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Review Article

Ecoimmunology and microbial ecology: Contributions to avian behavior,

physiology, and life history
Jessica K. Evans a,b, Katherine L. Buchanan a, Simon C. Grifth b, Kirk C. Klasing c, BriAnne Addison a,
a
School of Life and Environmental Sciences, Deakin University, Waurn Ponds, Geelong 3220, Victoria, Australia
b
Department of Biological Sciences, Macquarie University, 2122, New South Wales, Australia
c
Department of Animal Science, University of California, 1 Shields Avenue, Davis, CA 95616, USA

a r t i c l e i n f o a b s t r a c t

Article history: Bacteria have had a fundamental impact on vertebrate evolution not only by affecting the evolution of the im-
Received 31 August 2016 mune system, but also generating complex interactions with behavior and physiology. Advances in molecular
Revised 29 November 2016 techniques have started to reveal the intricate ways in which bacteria and vertebrates have coevolved. Here,
Accepted 5 December 2016
we focus on birds as an example system for understanding the fundamental impact bacteria have had on the evo-
Available online xxxx
lution of avian immune defenses, behavior, physiology, reproduction and life histories. The avian egg has multiple
Keywords:
characteristics that have evolved to enable effective defense against pathogenic attack. Microbial risk of patho-
Avian genic infection is hypothesized to vary with life stage, with early life risk being maximal at either hatching or
Bacteria edging. For adult birds, microbial infection risk is also proposed to vary with habitat and life stage, with molt
Ecoimmunology inducing a period of increased vulnerability. Bacteria not only play an important role in shaping the immune sys-
Egg tem as well as trade-offs with other physiological systems, but also for determining digestive efciency and nu-
Life history trient uptake. The relevance of avian microbiomes for avian ecology, physiology and behavior is highly topical
Microbiome and will likely impact on our understanding of avian welfare, conservation, captive breeding as well as for our
Migration
understanding of the nature of host-microbe coevolution.
Molt
2016 Elsevier Inc. All rights reserved.
Nestling
Pathogen

Contents

1. Introduction: microbial ecology, immune defense, and co-evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

1.1. Microbial ecology evolution and communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
1.2. Immune defense . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
2. Eggs and embryos . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
3. Nestlings and juveniles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
4. Adult phases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
4.1. Wintering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
4.2. Migration and migratory fuelling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
4.3. Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
4.4. Molt . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
5. Ecological considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
5.1. Microbial biogeography. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
5.2. Foraging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
6. Conclusion: key questions and techniques. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
6.1. What is the structure of microbial communities associated with birds and what are the functional roles of those microbes? . . . . . . . . . 0
6.2. How has co-evolution with microbes shaped metabolism and nutritional niches of birds? . . . . . . . . . . . . . . . . . . . . . . . . . 0
6.3. How have interactions with environmental and enteric microbes shaped life history evolution of birds? . . . . . . . . . . . . . . . . . . 0
Author contributions statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

Corresponding author.
E-mail address: b.addison@deakin.edu.au (B. Addison).

http://dx.doi.org/10.1016/j.yhbeh.2016.12.003
0018-506X/ 2016 Elsevier Inc. All rights reserved.

Please cite this article as: Evans, J.K., et al., Ecoimmunology and microbial ecology: Contributions to avian behavior, physiology, and life history,
Horm. Behav. (2016), http://dx.doi.org/10.1016/j.yhbeh.2016.12.003
2 J.K. Evans et al. / Hormones and Behavior xxx (2016) xxxxxx
1. Introduction: microbial ecology, immune defense, and co-
evolution
Ever since birds rst appeared in the Mesozoic era (Benson et al.,
2014), they have coexisted with microbes, potentially coevolving
with avian ontogeny, behavior, physiology and immune function.
There is even a growing literature to suggest that microbes were in-
strumental in determining early feather coloration and structure
(Carney et al., 2012; Moyer et al., 2014). To put the importance of
microbes into perspective: the microbial community inhabiting the
human gut (1014cells) is estimated to outnumber the somatic and
germ cells of the body (1013cells) (Savage, 1977) and en masse are
thought to exhibit a range of metabolic activity which exceeds that
of the human liver (Berg, 1996). As such, the microbial community
of vertebrates can be envisaged as a signicant biological entity,
with potential capacity to impose signicant selection pressure on
their hosts.
1.1. Microbial ecology evolution and communities
Whilst microbial ecology has been a topical focus for soil and
plant scientists (e.g. Berendsen et al., 2012), only in recent years
have animal biologists recognized the importance of the coevolved
bacterial communities associated with their study organisms (McFall-
Ngai et al., 2013). Such communities remain largely uninvestigated in
birds, except in the context of commercial production (Kogut, 2013;
Mancabelli et al., 2016), with a few notable exceptions which acknowl-
edge the fundamental impact bacteria have had on the digestive
efciency and evolution of some birds species (Roggenbuck et al.,
2014; Waite et al., 2012).
The interactions between microbes and their hosts are potentially
complex and commonly involve mutualism, commensalism and
pathogenesis (Ventura et al., 2009), whilst the nature of the interac-
tion may change according to conditions imposed on either the host
or the microbes (Sorci, 2013). Many members of a commensal
community may take multiple association roles. Some microbes may
be parasitic when considered alone, but may be benecial through the
production of antimicrobials against a more pathogenic microbe (Cash
et al., 2006).
