No evidence of canopy-scale leaf thermoregulation to cool leaves below air temperature across a range of forest ecosystems.

Understanding and predicting the relationship between leaf temperature (Tleaf) and air temperature (Tair) is essential for projecting responses to a warming climate, as studies suggest that many forests are near thermal thresholds for carbon uptake. Based on leaf measurements, the limited leaf homeothermy hypothesis argues that daytime Tleaf is maintained near photosynthetic temperature optima and below damaging temperature thresholds. Specifically, leaves should cool below Tair at higher temperatures (i.e., > ∼25-30°C) leading to slopes <1 in Tleaf/Tair relationships and substantial carbon uptake when leaves are cooler than air. This hypothesis implies that climate warming will be mitigated by a compensatory leaf cooling response. A key uncertainty is understanding whether such thermoregulatory behavior occurs in natural forest canopies. We present an unprecedented set of growing season canopy-level leaf temperature (Tcan) data measured with thermal imaging at multiple well-instrumented forest sites in North and Central America. Our data do not support the limited homeothermy hypothesis: canopy leaves are warmer than air during most of the day and only cool below air in mid to late afternoon, leading to Tcan/Tair slopes >1 and hysteretic behavior. We find that the majority of ecosystem photosynthesis occurs when canopy leaves are warmer than air. Using energy balance and physiological modeling, we show that key leaf traits influence leaf-air coupling and ultimately the Tcan/Tair relationship. Canopy structure also plays an important role in Tcan dynamics. Future climate warming is likely to lead to even greater Tcan, with attendant impacts on forest carbon cycling and mortality risk.

Cross-biome synthesis of source versus sink limits to tree growth.

Uncertainties surrounding tree carbon allocation to growth are a major limitation to projections of forest carbon sequestration and response to climate change. The prevalence and extent to which carbon assimilation (source) or cambial activity (sink) mediate wood production are fundamentally important and remain elusive. We quantified source-sink relations across biomes by combining eddy-covariance gross primary production with extensive on-site and regional tree ring observations. We found widespread temporal decoupling between carbon assimilation and tree growth, underpinned by contrasting climatic sensitivities of these two processes. Substantial differences in assimilation-growth decoupling between angiosperms and gymnosperms were determined, as well as stronger decoupling with canopy closure, aridity, and decreasing temperatures. Our results reveal pervasive sink control over tree growth that is likely to be increasingly prominent under global climate change.

A thin line between life and death: Radial sap flux failure signals trajectory to tree mortality.

This article comments on: Seeking the "point of no return" in the sequence of events leading to mortality of mature trees.

Trade-offs between xylem water and carbohydrate storage among 24 coexisting subtropical understory shrub species spanning a spectrum of isohydry.

Hydraulic capacitance and carbohydrate storage are two drought adaptation strategies of woody angiosperms. However, we currently lack information on their associations and how they are associated with species' degree of isohydry. We measured total stem xylem nonstructural carbohydrate (NSC) concentration in the dry and wet seasons, xylem hydraulic capacitance, native leaf water potentials, pressure-volume curve parameters and photosynthetic performance in 24 woody understory species differing in their degree of isohydry. We found a trade-off between xylem water and carbohydrate storage both in storage capacitance and along a spectrum of isohydry. Species with higher hydraulic capacitance had lower native NSC storage. The less isohydric species tended to show greater NSC depletion in the dry season and have more drought-tolerant leaves. In contrast, the more isohydric species had higher hydraulic capacitance, which may enhance their drought avoidance capacity. In these species, leaf flushing in the wet season and higher photosynthetic rates in the dry season resulted in accumulation rather than depletion of NSC in the dry season. Our results provide new insights into the mechanisms through which xylem storage functions determine co-occurring species' drought adaptation strategies and improve our capacity to predict community assembly processes under drought.

Hydraulic traits of Neotropical canopy liana and tree species across a broad range of wood density: implications for predicting drought mortality with models.

