Plant economics spectrum governs leaf nitrogen and phosphorus resorption in subtropical transitional forests.

BACKGROUND: Leaf nitrogen (N) and phosphorus (P) resorption is a fundamental adaptation strategy for plant nutrient conservation. However, the relative roles that environmental factors and plant functional traits play in regulating N and P resorption remain largely unclear, and little is known about the underlying mechanism of plant functional traits affecting nutrient resorption. Here, we measured leaf N and P resorption and 13 plant functional traits of leaf, petiole, and twig for 101 representative broad-leaved tree species in our target subtropical transitional forests. We integrated these multiple functional traits into the plant economics spectrum (PES). We further explored whether and how elevation-related environmental factors and these functional traits collectively control leaf N and P resorption. RESULTS: We found that deciduous and evergreen trees exhibited highly diversified PES strategies, tending to be acquisitive and conservative, respectively. The effects of PES, rather than of environmental factors, dominated leaf N and P resorption patterns along the elevational gradient. Specifically, the photosynthesis and nutrient recourse utilization axis positively affected N and P resorption for both deciduous and evergreen trees, whereas the structural and functional investment axis positively affected leaf N and P resorption for evergreen species only. Specific leaf area and green leaf nutrient concentrations were the most influential traits driving leaf N and P resorption. CONCLUSIONS: Our study simultaneously elucidated the relative contributions of environmental factors and plant functional traits to leaf N and P resorption by including more representative tree species than previous studies, expanding our understanding beyond the relatively well-studied tropical and temperate forests. We highlight that prioritizing the fundamental role of traits related to leaf resource capture and defense contributes to the monitoring and modeling of leaf nutrient resorption. Therefore, we need to integrate PES effects on leaf nutrient resorption into the current nutrient cycling model framework to better advance our general understanding of the consequences of shifting tree species composition for nutrient cycles across diverse forests.

Multiple time scale optimization explains functional trait responses to leaf water potential.

Plant response to water stress involves multiple timescales. In the short term, stomatal adjustments optimize some fitness function commonly related to carbon uptake, while in the long term, traits including xylem resilience are adjusted. These optimizations are usually considered independently, the former involving stomatal aperture and the latter carbon allocation. However, short- and long-term adjustments are interdependent, as 'optimal' in the short term depends on traits set in the longer term. An economics framework is used to optimize long-term traits that impact short-term stomatal behavior. Two traits analyzed here are the resilience of xylem and the resilience of nonstomatal limitations (NSLs) to photosynthesis at low-water potentials. Results show that optimality requires xylem resilience to increase with climatic aridity. Results also suggest that the point at which xylem reach 50% conductance and the point at which NSLs reach 50% capacity are constrained to approximately a 2 : 1 linear ratio; however, this awaits further experimental verification. The model demonstrates how trait coordination arises mathematically, and it can be extended to many other traits that cross timescales. With further verification, these results could be used in plant modelling when information on plant traits is limited.

Accounting for trait variability and coordination in predictions of drought-induced range shifts in woody plants.

Functional traits offer a promising avenue to improve predictions of species range shifts under climate change, which will entail warmer and often drier conditions. Although the conceptual foundation linking traits with plant performance and range shifts appears solid, the predictive ability of individual traits remains generally low. In this review, we address this apparent paradox, emphasizing examples of woody plants and traits associated with drought responses at the species' rear edge. Low predictive ability reflects the fact not only that range dynamics tend to be complex and multifactorial, as well as uncertainty in the identification of relevant traits and limited data availability, but also that trait effects are scale- and context-dependent. The latter results from the complex interactions among traits (e.g. compensatory effects) and between them and the environment (e.g. exposure), which ultimately determine persistence and colonization capacity. To confront this complexity, a more balanced coverage of the main functional dimensions involved (stress tolerance, resource use, regeneration and dispersal) is needed, and modelling approaches must be developed that explicitly account for: trait coordination in a hierarchical context; trait variability in space and time and its relationship with exposure; and the effect of biotic interactions in an ecological community context.

Dark respiration explains nocturnal stomatal conductance in rice regardless of drought and nutrient stress.