For the purposes of this discussion, microbes include the environ-
mental and commensal Archea and Eubacteria. Archea are generally
found environmentally with a few species associated with verte-
brates (Bang and Schmitz, 2015), whereas Eubacteria are found
both environmentally and commensally on and within vertebrates.
We focus on the literature on avian commensal microora, though
many of the concepts extend to other vertebrates. Some studies of
avian commensal microbes (e.g. Grizard et al., 2014) include consid-
eration of yeasts or other fungi, while others (e.g. Kurzak et al., 1998;
Peralta-Sanchez et al., 2012) limit measurements and manipulations
to a few known enterobacteria. Aerobic culture techniques have been
the primary method for the measurement of microbes associated with
birds, though more recent studies utilize molecular methods to identify
the components of the microbial community (Benskin et al., 2015; Hird
et al., 2015).
Avian commensal Archea include methanogens associated with
plant-eating birds utilizing gut fermentation (Wrede et al., 2012).
There are no known Archea pathogens in vertebrates, though it has
been proposed they should exist (Eckburg et al., 2003). Avian commen-
sal Eubacteria include Actinobacteria (e.g., Micrococcus), Bacteroidetes
(Bacteroides), Firmicutes (Clostridium, Bacillus), Mollicutes (Mycoplas-
ma), and Proteobacteria (Enterobacter, Escherichia) (Lu et al., 2008;
Soler et al., 2011; Su et al., 2014; Waite and Taylor, 2014) and can be
benecial, pathogenic, or have unknown associations. We will consider
microbial risk, focusing on the risk of acquiring a pathogenic microbe or
microbial infection, at different life stages and for different life histories
of birds.
Please cite this article as: Evans, J.K., et al., Ecoimmunology and microbial ecology: Contributions to avian behavior, physiology, and life history,
Horm. Behav. (2016), http://dx.doi.org/10.1016/j.yhbeh.2016.12.003
1.2. Immune defense
In adult birds an integrated immune defence is used to control
microbes, although, age-related immune development is largely
unquantied outside of the chicken (Fellah et al., 2008; Seto, 1981).
Passive antimicrobial molecules, such as lysozyme, complement,
and antimicrobial peptides, act on features of microbes to lyse their
cell walls (Millet et al., 2007). These passive antimicrobial molecules
are found on both the exterior and interior epithelia, interstitial uids,
as well as circulating in blood and deposited in eggs (Juul-Madsen et
al., 2008). These proteins are constitutively secreted by the liver and
the epithelia and their nutritional costs relative to their protective ben-
ets are low in healthy birds (Klasing, 1998), but increase markedly
during the acute phase of the immune response to an invasive pathogen
(Iseri and Klasing, 2014).
The acute phase of the immune response is a key immune defence
mechanism in vertebrates. It involves increased production of pro-
inammatory proteins, eicosanoids and other mediators that initiate a
variety of physiological changes which divert resources to immune
defense, sequester resources away from pathogens, and increase basal
body temperature beyond optimal conditions for pathogens (Gray et al.,
2013). The febrile response includes behavioral changes, such as de-
creased food intake and activity levels, feather pufng and thermogenic
shivering. Concurrent with the febrile response is the deployment of
acute phase proteins, such as mannan-binding protein, lysozyme, and
haptaglobin, which play various roles in the activation of other aspects
of innate immune function or in direct killing of microbes (Juul-Madsen
et al., 2008; Koutsos and Klasing, 2001).
Phagocytic cells include thrombocytes, heterophils and macrophages
(Harmon, 1998; Millet et al., 2007; Qureshi et al., 2000; Toth, 2000;
Wigley, 2013). Heterophils are the avian equivalent of mammalian neu-
trophils (Bogdan, 2001; Genovese et al., 2013). Avian thrombocytes are
functionally similar to mammalian platelets in regard to blood clotting
but they can also phagocytose bacteria and produce an oxidative burst
(Wigley et al., 1999). The recruitment of phagocytes and their conse-
quent activity are primarily responsible for inammation and the associ-
ated oxidative damage (Sorci and Faivre, 2009).
Adaptive immunity is mediated by lymphocytes that mature in
either the bursa of fabricius (B-cells) or the thymus (T-cells). Their re-
sponses are specic to the pathogen and include the production of anti-
bodies (B-cells) and direct killing (cytotoxic T-cells) through the release
of antimicrobial agents. Antigen responding B- and T-cells differentiate
into memory cells, enabling a faster and less inammatory clearance of
pathogens upon repeated exposure (Sharma and Tizard, 1984; Wigley,
2013).
The relative costs of different modes of immune function can poten-
tially be quantied in terms of energy expenditure, nutritional/protein
resources, and the opportunity cost of mounting this defense (Lee,
2006). Measuring the costs of immune defense in wild birds is difcult;
studies measuring immediate costs have focused on trade-offs with
reproductive effort (Ardia, 2005; Bonneaud et al., 2003) or growth
(Mauck et al., 2005). Lee et al. (2005) found costs related to invasion
potential of sparrow congeners. No studies of wild birds have attempted
to measure lifetime costs or immunopathology costs, nor have they
disentangled the mechanistic explanations of immune response costs.
