Pushing the envelope: do narrowly and widely distributed Eucalyptus species differ in response to climate warming?

Contemporary climate change will push many tree species into conditions that are outside their current climate envelopes. Using the Eucalyptus genus as a model, we addressed whether species with narrower geographical distributions show constrained ability to cope with warming relative to species with wider distributions, and whether this ability differs among species from tropical and temperate climates. We grew seedlings of widely and narrowly distributed Eucalyptus species from temperate and tropical Australia in a glasshouse under two temperature regimes: the summer temperature at seed origin and +3.5°C. We measured physical traits and leaf-level gas exchange to assess warming influences on growth rates, allocation patterns, and physiological acclimation capacity. Warming generally stimulated growth, such that higher relative growth rates early in development placed seedlings on a trajectory of greater mass accumulation. The growth enhancement under warming was larger among widely than narrowly distributed species and among temperate rather than tropical provenances. The differential growth enhancement was primarily attributable to leaf area production and adjustments of specific leaf area. Our results suggest that tree species, including those with climate envelopes that will be exceeded by contemporary climate warming, possess capacity to physiologically acclimate but may have varying ability to adjust morphology.

Leaf water potential measurements using the pressure chamber: Synthetic testing of assumptions towards best practices for precision and accuracy.

Leaf water potential (ψleaf ), typically measured using the pressure chamber, is the most important metric of plant water status, providing high theoretical value and information content for multiple applications in quantifying critical physiological processes including drought responses. Pressure chamber measurements of ψleaf (ψleafPC ) are most typical, yet, the practical complexity of the technique and of the underlying theory has led to ambiguous understanding of the conditions to optimize measurements. Consequently, specific techniques and precautions diversified across the global research community, raising questions of reliability and repeatability. Here, we surveyed specific methods of ψleafPC from multiple laboratories, and synthesized experiments testing common assumptions and practices in ψleafPC for diverse species: (i) the need for equilibration of previously transpiring leaves; (ii) leaf storage before measurement; (iii) the equilibration of ψleaf for leaves on bagged branches of a range of dehydration; (iv) the equilibration of ψleaf across the lamina for bagged leaves, and the accuracy of measuring leaves with artificially 'elongated petioles'; (v) the need in ψleaf measurements for bagging leaves and high humidity within the chamber; (vi) the need to avoid liquid water on leaf surfaces; (vii) the use of 'pulse' pressurization versus gradual pressurization; and (viii) variation among experimenters in ψleafPC determination. Based on our findings we provide a best practice protocol to maximise accuracy, and provide recommendations for ongoing species-specific tests of important assumptions in future studies.

The temperature optima for tree seedling photosynthesis and growth depend on water inputs.

Understanding how tree growth is affected by rising temperature is a key to predicting the fate of forests in future warmer climates. Increasing temperature has direct effects on plant physiology, but there are also indirect effects of increased water limitation because evaporative demand increases with temperature in many systems. In this study, we experimentally resolved the direct and indirect effects of temperature on the response of growth and photosynthesis of the widely distributed species Eucalyptus tereticornis. We grew E. tereticornis in an array of six growth temperatures from 18 to 35.5°C, spanning the climatic distribution of the species, with two watering treatments: (a) water inputs increasing with temperature to match plant demand at all temperatures (Wincr ), isolating the direct effect of temperature; and (b) water inputs constant for all temperatures, matching demand for coolest grown plants (Wconst ), such that water limitation increased with growth temperature. We found that constant water inputs resulted in a reduction of temperature optima for both photosynthesis and growth by ~3°C compared to increasing water inputs. Water limitation particularly reduced the total amount of leaf area displayed at Topt and intermediate growth temperatures. The reduction in photosynthesis could be attributed to lower leaf water potential and consequent stomatal closure. The reduction in growth was a result of decreased photosynthesis, reduced total leaf area display and a reduction in specific leaf area. Water availability had no effect on the response of stem and root respiration to warming, but we observed lower leaf respiration rates under constant water inputs compared to increasing water inputs at higher growth temperatures. Overall, this study demonstrates that the indirect effect of increasing water limitation strongly modifies the potential response of tree growth to rising global temperatures.

The partitioning of gross primary production for young Eucalyptus tereticornis trees under experimental warming and altered water availability.

