ANNE AAN*, LEA HALLIK* and OLEVI KULL* Journal of Ecology (2006) 94, doi: /j x

Transcription

1 Journal of Ecology 2006 Photon flux partitioning among species along a Blackwell Publishing Ltd productivity gradient of an herbaceous plant community ANNE AAN*, LEA HALLIK* and OLEVI KULL* *Institute of Botany and Ecology, University of Tartu, Lai 40, Tartu, Estonia, and Institute of Ecology, Riia 181, Tartu, Estonia Summary 1 We studied light partitioning among species along the natural productivity gradient of herbaceous vegetation with an above-ground dry mass of g m 2. The aim was to investigate how the light capturing ability per above-ground biomass and leaf nitrogen changes in an entire community and to reveal whether different species respond similarly to changes in soil conditions and competition. 2 Species becoming dominant at high soil resources have intrinsically low leaf area ratios (LAR) and lower tissue nitrogen concentration, and hence relatively high nitrogen use efficiency. These traits lead to dominance when soil resources allow rapid growth so that benefits arising from the ability to locate leaves above neighbours and thereby increasing asymmetry of competition, become more crucial. 3 In contrast to our expectations, above-ground efficiency of nitrogen use on the community level (anue) increased along the productivity gradient. Species level nitrogen use efficiency was unaffected by variation in site productivity; the increase in community anue was solely as a consequence of changes in species composition. 4 Light absorption per unit of above-ground mass, M, declined significantly at the community level and also in most species, indicating that light use efficiency increased with increased site productivity and LAI. 5 Light absorption per unit of leaf nitrogen, N, as an indicator of the ratio NUE/LUE showed no clear pattern on the community level because both NUE and LUE tend to increase with increased productivity. At the species level, N tends to decrease because NUE did not change with stand productivity. 6 Some subordinate species responded by enlarging their LAR to increased competition. Additionally, these species were the most responsive in their leaf chlorophyll/nitrogen ratio to changes in light conditions, which shows that physiological plasticity is important for species that are unable to compete for light with the ability to position their leaves above those of other species. 7 This study shows how plasticity in above-ground growth pattern and nitrogen allocation differs between species with respect to increased soil fertility and competition, leading to distinctive strategies of survival. Light partitioning analysis reveals that increased competition for light, resulting in changes in species composition, is the key factor that leads to decoupling of species and community level acclimation. Key-words: canopy, coexistence, competition, dominance, leaf area ratio, light partitioning, light use efficiency, nitrogen, plasticity, species composition Journal of Ecology (2006) doi: /j x Ecological Society Introduction An understanding of the relationship between biomass allocation, light interception and competition is essential Correspondence: Olevi Kull (tel ; fax ; olevi.kull@ut.ee). to describe the contribution of individual plant species to vegetation structure (Anten & Hirose 1998). It is essential because spatially and temporally heterogeneous distributions of resources and competitors have lead to diverse plant species, each with a unique set of traits with which to survive in particular communities. Diversity of plant traits has evolved to cope with

2 1144 A. Aan, L. Hallik & O. Kull above-ground competition that is most strongly related to capture and use of light resources. Due to its unidirectionality, plants have two options: (i) to grow taller or (ii) to grow in shade. Realization of either option leads to a unique set of particular traits and adaptations. Hirose & Werger (1994, 1995) proposed the concept of light partitioning within plant canopies by evaluating light capture based on leaf nitrogen and plant aboveground biomass expressed as M (light capture per unit of biomass) and N (light capture per unit of leaf nitrogen) as indices of plant efficiency to acquire resources. They concluded that light absorption per unit of nitrogen in an herbaceous community was unrelated to species position (dominant, subordinate) within the community. Their study also indicated that the efficiency of above-ground biomass in absorbing light is a trade-off between limited growth and remaining in shade, and enhanced growth resulting in well-illuminated leaves with reduced LAR (ratio of leaf area to above-ground biomass) and consequently reduced efficiency (Hirose & Werger 1995). Structural properties of individuals and stands are important in predicting patterns of light distribution among leaves, individuals and species. However, at least in some circumstances, interspecific differences in carbon gain per unit mass are more closely associated with differences in leaf physiology than with structural differences that determine light capture (Anten & Hirose 2003). Most analyses of N and M have been performed within single stands; a few studies (e.g. Anten & Hirose 1998, 2001; Werger et al. 2002) have addressed changes in light partitioning in stands with different productivity or different positions in a successional series. These studies suggest that plants react differently to changes in competition resulting from increased stand productivity and, for instance, species displacement can be described by differences in inherent constraints on the above-ground architecture of various species. However, no study has compared N and M between species along a productivity gradient. Interpretation of N and M may differ from that of their original use. For instance, high M may be viewed as efficient light capture by plant biomass (Hirose & Werger 1995), and therefore one would expect that if competition intensifies along a productivity gradient, M should increase inasmuch as competitive pressure should favour high light harvesting efficiency. However, if above-ground biomass is seen as a time integral of production, high M can also result from low light use efficiency (LUE, productivity per unit of absorbed light). Often LUE increases along a productivity gradient (Sinclair & Shiraiwa 1993; Kull 2002), and consequently M should decrease. Such a duality in interpretation is also possible with N, which was interpreted originally as an indicator of nitrogen use efficiency (NUE, productivity per unit of plant nitrogen) (Hirose & Werger 1994). Kull et al. (1995) hypothesized that total nitrogen in a canopy is limited because the benefit from increased production does not compensate for the cost of nitrogen needed to construct increasing foliage. Model calculations based on parameters measured for woody species with different shade tolerance have confirmed that this hypothesis can account for LAI distribution in layered tree canopies (Kull & Jarvis 1995; Kull & Kruijt 1999). If this hypothesis is valid then N can be interpreted as the energetic cost of maintaining nitrogen in foliage and, consequently, N should decrease when nitrogen availability in soil increases and the plant requires less energy to acquire nitrogen. Additionally, several studies have revealed that NUE decreases (Vitousek 1982) and LUE increases (Kull & Tulva 2002; Gordillo et al. 2003) when canopy LAI and/or soil fertility increases. Both of these trends should lead to a decrease in N inasmuch as N = NUE/LUE. However, increases in N can be expected when LAR declines because the relative cost of supporting tissue increases. This decline is expected in areas of high productivity with high biomass but relatively accessible soil resources. Consequently, it is very difficult to hypothesize what would happen with N when soil fertility increases. The aim of our study is to apply the approach of light partitioning to an herbaceous canopy along a natural productivity gradient and to examine how light capturing abilities of different species change relative to each other. We investigated how light capturing ability of an entire community changes and whether different species respond similarly to changes in soil conditions and competition, i.e. how much of the community level variation is related to universal responses of different species, and how much results from changes in species composition. Materials and methods Ten 1 1 m 2 plots were established in old grassland near Tartu, Estonia, where all agricultural activities had been abandoned 5 years previously. The plots were located along the slope of a small hillock that effectively produced a gradient in soil conditions, particularly in the depth of the humus horizon (Table 1). All measurements were made in July LIGHT AND LEAF ANGLE MEASUREMENTS All plots were marked and the canopy divided into three to five layers, each cm high. The actual profile of PAR radiation was measured with LI-185B quantum meter equipped with LI-191SB line quantum sensor (Li-Cor, Lincoln, Nebraska, USA). A series of measurements were made above the canopy and below each layer, with five readings per layer. Each series was repeated several times during two consecutive days. At least one series per plot was measured in overcast conditions and one series before sunrise to measure only diffusive radiation. Leaf angles were measured with a protractor in all plots and layers, for all major

