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.

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

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

High exposure of global tree diversity to human pressure.

Safeguarding Earth's tree diversity is a conservation priority due to the importance of trees for biodiversity and ecosystem functions and services such as carbon sequestration. Here, we improve the foundation for effective conservation of global tree diversity by analyzing a recently developed database of tree species covering 46,752 species. We quantify range protection and anthropogenic pressures for each species and develop conservation priorities across taxonomic, phylogenetic, and functional diversity dimensions. We also assess the effectiveness of several influential proposed conservation prioritization frameworks to protect the top 17% and top 50% of tree priority areas. We find that an average of 50.2% of a tree species' range occurs in 110-km grid cells without any protected areas (PAs), with 6,377 small-range tree species fully unprotected, and that 83% of tree species experience nonnegligible human pressure across their range on average. Protecting high-priority areas for the top 17% and 50% priority thresholds would increase the average protected proportion of each tree species' range to 65.5% and 82.6%, respectively, leaving many fewer species (2,151 and 2,010) completely unprotected. The priority areas identified for trees match well to the Global 200 Ecoregions framework, revealing that priority areas for trees would in large part also optimize protection for terrestrial biodiversity overall. Based on range estimates for >46,000 tree species, our findings show that a large proportion of tree species receive limited protection by current PAs and are under substantial human pressure. Improved protection of biodiversity overall would also strongly benefit global tree diversity.

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.

Plant hydraulics at the heart of plant, crops and ecosystem functions in the face of climate change.

Plant hydraulics is crucial for assessing the plants' capacity to extract and transport water from the soil up to their aerial organs. Along with their capacity to exchange water between plant compartments and regulate evaporation, hydraulic properties determine plant water relations, water status and susceptibility to pathogen attacks. Consequently, any variation in the hydraulic characteristics of plants is likely to significantly impact various mechanisms and processes related to plant growth, survival and production, as well as the risk of biotic attacks and forest fire behaviour. However, the integration of hydraulic traits into disciplines such as plant pathology, entomology, fire ecology or agriculture can be significantly improved. This review examines how plant hydraulics can provide new insights into our understanding of these processes, including modelling processes of vegetation dynamics, illuminating numerous perspectives for assessing the consequences of climate change on forest and agronomic systems, and addressing unanswered questions across multiple areas of knowledge.

Plasticity in branch water relations and stem hydraulic vulnerability enhances hydraulic safety in mangroves growing along a salinity gradient.

Coping with water stress depends on maintaining cellular function and hydraulic conductance. Yet measurements of vulnerability to drought and salinity do not often focus on capacitance in branch organs that buffer hydraulic function during water stress. The relationships between branch water relations, stem hydraulic vulnerability and stem anatomy were investigated in two co-occurring mangroves Aegiceras corniculatum and Rhizophora stylosa growing at low and high salinity. The dynamics of branch water release acted to conserve water content in the stem at the expense of the foliage during extended drying. Hydraulic redistribution from the foliage to the stem increased stem relative water content by up to 21%. The water potentials at which 12% and 50% loss of stem hydraulic conductivity occurred decreased by ~1.7 MPa in both species between low and high salinity sites. These coordinated tissue adjustments increased hydraulic safety despite declining turgor safety margins at higher salinity sites. Our results highlight the complex interplay of plasticity in organ-level water relations with hydraulic vulnerability in the maintenance of stem hydraulic function in mangroves distributed along salinity gradients. These results emphasise the importance of combining water relations and hydraulic vulnerability parameters to understand vulnerability to water stress across the whole plant.

Xylem and Phloem in Petioles Are Coordinated With Leaf Gas Exchange in Oaks With Contrasting Anatomical Strategies Depending on Leaf Habit.

As the single link between leaves and the rest of the plant, petioles must develop conductive tissues according to the water influx and sugar outflow of the leaf lamina. A scaling relationship between leaf area and anatomical traits of xylem and phloem is expected to improve the efficiency of these tissues. However, the different constraints compromising the functionality of both tissues (e.g., risk of cavitation) must not be disregarded. Additionally, deciduous and evergreen plants may have different strategies to produce and package their petiole conduits to cope with environmental restrictions. We explored in 33 oak species the relationships between petiole anatomical traits, leaf area, stomatal conductance, and photosynthesis rate. Results showed allometric scaling between anatomical structure of xylem and phloem with leaf area. We also found correlations between photosynthesis rate, stomatal conductance, and anatomical traits in the petiole. The main novelty is how oaks present a different strategy depending on the leaf habit. Deciduous species tend to increase their diameters to achieve greater leaf-specific conductivity. By contrast, evergreen oaks develop larger xylem conductive areas for a given leaf area than deciduous ones. This trade-off between safety-efficiency in petioles has never been attributed to the leaf habit of the species.

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

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

Accounting for trait variability and coordination in predictions of drought-induced range shifts in woody plants.

