Community assembly influences plant trait economic spectra and functional trade-offs at ecosystem scales.

Plant functional traits hold the potential to greatly improve the understanding and prediction of climate impacts on ecosystems and carbon cycle feedback to climate change. Traits are commonly used to place species along a global conservative-acquisitive trade-off, yet how and if functional traits and conservative-acquisitive trade-offs scale up to mediate community and ecosystem fluxes is largely unknown. Here, we combine functional trait datasets and multibiome datasets of forest water and carbon fluxes at the species, community, and ecosystem-levels to quantify the scaling of the tradeoff between maximum flux and sensitivity to vapor pressure deficit. We find a strong conservative-acquisitive trade-off at the species scale, which weakens modestly at the community scale and largely disappears at the ecosystem scale. Functional traits, particularly plant water transport (hydraulic) traits, are strongly associated with the key dimensions of the conservative-acquisitive trade-off at community and ecosystem scales, highlighting that trait composition appears to influence community and ecosystem flux dynamics. Our findings provide a foundation for improving carbon cycle models by revealing i) that plant hydraulic traits are most strongly associated with community- and ecosystem scale flux dynamics and ii) community assembly dynamics likely need to be considered explicitly, as they give rise to ecosystem-level flux dynamics that differ substantially from trade-offs identified at the species-level.

The impacts of rising vapour pressure deficit in natural and managed ecosystems.

An exponential rise in the atmospheric vapour pressure deficit (VPD) is among the most consequential impacts of climate change in terrestrial ecosystems. Rising VPD has negative and cascading effects on nearly all aspects of plant function including photosynthesis, water status, growth and survival. These responses are exacerbated by land-atmosphere interactions that couple VPD to soil water and govern the evolution of drought, affecting a range of ecosystem services including carbon uptake, biodiversity, the provisioning of water resources and crop yields. However, despite the global nature of this phenomenon, research on how to incorporate these impacts into resilient management regimes is largely in its infancy, due in part to the entanglement of VPD trends with those of other co-evolving climate drivers. Here, we review the mechanistic bases of VPD impacts at a range of spatial scales, paying particular attention to the independent and interactive influence of VPD in the context of other environmental changes. We then evaluate the consequences of these impacts within key management contexts, including water resources, croplands, wildfire risk mitigation and management of natural grasslands and forests. We conclude with recommendations describing how management regimes could be altered to mitigate the otherwise highly deleterious consequences of rising VPD.

A new empirical framework to quantify the hydraulic effects of soil and atmospheric drivers on plant water status.

Metrics to quantify regulation of plant water status at the daily as opposed to the seasonal scale do not presently exist. This gap is significant since plants are hypothesised to regulate their water potential not only with respect to slowly changing soil drought but also with respect to faster changes in air vapour pressure deficit (VPD), a variable whose importance for plant physiology is expected to grow because of higher temperatures in the coming decades. We present a metric, the stringency of water potential regulation, that can be employed at the daily scale and quantifies the effects exerted on plants by the separate and combined effect of soil and atmospheric drought. We test our theory using datasets from two experiments where air temperature and VPD were experimentally manipulated. In contrast to existing metrics based on soil drought that can only be applied at the seasonal scale, our metric successfully detects the impact of atmospheric warming on the regulation of plant water status. We show that the thermodynamic effect of VPD on plant water status can be isolated and compared against that exerted by soil drought and the covariation between VPD and soil drought. Furthermore, in three of three cases, VPD accounted for more than 5 MPa of potential effect on leaf water potential. We explore the significance of our findings in the context of potential future applications of this metric from plant to ecosystem scale.

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.

The role of height-driven constraints and compensations on tree vulnerability to drought.

Frequent observations of higher mortality in larger trees than in smaller ones during droughts have sparked an increasing interest in size-dependent drought-induced mortality. However, the underlying physiological mechanisms are not well understood, with height-associated hydraulic constraints often being implied as the potential mechanism driving increased drought vulnerability. We performed a quantitative synthesis on how key traits that drive plant water and carbon economy change with tree height within species and assessed the implications that the different constraints and compensations may have on the interacting mechanisms (hydraulic failure, carbon starvation and/or biotic-agent attacks) affecting tree vulnerability to drought. While xylem tension increases with tree height, taller trees present a range of structural and functional adjustments, including more efficient water use and transport and greater water uptake and storage capacity, that mitigate the path-length-associated drop in water potential. These adaptations allow taller trees to withstand episodic water stress. Conclusive evidence for height-dependent increased vulnerability to hydraulic failure and carbon starvation, and their coupling to defence mechanisms and pest and pathogen dynamics, is still lacking. Further research is needed, particularly at the intraspecific level, to ascertain the specific conditions and thresholds above which height hinders tree survival under drought.

