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1 Geobotanisches Institut ETH Zürich, Gladbachstr. 114, CH-8044 Zürich, Switzerland; and 2 Department of Botany and Ecology, Tartu University, Lai 40, EE-2400 Tartu, Estonia
Received for publication March 11, 1999. Accepted for publication July 6, 1999.
ABSTRACT
Trade-offs between acquisition capacities for aboveground and belowground resources were investigated by studying the phenotypic plasticity of leaf and root traits in response to different irradiance levels at low nutrient supply. Two congeneric grasses with contrasting light requirements, Dactylis glomerata and D. polygama, were used. The aim was to analyze phenotypic covariation in components of leaf area and root length in response to above- and belowground resource limitation and the consequences of this variation for resource acquisition and plant growth. At intermediate shading (30 and 20% of full sunlight) the plants were able to maintain their total root length, despite a strongly increased total leaf area and a reduced biomass allocation to roots. This was associated with an unaltered or slightly increased nutrient uptake and growth. At 5.5% relative irradiance, growth was severely reduced, especially in the shade-tolerant D. polygama. The results show that constraints on acquisition capacities for aboveground and belowground resources, caused by biomass allocation, may be alleviated by plasticity in other traits such as tissue-mass density and thickness of roots and leaves. The results also suggest different adaptive constraints for phenotypic plasticity and for genetically determined interspecific variation. Phenotypic plasticity tends to maximize resource acquisition and growth rate in the short term, whereas the higher tissue-mass density and the longer leaf life-span of shade-tolerant species indicate reduced loss rates as a more advantageous species-specific adaptation to shade in the long term.
Key Words: adaptation • biomass allocation • Dactylis • leaf area • nutrient acquisition • Poaceae • root length • shade tolerance • tissue-mass density
In most environments plants compete both for aboveground and belowground resources. The capacity to acquire aboveground resources is associated with leaf area (Lambers and Poorter, 1992
), and the capacity to acquire belowground resources is associated with root length (Ryser, 1998
). These traits are phenotypically plastic and their responses improve resource acquisition. Shade leads to an increased leaf area ratio, i.e., leaf area per total plant dry mass (Thompson, Kriedemann, and Craig, 1992;
Reich et al., 1998
), and low nutrient supply results in an increased root length ratio, i.e., root length per total plant dry mass (Boot and den Dubbelden, 1990
; Ryser and Lambers, 1995
). Variation both in leaf area ratio and in root length ratio is determined by three components: relative biomass allocation to the respective organ, thickness of that organ, and tissue-mass density, i.e., the volume of tissue a plant can produce with a given amount of dry matter (Dijkstra, 1989
; Ryser and Lambers, 1995
).
The balance between acquisition capacities for aboveground and belowground resources is commonly expressed as the ratio between leaf area and root length (Jordan, Miller, and Morris, 1979
; Körner and Renhardt, 1987
; Eissenstat et al., 1993
; Kohyama and Grubb, 1994
; Perez-Corona and Verhoeven, 1996; Richner, Soldati, and Stamp, 1996
). However, because of the obvious impossibility for a plant to allocate a given unit biomass simultaneously both in its leaves and roots, studies on resource acquisition and plant growth at dual resource limitation have mostly focused on biomass allocation. As a consequence of this, resource acquisition capacities aboveground and belowground are frequently considered to constrain each other, with growth maximization regarded as a result of optimal biomass partitioning to different organs (Schulze, Schilling, and Nagarajah, 1983
; Bloom, Chapin, and Mooney, 1985
; Hirose, 1987
; Mooney and Winner, 1991
; Van der Werf et al., 1993
; Bazzaz and Grace, 1997
), and species' performance along resource availability gradients being regarded as a consequence of their inherent biomass allocation pattern (Tilman, 1988
). This ignores the potential importance of other traits that determine leaf area and root length: leaf and root thickness and leaf and root tissue-mass density. Variation in these traits may help to overcome the constraint imposed by allocation, as shown for interspecific relationships. For instance, Dactylis glomerata is superior to Brachypodium pinnatum both in acquisition of aboveground and belowground resources: its low tissue-mass density enables it to have simultaneously a higher leaf area ratio and a higher root length ratio than B. pinnatum, and consequently to be more efficient in nutrient uptake and have a higher growth rate, independently of nutrient supply (Ryser and Lambers, 1995
).
The purpose of the present study was to gain understanding of the constraints and compensatory mechanisms between traits determining aboveground and belowground resource acquisition when both resources are at low availability. How does phenotypic covariation of the components of leaf area ratio and root length ratio maximize plant growth at low irradiance and low nutrient supply? The rare studies about phenotypic plasticity of belowground morphology in response to shading have so far delivered contradictory results: in tree seedlings the specific root length has been shown to increase (Van Hees, 1997
), decrease (Reich et al., 1998
), or remain unaltered (Cornelissen, Werger, and Zhong, 1994
) in response to shading. Next to biomass allocation, morphology, and tissue structure, we also studied the allocation pattern of the acquired nitrogen, which influences carbon assimilation capacity (Hirose and Werger, 1987a;
Evans, 1989
), and leaf life-span, which at low resource availability may be more important for plant fitness than growth rate, and is known to be constrained by tissue structure (Ryser, 1996
; Schläpfer and Ryser, 1996
). Simultaneous consideration of the variation in these parameters is necessary for understanding plants as integrated units that require both nutrients and light and to obtain insight into the nature and significance of morphological and anatomical trade-offs imposed on plants when both aboveground and belowground resources are low.