3 1145 Light partitioning along productivity gradient Table 1 The general characteristics of the plots used in this investigation Plot No. Depth of humus horizon (cm) Soil moisture (%) Bulk density (g cm 3 ) Nitrogen stock (kg m 2 ) Number of plant species Total above-ground dry mass (g m 2 ) species. In each plot, at least five measurements were taken per species in each layer. DETERMINATION OF LAI AND BIOMASS The canopy was harvested within a m area in the centre of the sample plot by three to five vertical layers depending on canopy height. The leaves and stems (+ inflorescences) of each species were collected and sorted. Fresh mass of each fraction was measured immediately following sorting and the dry mass was determined after drying at 80 C for 3 days. A sample of leaves from each species in all harvested canopy layers was taken for leaf area determination. Images of fresh leaves were digitized and the area calculated with an in-house computer program. The leaves were then dried separately to calculate leaf mass to area ratio (LMA). Dry mass data of leaves from each sampled canopy layer were then divided to LMA to determine the total leaf area of every species in each canopy layer. CHLOROPHYLL AND NITROGEN DETERMINATION Samples were taken from all species that had sufficient foliage within a sampled canopy layer. Chlorophyll concentration was determined in 80% aqueous acetone with a PS2000 spectrometer (Ocean Optics, Dunedin, Florida, USA) following the method of Porra et al. (1989). Nitrogen content was measured by the Kjeldahl method with a Kjeltec Auto 1030 analyser. SOIL SAMPLING One composite sample of soil from the A horizon was taken for analysis from each sample plot. Additionally, a small pit was excavated to measure the thickness of the A horizon and to take samples for bulk density analysis. The soil moisture content was determined as the difference in weight between fresh and dried samples; total N was determined by the Kjeldahl method. LIGHT ABSORPTION PARTITIONING BETWEEN SPECIES Light absorption was calculated using a modified approach similar to Anten & Hirose (1999). The modifications related to the leaf angle distribution and the spatial heterogeneity of the canopy, and accounted for light absorbed by non-leaf structures (e.g. stems, flowers, inflorescence). The total light absorbed by leaves for each species was calculated as: j = i ij eqn 1 where ij is the light absorbed by the foliage of shoots of species j in the ith canopy layer (counted from the top to the bottom). Each value of ij consists of two components: = + ij dr, ij df, ij eqn 2 where dr,ij and df,ij are the amounts of direct and diffuse light absorbed by foliage class ij, respectively. Direct light, dr,ij was determined as: dr, ij = j K 05 dr, ijαij fij 05. dr, i Kdr, ijαij fij eqn 3 where dr,i is the direct light absorbed by layer i, f ij the LAI (one-sided leaf area per unit ground area) of foliage class ij, and K dr,ij and α ij the extinction coefficient of black non-scattering leaves for direct light and the leaf absorbance of class ij, respectively. The 0.5 power in term α ij was incorporated to model the effects of leaf reflectance and transmittance on the light climate in the canopy (Goudriaan 1977). dr,i was quantified as:. = I exp 05 1 ΩK α f j dr, i dr, i i drij, ij ij eqn 4

4 1146 A. Aan, L. Hallik & O. Kull where I dr,i is the direct PFD at the top of layer i (the difference between the light absorbed by layer i 1 and the PFD at the top of that layer). Ω i is a clumping factor that depends on the spatial arrangement of foliar elements in layer i. Absorption of diffuse light by plants was calculated for each sky elevation angle separately with equations 1 4. The total diffuse light absorbed by foliage class ij was thus calculated as: = df, ij df, ijk k eqn 5 where df,ijk is the absorbed diffuse light originating from sky zone k determined as: df, ijk 05. Kdf, ijk ij fij 05. df, ik Kdf, ijkαij fij j = α eqn 6 where df,ik is the amount of diffuse light originating from sky zone k absorbed by layer i, and K df,ijk is the extinction coefficient of black non-scattering leaves of plant class ij for this radiation component. df,ik is quantified as:. = I exp 05 1 ΩK α f j df, ik df, ik i df, ijk ij ij eqn 7 where I df,ik is the diffuse PFD from the kth sky zone at the top of the layer i (the difference between the PFD absorbed by layer i 1 and the PFD at the top of that layer). The values of I df,k above the canopy