for
application during honey-producing months.
The fungal pathogens Hirsutella thompsonii and Metarhizium anisopliae have shown promise as potential biological control agents for varroa
mites (Kanga et al., 2003a,b), but problems with the pathogens sensitivity
to temperature and spore distribution within hives remain unsolved. If these
could be overcome, biological control could become a viable option for
managing parasitic mites.
Perhaps even more important than developing new treatments for bee
diseases and parasites is reinforcement of regulations aimed at prevention. Protection of North America against invasive pests and diseases from
abroad is the cornerstone of pollinator protection on the continent, but
existing regulations should be strictly enforced and strengthened to remain
effective. The Federal Honey Bee Act of 1922 prohibits the entry of honey
bees from countries where diseases and parasites harmful to honey bees are
known to exist (USDA-APHIS, 2002). The act authorizes the Animal and
Plant Health Inspection Service (APHIS) to regulate importation of honey
bees in the United States. In 2004, APHIS changed the regulation to allow
honey bee packages from Australia and New Zealand to be imported to
pollinate California almond groves (USDA-APHIS, 2004).
Although honey bee colonies from Australia and New Zealand can offer a short-term benefit in the pollination marketplace, great care must be
exercised to ensure that they do not carry new pests, parasites, pathogens,
and predators. APHIS and corresponding agencies in Canada and Mexico
should conduct periodic, coordinated monitoring of honey bee populations
to determine whether specific pests are present. Target species for monitoring should include Tropilaelaps clareae (parasitic mite), Hyplostoma fuligineus (large hive beetle), Varroa spp. and V. destructor haplotypes that are
not present in North America, Apis mellifera scutellata (African honey bee),
Apis mellifera capensis (another potentially invasive subspecies of honey bee
from South Africa), and other Apis species. APHIS could coordinate the

163
efforts with cognate agencies in Mexico and Canada. State departments of

agriculture should be included in the development of monitoring programs
and could provide valuable personnel. Shipments of bees from countries or
territories that have pests that are not already present throughout North
America should not be permitted if long-term safeguarding of North American pollination capacity is a priority.
APHIS should carefully assess the integrity of inspection in countries
interested in supplying bees to North America, and it should collect and
analyze samples of adult and immature honey bees from producers who
wish to ship to North America. Sampling in the countries of origin is necessary because the bees could have pests that are currently unidentified and
therefore not on the list of target species. Also, North American countries
should proceed with research on honey bee pests in the potential source
countries that have not yet arrived in North America to prepare the countries beekeeping industries for possible or eventual introductions.
Africanized Honey Bees
The consequences of the Africanized honey bee (AHB) infiltration of
U.S. and Canadian honey bee populations are difficult to predict. However, uncertainty and precedent in other nations suggest that it is prudent
to prepare for the worst. There are three general methods for managing
AHBs: eradication, genetic isolation, and breeding (http://www.ces.ncsu.
edu/depts/ent/notes/Bees/ahbactionplan2001.pdf). Several states, including
North Carolina, have developed action plans that include recommendations for best management practices for beekeepers, and procedures for
abatement, quarantine, outreach, and first-responder training. Other states
should develop similar plans, and much of the information they need is
available from existing resources.
Eradication is most effective against confirmed or suspected founder
colonies that are inadvertently imported by truck or ship, but before the
Africanized bees can become established. Genetic isolation is achieved
through various controlled-mating techniquessuch as geographic isolation, instrumental insemination, and drone saturation (Laidlaw and Page,
1998). Geographic isolation requires European honey bee production
apiaries to be established at a distance from AHB colonies that is sufficient
to prevent mating of the European queens with the Africanized drones.
Queen-and-package producers might be able to use this method to a limited
degree by placing operations in places that are so far free of Africanized
bees: the northern United States, Hawaii, Canada, Australia, and New
Zealand. Northern U.S. and Canadian operations could be of limited use,
however, because the colder weather prevents production of queens and
packages until late in the season. The United States began to import honey

164
bee packages from Australia and New Zealand for early-season pollination
after winter losses in 20042005 (Sumner and Boriss, 2006). Australia,
New Zealand, and Hawaii could be important sources of uncontaminated
germplasm in the future, but extreme vigilance would be needed to ensure
that additional invasive diseases or pests not be introduced.
A second way to control mating is through instrumental insemination
(Laidlaw, 1977), which allows for control of male and female sources of
germplasm and for maintenance of a secure, closed breeding population.
Instrumental insemination is a highly effective tool in the hands of qualified
practitioners and it is effective for the maintenance of domestic supplies
of germplasm that is free of AHB traits. However, it is impractical for the
production of commercial queens for sale to beekeepers: it is too timeconsuming and labor-intensive to be profitable (Laidlaw and Page, 1998).
The final method for controlling mating is drone saturation: flooding an
area with enough drones from a desired source to enhance the probability
that young queens will mate with them. More research is required, however,
to determine the degree of mating control required to produce behaviorally
acceptable colonies (Guzmn-Novoa and Page, 1994a).
Beekeepers are aware of liability issues that could result from stinging
incidents that involve Africanized bees. Guzmn-Novoa and Page (1994b,
1999) have reported that selective breeding within Africanized populations
can result in a reduction in defensive behavior. However, continuous breeding selection could be necessary to suppress defensive behavior, especially
where AHB stocks are prevalent.
Integrated Pest Management
Integrated pest management (IPM; Kogan, 1998) provides a unifying
framework for the management of many agricultural pests, including those
of honey bees. IPM coordinates the use of several pest control methods for
sustainable, economically feasible management. Whenever possible, IPM
uses reliable pest-sampling methods and economic injury thresholds to guide
treatment decisions. IPM is desirable because it allows beekeepers to use pest
information to avoid economically unnecessary applications of pesticides
and antibiotics, thereby extending the long-term utility of those products
by reducing the rate at which resistance evolves. It also allows beekeepers
to reduce or eliminate pesticide residues in hive products.
Each sector of the beekeeping industry will require an IPM program to
fit its size (the number of colonies) and its marketing goals (commercial or
natural foods). American foulbrood is one disease that is effectively treated
with IPM approaches. The combination of cultural methods with inspection
programs and the proper use of antibiotics provides good results for control
(Goodwin and Van Eaton, 1999). Continued extension efforts should be en-

165
couraged to widen acceptance of IPM of parasitic mites, especially by large

commercial operators. The future of IPMs application in the industry will
depend on the development of additional treatments and on the creation of
economic incentives to compensate for the additional costs involved.
Extension activities provide a primary mechanism for informing beekeepers about pest management options and the best ways to implement
them. Extension apiculturists should encourage the use of IPM whenever
possible, and extension personnel should encourage beekeepers to demand
third-party certification of resistant stock from commercial queen producers. Extension efforts directed toward queen breeders and commercial
queen producers should emphasize methods for stock development and
maintenance and the use of controlled mating, primarily through geographic
isolation and drone saturation.
ARS Honey Bee Research
Much of the applied research on honey bees in the United States is conducted in ARS honey bee laboratories. Research funding has increased from
$5.6 million in 1996 to $9.2 million in 2006, although the number of fulltime scientists has declined since 2003 (Table 6-1). Some of the approaches
to preventing or reversing pollinator decline outlined in this chapter depend
on strong ARS involvement in honey bee research. Maintaining current
research support and restoring lost scientist positionswith a special focus
on honey bee pollinationat ARS is critical to pollinator conservation and
restoration.
TABLE 6-1 Funding and Staffing ARS Bee Research

Fiscal Year
Funding ($ U.S.)
Full-Time Permanent
Staff Scientists
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
5,574,000
5,913,000
6,380,000
6,599,000
7,009,000
7,629,000
8,037,000
8,450,000
8,844,000
8,861,000
9,227,000
23
23
23
26
26
27
25
28
27
27
24
SOURCE: USDA-ARS.

166
Government Intervention
Although beekeepers have faced recent substantial increases in the
cost of mite control and hive transportation (Chapter 3, Chapter 4), those
expenses have been offset somewhat by higher pollinator rental rates and,
in some years, by higher honey prices. The higher prices signal shorter supplies of honey bees. Honey bee populations recovered after the winter kills
of 19951996 and 20012002 (USDA-NASS, 1999, 2004a) and pollinator
rental rates have increased as have competitive honey prices. Continuing
indirect federal price supports through the loan deficiency payment and
marketing assistance loan programs (USDA-FSA, 2006) also strengthen the
market. Beekeepers can be expected to re-establish the honey bee colonies
lost during the 20052006 winter. In general, although honey bee colony
numbers are much more volatile from year to year since the arrival of the
varroa mite (Chapter 2), the market for honey bee pollination services appears appropriate, and that signals help in stabilizing the number of pollinator colonies available (Sumner and Boriss, 2006). However, government
intervention could reduce volatility by encouraging research, extension, and
certification efforts; by creating stricter controls for importation of honey
bees from other countries; and by better monitoring of honey bee colonies
and pollination services (Chapter 5).
Faced with managing the varroa mite threat to the North American
honey bee population, the beekeeping industry might find that its funds
alone are insufficient to cover immediate research needs. Special, limitedterm federal support should be made available through a competitive research program targeted at honey bee genetics and management to protect
populations. The program could be administered by the USDA National
Research Initiative Competitive Grants Program or by the National Science
Foundation. Given the targeted agricultural nature of the problem, however, a USDA program would be more suitable. Long-term, programmatic
research support should continue through ARS.
The effects of increased research for improved varroa mite management will be emasculated in the absence of effective communication with
the honey bee industry. The recent reductions in federal funding for state
extension programs leave two avenues for improving communication. First,
state land grant universities should seek ways to cooperatively finance
positions for honey bee extension specialists, who could then increase the
benefits of research through education and outreach. Second, the honey
bee industry, represented by the American Beekeepers Federation and the
American Honey Producers Association, should continue and intensify its
efforts to communicate advances in honey bee hygiene and management
information. The industry also could collaborate with researchers to help

167
identify obstacles to the transition to IPM-based beekeeping, with resistant

stock as a foundation.
Continuous protection against invasive pests and diseases from abroad
is crucial to pollinator protection on the continent. The federal Honeybee
Act of 1922 authorizes APHIS to regulate imports. The 2004 revision
(USDA-APHIS, 2004), prompted, in part, by honey bee shortages in California almond groves, led to extensive APHIS collaboration with the Australian
Quarantine and Inspection Service and New Zealands Ministry of Agriculture and Forestry to establish rigorous inspection and quarantine procedures
(USDA-APHIS, 2004). Rigorous enforcement of sanitary rules on honey
bee colony and queen importation must continue, along with protection
against interstate transmission of pests. The revision (USDA-APHIS, 2004)
permits importation of other pollinator bee species (Bombus impatiens,
B. occidentalis, Megachile rotundata, Osmia lignaria, and O. cornifrons).
Importation of these bees is regulated to prevent the introduction of new of
diseases, parasites, and pest species.
Industry Initiatives
Beekeepers and the crop producers who require pollination have a special interest in the health of honey bees. The main fundraising mechanism
available to U.S. agricultural producers for research and promotion is the
Commodity, Promotion, Research and Information Act of 1996, which
authorizes check-off programs administered by the USDA Agricultural
Marketing Service (AMS) but managed by an industry board (USDA-AMS,
2005). Since its creation in 1987 through a USDA-administered referendum
of honey producers, the National Honey Board has administered a check-off
program that pools revenues from the fee of a penny per pound of honey
that is collected from producers who sell at least 3 tons of honey in a year.
The Honey Research, Promotion, and Consumer Information Order collects the funds for marketing and research to reduce production costs and
to enhance demand for honey (USDA-AMS, 2004). The specific focuses are
honey research and promotion, not work on pollination or pollinators.
Given the increasing importance to beekeepers of revenues from pollination fees and the importance of honey bee pollination to producers of
almonds and many other fruit and vegetable crops, the two groups might
consider joint fundraising to focus support on pollination-related research
and education. Research on methods to mitigate damage caused by parasitic
mites and to ensure strong colonies each spring are among the relevant topics that joint support could fund. Another is research on honey bee stock
development and maintenance.

168
Non-Apis Commercially Managed Bees

The potential for using wild bees as managed crop pollinators has long
been known (Bohart, 1972a) and several approaches have been explored
(Bosch and Kemp, 2002; Macfarlane et al., 1994; Stephen, 2003; Torchio,
2003). There is an extensive body of published work on methods of rearing
wild bees (Griffin, 1993; Hughes, 1996; Maeta and Kitamura, 1981; Strickler and Cane, 2003; van Heemert et al., 1990) that provides a strong foundation for efforts to identify and cultivate commercial pollinators among the
large number of wild bee species (Strickler and Cane, 2003).
Several native and nonnative species currently are being used commercially or have potential for use as agricultural pollinators in North America
(Chapter 1). Among the native North American bees, Osmia lignaria is
an efficient and cost-effective pollinator of sweet cherry, plum, and prune
(Bosch and Kemp, 1999) that has demonstrated potential as an almond
pollinator (Bosch et al., 2000; Torchio, 1981a,b, 1982). O. ribifloris is an
effective pollinator of blueberry (Sampson and Cane, 2000; Sampson et al.,
2004; Stubbs et al., 1994; Torchio, 1990). O. aglaia can be an effective pollinator of cultivated blackberry and raspberry (Cane, 2005), and O. excavata
and O. jacoti have potential as commercial pollinators (Wei et al., 2002).
Bumble bees and Andrena spp. are better pollinators of lowbush blueberry
than are honey bees (Javorek et al., 2002). Bumble bees are also highly efficient greenhouse crop pollinators (Box 3-1; Free, 1993).
O. cornifrons, the hornfaced bee, is an Asian species used extensively
for apple pollination in Japan (Batra, 1982; Maeta, 1990; Sekita, 2001)
that has good potential for North American pear pollination (Maeta et al.,
1993). It was imported into the United States in 1977 (Batra, 1979), but it
has not become established as a commercial pollinator. The alfalfa leafcutter
bee, Megachile rotundata, introduced from Eurasia, is superior to honey
bees for alfalfa pollination (Cane, 2002; Tepedino, 1997). M. rotundata also
can be an effective pollinator of blueberry (MacKenzie, 1997; Stubbs and
Drummond, 1997a) and oilseed rape (Soroka et al., 2001) but not cranberry
(MacKenzie, 1997).
Although USDA no longer introduces exotic bees to North America for
development as commercial pollinators, prospecting among native fauna for
new agricultural pollinators is an important way to encourage redundancy
that will promote pollination services and food security and stability. Although prospecting programs have been in operation for 50 years at ARS
and several university laboratories, the search for, biological evaluation of,
and development of propagation and rearing methods for alternative bee
pollinators have resulted in the wide-scale propagation of only a single species. The alfalfa leafcutter bee was propagated successfully as the result of
development of trap nest technology at the ARS Bee Biology and Systematics

169
Laboratory in Logan, Utah (Bohart, 1962, 1972 a,b; Bohart and Pedersen,
1963). The entire contemporary U.S. alfalfa leafcutter bee industry results
largely from this pioneering work by a few USDA and Canadian agricultural
scientists who, because of its behavior in Eurasia, recognized the leafcutter
bee as a legume crop pollinator. Strickler and Cane (2003) discussed lessons
learned from past experience on developing alternative pollinators and offered suggestions to guide future effort.
In view of the effort required to develop new commercially managed
pollinators, to complement efforts at the Logan laboratory, ARS could well
benefit from creating positions in research entomology for the ARS fruit and
vegetable laboratories across the United States. Their work might identify
candidate pollinators for the major crops requiring pollinators in different
regions, study the life history of promising species, identify potential pest
problems, and develop viable management and rearing methods for commercial use of those species.
In addition to increasing the effort to identify new commercial pollinators, research investments are needed to prevent declines in existing
commercially important species. The alfalfa leafcutter bee was devastated
by chalkbrooda fungal diseaseand the absence of any successful management strategy (Chapter 3) should spur research to develop tools for an
effective response.
U.S. bombiculture, the rearing of bumble bees, faces many more serious problems than does megachileculturethe rearing of leafcutter bees.
Bumble bees are susceptible to some of the same diseases and parasites that
plague honey bees, and disease limits their utility as commercial pollinators.
Infections of the bees can complicate long-term maintenance of captive
colonies. Two native species (B. occidentalis and B. vosnesenskii) have been
evaluated, mass reared, and used as pollinators in the United States, but
infections of Nosema and other pathogens in commercial insectaries led to
discontinuation of these efforts (Thorp, 2003; Winter et al., 2006). Today,
the only bumble bee raised for commercial greenhouse tomato pollination
in the United States is B. impatiens, which is native to the eastern United
States. Multinational agribusinesses have developed large-scale insectaries for year-round production of bumble bee colonies in Europe, Israel,
Canada, Mexico, and the United States (primarily B. terrestris in Europe, B.
impatiens in the eastern United States). In 2005, about 90,000 hivesfrom
all suppliers of bumble beessupplied bumble bees for pollination throughout Mexico, the United States, and Canada (Ren Ruiter, Koppert Biological Systems, personal communication, February 2006). U.S. bombiculture
presents risks to native bees that could be greater than the risks posed by
U.S. apiculture to honey bees (because there are no native North American
Apis species). If managed nonnative bumble bees escape, hybridization and
competition with native Bombus species could occur (Thorp, 2003; Winter

170
et al., 2006). The potential for such hybridization between European and
Japanese species has been demonstrated in the laboratory (http://www003.
upp.so-net.ne.jp/consecol/english/goka_report/goka_report.html).
Large-scale transportation of native and exotic bumble bee colonies
among regions of North America and internationally is already thought
to be a source of introduced pathogens in native North American Bombus
species (Chapter 3; Thorp, 2003). During the initial stages of bombiculture
development in the United States, native bumble bee queens of B. occidentalis captured in the United States were transported to Holland and used
to start colonies that were later returned to the United States (Ren Ruiter,
Koppert Biological Systems, personal communication, February 2006). The
concern has been raised that the bees reintroduction carried new parasites
or diseases (Chapter 3) into the United States. According to Colla and colleagues (2006), there is evidence that commercially-reared bumble bees
have higher prevalence of various pathogens than their wild counterparts.
Several studies have found that the intestinal protozoa Crithidia bombi
Lipa and Triggiani (Kinetoplastida: Trypanosomatidae) and Nosema bombi
Fantham and Porter (Microsporidia: Nosematidae), and the tracheal mite
Locustacarus buchneri Stammer (Acari: Podapolipidae) are far more abundant in commercial than wild bumble bees. Because bumble bees often
escape from and forage outside greenhouses where their colonies are used
for tomato pollination, they could transmit diseases to wild colonies of the
same and other Bombus species. Colla and colleagues (2006) reported a
significantly higher incidence of infection with parasites and pathogens in
various bumble bee species collected near greenhouses, than in individuals
collected farther away. In Japan, Niwa and colleagues (2004) documented
the transfer of pathogens from European to Japanese bumble bees, and
comparable pathogen spillover might have caused or contributed to the
recent decline and extirpation of several bumble bee species in the subgenus
Bombus and to the likely extinction of B. franklini (Chapter 3; Colla et al.,
2006; Thorp, 2005; Thorp and Shepherd, 2005).
Recently, bumble bee rearing in the United States has been accomplished without international bees in facilities certified monthly by APHIS
to be free of known bee diseases (Ren Ruiter, Koppert Biological Systems,
personal communication, February 2006). The United States and Canada
also have blocked imports of nonnative bumble bees (such as B. terrestris).
Industry groups are lobbying the Mexican government to allow introductions of B. terrestris (from Europe) into Mexico for tomato pollination in
greenhouses (Winter et al., 2006). Restriction of bumble bee transfers both
within the United States and from other countries is advisable because of
the potential for disease transmission to managed and native wild bumble
bee species and the invasiveness of some species (such as B. terrestris; Dafni
and Schmida, 1996; Hingston and McQuillan, 1997, 1998).

171
MAINTAINING WILD POLLINATORS

Wild pollinators are mobile organisms that often use many resources in
noncontiguous habitats. Some butterflies visit suburban gardens for nectar
but oviposit on the foliage of tree species in forest habitats. Many species
of hummingbirds that breed in the United States and Canada overwinter in
Mexico (Nabhan et al., 2004; Shepherd et al., 2003). Maintaining diverse
communities of wild pollinators therefore requires an understanding of
various habitat needs and of managing habitats and landscapes to provide
necessary resources (Table 6-2). Populations of pollinators can be supported
if habitats are managed to provide food, and areas for nesting, overwintering, and breeding (Dover, 1991; Erickson and West, 2003; Evelyn et al.,
2004; Fenton, 1997; Schultz and Dlugosch, 1999; Scott, 1986). Because
pollinators are mobile, the area over which they forage, disperse, and migrate must be considered in strategies to maintain populations. Adequate
resources must be available within foraging and dispersal areas (Westrich,
1996) and along migratory routes (Nabhan et al., 2004).
Managing pollinator populations and communities requires planning
and action locally, regionally, and across continents. Because of their ecological and economic significance and because they are in some respects
better known than are many other wild pollinators, bees can serve as a
paradigm group to illustrate how multiscale approaches can be implemented
in habitat restoration, conservation, and management.
Resource Requirements for Bee Species
All native and introduced bee species, whether solitary or social, require
the correct balance of water, floral hosts that offer sufficient pollen and nectar of the correct types (Roulston and Cane, 2000; Roulston et al., 2000),
nest-building materials (leaves, resins, sap, gums, floral oils, essential oils,
bark, plant trichomes, old mouse nests, snail shells, mud, sand, pebbles), and
nesting substrates (OToole and Raw, 1991; Roubik, 1989; Shepherd et al.,
2003) to survive as adults and rear their larval broods (Michener, 2000).
Michener (2000) provided a comprehensive review of floral resource
requirements for bees. Bees obtain pollen and nectar from cultivated and
wild plants. Pollen (usually moistened with nectar or floral oil) is used to
feed larval bees, and nectar is used to fuel the flight of adults. Many solitary
bees are active above ground as adults for only a few weeks or months.
Oligolectic bees specialize on one or a few closely related species within a
genus of flowering plants; polylectic bees collect pollen from an array of
unrelated plants. Species with long flight seasons are usually polylectic and
include the long-lived carpenter bees and euglossine orchid bees, those that
produce multiple generations within a season, and highly social bees with
annual or permanent colonies (honey bees, bumble bees, stingless bees).

172
TABLE 6-2 Pollinators and Resource Requirements

Pollinator Group
Resource Function
Resource
Honey bees, bumble bees, batsa
Nesting, roosting
sites or substrates
Nesting, roosting
sites
Nesting sites or
substrates
Nesting sites or
substrates
Nesting sites
Adult food
Larval food
Nesting sites
Cavities (underground, hollow

trees), large caves, mines
Trees (horizontal branches with
shelter from night sky)
Bare ground, vertical cliffs or ditch
banks, adobe walls
Soft woods, pithy twigs, beetle
burrows
Rodent, mouse nests
Pollen, nectar
Insects, organic matter, water
Plant galls, snail shells
Nesting sites
Sand dunes, sand or burrow pits,

gravel pits, quarries
Glandular secretions (beeswax,
exocrine secretions, Dufours)
Hummingbirdsb
Nonsocial bees, waspsc
Large and small carpenter bees,
leafcutter bees, mason beesd
Bumble beesa,e
Flies
Flies
Leafcutter and mason bees
(European)f
Nonsocial bees, wasps
Highly eusocial bees, honey
bees, bumble bees, stingless
bees
Nonsocial bees, some wasps;
mason bees, leafcutter bees,
masarid wasps, potter wasps
Leafcutter bees, mason bees,
masarid wasps
Nonsocial bees, some wasps
Building materials
Leafcutter bees, mason bees

Leafcutter bees, especially
anthidiines (carder bees)
Leafcutter bees, Apis, Melipona,
Trigona, orchid bees
Orchid bees
Bees
Birds, some bats, bees, masarid
wasps, butterflies, flies
Centris, Epicharis,
Paratetrapedia bees
Wasps, Pompilidae (spider
wasps)
Parasitic, nonparasitic wasps
Butterflies, moths
Ants
Beetles
Building materials
Mud, clay, sand
Building materials
Building materials
Building
Debris (bark, floral parts, seeds,

dead insect parts)
Water (mixed with soil to make
mud)
Leaves cut into pieces or masticated
Plant hairs (trichomes)
Building materials
Floral, plant resins
Pheromones
Food, building
materials
Food
Essential oils, such as

monoterpenoids collected by
males
Floral oils (Clusia, Dalechampia,
Krameria, Malpighiaceae)
Pollen, nectar
Food, building
materials
Larval food
Floral oils (Clusis, Dalechampia,

Krameria to mix with pollen)
Paralyzed spiders
Larval food
Larval food
Insect prey
Leaves, other plant parts (often
taxonomically restricted)
Nectar, honeydew, insect prey
Pollen, nectar, food bodies, organic
matter
Building materials
Adult, larval food

Adult, larval food

173
TABLE 6-2 Continued

Pollinator Group
Resource Function
Resource
Thrips
Adult, immature
food
Food
Building materials
Floral tissue, leaves, pollen, nectar
Hummingbirds
Hummingbirds

aMichener,
bEhrlich
Nectar, small insects

Spider webs (silk), lichens, fibers
1974.
et al., 1988.
cMichener, 2000.
dKrombein, 1967.
eHeinrich, 2004.
fOToole and Raw, 1991.
The bee species might require floral resources for weeks or months, so a
diversity of floral sources must be available; at least some of the flowering plants should have overlapping blooming periods that encompass the
bees long flight periods. For social bees that overwinter as adults (bumble
bees, honey bees), the temperate bloom of fall-blooming asteraceous species (goldenrods) are nectar and pollen sources that provide protein and
carbohydrate resources essential for winter survival (Shepherd et al., 2003;
Vaughan et al., 2004).
Bee species vary in floral resource requirements, and there is a wide
variation in nesting habits. Many dig nests in the ground (Halictidae, Andrenidae), others occupy abandoned rodent nests (Bombus spp.), some use
preexisting tunnels or cavities in dead tree trunks and limbs (Megachilidae,
some Apinae), and others actively excavate cavities in wood (Xylocopinae).
The diversity of a bee community is tied to the availability of different nesting substrates (Potts et al., 2005).
Most North American bees are ground-nesting. Like their more familiar
sand wasp relative, they vary by species in nest site selection criteria (Cane,
1991; Michener, 2000; OToole and Raw, 1991). Some ground-nesting bees
prefer to nest in open, horizontal areas of soil devoid of vegetation or debris;
others seek small areas of bare soil within lawns or nest in vertical banks,
either naturally occurring ones or those formed by adobe structures, wood
frame houses, and other buildings. Patches of bare earth warmed by the sun
and protected from flooding are especially preferred as nesting sites. Many
species prefer to nest in well-drained sandy soils or silty loams (Cane, 1991).
Some nest in dense aggregations that persist for decades (Michener, 2000);
others construct highly scattered ephemeral nests.
About 10 percent of North American bees nest in wood (Michener,
2000). Carpenter bees (Xylocopa spp.) have strong jaws to excavate extensive galleries in soft, dry, dead wood. Small carpenter bees (Ceratina), mason

174
bees (Osmia spp.), and some leafcutter bees (Megachile spp.) use cavities
made by wood-boring cerambycid or buprestid beetles. Nesting female bees
match the diameter of their bodies to evacuated natal tunnels of the beetles
(Krombein, 1967). This nesting biology makes it possible to trap nest and
collect numerous females of diverse species in the twig-nesting guild. Those
species will readily build nests in blocks of wood that have been drilled
with appropriate-sized holes (Gathmann et al., 1994; Krombein, 1967;
Tscharntke et al., 1998).
About 45 species of North American bumble bee nest principally in
cavities within the ground. Upon emerging from diapause in the early spring,
bumble bee queens seek rodent burrows, abandoned mouse nests, and other
cavities in which to found their colonies and rear their first broods (Goulson,
2003c; Heinrich, 1979, 2004; Michener, 1974). In the southwestern United
States, bumble bees (such as B. sonorus) often nest in or near human structuresunder boards, in sheds, in walls, or even in abandoned mattresses or
automobiles (S. Buchmann, unpublished data).
Once a nest is built, it can be modified by the addition of construction
materials or glandular secretions. Ground-nesting bees typically use nothing more than exocrine gland secretions (Michener, 2000; OToole and
Raw, 1991; Stephen et al., 1969). Bees that nest in pithy twigs, stems, or
dead wood often forage at some distance from their nests for additional
construction materials (Roubik, 1989). Pieces of foliage often are used by
leafcutter bees (Megachile spp.) to form cell walls and end plugs. Osmia spp.
often construct cell walls and end plugs from mud gathered nearby (Bosch
and Kemp, 2001). Other Megachile species use resins, pebbles, and plant
materials to form divisions between larval cells or to prevent entry to their
nests by ants, parasitic wasps, or birds (Krombein, 1967; Michener, 2000;
Stephen et al., 1969).
In agricultural plantings, where leafcutter and mason bees are used to
pollinate crops, it can be necessary to provide patches of fresh mud (for
Osmia spp. mason bees) or appropriate plants from which bees can cut
leaves to form their cells. In the case of the introduced alfalfa leafcutter bee,
alfalfa plants themselves provide pollen, nectar, and the leaves the bees use
to create their nests. Other twig- or wood-nesting bees (such as Xylocopa)
line their nests with layers of glandular exocrine secretions (Cane, 1991;
Michener, 2000; Roubik, 1989). Social bees, including bumble bees, stingless bees (meliponines), honey bees, and some orchid bees (euglossines),
use collected materials and beeswax secreted from their abdominal wax
glands to build nests (Michener, 1974). Even for commercially managed bee
pollinators, it can be necessary to provide supplemental sources of nesting
materials.

175
Restoring, Managing, and Conserving Wild Bee Habitat

The plant resources required by bees for food and nesting dictate that
strategies for maintaining healthy and diverse communities of pollinator
populations must focus on conserving and restoring diverse plant communities (Forup and Memmott, 2005; Kremen et al., 2002a; Matheson et
al., 1996; OToole, 1993, 1994). Providing sequences of blooming plants
that encompass the entire flight period of the pollinator is one important
component of maintaining pollinator populations, whether these series
result from small-scale modifications on farm sites or in gardens or from
large-scale regional restoration (Vaughan et al., 2004). Similarly, plans to
provide habitat for bees or other pollinators (Table 6-2) must consider not
only food resources, but also the specialized resources used for breeding,
nesting, or overwintering.
Several factors should be considered in determining appropriate planting mixes. First, native plants are generally preferable to introduced species
because they help maintain North American biodiversity of plants and pollinators (Shepherd et. al., 2003). Ideally, plants are not just native to the
continent but they are native to and genetically adapted to the region and
to the site conditions (McKay et al., 2005). Second, plants must provide a
complete phenological suite of resources for key pollinator species (Kremen
et al., 2002a). Developing an optimal plant list requires research on the
network of interactions between plants and pollinators and on which critical bridging plants might be needed to provide resources during periods
of dearth (see, for example, Forup and Memmott, 2005; Kremen et al.,
2002a). Finally, conserving existing original habitats generally should take
priority over restoration, because restored habitats might not replicate
every component that is functionally significant to pollinator species (Zedler
and Callaway, 1999), and goals for restoration can be difficult to establish
(Ehrenfeld and Toth, 1997).
Nesting Sites and Substrates
The alkali bee (Box 6-2), which has been successfully managed for
pollination of alfalfa in the Pacific Northwest (Chapter 2), provides an
example of how creation of supplemental or artificial nesting sites can
enhance bee populations. Remarkably, few restoration ecologists have
tested the efficacy of supplemental nesting sites for ground-nesting bees to
enhance wild populations or to provide stable long-term habitat (but see
Forup and Memmott, 2005). Investigating the effects of supplementation
on nest occupancy, abundance, and persistence of wild bees is therefore a
high priority for research.

176
BOX 6-2
Alkali Bee: Case Study in Managing a Ground-Nesting
Commercial Pollinator

Nomia melanderi, the alkali bee, is native to arid areas west of
the Rocky Mountains. It nests obligately in alkaline areas in California,
Colorado, Idaho, Nevada, Oregon, Washington, and Utah. Before human
colonization, alkali bees nested in dry lake beds and similar habitats,
requiring soils with an alkaline surface crust of salt. The bees nest at
depths of 816 cm in aggregations of as many as 240 bees per square
meter (Bohart, 1958, 1967, 1972b; Cane, 2003). Alkali bees visit native
legumes for pollen and nectar and are extremely efficient pollinators of
alfalfa, for which they are managed as commercial pollinators. Today,
specially prepared alkali bee nesting beds have been created in four
states. In Washingtons Touchet Valley the bee nesting beds average
6200m2the largest site had 1.7 million bee nests. In 1992, the cost per
acre to pollinate alfalfa with alkali bees was estimated at $30 (Willet and
Gary, 1992).

Methods for creating appropriate nesting conditions for N. melanderi
were developed and tested at the ARS Bee Biology and Systematics
Laboratory in Logan, Utah (Cane, 2003). To create artificial nesting beds,
prepared soil is moved into basins with underlying gravel or plastic and
standpipes to create an upwelling of moisture to the surface. Salt is applied heavily to the soil surface to form a crust that mimics the salt pans
and playas where bees nest naturally. Backhoes fitted with hydraulic
punches remove block soil cores from existing nesting aggregations, and
the cores are planted in new alkali bee beds to establish nesting sites
adjacent to commercial alfalfa fields. Although moving nests and underground cells of ground-nesting bees is notoriously difficult and rarely attempted, it has worked well for establishing nesting aggregations of alkali
bees in artificial nest beds. The bee beds are expensive initially, but once
established they are sustained by the bees themselves. Maintenance
costs are low and the beds last for decades.

In the 1960s and 1970s, alfalfa growers began to rely less on the native alkali bee for pollinating their crops (Mayer and Johansen, 2003) and
shifted to using the alfalfa leafcutter (Megachile rotundata), an introduced
species. The decline in the alkali bee industry probably was the result of
pesticide use for controlling rangeland grasshoppers, competition from
honey bees, and several rainy years, when the alkali bees underground
cells suffered unusually high mortality (Mayer and Johansen, 2003;
Chapter 3). Although few managed alkali bee beds remain, new research
and educational efforts are beginning to attract new practitioners to the
field (Cane, ARS, personal communication, January 2006).

177
Ground Nesters
Suitable habitats, including open ground or vertical walls, ditches, or
banks, can be created or modified within natural or anthropogenic habitats
as bee nesting sites. For example, piles of sand have been used in Europe to
create nesting substrates for bees (OToole and Raw, 1991). Some habitat
manipulations are simple and compatible with human habitation in Mexico
and the southwestern United States; solitary bees often nest within adobe
walls, which are relatively inexpensive, available, and durable (Buchmann,
unpublished data; Stephen, 2003).
Twig Nesters
Because wood-loving bees vary in size, nesting females choose tunnels
of appropriate diameter and depth that have been vacated by the emerging adult wood-boring beetle (Buprestidae, Cerambycidae) (Linsley, 1958).
Given that beetles and bees are ecological partners, actions to increase larval
substrates for wood-boring beetle taxa can increase the availability of nest
sites for pollinating bees and some wasps (Jones and Munn, 1998; Shepherd
et al., 2003). Not all woods or plant species provide suitable nesting substrates. Generally, soft woods that are not colonized by fungi are preferred
by guilds of wood-nesting bees (Krombein, 1967). Thus, retaining dead
branches or trees is an essential part of habitat management for healthy bee
populations and communities. Removing large amounts of dead wood for
fire wood (mesquite, palo verde, and ironwood in the southwestern United
States) results in the rapid elimination of many native bees (Buchmann and
Nabhan, 1996; Buchmann, unpublished).
Bee nesting habitats also can be created by attaching drilled-board trap
nests to fence posts, dead trees, or buildings (Griffin, 1999; Krombein, 1967;
Shepherd et al., 2003). A balanced strategy of conserving beetle-infested
dead trees and branches, setting out trap nests, and drilling holes into dead
trees should increase local bee populations (Buchmann, unpublished). Detailed instructions for drilled-board trap nests are in the literature (Bosch
and Kemp, 2001; Griffin, 1999; Krombein, 1967; Shepherd et al., 2003)
and online (http://snohomish.wsu.edu/mg/ombblock/ombblock.htm; http://
www.nwf.org/backyardwildlifehabitat/beehouse.cfm).
Cavity Nesters
Nest boxes made of wood or Styrofoam with plastic or rubber hose
entrance tunnels can be provided for bumble bee species that nest underground. The boxes can be buried or nestled into bank or ditch sides to attract founding bumble bee queens in the spring. Adding upholsterers cotton,
abandoned mouse nests, or other nesting materials can improve the nests

178
attractiveness (Heinrich, 2004; Intenthron and Gerrard, 1999). Nest boxes

yield variable success that depends largely on the skill and knowledge of the
builder and person placing the boxes in the field (Heinrich, 2004; Kearns
and Thomson, 2001; Pry s-Jones and Corbet, 1987). Extensive work on the
chemistry of bumble bee pheromones has been conducted for some species
(Bergstrm et al., 1996; ONeill et al., 1991); the use of pheromone lures
in the early spring to attract females to nest boxes could be useful although
it has not yet been evaluated.
If colonies are started in the laboratory from wild-caught queens, their
diet must be supplemented with pollen (often collected from Apis colonies
using pollen traps) and sugar water or diluted honey. Colonies replaced to
the wild should be kept away from areas where insecticides are sprayed, or
spraying should occur at night when bees are inside their nests. Although
established Bombus colonies can be purchased from commercial insectaries,
they should not be used in reintroduction programs or as crop pollinators
outside of greenhouses because of the possibility of transmitting pests and
pathogens to local conspecifics or congeners (Colla et al., 2006).
Seeding Areas with Established Nests
Nests of wood or ground-nesting bees can be collected in natural habitats
and introduced elsewhere to reestablish populations, although this approach
is still experimental. Occupied branches or inhabited dead trees can be moved
from one area to another to seed a new habitat with bees (Yurlina, 1998).
Trees and nesting blocks were used in New Jersey at the Fresh Kills landfill
to reintroduce native bee species to the active restoration site (Handel, 1997;
Handel et al., 1994; Yurlina, 1998). Introductions of occupied nests, however,
are more common in commercial agricultural pollination. Twig-, wood-, and
cavity-nesting bees are generally more manageable than are ground-nesting
bees (Bosch and Kemp, 2001). Several leafcutter and mason bee species are
routinely moved in artificial domiciles to orchards and alfalfa fields for agri
cultural pollination (Chapter 1). Other than alkali bees (Box62) (Bohart,
1958, 1962, 1972a; Cane, 2003), ground-nesting bees have been difficult
to manage commercially as pollinators. There is not enough information
available to determine whether reintroducing native twig-nesting bees into
restored habitats would allow establishment or whether ground-nesting bees
can be similarly reintroduced and established.
Agricultural Landscape Management
Floral Resources
Many of the options for increasing the diversity and abundance of
floral resources on farms to accommodate the needs of a diverse pollinator

179
community (Batra, 2001; Bugg et al., 1998; Matheson, 1994; Pywell et al.,
2006; Vaughan et al., 2004) do not necessarily reduce farming productivity,
and they can even improve productivity by providing additional benefits
beyond pollination services, such as nectar for natural enemies of crop
pests (Pickett and Bugg, 1998). The options are listed here in order from
the least expensive, most easily implemented to larger scale, more costly, or
more complex changes.
Growing polycultures rather than monocultures in a field results in a
more diverse set of floral resources. Including flowers that bloom at different
times of the year provides for and attracts a greater number of pollinator
species, including those with long flight seasons.
Tolerating weeds along crop borders can provide a diverse and abundant set of floral resources, at no cost to the farmer.
Insectary strips planted within crop fields or in field margins and in
buffer strips provide abundant pollen and nectar sources and attract bees
to the fields (Altieri and Nicholls, 2004; Carvell et al., 2004; Pywell et al.,
2005).
Planting cover crops on resting fields or as orchard understory and
allowing cover crops (such as clovers) to bloom before plowing them under
provides green manure that benefits both pollinators and soil fertility.
Planting wildflower mixes in fallow or old fields or allowing weeds
to colonize creates meadows that support pollinators as the fields rest.
Planting permanent hedgerows of native perennial forbs and shrubs
provides nest sites and preferred pollen and nectar sources for a diverse
community of pollinators in the spaces between fields. Such hedgerows may
also serve as wind-breaks or provide erosion control.
Restoring natural habitat patches on farms in permanent set-asides
focusing on areas that are more difficult to farm, such as edges of ditches,
ponds and riparian areas, on hills, or around utility polescan provide
undisturbed habitat for pollinators.
Some governments, particularly in Europe (Box 6-3), have developed
extensive monetary incentives to encourage environmental stewardship
by farmers and ranchers. They include promotion of fallow and set-aside
programs, as well as the planting of annual or perennial wildflowers for
forage for pollinators along field margins and between fields. Among the
specialty seed mixes of local wildflower species that have been developed
in Europe is the Tbingen mix, which is in wide use in Europe (Engels et
al., 1994; Matheson, 1994). Monitoring programs have demonstrated that
integrating low-cost pollen and nectar sources into field borders provides
measurable improvements in abundance and richness of several pollinator
groups (Carvell et al., 2004; Pywell et al., 2004, 2006). The increase in land-

180
BOX 6-3
EU Biodiversity Conservation in Agriculture

The European Union (EU) and most of its member states have set a target of halting the loss of biodiversity by 2010. Detailed EU-sponsored research
programs provide the scientific rationale for policy development (including the
ALARM program [Chapter 5] and the SAFFIE project). Several policy instruments are available (agri-environment schemes and biodiversity action plans)
to provide incentives for implementation.
Science Programs

ALARM, or Assessing Large Scale Environmental Risks to Biodiversity
with Tested Methods is funded by the European Commission under Framework 6. The overall research program has several aims:
Quantify distribution shifts in key pollinator groups across Europe.
Measure biodiversity and assess economic risks associated with the
loss of pollination services in agricultural and natural systems through
the development of standardized tools and protocols.
Determine the relative individual and combined importance of drivers
of pollinator loss (land use, climate change, fertilizer and pesticide
contamination, invasive species, socioeconomic factors).
Develop predictive models for pollinator loss and consequent risks
(Settele et al., 2005). ALARM has 54 EU partner institutions working
in a 5-year, 22-million-euro project (20042009; Box 2-3, Box 5-1).

SAFFIE, Sustainable Arable Farming for an Improved Environment, is
a United Kingdom research program designed to sustain the management
of arable farms to support more wildlife. Its main objectives concern testing
methods for enhancing farmland biodiversity. Farmers are encouraged to use
alternative approaches to habitat management of crop and field margins as
a way to develop more sustainable farming. The project has 20 partners and
3.5 million in funding over 5 years (20022007).
Policy Instruments

Agri-environmental schemes provide programs that encourage EU farmers to carry out environmentally beneficial activities on their land. The aim is
to enhance biological diversity in a range of plant and animal groups, including pollinators. Farmers recover the cost of supplying environmental services
through government payments. Examples of activities include the following:
Reversion of intensively used land to biologically diverse but less
profitable extensively farmed land
Reductions in nutrient use
Reduction or cessation of pesticide use (such as through organic
farming)
Creation of nature zones from lands removed from production
Continuation of traditional environmental land management in zones
liable to neglect

Maintenance of landscape features that are no longer agriculturally

viable

The programs are managed by regional or national authorities under a
decentralized system, subject to approval by the European Commission. The
costs are partly financed by the EU. Fifteen member states are operating agrienvironmental programs that cover 900,000 farms and 27 million hectares, about
20 percent of EU farmland (for information on EU, visit http://www.europa.eu.int/
comm/agriculture/envir/index_en.htm; for information on its member states
visit http://www.europa.eu.int/comm/agriculture/rur/countries/index_en.htm).

The agri-environment schemes in various European countries have
yielded mixed, taxon-specific results. Although positive results have not been
demonstrated for all taxa studied (Kleijn et al., 2001, 2004), some pollinator
groups, notably bees, butterflies, and flower flies, appear to benefit in some
cases (Carvell et al., 2004; Kleijn et al., 2001, 2004, 2006; Pywell et al., 2005,
2006; Weibull et al., 2003). Scientific monitoring of the schemes, particularly
before-after control-impact monitoring (Potts et al., 2006), is critical to assessments of effectiveness, and much can be learned and applied from the work
in Europe.

The United Kingdom operates four optional agri-environmental schemes
(U.K. Department of Environment, Food and Rural Affairs, 2002) that pay
farmers to practice environmentally friendly farming. The Countryside Steward
ship Scheme aims to conserve, enhance, and restore target landscapes. The
Organic Farming Scheme facilitates the shift from conventional to organic
farming. The Environmentally Sensitive Areas Scheme covers 22 specific
areas of national environmental significance.

The Entry Level Agri-Environment Scheme is a new program that is
expected to include more than 70 percent of British farms. The intention is to
promote simple, effective environmental management to enhance farmland
biodiversity across a range of plant and animal groups, decrease diffuse pollution, maintain landscape structure, and conserve the historic environment. The
program has several areas that promote pollinator biodiversity according to
replicated field experiments (Carvell et al., 2004; Pywell et al., 2004, 2006):
Field margins sown with buffer strips provide forage (nectar and pollen) and nesting resources for pollinators and safeguard boundary
habitats against chemical sprays.
Grasslands sown with mixes that include pollen-and-nectar flowers
can increase the diversity, abundance, and availability of forage resources, and increases bumble bee diversity and abundance.
Careful management of hedgerows can create and protect habitats
suitable for pollinators.
Permanent grasslands can be established with very low input to provide long-term pollinator habitat.
SOURCE: http://www.defra.gov.uk/erdp/schemes/default.htm#land.
181

182
scape heterogeneity that accompanies these methods also can be beneficial

(Tscharntke et al., 2005).
The U.S. federal government also offers incentives through the Farm
Bill, which is administered by USDAs Natural Resource Conservation Service (NRCS). This agency maintains and offers state lists of approved or suggested plants for revegetation (in buffer strips or for hillside erosion control)
or for seeding rangelands for cattle production (http://www.nrcs.usda.gov/;
http://plants.usda.gov/). Some recommended species are potentially invasive
exotic plants or are grasses that provide little or no floral reward for bees
and other pollinators. In some cases, most notably the new Conservation
Security Programs, pollinator-friendly plants are specifically recommended
(USDA-NRCS, 2004, 2006a,b). More work is needed to develop appropriate lists of plants that support pollinators and to customize those lists for
different ecoregions within North America.
Nesting Substrates
Methods also are available for providing or protecting nest sites and
substrates for bee species in the agricultural landscape (Matheson, 1994;
Vaughan et al., 2004); many of them do not interfere with farming. They
range from simple, low-cost measures to more complex and expensive
methods:
Management of irrigation to preserve ground-nesting bees. By using
drip or spray irrigation instead of flooding, farmers can avoid drowning
ground-nesting bees and larvae. Interference with foraging and nest cell
provisioning can be avoided by irrigating at night.
Management of tillage to protect existing bees nests. By shallower
tilling or using no-till agriculture, disturbance of nest sites can be avoided.
The density of squash bees (Peponapis pruinosa) on squash and pumpkin
farms in the eastern United States that practice no-till agriculture is three
times that of tilled farms (Shuler et al., 2005).
Active land management to provide nesting sites for bees. Examples
include creating patches of bare ground for ground-nesting bees within
perennial plantings, such as hedgerows, or mowing or weeding within pastures; leaving dead wood and standing snags, drilling holes in dead wood,
and putting out trap nests for twig-nesting bees; providing a sand-loam
mix for ground-nesting bees; putting out bumble bee nest boxes, buried or
above ground; and creating specialized conditions for nesting aggregations
(Box 6-2). More research is needed to determine which active management
techniques are most effective for pollinator conservation and to adapt them
for different bee faunas and site conditions.

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Alternatives to Chemical Pest Controls

According to the National Center for Food and Agricultural Policy,
more than 68 active ingredients are used to control insect pests on North
American farms (http://www.ncfap.org/whatwedo/index.php). Insecticides
are differentially toxic to nontarget species, depending on the active ingredients, the strength and composition of the formulation (dust, powder,
liquid), and the behavioral and physiological response of the target insect
(Johansen, 1977; Johansen and Mayer, 1990). Some pollinator species
might not be killed outright by pesticide applications, but they could suffer
sublethal effects, including reduced foraging ability, that ultimately hamper
their productivity (Morandin et al., 2005; Vaughan et al., 2004).
Short of eliminating insecticide use altogether, growers can reduce risks
to pollinators from pesticides in several ways (Johansen and Mayer, 1990;
NAPPC, 2006; Vaughan et al., 2004):
Choose appropriate pesticides. Some insecticides have active ingredients that are less likely to cause mortality or sublethal effects in bees, to
have formulations that are less toxic to bees (for example, granular powders
are less noxious than dust; Johansen and Mayer, 1990), and to break down
more rapidly than others do. Microencapsulated formulations should be
avoided because they mimic pollen.
Apply pesticides selectively. Growers can avoid using insecticides
during a crops bloom period, apply them at night while bees are in nests,
and apply them on the ground rather than in aerial spray.
Convert some or all fields to organic production. Growers thus provide areas that are refuges from pesticides (Vaughan et al., 2004).
Grassland and Grazed Land Management

Natural grasslands (prairies) are now considered the rarest North
American biome; more than 90 percent of the continents grassland area is
now in agricultural use, and 14 of the 16 temperate grassland, savanna, or
scrub ecoregions in North America are classified as either critical or endangered (Ricketts et al., 1999). The loss involves more than grasses; annual
wildflowers and perennial plants are important vegetative components of
grassland biomes. Flowering plant, arthropod, and vertebrate biodiversity
is often higher in grasslands than in other North American biomes (Butaye
et. al., 2005; WallisdeVries et al., 2002).
Management of prairies and grazed lands includes mowing, grazing,
or prescribed burns that can either harm or benefit pollinators (Carvell,
2002; Potts et al., 2003; Rathcke and Jules, 1993; Smallidge and Leopold,

184
1997). Plans for managing pollinator populations and communities also

must consider the effects of invasive species on the composition of natural
vegetation. Specific practices that provide nest sites for pollinator species
might need to be considered for management protocols.
Mowing or Grazing
Many butterflies and other insects depend on habitats in early succession (Smallidge and Leopold, 1997), and mowing or grazing can be essential
to maintaining the early successional habitat types as patches within the
landscape, particularly if organisms that formerly grazed there (such as
bison) are now missing. In habitats where fire is the natural agent of disturbance, mowing or grazing can be more beneficial to the maintenance of
pollinator habitats, particularly if habitat patches are small and isolated. In
particular, pollinator species of interest suffer some larval or adult mortality
from fire (Smallidge and Leopold, 1997). Mowing at the appropriate time
(August) is also a good method for maintaining early successional patches
for the endangered Karner blue butterfly (Lycaeides melissa samuelis) and its
lupine host plant (Lupinus perennis) within sandy pine barrens, pine-oak savannahs, and oak savannahs in the Great Lakes region. Mowing also allows
new patches to be localized within the dispersal limits of the butterfly, permitting colonization from nearby occupied patches of lupine (Smallidge and
Leopold, 1997). Recent grazing was linked to increased bumble bee richness
and abundance in calcareous grasslands. In the United Kingdom, grazing
probably contributed to bumble bee abundance by enhancing diversity and
the abundance of forage plants preferred by bumble bees and by reducing
vegetation height, canopy closure, and moss litter (Carvell, 2002).
Burning
Fire can cause mortality in pollinators that nest above ground (larval
and pupal lepidopterans and twig-nesting bees) and lead to reductions in
abundance (Smallidge and Leopold, 1997). Most ground-nesting bees, however, nest at a soil depth of more than 5 cm (Michener, 2000), so the soil
could insulate the nests and reduce or eliminate mortality from wildfires or
prescribed burns.
In fire-adapted communities, many plants require fire or heat to open
fruits or scarify seeds (for example, Givnish, 1986). Such communities often
respond to a fire with abundant new growth, including annual wildflowers,
plants from bulbs, or regenerated sprouts. The flush of postfire vegetation
often produces an equally dramatic spike in nectar and pollen for local
pollinators; one example is fireweed, Epilobium spp., in the eastern United
States (Heinrich, 2004).

185
From a site in Israel that had high pollinator biodiversity (Mt. Carmel),
Potts and colleagues (2003) discovered that fire initially was catastrophic
to plant and bee communities, but that recovery was rapid. Within 2 years
of the fires there was a peak in plant and bee diversity that was followed
by a long and steady decline over the next 50 years. They reported that bee
pollinator communities closely matched the plant community in recovery
and regeneration (Potts et al., 2001, 2003).
Like mowing and grazing, fire is an important management tool that
can be used to reset the successional sequence and maintain the diverse
and heterogeneous mosaic landscapes that include early successional stages
(oldfields) and late primary stages (climax forests). Resetting the successional sequence provides resources for a wider array of species (Pickett and
White, 1985; Smallidge and Leopold, 1997). More information is needed
on the short- and long-term effects of fireand its use as a management
techniqueon diverse North American plant and pollinator communities.
Nesting Habitat
Although solid expanses of grasses and forbs are not productive nesting habitats for bees, they do provide nest sites (larval host plants) for a
variety of Lepidoptera. Thus, grassland management protocols that are
well adapted for Lepidoptera also should consider provisions for bee-nesting sites. Nesting sites can be provided by creating patches of bare ground
or sand-loam mixes for ground-nesting bees; by maintaining a landscape
mosaic of wooded and grassy areas, protecting some dead wood and standing snags and drilling holes in some dead wood; putting out trap nests for
twig-nesting bees; and putting out bumble bee nest boxes, buried or above
ground (Box 6-4). Large-scale herbicide applications, such as are applied in
the southwestern United States to remove undesirable scrub and brush (mesquite and Prosopis plants), should be discouraged because they remove not
only nesting sites and refuges, but also pollen and nectar sources for native
bees, honey bees, and other pollinators (Buchmann and Nabhan, 1996).
MAINTAINING POLLINATION SERVICES
Maintaining commercial pollinator stocks and the diversity of wild pollinator communities differs from maintaining pollination services provided
by pollinators, because pollination services could be enhanced without an
increase in pollinators. This section presents strategies for maintaining pollination services to crops by commercial pollinators and pollination services
to crops and wild native plant populations by wild pollinators.

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BOX 6-4
Golf Courses and Other Urban and Suburban Green Spaces

Traditionally, golf courses have been inhospitable areas for pollinating
birds, bats, and insects because of the large amounts of fertilizers, herbicides, and pesticides used and their close-cropped mowing. The U.S. Golf
Association has adopted pollinator-friendly practices (Shepherd, 2002;
Shepherd and Tepedino, 2000; Shepherd et al., 2001) for out-of-play areas (roughs), where wildflowers are planted, nesting domiciles (drilled bee
boards) are provided, and few or no pesticides and herbicides are applied.
Some golf courses have combined to form an association of organic golf
courses (http://www.usga.org/turf/green_section_record/2005/jan_feb/
Inorganic.html; http://www.epa.gov/oppbppd1/PESP/strategies/2005/
ogmd05.htm).

Similar techniques could be applied in urban parks and greenbelts,
on large corporate campuses, and at a smaller scale in home gardens, to
improve habitat for pollinators in urban and suburban areas. The abundant
floral resources in backyard gardens in some urban areas already support
diverse communities of bees and nest sites for twig-nesters in wooden
fences or houses (Cane et al., 2006; Frankie et al., 2005).
Commercial Pollinators
Crops that require or are improved by animal pollination benefit from
the services of commercially managed honey bees or other commercially
managed bees. The supply of commercial honey bee colonies can be stabilized by reducing bees vulnerability to pests, parasites, pathogens, and
pesticides. If honey bee colonies are in short supply, a new and potentially
useful compensation is to increase the available colonies efficiency. Honey
bee brood pheromones have been identified that temporarily increase the
proportion of a colonys foragers that collect pollen (Pankiw, 2004). Hormone manipulations also can advance the age at which bees switch from
working in the hive to foraging and increase the proportion of a colonys
foraging-worker force (Robinson and Ratnieks, 1987). These pheromones
and hormones could be developed into slow-release stimulants to increase
a colonys pollinator force in a growers field, although possible negative
effects on bee hives also should be explored. The supply of alternative
commercial pollinators requires caution to reduce losses to pathogens and
parasites, as happened to the alfalfa leafcutter bee, for example. Intensified
research and technology transfer will be required for development of new
species of alternative pollinators.

187
Commercially managed pollinators can be brought to the crops that

need their services, ensuring service delivery. Thus, growers of commodities
that require pollination follow recommendations for pollinator stocking.
For example, hybrid sunflower production requires two colonies of honey
bees per hectare (Delaplane and Mayer, 2000). Although some improvements could be made to maximize benefits by altering the spacing of colonies in fields and the spacing of self-incompatible cultivars (Chapter 4), in
general, the great advantage of using commercially managed pollinators is
that service delivery can be controlled, or at least manipulated, by relative
placement of pollinators and cultivars.
Wild Pollinators
It is far more difficult to ensure that services from wild pollinators are
delivered to crops. Because the mechanisms are not still well understood,
managing wild pollinators requires a better understanding of foraging
ecology and population biology and how they are influenced by landscape
properties (Kremen and Ostfeld, 2005). The few existing studies, however,
suggest that healthy (diverse and abundant) pollinator communities could
provide enhanced pollination services for a wider array of crops, and ensure stability of services within seasons and across years (Klein et al., 2003;
Kremen and Chaplin, in press; Kremen et al., 2002a).
Because pollinators are mobile and they collect resources within the
foraging range of a nest, roost, or territory (for example, hummingbirds),
environmental qualities of the immediate site (local) and the surrounding
area (landscape) affect their population sizes, densities, and persistence.
Many pollinator species use a variety of floral and nesting resources that
can be distributed across different habitat types at different times of the
year (Westrich, 1996). Some pollinators use native plant resources that occur only in natural habitats in season, and weedy resources that occur in
agricultural habitats in the summer (Kremen et al., 2002a). Mass-flowering
resources provided by crops can also be important for selected species in a
landscape (Westphal et al., 2003).
Evidence suggests that the character of a landscape is important in
determining the richness, abundance, and composition of pollinator communities on farms. Pollinator species differ in their ability to provide services
to different crops (for example, Free, 1993; Kremen et al., 2002b), and their
effectiveness could vary with the community context in which they exist
(Greenleaf and Kremen, 2006b; Thomson and Goodell, 2001; Thomson
and Thomson, 1992). Therefore, alterations in the composition of pollinator communities due to landscape change influence both the quantity and
quality of pollination services to cropsalthough local site characteristics
also influence pollinator communities and services (reviewed in Kremen

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and Chaplin, in press). In Californias Mediterranean climate environment,

landscape factors (the proximity or proportional area of natural habitat
within a site) are the dominant factors for pollinator richness, composition,
abundance, and services (Greenleaf, 2005; Greenleaf and Kremen, 2006b;
Kremen et al., 2002b, 2004), although site characteristics (conventional or
organic management of farm sites) modulate these responses at the population level (Kim et al., 2006; Williams and Kremen, in press). In tropical
rainforest biomes of Central and South America and Indonesia and in
temperate grassland biomes in Germany and Canada, pollinator richness,
abundance, and services also respond primarily to proximity to natural or
seminatural habitat at the landscape level (Chacoff and Aizen, 2006; Klein
et al., 2002, 2003a; Morandin and Winston, 2005; Ricketts, 2004; Ricketts
et al., 2004; Steffan-Dewenter and Tscharntke, 1999; Steffan-Dewenter et
al., 2001, 2002), but local factors, such as light (Klein et al., 2002, 2003b)
and the abundance and richness of weedy floral resources (Morandin and
Winston, 2005), also have statistically significant effects.
Pollination services for wild plants that depend on or benefit from
animal pollination are generally provided exclusively by wild pollinator
populations, although managed honey bees often forage on wild plants and,
thus, provide some services (Kremen et al., 2002). Managing wild pollinator communities is needed to ensure pollination function for natural plant
communities. Pollination services to wild plants in habitat fragments can be
influenced by the size and isolation of the fragment, the characteristics of
the surrounding human-modified matrix, and the resulting population responses of plants and pollinators (Bronstein, 1995; Ghazoul, 2005c). Small
fragments tend to have small plant populations (MacArthur and Wilson,
1967), which can be less attractive to pollinators (Brody and Mitchell, 1997;
also reviewed in Kunin, 1997), and thus become pollinator limited (Box 4-1;
Groom, 2001). Smaller fragments often also contain smaller populations
and fewer pollinator species (MacArthur and Wilson, 1967; Miller et al.,
1995; Ricketts, 2001; Steffan-Dewenter, 2003) thus reducing pollinator
visitation (Aizen and Feinsinger, 1994; Cresswell and Osborne, 2004).
Empirical studies, however, have revealed positive, negative, and neutral effects of fragment size on pollinator abundance, richness, and services (Aizen
and Feinsinger, 1994; Cane et al., 2006; Danielsen et al., 2005; Miller et
al., 1995; Tonhasca et al., 2002; Winfree et al., 2006). The variability in
response is probably attributable to differences in habitat specificity and
dispersal ability among pollinator species (Law and Lean, 1999; Saville et
al., 1997; Steffan-Dewenter, 2003).
Geographic isolation also can affect pollination services to wild plants
(Ghazoul, 2005c). Plant populations in isolated fragments could be selflimited by the amount of compatible pollen available (Duncan et al., 2004).
Isolated fragments contain smaller populations and fewer pollinator and

189
plant species (MacArthur and Wilson, 1967) thus reducing pollinator visitation and fruit set (Cunningham, 2000; Steffan-Dewenter and Tscharntke,
1999). Corridors that link habitat fragments have been shown to increase
movement of selected pollinator species and enhance pollination of target
plants (Tewksbury et al., 2002; Townsend and Levey, 2005). Isolation also
can reduce pollinator visitation and seed set (Jennersten, 1988), but in some
cases, even highly isolated plants are known to receive sufficient out-crossed
pollen to reproduce (Nason and Hamrick, 1997; Schulke and Waser, 2001;
White et al., 2002).
All of the fragment-specific factors are likely to be modulated by
the type of human-dominated matrix that surrounds natural fragments
(Ricketts, 2001). If the surrounding matrix is hospitable to wild plants
(Mayfield and Daily, 2005) or contains nesting or floral resources for some
pollinator species (Klein et al., 2002; Westphal et al., 2003), the effects
of fragment size and isolation can be alleviated. Relatively few studies of
pollinator communities and pollination function in fragmented landscapes
consider matrix effects (Cane et al., 2006; Dauber et al., 2003; Hirsch et
al., 2003; Steffan-Dewenter et al., 2006; Williams and Kremen, in press;
Winfree et al., 2006).
Clearly, managing landscapes and sites will be important for restoring,
preserving, or maintaining diverse pollinator communities and ecological
service functions to crops and wild plants. How much natural habitat is
sufficient in the landscape for pollinator maintenance is an open question.
Kremen and colleagues (2004) observed a log-linear relationship between
the amount of pollination services provided to a watermelon crop and the
proportional area of natural habitat within several kilometers of a farm.
Full pollination services could be provided by wild bee communities at
30 percent or more natural habitat cover. Morandin and Winston (2006)
determined that removing 30 percent of land from canola seed production
would actually increase profits to canola farmers, because of the resulting
increased diversity, abundance, and services provided by wild bees. Ricketts
and colleagues (2004) suggested that fragments of at least 20 hectares of
tropical rainforest provide valuable services to coffee from wild bees that
are comparable to other land use values. Equivalent studies of native plants
in natural habitat fragments are lacking.
How patches of habitat should be configured to deliver pollination
services into the surrounding agricultural matrix (in the case of crops) or
to maintain gene flow and population persistence for isolated populations
of wild plants that are confined to fragments also is poorly understood. If
wild pollinators in an area indeed depend on natural habitat fragments for
nesting sites and critical floral resources, then crop pollination can benefit
from a service halo around the habitat fragment corresponding to the
foraging ranges of individual pollinator species (Ricketts, 2001; Ricketts

190
et al., 2004). Dispersing small fragments extensively throughout an area

seems logical but leaves open the question of how to configure large parcels to allow pollinator populations to persist. Both metapopulation theory
(reviewed in Hanski and Ovaskainen, 2000; Harrison and Fahrig, 1995)
and empirical data (Harrison et al., 1988) suggest that some larger patches
are needed to support larger sized populations that are more resistant to
extinction (see also Berger, 1990; Zayed and Packer, 2005). Larger areas also
will, in theory, contain more diverse assemblages of pollinators (MacArthur
and Wilson, 1967; Simberloff and Wilson, 1969) that might provide more
services, more consistently, and contribute to pollination of a wider variety
of crops (Kremen and Chaplin, in press) and other plants (Memmott, 1999;
Memmott et al., 2004). More research is needed to determine the optimal
configuration of landscape fragments and their connectedness to maintain
pollinator populations, communities, and functions.
PUBLIC POLICY AND POLLINATOR POPULATIONS
U.S. Endangered Species Act
The Endangered Species Act (ESA) of 1973 is the broadest and most
powerful U.S. law for the protection of endangered species and their habitats
(NRC, 1995). The act lists species of plants and animals (vertebrate and
invertebrate) as endangered or threatened according to assessments of their
risk of extinction (Congressional Research Service [CRS], 2006). Once a
species is listed, ESAs strict substantive provisions become legal tools to
assist in the species recovery and the protection of its habitat. Endangered
species and their critical habitats are entitled to strong protections. It is illegal, for example, to take any endangered species in the United States or its
territorial waters, and any federal action that will jeopardize the future of
an endangered species is prohibited, including any action that threatens to
destroy or damage critical habitat. At press time for this volume, in the fall
of 2006, 1879 U.S. and foreign animals and plants were listed as endangered
or threatened (U.S. Fish and Wildlife Service [USFWS], 2006).
ESAs major goals include the recovery of endangered and threatened
species to the point at which protection is no longer needed. As this volume
went to press, USFWS (2006) had cataloged 17 U.S. and foreign species
that had been recovered and removed from the list. The populations of
other listed species have increased, and some appear to have stabilized even
though they remain on the list.
A species is placed on the Endangered Species List on the initiative of
the secretary of the interior or of the secretary of commerce. The decision
is based on the best available scientific and commercial information and a

191
lengthy procedure that ensures public participation and the collection of

relevant information. Because Congress directed that listing have a scientific
foundation for the label of threatened or endangered, economic factors are
not considered in the listing decision. In June 2006, there were 282 candidate species for which no decision had been made. The status of those
species is to be monitored and, if any emergency poses a significant risk to
their continued existence, they must be listed promptly.
Modifications of ESA and other recently proposed changes could make
it more difficult to list pollinators than some other animals. A 1981 congressional revision specifically exempted any species of the Class Insecta
determined by the Secretary to constitute a pest whose protection under the
provisions of this Act would present an overwhelming and overriding risk
to man. Any species that has caused economic damage or could do so is
less likely to be protected. The larvae of some lepidopteran pollinators, for
example, and the adults of some hymenopteran pollinators can under some
circumstances cause economic damage. Securing endangered status for them
could prove problematic.
Recent efforts to amend ESA also could add new barriers to listing
pollinators. H.R. 3824, passed by the House of Representatives in 2005,
To amend and reauthorize the Endangered Species Act of 1973 to provide
greater results conserving and recovering listed species, and for other purposes replaces the criterion of best scientific and commercial data available with best available scientific data. More important, unlike ESA
itself, H.R. 3824 for the first time defines best available scientific data
as scientific data, regardless of source, that are available to the Secretary
at the time of a decision or action for which such data are required by this
Act and that the Secretary determines are the most accurate, reliable, and
relevant for use in that decision or action. The secretary is directed to issue regulations that establish criteria for best available scientific data and
must ensure that the information consists of empirical data or data found in
sources that have been subjected to peer review by people recognized by the
National Academy of Sciences [NAS] as qualified to independently review a
covered action in a manner that is in compliance with the Data Quality Act
(44 USC 3516) (Congressional Research Service, 2006). According to CRS,
Some contend that the specification of empirical data in H.R. 3824 would
exclude estimates derived from models and limit the type of data available
for use.... However, estimates derived from modeling could be allowed
under H.R. 3824, if it meets the NAS peer-review conditions set forth in the
bill. Because of the paucity of data available for many pollinator species
(Chapter 2), assessments of species status often are based on information
derived from population models or from genetic studies, which could be
excluded if ESA is amended as proposed.

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Incentives for Stewardship

The public benefits provided by wild pollinators justify public policy
that encourages stewardship of wild pollinators. Given the importance of
habitat, land stewardship policies constitute the majority of relevant mechanisms. However, consumer-oriented measures also have a role in pollinator
conservation policies.
For agricultural lands, there are four voluntary programs that can be
used or adapted to create or maintain pollinator habitat. The Farm Security
and Rural Investment Act of 2002 (the Farm Bill) authorized them:
The Wildlife Habitat Incentives Program (WHIP) (NRCS, 2006a)
provides cost sharing and incentive payments to eligible farmers for planting
native and nonnative plants that could enhance wildlife habitat (including
pollinators) through early successional habitat development, riparian herbaceous cover, tree and shrub establishment, and upland and wetland habitat
management.
The Environmental Quality Incentives Program (EQIP) (NRCS,
2006b) also provides money to eligible farmers who focus on soil and water
conservation. The program can be customized to include pollinator habitat
through improvements in hedgerows, riparian buffer strips, tree and shrub
planting, and wildlife habitat management.
The Conservation Reserve Program (CRP) (USDA-FSA, 2006) pays
eligible farmers to convert agricultural land to conservation uses under a
10-year contract. Farmers make bids that describe their land management
plans and the annual payments they would require. The Farm Service
Agency (FSA) evaluates the bids in light of technical advice from NRCS. The
evaluation is based on state priorities, and points are awarded for expected
conservation benefits from plans that include native species, especially
flowering shrubs and forbs. Currently, no points are assigned explicitly for
pollinator habitat.
The Conservation Stewardship Program (CSP) (NRCS, 2006c)
awards 10-year contracts to eligible farmers according to the farmers proposed intensity of stewardship and their proposed practices. CSP payments
for pollinator habitat are available as resource enhancements under the
rubric of wildlife habitat management. In 2005, North Dakotas state
NRCS program covered pollinator habitat under three CSP enhancements
involving native herbaceous cover plots, unharvested tame hay land, and
native woody cover plots (NRCS-North Dakota, 2005).
WHIP, EQIP, and CRP are available to farmers who have traditionally
raised wheat and feed grains eligible for federal price supports. Because of
the tightening federal budget, access to payments for conservation practices
is rationed through priorities established by state technical committees and

193
according to the characteristics of individual conservation plans submitted

by landowners. Many states do not assign points for enhancing pollinator habitat or provide guidance for doing so. In the states that do provide
points, such as Michigan, very few landowners had enrolled as of December
2005. CSP eligibility is further restricted to farmers in a limited number of
watersheds in each state on a list that rotates annually, with the goal of making each watershed eligible every 710 years (A. Herceg, NRCS, personal
communication, December 2005).
Although the four U.S. farm environmental stewardship programs provide a sound vessel for encouraging landowners to enhance pollinator habitat, interest among farmers has been limited. The research base for NRCS
to estimate the on-farm and external conservation benefits from pollinator
habitat also is limited. Development of a national monitoring program for
pollinator species would provide a remedy (Chapter 5).
For nonfarm, private landownershomeowners, public utilities, or
businessesinvestments in pollinator habitat could be encouraged through
income tax deductions. Public agencies involved in land management, such
as the U.S. Forest Service, the U.S. Department of the Interior, and the U.S.
Department of Transportation, could include provisions for pollinator protection or enhancement in their guidelines. The inclusion of pollinator protection in the criteria for federal land leases for grazing and timber harvest
also could encompass large areas of land. Some interstate highways already
have wildflower plantings, which could be enhanced by purposeful selection
of appropriate native plant species favored by wild pollinators.
Volunteer networks also could encourage creation or restoration of
pollinator habitats much as they have done for pollinator monitoring in the
Audubon Societys annual Christmas Bird Counts and the North American
Butterfly Associations Fourth of July counts (Chapters 2 and 5). Monarch
Watchs Monarch Waystation program has already resulted in the creation
and registration of more than 600 butterfly-friendly habitats with nectar resources and host plants. A private, nongovernmental organization interested
in pollinators might establish a friends of pollinators network that could
be diffused through school programs and public service announcements.
Interest could be sparked through activities such as a landscape architecture
competition for designs that invite and support pollinator populations.
Even consumers can engage in pollinator protection. Following the successful ecolabeling campaigns for dolphin-safe tuna and shade-grown coffee,
a label could be used to certify pollinator-safe fruits and vegetables. With
the important exception of the USDA organic label, most food certification
labelling is done by private organizations. Currently, however, there are no
known organizations that are both interested in and capable of developing
and providing certification for a pollinator-protector label.

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ADAPTIVE MANAGEMENT AND POLLINATOR MONITORING

Different management strategies can be used across landscapes, including public and private lands, working lands, and natural areas, to improve
conditions for pollinators and to maintain pollination function in crops
and wild plants. Strategies range from site-specific management that could
be performed by private landowners, to landscape and regional actions
that would require coordination by county, state, or regional authorities
and nongovernmental organizations. Although management actions can
be guided by a body of existing scientific knowledge, all are experimental;
therefore, concurrent monitoring of pollinator status and of pollination
function is needed (Chapter 5) to determine the efficacy of different strategies and to adapt measures to provide even better performance (Kremen et
al., 1993; Margoluis and Salafsky, 1998; Walters and Holling, 1990).
CONCLUSIONS
This chapter presents various actions that could be taken to maintain
commercial pollinators, wild pollinator species and communities, and pollination function. The committee suggests the following as priorities.
Apis
Develop and refine both traditional and molecular methods for
identifying bees with economically desirable traits for inclusion in honey
bee breeding programs.
Select model populations of honey bees with economically desirable
traits for adoption by the beekeeping industry.
Develop educational materials and programs to enable private-sector
queen producers to develop and maintain pest, parasite, and pathogen resistant stocks of honey bees and to serve as reliable sources of quality production queens that produce colonies expressing useful levels of economically
important traits.
Develop sustainable methods for ensuring that Africanized bees do
not degrade the commercial value of existing stocks of honey bees.
Develop resistance management programs to mitigate the adverse
effects of pesticide and antibiotic resistance in honey bee pest, parasite, and
pathogen populations.
Develop methods for the preservation of honey bee germplasm.
Other Commercial Species
Identify commercially viable solutions to the problem of chalkbrood
in the alfalfa leafcutter bee, Megachile rotundata.

195
Identify non-Apis bees with the potential to be developed into economically useful pollinators.
Develop commercially viable methods for culturing economically important species of bumble bees and solitary bees for use as crop
pollinators.
Wild Bees
Inform the publicin particular, the agricultural community and
managers of golf courses, urban parks, and other large urban-suburban
areas such as industrial and academic campusesabout current knowledge
of actions (such as creating pollinator habitat) that can be taken to manage
pollinators.
Conduct field studies in different regions of North America to determine the suites of key floral resources for use in restoration protocols in
each region.
Conduct additional studies that can be used to improve existing
restoration protocols, including monitoring the influence of restoration
activities on population and community dynamics of pollinators and understanding land managers willingness to adopt restoration practices.
Define land-management practices (by NRCS state offices) that encourage pollinator populations that are eligible for federal payments under
existing Farm Bill conservation programs such as EQIP, WHIP, CRP, and
CSP.
Integrate land management practices that encourage pollinator populations at the state level into existing Farm Bill conservation programs such
as EQIP, WHIP, CRP, and CSP.
Conserve existing natural habitats in human-dominated
landscapes.

7
Findings and Recommendations
The Committee on the Status of Pollinatorsa group of 15 academics,

museum-based systematists, and representatives of nongovernmental organizationsconvened in July 2005 and received a set of specific questions
to address:
Are pollinators experiencing serious decline, and if so, to what
degree?
What research and monitoring are needed to provide improved
information?
In cases where decline can be established by available data, what are
its causes and how can they be addressed?
What are the potential consequences of decline in agricultural and
natural ecosystems?
What conservation or restoration steps can be taken to slow, reverse,
or prevent pollinator decline?
The committee was asked to compile and analyze the published literature,
determine the state of knowledge on pollinator status, identify knowledge
gaps, and establish priorities for addressing these gaps. This chapter provides the committees recommendations as they relate to each question
in the statement of task. The recommendations are aimed at improving
documentation of population trends and monitoring declines, addressing
the causes of decline, developing methods of stopping or reversing declines,
and prioritizing research for preventing future declines.
The value of determining the status of North American pollinators
196

FINDINGS AND RECOMMENDATIONS
197
became abundantly clear in short order. More than three-quarters of

angiosperm plant species rely on animals for pollination. Although most
major food grains are wind-pollinated grasses that do not require services
of animal pollinators, most fruits and vegetableswhich add diversity to
the human diet and provide nutrientsare animal pollinated. Animalpollinated crops, including several key oilseed species, also tend to be of
greater economic value than are those not pollinated by animals, and they
provide relatively higher income to growers. Moreover, bee pollination is
required to produce the seeds of major forage and hay crops, such as alfalfa
and clover, which are used to feed animals that, in turn, supply meat and
dairy products. Thus, the contribution of pollinators to the quality of the
human diet makes determining their status in North America an issue of
prime importance.
Estimating the ecological value of pollinators and pollination and predicting the consequences of their losses are considerably more challenging
than estimating their economic value in agriculture. Such estimates are complicated by both the number of species involved and the relative paucity of
information available for most of these species (particularly those in natural
communities). As discussed in Chapter 1, it is reasonable to assume that a
large proportion of flora in uncultivated terrestrial communities of North
America rely upon pollinators to some degree. In a recent assessment of the
susceptibility of ecosystem services to species losses (Chapter 1), animalmediated pollination is considered a service for most ecosystems and losses
of pollinator would affect trophic stability.
Among the first topics examined was the question of how to differentiate between pollinator shortage and pollinator decline. Shortages and
declines were recognized as distinct but not necessarily related phenomena.
Shortages entail insufficient supply to meet demand according to recognized
norms; declines are trends toward reduction in population size or diversity
over time (Chapter 2). Using these definitions, the committee evaluated the
literature and consulted numerous experts to try to determine the status of
major groups of animal pollinators.
MANAGED POLLINATORS
Status
Population status of most managed pollinators, such as bumble bees
and alfalfa leafcutting bees, are not closely monitored in North America.
Evidence for decline is compelling for the honey bee (Apis mellifera), which
is among the few actively managed pollinator species. Current methods for
documenting the status of managed colonies of A. mellifera, a species of
enormous economic importance (Chapter 1), are surprisingly inadequate

198
(Chapters 2 and 5). Although the U.S. Department of Agricultures (USDAs)

National Agricultural Statistics Service (NASS) tracks managed honey bee
colonies, the surveys focus on honey production rather than on pollination.
The result is the double-counting of some honey-producing colonies and the
omission of others that do not produce honey for commercial sale in the
United States (Chapter 2). Moreover, NASS data do not consider colony
strength or quality. Because data are collected in the United States, Canada,
and Mexico by different methods, making direct comparisons is difficult.
Recommendation: Improved information gathering for the beekeeping
industry is critical, and the NASS should modify its data collection methodologies. The committee specifically recommends that NASS:
Refine its assessment of honey bee abundance. The information
would be more useful if all commercial honey bee colonies were counted
annually and in one location only (as is currently done every 5 years for the
census of agriculture). Greater accuracy also would be gained by determining whether colonies are leased for pollination, used to produce commercial
honey, or both, and which use is primary. NASS should adjust its data collection to include the number of colonies lost during the previous year for
any reason and the number lost over the previous winter. These data should
be available by state to provide a broad picture of the overall health of the
bee industry.
Collect commercial honey bee pollination data from beekeepers and
from crop growers. The availability of commercial honey bees as pollinators would be better understood if data were collected on the specific crops
pollinated and on the leasing fees per colony by crop.
Coordinate and reconcile data collection on honey bee colonies
throughout North America. NASS should make its annual survey definitions
compatible with its 5-year census of agriculture. The United States should
work with Canada and Mexico through the North American Free Trade
Agreements Commission for Environmental Cooperation and the Trilateral
Committee for Wildlife and Ecosystem Conservation and Management to
adopt common methodologies.
Causes of Decline
Introduced parasites and diseases have contributed to declines in managed bees. Varroa mite has had a dramatic negative impact on the abundance of honey bees in North America. Bumble bees also have suffered from
a number of parasites, notably the protozoan parasites Nosema bombi and
Crithidia bombi, and the tracheal mite Locustacris buchneri. Chalkbrood,

199
a fungal disease caused by Ascosphaera, nearly destroyed the ability to

produce alfalfa leafcutting bees in the United States.
For the first time since 1922, honey bees were imported in early 2005
from outside North America after a change in regulations promulgated
under the terms of the Honeybee Act of 1922. Bee imports could increase
the risk of introduction of pests and parasites.
Recommendation: The Animal and Plant Health Inspection Service (APHIS)
should ensure that its regulations prohibit introduction of new pests and
parasites along with imported bees, and Congress should expand the Honey
bee Act of 1922 to include bombiculture and the fostering and breeding
of other imported pollinator species. That is, Congress should extend in
principle the Honeybee Act to other managed pollinator species.
Other factors also could contribute to current and potential future declines in honey bee populations: antibiotic-resistant pathogens (American
foulbrood); pesticide use; and the encroachment of Africanized honey bees,
particularly in the southeastern United Statesa major regional source of
packages, queens, and migratory beekeepers for the rest of the country.
Recommendation: Through research at the Agricultural Research Board
(ARS) and competitive grant programs, USDA should not only continue,
but also expand its efforts to:
Encourage innovative approaches to protecting honey bee health
by
developing sustainable management programs for varroa
mites, including methods for managing pesticide resistance in
mite populations;
identifying additional natural and synthetic pesticides and
least-toxic alternatives for mite control and bee management
(for example, pheromones); and
developing nonchemical cultural bee management practices.
Improve genetic stocks of honey bees by
refining methods for identifying stocks with desirable traits
and for breeding, selecting, maintaining, and improving
stocks with such desirable traits as disease and pest resistance,
moderated temperament, and improved honey production,
taking advantage of the opportunities afforded by the recently
sequenced honey bee genome;
refining methods for high-quality queen production from
selected stocks including controlling mating (for example

200
instrumental insemination, isolated mating, and drone saturation) to ensure expression of desired traits in colonies;
expanding current efforts in germplasm preservation, including cryopreservation;
developing methods for the maintenance of European stocks
in areas of Africanization;
developing a third-party certification program to ensure the
quality and effectiveness of commercial queens marketed or
advertised as being parasite- or pathogen-resistant (or any
other specific trait); and
identifying markers (expressed sequence tags and quantitative
trait loci) as a support to breeding programs (Chapter 6).
The achievement of these objectives will be possible only if ARS maintains current support for research and restores lost positions for scientists.
A special focus will need to be placed on honey bee pollination, and reward
systems for technology transfer should be developed within ARS. Although
honey bees are important pollinators, there also are commercially important
non-Apis species that require attention. The development of management
protocols for wild species and the management of agricultural landscapes
to better sustain wild pollinator populations can help supplement honey bee
populations and reduce the risks associated with sole reliance on a single
pollinator, particularly as pollinator demands rise and shortages become
likely.
Recommendation: The USDA ARS should:
Create research entomology positions in its fruit and vegetable laboratories in geographically diverse regions of the United States to work on
developing new non-Apis pollinators for major crops, on identifying those
with potential for use as commercial pollinators, and on establishing protocols for management. These activities should augment work in the Bee
Biology and Systematics Laboratory in Logan, Utah, which currently serves
as a focal point for non-Apis research.
Develop and implement bombiculture disease management programs
to prevent pathogen spillover to wild populations.
Address pathogen problems in culturing alfalfa leafcutting bees
(megachileculture) to improve population sustainability and crop pollination efficacy.
Conduct and encourage research on landscape and farm management as related to pollinator populations and communities, and ARS should
provide guidance on pollinator-friendly management practices.

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Recommendation: Private-sector funding mechanisms for honey bee health

and technology transfer from federal, state, and university research facilities
should be created and enhanced to meet pollination needs. Industry checkoff programs, which now cover crop commodities and honey, could add
honey bee pollination services to the scope of existing programs. Check
off programs collect funds from an agricultural commodity group to support research and promote the commodity. This private-sector effort could
complement federally funded basic research efforts and promote translational research.
Pollinator declines will not jeopardize food supplies because grainsthe
worlds primary sources of dietary energydo not depend upon animal pollinators. However, supplies of animal-pollinated foodsfruits, vegetables,
and some nutswould be affected. Among the most conspicuous demonstrable consequences of changing pollinator status in agriculture are the
rising costs of pest control in apiculture (and hence rising costs for honey
bee rental) that accrue from the mite management required to maintain
stable honey bee populations. Honey bee rental costs also are rising because
of an increase in demand from almond growers that resulted from acreage
increases and seasonal instability in honey bee populations. Despite overwhelming reliance on one species, few alternative actively managed species
are being used. And despite evidence of their efficacy as crop pollinators,
wild species are not being exploited to the extent possible.
Recommendation: USDA should establish discovery surveys for crop pollinators throughout the range of crops in North America to identify the
contributions of wild species to agricultural pollination.
WILD POLLINATORS
Status
The committee found that the strength of the evidence for population
status varies from one taxon to another. In parts of their ranges, the declines
in several vertebrate pollinator species, particularly bats, are evidenced by
conservation program monitoring. Long-term studies by individual investigators and regional Heritage Programs also provide evidence for declines
(and possible extinction in some cases) among bumble bee species and some
1Translational
research is the process of applying ideas, insights, and discoveries generated

through basic scientific inquiry to industrial or agricultural uses.

202
butterflies as do recent additions to endangered species lists (Chapter 2).

Many other pollinators (including several flies, wasps, and beetles) could
be declining, even rapidly, but insufficient data are available to provide unambiguous documentation of trends. Historical data could be collected by
mining museum collections. However, data mining could be difficult for species that are not well described. Insects that constitute the majority of pollinator species are less well describedtaxonomically or ecologicallythan
are other animal pollinators. In fact, taxonomic impediments for insects are
enormous with respect to documenting declines (Chapter 2).
Recommendation: To address the taxonomic impediment to assessing
pollinator status, the USDAs ARS should expand basic research on the
systematics of pollinators and on the development of rapid identification
tools.
Causes of Decline
The causes of decline or factors contributing to it could be assigned
definitively in only a few cases (Chapter 3). Decline in populations of some
native bumble bees appears to be the result of infection with non-native
protozoan parasites, including Nosema bombi and Crithidia bombi. These
parasites probably came from commercial bumble bees imported from
Europe for greenhouse pollination. The managed bees used in greenhouse
pollination often harbor high pathogen loads, and when they escape from
greenhouses, pathogen spillover into native species occurs. For some species, competition with exotic pollinators (including honey bees) can lead to
population declines. Declines in many pollinator taxa also are thought to be
associated with habitat loss, fragmentation, and deterioration, although in
North America, data are in most cases inadequate to demonstrate causation
unambiguously. One exception is the decline in bat populations that is associated with destruction of cave roosts, but there is evidence that other factors
also contribute to pollinator species decline. Changes in the phenology of
interactions, ranges, and distributions that lead to loss of synchrony (possibly because of global climate change) and to disruption of migratory routes
(making migration an endangered phenomenon) are posited for humming
birds, nectar-feeding bats, and some butterflies and moths.
Recommendation: To prevent pathogen spillover to wild populations,
APHIS should require that any commercially produced bumble bee colony
shipped within the United States be certified as disease free.

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The consequences of pollinator decline in nonagricultural systems are
more difficult to document. Few plant species rely on a single pollinator;
many have more than one. Nevertheless, there are documented examples of
reduced fruit and seed set in native plants apparently in response to a paucity
of pollinators. Pollen limitation of seed set is common in wild plants, but its
population consequences are not clear. In the event of declining pollinator
populations, some plant populations could become more vulnerable to an
extinction vortexthe interacting factors that serve to progressively reduce
small populationsbecause of the increased risks of incurring the demographic and genetic consequences of small population size. These include
genetic erosion, inbreeding depression, decreased reproductive success, and
greater susceptibility to catastrophes and random changes in environmental
conditions. Therefore, the effects of pollinator decline on rare plant species
or on those with small populations also should be given special attention.
Recommendation: The U.S. Geological Survey, the Fish and Wildlife Service,
and other agencies responsible for natural resource protection should establish discovery surveys for pollinators of rare, threatened, and endangered
plant species.
Monitoring
Little is known about the status of most wild pollinators in North America because there is seldom a historical baseline with which modern data can
be compared. The committee notes that systematic, thorough monitoring
programs in Europe have revealed dramatic declines in pollinator abundance and diversity (Chapter 5); there are no comparable North American
programs. The European experience demonstrates that monitoring is needed
to document changes in populations and diversity, and that monitoring
programs profit from contributions by citizen-scientists. The quality and
validity of the information obtained by citizen-scientists monitoring should
be tested and calibrated against professional science monitoring.
Two sampling strategies could compensate for the absence of baseline
data. First, existing historical data could be used in conjunction with contemporary survey data to guide focused assessments of the status of pollinators in specific regions of North America. Second, a long-term annual
monitoring program could be initiated expressly to establish baseline data
for comparison at different times in the future. In contrast to an assessment
that provides a one-time snapshot, such monitoring can elucidate trends in
species abundance and in the relationships between changes in community
composition and their putative environmental causes. Understanding those

204
relationships is crucial for developing plans to mitigate environmental

change and to manage for species persistence.
Recommendation: The federal government should establish a network of
long-term pollinator-monitoring projects that use standardized protocols
and joint data-gathering interpretation in collaboration with Canada and
Mexico. A rapid, one-time assessment of the current status of wild pollinators in North America to establish a baseline for long-term monitoring is a
laudable initial goal.
Components of this two-part assessment and monitoring program should
include:
assessment that targets re-surveys of areas that had been well sampled in the past and mining museum collections (specimens and labels) and
the literature for historical data that correspond to areas of continuous,
high-intensity sampling;
monitoring that integrates the work of professional scientists and
citizen-scientists in tracking pollinator status and pollination function to
maximize the depth and breadth of effort.
The selection of study species should correspond to the strength of evidence for decline. In view of collective evidence of population declines, bees
would provide a logical initial focus. Lepidoptera constitute another group
for which a compelling need for monitoring exists, given recent extinctions
and the classifications of some species as endangered or threatened.
Conservation and restoration are crucial to the preservation of pollinator populations and diversity, but more must be learned about pollinator
biology. Research on the basic biology and ecology of wild pollinators is
inadequate.
Recommendation: Because of the importance of pollination as an ecosystem
service in both agricultural and natural ecosystems, the National Science
Foundation and USDA should recognize pollination as a cross-cutting
theme in their competitive grant programs and work together to integrate
research that ranges from the genomics of honey bees and the systematics
and ecology of wild pollinators to the effects of global climate change on
pollinator-plant interactions. Representative areas where research is needed
include:

205
Multidisciplinary research that promotes sustainable pollinator

populations;
Identification of causes and consequences (genetic erosion and pollen
limitation) of pollinator decline;
Ecology, restoration, conservation, and management of pollinators
and pollination services, including investigation of effects of invasive plants
and animals on pollination systems; and
Small Business Innovation Research programs to promote technology transfer to address the health and sustainability of commercially managed pollinators.
Despite sketchy data on wild pollinators, there are viable pollinatorfriendly land management practices. These include, for example, providing
corridors to link habitat fragments and thus to encourage pollinator movement; configuring landscape fragments to maintain pollinator populations,
communities, and functions; using low- and no-till agriculture to preserve
native pollinators nests in fields; and setting aside land for field margins to
provide nesting habitat and forage for pollinators. However, these practices
are not in wide use (Chapter 6), and land managers should be offered economic incentives to adopt such practices.
Recommendation: Economic incentives should be expanded for pollinator
conservation.
State-level Natural Resources Conservation Service (NRCS) offices
should provide lists of scientifically tested and approved pollinator-friendly
practices to farmers participating in USDA cost-share programs (the Wildlife
Habitat Incentives Program and the Environmental Quality Incentives Program), land retirement programs (the Conservation Reserve Program [CRP]
and the Conservation Reserve Enhancement Program), and the production
stewardship programs (Conservation Security Program [CSP]).
CRP should explicitly incorporate pollinator habitat in the
environmental-benefits index used to evaluate land parcel proposals.
CSP should incorporate the value of pollinator habitat development
into its determination of the stewardship tiers that are the basis for federal
payments.
USDA cost-sharing, land retirement, and production stewardship
programs should be available to producers of all commoditiesfruits, nuts,
and vegetablesthat depend on pollinators.
The NRCS should target new hiring of personnel whose expertise is
in biological sciences, especially ecology and natural-area management.
As discussed in Chapter 5, a two-part program to assess the current

206
status of wild pollinators in North America and to establish a framework

for long-term monitoring of pollinator populations and function over time
is a laudable goal. New long-term monitoring programs should maximize
results obtained per dollar spent by integrating professional scientist monitoring activity with citizen-scientist monitoring activity in assessing both
pollinator status and pollination function. The professional science activities
fall within the mandate of governmental agencies, including the USDA, the
U.S. Geological Survey, the U.S. Fish and Wildlife Service, and the National
Science Foundations proposed National Ecological Observatory Network.
The citizen-scientist activities could be coordinated through partnerships
among nongovernmental organizations (NGOs), governmental organizations, and citizen groups. Participating NGOs for a North American Pollination Monitoring Program could include the North American Pollinator
Protection Campaign, the Xerces Society, Monarch Watch, and likely citizen-scientist groups such as native plant societies, gardening clubs, schools,
friends of nature reserves, community farm alliances, or commodity groups.
The Pollinator Watch Program in Canada is currently under development
through the Environmental Monitoring and Assessment Networks Nature
Watch Program (http://www.eman-rese.ca/eman/naturewatch.html). Federal
agencies could stimulate collaborative programs that encourage agency,
university, and NGO scientists to work together via strategically formulated
funding announcements. The participation of volunteer citizen-scientists
through the NGOs could greatly increase the output of assessment programs
at little additional cost.
Nonfarm landowners, such as homeowners and private businesses,
also could contribute to conservation of pollinators, with little investment
(Box 6-3). Wildflower plantings provide resources for bees, and wood fences
can provide nesting sites for twig-nesting bees. Raising public awareness and
educating the next generation about the importance of pollinators and what
people could do to protect them is critical.
Recommendation: As part of their outreach, federal granting agencies
should make an effort to enhance public understanding of the importance
of pollination as an ecosystem service through support for citizen-scientist
monitoring programs, teacher education, and K12 and general public
education efforts that center on pollination.
Recommendation: Professional societies (Ecological Society of America,
Entomological Society of America, American Association of Professional
Apiculturists, Botanical Society of America) and NGOs (North American
Pollinator Protection Campaign, Xerces Society for the Preservation of
Endangered Invertebrates) should collaborate with landowners and the
public to increase awareness of the importance of pollinators and to pub-

207
licize simple activities the public can do to promote and sustain pollinator
abundance and diversity.
Although the object of the Endangered Species Act of 1973 (ESA) is to
protect endangered species and their habitats, many endangered pollinators
are not recognized candidates for endangered or threatened status. Congress
directed that listing of a species required a scientific determination of its
continued existence as threatened or endangered, but data on many pollinators are sparse. Also, a 1981 congressional revision of the ESA specifically
exempted any species of the Class Insecta determined by the Secretary to
constitute a pest whose protection under the provisions of this Act would
present an overwhelming and overriding risk to man. Some caterpillars
and carpenter bees, for example, can cause or have the potential to cause
damage, so it could be difficult to use ESA to achieve protection for those
species.
Recommendation: Congress should not consider any ESA amendment
that would create additional barriers to listing pollinator species as
endangered.

Glossary
Africanized honey bee Apis mellifera scutellata, originally from central

and south Africa, taken to Brazil in 1957, migrated northward through South and Central
America, finally to the southern regions of the
United States. Noted for defending nests vigorously and for throwing off swarms any time of
the year.
Allee effect
Inverse density dependence at low densities. For

example, seed set can decline drastically at low
plant densities if pollinators cannot find plants to
effect cross-pollination.
American foul brood
A bacterial disease (caused by Paenibacillus) of

honey bees that produces a foul odor in dead bee
larvae. A similar disease is called European foul
brood.
Anther
Pollen-bearing portion of a stamen.
Apiary
Groups of hives that contain honey bee colonies;

apiaries are sometimes called outyards.
Autogamy
The quality of self-fertility and self-pollinating in

plants.
Bee hive
The physical construct for honey bees: a hollow tree, a Langstroth hive, a woven straw skep,
or any other container of the right volume and
physical properties.
Beeswax
A complex lipoidal secretion from the fourpaired wax glands of young worker bees.
208

209
GLOSSARY
Bombiculture
Domestication of bumble bees for commercial

propagation.
Brood
The eggs, larvae, and pupae within a honey bee

or bumble bee colony. Immature honey bees live
in the central portion of older darkened combs;
pollen and honey are stored at the periphery of
the brood area.
Bulbil
Asexual bulb-shaped reproductive unit of agaves

and other plants. Bulbils are produced on flowering stalks if pollinators fail to visit flowers; they
are not produced by fertilization. Seeds are not
produced and before the death of the semelparous plant, clonal, tiny agaves grow from the
unfertilized flowers.
Bumble bee
Bee of the genus Bombus, widely distributed

throughout North America and some other continents. Bumble bees are social and have annual
colonies; some species are managed commercially for greenhouse pollination, especially of
tomatoes.
Buzz pollination
The process by which a pollinatorusually

bumble bee or a solitary bee, but not a honey
beeattaches itself to a flower and vibrates its
flight muscles. The pollinators movement causes
pollen to be dislodged from the anther.
Carpenter bee
Large solitary bee that lays eggs in tunnels bored

into wood or plant stems.
Colony
Social insects including honey bees organized

by caste (sterile female workers, male drones, a
queen mother). The bee colony has been labeled
a superorganism, and it can have as many as
60,000 individuals at its peak. The colony lives
in a hive or nest. Bumble bee colonies are annual
and much smaller (fewer than 30 bees at high
altitudes) than are honey bee colonies.

210
Crithidia bombi
An intestinal parasite (trypanosome) of bumble

bees.
Cross-pollination
Pollination by pollen from another plant.
Dioecia
The condition of plants with staminate and pistillate flowers borne on separate individuals.
Drone
A male honey bee that does not forage for itself

at flowers, but is fed by its sisters. Haplodiploid genetic sex determination in bees, ants, and
wasps results in males having one set of chromosomes. Drones are haploid; their sisters have two
sets of chromosomes and are diploid. Drone bees
develop from unfertilized eggs.
Event selection
Selection for successful genetic transformation

of a plant (for example, corn) with a genetically
engineered sequence.
Extinction vortex
Interaction of multiple factors that progressively forces an already small population into
extinction.
Fecundity
Ability to reproduce regularly and easily; typically measured in plants as fruit set or seed set.
Floret
A small flower in the composite (Asteraceae)

inflorescence or the spike of a grass.
Founder effect
Genetic drift that results from the founding of a

population by a small number of individuals.
Fruit set
Formation of fruit as a result of pollination and

fertilization.
Geitonogamy
Pollination by pollen from another flower on the

same plant.
Genetic drift
Change in the gene pool of a small population

attributable to chance (Campbell et al., 1999).

211
GLOSSARY
Haplodiploidy
Sex determination in bees, ants, and wasps.

The queen controls whether eggs are fertilized. The females, which emerge from fertilized
eggs, are workers and diploid with both sets of
chromosomes. Male are haploid, coming from
unfertilized eggs and having only one set of
chromosomes.
Hemizygosity
The state of having unpaired genes in an otherwise diploid cell.
Hermaphrodite
An organism that has male and female reproductive organs, for example, plants with perfect
flowers.
Heterozygosity
The state of possessing different alleles of the

same gene.
Hive
The location (the tree, Langstroth hive box, or

similar cavity) of a honey bee colony. Also called
the nest or nest box.
Homozygosity
The state of possessing two identical alleles of

the same gene.
Honey bee
A social, honey-making bee of the genus Apis,

found mostly in tropical Asian regions.
Inbreeding
The breeding of closely related plants or animals;

in plants, it occurs generally by repeated selfpollination (Raven et al., 2005).
Larva
Immature stage of insect species that undergo

metamorphosis (caterpillar, grub, maggot).
Leafcutter bee
Bee in the family Megachilidae that cuts rounded

pieces from leaves and flowers to line its nest.
Megachileculture
Culture of leafcutter bees for commercial

propagation.

212
Migratory beekeepers
Beekeepers who take their hives from one place

to another. They exploit ephemeral blooms to
make specialty honey or to provide pollination
service.
Monoecious
Staminate and pistillate flowers borne on the

same plant.
Nectar
The sugary often complex watery mixture produced by secretory glands within flowers and
from extrafloral nectaries. The high-energy sugar
fuel sought by bees and other pollinators, which
typically also contains amino acids. A floral
reward exchanged for pollination services.
Nectar robbing
Extraction of nectar through a hole pierced in

the corolla, a practice of some short-tongued
bumble bees and carpenter bees that allows them
to extract nectar from long-tubed flowers.
Nosema
A bee disease caused by a protozoan (Nosema

apis). Nosema bombi is a disease of bumble bees.
Ovule
A structure in seed plants containing the female

gametophyte with an egg cell; when fertilized
and mature, an ovule becomes a seed.
Package bees
A 23-lb aggregation of bees supplied by a

breeder. Packages are used to start new colonies.
Parthenocarpy
Fruit production in flowering plants without pollination. Parthenocarpy can be induced by plant
hormones or genetic modification.
Perfect flower
A flower that contains both male and female

reproductive parts.
Pistil
Female reproductive organ of a flower that consists of a stigma, style, and ovary.

213
GLOSSARY
Pollen
The male sex cells of flowering plants (angiosperms) that are found within the microscopic
tough-shelled pollen grains. Pollen must be
moved from flower to flower for fertilization.
The sex cells travel down pollen tubes that grow
through the floral style and fertilize the ovules.
Seeds develop within the ovary and the fruit
forms. Pollen grains also are the indispensable
protein and lipid-rich food of bees and many
other pollinators.
Pollination
The transfer of pollen grains from flower to

flower and usually plant to plant by wind, water,
or animals.
Queen bee
The mother of the bees in a nest; usually a single

queen inhabits a mature bee colony. The queen
can lay 1,500 or more eggs per day during her
lifespan of 23 years. If a queen dies, the colony
can produce a new queen from a diploid worker
egg.
Seed set
Formation of seeds, typically after pollination.
Self-compatibility
The condition that allows a plant to accept fertilization by its own pollen.
Self-incompatibility
The condition that prevents a plant from accepting fertilization by its own pollen.
Self-pollination
Pollination by pollen from the same flower or

same plant (see geitonogamy); selfing.
Split or divide
Beekeepers can divide or split half of the adults,

brood, and honey combs from a populous mother colony into two Langstroth hive boxes. A new
queen is supplied to the daughter colony, or the
bees are allowed to be queenless for a time and
to raise a new queen from an egg laid by the old
queen.
Stamen
Male reproductive organ of a flower that typically includes a filament bearing an anther.

214
Stigma
Region of a carpel (female productive organ of a

flower) that serves as a receptive surface for pollen grains and on which they germinate.
Tracheal mite
Acarapis woodi, parasite of honey bees, accidentally introduced into the United States that has
caused colony mortality in many locations.
Trioecious
Staminate, pistillate, and perfect flowers borne

on different plants.
Varroa mite
Varroa jacobsoni, a parasite, accidentally introduced from Asia that became established in the
United States. It continues to cause heavy mortality of bee colonies in some regions. The mite
feeds externally on bee larvae and pupae within
the brood combs.
Worker
One of the thousands of sterile daughters of the

queen. Worker ovaries usually are undeveloped.
Workers typically work inside and then outside
the nest as foragers, living for only 46 weeks
during the spring and summer months. Bumble
bee queens also produce workers, but many
fewer than honey bees.
Xenogamy
Cross-pollination and cross-fertilization of

plants.

References
AAAS (American Association for the Advancement of Science). 1994. Benchmarks for Science
Literacy. Available at http://www.project2061.org/publications/bsl/online/bolintro.htm.
Accessed May 31, 2006.
ABF (American Beekeeping Federation). 2005. Honey Bee Pollination Crisis: Shortage of Bees
May Reduce Crop Production. Available at: http://abfnet.org/?p=51. Accessed May 15,
2006.
Abu-Asab, M.S., P.M. Peterson, S.G. Shetler, and S.S. Orli. 2001. Earlier plant flowering in
spring as a response to global warming in the Washington, DC, area. Biodiversity Conservation 10:597612.
Acciarri, N., F. Restaino, G. Vitelli, D. Perrone, M. Zottini, T, Pandolfini, A. Spena, and G.L.
Rotino. 2002. Genetically modified parthenocarpic eggplants: improved fruit productivity
under both greenhouse and open field cultivation. BMC Biotechnology 2:4.
Adey, M., P. Walker, and P.T. Walker. 1986. Pest Control Safe for Bees. A Manual and
Directory for the Tropics and Subtropics. Cardiff: International Bee Research Association.
224pp.
Adlerz, W.C. 1966. Honey bee visit numbers and watermelon pollination. Journal of Economic
Entomology 59:2830.
Agosti, D., and N.F. Johnson, eds. 2005. Antbase. Available at: Antbase.org, version (May
2005).
Agosti, D., J.D. Majer, L.E. Alonso, and T.R. Schultz, eds. 2000. Ants: Standard Methods for
Measuring and Monitoring Biodiversity. Biological Diversity Handbook Series. Washington and London: Smithsonian Institution Press.
Aizen, M.A., and P. Feinsinger. 1994. Forest fragmentation, pollination, and plant reproduction
in a Chaco dry forest, Argentina. Ecology 75:330351.
Alippi, A.M, G.N. Albo, D. Leniz, I. Rivera, M.L. Zanelli, and A.E. Roca. 1999. Comparative study of tylosin, erythromycin and oxytetracycline to control American foulbrood of
honey bees. Journal of Apicultural Research 38(34):149158.
Allen, M.F., and B.V. Ball. 1996. The incidence and world distribution of the honey bee viruses.
Bee World 77:141162.
215

216
Allen-Wardell, G., P. Bernhardt, R. Bitner, A. Burquez, S. Buchmann, J. Cane, P.A. Cox,

V. Dalton, P. Feinsinger, M. Ingram, D. Inouye, C.E. Jones, K. Kennedy, P. Kevan,
H.Koopowitz, R. Medellin, S. Medellin-Morales, and G.P. Nabhan. 1998. The potential
consequences of pollinator declines on the conservation of biodiversity and stability of
food crop yields. Conservation Biology 12(1):817.
Altieri, M.A., and C.I. Nicholls. 2004. Biodiversity and Pest Management in Agroecosystems.
2nd edition. New York: Haworth Press.
Altizer, S., W.M. Hochachka, and A.A. Dhondt. 2004. Seasonal dynamics of mycoplasmal
conjunctivitis in eastern North American house finches. Journal of Animal Ecology
73:309322.
Ananthakrishnan, T.N. 1993. The role of thrips in pollination. Current Science (Bangalore)
65(3):262264.
Anderson, D.L., and J.W.H. Trueman. 2000. Varroa jacobsoni (Acari: Varroidae) is more than
one species. Experimental and Applied Acarology 24:165189.
Anderson, P.L., R.L. Hellmich, R. Jarrad, J.R. Prasifka, and L.C. Lewis. 2005. Effects on fitness
and behavior of monarch butterfly larvae exposed to a combination of Cry1Ab-Expressing corn anthers and pollen. Environmental Entomology 34(4):944952.
Anderson, R.P., M. Gomez-Laverde, and A.T. Peterson. 2002. Geographical distributions of
spiny pocket mice in South America: insights from predictive models. Global Ecology
and Biogeography 11:131141.
Anonymous. 1987. Varroa mites found in the United States. American Bee Journal
127:745746.
Anonymous. 2005. Minnesota beekeepers and DNR settle claims. Bee Culture 133:51.
Aratanakul, P., and M. Burgett. 1975. Varroa jacobsoni: a prospective pest of honeybees in
many parts of the world. Bee World 56:119121.
Arita, H.T. 1993. Conservation biology of the cave bats of Mexico. Journal of Mammalogy
74:693702.
Arita, H.T., and K. Santos-del-Prado. 1999. Conservation biology of nectar-feeding bats in
Mexico. Journal of Mammalogy 80:3141.
Arizaga, S., and E. Ezcurra. 1995. Insurance against reproductive failure in a semelparous plantBulbil formation in Agave macroacantha flowering stalks. Oecologia
101:329334.
Arizaga, S., and E. Ezcurra. 2002. Propagation mechanisms in Agave macroacantha (Agavaceae), a tropical arid-land succulent rosette. American Journal of Botany 89:632641.
Arizaga, S., E. Ezcurra, E. Peters, F.R. de Arellano, and E. Vega. 2002. Pollination ecology
of Agave macroacantha (Agavaceae) in a Mexican tropical desert. I. Floral biology and
pollination mechanisms. American Journal of Botany 87:10041010.
Arizmendi, M.C., and J.F. Ornelas. 1990. Hummingbirds and their floral resources in a tropical
dry forest in Mexico. Biotropica 22:172180.
Arizona Game and Fish Department. 2006. Hertitage Data Management System. Available at:
http://www.azgfd.gov/w_c/edits/documents/Leptcuye.fi.pdf. Accessed May 19, 2006.
Armstrong, J.A. 1986. Floral biology of Myristica fragrans Houtt. (Myristicaceae), the nutmeg
of commerce. Biotropica 18:3238.
Arroyo-Cabrales, J., R.R. Hollander, and J.K. Jones, Jr. 1987. Choeronycteris mexicana. Mammalian Species 291:15.
Asai, W.K. 2005. Nuts: striving for higher yields. American Fruit Grower 125:90.
Ascher, J.S. 2001. Hylaeus hyalinatus Smith, a European bee new to North America, with
notes on other adventive bees (Hymenoptera: Apoidea). Proceedings of the Entomological
Society of Washington 103:184190.
Asher, J., M. Warren, R. Fox, P. Harding, G. Jeffcoate, and S. Jeffcoate. 2001. Millennium Atlas
of Butterflies in Britain and Ireland. Oxford: Oxford University Press.

REFERENCES
217
Ashman, T.L., T.M. Knight, J.A. Steets, P. Amarasekare, M. Burd, D.R. Campbell, M.R.
Dudash, M.O. Johnston, S.J. Mazer, R.J. Mitchell, M.T. Morgan, and W.G. Wilson.
2004. Pollen limitation of plant reproduction: ecological and evolutionary causes and
consequences. Ecology 8:24082421.
Asikainen, E., and P. Mutikainen. 2005. Preferences of pollinators and herbivores in gynodioecious Geranium sylvaticum. Annals of Botany 95(5):879886.
Asner, G.P., A.J. Elmore, L.P. Olander, R.E. Martin, and A.T. Harris. 2004. Grazing systems,
ecosystem responses, and global change. Annual Review of Environment and Resources
29:261299.
Bailey, A.M., and R.J. Niedrach. 1965. Birds of Colorado. Denver: Denver Museum of Natural
History. Vol. 12, 895 pp.
Baker, H.G. 1975. Sugar concentrations in nectars from hummingbird flowers. Biotropica
7:3741.
Baker, H.G., and P.D. Hurd, Jr. 1968. Intrafloral ecology. Annual Review of Entomology
13:385414.
Baker, H.G., I. Baker, and S.A. Hodges. 1998. Sugar composition of nectars and fruits consumed by birds and bats in the tropics and subtropics. Biotropica 30:559586.
Baker, J.D.R., and W. Cruden. 1991. Thrips-mediated self-pollination of two facultatively
xenogamous wetland species. American Journal of Botany 78:959963.
Baker, R.J., L.C. Bradley, R.D. Bradley, J.W. Dragoo, M.D. Engstrom, R.F. Hoffmann, C.A.
Jones, F. Reid, D.W. Rice, and C. Jones. 2003. Revised Checklist of North American
Mammals North of Mexico, 2003. Occasional Paper OP-229. Lubbock, Tex.: Museum
of Texas Tech University, NSLR Publications. 24 pp.
Banda, H.J., and R.J. Paxton. 1991. Pollination of greenhouse tomatoes by bees. Acta Horticulturae 288:194198.
Banks, R.C., and W.A. Calder. 1989. Did Lewis and Clark discover the broad-tailed hummingbird (Selasphorus platycerus). Archives of Natural History 16:243244.
Barg, R., S. Shabtai, N. Carmi, M. Pilowsky, and Y. Salts. 2001. Transgenic parthenocarpy in
determinate and indeterminate tomato cultivars. Acta Horticulturae 560:207210.
Barkin, D. 2003. Alleviating poverty through ecotourism: promises and reality in the monarch
butterfly reserve of Mexico. Environment, Development and Sustainability 5:371382.
Barrett, D.P. 1955. History of American foulbrood in Michigan: period 19271954. Gleanings
in Bee Culture 83:460461.
Barth, F.G. 1985. Insects and Flowers: The Biology of a Partnership. Translated from German
by M.A. Biederman-Thorson. Princeton University Press. 297 pp.
Barth, F.G. 1991. Insects and Flowers: The Biology of a Partnership. Translated from German
by M.A.Biederman-Thorson. Princeton University Press. 408 pp.
Barthell, J.F., and R.W. Thorp. 1995. Nest usurpation among females of an introduced leafcutter bee, Megachile apicalis. Southwestern Entomologist 20:117124.
Barthell, J.F., G.W. Frankie, and R.W. Thorp. 1998. Invader effects in a community of cavity nesting megachilid bees (Hymenoptera: Megachilidae). Environmental Entomology
27:240247.
Barthell, J.F., J.M. Randall, R.W. Thorp, and A.M. Wenner. 2001. Promotion of seed set in
yellow star-thistle by honey bees: evidence of an invasive mutualism. Ecological Applications 11(6):18701883.
Bartholomew, C.S., and K.V. Yeargan. 2001. Phenology of milkweed (Asclepiadaceae) growth
and monarch (Lepidoptera: Nymphalidae) reproduction in Kentucky and ovipositional
preference between common and honeyvine milkweed. Journal of the Kansas Entomological Society 74:211220.
Batabyal, A.A., and P. Nijkamp. 2005. Alternate strategies for managing resistance to antibiotics and pesticides. Environmental Economics and Policy Studies 7(1):3951.

218
Batra, S.W.T. 1979. Osmia cornifrons and Pithitis smaragdula, two Asian bees introduced
into the United States for crop pollination. Proceedings of the Fourth International Symposium on Pollination, Maryland Agriculture Experiment Station Special Publication 1:
307312.
Batra, S.W.T. 1982. The hornfaced bee for efficient pollination of small farm orchards. Research for small farms. Pp. 116120 in Research for Small Farm, USDA Miscellaneous
Publication 1422, W.H. Kerr and L.V. Knutson, eds.
Batra, S.W.T. 1994a. Anthophora plumipes villosula Sm. (Hymenoptera: Anthophoridae),
a manageable Japanese bee that visits blueberries and apples during cool, rainy, spring
weather. Proceedings of the Entomological Society of Washington 96:98119.
Batra, S.W.T. 1994b. Diversify with pollen bees. American Bee Journal 134:591593.
Batra, S.W.T. 1998. Hornfaced bees for apple pollination. American Bee Journal
138(5):361365.
Batra, S.W.T. 2003. Bee introductions to pollinate our crops. Pp. 8598 in For Nonnative Crops,
Whence Pollinators of the Future? K. Strickler and J.H. Cane, eds. Proceedings, Entomological Society of America. Lanham, Md.: Thomas Say Publications in Entomology.
Bawa, K.S. 1974. Breeding systems of tree species of a lowland tropical community. Evolution
28:8592.
Bawa, K.S. 1990. Plant-pollinator interactions in tropical rain forests. Annual Review of Ecology and Systematics 21:399422.
Baxter, J., F. Eischen, J. Pettis, W.T. Wilson, and H. Shimanuki. 1998. Detection of fluvalinateresistant varroa mites in U.S. honey bees. American Bee Journal 138:291.
Baxter, J.R., M.D. Ellis, and W.T. Wilson. 2000. Field evaluation of ApistanReg and five
candidate compounds for parasitic mite control in honey bees. American Bee Journal
140(11):898900.
Beattie, A.J. 1985. The Evolutionary Ecology of Ant-Plant Mutualisms. New York: Cambridge
University Press.
Bednarek, A.T., and D.D. Hart. 2005. Modifying dam operations to restore rivers: ecological
responses to Tennessee river dam mitigation. Ecological Applications 15:9971008.
Beetsma, J. 1994. The varroa mite, a devastating parasite of western honeybees and an economic threat to beekeeping. Outlook on Agriculture 23:69175.
Belzunces, L.P., C. Pelissier, and G.B. Lewis, eds. 2001. Hazards of Pesticides to Bees. Paris:
INRA Editions.
Benting, J., I. Hauser-Hahn, R. Nauen, and R. Beffa. 2004. Molecular diagnosis of resistance.
Pflanzenschutz-Nachrichten-Bayer 57(1):7886.
Berenbaum, M.R. 2001. Interpreting the scientific literature: differences in the scientific and
lay communities. Plant Physiology 125:509512.
Berger, J. 1990. Persistence of different-sized populations: an empirical assessment of rapid
extinctions. Conservation Biology 4:9198.
Bergstrm, G., P. Bergman, M. Appelgren, and J.O. Schmidt. 1996. Labial gland chemistry of
three species of bumblebees (Hymenoptera: Apidae) from North America. Biorganic and
Molecular Chemistry 4:515519.
Bernays, E.A., and M. Graham. 1988. On the evolution of host specificity in phytophagous
arthropods. Ecology 69:886892.
Bernhardt, P. 1984. Mistletoes on mistletoes: the floral ecology of Amyema miraculosum and
its host, Amyema miquelii (Loranthaceae). Australian Journal of Botany 28:437451.
Bernhardt, P. 1999. The Roses Kiss; A Natural History of Flowers. Washington: Island Press/
Shearwater Books.
Bernhardt, P. 2000. Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. Plant Systematics and Evolution 222:293320.
Bernhardt, P. and R. Edens. 2004. A fertility clinic for flora. Plant Talk 30:2528.

REFERENCES
219
Bernhardt, P., and L.B Thien. 1987. Self-isolation and insect pollination in the primitive
angiosperms: new evaluations of older hypotheses. Plant Systematics and Evolution
156:159176.
Bertin, R.I. 1982. The ruby-throated hummingbird and its major food plants: ranges, flowering
phenology, and migration. Canadian Journal of Zoology 60:210219.
Beye, M., M. Hasselmann, K. Fondrk, R.E. Page, Jr., and S.W. Omholt. 2003. The gene csd is
the primary signal for sexual development in the honey bee and encodes a new SR-type
protein. Cell 114:419429.
Bhattacharjee, Y. 2005. OrnithologyCitizen scientists supplement work of Cornell researchersA half-century of interaction with bird watchers has evolved into a robust
and growing collaboration between volunteers and a leading ornithology lab. Science
308:14021403.
Biesmeijer J.C., S.P. Roberts, M. Reemer, R. Ohlemueller, M. Edwards, T. Peeters, A. Schaffers,
S.G. Potts, R. Kleukers, C.D. Thomas, J. Settele, and W.E. Kunin. 2006. Parallel declines
in pollinators and insect-pollinated plants in northwest Europe. Britain and the Netherlands. Science 313(5785):351354.
Bigger, D.S. 1999. Consequences of patch size and isolation for a rare plant: pollen limitation
and seed predation. Natural Areas Journal 19:239244.
Blackburn, H.D. 2002. Management of U.S. genetic resources. Proceedings of the 7th World
Congress on Genetics Applied to Livestock Production, Montpellier, France, August,
2002 Session 26, pp. 14. Montpellier: Institut National de la Recherche Agronomique
(INRA).
Bloch, D., N. Werdenberg, and A. Erhardt. 2006. Pollination crisis in the butterfly pollinated,
wild carnation Dianthus carthusianorum? New Phytologist 169:699706.
Boecking, O., K. Bienefeld, and W. Drescher. 2000. Heritability of the varroa-specific hygienic behaviour in honey bees (Hymenoptera: Apidae). Journal of Animal Breeding and
Genetics 117(6):417424.
Boggs, C.L., J.T. Smiley, and L.E. Gilbert. 1981. Patterns of pollen exploitation by Heliconius
butterflies. Oecologia 48:284289.
Bogler, D.J., J.L. Neff, and B.B. Simpson. 1995. Multiple origins of the yucca-yucca moth association. Proceedings of the National Academy of Sciences USA 92:68646867.
Bohart, G.E. 1958. Transfer and establishment of the alkali bee. In 10th Alfalfa Improvement
Conference, Ithaca, NY, July 2830, 4 pp.
Bohart, G.E. 1962. How to manage the leaf-cutting bee for alfalfa pollination. Utah Agriculture
Experimentation Station Circular 144, 7 pp.
Bohart, G.E. 1967. Management of wild bees. Pp. 109118 in Beekeeping in the United States,
Agriculture Handbook. 335. Washington: U.S. Department of Agriculture.
Bohart, G.E. 1970. Commercial production and management of wild bees-A new entomological industry. Bulletin of the Entomological Society of America 16(1):89.
Bohart, G.E. 1972a. Management of wild bees for the pollination of crops. Annual Review of
Entomology 17:287312.
Bohart, G.E. 1972b. Management of habitats for wild bees. Pp. 253266 in Proceedings Tall
Timbers Conference on Ecological Animal Control by Habitat Management No. 3.
Bohart, G.E., and M.W. Pedersen. 1963. The alfalfa leaf-cutting bee, Megachile rotundata (F.),
for pollination of alfalfa [lucerne] in cages. Crop-Science 3(2):183184.
Bond, W.J. 1994. Do mutualisms matter? Assessing the impact of pollinator and disperser
disruption on plant extinction. Philosophical Transactions of the Royal Society of London
Series BBiological Sciences 344:8390.
Bond, W.J. 1995. Assessing the risk of plant extinction due to pollinator and disperser failure.
Pp. 131140 in Extinction Rates, J.G. Lawton and R.M. May, eds. Oxford University
Press.

220
Borror, D., C.A. Triplehorn, and N.G. Johnson. 1989. An Introduction to the Study of Insects.
Philadelphia: Saunders College Publishing.
Bosch, J., and W.P. Kemp. 1999. Exceptional cherry production in an orchard pollinated with
blue orchard bees. Bee World 80(4):163173.
Bosch, J., and W.P. Kemp. 2000. Development and emergence of the orchard pollinator Osmia
lignaria (Hymenoptera: Megachilidae). Environmental Entomology 29:813.
Bosch, J., and W.P. Kemp. 2001. How to Manage the Blue Orchard Bee as an Orchard Pollinator. Sustainable Agriculture Network Handbook Series Book 5, National Agricultural
Library, Beltsville, Md. 88 pp.
Bosch, J., and W.P. Kemp. 2002. Developing and establishing bee species as crop pollinators:
the example of Osmia spp. (Hymenoptera: Megachilidae) and fruit trees. Bulletin of
Entomological Research 92(1):316.
Bosch, J., W.P. Kemp, and S.S. Peterson. 2000. Management of Osmia lignaria (Hymenoptera:
Megachilidae) populations for almond pollination: methods to advance bee emergence.
Environmental Entomology 29(5):874883.
Boucher, D.H., ed. 1985. The Biology of Mutualism: Ecology and Evolution. New York:
Oxford University Press.
Bowlin, W.R., V.J. Tepedino, and T.L. Griswold. 1993. The reproductive biology of Eriogonum
pelinophilum (Polygonaceae). Pp. 296300 in Proceedings of the Southwestem Rare
and Endangered Plant Conference, R. Sivinski and K. Lighffoot, eds. New Mexico State
Forestry and Resources Conservation Division, Miscellaneous Publication #2.
Brantjes, N.B.M. 1981. Ant, bee and fly pollination in Epipactis palustris (L.) Crantz (Orchidaceae). Acta Botanica Neerlandica 30:5968.
Brittain, W.H. 1933. Apple pollination studies in the Annapolis Valley, N.S., Canada 1928
1932. Canada Department of Agriculture Bulletin 162. 198 pp.
Brody, A.K., and R.J. Mitchell. 1997. Effects of experimental manipulation of inflorescence
size on pollination and pre-dispersal seed predation in the hummingbird-pollinated plant
Ipomopsis aggregata. Oecologia 110:8693.
Bromenshenk, J.J., G.C. Smith, and V.J. Watson. 1995. Assessing ecological risks in terrestrial
systems with honey bees. Pp. 930 in Biomonitors and Biomarkers as Indicators of Environmental Change, F.M. Butterworth, ed. New York: Plenum Press.
Bromenshenk J.J., C.B. Henderson, R.A. Seccomb, S.D. Rice, R.T. Etter, S.F.A. Bender, P.J.
Rodacy, J.A. Shaw, N.L. Seldomridge, L.H. Spangler, and J.J. Wilson. 2003. Can honey
bees assist in area reduction and landmine detection? Journal of Mine Action (Research,
Development and Technology in Mine Action), Issue 7.3.
Bronstein, J.L. 1988. Mutualism, antagonism and the fig-pollinator interaction. Ecology
69:12981302.
Bronstein, J.L. 1994a. Our current understanding of mutualism. Quarterly Review of Biology
69:3151.
Bronstein, J.L. 1994b. Conditional outcomes in mutualistic interactions. Trends in Ecology
and Evolution 9:214217.
Bronstein, J.L. 1995. The plant-pollinator landscape. Pp. 256288 in Mosaic Landscape and
Ecological Processes, L. Hansson, L. Fahrig, and G. Merriam, eds. London: Chapman
and Hall.
Bronstein, J.L., and D. McKey. 1989. The fig/pollinator mutualism: a model system for comparative biology. Experientia 45:601604.
Brown, D.G., K.M. Johnson, T.R. Loveland, and D.M. Theobald. 2005. Rural land-use trends
in the conterminous United States, 19502000. Ecological Applications 15:18511863.
Brown, K.S., and A.V.L. Freitas. 2000. Atlantic forest butterflies: indicators for landscape
conservation. Biotropica 32(4B SI):934956.
Brown, M.J.F., R. Loosli, and P. Schmid-Hempel. 2003. Condition-dependent expression of
virulence in a trypanosome infecting bumblebees. Oikos 91:421427.