Species occurrence along environmental gradients is determined by interspecific differences in functional traits, such as those influencing resource acquisition capacities. However, the intraspecific variation in these traits due to phenotypic plasticity is often larger than these interspecific differences (Corré, 1983
; Abrams and Kubiske, 1990
; Ashton and Berlyn, 1994
; Ryser and Lambers, 1995
). In order to understand the role of phenotypic plasticity in response to supply of a resource in comparison to interspecific differences among species with different ecological requirements for this resource, we conducted our study with two congeneric grass species with contrasting shade tolerance.
MATERIALS AND METHODS
Species
The study was conducted using two congeneric perennial grass species with contrasting light requirements—Dactylis glomerata L. and Dactylis polygama Horv. (nomenclature according to Lauber and Wagner, 1996
). Dactylis glomerata grows in open or partially shaded habitats, mostly in relatively productive, moderately disturbed grasslands. It grows also as a minor constituent in unproductive or heavily disturbed vegetation (Grime, Hodgson, and Hunt, 1988
). Dactylis polygama is restricted to more shady environments, usually broad-leaved forests on medium-rich soils (Oberdorfer, 1994
). Ecological indicator values of D. glomerata and D. polygama for light are 7 and 5, respectively, according to Ellenberg et al. (1992
; scale of increasing light exposure from 1 to 9). Dactylis glomerata is widespread and common throughout Europe and has been introduced to North America. Dactylis polygama is less frequent and more or less restricted to central Europe (Hulten and Fries, 1986
). In Switzerland Dactylis glomerata is usually tetraploid (2n = 28) and D. polygama diploid (2n = 14) (Hess, Landolt, and Hirzel, 1980
). These chromosome numbers were confirmed for the studied populations (Baltisberger and Ryser, 1999
).
Seeds of both species were collected in summer 1995 in Zürich, Switzerland: D. glomerata in a relatively nutrient-rich disturbed grassland (Allmend) and D. polygama in a shady park (Rieterpark).
Treatments
Plants were grown at four relative photon flux densities (PFD): 100, 30, 20, and 5.5% of full daylight. The range of PFDs used in the experiment corresponds with the range of light availability in the natural habitats where the studied species occur. The shade treatments were achieved by tents (3 x 4 x 2.3 m) covered on all sides with aluminum-coated shade cloths, OLS 60 and OLS 80 (Ludvig Svensson, Kinna, Sweden). The shade cloths consisted of 5-mm broad stripes, out of which two-thirds (OLS 60) and four-fifths (OLS 80) were covered with aluminium foil, the rest remaining open. Shading was thus not uniform but resulted in small sun flecks, equivalent to conditions on forest floors. The holes also improved circulation of air and the high reflection of irradiation reduced any effects on temperature in the shade tents. OLS 60 was used for tents with 30% PFD and OLS 80 for tents with 20% PFD. The 5.5% PFD was achieved by a combination of OLS 80 (top) and a regular black plastic shade cloth with 50% transmittance (bottom). Because of reduction in internal reflection by the black cloth, the achieved additional reduction in PFD was >50%. Each shading treatment was replicated by two tents, the full daylight treatment by two blocks with no shading structures in the vicinity. The actual levels of PFD were measured for 5–7 0.5-h periods on sunny and cloudy days in each tent at different times of day using Quantum sensors (LI-COR Inc., Lincoln, Nebraska, USA) and millivolt integrators (Delta-T Devices, Cambridge, UK). The measured relative photon flux densities were hardly affected by weather or time of day. The mean values for the three levels of shading were 30.4 ± 0.4, 19.8 ± 0.3, and 5.5 ± 0.2% of the unshaded treatment, respectively (mean value ± 1 SE). There were no significant differences between the replicate tents (nested ANOVA on arcsine-transformed values of relative PFD). Influence of the shade cloth on other environmental parameters, such as temperature and humidity, was minimal. In the tents with 5.5% PFD, afternoon maximum temperatures of 20°–25°C outside were reduced by 2°–3°, whereas nightly minima around 5°C were ~1° higher than outside. Relative humidity on a sunny day was 50–60% inside the shadiest tents, compared to the 30–40% outside. The influence of the 20 and 30% PFD treatments on temperature and humidity was less than that of the 5.5% PFD.
Precipitation was reduced to 43 ± 15, 27 ± 11, and 13 ± 4% of the outside values in the 30, 20, and 5.5% PFD tents, respectively (mean values ± 1 SD, six measurement periods). In order to avoid a possible influence of shading treatment on nutrient wash-out, any deficit of precipitation in the tents was compensated twice a week by adding the required amount of demineralized water.
