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.

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.

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.

Future climate doubles the risk of hydraulic failure in a wet tropical forest.

Future climate presents conflicting implications for forest biomass. We evaluate how plant hydraulic traits, elevated CO2 levels, warming, and changes in precipitation affect forest primary productivity, evapotranspiration, and the risk of hydraulic failure. We used a dynamic vegetation model with plant hydrodynamics (FATES-HYDRO) to simulate the stand-level responses to future climate changes in a wet tropical forest in Barro Colorado Island, Panama. We calibrated the model by selecting plant trait assemblages that performed well against observations. These assemblages were run with temperature and precipitation changes for two greenhouse gas emission scenarios (2086-2100: SSP2-45, SSP5-85) and two CO2 levels (contemporary, anticipated). The risk of hydraulic failure is projected to increase from a contemporary rate of 5.7% to 10.1-11.3% under future climate scenarios, and, crucially, elevated CO2 provided only slight amelioration. By contrast, elevated CO2 mitigated GPP reductions. We attribute a greater variation in hydraulic failure risk to trait assemblages than to either CO2 or climate. Our results project forests with both faster growth (through productivity increases) and higher mortality rates (through increasing rates of hydraulic failure) in the neo-tropics accompanied by certain trait plant assemblages becoming nonviable.

Local carbon reserves are insufficient for phloem terpene induction during drought in Pinus edulis in response to bark beetle-associated fungi.

Stomatal closure during drought inhibits carbon uptake and may reduce a tree's defensive capacity. Limited carbon availability during drought may increase a tree's mortality risk, particularly if drought constrains trees' capacity to rapidly produce defenses during biotic attack. We parameterized a new model of conifer defense using physiological data on carbon reserves and chemical defenses before and after a simulated bark beetle attack in mature Pinus edulis under experimental drought. Attack was simulated using inoculations with a consistent bluestain fungus (Ophiostoma sp.) of Ips confusus, the main bark beetle colonizing this tree, to induce a defensive response. Trees with more carbon reserves produced more defenses but measured phloem carbon reserves only accounted for c. 23% of the induced defensive response. Our model predicted universal mortality if local reserves alone supported defense production, suggesting substantial remobilization and transport of stored resin or carbon reserves to the inoculation site. Our results show that de novo terpene synthesis represents only a fraction of the total measured phloem terpenes in P. edulis following fungal inoculation. Without direct attribution of phloem terpene concentrations to available carbon, many studies may be overestimating the scale and importance of de novo terpene synthesis in a tree's induced defense response.

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.

Short-Term Groundwater Level Fluctuations Drive Subsurface Redox Variability.

As global change processes modify the extent and functions of terrestrial-aquatic interfaces, the variability of critical and dynamic transitional zones between wetlands and uplands increases. However, it is still unclear how fluctuating water levels at these dynamic boundaries alter groundwater biogeochemical cycling. Here, we used high-temporal resolution data along gradients from wetlands to uplands and during fluctuating water levels at freshwater coastal areas to capture spatiotemporal patterns of groundwater redox potential (Eh). We observed that topography influences groundwater Eh that is higher in uplands than in wetlands; however, the high variability within TAI zones challenged the establishment of distinct redox zonation. Declining water levels generally decreased Eh, but most locations exhibited significant Eh variability, which is associated with rare instances of short-term water level fluctuations, introducing oxygen. The Eh-oxygen relationship showed distinct hysteresis patterns, reflecting redox poising capacity at higher Eh, maintaining more oxidizing states longer than the dissolved oxygen presence. Surprisingly, we observed more frequent oxidizing states in transitional areas and wetlands than in uplands. We infer that occasional oxygen entering specific wetland-upland boundaries acts as critical biogeochemical control points. High-resolution data can capture such rare yet significant biogeochemical instances, supporting redox-informed models and advancing the predictability of climate change feedback.

Storage of carbon reserves in spruce trees is prioritized over growth in the face of carbon limitation.

