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Plant Ecology & Diversity

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Is light interception of understorey species

facilitated by light reflection from plant neighbours?
a

Anette Grff , Gerald Moser & Paul Heiselmayer

a

Organismic Biology, University of Salzburg, Salzburg, Austria

Plant Ecology, University of Giessen, Giessen, Germany

Published online: 25 Mar 2014.

To cite this article: Anette Grff, Gerald Moser & Paul Heiselmayer (2014): Is light interception of understorey species
facilitated by light reflection from plant neighbours?, Plant Ecology & Diversity, DOI: 10.1080/17550874.2014.898162
To link to this article: http://dx.doi.org/10.1080/17550874.2014.898162

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Plant Ecology & Diversity, 2014

http://dx.doi.org/10.1080/17550874.2014.898162

Is light interception of understorey species facilitated by light reection from plant neighbours?
Anette Grffa*, Gerald Moserb and Paul Heiselmayera
a

Organismic Biology, University of Salzburg, Salzburg, Austria; bPlant Ecology, University of Giessen, Giessen, Germany

Downloaded by [Universitaetsbibliothek Giessen], [Gerald Moser] at 07:10 27 March 2014

(Received 4 November 2010; nal version received 16 February 2014)

Background: Facilitation is an ecological process that has previously been discussed largely in relation to the modication
of abiotic conditions in extreme habitats. Here, we introduce the concept of reected radiation as a potential facilitation
mechanism that may raise the beneciarys resource level in light-limited habitats.
Objectives: We examined whether plants may be able to use their spatial architecture to increase their light absorption
through the use of radiation reected by their neighbours. We tested if this interaction resulted in increased biomass or leaf
area between the respective pairs of species.
Methods: We determined the biomass and leaf area of eight common herb-layer species, composed of four grass and four
herb species, in a beech forest. Plant three-dimensional architecture was digitised and used to simulate reected and
absorbed radiation between the species in a virtual black box. To accomplish this, a so-called light donor plant (which
reected light from its leaf surfaces) was surrounded by four receptor plants (which absorbed this reected radiation) at a
distance of 10 cm. This was repeated using every combination of the available species. We established a ray-trace
simulation, including measured light reection and transmission rates of leaves that enabled us to quantify the relative
light absorption by receptor plants, expressed as brightness per leaf area, and estimated the amount of incoming photons.
Furthermore, we calculated Seifans importance index as an indicator for the relevance of the postulated facilitation effect on
plant biomass and leaf area.
Results: The leaves of the species studied reected ca. 7% of radiation between 400 and 700 nm and 18% between 540 to
650 nm of daily incident photon ux density, corresponding to the accessory pigments range of efcacy. An average of
0.19% of radiation reected by a donor plant reached a receptor plant. The benets to receptor plants varied signicantly
with donor identity. Conspecic donors supplied signicantly larger benets for Stellaria, Galium, Brachypodium and
Hordelymus, which are rhizomatous plants with short stolons. Clones of these species may be able to increase their daily
light intake through absorption of reected light by 0.2%, 0.55.0%, 5.0% and 0.611.6%, respectively, depending on the
number of donor ramets and on the distance between the donor and receptor ramets. Nonetheless, the estimated conspecic
facilitation effects through light reectance within a single clone did not translate into increased biomass.
Conclusion: As light intensity decreases with distance according to Lamberts law, a signicant increase of light intake
through neighbours can only be predicted for plants with a high density of donor ramets, such as clonal species having many
ramets within a short distance. We suggest that in strongly light-limited habitats there may be an advantage to a clonal
growth strategy due to the observed facilitation effect of absorption of reected radiation. To evaluate the magnitude of this
effect, future studies should concentrate on payback times of leaves with low light intake to gauge the period of time
necessary for one leaf to offset the necessary investment in photosynthetic light capture, calculated as cost-benet
calculation between the cost of the leafs production and the net carbon gain realised by it.
Keywords: Brachypodium; facilitation; Galium; herb-layer; Hordelymus; light gain; plant architecture; reection; ray-trace
simulation; shade tolerance; Stellaria

Introduction
Facilitation is dened as the direct or indirect interaction
between two or more organisms, where the benefactor has
a positive effect on the growth or reproduction of a beneciary (Bertness and Leonard 1997). The term facilitation
has also been used to describe the amelioration of harsh
physical conditions in a variety of stressful environments
(Callaway 2007). However, Holmgren and Scheffer (2010)
have suggested focusing facilitation research not only on
physically harsh environments with low plant cover but
also on other habitats with high plant density, stronger
species competition and/or limited resources.
Mechanisms of direct facilitation include changes in
substrate characteristics and increases in resource

*Corresponding author. Email: anette-graeff@web.de

2014 Botanical Society of Scotland and Taylor & Francis

availability, while indirect facilitation may involve eliminating potential competitors or introducing other symbiotic organisms, such as soil microbes, mycorrhizae or
pollinators or species that offer protection from herbivores
(Callaway 1995, 2007). Facilitation mechanisms that
improve resource conditions for plant species have been
demonstrated in both water- and nutrient-limited environments (Pugnaire et al. 2011; Schb et al. 2012). However,
we are not aware of any study that investigated potential
facilitation through light reectance in light-limited habitats. So far, studies on facilitation effects have treated
radiation only as a factor creating stress in the form of
desiccation and heat that can be mitigated by nurse plants
through the creation of shade (Pugnaire et al. 2011).

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A. Grff et al.