REFERENCES
221
Bruneau, A. 1997. Evolution and homology of bird pollination syndromes in Erythrina

(Leguminosae). American Journal of Botany 84:5471.
Brys, R., H. Jacquemyn, P. Endels, F. Van Rossum, M. Hermy, L. Triest, L. De Bruyn, and
G.D.E. Blust. 2004. Reduced reproductive success in small populations of the selfincompatible Primula vulgaris. Journal of Ecology 92:514.
Bubalo, D., H. Pechhacker, E. Licek, N. Kezic, and D. Sulimanovic. 2005. The effect of Varroa
destructor infestation on flight activity and mating efficiency of drones (Apis mellifera L.).
Wiener Tierarztliche Monatsschrift 92:1115.
Buchmann, S.L. 1983. Buzz pollination in angiosperms. Pp. 73114 in Handbook of Experimental Pollination Biology, C.E. Jones and R.J. Little, eds. New York: Scientific and
Academic Editions.
Buchmann, S.L. 1987. The ecology of oil flowers and their bees. Annual Review of Ecology
and Systematics 18:343369.
Buchmann, S.L. 1996. Competition between honey bees and native bees in the Sonoran
Desert and global bee conservation issues. Pp. 125142 in The Conservation of Bees, A.
Matheson, S.L. Buchmann, C. OToole, P. Westrich, and I.H. Williams, eds. New York:
Academic Press.
Buchmann, S.L., and J.S. Ascher. 2005. The plight of pollinating bees. Bee World 86:7174.
Buchmann, S.L., and G.P. Nabham. 1996. The Forgotten Pollinators. Washington: Island
Press.
Bugg, R.L., Anderson, J. H., Thomsen, C. D., and J. Chandler. 1998. Pp. 339374 in Enhancing Biological Control: Habitat Management to Promote Natural Enemies of Agricultural
Pests, R.L. Bugg, ed. Berkeley: University of California Press.
Bull, J.J. 1983. Evolution of Sex Determining Mechanisms. Menlo Park: Benjamin Cummings
Publishing Company.
Burd, M. 1994. Batemans principle and plant reproduction: the role of pollen limitation in
fruit and seed set. Botanical Review 60:83139.
Burgett, M. 1994. Pacific Northwest winter loss1993/94. National Honey Market News
9:1314. U.S. Department of Agriculture, Agricultural Marketing Service.
Burgett, M. 2004. Pacific Northwest Honey Bee Pollination Survey2003. National Honey
Report XXIII1 (February 12, 2004):1215. U.S. Department of Agriculture, Agricultural Marketing Service. Available at: http://marketnews.usda.gov/portal/usda/templates/
honey/honey2004/20040213hny.pdf. Accessed December 28, 2005.
Burgett, M. 2005. Pacific Northwest Honey Bee Pollination Survey2004. National Honey
Report XXIV1 (February 10, 2005):912. U.S. Department of Agriculture, Agricultural Marketing Service. Available at: http://marketnews.usda.gov/portal/usda/templates/
honey/honey2005/20050210hny.pdf. Accessed December 15, 2005.
Burgett, M., R.R. Rucker, and W.N. Thurman. 2004. Economics and honeybee pollination
markets. American Bee Journal April 269271.
Brquez, A. 2003. Flora and vegetation of the Gran Desierto and Rio Colorado of Northwestern Mexico. Plant Systematics and Evolution 231:117123.
Brquez, A., and A. Martnez-Yrzar. 1997. Conservation and Landscape Transformation in
Sonora, Mxico. Journal of the Southwest 39(34):371398.
Butaye, J., D. Adriaens, and O. Honnay. 2005. Conservation and restoration of calcareous
grasslands: a concise review of the effects of fragmentation and management on plant
species. Biotechnology, Agronomy, Society and Environment 9(2):111118.
Butler, G.D., and M.J. Wargo. 1963. Biological notes on Megachile concinna Smith in Arizona.
Pan-Pacific Entomologist 39:201206.
Butz-Huryn, V.M.B. 1997. Ecological impacts of introduced honeybees. Quarterly Review of
Biology 72:275297.
Caldas, A., and R.K. Robbins. 2003. Modified Pollard transects for assessing tropical butterfly
abundance and diversity. Biological Conservation 110:211219.

222
Calder, W.A. 1987. Southbound through ColoradoMigration of rufous hummingbirds.

National Geographic Research 3:4051.
Calder, W.A. 2004. Rufous and broad-tailed hummingbirdsPollination, migration, and population biology. Pp. 5979 in Conserving Migratory Pollinators and Nectar Corridors in
Western North America, G.P. Nabhan, ed. Tucson: University of Arizona Press.
Calder, W.A., and L.L. Calder. 1992. Broad-tailed hummingbird (Selasphorus platycerus). The
Birds of North America, No. 16, A. Poole and F. Gill, eds. Philadelphia: The Academy of
Natural Sciences; Washington: The American Ornithologists Union.
Calder, W.A., S.M. Hiebert, N.M. Waser, D.W. Inouye, and S.J. Miller. 1983. Site fidelity,
longevity, and population dynamics of broad-tailed hummingbirds: a ten year study.
Oecologia 56:689700.
Calderone, N.W. 2000. Effective fall treatment of Varroa jacobsoni (Acari: Varroidae) with a
new formulation of formic acid in colonies of Apis mellifera (Hymenoptera: Apidae) in
the northeastern United States. Journal of Economic Entomology 93:10651075.
Calderone, N.W. 2005. Evaluation of drone brood removal for the management of Varroa
destructor (Acari: Varroidae) in colonies of the honey bee Apis mellifera L. (Hymenoptera:
Apidae) in the northeastern USA. Journal of Economic Entomology 98:645650.
Calderone, N.W., and M. Nasr. 1999. Evaluation of a formic acid formulation for the fall
control of Varroa jacobsoni (Acari: Varroidae) in colonies of the honey bee Apis mellifera (Hymenoptera: Apidae) in a temperate climate. Journal of Economic Entomology
92:526533.
Calderone, N.W., and H. Shimanuki. 1995. Evaluation of four seed-derived oils as controls
for Acarapis woodi (Acari: Tarsonemidae) in colonies of Apis mellifera (Hymenoptera:
Apidae). Journal of Economic Entomology 88:805809.
Calderone, N.W., and M. Spivak. 1995. Plant extracts for control of the parasitic mite Varroa
jacobsoni (Acari: Varroidae) in colonies of the western honey bee (Hymenoptera: Apidae).
Journal of Economic Entomology 88:12111215.
Calderone, N.W., W.T. Wilson, and M. Spivak. 1997. Plant extracts used for control of the
parasitic mites Varroa jacobsoni (Acari: Varroidae) and Acarapis woodi (Acari: Tarsonemidae) in colonies of Apis mellifera (Hymenoptera: Apidae). Journal of Economic
Camazine, S. 1986. Differential reproduction of the mite, Varroa jacobsoni (Mesostigmata:
Varroidae), on Africanized and European honey bees (Hymenoptera: Apidae). Annals of
the Entomological Society of America 79(5):801803.
Camazine, S., and R.A. Morse. 1988. The Africanized honeybee. American Scientist
76(5):464471.
Camerarius, R.J. 1694. Epistola ad M.B. Valentini de sexu plantarum [Letter on the Sexuality of Plants]. In Ostwalds Klassiker der exakten Naturwissenschaften, No. 105, 1899.
Leipzig: Verlag von Wilhelm Engelmann.
Cameron, S.A. 2004. Phylogeny and biology of Neotropical orchid bees (Euglossini). Annual
Review of Entomology 49:377404.
Campanhola, C., G. Rodrigues, and B. Dias. 1998. Agricultural biological diversity. Ciencia e
Cultura, Sao Paulo 50(1):1012.
Campbell, B., J. Heraty, J.Y. Rasplus, K. Chan, J. Steffan-Campbell, and C. Babcock. 2000.
Molecular systematics of the Chalcidoidea using 28S-rDNA. Pp. 5973 in The Hymenoptera: Evolution, Biodiversity and Biological Control, A.D. Austin and M. Dowton,
eds. Canberra: CSIRO Publishing.
Campbell, D.R., and K.J. Halama. 1993. Resource and pollen limitations to lifetime seed
production in a natural plant population. Ecology 74:10431051.
Campbell, D.R., and A.F. Motten. 1985. The mechanism of competition for pollination between 2 forest herbs. Ecology 66(2):554563.

REFERENCES
223
Campbell, N.A., J.B. Reece, and L.G. Mitchell. 1999. Biology (5th ed.). California: Benjamin
Cummings Publishing Company, Inc.
Cane, J.H. 1991. Soils of ground-nesting bees (Hymenoptera: Apoideae): texture, moisture, cell
depth and climate. Journal of the Kansas Entomological Society 64(4):406413.
Cane, J.H. 2002. Pollinating bees (Hymenoptera: Apiformes) of U.S. alfalfa compared for rates
of pod and seed set. Journal of Economic Entomology 95(1):2227.
Cane, J.H. 2003. Exotic non-social (Hymenoptera: Apoides) bees in North America. Pp.
113126 in For Nonnative Crops, Whence Pollinators of the Future?, K. Strickler and
J.H. Cane, eds. Proceedings, Entomological Society of America. Lanham, Md.: Thomas
Say Publications in Entomology.
Cane, J.H. 2005. Pollination potential of the bee Osmia aglaia for cultivated red raspberries
and blackberries (Rubus: Rosaceae). HortScience 40(6):17051708.
Cane J.H., and J.A. Payne. 1988. Foraging ecology of the bee Habropoda laboriosa (Hymenoptera: Anthophoridae), an oligolege of blueberries (Ericaceae: Vaccinium) in the Southeastern United States. Annals of the Entomological Society of America 81:419427.
Cane, J.H., and J.A. Payne. 1990. Native bee pollinates rabbiteye blueberry. Alabama Agricultural Experiment Statistics 37:4.
Cane, J.H., R.L. Minckley, and L.J. Kervin. 2000. Sampling bees (Hymenoptera: Apiformes)
for pollinator community studies: pitfalls of pan-trapping. Journal of the Kansas Entomological Society 73:225231.
Cane, J.H., R.L. Minckley, L.J. Kervin, T.H. Roulston, and N.M. Williams. 2006. Complex
responses within a desert bee guild (Hymenoptera:Apiformes) to urban habitat fragmentation. Ecological Applications 16:632644.
Caron, D.M., and J. Hubner. 2001. 2001 winter loss survey. American Bee Journal
141:778779.
Carroll, L.E., I.M. White, A. Freidberg, A.L. Norrbom, M.J. Dallwitz, and F.C. Thompson.
2005. Pest Fruit Flies of the World. Available at: http://delta-intkey.com/ffa/www/_wintro.
htm.
Carthew, S.M., and R.L. Goldingay. 1997. Non-flying mammals as pollinators. Trends in
Ecology and Evolution 12:104108.
Carvell, C., W.R. Meek, R.F. Pywell, and M. Nowakowski. 2004. The response of foraging
bumblebees to successional change in newly created arable field margins. Biological
Conservation 118:327339.
Caspersen, J.P., S.W. Pacala, J.C. Jenkins, G.C. Hurtt, P.R. Moorcroft, and R.A. Birdsey.
2000. Contributions of land-use history to carbon accumulation in U.S. forests. Science
290:11481151.
CBD (Convention on Biological Diversity). 2005. Agricultural Biodiversity: International Initiative for the Conservation and Sustainable Use of Pollinators. Available at: http://www.
biodiv.org/programmes/areas/agro/pollinators.asp. Accessed July 24, 2006.
Ceballos, G., and G. Oliva. 2005. Los Mamferos Silvestres de Mxico. Ed. Fondo de Cultura
Econmica and Conabio. Mexico D.F., 1986 pp.
Ceballos, G., T.H. Fleming, C. Chavez, and J. Nassar. 1997. Population dynamics of Leptonycteris curasoae (Chiroptera: Phyllostomidae) in Jalisco, Mexico. Journal of Mammalogy
78:12201230.
Chacoff, N., and M. Aizen. 2006. Edge effects on flower-visiting insects in grapefruit plantations
bordering premontane subtropical forest. Journal of Applied Ecology 43(1):1827.
Charlesworth, D., and B. Charlesworth. 1987. Inbreeding depression and its evolutionary
consequences. Annual Review of Ecology and Systematics 18:237268.
Chen, Y.P., J.A. Higgins, and M.F. Feldlaufer. 2005. Quantitative real-time reverse transcriptionCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.). Applied
and Environmental Microbiology 71:436441.

224
Clark, K.J. 1990. Field trials comparing vegetable oil and menthol as a control for tracheal
mites. American Bee Journal 130:799800.
Clark-Tapia, R., and F. Molina-Freaner. 2004. Reproductive ecology of the rare clonal cactus
Stenocereus eruca in the Sonoran desert. Plant Systematics and Evolution 247:155164.
Clay, J. 2004. World Agriculture and the Environment. Washington: Island Press.
Clinebell II, R.R., A. Crowe, D.P. Gregory, and P.C. Hoch. 2004. Pollination ecology of Gaura
and Calylophus (Onagraceae, tribe Onagreae) in western Texas, U.S.A. Annals of the
Missouri Botanical Garden 91:369400.
Cockrum, E.L., and Y. Petryszyn. 1991. The Long-Nosed Bat, Leptonycteris: An Endangered
Species in the Southwest? Occasional Paper OP-142. Lubbock, Tex.: Museum of Texas
Tech University, NSRL Publications.
Colla, S.R., M.C. Otterstatter, R.J. Gegear, and J.D. Thomson. 2006. Plight of the bumble
bee: pathogen spillover from commercial to wild populations. Biological Conservation
129:461467.
Collins, A.M. 2000. Survival of honey bee (Hymenoptera: Apidae) spermatozoa stored abovefreezing temperatures. Journal of Economic Entomology 93(3):568571.
Collins, A.M. 2004. Sources of variation in the viability of honey bee, Apis mellifera L., semen collected for artificial insemination. Invertebrate Reproduction and Development
45(3):231237.
Collins, A.M., and J.S. Pettis. 2001. Effect of varroa infestation on semen quality. American
Bee Journal 141:590593.
Collins, S.A., G.E. Robinson, and J.K. Conner. 1997. Foraging behavior of honey bees
(Hymenoptera: Apidae) on Brassica nigra and B. rapa grown under simulated ambient and enhanced UV-B radiation. Annals of the Entomological Society of America
90(1):102106.
Colwell, R.K. 2005. EstimateS, Version 7.5: statistical estimation of species richness and shared
species from samples (Software and Users Guide). Freeware published at http://viceroy.
eeb.uconn.edu/estimates.
Colwell, R.K., C.X. Mao, and J. Chang. 2004. Interpolating, extrapolating, and comparing
incidence-based species accumulation curves. Ecology 85:27172727.
Comins, H.N. 1986. Tactics for resistance management using multiple pesticides. Agriculture
Ecosystems and Environment 16(2):129148.
Condon, M. 1995. Biodiversity, systematics, and Tom Sawyer science. Conservation Biology
9:711714.
Congressional Research Service. 2006. Reauthorization of the Endangered Species Act (ESA): A
Comparison of Pending Bills and a Proposed Amendment with Current Law. Washington:
Library of Congress.
Cook, J.M. 1993. Sex determination in the hymenoptera: a review of models and evidence.
Heredity 71:421435.
Costanza, R., R. dArge, R. de Groot, S. Farber, M. Grasso, B. Hannon, K. Limburg, S. Naeem,
R.V. ONeill, J. Paruelo, R.G. Raskin, P. Sutton, and M. van den Belt. 1997. The value of
the worlds ecosystem services and natural capital. Nature 387:253260.
Council of Economic Advisers. 2006. Economic report of the President, February 13, 2006.
Available at: http://www.whitehouse.gov/cea/erp06.pdf. Accessed March 6, 2006.
Cox, B., F. Eischen, and H. Graham. 2005. American foulbrood survey in honey bees pollinating California almonds. Part I of three partswidespread incidence of AFB spores.
American Bee Journal 145(4):302304.
Cox, P.A. 1983. Extinction of the Hawaiian avifauna resulted in a change of pollinators for
the ieie, Freycinetia arborea. Oikos 41:195199.
Cox, P.A., and T. Elmqvist. 2000. Pollinator extinction in the Pacific Islands. Conservation
Biology 14:12371239.
Crane, E. 1983. The Archaeology of Beekeeping. London: Duckworth. 260 pp.

REFERENCES
225
Crane, E. 1990. Bees and Beekeeping. Ithaca, NY: Comstock Publishing Associates.
Crane, E. 1999. The World History of Beekeeping and Honey Hunting. London: Routledge.
Crespi, B.J., and D. Yanega. 1995. The definition of eusociality. Behavioral Ecology
6(1):109115.
Cresswell, J.E., and J.L. Osborne. 2004. The effect of patch size and separation on bumblebee foraging in oilseed rape: implications for gene flow. Journal of Applied Ecology
41:539546.
Crozier, L. 2003. Winter warming facilitates range expansion: cold tolerance of the butterfly
Atalopedes campetris. Oecologia 135:648656.
Cruden, R.W. 1973. Reproductive biology of weedy and cultivated Mirabilis (Nyctaginaceae).
American Journal of Botany 60:802809.
Cryan, P.M., and M.A. Bogan. 2003. Recurrence of the long-nosed bat (Choeronycteris mexicana) at historical sites in Arizona and New Mexico. Western North American Naturalist
63(3):314319.
Cunningham, S.A. 2000. Depressed pollination in habitat fragments causes low fruit set. Proceedings of the Royal Society of London Series BBiological Sciences 267:11491152.
DAntonio, C.M., and P.M. Vitousek. 1992. Biological invasions by exotic grasses, the grass/fire
cycle and global change. Annual Review of Ecology and Systematics 23:6387.
Daehler, C.S. 2003. Performance comparisons of co-occurring native and alien invasive plants:
implications for conservation and restoration. Annual Review of Ecology, Evolution, and
Systematics 34:183211.
Dafni, A., and A. Shmida. 1996. The possible ecological implications of the invasion of Bombus
terrestris (L.) (Apidae) at Mt. Carmel, Israel. Pp. 183200 in The Conservation of Bees,
A. Matheson, ed. London: Academic Press.
Dafni, A., P. Bernhardt, A. Shmida, Y. Ivir, S. Greenbaum, C. OToole, and L. Losito. 1990.
Red bowl-shaped flowers: convergence for beetle pollination in the Mediterranean region.
Israel Journal of Botany 39:8192.
Dafni, A., P.G. Kevan, and B. Husband, eds. 2005. Practical Pollination Biology. Cambridge,
Canada: Enviroquest Ltd.
Dag, A., and D. Eisikowitch. 2000. The effect of carbon dioxide enrichment on nectar production in melons under greenhouse conditions. Journal of Apicultural Research 39:8889.
Daily, G.C., P.A. Matson, and P.M. Vitousek. 1997. Ecosystem services supplied by soil.
Pp. 113132 in Natures Services: Societal Dependence on Natural Ecosystems, G. Daily,
ed. Washington: Island Press.
Dalton, R. 2005. Alcohol and science: saving the agave. Nature 438:10701071.
Daly, H.V. 1966. Biological studies on Ceratina dallatorreana, an alien bee in California which
reproduces by parthenogenesis (Hymenoptera: Apoidea). Annals of the Entomological
Society of America 59:11381154.
Daly, H.V., G.E. Bohart, and R.W. Thorp. 1971. Introduction of small carpenter bees into
California for pollination. I. Release of Pithitis smaragdula. Journal of Economic Entomology 64:11451150.
Danielsen, F., N.D. Burgess, and A. Balmford. 2005. Monitoring matters: examining the potential of locally-based approaches. Biodiversity and Conservation 14:25072542.
Danka, R.G., and T.E. Rinderer. 1986. Africanized bees and pollination. American Bee Journal
126:680682.
Danka, R.G., T.E. Rinderer, A.M. Collins, and R.L. Hellmich II. 1987. Responses of Africanized honey bees (Hymenoptera: Apidae) to pollination-management stress. Journal of
Economic Entomology 80(3):621624.
Danka, R.G., J.D. Villa, and N.E. Gary. 1993. Comparative foraging distances of Africanized,
European and hybrid honey bees (Apis mellifera L.) during pollination of cantaloupe
(Cucumis melo L.). Bee Science 3(1):1621.

226
Dauber, J., M. Hirsch, D. Simmering, R. Waldhardt, A. Otte, and V. Wolters. 2003. Landscape
structure as an indicator of biodiversity: matrix effects on species richness. Agriculture
Ecosystems and Environment 98:321329.
Davenport, T.R.B., W.T. Stanley, E.J. Sargis, D.W. De Luca, N.E. Mpunga, S.J. Machaga, and
L.E. Olson. 2006. A new genus of African monkey, Rungwecebus: morphology, ecology
and molecular phylogenetics. Science 312:13781381.
Davies, T.J., T.G. Barraclough, M.W. Chase, P.S. Soltis, D.E. Soltis, and V. Savolainen. 2004.
Darwins abominable mystery: insights from a supertree of the angiosperms. Proceedings
of the National Academy of Sciences, USA 101(7):19041909.
Davis, A.R. 2003. Influence of elevated CO2 and ultraviolet-B radiation levels on floral nectar production: a nectary-morphological perspective. Plant Systematics and Evolution
238:169181.
Day, L. Forthcoming (in prep). Field Guide to Bumblebees of Illinois and the Eastern United
States.
de Ruijter, A. 1997. Commercial bumblebee rearing and its implications. Pp. 261269 in
Proceedings of the 7th International Symposium on Pollination, K.W. Richards, ed. ISHS
Acta Horticulturae 437. Belgium: ISHS.
de Ruijter, A. 2002. Pollinator diversity and sustainable agriculture in the Netherlands.
Pp. 6770 in Pollinating BeesThe Conservation Link Between Agriculture and Nature,
P. Kevan and V.L. Imperatriz Fonseca, eds. Brasilia: Ministry of Environment.
Dedej, S., K.S. Delaplane, and H. Scherm. 2004. Effectiveness of honey bees in delivering the
biocontrol agent Bacillus sutilis to blueberry flowers to suppress mummy berry disease.
Biological Control 31:422427.
Degenhardt, S., and S. Gronemann. 1988. Die Zahlungsbereitschaft von Urlaubsgsten fr
denNaturschutz: Theorie und Empirie des Embeddings-Effektes. Frankfurt: Lang.
353+21 pp.
DeGrandi-Hoffman, G., and J.C. Watkins. 2000. The foraging activity of honey bees Apis
mellifera and non-Apis bees on hybrid sunflowers (Helianthus annuus) and its influence
on cross-pollination and seed set. Journal of Apicultural Research 39(12):3745.
DeJong, D. 1990. Mites: varroa and other parasites of brood. Pp. 200218 in Honey Bee
Pests, Predators, and Diseases, R.A. Morse and R. Nowogrodzki, eds. 2nd edition. Ithaca:
Cornell University Press.
DeJong, D. 1996. Africanized honey bees in Brazil, forty years of adaptation and success. Bee
World 77(2):6770.
DeJong, D., and P.H. DeJong. 1983. Longevity of Africanized honey bees (Hymenoptera:
Apidae) infested by Varroa jacobsoni (Parasitiformes: Varroidae). Journal of Economic
DeJong, D., P.H. DeJong, and L.S. Goncalves. 1982a. Weight loss and other damage to developing worker honey bees from infestation with Varroa jacobsoni. Journal of Apicultural
Research 21:165167.
DeJong, D., R.A. Morse, and G.C. Eickwort. 1982b. Mite pests of honeybees Apis spp.,
Varroa jacobsoni, Acarapis woodi, Tropilaelaps clareae. Annual Review of Entomology
27:229252.
DeJong, D., L.S. Goncalves, and R.A. Morse. 1984. Dependence on climate of the virulence
of Varroa jacobsoni. Bee World 65:117121.
Delaplane, K.S. 1992. Controlling tracheal mites (Acari: Tarsonemidae) in colonies of honey
bees (Hymenoptera: Apidae) with vegetable oil and menthol. Journal of Economic Entomology 85:21182124.
Delaplane, K.S., and D.F. Mayer. 2000. Crop Pollination by Bees. Oxon: CAB International.
Delfinado-Baker, M. 1984. Acarapis woodi in the United States. American Bee Journal
124:805806.

REFERENCES
227
Delfinado-Baker, M. 1988. The tracheal mite of honey bees: a crisis in beekeeping. Pp. 493497
in Africanized Honey Bees and Bee Mites, G.R. Needham, R.E. Page, Jr., M. DelfinadoBaker, and C.E. Bowman, eds. Chichester: Halsted Press.
Delpino, F. 18681875. Ulteriori osservazione sulla dicogamia nel regno vegetale. Atti della
Societa Italiana di Scienze Naturali Milano, Vols. 1 and 2.
Demauro, M.M. 1993. Relationship of breeding system to rarity in the lakeside daisy (Hymenoxys acaulis var. glabra). Conservation Biology 7:542550.
Dhondt, A.A., S. Altizer, E.G. Cooch, A.K. Davis, A. Dobson, M.J.L. Driscoll, B.K. Hartup,
D.M. Hawley, W.M. Hochachka, P.R. Hosseini, C.S. Jennelle, G.V. Kollias, D.H. Ley,
E.C.H. Swarthout, and K.V. Sydenstricker. 2005. Dynamics of a novel pathogen in an
avian host: mycoplasmal conjunctivitis in house finches. Acta Tropica 94:7793.
Dias, B.S.F., A. Raw, and V.L. Imperatri-Fonesca. 1999. International Pollinators: Initiative:
The So Paulo Declaration on Pollinators. Report on the Recommendations of the Workshop on Conservation and Sustainable Use of Pollinators in Agriculture with Emphasis
on Bees. Available at: http://www.rge.fmrp.usp.br/beescience/arquivospdf/workshop.pdf.
Dick, C.W. 2001. Genetic rescue of remnant tropical trees by an alien pollinator. Philosophical Transactions of the Royal Society of London Series BBiological Sciences
268:23912396.
Dietz, A., and C. Vergara. 1995. Africanized honey bees in temperate zones. Bee World
76(2):5671.
Dilley, J.D. 2000. The radiation of Calochortus: generalist flowers moving through a mosaic
of potential pollinators. Oikos 89:209222.
Dixon, D.P., and B.G. Fingler. 1982. The effects of the 1981 Manitoba emergency mosquito
control program on honey bees. Pp. 243247 in Western Equine Encephilitis in Manitoba.
Winnipeg: Government of Manitoba.
Dixon, D.P., and B.G. Fingler. 1984. The effects of the mosquito control program on bees.
Pp. 101121 in Final Technical Report on Environmental Monitoring Program for
the 1983 Spraying of Malathion to Combat Western Equine Encephalitis. Winnipeg:
Government of Manitoba.
Dobson, A., D. David Lodge, J. Alder, G.S. Cumming, J. Keymer, J. McGlade, H. Mooney, J.A.
Rusak, O. Sala, V. Wolters, D. Wall, R. Winfree, and M.A. Xenopoulos. 2006. Habitat
loss, trophic collapse, and the decline of ecosystem services. Ecology 87(8):19151924.
Dodson, C.H., R.L. Dressler, H.G. Hills, R.M. Adams, and N.H. Williams. 1969. Biologically
active compounds in orchid fragrances. Science 164:12431249.
Dodson, M., J. Bachmann, and P. Williams. 2002. Organic Greenhouse Tomato Production.
ATTRA Publication #IP190/197. Available at: http://www.attra.org/attra-pub/ghtomato.
html.
Dogterom, M.H., and M.L. Winston. 1999. Pollen storage and foraging by honey bees (Hymenoptera: Apidae) in highbush blueberries (Ericaceae), cultivar Bluecrop. Canadian
Donaldson, J.S. 2002. Pollination in agricultural landscapes, a South African perspective.
Pp. 97104 in Pollinating BeesThe Conservation Link Between Agriculture and Nature,
P. Kevan and V.L. Imperatriz Fonseca, eds. Brasilia: Ministry of Environment.
Donzella, G., A. Spena, and G.L. Rotino. 2000. Transgenic parthenocarpic eggplants: superior
germplasm for increased winter production. Molecular Breeding 6(1):7986.
Dover, J.W. 1991. The conservation of insects on arable farmland. Pp. 294318 in The Conservation of Insects and Their Habitats, N.M. Collins and J.A. Thomas, eds. Symposium
of the Royal Entomological Society of London, 15. London: Academic Press.
Duay, P., D. De Jong, and W. Engels. 2002. Decreased flight performance and sperm production
in drones of the honey bee (Apis mellifera) slightly infested by Varroa destructor mites
during pupal development. Genetics and Molecular Research 1:227232.

228
Dudash, M.R. 1990. Relative fitness of selfed and outcrossed progeny in a self-compatible,
protandrous species, Sabatia angularis L. (Gentianaceae)a comparison in three environments. Evolution 44:11291139.
Duff, S.R., and B. Furgala. 1993. Evaluation of amitraz and menthol as agents to control
honey bee tracheal mite infestations in non-migratory honey bee colonies in Minnesota.
Dukas, R., and P.K. Visscher. 1994. Lifetime learning by foraging honey bees. Animal Behavior
48:10071012.
Duncan, D.H., A.B. Nicotra, J.T. Wood, and S.A. Cunningham. 2004. Plant isolation reduces outcross pollen receipt in a partially self-compatible herb. Journal of Ecology
92:977985.
Dupont, Y.L., D.M. Hansen, A. Valido, and J.M. Olesen. 2004. Impact of introduced honey
bees on native pollination interactions of the endemic Echium wildpretii (Boraginaceae)
on Tenerife, Canary Islands. Biological Conservation 118:301311.
Eardley, C., D. Roth, J. Clarke, S. Buchman, and B. Gemmill, eds. 2006. Pollinators and
Pollination: A Resource Book for Policy and Practice. Pretoria: African Pollinator Initiative. 77 pp.
Ehrenfeld, J.G., and L.A. Toth. 1997. Restoration ecology and the ecosystem perspective.
Restoration Ecology 5(4):307317.
Ehrlich, P.R., and I. Hanski, eds. 2004. On the Wings of Checkerspots: A Model System for
Population Biology. New York: Oxford University Press.
Ehrlich, P.R., D.S. Dobkin, and D. Wheye. 1988. The birders handbook. New York: Simon
and Schuster.
Eickwort, G.C. 1980. Two European species of Chelostoma established in New York State
(Hymenoptera: Megachilidae). Psyche 87:315323.
Eischen, F.A. 1987. Overwintering performance of honey bee colonies heavily infested with
Acarapis woodi (Rennie). Apidologie 18(4):293303.
Eischen, F.A., D. Cardoso-Tamez, W.T. Wilson, and A. Dietz. 1989. Honey production of honey
bee colonies infested with Acarapis woodi (Rennie). Apidologie 20(1):18.
Eischen, F.A., W.T. Wilson, J.S. Pettis, A. Suarez, D. Cardoso-Tamez, D.L. Maki, A. Dietz,
J. Vargas, C.G. Estrada, and W.L. de Rubink. 1990. TI: The spread of Acarapis woodi
(Acari: Tarsonemidae) in northeastern Mexico. Journal of the Kansas Entomological
Society 63(3):375384.
Ellis, J.D., Jr., K.S. Delaplane, and W.M. Hood. 2001. Efficacy of bottom screen devices,
Apistan, and Apilife VAR in controlling Varroa destructor. American Bee Journal
141:813816.
Ellis, J.D., Jr., I.H. Rong, M.P. Hill, H.R. Hepburn, and P.J. Elzen. 2004a. The susceptibility
of small hive beetle (Aethina tumida Murray) pupae to fungal pathogens. American Bee
Journal 144:486488.
Ellis, J.D., Jr., R. Hepburn, B. Luckman, and P.J. Elzen. 2004b. Effects of soil type, moisture,
and density on pupation success of Aethina tumida (Coleoptera: Nitidulidae). Environmental Entomology 33(4):794798.
Ellstrand, N.C., and E.R. Elam. 1993. Population genetic consequences of small population
size: implications for plant conservation. Annual Review of Ecology and Systematics
24:217242.
Elzen, P.J., and D. Westervelt. 2002. Detection of coumaphos resistance in Varroa destructor
in Florida. American Bee Journal 142:291292.
Elzen, P.J., F.A Eischen, J.B Baxter, J.S Pettis, G.W. Elzen, and W.T. Wilson. 1998. Fluvalinate
resistance in Varroa jacobsoni from several geographic locations. American Bee Journal
138:674676.
Elzen, P.J., J.R. Baxter, F.A. Eischen, and W.T. Wilson. 1999a. Pesticide resistance in Varroa
mites: theory and practice. American Bee Journal 139(3):195196.

REFERENCES
229
Elzen, P.J., J.R. Baxter, D. Westervelt, C. Randall, K.S. Delaplane, L. Cutts, and W.T. Wilson.
1999b. Field control and biology studies of a new pest species, Aethina tumida Murray
(Coleoptera, Nitidulidae), attacking European honey bees in the Western Hemisphere.
Apidologie 30(5):361366.
Elzen, P.J., F.A. Eischen, J.R. Baxter, G.W. Elzen, and W.T. Wilson. 1999c. Detection of resistance in US Varroa jacobsoni Oud. (Mesostigmata:Varroidae) to the acaricide fluvalinate.
Apidologie 30:1317.
Elzen, P.J., J.R. Baxter, M. Spivak, and W.T. Wilson. 1999d. Amitraz resistance in Varroa: new
discovery in North America. American Bee Journal 139(5):362.
Elzen, P.J., J.R. Baxter, M. Spivak, and W.T. Wilson. 2000. Control of Varroa jacobsoni Oud.
resistant to fluvalinate and amitraz using coumaphos. Apidologie 31(3):437441.
Elzen, P.J., J.R. Baxter, P. Neumann, A. Solbrig, C. Pirk, H.R. Hepburn, D. Westervelt, and C.
Randall. 2001. Behaviour of African and European subspecies of Apis mellifera toward
the small hive beetle, Aethina tumida. Journal of Apicultural Research 40(1):4041.
Elzen, P.J., D. Westervelt, D. Causey, R. Rivera, J. Baxter, and M. Feldlaufer. 2002. Control of
oxytetracycline-resistant American foulbrood with tylosin and its toxicity to honey bees
(Apis mellifera). Journal of Apicultural Research 41:97100.
Elzinga, C.L, D.W. Salzer, J.W. Willoughby, and J.P. Gibbs. 2001. Monitoring Plant and Animal
Populations. Malden, Mass.: Blackwell Science Inc.
Endress, P.K. 1994. Diversity and Evolutionary Biology of Tropical Flowers. Cambridge:
Cambridge University Press. 511 pp.
Engels, W., and K. Schatton. 1986. Changes in hemolymph proteins and weight loss in worker
bees due to varroa parasitization. Arbeitsgemeinschaft der Institute fur Bienenforschung
E.V. Abstracts of the Varroa Workshop in Feldafing/Starnberg, West Germany.
Engels, W., U. Schultz, and M. Radle. 1994. Use of the Tubingen mix for bee pasture in
Germany. Pp. 5765 in Forage for Bees in an Agricultural Landscape, A. Matheson, ed.
Cardiff: International Bee Research Association.
Erickson, J.L., and S.D. West. 2003. Associations of bats with local structure and landscape
features of forested stands in western Oregon and Washington. Biological Conservation
109:95102.
Erwin, T.L. 1982. Tropical forests: their richness in Coleoptera and other arthropod species.
The Coleopterists Bulletin 36:7475
Erwin T.L. 2004. The biodiversity question: How many species of terrestrial arthropods are
there? Pp. 259-269 in Forest Canopies, 2nd edition, M.D.L. Lowman, and H.B. Rinker,
eds. Burlington, Vt.: Elsevier Academic Press.
Estrada, C., and C.D. Jiggins. 2002. Patterns of pollen feeding and habitat preference among
Heliconius species. Ecological Entomology 27:448456.
Etcheverry, A.V., and C.E.T. Aleman. 2005. Reproductive biology of Erythrina falcata (Fabaceae: Papilionoideae). Biotropica 37:5463.
Evans, J.D. 2003. Diverse origins of tetracycline resistance in the honey bee bacterial pathogen
Paenibacillus larvae. Journal of Invertebrate Pathology 83:4650.
Evelyn, M.J., D.A. Stiles, and R.A. Young. 2004. Conservation of bats in suburban landscapes:
roost selection by Myotis yumanensis in a residential area in California. Biological Conservation Newsletter 115(3):463473.
Faegri, K., and L. van der Pijl. 1966. The Principles of Pollination Biology. New York: Pergamon Press.
Faegri, K., and L. van der Pijl. 1979. The Principles of Pollination Ecology. 3rd edition. Oxford:
Pergamon Press.
FAO (Food and Agriculture Organization of the United Nations). 2005. FAOSTAT Online.
Available at: http://apps.fao.org. Accessed January 2005.
Farrar, K. 1999. Crop Profile for Figs in California. Available at: http://pestdata.ncsu.edu/
cropprofiles/docs/cafigs.html. Accessed March 22, 2006.

230
Farrell, B.D., and C. Mitter. 1993. Phylogenetic determinants of insect/plant community diversity. Pp. 253266 in Species Diversity: Historical and Geographical Perspectives, R.E.
Ricklefs and D. Schluter, eds. Chicago: University of Chicago Press.
Feldlaufer, M.F., J.S. Pettis, J.P. Kochansky, and H. Shimanuki. 1997. A gel formulation
of formic acid for the control of parasitic mites of honey bees. American Bee Journal
137(9):661663.
Fenster, C.B., and M.R. Dudash. 2001. Spatiotemporal variation in the role of hummingbirds
as pollinators of Silene virginica. Ecology 82:844851.
Fenster, C.B., S. Armbruster, P. Wilson, M. Dudash, and J.D. Thomson. 2004. Pollination
syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics 35:375403.
Fenton, M.B. 1997. Science and the conservation of bats. Journal of Mammalogy 78:114.
Finley, J., S. Camazine, and M. Frazier. 1996. The epidemic of honey bee colony losses during
the 19951996 season. American Bee Journal 136:805808.
Fisher, R.M., and N. Pomeroy. 1989. Incipient colony manipulation, Nosema incidence and
colony productivity of the bumble bee Bombus terrestris (Hymenoptera, Apidae). Journal
of the Kansas Entomological Society 62:581589.
Flanders, K.L., and E.B. Radcliff. 2000. Alfalfa IPM. Available at: http://ipmworld.umn.edu/
chapters/flanders.htm. Accessed May 17, 2006.
Flanders, R.V., W.F. Wehling, and A.L. Craghead. 2003. Laws and regulations on the import,
movement, and release of bees in the United States. Pp. 99111 in For Nonnative Crops,
Whence Pollinators of the Future?, K. Strickler and J.H. Cane, eds. Proceedings, Entomological Society of America. Lanham, Md.: Thomas Say Publications in Entomology.
Fleishman, E., J.R. Thomson, R. MacNally, D.D. Murphy, and J.P. Fay. 2005. Using indicator
species to predict species richness of multiple taxonomic groups. Conservation Biology
19:11251137.
Fleming, T.H. 2000. Pollination of cacti in the Sonoran Desert. American Scientist
88:432439.
Fleming, T.H. 2004. Nectar corridors. Migration and the annual cycle of lesser long-nosed
bats. Pp. 2342 in Conservation of Migratory Pollinators and Their Nectar Corridors
in North America, G. Nabhan, R.C. Brusca, and L. Holter, eds. ArizonaSonora Desert
Museum, Natural History of the Sonoran Desert Region, No. 2. Tucson: University of
Arizona Press.
Fleming, T.H., and J.N. Holland. 1998. The evolution of obligate pollination mutualisms:
senita cactus and senita moth. Oecologia 114:368375.
Fleming, T.H., and J. Nassar. 2002. The population biology of a nectar-feeding bat, Leptonycteris curasoae, in Mexico and northern South America. Pp. 283305 in Columnar
Cacti and Their Mutualists: Evolution, Ecology, and Conservation, T.H. Fleming and A.
Valiente-Banuet, eds. Tucson: University of Arizona Press.
Fleming, T.H., R.A. Nunez, and L. Sternberg. 1993. Seasonal changes in the diets of migrant
and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis. Oecologia 94:7275.
Fleming, T.H., T. Tibbitts, Y. Petryszyn, and V. Dalton. 2001a. Current status of pollinating
bats in the southwestern United States. In Monitoring Bat Populations in the United
States, T. OShea and M. Bogan, eds. Fort Collins: U.S. Geological Survey.
Fleming, T.H., C.T. Sahley, J.N. Holland, J.D. Nason, and J.L. Hamrick. 2001b. Sonoran
Desert columnar cacti and the evolution of generalized pollination systems. Ecological
Monographs 71:511530.
Flores, J.M., J.A. Ruiz, J.M. Ruz, F. Puerta, M. Bustos, F. Padilla, and F. Campano. 1996.
Effect of temperature and humidity of sealed brood on chalkbrood development under
controlled conditions. Apidologie 27:185192.
Flottum, K. 2005. Inner cover. Bee Culture 133:10, 49.

REFERENCES
231
Fontaine, C., I. Dajoz, J. Meriguet, and M. Loreau. 2006. Functional diversity of plantpollinator interaction webs enhances the persistence of plant communities. PLoS Biology
4:129135.
Forister, M.L., and A.M. Shapiro. 2003. Climatic trends and advancing spring flight of butterflies in lowland California. Global Change Biology 9:11301135.
Forup, M.L., and J. Memmott. 2005. The restoration of plant-pollinator interactions in hay
meadows. Restoration Ecology 13:265274.
Forys, E., and C.R. Allen. 2005. The impacts of sprawl on biodiversity: the ant fauna of the
lower Florida Keys. Ecology and Society 10(1):25.
Frank, G., ed. 2003. Alfalfa Seed and Leafcutter Bee Production and Marketing Manual.
Brooks, Alberta: Irrigated Alfalfa Seed Producers Association. 160 pp.
Frankie, G.W., R.W. Thorp, L.E. Newstrom-Lloyd, M.A. Rizzardi, J.F. Barthell, T.L. Griswold,
J.-Y. Kim, and S. Kappagoda. 1998. Monitoring solitary bees in modified wildland
habitats: implications for bee ecology and conservation. Enviromental Entomology
27:11371148.
Frankie, G.W., R.W. Thorp, M. Schindler, J. Hernandez, B. Ertter, and M. Rizzardi. 2005.
Ecological patterns of bees and their host ornamental flowers in two northern California
cities. Journal of the Kansas Entomological Society 78:227246.
Franklin, M.T, M.L. Winston, and L.A. Morandin. 2004. Effects of clothianidin on Bombus
impatiens (Hymenoptera: Apidae) colony health and foraging ability. Journal of Economic
Entomology 97(2):369373.
Frazier, M.T., J. Finley, C.H. Collison, and E. Rajotte. 1994. The incidence and impact of
honey bee tracheal mites and nosema disease on colony mortality in Pennsylvania. Bee
Science 3:94100.
Free, J.B. 1970. Insect Pollination of Crops. New York: Academic Press.
Free, J.B. 1993. Insect Pollination of Crops. 2nd edition. San Diego: Academic Press.
Freitas, B.M., and J.O.P. Pereira, eds. 2004. Solitary BeesConservation, Rearing and Management for Pollination. Fortaleza: Imprensa Universitria.
Frick, T.B., and D.W. Tallamy. 1996. Density and diversity of nontarget insects killed by suburban electric insect traps. Entomological News 107:7782.
Fries, I., S. Camazine, and J. Sneyd. 1994. Population dynamics of Varroa jacobsoni: a model
and a review. Bee World 75:528.
Frison, T.H. 1921. New distribution records for North American Bremidae, with the description of a new species (Hym). Entomology News 32:144148.
Fronk, W.D. 1963. Increasing alkali bees for pollination. Wyoming Agricultural Experimental
Station Mimeo Cirular 184.
Gaidet-Drapier, N., H. Fritz, M. Bourgarel, P.C. Renaud, P. Poilecot, P. Chardonnet, C. Coid,
D. Poulet, and S. Le Bel. 2006. Cost and efficiency of large mammal census techniques:
comparison of methods for a participatory approach in a communal area, Zimbabwe.
Biodiversity and Conservation 15:735754.
Galen, C., K.A. Zimmer, and M.E. Newport. 1987. Pollination in floral scent morphs of
Polemonium viscosum: a mechanism for disruptive selection on flower size. Evolution
41:599606.
Galindo, C., A. Sanchez, R.H. Quijano, and L.G. Herrera. 2004. Population dynamics of a
resident colony of Leptonycteris curasoae (Chiroptera: Phyllostomidae) in central Mexico.
Biotropica 36:382391.
Gary, N.E., R.E. Page, Jr., R.A. Morse, C.E. Henderson, M.E. Nasr, and K. Lorenzen.
1990. Comparative resistance of honey bees (Apis mellifera L.) from Great Britain and
United States to infestation by tracheal mites (Acarapis woodi). American Bee Journal
130:667669.

232
Gathmann, A., H.J. Greiler, and T. Tsharntke. 1994. Trap-nesting bees and wasps colonizing
set-aside fields: succession and body size, management by cutting and sowing. Oecologia
98:814.
Gegear, R.J., M.C. Otterstatter, and J.D. Thomson. 2005. Does parasitic infection impair the ability of bumblebees to learn flower-handling techniques? Animal Behaviour
70:209215.
Gels, J.A., D.W. Held, and D.A. Potter. 2002. Hazards of insecticides to the bumble bees Bombus impatiens (Hymenoptera: Apidae) foraging on flowering white clover in turf. Journal
of Economic Entomology 95(4):722728.
Genersch E., C. Yue, I. Fries, and J.R. de Miranda. 2006. Detection of deformed wing virus,
a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum)
with wing deformities. Journal of Invertebrate Pathology 91(1):6163.
Georghiou, G.P. 1980. Insecticide resistance and prospects for its management. Residue Reviews 76:131145.
Gerson, U., R. Mozes-Koch, and E. Cohen. 1991. Enzyme levels used to monitor pesticide
resistance in Varroa jacobsoni. Journal of Apicultural Research 30(1):1720.
Gess, F.W., and S.K. Gess. 1993. Effects of increasing land utilization on species representation and diversity of aculeate wasps and bees in the semi-arid areas of southern Africa.
Pp. 83113 in Hymenoptera and Biodiversity, J. LaSalle and I.D. Gauld, eds. Wallingford:
CAB International.
Ghazoul, J. 2005a. Buzziness as usual? Questioning the global pollination crisis. Trends in
Ecology and Evolution 20(7):367373.
Ghazoul, J. 2005b. Response to Steffan-Dewenter et al., 2005: Questioning the global pollination crisis. Trends in Ecology and Evolution 20(12):652653.
Ghazoul, J. 2005c. Pollen and seed dispersal among dispersed plants. Biological Reviews
80:413443.
Gibbs, D., D. Walton, L.P. Brower, and A.K. Davis. 2006. Monarch butterfly (Lepidoptera,
Nymphalidae) migration monitoring at Chincoteague, VA and Cape May, NJ: a comparison of long-term trends. Journal of the Kansas Entomological Society 79(2):56164.
Giles, V., and J.S. Ascher. 2006. A Survey of the Bees of the Black Rock Forest Preserve, New
York (Hymenoptera: Apoidea). Journal of Hymenoptera Research 15:208231.
Givnish, T.J. 1986. Serotiny, Geography, and Fire in the Pine Barrens of New Jersey. Evolution
35:101123.
Gochnauer, T.A. 1951. Drugs fight foul brood diseases in bees. Minnesota Farms and Home
Science 9:15.
Goettel, M.S., G.M. Duke, and D.W. Goerzen. 1997. Pathogenicity of Ascosphaera larvis
to larvae of the alfalfa leafcutting bee, Megachile rotundata. Canadian Entomologist
129:10591065.
Goldblatt, P., and J.C. Manning. 1999. Gladiolus in Southern Africa. Cape, South Africa:
Fernwood Press.
Goldblatt, P., P. Bernhardt, and J.C. Manning. 1998. Pollination of petaloid geophytes by monkey beetles (Scarabaeidae: Rutelinae: Hoplini) in southern Africa. Annals of the Missouri
Botanical Garden 85:215230.
Goldblatt, P., P. Bernhardt, P. Vogan, and J.C. Manning. 2004. Pollination by fungus gnats
(Diptera Myscetophilidae) and self-recognition sites in Tolmiea menziesii (Saxifragaceae).
Plant Systematics and Evolution 244:5567.
Goldblatt, P., J.C. Manning, and P. Bernhardt. 2005. The floral biology of Melasphaerula
(Iridaceae:Crococoideae): is this monotypic genus pollinated by March flies (Diptera:
Bibionidae)? Annals of the Missouri Botanical Garden 92:268274.
Goldingay, R.L., S.M. Carthew, and R.J. Whelan. 1991. The importance of non-flying mammals in pollination. Oikos 61:7987.

REFERENCES
233
Gmez, J.M. 2000. Effectiveness of ants as pollinators of Lobularia maritima: effects on main
sequential fitness components of the host plant. Oecologia 122:9097.
Gmez, J.M., R. Zamora, J.A. Hoda, and D. Garcia. 1996. Experimental study of pollination
by ants in Mediterranean high mountain and arid habitats. Oecologia 105:236242.
Goncalves, L.S., A.C. Stort, and D. DeJong. 1991. Beekeeping in Brazil. Pp. 359372 in
The African Honey Bee, M. Spivak, D.J.C. Fletcher, and M.D. Breed, eds. Oxford:
Westview Press.
Goodwillie, C. 2000. Inbreeding depression and mating systems in two species of Linanthus
(Polemoniaceae). Heredity 84:283293.
Goodwin, M., and C. Van Eaton. 1999. Elimination of American Foulbrood Without the Use
of Drugs. National Beekeepers Association of New Zealand. Tauranga, New Zealand:
Advance Print. 78 pp.
Gorguet, B., A.W. van Heusden, and P. Lindhout. 2005. Parthenocarpic fruit development in
tomato. Plant Biology 7(2):131139.
Gottsberger, G. 1989a. Beetle pollination and flowering rhythm of Annona spp. (Annonaceae)
in Brazil. Plant Systematics and Evolution 167:165187.
Gottsberger, G. 1989b. Comments on flower evolution and beetle pollination in the genera
Annona and Rolliniua (Annonaceae). Plant Systematics and Evolution 167:189194.
Goulson, D. 2003a. Effects of introduced bees on native ecosystems. Annual Review of Ecology and Systematics 34:126.
Goulson, D. 2003b. Conserving wild bees for crop pollination. Food, Agriculture and Environment 1(1):142144.
Goulson, D. 2003c. Bumblebees: Their Behaviour and Ecology. New York: Oxford University
Press.
Goulson, D., and L.C. Derwent. 2004. Synergistic interactions between an exotic honeybee and an exotic weed: pollination of Lantana camara in Australia. Weed Research
44:195202.
Goulson, D., M.E. Hanley, B. Darvill, J.S. Ellis, and M.E. Knight. 2005. Causes of rarity in
bumblebees. Biological Conservation 122:18.
Graham, C.H., S. Ferrier, F. Huettman, C. Moritz, and A.T. Peterson. 2004. New developments
in museum-based informatics and applications in biodiversity analysis. Trends in Ecology
and Evolution 19:497503.
Grant, K.A., and V. Grant. 1965. Flower Pollination in the Phlox Family. New York: Columbia
University Press.
Grant, K.A., and V. Grant. 1967. Effects of hummingbird migration on plant speciation in the
California flora. Evolution 21:457465.
Grant, K.A., and V. Grant. 1968. Hummingbirds and their flowers. New York: Columbia
University Press.
Grant, V. 1950. The pollination of Calycanthus occidentalis. American Journal of Botany
37:294297.
Grant, V. 1985. Additional observations on temperate North American hawkmoth flowers.
Botanical Gazette 146:517520.
Grant, V., and K.A. Grant. 1979. The pollination spectrum in the southwestern american cactus
flora. Plant Systematics and Evolution 133:2937.
Green, M.B., H.M. LeBaron, and W.K. Moberg. 1990. Managing Resistance to Agrochemicals: from Fundamental Research to Practical Strategies.Washington: Americal Chemical
Society. 496 pp.
Greenleaf, S.S. 2005. Local-scale and foraging-scale affect bee community abundances, species richness, and pollination services in Northern California. Ph.D thesis. Princeton
University.

234
Greenleaf, S.S., and C. Kremen. 2006a. Wild bee species increase tomato production but
respond differently to surrounding land use in Northern California. Biological Conservation 133:8187.
Greenleaf, S.S., and C. Kremen. 2006b. Wild bees enhance pollination by honey bees pollination of hybrid sunflower. Proceedings of the National Academy of Sciences USA
103:1389013895.
Gregory, D.P. 19631964. Hawkmoth pollination in the genus Oenothera. Aliso 5:357419.
Griffin, B.L. 1993. The Orchard Mason Bee. Bellingham: Knox Cellars Publishing. 69 pp.
Griffin, B.L. 1999. The Orchard Mason Bee: The Life History, Biology, Propagation and Use
of a Truly Benevolent and Beneficial Insect. Bellingham: Knox Cellars Publishing.
Griffith, M.P. 2004. The origins of an important cactus crop, Opuntia ficus-indica (Cactaceae):
new molecular evidence. American Journal of Botany 91:19151921.
Grimaldi, D., and M.S. Engel. 2005. Evolution of the Insects. New York: Cambridge University Press.
Grixti, J.C., and Packer, L. 2006. Changes in the bee fauna (Hymenoptera: Apoidea) of
an old field site in southern Ontario, revisited after 34 years. Canadian Entomologist
138(2):147164.
Groom, M.J. 1998. Allee effects limit population viability of an annual plant. American
Naturalist 151:487496.
Groom, M.J. 2001. Consequences of subpopulation isolation for pollination, herbivory,
and population growth in Clarkia concinna (Onagraceae). Biological Conservation
100:5563.
Guzmn-Novoa, E., and R.E. Page, Jr. 1994a. The impact of Africanized bees on Mexican
beekeeping. American Bee Journal 134(2):101106.
Guzmn-Novoa, E., and R.E. Page, Jr. 1994b. Genetic dominance and worker interactions
affect honeybee colony defense. Behavioral Ecology 5(1):9197.
Guzmn-Novoa, E., and R.E. Page, Jr. 1999. Selective breeding of honey bees (Hymenoptera:
Apidae) in Africanized areas. Journal of Economic Entomolology 92(3):521525.
Hackney, E.E., and J.B. McGraw. 2001. Experimental demonstration of an Allee effect in
American ginseng. Conservation Biology 1:129136.
Hall, R.J., S. Gubbins, and C.A. Gilligan. 2004. Invasion of drug and pesticide resistance
is determined by a trade-off between treatment efficacy and relative fitness. Bulletin of
Mathematical Biology 66(4):825840.
Halpern, S. 2001. Four Wings and a Prayer: Caught in the Mystery of the Monarch Butterfly.
New York: Pantheon.
Hambler, C., and M.R. Speight. 1996. Extinction rates in British nonmarine invertebrates since
1900. Conservation Biology 10:892896.
Handel, S.N. 1997. The role of plant-animal mutualisms in the design and restoration of
natural communities. Pp. 111132 in Restoration Ecology and Sustainable Development,
K.M. Urbanska, N.R. Webb, and P.J. Edwards, eds. Cambridge: Cambridge University
Press.
Handel, S.N., G.R. Robinson, and A.J. Beattie. 1994. Biodiversity resources for restoration
ecology. Restoration Ecology 2:230241.
Hanski, I., and O. Ovaskainen. 2000. The metapopulation capacity of a fragmented landscape.
Nature 404:755758.
Harbo, J.R. 1992. Breeding honey bees (Hymenoptera; Apidae) for more rapid development
of larvae and pupae. Journal of Economic Entomology 85(6):21252130.
Harbo, J.R. 1993. Evaluating bees for resistance to Varroa mites. American Bee Journal
133(12):865.
Harbo, J.R., and J.W. Harris. 1999a. Selecting honey bees for resistance to Varroa jacobsoni.

REFERENCES
235
Harbo, J.R., and J.W. Harris. 1999b. Heritability in honey bees (Hymenoptera: Apidae) of
characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae).
Journal of Economic Entomology 92(2):261265.
Harbo, J.R., and J.W. Harris. 2001. Resistance to Varroa destructor (Mesostigmata: Varroidae) when mite-resistant queen honey bees (Hymenoptera: Apidae) were free-mated with
unselected drones. Journal of Economic Entomology 94(6):13191323.
Harbo, J.R., and J.W. Harris. 2004. Effect of screen floors on populations of honey bees and
parasitic mites (Varroa destructor). Journal of Apicultural Research 43(3):114117.
Harbo, J.R., and J.W. Harris. 2005. Suppressed mite reproduction explained by the behaviour
of adult bees. Journal of Apicultural Research 44(1):2123.
Harbo, J.R., and R. Hoopingarner. 1995. Resistance to varroa expressed by honey bees in the
USA. American Bee Journal 135(12):827.
Harbo, J.R., R.A. Hoopingarner, and J.W. Harris. 1997. Evaluating honey bees for resistance
to varroa mites: procedures and results. American Bee Journal 137(3):223224.
Harder, L.D. 1982. Functional differences of the proboscides of short- and long-tongued bees
(Hymenoptera, Apoidae). Candian Journal of Zoology 61:15801586.
Harder, L.D. 1983. Flower handling efficiency of bumble bees: morphological aspects of probing time. Oecologia 57(12):274280.
Harder, L.D. 1986 Effects of nectar concentration and flower depth on flower handling efficiency of bumble bees. Oecologia 69:309315.
Harris, J.W., and T.E. Rinderer. 2004. Varroa resistance of hybrid ARS Russian honey bees.
American Bee Journal 144:797800.
Harris, J.W., T. Rinderer, V. Kuznetsov, R. Danka, G. Delatte, L. de Guzman, and J. Villa.
2002. Imported Russian honey bees: quarantine and initial selection for varroa resistance.
Harris, L.F., and S.D. Johnson. 2004. The consequences of habitat fragmentation for plantpollinator mutualisms. International Journal of Tropical Insect Science 24:2943.
Harrison, S., and L. Fahrig. 1995. Landscape pattern and population conservation. Pp. 293
308 in Mosaic Landscapes and Ecological Processes, L. Hansson, L. Fahrig, and G. Merriam, eds. New York: Chapman and Hall.
Harrison, S., D.D. Murphy, and P.R. Ehrlich. 1988. Distribution of the bay checkerspot butterfly, Euphydryas Editha Bayensis: evidence for a metapopulation model. American
Hartl, D.L., and A.G. Clark. 1997. Principles of Population Genetics. 3rd edition. Sunderland,
Mass.: Sinauer Associates.
Haseman, L., and L.F. Childers. 1944. Controlling American foulbrood with sulfa drugs. Missouri Agricultural Experimentation Station Bulletin 482:116.
Haugaasen, T., J. Barlow, and C.A. Peres. 2003. Effects of surface fires on understorey insectivorous birds and terrestrial arthropods in central Brazilian Amazonia. Animal Conservation 6:299306.
Haughton, A.J.,G.T. Champion, C. Hawes, M.S. Heard, D.R. Brooks, D.A. Bohan, S.J. Clark,
A.M. Dewar, L.G. Firbank, J.L. Osborne, J.N. Perry, P. Rothery, D.B. Roy, R.J. Scott, I.P.
Woiwod, C. Birchall, M.P. Skellern, J.H. Walker, P. Baker, E.L. Browne, A.J. Dewar, B.H.
Garner, L.A. Haylock, S.L. Horne, N.S. Mason, R.J. Sands, and M.J. Walker. 2003. Invertebrate responses to the management of genetically modified herbicide-tolerant and conventional spring crops. II. Within field epigeal and aerial arthropods. Philosophical Transactions
of the Royal Society of London Series BBiological Sciences 358(1439):8631877.
Hawes, C., A.J. Haughton, J.L. Osborne, D.B. Roy, S.J. Clark, and J.N. Perry. 2003. Responses
of plants and invertebrate trophic groups to contrasting herbicide regimes in the farm scale
evaluations of genetically modified herbicide-tolerant crops. Philosophical Transactions of
the Royal Society of London Series BBiological Sciences 358(1439):18991913.

236
Hayami, Y., and V.W. Ruttan. 1985. Agricultural Development: An International Perspective.
2nd edition. Baltimore: Johns Hopkins University Press.
Hayata, Y., Y. Niimi, and N. Iwasaki. 1995. Inducing parthenocarpic fruit of watermelon with
plant bioregulators. Acta Horticulturae (394):235240.
Headings, M.E. 2000. Biology and behavior of the small hive beetle, Aethina tumida, a new
potential pest in the Western Hemisphere. Pp. 227232 in Proceedings of the 35th Annual
Meeting, Caribbean Food Crops Society, Castries, St-Lucia, July 2531, 1999, W. Colon,
ed. Isabela, Puerto Rico: Caribbean Food Crops Society.
Heal, G. M. 2000. Nature and the Marketplace: Capturing the Value of Ecosystem Services.
Washington: Island Press.
Heard, M.S., C. Hawes, G.T. Champion, S.J. Clark, L.G. Firbank, A.J. Haughton, A.M. Parish,
J.N. Perry, P. Rothery, R.J. Scott, M.P. Skellern, G.R. Squire, and M.O. Hill. 2003. Weeds
in fields with contrasting conventional and genetically modified herbicide-tolerant crops:
effects on abundance and diversity. Philosophical Transactions of the Royal Society of
London Series BBiological Sciences 358(1439):18191832.
Hedrick, P.W., J. Gadau, and R.E. Page, Jr. 2006. Genetic sex determination and extinction.
Trends in Ecology and Evolution 21:5557.
Heinrich, B. 1979. Bumblebee Economics. Cambridge, Mass.: Harvard University Press.
Heinrich, B. 2004. Bumblebee Economics. Revised edition. Cambridge, Mass.: Harvard University Press.
Heinz, C. 2005. Honey Bees and RIFA Seminar. Almond Board of California. Available at:
http://almondboard.files.cms-plus.com/PDFs/Heintz%20-%20ABC%20Research%20Re
view.pdf. Accessed December 28, 2005.
Heiser, C.B. 1954. Variation and subspeciation in the common sunflower, Helianthus annuus.
American Midland Naturalist 51:287305.
Heithaus, E.R. 1982. Coevolution between bats and plantas. Pp. 327367 in Ecology of Bats,
T.H. Kunz, ed. New York: Plenum Press.
Hellmich, R.L. 1986. Mating European honey-bee queens to European drones in areas with
Africanized bees. American Bee Journal 126(12):830831.
Hellmich, R.L. 1991. Continuing commercial queen production after the arrival of Africanized
honey bees. Pp. 187197 in The African Honey-Bee. Oxford: Westview Press.
Hellmich, R.L., A.M. Collins, R.G. Danka, and T.E. Rinderer. 1988. Influencing matings of
European honey bee queens in areas with Africanized honey bees (Hymenoptera: Apidae).
Hellmich, R.L., B.D. Siegfried, M.K. Sears, D.E. Stanley-Horn, M.J. Daniels, H.R. Mattila,
T. Spencer, K.G. Bidne, and L.C. Lewis. 2001. Monarch larvae sensitivity to Bacillus
thuringiensis-purified proteins and pollen. Proceedings of the National Academy of Sciences USA 98:1192511930.
Helson, B.V., K.N. Barber, and P.D. Kingsbury. 1994. Laboratory toxicology of six forestry
insecticides to four species of bee (Hymenoptera: Apoidea). Archives of Environmental
Contamination and Toxicology 27:107114.
Herrera, C.M. 1987. Components of pollinator quality: comparative analysis of a diverse
insect assemblage. Oikos 50:7990.
Herrera, C.M. 1989. Seed dispersal by animals: a role in angiosperm diversification? American
Herrera, C.M. 2000. Flower-to-seedling consequences of different pollination regimes in an
insect-pollinated shrub. Ecology 81:1529.
Herring, T. 2003. The yellow pond lily of the Ozarks (Nuphar ozarkana): a pollination ecology
study. Thesis presented to the faculty of the Graduate School of Saint Louis University in
partial fulfillment of the requirements for the degree of Masters of Sciences.
Hickman, J.C. 1974. Pollination by ants: a low-energy system. Science 184(4143):12901292.

REFERENCES
237
Hill, J.K., C.D. Thomas, and B. Huntley. 1999. Climate and habitat availability determine
20th century changes in a butterflys range margin. Proceedings of the Royal Society of
London 266:11971206.
Hillesheim, E., W. Ritter, and D. Bassand. 1996. First data on resistance mechanisms of
Varroa jacobsoni (Oud.) against tau-fluvalinate. Experimental and Applied Acarology
20(5):283296.
Hines, H.M., and S.D. Hendrix. 2005. Bumble bee (Hymenoptera: Apidae) diversity and
abundance in tallgrass prairie patches: effects of local and landscape floral resources.
Environmental Entomology 34:14771484.
Hingston, A.B., and P.B. McQuillan. 1997. Displacement of Tasmanian native megachilid bees
by the recently introduced bumblebee Bombus terrestris (Linnaeus 1758)(Hymenoptera:
Apidae). Australian Journal of Zoology 47:5965.
Hingston, A.B., and P.B. McQuillan. 1998. Does the recently introduced bumblebee Bombus terrestris (Apidae) threaten Australian ecosystems? Australian Journal of Ecology
23:539549.
Hirsch, M., S. Pfaff, and V. Wolters. 2003. The influence of matrix type on flower visitors of
Centaurea jacea L. Agriculture Ecosystems and Environment 98:331337.
Hitchcock, J.D., J.O. Moffett, J.J. Lackett, and J.R. Elliott. 1970. Tylosin for control of American foulbrood disease in honey bees [Bacillus larvae, Apis mellifera]. Journal of Economic
Hoebeke, E.R., and A.G.J. Wheeler. 1999. Anthidium oblangatum (Illiger): an Old World bee
(Hymenoptera: Megachilidae) new to North America, and new North American records
for another adventive species, A. manicatum (L.). Scientific Papers, Natural History
Museum, The University of Kansasa continuation of the University of Kansas Science
Bulletin 24:2124.
Hoff, F.L., and J.K. Phillips. 1989. Honey: Background for 1990 farm legislation. AGES
8943.
Hlldobler, B., and E.O. Wilson. 1990. The Ants. Cambridge, Mass.: Belknap Press.
Hlldobler, B., and E.O. Wilson. 1994. Journey to the Ants: A Story of Scientific Exploration.
Cambridge, Mass.: Belknap Press.
The Honeybee Genome Sequencing Consortium. 2006. Insights into social insects from the
genome of the honeybee Apis mellifera. Nature 443:931949.
Hood, W.M. 2004a. The small hive beetle, Aethina tumida: a review. Bee World 85:5159.
Hood, W.M. 2004b. The biology and management of small hive beetles. In Proceedings of the
8th IBRA International Conference on Tropical Bees and VI Encontro sobre Abelhas,
Ribeirao Preto, Brasil, September 610, 2004. K.H. Hartfelder, D. de Jong, R.A. Pereira,
A. dos Santos Cristino, M.M. Morais, E.D. Tanaka, A.P. Lourenco, J.E.B. da Silva,
G.F. de Almeida, and A.M. de Nascimento, eds. Cardiff: International Bee Research
Association.
Hoopingarner, R. 1991. Assessment of the declining feral honeybee population. Annual Report
Indiana State Horticultural Society. The Society 121:154157.
Hoopingarner, R.H., and G.D. Waller. 1992. Crop pollination. Pp. 10431082 in The Hive
and the Honey Bee, J.M. Graham, ed. Hamilton, Ill.: Dadant and Sons.
Hoppe, H., W. Ritter, and E.W.C. Stephen. 1989. The control of parasitic bee mites: Varroa
jacobsoni, Acarapis woodi and Tropilaelaps clareae with formic acid. American Bee
Journal 129:739742.
Hughes, M.J. 1996. Commercial rearing of bumble bees. Pp. 4047 in Bumble Bees for Pleasure
and Profit, A. Matheson, ed. Cardiff: International Beekeeper Research Assocation.
Hunt, G.J., E. Guzman-Novoa, M.K. Fondrk, and R.E. Page, Jr. 1998. Quantitative trait loci
for honey bee stinging behavior and body size. Genetics 148(3):12031213.
Hunter, L.A., J.A. Jackman, and E.A. Sugden. 1993. Detection records of Africanized honey
bees in Texas during 1990, 1991 and 1992. Southwestern Entomologist 18(2):7989.

238
Husband, R.W., and R.N. Sinha. 1970. A revision of the genus Locustacarus with a key to
the genera of the family Podapolipidae (Acarina). Annals of the Entomological Society
of America 63(4):11521162.
Hutson, A.M., S.P. Mickleburgh, and P.A. Racey, compilers. 2001. Microchiropteran Bats:
Global Status Survey and Conservation Action Plan. IUCN/SSC Chiroptera Specialist
Group. Gland, Switzerland and Cambridge: IUCN. 258 pp.
Huxley, C.R., and D.F. Cutler, eds. 1991. Ant-Plant Interactions. New York: Oxford University
Press.
Imhoof, B., and P. Schmid-Hempel. 1999. Colony success of the bumble bee, Bombus terrestris,
in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi.
Insectes Sociaux 46:233238.
Imms, A.D. 1921. Isle of Wight disease in hive bees. Nature 2687:283284.
Inouye, D.W. 1977. Species structure of bumblebee communities in North America and Europe.
Pp. 3540 in W. J. Mattson, ed., The Role of Arthropods in Forest Eecosystems. New
York: Springer Verlag.
Intenthron, M., and J. Gerrard. 1999. Making Nests for Bumble Bees. Cardiff: International
Beekeeper Research Assocation. 38 pp.
IUCN (International Union for the Conservation of Nature and Natural Resources/The World
Conservation Union). 1996. 1996 IUCN Red List of Threatened Animals. Available at:
http://www.iucn.org/themes/ssc/96anrl/intro.htm. Accessed March 31, 2006.
Jacobs, G.H. 1992. Ultraviolet vision in vertebrates. American Zoologist 32:544554.
Janson, C.H., J. Terborgh, and L.H. Emmons. 1981. Non-flying mammals as pollinating agents
in the Amazonian forest. Biotropica 13:16 Suppl. S.
Janzen, D.H. 1974. The deflowering of Central America. Natural History 83:4853.
Janzen, D.H. 1985. The natural history of mutualisms. Pp. 4099 in The Biology of Mutualism,
D.H. Boucher, ed. New York: Oxford University Press.
Janzen, D.H. 2004. Setting up tropical biodiversity for conservation through non-damaging
use: participation by parataxonomists. Journal of Applied Ecology 41:181187.
Jarlan A., D. de Oliveira, and J. Gingras. 1997. Effects of Eristalis tenax (Diptera: Syrphidae)
pollination on characteristics of greenhouse sweet pepper fruits. Journal of Economic
Entomology 90(6):16501654.
Javorek, S.K., K.E. Mackenzie, and S.P. Vander-Kloet. 2002. Comparative pollination effectiveness among bees (Hymenoptera: Apoidea) on lowbush blueberry (Ericaceae: Vaccinium
angustifolium). Annals of the Entomological Society of America 95(3):345351.
Jaycox, E.R. 1967. An adventive Anthidium in New York State (Hymenoptera: Megachilidae).
Journal of the Kansas Entomological Society 40:124126.
Jennersten, O. 1988. Pollination in Dianthus deltoides (Caryophyllaceae): effects of habitat
fragmentation on visitation and seed set. Conservation Biology 2:359367.
Jesse, L.C.H., and J.J. Obrycki. 2002. Assessment of the non-target effects of transgenic Bt
corn pollen and anthers on the milkweed tiger moth, Euchatias egle Drury (Lepidoptera:
Arctiidae). Journal of the Kansas Entomological Society 75:5558.
Jimenez-Hidalgo I., G. Virgen, D. Martinez, G. Vandemark, J. Alego, and V. Olalde. 2004.
Identification and characterization of soft rot bacteria of Agave tequilana Weber Var Azul.
Journal of Plant Pathology 110:317331.
Johansen, C.A. 1977. Pesticides and pollinators. Annual Review of Entomology 22:177192.
Johansen, C.A., and D.F. Mayer. 1990. Pollinator Protection. A Bee and Pesticide Handbook.
Cheshire, Conn.: Wicwas Press.
Johnson, S.D., C.L. Collin, H.J. Wissman, E. Halvarsson, and J. Agren. 2004. Factors contributing to variation in seed production among remnant populations of the endangered
daisy Gerbera aurantiaca. Biotropica 36(2):48155.
Jones, F.M., and C.P. Kimball. 1943. The Lepidoptera of Nantucket and Marthas Vineyard.
Nantucket Maria Mitchell Association 4:1217.

REFERENCES
239
Jones, R., and P. Munn. 1998. Habitat Management for Wild Bees and Wasps. Cardiff: International Beekeeper Research Assocation. 38 pp.
Jousselin, E., J.Y. Rasplus, and F. Kjellberg. 2001. Shift to mutualism in parasitic lineages of
the fig/fig wasp interaction. Oikos 94:287294.
Juenger, T., and J. Bergelson. 2000. The evolution of compensation to herbivory in scarlet
gilia, Ipomopsis aggregata; herbivore-imposed selection and the quantitative genetics of
tolerance traits. Evolution 54(3):764777.
Kandori, I. 2002. Diverse visitors with various pollinator importance and temporal change
in the important pollinators of Geranium thunbergii (Geraniaceae). Ecological Research
17(3):283294.
Kanga, L.H.B., W.A. Jones, and R.R. James. 2003a. Field trials using the fungal pathogen,
Metarhizium anisopliae (Deuteromycetes: Hyphomycetes) to control the ectoparasitic
mite, Varroa destructor (Acari: Varroidae) in honey bee, Apis mellifera (Hymenoptera:
Apidae) colonies. Journal of Economic Entomology 96:10911099.
Kanga, L.H.B., R.R. James, and D.G. Boucias. 2003b. Hirsutella thompsonii and Metarhizium
anisopliae as potential microbial control agents of Varroa destructor, a honey bee parasite.
Journal of Invertebrate Pathology 81:175184.
Kato, M. 2000. Anthophilous insect community and plant-pollinator interactions on Amami
Islands in the Ryukyu Archipelago, Japan. Contributions from the Biological Laboratory,
Kyoto University 29:157252.
Kato, M., A. Shibata, T. Yasui, and H. Nagamasu. 1999. Impact of introduced honeybees, Apis
mellifera, upon native bee communities in the Bonin (Ogasawara) Islands. Researches on
Population Ecology 41:217228.
Kays, R.W. 1999. Food preferences of kinkajous (Potos flavus): a frugivorous carnivore. Journal of Mammalogy 80:589599.
Kearns, C.A. 1990. The role of fly pollination in montane habitats. Dissertation. University
of Maryland, College Park.
Kearns, C.A., and D.W. Inouye. 1993. Techniques for Pollination Biologists. Niwot, Colo.:
University Press of Colorado.
Kearns, C.A., and D.W. Inouye. 1997. Pollinators, flowering plants, and conservation biology.
BioScience 47:297307.
Kearns, C., and J. Thomson. 2001. The Natural History of Bumble Bees. A Sourcebook for
Investigations. Boulder: University Press of Colorado.
Kearns, C.A., D.W. Inouye, and N.M. Waser. 1998. Endangered mutualisms: the conservation
of plant-pollinator interactions. Annual Review of Ecology and Systematics 29:83112.
Kemp, W.P. 2000. The future of crop pollination. American Bee Journal 140:851853.
Kephart, D. 2005. Pollen-pollinator limitation. Pp. 364370 in Practical Pollination Biology,
A. Dafni, P.G. Kevan, and B.C. Husband, eds. Cambridge, Canada: Enviroquest.
Kephart, S., and K. Theiss. 2003. Pollinator-mediated isolation in sympatric milkweeds
(Asclepias): do floral morphology and insect behavior influence species boundaries? New
Phylogist 161:265277.
Kevan, P.G. 1972. Insect pollination of high arctic flowers. Journal of Ecology 60:813847.
Kevan, P.G. 1974. Pollination, pesticides and environmental quality. BioScience 24:198199.
Kevan, P.G. 1975a. Pollination and environmental conservation. Environmental Conservation
2:222227.
Kevan, P.G. 1975b. Forest application of the insecticide fenitrothion and its effects on wild bee
pollinators (Hymenoptera: Apoidea) of lowbush blueberries (Vaccinium spp.) in southern
New Brunswick, Canada. Biological Conservation 7:301309.
Kevan, P.G. 1984. Pollination by animals and angiosperm biosystematics. Pp. 271292 in Plant
Biosystematics, W.F. Grant, ed. Toronto: Academic Press.
Kevan, P.G. 1999. Pollinators as bioindicators of the state of the environment: species, activity
and diversity. Agriculture, Ecosystems and Environment 74:373393.

240
Kevan, P.G. 2001. Pollination: plinth, pedestal, and pillar for terrestrial productivity. The
why, how, and where of pollination protection, conservation, and promotion. Pp. 768
in Bees and Crop PollinationCrisis, Crossroads, Conservation, C.S. Stubbs and F.A.
Drummond, eds. Proceedings, Entomological Society of America. Lanham, Md.: Thomas
Say Publications in Entomology.
Kevan, P.G., and D. Eisikowitch. 1990. Self- and cross-pollination in canola (Brassica napus L.
var. O.A.C. Triton) and its implication on seed germination. Euphytica 45:3941.
Kevan, P.G., and V.L. Imperatriz-Fonseca, eds. 2002. Pollinating Bees: The Conservation Link
Between Agriculture and Nature. Proceedings of the Workshop on the Conservation and
Sustainable Use of Pollinators in Agriculture, with Emphasis on Bees, held in S. Paulo,
Brazil in October 1998. Brazil: Ministry of Environment. 313 pp.
Kevan, P.G., and D.M. Kendall. 1997. Liquid assets for fat bankers: summer nectarivory by
migratory moths in the Rocky Mountains, Colorado, USA. Arctic and Alpine Research
29:478482.
Kevan, P.G., and T.P. Phillips. 2001. The economic impacts of pollinator declines: an approach
to assessing the consequences. Conservation Ecology 5(1):8.
Kevan, P.G., and R.C. Plowright. 1995. Impact of pesticides on forest pollination. Pp. 607618
in Forest Insect Pests in Canada, J.A. Armstrong and W.G.H. Ives, eds. Ottawa: Natural
Resources Canada.
Kevan, P.G., E.A. Clark, and V.G. Thomas. 1990. Insect pollinators and sustainable agriculture.
American Journal of Alternative Agriculture 5:1322.
Kevan, P.G., W.A. Straver, M. Offer, and T.M. Laverty. 1991. Pollination of greenhouse tomatoes by bumblebees in Ontario. Proceedings of the Entomological Society of Ontario
122:1519.
Kevan, P.G., C.F. Greco, and S. Belaoussoff. 1997. Log-normality of biodiversity and abundance in diagnosis and measuring of ecosystemic health: pesticide stress on pollinators
on blueberry heaths. Journal of Applied Ecology 34:11221136.
Kevan, P.G., V.L. Shipp, J.P. Kapongo, and M.S. Al-mazraawi. 2005. Bee pollinators vector
biological control agents against insect pests of horticultural crops. Pp. 7795 in First
Short Course on Pollination of Horticulture Plants, J.M. Guerra-Sanz, A. Roldn Serrano,
and A. Mena Granero, eds. La Mojonera, Spain: CIFA.
Kevan, P.G., M.A. Hannan, N. Ostiguy, and E. Guzman-Novoa. 2006. A summary of the
Varroa-virus disease complex in honey bees. American Bee Journal 146:694697.
Kim, J., N. Williams, and C. Kremen. 2006. Effects of cultivation and proximity to natural
habitat on ground-nesting native bees in California sunflower fields. Journal of the Kansas
Entomological Society 79(4):309320.
Kincaid. 1963. The ant-plant, Orthocarpus pusillus, Bentham (Scrophulariaceae). Transactions
of the American Microscopical Society 82:101105.
Kingsley, K.J. 1996. Behavior of the Delhi Sands flower-loving fly (Diptera: Mydidae),
a little-known endangered species. Annals of the Entomological Society of America
89:883891.
Kirk, W.D.J. 1984. Pollen-feeding in thrips (Insecta: Thysanoptera). Journal of Zoology
204:107117.
Kirk, W.D.J. 1985. Pollen-feeding and the host specificity and fecundity of flower thrips (Thysanoptera). Ecological Entomology 10:281289.
Kirk, W.D.J. 1988. Thrips and pollination biology. Pp. 129135 (Chapter 10) in Dynamics of
Insect-Plant Interaction, T.N. Ananthakrishnan and A. Raman, eds. New Delhi: Oxford
and IBH.
Kirk, W.D.J. 1993. Thrips and pollen. Pp. 251258 (Chapter 15) in Advances in Thysanopterology, J.S. Bhatti, ed. New Delhi: Scientia Publishing.
Kirk, W.D.J. 1997. Feeding. Pp. 119174 (Chapter 4) in Thrips as Crop Pests, T. Lewis, ed.
Wallingford: CAB International.

REFERENCES
241
Klanderud, K., and H.J.B. Birks. 2003. Recent increases in species richness and shifts in altitudinal distributions of Norwegian mountain plants. The Holocene 13:16.
Kleijn, D., F. Berendse, R. Smit, and N. Gilissen. 2001. Agri-environment schemes do not effectively protect biodiversity in Dutch agricultural landscapes. Nature 413:723725.
Kleijn, D., F. Berendse, R. Smit, N. Gilissen, J. Smit, B. Brak, and R. Groeneveld. 2004. The
ecological effectiveness of agri-environment schemes in different agricultural landscapes
in The Netherlands. Conservation Biology 18:775786.
Kleijn, D., R.A. Baquero, Y. Clough, M. Daz, J. De Esteban, F. Fernndez, D. Gabriel, F.
Herzog, A. Holzschuh, R. Jhl, E. Knop, A. Kruess, E.J.P. Marshall, I. Steffan-Dewenter,
T. Tscharntke, J. Verhulst, T.M. West, and J.L. Yela. 2006. Mixed biodiversity benefits of
agri-environment schemes in five European countries. Ecology Letters 9(3):243.
Klein, A.M., I. Steffan-Dewenter, D. Buchori, and T. Tscharntke. 2002. Effects of land-use
intensity in tropical agroforestry systems on coffee flower-visiting and trap-nesting bees
and wasps. Conservation Biology 16:10031014.
Klein, A.M., I. Steffan-Dewenter, and T. Tscharntke. 2003a. Fruit set of highland coffee increases with the diversity of pollinating bees. Proceedings of the Royal Society of London
Series BBiological Sciences 270:955961.
Klein, A.M., I. Steffan-Dewenter, and T. Tscharntke. 2003b. Bee pollination and fruit set of Coffea arabica and C-canephora (Rubiaceae). American Journal of Botany 90:153157.
Klein, A.M., I. Steffan-Dewenter, and T. Tscharntke. 2003c. Pollination of Coffea canephora
in relation to local and regional agroforestry management. Journal of Applied Ecology
40:837845.
Klein, A.M., B.E. Vaissire, J.H. Cane, I. Steffan-Dewenter, S.A. Cunningham, C. Kremen, and
T. Tscharntke. 2007. Importance of pollinators in changing landscapes for world crops.
Proceedings of the Royal Society of London Series B. 274:303313.
Knight, T.M., J.A. Steets, J.C. Vamosi, S.J. Mazer, M. Burd, D.R. Campbell, M.R. Dudash,
M.O. Johnston, R.J. Mitchell, and T. Ashman. 2005a. Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology Evolution and Systematics
36:467497.
Knight, T.M., M.W. McCoy, J.M. Chase, K.A. McCoy, and R.D. Holt. 2005b. Trophic cascades
across ecosystems. Nature 437:880883.
Knight, T.M., J.A. Steets, and T.-L. Ashman. 2006. A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates
of pollen limitation. American Journal of Botany 92:27022776.
Knop, E., D. Kleijn, F. Herzog, and B. Schmid. 2006. Effectiveness of the Swiss agri-environment
scheme in promoting biodiversity. Journal of Applied Ecology 43:120127.
Knudsen J.T., L. Tollsten, and L.G. Bergstrom. 1993. Floral scentsA checklist of volatile
compounds isolated by head-space techniques. Phytochemistry 33:253280.
Knudsen, J.T., L. Tollsten, I. Groth, G. Bergstrom, and R.A. Raguso. 2004. Trends in floral
scent chemistry in pollination syndromes: floral scent composition in hummingbirdpollinated taxa. Botanical Journal of the Linnean Society 146:191199.
Knuth, P. 1906. Handbook of Flower Pollination. Volume I. Translated by J.R. Ainsworth
Davis, Oxford: Clarendon Press. 382 pp.
Knuth, P. 1908. Handbook of Flower Pollination. Volume II. Translated by J.R. Ainsworth
Davis, Oxford: Clarendon Press. 705 pp.
Knuth, P. 1912. Handbook of Flower Pollination. Volume II. Translated by J.R. Ainsworth
Davis, Oxford: Clarendon Press.
Kocher, S.D., and E.H. Williams. 2000. The diversity and abundance of North American butterflies vary with habitat disturbance and geography. Journal of Biogeography
27(4):785794.
Koeniger, N., G. Koeniger, and M. Delfinado-Baker. 1983. Observations on mites of the Asian
honeybee species. Apidologie 14:1978204.

242
Kogan, M. 1998. Integrated pest management: historical perspectives and contemporary developments. Annual Review of Entomology 43:243270.
Klreuter, J.G. 1761. Vorlufige Nachricht von einigen das Geschlecht der Pflanzen betreffenden Versuchen und Beobachtungen. Leipzig.
Koltunow, A.M., A. Vivian-Smith, and S.R. Sykes. 2000. Molecular and conventional breeding
strategies for seedless citrus. Acta Horticulturae (ISHS) 535:169174.
Kovach, J., R. Petzoldt, and G.E. Harman. 2000. Use of honeybees and bumble bees to disseminate Trichoderma harzianum 1295-22 to strawberries for Botrytis control. Biological
Control 18:235242.
Kral, R. 1960. A revision of Asimina and Deeringothamus (Annonaceae). Brittonia
12:233278.
Kraus, B., and R.E. Page. 1995. Effect of Varroa jacobsoni (Mesostigmata: Varroidae) on feral
Apis mellifera (Hymenoptera: Apidae) in California. Environmental Entomology 24:66,
14731480.
Krebbs, K., R.A. Medellin, Y. Petryzsyn, A. McIntire, L. Lewis, and D. Dalton. 2005. Lesser
long-nosed bat. Sonorensis. Newsletter of the Arizona-Sonora Desert Museum, Tucson,
Winter 2005 issue.
Krebs, C.J. 1999. Ecological Methodology. Menlo Park: Addison Wesley Longman.
Kremen, C. 1992. Assessing the indicator properties of species assemblages for natural areas
monitoring. Ecological Applications 2:203217.
Kremen, C., and R. Chaplin. Forthcoming (in press). Insects as providers of ecosystem services. In Insect Conservation Biology: Proceedings of the Royal Entomological Societys
23rd Symposium, A.J.A. Stewart, T.R. New, and O.T. Lewis, eds. Wallingford: CABI
Publishing.
Kremen, C., and R.S. Ostfeld. 2005. A call to ecologists: measuring, analyzing, and managing
ecosystem services. Frontiers in Ecology and the Environment 3:540548.
Kremen, C., and T. Ricketts. 2000. Global perspectives on pollination disruptions. Conservation Biology 14:12261228.
Kremen, C., R.K. Colwell, T.L. Erwin, D.D. Murphy, R.F. Noss, and M.A. Sanjayan. 1993.
Terrestrial arthropod assemblages: their use in conservation planning. Conservation
Biology 7:796808.
Kremen, C., R.L. Bugg, N. Nicola, S.A. Smith, R.W. Thorp, and N.M. Williams. 2002a. Native
bees, native plants and crop pollination in California. Fremontia 30:4149.
Kremen, C., N.M. Williams, and R.W. Thorp. 2002b. Crop pollination from native bees at
risk from agricultural intensification. Proceedings of the National Academy of Sciences
USA 99:1681216816.
Kremen, C., N.M. Williams, R.L. Bugg, J.P. Fay, and R.W. Thorp. 2004. The area requirements of an ecosystem service: crop pollination by native bee communities in California.
Ecology Letters 7:11091119.
Krombein, K.V. 1967. Trap-Nesting Wasps and Bees: Life Histories, Nests, and Associates.
Washington: Smithsonian Press. 570 pp.
Kron, P., B.C. Husband, and P.G. Kevan. 2001a. Across- and along-row pollen dispersal in
high density apple orchards: insights from allozyme markers. Journal of Horticultural
Science and Biotechnology 76:286294.
Kron, P., B.C. Husband, P.G. Kevan, and S. Belaoussoff. 2001b. Phenology, pollination neighborhood and distance affect pollen dispersal in high density apple orchards. HortScience
36:10391046.
Kudo, G., Y. Nishikawa, T. Kasagi, and S. Kosuge. 2004. Does seed production of spring
ephemerals decrease when spring comes early? Ecological Research 19(2):255259.
Kukuk, P. 1989. Evolutionary genetics of a primitive eusocial halictine bee, Dialictus zephyrus. Pp. 183202 in The Genetics of Social Evolution, M.D. Breed and R.E. Page, eds.
Boulder: Westview.

REFERENCES
243
Kunin, W.E. 1997. Population size and density effects in pollination: pollinator foraging and
plant reproductive success in experimental arrays of Brassica kaber. Journal of Ecology
85:225234.
Kunz, T.H. 1982. Roosting ecology of bats. Pp. 155 in Ecology of Bats, T.H. Kunz, ed. New
York: Plenum Press.
Labandeira, C.C. 1998. How old is the flower and the fly? Science 280:8588.
Labandeira, C.C., D.L. Dilcher, D.R. Davis, and D.L. Wagner. 1994. Ninety-seven million years
of angiosperm-insect association: paleobiological insights into the meaning of coevolution. Proceedings of the National Academy of Sciences USA 91:1227812282.
Ladley, J.J., and D. Kelly. 1995. Explosive New Zealand mistletoe. Nature 378:766.
Laidlaw, H.H., Jr. 1977. Instrumental Insemination of Honey Bee Queens. Hamilton, Ill.:
Dandant.
Laidlaw, H.H., Jr. 1992. Production of queens and package bees. Pp. 9891042 in The Hive
and the Honey Bee. Hamilton, Ill.: Dadant and Sons.
Laidlaw, H.H., Jr., and R.E. Page, Jr. 1998. Queen Rearing and Bee Breeding. Cheshire, Conn.:
WicWas Press. 224 pp.
Lake, J.C., and L. Hughes. 1999. Nectar production and floral characteristics of Tropaeolum majus L. grown in ambient and elevated carbon dioxide. Annals of Botany
84:535541.
Lammers, T.G., S.G. Weller, and A.K. Sakai. 1987. Japanese White-eye, an introduced passerine, visits the flowers of Clermontia arborescens, an endemic Hawaiian Lobelioid.
Pacific Science 41:7477.
Lamont, B.B., P.G.L. Klinkhamer, and E.T.F. Witkowski. 1993. Population fragmentation may
reduce fertility to zero in Banksia goodiia demonstration of the Allee effect. Oecologia
94:446450.
Langstroth, L.L. 1862. The Hive and the Honey Bee. New York: C.M. Saxton.
Lapidge, K.L., B.P. Oldroyd, and M. Spivak. 2002. Seven suggestive quantitative trait loci
influence hygienic behavior of honey bees. Naturwissenschaften 89(12):565568.
Larrea-Reynoso, E. 1998. Estudios preliminares para el control de los hongos Fusarium, Verticillium, Asterina y de una bacteria no clasificada en agave azul (Agave tequilana Weber
var. azul). Revista Mexicana de Fitopatologa 16:125.
Larsen, T.H., N. Williams, and C. Kremen. 2005. Extinction order and altered community
structure rapidly disrupt ecosystem functioning. Ecology Letters 8:538547.
Larson, B.M.H, and S.C.H. Barrett. 2000. A comparative analysis of pollen limitation in
flowering plants. Biological Journal of the Linnean Society 69:503520.
Larson, D.L., P.J. Anderson, and W. Newton. 2001. Alien plant invasion in mixed-grass
prairie: effects of vegetation type and anthropogenic disturbance. Ecological Applications
11(1):128141.
Law, B.S., and M. Lean. 1999. Common blossom bats (Syconycteris australis) as pollinators in
fragmented Australian tropical rainforest. Biological Conservation 91:201212.
Leclercq, J., C. Gaspar, J.-L. Marchal, C. Verstraeten, and C. Wonville. 1980. Analyse des 1600
premires cartes de lAtlas provisoire des Insectes de Belgique, et premire liste rouge
dInsectes menaces dans la faune belge. Notes fauniques de Gembloux 4:1104.
Lepczyk, C.A. 2005. Integrating published data and citizen science to describe bird diversity
across a landscape. Journal of Applied Ecology 42:672677.
Lepczyk, C.A., A.G. Mertig, and J. Liu. 2004. Landowners and cat predation across rural-tourban landscapes. Biological Conservation 115:191201.
Lepers, E., E.F. Lambin, A.C. Janetos, R. DeFries, F. Achard, N. Ramankutty, and R.J. Scholes.
2005. A synthesis of information on rapid land-cover change for the period 19812000.
Bioscience 55:115124.

244
Lesica, P., and B. McCune. 2004. Decline of arctic-alpine plants at the southern margin
of their range following a decade of climatic warming. Journal of Vegetation Science
15:679690.
Levin, M.D. 1983. Value of bee pollination to U.S. agriculture. Bulletin of the Entomological
Lewis, T. 1973. Thrips: Their Biology, Ecology and Economic Importance. London and New
York: Academic Press.
Lewis, T., ed. 1997. Thrips as Crop Pests. New York: CAB International.
Li, W., K. Wu, X. Wang, G. Wang, and Y. Guo. 2005. Impact of pollen grains from Bt Transgenic corn on the growth and development of Chinese Tussah silkworm, Antheraea pernyi
(Lepidoptera: Saturniidae). Environmental Entomology 34(4):922928(7).
Lilleboe, D. 2000. Californias Sacramento Valley. Sunflower Magazine February. Available
at: http://www.sunflowernsa.com/magazine/details.asp?ID=160&Cat=6. Accessed July
14, 2006.
Lin, S., and G. Bernardello. 1999. Flower structure and reproductive biology in Aspidosperma
quebracho-blanco (Apocynaceae), a tree pollinated by deceit. International Journal of
Plant Sciences 160:869878.
Linslely, E.G. 1958. The ecology of solitary bees. Hilgardia 27:543599.
Lippok, B., and S.S. Renner. 1997 Pollination of Nuphar (Nymphaeaceae) in Europe: flies and
bees rather than Donacia beetles. Plant Systematics and Evolution 207:273283.
Little, K.J., G. Dieringer, and M. Romano. 2005. Pollination ecology, genetic diversity and
selection on nectar spur length in Platanthera lacera (Orchidaceae). Plant Species Biology
20:183190.
Liu, T.P., and M.E. Nasr. 1993. Preventive treatment of tracheal mites, Acarapis woodi (Rennie)
with vegetable oil extender patties in the honey bee, Apis mellifera L. colonies. American
Lodesani, M., and M. Costa. 2005. Limits of chemotherapy in beekeeping: development of
resistance and the problem of residues. Bee World 86(4):102109.
Loper, G.M. 1995. A documented loss of feral bees due to mite infestations in S. Arizona.
Loper, G.M. 1996. Feral colonies and tracheal mites. Bee Culture 124:27.
Loper, G.M. 1997. Over-winter losses of feral honey bee colonies in southern Arizona, 1992
1997. American Bee Journal December:823.
Loper, G.M., D. Sammataro, J. Finley, and J. Cole. 2006. Feral honey bees in Southern Arizona,
10 years after Varroa infestation. American Bee Journal 146:521524.
Losey, J.E., and M. Vaughan. 2006. The economic value of ecological services provided by
insects. Bioscience 56:311323.
Losey, J.E., L.S. Rayor, and M.E. Carter. 1999. Transgenic pollen harms monarch larvae.
Nature 399:214.
Lumkin, D. 2005. Knuckling it through a winter with Varroa. Bee Culture 133:2224.
Lundie, A.E. 1940. The Small Hive Beetle, Aethina tumida. Science Bulletin 220. Union of
South Africa: Department of Agriculture and Forestry. 30 pp.
MacArthur, R.H., and E.O. Wilson. 1967. The Theory of Island Biogeography. Princeton:
Princeton University Press.
MacDonald, O.C., I. Meakin, and D.M. Richardson. 2003. The role and impact of the regulator in resistance management. Pp. 703708 in the BCPC International Congress: Crop
Science and Technology, Volumes 1 and 2. Proceedings of an International Congress held
at the SECC, Glasgow, Scotland, UK, November 1012, 2003.
Macedo, P.A., M.D. Ellis, and B.D. Siegfried. 2002. Detection and quantification of fluvalinate
resistance in Varroa mites in Nebraska. American Bee Journal 142:523526.
Macfarlane, R.P., K.D. Patten, L.A. Royce, B.K.W. Wyatt, and D.F. Mayer. 1994. Management
potential of sixteen North American bumble bee species. Melanderia 50:112.

REFERENCES
245
Macfarlane, R.P., J.J. Lipa, and H.J. Liu. 1995. Bumble bee pathogens and internal enemies.
Bee World 76:130148.
Machado, C.A., E.A. Herre, S. McCafferty, and E. Bermingham. 1996. Molecular phylogenies
of fig pollinating and non-pollinating wasps and the implications for the origin an devolution of the fig-fig wasp mutualism. Journal of Biogeography 23:531542.
Machado, C.A., N. Robbins, M.P.T. Gilbert, and E.A. Herre. 2005. Critical review of host
specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proceedings
of the National Academy of Sciences USA 102(Suppl 1):65586565.
MacKenzie, K.E. 1997. Pollination requirements of three highbush blueberry (Vaccinium
corymbosum L.) cultivars. Journal of the American Society for Horticultural Science
122(6):891896.
MacKenzie, K.E., E. Eickwort, and C. George. 1996. Diversity and abundance of bees (Hymenoptera: Apoidea) foraging on highbush blueberry (Vaccinium corymbosum L.) in Central
New York. Journal of the Kansas Entomological Society 69(4):185194.
MacKenzie, K.E., S. Javorek, and K.W. Richards. 1997. The potential of alfalfa leafcutter bees
(Megachile rotundata L.) as pollinators of cranberry (Vaccinium macrocarpon Aiton).
Acta Horticulturae (437):345351.
Mackie, W.W., and F.L. Smith. 1935. Evidence of field hybridization in beans. American Society
of Agronomy Journal 27:903909.
Maeta, Y. 1990. Utilization of wild bees. Farming Japan 24(6):1322.
Maeta, Y., and T. Kitamura. 1981. Pollinating efficiency of Osmia cornifrons in relation to the
number of bees required for economic fruit production. Honeybee Science 2(2):6572.
Maeta, Y., K. Goukon, and T. Tezuka. 1993. Utilization of Osmia cornifrons as a pollinator
of Japanese pears (Hymenoptera, Megachilidae). Chugoku Kontyu (7):112.
Magurran, A.E. 1988. Ecological Diversity and Its Measurement. Princeton: Princeton University Press.
Magurran, A.E. 2004. Measuring Biological Diversity. Malden, Mass.: Blackwell Publishers.
Mainland, D.M., and P. Eck. 1968. Induced parthenocarpic fruit development in highbush
blueberry. Proceedings of the American Society for Horticultural Science 92:284289.
Malloch, J.R. 1918. Occurrence of a European solitary bee (Andrena wilkella Kirby) in the
eastern United States. Proceedings of the Biological Society of Washington 31:6164.
Malone, L.A., and M.H. Pham-Delgue. 2001. Effects of transgene products on honey bees
(Apis mellifera) and bumblebees (Bombus sp.). Apidologie 32:287304.
Mangum, W.A., and R.W. Brooks. 1997. First records of Megachile (Callomegachile) sculpturalis Smith (Hymenoptera: Megachilidae) in the continental United States. Journal of
the Kansas Entomological Society 70:140142.
Margoluis, R., and N. Salafsky. 1998. Measures of Success: Designing, Managing, and Monitoring Conservation and Development Projects. Washington: Island Press.
Marlin, J.C., and W.E. LaBerge. 2001. The native bee fauna of Carlinville, Illinois, revisited
after 75 years: a case for persistence. Conservation Ecology 5(1):9.
Maroto, J.V., A. Miguel, S. Lopez-Galarza, A. San-Bautista, B. Pascual, J. Alagarda, and J.L.
Guardiola. 2005. Parthenocarpic fruit set in triploid watermelon induced by CPPU and
2,4-D applications. Plant Growth Regulation 45(3):209213.
Matheson, A. 1994. Forage for Bees in an Agricultural Landscape. Cardiff: International
Beekeeper Research Assocation. 75 pp.
Matheson, A. 1995. First documented findings of Varroa jacobsoni outside its presumed
natural range. Apiacta 30:18.
Matheson, A., S.L. Buchmann, C. OToole, P. Westrich, and I.H. Williams, eds. 1996. The
Conservation of Bees. London: Academic Press.
Matsumura, C., J. Yokoyama, and I. Washitani. 2004. Invasion status and potential ecological impacts of an invasive alien bumblebee, Bombus terrestris L. (Hymenoptera: Apidae)
naturalized in Southern Hokkaido, Japan. Global Environmental Research 8:5166.

246
Matton, D.P., N. Nass, A.E. Clarke, and E. Newbigin. 1994. Self-incompatibility: how plants
avoid illegitimate offspring. Proceedings of the National Academy of Sciences USA
91:19921997.
May, R.M. 1999. How many species? Philosophical Transactions of the Royal SocietySeries
B 330:293304.
May, R.M., J.H. Lawton, and N.E. Stork. 1996. Assessing extinction rates. Pp. 124 in Extinction Rates, J.H. Lawton and R.M. May, eds. Oxford: Oxford University Press.
Mayer, D.F., and C.A. Johansen. 2003. The rise and decline of Nomia melanderi (Hymenoptera: Halictidae) as a commercial pollinator for alfalfa seed. Pp. 139149 in For
Nonnative Crops, Whence Pollinators of the Future? K. Strickler and J.H. Cane, eds.
Proceedings, Entomological Society of America. Lanham, Md.: Thomas Say Publications
in Entomology.
Mayfield, M.M., and G.C. Daily. 2005. Countryside biogeography of neotropical herbaceous
and shrubby plants. Ecological Applications 15:423439.
Mayr, E. 1986. Joseph Gottlieb Kreuters contributions to biology. Osiris, 2nd Series
2:135176.
McAlpine, J.F., B.V. Peterson, G.E. Shewell, H.J. Teskey, J.R. Vockeroth, and D.M. Wood, coordinators. 1981, 1987, 1989. Manual of Nearctic Diptera. Volume 1, Research Branch,
Agriculture Canada, Monograph 27, vi + 1674 pp. [1981], volume 2, Research Branch,
Agriculture Canada, Monograph 28, vi + 6751332 pp. [1987], volume 3, Research
Branch, Agriculture Canada, Monograph 32, vi + 13331581 pp. [1989].
McCall, C., and R.B. Primack. 1992. Influence of flower characteristics, weather, time of day,
and season on insect visitation rates in three plant communities. American Journal of
Botany 79:434442.
McDade, L.A., and J.A. Weeks. 2004. Nectar in hummingbird-pollinated neotropical plants I:
patterns of production and variability in 12 species. Biotropica 36:196215.
McGraw, J.B., and M.A. Furedi. 2005. Deer browsing and population viability of a forest
understory plant. Science 307(5711):920922.
McGregor, S.E. 1976. Insect Pollination of Cultivated Crop Plants. USDA Handbook 496.
Washington: U.S. Department of Agriculture, Agricultural Research Service. 411 pp.
McKay, J.K., C.E. Christian, S. Harrison, and K.J. Rice. 2005. How local is local?a review
of practical and conceptual issues in the genetics of restoration. Restoration Ecology
13:432440.
McKenna, D.D., K.M. McKenna, S.B. Malcolm, and M.R. Berenbaum. 2001. Roadkill Lepidoptera: implications of roadways, roadsikes, and traffic rates for the mortality of butterflies in central Illinois. Journal of the Lepidopterists Society 55(2):6368.
McLaughlin, J.F., J.J. Hellmanndagger, C.L. Boggs, and P.R. Ehrlich. 2002. Climate change
hastens population extinctions. Proceedings of the National Academy of Sciences USA
99:60706074.
Medelln, R.A. 2003. Diversity and conservation of bats in Mxico: research priorities, strategies, and actions. Wildlife Society Bulletin 31:8797.
Medelln, R.A., H.T. Arita, and O. Sanchez. 1997. Identificacin de los murcilagos de Mxico.
Clave de campo. Asociacin Mexicana de Mastozoologa, A.C. Publicaciones Especiales
Nm. 2. Mexico City.
Medelln, R.A., J. Guillermo Tllez, and J. Arroyo. 2004. Conservation through research and
education: an example of collaborative integral actions for migratory bats. Pp. 4358 in
Conservation of Migratory Pollinators and Their Nectar Corridors in North America,
G. Nabhan, R.C. Brusca, and L. Holter, eds. ArizonaSonora Desert Museum, Natural
History of the Sonoran Desert Region, No. 2. Tucson: University of Arizona Press.
Memmott, J. 1999. The structure of a plant-pollinator food web. Ecology Letters
2:276280.

REFERENCES
247
Memmott, J., N.M. Waser, and M.V. Price. 2004. Tolerance of pollination networks to species
extinctions. Proceedings of the Royal Society of London Series BBiological Sciences
271:26052611.
Mezzetti, B., L. Landi, L. Scortichini, A. Rebori, A. Spena, and T. Pandolfini. 2002a. Genetic
engineering of parthenocarpic fruit development in strawberry. Acta Horticulturae
567(1):101104.
Mezzetti, B., L. Landi, A. Spena, R.M. Brennan, S.L. Gordon, and B. Williamson. 2002b.
Biotechnology for improving Rubus production and quality. Acta Horticulturae
(585):7378.
Mezzetti, B., L. Landi, T. Pandolfini, and A. Spena. 2004. The defH9-iaaM auxin-synthesizing
gene increases plant fecundity and fruit production in strawberry and raspberry. BMC
Biotechnology 4(March 15):4.
Michener, C.D. 1969. Comparative social behavior of bees. Annual Review of Entomology
14:299342.
Michener, C.D. 1974. The Social Behavior of the Bees: A Comparative Study. Cambridge,
Mass.: Belknap Press.
Michener, C.D. 2000. Bees of the World. Baltimore and London: The Johns Hopkins University
Press. 913 pp.
Michez, D., M. Terzo, and P. Rasmont, 2004a. Rvision des espces oust-palarctiques du
genre Dasypoda Latreille 1802 (Hymenoptera, Apoidea, Melittidae). Linzer Biologische
Beitrage 36(2):847900.
Michez, D., P. Patiny, and S. Iserbyt. 2004b. Apoidea remarquables observs dans les PyrnesOrientales, France (Hymenoptera, Andrenidae et Melittidae). Bulletin de la Socit entomologique de France 109(4):379382.
Mickleburgh, S.P., A.M. Hutson, and P.A. Racey. 2002. A review of the global conservation
status of bats. Oryx 36:1834.
Milani, N., and G. Della Vedova. 1996. Determination of the LC50 in the mite Varroa
jacobsoni of the active substances in Perizin and Cekafix. Apidologie 27:175184.
Millennium Ecosystem Assessment. 2005. Ecosystems and Human Well-Being: Biodiversity
Synthesis. Washington: World Resources Institute.
Miller, S.E., V.O. Becker, and R. Velez-Angel. 1995. Podalia bolivari (Lepidoptera: Megalopygidae): a highly sexually dimorphic neotropical pest. Proceedings of the Entomological
Society of Washington 97:117122.
Minckley, R.L., and S.G. Reyes. 1996. Capture of the orchid bee, Eulaema polychroma, (Friese)
(Apidae: Euglossini) in Arizona, with notes on northern distributions of other Mesoamerican bees. Journal of the Kansas Entomological Society 62(1):102104.
Mineau, P., C.M. Downes, D.A. Kirk, E. Bayne, and M. Csizy. 2005. Patterns of bird species
abundance in relation to granular insecticide use in the Canadian prairies. Ecoscience
12:267278.
Minorsky, P.V. 2001. The hot and the classic. Plant Physiology 127:709710.
Miriti, M.N., S.J. Wright, and H.F. Howe. 2001. The effects of neighbors on a dominant desert
shrub (Ambrosia dumosa). Ecological Monographs 71(4):491509.
Mississippi State University Extension Service. 2006. 2002 Annual Report of Mississippi State
University Extension Service. Available at: http://msucares.com/pubs/misc/m1281.html.
Accessed January 2006.
Mitchell, T.B. 1962. Bees of the eastern United States, Volume 2. North Carolina Agricultural
Experiment Station Technical Bulletin 152.
Moeller, D.A. 2004. Facilitative interactions among plants via shared pollinators. Ecology
85:32893301.
Molnar, S. 2004. Plant Reproductive Systems. Available at: http://www.geocities.com/we_
evolve/Plants/breeding_sys.html. Accessed March 10, 2006.

248
Mora, J.M., V.V. Mendez, and L.D Gomez. 1999. White-nosed coati Nasua narica (Carnivora:
Procyonidae) as a potential pollinator of Ochroma pyramidale (Bombacaceae). Revista
de Biologia Tropical 47:719721.
Morandin, L.A., and M.L. Winston. 2003. Effects of novel pesticides on bumble bee (Hymenoptera: Apidae) colony health and foraging ability. Environmental Entomology
32(3):555563.
Morandin, L.A., and M.L. Winston. 2005. Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecological Applications 15:871881.
Morandin, L.A., and M.L. Winston. 2006. Pollinators provide economic incentive to
preserve natural land in agroecosystems. Agriculture Ecosystems and Environment
116:289292.
Morandin, L.A., T.M. Laverty, P.G. Kevan, S. Khosla, and L. Shipp. 2001. Bumble bee (Hymenoptera: Apidae) activity and loss in commercial greenhouses. Canadian Entomologist
133:883893.
Morandin, L.A., M.L. Winston, M.T. Franklin, and V.A. Abbott. 2005. Lethal and sub-lethal
effects of spinosad on bumble bees (Bombus impatiens Cresson). Pest Management Science 61(7):619628.
Moreno, A. 1997. Murcielagos de Nuevo Leon. Grupo IMSA, Monterrey, Mexico.
Moreno-Valdez, A., R.L. Honeycutt, and W.E. Grant. 2004. Colony dynamics of Leptonycteris
nivalis (Mexican long-nosed bat) related to flowering agave in Northern Mexico. Journal
of Mammalogy 85:453459.
Moritz, R.F.A. 1985. Heritability of the postcapping stage in Apis mellifera and its relation to
Varroatosis resistance. Journal of Heredity 76:267270.
Moritz, R.F.A., and H. Hanel. 1984. Restricted development of the parasitic mite Varroa
jacobsoni Oud. in the cape honeybee Apis mellifera capensis Esch. Zeitschrift fr
Angewandte Entomologie. 97:9195.
Morris, W.F. 2003. Which mutualists are most essential? Buffering of plant reproduction
against the extinction of pollinators. P. 427 in The Importance of Species: Perspectives
on Expendability and Triage, P. Kareiva and S.A. Levin, eds. Princeton: Princeton University Press.
Morrison, L.W. 2002. Island biogeography and metapopulation dynamics of Bahamian ants.
Journal of Biogeography 29:387394.
Morse, R.A., and N.W. Calderone. 2000. The value of honey bees as pollinators of U.S. crops
in 2000. Bee Culture 128(3):115.
Morse, R.A., and K. Flottum. 1997. Honey Bee Pests, Predators, and Diseases. 3rd edition.
Medina, Ohio: The A. I. Root Company. 718 pp.
Morse, R.A., and L.S. Gonalves. 1979. Varroa disease, a threat to world beekeeping. Gleanings in Bee Culture 107:179181.
Morse, R.A. 1994. The New Complete Guide to Beekeeping. Woodstock, Vt.: The Countryman Press.
Mound, L.A. 1997. Biological diversity. Pp. 197215 (Chapter 6) in Thrips as Crop Pests, T.
Lewis, ed. Wallingford: CAB International.
Mller, H. 1869. DeCandolle, Prodromus systematis naturalis regni vegetabilis 16:16.
Mller, H., and F. Delpino. 1869. Application of the Darwinian theory to flowers and the insects
which visit them. Translated by R.L. Packard, 1871. American Naturalist 5:271297.
Muth, M.K., R.R. Rucker, W.N. Thurman, and C-T. Chuang. 2002 The fable of the bees
revisited: causes and consequences of the U.S. honey program. The Journal of Law and
Economics 46:479516 .
NAPPC (North American Pollinator Protection Campaign). 2006. Reducing Risks to Pollinators from Pesticides. Available at: http://www.nappc.org/PesticidesMain.html.
Nabhan, G.P., and S.L. Buchmann. 1996. Pollination services: biodiversitys direct link to world
food stability. In G. Daly, ed. Washington: Ecosystem Services, Island Press.

REFERENCES
249
Nabhan, G.P., R.C. Brusca, and L. Holter, ed. 2004. Conserving migratory pollinators and
nectar corridors in western North America. Tucson: University of Arizona Press.
Nadel, H., J.H. Frank, and R.J. Knight. 1992. Escapees and accomplices: the naturalization of
exotic Ficus and their associated faunas in Florida. Florida Entomologist 75:2938.
Nason, J.D., and J.L. Hamrick. 1997. Reproductive and genetic consequences of forest fragmentation: two case studies of neotropical canopy trees. Journal of Heredity 88:264276.
Nasr, M.E., G.W. Otis, and C.D. Scott-Dupree. 2001. Resistance to Acarapis woodi by honey
bees (Hymenoptera: Apidae): divergent selection and evaluation of selection progress.
National Plant Board. 2005. Annual Meeting, Biloxi, Mississippi, Resolution No. 7; Florida
Department of Agriculture and Consumer ServicesDivision of Plant Industry. Available at: http://www.doacs.state.fl.us/pi/plantinsp/apiary/africanbees.html; Florida Public
Advisory, July 11, 2005.
Neumann, P., and P.J. Elzen. 2004. The biology of the small hive beetle (Aethina tumida,
Coleoptera: Nitidulidae): gaps in our knowledge of an invasive species. Apidologie
35(3):229247.
Neuweiler, G. 2000. Biology of Bats. Oxford: Oxford University Press.
Nilsson, L.A. 1978. Pollination ecology of Epipactis palustris (Orchidaceae). Botaniska Notiser
131:355368.
Niwa, S., H. Iwano, S. Asada, M. Matsuura, and K. Goka. 2004. A microsporidian pathogen
isolated from a colony of the European bumblebee, Bombus terrestris, and infectivity on
Japanese bumblebee. Japanese Journal of Applied Entomology and Zoology 48:6064.
Norman, E.M., and D. Clayton. 1986. Reproductive biology of two Florida pawpaws; Asmina
ovata and A pygmaea. Bulletin of the Torrey Botanical Club 113:1622.
Norton, C. 2005. The price of Californias almond pollinationpart II of two parts. American
Bee Journal 145(5):387389.
Noss, R.F. 1990. Indicators for monitoring biodiversity: a hierarchical approach. Conservation
Biology 4:355364.
Noyes, J.S. 1998. Catalogue of Chalcidoidea of the World. CD-ROM series World Biodiversity
Database. Amsterdam, Netherlands: ETI Biodiversity Centre.
NRC (National Research Council). 1995. Science and the Endangered Species Act. Washington:
National Academy Press.
NRC. 1996. National Science Education Standards. Washington: National Academy Press.
NRC. 2000. The Future Role of Pesticides in U.S. Agriculture. Washington: National Academy
Press.
NRC. 2005. Valuing Ecosystem Services: Toward Better Environmental Decision-Making.
Washington: The National Academies Press.
NRCC (Natural Resource Council Canada). 1981. Pesticide-Pollinator Interactions. NRCC
Report No. 18471. Associate Committee on Scientific Criteria for Environmental Quality.
Ottawa: National Research Council of Canada. 190pp.
NRCS (Natural Resources Conservation Service). North Dakota. 2005. 2005 Conservation
Security Program. Natural Resources Conservation ServiceNorth Dakota, U.S. Department of Agriculture. Available at: http://www.nd.nrcs.usda.gov/programs/CSP/csp_2005.
asp. Accessed December 30, 2005.
NRCS. 2006a. Wildlife Habitat Incentives Program. U.S. Department of Agriculture. Available
at: http://www.nrcs.usda.gov/programs/whip/. Accessed March 10, 2006.
NRCS. 2006b. Environmental Quality Incentives Program. U.S. Department of Agriculture.
Available at: http://www.nrcs.usda.gov/programs/eqip/. Accessed March 10, 2006.
NRCS. 2006c. Conservation Security Program. U.S. Department of Agriculture. Available at:
http://www.nrcs.usda.gov/programs/csp/. Accessed March 10, 2006.

250
Oberhauser, K., M.D. Prysby, H.R. Mattila, D.E. Stanley-Horn, M.K. Sears, G. Dively, E.
Olson, J.M. Pleasants, W.-K.F. Lam, and R.L. Hellmich. 2001. Temporal and spatial
overlap between monarch larvae and corn pollen. Proceedings of the National Academy
of Sciences USA 98:1191311918.
OBrien, J.M., M.L. Rosenzweig, J.H. Thorne, and A.M. Shapiro. Forthcoming (in revision).
A cryptic decline of butterfly species diversity near Davis, California. Diversity and
Distributions.
OBrien, T.G., and M.F. Kinnaird. 2003. Caffeine and conservation. Science 300:587.
OCallaghan, M., T.R. Glare, E.P.J. Burgess, and L.A. Malone. 2005. Effects on plants genetically modified for insect resistance on nontarget organisms. Annual Review of Entomology 50:271292.
Oldroyd, B.P., and S. Wongsiri. 2006. Asian Honey Bees: Biology, Conservation, and Human
Interactions. Cambridge, Mass.: Harvard University Press.
Olesen, J.M., and S.K. Jain. 1994. Fragmented plant populations and their lost interactions.
Pp. 417426 in Conservation Genetics, V. Loeschcke, J. Tomiuk, and S.K. Jain, eds. Basel,
Switzerland: Birkhauser Verlag.
ONeill, K.M., H.E. Evans, and L.B. Bjostad. 1991. Territorial behaviour in males of three
North American species of bumble bees (Hymenoptera: Apidae, Bombus). Canadian
Journal of Zoology 69:604613.
Ornelas, J.F. 2000. Apodiformes: Trochilidae. Pp. 252262 in Las Aves de Mxico en Peligro
de Extincin, G. Ceballos y L. Mrquez Valdelamar, eds. UNAM, CONABIO, Fondo de
Cultura Econmica, Mxico, D.F.
Ornelas, J.F., M. Ordano, A. Hernandez, J.C. Lopez, L. Mendoza, and Y. Perroni. 2002.
Nectar oasis produced by Agave marmorata Roezl. (Agavaceae) lead to spatial and temporal segregation among nectarivores in the Tehuacan Valley, Mexico. Journal of Arid
Environments 52:3751.
Ortega-Rivas, C., and R. Ochoa-Bautista. 2004. La produccion de miel en Mexico: Modernidad
y Tradicion. Claridades Agropecuarias 128:313. Available at: http://www.infoaserca.
gob.mx/claridades/revistas/128/ca128.pdf. Accessed March 6, 2006.
Otis, G.W. 1990. Results of a survey on the economic impact of tracheal mites. American Bee
Journal 130:2831.
OToole, C. 1993. Diversity of native bees and agroecosystems. Pp. 69106 in Hymenoptera
and Biodiversity, J. LaSalle and I. Gauld, eds. Wallingford: CAB International.
OToole, C. 1994. Who cares for solitary bees? Pp. 4756 in Forage for Bees in an Agricultural
Landscape, A. Matheson, ed. Cardiff: International Bee Research Association.
OToole, C., ed. 2002. The New Encyclopedia of Insects and their Allies. Oxford: Oxford
University Press. 240 pp.
OToole, C., and A. Raw. 1991. Bees of the World. London: Blandford Publishing, 191pp.
Otterstatter, M.C., R.J. Gegear, S.R. Colla, and J.D. Thomson. 2005. Effects of parasitic mites
and protozoa on the flower constancy and foraging rate of bumble bees. Behavioral Ecology and Sociobiology 58:383389.
Oudemans, A.C. 1904. Acarological notes xiii. Entomologische berichten uitgegeven door de.
Nederlandsche Entomologische Vereeniging 1:169174.
Page, R.E., Jr., and N.E. Gary. 1990. Genotypic variation in susceptibility of honey bees (Apis
mellifera) to infestation by tracheal mites (Acarapis woodi). Experimental and Applied
Acarology 8:275283.
Page, R.E., Jr., and H.H. Laidlaw, Jr. 1982a. Closed population honeybee breeding. I. Population genetics of sex determination. Journal of Apicultural Research 21:3037.
Page, R.E., Jr., and H.H. Laidlaw, Jr. 1982b. Closed population honeybee breeding. II. Comparative methods of stock maintenance and selective breeding. Journal of Apicultural
Research 21:3844.

REFERENCES
251
Page, R.E., Jr., and H.H. Laidlaw, Jr. 1992. Honey bee genetics and breeding. Pp. 235267 in
The Hive and the Honey Bee. Hamilton, Ill.: Dadant and Sons.
Page, R.E., Jr., H.H. Laidlaw, Jr., and E.H. Erickson, Jr. 1983. Closed population honeybee
breeding 3. The distribution of sex alleles with gyne supersedure. Journal of Apicultural
Research 22:184190.
Page, R.E., Jr., H.H. Laidlaw, Jr., and E.H. Erickson, Jr. 1985. Closed population honeybee
breeding 4. The distribution of sex alleles with top crossing. Journal of Apicultural Research 24:3842.
Pagnotta, M.A. 1999. Genetic engineering of parthenocarpic vegetable crops. Pp. 301306
in Genetics and Breeding for Crop Quality and Resistance, Proceedings of the XV EUCARPIA Congress, Viterbo, Italy, September 2025, 1998. Dordrecht, Germany: Kluwer
Academic Publishers.
Pankiw, T. 2004. Brood pheromone regulates foraging activity of honey bees (Hymenoptera:
Apidae). Journal of Economic Entomology 97(3):748751.
Park, O.W. 1936. Disease resistance and American foulbrood. American Bee Journal
76:1215.
Park, O.W., F.C. Pellett, and F.B. Paddock. 1937. Disease resistance and American foulbrood.
Results of 2nd season of cooperative experiment. American Bee Journal 77(34):2025.
Park, O.W., F.C. Pellett, and F.B. Paddock. 1939. Results of Iowas 19371938 honeybee
disease resistance program. American Bee Journal 79:577582.
Parker, F.D. 1981. How efficient are bees in pollinating sunflowers? Journal of the Kansas
Parmesan, C., N. Ryrholm, C. Stefanescu, J.K. Hill, C.D. Thomas, H. Descimon, B. Huntley,
L. Kaila, J. Kullberg, T. Tammaru, W.J. Tennent, J.A. Thomas, and M. Warren. 1999.
Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579583.
Patiny, S. 1998. Contribution la connaissance de la rgression des populations du sous-genre
Taeniandrena Hedicke 1933 (Hym., Andrenidae, Andrena) et leurs habitudes pollinisatrices. Notes fauniques de Gembloux 35:2033.
Patiny, S., and C. Gaspar. 2000. Biogographie des Melitturga Latreille 1809, Meliturgula
Friese, 1903 et des genres proches (Hymenoptera: Andrenidae, Panurginae). Notes fauniques de Gembloux 39:344.
Paton, D.C. 1990. Budgets for the use of floral resources in mallee heath. Pp. 189193 in The
Mallee Lands: A Conservation Perspective, J.C. Noble, P.J. Joss and G.K. Jones, eds.
Melbourne: CSIRO.
Paton, D.C. 1993. Honeybees Apis mellifera in the Australian environment. Does Apis mellifera
disrupt or benefit native biota? Bioscience 43:95103.
Paton, D.C. 1996. Overview of Feral and Managed Honeybees in Australia: Distribution,
Abundance, Extent of Interactions with Native Biota, Evidence of Impacts and Future
Research. Canberra: Australian Nature Conservation Agency. Available at: http://www.
deh.gov.au/biodiversity/invasive/publications/bees/introduction.html. Accessed May 22,
2006.
Paton, D.C., L. Jansen, and D. Oliver. 1992. Interactions between honeybees and Australian
biota on Kangaroo Island.
Pauly, A. 1999. Catalogue des Hymnoptres Aculates de Belgique. Bulletin de la Socit
royale belge dEntomologie 135:98125.
Pauly, A., R.W. Brooks, L.A. Nilsson, Y.A. Pesenko, C.D. Eardley, M. Terzo, T. Griswold,
M. Schwarz, S. Patiny, J. Munzinger, and Y. Barbier. 2001. Hymenoptera Apoidea de
Madagascar et des les voisines. Annales du Muse royal de lAfrique centrale (Sciences
Zoologiques), Tervuren (Belgique) 286:1406.

252
Peakall, R., S.N. Handel, and A.J. Beattie. 1991. The evidence for, and importance of, ant
pollination. Pp. 421429 in Ant-Plant Interactions, C.R. Huxley and D.F. Cutler, eds.
Oxford: Oxford University Press.
Pearson, D.L., and R.L. Dressler. 1985. Two-year study of male orchid bee (Hymenoptera:
Apidae: Euglossini) attraction to chemical baits in lowland south-eastern Peru. Journal
of Tropical Ecology 1:3754.
Pellmyr, O. 2003. Yuccas, yucca moths, and coevolution: a review. Annals of the Missouri
Botanical Garden 90:3555.
Pellmyr, O., J.N. Thompson, J.M. Brown, and R.G. Harrison. 1996. Evolution of pollination
and mutualism in the yucca moth lineage. American Naturalist 148:827847.
Peuelas, J., I. Filella, and P. Comas. 2002. Changed plant and animal life cycles from 1952
2000 in the Mediterranean region. Global Change Biology 8:531544.
Peterson, S.S., C.R. Baird, and R.M. Bitner, 1992. Current status of the alfalfa leafcutting bee,
Megachile rotundata, as a pollinator of alfalfa seed. Bee Science 3:135142.
Pettis, J.S., and H. Shimanuki. 1999. A hive modification to reduce varroa populations. American Bee Journal 139:471473.
Pettis, J.S., W.T. Wilson, F.A. Eischen, and A. Suarez. 1987. Distribution of Acarapis woodi
among rustic and modern honey bee hives in northeast Mexico. American Bee Journal
127(12):849.
Pettis, J.S., A.M. Collins, R. Wilbanks, and M.F. Feldlaufer. 2004. Effects of coumaphos on
queen rearing in the honey bee, Apis mellifera. Apidologie 35:605610.
Pham-Delgue, M.-.H, A. Decourtye, L. Kaiser, and J. Devillers. 2002. Behavioural methods
to assess the effects of pesticides on honey bees. Apidologie 33:425432.
Phillips, J.R., J.B. Graves, and R.G. Luttrell. 1989. Insecticide resistance management: relationship to integrated pest management. Pesticide Science 27(4):459464.
Picket, C.H., and R.L. Bugg. 1998. Introduction: enhancing biological control-habitat management to promote natural enemies of agricultural pests. Pp. 124 in Enhancing Biological
Control, C.H. Picket and R.L. Bugg, eds. Berkeley: University of California Press.
Pickett, S.T.A., and P.S. White. 1985. Natural disturbance and patch dynamics: an introduction.
Pp. 313 in The Ecology of Natural Disturbance and Patch Dynamics, S.T.A. Pickett and
P.S. White, eds. Orlando: Academic Press.
Pierson, E.D. 1998. Tall trees, deep holes, and scarred landscapes: conservation biology of
North American bats. Pp. 309325 in Bats: Phylogeny, Morphology, Echolocation, and
Conservation Biology, T.H. Kunz and P.A. Racey, eds. Washington: Smithsonian Institution Press.
Pimm, S.L., M.P. Moulton, and L.J. Justice. 1994. Bird extinctions in the central Pacific.
Philosophical Transactions of the Royal Society of London Series BBiological Sciences
344:2733.
Pleasants, J.M., R.L. Hellmich, G. Dively, M.K. Sears, D.E. Stanley-Horn, H.R. Mattila, J.E.
Foster, P.L. Clark, and G.D. Jones. 2001. Corn pollen deposition on milkweeds in and near
cornfields. Proceedings of Natlional Academy of Sciences USA 98(21):1191911924.
Plowright, C. 1996. Bumble bee rearing. Melissa 9:1012.
Plowright, R.C., B.A. Pendrel, and I.A. McLaren, 1978. The impact of aerial fenitrothion spraying upon the population biology of bumble bees (Bombus Latr.: Hym.) in south western
New Brunswick. Canadian Entomologist 110(11):11451156.
Pollack, S., and A. Perez. 2005. Fruit and Tree Nuts Situation and Outlook Yearbook. FTS
2005. Washington: U.S. Department of Agriculture, Economic Research Service. Available
at: http://www.ers.usda.gov/publications/so/view.asp?f=/specialty/fts-bb/.
Potts, S.G., P. Willmer, A. Dafni, and G. Neeman. 2001. The utility of fundamental ecological
research of plant-pollinator interactions as the basis for landscape management practices.
VIII International Symposium on PollinationPollination: Integrator of Crops and
Native Plant Systems. ISHS Acta Horticulturae 561:141144.

