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1.  Comparison of methods for assessing the impact of different disturbances and nutrient conditions upon functional characteristics of grassland communities 
Annals of Botany  2010;106(5):823-831.
Background and Aims
Predicting the response of plant communities to variation in resources and disturbance is still a challenge, because findings depend on how ecological gradients are characterized and how grassland functional composition is assessed. Focusing on leaf dry matter content (LDMC), the efficacy of different methods for evaluating the best response of plant communities to either environmental or disturbance change is examined.
Methods
Data were collected on 69 grasslands located at four sites in the Pyrenees and Massif Central. N-Ellenberg indices and plant nutrient content (Ni) were compared to assess fertility, and either LDMC (meas) measured or calculated from a trait database for which traits were measured under the same environmental conditions (db). Management regime (MR) was characterized in terms of categories (grazing, cutting) and plant height.
Key Results
LDMCdb was positively correlated to LDMCmeas, but depended significantly on site temperature. N-Ellenberg and Ni were significantly correlated, and there was a significant effect of MR and temperature. LDMC responded to fertility, MR and temperature. Replacing MR by plant height in an REML analysis reduced the uncertainty of the LDMC prediction. LDMC was correlated to plant height at community level, whereas the correlation was weak at species level. Differences in LDMC between plant communities under any of the management regimes were significantly correlated to the standing herbage mass.
Conclusion
The N-Ellenberg index is a better indicator of fertility than Ni which is short-term and environment-dependent. LDMC taken from a database allows plant trait variation due to species abundance (excluding variation due to trait plasticity in response to management) to be captured. So the former is better suited for assessing agricultural services that mainly depend on plant phenology and tissue composition. LDMC responded to defoliation regime in addition to fertility because plant height is roughly correlated with LDMC at plant community level.
doi:10.1093/aob/mcq178
PMCID: PMC2958793  PMID: 20966187
Cutting; N-Ellenberg indices; fertility; grazing; leaf dry matter content; meadow; nitrogen; pasture; plant functional trait; plant height
2.  Specific Leaf Area and Dry Matter Content Estimate Thickness in Laminar Leaves 
Annals of Botany  2005;96(6):1129-1136.
• Background and Aims Leaf thickness plays an important role in leaf and plant functioning, and relates to a species' strategy of resource acquisition and use. As such, it has been widely used for screening purposes in crop science and community ecology. However, since its measurement is not straightforward, a number of estimates have been proposed. Here, the validity of the (SLA × LDMC)−1 product is tested to estimate leaf thickness, where SLA is the specific leaf area (leaf area/dry mass) and LDMC is the leaf dry matter content (leaf dry mass/fresh mass). SLA and LDMC are two leaf traits that are both more easily measurable and often reported in the literature.
• Methods The relationship between leaf thickness (LT) and (SLA × LDMC)−1 was tested in two analyses of covariance using 11 datasets (three original and eight published) for a total number of 1039 data points, corresponding to a wide range of growth forms growing in contrasted environments in four continents.
• Key Results and Conclusions The overall slope and intercept of the relationship were not significantly different from one and zero, respectively, and the residual standard error was 0·11. Only two of the eight datasets displayed a significant difference in the intercepts, and the only significant difference among the most represented growth forms was for trees. LT can therefore be estimated by (SLA × LDMC)−1, allowing leaf thickness to be derived from easily and widely measured leaf traits.
doi:10.1093/aob/mci264
PMCID: PMC4247101  PMID: 16159941
Leaf thickness; specific leaf area; leaf dry matter content; leaf density; interspecific variation; global comparative analysis
3.  Plant Trait Assembly Affects Superiority of Grazer's Foraging Strategies in Species-Rich Grasslands 
PLoS ONE  2013;8(7):e69800.
Background
Current plant – herbivore interaction models and experiments with mammalian herbivores grazing plant monocultures show the superiority of a maximizing forage quality strategy (MFQ) over a maximizing intake strategy (MI). However, there is a lack of evidence whether grazers comply with the model predictions under field conditions.
Methodology/Findings
We assessed diet selection of sheep (Ovis aries) using plant functional traits in productive mesic vs. low-productivity dry species-rich grasslands dominated by resource-exploitative vs. resource-conservative species respectively. Each grassland type was studied in two replicates for two years. We investigated the first grazing cycle in a set of 288 plots with a diameter of 30 cm, i.e. the size of sheep feeding station. In mesic grasslands, high plot defoliation was associated with community weighted means of leaf traits referring to high forage quality, i.e. low leaf dry matter content (LDMC) and high specific leaf area (SLA), with a high proportion of legumes and the most with high community weighted mean of forage indicator value. In contrast in dry grasslands, high community weighted mean of canopy height, an estimate of forage quantity, was the best predictor of plot defoliation. Similar differences in selection on forage quality vs. quantity were detected within plots. Sheep selected plants with higher forage indicator values than the plot specific community weighted mean of forage indicator value in mesic grasslands whereas taller plants were selected in dry grasslands. However, at this scale sheep avoided legumes and plants with higher SLA, preferred plants with higher LDMC while grazing plants with higher forage indicator values in mesic grasslands.
Conclusions
Our findings indicate that MFQ appears superior over MI only in habitats with a predominance of resource-exploitative species. Furthermore, plant functional traits (LDMC, SLA, nitrogen fixer) seem to be helpful correlates of forage quality only at the community level.
doi:10.1371/journal.pone.0069800
PMCID: PMC3724891  PMID: 23922805
4.  Two Measurement Methods of Leaf Dry Matter Content Produce Similar Results in a Broad Range of Species 
Annals of Botany  2007;99(5):955-958.
Background and Aims
Leaf dry matter content (LDMC) is widely used as an indicator of plant resource use in plant functional trait databases. Two main methods have been proposed to measure LDMC, which basically differ in the rehydration procedure to which leaves are subjected after harvesting. These are the ‘complete rehydration’ protocol of Garnier et al. (2001, Functional Ecology 15: 688–695) and the ‘partial rehydration’ protocol of Vendramini et al. (2002, New Phytologist 154: 147–157).