In forests, overstorey trees create light-limited conditions for the understorey through shading (Grime 1978);
for example, beneath dense beech forest canopies the
photosynthetically active radiation (PAR) ranges from
0.20.4% of full sunlight (Barness et al. 1998 in
Valladares 2003). Consequently, understorey plants must
be able to cope with low light availability and, for most of
the time, with the lack of direct sunlight (Whatley and
Whatley 1980). Transmission of PAR through forest canopies has been modelled in detail within the context of
remote sensing research at stand levels (e.g. Stadt et al.
2005). The tree leaf canopy of deciduous temperate forest
is a selective lter, and the radiation which passes through
is decient in red and blue zone and rich in green light and
near-infrared (IR). A higher proportion of chlorophyll b
relative to chlorophyll a was found in some shade plants to
enhance light-absorbing capacity in the blue-green wavebands (Packham et al. 1992).
The objective of this study was to test if light-limited
conditions could be improved by reection or transmittance of radiation among coexisting plants. In this study,
facilitation through plant neighbours was considered as an
increase in the level of diffuse radiation available for
absorption. The plant attributes responsible for the potential intensity of such an effect included the transmission
factor of the leaves, reection rate and spatial conguration that determine the amount of reected radiation.
The inuence of the spatial conguration of forest
understorey plants on leaf light-harvesting capacity has
been widely discussed (Givnish 1982; Takenaka 1994;
Pearcy and Yang 1998; Valladares 2003; Cescatti and
Niinemets 2004), and understorey light conditions have
been recognised as a major factor in species replacement,
especially in terms of forest succession (Bazzaz 1979).
The relative light intensity in the understorey of deciduous
forests was found to range mostly between 1 and 3%
(Emborg 1998).
Herbaceous forest understorey species are strongly
adapted to the stressing forest environment, and severe
shading is the strongest ecological selective factor
(Decocq and Hermy 2003). Shade-tolerant plants can tolerate low light conditions because of their high content of
chlorophyll and a combination of many other traits (see
Valladares and Niinemets 2008): they are usually chamaephytic, evergreen or wintergreen perennial species which
are able to build large colonies, have a spongy mesophyll
with very large palisade cells in leaves, with low metabolic
rates (Givnish 1988) and therefore low light compensation
points (5.69.3 mol m2 s1), attaining light saturation at
low levels (ca. 40110 mol m2 s1) (Packham et al.
1992). Clonal vegetative reproduction appears to be more
important than sexual reproduction, usually owing to stolons that allow the formation of long-lived creeping carpets of plagiotropic stems (Decocq and Hermy 2003).
These authors have suggested that such modular herbs
mobilise all their resources to maximise their foliar area
to capture light, while owering and fruiting are of secondary importance. For example Lamium galeobdolon

does not ower in the most shaded environment. Many

shade-tolerant species arrange the leaves in a wide planar
layer, which maximises light interception in deeply shaded
understories (Valladares and Niinemets 2008).
Jonsdottir and Watson (1997) suggested extensive integration of clonal growing plants to be an adaptation to the
low average availability of one or more resources. Plants
in resource-poor environments may benet by providing
them with a means of conserving scarce resources, developing a division of labour between ramets of different
generations, and exploiting patchily distributed resources
and providing a mechanism for strong intra-clonal control
of ramet production through apical dominance.
Kppers (1991) assumed that the way a species occupies, exploits and structures space may be more important
than maintaining a high surface area to potentially absorb
PAR. Anten and Hirose (1999) showed that light capture is
not only determined by height and total leaf area, but also
by the geometric arrangement of the leaf area. These
observations may be particularly relevant for clonally
grown plants, where a ramet can potentially absorb radiation that was reected by neighbouring ramets of the same
plant.
In this study understorey plants that reect radiation
from their leaf surfaces are referred to as donors. They
potentially increase the light yield of their neighbour
plants, which are called receptors.
We hypothesised that the utilisation of reected light
can constitute a resource in light-limited habitats, such as
the herb-layer of forests, thereby representing an important
aspect of the above-ground interaction of neighbouring
herb-layer species. Furthermore, if plants are able to prot
from light reected by their neighbours, we expect that
this benet may be measured in increased biomass and
leaf area of plants growing in association with lightreecting neighbours. Therefore, we addressed the following questions: (1) Do different herb-layer species supply
different amounts of reected light to neighbour plants,
dependent on the reection rate of leaves and plant architecture? (2) Which combinations of species are the most
favourable to increase the light interception of receptors?
(3) Is any potential reected light facilitation associated
with increased biomass of the receptor plants?

Materials and methods

Study area, plot selection and data collection
The eld work for this study was conducted in a mixed
deciduous forest growing on limestone bed-rock in
Thuringia, Germany (445 m a.s.l., 51 05 N, 10 28 E)
dominated by Fagus sylvatica L. The overstorey was
also composed of Fraxinus excelsior L. and Acer pseudoplatanus L.
The vegetation was recorded in four plots of 1 ha. In
each plot four transects (50 0.5 m) were randomly
positioned. Two randomly chosen subplots of 0.5 m
0.5 m were harvested in each transect in August 2002.

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Light reection as a facilitation factor

The phenological stage of grasses progressed from a fully
developed vegetative state over fruit setting to rst leaf
yellowing, while most herbs were in the fully developed
vegetative state.
Previous studies that evaluated the facilitation effect of
cushion plants or shrubs, through water or nutrient amelioration, selected the plots sizes corresponding to the
canopy size of the benefactor (e.g. Anthelme et al. 2011;
Howard et al. 2012). For interactions by light a distinct
interaction radius is difcult to derive, therefore the subplot size was determined to cover species co-occurrence
on a distance close enough to ensure that the individual
plants found within a subplot could intercept reected
light from each other. Furthermore, species studied here
varied in their lateral spread per year between 0.10.25 m
(Klimeov and Klime 2012). As our study focused on
individual plants, i.e. the sum of parental and offspring
ramets that form a physiological unit, we assumed that all
ramets of a species within the subplot belonged to the
same individual and pooled biomass and leaf area of all
ramets of a single species in each harvested subplot.
The leaf area of all plant species within each subplot
was measured after harvesting, using LiCor LI-3000C and
LI-3050C leaf area meters (Licor, Lincoln, Nebraska,
USA); leaf area was related to the ground area of the
subplot. The dry weight of stems, leaves, owers and
fruit was recorded after a minimum of 24 h of oven drying
at 80C. For the work reported we used the dominant
herb-layer species, i.e. the four perennial herbs: Galium
odoratum (L.) Scop., Stellaria holostea L., Mercurialis
perennis L., and Lamium galeobdolon (L.) L., and the
four perennial grasses: Brachypodium sylvaticum
(Huds.) P.B., Melica nutans L., Milium effusum L., and
Hordelymus europaeus (L.) Harz.
Based on the above-ground biomass and leaf area of
each species in each harvested forest subplot Seifans
importance index was calculated, to address the question
if potential reected light facilitation was associated with
increased biomass of receptor plants in the neighbourhood
of beneciary donors. Seifans index species the direction and intensity of plantplant interactions and represents the magnitude of the studied biotic interactions
relative to the magnitude of all other factors on the plant
including environmental and biotic factors (Seifan et al.
2010). It was calculated as:
Iimp Nimp =jNimp j jEimp j