Functional trade-offs are driven by coordinated changes among cell types in the wood of angiosperm trees from different climates.

Wood performs several functions to ensure tree survival and carbon allocation to a finite stem volume leads to trade-offs among cell types. It is not known to what extent these trade-offs modify functional trade-offs and if they are consistent across climates and evolutionary lineages. Twelve wood traits were measured in stems and coarse roots across 60 adult angiosperm tree species from temperate, Mediterranean and tropical climates. Regardless of climate, clear trade-offs occurred among cellular fractions, but did not translate into specific functional trade-offs. Wood density was negatively related to hydraulic conductivity (Kth ) in stems and roots, but was not linked to nonstructural carbohydrates (NSC), implying a functional trade-off between mechanical integrity and transport but not with storage. NSC storage capacity was positively associated with Kth in stems and negatively in roots, reflecting a potential role for NSC in the maintenance of hydraulic integrity in stems but not in roots. Results of phylogenetic analyses suggest that evolutionary histories cannot explain covariations among traits. Trade-offs occur among cellular fractions, without necessarily modifying trade-offs in function. However, functional trade-offs are driven by coordinated changes among xylem cell types depending on the dominant role of each cell type in stems and roots.

Global variation in nonstructural carbohydrate stores in response to climate.

Woody plant species store nonstructural carbohydrates (NSCs) for many functions. While known to buffer against fluctuations in photosynthetic supply, such as at night, NSC stores are also thought to buffer against environmental extremes, such as drought or freezing temperatures by serving as either back-up energy reserves or osmolytes. However, a clear picture of how NSCs are shaped by climate is still lacking. Here, we update and leverage a unique global database of seasonal NSC storage measurements to examine whether maximum total NSC stores and the amount of soluble sugars are associated with clinal patterns in low temperatures or aridity, indicating they may confer a benefit under freezing or drought conditions. We examine patterns using the average climate at each study site and the unique climatic conditions at the time and place in which the sample was taken. Altogether, our results support the idea that NSC stores act as critical osmolytes. Soluble Sugars increase with both colder and drier conditions in aboveground tissues, indicating they can plastically increase a plants' tolerance of cold or arid conditions. However, maximum total NSCs increased, rather than decreased, with average site temperature and had no relationship to average site aridity. This result suggests that the total amount of NSC a plant stores may be more strongly determined by its capacity to assimilate carbon than by environmental stress. Thus, NSCs are unlikely to serve as reservoir of energy. This study is the most comprehensive synthesis to date of global NSC variation in relation to climate and supports the idea that NSC stores likely serve as buffers against environmental stress. By clarifying their role in cold and drought tolerance, we improve our ability to predict plant response to environment.

Interaction of drought- and pathogen-induced mortality in Norway spruce and Scots pine.

Pathogenic diseases frequently occur in drought-stressed trees. However, their contribution to the process of drought-induced mortality is poorly understood. We combined drought and stem inoculation treatments to study the physiological processes leading to drought-induced mortality in Norway spruce (Picea abies) and Scots pine (Pinus sylvestris) saplings infected with Heterobasidion annosum s.s. We analysed the saplings' water status, gas exchange, nonstructural carbohydrates (NSCs) and defence responses, and how they related to mortality. Saplings were followed for two growing seasons, including an artificially induced 3-month dormancy period. The combined drought and pathogen treatment significantly increased spruce mortality; however, no interaction between these stressors was observed in pine, although individually each stressor caused mortality. Our results suggest that pathogen infection decreased carbon reserves in spruce, reducing the capacity of saplings to cope with drought, resulting in increased mortality rates. Defoliation, relative water content and the starch concentration of needles were predictors of mortality in both species under drought and pathogen infection. Infection and drought stress create conflicting needs for carbon to compartmentalize the pathogen and to avoid turgor loss, respectively. Heterobasidion annosum reduces the functional sapwood area and shifts NSC allocation patterns, reducing the capacity of trees to cope with drought.

Wood density and hydraulic traits influence species' growth response to drought across biomes.

