Journal of Ecology

2009,

97

, 508–517 doi: 10.1111/j.1365-2745.2009.01491.x

© 2009 The Authors. Journal compilation © 2009 British Ecological Society

Blackwell Publishing Ltd

Carbon gain in the competition for light between

genotypes of the clonal herb

Potentilla reptans

Peter J. Vermeulen

1

*, Josef F. Stuefer

2

, Niels P. R. Anten

1

and Heinjo J. During

1

1

Department of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, PO Box 80084, 3508 TB Utrecht, The Netherlands; and

2

Experimental Plant Ecology, Institute for Water and Wetland Research, Radboud

University, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands

Summary

1.

Different views exist as to what traits will lead to dominance when plants compete for light. Oneview is that taller plants with better relative positions in the canopy will exclude shorter plantsbecause they intercept almost all light and thus can achieve a higher carbon gain. Alternatively,resource competition models predict that plants that are capable of positive net photosynthesis atthe lowest light level will win. In a 5-year-old dense competition experiment with 10 genotypes ofthe clonal plant

Potentilla reptans

, both these views were tested to see if either of them could explainthe dominance of one of the genotypes, or the possible coexistence of several others.

2.

Using a combination of measured morphological and physiological traits, a canopy model wasconstructed to calculate whole-shoot daily photosynthetic rates of the genotypes in the differentlayers of the canopy in relation to the invested mass.

3.

Results show that the dominant genotype exhibited characteristics of relative shade tolerance:low rates of light-saturated photosynthesis and respiration. This resulted in a calculated daily car-bon gain at the bottom of the canopy, where other genotypes could not achieve that. However, thedominant genotype did not have the highest photosynthetic rates throughout the whole canopy.Some genotypes that persisted in the stand in coexistence with the dominant one achieved greaterdaily carbon gain at the top of the canopy.

4.

Synthesis

. The dominant genotype had characteristics similar to those predicted by resourcecompetition models such as the ability to have positive growth at lower light levels. The persistenceof several other genotypes, in contrast, may be explained by traits that allowed them to achievehigher carbon gains at the top of the canopy. This suggests that the light gradient formed by theplants themselves creates enough heterogeneity for strategies for dealing with different lightrequirements to coexist, even within a single species.

Key-words:

canopy, coexistence, clonal, competition, exclusion, height, light, model, photosyn-thesis, resource acquisition

Introduction

Photosynthetic carbon gain is an important resource forgrowth and reproduction. The efficiency with which plantsacquire light energy and use it for biomass productionthrough photosynthesis can therefore be considered as animportant factor determining the outcome of competition(Hirose 2005). Yet it remains an open question how differ-ences in the way plants acquire and use light energy may leadto the exclusion of plants with certain traits from the popu-lation on the one hand, and to the local coexistence of severalspecies on the other hand.

Some resource competition models suggest that the mostsuccessful competitors are those whose leaves have net positivephotosynthesis rates at the lowest light levels. In other words,species with a low

I*

(the light level at which gross photo-synthesis just compensates for respiration, see Tilman 1988) willwin the competition in well-mixed assemblages, as their lowerplaced leaves can contribute to total plant photosynthesis atlight levels where its competitors cannot grow (Tilman 1982;Huisman & Weissing 1994; Dybzinski & Tilman 2007;Vojtech

et al

. 2007). This would suggest that plants that winthis competition have physiological traits that allow them tocope with low light levels, that is, have shade tolerant traits.Alternatively, species with a higher

I*

that have a larger partof their biomass placed in high-light conditions, may exclude

*Correspondence author. E-mail: peterjvermeulen@gmail.com

Carbon gain in the competition for light

509

© 2009 The Authors. Journal compilation © 2009 British Ecological Society,

Journal of Ecology

,

97

, 508–517

species with lower

I*

as the former will capture more light andconsequently obtain a higher carbon gain than the latter(Tilman 1988; Weissing & Huisman 1994). Theoretical studiesinvolving game theory also predict that in a dense canopy thesuccessful competitors will be the plants that can achievehigher carbon gain than others by capturing more lightthrough an increase in height (Givnish 1982, 1995) or leafarea (Schieving 1998; Schieving & Poorter 1999), suggestingthat they are adapted to high light conditions. These twoclasses of models will for the purpose of simplicity be called‘resource models’ and ‘canopy models’ throughout this article.

Hypotheses as to how competition for light can result incoexistence have mainly focused on differences in heightgrowth (see also Falster & Westoby 2003) in combinationwith differences in photosynthetic characteristics. Tall, dom-inant plants have their leaves placed in high-light conditionsand also have high maximum rates of photosynthesis (Pmax).This combination results in high photosynthetic rates per unitmass (Pmass, Anten & Hirose 2003). However, these plantsalso have to invest disproportionately more mass in stems andthus necessarily invest relatively less in leaves, which thereforetend to have a lower area per unit mass (SLA, Corré 1983).Consequently, tall, dominant species may have similar valuesof light capture per unit above-ground mass (

Φ

mass) assubordinate species (Hirose & Werger 1995; Anten & Hirose1999; Werger

et al

. 2002; Aan

et al

. 2006). Also, as the costs ofproducing and maintaining additional stem material androots that are necessary to support the leaves and supplyit with nutrients rise with increasing plant stature (Givnish1988; Anten & Hirose 2001), the total leaf area per unitground area is expected to decrease with increasing plant can-opy height (Givnish 1988; Anten 2005). This lower amount oftotal leaf area of tall plants could allow for more light to reachthe lower canopy layers, which may be used by shorter, sub-ordinate species of a different architecture (e.g. prostratespecies with high investment in leaves) that are adapted to alower light level, that is, have a lower

I*

(Huisman

et al.

1999).In this way species with different height-growth strategiesmay be able to coexist.

Coexistence of genetically different individuals occurs notonly in mixed-species vegetation but also in mono-speciesstands. Within-species variation in shoot structure, however,may not be large enough to allow subordinate individuals topersist in the lower layers of the stand (Anten 2005), castingdoubt whether within species the same mechanisms will leadto coexistence as between species. Using canopy models,several studies have shown that taller individuals capturedisproportionately more light than subordinate individuals indense mono-specific stands (Anten & Hirose 1998; Hikosaka

et al.

1999; Hikosaka

et al.

2003). In addition, taller plantstend to have a higher carbon gain per unit absorbed light (

ε

)than their shorter conspecifics, leading to higher photosyntheticrates per unit above-ground mass (Pmass; Pmass =

Φ

mass

×

ε

,Anten & Hirose 2001). These canopy models thereforesuggest that within-species competition for light will overtime be won by tall plants that can achieve high carbon gainat the top of the canopy.