(1)

Nimp PN  PN

(2)

Eimp PN  MPN

(3)

with

where P+N is the biomass of the target plant in the presence of neighbours, PN being the biomass of the target
plant in the absence of neighbours, and MPN is the

maximum value of the biomass of species in the studied

system regardless of neighbouring plants (Seifan et al.
2010).
Seifans importance index was calculated for all possible combinations of the eight studied species. To estimate, for example, PN for the species combination
Galium and Stellaria, we used the biomass data of those
subplots where we encountered only Galium while
Stellaria was missing. To estimate P+N for the same species combination we used the biomass data of those subplots where we encountered both the target plant species
Galium and the examined neighbour species Stellaria. As
a complementary estimate of the receptor prot we calculated Seifans importance index with leaf area data from
the harvested plants.
Data concerning the morphological attributes of plants
with clonal reproduction were taken from CloPla3 - database of clonal growth of plants from Central Europe
(Klimeov and Klime 2012).
Optical properties and modelling
In the following, the terminology for the modelling of the
progression of radiation between plants dened in Table 1
was used throughout the manuscript.
The spectral reection factor of the light-exposed surface of the grown leaves (n = 10 leaves per species) within
the photosynthetically active part of the spectrum was
measured with the Color Quest XE spectrophotometer
(Hunter Associates Laboratory Inc.). In the case of the
herbs, the light-exposed surface was the upper surface of
the leaves. The examined grasses, however, rotate their
lamina during their juvenile development, thus turning
their leaves morphological lower surface towards the
light. Therefore, we measured the spectral reection of
the lower leaf surface of the grass species. ColorQuest is
a device typically employed to measure colours with the
CIELAB system (McLaren 1976). The CIELAB system
denes a colour space using three axes. We utilised the
light-dark-axis L, which supplies an approximate
Table 1. Denitions of plant interactions in relation to light
reectance-absorbance.
Term
Donor

Denition

A plant or ramet that reects radiation on its leaf

surfaces, potentially increasing the light yield
of its neighbour
Conspecic
A donor plant or ramet that reects radiation to
donor
another plant or ramet of the same species
Heterospecic A donor plant or ramet reecting radiation to a
donor
plant or ramet of another species
Donor
Amount of radiation reected from a donor, as
performance
determined by leaf area, degree of selfshading and species-specic reection rate of
the donor
Receptor
A plant or ramet that absorbs radiation reected
by its neighbours leaves
Receptor prot Amount of radiation absorbed by a receptor

A. Grff et al.

reection factor. For a colour sample n, it is calculated as

follows:
L 116Y =Yn 1=3  16

(4)

with Y = hue standard value for ideal white and Yn as the

summed integral over the wavelength range 400700 nm.

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Yn F

S Ry

(5)

The algorithm of the norm tri-stimulus value Y is

inuenced by S, the light intensity of the illuminating
lamp, and R, the reection factor of the colour sample. F
is the normalising factor.
To determine the transmission factor of the leaves of
understorey plants we sampled 40 leaves per species and
tested them in the lab between 400 and 700 nm with a UV/
VIS/NI spectrophotometer (Perkin-Elmer Life and
Analytical Sciences Inc.).
During overcast sky conditions hemispherical photos
were taken at the respective subplot positions with a sheye lens placed at ground level. These were used as input
les in order to characterise the light environment beneath
the tree canopy using Hemiview Canopy Analysis
Software 2.1 (Delta-T Devices Ltd, Cambrige UK, see
Rich et al. 1999) to calculate the global site factor
(GSF), which gives the proportion of global radiation
under the tree canopy relative to that above the canopy.
The three-dimensional architecture of the species was
measured by using 40 plants chosen at random from outside the harvested subplot. The detailed measurements
were recorded following the data input requirements of
the free software Yplant (Pearcy and Yang 1996; available
under http://prometheuswiki.publish.csiro.au) that supplies
a three-dimensional crown model for the analysis of plant
light absorption and carbon yield. The software requires

information concerning linear stipe, culm and petiole segments (length, diameter, inclination, orientation and relative position) and leaves or linear grass leaf segments
(form of lamina, length, breadth, inclination, orientation
of mid-nerve, orientation of inclination and relative
position).
The three-dimensional architecture of the eight species
was thus reconstructed using Yplant, and the software
supplied the x, y and z coordinates of stipes, culmes,
petioles and leaves, in addition to leaf area and degree of
self-shading.
The coordinates of each plant were imported into
AutoCAD 8.0 (Autodesk, San Rafael, USA) and converted to 3D objects that were arranged in different congurations in a virtual black box for further modelling
(Figure 1). The donor plant was located on the point of
origin on the oor of the black box and surrounded by four
receptor plants (coordinates 0, 0, 10; 0, 0, 10; 10, 0, 0;
10, 0, 0). As most of the digitised plants showed an
obvious asymmetry in the plant architecture, the four
receptors that surround the donor integrated prots
depending on the relative position of the receptor and the
donor. We placed donor and receptor plants at a distance
of 10 cm to each other, as we believed this to be a distance
which is close enough to ensure that the species were
interacting.
To simulate the reection of radiation on leaf surfaces
in AutoCAD, virtual spotlights were positioned on the
centre of gravity of each leaf or each leaf segment (curved
grass leaves often had to be divided into three or more
plane sections). The intensity of the light emitted by these
light sources was adjusted in accordance with each species reection rate to simulate exactly the specic amount
of reected photons per leaf of the corresponding donor
plant. This reection rate is inuenced by the reection
factor, leaf area and the amount of incoming radiation as
determined by the leaf angle. The reection rate (R),

