Chris J. Blackman

Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms

Hydraulic dysfunction in leaves determines key aspects of whole-plant responses to water stress; however, our understanding of the physiology of hydraulic dysfunction and its relationships to leaf structure and ecological strategy remains incomplete. Here, we studied a morphologically and ecologically diverse sample of angiosperms to test whether the water potential inducing a 50% loss in leaf hydraulic conductance (P50(leaf)) is predicted by properties of leaf xylem relating to water tension-induced conduit collapse. We also assessed the relationships between P50(leaf) and other traits considered to reflect drought resistance and ecological strategy. Across species, P50(leaf) was strongly correlated with a theoretical predictor of vulnerability to cell collapse in minor veins (the cubed ratio of the conduit wall thickness to the conduit lumen breadth). P50(leaf) was also correlated with mesophyll traits known to be related to drought resistance, but unrelated to traits associated with carbon economy. Our data indicate a link between the structural mechanics of leaf xylem and hydraulic function under water stress. Although it is possible that collapse may contribute directly to dysfunction, this relationship may also be a secondary product of vascular economics, suggesting that leaf xylem is dimensioned to avoid wall collapse.

Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species

Efficient conduction of water inside leaves is essential for leaf function, yet the hydraulic-mediated impact of drought on gas exchange remains poorly understood. Here we examine the decline and subsequent recovery of leaf water potential (Psi(leaf)), leaf hydraulic conductance (K(leaf)), and midday transpiration (E) in four temperate woody species exposed to controlled drought conditions ranging from mild to lethal. During drought the vulnerability of K(leaf) to declining Psi(leaf) varied greatly among the species sampled. Following drought, plants were rewatered and the rate of E and K(leaf) recovery was found to be strongly dependent on the severity of the drought imposed. Gas exchange recovery was strongly correlated with the relatively slow recovery of K(leaf) for three of the four species, indicating conformity to a hydraulic-stomatal limitation model of plant recovery. However, there was also a shift in the sensitivity of stomata to Psi(leaf) suggesting that the plant hormone abscisic acid may be involved in limiting the rate of stomatal reopening. The level of drought tolerance varied among the four species and was correlated with leaf hydraulic vulnerability. These results suggest that species-specific variation in hydraulic properties plays a fundamental role in steering the dynamic response of plants during recovery.

Two measures of leaf capacitance: insights into the water transport pathway and hydraulic conductance in leaves

The efficiency and stress tolerance of leaf water transport are key indicators of plant function, but our ability to assess these processes is constrained by gaps in our understanding of the water transport pathway in leaves. A major challenge is to understand how different pools of water in leaves are connected to the transpiration stream and, hence, determine leaf capacitance (Cleaf) to short- and medium-term fluctuations in transpiration. Here, we examine variation across an anatomically and phylogenetically diverse group of woody angiosperms in two measures of Cleaf assumed to represent bulk-leaf capacitance (Cbulk) and the capacitance of leaf tissues that influence dynamic changes in leaf hydration (Cdyn). Among species, Cbulk was significantly correlated with leaf mass per unit area, whereas Cdyn was independently related to leaf lignin content (%) and the saturated mass of leaf water per unit dry weight. Dynamic and steady-state measurements of leaf hydraulic conductance (Kleaf) agreed if Cdyn was used rather than Cbulk, suggesting that the leaf tissue in some species is hydraulically compartmentalised and that only a proportion of total leaf water is hydraulically well connected to the transpiration stream. These results indicate that leaf rehydration kinetics can accurately measure Kleaf with knowledge of the capacitance of the hydraulic pathway.

Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms

The ability of plants to maintain water flow through leaves under water stress-induced tension (assessed as the leaf hydraulic vulnerability; P50leaf) is intimately linked with survival. We examined the significance of P50leaf as an adaptive trait in influencing the dry-end distributional limits of cool temperate woody angiosperm species. We also examined differences in within-site variability in P50leaf between two high-rainfall montane rainforest sites in Tasmania and Peru, respectively. A significant relationship between P50leaf and the 5th percentile of mean annual rainfall across each species distribution was found in Tasmania, suggesting that P50leaf influences species climatic limits. Furthermore, a strong correlation between P50leaf and the minimum rainfall availability was found using five phylogenetically independent species pairs in wet and dry evergreen tree species, suggesting that rainfall is an important selective agent in the evolution of leaf hydraulic vulnerability. Greater within-site variability in P50leaf was found among dominant montane rainforest species in Tasmania than in Peru and this result is discussed within the context of differences in spatial and temporal environmental heterogeneity and parochial historical ecology.

An ecoclimatic framework for evaluating the resilience of vegetation to water deficit

The surge in global efforts to understand the causes and consequences of drought on forest ecosystems has tended to focus on specific impacts such as mortality. We propose an ecoclimatic framework that takes a broader view of the ecological relevance of water deficits, linking elements of exposure and resilience to cumulative impacts on a range of ecosystem processes. This ecoclimatic framework is underpinned by two hypotheses: (i) exposure to water deficit can be represented probabilistically and used to estimate exposure thresholds across different vegetation types or ecosystems; and (ii) the cumulative impact of a series of water deficit events is defined by attributes governing the resistance and recovery of the affected processes. We present case studies comprising Pinus edulis and Eucalyptus globulus, tree species with contrasting ecological strategies, which demonstrate how links between exposure and resilience can be examined within our proposed framework. These examples reveal how climatic thresholds can be defined along a continuum of vegetation functional responses to water deficit regimes. The strength of this framework lies in identifying climatic thresholds on vegetation function in the absence of more complete mechanistic understanding, thereby guiding the formulation, application and benchmarking of more detailed modelling.

Climate drives vein anatomy in Proteaceae

PREMISE OF STUDY The mechanisms by which plants tolerate water deficit are only just becoming clear. One key factor in drought tolerance is the ability to maintain the capacity to conduct water through the leaves in conditions of water stress. Recent work has shown that a simple feature of the leaf xylem cells, the cube of the thickness of cell walls divided by the lumen width (t/b)(3), is strongly correlated with this ability. METHODS Using ecologically, phylogenetically, and anatomically diverse members of Proteaceae, we tested the relationships between (t/b)(3) and climate, leaf mass per unit area, leaf area, and vein density. To test relationships at high phylogenetic levels (mostly genus), we used phylogenetic and nonphylogenetic single and multiple regressions based on data from 50 species. We also used 14 within-genus species pairs to test for relationships at lower phylogenetic levels. KEY RESULTS All analyses revealed that climate, especially mean annual precipitation, was the best predictor of (t/b)(3). The variation in (t/b)(3) was driven by variation in both lumen diameter and wall thickness, implying active control of these dimensions. Total vein density was weakly related to (t/b)(3) but unrelated to either leaf area or climate. CONCLUSIONS We conclude that xylem reinforcement is a fundamental adaptation for water stress tolerance and, among evergreen woody plants, drives a strong association between rainfall and xylem anatomy. The strong association between (t/b)(3) and climate cannot be explained by autocorrelation with other aspects of leaf form and anatomy that vary along precipitation gradients.

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.

Whole-plant capacitance, embolism resistance and slow transpiration rates all contribute to longer desiccation times in woody angiosperms from arid and wet habitats

Low water potentials in xylem can result in damaging levels of cavitation, yet little is understood about which hydraulic traits have most influence in delaying the onset of hydraulic dysfunction during periods of drought. We examined three traits contributing to longer desiccation times in excised shoots of 11 species from two sites of contrasting aridity: (i) the amount of water released from plant tissues per decrease in xylem water potential (WΨ); (ii) the minimum xylem water potential preceding acute water stress (defined as P50L; water potential at 50% loss of leaf conductance); and (iii) the integrated transpiration rate between the points of full hydration and P50L (Wtime). The time required for species to reach P50L varied markedly, ranging from 1.3 h to nearly 3 days. WΨ, P50L and Wtime all contributed significantly to longer desiccation times, explaining 28, 22 and 50% of the variance in the time required to reach P50L. Interestingly, these three traits were nearly orthogonal to one another, suggesting that they do not represent alternative hydraulic strategies, but likely trade off with other ecological strategies not evaluated in this study. The majority of water lost during desiccation (60-91%) originated from leaves, suggesting an important role for leaf capacitance in small plants when xylem water potentials decrease below -2 MPa.