2. Eggs and embryos
Eggs and embryos are associated with microbe communities present
in nests, as well as on the skin, feathers and feces of parents. Birds utilize
a wide variety of different nesting materials including with potentially
distinct microbial communities and some materials may even have
antimicrobial characteristics. Feathers have been proposed to have
antimicrobial characteristics and can prevent or manipulate microbial
colonization (Peralta-Sanchez et al., 2012; Ruiz-Castellano et al., 2016;
Shawkey et al., 2003). Fresh plant material added to nests can provide
 J.K. Evans et al. / Hormones and Behavior xxx (2016) xxxxxx
antimicrobial defense compounds (Gwinner and Berger, 2005;
Mennerat et al., 2009; Mller et al., 2013).
Layered onto this nest microbe community is the microbial commu-
nity introduced from the parents building the nest and antimicrobial se-
cretions of preen oil and saliva (e.g. Martin-Vivaldi et al., 2010).
Microbes are found on the feathers and skin of parents and may also
be introduced through saliva, nasal or eye secretions and fecal matter
(Benskin et al., 2009; Berger et al., 2003; Kyle and Kyle, 1993; Mills et
al., 1999; Singleton and Harper, 1998). The microbe community found
on the shell of eggs presumably represents the balance of microbial in-
puts from the nest, parents, and invaders against the antimicrobial
compounds present in nest material, secreted by parents, and deposited
on the outermost layers of the egg. It is the community on the eggshell
surface with which the embryo must contend. Soler et al. (2011) found
eggshell bacteria load was inversely related to innate immune function
of adults and suggested that innate immune function evolves to alter
the probability of vertical transmission of bacteria.
Much of the research assessing the vulnerability of eggs to bacterial
infection is focused on commercial production within the poultry indus-
try (Berrang et al., 1999). The egg is endowed with a number of antimi-
crobial properties (Adil, 2016). Developing chicks in the egg are
protected from pathogenic bacteria by the egg shell, maternal antibod-
ies, and by numerous peptides and proteins in the egg cuticle, albumen,
and yolk that have antimicrobial properties (Bedrani et al., 2013; Fellah
et al., 2008). The eggshell is a semipermeable membrane, designed to
permit gas exchange for embryonic metabolism. It is well documented
that egg pathogens utilize this vulnerability of eggs (Cook et al., 2003,
2005b). De Reu et al. (2006) found that egg shells were most vulnerable
to gram-negative, motile, non-clustering bacteria, and bacterial
resistance to egg white defense proteins was the most important factor
determining pathogenicity of the bacteria to the egg. Embryo vulnera-
bility to pathogenic microbes rises sharply when the chorioallantoic
membrane fuses with the egg shell membrane to facilitate gas exchange
(Fig. 1). At this early developmental stage, for both precocial and
altricial birds, the embryo has a very immature immune system and
lacks an effective lymphocyte mediated response. It has been suggested
that microbial infection of egg contents and high microbial loads
on eggshells are the primary causes of embryonic death in birds
Microbial Risk
Fig. 1. The relationship between chronological age and important developmental events for specic and non-specic immunity in the chicken with speculated microbial risk throughout
development (adapted from Klasing and Leshchinsky (1999).
Please cite this article as: Evans, J.K., et al., Ecoimmunology and microbial ecology: Contributions to avian behavior, physiology, and life history,
Horm. Behav. (2016), http://dx.doi.org/10.1016/j.yhbeh.2016.12.003
3
(Peralta-Sanchez et al., 2012; Pinowski et al., 1994). Penetration of the
egg, or trans-shell infection, is thought to be determined by the climatic
conditions that dictate microbial growth on the egg shell, microbial nu-
trient availability, as well as the presence of water which facilitates the
transfer of microbes to the interior of the egg (Board and Halls, 1973;
Cook et al., 2005a). Field studies on wild birds have shown that bacterial
contamination is diminished and hatching success improved by
cleaning eggs (Cook et al., 2003), and when humidity is lower (Cook
et al., 2003), and due to the thermal impact of incubation (see below,
Cook et al., 2005a). The importance of cleaning, ambient temperature
and humidity, and control of bacteria during incubation are thought to
be diminished in the temperate zone, compared to the presumably
rich and stable tropical microbial community (Wang et al., 2011).
The eggshell cuticle also plays a role in immune defense. Its thick-
ness and composition varies greatly between species, with those having
hard nest surfaces being thicker than those with soft nest surfaces, and
those nesting in damp environments having thicker cuticles than those
nesting in dry environments (Kusuda et al., 2011). As non-motile mi-
crobes can enter eggs through pores via water in humid environments,
Australian brush-turkeys (Alectura lathami), which incubate their eggs
in humid compost mounds, have specialized pore-blocking calcite
spheres incorporated into egg cuticles (D'Alba et al., 2014). The primary
antimicrobial compounds of egg shell cuticles are ovocleidin, which
binds bacterial polysaccharides (Wellman-Labadie et al., 2008),
ovocalyxin, which inhibits microbial proteases (Wellman-Labadie
et al., 2007), and histones H1 and H2B, which bind microbial DNA and
membrane LPS (Kawasaki and Iwamuro, 2008). The cuticle also
contains defenses normally associated with the egg white, including
lysozyme, which cleaves peptidoglycans on the cell membrane of
gram-positive bacteria, and ovotransferrin, which binds and sequesters
iron to inhibit bacterial growth. Egg white also contains antibodies
(King et al., 2010; Rose et al., 1974) IgA and IgM, and yolk contains
IgY, which opsonize microbes, helping to block their pathogenic activity
and marking them for attack by cellular immune components.