Figure 1. Example of ray-tracing in AutoCAD. Spot lights are situated on the leaf surfaces of the donor plant (Melica) in the centre of
the image. The intensity of the light sources represents the reection coefcient of the donors leaf surfaces. Four receptor plants (Galium)
surround the donor plant, to consider the asymmetry of donor plant architecture and consequent light reection. Bright leaf areas of the
receptor plants indicate interception of reected light which was quantied through brightness value and leaf area.

Light reection as a facilitation factor

designated as donor-provided photon ux density (PFD),
was calculated as:
R

leaf 1n iPEDsh mol m2 s1 x LAshade m2 x L%

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(6)
with iPFDsh being the daily integral of incident PFD (10
June, latitude 10.22 East), LAshade as shaded leaf area and
L as reection factor. Incident PFD and the leaf area were
calculated via a Yplant simulation. The analysis of the
hemispherical photos with Hemiview Canopy Analysis
Software 2.1 (Delta-T Devices Ltd, Cambridge, UK)
showed that below the tree canopy there was only indirect
radiation. Hence the sunlit area of the leaves subjected to
direct incoming radiation could be left out of
consideration.
After positioning the light sources, the scenes were
rendered within AutoCAD by employing the photo raytrace procedure, calculating the path of rays three-dimensionally starting at the donor leaf surfaces, in accordance
with the corresponding optical laws. The accumulated
amount of photons reaching the leaves of the receptor
plants was then quantied as relative brightness.
All possible donor receptor combinations of the
eight species were simulated. Simulations of the grass
species involved one individual in vegetative state and
one owering in each combination to take the phenology
into account. Each species combination was repeated ve
times with randomly chosen 3D models of donor and
receptor plants obtained from plant architecture data digitised with Yplant based on 10 measured individuals per
species. To determine light incidence on the receptor leafs
upper and lower surfaces, we varied the viewing angle in

AutoCAD (from 79.4 to 280.2 on the x-axis, from 35.5 to

66.4 on the y-axis) and rendered two perspectives for
each scene.
AutoCAD is a vector-based software which is unable to
calculate the amount of photons striking a certain surface.
Hence the rendered images were converted into pixel-based
formats to evaluate the brightness values with CorelDraw 8
software (Corel Corporation, Ottawa, Canada). In the
underlying RGB colour model of CorelDraw, it was possible to quantify receptor prot as the relative brightness
value of the leaf surface, yielding non-dimensional values
on a relative scale from 0255. In order to be able to
estimate the relevance of a facilitation effect, we used our
own calibration to calculate photon levels from brightness.
We applied a linear regression to the leaf brightness values
created by the chosen PFD (this conforms to the spotlights
brightness) and encountered the following correlation (df =
12, P 0.00001, r2 = 0.951, r2adj = 0.947):
y  3:336 98:3894x

(7)

For each modelled plant the resulting PFD values were

summed up for all leaves and divided by four to obtain the
mean receptor prot (P1R-1D) of one receptor from one donor
over a 10 cm distance. To estimate the total receptor prot of a
plant with clonal growth (Pclone) we summed the prot of all
receptor ramets of a 5-year-old clonal plant for each species,
growing within a circle (see examples in Figure 2).
Reasonable numbers of ramets for a 5-year-old plant of each
species were determined with data on clonal growth over a
horizontal direction (m year1) and the total number of ramets
per clonal plant of the respective species from Schubert et al.
(1987) (in Klimeov and Klime 2012; see Table 2). The

Figure 2. Idealised growth form of clonal plants of the eight considered plant species. A number of reasonable ramets of each species
(see Table 2) were placed on a regular grid within a circle, assuming that herbs may have up to six neighbouring donor ramets and grasses
up to eight neighbouring donor ramets. These or similar images were used to determine the amount of ramets with a distinct number of
neighboured donor ramets to calculate total receptor prot of entire clonal plants. In brackets the numbers of displayed ramets are given,
the ramet brightness indicates its relative receptor prot and the number of neighbouring donor ramets.

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A. Grff et al.

potential number of interconnected ramets in the clone is

species specic and depends on the duration during which
the connections between ramets are maintained as well as the
number of offspring generated per parent ramet per year. For
the studied species the maximum potential number of sister
ramets ranges between 4 and >100 (see Table 2).
Based on photos of the subplots taken before the
harvest we assumed that herbs may have, on average, six
direct neighbour ramets and grasses about eight directly
neighbouring donor ramets. For each species the number
of ramets was then placed on a regular grid covering a
circle (see Figure 2). For each receptor ramet (1 n) the
value of P1R-1D (in mol ramet1 day1) of the respective
species was multiplied by its potential number of donor
ramets, which was dependent on its relative position
within the circle, and the total prots of all ramets of the
clone were then calculated. For example, from 50 ramets
of a 5-year-old Galium plant, as displayed in Figure 2, 28
receptor ramets had six potential donor ramets, two ramets
had ve donors, 12 ramets had four donors and the last
eight ramets had three donor ramets. So the absolute
receptor prot (Pclone) for this entire clonal Galium
plant with its 50 ramets was then calculated as the
250-fold P1R-1D (= 28 6 + 2 5 + 12 4 + 8 3)
using the equation below:
Pclone

with DR1n as the number of potential donor ramets for the

respective receptor ramet.

