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.

Increased belowground tree carbon allocation in a mature mixed forest in a dry versus a wet year.

Tree species differ in their carbon (C) allocation strategies during environmental change. Disentangling species-specific strategies and contribution to the C balance of mixed forests requires observations at the individual tree level. We measured a complete set of C pools and fluxes at the tree level in five tree species, conifers and broadleaves, co-existing in a mature evergreen mixed Mediterranean forest. Our study period included a drought year followed by an above-average wet year, offering an opportunity to test the effect of water availability on tree C allocation. We found that in comparison to the wet year, C uptake was lower in the dry year, C use was the same, and allocation to belowground sinks was higher. Among the five major C sinks, respiration was the largest (ca. 60%), while root exudation (ca. 10%) and reproduction (ca. 2%) were those that increased the most in the dry year. Most trees relied on stored starch for maintaining a stable soluble sugars balance, but no significant differences were detected in aboveground storage between dry and wet years. The detailed tree-level analysis of nonstructural carbohydrates and δ13 C dynamics suggest interspecific differences in C allocation among fluxes and tissues, specifically in response to the varying water availability. Overall, our findings shed light on mixed forest physiological responses to drought, an increasing phenomenon under the ongoing climate change.

Context-dependent benefits of forest soil addition on Aleppo pine seedling performance under drought and grass competition.

Seedling establishment under natural conditions is limited by numerous interacting factors. Here, we tested the combined effects of drought, herbaceous competition, and ectomycorrhizal inoculation on the performance of Aleppo pine seedlings grown in a net-house. The roots of all pine seedlings were strongly dominated by Geopora, a fungal genus known to colonize seedlings in dry habitats. Ectomycorrhizal fungi (EMF) inoculum significantly increased seedling height, biomass, and the number of side branches. However, under either competition or drought, the positive effect of EMF on seedling biomass and height was greatly reduced, while the effect on shoot branching was maintained. Further, under a combination of drought and competition, EMF had no influence on either plant growth or shape. The discrepancy in pine performance across treatments highlights the complexity of benefits provided to seedlings by EMF under ecologically relevant settings.

Xylem resistance to cavitation increases during summer in Pinus halepensis.

Cavitation resistance has often been viewed as a relatively static trait, especially for stems of forest trees. Meanwhile, other hydraulic traits, such as turgor loss point (Ψtlp ) and xylem anatomy, change during the season. In this study, we hypothesized that cavitation resistance is also dynamic, changing in coordination with Ψtlp . We began with a comparison of optical vulnerability (OV), microcomputed tomography (µCT) and cavitron methods. All three methods significantly differed in the slope of the curve,Ψ12 and Ψ88 , but not in Ψ50 (xylem pressures that cause 12%, 88%, 50% cavitation, respectively). Thus, we followed the seasonal dynamics (across 2 years) of Ψ50 in Pinus halepensis under Mediterranean climate using the OV method. We found that Ψ50 is a plastic trait with a reduction of approximately 1 MPa from the end of the wet season to the end of the dry season, in coordination with the dynamics of the midday xylem water potential (Ψmidday ) and the Ψtlp . The observed plasticity enabled the trees to maintain a stable positive hydraulic safety margin and avoid cavitation during the long dry season. Seasonal plasticity is vital for understanding the actual risk of cavitation to plants and for modeling species' ability to tolerate harsh environments.

Differential climatic conditions drive growth of Acacia tortilis tree in its range edges in Africa and Asia.

PREMISE: Tree growth is a fundamental biological process that is essential to ecosystem functioning and water and element cycling. Climate exerts a major impact on tree growth, with tree species often requiring a unique set of conditions to initiate and maintain growth throughout the growing season. Still, little is known about the specific climatic factors that enable tree growth in savannah and desert tree species. Among the global tree species, Acacia tortilis occupies one of the largest distribution ranges (crossing 6500 km and 54 latitudes), spanning large parts of Africa and into the Middle East and Asia. METHODS: Here we collected climate data and monitored Acacia tortilis tree growth (continuous measurements of stem circumference) in its southern and northern range edges in South Africa (SA) and Israel (IL), respectively, to elucidate whether the growth-climate interactions were similar in both edges. RESULTS: Growth occurred during the summer (between December and March) in SA and in IL during early summer and autumn (April-June and October-November, respectively). Surprisingly, annual growth was 40% higher in IL than in SA. Within the wide distribution range of Acacia tortilis, our statistical model showed that climatic drivers of tree growth differed between the two sites. CONCLUSIONS: High temperatures facilitated growth at the hot and arid IL site, while high humidity permitted growth at the more humid SA site. Our results confer an additional understanding of tree growth adaptation to extreme conditions in Acacia's world range edges, a major point of interest with ongoing climate change.