Methods
To test differences in LDMC due to the use of different methods, LDMC was measured on 51 native and cultivated species representing a wide range of plant families and growth forms from central-western Argentina, following the complete rehydration and partial rehydration protocols.
Key Results and Conclusions
The LDMC values obtained by both methods were strongly and positively correlated, clearly showing that LDMC is highly conserved between the two procedures. These trends were not altered by the exclusion of plants with non-laminar leaves. Although the complete rehydration method is the safest to measure LDMC, the partial rehydration procedure produces similar results and is faster. It therefore appears as an acceptable option for those situations in which the complete rehydration method cannot be applied. Two notes of caution are given for cases in which different datasets are compared or combined: (1) the discrepancy between the two rehydration protocols is greatest in the case of high-LDMC (succulent or tender) leaves; (2) the results suggest that, when comparing many studies across unrelated datasets, differences in the measurement protocol may be less important than differences among seasons, years and the quality of local habitats.
doi:10.1093/aob/mcm022
PMCID: PMC2802913  PMID: 17353207
Argentina; leaf dry matter content; leaf rehydration; plant comparative ecology; plant functional traits
5.  Plastic Traits of an Exotic Grass Contribute to Its Abundance but Are Not Always Favourable 
PLoS ONE  2012;7(4):e35870.
In herbaceous ecosystems worldwide, biodiversity has been negatively impacted by changed grazing regimes and nutrient enrichment. Altered disturbance regimes are thought to favour invasive species that have a high phenotypic plasticity, although most studies measure plasticity under controlled conditions in the greenhouse and then assume plasticity is an advantage in the field. Here, we compare trait plasticity between three co-occurring, C4 perennial grass species, an invader Eragrostis curvula, and natives Eragrostis sororia and Aristida personata to grazing and fertilizer in a three-year field trial. We measured abundances and several leaf traits known to correlate with strategies used by plants to fix carbon and acquire resources, i.e. specific leaf area (SLA), leaf dry matter content (LDMC), leaf nutrient concentrations (N, C∶N, P), assimilation rates (Amax) and photosynthetic nitrogen use efficiency (PNUE). In the control treatment (grazed only), trait values for SLA, leaf C∶N ratios, Amax and PNUE differed significantly between the three grass species. When trait values were compared across treatments, E. curvula showed higher trait plasticity than the native grasses, and this correlated with an increase in abundance across all but the grazed/fertilized treatment. The native grasses showed little trait plasticity in response to the treatments. Aristida personata decreased significantly in the treatments where E. curvula increased, and E. sororia abundance increased possibly due to increased rainfall and not in response to treatments or invader abundance. Overall, we found that plasticity did not favour an increase in abundance of E. curvula under the grazed/fertilized treatment likely because leaf nutrient contents increased and subsequently its' palatability to consumers. E. curvula also displayed a higher resource use efficiency than the native grasses. These findings suggest resource conditions and disturbance regimes can be manipulated to disadvantage the success of even plastic exotic species.
doi:10.1371/journal.pone.0035870
PMCID: PMC3335023  PMID: 22536448
6.  Community Functional Responses to Soil and Climate at Multiple Spatial Scales: When Does Intraspecific Variation Matter? 
PLoS ONE  2014;9(10):e111189.
Despite increasing evidence of the importance of intraspecific trait variation in plant communities, its role in community trait responses to environmental variation, particularly along broad-scale climatic gradients, is poorly understood. We analyzed functional trait variation among early-successional herbaceous plant communities (old fields) across a 1200-km latitudinal extent in eastern North America, focusing on four traits: vegetative height, leaf area, specific leaf area (SLA), and leaf dry matter content (LDMC). We determined the contributions of species turnover and intraspecific variation to between-site functional dissimilarity at multiple spatial scales and community trait responses to edaphic and climatic factors. Among-site variation in community mean trait values and community trait responses to the environment were generated by a combination of species turnover and intraspecific variation, with species turnover making a greater contribution for all traits. The relative importance of intraspecific variation decreased with increasing geographic and environmental distance between sites for SLA and leaf area. Intraspecific variation was most important for responses of vegetative height and responses to edaphic compared to climatic factors. Individual species displayed strong trait responses to environmental factors in many cases, but these responses were highly variable among species and did not usually scale up to the community level. These findings provide new insights into the role of intraspecific trait variation in plant communities and the factors controlling its relative importance. The contribution of intraspecific variation to community trait responses was greatest at fine spatial scales and along edaphic gradients, while species turnover dominated at broad spatial scales and along climatic gradients.
doi:10.1371/journal.pone.0111189
PMCID: PMC4203824  PMID: 25329794
7.  Leaf and Shoot Water Content and Leaf Dry Matter Content of Mediterranean Woody Species with Different Post-fire Regenerative Strategies 
Annals of Botany  2007;99(3):545-554.
Background and Aims
Post-fire regeneration is a key process in Mediterranean shrubland dynamics, strongly determining the functional properties of the community. In this study, a test is carried out to deteremine whether there is co-variation between species regenerative types and functional attributes related to water use.
Methods
An analysis was made of the seasonal variations in leaf relative water content (RWC), leaf dry matter content (LDMC), leaf moisture (LM) and live fine fuel moisture (LFFM) in 30 woody species of a coastal shrubland, with different post-fire regenerative strategies (seeding, resprouting or both).
Key Results
RWC results suggest that the studied resprouters have more efficient mechanisms to reduce water losses and maintain water supply between seasons. In contrast, seeders are more drought tolerant. LDMC is higher in resprouters over the course of the year, suggesting a more efficient conservation of nutrients. The weight of the phylogenetic constraint to understand differences between regenerative strategies tends to be important for LDMC, while it is not the case for variables such as RWC.
