Tree water uptake patterns across the globe.

Plant water uptake from the soil is a crucial element of the global hydrological cycle and essential for vegetation drought resilience. Yet, knowledge of how the distribution of water uptake depth (WUD) varies across species, climates, and seasons is scarce relative to our knowledge of aboveground plant functions. With a global literature review, we found that average WUD varied more among biomes than plant functional types (i.e. deciduous/evergreen broadleaves and conifers), illustrating the importance of the hydroclimate, especially precipitation seasonality, on WUD. By combining records of rooting depth with WUD, we observed a consistently deeper maximum rooting depth than WUD with the largest differences in arid regions - indicating that deep taproots act as lifelines while not contributing to the majority of water uptake. The most ubiquitous observation across the literature was that woody plants switch water sources to soil layers with the highest water availability within short timescales. Hence, seasonal shifts to deep soil layers occur across the globe when shallow soils are drying out, allowing continued transpiration and hydraulic safety. While there are still significant gaps in our understanding of WUD, the consistency across global ecosystems allows integration of existing knowledge into the next generation of vegetation process models.

Contrasting coordination of non-structural carbohydrates with leaf and root economic strategies of alpine coniferous forests.

Non-structural carbohydrates (NSCs), as the labile fraction and dominant carbon currency, are essential mediators of plant adaptation to environments. However, whether and how NSC coordinates with plant economic strategy frameworks, particularly the well-recognized leaf economics spectrums (LES) and root economics space (RES), remains unclear. We examined the relationships between NSC and key plant economics traits in leaves and fine roots across 90 alpine coniferous populations on the Tibetan Plateau, China. We observed contrasting coordination of NSC with economics traits in leaves and roots. Leaf total NSC and soluble sugar aligned with the leaf economic spectrum, conveying a trade-off between growth and storage in leaves. However, NSC in roots was independent of the root economic spectrum, but highly coordinated with root foraging, with more starch and less sugar in forage-efficient, thinner roots. Further, NSC-trait coordination in leaves and roots was, respectively, driven by local temperature and precipitation. These findings highlight distinct roles of NSC in shaping the above- and belowground multidimensional economics trait space, and NSC-based carbon economics provides a mechanistic understanding of how plants adapt to heterogeneous habitats and respond to environmental changes.

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.

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.

Carbon starvation following a decade of experimental drought consumes old reserves in Pinus edulis.

Shifts in the age or turnover time of non-structural carbohydrates (NSC) may underlie changes in tree growth under long-term increases in drought stress associated with climate change. But NSC responses to drought are challenging to quantify, due in part to large NSC stores in trees and subsequently long response times of NSC to climate variation. We measured NSC age (Δ14 C) along with a suite of ecophysiological metrics in Pinus edulis trees experiencing either extreme short-term drought (-90% ambient precipitation plot, 2020-2021) or a decade of severe drought (-45% plot, 2010-2021). We tested the hypothesis that carbon starvation - consumption exceeding synthesis and storage - increases the age of sapwood NSC. One year of extreme drought had no impact on NSC pool size or age, despite significant reductions in predawn water potential, photosynthetic rates/capacity, and twig and needle growth. By contrast, long-term drought halved the age of the sapwood NSC pool, coupled with reductions in sapwood starch concentrations (-75%), basal area increment (-39%), and bole respiration rates (-28%). Our results suggest carbon starvation takes time, as tree carbon reserves appear resilient to extreme disturbance in the short term. However, after a decade of drought, trees apparently consumed old stored NSC to support metabolism.

Fermentation-mediated growth, signaling, and defense in plants.

While traditionally considered important mainly in hypoxic roots during flooding, upregulation of fermentation pathways in plants has recently been described as an evolutionarily conserved drought survival strategy, with acetate signaling mediating reprograming of transcription and cellular carbon and energy metabolism from roots to leaves. The amount of acetate produced directly correlates with survival through potential mechanisms including defense gene activation, biosynthesis of primary and secondary metabolites, and aerobic respiration. Here, we review root ethanolic fermentation responses to hypoxia during saturated soil conditions and summarize studies highlighting acetate fermentation under aerobic conditions coupled with respiration during growth and drought responses. Recent work is discussed demonstrating long-distance transport of acetate via the transpiration stream as a respiratory substrate. While maintenance and growth respiration are often modeled separately in terrestrial models, here we propose the concept of 'Defense Respiration' fueled by acetate fermentation in which upregulation of acetate fermentation contributes acetate substrate for alternative energy production via aerobic respiration, biosynthesis of primary and secondary metabolites, and the acetylation of proteins involved in defense gene regulation. Finally, we highlight new frontiers in leaf-atmosphere emission measurements as a potential way to study acetate fermentation responses of individual leaves, branches, ecosystems, and regions.