The allocation of carbon (C) is an important component of tree physiology that influences growth and ecosystem C storage. Allocation is challenging to measure, and its sensitivity to environmental changes such as warming and altered water availability is uncertain. We exposed young Eucalyptus tereticornis trees to +3°C warming and elimination of summer precipitation in the field using whole-tree chambers. We calculated C allocation terms using detailed measurements of growth and continuous whole-crown CO2 and water exchange measurements. Trees grew from small saplings to nearly 9 m height during this 15-month experiment. Warming accelerated growth and leaf area development, and it increased the partitioning of gross primary production (GPP) to aboveground respiration and growth while decreasing partitioning below ground. Eliminating summer precipitation reduced C gain and growth but did not impact GPP partitioning. Trees utilized deep soil water and avoided strongly negative water potentials. Warming increased growth respiration, but maintenance respiration acclimated homeostatically. The increasing growth in the warmed treatment resulted in higher rates of respiration, even with complete acclimation of maintenance respiration. Warming-induced stimulations of tree growth likely involve increased C allocation above ground, particularly to leaf area development, whereas reduced water availability may not stimulate allocation to roots.

Range size and growth temperature influence Eucalyptus species responses to an experimental heatwave.

Understanding forest tree responses to climate warming and heatwaves is important for predicting changes in tree species diversity, forest C uptake, and vegetation-climate interactions. Yet, tree species differences in heatwave tolerance and their plasticity to growth temperature remain poorly understood. In this study, populations of four Eucalyptus species, two with large range sizes and two with comparatively small range sizes, were grown under two temperature treatments (cool and warm) before being exposed to an equivalent experimental heatwave. We tested whether the species with large and small range sizes differed in heatwave tolerance, and whether trees grown under warmer temperatures were more tolerant of heatwave conditions than trees grown under cooler temperatures. Visible heatwave damage was more common and severe in the species with small rather than large range sizes. In general, species that showed less tissue damage maintained higher stomatal conductance, lower leaf temperatures, larger increases in isoprene emissions, and less photosynthetic inhibition than species that showed more damage. Species exhibiting more severe visible damage had larger increases in heat shock proteins (HSPs) and respiratory thermotolerance (Tmax ). Thus, across species, increases in HSPs and Tmax were positively correlated, but inversely related to increases in isoprene emissions. Integration of leaf gas-exchange, isoprene emissions, proteomics, and respiratory thermotolerance measurements provided new insight into mechanisms underlying variability in tree species heatwave tolerance. Importantly, warm-grown seedlings were, surprisingly, more susceptible to heatwave damage than cool-grown seedlings, which could be associated with reduced enzyme concentrations in leaves. We conclude that species with restricted range sizes, along with trees growing under climate warming, may be more vulnerable to heatwaves of the future.

Trees tolerate an extreme heatwave via sustained transpirational cooling and increased leaf thermal tolerance.

Heatwaves are likely to increase in frequency and intensity with climate change, which may impair tree function and forest C uptake. However, we have little information regarding the impact of extreme heatwaves on the physiological performance of large trees in the field. Here, we grew Eucalyptus parramattensis trees for 1 year with experimental warming (+3°C) in a field setting, until they were greater than 6 m tall. We withheld irrigation for 1 month to dry the surface soils and then implemented an extreme heatwave treatment of 4 consecutive days with air temperatures exceeding 43°C, while monitoring whole-canopy exchange of CO2 and H2 O, leaf temperatures, leaf thermal tolerance, and leaf and branch hydraulic status. The heatwave reduced midday canopy photosynthesis to near zero but transpiration persisted, maintaining canopy cooling. A standard photosynthetic model was unable to capture the observed decoupling between photosynthesis and transpiration at high temperatures, suggesting that climate models may underestimate a moderating feedback of vegetation on heatwave intensity. The heatwave also triggered a rapid increase in leaf thermal tolerance, such that leaf temperatures observed during the heatwave were maintained within the thermal limits of leaf function. All responses were equivalent for trees with a prior history of ambient and warmed (+3°C) temperatures, indicating that climate warming conferred no added tolerance of heatwaves expected in the future. This coordinated physiological response utilizing latent cooling and adjustment of thermal thresholds has implications for tree tolerance of future climate extremes as well as model predictions of future heatwave intensity at landscape and global scales.

Traits and trade-offs in whole-tree hydraulic architecture along the vertical axis of Eucalyptus grandis.