Wood density (WD) is often used as a proxy for hydraulic traits such as vulnerability to drought-induced xylem cavitation and maximum water transport capacity, with dense-wooded species generally being more resistant to drought-induced xylem cavitation, having lower rates of maximum water transport and lower sapwood capacitance than light-wooded species. However, relationships between WD and the hydraulic traits that they aim to predict have not been well established in tropical forests, where modeling is necessary to predict drought responses for a high diversity of unmeasured species. We evaluated WD and relationships with stem xylem vulnerability by measuring cavitation curves, sapwood water release curves and minimum seasonal water potential (Ψmin) on upper canopy branches of six tree species and three liana species from a single wet tropical forest site in Panama. The objective was to better understand coordination and trade-offs among hydraulic traits and the potential utility of these relationships for modeling purposes. We found that parameters from sapwood water release curves such as capacitance, saturated water content and sapwood turgor loss point (Ψtlp,x) were related to WD, whereas stem vulnerability curve parameters were not. However, the water potential corresponding to 50% loss of hydraulic conductivity (P50) was related to Ψtlp,x and sapwood osmotic potential at full turgor (πo,x). Furthermore, species with lower Ψmin showed lower P50, Ψtlp,x and πo,x suggesting greater drought resistance. Our results indicate that WD is a good easy-to-measure proxy for some traits related to drought resistance, but not others. The ability of hydraulic traits such as P50 and Ψtlp,x to predict mortality must be carefully examined if WD values are to be used to predict drought responses in species without detailed physiological measurements.

Below-ground determinants and ecological implications of shrub species' degree of isohydry in subtropical pine plantations.

The degree of plant iso/anisohydry is a popular framework for characterising species-specific drought responses. However, we know little about associations between below-ground and above-ground hydraulic traits as well as the broader ecological implications of this framework. For 24 understory shrub species in seasonally dry subtropical coniferous plantations, we investigated contributions of the degree of isohydry to species' resource economy strategies, abundance, and importance value, and quantified the hydraulic conductance (Kh ) of above-ground and below-ground organs, magnitude of deep water acquisition (WAdeep ), shallow absorptive root traits (diameter, specific root length, tissue density), and resource-use efficiencies (Amax , maximum photosynthesis rate; PNUE, photosynthetic nitrogen-use efficiency). The extreme isohydric understory species had lower wood density (a proxy for higher growth rates) because their higher WAdeep and whole-plant Kh allowed higher Amax and PNUE, and thus did not necessarily show lower abundance and importance values. Although species' Kh was coordinated with their water foraging capacity in shallow soil, the more acquisitive deep roots were more crucial than shallow roots in shaping species' extreme isohydric behaviour. Our results provide new insights into the mechanisms through which below-ground hydraulic traits, especially those of deep roots, determine species' degree of isohydry and economic strategies.

Linking reliance on deep soil water to resource economy strategies and abundance among coexisting understorey shrub species in subtropical pine plantations.

Strategies for deep soil water acquisition (WAdeep ) are critical to a species' adaptation to drought. However, it is unknown how WAdeep determines the abundance and resource economy strategies of understorey shrub species. With data from 13 understorey shrub species in subtropical coniferous plantations, we investigated associations between the magnitude of WAdeep , the seasonal plasticity of WAdeep , midday leaf water potential (Ψmd ), species abundance and resource economic traits across organs. Higher capacity for WAdeep was associated with higher intrinsic water use efficiency, but was not necessary for maintaining higher Ψmd in the dry season nor was it an ubiquitous trait possessed by the most common shrub species. Species with higher seasonal plasticity of WAdeep had lower wood density, indicating that fast species had higher plasticity in deep soil resource acquisition. However, the magnitude and plasticity of WAdeep were not related to shallow fine root economy traits, suggesting independent dimensions of soil resource acquisition between deep and shallow soil. Our results provide new insights into the mechanisms through which the magnitude and plasticity of WAdeep interact with shallow soil and aboveground resource acquisition traits to integrate the whole-plant economic spectrum and, thus, community assembly processes.

Historical changes in the stomatal limitation of photosynthesis: empirical support for an optimality principle.