Data analysis
KolmogorovSmirnov tests showed that plant trait data
including the donor performance values and the values of
receptor prot were not normally distributed. Hence all
applied tests followed non-parametric procedures. To test
for signicant differences in receptor prots among different
donor species, we employed a KruskallWallis test and a
WilcoxonMannWhitney test was used as post-hoc test to
locate pair wise differences of species traits. A Bonferroni
correction was applied to adjust the -level of the test.
Spearmans Rho was calculated to analyse correlations
between the degree of self-shading and donor performance.

Results
Leaf area and reection

ramet1n DR1n  P1R1D mol ramet1 day1 

(8)

At the harvest date in August only indirect radiation

reached the harvested subplots and the closed tree canopy
transmitted only 0.140.25% of the incident radiation
(derived from hemispherical photos), creating light-limited
growth conditions for the understorey plants.
From the eight studied understorey species Mercurialis
had the largest leaf area per plant, followed by Brachypodium;
next were Hordelymus, Milium, Lamium and Stellaria with

Table 2. Incident photon ux density (iPFD) per plant/ramet (mean SD) of eight understorey species, receptor prot per single plant/
ramet from a single donor at 10 cm distance (P1R-1D), potential number of clonal offsprings and reported distance between them, and total
receptor prot of clonal plants (Pclone). Both receptor prots are given in relative and absolute values based on the daily integral of iPFD
of a single plant/ramet. Numbers of connected clonal offsprings of plants were calculated by data on the persistence of the connections
between parent and offspring ramets and number of offspring shoots per parent shoot per year. To calculate Pclone with Equation (8) we
used the given absolute values of P1R-1D and the potential number of ramets of clonal plants. Different letters indicate signicant
difference between species (P = 0.05, KruskalWallis and Wilcoxon test).
Incident PFD
daily integral
iPFD

Per plant/ramet

Receptor species
Brachypodium
sylvaticum
Galium odoratum
Hordelymus
europaeus
Lamium
galeobdolon
Melica nutans
Mercurialis
perennis
Milium effusum
Stellaria holostea
#

[mol ramet1
day1]

Receptor prot from

1 donator P1R-1D

Potential number of
conspecic
donators1

Distance
between
ramets#
Clonal growth
in horizontal
direction

Relative

Absolute

Ramets of a
single 5-year-old
clonal plant

[%]

[mol ramet1
day1]

[Number of
connected
clonal offsprings]

[m year

Total receptor prot

of a clonal plant Pclone

Relative

Absolute

[%]

[mol clone1
day1]

0.018

3.02 0.12f
4.02 0.12e

0.020
0.020

6.0 104
8.0 104

7100
>74

0.010.25
<0.01

4.17 0.13e

0.016

6.7 104

7100

<0.25

2.49 0.11g
13.54 0.14a

0.023
0.019

5.7 104
25.7 104

16
16

0.010.25
0.010.25

1.93
1.48

0.05
0.20

5.58 0.12c
4.68 0.12d

0.017
0.016

9.5 104
7.5 104

>74
4

0.010.25
0.010.25

8.60
0.19

0.48
0.01

8.24 0.11

14.8 10

data from Schubert et al. (1987) in Klimeov & Klime (2012).

44

<0.01

5.00
0.505.00
10.12

0.41
0.020.32
0.41

0.5511.60 0.020.35

Downloaded by [Universitaetsbibliothek Giessen], [Gerald Moser] at 07:10 27 March 2014

Light reection as a facilitation factor

leaf areas of similar size; Galium and Melica possessed signicantly smaller leaf areas (at a signicance level P = 0.05;
Figure 3). Radiation transmitted through the leaves turned out
to be a negligible factor for the herb-layer species less than
3 of incoming PAR (Figure 4). Milium and Melica leaves
had highest values of transmitted radiation, with levels of 2.49
and 2.42, respectively (for details see Table 3).
The reection of PAR followed a unimodal distribution (Figure 5). Reection peaked at wavelengths between
540 and 650 nm, where up to 18% of incoming light was
reected. This wavelength range corresponds to the
absorption gap of chlorophyll a and b, but it is within
the absorption range of the accessory pigments. Averaged
over the range between 400 and 700 nm the species
reected between 8% and 12% of incoming radiation

with no signicant difference between the species

(Table 3). However, in total, the grasses transmitted and
reected signicantly more radiation than the herbs (in
both cases P < 0.001, KruskalWallis and Wilcoxon test).
Receptor prot
The simulation showed that a single receptor at a distance
of 10 cm from a single donor was able to absorb an
average of 0.19% of the radiation reected by the donors
leaves. As an average calculated across all receptors and
donors, this receptor prot corresponded to an increase of
daily incident PFD of 0.019% for the herb-layer plants per
donor (Table 2). The lowest receptor prot averaged
across all donors was obtained by Lamium and Stellaria
receptors, absorbing only 0.16% of the radiation reected
by the donors. Despite having the smallest leaf area, the
grass species Melica was able to intercept the largest
amount of reected radiation, followed by Galium and
Hordelymus, but these small differences in mean receptor
prot were not signicantly different (P > 0.05; Table 4).
To estimate the total light yield of a plant with clonal
growth, and not only of a single ramet, the total receptor
prots of all ramets of a clonal plant were combined using
Equation (8). Due to the increase of the incident PFD
when calculated all ramets of the clonal plants Pclone the
absorption of reected light ranged from 0.2% of incident
PFD of a single plant/ramet for Stellaria, 1.4% for
Mercurialis and 1.9% for Melica, 5.0% for
Brachypodium, 0.55.0% for Galium, 10.1% for
Hordelymus and 0.611.6% for Lamium (Table 4).
Donor dependency of receptor prot

Figure 3. Mean leaf area per plant and species derived

from Yplant calculations. Given are ranges, quartiles and arithmetic means. Different letters indicate signicant differences
in leaf area between species (P < 0.05; KruskalWallis and
Wilcoxon test).