Conclusions
Groups of species with different post-fire regenerative strategies (seeders and resprouters) have different functional traits related to water use. In addition to the role of phylogenetical constraints, these differences are also likely to be related to the respective life history characteristics. Therefore, the presence and abundance of species with different post-fire regenerative responses influence the functional properties of the communities.
doi:10.1093/aob/mcl284
PMCID: PMC2802959  PMID: 17237213
Functional traits; leaf dry matter content; Mediterranean plants; post-fire; regenerative strategy; relative water content; resprouter; seeder; woody species
8.  The adaptive value of functional and life-history traits across fertility treatments in an annual plant 
Annals of Botany  2010;106(6):979-988.
Background and Aims
Plant functional traits are assumed to be adaptive. As selection acts on individuals and not on traits, interpreting the adaptive value of a trait not may be straightforward. For example, productive leaves are associated with fertile environments. However, it is not clear if productive leaves confer an advantage in these habitats, or if they are an advantage as part of a suite of coordinated traits.
Methods
Genotypes of Arabidopsis thaliana were grown in high and low nutrient treatments and low, neutral and high pH treatments. Nutrient availability is reduced in acidic or basic soils relative to neutral pH soils. pH treatments were used to alter the availability of resources rather than the amount of resources.
Key Results
Leaf function (specific leaf area, SLA) and life history (size at reproduction, age at reproduction) were variable across genotypes and were plastic. High nutrient availability induced higher SLA and larger size at reproduction. Genotypes that reproduced at large size in high nutrient conditions at neutral pH had the greatest fruit production. SLA was only indirectly related to fruit production through a causal relationship with rosette size; in high nutrient conditions, plants with high SLA were large at reproduction and had higher fruit production. In high nutrient and high pH treatments, plants were large at reproduction, but large size at reproduction was associated with low fecundity. This suggests that large size is adaptive under high nutrient availability.
Conclusions
Interpreting the adaptive value of functional traits will sometimes only be possible when these traits are considered as a suite of correlated and coordinated traits. Leaf functional traits may be important in defining adaptive strategies in A. thaliana but only through how they affect plant life history. Finally, manipulating soil pH can be a valuable tool in assessing adaptive plasticity on nutrient gradients.
doi:10.1093/aob/mcq195
PMCID: PMC2990665  PMID: 20880932
Adaptive plasticity; age at reproduction; Arabidopsis thaliana; functional traits; soil pH; rosette growth form; size at reproduction; SLA
9.  Spatial and temporal functional changes in alpine summit vegetation are driven by increases in shrubs and graminoids 
AoB Plants  2014;6:plu008.
In order to determine the mechanisms that drive changes in plant community composition across spatial and temporal scales, plant functional traits were used to interpret the results of a repeat species survey across a gradient of five alpine summits in south-east Australia. Vegetation changes were strongly affected by the high and increasing proportion of tall shrubs and graminoids, especially at the lower elevation summits. Several significant relationships between the community trait-weighted mean of different traits and elevation may suggest processes such as competition are influencing vegetation preferentially across the elevation gradient, with shrubs and graminoids driving these patterns.
Classical approaches to investigating temporal and spatial changes in community composition offer only partial insight into the ecology that drives species distribution, community patterns and processes, whereas a functional approach can help to determine many of the underlying mechanisms that drive such patterns. Here, we aim to bring these two approaches together to understand such drivers, using an elevation gradient of sites, a repeat species survey and species functional traits. We used data from a repeat vegetation survey on five alpine summits and measured plant height, leaf area, leaf dry matter content and specific leaf area (SLA) for every species recorded in the surveys. We combined species abundances with trait values to produce a community trait-weighted mean (CTWM) for each trait, and then combined survey results with the CTWMs. Across the gradient of summits, more favourable conditions for plant growth (warmer, longer growing season) occurred at the lower elevations. Vegetation composition changes between 2004 and 2011 (according to non-metric multi-dimensional scaling ordination) were strongly affected by the high and increasing abundance of species with high SLA at high elevations. Species life-form categories strongly affected compositional changes and functional composition, with increasing dominance of tall shrubs and graminoids at the lower-elevation summits, and an overall increase in graminoids across the gradient. The CTWM for plant height and leaf dry matter content significantly decreased with elevation, whereas for leaf area and SLA it significantly increased. The significant relationships between CTWM and elevation may suggest specific ecological processes, namely plant competition and local productivity, influencing vegetation preferentially across the elevation gradient, with the dominance of shrubs and graminoids driving the patterns in the CTWMs.
doi:10.1093/aobpla/plu008
PMCID: PMC4038439  PMID: 24790129
Alpine vegetation; community composition; functional composition; functional traits; GLORIA; Snowy Mountains.
10.  Plasticity in above- and belowground resource acquisition traits in response to single and multiple environmental factors in three tree species 
Ecology and Evolution  2013;3(4):1065-1078.
Functional trait plasticity is a major component of plant adjustment to environmental stresses. Here, we explore how multiple local environmental gradients in resources required by plants (light, water, and nutrients) and soil disturbance together influence the direction and amplitude of intraspecific changes in leaf and fine root traits that facilitate capture of these resources. We measured population-level analogous above- and belowground traits related to resource acquisition, i.e. “specific leaf area”–“specific root length” (SLA–SRL), and leaf and root N, P, and dry matter content (DMC), on three dominant understory tree species with contrasting carbon and nutrient economics across 15 plots in a temperate forest influenced by burrowing seabirds. We observed similar responses of the three species to the same single environmental influences, but partially species-specific responses to combinations of influences. The strength of intraspecific above- and belowground trait responses appeared unrelated to species resource acquisition strategy. Finally, most analogous leaf and root traits (SLA vs. SRL, and leaf versus root P and DMC) were controlled by contrasting environmental influences. The decoupled responses of above- and belowground traits to these multiple environmental factors together with partially species-specific adjustments suggest complex responses of plant communities to environmental changes, and potentially contrasting feedbacks of plant traits with ecosystem properties. We demonstrate that despite the growing evidence for broadly consistent resource-acquisition strategies at the whole plant level among species, plants also show partially decoupled, finely tuned strategies between above- and belowground parts at the intraspecific level in response to their environment. This decoupling within species suggests a need for many species-centred ecological theories on how plants respond to their environments (e.g. competitive/stress-tolerant/ruderal and response-effect trait frameworks) to be adapted to account for distinct plant-environment interactions among distinct individuals of the same species and parts of the same individual.
