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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.
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.
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.
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.
PMCID: PMC4247101  PMID: 16159941
Leaf thickness; specific leaf area; leaf dry matter content; leaf density; interspecific variation; global comparative analysis
3.  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).
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.
PMCID: PMC2802913  PMID: 17353207
Argentina; leaf dry matter content; leaf rehydration; plant comparative ecology; plant functional traits
4.  Plant Trait Assembly Affects Superiority of Grazer's Foraging Strategies in Species-Rich Grasslands 
PLoS ONE  2013;8(7):e69800.
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.
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.
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.
PMCID: PMC3724891  PMID: 23922805
5.  A Functional Characterisation of a Wide Range of Cover Crop Species: Growth and Nitrogen Acquisition Rates, Leaf Traits and Ecological Strategies 
PLoS ONE  2015;10(3):e0122156.
Cover crops can produce ecosystem services during the fallow period, as reducing nitrate leaching and producing green manure. Crop growth rate (CGR) and crop nitrogen acquisition rate (CNR) can be used as two indicators of the ability of cover crops to produce these services in agrosystems. We used leaf functional traits to characterise the growth strategies of 36 cover crops as an approach to assess their ability to grow and acquire N rapidly. We measured specific leaf area (SLA), leaf dry matter content (LDMC), leaf nitrogen content (LNC) and leaf area (LA) and we evaluated their relevance to characterise CGR and CNR. Cover crop species were positioned along the Leaf Economics Spectrum (LES), the SLA-LDMC plane, and the CSR triangle of plant strategies. LA was positively correlated with CGR and CNR, while LDMC was negatively correlated with CNR. All cover crops could be classified as resource-acquisitive species from their relative position on the LES and the SLA-LDMC plane. Most cover crops were located along the Competition/Ruderality axis in the CSR triangle. In particular, Brassicaceae species were classified as very competitive, which was consistent with their high CGR and CNR. Leaf functional traits, especially LA and LDMC, allowed to differentiate some cover crops strategies related to their ability to grow and acquire N. LDMC was lower and LNC was higher in cover crop than in wild species, pointing to an efficient acquisitive syndrome in the former, corresponding to the high resource availability found in agrosystems. Combining several leaf traits explained approximately half of the CGR and CNR variances, which might be considered insufficient to precisely characterise and rank cover crop species for agronomic purposes. We hypothesised that may be the consequence of domestication process, which has reduced the range of plant strategies and modified the leaf trait syndrome in cultivated species.
PMCID: PMC4366015  PMID: 25789485
6.  C:N:P Stoichiometry and Leaf Traits of Halophytes in an Arid Saline Environment, Northwest China 
PLoS ONE  2015;10(3):e0119935.
Salinization is an important and increasingly prevalent issue which has broad and profound effects on plant survival and distribution pattern. To understand the patterns and potential drivers of leaf traits in saline environments, we determined the soil properties, leaf morphological traits (specific leaf area, SLA, and leaf dry matter content, LDMC), leaf chemical traits (leaf carbon, C, nitrogen, N, and phosphorus, P, stoichiometry) based on 142 observations collected from 23 sites in an arid saline environment, which is a vulnerable ecosystem in northwest China. We also explored the relationships among leaf traits, the responses of leaf traits, and plant functional groups (herb, woody, and succulent woody) to various saline environments. The arid desert halophytes were characterized by lower leaf C and SLA levels, higher N, but stable P and N:P. The leaf morphological traits were correlated significantly with the C, N, and P contents across all observations, but they differed within each functional group. Succulent woody plants had the lowest leaf C and highest leaf N levels among the three functional groups. The growth of halophytes might be more limited by N rather than P in the study area. GLM analysis demonstrated that the soil available nutrients and plant functional groups, but not salinity, were potential drivers of leaf C:N:P stoichiometry in halophytes, whereas species differences accounted for the largest contributions to leaf morphological variations. Our study provides baseline information to facilitate the management and restoration of arid saline desert ecosystem.
PMCID: PMC4370893  PMID: 25798853
7.  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.
PMCID: PMC3335023  PMID: 22536448
8.  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.
PMCID: PMC4203824  PMID: 25329794
9.  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.
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.
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.
PMCID: PMC2802959  PMID: 17237213
Functional traits; leaf dry matter content; Mediterranean plants; post-fire; regenerative strategy; relative water content; resprouter; seeder; woody species
10.  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.
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.
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.
PMCID: PMC2990665  PMID: 20880932
Adaptive plasticity; age at reproduction; Arabidopsis thaliana; functional traits; soil pH; rosette growth form; size at reproduction; SLA
11.  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.