However, none of the above-mentioned models haveincluded other genotypic differences that may occur, such asdifferences in morphological and physiological traits. If withinspecies some genotypes have leaves adapted to high-lightconditions while other genotypes have more shade tolerantleaves, the former will be able to achieve higher carbon gain atthe top, while the latter will be able to grow at the lower lightat the bottom of the canopy. Consequently, the light gradientthat is created by the plants themselves may create enoughheterogeneity for genotypes with different morphological andphysiological traits to coexist.

In 1998 an experiment was started with 10 genotypes of theclonal stoloniferous plant

Potentilla reptans

, all growingtogether in competition. At the beginning of the experiment,all 10 genotypes occurred at equal frequencies. Analysis of therelative frequency of these genotypes after 5 years throughDNA extractions, using ISSR primers to identify the geno-types, revealed that one genotype had become most abundant(approximately 40% of all leaves in all replicates), but thatseveral others were still present at approximately the same orslightly higher frequency as they were at the start of the experi-ment. Other genotypes had declined in frequency (J.F. Stuefer,unpublished data, see also figure 1). This suggests that possiblyboth exclusion and coexistence had occurred. The main goalof this article is to see whether these patterns can be betterexplained by the dominant genotypes having traits as pre-dicted by either canopy models or by resource models, orwhether these different strategies could potentially coexist.

To achieve this goal, the photosynthetic characteristics ofthe different genotypes within this competition experimentwere measured and used to construct a canopy model to cal-culate the carbon gain of the genotypes within the differentlayers of the vegetation. Following the predictions of othercanopy models, the most abundant genotypes should havetraits that enable them to utilize the high light conditions atthe top of the canopy, that is, have high maximum photo-synthesis rates (Pmax), leading to high photosynthetic rates perunit above-ground mass (Pmass). Alternatively, if the shift infrequencies occurred due to processes described by resourcecompetition models, the most successful genotypes arepredicted to have traits that allow them to survive at low lightlevels, that is, have low respiration rates, resulting in positivecalculated carbon gain at the low-light levels at the bottom ofthe canopy where other genotypes can not do the same. Ifboth strategies are represented in the experimental plots bygenotypes that are still abundant after five years, this wouldindicate that both these strategies can coexist.

Methods

PLANT

MATERIAL

AND

EXPERIMENTAL

SET

UP

Potentilla reptans

is a stoloniferous herb found in moderately dis-turbed, productive pastures, mown grasslands, at lake and rivershores and road margins (Van der Meijden 1996). The plant pro-duces sympodially growing stolons, which can form a long stringof interconnected ramets on their nodes. In the absence of physical

510

P. J. Vermeulen

et al.

© 2009 The Authors. Journal compilation © 2009 British Ecological Society,

Journal of Ecology

,

97

, 508–517

disturbance the ramets remain interconnected throughout onegrowing season. Because internodes between rosette leaves do notelongate, height growth is exclusively achieved by petiole elongation(Huber 1995, 1996).

In our competition experiment, leaves emerged in spring from thetap roots, and new rosette leaves were placed above older leaves (seeVermeulen

et al

. 2008a). This height growth continued until earlysummer. The leaf area index (m

2

m

−

2

ground surface) quickly reachedhigh values and remained high from then on. Throughout the season,leaf turnover was high, with an average leaf lifespan of around fourto six weeks (Vermeulen 2008).

In 1996 10 ramets of

P. reptans

were taken from 10 different locations,from a broad array of natural and semi-natural habitats from parkinglots to river flood plains, and propagated on potting compost in thebotanical gardens of Utrecht University. Eight experimental popu-lations containing 10 ramets of each these genotypes were established in1998 in plots of 2

×

2 m in the same botanical gardens, on a 1 : 1 : 1mixture of sand, potting compost and leaf litter. Each populationstarted with a total of 100 similar-sized, juvenile ramets planted inLatin Square arrangements in the central 1

×

1 m area of each plot.Each of the genotypes had an initial frequency of 10%. Three timesper vegetation period all plots were fertilized with commercial lawnfertilizer (ASEF® Evergrow, Scotts Benelux, Belgium; 35 g m

–2

)containing inorganic and organic nitrogen sources.

GENOTYPE

FREQUENCIES

AND

LEAF

MORPHOLOGY

IN

THE

COMPETIT ION

EXPERIMENT

At the beginning of July 2003, 5 years after establishment, a lightprofile was measured in four subplots per plot under an overcast sky.Starting at the top of the vegetation two measurements were madeat 5-cm intervals using a ceptometer (Delta-T Devices, Cambridge,UK). Photosynthetic Photon Flux Density above the canopy(PPFD

o

) was measured simultaneously using a Licor Li190 quantumsensor. Then, 100 leaves in each plot were harvested at randomlychosen grid points. The vegetation of the plot was visually dividedinto three layers and each leaf was sampled from a randomly chosenlayer. The leaf whose lamina was horizontally closest to the gridpoint compared to the other leaves placed in the same layer wassampled. Only leaves with fully developed laminas were taken intoaccount. Since the plots were part of an ongoing experiment, wesampled only leaves and left stolons and roots intact.

A leaf was defined here as the petiole plus the palmate lamina,which consists of five to seven leaflets. For each leaf the height of thelamina above the ground and the height of the vegetation at theposition of the sampled leaf were measured. From these two meas-urements we calculated the depth of the vegetation at the height ofthe lamina. Chlorophyll content of each lamina was estimated byone measurement with a SPAD 502 m (Minolta, Japan; see below).Then the lamina was split in two parts: one for the ISSR analysis todetermine its genotype (J.F. Stuefer, unpublished data), and theother for weight and nitrogen measurements. For both parts thelamina area was measured. From the latter half the lamina dry masswas measured, together with the petiole dry mass. Total lamina masswas calculated using the specific lamina area (SL

am

A, m

2

lamina areag

–1

lamina mass) of this latter part, and the combined lamina area ofthe two parts.

To get sufficient material for nitrogen analyses, all lamina halvesof each genotype with similar depth were pooled per plot. Total N(Nt

i

, as %gN of total lamina mass) was analyzed on homogenizeddry material with an elemental analyzer (Carlo Erba, Model EA NA1110, Milan, Italy).

CANOPY

STRUCTURE

AND

L IGHT

EXTINCTION

IN

THE

COMPETIT ION

EXPERIMENT

The leaf area index (LAI, m

2

leaf area m

–2

ground surface) and leafarea distribution in each subplot in 2003 were estimated from themeasured light distributions in 2003 and the extinction coefficientfor light (

K

) by rewriting Beer’s law for light distribution (Monsi &Saeki 1953):

L_c = ln (

I

/

I

o) /

K

eqn 1

where L_c is the cumulative LAI above a given point in the canopyand

I

and

I

o the light intensity at that point and above the canopy,respectively. The LAI in 2003 was estimated by substituting

I

by thelight intensity below the canopy.

