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.

Resilience and vulnerability: distinct concepts to address global change in forests.

Resilience and vulnerability are important concepts to understand, anticipate, and manage global change impacts on forest ecosystems. However, they are often used confusingly and inconsistently, hampering a synthetic understanding of global change, and impeding communication with managers and policy-makers. Both concepts are powerful and have complementary strengths, reflecting their different history, methodological approach, components, and spatiotemporal focus. Resilience assessments address the temporal response to disturbance and the mechanisms driving it. Vulnerability assessments focus on spatial patterns of exposure and susceptibility, and explicitly address adaptive capacity and stakeholder preferences. We suggest applying the distinct concepts of resilience and vulnerability where they provide particular leverage, and deduce a number of lessons learned to facilitate the next generation of global change assessments.

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.

Increased hydraulic risk in assemblages of woody plant species predicts spatial patterns of drought-induced mortality.

Predicting drought-induced mortality (DIM) of woody plants remains a key research challenge under climate change. Here, we integrate information on the edaphoclimatic niches, phylogeny and hydraulic traits of species to model the hydraulic risk of woody plants globally. We combine these models with species distribution records to estimate the hydraulic risk faced by local woody plant species assemblages. Thus, we produce global maps of hydraulic risk and test for its relationship with observed DIM. Our results show that local assemblages modelled as having higher hydraulic risk present a higher probability of DIM. Metrics characterizing this hydraulic risk improve DIM predictions globally, relative to models accounting only for edaphoclimatic predictors or broad functional groupings. The methodology we present here allows mapping of functional trait distributions and elucidation of global macro-evolutionary and biogeographical patterns, improving our ability to predict potential global change impacts on vegetation.

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.

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.

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.

Networking the forest infrastructure towards near real-time monitoring - A white paper.

Forests account for nearly 90 % of the world's terrestrial biomass in the form of carbon and they support 80 % of the global biodiversity. To understand the underlying forest dynamics, we need a long-term but also relatively high-frequency, networked monitoring system, as traditionally used in meteorology or hydrology. While there are numerous existing forest monitoring sites, particularly in temperate regions, the resulting data streams are rarely connected and do not provide information promptly, which hampers real-time assessments of forest responses to extreme climate events. The technology to build a better global forest monitoring network now exists. This white paper addresses the key structural components needed to achieve a novel meta-network. We propose to complement - rather than replace or unify - the existing heterogeneous infrastructure with standardized, quality-assured linking methods and interacting data processing centers to create an integrated forest monitoring network. These automated (research topic-dependent) linking methods in atmosphere, biosphere, and pedosphere play a key role in scaling site-specific results and processing them in a timely manner. To ensure broad participation from existing monitoring sites and to establish new sites, these linking methods must be as informative, reliable, affordable, and maintainable as possible, and should be supplemented by near real-time remote sensing data. The proposed novel meta-network will enable the detection of emergent patterns that would not be visible from isolated analyses of individual sites. In addition, the near real-time availability of data will facilitate predictions of current forest conditions (nowcasts), which are urgently needed for research and decision making in the face of rapid climate change. We call for international and interdisciplinary efforts in this direction.

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.

Non-structural carbohydrates and morphological traits of leaves, stems and roots from tree species in different climates.

OBJECTIVES: Carbon fixed during photosynthesis is exported from leaves towards sink organs as non-structural carbohydrates (NSC), that are a key energy source for metabolic processes in trees. In xylem, NSC are mostly stored as soluble sugars and starch in radial and axial parenchyma. The multi-functional nature of xylem means that cells possess several functions, including water transport, storage and mechanical support. Little is known about how NSC impacts xylem multi-functionality, nor how NSC vary among species and climates. We collected leaves, stem and root xylem from tree species growing in three climates and estimated NSC in each organ. We also measured xylem traits linked to hydraulic and mechanical functioning. DATA DESCRIPTION: The paper describes functional traits in leaves, stems and roots, including NSC, carbon, nitrogen, specific leaf area, stem and root wood density and xylem traits. Data are provided for up to 90 angiosperm species from temperate, Mediterranean and tropical climates. These data are useful for understanding the trade-offs in resource allocation from a whole-plant perspective, and to better quantify xylem structure and function related to water transportation, mechanical support and storage. Data will also give researchers keys to understanding the ability of trees to adjust to a changing climate.

