Critical transitions in the Amazon forest system.

The possibility that the Amazon forest system could soon reach a tipping point, inducing large-scale collapse, has raised global concern1-3. For 65 million years, Amazonian forests remained relatively resilient to climatic variability. Now, the region is increasingly exposed to unprecedented stress from warming temperatures, extreme droughts, deforestation and fires, even in central and remote parts of the system1. Long existing feedbacks between the forest and environmental conditions are being replaced by novel feedbacks that modify ecosystem resilience, increasing the risk of critical transition. Here we analyse existing evidence for five major drivers of water stress on Amazonian forests, as well as potential critical thresholds of those drivers that, if crossed, could trigger local, regional or even biome-wide forest collapse. By combining spatial information on various disturbances, we estimate that by 2050, 10% to 47% of Amazonian forests will be exposed to compounding disturbances that may trigger unexpected ecosystem transitions and potentially exacerbate regional climate change. Using examples of disturbed forests across the Amazon, we identify the three most plausible ecosystem trajectories, involving different feedbacks and environmental conditions. We discuss how the inherent complexity of the Amazon adds uncertainty about future dynamics, but also reveals opportunities for action. Keeping the Amazon forest resilient in the Anthropocene will depend on a combination of local efforts to end deforestation and degradation and to expand restoration, with global efforts to stop greenhouse gas emissions.

Basin-wide variation in tree hydraulic safety margins predicts the carbon balance of Amazon forests.

Tropical forests face increasing climate risk1,2, yet our ability to predict their response to climate change is limited by poor understanding of their resistance to water stress. Although xylem embolism resistance thresholds (for example, [Formula: see text]50) and hydraulic safety margins (for example, HSM50) are important predictors of drought-induced mortality risk3-5, little is known about how these vary across Earth's largest tropical forest. Here, we present a pan-Amazon, fully standardized hydraulic traits dataset and use it to assess regional variation in drought sensitivity and hydraulic trait ability to predict species distributions and long-term forest biomass accumulation. Parameters [Formula: see text]50 and HSM50 vary markedly across the Amazon and are related to average long-term rainfall characteristics. Both [Formula: see text]50 and HSM50 influence the biogeographical distribution of Amazon tree species. However, HSM50 was the only significant predictor of observed decadal-scale changes in forest biomass. Old-growth forests with wide HSM50 are gaining more biomass than are low HSM50 forests. We propose that this may be associated with a growth-mortality trade-off whereby trees in forests consisting of fast-growing species take greater hydraulic risks and face greater mortality risk. Moreover, in regions of more pronounced climatic change, we find evidence that forests are losing biomass, suggesting that species in these regions may be operating beyond their hydraulic limits. Continued climate change is likely to further reduce HSM50 in the Amazon6,7, with strong implications for the Amazon carbon sink.

Double stress of waterlogging and drought drives forest-savanna coexistence.

Forest-savanna boundaries are ecotones that support complex ecosystem functions and are sensitive to biotic/abiotic perturbations. What drives their distribution today and how it may shift in the future are open questions. Feedbacks among climate, fire, herbivory, and land use are known drivers. Here, we show that alternating seasonal drought and waterlogging stress favors the dominance of savanna-like ecosystems over forests. We track the seasonal water-table depth as an indicator of water stress when too deep and oxygen stress when too shallow and map forest/savanna occurrence within this double-stress space in the neotropics. We find that under a given annual precipitation, savannas are favored in landscape positions experiencing double stress, which is more common as the dry season strengthens (climate driver) but only found in waterlogged lowlands (terrain driver). We further show that hydrological changes at the end of the century may expose some flooded forests to savanna expansion, affecting biodiversity and soil carbon storage. Our results highlight the importance of land hydrology in understanding/predicting forest-savanna transitions in a changing world.

Functional recovery of secondary tropical forests.