From an evolutionary standpoint, species that are prone to bacterial
infections due to the nature of the incubation period or the environment
would be predicted to have more efcient bacterial defenses. Thermal
effects, likely due to the activation of defense enzymes, appear to
High
Low
4 J.K. Evans et al. / Hormones and Behavior xxx (2016) xxxxxx
inuence microbial load and egg viability (Cook et al., 2005a; Godard
et al., 2007; Javurkova et al., 2014; Lee et al., 2014; Peralta-Sanchez
et al., 2014; Shawkey et al., 2009; Wang et al., 2011). Studies have also
found that intensive incubation decreases bacterial load on eggshells
(Ruiz-de-Castaneda et al., 2012). Incubation of wood duck (Aix sponsa)
eggs showed a decrease in density of up to 87% of eggshell microorgan-
isms (Walls et al., 2012). Incubation initiates non-specic antimicrobial
enzymes inside the albumen of the egg (activated when temperatures
are over 27 C (Wilson, 1991)). It also protects the egg from becoming
damp, reducing trans-shell infection by microbes via water (D'Alba
et al., 2010; Ruiz-De-Castaneda et al., 2011). Antimicrobial chemicals
associated with symbiotic bacteria have been identied in the preen se-
cretions in the European hoopoe (Upupa epops) and green woodhoopoe
(Phoeniculus purpureus) (Martin-Vivaldi et al., 2010). Bacterial and fun-
gal diversity on the eggshell surface have been found to decrease during
the late stages of incubation (Grizard et al., 2014). This may support the
hypothesis that benecial bacteria are promoted during incubation and
pathogenic bacteria are eliminated, although evidence for this is limited
(Shawkey et al., 2009).
In birds, maternal IgY antibodies, developed in response to specic
pathogens, are transferred to the yolk (Bedrani et al., 2013; King et al.,
2010). Maternally derived IgM (Rose et al., 1974) and IgA (King et al.,
2010) are deposited in the albumen. Maternal antibody titre is depen-
dent on the mothers' physiological condition (Ardia et al., 2011) and dif-
fers according to life history (Addison et al., 2009). Although there is
great variation among species of birds, maternal antibodies usually per-
sist in effective concentrations in the hatchling for 514 days, by which
time the nestling will start producing its own antibodies at 1014 days
post-hatch (Grindstaff et al., 2006; Hasselquist and Nilsson, 2009).
Exposure to microorganisms and pathogens during the rst few days
following hatching is important for the development and diversication
of B cells (Addison et al., 2010; Baumgarth et al., 2005). Prior to the de-
velopment of lymphocyte mediated immunity, protection depends on
maternal immunity, phagocytes and protective proteins (Ardia et al.,
2011).
3. Nestlings and juveniles
Bacterial nest densities and assemblages (Berger et al., 2003) are hy-
pothesized to play an important role in determining nestling growth
and development. Siblings share more similar bacterial assemblage
composition than would be expected by chance, demonstrating the po-
tential role of the nest environment in shaping immune development
(Brandl et al., 2014). To understand relationships between nestling im-
mune function and bacteria, it is important to understand how immune
function development maps onto the risk of infection (see Fig. 1).
The potential detrimental effects of bacteria presumably underlie
the well documented phenomenon of nest sanitation, (Ruiz-Castellano
et al., 2016; Soler et al., 2010). Bacterial colonization is assumed to
come from the introduction of food, coprophagy, parent secretions
(e.g. saliva, crop milk), and cloacal drinking of the fecal excretions that
build during the nestling period. Mills et al. (1999) found that levels of
cloacal gram negative enteric fermenter bacteria correlated positively
with degree of wing asymmetry in tree swallow nestlings, suggesting
a negative impact upon edging survival, as wing asymmetry impacts
ying ability. Escherichia coli has been found to be negatively associated
with the growth rate of sparrow nestlings, also causing egg mortality
and nestling death (Pinowski et al., 1994). However, Berger et al.
(2003) found no relationship between the nest bacterial load and star-
ling edging success.
Interest in the importance of avian microbiota in determining
growth, development and tness has grown substantially in recent
years, due to the development of molecular techniques allowing for
the description and quantication of bacterial assemblages (Kohl,
2012). The fundamental links between gut microbiota and digestive ef-
ciency have been repeatedly demonstrated in poultry, both through
Please cite this article as: Evans, J.K., et al., Ecoimmunology and microbial ecology: Contributions to avian behavior, physiology, and life history,
Horm. Behav. (2016), http://dx.doi.org/10.1016/j.yhbeh.2016.12.003
comparisons of growth rates in germ free and conventional chickens
(Forbes and Park, 1959), as well as more recent experiments which
show that selection for digestive efciency affects microbiome composi-
tion (Mignon-Grasteau et al., 2015). An experimental test of the role of
probiotics in wild pied ycatchers (Ficedula hypoleuca), found that cloa-
cal bacteria, and more specically the presence of Enterococcus faecium,
were found to relate positively to tarsus size and mass in nestlings
(Moreno et al., 2003). E. faecium has also been found to be a growth pro-
moting probiotic in chickens (Cao et al., 2013). Bacteriocin production
and antimicrobial peptides produced by E. faecium are thought to de-
stroy potential bacterial pathogens (Audisio et al., 2000; Guillot, 1998;
Moreno et al., 2003). Probiotic effects are thought to be mediated
through a combination of improvements to digestive efciency,
suppression of pathogenic bacteria and regulatory inuences on the
immune system (Walker et al., 2006).