were calculated assuming a standard overcast sky (Goudriaan 1977). EXTINCTION COEFFICIENTS, LEAF ABSORBANCE AND CLUMPING FACTOR The extinction coefficient for direct light, K dr,ij, for a given species in layer i was calculated as a function of solar elevation angle θ and assuming an ellipsoidal leaf angle distribution following Campbell (1986): (cos θ( x 1) + 1) K = cos θ( x ( x ) ) eqn 8 where x is the ratio of vertical to horizontal projection of a representative volume of foliage. Using the results from numerical integration of Campbell s ellipsoidal angle distribution function, Wang & Jarvis (1988) derived an empirical equation relating x to the canopy mean leaf inclination angle Θ: Θ if Θ Θ x = Θ if Θ < Θ eqn 9 The extinction coefficients for diffuse light K df,ijk were calculated similarly, with the solar elevation angle being replaced by sky zone elevation angles. Leaf absorbance (α ij ) was calculated following Evans (1993): α ij chlij = chl + 76 ij eqn 10 where chl ij is the average chlorophyll content per unit leaf area (µmol m 2 ) for leaves of species j in layer i. The clumping factor Ω i was determined for each layer by regressing calculated absorbed diffuse light (using eqn 7) against measured layer absorbance in diffuse light conditions (overcast or before sunrise). ANALYSIS The total light absorbed per unit of above-ground plant mass for each species was calculated as: M = / M eqn 11 where was calculated according to eqn 1 and M is above-ground dry mass of the species. The total light absorbed per unit of leaf nitrogen for each species was calculated as: N = /N L eqn 12 where N L is the total leaf nitrogen of the species. Leaf area ratio was calculated as: LAR = S L / M eqn 13 where S L is the total leaf area and M is above-ground dry mass of the species. An estimate of above-ground nitrogen use efficiency was calculated as: anue =M/ N L eqn 14 where M is above-ground dry mass and N L the total leaf nitrogen of the species. Asymmetry of competition, B, was calculated from the equation (Anten & Hirose 1998): B j = cm ( j ) eqn 15 where j is the total absorbed light and M j the total above-ground dry mass of the species j, and c is a constant. The value of B was calculated for each plot from simple linear regression of log-transformed values of j and M j. Statistical analysis was performed using Statistica software version 5.5 (StatSoft Inc., Tulsa, Oklahoma, USA). Pearsons s correlation was calculated in analysis of soil and vegetation parameters, and the general linear models procedure was used for the regression analysis. No data trans-formation was necessary for these calculations.

5 1147 Light partitioning along productivity gradient Results The low angle slope (approximately 5 ) resulted in a clear gradient in soil conditions, the most apparent of which is the thickness of the humus horizon (Table 1). Total soil nitrogen correlates less strongly with depth (r = 0.515, P < 0.128) than with the nitrogen fraction in the A horizon (r = 0.853, P < 0.002). This soil profile resulted in a gradient in above-ground biomass from 150 g up to 490 g [DW] m 2 (Table 1). It is notable that the correlation between the thickness of the A horizon and LAI (r = 0.897, P < 0.001; Fig. 1) is greater than the correlation between the A horizon thickness and above-ground biomass (r = 0.737, P < 0.015). There was no clear pattern in species diversity along the productivity gradient (Table 1). Six species, Achillea millefolium L., Cirsium arvense (L.) Scop., Taraxacum officinale Weber ex Wigg., Dactylis glomerata L., Festuca pratensis Huds. and Phleum pratense L., produced most of the biomass (65 95%) in all plots and were present along the entire gradient (Fig. 1). These six species were examined in more detail. Other species were present in a few plots but formed only a small proportion of the biomass and were pooled together in our analysis. Despite minor changes in species composition, clear differences in species biomass proportions were identified along the gradient. Grasses (mainly D. glomerata and P. pratense) formed less than Fig. 1 (a) Relationship between thickness of soil humus horizon and one-sided leaf area index of the stand at the date of sampling (R 2 = 0.781; P < 0.001; intercept n.s.) and (b) share of major species in total above-ground biomass of the stand. The studied plots are ordered into increasing sequence according to the total above-ground biomass. Species: (1) Achillea millefoilium L., (2) Cirsium arvense (L.) Scop., (3) Taraxacum officinale Weber ex Wigg., (4) Dactylis glomerata L., (5) Festuca pratensis Huds., (6) Phleum pratense L. and (7) all other species pooled together.