Modeling the mechanisms of conifer mortality under seawater exposure.

Relative sea level rise (SLR) increasingly impacts coastal ecosystems through the formation of ghost forests. To predict the future of coastal ecosystems under SLR and changing climate, it is important to understand the physiological mechanisms underlying coastal tree mortality and to integrate this knowledge into dynamic vegetation models. We incorporate the physiological effect of salinity and hypoxia in a dynamic vegetation model in the Earth system land model, and used the model to investigate the mechanisms of mortality of conifer forests on the west and east coast sites of USA, where trees experience different form of sea water exposure. Simulations suggest similar physiological mechanisms can result in different mortality patterns. At the east coast site that experienced severe increases in seawater exposure, trees loose photosynthetic capacity and roots rapidly, and both storage carbon and hydraulic conductance decrease significantly within a year. Over time, further consumption of storage carbon that leads to carbon starvation dominates mortality. At the west coast site that gradually exposed to seawater through SLR, hydraulic failure dominates mortality because root loss impacts on conductance are greater than the degree of storage carbon depletion. Measurements and modeling focused on understanding the physiological mechanisms of mortality is critical to reducing predictive uncertainty.

No carbon storage in growth-limited trees in a semi-arid woodland.

Plant survival depends on a balance between carbon supply and demand. When carbon supply becomes limited, plants buffer demand by using stored carbohydrates (sugar and starch). During drought, NSCs (non-structural carbohydrates) may accumulate if growth stops before photosynthesis. This expectation is pervasive, yet few studies have combined simultaneous measurements of drought, photosynthesis, growth, and carbon storage to test this. Using a field experiment with mature trees in a semi-arid woodland, we show that growth and photosynthesis slow in parallel as [Formula: see text] declines, preventing carbon storage in two species of conifer (J. monosperma and P. edulis). During experimental drought, growth and photosynthesis were frequently co-limited. Our results point to an alternative perspective on how plants use carbon that views growth and photosynthesis as independent processes both regulated by water availability.

Vegetation browning: global drivers, impacts, and feedbacks.

As global climate conditions continue to change, disturbance regimes and environmental drivers will continue to shift, impacting global vegetation dynamics. Following a period of vegetation greening, there has been a progressive increase in remotely sensed vegetation browning globally. Given the many societal benefits that forests provide, it is critical that we understand vegetation dynamic alterations. Here, we review associative drivers, impacts, and feedbacks, revealing the complexity of browning. Concomitant increases in browning include the weakening of ecosystem services and functions and alterations to vegetation structure and species composition, as well as the development of potential positive climate change feedbacks. Also discussed are the current challenges in browning detection and understanding associated impacts and feedbacks. Finally, we outline recommended strategies.

Physiological response and photosynthetic recovery to an extreme drought: Evidence from plants in a dry-hot valley savanna of Southwest China.

The frequency of extreme drought events has been rising worldwide, but due to its unpredictability, how plants will respond remains poorly understood. Here, we aimed to characterize how the hydraulics and photosynthesis of savanna plants respond to extreme drought, and tested whether they can subsequently recover photosynthesis after drought. There was an extreme drought in 2019 in Southwest (SW) China. We investigated photosynthetic gas exchange, leaf-, stem-, and whole-shoot hydraulic conductance of 18 plant species with diverse leaf habits (deciduous, semi-deciduous and evergreen) and growth forms (tree and shrub) from a dry-hot valley savanna in SW China for three rainy seasons from 2019 to 2021. We also compared photosynthetic gas exchange to those of a regular year (2014). We found that leaf stomatal and hydraulic conductance and maximum photosynthetic rate were significantly lower during the drought in 2019 than in the wetter years. In 2019, all studied plants maintained stomatal conductance at their minimum level observed, which could be related to high vapor pressure deficits (VPD, >2 kPa). However, no significant difference in stem and shoot hydraulic conductance was detected across years. The reductions in leaf hydraulic conductance and stomatal regulation under extreme drought might help keep the stem hydraulic function. Stomatal conductance and photosynthesis after drought (2020 and 2021) showed comparable or even higher values compared to that of 2014, suggesting high recovery of photosynthetic gas exchange. In addition, the response of hydraulic and photosynthetic traits to extreme drought was convergent across leaf habits and growth forms. Our results will help better understand the physiological mechanism underlying the response of savanna ecosystems to climate change.