Figure 4. Percentage of transmitted light between 400 and 700

nm at 40 fresh leaves per plant species measured in the lab with a
UV/VIS/NI spectrophotometer.

Receptor prots varied signicantly with donor identity

(Table 5). There were, however, no larger prots with
grassgrass or herbherb donorreceptor constellations (P
> 0.05). The grass species Melica received the highest prot
from the herb species Galium and Stellaria (Table 4). For
Hordelymus, Stellaria and Galium, the largest or second
largest reected PAR prots, were both gathered from conspecic donors (Table 4). Hordelymus and Stellaria, followed by Galium were the most effective heterospecic
donors among the eight species, while Brachypodium,
Lamium, Melica, Mercurialis and Milium were the least
effective heterospecic donors (Table 3 and 4).
The amount of light reected by a donor does not only
depend on its leaf surface area, but also on the degree of
self-shading. Self-shading decreases iPFD particularly
when dealing with species with a large leaf surface area
(Mercurialis: Spearmans Rho between leaf area and iPFD
0.721, P < 0.019, Milium: Spearmans Rho between leaf
area and iPFD 0.661, P < 0.002).
Brachypodium received signicantly more radiation
from Hordelymus and Melica than from Mercurialis
(Table 4). Likewise, Galium and Milium absorbed signicantly more radiation from Galium and Stellaria than from
Brachypodium and Mercurialis. Melica received

A. Grff et al.

Table 3. Donor traits. Listed are percentage of leaf transmittance and reectance in the range of 400700 nm, mean photon ux density
(PFD) provided by a donator plant (mean SD) and targets relative performance as donator. The heterospecic Donor Performance is
given as the median order of species, for example 1 was, on average, the best heterospecic donor and 4 means this species was in no
case the best donor. The conspecic Donor Performance is given as the order of species from 18, according to how many heterospecic
donors provide higher prot than the conspecic donor. 1 indicates that the conspecic donor provides highest amount of reected
radiation of all possible donors, 8 indicates lowest receptor prot from a conspecic donator. Different letters indicate signicant
differences between species (P = 0.05, KruskalWallis and Wilcoxon test).
Donor traits

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Species
Brachypodium sylvaticum
Galium odoratum
Hordelymus europaeus
Lamium galeobdolon
Melica nutans
Mercurialis perennis
Milium effusum
Stellaria holostea

Leaf
transmittance []
0.67
1.05
0.79
2.42
1.07
2.49
0.47

n.d.
0.26a
1.31bcd
0.26ab
0.75e
0.20c
3.22de
0.07a

Leaf
reectance [%]
9.76
10.54
9.98
8.41
11.41
9.31
9.77
8.67

1.00a
2.14a
1.27a
0.71a
1.46a
1.08a
1.23a
1.72a

Mean donor provided

PFD [mmol m2 day1]
9.35
8.31
8.60
6.58
0.12
5.97
0.12
0.12

1.31a
1.16a
1.07a
1.23b
0.82c
1.26b
1.00c
0.96c

Heterospecic
donor performance

Conspecic donor
performance

4
3
2
4
4
4
4
1

7
2
1
5
4
8
6
1

0.21; Brachypodium-Stellaria: Iimp = 0.16; see Table S1,

supplementary material). Utilising the importance index
derived from leaf area index we detected positive interactions between the receptor Brachypodium and the donors
Stellaria (Iimp = 0.33), Milium (Iimp = 0.32) and
Hordelymus (Iimp = 0.16).

Discussion

Figure 5. Percentage of reected radiation between 400 and

700 nm at leaf surfaces of the eight considered plant species.
Measurements of 10 fresh and full-grown leaves per species were
conducted in the lab with a Color Quest XE spectrophotometer.
The reection rate was measured on the morphological upper leaf
surface in the case of the four herbs, but on the morphological
lower surface for grass leaves because in situ this leaf side is
usually the light-exposed one.

signicantly more radiation from Galium, Hordelymus,

Melica and Stellaria than from Brachypodium and
Mercurialis. In contrast, Hordelymus and Stellaria
received signicantly more radiation from a conspecic
individual than from Brachypodium and Mercurialis.

Plant biomass in relation to species associations

A signicant effect of reected light facilitation on biomass was only observed for one pair of species; the
receptor Hordelymus exhibited increased biomass when
growing alongside Brachypodium than when growing in
a monospecic stand (Hordelymus-Brachypodium: Iimp =
0.44). Two other pairs of species showed a small positive
but non-signicant effect (Brachypodium-Milium: Iimp =

The results of the overstorey transmittance analysis

demonstrated signicant light limitation in the understorey
of the beech forest, where the eight studied understorey
species experienced only 0.140.25% of the incident
radiation levels above the tree canopy. Leaves of the
eight species showed negligible transmittance (<3), but
a signicantly higher reectance (811%) of PAR. The
leaf reectance in combination with signicant differences
in leaf area between the species resulted in signicant
differences in donor performance and donor-dependant
single receptor prot per donor (P1R-1D), which did not
correlate with the biomass or leaf area of the respective
receptor. In general, P1R-1D was rather low for single plants
(<0.03% of iPFD), but cumulatively for all connected
ramets of a 5-year-old clonally growing plant the receptor
prot was in most cases >1% (except for Stellaria) and
peaked at values between 5 and 10 (12)% of iPFD for
clones of Brachypodium, Galium, Milium and Hordelymus
(and Lamium). This indicates that clonal growth may be
regarded as foraging mechanism which can improve the
utilisation of the limited light resource.
The canopies of deciduous forests change the intensities of radiation passing through them, and highly selectively absorb the wavelength range of 400500 and 600
700 nm (Coombe 1957). The herb-layer has to cope with
the reduced availability of light in the blue and red wavelength ranges, which are the main absorption ranges for
chlorophyll a and b.