Background and Aims: Sapwood traits like vessel diameter and intervessel pit characteristics play key roles in maintaining hydraulic integrity of trees. Surprisingly little is known about how sapwood traits covary with tree height and how such trait-based variation could affect the efficiency of water transport in tall trees. This study presents a detailed analysis of structural and functional traits along the vertical axes of tall Eucalyptus grandis trees. Methods: To assess a wide range of anatomical and physiological traits, light and electron microscopy was used, as well as field measurements of tree architecture, water use, stem water potential and leaf area distribution. Key Results: Strong apical dominance of water transport resulted in increased volumetric water supply per unit leaf area with tree height. This was realized by continued narrowing (from 250 to 20 µm) and an exponential increase in frequency (from 600 to 13 000 cm-2) of vessels towards the apex. The widest vessels were detected at least 4 m above the stem base, where they were associated with the thickest intervessel pit membranes. In addition, this study established the lower limit of pit membrane thickness in tall E. grandis at ~375 nm. This minimum thickness was maintained over a large distance in the upper stem, where vessel diameters continued to narrow. Conclusions: The analyses of xylem ultrastructure revealed complex, synchronized trait covariation and trade-offs with increasing height in E. grandis. Anatomical traits related to xylem vessels and those related to architecture of pit membranes were found to increase efficiency and apical dominance of water transport. This study underlines the importance of studying tree hydraulic functioning at organismal scale. Results presented here will improve understanding height-dependent structure-function patterns in tall trees.

Aridity drove the evolution of extreme embolism resistance and the radiation of conifer genus Callitris.

Xylem vulnerability to embolism is emerging as a major factor in drought-induced tree mortality events across the globe. However, we lack understanding of how and to what extent climate has shaped vascular properties or functions. We investigated the evolution of xylem hydraulic function and diversification patterns in Australia's most successful gymnosperm clade, Callitris, the world's most drought-resistant conifers. For all 23 species in this group, we measured embolism resistance (P50 ), xylem specific hydraulic conductivity (Ks ), wood density, and tracheary element size from natural populations. We investigated whether hydraulic traits variation linked with climate and the diversification of this clade using a time-calibrated phylogeny. Embolism resistance varied widely across the Callitris clade (P50 : -3.8 to -18.8 MPa), and was significantly related to water scarcity, as was tracheid diameter. We found no evidence of a safety-efficiency tradeoff; Ks and wood density were not related to rainfall. Callitris diversification coincides with the onset of aridity in Australia since the early Oligocene. Our results highlight the evolutionary lability of xylem traits with climate, and the leading role of aridity in the diversification of conifers. The uncoupling of safety from other xylem functions allowed Callitris to evolve extreme embolism resistance and diversify into xeric environments.

An empirical method that separates irreversible stem radial growth from bark water content changes in trees: theory and case studies.

Substantial uncertainty surrounds our knowledge of tree stem growth, with some of the most basic questions, such as when stem radial growth occurs through the daily cycle, still unanswered. We employed high-resolution point dendrometers, sap flow sensors, and developed theory and statistical approaches, to devise a novel method separating irreversible radial growth from elastic tension-driven and elastic osmotically driven changes in bark water content. We tested this method using data from five case study species. Experimental manipulations, namely a field irrigation experiment on Scots pine and a stem girdling experiment on red forest gum trees, were used to validate the theory. Time courses of stem radial growth following irrigation and stem girdling were consistent with a-priori predictions. Patterns of stem radial growth varied across case studies, with growth occurring during the day and/or night, consistent with the available literature. Importantly, our approach provides a valuable alternative to existing methods, as it can be approximated by a simple empirical interpolation routine that derives irreversible radial growth using standard regression techniques. Our novel method provides an improved understanding of the relative source-sink carbon dynamics of tree stems at a sub-daily time scale.

A common thermal niche among geographically diverse populations of the widely distributed tree species Eucalyptus tereticornis: No evidence for adaptation to climate-of-origin.

Impacts of climate warming depend on the degree to which plants are constrained by adaptation to their climate-of-origin or exhibit broad climatic suitability. We grew cool-origin, central and warm-origin provenances of Eucalyptus tereticornis in an array of common temperature environments from 18 to 35.5°C to determine if this widely distributed tree species consists of geographically contrasting provenances with differentiated and narrow thermal niches, or if provenances share a common thermal niche. The temperature responses of photosynthesis, respiration, and growth were equivalent across the three provenances, reflecting a common thermal niche despite a 2,200 km geographic distance and 13°C difference in mean annual temperature at seed origin. The temperature dependence of growth was primarily mediated by changes in leaf area per unit plant mass, photosynthesis, and whole-plant respiration. Thermal acclimation of leaf, stem, and root respiration moderated the increase in respiration with temperature, but acclimation was constrained at high temperatures. We conclude that this species consists of provenances that are not differentiated in their thermal responses, thus rejecting our hypothesis of adaptation to climate-of-origin and suggesting a shared thermal niche. In addition, growth declines with warming above the temperature optima were driven by reductions in whole-plant leaf area and increased respiratory carbon losses. The impacts of climate warming will nonetheless vary across the geographic range of this and other such species, depending primarily on each provenance's climate position on the temperature response curves for photosynthesis, respiration, and growth.

