Leaf nutrient basis for the differentiation of photosynthetic traits between subtropical evergreen and deciduous trees.

Compared to evergreens, deciduous tree species usually have higher photosynthetic efficiency to complete vegetative and reproductive growth in a shorter growing season. However, the nutrient basis for the differentiation of photosynthesis functional traits between evergreen and deciduous tree species has not yet been clarified. Thirty evergreen and twenty deciduous angiosperm tree species from a subtropical common garden were compared in terms of photosynthetic traits and leaf nutrients. Generally, their differences in area-based photosynthetic capacity were uncorrelated with area-based leaf nutrient content but were caused by the fraction of nitrogen allocated to photosynthetic components. By comparison, the differences in mass-based photosynthetic capacity were more correlated with leaf nitrogen content than leaf phosphorus and potassium content. Convergence in phosphorus and potassium constraints to photosynthesis occurred in deciduous tree species but not in evergreen tree species. Furthermore, leaf C/N ratio played a more significant role than leaf mass per area in determining the differentiation of photosynthetic traits between evergreen and deciduous groups. Our findings provide insight into the nutrient basis for photosynthetic carbon gain and functional strategies across trees species.

A new dimension of leaf economic spectrum: temporal instability of relationships among genotypes.

Leaf economic spectrum (LES) relationships have been studied across many different plant lineages and at different organizational scales. However, the temporal stability of the LES relationships is largely unknown. We used the wild blueberry system with high genotypic diversity to test whether trait-trait relationships across genotypes demonstrate the same LES relationships found in the global database (GLOPNET) and whether they are stable across years. We studied leaf structure, photosynthesis, and leaf nutrients for 16 genotypes of two wild blueberry species semi-naturally grown in a common farm in Maine, USA, across 4 yr. We found substantial variation in leaf structure, physiology, and nutrient traits within and among genotypes, as well as across years in wild blueberries. The LES trait-trait relationships (covariance structure) across genotypes were not always found in all years. The trait syndrome of wild blueberries was shifted by changing environmental conditions over the years. Additionally, traits in 1 yr cannot be used to predict those of another year. Our findings show that LES generally holds among genotypes but is temporally unstable, stressing the significant influence of trait plasticity in response to fluctuating environmental conditions across years, and the importance of temporal dimensions in shaping functional traits and species coexistence.

Optimising height-growth predicts trait responses to water availability and other environmental drivers.

Future changes in climate, together with rising atmospheric CO 2 ${\text{CO}}_{2}$ , may reorganise the functional composition of ecosystems. Without long-term historical data, predicting how traits will respond to environmental conditions-in particular, water availability-remains a challenge. While eco-evolutionary optimality theory (EEO) can provide insight into how plants adapt to their environment, EEO approaches to date have been formulated on the assumption that plants maximise carbon gain, which omits the important role of tissue construction and size in determining growth rates and fitness. Here, we show how an expanded optimisation framework, focussed on individual growth rate, enables us to explain shifts in four key traits: leaf mass per area, sapwood area to leaf area ratio (Huber value), wood density and sapwood-specific conductivity in response to soil moisture, atmospheric aridity, CO 2 ${\text{CO}}_{2}$ and light availability. In particular, we predict that as conditions become increasingly dry, height-growth optimising traits shift from resource-acquisitive strategies to resource-conservative strategies, consistent with empirical responses across current environmental gradients of rainfall. These findings can explain both the shift in traits and turnover of species along existing environmental gradients and changing future conditions and highlight the importance of both carbon assimilation and tissue construction in shaping the functional composition of vegetation across climates.

Genotype × environment × management analysis to define allometric rules between leaves and stems in wheat.