Functional traits offer a promising avenue to improve predictions of species range shifts under climate change, which will entail warmer and often drier conditions. Although the conceptual foundation linking traits with plant performance and range shifts appears solid, the predictive ability of individual traits remains generally low. In this review, we address this apparent paradox, emphasizing examples of woody plants and traits associated with drought responses at the species' rear edge. Low predictive ability reflects the fact not only that range dynamics tend to be complex and multifactorial, as well as uncertainty in the identification of relevant traits and limited data availability, but also that trait effects are scale- and context-dependent. The latter results from the complex interactions among traits (e.g. compensatory effects) and between them and the environment (e.g. exposure), which ultimately determine persistence and colonization capacity. To confront this complexity, a more balanced coverage of the main functional dimensions involved (stress tolerance, resource use, regeneration and dispersal) is needed, and modelling approaches must be developed that explicitly account for: trait coordination in a hierarchical context; trait variability in space and time and its relationship with exposure; and the effect of biotic interactions in an ecological community context.

How woody plants adjust above- and below-ground traits in response to sustained drought.

Future increases in drought severity and frequency are predicted to have substantial impacts on plant function and survival. However, there is considerable uncertainty concerning what drought adjustment is and whether plants can adjust to sustained drought. This review focuses on woody plants and synthesises the evidence for drought adjustment in a selection of key above-ground and below-ground plant traits. We assess whether evaluating the drought adjustment of single traits, or selections of traits that operate on the same plant functional axis (e.g. photosynthetic traits) is sufficient, or whether a multi-trait approach, integrating across multiple axes, is required. We conclude that studies on drought adjustments in woody plants might overestimate the capacity for adjustment to drier environments if spatial studies along gradients are used, without complementary experimental approaches. We provide evidence that drought adjustment is common in above-ground and below-ground traits; however, whether this is adaptive and sufficient to respond to future droughts remains uncertain for most species. To address this uncertainty, we must move towards studying trait integration within and across multiple axes of plant function (e.g. above-ground and below-ground) to gain a holistic view of drought adjustments at the whole-plant scale and how these influence plant survival.

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.

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.

Rooting depth and xylem vulnerability are independent woody plant traits jointly selected by aridity, seasonality, and water table depth.

Evolutionary radiations of woody taxa within arid environments were made possible by multiple trait innovations including deep roots and embolism-resistant xylem, but little is known about how these traits have coevolved across the phylogeny of woody plants or how they jointly influence the distribution of species. We synthesized global trait and vegetation plot datasets to examine how rooting depth and xylem vulnerability across 188 woody plant species interact with aridity, precipitation seasonality, and water table depth to influence species occurrence probabilities across all biomes. Xylem resistance to embolism and rooting depth are independent woody plant traits that do not exhibit an interspecific trade-off. Resistant xylem and deep roots increase occurrence probabilities in arid, seasonal climates over deep water tables. Resistant xylem and shallow roots increase occurrence probabilities in arid, nonseasonal climates over deep water tables. Vulnerable xylem and deep roots increase occurrence probabilities in arid, nonseasonal climates over shallow water tables. Lastly, vulnerable xylem and shallow roots increase occurrence probabilities in humid climates. Each combination of trait values optimizes occurrence probabilities in unique environmental conditions. Responses of deeply rooted vegetation may be buffered if evaporative demand changes faster than water table depth under climate change.

Axial conduit widening, tree height, and height growth rate set the hydraulic transition of sapwood into heartwood.

The size-related xylem adjustments required to maintain a constant leaf-specific sapwood conductance (KLEAF) with increasing height (H) are still under discussion. Alternative hypotheses are that: (i) the conduit hydraulic diameter (Dh) at any position in the stem and/or (ii) the number of sapwood rings at stem base (NSWr) increase with H. In addition, (iii) reduced stem elongation (ΔH) increases the tip-to-base conductance through inner xylem rings, thus possibly the NSWr contributing to KLEAF. A detailed stem analysis showed that Dh increased with the distance from the ring apex (DCA) in all rings of a Picea abies and a Fagus sylvatica tree. Net of DCA effect, Dh did not increase with H. Using sapwood traits from a global dataset, NSWr increased with H, decreased with ΔH, and the mean sapwood ring width (SWrw) increased with ΔH. A numerical model based on anatomical patterns predicted the effects of H and ΔH on the conductance of inner xylem rings. Our results suggest that the sapwood/heartwood transition depends on both H and ΔH, and is set when the carbon allocation to maintenance respiration of living cells in inner sapwood rings produces a lower gain in total conductance than investing the same carbon in new vascular conduits.

No evidence of age-related decline in propagated Acer pseudoplatanus and Fraxinus excelsior plants.