6 1148 A. Aan, L. Hallik & O. Kull Fig. 2 Asymmetry of competition (parameter B in eqn 15) as a function of the stand LAI. Values of B > 1.0 show that larger species acquire a disproportionate amount of light relative to their size compared to smaller species. 50% of the stand biomass at the less productive part of the gradient and increased to more than 80% in the more productive areas of the gradient (Fig. 1). Forbs (A. millefolium, C. arvense and T. officinale) had a biomass maximum in the middle of the gradient and declined in more productive sections due to competition with grasses. Grass species shared a very similar niche in the community because the occasional increase in one species biomass was often accompanied by a decrease in another species, e.g. D. glomerata and P. pratense in plot 5 or D. glomerata and F. pratensis in plot 9 (Fig. 1). PPFD partitioning between species within a canopy depended strongly on the relative biomass of the species in the stand. However, a relative gain in light absorption of a species from increasing biomass, depended clearly on site productivity and total LAI because the asymmetry parameter B increased with increasing stand total LAI (Fig. 2). This implies that asymmetry of competition increased with increasing stand biomass, inasmuch as species benefit from the relative increase in domination with disproportionally higher light capturing ability. Species differed in their range of LAR, N, M and anue (Fig. 3). Grasses tended to have intrinsically low LAR and relatively high N and anue, compared with forb species, especially A. millefolium and T. officinale. Mean values of M among species showed no clear pattern. For instance, the mean and variance of M among grasses varied greatly (Fig. 3). As expected, a species level comparison showed a weak, statistically insignificant, negative relationship between LAR and N. There was also a general positive relationship between anue and N ; however, species specificity of M strongly influenced the scatter of data points (Fig. 3). Total canopy increased with increasing productivity, but canopy level M decreased substantially with increasing stand biomass (Fig. 4). This effect was related at least partially to the increasing cost of supporting tissue, as the average LAR of a plot decreased. Two nitrogen-related parameters, N and anue, exhibited unexpected behaviour on the stand level. In contrast to expectations, anue revealed a clear increasing trend with increased soil fertility (Fig. 4). Although N decreased with increasing stand biomass in the less productive section of the gradient, the overall relationship revealed no clear trend (Fig. 4). The behaviour of N at the stand level resulted mainly from changes in the relative share of species with different speciesspecific values of N. Some species (A. millefolium, T. officinale and F. pratensis) had no change in N with increased soil fertility, whereas light capture per unit of foliar nitrogen decreased for other species (C. arvense, D. glomerata) (Fig. 5). Therefore, the stand level increase in N in the more productive section of the gradient was caused mainly by the increased domination of D. glomerata and P. pratense with relatively high average values of N. The same explanation was valid for stand level variation in anue because there was almost no dependence of anue on soil fertility for any species (except A. millefolium with a significant decrease in anue; Fig. 6). Similarly, light capture per unit of mass declined noticeably along the gradient for two species with smaller declines for the other species (Fig. 7). However, because the average M of two grasses, P. pratense and F. pratensis, was less than in the other species, a change in relative abundance with increased productivity amplified the decreasing trend of M on the stand level (Fig. 4). Species showed contrasting morphological responses to changes in soil fertility. The LAR of all grasses decreased with increased productivity, although the only significant decrease was for P. pratense. In contrast, LAR increased for two forb species, A. millefolium and T. officinale (Fig. 8). Both species, which increased their LAR in response to intensified competition, showed the most plastic response in leaf Chl/N ratio to changes in incident light (Fig. 9). Additionally, both species had relatively high leaf nitrogen levels in the lower canopy layer and the highest Chl/N ratios, indicating