K

was estimated from measure-ments made in 2005 (see below). This approach assumes that theextinction coefficient for light did not change significantly between2003 and 2005, which is reasonable given the fact that

K

dependsmostly on leaf angle distribution (Goudriaan 1988) which did notdiffer between genotypes. In addition, the estimated average LAI perplot in 2003 (4.97 ± 0.08) was very similar to the average LAI in 2005(4.96 ± 0.12). In July 2005 the light distribution was measured againas described above. Subsequently all laminas were clipped in each 5-cmhorizontal layer and their area was measured with a leaf area meter(LI-3100 LiCor).

K

was then calculated using eqn 1.

K

was taken asthe average of all eight plots, and was found to be 0.84 ± 0.008 (1 SE,a normal value for a dicotyledonous species (Monsi & Saeki 1953).Because several genotypes were rare and did not occur in many ofthe subplots, the data of the four subplots of each plot were pooled.

Lamina absorbance (

α

) was calculated as a function of laminachlorophyll content (chl,

μ

mol m

–2

) following Evans (1993):

α

= chl/(chl + 76

)

eqn 2

The chlorophyll content in turn was estimated from theSPAD measurements that was done on each lamina sampled (seeabove) using a calibration line made for separate sets of leaves(chl = 27.66

×

SPAD + 21.88,

r

2

= 0.88). Chlorophyll content ofthese leaves was determined with a spectrophotometer on a 2-cm

2

fresh sample extracted in dimethylformamide (Inskeep & Bloom1985). The thus estimated

α

-values neither differ significantly betweengenotypes nor between laminas from different depths, so

α

was setat 0.83, the average that was found for all laminas.

LEAF

GAS

EXCHANGE

MEASUREMENTS

IN

MONOCULTURE

For each genotype (i) gross photosynthesis at saturating light (

P

max

i

)and dark respiration (Rd

i

) were measured on 15 leaves, which weretaken from different layers in the stock populations. Petioles werecut and put in water. Then the petioles were cut again under water,to prevent air blocking the water supply to the laminas. A gas-exchange measuring system was used with leaf chambers with a69

×

67 mm window (Pons & Welschen 2002). An infrared gasanalyzer (LI-6262, LI-COR) was used to measure CO

2

and H

2

Opartial pressure. Lamina temperature was maintained at 25

°

C;lamina-to-air vapour pressure difference was approximately 1 kPa,and CO

2

partial pressure of the air entering the leaf chambers was38 Pa. Light availability was kept at 2000

μ

mol m

–2

s

–1

for laminastaken from the top of the canopy and 1000

μ

mol m

–2

s

–1

for laminastaken from the lower parts, the latter to prevent photo-inhibition

Carbon gain in the competition for light

511

© 2009 The Authors. Journal compilation © 2009 British Ecological Society,

Journal of Ecology

,

97

, 508–517

taking place. Net rates of photosynthesis (

P

net) were calculatedaccording to Caemmerer and Farquhar (1981). Dark respirationrates (

Rd

i

) were measured after 20 min in the dark.

P

max is the sumof

P

net

i

and

Rd

i

. The lamina area enclosed in the chamberwas measured, after which the nitrogen content was measured asdescribed above. From these data the relation between the

P

max andthe nitrogen per unit area (

N

area, g m

−

2

) and Rd and

N

area for eachgenotype

i

can be found from the following equations (Hirose &Werger 1987):

P

max

i

= api × Narea + bpi eqn 3a

Rdi = ari × Narea + bri eqn 3b

MODEL

We calculated net daily photosynthesis of each genotype in differentlayers and in the whole vegetation using a canopy model based onprevious models (Hirose & Werger 1987; Hikosaka et al. 1999),with modifications to account for the growth form of P. reptans.The model calculations were applied to each plot individually(n = 8).

The model consists of two parts: the first part describes how thedata from the individual leaves (genotype frequencies and leaf mor-phology) and the canopy structure data, giving the lamina area perm2, are combined to describe the abundance of the genotypes andtheir consequent morphological and physiological traits at them2-scale. The second part describes how the model calculates thephotosynthetic rates per unit mass (Pmass, mol g–1 day–1), which weconsider to be a measure of performance (see below).

LEAF MASS, LAMINA AREA AND NITROGEN DISTRIBUTION WITHIN THE CANOPY

We had two data sets with different dimensions: the frequency harvestdata, with genotype frequency as the number of leaves that werefound out of 100 sampled leaves per plot, and the canopy structuredata, giving the lamina area (m2) within a 5-cm layer. From thesedata, a model was constructed for each plot, with canopy layers of2.5 cm thickness, an intermediate between the canopy structure dataof 5 cm and the frequency data of individual leaves (positions in thecanopy measured to the nearest cm), resulting in nine canopy layers.To calculate the total lamina area within these model layers, thelamina area in each 5-cm layer from the canopy structure data wasequally divided by two. The individual leaves from the frequencyharvest were assigned to these model layers according to theirmeasured depth within the vegetation.

The total number of leaves of a given genotype i in layer j of a plotQLij was calculated as:

QLij = QL_cnsij × LAj / LA_cnsj eqn 4

where QL_cnsij is the number of leaves of that genotype sampledfrom the layer during the census of the frequency harvest, LAj thetotal lamina area including all genotypes in layer j estimated fromthe light distribution, and LA_cnsj the total lamina area sampledfrom this layer during the frequency harvest.

The average lamina area (Lavij, m2), lamina mass (g), petiole mass

(g) and total leaf mass (g m–2 ground layer, lamina mass + petiolemass) of a single leaf of genotype i in layer j was calculated from thefrequency data. Total lamina mass (Mlaij, g m–2 ground layer), totalpetiole mass (g m−2 ground layer) and total leaf mass (Mij, g m–2

ground layer) of genotype i in layer j were then found by multiplyingthe average mass values by the number of leaves QLij. Similarly, thetotal lamina area per genotype (Lij, m–2 m–2 ground layer) can befound using the average lamina area and the number of leaves.

Lij = QLij × Lavij eqn 5

The total lamina area in layer j (Lj) is the sum of the lamina area ofall genotypes within this layer.

The average nitrogen content per unit lamina mass of genotype iin layer j (Nij, mmol N g–1 lamina mass) was taken as the nitrogencontent (Nti, see genotype frequencies and leaf morphology in thecompetition experiment above) of the laminas of genotype i assignedto the model layer j. Nitrogen per unit lamina area of genotype i inlayer j (Nareaij, mmol N m−2) can be found as:

Nareaij = (Nij × Mlaij)/Lij eqn 6

CALCULATION OF THE CARBON GAIN IN THE CANOPY

Following Anten & Hirose (2001), the daily net photosynthetic rateper unit above-ground mass (Pmass, mol g–1 day–1) was used as a per-formance measure. This way, the carbon gain can be comparedbetween genotypes that differ in abundance, and therefore in mass.The Pmass of genotype i can be seen as the return in terms of dailynet photosynthetic rates over the whole canopy (Pi, mol day−1) fromthe total above-ground mass that the genotype has invested. Pmasshas been found to correlate with future growth (Hikosaka et al.2003; Van Kuijk et al. 2008). Pmass can be defined both at the levelof the entire canopy (canopy-Pmassj) and within each canopy layer(layer-Pmassij). We thus write:

canopy – Pmassi = Pi / Mi eqn 7

layer – Pmassij = Pij / Mij eqn 8

where Mj and Mij are the total mass of all leaves of genotype inpresent in either canopy or layer i within the canopy. Since there isno main stem, the invested mass per layer (Mij) is simply the totalweight of the laminas in that layer plus the whole weight of thepetioles (from lamina height to the ground) that supported them.