PMCID: PMC4038439  PMID: 24790129
Alpine vegetation; community composition; functional composition; functional traits; GLORIA; Snowy Mountains.
12.  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.
PMCID: PMC3631414  PMID: 23610644
Intraspecific variation; light availability; plant functional traits; plant physiological ecology; seabird burrowing; soil nutrients; specific leaf area; specific root length
13.  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.
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.
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.
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
14.  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.
PMCID: PMC3146528  PMID: 21829576
15.  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.
PMCID: PMC2706187  PMID: 17591590
leaf area; leaf mass; specific leaf area; allometry; scaling; power laws.
16.  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.
PMCID: PMC3601108  PMID: 23527041
17.  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.
PMCID: PMC3877083  PMID: 24391815
18.  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.
PMCID: PMC3867905  PMID: 24363898
Inner Mongolia; leaf functional traits; leaf phenolics; Tibetan Plateau; ultraviolet absorbing compounds; UV radiation
19.  Leaf economics of evergreen and deciduous tree species along an elevational gradient in a subtropical mountain 
AoB Plants  2015;7:plv064.
We used leaf economics spectrum (LES) theory to explain the bimodal elevational distribution of evergreen tree species, which is one of the most puzzling biogeographic patterns in the world. Our results suggest that elevation acts as an environmental filter to both select the locally adapted evergreen and deciduous species with sufficient phylogenetic variation and distinct leaf economic strategies and regulate their distribution along the elevational gradient based on their coordinated spreading of phylogenetic divergence and leaf economic variation. If species are filtered from regional species pools, changing climate may affect both the species and leaf economic composition of plant communities.
The ecophysiological mechanisms underlying the pattern of bimodal elevational distribution of evergreen tree species remain incompletely understood. Here we used leaf economics spectrum (LES) theory to explain such patterns. We measured leaf economic traits and constructed an LES for the co-existing 19 evergreen and 15 deciduous species growing in evergreen broad-leaved forest at low elevation, beech-mixed forest at middle elevation and hemlock-mixed forest at high elevation in Mao'er Mountain, Guangxi, Southern China (25°50′N, 110°49′E). Leaf economic traits presented low but significant phylogenetic signal, suggesting trait similarity between closely related species. After considering the effects of phylogenetic history, deciduous species in general showed a more acquisitive leaf strategy with a higher ratio of leaf water to dry mass, higher leaf nitrogen and phosphorous contents, higher photosynthetic and respiratory rates and greater photosynthetic nitrogen-use efficiency. In contrast, evergreen species exhibited a more conservative leaf strategy with higher leaf mass per area, greater construction costs and longer leaf life span. With the elevation-induced decreases of temperature and soil fertility, both evergreen and deciduous species showed greater resource conservation, suggesting the increasing importance of environmental filtering to community assembly with increasing elevation. We found close inter-specific correlations between leaf economic traits, suggesting that there are strong genetic constraints limiting the independent evolution of LES traits. Phylogenetic signal increased with decreasing evolutionary rate across leaf economic traits, suggesting that genetic constraints are important for the process of trait evolution. We found a significantly positive relationship between primary axis species score (PASS) distance and phylogenetic distance across species pairs and an increasing average PASS distance between evergreen and deciduous species with increasing elevation, implying that the frequency of distantly related evergreen and deciduous pairs with wide spreading of leaf economic values increases with increasing elevation. Our findings thus suggest that elevation acts as an environmental filter to both select the locally adapted evergreen and deciduous species with sufficient phylogenetic variation and regulate their distribution along the elevational gradient based on their coordinated spreading of phylogenetic divergence and leaf economic variation.
PMCID: PMC4571104  PMID: 26056133
Bimodal distribution; deciduous tree species; elevation; evergreen tree species; leaf economics spectrum; phylogenetic comparative methods; phylogenetic distance
20.  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.
PMCID: PMC4243646  PMID: 12805082
Balearic endemic species; leaf nitrogen content; Mediterranean climate; photosynthesis; specific leaf area
21.  Development and validation of an epitope prediction tool for swine (PigMatrix) based on the pocket profile method 
BMC Bioinformatics  2015;16(1):290.
T cell epitope prediction tools and associated vaccine design algorithms have accelerated the development of vaccines for humans. Predictive tools for swine and other food animals are not as well developed, primarily because the data required to develop the tools are lacking. Here, we overcome a lack of T cell epitope data to construct swine epitope predictors by systematically leveraging available human information. Applying the “pocket profile method”, we use sequence and structural similarities in the binding pockets of human and swine major histocompatibility complex proteins to infer Swine Leukocyte Antigen (SLA) peptide binding preferences.