Once edglings and juveniles depart the nest they will be introduced
to microbial communities associated with habitat vegetation and soil,
associations with other vertebrate species, and potentially a broader
prey base. Vulnerability to microbes may be at a peak at this stage
(Fig. 1) feather growth is not always complete, skin on the feet and
face is probably softest, adaptive immunity is immature and maternal
antibodies and parental antimicrobial secretions unavailable. This
post-edging period is extremely difcult to study in wild birds, and
thus virtually nothing is known about the consequences of microbial
risk during this period.
4. Adult phases
Adult microbial exposure is hypothesized to be a function of species'
ecology, behavior and life history strategy which interact to produce
variation in the relative risk of pathogenic microbe exposure (Fig. 2).
Both comparative studies and manipulative experiments that alter the
microbial exposure of birds at various stages of their life history could
reveal the nature of physiological trade-offs that might be relevant in
mediating the cost of bacterial defense. For example, Evans et al.
(2016) found that nest sanitation and bacterial load affected adaptive
immune responses, but not innate responses of adult (but not nestling),
domesticated zebra nches (Taeniopygia guttata). The study also sug-
gested that adult bacterial defense varied with reproductive stage, de-
creasing from incubation to nestling feeding (Evans et al., 2016).
We propose that the variability in microbial risk (the risk of infection
by pathogenic microorganisms) across the entire annual cycle should
depend on the life history strategy employed and habitats utilized. For
example, tropical residents are hypothesized to have a relatively high
but monotonic microbial risk across their annual cycle due to relatively
stable temperatures throughout the year, with small peaks in risk dur-
ing molt events, and variation determined by seasonal variability in
the microbial community. In contrast, migrants and species that are sea-
sonally colonial are hypothesized to experience highly variable microbi-
al risk across their annual cycle. Variability in microbial exposure and
competing life history demands across the annual cycle should select
for plasticity in immune function (Weil et al., 2015). Hegemann et al.
(2012) nd no seasonal modulation of acute phase response in skylarks
(Alauda arvensis), however they sampled a partial migrant species from
a single locality, and so may only have measured the inuence of the
local environment and missed seasonal modulations by individuals uti-
lizing different habitats for breeding or wintering. Many other species
have indeed shown seasonal modulation of acute phase response as
reviewed by Ashley and Wingeld (2011) (but also see Adelman et al.,
2010; Owen-Ashley and Wingeld, 2006, 2007). Benskin et al. (2015)
nd a signicant relationship between fecal microbial diversity and sur-
vival probability to the following year, with additive effects of specic
bacterial species where one identied species had a negative impact
on probability of survival and another had a positive effect on probabil-
ity of survival. In the remainder of this section we suggest hypotheses
 J.K. Evans et al. / Hormones and Behavior xxx (2016) xxxxxx 5

Fig. 2. Hypothesized microbial risk as an individual moves through the different phases of the annual cycle for various life strategies. Temperate regions are considered to have lower
microbial risk than tropical regions, however there is more variance in risk in temperate regions, with the warmer temperatures of the breeding season being associated with
increased microbial risk. Migration periods are presumed to have roughly the same risk as wintering periods for non-migrants. Periods of congregation of conspecics, such as at
migratory stopover sites, breeding colonies, or dense communal roosting would be associated with higher risk due to higher transmission probabilities. Finally molt should be a high-
risk period due to compromised integument, decreased mobility, and increased protein requirements.

for microbial risk at the different life phases of adult birds, and review,
where available, some of the evidence.
4.1. Wintering
During wintering the microbial risk to adult birds is predicted to be
low to moderate depending on the habitat. The temperate resident life
history strategy will generally produce the lowest risk level in the annu-
al cycle. For very wet, unfrozen winter habitats microbial risk may be
more similar to summer (breeding) risk conditions. For species that
use communal roosts in winter, having very high densities of conspe-
cics, we predict the microbial risk will be very high due to high trans-
mission rates between conspecic hosts. Migrants and tropical
residents likely face high microbial risks. However, relative to more
seasonal environments we suspect the microbial community they are
exposed to may be more stable and predictable based on theory of mi-
crobial biogeography (see below). North tropical wintering grounds
(tropical dry season) for example, are habitats that are likely to have a
dip in microbial abundance.