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.

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 Change Risks to Global Forest Health: Emergence of Unexpected Events of Elevated Tree Mortality Worldwide.

Recent observations of elevated tree mortality following climate extremes, like heat and drought, raise concerns about climate change risks to global forest health. We currently lack both sufficient data and understanding to identify whether these observations represent a global trend toward increasing tree mortality. Here, we document events of sudden and unexpected elevated tree mortality following heat and drought events in ecosystems that previously were considered tolerant or not at risk of exposure. These events underscore the fact that climate change may affect forests with unexpected force in the future. We use the events as examples to highlight current difficulties and challenges for realistically predicting such tree mortality events and the uncertainties about future forest condition. Advances in remote sensing technology and greater availably of high-resolution data, from both field assessments and satellites, are needed to improve both understanding and prediction of forest responses to future climate change.

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.

The 2018 European heatwave led to stem dehydration but not to consistent growth reductions in forests.

Heatwaves exert disproportionately strong and sometimes irreversible impacts on forest ecosystems. These impacts remain poorly understood at the tree and species level and across large spatial scales. Here, we investigate the effects of the record-breaking 2018 European heatwave on tree growth and tree water status using a collection of high-temporal resolution dendrometer data from 21 species across 53 sites. Relative to the two preceding years, annual stem growth was not consistently reduced by the 2018 heatwave but stems experienced twice the temporary shrinkage due to depletion of water reserves. Conifer species were less capable of rehydrating overnight than broadleaves across gradients of soil and atmospheric drought, suggesting less resilience toward transient stress. In particular, Norway spruce and Scots pine experienced extensive stem dehydration. Our high-resolution dendrometer network was suitable to disentangle the effects of a severe heatwave on tree growth and desiccation at large-spatial scales in situ, and provided insights on which species may be more vulnerable to climate extremes.

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.

Reserve Accumulation Is Prioritized Over Growth Following Single or Combined Injuries in Three Common North American Urban Tree Species.

Trees that grow in urban areas are confronted with a wide variety of stresses that undermine their long-term survival. These include mechanical damage to the crown, root reduction and stem injury, all of which remove significant parts of plant tissues. The single or combined effects of these stresses generate a complex array of growth and ecophysiological responses that are hard to predict. Here we evaluated the effects of different individual and combined damage on the dynamics of non-structural carbohydrates (NSC, low weight sugars plus starch) concentration and new tissue growth (diameter increment) in young trees. We hypothesized that (i) tissue damage will induce larger reductions in diameter growth than in NSC concentrations and (ii) combinations of stress treatments that minimally alter the "functional equilibrium" (e.g., similar reductions of leaf and root area) would have the least impact on NSC concentrations (although not on growth) helping to maintain tree health and integrity. To test these hypotheses, we set up a manipulative field experiment with 10-year-old trees of common urban species (Celtis occidentalis, Fraxinus pennsylvanica, and Tilia cordata). These trees were treated with a complete array of mechanical damage combinations at different levels of intensity (i.e., three levels of defoliation and root reduction, and two levels of stem damage). We found that tree growth declined in relation to the total amount of stress inflicted on the trees, i.e., when the combined highest level of stress was applied, but NSC concentrations were either not affected or, in some cases, increased with an increasing level of stress. We did not find a consistent response in concentration of reserves in relation to the combined stress treatments. Therefore, trees appear to reach a new "functional equilibrium" that allows them to adjust their levels of carbohydrate reserves, especially in stems and roots, to meet their metabolic demand under stressful situations. Our results provide a unique insight into the carbon economy of trees facing multiple urban stress conditions in order to better predict long-term tree performance and vitality.

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.