Allometric rules provide insights into structure-function relationships across species and scales and are commonly used in ecology. The fields of agronomy, plant phenotyping, and modeling also need simplifications such as those provided by allometric rules to reconcile data at different temporal and spatial levels (organs/canopy). This study explores the variations in relationships for wheat in terms of the distribution of crop green area between leaves and stems, and the allocation of above-ground biomass between leaves and stems during the vegetative period, using a large dataset covering different years, countries, genotypes, and management practices. The results showed that the relationship between leaf and stem area was linear, genotype-specific, and sensitive to radiation. The relationship between leaf and stem biomass depended on genotype and nitrogen fertilization. The mass per area, associating area and biomass for both leaf and stem, varied strongly by developmental stage and was significantly affected by environment and genotype. These allometric rules were evaluated and shown to have satisfactory performance, and their potential use is discussed with regard to current phenotyping techniques and plant/crop models. Our results enable the definition of models and minimum datasets required for characterizing diversity panels and making predictions in various genotype × environment × management contexts.

Heterotic growth of hybrids of Arabidopsis thaliana is enhanced by elevated atmospheric CO2.

PREMISE: With the global atmospheric CO2 concentration on the rise, developing crops that can thrive in elevated CO2 has become paramount. We investigated the potential of hybridization as a strategy for creating crops with improved growth in predicted elevated atmospheric CO2. METHODS: We grew parent accessions and their F1 hybrids of Arabidopsis thaliana in ambient and elevated atmospheric CO2 and analyzed numerous growth traits to assess their productivity and underlying mechanisms. RESULTS: The heterotic increase in total dry mass, relative growth rate and leaf net assimilation rate was significantly greater in elevated CO2 than in ambient CO2. The CO2 response of net assimilation rate was positively correlated with the CO2 response of leaf nitrogen productivity and with that of leaf traits such as leaf size and thickness, suggesting that hybridization-induced changes in leaf traits greatly affected the improved performance in elevated CO2. CONCLUSIONS: Vegetative growth of hybrids seems to be enhanced in elevated CO2 due to improved photosynthetic nitrogen-use efficiency compared with parents. The results suggest that hybrid crops should be well-suited for future conditions, but hybrid weeds may also be more competitive.

Leaf mass per area: An investigation into the application of the ubiquitous functional trait from a paleobotanical perspective.

PREMISE: Leaf mass per area (LMA) is a widely used functional trait in both neobotanical and paleobotanical research that provides a window into how plants interact with their environment. Paleobotanists have used site-level measures of LMA as a proxy for climate, biome, deciduousness, and community-scale plant strategy, yet many of these relationships have not been grounded in modern data. In this study, we evaluated LMA from the paleobotanical perspective, seeking to add modern context to paleobotanical interpretations and discover what a combined modern and fossil data set can tell us about how LMA can be best applied toward interpreting plant communities. METHODS: We built a modern data set by pulling plant trait data from the TRY database, and a fossil data set by compiling data from studies that have used the petiole-width proxy for LMA. We then investigated the relationships of species-mean, site-mean, and site-distribution LMA with different climatic, phylogenetic, and physiognomic variables. RESULTS: We found that LMA distributions are correlated with climate, site taxonomic composition, and deciduousness. However, the relative contributions of these factors are not distinctive, and ultimately, LMA distributions cannot accurately reconstruct the biome or climate of an individual site. CONCLUSIONS: The correlations that make up the leaf economics spectrum are stronger than the correlations between LMA and climate, phylogeny, morphospace, or depositional environment. Fossil LMA should be understood as the culmination of the influences of these variables rather than as a predictor.

The ratio of electron transport to assimilation (ETR/AN): underutilized but essential for assessing both equipment's proper performance and plant status.