Although a substantial body of evidence suggests that large and old trees have reduced metabolic levels, the search for the causes behind this observation has proved elusive. The strong coupling between age and size, commonly encountered in the field, precludes the isolation of the potential causes. We used standard propagation techniques (grafting and air-layering) to decouple the effects of size from those of age in affecting leaf structure, biochemistry and physiology of two broadleaved trees, Acer pseudoplatanus (a diffuse-porous species) and Fraxinus excelsior (a ring-porous species). The first year after establishment of the propagated plants, some of the measurements suggested the presence of age-related declines in metabolism, while other measurements either did not show any difference or suggested variability across treatments not associated with either age or size. During the second year after establishment, only one of the measured properties (specific leaf area) continued to show some evidence of an age-mediated decline (although much reduced compared to the field), whereas, for some properties (particularly for F. excelsior), even the opposite trend of age-related increases was apparent. We concluded that (1) our plants suffered from grafting shock during year 1 and they gradually recovered during year 2; (2) the results over 2 years do not support the statement that age directly mediates ageing in either species but instead suggest that size directly mediates ageing processes; and (3) neither shoots nor roots of A. pseudoplatanus showed any evidence of senescence.

Forest system hydraulic conductance: partitioning tree and soil components.

Soil-leaf hydraulic conductance determines canopy-atmosphere coupling in vegetation models, but it is typically derived from ex-situ measurements of stem segments and soil samples. Using a novel approach, we derive robust in-situ estimates for whole-tree conductance (ktree ), 'functional' soil conductance (ksoil ), and 'system' conductance (ksystem , water table to canopy), at two climatically different tropical rainforest sites. Hydraulic 'functional rooting depth', determined for each tree using profiles of soil water potential (Ψsoil ) and sap flux data, enabled a robust determination of ktree and ksoil . ktree was compared across species, size classes, seasons, height above nearest drainage (HAND), two field sites, and to alternative representations of ktree ; ksoil was analysed with respect to variations in site, season and HAND. ktree was lower and changed seasonally at the site with higher vapour pressure deficit (VPD) and rainfall; ktree differed little across species but scaled with tree circumference; rsoil (1/ksoil ) ranged from 0 in the wet season to 10× less than rtree (1/ktree ) in the dry season. VPD and not rainfall may influence plot-level k; leaf water potentials and sap flux can be used to determine ktree , ksoil and ksystem ; Ψsoil profiles can provide mechanistic insights into ecosystem-level water fluxes.

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

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

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.

Upscaling xylem phenology: sample size matters.

BACKGROUND AND AIMS: Upscaling carbon allocation requires knowledge of the variability at the scales at which data are collected and applied. Trees exhibit different growth rates and timings of wood formation. However, the factors explaining these differences remain undetermined, making samplings and estimations of the growth dynamics a complicated task, habitually based on technical rather than statistical reasons. This study explored the variability in xylem phenology among 159 balsam firs [Abies balsamea (L.) Mill.]. METHODS: Wood microcores were collected weekly from April to October 2018 in a natural stand in Quebec, Canada, to detect cambial activity and wood formation timings. We tested spatial autocorrelation, tree size and cell production rates as explanatory variables of xylem phenology. We assessed sample size and margin of error for wood phenology assessment at different confidence levels. KEY RESULTS: Xylem formation lasted between 40 and 110 d, producing between 12 and 93 cells. No effect of spatial proximity or size of individuals was detected on the timings of xylem phenology. Trees with larger cell production rates showed a longer growing season, starting xylem differentiation earlier and ending later. A sample size of 23 trees produced estimates of xylem phenology at a confidence level of 95 % with a margin of error of 1 week. CONCLUSIONS: This study highlighted the high variability in the timings of wood formation among trees within an area of 1 km2. The correlation between the number of new xylem cells and the growing season length suggests a close connection between the processes of wood formation and carbon sequestration. However, the causes of the observed differences in xylem phenology remain partially unresolved. We point out the need to carefully consider sample size when assessing xylem phenology to explore the reasons underlying this variability and to allow reliable upscaling of carbon allocation in forests.

Climate and functional traits jointly mediate tree water-use strategies.

Tree water use is central to plant function and ecosystem fluxes. However, it is still unknown how organ-level water-relations traits are coordinated to determine whole-tree water-use strategies in response to drought, and whether this coordination depends on climate. Here we used a global sap flow database (SAPFLUXNET) to study the response of water use, in terms of whole-tree canopy conductance (G), to vapour pressure deficit (VPD) and to soil water content (SWC) for 142 tree species. We investigated the individual and coordinated effect of six water-relations traits (vulnerability to embolism, Huber value, hydraulic conductivity, turgor-loss point, rooting depth and leaf size) on water-use parameters, also accounting for the effect of tree height and climate (mean annual precipitation, MAP). Reference G and its sensitivity to VPD were tightly coordinated with water-relations traits rather than with MAP. Species with efficient xylem transport had higher canopy conductance but also higher sensitivity to VPD. Moreover, we found that angiosperms had higher reference G and higher sensitivity to VPD than did gymnosperms. Our results highlight the need to consider trait integration and reveal the complications and challenges of defining a single, whole-plant resource use spectrum ranging from 'acquisitive' to 'conservative'.