The daily net photosynthetic rate for genotype i in layer j (Pij) wasfound by integration over the day of the product of the net leafphotosynthesis within a one hour interval (Plij, μmol m–2 s–1) and thetotal lamina area (m2 m−2 ground layer) of genotype i in layer j (Lij):

eqn 9

Plij, in turn, was found using a non-rectangular hyperbola, thatdescribes the classical response curve of gross leaf photosynthesis inrelation to the light availability Ij, and the dark respiration Rdij

(μmol m–2 s–1), following (Marshal & Biscoe 1980):

eqn 10

Pmaxij (μmol m–2 s–1) is the light-saturated rate of gross photo-synthesis, that is, the asymptote of the curve. Pmaxij and Rdij werefound by substituting Nareai in eqns 3a and 3b by Nareaij.

P P L Tij Lij ij = �0

24

d

PIP I P I P I

Rij

ij j ij j ij j

dij max max max

.

=+( ) − +( ) −⎡

⎣⎢⎤⎦⎥ −

Φ Φ Φ2

0 5

4

2

θ

θ

512 P. J. Vermeulen et al.

© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 508–517

Φ is the quantum yield (mol mol–1), or the initial slope of the rela-tion between gross photosynthetic rate and light availability, and θ isthe curvature factor that describes the curve from the initial slopetowards the asymptote. Φ was taken to be 0.05 (Ehleringer & Björkman1977), while θ was assumed to be 0.8 (see Hirose et al. 1997).

Ij (μmol m−2 s−1) is the incident photon flux density (PPFD)absorbed by the laminas in layer j. It can be calculated assumingBeer’s law following (Hikosaka 2003):

eqn 11

where Io is the average PPFD above the canopy, Ljt the averagecumulative LAI above layer j, Lj the LAI of that layer, K the lightextinction coefficient and α the lamina absorbance, taken fromeqn 2. This calculation (Ljt + 0.5 × Lj) assumes that the light availa-bility of the laminas in a layer can be calculated based on the medianheight of that layer (e.g. for layer 0–2.5 cm that would be 1.25 cm).It further assumes that the optical and geometric characteristics ofleaves do not differ between genotypes. The distribution of lightabove the canopy (Io) over the day is assumed to follow a sinusoidalpattern (Hirose & Werger 1987):

eqn 12

where Ioo is the noon PPFD above the canopy set at 2000 μmol m–2 s–1

and T the average solar time within the 1-h interval (i.e. 06.30u,07.30u etc.).

In the results and discussion Pmassij and Pmassi will be referred toas layer P-mass and canopy –Pmass, respectively, to emphasize thedifferences between the two.

STATISTICS

A one way ancova was performed to test if genotypes differed intheir relation between Pmax and Narea and between Rd and Narea,using Pmax and Rd as dependent variables, genotype as randomvariable, and Narea as covariate. A two-way covariance analysis wasused to test if genotypes differed in their decrease of N content andNarea with increasing depth in the canopy, using nitrogen content Nper unit lamina mass and Narea as dependent variables, both geno-type and plot as random factors and canopy depth as covariate. Atwo-way covariance with layer–Pmass, net photosynthesis and totalmass as dependent variables, both genotype and plot as random factorsand layer as covariable, was used to test for differences betweengenotypes for the data calculated by the model. As genotypes A, B, andE occurred in too low a frequency over the whole depth of the canopy,they were left out of these two-way covariance analyses. Finally, atwo-way analysis of variance with both genotype and plot as ran-dom factors was performed to test for differences in canopy–Pmass.

Results

Figure 1 shows the frequency of leaves of the 10 genotypes ineach of the three vegetation layers after 5 years of competition.One genotype (genotype I) was most abundant in all threelayers. No leaves were found of genotype B. Of the othergenotypes some had a frequency close to or higher than theirinitial frequency of 10% (genotypes D, F and H), while theother genotypes had decreased in frequency after 5 years.

The averages of the morphological traits in the model weretaken from the data published in Vermeulen et al. (2008b).Only a short description is given here. The specific laminaarea (SLamA, m2 lamina area g–1 lamina mass) increased withdepth, and thus with age, in the canopy, as did the laminamass ratio (LamMR, g lamina mass g–1 total leaf mass). However,despite these differences, leaves at the same height capturedsimilar amounts of light per unit area (Φarea). Consequently,differences between genotypes for light interception per unitmass (Φmass = Φarea × LamAR) were also small. Differencesbetween genotypes in overall light interception per unit mass(e.g. on a whole canopy basis) depended on the relativeamount of leaves present at the top of the canopy. This wasbecause the Φmass values of leaves placed higher up werealways higher than those of leaves placed lower down. Thedominant genotype I had a relatively even distribution ofleaves in the three layers (Fig. 1), while some genotypes hadmore leaves at the top (and thus a high canopy Φmass). Con-sequently, the most abundant genotype did not capture morelight per unit total mass on a whole canopy basis than lessabundant genotypes.

PHOTOSYNTHETIC TRAITS IN MONOCULTURE

Both maximum photosynthesis (Pmax) and dark respiration(Rd) increased with increasing nitrogen content per unit area(Narea, Fig. 2). Genotypes differed in both the relationbetween Pmax and Narea and Rd and Narea (Table 1). Twoof the genotypes that strongly declined in abundance overtime, genotypes B and C, had a relatively high Rd per unitNarea. The dominant genotype I had both the lowest Pmaxand the lowest Rd values for a given Narea.

NITROGEN CONTENT IN COMPETIT ION EXPERIMENT

Overall, nitrogen content per unit mass (Nmass) was notstrongly related to the position in the canopy (Fig. 3a). Therelationship, however, differed between genotypes (signifi-cant genotype effect, Table 1). In some genotypes, includinggenotype I, Nmass decreased with depth in the canopy, but in

IKI K L L

jo jt j

exp ( . )

.=− + ×( )0 5

0 5α

I IT

T

I T T

o oo

o

sin( )

( )

( , )

=−⎡

⎣⎢

⎤

⎦⎥ ≤ <

= ≤ < ≤ <

2 612

6 18

0 0 6 18 24

π

Fig. 1. Average frequency per plot (percentage of total leaves + 1SE) of all genotypes in the three harvested layers: left, dotted bars:bottom layer; middle bars: middle layer and right, black bars: toplayer. Data are unpublished data from J.F. Stuefer.