Drought-induced increase in tree mortality and corresponding decrease in the carbon sink capacity of Canada's boreal forests from 1970 to 2020.

Canada's boreal forests, which occupy approximately 30% of boreal forests worldwide, play an important role in the global carbon budget. However, there is little quantitative information available regarding the spatiotemporal changes in the drought-induced tree mortality of Canada's boreal forests overall and their associated impacts on biomass carbon dynamics. Here, we develop spatiotemporally explicit estimates of drought-induced tree mortality and corresponding biomass carbon sink capacity changes in Canada's boreal forests from 1970 to 2020. We show that the average annual tree mortality rate is approximately 2.7%. Approximately 43% of Canada's boreal forests have experienced significantly increasing tree mortality trends (71% of which are located in the western region of the country), and these trends have accelerated since 2002. This increase in tree mortality has resulted in significant biomass carbon losses at an approximate rate of 1.51 ± 0.29 MgC ha-1  year-1 (95% confidence interval) with an approximate total loss of 0.46 ± 0.09 PgC year-1 (95% confidence interval). Under the drought condition increases predicted for this century, the capacity of Canada's boreal forests to act as a carbon sink will be further reduced, potentially leading to a significant positive climate feedback effect.

Short-term variation in leaf-level water use efficiency in a tropical forest.

The representation of stomatal regulation of transpiration and CO2 assimilation is key to forecasting terrestrial ecosystem responses to global change. Given its importance in determining the relationship between forest productivity and climate, accurate and mechanistic model representation of the relationship between stomatal conductance (gs ) and assimilation is crucial. We assess possible physiological and mechanistic controls on the estimation of the g1 (stomatal slope, inversely proportional to water use efficiency) and g0 (stomatal intercept) parameters, using diurnal gas exchange surveys and leaf-level response curves of six tropical broadleaf evergreen tree species. g1 estimated from ex situ response curves averaged 50% less than g1 estimated from survey data. While g0 and g1 varied between leaves of different phenological stages, the trend was not consistent among species. We identified a diurnal trend associated with g1 and g0 that significantly improved model projections of diurnal trends in transpiration. The accuracy of modeled gs can be improved by accounting for variation in stomatal behavior across diurnal periods, and between measurement approaches, rather than focusing on phenological variation in stomatal behavior. Additional investigation into the primary mechanisms responsible for diurnal variation in g1 will be required to account for this phenomenon in land-surface models.

Leaves as bottlenecks: The contribution of tree leaves to hydraulic resistance within the soil-plant-atmosphere continuum.

Within vascular plants, the partitioning of hydraulic resistance along the soil-to-leaf continuum affects transpiration and its response to environmental conditions. In trees, the fractional contribution of leaf hydraulic resistance (Rleaf ) to total soil-to-leaf hydraulic resistance (Rtotal ), or fRleaf (=Rleaf /Rtotal ), is thought to be large, but this has not been tested comprehensively. We compiled a multibiome data set of fRleaf using new and previously published measurements of pressure differences within trees in situ. Across 80 samples, fRleaf averaged 0.51 (95% confidence interval [CI] = 0.46-0.57) and it declined with tree height. We also used the allometric relationship between field-based measurements of soil-to-leaf hydraulic conductance and laboratory-based measurements of leaf hydraulic conductance to compute the average fRleaf for 19 tree samples, which was 0.40 (95% CI = 0.29-0.56). The in situ technique produces a more accurate descriptor of fRleaf because it accounts for dynamic leaf hydraulic conductance. Both approaches demonstrate the outsized role of leaves in controlling tree hydrodynamics. A larger fRleaf may help stems from loss of hydraulic conductance. Thus, the decline in fRleaf with tree height would contribute to greater drought vulnerability in taller trees and potentially to their observed disproportionate drought mortality.