One-third of all Neotropical forests are secondary forests that regrow naturally after agricultural use through secondary succession. We need to understand better how and why succession varies across environmental gradients and broad geographic scales. Here, we analyze functional recovery using community data on seven plant characteristics (traits) of 1,016 forest plots from 30 chronosequence sites across the Neotropics. By analyzing communities in terms of their traits, we enhance understanding of the mechanisms of succession, assess ecosystem recovery, and use these insights to propose successful forest restoration strategies. Wet and dry forests diverged markedly for several traits that increase growth rate in wet forests but come at the expense of reduced drought tolerance, delay, or avoidance, which is important in seasonally dry forests. Dry and wet forests showed different successional pathways for several traits. In dry forests, species turnover is driven by drought tolerance traits that are important early in succession and in wet forests by shade tolerance traits that are important later in succession. In both forests, deciduous and compound-leaved trees decreased with forest age, probably because microclimatic conditions became less hot and dry. Our results suggest that climatic water availability drives functional recovery by influencing the start and trajectory of succession, resulting in a convergence of community trait values with forest age when vegetation cover builds up. Within plots, the range in functional trait values increased with age. Based on the observed successional trait changes, we indicate the consequences for carbon and nutrient cycling and propose an ecologically sound strategy to improve forest restoration success.

Vapour pressure deficit modulates hydraulic function and structure of tropical rainforests under nonlimiting soil water supply.

Atmospheric conditions are expected to become warmer and drier in the future, but little is known about how evaporative demand influences forest structure and function independently from soil moisture availability, and how fast-response variables (such as canopy water potential and stomatal conductance) may mediate longer-term changes in forest structure and function in response to climate change. We used two tropical rainforest sites with different temperatures and vapour pressure deficits (VPD), but nonlimiting soil water supply, to assess the impact of evaporative demand on ecophysiological function and forest structure. Common species between sites allowed us to test the extent to which species composition, relative abundance and intraspecific variability contributed to site-level differences. The highest VPD site had lower midday canopy water potentials, canopy conductance (gc ), annual transpiration, forest stature, and biomass, while the transpiration rate was less sensitive to changes in VPD; it also had different height-diameter allometry (accounting for 51% of the difference in biomass between sites) and higher plot-level wood density. Our findings suggest that increases in VPD, even in the absence of soil water limitation, influence fast-response variables, such as canopy water potentials and gc , potentially leading to longer-term changes in forest stature resulting in reductions in biomass.

Microbial drivers of plant richness and productivity in a grassland restoration experiment along a gradient of land-use intensity.

Plant-soil feedbacks (PSFs) underlying grassland plant richness and productivity are typically coupled with nutrient availability; however, we lack understanding of how restoration measures to increase plant diversity might affect PSFs. We examined the roles of sward disturbance, seed addition and land-use intensity (LUI) on PSFs. We conducted a disturbance and seed addition experiment in 10 grasslands along a LUI gradient and characterized plant biomass and richness, soil microbial biomass, community composition and enzyme activities. Greater plant biomass at high LUI was related to a decrease in the fungal to bacterial ratios, indicating highly productive grasslands to be dominated by bacteria. Lower enzyme activity per microbial biomass at high plant species richness indicated a slower carbon (C) cycling. The relative abundance of fungal saprotrophs decreased, while pathogens increased with LUI and disturbance. Both fungal guilds were negatively associated with plant richness, indicating the mechanisms underlying PSFs depended on LUI. We show that LUI and disturbance affect fungal functional composition, which may feedback on plant species richness by impeding the establishment of pathogen-sensitive species. Therefore, we highlight the need to integrate LUI including its effects on PSFs when planning for practices that aim to optimize plant diversity and productivity.

Local hydrological gradients structure high intraspecific variability in plant hydraulic traits in two dominant central Amazonian tree species.