doi:10.1002/ece3.520
PMCID: PMC3631414  PMID: 23610644
Intraspecific variation; light availability; plant functional traits; plant physiological ecology; seabird burrowing; soil nutrients; specific leaf area; specific root length
11.  Leaf trait co-ordination in relation to construction cost, carbon gain and resource-use efficiency in exotic invasive and native woody vine species 
Annals of Botany  2010;106(2):371-380.
Background and Aims
Success of invasive plant species is thought to be linked with their higher leaf carbon fixation strategy, enabling them to capture and utilize resources better than native species, and thus pre-empt and maintain space. However, these traits are not well-defined for invasive woody vines.
Methods
In a glass house setting, experiments were conducted to examine how leaf carbon gain strategies differ between non-indigenous invasive and native woody vines of south-eastern Australia, by investigating their biomass gain, leaf structural, nutrient and physiological traits under changing light and moisture regimes.
Key Results
Leaf construction cost (CC), calorific value and carbon : nitrogen (C : N) ratio were lower in the invasive group, while ash content, N, maximum photosynthesis, light-use efficiency, photosynthetic energy-use efficiency (PEUE) and specific leaf area (SLA) were higher in this group relative to the native group. Trait plasticity, relative growth rate (RGR), photosynthetic nitrogen-use efficiency and water-use efficiency did not differ significantly between the groups. However, across light resource, regression analyses indicated that at a common (same) leaf CC and PEUE, a higher biomass RGR resulted for the invasive group; also at a common SLA, a lower CC but higher N resulted for the invasive group. Overall, trait co-ordination (using pair-wise correlation analyses) was better in the invasive group. Ordination using 16 leaf traits indicated that the major axis of invasive-native dichotomy is primarily driven by SLA and CC (including its components and/or derivative of PEUE) and was significantly linked with RGR.
Conclusions
These results demonstrated that while not all measures of leaf resource traits may differ between the two groups, the higher level of trait correlation and higher revenue returned (RGR) per unit of major resource need (CC) and use (PEUE) in the invasive group is in line with their rapid spread where introduced.
doi:10.1093/aob/mcq119
PMCID: PMC2908172  PMID: 20534595
Construction cost; leaf physico-chemical properties; plant invasion; photosynthesis; resource-use efficiency; specific leaf area; woody vines; Anredera; Araujia; Cardiospermum; Macfadyena; Pandorea; Parsonsia
12.  The scaling of leaf area and mass: the cost of light interception increases with leaf size 
For leaves, the light-capturing surface area per unit dry mass investment (specific leaf area, SLA) is a key trait from physiological, ecological and biophysical perspectives. To address whether SLA declines with leaf size, as hypothesized due to increasing costs of support in larger leaves, we compiled data on intraspecific variation in leaf dry mass (LM) and leaf surface area (LA) for 6334 leaves of 157 species. We used the power function LM=α LAβ to test whether, within each species, large leaves deploy less surface area per unit dry mass than small leaves. Comparing scaling exponents (β) showed that more species had a statistically significant decrease in SLA as leaf size increased (61) than the opposite (7) and the average β was significantly greater than 1 (βmean=1.10, 95% CI 1.08–1.13). However, scaling exponents varied markedly from the few species that decreased to the many that increased SLA disproportionately fast as leaf size increased. This variation was unrelated to growth form, ecosystem of origin or climate. The average within-species tendency found here (allometric decrease of SLA with leaf size, averaging 13%) is in accord with concurrent findings on global-scale trends among species, although the substantial scatter around the central tendency suggests that the leaf size dependency does not obligately shape SLA. Nonetheless, the generally greater mass per unit leaf area of larger than smaller leaves directly translates into a greater cost to build and maintain a unit of leaf area, which, all else being equal, should constrain the maximum leaf size displayed.
doi:10.1098/rspb.2007.0417
PMCID: PMC2706187  PMID: 17591590
leaf area; leaf mass; specific leaf area; allometry; scaling; power laws.
13.  Seedling Stage Strategies as a Means of Habitat Specialization in Herbaceous Plants 
PLoS ONE  2011;6(7):e23006.
The regeneration niche has been little investigated in studies of community assembly and plant distribution. We examined adaptive associations between seedling traits and habitat specialization. Two habitat contrasts were investigated across several evolutionary lineages of angiosperms: species specialized to forest vs. open habitats and to dry vs. wet habitats. We also tested whether effects of shade and drought vary independently or, alternatively, if shade may amplify effects on drought-stressed plants. Seedling response in terms of growth rate, height, slenderness, specific leaf area (SLA) and degree of elongation (longest internode; petiole or leaf-sheath depending on species' morphology) to light and watering treatments was assessed. We used a factorial design involving three light regimes and two watering frequencies. The open-shaded habitat contrast and the dry-wet habitat contrast were investigated using six and five pairs of congeneric species, respectively. The congeneric species pair design controlled for confounding effects of evolutionary history prior to divergence in habitat specialization. Seedling growth rate generally decreased with shade and reduced watering frequency. Plant height was generally largest at intermediate light. Specialization to shaded habitats was associated with a more conservative growth strategy, i.e. showing a more modest growth response to increasing light. Species from all habitats showed the highest relative elongation at intermediate light, except for the moist-habitat species, for which elongation increased with shade. Contrary to our expectations, species from dry habitats grew bigger than species from moist habitats in all treatments. SLA responded to the light treatment, but not to watering regime. The contrasting light and moisture conditions across habitats appear to not have selected for differences in SLA. We conclude that seedling phase strategies of resource allocation in temperate herbs contribute to their habitat specialization. Habitat-specific seedling strategies and trade-offs in response to resource availability and environmental conditions may be important to adaptive specialization.
doi:10.1371/journal.pone.0023006
PMCID: PMC3146528  PMID: 21829576
14.  Intraspecific Relationships among Wood Density, Leaf Structural Traits and Environment in Four Co-Occurring Species of Nothofagus in New Zealand 
PLoS ONE  2013;8(3):e58878.