REFERENCES
253
Potts, S.G., B. Vulliamy, A. Dafni, G. Neeman, C. OToole, S. Roberts, and P.G. Willmer. 2003.
Response of plant-pollinator communities following fire: changes in diversity, abundance
and reward structure. Oikos 101:103112.
Potts, S.G., P.G. Kevan, and J.W. Boone. 2005. Conservation in pollination: collecting, surveying and monitoring. Pp. 401434 in Pollination Ecology: A Practical Approach, A. Dafni
and P. Kevan, eds. Cambridge, Canada: Enviroquest.
Potts, S.G., R.B. Bradbury, S.R. Mortimer, and B.A. Woodcock. 2006. Commentary on Kleijn
et al., 2006, Ecology Letters 9(3):254256.
Powell, J.A. 1992. Interrelationships of yuccas and yucca moths. Trends in Ecology and Evolution 7:1015.
Powell, J.A., C. Mitter, and B.D. Farrell. 1998. Evolution of larval food preferences in Lepidoptera. Pp. 403422 in Handbook of Zoology, Part 35, Vol. 1. Evolution, Systematics
and Biogeography, N. Kristensen, ed. New York: de Gruyter.
Power, A.G., and C.E. Mitchell. 2004. Pathogen spillover in disease epidemics. American
Prescott-Allen, C., and R. Prescott-Allen. 1986. The First Resource: Wild Species in the North
American Economy. New Haven: Yale University Press.
Prescott-Allen, R., and C. Prescott-Allen. 1990. How many plants feed the world? Conservation Biology 4:365374.
Price, M.V., N.M. Waser, R.E. Irwin, D.R. Campbell, and A.K. Brody. 2005. Temporal and
spatial variation in pollination of a montane herb: a seven-year study. Ecology 86:2106
2116 (B-56).
Primack, D., C. Imbres, R.B. Primack, A.J. Miller-Rushing, and P. Del Tredici. 2004. Herbarium specimens demonstrate earlier flowering times in response to warming in Boston.
Procter, W. 1946. Biological Survey of the Mount Desert Region. Part VII. The Insect Fauna
with Reference to Methods of Capture, Food Plants, the Flora and Other Biological
Factors. Philadelphia: Wistar Institute, 566 pp.
Proctor, M., P. Yeo, and A. Lack. 1996. The Natural History of Pollination. Portland: Timber
Press.
Prys-Jones, O.E., and S.A. Corbet. 1987. Bumblebees. Cambridge: Cambridge University
Press.
Puterbaugh, M.N. 1998. The roles of ants as flower visitors: experimental analysis in three
alpine species. Oikos 83:3646.
Pyke, G.H., and N.M. Waser. 1981. The production of dilute nectars by hummingbird and
honeyeater flowers. Biotropica 13:260270.
Pywell, R.F., E.A. Warman, T.H. Sparks, J.N. Greatorex-Davis, K.J. Walker, W.R. Meek, C.
Carvell, S. Petit, and L.G. Firbank. 2004. Assessing habitat quality for butterflies on
intensively managed farmland. Biological Conservation 118:313325.
Pywell, R.F., E.A. Warman, C. Carvell, T.H. Sparks, L.V. Dicks, D. Bennett, A. Wright, C.N.R.
Critchley, and A. Sherwood. 2005. Providing foraging resources for bumblebees in intensively farmed landscapes. Biological Conservation 121:479494.
Pywell, R.F., E.A. Warman, L. Hulmes, S. Hulmes, P. Nuttall, T.H. Sparks, C.N.R. Critchley,
and A. Sherwood. 2006. Effectiveness of new agri-environment schemes in providing
foraging resources for bumblebees in intensively farmed landscapes. Biological Conservation 129(2):192206.
Quesada, M., K.E. Stoner, V. Rosas-Guerrero, C. Palacios-Guevara, and J.A. Lobo. 2003. Effects of habitat disruption on the activity of nectarivorous bats (Chiroptera: Phyllostomidae) in a dry tropical forest: implications for the reproductive success of the neotropical
tree Ceiba grandiflora. Oecologia 135:400406.

254
Raguso, R.A., C. Henzel, S.L. Buchmann, and G.P. Nabhan. 2003. Trumpet flowers of the
Sonoran Desert: floral biology of Peniocereus cacti and Sacred Datura. International
Journal of Plant Sciences 164:877892.
Ramrez, V. 1998. Inventario revela existencia de 203 millones de plantas. Pp. 163164 in
Foro de Anlisis de la problemtica de la cadena productiva agave tequila. Guadalajara,
Mxico: Consejo Regulador del Tequila.
Rappole, J.H., and M.V. McDonald. 1994. Cause and effect in migratory bird population
changes. Auk 111:652660.
Rasmont, P., and A. Adamski. 1995. Bumblebees of Corsica (Hymenoptera, Apoidea, Bombinae). Faunal Notes of Gembloux 31:387.
Rasmont, P., and Y. Barbier. 2003. Biodiversit du Maroc. Available at: http://zoologie.umh.
ac.be/marocbiodiv/taxon.asp?parentID=2094&fiche=false.
Rasmont, P., and D. Flagothier, 1996. Biogographie et choix floraux des bourdons (Hymenoptera, Apidae) de la Turquie. Rapport prliminaire O.T.A.N.-N.A.T.O. 19951996.
Universit de Mons-Hainaut, Mons, Belgique, 69 + III pp.
Rasmont, P., and C. Gaspar, eds. 2002. Atlas Hymenoptera. Available at: http://zoologie.umh.
ac.be/hymenoptera/.
Rasmont, P., and P. Mersch. 1988. Premire estimation de la drive faunique chez les bourdons de la Belgique (Hymenoptera: Apidae). Annales de la Socit royale zoologique de
Belgique 118:141147.
Rasmont, P., J. Leclercq, A. Jacob-Remacle, A. Pauly, and C. Gaspar. 1993. The faunistic drift
of Apoidea in Belgium. Pp. 6587 in Bees for Pollination, E. Bruneau, ed. Brussels: Commission of the European Communities. 237 pp.
Rasmont, P., P.A. Ebmer, J. Banaszak, and G. van der Zanden. 1995. Hymenoptera Apoidea
Gallica. Taxonomic list of the bees of France, of Belgium, of Switzerland and the Grand
Duchy of Luxembourg. Bulletin of the Entomological Company of France, 100(excerpt
series):198.
Rasmont, P., A. Pauly, M. Terzo, S. Patiny, D. Michez, S. Iserbyt, Y. Barbier, and E. Haubruge.
2006. The survey of wild bees (Hymenoptera, Apoidea) in Belgium and France. In Status
of the Worlds Pollinators. Rome: Food and Agriculture Organisation of the United
Nations. 18 pp.
Rasmussen, K.K., and J. Kollmann. 2004. Pollen limitation and inbreeding depression in the
rare tree Sorbus torminalis. Acta Oecologica 25:211218.
Rasplus, J.Y., C. Kerdelhu, I. Le Clainche, and G. Mondor. 1998. Molecular phylogeny of fig
waps (Hymenoptera). Agaonidae are not monophyletic. Compte Rendu de lAcadmie
des Sciences de Paris 321:517527.
Rath, W. 1999. Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud. Apidologie
30:97110.
Rathcke, B.J., and E.S. Jules. 1993. Habitat fragmentation and plant-pollinator interactions.
Current Science 65:273277.
Ratnieks, F.L.W. 1992. American foulbrood: the spread and control of an important disease
of the honey bee. Bee World 73:177191.
Rausser, G., and A. Small. 2000. Valuing research leads: bioprospecting and the conservation
of genetic resources. Journal of Political Economy 108(1):173206.
Raven, P.H., R.F. Evert, and S.E. Eichhorn. 2005. Biology of Plants. New York: W.H. Freeman
and Company.
Reid, F.A. 1997. A field guide to the mammals of Central America and southeast Mexico. New
York: Oxford University Press. 334 pp.
Renner, S.S., and K.A. Johanson. 1995. Breeding system and pollination of Nuphar luteum (l.)
Smith (Nymphaeaceae) in Norway. Flora 190:109113.
Rennie, J. 1921. Notes on Acarine disease. Bee World 2:144145.

REFERENCES
255
Riba-Hernandez, P., and K.E. Stoner. 2005. Massive destruction of Symphonia globulifera
(Clusiaceae) flowers by Central American spider monkeys (Ateles geoffroyi). Biotropica
37:274278.
Richards, A.J. 1997. Plant Breeding Systems. 2nd edition. London: Garland Science.
Richards, C.S., M.P. Hill, and J.F. Dames. 2005. The susceptibility of small hive beetle (Aethina
tumida Murray) pupae to Aspergillus niger (van Tieghem) and A. flavus (Link:Grey).
Richards, K.W. 2003. Potential use of the alfalfa leafcutter bee Megachile rotundata to pollinate
sweet clover. Journal of Apicultural Research 42(1/2):2124.
Richards, O.W. 1963. The Species of Pseudomasaris Ashmead. Berkeley: University of California Press. 28 pp.
Richards, O.W. 1966. New Records of Pseudomasaris Ashmead (Hymenoptera: Vespoidea,
Masaridae), with notes on P. phaceliae Rohwer and P. cazieri R.M. Bohart. Proceedings
of the Royal Society of London Series BBiological Sciences 35:4755.
Richardson, D.M., R.M. Cowling, and B.B. Lamont. 1996. Non-linearities, synergisms and
plant extinctions in South African fynbos and Australian kwongan. Biodiversity Conservation 5(9):10351046.
Ricketts, T.H. 2001. The matrix matters: effective isolation in fragmented landscapes. American Naturalist 158:8799.
Ricketts, T.H. 2004. Tropical forest fragments enhance pollinator activity in nearby coffee
crops. Conservation Biology 18:12621271.
Ricketts, T.H., E. Dinerstein, D.M. Olson, C.J. Loucks, W. Eichbaum, D. DellaSala, K. Kavanagh, P. Hedao, P.T. Hurley, K.M. Carney, R. Abell, and S. Walters. 1999. Terrestrial
Ecoregions of North America: A Conservation Assessment. Washington: Island Press.
Ricketts, T.H., G.C. Daily, P.R. Ehrlich, and C.D. Michener. 2004. Economic value of tropical forest to coffee production. Proceedings of the National Academy of Sciences USA
101:1257912582.
Rico-Gray, V., and P.S. Oliveira. 2006. Ecology of Ant-Plant Interactions. Chicago: University
of Chicago Press.
Rinderer, T.E. 1986. Africanized bees: the Africanization process and potential range in the
United States. Bulletin of the Entomological Society of America Winter:222227.
Rinderer, T.E., L.I. de Guzman, V.A. Lancaster, G.T. Delatte, and A. Stelzer. 1999. Varroa in
the mating yard: I. The effects of Varroa jocobsoni and Apistan on drone honey bees.
Rinderer, T.E., L.I. de Guzman, G.T. Delatte, J.A. Stelzer, V.A. Lancaster, V. Kuznetsov,
L. Beaman, R. Watts, and J.W. Harris. 2001. Resistance to the parasitic mite Varroa
destructor in honey bees from far-eastern Russia. Apidologie 32:381394.
Rinderer, T.E., L.I. de Guzman, G.T. Delatte, and C. Harper. 2003. An evaluation of ARS
Russian honey bees in combination with other methods for the control of varroa mites.
Rinderer, T.E., L.I. de Guzman, and R. Danka. 2005. A new phase begins for the USDA-ARS
Russian Honey Bee Breeding Program. American Bee Journal 145:579582.
Robbins, C.S., J.R. Sauer, R.S. Greenberg, and S. Droege. 1989. Population declines in North
American birds that migrate to the neotropics. Proceedings of the National Academy of
Sciences USA 86(19):76587662.
Roberts, D.L., R.J. Cooper, and L.J. Petit. 2000. Use of premontane moist forest and shade coffee
agroecosystems by army ants in western Panama. Conservation Biology 14:192199.
Roberts, R.B. 1978. The nesting biology, behavior and immature stages of Lithurge chrysurus,
an adventitious wood-boring bee in New Jersey (Hymenoptera: Megachilidae). Journal
of Kansas Entomological Society 51:735745.
Robertson, A.W., D. Kelly, J.J. Ladley, and A.D. Sparrow. 1999. Effects of pollinator loss on
endemic New Zealand mistletoes (Loranthaceae). Conservation Biology 13:499508.

256
Robertson, C. 1929. Flowers and Insects. Lists of Visitors to Four Hundred and Fifty-Three
Flowers. Lancaster, Pa.: Science Press Printing Company.
Robinson, G.E. 1992. The regulation of division of labor in insect societies. Annual Review
of Entomology 37:637665.
Robinson, G.E., and F.L.W. Ratnieks. 1987. Induction of premature honey bee (Hymenoptera:
Apidae) flight by juvenile hormone analogs administered orally or topically. Journal of
Economic Entomology. 80:784787.
Robinson, G.E., C.M. Grozinger, and C.W. Whitfield. 2005. Sociogenomics: social life in
molecular terms. Nature Reviews Genetics 6:257270.
Robinson, W.S., R. Nowogrodzki, and R.A. Morse. 1989a. The value of honey bees as pollinators of U.S. crops. Part I of a two-part series. American Bee Journal 129:411423.
Robinson, W.S., R. Nowogrodzki, and R.A. Morse. 1989b. The value of honey bees as pollinators of U.S. crops. Part II of a two-part series. American Bee Journal 129:477487.
Rocha, M., A. Valera, and L.E. Eguiarte. 2005. Reproductive ecology of five sympatric
Agave littaea (Agavaceae) species in Central Mexico. American Journal of Botany
92:3301341.
Rodman, J.E., and J.H. Cody. 2003. The taxonomic impediment overcome: NSFs partnerships for enhancing expertise in taxonomy (PEET) as a model. Systematic Biology
52:428435.
Rogg, K.A., O.R. Taylor, and D.L. Gibo. 1999. Mark and recapture during the monarch
migration: a preliminary analysis. Pp. 133138 in 1997 North American Conference on
the Monarch butterfly, J. Hoth, L. Merino, L. Oberhauser, I. Piscanty, S. Price, and T.
Wilkinson, eds. Quebec: Commission for Environmental Cooperation.
Rothenbuhler, W.C. 1964. Behavioral genetics of nest cleaning in the honeybee. I. Response of
four inbred lines to disease-killed brood. Animal Behavior 4:578583.
Rotino, G.L., E. Perri, M. Zottini, H. Sommer, and A. Spena. 1997. Genetic engineering of
parthenocarpic plants. Nature Biotechnology 15(13):13981401.
Roubik, D.W. 1978. Competitive interactions between neotropical pollinators and Africanized
honey bees. Science 201:10301032.
Roubik, D.W. 1980. Foraging behavior of competing africanized honeybees and stingless bees.
Ecology 61(4):836845.
Roubik, D.W. 1983. Experimental community studies: Timeseries tests of competition between African and Neotropical bees. Ecology 64:971987.
Roubik, D.W. 1989. Ecology and Natural History of Tropical Bees. New York: Cambridge
University Press.
Roubik, D.W., ed. 1995. Pollination of Cultivated Plants in the Tropics. Food and Agriculture
Organization Agricultural Services Bulletin 118. 196 pp.
Roubik, D.W. 2001. Ups and downs in pollinator populations: when is there a decline? Conservation Ecology 5(1):2.
Roubik, D.W. 2002. The value of bees to the coffee harvest. Nature 417:708.
Roubik, D.W., and P.E. Hanson. 2004. Orchid Bees of Tropical America: Biology and Field
Guide. Heredia, Costa Rica: INBIO.
Roubik, D.W., and H. Wolda. 2001. Do competing honey bees matter? Dynamics and
abundance of native bees before and after honey bee invasion. Population Ecology
43(1):5362.
Roulston, T.H., and J.H. Cane. 2000. Pollen nutritional content and digestibility for animals.
Plant Systematics and Evolution 222(14):187209.
Roulston, T.H., J.H. Cane, and S.L. Buchmann. 2000. What governs the protein content of
pollen grains: pollinator preferences, pollen-pistil interactions, or phylogeny? Ecological
Monographs 70:617643.
Roy, D.B., and T.H. Sparks. 2000. Phenology of British butterflies and climate change. Global
Change Biology 6:407416.

REFERENCES
257
Roy, D.B., P. Rothery, D. Moss, E. Pollard, and J.A. Thomas. 2001. Butterfly numbers and
weather: predicting historical trends in abundance and the future effects of climate change.
Journal of Animal Ecology 70(2):201217.
Roy, D.B., D.A. Bohan, A.J. Haughton, M.O. Hill, J.L. Osborne, S.J. Clark, J.N. Perry, P.
Rothery, R.J. Scott, D.R. Brooks, G.T. Champion, C. Hawes, M.S. Heard, and L.G.
Firbank. 2003. Invertebrates and vegetation of field margins adjacent to crops subject
to contrasting herbicide regimes in the Farm Scale Evaluations of genetically modified
herbicide-tolerant crops. Philosophical Transactions of the Royal Society of London
BBiological Sciences 358:18791898.
Rucker, R.R., W.N. Thurman, and M. Burgett. 2005. Internalizing Reciprocal Benefits:
The Economics of Honeybee Pollination Markets. North Carolina State University,
Department of Agricultural and Resource Economics, Raleigh, NC, March 6, 2005.
Unpublished manuscript. Available at: http://legacy.ncsu.edu:8020/classes/ecg701001/
personal/Internalization_of_Reciprocal_Benefits-full_March_2005.pdf.
Russell, K.N., H. Ikerd, and S. Droege. 2005. The potential conservation value of unmowed
powerline strips for native bees. Biological Conservation 124:133148.
Russell, R.W., F.L. Carpenter, M.A. Hixon, and D.C. Paton. 1994. The impact of variation
in stopover habitat quality on migrant Rufous hummingbirds. Conservation Biology
8:483490.
Rust, R.W. 1974. The systematics and biology of the genus Osmia, subgenera Osmia, Chalcosmia, and Cephalosmia (Hymenoptera: Megachilidae). Wasmann Journal of Biology
32:193.
Saavedra F., D.W. Inouye, M.V. Price, and J. Harte. 2003. Changes in flowering and abundance
of Delphinium nuttallianum (Ranunculaceae) in response to a subalpine climate warming
experience. Global Change Biology 9:885894.
SAGARPA. 2005. Estadisticas: Estimacion de Consumo Nacional Aparente: Miel de Abeja.
Secretaria de Agricultura, Ganaderia, Desarrollo Rural, Pesca y Alimentacion. Available at: http://www.sagarpa.gob.mx/Dgg/CNAmiel.htm (last updated March 16, 2005).
Accessed March 6, 2006.
Sammataro, D., U. Gerson, and G. Needham. 2000. Parasitic mites of honey bees: life history,
implications, and impact. Annual Review of Entomology 45:519548.
Sampson, B.J., and J.H. Cane. 1999. Impact of enhanced ultraviolet-B radiation on flower,
pollen, and nectar production. American Journal of Botany 86:108114.
Sampson, B.J., and J.H. Cane. 2000. Pollination efficiencies of three bee (Hymenoptera:
Apoidea) species visiting rabbiteye blueberry. Journal of Economic Entomology
93(6):17261731.
Sampson, B.J., S.J. Stringer, J.H. Cane, and J.M. Spiers. 2004. Screenhouse evaluations of a
mason bee Osmia ribifloris (Hymenoptera: Megachilidae) as a pollinator for blueberries
in the southeastern United States. Small Fruits Review 3(34):381392.
Srospataki, M., J. Novk, and V. Molnr. 2005. Assessing the threatened status of bumble
bee species (Hymenoptera: Apidae) in Hungary, Central Europe. Biodiversity and Conservation 14:24372446.
Saskatchewan Agriculture and Food. 2004. A brief history of beekeeping in Saskatchewan.
Available at: http://www.agr.gov.sk.ca/docs/crops/apiculture/History_Beekeeping.pdf.
Sauer, J.R., J.E. Hines, and J. Fallon. 2005. The North American Breeding Bird Survey, Results
and Analysis 19662005. Version 6.2.2006. Laurel, Md.: USGS Patuxent Wildlife
Research Center. Available at: http://www.mbr-pwrc.usgs.gov/bbs/bbs2005.html.
Saville, N.M., W.E. Dramstad, G.L.A. Fry, and S.A. Corbet. 1997. Bumblebee movement
in a fragmented agricultural landscape. Agriculture Ecosystems and Environment
61:145154.

258
Schaffer, W.M., D.B. Jenson, D.E. Hobbs, J. Gurevitch, J.R. Todd, and M.V. Schaffer. 1979.
Competition, foraging energetics and the cost of sociality in three species of bees. Ecology 60:976987.
Schaffer, W.M., D.W. Zeh, S.L. Buchmann, S. Kleinhaus, M.V. Schaffer, and J. Antrim. 1983.
Competition for nectar between introduced honeybees and native North American bees
and ants. Ecology 64:564577.
Schell, R. 2005. A big win for beekeepers. American Bee Journal 145:392394.
Schery, R.W. 1972. Plants for Man. 2nd edition. Englewood Cliffs: Prentice-Hall.
Schiff, N.M., and W.S. Sheppard. 1995. Genetic analysis of commercial honey bees (Hymenoptera: Apidae) from the southeastern United States. Journal of Economic Entomology
88(5):12161220.
Schiff, N.M., and W.S. Sheppard. 1996. Genetic differentiation in the queen breeding population of the western United States. Apidologie 27:7786.
Schiff, N.M., W.S. Sheppard, G.R. Loper, and H. Shimanuki. 1994. Genetic diversity of feral
honey bee (Hymenoptera: Apidae) populations in the southern United States. Annals of
the Entomological Society of America 87:842848.
Schlosser, W., K. Blatner, and R. Chapman. 1991. Economic and marketing implications of
special forest products harvest in coastal Pacific Northwest. Western Journal of Applied
Forestry 6:6772.
Schneider, E.L., J. Buchanan, and L.A. Moore. 1977. Morphological studies of the Nymphaeceae VII. The floral biology of Nuphar lutea subsp. macrophylla. Brittonia 29:8899.
Schneider, P. 1986. The influence of Varroa infestation during pupal development on the flight
activity of the worker honey bees. Apidologie 17:366368.
Schneider, P., and W. Drescher. 1987. Einfluss der parasitierung durch die Milbe Varroa jacobsoni Oud. auf da Schlupfgewicht, die Gewichsentwicklung, die Entwicklung der Hypopharynxdrsen und die Levensdauer von Apis mellifera L. Apidologie 18:101110.
Schneider, S.S., G. Degrandi-Hoffman, and D.R. Smith. 2004. The African honey bee: factors contributing to a successful biological invasion. Annual Review of Entomology
49:351376.
Schondube, J.E., S. Contreras-Martinez, I. Ruan-Tejeda, W.A. Calder, and E. Santana. 2004.
Migratory patterns of the rufous hummingbird in western Mexico. Pp. 8095 in Conservation of Migratory Pollinators and Their Nectar Corridors in North America, G. Nabhan, R. C. Brusca, and L. Holter, eds. ArizonaSonora Desert Museum, Natural History
of the Sonoran Desert Region, No. 2. Tucson: University of Arizona Press.
Schulke, B., and N.M. Waser. 2001. Long-distance pollinator flights and pollen dispersal between populations of Delphinium nuttallianum. Oecologia 127:239245.
Schultz, C.B., and K. Dlugosch. 1999. Nectar and hostplant scarcity limit populations of an
endangered Oregon butterfly. Oecologia 119:231238.
Schurch, S., M. Pfunder, and B.A. Roy. 2000. Effects of ants on the reproductive success of
Euphorbia cyparissias and associated pathogenic rust fungi. Oikos 88:612.
Scott, J.A. 1986. Butterflies of North America. Stanford: Stanford University Press. 583 pp.
Scott-Dupree, C.D., and G.W. Otis. 1992. The efficacy of four miticides for the control of
Acarapis woodi (Rennie) in a fall treatment program. Apidologie 23(2):97106.
Scott-Dupree, C.D., and M.L. Winston. 1987. Wild bee pollinator diversity and abundance in
orchard and uncultivated habitats in the Okanagan Valley, British Columbia. Canadian
Entomologist 119:735745.
Scott-Dupree, C.D., M. Winston, G. Hergert, S.C. Jay, D. Nelson, J. Gates, B. Termeer, and G.
Otis, eds. 1995. A Guide to Managing Bees for Crop Pollination. Canadian Association
of Professional Apiculturalists.

REFERENCES
259
Sears, M.K., R.L. Hellmich, D.E. Stanley-Horn, K.S. Oberhauser, J.M. Pleasants, H.R. Mattila, B.D. Siegfried, and G.P. Dively. 2001. Impact of Bt corn pollen on monarch butterfly
populations: a risk assessment. Proceedings of the National Academy of Sciences USA
98:1193711942.
Seeley, T.D. 1985. Honeybee Ecology. Princeton: Princeton University Press. 201 pp.
Seeley, T.D. 2003. Bees in the forest, still. Bee Culture 131:2427.
Sekita, N. 2001. Managing Osmia cornifrons to pollinate apples in Aomori Prefecture, Japan.
Acta Horticulturae 561:303307.
SEMARNAT (Secretara de Medio Ambiente y Recursos Naturales). 2002. Norma Oficial
Mexicana NOM-059-ECOL-2001, Proteccin ambientalEspecies nativas de Mxico
de flora y fauna silvestresCategoras de riesgo y especificaciones para su inclusin,
exclusin o cambioLista de especies en riesgo. Diario Oficial, March 6, 2002:156.
Settele, J., V. Hammen, P. Hulme, U. Karlson, S. Klotz, M. Kotarac, W. Kunin, G. Marion,
M. OConnor, T. Petanidou, K. Peterson, S. Potts, H. Pritchard, P. Pysek, M. Rounsevell,
J. Spangenberg, I. Steffan-Dewenter, M. Sykes, M. Vighi, M. Zobel, and I. Khn. 2005.
ALARM: Assessing large-scale environmental risks for biodiversity with tested methods.
Gaia 14:6972.
Sheffield, C.S. 2006. Diversity and management of bees for the pollination of apple in the Annapolis Valley of Nova Scotia. Ph.D. thesis, University of Guelph, Canada.
Shelton, A.M., and R. Roush. 1999. False reports and the ears of men. Nature Biotechnology
17:832.
Shepherd, M.D. 2002. Making Room for Pollinators: How to Create Habitat for Pollinator
Insects on Golf Courses. 2002. Far Hills, N.J.: U.S. Golf Association.
Shepherd, M.D., and V.J. Tepedino. 2000. The birdies and the bees. Green Section, Record
38:1721.
Shepherd, M.D., D. Heagerty, and B. Baker. 2001. Environmental opportunity: pollinating
bugs need homes. Golf Course Management. February:5560.
Shepherd, M.D., S.L. Buchmann, M. Vaughan, and S.H. Black. 2003. Pollinator Conservation
Handbook: A Guide to Understanding, Protecting, and Providing Habitat for Native
Pollinator Insects. The Xerces Society in Association with The Bee Works. Portland: The
Xerces Society. 145 pp.
Shepherd, M.D., D.M. Vaughan, and S.H. Black. eds. 2005. Red List of Pollinator Insects of
North America. CD-ROM Version 1 (May 2005). Portland: The Xerces Society for Invertebrate Conservation. Available at: http://www.xerces.org/Pollinator_Red_List/index.
htm.
Sheppard, W.S. 1989a. A history of the introduction of honey bee races into the United States.
I. American Bee Journal 129:617619.
Sheppard, W.S. 1989b. A history of the introduction of honey bee races into the United States.
II. American Bee Journal 129:664667.
Sheppard, W.S. 2006. Breeding bees, mite resistance to pesticides and the limitations of bee
research. Bee Culture 134:1516.
Sherman, P.W., E.A. Lacey, H.K. Reeve, and L. Keller. 1995. The eusociality continuum. Behavioral Ecology 6(11):102108.
Shimanuki, H. 1997. Bacteria. In: Honey Bee Pests, Predators, and Diseases, R.A. Morse and
K. Flottum, eds., 3rd edition. Medina, Ohio: A. I. Root Company.
Shimanuki, H., and D.A. Knox. 1994. Susceptibility of Bacillus larvae to Terramycin. American
Bee Journal 134(2):125126.
Shimanuki, H., D.A. Knox, M. Delfinado-Baker, and P.J. Lima. 1983. National honey bee mite
survey. Apidologie 14(4):329332.
Shimanuki, H., N.W. Calderone, and D.A. Knox. 1994. Parasitic mite syndrome: the symptoms. American Bee Journal 134:827828.

260
Shuler, R.E., T.H. Roulston, and G.E. Farris. 2005. Farming practices influence wild pollinator
populations on squash and pumpkins. Journal of Economic Entomology 98:790795.
Shykoff, J.A., and P. Schmid-Hempel. 1991. Incidence and effects of four parasites in natural
populations of bumble bees in Switzerland. Apidologie 22(2):117125.
SIAP (Sistema Integral de Informacin Agroalimentaria y Pesquera). 2005. Abeja: Populacin
Apcola.), Secretara de Agricultura, Ganadera, Desarrollo Rural, Pesca y Alimentacin
(SAGARPA). Available at: http://www.siap.sagarpa.gob.mx/ar_compec_pobgan.html.
Accessed April 17, 2006.
Sibley, D.A. 2000. The Sibley Guide to Birds. New York: Alfred A. Knopf.
Simberloff, D.S., and E.O. Wilson. 1969. Experimental zoogeography of islands: the colonization of empty islands. Ecology 50:278289.
Simpson, R.D. 2002. Definitions of Biodiversity and Measures of Its Value. Discussion Paper
02-62. Washington: Resources for the Future.
Simpson, R.D., R.A. Sedjo, and J.W. Reid. 1996. Valuing biodiversity for use in pharmaceutical
research. Journal of Political Economy 104(1):163185.
Singer, R.B. 2003. Orchid pollination: recent developments from Brazil. Lankesteriana
7:111114.
Sinnott, E.W. 1946. Botany Principles and Problems. 4th edition. New York: McGraw-Hill.
726 pp.
Slauson, L.A. 2000. Pollination biology of two chiropterophilous agaves in Arizona. American
Journal of Botany 87:825836.
Slauson, L.A. 2001. Insights on the pollination biology of Agave (Agavaceae). Haseltonia
8:1023.
Smallidge, P.J., and D.J. Leopold. 1997. Vegetation management for the maintenance and
conservation of butterfly habitats in temperate human-dominated landscapes. Landscape
and Urban Planning 38(34):259280.
Smith, D.A. 1977. The first honeybees in America. Bee World 58:56.
Snelling, R.R. 1983. Studies on North American bees of the genus Hylaeus: 6. An adventive
Palearctic species in Southern California (Hymenoptera: Colletidae). Bulletin of the
Southern California Academy of Sciences 82:1216.
Snow, A.A., and D.F. Whigham. 1989. Costs of flower and fruit production in Tipularia discolor (Orchidaceae). Ecology 70:12861293.
Snyder, R.G. 1999. Southeastern United States Greenhouse Vegetable Growers Conference and
Trade Show Proceedings. Available at: http://nfrec-sv.ifas.ufl.edu/Reports%20HTML/
proceedings.htm. Accessed June 13, 2006.
Snyder, R.G. 2006. Letter to potential exhibitors for the 16th annual Greenhouse Tomato Short
Course. Available at: http://www.msstate.edu/dept/cmrec/ExhibLetterWeb.pdf.
Soroka, J.J., D.W. Goerzen, K.C. Falk, and K.E. Bett. 2001. Alfalfa leafcutting bee (Hymenoptera: Megachilidae) pollination of oilseed rape (Brassica napus L.) under isolation tents
for hybrid seed production. Canadian Journal of Plant Science 81(1):199204. Ottawa:
Agricultural Institute of Canada.
Southwick, E.E., and L. Southwick, Jr. 1992. Estimating the economic value of honey bees
(Hymenoptera: Apidae) as agricultural pollinators in the United States. Journal of Economic Entomology 85(3):621633.
Spivak, M., and D.L. Downey. 1998. Field assays for hygienic behaviour in honey bees (Hymenoptera: Apidae). Journal of Economic Entomology 91(1):6470.
Spivak, M., and M. Gilliam. 1998a. Hygienic behaviour of honey bees and its application
for control of brood diseases and Varroa. Part I. Hygienic behaviour and resistance to
American foulbrood. Bee World 79(3):124134.
Spivak, M., and M. Gilliam. 1998b. Hygienic behaviour of honey bees and its application for
control of brood diseases and varroa. Part II. Studies on hygienic behaviour since the
Rothenbuhler era. Bee World 79(4):169186.

REFERENCES
261
Spivak, M., and G.S. Reuter. 1998. Performance of hygienic honey bee colonies in a commercial
apiary. Apidologie 29:285296.
Spivak, M., G.S. Reuter, and M. Lamb. 1995. Frequency of hygienic behavior in naturally
mated daughters of a hygienic breeder queen. American Bee Journal 135(12):830.
Sprengel, C.K. 1793. Das entdeckte Geheimniss der Natur im Bau und in der Befruchtung
der Blumen [The Secret of Nature in the Form and Fertilization of Flowers Discovered].
Berlin: Friedrich Vieweg der ltere.
Stang, M., P.G.L. Kinkhamer, and E. van der Meijden. 2006. Size constraints and flower
abundance determine the number of interactions in a plant-flower visitor web. Oikos
112:111121.
Stanghellini, M.S., J.T. Ambrose, and J.R. Schultheis. 1996a. Establishing bumble bees as
supplementary pollinators for honey bees for watermelon. HortScience 31(4):668.
Stanghellini, M.S., J.T. Ambrose, and J.R. Schultheis. 1996b. Bumble bee: an alternative pollinator for cucumber. HortScience 31(5):746.
Stanghellini, M.S., J.T. Ambrose, and J.R. Schultheis. 1997. The effects of honey bee and
bumble bee pollination on fruit set and abortion of cucumber and watermelon. American
Stanley-Horn, D.E., G.P. Dively, R.L. Hellmich, H.R. Mattila, M.K. Sears, R. Rose, L.C. Jesse,
J.E. Losey, J.J. Obrycki, and L. Lewis. 2001. Assessing the impact of Cry1Ab-expressing
corn pollen on monarch butterfly larvae in field studies. Proceedings of the National
Academy of Sciences USA 98:1193111936.
Stannard, L.J. 1957. The phylogeny and classification of the North American genera of the
suborder Tubulifera (Thysanoptera). Illinois Biological Monographs 25:1200.
Stannard, L.J. 1968. The thrips, or Thysanoptera, of Illinois. Bulletin of the Illinois Natural
History Survey 29:211252.
Statistics Canada. 2006. Production and Value of Honey and Maple. Catalogue No. 23-221XIB. Ottawa: Statistics Canada. Available at: http://www.statcan.ca/english/freepub/
23221XIB/23-221-XIB2005000.pdf.
Stebbins, G.L. 1950. Variation and Evolution in Plants. New York: Columbia University
Press.
Stebbins, G.L. 1974. Flowering Plants. Evolution above the Species Level. Cambridge, Mass.:
Harvard University Press.
Stefanescu, C., J. Peuelas, and I. Filell. 2003. Effects of climatic change on the phenology of
butterflies in the northwest Mediterranean Basin. Global Change Biology 9(10):1494.
Steffan-Dewenter, I. 2003. Importance of habitat area and landscape context for species
richness of bees and wasps in fragmented orchard meadows. Conservation Biology
17:10361044.
Steffan-Dewenter, I., and T. Tscharntke. 1999. Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432440.
Steffan-Dewenter, I., U. Mnzenberg, and T. Tscharntke. 2001. Pollination, seed set and seed
predation on a landscape scale. Proceedings of the Royal Society of London Series B
268:16851690.
Steffan-Dewenter, I., U. Munzenberg, C. Burger, C. Thies, and T. Tscharntke. 2002.
Scale-dependent effects of landscape context on three pollinator guilds. Ecology
83:14211432.
Steffan-Dewenter, I., S.G. Potts, and L. Packer. 2005. Pollinator diversity and crop pollination
services are at risk. Trends in Ecology and Evolution 20(12):651652.
Steffan-Dewenter, I., A.M. Klein, V. Gaebele, T. Alfert, and T. Tscharntke. 2006. Bee diversity
and plant-pollinator interactions in fragmented landscapes. Pp. 387410 in Specialization
and Generalization in PlantPollinator Interactions, N.M. Waser and J. Ollerton, eds.
Chicago: University of Chicago Press.

262
Steiner K.E., and V.B. Whitehead.1996. The consequences of specialization for pollination in
a rare South African shrub, Ixianthes retziodes (Scrophulariaceae). Plant Systematics and
Evolution 201:131138.
Stephanou, M., Y. Petropoulou, O. Georgiou, and Y. Manetas. 2000. Enhanced UV-B radiation, flower attributes and pollinator behaviour in Cistus creticus: a Mediterranean field
study. Plant Ecology 147:165171.
Stephen, W.P. 2003. Solitary bees in North American agriculture: a perspective. Pp. 4166 in
For Nonnative Crops, Wence Pollinators of the Future, K. Strickler and J.H. Cane, eds.
in Entomology.
Stephen, W.P., and B.L. Fichter. 1990a. Chalkbrood (Ascosphaera aggregata) resistance in
the leafcutting bee (Megachile rotundata). I. Challenge of selected lines. Apidologie
21(3):209219.
Stephen, W.P., and B.L. Fichter. 1990b. Chalkbrood (Ascosphaera aggregata) resistance in the
leafcutting bee (Megachile rotundata). II. Random matings of resistant lines to wild type.
Stephen, W.P., and P.F. Torchio. 1961. Biological notes on the leaf-cutter bee, Megachile (Eutricharaea) rotundata (Fabricius). Pan-Pacific Entomologist 37:8593.
Stephen, W.P., G.E. Bohart, and P.F. Torchio. 1969. The Biology and External Morphology of
Bees. Corvallis: Agricultural Experiment Station, Oregon State University.
Stephen, W.P., J.D. Vandenberg, and B.L. Fichter. 1981. Etiology and epizootiology of chalkbrood in the leafcutting bee, Megachile rotundata (Fabricius), with notes on Ascosphaera
species. Oregon State University Agricultural Experimentation Station Bulletin 653.
Stephenson, A.G. 1981. Toxic nectar deters nectar thieves of Catalpa speciosa. American
Midland Naturalist 105:381383.
Stiles, F.G., and A.F. Skutch. 1989. A Guide to the Birds of Costa Rica. New York: Cornell
University Press.
Stoner, K.E., K.A.O. Salazar, R.C.R. Fernandez, and M. Quesada. 2003. Population dynamics,
reproduction, and diet of the lesser long-nosed bat (Leptonycteris curasoae) in Jalisco,
Mexico: implications for conservation. Biodiversity and Conservation 12:357373.
Stork, N.E. 1988. Insect diversitiy: Facts, fiction, and speculation. Biological Journal of the
Linnean Society 35:321337.
Stork, N.E. 1997. Measuring global biodiversity and its decline. Pp. 4168 in Biodiversity II:
Understanding and Protecting our Biological Resources, M.L. Reaka-Kudla, D.E. Wilson,
and E.O. Wilson, eds. Washington: Joseph Henry Press. 551 pp.
Strickler, K., and J. Cane, eds. 2003. For Nonnative Crops, Whence Pollinators of the Future?
in Entomology. 204 pp.
Stubbs, C.S., and F.A. Drummond. 1997a. Pollination of wild lowbush blueberry, Vaccinium
angustifolium by the alfalfa leafcutting bee, Megachile rotundata. Acta Horticulturae
(446):189196.
Stubbs, C.S., and F.A. Drummond. 1997b. Management of the alfalfa leafcutting bee, Megachile rotundata (Hymenoptera: Megachilidae), for pollination of wild lowbush blueberry.
Journal of the Kansas Entomological Society 70(2):8193.
Stubbs, C.S., and F.A. Drummond. 2001. Bees and Crop PollinationCrisis, Crossroads,
Conservation. Proceedings, Entomological Society of America. Lanham, Md.: Thomas
Say Publications in Entomology. 156 pp.
Stubbs, C.S., F.A. Drummond, and E.A. Osgood. 1994. Osmia ribifloris bidermannii and Megachile rotundata (Hymenoptera: Megachilidae) introduced into the lowbush blueberry
agroecosystem in Maine. Journal of the Kansas Entomological Society 67:173185.
Stubbs, C.S., F.A. Drummond, and S.L. Allard. 1997. Bee conservation and increasing Osmia
spp. in Maine wild blueberry fields. Northeastern Naturalist 4:133144.

REFERENCES
263
Sumner, D.A., and H. Boriss. 2006. Bee-conomics and the leap in pollination fees. Agricultural
and Resource Economics Update 9(Jan/Feb):911. Available at: http://www.agecon.
ucdavis.edu/uploads/update_articles/v9n3_3.pdf.
Swengel, A.B. 1990. Monitoring butterfly populations using the Fourth of July butterfly count.
American Midland Naturalist 124:395406.
Swengel, A.B. 1995. Population fluctuations of the Monarch (Danaus plexippus) in the 4th of
July butterfly count 19771994. American Midland Naturalist 134:205221.
Swingle, W.T. 1908. The Fig in California. Papers and discussions presented before the 34th
and 35th Fruit-Growers Convention, California. Sacramento: State Commission on
Horticulture.
Tang, J., J. Wice, V.G. Thomas, and P.G. Kevan. 2005. Assessment of the Capacity of Canadian
Federal and Provincial Leglislation to Conserve Native and Managed Pollinators. The
International Network of Expertise for Sustainable Pollination, for the North American
Pollinator Protection Campaign. Available at: http://www.pollinator.org/Laws%20Affec
ting%20Pollinators-Canada.pdf.
Tasi, J.N., H. Sabik, L. Pirastru, E. Langiu, J.M. Blanche, J. Fournier, and J.P. Taglioni. 1994.
Effects of sublethal doses of deltamethrin (Decis) on Bombus terrestris. Journal of Apicultural Research 33:129135.
Tasi, J.N., G. Ripault, and E. Rivault. 2001. Hazards of imidacloprid seed coating to Bombus terrestris (Hymenoptera: Apidae) when applied to sunflower. Journal of Economic
Taylor, O.R., Jr. 1977. The past and possible future spread of Africanized honeybees in the
Americas. Bee World 58(1):1930.
Taylor, O.R., Jr. 2000. 40 years of tagging Monarch. Watch Season 2000 Summary 8:4446.
Tllez, G., and J. Ortega. 1999. Musonycteris harrisoni. Mammalian Species (American Society
of Mammalogists) 622:13.
Temeles, E.J., Y.B. Linhart, M. Masonjones, and H.D. Masonjones. 2002. The role of flower
width in hummingbird bill length-flower length relationships. Biotropica 34:6880.
Tepedino, V.J. 1997. A comparison of the alfalfa leafcutting bee (Megachile rotundata) and the
honey bee (Apis mellifera) as pollinators for hybrid carrot seed in field cages. Pp. 457461
in Proceedings of the 7th International Symposium on Pollination, Lethbridge, Alberta,
Canada, 2328 June 1996, K.W. Richards, ed. Leiden, Netherlands: International Society
for Horticultural Science.
Tepedino, V.J., and H.S. Ginsberg. 2000. Report of the U.S. Department of Agriculture and
U.S. Department of Interior Joint Workshop on Declining Pollinators, May 2728, 1999,
Logan, Utah. U.S. Geological Survey, Biological Resources Division, Information and
Technology Report USGS/BRD/ITR-2000-0007, 9 pp.
Tequila Aficionado. 2001. Tequila Sales Skyrocket; Agave Shortage Continue. Available at:
http://www.tequilaaficionado.com/article.php?sid=83. Accessed February 24, 2001.
Terry, I. 1997. Host selection, communication, and reproductive behaviour. Pp. 64118 in
Thrips as Crop Pests, T. Lewis, ed. London: CAB International.
Terry, I. 2001. Thrips and weevils as dual, specialist pollinators of the Australian cycad Macrozamia communis (Zamiaceae). International Journal of Plant Sciences 162:12931305.
Terzo, M., and F.J. Ortiz-Sanchez. 2004. Nuevos datos para las species de ceratinini de Espaia
y Portugal, con una clave para su identificatin (Hymenoptera, Apoidea, Xylocopinae).
Graellsia 60(1):1326.
Terzo, M., and P. Rasmont. 2004. Biogographie et systmatique des abeilles rubicoles du
genre Ceratina Latreille au Turkestan (Hymenoptera, Apoidea, Xylocopinae). Annales
de la Socit Entomologique de France 40(2):109130.

264
Tewksbury, J.J., D.J. Levey, N.M. Haddad, S. Sargent, J.L. Orrock, A. Weldon, B.J. Danielson,
J. Brinkerhoff, E.I. Damschen, and P. Townsend. 2002. Corridors affect plants, animals,
and their interactions in fragmented landscapes. Proceedings of the National Academy
Thien, L.B. 1974. Floral biology of Magnolia. American Journal of Botany 61:10371045.
Thien, L.B., and V. Rico-Gray. 2004. Ant-orchid interactions. Orchids 73(8):606617.
Thien, L.B., and F. Utech. 1970. The mode of pollination in Habenaria obtusata (Orchidaceae).
Thien, L.B., E. Elgaard, M. Devall, S. Ellgaard, and R. Ramp. 1999. Population structure
and reproductive biology of Saururus cenuus L. (Saururacee). Plant Species Biology
9:4755.
Thomas, C.D., A. Cameron, R.E. Green, M. Bakkenes, L.J. Beaumont, Y.C. Collingham, B.F.N.
Erasmus, M.F. de Siqueira, A. Grainger, L. Hannah, L. Hughes, B. Huntley, A.S. van
Jaarsveld, G.F. Midgley, L. Miles, M.A. Ortega-Huerta, A.T. Peterson, O.L. Phillips, and
S.E. Williams. 2004. Extinction risk from climate change. Nature 427:145148.
Thomas, J.A., M.G. Telfer, D.B. Roy, C.D. Preston, J.J.D. Greenwood, J. Asher, R. Fox, R.T.
Clarke, and J.H. Lawton. 2004. Comparative losses of british butterflies, birds, and plants
and the global extinction crisis. Science 303:18791881.
Thomas, M.C. 1998. Florida pest alertthe small hive beetle. American Bee Journal
138:565.
Thompson, A.R. 2003. The issues facing the industry of the management of resistance in Europe. Pp. 695702 in The BCPC International Congress: Crop Science and Technology,
Volumes 1 and 2 Proceedings of an International Congress held at the SECC, Glasgow,
Scotland, UK, November 1012, 2003. Alton: British Crop Protection Council.
Thompson, F.C. 1990. Biosystematic information: dipterists ride the third wave. Pp. 179201
in Systematics of the North American Insects and Arachnids: Status and Needs, M.
Kosztarab and C.W. Schaefer, eds. Virginia Agricultural Experiment Station Information
series 90-1. Blacksburg: Virginia Polytechnic Institute and State University.
Thompson, F.C., ed. 2006. Biosystematic Database of World Diptera. Available at: http://www.
diptera.org/names. Accessed April 22, 2006.
Thompson, H.M. 2001. Assessing the exposure and toxicity of pesticides to bumblebees
(Bombus sp.). Apidologie 32:305321.
Thompson, J.N. 1982. Interaction and Coevolution. New York: Wiley and Sons. 179 pp.
Thompson, J.N. 1994. The Coevolutionary Process. Chicago: University of Chicago Press.
387 pp.
Thompson, J.N. 2005. The Geographic Mosaic of Coevolution. Chicago: University of Chicago Press.
Thomson, D.M. 2004. Competitive interactions between the invasive European honey bee and
native bumble bees. Ecology 85(2):458470.
Thomson, D.M. 2006. Detecting the effects of introduced species: a case study of competition
between Apis and Bombus. Oikos 114(3):407418.
Thomson, J.D., and K. Goodell. 2001. Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers. Journal of Applied Ecology 38:10321044.
Thomson, J.D., and B.A. Thomson. 1992. Pollen presentation and viability schedules in
animal-pollinated plants: consequences for reproductive success. Pp. 124 in Ecology and
Evolution of Plant Reproduction: New Approaches, R. Wyatt, ed. New York: Chapman
and Hall.
Thomson, J.D., R.C. Plowright, and G.R. Thaler. 1985. Matacil insecticide spraying, pollinator
mortality, and plant fecundity in New Brunswick forests. Canadian Journal of Botany
63:20562061.

REFERENCES
265
Thorp, R.W. 1996. Resource overlap among native and introduced bees in California.
Pp. 143151 in The Conservation of Bees, A. Matheson, S.L. Buchmann, C. OToole, P.
Westrich, and H. Williams, eds. London: Academic.
Thorp, R.W. 2003. Bumble bees (Hymenoptera: Apidae): commercial use and environmental
concerns. Pp. 2140 in For Nonnative Crops, Whence Pollinators of the Future? K.
Strickler and J.H. Cane, eds. Proceedings, Entomological Society of America. Lanham,
Md.: Thomas Say Publications in Entomology.
Thorp, R.W. 2005. Bombus franklini Frison, 1921 Franklins bumble bee (Hymenoptera:
Apidae: Apinae: Bombini). In Red List of Pollinator Insects of North America. CD-ROM
Version 1, M.D. Shepherd, M.Vaughan, and S.H. Black, eds. Portland: The Xerces Society
for Invertebrate Conservation.
Thorp, R.W., and M.D. Shepherd. 2005. Species profile: subgenus Bombus. In Red List of
Pollinator Insects of North America. CD-ROM Version 1, M.D. Shepherd, M.Vaughan,
and S.H. Black, eds. Portland: Xerces Society for Invertebrate Conservation.
Thorp, R.W., A.M. Wenner, and J.F. Barthell. 2000. Proceedings of the Fifth California Islands
Symposium, D.R. Browne, K.L. Mitchell, and H.W. Chaney, eds. Washington: U.S. Depart
ment of the Interior, Mineral Management Service.
Thorp, R.W., P.C. Schroeder, and C.S. Ferguson. 2003. Bumble bees: boisterous pollinators of
native California flowers. Fremontia 30(34):2631.
Tilden, J.W. 1956. San Franciscos vanishing butterflies. Lepidoptera News 10:133145.
Ting, Z.,Q. Wang, and Y. Jun. 2003. I: Advances in research of fluvalinate resistance in Varroa
destructor: sodium channels involved. Entomological Knowledge 40(6):491495.
Toledo, V.M. 1977. Pollination of some rain forest plants by non-hovering birds in Veracruz,
Mexico. Biotropica 9:262267.
Toledo, V.M., and H.M. Hernandez. 1979. Erythrina oliviaeNew case of oriole pollination
in Mexico. Annals of the Missouri Botanical Garden 66:503511.
Tonhasca, A., J.L. Blackmer, and G.S. Albuquerque. 2002. Abundance and diversity of euglossine bees in the fragmented landscape of the Brazilian Atlantic forest. Biotropica
34:416422.
Torchio, P.F. 1973. Relative toxicity of insecticides to the honey bee alkali bee and alfalfa
leaf-cutting bee hymenoptera apidae halictidae megachilidae. Journal of the Kansas Entomological Society 46:446453.
Torchio, P.F. 1981a. Field experiments with Osmia lignaria propinqua Cresson as a pollinator
in almond orchards. I. 1975 studies (Hymenoptera: Megachilidae). Journal of the Kansas
Torchio, P.F. 1981b. Field experiments with Osmia lignaria propinqua Cresson as a pollinator
in almond orchards. II. 1976 studies (Hymenoptera: Megachilidae). Journal of the Kansas
Torchio, P.F. 1982. Field experiments with Osmia lignaria propinqua Cresson as a pollinator in
almond orchards. III. 1977 studies (Hymenoptera: Megachilidae). Journal of the Kansas
Torchio, P.F. 1990. Diversification of pollination strategies for U.S. crops. Environmental
Entomology 19(6):16491656.
Torchio, P.F. 2003. The development of Osmia lignaria Say (Hymenoptera: Megachilidae)
as a managed pollinator of apple and almond crops: a case history. Pp. 6784 in For
Nonnative Crops, Whence Pollinators of the Future? K. Strickler and J.H. Cane, eds.
in Entomology.
Torchio, P.F., and E. Asensio. 1985. The introduction of the European bee, Osmia cornuta, into
the USA as a potential pollinator of orchard crops, and a comparison of its manageability
with Osmia lignaria propinqua (Hymenoptera: Megachilidae). Journal of the Kansas
Entomological Society 58:4252.

266
Torchio, P.F., E. Asensio, and R.W. Thorp. 1987. Introduction of the European bee, Osmia
cornuta, into California almond orchards (Hymenoptera: Megachilidae). Environmental
Torres, J.A., and R.R. Snelling. 1997. Biogeography of Puerto Rican ants: a non-equilibrium
case. Biodiversity Conservation 6(8):11031121.
Townsend, P.A., and D.J. Levey. 2005. An experimental test of whether habitat corridors affect
pollen transfer. Ecology 86:466475.
Trejo, I., and R. Dirzo. 2000. Deforestation of seasonally dry tropical forest: a national and
local analysis in Mexico. Biological Conservation 94:133142.
Tschapka, M., and O. von Helversen. 1999. Pollinators of syntopic Marcgravia species in Costa
Rican lowland rain forest: bats and opossums. Plant Biology 1:382388.
Tscharntke, T., A. Gathmann, and I. SteffanDewenter. 1998. Bioindication using trap-nesting
bees and wasps and their natural enemies: community structure and interactions. Journal
of Applied Ecology 35:708719.
Tscharntke, T., A.M. Klein, A. Kruess, I. Steffan-Dewenter, and C. Thies. 2005. Landscape
perspectives on agricultural intensification and biodiversityecosystem service management. Ecology Letters 8(8):857874.
Tudor, O., R.L.H. Dennis, J.N. Greatorex-Davies, and T.H. Sparks. 2004. Flower preferences
of woodland butterflies in the UK: nectaring specialists are species of conservation concern. Biological Conservation 119:397403.
Turner, W.R. 2003. Citywide biological monitoring as a tool for ecology and conservation in
urban landscapes: the case of the Tucson Bird Count. Landscape and Urban Planning
65:149166.
Turncock, V.J., P.G. Kevan, T.M.Laverty, and L. Dumouchel. Abundance of species of
bumble bees (Hymenoptera, Apoidea, Bombinae) in fields of Canola, Brassica rapa L, in
Manitoba, an 8-year record. In preparation.
Turner, W.R., T. Nakamura, and M. Dinetti. 2004. Global urbanization and the separation of
humans from nature. Bioscience 54:585590.
Tuttle, M.D. 2000. Where the bats arepart III: caves, cliffs, and rock crevices. Bat Magazine
18(1):611.
Ullman, D.E., J.L. Sherwood, and T.G. German. 1997. Thrips as vectors of plant pathogens.
Pp. 539565 in Thrips as Crop Pests, T.L. Lewis, ed. London: CAB International.
UK Department of Environment, Food and Rural Affairs. 2002. ERDP Scheme Introduction.
Available at: http://www.defra.gov.uk/erdp.schemes/default.htm. Accessed August 23,
2006.
USDA-AMS (U.S. Department of Agriculture Agricultural Marketing Service). 2004. Honey
Research, Promotion, and Consumer Information Order. U.S. Department of Agriculture.
Available at: http://www.ams.usda.gov/fv/rphoney.html. Accessed March 10, 2006.
USDA-AMS. 2005. How to Request a National Research and Promotion Program. Livestock
and Seed Program, Agricultural Marketing Service, U.S. Department of Agriculture.
Available at: http://www.ams.usda.gov/lsg/mpb/generic/generic.htm. Accessed December
30, 2005.
USDA-APHIS (U.S. Department of Agriculture Animal and Plant Health Inspection Service).
2002. Risk Assessment: Importation of Adult Queens, Package Bees and Germplasm of
Honey Bees, Apis mellifera L., from Australia. U.S. Department of Agriculture, APHIS.
Available at: http://www.aphis.usda.gov/ppq/pra/honeybees/aushbee_pra.html. Accessed
December 30, 2005.
USDA-APHIS. 2004. Animal and Plant Health Inspection Service: Bees and Related Articles,
Final Rule. Federal Register 7 CFR Parts 319 and 322, 69(203):6173561755.
USDA-ERS (U.S. Department of Agriculture Economic Research Service). 2004. Fruit and
Tree Nuts Outlook. U.S. Department of Agricutlure. Available at: http://www.ers.usda.
gov/Briefing/FruitandTreeNuts/fruitnutpdf/Figs.pdf. Accessed May 16, 2006.

REFERENCES
267
USDA-FSA (U.S. Department of Agriculture Farm Service Agency). 2006. Conservation

Reserve Program. U.S. Department of Agriculture. Available at: http://www.fsa.usda.
gov/dafp/cepd/crp.htm. Accessed March 10, 2006.
USDA-NASS (U.S. Department of Agriculture National Agricultural Statistics Service). 1995.
Honey: Final estimates for 19861992. Statistical Bulletin No. 912, March. Washington:
U.S. Department of Agriculture.
USDA-NASS. 1999. Honey: Final estimates for 19931997. Statistical Bulletin No. 956, February. Washington: U.S. Department of Agriculture.
USDA-NASS. 2004a. 2002 Census of Agriculture: United States Summary and State Data.
AC-02-A-51 (June). Washington: U.S. Department of Agriculture. Available at: http://
www.nass.usda.gov/census/census02/volume1/us/USVolume104.pdf. Accessed March
19, 2006.
USDA-NASS. 2004b. Honey: Final estimates for 19982002. Statistical Bulletin No. 992.
April. Washington: U.S. Department of Agriculture.
USDA-NASS. 2005. Honey. Washington: U.S. Department of Agriculture. Available at: http://
usda.mannlib.cornell.edu/reports/nassr/other/zho-bb/hony0205.pdf. Accessed February
28, 2005.
USDA-NASS. 2006a. Honey. Washington: U.S. Department of Agriculture.
USDA-NASS. 2006b. Crop Values: 2005 Summary. Washington: U.S. Department of
Agriculture.
USDA-NRCS (U.S. Department of Agriculture Natural Resources Conservation Service).
2004. Habitat development for pollinator insects. Biology Technical Note No. MT-20.
Washington: U.S. Department of Agriculture.
USDA-NRCS. 2006a. Native, culturally significant plants. Conservation Security Program Enhancement Activity Job Sheet. Plant Management EPL 40. Washington: U.S. Department
of Agriculture. Available at: http://www.pa.nrcs.usda.gov/technical/Jobsheets/EPL40_Native_Culturally_Significant_Plants.pdf. Accessed April 5, 2006.
USDA-NRCS. 2006b. Nectar corridors. Conservation Security Program Enhancement Activity Job Sheet. Plant Management EPL 41. Washington: U.S. Department of Agriculture.
Available at: http://www.pa.nrcs.usda.gov/technical/Jobsheets/EPL41_Nectar_Corridors.
pdf. Accessed April 5, 2006.
USFWS (U.S. Fish and Wildlife Service). 1988. Endangered and Threatened Wildlife and
Plants; Determination of Endangered Status for Two Long-nosed Bats. Federal Register
53:3845638460. U.S. Department of the Interior.
USFWS. 1994. Endangered and Threatened Wildlife and Plants. August 20, 1994. 50 CFR
17.11 and 17.12. U.S. Department of the Interior.
USFWS. 2006. USFWS Threatened and Endangered Species System. U.S. Department of the
Interior. Available at: http://ecos.fsw.gov. Accessed September 12, 2006.
Valenzuela-Zapata, A.G. 1994. El agave tequilero: Su cultivo e industrializacin. Guadalajara,
Mexico: Editorial Agata.
Valenzuela-Zapata, A.G., and G.P. Nabhan. 2004. Tequila: A Natural and Cultural History.
Tucson: University of Arizona Press.
Valiente-Banuet, A. 2002. Vulnerability of pollination systems of columnar cacti of Mexico.
Revista Chilena de Historia Natural 75(1):99104.
Valiente-Banuet, A., M.C. Arizmendi, A. Rojas-Martnez, and L. Domnguez-Canseco. 1996.
Ecological relationships between columnar cacti and nectar feeding bats in Mexico.
Journal of Tropical Ecology 12:103119.
Vamosi, J.C., T.M. Knight, J. Streets, S.J. Mazer, M. Burd, and T.-L. Ashman. 2006. Pollination decays in biodiversity hotspots. Proceedings of the National Academy of Sciences
103:956961.
Van der Cingel, N.A. 2001. An Atlas of Orchid Pollination: America, Africa, Asia and Australia. Rotterdam, Holland: A.A. Balkana.

268
van der Pijl, L. 1982. Principles of Dispersal in Higher Plants. Berlin: Springer-Verlag.
214pp.
van Heemert, C., A. de Ruijter, J. van den Eijnde, and J. van der Steen. 1990. Year round
production of bumble bee colonies for crop pollination. Bee World 71(2):5456.
Vance, M.D., L. Fahrig, and C.H. Flather. 2003. Effect of reproductive rate on minimum
habitat requirements of forest-breeding birds. Ecology 84:26432653.
Vance, N.C., P. Bernhardt, and R.M. Edens. 2004. Pollination and seed production in Xerophyllum tenax (Melanthiaceae) in the Cascade Range of Central Oregon. American
Journal of Botany 91:20602068.
Vandenberg, J.D., and W.P. Stephen. 1983. Pathogenesis of chalkbrood in the alfalfa leafcutting
bee, Megachile rotundata. Apidologie 14(4):333341.
Vaughan, M., M. Shepard, C. Kremen, and S.H. Black. 2004. Farming for Bees: Guidelines for
Providing Native Bee Habitat on Farms. Portland: The Xerces Society for Invertebrate
Conservation.
Vazquez, D.P., and M.A. Aizen. 2004. Asymmetric specialization: a pervasive feature of plantpollinator interactions. Ecology 85:12511257.
Velthuis, H.H.W. 2002. The historical background of the domestication of the bumble-bee,
Bombus terrestris, and its introduction in agriculture. Pp. 177184 in Pollinating Bees
The Conservation Link Between Agriculture and Nature, P. Kevan and V.L. Imperatriz
Fonseca, eds. Brazil: Ministry of Environment.
Villanueva-Gutierrez, R., D.W. Roubik, and W. Colli-Ucan. 2005. Extinction of Melipona
beecheii and traditional beekeeping in the Yucatan peninsula. Bee World 86(2):3541.
Vinson, S.B., G.W. Frankie, and J. Barthell. 1993. Threats to the diversity of solitary bees in a
neotropical dry forest in Central America. Pp. 5382 in Hymenoptera and Biodiversity,
J. LaSalle and I.D. Gauld, eds. Oxon: CAB International.
Visscher, P.K., and T.D. Seeley. 1982. Foraging strategy of honeybee colonies in a temperate
deciduous forest. Ecology 63:17901801.
Vogel, S. 1969. Chiropterophilie in der neotropischen Flora. Neue Mitteilungen II. Flora (B)
158:185222.
von Frisch, K. 1967. Tanzsprache und Orientierung der Bienen [The Dance Language and
Orientation of Bees]. Cambridge, Mass.: Harvard University Press.
von Helversen, O., and Y. Winter. 2003. Glossophagine bats and their flowers: cost and benefit
for plant and pollinator. Pp. 346397 in Bat Ecology, T.H. Kunz and M.B. Fenton, eds.
Chicago: University of Chicago Press.
von Helversen, O., L. Winkler, and H.J. Bestmann. 2000. Sulphur-containing perfumes
attract flower-visiting bats. Journal of Comparative Physiology A: Sensory, Neural, and
Behavioral Physiology 186:143153.
Walker-Simmons, M.K. 2003. New USDA-ARS research in biotechnology risk assessment.
Pp. 9599 in NABC Report 15: Biotechnology: Science and Society at a Crossroad, A.
Eaglesham, S. Ristow, and R.W.F. Hardy, eds. Ithaca: National Agricultural Biotechnology
Council.
WallisdeVries, M.F., J.P. Bakker, and S.E. Van Wieren. 1998. Grazing and Conservation. Dordrecht, Boston, London: Kluwer Academic Publishers.
WallisDeVries, M.F., P. Poschlod, and J.H. Willems, 2002. Challenges for the conservation of
calcareous grasslands in northwestern Europe: integrating the requirements of flora and
fauna. Biology Conservation 104:265273.
Walters, C.J., and C.S. Holling. 1990. Large-scale management experiments and learning by
doing. Ecology 71(6):20602068.
Walther, G.R. 2004. Plants in a warmer world. Perspectives in Plant Ecology, Evolution and
Systematics 6:169185.

REFERENCES
269
Walton, R.K., L.P. Brower, and A.K. Davis. 2005. Long-term monitoring and fall migration
patterns of the Monarch butterfly in Cape May, New Jersey. Annals of the Entomological
Wang, R.W., Z.Q. Liu, K. Dong, P.J. Elzen, J. Pettis, and Z.Y. Huang. 2002. Association of
novel mutations in a sodium channel gene with fluvalinate resistance in the mite, Varroa
destructor. Journal of Apicultural Research 41(12):1725.
Ward, M., and S.D. Johnson. 2005. Pollen limitation and demographic structure in small fragmented populations of Brunsvigia radulosa (Amaryllidaceae). Oikos 108(2):253.
Warren, M.S., J.K. Hill, J.A. Thomas, J. Asher, R. Fox, B. Huntley, D.B. Roy, M.G. Telfer, S.
Jeffcoate, P. Harding, G. Jeffcoate, S.G. Willis, J.N. Greatorex-Davies, D. Moss, and C.D.
Thomas. 2001. Rapid responses of British butterflies to opposing forces of climate and
habitat change. Nature 414:6569.
Waser, N.M. 1978. Competition for hummingbird pollination and sequential flowering in two
Colorado wildflowers. Ecology 59:934944.
Waser, N.M.1979. Pollinator availability as a determinant of flowering time in ocotillo (Fouquieria splendens) .Journal Oecologia 39(1):1 107121.
Waser, N.M., and J. Ollerton, eds. 2006. Plant-Pollinator Interactions: From Specialization to
Generalization. Chicago: University of Chicago Press. 488 pp.
Waser, N.M., L. Chittka, M.V. Price, N.M. Williams, and J. Ollerton. 1996. Generalization in
pollination systems, and why it matters. Ecology 77:10431060.
Watanabe, M.E. 1994. Pollination worries rise as honey bees decline. Science 265:1170.
Watson, L., and M.J. Dallwitz. 1992. The Families of Flowering Plants: Descriptions, Illustrations, Identification, and Information Retrieval. Version: June 2, 2006. http://delta-intkey.
com.
Wei, S.G., R. Wang, M.J. Smirle, and H.L. Xu. 2002. Release of Osmia excavata and Osmia
jacoti (Hymenoptera: Megachilidae) for apple pollination. Canadian Entomologist
134(3):369380.
Weiblen, G.D. 2002. How to be a fig wasp. Annual Review of Entomology 47:299330.
Weibull, A.-Ch., . stman, and . Granqvist. 2003. Species richness in agro-ecosystems:
the effect of landscape, habitat and farm management. Biodiversity and Conservation
12:13351355.
Weller, S.G. 1994. The relationship of rarity to plant reproductive biology. Pp. 90117 in Restoration of Endangered Species. Conceptual Issues, Planning and Implementation, M.L.
Bowles and C.J. Whelan, eds. Cambridge, Mass.: Cambridge University Press.
Westphal, C., I. Steffan-Dewenter, and T. Tscharntke. 2003. Mass flowering crops enhance
pollinator densities at a landscape scale. Ecology Letters 6:961965.
Westrich, P. 1989. Pp. 381390 in Die Wildbienen Baden Wrttembergs. Stuttgart: Eugen
Ulmer.
Westrich, P. 1990. Pp. 432972 in Die Wildbienen Baden-Wrttembergs. Vol. 2. Stuttgart:
Ulmer Verlag.
Westrich, P. 1996. Habitat requirements of central European bees and the problems of partial
habitats. Pp. 116 in The Conservation of Bees, A. Matheson, S.L. Buchmann, C. OToole,
P. Westrich, and I.H. Williams, eds. London: Academic Press.
White, G.F. 1920. American foulbrood. US Department of Agriculture Bulletin 809:46.
White, G.M., D.H. Boshier, and W. Powell. 2002. Increased pollen flow counteracts fragmentation in a tropical dry forest: an example from Swietenia humilis Zuccarini. Proceedings
of the National Academy of Sciences USA 99:20382042.
Whittington, R., M.L Winston, C. Tucker, and A.L. Parachnowitsch. 2004. Plant-species
identity of pollen collected by bumblebees placed in greenhouses for tomato pollination.
Canadian Journal of Plant Science 84:599602.

270
Wilkinson, G.S., and T.H. Fleming. 1996. Migration and evolution of lesser long-nosed
bats Leptonycteris curasoae, inferred from mitochondrial DNA. Molecular Ecology
5:329339.
Willett, G.S., and W.J. Gary. 1992. Alfalfa seed enterprise budget Walla Walla County, Washington. Washington State University Cooperative Extension EB 1375. 13 pp.
Williams, C.G., Y. Zhou, and S.E. Hall. 2001. A chromosomal region promoting outcrossing
in a conifer. Genetics 159:12831289.
Williams, N., and C. Kremen. Forthcoming (in press). The importance of local habitat, landscape composition and connectivity for population persistence of a solitary bee, Osmia
lignaria, in a mosaic agricultural landscape. Ecological Applications.
Williams, N.M., R.L. Minckley, and F.A. Silveira. 2001. Variation in native bee faunas and its
implications for detecting community changes. Conservation Ecology 5:7.
Williams, P. 1998. An annotated checklist of bumble bees with an analysis of patterns of
description (Hymenoptera: Apidae, Bombini). Bulletin of the Natural History Museum,
London (Entomology) 67(1):79152.
Williams, T.A., and M.T. Abberton. 2004. Earlier flowering between 1962 and 2002 in agricultural varieties of white clover. Oecologia 138(1):122126.
Williamson, M.S., J.A Anstead, G.J. Devine, A.L. Devonshire, L.M. Field, S.P. Foster,
G.D. Moores, and I. Denholm. 2003. Insecticide resistance: from science to practice.
Pp. 681688 in BCPC International Congress: Crop Science and Technology, Volumes
1 and 2. Proceedings of an international congress held at the SECC, Glasgow, Scotland,
UK, November 1012, 2003.
Wilson, D.E., D.V. Lanning, and R.A. Medellin. 1985. Bats from Northeastern Mexico, with
a Checklist of Species. Washington: U.S. Fish and Wildlife Service, Museum Section.
30pp.
Wilson, E O. 1971. The Insect Societies. Cambridge: Belknap.
Wilson, E.O. 2003. The encyclopedia of life. Trends in Ecology and Evolution 18:2:7780.
Wilson, E.O., and B. Hlldobler. 2005. Eusociality: origin and consequences. Proceedings of
the National Academy of Sciences USA 102(38):1336713371.
Wilson, R., D. Gutirrez, J. Gutirrez, D. Martnez, R. Agudo, and V.J. Monserrat. 2005.
Changes to the elevational limits and extent of species ranges associated with climate
change. Ecology Letters 8(11):1138.
Wilson, W.T. 1970. Inoculation of the pupal honeybee with spores of Bacillus larvae. Journal
of Apicultural Research 9:3337.
Wilson, W.T., and A.M. Collins. 1993. Formic acid or amitraz for spring or fall treatment of
Acarapis woodi. American Bee Journal 133(12):871.
Wilson, W.T., J.R. Elliott, and J.D. Hitchcock. 1973. Treatment of American foulbrood
with antibiotic extender patties and antibiotic paper packs. American Bee Journal
113:341344.
Wilson, W.T., J.S. Pettis, and A.M. Collins. 1989. Efficacy of different isomers of menthol
against the honey bee tracheal mite. American Bee Journal 129:826.
Wilson, W.T., R.L. Cox, J.O. Moffett, and M. Ellis. 1990. Improved survival of honey bee
(Apis mellifera L.) colonies from long-term suppression of tracheal mites (Acarapis woodi
Rennie) with menthol. Bee Science 1:4854.
Winfree, R., T. Griswold, and C. Kremen. 2007. Effect of human disturbance on bee communities in a forested ecosystem. Conservation Biology 21:213223.
Winston, M.L. 1979. Intra-colony demography and reproductive rate of the Africanized honeybee in South America. Behavioral Ecology and Sociobiology 4(3):279292.
Winston, M.L. 1987. Biology of the Honey Bee. Cambridge, Mass.: Harvard University Press.
281 pp.
Winston, M.L. 1992. Killer Bees. The Africanized Honey Bee in the Americas. Cambridge,
Mass.: Harvard University Press. xiii + 162 pp.

REFERENCES
271
Winston, M.L., G.W. Otis, and O.R. Taylor, Jr. 1979. Absconding behaviour of the Africanized
honeybee in South America. Journal of Apicultural Research 18(2):8594.
Winston, M.L., J.A. Dropkin, and O.R. Taylor, Jr. 1981. Demography and life history characteristics of two honey bee races (Apis mellifera). Oecologia 48:407413.
Winston, M.L., O.R. Taylor, Jr., and G.W. Otis. 1983. Some differences between temperate European and tropical African and South American honeybees. Bee World 64(1):1221.
Winter, K., L. Adams, R. Thorp, D. Inouye, L. Day, J. Ascher, and S. Buchmann. 2006. Importation of Non-native Bumble Bees into North America: Potential Consequences of using
Bombus terrestris and other Non-native Bumble Bees for Greenhouse Crop Pollination in
Canada, Mexico, and the United States. White Paper of the North American Pollinator
Protection Campaign. Available at: http://www.nappc.org/WhitePaper-news_release_
FINAL.pdf.
Winter, Y., and O. von Helversen. 2001. Bats as pollinators: foraging energetics and floral adaptations. Pp. 148170 in Cognitive Ecology of Pollination, L. Chittka and J.D. Thomson,
eds. Cambridge: Cambridge University Press.
Wolda, H. 1988. Insect seasonality: why? Annual Review of Ecology and Systematics
19:118.
Wraight, C.L., A.R. Zangerl, M.J. Carroll, and M.R. Berenbaum. 2000. Absence of toxicity
of Bacillus thuringiensis pollen to black swallowtails under field conditions. Proceedings
of the National Academy of Sciences USA 97(14):77007703.
Wu, J.Q., B.D. Siegfried, and M.D. Ellis. 2003. An investigation of the metabolic detoxification
of fluvalinate in Varroa destructor Anderson and Truemann. Resistant Pest Management
Newsletter 13(1):7075.
Wyatt, R. 1981. Ant-pollination of the granite outcrop endemic Diamorpha smallii (Crassulaceae). American Journal of Botany 68:12121217.
Wyatt, R., and A. Stoneburner. 1981. Patterns of ant-mediated pollen dispersal in Diamorpha
smallii (Crassulaceae). Systematic Botany 6:17.
Young, A.M. 1981. The ineffectiveness of the stingless bee Trigona-Jaty (Hymenoptera, Apidae,
Meliponinae) as a pollinator of cocoa (Theobroma-Cacao L). Journal of Applied Ecology
18(1):149155.
Young, A.M. 1982. Effects of shade cover and availability of midge breeding sites on pollinating midge populations and fruit-set in 2 cocoa farms. Journal of Applied Ecology
19(1):4763.
Young, A.M. 1985. Pollen-collecting by stingless bees on cacao flowers. Experientia
41(6):760762.
Young, A.M. 1986. Distribution and abundance of Diptera in flypaper traps at TheobromaCacao L (Sterculiaceae) flowers in Costa Rican cacao plantations. Journal of the Kansas
Young, A.M. 1994. The Chocolate Tree: A Natural History of Cacao. Washington: Smithsonian Institute Press.
Yurlina, M.E. 1998. Bee mutualists and plant reproduction in urban woodland restorations.
Ph.D. thesis, Rutgers University, New Brunswick, New Jersey.
Zangerl, A.R., D. McKenna, C.L. Wraight, M. Carroll, P. Ficarello, R. Warner, and M.R.
Berenbaum. 2001. Effects of exposure to event 176 Bacillus thuringiensis corn pollen
on monarch and black swallowtail caterpillars under field conditions. Proceedings of the
National Academy of Sciences USA 98:1190811912.
Zavaleta, E.S., R.J. Hobbs, and H.A. Mooney. 2001. Viewing invasive species removal in a
whole ecosystem context. Trends in Ecology and Evolution 16:454459.
Zayed, A., and L. Packer. 2001. High levels of diploid male production in a primitively eusocial
bee (Hymenoptera: Halictidae). Heredity 87:631636.

272
Zayed, A., and L. Packer. 2005. Complementary sex determination substantially increases
extinction proneness of haplodiploid populations. Proceedings of the National Academy
Zayed, A., D.W. Roubik, and L. Packer. 2004. Use of diploid male frequency data as an indicator of pollinator decline. Proceedings of the Royal Society of London Series BBiological
Sciences 271:S9S12.
Zedler, J.B., and J.C. Callaway. 1999. Tracking wetland restoration: Do mitigation sites follow
desired trajectories? Restoration Ecology 7(1):6973.
Zimmerman, M., and G.H. Pyke. 1988. Reproduction in Polemonium: assessing the factors
limiting seed set. American Naturalist 131:732738.

Appendixes


A
Committee Biographies
May Berenbaum (Chair) is Swanlund Professor and head of the Department

of Entomology at the University of Illinois, Urbana-Champaign. Dr. Berenbaum obtained her Ph.D. in ecology and evolutionary biology from Cornell University in 1980 and joined the University of Illinois faculty shortly
thereafter; she currently holds affiliate appointments in the Department of
Plant Biology, the Department of Natural Resources and Environmental
Sciences, and the Program in Ecology and Evolutionary Biology, and at the
Center for Ecological Entomology at the Illinois Natural History Survey.
Her primary research is on chemical mediation of interactions between
plants and herbivorous insects, and her work ranges from the molecular
to the community level. Dr. Berenbaum is a member of the National Academy of Sciences (NAS) and a fellow of several scientific societies, including
the American Academy of Arts and Sciences. Her service to the National
Academies has included two-terms as chair of the Board on Agriculture
and Natural Resources, member of the NAS Council, and member of the
National Research Council Report Review Committee. Dr. Berenbaum
serves on several advisory boards and is currently president of the Board of
Directors of the Xerces Society, an organization dedicated to the conservation of invertebrate animals.
Peter Bernhardt is a professor in the Department of Biology at St. Louis
University and an associate of the Missouri Botanical Garden and the Royal
Botanic Garden of Sydney. He received his Ph.D. in botany from the School
of Botany at the University of Melbourne, Victoria, Australia. Since 1976,
Dr. Bernhardt has done field work in the ecology of animal-pollinated angio275

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sperms in relation to the compatibility (SI) systems. In North America, Dr.

Bernhardts studies have included work on insect-pollinated Erythronium,
Hepatica, Tolmeia, Penstemon, and Xerophyllum spp. His laboratory is
under contract with the U.S. Department of Agriculture Forest Services
(Corvallis, Oregon) to study the pollination of three Potentilla species,
Paeonia brownie, and Cypripedium montanum.
Stephen Buchmann is an adjunct professor of entomology and a research
associate at the Arizona-Sonora Desert Museum and in the Department of
Ecology and Evolutionary Biology at the University of Arizona. He is president and cofounder of The Bee Works, LLC, an environmental consulting
company in Tucson. For 21 years, Dr. Buchmann was a research entomologist with the Carl Hayden Bee Research Center of the U.S. Department of
Agriculture Agricultural Research Service. His research is on conservation
biology, pollination ecology, bee nesting, mating biology and chemical
ecology, buzz pollination of crops, and the oil-harvesting centridine bees
of the New World tropics. He is the author of more than 150 scientific
publications and of 8 books, including The Forgotten Pollinators published
in 1996 with Dr. Gary Nabhan, and Pollinators of the Sonoran Desert,
Pollinator Conservation Handbook, and Letters from the Hive. His first
childrens book is The Bee Tree (Cinco Puntos Press). With Gary Nabhan,
he cofounded and directed the trinational Forgotten Pollinators Campaign
from the Arizona-Sonora Desert Museum. Dr. Buchmann is a research associate in entomology with the American Museum of Natural History in New
York City. He is a fellow of the Linnean Society of London. He serves on the
steering committee of the North American Pollinator Protection Campaign
and as its research chair. Dr. Buchmann routinely works with natural history
film-makers and was associate producer of the 2001 Pollinators in Peril
television documentary, produced by Turner Original Productions and the
National Wildlife Federation.
Nicholas W. Calderone is director of the Cornell University Dyce Laboratory
for Honey Bee Studies. He received his M.S. and Ph.D. from the Ohio State
University. He currently has responsibilities in research, teaching, and extension, and he does work on methods for controlling parasites and pathogens
of honey bees. His research concerns the development of Africanized-free
honey bees that are resistant to parasitic mites and honey bee pathogens.
He spent 7 years with the U.S. Department of Agriculture Agricultural Research Services Bee Research Laboratory in Beltsville, Maryland where he
focused on the biology of Varroa destructor and on the use of integrated
pest management to control parasitic mites in honey bees. Dr.Calderone is
the author of more than 40 peer-reviewed research papers and more than 30

APPENDIX A
277
extension articles on honey bee management. In 2000, he was coauthor of

an article on the value of honey bee pollination to agricultural production
in the United States. He also has developed a master beekeeper program
that serves beekeepers in the northeastern United States.
Paul Goldstein is the assistant curator of Lepidoptera at the McGuire Center
for Lepidoptera and Biodiversity of the Florida Museum of Natural History
in Gainesville. Before moving to Florida, Dr. Goldstein was curator in the
Division of Insects at the Field Museum of Natural History in Chicago, Illinois, where he presided over the Lepidoptera collection and served as a principal investigator in the Pritzker Laboratory for Molecular Systematics. Dr.
Goldsteins research has focused on the evolution of host plant associations
in herbivorous insects, particularly moths, and on conservation genetics
and invertebrate conservation and monitoring programs in prairies, and in
pitch pine and scrub oak barrens, among other unusual plant communities.
Since 1986, Dr. Goldstein has devoted many of his conservation efforts to
the Massachusetts coastline and its offshore islands, where he works on the
conservation genetics of the northeastern beach tiger beetle, the reintroduction of the imperial moth, and the use of assemblages of threatened moths
and butterflies for landscape-level conservation.
David W. Inouye is a professor in the Department of Biology at the University of Maryland, College Park. He was an undergraduate at Swarthmore
College, and he received his Ph.D. in zoology from the University of North
Carolina. He directs the graduate program in sustainable development and
conservation biology at the University of Maryland and teaches courses in
ecology and conservation biology. From 1988 to 1990, he was director of
the University of Colorados Mountain Research Station. Dr. Inouye has
conducted field research at the Rocky Mountain Biological Laboratory
(Colorado) since 1971, where he has studied resource partitioning in bumble
bees, pollination biology, plant demography, and ant-plant mutualisms. His
current work is on long-term studies of variation in the phenology and abundance of flowering by wildflowersto identify the effects of environmental
variables and climate change on flowering and to identify the consequences
for consumers. He also has done research on pollination biology in the
Snowy Mountains in Australia and in Panama. His field work has taken him
to South Africa, Austria, and Costa Rica. Dr. Inouye is coauthor of the book
Techniques for Pollination Biologists. He is a member of the Steering Committee of the North American Pollinator Protection Campaign, a member
of the Task Force on Declining Pollination Services, of the Species Survival
Commission of the IUCN (The World Conservation Union), and secretary
of the Governing Board of the Ecological Society of America.

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APPENDIX A
Peter Kevan is a professor of environmental biology and botany at the University of Guelph, Ontario, Canada. His experience in pollination started
with work in the Canadian High Arctic. Since receiving his doctorate in
1970, Dr. Kevan has worked on pollination ecology in Asia, the Americas,
Africa, Australia, and Europe. He also has worked extensively on natural, agricultural, plantation, and forest pollination problems, with special
emphasis on practical and conservation issues. His research in the 1970s
on the demise of pollinators caused by insecticides in New Brunswick,
Canada, stimulated serious consideration of the consequences of pesticide
use in forestry. He is chair of the Task Force on Declining Pollination of the
IUCN (The World Conservation Union), he is actively involved in pollination initiatives arising from the Convention on Biological Diversity, and he
is a member of the Steering Committee for the North American Pollinator
Protection Campaign.
Claire Kremen is an assistant professor in the Department of Environmental
Science, Policy, and Management at the University of California, Berkeley,
and an associate conservationist with the Wildlife Conservation Society. She
received her Ph.D. in zoology from Duke University and her B.Sc. in biology from Stanford University. Her current work is on the use of biological,
social, and economic data to develop conservation plans that benefit people
and the environment. She has studied an array of topics in conservation biology, including the economics and ecology of ecosystem services, sustainable
forestry, the ecology and biogeography of tropical butterflies, the population
biology of lemurs, and ecological monitoring. Her work reaches from theory
to practice and includes hands-on conservation action. From 1993 to 1997,
she designed and helped to establish Madagascars largest National Park on
the Masoala Peninsula. Her current research examines the functional links
between the spatial distribution of wildlands, the composition of wild bee
communities, farm management practices, and the delivery of pollination
services for agriculture in California and New Jersey. She is leading a National Center for Ecological Analysis and Synthesis working group that uses
models and meta-analysis to identify ways to restore pollination services in
degraded landscapes. She also is working with organizations in Madagascar
to establish a national conservation-planning tool by accumulating data on
species occurrences, developing predictive models of species distributions,
and conducting conservation analyses. She is a scientific advisor for several
conservation organizations and she sits on the editorial board of Conservation Biology. She is a 2001 recipient of the McDonnell 21st Century
Research Award.
Rodrigo A. Medelln is director of the Institute of Ecology at the National
Autonomous University of Mexico. He is also an adjunct professor at

APPENDIX A
279
Columbia University in New York City and an associate researcher at the

Arizona-Sonora Desert Museum. Dr. Medelln has studied and worked on
the ecology and conservation of mammals in Mexico for 25 years. After
completing his undergraduate studies at the University of Mexico he obtained his Ph.D. from the University of Florida. Dr. Medellns work in
rainforests, deserts, and montane forests has included diverse approaches:
community ecology, plant-animal interactions, population biology, and
more recently, molecular ecology. He has produced more than 70 publications, including more than 40 scientific papers in international journals and
6 books and book chapters on bat ecology and conservation, mammal diversity analyses, and conservation of large mammals. Dr. Medelln was head
of the Wildlife Department of the Mexican federal government from 1995
to 1996. He has been president of the Mexican Society of Mammalogists
and has served as chair of the Committee for International Relations. He
currently chairs the Latin American Fellowship Committee of the American
Society of Mammalogists, and has been a member of the Board of Directors
for that society for 6 years and was elected in June 2004 to a third 3-year
term. He is a member of the Scientific Advisory Board of Bat Conservation
International, and he is founder and director of the 10-year-old Program
for the Conservation of Bats of Mexico.
Taylor Ricketts is the director of World Wildlife Fund conservation science
program. His research is on global patterns of biodiversity and threats,
ecological and economic consequences of habitat fragmentation, and interactions between people and nature in agricultural landscapes. Dr. Ricketts
analyzes compiled data sets for insight about the global picture of bio
diversity, how patterns in biodiversity relate to those of human threats,
and how the information can be applied to support conservation efforts.
Dr. Rickettss field studies focus on the value of tropical forest fragments as
sources of wild pollinators for neighboring coffee crops. That project is part
of his long-standing interests in the interactions between habitat fragments
and surrounding agricultural areas and in improving the potential of those
landscapes to support native biodiversity. Dr. Ricketts received his Ph.D.
from Stanford University and has received numerous awards for his work
from the Society for Conservation Biology, the National Science Foundation,
the Summit Foundation, and others.
Gene E. Robinson joined the faculty of the University of Illinois, UrbanaChampaign, in 1989 and is the universitys G. William Arends Professor of
Integrative Biology. He is also the director of the University of Illinois Bee
Research Facility, director of the Neuroscience Program, theme leader at the
Institute for Genomic Biology, and a professor of entomology with affiliate
appointments in the Departments of Cell & Developmental Biology and

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APPENDIX A
Animal Biology and in the Beckman Institute of Science and Technology.

Dr. Robinson obtained his Ph.D. in entomology from Cornell University in
1986. He is the author or coauthor of more than 150 publications, including
articles published in Nature, Science, and the Proceedings of the National
Academy of Sciences. He pioneered the application of genomics to the study
of social behavior, led the effort to gain approval from the National Institutes of Health for sequencing the honey bee genome, and heads the Honey
Bee Genome Sequencing Consortium. Dr. Robinson has been honored as
a University Scholar, Fulbright Fellow, and Guggenheim Fellow. He is a
member of the American Academy of Arts & Sciences and NAS.
Allison A. Snow is a professor of evolution, ecology, and organismal biology
at the Ohio State University in Columbus. Dr. Snow received her Ph.D. in
botany from the University of Massachusetts. She is noted for her expertise
in the evolutionary ecology of plant populations, including breeding systems, pollination ecology, and conservation biology. Dr. Snows research
focuses on hybridization as a stimulus for rapid evolution in weedy and
invasive plants. She has published widely in peer-reviewed journals, and
she has produced several technical reports and book chapters on transgenic
plants, pollination ecology, and gene flow. Dr. Snow is an Aldo Leopold
Leadership Fellow of the Ecological Society of America and is the current
president of the Botanical Society of America. She served on the National
Research Councils Committee on Genetically Modified Pest-Protected
Plants and on the Committee on Biological Confinement of Genetically
Engineered Organisms.
Scott M. Swinton is a professor of agricultural economics at Michigan State
University in East Lansing. Dr. Swinton teaches agricultural production economics, agribusiness operations management, and ecological economics. He
received his M.S. from Cornell University and Ph.D. from the University of
Minnesota. His economic research on agricultural production and environmental management focuses on technology evaluation and policy analysis.
He concentrates on understanding the conditions required for business
profitability to be compatible with environmental stewardship. Dr. Swinton
also is engaged in research on agricultural and natural resource management in Latin America and Africa. He has published more than 45 journal
articles and edited 3 books. He currently serves on the editorial board of
the American Journal of Agricultural Economics.
Leonard B. Thien is a professor in the Department of Cell and Molecular
Biology at Tulane University in New Orleans, Louisiana. He received an
M.S. in botany (systematics and evolution) from Washington University, St.Louis, and a Ph.D. in botany (evolution) from the University of

APPENDIX A
281
alifornia, Los Angeles. Dr. Thiens research is on the pollination biolC

ogy of ancient plants in the ANITA groupthe first three branches of
the flowering plant phylogenetic tree. Dr. Thien has published papers on
the pollination mechanisms and population structure of Amborella (sister
to theangiosperms). He also elucidated the pollination mechanisms and
breeding systems of Illicium and Trimenia (the third branch of the angiosperm cladogram). In North America, Dr. Thiens work includes mosquito
pollination in orchids (Habenaria in northern Wisconsin and Canada), bee
pollination of orchids in the bogs of northern Wisconsin, and beetle and
flypollination of magnolia in the southern United States and Mexico. In
1991, Dr. Thien was elected a fellow of the American Association for the
Advancement of Science for his work on pollination mechanisms in basal
(ancient) angiosperms. Dr.Thien is working with a group of Chinese scientists on the pollination of Schisandra (ANITA group, third branch) in North
America and Southeast Asia. The work involves pollination, construction of
a DNA cladogram, and an analysis of all aspects of the breeding system.
F. Christian Thompson is a research entomologist at the Systematic Entomology Laboratory of the U.S. Department of Agriculture and a scientist
in the Department of Entomology at the Smithsonian Institution. He received his B.S. and Ph.D. from the University of Massachusetts, Amherst.
His research is in the systematics of flower flies (Syrphidae). He also has
expertise on other families of agricultural concern (Anthomyiidae, Asilidae,
Braulidae, Phoridae, and Pipunculidae) and other groups important for
biological control (Pipunculidae, Conopidae). His current research includes
projects on the flower flies of Costa Rica, nearctic flower flies, and genera
of flower flies.

B
Presentations to the Committee
Keck Center, The National Academies

Washington, DC
July 6, 2005
Perspective of sponsoring agencies
Kevin Hackett, U.S. Department of Agriculture, Agricultural Research
Service
William Walker, U.S. Geological Survey
Comments from the North American Pollinator Protection Campaign:
Information sources from NAPPC
Laurie Adams, North American Pollinator Protection Campaign
Workshop on the Status of Pollinators in North America
National Academy of Sciences Building
Washington, DC
October 1819, 2005
SESSION 1: Direct and Indirect Indication of Pollinator Population Size
Databases on pollinators in North America
Terry Griswold, U.S. Department of Agriculture, Agricultural Research
Service
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283
Databases on pollinators in North Americanatural history collections

John Ascher, American Museum of Natural History
Databases on pollinators in North America
Sam Droege, U.S. Geological Survey, Patuxent Wildlife Research Center
Databases on pollinators in North America and the Monarch Watch
Orley Taylor, University of Kansas
Databases on pollinators in Mexico
Ma. del Coro Arizmendi, National Autonomous University of Mexico
Long-term bee survey
Robert Minckley, Rochester University
Xerces Societys red list
Scott Hoffman Black, Xerces Society
SESSION 2: Possible Causes of Pollinator Decline
Effects of climate change on pollinator populations
Jessica Hellmann, University of Notre Dame
Effects of pollinator declines on the ecological genetics of plant
populations
Kent Holsinger, University of Connecticut
Demographic and genetic factors as causes of pollinator decline
Laurence Packer, York University, Canada
Impact of landscape ecology, habitat fragmentation, and agricultural
intensification on pollinator populations
Nick Haddad, North Carolina State University
Impact of invasive species on pollinator populations and the implications
for land and resource management
Diane Larson, U.S. Geological Survey, North Prairie Wildlife Research
Center
Factors that influence population sizes in bumble bees and other members
of the native bee community
Robbin Thorp, University of California, Davis

284
APPENDIX B
Causes and consequences on honey bee decline with emphasis on the

almond industry
Marla Spivak, University of Minnesota, St. Paul
Causes and consequences on honey bee decline
Joe Traynor, Scientific Ag Co.
SESSION 3: Consequences of Pollinator Decline
Consequences of population decline in nectar-feeding bats
Ted Fleming, University of Miami
Effects of pollinator declines on the ecological genetics of plant
populations
Tia-Lynn Ashman, University of Pittsburgh
Environmental Economics of Pollinator Decline
Stephen Polasky, University of Minnesota
Biological and economic factors that impact the overall health of the
honey bee industry
Daniel Weaver, B. Weaver Apiaries and the American Bee Keeping
Federation
Conservation of biodiversity of pollinators in natural and agro ecosystems
Simon G. Potts, University of Reading
Beckman Center, The National Academies
Irvine, CA
January 14, 2006
The current status of the alfalfa leafcutting bee as a pollinator of alfalfa
seed
Ron Bitner, International Pollination Systems
Monitoring schemes and citizen science program for pollinators
Gordon W. Frankie, University of California, Berkeley
Pollination decline: Is it the canary in the mine shaft?
Jerry Hayes, Florida Department of Agriculture and Consumer Services
Economics of pollinator services and potential policy implications
Daniel Sumner, University of California, Davis

C
Recently Extinct Insects
from Around the World
Scientific Name
Coleoptera
Dryophthorus distinguendus
Dryotribus mimeticus
Karocolens tuberculatus
Macrancyclus linearis*
Mecodema punctellum
Megadytes ducalis
Oedemasylus laysanensis
Pentarthrum blackburni
Rhantus orbignyi
Rhantus papuanus
Rhyncogonus bryani
Siettitia balsetensis
Trigonoscuta rossi
Diptera
Campsicnemus mirabilis
Drosophila lanaiensis
Stonemyia volutina
Ephemeroptera
Acanthometropus pecatonica
Pentagenia robusta Robust
Homoptera
Clavicoccus erinaceus
Phyllococcus oahuensis
Lepidoptera
Agrotis crinigera*
Agrotis fasciata*
Agrotis kerri*
Common Name
Weevil [unnamed]
Weevil [unnamed]
Weevil [unnamed]
Weevil [unnamed]
Ground beetle [unnamed] (New Zealand)
Water beetle [unnamed] (Brazil)
Weevil [unnamed] (Hawaiian Islands)
Blackburn weevil
Water beetle [unnamed] (New Caledonia)
Water beetle [unnamed] (New Guinea)
Weevil [unnamed]
Perrin cave beetle
Fort Ross weevil
Longlegged fly [unnamed] (Hawaii)
Vinegar fly [unnamed] (Hawaii)
Volutine stoneyian tabanid fly
Pecatonica River mayfly
Burrowing mayfly [unnamed]
Mealy bug [unnamed]
Aphid [unnamed] Hawaii
Noctuid moth [unnamed]*
Midway noctuid moth*
Kerrs noctuid moth*
285

286
APPENDIX C
Scientific Name
Common Name
Agrotis photophila*
Agrotis procellaris*
Argyresthia castaneela*
Coleophora leucochrysella*
Deloneura immaculate*
Ectodemia castaneae*
Genophantis leahi*
Glaucopsyche xerces*
Lepidochrysops hypopolia*
Levuana irridescens*
Libythea cinyras*
Maculinea alcon arenaria*
Oeobia sp.*
Parnassius clodius strohbeeni*
Scotorythra megalophylla*
Scotorythra nesiotes*
Scotorythra paratactis*
Speyeria adiaste atossa*
Tischeria perplexa*
Odonata
Megalagrion jugorum
Orthoptera
Sympetrum dilatatum
Orthoptera
Conozoa hyalina
Neduba extincta
Plecoptera
Alloperla roberti
Trichoptera
Rhyacophila amabilis
Triaenodes phalacris
Triaenodes tridonata
Noctuid moth [unnamed]*

Procellaris grotis noctuid moth*
Chestnut ermine moth*
Casebearer moth [unnamed]
Hairsteak butterfly [unnamed]*
American chestnut moth*
Looper moth [unnamed]*
Xerces blue*
Hairsteak butterfly [unnamed] (South Africa)
Levuana moth*
Snout butterfly [unnamed] (Mauritius)*
Dutch alcon blue*
Pyralid moth [unnamed]*
Strohbeen parnassian*
Kona giant looper moth*
Koolau giant looper moth*
Hawaiian hopseed looper moth*
Atossa fritillary*
Chestnut clearwing moth*
Jugorum megalagrion damsefly
Dragonfly [unnamed]
Central Valley grasshopper
Antioch Dunes shieldback katydid
Roberts stonefly
Castle Lake caddisfly
Athens caddisfly
Three-tooth caddisfly
*Potential pollinator; species is known to visit flowers for nectar or pollen.

SOURCE: Adapted from http://extinctanimals.petermaas.nl/.

D
Endangered Insects
in the Continental United States
Scientific Name
Common Name
Coleoptera
Batrisodes texanus
Batrisodes venyivi
Brychius hungerfordi
Cicindela ohlone
Heterelmis comalensis
Nicrophorus americanus
Polyphylla barbata
Rhadine exilis
Rhadine infernalis
Rhadine persephone
Stygoparnus comalensis
Texamaurops reddelli
Diptera
Rhaphiomidas terminatus abdominalis*
Lepidoptera
Apodemia mormo langei
Boloria acrocnema*
Callophrys mossii bayensis*
Euphilotes battoides allyni*
Euphilotes enoptes smithi*
Euphydryas editha quino (=E. e. wrighti)*

Glaucopsyche lygdamus palosverdesensis*

Heraclides aristodemus ponceanus*
Icaricia icarioides fenderi*
Icaricia icarioides missionensis*
Lycaeides argyrognomon lotis*
Coffin cave mold beetle

Helotes mold beetle
Hungerford crawling water beetle
Ohlone tiger beetle
Comal Springs riffle beetle
American burying beetle
Mount Hermon June beetle
Ground beetle [unnamed]
Ground beetle [unnamed]
Tooth Cave ground beetle
Comal Springs dryopid beetle
Kretschmarr Cave mold beetle
Delhi Sands flower-loving fly*
Lange metalmark butterfly*
Uncompahgre fritillary butterfly*
San Bruno elfin butterfly*
El Segundo blue butterfly*
Smith blue butterfly*
Wrights euphydryas (Quino checkerspot
butterfly)*
Palos Verdes blue butterfly*
Schaus swallowtail butterfly*
Fender blue butterfly*
Mission blue butterfly*
Lotis blue butterfly*
287

288
APPENDIX D
Scientific Name
Common Name
Lycaeides melissa samuelis*

Manduca blackburni*
Neonympha mitchellii francisci*
Neonympha mitchellii mitchellii*
Pseudocopaeodes eunus obscurus*
Pyrgus ruralis lagunae*
Speyeria callippe callippe*
Speyeria zerene behrensii*
Speyeria zerene myrtleae*
Odonata
Somatochlora hineana
Orthoptera
Trimerotropis infantilis
Karner blue butterfly*

Blackburn sphinx moth*
Saint Francis satyr butterfly*
Mitchell satyr butterfly*
Carson wandering skipper*
Laguna Mountains skipper*
Callippe silverspot butterfly*
Behren silverspot butterfly*
Myrtle silverspot butterfly*
Hine emerald dragonfly
Zayante band-winged grasshopper
*Potential pollinator; species is known to visit flowers for nectar or pollen.

SOURCE: Adapted from http://ecos fws gov/tess_public/SpeciesReport.do?kingdom=I&listingType=L.

E
Bee Species in Decline in North America
Bombus (Bombus) franklini (Frison)

Bombus (Bombus) occidentalis Greene
Bombus (Bombus) affinis Cresson
Bombus (Bombus) terricola Kirby
Bombus (Fervidobombus) sonorus Say
Bombus (Fervidobombus) pensylvanicus (DeGeer)
Epeoloides pilosula (Cresson)
SOURCE: Robbin Thorp, University of California, Davis.
289

F
Meetings and Conferences on
Pollinator Issues 19792006
Event
Sponsor
Location
Date
Publication
PesticidePollinator
Interactions
National
Research
Council
Canada
Toronto,
Ont.
1979
1980
NRCC, 1981
Guelph,
Ont.
April 12,
1986
Winnipeg,
Man.
Proceedings of the
Entomological
Society of
Ontario, 118
(1988)
Agriculture
Canada
United
Kingdom
April
45,
1989
Aug.
1013,
1992
1995
Various, including
1999
Buchmann and
Nabhan, 1996
April
Matheson et al.,
1995
1996
Burlington,
Vt.
Feb. 26,
1997
Alternative Pollinators for

Ontarios Crops
National Workshop on
Bee and Pollination
Research
International Workshop
on Non-Apis Bees
Agriculture
Canada
Tri-National Forgotten
Pollinators Campaign
ArizonaTucson
Desert
Museum
International
Bee Research
Association;
Linnaean
Society
Entomological
Society of
America
Conservation of Bees
Bees and Crop

PollinationCrisis,
Crossroads,
Conservation
U.S. Department Logan, Utah

of Agriculture
Phoenix,
Ariz.
Stubbs and
Drummond,
2001
290

291
APPENDIX F
Event
Sponsor
Location
Date
Publication
Pollinators and Mother

Earth: Global
Perspectives in
Productivity, Diversity,
and Behavior
For Non-Native Crops,
Whence Pollinators of
the Future?
Saving Americas
Pollinators
Entomological
Society of
Canada
Edmonton,
Alta.
Oct.
48,
1997
None
Entomological
Society of
America
National Fish
and Wildlife
Foundation,
Coevolution
Institute,
National
Zoological
Park
Brazilian
Ministry of
Environment
Las Vegas,
Nev.
Nov.
812,
1998
June 18,
1998
Strickler and
Cane, 2003
Oct.
79,
1998
Kevan et al., 2002
Pollinating Bees: The

Conservation Link
Between Agriculture
and Nature
Workshop on Declining
Pollinators
Causes and Extent of

Declines Among Native
Invertebrate Pollinators:
Detection, Evidence and
Consequences
North American
Pollinator Protection
Campaign
International Congress of
Entomology
National Conference on
Pollination Ecology
and Its Contribution
to Conservation and
Biodiversity
FAO International
Pollinators Initiative,
Plan of Action
Washington,
D.C.
So Paulo,
Brazil
None
U.S. Department Logan, Utah

of Agriculture,
U.S. Department
of Interior
National Center Santa
for Ecological
Barbara,
Analysis and
Calif.
Synthesis
May
USGS/BRD/ITR2728,
2000-0007
1999
October
1999
Conservation
Ecology 5
(2001)
Coevolution
Institute
Annually
since
2000
2000
None, but see

http://www.
nappc.org
None
United Nations
Food and
Agriculture
Organization
Washington,
D.C., and
area
Foz Iguazu,
Brazil
Andhra
University,
India
Rome, Italy
Feb.
Souvenir and
2224,
abstracts
2000
published
by Andhra
University,
Visakhapatnam,
Andhra
Pradesh, India
Nov.
See http://www.
1416,
fao.org/
2000

292
appendix f
Event
Sponsor
Protecting and Promoting

Our Pollinators
Entomological
Montreal,
Society of
Que.
Quebec,
Entomological
Society of
Canada,
Entomological
Society of
America
Montreal,
Que.
Managing Biodiversity
in Agricultural
Ecosystems: Convention
on Biological Diversity
First Meeting of the
African Pollinators
Initiative
Pollinators Workshop
So Paulo Declaration on
Pollinators + 5 Forum
International Workshop
on Solitary Bees and
their Role in Pollination
United Nations
Convention on
Biodiversity, Conference
of the Parties, General
Meeting 8
Location
Nairobi,
Kenya
Mabula,
South
Africa
So Paulo,
Brazil
Beberibe,
Cear,
Brazil
Curitiba,
Brazil
Date
Publication
Dec.
36,
2000
None
Nov.
810,
2001
See http://
www.unu.
edu/env/plec/cbd
Feb.
1822,
2002
June
2729,
2003
Oct.
2730,
1998
April
2629,
2004
March
2006
Web site
Eardley et al.,
2006
Kevan and
ImperatrizFonseca, 2002
Freitas and
Pereira, 2004
Pollinators and
Pollination: A
Resource Book
for Policy and
Practice

G
Methods for Analyzing
Status of Pollinators
DIRECT MONITORING
The status of pollinator populations and assemblages can be assessed
in many ways, both direct and indirect. Because a decline is a decrease in
abundance over time, long-term surveys are the most valuable indicators
for assessing pollinator status. The inherent year-to-year variability of
pollinator populations, however, makes trend analysis difficult. Roubik
(2001) surveyed various studies of the population dynamics of 59 bee speciesshort-term projects (24 years) and longer studies (1721 years, all
tropical)and reported that the species mean abundances had varied by
factors of 2.06 for temperate bees and 2.16 for tropical bees (see Appendix
F). Because the natural variability of populations can lead them to halve or
double the average in 1-year intervals, reliable population trends cannot be
determined from short-term studies, and even trends from long-term studies
might not be definitive.
Although direct monitoring of natural populations is invaluable for
identification of pollinator population trends, the ease of use and the accuracy of monitoring techniques differ among species. Some of the best examples of large-scale, long-term monitoring involve birds. Banding records
from research stations and the annual Audubon Christmas Bird Counts
have combined to provide more than a centurys worth of census data on
the birds of North America (http://www.audubon.org/bird/cbc/). Focused
research on a handful of species of particular interestsuch as monarch
butterflies or specific threatened or model species, for examplealso can
provide an accurate picture of population trends (for example, Ehrlich and
Hanski, 2004).
293

294
appendix G
Visual counts can be used effectively for direct assessment of abundance

for vertebrate pollinators, such as bats and hummingbirds. Mist nets can
also be used to capture these flying vertebrates, and their density can be
accurately estimated because the individuals are large enough to be banded
or marked by some other method. Direct assessment of insect pollinator
abundance is typically conducted by observation at the flowers they visit.
Pollinating insects are much more conspicuous when visiting flowers than
they are in transit among foraging areas or when engaged in other activities; for example, ground-nesting bees nests can be difficult to find. One
method is to count all visitors to a set number of flowers, generally of a
single species, during a specified period (typically 10 minutes), when meteorological observations are simultaneously recorded (Kearns and Inouye,
1993). In addition to providing an estimate of pollinator visitation rate, this
method allows a snapshot assessment of the dependence of insect activity on
environmental factors, such as temperature, humidity, wind, and light (for
example, McCall and Primack, 1992). However, one problem with assessing
pollinator populations based on flower visits is that floral abundance and
diversity often vary greatly as well.
An alternative method for estimating insect pollinator abundance
involves counting or collecting individuals along a transect (for example,
1m 25 m, or 1 m for a fixed period), as in a Pollard walk census for butterflies (Caldas and Robbins, 2003), or in a recent survey of bumble bee
populations (Knop et al., 2006). Bees that are not collected can be captured,
marked, and released to distinguish individuals and prevent redundant
counting (Hines and Hendrix, 2005). Netting at flowers along transects in
permanent, one-hectare plots also has been used for native bees (Cane et
al., 2000). Insects that readily adopt artificial nest sitessuch as nest boxes
for bumble bees or trap nests for solitary beescan be monitored by placing the nests in appropriate habitats. A disadvantage of this method is that
adoption rates can be low (as is often the case for bumble bees; Inouye, unpublished). Pollinators that can be manipulated by rewardeuglossine bees
are attracted to terpene-soaked blotter paper (Dodson et al., 1969; Roubik,
1989; Roubik and Hanson, 2004), hummingbirds will consume artificial
nectar from feeders, moths fly to traps baited with fermenting fruitare
more easily monitored than are those that cannot be reliably attracted to a
particular location.
Passive traps that collect insects indiscriminately are not always suitable. Entomologists have long used Malaise traps (screen tents that catch
insects and funnel them up into a collecting head) because they work well for
many kinds of flies. However, the traps rarely capture butterflies, moths, or
bumble bees. The selectivity of pan traps for bees depends on the use of appropriate combinations of trap size, color, and number (S. Droege, Patuxent
Wildlife Research Center, presentation to the committee, October 18, 2005),

295
APPENDIX G
and pan traps can be used to provide reliable population estimates (Russell
et al., 2005). Light traps, which attract insects with mercury vapor lamps
(visible and ultraviolet light) or various short- and long-wave ultraviolet
lights, are also used to sample insect pollinators (some nocturnal bees,
beetles, flies, wasps, moths) in diverse temperate and tropical habitats.
DATABASES
Because direct long-term monitoring studies are so rare, population
patterns over time must be ascertained in other ways. Biological databasestaxonomic and genomic databases and information collected from
conservation-related enterprisescan often be mined for data on historic
patterns of pollinator distribution and, in some cases, abundance.
Specimen databases contain the information associated with vouchers in museum collections. At a miminum, the records show when, where,
how, and by whom particular specimens were collected as well as their
presumptive identifications. Specimen databases also can hold information
about field observations. Museums capture information associated with the
specimens in their collections, usually processing information on the best
known and most widely studied groups first and then moving on to groups
that are less well characterized. It is so widely assumed that mammal and
bird species have been described that discovery of an undescribed primate
genus (Rungwecebus) makes worldwide headlines (Davenport et al., 2006).
In contrast, some groups with greater relevance to pollination, such as flies,
are so diverse that experts cannot even venture a guess as to what proportion
of genera remain to be described.
Specimen databases may be accessible online, and software applications
grant access to all available databases together. The Global Biodiversity Information Facility (GBIF) provides a single interface that queries all online
specimen databases that conform to community standards and protocols.
The GBIF portal provides access to 90 million records from more than 700
collections (http://www.europe.gbif.net/portal/index.jsp). Sample queries
for the honey bee returned 6,362 records from 9 data providers; most
records were from Costa Rica (INBio, 5,920 records). The ruby-throated
hummingbird, in contrast, returned 15,912 records from 9 data providers.
Although specimen databases are optimal sources for trend information,
few museum collections have digital databases of their specimen holdings,
particularly of insects.
Character databases document the characteristics that taxonomists use
to distinguish groups of organisms, primarily for specialists. The information
also can be used to construct interactive identification aids for parataxonomists and citizen-scientists. There are three principal character databases:
MorphBank (http://www.morphbank.net/) and MorphoBank (http://www.

296
appendix G
morphobank.org/) contain morphological characters, and GenBank (http://

www.ncbi.nlm.nih.gov/Genbank/) has DNA sequence characters.
Nomenclatural databases provide information and documentation on
the scientific names of organisms. They provide the correct (valid) names for
species so users have the appropriate search terms for queries in other databases. Like specimen databases, the number of nomenclature databases for
particular groups and areas is increasing, and so is the number of software
applications that consolidate or provide access to them. The Catalogue of
Life, through its annual checklist, provides minimal information on more
than a half-million species; all of that information is integrated with the
services of GBIF as part of the Electronic Catalogue of Life Names of Known
Organisms. The Universal Biological Indexer and Organizer contains approximately 5 million names; the Taxonomic Search Engine searches all
major nomenclators; and the Integrated Taxonomic Information System
provides the official taxonomy of living organisms for the United States,
Canada, and Mexico. Some specialized databases that include pollinator
data are the BioSystematic Database of World Diptera and the Hymenoptera
Name Server.
Species databases provide information and documentation on organisms. Unfortunately, a comprehensive database does not yet exist, although
ultimately, species databases will be transformed into the envisioned Electronic Encyclopedia of Life (Wilson, 2003). Species databases sort information by attributes, such as the pollinators of a given plant, and they provide
summaries about species or links to species web pages.
Literature databases compile published information and they comprise
the same sources used generally for the biological sciences. Literature databases range from general commercial compilations, such as Biological
Abstracts and the Zoological Record, to specialized research databases,
such as AnimalBase, which links digital versions of the early zoological
literature to personally maintained, but publicly accessible databases. One
example is the Pollination Biology Database, maintained by David Inouye
at the University of Maryland.
Conservation-oriented databases exist to track and monitor putatively
threatened populations of animals and plants. Among them are the NatureServe Explorer and the Heritage Program network; the federal database of
species protected by the U.S. Endangered Species Act; and international
lists, such as those from the Convention on International Trade in Endangered Species of Wild Fauna and Flora (www.cites.org/) and the World
Conservation Union (IUCN; www.redlist.org/). The Heritage Program and
NatureServe tracking systems provide a first step in understanding patterns
of decline.
Numerous sources of dataincluding museum collections, naturalists
observations, and accounts published in peer-reviewed literaturecontrib-

APPENDIX G
297
ute to formal rankings of rarity and abundance making them dynamic and
subject to continuing input. In the United States, the Heritage Program
has established a global rank system that denotes global, regional, and
state-specific rarity. The rank of G1, for example, denotes fewer than five
occurrences of a given species or community globally; G2 and G3 represents 620 occurrences and 21100 occurrences, respectively; G4 and G5
denotes apparently abundant globally and demonstrably widely abundant
species globally, repsectively. The state rankings within the United States are
equivalent: S1S5 parallels G1G5. Those data are available to the public
through NatureServe.org.

H
Xerces Society Red List of
Pollinating Insects of North America
A species is placed on the Xerces Society Red List based on consultation with scientists or upon identification by a federal or state agency as
endangered, threatened, or at risk.
TABLE H-1 Lepidoptera, Red List Status and North American
Distribution
Scientific Name
Agathymus evansi
Agathymus mariae
(complex inc.
gilberti)
Amblyscirtes linda
Apodemia mormo
langei*
Atrytone arogos
Boloria
acrocnema*
Common
Name
Status
Canada
Mexico
United States
SO,
CH,
CI
CH, CI
AZ
Huachuca
giant
skipper
Mary giant
skipper
Imperiled
Linda
roadside
skipper
Lange
metalmark
Arogos
skipper
Vulnerable
AR, IL, KS, MO,

OK, TN
Critically
imperiled
Vulnerable
CA
Uncompahgre
fritillary
Critically
imperiled
Data
deficient
NM, TX
AL, AR, CO, FL,

GA, IA, IL, KS,
MN, MO, MS, MT,
NC, ND, NE, NJ,
NY, OK, PA, SC,
TX, WY
CO
298

299
APPENDIX H
TABLE H-1 Continued

Scientific Name
Common
Name
Status
Canada
Alberta
fritillary
Northern
metalmark
Vulnerable
AB, BC
Callophrys
comstocki
Callophrys irus
Desert green
hairstreak
Frosted elfin
Imperiled
Imperiled
ON
Callophrys
lanoraieensis
Bog elfin
Vulnerable
NB,
NS,
ON,
QC
Callophrys mossii
bayensis*
Celotes limpia
San Bruno
elfin
Scarce
streakyskipper
Miami blue
Critically
imperiled
Vulnerable
Boloria alberta
Calephelis borealis
Cyclargus thomasi
bethunebakeri
Erora laeta
Early
hairstreak
Critically
imperiled
Vulnerable
Persius
duskywing
Imperiled
Euchloe ausonides
insulana
Euphilotes
battoides allyni*
Euphilotes baueri
Island marble
Critically
imperiled
Critically
imperiled
Imperiled
Euphilotes enoptes
smithi*
Euphilotes mojave
Euphydryas anicia
cloudcrofti
Mojave
dotted blue
Sacramento
Mountains
checkerspot
Critically
imperiled
Imperiled
Critically
imperiled
United States
MT
Vulnerable
Erynnis persius
persius
El Segundo
blue
Bauer dotted
blue
Smith blue
Mexico
AR, CT, IL, IN, KY,

MD, MO, NJ, NY,
OH, OK, PA, VA,
WV
AZ, CA, CO, NV,
UT
AL, AR, CT, DC,
DE, GA, IL, IN, KS,
KY, LA, MA, MD,
ME, MI, NC, NH,
NJ, NY, OH, OK,
PA, RI, SC, TN,
TX, VA, WI, WV
ME, NH, NY
CA
CI
TX
FL
NB,
NS,
ON,
QC
ON
GA, KY, MA, MD,

ME, MI, NC, NJ,
NY, PA, TN, VA,
VT, WI, WV
CT, IN, MA, MD,
ME, MI, MN, MO,
NH, NJ, NY, PA,
RI, VA, VT, WI
WA
CA
AZ, CA, NV
CA
BN
AZ, CA, NV, UT

NM
continues

300
appendix H
TABLE H-1 Continued

Scientific Name
Euphydryas editha
bayensis*
Euphydryas editha
quino*
Euphydryas editha
taylori
Euphydryas gillettii
Euphyes bayensis
Euphyes dukesi
Euproserpinus
euterpe
Fixsenia [Satyrium]
polingi
Glaucopsyche
lygdamus
palosverdesensis*
Heraclides
aristodemus
ponceanus*
Hesperia dacotae
Hesperia leonardus
montana*
Hesperia ottoe
Hesperopsis
gracielae
Icaricia icarioides
fenderi*
Icaricia icarioides
missionensis*
Lycaeides idas
lotis*
Common
Name
Status
Canada
Mexico
United States
Bay
checkerspot
Quino
checkerspot
Taylor
checkerspot
Gillett
checkerspot
Bay skipper
Dukes
skipper
Critically
imperiled
Critically
imperiled
Critically
imperiled
Vulnerable
CA
BC
OR, WA
AB, BC
ID, MT, UT, WY
Vulnerable
Vulnerable
ON
Kern
primrose
sphinx
moth
Poling
hairstreak
Palos Verde
blue
Critically
imperiled
BN
Imperiled
CA
MS, TX
AL, AR, FL, GA,
IL, IN, KY, LA, MI,
MO, MS, NC, OH,
SC, TX, VA
CA
CI
NM, TX
Critically
imperiled
CA
Schaus
swallowtail
Critically
imperiled
FL
Dakota
skipper
Pawnee
montane
skipper
Ottoe skipper
Imperiled
Macneils
saltbush
sootywing
Fender blue
Vulnerable
Mission blue
Lotis blue
MB,
SK
IA, IL, MN, ND,

SD
CO
MB
CO, IA, IL, IN,

KS,MI, MN, MO,
MT, ND, NE, OK,
SD, TX, WI, WY
AZ, CA, NV, UT
Imperiled
Vulnerable
Critically
imperiled
Critically
imperiled
Critically
imperiled
(possibly
extinct)
BN, BS
OR
CA
CA
continues

301
APPENDIX H
TABLE H-1 Continued

Scientific Name
Lycaeides melissa
samuelis*
Manduca
blackburni*
Mitoura hesseli
Common
Name
Karner blue
Blackburn
sphinx
moth
Hessel
hairstreak
Status
Canada
Critically
imperiled
Critically
imperiled
ON
Vulnerable
St. Francis
satyr
Critically
imperiled
Mitchell satyr
Critically
imperiled
Powesheik
skipperling
Ozark
woodland
swallowtail
Mardon
skipper
Rare skipper
Imperiled
Problema byssus
Byssus
skipper
Vulnerable
Pseudocopaeodes
eunus obscurus*
Carson
wandering
skipper
Laguna
Mountains
skipper
King
hairstreak
Critically
imperiled
Callippe
silverspot
Diana
fritillary
Critically
imperiled
Vulnerable
Neonympha
mitchellii
francisci*
Neonympha
mitchellii
mitchellii*
Oarisma
powesheik
Papilio joanae
Polites mardon
Problema bulenta
Pyrgus ruralis
lagunae*
Satyrium kingi
Speyeria callippe
callippe*
Speyeria diana
Mexico
United States
IL, IN, MI, MN,
NH, NY, OH, WI
HI
AL, CT, DE, FL,

GA, MA, MD, ME,
NC, NH, NJ, NY,
RI, SC, VA
NC
IN, MI, OH
Vulnerable
IA, IL, MI, MN,

ND, SD, WI
AR, MO (KY?)
Imperiled
CA, OR, WA
Imperiled
DE, GA, MD, NC,

NJ, SC, VA
AL, AR, FL, GA,
IA, IL, IN, KS, MO,
MS, NC, OK, SC,
TX, WI
CA, NV
Critically
imperiled
MB
CA
AL, AR, DE, FL,

GA, MD, MS, NC,
TX, VA
CA
AL, AR, GA, IN,
KY, MO, NC, OH,
OK, SC, TN, VA,
WV
continues

302
appendix H
TABLE H-1 Continued

Scientific Name
Common
Name
Status
Canada
Speyeria idalia
Regal
fritillary
Vulnerable
MB,
ON
Speyeria zerene
behrensii*
Speyeria zerene
hippolyta*
Speyeria zerene
myrtleae*
Stallingsia
maculosus
Behren
silverspot
Oregon
silverspot
Myrtle
silverspot
Manfreda
giantskipper
Critically
imperiled
Critically
imperiled
Critically
imperiled
Imperiled
Mexico
United States
AR, CO, CT, DC,
DE, IA, IL, IN, KS,
KY, MA, MD, ME,
MI, MN, MO, NC,
ND, NE, NH, NJ,
NY, OH, OK, PA,
RI, SD, VA, VT, WI,
WV, WY
CA
CA, OR, WA
CA
NL, ?
TX
KEY: Imperiled, at high risk of extinction because of highly restricted range, rare populations
(often 20 or fewer), steep declines, or other factors; data deficient, inadequate information
for assessment of risk category because of a lack of information about population size or
about threats to the population or because of taxonomic uncertainty about the validity of the
taxon; vulnerable, at moderate risk of extinction because of restricted range, relatively rare
populations (often 80 or fewer), recent and widespread declines, or other factors; critically
imperiled, at high risk of extinction because of extreme rarity of populations (often 5 or
fewer), steep declines, or other factors; possibly extinct, missing or known only from historical
occurrences but with some hope of rediscovery.
*Listed under the terms of the U.S. Endangered Species Act.
Listed under the terms of Canadas Species at Risk Act.
SOURCE: Adapted from Shepherd, M.D., D.M. Vaughan, and S.H. Black (Eds). Red List of
Pollinator Insects of North America. CD-ROM Version 1 (May 2005). Xerces Society for
Invertebrate Conservation, Portland, Oregon, http://www.xerces.org/Pollinator_Red_List/
Table_Lepidoptera.htm.

303
APPENDIX H
TABLE H-2 Hymenoptera, Red List Status and North American

Distribution
Scientific Name
Common
Name
Status
Andrena aculeata
Vulnerable
Andrena
winnemuccana
Vulnerable
(data
deficient)
Vulnerable
Vulnerable
Ashmeadiella sculleni
Bombus affinis
(subgenus Bombus)
Bombus franklini
(see also subgenus
Bombus)
Bombus lucorum
(subgenus Bombus)
Bombus occidentalis
(subgenus Bombus)
Bombus terricola
(subgenus Bombus)
Calliopsis barri
Franklin
bumble
bee
Vulnerable
Vulnerable
(data
deficient)
Vulnerable
(data
deficient)
Critically
imperiled
Data
deficient
Vulnerable
(data
deficient)
Vulnerable
Vulnerable
Hoplitis orthognathus
Hoplitis producta
subgracilis
Hylaeus akoko
Columbia River
Basin
OR
OR, NV
CA, OR
Vulnerable
Eucera douglasiana
Halictus
pinguismentus
Hesperapis kayella
United States
Vulnerable
Critically
imperiled
Halictus harmonius
Mexico
Critically
imperiled
(possibly
extinct)
Vulnerable
Epeoloides pilosula
Eucera frater lata
Canada
Critically
imperiled
MB,
ON,
SK
ID, OR
CT, GA, MA, MD,

MI, MT, NC, ND,
NJ, OH, PA, NY,
VA, WI, WV
WA
Columbia River
Basin
CA
BN
ID, NV
ID, OR, NV
Columbia River
Basin
HI
continues

304
appendix H
TABLE H-2 Continued

Scientific Name
Hylaeus anomalus
Common
Name
Anomalous
yellowfaced
bee
Hylaeus anthracinus
Hylaeus assimulans
Hylaeus dimidiatus
Hylaeus facilis
Hylaeus finitimus
Hylaeus flavifrons
Hylaeus gliddenae
Hylaeus hilaris
Hylaeus hula
Hylaeus kona
Hylaeus kuakea
Hylaeus longiceps
Hylaeus lunicraterius
Hylaeus mana
Hylaeus mauiensis
Hylaeus melanothrix
Hylaeus nalo
Easy
yellowfaced
bee
Status
Canada
Mexico
United States
Critically
imperiled
(possibly
extinct)
Critically
imperiled
Critically
imperiled
Critically
imperiled
Critically
imperiled
HI
Critically
imperiled
(possibly
extinct)
Critically
imperiled
Critically
imperiled
(possibly
extinct)
Critically
imperiled
Imperiled
Critically
imperiled
Critically
imperiled
Critically
imperiled
Vulnerable
Critically
imperiled
Critically
imperiled
(possibly
extinct)
Critically
imperiled
Critically
imperiled
(possibly
extinct)
HI
HI
HI
HI
HI
HI
HI
HI
HI
HI
HI
HI
ID
HI
HI
HI
HI
continues

305
APPENDIX H
TABLE H-2 Continued

Scientific Name
Common
Name
Hylaeus niloticus
Hylaeus ombrias
Hylaeus paradoxicus
Hylaeus perspicuus
Hylaeus psammobius
Hylaeus satelles
Hylaeus simplex
Hylaeus solaris
Macropis steironema
opaca
Osmia ashmeadii
Osmia cascadica
Perdita accepta
Perdita barri
Perdita crassihirta
Perdita salicis
euxantha
Perdita salicis
sublaeta
Perdita similis
pascoensis
Perdita wyomingensis
sculleni
Perdita wyomingensis
wyomingensis
Simple
yellowfaced
bee
Status
Canada
Mexico
United States
Critically
imperiled
(possibly
extinct)
Critically
imperiled
Critically
imperiled
Critically
imperiled
(possibly
extinct)
Critically
imperiled
Critically
imperiled
Critically
imperiled
HI
Critically
imperiled
Critically
imperiled
(possibly
extinct)
Critically
imperiled
Vulnerable
Data
deficient
Data
deficient
Data
deficient
Vulnerable
HI
Vulnerable
OR
Vulnerable
WA
Vulnerable
Columbia River
Basin
WY
Data
deficient
HI
HI
HI
HI
HI
HI
WA
OR
OR, WA
OR
ID
WA
ID, OR
continues

306
appendix H
Scientific Name
Protandrena
subdilatipes
Protodufourea
wasbaueri
Sphecodogastra
antiochensis
Common
Name
Status
Canada
Mexico
United States
Vulnerable
WY
Data
deficient
Critically
imperiled
AZ, CA
KEY: Vulnerable, at moderate risk of extinction because of restricted range, relatively rare
populations (often 80 or fewer), recent and widespread declines, or other factors; data deficient,
inadequate information for assessment of risk category because of a lack of information about
population size or about threats to the population or because of taxonomic uncertainty about
the validity of the taxon; critically imperiled, at high risk of extinction because of extreme rarity
of populations (often 5 or fewer), steep declines, or other factors; possibly extinct, missing
or known only from historical occurrences but with some hope of rediscovery; imperiled, at
high risk of extinction because of highly restricted range, rare populations (often 20 or fewer),
steep declines, or other factors.
SOURCE: Adapted from Shepherd, M.D., D.M. Vaughan, and S.H. Black (Eds). Red List of
Pollinator Insects of North America. CD-ROM Version 1 (May 2005). Xerces Society for
Invertebrate Conservation, Portland, Oregon, http://www.xerces.org/Pollinator_Red_List/
Table_Bees.htm.