Addressing the intraspecific variability of functional traits helps understand how climate change might influence the distribution of organismal traits across environments, but this is notably understudied in the Amazon, especially for plant hydraulic traits commonly used to project drought responses. We quantified the intraspecific trait variability of leaf mass per area, wood density, and xylem embolism resistance for two dominant central Amazonian tree species, along gradients of water and light availability, while accounting for tree age and height. Intraspecific variability in hydraulic traits was high, with within-species variability comparable to the whole-community variation. Hydraulic trait variation was modulated mostly by the hydrological environment, with higher embolism resistance of trees growing on deep-water-table plateaus compared with shallow-water-table valleys. Intraspecific variability of leaf mass per area and wood density was mostly modulated by intrinsic factors and light. The different environmental and intrinsic drivers of variation among and within individuals lead to an uncoupled coordination among carbon acquisition/conservation and water-use traits. Our findings suggest multivariate ecological strategies driving tropical tree distributions even within species, and reflect differential within-population sensitivities along environmental gradients. Therefore, intraspecific trait variability must be considered for accurate predictions of the responses of tropical forests to climate change.

Small and slow is safe: On the drought tolerance of tropical tree species.

Understanding how evolutionary history and the coordination between trait trade-off axes shape the drought tolerance of trees is crucial to predict forest dynamics under climate change. Here, we compiled traits related to drought tolerance and the fast-slow and stature-recruitment trade-off axes in 601 tropical woody species to explore their covariations and phylogenetic signals. We found that xylem resistance to embolism (P50) determines the risk of hydraulic failure, while the functional significance of leaf turgor loss point (TLP) relies on its coordination with water use strategies. P50 and TLP exhibit weak phylogenetic signals and substantial variation within genera. TLP is closely associated with the fast-slow trait axis: slow species maintain leaf functioning under higher water stress. P50 is associated with both the fast-slow and stature-recruitment trait axes: slow and small species exhibit more resistant xylem. Lower leaf phosphorus concentration is associated with more resistant xylem, which suggests a (nutrient and drought) stress-tolerance syndrome in the tropics. Overall, our results imply that (1) drought tolerance is under strong selective pressure in tropical forests, and TLP and P50 result from the repeated evolutionary adaptation of closely related taxa, and (2) drought tolerance is coordinated with the ecological strategies governing tropical forest demography. These findings provide a physiological basis to interpret the drought-induced shift toward slow-growing, smaller, denser-wooded trees observed in the tropics, with implications for forest restoration programmes.

Local drivers of heterogeneity in a tropical forest: epiphytic tank bromeliads affect the availability of soil resources and conditions and indirectly affect the structure of seedling communities.

Environmental heterogeneity is a key component in explaining the megadiversity of tropical forests. Despite its importance, knowledge about local drivers of environmental heterogeneity remains a challenge for ecologists. In Neotropical forests, epiphytic tank bromeliads store large amounts of water and nutrients in the tree canopy, and their tank overflow may create nutrient-rich patches in the soil. However, the effects of this nutrient flux on environmental heterogeneity and plant community structure in the understory remain unexplored. In a Brazilian coastal sandy forest, we investigated the effects of the presence of epiphytic tank bromeliads on throughfall chemistry, soil chemistry, soil litter biomass, light, and seedling community structure. In the presence of epiphytic tank bromeliads, the throughfall nitrogen concentration increased twofold, the throughfall phosphorus concentration increased threefold, and the soil patches had a 3.96% higher pH, a 50% higher calcium concentration, and 11.88% less light. By altering the availability of soil resources and conditions, the presence of bromeliads partially shifted the available niche spaces for plant species and indirectly affected the structure of the seedling communities, decreasing their diversity, density, and biomass. For the first time, we showed that the presence of tank bromeliads in the canopy can create characteristic soil patches in the understory, affecting the structure of seedling communities via fertilization. Our results reveal a novel local driver of environmental heterogeneity, reinforcing and expanding the key role of tank bromeliads both in nutrient cycling and plant community structuring of Neotropical coastal sandy forests.

Hydraulic prediction of drought-induced plant dieback and top-kill depends on leaf habit and growth form.