MAIN CONCLUSION: ETR/AN ratios should be in the range 7.5-10.5 for non-stressed C3 plants. Ratios extremely out of this range can be reflecting both uncontrolled plant status and technical mistakes during measurements. We urge users to explicitly refer to this ratio in future studies as a proof for internal data quality control. For the last few decades, the use of infra-red gas-exchange analysers (IRGAs) coupled with chlorophyll fluorometers that allow for measurements of net CO2 assimilation rate and estimates of electron transport rate over the same leaf area has been popularized. The evaluation of data from both instruments in an integrative manner can result in additional valuable information, such as the estimation of the light respiration, mesophyll conductance and the partitioning of the flux of electrons into carboxylation, oxygenation and alternative processes, among others. In this review, an additional and more 'straight' use of the combination of chlorophyll fluorescence and gas exchange-derived parameters is presented, namely using the direct ratio between two fully independently estimated parameters, electron transport rate (ETR)-determined by the fluorometer-and net CO2 assimilation rate (AN)-determined by the IRGA, i.e., the ETR/AN ratio, as a tool for fast detection of incongruencies in the data and potential technical problems associated with them, while checking for the study plant's status. To illustrate this application, a compilation of 75 studies that reported both parameters for a total of 178 species under varying physiological status is presented. Values of ETR/AN between 7.5 and 10.5 were most frequently found for non-stressed C3 plants. C4 species showed an average ETR/AN ratio of 4.7. The observed ratios were larger for species with high leaf mass per area and for plants subjected to stressful factors like drought or nutritional deficit. Knowing the expected ETR/AN ratio projects this ratio as a routinary and rapid check point for guaranteeing both the correct performance of equipment and the optimal/stress status of studied plants. All known errors associated with the under- or overestimation of ETR or AN are summarized in a checklist that aims to be routinely used by any IRGA/fluorometer user to strength the validity of their data.

Why can't we predict traits from the environment?

Plant functional traits are powerful ecological tools, but the relationships between plant traits and climate (or environmental variables more broadly) are often remarkably weak. This presents a paradox: Plant traits govern plant interactions with their environment, but the environment does not strongly predict the traits of plants living there. Unpacking this paradox requires differentiating the mechanisms of trait variation and potential confounds of trait-environment relationships at different evolutionary and ecological scales ranging from within species to among communities. It also necessitates a more integrated understanding of physiological and evolutionary equifinality among many traits and plant strategies, and challenges us to understand how supposedly 'functional' traits integrate into a whole-organism phenotype in ways that may be largely orthogonal to environmental tolerances.

Cell wall thickness has phylogenetically consistent effects on the photosynthetic nitrogen-use efficiency of terrestrial plants.

Leaf photosynthetic nitrogen-use efficiency (PNUE) diversified significantly among C3 species. To date, the morpho-physiological mechanisms and interrelationships shaping PNUE on an evolutionary time scale remain unclear. In this study, we assembled a comprehensive matrix of leaf morpho-anatomical and physiological traits for 679 C3 species, ranging from bryophytes to angiosperms, to comprehend the complexity of interrelationships underpinning PNUE variations. We discovered that leaf mass per area (LMA), mesophyll cell wall thickness (Tcwm ), Rubisco N allocation fraction (PR ), and mesophyll conductance (gm ) together explained 83% of PNUE variations, with PR and gm accounting for 65% of those variations. However, the PR effects were species-dependent on gm , meaning the contribution of PR on PNUE was substantially significant in high-gm species compared to low-gm species. Standard major axis (SMA) and path analyses revealed a weak correlation between PNUE and LMA (r2 = 0.1), while the SMA correlation for PNUE-Tcwm was robust (r2 = 0.61). PR was inversely related to Tcwm , paralleling the relationship between gm and Tcwm , resulting in the internal CO2 drawdown being only weakly proportional to Tcwm . The coordination of PR and gm in relation to Tcwm constrains PNUE during the course of evolution.

Plasticity of mesophyll cell density and cell wall thickness and composition play a pivotal role in regulating plant growth and photosynthesis under shading in rapeseed.