I
Annual Bee Variability
of Bee Abundances
Family
Genus
Apidae
Apidae
Apis
Centris
Apidae
Apidae
Apidae
Apidae
Colletidae
Halictidae
Halictidae
Megachilidae
Megachilidae
Centris
Euglossini
Euglossini
Meliponini
Ptiloglossa
Megalopta
Rhinetula
Megachile
Osmia
Annual
Variability
Years
Reference
1
1
5.04
1.77
10
4
1
6
32
10
1
2
1
3
1
4.74
1.77
1.36
4.06
2.45
2.15
3.45
2.07
2.46
17
2
20
17
17
17
17
3
23
Roubik and Wolda, 2001

Roubik, 1989; unpublished
data
Pearson and Dressler, 1985
Roubik, 2001
Frankie et al., 1998
Frankie et al., 1998
Species
NOTE: Annual variability in bee abundance was determined from short- and long-term
censuses in two tropical regions (Peru and Panama) and one temperate region (California).
SOURCE: Adapted from Roubik, 2001.
307


PLATE 1 Structure of a flower (Frasera speciosa, Gentianaceae; visited by the

bumble bee Bombus flavifrons). Photo by David Inouye, University of Maryland,
CollegePark.

PLATE 2 Pollinating insects, clockwise

from top left: honey bee (Apis mellifera,
photo by S. Buchmann, University of
Arizona, Tucson); sphinx moth (Hyles
lineata, photo by W. May); yucca moths
(Tegeticula yuccasella, photo by W.
May); a fly (Bombyliidae, photo by D.
Inouye, University of Maryland, College
Park).

PLATE 3 Lesser long-nosed bat (Leptonycteris nivalis), a mammalian pollinator (photo

Merlin D. Tuttle, Bat Conservation International, reprinted with permission).

PLATE 4 Hummingbird, an avian pollinator (photo by W. May).
Outline for Report n2
1. Introduction
2. Material & methods
EFSA Report 1 (inventory)

EFSA networks (AFSCO, AHAW, EMRISK, GMO, PLH, PRAS)
COLOSS network
DG-Research (and DG-ENV) projects (Directorate General)
EFSA Colloquium n18 on bees (May 2013)
3. Results
3.1. ToR 2a State of the art of the work carried out outside EFSA in the area of bees
and RA
Projects from networks

Projects from EC-DGs
Projects from DG-Colloquium (Discussion Groups)
3.2. ToR 2b Gap analysis on the data collected inside and outside EFSA in order to
highlight cross-cutting issues, risk assessment and data gaps
Inside: EFSA Report 1 and bibliometric analysis (tbc)

Outside: feedback from DG-Colloquium
4. Conclusions and recommendations: ToR 2c
Summarise recommendations (e.g. per identified area/discussion group)

Make recommendations on cross-cutting issues (e.g. RA approach in GMO/Pesticides),
horizontal scientific collaborations across units, DG-Research, EFSA Grant Scheme,
etc.
SAP Minutes No. 2012-06
A Set of Scientific Issues Being Considered by the

Environmental Protection Agency Regarding Pollinator Risk
Assessment Framework
September 11 14, 2012

FIFRA Scientific Advisory Panel Meeting
Held at the
Environmental Protection Agency Conference Center
Arlington, VA
NOTICE
These meeting minutes have been written as part of the activities of the Federal Insecticide,
Fungicide, and Rodenticide Act (FIFRA), Scientific Advisory Panel (SAP). The meeting
minutes represent the views and recommendations of the FIFRA SAP, not the United States
Environmental Protection Agency (Agency). The content of the meeting minutes does not
represent information approved or disseminated by the Agency. The meeting minutes have not
been reviewed for approval by the Agency and, hence, the contents of these meeting minutes do
not necessarily represent the views and policies of the Agency, nor of other agencies in the
Executive Branch of the Federal Government, nor does mention of trade names or commercial
products constitute a recommendation for use.
The FIFRA SAP is a Federal advisory committee operating in accordance with the Federal
Advisory Committee Act and established under the provisions of FIFRA as amended by the
Food Quality Protection Act (FQPA) of 1996. The FIFRA SAP provides advice, information,
and recommendations to the Agency Administrator on pesticides and pesticide-related issues
regarding the impact of regulatory actions on health and the environment. The Panel serves as
the primary scientific peer review mechanism of the Environmental Protection Agency, Office of
Pesticide Programs (OPP), and is structured to provide balanced expert assessment of pesticide
and pesticide-related matters facing the Agency. FQPA Science Review Board members serve
the FIFRA SAP on an ad hoc basis to assist in reviews conducted by the FIFRA SAP. Further
information about FIFRA SAP reports and activities can be obtained from its website at
http://www.epa.gov/scipoly/sap/ or the OPP Docket at (703) 305-5805. Interested persons are
invited to contact Fred Jenkins, Jr., Ph.D., SAP Designated Federal Official, via e-mail at
jenkins.fred@epa.gov.
In preparing these meeting minutes, the Panel carefully considered all information provided and
presented by EPA, as well as information presented by public commenters.
TABLE OF CONTENTS
PARTICIPANTS ...................................................................................................................6
INTRODUCTION .................................................................................................................9
PUBLIC COMMENTS ..........................................................................................................10
SUMMARY OF PANEL DISCUSSION AND RECOMMENDATIONS ...........................11
DETAILED PANEL DELIBERATIONS AND RESPONSE TO CHARGE .......................40
REFERENCES ......................................................................................................................98
Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA)

Scientific Advisory Panel (SAP)
Pollinator Risk Assessment Framework
September 11 14, 2012
PARTICIPANTS
FIFRA SAP Chair
Daniel Schlenk, Ph.D.
Professor of Aquatic Ecotoxicology & Environmental Toxicology
Department of Environmental Sciences
University of California, Riverside
Riverside, CA
Designated Federal Official
Fred Jenkins, Jr., Ph.D.
US Environmental Protection Agency
Office of Science Coordination & Policy
FIFRA Scientific Advisory Panel
EPA East Building, MC 7201M
Phone (202) 564-3327
Fax (202) 564-8382
jenkins.fred@epa.gov
FIFRA Scientific Advisory Panel Members
Kenneth Delclos, Ph.D.
Pharmacologist
National Center for Toxicological Research
U.S. Food and Drug Administration
Jefferson, AR
Stephen Klaine, Ph.D.
Professor & Director
Environmental Toxicology & Biological Sciences
Clemson Institute of Environmental Toxicology
Pendleton, SC
Martha Sandy, Ph.D.

Senior Toxicologist & Chief
Cancer Toxicology & Epidemiology Section
Reproductive and Cancer Hazard Assessment Branch
Office of Environmental Health Hazard Assessment
California Environmental Protection Agency
Oakland, CA
James McManaman, Ph.D.
Professor & Chief
Section of Basic Reproductive Sciences
Department of Obstetrics & Gynecology, Physiology & Biophysics
University of Colorado, Denver
Aurora, CO
FQPA Science Review Board Members
May Berenbaum, Ph.D.
Professor & Department Head
Department of Entomology
University of Illinois at Urbana-Champaign
Urbana, IL
Nina Fefferman, Ph.D.
Associate Professor
Department of Ecology, Evolution & Natural Resources
The Center for Discrete Mathematics & Theoretical Computer Science
Rutgers University
New Brunswick, NJ
Greg Hunt, Ph.D.
Professor
Purdue University
West Lafayette, IN
Rosalind James, Ph.D.
Research Leader
Pollinating Insect-Biology, Management & Systematics Research Unit
US Department of Agriculture-Agricultural Research Service
Department of Biology
Utah State University
Logan, UT
Nancy Ostiguy, Ph.D.

Associate Professor
Pennsylvania State University
University Park, PA
Jeff Pettis, Ph.D.
Research Leader
Bee Research Laboratory
Beltsville, MD
Mr. Jens Pistorius
Scientist
National Examination Centre for Bee Poisoning Incidents
Julius Khn InstituteFederal Research Centre for Cultivated Plants
Institute for Plant Protection in Field Crops and Grassland
Julius Khn-Institut (JKI) [Institut fr Pflanzenschutz in Ackerbau und Grnland
Braunschweig, Germany
Thomas Potter, Ph.D.
Research Chemist
Southeast Watershed Laboratory
Tifton, GA
Arthur P. Schwab, Ph.D.
Professor
Department of Soil & Crop Sciences
Texas A&M University
College Station, TX
David Tarpy, Ph.D.
Associate Professor & Extension Apiculturist
North Carolina State University
Raleigh, NC
INTRODUCTION
On September 11-14, 2012, the United States (US) Environmental Protection Agency (EPA)
convened a public meeting of the FIFRA Scientific Advisory Panel (SAP) to address scientific
issues associated with the Office of Pesticides Programs (OPP) proposed Pollinator Risk
Assessment Framework. Several sources have reported declines in certain pollinator species
globally. A number of factors/agents have been hypothesized as potential contributors to recent
declines in honey bee health in general. Currently, no factor has been identified as the single
cause. Rather, the available science suggests that pollinator declines are a result of multiple
factors which may be acting in various combinations. The purpose of this SAP was to advise
OPP on the proposed Pollinator Risk Assessment Framework which focuses on a tiered process
for quantitatively evaluating the potential risk to pollinators (using honey bees, Apis mellifera, as
a surrogate) associated with the registered use of both systemic and non-systemic pesticides and
the exposure and effects data needed to support that process. During this SAP, the US EPA
provided an overview of the proposed process for quantifying potential risks of pesticides to
honey bees. This overview reflected OPPs collective efforts with the Pest Management
Regulatory Agency (PMRA), and the California Department of Pesticide Regulation (CalDPR).
Opening remarks at the meeting were provided by:
Steven Bradbury, Ph.D. (Director of the Office of Pesticide Programs)
EPA; Donald Brady, Ph.D. (Director of the Environmental Fate and Effects Division (EFED))
US EPA presentations were provided by the following staff:
Reuben Baris, MS
Joseph Decant, MS
Kristina Garber, MS
Thomas Moriarty, MS
Keith Sappington, MS
Thomas Steeger, Ph.D.
Christina Wendell, MS
Presentations from the Pest Management Regulatory Agency (PMRA), Health Canada and the
California Department of Pesticide Regulation, California Environmental Protection Agency
(CAL, EPA) were provided by:
Mary Mitchell (PMRA)
Richard Bireley (CAL EPA)
Public Comments
Public comments were provided by (listed in order of that they presented):
Dr. Ray McAllister, Dr. David Fischer, and Dr. Jay Overmyer on behalf of CropLife America
Mr. Pierre Petelle and Maria Trainer on behalf of CropLife Canada
Mr. William Kelly on behalf of the Center for Regulatory Effectiveness
Mr. Scott Schertz on behalf of the National Agricultural Aviation Association
Mr. Peter Jenkins on behalf of the Center for Food Safety
Ms. Nichelle Harriet on behalf of Beyond Pesticides
Mr. James Doan on behalf of Doan Family Farms
Dr. Michael Beavers on behalf of the California Agricultural Research Inc.
Mr. Rod Synder on behalf of the National Corn Growers Association
Mr. Steven McFadden of Independent Scientific Research Advocates on behalf of themselves
10
Summary of Panel Recommendations

1. Section 2.2.1 of the white paper discusses the protection goals and associated assessment
endpoints for assessing risks to honeybees (Apis mellifera). The protection goals are:
protection of pollination services;
protection of honey and hive product production; and,
protection of pollinator biodiversity.
As described in the white paper, assessment endpoints are based on their ecological relevance,
their susceptibility to known or potential stressors and their relevance to protection goals.
a. Please comment on whether the assessment endpoints (e.g., population size and stability of
managed bees, quantity and quality of hive products, and species richness and abundance)
identified in Table 1 in Section 2.2.1 of the white paper are consistent with the Agencys
protection goals. Please include a discussion of any additional assessment endpoints that may
be necessary to meet those protection goals.
Panel Summary
Overall the Panel believes that the Agency did an excellent job in writing the white paper. In
regard to the assessment endpoints listed in Table 1 of the white paper, the Agency should clarify
the terminology in this Table. For example, managed bees should be clearly defined as
commercial bees including bumble bees, alfalfa leafcutting bees, mason bees, and any other bee
species that may become managed in the future. Also the term population size is not explicitly
characterized in Table 1. Thus, the Panel recommends that this term be specifically defined as
the numbers of colonies.
The Panel also believes that the Agencys protection goal of contribution to pollinator
biodiversity is too broad. This is because pollinators are comprised of very large numbers of
organisms including many bee species and other pollinating insects (i.e. some butterflies, pollen
wasps, pollen beetles, etc.) and animals (i.e. some birds, and bats). Considering the large number
of different pollinators and taking into account the focus of the Agencys white paper, the Panel
advises that the Agency revise this protection goal to be contribution to bee diversity.
11
b. Please comment on whether the measurement endpoints at the level of the colony (e.g., colony
strength and survival, contamination of pollen and nectar and species richness and
abundance) identified in Table 1 are consistent with the assessment endpoints identified in the
table and any additional assessment endpoints discussed in Part a of this question. Please
include a discussion of any additional measurement endpoints that may be necessary to
represent those assessment endpoints.
Panel Summary
Regarding the measurement endpoint colony strength, the Agency should take note of the fact
that 98% of native bee species are solitary, and thus a colony measurement endpoint does not
include solitary bees. The Panel believes that this endpoint is acceptable for use as long as this
caveat is considered. The Panel advises the Agency to add colony development as a
measurement endpoint along with colony strength and survival. The Panel also recommends that
the Agency explicitly identify pesticide residues in honey, pollen, wax, propolis, and royal jelly
as a measurement endpoint.
The assessment endpoint of species richness and abundance is an appropriate goal for
assessment; however, the measurements associated with this endpoint are not described in the
white paper. Moreover, the Panel notes that there is no means of assessing species diversity
using only one surrogate species, the honeybee. It is also important to note that the honey bee is
a domesticated organism that is not native to the Americas. Furthermore, a substantial amount of
research indicates that the presence of honeybees can have a harmful impact on native species of
bees (Badano, 2011, Dohzono, 2010, Thomson, 2006 & 2004, Roubik, 2001, & Schaffer, 1983).
The Panel also recognizes that within-species richness and diversity is a good assessment
endpoint to address. Thus, the Panel suggests that the Agency explore measurement of genetic
variation within the species as an approach for assessing species richness and diversity. Genetic
population modeling reveals genetic variation within a species and can be a valuable means of
determining long term effects to population size.
c. Please comment on whether the measurement endpoints at the level of the individual bee (e.g.,
individual adult and larval [brood] survival, queen fecundity, brood emergence success,
worker longevity) identified in Table 1 are consistent with assessment endpoints identified in
the table and any additional assessment endpoints discussed in Part a of this question.
Please include a discussion of any additional measurement endpoints that may be necessary
to represent those assessment endpoints.
Panel Summary
The Panel agrees that individual worker survival is a useful individual measurement. In addition,
the Panel recommends that the Agency conduct larval survival assays. These assays will serve
an important role in ascertaining more subtle effects of pesticides on bees. The Panel also
recommends for the sake of clarity that the term brood success in Table 1 be replaced with
larval survival, delayed development and pupal survival. An additional term that should be
12
renamed to provide more clarity is brood size. Brood size should be changed to brood nest
size (defined as the area of the sealed brood in a colony). Queen fecundity (the total number
eggs laid in a defined time period) is another useful endpoint, but it is difficult to measure.
Queen reproductive success (the size and quality of the brood nest, or survival of eggs through
the larval, pupae and adult stage) is a superior endpoint. In regard to worker bee longevity as a
measurement endpoint, the Panel notes that it is difficult and unreliable to measure and therefore,
not recommended.
2. Section 2.2 of the white paper discusses a series of conceptual models for assessing risks of
honeybees resulting from pesticide applications. These models depict the nature of the
stressor (i.e., nonsystemic and systemic pesticides that are applied as foliar treatments, soil
and/or seed treatments, or trunk injection), its source (e.g., direct deposition on bees or
pollen), the exposure media (e.g., residues on plants, residues in/on pollen/nectar), receptors
(e.g., foraging bees, developing brood) and attribute changes (e.g., reduced [bee] population,
reductions in the quantity/quality of honey).
a. Please comment on whether the conceptual models depicted in Figures 4 through 8 are
consistent with the protection goals and assessment endpoints identified in Table 1 and
discussed in Question 1.
Panel Summary
The Panel believes that the Agencys conceptual models effectively assess pollinator risk while
providing considerable detail. However, the Panel recommends some revisions. Examples
include the potential receptor pathway/exposure route via wax and propolis specifically during
the larval stage and the potential exposure due to consumption or contact with pesticide
contaminated water, soil, and dust. Other suggested revisions are identified in Figures 4-9 of the
Detailed Panel Deliberations and Response to Charge section of this report.
13
3. The focus of the white paper and proposed risk assessment process on the honeybee reflects
two important factors: 1) honeybees are considered one of the most important pollinators
globally from both a commercial and ecological perspective; and 2) standardized test methods
for evaluating exposure and effects of chemicals in a regulatory context are more developed
with the honey bee compared to non-Apis bees. Both the Introduction (Section 1) and the
Problem Formulation sections (Section 2) of the white paper indicate that honey bees have
historically served as a surrogate for other beneficial insects. As discussed in Section 5.3 of
the white paper, there is uncertainty regarding the extent to which honey bees serve as
surrogates for native species, especially where life history strategies and differential
sensitivity across species render native species more or less vulnerable to pesticides.
a. Please comment on the extent to which the assessment of risks to the honey bee may serve to
meet the protection goals identified in the white paper (i.e., protection of pollination services;
protection of honey and hive product production; and protection of pollinator biodiversity).
b. Until guidelines are developed for testing non-Apis species of bees, please comment on the
extent to which the honey bee may or may not serve as a reasonable surrogate for non-Apis
bees, given the differences in life history strategies and potential different sensitivities to
pesticide toxicants. Please include a discussion of which types of non-Apis bees may be
particularly well represented by either the individual-level or colony level endpoints identified
in Table 1 of the white paper; as well as which types of non-Apis bees may not be as well
represented, and therefore, may be the focus of potential areas for future research.
Panel Summary
Subparts Questions 3a. and 3b. are closely connected; therefore, the Panel prefers a joint
response to them. The Panel believes that honey bees are a reasonable surrogate. They are
easier to obtain than most other bees, and testing methods are more readily available. However,
if honey bees are to serve as a surrogate species, the Agency must recognize that this species is
merely a representative of other bee species. It is important to consider the differences between
honey (Apis mellifera) and other bees. For example, some non-Apis bees may consume
proportionately more pollen and less nectar. If pesticide residues in pollen are dissimilar from
nectar residues these differences in consumption rates may impact dietary exposure estimates.
Also, honey bees do not frequent soil while other bees do. For example, many solitary bees
build nests with soil; thus they may be exposed to pesticide residues in soil. The Agencys white
paper does not have risk diagrams that take into account this potential exposure pathway when
non-systemic pesticides are applied to the soil (See Panel Proposed Figure 8 in Question 2 Part a.
of the Detailed Panel Deliberations and Response to Charge Section). In addition contact
toxicity assessments for other soil applied pesticides are lacking. An additional consideration
that the Agency should address is that honey bees have the capability of recruiting more workers
from the young nurse bees, if necessary. In the case of solitary bees, all females are queens.
Thus, adult mortality could have a greater impact on these bee populations in the following year
than would be the case for honey bees.
The Agency may want to consider testing which entails other bee species. The commercially
available alfalfa leafcutting bee, Megachile rotundata and Osmia spp. (mason and orchard bees)
14
would likely be relatively easy to include in Tier I testing. Bumble bees (also commercially
available) (Bumbus spp.) may be appropriate for use in Tier II tests although it would be difficult
to assess larval development and brood size or larval mortality. The Panel recommends that the
Agency require testing on at least one additional species to address the stated goal of protecting
diversity.
4. Contact Exposure. The exposure characterization of the white paper (specifically, Section
3.1.1.2) proposes a screening-level (Tier I) approach for quantifying contact exposure to
foraging bees for pesticides applied via foliar spray. This proposed method is based on the
maximum of residue values on honey bees from a field study conducted by Koch and Weisser
(1997). The white paper also discusses a method based on the T-REX (Terrestrial Residue
Exposure model) upper-bound concentration for arthropods directly sprayed with pesticides
while located directly on a treated field. Although the second method is not proposed for the
Tier I exposure assessment for honey bees, it could be used to assess contact exposures to
other insect pollinators.
a. Please comment on the strengths and limitations of the proposed approach for assessing
contact exposures to honey bees in Tier I exposure assessments (i.e., 2.7 g a.i./bee per 1 lb
a.i./A), which is based on the honey bee specific maximum concentration reported by Koch
and Weisser (1997).
Panel Summary
The Panel agrees that contact exposure is likely a significant pesticide exposure pathway. The
approach described in the white paper for determining contact toxicity has many merits. It also
has several limitations. Given the general lack of actual contact exposure data, a model appears
necessary to estimate contact exposures. An example of the strength of the modeling approach
described is that the concentration reported was the highest value (normalized). Consequently,
this value should be protective. Major weaknesses of this approach are that the primary study is
15 years old and investigators did not use a formulated pesticide to evaluate exposure. Followup studies may be needed to assess study relevance and validity.
b. Please comment on the potential utility of the T-REX upper-bound residue value (i.e., 12 g
a.i./bee per 1 lb a.i./A), for a broader number of arthropod species to represent contact
exposures to honey bees and to other insect pollinators that are directly sprayed with
pesticides.
Panel Summary
A primary strength of T-REX is that the data that the model uses were derived from pesticide
residue measurements on arthropods thus they are expected to be similar to what might be
expected for both honey and non-Apis bees. A main weakness is that T-REX was developed
using data from only carbamate and organophosphate insecticides. Other pesticides, e.g. the
neonicotinoids, have different chemical properties and are applied in different ways; thus they
may respond differently. Studies are needed to assess the potential differences in the magnitude
of residues as a function of pesticide and formulation properties and mode of application.
15
Overall, considering the strengths and weakness of the T-REX approach, the Panel supports use
of this model as a means of estimating the interception of a pesticide during a spray application
to a crop. One panel member also recommends that the Agency considers a more direct
approach to assessing potential exposure based on the surface area of adult honey bees. Values
in the 2.4 cm-2 per bee range have been reported in the literature (Roberts & Harrison, 1999).
Exposure estimates can be derived by multiplying the surface area times the spray rate. Some
consideration for the rate of spray interception may also be included in the calculation. Using
the default value of 100% interception will result in exposure estimates with a factor of 2X of the
exposure estimates derived with the TREX model.
5. Dietary Exposure (Consumption Rates). As discussed in the effects assessment section of
the white paper (Section 4.1), acute oral toxicity data (LD50) are necessary for adult and larval
bees in order to characterize the potential risks of a pesticide. Because these toxicity data are
expressed on a dose basis (i.e., g a.i./bee), it is necessary to convert estimated concentrations
of pesticides in food (expressed as mg a.i./kg) into doses. Honey bees fulfill their nutritional
requirements through consumption of nectar, honey, and bee bread (pollen/honey). In addition
to requiring bee bread and nectar or honey, bees also require royal jelly and brood food (jelly)
to fulfill their nutritional requirements. In the proposed approach, it is assumed that exposures
through consumption of nectar and pollen are conservative representations of potential
exposures through consumption of honey and bee bread, respectively. This approach is likely
to be conservative because it assumes that pesticides do not degrade while honey and bee
bread are stored in the hive and have undergone some degree of processing (e.g.,
fermentation). For bees that consume honey, it is assumed that the estimated pesticide
exposures can be related back to the original concentration in nectar by accounting for the
amount of sugar consumed by bees. It is also assumed that pesticide exposures through
consumption of pollen and nectar are protective of pesticide through consumption of royal
jelly and brood food given that empirical data indicate that pesticide concentrations in royal
jelly are >100 times lower than concentrations in food consumed by nurse bees. In the
proposed approach, pesticide doses received by bees are calculated using nectar and pollen
consumption rates for larval and adult worker bees. As discussed in detail in Appendix 1 of
the white paper, the proposed values for larvae and adult workers are based on an analysis
conducted by EPA, which built upon work published by Rortais et al. (2005), Crailshaim et
al. (1992 and 1993) and others. For larvae, the proposed total food consumption rate is 120
mg/day, which is based on the total daily consumption of pollen and nectar (based on honey
consumption) by larvae during day 5 of the uncapped larval life stage. For adult worker bees,
the proposed food consumption rate is 292 mg/day, based on food consumption rates of nectar
foraging bees, which are expected to receive the greatest dietary exposures among different
types of worker bees. In addition, as discussed in Appendix 1, it is likely that these food
consumption rates are protective of drones and queens.
16
a. Although bee larvae typically consume processed foods in the form of royal jelly and brood
food throughout much of their development, they also consume honey and pollen during the
last two days of the uncapped period. Please comment on the proposed use of nectar and
pollen consumption rates of larvae during the last day of the larval developmental stage.
Please include a discussion of the conservatism, strengths and limitations of this approach as
well as a discussion of how this value may or may not correspond to data generated from
larval toxicity endpoints.
Panel Summary
The Panel generally concurs that unprocessed pollen and nectar consumption represents a worst
case scenario as well as a conservative estimate when compared to processed foods such as
brood food and royal jelly. Regarding larval assays, as demonstrated by published literature
larval tests can be done using dilute royal jelly as food. Further, spiking royal jelly with
pesticides will allow the larvae to be orally exposed. Although the Agencys proposed method
appears conservative the Panel questions the Tier I laboratory larval feeding concentrations. As
identified in the white paper the Agency assumes that pesticide residue concentration in royal
jelly is 100-fold lower than in the pollen and nectar that a bee ingests to prepare royal jelly. The
Panel recommends using the original estimated adult ingestion concentration because the 100fold lower value used for royal jelly was derived from a small number of measurements. There
is relatively high uncertainty in concentration estimates associated with this small sample size.
Concerning larval food intake, the Agency assumes an intake value of 120 mg per day. This is
likely a highly conservative value. As indicated in published studies, larvae of the first up to the
last larval stages would consume less food. The Panel also notes regarding food consumption
that the total food consumption during the larval stage may be the most appropriate means of
estimating exposure. This approach would likely provide a more accurate pesticide exposure
estimate of both honey and non-Apis bee larvae. The Panel notes that honey and solitary bee
larvae have 7 and 1 day time periods respectively over which food is collected for larval
consumption.
b. Please comment on the strengths and limitations of basing the Tier I screen for adult honey
bees on food consumption rates of nectar foraging bees, including a discussion of the
conservatism of this approach, and how it relates to other types of worker bees and castes.
Panel Summary
Panel members believe that Tier 1 screening using nectar consumption only is generally
appropriate. However, this approach may not be for newly-emerged bees since these young bees
may consume very large amounts of pollen or nectar. Since Tier I studies generally use random
aged bees exposure estimates based on nectar consumption appears appropriate. The Panel notes
that the proposed value for nectar consumption, 292 mg per day will likely be highly protective
for nectar consumption of non-Apis species.
The Panel notes that since queens and drones do not normally feed themselves and are fed by
worker bees, the proposed Tier I food consumption values are likely acceptable for determining
LD50 values. However, the Panel advises the Agency to also consider the high daily feeding rate
17
of the queens. This may result in much higher exposure when compared to the workers alone.
To some degree this is moderated by lower pesticide concentration levels in the brood food fed
to the queens. With regard to adjusting for castes and species differences, the Panel recommends
computing exposure as a function of bee weight as opposed to a per bee basis, as is done in the
white paper.
c. Please comment on the assumption that exposures through consumption of nectar and pollen
are conservative representations of potential exposures through consumption of honey, bee
bread, brood food and royal jelly, all of which represent processed foods.
Panel Summary
The Panel agrees that the proposed nectar and pollen consumption rates provide conservative
representations of exposure levels compared to processed brood food (honey and bee bread) and
royal jelly. However, the Panel notes that this conclusion is not easily extrapolated to non-Apis
native bees because their larvae receive provisions of pollen and relatively little nectar.
Additionally, native bee larvae are not fed brood food or royal jelly.
6 Dietary Exposure. The dietary exposure methods described in Section 3.1 of the white paper
differ in the nature of the estimated concentrations in pollen and nectar consumed by bees. For
foliar spray applications, the proposed approach involves the use of the tall-grass residue
value from the T-REX model (v. 1.5) as a surrogate for pesticide concentrations in nectar and
pollen. For soil treatments, the white paper proposes the use of the Briggs model, which is
designed to estimate pesticide concentrations in plant shoots resulting from plant uptake of
pesticides from treated soil. Estimated pesticide concentrations in plant shoots are proposed
as a surrogate for concentrations in pollen and nectar. For seed treatments, the white paper
proposes the use of the International Commission for Plant-Bee Relationships (ICP-BR) 1
mg a.i./kg concentration as an upper-bound concentration in nectar and pollen. The paper
explores the strengths and limitations of each method relative to the ability to derive
reasonably conservative estimates of pesticide exposures to bees, with a focus on how well the
estimates relate to empirically based measures of pesticides in pollen and nectar from crops
treated with pesticides.
a.
Foliar spray: Please comment on the analysis presented in Section 3.1.1.1, with a focus on
the extent to which the T-REX tall-grasstall-grass upper-bound residue may serve as an
adequate surrogate to represent upper-bound pesticide concentrations in pollen and nectar
of flowers that are directly sprayed with pesticides.
Panel Summary
The Panel believes that due to the limited amount of data on pollen and nectar pesticide residues,
the T-REX or other models are needed to predict upper-bound pesticide concentrations in these
exposure media. The Panel strongly recommends a focused effort to collect more residue data
on pollen and nectar to determine whether the T-REX estimates are an appropriate surrogate for
these materials. The Panel notes several strengths and weaknesses associated with the use of TREX. Examples of these strengths and weaknesses include:
18
Strengths
T-REX is a model currently endorsed and used by US EPA in Tier I studies.

The model was developed using experimental (empirical) observations on stems of plants
in 11 direct spray studies.
Weaknesses
Residue data on nectar and pollen data are limited. Thus, there is difficulty and high
uncertainty associated with determining whether T-REX serves as an appropriate
surrogate for assessing residue values.
Linear extrapolation to 1 lb a.i./acre has not been validated. Changes may be non-linear.
Crop specific factors are not accounted for including differences in plant surface
composition and characteristics of grass stems (T-REX model) that impact pesticide
retention and other plant parts (e.g. blossoms).
b. Soil applications: Please comment on the analysis presented in Section 3.1.2, with a focus on
the extent to which the Briggs model may generate estimates of pesticide exposure in plant
stems that can represent upper bound pesticide concentrations in pollen and nectar of
flowers.
Panel Summary
The Briggs model has several strengths, uncertainties, and weaknesses. A few examples of
these include:
Briggs Model Strengths:
The Briggs, among available plant uptake equations, was determined by the United
Kingdoms Environmental Agency to represent the best fit to empirical data.
This model is used in other Agency models such as PRZM.
The range in log Kow values, -0.57 to 4.6, used to derive the Briggs equation includes a
large number of pesticides including the neonicotinoids.
Briggs Model Weaknesses:
The model examines nonionic compounds only. Pesticides that ionize will not be well
represented by this approach.
Pesticides tested were limited to carbamates and phenyl-ureas and only one plant species
(barley). It is unknown whether the model holds for other pesticides or plants.
Soil parameters used in the Ryan modification may not be known, particularly soil
moisture content. The fact that other parameters like bulk density and foc are spatially
dependent will also add uncertainty to results.
19
Burken and Schnoor (1998) assessed the Briggs model using another plant species and a much
broader array of chemicals. The Panel recommends the Burken and Schnoor (1998) analysis of
the Briggs model be incorporated into the Agencys evaluation.
c. Soil applications: Please discuss the relative strengths and limitations of the 1 mg a.i./kg
value and the soil uptake model (the Briggs model) proposed in the white paper as Tier I
screens, including consideration of the extent to which this method may generate conservative
Tier I estimates of dietary exposures to bees. Does the Panel conclude that the one approach
may be better suited to specific types of assessment scenarios? If so, please elaborate.
Alternatively, if both approaches are equally suited for a Tier I screen, please provide
guidance on how to be capture variability and uncertainty in the exposure estimates using the
two approaches.
Panel Summary
The Panel concludes that although the Briggs approach has multiple uncertainties and
weaknesses, it is a more rational and defendable approach to estimate Tier I pesticide dietary
exposures to bees than the European and Mediterranean Plant Protection Organization (EPPO)
default value (1 mg a.i./kg). This value does not appear to take into account pesticide properties
as does the Briggs method. Consequently, the Panel believes that the Briggs approach is
stronger mechanistically, and is a superior method for estimating pollen and nectar pesticide
concentrations.
d. Seed Treatments: Please comment on the analysis presented in Section 3.1.3, including a
discussion of the strengths and limitations of the use of 1 mg a.i./kg value as an upper-bound
concentration for pollen and nectar of seed-treated crops.
Panel Summary
There are a few strengths, but many more weaknesses associated with use of the 1 mg a.i./kg
value as an upper-bound concentration for pollen and nectar of seed-treated crops. The Panel
concludes that the value is likely conservative, but believes that a comprehensive assessment of
measured data is needed before this approach can be confidently used. The Panel recommends
that a concerted effort be made to compile all available data to assess potential ranges in
observed pesticide concentrations in pollen and nectar with different plants and pesticides.
e. Please comment on other approaches or data that should be considered for estimating
upper-bound estimates of pesticide residues in pollen and nectar as a Tier I screening-level
assessment for pesticides applied via foliar spray, soil application or seed treatment.
20
Panel Summary
As indicated in the Agencys white paper, there are other methods for estimating Tier I upperbound pesticide residue estimates in pollen and nectar resulting from foliar spray, soil
application, and seed treatments. They are for example:
Direct measurement of the pesticide in question on the plant parts of interest (nectar,
pollen, etc.).
Direct measurement of the pesticide in question in other plant tissues (stems, leaves, etc.).
Direct measurement of surrogate pesticides in plant tissues.
As noted previously, (see response to Question 6. d.) the Panel strongly advises a data call-in to
assist in evaluation of these approaches and determining appropriate upper-bound values for use
in Tier I assessments.
7. Consideration of other Exposure Pathways. The proposed measures of exposure are based
on what are believed to be the primary routes, i.e., direct contact and ingestion of
contaminated pollen and nectar. Additional routes of exposure are considered (e.g., dust,
drinking water), but not included in the proposed Tier I exposure assessment method. As
discussed in Section 3.1.4.1 of the white paper, effective quantitative screening methods for
estimating exposures through contaminated dust are not discernible at this time. The most
effective management of bees exposure to pesticides through dust appears to be through
pesticide application (e.g., stickers) and seed planting practices, especially since dust exposure
is expected to be a concern for only a limited number of pesticides and application scenarios.
In regard to pesticide exposures through drinking water, Appendix 2 presents an analysis of
potential exposures to bees through various sources of water to support the exclusion of
drinking water exposure in the Tier I screen. The results of this analysis indicate that if bees
consume the majority of their water from puddles or ponds, the exposures relative to dietary
and direct spray are insignificant. The preliminary analysis indicates that if bees drink a
substantial amount of water from guttation fluid or dew, conservative exposures may be
similar to or even exceed pesticide exposures through the diet or direct spray. Further
investigation concluded that pesticide exposures through dew and guttation fluid are not
expected to be as significant when compared to diet, primarily because they are not likely to
consistently drink a substantial amount of water from these sources.
a. Please comment on the strengths and limitations of basing the Tier I exposure method on
contact and diet. Does the Panel agree that for the majority of pesticide applications, the
primary exposure routes for bees will be represented by contact and diet?
Panel Summary
In general the Panel concurs that diet and direct contact are the primary pesticide exposure
pathways. However, the Panel considers exposure from seed treatments to also be a potential
exposure pathway particularly since bee mortalities during planting of seeds treated with certain
insecticides are widely reported. Exposure in this case is expected to occur via direct contact and
21
oral uptake with dust generated during the planting of pesticide treated seed, granular
formulation application. The Panel also believes that pesticide exposure via contact and
consumption of pesticide contaminated water should be included in Tier I assessments.
b. Dust: If the Panel believes that this exposure route should be quantitatively included in the
Tier I exposure method, for the relevant application type(s) (i.e., seed treatment), please
discuss the data that may be needed to address the exposure route quantitatively.
Panel Summary
The Panel concurs with the white paper findings that bees may be exposed via contact to
pesticides in dust while in flight or when visiting flowers and other vegetated surfaces where
dusts have deposited. The Panel also recognizes that there have been widespread reports of
honey bee mortality associated with dust emissions during planting of pesticide treated seed.
Thus, the Panel notes that in many cases deaths due to pesticide exposure were confirmed by
detection of pesticide concentrations above lethal limits in bees.
The Panel acknowledges that no matter what the dust source, an exposure assessment is
challenging since there are many variables involved and little published data. Recently
published work may provide some insight with regard to pesticide emissions associated with
abraded seed coatings. For example, Tapparo et al. (2012) reported on the percentage of applied
pesticide that may be emitted in planter exhaust from corn seed coated with various commercial
insecticide treatments. Such data are needed to evaluate exposure estimates. One panel member
notes that consideration of dust exposure and effects as well as potential mitigation measures
should be addressed by higher tier testing and/ or risk management measures.
c. Drinking Water: Please comment on the analyses, discussions provided in Appendix 2 of the
white paper and the conclusion that pesticide exposure to bees through drinking contaminated
water is not expected to be a major route of exposure when compared to contact (following
foliar spray applications) and diet. If the Panel believes that this exposure route should be
quantitatively included in the Tier I exposure method, for the relevant application type(s) (i.e.,
foliar spray, soil treatment, seed treatment, or trunk spray), please discuss why and what data
may be needed to address the exposure route quantitatively.
Panel Summary
Honey and other bees may be exposed to pesticides in water contaminated with pesticides via
direct water consumption and/or during contact when worker bees carry water in their honey
stomachs to the hive for use in hive evaporative cooling. The Panel notes that water exposure
assessments in the white paper are limited to estimates of drinking water consumption. The
Panel concurs that potential exposures should also include other types of water contact.
However, the Panel believes that even when both consumptive and non-consumptive water
contact are assessed, it is assumed that worker bees absorb 100 % of the pesticide transported in
water in honey sacks. Potential exposures to water from contaminated ponds appear small when
compared to dietary or contact exposures described for Tier I. In regard to the potential use of
puddles in farm fields as bee water sources, the white paper also indicates potential exposures
22
were likely very small when compared to diet and direct contact exposure in Tier I estimates.
Regarding this point, the Panel disagrees and notes that values with incorrect units were used in
Equation 2-1 found at the top of page 210 in Appendix 2 of the white paper. The Panel believes
that the equation is written correctly, but careful attention must be paid to input parameter units.
Failure to do so in the computations described in the white paper resulted in 1000-fold
underestimates of pesticide concentrations in puddle scenarios. Use of appropriate input values
indicates that pesticide exposure via consumption or contact with water in puddles on or adjacent
to pesticide treated fields may be relatively high. These estimates appear to be within the same
range as reported for both dietary and contact exposure. The Panel also proposes an alternate
approach for estimating pesticide concentrations in field puddles that was develop for the
Agencys ECOFRAM (Ecological Risk Assessment Framework; US EPA, 2012). Use of this
model may provide further insight into potential pesticide exposures via this pathway.
Concerning guttation water, the Panel believes that guttation water may not be an important
water source for bees since the drops are usually found in the morning only. However, the Panel
notes that there is uncertainty regarding the extent to which honey bees may be exposed to
guttation water and cautions that published studies show that residue levels in guttation water
may be high.
d. Other Routes: Please identify and discuss additional exposure routes (if there are any besides
contact with dust and consumption of drinking water) that would contribute significantly to
pesticide exposure of bees and explain how and why such exposures could be considered
quantitatively in establishing the Tier I exposure value.
Panel Summary
The Panel believes that a potentially significant route of exposure for some non-Apis species is
direct contact with pesticide contaminated soil. Many solitary bee species nest in the ground.
Also some cavity nesting bees use mud to wall off and divide the cells in their nest. Since the
Agency currently does not have models for estimating these types of pesticide exposures the
Panel recommends that research be conducted to directly address these exposures.
23
8. Tier I Effects Assessments. As discussed in the Problem Formulation (Section 2.2.1), the
assessment endpoints for the ecological risk assessment of bees involve maintaining honey
bee population size, stability of managed bees, quality and quantity of hive products, species
richness and abundance. In order to use the results of toxicity studies quantitatively in risk
assessment, it is important to identify specific endpoints which will be measured in toxicity
tests as these measurement endpoints must have clear linkages to assessment endpoints. As
indicated in Table 1 of Section 2.2.1, at the individual bee level (which is the focus of the
Tier I assessment), measurement endpoints relevant to these assessment endpoints include:
individual survival, adult bee longevity, brood size, brood success, and queen fecundity. The
acute and chronic toxicity tests with larvae and adults can be used to quantify effects of
pesticides on all of these endpoints, with the exception of queen fecundity (which would
require an egg laying study involving the queen). The focus of the chronic toxicity tests with
larvae and adults is on mortality that may occur during the tests. Potential impacts of a
pesticide on brood size and success can be assessed by determining whether there is decrease
in the number of brood (i.e., larvae) following a chronic exposure of larvae to that pesticide.
Potential impacts of a pesticide on adult survival and longevity can be assessed by
determining the mortality and the decrease in the life spans of adult bees following chronic
exposures to the pesticide. The notable limitation to the proposed chronic toxicity endpoints is
that they do not include measures of queen fecundity.
a. Please comment on the extent to which currently available bee toxicity tests, which focus
primarily on mortality/survival, serve as an effective Tier 1 screen.
Panel Summary
The Panel notes that the Agency provided a clearly articulated, detailed, and thorough
description of its Tier I bioassays in the white paper. In regard to suggested enhancements to the
Tier I assays, the Panel provides the following considerations. Firstly, the Panel believes that
these bioassays do not account for the subtle variation among individual bees. Thus, the Panel
suggests that standardizing to honey bee weight seems to be a useful approach that would
translate more effectively to other bee castes and especially other bee species. Secondly, the
Panel notes that the current Tier I screens (which measure the percent mortality after 48 to 96
hrs) do not evaluate the temporal variation on final mortality. Thus, the Panel recommends that
standard survival analyses would provide more information, as it would account for not only the
percent mortality at each time point measured, but it would also statistically compare the slopes
of the mortality curves. This information could be more readily applied in the social context of a
bee colony. Thirdly, the Panel suggests that the Agency consider employing two types of Tier I
honey bee cage studies. Each would be informative in different ways. These two include a onetime application study and a continuous exposure by feeding study. The Panel also advises the
Agency to consider the physiological differences between summer and winter honey bees, and
short-duration colony events (e.g. increased honey-store consumption during smoke application),
and how the timing of pesticide applications could result in different outcomes due to these
differences. Lastly, the Panel recommends that the Agency recognizes the genetic differences
among populations as well as the need to consider the behavioral (sub-lethal) abnormalities that
may occur from pesticide exposures. Since no trigger values are established for sub-lethal
24
effects, the risk assessor should have the flexibility to ask for additional data or higher tier tests
when concern is raised on the basis of sub-lethal effects observed in laboratory studies.
b. Please comment on additional measurement endpoints (e.g., growth) which should be
considered in future modifications of Tier I test protocols and which are appropriately linked
to the proposed assessment endpoints. Given that the queen is the reproductive unit of the
colony, please comment on methods to evaluate effects on individual queens, considering
practical limitations of testing with queens.
Panel Summary
Currently there are no methods available for assessing effects on individual queens. However,
the Panel notes that quantifying reproductive potential in queens can be done in many different
ways including evaluating ovariole number, morphometrics, and pheromone production (c.f.,
Delaney et al. 2011).
In regard to additional measurement endpoints to be considered for Tier I protocols, the Panel
suggests the following:
A temporal component to Tier I bioassays, using survival statistics to quantify slopes as well
as final percent mortality (see Question 8a).
Quantification of immuno-competence on adults (and larvae) to assess the possible long-term
sub-lethal consequences of exposure (however, bearing in mind the caveat that little is known
about the linkages of the immune system to colony health at this point to make such
inferences very strong).
Measurement of motility, social interactions, and other behavioral changes (in addition to the
survival measurement currently assessed by the Agency).Addition of a Proboscis Extension
Reflex (PER) and learning bioassay. PER is a well vetted and commonly performed
bioassay for learning and memory, which uses the instinctive reflex of a harnessed adult
worker honey bee sticking out her proboscis when her antenna contacts a droplet of sucrose
solution. However, one panel member disagrees that PER tests are currently very useful in
risk assessments as they assert that there is a lack of available data which link these tests to
the realistic situations that bee colonies encounter.
Investigation into the development of a study that would test the impact of pesticides on
pheromone production.
Evaluation of viability of sperm within queens.
Analysis of queens fecal materials (a test that can provide some useful information and
which can be done without sacrificing the queens).
25
9. Tier I Larval Toxicity Testing. Section 4.1 of the white paper discusses new data
requirements for the screening-level effects assessment and recommends obtaining and using
larval toxicity data on individual bees. The paper specifically identifies the assay initially
proposed by Aupinel et al. (2007) as one methodology for quantifying acute oral larval
toxicity in the Tier I screen. These assays rely on feeding bees a sugar solution which has
been spiked with the test material; however, this in vitro method of feeding larvae differs
from the process by which the larvae would typically be fed within the colony environment,
i.e. by nurse bees secreting either brood food or royal jelly.
a. Please comment on the extent to which the Aupinel et al. (2007) in-vitro method serves as an
appropriately conservative estimate of Tier 1 acute oral exposure of honey bee larvae to
pesticides, given differences in this test design from actual in-hive exposure conditions (e.g.,
during the first 3 days of the larval development stage larvae consume royal jelly and brood
food) and the uncertainty regarding the extent to which larvae rely exclusively on
pollen/nectar as opposed to royal jelly/brood food.
Panel Summary
As mentioned in the Agency white paper, larval toxicity in vitro testing is complicated by
factors such as genetic differences among colonies and difficulties synchronizing larval age. An
additional complicating factor is the uncertainty regarding how larval food (i.e., royal jelly/brood
food, honey and beebread) may alter the responses of pesticides.
An additional concern is that an acute dose for a larva may be biologically difficult to interpret.
This is because larvae receive food on a continual/chronic basis. Thus, the Panel suggests that
with in vitro larval tests it is preferred that larvae are given contaminated food every day on a
chronic basis as opposed to being fed on an acute basis in which the larvae are only given
contaminated food once on Day 4, and on the other days uncontaminated food.
b. Please comment on the extent to which pesticides would be more or less bioavailable using
the synthetic matrix relied on for feeding developing bees in this in vitro method.
Panel Summary
Bioavailability is directly impacted by the characteristics of the pesticide, larval metabolism, and
food composition. Currently, there is an inadequate amount of data for the Panel to assess this
question. For example, the Aupine et al. (2005) acute larval toxicity test used an
organophosphate, dimethoate (which has relatively high water solubility). It is not clear how
other types of pesticides will behave in the synthetic matrix.
c. Please comment on the extent to which the absence of trophallaxis (i.e., the transfer of
food/fluids between colony members) may render larvae more or less vulnerable to pesticides.
26
Panel Summary
The Panel deems the impact of trophallaxis on pesticide resistance or susceptibility as
completely unknown. To the Panels knowledge, the understanding of this impact represents an
absolute data gap.
d. Please comment on alternative methods for testing individual larvae that may be appropriate
for quantitative use in a Tier I screening-level assessment.
Panel Summary
Published studies on alternative methods for quantitatively testing larvae are rare. Even rarer are
literature reports of alternative methods for testing larvae quantitatively. One approach
described by Atkins and Kallum (1986) involved treating larvae in a colony by micropipetting
pesticides directly into the cells.
There has not been a common use of pupal bioassays for pesticide toxicity testing. However
these bioassays have been commonly used in other milieux (e.g. pathogenicity of fungi.) Such
studies may be reproducible and provide some informative means of developing pupal bioassays
testing pesticides.
There are available data which describe the larval transcriptomes and methylomes of honey bees
(Johnson et al. 2009). These data could provide a useful means of developing quantitative
measures of effects of toxins on larval development that might be useful as alternative indicators
of larval actions/health.
e. Typically acute toxicity tests are concluded between 48 96 hrs. Please comment on the
appropriate duration of toxicity tests for assessing acute toxicity to individual larval and adult
bees.
Panel Summary
A two to four day time period toxicity test presents some problems for adequately interpreting
larval survival. This is because the four-day endpoint represents only 80% of the period of
active feeding. Thus, it would be difficult to distinguish between acute and chronic effects. The
Panel suggests for the present time that the Agency conclude acute toxicity tests after a duration
of seven days. This will enable the Agency to harmonize international efforts at the OECD level.
However, the Panel advises that in the meantime development of a satisfactory standard pupation
assay should be a priority. The Panel also suggests that a repeated dose testing method would be
most realistic for assessing potential acute effects (i.e., effects at the larval stage) and chronic
effects (i.e., effects at the latter brood stages) of pesticides.
27
10. Tier I Chronic Toxicity Testing Bees. Section 4.1.2 of the white paper discusses the status
of chronic toxicity tests with individual adult and larval bees. At this time, no formal
guidelines have been developed for conducting chronic toxicity tests with either adult or
larval bees, although studies with individual bees of various ages are routinely reported in
open literature.
a. Please comment on the conclusion that adequate procedures have not been sufficiently
developed and validated for assessing chronic toxicity to individual bees in a risk assessment
context.
Panel Summary
The Panel believes that social characteristics of honey bees present a challenge to interpreting
individual bee toxicity testing to the colony level. Thus, the Panel advises the Agency to
consider the OECD (The Organization for Economic Co-operation and Development) 213 study
guideline (OECD, 1998). It provides a study design that may help in addressing this challenge.
b. Please comment on the potential use of the 10-d adult worker and 7-day in vitro larval
toxicity tests discussed in the white paper for assessing chronic toxicity once these methods
are fully vetted.
Panel Summary
The ideal study design for a larval in vitro study would encompass the entire active feeding
period through pupation, with time to pupation, pupal weight and percent pupation as
quantifiable and interpretable measures of pesticide impact. In regard to adult toxicity testing,
the 10-day viability for adult bees has the inherent advantage of supporting harmonization
efforts.
c. Although 10-day adult and 7-day larval toxicity tests have been proposed, please comment on
whether alternative durations of pesticide exposure may be more appropriate for determining
chronic toxicity for adult and larval bees at a Tier I screen.
Panel Summary
The Panel recommends that the Agency consider the use of caged brood or broodless bee cups (it
is important to note that this is not a standard methodology) to assess the social context of honey
bees. In regard to larval toxicity tests, the Panel suggests extending the test duration through the
pupation stage.
28
d. The white paper identifies NOAEC No observable effect effective concentration as the chronic
toxicity measurement endpoint. Please comment on the possible use of ECx values as a
measure of chronic toxicity for use in RQ calculations.
Panel Summary
The Panel recommends that whenever possible both NOAEC and ECx values be used. There are
uncertainties and challenges in tying the outcomes of both methods with the protection goals.
However, both methods have utility for triggering higher tier tests.
e. Please provide comments on what percent effect would be considered a relevant measure of
chronic toxicity for individual bees given the potential compensatory effects which honey bee
colonies may exhibit relative to the effects of pesticides.
Panel Summary
The Panel believes that compensatory effects as a bee colony/societal phenomenon are most
appropriately addressed at the Tier II assessment level. In regard to a specific percent effect, the
EC20 (20% difference between controls and experiment to trigger concern) may be a
conservative endpoint considering that, one model available demonstrated that (Khoury et al.
2011) a loss of 30% or more foragers daily triggers the death spiral.
f. Although the white paper identifies some measurement endpoints for assessing chronic
toxicity to individual bees (e.g., survival), please comment on other endpoints to consider in
chronic toxicity studies which the Panel believes are important and the associated study
design elements.
Panel Summary
Other chronic toxicity endpoints recommended by the Panel include behavioral impacts such as
learning assays, automated recording of motility and behavioral interactions. Endpoints for
future consideration include gene expression relevant to detoxification and/or antioxidant status,
immunocompetence, and senescence. One research study suggested the use of ribosomal RNA
fragments as a biomarker (Johnson et al. 2009). Nevertheless, such studies should be validated
and it should be clear how the results of these studies can be used in risk assessment.
29
g. Section 4.1.3 4.1.2.1.2. of the white paper discusses the uncertainties associated with
developing risk assessments based on studies of sublethal effects when sufficient linkages have
not been developed to understand how the sublethal endpoints may be quantitatively related
to typical assessment endpoints (i.e., growth, impaired survival, and reproduction) at the
whole colony level. Please comment on the proposal to use data on sublethal endpoints to
qualitatively (i.e., no Risk Quotient is derived) characterize effects and risk until sufficient
linkages between these endpoints and the defined assessment endpoints have been developed
(e.g., Adverse Outcome Pathways).
Panel Summary
The social nature of some bees contributes to colony function as a super-organism and adds
complexity to the assessment of sublethal endpoints. Nevertheless, it is still important to identify
and assess sublethal effects in order to gain insight into potential impacts to the super-organism.
The Panel advises the Agency to advance this effort by placing a high priority on generating
research data on bee neurotoxicological symptoms. This may provide knowledge regarding the
potential for impacts on bee behavior and other sublethal effects. The outcomes of these studies
can trigger the need for additional tests at the Tier II level.
11. Tier II Semi-field Effects Assessments (Whole Colony). For Tier II assessments, Section
4.2 of the white paper identifies two types of test methods that may be used to assess colonylevel effects, i.e., semi-field tunnel tests [OECD 75; EPPO 170]; and semi-field feeding
studies (OECD, 2007; EPPO, 2001). These studies are intended to help characterize risks
identified in the Tier I level assessment that are based on exposures and toxicity data for
individual bees and quantified using Risk Quotients.
a. Although colonies are typically confined to enclosures for Tier II studies and these enclosures
can limit the environmental realism of the study conditions, tunnel studies provide an
opportunity to collect colony-level effects and potentially exposure information. Please
comment on the relative strengths (e.g., foraging activity by adult worker bees is limited to
treated crop; trophyllaxis enabled) and limitations (e.g., limited study duration, smaller
colony sizes, reduced forage area) of these methods.
Panel Summary
The Panel believes that these proposed Tier II tunnel studies are very important for providing
information at the colony level that LD50 measurements made for Tier I assessments are unable
to adequately accomplish. An inherent strength of proposed Tier II studies is that they provide
the basal level in which to properly quantify LD50 estimates. An example of a limitation of Tier
II tunnel studies is that it is difficult to acquire a sufficient sample size due to the inherent
variability between colonies. Thus, there are increased risks of Type II errors (false negatives)
with these high-tiered tests. In regard to feeding designs for these studies, the Panel recommends
that feeding with spiked food should only be used to extend exposure when it is necessary and
when it is not possible to do a design with extended flowering of the realistic crop (e.g., if there
is concern for chronic long-term exposure).
30
b. Please comment on any other types of colony-level studies that should be considered as part
of Tier II.
Panel Summary
The Panel suggests that the Agency consider observation hives to record behavior and estimate
interactions as an alternative study design. This will be useful in addressing sublethal effect
questions. The Panel also recommends that the Agency explore potential in vitro, whole minicolony tests that could be implemented in the short term that blur the lines between Tiers I and
II. For example, Tier I tests of bee cups each containing a queen could be confirmed with Tier
II tests of baby nuc colonies housed in incubators. While still in vitro, such colonies would
contain queens, brood, comb, and other full-colony phenotypes that could be measured. For all
tests that entail artificial feeding, the Oomen Test can be used as an intermediate test between
Tier I and Tier II (Oomen et al., 1992). Some special study designs can be employed to
investigate special effects or exposure routes. Examples may include studies to evaluate the
effect of a pesticide on queen rearing, (e.g., a shook swarm) or swarm box method of queen
rearing, exposure via the crop and observation of the number of reared queens and rearing
success of hatched queens. Such studies would be important since there are some published
reports suggesting that queens may be sensitive to some pesticides. The Panel recommends that
an alternative study design be developed to investigate such specialized impacts and potential
pesticide exposure routes that may cause them.
c.
Please comment on the most important endpoints that should be measured in the Tier II
studies (e.g., adult forage bee mortality, brood development, queen fecundity, overall
colony strength) that are linked to assessment endpoints and their associated protection
goals.
Panel Summary
The Panel suggests the following as the most important measures that should be conducted to
link assessment endpoints and their associated protection goals:
Measurement of effects on different colony phenotypes.

Assessment of the association between foraging activity and colony phenotype.
Implementation of tunnel studies whose design is based on the expected exposure routes.
Assessment of the behavior of foragers both at the hive entrance and during foraging on a
crop.
Employment of the OECD 75 method using maps or digital imaging of the brood to assess
the impact on queen fecundity by evaluating the amount of brood in the hives at certain
intervals, and the effects on larval development and brood rearing success (OECD, 2007).
31
d. Section 4.2.2 of the white paper discusses a full-field feeding design. This methodology is
discussed under Tier II assessments since the colony is relatively confined to foraging on either
spiked sucrose solutions or spikes pollen. The intent of this methodology is to ensure that
colonies are exposed to known residue levels over longer durations than the semi-field tunnel
study designs. A limitation to the study is that bees may simply store spiked food rather than
consume it and that the reliance on a single source of food may introduce confounding effects
(e.g., nutritional deficits) into the study. Please comment on the environmental realism and
utility of full-field feeding studies as a line of evidence in characterizing risk to honey bee
colonies.
Panel Summary
The Panel believes that full-field feeding studies are not appropriate for risk assessment
purposes. At best, they can be used as supplemental information of limited value as they are not
environmentally realistic. The Panel advises that OECD 75 and EPPO 170 guideline studies are
used for Tier II and Tier III studies, since these studies may be the most appropriate test designs
for capturing contact and oral exposure pathways (OECD, 2007; EPPO, 2001).
e. As discussed in Section 4.3.4 of the white paper, it is important to consider the biological
significance of a measured effect in addition to its statistical significance. Please comment on
the nature and magnitude of effects that would be sufficient to conclude biologically significant
effects on the colony and/or the need to transition to Tier III assessments.
Panel Summary
The Panel provides the following list of prioritized potential measurement outcomes (Table A) as
a means of orienting risk assessors towards more-informative measurements that have greater
penetration (i.e., they likely measure a stronger biological signal in the system):
Table A. Prioritized potential measurement outcomes
Relative utility for
Ecological
Colony measures
Individual measures
measuring risk
measures
Mortality in the
Colony strength
Pesticide residues
crop
Mortality at the
Weight of the hive
Longevity
hive
Mortality of
Food stores
Behavioral
drones and
abnormalities
pupae
Foraging activity Presence of the same
in the crop
queen
Higher
Returning
Ability to requeen
utility
foragers
Levels of disease
Lower utility
Over-wintering success
32
12. Tier III Effects Assessments. Section 4.3 of the white paper discusses the proposed risk
assessment process in Tier III that relies on assessing effects at the colony level where
colonies are not confined (i.e., full field) and exposure is intended to represent
environmentally realistic conditions. As discussed in the white paper, interpretation of the
biological significance of colony-level effects can be challenging, regardless of their
statistical significance. Conversely, high variability in field studies can limit the statistical
power of the study to detect treatment effects. The paper identifies uncertainties associated
with the extent to which bees forage on the treated crop, the size of treatment site, controlling
for alternative forage/pesticide use area, and ensuring suitable controls; these factors combine
to render these studies highly resource intensive.
a. Please comment on the strengths and limitations of full field studies described in the white
paper.
Panel Summary
Tier III studies are intended to be the best test of real world exposures and possible effects.
Nevertheless, these studies have many weaknesses since their reliability depends on performing
a controlled experiment in an open environment with adequate controls. The European Union
has extensive experience in conducting these experiments. When they are correctly conducted
they may provide the best way of assessing possible pesticide risk to Apis mellifera colonies and
other managed pollinators (e.g., Bombus or Osmia).
Examples of Tier III study strengths:
Natural exposure can be achieved by allowing bees to forage freely on a treated crop.
Measurement of endpoints that test for effects at the colony level can be made that are
unattainable at Tier I and II level testing.
Exposure can accurately simulate the actual use of the pesticide.
Examples of Tier III weaknesses
Variability among colonies may be high thus there is a need for replication and large sample
size.
Study site selection is critical since the presence of untreated crops and vegetation that serve
as alternate food sources for bees can result in low to no exposure to the target crop,
especially if the plot size is limited or the crop is marginally attractive.
Plot size will vary with less attractive crops needing larger plots to insure adequate foraging
and exposure to the target crop.
33
b. Please comment on the proposed modifications to the field study design elements presented in
Section 4.3.2 of the white paper.
Panel Summary
A concern about Tier III study design that the Panel notes is the lack of control regarding bee
foraging which consequently causes uncertainty about pesticide exposure. The Panel
recommends lessoning this concern, by performing an estimated calculation of foraging activity
(given the Agency identified foraging range of 78.5 mi2 area) and also by analyzing a relatively
small number of samples of foraging bees over the duration of the study in order help quantify
the pesticide exposure. The Panel also recommends using Bombus sp. or Osmia sp. as test
species since they fly shorter distances, and consequently, their level of exposure can be greater
and/or more controlled.
c. Please comment on factors that should be considered in evaluating the biological significance
of effects measured in full-field studies in relation to the proposed assessment endpoints and
related protection goals.
Panel Summary
The collective set of the weight of evidence built in the different tiers including information on
acute mortality of adults and larvae as well as colony development and behavior should be taken
into account. In particular it is important to note that effects on queen survival or replacement
are of biological significance and have implications for colony survival that may not be
accounted for if test duration is only a few weeks or months. Ultimately it should be recognized
that colonies are complex super-organisms and that several endpoint measures may be more
appropriate than relying any single endpoint.
d. Please comment on factors and methods that should be considered when extrapolating
observed effects at the colony level in semi-field and field studies to those expected to occur in
the environment (e.g., spatial and temporal scale of exposure, hive management practices,
presence of multiple chemical and non-chemical stressors, etc).
Panel Summary
Tier II and III studies are unable to incorporate all seasonal and colony management practices
that may impact the response of colonies to pesticide exposure. However, an adequate level of
confidence in a study can be achieved if the study is performed in the normal growing season in
which the test pesticide is expected to be used. Examples of factors to consider in conducting
Tier III studies include the length of the study (as the longer the study duration the more likely
outside variables such as pests and disease will interfere with the results). Also if a crop is major
and widely planted, the study may not reflect the level of exposure bees may receive once the
pesticide is used widely across a region. The acreage treated may be proportionally greater than
in the study (e.g., corn or soybeans in the Midwest).
34
e. A number of study design elements are discussed in Section 4.3.5 of the white paper;
however, even in the best designed studies, there can be confounding effects which can limit
the utility of these studies in risk assessment. Please comment on factors that should be
considered in determining the utility of field studies for pesticide risk assessment, including a
discussion of the representativeness of a study for a National Level assessment (i.e., the
pesticide may be used anywhere in the United States and its territories).
Panel Summary
The single measure that gives the highest level of confidence in the studys validity is the
measurement of exposure linked to incoming pollen during the exposure period. Additional
considerations include: 1) field testing which involves use of formulated products, 2)
representativeness of various crop environments in which a compound may be used, 3) size of
the test plots (the larger the test plot the better; one Panel member recommends a field plot size
of 40 acres.), and the number of bees in a test trial (the Panel recommends that a good rule of
thumb for the maximum number of bees in a field trial is 30,000 adult females per acre).
13. Risk Estimation. Sections 2 (Proposed Risk Assessment Process) and 5 (Risk
Characterization) of the white paper indicate that the proposed risk assessment process is
intended to be tiered and iterative. As part of the Tier I screen, a number of iterations can be
conducted on exposure estimates that allow the risk quotient (RQ) values to be further
refined and potentially pass the screen without requiring higher tier effects testing at the
semi- or full-field level. However, while the proposed Tier I process for bees is quantitative
and results in an RQ value which can in turn be compared to a Level of Concern (LOC),
higher tier refinements are used to qualitatively (i.e., no RQ derivation) determine whether
whole hives will be adversely affected from the use of a pesticide based on the initial
screening-level assessment.
a. Please comment on the use of data on individual bees to transition to higher tier studies given
that the Tier I studies focus on survival as the primary measurement endpoint although
additional endpoints may be forthcoming as test designs continue to develop.
Panel Summary
Higher tier studies are vital to determine pesticide risks under the conditions that bee colonies
experience in the field. Measurements of individual endpoints (e.g. LD50), in Tier 1 may not
translate effectively into what will happen at the super-organism/colony level. Mathematical
modeling (after calibration and validation) can be helpful towards this translation. It would also
be helpful to assess pesticide mode-of-action in order to qualitatively assess exposure risks both
individually and cumulatively. Although results of a Tier I study may not characterize the
overall impact on the super-organism, these studies are critical. When they are appropriately
conservative, Tier I tests trigger higher tier studies that have the potential to detect adult or larval
toxicity and behavioral abnormalities via multiple exposure routes.
b. Please comment on the derivation of the Level of Concern (i.e., LOC=0.4) and the extent to
which it serves as an appropriate screen to transition to higher tiers of testing/refinement.
35
Panel Summary
EPA proposes to set this LOC value at 0.4 which is equivalent to approximately 10% mortality.
Considering the uncertainty associated with extrapolating effects on individual bees to effects on
the colony, it is hard to consider an appropriate level of concern for adult bee mortality at the
Tier I level. Other endpoints such as behavior, development, and growth rate may be more
appropriate and reflective of colony health. Currently, the science does not support the premise
that 10% mortality of adult bees would result in colony collapse or even instability. Thus, the
Panel believes that the 0.4 LOC value may be too conservative. To estimate a more realistic
mortality, the Panel suggests that the Agency consider exploring the use of a sensitivity analysis
of mortality in currently existing population biology models such as described by Fefferman and
Starks (2006).
c. Please comment of the quantitative aspect of the screening-level (Tier I) assessment and the
use of Tier II and Tier III whole hive studies to qualitatively characterize risk.
Panel Summary
Generally, the Panel agrees that higher tier studies are best suited to assess real world scenarios.
The conservative approach of Tier I tests is to ensure that higher tiers are triggered when
appropriate. The Tier II tests represent a worst case scenario, and are sensitive to finding effects
(since they involve bee confinement scenarios). Tier III studies embody more realistic situations
in that they take into account all multiple stressors and multiple issues that cannot be addressed
by Tier II studies (e.g., homing behavior).
d. Please comment on the assumption that the effects on individual bees measured in laboratory
studies must be considered in the context of whole colony studies conducted under semi-field
and full-field conditions.
Panel Summary
The Panel believes that individual phenotype is not an appropriate substitute for colony
phenotype. Nevertheless knowing the impact to the individual bee is critical since colonies are
made of individuals. Considering the type of effects and the nature of the pesticide, higher tiered
studies may need modifications to address the chemical under evaluation.
e. Please comment on the proposed use of a weight-of-evidence approach based on information
obtained from multiple tiers of risk assessment for characterizing pesticide risks to honey
bees.
36
Panel Summary
Identifying a line of evidence with strong linkages among its pieces is fundamental to the weight
of evidence approach. The pieces of evidence the Panel recommends utilizing are: 1) reliable
and repeatable high throughput methods, 2) properly investigated incident reports, and 3)
qualitative evidence (which is more important in social systems than simple mortality derived
from solitary systems).
f. Please comment on how best to characterize overall uncertainty or weigh different areas of
uncertainty in risk characterization.
Panel Summary
Tier II and Tier III studies are prone to Type I (appearing to have significant effects, when in
reality there are none) and Type II (appearing to have no significant effects when these effects do
exist) statistical errors respectively. To minimize uncertainties, the Panel advises that results of
these tests be validated against the preponderance of evidence discovered at the lower tiers.
g. Please comment on how to focus/prioritize uncertainties when designing and interpreting Tier
II and Tier III studies.
Panel Summary
The Panel recommends focusing on the following areas when designing and interpreting Tier II
and Tier III studies: 1) increasing the sample size, 2) including replication, 3) factoring in genetic
variability, and 4) concentrating on the Tier II level. The Panel also advises the Agency to
consider utilizing Bayesian methods in interpreting data as these methods are intended to
determine "what is the significance of what we were able to observe" rather than applying a
"significant or not" test that relies on traditional views of statistical power that may be unrealistic
for studies of expensive or difficult scenarios.
14. Colony-level Modeling. As part of the proposed risk assessment process, Section 5.4 of the
white paper discusses the concept of using colony-level models as a means of integrating
exposure and effects information generated from the multiple risk assessment tiers and in
turn linking this information quantitatively to the proposed assessment endpoints.
Conceptually, such models could inform the need for transitioning from lower tiers to higher
tiers in the risk assessment process. They could also be considered in identifying critical
design elements of higher tier studies (e.g., semi-filed or full field studies).
a. Please comment on the concept of using colony-level ecological models to inform the
proposed risk assessment process for honey bees, as indicated above.
Panel Summary
37
Generally the Panel believes in theory that utilization of colony-level models should enhance the
capacity of performing valid risk assessments for honey bees. The Panel cautions that there are
many potential drawbacks to models. Most notably it would be a mistake to operate under the
presumption that a model that incorporates all aspects of colony life should be used to inform
ecological risk assessments. Such models would inherently have a large amount of uncertainty.
Instead, models that concentrate on smaller more localized questions should be utilized to
support risk assessment.
The Panel recommends that the Agency consider analytical models in addition to the
simulation models being considered. An analytical model is a model that focuses on the causal
relationships among variables and parameters. Equations are used to capture these relationships,
and provide insight into system-level processes (e.g., threshold behaviors for phase transitions).
The Panel advises that it is important to validate models that are used via a statistical analysis of
the correlation between model outcomes and measurements made in real-world scenarios. The
Panel cautions against using modeling outputs to fill data gaps.
b. Please comment on the state of the science regarding available honey bee models discussed in
Section 5.4.2 of the white paper in relation to their potential application in a regulatory risk
assessment context. In particular, please comment on the extent that such models have been
evaluated using empirical data related to honey bee population dynamics and the availability
of such data for their parameterization.
Panel Summary
The Panel notes the limited availability of input data for many of the models discussed in the
white paper. It is important to emphasize that more input (i.e. measurements of parameter values
and valid characterizations of functional relationships) and validation data (i.e., measurements
for comparison with predicted model outcomes) are needed to support models. Consideration
must also be given to what is considered an appropriate level of agreement between measured
and predicted values during both model calibration and validation. While the Panel agrees that it
will be important to collect further input data (i.e. measurements of parameter values and valid
characterizations of functional relationships), and to collect validation data (i.e., measurements
from the real world for comparison with predicted model outcomes), the Panel notes that analytic
models can be useful in the absence of such data. The Panel cautions that even when the proper
input data and validation data are available there is a danger in assuming that a model
consistently and accurately predicts one outcome of a system without a peer review step for the
analytic representation of relationships among model components. The Panel believes that few,
if any, of the models described in the white paper have been compared to other models or tested
for robustness of model choices apart from their specific focal questions. The Panel also advises
that a model under consideration undergo appropriate sensitivity and robustness testing for
individual parameters, variables, and functional relationships. One panel member stresses that
although models may have the potential to inform risk assessment, the state of modeling is
currently insufficient for practical use and that instead there should be more reliance on higher
tier tests.
38
c. Please comment on the most important elements that should be considered in reviewing
available honey bee colony ecological models for potential application in risk assessments.
Panel Summary
The Panel concludes that there should be two initial questions with any model. They are: 1)
What insight does it provide that accurate empirical studies do not? and 2) How does the
model spare effort or expense to provide those insights? Furthermore, the Panel concludes that
the models introduced in the white paper are not designed to answer these types of questions.
However, they may be helpful in developing answers within each level of concern and in guiding
the risk assessment.
39
DETAILED PANEL DELIBERATIONS AND RESPONSE TO CHARGE

1. Section 2.2.1 of the white paper discusses the protection goals and associated assessment
endpoints for assessing risks to honey bees (Apis mellifera). The protection goals are:
protection of pollination services;
protection of honey and hive product production; and,
protection of pollinator biodiversity.
As described in the white paper, assessment endpoints are based on their ecological relevance,
their susceptibility to known or potential stressors and their relevance to protection goals.
a. Please comment on whether the assessment endpoints (e.g., population size and stability of
managed bees, quantity and quality of hive products, and species richness and abundance)
identified in Table 1 in Section 2.2.1 of the white paper are consistent with the Agencys
protection goals. Please include a discussion of any additional assessment endpoints that
may be necessary to meet those protection goals.
The Panel commends the Agency for doing an excellent job in writing the white paper. It is a
very thorough document. It is apparent the white paper was written with a great amount of
forethought. The Panel believes that the Agencys proposed Pollinator Risk Assessment
Framework is a step in the right direction for improving the assessment of pesticide risks to
pollinators. To further enhance the Agencys effort, the Panel recommends the following
regarding the assessment endpoints identified in Table 1 in Section 2.2.1 of the white paper.
In column 2 row 1 of Table 1 of the white paper, the term managed bees is used. The Panel
notes that the Agency should be clear in identifying managed bees as all commercial bees
including commercial bumble bees, alfalfa leafcutting bees, mason bees, and any other bee
species that may become managed in the future.
The Panel is unclear regarding how the Agency defines the term population size listed in Table
1. The Panel recommends that the Agency define the term population size to specifically mean
the numbers of colonies.
The Panel agrees that it is appropriate to identify quality and quantity of hive products as
assessment endpoints in Table 1. However, the Panel believes that it may be adequate to use
only hive product quantity as an assessment endpoint. This would avoid confusion since hive
quality can mean many things that may not be relevant to assessing pesticide risks. However,
quality of hive products would be an important assessment endpoint, particularly if it were solely
assessed on the amount pesticide residues in a hive.
The Panel believes that the Table 1 (row 3) protection goal, contribution to pollinator
biodiversity is too broad and unrealistic. The assessment endpoint of this goal, species richness
and abundance, is also too broad and unrealistic. Furthermore, there are no measures listed for
species richness and abundance throughout the Agencys white paper.
The Panel believes that this broad protection goal is not realistic because pollinators are
comprised of large numbers of organisms that include not only bee species but many other
40
pollinating insects (e.g. some butterflies, pollen wasps, pollen beetles, etc.) and other animals
(i.e. some birds, and bats). Bee species native to the Americas are also vastly diverse. There are
approximately 4000 native bees in North America, and new native bees are discovered every
year. Notably, honey bees (including the entire genus of Apis) are not native to the Americas.
Given the large numbers and diversity of pollinators and given the specific scope of the
Agencys white paper, the Panel recommends that the Agency adjusts this protection goal to be
contribution to bee diversity.
b. Please comment on whether the measurement endpoints at the level of the colony (e.g., colony
strength and survival, contamination of pollen and nectar and species richness and
abundance) identified in Table 1 are consistent with the assessment endpoints identified in the
table and any additional assessment endpoints discussed in Part a of this question. Please
include a discussion of any additional measurement endpoints that may be necessary to
represent those assessment endpoints.
With regard to the measurement endpoint of colony strength, the Panel notes that
approximately 98 % of bee species are solitary. Thus colony strength is not an applicable
measure for solitary bees. Effective population size may be the more appropriate measurement
endpoint for those other bee species. However if honey bees serve as a surrogate for all bee
species, the Panel believes that this endpoint should be fine as long the Agency is aware of this
distinction.
The Panel suggests that the Agency add colony development as another measurement endpoint
along with colony strength and survival. Colony development would entail the growth of a
colony during a growing season, in essence adding a temporal component to the measurement.
The Panel also recommends that the Agency remove the term quality but keep the term
pesticide residues within the category of measurement endpoints at the population level and
higher. In addition, the Agency should add pollen, propolis, and royal jelly to the list of hive
products where pesticide residues are measured (all of these are sold as commercial products).
The measured endpoint will read as quantity of hive products and residue levels in honey,
pollen, wax, propolis, and royal jelly. This recommendation will reflect the potential exposure
of native and honey bees to plant resins that may be contaminated with pesticides.
The Panel agrees that species richness and abundance is an important assessment endpoint;
however, measurements of this type are not mentioned in the white paper. Additionally the
Panel notes it is impossible, by definition, to assess greater species diversity using only one
species, (in this case, the honey bee) as a surrogate. This is particularly true since the honey bee
is a domesticated organism that is not a recent native to the Americas. Moreover, there is a
considerable body of research which suggests that the presence of honey beesin certain
habitats and ecological conditionsmay impose a negative impact on native species of bees
through competitive displacement. (e.g. Sugden et. al. 1996, Kremen et al. 2002, Goulson 2003,
Klein, et al. 2003, Mayer and Johansen 2003, Tepedino et al. 2007). For these reasons, the Panel
believes that the honey bee should not be used to measure species richness and diversity.
Consequently, the following Table 1 footnote is inaccurate and the Panel advises the Agency to
delete it from the Pollinator Risk Assessment Framework:
41
Table 1 Footnote:
Use of honey bees as a surrogate for other insect pollinators has limitations; however,
it is assumed that as with all surrogates, data on individual organisms as well as
colonylevel data would provide some relevant information on the potential effects of a
pesticide on both solitary bees as well as eusocial taxa. In addition, protection of honey
bees would contribute to pollinator diversity indirectly by preserving the pollination
and propagation of the many plants species pollinated by honey bees, which also serve
as food sources for other pollinating insects.
The Panel also recognizes that species richness and diversity are good assessment endpoints to
address. Nevertheless, the Agency has not addressed how this will be done in the white paper.
Genetics population modeling indicates that genetic variation within a species can be a very
effective means of determining the long term effects to population size (Laude and Barowclough,
1987; Frankham, 1995). Thus, the Panel suggests that measuring genetic variation within a
species may be a potentially useful measurement for assessing species richness and diversity.
c. Please comment on whether the measurement endpoints at the level of the individual bee
(e.g., individual adult and larval [brood] survival, queen fecundity, brood emergence
success, worker longevity) identified in Table 1 are consistent with assessment endpoints
identified in the table and any additional assessment endpoints discussed in Part a of this
question. Please include a discussion of any additional measurement endpoints that may be
necessary to represent those assessment endpoints.
Individual worker survival is a good individual-level measure. In addition, the Panel
recommends the inclusion of larval survival. Larval assays will likely be very important in
understanding pesticide effects on bees. The Panel suggests using the term larvae instead of
brood so that it is clearly inclusive of all bees and not just honey bees. The term brood ordinarily
only refers to honey bees. The Panel also recommends that the Agency also consider evaluating
larval development time. This includes the time period from when an egg is laid to when the cell
is capped and the time from capping to successful hatch. The negative effects of some pesticides
(i.e., insect growth regulators) may be best detected in this sub-lethal measure.
The Panel is unclear how the term brood success is being defined. Thus, the Panel
recommends changing this term to larval survival and delayed development instead of
delayed success (Row 2 of Table 1).
Brood size is a good measure, and there are fairly standard ways for measuring this in the hive.
However, this term may be mistaken to mean the size of individual larvae. Thus, the Panel
recommends renaming brood size to be brood nest size and define it as the area of the sealed
brood within a honey bee colony.
Queen fecundity is also a very useful endpoint, but at this time, it is very difficult to quantify.
Queen reproductive potential (sensu Delaney et al., 2011) is perhaps a better endpoint than queen
fecundity as the latter generally refers to the egg laying rate of a queen (or the total eggs in a
defined time period). Reproductive potential could include the size and quality of the brood nest,
42
or survival of eggs through the larval, pupae and adult stages.

Adult worker bee longevity can be difficult to measure because it requires taking the bees out of
their colony. Removing workers from the colony to use them in bioassays greatly reduces their
longevity, and thus may affect the study results. Another method for measuring adult longevity
is to mark or tag a large number of workers in a colony and monitor them over an extended
period of time (e.g., Rueppell et al., 2007). This may give a more reliable measure of adult
longevity, but it is also very time consuming and labor intensive. However, electronic
monitoring devices for individual bees can be used to simplify this task.
2. Section 2.2 of the white paper discusses a series of conceptual models for assessing risks of
honey bees resulting from pesticide applications. These models depict the nature of the
stressor (i.e., nonsystemic and systemic pesticides that are applied as foliar treatments, soil
and/or seed treatments, or trunk injection), its source (e.g., direct deposition on bees or
pollen), the exposure media (e.g., residues on plants, residues in/on pollen/nectar), receptors
(e.g., foraging bees, developing brood) and attribute changes (e.g., reduced [bee] population,
reductions in the quantity/quality of honey).
a. Please comment on whether the conceptual models depicted in Figures 4 through 8 are
consistent with the protection goals and assessment endpoints identified in Table 1 and
discussed in Question 1.
The Agencys conceptual models are comprehensive and provide substantial detail. However,
the Panel proposes the following revisions (See Panel proposed revisions in Figures 4-9 below).
All the conceptual models should be modified to include the potential receptor pathway/exposure
route via wax and propolis specifically during the larval stage. Wax and propolis are already
considered as a potential exposure/receptor route to adult bees. However, they also need to be
considered as potential routes of exposure for the larval bees.
Each of the models has dashed lines which represent routes of exposure that are not considered
to be major pathways. The Panel advises that the Agency replace these dashed lines with solid
lines because these pathways may potentially be significant.
Because honey bees are being used as a surrogate for all managed bee pollinators, exposures that
are potentially important to non-honey bees (referred to here as non-Apis bees) should be
included in all diagrams (even when a specific exposure is not important to honey bees). For
instance, many non-Apis pollinators are ground nesting and all life stages will have direct contact
with soil. As an example, residues in soil may be a significant source of exposure to solitary
bees that use mud (made from soil) to partition their nests. When mud is used in the nests, the
adult female bee may be exposed to residues while building her nest, and the larvae may be
exposed in the nest. Alkali bees, which nest in the soil and are used for alfalfa pollination,
provide another example of non-Apis exposure via soil. The alfalfa leafcutting bee is also an
important commercial pollinator for alfalfa seed. As many, or nearly as many, managed
leafcutting bees are moved into alfalfa seed fields (many imported from Canada each year) for
pollination as honey bees are moved into almonds for pollination. Adult alfalfa leafcutting bees
43
can frequently be found crawling on the ground in front of nesting shelters in the morning before
the day has warmed sufficiently for them to fly well. Soil exposure routes could also result from
wind and tillage generated dusts that settle on plant leaves. These leaves could be used by
leafcutting bees as part of the nesting structure, exposing both the nesting females and the larvae
that develop inside the leafy nests. Thus, the Panel recommends that soil be included as a
significant potential route of exposure in Figures 4, 5, and 6. In addition, topical exposure routes
should be added to Figure 7, and a new figure should be created to include non-systemic soil
applied pesticides for the same reason.
Abraded seed coatings and dust can drift during sowing (Krupke et al., 2012). Thus, pesticide
treated seed should be given consideration as an exposure route. In the spring of 2012 one
hundred and thirty bee incident reports associated with corn planting were reported in Canada.
In addition many reports were made in the US (although most of the US reports are being
analyzed by state labs and have not yet been reported to the EPA). In Indiana all the dead bees
from the incidence reports made to the State contained residues of the neonicitinoid insecticide,
clothianidin.
The Panel believes that it would be a good idea to consider summing the larval RQs from oral
and contact exposures rather than evaluating the RQs separately. This idea would mimic the
simultaneous acute and oral exposures that occur for the larvae.
Also in regards to bee larvae, the total food consumption during larval stage would be a better
assessment of larval dietary exposure. Using the total food consumption would more accurately
assess the exposure of honey bee and non-Apis bee larvae. For honey bee larvae the period of
time over which food is consumed is a short 7 days and food provisions for solitary bee larvae
are typically collected in a single day.
44
Non-Systemic Pesticide: Foliar Spray Application
Stressor
Source
Spray Deposition
On Bees
Deposition onto
Plants
Residues On
Plant
Surfaces
Exposure
Media
Deposition onto
Soil
Receptors
Residues On
Pollen, Nectar,
Exudates, Honey
Dew, Non-Crop
Plants
Residues
In Soil
Dermal Uptake &

Inhalation
Residues
in Surface
Water
Ingestion
Wax,
Propolis
Foraging Bees
(workers)
Bee Brood
Hive Bees (Nurse,

Pollen & Nectar Processing, Worker, Drone**)
Ingestion; Comb Production
Attribute
Change
Deposition onto
Surface Water
Runoff/
Erosion
Population Size and Stability of Colonies

Reduced colony strength and survival
Reduced queen fecundity & brood success
Reduced individual survival, behavior changes
Royal Jelly
Queen**
Quantity and Quality of Hive Products

Reduced honey, wax, propolis production
Contribution to Pollinator Biodiversity
Reduced species richness and abundance
* Brood initially rely on royal and brood jelly, but later consume processed pollen and honey; whereas queens rely solely on royal jelly.
** Interception of spray droplets is also a potential route of exposure during mating and orientation flights
Figure 4. Generic Conceptual Model of Non-Systemic, Foliar-Applied Pesticides for Honey Bee
Risk Assessment.
45
Systemic Pesticide: Foliar Spray Application
Stressor
Source
Spray Deposition
On Bees
Deposition onto
Plants
Deposition onto
Soil
Foliar Translocation
Residues On
Plant
Surfaces
Exposure
Media
Residues
In Soil
Dermal Uptake &

Inhalation
Receptors
Foraging Bees
(workers)
Root
Uptake
Residues In (On)
Pollen, Nectar,
Exudates, Honey
Dew, Non-Crop
Plants
Residues
in Surface
Water
Ingestion
Wax,
Propolis
Bee Brood
Hive Bees (Nurse,

Pollen & Nectar Processing, Worker, Drone**)
Attribute
Change
Deposition onto
Surface Water
Runoff/
Erosion

Royal Jelly
Queen**

* Brood initially rely on royal and brood jelly, but later consume processed pollen and honey; whereas queens rely solely on royal jelly.
** Interception of spray droplets is also a potential route of exposure during mating and orientation flights
Figure 5. Generic Conceptual Model of Systemic, Foliar-Applied Pesticides for Honey Bee Risk
Assessment. Red arrows depicts systemic pathways. The red font indicates the Panels proposed
revisions.
46
Systemic Pesticide: Soil Application
Stressor
Runoff/
Erosion
Source
Residues in Soil*
Root Uptake
Exposure
Media
Residues in
Surface Water
Residues In (On) Pollen,

Nectar, Exudates, NonCrop Plants
Ingestion
Receptors
Wax,
Propolis
Foraging Bees
(workers)
Bee Brood
Hive Bees (Nurse,

Pollen & Nectar Processing, Worker, Drone***)
Attribute
Change

Royal Jelly
Queen***

* For spray applications to soil, exposure of bees via off site drift of pesticide would be addressed as illustrated for foliar spray
applications, accounting for the amount of pesticide drift. ** Brood initially rely on brood jelly and royal jelly, but later in development
consume processed pollen and honey; whereas queens rely solely on royal jelly. *** Interception of spray droplets is also a potential
route of exposure during mating and orientation flights
Figure 7. Generic Conceptual Model of Soil-Applied Systemic Pesticides for Honey Bee Risk
Assessment. Red depicts systemic pathways. Red arrows depicts systemic pathways. The red
font indicates the Panels proposed revisions.
48
Stressor
Non-Systemic Pesticide: Soil Application
Source
Runoff/
Erosion
Exposure
Media
Residues in
Surface Water
Residues in Soil*
Residues In (On) Pollen,

Nectar, Exudates, NonCrop Plants
Ingestion
Receptors
Wax,
Propolis
Foraging Bees
(workers)
Bee Brood
Hive Bees (Nurse,

Pollen & Nectar Processing, Worker, Drone***)
Attribute
Change

Royal Jelly
Queen***

* For spray applications to soil, exposure of bees via off site drift of pesticide would be addressed as illustrated for foliar spray
applications, accounting for the amount of pesticide drift. ** Brood initially rely on brood jelly and royal jelly, but later in development
consume processed pollen and honey; whereas queens rely solely on royal jelly. *** Interception of spray droplets is also a potential
route of exposure during mating and orientation flights.
Figure 8: Generic Conceptual Model of Soil-Applied Non-Systemic Pesticides for Honey Bee
Risk Assessment. The red font indicates the Panels proposed revisions.
49
Systemic Pesticide: Trunk Injection
Stressor
Residues in
Plant Trunk
Source
Translocation
Residues In Pollen,
Nectar, Exudates,
Non-Crop Plants
Exposure
Media
Ingestion
Receptors
Pollen & Nectar Processing,

Attribute
Change
Wax,
Propolis
Foraging Bees
(workers)
Bee Brood
Hive Bees (Nurse,
Worker, Drone)

Royal Jelly
Queen

* Brood initially rely on brood jelly and royal jelly, but later in development consume processed pollen and honey;
whereas queens rely solely on royal jelly.
Figure 9. Conceptual Model of Trunk-Injected or Trunk-Drench Systemic Pesticides for Honey

Bee Risk Assessment. Red arrows depicts systemic pathways. The red font indicates the Panels
proposed revisions.
A few other potential routes of exposure are missing from the conceptual models. Non-crop
plants (weeds, other flowering plants) may be a significant source of pollen, nectar or propolis
and may be impacted by overspray. Additionally, not all plants in a field are crop plants; some
of these may provide resources to pollinators and the plants may take up residues in soils. This
possibility should be incorporated into the models.
The wax and propolis may become contaminated by foraging bees that receive pesticide
exposures which may then become a source of repeated pesticide exposure to hive bees (nurses,
workers, and drones). This may also lead to one means of exposure to the brood. If the
contaminants are persistent in wax, contaminant levels could increase over time. It is also
possible, if the contaminant is volatile, that there could be inhalation exposure.
Surface water is assumed in the Agency models to be a minor source of pesticide exposure, but
the Panel does not completely agree. There are two types of water used in the hive: 1) water that
is consumed by the bees and 2) water that is used for cooling the colony. A significant
proportion of the water collected by bees is used for cooling. Any pesticide contaminants in the
50
water will remain in the hive after the water has evaporated providing a source of future
exposure to the bees. Thus, puddle water and water from irrigation ditches should be included in
the surface water exposure. Pesticide residues in puddle water and water from irrigation may
contribute relatively high exposures to bees. Thus, the Panel recommends that these be added
explicitly as potential surface water routes of exposure.
It is true that foraging bees are the main life stage that receives initial exposures, but their only
function may be to transport potentially contaminated materials. These bees do not necessarily
ingest the materials gathered, e.g., nurse bees consume more pollen than do foragers. Likewise,
foragers transport water to cool the hive. Foragers carry propolis and may have dermal contact
with residues. But often, it is lifestages within the colony (or nest in the case of solitary bees)
that have the greatest exposure rates, or consumption rates, of contaminated materials.
3. The focus of the white paper and proposed risk assessment process on the honey bee reflects
two important factors: 1) honey bees are considered one of the most important pollinators
globally from both a commercial and ecological perspective; and 2) standardized test
methods for evaluating exposure and effects of chemicals in a regulatory context are more
developed with the honey bee compared to non-Apis bees. Both the Introduction (Section 1)
and the Problem Formulation sections (Section 2) of the white paper indicate that honey bees
have historically served as a surrogate for other beneficial insects. As discussed in Section
5.3 of the white paper, there is uncertainty regarding the extent to which honey bees serve as
surrogates for native species, especially where life history strategies and differential
sensitivity across species render native species more or less vulnerable to pesticides.
a. Please comment on the extent to which the assessment of risks to the honey bee may serve to
meet the protection goals identified in the white paper (i.e., protection of pollination
services; protection of honey and hive product production; and protection of pollinator
biodiversity).
b. Until guidelines are developed for testing non-Apis species of bees, please comment on the
extent to which the honey bee may or may not serve as a reasonable surrogate for non-Apis
bees, given the differences in life history strategies and potential different sensitivities to
pesticide toxicants. Please include a discussion of which types of non-Apis bees may be
particularly well represented by either the individual-level or colony level endpoints
identified in Table 1 of the white paper; as well as which types of non-Apis bees may not be
as well represented, and therefore, may be the focus of potential areas for future research.
Because subpart Questions 3a. and 3b. are closely related the Panel prefers to respond jointly to
them. The Panel agrees that it is appropriate for EPA to use surrogates for ecological risk
assessment for all bees and that honey bees serve as a reasonable surrogate. Honey bees vary in
their susceptibility to pesticides relative to other bee species;however, this variance is not large.
Furthermore, honey bees are easier to obtain than most other bees, and testing methods are more
readily available.
If honey bees are used as a surrogate species, it is important that EPA risk assessors and
managers recognize that these species are merely representative of other bee species.
51
In some circumstances differences between honey bees and other bees may need to be taken into
account. For example, solitary bees do not have other hive products (i.e. honey, wax, and royal
jelly) that are used by people. Also, these bees may be more dependent on pollen for nutrition
than other bees, and consequently, they may consume more pollen, or proportionately more
pollen than nectar. If pesticide residues are different in pollen than nectar, this could be
important for evaluating risks.
Honey bees do not spend time in the soil, or on the soil surface. Therefore, the white paper does
not include risk diagrams for non-systemic pesticides applied to the soil, and the pathways do not
include contact toxicity for any soil applied pesticides. However, many solitary bees and bumble
bees nest in the soil. Others collect soil to make mud partitions in cavity nests. Thus, non-Apis
bees do come into contact with the soil, and therefore, contact toxicity tests should be included in
risk assessments for both the adults and larvae. Honey bees could not be used for these tests as
surrogates.
Also, the complex social behaviors of honey bees may buffer them against environmental
stresses in ways that other bees cannot. For example, many native bees are specialist pollinators.
That is, they collect their food (pollen and nectar) from a limited number of plant species. NonApis bees also often have much shorter seasons than honey bees. The adults may construct their
nests during a short window of time (a few weeks), and after that, the other life stages are
contained within the nest until the next season. Thus, all the pollen and nectar collected during
this window is what feeds the next generation of bees. Honey bees can store food for long
periods, allowing them to avoid collecting nectar and pollen from undesirable sources. Also,
honey bees have a highly plastic division of labor among its facultatively sterile workforce, but
for solitary bees, all females are reproductive females. Thus, adult mortality could have a greater
impact on the native bee populations the next year than for honey bees. For solitary bees, the
individual measures are more important than the colony-level measures. Bumble bees form
small colonies but overwinter as individual queens (the colonies do not overwinter), so
individual-level measures are probably more important for bumble bees, as well.
The Panel suggests that EPA include other bee species for testing as well. The alfalfa leafcutting
bee, Megachile rotundata and Osmia spp. (mason and orchard bees) are the easiest to include for
Tier I testing. Both these bees are commercially available in large numbers and would be fairly
easy to use for higher tiered tests, as well. Bumblebees (Bombus spp.) are also available
commercially, and considerable research is available on how to raise them. They would be
useful for Tier II tests, although it is more difficult to assess their larval development, brood-nest
size, and larval mortality. The Panel recommends that EPA consider using at least one
additional bee species other than Apis mellifera to address the goal of protecting diversity.
52
4. Contact Exposure. The exposure characterization of the white paper (specifically, Section
3.1.1.2) proposes a screening-level (Tier I) approach for quantifying contact exposure to
foraging bees for pesticides applied via foliar spray. This proposed method is based on the
maximum of residue values on honey bees from a field study conducted by Koch and Weisser
(1997). The white paper also discusses a method based on the T-REX upper-bound
concentration for arthropods directly sprayed with pesticides while located directly on a
treated field. Although the second method is not proposed for the Tier I exposure assessment
for honey bees, it could be used to assess contact exposures to other insect pollinators.
a.
Please comment on the strengths and limitations of the proposed approach for assessing
contact exposures to honey bees in Tier I exposure assessments (i.e., 2.7 g a.i./bee per 1 lb
a.i./A), which is based on the honey bee specific maximum concentration reported by Koch
and Weisser (1997).
Direct contact by foliar pesticide sprays can result in some of the highest exposure levels (other
than dietary exposure to foliar spray). Consequently, this could lead to the highest level of
exposure to foraging bees. Data for bee contact exposure to key pesticides is lacking, thus a
proxy methodology for estimating contact exposure is necessary. To this end, the approach
described in the white paper has merit; but, for many reasons, this approach also has limitations.
In the absence of data, the T-REX model is an alternative that can help identify sensitive
parameters and provide general ranges of residue levels. However, relying on a model when
actual data is available is not advisable. Thus, T-REX for non-Apis bees is more reasonable than
for Apis bees. Generally, Apis bees have been studied far more and have considerably more data
available than non-Apis bees. Thus, T-REX may be the best approach for non-Apis bees and
may help fill data gaps for Apis bees.
The Panel identifies the following strengths and weaknesses of the proposed method.
Strengths:
The surrogate tracer used in the Koch and Weisser (1997) study most certainly was not
being used anywhere in the region. Thus there are no possible confounding factors
associated with bees foraging in unknown areas where the spray was applied.
The concentration reported was the highest value (normalized), and thus should be
protective.
Weaknesses:
The study was conducted in 1997. A 15-year-old study is not necessarily poor just
because of its age, but follow-up and updating are in order.
The compound used was sodium fluorescein, a fluorescent dye. Its chemistry may be
radically different from any pesticide, and one cannot assume it is an appropriate
surrogate.
Bees were foraging during application and subject to direct spray. This may have
contributed to anomalously high exposure estimates.
Normalization to a single application rate assumed a linear relationship between rate of
spraying and rate of accumulation by the bees. This is not necessarily valid.
53
The Koch and Weisser (1997) approach is reasonable, but the formulation of the spray
for the fluorescein is important. It is unknown whether the fluorescein sprayed behaved
the same as fully formulated pesticides since spreaders and stickers, surfactants and other
adjuvants are routinely combined in pesticide sprays. These adjuvants have a large
impact on the distribution and fate of pesticides sprayed on leaf surfaces. Also, it is
likely that flower surface areas differ substantially from grass stems. This is important
since cuticular waxes and other components on plant surfaces may impact pesticide
behavior. Panel members note that there appears to be a pressing need to answer these
and related questions experimentally.
Reporting pesticide loads in terms of per bee rather than per unit mass (e.g., per mg) is a
concern. The Panel believes that this will make for a better transference of
measurements. Reporting pesticides on a surface area basis may apply to other areas of
the paper as well. One panel member suggested that per unit mass for queen would not
be a good choice due to the unique aspects of the feeding and longevity of queens.
The Panel expressed concerned about studying only one race of bee.
The consumption rate being proposed was on a per day basis. For larvae, the
consumption is not the same over the full development period. Thus, total consumption
for larvae may be a better approach than consumption on a per day basis.
The Panel recommends that integrating mass accumulated over time as a good approach
for the adult bees but not for the larvae.
Please comment on the potential utility of the T-REX upper-bound residue value (i.e., 12 g
a.i./bee per 1 lb a.i./A), for a broader number of arthropod species to represent contact
exposures to honey bees and to other insect pollinators that are directly sprayed with
pesticides.
b.
As noted in Panels comments on Question 4a, direct studies of bee exposures to foliar applied
chemicals are preferred. In the absence of such data, the Panel believes that a model may be a
suitable alternative. However, there is substantial uncertainty. The Panel encourages the
implementation of a bee exposure study which will generate these data.
In regard to the potential utility of the T-REX upper-bound residue values, the Panel points out
the following strengths and weaknesses of this approach.
Strengths:
The data used in generating T-REX represent actual measurements on arthropods and are
expected to be reflective of what might be expected for honey bees and non-Apis bees.
The arthropod data used to generate T-REX are probably no more uncertain than tracer
estimates.
54
Weaknesses:
T-REX was developed based on 14 studies using carbamate and organophosphate

insecticides. Other pesticides, e.g. the neonicotinoids, have a totally different chemistry,
thus whether they behave similarly is unknown.
The original data used in developing T-REX are subject to some question as to the route
of exposure.
Doses and residues are based on normalization that assumes linear upscaling or
downscaling, and this may not be the case.
Given strengths and weakness of the T-REX approach, one panel member suggests a
potential alternative for estimating the interception of a pesticide during a spray application
to a crop. The approach involved consideration of a standard spray rate of 1 lb acre-1 which
is equivalent to 11 g cm-2. Using the reported mean surface area of a honey bee, 2.4 cm-2
(Roberts & Harrison, 1999) and assuming 100% coverage of a bee during spraying, the
maximum potential exposure can be evaluated by multiplying the surface area times the
spray rate. In this case the value is estimated to be 26 g per bee. Comparison of this value
to the T-REX upper-bound residue estimate of 12 g per bee indicates that T-REX approach
would result in assuming an interception rate of about 45%. Interception at this rate appears
high for a number of reasons, thus the Panel felt that the T-REX estimate was reasonably
conservative. This was based on Panel discussions that pesticide sprays to the environment
entail a 3 dimensional intercept of pesticide residues (i.e. interception to the various layers of
media/biota including plant leaves, stems, and the ground) thus limiting the amount of
pesticide that a bee may intercept. A caveat is that the hairs on bees bodies may enable them
to retain spray residues at much higher levels than their body surface area (Mean surface
areas were: head, 26.80.3 mm2; abdomen, 79.52.2 mm2; thorax (minus legs and wings),
62.81.0 mm2; legs, 68.31.1 mm2). In conclusion, comparison of the direct spray-surface
area calculations to T-REX estimates suggests that the T-REX value may provide a
reasonable upper bound estimate. In response to this, one panel member adds that, in terms
of surface area, perhaps we should consider only active adsorbing surface area. However,
another panel member does not like the interception approach for two reasons: the 3
dimensional nature of spraying and the ability of the bees to retain sprays through little hairs
on their bodies.
5. Dietary Exposure (Consumption Rates). As discussed in the effects assessment section
of the white paper (Section 4.1), acute oral toxicity data (LD50) are necessary for adult and
larval bees in order to characterize the potential risks of a pesticide. Because these toxicity
data are expressed on a dose basis (i.e., g a.i./bee), it is necessary to convert estimated
concentrations of pesticides in food (expressed as mg a.i./kg) into doses. Honey bees fulfill
their nutritional requirements through consumption of nectar, honey, and bee bread
(pollen/honey). In addition to requiring bee bread and nectar or honey, bees also require
royal jelly and brood food (jelly) to fulfill their nutritional requirements. In the proposed
approach, it is assumed that exposures through consumption of nectar and pollen are
conservative representations of potential exposures through consumption of honey and bee
bread, respectively. This approach is likely to be conservative because it assumes that
55
pesticides do not degrade while honey and bee bread are stored in the hive and have
undergone some degree of processing (e.g., fermentation). For bees that consume honey, it
is assumed that the estimated pesticide exposures can be related back to the original
concentration in nectar by accounting for the amount of sugar consumed by bees. It is also
assumed that pesticide exposures through consumption of pollen and nectar are protective
of pesticide through consumption of royal jelly and brood food given that empirical data
indicate that pesticide concentrations in royal jelly are a >100 times lower than
concentrations in food consumed by nurse bees. In the proposed approach, pesticide doses
received by bees are calculated using nectar and pollen consumption rates for larval and
adult worker bees. As discussed in detail in Appendix 1 of the white paper, the proposed
values for larvae and adult workers are based on an analysis conducted by EPA, which
built upon work published by Rortais et al. (2005), Crailshaim et al. (1992 and 1993) and
others. For larvae, the proposed total food consumption rate is 120 mg/day, which is based
on the total daily consumption of pollen and nectar (based on honey consumption) by
larvae during day 5 of the uncapped larval life stage. For adult worker bees, the proposed
food consumption rate is 292 mg/day, based on food consumption rates of nectar foraging
bees, which are expected to receive the greatest dietary exposures among different types of
worker bees. In addition, as discussed in Appendix 1, it is likely that these food
consumption rates are protective of drones and queens.
a. Although bee larvae typically consume processed foods in the form of royal jelly and brood
food throughout much of their development, they also consume honey and pollen during the
last two days of the uncapped period. Please comment on the proposed use of nectar and
pollen consumption rates of larvae during the last day of the larval developmental stage.
Please include a discussion of the conservatism, strengths and limitations of this approach as
well as a discussion of how this value may or may not correspond to data generated from
larval toxicity endpoints.
The Panel generally agrees that unprocessed pollen and nectar will represent a worst case
scenario and conservative estimate over processed foods such as brood food or royal jelly. The
data presented by EPA on the nearly 100-fold decrease in residues from pollen or nectar into
royal jelly supports the conclusion that food processing by nurse bees results in low residue
levels in royal jelly, brood food, or both.
Concerning larval assays these studies are conducted using dilute royal jelly but the spiking of
this food with specific levels of pesticides does allow for an oral larval exposure. The absence of
an artificial diet for larval bees necessitates the use of royal jelly for larval rearing but each lot of
royal jelly has to be tested in order to be certain it is free of antibiotic and/or pesticide residues.
Recent studies by Crailshiem and colleagues in Austria have demonstrated that larval rearing can
be completed and a high level of pupation and adult emergence achieved along with test in
observation hives which demonstrated that these in vitro reared individuals had equal life-span
and foraging rates as colony (in vivo) reared sister worker bees (Prevention Colony Losses
Network (COLOSS), 2010). Thus, with practice the larval rearing can be used or extended to
examine milestones in development such as pupation and adult bee emergence.
56
The proposed method seems sufficiently conservative except that the Panel questions the Tier I
laboratory larval feeding concentrations. The white paper identifies the concentration in royal
jelly as being a factor of 100 lower than the original concentration bees ingest before processing,
but the Panel recommends using the original estimated adult ingestion concentration because the
lower value was derived on too small a number of substances.
The food intake seems to be highly conservative as the value of 120 mg per day is assumed;
definitely larvae of the first up to the last larval stages would consume less. This value is even
higher than the likely ingestion in the last larval day, when the feeding rate is at its peak. This is
confirmed by comparing the value of 120 mg to the amounts used in the feeding regime in the invitro test of Aupinel which is 50 L of total food on Day 6 ( and 160 l over the whole larval
development), even if the density of the food is higher than 1. It has been demonstrated that with
the feeding regime used in the Aupinel et al. (2005) method a normal bee size will be obtained.
The Panel believes that it would be a good idea to consider summing the larval RQs from oral
and contact exposures rather than evaluating the RQs separately. This idea would mimic the
simultaneous acute and oral exposure that occurs for the larvae. (See discussion of contact
exposure in brood cells in Question 2.)
Also in regards to bee larvae, the total food consumption during larval stage would be a better
assessment of larval dietary exposure. Using the total food consumption would more accurately
assess the exposure of honey bee larva and the exposure of non-Apis bees would be more
accurately approximated. For honey bee larvae the period of time over which food is consumed
is a short 7 days, and food provisions for solitary bee larvae are collected in a single day.
b. Please comment on the strengths and limitations of basing the Tier I screen for adult honey
bees on food consumption rates of nectar foraging bees, including a discussion of the
conservatism of this approach, and how it relates to other types of worker bees and castes.
Tier 1 screening using nectar consumption only is generally appropriate but may not be as valid
if newly-emerged bees are used in the Tier 1 assay as these young bees would normally consume
large amounts of pollen rather than nectar. Many Tier 1 studies use random aged bees in which
case nectar consumption alone for these tests is appropriate.
Queens and drones do not normally feed themselves but are rather fed by worker bees and thus
the testing in Tier 1 is acceptable to determine LD50 values. However, some consideration must
be made as to the high rate of feeding that the queen receives during a day and thus she has the
potential to receive a much higher exposure than workers alone. This is in part moderated by the
demonstrated lower residue levels found in brood food that is fed to queens. One member of the
Panel suggests using protein needs for egg production to estimate consumption rates for queens
in a way analogous to the way energetic flight needs were used to estimate consumption rates for
foragers.
One simple means to adjust for caste and species differences is to look at exposure as a function
of bee weight as opposed to on a per bee basis as is currently done. The chosen value will cover
all other bees and seems highly protective for nectar consumption of other casts; as it is
57
concluded most energy is needed for foraging activity and other casts are also covered. In
theory, pollen foragers should also have the same energy demand as nectar foragers. Even if it is
not clear if the pollen forager nectar consumption is underestimated or the nectar value is
overestimated for nectar consumption, the proposed values seem sufficiently conservative for
Tier I. The Panel also agreed that use of consumption rates during normal colony processes
may be insufficiently conservative for estimating risk from consumption of contaminated honey
or pollen stores during rare but unavoidable circumstances (e.g. nest disruption, smoking,
swarming, etc.). Under cases in which bees are expected to gorge on stored food, there may be
short bursts of increased exposure from consumption without any difference in the exposure per
unit of food and these would be very important to take into account for long-term colony
viability.
c.
Please comment on the assumption that exposures through consumption of nectar and pollen
are conservative representations of potential exposures through consumption of honey, bee
bread, brood food and royal jelly, all of which represent processed foods
The Panel concurs that nectar and pollen are conservative representations of exposure levels
compared to processed brood food (honey and bee bread) and royal jelly. However, one panel
member notes that this assumption is not readily extrapolated to native bees because as larvae
they are receiving provisions of pollen and potentially a little nectar. However, native bee larvae
arent fed brood food or royal jelly.
Although the Panel agreed that the processed food would have lower pesticide concentrations,
there is some uncertainty regarding the degree to which bee food processing affects pesticide
concentrations.
6. Dietary Exposure. The dietary exposure methods described in Section 3.1 of the white
paper differ in the nature of the estimated concentrations in pollen and nectar consumed by
bees. For foliar spray applications, the proposed approach involves the use of the tall-grass
residue value from the T-REX model (v. 1.5) as a surrogate for pesticide concentrations in
nectar and pollen. For soil treatments, the white paper proposes the use of the Briggs model,
which is designed to estimate pesticide concentrations in plant shoots resulting from plant
uptake of pesticides from treated soil. Estimated pesticide concentrations in plant shoots are
proposed as a surrogate for concentrations in pollen and nectar. For seed treatments, the
white paper proposes the use of the International Commission for Plant-Bee Relationships
(ICP-BR) 1 mg a.i./kg concentration as an upper-bound concentration in nectar and pollen.
The paper explores the strengths and limitations of each method relative to the ability to
derive reasonably conservative estimates of pesticide exposures to bees, with a focus on how
well the estimates relate to empirically based measures of pesticides in pollen and nectar
from crops treated with pesticides.
a.
Foliar spray: Please comment on the analysis presented in Section 3.1.1.1, with a focus on
the extent to which the T-REX tall-grass upper-bound residue may serve as an adequate
surrogate to represent upper-bound pesticide concentrations in pollen and nectar of flowers
that are directly sprayed with pesticides.
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Due to the limited data on actual residue data on pollen and nectar, the Panel believes that the
use of the T-REX model was necessary to estimate upper-bound pesticide concentrations in
nectar and pollen. The Panel notes the following strengths and weaknesses of using T-REX to
perform these estimations.
T-REX Strengths for nectar residues:
T-REX is a model currently endorsed and used by US EPA in Tier 1 studies.

The model was developed using experimental (empirical) observations on stems of
plants.
The model uses very few input parameters.
The nomograph employed uses a large quantity of field data. The upper-limit values are
the upper bound of residue values from actual measurements.
Empirical data for nectar concentrations were compiled to evaluate T-REX upper
boundaries. Seven studies were used.
The T-REX values were compared to several field studies, and the upper bound was
selected to be conservative without being excessively restrictive. Tall-grass was chosen
because it is 3 times higher than the highest upper bound in the nectar empirical data.
T-REX Strengths for pollen residues:
Eleven studies for direct spray were used in developing T-REX.