Hydraulic failure caused by severe drought contributes to aboveground dieback and whole-plant death. The extent to which dieback or whole-plant death can be predicted by plant hydraulic traits has rarely been tested among species with different leaf habits and/or growth forms. We investigated 19 hydraulic traits in 40 woody species in a tropical savanna and their potential correlations with drought response during an extreme drought event during the El Niño-Southern Oscillation in 2015. Plant hydraulic trait variation was partitioned substantially by leaf habit but not growth form along a trade-off axis between traits that support drought tolerance versus avoidance. Semi-deciduous species and shrubs had the highest branch dieback and top-kill (complete aboveground death) among the leaf habits or growth forms. Dieback and top-kill were well explained by combining hydraulic traits with leaf habit and growth form, suggesting integrating life history traits with hydraulic traits will yield better predictions.

Linking plant hydraulics and the fast-slow continuum to understand resilience to drought in tropical ecosystems.

Tropical ecosystems have the highest levels of biodiversity, cycle more water and absorb more carbon than any other terrestrial ecosystem on Earth. Consequently, these ecosystems are extremely important components of Earth's climatic system and biogeochemical cycles. Plant hydraulics is an essential discipline to understand and predict the dynamics of tropical vegetation in scenarios of changing water availability. Using published plant hydraulic data we show that the trade-off between drought avoidance (expressed as deep-rooting, deciduousness and capacitance) and hydraulic safety (P50 - the water potential when plants lose 50% of their maximum hydraulic conductivity) is a major axis of physiological variation across tropical ecosystems. We also propose a novel and independent axis of hydraulic trait variation linking vulnerability to hydraulic failure (expressed as the hydraulic safety margin (HSM)) and growth, where inherent fast-growing plants have lower HSM compared to slow-growing plants. We surmise that soil nutrients are fundamental drivers of tropical community assembly determining the distribution and abundance of the slow-safe/fast-risky strategies. We conclude showing that including either the growth-HSM or the resistance-avoidance trade-off in models can make simulated tropical rainforest communities substantially more vulnerable to drought than similar communities without the trade-off. These results suggest that vegetation models need to represent hydraulic trade-off axes to accurately project the functioning and distribution of tropical ecosystems.

Harvesting water from unsaturated atmospheres: deliquescence of salt secreted onto leaf surfaces drives reverse sap flow in a dominant arid climate mangrove, Avicennia marina.

The mangrove Avicennia marina adjusts internal salt concentrations by foliar salt secretion. Deliquescence of accumulated salt causes leaf wetting that may provide a water source for salt-secreting plants in arid coastal wetlands where high nocturnal humidity can usually support deliquescence whereas rainfall events are rare. We tested the hypotheses that salt deliquescence on leaf surfaces can drive top-down rehydration, and that such absorption of moisture from unsaturated atmospheres makes a functional contribution to dry season shoot water balances. Sap flow and water relations were monitored to assess the uptake of atmospheric water by branches during shoot wetting events under natural and manipulated microclimatic conditions. Reverse sap flow rates increased with increasing relative humidity from 70% to 89%, consistent with function of salt deliquescence in harvesting moisture from unsaturated atmospheres. Top-down rehydration elevated branch water potentials above those possible from root water uptake, subsidising transpiration rates and reducing branch vulnerability to hydraulic failure in the subsequent photoperiod. Absorption of atmospheric moisture harvested through deliquescence of salt on leaf surfaces enhances water balances of Avicennia marina growing in hypersaline wetlands under arid climatic conditions. Top-down rehydration from these frequent, low intensity wetting events contributes to prevention of carbon starvation and hydraulic failure during drought.

Towards the flower economics spectrum.

Understanding how floral traits affect reproduction is key for understanding genetic diversity, speciation, and trait evolution in the face of global changes and pollinator decline. However, there has not yet been a unified framework to characterize the major trade-offs and axes of floral trait variation. Here, we propose the development of a floral economics spectrum (FES) that incorporates the multiple pathways by which floral traits can be shaped by multiple agents of selection acting on multiple flower functions. For example, while pollinator-mediated selection has been considered the primary factor affecting flower evolution, selection by nonpollinator agents can reinforce or oppose pollinator selection, and, therefore, affect floral trait variation. In addition to pollinators, the FES should consider nonpollinator biotic agents and floral physiological costs, broadening the drivers of floral traits beyond pollinators. We discuss how coordinated evolution and trade-offs among floral traits and between floral and vegetative traits may influence the distribution of floral traits across biomes and lineages, thereby influencing organismal evolution and community assembly.