Plant functional traits capture important variation in plant strategy and function. Recent literature has revealed that within-species variation in traits is greater than previously supposed. However, we still have a poor understanding of how intraspecific variation is coordinated among different traits, and how it is driven by environment. We quantified intraspecific variation in wood density and five leaf traits underpinning the leaf economics spectrum (leaf dry matter content, leaf mass per unit area, size, thickness and density) within and among four widespread Nothofagus tree species in southern New Zealand. We tested whether intraspecific relationships between wood density and leaf traits followed widely reported interspecific relationships, and whether variation in these traits was coordinated through shared responses to environmental factors. Sample sites varied widely in environmental variables, including soil fertility (25–900 mg kg–1 total P), precipitation (668–4875 mm yr–1), temperature (5.2–12.4 °C mean annual temperature) and latitude (41–46 °S). Leaf traits were strongly correlated with one another within species, but not with wood density. There was some evidence for a positive relationship between wood density and leaf tissue density and dry matter content, but no evidence that leaf mass or leaf size were correlated with wood density; this highlights that leaf mass per unit area cannot be used as a surrogate for component leaf traits such as tissue density. Trait variation was predicted by environmental factors, but not consistently among different traits; e.g., only leaf thickness and leaf density responded to the same environmental cues as wood density. We conclude that although intraspecific variation in wood density and leaf traits is strongly driven by environmental factors, these responses are not strongly coordinated among functional traits even across co-occurring, closely-related plant species.
doi:10.1371/journal.pone.0058878
PMCID: PMC3601108  PMID: 23527041
15.  UV radiation is the primary factor driving the variation in leaf phenolics across Chinese grasslands 
Ecology and Evolution  2013;3(14):4696-4710.
Due to the role leaf phenolics in defending against ultraviolet B (UVB) under previously controlled conditions, we hypothesize that ultraviolet radiation (UVR) could be a primary factor driving the variation in leaf phenolics in plants over a large geographic scale. We measured leaf total phenolics, ultraviolet-absorbing compounds (UVAC), and corresponding leaf N, P, and specific leaf area (SLA) in 151 common species. These species were from 84 sites across the Tibetan Plateau and Inner Mongolian grasslands of China with contrasting UVR (354 vs. 161 mW/cm2 on average). Overall, leaf phenolics and UVAC were all significantly higher on the Tibetan Plateau than in the Inner Mongolian grasslands, independent of phylogenetic relationships between species. Regression analyses showed that the variation in leaf phenolics was strongly affected by climatic factors, particularly UVR, and soil attributes across all sites. Structural equation modeling (SEM) identified the primary role of UVR in determining leaf phenolic concentrations, after accounting for colinearities with altitude, climatic, and edaphic factors. In addition, phenolics correlated positively with UVAC and SLA, and negatively with leaf N and N: P. These relationships were steeper in the lower-elevation Inner Mongolian than on the Tibetan Plateau grasslands. Our data support that the variation in leaf phenolics is controlled mainly by UV radiation, implying high leaf phenolics facilitates the adaptation of plants to strong irradiation via its UV-screening and/or antioxidation functions, particularly on the Tibetan Plateau. Importantly, our results also suggest that leaf phenolics may influence on vegetation attributes and indirectly affect ecosystem processes by covarying with leaf functional traits.
doi:10.1002/ece3.862
PMCID: PMC3867905  PMID: 24363898
Inner Mongolia; leaf functional traits; leaf phenolics; Tibetan Plateau; ultraviolet absorbing compounds; UV radiation
16.  Relationship between Maximum Leaf Photosynthesis, Nitrogen Content and Specific Leaf Area in Balearic Endemic and Non‐endemic Mediterranean Species 
Annals of Botany  2003;92(2):215-222.
Gas exchange parameters, leaf nitrogen content and specific leaf area (SLA) were measured in situ on 73 C3 and five C4 plant species in Mallorca, west Mediterranean, to test whether species endemic to the Balearic Islands differed from widespread, non‐endemic Mediterranean species and crops in their leaf traits and trait inter‐relationships. Endemic species differed significantly from widespread species and crops in several parameters; in particular, photosynthetic capacity, on an area basis (A), was 20 % less in endemics than in non‐endemics. Similar differences between endemics and non‐endemics were found in parameters such as SLA and leaf nitrogen content per area (Na). Nevertheless, most of the observed differences were found only within the herbaceous deciduous species. These could be due to the fact that most of the non‐endemic species within this group have adapted to ruderal areas, while none of the endemics occupies this kind of habitat. All the species—including the crops—showed a positive, highly significant correlation between photosynthetic capacity on a mass basis (Am), leaf nitrogen content on a mass basis (Nm) and SLA. However, endemic species had a lower Am for any given SLA and Nm. Hypotheses are presented to explain these differences, and their possible role in reducing the distribution of many endemic Balearic species is discussed.
doi:10.1093/aob/mcg123
PMCID: PMC4243646  PMID: 12805082
Balearic endemic species; leaf nitrogen content; Mediterranean climate; photosynthesis; specific leaf area
17.  The relationship of leaf photosynthetic traits – Vcmax and Jmax – to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study 
Ecology and Evolution  2014;4(16):3218-3235.