Tree species display a wide variety of water-use strategies, growth rates and capacity to tolerate drought. However, if we want to forecast species capacity to cope with increasing aridity and drought, we need to identify which measurable traits confer resilience to drought across species. Here, we use a global tree ring network (65 species; 1931 site series of ring-width indices-RWI) to evaluate the relationship of long-term growth-drought sensitivity (RWI-SPEI drought index relationship) and short-term growth response to extreme drought episodes (resistance, recovery and resilience indices) with functional traits related to leaf, wood and hydraulic properties. Furthermore, we assess the influence of climate (temperature, precipitation and climatic water deficit) on these trait-growth relationships. We found a close correspondence between the long-term relationship between RWI and SPEI and resistance and recovery of tree growth to severe drought episodes. Species displaying a stronger RWI-SPEI relationship to drought and low resistance and high recovery to extreme drought episodes tended to have a higher wood density (WD) and more negative leaf minimum water potential (Ψmin). Such associations were largely maintained when accounting for direct climate effects. Our results indicate that, at a cross-species level and global scale, wood and hydraulic functional traits explain species' growth responses to drought at short- and long-term scales. These trait-growth response relationships can improve our understanding of the cross-species capacity to withstand climate change and inform models to better predict drought effects on forest ecosystem dynamics.

Parenchyma fractions drive the storage capacity of nonstructural carbohydrates across a broad range of tree species.

PREMISE: Nonstructural carbohydrates (NSCs) play a key role in tree performance and functioning and are stored in radial and axial parenchyma (RAP) cells. Whether this relationship is altered among species and climates or is linked to functional traits describing xylem structure (wood density) and tree stature is not known. METHODS: In a systematic review, we collated data for NSC content and the proportion of RAP in stems for 68 tree species. To examine the relationships of NSCs and RAP with climatic factors and other functional traits, we also collected climatic data at each tree's location, as well as wood density and maximum height. A phylogenetic tree was constructed to examine the influence of species' evolutionary relationships on the associations among NSCs, RAP, and functional traits. RESULTS: Across all 68 tree species, NSCs were positively correlated with RAP and mean annual temperature, but relationships were only weakly significant in temperate species and angiosperms. When separating RAP into radial parenchyma (RP) and axial parenchyma (AP), both NSCs and wood density were positively correlated with RP but not with AP. Wood in taller trees was less dense and had lower RAP than in shorter trees, but height was not related to NSCs. CONCLUSIONS: In trees, NSCs are stored mostly in the RP fraction, which has a larger surface area in warmer climates. Additionally, NSCs were only weakly linked to wood density and tree height. Our analysis of evolutionary relationships demonstrated that RAP fractions and NSC content were always closely related across all 68 tree species, suggesting that RAP can act as a reliable proxy for potential NSC storage capacity in tree stems.

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'.

Towards a statistically robust determination of minimum water potential and hydraulic risk in plants.

Minimum water potential (Ψmin ) is a key variable for characterizing dehydration tolerance and hydraulic safety margins (HSMs) in plants. Ψmin is usually estimated as the absolute minimum tissue Ψ experienced by a species, but this is problematic because sample extremes are affected by sample size and the underlying probability distribution. We compare alternative approaches to estimate Ψmin and assess the corresponding uncertainties and biases; propose statistically robust estimation methods based on extreme value theory (EVT); and assess the implications of our results for the characterization of hydraulic risk. Our results show that current estimates of Ψmin and HSMs are biased, as they are strongly affected by sample size. Because sampling effort is generally higher for species living in dry environments, the differences in current Ψmin estimates between these species and those living under milder conditions are partly artefactual. When this bias is corrected using EVT methods, resulting HSMs tend to increase substantially with resistance to embolism across species. Although data availability and representativeness remain the main challenges for proper determination of Ψmin , a closer look at Ψ distributions and the use of statistically robust methods to estimate Ψmin opens new ground for characterizing plant hydraulic risks.

Low forest productivity associated with increasing drought-tolerant species is compensated by an increase in drought-tolerance richness.

Many temperate forests are changing in composition due to a combination of changes in land-use, management and climate-related disturbances. Previous research has shown that in some regions these changes frequently favour drought-tolerant tree species. However, the effects of these changes in composition on forest functioning (e.g. productivity) are unclear. We studied 25 years of change in individual tree biomass growth, ingrowth and mortality, and community composition and total plot biomass across 2663 permanent forest plots in Catalonia (NE Spain) comprising 85,220 trees of 59 species. We focused on the relationship between community-level forest productivity and drought tolerance (DT), which was estimated using hydraulic traits as well as biogeographic indicators. We found that there was a small increase (1.6%-3.2% on average) in community-mean DT (DTcwm) during the study period, concurrent with a strong increase (12.4%-19.4% on average) in DT richness (DTric; i.e. trait range). Most importantly, we found that the mean DT was negatively related to forest productivity, which was explained because drought-tolerant tree species have lower tree-level growth. In contrast, DT richness was strongly and positively related to forest productivity, probably because it allowed for a more stable production along wet and dry periods. These results suggest a negative impact of ongoing climate change on forest productivity mediated by functional composition shifts (i.e. selection of drought-tolerant species), and a positive effect of increased DT richness as a consequence of land-use legacies. Such a trend towards functional diversification, although temporary, would increase forests' capacity to resist drought and place them in a better position to face the expected change in climate.