Plant traits controlling growth change in response to a drier climate.

Plant traits are increasingly being used to improve prediction of plant function, including plant demography. However, the capability of plant traits to predict demographic rates remains uncertain, particularly in the context of trees experiencing a changing climate. Here we present data combining 17 plant traits associated with plant structure, metabolism and hydraulic status, with measurements of long-term mean, maximum and relative growth rates for 176 trees from the world's longest running tropical forest drought experiment. We demonstrate that plant traits can predict mean annual tree growth rates with moderate explanatory power. However, only combinations of traits associated more directly with plant functional processes, rather than more commonly employed traits like wood density or leaf mass per area, yield the power to predict growth. Critically, we observe a shift from growth being controlled by traits related to carbon cycling (assimilation and respiration) in well-watered trees, to traits relating to plant hydraulic stress in drought-stressed trees. We also demonstrate that even with a very comprehensive set of plant traits and growth data on large numbers of tropical trees, considerable uncertainty remains in directly interpreting the mechanisms through which traits influence performance in tropical forests.

Root positioning and trait shifts in Hibbertia racemosa as dependent on its neighbour's nutrient-acquisition strategy.

Nutrient-poor ecosystems globally exhibit high plant diversity. One mechanism enabling the co-existence of species in such ecosystems is facilitation among plants with contrasting nutrient-acquisition strategies. The ecophysiological processes underlying these interactions remain poorly understood. We hypothesized that root positioning plays a role between sympatric species in nutrient-poor vegetation. We investigated how the growth traits of the focal mycorrhizal non-cluster-rooted Hibbertia racemosa change when grown in proximity of non-mycorrhizal Banksia attenuata, which produces cluster roots that increase nutrient availability, compared with growth with conspecifics. Focal plants were placed in the centre of rhizoboxes, and biomass allocation, root system architecture, specific root length (SRL), and leaf nutrient concentration were assessed. When grown with B. attenuata, focal plants decreased root investment, increased root growth towards B. attenuata, and positioned their roots near B. attenuata cluster roots. SRL was greater, and the degree of localized root investment correlated positively with B. attenuata cluster-root biomass. Total nutrient contents in the focal individuals were greater when grown with B. attenuata. Focal plants directed their root growth towards the putatively facilitating neighbour's cluster roots, modifying root traits and investment. Preferential root positioning and root morphological traits play important roles in positive plant-plant interactions.

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.

Stomatal optimization based on xylem hydraulics (SOX) improves land surface model simulation of vegetation responses to climate.

Land surface models (LSMs) typically use empirical functions to represent vegetation responses to soil drought. These functions largely neglect recent advances in plant ecophysiology that link xylem hydraulic functioning with stomatal responses to climate. We developed an analytical stomatal optimization model based on xylem hydraulics (SOX) to predict plant responses to drought. Coupling SOX to the Joint UK Land Environment Simulator (JULES) LSM, we conducted a global evaluation of SOX against leaf- and ecosystem-level observations. SOX simulates leaf stomatal conductance responses to climate for woody plants more accurately and parsimoniously than the existing JULES stomatal conductance model. An ecosystem-level evaluation at 70 eddy flux sites shows that SOX decreases the sensitivity of gross primary productivity (GPP) to soil moisture, which improves the model agreement with observations and increases the predicted annual GPP by 30% in relation to JULES. SOX decreases JULES root-mean-square error in GPP by up to 45% in evergreen tropical forests, and can simulate realistic patterns of canopy water potential and soil water dynamics at the studied sites. SOX provides a parsimonious way to incorporate recent advances in plant hydraulics and optimality theory into LSMs, and an alternative to empirical stress factors.

The Pneumatron: An automated pneumatic apparatus for estimating xylem vulnerability to embolism at high temporal resolution.