Great uncertainty exists in the global exchange of carbon between the atmosphere and the terrestrial biosphere. An important source of this uncertainty lies in the dependency of photosynthesis on the maximum rate of carboxylation (Vcmax) and the maximum rate of electron transport (Jmax). Understanding and making accurate prediction of C fluxes thus requires accurate characterization of these rates and their relationship with plant nutrient status over large geographic scales. Plant nutrient status is indicated by the traits: leaf nitrogen (N), leaf phosphorus (P), and specific leaf area (SLA). Correlations between Vcmax and Jmax and leaf nitrogen (N) are typically derived from local to global scales, while correlations with leaf phosphorus (P) and specific leaf area (SLA) have typically been derived at a local scale. Thus, there is no global-scale relationship between Vcmax and Jmax and P or SLA limiting the ability of global-scale carbon flux models do not account for P or SLA. We gathered published data from 24 studies to reveal global relationships of Vcmax and Jmax with leaf N, P, and SLA. Vcmax was strongly related to leaf N, and increasing leaf P substantially increased the sensitivity of Vcmax to leaf N. Jmax was strongly related to Vcmax, and neither leaf N, P, or SLA had a substantial impact on the relationship. Although more data are needed to expand the applicability of the relationship, we show leaf P is a globally important determinant of photosynthetic rates. In a model of photosynthesis, we showed that at high leaf N (3 gm−2), increasing leaf P from 0.05 to 0.22 gm−2 nearly doubled assimilation rates. Finally, we show that plants may employ a conservative strategy of Jmax to Vcmax coordination that restricts photoinhibition when carboxylation is limiting at the expense of maximizing photosynthetic rates when light is limiting.
doi:10.1002/ece3.1173
PMCID: PMC4222209  PMID: 25473475
Carbon assimilation; carbon cycle; carboxylation; DGVM; electron transport; Farquhar model; land surface model; meta-analysis; mixed-effect multiple regression; noncarbon photosynthesis; TBM
18.  Relationships between Nutrient-Related Plant Traits and Combinations of Soil N and P Fertility Measures 
PLoS ONE  2013;8(12):e83735.
Soil fertility and nutrient-related plant functional traits are in general only moderately related, hindering the progress in trait-based prediction models of vegetation patterns. Although the relationships may have been obscured by suboptimal choices in how soil fertility is expressed, there has never been a systematic investigation into the suitability of fertility measures. This study, therefore, examined the effect of different soil fertility measures on the strength of fertility–trait relationships in 134 natural plant communities. In particular, for eight plot-mean traits we examined (1) whether different elements (N or P) have contrasting or shared influences, (2) which timescale of fertility measures (e.g. mineralization rates for one or five years) has better predictive power, and (3) if integrated fertility measures explain trait variation better than individual fertility measures. Soil N and P had large mutual effects on leaf nutrient concentrations, whereas they had element-specific effects on traits related to species composition (e.g. Grime's CSR strategy). The timescale of fertility measures only had a minor impact on fertility–trait relationships. Two integrated fertility measures (one reflecting overall fertility, another relative availability of soil N and P) were related significantly to most plant traits, but were not better in explaining trait variation than individual fertility measures. Using all fertility measures together, between-site variations of plant traits were explained only moderately for some traits (e.g. 33% for leaf N concentrations) but largely for others (e.g. 66% for whole-canopy P concentration). The moderate relationships were probably due to complex regulation mechanisms of fertility on traits, rather than to a wrong choice of fertility measures. We identified both mutual (i.e. shared) and divergent (i.e. element-specific and stoichiometric) effects of soil N and P on traits, implying the importance of explicitly considering the roles of different elements to properly interpret fertility–trait relationships.
doi:10.1371/journal.pone.0083735
PMCID: PMC3877083  PMID: 24391815
19.  A Comparison of the Functional Traits of Common Reed (Phragmites australis) in Northern China: Aquatic vs. Terrestrial Ecotypes 
PLoS ONE  2014;9(2):e89063.
Common reed (Phragmites australis (Cav.) Trin. ex Steud.) is distributed widely throughout the world with various ecotypes. This research compares the functional traits and biomass allocation patterns of two contrasting reed ecotypes. Twelve pairs of aquatic and terrestrial reed samples were collected in northern China. Significant differences in functional traits between the two reed ecotypes were observed, while biomass allocation patterns of reed organs did not differ significantly except for at the root. The dry matter content (DMC) in the whole of the reed plant, leaf, root, and rhizome was higher; while the specific leaf area (SLA) and specific root length (SRL) were lower in terrestrial versus aquatic reed. The biomass allocation in organs of the two forms of reed was isometric, only root in the terrestrial habitat increased faster with an increase in the whole plant biomass. It can be affirmed that aquatic and terrestrial reed that adapt to different environments generally has distinct leaf and root functional traits but isometric biomass allocation patterns. This suggests different resource acquisition strategies: (1) aquatic reed grows faster with high SLA and SRL and is more responsive to the environment, while (2) terrestrial reed with high DMC grows slower and is less responsive to the adverse environment (e.g. dry soil conditions).
doi:10.1371/journal.pone.0089063
PMCID: PMC3929632  PMID: 24586505
20.  Responses of leaf structure and photosynthetic properties to intra-canopy light gradients: a common garden test with four broadleaf deciduous angiosperm and seven evergreen conifer tree species 
Oecologia  2012;170(1):11-24.