Nutrients were given twice a week as 200 mL of diluted (1:80) nutrient solution. On each occasion, each pot received the following amounts of nutrients: 6.25 µmol KH2PO4, 18.75 µmol KNO3, 6.25 µmol Ca(NO3)2, 2.5 µmol MgSO4, 0.0024 µmol CuSO4, 0.00095 µmol ZnSO4, 0.023 µmol MnCl2, 0.058 µmol H3BO3, 0.0006 µmol Na2MoO4, 0.025 µmol FeCl3, and 3.75 µg tartaric acid.
Mean daily temperature until the first harvest (days 1–28) was 18.0°C, and 14.2°C between the two harvests (days 29–53). Mean daily irradiations for these periods were 17.5 and 13.6 MJ/m2, respectively (measurements done at Schweizerische Meteorologische Anstalt in Zü-rich, 5.5 km south east of the experimental garden at 556 m a.s.l.).
Experiment
Seeds were sown on 3 July 1996 on perlite. On 23 July the seedlings were planted into plastic tubes (diameter 10 cm, height 30 cm) in the experimental garden of the Geobotanical Institute ETH on Hönggerberg, Zürich (520 m a.s.l.). The substrate used was white quartz sand of 0.1–0.7 mm grain size. To avoid any treatment effects on water availability, the pots stood in shallow trays, which were filled with water up to 2–3 cm depth. Capillary movement of water kept the sand moist and ensured a continuous water supply for the plants. Two harvests were conducted, the first on 16–19 August, and the second on 10–13 September, with an interval of 25 d for each species and treatment. Eight plants (in two blocks of four) of each species and treatment were harvested at each occasion and separated into leaf blades, leaf sheaths (stems), and roots. Fresh mass of the parts and leaf area were measured at harvest. The plants were kept moist until fresh mass measurement. Leaf area was measured with a LI-3100 area meter (LI-COR Inc., Lincoln, Nebraska, USA). Dry masses were measured after at least 24 h at 70°C. Before measurement of root dry mass, specific root length and, at the second harvest, root diameter distribution were measured. Before the measurement, the roots were stored for 1–4 wk in 50% ethanol. Root length was measured using the grid-intersection method (Tennant, 1975
). For each plant in the second harvest, diameter distribution of 70–100 roots crossing a line on an object slide was measured with a light microscope using a 40-fold magnification. Root volume was calculated using root diameter distribution and SRL (Ryser and Lambers, 1995
). Plants from the second harvest were analyzed for carbon and nitrogen contents, separately for leaf blades and for the remaining parts. Dried plant material was ground with a ball mill (type MM2, Retsch, Arlesheim, Switzerland) and analyzed on an elemental analyser (LECO CHN-1000, LECO Corp., St. Joseph, Michigan, USA). At 5.5% PFD most of the plants were too small to be analyzed separately for N and C content. Therefore, the four smallest D. glomerata plants were pooled into two composite samples. In D. polygama all plants of that treatment had to be pooled to one sample.
Growth parameters
The following parameters were determined: leaf area ratio (LAR; square metre per kilogram), root length ratio (RLR; metre per gram), leaf mass ratio (LMR; gram per gram), root mass ratio (RMR; gram per gram), specific leaf area (SLA; square metre per kilogram), specific root length (SRL; metre per gram), leaf dry mass to fresh mass ratio (DML/FML; gram per gram), stem dry mass to fresh mass ratio (DMS/FMS; gram per gram), root dry mass to volume ratio (DMR/VR; milligram per cubic millimetre), leaf area to fresh mass ratio (AL/FML; square metre per kilogram), root length to volume ratio of all roots (LR/VR; millimetre per cubic millimetre), fine root length to volume ratio (roots < 0.25 mm; LFR/VFR; millimetre per cubic millimetre), proportion coarse root length (roots > 0.25 mm; metre per metre), plant nitrogen concentration (PNC; millimol per gram dry mass), total plant nitrogen to total root length ratio (PN/RL; millimol per metre), leaf nitrogen ratio (LNR; mol N leaf per mol N plant), mass-based leaf nitrogen concentration (LNCM; millimol per gram), area-based leaf nitrogen concentration (LNCA; millimol per square metre), C/N ratio of leaves (CNL; mol C per mol N).
LAR (leaf area per total plant dry mass) and RLR (root length per total plant dry mass) express a plant's potential to acquire aboveground and belowground resources, respectively. These parameters are a product of a component expressing the relative amount of biomass allocated to the respective organs (LMR, RMR) and a component expressing the leaf area or root length made with this biomass (SLA, SRL; Evans, 1972
). The latter component can be expressed as a ratio of components that reflect leaf and root fineness (leaf area per leaf fresh mass, AL/FML; root length per root volume, LR/VR) and tissue-mass density (leaf dry mass per leaf fresh mass, DML/FML; root dry mass per root volume, DMR/VR; Ryser and Lambers, 1995
). Relationships between these parameters are summarized by the following equations:
During the experiment, some leaf mortality was observed. The ratio of dead leaves to the total number of leaves produced was used as a parameter to express leaf turnover.