Xylem vulnerability to embolism represents an important trait to determine species distribution patterns and drought resistance. However, estimating embolism resistance frequently requires time-consuming and ambiguous hydraulic lab measurements. Based on a recently developed pneumatic method, we present and test the "Pneumatron", a device that generates high time-resolution and fully automated vulnerability curves. Embolism resistance is estimated by applying a partial vacuum to extract air from an excised xylem sample, while monitoring the pressure change over time. Although the amount of gas extracted is strongly correlated with the percentage loss of xylem conductivity, validation of the Pneumatron was performed by comparison with the optical method for Eucalyptus camaldulensis leaves. The Pneumatron improved the precision of the pneumatic method considerably, facilitating the detection of small differences in the (percentage of air discharged [PAD] < 0.47%). Hence, the Pneumatron can directly measure the 50% PAD without any fitting of vulnerability curves. PAD and embolism frequency based on the optical method were strongly correlated (r2 = 0.93) for E. camaldulensis. By providing an open source platform, the Pneumatron represents an easy, low-cost, and powerful tool for field measurements, which can significantly improve our understanding of plant-water relations and the mechanisms behind embolism.

Amazonia trees have limited capacity to acclimate plant hydraulic properties in response to long-term drought.

The fate of tropical forests under future climate change is dependent on the capacity of their trees to adjust to drier conditions. The capacity of trees to withstand drought is likely to be determined by traits associated with their hydraulic systems. However, data on whether tropical trees can adjust hydraulic traits when experiencing drought remain rare. We measured plant hydraulic traits (e.g. hydraulic conductivity and embolism resistance) and plant hydraulic system status (e.g. leaf water potential, native embolism and safety margin) on >150 trees from 12 genera (36 species) and spanning a stem size range from 14 to 68 cm diameter at breast height at the world's only long-running tropical forest drought experiment. Hydraulic traits showed no adjustment following 15 years of experimentally imposed moisture deficit. This failure to adjust resulted in these drought-stressed trees experiencing significantly lower leaf water potentials, and higher, but variable, levels of native embolism in the branches. This result suggests that hydraulic damage caused by elevated levels of embolism is likely to be one of the key drivers of drought-induced mortality following long-term soil moisture deficit. We demonstrate that some hydraulic traits changed with tree size, however, the direction and magnitude of the change was controlled by taxonomic identity. Our results suggest that Amazonian trees, both small and large, have limited capacity to acclimate their hydraulic systems to future droughts, potentially making them more at risk of drought-induced mortality.

Drought response strategies of deciduous and evergreen woody species in a seasonally dry neotropical forest.

Deciduous and evergreen trees are usually considered the main coexisting functional groups in seasonally dry tropical forests (SDTF). We compared leaf and stem traits of 22 woody species in the Brazilian Caatinga to investigate whether deciduous (DC) and evergreen (EV) species have divergent water-use strategies. Our hypothesis was that DC trees compensate for their short leaf longevity by being less conservative in water use and showing higher variation in the seasonal water potential after leaf shedding. Evergreen species should exhibit a highly conservative water use strategy, which reduces variations in seasonal water potential and the negative effects of desiccation. Our leaf dynamics results indicate that the crown area of DC trees is more sensitive to air and soil drought, whereas EV trees are only sensitive to soil drought. Deciduous species exhibit differences in a set of leaf traits confirming their acquisitive strategy, which contrasts with evergreen species. However, when stomatal traits are considered, we found that DC and EV have similar stomatal regulation strategies (partially isohydric). We also found divergent physiological strategies within DC. For high wood density DC, the xylem water potential (Ψxylem) continued to drop during the dry season. We also found a negative linear relationship between leaf life span (LL) and the transpiration rate per unit of hydraulic conductivity (Λ), indicating that species with high LL are less vulnerable to hydraulic conductivity loss than early-deciduous species. Collectively, our results indicate divergence in the physiology of deciduous species, which suggests that categorizing species based solely on their leaf phenology may be an oversimplification.