Spectra of leaf traits in northern temperate forest canopies reflect major differences in leaf longevity between evergreen conifers and deciduous broadleaf angiosperms, as well as plastic modifications caused by within-crown shading. We investigated (1) whether long-lived conifer leaves exhibit similar intra-canopy plasticity as short-lived broadleaves, and (2) whether global interspecific relationships between photosynthesis, nitrogen, and leaf structure identified for sun leaves adequately describe leaves differentiated in response to light gradients. We studied structural and photosynthetic properties of intra-tree sun and shade foliage in adult trees of seven conifer and four broadleaf angiosperm species in a common garden in Poland. Shade leaves exhibited lower leaf mass-per-area (LMA) than sun leaves; however, the relative difference was smaller in conifers than in broadleaves. In broadleaves, LMA was correlated with lamina thickness and tissue density, while in conifers, it was correlated with thickness but not density. In broadleaves, but not in conifers, reduction of lamina thickness was correlated with a thinner palisade layer. The more conservative adjustment of conifer leaves could result from a combination of phylogenetic constraints, contrasting leaf anatomies and shoot geometries, but also from functional requirements of long-lived foliage. Mass-based nitrogen concentration (Nmass) was similar between sun and shade leaves, and was lower in conifers than in deciduous broadleaved species. Given this, the smaller LMA in shade corresponded with a lower area-based N concentration (Narea). In evergreen conifers, LMA and Narea were less powerful predictors of area-based photosynthetic rate (Amax(area)) in comparison with deciduous broadleaved angiosperms. Multiple regression for sun and shade leaves showed that, in each group, Amax(mass) was related to Nmass but not to LMA, whereas LMA became a significant codeterminant of Amax(mass) in analysis combining both groups. Thus, a fundamental mass-based relationship between photosynthesis, nitrogen, and leaf structure reported previously also exists in a dataset combining within-crown and across-functional type variation.
Electronic supplementary material
The online version of this article (doi:10.1007/s00442-012-2279-y) contains supplementary material, which is available to authorized users.
doi:10.1007/s00442-012-2279-y
PMCID: PMC3422461  PMID: 22349756
Plant functional types; Leaf plasticity; Shade acclimation; Evergreen leaves; Leaf mass-per-area
21.  Functional Trait Trade-Offs for the Tropical Montane Rain Forest Species Responding to Light from Simulating Experiments 
The Scientific World Journal  2014;2014:649031.
Differences among tropical tree species in survival and growth to light play a key role in plant competition and community composition. Two canopy species with contrasting functional traits dominating early and late successional stages, respectively, in a tropical montane rain forest of Hainan Island, China, were selected in a pot experiment under 4 levels of light intensity (full, 50%, 30%, and 10%) in order to explore the adaptive strategies of tropical trees to light conditions. Under each light intensity level, the pioneer species, Endospermum chinense (Euphorbiaceae), had higher relative growth rate (RGR), stem mass ratio (SMR), specific leaf area (SLA), and morphological plasticity while the shade tolerant climax species, Parakmeria lotungensis (Magnoliaceae), had higher root mass ratio (RMR) and leaf mass ratio (LMR). RGR of both species was positively related to SMR and SLA under each light level but was negatively correlated with RMR under lower light (30% and 10% full light). The climax species increased its survival by a conservative resource use strategy through increasing leaf defense and root biomass investment at the expense of growth rate in low light. In contrast, the pioneer increased its growth by an exploitative resource use strategy through increasing leaf photosynthetic capacity and stem biomass investment at the expense of survival under low light. There was a trade-off between growth and survival for species under different light conditions. Our study suggests that tree species in the tropical rainforest adopt different strategies in stands of different successional stages. Species in the earlier successional stages have functional traits more advantageous to grow faster in the high light conditions, whereas species in the late successional stages have traits more favorable to survive in the low light conditions.
doi:10.1155/2014/649031
PMCID: PMC4075036  PMID: 25019095
22.  Leaf Structural and Photosynthetic Characteristics, and Biomass Allocation to Foliage in Relation to Foliar Nitrogen Content and Tree Size in Three Betula Species 
Annals of Botany  2002;89(2):191-204.
Young trees 0·03–1·7 m high of three coexisting Betula species were investigated in four sites of varying soil fertility, but all in full daylight, to separate nutrient and plant size controls on leaf dry mass per unit area (MA), light‐saturated foliar photosynthetic electron transport rate (J) and the fraction of plant biomass in foliage (FL). Because the site effect was generally non‐significant in the analyses of variance with foliar nitrogen content per unit dry mass (NM) as a covariate, NM was used as an explaining variable of leaf structural and physiological characteristics. Average leaf area (S) and dry mass per leaf scaled positively with NM and total tree height (H) in all species. Leaf dry mass per unit area also increased with increasing H, but decreased with increasing NM, whereas the effects were species‐specific. Increases in plant size led to a lower and increases in NM to a greater FL and total plant foliar area per unit plant biomass (LAR). Thus, the self‐shading probably increased with increasing NM and decreased with increasing H. Nevertheless, the whole‐plant average MA, as well as MA values of topmost fully exposed leaves, correlated with NM and H in a similar manner, indicating that scaling of MA with NM and H did not necessarily result from the modified degree of within‐plant shading. The rate of photosynthetic electron transport per unit dry mass (JM) scaled positively with NM, but decreased with increasing H and MA. Thus, increases in MA with tree height and decreasing nitrogen content not only resulted in a lower plant foliar area (LAR = FL/MA), but also led to lower physiological activity of unit foliar biomass. The leaf parameters (JM, NM and MA) varied threefold, but the whole‐plant characteristic FL varied 20‐fold and LAR 30‐fold, indicating that the biomass allocation was more plastically adjusted to different plant internal nitrogen contents and to tree height than the foliar variables. Our results demonstrate that: (1) tree height and NM may independently control foliar structure and physiology, and have an even greater impact on biomass allocation; and (2) the modified within‐plant light availabilities alone do not explain the observed patterns. Although there were interspecific differences with respect to the statistical significance of the relationships, all species generally fit common regressions. However, these differences were consistent, and suggested that more competitive species with inherently larger growth rates also more plastically respond to N and H.
doi:10.1093/aob/mcf025
PMCID: PMC4233790  PMID: 12099350
Betula nana; Betula pendula; Betula pubescens; construction cost; leaf density; leaf dry mass per unit area; leaf size; nitrogen content; photosynthetic electron transport rate; plasticity; tree height
23.  Species-specific Variation in the Importance of the Spectral Quality Gradient in Canopies as a Signal for Photosynthetic Resource Partitioning 
Annals of Botany  2004;94(5):725-732.