The ecological mechanism underlying nocturnal stomatal conductance (gsn ) in C3 and C4 plants remains elusive. In this study, we proposed a 'coordinated leaf trait' hypothesis to explain gsn in rice plants. We conducted an open-field experiment by applying drought, nutrient stress and the combined drought-nutrient stress. We found that gsn was neither strongly reduced by drought nor consistently increased by nutrient stress. With the aforementioned multiple abiotic stressors considered as random effects, gsn exhibited a strong positive correlation with dark respiration (Rn ). Notably, gsn primed early morning (5:00-7:00) photosynthesis through faster stomatal response time. This photosynthesis priming effect diminished after mid-morning (9:00). Leaves were cooled by gsn -derived transpiration. However, our results clearly suggest that evaporative cooling did not reduce dark respiration cost. Our results indicate that gsn is more closely related to carbon respiration and assimilation than water and nutrient availability, and that dark respiration can explain considerable variation of gsn .

Coordination of photosynthetic traits across soil and climate gradients.

"Least-cost theory" posits that C3 plants should balance rates of photosynthetic water loss and carboxylation in relation to the relative acquisition and maintenance costs of resources required for these activities. Here we investigated the dependency of photosynthetic traits on climate and soil properties using a new Australia-wide trait dataset spanning 528 species from 67 sites. We tested the hypotheses that plants on relatively cold or dry sites, or on relatively more fertile sites, would typically operate at greater CO2 drawdown (lower ratio of leaf internal to ambient CO2 , Ci :Ca ) during light-saturated photosynthesis, and at higher leaf N per area (Narea ) and higher carboxylation capacity (Vcmax 25 ) for a given rate of stomatal conductance to water vapour, gsw . These results would be indicative of plants having relatively higher water costs than nutrient costs. In general, our hypotheses were supported. Soil total phosphorus (P) concentration and (more weakly) soil pH exerted positive effects on the Narea -gsw and Vcmax 25 -gsw slopes, and negative effects on Ci :Ca . The P effect strengthened when the effect of climate was removed via partial regression. We observed similar trends with increasing soil cation exchange capacity and clay content, which affect soil nutrient availability, and found that soil properties explained similar amounts of variation in the focal traits as climate did. Although climate typically explained more trait variation than soil did, together they explained up to 52% of variation in the slope relationships and soil properties explained up to 30% of the variation in individual traits. Soils influenced photosynthetic traits as well as their coordination. In particular, the influence of soil P likely reflects the Australia's geologically ancient low-relief landscapes with highly leached soils. Least-cost theory provides a valuable framework for understanding trade-offs between resource costs and use in plants, including limiting soil nutrients.

Changes in trait covariance along an orographic moisture gradient reveal the relative importance of light- and moisture-driven trade-offs in subtropical rainforest communities.

A range of functional trait-based approaches have been developed to investigate community assembly processes, but most ignore how traits covary within communities. We combined existing approaches - community-weighted means (CWMs) and functional dispersion (FDis) - with a metric of trait covariance to examine assembly processes in five angiosperm assemblages along a moisture gradient in Australia's subtropics. In addition to testing hypotheses about habitat filtering along the gradient, we hypothesized that trait covariance would be strongest at both ends of the moisture gradient and weakest in the middle, reflecting trade-offs associated with light capture in productive sites and moisture stress in dry sites. CWMs revealed evidence of climatic filtering, but FDis patterns were less clear. As hypothesized, trait covariance was weakest in the middle of the gradient but unexpectedly peaked at the second driest site due to the emergence of a clear drought tolerance-drought avoidance spectrum. At the driest site, the same spectrum was truncated at the 'avoider' end, revealing important information about habitat filtering in this system. Our focus on trait covariance revealed the nature and strength of trade-offs imposed by light and moisture availability, complementing insights gained about community assembly from existing trait-based approaches.

Multi-trait genetic variation in resource-use strategies and phenotypic plasticity correlates with local climate across the range of a Mediterranean oak (Quercus faginea).