Carbon gain in the competition for light 513

© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 508–517

most genotypes no such decrease with depth was found.Nitrogen per unit lamina area (Narea, mmol N m–2), however,decreased strongly with increasing vegetation depth (Fig. 3b)in all genotypes. Genotypes differed in Narea at a given depth(Table 1, among intercepts), but the slope of Narea vs. depthdid not differ between genotypes (Table 1; among slopes).The dominant genotype I had intermediate Narea values,while genotypes D and F that had also increased in frequencyhad similar or slightly lower Narea values. Plot did not interactwith any of these variables.

MODEL OUTCOME: CARBON GAIN IN THE COMPETIT ION EXPERIMENT

The model showed that the genotypes differed with respect totheir calculated total carbon gain per unit above-ground mass(canopy–Pmass), without there being a plot effect (Fig. 4).Genotypes G and H had high calculated canopy–Pmassvalues, while genotype I had canopy–Pmass values that wereintermediate between those of the other genotypes. Genotype

I had accumulated relatively high amounts of biomass in thelower layers, where little photosynthesis takes place, andmuch more so than the genotypes with high canopy–Pmass(Fig. 5a and b, significant genotype × layer interaction,Table 1).

Fig. 2. Relation between Pmax (a) and Rd with Narea (b) for the 10 genotypes in their monoculture.

Fig. 3. Relation between N content (percentage gN of total lamina mass) (a) and nitrogen per unit area (Narea, mmol N m–2) (b) with depthfor the different genotypes in the competition experiment. Lines represent linear regression lines of the genotypes based on log-transformed dataof all plots pooled together. Only the regression lines are given, as they are based on 788 points. Genotypes A, B and E are left out because oftheir low occurrence over the whole gradient. Symbols follow the legend of Fig. 2.

Fig. 4. Average genotype Pmass (mol g−1 day−1, + SE) for eachgenotype. P-values of anova analysis are given in top right corner.

514 P. J. Vermeulen et al.

© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 508–517

Carbon gain per unit above-ground mass in a layer (layer–Pmass) of all genotypes decreased strongly with increasingdepth in the canopy (Fig. 5c). This was due to the decreasinglight availability and the lower nitrogen content per unit area,resulting in lower maximum photosynthesis rates. The slopeof this Pmass–depth relationship differed between genotypes.Genotype I had intermediate layer–Pmass values comparedto other genotypes at the top of the vegetation, but had thehighest layer–Pmass values in the bottom layers, where leavesof most other genotypes that were present exhibited a negativecarbon gain (Fig. 5c, significant genotype × layer interaction,Table 1). Genotypes D and F, which also had increased infrequency, had high layer–Pmass values in the top layers ofthe canopy.

Discussion

The main question of this article was whether dominantgenotypes had traits that allow them to have high carbongain, as predicted by canopy models (Anten & Hirose 2001;Hikosaka et al. 2003), or by traits related to low light require-ments, as predicted by resource competition models (Tilman1988; Huisman & Weissing 1994). Our results support thelatter indicating that the dominance of one genotype was theresult of its low light requirements. However, our results alsosuggest that the persistence of several other genotypes may beexplained by their high carbon gain at the top, implying thatplants with these different strategies are able to coexist.

Plants which can position their leaves higher up in the canopyare considered to have a competitive advantage because theycan intercept more light and cast shade on shorter plantswhich have most of their leaves lower down in the canopy(Tilman 1988; Weiner 1990; Falster & Westoby 2003). Our

data, however, do not confirm this prediction. All genotypespresent in the experimental populations after 5 years couldreach the top of the vegetation, and no asymmetric competitionfor light between genotypes was found (Vermeulen et al. 2008b).Nonetheless, leaves placed in higher canopy layers had highernitrogen content per unit area (Narea) and captured morelight per unit mass, resulting in higher calculated photo-synthetic rates per unit above-ground mass (layer–Pmass) thanleaves positioned further down in the light gradient. Con-sequently, genotypes with a higher proportion of their leavespositioned at the top of the canopy showed higher values ofPmass over the whole canopy (canopy–Pmass). The mostdominant genotype had relatively many leaves at the bottomof the vegetation, explaining why its canopy–Pmass value waslower than that of some other, less abundant genotypes, whichhad relatively more upper leaves than bottom leaves. In addi-tion, the most abundant genotype had a low maximum rate ofphotosynthesis (Pmax) per Narea (Fig. 2a), and relativelylow levels of leaf respiration in monoculture (Fig. 2b). Bothof these traits can be seen as indicators of shade tolerance inphotosynthetic characteristics (Grime 1965; Givnish 1988).These findings suggest that the hypothesis that high carbongain rates at the top of the canopy confer dominance, derivedfrom game theoretical studies and canopy models (Givnish1982; Anten & Hirose 1998; Falster & Westoby 2003), doesnot apply to these multi-genotypic stands.

Resource competition models predict that plants with thelowest light requirements for positive growth will ultimatelywin the competition in well-mixed canopies (Huisman &Weissing 1994). Although the most dominant genotype didnot have the lowest nitrogen content per unit area (Narea), itdid have lower respiration rates per unit Narea. Consequently,in our study this genotype had the ability to attain positivelevels of carbon gain at lower light levels than its contenders.The lowest placed leaves of the dominant genotype thuscontributed to positive net total plant photosynthesis rates,whereas leaves of other genotypes placed at similar light levelscould not obtain positive carbon gain. So, the dominantgenotype had characteristics similar to those predicted byresource competition models, supporting the experimentaldata on competition between species pairs by others (i.e.Dybzinksi & Tilman 2007; Vojtech et al. 2007).

The reason why a genotype with rather shade-tolerantphysiological traits may have become dominant in this vege-tation may be due to the high leaf area that develops duringthe growth season. After winter, new leaves emerge from thetap roots and these are placed in high light conditions(Vermeulen 2008). Once the leaf lamina reaches high lightconditions its height growth stops. Soon thereafter, it isovertopped by younger leaves (Vermeulen et al. 2008a). As aconsequence, the amount of light available to a leaf stronglydecreases during its own life span, and the benefit of beingable to have high carbon gain in high light conditions arequickly lost. Therefore, leaves of genotypes with high maximumphotosynthetic rates may achieve lower net photosyntheticrates than genotypes with a lower Pmax when light levels havedropped, given that respiration (Rd) increases with Pmax as

Table 1. Results of two-way ancova. All values are F-values. Logand arcsinsqrt means data are log-transformed and arcsin-squareroot transformed, respectively. G × P means genotype and plotinteraction. ns: P > 0.05, *0.01 ≤ P < 0.05, **0.001 ≤ P < 0.01 and***P < 0.001

Dependent Covariate FactorAmong slopes

Among intercepts

N contentarcsinsqrt Depthns Genotype 2.645*Plot 1.218ns

G × P 1.520ns

Narealog Depth*** Genotype 1.600ns 3.508**Plot 0.553ns 2.429*G × P 1.073ns

Pmax Narea*** Genotype 1.082ns 3.446**Rd Narea*** Genotype 1.353ns 7.945***Pmass Layer*** Genotype 3.946***

Plot 2.336*G × P 0.805ns

Pdglog Layerns Genotype 0.635ns

Plot 4.365***G × P 0.981ns

Tdwlog Layer*** Genotype 1.650ns

Plot 5.365***G × P 0.917ns

Carbon gain in the competition for light 515

© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 508–517

was found here. This would support the notion that environ-ments characterized by strong and predictable declines inlight availability during the life span of a leaf may select forthe production of shade tolerant leaves to prevent a strongmismatch between structure and physiology of light-adaptedleaves and low-light levels experienced later on in time(Elemans 2005).