T-REX values compared to empirical values showed T-REX for tall-grass is 2-times
higher than the highest measured pollen value.
Twenty three data points were employed in the empirical data set.
The 110 mg/kg (per 1 lb a.i./acre) limit should be protective.
T-REX Weaknesses for nectar and pollen residues:
Actual nectar and pollen data are limited making this value subject to high uncertainty.
Normalizing to 1 lb a.i./acre assumes that changes are linear.
The model does not contain actual values for pollen and nectar from flowers that were
directly sprayed.
The highest empirical values correspond to a mean measurement of pesticides in nectar,
not a maximum. Therefore, the comparisons were made to T-REX means not upper
bounds.
Crop specific factors cannot be accounted for.
T-REX for tall-grass appears conservative, but some published data summarized in the
white paper to support this conclusion appear uncertain. In particular a review of the
manuscript by Choudary and Sharma identified questions about analytical limits of
detection and study design. As indicated this was a field study in which pesticide was
applied at 50% bloom with a backpack sprayer. Pollen was collected from bee legs, and
nectar removed from stomachs. It is unknown whether bees foraged exclusively in
treated areas or had access to flowers that opened after spray application. Further it is
59
unknown whether flowers and stems received the same dose from the broadcast spray.
Table 6 suggests this, but data are limited. Finally it was noted that flower morphology
may be important (e.g., dandelion versus tomato blossom) and that solubility may govern
nectar concentrations and define upper concentrations. Panelists concluded that
relatively simple studies to assess pesticide solubility in surrogate nectar (30% sucrose)
may provide useful insights.
T-REX may indeed be conservative when considering only the active ingredient, but it
may not be representative of how the formulated product may behave in the environment.
The Panel suggests exploring the managed pollinator coordinated agricultural project that has
managed aviaries in several states throughout the US (Mullin et al., 2010). This project has
collected a significant amount of pesticide residue data on various media including bees, pollen,
wax etc. These studies may help the Agency to identify maximum pesticide concentrations on
pollen and nectar.
b. Soil applications: Please comment on the analysis presented in Section 3.1.2, with a focus on
the extent to which the Briggs model may generate estimates of pesticide exposure in plant
stems that can represent upper bound pesticide concentrations in pollen and nectar of
flowers.
There are several strengths and weaknesses associated with using the Briggs model analysis to
predict pesticide exposure estimates in plant stems. They are as follows:
Briggs model strengths:
a. The Briggs equation was selected by United Kingdoms Environmental Agency as
coming closest to estimating empirical data. Requirements: must be more conservative
than empirical but within an order of magnitude.
b. This approximation is also used in other models such as PRZM.
c. All pesticides used in developing the model were non-ionic.
d. The range in log Kow values was -0.57 to 4.6, and this range will include the
neonicotinoids.
e. The original model was based only on the log Kow and regression analysis of
experimental data.
f. The Ryan modification added three soil parameters to make the model more specific: soil
bulk density, soil water content, fraction of organic content in the soil.
g. The resulting model was tested against experimental data on five chemicals. Modeling
was conservative to maximize concentrations in solution.
h. Predicted data was within an order of magnitude of experimental.
i. To make the model more conservative, the model was redeveloped by including an extra
data point eliminated by Briggs and adding 95th percentile upper bound estimates of
TSCF.
j. One of the panel members commented that stem concentrations are conservative relative
to pollen.
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Briggs model Weaknesses:

a. It is a model that examines nonionic compounds only. Pesticides that ionize will not be
well represented by this approach.
b. Pesticides tested were carbamates (insecticides) and phenyl-ureas (herbicides) and on one
species of plant (barley).
c. The soil parameters used in the Ryan modification may not be known, particularly the
soil moisture content. Bulk density and foc are spatially dependent.
d. The model is used for stem transpiration stream concentrations, not pollen or nectar.
e. In testing the model against 5 chemicals with experimental data, foc was assumed to be
0.01, and bulk density and soil water content were set to a relatively high value. Multiple
assumptions were made, and this defeats the purpose of putting in soil specific
parameters.
f. Concentrations in stem transpiration stream were assumed to be equivalent to
pollen/nectar concentrations.
g. Not all values predicted by Briggs model were greater than experimental data.
h. Re-modeled data with 95th percentile upper bound did not bring all the data above the
empirical data. Therefore, this approach is not fully conservative.
i. An upper bound on water concentration of the pesticide determined by the solubility of
the compound in question needs to be considered. It is quite possible to have calculated
concentrations that exceed the water solubility, and this should be avoided.
j. Briggs et al is a good first effort. As noted the need exists for data for other plants, and
transport of weak acids and bases are not covered by the equation but are impacted by pH
both in and out of plant. One possible alternative is the Dynamicrop model which
appears to be much stronger mechanistically (Frank et al., 2012). The model is freely
available.
The Briggs relationship was evaluated by Burken and Schnoor with another plant species and a
much broader array of chemicals (Burken, & Schnoor, 1998). These data should be part of the
Agencys evaluation of the Briggs model. This will require recalculating the 95th percentile
upper bound for the equation.
One of the panel members commented that stem concentrations are conservative relative to
pollen. Experimental data show this.
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c. Soil applications: Please discuss the relative strengths and limitations of the 1 mg a.i./kg value
and the soil uptake model (the Briggs model) proposed in the white paper as Tier 1 screens,
including consideration of the extent to which this method may generate conservative Tier I
estimates of dietary exposures to bees. Does the Panel conclude that the one approach may
be better suited to specific types of assessment scenarios? If so, please elaborate.
Alternatively, if both approaches are equally suited for a Tier I screen, please provide
guidance on how to be capture variability and uncertainty in the exposure estimates using the
two approaches.
The Panel provided a review of the Briggs model in the above Question 6b. Thus, it will not be
addressed further here (in the response to Question 6c). In the discussion immediately below
(Question 6d), the merits of the 1 mg a.i./kg value are discussed and will not be repeated here.
Rather, this discussion will focus on the relative merits of Briggs versus the EPPO approach in
the complete absence of empirical data.
The EPPO approach is the default position assuming that nothing is known about the soil, plants,
or pesticide. This approach assumes that any attempt to estimate pesticide residues offers no
more reliability or unreliability than simply assigning a value.
The Briggs model approach makes an attempt to integrate information about soil, plant, and
chemicals and make a projection of the pesticide concentrations in pollen and nectar. As
discussed earlier, the Briggs approach is riddled with uncertainties and weaknesses, but it does
offer a more rational and defendable approach than the EPPO approach. Because the default
concentration does not take into account pesticide properties, the Briggs et al. approach is much
stronger mechanistically. In conclusion, considering the limitations of the Briggs model and the
EPPO approach, the best option is to attain more pollen and nectar pesticide concentrations.
62
d. Seed Treatments: Please comment on the analysis presented in Section 3.1.3, including a
discussion of the strengths and limitations of the use of 1 mg a.i./kg value as an upper-bound
concentration for pollen and nectar of seed-treated crops.
Section 3.2.2 of the Agencys white paper states, if pesticide-specific residues in pollen and
nectar are not available, a screening value of 1 mg a.i./kg plant matrix is the assumed exposure
(EPPO, 2010). This assumption is based on the upper limit value from empirical data of
pesticide concentrations in different plant parts. The Panel believes the respective strengths and
weakness of utilizing this value are as follows:
Strengths
The white paper states that 1 mg a.i./kg tends to be higher than reported values.
Most pesticides tend to be 2 orders of magnitude below the selected value.
Weaknesses:
a. Selecting a value is inferior to acquiring experimental data.
b. The value is not completely protective.
c. This value takes into account no aspect of field situations.
d. The Briggs model is stronger mechanistically.
e. Need more data.
Given the above list of strengths and weaknesses the Panel concludes that if the only goal is to
generate a conservative value for Tier 1, this is an acceptable approach. Otherwise, this is a very
poor substitute for true data.
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e. Please comment on other approaches or data that should be considered for estimating upperbound estimates of pesticide residues in pollen and nectar as a Tier I screening-level assessment
for pesticides applied via foliar spray, soil application or seed treatment.
As listed in the Agencys white paper, the other methods for estimating upper-bound estimates of
pesticide residues in pollen and nectar for a Tier I screening-level assessment for pesticides
applied via foliar spray, soil application or seed treatment are:
Direct measurement of the pesticide in question on the plant parts of interest (nectar,
pollen, etc.).
Direct measurement of the pesticide in question in other plant tissues (stems, leaves, etc.).
Direct measurement of surrogate pesticides in plant tissues.
Modeling of pesticides in the plant tissues after foliar spraying (T-REX).
Modeling of pesticide uptake from soil after seed application (Briggs/Ryan).
Assigning a default value when no other method is available.
Variations of these approaches are available including different models, different ways of
designing experiments, different uptake algorithms, and different default values. However, these
are simply tweaks to the approach and not truly different.
The Panel believes the Agency needs a data call-in followed by a rigorous evaluation of the data.
This was noted in the Pellston executive summary. Much of what has been proposed appears
conservative, but uncertainties are high.
7. Consideration of other Exposure Pathways. The proposed measures of exposure are based
on what are believed to be the primary routes, i.e., direct contact and ingestion of
contaminated pollen and nectar. Additional routes of exposure are considered (e.g., dust,
drinking water), but not included in the proposed Tier I exposure assessment method. As
discussed in Section 3.1.4.1 of the white paper, effective quantitative screening methods for
estimating exposures through contaminated dust are not discernible at this time. The most
effective management of bees exposure to pesticides through dust appears to be through
pesticide application (e.g., stickers) and seed planting practices, especially since dust exposure
is expected to be a concern for only a limited number of pesticides and application scenarios.
In regards to pesticide exposures through drinking water, Appendix 2 presents an analysis of
potential exposures to bees through various sources of water to support the exclusion of
drinking water exposure in the Tier I screen. The results of this analysis indicate that if bees
consume the majority of their water from puddles or ponds, the exposures relative to dietary
and direct spray are insignificant. The preliminary analysis indicates that if bees drink a
substantial amount of water from guttation fluid or dew, conservative exposures may be
similar to or even exceed pesticide exposures through the diet or direct spray. Further
investigation concluded that pesticide exposures through dew and guttation fluid are not
expected to be as significant when compared to diet, primarily because they are not likely to
consistently drink a substantial amount of water from these sources.
a. Please comment on the strengths and limitations of basing the Tier I exposure method on
contact and diet. Does the Panel agree that for the majority of pesticide applications, the
primary exposure routes for bees will be represented by contact and diet?
64
The Panel generally agrees that diet and direct contact are likely dominant pesticide exposure
pathways. However, the Panel believes that contact with dust generated during planting of
pesticide treated seed and granular formulation applications, may be quantitatively relevant.
These dusts tend to be strongly enriched with pesticides. Bee mortalities during planting of
seeds treated with certain insecticides are widely reported. In addition, the Panel believes that
pesticide exposure via contact and consumption of pesticide contaminated water should be
evaluated. As reported in the white paper, bees consume water to meet physiological needs
and transport water to hives for use in colony thermoregulation. The Panel suggests that risk
assessments would be improved by considering dust and water exposures in Tier 1. One
panelist notes that substances of concern would be identified in the currently proposed Tier I
approach that focuses on diet and contact exposure. Specifically this panelist believes that
consideration of dust exposure and effects as well as potential mitigation measures should be
considered by higher tier testing and or as a risk management measure.
b. Dust: If the Panel believes that this exposure route should be quantitatively included in the
Tier I exposure method, for the relevant application type(s) (i.e., seed treatment), please
discuss the data that may be needed to address the exposure route quantitatively.
The Panel notes that dusts strongly enriched with pesticide active ingredients can be generated
when treated seeds are sown, during application of granular formulations, and by wind erosion of
fine particulate matter, in particular PM10 size range material. The Panel agrees with the white
paper findings that bees may be exposed via contact to pesticides in dust while in flight or when
visiting flowers and other vegetated surfaces where dusts have deposited. Another possible
exposure route discussed is contact of dust deposited directly on hives that are downwind of
agricultural fields. The Panel acknowledges widespread reports of honey bee mortality
associated with dust emissions during planting of pesticide treated seed, and they note that in
many cases deaths due to pesticide exposure were confirmed by detection of pesticide
concentrations above lethal limits in bees. No reports of bee mortalities due to contact with other
dusts including those generated from granular formulation application and in PM10 derived from
agricultural fields were noted. One panelist emphasizes that little is known about pesticide levels
in PM10 and that more research is needed to determine the types and amounts of pesticides that
may be present in PM10 collected in agricultural areas. The Panel notes that a recent doctoral
dissertation indicated that PM10 may be enriched in pesticides by factors of 100 to 1000 when
compared to nearby surface soil (De Rossi, 2010). A second study indicated that that from
1 to 6 % of the herbicides applied to farm fields may be lost in wide blown dust (Larney et al.,
1999).
Regardless of dust source, the Panel recognizes that exposure assessment is challenging noting
that there are many variables and factors in quantifying emissions from planters sowing treated
seed. They are particularly difficult to quantify because many variables and factors are involved
including seed type, seed treatment rate, quality and abrasion potential of coatings, the
machinery used and use and efficacy of deflectors and other mitigation measures. To this end
the Panel advises that there are several publications that provide insight into pesticide emission
rates associated with treated seed planting. For example, the study by Tapparo et al. (2012)
indicated that from 0.5 to 2 % of the pesticide applied may be emitted in planter exhaust from
65
corn seed coated with various commercial insecticide treatments. It is suggested that these data
could be used to estimate exposure as follows using an approach similar that described in the
Question 4b. response. If a 2% loss rate from the maximum application rate reported by Tapparo
et al (1.25 mg of active ingredient seed and 66000 seed ha-1) or 1 kg ha-1 (as done by EPA) is
assumed then computed emission rates would be equivalent to 17 to 200 ng/cm-2. Multiplying
these rates by the reported surface area of an adult honey bee, 2.4 cm-2, (Roberts and Harrison,
1999) assuming complete coverage would provide exposure estimates of 40 to 480 ng/bee.
These values are in the same range as estimated in the white paper for dietary exposure from a
systemic seed treatment (up to 300 ng/bee per day). It was noted that Tapparo et al (2012) also
reported detection of 25 to 1400 ng of the insecticide clothianidin in bees exposed to planter
exhaust when corn seed coated with a commercial formulation of this product was sown. Dust
exposure may also lead to dietary exposure. Krupke et al. (2012) measured clothianidin levels of
up to 88 ppb in bee-collected pollen and most of their measurements were an order of magnitude
higher than levels found in pollen from systemic movement of pesticide. Therefore these levels
are probably resulting from drifting dust and such empirical measurements provide another
means of measuring exposure. Given that dietary and dust exposure estimates are within the
same range it appears that consideration of both exposure pathways in exposure estimates may
be appropriate (Forster et al., 2012).
c. Drinking Water: Please comment on the analyses, discussions provided in Appendix 2 of the
white paper and the conclusion that pesticide exposure to bees through drinking
contaminated water is not expected to be a major route of exposure when compared to
contact (following foliar spray applications) and diet. If the Panel believes that this
exposure route should be quantitatively included in the Tier I exposure method, for the
relevant application type(s) (i.e., foliar spray, soil treatment, seed treatment, or trunk spray),
please discuss why and what data may be needed to address the exposure route
quantitatively.
Honey and other bees may be exposed to pesticides dissolved in contaminated water via direct
consumption and or during contact when worker bees carry water in their honey stomachs to
the hive for use in hive evaporative cooling. Further, since the latter is done by spreading water
onto wax and other surfaces, pesticides not absorbed by the worker bees during water transport
may accumulate in the hive and serve as a source of exposure for the entire colony. The Panel
notes that water exposure assessments in the white paper are limited to estimates of drinking
water consumption, approximately 0.045 mL day-1. The Panel agrees that this volume should be
increased to include other water contact. As noted in the white paper this could increase
volumes used in exposure assessment calculations to between 0.45 and 1.8 mL day-1. The Panel
believes that even when it is assumed that the highest volume is used, and it is assumed that
worker bees absorb 100 % of the pesticide transported in water in honey sacks, potential
exposures when water from contaminated ponds are used as a water source by bees appear small
when compared to dietary or contact exposure described for Tier 1. This is in agreement with
findings described in the white paper. The relatively low exposure rate in this case was linked to
the relatively low estimated pesticide concentration in ponds using the GENEEC (GENeric
Estimated Environmental Concentration) model (US EPA, 2001). In addition, panelists
acknowledge that the model generally provides conservative (high) concentration estimates.
66
In the case of the potential use of puddles in farm fields as bee water sources, the white paper
also indicates potential exposures were likely very small when compared to diet and direct
contact exposure Tier I estimates. Regarding this point, the Panel disagrees as they note that
incorrect units are used in Equation 2-1 found at the top of page 210 in Appendix 2 of the white
paper. The Panel notes that the equation is written correctly, but putting values into the equation
becomes problematic if all parameters are not in proper units. For application in the exercise in
Appendix 2, the Panel recommends the following modified equation:
Here cw is in units of g/L, mai in units of kg ha-1, dw and dsed are in units of m, sed (porosity)
unitless, b in kg m-3, and Kd in L/kg-1. Re-computation of the worst case puddle scenario used
in the white paper (1 lb acre-1application to a puddle 0.013 m deep with equilibrium to a depth of
0.0013 cm in the sediment and a pesticide Kd=0.1) yields a concentration of 8100 g/L-1. The
value reported in the white paper is 5.7 ug/L-1. Using the corrected value in calculations
indicated that worst case exposure via direct water ingestion is in the 0.4 g/bee per day. If total
water exposure is considered and 100% pesticide absorption is assumed then exposure would be
4 to 15 ug/bee/day. This is within the range estimated for direct contact and diet in Tier 1. Thus,
the Panel recommends that water exposure be considered in Tier 1 assessments. Finally one
panelist notes that the Agency may want to consider an alternative approach to computing
pesticide concentrations in puddles that was developed for ECOFRAM simulations (US EPA,
2012).
The Panel agrees that guttation water expressed on leaves of some plants is a potential bee water
source. In addition, the Panel acknowledges that some publications have indicated that pesticide
concentrations in guttation water may be high when some systemic insecticides are applied to
seeds. The summary of some of these data in Table 2-9 (page 215) is noted with a
recommendation that if values are scaled to a 1 lb acre-1 nominal rate that maximum projected
concentrations should not exceed the water solubility of the active ingredients. Many of the
adjusted values in this Table exceed the water solubility of the pesticides identified. The Panel
also suggests that guttation water may not be an important water source for bees since the drops
are usually found in the morning only. In summary, the Panel agrees that the extent to which
bees may be exposed to pesticides in guttation water is unknown.
d.
Other Routes: Please identify and discuss additional exposure routes (if there are any
besides contact with dust and consumption of drinking water) that would contribute significantly
to pesticide exposure of bees and explain how and why such exposures could be considered
quantitatively in establishing the Tier I exposure value.
A described earlier, a possible route of exposure to some non-Apis species is through contact
with soil. Many solitary bees nest in the ground, and some cavity nesting bees use mud to
partition the cells in their nests. The main route of exposure via soil residues, in these cases,
would be topical. Since EPA already has models for estimating pesticide residue concentrations
in soils, exposure estimates via this route appear feasible.
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8.Tier I Effects Assessments. As discussed in the Problem Formulation (Section 2.2.1), the
assessment endpoints for the ecological risk assessment of bees involve maintaining honey bee
population size, stability of managed bees, quality and quantity of hive products, species richness
and abundance. In order to use the results of toxicity studies quantitatively in risk assessment, it
is important to identify specific endpoints which will be measured in toxicity tests as these
measurement endpoints must have clear linkages to assessment endpoints. As indicated in Table
1 of Section 2.2.1, at the individual bee level (which is the focus of the Tier I assessment),
measurement endpoints relevant to these assessment endpoints include: individual survival, adult
bee longevity, brood size, brood success, and queen fecundity. The acute and chronic toxicity
tests with larvae and adults can be used to quantify effects of pesticides on all of these endpoints,
with the exception of queen fecundity (which would require an egg laying study involving the
queen). The focus of the chronic toxicity tests with larvae and adults is on mortality that may
occur during the tests. Potential impacts of a pesticide on brood size and success can be assessed
by determining whether there is decrease in the number of brood (i.e., larvae) following a
chronic exposure of larvae to that pesticide. Potential impacts of a pesticide on adult survival and
longevity can be assessed by determining the mortality and the decrease in the life spans of adult
bees following chronic exposures to the pesticide. The notable limitation to the proposed chronic
toxicity endpoints is that they do not include measures of queen fecundity.
a. Please comment on the extent to which currently available bee toxicity tests, which focus
primarily on mortality/survival, serve as an effective Tier 1 screen.
The Panel believes that the Agencys articulation of the Tier I bioassays in the white paper is
thorough and detailed. The Panel also notes that the incorporation of larval and other bioassays
in the Tier I screening process is a welcomed step. The discussions below are aimed to further
elucidate how social insects such as honey bees introduce some additional considerations for
such screening as a surrogate for all bee pollinators.
These bioassays use the individual as the basal denominator. This does not take into account
subtle variation among individual honey bees. Standardizing to honey bee weight would seem to
make sense, which might perhaps also translate more effectively to other honey bee castes
(queens and drones, which weigh ~1.5x than worker bees) and particularly other bee species,
particularly solitary species which are often quite smaller than honey bee workers.
Moreover, it can be quite misleading to test an obligatory social insect, such as honey bees, in an
individual context. Thus, it is much more biologically relevant to test honey bees in a social
context, ranging from small groups in vitro (see below) to large colonies in vivo (see Tier II).
The Tier I screens on adults as outlined in the white paper (both topical and oral exposure) also
do not capture temporal variation but rather focus on final mortality after a pre-determined
period of time (typically 48-hours, but sometimes extended to 96-hours). Standard survival
analyses would be much more informative, as it would capture not only the percent mortality at
each time point measured, but it would also statistically compare the slopes of the mortality
curves. In doing so, quantifying survival in a social environment in vitro is much more
meaningful than individually for social bees such as honey bees.
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Employing two types of Tier I honey bee cage studies would each be informative in different
ways: one-time application vs. continuous exposure by feeding. The one-time application
bioassay would involve topically treating bee cups with a cohort of marked honey bees in a
caged group (~50 newly emerged adult workers) and monitoring their survival over time until all
focal bees die (which can take many weeks), replacing all dead bees daily with newly emerged
workers to maintain adequate group size (e.g., Evans et al. 2009). The continuous exposure
application would be to similarly monitor a marked cohort of untreated workers in a cage fed
with treated food. Because a one-time dose would not adequately represent bee exposures,
chronic tests would better represent real exposures. Also, chronic tests would better represent
solitary bee larval exposures because the entire food provision for each larva is usually collected
over a relatively short time period (within a day).
Summer and winter honey bees are physiologically different. The timing of the proposed
compound and when honey bees are exposed ought to also take this into consideration.
Finally, we need to be cognizant of genetic differences among populations as well as pay
attention to behavioral (sub-lethal) abnormalities. As no trigger values are established for sublethal effects, the risk assessor needs to have the flexibility to ask for additional data or higher
tier tests when concern is raised on the basis of sub-lethal effects in laboratory. While
recognized insecticidal substances will always cause sub-lethal effects before mortality, some
substances that are not classified as mortally toxic to bees do cause reproducible behavioral
abnormalities. As such, the tiered system needs to allow the flexibility to ask for additional data
and must not serve as a cut-off value approach.
b. Please comment on additional measurement endpoints (e.g., growth) which should be
considered in future modifications of Tier 1 test protocols and which are appropriately
linked to the proposed assessment endpoints. Given that the queen is the reproductive unit of
the colony, please comment on methods to evaluate effects on individual queens, considering
practical limitations of testing with queens.
It would be helpful to include a temporal component to Tier I bioassays, using survival statistics
to quantify slopes as well as final percent mortality (see Question 8a). These measurements
would then extend well beyond the 48-hour or even 7-day measurement period, and measure the
entire lifespan of individual honey bees (often several weeks). While longer in duration, the
Panel believes that the increased information gleaned from such comparisons more than
compensates for their inclusion in such bioassays.
The question specifically asks for recommendations for effects on queens. Due to reports on
queen failure, we need to try to measure effects on queens, even though methods are not fully
developed yet. As no defined methods for evaluation of effects on individual queens are
available, higher tier tests in semi-field and field settings can be used to evaluate the effects on
queen fecundity and also on queen rearing. Effects on queens can be quantified in multiple
ways, including effects of rearing environment on morphology and insemination/mating success.
Quantifying queen reproductive potential at the individual level can be accomplished in multiple
ways (ovariole number, fat bodies, other morphometrics, pheromone production; see Delaney et
al. 2011) and can translate to colony-level phenotype, but they do not serve as exact proxies. It
69
is therefore difficult to distinguish between tiers I and II with respect to reproductives because of
their inherent need of a social-rearing environment. Nonetheless, adding queens to the proposed
bee cup bioassays is possible and simply examine mortality/longevity. Measuring the other
sexual reproductives in a colony, the drones (e.g., sperm viability), is important to help fill a data
gap in the scientific literature. This is an important measure because drones serve a vital role in
the reproductive biology of honey bees.
Quantifying immuno-competence on adults (and larvae) would also be helpful to assess the
possible long-term sub-lethal consequences of exposure, but so little is known about the linkages
of the immune system to colony health at this point to make such inferences very strong.
Other measurements beside survival may be motility, social interactions, and other behavioral
changes. As discussed in Question 8a, sub-lethal behavioral changes at the individual level may
have profound effects on the health and productivity of a honey bee colony colony (e.g., Wu et
al. 2011). Technology that helps to automate the recording of such data would streamline the
logistics of these measurements.
The Proboscis Extension Reflex (PER) and learning is another bioassay and outcome that can be
informative. The Proboscis Extension Reflex is a well-studied and common bioassay for
learning and memory (e.g., Ciarlo et al., 2012), which uses the instinctive reflex of a harnessed
adult worker honey bee sticking out her proboscis when her antenna contacts a droplet of sucrose
solution. This reflex can be conditioned to other stimuli, such as odors or tactile cues, so that
they associate the two. This enables the proboscis extension as a reliable signal of signal
detection and learning. Differential effects of learning, as reported by PER, can distinguish
treated vs. untreated cohorts of workers. PER still needs to be linked to colony life/survival, but
nonetheless could be used to trigger higher tiered tests.
Another potential assay that could be explored for development could be one that tests the effects
of pesticides on queen pheromone production. For example, there is some recent research on
how disease impacts pheromone production (e.g., Alaux et al., 2011). Thus, it seems
conceivable that pesticides may also have an effect on pheromone production.
The viability of sperm within queens could also be a potentially useful measurement. Also, the
fecal samples of queens could be extracted without sacrificing them. Analysis could be
performed on the fecal material that may produce some valuable information.
For in vitro tests, it is presently uncertain if growthas measured by weight of larvaeis a
reliable factor, but it can be measured on the larvae gained by artificial rearing in the in vitro
method of Aupinel. Also, the growth of individual larvae can be assessed in higher tier tests by
weighing individual larvae, e.g. in the Oomen method (which is a somewhat intermediate
between a tiers) or the higher tier test method OECD 75 (Oomen et al., 1992; OECD, 2007). For
OECD 213/214 (oral and contact toxicity) tests in the laboratory, the slope should be provided
(OECD a & b , 1998).
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Tier 1 Larval Toxicity Testing. Section 4.1 of the white paper discusses new data
requirements for the screening-level effects assessment and recommends obtaining and using
larval toxicity data on individual bees. The paper specifically identifies the assay initially
proposed by Aupinel et al. (2007) as one methodology for quantifying acute oral larval
toxicity in the Tier I screen. These assays rely on feeding bees a sugar solution which has
been spiked with the test material; however, this in vitro method of feeding larvae differs
from the process by which the larvae would typically be fed within the colony environment,
i.e. by nurse bees secreting either brood food or royal jelly.
a. Please comment on the extent to which the Aupinel et al. (2007) in-vitro method serves as an
appropriately conservative estimate of Tier 1 acute oral exposure of honey bee larvae to
pesticides, given differences in this test design from actual in-hive exposure conditions (e.g.,
during the first 3 days of the larval development stage larvae consume royal jelly and brood
food) and the uncertainty regarding the extent to which larvae rely exclusively on
pollen/nectar as opposed to royal jelly/brood food.
Determining the toxicity of pesticides on larvae using in vitro testing is complicated due to
several factors including possible genetic differences among colonies and difficulties
synchronizing larval age, both of which were noted by Aupinel et al. (2007) and mentioned in
the white paper. In addition, as yet uncharacterized attributes of royal jelly/brood food, honey
and beebread may be relevant to pesticide tolerance in larvae. Royal jelly, for example contains
substances that inhibit DNA methylation and histone deacetylase activity (Spannhoff et al. 2011)
and promote gene expression. Similarly, honey and beebread contain phytochemicals that
upregulate detoxification genes in worker bees (Johnson et al. 2012). These factors have the
potential of altering responses to pesticides. Without a more complete understanding of how the
composition of food affects toxicity or bioavailability of spiked compounds, conclusively stating
that the method is conservative is difficult, although available information points in that
direction.
One specific concern is that the proposed method for testing larvae is based on pesticide levels in
pollen/nectar administered to 5 day old larvae (p59 of the Agencys white paper). If 5 day old
larvae destined to be queens eat royal jelly, and if royal jelly has 100x lower pesticide levels than
nectar/pollen, then tests conducted in Tier 1 will have maximum concentrations of pesticides
based on worker exposure that are much higher than those experienced by queen larvae. In
terms of toxicity this approach seems reasonable, but if caste determination and viability are
concerns then pesticide amounts may be inappropriate. As noted earlier, the assumption that
royal jelly concentrations are 1/100th those found in other foods is apparently based on only one
published, Davis and Shuel 1988, and one unpublished, Kamel et al. , study.
The impact of larval diet on pesticide detoxification represents a significant data gap. In the
artificial diet used for this bioassay, glucose and fructose serve as proxies for honey; chemically,
however, honey is considerably more than just sugar. Phytochemicals in honey may well
influence pesticide toxicity and metabolism (as they do in other herbivorous insects*) and
interpreting toxicity data in their absence presents a challenge. (Riskallah et al. 1986; Kennedy
et al. 1987; Abd-Elghafar et al. 1990; Robertson et al. 1990; Liang et al. 2007)
71
More generally, the concept of an acute dose for a larva may be biologically difficult to interpret.
Unlike workers, which may experience one-time encounters through pesticide drift outside the
hive larvae are continuously provided with food that for the most part has been processed by
workers, and seem less likely to have such encounters (although they are occasionally fed raw
pollen and by that route could conceivably consume an acute dose). Moreover, because larvae
are confined during their development, they are subject to continuous contact with wax, which if
contaminated is likely to be a source of toxicity not directly assessed by proposed methods.
Contact bioassays using pupae might be optimal for assessing topical toxicity.
The in vitro method is described and some validation testing has been conducted, but it is
currently not validated for the period from pupation to eclosion. As designed, current test
protocols would fail to detect effects of IGR (insect growth regulators) on bee brood that are
manifested post-pupation. Thus, if pesticides to be evaluated are known or suspected to be
growth inhibitors, higher tier tests such as the OECD 75 are needed (OECD, 2007).
The Aupinel test has a high degree of uncertainty associated with variable reproducibility and
some additional limitations. It is expected that further discussions (starting October 2012 in the
context of the OECD proposal for guideline development) will improve the system. There is
also some uncertainty regarding the dosing. For example, there is ambiguity in identifying
ecologically appropriate doses in the absence of unambiguous nectar/pollen data.
b. Please comment on the extent to which pesticides would be more or less bioavailable using
the synthetic matrix relied on for feeding developing bees in this in vitro method.
Bioavailability will be influenced by the nature of the compound, larval metabolism, and food
composition. Without accurate information about how these factors influence bioavailability
within honey bee larvae, it is not possible for the Panel to assess this question. Aupinel et al.
used dimethoate, an organophosphate that is highly water-soluble; it is not clear how pesticides
with different structures and properties will perform in the synthetic matrix.
c. Please comment on the extent to which the absence of trophallaxis (i.e., the transfer of
food/fluids between colony members) may render larvae more or less vulnerable to
pesticides.
The Panel believes that contributions of trophallaxis to pesticide resistance or susceptibility
are, to our knowledge, totally unknown. This lack of knowledge in the research represents a
data chasm.
d. Please comment on alternative methods for testing individual larvae that may be appropriate
for quantitative use in a Tier I screening-level assessment.
Literature reports of alternative methods for testing larvae quantitatively are vanishingly rare.
Atkins and Kallum 1986 treated larvae in a colony by micropipetting pesticides directly into the
cells. (Atkins & Kallum 1986)
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Pupal bioassays have not been widely used for pesticide toxicity, but they have been used in
other contexts (e.g., pathogenicity of fungi). Furthermore, these studies may be productively
employed. Hendriksma et al. (2011) is noteworthy in this regard; this bioassay uses a
nongrafting method to manipulate larvae and uses prepupal weight as a bioassay endpoint to
calculate LD50 values for dimethoate). A few other protocols for testing effects of pesticides on
honey bee larvae are available, (e.g. Wittmann D., 1982). In addition, some methods have been
described for larval testing of Osmia and other bees but these have not yet been validated or ringtested.
Larval transcriptomes and methylomes of honey bees have been described. The existence of
these data provides potential quantitative measures of effects of toxins on larval development
that might be useful as alternative indictors of larval actions/health. Genetic resources may
allow use of gene expression, detoxification and/or antioxidant enzyme activities, senescence
traits (vitellogenin) as biomarkers. Johnson et al. 2009 suggested the use of ribosomal RNA
fragments as a biomarker. Such methods, however, would need validation before they could be
used in Tier 1 screening.
e. Typically acute toxicity tests are concluded between 48 96 hrs. Please comment on the
appropriate duration of toxicity tests for assessing acute toxicity to individual larval and
adult bees.
There are problems interpreting larval survival over a 2 to 4 day period as a metric of toxicity.
The four-day endpoint represents 80% of the period of active feeding, so distinguishing between
acute and chronic becomes difficult. Some agents may induce toxicity due to delayed larval
development, which would be overlooked in the proposed approach.
In general, a biological transition, such as pupation, provides a more reliable, consistent, and
interpretable endpoint. Furthermore, the endpoints-time to pupation, pupation rate, and pupal
weight are more biologically meaningful, and different castes (queens and drone)s can be
assessed separately. Such tests, however, have not yet been vetted thoroughly. Assessing acute
toxicity over seven days for the present time will allow EPA to harmonize international efforts at
the OECD level until a satisfactory standard pupation assay has been developed but developing
such a test should be a priority. Among other things, such assays will be more sensitive to
pesticide impacts on growth rate and development (e.g., IGRs).
Currently, the Aupinel method describes both single dosing vs. repeated dosing of the substance.
The latter (dosing of the food every day) seems to be the most realistic, but there may be a need
for two toxicity standards. This is because there may be substances that are acutely toxic to
young larvae (uncapped brood) and some that only affect later brood stages (capped brood, e.g.
fenoxycarb; Aupinel et al., 2007). More effort should be focused on establishing a validated,
and reliable method that also covers the time from pupation to eclosion.
10. Tier 1 Chronic Toxicity Testing Bees. Section 4.1.2 of the white paper discusses the status
of chronic toxicity tests with individual adult and larval bees. At this time, no formal
guidelines have been developed for conducting chronic toxicity tests with either adult or
larval bees, although studies with individual bees of various ages are routinely reported in
open literature.
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a. Please comment on the conclusion that adequate procedures have not been sufficiently
developed and validated for assessing chronic toxicity to individual bees in a risk assessment
context.
The concept of the individual adult bee presents a challenge for assessing toxicity in Apis
mellifera because of the importance of the social context. Age-related polyethism over time is
circumvented in the absence of a social context and foragers are hard to keep alive individually.
However, exposing emerging workers for ten days at low dose with known ages of bees has been
attempted according to OECD 213 with some success (OECD, 1998). Chronic tests in the
laboratory can be conducted by using the protocols of OECD 213 (with small adjustments, e.g.,
using freshly emerged bees). Caged brood tests or broodless bee cup tests may be employed
productively in this context.
b.
Please comment on the potential use of the 10-d adult worker and 7-day in vitro larval
toxicity tests discussed in the white paper for assessing chronic toxicity once these methods
are fully vetted.
The optimal design for a larval in vitro test would be one encompassing the entire active feeding
period through pupation, with time to pupation, pupal weight and percent pupation as
quantifiable and interpretable measures of pesticide impact (As demonstrated by Hendriksma et
al. 2011, with prepupal weight and survival to prepupation as assay endpoints. Such a test can
provide data on both acute and delayed responses). Obviously however, such testing would
require vetting. With respect to adults, use of a 10-day viability test for adult bees has the virtue
of allowing for harmonization with ongoing efforts in Europe.
c.
Although 10-day adult and 7-day larval toxicity tests have been proposed, please comment
on whether alternative durations of pesticide exposure may be more appropriate for
determining chronic toxicity for adult and larval bees at a Tier I screen.
A ten-day test of adult survival can be informative, but interpreting the biological meaning
outside the social context presents a challenge. Rather than an alternative duration of exposure,
an alternative design should be considered. Survival could be assessed in the social context with
the use of caged brood or broodless bee cups (although not a standard methodology), which have
been used with success. As for larval toxicity tests, as stated earlier, extending the test duration
through pupation rather than terminating it at an arbitrary interval would be most appropriate.
d.
The white paper identifies NOAEC No observable effect effective concentration as the
chronic toxicity measurement endpoint. Please comment on the possible use of ECx values
as a measure of chronic toxicity for use in RQ calculations.
The proposed regression-based method for calculating ECx levels seems feasible if a sufficient
number of concentrations can be tested to allow for confident estimates (confidence levels drop
at low and high ends of dose-response curves). Including the temporal component of chronic
effects provides a more quantitative method for estimating effective concentrations causing
74
chronic effects (e.g., survivorship curves). Unique attributes of bees favor anything that works
well with small sample size and high variability.
NOAEC values may depend on selection of endpoints and appropriate concentrations for assay.
Both NOAEC and ECx values should be provided wherever possible. There are some
uncertainties and difficulties with linking the outcomes for both methods with the protection
goals, but they are still useful for triggering higher tier tests. The European Food Safety
Authority opinion (EFSA, 2012) may have useful suggestions as to how chronic tests can inform
risk assessment.
e.
Please provide comments on what percent effect would be considered a relevant measure
of chronic toxicity for individual bees given the potential compensatory effects which honey
bee colonies may exhibit relative to the effects of pesticides.
Compensatory effects are a societal phenomena that are better suited for Tier II assessment.
Recruitment of precocious foragers provides a short-term solution to colony needs but may exact
long-term costs on colony health. Khoury et al. 2011 estimates that reduction in worker
longevity by 2.8 days corresponds to a loss of 0.35 bees per day. Incorporating a time
component may be useful.
Thus, EC20 (20% difference between controls and experiment to trigger concern) may be a
conservative point to set, given that, according to the one model available (Khoury et al. 2011),
loss of 30% or more foragers daily triggers the death spiral (losses at that level are
irrecoverable). Additional modeling can be useful here, inasmuch as this estimate is not based
on an abundance of empirical data. Timing of loss would matter, too (losses are more
sustainable in the fall season. Thus, the EC20 may vary depending on the season).
f.
Although the white paper identifies some measurement endpoints for assessing chronic
toxicity to individual bees (e.g., survival), please comment on other endpoints to consider in
chronic toxicity studies which the Panel believes are important and the associated study
design elements.
As mentioned in the response to Question 8, other endpoints to consider in chronic toxicity tests
include behavioral impacts (e.g., learning assays, automated recording of motility and behavioral
interactions). Future endpoints could include gene expression relevant to detoxification and/or
antioxidant status, immunocompetence, and senescence (e.g., vitellogenin). Johnson et al.
(2009) suggested the use of ribosomal RNA fragments as a biomarker. Such surrogate
biomarkers (an approach widely used in human risk assessment) need to be validated for bees.
g. Section 4.1.3 4.1.2.1.2. of the white paper discusses the uncertainties associated with
developing risk assessments based on studies of sublethal effects when sufficient linkages
have not been developed to understand how the sublethal endpoints may be quantitatively
related to typical assessment endpoints (i.e., growth, impaired survival, and reproduction) at
the whole colony level. Please comment on the proposal to use data on sublethal endpoints to
qualitatively (i.e., no Risk Quotient is derived) characterize effects and risk until sufficient
75
linkages between these endpoints and the defined assessment endpoints have been developed
(e.g., Adverse Outcome Pathways).
The social environment complicates the process of identifying reliable, reproducible and relevant
sublethal endpoints. Given these complexities, the use of sublethal endpoints is conservative and
important for providing insight into super-organism responses. They are also critical triggers for
signaling a need for moving to Tier II.
A high priority for future research includes the development of assessments for neurotoxicity
symptoms; although direct links to colony health may not yet be fully understood, they are
indicative of biological activity of chemicals. The results of these types of studies can
demonstrate a need for additional quantitative tests at Tier II. Eventually, links must be made.
Proboscis extension reflex, albeit a high throughput assay for behavior, measures appetitive
learning but many other forms of learning are essential to colony health and few measures exist
for documenting impacts on those forms of learning.
11.Tier II Semi-field Effects Assessments (Whole Colony). For Tier II assessments, Section
4.2 of the white paper identifies two types of test methods that may be used to assess colonylevel effects, i.e., semi-field tunnel tests [OECD 75; EPPO 170]; and semi-field feeding studies
(OECD 2007; EPPO, 2001). These studies are intended to help characterize risks identified in
the Tier I level assessment that are based on exposures and toxicity data for individual bees and
quantified using Risk Quotients.
a.
Although colonies are typically confined to enclosures for Tier II studies and these
enclosures can limit the environmental realism of the study conditions, tunnel studies
provide an opportunity to collect colony-level effects and potentially exposure information.
Please comment on the relative strengths (e.g., foraging activity by adult worker bees is
limited to treated crop; trophyllaxis enabled) and limitations (e.g., limited study duration,
smaller colony sizes, reduced forage area) of these methods.
Simple LD50 measurements of topical toxicity to a solitary adult worker honey bee do not
adequately capture the myriad outcomes of exposure for social insects. This is because there
are other deleterious sub-lethal effects beyond simple adult mortality due to exposure. Thus
while quantifying contact toxicity by contact and ingestion is an important dimension to
quantify, it is only one side of a multi-faceted problem. This is a fundamental issue that faces
the Panel. Because honey bees are social insects and function like super-organisms, the colony
is the basal unit to test toxicity. As such, in vitro approaches are limited because they do not
test at that higher level of biological organization. The analogy for mammalian systems, for
example, is to screen compounds on tissue cultures and assume an LD50 on the whole animal
from cellular information. While informative, it does not adequately capture the entire
biological reality of the system in question. Employing the additional bioassays discussed in
Question 8 would help bridge this gap and serve as effective screens, but they will still not
fully serve as an adequate proxy for testing colony-level effects.
Strengths of the proposed Tier II studies in the white paper are that the effects are measured in
vivo, rather than extrapolated to a complex environment from a simplistic in vitro bioassay.
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Because of the additional level of biological complexity, the Tier II level for a super-organism
is the basal level in which to properly quantify LD50 estimates.
Limitations to this approach are increased among-colony variation, which requires high
samples sizes to detect weak but biologically relevant effects, as well as ability to standardize
across different trials. Because it is difficult to acquire a sufficient sample size due to the
inherent variability between colonies, there are increased risks of Type II errors (false
negatives) with high-tiered tests. Modeling may help facilitate data collection and analysis.
The Panel also notes that that honey bees can also buffer potential effects because of their
sociality. Consequently, this may obfuscate effects that may be important for solitary bees.
The semi-field design is a worst-case enclosure appropriate for determination of acute effects
on bees. The exposure is maximized in the tunnels/tents as bees are confined to the treated
area; where dose responses (by application of different field rates) and mitigation measures
(e.g., application after bee flight instead of application during full bee flight activity) can be
tested. Thus, with semi-field tests a very high degree of certainty is observed. One further
limitation is that some colonies respond with a reduction of the breeding/larval rearing activity,
making interpretation of effects on colonies under real conditions more difficult. For
addressing the individual larvae, the OECD 75 may be used (OECD, 2007).
Standardizing by weights of individual bees, as well as for colony size, will be helpful to
standardize across colonies, studies, and other systems. In doing so, there is a need to
determine linear vs. non-linear effects based on exposure concentration.
Also bumble bees can be used in Tier II studies, particularly for caged designs. The possibility
of using Bombus as a model system to test social effects may be more effective in some ways
because they are amenable to field-realistic foraging behavior in confined spaces. It would be
helpful to test both Apis and Bombus, but if Bombus is used for semi-field analyses it would
help translate between them. While both may be utilized, Apis may be more amenable to
feeding experimental designs, whereas Bombus may be more amenable to cage designs.
It is a general question as to how feeding methods fit into Tier II tests. For example, the
Oomen test is regarded as an intermediate between Tier I and Tier II, but in general the feeding
tests are not acceptable as Tier II tests especially under free flying conditions (Oomen et al.,
1992). In the case of a combination of a feeding method with colonies free-flying, a minority
of the panel members believe that the studies should be rejected and not considered as valid as
the exposure cannot be quantified. Exposure can only be quantified and assessed if these tests
are conducted in semi-field conditions in closed tunnels; the bees must not have access to other
uncontaminated food sources. Other panel members, however, feel that while precise exposure
levels cannot be obtained, they can still be estimated and quantified (amount of food consumed
over time, quantifying alternative foraging activity) and therefore have some utility.
Enclosures limit the time a test can be run because it is very difficult to provide sufficient
bloom resources (pollen and nectar from flowers) in an enclosure. Thus, enclosures might not
adequately represent field exposure levels (if exposures are based on residues on treated crops
within the enclosure), thus a better method might be free-flying but fed pesticides.
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Feeding with spiked food should only be used to extend exposure where necessary, and it is not
possible to do a design with extended flowering of the realistic crop (e.g., if there is concern
for chronic long-term exposure). For some crops (e.g., maize), it may be possible to extend the
duration of exposure also by planting crops at different time intervals, but for other crops (e.g.,
winter oilseed rape) this may not be possible. In these cases, the treated crop of concern should
be used for realistic exposure during flowering and thereafter could be extended with feeding
both nectar/sugar solution and pollen/pollen patties enriched with field realistic concentrations.
In all feeding studies, it should be kept in mind that only both contaminated nectar and
contaminated pollen are fed. Exceptions in terms of using only spiked nectar/sugar solution or
spiked pollen are only acceptable if a special use of a special crop is investigated (e.g., maize,
which only supplies pollen).
b.
Please comment on any other types of colony-level studies that should be considered as
part of Tier II.
Alternative study designs that may be further explored include observation hives to record
behavior and estimate interactions. This directly addresses questions about sub-lethal behavioral
effects outlined in Question 8a. Moreover, it would be very straight forward and highly
informative to rear queens and drones and to see the effects on reproductives. This could be
done in either semi-field experimental designs (enclosed flight cage of free-flying colonies fed
supplementally). Finally, the Panel believes that there may be in vitro, whole mini-colony tests
that could be implemented in the short term that blur the lines between tiers I and II. For
example, Tier I tests of bee cups each containing a queen could be verified with Tier II tests of
baby nuc colonies housed in incubators. While still in vitro, such colonies would contain
queens, brood, comb, and other full-colony phenotypes that could be measured.
With all tests that include artificial feeding, as an intermediate test between Tier I and Tier II, the
Oomen Test can be used (Oomen et al., 1992). Limitations are identified so the original method
should be optimized to ensure exposure (e.g., the feeding period should be extended to feeding
contaminated sugar solution not only on one day but for more than 9 days). Also, this method
has some pros and cons, some of which are also described in the EFSA opinion (EFSA, 2012).
For other feeding methods, there are no guidelines available. Historically, only the Oomen
method has been used.
Some special study designs can be used for investigation of special effects or exposure routes.
Examples include studies to assess the effect of a pesticide on queen rearing, (e.g. a shook
swarm) or swarm box method of queen rearing, exposure via the crop and observation of the
number of reared queens and rearing success of hatched queens. This may be an important area
of risk assessment since studies have shown that queens are highly sensitive to some pesticides
during development and beekeepers report anecdotally that queen longevity appears to be
reduced in the past decade or so.
Another example is investigating the potential effects of guttation. In semi-field studies,
controlled conditions in tents offer the possibility to simulate water collection from guttation
droplets and other water sources. Clean water sources can be excluded to ensure maximum
exposure. The effects on foragers and hive bees and different brood stages can be measured in
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worst-case exposure scenarios. Nevertheless, it is pointed out that semi-field studies may have a
limited potential for extrapolation of the findings to field conditions.
c.
Please comment on the most important endpoints that should be measured in the Tier II
studies (e.g., adult forage bee mortality, brood development, queen fecundity, overall
colony strength) that are linked to assessment endpoints and their associated protection
goals.
Measuring different colony phenotypes is important. Calculating change in each, as well as

using Principle Component Analyses (PCA) for generating a composite variable, would be most
effective. Measuring queen and drone viability would also be helpful.
The Panel also sees a need to verify foraging behavior on the crop to quantify exposure rates of
the foragers. In other words, there needs to be a documented association between foraging
activity and colony phenotype.
Tunnel studies can vary by experimental design depending on the expected exposure route, either
with the target crop in the tunnel or not. Using a crop results in uncertainties about dose, but
panel members disagree about their relative utility. If the exposure is expected to be primarily
through pollen collected by bees, then a spiked pollen patty is appropriate. If it is expected to be
through contact with the crop, having a treated target crop is appropriate. Spiked syrup can be
used if there is concern for exposure to systemics via nectar.
Tunnels should be air conditioned and sufficiently large to keep the maximum temperature at
85F or less. It works best if the nuclear hives (nucs) are moved in with mostly bees that had not
foraged. A water source such as a tray with gravel and water should be provided.
For all tests with bee colonies, the behavior at the hive entrance as well as the behavior of bees
which are foraging on crop should be assessed. There is a need to sample and process returning
foragers to see what they are foraging on.
Queen fecundity may best be addressed by the assessment of the amount of brood in the hives at
certain intervals, the effects on larval development and successful brood rearing with the OECD
75 method, using maps or digital imaging of the brood (OECD, 2007).
d. Section 4.2.2 of the white paper discusses a full-field feeding design. This methodology is
discussed under Tier II assessments since the colony is relatively confined to foraging on
either spiked sucrose solutions or spikes pollen. The intent of this methodology is to ensure
that colonies are exposed to known residue levels over longer durations than the semi-field
tunnel study designs. A limitation to the study is that bees may simply store spiked food
rather than consume it and that the reliance on a single source of food may introduce
confounding effects (e.g., nutritional deficits) into the study. Please comment on the
environmental realism and utility of full-field feeding studies as a line of evidence in
characterizing risk to honey bee colonies.
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Direct feeding is helpful, as it gauges known consumption. However, it detracts from realistic
field effects and contains inherent aspects that are not altogether meaningful. It may be more
helpful to sample incoming foragers, processing pollen and nectar loads from each in order to
determine the variation and degree of exposure. It is also necessary to control for the amount
consumed.
With increased variation, which is always the case with colony-level phenotype in an
ecological setting, replication and large sample size is paramount. Forced feeding eliminates
the natural foraging behaviors, including colony communications and avoidance behaviors.
Twenty-eight days may not be long enough to detect certain sub-lethal effects. Two brood
cycles (42 days) would quantify not only affected foragers but also the bees raised in the
controlled environment. Even if left in tunnels for a shorter period of time, extending
observations afterwards seems critical.
With the proposed feeding tests, an underestimation of exposure is possible or even very likely.
Free flying is not considered appropriate by some panel members as additional uncontaminated
nectar and pollen will be foraged, thus there is no worst case exposure. Feeding in enclosed
semi-fields is considered adequate but feeding studies should be designed carefully to ensure
that no underestimation of exposure is possible.
Full-field feeding studies are not considered appropriate for risk assessment purposes. At best,
they can be used as supplemental information of limited value as they are not environmentally
realistic.
In general, it is recommended the methods as described in OECD 75 and EPPO 170 be used
for Tier II and Tier III studies (OECD, 2007; EPPO, 2007). As there may be effects by contact
and/or oral exposure, the majority of the Panel feels that these study designs are appropriate to
test the exposure to both pathways and the combination of both as it may occur in realistic
conditions.
If carefully designed, feeding studies in general only cover oral but not contact concerns (see
above).
e. As discussed in Section 4.3.4 of the white paper, it is important to consider the biological
significance of a measured effect in addition to its statistical significance. Please comment
on the nature and magnitude of effects that would be sufficient to conclude biologically
significant effects on the colony and/or the need to transition to Tier III assessments.
Power analyses would be informative on this point. If sample size is small, a power analysis
would indicate the biological significance of the results. Replication and meta-analysis would
do the same. Effects on fertility should trigger Tier III testing, or the ratio of mortality to
reproductive potential (small effects on reproduction are more important if coupled with a high
bee mortality from toxicity).
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Ground-truthing with transect walks of foraging bees would quantify, at least to a certain
extent, the foraging capacity at the target crop. Sampling returning foragers would also be very
informative, although they would require greater inputs to obtain those data.
The Panel notes that the step-wise process that assumes a low risk in vitro immediately equates
with a low risk in vivo. Because of unforeseen synergistic interactions, sequestration, and
concentration, Tier II and III studies should be performed regardless as determined by the risk
assessor, but the degree and sample size may vary depending on the findings at lower tiers and
the likelihood of pollinators encountering the pesticide in its application.
Combining all similar studies in a common database would facilitate further inferences by
quantifying expected colony phenotypes.
Single metrics can be misleading in their independent importance (e.g., worker mortality in
absence of an understanding that workforce strength is the ongoing demographic process
involving the ratio of death to eclosion). Nonetheless, the Panel has attempted to prioritize the
list of potential measurement outcomes listed in the white paper on pages 132-133 (see Table
A) as a means to orient risk assessors towards more-informative measurements that have
greater penetration (i.e., they likely measure a stronger biological signal in the system).
Table A. Prioritized potential measurement outcomes
Relative utility for
Ecological
Colony measures
Individual measures
measuring risk
measures
Mortality in the
Colony strength
Pesticide residues
crop
Mortality at the
Weight of the hive
Longevity
hive
Mortality of
Food stores
Behavioral
drones and
abnormalities
pupae
Foraging activity Presence of the same
in the crop
queen
Higher
Returning
Ability to requeen
utility
foragers
Levels of disease
Lower utility
Over-wintering success
It should be noted that colony strength is a general term and is a non-empirical composite of
many inter-correlated factors (e.g., adult worker population, brood area). Ideally, many of these
measurements can be made and then compared using Principle Component Analysis to relate
overall colony phenotype (i.e., colony strength). The potential endpoints listed are useful and
appropriate to look for potential adverse effects at the colony level. The endpoint listed as the
returning of foraging bees should be listed as colony foraging activity measured as bees
returning / 3 minute period. Also, weight of hive should be listed as change in colony
weight. Lastly, a measure of the consistency of the brood pattern can be made by counting
the number of open cells in several (3-4) 100 cell areas across 3-4 frames containing sealed
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brood. Poor brood patterns, while perhaps not indicative of pesticide exposure, have been linked
to poor colony performance and or increased likelihood of colony mortality.
Expert judgment is needed to interpret the statistics with respect to biological significance.
Depending on the statistical power and certainty needed, statistics are possible but need very
careful understanding. Absence or presence of statistical significance is not an indication of no
effects or acceptable effects or respectively of adverse effects. The different endpoints may have
different statistical value for the interpretation.
12. Tier III Effects Assessments. Section 4.3 of the white paper discusses the proposed risk
assessment process in Tier III that relies on assessing effects at the colony level where
colonies are not confined (i.e., full field) and exposure is intended to represent
environmentally realistic conditions. As discussed in the white paper, interpretation of the
biological significance of colony-level effects can be challenging, regardless of their
statistical significance. Conversely, high variability in field studies can limit the statistical
power of the study to detect treatment effects. The paper identifies uncertainties associated
with the extent to which bees forage on the treated crop, the size of treatment site, controlling
for alternative forage/pesticide use area, and ensuring suitable controls; these factors combine
to render these studies highly resource intensive.
a. Please comment on the strengths and limitations of full field studies described in the white
paper.
Tier III studies should be designed to provide real world exposures and integrate their potential
effects at the colony level. However, these studies have many potential pitfalls with regard to
their ability to carry out a controlled experiment in the open environment with adequate controls.
Such tests are already widely used in the EU. When properly executed, Tier III studies are the
best means to assess the risks and or impacts of pesticides to Apis mellifera colonies and other
managed pollinators e.g. Bombus or Osmia. In the context of the regulatory framework Tier III
studies are considered highly refined studies meant to address specific concerns raised in lower
tier studies. Thus, each study will vary depending on their measured endpoints to address
specific concerns raised in Tier I or II testing. There are many strengths and weaknesses in
doing Tier III testing. The Panel identifies them below:
Tier III study strengths:
The natural exposure that can be achieved by allowing bees to forage freely on a treated crop,
giving the test more relevance to real-world situations.
The measurement of endpoints to test for effects at the colony level that are unattainable at the
Tier I and II level testing.
The exposure achieved can accurately simulate the actual use of the pesticide.
Tier III tests allow for colony level testing of protection goals. The use of full size colonies
will provide information on colony development, multiple exposure routes and additional,
non-pesticide related stressors, such as factors and endpoints which can only be assessed to a
limited extent in tier II tests.
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If significant effects are noted at the colony level then the results can be interpreted with a
high level of confidence as the colony has many buffering mechanisms such as a reserve
worker force, ability to compensate or replace dead or impaired worker bees etc.
The use of surrogate crops such as Phacelia is possible to help increase foraging on the crop
and thus exposure.
Tier III study weaknesses:
Increased variability among colonies, and thus there is a significant need for replication and
large sample size.
Study site selection is critical as competing crops or vegetation can result in low to no
exposure to the target crop, especially if the plot size is limited or the crop is marginally
attractive.
Plot size will vary with the less attractive crops needing larger plots to insure adequate
foraging and thus exposure to the target crop.
Bees will forage on the most attractive plant within flight range and this can lead to
inadequate exposure and high variability in results.
Pests may need to be controlled in the control plots, and thus may need to receive pesticides
that could compound effects of the pesticide being tested. Positive control plots can be
expensive, and thus people will want to avoid them.
Studies with sufficient levels of replication to provide appropriate sample power in varying
climatic regimes and eco-regions where target crops are produced may be very costly.
In regard to evaluating the potential interactions of multiple pesticides, complete exclusion of
this evaluation runs counter to the goal of Tier III assessments being real-world and
biologically relevant. While it would be infeasible to test such interactions in a pairwise
matrix, using known and commonly exposed pesticides as a background environment seems
paramount.
Consolidating data into a common database with repeated meta-analysis would help in
evaluating varied information. Making these data public would help transparency and
reassurance.
b. Please comment on the proposed modifications to the field study design elements presented
in Section 4.3.2 of the white paper.
One of the concerns raised by the Panel regarding Tier III study design is a lack of control
regarding bee foraging. This leads to uncertainty regarding pesticide exposure. This lack of
control is implicit in a field study. However, there may be ways to estimate the foraging
activity and further ways to reduce the concerns regarding estimation of pesticide exposure. For
example, as illustrated by EPA during the public meeting the maximum foraging radius for a
honey bee is 5 mi. If a field study had plot sizes of greater than or equal to the 78.5 mi2 area of
this circle the probability of bee foraging on treated crops would be 100%. Furthermore, the
pesticide exposure can be quantified by analyzing a relatively small number of samples of
foraging bees over the duration of the study. Of course, this size field plot is impractical and
virtually impossible to implement in a field study. However, this does represent one end
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where
is the expected use by bees for the annulus surrounding the field plot with radius
extending from z to F,
represents the attractiveness (both quality and density of forage)
over area of the annulus with minimum radius z and maximum radius F about the origin.
Finally, assuming bees can fly anywhere inside the maximum circle with radius F, the
probability of plot usage, A, can be quantified through the equation:
If one assumes that uncertainty in the exposure term is inversely proportional to A, strategy for
foraging bee sampling to quantify pesticide residues can be designed appropriately (e.g.,
frequency of sampling increases as A decreases).
It should be noted that one assumption of this exercise is the relationship used to describe bee
foraging. The sensitivity of this assumption can be assessed by changing the form of the
relationship (e.g., exponential, linear, logarithmic) or changing the type of exponential (e.g.,
,
).
Regardless of how risk assessment accounts for differences in foraging area, incident data
show that carefully designed Tier III studies are well suited to assess the risk and thereby
protect managed bee colonies. In the EPPO guideline 170, minimum values for the number of
foraging bees are described to ensure that sufficient exposure is achieved (EPPO, 2001). As
described in the guideline, the minimum number of colonies should be 4 per test site,
depending on the available forage. For increased test field size, larger numbers of colonies are
appropriate.
The Panel also notes the following about Tier III assessments:
The Panel agrees that plot location is a critical consideration, and competing vegetation is an
important factor to ensure exposure to the target crop. Plot size will be affected by this, with
less-attractive crops needing larger plots to insure adequate foraging and thus exposure to the
target crop. As such, we believe that study site selection is perhaps the single most important
element followed closely by determination of adequate plot size.
Distance between control and treated plots should be a minimum of 4-6 km but increasing this
distance must be balanced against having plots in different microclimatic conditions as the
distance between plots increases.
Testing of formulations at highest label rate is valid, as this provides a worst case scenario
for a given pesticide. In doing so, the exposure achieved can accurately simulate the actual
use of the pesticide. However, limited plot size results in a less than worse case test scenario;
it is not until the pesticide is in actual use that large acreages may be sprayed and the full
extent of exposure and potential effects can be fully evaluated.
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The Panel agrees that balancing or equalizing bee colonies is an important step to be taken in
advance of placing hives on study sites; otherwise, colony variation is too great to see
differences in colony growth and other measured endpoints. The Panel concurs that opening
of hives can result in increased disturbance and the possible introduction of variation within
the results (e.g., increased queen loss) but this should not prevent the inspections needed to
collect endpoint measurements. Good beekeeping methods can alleviate this concern, which
can be readily accomplished by utilizing skilled and experienced beekeepers.
Power analysis is a useful tool to determine the number of colonies needed to produce
statistically significant results. However, the number of colonies needed may not be feasible
due to cost constraints but can be offset by good endpoint measurements and observations on
changes that are considered biologically significant (adult bee mortality) but may be
statistically not significant due to small sample size.
The Panel concurs that the duration of a field trial can be variable and will be dictated by the
endpoints of interest.
One addition to the traditional field study would be the addition of Bombus or Osmia to the field
as they fly shorter distances and thus the level of exposure can be greater or more controlled and
also the colony sizes are smaller and solitary females will be tested under field conditions.
Additionally, studies (e.g., Whitehorn et al. 2012) have shown that reproduction can be impacted
with sub-lethal exposure at field-realistic exposure levels making these solitary or smaller social
colonies more sensitive to pesticide exposure. The use of these additional bee species in a Tier
III study would not add significantly to the costs and they overcome some of the problems
associated with the long flight range of honey bees.
c. Please comment on factors that should be considered in evaluating the biological
significance of effects measured in full-field studies in relation to the proposed assessment
endpoints and related protection goals.
All the weight of evidence achieved in the different tiers including information on acute
mortality of adults and larvae as well as colony development, behavior and behavior need to be
taken into account.
Colony growth patterns, as measured by brood production and or adult bee population, are robust
measures of colony health and directly related to the protection goals.
Similarly, colony mortality would be a biologically adverse effect, but direct colony mortality is
unlikely to be detected because of other factors, and thus a consideration of other endpoints and
their relative importance is warranted.
Effects on queen survival or replacement would be of biological significance and have
implications for colony survival that may not be accounted for if test duration is only a few
weeks or months.
Similarly, overwintering success is the ultimate endpoint, but the more temporally removed the
exposure period is from the winter period the more likely that confounding factors (e.g., parasites
and pathogens, foraging conditions) will come into play making interpretation of results difficult.
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Adult mortality is a good biological indicator as are foraging rates and adult bee longevity; each
of these can be good indicators of adverse effects but the effects could be transitory in nature,
and thus extrapolation to colony-level impacts are not necessarily direct. Taken together any
effects noted in the above endpoints could be used in the risk assessment decision making even if
each endpoint alone was not significant. Colonies are complex super-organisms and thus several
endpoint measures may be a more appropriate than relying on any one endpoint alone.
Disease and pests levels, worker longevity, foraging rates and most other endpoints measured at
the colony level are less robust than those listed above and should be considered as contributing
to a measure of colony success but may not be of biological significance by themselves in
relation to protection goals. Adverse effects noted in these less robust endpoint measures should
be taken into consideration with earlier results from Tier I and II testing.
As long as the plots are not small, one could sample bee diversity (in addition to honey bee
measures). A simple method is colored bowl traps traps, where yellow or blue bowls are filled
with water and soap, then placed in the field for a pre-determined duration to trap bees (e.g.,
Tuell et al., 2009).
d.
Please comment on factors and methods that should be considered when extrapolating
observed effects at the colony level in semi-field and field studies to those expected to occur
in the environment (e.g., spatial and temporal scale of exposure, hive management
practices, presence of multiple chemical and non-chemical stressors, etc).
Tier II and III studies cannot incorporate all seasonal and colony management practices that
could change the response of colonies to pesticide exposure. If testing is conducted in the
normal growing season then an adequate level of confidence can be obtained with the results
generated. As has been stated earlier, colonies used in either field or semi-field studies must be
uniform in strength and as disease and pest free as possible at the start of the study.
The seasonal nature of colony growth and the importance of colony preparation for winter (extra
stores of honey and pollen and the production of winter bees) should be taken into consideration
when interpreting colony level results. If crops of interest are to be grown primarily in the late
summer then tests should be run in this season to make them relevant to the real world.
The longer a Tier III study continues the more likely that outside variables (e.g., pests and
disease, other contamination of hive products) can influence the results. These outside
influences can be minimized by moving the colonies to a remote common area, away from urban
and agricultural settings.
If a crop is major and broadly planted then, the best field test may still not simulate the level of
exposure bees may receive once the pesticide is in wide use (e.g. corn or soybeans in the
Midwest).
Other agrochemicals need for successful crop production need to be selected carefully since
synergism and or antagonism are concerns that may confound results.
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e.
A number of study design elements are discussed in Section 4.3.5 of the white paper;
however, even in the best designed studies, there can be confounding effects which can
limit the utility of these studies in risk assessment. Please comment on factors that should
be considered in determining the utility of field studies for pesticide risk assessment,
including a discussion of the representativeness of a study for a National Level assessment
(i.e., the pesticide may be used anywhere in the United States and its territories).
The design elements of plot size, and plot separation as stated above are critical. However, the
measure of exposure to identify incoming pollen during the exposure period is critical to
ensuring the studys validity. This is the single measure that gives the highest level of
confidence that exposure occurred and, residue analysis of the pollen can address this issue.
The ideal test would use the formulated product on the crop of interest that has the highest level
of attraction to bees and is most widely planted. This is because the formula might affect
residue levels and attraction to the bees (in addition to possible toxic effects that the formulation
might pose). A past example was a microencapsulated pesticide that bees tended to collect like
pollen, increasing their exposure over what was anticipated. If visitation to the crop is confirmed
and no adverse effects are noted, then use of the product could be assumed safe with a reasonable
degree of confidence.
If the pesticide is to be used on a widely planted and common crop in the US, then testing should
be representative of the environments in which the crop is normally grown (i.e. tested in several
different geographic regions). Additionally, climate change is a continuing concern for study
design and implementation. This includes changes that may impact regional cropping practices,
pests, yields, etc. Climate extremes (e.g., heat, cold, storms) may also have major biological
impacts and make study interpretation difficult. These factors are especially important for nonApis species. A risk assessment that is adequate and representative of different environments
and climatic zones may be best achieved by conducting repetitive studies in different
environments and climate zones.
Also the plot size should be large. The larger the plot size, the fewer issues one has to deal with
when interpreting the results (i.e., determining whether the bees are visiting adjacent fields or
wild areas instead of the treated crop, and if the bees are running out for forage in the treated
field). One Panel member recommends a field plot size of 40 acres. In addition the design could
entail having several hives used in each field. Replicate fields for each treatment are needed.
However, if several hives are used per field, then fewer replicate fields would be needed than if
only one hive was used per field.
The Panel recommended as a good rule of thumb that the maximum number of bees in a field
trial is 30,000 adult females per acre. This recommendation is based on the alfalfa leafcutting
bee in blooming alfalfa (honey bees are larger, so should not exceed this number). 30,000 bees is
one moderately sized honey bee colony.
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13. Risk Estimation. Sections 2 (Proposed Risk Assessment Process) and 5 (Risk
Characterization) of the white paper indicate that the proposed risk assessment process is
intended to be tiered and iterative. As part of the Tier I screen, a number of iterations can be
conducted on exposure estimates that allow the risk quotient (RQ) values to be further
refined and potentially pass the screen without requiring higher tier effects testing at the
semi- or full-field level. However, while the proposed Tier I process for bees is quantitative
and results in an RQ value which can in turn be compared to a Level of Concern (LOC),
higher tier refinements are used to qualitatively (i.e., no RQ derivation) determine whether
whole hives will be adversely affected from the use of a pesticide based on the initial
screening-level assessment.
a. Please comment on the use of data on individual bees to transition to higher tier studies
given that the Tier I studies focus on survival as the primary measurement endpoint although
additional endpoints may be forthcoming as test designs continue to develop.
Individual-level phenotype does not translate to colony-level phenotype in very effective ways.
Changes in worker longevity and life-history transitions (i.e., age at first foraging) would likely
be most impacted. Use of mathematical modeling would assist empirical measures greatly by
generating expectations that can be verified.
Data on individual pupae can be very informative and have a greater direct impact from lower
tiers to higher tiers (see Question 9 to Panels Response). In doing so, there is a need to assess
mode-of-action in order to qualitatively assess risks. For example, Insect Growth Regulators
(IGRs) are not as likely to have acute toxicity, but they can also affect development or egg
viability (Hodgson et al., 2011).
Higher tier studies are necessary to address risk under more realistic conditions with bee colonies
and the function of hives. The function of a hive and the multiple behaviors that are needed to
sustain a viable colony, the super-organism, may not be detectable in laboratory studies. Thus, if
a conservative Tier I triggers higher studies because of adult or larval toxicity and behavioral
aspects, higher tier tests taking into account the different important exposure routes are essential.
b. Please comment on the derivation of the Level of Concern (i.e., LOC=0.4) and the extent to
which it serves as an appropriate screen to transition to higher tiers of testing/refinement.
A given LOC, however, does provide a context by which a default concentration can be tested.
Essentially, EPA is proposing to bring the LOC to the NOEC. The current data is based on
young worker bees. The Panel proposes including larvae and oral toxicity, so this will make the
tests more sensitive.
Similarly, one basal assumption in the calculation of the LOC and its extrapolation to the field is
that the compounds are used following best management practices (BMP). One of the most
important values of Tier III screenings is that they may enable the capture of real-world
applications including instances of non-BMP.
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In the white paper, the level of concern is compared to a risk quotient that is defined as the
contact or dietary exposure value divided by the contact or oral LD50 value. EPA proposes to set
this value at 0.4 which is equivalent to approximately 10% mortality. Given the uncertainty in
extrapolating effects on individual bees to effects on the colony, it is difficult to consider an
appropriate level of concern for adult bee mortality at the Tier I level. As discussed in other
questions, other endpoints (e.g., behavior, development, growth rate) may be more appropriate
and reflective of colony health. At this point, the science does not support that 10% mortality of
adult bees would result in colony collapse or even instability. Hence, the Panel believes this
value is too conservative.
In order to approximate a more realistic mortality, one might look at a sensitivity analysis of
mortality in currently existing population biology models such as described by Fefferman and
Starks 2006.
The suggested approach seems very conservative, and is even more protective than the
established Hazard Quotient (HQ) method triggering higher tier studies if the HQ is greater than
50 and seems to ensure high certainty.
c. Please comment of the quantitative aspect of the screening-level (Tier I) assessment and the
use of Tier II and Tier III whole hive studies to qualitatively characterize risk.
The main utility is to provide a scale of concentrations. The field-tested concentrations,
however, would need to be modulated up or down depending on effects on colony phenotype.
Different realistic exposure scenarios and different stressors are automatically included in higher
tiers and are better suited to real life. As Tier I appears to be very conservative, the approach
seems to ensure that higher tiers are triggered. Tier II represents a worst case which are sensitive
to discover effects (confinement). Tier III represents a more realistic scenario by integrating all
multiple stressors and effects that cannot be addressed by Tier II studies (e.g., homing behavior).
d. Please comment on the assumption that the effects on individual bees measured in laboratory
studies must be considered in the context of whole colony studies conducted under semi-field
and full-field conditions.
The Panel believes that this is the fundamental assumption that defines the problem that
individual phenotype is not a proxy for colony phenotype. However because colonies are
comprised of individuals, knowing both is paramount.
Depending on the nature of effects and taking into account the mode of action, the efficacy
information (e.g., IGR properties), substance properties (e.g., systemic), the application method,
and persistency of a compound, higher tier studies may need special adaptations to be ensure that
the concerns about a substance/product are investigated.
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e. Please comment on the proposed use of a weight-of-evidence approach based on information

obtained from multiple tiers of risk assessment for characterizing pesticide risks to honey
bees.
Using one level of biological organization as a proxy for others is always fraught with difficulty.
However, some correlations are stronger than others, thus identifying those with the strongest
linkages is key. In doing so, high-throughput methods that are reliable and repeatable will be
most valuable. Qualitative evidence is more important in social systems than simple mortality
derived from solitary systems.
The Panel also feels that the weight of evidence should be centralizing toward the Tier II level as
being the most informative for social insects, because the colony is the basal unit of selection
(see Question 8).
Feedback for the weight of evidence from investigations of incidents needs to be taken into
account. Detecting incidents may be used to inform risk assessors and risk managers. Every
single incident may not necessarily change the outcome of a risk assessment. This is because
there needs to be a careful investigation of the cause (e.g., proper use/ misuse and whether there
is a sound conclusion) before incidents should be taken into account for the weight of evidence.
Using incident reporting may be helpful, but when considering an incident one must differentiate
from the proper and improper use of a pesticide.
f. Please comment on how best to characterize overall uncertainty or weigh different areas of
uncertainty in risk characterization.
Tier III studies are much more prone to a Type II statistical error (appearing to not have any
significant effects, when there really are some), while Tier II studies are more prone to a Type I
statistical error (appearing to have significant effects, when in reality there are none). The level
of uncertainty can be determined in a Tier I type of experiment, but it is more difficult to
determine in Type III studies with honey bee hives. Thus, if the test pesticide appears to have no
negative effects in Tier III studies, these results need to be checked against the preponderance of
evidence at lower tier levels (see also Question 13e). The number of studies with negative
effects should affect the weight given to uncertainty.
g. Please comment on how to focus/prioritize uncertainties when designing and interpreting
Tier II and Tier III studies.
Most of these recommendations have been addressed previously by the Panel, such as increasing
sample size, increasing statistical power, including replication, factoring in genetic variability,
and focusing at the Tier II level (see also Question 13d to Panels Response).
In doing so, it is important to focus on those potential problems that are identified at lower tiers.
For example, if chronic larval exposure is identified as problematic at Tier I compared to acute
adult mortality, then focusing on colony-level brood measurements at Tiers II and III should take
priority. Thus, focusing on a standard one or two factor/s for every study does not adequately
91
address the complexities of honey bee colonies; rather, those hypotheses need to be modulated
according to the route of exposure and potential impact at the colony level.
One panelist notes that Bayesian methods may be useful tools for data analysis. They are
designed to determine "what is the significance of what we were able to observe" rather than
applying a "significant or not" test that relies on traditional, frequentist views of statistical power
that may be unrealistic for studies of expensive or difficult scenarios.
14. Colony-level Modeling. As part of the proposed risk assessment process, Section 5.4 of the
white paper discusses the concept of using colony-level models as a means of integrating
exposure and effects information generated from the multiple risk assessment tiers and in turn
linking this information quantitatively to the proposed assessment endpoints. Conceptually, such
models could inform the need for transitioning from lower tiers to higher tiers in the risk
assessment process. They could also be considered in identifying critical design elements of
higher tier studies (e.g., semi-filed or full field studies).
a. Please comment on the concept of using colony-level ecological models to inform the
proposed risk assessment process for honey bees, as indicated above.
The Panel agrees that, in concept, employing colony-level ecological models should greatly
strengthen the ability to generate valid risk assessment for honey bees. As an example,
interactions and scaling questions from individual effects to colony level effects are exactly one
sort of thing that mathematical models can do.
The most useful way models can accomplish this is to identify proximate, measurable outcomes
that should be monitored for, rather than requiring a Boolean outcome of colony death. As long
as the identified metrics are things that can actually be observed and measured, then we can use
the models to identify which individual- and group-communication-level responses to pesticide
exposure may lead to colony-level compromise of function without testing each type of
exposure/interaction empirically.
There are a number of potential pitfalls that should be avoided. Most importantly, the Panel
agrees that colony-level simulation models attempt to model, most or all aspects of colony life
should not be used. As discussed/evidenced in much of the white paper discussing empirical
results prior to section 5.4, critical elements on which any colony-level ecological model could
be built remain unknown/uncertain. These uncertainties exist in both empirical measurements
for important parameters, and in functional response relationships among variables. While the
Panel agreed that models should still play a vital role in risk assessment, under these conditions,
many smaller models, examining the role of uncertainty in within-colony dynamics and
responses to particular parameters should be explored independently prior to inclusion in a single
ecological model that is intended to capture everything. Applied mathematical models have
repeatedly demonstrated how seemingly insignificant interactions among uncertain terms and
functional responses can cause the predictive power of a model to drop substantially relative to
the insight that can be gained by the careful consideration of the impact of uncertainties on
92
smaller, more local questions, then interpreted together to inform a global result (Regan et al. ,
2003; Lek, 2007).
One panel member believes that models should be used to add Tier I measures, but not to reject
measures. However, more generally, the Panel agrees that, as indicated in Figure 1 of the
whitepaper, risk assessment is an iterative process, and the findings from validated colony-level
models can be used to evaluate the usefulness of Tier I toxicity tests and assessment endpoints in
predicting colony level effects. This information can then be used to revisit, refine, and revise
Tier I toxicity testing requirements, as necessary, in order to make the Tier I tests more relevant
to the Agency's protection goals for bees.
The Panel generally expresses enthusiasm about the inclusion of modeling efforts as part of a
thorough risk assessment. There was initial, abstract discussion about how models could be used
to deal with questions of scale (i.e., how individual-level effects might interact or act in parallel
to yield colony- or even population-level effects). Further, the Panel agrees with the potential for
models to aid in determining when particular outcomes from spatially or temporally local studies
might provide insight into broader, nation-wide or multi-year processes. (Many of these
comments and discussions occurred during discussion of other charge questions, though in
reference to eventual discussion during Charge Question 14 and its parts.)
The Panel expresses the view that both simulation models (as those discussed in the white paper)
and analytic models would be of use to pollinator risk assessment efforts. In clarification,
analytic models are those that focus on the causal relationships among variables and parameters.
They use equations to capture these relationships, and are primarily used to generate insight into
system-level processes (e.g., threshold behaviors for phase transitions). Examples of such phase
transitions include the formation of crystals as liquids solidify, rain falling from a cloud,
epidemics emerging from endemic disease spread depending on birth rates, and to end with an
example from bees the convergence to consensus for a new nest site during swarming. Each of
these insights into what combinations of conditions lead to the transition (i.e., liquid vs. solid,
argument vs. consensus, etc.) can be made using an analytic model without the need for
empirical measurement of the system. For example, there is no need for information on the
number of bees arguing for each of how many different new potential nest sites to be able to use
the model to determine a set of necessary and sufficient conditions for the decision to be made.
Analysis can then be made about questions such as trade-offs in time vs. optimality of site
quality. Similarly in the more physical examples, how to successfully seed clouds, or provide an
initial lattice on which crystal formation can coalesce to produce crystals with particular
properties. Basically, analytic models provide insight into how to manipulate the system, so long
as the understanding of causal relationships has been appropriately captured. Peer review of
analytic models focuses on appropriately capturing these causal relationships, rather than on
particular values for variables or parameters, and validation refers to validation of the
relationships (usually by describing conditions that imply, by logical necessity, certain behaviors,
rather than comparison of predictions of particular numbers with real world measurements).
From these analytic models, one can then build simulations. In these simulations, the equations
are used with particular initial variable values, and particular informed parameters to compute
what are called numerical solutions (i.e., values predicted by the analytic equations).
93
Producing these values is different from analyzing the equations because it will reveal outcomes
as measured values, rather than showing where those values must occur (i.e., we tried running
this model at increasing values from 0.1 to 0.9, and after we make this number bigger than 0.5,
we get crystals, but not when its less than 0.5 instead of due to the nature of these equations,
we can solve for the critical number for crystallization, and that equation will hold no matter
what the parameter values for our liquid will be, so long as the relationships represented in the
model are correct).
Whatever models are used, model validation involves statistical analysis of the correlation
between model outcomes and real-world observations.
In choosing models to aid in pollinator risk assessment, the Panel expressed concern that,
especially for Tier 1-level studies, the value of simulation models may be obviated by the need
for as many measurements to parameterize them as would be needed to simply answer the
question of interest. This is not the case in Tiers II and III.
Brief Examples of Analytic Models:
An example from physics can be found in the ideal gas relationship between Temperature,
Volume, and Pressure expressed as PV=nRT-Where n is number of moles, and R is the
universal gas constant. If we did not know this formula, we could experimentally determine that
the relationship between temperature pressure are linear for a given volume. However then,
every volume and type of gas would require validation testing to identify the constant k.
Knowing the full formula provides us a way to evaluate how the relationship between
temperature and volume determines pressure for every ideal gas, rather than generating a
separate simulation model for each gas in order to predict the outcome. This provides insight into
the existence of potential thresholds, and the values of these thresholds lead to sufficient criteria
for empirical measurement to ensure that a system would remain within acceptable boundaries
for application.
A honey bee example that is analogous to this system would be the use of daily worker mortality
as a single-metric test for colony failure, as discussed during earlier Panel deliberations.
However, death rates are much less informative or predictive of failure than the relationship
between daily worker mortality and daily worker eclosion (the emergence of new workers). If
the eclosion rate is greater than the rate that the workforce is dying, worker death is unlikely to
cause failure, even if percent mortality intuitively seems relatively high. The ratio of workforce
loss to workforce recruitment is what should be considered. This is an example of how an
analytic model of demographic colony processes improves our understanding and reveals how
the single proposed metric may fail to capture the outcome of interest.
Notice that the new metric, this ratio of birth and death rates, allows insight into whether a
colony is thriving or dying without measuring a single empirical number to plug into the
equations. This is the hallmark of a valuable analytic mathematical model. It provides a valuable
measure that is testable. Of course, this ratio is unlikely to be all that is needed, there must also
be some thresholds, such as a minimum population size for colony persistence, and potentially a
maximum population size to include swarming within a colony and carrying capacity within a
location.)
94
The Panel also agrees that analytic models can indicate what to go measure or simulate to
understand which aspects are truly important to colony success. Models in this and other
contexts have already shown cases in which intuitively important values turn out to be mostly
irrelevant (Fefferman and Starks 2006), and cases in which intuitively irrelevant values turn out
to be critical (Boccara 2004.).
The Panel pointed out that this does not mean there is the equivalent of a data gap here. One of
the benefits of analytic models for this use is that all the building blocks for this type of model
are already available for honey bee colony processes in various forms: growth, fission, foraging,
etc. (Fefferman and Starks 2006, Khoury et al. 2011). These models can be used with the new
focal questions of pesticide exposure to explore which particular elements will be most relevant
to test and at which Tiers of effect.
Lastly, the Panel agreed that the Tiers themselves become problematic in a modeling context.
Colony-level models can and should be used to backwards inform which individual-level
measurements will be critical to colony survival. This is not a loop in the conceptual model
sense, but changes the direction of the conceptual-flow. Thus, flow arrows. In these cases, it
would be a mistake to use Tier 1 equivalent models as the first-pass studies, progressing to other
Tiers only when Tier 1 results seem to indicate the need for concern. Instead, colony-level or
population-level models that would mirror the types of empirical studies performed in Tiers II or
III can be modeled with analytic models to determine which individual-bee tests would be likely
to scale up to colony-level issues of concern. This can help directly with the relatively qualitative
problem of cumulative sub-lethal effects failing to trigger Tier I progression to Tier II, while still
resulting in serious compromise to colony- level success.
b.
Please comment on the state of the science regarding available honey bee models discussed
in Section 5.4.2 of the white paper in relation to their potential application in a regulatory
risk assessment context. In particular, please comment on the extent that such models have
been evaluated using empirical data related to honey bee population dynamics and the
availability of such data for their parameterization.
The Panel notes that many of the models discussed directly in the white paper have access to
only sparse data, thus far. While the Panel agrees that it will be important to collect further input
data (i.e. measurements of parameter values and valid characterizations of functional
relationships), and important to collect validation data (i.e., measurements from the real world
for comparison with predicted model outcomes), the Panel also noted that analytic models can be
useful in the absence of such data. It would be a mistake to value the input of all models only
once empirical measurements to appropriately parameterize simulation models exist. The
conclusions of models can provide insight into how systems work (see discussion of analytic
models above), in addition to making more specific predictions about system outcomes for focal
metrics. For purposes of risk assessment, the Panel notes that this more general type of
employment for models can help assess the importance of unknown threats. (e.g. In the cases in
which a model demonstrates that only individual sensitivity greater than some threshold X per
unit of exposure could cause the collapse of a colony by significantly altering the death-toeclosion ratio. Even if very little is known about individual sensitivity to exposure, this can
provide valuable insight.)
95
Further, even where data for parameterization and validation of the models have been available,
these data have frequently been in aid of testing the specific predictions of each simulation
models motivating question. There is danger in assuming that a model that can consistently
predict one outcome of a system is accurately capturing (and could therefore predict) all of the
workings of the system without a peer review step for the analytic representation of relationship
among model components. Few, if any, of these models have been compared to other models or
tested for robustness of model choices apart from their specific focal questions. Model validation
and calibration is also problematic since there little agreement on what constitutes an appropriate
level of agreement between measured and predicted values.
Within the narrower context of models and their use for empirical simulation and prediction , the
Panel notes the need to discuss appropriate sensitivity and robustness testing for individual
parameters, variables, and functional relationships. These need to explicitly and separately
discuss how to extract useful insight despite both biological stochasticity and
measurement/relational uncertainty (this relates to Question 13.f). The Panel concluded that
these discussions must be accomplished on a model-by-model basis because the impact of these
different forces will vary by model design.
One panel member believes that although models may have the potential to inform risk
assessment, the state of modeling is currently insufficient for practical use and that instead there
should be more reliance on higher tier tests. This panel member further stresses that the current
state of modeling is limited because it cannot account for all the various complexities of a bee
colony.
c.
Please comment on the most important elements that should be considered in reviewing
available honey bee colony ecological models for potential application in risk assessments.
The Panel concludes that the first two questions that should be asked with any model are What
insight does it provide that accurate empirical studies could not or, if there is none, How does
the model spare effort or expense to provide those insights. In the case of risk assessment, there
are two main components: How likely is the scenario in question to occur, and how severe is the
likely outcome if that scenario were to occur. For colony-level ecological models, the former
question relates to exposure in individual bees and how those individual doses interact to affect
single colony behavior/survival. The latter question relates to the impact of individual colony
responses on the broader ecology of honey bees, and on the use of the population as effective
pollinators.
The Panel further concludes that, as the models presented in the white paper were not designed
with these types of questions in mind, they do not specifically address these questions in directly
useful ways, but could be very important in formulating answers within each level of concern to
eventually produce a useful risk assessment. However, the Panel agreed that this again points to
the need for an analytic set of models to designate and integrate each of these more specific
models into a broader understanding of where the focal research results for each aspect will fit
into the context of broader risk assessment. Many of the panel members agreed that expanding
to include this type of modeling as well will generate insight into which metrics will be most
96
useful, and then will allow us to generate the simulation/numerical solution models to predict
actual outcomes based on values obtained experimentally.
97
References
Alaux, C., M. Folschweiller, C. McDonnell, D. Beslay, M. Cousin, C. Dussaubat, J. L. Brunet,
and Y. Le Conte. 2011. Pathological effects of the microsporidium Nosema ceranae on honey
bee queen physiology (Apis mellifera). Journal of Invertebrate Pathology 106: 380-385.
Atkins, E.L. and D. Kallum 1986. Comparative morphogenetic and toxicity studies on the effect
of pesticides on honey bee brood. Journal of Apicultural Research 25: 242-255.
Aupinel, P., D. Fortini, H. Dufour, J.-N. Tasei, B. Michaud, J.-F. Odoux and M.-H. PhamDelegue. 2005. Improvement of artificial feeding in a standard in vitro method for rearing Apis
mellifera larvae. Bulletin of Insectology 58: 107-111.
Aupinel, P., D. Fortini, B. Michaud, F. Marolleau, JN. Tasei and JF. Odoux. 2007. Toxicity of
dimethoate and fenoxycarb to honey bee brood (Apis mellifera), using a new in vitro
standardized feeding method. Pest Management Science 63: 1090 1094.
Badano, E.I. 2011. Potential negative effects of exotic honey bees on the diversity of native
pollinators and yield of highland coffee plantations. Agricultural and forest entomology 13(4):
365-372.
Boccara, N. 2004. Modeling Complex Systems. Springer, Chicago, Illinois
Buchmann, S. L. and G. P. Nabhan. 1996. The Forgotten Pollinators. Island Press/Shearwater
Press, Washington, D.C.
Burken, J. G., and J. L. Schnoor. 1998. Predictive relationships for uptake of organic
contaminants by hybrid poplar trees. Environmental Science and Technology. 32:3379-3385
Ciarlo, T. J., C. A. Mullin, J. L. Frazier and D. R. Schmehl. 2012. Learning impairment in honey
bees caused by agricultural spray adjuvants. PLoS ONE, 7, e40848-e40848.
COLOSS, 2010. Proceedings of the COLOSS Workshop Method standardization for larval,
Graz, Austria, Available online at:
http://www.coloss.org/publications/ProceedingsCOLOSSLarvalRearingGraz2010.pdf
Davis, A.R. and R.W. Shuel. 1988. Distribution of C(14)Labeled carbofuran and dimethoate in
royal jelly, queen larvae and nurse honey bees. Apicologie, 19 (1): 3750.
Delaney, D. A., J. J. Keller, J. R. Caren and D. R. Tarpy. 2011. The physical, insemination, and
reproductive quality of honey bee queens (Apis mellifera). Apidologie, 42, 1-13.
De Rossi, C. 2010. (Dissertation) Pesticides in the atmosphere Occurrence, distribution and
behaviour of selected pesticides in the vinicultural area of Trier, Germany(http://ubt.opus.hbz
nrw.de/volltexte/2010/573/pdf/DeRossiChiaraDiss.pdf).
98
Dohzono, I. 2010. Impacts of alien bees on native plant-pollinator relationships: A review with
special emphasis on plant reproduction. Applied entomology and zoology 45(1):37-47.
EFSA. 2012. Scientific Opinion on the science behind the development of a risk assessment of
Plant Protection Products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA Journal
2012; 10(5) 2668. [275 pp.] doi:10.2903/j.efsa.2012.2668. Available online at:
www.efsa.europa.eu/efsajournal
Evans, J. D., Y. P. Chen, G. Di Prisco, J. Pettis and V. Williams. 2009. Bee cups: single-use
cages for honey bee experiments. Journal of Apicultural Research, 48, 300-302.
Fefferman, N.H. and P.T.B. Starks. 2006. A modeling approach to swarming in honey bees.
Insectes Sociaux 53(1):37-4
Forster et al., 2012. ICPBR-Working Group Risks posed by dusts: overview of the area and
Recommendations, Julius-Khn-Archiv, 437: 191-198
Franke. P, Juraske, R., Anton, A., Charles, R. Jolliet, O. 2012. Evaluation of Pesticides In FoodA Dynamic Multicrop Model, 6th SETAC World Congress
Available online at: http://www.lc-impact.eu/userfiles/Fantke_SETAC2012a.pdf
Frankham, R. 1995. Effective population size/adult population size ratios in wildlife: a review.
Genetical Research, 66, pp 95-107 doi:10.1017/S0016672300034455.
Goulson, D. 2003. Effects of introduced bees on native ecosystems. Annual Review of Ecology
and Systematics 34: 1-26.
Hendriksma HP, Hartel S, Steffan-Dewenter I 2011, Honey bee risk assessment: new approach
for in vitro larvae rearing and data analysis. Methods in Ecology and Evolution 2: 509-517)
Hodgson, E. W., T. L. Pitts-Singer, and J. D. Barbour. 2011. Effects of the insect growth
regulator, novaluron, on immature alfalfa leafcutting bees, Megachile rotundata. J. Insect Sci. 11:
43.
Johnson, R. M., J. D. Evans, G. E. Robinson and M. R. Berenbaum. 2009. Changes in transcript
abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proceedings of the
National Academy of Sciences of the United States of America, 106, 14790-14795.
Johnson RM, Mao W, Pollock HS, Niu G, Schuler MA, et al. 2012. Ecologically Appropriate
Xenobiotics Induce Cytochrome P450s in Apis mellifera. PLoS ONE 7(2): e31051.
doi:10.1371/journal.pone.0031051
Kamel, A.; Dively, G.; Hawthorn, D. and J. Pettis. Unpublished research examining the fate of
imidacloprid and its metabolites in honey bee hives.
Klein, A.-M., I. Steffan-Dewenter, and T. Tscharntke. 2003. Fruit set of highland coffee
increases with the diversity of pollinating bees. Proc. R. Soc. Lond. B. 27: 955-961.
99
Khoury, D.S., M.R. Myerscough, and A.B. Barron. 2011. A Quantitative Model of Honey Bee
Colony Population Dynamics. PLoS ONE 6(4): e18491.
Kremen, C., N. M. Williams, and R. W. Thorp. 2002. Crop pollination from native bees at risk
from agricultural intensification. Proceedings of the National Academy of Sciences 99:1681216816.
Lande, R. and G.F. Barrowclough. 1987. Effective population size, genetic variation, and their
use in population management. Pages 87-123 in M.E. Soule, ed. Viable populations for
conservation. Cambridge University Press, Cambridge, England.
Larney, F.J., A.J. Cessan, and M.S. Bullock. 1999. Herbicide transport on wind-eroded sediment.
Journal of Environmental Quality 28:1412-1421.
Lek, S.S. 2007. Uncertainty in Ecological Models. Ecological Modelling 207, 1 1-2.
Mayer, D. F. and C. A. Johansen. 2003. The rise and decline of Nomia melanderi (Hymenoptera:
Halictidae) as a commercial pollinator for alfalfa seed. In (K. Strickler and J. H. Cane, Eds.) For
Nonnative Crops, Whence Pollinators of the Future? Thomas Say Publications in Entomology:
Proceedings. Entomological Society of America. Lanham, MD. pp. 139-149.
Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, et al. (2010) High Levels of Miticides
and Agrochemicals in North American Apiaries: Implications for Honey Bee Health. PLoS ONE
5(3): e9754. doi:10.1371/journal.pone.0009754
OECD a.. 1998. Guidelines for the testing of chemicals Number 213 Honey bees, acute oral
toxicity test, OECD, Environmental Health and Safety Division, Paris,.
OECD b. 1998. Guidelines for the testing of chemicals Number 214 Honey bees, acute contact
toxicity test, OECD, Environmental Health and Safety Division, Paris,
OECD 2007. OECD Guidance Document 75. 2007. Guidance document on the honey bee (Apis
mellifera L.) brood test under semi-field conditions. Series on testing and assessment, Number
75. ENV JM MONO22.
OEPP/EPPO 2001. Guideline for the efficacy evaluation of plant protection products Side
effects on honey bees.- OEPP/EPPO Bulletin, PP 1/170(3) update 2000, 19-23.
Oomen PA, De Ruijter A and Van der Steen J 1992. Method for honey bee brood feeding tests
with insect growth-regulating insecticides. EPPO Bull. 22: 613-616.
Regan, H. M., H.R. Akcakaya, S. Ferson, K.V. Root, S. Carroll, L.R. Ginzburg. 2003.
Treatments of Uncertainty and Variability in Ecological Risk Assessment of Single-Species
Populations. Human and Ecological Risk Assessment. Vol. 9, no. 4, pp. 889-906.
100
Rortais, A., Arnold, G., Halm, M.P., F. TouffetBriens. 2005. Modes of honey bees exposure to
systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by
different categories of bees. Apidologie, 36: 7183.
Rueppell, O., C. Bachelier, M. K. Fondrk and R. E. Page. 2007. Regulation of life history
determines lifespan of worker honey bees (Apis mellifera L.). Experimental Gerontology, 42,
1020-1032.
Rubik, D.W and H. Wolda. 2001. Do competing honey bees matter? Dynamics and abundance of
native bees before and after honey bee invasion. Population Ecology 43(1):53-62.
Roberts, S.P. and J. F. Harrison. 1999. Mechanisms of thermal stability during flight in honey
bee Apies Mellifera. J. Expt Biol. 202, 15231533 1999.
Schaffer, W.M. D.W. Zeh, S.L. Buchmann, S Kleinhans, M.V. Schaffer, and J. Antrim. 1983.
Competition for Nectar between Introduced Honey Bees and Native North American Bees and
Ants. Ecology 64(3):564-577.
Shaw, K.E., G. Davidson, S.J. Clark, B.V. Ball, D. Chandler, and K.D. Sunderland, 2002.
Laboratory bioassays to assess the pathogenicity of mitosporic fungi to Varroa destructor (Acari:
Mesostigmata), an ectoparasitic mite of the honey bee, Apis mellifera. Biological Control 24:
266-276.
Spannhoff, A. 1, KeeKim, Y1, Raynal, N. 2, Gharibyan, V. 2, Su, M., Zhou, Y, Li, J. 3,
Castellano, S. , Sbardella, G, Issa, J& Bedford, M. 1,
2011. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees,
EMBO reports VOL 12 | NO 3 | 2011 &2011 European Mollecular Biology Organization
Sugden, E. A., R. W. Thorp, and S. L. Buchmann. 1996. Honey bee-native bee competition:
focal point for environmental change and apicultural response in Australia. Bee World. 77: 2644.
US EPA. 2001. GENeric Estimated Environmental Concentration Model (GENEEC),
Available online at: http://www.epa.gov/oppefed1/models/water/geneec2_description.htm
US EPA 2012. EPA: Pesticides - A Discussion with the FIFRA Scientific Advisory Panel
Regarding the Terrestrial and Aquatic Level II Refined Risk Assessment Models (Version 2.0) Chapter III. Terrestrial Level II Model). Available at:
http://www.epa.gov/oppefed1/ecorisk/fifrasap/rra chap three.htm
Tapparo, A., D. Marton, C. Giorio, A. Zanella, L. Solda, M. Marzaro, L. Vivian, and V.
Girolami, 2012. Assessment of the environmental exposure of honeybess to particulate matter
containing neonicotinoid insecticides coming from treated corn seeds. Environmental Science
Technology 46: 2592-2599.
101
Tepedino, V. J., Alston, D. G.; Bradley, B. A., Toler, T. R., and Griswold, T. L. 2007. Orchard
pollination in Capitol Reef National Park, Utah, USA. Honey bees or native bees? Biodiversity
and Conservation. 16: 3083-3094.
Thomson, D. 2004. Competitive interactions between the invasive European honey bee and
native bumble bees. Ecology 85(2):458-470.
Thomson, D.M. 2006. Detecting the effects of introduced species: a case study of competition
between Apis and Bombus. Oikos 114(3):407-418.
Tuell, J. K., J. S. Ascher and R. Isaacs. (2009). Wild Bees (Hymenoptera: Apoidea: Anthophila)
of the Michigan Highbush Blueberry Agroecosystem. Annals of the Entomological Society of
America, 102, 275-287.
Wittmann D. (1982) Determination of the LC50 of Dimilin 25 WP for honey bee brood on free
flying colonies as an example for the use of a new Apis larvae-test, Apidologie 13, 104107
Wu, J. Y., C. M. Anelli and W. S. Sheppard. (2011). Sub-Lethal Effects of Pesticide Residues in
Brood Comb on Worker Honey Bee (Apis mellifera) Development and Longevity. PLoS ONE, 6.
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Cluster meeting on Pollinators EPA/EFSA/PMRA

7 February 2013 (Thursday)
9.00-11.00 am ET Arlington VA/US-15.00-17.00 pm Parma IT
______________________________________________________________
Coordination of the telephone call and pass code to be sent later to all participants by
Rochelle Richardson richardson.rochelle@epa.gov Tel 703-308-6860
__________________________________________________________________________________
Attendants:
US EPA: Don Braddy , Tom Steeger, Richard Keigwin
EFSA: Agns Rortais, Csaba Szentes , Domenica Auteri
Canada: PMRA Mary Mitchel, Connie Hart , Marguerita Conti
USDA/ARS: David Epstein, Kevin J. Hackett; Jeff Pettis, Mary Purcel
FDA//CFSAN : Marty Stutsman , Charlotte Liang;
FDA / CVM Julia Oriani and Lynn Friedlander , Emily Smith, Michelle Kornele.
Anna OBrien, Prajwal Regmi, Brent Volker.
NAS Robin Schoen (to be confirmed)
Welcome and introduction of the participants

1.
9.00 am To be confirmed: EPA Steve Bradbury (or Don Brady), EFSA Catherine Geslain-Laneele (or
Jordi), PH Canada Richard Aucoin (or Mary Mitchell) ) (5 )
2.
09.05 am . White paper SAP Pollinator meeting (final report) : EPA short presentation and
Exchange of views, (Implications for the Risk assessments in case of divergent opinions).
EPA/PMRA/: Tom Steeger will present this joint project /Connie Hart PMRA Rep (20)
EFSA: Csaba Szentes (comments from EFSA)
Open Discussion Q & A (10)
3.
09.35 am . USDA proceedings report of the last Stakeholder meeting : The Steering Committee
for CCD (USDA/ARS / EPA) will finalize a position paper on research priorities based on the last
National Stakeholder meeting conclusions.
USDA/ ARS : David Epstein will be presenting the Bee Health Workshop Report progress on
behalf of the CCD Steering Committee, (15 )
Open discussion Q& A (5 )
09.55 am EFSA briefing about the next EFSA global report on pollinators for May 2013 : Briefing
from EFSA on the a global report to be presented in for May 2013 with the support of the Task force on
honey bees
EFSA : Agns Rortais (15)
Open discussion Q& A (5)
5.
10.15 am OECD/PEIP Activities by FDA and EFSA in the working group - Pesticide Effects
on
Insect Pollinators - Exchange of views of the current activities for better understanding and
cooperation
EPA/: Don Brady PMRA Connie Hart ( 3)
EFSA :Csaba Szentes (3)
Open discusin (4)
6.
10.25 am Neonicotinoids
possible collaboration on data and risk evaluation.
EPA/ Richard Keigwin . PMRA: Marguerita Conti .Explanation of the current join work and
work schedule 6
EFSA : Domenica Auteri.Short explanation of the last scientific opinions and expected future
tasks (4)
Open discussion 10
7.
10.45 am . ANY OTHER BUSINESS

EFSA (Agnes) will explain the scheduled Colloquium for nest 16/05/2013 and invite the
participants to attend (3)
EPA: Don Braddy (3)
i)
H. Update on other pollinator activities
ii)
Pollinator summit in US
iii)
PPDC Workgroup status
PMRA: Mary Mitchell Canadian incident analysis and risk mitigation publication (3)
ARS ; David Epstein (?)
Other participants 5
8.
10.55 am Follow up Don Brady/Jordi Serratosa/ Mary Mitchel
Documents enclosed :
Point 2 :
Final report September FIFRA sap pollinator meeting pdf.
Point 4
EFSA 's Mandate/charge of the task force attached ; draft of the outline of the report
AOB:
EFSA mandate of the Colloquium on bees planned for 15-16/05/2013 pdf
Additional Doc National Academy of Science doc from 2007
_______________________________________________________________________
EFSA: Csaba Szentes (comments from EFSA)

Open Discussion Q & A (10)
3. 09.35 am . USDA proceedings report of the last Stakeholder meeting : The Steering
Committee for CCD (USDA/ARS / EPA) will finalize a position paper on research priorities
based on the last National Stakeholder meeting conclusions.
USDA/ ARS : David Epstein will be presenting the Bee Health Workshop Report
progress on behalf of the CCD Steering Committee,(15 )
Open discussion Q& A (5 )
4 09.55 am EFSA briefing about the next EFSA global report on pollinators for May 2013 :
Briefing from EFSA on the a global report to be presented in for May 2013 with the support of
the Task force on honey bees
EFSA : Agns Rortais (15)

Open discussion Q& A (5)
5. 10.15 am OECD/PEIP Activities by FDA and EFSA in the working group - Pesticide Effects
on Insect Pollinators - Exchange of views of the current activities for better
understanding and cooperation
EPA/: Don Brady PMRA Connie Hart ( 3)

EFSA :Csaba Szentes (3)
Open discussion (4)
6. 10.25 am Neonicotinoids
possible collaboration on data and risk evaluation.
EPA/ Richard Keigwin . PMRA: Marguerita Conti .Explanation of the current join
work and work schedule 6
EFSA : Domenica Auteri.Short explanation of the last scientific opinions and expected
future tasks (4)
Open discussion 10
7. 10.45 am . ANY OTHER BUSINESS
EFSA (Agnes) will explain the scheduled Colloquium for nest 16/05/2013 and
invite the participants to attend (3)
EPA: Don Brady (3)
i. H. Update on other pollinator activities
ii. Pollinator summit in US
iii. PPDC Workgroup status
PMRA: Mary Mitchell Canadian incident analysis and risk mitigation publication
(3)
ARS ; David Epstein (?)

Other participants 5
8. 10.55 am Follow up Don Brady/Jordi Serratosa/ Mary Mitchell
Documents enclosed :
Agenda
Point 2 : Final report September FIFRA sap pollinator meeting pdf.

Point 4 EFSA 's Mandate/charge of the task force attached ; draft of the outline of the report
AOB: EFSA mandate of the Colloquium on bees planned for 15-16/05/2013 pdf
Additional Doc National Academy of Science doc from 2007
_______________________________________________________________________
From:
To:
Cc:

John Scott; Cindy Baker-Smith; Iain Kelly; Steve Coy; Joel; dparker@cotton.org;
rmcallister@croplifeamerica.org; Connie Hart; Bagdon, Joseph - NRCS, Amherst, MA; willett@nwhort.org;
skegley@pesticideresearch.com; Rick Smith; ScottSchertz@schertzaerial.com;(b) (6)
; John
Abbott; Tim.McPherson@usa.dupont.com; Julie.Schlekau@valent.com; clock-rust.mary@epa.gov;
Moriarty.Thomas@epa.gov
PMRA - Pollinator Protection: Reducing Risk from Treated Seed
Wednesday, February 06, 2013 2:50:46 PM
image001.png
image002.png
image003.png
image004.png
image005.png
Subject:
Date:
Attachments:
Recently, Connie Hart (PMRA) sent me a link to the publication Pollinator Protection: Reducing Risk
from Treated Seed (http://www.hc-sc.gc.ca/cps-spc/pubs/pest/_fact-fiche/pollinator-protectionpollinisateurs/index-eng.php) that was just posted on their website.
(b) (5)
Take care,
Erik W. Johansen
Phone: (360) 902-2078
Fax: (360) 902-2093
WSDA is now on
From:
To:
Subject:
Date:
Attachments:
Epstein, David
stelinski@ufl.edu
neonics
FFVA Neonic Project -- April 16.docx
Hey Luk,
I received a request from the FL Fruit & Vegetable Assoc (b) (5)
(b) (5)
I have attached a document they forwarded to me.
Any feedback you can provide that will help me prepare for my meeting with them this Thursday is
appreciated.
How did it go in Pullman?
Regards,
David
Office: (202) 720-9877
Mobile:(b) (6)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
From:
To:
Subject:
Date:
Attachments:
timothy.wilson@syngenta com
Epstein, David
MCFA CLA IMT 3.14.12 pptx
Wednesday, March 14, 2012 2:40:06 PM
MCFA CLA IMT 3.14.12 pptx
David,
Here is the presentation given today to the Minor Crop farm Alliance.
Best Regards,
Tim Wilson
_______________________________________________________________________________________________________________________________
Timothy E Wilson, Ph.D. | Senior Regulatory Product Manager Insecticides | Syngenta Crop Protection | 336.632.2877 |cell
(b) (6)
|timothy.wilson@syngenta.com
This message may contain confidential information. If you are not the designated recipient, please notify the sender immediately, and delete the original and any copies. Any use of
the message by you is prohibited.
From:
To:
Cc:
Subject:
Date:
Attachments:
Hackett, Kevin
Adamczyk, John; clint.hoffmann@gmail.com; Rinderer, Tom; Evans, Jay; Pettis, Jeff; Chen, Judy; Corona,
Miguel; Cook, Steven; Yocum, George; Rinehart, Joseph; Teal, Peter; James, Rosalind; Pitts Singer, Theresa;
Hoffman, Gloria; Meikle, William; Anderson, Kirk; Beck, John; Zhu, YC; Thomson, Steve; Huang, Yanbo; Fritz,
Brad; Aronstein, Kate; Danka, Bob; Kemp, William; Jones, Gretchen
King, Edgar; Purcell, Mary - ARS; Schneider, Sally; Upchurch, Dan; Sypura, Karin; Hanes, Glenn; Simmons,
Kay; Kunickis, Sheryl; Steeger, Thomas; Epstein, David; Jacobs-Young, Chavonda - ARS; Knipling, Edward;
Rexroad, Caird; Sonny.ramaswamy@oregonstate.edu; Hammond, Andrew; Whalen, Maureen; McHugh, Tara;
Spence, Joseph; Shafer, Steven; Chandler, Larry; McGuire, Michael (Mickey); Matteri, Robert; Brennan,
Deborah; Kaplan, Kim; Scott, Roy
Launch of Pesticide Effects on Honey Bee Project
Wednesday, May 29, 2013 3:44:20 PM
ARS Pesticide Researchers.docx
Honey Bee Conference Report FINAL 4-16-2013.pdf
Hello,
Industry has urgently requested that ARS investigate risk posed to honey bees by pesticides. ARS is
responding by funding several projects on a temporary (FY13) basis. Together with base funding in
this area, we have an exciting opportunity to accelerate progress in addressing two major questions:
1) What hazards do pesticides (especially neonicotinoid pesticides) and fungicides pose to the
honey bee?
2) What can be done to limit honey bee exposure to pesticides used in agriculture, particularly
those used in cotton, but also in almond and other crops?
For the $800,000 Southern Cotton Project listed at the top of the attached chart, John Adamczyk
(with experience in heading both cotton IPM and bee labs) has agreed to take lead for overall
project coordination. Tom Rinderer will take the lead for bee aspects. Clint Hoffmann has agreed to
take the lead for pesticide application technology; his experience in working with EPA will be
important since we need to make sure that we follow good laboratory practices (GLP) or the data
will be nearly useless for EPA decision-making. John, Tom, and Clint will be putting together a plan
of work for the Southern Cotton Project. To reduce redundancy in national effort, I have attached a
chart that highlights work being done in projects elsewhere at ARS. As a heads-up, I have copied
several researchers who do not necessarily have a role in the bee pesticide work, but may be asked
to provide critical input or, in some cases, to cooperate with the research. I have also copied John
Beck, at Albany, who is on detail doing a meta-analysis of the data on pesticide effects on honey
bees. His report, when it is completed, could provide important insights to guide the research.
Additionally, I have copied Mary Purcell (NIFA), who is co-chair of the Colony Collapse Disorder
Steering Committee and is detailing to ARS for the next few months to help with the NP304
Accomplishment Report (which has considerable bee work). Sheryl Kunickis is currently acting
Director of the REE Office of the Chief Scientist and is leading an effort to report ARS bee research
to Under Secretary Woteki; this pesticide research effort will be a key part of that report and will be
tracked rather closely at all levels in USDA and EPA. Tom Steeger, EPA, has been copied so that he is
aware that this project has been launched; he is an excellent contact for GLP experimental design
and has worked closely with us for several years. David Epstein, Office of Pest Management Policy,
recently (Oct 2012) led a national customer workshop on bees, and completion of the report of
attendees, which has important recommendations in the pesticide area (attached). Kim Kaplan, on
the ARS writing staff, is helping with the writing of the Bee Health and Colony Collapse Disorder
Action Plan. Others, with key administrative and oversight roles, were also copied in this first
message so that they are aware that this project will be taking place.
Everyone is encouraged to cooperate to help make the overall effort a success. The beekeeping
industry is in serious jeopardy and really does need our help. If pesticides are causing synergistic
sublethal effects, we really need to know. In particular, we need to answer the two questions posed
above. We came together around CCD when it first became a contributor to bee loss and have
made important gains as an agency. We need to do the same in the area of pesticide effects on
bees.
Also, note that Tom Rinderer has arranged a listening session for beekeepers in Baton Rouge on
June 4-5, 2013. This will provide additional input to the process.
Sally Schneider, Roy Scott, and I are ONP leads on the project.
Thank you for any help that you can give to make this project succeed.
Kevin

301-504-4680 (office)
301-504-6191 (fax)
Report on the National Stakeholders Conference on Honey Bee

Health
National Honey Bee Health Stakeholder

Conference Steering Committee
Sheraton Suites Old Town Alexandria Hotel

Alexandria, Virginia
October 1517, 2012
National Honey Bee Health Stakeholder Conference Steering Committee
USDA Office of Pest Management Policy (OPMP)

David Epstein
Pennsylvania State University, Department of Entomology

James L. Frazier
USDA National Institute of Food and Agriculture (NIFA)

USDA Agricultural Research Service (ARS)

Kevin Hackett
USDA Animal and Plant Health and Inspection Service (APHIS)

Robyn Rose
USDA Natural Resources Conservation Service (NRCS)

Terrell Erickson
U. S. Environmental Protection Agency (EPA) Office of Pesticide Programs (OPP)

Thomas Moriarty
Thomas Steeger
ii
Disclaimer:
This is a report presenting the proceedings of a stakeholder conference organized

and conducted by members of the National Honey Bee Health Stakeholder
Conference Steering Committee on October 15-17, 2012 in Alexandria, VA. The
views expressed in this report are those of the presenters and participants and do
not necessarily represent the policies or positions of the Department of Agriculture
(USDA), the Environmental Protection Agency (EPA), or the United States
Government (USG).
iii
Executive Summary
After news broke in November 2006 about Colony Collapse Disorder (CCD), a
potentially new phenomenon described by sudden and widespread disappearances of
adult honey bees from beehives in the U.S., the CCD Steering Committee was formed
with the charge to help coordinate a federal response to address this problem. The CCD
Steering Committee consists of scientists from the Department of Agricultures (USDA)
Agricultural Research Service (ARS), National Institute of Food and Agriculture (NIFA),
Animal Plant Health Inspection Service (APHIS), Natural Resources Conservation
Service (NRCS), Office of Pest Management Policy (OPMP), the National Agricultural
Statistics Service (NASS), and also includes scientists from the Environmental Protection
Agency (EPA). At that time, the Committee requested input and recommendations from
a broad range of experts in apiculture about how to approach the problem. Out of this,
the steering committee developed the CCD Action Plan
(www.ars.usda.gov/is/br/ccd/ccd_actionplan.pdf), which outlined the main priorities for
research and outreach to be conducted to characterize CCD and to develop measures to
mitigate the problem. Since formation of the CCD Steering Committee early in 2007, the
USDA, EPA and public and private partners have invested considerable resources to
better address CCD and other major factors adversely affecting bee health.
Despite a remarkably intensive level of research effort towards understanding causes of

managed honeybee colony losses in the United States, overall losses continue to be high
and pose a serious threat to meeting the pollination service demands for several
commercial crops. Best Management Practice (BMP) guides have been developed for
multiple stakeholders, but there are numerous obstacles to widespread adoption of these
practices. In addition, the needs of growers and other stakeholders must be taken into
consideration before many practices can be implemented.
To address these needs, several individuals from the CCD Steering Committee, along
with Pennsylvania State University, organized and convened a conference on October 1517, 2012, in Alexandria, Virginia that brought together stakeholders with expertise in
iv
honey bee health. Approximately 175 individuals participated, including beekeepers,

scientists from industry/academia/government, representatives of conservation groups,
beekeeping supply manufacturers, commodity groups, pesticide manufacturers, and
government representatives from the U.S., Canada, and Europe.
A primary goal of the conference was for the CCD Steering Committee to receive input
from stakeholders as they consider future actions to promote health and mitigate risks to
managed honey bees in the United States. The meeting had three objectives:
1) Synthesize the current state of knowledge regarding CCD, bee pests, pathogens, and
nutrition, potential pesticide effects on bees, and bee biology, genetics and breeding; 2)
Facilitate the development and implementation of BMPs that stakeholders can
realistically incorporate; and 3) Identify priority topics for research, education and
outreach to be considered by the CCD Steering Committee for an updated Action Plan.
Dr. May Berenbaum gave the keynote address and provided an overview of the historical
and current state of pollinators in the United States, from the invention of the first
movable hive frame in 1852 and the first printed reference to non-target impacts of
agricultural pesticides on bees in 1891, through the first U.S. detection of the parasitic
Varroa mite in 1987 and the more recent colony declines over the past decade. Leaders
in apicultural research gave comprehensive presentations of research progress on CCD,
bee pests and pathogens, nutrition, pesticides, bee biology, breeding and genetics.
Highlights of Research Overviews: As noted earlier, the views expressed in this report
are those of the presenters and do not necessarily represent the policies or positions of
the U.S. Department of Agriculture, the Environmental Protection Agency, or the United
States Government.
Consensus is building that a complex set of stressors and pathogens is associated

with CCD, and researchers are increasingly using multi-factorial approaches to
studying causes of colony losses.
The parasitic mite Varroa destructor remains the single most detrimental pest of
honey bees, and is closely associated with overwintering colony declines.
Multiple virus species have been associated with CCD.
Varroa is known to cause amplified levels of viruses.
The bacterial disease European foulbrood is being detected more often in the U.S.
and may be linked to colony loss.
Nutrition has a major impact on individual bee and colony longevity.
Research indicates that gut microbes associated with honey bees play key roles in
enhancement of nutrition, detoxification of chemicals, and protection against
diseases.
Acute and sublethal effects of pesticides on honey bees have been increasingly
documented, and are a primary concern. Further tier 2 (semi-field conditions) and
tier 3 (field conditions) research is required to establish the risks associated with
pesticide exposure to U.S. honey bee declines in general.
The most pressing pesticide research questions lie in determining the actual fieldrelevant pesticide exposure bees receive and the effects of pervasive exposure to
multiple pesticides on bee health and productivity of whole honey bee colonies.
Long-term cryopreservation of honey bee semen has been successfully developed

and provides the means for long-term preservation of top-tier domestic honey
bee germplasm for breeding. Genetic variation improves bee thermoregulation,
disease resistance and worker productivity.
Genomic insights from sequencing the honey bee genome are now widely used to
understand and address major questions of breeding, parasite interactions, novel
controls (e.g., RNAi), and management to make bees less stressed and more
productive.
To facilitate discussion of BMPs and development of priorities, stakeholders were formed

into work groups centered on the four main issues affecting bee health: 1) nutrition, 2)
pesticides, 3) parasites/pathogens and 4) genetics/ biology/ breeding. The most common
themes expressed in several breakout groups were:
vi
Federal and state partners should consider actions affecting land management to
maximize available nutritional forage to promote and enhance good bee health and
to protect bees by mitigating their movement into pesticide-treated crop acreage.
Undernourished or malnourished bees appear to be more susceptible to pathogens,

parasites, and other stressors, including toxins. Research is needed on forage,
pollen, insect metabolic pathways, artificial and natural food sources, and food
processing and storage in the hive.
More outreach programs targeting farmers on managing potential exposure of

honey bees to pesticides is needed. Efforts would benefit from involvement of
beekeepers, crop consultants, pesticide manufacturers and applicators, and State
lead agencies and extension agents.
BMPs associated with bees and pesticide use, exist, but are not widely or
systematically implemented by members of the crop producing industry. A central
theme of the pesticides session was the need for informed and coordinated
communication/education/extension of growers and beekeepers and the need for
effective collaboration between stakeholders.
Beekeepers accentuated the need for accurate and timely beekill incident reporting,
monitoring, and enforcement.
Pathogens and arthropod pests have major negative impacts on colonies.

Management of Varroa and viruses was recognized as a special concern.
Breeding emphasis is on traits, including hygienic behavior, that confer improved

resistance to Varroa mites and diseases, such as American Foulbrood.
Although a post meeting survey was not conducted, meeting participants indicated that
the conference gave them the opportunity to voice their concerns, to hear the concerns of
others, and to offer their perspectives to Federal officials on future directions the
government might take to ensure the future of America's pollinators. The CCD Steering
Committee plans to revise the CCD Action Plan, a document that will synthesize this
input. The Action Plan will outline major priorities to be addressed in the next 5-10
years. This plan will serve as a reference document for policy makers, legislators and the
public and to help coordinate the federal strategy in response to honey bee losses. Finally,
vii
given the depth of issues effecting pollinator health, consideration should be given to
renaming this committee to reflect the broader range of factors discussed in this report.
viii
Table of Contents
National Honey Bee Stakeholder Conference Steering Committee Members ...ii
Disclaimer .. ............. iii
Executive Summary ...iv
Background ......................................................................................................................... 1
Conference Overview ......................................................................................................... 2
Conference Opening Remarks and Comments ................................................................... 4
Conference Research Presentations .................................................................................... 4
Current State of Knowledge of CCD and its Relation to Honey Bee Health ........... 5
Current State of Knowledge of Bee Biology............................................................ 7
Current State of Knowledge of Nutrition ............................................................... 10
Current State of Knowledge of Pathogens ............................................................. 12
Current State of Knowledge of Arthropod Pests .................................................... 15
Current State of Knowledge of Pesticides .............................................................. 16
Current State of Knowledge of Bee Genetics & Breeding ..................................... 20
Work Groups ..................................................................................................................... 22
Nutrition. 22
Pathogens and Arthropod Pests .............................................................................. 24
Pesticides .... 27
Bee Genetics, Breeding, and Biology 33
Conclusion . ...38
Acknowledgment .. ....38
Appendix 1: Conference Agenda ...................................................................................... 39
Appendix 2: Questions Developed For Work Group Discussions 42
Nutrition.. 42
Pathogens................................................................................................................ 42
Arthropods.. 43
Pesticides ................................................................................................................ 44
Genetics, Breeding & Biology ............................................................................... 46
ix
Appendix 3: Invited Work Group Participants ................................................................. 49

Nutrition.. 49
Pathogens / Arthropods .......................................................................................... 51
Pesticides ................................................................................................................ 53
Genetics, Breeding & Biology ............................................................................... 55
Appendix 4: Cited References for Biology Research Presentation .................................. 57
Appendix 5: Cited References for Pesticide Research Presentation ................................. 60
Appendix 6. Cited References for Biology, Genetics, Breeding Research Presentation...62
Background
In response to unexplained losses of U.S. honey bee (Apis mellifera) colonies that began to be
reported in 2006 as a condition named Colony Collapse Disorder (CCD), the U.S. Department of
Agriculture (USDA) established a Colony Collapse Steering Committee to lead an effort to
define an approach for understanding and resolving the problem. CCD is characterized by the
sudden loss of worker adults from managed hives, leading to the eventual collapse of the entire
colony within a few weeks. It is a complex phenomenon, because several factors seem to be
interacting to cause CCD (http://www.ars.usda.gov/is/br/ccd/ccdprogressreport2012.pdf) (CCD
Progress Report 2012). The suspected factors include pests, pathogens, pesticides, nutritional
deficiencies and bee hive management practices.
The CCD Steering Committee, formally
established in 2007, was initially composed of program leaders from ARS, NIFA, APHIS,
NRCS, and NASS, the U.S. Environmental Protection Agency Office of Pesticide Programs
(EPA) and two land-grant university administrators from Pennsylvania State University and
Purdue University. Using input and recommendations received by university and government
researchers, extension specialists and beekeepers, the steering committee developed the CCD
Action Plan in July 2007 to establish key priorities for research and development of management
practices to address CCD (http://www.ars.usda.gov/is/br/ccd/ccd actionplan.pdf). Currently, the
steering committee includes USDAs Office of Pest Management Policy (OPMP); formal
participation of the two land-grant universities ended.
In the past five years, significant progress has been made in our understanding of the factors that
are associated with CCD and the overall health of honey bees. Survey data generated by USDA
(http://www.ars.usda.gov/is/pr/2011/110523.htm) indicate that overwinter losses for commercial
beekeepers ranged from approximately 28 to 33 percent between 2007 and 2011 and were
reported as 22 percent in 2012. It was noted in 2010-11 winter loss survey that fewer beekeepers
attributed losses to CCD than in previous years (vanEngelsdorp et al. 2012), even though those
reporting CCD as the cause of their losses suffered higher than average losses. Nevertheless,
overall losses far exceed the historical rate (approximately 10 to 15 percent) and represent a
threat to both beekeepers and to those agricultural crops that rely upon pollination as a
production input. Since 2006 an estimated 10 million bee hives at an approximate current value
1
of $200 each have been lost and the total replacement cost of $2 billion dollars has been borne by
the beekeepers alone (J. Frazier, unpublished).
Members of the CCD Steering Committee believed that, after five years of investigating CCD, it
was necessary to assess the current state of knowledge of CCD, and of the primary factors that
affect honey bee health. To this end, a subcommittee formed to plan and conduct a stakeholder
conference, with the objective of seeking input from the stakeholder community regarding
current understanding of research priorities, and the development of BMPs to address the needs
of beekeepers and growers.
A stakeholder conference was held on October 15-17, 2012 in Alexandria, Virginia.

Approximately 150 individuals were invited to the conference, including beekeepers, scientists,
representatives of advocacy groups, beekeeping supply manufacturers, commodity groups,
pesticide producers, academia, and State and Federal government representatives from the U.S.,
Canada, and Europe. The meeting was planned, organized and conducted by representatives
from multiple agencies within the USDA and the U.S. EPA, along with Dr. James Frazier,
Pennsylvania State University.
Conference Overview:
The goal of the conference was for officials from USDA and U.S. EPA to receive input from
scientists, state governments, non-governmental organizations, industry and other stakeholders as
they consider future actions to promote health and mitigate risks to North Americas managed
honey bees. The meeting had four aims:
Synthesize the state of knowledge regarding CCD
Synthesize the current state of knowledge regarding each of the factors believed to be associated
with declines in
honey bee health
o Arthropod pests and pathogens
o Nutrition
o Pesticides
o Bee biology, genetics, and breeding
2
Discuss and identify priority topics for research and BMPs to be considered by the CCD
Steering Committee for action
The first day of the meeting was devoted to examining current and recent (past 5 years) research
on each of the above four factors known to affect honey bee health. Eleven researchers from
land-grant universities and the USDA Agricultural Research Service (ARS) presented research
summaries addressing each health-factor topic. On the second day of the conference, participants
were assigned to one of four work groups in which they were encouraged to discuss viewpoints
on one of the specific areas associated with honey bee health. Work group assignments were
based on participants knowledge in the topic area. Work group discussions were led by the
researchers, who presented the research summaries on day one, and were facilitated by USDA
and U.S. EPA personnel. The research leads, along with conference organizers, developed a set
of questions designed to guide discussion within each work group (Appendix 2).
Participants reconvened during the afternoon of the second day, when recorders from each work
group summarized the key questions and recommendations developed in the morning sessions. A
general discussion session followed, which ensured that participants could contribute additional
ideas to work groups other than to the one to which they had been assigned.
Day 1: Opening Remarks and Comments
USDA Deputy Secretary, Kathleen Merrigan, U.S. EPA Deputy Administrator, Bob Perciasepe,
and USDA National Institute of Food and Agriculture (NIFA) Director Sonny Ramaswamy each
provided opening remarks, addressing the importance of the issues to be discussed during the
conference, and commitments by both organizations to respond to the challenges of promoting
bee health while mitigating risk.
The following representatives of several stakeholder groups were also invited to provide opening
comments:
Darren Cox, Beekeeper Representative to the EPA Pesticide Program Dialogue

Committee; Cox Honeyland, Logan, Utah
Daniel Botts, Minor Crop Farmer Alliance and Florida Fruit & Vegetable Association,
Maitland, Florida
Dr. Gabrielle Ludwig, Senior Manager of Global, Technical and Regulatory Affairs,
Almond Board of California, Modesto, California
Dr. Barbara Glenn, Senior Vice President, Science and Regulatory Affairs, CropLife
America, Washington, District of Columbia
Laurie Davies Adams, Executive Director, North American Pollinator Protection

Campaign, San Francisco, California
Christi Heintz, Executive Director, Project Apis m., Tucson, Arizona
Day 1: Research Presentations: The keynote speaker was Dr. May Berenbaum of the
University of Illinois Urbana-Champaign, who provided a comprehensive overview of honey bee
declines. Berenbaums presentation included an overview of historical focus on the conduct of
honey bee research efforts, including challenges in experimental design and conduct yielding
relevant results regarding colony health.
Leading scientists who study honey bees were identified and selected by the conference steering
committee to present on a range of topics associated with honey bee health. Each presentation
was followed by an open forum, during which conference participants were encouraged to ask
4
questions or provide commentary. Comments recorded, below, in the research summaries do not
represent the expressed opinions of agencies or personnel of the USDA, the US EPA, or the U.S.
Government.
Current State of Knowledge of CCD and its Relation to Honey Bee Health
(Dr. Jeff Pettis, USDA ARS, Beltsville, Maryland; Dr. Dennis vanEngelsdorp, University of
Maryland, College Park, Maryland)
Summary of Research Presentation: No single silver bullet will solve the problems affecting
honey bees and other pollinators. Habitat enhancement, judicious and targeted pesticide use,
improved colony management techniques and improved disease and pest resistant stocks of bees
are collectively needed to improve the health of honey bee colonies. It is imperative that we
increase honey bee survival both to make beekeeping profitable but more importantly to meet the
demands of U.S. agriculture for pollination and thus ensure of food security.
Healthy honey bee colonies are critical for meeting the demands of food production in the
United States.
Currently, the survivorship of honey bee colonies is too low for us to be confident in our
ability to meet the pollination demands of U.S. agricultural crops.
Historically, the U.S. had as many as 6 million colonies in 1947, with declines since that
time to about 4 million in 1970 and 3 million in 1990. Todays colony strength is about
2.5 million.
Pollination demands have increased in recent years such that a single crop, almonds in
California, now require over 60 percent of all managed colonies.
Honey bee colonies have been dying at a rate of about 30 percent per year over the past
few winters which leave virtually no cushion of bees for pollination.
Because of the early almond pollination requirement, a 30 percent loss of the 2.5 million
colonies would leave only 1.75 million colonies to meet the 1.5 to 1.7 million colonies
currently needed in almonds. This situation leaves growers in a precarious position, and
Dr. Pettis stated, We are one poor weather event or high winter bee loss away from a
pollination disaster.
5
Surveys of beekeepers throughout the United States have documented this 30 percent or
greater loss for five consecutive years while for the most recent winter, 2011-2012, the
losses were only 22 percent.
While the lower level of loss for overwintering hives in 2011-2012 was encouraging, one year
does not make a trend and reports of losses in the latter part of 2012 look like we are in for
another high loss winter rate. We need to improve colony survivorship, however, honey bee
health issues, including CCD, have proven to be multi-faceted and difficult to solve.
Research into CCD and poor colony health has been unable to identify a unique causative
agent but consensus is building that a complex set of stressors and pathogens can result in
colony losses.
Factors that can lead to poor health include disease and arthropod pests, pesticides, poor
nutrition and beekeeping practices.
The parasitic mite Varroa destructor remains the single most detrimental pest of honey
bees and can magnify the role of viruses in bee health.
Pesticide exposure to pollinators continues to be an area of research and concern,

particularly the systemic pesticides such as neonicotinoids. Despite concerns regarding
the potential hazard that systemic pesticides may represent to honey bee colonies, when
pesticides are viewed in the aggregate at the national level, the frequency and quantity of
residues of pyrethroids coupled with the toxicity of these insecticides to bees could pose a
3-fold greater hazard to the colony than the systemic neonicotinoids.
Several studies have demonstrated that sublethal neonicotinoid exposure in immature bees
resulted in an increased susceptibility to the gut pathogen Nosema, demonstrating that
complex interaction between factors are likely contributing to poor colony health.
Nutrition has a major impact on individual and colony longevity. There is a belief among
beekeepers and researchers alike that land use patterns have changed to an extent where
there is less forage available for honey bee colonies. Research is beginning to look at ways
to diversify the agricultural landscape to increase resource availability for pollinators.
The use of modern weed control methods in agriculture, forestry and States Rights of
Way land management have reduced availability of weeds that once provided valuable
nutrition to bees.
6
Current State of Knowledge of Bee Biology

(Dr. Jay Evans, USDA ARS, Beltsville, Maryland)
Summary of Research Presentation: Research on honey bees involves several fields of

biology, and advances in these fields are just now having an impact on maintaining healthy
pollinator populations in the face of biotic and abiotic threats. New genetic and experimental
approaches to address pollinator health are in use.
A challenge to the research community is how do we weigh the relative importance of

behavioral and physiological traits on bee health?
o Understanding the relative importance of individual and social traits and the tradeoffs in terms of costs of maintaining these traits, will lead to better bee breeding and
management (Evans and Spivak, 2010)
o Pathogens and parasites of honey bees have been described in great detail, linking
important microbes with negative (Runckel et al., 2011; Cornman et al., 2012) and
positive (Anderson et al., 2011; Engel, Martinson, and Moran, 2012) effects on bee
health.
o The genetics behind individual bee responses to viruses, bacteria, and gut parasites
like Nosema (Siede, Meixner, and Bchler, 2012) and of how adult bees within the
hive respond to signs of disease among their nestmates (Oxley, Spivak, and Oldroyd,
2010) are becoming more clear.
o Evidence that infected honey bees may suicidally take risks that decrease chances
they will transmit disease to nestmates (Rueppell, Hayworth, and Ross, 2010) may
enable more efficient breeding programs aimed at producing disease resistant bees.
How signals shared among & between bees & their varied pests can be exploited to:
o Control pests, i.e., by understanding how Varroa mites, the primary pest of honey
bees worldwide, perceive vulnerable bees (Caldern et al., 2009) and the means by
which bees perceive and remove these mites (Harris, Danka, and Villa, 2012).
o Manipulate foraging and other colony traits by understanding how bee behavior
reflects the interplay between bee proteins, developmental stage, and environmental
cues. Planned research will be extended to find key traits involved with recognizing
and removing pests, such as hygienic behavior.
7
o Raise and maintain robust queens. For example, recent work describes how the
genome of developing queen and worker bees is altered during development,
revealing that a large number of genomic regions are silenced in developing bees
using methylation (Foret et al., 2012), a way of painting chromosomal regions into
silence or activity; previously thought to be of only minor importance for insects.
We need consistent protocols for bee research, from genetics to field experiments in order
to compare data on the impacts of parasites, pathogens, nutrition and chemicals on bee
health.
o A major effort is underway to increase common practices among bee scientists and to
disseminate scientific findings to the beekeeping world. The Beebook (Williams et
al., 2012) is a growing compendium of research protocols and insights that will
enable more consistent experiments aimed at understanding bee health and bee
biology. Information from the Beebook will be joined with the key venues for
dispersing honey bee information among stakeholders, regulators, and researchers,
including
the
USDA-funded
Extension.org
(http://www.extension.org/bee health),
the
site
Colony
for
Loss
bee
health
network
(http://www.coloss.org/) and the newly established Bee Informed Partnership

(http://beeinformed.org).
What is the current consensus on biological and abiological factors that act non-additively
to impact bee health, and how do we use this knowledge?
There is a huge shift towards multi-factorial studies in all fields of bee research. Studies of
bee biology and bee health have tended to focus on one factor (one genetic trait or one
environmental component) and the impacts of this factor on bee health. Recent work on
non-additive interactions between chemical insults to bees and parasites (e.g., Alaux et al.,
2010; Pettis et al., 2012), and on the interplay between nutrition and disease, exemplify
the benefits of looking at problems of bee health from the standpoint of multiple inputs.
Other examples include:
o The impacts of bee genetics and the environment on bee foraging (Ament et al., 2012;
Page Jr, Fondrk, and Rueppell, 2012)
o The effects of larvae and nurse bees on the development of new queens (Linksvayer
et al., 2011). This will lead to richer insights into bee biology and presumably new
ideas for the management and breeding of healthy bees.
The description of the Honey Bee Genome Project Honeybee Genome Sequencing
Consortium (2006) has become the most-cited research paper in honey bee biology.
Genomic insights are now widely used to understand and address the major questions of
breeding, vetting traits, parasite interactions, novel controls (RNAi), and management to
make bees less stressed and more productive.
o Scientists are using the power of genome-wide expression analysis to understand:
Bee responses to Varroa (Nazzi et al., 2012).
Bee responses to poor nutrition (Alaux et al., 2011).
Results from CCD-driven studies have changed dogma related to:

o The frequency with which bees are exposed to pathogens on flowers (Singh et al.,
2010).
o The global nature of bee parasites and pathogens (Fries, 2010).
o The physiological and behavioral toll of poor nutrition and exposure to chemicals
(Gregorc and Ellis, 2011; Gregorc et al., 2012; Henry et al., 2012).
Conclusions and Future Efforts: There remain many major knowledge gaps in bee
biology, including:
o Impacts of nutrition and food diversity on the longevity of queens and workers.
o Importance and maintenance of the microbiome within the bee digestive tract.
o Movement of parasites and pathogens across species and across continents.
o Impacts of human barriers to spread of disease agents, including trade regulation and
surveys.
o The causes and sustainable exploitation of what seems to be an immense genetic
diversity of traits related to both individual and colony-level disease resistance.
o The reasons behind what seem to be inconsistent, but important, bee losses due to
exposure to pesticides and other chemicals.
Current State of Knowledge of Nutrition and Best Management Practices

(Dr. Gloria DeGrandi-Hoffman, USDA ARS, Tucson, Arizona; and Dr. Nancy Moran, Yale
University, New Haven, Connecticut)
Summary of Research Presentation: A broad overview of recent honey bee nutrition research
was presented that spanned topics from the relationship between nutrition and colony survival to
the role of microbes in food processing, preservation and digestion of nutrients. Comprehensive
investigation into the role of nutrition in honey bee colony health has only recently begun at the
landscape, colony and molecular levels. A more in-depth understanding of the nutritional value
of pollen sources and the factors affecting nutrient acquisition will provide more accurate
assessments of the nutritional benefits of different pollen sources and artificial diets. We also
will be able to evaluate the effects of antibiotics and pesticides on colony growth and survival
from a nutritional perspective by determining their effects on nutrient acquisition and
metabolism. This work will complement the need for increased bee forage and the selection of
plants that would most benefit colony growth.
Specifically, the presentation included mathematical model predictions of nutrition effects on

worker longevity and the repercussions on colony growth, and vulnerability to loss from
parasites, such as Varroa mites. Information on the nutritional value of pollen and the changes in
protein and amino acid concentrations after conversion of pollen to bee bread (a mixture of plant
pollen, nectar, enzymes, bacteria and fungi used as food) also was provided. Recent studies have
revealed new understanding about the role of nutrients and importance of beneficial microbes on
honey bee health such as:
Nutritional stress on overwintering colonies reduces the lifespan of adult workers by four
days; from an average of 35 to 31 days.
Pollen is the key protein source and bee bread is the dominant amino acid source in honey
bee diets.
Studies from several research groups reveal a distinctive set of species of gut microbes
present in adult honey bees worldwide (Africa, Australia, Asia, North America, South
America, Europe)
o Eusociality enables efficient transmission of specialized bacterial communities.
10
o Eight distinctive microbial species make up 95 to 99 percent of gut bacteria in most

bees.
Possible roles of microbes in bee health:

o Biosynthesis of needed nutrients
o Enzymes for pollen digestion
o Detoxification of compounds in diet
o Protection against parasites or diseases (e.g., infection levels by Crithidia parasites)
depends on which strains of gut bacteria are present in the bee.
Bacterial species colonize specific regions of the adult honey bee gut.
Two primary bacterial microbes are present in worker bees and in highly specific gut
locations :
o Snodgrassella alvi
o Gilliamella apicola
Advances in genomics research are providing unprecedented opportunities to explore

diversity and function of gut microbiota. Examples of studies could include the following:
o Bacterial sampling directly from bees or from cultured bee bacteria
o Massive sequencing of microbial genomic DNA
o Bioinformatics using databases from model bacterial systems
o Predicting and validating functional capabilities of bacteria at the individual and
colony level.
Within a single bee, gut bacteria encode enzymes involved in the breakdown of dietary
components, transport of sugars and amino acids, and biosynthesis of nutrients (i.e. Some
strains of Gilliamella encode pectate lyase enzymes for breakdown of pectin, a major
component of pollen walls).
Antibiotic resistance genes have accumulated in bee gut bacteria in the U.S. due to history
of frequent use for public and agricultural treatments.
The presentation ended with specific questions that need to be addressed in future work.
o What is next and what else do we need to know about honey bee microbiota?
o What is the role of microbes in bee bread and honey in the hive?
o Do honey bee-associated bacteria help to protect against disease?
o What is the role of microbes in making nutrients or in utilizing dietary components?
11
o Can we promote beneficial microbes in the colonies by beekeeping practices?

o What are effects of antibiotic use and artificial diets on the composition and
functioning of bee microbiota, both within the gut and within the colony?
Current State of Knowledge of Pathogens and Best Management Practices

(Dr. Diana Cox-Foster, Pennsylvania State University, University Park, Pennsylvania; Dr. Jay
Evans, USDA ARS, Beltsville, Maryland)
Summary of Research Presentation: Greater information and knowledge about the normal
microflora and pathogens associated with honey bees have been revealed through next
generation sequencing and epidemiological studies and surveys. There is a dynamic ecology or
flux in pathogens over time within a colony and among colonies. While new species have been
discovered using metagenomics, and new pathologies have been described, including
melanization (chemical defense against invasion of internal tissues by pathogens) of bee organs
and brood pathologies such as snotty brood, careful experimentation is now needed to
associate novel bee health concerns with specific microbes.
Viruses:
o New virus species have been characterized in bees in the United States.
o Multiple virus species have been associated with CCD
o Closely related dicistroviruses most associated with the colonies include:
Israeli Acute Paralysis Virus
Kashmir Bee Virus
Acute Bee Paralysis Virus
No detection of slow bee paralysis virus in colonies in the U.S. to date
o Most predominant viruses in U.S. are Deformed Wing Virus and Black Queen
Cell Virus
o Varroa is the primary factor known to cause amplified levels of some bee viruses
o Other factors potentially affecting virus levels include:
Nutrition
Environmental chemicals (i.e. pesticides and in-hive miticides)

12
Other pathogens
Age of bees.
o Several questions exist concerning viruses
How do viruses kill bees and the colony?
How can viruses impact other aspects of colony health, such as behavior
(learning), chemical communication, and reproduction?
What impact do viruses have on the brood?
o Viral infections have also been detected in other hymenopteran pollinators and have
been shown to negatively impact alfalfa leaf cutting bees and bumble bees. This
raises the question whether the decline in native hymenopteran pollinators is a result
of viral infections, perhaps interacting with the same stress factors affecting honey
bees.
Bacterial:
o New information is available on variation among American foulbrood (Paenibacillus
larvae, the most widespread and destructive of honey bee brood diseases) strains and
the potential for these bacteria to interact with other gut microbes.
o Some American Foulbrood strains have developed antibiotic resistance.
o European foulbrood is being detected more often and may be linked to colony loss, in
contrast to its rare detection in the past years.
Fungi:
o Chalkbrood detected more often in colonies over the past decade.
o There are potentially other unknown fungal pathogens in bees, since characteristic
symptoms are observed in some autopsies of bees from collapsing colonies.
Microsporidia:
o Nosema ceranae widespread occurrence in U.S. colonies with some N. apis also
present.
Data support a shift in prevalence in species composition during the last 50 years
to favor N. ceranae over N. apis.
No widespread colony losses can be attributed to N. ceranae in the U.S.
Some colony losses may be associated with microsporidia since some beekeepers
that treated with fumagillin (which kills microsporidia and other fungi) have
13
reported fewer colony losses; although research data suggest that fumagillin may
actually stress bees resulting in poor colony health
New insights into N. ceranae biology and its association with bees have resulted
from several cage studies.
Nosema genome has been sequenced.
Nosema immunosuppresses honey bees.
Synergism between pesticide exposure and Nosema infections negatively

impacted bee health.
Nosema adversely impacts nutrient utilization.
o Nosema potentially interacts with other pathogens/parasites.
Understudied pathogens and parasites that merit more research:

o Crithidia mellificae, a trypanosome, is highly prevalent. Adverse effects by other
species of Crithidia are known in bumble bees, and it seems likely that C. mellificae
has negative effects on honey bees, at least in some circumstances.
o Spiroplasma bacteria also occur in bees; possible seasonal effects on bee health.
o Both positive and negative impacts of diverse digestive tract bacteria and other
microbes on bee and colony health.
Vigilance needed to prevent introduction of pests not yet detected in U.S.

o Slow Bee Paralysis Virus
o Varroa spp.
o New strains of Thai Sacbrood Virus
14
Current State of Knowledge of Arthropod Pests and Best Management Practices

(Dr. Dennis vanEngelsdorp, University of Maryland, College Park, Maryland; and Dr. Jeff
Pettis, USDA ARS, Beltsville, Maryland)
Summary of Research Presentation:
Arthropod Pests in Bees:

o Varroa mites (V. destructor)
Recognized as the major factor underlying colony loss in the U.S. and other
countries, but is not associated as a primary factor in colony collapse disorder in
the United States.
Immunosuppresses bees and vectors viruses that infect bees.
Has rapidly spread into Hawaiian honey bee colonies, despite the best efforts to
control its spread.
There is evidence for widespread resistance to the chemicals used to kill mites
(miticides), e.g., fluvalinate and coumaphos, and a need for development of new
effective treatments and alternative methods of mite control.
Other treatments that beekeepers have utilized do not appear to offer effective
control or may have limited use.
The miticide, amitraz, may provide limited control due to developing resistance
in Varroa, but data indicate that the amitraz formulation is important, as the
formulation used in crop-pest control has increased toxicity to bees as opposed to
the formulation intended for use in-hive (ApiVar).
The adoption of bee stocks with behavioral resistance to Varroa has not been
widely utilized.
New insights into Varroa may result from its genome having been sequenced
(Cornman, 2010).
o Tracheal mites (Acarapis woodi): Not widely detected nor regarded as a major factor
in U.S. colony loss.
o Small hive beetle can lead to increased colony loss via unknown mechanisms; use of
in-hive small hive beetle traps results in significantly lower colony loss.
15
o Africanized bees continue to spread in the U.S. and have been permanently
established in several states. To help impede additional spread, an improved
identification system for Africanized bees is needed along with best management
practices.
o Phorid flies are not considered to be a widespread problem or threat to colony health.
o Bee louse and wax moths are not of major concern at the current time.
Vigilance needed to prevent introduction of pests and other bees and wasps not yet
detected in U.S.
o Tropilaelaps spp. (T. clareae and T. koenigerum) parasitic mite (Asia)
o Other bee subspecies and species: A. mellifera capensis (southern Africa), A. ceranae
and A. florea
o The Asian predatory hornet Vespa velutina (Asia, Europe)
Current State of Knowledge of Pesticides and Best Management Practices

(Dr. Reed Johnson, Ohio State University, Columbus, Ohio; Dr. James Frazier, Pennsylvania
State University, University Park, Pennsylvania)
Summary of Research Presentation: There is broad consensus among all stakeholders that
pesticide use should not affect honey bees in such a way that 1. Honey production is reduced or
2. Pollination services provided by bees are threatened (Pesticide Risk Assessment for
Pollinators Executive Summary, SETAC, 2011). However, it is not clear, based on current
research, whether pesticide exposure is a major factor associated with U.S. honey bee health
declines in general, or specifically affects production of honey or delivery of pollination services.
It is clear, however, that in some instances honey bee colonies can be severely harmed by
exposure to high doses of insecticides when these compounds are used on crops, or via drift onto
flowers in areas adjacent to crops that are attractive to bees.
For example, dust produced in the process of planting pesticide-coated seeds has been
shown to contain high levels of insecticide with the potential to harm bees.
16
o Germany 2008: Seed treatment dust containing 12 to 28 percent clothianidin or

thiamethoxam (Pistorius et al., 2009, 10th Int. Symposium of the ICP-Bee Protection
Group)
U.S. 2010: Talc containing 0.3 to 1.5 percent clothianidin or thiamethoxam (Krupke et al.,
2012, PLoS ONE)
It is also clear, based on chemical analysis of bees and bee products, that exposure of bees to a
gamut of pesticides is commonplace, but the level of exposure to any particular pesticide is
generally not enough to immediately or acutely kill bees (Mullin et al, 2010).
Traditional laboratory-based acute toxicity testing on adult workers (Tier 1), which
determines LD50 or LC50 values, is required for registration of all pesticide testing.
Acute toxicity testing does not test for effects beyond acute mortality and cannot detect
any harm caused by pesticides that do not cause lethal effects, such as fungicides and
herbicides.
Acute toxicity testing cannot address sub-lethal insecticide effects on bees at levels too
low to kill outright.
o It is relatively straightforward to determine the level of pesticides contaminating both
beehives and the environment. The most pressing research questions lie in
determining the true pesticide exposure that bees receive and the effect, if any, that
pervasive exposure to multiple pesticides have on the health and productivity of
whole honey bee colonies. Determining the actual dose of pesticide that bees receive
in ecologically relevant situations will help connect laboratory-based experiments
using individual bees or bee tissues to expected pesticide effects in whole colonies.
How are pesticides transferred to bees and exchanged between bees?
o How do pesticides move within bees and the bee hive and how are these compounds
metabolized and excreted by bees and bee colonies?
o Which molecular receptors inside bees interact with pesticides?
Can sublethal tests at the individual level predict effects on whole colonies?
o Drones: Sperm number and viability/Longevity
o Workers: Foraging success/Longevity
17
o Queens: Egg laying rate/Egg hatch/Longevity
Many recent studies assessing sublethal effects in individual workers:

o Proboscis Extension Assay (learning) (Ciarlo et al., 2012)
o Waggle dance behavior (Nieh et al., 2012, J. Exp. Biol)
o Sucrose responsiveness (Nieh et al., 2012, J. Exp. Biol)
o Mobility (Teeters et al., 2012, Env. Tox. Chem.)
o Foraging behavior - Short-term (3 hour) effects of neonicotinoids (Schneider et al.,
2012, PLoS ONE)
o Forager loss - Henry et al., 2012, Science; Predict effects of forager loss on colony
growth using a demographic model (Khoury et al., 2011, PLoS ONE)
Laboratory tests on individual honey bees have shown that field-relevant, sublethal doses of
some pesticides have effects on bee behavior and susceptibility to disease. However, it remains
a challenge to measure the effects of low-level, field-relevant exposure where it matters most: in
real honey bee colonies. The social complexity of honey bees and the uncontrollable aspects of
field research present substantial challenges to determining pesticide effects in whole-colonies.
While experiments using whole colonies have the potential to directly address the effects of
pesticides on honey production and pollination services, challenges presented by field or semifield experiments include:
Many colonies are needed per treatment due to high variability between honey bee
colonies.
The actual levels of exposure to pesticides that bees receive are still a big question.
Computer modeling of colony demographics following pesticide exposure shows promise in

linking the results of laboratory-based pesticide studies with pesticide effects on whole-colony
health.
However, model predictions depend on the parameters used (Cresswell and Thompson,
2012, Science)
Studies in progress seek to address this concern (Zhu et al. 2012 unpublished); model
includes analyses of:
o Food collection: number of foragers/food storagers
o Queen egg-laying: queen fitness, brood care, available cells
18
o Brood: egg input, development

o Good hygiene
o Food storage: pollen, honey
An improved understanding of the physiological basis of pesticide toxicity in honey bees could
lead to an understanding of the toxicity of pesticide mixtures and the potential interactions
between pesticides and pathogens, nutrition and genetics.
Interactions to be studied:
o Pesticide-pesticide combinations are likely (Mullin et al., 2010, PLoS ONE)
Average of 7.1 pesticides in pollen
Average of 2.5 pesticides in bees
o Pesticide combinations can be more (or less) toxic (Johnson et al., 2013, PLoS
ONE) need further research
o Additive (pesticide 1 + pesticide 2)
o Synergistic (pesticide 1 x pesticide 2)
o Antagonistic (pesticide 1 pesticide 2)
o Miticide-drug interactions Oxy-tetracycline, tau-fluvalinate (Hawthorne and
Dively, 2012, PLoS ONE, multi-drug resistance transporters )
o Many
potential
interactions
remain
to
be
explored:
Pesticide-
food/disease/season/temperature/age/genetics/management
How can we better address the effects of pesticides on pollination and honey production?
o Management
Improve communication between stakeholders
Further development of BMPs needed
Provide alternate forage
o Continuing research being done:
Ecologically relevant dose
Modeling colonies
Sublethal effects
Interactions
19
Current State of Knowledge of Bee Genetics, Breeding, and Best Management Practices
(Dr. Marla Spivak, University of Minnesota, St. Paul, Minnesota; and Dr. W. Steve Sheppard,
Washington State University, Pullman, Washington)
Summary of Research Presentation
Historical pattern of honey bee introductions to the New World primarily occurred
between 1622 and 1922. Eight Old World subspecies were introduced, including several
from Africa, the Middle East and Europe. Only three European strains found favor with
U.S. beekeepers: Italian, Carniolan, and Caucasian.
Genetic diversity is critical to honey bees colonies

o At the intra-colony level: genetic variation improves thermoregulation, disease
resistance, worker productivity, i.e., related to colony health
o At the population level: U.S. honey bees show effects of multiple bottlenecks
Initial introductions of limited numbers of queens, queen production methods

(One million queens produced from less than 600 mother queens),
highly restricted importation of new breeding germplasm since 1922
Introduction of novel Old World genetic stock for breeding

o USDA importation, selection and distribution of new stock (Russian Honey Bees)
o WSU importation, selection and distribution of honey bee germplasm (semen) from
original sources for three favored U.S. strains (Italian, Carniolan and Caucasian)
o Recent development of practical means for long term storage (cryopreservation)
provides means to store top-tier domestic honey bee germplasm for breeding use
through time and space and to conserve germplasm collected from original source
populations in Europe
Bee Breeding Cultural Shift

o Growing interest to produce locally, regionally adapted strains of honey bees through
small scale queen production
o Driven in part by interest to breed bees more tolerant of mites and resistant to
diseases and to reduce the amount of in-hive chemical inputs (miticides, antibiotics)
needed to maintain healthy bees
Tech Transfer Teams

20
o Assist the bee breeding industry incorporate objective selection-trait criteria in

breeding
o Help implement scientific and technological advances to enhance sustainability and
profitability
Future of Bee Breeding

o Marker-assisted selection (i.e., selection of bees that posses genetic markers for
desired traits).
o Field assays for Varroa Sensitive Hygiene (VSH, a selectable trait whereby bees
detect Varroa infested brood in capped cells and remove infested bee pupae,
disrupting the mites reproductive cycle) and other traits.
o Increased baseline genetic diversity for trait selection.
21
Work Groups
On the second day of the conference, invited participants were assigned to one of four work
groups and invited to address questions developed by the Steering Committee and openly discuss
facts, experiences, and viewpoints on one of the areas associated with honey bee health
(Appendix 3). The sections that follow contain a summary of those work group discussions. As
noted earlier, the views expressed in this report are those of the presenters and do not
necessarily represent the policies or positions of the U.S. Department of Agriculture, the
Environmental Protection Agency or the United States Government.
Nutrition
The nutrition work group was chaired by Dr. Gloria DeGrandi-Hoffman (USDA ARS, Tucson,
Arizona), and Dr. Nancy Moran (Yale University, New Haven, Connecticut). Dr. Mary PurcellMiramontes (USDA NIFA) and Dr. Terrell Erickson (USDA NRCS) facilitated the discussion.
Questions developed to guide the discussion (Appendix 2) probed the nutritional composition of
pollen before and after it is converted to bee bread and the contributions of beneficial microbes
in metabolism, and food processing and storage for the hive. The discussion among stakeholders
in the nutrition working group, though, primarily revolved around the shortage of high-quality
forage for bees in the form of flowering plants, spatially and temporally. It was noted that
availability of open foraging areas has declined drastically in the last few years, due to land use
changes driven, in part, by economic and agricultural developments such as increased planting of
row crops, such as corn, as commodity prices have risen, and in sites that formerly were
undisturbed.
Although the purpose of this workgroup was not to recommend policies, some participants
expressed the need for a land use policy that provides pesticide-free areas with blooming plants
where beekeepers can safely place colonies. The primary point of this discussion was that
beekeepers need access to more high-quality forage. Because of year-to-year weather
fluctuations, forage areas should span a variety of regions and land types, particularly as parallels
typical beekeeper migratory routes. For example, a drought in one part of the country can
22
drastically reduce the availability and quality of forage plants, and beekeepers need alternative
sites and plants to cope with these fluctuations. Although diet supplements are essential for
large-scale beekeepers, they are only a temporary substitute for high-quality floral resources.
Therefore, good bee nutrition depends on how land around colonies is managed, and what
flowers are available to bees.
The availability of diverse and nutritional forage was noted as being particularly important for
building colony populations prior to and throughout pollination (especially of almonds) and
afterward, because colonies need to recover from stresses associated with transport. Beekeepers
remarked that colonies with access to good floral resources were generally healthier than those
located where few floral resources exist (i.e. sites dominated by row crops) and fed dietary
supplements. Undernourished or malnourished bees appear to be more susceptible to pathogens,
parasites, and other stressors including toxins. Thus, nutrition might be a fundamental factor in
mitigating negative effects of other stress factors on bee health. Issues related to Federal and
State land management agencies, as well as policies or programs that affect land use and
maintenance (such as The National Management Plan for Invasive Species), may be important
considerations to bear on the issue of alternative forage.
It was apparent during the work group discussion that these are complex issues that will require
the involvement of multiple agencies and individuals. Forage areas are impacted by various
Federal and State agencies, individual landowners and growers. Management of these lands
affects not only beekeepers, but also other interest groups, including environmentalists and
sportsmen. There appeared to be wide agreement that solid research on the factors determining
good bee nutrition will be an essential element for informing these decisions.
Questions and recommendations generated by stakeholders included the following:
How much natural (or relatively unmanaged) forage is needed to support honey bees so
that hives can produce surplus honey and provide vital pollination services?
What are the benefits to agriculture (measured in increased yield) of having colonies near
crops (such as soybeans and other crops not contracting for pollination services) if
23
increases in yield are realized, would this affect the attitudes and practices of growers in
taking steps to mitigate potential risks to bee colonies in or near their fields?
How do particular land management practices, from right of way management to existing
and potential NRCS programming, or seed mixes affect bee nutrition and movement into
adjacent cropping systems?
Farm Services Agency Conservation Reserve Program Managers: Should Conservation

Reserve Program consider alternatives to expensive seed mixes currently promoted (such
as prairie grass/wildflower), toward less expensive mixes with legumes, which may give
growers a greater incentive? Alfalfa could serve as a cheaper way of providing pollinator
habitat. Development of a cost benefit analysis related to seed mixes used on Farm
Services Agency Conservation Reserve Program Lands may provide insight on possible
seed mix alternatives for these scenarios.
How do particular supplements or other bee management practices affect nutrition?