Resource-use strategies are hypothesized to evolve along climatic gradients. However, our understanding of the environmental factors driving divergent evolution of resource-use strategies and the relationship between trait genetic variation and phenotypic plasticity is far from complete. Using the Mediterranean tree Quercus faginea as study system, we tested the hypothesis that a conservative resource-use strategy with increased drought tolerance and reduced phenotypic plasticity has evolved in areas with longer and more severe dry seasons. We conducted a glasshouse experiment in which we measured leaf morphological, physiological, growth and allocation traits in seedlings from 10 range-wide climatically contrasting populations, grown under two different watering treatments. Both univariate and multivariate analyses revealed a genetic gradient of resource-use strategies and phenotypic plasticity associated with provenance climate. In particular, populations from harsher (drier and colder) environments had more sclerophyllous leaves, lower growth rates, better physiological performance under dry conditions and reduced multi-trait phenotypic plasticity compared to populations from more mesic and milder environments. Our results suggest that contrasting precipitation and temperature regimes play an important role in the adaptive intraspecific evolution of multivariate phenotypes and their plasticity, resulting in coordinated morphology, physiology, growth and allometry according to alternative resource-use strategies.

Root exudation as a major competitive fine-root functional trait of 18 coexisting species in a subtropical forest.

Root exudation stimulates microbial decomposition and enhances nutrient availability to plants. It remains difficult to measure and predict this carbon flux in natural conditions, especially for mature woody plants. Based on a known conceptual framework of root functional traits coordination, we proposed that root functional traits may predict root exudation. We measured root exudation and other seven root morphological/chemical/physiological traits for 18 coexisting woody species in a deciduous-evergreen mixed forest in subtropical China. Root exudation, respiration, diameter and nitrogen (N) concentration all exhibited significant phylogenetic signals. We found that root exudation positively correlated with competitive traits (root respiration, N concentration) and negatively with a conservative trait (root tissue density). Furthermore, these relationships were independent of phylogenetic signals. A principal component analysis showed that root exudation and morphological traits loaded on two perpendicular axes. Root exudation is a competitive trait in a multidimensional fine-root functional coordination. The metabolic dimension on which root exudation loaded was relatively independent of the morphological dimension, indicating that increasing nutrient availability by root exudation might be a complementary strategy for plant nutrient acquisition. The positive relationship between root exudation and root respiration and N concentration is a promising approach for the future prediction of root exudation.

Climate and functional traits jointly mediate tree water-use strategies.

Tree water use is central to plant function and ecosystem fluxes. However, it is still unknown how organ-level water-relations traits are coordinated to determine whole-tree water-use strategies in response to drought, and whether this coordination depends on climate. Here we used a global sap flow database (SAPFLUXNET) to study the response of water use, in terms of whole-tree canopy conductance (G), to vapour pressure deficit (VPD) and to soil water content (SWC) for 142 tree species. We investigated the individual and coordinated effect of six water-relations traits (vulnerability to embolism, Huber value, hydraulic conductivity, turgor-loss point, rooting depth and leaf size) on water-use parameters, also accounting for the effect of tree height and climate (mean annual precipitation, MAP). Reference G and its sensitivity to VPD were tightly coordinated with water-relations traits rather than with MAP. Species with efficient xylem transport had higher canopy conductance but also higher sensitivity to VPD. Moreover, we found that angiosperms had higher reference G and higher sensitivity to VPD than did gymnosperms. Our results highlight the need to consider trait integration and reveal the complications and challenges of defining a single, whole-plant resource use spectrum ranging from 'acquisitive' to 'conservative'.

Water uptake depth is coordinated with leaf water potential, water-use efficiency and drought vulnerability in karst vegetation.

Root access to bedrock water storage or groundwater is an important trait allowing plant survival in seasonally dry environments. However, the degree of coordination between water uptake depth, leaf-level water-use efficiency (WUEi) and water potential in drought-prone plant communities is not well understood. We conducted a 135-d rainfall exclusion experiment in a subtropical karst ecosystem with thin skeletal soils to evaluate the responses of 11 co-occurring woody species of contrasting life forms and leaf habits to a severe drought during the wet growing season. Marked differences in xylem water isotopic composition during drought revealed distinct ecohydrological niche separation among species. The contrasting behaviour of leaf water potential in coexisting species during drought was largely explained by differences in root access to deeper, temporally stable water sources. Smaller-diameter species with shallower water uptake, more negative water potentials and lower WUEi showed extensive drought-induced canopy defoliation and/or mortality. By contrast, larger-diameter species with deeper water uptake, higher leaf-level WUEi and more isohydric behaviour survived drought with only moderate canopy defoliation. Severe water limitation imposes strong environmental filtering and/or selective pressures resulting in tight coordination between tree diameter, water uptake depth, iso/anisohydric behaviour, WUEi and drought vulnerability in karst plant communities.