Leaf photosynthetic, economics and hydraulic traits are decoupled among genotypes of a widespread species of eucalypt grown under ambient and elevated CO2

Summary Leaf economics and hydraulic traits strongly influence photosynthesis. While the level of coordination among these traits can differ between sets of species, leaf functional trait coordination within species remains poorly understood. Furthermore, elevated concentrations of atmospheric CO2 commonly influence the expression of leaf photosynthetic, economics and hydraulic traits in contrasting ways, yet the effect of variable concentrations of atmospheric CO2 on patterns of trait coordination within species remains largely untested. We examined the relationships among key leaf photosynthetic (e.g. net photosynthesis and photosynthetic biochemistry), economics and water-use (e.g. leaf mass per unit area and stomatal conductance) and hydraulic traits (e.g. vein density) in 14 genotypes of Eucalyptus camaldulensis grown in ambient (aCO2) and elevated (eCO2) [CO2]. We examined the level of coordination among leaf traits in aCO2 and then assessed whether growth in eCO2 altered that coordination. We found that leaf traits related to photosynthetic capacity, economics and water-use, and hydraulics were decoupled among genotypes grown in aCO2, yet strong relationships were generally observed among suites of traits within each ‘functional group’. Significant responses to growth in eCO2 were observed for most leaf photosynthetic and economics and water-use traits, with the magnitude and direction of the response varying among traits. In contrast, leaf hydraulics traits were unaffected by variable growth CO2. Despite this, growth in eCO2 did not substantially alter patterns of leaf trait coordination observed in aCO2. These results suggest suites of leaf traits associated with photosynthetic capacity, economics and water-use and hydraulics, respectively, can form independent axes of variation among genotypes of a single species, regardless of growth CO2. Although growth in eCO2 did not substantially alter patterns of trait coordination, decoupling of leaf functional traits among genotypes may allow genetically distinct populations to produce novel combinations of traits that may be adaptive in response to changes in their local environment.

Weak coordination among petiole, leaf, vein, and gas-exchange traits across Australian angiosperm species and its possible implications

Abstract Close coordination between leaf gas exchange and maximal hydraulic supply has been reported across diverse plant life forms. However, it has also been suggested that this relationship may become weak or break down completely within the angiosperms. We examined coordination between hydraulic, leaf vein, and gas‐exchange traits across a diverse group of 35 evergreen Australian angiosperms, spanning a large range in leaf structure and habitat. Leaf‐specific conductance was calculated from petiole vessel anatomy and was also measured directly using the rehydration technique. Leaf vein density (thought to be a determinant of gas exchange rate), maximal stomatal conductance, and net CO 2 assimilation rate were also measured for most species (n = 19–35). Vein density was not correlated with leaf‐specific conductance (either calculated or measured), stomatal conductance, nor maximal net CO 2 assimilation, with r 2 values ranging from 0.00 to 0.11, P values from 0.909 to 0.102, and n values from 19 to 35 in all cases. Leaf‐specific conductance calculated from petiole anatomy was weakly correlated with maximal stomatal conductance (r 2 = 0.16; P = 0.022; n = 32), whereas the direct measurement of leaf‐specific conductance was weakly correlated with net maximal CO 2 assimilation (r 2 = 0.21; P = 0.005; n = 35). Calculated leaf‐specific conductance, xylem ultrastructure, and leaf vein density do not appear to be reliable proxy traits for assessing differences in rates of gas exchange or growth across diverse sets of evergreen angiosperms.