Climate determines vascular traits in the ecologically diverse genus Eucalyptus.

Current theory presumes that natural selection on vascular traits is controlled by a trade-off between efficiency and safety of hydraulic architecture. Hence, traits linked to efficiency, such as vessel diameter, should show biogeographic patterns; but critical tests of these predictions are rare, largely owing to confounding effects of environment, tree size and phylogeny. Using wood sampled from a phylogenetically constrained set of 28 Eucalyptus species, collected from a wide gradient of aridity across Australia, we show that hydraulic architecture reflects adaptive radiation of this genus in response to variation in climate. With increasing aridity, vessel diameters narrow, their frequency increases with a distribution that becomes gradually positively skewed and sapwood density increases while the theoretical hydraulic conductivity declines. Differences in these hydraulic traits appear largely genotypic in origin rather than environmentally plastic. Data reported here reflect long-term adaptation of hydraulic architecture to water availability. Rapidly changing climates, on the other hand, present significant challenges to the ability of eucalypts to adapt their vasculature.

Phloem as capacitor: radial transfer of water into xylem of tree stems occurs via symplastic transport in ray parenchyma.

The transfer of water from phloem into xylem is thought to mitigate increasing hydraulic tension in the vascular system of trees during the diel cycle of transpiration. Although a putative plant function, to date there is no direct evidence of such water transfer or the contributing pathways. Here, we trace the radial flow of water from the phloem into the xylem and investigate its diel variation. Introducing a fluorescent dye (0.1% [w/w] fluorescein) into the phloem water of the tree species Eucalyptus saligna allowed localization of the dye in phloem and xylem tissues using confocal laser scanning microscopy. Our results show that the majority of water transferred between the two tissues is facilitated via the symplast of horizontal ray parenchyma cells. The method also permitted assessment of the radial transfer of water during the diel cycle, where changes in water potential gradients between phloem and xylem determine the extent and direction of radial transfer. When injected during the morning, when xylem water potential rapidly declined, fluorescein was translocated, on average, farther into mature xylem (447 ± 188 µm) compared with nighttime, when xylem water potential was close to zero (155 ± 42 µm). These findings provide empirical evidence to support theoretical predictions of the role of phloem-xylem water transfer in the hydraulic functioning of plants. This method enables investigation of the role of phloem tissue as a dynamic capacitor for water storage and transfer and its contribution toward the maintenance of the functional integrity of xylem in trees.

Toward an index of desiccation time to tree mortality under drought.

Research in plant hydraulics has provided important insights into plant responses to drought and species absolute drought tolerance. However, our ability to predict when plants will die from hydraulic failure under extreme drought is limited by a lack of knowledge with regards to the dynamics of plant desiccation following stomatal closure. Thus, we develop a simple hydraulics model based on branch-level traits that incorporates key aspects of allometry, rates of water loss and resistance to embolism thresholds in order to define species differences in the time it takes plants to desiccate from stomatal closure to lethal levels of drought stress.

Vessel diameter and related hydraulic traits of 31 Eucalyptus species arrayed along a gradient of water availability.

We present two comprehensive data sets that describe xylem vessel diameters and related sapwood traits for species of Eucalyptus from arid and semi-arid woodlands and forests in Australia. Between 2009 and 2014, sapwood of mature trees was sampled in south-western, south-eastern and eastern Australia. One additional species was sampled from tropical north-western Australia. The first data set describes samples collected from the basal stem section (130 cm above ground) of three individuals of 31 species of which eight species were replicated at sites that differed in climatic conditions. The second data set describes vessel characteristics of three trees from each of 10 species that were sampled at 8 m below the tree apex. The sampled trees of these 10 species are also part of the first data set. In total, we report diameters (D) for over 25 100 vessels, from 494 digital images taken from 117 trees. We also report vessel frequencies, void-to-wood ratios, sapwood densities and hydraulically weighted vessel diameters (Dh). Supporting data of the first data set include tree diameter at breast height (130 cm above ground), tree height, sample locations, and summary climate data. In this data set, diameter of individual vessels ranges from 10 to over 300 µm, and vessel frequency from 360 to 9070 vessels cm-2 . Wood density ranges from 0.47 to 0.96 g cm-3 . Void-to-wood ratio ranges from 6% to 27% and Dh ranges from 46 to 236 µm. Mean annual rainfall (P) at sample sites ranges from 246 to 2274 mm and FAO56 reference evaporation (E) from 777 to 2110 mm. The aridity index (E/P) ranges from 0.15 to 2.93 (dimensionless). Tree diameters range from 9 to 90 cm and tree heights range from 6 to 70 m. D and Dh in the second data set range from 11 to 271 and 68 to 205 µm, respectively. These datasets will make a valuable contribution to future continental-scale and global-scale studies of the relationship between xylem hydraulic architecture and climate. The data sets are unique in the sense that they are phylogenetically constrained, allowing in-depth assessment of plasticity of hydraulic attributes within a single tree genus.