7 1149 Light partitioning along productivity gradient Fig. 3 (a) Species average values (± SD) of N and LAR (R 2 = 0.304; P = n.s.) and N and (b) anue (overall R 2 = 0.463; P < 0.056; intercept n.s.). Lines (b) represent relationship between N and anue at constant values of M. Species numbers as in Fig. 1. their success in forming robust photosynthetic apparatus under low light conditions and probably their unlikely expenditure of nitrogen on structures other than photosynthetic apparatus. Discussion WHAT DO anue, M AND N SHOW? Using the inverse of tissue N concentration as a rough estimate of NUE is a common practice (Chapin 1980; Shaver & Melillo 1984). However, a more precise analysis requires a distinction between the two components of NUE: (i) nitrogen productivity, and (ii) the mean residence time of N (Berendse & Aerts 1987). In our study, vegetation was harvested at the peak time of seasonal biomass production; the value of anue should reflect nitrogen productivity. Systematic differences in rootshoot allocation or tissue turnover, as well as in growth dynamics, may affect the relationship between anue and actual nitrogen productivity. This ambiguity should be considered when interpreting the results; however, it remains impossible to measure all the necessary parameters to determine the true NUE at a stand level without loosing the integrity of the plant stand. Our study shows that species-specific anue depends neither on site productivity nor on competitive pressure even when the allocation pattern (measured as LAR) changes. This contradicts the litter fall-based estimates of NUE in several studies, suggesting that nutrient use efficiency increases monotonically when nutrient availability declines (Vitousek 1982; Shaver & Melillo 1984). However, this notion has been challenged on several grounds (Pastor & Bridgham 1999). A detailed analysis of the components of NUE in a study with 14 plant species growing in two contrasting habitat types, has shown that above-ground nutrient use efficiency, was unaffected by habitat (Eckstein & Karlsson 1997). The calculation of light absorption based on plant biomass, an approach introduced by Hirose & Werger (1995), has led to an understanding of resource capture partitioning among individuals or species in a stand. We emphasize that M is not predicted solely by morphological traits and spatial arrangement of leaves but strongly influenced by light use efficiency of the plant. It is apparent that when light is efficiently converted into biomass then light absorption by plant mass should decline even when available light resources do not change. In our opinion this should be considered when interpreting light partitioning data. We found M

8 1150 A. Aan, L. Hallik & O. Kull estimates, N equals the ratio of instantaneous NUE/ LUE. Consequently, N can be used as a surrogate measure for NUE only in circumstances when LUE is unchanging. This assumption is certainly not true for plant stands along a productivity gradient if LAI changes. When comparing means of anue, LAR, N and M for species (Fig. 3), a positive relationship between anue and N exists, although it varies as M changes. However, within species, patterns in N along productivity gradients (Fig. 5) differ substantially from that of anue (Fig. 6). This uncoupling is caused by the systematic trend of LUE along the gradient. Assuming that N represents the energetic cost of keeping foliar nitrogen functional, it appears that at a species level, the decreased cost of nitrogen acquisition due to higher soil nitrogen availability along the productivity gradient dominates the increased cost of the supporting tissue, even in species with a decreasing LAR, inasmuch as N decreases (Fig. 5). The same tendency is apparent in the less productive section of the gradient on a stand level (Fig. 4). However, under high productivity, the cost of supporting tissue evidently increases more rapidly and the increasing cost of nitrogen is not compensated for by the enhanced availability from the soil. This may indicate increased competition that forces plants to decrease their LAR more rapidly than increased soil fertility alone would allow. Fig. 4 Stand level values of (a) N, (b) M, (c) anue and (d) LAR as a function of total above-ground dry mass. Linear equations are used for fitting except in (a) where the second order polynomial is used. Significant coefficients are marked: *** P < 0.01, ** P < 0.05, * P < 0.1. to decrease with productivity, as was found by Anten & Hirose (1998, 1999). Therefore, low M should not be interpreted as the plant s inability to increase light harvesting efficiency but as evidence for increased LUE. Such an increase in LUE is typical when LAI increases (Sinclair & Shiraiwa 1993; Kull & Tulva 2002; Gordillo et al. 2003). The underlying reason for such a change in LUE results from the fundamental structure of the photosynthetic apparatus, so that an increased amount of photosynthesizing tissue per unit of intercepted light, leads ultimately to an increase in LUE (Kull 2002). Originally N was used as an indicator of NUE (Hirose & Werger 1994). Although in this study, N showed a high level of conformity with other NUE COMPETITION AND ACCLIMATION ALONG PRODUCTIVITY