Also, the model calculations presented in Figs 4 and 5were made assuming clear sky conditions (noon-PPFD2000 μmol m–2 s–1). If we assume overcast conditions (e.g.noon-PPFD = 400 μmol m–2 s–1), genotype I was found tohave the highest Pmass of all genotypes (calculations notshown). Since weather conditions are frequently overcast inThe Netherlands, this emphasizes the benefit of havingrelatively shade tolerant leaf traits.

In addition, these differences in physiological traits mayalso lead to differences in leaf longevity. To optimize wholeplant carbon gain, leaves should be shed before their netphotosynthesis rates fall below zero (Boonman et al. 2006;Oikawa et al. 2006). High maximum photosynthetic rates arerelated to a high light compensation point (Kikuzawa 1995;Meziane & Shipley 2001; Selaya 2007), and thus genotypeswith a high Pmax may reach the point were net photosynthesisbecomes negative at higher light levels, leading to a shorterleaf life span. In tropical secondary forests, the longer leaf lifespan of long-lived pioneer species has been found to result ina higher light capture over the leaf life span than in short-lived

pioneer species, enabling these species to replace the latter inthe long run (Selaya et al. 2008). Although we have no data onthe differences in leaf turnover between the genotypes withinthis competition experiment, the average leaf life span isapproximately 1.5 months (Vermeulen 2008), indicating itplays an important role in the development of the canopy. Ifa low-light requirement (i.e. a low I*) is associated with alonger leaf life span, then this may allow the dominant gen-otype I to have higher life time carbon gains than genotypeswith high-light adapted and hence shorter-lived leaves. As ahigh leaf density can be formed quite quickly after the initialplanting of the ramets, and also develops quickly each year(Vermeulen 2008), such higher life-time carbon gains duringthe 5-years since the experiment was started will have beenadvantageous to genotype I.

However, not all other genotypes had declined in frequencyafter 5 years. This may be due to the fact that the dominantgenotype did not have the highest carbon gain per unit above-ground mass (layer–Pmass) throughout the whole canopy.Several of the genotypes that had persisted (i.e. D and F) hadhigher rates of photosynthesis per unit mass at the top of thecanopy. This was because of the greater layer-level photosyn-thetic nitrogen-use efficiency (PPNUE = Pmax/Narea). Incontrast, at the bottom of the canopy these genotypes had lowcalculated rates of photosynthesis, or even negative rates,because they had high respiration rates. For the dominantgenotype the reverse was true: it had lower rates of photosynthesis

Fig. 5. (a) Net total photosynthesis (mol m−2 ground surface day-1) and (b) total mass (g m−2 ground surface), the components of the averagePmass (c, mol g−1 day−1) of the genotypes in different layers of the canopy. Genotypes A, B and E are left out due to their low occurrence inthe plots.

516 P. J. Vermeulen et al.

© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 508–517

than the other persistent genotypes because its Pmax waslower, but it could reach a positive carbon gain at the bottomof the canopy due to low respiration rates. Our data thus sug-gest that the persistence of several genotypes occurredbecause due to their differences in photosynthetic traits theycould achieve higher carbon gains per unit mass than othersin different parts of the vegetation.

The persistence of genotypes with high Pmax traits may befacilitated by the seasonal dynamics of the light conditions,but also by the dynamics of the vegetation itself. Long periodsof high-light conditions, like in the month before the harvest,will benefit the genotypes with high Pmax traits, as they canachieve high Pmass rates, whereas constant low conditionswill benefit the dominant genotype. Also, before the onset ofwinter, all above-ground parts die off and the first leavesproduced in the following season are thus placed at high light.Genotypes with high maximum photosynthesis rates (Pmax)may then achieve a high carbon gain. Although these leavesare quickly shaded, each new leaf of such a genotype has thisinitial benefit. Because many leaves are formed (on averagenine over the initial 3 months of the growing season; Vermeulen2008), these initial high carbon gains at the top can add upand may result in a similar carbon gain over the whole seasonto the one the dominant genotype obtained, allowing theseleaves to coexist despite a shorter leaf life span.

Dynamic adjustments to changing light gradients of traitssuch as specific leaf area and nitrogen content per unit leafarea can enhance carbon gain of the whole plant (Hirose& Werger 1987; Anten & Werger 1996; Schieving & Poorter1999). Such plastic responses may prevent leaves from beingmaladapted to low light levels and potentially could allow asingle genotype to have the highest carbon gain in all layers ofthe canopy. Yet, an interaction was found for carbon gain perunit mass (layer–Pmass) between genotype and the canopylayer (Table 1). Genotypes with a high layer–Pmass at the topof the canopy tended to exhibit low values at the bottom, andno genotype had high layer–Pmass values throughout thewhole vegetation. This corresponds to structural limits to leafplasticity. When the leaf emerges from the canopy into highlight conditions, its area will become fixed (Pons & Pearcy1994) and the specific leaf area can then only change througha translocation of non-structural carbohydrates and enzymes(Shipley 2000). Leaves adjusted to high light conditions tendto be thicker with more cell layers (Terashima et al. 2001;Oguchi et al. 2003). The formation of high-light leaves thusrequires a substantial investment of carbon and nitrogen forthe production of cell walls (Onoda et al. 2004; Takashimaet al. 2004). Plants may not be able to recover and re-allocatethese structural components during light acclimation beforesenescence, and therefore high-light leaves may be less efficient interms of resource re-allocation. Structural constraints maythus ultimately limit the ability of plants to attain high carbongain rates at the top of the canopy and, at the same time, func-tionally adjust older leaves to low light levels of irradiancewhich they experience at the bottom of the canopy.

Our data are not suitable to prove persistence of severalgenotypes and stable coexistence over longer periods of time.