Stakeholders stated a need to understand how bee-associated microbes play a role in the
nutrition of bees, potentially enabling them to make better use of particular foods.
Pathogens and Arthropod Pests

Dr. Dennis vanEngelsdorp (University of Maryland, College Park, Maryland), Dr. Diana CoxFoster (Pennsylvania State University, University Park, Pennsylvania), and Dr. Jay Evans
(USDA ARS, Beltsville, Maryland) chaired discussion in the work group. Dr. Kevin Hackett
(USDA ARS) and Dr. Robyn Rose (USDA APHIS) acted as facilitators.
There was general agreement that each question posed to guide the discussion (Appendix 2)
regarding pathogens of honey bees was relevant, and further research is needed to develop
solutions, but that some arthropod pests, such as small hive beetle, phorid flies, wax moth, and
the bee louse, have less impact on colony health, and do not warrant increased research at this
time. The group further agreed that additional information is needed about the biology of several
pathogens and arthropod pests in order to develop new approaches to safeguarding honey bee
health.
In addition, the group recognized that new approaches to disease prevention and
pathogen /arthropod pest introduction are urgently needed. Efforts toward research on disease
24
prevention should progress with as much synergism and coordination with international
researchers and regulators as possible. These recommendations are summarized below.
Biology of Pathogen and Arthropod Pests Research Needs:
Develop a better understanding of interactions between honey bee symbionts, associated

bee pathogens and arthropod pests.
Pathogen and arthropod pests having major impact are in need of additional research, with
Varroa being recognized of special concern, especially in association with viral diseases.
Interaction of gut microbiome with immune systems in determining the outcome of

pathogen infections needs to be better understood.
Determine the mechanisms of pathogen and arthropod pest resistance to control tactics.
Determine the basis for tolerance/resistance by the bees to the pathogens and arthropod
pests.
Determine the effects of different stresses (pesticides, nutrition, and climate) on disease
biology in honey bees.
Determine the role of arthropod pests in vectoring disease pathogens.
New approaches to disease prevention and pathogen/arthropod introduction
Create a Diagnostics Decision Tree for disease diagnosis in honey bee colonies.
Define the disease symptoms and develop a computerized diagnosis system that might be
delivered as a smart phone app for use by beekeepers.
Characterize symptoms of atypical death so it is immediately recognized and noted.
Develop a standardized sampling method for different disease/arthropod pest symptoms
Develop standardized diagnostics that have rapid turn-around.
Create a centralized lab for diagnosis of samples submitted by beekeepers, researchers,

and regulators.
Develop methods to identify rogue variants or new virulent strains of pathogens/arthropod

pests to allow for their rapid identification and response (see below).
25
Management strategies for control of pathogens and arthropods Research/Extension

Needs:
Integrate disease surveys with surveys of management practices (i.e. Bee Informed
survey).
Improve integrated management tools (e.g., monitoring tools) for pathogen and arthropod
pest management.
Develop new control measures for pathogens and arthropod pests, including new chemical
approaches, traps, biocontrol, etc.
Monitor for resistance in both arthropod and pathogen pests.
Tailor approaches suitable for backyard bee keepers versus commercial operations.
Develop novel dissemination tools (e.g., smartphone apps).

Surveillance Research/Extension Needs:
Link and sustain different efforts that monitor bee health over time. Develop sampling
methods of surveillance data to associate pest or pathogen levels with economic thresholds
for bee colonies under different environmental regions of the U.S.
Document, via surveys, as many pathogens and arthropod pests as possible, with
integration of other data, such as: management strategies and control measures, nutritional
state, pollen sources, crop / pesticide use in area, and climatic conditions.
Determine what time of year works best for surveys, ideally having more than one
survey/yr.
Use the survey data to develop prediction models of bee mortality.
Develop targeted surveys, including ports of entry with establishment of surveillance

apiaries and swarm capture systems, for early detection of new arthropod and pathogen
pests.
Monitor for resistance to treatments in arthropod and pathogen pests.
Develop a rapid response network for new pathogen and arthropod pest threats
Establish risk assessment methodologies for all known pathogen and arthropod pests.
26
Create a national committee that can more rapidly respond and have the authority to carry
out actions to protect honey bee colonies and the pollination industry.
A response plan is needed that may include quarantines for newly introduced exotic pests
(e.g., Tropilaelaps) and/or BMPs that may include destruction of infected/infested
apiaries. A participant stated that it is essential that the plan include guaranteed measures
for the financial compensation of beekeepers and efforts to restock their apiaries with
clean colonies.
Synergize with similar efforts being done internationally to address bee health issues in
both research and regulation arenas.
Pesticides
Dr. Reed Johnson (Ohio State University, Columbus, Ohio) chaired discussion in the pesticides
work group with facilitation provided by Dr. Tom Steeger and Tom Moriarty (U.S. EPA,
Washington, District of Columbia) and Terry Anderson (Consultant, ARS, Beltsville, Maryland).
A central theme throughout the work group session was the need for informed and coordinated
communication/education/extension of growers and beekeepers and the need for effective
collaboration between stakeholders.
(Pesticide Work Group Discussion Questions are in Appendix 2)
Best Management Practices
Beekeepers noted that moving colonies, placed in or near crops prior to pesticide
application can reduce the negative effects of pesticides to colonies; however, depending
on the season, it can be difficult to move colonies of differing sizes/weights and it can be
difficult to locate suitable places to which to move the colonies.
Altering colony locations can result in reduced homing success by forager bees.
Commodity group representatives noted that some growers dont require pollination
services and that a knowledge gap exists between growers who need to treat pests quickly
on a non-commercially pollinated crop and the potential presence of bees in the vicinity of
these fields.
27
Drift-Watch (http://www.driftwatch.org; recently renamed as FieldWatch), a webbased tool to help identify where and when pesticide spray operations are occurring, and
the process of registering the location of beehives were discussed as ways of identifying
apiary locations and promoting communication with growers. However, it was noted that
in certain existing state pesticide regulation programs that do use registries (such as Drift
Watch) notification (of beekeepers) is recommended 48 hours prior to application, which
may not provide enough time to move colonies.
Another concern expressed is that beekeepers on contract to one grower may not be
protected by pesticide applications to crops in adjacent fields. Beekeepers may receive
notification from the adjacent grower, but the beekeepers may not be able to relocate their
colonies because of their contract to provide pollination services.
The use of repellents to deter bees from foraging in crop areas treated with pesticides was
discussed. Some research has been done in the area of repellants, but participants stated
more research is needed.
Beekeepers expressed concern about hive placement in relation to needs of sufficient

water and floral sources.
o Supplemental diets (sugar/pollen/pollen substitutes) and supplemental water are
potential means of providing uncontaminated sources of nutrition and water for bees.
o Beekeepers reiterated the need to develop appropriate forage areas for bees.
Night application was identified as a potential option for growers to reduce the risk of bee
exposure to pesticides.
o Better communication/education on proper application procedures could serve as an
incentive for growers to apply pesticides with short residual toxicity at night.
o Beekeepers also are doubtful that nighttime application of fungicides is an effective
risk mitigation measure for honey bees.
Some beekeepers raised concern that fungicides dont contain pollinator language on their
labels, resulting in growers and beekeepers being uninformed about potential effects on
bees.
One participant suggested that education/mitigation efforts might focus on specific crops
that pose the greatest risk to pollinators, although identifying particular crops as
problematic may create divisions with growers who rent land to beekeepers.
28
Participants recommended providing pesticide residual toxicity (RT25 , the time required
for 25 percent bee mortality based on the test bee population exposed to the formulated
pesticide product applied to foliage) data as a label advisory to improve pollinator
protection.
Bee safe labeling (i.e., applying a bee friendly logo to certain product), which has
been successfully instituted in France, was mentioned as a possible incentive for industry.
One participant noted that when EPAs registration process includes uncertainties (e.g.
regarding potential effects), the burdens of which are unfairly born by the public. EPA
therefore, should better account for potential risks before registering a pesticide. The
participant also commented that EPA should have a better understanding of beekills;
however, beekills often go unreported by beekeepers. (EPA is currently developing
guidance to better standardize beekill investigations).
Communication/Education
Extension information such as the Bee Informed Partnership (http://beeinformed.org/),

which uses survey information collected directly from beekeepers, continue to be
developed.
There was a general sense that universities are developing materials on BMPs and
pollinator protection; however, these materials may not be adequately distributed.
A representative of Health Canadas Pest Management Regulatory Agency (PMRA)

described the process in which apiarists are assigned to each Province to work
collaboratively with provincial departments of agriculture, grower groups, apiarists, and
beekeepers in Canada.
o Crop guidance documents prepared by provinces have pollinator information that is
informed by PMRA risk assessments.
o Beekeepers contact provincial officials to report beekill incidents and to obtain
additional information; however, they do not report these incidents directly to federal
officials.
Commodity group representatives in the U.S. indicated that crop advisors are reliable
sources of information. Commodity group representatives also noted that:
29
o U.S. growers may not be aware of the affects their activities may have on bees, and
stated that most growers would willingly act to protect bees, if provided the proper
education.
o Commenting on the fact that relationships are often at the base of rural agriculture,
growers report a range of experiences when working with beekeepers.
o Many growers are unaware of potential risks associated with the newer pesticide
chemistries, particularly newer compounds such as the neonicotinoids that were
promoted as reduced-risk (e.g.., overall lower impact on human health and the
environment) after passage of the Food Quality Protection Act (1996).
o Growers/applicators may not be reading labels, and their primary information for
pesticide comes verbally from crop advisors, who may not be well-informed of the
potential effects of newer chemistries on bees.
It was suggested that communications between growers and their crop advisors should
include information-sharing with beekeepers, current examples include:
o Industry organizations, such as CropLife America and Responsible Industry for a
Sound Environment (RISE, an affiliate of CropLife America working in urban
environments), have included sessions on pollinator issues in annual meetings with
their constituents.
o The California Department of Pesticide Regulation has initiated efforts to have
pollinator protection-related materials included in Pest Control Advisor certification
course work.
o Crop advisors recognize the limited time growers may have to discuss treatment
options, and so discussions and, meetings are frequently conducted at edge of field.
Situations such as this highlight the dynamic and sometimes difficulty in consulting
with beekeepers prior to pesticide application.
Web tools were mentioned as a means of distributing regionally specific information.
Integrated pest management centers were also identified as sources of information about
alternatives to pesticides?
Leaflets developed by the French Ministry of Agriculture to describe their registration

process were discussed as an example of how certain types of management information
can be distributed.
30
Beekeepers suggested that they have good relationships with growers and extension
agents; subscribe to various list serves to obtain crop-specific information to stay abreast
of emerging treatment options they may face when their colonies are in close proximity to
these crops.
Participants indicated the need for improving the knowledge of crop advisors in bee
protection practices, as well as crop protection practices.
Webinars, blogs, list serves, social media (e.g., Twitter, Facebook) and commodityspecific newsletters, especially for crops not commercially pollinated (e.g., grains), were
discussed as a means of distributing information.
Regulatory
The importance of beekill reports and how they inform pesticide risk assessments was
discussed.
Accurate and timely beekill incident reporting, monitoring, and enforcement were
identified as important.
o Some beekeepers have been reluctant to report incidents for fear of damaging
relationships with growers on whom they depend for pollination service contracts or
honey production.
o Concerns were expressed regarding beekeeper fear of retribution and/or distrust of
government agencies they fear may cite them for illegal pesticide use for treatment of
in-hive pests.
Funding limitations have resulted in many States eliminating apiary inspectors and have
also reduced extension efforts.
Funding limitations have resulted in many States eliminating apiary inspectors and have
also reduced extension efforts. This reduction in resources has led to loss of expert
knowledge, thereby resulting in gaps in communication between beekeepers and growers.
Stakeholders identified the need for a national coordinator that, among other things, would
facilitate the dissemination of information to and between parties.
31
Research Needs/Funding
Research funded by commodity groups may yield information that is not widely
disseminated beyond specific, and often poorly attended, commodity group meetings.
Beekeepers noted the need for suitable forage areas to protect bees from pesticides.
o Minimizing bee movement from bee yards into pesticide-treated crop land with use of
forage plantings preferred by bees research into size and composition of plantings.
o Rights-of-way management that provides beneficial pollinator habitat moves away
from use of herbicides.
o Land managers expressed concerns that invasive weed control efforts may be
reducing the amount and diversity of available pollinator forage areas, particularly as
associated with Rights-of-Way management.
Stakeholders noted the need to identify drivers that make a difference in risk
management/assessment; these may best be identified though the use of some of the
forecasting models that have been developed with specific measurement end points that
have the greatest effect on colony survival.
Concern was expressed that land-grant scientists do not have incentives to engage in
applied research that does not contribute to tenure/publications. Participants stated that
such incentives should be increased to encourage researchers to further develop practices
that mitigate the risk of bees to pesticide exposure.
Funding mechanisms need to be identified that may allow government and university
researchers to seek funds provided through industry/commodity groups without
appearance of undue influence (e.g., possible use of 501c (3) organizations).
o University researchers reported reluctance in accepting any money from industry
because outside observers may question whether the resulting research was biased.
Credibility issues were identified with industry-funded research supporting pesticide

registration.
o An opinion was expressed that the EPA Federal Insecticide, Fungicide, and
Rodenticide Act (FIFRA) Scientific Advisory Panel selection process is biased by
avoiding any associations with industry
32
o EPA personnel noted that under the FIFRA, the regulated community is required to
provide data to support the registration of pesticides and that this burden for
generating such data does not fall on taxpayers.
Participants stated there is a need for applied research in addition to basic research to
address some of the questions regarding BMP development and efficacy evaluations.
Bee Genetics, Breeding, and Biology

The bee genetics, breeding, and biology work group discussion group was chaired by Dr. Marla
Spivak (University of Minnesota, St. Paul, Minnesota) and Dr. W. Steve Sheppard (Washington
State University, Pullman, Washington), and facilitated by Dr. David Epstein (USDA OPMP,
Washington, District of Columbia).
(Genetics/Breeding/Biology Work Group Questions in Appendix 2)
At the outset, the work group participants noted that long-term, sustainable solutions for honey
bee health and productivity issues would most likely derive from selective breeding and genetic
improvement of honey bees. A strong and healthy population of managed honey bees is required
to provide pollination services for the agricultural sector, an activity critical to U.S. food
security.
Breeding Populations: Honey bees are not native to North America, and our current managed
honey bee population reflects the genetic consequences of historical introductions that included
representatives from only 25 percent of the described honey bee subspecies in the Old World.
Recent research indicates that North American honey bees show evidence of admixture among
some of the subspecies sampled in these early introductions, a feature that may have helped U.S.
honey bees avoid inbreeding-related problems (Delaney et al. 2009, Harpur et al. 2012,
Sheppard 1989). As is typical with other agricultural animals and crops with Old World origins,
sources of novel germplasm and genetic diversity for long-term breeding efforts can be secured
through importation, quarantine, and screening of genetic material from areas of original
distribution.
33
Breeding Tools/Trait Selection:
Emphasis is on selection for increased hygienic behavior in commercial strains of bees.

o Colonies expressing high levels of hygienic behavior show improved resistance to
Varroa mites and diseases, such as American Foulbrood
Work group participants indicated that a number of additional traits would be useful to
include in breeding efforts and called for the development of both marker-assisted
selection and improved field assays for testing various traits.
The following traits were discussed; group consensus was that significant progress toward
incorporation of these traits in breeding efforts might be expected in the short term:
o Varroa-Sensitive Hygiene (VSH)
o Grooming Behavior (against Varroa mite): whereby mites are physically removed
from infested adult bees, or sometimes killed by chewing (highly expressed in the
species, A ceranae; original host of Varroa). Several labs are working on this trait;
progress has been made toward identifying genetic markers that may be used to assist
breeding.
o Chalkbrood resistance: Developing assays to select for resistance to this fungal
disease in honey bee populations would be useful.
Bee strains are available that express the above listed traits. However, participants
recommended that association studies between traits and genetic markers be conducted,
with the ultimate goal being marker-assisted selection. The rationale of this approach is
that the ability to select for desirable traits within current commercial queen producer
stocks would be most likely to engender acceptance among queen producers and also
permit the rapid dissemination of these traits into the wider U.S. honey bee population.
There was a general discussion of specific commercial strains of honey bees that have an
innate resistance to various parasitic mites, particularly the Russian honey bee,
originating in Russia and imported by the Baton Rouge Agricultural Research Service lab.
The consensus was that current commercial production of this strain (approximately 2,000
queens per year) was not likely to make a significant genetic impact on overall
commercial production of queens in the United States (approximately 1 million queens
annually). However, specific traits associated with this strain (mite tolerance) and with
USDA-developed VSH bees (mite resistance) are highly desirable and an effort should be
34
made to select for or otherwise incorporate similar traits within the U.S. breeding
population.
Germplasm Repository: The recent development and improvement of cryopreservation

methods for honey bee semen provides significant opportunities for honey bee breeders.
Workshop participants discussed the potential importance of establishing a honey bee
germplasm repository and supporting research on honey bee cryopreservation to evaluate
storage characteristics and limitations. Cryogenic reproductive technology is widely used
in breeding programs with a number of agricultural animals (e.g., turkeys, sheep, beef and
dairy cattle, and swine) and has been responsible for significant improvements in
measures of stock productivity where it has been introduced. Cryogenic preservation of
bee germplasm resources provides both a means to address conservation needs and
practical breeding goals.
A honey bee germplasm repository would serve as a place to maintain (for many years or
decades) novel honey bee germplasm of three subspecies (A. mellifera ligustica, A.
mellifera carnica, and A. mellifera caucasica) currently being imported from the Old
World under a permit granted by the Animal and Plant Health Inspection Service.
o At present, aliquots of this semen are being used to inseminate U.S. queen bees for
release in a collaborative project with western U.S. queen producers and others are
maintained in cryogenic storage as part of a long-term breeding program.
A germplasm repository would allow for the preservation of top tier domestic genetic
resources from the current U.S. honey bee population.
o Queen producers could cryopreserve examples of their best lines of honey bees and
then, years or decades later, retrieve these from liquid nitrogen storage to backcross to
extant populations.
o Such a repository effectively provides the option for queen producers to breed across
time (different year classes) and space (easy transportation of genetic material) in
ways previously unavailable.
Technology Transfer Teams: Workshop participants also discussed the establishment and
support of Tech Teams regionally within the U.S. to assist beekeepers. The system
discussed was based on a model in use in Canada and another one currently operating in
35
California to assist queen breeders. The concept of the Tech Team is that a group of
trained individuals work in the field with beekeepers to assess stocks and provide
information that would inform management decisions to assess and breed bees (in the case
of queen producers) or maintain colony health (all locations). The approach represents a
new, field-active model of extension and a tool for action at the interface of science
(applied research) and industry (informed management). The model calls for a fee-forservice approach that will make the tech teams self-supporting within a few years.
The Tech Team currently assisting California queen bee breeders provides data that allows
producers to assess their genetic stocks for specific traits of interest (hygienic behavior,
for example). The teams are in place to also provide selection assistance to breeders as
other traits become available. The Tech Team approach provides a means to incorporate
objective criteria into the breeders traditional process of choosing breeding queens.
In addition to assisting the industry with the implementation of research findings such as
genetic improvement (in California) or colony health (California, and Midwestern and
Southeastern states), Tech Teams also provide a means for capturing data on current
honey bee populations that can be used for epidemiological analyses or breeding (through
identification of high-quality stocks).
A new Tech Team is starting up in the Midwest as part of the Bee Informed Partnership
(http://beeinformed.org/ ), and there is strong interest to develop a Tech Team for the
southeastern United States.
Diagnostic Laboratories: Few diagnostic laboratories are available in the United States to
support beekeepers that wish to submit samples of their bees for determination of
pathogen and parasite loads. Work group participants discussed the utility of establishing
one or more diagnostic laboratories tasked with providing rapid turnaround analyses of
pathogens and parasites for Tech Teams and beekeepers.
The primary organisms that need to be analyzed by diagnostic laboratories include

Nosema spp., V. destructor, and tracheal mites (Acarapis woodi), although these
laboratories could also be useful in evaluating submitted stocks for genetic markers for
trait selection, as that technology becomes available.
In areas where Africanized honey bees occur, there would also be a demand to analyze
samples to determine the extent of genetic introgression from Africanized honey bees.
36
Other Issues: The following additional topics were noted by participants as needing
additional research:
Queen failures: There is a widespread perception that honey bee queens do not live as long
as they used to. Research into the possible causes of early supersedure, the process by
which one queen bee is replaced by a new queen, or queen failure without replacement is
needed to determine prevalence and causes, such as genetics, pathogen, pesticides,
nutrition, management, and shipping.
Genetically based treatments for pathogens: Interference RNA (RNAi), technology

research is needed on honey bees and other pollinators. RNAi is a process used by many
different organisms to regulate the activity of genes, and is also known as posttranscriptional gene silencing.
Signaling and communication: Basic research is needed to understand signaling and

communication within the colony and between pests and bees.
Lack of research funding for applied bee issues: Work group participants also discussed
the difficulty that researchers have in finding adequate funding to carry out studies in
applied bee research. Participants recommended exploring whether USDA could develop
a call for proposals on applied issues in colony health and beekeeping sustainability.
37
Conclusion
Overall and consistent with the stated objective, this conference provided an overview of a
significant body of new knowledge on the current state of the science of honey bee health to the
CCD Steering Committee that will be helpful in updating the CCD action plan. Stakeholders also
identified a number of BMPs to potentially address factors associated with declines, and research
needs were clearly articulated as well toward addressing uncertainties. In response to stakeholder
input provided at the conference and based on the available science and its associated
uncertainties, the CCD Sterring Committee will revise the CCD action plan, The purpose of the
action plan is to synthesize current recommendations from stakeholders and to coordinate an
updated Federal strategy to address honey bee losses. The decline of honey bees and other
pollinators continues to be a high priority topic for the USDA and the U.S. EPA. Intramural and
extramural research and extension to elucidate the factors associated with losses and mitigating
risks remains a high priority. We anticipate that the next CCD action plan will be completed in
2013 to early 2014.
Acknowledgment
This conference was partially supported by a USDA NIFA Agriculture and Food Research
Initiative Competitive Grant No. 2012-67013-19959 to J.L. Frazier. Funding was also provided
by USDA ARS and USDA APHIS (Cooperative Agreement No. 12-8100-1652) also to J.L
Frazier at Pennsylvania State University.
The USDA Office of Pest Management Policy
provided staff support.
38
Appendix 1. Conference Agenda
National Stakeholders Conference on Honey Bee Health

October 15-17, 2012
Sheraton Suites Old Town Alexandria, 801 North St. Asaph Street, Alexandria, Virginia
Agenda: Day 1, October 15, 2012
Plenary session
8:00AM 8:30AM: Opening Remarks: USDA Deputy Secretary, Kathleen Merrigan; U.S. EPA
Deputy Administrator, Bob Perciasepe.
8:30AM 8:40AM: Welcome, Sonny Ramaswamy, USDA NIFA Director
8:40AM 9:30AM: Keynote Speaker, May Berenbaum, University of Illinois, UrbanaChampaign: Overview of the State of Our Pollinators
9:30AM-10:40AM: Stakeholder Opening Comments
Presenters: Darren Cox, Beekeeper Representative to US EPA Pollinator Program
Dialogue Committee; Dan Botts, Minor Crop Farm Alliance; Gabrielle Ludwig, Almond
Board of California; Barbara Glenn, Senior VP, Science and Regulatory Affairs, CropLife
America; Laurie Davies Adams, Executive Director, North American Pollinator
Protection Campaign; Christi Heintz, Apis m
Topic Presentations:
11:00AM 11:30AM: Current State of Knowledge of CCD and its Relation to Honey Bee
Health; Jeff Pettis, USDA ARS; Dennis vanEngelsdorp, University of Maryland
11:30AM 12:00AM: Current State of Knowledge of Bee Biology; Jay Evans, USDA ARS
1:30AM 2:00PM: Current State of Knowledge of Nutrition and Best Management Practices;
Gloria DeGrandi-Hoffman, USDA ARS, Tucson, Arizona; Nancy Moran, Yale University
2:00PM 2:30PM: Current State of Knowledge of Pathogens and Best Management Practices;
Diana Cox-Foster, Pennsylvania State University; Jay Evans, USDA ARS
39
2:30PM 3:00PM: Current State of Knowledge of Arthropod Pests and Best Management
Practices; Dennis vanEngelsdorp, University of Maryland; Jeff Pettis, USDA ARS
3:30PM 4:00PM: State of Knowledge of Pesticides and Best Management Practices; Reed
Johnson, Ohio State University; Jim Frazier, Pennsylvania State University
4:00PM 4:30PM: Current State of Knowledge of Bee Genetics, Breeding and Best
Management Practices; Marla Spivak, University of Minnesota; Steve Sheppard,
Washington State University
5:00PM 7:00PM: Evening Discussion/Networking Session Transition to Day 2 Work Group
Sessions
Day 2, October 16, 2012

8:00AM 10:00AM: Work Group Sessions
- Nutrition
- Pathogens and Arthropod Pests
- Pesticides
- Bee Genetics, Breeding, Biology
10:20AM 12:00PM: Work Group Sessions
- Nutrition
- Pathogens and Arthropod Pests
- Pesticides
- Bee Genetics, Breeding and Biology
- Work Group Reports to the Whole:
1:30 2:15: Nutrition
2:15 3:00: Pests
40

- Work Group Reports to the Whole:
3:25 4:10: Bee Genetics, Breeding, Biology
4:10 - 5:00: Pesticides
Day 3, October 17, 2012

8:30AM 10:00PM: Federal CCD Steering Committee meeting with research leaders to
summarize conference input.
10:00 AM 12:00PM: Federal CCD Steering Committee meeting to revise Federal CCD Action
Plan.
Conference Steering Committee:

David Epstein, USDA OPMP; Tom Moriarty and Tom Steeger, US EPA; Kevin Hackett,
USDA ARS; Robyn Rose, USDA APHIS; Mary Purcell-Miramontes, USDA NIFA;
Terrell Erickson, USDA NRCS.
41
Appendix 2. Questions Developed for Day 2 Work Groups.
Questions developed for discussion in the Nutrition Work Group:
1) How do we evaluate the nutritional value of pollen? How does the nutritional composition
of pollen change after it is converted to bee bread?
2) How do protein and carbohydrate supplements affect beneficial gut microbes?
3) Does pollen and nectar contamination with pesticides/fungicides affect beneficial
microbes in stored pollen and the bees digestive system?
4) Is there an interaction between nutritional status in a colony and its susceptibility to
disease and parasites? Is a colonys response to treatments for foulbrood, Nosema or mites
affected by nutrition?
5) How can we balance treatments so that beneficial microbes are not negatively affected,
while still controlling pathogens and pests?
6) Has anyone noticed apparent detrimental effects from treatments with Tylosin,
Terramycin, or other anti-microbials?
7) What research projects would add most information to understanding how microbes in
colonies are affecting colony health?
Questions developed for discussion in the Pathogens Work Group:
1) What are the best ways to describe a pathogen/disease so that others can determine if they
have the same organism?
2) What are the health impacts of neglected parasites/pathogens/or potential symbionts like
Crithidia, fungi, amoebae, lactobacteria, spiroplasma?
3) How best to sample, preserve and screen samples for disease both unknown and known?
4) How can surveys be better used to predict/mitigate disease (targets, time scales, costs)?
5) Which management processes are responsible for enabling disease spread/ minimizing
disease occurrence?
6) Are other pollinator species also being impacted by viral infections and common stress
factors?
42
7) How does Varroa increase virulence of transmitted viruses via impacts on bee immunity
and impacts on viral load and readiness?
8) Can a single method be developed to sample adult bees or brood that will work for most
pests and pathogens or do we need specific sampling regimes for each?
Questions developed for discussion in the arthropod pests Work Group:
1) Can Varroa and European honey bees reach stable host-parasite equilibrium if we reduce
chemical controls?
a.
Do we have commercial stocks that are viable for pollination?
b. Are chemical treatments doing more harm than good?

2) Rank the following in terms of importance for dealing with Varroa new chemical
controls, new biological controls, understanding of resistance mechanisms by Africanized
and Asian honey bees, means to understand and disrupt the mite-virus interaction.
3) Are the current traps and chemical controls adequate for dealing with small hive beetle
and if not what are areas of research that would be most helpful?
4) Have chemical treatments for Varroa made tracheal mites scarce or has natural selection
driven tracheal mite levels down?
5) Are tracheal mites still an issue in bee health?
6) Should research be directed at novel or rare pests (i.e. phorid flies, the bee louse Braula,
etc)?
7) Should research be conducted on known threats from abroad and if so rank the following?
( Tropilaelaps mites, Apis cerana, capensis honey bees and Thai sacbrood)
8) What do we need to know about the lifecycles of honey bee threats not found in the U.S.
in order to be prepared for eradication efforts and/ or providing management advice in the
event of their introduction?
9) Do we need new control methods for wax moths?
10) How best management practices are effectively disseminated through the beekeeping
community?
43
Questions developed for discussion in the Pesticide Work Group: Management Practices
1) Best Management Practices:

a.
Are there sources for grower/beekeeper BMPs that are currently in use (Project Apis m)?
b. What practices do beekeepers use or prefer in order to minimize the potential impact of
pesticides to managed honey bees? Do practices differ by crop or region?
c.
To what extent are growers aware of the potential impact their activity may have on
bees?
d. What practices do applicators or growers use or prefer to minimize the potential impact of
pesticides to managed honey bees?
2) Who/what are the best information sources for growers when choosing products to protect
crops?
a.
Do these sources (such as Pest Control Advisors (PCAs) have access to information on
best management practices with respect to pollinator protection?
b. Do beekeepers consult with these sources (such as PCAs) or with growers to work out
management practices that may present lower potential risk from pesticides? If not, why
not?
3) What options are available to improve communication between stakeholders (state
officials, growers, applicators and beekeepers improve risk management?
4) How can stakeholders (state officials, beekeepers, growers, and applicators) work together
to build integrated plans to protect against pests insects and protect managed pollinators?
5) Are there efforts underway to develop Best Management Practices that apply to pesticide
use in agricultural settings? Are there efforts underway to develop Best Management
Practices that apply to in-hive use of pesticides? If so, what is likely to result from these
efforts? If not, why not? Are there exposure scenarios or routes that stakeholders feel
have not been identified by federal/state regulatory partners?
6) Does reserve/non-crop land provide a pesticide-free forage scenario for managed bees,
and if not, why and how can it be managed?
7) How can a beekeeper know if pesticides exposure is a factor in colony loss or weakening?
a.
At the colony level, how does acute exposure to a pesticide differ from that of chronic
exposure?
44
8) Historically, what is the typical loss a beekeeper experiences from pesticides?

a.
Aside from obvious losses, do beekeepers feel that delivery of pollination services and
honey production have been affected by pesticide exposure?
b. Do beekeepers feel that current loss due to pesticides is equally associated across crops, or
across the country? That is, do beekeepers feel that their losses from pesticides would be
different if they worked in different states or contracted with different crops?
9) Do miticides cause losses? What is an acceptable level of loss due miticide exposure?
Can beekeeping survive and be profitable without use of miticides?
10) To what extent are alternative forage areas a viable option in heavily developed
agricultural areas?
Questions developed for discussion in the Pesticide Work Group: Research
11) Can we directly measure the effects of pesticide exposure on delivery of pollination
services and honey production? Can other, more easily measured, endpoints be used to
predict pesticide effects on pollination and honey production? Is colony strength an
adequate measurement endpoint?
12) Can sublethal pesticide exposure be shown to affect pollination and honey production?
How can we relate sublethal exposure effects of individual bees (PER, mobility, homing)
to whole colony success? Can sublethal testing on individuals be improved?
13) How can we get to a better estimate of bees pesticide exposure? Is it possible to estimate
individual bees body burden (the Ecologically Relevant Concentration) of pesticide
through empirical measurement or toxicokinetic/toxicodynamic modeling?
14) Interactions could occur between insecticides, miticides, fungicides, herbicides, adjuvants,
pests, pathogens, nutritional status, microbial community, plant xenobiotics, seasonality,
management practices, caste, life stage and genetics. Some combinations are likely to be
either harmful or beneficial to bees how do we discover these without testing all possible
combinations?
15) How do we pay for pesticide-related bee research?
45
Questions developed for discussion in the Genetics/Breeding/Biology Work Group:
1. Genetic Diversity: Genetic diversity of the honey bee may now be considered on a global
scale. For example: the total diversity of managed Italian honey bees may be best
represented by honey bees from Italy (the original subspecies) and managed populations
in the Americas and Australia. All of these may be viable pools that could contribute to
establishing populations for selective breeding. A cryogenic storage facility could
maintain germplasm from both natural and managed honey bee populations for future
breeding. Thus, in addition to Old World source populations, genetic samples of specific
desirable commercial lines of bees could be placed into cryogenic storage for later
recovery. Cryogenic storage addresses an overarching USDA mandate to preserve
germplasm from animals and plants of agricultural significance: The mission of the
National Center for Genetic Resources Preservation (NCGRP) is to acquire, evaluate,
preserve, and provide a national collection of genetic resources to secure the biological
diversity that underpins a sustainable U.S. agricultural economy through diligent
stewardship, research, and communication. Despite initial efforts to sustain a honey bee
stock center, the cost needed to maintain genetic diversity in large cohorts of living
colonies was prohibitive. Now that functional cryopreservation technology is available, is
it time to reconsider the status quo? That is: Is there a need for a major effort to establish
a national honey bee germplasm repository?
2. Breeding Commercial bee breeding: The goal of the tech-transfer Bee Team, funded
by the Bee Informed Partnership and fees-for-service, is to work directly with bee
breeders in California to improve stock selection, enhance genetic diversity, and engage in
disease and parasite-related diagnostic evaluations. In addition to helping bee breeders
keep track of and select colonies with the lowest mite, Nosema and virus levels, the Bee
Team assists with selection for hygienic behavior using the freeze-killed brood assay.
a.
What other traits could be selected? Are we ready to implement marker-assisted

selection for grooming behavior and VSH (e.g., the Bee Team could send samples to a lab
for genetic testing)?
46
b. Toward a sustainable and diverse genetic base: What is the best way to incorporate
additional imported honey bee genetic material into the actual breeding populations of the
U.S.?
Local/ regional bee breeding: Many beekeepers would like to select for one or more of the
following: locally adapted stock; survival stock; and/or stock that does not require any
chemical treatments.
a. How to balance genetic diversity and selecting for resistance, while trying to keep things
locally adapted? What does locally adapted mean in terms of honey bees?
b. Given the perceived differences in selection criteria between large commercial interests
and beekeepers working to develop locally selected populations, how do the roles of
subspecies origin, selection criteria for pest and parasite control and overwintering
strategies inform the choice of the initial population for breeding?
3. Queen Failures: Real or Perceived?
a. If real: Is this problem tied to race, stock, type of beekeeping operation, old vs. new
combs? Is the problem caused by not enough time spent in mating nucs? Or pathogen
(viruses, Nosema?) Or pesticide residue?
4. How do we weigh the impacts of behavioral and physiological (immunity, development)
traits on bee health? Similarly for individual and social traits? There must be trade-offs
for bees, in terms of costs of maintaining these traits, so we cant just push them to be
above average at everything.
5. How can bee x bee and bee x pest signaling be exploited to 1) control pests, 2) manipulate
foraging and other colony traits, 3) maintain respect for the queen?
6. How can standards and protocols be normalized across labs and countries: controlled
language, Beebook for protocols, true Standard Operating Procedures? These are all
needed, especially with touchy regulatory issues.
7. What is the current consensus on biological and abiological factors that act non-additively
to impact bee health, do any cancel each other out or is it always 1 + 1 2? How do we
use this knowledge (e.g., are survey tools economic for making management decisions?
Can knowing that certain factors interact negatively for bees be used to more strongly
regulate those factors when they are likely to co-occur?
47
8. Six years post-honeybee genome what have we learned about bee biology and what is in
place for the major questions of breeding, vetting traits, parasite interactions, novel
controls (RNAi), and management to make bees less stressed and more productive.
9. Six years post-CCD what have we learned from the added efforts put into bee disease and
responses to chemical stresses? Which new tools or ways of thinking/models are going to
change the field and improve bee health?
10. Will the world accept genetic strategies from i) RNAi versus pests, ii) RNAi to influence
bee behaviors? iii) germline transformation of bees even if it tackles a critical weak point
like viral resistance?
48
Appendix 3: Invited Work Group Participants
(The participant lists in this appendix do not represent all who actually participated in each work
group. Some invitees did not attend the conference. Note that recorders are not listed.)
Invited Work Group Participants - Nutrition
Leaders
Degrandi-Hoffman, Gloria
USDA ARS
Erickson, Terrell,
USDA NRCS
Moran, Nancy,
Yale University
Purcell Miramontes, Mary
USDA NIFA
Participants
Berger, Lori
California Specialty Crop Association
Browning, Zach
Browning Honey Co. Inc.
Davies-Adams, Laurie
North American Pollinator Protection Campaign
Delaney, Deborah
University of Delaware
Downey, Danielle
Apiary Inspectors of America
Hayes, Jerry
Monsanto/Beeologics
Heintz, Christi
Project Apis m
Johnson, Jody
Smithers Viscient
Kelly, Iain
Bayer CropScience
Kuivila, Kathryn
USGS
Ludwig, Gabrielle
Almond Board of California
Overmyer, Jay
Syngenta Crop Protection
Verhoek, Randy
Harvest Honey Inc ND, NHBA
Wehling, Wayne
USDA APHIS
49
Unable to Attend
Eischen, Frank
USDA ARS
Esaias, Wayne
UMD/NASA (emeritus)
Haun, Gray
Tennessee Department of Agriculture
Hyberg, Skip
USDA FSA
Mussen, Eric
California Department of Food and Agriculture
Rao, Sujaya
Oregon State University
Sanroma, Joe
LA Beekeepers Association, AHPA
Trumble, John
UC Riverside
Tucker, Tim
Tucker Bees, Kansas, ABA
Vaughn, Mace
Xerces Society
Wardel, Gordy
Paramount Farms, CA
50
Invited Work Group Participants Pathogens/Arthropods
Leaders
Cox-Foster, Diana
Pennsylvania State University
Evans, Jay
USDA ARS
Hackett, Kevin
USDA ARS
Rose, Robyn
USDA APHIS
vanEngelsdorp, Dennis
University of Maryland
Participants
Abbott, John
Syngenta Crop Protection
Burand, John
University of Massachusetts
Caron, Dewey
University of Delaware
Cox, Darren
Cox Honeyland, NHBA
Coy, Steve
Coy's Honey Farm
Cruise, Chris
Mann Lake Beekeeping Supplies
Feken, Max
Florida Dept of Agriculture and Consumer Services
Glenn, Barb
CropLife America
Hackenberg, David
Hackenberg Apiaries, ABF
Huang, Wei-Fone
University of Illinois
James, Rosalind
USDA ARS
Meikle, William
USDA ARS
Rogers, Dick
Bayer CropScience
Skinner, John
University of Tennessee
Smallwood, Ben
USDA NRCS
Stewart, Colin
USDA APHIS
Stoner, Kimberly
Connecticut Agricultural Experiment Station
Teal, Peter
USDA ARS
Webster, Tom
Kentucky State University
Westervelt, David
51
Unable to Attend
Averill, Anne
University of Massachusetts
DiSalvo, Carol
National Park Service
Haterius, Stephen
National Association of State Departments of Agriculture
Kozak, Paul
Canadian Association of Professional Apiculturists
Kramer, Vince
Dow AgroSciences
Levi, Ed
Arkansas State Plant Board
52
Invited Work Group Participants - Pesticides
Leaders
Johnson, Reed,
Research Leader, Ohio State University
Steeger, Tom,
Facilitator, U.S. EPA Office of Pesticide Programs
Moriarty, Tom,
Facilitator, U.S. EPA Office of Pesticide Programs
Anderson, Terry
Facilitator, USDA ARS
Participants
Adee, Bret
American Honey Producers Association
Alix, Anne
Dow AgroSciences
Berenbaum, May
University of Illinois, Champaign-Urbana
Bireley, Richard
California Dept. of Pesticide Regulation
Christiansen, Jessica
Monsanto/Beeologics
Egan, Peter
Armed Forces Pest Management Board
Fischer, David
Bayer Crop Science
Hansen, George
American Beekeepers Federation
Harriot, Nichelle
Beyond Pesticides
Hart, Connie
Canada Pest Management Regulatory Agency
Hooven, Louisa
Hou, Wayne
Canada Pest Management Regulatory Agency
Johansen, Erik
Washington State Department of Agriculture
McCain, Pat
Syngenta Crop Science
Mendes, Dave
Commercial Beekeeper, FL
O'Neill, Bridget
DuPont Chemical
Parker, Don
National Cotton Council
Pettis, Jeff
USDA ARS
Ruckert, Ed
McDermott Will & Emery LLP
Seetin, Mark
U.S. Apple Committee
Tindal, Nick
Association of Equipment Manufacturers
Trainer, Maria
CropLife Canada
53
Walker, Larissa
Wisk, Joe
BASF
Unable to Attend
Dively, Galen
Lu, Chensheng
Harvard University
Rowe, Brian
Michigan Department of Agriculture
Sass, Jennifer
Natural Resources Defense Council
Tignor, Keith
Apiary Inspectors of America
Willet, Mike
Northwest Horticultural Council
Wu, Mae
Natural Resources Defense Council
54
Invited Work Group Participants Biology/Genetics/Breeding
Leaders
Epstein, David
USDA ARS
Sheppard, Steve
Washington State University
Spivak, Marla
University of Minnesota
Participants
Bobb, Jim
Eastern Apiculture Society
Boess, Bruce
USDA NASS
Culiney, Tom
USDA APHIS
Danka, Robert
USDA ARS
de Guzman, Lilia
USDA APHIS
Dolezal, Adam
Iowa State University
Dykes, Mark
Hawthorne, David
Henderson, Colin
Bee Alert Technology
Mattila, Heather
Wellesley College
McCallister, Ray
CropLife America
Pruisner, Robin
Iowa Dept of Agriculture
Rinderer, Tom
USDA ARS
Rouse, Gus
Kona Queen Hawaii, Inc
Rueppell, Olav
University of North Carolina
Tarpy, Dave
North Carolina State University
Zisook, Elsa
Valent U.S.A. Corporation
Unable to Attend
Bourgeois, Lanie
USDA ARS
Buchman, Steve
Pollinator Partnership
Cane, Jim
USDA ARS
Derisi, Joe
University of California San Francisco

55
Sagili, Ramesh
Weaver, Danny
BeeWeaver Apiaries, TX
56
Appendix 4. Cited References for Biology Research Presentation
Alaux, C., Brunet, J. L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., Brillard, J.,
Baldy, A., Belzunces, L. P., and Le Conte, Y. (2010). Interactions between Nosema
microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environmental
Microbiology 12(3), 774-782.
Alaux, C., Dantec, C., Parrinello, H., and Le Conte, Y. (2011). Nutrigenomics in honey bees:
Digital gene expression analysis of pollen's nutritive effects on healthy and Varroaparasitized bees. BMC Genomics 12.
Ament, S. A., Wang, Y., Chen, C., Blatti, C. A., Hong, F., Liang, Z. S., Negre, N., White, K. P.,
Rodriguez-Zas, S. L., Mizzen, C. A., Sinha, S., Zhong, S., and Robinson, G. E. (2012).
The transcription factor ultraspiracle influences honey bee social behavior and behaviorrelated gene expression. PLoS Genetics 8(3).
Anderson, K. E., Sheehan, T. H., Eckholm, B. J., Mott, B. M., and DeGrandi-Hoffman, G.
(2011). An emerging paradigm of colony health: Microbial balance of the honey bee and
hive (Apis mellifera). Insectes Sociaux 58(4), 431-444.
Caldern, R. A., Fallas, N., Zamora, L. G., van Veen, J. W., and van Snchez, L. A. (2009).
Behavior of Varroa mites in worker brood cells of Africanized honey bees. Experimental
and Applied Acarology 49(4), 329-338.
Cornman, R. S., Tarpy, D. R., Chen, Y., Jeffreys, L., Lopez, D., Pettis, J. S., vanEngelsdorp, D.,
and Evans, J. D. (2012). Pathogen webs in collapsing honey bee colonies. PLoS ONE
7(8).
Engel, P., Martinson, V. G., and Moran, N. A. (2012). Functional diversity within the simple gut
microbiota of the honey bee. Proceedings of the National Academy of Sciences of the
United States of America 109(27), 11002-11007.
Evans, J. D., and Spivak, M. (2010). Socialized medicine: Individual and communal disease
barriers in honey bees. Journal of Invertebrate Pathology 103(SUPPL. 1).
Foret, S., Kucharski, R., Pellegrini, M., Feng, S., Jacobsen, S. E., Robinson, G. E., and Maleszka,
R. (2012). DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative
phenotypes in honey bees. Proceedings of the National Academy of Sciences of the
United States of America 109(13), 4968-4973.
57
Fries, I. (2010). Nosema ceranae in European honey bees (Apis mellifera). Journal of
Invertebrate Pathology 103(SUPPL. 1).
Gregorc, A., and Ellis, J. D. (2011). Cell death localization in situ in laboratory reared honey bee
(Apis mellifera L.) larvae treated with pesticides. Pesticide Biochemistry and Physiology
99(2), 200-207.
Gregorc, A., Evans, J. D., Scharf, M., and Ellis, J. D. (2012). Gene expression in honey bee
(Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor).
Journal of Insect Physiology 58(8), 1042-1049.
Harris, J. W., Danka, R. G., and Villa, J. D. (2012). Changes in infestation, cell cap condition,
and reproductive status of Varroa destructor (Mesostigmata: Varroidae) in brood exposed
to honey bees with Varroa sensitive hygiene. Annals of the Entomological Society of
America 105(3), 512-518.
Henry, M., Bguin, M., Requier, F., Rollin, O., Odoux, J. F., Aupinel, P., Aptel, J.,
Tchamitchian, S., and Decourtye, A. (2012). A common pesticide decreases foraging
success and survival in honey bees. Science 336(6079), 348-350.
HoneybeeGenomeSequencingConsortium (2006). Insights into social insects from the genome of
the honeybee Apis mellifera. Nature 443(7114), 931-949.
Linksvayer, T. A., Kaftanoglu, O., Akyol, E., Blatch, S., Amdam, G. V., and Page, R. E. (2011).
Larval and nurse worker control of developmental plasticity and the evolution of honey
bee queen-worker dimorphism. Journal of Evolutionary Biology 24(9), 1939-1948.
Nazzi, F., Brown, S. P., Annoscia, D., Del Piccolo, F., Di Prisco, G., Varricchio, P., Vedova, G.
D., Cattonaro, F., Caprio, E., and Pennacchio, F. (2012). Synergistic parasite-pathogen
interactions mediated by host immunity can drive the collapse of honeybee colonies.
PLoS Pathogens 8(6).
Oxley, P. R., Spivak, M., and Oldroyd, B. P. (2010). Six quantitative trait loci influence task
thresholds for hygienic behaviour in honeybees (Apis mellifera). Molecular Ecology
19(7), 1452-1461.
Page Jr, R. E., Fondrk, M. K., and Rueppell, O. (2012). Complex pleiotropy characterizes the
pollen hoarding syndrome in honey bees (Apis mellifera L.). Behavioral Ecology and
Sociobiology 66(11), 1459-1466.
58
Pettis, J. S., Vanengelsdorp, D., Johnson, J., and Dively, G. (2012). Pesticide exposure in honey
bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99(2),
153-158.
Rueppell, O., Hayworth, M. K., and Ross, N. P. (2010). Altruistic self-removal of healthcompromised honey bee workers from their hive. Journal of Evolutionary Biology 23(7),
1538-1546.
Runckel, C., Flenniken, M. L., Engel, J. C., Ruby, J. G., Ganem, D., Andino, R., and DeRisi, J.
L. (2011). Temporal analysis of the honey bee microbiome reveals four novel viruses and
seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS ONE 6(6): e20656.
Siede, R., Meixner, M. D., and Bchler, R. (2012). Comparison of transcriptional changes of
immune genes to experimental challenge in the honey bee (Apis mellifera). Journal of
Apicultural Research 51(4), 320-328.
Singh, R., Levitt, A. L., Rajotte, E. G., Holmes, E. C., Ostiguy, N., Vanengelsdorp, D., Lipkin,
W. I., Depamphilis, C. W., Toth, A. L., and Cox-Foster, D. L. (2010). RNA viruses in
hymenopteran pollinators: Evidence of inter-taxa virus transmission via pollen and
potential impact on non-Apis hymenopteran species. PLoS ONE 5(12).
Williams, G. R., Dietemann, V., Ellis, J. D., and Neumann, P. (2012). An update on the
COLOSS network and the BEEBOOK: Standard methodologies for Apis mellifera
research. Journal of Apicultural Research 51(2), 151-153.
59
Appendix 5. Cited References for Pesticide Research Presentation
Ciarlo, T. J., C. A. Mullin, J. L. Frazier and D. R. Schmehl. 2012. Learning impairment in honey
bees caused by agricultural spray adjuvants. PLoS ONE, 7, e40848-e40848.
Cresswell, J. E. and H. M. Thompson. 2012. 'Comment on A Common Pesticide Decreases
Foraging Success and Survival in Honey Bees, Science 337, 1453.
Eiri, D and J.C. Nieh. 2012. A nicotinic acetylcholine receptor agonist affects honey bee sucrose
responsiveness and decreases waggle dancing. J Exp Biol. 215:2022-2029.
Hawthorne DJ, Dively GP. 2011. Killing them with kindness? In-hive medications may inhibit
xenobiotic efflux transporters and endanger honey bees. PLoS One. 2011; 6 (11):e26796.
Johnson RM, Mao W, Pollock HS, Niu G, Schuler MA, et al. 2012. Ecologically Appropriate
Xenobiotics Induce Cytochrome P450s in Apis mellifera. PLoS ONE 7(2): e31051.
Johnson RM, Dahlgren L, Siegfried BD, Ellis MD (2013) Acaricide, Fungicide and Drug
Interactions in Honey Bees (Apis mellifera). PLoS ONE 8(1): e54092.
Khoury DS, Myerscough MR, Barron AB (2011) A Quantitative Model of Honey Bee Colony
Population Dynamics. PLoS ONE 6(4): e18491. doi:10.1371/journal.pone.0018491
Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K (2012) Multiple Routes of Pesticide
Exposure for Honey Bees Living Near Agricultural Fields. PLoS ONE 7(1): e29268.
doi:10.1371/journal.pone.0029268
Mullin, C.A., M. Frazier, J. L. Frazier, S, Ashcraft1, R, Simonds, D, vanEngelsdorp, J. S. Pettis.
2010. High Levels of Miticides and Agrochemicals in North American Apiaries:
Implications for Honey Bee Health. PLoS. ONE.5 (3): e9754.
J. Pistorius, G. Bischoff, U. Heimbach, M. Sthler. 2009. Bee poisoning incidents in Germany in
spring 2008 caused by abrasion of active substance from treated seeds during sowing of
maize, In: Oomen and Thompson (Eds). Hazards of pesticides to bees: 10th Int. Symp. of
the ICP-BR Bee Protection Group, Bucharest (Romania), Oct 8-10, 2008. pp118
Schneider C. W., Tautz J., Grnewald B., Fuchs S. (2012). RFID tracking of sub-lethal effects of
two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS ONE 7,
e30023.
60
Teeters, B.S. R. M. Johnson, M D. Ellis, B D. Siegfried. 2012. Using video-tracking to assess

sublethal effects of pesticides on honey bees (Apis mellifera L.), Environmental
Toxicology and Chemistry. 13491354
61
Appendix 6. Cited References for Biology, Genetics, Breeding Research Presentation
Delaney, D. A., M. D. Meixner, N. M. Schiff, and W. S. Sheppard. 2009. Genetic

Characterization of Commercial Honey Bee (Hymenoptera: Apidae) Populations in the
United States by Using Mitochondrial and Microsatellite Markers, Annals of the
Entomological Society of America, 102(4):666-673.
Harpur, B.A., S. Minaei, C.F. Kent and A. Zayed. 2012. Management increases genetic diversity
of honey bees via admixture, Molecular Ecology 21, 44144421.
Sheppard, W. S. 1989. A History of the Introduction of Honey Bee Races Into the United States:
Parts I and II of a Two-part Series, USDAARS, Beneficial Insects Laboratory, Bldg. 476,
BARCEast Beltsville, Maryland 20705.
62
ARS Research Project on Pesticide Effects on Bees

K. Hackett
5/29/13
Southern Cotton Project:
Project Lead: J. Adamczyk
Bee Lead: T. Rinderer
Application Lead: C. Hoffmann
Participants: TBD
Beltsville: Evans
Base and $800K

temporary, to be
distributed to Baton
Rouge, College
Station, Poplarville,
Stoneville
$100K temporary
Beltsville: TBD
$200K temporary
Beltsville: Pettis, Chen, Corona &

Cook
Base
Fargo: Yocum & Rinehart
Base
Gainesville: Teal
Base
Logan: James & Pitts-Singer
Base
Tucson: TBD
$200K temporary
Tucson: Hoffman
Tucson: Meikle
Base & temporary

(Valent)
Base
Tucson: Anderson
Base
Project Plan to be drafted on

research on pesticide risks (hazard
and exposure) to honey bees
Bioinformatics of bee response to

pesticide exposure
Synergistic sublethal effects of
neonics and pathogens
Synergistic sublethal effects of
pesticides and pathogens, including
pesticide oxidative stress and
metabolic rate; sublethal effects of
pesticides on sperm viability
Pesticide related stress factors in
migratory beekeeping, including
pesticides; Smart Frame sensing of
hive strength and survival
likelihood
Sublethal effects of fluvalinate and
coumophos on honey bee juvenile
hormone
Epidemiological study of bee loss
factors, including pesticides; effects
of pesticides on non-Apis bee
immunity; fungicide effects on
nesting and foraging of non-Apis
bees
Synergistic effects of pesticides
used in almond
Synergistic effects of pesticides
used in cotton
Smart Hive sensing of bee stress
factors, including
fungicide/miticide/insecticide
interactions and their effects on
bees, e.g., queen health and
pheromone production and
supersedure
Fungicide effects on bee bread
Action Plan. Others, with key administrative and oversight roles, were also copied in this first
message so that they are aware that this project will be taking place.
Everyone is encouraged to cooperate to help make the overall effort a success. The beekeeping
industry is in serious jeopardy and really does need our help. If pesticides are causing synergistic
sublethal effects, we really need to know. In particular, we need to answer the two questions posed
above. We came together around CCD when it first became a contributor to bee loss and have
made important gains as an agency. We need to do the same in the area of pesticide effects on
bees.
Also, note that Tom Rinderer has arranged a listening session for beekeepers in Baton Rouge on
June 4-5, 2013. This will provide additional input to the process.
Sally Schneider, Roy Scott, and I are ONP leads on the project.
Thank you for any help that you can give to make this project succeed.
Kevin

301-504-4680 (office)
301-504-6191 (fax)
From:
To:
Cc:
Subject:
Date:
Attachments:
Don Parker
Epstein, David
Keith Menchey
FW: URGENT; Info for Don Parker Cotton Council
Tuesday, October 25, 2011 5:19:52 PM
image003.png
Attachment 3 024875 D385088 Review of Systemicity of Keto-enols with label language.pdf
Attachment 2 cotton rebuttal.ppt
Attachment 1 Spiromesifen Bee Safety Summary.pdf
David,
Bayer has said I could share this with you. This is related to NCCs concern that EFED has taken a
position that cotton is a major risk for honey bees. You will see below that EFED states labeling
based on bloom is not effective mitigation for cotton because of extra-floral nectaries.
(b) (5)
Feel free to contact me.
Regards,
Don Parker
Manager, IPM
National Cotton Council
PO Box 2995
Cordova, TN 38088-2995
901.274.9030
From: Alan Ayers [mailto:alan.ayers@bayer.com]
Sent: Tuesday, October 25, 2011 2:49 PM
To: Don Parker
Cc: Iain Kelly
Subject: FW: URGENT; Info for Don Parker Cotton Council
Don
Please review and give Iain and me a call with questions.
Alan
From: Iain Kelly

Sent: Tuesday, October 25, 2011 1:54 PM
To: Alan Ayers
Cc: Clive Halder; David Fischer; Sherry Movassaghi; Lisa Bowers
Subject: URGENT; Info for Don Parker Cotton Council
Below is the information Don Parker requested on cotton. Alan will send onto him later today. Can
you please let Alan know of any concerns/Changed needed
___________________________________
Don,
Although spiromesifen has been registered for several years on cotton, Bayer CropScience has
continued to work on the potential toxicity to bees as the science has been developing and has had
numerous discussions with EPA on the issue.
Attachment 1 summarizes our assessment of the risk to bees from spiromesifen use. Extensive bee
testing has been conducted with the ketoenol class of chemistry. As discussed in Attachment 1,
based on this testing, it can be concluded that spiromesifen is practically non-toxic to adult bees
and is intrinsically toxic to bee larvae if the exposure level is high enough. Spiromesifen
applications can reduce survival of bee larvae under artificial conditions when bees are confined in
tents or cages and forced to forage on treated flowering crops. Under these artificial conditions, the
colonies recover within a few weeks. Under actual field conditions when colonies of free-ranging
bees are placed next to treated flowering crops, no adverse effects are expected. Survival of bee
larvae, colony strength and colony viability were not adversely impacted under real world field
conditions. Therefore, it can be concluded that agricultural use of spiromesifen per label directions
pose a de minimis risk to bees.
While we are still in discussion with EPA over the our assessment, there is agreement with EPA,
that while lower tier studies showed potential brood effects, the cotton field study demonstrated no
effect on brood - see Attachment 2. Despite this, EPA has continued to raise what if concerns
about potential issues with spiromesifen including a) other endpoints that may have been shown an
effect in the field study; b) potential systemicity, and; c) concerns about the statistical power of the
field tests. We have worked to address all of these concerns. Our response to concern (a) about
other endpoints is laid out in Attachment 2.
The systemicity concern (b) was raised partly because of the mobility of a related compound,
spirotetramat which we have not registered in cotton. Attachment 3 is the current response we
have from EPA relating to spiromesifen mobility. As we discussed with you, Bayer has developed
three different ketoenol active ingredients in the lipid biosynthesis inhibitor class of insecticides
spirotetramat (Movento), spirodiclofen (Envidor) and spiromesifen (Oberon). Although related
chemically, each of these active ingredients have very different mobility characteristics within
plants. Spirotetramat is fully systemic exhibiting both xylem and phloem mobile, while spirodiclofen
is immobile and spiromesifen shows translaminar mobility within the treated leaf, only. EPAs
response in Attachment 3 indicates that EPA now agrees that systemicity of spiromesifen should not
be an issue.
Bayer has also reexamined the statistical power of the field tests (c) which we can demonstrate is
sufficient, and has scheduled a meeting with EPA in early November to address this issue.
Despite us having conducted extensive studies to demonstrate spiromesifens safety under field
conditions EPA has taken a precautionary approach, wanting to eliminate exposure possibilities for
all crops and stated in Attachment 3 for cotton:

The information can be shared with David Epstein as it should be public record. Our main concerns,
though, as we discussed are more generic in nature. EPA is taking a precautionary approach to
registrations in relation to bees citing extrafloral nectaries and systemicity as areas of concern.
These are not new issues as systemic compounds have been used in cotton for many years. How
does EPA equate its position with the fact that cotton does not require pollination services and
appears only moderately attractive to bees?
Hope this helps but because of the extensive interactions with EPA the above may appear
somewhat convoluted but if anything needs clarifying please contact us
________________________________________
Coordinator U.S. Bee Health Issues
Phone: +1 919-549-2552
Mobile: (b) (6)
From:
To:
Subject:
Date:
Attachments:
Kunickis, Sheryl
Epstein, David
Fw: Urgent comments re neonicotinoid label changes
Thursday, August 08, 2013 3:54:19 PM
EPA letter.pdf
Grower Alert.pdf
See below.
From: Lin Schmale [mailto:lschmale@safnow.org]

Sent: Thursday, August 08, 2013 03:44 PM
To: rmcallister@croplifeamerica.org; Jeff Case <JCase@croplifeamerica.org>; Kellie Bray
<kbray@croplifeamerica.org>; Ed Ruckert <eruckert@mwe.com>; Gabrielle Ludwig
<gludwig@almondboard.com>; Chin, Teung; Kunickis, Sheryl
Cc: Joe Bischoff <jbischoff@anla.org>
Subject: FW: Urgent comments re neonicotinoid label changes
We have sent the attached comments and our earlier "Grower Alert" to EPA.

To: 'Laws.meredith@epa.gov'
Cc: 'Bradbury.steven@epa.gov'; 'rossi.lois@epa.gov'
Subject: Urgent comments re neonicotinoid label changes
Dear Ms. Laws:
Because of the great importance of neonicotinoids to the greenhouse, nursery and landscaping
industries in the U.S., we are submitting the comments of the Society of American Florists and the
American Nursery & Landscape Association, representing those industries, to you as you consider
changes to the pollinator language of the neonicotinoid labels. As noted in the letter, we are also
attaching a copy of a recent pesticide stewardship "Grower Alert" that our organizations sent to
growers across the U.S. in the wake of the tragic Oregon bee kill. I will send a paper copy of the
attachments by mail, but wanted to be sure that you have this letter as quickly as possible.
We hope you will consider our comments as you make your decision. We would appreciate the
opportunity to meet with EPA, and would be happy to bring along scientists who have been
instrumental in some of the important efforts noted in the letter.
Thank you very much for your careful approach to this very important issue. Please feel free to call
us should you have questions or wish further information.
Lin Schmale
Senior Director - Government Relations
Society of American Florists
1601 Duke Street
Alexandria, VA 22314
(703) 838-5232
cell:(b) (6)
LSchmale@safnow.org
Joseph Bischoff, PhD

Director of Government Relations
American Nursery & LandscapeAssociation
1200 G St. NW, Suite 800 Washington,DC 20005
(202) 434-8686 direct;
(b) (6)
cell
JBischoff@anla.org
From:
To:
Cc:
Subject:
Date:
Attachments:
Kunickis, Sheryl
Nowierski, Robert
Fitzner, Michael; Draper, Martin; Epstein, David
FW: Update regarding Meeting on September 18, 2013, 3:00-4:30 pm, regarding Pollinator
Protection/Alternative Seed Lubricant Issue -- Room S-4370-80 Potomac Yards South
Wednesday, September 18, 2013 11:00:49 AM
[Untitled].pdf
Hi Bob,
I understand you may be attending today's meeting at EPA on the issue of pollinators and seed
treatment - is that correct? Marty participated by phone at the meeting held several weeks ago. I had
a call from EPA this morning and they have asked me to say a few words on what USDA is doing to get
the word out. Mike will remember that I discussed EPA's interest in NIFA's participation during a recent
meeting with Dr. Ramaswamy. The meeting today is with a large number of stakeholders. EPA will
open the meeting, there will be introductions, Bayer will provide a presentation, equipment
manufacturers, applicators, and growers will speak, and then I will be asked to say a few words. Is
there anything I can mention with regard to outreach and extension? I have a couple of items to say for
NRCS and ARS, but NIFA is key to this effort. Any help is appreciated. I hope you - and/or Marty will
be able to attend. A call in number is also available if you are not able to get there in person.
Thanks,
Sheryl
-----Original Message----From: Fehrenbach, Margie [mailto:Fehrenbach.Margie@epa.gov]
Sent: Monday, September 16, 2013 4:23 PM
To: 'ntindall@AEM.org'; 'HoehnKevinW@johndeere.com'; 'dochtermanandrewc@johndeere.com';
'karl.klotzbach@cnh.com'; 'monte.weller@cnh.com'; 'DHahn@kinze.com';
'Chris.coleman@agcocorp.com'; 'mikem@greatplainsmfg.com'; 'jessica.christiansen@monsanto.com';
'jennifer.m.greminger@monsanto.com'; 'donna.r.farmer@monsanto.com';
'shea.w.murdock@monsanto.com'; 'Erik.jacobs@monsanto.com'; 'richard@aradc.org';
'Warren.Richardson@Pioneer.com'; 'gregory.lamka@pioneer.com'; 'Natalie.l.hubbard@CGR.dupont.com';
'alavigne@amseed.org'; 'lnichols@amseed.org'; 'mark.trostle@cpsagu.com'; 'scensky@soy.org';
'bschuermann@soy.org'; tolman@ncga.com; 'stemme@ncga.com'; 'Snyder@dc.ncga.com';
'dparker@cotton.org'; 'kmenchey@cotton.org'; 'bnorman@cotton.org'; 'eruckert@mwe.com';
'John.abbott@syngenta.com'; 'patrick.mccain@syngenta.com'; 'Janis.mcfarland@syngenta.com';
'Amy.S.Dugger-Ronyak@basf.com'; 'maximilian.safarpour@basf.com'; 'julie.schlekau@valent.com';
'sue.shen@valent.com'; 'LDA@pollinator.org'; Kunickis, Sheryl; Epstein, David; 'marion.law@hc-sc.gc.ca';
'margherita.conti@hc-sc.gc.ca'; 'mary.mitchell@hc-sc.gc.ca'; 'Richard Gupton,'; (b) (6)
;
'deansarahp@johndeere.com'; 'paul.hoekstra@syngenta.com'; 'khalid.akkari@basf.com';
'timothy.mahl@basf.com'; rmcallister@croplifeamerica.org; 'Clive Halder';
'daniel.j.jenkins@monsanto.com'; 'kklotzbach@aem.org'
Subject: Update regarding Meeting on September 18, 2013, 3:00-4:30 pm, regarding Pollinator
Protection/Alternative Seed Lubricant Issue -- Room S-4370-80 Potomac Yards South
This is a follow-up to the August 23 email from Dr. Steven Bradbury, Director, Office of Pesticide
Programs, (attached) inviting your participation to a meeting/conference call on Wednesday, September
18, 2013, from 3:00-4:30 Eastern, regarding Pollinator Protection/Alternative Seed Lubricant Issue.
Please note the meeting will be held in S-4370/80 of Potomac Yards South, 2777 Crystal Drive,
Arlington, VA.
When you arrive to sign in with Security, please contact one of the following individuals who will escort
you to the meeting on the 4th floor of our building. (Please note that you should try to arrive a little
early to make sure you have enough time to get through Security.)
Thomas Moriarty, 703/305-5035
Debra Rate, 703/306-0309
There will be some additional EPA staff in the lobby to try to assist with escorting you to this meeting.
The conference line for this meeting is as follows:

1 866 299-3188
Code 703 308 4775 #
If you have any questions, please let me know. thanks.
Margie Fehrenbach
703 308-4775
Mention of trade names or commercial products in this report is solely for the purpose of
providing specific information and does not imply recommendation or endorsement by
the U.S. Department of Agriculture.
This publication reports research involving pesticides. It does not contain
recommendations for their use nor does it imply that uses discussed here have been
registered. All uses of pesticides must be registered by appropriate State and/or Federal
agencies before they can be recommended.
The U.S. Department of Agriculture (USDA) prohibits discrimination in all its programs
and activities on the basis of race, color, national origin, age, disability, and where
applicable, sex, marital status, familial status, parental status, religion, sexual orientation,
genetic information, political beliefs, reprisal, or because all or part of an individuals
income is derived from any public assistance program. (Not all prohibited bases apply to
all programs.) Persons with disabilities who require alternative means for communication
of program information (Braille, large print, audiotape, etc.) should contact USDAs
TARGET Center at (202) 720-2600 (voice and TDD). To file a complaint of
discrimination, write to USDA, Director, Office of Civil Rights, 1400 Independence
Avenue S.W., Washington, D.C. 20250-9410, or call (800) 795-3272 (voice) or (202)
720-6382 (TDD). USDA is an equal opportunity provider and employer.
Cover: Honey bee with full pollen sacs on a flower. Courtesy of David Cappaert,
Michigan State University, http://www.bugwood.org.
CCD Steering Committee Members
USDA Agricultural Research Service (co-chair)

Kevin Hackett
USDA National Institute of Food and Agriculture (co-chair)
USDA Animal and Plant Health Inspection Service
Robyn Rose
Colin Stewart
Alan Dowdy
USDA National Agricultural Statistics Service
Bruce Boess
LaKeya Jones
USDA Natural Resources Conservation Service
Doug Holy
David Epstein
Thomas Steeger
Thomas Moriarty
Allen Vaughan
Executive Summary
This report describes research progress on Honey Bee Colony Collapse Disorder during
2011. Mandated by Congress in the 2008 Farm Bill [Section 7204 (h) (4)], this fourth
annual report represents the work of a large number of scientists from 8 Federal agencies,
2 State departments of agriculture, 22 universities, and several private research efforts.
In response to unexplained losses of U.S. honey bee colonies that began to be reported in
2006 as a condition named Colony Collapse Disorder (CCD), USDAs Agricultural
Research Service (ARS) and National Institute of Food and Agriculture (NIFA) led a
collaborative effort to define an approach for characterizing and resolving the problem;
this effort resulted in the CCD Action Plan in July 2007. Many universities and Federal,
State, and private organizations helped develop the plan and, through 2011, continued to
carry out work to address CCD.
A survey of managed honey bee colonies found overall losses of 22 percent on average
during winter 2012 (October 2011 to April 2012), down from losses of approximately 33
percent reported in 2010. In general, in the years since CCD began to be reported, winter
losses have been averaging around 33 percent, of which approximately one-third was
attributed to CCD. Many factors could be involved in the lower level of overall losses in
2011, including the mild winter weather in many parts of the United States. Nevertheless,
the overall proportion of winter losses is still high, and the continued economic viability
of pollination by honey bees remains threatened.
Although a number of factors continue to be associated with CCD, including parasites
and pathogens, poor nutrition, pesticides, bee management practices, habitat
fragmentation, and agricultural practices, no single factor or pattern of factors has been
proven to be the cause of CCD.
Some recent scientific evidence appears to indicate that some pesticides may have
sublethal effects on honey bees; however, the relevancy of some of these effects to
estimating overall risks to honey bees is uncertain. In early 2010, ARS held a workshop
with the U.S. Environmental Protection Agency to discuss how the potential effects of
pesticides could be better documented in laboratory and field-based studies. ARS
scientists and others have been examining whether pesticide-related effects may correlate
with CCD incidents or other bee health problems.
The CCD Steering Committee is examining the current accumulation of knowledge
concerning CCD and has begun the process of identifying new and relevant research
needs to determine the cause or causes of CCD and how other factors or specific
combinations of factors contribute to declining pollinator health. Scientists, beekeepers,
growers, and other stakeholders have been invited to convene in October 2012 to update
the CCD Action Plan for the next 5 years (20132017). Participants in the October
meeting will consider the development of strategies to address the multiple factors (
parasites and pathogens, poor nutrition, pesticides, and bee management practices)
associated with diminished pollinator health in general, rather than focus exclusively on
honey bees and CCD.
Research continued in 2011 in the four topic areas outlined in the 2007 CCD Action Plan.
The studies encompassed honey bee and pollinator losses in general, not just CCD.
Progress in the four topic areas is highlighted below.
Topic I: Survey and Sample Data Collection. Surveys continued to provide

evidence of high honey bee losses due to a combination of CCD and declines in
pollinator health. Research has shown that weak colonies had overall higher
pathogen levels and evidence of pesticide residues, although no pattern of specific
pathogens or pesticides was indicated. Colonies in comparatively good health also
contained a wide range of pesticide residues.
Topic II: Analysis of Existing Samples. Previously, viruses and other pathogens
and parasites were found to be present at greater levels in colonies affected by
CCD than in those not affected by CCD. Studies in 2010 revealed several new
viruses and other pathogens affecting honey bees. Additional studies to determine
whether these new pathogens are involved in CCD-affected hives are continuing.
Attempts to Recreate CCD Symptomology. CCD was initially characterized by
the rapid loss of adult worker bees from the colony, lack of dead worker bees in
or immediately outside of the hive, and delayed invasion of hive pests.
Researchers have observed that the Varroa mite and other pathogens such as
Nosema may be contributing factors to CCD, although these occur at levels that
are typically considered below economic damage thresholds. Researchers
continued their efforts to document whether correlations exist between overall
colony health and the presence of Varroa mites, diverse pathogens, and
pesticides.
Topic IV: Mitigation and Management Preventive Measures. Two national
multiyear projects, the ARS Area-wide Project on Honey Bee Health and a NIFAfunded Coordinated Agricultural Project, progressed in developing management
strategies to combat bee losses. The Bee Informed Partnership
(http://beeinformed.org), sponsored by NIFA, continued to examine bee
management practices and facilitate communication among beekeepers of
practices that reduce colony losses while promoting bee health. The eXtension
Community of Practice (www.extension.org/bee_health) also continued to
disseminate information on honey bee health and management practices. A
National stakeholders meeting scheduled for October 1517, 2012, is intended to
identify management practices for the different factors affecting honey bee health.
The Natural Resources Conservation Service has revised its appropriate
conservation practices to include more concern for pollinator protection, and the
agency continues to encourage landowners to provide quality pollinator habitat.
Colony Collapse Disorder

2011 Annual Progress Report
This is the fourth annual report prepared in response to a requirement in the 2008 Farm
Bill, Section 7204 (h) (4), which directed the Secretary of Agriculture to
submit to the Committee on Agriculture of the House of Representatives and the
Committee on Agriculture, Nutrition, and Forestry of the Senate an annual report
describing the progress made by the Department of Agriculture in:
(A) Investigating the cause or causes of honey bee colony collapse; and
(B) Finding appropriate strategies to reduce colony loss.
Background and Highlights of Research
After the large-scale, unexplained losses of managed honey bee (Apis mellifera L.)
colonies began in the United States during the winter of 20062007, researchers
identified a set of symptoms that were termed Colony Collapse Disorder (CCD). In
response to these continued losses, Federal and State government, university, and private
researchers led by the Department of Agricultures (USDAs) Agricultural Research
Service (ARS) and National Institute of Food and Agriculture (NIFA) mobilized to define
an approach to CCD, an effort that resulted in the formation of the CCD Steering
Committee and publication of the CCD Action Plan in July 2007. As of 2011, the CCD
Steering Committee included representatives from various USDA offices, including
ARS, NIFA, Animal and Plant Health Inspection Service (APHIS), Natural Resources
Conservation Service, National Agricultural Statistics Service, and Office of Pest
Management Policy; and the Environmental Protection Agencys (EPAs) Office of
Pesticide Programs. In addition, many public and private organizations are actively
working to remedy CCD.
CCD is a complex syndrome that has been hard to define and combat. Thus, developing
effective solutions to the problem requires a considerable commitment of Federal
resources.
During the past 5 years (20062011), numerous causes for CCD have been proposed and
examined. Many potentially associated factors have been identified throughout the course
of research, a number of which appear to have a high correlation with the pattern of CCD
incidents. However, the strength of these associations has varied considerably, and it has
become increasingly clear that no single factor is responsible for the syndrome. In
addition, research has not been able to determine whether all cases of CCD are caused by
the same set of factors or the same factors in a particular combination.
Independent studies have shown that bees are exposed to a wide range of pesticides.
Pesticides found in colonies range from those used to control pathogens or pests that
adversely affect honey bees, to commercial agricultural products. A survey of bees,
honey, and comb for the presence of 170 pesticides or pesticide residues performed in
2010 did not find any pattern of exposure that correlated with CCD incidents, which
would be expected if pesticides were a major factor in causing CCD. The pesticides
detected with the greatest frequency and in the largest quantities were those used by
beekeepers to control Varroa mites. Pesticide effects on bees continue to be a subject

area of intense research.
Other data indicate that some pesticides at high concentrations interact with other
pesticides, honey bee parasites, or pathogens in ways that significantly increase
individual bee mortality rates. Further studies are needed to ascertain whether these
synergistic effects occur at environmentally relevant concentrations or whether managed
honey bee colonies are commonly exposed to these levels of pesticides.
In addition, some studies have shown that exposure to certain pesticides can have
sublethal deleterious effects on bee behavior. However, while individual bees were found
to be adversely effected by sublethal exposure to some pesticides under experimental
conditions, further studies are needed to show whether a colonys abilities to pollinate
crops, produce honey, and maintain overall population are compromised by a specific
sublethal effect of pesticide exposure on individual bees.
In an effort to address the multiple factors associated with pollinator declines, the CCD
Action Plan was organized under four areas: (1) survey and sample data collection; (2)
analysis of existing samples; (3) research to identify factors affecting honey bee health,
including attempts to recreate CCD symptomology; and (4) mitigation and preventive
measures. Summaries of research under each of the four topic areas are presented below.
A survey of beekeepers throughout the United States was jointly conducted for the fifth
consecutive year by the Apiary Inspectors of America and ARS with additional assistance
this year from the Bee Informed Partnership.1 Total average losses of honey bee colonies
for winter 20112012 (October 2011April 2012) were 22 percent, which is lower than
previous surveys performed between 2007 and 2010.2 CCD is characterized by a sudden
dwindling of bees as winter turns to spring with a queen, some brood, and a few nurse bees
remaining in the hive, but at levels below those needed (10,000 bees) for a colony to survive
as it begins to forage and rear brood. The unusually warm 20112012 winter could be one
contributing factor to the drop in colony losses, although no direct scientific research has
been performed to discern whether a connection exists between weather and CCD. The
National Oceanic and Atmospheric Administration reported that January 2012 was the
fourth warmest January on record.
Of beekeepers responding to the survey who reported losing any colonies, 37 percent said
they lost at least some of their colonies with no dead bees present, which is indicative of
CCD (http://beeinformed.org/2012/05/winter2012/).
1
Bee Informed, sponsored by NIFA, is an extension project that is trying to decrease the winter mortality
of managed honey bee colonies.
Average losses were 31 percent during the 2007 winter, 35 percent in 2008, 29 percent in 2009, 34
percent in 2010, and 30 percent in 2011.
APHIS continued its survey of beekeepers in 34 States to detect exotic pests and diseases
of honey bees. The survey conducted thus far has not detected Apis ceranae, the Asiatic
honey bee; the slow paralysis virus, which has been reported in Australia; or the parasitic
mite Tropilaelaps, which is commonly found in Asia on several species of honey bees; so
these pests have likely not invaded the United States. Nosema ceranae, a microsporidial
pathogen that was recently introduced into the United States, was the dominant species of
Nosema detected. N. ceranae has been tentatively linked in some studies as contributing
to CCD in the United States, although no conclusive evidence has been found.
In the 2007 CCD Action Plan, USDAs National Agricultural Statistics Service (NASS)
was called on to expand its survey of apiaries used for honey production into a
comprehensive survey of honey bee colony production and health, including measuring
colony losses. NASS has not carried out such a survey because funds have not been
appropriated for that purpose.
A series of colony samples collected from throughout the United States in 2006 and 2007
was further analyzed using DNA sequencing in an effort to detect the presence of exotic
or novel pathogens that might have been overlooked in studies that were conducted in
2007.3
Analysis of a broad set of healthy and CCD-affected hives did not reveal a sole causative
agent but rather a host of viral, bacterial, and fungal pathogens that occurred at higher
levels in CCD-affected hives.4
Recent efforts by Cornman and colleagues4 did not identify a single unique pathogen that
could be a CCD causative agent, but the data did lend support to earlier studies
suggesting that whereas a complex set of pathogens may be involved in the cause of
colony losses, no single pathogen can be solely linked to CCD.
Attempts to Recreate CCD Symptomology
Research efforts jointly supported by ARS and NIFA continue to investigate numerous
factors alone or in combination that may play a role in causing CCD. These include
parasites and pathogens, pesticides, poor nutrition, bee management practices, and to a
lesser extent, other pests such as the small hive beetle (Aethina tumida).
Cox-Foster DL, Conlan S, Holmes EC, et al. Metagenomic survey of microbes in honey bee Colony
Collapse Disorder. Science. 2007:318;283.
Cornman RS, Tarpy DR, Chen Y-P, Jeffreys L, Lopez D, Pettis JS, vanEngelsdorp D, Evans JD.
Pathogen webs in collapsing honey bee colonies. PloS One. (In press.)
The Varroa destructor mite remains one of the primary threats to honey bee health.
Several new and existing Varroa mite control agents are being tested by ARS researchers
that may help to control these mites:
A new chemical product is in the final year of testing for overall efficacy. This
product holds great promise but is still proprietary and unavailable at this time.
A new product, Apivar (Vto-pharma, Villebon-sur-Yvette, France), which
contains the active ingredient amitraz (a nonsystemic acaricide and insecticide),
has been tested by ARS researchers. Apivar was found to have good efficacy, and
there were no observed adverse bee health issues. The ARS laboratory in
Beltsville, MD, is proposing residue testing for approval by the EPA to support
efforts to register the pesticide in the United States for use overwinter (i.e., not
during honey flow, which is that period in the year when one or more major
sources of nectar are in bloom).
A relatively new product, HopGuard,5 which uses beta plant acids from hops
plants, has been formulated and is now in commercial production. There is no
evidence to suggest that the product harms bees or broods, and it leaves no
residue. It is highly effective in reducing mite populations when applied to
colonies without capped brood (covered brood cells in which bee larvae and
pupae are present), or in package bees (a screen box that includes a queen and
worker bees). Because multiple applications are needed, HopGuard is being used
primarily by hobbyists who have more time than commercial beekeepers to attend
to colonies; however, research is underway to develop a slow-release formulation
acceptable to all operations.
Pesticide Effects
Field exposure of pollinator insects, including honey bees, to pesticides at both lethal and
sublethal levels continues to be a concern. Extensive discussions have occurred in the
media and among researchers about whether pesticides are a significant threat to
pollinators. In particular, exposure to pesticide-contaminated dust from abrasion of
certain pesticide-treated seed (e.g., corn) during spring plantings appears to have negative
effects on individual honey bees in experimental (laboratory and field) settings. Dust
collected from within mechanized planters during spring planting has been shown to
contain pesticide concentrations in parts per thousand (i.e., concentrations 1 million times
greater than parts per billion).6 However, there are no data to indicate that bees are
exposed to residue levels in the environment that even approach those measured in the
seeding equipment. Researchers have not yet determined how honey bees and other
pollinators react when exposed to environmentally relevant levels and whether a
significant number of bees would likely be present in or around fields that are planted or
seeded. Also, recent advances in seeders are reducing the hazard associated with
pesticide-contaminated dust.
5
HopGuard is produced by BetaTec Hop Products (Washington, D.C.) under a Cooperative Research and
Development Agreement with ARS.
6
Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K. Multiple routes of pesticide exposure for honey
bees living near agricultural fields. PLoS ONE. 2012;7(1): e29268. DOI: 10.1371/journal.pone.0029268.
In study results published in 2012,7 exposure of individual, immature honey bees to

sublethal levels of neonicotinoids resulted in increased susceptibility to the gut pathogen
Nosema, although the response was not concentration dependent. The colonys overall
health, population, ability to gather nectar, and pollinate were not affected by these
sublethal effects on individual bees, but this study does demonstrate that there are
complex interactions among various factors that could contribute to weakening individual
bees and making them more susceptible to additional perturbations.
When pesticides are viewed in aggregate on a national scale, residues of pyrethroids (a
large class of man-made pesticides similar to the natural pesticide pyrethrum produced
from Chrysanthemum flowers) pose a threefold greater hazard to bee colonies than
neonicotinoids, based on mean and frequency of detection in pollen samples and relative
acute toxicity.8 The synthetic pyrethroid detected in the highest quantity and frequency in
honey bee colonies that is used by beekeepers to control Varroa mite is tau fluvalinate.9
Because pyrethroids are nonsystemic, adoption of agricultural practices that mitigate
exposure should be pursued. Additionally, when honey bees were challenged with both
pesticides and Varroa mites, they showed increased immune response.10 Additional
studieson diet and pathogen interactionsrevealed that nutrition could modulate viral
infections.11
Nutrition and Nosema Effects
There were significant efforts in 2011 to determine the effects and outcomes of feeding
honey bee colonies commercial diets and supplements, especially as a support for
overwintering colonies. Many of the commercial diets were determined sufficient to
increase brood production and adult bee populations. A new pollen substitute
(MegaBee, S.A.F.E. R&D, distributed by Dadant & Sons, Inc., Hamilton, Ill.) is now in
commercial production. When MegaBee is fed in liquid or solid form, it stimulates brood
production and immune response at levels comparable to those when honey bees are fed
pollen alone.
Pettis J, vanEngelsdorp D, Johnson J, Dively G. Pesticide exposure in honey bees results in increased
levels of the gut pathogen Nosema. Naturwissenschaften. 2012;99:153158.
Frazier JL, Frazier MT, Mullin CA, Ashcraft S. Pesticides and their involvement in Colony Collapse
Disorder. Am Bee J. 2011;August:779784.
Mullin C, Frazier M, Frazier J, Ashcraft S, Simonds R, vanEnglesdorp D, Pettis J. High levels of

miticides and agrochemicals in North American apiaries: implications for Honey Bee Health. Plos One.
2010;5(3):39754.
10
Gregorc A, Evans JD, Scharf M, Ellis JD. Gene expression in honey bee (Apis mellifera) larvae exposed
to pesticides and Varroa mites (Varroa destructor). J Insect Physiol. 2012;April 9 [Epub ahead of print].
11
DeGrandi-Hoffman G, Chen Y, Huang E, Huang M. The effect of diet on protein concentration,

hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.) J Insect
Physiol. 2010;56:11841191.
Stakeholders have called for a study of the epidemiology of N. ceranae, the establishment
of economic damage thresholds, and the testing of new products for efficacy in treating
Nosema. At this point, only a single product, the antibiotic fumagillin,12 is commercially
available to control Nosema. Some beekeepers use it as a prophylactic for Nosema
infections when treatment is not warranted. To date, no treatment thresholds have been
established for the use of the antibiotic, and new guidance on its use is needed to prevent
target species resistance that can develop with the continued use of a single product.
Several additional products for Nosema control were tested by ARS scientists in
Weslaco, TX, but none have yet been found to be effective.
Land Use/Pollinator Effects
Honey bees are essential pollinators for many crops, but in light of CCD and other new
threats that have arisen in the last 15 years, researchers have begun assessing the use of
alternative insects such as bumble bees (Bombus sp.) and blue orchard bees (Osmia
lignaria) to serve as crop pollinators. Unfortunately, even as this research is occurring,
new problems in insect management have arisen. For example, a recent study
demonstrated a high degree (7393 percent) of cross-infection of viruses between honey
bees and native bumble bees.13 Thus, it is possible that co-infections and reinfection
pathways may develop, thereby complicating the use of alternative pollinators.
Topic IV: Mitigation and Management Measures
Research to resolve CCD and improve the overall health of pollinator insects is being
undertaken primarily through the ARS Area-wide Project on Honey Bee Health and the
NIFA Coordinated Agricultural Project (CAP). Funding from ARS and NIFA, with
additional contributions by the National Honey Board, the Almond Board of California,
Burts Bees, Hagen-Dazs, the North American Pollinator Protection Campaign, Project
Apis m. (PAm), and the Foundation for the Preservation of Honey Bees has supported a
variety of new studies. Results from these research efforts continue to be published.
The eXtension14 Web site (http://www.extension.org/bee%20health), established in 2010,
is providing reliable, research-based information to beekeepers and the general public,
among other resources.
A new NIFA-funded CAP, the Bee Informed Partnership (http://beeinformed.org), is
endeavoring to decrease the number of managed honey bee colonies that die each winter
12
Fumagillin, a complex biological molecule, was isolated in 1949 from the bacterium Aspergillus
fumigates. It is used today as an antimicrobial agent.
13
Singh R, Levitt AL, Rajotte EG, et al. RNA viruses in Hymenopteran pollinators: Evidence of inter-taxa
virus transmission via pollen and potential impact on non-Apis Hymenopteran species. PLoS ONE.
2010;5(12): e14357. DOI: 10.1371/journal.pone.0014357.
14
The eXtension initiative is an internet-based educational partnership of 74 Land Grant universities in the
United States that operates under the auspices of the eXtension Foundation, which broadly functions as part
of NIFAs Cooperative Extension System.
by helping determine which management practices are working best to keep bees alive. It
will also examine various data collections to assess pest and disease levels in an effort to
bridge the gap between research and extension and present the best management
information. In addition, the Bee Informed Partnership has joined ARS and the Apiary
Inspectors of America in carrying out the annual survey of winter losses of managed
honey bee colonies that have occurred since 2007.
A Bee Team has been established at the University of California Cooperative Extension
office in Oroville, CA, with funding from the CAP program, the University of Minnesota,
National Honey Board, and Almond Board of California. The goal of the team is to help
beekeepers monitor diseases and arthropod pests and select for more disease- and miteresistant breeder stocks. The Bee Team will test for hygienic behavior (i.e., behavior in
which mite-infested brood are removed from the hive), the presence of Varroa mites, and
Nosema spp. in at least 50 colonies at each participating bee breeders operation three
times each year. Data from the samplings will be provided to each bee breeder to help
them make informed decisions on choosing breeder queens and appropriate treatments.
The bee breeders have agreed to pay a fee for these services so that in the future, the Bee
Team can be self-sustaining. If this model is determined to work well, the Bee Team
hopes to establish similar teams to assist queen producers in the Southeast and other parts
of the United States.
Finally, another NIFA-funded CAP program has published a best management practices
guide, educational videos, and health bulletins for beekeepers. These materials are also
available through the Bee Health Community Page
(http://www.extension.org/bee health), which serves as a repository of peer-reviewed,
credible scientific information for the bee community.
In an effort to provide healthy habitat for all pollinators, the Natural Resources
Conservation Service has revised appropriate conservation practices to include concern
for all pollinators, and it is encouraging landowners to include in their conservation seed
mixes and practices vegetation that will provide desired forage for pollinators from early
spring to late fall.
Summary
While research has developed new scientific information about CCD and honey bee
health and management in general during the past 5 years, the complex problems of
maintaining a strong pollinator industry have only grown more complicated. What is
clear is that researchers must look beyond simple one-factor causes of bee decline and
losses. This research is multifactoral and more challenging. In light of the complexities
involved in pollinator health, research continues to seek scientific facts on bee health and
ultimately to safeguard the health of the countrys critical pollinators.
David Epstein on April 1, 2013

From the Conference report for your consideration:
Research into CCD and poor colony health has been unable to identify a unique causative agent but
consensus is building that a complex set of stressors and pathogens can cause colony losses.
Acute and sublethal effects of pesticides on honey bees have been increasingly documented, and are a
primary concern. Further tier 2 (semi-field conditions) and tier 3 (field conditions) research is required to
establish the risks associated with pesticide exposure to U.S. honey bee declines in general.
The most pressing pesticide research questions lie in determining the actual field-relevant pesticide
exposure bees receive and the effects of pervasive exposure to multiple pesticides on bee health and
productivity of whole honey bee colonies.
However, it is not clear, based on current research, whether pesticide exposure is a major factor
associated with U.S. honey bee health declines in general, or specifically affects production of honey or
delivery of pollination services. It is clear, however, that in some instances honey bee colonies can be
severely harmed by exposure to high doses of insecticides when these compounds are used or via drift
onto flowers that are attractive to bees.
It is also clear, based on chemical analysis of bees and bee products, that exposure of bees to a gamut
of pesticides is commonplace, but the level of exposure to any particular pesticide is generally not
enough to immediately or acutely kill bees (Mullin et al, 2010).
Laboratory tests on individual honey bees have shown that field-relevant, sublethal doses of some
pesticides have effects on bee behavior and susceptibility to disease. However, it remains a challenge to
measure the effects of low-level, field-relevant exposure where it matters most: in real honey bee
colonies. The social complexity of honey bees and the uncontrollable aspects of field research present
substantial challenges to determining pesticide effects in whole-colonies. While experiments using
whole colonies have the potential to directly address the effects of pesticides on honey production and
pollination services, challenges presented by field or semi-field experiments include:
Many colonies are needed per treatment due to high variability between honey bee colonies
The actual levels of exposure to pesticides that bees receive are still a big question
Computer modeling of colony demographics following pesticide exposure shows promise in linking the
results of laboratory-based pesticide studies with pesticide effects on whole-colony health.
From:
To:
Subject:
Date:
Attachments:
Kunickis, Sheryl
Epstein, David
FW: SANCO seed treatment draft guidance document - Comments by Friday 7 February 2014
Tuesday, January 28, 2014 7:29:15 AM
Seed GD SANCO 10553 2013 ver Jan 2014.doc
See below.
From: Keigwin, Richard [mailto:Keigwin.Richard@epa.gov]

To: Kunickis, Sheryl
Subject: FW: SANCO seed treatment draft guidance document - Comments by Friday 7 February 2014
Fyi
In case you havent seen this.
From: Steeger, Thomas

To: Brady, Donald; Keigwin, Richard; Rossi, Lois
Cc: Laws, Meredith; Moriarty, Thomas; Pease, Anita
Subject: FW: SANCO seed treatment draft guidance document - Comments by Friday 7 February 2014
As you may be aware, the European Commissions Directorate General for Health and Consumers
(DG SANCO) has released a draft guidance for evaluating/marketing treated seeds in the European
Commission (attached). Member states are being requested to comment on the draft guidance;
SANCO is accepting comments [on the guidance] until early February 2014. The guidance alludes to
risk mitigation options that are still evolving and refers to specific provisions for neonicotinoid seed
treatments:
- the seed coating shall only be performed in professional seed treatment facilities. Those
facilities must apply the best available techniques in order to ensure that the release of dust
during application to the seed, storage, and transport can be minimized,
- adequate seed drilling equipment shall be used to ensure a high degree of incorporation in
soil, minimization of spillage and minimization of dust emission,
- the conditions of the authorization, include, where appropriate, risk mitigation measures to
protect honey bees and other non-Apis pollinators.
- monitoring programs are initiated to verify the real exposure of bees to the active substance
in areas extensively used by bees for foraging or by beekeepers, where and as appropriate.
- Conditions of use shall include risk mitigation measures, where appropriate.
The guidance also recommends elements that should be considered in evaluating potential risks
associated with treated seeds including an assessment of the potential for generating dust. Some of
the recommendations in the draft SANCO guidance are consistent with the international standards
proposed by industry (e.g., ISO/CD 17962) and with the best management practices identified in the
PMRAs guidance entitled Pollinator Protection: Reducing Risk from Treated Seed.
Also, the Pollinator Partnerships Corn Dust Research Consortium (CDRC) has completed a
preliminary analysis of research results related to dusts generated during the planting of treated
corn seed. The CDRC is planning to release some general observations/recommendations from this
research, but believes that additional research is needed to determine the efficacy of alternative
lubricants in reducing dusts during planting of treated corn seed as well as understanding the
potential for pollinator exposure to such dusts. The Pollinator Partnership will soon release a
request for proposals (RFP).
EUROPEAN COMMISSION
HEALTH & CONSUMER PROTECTION DIRECTORATE-GENERAL
Safety of the food chain
Chemicals, contaminants, pesticides
SANCO/10553/2012
January 2014
Draft
Authorisation of Plant Protection Products for
Seed Treatment
COMMISSION GUIDANCE DOCUMENT - DOES NOT NECESSARILY REPRESENT THE VIEWS OF THE
COMMISSION SERVICES
Table of content
Table of content ...................................................................................................................................... 3
1
Introduction........................................................................................................................... 1
Treatment, placing on the market and labelling of treated seeds........................................ 2

2.1 Treatment of seed .......................................................................................................................2
2.2 Placing on the market of treated seeds in the EU .......................................................................2
2.3 Treatment of seeds for export outside the EU ............................................................................3
2.4 Labelling of treaded seeds ...........................................................................................................3
Risk Mitigation measures ...................................................................................................... 5
Evaluation and authorisation process ................................................................................... 6

4.1 Zonal evaluation ..........................................................................................................................6
4.2 Dossier content............................................................................................................................7
4.3 Guidance documents ...................................................................................................................7
4.4 Quality check of seed treatment process and treated seed .......................................................7
Physico-chemical properties ................................................................................................. 8

5.1 Guidance ......................................................................................................................................8
Analytical methods ................................................................................................................ 9

6.1 Guidance ......................................................................................................................................9
Efficacy ................................................................................................................................ 10
7.1 Guidance ................................................................................................................................... 10
Residues............................................................................................................................... 11
8.1 Guidance ................................................................................................................................... 11
Occupational health assessment......................................................................................... 12

9.1 Guidance ................................................................................................................................... 12
9.2 Exposure assessment................................................................................................................ 12
9.3 Treatment of seeds................................................................................................................... 12
9.4 Sowing of treated seeds ........................................................................................................... 13
9.5 Exposure to dust ....................................................................................................................... 13
10
Environmental exposure ..................................................................................................... 15
10.1 Guidance ................................................................................................................................... 15

10.2 Emissions to the environment from seed treatment processes .............................................. 15
10.3 Sowing of treated seeds ........................................................................................................... 15
10.4 In-field environmental exposure .............................................................................................. 16
10.4.1
Leaching to ground water ............................................................................................. 16
10.4.2
Exposure to surface water............................................................................................. 16
10.4.3
Exposure to soil ............................................................................................................. 16
10.5 Exposure resulting from dust drift deposition ......................................................................... 18

10.5.1
Seed quality parameters and dust drift......................................................................... 18
10.5.2
Choice of the appropriate seed quality values for risk assessment .............................. 20
10.5.3
Standard 2-D ground deposition exposure assessment................................................ 22
10.5.4
Standard 3-D exposure assessment .............................................................................. 25
10.5.5
Leaching to ground water ............................................................................................. 26
10.5.6
Exposure of surface water from dust drift deposition .................................................. 27
11
Risk assessment non-target organisms ............................................................................... 28

11.1 Guidance ................................................................................................................................... 28
11.2 Birds and mammals .................................................................................................................. 28
11.3 Aquatic organisms .................................................................................................................... 28
11.4 Bees .......................................................................................................................................... 29
11.5 Non-target arthropods ............................................................................................................. 29
11.6 Soil organisms ........................................................................................................................... 31
11.7 Non-target terrestrial plants .................................................................................................... 32
12
References ........................................................................................................................... 33
Appendices ............................................................................................................................................ 35
Appendix I
Standardised GAP seed treatment ......................................................................... 36
Appendix II
Overview of maximum seed sowing rates for different crops ............................... 41
Appendix III
Seed quality parameters regarding dust drift for maize, oil seed rape, cereals and
sugar beet ............................................................................................................................ 42
A
Maize ................................................................................................................................... 42
Oil seed rape........................................................................................................................ 45
Cereals ................................................................................................................................. 47
Sugar beet ........................................................................................................................... 49
Appendix IV Overview of field studies considered for the derivation of dust deposition values
from treated seed. Detailed study description - see Appendix VII .................................... 52
Appendix V
2D Dust ground deposition after sowing treated maize, oil seed rape, cereals and
sugar beet seeds.................................................................................................................. 55
A
Maize ................................................................................................................................... 55
Oil seed rape........................................................................................................................ 57
Cereals ................................................................................................................................. 58
Sugar beet ........................................................................................................................... 59
Adjustment of dust ground deposition for the sowing width of the treated field ............. 61
Appendix VI
Estimation of an extrapolation factor from 2D to 3D off-field dust deposition ..... 63
Appendix VII
Detailed description of dust drift exposure studies (2D / 3D) ................................ 64
Study 1 (JKI/ 0905)............................................................................................................... 64
Study 2 (JKI/ 1008)............................................................................................................... 67
Study 3 (JKI/ 1115)............................................................................................................... 70
Study 4 (JKI/ 1205)............................................................................................................... 73
Study 5 (JKI/ 1122)............................................................................................................... 76
Study 6 (JKI/ 0822)............................................................................................................... 79
Study 7 (JKI/ 1224)............................................................................................................... 81
Study 8 (IVA-DUST 1) ........................................................................................................... 84
Study 9 (IVA-MAIZE-DUST 1) ............................................................................................... 90
Study 10 (IVA-OSR-DUST 1) ................................................................................................. 94
Study 11 (IVA-OSR-DUST 2) ................................................................................................. 97
Study 12 (IVA-SB-DUST 1) .................................................................................................. 100
Study 13 (Nikolakis, 2009) ................................................................................................. 102
Appendix VIII Recommendations on studies for the derivation of seed quality parameters
regarding dust drift............................................................................................................ 107
A
Amount of dust (Heubach dust) ........................................................................................ 107
Content of active substance in Heubach dust ................................................................... 107
Appendix IX
Effects on non-target organisms comparison of exposure via dust drift to
sprayed residues................................................................................................................ 108
Appendix X
Good practices and quality standards for the treatment of seeds and for the use of
treated seeds ..................................................................................................................... 110
A
Seed treatment process .................................................................................................... 111
Handling steps ................................................................................................................... 113
Drilling machines ............................................................................................................... 114
Recommendations for the employment of pneumatic seed drillers ................................ 117
Drilling conditions .............................................................................................................. 120
Raising Good Practice awareness throughout the value chain ......................................... 121
Conclusions and recommendations .................................................................................. 122
Appendix XI
Appropriate risk mitigation phrases ..................................................................... 125
Appendix XII Coating practices: Representative coating practice and conditions of use of coated
seeds within the EU ........................................................................................................... 126
References in the Appendices ........................................................................................................ 129
1 Introduction
The purpose of this guidance document is to provide for a harmonised implementation of the
different provisions of Regulation (EC) No 1107/2009 which are related to the treatment of seeds
with plant protection products. Firstly, it intends to harmonise the implementation of the provisions
of Regulation (EC) No 1107/2009 on the placing on the market and the labelling of treated seeds.
Secondly it intends also to provide guidance for the performance of the risk assessment and the
application of the criteria for the purpose of authorisation of plant protection products for seed
treatment. In particular risks related to exposure to dust are addressed. Further information and data
related to the risk assessment is presented in appendices.
References to articles in the present guidance document should be read as references to articles in
Regulation (EC) No 1107/2009. This guidance is without prejudice to EU legislation on the placing on
the market of plant reproductive material. For the purpose of this guidance document seed is
defined as seed intended for sowing and for any cultivation purpose, including pre-germinated or
primed seed.
The guidance document is applicable also for bulbs and tubers, although for the time being no
specific guidance for the risk assessment is included.
Not included in the definition of seed in this guidance document are:
Other types of propagating material such as seedlings, plantlets and any other part of
plants used for the production of a new plant.
Treated compost on which seed is placed prior to covering with compost in a modulebased system.
Seeds intended for consumption or processing (grain).
Any type of granule (although many general principles for the risk assessment might be
used for granules as well.
2 Treatment, placing on the market and labelling of treated seeds

2.1
Treatment of seed
According to Article 28(1) a national authorisation is required for the use of a plant protection
product for seed treatment in that Member State. This is comparable to any other use of a plant
protection product, such as for example foliar treatment of a crop. The resulting treated seeds are
not considered as plant protection products.
Article 2(1) states that the Regulation applies to the products intended for one of the uses listed in
the provision and especially to protect "plants or plant products against all harmful organisms or
preventing the action of such organisms, unless the main purpose of these products is considered to
be for reasons of hygiene rather than for the protection of plants or plant products" [Article 2(1)(a)].
Article 3(5) defines "plants" as "live plants and live parts of plants, including fresh fruit, vegetables
and seeds". Therefore, the treatment of seeds is considered as one of the possible uses of plant
protection products and the notion of "use" covers the treatment of seeds and not the sowing of
treated seeds.
The treatment of seeds must be done in the Member State in which the product used for the
treatment has been authorised. This implies that an undertaking producing, for instance, treated
seeds in Member State A cannot treat them with a product authorised in Member State B.
Furthermore, the Implementing Regulations approving the active substances might include
conditions concerning the use of a plant protection product for the treatment of seeds.
2.2
Placing on the market of treated seeds in the EU
Article 49 (Placing on the market of treated seeds) of the Regulation, lays down rules on the
marketing of seeds treated with plant protection products. Article 49(1) provides that Member
States shall not prohibit placing on the market and use of seeds treated with plant protection
products authorised for that use in at least one Member State. Therefore Member States may not
impose any ban on the marketing of treated seed, if the seed has been treated with a plant
protection product that is authorised in at least one Member State for the treatment of that seed.
However, where there are substantial concerns that treated seeds are likely to constitute a serious
risk to human or animal health or to the environment and that such risk cannot be contained
satisfactorily by means of measures taken by the Member State(s) concerned, Article 49(2) provides
that the Commission shall immediately take measures to restrict or prohibit the use and/or sale of
such treated seeds. Before taking such measures the Commission will examine the evidence and may
request an opinion from the European Food Safety Authority (EFSA).
The placing on the market and use of seeds treated with plant protection products that has not been
authorised in any Member State is not specifically addressed. However, this behaviour is considered
contrary to the objectives of Regulation (EC) No 1107/2009. The fact that Article 49, paragraph 2, is
referring only to the treated seeds mentioned in the first paragraph of the provision means that only
seeds "treated with plant protection products authorised for that use in at least one Member State"
can be placed on the market and used in the Union. As a consequence, seeds treated with a plant
protection product not authorised in any Member State should not be placed on the market.
2
In the case where seeds are treated with a plant protection product that is no longer authorised in
any Member State, these treated seeds do not benefit from free movement within the EU under
Article 49(1). Therefore the economic operator cannot invoke Article 49(1) in case other Member
States would refuse to place such treated seeds on the market.
2.3
Treatment of seeds for export outside the EU
There are no special EU rules for the treatment of seeds destined to export outside the EU. The use
of a plant protection product to treat seeds in Member States is subject to authorisation. Article 28
states the following: A plant protection product shall not be placed on the market or used unless it
has been authorised in the Member State concerned in accordance with this Regulation. The
derogation in Article 28(2)(d) concerns the production, storage or movement of a plant protection
product intended for use in a third country. This means that for the treatment of seeds in the
Member States only an authorised plant protection product may be applied, even if the treated seed
is destined for export outside the EU.
Moreover, Article 67 establishes obligation for all professional users of plant protection products to
keep, for at least three years, records of the plant protection products they use, containing the name
of the plant protection product, the time and the dose of application, the area and the crop where
the plant protection product was used. This provision applies to the operator which is treating seeds
with plant protection products in the EU.
2.4
Labelling of treaded seeds
For labelling and packaging obligations, it is important to distinguish between the provisions
applicable to plant protection products and to treated seeds. Plant protection products shall be
labelled as required under Commission Regulation (EC) No 547/2011. The standard phrases for
special risks provided in Annex II to that Regulation supplements the phrases provided for in
Directive 1999/45/EC 1 on classification, packaging and labelling of dangerous preparations.
Concerning treated seeds one should refer to Article 49(4) of Regulation (EC) No 1107/2009 in which
rules concerning the labelling of treated seeds are set out. According to this provision, the
documents and the label accompanying the treated seeds (not on the official label for seed
certification) shall include:
the name of the plant protection product;
the name of the active substance of the product;
standard phrases for safety precautions as provided for in Directive 1999/45/EC and
risk mitigation measures set in the authorisation of that plant protection product where
appropriate.
'Standard phrases for safety precautions as provided for in Directive 1999/45/EC' should be read as
referring to 'Safety advice (S phrases)' referred to in Article 10 paragraph 2.6 of this Directive. The
wordings of the safety precautions applicable to the plant protection product applied on the seed
1
OJ L 200, 30.7.1999, p. 1.
can be found in Annex IV of Directive 67/548/EEC on the classification, packaging and labelling of
dangerous substances 2. Article 49(4) of Regulation (EC) No 1107/2009 does not impose to place on
the label the danger symbol provided for in Directive 67/548/EEC nor to report the hazard
pictograms listed in Regulation (EC) No 1272/2008 on the classification, labelling packaging of
substances and mixtures 3. Directive 1999/45/EC will remain in force until 1 June 2015. After this
date, Regulation (EC) No 1272/2008 will apply.
The safety phrases put on the label of the seed packages should be limited to the ones that are
applicable to handling and sowing treated seed.
The language of the label for treated seed is important for local farmers and growers. As provided in
Regulation (EC) No 547/2011 for plant protection products, Member States may make the placing on
the market of treated seeds in their territories subject to their being labelled in their national
language or languages. Finally, Article 49(4) of Regulation 1107/2009 does not provide for reduced
labelling obligations for small packages. Therefore the labelling obligations apply independently of
the size of the package.
OJ 196, 16.8.1967, p. 1.
OJ L 353, 31.12.2008, p. 1.
3 Risk Mitigation measures

In order to inform users of dangers and precautions to be taken, authorisations should include the
risk mitigations measures which are destined to be on the label of seed packages. Besides generic
risk mitigation measures to be set for all seed treatments and seeding operations with treated seed
through appropriate legislation, additional product and use specific ones might be set when
authorising the plant protection products.
To facilitate the free circulation of seeds, these mitigation measures should be harmonised into a set
of standard phrases. National agricultural practices and environmental conditions need to be
considered when doing this. It is therefore important that until such a list is established concerned
Member States take the opportunity to comment on the labelling proposed in the Draft Registration
Report for plant protection products intended for seed treatment.
For example Commission Implementing Regulation (EU) 485/2013 amending specific provisions
relating to clothianidin, thiametoxam and imidacloprid states that Member States shall ensure that:
the seed coating shall only be performed in professional seed treatment facilities. Those
facilities must apply the best available techniques in order to ensure that the release of dust
during application to the seed, storage, and transport can be minimised,
adequate seed drilling equipment shall be used to ensure a high degree of incorporation in
soil, minimisation of spillage and minimisation of dust emission,
the conditions of the authorisation, include, where appropriate, risk mitigation measures to
protect honey bees and other non-Apis pollinators.
monitoring programmes are initiated to verify the real exposure of bees to the active
substance in areas extensively used by bees for foraging or by beekeepers, where and as
appropriate.
Conditions of use shall include risk mitigation measures, where appropriate.
It is acknowledged that both drilling equipment and weather conditions may vary from one Member
State to another. Machinery and risk mitigation measures also evolve over time. Thus it is important
that knowledge is updated constantly and shared between Member States, so that they may adapt
their specific recommendations based on the state of the art and in the most harmonized way.
The decision to issue the corresponding recommendations, or product specific labelling, is a Member
State responsibility, although it does not preclude from agreeing on a common tool box for risk
management measures. It is therefore recommended that a website is developed, which would
contain all the necessary information and scientific resources on risk management tools that are
available for implementation in Member States or under development.
Examples of appropriate phrases for risk mitigation measures are given in Appendix XI.
4 Evaluation and authorisation process