Embolism resistance explains mortality and recovery of five subtropical evergreen broadleaf trees to persistent drought.

Subtropical evergreen broadleaf forests (SEBF) are experiencing and expected to suffer more frequent and severe drought events. However, how the hydraulic traits directly link to the mortality and recovery of SEBF trees remains unclear. In this study, we conducted a drought-rewatering experiment on tree seedlings of five dominant species to investigate how the hydraulic traits were related to tree mortality and the resistance and recovery of photosynthesis (A) and transpiration (E) under different drought severities. Species with greater embolism resistance (P50 ) survived longer than those with a weaker P50 . However, there was no general hydraulic threshold associated with tree mortality, with the lethal hydraulic failure varying from 64% to 93% loss of conductance. The photosynthesis and transpiration of tree species with a greater P50 were more resistant to and recovered faster from drought than those with lower P50 . Other plant traits could not explain the interspecific variation in tree mortality and drought resistance and recovery. These results highlight the unique importance of embolism resistance in driving carbon and water processes under persistent drought across different trees in SEBFs. The absence of multiple efficient drought strategies in SEBF seedlings implies the difficulty of natural seedling regeneration under future droughts, which often occurs after destructive disturbances (e.g., extreme drought events and typhoon), suggesting that this biome may be highly vulnerable to co-occurring climate extremes.

Emerging signals of declining forest resilience under climate change.

Forest ecosystems depend on their capacity to withstand and recover from natural and anthropogenic perturbations (that is, their resilience)1. Experimental evidence of sudden increases in tree mortality is raising concerns about variation in forest resilience2, yet little is known about how it is evolving in response to climate change. Here we integrate satellite-based vegetation indices with machine learning to show how forest resilience, quantified in terms of critical slowing down indicators3-5, has changed during the period 2000-2020. We show that tropical, arid and temperate forests are experiencing a significant decline in resilience, probably related to increased water limitations and climate variability. By contrast, boreal forests show divergent local patterns with an average increasing trend in resilience, probably benefiting from warming and CO2 fertilization, which may outweigh the adverse effects of climate change. These patterns emerge consistently in both managed and intact forests, corroborating the existence of common large-scale climate drivers. Reductions in resilience are statistically linked to abrupt declines in forest primary productivity, occurring in response to slow drifting towards a critical resilience threshold. Approximately 23% of intact undisturbed forests, corresponding to 3.32 Pg C of gross primary productivity, have already reached a critical threshold and are experiencing a further degradation in resilience. Together, these signals reveal a widespread decline in the capacity of forests to withstand perturbation that should be accounted for in the design of land-based mitigation and adaptation plans.

The influence of increasing atmospheric CO2 , temperature, and vapor pressure deficit on seawater-induced tree mortality.

Increasing seawater exposure is killing coastal trees globally, with expectations of accelerating mortality with rising sea levels. However, the impact of concomitant changes in atmospheric CO2 concentration, temperature, and vapor pressure deficit (VPD) on seawater-induced tree mortality is uncertain. We examined the mechanisms of seawater-induced mortality under varying climate scenarios using a photosynthetic gain and hydraulic cost optimization model validated against observations in a mature stand of Sitka spruce (Picea sitchensis) trees in the Pacific Northwest, USA, that were dying from recent seawater exposure. The simulations matched well with observations of photosynthesis, transpiration, nonstructural carbohydrates concentrations, leaf water potential, the percentage loss of xylem conductivity, and stand-level mortality rates. The simulations suggest that seawater-induced mortality could decrease by c. 16.7% with increasing atmospheric CO2 levels due to reduced risk of carbon starvation. Conversely, rising VPD could increase mortality by c. 5.6% because of increasing risk of hydraulic failure. Across all scenarios, seawater-induced mortality was driven by hydraulic failure in the first 2 yr after seawater exposure began, with carbon starvation becoming more important in subsequent years. Changing CO2 and climate appear unlikely to have a significant impact on coastal tree mortality under rising sea levels.