Relationships between xylem embolism and tree functioning during drought, recovery, and recurring drought in Aleppo pine.

Recent findings suggest that trees can survive high levels of drought-induced xylem embolism. In many cases, the embolism is irreversible and, therefore, can potentially affect post-drought recovery and tree function under recurring droughts. We examined the development of embolism in potted Aleppo pines, a common species in hot, dry Mediterranean habitats. We asked (1) how post-drought recovery is affected by different levels of embolism and (2) what consequences this drought-induced damage has under a recurring drought scenario. Young trees were dehydrated to target water potential (Ψx ) values of -3.5, -5.2 and -9.5 MPa (which corresponded to ~6%, ~41% and ~76% embolism), and recovery of the surviving trees was measured over an 8-months period (i.e., embolism, leaf gas-exchange, Ψx ). An additional group of trees was exposed to Ψx of -6.0 MPa, either with or without preceding drought (Ψx of -5.2 MPa) to test the effect of hydraulic damage during repeated drought. Trees that reached -9.5 MPa died, but none from the other groups. Embolism levels in dying trees were on average 76% of conductive xylem and no tree was dying below 62% embolism. Stomatal recovery was negatively proportional to the level of hydraulic damage sustained during drought, for at least a month after drought relief. Trees that experienced drought for the second time took longer to reach fatal Ψx levels than first-time dehydrating trees. Decreased stomatal conductance following drought can be seen as "drought legacy," impeding recovery of tree functioning, but also as a safety mechanism during a consecutive drought.

Carbohydrate dynamics in Populus trees under drought: An expression atlas of genes related to sensing, translocation, and metabolism across organs.

In trees, nonstructural carbohydrates (NSCs) serve as long-term carbon storage and long-distance carbon transport from source to sink. NSC management in response to drought stress is key to our understanding of drought acclimation. However, the molecular mechanisms underlying these processes remain unclear. By combining a transcriptomic approach with NSC quantification in the leaves, stems, and roots of Populus alba under drought stress, we analyzed genes from 29 gene families related to NSC signaling, translocation, and metabolism. We found starch depletion across organs and accumulation of soluble sugars (SS) in the leaves. Activation of the trehalose-6-phosphate/SNF1-related protein kinase (SnRK1) signaling pathway across organs via the suppression of class I TREHALOSE-PHOSPHATE SYNTHASE (TPS) and the expression of class II TPS genes suggested an active response to drought. The expression of SnRK1α and ß subunits, and SUCROSE SYNTHASE6 supported SS accumulation in leaves. The upregulation of active transporters and the downregulation of most passive transporters implied a shift toward active sugar transport and enhanced regulation over partitioning. SS accumulation in vacuoles supports osmoregulation in leaves. The increased expression of sucrose synthesis genes and reduced expression of sucrose degradation genes in the roots did not coincide with sucrose levels, implying local sucrose production for energy. Moreover, the downregulation of invertases in the roots suggests limited sucrose allocation from the aboveground organs. This study provides an expression atlas of NSC-related genes that respond to drought in poplar trees, and can be tested in tree improvement programs for adaptation to drought conditions.

In situ, direct observation of seasonal embolism dynamics in Aleppo pine trees growing on the dry edge of their distribution.