The capacity to cope with climate warming declines from temperate to tropical latitudes in two widely distributed Eucalyptus species.

As rapid climate warming creates a mismatch between forest trees and their home environment, the ability of trees to cope with warming depends on their capacity to physiologically adjust to higher temperatures. In widespread species, individual trees in cooler home climates are hypothesized to more successfully acclimate to warming than their counterparts in warmer climates that may approach thermal limits. We tested this prediction with a climate-shift experiment in widely distributed Eucalyptus tereticornis and E. grandis using provenances originating along a ~2500 km latitudinal transect (15.5-38.0°S) in eastern Australia. We grew 21 provenances in conditions approximating summer temperatures at seed origin and warmed temperatures (+3.5 °C) using a series of climate-controlled glasshouse bays. The effects of +3.5 °C warming strongly depended on home climate. Cool-origin provenances responded to warming through an increase in photosynthetic capacity and total leaf area, leading to enhanced growth of 20-60%. Warm-origin provenances, however, responded to warming through a reduction in photosynthetic capacity and total leaf area, leading to reduced growth of approximately 10%. These results suggest that there is predictable intraspecific variation in the capacity of trees to respond to warming; cool-origin taxa are likely to benefit from warming, while warm-origin taxa may be negatively affected.

Stomatal structure and physiology do not explain differences in water use among montane eucalypts.

Understanding the regulation of water use at the whole-tree scale is critical to advancing the utility of physiological ecology, for example in its role in predictive hydrology of forested catchments. For three eucalypt species that dominate high-elevation catchments in south-eastern Australia, we examined if whole-tree water use could be related to three widely discussed regulators of water use: stomatal anatomy, sensitivity of stomata [i.e. stomatal conductance (g(s))] to environmental influences, and sapwood area. While daily tree water use varied sixfold among species, sap velocity and sapwood area varied in parallel. Combined, stomatal structure and physiology could not explain differences in species-specific water use. Species which exhibited the fastest (Eucalyptus delegatensis) and slowest (Eucalyptus pauciflora) rates of water use both exhibited greater capacity for physiological control of g(s) [indicated by sensitivity to vapour pressure deficit (VPD)] and a reduced capacity to limit g(s) anatomically [indicated by greater potential g(s) (g(max))]. Conversely, g(s) was insensitive to VPD and g(max) was lowest for Eucalyptus radiata, the species showing intermediate rates of water use. Improved knowledge of stomatal anatomy will help us to understand the capacity of species to regulate leaf-level water loss, but seems likely to remain of limited use for explaining rates of whole-tree water use in montane eucalypts at the catchment scale.

Woody clockworks: circadian regulation of night-time water use in Eucalyptus globulus.

The role of the circadian clock in controlling the metabolism of entire trees has seldom been considered. We tested whether the clock influences nocturnal whole-tree water use. Whole-tree chambers allowed the control of environmental variables (temperature, relative humidity). Night-time stomatal conductance (gs ) and sap flow (Q) were monitored in 6- to 8-m-tall Eucalyptus globulus trees during nights when environmental variables were kept constant, and also when conditions varied with time. Artificial neural networks were used to quantify the relative importance of circadian regulation of gs and Q. Under a constant environment, gs and Q declined from 0 to 6 h after dusk, but increased from 6 to 12 h after dusk. While the initial decline could be attributed to multiple processes, the subsequent increase is most consistent with circadian regulation of gs and Q. We conclude that endogenous regulation of gs is an important driver of night-time Q under natural environmental variability. The proportion of nocturnal Q variation associated with circadian regulation (23-56%) was comparable to that attributed to vapor pressure deficit variation (25-58%). This study contributes to our understanding of the linkages between molecular and cellular processes related to circadian regulation, and whole-tree processes related to ecosystem gas exchange in the field.