Statistical analysis
The experiment had a split-plot design with two replicates for each of the four light treatment levels. At each harvest four plants per species were collected in each replicate tent or plot. Statistical analysis was conducted using SyStat statistical package (SyStat: Statistics, Version 5.2 for Macintosh, SyStat Inc. Evanston, Illinois, USA, 1992). Interspecific differences and influence of treatments were tested with a nested ANOVA using the General Linear Model with species, light, harvest day (only for parameters measured at two harvests), and block as categorical variables, blocks nested within light. Because most of the measured parameters showed a dependence on plant size, log-transformed plant total dry mass was used as covariate. All interactions were initially included into the model, the nonsignificant ones being then stepwise excluded. Percentage data, such as biomass allocation parameters, dry mass:fresh mass ratio, and leaf mortality, were arcsine transformed prior to analysis. Other parameters were log transformed. Relative growth rates for the interval between the two harvests were calculated using linear regressions of log-transformed plant biomass data. The strong dependence of several growth parameters on plant size made it necessary to calculate adjusted values for the parameters before comparing the parameter values of the species and the amount of phenotypic plasticity of the parameters. Adjusted values for the average plant size (40.3 mg) were calculated using a linear regression between the transformed values of the parameters and log-transformed total plant dry mass.
The amount of phenotypic plasticity of the parameters in response to the treatments was expressed for each species as coefficient of variation, calculated as CV = 100 x standard deviation of individual treatment means, divided by the grand mean of the treatment means (Schlichting and Levin, 1986
). The P value for treatment x species interaction in the ANOVA (see above) shows whether interspecific differences in plasticity are significant (Schlichting, 1986
). The degree of interspecific difference in parameter values is expressed as percentage difference in the grand means of the two species, the smaller of the two values being equal to 100%.
RESULTS
Growth
Shading reduced plant growth only at 5.5% PFD treatment (Fig. 1; Table 1). In the first harvest mean values for total plant dry mass of D. polygama and D. glomerata at 5.5% PFD were 37 and 48%, respectively, of those in full light and in the second harvest 9.7 and 14%. Intermediately shaded plants at 30 and 20% PFD treatments were 35–78% (first harvest) and 22–54% (second harvest) larger than those grown in full light (P < 0.001 for both species and harvests, test of effects). Dactylis glomerata had a larger biomass than D. polygama in all treatments (Fig. 1). This was caused by its larger seed size, but also by its higher relative growth rates during the experiment. At 5.5% PFD, RGR of D. glomerata between the two harvests was almost double that of D. polygama. In the other treatments no clear interspecific differences were observed (Table 1), possibly because these were masked by size effects, as D. glomerata was larger than D. polygama already at the first harvest.
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General interspecific differences in leaf and root characteristics
Dactylis glomerata had a higher LAR than D. polygama in all treatments except in full light, and a higher RLR except in the deepest shade. Compared with the effect of the treatments, interspecific differences were relatively small (Table 3).
The general differences in LAR and RLR were, to a large extent, due to the higher SLA and SRL in D. glomerata, although the species effect on SRL was not significant (Table 2). Mean values of biomass allocation parameters across all the treatments were about the same for both species although the values for D. glomerata varied more with the treatments (Fig. 2c, d; Table 3).
The slight differences in SLA and SRL concealed larger but contrasting interspecific differences in their components. Dactylis polygama had thinner leaves than D. glomerata, but the latter had a lower leaf tissue-mass density (Fig. 2i, g; Table 3). Roots of D. polygama had a higher tissue-mass density but were thinner due to a higher length:volume ratio of the roots <0.25 mm diameter (Fig. 2h, k; Table 3). Tissue densities in leaves, stems, and roots showed the largest interspecific differences of all parameters (Table 4).
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Leaf turnover
Some leaf mortality occurred during the experiment. Excluding the deepest shade from the analysis, where only leaves present already at planting died, the percentage of dead leaves of the total leaf number produced was significantly lower for D. polygama (4.8 ± 0.8%) than for D. glomerata (8.1 ± 1.0%; mean values ± 1 SE; P = 0.028). Photon flux density had no significant effect on leaf turnover.
DISCUSSION
Phenotypic response to light at low levels of nutrients
Reduction in photosynthetic photon flux by 70 and 80% doubled to tripled the leaf area and strongly reduced biomass allocation to roots. Nevertheless, it did not reduce root length, nitrogen acquisition, nor plant growth. The constancy in root length across the treatments, except the most shaded one, was striking, considering the strong morphological response of the plants to these treatments. This emphasizes how important it is to regard phenotypic plasticity at the whole plant level as a concerted response of different traits. Greater investment in light harvesting does not necessarily occur at the cost of nutrient uptake, even at low nutrient availability.
In contrast to this, in plants that have not had a possibility to adjust their morphology and physiology to the actual resource availabilities, a decrease in irradiance also reduces their ability to acquire nutrients. Short-term shading of plants with a phenotype adapted to high-light conditions has a negative effect on the acquisition of belowground resources, as root growth decreases and nutrient uptake is reduced (Jackson and Caldwell, 1992
; MacDuff and Jackson, 1992
; Casadesus, Tapia, and Lambers, 1995
). This is observed already at 50–60% reduction of PFD, far less than the shading in our experiment (Crapo and Ketellapper, 1981
; Rufty, Raper, and Jackson, 1981
; Bilbrough and Caldwell, 1995
; Cui and Caldwell, 1997
).