BACKGROUND AND AIMS: Plasticity of leaf growth and photosynthesis is an important strategy of plants to adapt to shading stress; however, their strategy of leaf development to achieve a simultaneous increase in leaf area and photosynthesis under shading remains unknown. METHODS: In the present study, a pot experiment was conducted using three rapeseed genotypes of Huayouza 50 (HYZ50), Zhongshuang 11 (ZS11) and Huayouza 62 (HYZ62), and the responses of plant growth, leaf morphoanatomical traits, cell wall composition and photosynthesis to shading were investigated. KEY RESULTS: Shading significantly increased leaf area per plant (LAplant) in all genotypes, but the increase in HYZ62 was greater than that in HYZ50 and ZS11. The greater increment of LAplant in HYZ62 was related to the larger decrease in leaf mass per area (LMA) and leaf density (LD), which were in turn related to less densely packed mesophyll cells and thinner cell walls (Tcw). Moreover, shading significantly increased photosynthesis in HYZ62 but significantly decreased it in HYZ50. The enhanced photosynthesis in HYZ62 was related to increased mesophyll conductance (gm) due primarily to thinner cell walls. CONCLUSIONS: The data presented indicate that the different plasticity of mesophyll cell density, cell wall thickness and cell wall composition in response to shading can dramatically affect leaf growth and photosynthesis.

Disentangling leaf structural and material properties in relationship to their anatomical and chemical compositional traits in oaks (Quercus L.).

BACKGROUND AND AIMS: The existence of sclerophyllous plants has been considered an adaptive strategy against different environmental stresses. Given that it literally means 'hard-leaved', it is essential to quantify the leaf mechanical properties to understand sclerophylly. However, the relative importance of each leaf trait for mechanical properties is not yet well established. METHODS: Genus Quercus is an excellent system to shed light on this because it minimizes phylogenetic variation while having a wide variation in sclerophylly. We measured leaf anatomical traits and cell wall composition, analysing their relationship with leaf mass per area and leaf mechanical properties in a set of 25 oak species. KEY RESULTS: The upper epidermis outer wall makes a strong and direct contribution to the leaf mechanical strength. Moreover, cellulose plays a crucial role in increasing leaf strength and toughness. The principal component analysis plot based on leaf trait values clearly separates Quercus species into two groups corresponding to evergreen and deciduous species. CONCLUSIONS: Sclerophyllous Quercus species are tougher and stronger owing to their thicker epidermis outer wall and/or higher cellulose concentration. Furthermore, section Ilex species share common traits, although they occupy different climates. In addition, evergreen species living in mediterranean-type climates share common leaf traits irrespective of their different phylogenetic origin.

The structural correlations and the physiological functions of stomatal morphology and leaf structures in C3 annual crops.

MAIN CONCLUSION: This study suggests that stomatal and leaf structures are highly correlated, and mesophyll cell size is an important anatomical trait determining the coordination between stomatal size and mesophyll porosity. A comprehensive study of the correlations between the structural traits and on their relationships with gas exchange parameters may provide some useful information into leaf development and improvement in efficiencies of photosynthetic CO2 fixation and transpirational water loss. In the present study, nine plant materials from eight crop species were pot grown in a growth chamber. Leaf structural traits, gas exchange, and leaf nitrogen content were measured. We found that stomatal size, mesophyll cell size (MCS), and mesophyll porosity were positively correlated and that the surface areas of mesophyll cells and chloroplasts facing intercellular air spaces were positively correlated with both stomatal density and stomatal area per leaf area (SA). These results suggested that the developments of stomata and mesophyll cells are highly correlated among different crop species. Additionally, MCS was positively correlated with leaf thickness and negatively correlated with leaf density and leaf mass per area, which indicated that MCS might play an important role in leaf structural investments and physiological functions among species. In summary, this study illustrates the correlations between stomatal and mesophyll structures, and it highlights the importance of considering the covariations among leaf traits with the intent of improving photosynthesis and iWUE.

The plastid-nucleus localized DNA-binding protein WHIRLY1 is required for acclimation of barley leaves to high light.