Light reection as a facilitation factor

Table 4. Mean receptor prots per plant as the relative portion of reected light from the incident photon ux density (iPFD) of one
single donor (in %). Signicance of the variation between the donors (post-hoc MannWhitney tests on paired differences) was tested
only if the receptor yield differed signicantly between species (see Table 4). Different letters within a column indicate signicant
differences at P < 0.05; no signicant differences of mean prots occurred between species. For the level a Bonferroni correction was
applied. The receptors prots from the best donor species are printed in bold. During post-hoc testing of receptor yields, only the
differences between the both most and the both least effective donors were tested for signicance to keep the risk of a type II error to a
minimum.
Receptor

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Donor
Brachypodium sylvaticum
Galium odoratum
Hordelymus europaeus
Lamium galeobdolon
Melica nutans
Mercurialis perennis
Milium effusum
Stellaria holostea
Mean prot

Brachypodium
sylvaticum

Galium
odoratum

Hordelymus
europaeus

Lamium
galeobdolon

Melica
nutans

Mercurialis
perennis

Milium
effusum

Stellaria
holostea

0.11 ab
0.20
0.24 a
0.20
0.22 a
0.09 b
0.16
0.19
0.18A

0.09 b
0.27 a
0.26
0.21
0.22
0.05 b
0.19
0.32 a
0.20A

0.14 b
0.24
0.28 a
0.18
0.25 ab
0.08 b
0.17
0.24
0.20A

0.09 a
0.19
0.21 a
0.15
0.20
0.06 a
0.14
0.25 a
0.16A

0.12 b
0.31 a
0.29
0.26
0.28
0.08 b
0.23
0.30 a
0.23A

0.10 a
0.25 a
0.26 a
0.20
0.24
0.08 a
0.17
0.19
0.19A

0.09 b
0.25 a
0.22
0.18
0.19
0.05 b
0.17
0.26 a
0.17A

0.07 b
0.23
0.25 ab
0.14
0.17
0.03 b
0.15
0.29 a
0.16A

Table 5. Results from a non-parametric one-way analysis of

variance (KruskallWallis) of receptors prots. Identity of
donor plant was used as the single independent variable factor
and receptor prot as dependent variable. Each receptor species
was tested separately. *P < 0.05; **P < 0.01.
Receptor
Brachypodium sylvaticum
Galium odoratum
Hordelymus europaeus
Lamium galeobdolon
Melica nutans
Mercurialis perennis
Milium effusum
Stellaria holostea

Chi-Square

df

P (asymptotic)

51.97
15.79
24.61
6.07
18.32
6.78
34.43
24.87

7
7
7
7
7
7
7
7

0.000 *
0.027 *
0.001 **
0.532
0.011 *
0.453
0.000 **
0.001 **

There is mounting evidence that a change in the stoichiometry of pigments in the photosystems induced by
these changes in spectral quality is crucial for the efciency of photosynthesis (Chow et al. 1990; Walters and
Horton 1995). Demming-Adams and Adams (1992) and
Thayer and Bjrkman (1990) found a larger amount of carotine and a higher : carotine ratio in leaves adapted
to shaded environments, especially in plant species considered to be highly tolerant of shade. These deep-shade
species exhibit slightly more lutein and neoxanthin relative
to the content of chlorophyll than species of less shaded
habitats, probably enabling them to increase their lightharvesting efciency at very low radiation intensities
(Rosevear et al. 2001). Thus both an increase of light
intensity within the absorption range of chlorophyll a
and b, as well as an increase of light intensity within the
absorption range of the accessory pigments, potentially
presents a relevant boost to the available resource level
of the light-limited species examined in this study.
The number of donors and their distance from the
receptor ramets are crucial factors for the magnitude of
the facilitation effect due to the inverse-square decrease of

light intensity with distance (Lamberts distance law).

Signicant increases in daily light yield via absorption of
reected light can only be assumed for plants with a clonal
growth form. In our study, each single ramet could benet
from the interception of light reected by several close
neighbouring donor ramets (Table 2).
Conspecic donors supplied signicantly higher prots
for Hordelymus and Stellaria. Both are perennial rhizomatous plants that produce connected shoots adjacent to one
another. Stellaria has a very low rate of clonal multiplication,
and the connections between ramets are cut after 2 years
(Klimeov and Klime 2012). Hence we can expect no
more than four connected conspecic donors and receptors
in a 5-year-old Stellaria clone. Such clones are limited in the
extent of any potential increase in daily iPFD to 0.19% due to
the absorption of reected light within the clone. However, if
one clone is surrounded by conspecic, but disconnected
ramets it may achieve a receptor prot of 0.38% of iPFD.
In our study Lamium would not reach the theoretical
maximum receptor prot of 11.6% of iPFD calculated
here, as the clonal growth form we observed would not
t to the theoretical one we used for the simulation. In our
forest stands the distance between upright Lamium ramets
was greater than 10 cm and its receptor prot may therefore be disregarded (=0). Nevertheless, we know from
other forest sites that this species is able to build clones
that are identical to the one simulated in Figure 2.
In the virtual black box simulation, we placed donor
and receptor plants at a consistent distance of 10 cm;
however, previous studies observed a range of distances
from 0.010.25 m between parent and offspring ramets
for all species with the exception Brachypodium and
Hordelymus (Klimeov and Klime 2012). More precise
estimates of the observed facilitation effect requires more
accurate data on the number of connected and disconnected clonal offspring of the species, on the distance

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10

A. Grff et al.

between the ramets and on the number of donor ramets.