Xylem embolism impairs hydraulic conductivity in trees and drives drought-induced mortality. While embolism has been monitored in vivo in potted plants, and research has revealed evidence of embolism in field-grown trees, continuous in situ monitoring of cavitation in forests is lacking. Seasonal patterns of embolism were monitored in branchlets of Aleppo pine (Pinus halepensis) trees growing in a dry Mediterranean forest. Optical visualization (OV) sensors were installed on terminal branches, in addition to monthly sampling for micro computed tomography scans. We detected 208 cavitation events among four trees, which represented an embolism increase from zero to c. 12% along the dry season. Virtually all the cavitation events occurred during daytime hours, with 77% occurring between 10:00 and 17:00 h. The probability for cavitation in a given hour increased as vapor pressure deficit (VPD) increased, up to a probability of 42% for cavitation when VPD > 5 kPa. The findings uniquely reveal the instantaneous environmental conditions that lead to cavitation. The increased likelihood of cavitation events under high VPD in water-stressed pines is the first empirical support for this long hypothesized relationship. Our observations suggest that low levels of embolism are common in Aleppo pine trees at the dry edge of their distribution.

Asymmetric belowground carbon transfer in a diverse tree community.

Mycorrhizal fungi can colonize multiple trees of a single or multiple taxa, facilitating bidirectional exchange of carbon between trees. Mycorrhiza-induced carbon transfer was shown in the forest, but it is unknown whether carbon is shared symmetrically among tree species, and if not, which tree species are better donors and which are better recipients. Here, we test this question by investigating carbon transfer dynamics among five Mediterranean tree species in a microcosm system, including both ectomycorrhizal (EM) and arbuscular (AM) plants. Trees were planted together in "community boxes" using natural soil from a mixed forest plot that serves as a habitat for all five tree species and their native mycorrhizal fungi. In each box, only the trees of a single species were pulse-labelled with 13 CO2 . We found that carbon transfer was asymmetric, with oak being a better donor, and pistacia and cypress better recipients. Shared mycorrhizal species may have facilitated carbon transfer, but their diversity did not affect the amount, nor timing, of the transfer. Overall, our findings in a microcosm system expose rich, but hidden, belowground interactions in a diverse population of trees and mycorrhizal fungi. The asymmetric carbon exchange among cohabiting tree species could potentially contribute to forest resilience in an uncertain future.

Closing in on the last frontier: C allocation in the rhizosphere.

Increased belowground C allocation of trees, especially enhanced rhizodeposition, might lead to long-term C sequestration in forest soil. Microbes are crucial players in this complex process of forming stable soil organic carbon (SOC). Hence, research must be accelerated to understand the complex rhizosphere processes and their effect on stable SOC formation. This is a commentary on Hikino et al., 2022, https://onlinelibrary.wiley.com/doi/full/10.1111/gcb.16388.

Rapid starch degradation in the wood of olive trees under heat and drought is permitted by three stress-specific beta amylases.

Carbon reserve use is a major drought response in trees, enabling tree survival in conditions prohibiting photosynthesis. However, regulation of starch metabolism under drought at the whole-tree scale is still poorly understood. To this end, we combined measurements of nonstructural carbohydrates (NSCs), tree physiology and gene expression. The experiment was conducted outside on olive trees in pots under 90 d of seasonal spring to summer warming. Half of the trees were also subjected to limited water conditions for 28 d. Photosynthesis decreased in dehydrating trees from 19 to 0.5 µmol m-2  s-1 during the drought period. Starch degradation and mannitol production were a major drought response, with mannitol increasing to 71% and 41% out of total NSCs in shoots and roots, respectively. We identified the gene family members potentially relevant either to long-term or stress-induced carbon storage. Partitioning of expression patterns among ß amylase and starch synthase family members was observed, with three ß amylases possibly facilitating the rapid starch degradation under heat and drought. Our results suggest a group of stress-related, starch metabolism genes, correlated with NSC fluctuations during drought and recovery. The daily starch metabolism gene expression was different from the stress-mode starch metabolism pattern, where some genes are uniquely expressed during the stress-mode response.

Intraspecific responses to climate reveal nonintuitive warming impacts on a widespread thermophilic conifer.