Water flux of Eucalyptus regnans: defying summer drought and a record heatwave in 2009.

Making predictions as to how heatwaves will affect forests in the future is a major challenge in ecosystem science, not the least because we have few documented examples of how they respond now. We captured the effects of drought and a record-breaking heatwave on whole-tree water use (Q) in Eucalyptus regnans during the summer drought of 2008/2009 in southeastern Australia. While air temperatures steadily increased, average maximum sap flow (J Smax) declined with progression of the drought prior to the heatwave. In the period approaching the heatwave, Q during daytime (Q d) steadily declined, while nighttime Q (Q n) increased. This pattern was particularly pronounced during nights that followed hot days (>32 °C) where Q n was frequently 20-30 % of Q d. We found clear trends in the relation of Q d to Q n that point to the increasing importance of refilling depleted stem water stores following hot days. On the day the heatwave climaxed (7 February 2009), sap flow (J S) was dramatically low, and declined as weather conditions became increasingly arid (air temperature > 42 °C, vapor pressure deficit >7 kPa). Almost immediately after the heatwave passed J S resumed its common diurnal hysteresis, albeit at slightly slower rates. In the context of prognosticated effects of future climate, our data highlight that depletion and refill of stored water in E. regnans are likely important features for the tree to endure drought- and heat-related climatic extremes. We suggest that elucidating the peculiarity of capacitance and defining its threshold for keystone tree species, such as E. regnans, can add to our understanding of how climatic extremes may affect forests.

Site-specific responses to short-term environmental variation are reflected in leaf and phloem-sap carbon isotopic abundance of field grown Eucalyptus globulus.

The carbon isotopic composition (δ(13) C) of plant material has been used extensively as an indirect measure of carbon fixation per volume of water used. More recently, the δ(13) C of phloem sap (δ(13) C(phl) ) has been used as a surrogate measure of short-term, canopy scale δ(13) C. Using a combination of δ(13) C physiological, structural and chemical indices from leaves and phloem sap of Eucalyptus globulus at sites of contrasting water availability, we sought to identify short-term, canopy scale resource limitations. Results illustrate that δ(13) C(phl) offers valid reflections of short-term, canopy scale values of leaf δ(13) C and tree water status. Under conditions limited by water, leaf and phloem sap photoassimilates differ in (13) C abundance of a magnitude large enough to significantly influence predictions of water use efficiency. This pattern was not detected among trees with adequate water supply indicating fractionation into heterotrophic tissues that may be sensitive to plant water status. Trees employed a range of physiological, biochemical and structural adaptations to acclimate to resource limitation that differed among sites providing a useful context upon which to interpret patterns in δ(13) C. Our results highlight that such easily characterized properties are ideal for use as minimally invasive tools to monitor growth and resilience of plants to variations in resource availability.

The relationship between tree size and tree water-use: is competition for water size-symmetric or size-asymmetric?

Relationships between tree size and water use indicate how soil water is partitioned between differently sized individuals, and hence competition for water. These relationships are rarely examined, let alone whether there is consistency in shape across populations. Competition for water among plants is often assumed to be size-symmetric, i.e., exponents (b1) of power functions (water use ∝ biomassb1) equal to 1, with all sizes using the same amount of water proportionally to their size. We tested the hypothesis that b1 actually varies greatly, and based on allometric theory, that b1 is only centered around 1 when size is quantified as basal area or sapwood area (not diameter). We also examined whether b1 varies spatially and temporally in relation to stand structure (height and density) and climate. Tree water use ∝ sizeb1 power functions were fitted for 80 species and 103 sites using the global SAPFLUXNET database. The b1 were centered around 1 when tree size was given as basal area or sapwood area, but not as diameter. The 95% confidence intervals of b1 included the theoretical predictions for the scaling of plant vascular networks. b1 changed through time within a given stand for the species with the longest time series, such that larger trees gained an advantage during warmer and wetter conditions. Spatial comparisons across the entire dataset showed that b1 correlated only weakly (R2 < 12%) with stand structure or climate, suggesting that inter-specific variability in b1 and hence the symmetry of competition for water may be largely related to inter-specific differences in tree architecture or physiology rather than to climate or stand structure. In conclusion, size-symmetric competition for water (b1 ≈ 1) may only be assumed when size is quantified as basal area or sapwood area, and when describing a general pattern across forest types and species. There is substantial deviation in b1 between individual stands and species.