• Background and Aims Plants adjust the distribution of photosynthetic capacity and chlorophyll to canopy density. The importance of the gradient in the red : far-red ratio (R : FR) relative to the irradiance gradient was studied for its perception with respect to this partitioning of photosynthetic resources. Whether the relative importance of these two signals varied between six species of different growth habit (Phaseolus vulgaris, Lysimachia vulgaris, Hedera helix, Ficus benjamina, Carex acutiformis and Brachypodium pinnatum) was investigated further.
• Methods Single leaves of plants were shaded in daylight by a spectrally neutral filter or a leaf. In another experiment, leaves were treated with supplemental FR. In most cases, treatment effects were evaluated after 2 weeks.
• Key Results Nitrogen and photosynthetic capacity (Amax) per leaf area, parameters pertaining to between-leaf resource partitioning, were strongly reduced in neutral shade but not additionally by spectral leaf shade. Supplemental FR reduced these parameters also, except in Carex. Acceleration of induction of senescence was observed in spectral leaf shade in primary bean leaves. Amax per unit chlorophyll, a parameter pertaining to within-leaf resource partitioning, was reduced in neutral shade, but not in spectral leaf shade or supplemental FR.
• Conclusions Signalling mechanisms associated with perception of the R : FR gradient in canopies were less important than those associated with the irradiance gradient for between-leaf and within-leaf partitioning of photosynthetic resources. The relative importance of the signals differed between species because Carex was the only species for which no indications were found for an involvement of the spectral gradient in perception of canopy density.
doi:10.1093/aob/mch197
PMCID: PMC4242218  PMID: 15374835
Chlorophyll; herbaceous dicotyledonous species; irradiance; leaf canopies; light gradient; monocotyledonous species; photosynthetic capacity; photosynthetic resource partitioning; red : far-red ratio; spectral quality; shade acclimation; woody species
24.  Seedling Growth Strategies in Bauhinia Species: Comparing Lianas and Trees 
Annals of Botany  2007;100(4):831-838.
Background and Aims
Lianas are expected to differ from trees in their growth strategies. As a result these two groups of woody species will have different spatial distributions: lianas are more common in high light environments. This study determines the differences in growth patterns, biomass allocation and leaf traits in five closely related liana and tree species of the genus Bauhinia.
Methods
Seedlings of two light-demanding lianas (Bauhinia tenuiflora and B. claviflora), one shade-tolerant liana (B. aurea), and two light-demanding trees (B. purpurea and B. monandra) were grown in a shadehouse at 25 % of full sunlight. A range of physiological, morphological and biomass parameters at the leaf and whole plant level were compared among these five species.
Key Results
The two light-demanding liana species had higher relative growth rate (RGR), allocated more biomass to leaf production [higher leaf mass fraction (LMF) and higher leaf area ratio (LAR)] and stem mass fraction (SMF), and less biomass to the roots [root mass fraction (RMF)] than the two tree species. The shade-tolerant liana had the lowest RGR of all five species, and had a higher RMF, lower SMF and similar LMF than the two light-demanding liana species. The two light-demanding lianas had lower photosynthetic rates per unit area (Aarea) and similar photosynthetic rates per unit mass (Amass) than the trees. Across species, RGR was positively related to SLA, but not to LAR and Aarea.
Conclusions
It is concluded that the faster growth of light-demanding lianas compared with light-demanding trees is based on morphological parameters (SLA, LMF and LAR), and cannot be attributed to higher photosynthetic rates at the leaf level. The shade-tolerant liana exhibited a slow-growth strategy, compared with the light-demanding species.
doi:10.1093/aob/mcm179
PMCID: PMC2749636  PMID: 17720978
Relative growth rate; biomass allocation; shade tolerance; liana; tree; photosynthesis; Bauhinia
25.  Plant Diversity Changes during the Postglacial in East Asia: Insights from Forest Refugia on Halla Volcano, Jeju Island 
PLoS ONE  2012;7(3):e33065.
Understanding how past climate changes affected biodiversity is a key issue in contemporary ecology and conservation biology. These diversity changes are, however, difficult to reconstruct from paleoecological sources alone, because macrofossil and pollen records do not provide complete information about species assemblages. Ecologists therefore use information from modern analogues of past communities in order to get a better understanding of past diversity changes. Here we compare plant diversity, species traits and environment between late-glacial Abies, early-Holocene Quercus, and mid-Holocene warm-temperate Carpinus forest refugia on Jeju Island, Korea in order to provide insights into postglacial changes associated with their replacement. Based on detailed study of relict communities, we propose that the late-glacial open-canopy conifer forests in southern part of Korean Peninsula were rich in vascular plants, in particular of heliophilous herbs, whose dramatic decline was caused by the early Holocene invasion of dwarf bamboo into the understory of Quercus forests, followed by mid-Holocene expansion of strongly shading trees such as maple and hornbeam. This diversity loss was partly compensated in the Carpinus forests by an increase in shade-tolerant evergreen trees, shrubs and lianas. However, the pool of these species is much smaller than that of light-demanding herbs, and hence the total species richness is lower, both locally and in the whole area of the Carpinus and Quercus forests. The strongly shading tree species dominating in the hornbeam forests have higher leaf tissue N and P concentrations and smaller leaf dry matter content, which enhances litter decomposition and nutrient cycling and in turn favored the selection of highly competitive species in the shrub layer. This further reduced available light and caused almost complete disappearance of understory herbs, including dwarf bamboo.
doi:10.1371/journal.pone.0033065
PMCID: PMC3306376  PMID: 22438890

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