GRADIENT Change in below-ground competition along a nutrient availability gradient remains under debate (Aerts 1999). However, most investigators agree that aboveground competition for light increases considerably. As in our study, an increase in soil nitrogen availability usually leads to increased LAI and a decline in available light per leaf area or biomass. Consequently, a decline in M is an indicator of increased competition. The directionality of light makes it possible for dominant species to monopolize this resource more readily than nutrients and therefore, competitive asymmetry usually increases in high nutrient soil (Grime 1979; Schippers et al. 1999). Competitive asymmetry is also influenced by growth form and usually asymmetry declines under nutrient-poor conditions (Schippers & Kropff 2001). Our data show that relative benefits from enlarged biomass to capture a higher proportion of available light clearly rise with increasing site productivity (Fig. 2) and in our opinion this is clear evidence of increased asymmetry in between-species competition (Freckleton & Watkinson 2001). Our data suggest that competition for light between species tends to be size-symmetric in stands with LAI < 2.5 and becomes asymmetric above that limit (Fig. 2). Our unexpected finding, that NUE did not decrease with increasing nitrogen availability either at the species or community level, may also be attributed to increasing competition. If selection favours high nutrient productivity

9 1151 Light partitioning along productivity gradient Fig. 5 Relationship between species specific values of N and stand total above-ground dry mass. Significant relationships are marked: *** P < 0.01, ** P < 0.05, * P < 0.1. Fig. 6 Relationship between species specific values of anue and stand total aboveground dry mass. Significant relationships are marked: *** P < 0.01; ** P < 0.05; * P < 0.1. then the actual trend in NUE along a productivity gradient may depend on the relative importance and strength of the competition; this may help resolve some of the contrasting findings of Vitousek (1982). For instance, intraspecies competition in managed forests is usually excluded and often competition between individuals of the same species is suppressed by management activities. Nutrient availability often has a profound influence on the competitive performance of species. However, interactions between species are complex and pairwise experiments have shown that competitive ability of a species may not change linearly along nutrient availability gradients (Li & Watkinson 2000). In this investigation, all the species were present along the entire extent of the gradient. Consequently, we cannot refer to species replacement or distinguish between species of nutrient rich vs. nutrient poor habitats. Although some species were present only at one end of the gradient, their relative contribution to the total biomass was very low and from a functional aspect they are considered transient species according to Grime (1998). Consequently, the relevant question in this study is to understand why some species become dominant

10 1152 A. Aan, L. Hallik & O. Kull Fig. 7 Relationship between species specific values of M and stand total aboveground dry mass. Significant relationships are marked: *** P < 0.01; ** P < 0.05; * P < 0.1. Fig. 8 Relationship between species specific values of LAR and stand total aboveground dry mass. Significant relationships are marked: *** P < 0.01; ** P < 0.05; * P < 0.1. when productivity increases, whereas others become subordinates. Our data show that the features most likely to lead to domination in high productive sites are intrinsically low LAR and stature, which allow plant species to overtop others with the cost of an even greater reduction in LAR. Additionally, these species had relatively high NUE. The fact that these plants, which had grown larger during the same time-period (from the beginning of the vegetation period till harvesting), also had a high anue is relatively immaterial, because larger plants should have more nitrogen-poor support tissue (Lemaire & Millard 1999). This competitive success is often related to high photosynthesis rates (McAllister et al. 1998). It is likely that the high productivity of the dominant species in our study was achieved via increased photosynthetic nitrogen use (nitrogen productivity) and not via an increased amount of photosynthesizing apparatus in the leaves, inasmuch as these species tended to have relatively low leaf area N content. Eckstein & Karlsson (1997) suggested that in highnutrient habitats, selection is greatest for species with high nutrient productivity and that species cannot adapt to nutrient-poor conditions by increasing their