The faster growth due to intermediate shading in our study at low nutrient availability indicates that the shade phenotypes were better at resource acquisition and growth. This is probably a result of the larger total leaf area in association with an unchanged root length. Similarly, the low-light phenotype (grown at 200 µmol·m-2·s-1) of Abutilon theophrasti, has been found to grow faster than the high-light phenotype (grown at 900 µmol·m-2·s-1) even when transferred to the high-light conditions (Rice and Bazzaz, 1989
). In that experiment, the higher leaf area of the low-light phenotype more than compensated for its lower photosynthetic capacity per leaf area at the high-light conditions.
Shading reduced the area-based N concentration by one-third compared to that in full sunlight, despite the increased allocation of N to leaf blades. Area-based N concentration decreased, even at 5.5% PFD, as SLA increased more than the mass-based N concentration. The low area-based N concentration may have helped to maintain the amount of biomass produced per unit N and time, as the photosynthetic nitrogen-use efficiency (PNUE) increases with a decrease of N concentration per leaf area (Pons, Van der Werf, and Lambers, 1994
). Similarly, the productivity per unit P in the leaves increases with decreasing area-based leaf P concentration (Ryser, Verduyn, and Lambers, 1997
). Also, the response here is different if the plants have no possibility to adjust their growth form and nutrient distribution, such that short-term shading reduces PNUE (Hirose and Werger, 1987b
). The higher ratio between the total amount of nitrogen taken up by the plants and their total root length in the shaded treatments indicates that the specific nitrogen uptake rate may be increased in the shade.
It is important to include the experimental shading pattern in the consideration of these results. The shade cloth we used created a light environment with small-scale spatiotemporal variations, similar to sunflecks on the forest floor. Heterogeneous shading reduces the daily carbon gain per leaf area more than uniform shading (Pearcy et al., 1994
), but this may be compensated by a larger leaf area, as shading with a broader range of light conditions triggers a larger phenotypic response at a certain level of PFD (Wayne and Bazzaz, 1993
).
An ecological disadvantage of shade-grown plants is often assumed to be a greater vulnerability to herbivores and pathogens, due to a lower C/N ratio, which leads to lower amounts of structural defenses, such as lignin and phenols (Herms and Mattson, 1992
). However, our data indicate that shading results in a lower C/N ratio only when photon flux density is growth limiting. As long as growth was not reduced, i.e., at 20 and 30% PFD, the reduced photon flux density had a positive effect on the leaf C:N ratio, as C allocation to leaves was stimulated more than N allocation. Tissue-mass density under these treatments was lower, however, possibly resulting in a higher vulnerability of these plants.
Besides a response to shade treatments, most of the studied parameters showed a strong ontogenetic drift. This clearly confirms the point that distinction of size effects in the analysis of plasticity is essential (Evans, 1972
; Coleman, McConnaughay, and Ackerly, 1994
).
Interspecific differences compared with phenotypic variation
Our data indicate different adaptive constraints for phenotypic plasticity and genetically determined interspecific variation. This may be a consequence of the different time scales these mechanisms operate at. Plastic response to shade tends to maximize resource capture and growth rate by increasing leaf area and root length, e.g., by decreasing tissue-mass density. The generally higher tissue-mass density and the lower initial leaf turnover of the shade-tolerant species suggest, however, that shade-tolerant species distinguish themselves by maximizing resource conservation. Growth maximization may be an advantage when shading is short term, e.g., caused by competing neighboring plants, and can be overcome. As a long-term adaptation to continually shady environments, resource conservation is likely to be more advantageous. Such a contrast between phenotypic and interspecific variation cannot be found with respect to responses to nutrient supply. Nutrient limitation increases tissue-mass density, and species from nutrient-poor habitats generally have a high tissue-mass density and long leaf and root life-spans (Ryser and Lambers, 1995
; Ryser, 1996
; Schläpfer and Ryser, 1996
).
Generalizations with respect to shade-tolerant and shade-sensitive species based solely on a comparison of two species have to be regarded with caution, but the interspecific differences in our experiment agree with other studies. Shade-sensitive species generally have higher growth rates even in shade, which is associated with a high LAR, SLA, and SRL (Thompson, Kriedemann, and Craig, 1992;
Kitajima, 1994
; Walters and Reich, 1996
; Reich et al., 1998
). The higher SLA of shade-sensitive species (Holmgren, 1968
; Walters and Field, 1987
; Abrams and Kubiske, 1990
; Walters, Kruger, and Reich, 1993
; Kitajima, 1994
) in combination with their thicker leaves (Jackson, 1967
; Pons, 1977
; Abrams and Kubiske, 1990
; Thompson, Kriedemann, and Craig, 1992;
Ashton and Berlyn, 1994
) is evidence for a generally lower tissue-mass density of these species, as a high SLA is either caused by thin leaves, low tissue-mass density, or both (Dijkstra, 1989
; Garnier and Laurent, 1994
; Ryser and Lambers, 1995
). Thus, thin leaves do not necessarily mean low biomass investments per unit area. Tissue-mass density was measured by Pons (1977)
, who found a lower dry mass:fresh mass ratio for the shade-sensitive Cirsium arvense than for the shade-tolerant Geum urbanum, both at high- and at low-irradiance levels.