We developed epitope-prediction matrices (PigMatrices), for three SLA class I alleles (SLA-1*0401, 2*0401 and 3*0401) and one class II allele (SLA-DRB1*0201), based on the binding preferences of the best-matched Human Leukocyte Antigen (HLA) pocket for each SLA pocket. The contact residues involved in the binding pockets were defined for class I based on crystal structures of either SLA (SLA-specific contacts, Ssc) or HLA supertype alleles (HLA contacts, Hc); for class II, only Hc was possible. Different substitution matrices were evaluated (PAM and BLOSUM) for scoring pocket similarity and identifying the best human match. The accuracy of the PigMatrices was compared to available online swine epitope prediction tools such as PickPocket and NetMHCpan.
PigMatrices that used Ssc to define the pocket sequences and PAM30 to score pocket similarity demonstrated the best predictive performance and were able to accurately separate binders from random peptides. For SLA-1*0401 and 2*0401, PigMatrix achieved area under the receiver operating characteristic curves (AUC) of 0.78 and 0.73, respectively, which were equivalent or better than PickPocket (0.76 and 0.54) and NetMHCpan version 2.4 (0.41 and 0.51) and version 2.8 (0.72 and 0.71). In addition, we developed the first predictive SLA class II matrix, obtaining an AUC of 0.73 for existing SLA-DRB1*0201 epitopes. Notably, PigMatrix achieved this level of predictive power without training on SLA binding data.
Overall, the pocket profile method combined with binding preferences from HLA binding data shows significant promise for developing T cell epitope prediction tools for pigs. When combined with existing vaccine design algorithms, PigMatrix will be useful for developing genome-derived vaccines for a range of pig pathogens for which no effective vaccines currently exist (e.g. porcine reproductive and respiratory syndrome, influenza and porcine epidemic diarrhea).
Electronic supplementary material
The online version of this article (doi:10.1186/s12859-015-0724-8) contains supplementary material, which is available to authorized users.
PMCID: PMC4570239  PMID: 26370412
PigMatrix; EpiMatrix; Computational vaccinology; Epitope prediction; HLA; SLA; MHC; Class I; Class II; Porcine; PRRSV; Influenza; Genome-derived vaccine; T cell epitope
22.  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).
PMCID: PMC3929632  PMID: 24586505
23.  Trait differences between naturalized and invasive plant species independent of residence time and phylogeny 
Conservation Biology  2014;29(2):360-369.
The ability to predict which alien plants will transition from naturalized to invasive prior to their introduction to novel regions is a key goal for conservation and has the potential to increase the efficacy of weed risk assessment (WRA). However, multiple factors contribute to plant invasion success (e.g., functional traits, range characteristics, residence time, phylogeny), and they all must be taken into account simultaneously in order to identify meaningful correlates of invasion success. We compiled 146 pairs of phylogenetically paired (congeneric) naturalized and invasive plant species in Australia with similar minimum residence times (i.e., time since introduction in years). These pairs were used to test for differences in 5 functional traits (flowering duration, leaf size, maximum height, specific leaf area [SLA], seed mass) and 3 characteristics of species’ native ranges (biome occupancy, mean annual temperature, and rainfall breadth) between naturalized and invasive species. Invasive species, on average, had larger SLA, longer flowering periods, and were taller than their congeneric naturalized relatives. Invaders also exhibited greater tolerance for different environmental conditions in the native range, where they occupied more biomes and a wider breadth of rainfall and temperature conditions than naturalized congeners. However, neither seed mass nor leaf size differed between pairs of naturalized and invasive species. A key finding was the role of SLA in distinguishing between naturalized and invasive pairs. Species with high SLA values were typically associated with faster growth rates, more rapid turnover of leaf material, and shorter lifespans than those species with low SLA. This suite of characteristics may contribute to the ability of a species to transition from naturalized to invasive across a wide range of environmental contexts and disturbance regimes. Our findings will help in the refinement of WRA protocols, and we advocate the inclusion of quantitative traits, in particular SLA, into the WRA schemes.