Co-ordination between xylem anatomy, plant architecture and leaf functional traits in response to abiotic and biotic drivers in a nurse cushion plant.

BACKGROUND AND AIMS: Plants in dry Mediterranean mountains experience a double climatic stress: at low elevations, high temperatures coincide with water shortage during summer, while at high elevations temperature decreases and water availability increases. Cushion plants often act as nurses by improving the microclimate underneath their canopies, hosting beneficiary species that may reciprocally modify their benefactors' microenvironment. We assess how the nurse cushion plant Arenaria tetraquetra subsp. amabilis adjusts its hydraulic system to face these complex abiotic and biotic constraints. METHODS: We evaluated intra-specific variation and co-ordination of stem xylem anatomy, leaf functional traits and plant architecture in response to elevation, aspect and the presence of beneficiary species in four A. tetraquetra subsp. amabilis populations in the Sierra Nevada mountains, southern Spain. KEY RESULTS: Xylem anatomical and plant architectural traits were the most responsive to environmental conditions, showing the highest mutual co-ordination. Cushions were more compact and had smaller, more isolated conductive vessels in the southern than in the northern aspect, which allow minimization of the negative impacts of more intense drought. Only vessel size, leaf mass per area and terminal branch length varied with elevation. Nurse cushions co-ordinated plant architecture and xylem traits, having higher canopy compactness, fewer leaves per branch and fewer, more isolated vessels than non-nurse cushions, which reflects the negative effects of beneficiary plants on nurse water status. In non-nurse cushions, plant architecture co-ordinated with leaf traits instead. The interacting effects of aspect and elevation on xylem traits showed that stress due to frost at high elevation constrained xylem anatomy in the north, whereas stress due to drought had a parallel effect in the south. CONCLUSIONS: Trait co-ordination was weaker under more demanding environmental conditions, which agrees with the hypothesis that trait independence allows plants to better optimize different functions, probably entailing higher adjustment potential against future environmental changes.

Contrasting dynamics and trait controls in first-order root compared with leaf litter decomposition.

Decomposition is a key component of the global carbon (C) cycle, yet current ecosystem C models do not adequately represent the contributions of plant roots and their mycorrhizae to this process. The understanding of decomposition dynamics and their control by traits is particularly limited for the most distal first-order roots. Here we followed decomposition of first-order roots and leaf litter from 35 woody plant species differing in mycorrhizal type over 6 years in a Chinese temperate forest. First-order roots decomposed more slowly (k = 0.11 ± 0.01 years-1) than did leaf litter (0.35 ± 0.02 years-1), losing only 35% of initial mass on average after 6 years of exposure in the field. In contrast to leaf litter, nonlignin root C chemistry (nonstructural carbohydrates, polyphenols) accounted for 82% of the large interspecific variation in first-order root decomposition. Leaf litter from ectomycorrhizal (EM) species decomposed more slowly than that from arbuscular mycorrhizal (AM) species, whereas first-order roots of EM species switched, after 2 years, from having slower to faster decomposition compared with those from AM species. The fundamentally different dynamics and control mechanisms of first-order root decomposition compared with those of leaf litter challenge current ecosystem C models, the recently suggested dichotomy between EM and AM plants, and the idea that common traits can predict decomposition across roots and leaves. Aspects of C chemistry unrelated to lignin or nitrogen, and not presently considered in decomposition models, controlled first-order root decomposition; thus, current paradigms of ecosystem C dynamics and model parameterization require revision.

Plant profit maximization improves predictions of European forest responses to drought.

Knowledge of how water stress impacts the carbon and water cycles is a key uncertainty in terrestrial biosphere models. We tested a new profit maximization model, where photosynthetic uptake of CO2 is optimally traded against plant hydraulic function, as an alternative to the empirical functions commonly used in models to regulate gas exchange during periods of water stress. We conducted a multi-site evaluation of this model at the ecosystem scale, before and during major droughts in Europe. Additionally, we asked whether the maximum hydraulic conductance in the soil-plant continuum kmax (a key model parameter which is not commonly measured) could be predicted from long-term site climate. Compared with a control model with an empirical soil moisture function, the profit maximization model improved the simulation of evapotranspiration during the growing season, reducing the normalized mean square error by c. 63%, across mesic and xeric sites. We also showed that kmax could be estimated from long-term climate, with improvements in the simulation of evapotranspiration at eight out of the 10 forest sites during drought. Although the generalization of this approach is contingent upon determining kmax , it presents a mechanistic trait-based alternative to regulate canopy gas exchange in global models.