Also, below-ground processes such as competition for resources,mycorrhizal effects and interactions with pathogens mayaffect the competitive interactions between genotypes. Inaddition, pinpointing why and how some genotypes were(almost) excluded (such as genotypes A, B and C) has provento be difficult so far (see Vermeulen 2008). Nevertheless, ourdata suggest that the dynamics of within-canopy light gradientsdriven by plant growth and development may create enoughheterogeneity in space and time for multiple genotypes tocoexist. Apparently, the strong differences in growth formand resource distribution strategies that have been proposedas mechanisms for species coexistence in grasslands andtropical forests (Hirose & Werger 1995; Anten 2005) are notnecessarily required for coexistence in such simple communities.At the level of plant species a larger continuum of carbon andnutrient strategies ranging from short-lived leaves with highcarbon gain rates to long-lived leaves with slow metabolicrates has been found (Poorter 1994; Reich et al. 1998; Westobyet al. 2002; Wright et al. 2004; Poorter & Bongers 2006). Thissuggests that, at least in seasonal communities, the twostrategies may also allow for different species to coexist.

Acknowledgements

We thank Annemiek Smit-Tiekstra, Henri Noordman, Sander van Hal, BettyVerduyn and Sonja Huggers for technical assistance and Professor M.J.A.Werger for comments on the manuscript.

References

Aan, A., Hallik, L. & Kull, O. (2006) Photon flux partitioning among speciesalong a productivity gradient of an herbaceous plant community. Journal ofEcology, 94, 1143–1155.

Anten, N.P.R. & Hirose, T. (1998) Biomass allocation and light partitioningamong dominant and subordinate individuals in Xanthium canadensestands. Annals of Botany, 82, 665–673.

Anten, N.P.R. & Hirose, T. (1999) Interspecific differences in above-groundgrowth patterns result in spatial and temporal partitioning of light amongspecies in a tall-grass meadow. Journal of Ecology, 87, 583–597.

Anten, N.P.R. & Hirose, T. (2001) Limitations on photosynthesis of competingindividuals in stands and the consequences for canopy structure. Oecologia,129, 186–196.

Anten, N.P.R. & Hirose, T. (2003) Shoot structure, leaf physiology, anddaily carbon gain of plant species in a tallgrass meadow. Ecology, 84,955–968.

Anten, N.P.R. & Werger, M.J.A. (1996) Canopy structure and nitrogen distri-bution in dominant and subordinate plants in a dense stand of Amaranthusdubius L with a size hierarchy of individuals. Oecologia, 105, 30–37.

Anten, N.P.R. (2005) Optimal photosynthetic characteristics of individualplants in vegetation stands and implications for species coexistence. Annalsof Botany, 95, 495–506.

Boonman, A., Anten, N.P.R., Dueck, T.A., Jordi, W.J.R.M., Van der Werf, A.,Voesenek, L.A.C.J. & Pons, T.L. (2006) Functional significance of shade-induced leaf senescence in dense canopies: An experimental test usingtransgenic tobacco. American Naturalist, 168, 597–607.

Caemmerer, S.V. & Farquhar, G.D. (1981) Some relationships betweenbiochemistry of photosynthesis and gas exchange of leaves. Planta, 153,376–387.

Corré, W.J. (1983) Growth and morphogenesis of sun and shade plants. I. Theinfluence of light intensity. Acta Botanica Neerlandica, 32, 49–62.

Dybzinski, R. & Tilman, D. (2007) Resource use patterns predict long-termoutcomes of plant competition for nutrients and light. American naturalist,170, 318.

Ehleringer, J. & Björkman, O. (1977) Quantum yields for CO2 uptake in C3 andC4 plants: dependence on temperature, CO2 and O2 concentration. PlantPhysiology, 59, 86–90.

Carbon gain in the competition for light 517

© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 508–517

Elemans, M. (2005) Plant traits in forest understory – a modeling study. PhDthesis, Utrecht University, Utrecht.

Evans, J.R. (1993) Photosynthesis acclimation and nitrogen partitioningwithin a lucerne canopy. II. Stability through time and comparison with atheoretical optimum. Australian Journal of Plant Physiology, 20, 69–82.

Falster, D.S. & Westoby, M. (2003) Plant height and evolutionary games.Trends in Ecology & Evolution, 18, 337–343.

Givnish, T.J. (1982) On the adaptive significance of leaf height in forest herbs.American naturalist, 120, 353–381.

Givnish, T.J. (1988) Adaptation to sun and shade: a whole-plant perspective.Functional Plant Biology, 15, 63–92.

Givnish, T.J. (1995) Plant stems: biomechanical adaptation for energy captureand influence on species distribution. Plant Stems: Physiology and FunctionalMorphology (ed. B.L. Gartner), pp. 3–49. Academic press, San Diego.

Goudriaan, J. (1988) The bare bones of leaf angle distribution in radiationmodels for canopy photosynthesis and energy exchange. Agricultural andForest Meteorology, 43, 155–169.

Grime, J.P. (1965) Shade tolerance in flowering plants. Nature, 208, 161–163.Hikosaka, K. (2003) A model of dynamics of leaves and nitrogen in a plant

canopy: An integration of canopy photosynthesis, leaf life span, andnitrogen use efficiency. American Naturalist, 162, 149–164.

Hikosaka, K., Sudoh, S. & Hirose, T. (1999) Light acquisition and use by indi-viduals competing in a dense stand of an annual herb, Xanthium canadense.Oecologia, 118, 388–396.

Hikosaka, K., Yamano, T., Nagashima, H. & Hirose, T. (2003) Light-acquisitionand use of individuals as influenced by elevated CO2 in even-aged mono-specific stands of Chenopodium album. Functional Ecology, 17, 786–795.

Hirose, T. & Werger, M.J.A. (1987) Nitrogen use efficiency in instantaneousand daily photosynthesis of leaves in the canopy of Solidago altissima stand.Physiologia Plantarum, 70, 215–222.

Hirose, T. & Werger, M.J.A. (1995) Canopy structure and photon fluxpartitioning among species in a herbaceous plant community. Ecology,76, 466–474.

Hirose, T. (2005) Development of the Monsi-Saeki theory on canopy structureand function. Annals of Botany, 95, 483–494.

Hirose, T., Ackerly, D.D., Traw, M.B., Ramseier, D. & Bazzaz, F.A. (1997) CO2

elevation, canopy photosynthesis, and optimal leaf area index. Ecology, 78,2339–2350.

Huber, H. (1995) Growth form and plasticity of the hybrid Potentilla anglicaand its two parent species. Abstracta Botanica, 19, 61–73.

Huber, H. (1996) Plasticity of internodes and petioles in prostrate and erectPotentilla species. Functional Ecology, 10, 401–409.

Huisman, J. & Weissing, F.J. (1994) Light-limited growth and competition forlight in well-mixed aquatic environments: an elementary model. Ecology, 75,507–520.

Huisman, J., Grover, J.P., Van der Wal, R. & Van Andel, J. (1999) Competi-tion for light, plant-species replacement and herbivore abundance alongproductivity gradients. Herbivores: between Plants and Predators (eds H.Olff, V.K. Brown & R.H. Drent), pp. 239–269. Blackwell Science, London.