The ratio of leaf internal (ci ) to ambient (ca ) partial pressure of CO2 , defined here as χ, is an index of adjustments in both leaf stomatal conductance and photosynthetic rate to environmental conditions. Measurements and proxies of this ratio can be used to constrain vegetation model uncertainties for predicting terrestrial carbon uptake and water use. We test a theory based on the least-cost optimality hypothesis for modelling historical changes in χ over the 1951-2014 period, across different tree species and environmental conditions, as reconstructed from stable carbon isotopic measurements across a global network of 103 absolutely dated tree-ring chronologies. The theory predicts optimal χ as a function of air temperature, vapour pressure deficit, ca and atmospheric pressure. The theoretical model predicts 39% of the variance in χ values across sites and years, but underestimates the intersite variability in the reconstructed χ trends, resulting in only 8% of the variance in χ trends across years explained by the model. Overall, our results support theoretical predictions that variations in χ are tightly regulated by the four environmental drivers. They also suggest that explicitly accounting for the effects of plant-available soil water and other site-specific characteristics might improve the predictions.

Water potential control of turgor-driven tracheid enlargement in Scots pine at its xeric distribution edge.

The extent to which water availability can be used to predict the enlargement and final dimensions of xylem conduits remains an open issue. We reconstructed the time course of tracheid enlargement in Pinus sylvestris trees in central Spain by repeated measurements of tracheid diameter on microcores sampled weekly during a 2 yr period. We analyzed the role of water availability in these dynamics empirically through time-series correlation analysis and mechanistically by building a model that simulates daily tracheid enlargement rate and duration based on Lockhart's equation and water potential as the sole input. Tracheid enlargement followed a sigmoid-like time course, which varied intra- and interannually. Our empirical analysis showed that final tracheid diameter was strongly related to water availability during tracheid enlargement. The mechanistic model was calibrated and successfully validated (R2  = 0.92) against the observed tracheid enlargement time course. The model was also able to reproduce the seasonal variations of tracheid enlargement rate, duration and final diameter (R2  = 0.84-0.99). Our results support the hypothesis that tracheid enlargement and final dimensions can be modeled based on the direct effect of water potential on turgor-driven cell expansion. We argue that such a mechanism is consistent with other reported patterns of tracheid dimension variation.

A dynamic yet vulnerable pipeline: Integration and coordination of hydraulic traits across whole plants.

The vast majority of measurements in the field of plant hydraulics have been on small-diameter branches from woody species. These measurements have provided considerable insight into plant functioning, but our understanding of plant physiology and ecology would benefit from a broader view, because branch hydraulic properties are influenced by many factors. Here, we discuss the influence that other components of the hydraulic network have on branch vulnerability to embolism propagation. We also modelled the impact of changes in the ratio of root-to-leaf areas and soil texture on vulnerability to hydraulic failure along the soil-to-leaf continuum and showed that hydraulic function is better maintained through changes in root vulnerability and root-to-leaf area ratio than in branch vulnerability. Differences among species in the stringency with which they regulate leaf water potential and in reliance on stored water to buffer changes in water potential also affect the need to construct embolism resistant branches. Many approaches, such as measurements on fine roots, small individuals, combining sap flow and psychrometry techniques, and modelling efforts, could vastly improve our understanding of whole-plant hydraulic functioning. A better understanding of how traits are coordinated across the whole plant will improve predictions for plant function under future climate conditions.

Coordination and trade-offs between leaf and stem hydraulic traits and stomatal regulation along a spectrum of isohydry to anisohydry.

The degree of plant iso/anisohydry, a widely used framework for classifying species-specific hydraulic strategies, integrates multiple components of the whole-plant hydraulic pathway. However, little is known about how it associates with coordination of functional and structural traits within and across different organs. We examined stem and leaf hydraulic capacitance and conductivity/conductance, stem xylem anatomical features, stomatal regulation of daily minimum leaf and stem water potential (Ψ), and the kinetics of stomatal responses to vapour pressure deficit (VPD) in six diverse woody species differing markedly in their degree of iso/anisohydry. At the stem level, more anisohydric species had higher wood density and lower native capacitance and conductivity. Like stems, leaves of more anisohydric species had lower hydraulic conductance; however, unlike stems, their leaves had higher native capacitance at their daily minimum values of leaf Ψ. Moreover, rates of VPD-induced stomatal closure were related to intrinsic rather than native leaf capacitance and were not associated with species' degree of iso/anisohydry. Our results suggest a trade-off between hydraulic storage and efficiency in the leaf, but a coordination between hydraulic storage and efficiency in the stem along a spectrum of plant iso/anisohydry.