Microbial defense during the non-breeding season should match rel-
ative risk. Species that will encounter the same microbial community
for repeated years, particularly tropical residents, should invest in de-
fense strategies that include functional memory such as B- and T-cell
mediated defense, to the extent that it can be used to defend against a
particular pathogen microbe. Buehler et al. (2009) found that red
knots (Calidris canutus) had higher natural antibodies, a constitutive
(innate) B-cell product, on their lower latitude wintering grounds
than their high latitude breeding grounds, suggesting increased bacteri-
al pathogen pressure during the winter. They also found young, but not
older birds had higher leukocyte counts in low quality wintering habi-
tats, suggesting the younger birds may need to rely on cellular immuni-
ty having not had prior exposure (Buehler et al., 2009). In cold
wintering environments, it has been suggested that the cellular immune
response is costly and must be offset by higher food intake (Barbosa and
Moreno, 2004). It is also important to note the hormonal changes during
winter are thought to redirect energy into immune function to enhance
survival and divert energy away from energetically expensive functions,
such as reproduction. Melatonin release, is known to increase in winter,
and augment some aspects of immune defense (Nelson and Demas,
1996). Other hormone changes during winter include decreases in sex
steroids and prolactin, directing resources away from reproduction
(as reviewed by Martin et al., 2008; Nelson and Demas, 1996).
4.2. Migration and migratory fuelling
For species that migrate, the background microbial risk will depend
on the migratory strategy, but two aspects of migration make this
period a particularly high-risk life phase. First, migrants generally pass
through numerous habitat types, with associate high microbial
diversity. Second, migratory stopover sites have very high densities of
conspecics and potential vectoring heterospecics, making microbial
transmission probabilities very high. As an extension of this, species
with long migratory routes encounter a richer pathogen pool (Dunn
et al., 2010; Guilhaumon et al., 2012; Stephens et al., 2016).
Migration is therefore a time of particularly high microbial exposure
with the further challenge that migration timing is crucial to success
(Bauer and Hoye, 2014). Fueling is prioritized over all other demands
and a migrating individual must balance investment in time spent
mounting immune defenses against the risk of time lost to sickness.
The timeframe of B- and T-cell responses is longer than the timeframe
of the migratory period for many species, and the resources lost to a fe-
brile response would represent a large deviation from a tight fueling
schedule. A model illustrating immune-pathogen interactions in mi-
grants is presented in Buehler et al. (2010a). For adult birds, immune

Please cite this article as: Evans, J.K., et al., Ecoimmunology and microbial ecology: Contributions to avian behavior, physiology, and life history,
Horm. Behav. (2016), http://dx.doi.org/10.1016/j.yhbeh.2016.12.003
6 J.K. Evans et al. / Hormones and Behavior xxx (2016) xxxxxx
defense is proposed to primarily draw from lower cost antibody-
mediated immunity, particularly as they have repeated exposure to
the migratory stopovers throughout their lifetime (Buehler et al.,
2010a). However several constitutive aspects of immunity have been
shown to increase over time at a stopover site (Buehler et al., 2010b),
suggesting that fueling birds may bolster their immune function in re-
sponse to pathogens at the site. Migratory birds have marked increases
in blood butyrate (fatty acid produced by gut microbes) just after a
long ight, which then decreases after food intake (Landys et al.,
2005). This suggests that butyrate and butyrate producing microbes
may play a functional role during periods of fasting (as demonstrated
in Gao et al., 2009; Lin et al., 2012). Butyrate is important for modulating
immune response and is an anti-inammatory agent (Chang et al.,
2014). In chickens, butyrate is shown to increase antibacterial proper-
ties of monocytes against pathogenic bacteria (Sunkara et al., 2011).
Modulation of butyrate during migration could reect microbial modu-
lation of immunity, and these kinds of microbe-immune interactions
present promising future research questions.
4.3. Reproduction
Generally, the reproductive phase of avian lives occurs in relatively
warm seasons or climates, which should enhance microbial abundance
and diversity at a time when adults are also investing signicant re-
sources into reproductive investment, making it a particularly vulnera-
ble period. Mating success can be both costly and stressful, and often
mating success is inuenced by pathogens (e.g. Jacobs et al., 2015).
The demands of egg formation could mean that nutritional resources
and immune molecules are allocated towards reproduction, imposing
a dampening of expensive defense mechanisms like the acute phase re-
sponse, though the maintenance of leukocytes has been identied as
relatively inexpensive (Klasing, 1998).
In addition to seasonal and habitat effects, defense strategy during
the reproductive phase may depend on reproductive roles (Lozano
et al., 2013). Females must generate defense molecules for eggs, and
so are expected to be investing in the generation of proteins such
as lysozyme and avidin, and may also increase their plasma cell se-
cretion of IgY for yolk antibodies (Addison et al., 2009; Klasing,
1998). Males with many mating opportunities to lose due to sickness
may utilize a combination of tolerance and rapid innate immune
strategies (Lozano et al., 2013), while those employing monogamous
mating strategies may utilize immune strategies best suited to the
local disease environment, or other life history considerations.
Kittiwakes (Rissa tridactyla), maintain antibodies to lyme disease
(Borrelia bacteria) (Staszewski et al., 2007), and transfer these anti-
bodies to their offspring via eggs (Gasparini et al., 2001). However,
food availability decreases humoral immunity (Gasparini et al.,
2006) and the transfer of antibodies to eggs (Gasparini et al., 2007).