Despite the strong phenotypic response to shading and the large interspecific difference in the degree of plasticity, the biomass allocation pattern did not show any overall differences between the species. This is in agreement with comparative studies of species with contrasting nutrient demands, in which no consistent differences in allocation pattern have been found (Lambers and Poorter, 1992
). However, among woody species with contrasting light requirements, the shade-sensitive species tend to have higher biomass allocation to leaves than the shade-tolerant ones (Hunt and Cornelissen, 1997
; Veneklaas and Poorter, 1998
). This is a further contrast between interspecific variation and phenotypic plasticity in responses to different levels of irradiance, since increasing irradiance leads to reduced biomass allocation to leaves.
Ecological and evolutionary consequences
Plants are able to compensate for a considerable shade-induced reduction in biomass allocation to roots by modifying other traits and are consequently able to prevent a reduction in root length, nutrient acquisition, and growth over a wide range of reduced irradiance. This emphasizes the importance of a concerted plastic response of plant characteristics as a means of maintaining balanced acquisition of aboveground and belowground resources and shows the necessity of considering a wide range of traits to fully understand plant responses to environmental conditions.
Adaptive constraints for phenotypic plasticity and for interspecific differentiation seem to be different. Phenotypic response to shade maximizes growth and is probably an advantage mainly in the short term, e.g., when shading is caused by competition and can be overcome. However, species-specific adaptations to generally shady habitats tend to increase tissue-mass density, resulting in a slower biomass turnover, and a long-term advantage due to reduced loss rates.
FOOTNOTES
1 The authors thank Ms Martina Bächli (Student Exchange Office ETH Zürich) for co-operation in organizing the stay of L. Eek in Switzerland, and Johannes Kollmann, Hans Lambers, and Hans Cornelissen for comments on the manuscript. The research was financially supported by the Rectorate of ETH Zürich. 
2 Author for correspondence (e-mail: ryser{at}geobot.umnw.ethz.ch
).
LITERATURE CITED
Abrams, M. D., and M. E. Kubiske. 1990 Leaf structural characteristics of 31 hardwood and conifer tree species in central Wisconsin: influence of light regime and shade-tolerance rank. Forest Ecology and Management 31: 245–253.
Ashton, P. M. S., and G. P. Berlyn. 1994 A comparison of leaf physiology and anatomy of Quercus (section Erythrobalanus-Fagaceae) species in different light environments. American Journal of Botany 81: 589–597. [CrossRef][ISI]
Baltisberger, M., and P. Ryser. 1999 Chromosome numbers. In C. A. Stace, IOPB chromosome data 15. IOPB Newsletter 31, 12.
Bazzaz, F. A., and J. Grace. 1997 Plant resource allocation. Academic Press, San Diego, California, USA.
Bilbrough, C. J., and M. M. Caldwell. 1995 The effects of shading and N status on root proliferation in nutrient patches by the perennial grass Agropyron desertorum in the field. Oecologia 103: 10–16. [CrossRef][ISI]
Bloom, A. J., F. S. Chapin III, and H. A. Mooney. 1985 Resource limitation in plants—an economic analogy. Annual Review of Ecology and Systematics 16: 363–362. [ISI]
Boot, R. G. A., and K. C. den Dubbelden. 1990 Effects of nitrogen supply on growth, allocation and gas exchange characteristics of two perennial grasses from inland dunes. Oecologia 85: 115–121. [CrossRef][ISI]
Casadesus, J., L. Tapia, and H. Lambers. 1995 Regulation of K+ and NO3- fluxes in roots of sunflower (Helianthus annuus) after changes in light intensity. Physiologia Plantarum 93: 279–285. [CrossRef]
Coleman, J. S., K. D. M. McConnaughay, and D. D. Ackerly. 1994 Interpreting phenotypic variation in plants. Trends in Ecology and Evolution 9: 187–191. [CrossRef]
Cornelissen, J. H. C., M. J. A. Werger, and Z.-C. Zhong. 1994 Effects of canopy gaps on the growth of tree seedlings from subtropical broad-leaved evergreen forests in southern China. Vegetatio 110: 43–54. [ISI]
Corré, W. J. 1983 Growth and morphogenesis of sun and shade plants. I. The influence of light intensity. Acta Botanica Neerlandica 32: 49–62.
Crapo, N. L., and H. J. Ketellapper. 1981 Metabolic priorities with respect to growth and mineral uptake in roots of Hordeum, Triticum and Lycopersicon. American Journal of Botany 68: 10–16. [CrossRef][ISI]
Cui, M., and M. M. Caldwell. 1997 Shading reduces exploitation of soil nitrate and phosphate by Agropyron desertorum and Artemisia tridentata from soils with patchy and uniform nutrient distributions. Oecologia 109: 177–183. [CrossRef][ISI]
Dijkstra, P. 1989 Cause and effect of differences in specific leaf area. In H. Lambers M. L. Cambridge, H. Konings, and T. L. Pons [eds.], Causes and consequences of variation in growth rate and productivity of higher plants, 125–140. SPB Academic Publishing, The Hague, The Netherlands.