Processes and mechanisms of coastal woody-plant mortality.

Observations of woody plant mortality in coastal ecosystems are globally widespread, but the overarching processes and underlying mechanisms are poorly understood. This knowledge deficiency, combined with rapidly changing water levels, storm surges, atmospheric CO2 , and vapor pressure deficit, creates large predictive uncertainty regarding how coastal ecosystems will respond to global change. Here, we synthesize the literature on the mechanisms that underlie coastal woody-plant mortality, with the goal of producing a testable hypothesis framework. The key emergent mechanisms underlying mortality include hypoxic, osmotic, and ionic-driven reductions in whole-plant hydraulic conductance and photosynthesis that ultimately drive the coupled processes of hydraulic failure and carbon starvation. The relative importance of these processes in driving mortality, their order of progression, and their degree of coupling depends on the characteristics of the anomalous water exposure, on topographic effects, and on taxa-specific variation in traits and trait acclimation. Greater inundation exposure could accelerate mortality globally; however, the interaction of changing inundation exposure with elevated CO2 , drought, and rising vapor pressure deficit could influence mortality likelihood. Models of coastal forests that incorporate the frequency and duration of inundation, the role of climatic drivers, and the processes of hydraulic failure and carbon starvation can yield improved estimates of inundation-induced woody-plant mortality.

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.

Reduced ecosystem resilience quantifies fine-scale heterogeneity in tropical forest mortality responses to drought.

Sensitivity of forest mortality to drought in carbon-dense tropical forests remains fraught with uncertainty, while extreme droughts are predicted to be more frequent and intense. Here, the potential of temporal autocorrelation of high-frequency variability in Landsat Enhanced Vegetation Index (EVI), an indicator of ecosystem resilience, to predict spatial and temporal variations of forest biomass mortality is evaluated against in situ census observations for 64 site-year combinations in Costa Rican tropical dry forests during the 2015 ENSO drought. Temporal autocorrelation, within the optimal moving window of 24 months, demonstrated robust predictive power for in situ mortality (leave-one-out cross-validation R2  = 0.54), which allows for estimates of annual biomass mortality patterns at 30 m resolution. Subsequent spatial analysis showed substantial fine-scale heterogeneity of forest mortality patterns, largely driven by drought intensity and ecosystem properties related to plant water use such as forest deciduousness and topography. Highly deciduous forest patches demonstrated much lower mortality sensitivity to drought stress than less deciduous forest patches after elevation was controlled. Our results highlight the potential of high-resolution remote sensing to "fingerprint" forest mortality and the significant role of ecosystem heterogeneity in forest biomass resistance to drought.

Hotter droughts alter resource allocation to chemical defenses in piñon pine.

Heat and drought affect plant chemical defenses and thereby plant susceptibility to pests and pathogens. Monoterpenes are of particular importance for conifers as they play critical roles in defense against bark beetles. To date, work seeking to understand the impacts of heat and drought on monoterpenes has primarily focused on young potted seedlings, leaving it unclear how older age classes that are more vulnerable to bark beetles might respond to stress. Furthermore, we lack a clear picture of what carbon resources might be prioritized to support monoterpene synthesis under drought stress. To address this, we measured needle and woody tissue monoterpene concentrations and physiological variables simultaneously from mature piñon pines (Pinus edulis) from a unique temperature and drought manipulation field experiment. While heat had no effect on total monoterpene concentrations, trees under combined heat and drought stress exhibited ~ 85% and 35% increases in needle and woody tissue, respectively, over multiple years. Plant physiological variables like maximum photosynthesis each explained less than 10% of the variation in total monoterpenes for both tissue types while starch and glucose + fructose measured 1-month prior explained ~ 45% and 60% of the variation in woody tissue total monoterpene concentrations. Although total monoterpenes increased under combined stress, some key monoterpenes with known roles in bark beetle ecology decreased. These shifts may make trees more favorable for bark beetle attack rather than well defended, which one might conclude if only considering total monoterpene concentrations. Our results point to cumulative and synergistic effects of heat and drought that may reprioritize carbon allocation of specific non-structural carbohydrates toward defense.