MAIN CONCLUSION: In accordance with a key role of WHIRLY1 in light-acclimation mechanisms, typical features of acclimation to high light, including photosynthesis and leaf morphology, are compromised in WHIRLY1 deficient plants. Acclimation to the environment requires efficient communication between chloroplasts and the nucleus. Previous studies indicated that the plastid-nucleus located WHIRLY1 protein is required for the communication between plastids and the nucleus in situations of high light exposure. To investigate the consequences of WHIRLY1 deficiency on the light acclimation of photosynthesis and leaf anatomy, transgenic barley plants with an RNAi-mediated knockdown of HvWHIRLY1 were compared to wild-type plants when growing at low and high irradiance. While wild-type plants showed the typical light acclimation responses, i.e. higher photosynthetic capacity and thicker leaves, the WHIRLY1 deficient plants were not able to respond to differences in irradiance. The results revealed a systemic role of WHIRLY1 in light acclimation by coordinating responses at the level of the chloroplast and the level of leaf morphology.

The leaf economics spectrum of triploid and tetraploid C4 grass Miscanthus x giganteus.

The leaf economics spectrum (LES) describes multivariate correlations in leaf structural, physiological and chemical traits, originally based on diverse C3 species grown under natural ecosystems. However, the specific contribution of C4 species to the global LES is studied less widely. C4 species have a CO2 concentrating mechanism which drives high rates of photosynthesis and improves resource use efficiency, thus potentially pushing them towards the edge of the LES. Here, we measured foliage morphology, structure, photosynthesis, and nutrient content for hundreds of genotypes of the C4 grass Miscanthus× giganteus grown in two common gardens over two seasons. We show substantial trait variations across M.× giganteus genotypes and robust genotypic trait relationships. Compared to the global LES, M.× giganteus genotypes had higher photosynthetic rates, lower stomatal conductance, and less nitrogen content, indicating greater water and photosynthetic nitrogen use efficiency in the C4 species. Additionally, tetraploid genotypes produced thicker leaves with greater leaf mass per area and lower leaf density than triploid genotypes. By expanding the LES relationships across C3 species to include C4 crops, these findings highlight that M.× giganteus occupies the boundary of the global LES and suggest the potential for ploidy to alter LES traits.

Testing unified theories for ozone response in C4 species.

There is tremendous interspecific variability in O3  sensitivity among C3  species, but variation among C4  species has been less clearly documented. It is also unclear whether stomatal conductance and leaf structure such as leaf mass per area (LMA) determine the variation in sensitivity to O3 across species. In this study, we investigated leaf morphological, chemical, and photosynthetic responses of 22 genotypes of four C4 bioenergy species (switchgrass, sorghum, maize, and miscanthus) to elevated O3 in side-by-side field experiments using free-air O3 concentration enrichment (FACE). The C4  species varied largely in leaf morphology, physiology, and nutrient composition. Elevated O3 did not alter leaf morphology, nutrient content, stomatal conductance, chlorophyll fluorescence, and respiration in most genotypes but reduced net CO2 assimilation in maize and photosynthetic capacity in sorghum and maize. Species with lower LMA and higher stomatal conductance tended to show greater losses in photosynthetic rate and capacity in elevated O3 compared with species with higher LMA and lower stomatal conductance. Stomatal conductance was the strongest determinant of leaf photosynthetic rate and capacity. The response of both area- and mass-based leaf photosynthetic rate and capacity to elevated O3 were not affected by LMA directly but negatively influenced by LMA indirectly through stomatal conductance. These results demonstrate that there is significant variation in O3  sensitivity among C4  species with maize and sorghum showing greater sensitivity of photosynthesis to O3 than switchgrass and miscanthus. Interspecific variation in O3  sensitivity was determined by direct effects of stomatal conductance and indirect effects of LMA. This is the first study to provide a test of unifying theories explaining variation in O3  sensitivity in C4 bioenergy grasses. These findings advance understanding of O3 tolerance in C4  grasses and could aid in optimal placement of diverse C4 bioenergy feedstock across a polluted landscape.