Investigating old-growth ponderosa pine physiology using tree-rings, δ13 C, δ18 O, and a process-based model.

In dealing with predicted changes in environmental conditions outside those experienced today, forest managers and researchers rely on process-based models to inform physiological processes and predict future forest growth responses. The carbon and oxygen isotope ratios of tree-ring cellulose (δ13 Ccell , δ18 Ocell ) reveal long-term, integrated physiological responses to environmental conditions. We incorporated a submodel of δ18 Ocell into the widely used Physiological Principles in Predicting Growth (3-PG) model for the first time, to complement a recently added δ13 Ccell submodel. We parameterized the model using previously reported stand characteristics and long-term trajectories of tree-ring growth, δ13 Ccell , and δ18 Ocell collected from the Metolius AmeriFlux site in central Oregon (upland trees). We then applied the parameterized model to a nearby set of riparian trees to investigate the physiological drivers of differences in observed basal area increment (BAI) and δ13 Ccell trajectories between upland and riparian trees. The model showed that greater available soil water and maximum canopy conductance likely explain the greater observed BAI and lower δ13 Ccell of riparian trees. Unexpectedly, both observed and simulated δ18 Ocell trajectories did not differ between the upland and riparian trees, likely due to similar δ18 O of source water isotope composition. The δ18 Ocell submodel with a Peclet effect improved model estimates of δ18 Ocell because its calculation utilizes 3-PG growth and allocation processes. Because simulated stand-level transpiration (E) is used in the δ18 O submodel, aspects of leaf-level anatomy such as the effective path length for transport of water from the xylem to the sites of evaporation could be estimated.

Iso/Anisohydry: Still a Useful Concept.

The iso/anisohydry concept characterizes plants according to their water status regulation. Coexisting definitions and misconceptions have recently led to considerable criticism. We discuss here reasons for the misconceptions, and propose a robust definition of iso/anisohydry using the leaf turgor loss point to integrate the complex interplay of plant hydraulic traits.

Correction to: Allocation to leaf area and sapwood area affects water relations of co-occurring savanna and forest trees.

The original version of this article unfortunately contained a mistake. The Electronic supplementary material (ESM) was accompanying this article by mistake.

Metrics and proxies for stringency of regulation of plant water status (iso/anisohydry): a global data set reveals coordination and trade-offs among water transport traits.

Plants operate along a continuum of stringency of regulation of plant water potential from isohydry to anisohydry. However, most metrics and proxies of plant iso/anisohydric behavior have been developed from limited sets of site-specific experiments. Understanding the underlying mechanisms that determine species' operating ranges along this continuum, independent of site and growing conditions, remains challenging. We compiled a global database to assess the global patterns of metrics and proxies of plant iso/anisohydry and then explored some of the underlying functional traits and trade-offs associated with stringency of regulation that determines where species operate along the continuum. Our results showed that arid and semi-arid biomes were associated with greater anisohydry than more mesic biomes, and angiosperms showed marginally greater anisohydry than gymnosperms. Leaf water potential at the turgor loss point (Ψtlp) and wood density were the two most powerful proxies for ranking the degree of plant iso/anisohydry for a wide range of species and biomes. Both of these simple traits can be easily and rapidly determined, and therefore show promise for a priori mapping and understanding of the global distribution pattern of the degree of plant iso/anisohydry. Generally, the most anisohydric species had the most negative values of Ψtlp and highest wood density, greatest resistance to embolism, lowest hydraulic capacitance and lowest leaf-specific hydraulic conductivity of their branches. Wood density in particular appeared to be central to a coordinated series of traits, trade-offs and behaviors along a continuum of iso/anisohydry. Quantification of species' operating ranges along a continuum of iso/anisohydry and identification of associated trade-offs among functional traits may hold promise for mechanistic modeling of species-specific responses to the anticipated more frequent and severe droughts under global climate change scenarios.