Eissenstat, D. M., J. H. Graham, J. P. Syvertsen, and D. L. Drouillard. 1993 Carbon economy of sour orange in relation to mycorrhizal colonization and phosphorus status. Annals of Botany 71: 1–10.
Ellenberg, H., H. E. Weber, R. Düll, V. Wirth, W. Werner, and D. Paulissen. 1992 Zeigerwerte von Pflanzen in Mitteleuropa. Scripta Geobotanica 18: 1–258.
Evans, G. C. 1972 The quantitative analysis of plant growth. Blackwell Scientific, Oxford, UK.
Evans, J. R. 1989 Photosynthesis—the dependence on nitrogen partitioning. In H. Lambers M. L. Cambridge, H. Konings, and T. L. Pons [eds.], Causes and consequences of variation in growth rate and productivity of higher plants, 159–174. SPB Academic Publishing, The Hague, The Netherlands.
Garnier, E., and G. Laurent. 1994 Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species. New Phytologist 128: 725–736. [CrossRef][ISI]
Grime, J. P., J. G. Hodgson, and R. Hunt. 1988 Comparative plant ecology: a functional approach to common British species. Unwin Hyman, London, UK.
Herms, D. A., and W. J. Mattson. 1992 The dilemma of plants: to grow or defend. Quarterly Review of Biology 67: 283–335. [CrossRef]
Hess, H. E., E. Landolt, and R. Hirzel. 1980 Flora der Schweiz, 2nd ed. Birkhäuser, Basel, Switzerland.
Hirose, T. 1987 A vegetative plant growth model: adaptive significance of phenotypic plasticity in matter partitioning. Functional Ecology 1: 195–202.
———, and M. J. A. Werger. 1987a Maximizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72: 520–526. [CrossRef][ISI]
———, and ———. 1987b Nitrogen use efficiency in instantaneous and daily photosynthesis of leaves in the canopy of a Solidago altissima stand. Physiologia Plantarum 70: 215–222. [CrossRef]
Holmgren, P. 1968 Leaf factors affecting light-saturated photosynthesis in ecotypes of Solidago virgaurea from exposed and shaded habitats. Physiologia Plantarum 21: 676–698. [CrossRef]
Hulten, E., and M. Fries. 1986 Atlas of North European vascular plants: north of the tropic of cancer. Koeltz Scientific Books, Koenigstein, Germany.
Hunt, R., and J. H. C. Cornelissen. 1997 Components of relative growth rate and their interrelations in 59 temperate plant species New Phytologist 135: 395–417. [CrossRef][ISI]
Jackson, L. W. R. 1967 Effect of shade on leaf structure of deciduous tree species. Ecology 48: 498–499. [CrossRef][ISI]
Jackson, R. B., and M. M.Caldwell. 1992 Shading and the capture of localized soil nutrients: nutrient contents, carbohydrates, and root uptake kinetics of a perennial tussock grass. Oecologia 91: 457–462. [CrossRef][ISI]
Jordan, W. R., F. R. Miller, and D. E. Morris. 1979 Genetic variation in root and shoot growth of sorghum in hydroponics. Crop Science 19: 468–472.
Kitajima, K. 1994 Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98: 419–428. [CrossRef][ISI]
Körner, Ch., and U. Renhardt. 1987 Dry matter partitioning and root length/leaf area ratios in herbaceous perennial plants with diverse altitude distribution Oecologia 74: 411–418. [CrossRef][ISI]
Kohyama, T., and P. J. Grubb. 1994 Below- and above-ground allometrics of shade-tolerant seedlings in a Japanese warm-temperate rain forest Functional Ecology 8: 229–236. [CrossRef][ISI]
Lambers, H., and H. Poorter. 1992 Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Advances in Ecological Research 23: 187–261. [ISI]
Lauber, K., and G. Wagner. 1996 Flora Helvetica. Paul Haupt Verlag, Bern, Switzerland.
MacDuff, J. H., and S. B. Jackson. 1992 Influx and efflux of nitrate and ammonium in Italian ryegrass and white clover roots: comparisons between effects of darkness and defoliation. Journal of Experimental Botany 43: 525–535.
Mooney, H. A., and W. E. Winner. 1991 Partitioning response of plants to stress. In H. A. Mooney, W. E. Winner, and E. J. Bell [eds.], Response of plants to multiple stresses, 129–141. Academic Press, San Diego, California, USA.
Oberdorfer, E. 1994 Pflanzensoziologische Exkursionsflora, 7th ed. Eugen Ulmer, Stuttgart, Germany.
Pearcy, R. W., R. L. Chazdon, L. J. Gross, and K. A. Mott. 1994 Photosynthetic utilization of sunflecks: a temporally patchy resource on a time scale of seconds to minutes. In M. M.Caldwell and R. W. Pearcy [eds.], Exploitation of environmental heterogeneity by plants, 175–208. Academic Press, San Diego, California, USA.