Moreover, in kittiwakes, cell-mediated immunity declines during the
chick feeding stage, suggesting this aspect of immunity may be difcult
to maintain during the energy demanding nestling phase of breeding
(Broggi et al., 2010). Trade-offs are commonly found between reproduc-
tive effort and immune defense (Ardia, 2005; Deerenberg et al., 1997;
Ilmonen et al., 2000). It would be informative to study immune defense
and reproductive investment in a species which breeds across environ-
ments of vastly different microbial risk.
4.4. Molt
Microbial risk at molt depends on the environment used and some
species may seek out habitats with lower microbial risk for their molt
period, or reduce movement activities to minimize exposure to novel
microbes. Conspecic transmission of pathogens may be at its highest,
as some species congregate during the molt period and the compro-
mised integument should increase transmission probabilities. During
the molt-fast, little penguins (Eudyptula minor) and king penguins
Please cite this article as: Evans, J.K., et al., Ecoimmunology and microbial ecology: Contributions to avian behavior, physiology, and life history,
Horm. Behav. (2016), http://dx.doi.org/10.1016/j.yhbeh.2016.12.003
(Aptenodytes patagonicus) have marked changes in their gut microbiota
between the start and end of molt (Dewar et al., 2014), with potential
butyrate producing microbes increasing in king penguins and not
changing in little penguins.
The protein demands of molt are purported to be high (Lindstrom et
al., 1993), and protein availability potentially limiting, and so defense
should rely on reusable enzymes/complement to minimize protein
costs. Moreover, there is now a substantial and rapidly growing litera-
ture on the effects of feather degrading bacteria on feather quality and
the consequences for long-term tness (Flp et al., 2016; Leclaire
et al., 2014). We hypothesize that the usual immune strategies may be
modied to reduce protein expenditures, such as an acute phase re-
sponse employing febrile response without as much dependency on
acute phase proteins, or phagocytosis of pathogens, but with lower
carryover into the specic antibody production phase of immune
response. Holt (1992) reports a depression of cellular immunity
but not antibody response during induced molt of hens, however
the effects of molt status cannot be disentangled from the effects of
nutritional status in this study. Hypertrophy of immune organs
such as the spleen and thymus are associated with molt (Silverin
et al., 1999; Ward and D'Cruz, 1968). This is thought to be caused
by high lymphoid activity as a result of infection from feather break-
ages (Silverin et al., 1999). As reviewed by Hoye and Buttemer
(2011), other immune changes during molt include decreases in hu-
moral immunity (Alodan and Mashaly, 1999; Buehler et al., 2008)
and inammatory response (Alodan and Mashaly, 1999; Buehler
et al., 2008; Martin, 2005), and increases in total immunoglobulins
(Bourgeon et al., 2007; Pap et al., 2010) and monocytes (Buehler
et al., 2008; Nava et al., 2001). Experimental immune activation
delays molt (pied ycatchers Ficedula hypoleuca; Sanz et al., 2004),
which could be due to competing protein demands, or possibly an
adaptive response to ensure the vulnerable molt stage doesn't
overlap with infection. In great tits, heterophils increase during the
rst half of the molt period and immunoglobulins increase in the
second half of the molt period (Pap et al., 2010), perhaps suggesting
that the early and late molt susceptibility and immune costs demand
different responses or that the pathogens change across the molt
period.
5. Ecological considerations
5.1. Microbial biogeography
Global microbe diversity and density are predicted to follow latitudi-
nal diversity trends (Fuhrman et al., 2008; Stephens et al., 2016) but
biogeography of microorganisms is complicated by host associations
(e.g. Altizer et al., 2007; Huang et al., 2015; O'Dwyer et al., 2012) and
a release from some of the biogeographical processes that shape
macroorganism diversity and distribution (Horner-Devine et al., 2007;
Martiny et al., 2006). Within high latitude zones temperature predicts
pathogen richness, while within low latitude zones precipitation
predicts pathogen richness (Cashdan, 2014). There are monotonic
altitudinal trends in microbial diversity, with highest diversity at
lowest altitudes, and declining diversity with increasing altitude
(Bryant et al., 2008). Water and water transport is an important
predictor of free-living microbial diversity (Martiny et al., 2006),
and diversity follows aridity clines (Horrocks et al., 2012). Another
important predictor of microbial exposure for adult birds is the
density of conspecics and heterospecics that may act as alternate
hosts for colonizing microbes (Huang et al., 2015). Pedersen and
Davies (2009) map human zoonoses risk by considering pathogen diver-
sity in primates with range overlaps with human settlements, corrected
for the phylogenetic relatedness of the primates, and consider host shifts
to be a primary factor in pathogen risk. We know of no such approach
for birds, where even inuenza studies have failed to correct for host
phylogeny (e.g. Herrick et al., 2013).
 J.K. Evans et al. / Hormones and Behavior xxx (2016) xxxxxx
5.2. Foraging
The microbiome of bird species will undoubtedly be a function of
their foraging habitat, sex and seasonal variation found in their foraging
habitats, but the study of comparative avian microbiomes remains wide
open. We predict that species which are generalists are more likely to be
exposed to a wide variety of bacterial assemblages, whilst specialist
feeders will have much narrower bacterial exposure, in line with predic-
tions and ndings for human gut microbiomes (Heiman and Greenway,
2016). We further predict that species that forage cooperatively are
more likely to share bacterial assemblages between individuals than
species that forage alone, suggesting that cooperative foragers may
show greater consistency in their seasonal immune defense variation.