Many ecologically important forest trees from dry areas have been insufficiently investigated for their ability to adapt to the challenges posed by climate change, which hampers the implementation of mitigation policies. We analyzed 14 common-garden experiments across the Mediterranean which studied the widespread thermophilic conifer Pinus halepensis and involved 157 populations categorized into five ecotypes. Ecotype-specific tree height responses to climate were applied to projected climate change (2071-2100 ad), to project potential growth patterns both locally and across the species' range. We found contrasting ecotypic sensitivities to annual precipitation but comparatively uniform responses to mean temperature, while evidence of local adaptation for tree height was limited to mesic ecotypes. We projected intriguing patterns of response range-wide, implying either height inhibition or stimulation of up to 75%, and deduced that the ecotype currently experiencing more favorable (wetter) conditions will show the largest inhibition. Extensive height reductions can be expected for coastal areas of France, Greece, Spain and northern Africa. Our findings underline the fact that intraspecific variations in sensitivity to precipitation must be considered when projecting tree height responses of dry forests to future climate. The ecotype-specific projected performances call for management activities to ensure forest resilience in the Mediterranean through, for example, tailored deployment strategies.

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.

Share the wealth: Trees with greater ectomycorrhizal species overlap share more carbon.

The mutualistic symbiosis between forest trees and ectomycorrhizal fungi (EMF) is among the most ubiquitous and successful interactions in terrestrial ecosystems. Specific species of EMF are known to colonize specific tree species, benefitting from their carbon source, and in turn, improving their access to soil water and nutrients. EMF also form extensive mycelial networks that can link multiple root-tips of different trees. Yet the number of tree species connected by such mycelial networks, and the traffic of material across them, are just now under study. Recently we reported substantial belowground carbon transfer between Picea, Pinus, Larix and Fagus trees in a mature forest. Here, we analyze the EMF community of these same individual trees and identify the most likely taxa responsible for the observed carbon transfer. Among the nearly 1,200 EMF root-tips examined, 50%-70% belong to operational taxonomic units (OTUs) that were associated with three or four tree host species, and 90% of all OTUs were associated with at least two tree species. Sporocarp 13 C signals indicated that carbon originating from labelled Picea trees was transferred among trees through EMF networks. Interestingly, phylogenetically more closely related tree species exhibited more similar EMF communities and exchanged more carbon. Our results show that belowground carbon transfer is well orchestrated by the evolution of EMFs and tree symbiosis.

The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought.

Climate change is expected to exacerbate drought for many plants, making drought tolerance a key driver of species and ecosystem responses. Plant drought tolerance is determined by multiple traits, but the relationships among traits, either within individual plants or across species, have not been evaluated for general patterns across plant diversity. We synthesized the published data for stomatal closure, wilting, declines in hydraulic conductivity in the leaves, stems, and roots, and plant mortality for 262 woody angiosperm and 48 gymnosperm species. We evaluated the correlations among the drought tolerance traits across species, and the general sequence of water potential thresholds for these traits within individual plants. The trait correlations across species provide a framework for predicting plant responses to a wide range of water stress from one or two sampled traits, increasing the ability to rapidly characterize drought tolerance across diverse species. Analyzing these correlations also identified correlations among the leaf and stem hydraulic traits and the wilting point, or turgor loss point, beyond those expected from shared ancestry or independent associations with water stress alone. Further, on average, the angiosperm species generally exhibited a sequence of drought tolerance traits that is expected to limit severe tissue damage during drought, such as wilting and substantial stem embolism. This synthesis of the relationships among the drought tolerance traits provides crucial, empirically supported insight into representing variation in multiple traits in models of plant and ecosystem responses to drought.

Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe.

Drought-induced tree mortality has been observed globally and is expected to increase under climate change scenarios, with large potential consequences for the terrestrial carbon sink. Predicting mortality across species is crucial for assessing the effects of climate extremes on forest community biodiversity, composition, and carbon sequestration. However, the physiological traits associated with elevated risk of mortality in diverse ecosystems remain unknown, although these traits could greatly improve understanding and prediction of tree mortality in forests. We performed a meta-analysis on species' mortality rates across 475 species from 33 studies around the globe to assess which traits determine a species' mortality risk. We found that species-specific mortality anomalies from community mortality rate in a given drought were associated with plant hydraulic traits. Across all species, mortality was best predicted by a low hydraulic safety margin-the difference between typical minimum xylem water potential and that causing xylem dysfunction-and xylem vulnerability to embolism. Angiosperms and gymnosperms experienced roughly equal mortality risks. Our results provide broad support for the hypothesis that hydraulic traits capture key mechanisms determining tree death and highlight that physiological traits can improve vegetation model prediction of tree mortality during climate extremes.