Inskeep, W.P. & Bloom, P.R. (1985) Extinction coefficients of chlorophyll a andb in N,N-dimethylformamide and 80% acetone. Plant Physiology, 77, 483–485.

Kikuzawa, K. (1995) The basis for variation in leaf longevity of plants. PlantEcology, 121, 89–100.

Marshal, B. & Biscoe, P.V. (1980) A model for C3 leaves describing the depend-ence of net photosynthesis on irrandiance. Journal of Experimental Biology,31, 29–39.

Meziane, D. & Shipley, B. (2001) Direct and indirect relationships betweenspecific leaf area, leaf nitrogen and leaf gas exchange. Effects of irradianceand nutrient supply. Annals of Botany, 88, 915–927.

Monsi, M. & Saeki, T. (1953) Über den lichtfaktor in den pflanzengesellschaftenund seine bedeutung für die stoffproduktion. Japanese Journal of Botany, 15,60–82.

Oguchi, R., Hikosaka, K. & Hirose, T. (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant Cell and Environment, 26,505–512.

Oikawa, S., Hikosaka, K. & Hirose, T. (2006) Leaf lifespan and lifetime carbonbalance of individual leaves in a stand of an annual herb, Xanthiumcanadense. New Phytologist, 172, 104–116.

Onoda, Y., Hikosaka, K. & Hirose, T. (2004) Allocation of nitrogen to cell wallsdecreases photosynthetic nitrogen-use efficiency. Functional Ecology, 18,419–425.

Pons, T.L. & Pearcy, R.W. (1994) Nitrogen Reallocation and Photosynthetic

Acclimation in Response to Partial Shading in Soybean Plants. PhysiologiaPlantarum, 92, 636–644.

Pons, T.L. & Welschen, R.A.M. (2002) Overestimation of respiration rates incommercially available clamp-on leaf chambers. Complications with meas-urement of net photosynthesis. Plant Cell and Environment, 25, 1367–1372.

Poorter, H. (1994) Construction cost and payback time of biomass: a wholeplant perspective. A Whole Plant Perspective on Carbon-Nitrogen Inter-actions (eds E. Roy & E. Garnier), pp. 111–127. SPB Academic, The Hague.

Poorter, L. & Bongers, F. (2006) Leaf traits are good predictors of plant per-formance across 53 rain forest species. Ecology, 87, 1733–1743.

Reich, P.B., Walters, M.B., Ellsworth, D.S., Vose, J.M., Volin, J.C., Gresham, C.& Bowman, W.D. (1998) Relationships of leaf dark respiration to leaf nitrogen,specific leaf area and leaf life-span: a test across biomes and functionalgroups. Oecologia, 114, 471–482.

Schieving, F. & Poorter, H. (1999) Carbon gain in a multispecies canopy: therole of specific leaf area and photosynthetic nitrogen-use efficiency in thetragedy of the commons. New Phytologist, 143, 201–211.

Schieving, F. (1998) Plato’s Plant. Utrecht University, Backhuys, Leiden.Selaya, N.G. (2007) Sprinting, climbing and persisting; light interception and carbon

gain in a secondary tropical forest succession. PhD thesis, Utrecht University,Utrecht.

Selaya, N.G., Oomen, R.J., Netten, J.J.C., Werger, M.J.A. & Anten, N.P.R.(2008) Biomass allocation and leaf life span in relation to light interceptionby tropical forest plants during the first years of secondary succession.Journal of Ecology, 96, 1211–1221.

Shipley, B. (2000) Plasticity in relative growth rate and its components followinga change in irradiance. Plant Cell and Environment, 23, 1207–1216.

Takashima, T., Hikosaka, K. & Hirose, T. (2004) Photsynthesis or persistence:nitrogen allocation in leaves of evergreen and deciduous Quercus species.Plant Cell and Environment, 27, 1047–1054.

Terashima, I., Miyazawa, S.I. & Hanba, Y.T. (2001) Why are sun leaves thickerthan shade leaves? Consideration based on analyses of CO2 diffusion in theleaf. Journal of Plant Research, 114, 93–105.

Tilman, D. (1982) Resource Competition and Community Structure. PrincetonUniversity Press, Princetion, New Jersey, USA.

Tilman, D. (1988) Plant Strategies and the Dynamics and Structure of PlantCommunities. Princeton University Press, Princeton, New Jersey, USA.

Van der Meijden, R. (1996) Heukels’ Flora van Nederland. Wolters-Noordhoff,Groningen, the Netherlands.

van Kuijk, M., Anten, N.P.R., Oomen, R.J., van Bentum, D.W. & Werger,M.J.A. (2008) The limited importance of size-asymmetric light competitionand growth of pioneer species in early secondary forest succession in Vietnam.Oecologia, 157, 1–12.

Vermeulen, P.J. (2008) Plastic responses in the competition for light among gen-otypes of a stoloniferous plant. PhD thesis, Utrecht University, Utrecht.

Vermeulen, P.J., Anten, N.P.R., Schieving, F., Werger, M.J.A. & During, H.J.(2008a) Height convergence in response to neighbour growth: genotypicdifferences in the stoloniferous plant Potentilla reptans. New Phytologist,177, 688–697.

Vermeulen, P.J., Stuefer, J.F., During, H.J. & Anten, N.P.R. (2008b) Leaf invest-ment and light partitioning among leaves of different genotypes of the clonalplant Potentilla reptans in dense stands after five years of competition.Annals of Botany 102, 935–943.

Vojtech, E., Turnbull, L.A. & Hector, A. (2007) Differences in light inter-ception in grass monocultures predict short-term competitive outcomesunder productive conditions. PLoS ONE, 2, e499.

Weiner, J. (1990) Asymmetric competition in plant-populations. Trends inEcology and Evolution, 5, 360–364.

Weissing, F.J. & Huisman, J. (1994) Growth and Competition in A LightGradient. Journal of Theoretical Biology, 168, 323–336.

Werger, M.J.A., Hirose, T., During, H.J., Heil, G.W., Hikosaka, K., Ito, T.,Nachinshonhor, U.G., Nagamatsu, D., Shibasaki, K., Takatsuki, S., vanRheenen, J.W. & Anten, N.P.R. (2002) Light partitioning among species andspecies replacement in early successional grasslands. Journal of VegetationScience, 13, 615–626.

Westoby, M., Falster, D.S., Moles, A.T., Vesk, P.A. & Wright, I.J. (2002) Plantecological strategies: some leading dimensions of variation between species.Annual Review of Ecology and Systematics, 33, 125–159.

Wright, I.J., Reich, P.B., Westoby, M., Ackerly, D.D., Baruch, Z., Bongers, F.et al. (2004) The worldwide leaf economics spectrum. Nature, 428, 821–827.

Received 3 September 2008; accepted 11 February 2009Handling Editor: Stephen Bonser