The same could be predicted of species that conduct incubation feeding,
where males feed their partner on the nest, presumably transferring
some of their own bacterial assemblage. However, no work has been
done to date to quantify these effects. We know of little work testing
the effect of trophic level on microbial infection risk or microbiome di-
versity (Waite and Taylor, 2015) in birds.
6. Conclusion: key questions and techniques
Much remains to be revealed about the inuence of microbes on
avian immunology, endocrinology, and behavior. Here, we present the
key questions to be pursued in avian microbial ecology if we are to un-
derstand this neglected inuence on life history evolution.
6.1. What is the structure of microbial communities associated with birds
and what are the functional roles of those microbes?
Our understanding of which microbes are relevant, either
pathogenically, symbiotically or commensally to wild birds is relatively
poor. Much of the work on microbes in wild birds has focused on path-
ogens, particularly of zoonotic or economic signicance (Huang et al.,
2014; Stephens et al., 2016). Incorporating consideration of the
microbiome in immunobiology and life history evolution will require
the use of cutting edge sequencing technology to interpret the role of
microbial ecology. Avian biology, as for studies of most wild vertebrates,
has yet to take full advantage of recent advances in molecular tech-
niques for the characterization of avian-associated microbe commu-
nities. Well established techniques such as terminal restriction
fragment length polymorphism (T-RFLP) and denaturing- or tem-
perature-gradient gel electrophoresis (DGGE (e.g. Klomp et al.,
2008) and TGGE) are simple, inexpensive, and offer good community
coverage for studies of microbiomes (Rastogi and Sani, 2011). In ad-
dition, the new technological leaps in genomics and transcriptomics
will offer exciting opportunities to obtain more detailed descriptions
of microbe communities. As studies build in this area integrating
these data will enable greater knowledge of microbial interactions
with wild vertebrates (Rastogi and Sani, 2011), as they offer deeper
community coverage, and should also serve to reveal aspects of
functional roles. Moreover new culture methods are now available
(Allen-Vercoe, 2013) to allow us for the rst time to culture commensal
gut microora, making it feasible to do manipulative, experimental
microbial biology in vertebrates.
How has co-evolution with microbes shaped immune defense and
how readily can the immune system adjust to rapidly modied microbe
communities? Whilst germ free models have greatly helped shape our
proximate understanding of immune function it is now important to
consider ecologically relevant settings, in order to understand how
evolution has shaped the immune system of birds. We know that bird
species vary widely in their immune strategies, but we have little micro-
bial context that might help to explain these differences. Characterizing
immune function in relation to microbial pressures will highlight the
tradeoffs between immunity and other costly processes wild animals
face.
Please cite this article as: Evans, J.K., et al., Ecoimmunology and microbial ecology: Contributions to avian behavior, physiology, and life history,
Horm. Behav. (2016), http://dx.doi.org/10.1016/j.yhbeh.2016.12.003
7
6.2. How has co-evolution with microbes shaped metabolism and nutrition-
al niches of birds?
It is well established that commensal gut microora are important to
nutrition and nutritional utilization of vertebrates. However, the extent
to which microbes might inuence avian metabolism, the nutritional
niches or indeed the behaviour of birds is poorly quantied. Host spe-
cies must evolve to facilitate the development of healthy commensal
microbiomes. Gut microbial diversity is also dependent on host gut
size, where longer guts provide for a wider niche space leading to higher
microbial biodiversity (Godon et al., 2016). Individual variation in gut
microbiomes could lead to individual variation in metabolism or feed
utilization efciency (e.g. Sonnenburg and Backhed, 2016).
6.3. How have interactions with environmental and enteric microbes
shaped life history evolution of birds?
Because bird-microbe interactions can be pathogenic or benecial,
there are both avoidance and afnity associations which might inu-
ence evolution of life history and behavior. As discussed throughout,
understanding how microorganisms impact life history traits such as
reproduction, growth, and movement, is crucial in gaining a full under-
standing of how microbes have shaped evolution in wild birds. Further-
more, tradeoffs between life history activities and immune function
needs might inuence the outcomes of microbial interactions. This
could also reveal the characteristics and identity of spreaders of disease.
An integrative approach, measuring aspects of microbial communi-
ties, and their functions, associated with avian species across numerous
habitats and a spread of life history characteristics, will begin to reveal
the many ways that microbes have inuenced the physiological
and ecological diversity of birds. Future studies should utilize new
techniques that allow the quantication and manipulation of entire
microbiomes, rather than individual microbes, and take consideration
of immunological, nutritional, and endocrine mediators of the inu-
ences of microbes on avian life history and behavior.
Author contributions statement
JKE wrote the rst draft of the Eggs and Embryos and Nestlings and
Juveniles sections. BA wrote the rst draft of the Adult Phases section.
KLB and BA jointly wrote the Ecological Considerations sections. JKE
and KCK developed Fig. 1. BA and KLB developed Fig. 2. JKE and BA
jointly wrote the Introduction and Conclusion sections. KLB, SG, and
KCK revised the subsequent manuscript drafts.
Acknowledgements
We wish to thank the editors of the special issue for the invitation to
submit our review.
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