Climate change is expected to pose a global threat to forest health by intensifying extreme events like drought and insect attacks. Carbon allocation is a fundamental process that determines the adaptive responses of long-lived late-maturing organisms like trees to such stresses. However, our mechanistic understanding of how trees coordinate and set allocation priorities among different sinks (e.g., growth and storage) under severe source limitation remains limited. Using flux measurements, isotopic tracing, targeted metabolomics, and transcriptomics, we investigated how limitation of source supply influences sink activity, particularly growth and carbon storage, and their relative regulation in Norway spruce (Picea abies) clones. During photosynthetic deprivation, absolute rates of respiration, growth, and allocation to storage all decline. When trees approach neutral carbon balance, i.e., daytime net carbon gain equals nighttime carbon loss, genes encoding major enzymes of metabolic pathways remain relatively unaffected. However, under negative carbon balance, photosynthesis and growth are down-regulated while sucrose and starch biosynthesis pathways are up-regulated, indicating that trees prioritize carbon allocation to storage over growth. Moreover, trees under negative carbon balance actively increase the turnover rate of starch, lipids, and amino acids, most likely to support respiration and mitigate stress. Our study provides molecular evidence that trees faced with severe photosynthetic limitation strategically regulate storage allocation and consumption at the expense of growth. Understanding such allocation strategies is crucial for predicting how trees may respond to extreme events involving steep declines in photosynthesis, like severe drought, or defoliation by heat waves, late frost, or insect attack.

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.

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.

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.

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.

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.

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.

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.

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.

Declining carbohydrate content of Sitka-spruce treesdying from seawater exposure.

Increasing sea levels associated with climate change threaten the survival of coastal forests, yet the mechanisms by which seawater exposure causes tree death remain poorly understood. Despite the potentially crucial role of nonstructural carbohydrate (NSC) reserves in tree survival, their dynamics in the process of death under seawater exposure are unknown. Here we monitored progressive tree mortality and associated NSC storage in Sitka-spruce (Picea sitchensis) trees dying under ecosystem-scale increases in seawater exposure in western Washington, USA. All trees exposed to seawater, because of monthly tidal intrusion, experienced declining crown foliage during the sampling period, and individuals with a lower percentage of live foliated crown (PLFC) died faster. Tree PLFC was strongly correlated with subsurface salinity and needle ion contents. Total NSC concentrations in trees declined remarkably with crown decline, and reached extremely low levels at tree death (2.4% and 1.6% in leaves and branches, respectively, and 0.4% in stems and roots). Starch in all tissues was almost completely consumed, while sugars remained at a homeostatic level in foliage. The decreasing NSC with closer proximity to death and near zero starch at death are evidences that carbon starvation occurred during Sitka-spruce mortality during seawater exposure. Our results highlight the importance of carbon storage as an indicator of tree mortality risks under seawater exposure.

Seawater exposure causes hydraulic damage in dying Sitka-spruce trees.

Sea-level rise is one of the most critical challenges facing coastal ecosystems under climate change. Observations of elevated tree mortality in global coastal forests are increasing, but important knowledge gaps persist concerning the mechanism of salinity stress-induced nonhalophytic tree mortality. We monitored progressive mortality and associated gas exchange and hydraulic shifts in Sitka-spruce (Picea sitchensis) trees located within a salinity gradient under an ecosystem-scale change of seawater exposure in Washington State, USA. Percentage of live foliated crown (PLFC) decreased and tree mortality increased with increasing soil salinity during the study period. A strong reduction in gas exchange and xylem hydraulic conductivity (Ks) occurred during tree death, with an increase in the percentage loss of conductivity (PLC) and turgor loss point (πtlp). Hydraulic and osmotic shifts reflected that hydraulic function declined from seawater exposure, and dying trees were unable to support osmotic adjustment. Constrained gas exchange was strongly related to hydraulic damage at both stem and leaf levels. Significant correlations between foliar sodium (Na+) concentration and gas exchange and key hydraulic parameters (Ks, PLC, and πtlp) suggest that cellular injury related to the toxic effects of ion accumulation impacted the physiology of these dying trees. This study provides evidence of toxic effects on the cellular function that manifests in all aspects of plant functioning, leading to unfavourable osmotic and hydraulic conditions.

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.

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.