Detecting forest response to droughts with global observations of vegetation water content.

Droughts in a warming climate have become more common and more extreme, making understanding forest responses to water stress increasingly pressing. Analysis of water stress in trees has long focused on water potential in xylem and leaves, which influences stomatal closure and water flow through the soil-plant-atmosphere continuum. At the same time, changes of vegetation water content (VWC) are linked to a range of tree responses, including fluxes of water and carbon, mortality, flammability, and more. Unlike water potential, which requires demanding in situ measurements, VWC can be retrieved from remote sensing measurements, particularly at microwave frequencies using radar and radiometry. Here, we highlight key frontiers through which VWC has the potential to significantly increase our understanding of forest responses to water stress. To validate remote sensing observations of VWC at landscape scale and to better relate them to data assimilation model parameters, we introduce an ecosystem-scale analog of the pressure-volume curve, the non-linear relationship between average leaf or branch water potential and water content commonly used in plant hydraulics. The sources of variability in these ecosystem-scale pressure-volume curves and their relationship to forest response to water stress are discussed. We further show to what extent diel, seasonal, and decadal dynamics of VWC reflect variations in different processes relating the tree response to water stress. VWC can also be used for inferring belowground conditions-which are difficult to impossible to observe directly. Lastly, we discuss how a dedicated geostationary spaceborne observational system for VWC, when combined with existing datasets, can capture diel and seasonal water dynamics to advance the science and applications of global forest vulnerability to future droughts.

Adaptation and coordinated evolution of plant hydraulic traits.

Hydraulic properties control plant responses to climate and are likely to be under strong selective pressure, but their macro-evolutionary history remains poorly characterised. To fill this gap, we compiled a global dataset of hydraulic traits describing xylem conductivity (Ks ), xylem resistance to embolism (P50), sapwood allocation relative to leaf area (Hv) and drought exposure (ψmin ), and matched it with global seed plant phylogenies. Individually, these traits present medium to high levels of phylogenetic signal, partly related to environmental selective pressures shaping lineage evolution. Most of these traits evolved independently of each other, being co-selected by the same environmental pressures. However, the evolutionary correlations between P50 and ψmin and between Ks and Hv show signs of deeper evolutionary integration because of functional, developmental or genetic constraints, conforming to evolutionary modules. We do not detect evolutionary integration between conductivity and resistance to embolism, rejecting a hardwired trade-off for this pair of traits.

Temperature and water potential co-limit stem cambial activity along a steep elevational gradient.

Efforts to develop mechanistic tree growth models are hindered by the uncertainty of whether and when tree growth responses to environmental factors are driven by carbon assimilation or by biophysical limitations of wood formation. In this study, we used multiannual weekly wood-formation monitoring of two conifer species (Larix decidua and Picea abies) along a 900 m elevational gradient in the Swiss Alps to assess the biophysical effect of temperature and water potential on wood formation. To this end, we developed a model that simulates the effect of water potential on turgor-driven cambial division, modulated by the effect of temperature on enzymatic activity. The model reproduced the observed phenology of tracheid production, as well as intra- and interannual tracheid production dynamics of both species along the elevational gradient, although interannual model performance was lower. We found that temperature alone explains the onset of tracheid production, yet water potential appears necessary to predict the ending and the total amount of tracheids produced annually. We conclude that intra-annual cambial activity is strongly constrained by both temperature and water potential at all elevations, independently of carbon assimilation. At the interannual scale, biophysical constraints likely interact with other factors.

Water potential control of turgor-driven tracheid enlargement in Scots pine at its xeric distribution edge.