Diferencia de Características entre Especies de Plantas Naturalizadas e Invasoras Independientes del Tiempo de Residencia y de la Filogenia
La habilidad para predecir cuáles plantas exóticas harán la transición de naturalizadas a invasoras antes de su introducción a regiones nuevas es un objetivo clave para la conservación y tiene el potencial de incrementar la eficiencia de la evaluación de riesgo de hierbas (ERH). Sin embargo, múltiples factores contribuyen al éxito invasor de las plantas (p. ej.: características funcionales, características de cobertura, tiempo de residencia, filogenia) y todos deben considerarse simultáneamente para poder identificar correlaciones significativas del éxito invasor. Recopilamos en Australia 146 parejas de especies de plantas invasoras y naturalizadas emparejadas filogenéticamente (congéneres) y con tiempos de residencia mínima similares (es decir, el tiempo transcurrido desde su introducción en años). Estas parejas se usaron para probar diferencias en cinco características funcionales (duración de la floración, tamaño de la hoja, altura máxima, área específica de la hoja [AEH], masa de la semilla) y en tres características de cobertura nativa de las especies (ocupación de bioma, temperatura media anual y amplitud de pluviosidad) entre especies invasoras y naturalizadas. Las especies invasoras, en promedio, tuvieron una mayor AEH, periodos de floración más largos y fueron más altas que sus parientes congéneres naturalizadas. Las invasoras también exhibieron una mayor tolerancia a diferentes condiciones ambientales en su cobertura nativa, donde ocuparon más biomas y una mayor amplitud de pluviosidad y condiciones de temperatura que sus congéneres naturalizadas. Sin embargo, ni la masa de la semilla ni el tamaño de hoja difirieron entre las parejas de especies naturalizadas e invasoras. Un hallazgo relevante fue el papel de la AEH en la distinción entre las parejas naturalizadas e invasoras. Las especies con valores altos de AEH estuvieron asociadas típicamente con tasas mayores de crecimiento, pérdida rápida de volumen de material de hojas y periodos de vida más cortos que aquellas especies con AEH baja. Este conjunto de características puede contribuir a la habilidad de las especies para llevar a cabo la transición de naturalizada a invasora a lo largo de una amplia cobertura de contextos ambientales y regímenes de perturbación. Nuestros hallazgos ayudarán en la mejora de los protocolos de ERH, y abogamos por la inclusión de las características cuantitativas, en particular la AEH, en los esquemas de ERH.
PMCID: PMC4405095  PMID: 25369762
functional traits; integrative invasion science; invasion continuum; invasive species; native range characteristics; naturalized plants; residence time; sleeper weeds; características de cobertura nativa; características funcionales; ciencia integrante de la invasión; continuo de invasión; especies invasoras; hierbas sigilosas; plantas naturalizadas; tiempo de residencia
24.  Relative growth rate variation of evergreen and deciduous savanna tree species is driven by different traits 
Annals of Botany  2014;114(2):315-324.
Background and Aims
Plant relative growth rate (RGR) depends on biomass allocation to leaves (leaf mass fraction, LMF), efficient construction of leaf surface area (specific leaf area, SLA) and biomass growth per unit leaf area (net assimilation rate, NAR). Functional groups of species may differ in any of these traits, potentially resulting in (1) differences in mean RGR of groups, and (2) differences in the traits driving RGR variation within each group. We tested these predictions by comparing deciduous and evergreen savanna trees.
RGR, changes to biomass allocation and leaf morphology, and root non-structural carbohydrate reserves were evaluated for juveniles of 51 savanna species (34 deciduous, 17 evergreen) grown in a common garden experiment. It was anticipated that drivers of RGR would differ between leaf habit groups because deciduous species have to allocate carbohydrates to storage in roots to be able to flush leaves again, which directly compromises their LMF, whereas evergreen species are not subject to this constraint.
Key Results
Evergreen species had greater LMF and RGR than deciduous species. Among deciduous species LMF explained 27 % of RGR variation (SLA 34 % and NAR 29 %), whereas among evergreen species LMF explained between 2 and 17 % of RGR variation (SLA 32–35 % and NAR 38–62 %). RGR and LMF were (negatively) related to carbohydrate storage only among deciduous species.
Trade-offs between investment in carbohydrate reserves and growth occurred only among deciduous species, leading to differences in relative contribution made by the underlying components of RGR between the leaf habit groups. The results suggest that differences in drivers of RGR occur among savanna species because these have different selected strategies for coping with fire disturbance in savannas. It is expected that variation in the drivers of RGR will be found in other functional types that respond differently to particular disturbances.
PMCID: PMC4111386  PMID: 24958787
Carbohydrate storage; deciduous; ecological traits; evergreen; functional types; plant growth variation; relative growth rate; RGR; savanna trees
25.  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.
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

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