Perez-Corona, M. E., and J. T. A. Verhoeven. 1996 Effects of soil P status on growth and P and N uptake of Carex species from fens differing in P-availability. Acta Botanica Neerlandica 45: 381–392. [ISI]
Pons, T. L. 1977 An ecophysiological study in the field layer of ash coppice II. Experiment with Geum urbanum and Cirsium palustre in different light intensities. Acta Botanica Neerlandica 26: 29–42. [ISI]
———, A. Van der Werf, and H. Lambers. 1994 Photosynthetic nitrogen use efficiency of inherently slow- and fast-growing species: possible explanations for observed differences. In J. Roy and E. Garnier [eds.], A whole plant perspective on carbon-nitrogen interactions, 61–77. SPB Academic Publishing, The Hague, The Netherlands.
Reich, P. B., M. G. Tjoelker, M. B. Walters, D. W. Vanderklein, and C. Buschena. 1998 Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Functional Ecology 12: 327–338. [CrossRef][ISI]
Rice, S. A., and F. A. Bazzaz. 1989 Growth consequences of plasticity of plant traits in response to light conditions. Oecologia 78: 508–512. [CrossRef][ISI]
Richner, W., A. Soldati, and P. Stamp. 1996 Shoot-to-root relations in field-grown maize seedlings. Agronomy Journal 88: 56–61.
Rufty, T. W., C. D. Raper, and W. A. Jackson. 1981 Nitrogen assimilation, root growth and whole plant responses of soybean root temperature, and to carbon dioxide and light in the aerial environment. New Phytologist 88: 607–619. [ISI]
Ryser, P. 1996 The importance of tissue density for growth and life span of leaves and roots: a comparison of five ecologically contrasting grasses. Functional Ecology 10: 717–723. [CrossRef][ISI]
———. 1998 Intra- and interspecific variation in root length, root turnover and the underlying parameters. In H. Lambers, H. Poorter and M. M. I. Van Vuuren [eds.], Variation in plant growth, physiological mechanisms and ecological consequences, 441–465. Backhuys Publishers, Leiden, The Netherlands.
———, and H. Lambers. 1995 Root and leaf attributes accounting for the performance of fast- and slow-growing grasses at different nutrient supply. Plant and Soil 170: 251–265. [CrossRef][ISI]
———, B. Verduyn, and H. Lambers. 1997 Phosphorus allocation and utilization in three grass species with contrasting response to N and P supply. New Phytologist 137: 293–302. [CrossRef][ISI]
Schläpfer, B., and P. Ryser. 1996 Leaf and root turnover of three ecologically contrasting grass species in relation to their performance along a productivity gradient. Oikos 75: 398–406. [CrossRef][ISI]
Schlichting, C. D. 1986 The evolution of phenotypic plasticity in plants. Annual Review of Ecology and Systematics 17: 667–693. [CrossRef][ISI]
———, and D. A. Levin. 1986 Phenotypic plasticity: an evolving plant character. Biological Journal of Linnean Society 29: 37–47. [CrossRef]
Schulze, E.-D., K. Schilling, and S. Nagarajah. 1983 Carbohydrate partitioning in relation to whole plant production and water use of Vigna unguiculata. Oecologia 58: 169–177. [CrossRef][ISI]
Tennant, D. 1975 A test of a modified line intersect method of estimating root length. Journal of Ecology 63: 995–1001. [CrossRef]
Thompson W. A., P. E. Kriedemann, and I. E. Craig. 1992 Photosynthetic response to light and nutrients in sun-tolerant and shade-tolerant rainforest trees. I. Growth, leaf anatomy and nutrient content. Australian Journal of Plant Physiology 19: 1–18.
Tilman, D. 1988 Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton, New Jersey, USA.
Van der Werf, A., A. J. Visser, F. Schieving, and H. Lambers. 1993 Evidence for optimal partitioning of biomass and nitrogen availabilities for a fast- and slow-growing species. Functional Ecology 7: 63–74. [CrossRef][ISI]
Van Hees, A. F. M. 1997 Growth and morphology of pedunculate oak (Quercus robur L.) and beech (Fagus sylvatica L.) seedlings in relation to shading and drought. Annales des Sciences Forestieres 54: 9–18.
Veneklaas, E. J., and L. Poorter. 1998 Growth and carbon partitioning of tropical tree seedlings in contrasting light environments In H. Lambers, H. Poorter, and M. M. I. Van Vuuren [eds.], Variation in plant growth, physiological mechanisms and ecological consequences, 337–361. Backhuys Publishers, Leiden, The Netherlands.
Walters, M. B., and C. B. Field. 1987 Photosynthetic light acclimation in two rainforest Piper species with different ecological amplitudes. Oecologia 72: 449–456. [CrossRef][ISI]
———, E. L. Kruger, and P. B. Reich. 1993 Growth, biomass distribution and CO2 exchange of northern hardwood seedlings in high and low light: relationships with successional status and shade tolerance. Oecologia 94: 7–16. [CrossRef][ISI]
———, and P. B. Reich. 1996 Are shade tolerance, survival, and growth linked? Low light and nitrogen effects on hardwood seedlings. Ecology 77: 841–853. [CrossRef][ISI]
Wayne, P. M., and F. A. Bazzaz. 1993 Birch seedling responses to daily time courses of light in experimental forest gaps and shadehouses. Ecology 74: 1500–1515. [CrossRef][ISI]
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