Tree growth and water-use in hyper-arid Acacia occurs during the hottest and driest season.

Drought-induced tree mortality has been recently increasing and is expected to increase further under warming climate. Conversely, tree species that survive under arid conditions might provide vital information on successful drought resistance strategies. Although Acacia (Vachellia) species dominate many of the globe's deserts, little is known about their growth dynamics and water-use in situ. Stem diameter dynamics, leaf phenology, and sap flow were monitored during 3 consecutive years in five Acacia raddiana trees and five Acacia tortilis trees in the Arid Arava Valley, southern Israel (annual precipitation 20-70 mm, restricted to October-May). We hypothesized that stem growth and other tree activities are synchronized with, and limited to single rainfall or flashflood events. Unexpectedly, cambial growth of both Acacia species was arrested during the wet season, and occurred during most of the dry season, coinciding with maximum daily temperatures as high as 45 °C and vapor pressure deficit of up to 9 kPa. Summer growth was correlated with peak sap flow in June, with almost year-round activity and foliage cover. To the best of our knowledge, these are the harshest drought conditions ever documented permitting cambial growth. These findings point to the possibility that summer cambial growth in Acacia under hyper-arid conditions relies on concurrent leaf gas exchange, which is in turn permitted by access to deep soil water. Soil water can support low-density tree populations despite heat and drought, as long as recharge is kept above a minimum threshold.

A synthesis of radial growth patterns preceding tree mortality.

Tree mortality is a key factor influencing forest functions and dynamics, but our understanding of the mechanisms leading to mortality and the associated changes in tree growth rates are still limited. We compiled a new pan-continental tree-ring width database from sites where both dead and living trees were sampled (2970 dead and 4224 living trees from 190 sites, including 36 species), and compared early and recent growth rates between trees that died and those that survived a given mortality event. We observed a decrease in radial growth before death in ca. 84% of the mortality events. The extent and duration of these reductions were highly variable (1-100 years in 96% of events) due to the complex interactions among study species and the source(s) of mortality. Strong and long-lasting declines were found for gymnosperms, shade- and drought-tolerant species, and trees that died from competition. Angiosperms and trees that died due to biotic attacks (especially bark-beetles) typically showed relatively small and short-term growth reductions. Our analysis did not highlight any universal trade-off between early growth and tree longevity within a species, although this result may also reflect high variability in sampling design among sites. The intersite and interspecific variability in growth patterns before mortality provides valuable information on the nature of the mortality process, which is consistent with our understanding of the physiological mechanisms leading to mortality. Abrupt changes in growth immediately before death can be associated with generalized hydraulic failure and/or bark-beetle attack, while long-term decrease in growth may be associated with a gradual decline in hydraulic performance coupled with depletion in carbon reserves. Our results imply that growth-based mortality algorithms may be a powerful tool for predicting gymnosperm mortality induced by chronic stress, but not necessarily so for angiosperms and in case of intense drought or bark-beetle outbreaks.

Association between sap flow-derived and eddy covariance-derived measurements of forest canopy CO2 uptake.

The carbon sink intensity of the biosphere depends on the balance between gross primary productivity (GPP) of forest canopies and ecosystem respiration. GPP, however, cannot be directly measured and estimates are not well constrained. A new approach relying on canopy transpiration flux measured as sap flow, and water-use efficiency inferred from carbon isotope analysis (GPPSF ) has been proposed, but not tested against eddy covariance-based estimates (GPPEC ). Here we take advantage of parallel measurements using the two approaches at a semi-arid pine forest site to compare the GPPSF and GPPEC estimates on diurnal to annual timescales. GPPSF captured the seasonal dynamics of GPPEC (GPPSF  = 0.99 × GPPEC , r(2)  = 0.78, RMSE = 0.82, n = 457 d) with good agreement at the annual timescale (653 vs 670 g C m(-2)  yr(-1) ). Both methods showed that GPP ranged between 1 and 8 g C m(-2)  d(-1) , and the GPPSF /GPPEC ratio was between 0.5 and 2.0 during 82% of the days. Carbon uptake dynamics at the individual tree scale conformed with leaf scale rates of net assimilation. GPPSF can produce robust estimations of tree- and canopy-scale rates of CO2 uptake, providing constraints and greatly extending current GPPEC estimations.