Cost-benefit analysis of mesophyll conductance: diversities of anatomical, biochemical and environmental determinants.

BACKGROUND: Plants invest photosynthates in construction and maintenance of their structures and functions. Such investments are considered costs. These costs are recovered by the CO2 assimilation rate (A) in the leaves, and thus A is regarded as the immediate, short-term benefit. In photosynthesizing leaves, CO2 diffusion from the air to the carboxylation site is hindered by several structural and biochemical barriers. CO2 diffusion from the intercellular air space to the chloroplast stroma is obstructed by the mesophyll resistance. The inverses is the mesophyll conductance (gm). Whether various plants realize an optimal gm, and how much investment is needed for a relevant gm, remain unsolved. SCOPE: This review examines relationships among leaf construction costs (CC), leaf maintenance costs (MC) and gm in various plants under diverse growth conditions. Through a literature survey, we demonstrate a strong linear relationship between leaf mass per area (LMA) and leaf CC. The overall correlation of CC vs. gm across plant phylogenetic groups is weak, but significant trends are evident within specific groups and/or environments. Investment in CC is necessary for an increase in LMA and mesophyll cell surface area (Smes). This allows the leaf to accommodate more chloroplasts, thus increasing A. However, increases in LMA and/or Smes often accompany other changes, such as cell wall thickening, which diminishes gm. Such factors that make the correlations of CC and gm elusive are identified. CONCLUSIONS: For evaluation of the contribution of gm to recover CC, leaf life span is the key factor. The estimation of MC in relation to gm, especially in terms of costs required to regulate aquaporins, could be essential for efficient control of gm over the short term. Over the long term, costs are mainly reflected in CC, while benefits also include ultimate fitness attributes in terms of integrated carbon gain over the life of a leaf, plant survival and reproductive output.

Leaf trait covariation and controls on leaf mass per area (LMA) following cotton domestication.

BACKGROUND AND AIMS: The process of domestication has driven dramatic shifts in plant functional traits, including leaf mass per area (LMA). It remains unclear whether domestication has produced concerted shifts in the lower-level anatomical traits that underpin LMA and how these traits in turn affect photosynthesis. METHODS: In this study we investigated controls of LMA and leaf gas exchange by leaf anatomical properties at the cellular, tissue and whole-leaf levels, comparing 26 wild and 31 domesticated genotypes of cotton (Gossypium). KEY RESULTS: As expected, domesticated plants expressed lower LMA, higher photosynthesis and higher stomatal conductance, suggesting a shift towards the 'faster' end of the leaf economics spectrum. At whole-leaf level, variation in LMA was predominantly determined by leaf density (LD) both in wild and domesticated genotypes. At tissue level, higher leaf volume per area (Vleaf) in domesticated genotypes was driven by a simultaneous increase in the volume of epidermal, mesophyll and vascular bundle tissue and airspace, while lower LD resulted from a lower volume of palisade tissue and vascular bundles (which are of high density), paired with a greater volume of epidermis and airspace, which are of low density. The volume of spongy mesophyll exerted direct control on photosynthesis in domesticated genotypes but only indirect control in wild genotypes. At cellular level, a shift to larger but less numerous cells with thinner cell walls underpinned a lower proportion of cell wall mass, and thus a reduction in LD. CONCLUSIONS: Taken together, cotton domestication has triggered synergistic shifts in the underlying determinants of LMA but also photosynthesis, at cell, tissue and whole-leaf levels, resulting in a marked shift in plant ecological strategy.

Deciduous and evergreen oaks show contrasting adaptive responses in leaf mass per area across environments.