As a bunch grass, Hordelymus produces tillers at distances of less than 1 cm (Klimeov and Klime 2012);
due to the very close proximity of ramets we might
assume an even higher receptor prot than the calculated
10.12% of the iPFD for an individual plant of this
species.
By means of Seifans importance index Iimp we tested
if the postulated effect of facilitation through light reectance does translate into increased biomass or leaf area at
observed understorey conditions with the simultaneous
presence of all other interfering environmental (e.g. soil
properties) or biotic interactions (including shading). We
expected to encounter receptors with greater biomass or
leaf area next to donor species from which they might
receive a signicantly larger amount of reected radiance.
Hordelymus had a greater biomass and leaf area when
growing in one plot together with Brachypodium. This
did not concur with our ndings, according to which
Hordelymus received the smallest amount of reected
radiation from Brachypodium. This shows with regard to
in situ spatial correlations that it is impossible to differentiate between facilitation and shared physical microhabitat requirements (Callaway 1995), microscale habitat
differences, effects of different age of plant individuals
and many other plant interactions including competition
for nutrients and shading. Nonetheless, facilitation through
reected light may have affected other plant traits than
biomass and leaf area, for example reproduction success or
photochemistry.
As our dataset evaluating the importance of facilitation
consisted of only 32 plots, the calculation of Iimp was
strongly inuenced by outliers. Homogeneous pure stands
generated high values of MPN, thus reducing the rank of
P+N values, so that further positive spatial correlations
have possibly been overlooked. More importantly, our
conspecic facilitation effects could not be conrmed by
Iimp as we used data on the level of the entire clone and not
in terms of single ramets of the same individual. Data
analysis based on the presence of ramets is restricted as
these data cannot be regarded as statistically independent
units.
As facilitation is dened as a positive effect resulting
from the interaction between different organisms here
considered as an increased level of diffuse radiation
obtained by the receptor the positive increase in light
yield of an entire clonal growing plant via cross-wise
reection and absorption of radiation by its sister ramets
would not be consistent with the denition of facilitation
in its strict sense. Nonetheless, consideration has to be
given to the duration of connections between the parental
and offspring ramets. These connections are often cut after
some years, dependent upon the species, so that the interaction would subsequently take place between discrete
organisms. Clonally growing plants may be interpreted
as a special case of nurse plants for non-sexual reproduction, in which maternal ramets provide increased light
resource availability for their offspring and facilitation in

its strict sense begins as soon as the inter-ramet connections are cut.
To be able to classify the ecological relevance of the
facilitation effect by reected radiation more accurately,
we suggest utilising the concept leaf payback time, introduced by Jurik and Chabot (1986). They dened the payback time of a leaf as the period of time necessary for one
leaf to amortise; calculated as a cost-benet calculation
between investment in production of the leaf and its net
carbon gain realised over time (Poorter et al. 2005),
including the allocation of metabolites to maintenance
respiration and growth over the course of the growing
season. We assume that the facilitation effect can reduce
the payback time at low-light leaves. To verify this, we
need extensive data concerning construction costs, apparent quantum yield, the curvature of the light-response
curve as well as mass-based photosynthetic capacity and
respiration (Poorter et al. 2005). At the same time it will be
necessary to isolate positive plantplant interactions from
all possible environmental factors by employing a research
design with a starting point and nal harvest of target in
addition to control group plants for comparison (Connolly
et al. 2001).

Conclusions
Based on this study, we assume that the facilitation effect
by reected radiation from neighbours constitutes an
innate advantage of the phalanx strategy (sensu Lovett
Doust 1981) in deep-shaded environments. Clonal
growth is regarded as a foraging mechanism that can
improve the utilisation of the available resources while
reducing intra-clonal competition (Harper 1985). The
ability to share resources among modules is considered
to be a benet of the clonal growth habit. Parent ramets
that support their offspring may temporarily buffer the
whole clone against locally adverse conditions, leading
to an increased performance of connected ramets
(Wijesinghe and Handel 1994). Furthermore, cascade
utilisation of reected PAR within the clone can increase
overall light use efciency.

Acknowledgments
We are grateful to F. Grff, C. Grff, T. Philip and A. Shinikov
for their help in the eld. We especially thank N. Czaja and S.
Graeff for critical comments on an earlier draft that signicantly
improved this manuscript and M. Haworth for nal proof-reading. We are indebted to H. Witt, R.W. Pearcy, M. Karatassiou, F.
Mayerhofer, V. Bremerich and G. Zotz for great support with
data processing in Yplant and AutoCAD, and C. Reim and F.
Heidenhain for statistical advice. We thank L. Kador for the
opportunity to carry out reectance measurements. We thank T.
Vogtman for assistance with transmittance measurements.
Discussions with H. Lddeckens, E. Derichs, W. Glaubitt, N.
Soethe and S. Fleck provided helpful insight. We thank M.
Wartinger and K. Lblich-Ille for laboratory analysis and M.
Schmidt for providing eld equipment. We especially thank
three anonymous referees and the editor for valuable comments
on earlier versions of this manuscript.

Light reection as a facilitation factor

Notes on contributors
Anette Grff is a vegetation ecologist interested in the interaction
of plants in managed ecosystems of Central Europe, from grasslands to forests with special interest on the succession after
disturbance.

Downloaded by [Universitaetsbibliothek Giessen], [Gerald Moser] at 07:10 27 March 2014

Gerald Moser is a plant ecologist studying C- and N-cycling of

natural and managed ecosystems from the tropics to the polar
zone, focusing on root dynamics and the effect of climate change
on plant species contribution to the ecosystem productivity, studied along elevation gradients, in throughfall displacement
experiments and free air carbon dioxide enrichment (FACE)
experiments.
Paul Heiselmayer is an experienced vegetation ecologist with
special interest to the biogeography of the Alps and the vegetation ecology of grasslands and pastures, montane forests, subalpine and alpine vegetation in Europe.

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