Fire deficits have increased drought sensitivity in dry conifer forests: Fire frequency and tree-ring carbon isotope evidence from Central Oregon.

A century of fire suppression across the Western United States has led to more crowded forests and increased competition for resources. Studies of forest thinning or stand conditions after mortality events have provided indirect evidence for how competition can promote drought stress and predispose forests to severe fire and/or bark beetle outbreaks. Here, we demonstrate linkages between fire deficits and increasing drought stress through analyses of annually resolved tree-ring growth, fire scars, and carbon isotope discrimination (Δ13 C) across a dry mixed-conifer forest landscape. Fire deficits across the study area have increased the sensitivity of leaf gas exchange to drought stress over the past >100 years. Since 1910, stand basal area in these forests has more than doubled and fire-return intervals have increased from 25 to 140 years. Meanwhile, the portion of interannual variation in tree-ring Δ13 C explained by the Palmer Drought Severity Index has more than doubled in ca. 300-500-year-old Pinus ponderosa as well as in fire-intolerant, ca. 90-190-year-old Abies grandis. Drought stress has increased in stands with a basal area of ≥25 m2 /ha in 1910, as indicated by negative temporal Δ13 C trends, whereas stands with basal area ≤25 m2 /ha in 1910, due to frequent or intense wildfire activity in decades beforehand, were initially buffered from increased drought stress and have benefited more from rising ambient carbon dioxide concentrations, [CO2 ], as demonstrated by positive temporal Δ13 C trends. Furthermore, the average Δ13 C response across all P. ponderosa since 1830 indicates that photosynthetic assimilation rates and stomatal conductance have been reduced by ~10% and ~20%, respectively, compared to expected trends due to increasing [CO2 ]. Although disturbance legacies contribute to local-scale intensity of drought stress, fire deficits have reduced drought resistance of mixed-conifer forests and made them more susceptible to challenges by pests and pathogens and other disturbances.

Woody plants optimise stomatal behaviour relative to hydraulic risk.

Stomatal response to environmental conditions forms the backbone of all ecosystem and carbon cycle models, but is largely based on empirical relationships. Evolutionary theories of stomatal behaviour are critical for guarding against prediction errors of empirical models under future climates. Longstanding theory holds that stomata maximise fitness by acting to maintain constant marginal water use efficiency over a given time horizon, but a recent evolutionary theory proposes that stomata instead maximise carbon gain minus carbon costs/risk of hydraulic damage. Using data from 34 species that span global forest biomes, we find that the recent carbon-maximisation optimisation theory is widely supported, revealing that the evolution of stomatal regulation has not been primarily driven by attainment of constant marginal water use efficiency. Optimal control of stomata to manage hydraulic risk is likely to have significant consequences for ecosystem fluxes during drought, which is critical given projected intensification of the global hydrological cycle.

Hydraulics play an important role in causing low growth rate and dieback of aging Pinus sylvestris var. mongolica trees in plantations of Northeast China.

The frequently observed forest decline in water-limited regions may be associated with impaired tree hydraulics, but the precise physiological mechanisms remain poorly understood. We compared hydraulic architecture of Mongolian pine (Pinus sylvestris var. mongolica) trees of different size classes from a plantation and a natural forest site to test whether greater hydraulic limitation with increasing size plays an important role in tree decline observed in the more water-limited plantation site. We found that trees from plantations overall showed significantly lower stem hydraulic efficiency. More importantly, plantation-grown trees showed significant declines in stem hydraulic conductivity and hydraulic safety margins as well as syndromes of stronger drought stress with increasing size, whereas no such trends were observed at the natural forest site. Most notably, the leaf to sapwood area ratio (LA/SA) showed a strong linear decline with increasing tree size at the plantation site. Although compensatory adjustments in LA/SA may mitigate the effect of increased water stress in larger trees, they may result in greater risk of carbon imbalance, eventually limiting tree growth at the plantation site. Our results provide a potential mechanistic explanation for the widespread decline of Mongolian pine trees in plantations of Northern China.