4.1
Zonal evaluation
According to Article 33 (2)(b) the EU is considered as one zone concerning the assessment of
applications for authorisation of plant protection products for seed treatment. When a plant
protection product is authorised for seed treatment in a certain Member State, the treated seeds can
be freely traded to, and used in all EU Member States. This means that for both the treatment of
seeds, and the sowing of the treated seeds, Member States are dependent on the assessment carried
out by another Member State.
The procedure for the evaluation and authorisation of the product intended for seed treatment is the
same as for other plant protection products. However, for seed treatment there is only one zonal
Rapporteur Member State (zRMS) for the whole EU which evaluates the application and prepares the
Registration Report taking account of all conserned Member States. The procedures outlined in the
Guidance document on zonal evaluation and mutual recognition under Regulation (EC) No
1107/2009 SANCO/13169/2010 should be followed and the other concerned Member States shall
decide on authorisations or not on the basis of the conclusions of the assessment of the zRMS. To
ascertain harmonised assessments and free movement of seeds within the EU it is important that not
only those Member States with an application for authorisation, but also those where the treated
seeds may be placed on the market and used, participate in the evaluation by means of commenting
on the Draft Registration Report.
In the evaluation process of a plant protection product for seed treatment the following
differentiations need to be considered:
a) Evaluation and authorisation of the product intended for seed treatment.
b) Evaluation of the treatment process of seed (covered by operator exposure studies and
model calculation).
c) The sowing process in the field.
General points of attention for the risk assessment for the EU as one zone includes:
a)
Sowing practice (e.g. density, depth, and incorporation) differs between different kinds
of seeds and also between Member States. For the environmental risk assessment this
means that exposure concentrations may differ among Member States.
b)
Risk mitigation measures, e.g. equipment to reduce the drift at sowing, may differ
between Member States.
c)
Dissipation/degradation in soil, water, plant and invertebrate material differs between

regions in EU which may result in different predicted environmental concentration in the
soil.
4.2
Dossier content
The dossier submitted with an application for authorisation of plant protection product for seed
treatment should, besides fulfilling the data requirements in Regulation (EU) No 283/2013 and
Regulation (EU) No 284/2013, reflect the fact that the resulting treated seeds can be freely traded to,
and used in all EU Member States. Hence, a risk assessment regarding the sowing of the treated
seeds in all Member States where the crop could potentially be cultivated should be part of the
dossier. The agricultural practices and environmental conditions in those Member States need to be
considered.
Specifications on the seed quality as regards to dust abrasion and the amount of active substance in
abraded dust should be provided. This would be the basis for the risk assessment for operators,
bystanders and non-target organisms regarding exposure to dust. The acceptable maximum Heubach
value e.g. g dust/ha and active substance content (a.s. % in dust released from the treated seeds)
could be set in the authorisation, if applicable. Further details are given in section 9.5.
4.3
Guidance documents
The risk to human and animal health and the environment should be assessed using the relevant
existing guidance documents. Where such guidance is lacking methods are proposed in the present
guidance document.
4.4
Quality check of seed treatment process and treated seed
Recognised guidance documents should be used to assess the quality of the seed treatment process
and the quality of the treated seed (rules developed at national level or by stakeholders). The
assessment should include:
a) a quality scheme addressing delivery and storage of plant protection products,
preparation of seed treatment mixture, application of the seed treatment, drying and
packaging of treated seeds, labelling, waste management
b) harmonised protocols for the determination of dust values
c) definition of maximum dust values as general quality standard for different seed types
d) harmonized protocols for the determination of the active substance quantity in abraded
dust
e) an audit system to control the practices performed for seed treatment
In order to increase the quality of seed treatment, certification of seed treatment facilities is an
appropriate procedure. Where high quality standards are to be ensured, e.g. in order to reach
acceptability criteria in risk assessment procedures, the treatment of seeds in certified seed
treatment facilities might be a management requirement. Further information on the seed treatment
process and certification systems is given in Appendix X.
5 Physico-chemical properties
5.1
Guidance
For the assessment of physic-chemical properties of plant protection products intended for seed
treatment, no additional guidance is needed in most areas. The assessment is covered by the current
system (Manual on Development and Use of FAO and WHO Specifications for Pesticides, current
edition and Croplife International: Technical Monograph No. 17). One exception is the determination
of the amount of dust that can be abraded during handling and sowing of treated seeds.
Dust and abrasion tests (e.g. Heubach-test) have been introduced or specifically adapted since
several years and standard operation procedures are commonly available (see Appendix X). The
Heubach method is considered as reliable for maize, oil seed rape and sugar beet seed and has
recently also been intensively tested for seed of other cereal (small grain) species.
Dust abrasion tests generate data on the amount of dust particles of given sizes (e.g. < 200 m in
Heubach test). Small particles are considered most relevant for risk characterization, because they
are most prone for drifting and residue content has been shown to be highest in small sized particles.
Therefore, so called Heubach-values that give the amount of fine dust per sown area may be used
as surrogate values to describe the amount of dust released during drilling of treated seeds. The
active substance content of the dust (a.s. %) should also be given. However, further testing should be
performed in future to understand the relationship between coarse and fine dust amounts for
different seed types and the importance of coarser dust particles for exposure assessment.
6 Analytical methods
6.1
Guidance
Analytical methods are covered by the following guidance:

'Technical Material and Preparations: Guidance for generating and reporting methods of analysis in
support of pre- and post-registration data requirements for Annex II (part A, Section 4) and Annex III
(part A, Section 5) of Directive 91/414.SANCO/3030/99 and Guidance document on pesticide residue
analytical methods SANCO/825/00)'.
When treated seeds are used in Member States other than the zRMS, residue analytical methods
need to be available for enforcement purposes (for both environment and consumers) for these
Member States. Therefore, residue analytical methods should be submitted and evaluated, by the
zRMS, even if the treated seed is used for trade to other EU Member States only. Regarding
measurements of residues in abraded dust, it needs to be ensured that the method for analysing
residues in air is adapted to include this.
7 Efficacy
7.1
Guidance
For the assessment of the efficacy of plant protection products applied as a seed treatment no
additional guidance is needed. The guidance is covered by EPPO standards that are regularly
discussed and updated on expert level.
10
8 Residues
8.1
Guidance
No residues are expected in the harvested product for the majority of uses as seed treatment,
although residues cannot be excluded. Properties of the active substance, such as its systemic
properties and metabolic behaviour, the dose rate and the growth rate of the crop might determine
whether residues are (still) present at the time of harvest. Therefore, a complete residue dossier
should in general be provided for crops used for consumer and livestock products.
Seed treatment is described in the current EU guidance for the assessment of residues: Guidelines
for the generation of data concerning residues as provided in Annex II part A, section 6 and Annex III,
part A, section 8 of Directive 91/414/EEC concerning the placing of plant protection products on the
market, Appendices A-I. Special data sets are needed for metabolism (i.e. application by seed
treatment or soil treatment, appendix A of the EU guidance). Furthermore, a separate extrapolation
table for supervised residue trials is applicable to seed treatment (table 5 of Appendix D).
For seed treatment, the EU is considered as one zone and the evaluation should therefore take into
account the use of treated seeds in all Member States where these could be sown. For residues
there is a requirement for trials to be carried out in northern and southern zones. This means that
residue trials performed according to worst critical GAP in each of these zones cover the uses in the
entire EU. For the other aspects (like storage stability, metabolism and feeding in livestock, MRL
setting) the same procedures and guidance apply as to foliar applications.
11
9 Occupational health assessment

9.1
Guidance
In 2010, the EFSA Panel on 'Plant Protection products and their Residues' have prepared a draft
scientific opinion on the preparation of a Guidance Document on pesticide exposure assessment for
workers, operators, bystanders and residents. The finalisation of the Guidance Document is expected
in 2013.
Data developed by industry has been included in a model called SEEDTROPEX, which estimates
operator exposure during several activities of seed treatment, such as calibration, mixing/loading,
cleaning, and bagging of seeds. These data cover static and mobile seed treatment units. The
SEEDTROPEX model includes also monitoring data of forklift drivers to assess background exposure
of subjects being not directly involved in the seed treatment process. However, the data are owned
by a Task Force and are not publicly available. Moreover, the data are applicable for certain types of
seed and certain circumstance only. Additionally, it appears that different versions of the
SEEDTROPEX model exist. The draft EFSA GD on pesticide exposure does not propose the use of the
SEEDTROPEX model, and concludes that the SEEDTROPEX data should be used in the same way as
other ad hoc data sets.
9.2
Exposure assessment
For the human risk assessment, three distinct aspects should be considered:
a. risk assessment of people involved in the treatment (treating or coating) of seeds with
plant protection products;
b. risk assessment of people handling the treated seeds during the sowing activities, and
c. risk assessment of people located in the vicinity of the sowing site (the so-called
bystander) or working or living in the vicinity of the sowing site (the so-called resident).
A first tier assessment for operator and worker exposure is generally based on models. Where no
satisfactory model is available for an exposure scenario, or the initial risk assessment using a
conservative model gives inadequate reassurance of safety, the applicant may generate higher tier
exposure estimates through an ad hoc study specific to the circumstances in which the pesticide will
be used (EFSA, 2010).
9.3
Treatment of seeds
The treatment of seeds with plant protection products is usually performed by highly specialized
operators in a (semi-) industrial environment. However, some seeds e.g. cereal, oil seed rape and
grass seed are sometimes treated by farmers using less automated equipment or with mobile
processing equipment of contractors. Workers may then be exposed to treated seed during the seed
treatment process, e.g. mixing, calibration and bagging.
12
9.4
Sowing of treated seeds
Workers are potentially exposed to plant protection products when they load the equipment with
treated seeds. Workers, bystanders and residents could be exposed during the actual sowing, and
this exposure is therefore relevant for risk assessment.
Dermal adsorption and inhalation are the main routes of exposure during sowing. Dermal exposure
to plant protection products can occur via contact with the treated seeds and contaminated
equipment, or through deposition on the skin. Inhalation exposure may occur as a result of drift from
particles abraised from seeds, and additionally from solid or dried plant protection products from the
treated seeds that become airborne or from soil contaminated with residues from treated seeds. The
secondary drift from contaminated soil is however not considered relevant for the farmer, plant
growers and worker exposure.
Oral exposure may occur secondarily to dermal exposure, through hand to mouth transfer. This is
especially relevant for infants or toddlers playing on contaminated surfaces. However, maximum
potential exposure by this route is generally assumed to be negligible in comparison with that via the
skin and by inhalation.
9.5
Exposure to dust
Dust drift from treated seeds during sowing is the main source of airborne exposure. The seed
treatment process has an influence on the resulting amount of dust in the end product (bags with
seeds). Adequate processes for treatment of seed have a positive impact on minimizing dust
abrasion. For example, only dust free seeds should be used. Any dust produced during the process
should be sucked off and dust should also be sucked off before packing (preferably on dry seeds).
Additives such as binders have a positive impact on the dust formation during the sowing activities.
However, aging of the treated seeds can have a negative impact on the dust formation during the
sowing.
Studies performed by the Julius Khn-Institut (JKI) in Germany show that a considerable amount of
fine dust (< 0.5 mm) may be present in bagged seeds. The pesticide residue has been determined in
both fine and coarse dust present in the seed bags. In fine dust the residue content was around 2030%, while in coarse dust it was around 10 to 15%. The amount of residue is influenced e.g. by the
content of the active substance in the formulation and the application rate. Highest dust levels were
measured in maize, while lower levels were found in rape seed, sugar beet, carrot and onion. Barley,
wheat, triticale and rye also contained a relatively large amount of both fine and coarse dust in seed
bags. Differences were seen between coating facilities and crop type.
The European Seed Association (ESA) has drawn up guidance for proper seed treatment facilities and
adequate seed drilling equipment. Advice on safe use of treated seed is also given to workers,
farmers and plant growers. The recommendations in the ESA guidance are targeted at minimizing the
environmental risks linked to abraded dust from treated seeds (STISSC & ESA, 2010). However, no
clear specifications on adequate equipment are given (see Appendix X for the ESA guidance).
Workers, farmers and plant growers should avoid exposure as much as possible. Care should be
taken not to shake the dusts off the bags or to load the dust in the bottom of bags into the driller.
Hand contacts with the seeds in the hopper, for example with the aim to spread the seeds, should be
13
avoided. During loading operations they must have appropriate individual protection. Clear water
should be available on the tractor to rinse any dusts they could come in contact with and to rinse
gloves after loading. Rinsed gloves should then be removed. In case where a re-loading of the drilling
machine is necessary, the turbine of the driller should be stopped. During sowing operations wind
direction and wind speed must be considered to avoid contamination of surrounding areas.
For data on dust drift at sowing see chapter 9, which may be applicable also for assessment of risk to
bystanders and residents.
14
10 Environmental exposure
10.1
Guidance
For the calculation of predicted environmental concentrations (PEC) in different environmental

compartments resulting from treatment of seeds and sowing of treated seeds, already available
guidance documents should be followed in most cases. Two exceptions are calculations of in-field
PEC for soil and off-field exposure from deposition of dust. A proposal for calculation of in-field PEC
for soil is given in 10.4.3, and for the estimation of exposure from dust drift deposition for the
different off-field compartments a summary is given in chapter 10.5.4. Details of the rationale behind
the dust drift risk assessment (available data, study descriptions and experimental data treatment)
are included in Appendix III to Appendix VII.
The assessment schemes and measures described below are of preliminary nature since the data
base available is still small. Guidance will be improved as soon as a broader data base will be
available.
10.2
Emissions to the environment from seed treatment processes
The environmental risk assessment regarding emission and effects on non-target organisms resulting
from the coating process of seeds needs a harmonised evaluation method. Currently, no method is
available but preliminary guidance to minimize emission and environmental exposure from seed
treatment facilities is given in Appendix X.
10.3
Sowing of treated seeds
As the amount of plant protection product used per units of seeds together with the seeding rate per
ha determine the dose level in gram active substance per crop area, high seed densities could result
in higher residues. This is especially true for the in-field area. Therefore, experimental data for the
exposure assessment of specific products should be generated according to the worst case seed
density in the EU as indicated in the GAP-table (risk envelope approach).
Indicative maximum sowing rates per hectare for different crops are given in Appendix II. Clearly,
there are differences in drilling practice within Europe and the use of seeds treated with one product
might lead to lower exposure in regions with low seed densities than in another with higher sowing
rates per hectare.
The type of driller used during the sowing process, highly influences the amount of dust released
from the treated seeds and emitted in the environment. For example, dust drift is lower from
mechanic drillers than from pneumatic machines, particularly if vacuum equipment is used. Further
information on technical driller equipment is provided in Appendix X. Additional specific guidance on
good practices for the use of treated seeds and the sowing process is also given in Appendix X.
15
10.4
In-field environmental exposure
10.4.1
Leaching to ground water
Calculations of predicted environmental concentrations in ground water (PECgw) are currently

covered by FOCUS GW (FOCUS 2009) with a crop interception value of 0 combined with application
made on the date of planting/sowing and incorporation into the soil over the top centimetre (cm).
10.4.2
Exposure to surface water
The exposure to surface water due to run-off and drainage is covered by FOCUS SW (FOCUS 2001).
For calculation of PECsw values due to dust drift deposition see chapter10.5.6.
10.4.3
Exposure to soil
Pending the on-going revision of the Guidance Document on Terrestrial Ecotoxicology it is proposed
to calculate PECsoil for large seeds in a different way than for small seeds. For small seeds that are
densely sown, the PEC value should be calculated assuming equal spread over the top 5 cm. For large
seeds with a low sowing density the worst case PECsoil may be in the direct surrounding of the seed
kernel. For an adequate risk assessment a refined approach may therefore be needed.
A division in small and large seeds is therefore proposed.
Small seeds
For small seeds (diameter <0.5 cm) PEC can be calculated in the same way as for spray applications.
For spray formulations the homogeneous distribution of the active substance in the top 5 cm layer of
the soil is considered. For the calculation of the predicted initial environmental concentration (PIEC)
interception is taken into account but disappearance routes such as evaporation, photochemical
transformation and microbial degradation are not. The volume of soil with a layer thickness of 5 cm
of a hectare is 500 m3, and the mass of the soil is 750*103 kg (at a bulk density of 1500 kg/m3). The
dose of active substance divided by the mass of the soil then yields a measure for the acute exposure
of soil organisms (= PIEC).
Large seeds
For seeds with a diameter larger than 0.5 cm which are sown at low density at a depth of 5 cm or
deeper, an alternative PEC sphere calculation methodology for the soil compartment is proposed. A
scenario as presented below should be followed (Figure 10-1). The scenario assumes that the treated
seed has a spherical shape. In practice, larger seeds will usually be spherical once they are treated.
For treated seeds that are not spherical the maximum radius could be used as a conservative
approach.
16
Table 10-1:
Description of parameters.
Input
Description
Unit
radius of sphere of influence of the seed
radius of the seed
seed density
ha-1
Dose
kg a.s. ha-1
dry bulk density of the soil
kg m-3
volume of the sphere of influence of a seed
m3
Vseed
volume of a seed
m3
total volume of soil within the sphere of influence of

the seeds on a hectare of soil
m3 ha-1
total mass of soil within the sphere of influence of

the seeds on a hectare of soil
kg ha-1
Predicted Initial Environmental Concentration
mg a.s./ kg soil
Intermediates
Output
PIEC
10.5
Exposure resulting from dust drift deposition
The aim of this chapter is to provide guidance on how to calculate PEC values in different
environmental compartments arising from dust deposition after sowing seeds treated with plant
protection products. As will be discussed below, seed quality parameters do influence the amount of
dust emitted during sowing and also the amount of active substance emitted with dust. In contrast to
off-field exposure assessment for sprayed products, the application rate in-field is not (alone)
determinant of off-field exposure. The quality parameters important for the correct assessment of
the dust drift resulting from sowing of treated seeds are elucidated in the next chapters, together
with guidance on how to address different regulatory scenarios in the risk assessment of products
submitted for authorization.
10.5.1
Seed quality parameters and dust drift
The emission of dust from treated seeds during seeding is variable, depending upon the care taken
during all the steps; from the preparation of seeds before treatment, up to the type of driller used
(see chapter 10.3 and Appendix X). For the purpose of this guidance document it is assumed that
pneumatic machines are equipped with pertinent devices ensuring dust deflection to soil.
The exposure of non-target organisms in off-field areas will in general depend on the amount of dust
abraded from treated seeds and emitted during sowing. However, not only the mere amount of dust
will be determinant of exposure, but also the content of active substance (a.s.) in the abraded dust
18
that will deposit off-field. The parameters amount of dust and content of active substance in dust
and the relationships between them are therefore decisive for the off-field exposure assessment.
The amount of dust that is easily abraded from treated seeds can be measured with standard test. In
this guidance, it is usually referred to dust amounts as measured with the Heubach test method.
These data give the amount of fine dust (<200 m approx.) per seed unit and are recalculated as to
account for the specific thousand grain weight and seeding density (see Appendix III). Therefore, the
Heubach value refers to the amount of dust per sown area (e.g. g dust/ha).
The active substance content (in % a.s.) in Heubach dust released from treated seeds is deemed to
be determined by the active substance dose applied per seed unit. However, the data base available
up to now does not allow for this general conclusion. A relationship between dose applied and
content of a.s. in dust can only be seen when the dressing technique is rather simple (e.g. for cereals,
see Figure A- 5 in Appendix III). However, when the coating process is rather complex, as for example
in maize, the relationship between dose applied and a.s. content is fogged by other parameters (e.g.
seed variety, seed coating and cleaning, use of sticker, colours etc., subsequent dressing of several
products and additives). No relationship is evident between Heubach values (g dust/ha) and active
substance content of the dust (a.s. %). This means that the percentage of active substance in the dust
does not change as a function of the amount of abraded dust (see Appendix III). Moreover, when
lowest feasible Heubach values for a specific seed crop are approached, technical limits might lead to
high concentration of active substance in the remaining dust.
From the considerations above it must be concluded that no general, constant relationships can be
described between dust amounts (Heubach values) and the active substance contents (%) in dust
from treated seeds on the one hand and the seed dressing or field application rates on the other
hand. This has further significant implications for the assessment of the risk arising from the sowing
of treated seeds, since the seed quality parameter Heubach value (g dust/ha) and active substance
content (a.s. % in dust) do drive the deposition rates of active substances in the off-field, and not the
application rate in-field (see chapter below).
To facilitate the risk assessment procedure regarding dust abraded from treated seeds, a proxy
parameter is defined that best describes and aggregates the seed quality parameter described above
in terms of emission of contaminated dust. This variable is the amount of active substance released
with Heubach dust per sown area (Heubach a.s. in g a.s./ha) and can directly be employed in the
determination of predicted environmental concentrations in non-target areas:
Heubach a.s. (g a.s. in dust/ha ) =
Heubach value (g dust/ha ) a.s. (% in dust )

100
where
a.s. =
active substance
Heubach value = amount of abraded fine dust (<200 m) in g per seed unit or sown area (ha)
Since the variable Heubach a.s. (g a.s. in dust/ha) combines different parameters, similar seed
qualities in terms of active substance released per sown area can be achieved by varying both the
19
amount of dust emitted (Heubach value) and the content of active substance in the dust (a.s. % in
dust).
Regarding this aggregate variable, high amounts of active substance in dust Heubach a.s. (g a.s. in
dust/ha) are generally associated to high Heubach values (g dust/ha). This means that the more dust
is abraded, the more active substance is abraded with the dust and no dilution of the active
substance occurs. The relationship can be steep or gentler depending on dressing rate, seed quality
and the dressing process of single breeder or facility. When several variables in the dressing process
are kept constant, a tight correlation might emerge (e.g. for oil seed rape seeds, see Appendix III).
10.5.2
Choice of the appropriate seed quality values for risk assessment
In order to assess the risk for non-target organisms in off-field areas arising from the sowing of
treated seeds, the seed quality parameters determinant for exposure should be known or correctly
estimated.
Generally, one out of the following regulatory scenarios applies:
A) The applicant seeking for authorization has submitted sufficient, reliable and representative
data regarding the relevant quality parameter of the product to be assessed
product specific risk assessment
B) The quality parameters regarding the treated seeds to be assessed have to comply with legal
requirements laid down by the European Union or single Member States (e.g. some MS
legislations on treated maize seeds). The compliance with minimum data requirements is
established through certification of the seed treatment facilities
risk assessment on the basis of currently defined reference values
C)
No legal requirements apply and/or no quality data are available or certified regarding the
treated seeds to be assessed
risk assessment on the basis of defined worst case values
Table 10-2 lists reference and worst case values for the amount of dust released during sowing
(Heubach value; g dust/ha), the content of active substance in the fine Heubach dust (% a.s. in
dust) and the aggregate parameter amount of active substance released during sowing (Heubach
a.s.; g a.s. in dust/ha) for widely used crops types (i.e. maize, oilseed rape, cereals, sugar beet). The
list will be amended for other crop seeds as soon as data will become available. The data base
employed to derive reference and worst case values is described in Appendix III. Data analysis and
derivation of aggregated standard statistical location parameter (e.g. mean/maximum values,
percentiles) follows in principles the approach adopted in the derivation of drift arising from spray
applications (e.g. Ganzelmeyer & Rautmann 2000). The choice of the appropriate regulatory scenario
is a management decision.
Regarding Heubach values (in g dust/ha), reference values for several crop seeds exists that are met
by certified seed treatment facilities. Figures in Appendix III show the distribution of measured values
over dust amount classes for several crops. The reference values were set in the range of the 90th
percentile of the available data. Worst case values were estimated from the maximum determined
20
values. The definition of reference values for Heubach dust can be amended as soon as seed
treatments and certification of seed treatment facilities progress.
Regarding the content of active substance in Heubach dust (% a.s. in dust), the data base is less
comprehensive. As described in the previous chapter, the intuitive relationship between content of
active substance in the dust and the seed dressing rate is not always detectable.
In the case of treated cereal seeds and oilseed rape seeds, a good correlation is given and it is
possible to derive values for the content of % a.s. in the dust when knowing the seed dressing
rate (Appendix III for regression analyses).
By contrast, for maize and sugar beet, only reference and worst case values for a.s. content in
dust (%) can be given. Moreover, these do only cover the range of available seed dressing data
(Maize approx. max. 150 g a.s./ha, sugar beets max. 60 g a.s./ha; see Appendix III). If products
with very low dressing rates are applied, then reference values might overestimate the content
of a.s. in dust. In this case, product specific data would help refine the exposure estimate.
For every refinement of reference or worst case values and for all crop seeds that are not described
in Table 10-2, data regarding typical Heubach values (g dust/ha) and active substance content (% a.s.
in dust) should be delivered by applicants for the specific products to be assessed. Appendix VIII gives
guidance on minimum quality requirements for studies aimed at data refinement.
21
Table 10-2: Seed quality parameters determinant for dust drift during sowing: Amount of easily
abraded dust (Heubach value; g fine dust /seed unit or ha) and content of active
substance in abraded fine dust (% a.s. in dust) for four major crops. Given are values for
different regulatory scenarios (see text for details):
A) sufficient and reliable product specific data on seed quality parameter are submitted
B) crop specific reference values are available and certified
C) worst case if no legal requirements apply and/or no quality data available or certified
values calculated on the basis of available data (see Appendix III for list of studies).
Regulatory
scenario
Crop (reference unit)

Maize
(100,000 seeds)
Oil seed rape

(700,000 seeds)
Cereals
(180 kg/ha)*
Sugar beet
(100,000 seeds)
Heubach-value (abraded fine dust <200m)(g dust/unit seed or ha)

A) Product specific
measured
measured
measured
measured
B) Reference value
0.75
0.3
2/3.5**
0.05
C) Worst case
1.50
0.5
3/4.5**
0.10
measured or
***13% of seed
dressing rate
(g/180 kg)
measured
Content of active substance in dust (% a.s. in dust)

measured or
***25% of seed
A) Product specific
measured
dressing rate
(g/700,000 seeds)
B) Reference value
35
10
10
C) Worst case
50
25
25
10
Active substance in dust Heubach a.s. (g a.s. in dust/ha)

A) Product specific
measured
measured
measured
measured
B) Reference value
0.26
0.030
0.20
0.001
C) Worst case
0.75
0.125
0.75
0.010
* For purpose of comparison, and to derive general values, the Heubach values have been normalized to 180 kg. Since the
sowing densities are different across Europe, mean Heubach values should always be recalculated according to the
specific sowing practice.
** with/without sticker
*** see Appendix III for data analyses
10.5.3
Standard 2-D ground deposition exposure assessment
Dust drift deposition values in non-target areas were measured after sowing of representative
treated seed lots. The recorded environmental concentrations of active ingredients in non-target
areas were used to define standard values for exposure assessment of dust drift.
Ground dust drift deposition values from treated seeds at 1 m distance from field edge (defined as
PEC 2D dust ground deposition) were experimentally determined for four crops. Appendix IV lists the
field experiments evaluated; Appendix VII gives full details of the single studies. The dust deposition
22
values in two dimensional structures describe the exposure of non-target species in terrestrial
habitats but also the input in surface water bodies located at 1 m distance from the field edge (see
chapter 10.5.6).
In the field tests, the deposition in non-target areas has proven to be related to the amount of active
substance released during sowing, i.e. to the seed quality of the sown seeds as Heubach a.s. values
(g a.s. in Heubach dust /ha, see previous chapter). This means that, in contrast to the drift deposition
of sprayed formulations, the deposition of active substances with abraded dust in non-target areas is
not a straight function of the amount of applied active substance in-field, but depends strongly on
the seed quality. Values recorded in the field tests were normalised for reference or worst case seed
quality parameter, respectively, so to derive ground deposition values of active substances deposited
with dust for different regulatory scenarios. Details of the calculations are given in Appendix V. The
choice of the appropriate regulatory scenario (A, B or C, see previous chapter) depends on the actual
availability of data on the specific seed quality, the legal requirements and the enforcement of seed
treatment certifications.
As Table 10-3 shows, 2 dimensional ground deposition values (at 1 m distance from field edge) in
non-target areas are a function of the amount of active substance released during sowing i.e. of the
aggregate variable Heubach a.s. (g a.s.in dust /ha). The PEC 2D dust ground deposition can be
calculated using this relationship as expressed in the following equation. As soon as more data
become available, the table will be amended with reference and worst case values for other crops.
Please note that the listed exposure values are valid only if pneumatic suction drillers are equipped
with deflectors.
PEC 2 D dust ground deposition (g a.s. ha ) = Heubach a.s. (g a.s. ha ) crop specific deposition factor
where
PEC=
Predicted Environmental Concentration
a.s. =
active substance
Heubach a.s.=
g active substance in abraded Heubach dust per ha of sown area
Deposition factor = deposition factor determined in field studies with different crop types.
The deposition factor was calculated by regression analyses (Appendix V).
23
Table 10-3: Ground dust drift values (PEC 2D dust ground deposition) for the risk assessment of
contaminated dust in non-target areas at 1 m distance from field edge as a function of
the amount of active substance released with dust per sown area (Heubach a.s.; g a.s.
in dust/ha). Regulatory scenario:
Deposition data are derived from 8 field experiments. See text for details, Appendix V
for study descriptions and further details.
(g a.s./ha)
PEC 2D dust ground

deposition
of active substance
in off-crop areas
(g a.s./ha)
A) Product specific
Heubach a.s. values

measured
Heubach a.s. values

x 1.6
B) Reference value
0.26
0.42
C) Worst case
0.75
1.20
A) Product specific
Heubach a.s. values

measured
Heubach a.s. values

x 1.6
B) Reference value
0.03
0.05
C) Worst case
0.125
0.20
A) Product specific
Heubach a.s. values

measured
Heubach a.s. values

x 0.5
B) Reference value
0.20
0.10
C) Worst case
0.75
0.375
A) Product specific
Heubach a.s. values

measured
-*
B) Reference value
0.001
0.02
C) Worst case
0.010
-*
Regulatory
scenario
Heubach a.s. values,

active substance in dust
per sown area
Crop
Maize
Oil seed
rape
Cereals
Sugar
beets
*no sufficient data available, for details see Appendix V
24
10.5.4
Standard 3-D exposure assessment
Investigations after the bee incidents in Europe have shown that species living or foraging in 3dimensional structures like hedgerows, trees or other crops are exposed to higher deposition rates of
contaminated dust than the species living on the ground. To address this issue, an extrapolation
factor between 2-D and 3-D deposition was derived. Based on the experimental results from several
studies in different crops (see Appendix VI), a factor of 13 has been determined to exist between
residue levels of active substances in petri dishes on the soil surface and the vertical projection area
of gauze net as surrogate for natural structures. In order to comply with the rationale behind the
deposition calculations for spray drift, the proposed factor represents the median of all possible
ratios of each sampling block of residues samples 2D/3D from experimental data since it is applied
on ground deposition data that derive from 90th percentile values.
A number of non-target organisms are potentially exposed to contaminated abraded dust in 3-D like
structures. Measured or calculated 3-D dust drift values can be used for the off-field risk assessment
for these organisms like e.g. honeybees and foliar-dwelling non-target arthropods (see chapters
below). The PEC 3D dust deposition can be calculated as follows:
PEC 3 D dust deposition (g a.s. ha ) = PEC 2 D ground dust deposition (g a.s. ha ) 3D extrapolation factor
where
PEC=
a.s. =
3D factor=

active substance
extrapolation factor was determined in field studies with different crop
types to be 13. The 3D extrapolation factor describes the ratio between
dust deposition in 3D structures (measured in gauze netting) and 2D
structures (measured in Petri dishes). Please see Appendix VI for details.
25
Table 10-4: Predicted Environmental Concentration in 3 dimensional structures in non-target areas

due to deposition of dust drift after sowing treated seeds. Values are given for different
regulatory scenarios:
The extrapolation factor from 2 D deposition values to 3 D structures was determined in
9 field studies to be 13. See text and Appendix VI for details.
Regulatory
scenario
Crop
Maize
Oil seed
rape
Cereals
Sugar
beets
PEC 2D dust ground

deposition
of active substance
in off-crop areas
(g a.s./ha)
PEC 3D dust deposition

of active substance
in off-crop areas
(g a.s./ha)
measured
PEC 2D dust ground deposition
x 13
A) Product specific
measured
B) Reference value
0.42
5.46
C) Worst case
1.20
15.60
measured
x 13
A) Product specific
measured
B) Reference value
0.05
0.65
C) Worst case
0.20
2.60
measured
x 13
A) Product specific
measured
B) Reference value
0.10
1.30
C) Worst case
0.38
4.88
A) Product specific
-*
B) Reference value
0.02
0.26
-*
-*
C) Worst case
-*
*no sufficient data available, for details see Appendix V
10.5.5
Leaching to ground water
The exposure calculation to ground water from dust deposition from plant protection products
applied via treated seeds is considered to be covered by the in-field assessment.
26
10.5.6
Exposure of surface water from dust drift deposition
In relation to FOCUS SW, exposure to surface water via dust was covered by a PPR Panel Opinion that
has developed procedures to estimate dust drift deposition of Non Spray Application (NSAs) onto
surface water. However, the proposed parameterization of the model input for the entries of various
NSAs cover only granular formulations (EFSA 2004).
Since no agreed scenario in FOCUS SW (FOCUS 2001) addresses water bodies in different distances
from field edge regarding dust drift generated at sowing of treated seeds, concentrations in surface
water from dust drift deposition can be calculated in a first approximation by using the PEC 2D dust
ground deposition presented in chapter 10.5.3.
The predicted environmental concentrations in a water body located 1 m from field edge can be
calculated via the PEC 2D dust ground deposition deposited in the non-target area (in g a.s./ha)
converted into a PEC surface water dust (g a.s./L) in a standard water body as follows:
PEC surface water dust (g a.s. L ) =
PEC 2 D dust ground deposition (g a.s. ha ) 100

water volume (L m )
where
PEC=
a.s. =
water volume=

active substance
300 L/m surface area in a ditch of 1 m width, 0.3 m depth at a 1 m
distance from the field edge
27
11 Risk assessment non-target organisms

11.1
Guidance
It is not the intention of this guidance document to go into detail on the assessment of risk to nontarget organisms, since for most groups of organisms the already available guidance can be used or is
being developed. However, it should be noted that the higher tier risk assessment for the EU as one
zone will have to differentiate between Member States and/or EU-regions for several refinement
options that may differ between Member States. For example sowing practice (e.g. density, depth,
and incorporation), dissipation/degradation data in soil, water, plant and invertebrate material and
risk mitigation measures may differ between regions in EU.
11.2
Birds and mammals
Birds can be exposed to the active substance as a result from consumption of treated seeds, which is
covered in the existing guidance for birds and mammals (EFSA, 2009).
It should be noted that the higher tier risk assessment for the EU as one zone will have to
differentiate between Member States and/or EU-regions for several refinement options for birds and
mammals that may differ between Member States. This is the case for focal species and
accompanying refined PD and PT and residue decline data in soil, plant and invertebrate material.
Soil PECs may differ within the EU regulatory zones and/or regions (EFSA PPR 2012).
It is assumed that the in-field risk assessment for birds and mammals will also cover the potential
exposure via dust drift.
11.3
Aquatic organisms
Aquatic organisms could be exposed to the active substance via the soil as a result from run off and
drainage. This is covered with the existing methods (FOCUS SW). Aquatic organisms may also be
exposed to the active substance via dust drift deposition into surface water.
For the risk associated with dust drift deposition, Toxicity to Exposure Ratios (TER) can be calculated
using the PEC surface water dust values described in chapter 10.5.6, resulting in:
TER
surface water dust
Ecotoxicological Endpoint
( g a.s. L )
liquid formulation
( g a.s. L )
PEC
surface water dust
where
TER
=
a.s.
=
PEC surface water dust =
Toxicity to Exposure Ratio

active substance
Predicted Environmental Concentration after
deposition of abraded dust in adjacent water bodies
28
As long as no toxicological studies with dust in the aquatic environment are available and there is no
evidence that dust might be more toxic in water than spray droplets, the endpoints from studies with
the liquid formulations with the active substance can be used for the risk assessment.
It should be noted that the higher tier risk assessment for the EU as one zone will have to
differentiate between Member States and/or EU-regions for several refinement options (e.g.
mesocosms) and risk mitigation measures. For the risk assessment of aquatic organisms, the EFSA
Guidance on tiered risk assessment for plant protection products for aquatic organisms in edge-offield surface waters applies (EFSA 2013b).
11.4
Bees
Bees can be exposed to the active substance via dust drift at sowing and via nectar, pollen and
honeydew as a result of systemic uptake of the active substance by the plant from the treated seed.
The EFSA Guidance Document on the risk assessment of plant protection products on bees (Apis
mellifera, Bombus spp and solitary bees (EFSA, 2013a) covers in relation to seed treatment the risk to
bees from
exposure via contact to dust particles when bees are foraging in plants at the field margin
and in adjacent crop
consumption of pollen and nectar from treated crop, weeds in the field, plants in field margin
and the adjacent crop or succeeding crop/permanent crop the following year
consumption of water guttation fluid, surface water and puddles
metabolites present in pollen and nectar
Regarding data on dust drift deposition it is recommended that for the time being the guidance in
section 10.5.4 of this document is followed. Note that listed exposure values are valid only if
pneumatic suction drillers are equipped with deflectors.
11.5
Non-target arthropods
For the effect assessment on non-target arthropods other than bees, the guidance already in place
should be followed. A revision of the Guidance Document on Terrestrial Ecotoxicology, including
further consideration on protection goals and level of protection to be kept in in-field and off-field
areas is conducted by EFSA. The EFSA Opinion on Protection Goal in Risk Assessment (EFSA PPR 2010)
could also be consulted. Until the revision is complete, the currently available guidance should be
used (ESCORT 2). However, not all specific questions on the assessment of the risk arising from
treated seeds are addressed in the document. Therefore, some special points are discussed below.
When higher tier non-target arthropod field testing is performed, it should be assessed whether the
tests can be used to address the whole EU zone or just a limited area regarding the crop cultivation
area. When recovery is included in the endpoint, preferably field testing is performed. In De Jong et
al. (2010), the following is stated on this issue:
Furthermore Candolfi et al. (2000a) indicate that field studies cannot be extrapolated from Southern
European countries to Northern European countries and the other way round. This is especially valid
29
concerning recovery. Due to higher temperatures other species occur, a number of organisms have
shorter life cycles in Southern Europe, or more generations per year as compared to Northern Europe.
Non-target arthropods outside the field sown with treated seeds will be exposed to the active
substance through the deposition of abraded dust. Foliar dwelling non-target arthropods have to be
considered particularly at risk. It is considered that the realistic worst case exposure for terrestrial
invertebrates especially pollinators will not be found on the ground but in 3 dimensional spatial
structures (e.g. trees, hedges, adjacent crops) (see Appendix VI for more details). Thus, the predicted
3-D exposure data as listed Table 10-4 will be employed in the assessment of the risk for foliardwelling non-target arthropods exposed to contaminated dust. As long as no generic factors are
available for every crop, a worst case extrapolation factor of 13 is used to derive 3-D exposure data
from 2-D ground deposition data.
Because of the attractiveness of flowers to pollinators, a vegetation dilution factor is deemed to
underestimate the risk for species e.g. foraging in the outer part of a flowering hedge. Moreover,
pollinators like bees or butterflies will forage from one flower to the next and accumulate high
amount of dust. Thus, no vegetation distribution factor should be used to assess the realistic
environmental risk for non-target arthropods exposed to contaminated dust deposited in 3dimensional structures.
The very first studies on the effects of dust from treated seeds on non-target arthropods show that
the standard beneficial test species are less sensitive to dust than to the liquid seed treatment
formulation under the tested conditions. As long as no further data on the effects of dust on other
non-target arthropods are available, it is proposed to use the standard endpoint from the liquid seed
treatment formulation from the species which showed the highest sensitivity to the active substance.
At present, a problem may be that in dossiers for seed treatments usually no data for the standard
arthropod indicator species are available (Aphidius and Typhlodromus), but only for in-soil/soilsurface dwelling species (tests conducted with a.s. mixed in sand/soil). If this is the case, it should be
decided case-by-case if additional tests with the indicator species A. rhopalosiphi and T. pyri are
required (for example depending on the margin of safety with the soil dwellers and aquatic
invertebrates). Additional tests can be conducted more easily with the liquid seed treatment
formulation than not yet harmonised and validated dust laboratory tests, and is therefore
acceptable.
If the endpoint results from a glass plate or 2-dimensional study, no further considerations are
necessary, since the endpoint and the exposure in the tests represent a worst case for field
situations. However, if the endpoint results from a 3-dimensional extended laboratory test, then
regulatory decisions should be taken case by case. Further considerations should be given to the
relationship between LR50 from test with glass plates and test with natural substrates. Especially
when no standard endpoints from worst case exposure are available, results from 3-D test with liquid
formulations should be evaluated with care since the test design of a 3-dimensional (sprayed plant)
extended laboratory test is not comparable to the exposure to dust filtered out and accumulated in
3-D structure (e.g. flowers, hedgerows) and might therefore underestimate the risk.
As a higher tier approach, the standard species or other non-target species like wild bees, bumble
bees or butterflies can be tested in the non-target area with the dust from the respective seed
30
treatment formulation. As no agreed guidelines currently exist, it is recommended that the study
protocols are discussed beforehand with the regulatory authority (Appendix IX for more details).
The TER-ratio can be calculated as follows:
TER
3D dust
Ecotoxicological Endpoint
liquid formulation
(g a.s. ha )
PEC
3D dust deposition
(g a.s. ha )
where
TER
=
a.s.
=
PEC 3D dust deposition =
Toxicity to Exposure Ratio

active substance
Predicted Environmental Concentration after deposition of
abraded dust in adjacent 3-dimensional structures
A TER trigger value of 10 or 5 (Uniform principles; Regulation (EU) No 546/2011) is proposed. These
triggers are in line with the ESCORT 2 safety factors of 10 or 5 in the off-field risk assessment based
on resp. first tier and extended laboratory tests.
11.6
Soil organisms
New guidance is in development by EFSA with the revision of the Guidance Document on Terrestrial
Ecotoxicology (SANCO/10329/2002). As long as this Guidance Document is under revision, the
currently available guidance on soil organism risk assessment can be used. The EFSA Opinion on the
scenarios for selection and parameterisation for predicting environmental concentrations in soil over
Europe (EFSA PPR 2012) and the EFSA Opinion on protection goals in the risk assessment of pesticide
in in-field and off-field environments (EFSA PPR 2010) may be consulted.
Soil organisms can be exposed to the active substance via the soil. In section 10.4.3 of this guidance
document the estimation of the soil concentration resulting from treated seeds sown in the field is
elaborated. If a relevant PECsphere has been calculated that is significantly higher than the
homogenous PECsoil, the first should be used for risk assessment.
Current test guidelines with soil non-target arthropods and earthworms are based on homogenous
mixing of the test substance with the test soil. From a scientific point of view however, it is best to
have matching types of exposure and effect concentrations in the risk assessment. Therefore,
performing ecotoxicity tests (laboratory and/or field) with treated seeds could be a possible higher
tier option for the risk assessment. When higher tier field testing is performed it should be assessed
whether the tests can be used to address the whole EU zone or just a limited crop cultivation area.
Comparable climates, landscapes and crops are essential if results on recovery are to be extrapolated
from one area to another. Therefore, when recovery is included in the endpoint, preferably field
testing is performed in both Northern and Southern EU if the crop is grown in both north and south
EU. For further guidance to the comparability of conditions between given areas EPPO Standard
PP1/241(1) should be followed (EPPO 2005). The off-field risk to soil organisms is considered to be
covered by the in-field risk assessment.
31
11.7
Non-target terrestrial plants
For non-target terrestrial plants no direct exposure via the soil as a result of treated seeds is
expected. Since herbicides are not used for seed treatment a risk assessment for non-target plants
via dust is currently not considered necessary, except when (screening) data indicate that the
product may have adverse effects on plants.
32
12 References
BROWSE (2011a) Bystanders, Residents, Operators and WorkerS Exposure models for plant
protection products, Deliverable 1.1 Review of existing models and data for Operator
exposure. SEVENTH FRAMEWORK PROGRAMME
BROWSE (2011b) Bystanders, Residents, Operators and Workers Exposure models for plant
protection products, Deliverable 2.1 Overview of currently used and emerging worker
exposure models and data. SEVENTH FRAMEWORK PROGRAMME
European Commission (2013) Commission implementing Regulation (EU) No 540/2011, as regards
the conditions of approval of the active substances clothianidin, thiamethoxam and
imidacloprid, and prohibiting the use and sale of seeds treated with plant protection
products containing those active substances.
Candolfi et al. (2000a
De Jong et al. (2010),
EFSA (2004) Opinion of the Scientific Panel on Plant Health, Plant Protection Products and their
Residues on a request of EFSA related to FOCUS sw scenarios. The EFSA Journal
(2004)145,1-31.
EFSA (2009) Guidance Document on Risk Assessment for Birds & Mammals on request from EFSA.
EFSA Journal 2009; 7(12):1438. doi:10.2903/j.efsa.2009.1438.
EFSA (2010) Preparation of a Guidance Document on Pesticide Exposure Assessment for Workers,
Operators, Bystanders and Residents. EFSA Journal 2010;8(2):1501 26
EFSA (2010) Scientific Opinion on the development of specific protection goal options for
environmental risk assessment of pesticides, in particular in relation to the revision of the
Guidance Documents on Aquatic and Terrestrial Ecotoxicology (SANCO/3268/2001 and
SANCO/10329/2002). EFSA Journal 2010;8(10):1821. [55 pp.]
doi:10.2903/j.efsa.2010.1821.
EFSA (2012) Scientific Opinion on the science behind the guidance for scenario selection and scenario
parameterisation for predicting environmental concentrations in soil. EFSA Journal
2012;10(2):2562. [76 pp.] doi:10.2903/j.efsa.2012.2562.
EFSA (2013a) Guidance on the risk assessment of plant protection products on bees (Apis mellifera,
Bombus spp. and solitary bees). EFSA Journal 2013;11(7):3295, 266 pp.
doi:10.2903/j.efsa.2013.3295
EFSA (2013b) Guidance on tiered risk assessment for plant protection products for aquatic organisms
in edge-of-field surface waters. EFSA Journal 2013;11(7):3290, 268 pp.
doi:10.2903/j.efsa.2013.3290.
ESCORT 2 (2001) Guidance document on regulatory testing and risk assessment procedures for plant
protection products with non-target arthropods. Escort 2 workshop (European Standard
Characteristics of Non-Target Arthropod Regulatory Testing); MP Candolfi, KL Barrett, PJ
Campbell, R Forster, N Grandy, M-C Huet, G Lewis, PA Oomen, R Schmuck, H Vogt (eds).
SETAC, 25pp.
33
EPPO (2005) EPPO Standard PP 1/241 (1) Guidance on comparable climates. European and
Mediterranean Plant Protection Organization.
FOCUS (2000) FOCUS groundwater scenarios in the EU review of active substances Report of the
FOCUS Groundwater Scenarios Workgroup, EC Document Reference SANCO/321/2000
rev.2, 202pp].
FOCUS (2001) FOCUS Surface Water Scenarios in the EU Evaluation Process under 91/414/EEC.
Report of the FOCUS Working Group on Surface Water Scenarios, EC Document
Reference SANCO/4802/2001-rev.1. 221
Ganzelmeier, H. and D. Rautmann (2000) Drift, drift reducing sprayers and sprayer testing. Aspects of
Applied Biology, 57, 1-10
Hamey P, Byron N, Hanley L, Leslie W, Morgan N, Steurbaut W, de Backer E, Vergucht S. Project to
assess current approaches and knowledge with a view to develop a Guidance Document
for pesticide exposure assessment for workers, operators, bystanders and residents. Final
report, version 1.02. EFSA, EFSA/PPR/2007/01, 2008.
Pistorius, J., Bischoff, G., Heimbach, U. (2009) Bienenvergiftung durch Wirkstoffabrieb von
Saatgutbehandlungsmitteln whrend der Maissausaat in Frhjahr 2008. Journal fr
Kulturplanzen, 61(1). S. 9-14.
STISSC& ESA (2010) Seed Treatment Industry Stewardship Steering Committee Working Group and
the European Seed Association. Professional seed treatment facilities, Adequate seed
drilling equipment, treated seed safe use advise, April 2010.
34
Appendices
35
Appendix I
Standardised GAP seed treatment
For seed treatment the following GAP should be used.

Details of all national GAPs within each zone (to be sorted by crop)
PPP (product name/code):
Active substance(s) (name and content, g/L or g/kg):
Formulation type:
Field of use:
Zone:
1
Use- Member Crop and/

No. state(s) or situation
MS
F
G
or
I
Pests or Group of
pests controlled
Application
Method /
Kind
Timing / Growth min. Interval

between
stage of crop &
season
sowing in
greenhouse
and
transplating
to the field
I or G or F
(treatment of
seeds)
Seed treatment
at BBCH 00.
G or F
(sowing)
BBCH 00 +
G or F
(transplanting)
BBCH +
10
11
12
Application rate per treatment

ml
product /
100 kg
seeds
maximum Maximum
g as/ha
seedling
rate (kg
seeds/ha)
n.a
n.a
13
14
Remarks:
PHI
(days)
a) TGWT (Thousand grain
weight)
b)
Min/max sowing or planting

density
c)
additional remarks
n.a
(mention
months when
sowing takes
place)
(mention
months when
transplanting
place)
36
Guidance for filling the GAP table

In the GAP it should be made clear where the seed is treated, where it is sown and if the young plants are transplanted.
General remarks/explanations:
All abbreviations in the GAP-Sheet used must be explained.
Make use of existing standards like EPPO and BBCH.
Formulation:
Type:
e.g. wettable powder (WP), emulsifiable concentrate (EC), granule (GR)
see: GCPF Codes - GIFAP Technical Monograph No 2, 1989
Conc. of as:
g/kg or g/L
In case the plant protection product contains more than one active substance the amount applied for each active substance occurs in the same order as the substances are
mentioned in the heading.
Explanations to the particular columns:
No.:
Numeration would be important when references are necessary e. g. to the dossier or to the authorisation certificate.
Member state(s):
For a better general view of the valid uses for the particular zones/MS it would be helpful to mention both (the zone as well as the MS) in the column. However, to keep the
table clearly arranged it seems dispensable to cite the zone; each MS is distinctly allocated to one zone; moreover the zone(s) are cited in the head of the table.
Desirably MS are put in order accordant to the zone they belong.
Crop and/or situation:
37
The common name(s) of the crop and the EC (EPPO)-Codes or at least the scientific name(s) [EU and Codex classifications (both)] should be used; where relevant, the
situation should be described (e.g. fumigation of a structure). In case of crop groups all single crops belonging to that group should be mentioned, (either in the respective
table element or in case of a very extensive crop group - at least in a footnote).
In case of crop groups all single crops belonging to that group should be mentioned, (either in the respective table element or in case of a very extensive crop group - at
least in a footnote). If it is not possible to mention all single crops belonging to a crop group (e.g. for horticulture), it should be referred to appropriate crop lists (e.g. EPPO,
residue (codex). It would be desirable to have a joint list of crop groups for the zones.
Exceptions of specific crops/products/objects or groups of these and restrictions to certain uses (e.g. only for seed production, fodder) must be indicated.
This column should also include when indicated information concerning crop destination or purpose of crop.
Conditions / location of use:
Outdoor or field use (F), glasshouse application (G) or indoor application (I)
Glasshouse indicates that the respective trials are acceptable for all zones.
As results achieved in compartments without controlled conditions (temperature, light exposure), e.g. simple plastic tunnels [for those GAPs field trials have to be
conducted in the respective zone the use is applied for], are not considered to be applicable for use in other zones the kind of glasshouse should be clearly indicated.
[Remark: Greenhouse definitions are at the moment under evaluation].
Conditions include also information concerning the substrate (natural soil, artificial substrate).
In this column it should also be indicated, whether the product is intended for professional or for non-professional use
Pests or Group of pests controlled:
Scientific names and EPPO-Codes of target pests/diseases/ weeds or when relevant the common names of the pest groups (e.g. biting and suckling insects, soil born insects,
foliar fungi, weeds) and the developmental stages of the pests and pest groups at the moment of application must be named.
If necessary in case of pest groups - exceptions (e.g. sucking insects excluding scale insects) should be indicated.
In some cases, the set of pests concerned for a given crop may vary in different parts of the EU region (where appropriate the pests should be specified individually).
If the product is used as growth regulator the target organism is the specific cop, whose development should be influenced; the aim could also be e.g. an empty room for
treatment.
38
Application details:
Method / Kind:
Method: Seed treatment (in case of e.g. phytodrip is claimed this can also be mentioned here)
Kind: It would also be helpful to indicate whether seeds are surface broadcast or precision drilled together with depth of sowing
Timing of Application / Growth stage of crop & season:
Time(s), period, first and last treatment, e.g. autumn or spring, pre- or post-emergence, at sufficient pest density or begin of infection, including restrictions (e.g. not during
flowering).
Growth stage of crop (BBCH-code, ) period, first and last treatment.
Since the BBCH-codes are accomplished in the individual member states at different time periods the month(s) of application should be indicated in addition.
BBCH Monograph, Growth Stages of Plants, 1997, Blackwell, ISBN 3-8263-3152-4
It seems sensible to constrain specifications in this column only to the crop, - information concerning the pest should be dealt in column pest or group of Pests controlled.
In certain circumstances it might be helpful to give information about the expected rate of interception related to the BBCH codes. In many minor crops no
BBCH/interception rate scenarios have been specified so far. This could also simplify grouping for the envelope approach.
Min. Interval between sowing in greenhouse and transplating to the field
If it is relevant the number of days between sowing and transplanting to the field can be mentioned in this column
Application rate per treatment:
Application rate of the product per ha:
(Maximum) ml product rate per 100 kg seeds).
Maximum g, kg as/ha:
The dimension (g, kg) must be clearly specified by the applicant. The value in this column can be calculated if thousand grain weight and the seedling rate are known.
Maximum seedling rate (kg seeds /ha);
PHI (days) minimum pre harvest interval
PHI - minimum pre-harvest interval
39
For some crop situations a specific PHI may not be relevant. If so an explanation (e. g. the PHI is covered by the time remaining between application and harvest.) should be
given in the remarks column (e.g. crop harvest at maturity or specific growth stages).
Remarks:
Remarks may include: Extent of use/economic importance/restrictions
e.g. limiting the number of uses per crop and season, if several target pests/diseases are controlled with the same product.
TGWT (Thousand grain weight)
Min/max sowing or planting density
Additional recommendations:
For the description of uses of a PPP the following EPPO Standards should be considered:
EPPO Standard PP 1/240 Harmonized basic information for databases on plant protection products
EPPO Standard PP1/ 248 Harmonized classification and coding of the uses of plant protection products
Whereas EPPO Standard PP1/ 248 gives more general information on possible description of uses, EPPO Standard PP 1/240 especially gives an overview of all points
necessary to fully understand a use.
For EPPO-Guidelines, see: http://archives.eppo.org/EPPOStandards/efficacy.htm
For EPPO extrapolation tables, see http://www.eppo.org/PPPRODUCTS/extrapolation/tables.htm
For EPPO Plant Protection Thesaurus, see: http://eppt.eppo.org/
40
Appendix III
Seed quality parameters regarding dust drift for maize, oil seed
rape, cereals and sugar beet
The seed quality parameters amount of dust (Heubach dust) and content of active substance in
Heubach dust are introduced in chapter 10.5.1, page 19 and their relevance for off-field exposure
assessment is described. In this Appendix available data sources are summarized in order to show
the range for this two parameters and the relationship between them. The parameters are compared
for four main crop types (i.e. maize, oilseed rape, cereals, and sugar beet).
A Maize
Heubach dust (amount of dust)
Two available data sources with information of the amount of dust abrasion expressed as Heubach
value show average values of 0.30 and 0.68 g dust/100,000 maize seeds. Based on data from the
European Seed Association (ESA, 2013) the 95th percentile is below 0.70 g dust/100,000 maize seeds.
In three field experiments regarding dust drift deposition in the years 2010, 2011 and 2012 by Julius
Khn-Institut (JKI) the 90th percentile is 0.84 g dust/100,000 maize seeds. A summary is shown in
Table A- 2 and Figure A- 1.
Table A- 2: Seed quality parameter regarding dust expressed as Heubach value for treated maize
seeds
Reference
Batch (year)
Number of
batches
Heubach value
(mean)
(g dust/100,000 seeds)
Heubach value
th
(90 percentile)
(g dust/100,000 seeds)
JKI (2011,
2012a,
2013a)
2010-2012
3x4
0.68
0.84
2009-2012
2009: 2159
2010: 5273
2011: 6375
2012: 5318
0.30
0.70*
ESA (2013)
*95% of the treated seeds are below this Heubach value
42
Figure A- 2 represents as an example for maize seeds of 2012 the active substance content in
Heubach dust as a function of Heubach dust. Figure A- 2 shows data for several batches of maize
seeds all treated with the same product with the active substance Methiocarb at the same seed
dressing rate. As can be seen from the different symbols, the provenience of the seeds from different
breeders and seed treatment facilities has an influence on the amount of dust released from the
seeds as well as on the amount of active substance in the abraded dust. A broad range of active
substance content in dust can be seen in the data -from low values to more than 50 % active
substance content in dust.
Figure A- 2: Active substance content in Heubach dust (mg a.s./100,000 seeds) of maize seeds (2012)
as a function of Heubach dust (g dust/100,000 seeds) based on 193 seed batches with
two replicates of 9 maize breeders (data source: Jrgen Rath, German Maize Committee,
Bonn, 2013, submitted).
44
Table A- 6: Seed quality parameter regarding dust expressed as Heubach value for treated cereal
seeds. For purpose of comparison, the Heubach values have been normalized to 180 kg.
Reference
Batch
(year)
Number of batches
Heubach value
(mean)
(g dust/180 kg)
Heubach value
th
(90 percentile)
(g dust/180 kg)
42 (with sticker)
11 (without sticker)
74 (with sticker)
16 (without sticker)
0.9
2.4
0.5
2.0
1.7
3.2
0.9
3.1
2 (without sticker)
1.8
2.2
4 (with sticker)
3 (without sticker)
1 (with sticker)
4 (without sticker)
1.0
2.4
1.7
2.1
1.2
2.8
3.2
4 (with sticker)
2.1
Product A
JKI/ Winter barley
2011
JKI/ Winter wheat
2011
Product B
JKI/ Winter wheat
2011
Product C
JKI/ Winter barley
2011
JKI/ Winter wheat
2011
Product D and E
JKI/ Winter barley
2008
2012
Content of active substance in Heubach dust
Table A- 7 shows on the example of cereal seeds of 2011 that the average percentage active
substance content in Heubach dust ranges from 0.2 to 8.0 %.
Table A- 7: Summary of the content of active substance in Heubach dust for treated cereal seeds
Reference
Number of active
substances and
batches
(No.)
JKI / winter barley,

winter wheat,
2011
JKI (2009, 2013b)/

winter barley,
2008, 2012
Seed dressing
% a.s. in
% a.s. in
rate
Heubach dust Heubach dust
th
(mean)
(90 percentile)
Heubach dust
(mean)
(g a.s./ha)
(%)
(%)
g dust/180 kg seed
a.s. A
a.s. A
23
2
0.8 1.0
0.2
0.2
1.3
a.s. B
a.s. C
a.s. D
23
23
7
4.0 5.0
0.6
1.0
1.3
a.s. E
a.s. F
a.s. G
a.s. H
2
2
7
7
6.0 8.4
1.8
3.1
2.0
a.s. I
a.s. J
4
4
30.0 35.0
8.0
2.1
48
Content of active substance in Heubach dust
Table A- 9 shows one example of a treated sugar beet seed batch of 2012: the average percentage
active substance content in Heubach dust ranged from 0.3 to 3.5 %, the 90th percentile ranged from
0.5 to 8.9 %.
Table A- 9: Summary of the content of active substance in Heubach dust for treated sugar beet seeds
Reference
Block
(2012)
Seed dressing rate

(Number of batches)
% a.s. in
Heubach dust
(mean)
% a.s. in
Heubach dust
th
(90 percentile)
(g a.s./ha)
(%)
(%)
0.4
Product 1
Active substance A
6 g a.s./ha
(n=4)
Active substance A
8 g a.s./ha
(n=24)
Product 2
Active substance B
15 g a.s./ha
(n=4)
Active substance B
60 g a.s./ha
(n=24)
a.s. in
Heubach dust
(mean)
(mg a.s./
100,000 seeds)
a.s. in
Heubach dust
th
(90 percentile)
(mg a.s./
100,000 seeds)
0.5
0.087
0.107
1.3
2.9
0.046
0.099
0.3
0.5
0.082
0.123
3.5
8.9
0.189
0.407
In Figure A- 7 and Figure A- 8 the active substance amount in Heubach dust as a function of Heubach
dust on the example of two plant protection products and four sugar beet breeders in Germany are
represented. The active substances depicted are the same as in Table A- 9. No clear relationship is
shown between seed dressing rate and the amount of active substance in the dust. Seeds from
different breeders/seed treatment facilities may show high differences in a.s. content at the same
dressing rates.
50
Normalisation approach of study parameters:

Heubach value: normalized to a reference Heubach value of 0.75 g/100,000.
Concentration a.s. in Heubach dust: Residue content in dust was corrected for the reference
value (35 %).
Drill width: The drift curves of the experiments were corrected for the limited experimental
sowing widths of a norm field of 100 m width (see point E of this Appendix for details).
The normalisation factors for each study and the normalised ground dust drift values to standard
quality criteria are summarized in Table A- 11.
Table A- 11: 90th percentile of measured ground dust drift values, normalisation factors to reference
quality criteria and normalised 2D-exposure dust drift data (in g a.s./ha) at 1 m distance
after seeding maize
Reference /
Sowing
method
Crop /
Number of
Year of
experiments/
experiment
Number of
Petri dishes
2D-ground dust
Normalisation factor for
deposition at
Heubach
a.s.
Drilling
1 m distance
value
content
width
th
(90 percentile)
in dust
Normalised 2Dground dust

deposition at
1 m distance
th
(90 percentile)
(g a.s./ha)
(g a.s./ha)
JKI /
pneumatic,
vacuum
technique
Maize 2009
1/19
0.688
0.35
1.58
1.05
0.40
Maize 2010
1/15
0.153
0.87
3.30
1.03
0.45
Maize 2011
1/11
0.220
1.67
1.83
1.07
0.72
Maize 2012
1/12
0.038
1.42
4.86
1.03
0.27
In Figure A- 9, the measured 2D dust ground deposition in four field experiments after sowing maize
by Julius Khn-Institut (JKI) is depicted as a function of the amount of active substance released with
Heubach dust (Heubach a.s. in g a.s. in dust/ha). Compared are also normalised and original values.
The regression equation has a high coefficient of determination and relates the deposition in the offfield directly to the amount of abraded active substance during drilling.
As can be seen when comparing the values of the field experiments in the year 2010 and 2011 in
Table A- 10 and in Table A- 11, the application rate in-field (in g a.s./ha) does not correlate with the
2D deposition rate in the off-crop area.
Using the highly significant regression equation shown in Figure A- 9 the relationship between the 2D
ground dust deposition and Heubach a.s. can be expressed as 1.6 x Heubach a.s.. For the maize
reference quality criteria Heubach a.s. of 0.26 g a.s. in dust/ha, a 2D ground dust deposition of
0.42 g a.s./ha is calculated. This is the reference value to be used for 2D ground deposition dust for
the crop maize, when the treated seeds to be assessed comply with the legal requirement and the
seed quality is certified (see chapter 10.5.3, page 22).
56
Normalisation approach of study parameters:

Heubach value: Normalisation of the dust deposition values for the experimental Heubach value
of 1.6 g dust/ha to the reference value of 2.0 g dust/ha.
Concentration a.s. in Heubach dust: Residue content in dust was corrected for the reference
value (10 %).
Drill width: The drift curve of the experiment in 2012 was corrected for the limited experimental
sowing width of 45 m for a sowing width of a norm field of 100 m width (see point E of this
Appendix for details).
The normalisation factors for each study parameter and the normalised ground dust drift deposition
to standard quality criteria are summarized in Table A- 15.
Table A- 15: 90th percentile of measured ground dust drift values, normalisation factors to standard
quality criteria and normalised 2D-exposure dust drift data (in g a.s./ha) at 1 m distance
after seeding barley
Reference /
Crop /
Number of
2D-ground dust
Normalisation factor for
Sowing
Year of
experiments/
deposition at
Heubach
a.s.
Drilling
method
1 m distance
experiment Number of Petri
value
content
width
th
(90 percentile)
dishes
in dust
(g a.s./ha)
JKI /
pneumatic
Barley 2008
1/9
Barley 2012
1/12
imidacloprid
0.046
imidacloprid
0.038
triadimenol
0.046
Normalised 2Dground dust

deposition at
1 m distance
th
(90 percentile)
(g a.s./ha)
1.27
1.25
1.00
0.07
1.29
1.80
1.11
0.10
1.29
1.25
1.11
0.08
As Reference value for 2D ground dust deposition to be used for exposure assessment of cereals is
0.10 g a.s./ha. It is based on the relationship between the 2D ground dust deposition in the off-field
and the Heubach a.s., which corresponds to a PEC 2D ground dust deposition (g a.s./ha) = 0.5 x
Heubach a.s.(g a.s.in dust /ha).
D Sugar beet
For sugar beet, not sufficient data presenting Heubach values and residue content of a.s. in dust
were available. From 19 experiments reviewed by Fent (2012), only one field study with measured
Heubach value can be considered for the derivation of the 2D ground dust deposition (Table A- 16).
In this experiment, the Heubach value was 0.005 g dust/100,000 seeds, which is ten times lower than
the reference value of 0.05 g dust/100,000 seeds. The active substance content in Heubach dust was
not analysed.
59
recommended for the submission of new field studies regarding 2D dust drift deposition to consider
an appropriate residue analysis.
Furthermore, important aspects for product specific authorization of sugar beet are, e.g.:
realistic Heubach values

realistic amount of active substance in Heubach dust (% a.s.)
adequate application rate
adequate size of the field plot
sowing method
adequate replicates
E Adjustment of dust ground deposition for the sowing width of the treated field
The drilling of a smaller field size is deemed to underestimate the total amount of dust deposition in
off-field areas. In order to normalise dust ground deposition rates which were measured in different
experiments with different test conditions, a normalisation of the deposition values was performed.
The evaluation was carried out by Schmidt (Landwirtschaftliches Technologiezentrum LTZ
Augustenberg, Germany). The 2D values estimated in the treated plot were upscaled to a reference
field with a drilled area of 100 m width.
In the first step, the measured mean dust ground deposition values collected with Petri dishes at
different distances (e.g. 1 m, 3 m, 5 m, 10 m, 20 m, 30 m) from the first sowing row were used to
calculate a exponential curve per experiment. The derived exponential equation is given in Table A18. In the next step, the exponent of each equation was considered to calculate the contribution of
each single sowing row to the total amount of deposition of all sowing rows of a 100 m wide treated
field. Based on these results, the correction factor was derived for a drilled field size from 3 m up to
100 m (see Figure A- 10). The correction factor represents the difference of dust deposition between
actual sowing width and the reference sowing width of 100 m. In Table A- 18 the normalisation factor
for the considered field experiments is summarised.
61
dust)
a.s. amount in
dust particles
related to
sowing rate
("Heubach"
g a.s./ha)
0.086 g imidacloprid /ha

0.124 g triadimenol /ha
Type of study
(tunnel, semifield, field etc.)
field
Time of year
Field Phase: Sept. 2012

Analytical Phase: Sept. Oct. 2012
Study location
The dust drift monitoring has been conducted on agricultural land in the area of
Braunschweig near Lucklum, Germany.
Study
description/
material and
methods
The adjacent area of the field sown was divided into 2-3 replicated areas of
about 50 m length covered with flowering mustard (BBCH65) and 40 m long
areas with bare soil, where the crop had been removed. Before drilling the
adjacent plants were wetted with glycerol to create a worst case situation for
adhesion of dust particles during harvest of plant material for residue analysis.
In the bare soil area dust drift was measured with 3 - 4 Petri dishes (with filter
paper wetted with glycerol inlet) per replicate, placed at different distances to
the area sown from 0.15 m up to 30 m (0.15, 1, 3, 5, 10, 20, 30 m).
Additionally, at 3 m distance one vertical gauze net per plot was placed (2 m
height x 3.50 length, net wetted also with glycerol). 3 samples of 0.25 m size
per net at a height of 0.40 0.90 m were taken for residue analysis.
The filter effect of the directly adjacent vegetation was calculated after
measuring the a.s. deposits on all plants harvested in 0.1 m large areas as well
as the soil deposition on Petri dishes placed within the crop (4 replicates for
both sample types and distance) and then comparing the values in Petri dishes
in open area to total depositions in the adjacent crop areas.
Drilling usually lasted about 1 hour. Plants, gauze net and Petri dishes/ filter
collectors were sampled shortly after drilling. Samples were deep frozen after
delivery to the analytical laboratory. The identification of different substances
in Petri dishes/filter collectors, gauze net, and plants was carried out with a
LC/MS/MS-system of Dionex UltiMate 3000 coupled to an AB SCIEX QTRAP
5500. For quantification matrix-matched calibration with internal standards
(acetamiprid D3 as surrogate, clothianidin D3 or imidacloprid D4) were used.
The method was validated by conducting recovery experiments with Petri
dishes/filter, gauze net, and plants.
Limits of quantification
petri dishes/filter:
0.7 mg/ha for both actives
gauze:
4.0 mg/ha for both actives
plants (open flowers): 1.0 mg/ha for imidacloprid
plants (rest):
1.0 mg/ha for imidacloprid
Drilling width
of the plot
45 m
Wind speed
3.57 m/sec (mean during drilling period)

82
Application rate
of a.s./ha
104.63 g a.s. /ha
Seed quality
(Heubach value,
content a.s. in
dust)
Heubach value:
at time of bagging (May 6, 2009): 0.81 g /100,000 seeds
at time of drilling (May 29, 2009): 1.23 g /100,000 seeds
a.s.-content (%) in dust: not analyzed
a.s. amount in
dust particles
related to
sowing rate
("Heubach"
g a.s./ha)
not applicable
Type of study
field
Time of year
Start and end of field activities: 29 May 2009 26 June 2009

Start and end of analytical activities: 02 June 2009 06 July 2009
Study location
The study was conducted on commercial agricultural land around Bayers

headquarter in D-40789 Monheim, North Rhine-Westphalia, Germany, on a
study plot typical for maize growing (total field size: 8.9 ha, 220 m x 54 m).
Study
description/
material and
methods
Material and methods

The aim of the study by Neumann & Jene (2010) was to gain experience with
technical options to quantify aerial dust drift and deposition from the sowing of
treated seeds in future drift trials. Therefore, the capture efficiency of several
types of artificial, vertically oriented sampling devices and a semi-natural hedge
were compared for the assessment of aerial dust drift occurring during sowing
maize seeds with a JKI (Julius Khn-Institut, Germany) approved modified
pneumatic drilling machine. Samplers were located downwind from the drilled
area at different heights above the ground.
All sampling systems were installed prior to the drilling procedure at distinct
locations along the downwind long edge of the drilling area (base line) and at
different heights. The distance to the first row of maize seeds (zero-line) was 3
m. Petri dishes were placed in metal placeholders on the soil surface and filled
with an acetonitrile-water mixture (2/8, v/v). The following types of passive
dust samplers were installed at 0.65 and 1.65 m height: Pipe cleaners,
polypropylene scourer pads, and BSNE wind aspirated dust sampler. Gauze
netting, and artificial hedge (made from cherry laurel branches) screens (5 m
wide and 2 m high) were also used. Additional polypropylene scourer pads
were installed on a pylon at 1 m, 2 m, 3 m, 4 m, 5 m and 6 m above the soil
surface. With exception of the pipe cleaners and the BSNE samplers, all passive
samplers were wetted with a glycerol/water mixture (1/1, v/v) to enhance dust
retention. The only active dust samplers were HVAS (high volume air sampler),
which were also installed at 0.65 and 1.65 m height.
Sowing started at the zero-line. After the drilling of 8 rows in alternate
directions was completed, there was an additional waiting period of 30 minutes
before the collection of samplers, to allow those dust particles which had not
yet been deposited to settle on the sampling area (primary drift).
After collection of the primary drift samples, new polypropylene scourer pads
85
and new BNSE dust sampler were installed to assess the secondary drift over a
period of 24 h in order to quantify the amount of COMPOUND* which may be
dislodged from the sowing area during this period. Subsequently, after
completing the 24 h secondary dust drift sampling, additional 4 week secondary
drift was sampled by installing a new BSNE wind aspirated passive dust
samplers on each of the four sides of the drilled area.
Sampling system and layout
Sampling layout
The orientation of the field plot and setup with the three discrete sampling
locations for the petri dishes, the gauze net and hedge proxy is shown in Figure
A- 18.
Petri dishes
At three discrete sampling locations (A, B, C; see Figure A- 18), 10 polysty-rene
petri dishes ( 13.7 cm, height 1.7 cm, 147.41 cm) were placed in metal
placeholders on the field ground with a distance of 1 meter between the dishes
and with a sampling distance of 3 m relative to the planter zero-line (first
seed row). Hence, a total of 30 samples were taken. Prior to the maize drilling
procedure, all Petri-dishes were filled with 100 ml of an acetonitrile-water
mixture (2/8, v/v). After drilling and the additional waiting period of 30
minutes, the content of each Petri-dish was trans-ferred into 250 mL
polyethylene flasks by means of a polyethylene funnel.
Gauze Net
At three further discrete locations (G, H, I; Figure A- 18) along the down-wind
long edge of the drilled plot, at 3 m distance from the planter zero-line, an
array of passive dust-drift samplers made of gauze netting fabric (Tana Netting
100 denier mosquito net, Mesh 156, 40 g m-2, untreated) were fixed to a
construction fence. The netting (5 m x 2 m) was attached by cable ties, so that it
did not become displaced by wind. In order to enhance dust adhesion, the
netting was evenly wetted for 60 s with a glycerol/water mixture (1/1, v/v).
Starting 30 minutes after completion sowing, ten sections of material (50 cm x
50 cm) were cut from the netting. Five sections were taken such that their
centre was at 0.65 m height from soil surface and five sections with their centre
at 1.65 m. In total, 30 netting samples were collected, sampling height (0.65 m
or 1.65 m).
Semi-natural Hedge Proxy
At three discrete locations (J, K, L; Figure A- 18) along the downwind long edge
of the drilled plot, at 3 m distance from the planters zero-line, a semi-natural
hedge consisting of freshly pruned cherry laurel branches and leaves was
installed, attached to a construction fence. In order to enhance dust adhesion
to the leaves, the plant parts were evenly wetted for 120 s from the front and
60 s from the back with a glycerol/water mixture (1/1, v/v). Starting 30 minutes
after sowing, ten section areas of cherry laurel branches, twigs and leaves (each
comprising 50 cm x 50 cm fence area) were detached, with five sections taken
such that their centre was at 0.65 m height from soil surface and five sections
taken with their centre at 1.65 m. The section areas were arranged in such a
way that there was a verge of at least 10 cm to the overhang of the hedge, to
avoid sampling plant material where drift deposition could have been affected
by edge effects.
Soil Characterization
86
Figure A- 19: Wind conditions during sowing and waiting period
Figure A- 20: Gauze netting with sample high at 0.65 and 1.65 m height
88
dust)
Amount of dust after transport: 0.965 g /100 kg seeds

(=0.216 g/100,000 seeds)
a.s.-content (%) in dust: not analyzed
a.s. amount in
dust particles
related to
sowing rate
("Heubach"
g a.s./ha)
not applicable
Type of study
field
Time of year
Start of field work: 02 November 2010

End of residue analysis: 20 January 2011
Study location
Maize seeds, pre-treated with COMPOUND-MA (provided by BASF SE), were

sown in the vicinity of Ubstadt-Stettfeld (Baden-Wrttemberg) on
02 November 2010.
Study
description/
material and
methods
The field study was conducted in Germany during autumn 2010. The plot had a
size of 200 m x 54 m and was drilled with treated maize seed with downwind
collection of emitted dust. 30 Petri dishes, filled with glycerol/water (1/1, v/v),
30 Petri dishes filled with sand wetted with glycerol/water (1/1, v/v), and three
gauze netting sheets of 5 m length and 2 m height were placed at 3 m distance
from the zero line (first driller pass + row spacing). The Petri dishes were
placed horizontally on the ground, and the gauze netting was attached to a
mobile building fence. In addition, the gauze netting was wetted with a
glycerol/water mixture (1/1, v/v, 44 mL/m; glycerol 87 % technical grade) to
enhance dust adsorption.
Soil samples from the upper 10 cm were taken for soil characterisation and for
a potential analysis of residues of COMPOUND-MA. Soil samples from the
upper 5 cm were taken for the moisture content determination. Petri dishes
and gauze netting samples were analysed for the residues of COMPOUND-MA.
Soil samples were not analysed for residues.
The LOQ for COMPOUND-MA was 0.002 g/dish (equivalent to 1.397
mg a.s./ha) or 0.010 g/gauze sample (equivalent to 0.40 mg a.s./ha).
Petri dish Sampling: Starting 30 minutes after completion of drilling of the final
row, Petri dishes were covered with Petri dish lids and then removed from the
deposition plot starting with sector A, followed by sector B and C.
The gauze samples were not collected until the expiration of a 30-minute
waiting period subsequent to drilling. The pre-marked squares were carefully
cut out of the gauze netting. The material was folded and transferred into HD
PE 2.5 L plastic containers.
All samples (except soil characterisation samples, Heubach samples and water
content samples) were deep frozen two hours after sampling and stored at 18C at the test facility.
Drilling width
of the plot
54 m
Wind speed
3.02 0.47 m/s (0.90 m/s to 5.46 m/s)

91
methods
Immediately before starting the sugar beet sowing operation, a composite soil
sample from the upper 5 cm was taken from at least 20 locations randomly
selected on the drilling area and filled in a plastic bag. The analyses of the
topsoil immediately before drilling revealed a water content in the upper 5 cm
of 8%. The soil characterisation revealed a heavy loamy sand soil.
All COMPOUND-SB-containing dust and abrasion particles which deposited at 1,
3, 5, 10, 20, 30 and 50 metres distance from the drilling area during sugar beet
sowing ("primary drift") were sampled in polystyrene Petri-dishes (13.7 cm,
147.41 cm), filled with an acetonitrile-water mixture (2/8, v/v), For each
sampling distance, three arrays of 10 Petri-dishes each were installed with a
distance of 1 metre between the dishes and 50 m between the arrays.
Accordingly, a total of 30 samples were taken for each sampling distance. After
drilling was completed, an additional waiting period of ca. 15 minutes was left
before the beginning of sampling to allow those dust particles which had not
yet been deposited to settle on the sampling area. Sowing started directly
adjacent to the sampling area. After the additional waiting period of 15
minutes, the content of each Petri-dish was quantitatively transferred into
individually labelled polyethylene flasks by means of a polyethylene funnel and
each polyethylene flask was tightly closed with its corresponding polypropylene
screw cap. Sampling always started at the 50 metre distance and proceeded
towards the drilling area in order to avoid any downwind cross-contamination,
passive dust-drift collectors were installed at 1 m, 2 m, 3 m, 4 m and 5 m above
the soil surface. The dust collectors were made of a polypropylene fabric mesh,
built up of filaments with a 0.80 x 0.18 mm cross-section. This type of collector
has a slightly oval shape with a length of 85 mm and a diameter of 65 mm;
at its poles, the diameter is 50 mm. The polypropylene fabric mesh collectors
were pinned on each end of horizontal metal rods, which in turn were mounted
at the respective height on a vertical tripod-pylon (height 6 m), giving in total
10 collectors per pylon (2 at each height). In all arrays, a pylon was installed at 5
and 30 m distance from the drilling area, respectively, resulting in 6 collectors
per height per distance. Once the 30 m line and later on, the 5 m line have been
reached during the sampling process of the Petri-dishes ("primary drift"; see
above), also the passive collectors were sampled and placed in individually
labelled plastic containers. In the laboratory, each individual passive collector
was extracted with an appropriate volume of acetonitrile/water (2/8, v/v) in an
ultrasonic bath to enhance the extraction process.
After the Petri-dishes filled with acetonitrile/water (2/8, v/v) and the passive
dust-drift collectors had been sampled ("primary drift" and "atmospheric drift",
see above), ten new polystyrene Petri-dishes ( 13.7 cm, height 1.7 cm, 147.41
cm2 surface) were installed on the field ground of the sampling area in all arrays
at three distances from the "zero line" (1, 5 and 50 m), respectively. The Petridishes were filled with about 100 mL of an glycerol/(Millipore-)water mixture
(1/1, v/v) and were exposed for a period of 24 h in order to quantify the
amount of COMPOUND-SB which may be dislodged from the sowing area via
secondary processes ("secondary drift"). After 24 h, the content of each Petridish was quantitatively transferred into individually labelled polyethylene flasks
by means of a polyethylene funnel and each polyethylene flask was tightly
closed with its corresponding polypropylene screw cap.
Drilling width
of the plot
48.6
104
Appendix VIII Recommendations on studies for the derivation of seed quality

parameters regarding dust drift
When assessing results of exposure studies describing dust drift deposition in non-target areas, it is
important that the products, recipes and coating facilities are documented. Moreover, drift values
used as a basis for risk assessment should not be generated with seed batches having outstandingly
good treatment quality (i.e. comparably low Heubach-values and/or low concentrations of a.s. in the
dust), since these are not representative for the quality of seed on the market. As both parameters
'amount of dust' and 'a.s. in dust' directly influence the possible off-crop exposure, it is
recommended that the Heubach abrasion values should also be recalculated as 'g dust a.s./ha',
taking into account both maximum values for abrasion as well as content of a.s. in dust. Therefore, it
is required that for both parameters the possible range of amounts for the applied PPP is
documented.
The minimum requirement for the definition of typical values for Heubach dust (g dust/seed unit)
and the content of active substance in dust Heubach a.s. (g a.s. in dust/ha) should be defined. It is
not the intention of the Member States to replace reference values determined on a basis of several
data with results of single studies.
A Amount of dust (Heubach dust)

To be amended after consultation of MS.
B Content of active substance in Heubach dust

A further key parameter, which directly influences the amount of the dust deposited in off-field areas
is the content of active substance in Heubach dust (% a.s. in dust). Therefore, it is recommended
that the range of the active substance content in dust is documented by the applicant for
authorization of a PPP as seed treatment. The content range is dependent on the seed quality of the
treated seeds. Therefore, it is recommended that the submitted sample covers a variety of batches
from different breeders in European Member States. The calculation of Heubach a.s. (g a.s. in
dust/ha) to be used in the exposure assessment should be based on the content of active substance
in Heubach dust as the 90th percentile of all batches. The a.s. content in dust should be
documented as mass content per seed reference unit and as percentage. Furthermore, it is
recommended that the seed batches are treated with the maximal intended application rate of the
PPP.
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Appendix IX
Effects on non-target organisms comparison of exposure via dust

drift to sprayed residues
Experimental data
First trials have been made to compare the sensitivity of standard non-target arthropod species
towards dust and spray exposure (Table A- 20). Preliminary results show that the sensitivity of
standard non-target arthropods species (Aphidius rhopalosiphi, Typhlodromus pyri and Chrysoperla
carnea) is comparable or lower when exposed to contaminated dust versus liquid formulation.
However, according to preliminary results (data from applicants and JKI, pers. comm.) honey bees
seem to be more sensitive to dust drift compared to spray drift, especially to fine dust particles.
These first results are to be validated and it is still questionable if the standard laboratory test species
are representative for all arthropods regarding the sensitivity to contaminated dust (with special
regards to pesticide uptake, e.g. activity and grooming behaviour) as they are currently considered
for the risk assessment of spray formulations. It cannot be excluded that e.g. dust may stick longer at
more hairy species -and thus these species may have a higher contact exposure. Non-Apis pollinator
species are not expressly covered in the current valid Guidance Document on Terrestrial
Ecotoxicology.
Another exposure route which has not being addressed up to now is the oral uptake of dust particles
together with pollen. In flowers, high concentration of contaminated dust can be expected, which
might constitute a high risk for pollinators (see below).
Table A- 20: Toxicity of active ingredients (a.s.) to arthropods, applied as spray formulations or as
dust particles.
Species
A. rhopalosiphi
T. pyri
C. carnea
Formulation toxicity
L(E)R50 (g a.s./ha)
liquid
0.058
0.177
133.3
197
4.08
36.4
dust
0.331
9.42
> 800
> 256.1
26.2
262.4
Factor dust/
spray toxicity
5.7
53.2
> 6.0
> 1.3
6.4
7.2
Source
Stevens (2010)
Jans (2010a,b)
Fallowfield (2010)
Jans (2010c,d)
Spincer (2010)
Jans (2010e,f)
Conclusions
The very first studies on the effects of dust from treated seeds on non-target arthropods show that
the standard beneficial test species are less sensitive to dust than to the liquid seed treatment
formulation under the tested conditions. By contrast, first results of tests with honey bees show that
the standard species tested for liquid formulations may not be representative for species sensitive to
the exposure toward contaminated dust. Wild bee species or butterflies might be more sensitive to
the same compounds than the standard laboratory test species due to their body surface structure
(e.g. hairs, scales).
Using effect studies with the liquid PPP formulation, which are not designed and validated for
contaminated dust, has two deficiencies. On the one hand, the 2-dimensional sprayed glass plate test
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may lead to a conservative toxicity input value for risk assessment. On the other hand, the test
design of a 3-dimensional (sprayed plant) extended laboratory test is not comparable to the
exposure to dust filtered out and accumulated in 3-D structure (e.g. flowers, hedgerows) and
therefore might underestimate the risk.
As long as no further data on the effects of dust on other non-target arthropods are available, it is
proposed to use the standard endpoint from the liquid seed treatment formulation from the species
which showed the highest sensitivity to the active substance. Additional tests can be conducted more
easily with the liquid seed treatment formulation than not yet harmonised and validated dust
laboratory tests, and is therefore acceptable.
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Appendix X
Good practices and quality standards for the treatment of seeds

and for the use of treated seeds
Seed coating, i.e. the application of a plant protection product (PPP) directly onto the seed, is
commonly considered as less dispersive than spraying the product in the field on bare soil or on early
growth stages of the crop. In avoiding spray drift, the dispersion of active ingredient outside the field
is considered low and the proportion of active ingredient soluble in the soil, being not bound to the
seeds, and thus being subject to leaching, is considered limited.
The use of coated seeds may however lead, to exposure at sowing due to dust dispersion. Coating
quality and especially the presence of dusts on the seed during the coating process, are known to
contribute to dust release during the handling of seeds and seed-bags. In addition, seeding drills
might contribute to the generation of dusts.
The release of pesticides into adjacent areas via dust is influenced by following aspects:
Drilling density of seeds per ha; width of drilling, application rate of active ingredient per ha
Quantity of dust per seed unit after seed treatment and dust fraction size
Resistance to abrasion of treated seeds in packages and in sowing machines
Concentration of active substances in the dust
Drilling technique
Wind speed and direction
Soil humidity conditions
Stickiness and structure of adjacent plants.
This chapter is meant to give guidance mainly for the control of release of contaminated dust during
drilling. The emission of seed dust during seeding is variable, depending upon the care taken during
all the steps from the preparation of seeds before treatment to the type of driller used. In extreme
cases, the amount of dusts has proven to be high enough to impact honey bees and has led to the
poisonings reported in Germany and Italy in 2008, Austria and Slovenia in 2008 to 2011. These high
amounts of dust were highly contaminated with insecticidal active substances. While an aggravating
factor for pollinators is the coincidental presence of flowering crops or weeds in the immediate
vicinity of the fields sown, the emission of dusts towards aquatic systems or vegetated corridors may
also affect aquatic and terrestrial life, even not mentioning the exposure of the farmer himself or of
by-standers.
For these reasons, it is essential to ensure that the practice of seed protection is controlled so as to
limit the quantity of dust generated and dispersed to the minimum. The same is valid for the
concentration of active substances in the dust.
It is acknowledged that technologies will evolve in future so that the level of dust reduction being
technologically reachable and the related recommendations will evolve accordingly. Thus the
recommendations below are to be understood as reflecting the current state-of-the-art in the area
and will be revised based on updated science.
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A Seed treatment process

Seed preparation is one of the most critical steps as cleaning is widely recognized as a means to
reduce dust values. Indeed removing dusts before treatment improves the adherence of coating
onto seeds. Cleaning may be automatically performed in industrial processes and devices exist that
may allow seeds to be cleaned at the facility. Although cleaning is an effective means, the step is not
strictly controlled as the quantity removed depends on the seed type, aspiration method etc. The
efficacy of the whole process is controlled through dust values measured at the end of the process
on random seed batches.
Before the actual seed treatment can be applied the seed needs to be properly cleaned and for
certain crops calibrated in a seed cleaning line.
The different cleaning steps are:
pre-cleaning
o by sorting out bigger particles etc.;
o taking off dust by aspiration.
cleaning
o taking off under and oversized seeds;
o calibration of the seeds depending on the species;
o minimizing dust by further aspiration.
After these steps the seed is ready to be treated.
Treatment of seeds should follow recipes that are optimized for adherence and resistance to
abrasion. The seed treatment is done by and in professional treating equipment:
batch treaters for corn, oilseed rape, sunflower, sugar beet and vegetables;
batch treaters as well as continuous treaters for cereals;
during the treating process and when bagging, further aspiration needs to be done to absorb
remaining contaminated dust as much as possible.
To avoid further stress for the bagged seeds, the bags are palletized and stretch wrapped with plastic
foil for storing and distribution.
Each step should be carefully controlled and certification systems allow an appropriate supervision of
all the steps in the process.
Additional to dust avoidance activities, only seed treatment recipes should be used which minimize
the content of active substance in dust. Before new recipes are introduced for seed treatment, it
needs to be checked if the content of a.i. in dust is not increased.
Examples of seed treatment process certification systems are the dust control program (Plan qualit
poussire) in use in France, the certification for seed treatment plants in use in Germany and ESTA,
the new European seed treatment and treated seed certification scheme developed by European
Seed Association (ESA).
Process certification systems have found wide acceptance in the food and animal feed industry as
they combine security aspects with process control. Process control implies that testing each and
every batch of product is not necessary; monitoring adequate functioning of the processes secures
reliability. Testing ad random samples is one of the tools to monitor the adequate functioning of the
processes. Retaining a reference sample of each batch after treatment is done in order to always be
able to respond to questions on the quality of the treated seed.
For facilities treating seed with plant protection products, the ESA is developing a quality
management system (ESTA) that will lead to certification of seed treatment plants and of the treated
seed coming from these plants. A general (i.e., not crop-specific) standard has been developed as
the basis for ESTA.
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In France and Germany certifications are in place already for maize and oil seed rape treatments,
respectively. Extension to other crops is under way in both countries. Work is on-going between
these national initiatives and ESA to align the certifications, aiming at one EU-wide ESTA certification
(and ESTA labelled seed) in future.
Treatments performed in non-certified processes are in principle possible and may be allowed if they
reach the relevant quality criteria and the representativeness for a European authorization given.
In some countries, the abrasion resistance of treated seeds is controlled and compared to a
threshold or quality standard imposed by the legislation, as an example in France or Germany for
maize seeds (JORF, 2010).
The amount of dusts produced is commonly measured through a Heubach test (Figure A- 22).
Figure A- 22: Measurement of dust on seed batch using the Heubach test (source Julius KhnInstitut; DE).
Another test has been developed, known as CERES. This test relies on a different principle as seeds
are not shaken in order to generate an abrasion but are placed in a device equipped with an
aspiration that will collect air and dusts being present in the sample. The comparison of the amount
of dusts quantified in both systems has been extensively described and indicates that values
generated with the Heubach test, which is more abrasive, are more representative of a worst case.
Thus the Heubach test has been selected for further development and a use as a reference test for
abrasion dust control.
ESA and the European Seed Treatment Manufacturers have agreed one standard dust test protocol,
available on the ESA website (http://www.euroseeds.org/codes/esta-european-seed-treatmentassurance/). The choice for Heubach equipment was made as this test actually abrades the (treated)
seed, in contrast to the milder CERES test system.
In France for example, the Heubach test is currently performed on seed batches for maize. The
threshold values used are 3 g/100kg seed to check that the seeds match with quality criteria. Any
value comprised between 3 and 4 g/100kg seed a new control is performed and the treatment
process is corrected. Any value higher than 4 g/100 kg seed leads to the interruption of the
treatment process (JORF, 2009).
For the standardized Heubach dust test, several accredited reference laboratory exists over Europe.
For example, a certification system for independent, or seed company laboratories is operated by the
Socit Gnrale de Surveillance (SGS). The SGS certification scheme features yearly ring tested
calibration comparisons between the laboratories to assure continuous data comparability, as well as
random cross testing of commercial analyses performed by the labs to ensure quality of operations.
Also management of deviations from the norms is comprised in the SGS certification scheme. SGS
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has trained auditors making the programme available for implementation across the whole of
Europe.
Dust values generated from the tests are in general expressed as weight of dust reported to a weight
of seed (g dust/100 kg seeds) or weight of dust reported to a quantity of seeds (e.g. g dust / 100,000
seeds). Because seeding density varies among countries and even locally, pending on the drilling
equipment, dust values expressed as g dust/thousand grains allows an amount of dust /number of
seeds to be defined for risk assessment purposes.
It is acknowledged that drilling practice may differ among countries and for vegetable especially
depending on harvest use patterns particularly with regard to the drilling density. Specificities will be
easily accounted for through the expression of dust values per thousand grains.
B Handling steps
Several important steps preceding drilling itself may also contribute to the abrasion of seeds / dust
emission if not considered with care. These steps include:
Seed-bags or containers deliver and handling
Seed-bags or containers stocking
Loading of the driller
Sowing
After drilling, handling of the empty bags.
Seed-bags or container delivery and handling
Seed bags should be handled gently during the entire course of their use. This includes physical
movements of the seed at the treatment site throughout the distribution chain, and on the farm.
Abrasion through friction between individual seed kernels is a source of dust, and should be
minimized. This can be done by:
Always move individual seed bags with care. Never throw them.
When transporting many seed bags always do so on stretch wrapped pallets. By stretch
wrapping the seed bags onto a pallet, the movement of seed inside the bag is restricted, as
the bag cannot move, and thus also seed abrasion. Seed bags moved together on a pallet
are also less susceptible to damage during loading/unloading, than if they would be managed
individually.
It could be recommended to print the sentence Fragile - handle with care on seed-bags or
on stickers to be used on each pallet of seed.
The integrity of bags or containers should be checked by providers and also users at their delivery.
Seeds from visibly damaged packaging or bags should not be used.
Seed treatment, seed companies and distributors have a responsibility to make sure that forwarders
are made aware, and adhere to, the above recommendations.
Seed-bag or container storage
Seeds-bags or containers should be kept safely closed during the entire stocking period. They should
be kept in safe and premises and out of sun, heat, humidity and kept out of access for children,
livestock or wildlife. If possible premises should be locked. Repeated stacking of bags should be
avoided.
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Loading the seed drillers
Even with maximum caution, the complete absence of dusts in containers or bags might not be
possible. Thus care should be taken in opening containers and loading the seed driller that the dusts
will not disperse outside the sowing area. It may then be recommended to load the driller at a safe
distance from water bodies, vegetated areas, flowering bushes, and bee hives. Also in choosing a
place to stop the driller to proceed to loading, care should be taken in such a way to not load on the
leeward side of sensitive areas.
Care should be taken to not shake the dusts off the bags or to load the dust in the bottom of bags
into the driller. Hand contacts with the seeds in the hopper, for example with the aim to spread the
seeds, should be avoided.
If for loading the driller any transport systems from the storage of seeds (e.g. wagon) to the driller
are used, this should be closed systems with as little as possible mechanical abrasion.
During the whole loading stage farmers should wear individual protections like glasses and gloves
and mask to avoid the contact with skin and mucous. Clear water should be available on the tractor
to rinse any dusts they could come in contact with and to rinse gloves after loading. Rinsed gloves
should then be removed.
In case where a re-loading is necessary, the turbine of the driller should be stopped.
Handling of the empty bags or containers after use
Bags and containers should not be left in the field without surveillance.
Bags and containers should be brought back after use. Preferably they should not be re- used but
rather be recycled in a dedicated process or eliminated according to local legislation. They should be
stocked in dry premises out of sun and heat. They should not be burnt or eliminated with household
waste. Labelling of bags and containers having been used should be kept by for further possible
control.
All relevant handling steps to be considered by the user before, during and after sowing in order to
ensure minimization of dust exposure of the environment are summarized in the generic ESA Safe
Use Bag Tags.
C Drilling machines
Drilling machines need to separate the seeds to achieve an appropriate spacing of seeds in the seed
furrow. There are three principal approaches used for this separation of seeds during the drilling
process
Vacuum-pneumatic seed separation
To achieve a precise deposition of the seeds in the soil (precision seeding), seeds are fed from a seed
reservoir to the driller head and held in place via vacuum (negative air pressure) on a perforated
sowing disc (Figure A- 23). Seeds are separated by being held onto the holes on the sowing disc as
long as the vacuum across the holes in the sowing disc is sustained (suction phase). During the
rotation of the sowing disk, the seeds are individually released from the disk by releasing the vacuum
in the corresponding holes, and the seeds then drop into the furrow created by the driller. During
the suction phase, any abraded particles are pulled through the holes in the system and are
transported with the exhaust air through the fan that generates the vacuum for the seed separation
process. From the fan the air and any particles are either released with a high velocity from one
single outlet 0.5 - 2 m above the ground (= un-modified vacuum-pneumatic driller) or from various
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outlets, that increase the total cross-section of the outlet area, close to the ground with a reduced
velocity (= modified vacuum-pneumatic driller).
Figure A- 23: Seeds caught by the disc of a vacuum pneumatic seeder.
Pneumatic seed separation using air streams (compressed air)
Pneumatic drillers that work with compressed air can be separated into two types.
One type (precision seeding) separates the seeds with the help of funnel-shaped cells which are
gravity filled with several seeds and excess seeds are blown-out of the funnel back into a seed
reservoir by an air stream. The air and any dust particles are released, directed at the ground.
The alternative type separates seeds from a central seed container with a mechanical dosing unit
into a riser tube. Inside the riser tube, an air stream transports the seeds to a seed dispersion unit.
Once the seeds have passed the dispersion unit, the air, the seeds, and any abraded dust are equally
distributed via tubes down to all seed furrows and are released, directed into the ground.
Mechanical seed separation (without air assistance)
Mechanical drilling does not operate with any air assistance. In order to accomplish a seed
separation, rotating disks with individual cells and other mechanical devices separate and transport
seed from the seed reservoir to the seed outlet, where the seeds drop via gravity into the seed
furrow. Abraded particles are therefore also released close to the ground, but not in any air stream
created by the driller.
Representative machines used for each seed type
The majority of planters sold in Europe are pneumatic planters as they offer a bigger precision at
drilling than mechanic planters.
The table below lists representative machines used to drill the mains crop cultivated in Europe. It is
important to note however that a farmer may wish to use one driller for all his crops.
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Table A- 21: Representative maschines used to drill the mains crop cultivated in Europe.
Machine
Mechanical seed drills
Crop
Wheat, Barley, Triticale, Oat
Oilseed rape
Alfalfa
Soybean
Peas
Pneumatic seed drills (compressed air)

Wheat, Barley, Triticale, Oat
Oilseed rape
Alfalfa
Soybean
Peas
Vacuum-pneumatic precision seed drill
Corn (maize)
Sugar beet
Rarely Oilseed rape
Sorghum
Sunflower
Cotton
Beans Peas
Some vegetables
Mechanical precision seed drill
Sugar beet
Pneumatic Miniseeds and vegetable machines
Vegetables
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The aim is to reach a 90% reduction in dust dispersion on the ground. This 90% reduction is
measured compared to a reference (i.e. standard machines used in the past), in redirecting air to the
soil.
For an efficient redirection of air, it is generally recommended to fix the deflector pipes so that the
outflow section is at 10- to 30-cm height above the soil. While currently deflector kits can be
installed on the driller, equipment manufacturer are now developing drillers integrally fitted with
deflectors at manufacture on all models sold in Europe.
Example of dust measurements is given in Figure A- 26.
Figure A- 26: Example of dust measurement process for machine with and without deflectors
(source JKI).
Survey of techniques to reduce dust output from machines
The efficacy of these kits, measured for the kit itself or as a couple kit + driller is commonly measured
in Germany, France and the Netherlands and experiments have been initiated in Italy.
Germany
In Germany, a drift test has been developed by the Julius Khn-Institut (JKI) together with
manufacturers, where equipped sowing machines are tested against standard machines (Herbst et
al., 2010). The drift is quantified from ground samples collected in petri dishes placed at 1, 3 and 5
metres from the sowing area. In this test the driller is filled with dust of small size, so that the
measured drift represents a worst case.
In the approval process, JKI certifies the whole turbine + deflector combination so that not all
seeders on the market need to be tested. To date, 223 turbine-deflector combinations from 16
manufacturers have been approved, the list of which may be found on their website
(http://www.jki.bund.de/de/startseite/institute/anwendungstechnik/geraetelisten/abdriftmindernd
e-maissaegeraete.html). A label is put on the deflector, which allows checking of the origin of the
deflector kit. The use of a deflector turbine combination requires the kit to be installed by a
professional. A list of equipment under technical check is provided.
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France
In France operators may choose the equipment via three different solutions:
drift reducing techniques provided by seeder manufacturers
deflector kit manufacturers (4 models available)
deflectors manufactured by farmers themselves.
As for Germany, overall the goal is to reduce dust dispersion by 90% without affecting the
effectiveness of seeding and to ensure the process does not degrade seeding quality.
Specifications and guidance for deflector installation are provided for all systems. The system shall
meet several characteristics:
gathering air flow and which is to be directed to the ground
the system shall be free of leaks and designed to avoid deposition of dust
the sum of the area of output sections of the device shall be at least twice the area of the
turbine outlet
the height of output air flow shall not be more than 30 cm 10 cm being optimal from the
ground.
A recent survey has investigated drillers equipped with deflector from manufacturers (10 drillers), 3
deflectors kit manufacturers and 9 devices proposed by the farmers themselves. The seal was tested
with flour (Grimbuhler et al., 2011). The results indicated that all drillers met the above mentioned
specifications.
Italy
In Italy, some experiments have been undertaken by Balsari (2010) and more particularly in the
research project Apenet. The aim was to measure dust drift at various distances from the sowing row
and to compare driller equipments. Two reports are available, which indicate coinciding results
compared to Germany and France. In 2009 some experiments displayed a limited efficacy of
deflector devices, however the report does not state the effectiveness of the equipment used and
dust deposition was very low, with or without deflector (maxima were ranging from 35 to 45 mg
dust/ha). These results indicate that measuring dust reduction achieved with a deflector as a
percentage from the reference without deflectors could tend to favor drillers that generate the
highest level of dusts without deflectors. In other words, a dust reduction of 90% achieved on a low
performance driller can easily be achieved whereas on a high performing driller a similar reduction
rate is much more difficult to achieve. Consideration should be given to the level of dust that is
actually generated once the drift reduction device is used.
The Netherlands
In the Netherlands, no specific experiments have been undertaken but deflectors are prescribed for
insecticide-treated maize sowing machines since 2010, which, together with a low dust level on the
seeds aims at 90% dust drift reduction.
State of the art and recommendations
The devices developed have been progressively implemented in Member states since 2008, date at
which the first important accident allocated to seed dust dispersion was recorded. Since the
implementation of driller equipment with deflectors has increased, even with home-made devices,
sometimes because the availability of marketed devices was not wide enough to equip all the
farmers demanding for, while the equipment had turned to be mandatory, as in France for example.
Data available from the monitoring implemented in France alongside the use of maize seeds coated
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In Austria, an order dated March 2010 fixes wind conditions to 5 m/s (18 km/h) (Womastek, 2011).
In the Netherlands, wind conditions for spray applications are also fixed to 5 m/s (xxxreferentie}. This
value is taken to apply also to sowing wind conditions.
To avoid the exposure of the farmer, the tractor cabin should be kept closed (no open window).
To avoid the exposure of granivorous birds and mammals to treated seeds, the presence of
remaining seeds on the soil surface should be avoided. Seeds should be entirely incorporated into
the soil and it should be ensured that the product is also fully incorporated at the end of rows.
Spillages should be removed. This may easily be ensured by for example covering all remaining seeds
with soil.
F Raising Good Practice awareness throughout the value chain

Assuring the awareness, and furthermore adopted behaviour of what is good handling and use
practice of treated seed, among all players in contact with the seed, is a challenging task, which
merits significant thought to be successful. The Crop Protection industry has significant experience of
stewardship activities directed to farm users and can be a good source for help in this task.
Key aspects to consider in the case of treated seed are:
Simplicity focus on the key messages will make retention and understanding easier, and
then allow for interest for the rest of the message.
Relevance if the message is not relevant, it will be rejected e.g. the set of safety phrases for
Seed Treatment chemicals are only in exceptional cases relevant to the seed treated with
those chemicals. If the sentences with safety advice for treated seed are out of proportion,
they will be dismissed by the user the farmer - as irrelevant, and not considered.
Ease of access The user must be able to appropriate the message without much effort.
Pictograms are often more efficient than fine print text, and do not require to make the
effort to put glasses on to be able to understand the message. The language needs to be
understood by the target user.
Consistency the messages need to be consistent and repeated to be understood. The less
confusion and the more enforcement of the message the easier to adopt good behaviour.
Recognizing that seed is traded across Europe today, good practice messages have to be the
same across all European countries. As the basic good treated use practices also are the
same irrespective of kind of seed treatment and crop, it is highly recommended to keep the
message consistent also across the treatment types.
Channels In order to be effective, the same message should reach the user through
different sources. Seed bag labelling is one, but information leaflets and farmer/industry/onjob trainings are other source for information.
Current standard set of S-phrases, may in part be relevant for treated seed, but these S-phrases for
the seed treatment product (to be included in the labelling of the treated seed according to Article
49 (4) of Regulation (EC) No 1107/2009) do not necessarily provide an adequate picture of measures
relevant to treated seed. Further, the standardized wording of S-phrases, needs support by
alternative, easy-to-understand, ways of assuring understanding of the messages.
ESA, together with the main seed treatment suppliers, have, based on the principles above,
developed a voluntary EU-wide generic seed labelling initiative, which currently is being
implemented. It is intended to support an effective communication of Good Practice messages for
treated seed, irrespective of crop and seed treatment used. It is to be completed by crop/seed
treatment specific requirements. More information can be found under www.euroseeds.org/esta .
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Figure A- 28: Safety recommendations related to treated seed use (source ESTA).
G Conclusions and recommendations

The information gathered in this section is proposed as a support in evaluating the relevance of seed
dusts at sowing as an exposure route for humans and the environment. PPP are evaluated for each
specific use and as seed treatments, for the coating of specific seeds. Thus, for each type of seed,
this chapter proposes the typical associated types of drillers (Table A- 21) from which it may be
deduced if any dust production is expected or not.
Drilling equipment and deflectors
If the practice involves vacuum pneumatic drillers for a specific seed in a country, recommendations
for risk management should be followed. These recommendations imply the equipment of drillers
with deflectors and the respect of weather conditions at which a low dispersion of the dusts, if any, is
expected. These recommendations may be either generic, as for example through orders published
in the Official Journal as in France (JORF, 2010), or recommended through the labelling of the PPP.
Practical recommendations with regard to the specifications of deflectors are provided in section 1.3.
In Germany and France, technical controls are performed and a list of devices having been tested is
available. In future, it is expected that drillers will be generically designed to avoid dust release even
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in the case of precision drilling. Until then, it is proposed that a list of technically accepted devices is
shared within Member States, for example through a website, in order to provide an access to
updated information with regard to the effectiveness of drilling material to reduce seed dust at
drilling. For this purpose COM can offer as a tool an "interest group" in circa to be used to share
information between MS authorities.
Drilling conditions-weather
Practical recommendations with regard to drilling conditions are provided in section 1.4. Similarly
these recommendations may be either generic (see for an example JORF, 2010), or recommended
through the labelling of the PPP. Weather conditions and more particularly wind conditions differ
between countries, and the relative contribution of this factor may thus not be considered in a
harmonized way. Thus efforts to further reduce dust emission at source should be continued as they
may represent the most effective way to limit exposure to negligible levels.
Coating quality and quality control
Coating quality as well as the presence of dusts on the seed during coating, may, if wrongly
performed contribute to releasing dusts during the handling of seeds and seed-bags. Much effort is
invested into the development of formulations being optimized for adherence and resistance to
abrasion to very low levels.
The treatment itself is performed either in industrial facilities or at the farm by farmers themselves
or by contractors.
When performed by seed producers, coated seeds may be certified. Certification systems have been
developed in some countries, as for example in France and Germany, for maize and oil seed rape
treatments, respectively. Certification aims at ensuring a high quality of coating through a high
quality coating process.
The abrasion resistance of treated seeds may easily be controlled and compared to a threshold or
quality standard imposed by the legislation, as an example in France for maize seeds (JORF, 2010).
The amount of dusts produced is commonly measured through a Heubach test. This way, thanks to
the work undertaken in developing certification systems it is possible to define the level of quality it
may be expected to reach for each type of seed.
Seed quality criteria are as a priority needed for seed types that may involve vacuum pneumatic
drillers that need a deflector equipment (as it means the air is pushed up and not down at the soil).
It was the case for maize and oilseed rape which were the first seed types for which coating quality
criteria were developed. Extension to other crops is under way and work is ongoing between these
national initiatives and ESA to align the certifications, aiming at one EU-wide harmonised certification
(and ESTA labelled seed) in future.
Treatment performed in certified facilities can be considered as fulfilling the standard criteria.
Whatever the process used, a control of batches is recommended and batches should be sampled by
the plant/farmer in order to be controlled and prove that they match quality criteria in terms of dust
values.
In Member States, recommendations with regard to coating quality may be either regulatory or
belong to a definition of Good Practice. If regulated, they may, as for driller equipment and weather
conditions, be either generic, or recommended through the labelling of the PPP. The status of seed
coating quality is a Member State issue, although the implementation of certified systems may
contribute to a broader harmonization of practices and make seed exchanges between countries
easier. Further discussions are needed at Authority level to agree on the best way to implement
these measures.
123
Handling conditions
Although representing good sense and good practice, a broad communication about the importance
of handling steps in ensuring that the benefit achieved during the previous step (seed coating
quality) and later step (drilling) is not lost is essential.
124
Appendix XI
Appropriate risk mitigation phrases
Article 49 (4) of Regulation (EC) No 1107/2009 states that "standard phrases for safety precautions as
provided for in directive 99/45/EC have to be included in the labelling of the treated seeds and the
interpretation of this wording should be read as referring to "Safety advice (S phrases)" referred to in
Article 10 paragraph 2.6 of Directive 99/45/EEC. Those can be found in Directive 67/548/EEC. The
safety phrases will be the ones applicable to the plant protection product applied on the seed.
In addition, according to Article 49 (4) of Regulation (EC) No 1107/2009, risk mitigation measures set
out in the authorisation for the seed treatment product have to be included in the labelling of the
treated seeds.
Examples of appropriate safety and risk mitigation phrases adopted at national level are given below:
To protect (aquatic organisms/groundwater/non-target plants/non-target arthropods) (this

product/seed treated with this product) may only be (applied/drilled) with equipment
classified as drift reducing by at least (50%/75%/90%) (cf. Register of risk mitigating application
conditions ...).
The following label must be printed on the seed package: "Treated seeds may only be sown by
using a pneumatic seeding machine which operates with negative pressure, if this machine is
registered in the "List of drift reducing sowing equipment" (Julius Khn-Institut's website at
<http://www.jki.bund.de/geraete)/>)."
To protect (groundwater/aquatic organisms/non-target plants/non-target

arthropods/insects/birds/wild mammals) it is to be assured with an appropriate treatment
process, which includes the use of an appropriate adhesive agent, that the treated seed is
dust-free and abrasion-resistant, unless similarly efficient measures are taken or conditions are
fulfilled (cf. Guideline for the proper compliance with use conditions ....).
The seed treatment shall only be performed in professional seed treatment facilities, which are
registered in the index of "Seed Treatment Facilities with Quality Assurance Systems to
Minimise Dust" (Julius Khn-Institut <http://www.jki.bund.de)/>).
On packaging containing dressed seeds, the following label is necessary: "Do not sow treated
seeds at wind speeds of more than 5 m/s".
On packaging containing dressed seeds, the following label is necessary: "The treated seeds,
including any dust they contain, or dust which is produced during the sowing process, has to
be incorporated completely into the soil".
The following label must be printed on the seed package: The farm manager is obligated to
notify the area designated for the sowing of the treated seeds to beekeepers, whose bee hives
are located within a radius of 60 m to the sowing area, at least 48 hours prior to sowing.
125
Appendix XII
Coating practices: Representative coating practice and conditions

of use of coated seeds within the EU
Table A- 22: Representative coating practice and conditions of use of coated seeds
Crop
arable crops
cereals - spring
Direct sowing or
transplanting
Direct sowing
cereals - winter
Direct sowing
maize, sweet
corn, sorghum
Direct sowing
oilseed rape
Direct sowing
sunflower
Direct sowing
beet (sugar and

fodder)
Direct sowing
beans, peas
Direct sowing
cotton
Direct sowing
flax, poppy seed
Direct sowing
grasses,
grasseed
alfalfa, caraway,
green manure
crops
outdoor
vegetables
onion, carrot,
radish
Direct sowing
Direct sowing
Direct sowing
If direct sowing outdoors,

1
type of driller
Seed treatment technology
mostly mechanical and

seed treatment facilities ( fixed or
pneumatic seed drill equipment,
mobile) and on farm treatment
pneumatic with vacuum
basic seed treatment / basic coating
principle upcoming
stickers more recently introduced
more widely
mostly mechanical and
seed treatment facilities ( fixed or
pneumatic seed drill equipment,
mobile) and on farm treatment
pneumatic with vacuum
stickers more recently introduced
principle upcoming
more widely
Yes, 90% vacuum principle
Professional treatment
basic seed treatment direct on the
seed (active ingredient can be
present on the outside surface of
the seed)
mechanical and pneumatic seed
drill equipment, pneumatic with basic seed treatment / basic coating
vacuum principle upcoming
finishing powder to ensure
flowability of seeds
both mechanical and pneumatic
with and without vacuum
technique are possible
finishing powder to ensure
flowability of seeds
Pneumatic or mechanical
precision drilling equipment
pelleting, with active ingredient not
on the outside of the seed but
closed in by an inert layer; new
development: filmcoating on top of
the pellet
Pneumatic (mainly vacuum
technique) or mechanical
precision drilling equipment
Vacuum pneumatic drilling
equipment
delinting process
mostly mechanical seed drill
equipment, pneumatic with
vacuum principle upcoming
both mechanical and pneumatic basic seed treatment / basic coating
(vacuum) are possible
both mechanical and pneumatic
no seed treatments
(vacuum) are possible
Pneumatic precision drilling

equipment
Film coating/rotostat;
126
Crop
leek
asparagus
chicory, endive,
lamb's lettuce
spinach
beetroot
greenhouse
vegetables
lettuce,
including
lettuce-like
(radichio rosso,
endive,
etcetera)
brassica,
including head
cabbages,
Brussels
sprouts,
cauliflower,
broccoli,
Chinese
cabbage, kale
fruiting
vegetables
(tomatoes,
cucumber, weet
pepper,
eggplant,
etcetera)
celeriac
ornamentals
several
Direct sowing or
1
transplanting
type of driller
Most sowing in
seed beds and
equipment
transplanting later,
approximately
10% direct sowing.
Mostly sowing
outdoors, some
sowing indoors in
trays.
Sowing in seed
beds, later
transplanted.
Direct sowing
mainly coated seed, pneumatic ;
also pelleted seeds, sown
mechanically
Direct sowing
mainly mechanically drilled,
pneumatic equipment upcoming
(both vacuum and gauge
pressure principle)
Direct sowing
equipment
filmcoating/rotostat;
filmcoating/rotostat
filmcoating/rotostat
basic coating, partly filmcoating,
and sometimes toplayer
basic coating
All these crops are

only sown and
raised to young
plants indoors;
later transplanted
indoors or
outdoors.
All these crops are
only sown and
raised to young
plants indoors;
later transplanted
indoors or
outdoors.
not applicable
pelleting, with active ingredient not

on the outside of the seed but
closed in by an inert layer
not applicable
filmcoating/rotostat, and
sometimes top layer
Plant raising only

indoors, later
transplanted
indoors or
outdoors.
In case of outdoor
sowing (e.g.
cucumber in
Germany) vacuum
systems are used.
Sown indoors,
later transplanted
outdoors.

equipment
Cultivation both
not applicable
filmcoating (high value seeds)

127
Crop
ornamental
crops from seed
Direct sowing or
transplanting
indoors and
outdoors; many
crops through
plant raising
indoors; limited
crops directly
sown outdoors.

1
type of driller
1) Mechanical seed drill equipment does not work with air and therefore cannot release air flows.
With pneumatic seed drill equipment there are two principles: using the vacuum principle and using
the gauge pressure principle. When using the gauge pressure principle there is no more air
replacement (with potential dust) than with mechanical seed drill equipment. When using the
vacuum principle seeds are put in the sowing row by vacuum and the excess air will come free. At
conventional corn sowing machines, this exhaust air was directed upwards. Meanwhile, these
machines can be modified: they might be implemented with deflectors directing the exhaust air
downwards to the soil. For vegetable vacuum seed drilling machines, the airflows already always
were directed towards the soil.
2) There is no complete one-on-one relationship crop - seed treatment: which method is used also
depends on e.g. the type of pesticide used, the composition of that pesticide and whether multiple
pesticides are used, seed type (smooth, rough, etc.), to a certain extent for which market the seed is
treated, etc. Also, various terms are used. This table presents an indication. In general, the more
valuable the seed is, the higher quality (and more expensive) seed treatment technology can be
used. Furthermore: coating means stickers are used; in basic coating the pesticide can irregularly be
distributed over the seed, in film coating a regular layer is spread over the seed (used for somewhat
higher valuable seeds); a part of the market has on top of that a top layer (without active ingredient).
128
References in the Appendices

Balsari, P. (2010): Soluzioni operative per il contenimento della dispersione delle polveri nella semina
del mais, Api e mais. Una convivenza possibile Workshop, Rome, July 6, 2010.
Block, T. (2012), data protection claimed.
ESA (2013): European Seed Treatment Assurance a success story in the making.
http://www.euroseeds.org/copy_of_ESA_13.0229.1.pdf
Fallowfield, L. (2010), data protection claimed.
Fent, G. (2012): Non-target ground deposition of dust resulting from sowing pesticide treated seeds
evaluation and analysis of current experimental datasets to establish dust deposition
tables. Source: Industrieverband Agrar, IVA Germany, amendment to report from
November 14th, 2011. Data protection claimed.
Grimbuhler, S. and DGAL (2011): Measurement and risk assessment: efficacy of deflectors. European
workshop on seed protection "Use of Coated Seeds and Granules - Definition of Good
Practices". Paris, 10th and 11th May 2011.
Heimbach et al. (2009): Monitoring of dust drift deposits during the sowing of barley, treated with
Manta Plus in Petri dishes on bare soil in Germany in 2008. Study code: JKI 0822, Julius
Khn-Institut, Braunschweig, Germany (unpublished report)
Heimbach et al. (2010): Monitoring of dust drift deposits during the sowing of maize, treated with
Poncho in adjacent flowering oil seed rape and in petridishes on bare soil in Germany in
2009. Study code: JKI 0905, Julius Khn-Institut, Braunschweig, Germany (unpublished
report)
Heimbach et al. (2011): Monitoring of dust drift deposits during the sowing of maize, treated with
Poncho in adjacent flowering oil seed rape, in Petri dishes on bare soil and in gauze nets
in Germany in 2010. Study code: JKI 1008, Julius Khn-Institut, Braunschweig, Germany
(unpublished report)
Heimbach et al. (2012a): Monitoring of dust drift deposits during the sowing of maize, treated with
Poncho in adjacent flowering oil seed rape, in Petri dishes on bare soil and in gauze nets
in Germany in 2011. Study code: JKI 1115, Julius Khn-Institut, Braunschweig, Germany
Heimbach et al. (2012b): Monitoring of dust drift deposits during the sowing of oil seed rape, treated
with Elado in adjacent flowering Sinapis, in Petri dishes on bare soil and in gauze nets in
Germany in 2011. Study code: JKI 1122, Julius Khn-Institut, Braunschweig, Germany
Heimbach et al. (2013a): Monitoring of dust drift deposits during the sowing of maize, treated with
Poncho Pro in adjacent flowering oil seed rape, in Petri dishes on bare soil and in gauze
nets in Germany in 2012. Study code: JKI 1205, Julius Khn-Institut, Braunschweig,
Germany (unpublished report)
Heimbach et al. (2013b): Monitoring of dust drift deposits during the sowing of barley, treated with
Gaucho 600 FS and Baytan uFB in adjacent flowering Sinapis, in Petri dishes on bare soil
129
and in gauze nets in Germany in 2012. Study code: JKI 1224, Julius Khn-Institut,
Braunschweig, Germany (unpublished report)
Herbst A., Rautmann D., Osteroth H.J., Wehmann H.J. and H. Ganzelmeier (2010): Drift of seed
dressing chemicals during the sowing of maize. Asp. Appl.Biol. 99, 1-5.
Hke S., and W. Burghardt (1997): Schadstoffgehalte und -ausbreitung bodenbrtiger Stube in
Stadt- und Industriegebieten - Teil I: Literaturstudie. Universitt GH Essen, 159 pages
Jans, D. (2010a), data protection claimed.
Jans, D. (2010b), data protection claimed.
Jans, D. (2010c), data protection claimed.
Jans, D. (2010e), data protection claimed.
Jans, D. (2010f), data protection claimed.
Jans. D. (2010d), data protection claimed.
JORF (2009)
JORF (2010): Arrt du 13 avril 2010 modifiant larrt du 13 janvier 2009 relatif aux conditions
denrobage et dutilisation des semences traites par des produits mentionns larticle
L. 253-1 du code rural en vue de limiter lmission des poussires lors du procd de
traitement en usine. Journal Officiel de la Rpublique Franaise, 28 avril 2010, NOR :
AGRG1007789A, texte 22/116.
Knbe, S. (2011a): Investigating the dust deposition during sowing of seed-treated maize seeds with
modified (deflected) vacuum-pneumatic sowing machinery, Eurofins Agroscience Services
GmbH, Germany, Study code: S10-03420, GLP, not published, data protection claimed.
Knbe, S. (2011b): Investigating the dust deposition during sowing of seed-treated oilseed rape seeds
with air assisted (pneumatic) sowing machinery, Eurofins Agroscience Services GmbH,
Germany, Study code: S10-03418, GLP, not published, data protection claimed.
Knbe, S. (2011c): Investigating the dust deposition during sowing of seed-treated oilseed rape seeds
with air assisted (pneumatic) sowing machinery, Eurofins Agroscience Services GmbH,
Germany, Study code: S10-03419, GLP, not published, data protection claimed.
Knbe, S. (2011d): Investigating the dust deposition during sowing of seed-treated sugar beet seeds
with modified (deflected) vacuum-pneumatic sowing machinery, Eurofins Agroscience
Services GmbH, Study code: S10-03228, GLP, not published, data protection claimed.
Neumann, P. and B. Jene (2010): Comparison of measurement methods to assess off-crop drift
deposition patterns of seed treatment particles abraded from dressed maize seeds,
emitted during sowing with a deflector modified pneumatic machine. Source:
Industrieverband Agrar, IVA Germany, Date: January 13th, 2010. Data protection claimed.
Nikolakis, A., A. Chapple, R. Friessleben, P. Neumann, Th. Schad, R. Schmuck, H.F. Schnier, H.J.
Schnorbach, R. Schning and Ch. Maus (2009): An effective risk management approach to
prevent bee damage due to the emission of abraded seed treatment particles during
sowing of seeds treated with bee toxic insecticides. Julius-Khn-Archiv 423: 132-148.
Nikolakis, A. (2009), data protection claimed.
130
Spincer, D. (2010), data protection claimed.

Stevens, J. (2010), data protection claimed.
131
From:
To:
Subject:
Date:
Attachments:
Dwinell, Steve
Kunickis, Sheryl; Epstein, David
FW: Release of SFIREG Interpretation of Neonic Pollinator Protection Label Statements
Wednesday, February 19, 2014 2:28:11 PM
SFIREG Interpretation-Guidance of Neonic Label Statements 21914.pdf
bee-label-info-ltr.pdf
FYI please call if you have any questions or want to discuss.
Steven E. Dwinell
Assistant Director
Division of Agricultural Environmental Services
Florida Department of Agriculture and Consumer Services
850-617-7913
(b) (6)
cell
steven.dwinell@freshfromflorida.com
3125 Conner Boulevard
Tallahassee Florida 32399
www.FreshFromFlorida.com
Please note that Florida has a broad public records law (Chapter 119, Florida Statutes).
Most written communications to or from state employees are public records obtainable
by the public upon request. Emails sent to me at this email address may be considered
public and will only be withheld from disclosure if deemed confidential pursuant to the
laws of the State of Florida.
From: Dwinell, Steve

Sent: Wednesday, February 19, 2014 2:24 PM
To: 'grier stayton'
Cc: Comstock, Jeff; Rabe, Bonnie; Rose Kachadoorian; 'Rowe, Brian (MDA)'; 'Giguere, Cary'
(Cary.Giguere@state.vt.us); 'Meyer, Roy'
Subject: Release of SFIREG Interpretation of Neonic Pollinator Protection Label Statements
Please post the attached document on the SFIREG website and please distribute to SLAs via the list
serve. This document was developed by an ad-hoc committee of SFIREG to provide guidance to
state lead agencies on interpreting the pollinator protection label language required in the August
15, 2013 letter to registrants by USEPA. The document has also been shared with the Office of
Pesticide Programs.
Please direct questions to my attention. Thanks.
Steven E. Dwinell
Assistant Director
850-617-7913
(b) (6)
cell
February 19, 2014

Guidance for state lead agencies on interpretation of pollinator
protection labeling for nitroguanidine neonicotinoid products
required by USEPA in August 15, 2013 letter to registrants. Guidance
developed by SFIREG.
PROTECTION OF POLLINATORS
[Interpretation: This page contains advisory information that is unenforceable. Use of the term
advisory is based on the EPA Label Review Manual, Chapter 3, General Labeling Requirements,
Section III(A). ]
APPLICATION RESTRICTIONS EXIST FOR THIS

PRODUCT BECAUSE OF RISK TO BEES AND OTHER INSECT
POLLINATORS. FOLLOW APPLICATION RESTRICTIONS FOUND IN THE
DIRECTIONS FOR USE TO PROTECT POLLINATORS.
Look for the bee hazard icon in the Directions for Use for each
application site for specific use restrictions and instructions to protect bees
and other insect pollinators.
This product can kill bees and other insect pollinators.
Bees and other insect pollinators will forage on plants when they flower, shed pollen, or
produce nectar.
Bees and other insect pollinators can be exposed to this pesticide from:
o Direct contact during foliar applications, or contact with residues on plant surfaces
after foliar applications
o Ingestion of residues in nectar and pollen when the pesticide is applied as a seed
treatment, soil, tree injection, as well as foliar applications.
When Using This Product Take Steps To:
o Minimize exposure of this product to bees and other insect pollinators when they are
foraging on pollinator attractive plants around the application site.
o Minimize drift of this product on to beehives or to off-site pollinator attractive
habitat. Drift of this product onto beehives or off-site to pollinator attractive habitat can
result in bee kills.
Information on protecting bees and other insect pollinators may be found at the Pesticide
Environmental Stewardship website at:
http://pesticidestewardship.org/PollinatorProtection/Pages/default.aspx.
Pesticide incidents (for example, bee kills) should immediately be reported to the state/tribal lead agency.
For contact information for your state, go to: www.aapco.org/officials.html. Pesticide incidents should also
be reported to the National Pesticide Information Center at: www.npic.orst.edu or directly to EPA at:
beekill@epa.gov
Page 1 of 5
SFIREG http://www.aapco.org/sfireg.html
February 19, 2014
DIRECTIONS FOR USE

1. FOR CROPS UNDER CONTRACTED POLLINATION SERVICES
[Interpretation: This category would include any situation in which beekeepers and
growers/applicators have entered into contracts and agreements that are legally binding
for pollinator services. It would not apply where contracts or agreements (written or
otherwise) pertain to placement of bees on land for honey production.]
Do not apply this product while bees are foraging.
[Interpretation: This would prohibit applications only when bees are actually foraging in
the area to be treated at the time of treatment. However, if other, crop-specific
pollinator protection label statements are more restrictive, those statements would take
precedence.] It is advised that state lead agencies use the Guidance for Inspecting
Alleged Cases of Pesticide-Related Bee Incidents and site inspection evidence to
determine if it can be determined that bees were foraging at the time of application.
The guidance can be found
at http://www.epa.gov/compliance/resources/policies/monitoring/fifra/bee-inspectionguide.pdf
Do not apply this product until flowering is complete and all petals have
fallen
[Interpretation: Application can occur pre-bloom and if flowering has completed on the
crop being treated to the extent that bees are no longer foraging in the crop being
treated.]
unless the following condition has been met.
If an application must be made when managed bees are at the
treatment site, the beekeeper providing the pollination services must
be notified no less than 48-hours prior to the time of the planned
application so that the bees can be removed, covered or otherwise
protected prior to spraying.
[Interpretation: The application of pesticide would be allowed in situations
where managed bees are in or near a treatment site that is under a pollination
contract or agreement. This statement does not exempt the applicator from any
other label use restrictions. See individual crops for specific pollinator protection
application restrictions. If none exist under the specific crop, for foliar
applications, follow all application directions for crops that are contracted to
have pollinator services or for food/feed & commercially grown ornamentals that
are attractive to pollinators.]
2. FOR FOOD CROPS AND COMMERCIALLY GROWN ORNAMENTALS NOT
UNDER CONTRACT FOR POLLINATION SERVICES BUT ARE ATTRACTIVE TO
POLLINATORS
Page 2 of 5
February 19, 2014
[Interpretation: This category would include any situation in which no legally binding
contract or agreement pertaining to pollination services exists between the beekeeper
and the grower of crops that are attractive to pollinators. Such crops are limited to
food/feed crops and commercially grown ornamentals that are attractive to pollinators.
States identify a listing of crops that are considered to be attractive to pollinators for use
when registrants do not voluntarily differentiate crops listed on the label as attractive to
pollinators. For crops that may not drop all petals, flowering is considered complete
when bees are no longer foraging on the crop (e.g. sunflowers).
Food crops are defined by use pattern and include foliar applications to terrestrial food
crop, terrestrial feed crop, aquatic food crop, and greenhouse food crop use sites.
40 CFR 158.1410 Residue chemistry data requirements table.
(b) Use pattern . (1) Data are required or conditionally required for all pesticides used in
or on food and for residential outdoor uses where food crops are grown. Food use
patterns include products classified under the general use patterns of terrestrial food
crop use, terrestrial feed crop use, aquatic food crop use, greenhouse food crop use, and
indoor food use.
Do not apply this product while bees are foraging.