Differences in growth-economics of fast vs. slow growing grass species in response to temperature and nitrogen limitation individually, and in combination.

BACKGROUND: Fast growing invasive alien species are highly efficient with little investment in their tissues. They often outcompete slower growing species with severe consequences for diversity and community composition. The plant economics trait-based approach provides a theoretical framework, allowing the classification of plants with different performance characteristics. However, in multifaceted background, this approach needs testing. The evaluation and prediction of plant performance outcomes in ecologically relevant settings is among the most pressing topics to understand and predict ecosystem functioning, especially in a quickly changing environment. Temperature and nutrient availability are major components of the global environmental change and this study examines the response of growth economic traits, photosynthesis and respiration to such changes for an invasive fast-growing (Bromus hordaceus) and a slow-growing perennial (Bromus erectus) grass species. RESULTS: The fully controlled growth chamber experiment simulated temperature-and changes in nitrogen availability individually and in combination. We therefore provide maximum control and monitoring of growth responses allowing general growth trait response patterns to be tested. Under optimal nitrogen availability the slow growing B. erectus was better able to handle the lower temperatures (7 °C) whilst both species had problems at higher temperatures (30 °C). Stresses produced by a combination of heat and nutrient availability were identified to be less limiting for the slow growing species but the combination of chilling with low nutrient availability was most detrimental to both species. CONCLUSIONS: For the fast-growing invader B. hordeaceus a reduction of nitrogen availability in combination with a temperature increase, leads to limited growth performance in comparison to the slow-growing perennial species B.erectus and this may explain why nutrient-rich habitats often experience more invasion than resource-poor habitats.

Vestured pits and scalariform perforation plate morphology modify the relationships between angiosperm vessel diameter, climate and maximum plant height.

Shared ancestry among species and correlation between vessel diameter and plant height can obscure the mechanisms linking vessel diameter to current climate distributions of angiosperms. Because wood is complex, various traits may interact to influence vessel function. Specifically, pit vesturing (lignified cell wall protuberances associated with bordered pits) and perforation plate morphology could alter the relationships between vessel diameter, climate and plant height. Using phylogenetically informed analyses, we tested for associations between vessel diameter, climate and maximum plant height across angiosperm species with different pit vesturing (presence/absence) and perforation plate morphology (simple/scalariform and quantitative variation). We show significantly larger changes in vessel diameter and maximum plant height across climates for species with vestures and simple perforation plates, compared to nonvestured species and those with scalariform plates. We also found a significantly greater increase in height for a given increase in vessel diameter with lower percentage of scalariform plates. Our study provides novel insights into the evolution of angiosperm xylem by showing that vessel pit vesturing and perforation plate morphologies can modify relationships among xylem vessels, climate and height. Our findings highlight the complexity of xylem adaptations to climate, substantiating an integrative view of xylem function in the study of wood evolution.

Decoupled leaf and root carbon economics is a key component in the ecological diversity and evolutionary divergence of deciduous and evergreen lineages of genus Rhododendron.

PREMISE: We explored trait-trait and trait-climate relationships for 27 Rhododendron species while accounting for phylogenetic relationships and within-species variation to investigate whether leaf and root traits are coordinated across environments and over evolutionary time, as part of a whole-plant economics spectrum. METHODS: We examined specific leaf area (SLA) and four root traits: specific root length (SRL), specific root tip abundance (SRTA), first order diameter, and link average length, for plants growing in a cold, seasonal climate (Kirtland, Ohio) and a warmer, less seasonal climate (Federal Way, Washington) in the United States. We estimated a phylogeny and species' climate of origin, determined phylogenetic signal on mean traits and within-species variation, and used phylogenetically informed analysis to compare trait-trait and trait-climate relationships for deciduous and evergreen lineages. RESULTS: Mean SLA and within-species variation in SRL were more similar between close relatives than expected by chance. SLA and root traits differed according to climate of origin and across growth environments, though SLA differed within- and among-species less than roots. A negative SRL-SRTA correlation indicates investment in foraging scale vs. precision as a fundamental trade-off defining the root economic spectrum. Also, the deciduous clade exhibited a strong negative relationship between SLA and SRL, while evergreen clades showed a weaker positive or no relationship. CONCLUSIONS: Our work suggests that natural selection has shaped relationships between above- and belowground traits in genus Rhododendron and that leaf and root traits may evolve independently. Morphological decoupling may help explain habitat diversity among Rhododendron species, as well as the changes accompanying the divergence of deciduous and evergreen lineages.