11 1153 Light partitioning along productivity gradient Fig. 9 Relationship between leaf total chlorophyll to nitrogen ratio in leaves at the lowest canopy layer and PhAR incident to that layer. Significant relationships are marked: *** P < 0.01; ** P < 0.05; * P < 0.1. NUE. In a paired comparison between F. pratensis and D. glomerata, the same species as in our study, Carlen et al. (1999) showed that the superior competitive ability of D. glomerata was achieved under non-limiting soil conditions through higher nitrogen productivity, thus confirming our findings. Our data offer no explanation as to why intrinsically high NUE species cannot become dominant in the nutrient-poor section of the gradient. We speculate that these species are more ruderal or high resource type according to Chapin et al. (1993), and respond with rapid changes in growth to variations in nutrient availability, in contrast to species that remain subordinate. Low tissue N concentration, a possible indicator of high NUE, is typical for fast growing species with ruderal life histories (McJannet et al. 1995). Apparently, growth limitation at the less productive section of our gradient was sufficiently severe to reduce the growth of high resource species to the level of other species. In our earlier study on the productivity gradient generated by light availability, we compared graminoid and forb growth forms and found that the dominance of graminoids at the more productive section of the gradient was achieved mainly via high NUE and rapid growth without any substantial evidence of overtopping (Kull & Aan 1997). This result supports the view that dominance in such an herbaceous community is more a result of differences in species-specific growth rate, than of asymmetric competition. One striking difference between dominant and subordinate species in this study was their plasticity in LAR. In contrast to dominant species the subordinates responded to strong competition with an enlargement of their LAR. Apparently, there are two contrasting adaptive possibilities to cope with increased competition: (i) to overtop others with cost in decreased LAR, or (ii) to increase light capturing ability with increased LAR. The fact that the subordinates are directed to better adaptations with low light in the shade of dominants is also demonstrated by their better plasticity of adjusting photosynthetic apparatus, as reflected by Chl/N ratio. Stoichiometry of leaf photosynthetic apparatus changes such that at low irradiance there is relatively more chlorophyll-containing, yet nitrogen-poor light harvesting apparatus, and less nitrogen-rich biochemical apparatus for electron transport and carbon fixation than at high irradiance levels (Anderson & Osmond 1987; Evans 1989; Eichelmann et al. 2005). In addition, species differ largely in their ability to adjust their photosynthetic apparatus for particular PPFD conditions (Turnbull et al. 1993; Murchie & Horton 1997; Kursar & Coley 1999). Our study shows that subordinate species without a strategy to grow tall in response to intensified competition have a more plastic adjustment to shade in their photosynthetic apparatus, and the ratio of leaf chlorophyll to nitrogen content is more plastic in subordinate species than in dominant species. Conclusions The study shows that species dominating high soil resources have lower tissue nitrogen concentrations and intrinsically low leaf area ratios. In contrast to expectations, above-ground efficiency of nitrogen use in the entire community increased with increasing productivity, but this rise was caused solely by changes in species composition. Light absorption per unit of above-ground plant mass declined at the community level and also in most species, indicating that light use efficiency increased with increasing site fertility. Light absorption per unit of leaf nitrogen as an indicator of

12 1154 A. Aan, L. Hallik & O. Kull the ratio (nitrogen use efficiency)/(light use efficiency) showed no clear pattern at the community level because both efficiencies tend to increase with increased productivity. There were clear differences in acclimation patterns between species that became dominant at high productivity plots and species that remained as subordinates. Our study revealed that plasticity in aboveground growth pattern and nitrogen allocation differs between species in reaction to increased soil fertility and competition, leading to substantially different strategies of survival and the decoupling of species and community level acclimation. Acknowledgements We thank Igna Rooma, who performed the description and analysis of soil parameters. We are also grateful to Maarika Mäesalu and Marek Mäesalu for helping us with the fieldwork and to Robert Szava-Kovats for editing the language. This work was supported by Estonian Sciences Foundation Grant no References Aerts, R. 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