Increases in leaf mass per area (LMA) are commonly observed in response to environmental stresses and are achieved through increases in leaf thickness and/or leaf density. Here, we investigated how the two underlying components of LMA differ in relation to species native climates and phylogeny, across deciduous and evergreen species. Using a phylogenetic approach, we quantified anatomical, compositional and climatic variables from 40 deciduous and 45 evergreen Quercus species from across the Northern Hemisphere growing in a common garden. Deciduous species from shorter growing seasons tended to have leaves with lower LMA and leaf thickness than those from longer growing seasons, while the opposite pattern was found for evergreens. For both habits, LMA and thickness increased in arid environments. However, this shift was associated with increased leaf density in evergreens but reduced density in deciduous species. Deciduous and evergreen oaks showed fundamental leaf morphological differences that revealed a diverse adaptive response. While LMA in deciduous species may have diversified in tight coordination with thickness mainly modulated by aridity, diversification of LMA within evergreens appears to be dependent on the infrageneric group, with diversification in leaf thickness modulated by both aridity and cold, while diversification in leaf density is only modulated by aridity.

Prediction of photosynthetic light-response curves using traits of the leaf economics spectrum for 75 woody species: effects of leaf habit and sun-shade dichotomy.

PREMISE: Photosynthetic light-response (PLR) curves for leaves are important components of models related to carbon fixation in forest ecosystems, linking the Mitscherlich equation and Michaelis-Menten equation to traits of the leaf economics spectrum (LES). However, models do not consider changes in leaf habits (i.e., evergreen and deciduous) and within-canopy shading variation in these PLR curves. METHODS: Here, we measured the PLR curves in sun and shade leaves of 44 evergreen and 31 deciduous species to examine the relationships between variables of the Mitscherlich equation and Michaelis-Menten equation, leaf nitrogen (N) and phosphorus (P) content, and leaf mass per area (LMA). RESULTS: Small changes were caused by different leaf habits and shade variations in relationships linking variables of the two equations to leaf N and P content and LMA. Values of the scaling exponents for PLR curve parameters did not differ regardless of canopy position and leaf habit (P > 0.05). The PLR curves in species with different leaf habits (i.e., evergreen and deciduous) at different canopy positions could be predicted using the general allometric relations between leaf traits and PLR parameters in the two equations. For photosynthetic photon flux densities from 0 to 2000 µmol m-2 s-1 , approximately 71% (Mitscherlich equation) and 70% (Michaelis-Menten equation) of the net assimilation rates could be predicted. CONCLUSIONS: These findings indicate that leaf net assimilation rates can be predicted through the large available data for LES traits. Incorporation of values for these traits available in the LES databases into ecosystem models of forest productivity and carbon fixation warrants further investigation.

Linkage between species traits and plant phenology in an alpine meadow.

Plant phenology differs largely among coexisting species within communities that share similar habitat conditions. However, the factors explaining such phenological diversity of plants have not been fully investigated. We hypothesize that species traits, including leaf mass per area (LMA), seed mass, stem tissue mass density (STD), maximum plant height (Hmax), and relative growth rate in height (RGRH), explain variation in plant phenology, and tested this hypothesis in an alpine meadow. Results showed that both LMA and STD were positively correlated with the onset (i.e., beginning) and offset (i.e., ending) times of the four life history events including two reproductive events (flowering and fruiting) and two vegetative events (leafing and senescing). In contrast, RGRH was negatively correlated with the four life phenological events. Moreover, Hmax was positively correlated with reproductive events but not with vegetative events. However, none of the eight phenological events was associated with seed size. In addition, the combination of LMA and STD accounted for 50% of the variation in plant phenologies. Phylogenetic generalized least squares analysis showed plant phylogeny weakened the relationships between species traits vs. phenologies. Phylogeny significantly regulated the variation in the ending but not the beginning of phenologies. Our results indicate that species traits are robust indicators for plant phenologies and can be used to explain the diversity of plant phenologies among co-occurring herbaceous species in grasslands. The findings highlight the important role of the combination of and trade-offs between functional traits in determing plant phenology diversity in the alpine meadow.