[Interpretation: This would prohibit applications only when bees are actually foraging in
the area to be treated at the time of treatment. However, if other, crop-specific
pollinator protection label statements are more restrictive, those statements would take
precedence.]
Do not apply this product until flowering is complete and all petals have
fallen unless one of the following conditions is met:
[Interpretation: Application can occur pre-bloom, unless other crop specific protection
statements (e.g., pre-bloom restriction) are listed under a specific crop, and if flowering
has completed for the crop being treated to the extent that bees are no longer foraging
in the crop. For crops that may not drop all petals, flowering is considered complete
when bees are no longer foraging on the crop (e.g. sunflowers).]
[Interpretation note: The following conditions apply to both of the directions for
use statements directly above regarding application while bees are foraging and
condition of flowering]
The application is made to the target site after sunset
[Interpretation: The application is made after sunset and before sunrise. Sunset
and sunrise timing is to be established using local weather/solar information. If
other pollinator protection statements on the label are more specific about
nocturnal application timing, they would take precedence.]
Page 3 of 5
February 19, 2014

The application is made to the target site when temperatures are
below 55F
[Interpretation: The air temperature must remain at or below 55F throughout
the application period. Temperature established using local weather station
data.]
The application is made in accordance with a government-initiated
public health response
[Interpretation: Applications for government initiated public health response
would be completed in coordination with state or local government agency
order.]
The application is made in accordance with an active state
administered apiary registry program where beekeepers are notified
no less than 48-hours prior to the time of the planned application so
that the bees can be removed, covered or otherwise protected prior
to spraying.
[Interpretation: If a state maintains a voluntary or regulatory apiary registry
program, the applicator must notify beekeepers with registered apiary locations
in order to use this option. States should identify a specific distance from the
treated crop site within which registered apiary notification will occur.
The application is made due to an imminent threat of significant
crop loss, and a documented determination consistent with an IPM
plan or predetermined economic threshold is met. Every effort
should be made to notify beekeepers no less than 48-hours prior to
the time of the planned application so that the bees can be removed,
covered or otherwise protected prior to spraying.
[Interpretation: Criteria to determine when an imminent threat exists and is
documented would need to be determined by applicator in consultation with
Cooperative Extension, crop consultant, certified crop advisor, or a state
recognized pest management model/tool. Using a state maintained voluntary or
regulatory apiary registry program, the applicator must notify beekeepers with
registered apiary locations. States should identify a specific distance from the
treated crop site within which registered apiary notification will occur. State lead
agencies will determine the adequacy of the level of effort to notify beekeepers
on a case by case basis.]
Page 4 of 5
February 19, 2014

3. Non-Agricultural Products:
Do not apply [insert name of product] while bees are foraging.
[Interpretation: This would prohibit application while bees are actually foraging in the
area to be treated at the time of treatment. If other, crop-specific pollinator protection
label statements are more restrictive, those statements would take precedence.]
Do not apply [insert name of product] to plants that are flowering. Only
apply after all flower petals have fallen off.[
[Interpretation: Application can occur pre-bloom and if flowering has completed to the
extent that bees are no longer foraging in the plants. If other, crop-specific pollinator
protection label statements are more restrictive, those statements would take
precedence (e.g., pre-bloom resctriction).] ASPCRO is developing guidance relative to
residential/structural bee labeling.
Pollinator Protection Labeling FAQ/Guidance
Protection of Pollinators Box
1. The term bee(s) is understood to be a generic term used to identify honeybees,
bumble bees, and other bees that pollinate or collect pollen as forage.
2. The pollinator box is advisory in nature. It is not intended to create regulatory
directions for use or to use web based information in a regulatory fashion. It is only
intended to increase awareness and promote pollinator protective activities. It clearly
indicates application restrictions are found in the directions for use portion of the
label. While the pollinator box references various methods of application such as foliar,
soil, injection, the restrictive use direction language only applies to foliar applications.
3. EPA recognizes that the pollinator box may be too large for consumer labeled products
and is working with consumer product manufacturers to fit the information on
consumer product labels.
4. States should identify a listing of crops that are considered to be attractive to
pollinators. Restrictive use direction language applies to foliar applications only.
5. The statements using minimize relative to exposure or drift onto beehives is advisory
and does not prevent misuse enforcement. Drift onto hives or off target to pollinator
attractive plants (non-target sites) is a violation of directions for use (legal use sites).
Enforcement relative to exposure depends on the direction for use and application use
restrictions if bees are foraging.
Page 5 of 5
From:
To:
Subject:
Date:
Attachments:
Epstein, David
Kunickis, Sheryl
FW: Presentation on SLA efforts
Monday, January 13, 2014 8:55:00 AM
Beekeeper presentation 2014.pdf
FYI: re FL efforts to develop statewide collaboration between beekeepers/growers/aqpplicators
From: Dwinell, Steve [mailto:Steven.Dwinell@freshfromflorida.com]

Sent: Friday, January 10, 2014 8:16 AM
To: John Campbell; JGray@nd.gov; john.scott@ag.state.co.us; Howard, Dennis; Epstein, David
Subject: Presentation on SLA efforts
Attached is the information presented on Jan. 8 to the American Honey Producers Assn meeting on
SLA efforts to improve bee keeper/crop producer cooperation.
Steven E. Dwinell
Assistant Director
850-617-7913
(b) (6)
cell
From:
To:
Subject:
Date:
Attachments:

Epstein, David
FW: Presentation for PNW Insect Management Conference
image001.png
image002.png
image003.png
image004.png
image005.png
Johansen - Pesticide Risk Assessment and Mitigation.pptx
Hi David,
It was good to see you in Portland! Here is my presentation for the PNWIMC.
Take care,
Erik
From: Johansen, Erik (AGR)

To: 'Jana.Lee@ARS.USDA.GOV'
Subject: Presentation for PNW Insect Management Conference
Hi Jana,
Here is my presentation for the PNW Insect Management Conference (Section II, second
presentation).
Take care,
Erik W. Johansen
Phone: (360) 902-2078
Fax: (360) 902-2093
WSDA is now on
CHANGING PESTICIDE RISK ASSESSMENT

AND MITIGATION REQUIREMENTS FOR
POLLINATOR PROTECTION
Erik Johansen, WSDA
PNW Insect Management Conference
Portland, OR
January 6 & 7, 2014
Past - 1
Late 1800s: In WA, crops pollinated by bees
included berries, tree fruits (esp. apples), and
seed crops.
1901: First regulation of pesticides in WA.
1913: WSDA was created.
1921: First known bee poisoning in WA,
copper acetoarsenite (Paris Green) use on
apples. Need to prohibit application during
bloom to protect bees (Melander, WSC).
Past - 2
1952 2002: WSU research on pollination (tree
fruits, small fruits, seed crops) and bee poisoning
from pesticides (Johansen and Mayer).
1960s: Bee poisoning in WA, carbaryl use on corn
(pollen). WSDA adopted rules to protect bees.
1970: EPA was created.
1970s: Bee poisoning in WA, microencapsulated
methyl parathion (Penncap M) use on various
crops, including apples. WSDA adopted rules to
protect bees.
Past - 3
1990s: Bee poisoning in WA; acephate use on
mint, carbaryl use on apples, chlorpyrifos use on
carrot seed crop, methyl parathion EC use on
canola, microencapsulated methyl parathion
(Penncap M) use on apples. WSDA revised rules,
and Section 24c SLN labels, to protect bees.
2000: EPA developed a draft PR Notice on
pollinator protection (not finalized).
2002: Bee poisoning in WA, thiamethoxam use on
pears. WSDA adopted rules to protect bees.
Past Key Points

Severe bee poisoning incidents: highly toxic
insecticides (acute LD50 2 micrograms or less),
with extended residual hazard (RT25 >8 hours).
Label restrictions based on acute toxicity to
adult honey bees (foliar), emphasis was on
agricultural uses.
In general, bee poisoning from systemic
insecticides was not a major concern.
Limited information on other species of bees.
Present - 1
2007: Development of risk assessment for
systemic pesticides in France.
2007 & 2008: Concerns with clothianidin and
dinotefuran in New York, denial of seven
pesticides by NYSDEC.
2007 & 2008: Bumble bee poisoning in Delaware
from imidacloprid use on linden (ornamental).
2008: Bee poisoning in Germany from
clothianidin in fugitive dust (corn seed
treatment).
Present - 2
2011: SETAC Pellston on Pesticide Risk Assessment
for Pollinators, participants from 5 continents.
2011: WSU research on sub-lethal effects of pesticide
residues in brood comb (Wu et al).
2012: EPA SAP White Paper on Pesticide Risk
Assessment for Pollinators: CDPR, Health Canada
(PMRA), and EPA.
2012: Bee poisoning in Canada from clothianidin and
thiamethoxam in fugitive dust (corn seed treatment).
2012: Are Neonicotinoids Killing Bees? (Xerces).
Present - 3
2012: USDA / EPA conference on honey bee health.
Numerous factors (including pesticides) contributing to
decline in honey bee health.
2013: EFSA review of clothianidin, fipronil, imidacloprid
and thiamethoxam.
2013: Petition from Thurston County to restrict use of
neonicotinoids by homeowners. WSDA denied the
petition, submitted comments to EPA, developed a
brochure for homeowners, and supported research.
2013: Interim EPA label restrictions on nitroguanidine
neonicotinoids.
Present - 4
2013: Bumble bee poisoning in Oregon from dinotefuran and
imidacloprid use on linden (ornamental). ODA has required
that labels prohibit use on linden.
2013: How to Reduce Bee Poisoning from Pesticides (OSU
and WSDA).
2013: Penn State research on comparative toxicities and
synergism of insecticides and fungicides to honey bees and
mason bees (Biddinger et al).
2013 & 2014: WSU research on residues of nitroguanidine
neonicotinoids in urban and rural honey bee apiaries
(Lawrence and Sheppard).
Present Key Points

Realization among regulatory agencies worldwide
that existing risk assessment and mitigation to
protect pollinators from pesticides is inadequate.
Acute and chronic effects (adult and immature),
insecticides and fungicides, miticides, multiple
species of bees, multiple routes of exposure,
agricultural and ornamental uses.
(b) (5)
Future
(b) (5)
Questions?
Erik Johansen, WSDA
(360) 902-2078
ejohansen@agr.wa.gov
agr.wa.gov
From:
To:
Subject:
Date:
Epstein, David
Kunickis, Sheryl
FW: Neonicotinoid Discussion
Thursday, July 19, 2012 7:30:00 AM
Should we consider making a formal comment?
From: Zimmer, Trina M [AGLS] [mailto:trina@iastate.edu] On Behalf Of Wintersteen, Wendy [AEX S]

Sent: Wednesday, July 18, 2012 12:10 PM
To: Epstein, David
Subject: Neonicotinoid Discussion
Dear David,
I am writing as a follow-up to the invitation below regarding the Thursday, July 26 discussion
onneonicotinoidseed treatments and the potential impacts on beneficial insects.
Below is a short agenda for the meeting. The topic of our discussion is fugitivedust
fromneonicotinoidseedtreatments and strategies to reduce fugitive dust and movement of
dust off-site. Our goal is to have a fruitful discussion on this topic. Mr. Steve Adams, ISU
Extension Communities Specialist, will serve as the facilitator, assisted by Ms. Lynn Adams,
ISU Extension Communities Specialist. Steve will review ground rules for discussion and
facilitate the discussion so everyone is given a chance to participate.
Registration will open at 9:30 am. Each individual will be asked to register and indicate if
they have formal comments to make during the meeting. Formal comments will be limited
to 5 minutes. A computer and projector will be available if a participant would like to show
a limited number of slides; bring a flash drive to be able to access slides from the laptop.
There is no registration fee and lunch is complimentary. Individuals who are required to pay
for their meals should bring a check made out to Iowa State University for $13. The session
will be held from 10 a.m. to 3 p.m. at the ISU Memorial Unions Gallery Room.
If you have questions, please contact me atwwinters@iastate.eduor at (515) 294-2518.
Thank you.
Agenda
9:30 am:Registration
10:00 am: Welcome
--Dean Wendy Wintersteen andGretchen Paluch, Pesticide Bureau Chief
EPA Staff Introductions and Opening Comments

--Dr. Steve Bradbury, Director, Office of Pesticide Programs, EPA
10:30: Discussion session
Noon: Lunch and small group discussions
1:00 pm: Discussion session, continued
3:00 pm: Adjourn
Sincerely,
Wendy Wintersteen
---------------------------- First invitation-------------------July 10, 2012
Iowa State Universitys College of Agriculture and Life Sciences and the Iowa Department of
Agriculture and Land Stewardship are hosting a discussion of neonicotinoid seed treatments
and potential impacts on beneficial insects. Dr. Steve Bradbury, Director, Office of Pesticide
Programs at the U.S. Environmental Protection Agency, will participate in the discussion.
Stakeholders representing farmers, seed companies, pesticide companies and formulators,
bee keepers, equipment manufacturers and state and federal agencies have been invited to
participate.
The format for this session will be informal. We hope to learn about what different groups
are doing to understand and address potential dust drift and collectively explore practical,
innovative opportunities for minimizing dust drift potential.
The session will be held on Thursday, July 26, from 10 a.m. to 3 p.m. at the ISU Memorial
Unions Gallery Room. A light lunch will be served. Parking is available for a fee in the
Memorial Union Parking Ramp.
If you are available to attend, please RVSP by Friday, July 20, by emailing or calling Trina
Zimmer attrina@iastate.eduor515-294-2518. If you have any questions, please call us.
Sincerely,
Wendy Wintersteen, Dean Bill

Northey, Secretary
Wendy Wintersteen
Dean,CollegeofAgricultureand Life Sciences
Director,IowaAgriculture and Home Economics
Experiment Station
138 Curtiss Hall
Ames,IA50011
515-294-2518
wwinters@iastate.edu
From:
To:
Subject:
Date:
Attachments:
Epstein, David
"depstein315@gmail.com"
FW: Joint USDA - EPA Briefing on Pollinators
Wednesday, June 13, 2012 1:30:00 PM
Draft - Joint USDA-EPA Pollinator Briefing Outline (6-12-12).docx
From: Thomas Moriarty [mailto:Moriarty.Thomas@epamail.epa.gov]

Sent: Tuesday, June 12, 2012 9:44 AM
Cc: Kevin.J.Hackett@usda.gov; Thomas Steeger
Subject: Joint USDA - EPA Briefing on Pollinators
Dave, Jeff,
attached is a revised briefing outline, which reflects comments from our senior management.
I would like to a brief conversation today between us.
I suggest noon.
tm
(See attached file: Draft - Joint USDA-EPA Pollinator Briefing Outline (6-12-12).docx)
(b) (5)
(b) (5)
From:
To:
Cc:
Subject:
Date:
Attachments:
Epstein, David
Pettis, Jeff
Kunickis, Sheryl
FW: Joint Briefing
Tuesday, June 12, 2012 9:26:00 AM
Joint USDA-EPA Briefing Outline - Pollinator Protection (EPA Draft 6-7-12).docx
Jeff,
Please see email from Tom Moriarty, below, and attached Word doc. This is the document we
discussed last week being developed for a meeting between upper administration at USDA and EPA.
Let me know your thoughts. I am working from home, all week. Mobile # 202-603-9142.
Dave
From: Thomas Moriarty [mailto:Moriarty.Thomas@epamail.epa.gov]

Sent: Tuesday, June 12, 2012 6:41 AM
To: Epstein, David
Subject: Joint Briefing
Dave,
Our respective agencies are going to need to start drafting the Joint Briefing Paper immediately.
We should be sure that both of us are in agreement with the structure; and who will be taken which
section for presentation.
Can I speak with you at some point today? Should you (or we) speak with Sheryl on these points?
I hope you're feeling ok and that this sort of stuff doesn't prolong your difficulties.
OK,
writer or call me and we can go from there.
tom m
703.305.5035
c: 301.775.0593
(b) (5)
(b) (5)
From:
To:
Subject:
Date:
Kunickis, Sheryl
Epstein, David
FW: From Canada: New 2014 BMPs for Pollinator Protection and Use of Insecticide Treated Seed | OMAF and
MRA Field Crop News
Tuesday, April 01, 2014 11:21:16 AM
http://fieldcropnews.com/2014/01/new-2014-bmps-for-pollinator-protection-and-use-ofinsecticide-treated-seed/
New 2014 BMPs for Pollinator Protection and Use of Insecticide Treated Seed
by Tracey Baute January 20, 2014 OMAF and MRA and the Pest Management Regulatory
Agency (PMRA) have worked together to develop new Best Management Practices (BMPs)
for Pollinator Protection and Responsible Use of Insecticide Treated Seed for the 2014
season. The new BMPs can be found here: 2014 BMPs for Pollinator Protection and will also
available on both of the pollinator protection webpages of PMRA and OMAF.
Three key components of the BMPs that need to be pointed out are:
1. New Lubricant Requirement: For 2014, the Fluency Agent by Bayer CropScience is the
only lubricant that can be used for seed flow purposes in corn and soybean planters that are
planting neonicotinoid treated seed (eg Poncho, Cruiser, Stress Shield etc). Talc and
graphite are no longer permitted for this purpose.
What does this mean? If a grower needs a lubricant for seed flow in his corn or soybean
planter, they must use the Fluency Agent. Talc and talc/graphite blends are not allowed to
be used for this purpose. If a grower requires graphite to lubricate the planting mechanism
(eg. finger pick-up units for corn or for mechanical metering units for soybeans) this is still
acceptable.
If a grower hasnt used a lubricant in their planter in the past, then they dont have to start
using the Fluency Agent now. This is strictly to replace the past usage of talc and graphite
for planters that needed it to help move the seed through the system.
The rate is the same for both corn and soybeans at 1/8 of a cup per unit of seed (80,000
kernels of corn or 140,000 soybean seeds). DO NOT use more than the recommended rate
or you risk producing more contaminated dust from the exhaust manifolds.
2. Reduce Dust Drift: Multiple measures, in combination, will be needed to reduce

pollinator exposure from contaminated dust coming from vacuum planters. This includes
using the Fluency Agent as well as using deflector equipment, where appropriate to direct
exhaust to the ground level and avoid planter dust drifting onto flowering trees and weeds.
Another recommendation is to clean the fan housing and hoppers of vacuum planters
regularly between planting fields to reduce the accumulation of contaminated dust within
the exhaust manifolds and hoppers.
A study conducted in 2013 by Baute (OMAF), Schaafsma (UGRC) and Scott Dupree (UG
SES) found that there is no doubt that a significant amount of contaminated dust is
exhausted from negative vacuum planters and that the Bayer Fluency Agent can reduce the
quantity of neonic active ingredient in the dust emitted by 28%. Our study also found that
flowering trees (esp. maples, willows, hawthorn, apples and dogwood) around/near field
perimeters are a major foraging resource for bees during corn planting and that
contaminated dust likely reaches these trees during planting, posing a significant exposure
risk. A combination of measures need to be taken to reduce both the quantity of dust being
emitted from the planters as well as the drifting of this dust onto the flowering trees and
weeds along the fields boundaries.
Information on deflector equipment will be made available later this week and will be
posted on this site. Stay tuned.
3. Follow IPM and Use Fungicide Only Seed: It is time to start using these insecticide
seed treatments only when necessary. Not every acre in the province needs protection
from wireworm and grubs. Only 10 to 20% of the acres are at risk of these two pests,
particularly those fields with sandy or silty soils. It is time to re-assess which fields are at
high risk. Growers in low pest risk situations should consider planting fungicide only seed.
Growers with fields near bee yards or those with significant foraging resources around
their fields (flowering trees and weeds like willows, maples, hawthorns etc, dandelions)
should consider planting those fields to fungicide only seed unless they are at high risk of
pest issues. If these types of fields must be planted with a neonic seed treatment, then
the grower needs to take the extra measures to reduce the dust drift described above
under #2.
Current information on high risk factors and scouting techniques for early season pests can
be found here: http://www.omafra.gov.on.ca/english/crops/pub811/13general.htm OMAF
and MRA is also working on an IPM/Soil Insect Scouting booklet which will be made available
for this planting season to help growers and reps with their decision making.
These three components above are not the only important recommendations for 2014. I
encourage you to take the time to read the 2014 BMPs for Pollinator Protection document
and implement as many measures as possible to reduce pollinator risk.
We all have a role to play in reducing the risk to pollinators this spring. If we want to still
have access to neonicotinoid insecticide treated seed for crop protection when needed, we
need to take extra measures this year in particular to keep the dust from leaving these
fields. We need to see fewer bee kill incidents at planting time if we have any hope of
showing a balance can be met, where neonic insecticide seed treatments can be used where
needed without placing pollinators at risk.
Print Friendly
http://fieldcropnews.com/2014/01/new-2014-bmps-for-pollinator-protection-and-use-ofinsecticide-treated-seed/
From:
To:
Cc:
Subject:
Date:
Attachments:
Kunickis, Sheryl
Onwulata, Charles
Epstein, David
Fw: Dr. Onwulata
Monday, October 28, 2013 3:01:16 PM
Honey Bee Colony Declines Onwulat.docx
USDA bee research.docx
Final Report HB Stakeholder Conference 2013.pdf
CO slides.pptx
Hi Charles,
Dr. Epstein has prepared materials for your use (see attached) and message below. As we were not
sure how this and "an evidence-based approach" fits with the template you sent, we thought it
would work better if you populate the slides based on how you want to present the information. Let
us know if you have questions. We are available to answer questions, etc. Also, could you send the
agenda for Science Council?
Thanks!
Sheryl

Sent: Monday, October 28, 2013 02:00 PM
Subject: Dr. Onwulata
Sheryl,
In response to Dr. Onwulatas request for information related to Honey Bees:
Evidentiary Research: (b) (5)
The five possible causes:(
b
)
(
5
)
Current research or policy: Current research not captured in the USDA research attached
document:
a)
USDA funded a Honey Bee Area-wide project to increase colony survival and
availability for pollination and thus increase the profitability of beekeeping. The
project included four ARS labs in 4 states (MD, AZ, LA and TX) and showed
improvement in bee survival by use of newly developed resistant bees, supplemental
protein feeding over winter, and aggressive management of the varroa mite.
b)
USDA funded two Coordinated Agricultural Project (CAP) grants that assembled a
nationally-coordinated team of experts with proven capacity in extension, genomics,
pathology, toxicology, management, pollination, and bee behavior, with a long-term
c)
d)
e)
f)
g)
h)
goal to restore large and diverse populations of managed bee pollinators across the
United States to sustain natural and agricultural plant communities.
USDA continues on-going measures to (i) better understand the potential hazards
pesticides pose to bees, specifically neonicotinoids and fungicides; and (ii) reduce
exposure from pesticides to bees specifically at almond farms and field crops such as
cotton, corn, and soybean. Increasing this focus, USDA recently (FY 2013)
implemented a one year, Area-wide scale project to find means to limit honey bee
exposure to pesticides. EPA will contribute to this research effort.
USDA continues on-going measures to determine, on a regional basis, plants that
provide the best nectar and pollen resources for honey bees and for which seeds are
available and economically feasible for landowners.
USDA sponsors annual surveys of: i) honey bee pests and diseases and ii) assessment
of bee health, colony numbers, and to collect beekeeper input on honey production
hives and invasive pest detection in hives .
USDA continues efforts provide quality honey bee forage and to increase beekeeper
access to federal and private lands, particularly through the Crop Reserve Program
(CRP) and the Environmental Quality Incentives Program.
USDA is beginning a five-state project in ND, SD, MN, WI and MI to increase
managed honey bee access to healthy forage. Over sixty percent of managed honey
bees spend the summer months in the upper Midwest.
Corn dust consortium: research project involving 2 land-grant universities, US Corn
Growers Association, an NGO, ag equipment manufacturers, seed and crop
protection product companies investigate use of alternative see lubricants for use
in corn seed planters to mitigate pesticide abraded dust associated with planting
Gaps (area where research could be funded): (b) (5)
Regards,
David
Office: (202) 720-9877
Work Mobile:(b) (6)
(b) (5)
(b) (5)
(b) (5)
10-23-2013
Honey Bee Colony Declines
Honey bee colony declines over the past decade are a serious problem threatening the health
of honey bees and the economic stability of commercial beekeeping and pollination
operations in the United States. In October 2006, some beekeepers began reporting losses of
30-90 percent of their hives. While colony losses are not unexpected, especially over the
winter, this magnitude of losses was unusually high.
Despite a number of claims in the general and scientific media, a cause or causes of colony
declines and Colony Collapse Disorder have not been identified by researchers.
There are multiple factors playing a role in pollinator declines, including parasites and
disease, genetics, poor nutrition and pesticide exposure.
Parasites and Disease:

The parasitic Varroa mite is recognized as the major factor underlying colony loss in the
U.S. and other countries. There is widespread resistance to the chemicals beekeepers use
to control mites within the hive. New virus species have been found in bees in the U.S.
and several of these have been associated with CCD. The Varroa mite is a primary factor
known to increase levels of some bee viruses.
Genetics:
U.S. honeybee colonies need increased genetic diversity. Genetic variation improves bee
thermoregulation (the ability to keep body temperature steady even the surrounding
environment is different), disease resistance and worker productivity.
Poor Nutrition:
Nutrition has a major impact on individual bee and colony longevity. Poor nutrition can
shorten bee life spans and make bees more susceptible to harm from exposure to disease,
parasites and other stressors, including pesticides and other environmental contaminants.
Bees need better access to a variety of plants for forage to support colony health.
Pesticide Exposure:
Acute and sublethal effects of pesticides on honey bees have been increasingly
documented, and are a concern but it is not clear, based on current research, whether
pesticide exposure is a major factor associated with U.S. honey bee health declines. The
most pressing research questions relate to determining the effects of actual field-level
pesticide exposures that bees experience.
Consensus is building that a complex set of stressors contribute to pollinator declines, and
researchers are increasingly studying multiple factors of colony losses. Steering committee
members and stakeholders at the October 15, 2012 national conference agreed that the following
research questions and policy actions should be considered:
Undernourished or malnourished bees appear to be more susceptible to pathogens,

parasites, and other stressors, including pesticides and other environmental contaminants.
Research is needed on forage, pollen quality, artificial and natural food sources, and food
processing and storage in the hive.
Federal and state partners should consider actions affecting land management, including
management of rights-of-way, to maximize available nutritional forage to promote and
enhance good bee health and to protect bees by keeping them away from pesticide-treated
crop acreage.
1
10-23-2013
Pathogens and parasites have major negative impacts on colonies. The management of
the parasitic Varroa mite and viruses needs special attention.
More outreach to farmers on managing potential exposure of honey bees to pesticides is
needed. Efforts would benefit from involvement of beekeepers, crop consultants,
pesticide manufacturers, pesticide applicators, state lead agencies and extension agents.
Beekeepers accentuated the need for accurate and timely beekill incident reporting,
monitoring, and enforcement.
Breeding should emphasize traits such as hygienic behavior that confer improved
resistance to Varroa mites and diseases (such as American Foulbrood).
Best management practices associated with bees and pesticide use exist, but are not
widely prioritized or systematically followed by members of the crop producing industry.
We need informed and coordinated communication between growers and beekeepers and
effective collaboration between stakeholders.
From:
To:
Subject:
Date:
Attachments:
Epstein, David
Kunickis, Sheryl
FW: Decsion by the Netherlands on several imidacloprid=based products
Monday, February 03, 2014 9:25:39 AM
Bayer Statement Imidacloprid NL final.pdf

Received: Sunday, 02 Feb 2014, 4:41pm
To: Kunickis, Sheryl [Sheryl.Kunickis@ARS.USDA.GOV]; Epstein, David
[David.Epstein@ARS.USDA.GOV]
Subject: Decsion by the Netherlands on several imidacloprid=based products
I would like to advise you of a public announcement being made this week by the Dutch Board for the
Authorization of Plant Protection Products and Biocides (Ctgb) regarding their re-evaluation of
imidacloprid-based crop protection products and resulting regulatory action.
Attached is a statement explaining the actions being taken and Bayer CropSciences position on it. If
you have any questions, please feel free to contact me.
Jean Reimers
Bayer CropScience
Suite 720
Tel: 202-756-3779
Fax: 202-628-6622
Mobile: (b) (6)

Statement on recent decisions by the Dutch authority (Ctgb) to withdraw

authorizations for certain Imidacloprid uses
In January 2014 the Dutch Board for the Authorisation of Plant Protection Products and
Biocides (Ctgb) in the Netherlands decided to withdraw the authorization for certain
Imidacloprid uses. Bayer CropScience comments as follows:
Gaucho use in sugar beet and fodder beet; Gaucho Tuinbouw use in cabbage
Ctgb has decided to withdraw the registrations of Gaucho (Imidacloprid WS 70) for use in
sugar beet and fodder beet, and of Gaucho Tuinbouw (Imidacloprid WS 70) in cabbage as of
31 January 2014. The period of grace for the use of existing stocks of Gaucho Tuinbouw in
cabbages is until 1 May and until 1 July for Gaucho in sugar beet and fodder beet. These
deadlines still allow for treatment of the concerned crops in the upcoming growing season
2014. The uses of Gaucho Tuinbouw in lettuce and endive remain authorized.
In Bayer CropSciences opinion, its seed treatment products Gaucho and Gaucho Tuinbouw
are safe for birds, when used responsibly and properly, according to label instructions. The
basis for Ctgbs decision regarding beets and cabbages are new bird risk assessments
which are not based on new data but on new assumptions concerning exposure. For beets
the allegedly identified risk involves exposure of birds to beet pills mistaken for grit, and for
cabbages it concerns exposure via the uptake of seedlings.
Bayer CropScience considers the conducted risk assessments to be highly conservative and
therefore unrealistic. An example for the highly conservative assumptions in the risk
assessment is the underlying exposure value for cabbage which was taken to be a
consumption of 228 grams of cabbage per bird within a short period of time.
Admire field applications

Ctgb decided to withdraw several field applications of Admire (Imidacloprid WG 70) in
ornamental crops (spray applications in ornamentals, tree nursery, flower bulbs, perennials)
as of 31 January 2014. The period of grace for use of existing stock is until 1 May 2014.
Admire fields of uses such as dipping of bulbs of ornamentals (e.g. lily), and all greenhouse
uses remain authorized.
This decision to withdraw Admire uses was triggered by a recently published study by
Roessink et al.1. The results of this study caused the authority to lower the endpoint relevant
for the aquatic risk assessment. While the Roessink study was carried out under laboratory
conditions, Bayer CropScience conducted an additional semi field study carried out under
more realistic agricultural conditions. The protocol had been discussed with Ctgb and the
study was carried out with Roessink as independent study director. The new data clearly
demonstrates that there are no unacceptable long term effects on the sensitive aquatic
organism tested under field conditions.
Based on available data, Bayer CropScience is convinced that changing the endpoint for
imidacloprid on aquatic organisms is not justified.
Bayer CropScience is willing to continue to work together with the Dutch board for the
Authorisation of Plant Protection Products (Ctgb) to handle the complex issue of appropriate
and realistic risk assessments of imidacloprid.
1
Roessink I., Merga L.B., Zweers H.J., Van den Brink P.J. (2013): The neonicotinoid imidacloprid shows high chronic toxicity to
mayfly nymphs. Environ Toxicol Chem. 2013 Apr;32(5):1096-100. doi: 10.1002/etc.2201. Epub 2013 Apr 3.
From:
To:
Subject:
Date:
Epstein, David
Kunickis, Sheryl
FW: bees, potatoes
Fyi: interesting portrayal of ownership of the list under development

-----Original Message----From: Laws, Meredith [Laws.Meredith@epa.gov]
Received: Tuesday, 28 Jan 2014, 2:31pm
To: Andy Jensen [ajensen@potatoes.com]; Rossi, Lois [Rossi.Lois@epa.gov]
CC: Epstein, David [David.Epstein@ARS.USDA.GOV]
Subject: RE: bees, potatoes
Dear Dr. Jensen,
Thank you for your inquiry. At this time EPA does not have a list of crops or plants that are attractive
to bees. Its my understanding that a list is being developed by USDA. You may wish to contact Dr.
David Epstein at USDAs Office of Pest Management Policy. Ive copied him on this email. He may be
able to advise you.
Sincerely,
Meredith
Meredith Laws
(703) 308-7038
From: Andy Jensen [mailto:ajensen@potatoes.com]

To: Rossi, Lois; Laws, Meredith
Subject: bees, potatoes
Ms. Rossi and Laws,
I work in research management for the potato industry in the Northwest. We have been concerned
about the future of neonicotinoids in potatoes. I have been asked to find the answer to a specific
question: Does the EPA have a list of crops or plants that are considered to be attractive to
pollinators? Or conversely, a list of crops NOT attractive to pollinators? We know that potato
flowers are rarely visited by bees, but wonder whether scientific documentation of this would be
important. Any existing opinions or lists from EPA regarding crops attractive to bees would
therefore be valuable.
Regards,
Andy
Andy Jensen, Ph.D.

Manager, Northwest Potato Research Consortium
4032 N Ballantyne Ln.
Eagle, ID 83616
Home Office: 208-939-9965

Cell: (b) (6)
Web: www.nwpotatoresearch.com
From:
To:
Subject:
Date:
Attachments:
Kunickis, Sheryl
Epstein, David
FW:
Wednesday, September 04, 2013 2:49:16 PM
0048F86C1.pdf
David,
This letter was received at USDA. I have indicated that EPA should respond. Thought you
would find it interesting.(b) (5)
Sheryl
(b) (5)
(b) (5)
(b) (5)
From:
To:
Subject:
Date:
Attachments:
Keigwin, Richard
Kunickis, Sheryl
Fw: Agenda & Update document for Monday
Monday, July 29, 2013 2:15:56 PM
Letterhead Agenda.docx
From: Keigwin, Richard

Sent: Sunday, July 28, 2013 9:17:59 AM
To: Bradbury, Steven; Brady, Donald; Rossi, Lois; Guilaran, Yu-Ting; Ellenberger, Jay; Steeger,
Thomas; Clock-Rust, Mary; Laws, Meredith; Pease, Anita; Moriarty, Thomas; Anderson, Neil
Cc: Fehrenbach, Margie
Subject: FW: Agenda & Update document for Monday
Materials for Monday's 2pm meeting with ASTA and CLA.
From: Andy LaVigne <alavigne@amseed.org>

Sent: Friday, July 26, 2013 2:21 PM
To: Keigwin, Richard
Cc: Ray McAllister; Bernice Slutsky; Mary Emma Young (MYoung@croplifeamerica.org)
Subject: Agenda & Update document for Monday
Rick,
I hope this forward isnt too late for yall to review before the meeting on Monday. I got a little
behind this week because of a trip to CA. For your information, I am attaching:
1. A draft document for the meeting Monday. We realize that we have an hour and want to
make sure there is plenty of time for Q & A/dialogue following the presentations.
2. A progress report on where we are on the Seed Treatment Stewardship Guide education &
outreach effort to date.
Let me know if you have any questions or would like any additional information for the meeting.
Best regards,
Andy
Andrew W. LaVigne
President and CEO
American Seed Trade Association
(703)837-8140 - office
(b) (6)
- cell
(703)837-9365 - fax
alavigne@amseed.org
American Seed Trade Association/CropLife America
Environmental Protection Agency

2-3pm, July 29, 2013
Agenda
Welcome
Steve Bradbury, EPA
Introductions
Andy LaVigne, ASTA
Ray McAllister, CropLife America
Seed Treatment Stewardship Report and Plan
Andy LaVigne
Phase I
General Communications and Outreach Successes
March - July, 2013
Phase II
Crop-Specific Communications & Outreach: Corn
August 2013 - June 2014
Comments, Input and Questions
1) Website Analytics
Google Analytics as of July 17, 2013: www.seed-treatment-guide.com
Since Launch: Last 30 Days:
Visits:
5.804
715
Unique Visitors:
4,517
565
Page views:
16,773
1,927
Pages per visits:
2.89
2.70
Average time of site: 2:46
2:36
Bounce rate:
48.69%
52.31%
New visits:
77.83%
74.83%
Bounce rate -- anything between 40-60% is standard.
A bounce occurs when a web site visitor only views a single page on a website, that is,
the visitor leaves a site without visiting any other pages before a specified sessiontimeout occurs.
Average time on site is above average.
Average time on site is a type of visitor report that provides data on the amount of time
(in minutes or seconds) visitors have spent on the website.
Direct traffic accounts for 3,035 visits or 59.89% of the traffic.
Direct traffic represents the number of visitors who directly access the website.
Demographics:
Visitors primarily come from the US and Canada. In the US, top states sending traffic
are:
1. Iowa
2. Missouri
3. North Carolina
4. Minnesota
5. Illinois
6. Virginia
7. Indiana
8. California
9. Ohio
10. DC
11. Colorado
9.37% of users are on mobile devices, 3.78% are on tablets, and the remaining
86.85% are on computers
24% of users who come in on the homepage click directly to the Guide.
8% of users come in directly on the guide itself.
Indirect Links
Google reports that the website links pointing to the site from over 251 domains.
Domains
amseed.org
ncga.com
websitetestlink.com
seedquest.com
sentryair.com
geoipfacts.com
precisionpays.com
agprofessional.com
apinews.com
minnesotafarmguide.co
m
free-doc-lib.com
financialcontent.com
seedworld.com
vt.edu
agwired.com
prlog.ru
farmandranchguide.com
ulitzer.com
ilsoy.org
igrow.org
brownfieldagnews.com
midwestproducer.com
wiki.gov.cn
blogspot.com
theprairiestar.com
croplifeamerica.org
seedtoday.com
agropages.com
ksfy.com
einnews.com
wlbt.net
woi-tv.com
newson6.com
ocj.com
pesticidestewardship.org
oregonseed.org
wufile.com
kfvs12.com
kten.com
wafb.com
wtvm.com
thegrower.com
wcax.com
domainmetrics.de
agmachine-benelux.com
wspa.com
optimum.net
wordpress.com
americanagnetwork.com
topsy.com
noodls.com
kwqc.com
4-traders.com
bayer.com
worldnow.com
ktul.com
growingtennessee.com
newswest9.com
growingalabama.com
19actionnews.com
cbs19.tv
bizjournals.com
growingillinois.com
ksn.com
fox4now.com
growingcoloradofarms.c
om
plantmanagementnetwor
k.org
nbc11news.com
growingnm.com
growingindiana.com
askives.com
kalb.com
wxtx.com
google.com
hsoub.com
9and10news.com
cw15kxvo.com
growingpennsylvania.co
m
seedbuzz.com
wkbn.com
lawbc.com
southeastfarmpress.com
growingohio.com
growingsc.com
wripmc.org
sacbee.com
wsfa.com
wrdw.com
kcbd.com
kltv.com
ufl.edu
growingms.com
russiaherald.com
kionrightnow.com
counton2.com
mssoy.org
klkntv.com
kiiitv.com
seoprofiler.com
nbc4i.com
thecropsite.com
naega.org
boston.com
eurofinsus.com
cbs8.com
wboy.com
nsai.co.in
growingiowa.com
wdam.com
sccsafarms.org
growingkentucky.com
wbay.com
cnbc.com
stockenews.com
kait8.com
sandiegojack.com
hpj.com
wfmj.com
kgwn.tv
ntokcotton.org
kxnet.com
montana.edu
epa.gov
actagroup.com
growingtx.com
wtoc.com
ksla.com
14news.com
farmprogress.com
asabe.org
kctv5.com
statscrop.com
katv.com
hometownstations.com
growingwisconsin.com
hoosieragtoday.com
wric.com
asme.org
growingnorthdakota.co
m
linexlegal.com
growingoregon.com
koenigequipment.com
pbcgov.com
growingnorthcarolina.co
m
kljb.com
yahoo.com
kycorn.org
kxxv.com
dealbreaker.com
give-me-doc.com
keyc.tv
growingid.com
mexicostar.com
agrimarketing.com
valleynewslive.com
investorpoint.com
farmindustrynews.com
growinglouisiana.com
wrcbtv.com
nytimes.com
kmph-kfre.com
farmandlivestockdirecto
ry.com
walb.com
independentseeds.com
ktvn.com
justmeans.com
wooeb.com
foxnebraska.com
internationalsugarjourna
l.com
syngentacropprotection.
com
kpho.com
growingmissouri.com
sfntoday.com
nasdaq.com
doc-txt.com
aberdeennews.com
istockanalyst.com
growingoklahoma.com
sys-con.com
kcautv.com
ibtimes.com
wnd.com
growingny.com
sd.gov
syngenta-us.com
wnem.com
growingminnesota.com
fox8live.com
alabamas13.com
everything-pr.com
sectorpublishingintellige
nce.co.uk
ebookbrowse.com
pioneer.com
newschannel10.com
wlox.com
digitaljournal.com
sugarproducer.com
greenbook.net
wxvt.com
wset.com
kusi.com
moseed.org
hawaiinewsnow.com
arabherald.com
nj.com
toledonewsnow.com
tpsalliance.org
federaleagle.com
nufarm.com
wfsb.com
growingsouthdakota.co
m
waff.com
prnewswire.com
growingwashington.com
growinggeorgia.com
growingarizonafarms.co
m
growingkansas.com
lasvegasherald.com
mediaroom.com
wsls.com
growingfl.com
news10.com
tucsonnewsnow.com
growingva.com
agra-net.com
travelweekly.com
news9.com
futurefarm.eu
myfoxal.com
wowktv.com
reuters.com
wthr.com
croplife.com
bioportfolio.com
beckerunderwood.com
redorbit.com
wedbush.com
klfy.com
3blmedia.com
streetinsider.com
growingnebraska.com
syngentaprofessionalpro
ducts.com
wkrg.com
wnct.com
khq.com
wjhl.com
elnonline.com
nbc29.com
growingmi.com
ktxdtv.com
cbs3springfield.com
Traffic has been brought to the website via searching for 212 organic keyword
phrases. The most popular of which have been:
Seed treatment
Seed treatment guide
Seed treatment stewardship website
Seed treatment stewardship
Seed treatments stewardship
Seed treatment products
Seed act
ASTA seed treatment
Croplife seed treatment
ASTA seed stewardship
Croplife seed stewardship
Seed treatment tags
Seed treatment and presentation
Dust seed treatment plant protection
products
Guidelines for managing treated seed
effectively
Handling treated seed
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Seeds treated with pesticides
environmental hazards
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America
Refilling containers pesticide seed
treatments
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Safe storage of treated seed
Treated seed
Treated seeds
Seed treatment guidelines
Seed treatment questions
Seed treatment rules
Seed treatment worker safety
Transporting treated seed
Seed glossary
Disposal of treated seed
2) Circulation Numbers
Description: The Guide to Seed Treatment Stewardship received media coverage in
approximately twelve multi-media outlets in the agriculture trade sector, representing
radio, print and online coverage. The list below includes total circulation numbers of
news outlets that reported on the Guide to Seed Treatment Stewardship, representing total
quantifiable potential impressions.
Minnesota Farm Guide:
Print: 26,194
Online: 2,161 (unique visitors per month); 5,315 (page views per month)
Southeast Farm Press:
Print: 45,000
CropLife Magazine:
Print: 20,818
Farm Futures:
Print: N/A
AgWired:
KTIC-AM Online:
AgProfessional:
Print: 23,038
The Crop Site:
Online: Approximately 22,000 (unique visitors per month)
New Seed Treatment Guide Helps Farmers, Others

(Posted Mon. Mar 25th, 2013)
Mar. 25: A new guide to seed treatment stewardship has been developed by the
American Seed Trade Association and CropLife America to promote the safe handling
and management of treated seed by farmers and others, a service appreciated by the
National Corn Growers Association.
This guide will be an invaluable resource for our members, said NCGA President Pam
Johnson and Iowa corn grower. Were encouraging all corn growers to refer to it before,
during and after the corn planting season.
Endorsed by NCGA, the American Farm Bureau Federation and the American Soybean
Association, The Guide to Seed Treatment Stewardship provides farmers and seed
companies with critical information and up-to-date guidelines for managing treated seed
effectively to further minimize the risk of exposure to non-target organisms.
ASTA and CLA began aggregating seed treatment research and safety information from
universities, seed companies, international seed associations and others in early 2012 in
response to growing concern about the effect of seed treatment dust on pollinators.
The guide contains recommendations for planting of treated seed, safe use of seed
treatment products, safe handling and transport of seed, selection of treatment products,
labeling of treated seeds and storage of treated seed. It also includes a seed treatment
glossary and an exhaustive list of resources.
3.
March 22nd Syngenta news release, Now available: Seed Treatment Stewardship
Guide http://www.syngenta-us.com/news releases/news.aspx?id=171554
With spring planting upon us, it is critical growers and others who work with treated
seeds practice careful stewardship. ASTA and CropLife America launched new website
www.seed-treatment-guide.com featuring a comprehensive Seed Treatment
Stewardship Guide, helpful resource links and valuable information concerning handling,
transporting and storage of treated seeds.
4.
March 25th CropLife America news release, Ag Industry Launches Campaign to
Promote Safe Use of Seed Treatments http://www.croplifeamerica.org/news/cla/32513Ag-Industry-Launches-Campaign-to-Promote-Safe-Use-of-Seed-Treatments
Washington, DC The American Seed Trade Association (ASTA) and CropLife

America (CLA), two industry leaders in agricultural seed, products, services, and plant
science solutions, announced today the release of The Guide to Seed Treatment
Stewardship, an industry-wide initiative to promote the safe handling and management of
treated seed.
Endorsed by the National Corn Growers Association, the American Farm Bureau
Federation and the American Soybean Association, The Guide provides farmers and seed
companies with critical information and up-to-date guidelines for managing treated seed
effectively to further minimize the risk of exposure to non-target organisms.
The Guide serves as an all-in-one resource that addresses every stage of a seeds journey
from treatment to planting, said ASTA President and CEO Andrew W. LaVigne. Its
designed to be convenient, easy-to-understand and useful to the entire seed and crop
production value chain.
The Guide will be an invaluable resource for our members, said Pam Johnson,
president of the National Corn Growers Association. Were encouraging all corn
growers to refer to it before, during and after the corn planting season."
ASTA and CLA began aggregating seed treatment research and safety information from
universities, seed companies, international seed associations and others in early 2012 in
response to growing concern about the effect of seed treatment dust on pollinators.
"The health of pollinators, especially honey bees, is crucial to agricultural production in
the U.S. and worldwide, noted Jay Vroom, president and CEO of CLA. The crop
protection industry, seed growers and breeders, seed treatment companies, equipment
manufactures and farmers all play a role in supporting thriving bee populations through
stewardship and sound science.
The Guide contains recommendations for such processes as:
Planting of Treated Seed
Safe Use of Seed Treatment Product
Safe Handling and Transport of Seed
Selection of Treatment Product
Treated Seed Labeling
Storage of Treated Seed
The Guide, which also includes a seed treatment glossary and an exhaustive list of
resources, has been shared with EPA and USDA, both of whom have applauded the
industrys initiative in this effort.
Released in advance of the April 11, 2013 Corn Planting Day, The Seed Treatment
Stewardship Guide is available online and in PDF format at www.seed-treatmentguide.com.
This item also ran in Seed Association newsletters in Oregon, Illinois, Iowa and Texas.
5.
Wall Street Journal: June 13, 2013 Monsanto Company Forms Honey Bee
Advisory Council, Pledges Support For Honey Bee Health At First-Of-Its-Kind Summit
http://online.wsj.com/article/PR-CO-20130613-909292.html?mod=googlenews wsj
6.
Pesticide & Chemical Policy: April 4, 2013 Industry addresses neonic concerns
with treated seed stewardship manual http://www.agranet.com/portal2/ptcn/home.jsp?template=newsarticle&artid=20018035912&pubid=ag100
7.
Minnesota Farm Guide: March 27, 2013 Seed/plant science associations
release Guide to Seed Treatment Stewardship
http://www.minnesotafarmguide.com/news/crop/seed-plant-science-associations-releaseguide-to-seed-treatment-stewardship/article 573d21e8-96b9-11e2-84610019bb2963f4.html
8.
Southeast Far m Press: March 27, 2013 New seed treatment guide helps
farmers, others http://southeastfarmpress.com/grains/new-seed-treatment-guide-helpsfarmers-others
9.
CropLife Magazine: March 25, 2013 - CropLife America, ASTA Release Seed
Stewardship Guide http://www.croplife.com/article/33532/croplife-america-astarelease-seed-stewardship-guide
10.
Hoosier Ag Today: March 25, 2013 - New Seed Treatment Stewardship Guide
Available http://www.hoosieragtoday.com/index.php/2013/03/25/new-seed-treatmentstewardship-guide-available/
11.
Farm Futures: March 26, 2013 - New Guide Aggregates Seed Treatment
Research, Safety Info http://farmfutures.com/story-new-guide-aggregates-seedtreatment-research-safety-info-13-96491
12.
AgWired: March 6, 2013 - ASTA Seed Treatment Guide
http://agwired.com/2013/03/06/asta-seed-treatment-guide/
13.
KTIC (Rural Radio):
http://kticradio.com/news/agricultural/index.php?more=qj2tc6ns
14.
Brownfield: March 25, 2013 The Guide to Seed Treatment Stewardship
website launched http://brownfieldagnews.com/2013/03/25/the-guide-to-seed-treatmentstewardship-website-launched/
15.
American Ag Radio Network: March 26, 2013 Seed treatment guide developed
to assist farmers http://americanagnetwork.com/2013/03/seed-treatment-guidedeveloped-to-assist-farmers/
16.
AgProfessional: March 21, 2013 ASTA, CLA's seed treatment stewardship
website to launch http://www.agprofessional.com/news/ASTA-CLAs-seed-treatmentstewardship-website-to-launch-199210611.html
17.
The Crop Site: March 26, 2013 Promoting Safe Use of Seed Treatments
http://www.thecropsite.com/news/13314/promoting-safe-use-of-seed-treatments
18.
SeedWorld: ISF World Seed Congress Issue May 2013- Future of Seed
Treatments in Europe and North America
19.
Iowa Seed Association News Release: July 2, 2013-Deal with Leftover Seed
Properly
http://iowaseed.org/2011/07/05/treat-leftover-treated-seed-properly/
20.
High Plains Journal July 2013- Manage treated seed effectively
21.
Syngenta Magazine Thrive August 2013- To be titled Q&A on Seed Treatment

Stewardship
Syngenta briefed their Sales Leadership Team in March 2013 on the Seed
Treatment Stewardship Guide and website as a resource to utilize with
customers. In addition an email communication regarding the Guide was sent to
all US sales representatives which included a prepared message about the Guide
to be forwarded to their customers.
Since the release of the Guide to Seed Treatment Stewardship DuPont Pioneer
has referenced the guide to internal and external audiences. Efforts to date
include:
- A Seed Treatment Stewardship Statement that references the ASTA Guide,
posted on Pioneer.com.
- Utilized Ready Rep to communicate with DuPont Pioneer Sales Reps
referencing the ASTA stewardship Guide - Count ~2,500
- Utilized Pro Grower to communicate with farmers referencing the ASTA
Stewardship Guide - Count ~7,500
- Released internal Seed Treatment Stewardship talking points with reference to
ASTA Stewardship Guide.
- E-mail sent to non-customer facing employees on issue with reference to ASTA
Stewardship Guide - Count ~3,000.
- Talking points referencing ASTA Stewardship Guide has been shared
internationally via international communications contacts.
At Oliver Manufacturing, each of the management, sales and engineering staff

was assigned the task of reading The Guide to better understand how their
products development fits into being the right solution for handling wet seed
safely and effectively in a seed processing or condition facility. More information
was posted on their website www.olivermanufacturing.com as well as on
YouTube.
Phase II: Crop-Specific Outreach

August 2013 June 2014
Goal:
Focusing initially on the corn producing industry, create a template for a comprehensive seed
treatment stewardship communication and education campaign that can be customized for other
crops.
Strategy:
Educate corn growers about the importance of and best practices for seed treatment stewardship
through outreach to seed and seed-related companies, grower associations, agriculture advisors
and agencies, the media and direct communication.
Focus on the top 10 corn growing states:
Illinois
Kansas
Iowa
Minnesota
Indiana
South Dakota
Nebraska
Ohio
Missouri
Wisconsin
Timeline/Points of Contact:
The following are key opportunities throughout the year when national, regional and local entities
are in contact with corn growers and can share information about seed treatment stewardship.
Autumn (Harvesting) Seed companies > in advance of sales presentations
Winter (Seed Ordering) -- Grower groups > at national and state grower meetings;
agriculture agencies and advisors > during education/recertification classes
Spring (Planting) -- Seed companies > during seed delivery/pick-up; media > leading up
to planting
Summer (Growing) -- Direct communications via online content and social media; seed
companies > at field days and extension grow out programs
Tactics:
In advance of the opportunities above, the following communications and educational support
will be provided to help companies, grower groups and associations, agencies and the media
reach corn growers.
1) Seed and seed-related companies (growers, treaters, distributors, retailers, equipment
manufacturers)
a. Seed sales season (Nov-Jan): presentation and meetings at ASTAs Corn &
Sorghum Seed Research Conference; collateral materials for extension field days
b. Seed deliveries/pick-ups (Feb-April): collateral materials (handouts, posters, etc.)
2) National, regional and state grower associations (corn grower associations, state farm
bureaus, AFBF, etc.)
a. Fall launch and spring planting: content for member communications vehicles
(newsletters, web content, etc.), webinars
b. Winter state grower meetings: presentations (video, handouts)
3) Agriculture advisors and agencies (state pesticide safety coordinators, certified crop
advisors, extension agents)
a. Dec-April: Curriculum materials for training and recertification classes (video,
presentations, content)
b. Online content for agency websites
4) Agricultural media
a. Seed sales season (Nov-Jan.): Publicity campaign launch at National Association
of Farm Broadcasting Trade Talk (Nov.)
b. Planting season (April): Publicity campaign launch at Commodity Classic (Feb)
and AFBF (Jan)
5) Direct communication
a. Corn-specific website content (video, FAQs, articles, etc.) with search engine
optimization and marketing campaigns
b. Mobile app
c. Social media
From:
To:
Cc:
Subject:
Date:
Attachments:
Bartuska, Ann - OSEC

Kunickis, Sheryl; MacMillan, Anne - OSEC; Harden, Krysta - OSEC; McFarland, Lilia - OSEC;
"lilia.mcfarland2@usda.gov"; Woteki, Catherine - OSEC; Ramaswamy, Sonny; Knipling, Edward; Rexroad, Caird
Epstein, David; Pettis, Jeff; Hackett, Kevin
Re: CONFIDENTIAL: EPA action on labels to address bees
Wednesday, August 14, 2013 6:51:42 PM
image001.jpg
Are you working with Comms on messages?

Sent: Wednesday, August 14, 2013 08:47 PM Coordinated Universal Time
To: MacMillan, Anne - OSEC; Harden, Krysta - OSEC; McFarland, Lilia - OSEC; McFarland, Lilia (OSEC)
<lilia.mcfarland2@usda.gov>; Woteki, Catherine - OSEC; Bartuska, Ann - OSEC; Ramaswamy, Sonny;
Knipling, Edward; Rexroad, Caird
Cc: Epstein, David; Pettis, Jeff; Hackett, Kevin
Subject: CONFIDENTIAL: EPA action on labels to address bees
(b) (5)
(b) (6)
The four products are neonicotinoids thiamethoxam,

clothianidin, dinotefuran, and imidachloprid. A splash will hit the EPA website by noon tomorrow
and registrants will be notified by phone. The goal is for registrants to produce the new labels with
the required language within 30 days, so that they are available for the 2014 growing season. The
new language will have a graphic indicating a pollinator hazard, it will communicate information and
provide a heightened sense of awareness, include contact information in case of an issue, and
provide info on BMPs. It will address crops that use pollinator services, crops that are attractive to
bees, and non-ag sites.
These pesticides are high benefit pesticides for the agricultural community. The hope is this
action will slow/stop the banning of these products by States.
FYI USDA scientists reviewed and commented on the draft label language.
Please let me know if there are questions.

Sheryl

Director
(202) 720-5375 Office

(b) (6)
Cell
made to notify beekeepers no less than 48-hours prior to the time of

the planned application so that the bees can be removed, covered or
otherwise protected prior to spraying.
Non-Agricultural Products:
Do not apply [insert name of product] while bees are foraging. Do not
apply [insert name of product] to plants that are flowering. Only apply after
all flower petals have fallen off.
Yancey, Constance - OCIO

Sent:
To:
Subject:
Thursday, December 09, 2010 5:27 PM

'Teung.F.Chin@aphis.usda.gov'; Coble, Harold; 'dtrogers3@hotmail.com'; Smith, Kent;
Herzi, Dhol
Clothianidin- neonic
This message has been archived. View the original item

Good meeting w/ Steve today. Who has the above-referenced insecticide? Much going on. Go to
www.beyondpesticides.org/dailynewsblog and see their spin. EPA totally disagrees and refutes their
claims. (b) (5)
More at staff meeting on Monday.
Cheers,
Sheryl
Request for Proposals - February 4, 2013
Pollinator Partnership Corn Dust Research Consortium

Call for Research Proposals Related to
Reducing Honey Bee Exposure to Dust Emitted During
Planting of Treated Corn Seeds
Background
The Pollinator Partnership has formed a Corn Dust Research Consortium (CDRC) to
fund, oversee, and advise on two proposed research projects to further our
understanding of best management practices for mitigating seed treatment exposure to
honey bees during corn planting. The Pollinator Partnership has issued CDRC
invitations to stakeholders from crop protection, seed production, farm equipment, corn
growing, beekeeping, academic, governmental and conservation organizations.
The Corn Dust Research Consortium is seeking research proposals from North
American researchers addressing two specific approaches to the issue.
Research Priorities and Funding
We anticipate funding (from pooled resources of $320,000) proposals that address two
questions: Project 1- Use by Honey Bees of Flowering Resources In and Around
Cornfields, and Project 2 - Efficacy of Seed Lubricant Products.
The Consortium will allocate the funding between the two project questions based on
the proposals received. Proposals will be considered that address either or both
questions. Funds must be used within an eight-month period (March 2013 to November
2013). Focused, targeted projects with a high likelihood of providing tangible results
that can be applied to best management practices for mitigating seed treatment
exposure to honey bees are preferred. Proposals providing valuable extensions of
previously funded projects will be considered. Proposals that involve coordinated
applications between institutions, multiple geographic locations in North America,
replication of or direct analysis of working field conditions and standard planting
equipment are preferred. The projects will be funded for one year, with discussion of
extensions to be considered at the end of the first year (fall of 2013).
Background and Specifics
The Corn Dust Research Consortium has identified two priority areas for funding.
Principal Investigators may apply to address either or both of the proposed projects.
Page 1 of 8
423 Washington St. 5th Fl. San Francisco, CA 94111
Telephone: 415.362.1137 Fax: 415.362.3070
A number of ideas for reducing exposure to planter-emitted dust from treated seeds
have been proposed (please see Issue Overview on page 6). These include:
1) development of seed coatings that reduce the amount of toxic dust abraded
from the seeds,
2) removal of flowering plants in or near fields prior to planting to reduce
the likelihood bees come in contact with seed dust deposits,
3) modification of planting equipment to either limit the amount of dust released
into the air or direct emitted dust toward the ground so that the potential for
off-site drift is reduced,
4) development and use of seed lubricants that reduce the amount of dust
abraded from treated seeds,
5) confining bees to hives on days when nearby fields are planted, and
6) using untreated seeds and managing pests in a different way.
Proposed Research Projects
While there may be a role for all of these mitigation approaches, an immediate need for
research on points 2 and 4 (in bold above) has been identified.
Project 1: Use by Honey Bees of Flowering Resources in and around Cornfields
during Spring Planting and How this Behavior can be Effectively Managed to
Reduce Exposure to Pesticide Dust and Residues.
The first research project is to develop a greater understanding of the use by honey
bees of flowering cover crops and weeds in and around cornfields during spring planting
season and how this is influenced by vegetation management practices.
The ultimate goal is to develop recommendations for best management practices that
growers can follow in order to minimize exposure of forager honey bees to seed dust
while maintaining as much forage for honey bees as possible. This may involve a
trade-off of promoting presence of these flowering plants at some times and locations
and their removal via herbicide applications at other times and locations.
Questions of interest include: Are honey bees mainly attracted to certain kinds of
flowering weeds and cover crops, and if so, which species and at what floral densities?
How important are flowering weeds as a food source to honey bees at the time of year
when corn is planted?
Research methods may include trapping pollen at sentinel hives placed in landscapes
dominated by cornfields to determine the relative use of bees of different kinds of plants,
direct observations of honey bee visits to flowers in and around fields, and surveying
corn growers and fields to determine current vegetation management practices. Some
existing and potential practices, i.e. removal of flowering plants, may adversely affect
native bee communities, an issue not addressed in this RFP.
Page 2 of 8
Telephone: 415.362.1137 Fax: 415.362.3070
Project 2: Efficacy of Seed Lubricant Products

The second research project is to evaluate the effectiveness of a new seed lubricant
product that has been developed by Bayer CropScience. The project proposes
measuring deposition levels of pesticide dust deposited in and around fields when
commercially available neonicotinoid-treated corn seed products are planted using this
new product in comparison to standard lubricants (talc and graphite). Such
measurements should be made with a range of planter types and be replicated in
several corn-growing regions (e.g., several major corn-growing states or provinces).
As the time frame of this study is short and the planting season is rapidly approaching,
BCS or Syngenta field personnel can aid in locating and signing up cooperating corn
growers; however, to the extent practicable, Principal Investigators are encouraged to
use independently solicited contacts. BCS will provide free of charge to study personnel
the new seed lubricant product as well as technical support for its use.
Each cooperating grower would plant two fields with the same planter, seed type and
seed treatment. On one field the standard lubricant (talc or graphite) for the planter type
would be used, while the new BCS lubricant product would be used on the other field.
Lubricants should be added to and mixed with the pesticide-treated seeds in the planter
hopper per label directions and after mixing, a sample of the seeds should be collected
for possible later laboratory analysis of release levels of dust and active ingredient using
a Heubach dustmeter. Study personnel will establish sampling locations and devices
prior to planting and measure the amount of pesticide active ingredient in dust
deposited at sampling stations in and around the field. Stations should be located
within and at prescribed distances downwind from each test field.
At each station, samples should be collected at various heights above ground. The
order in which the two lubricant types are used and the fields to which they are applied
should be determined randomly, and the pneumatic system of the planter should be
cleaned of any leftover lubricant powder and seed debris before each of the fields is
planted.
Collected samples will be analyzed to determine the amount of active ingredient
deposited on sampling devices per unit area (i.e., the measurement needs to be able to
be converted to g a.i./m2). Evaluations of each planter and seed treatment type should
be replicated at least three times in each region studied.
Geographic Scope
The intent is to evaluate factors that can reduce honey bee exposure to corn seed dust
in the US Midwest and in the main corn growing areas of Canada. Ideally, field
investigations should be replicated in multiple locations in these regions.
Page 3 of 8
Telephone: 415.362.1137 Fax: 415.362.3070
Quality Assurance
The research does not need to be conducted in strict compliance with Good Laboratory
Practice requirements, but should be conducted in accordance with the spirit of GLP
requirements which include preparation of a written study protocol and standard
operating procedures for data collection prior to study initiation, recording and
maintenance of raw data, and documentation of any deviations from the protocol or
SOPs that occurred.
The goal is to produce peer-reviewed published papers to advance the understanding of
the issue broadly and transparently. We encourage budgets to provide for
photographic/videographic capture of the study as it is being conducted as a means to
demonstrate the methods and to communicate results to wide-ranging audiences, from
practical advice for producers and beekeepers, to economic analysis for agribusiness,
to reproducible science for the research community, and to general interest for the
broader public.
Research Constraints and Reporting
So that results are representative of real-world corn planting scenarios, field work
should be conducted mainly during the spring corn planting season (April-May).
In addition to conclusions and analysis, a copy of original datasets will be made
available for researchers to use in the future. Reports from both projects are needed by
end of November 2013 in order to be incorporated into recommendations
communicated to beekeepers and corn growers for the 2014 planting season. Such
recommendations may need to be provisional pending additional research during the
2014 and 2015 planting seasons.
Project Oversight
The Corn Dust Research Consortium has been formed to review proposals and oversee
the project execution, including review and comment on study protocols, draft reports
and presentation materials prior to their execution and public release. Final decisions
on technical interpretation of the study findings and content of study reports,
publications and presentations will be made by study personnel. The role of the Corn
Dust Research Consortium on these matters will be advisory only. The Corn Dust
Research Consortium intends to include at least one representative from each primary
sponsoring organization (industry, beekeeping, academia, government, and
conservation). The CDRC will also seek input from regulatory agencies, including the
US Environmental Protection Agency (EPA) and the Canadian Pest Management
Regulatory Agency (PMRA).
Proposal Requirements
1) Cover page including:
a. Project or projects the proposal will address (Project 1, Project 2 or both.)
b. Contact information including email(s), physical mailing address, and
telephone number(s).
2) A 4-page (maximum) project description for each project proposal being
submitted with sufficient background and description of methods to ascertain the
Page 4 of 8
Telephone: 415.362.1137 Fax: 415.362.3070
importance and feasibility of the studies. Please use Arial, 12-pt font, single
spaced, with page numbers. References are not included in this page limit. If the
proposal combines the two projects, the limit would be 8 pages.
3) Detailed budget that includes funds for the Principal Investigator and a research
timeline by month (approximately March 2013 to November 2013).
4) 2-page CV of the principal investigator(s).
5) Please include funding details if the proposal is under consideration by other
funding organizations.
Submission
Email your proposal packet as a single PDF file to Jennifer Tsang (jt@pollinator.org) by
3PM PDT on Friday, March 1, 2013.
Please identify the email subject line and the PDF attachment using Project (1 and/or
2), PI Last Name, First Name.
Funding Decisions
The proposals will be evaluated by members of the Corn Dust Research Consortium
Advisory panel, and funding decisions will be made by Friday, March 15, 2013.
Page 5 of 8
Telephone: 415.362.1137 Fax: 415.362.3070
Issue Overview
Seeds of several major crops, such as corn and soybeans, are frequently sold with a
pesticide coating that protects germinating and seedling plants from a variety of pests
and diseases. These seed dressings provide early-season control of plant diseases
and pests and help ensure that farmers receive a good return on their investment when
they purchase high-yield varieties of hybrid seeds.
Putting the chemical on the seed in many cases eliminates the need for early-season
foliar pesticide spraying, and significantly reduces the loading of agrochemicals to
cropland and the potential for contamination of adjacent land and water. While seed
coatings are used to keep pesticide treatments adhered to the seed, mechanical
abrasion (i.e., seeds rubbing against metal surfaces and each other) inside planters
causes some of the chemical treatment to come off the seeds in the form of fine dust
particles.
Seed lubricant powders such as talc and graphite that are commonly added to facilitate
an even flow of seeds through the planter will increase the total amount of dust inside
the planter. Modern pneumatic planters, which use air pressure to precisely deliver
seeds to the seed furrow, may exhaust this dust into the air, and the emitted particles
may in turn be carried some distance downwind.
Bees may potentially contact seed dust particles when the planter-emitted dust is
airborne (i.e., if bees fly through the exhaust plume of a planter), or after deposition on
vegetation or other surfaces. Previous studies in Europe have produced conflicting data
regarding the relative importance of these two exposure scenarios. Studies in Germany
(Pistorius et al. 2009) and in Italy (Sgolastra et al. 2012) identified dust deposition on
flowers as the important route of toxic exposure of honey bees to corn seed dust. Other
studies in Italy (Marzaro et al. 2011; Giorolami et al. 2012; Tapparo et al. 2012) found
that toxic effects did not generally occur from bees visiting dusted flowers, but
sometimes occurred when bees flew through the airborne emissions of a pneumatic
corn planter. The opportunity for a significant number of forager bees from a hive to fly
through planter exhaust plumes would appear to be limited in actual practice because
the planting machinery is in constant motion, and there is no reason to suspect that
bees would preferentially fly through this airspace as they were trained to do in the
experiments conducted by the Italian research team.
Greater potential for exposure of bees seems likely from dust particles deposited on
flowers that may be present along the perimeter of fields or even within the fields
themselves in some cases (e.g., no-till fields containing flowering weeds or a cover
crop). Dust particles on flowers may be available to visiting bees for a period of days
over a broad area inside and downwind of planted fields. When bees visit these
flowers, the particles may become attached to their body hairs and be transported back
to the hive in the same way that natural pollen grains are. Whether such exposures
result in adverse effects is probably a function of (1) the chemical load of the dust
deposits, (2) the intrinsic toxicity of the chemical, (3) the frequency that forager bees
Page 6 of 8
Telephone: 415.362.1137 Fax: 415.362.3070
visit dusted flowers and (4) the degree to which dust particles act like pollen grains in
their size, electrostatic activity, etc.
That this exposure scenario could be of sufficient magnitude to cause toxic effects was
demonstrated by a large bee kill incident in 2008 in southern Germany that was caused
by a combination of poor adherence of a neonicotinoid insecticide treatment to corn
seeds and the close proximity of corn fields being planted to blooming, bee-attractive
crops such as oil-seed rape (Pistorius et al. 2009). Follow-up research (Georgiadis et
al. 2012) identified threshold levels for toxic effects on honey bees for the insecticide
involved when it is applied as a dust to bee-attractive flowers inside bee tunnels.
There are several differences between agricultural practices in North America and
Europe that may influence exposure to bees to dust of treated seeds. In the U.S., seed
lubricant powders such as talc and graphite are frequently added to corn seeds to
improve consistency of planting.
A previous study by Krupke et al. (2012), partially funded by a P2 sponsored North
American Pollinator Protection Campaign (NAPPC) Honey Bee Health Task Force
grant, showed that these lubricant powders become contaminated with abraded
particles from the treated seeds and suggested that emissions of these materials either
during planting or during cleaning of pneumatic equipment pose a hazard to bees. This
has triggered the development of a new seed lubricant product designed to lower such
emissions that will be available in the 2013 planting season for field testing.
Another difference is the prevalence of no-till or minimum-tillage practices in the U.S. In
such fields, flowering weeds such as dandelions and wild mustard may be present
during planting not only in the non-cultivated land around the field, but also in the field
itself. Similarly, US growers sometimes plant corn into fields containing a cover crop
such as clover that is attractive to bees.
The extent to which bee-attractive flowering plants are present in and around fields at
the time of planting may be an important factor influencing the likelihood that forager
bees will be exposed to planter-emitted dust. This further suggests that these
exposures might be reduced by application of burn-down herbicides prior to planting.
However, up until planting time these plants may provide a benefit to farmers (e.g., by
replenishing soil nutrients, decreasing soil erosion, etc.) as well as to bees and other
animals. A better understanding of the abundance of flowering weeds in and around
corn fields at planting time, their use by honey bees, and resulting honey bee exposure
levels to seed treatment dust is needed to develop optimal recommendations for corn
growers.
Page 7 of 8
Telephone: 415.362.1137 Fax: 415.362.3070
Literature Cited
Giorgiadus P-T, Pistorius J, and Heimbach U. 2012. Manual application of insecticidal

dust in semi-field trials: effects on honey bees (Apismellifera L.). Abstract only.
EurBee 5 Scientific Program www.eurbee.com.
Girolami V, Marzaro M, Vivan L, Mazzon L, Greatti M., Giorio C, Marton D, and Tapparo
A. 2012. Fatal powdering of bees in flight with particulates of neonicotinoids seed
coating and humidity implication. J. Appl. Entomol. doi: 10.1111/j.14390418.2011.01648.x.
Krupke CH, Hunt GJ, Eitzer B, Andino G, and Krispn G. 2012. Multiple routes of
pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7(1):
e29268. doi.10.1371/journal.pone.0029268.
Marzaro M, Vivan L, Targa A, Mazzon L, Mori N, Greatti M, Toffolo EP, Di Bernardo A,
Giorio C, Marton D, Tapparo A, Girolami V. 2011. Lethal aerial powdering of honey
bees with neonicotinoids from fragments of maize seed coat. Bull. Insectol. 64, 118
125.
Pistorius J, Bischoff G, Heimbach U, Sthler M. 2009. Bee poisoning incidents in
Germany in spring 2008 caused by abrasion of active substance from treated seeds
during sowing of maize. Julius Khn Archives 423:118-126.
Sgolastra F., Renzi, T et al. (2012) Effects of neonocotinoid dust from maize seed
dressing on honey bees. Bulletin of Insectology 65 (2):273-280.
Tapparo A, Marton D, Giorio C, Zanella A, Solda L, Marzaro M, Vivan L, and Girolami V.
2012. Assessment of the Environmental Exposure of Honeybees to Particulate
Matter Containing Neonicotinoid Insecticides Coming from Corn Coated Seeds.
Environmental Science and Technology.doi. 0.1021/es2035152.
Page 8 of 8
Telephone: 415.362.1137 Fax: 415.362.3070

Subject: RE: Urgent comments re neonicotinoid label changes
Like I said, (b) (5)

To: Epstein, David
Subject: Fw: Urgent comments re neonicotinoid label changes
See below.

To: rmcallister@croplifeamerica.org; Jeff Case <JCase@croplifeamerica.org>; Kellie Bray <kbray@croplifeamerica.org>; Ed Ruckert
<eruckert@mwe.com>; Gabrielle Ludwig <gludwig@almondboard.com>; Chin, Teung; Kunickis, Sheryl
Cc: Joe Bischoff <jbischoff@anla.org>
Subject: FW: Urgent comments re neonicotinoid label changes
We have sent the attached comments and our earlier "Grower Alert" to EPA.

To: 'Laws.meredith@epa.gov'
Cc: 'Bradbury.steven@epa.gov'; 'rossi.lois@epa.gov'
Subject: Urgent comments re neonicotinoid label changes
Dear Ms. Laws:
Because of the great importance of neonicotinoids to the greenhouse, nursery and landscaping industries in the U.S., we are
submitting the comments of the Society of American Florists and the American Nursery & Landscape Association, representing
those industries, to you as you consider changes to the pollinator language of the neonicotinoid labels. As noted in the letter,
we are also attaching a copy of a recent pesticide stewardship "Grower Alert" that our organizations sent to growers across the
U.S. in the wake of the tragic Oregon bee kill. I will send a paper copy of the attachments by mail, but wanted to be sure that
you have this letter as quickly as possible.
We hope you will consider our comments as you make your decision. We would appreciate the opportunity to meet with EPA,
and would be happy to bring along scientists who have been instrumental in some of the important efforts noted in the letter.
Thank you very much for your careful approach to this very important issue. Please feel free to call us should you have
questions or wish further information.
Lin Schmale
Senior Director - Government Relations
Society of American Florists
1601 Duke Street
Alexandria, VA 22314
(703) 838-5232
cell: (b) (6)
LSchmale@safnow.org
file:///H|/...14-F/Kunickis/RE%20Neonic%20Labeling_files/RE%20Urgent%20comments%20re%20neonicotinoid%20label%20changes.htm[7/16/2014 1:06:23 PM]
Joseph Bischoff, PhD

Director of Government Relations
American Nursery & LandscapeAssociation
1200 G St. NW, Suite 800 Washington,DC 20005
(202) 434-8686 direct;
(b) (6)
cell
JBischoff@anla.org
file:///H|/...14-F/Kunickis/RE%20Neonic%20Labeling_files/RE%20Urgent%20comments%20re%20neonicotinoid%20label%20changes.htm[7/16/2014 1:06:23 PM]

Sent: Friday, June 21, 2013 2:26 PM
To: 'Bradbury.Steven@epa.gov'
Subject: Re: NGO letter to Obama on neonics
Thanks. I am in a retina doctors office. Let's talk Monday if ok.
From: Bradbury, Steven [mailto:Bradbury.Steven@epa.gov]

Sent: Friday, June 21, 2013 01:39 PM
Subject: Fw: NGO letter to Obama on neonics
Sheryl. - just got this. The letter focus on epa should suspend neonics like the EU. There is reference to the oct 2012 conference
report, and the proceedings are dismissed as non peer reviewed and involved non scientists (which of course included bee
keepers). (b) (5)
(b) (5)
From: Fehrenbach, Margie

Sent: Friday, June 21, 2013 1:11:48 PM
To: Bradbury, Steven; Jordan, William; Keigwin, Richard; Brady, Donald; Pease, Anita; Moriarty, Thomas; Steeger, Thomas;
McNally, Robert; Overstreet, Anne; Sisco, Deborah; Strauss, Linda; Sterling, Sherry
Subject: NGO letter to Obama on neonics
Not sure if you have seen this yet - Jim Aidala sent me a copy.
file:///H|/2014-OCIO-01714-F/Kunickis/RE%20Neonic%20Labeling_files/Re%20NGO%20letter%20to%20Obama%20on%20neonics htm[7/16/2014 1:06:06 PM]

Sent: Thursday, September 06, 2012 4:20 PM
To: Chin, Teung; Epstein, David; Rogers, Ted; Coble, Harold; Fajardo, Julius - ARS
Subject: RE: Neonicotinoid Insecticides, Clothianidin and Thiamethoxam - Endangered Species Risk
Assessment - Three Environmental/Public Interest Groups have " ... filed a Sixty-Day Notice letter
with EPA announcing their intent to jointly sue EPA for ...
We are one weird bunch we are!
From: Chin, Teung

To: Epstein, David; Kunickis, Sheryl; Rogers, Ted; Coble, Harold; Fajardo, Julius - ARS
Subject: RE: Neonicotinoid Insecticides, Clothianidin and Thiamethoxam - Endangered Species Risk Assessment - Three
Environmental/Public Interest Groups have " ... filed a Sixty-Day Notice letter with EPA announcing their intent to jointly sue EPA for
...
David has all the fun!

To: Kunickis, Sheryl; Chin, Teung; Rogers, Ted; Coble, Harold; Fajardo, Julius - ARS
Subject: FW: Neonicotinoid Insecticides, Clothianidin and Thiamethoxam - Endangered Species Risk Assessment - Three
...
And the fun continues
From: FIEN, LLC - Jack Cooper [mailto:JLC@fien.com]

To: JLC@fien.com
Subject: Neonicotinoid Insecticides, Clothianidin and Thiamethoxam - Endangered Species Risk Assessment - Three
...
Neonicotinoid Insecticides, Clothianidin and Thiamethoxam - Endangered Species Risk Assessment

- The Environmental/Public Interest Groups, Center for Food Safety, Beyond Pesticides and the
Sierra Club have " ... filed a Sixty-Day Notice letter with EPA announcing their intent to jointly sue the
agency for Endangered Species Act (ESA) violations ..." - According to the groups, EPA has failed "
... to ensure, through consultation with the U.S. Fish and Wildlife Service, that its numerous product
approvals for the neonicotinoid insecticides clothianidin and thiamethoxam are not likely to
jeopardize any Federally-listed threatened or endangered species ... The Notice of Intent to Sue
follows a legal petition previously filed by several environmental organizations and more than two
dozen beekeepers demanding that EPA immediately suspend use of the chemical clothianidin that
poses fatal harm to pollinators. While refusing to issue an immediate suspension, the EPA agreed to
open a public comment docket to review additional points raised in the legal petition ... The SixtyDay Notice cites several violations of the ESA, all of which address EPA actions that have enabled
clothianidin and thiamethoxam to be applied over a vast amount of U.S. farmland and in, or near, a
wide range of critical habitats and ecosystems. If the ESA violations are not resolved within 60 days,
the letter signers may then sue EPA ..."
Document Title: The title of the September 6, 2012 Center for Food Safety News Release is "Environmental, Public
Interest Groups Ready for Legal Action Over EPA Approval of Wildlife Endangering Chemicals; Longstanding
file:///H|/2014-OCIO-01714-F/Kunickis/RE%20Neonic%20Labeling_files/RE%20Neonicotinoid%20InsecticNeonics.htm[7/16/2014 1:05:52 PM]
violation of Endangered Species Act provisions highlights Sixty-Day Notice filing"

Organization: Center for Food Safety, Beyond Pesticides and the Sierra Club
Source: September 6, 2012 Center for Food Safety News Release
Web site: The September 6, 2012 Center for Food Safety News Release is posted at
http://www.centerforfoodsafety.org/2012/09/06/environmental-public-interest-groups-ready-for-legal-action-over-epaapproval-of-wildlife-endangering-chemicals/
Contact: none at this time
Summary: The text of the September 6, 2012 Center for Food Safety News Release follows
Washington, D.C. September 6, 2012
Today, the Center for Food Safety, Beyond Pesticides and the Sierra Club, along with affected citizens from around the
country, filed a Sixty-Day Notice letter with the Environmental Protection Agency (EPA) announcing their intent to
jointly sue the agency for Endangered Species Act (ESA) violations. The planned lawsuit highlights EPAs continuing
failure to ensure, through consultation with the U.S. Fish and Wildlife Service, that its numerous product approvals for
the neonicotinoid insecticides clothianidin and thiamethoxam are not likely to jeopardize any Federally-listed
threatened or endangered species.
EPA has failed to uphold the clear standards of the Endangered Species Act, said Peter Jenkins, attorney at the
Center for Food Safety. By continuing to ignore the growing number of reports and studies demonstrating the risks of
neonicotinoids to honey bees and a large number of already threatened and endangered species, the EPA is exposing
these already compromised populations to potentially irreversible harm.
The Notice of Intent to Sue follows a legal petition previously filed by several environmental organizations and more
than two dozen beekeepers demanding that EPA immediately suspend use of the chemical clothianidin that poses fatal
harm to pollinators. While refusing to issue an immediate suspension, the EPA agreed to open a public comment
docket to review additional points raised in the legal petition.
EPAs failure to follow the law potentially poses a direct, long-term threat to the sustainability of fragile ecosystems,
said Jay Feldman, executive director of Beyond Pesticides. Given the known hazards of clothianidin and all
neonicotinoid pesticides, EPAs lack of respect for known scientific evidence and existing regulations endangers
environments essential to our well-being.
In the nine years since the EPA conditionally registered clothianidin for use on corn and canola, the agency has
admitted to both the hazards of the insecticide and the need for compliance with ESA. The EPA fact sheet on
clothianidin reads as follows:
Clothianidin is expected to present acute and/or chronic toxicity risk to endangered/threatened birds and mammals via
possible ingestion of treated corn and canola seeds. Endangered/threatened non-target insects may be impacted via
residue laden pollen and nectar. The potential use sites cover the entire U.S. because corn is grown in almost all U.S.
states.
The agency has also made the same admission regarding thiamethoxam.
Despite EPAs recognition of the acute and chronic toxicity risks to endangered and threatened birds, mammals and
insects from these chemicals nearly a decade ago, the agency has continued to ignore concerns surrounding the effects
on these critical species. Over the past twelve years, EPA has approved a total of 86 products containing clothianidin
and thiamethoxam, and it permits the use of these insecticides on more than 30 crops, as well as ornamental, turfgrass
and structural applications.
The disconnect at EPA between the serious risks these toxic chemicals pose to pollinators and the approval of the
products that contain them is inexcusable, said Laurel Hopwood, Sierra Clubs Genetic Engineering Action Team
chairwoman. One-third of our food supply relies on the presence of pollinators. EPA should be protecting, not
imperiling them.
The Sixty-Day Notice cites several violations of the ESA, all of which address EPA actions that have enabled
clothianidin and thiamethoxam to be applied over a vast amount of U.S. farmland and in, or near, a wide range of
critical habitats and ecosystems. If the ESA violations are not resolved within 60 days, the letter signers may then sue
EPA.
###
About Center for Food Safety - The Center for Food Safety is a national, non-profit, membership organization founded
in 1997 to protect human health and the environment by curbing the use of harmful food production technologies and
by promoting organic and other forms of sustainable agriculture. More information can be found at
www.centerforfoodsafety.org
About Beyond Pesticides - Beyond Pesticides, founded in 1981, works with allies in protecting public health and the
environment by identifying the hazards of chemical-intensive land, building and community management practices and
promoting healthy, sustainable and organic systems. More information can be found at www.beyondpesticides.org
About The Sierra Club - The Sierra Club, the countrys largest grassroots conservation organization, seeks to practice
and promote the responsible use of the earths ecosystems and resources. More information can be found at
www.sierraclub.org/biotech/
Prepared by: This message was distributed by Jack Cooper, who may be reached at e-mail: jlc@fien.com or 301384-8287
This article (#22980) was distributed by e-mail on September 6, 2012 to those whose names are on the FIEN, LLC
Subject Matter Distribution Lists for Crop Protection; Endangered Species; Non Governmental Organization Actions;
Risk Assessment and Communication
end
This information was sent to you by Jack Cooper of the Food Industry Environmental Network, LLC --http://www.fien.com --- 33 Falling Creek Court, Silver Spring, Maryland 20904 --- Cell Phone: (b) (6)
--- EMail: JLC@fien.com
* Messages prefaced by [SFM] are Shortened FIEN Messages, similar to those that would be sent through Twitter.
* The Searchable Index of Previously Distributed FIEN Messages is available at
http://www.fien.com/login/logins.php?RELOAD=/search_article.php
From: Keigwin, Richard [Keigwin.Richard@epa.gov]

Sent: Friday, August 09, 2013 5:23 PM
Subject: Re: Neonic Labeling
In response to your comment, Meredith Laws yes the answer to your question is (b) (5)
From: Keigwin, Richard
Sent: Friday, August 09, 2013 2:03:57 PM
To: Dr. David Epstein; Dr. Sheryl Kunickis
Subject: Re: Neonic Labeling
Thanks! I'll send your comment to RD. Thank you for looking at this so quickly.
From: Epstein, David <David.Epstein@ARS.USDA.GOV>
Sent: Friday, August 09, 2013 1:47:00 PM
To: Keigwin, Richard; Kunickis, Sheryl
Subject: RE: Neonic Labeling
Rick,
One comment on the Directions for Use doc:
2. FOR FOOD CROPS AND COMMERCIALLY GROWN ORNAMENTALS NOT UNDER

CONTRACT FOR POLLINATION SERVICES BUT ARE ATTRACTIVE TO POLLINATORS
Do not apply this product while bees are foraging. Do not apply this product until
flowering is complete and all petals have fallen unless one of the following conditions
is met:
The application is made to the target site when temperatures are below 55F[d1]

Sent: Friday, August 09, 2013 10:44 AM
Subject: Fw: Neonic Labeling
Here is some draft labeling that will be shared with the registrants later today. We are seeking reactions by COB Monday.
From: Laws, Meredith
Sent: Friday, August 09, 2013 9:28:02 AM
Cc: Rossi, Lois
Subject: Neonic "Final" Labeling
Hi Rick: Here are the 2 documents that are the final neonic labeling.
file:///H|/2014-OCIO-01714-F/Kunickis/RE%20Neonic%20Labeling_files/Re%20Neonic%20Labeling.htm[7/16/2014 1:05:30 PM]
Meredith
[d1]Does this allow for early morning application when temperatures are expected to go above 55 shortly following application?
recipients. Any unauthorized interception of this message or the use or disclosure of the information it
contains may violate the law and subject the violator to civil or criminal penalties. If you believe you
have received this message in error, please notify the sender and delete the email immediately.
file:///H|/2014-OCIO-01714-F/Kunickis/RE%20Neonic%20Labeling_files/Re%20Neonic%20Labeling.htm[7/16/2014 1:05:30 PM]

Sent: Monday, July 29, 2013 7:31 AM
To: Draper, Martin; Holy, Doug - NRCS, Rosslyn, VA; Purcell, Mary - ARS; Epstein, David; Purcell,
Mary
Subject: RE: Meeting with the American Seed Trade Association on July 29th
This is a note to remind everyone of the meeting today with the AMTA, CLA, etc with EPA today.
Thanks,
Sheryl

Sent: Thursday, July 18, 2013 3:48 PM
Cc: Draper, Martin; Holy, Doug - NRCS, Rosslyn, VA; Epstein, David; Purcell, Mary - ARS; Purcell, Mary
Thanks Sheryl. We will meet at OPPs offices at 2777 Crystal Drive, Arlington, VA. Room 9100-South. When you clear security,
please call 703-308-8000 to request an escort to the meeting. Please tell the person that answers that you have a meeting with
me. If you have difficulties, please call my cell: (b) (6)
.
For those of you who are not able to participate in person, here is the call-in information:
Call-in number: 1-866-299-3188

Conference code: 703-308-8200
If anyone has any questions, please do not hesitate to get in touch with me.
From: Kunickis, Sheryl [mailto:Sheryl.Kunickis@ARS.USDA.GOV]

Sent: Thursday, July 18, 2013 1:30 PM
Cc: Draper, Martin; Holy, Doug - NRCS, Rosslyn, VA; Epstein, David; Purcell, Mary - ARS; Purcell, Mary; Kunickis, Sheryl
Rick,
USDA appreciates the invitation to participate in the meeting with ASTA and EPA on July 29 at 2 p.m. Confirmed participants
are:
Doug Holy, NRCS
Dave Epstein, OPMP
Marti Draper, NIFA
Mary Purcell, NIFA/ARS
I may join if my schedule permits. I have ccd the USDA delegation on this message. Could you provide your physical address
for those that have not been to your offices? Also, could a call in number be available for Mary as she is in Beltsville?
Thanks,
Sheryl

Director
file:///H|/...20Labeling_files/RE%20Meeting%20with%20the%20American%20Seed%20Trade%20Association%20on%20July%2029th htm[7/16/2014 1:05:17 PM]

(202) 720-5375 Office

(b) (6)
Cell
This electronic message contains information generated by the USDA solely for the intended recipients. Any
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notify the sender and delete the email immediately.
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file:///H|/...20Labeling_files/RE%20Meeting%20with%20the%20American%20Seed%20Trade%20Association%20on%20July%2029th htm[7/16/2014 1:05:17 PM]

Sent: Wednesday, August 07, 2013 7:26 AM
Subject: RE: Letter to Bradbury on neonics
OK

To: Epstein, David
Subject: Re: Letter to Bradbury on neonics
Catch up on all activities- agency updates-get everyone on the same page. Seems like new things are happening and not
everyone knows....

I am available. To what purpose(s)?

To: Epstein, David
I am thinking - should convene the entire bee group on Tues. Thoughts?

Next Wednesday.

To: Epstein, David
Ok. Good meeting! (b) (5)
When do you leave for Penn 4tate?

Good morning, Sheryl,
(b) (5)
My back condition has improved from yesterday, but I am still unable to stand or sit for more than a few minutes at a time. I
file:///H|/2014-OCIO-01714-F/Kunickis/RE%20Neonic%20Labeling_files/RE%20Letter%20to%20Bradbury%20on%20neonics htm[7/16/2014 1:05:01 PM]
think it best that I use a sick day for today, and, hopefully, will be able to come in to the office, tomorrow.
David

Sent: Tuesday, August 06, 2013 2:24 PM
To: Epstein, David
Subject: Fw: Letter to Bradbury on neonics
FYI

Subject: Letter to Bradbury on neonics
Sheryl:
Attached is the letter that Jay Vroom has sent to numerous commodity groups regarding the situation with neonic insecticides.
Attached to the letter is the one Steve Bradbury has sent to the neonic registrants that I mentioned earlier today. Please feel
free to share it with your staff.

CropLife America
202-872-3874 (office)
7 (cell)
(b) (6)
ray@croplife.us
This e-mail message may contain privileged and/or confidential information, and is intended to be received only by persons entitled to receive such information. If you
have received this e-mail in error, please notify the sender immediately. Please delete it and all attachments from any servers, hard drives or any other media. Other use
of this e-mail by you is strictly prohibited.
All e-mails and attachments sent and received are subject to monitoring, reading and archival by CropLife America and RISE. The recipient of this e-mail is solely
respons ble for checking for the presence of "Viruses" or other "Malware". CropLife America and RISE accepts no liability for any damage caused by any such code
transmitted by or accompanying this e-mail or any attachment.
file:///H|/2014-OCIO-01714-F/Kunickis/RE%20Neonic%20Labeling_files/RE%20Letter%20to%20Bradbury%20on%20neonics htm[7/16/2014 1:05:01 PM]

To: Caraher, Kai - APHIS
Subject: RE: Fwd: EU commission decision on neonicotinoids
Please share with others.

EU Proposal to Restrict the Use of 3 Neonicotinoids (Clothianidin, Imidacloprid and Thiametoxam), effective December 1, 2013 and
Intended to Reduce Risk to Bee Health, Did Not Reach a Qualified Majority among the Member States - By a vote of 15 to 8 for the
proposal with 4 Member States abstaining, the proposal would have restricted the use of these insecticides for "... seed treatment, soil
application (granules) and foliar treatment on bee attractive plants and cereals ... [with] exceptions ... limited to the possibility to treat
bee-attractive crops in greenhouses, in open-air fields only after flowering ... In absence of an agreement between Member States, it is
now for the [European] Commission to decide on the adoption of the proposed restriction ..." - The Commission's action is a "...
response to the European Food Safety Authority's (EFSA) [January 16, 2013] scientific report which identified 'high acute risks' for
bees as regards exposure to dust in several crops such as maize, cereals and sunflower, to residue in pollen and nectar in crops like
oilseed rape and sunflower and to guttation in maize ..."
Document Title: The title of the April 29, 2013 European Commission Press Release is "Bees & Pesticides: Commission to proceed with plan
to better protect bees"
Organization: Press Office of the European Commission (EC)
Summary: The text of the April 29, 2013 EC Press Release follows:
Today, EU Member States did not reach a qualified majority either in favour or against - in the Appeal Committee1 which discussed a
Commission proposal to restrict the use of 3 neonicotinoid insecticides.
Tonio Borg, Health and Consumer Commissioner, said: "Although a majority of Member States now supports our proposal, the necessary
qualified majority was not reached. The decision now lies with the Commission. Since our proposal is based on a number of risks to bee health
identified by the European Food Safety Authority, the Commission will go ahead with its text in the coming weeks." To conclude: "I pledge to do
my utmost to ensure that our bees, which are so vital to our ecosystem and contribute over 22 billion annually to European agriculture, are
protected."
15 Member States supported the restriction, 8 Member States voted against and 4 Member States abstained during the appeal committee vote.
Main elements of the proposal
The proposal restricts the use of 3 neonicotinoids (clothianidin, imidacloprid and thiametoxam) for seed treatment, soil application (granules) and
foliar treatment on bee attractive plants and cereals.
In addition, the remaining authorised uses are available only to professionals.
Exceptions will be limited to the possibility to treat bee-attractive crops in greenhouses, in open-air fields only after flowering.
The restrictions will apply from 1 December 2013.
As soon as new information is available, and at the latest within 2 years, the Commission will review the conditions of approval of the 3
neonicotinoids to take into account relevant scientific and technical developments.
Next steps
In absence of an agreement between Member States, it is now for the Commission to decide on the adoption of the proposed restriction.
Background
Following the request of the European Commission, the European Food Safety Authority (EFSA) published, on 16 January, its scientific findings
on the risks associated with the use of three pesticides, belonging to the neonicotinoid family, on bee health. On the basis of this opinion, the
Commission tabled a proposal for discussion with Member States.
Experts representing the EU-27 met in the Standing Committee on the Food Chain and Animal Health on 15 March and failed to reach a
qualified majority - either in favour or against the proposal to restrict the use of three neonicotinoid. 13 Member States supported the
restriction, 9 Member States voted against and 5 Member States abstained. The proposal was then referred to the appeal committee on 29
April.
file:///H|/...714-F/Kunickis/RE%20Neonic%20Labeling_files/RE%20Fwd%20EU%20commission%20decision%20on%20neonicotinoids htm[7/16/2014 1:04:42 PM]
For more information:

http://ec.europa.eu/food/animal/liveanimals/bees/neonicotinoids en.htm
EFSA's website:
http://www.efsa.europa.eu/en/topics/topic/beehealth.htm?wtrl=01
Follow us on Twitter: EU_Health
http://twitter.com/EU Health
Source: April 29, 2013 European Commission Press Release
Web site: The April 29, 2013 EC Press Release is posted at
http://europa.eu/rapid/press-release IP-13-379 en.htm?locale=en
Additional information about the proposal to protect bees in the EU is available at
http://ec.europa.eu/food/animal/liveanimals/bees/neonicotinoids en.htm
The January 16, 2013 EFSA Press Release, titled "EFSA identifies risks to bees from neonicotinoids", is posted at
http://www.efsa.europa.eu/en/press/news/130116.htm
The January 16, 2013 EFSA "Conclusion on the peer review of the pesticide risk assessment for bees for the active substance clothianidin" is
posted at
http://www.efsa.europa.eu/en/efsajournal/pub/3066.htm
The January 16, 2013 EFSA "Conclusion on the peer review of the pesticide risk assessment for bees for the active substance imidacloprid" is
posted at
The January 16, 2013 EFSA "Conclusion on the peer review of the pesticide risk assessment for bees for the active substance thiamethoxam" is
posted at
The previous FIEN message related to this topic is posted at
http://www.fien.com/articleDisplay.php?id=24299
Contact: The contacts listed in the EC Press Release are as follows:
* Frdric Vincent at +32 2 298 71 66; e-mail: Frederic.Vincent@EC.EUROPA.EU
* Aikaterini Apostola at +32 2 298 76 24; e-mail: Aikaterini.Apostola@EC.EUROPA.EU
* Tonio Borg is the EC Commissioner for Health and Consumer Policy and may be reached by e-mail at CAB-BorgWebPage@EC.EUROPA.EU
Prepared by: This message was distributed by Jimmy Liu, who may be reached at e-mail: liu@fien.com or 240-476-5958
From: Caraher, Kai - APHIS

Subject: Fw: Fwd: EU commission decision on neonicotinoids
From: O'Toole, Susan J - APHIS

To: Rose, Robyn I - APHIS; Baca, Robert M - APHIS; Caraher, Kai - APHIS
Subject: Fwd: EU commission decision on neonicotinoids
Sent from my iPhone
Begin forwarded message:

From: "Parra, Gregory R - APHIS" <Greg.R.Parra@aphis.usda.gov>
Date: April 29, 2013, 10:02:38 AM EDT
To: "Hollingsworth, Charla R - APHIS" <Charla.Hollingsworth@aphis.usda.gov>, "Bulluck, Russ - APHIS"
<Russ.Bulluck@aphis.usda.gov>
Cc: "Lewis, Phillip A - APHIS" <Phillip.A.Lewis@aphis.usda.gov>, "Mastro, Victor C - APHIS"
<Vic.Mastro@aphis.usda.gov>, "Lance, David R - APHIS" <David.R.Lance@aphis.usda.gov>, "Ciomperlik, Matthew
A - APHIS" <Matt.A.Ciomperlik@aphis.usda.gov>, "Bartels, David - APHIS" <David.W.Bartels@aphis.usda.gov>,
"Simmons, Gregory S - APHIS" <Gregory.S.Simmons@aphis.usda.gov>, "Braswell, Evan - APHIS"
<Evan.Braswell@aphis.usda.gov>, "O'Toole, Susan J - APHIS" <Susan.J.O'Toole@aphis.usda.gov>
Subject: EU commission decision on neonicotinoids
From the most recent vote of the EU Commission after consideration by an appeals committee, it
appears that there will be a two year restriction on three neonicotinoids; clothianidin, imidacloprid, and
thiametoxam.
The use of the neonicotinoids will be restricted to crops not attractive to bees and other
pollinators
The sale and use of seeds treated with neonicotinoids will be prohibited
The moratorium is to begin no later than July 1, 2013 (current goal by Commission)
All member countries of the EU must comply with the restriction
Gregory R. Parra
National Program Staff Scientist
Arthropod Pests
Center for Plant Health, Science and Technology
USDA, APHIS, PPQ
1730 Varsity Drive, Suite 400
Raleigh, NC 27606
office: 919-855-7548
mobile: (b) (6)
fax: 919-855-7480
http://www.aphis.usda.gov/plant health/cphst/index.shtml

Sent: Thursday, March 28, 2013 9:37 AM
To: Rasmussen, Mark FAS; Mikulski, Neil FAS; Francom, Michael (FAS)
Cc: Wagner, Elisa (FAS); Epstein, David
Subject: RE: Additional information on neonicotinoids - URGENT and CONFIDENTAL; ECPA information
Good Morning,
The USDA Office of Pest Management Policy is providing leadership on bee issues and we are glad to assist in any way we can.
Dr. David Epstein, entomologist, is fully engaged on the issues surrounding the neonicotinoids. Please let us know if we can
provide assistance/expertise on pesticides/etc. We also work closely with CLA and EPA on these issues.
Thanks,
Sheryl Kunickis

Director
(202) 720-5375 Office

(b) (6)
Cell

Sent: Wednesday, March 27, 2013 6:11 PM
To: Rasmussen, Mark FAS; Mikulski, Neil FAS; Francom, Michael (FAS)
Cc: Wagner, Elisa (FAS); Kunickis, Sheryl; Barbara Glenn
Subject: FW: Additional information on neonicotinoids - URGENT and CONFIDENTAL; ECPA information
Importance: High
TO: Mark Rasmussen, Neil Mikulski, Michael Francom; USDA/FAS

Daniella Taveau, EPA
Cc: Elisa Wagner; Sheryl Kunickis
FROM: Ray S. McAllister, PhD

CropLife America
202-872-3874 (office)
(cell)
(b) (6)
ray@croplife.us
this is the third and final message, with information from the European Crop Protection Association on the neonicotinoids. If you
did not receive all three messages, please let me know.
file:///H|/...tional%20information%20on%20neonicotinoids%20-%20URGENT%20and%20CONFIDENTAL,%20ECPA%20information htm[7/16/2014 1:04:12 PM]
From: Ray McAllister

To: Jane_Doherty@ustr.eop.gov
Cc: Barbara Glenn
Subject: Additional information on neonicotinoids - URGENT and CONFIDENTAL
Importance: High
Jane:
This follows up on the message that Barb Glenn sent you over the weekend. After this message, I will forward one more with
additional information provided by Bayer CropScience. We understand that Bayer may have already provided the information
we are sending to you, to the folks at EPA who are working on the comments for the SPS Committee.
Our colleagues in the European Crop Protection Association (ECPA) have shared with us the following attached documents that
provide useful background and technical details on the neonicotinoid situation in Europe. (b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)

CropLife America
202-872-3874 (office)
7 (cell)
(b) (6)
ray@croplife.us
file:///H|/...tional%20information%20on%20neonicotinoids%20-%20URGENT%20and%20CONFIDENTAL,%20ECPA%20information htm[7/16/2014 1:04:12 PM]
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
(b) (5)
July 30, 2013

Col. Edgar W. Duskin
Executive Vice President
Southern Crop Protection Association
PO Box 686
Dawson, GA 31742
Dear Ed,
I write to you with a sense of urgency today to address an issue that has been on the forefront of the
crop protection industry and has recently gained renewed attention with the introduction of new
legislation and increased media coverage: the health of pollinating insects and their intersection with
U.S. agriculture. Extremist NGOs and some legislators are working relentlessly to severely restrict or
even completely stop the use of neonicotinoid insecticides, which they allege are negatively impacting
honeybee health. We would like to discuss this outreach with you in more detail, but I wanted to make
you aware of the gravity of this situation without delay. Areas for engagement include:
1) Sign onto a letter to President Obama, responding the NGO letter (described below);
2) Request a meeting with EPA senior management to express concerns and insist that sound science
be followed;
3) Participate in visits to Capitol Hill to discuss the need for crop protection and to emphasize the
stewardship efforts already in place;
4) Support ongoing media outreach; and
5) Push for practical pollinator research from USDA to address the key issues of pollinator health.
We will be reviewing these suggested action items and other ideas at an upcoming CLA-sponsored
Commodity Coffee in August.
Despite research indicating that multiple factors are at work in pollinator health and that the impact of
these few insecticide products is minimal, we continue to hear strong and persistent voices targeted
against crop protection products (some specific, others very general) and the agricultural industry.
A proposed suspension of neonicotinoids found in legislation (H.R. 2692) introduced on July 16, 2013
by Rep. John Conyers (D-MI) and co-sponsored by Reps. Blumenauer (D-OR) and Clay (D-MO) would
have sweeping consequences for farmers across the country and for the crop protection industry. Not
only would such a move change the face of agriculture in the U.S. by severely hampering productivity,
but it would negatively impact competitiveness of U.S. agriculture in international markets. We need
only look at the neonicotinoid restrictions that are being imposed in Europe to understand what this
kind of outcome could do to our economy and agricultural livelihood. In Europe, and increasingly here,
the talk is trending to attack other insecticides beyond the neonicotinoids.
The terrible incident in Oregon, where an apparently improper application of an insecticide on
ornamental trees resulted in a significant bumblebee kill, is also a reminder of how seemingly innocent
accidents exacerbate this issue.
Representing the Crop Protection Industry

1156 15th St. N.W., Suite 400 Washington, D.C. 20005 202.296.1585 phone 202.463.0474 fax
Last week, published research by USDA and the University of Maryland alleged negative effects of
pesticides on honeybees, while ignoring positive results, opposing results and dismissing statistical
realities. That paper attributes a very weak increase in bee disease to presence of fungicide residues in
pollen, while ignoring their own results showing that most pesticide residues were associated with a
decreased presence of the disease pathogen.
In a July 22 letter (copy attached) to crop protection registrants of neonicotinoid products, the U.S. EPA
makes significant demands, including proposed changes in labeling targeted for the 2014 growing
season. These labeling changes could have a significant impact on various uses of these products. We
are seeking clarifications / improvements from EPA in the approach to the questions in this letter. If
nothing else, the letter is another affirmation of the political pressure our government is facing on
pollinator health. We encourage you to make your voices heard on the feasibility and effects on your
members of these proposals as they are developed.
The increasingly shrill and brazen voices in the public debate continue to blame crop protection
products entirely for the woes of bees, while trampling and ignoring the overwhelming scientific
evidence to the contrary. Some of those voices have called on President Obama by letter to abandon
U.S. sovereignty over regulatory decisions based on science in this matter, and blindly follow a
misguided European path. When honeybee colonies appear to suffer, it is easy to blame pesticides,
because the evidence is made murky and investigation is inconsistent or entirely lacking. Inexplicably,
there exists no robust program to investigate, determine, and enforce compliance with validated Best
Management Practices in beekeeping that would quantify the real, top causes of poor bee health:
rampant parasite infestations in the hives, serious bee disease problems, overworking of some bees,
monolithic bee genetics, and difficulties with nutrition of the bees.
I urge you to join CLA and our members as we tackle this issue on all fronts by collaborating with
regulatory agencies, beekeepers, scientists and a large network of stakeholders to pursue science-based
strategies for improving pollinator health; by educating consumers on the vital role of pollinators in
agriculture; and by remaining engaged on this key issue that stands to impact all of U.S. agriculture.
Stewardship of crop protection chemicals is always a top priority now is an important time to remind
all pesticide users to carefully read and follow label directions.
Our combined efforts are necessary in order to implement solutions based on science rather than
unfounded fear, and help further American agriculture. Neonicotinoids are vital tools for Americas
farms, forests, and ornamental plants. They are crucial to protection from invasive insect pests, while
reducing potential risks to the environment. The need is urgent. Our voices need to be heard in the
halls of Congress and the Federal agencies, and in the media, at least as loud and often as the naysayers.
Delayed or inadequate defense of this technology will open the path for similar attacks on other
essential crop protection tools, threatening the very success that has made our agricultural economy the
envy of the world.
Sincerely,
Jay Vroom
President & CEO
attachment
Representing the Crop Protection Industry

1156 15th St. N.W., Suite 400 Washington, D.C. 20005 202.296.1585 phone 202.463.0474 fax

To: Epstein, David
Subject: Fw: Letter to Bradbury on neonics and CLA's response
Attachments: Letter to SCPA.PDF
Don't share. See the what I know part.

Sent: Wednesday, August 07, 2013 06:00 PM
To: MacMillan, Anne - OSEC; Harden, Krysta - OSEC; Palmieri, Suzanne - OSEC
Subject: Fw: Letter to Bradbury on neonics and CLA's response
Thought you'd want to see the attached letters if you haven't already as they are getting attention. (b) (5)
(b) (5)
Let me know if you hear anything!

Sheryl

Subject: Letter to Bradbury on neonics
Sheryl:
Attached is the letter that Jay Vroom has sent to numerous commodity groups regarding the situation with neonic insecticides.
Attached to the letter is the one Steve Bradbury has sent to the neonic registrants that I mentioned earlier today. Please feel
free to share it with your staff.

CropLife America
202-872-3874 (office)
(cell)
(b) (6)
ray@croplife.us
file:///H|/...ickis/RE%20Neonic%20Labeling_files/Fw%20Letter%20to%20Bradbury%20on%20neonics%20and%20CLA's%20response htm[7/16/2014 1:03:12 PM]
From: janis.mcfarland@syngenta.com
Sent: Friday, August 09, 2013 4:11 PM
To: Kunickis, Sheryl; Epstein, David; Chin, Teung; Harold.D.Coble@usda.gov
Cc: john.abbott@syngenta.com; dan.campbell@syngenta.com
Subject: FW: Letter from Lois Rossi Concerning Neonic Labeling + "Final" Labeling
Attachments: Letter from Lois Rossi on Neonic Labeling.pdf; Pollinator Protection Box Final.docx; DIRECTIONS FOR
USE Final.docx
Importance: High
Hi all, FYI-please see attached message sent to Syngenta earlier today. We are working on our feedback on any needed
clarifications and questions. We look forward to progressing the harmonization of label language as well as to continued
progress in stewardship and education. Hope you all are having a great August-We will keep you posted on our work in this
area. Best regards-Janis
From: Laws, Meredith [mailto:Laws.Meredith@epa.gov]
Sent: Friday, August 09, 2013 9:56 AM
To: Clive Halder; julie.schlekau@valent.com; Abbott John USGR; Levey Charles USGR; Lsorenson@landisintl.com
Subject: Letter from Lois Rossi Concerning Neonic Labeling + "Final" Labeling
Good Morning:
Please find attached a letter from Lois that references the final labeling we have developed to enhance pollinator protection
on the neonicotinoid products. This labeling is intended to be placed on liquid formulations that are applied as foliar
applications.
As I mentioned in my phone calls and is also stated in the letter, we need any thoughts you have by COB Monday.
Thanks very much everyone, have a nice weekend.
Meredith
Meredith Laws
(703) 308-7038
This message may contain confidential information. If you are not the designated recipient, please notify the sender immediately, and delete the original and any copies.
Any use of the message by you is prohibited.
file:///H|/...abeling_files/FW%20Letter%20from%20Lois%20Rossi%20Concerning%20Neonic%20Labeling%20+%20Final%20Labeling htm[7/16/2014 1:02:39 PM]
February 4, 2013
For Immediate Release
Tom Van Arsdall tva@pollinator.org t 703.509.4746
Laurie Davies Adams LDA@pollinator.org t 415.362.1137
Corn Dust Research Consortium Formed to Address

Honey Bee Questions
Unique Stakeholder Consortium Sponsors
Research to Reduce Honey Bee Exposure to Corn Planting Dust
San Francisco, California The non-profit Pollinator Partnership (P2) today announced the formation of
the Corn Dust Research Consortium (CDRC), a multi-stakeholder initiative they are coordinating to invest
research dollars in reducing honey bee exposure to dust emitted during planting of treated corn seeds.
Pollinator Partnership is coordinating the Corn Dust Research Consortium and has invited stakeholders from
crop protection, seed production, farm equipment, corn growing, beekeeping, academic, governmental, and
conservation organizations to fund and oversee two proposed research projects to better understand ideas
for mitigating risks to honey bees from exposure to planter-emitted dust during corn planting.
It is truly rare to see this kind of large-scale collaboration between disparate stakeholders each of whom
shares equally in the supervision of the project, said Executive Director Laurie Davies Adams, emphasizing
her organizations enthusiasm for the consortium approach to problem solving. Public-private partnerships
that seek practical solutions for cooperative conservation and commerce represent an improved model.
Industry participants are to be commended for providing major funding while sharing responsibility and
authority with all CDRC partners.
Seed lubricant powders such as talc and graphite that are commonly added to facilitate an even flow of
seeds through the planter can increase the total amount of dust inside the planter. Modern pneumatic
planters, which use air pressure to deliver seeds precisely to the seed furrow, may exhaust this dust into the
air, and the emitted particles may in turn be carried some distance downwind. Honey bees may potentially
contact seed dust particles when the planter-emitted dust is airborne (i.e., if bees fly through the exhaust
plume of a planter), or after deposition on vegetation or other surfaces.
Greater potential for exposure of honey bees seems likely for dust particles deposited on flowers that may
be present along the perimeter of fields or even within the fields themselves in some cases (e.g., no-till fields
containing flowering weeds or a cover crop). Dust particles on flowers may be available to visiting honey
bees for a period of days over a broad area inside and downwind of planted fields. When honey bees visit
these flowers, the particles may become attached to their body hairs and transported back to the hive in the
same way that natural pollen grains are transported. Whether such exposures result in adverse effects is
probably a function of (1) the chemical load of the dust deposits, (2) the intrinsic toxicity of the chemical, (3)
the frequency that forager honey bees visit dusted flowers and (4) the degree to which dust particles act like
pollen grains in their size, electrostatic activity, etc.
While the CDRC has identified a number of mitigation options, an immediate need for research is focusing
on two projects being funded by CDRC.
Page 1 of 2
Telephone: 415.362.1137 Fax: 415.362.3070
The first research project is to develop a greater understanding of the use by bees of flowering cover crops
and weeds in and around cornfields during spring planting season and how this is influenced by vegetation
management practices. The ultimate goal is to develop recommendations for best management practices
that growers can follow in order to minimize exposure of forager honey bees to seed dust while maintaining
as much forage for honey bees as possible. Native bee communities may also be affected by exposure
through forage, an issue not addressed in this research.
The second research project is to evaluate the effectiveness of a new seed lubricant product by measuring
deposition levels of pesticide dust in and around fields when commercially available neonicotinoid-treated
corn seed products are planted using this new product in comparison to standard lubricants (talc and
graphite). The product, developed by Bayer CropScience, has already had some field research in other
countries, but none in North America.
The CDRC has taken the following steps: (1) Invited stakeholders from disparate perspectives to contribute
funding and share equally in the oversight responsibility; and (2) Ensured that final decisions on technical
interpretation of the study findings and content of study reports, publications and presentations will be made
by researchers. The research will be conducted in multiple locations during the 2013 corn seed planting
season.
Stakeholders in this consortium are putting aside any preconceived bias, added Dr. David Inouye, a CDRC
member representative. I cannot think of any other instance in North America where this kind of
cooperative venture has been attempted we are working in an open and collaborative manner to bring
sound science to best practice recommendations where corn planting and honey bee health interface.
The complete RFP is attached as a separate document. The research proposals are due Friday,
March 1. The CDRC will evaluate the proposals. Funding decisions will be made by Friday, March 15.
ABOUT POLLINATOR PARTNERSHIP
Established in 1997, the Pollinator Partnership (P2) is the largest 501(c) 3 non-profit organization dedicated
exclusively to the health, protection, and conservation of all pollinating animals. For further information, visit
www.pollinator.org.
Page 2 of 2
Telephone: 415.362.1137 Fax: 415.362.3070
FW: I wanted to be sure you saw this
From: Nowierski, Robert

Sent: Wednesday, October 30, 2013 1:44 PM
To: Purcell, Mary; Schmoldt, Daniel; Bewick, Thomas A; Kunickis, Sheryl; Draper, Martin; Bolton,
Herbert T; Hedberg, Robert; Ramaswamy, Sonny; Fitzner, Michael; Peet, Mary; Sheely,
Deborah; Kunickis, Sheryl
Subject: Briefing on Pollinator health for John Holdren; Corn dust; neonicotinoid insecticides
Attachments: CornDust_2013_PressRelease_V9 FINAL.pdf; Request for Proposals V2 FINAL 02 04 13.pdf
Hi Mary!
The North Central Regional Integrated Pest Management Program (NC-RIPM) funded a pollinator project in 2012
entitled QUANTIFYING THE INTERSECTIONS BETWEEN NEONICOTINOID INSECTICIDE USE FOR SEED
TREATMENTS AND FORAGING HONEY BEES
(The CRIS Report for this project can be found at: http://cris.nifa.usda.gov/cgi-bin/starfinder/0?
path=fastlink1.txt&id=anon&pass=&search=R=54285&format=WEBLINK). According to Sue Ratcliffe, Director of the
North Central IPM Center, this was one of the initial projects that led to the grant program described in the second
attachment.
Thanks and Best Regards,
Bob
Robert M. Nowierski, Ph.D.
National Program Leader for
Bio-Based Pest Management
USDA-National Institute of Food and Agriculture (NIFA)
Washington, DC
***************************************************************************************************
Address:
USDA-NIFA
Room 3322 Waterfront Centre
800 9th Street, SW
Phone: 202-401-4900
FAX: 202-401-1782
rnowierski@nifa.usda.gov
***************************************************************************************************
Investing In Science, Securing Our Future!
www.nifa.usda.gov
file:///H|/.. riefing%20on%20Pollinator%20health%20for%20John%20Holdren,%20Corn%20dust,%20neonicotinoid%20insecticides%20 htm[7/16/2014 12:45:08 PM]
In the face of severely declining bee colonies nationally with beekeepers reporting record
losses this year it would not be responsible to continue to allow these threatening
compounds to be used so broadly. Independent scientists and commercial beekeepers attribute
dramatic bee die-offs to a combination of factors, but exposure to neonicotinoids is a key
contributor. We are asking you as Chief Executive to direct the EPA to follow the EU and EFSA
lead and recognize the risks are unacceptably high. Pollination services provided by honey bees
and the other even less-studied wild bees are far too important for agriculture, gardens and
wild plants to treat them in a non-precautionary manner. Many thousands of beekeeper
livelihoods, and indeed the future viability of commercial beekeeping and the crops relying on
these pollination services, are potentially in jeopardy. Experts have identified the potential for
domino effects of cascading inadequate crop pollination due to shortage of viable pollinators.
This could rapidly evolve into devastating, perhaps irreversible, losses to farmers, consumers
and the economy as a whole, which relies on domestically-produced bee-pollinated food and
fiber crops.
In recent statements about the EUs decision, EPA officials highlighted a recent USDA report,
the Report on the National Stakeholders Conference on Honey Bee Health - National Honey Bee
Health Stakeholder Conference Steering Committee. Unlike the peer-reviewed, scientific EFSA
report, the USDA report was not peer-reviewed; it derived from a meeting of numerous
stakeholders including many non-scientists. It is dated and not comprehensive. Further, there
was not consensus among the stakeholders on the statements in the final report.
We would like to bring your attention to recent acknowledgments of key facts by EPA officials,
made in public statements at recent meetings, in media statements, in EPA documents and
other venues:
They acknowledged EPAs enforcement guidance for neonicotinoid use was inadequate.
They acknowledged EPAs bee kill incident reporting system was inadequate.
They have stated the labels on neonicotinoid products are inadequate to mitigate
adverse environmental effects, specifically to avoid seed dust-mediated mortality to
honey bees and other beneficial insects in or near corn fields.
They recognize the current corn planting machinery poses significant dust-off risks and
needs changing, while also recognizing that such changes will likely take many years and
stating that EPA lacks authority to mandate machinery changes.
They acknowledge that bee health and populations, and crop pollination, are in a nearcrisis state based on several synergistic factors including insecticide use.
They indicated the agency has not consulted with the U.S. Fish and Wildlife Service on
potential effects on threatened or endangered species under Sec. 7 of the Endangered
Species Act for the neonicotinoid insecticides.
Despite the above, EPA has refused to exercise its regulatory power to address the one factor it
could address tomorrow the major contribution of these insecticide to bee declines and
instead has pointed to land use decisions, crop planting choices by farmers, pathogens, bee
nutrition and other factors over which EPA has no authority. Indeed, no other Federal agency
2
has the power to help stem bee declines by addressing any of those synergistic factors within a
reasonable timeframe.
We would like to further highlight a broader threat: water contamination by imidacloprid,
clothianidin, thiamethoxam and the other compounds, the effect of which is to sterilize much
of the invertebrate food chain, threatening insects, fish, amphibians and other taxa, including,
but not limited to, aquatic and insectivorous birds. Recently, the American Bird Conservancy
(ABC) released a report, The Impact of the Nations Most Widely Used Insecticides on Birds,
researched by an internationally-recognized avian toxicologist, Pierre Mineau, who examined
the key EPA risk assessment documents and found numerous failures in the agencys approvals.
The report showed high direct and indirect mortality risks to a broad suite of birds, as well as to
aquatic invertebrates and ecosystems generally. It found that the observed acute threats from
water contamination by EPA-approved neonicotinoids may be totally unprecedented in the
history of pesticide registration. It also stated: EPA has not been heeding the warnings of its
own toxicologists. Dr. Mineau examined the approved product labels and found them
inadequate, stating regulators are clearly mistaken in believing that exposure to treated seed
can be minimized by label statements or adherence to good agricultural practices. The report
describes EPAs analysis as scientifically unsound. It urges the agency to suspend use of these
products and to ban neonicotinoid seed treatments altogether.
The leeway for your Administration to somehow disregard the ABC report was drastically
reduced by the peer-reviewed publication in PLOS ONE on May 1 of this year of a major Dutch
study, Macro-Invertebrate Decline in Surface Water Polluted with Imidacloprid. This multi-year,
comprehensive, field study states (emphasis added):
While a large amount of evidence exists from laboratory single species and
mesocosm experiments, our study is the first large scale research based on
multiple years of actual field monitoring data that shows that neonicotinoid
insecticide pollution occurring in surface water has a strong negative effect on
aquatic invertebrate life, with potentially far-reaching consequences for the
food chain and ecosystem functions.
In short, we could face a second Silent Spring above and beyond the threats to managed and
wild pollinators. Unfortunately, EPAs planned deadline of completing its Registration Reviews
for the major neonicotinoids by 2018 is far too slow in view of their potentially calamitous risks.
We trust you do not want to preside over this pending crisis. Directing EPA to follow the EUs
lead would be a first step but even more protective measures are needed, including a minimum
two-year suspension for all outdoor uses of neonicotinoid insecticides pending resolution of
their risks.
Thank you for your consideration of this urgent appeal. We look forward to your response.*
Sincerely,
George H. Fenwick
American Bird Conservancy
Jay Feldman
Beyond Pesticides
Patty Clary
Californians for Alternatives to Toxics
Michael Green
Center for Environmental Health
Andrew Kimbrell
Jamie Rappaport Clark

Defenders of Wildlife
Wenonah Hauter
Food & Water Watch
Erich Pica
Friends of the Earth
Kim Leval
Northwest Coalition for Alternatives to Pesticides
Judy Hatcher
Pesticide Action Network North America
Michael Brune
Sierra Club
Scott Hoffman Black

The Xerces Society
CC:
Tom Vilsack, Secretary of Agriculture

Sally Jewell, Secretary of the Interior
Nancy Sutley, Chair, Council on Environmental Quality
Bob Perciasepe, Acting Administrator, EPA
*To reply to the signers please contact: Ms. Larissa Walker, Policy & Campaign Coordinator
Center for Food Safety, 660 Pennsylvania Ave. SE, Suite 302, Washington, DC 20003
email: lwalker@centerforfoodsafety.org; tel: 202.547.9359; fax: 202.547.9429

Responsive Document: CREW: Department of Agriculture: Regarding Pesticides: 8/1/2014

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Control Number: 7112161

Control Number: 7112161

COLONY COLLAPSE DISORDER

CCD Steering Committee

CCD Steering Committee Members

USDA Agricultural Research Service (co-chair)

Colony Collapse Disorder (CCD)

Topic IV: Mitigation and Management Preventive Measures

APPENDIX: Accomplishments by Action Plan Component

Topic I: Survey and Sample Data Collection

Topic II: Analysis of Existing Samples

Gene-expression Analyses Using Candidate Immune- and Stress-response Genes. Gene

Funding: USDA-ARS and USDA-NIFA.

Goal 2: Confirm or eliminate potential pathogens as contributing causes of CCD.

Goal 3: Confirm or eliminate pests as contributing causes of CCD.

Topic IV: Mitigation and Management Preventive Measures

Controlling the Key Parasite Varroa destructor Through Application of Genomics. A

Cryopreservation of Honey Bee Germplasm. In 2010, the Washington State University

The eXtension.org Community of Practice (CoP) continues to disseminate Web-based

Other ongoing Web-related outreach tools include email campaigns, articles in

Funding: USDA-NIFA and USDA-ARS.

Control Number: 7243719

Control Number: 7264659

Control Number: 7428462

Control Number: 7428462

Control Number: 7677581

Control Number: 7754909

Control Number: 7781413

Joe Harman (b) (6)

Ban GE alfalfa. The risk of damage to other crops is too great.

Joe and Evy Harman

Control Number: 7852062

Jamie Rappaport Clark

Scott Hoffman Black

Tom Vilsack, Secretary of Agriculture

Control Number: 7754719

Control Number: 7653931

Control Number: 7653931

Synthesize the current state of knowledge regarding each of the

Bee biology, genetics, and breeding

members of the CCD Steering Committee that participated in the

This is a report presenting the proceedings of a stakeholder conference

Sheryl H. Kunickis, Ph.D.

(202) 720-5375 Office

Johansen, Erik (AGR)

Hi Marylou and Dave,

or you can subscribe or unsubscribe to WSDA News Clips

Dear Ms. Mendicino,

Sheryl H. Kunickis, Ph.D.

(202) 720-5375 Office

Sheryl H. Kunickis, Ph.D.

(202) 720-5375 Office

Bottom line: (b) (5)

From: Jeffrey Gore [mailto:JGore@drec.msstate.edu]

P.O. Box 197

Scott D. Stewart, Professor and IPM Coordinator

Wilde et al. (2007):

Petzold-Maxwell, JL, LJ Meinke, ME Gray, RE Estes, and AJ Gassmann. 2013. Effect of Bt

Johansen, Erik (AGR)

Hi Marylou and David,

or you can subscribe or unsubscribe to WSDA News Clips

BOARD OF COUNTY COMMISSIONERS

Dear Mr. Hover,

Notes on the study of WHITEHORN et al. (2012)