Leaf habit and plant architecture integrate whole-plant economics and contextualize trait-climate associations within ecologically diverse genus Rhododendron.

Plant resource strategies negotiate a trade-off between fast growth and stress resistance, characterized by specific leaf area (SLA). How SLA relates to leaf structure and function or plant climate associations remains open for debate, and leaf habit and plant architecture may alter the costs versus benefits of individual traits. We used phylogenetic canonical correspondence analysis and phylogenetic least squares to understand the relationship of anatomy and gas exchange to published data on root, wood, architectural and leaf economics traits and climate. Leaf anatomy was structured by leaf habit and carbon to nitrogen ratio was a better predictor of gas exchange than SLA. We found significant correspondence of leaf anatomy with branch architecture and wood traits, gas exchange corresponded with climate, while leaf economics corresponded with climate, architecture, wood and root traits. Species from the most seasonal climates had the highest trait-climate correspondence, and different aspects of economics and anatomy reflected leaf carbon uptake versus water use. Our study using phylogenetic comparative methods including plant architecture and leaf habit provides insight into the mechanism of whole-plant functional coordination and contextualizes individual traits in relation to climate, demonstrating the evolutionary and ecological relevance of trait-trait correlations within a genus with high biodiversity.

Intraspecific variation of a desert shrub species in phenotypic plasticity in response to sand burial.

Shoot elongation is one of the main plastic responses of plants to burial, a ubiquitous stress factor in dry ecosystems. Yet, intraspecific variation in this response to burial and the extent to which this variation is functionally coordinated with variation in other trait responses are largely unknown. We subjected seedlings of the shrub Caragana intermedia from 18 maternal parents (i.e. different half-sib families) to repeated partial burial to investigate how burial affects shoot growth, stem mechanical traits and associated plasticity. Burial increased both stem elongation and diameter growth of plants, but decreased biomass production. Half-sib families had different rates of shoot elongation, and differed in their response to burial with respect to biomechanical stem properties. Across half-sib families, the magnitude of these responses in mechanical traits was positively correlated with the magnitude of the stem elongation response. These results indicate that plasticity in different stem traits in response to sand burial and intraspecific variation therein are functionally coordinated with respect to mechanical stability. The results emphasize the importance of considering functionally coordinated traits when analyzing phenotypic plasticity in plants.

Intraspecific variations of leaf hydraulic, economic, and anatomical traits in Cinnamomum camphora along an urban-rural gradient.

Urbanization brings numerous benefits to residents, but it also introduces complex, variable, and heterogeneous habitat conditions to urban plants, resulting in an arid and hot urban environment that decreases tree growth and the ecological service capacity of trees. In this study, we evaluated leaf hydraulic, economic, and anatomical traits and their covariations of Cinnamomum camphora along an urban-rural gradient in Hefei, Eastern China. We found that Cinnamomum camphora in urban adopted a conservative hydraulic strategy with low leaf turgor loss point (Tlp), leaf hydraulic conductance (Kleaf), and leaf water potential resulting in 50 % loss of hydraulic conductance (P50), as well as a quick investment-return economic strategy with low unit leaf dry matter content (LMA) and high leaf nitrogen content (Leaf N). P50, Kleaf and LMA were significantly positively correlated with the urban-rural gradient (PC1urban-rural gradient), while Leaf N exhibited a negative correlation with it. The results showed a trade-off between intraspecific safety and efficiency in leaf hydraulic traits along the urban-rural gradient and an intraspecific coordinated variation in leaf hydraulic and economic traits. In addition, based on the analysis of a trait coordination network, it was revealed that leaf mesophyll and stomata were key structures for trait adjustment and coordination. Furthermore, our findings offer a significant theoretical underpinning for the effective management of landscape trees and the strategic planning of urban tree species.