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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
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
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).
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
(1)
Nimp PN PN
(2)
(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
Denition
A. Grff et al.
(4)
Yn F
S Ry
(5)
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.
(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
(7)
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.
A. Grff et al.
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
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]
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
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
44
<0.01
5.00
0.505.00
10.12
0.41
0.020.32
0.41
0.5511.60 0.020.35
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
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
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
Discussion
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
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
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
10
A. Grff et al.
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.
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