The extent to which water availability can be used to predict the enlargement and final dimensions of xylem conduits remains an open issue. We reconstructed the time course of tracheid enlargement in Pinus sylvestris trees in central Spain by repeated measurements of tracheid diameter on microcores sampled weekly during a 2 yr period. We analyzed the role of water availability in these dynamics empirically through time-series correlation analysis and mechanistically by building a model that simulates daily tracheid enlargement rate and duration based on Lockhart's equation and water potential as the sole input. Tracheid enlargement followed a sigmoid-like time course, which varied intra- and interannually. Our empirical analysis showed that final tracheid diameter was strongly related to water availability during tracheid enlargement. The mechanistic model was calibrated and successfully validated (R2  = 0.92) against the observed tracheid enlargement time course. The model was also able to reproduce the seasonal variations of tracheid enlargement rate, duration and final diameter (R2  = 0.84-0.99). Our results support the hypothesis that tracheid enlargement and final dimensions can be modeled based on the direct effect of water potential on turgor-driven cell expansion. We argue that such a mechanism is consistent with other reported patterns of tracheid dimension variation.

Growth and resilience responses of Scots pine to extreme droughts across Europe depend on predrought growth conditions.

Global climate change is expected to further raise the frequency and severity of extreme events, such as droughts. The effects of extreme droughts on trees are difficult to disentangle given the inherent complexity of drought events (frequency, severity, duration, and timing during the growing season). Besides, drought effects might be modulated by trees' phenotypic variability, which is, in turn, affected by long-term local selective pressures and management legacies. Here we investigated the magnitude and the temporal changes of tree-level resilience (i.e., resistance, recovery, and resilience) to extreme droughts. Moreover, we assessed the tree-, site-, and drought-related factors and their interactions driving the tree-level resilience to extreme droughts. We used a tree-ring network of the widely distributed Scots pine (Pinus sylvestris) along a 2,800 km latitudinal gradient from southern Spain to northern Germany. We found that the resilience to extreme drought decreased in mid-elevation and low productivity sites from 1980-1999 to 2000-2011 likely due to more frequent and severe droughts in the later period. Our study showed that the impact of drought on tree-level resilience was not dependent on its latitudinal location, but rather on the type of sites trees were growing at and on their growth performances (i.e., magnitude and variability of growth) during the predrought period. We found significant interactive effects between drought duration and tree growth prior to drought, suggesting that Scots pine trees with higher magnitude and variability of growth in the long term are more vulnerable to long and severe droughts. Moreover, our results indicate that Scots pine trees that experienced more frequent droughts over the long-term were less resistant to extreme droughts. We, therefore, conclude that the physiological resilience to extreme droughts might be constrained by their growth prior to drought, and that more frequent and longer drought periods may overstrain their potential for acclimation.

Greater focus on water pools may improve our ability to understand and anticipate drought-induced mortality in plants.

Drought-induced tree mortality has major impacts on ecosystem carbon and water cycles, and is expected to increase in forests across the globe with climate change. A large body of research in the past decade has advanced our understanding of plant water and carbon relations under drought. However, despite intense research, we still lack generalizable, cross-scale indicators of mortality risk. In this Viewpoint, we propose that a more explicit consideration of water pools could improve our ability to monitor and anticipate mortality risk. Specifically, we focus on the relative water content (RWC), a classic metric in plant water relations, as a potential indicator of mortality risk that is physiologically relevant and integrates different aspects related to hydraulics, stomatal responses and carbon economy under drought. Measures of plant water content are likely to have a strong mechanistic link with mortality and to be integrative, threshold-prone and relatively easy to measure and monitor at large spatial scales, and may complement current mortality metrics based on water potential, loss of hydraulic conductivity and nonstructural carbohydrates. We discuss some of the potential advantages and limitations of these metrics to improve our capacity to monitor and predict drought-induced tree mortality.

Adjustments and coordination of hydraulic, leaf and stem traits along a water availability gradient.

Trait variability in space and time allows plants to adjust to changing environmental conditions. However, we know little about how this variability is distributed and coordinated at different organizational levels. For six dominant tree species in northeastern Spain (three Fagaceae and three Pinaceae) we quantified the inter- and intraspecific variability of a set of traits along a water availability gradient. We measured leaf mass per area (LMA), leaf nitrogen (N) concentration, carbon isotope composition in leaves (δ13 C), stem wood density, the Huber value (Hv, the ratio of cross-sectional sapwood area to leaf area), sapwood-specific and leaf-specific stem hydraulic conductivity, vulnerability to xylem embolism (P50 ) and the turgor loss point (Ptlp ). Differences between families explained the largest amount of variability for most traits, although intraspecific variability was also relevant. Species occupying wetter sites showed higher N, P50 and Ptlp , and lower LMA, δ13 C and Hv. However, when trait relationships with water availability were assessed within species they held only for Hv and Ptlp . Overall, our results indicate that intraspecific adjustments along the water availability gradient relied primarily on changes in resource allocation between sapwood and leaf area and in leaf water relations.