1. Introduction
Predicted increases in extremes such as drought events and heat waves, in conjunction with long-term changes in water availability (increasing or decreasing) and temperature regimes (increasing) will potentially drive significant changes in forest productivity. Successful management of existing or new forests to deliver a range of commodities and environmental services under these conditions must include careful consideration of species capacity to absorb future climatic disturbances and adapt to future climate regimes. This requires a deeper understanding of the role of ecophysiological traits in enabling adaptation of species and genotypes to high temperature and water deficit.
Adaptation to water deficit can be defined in relation to mechanisms that control leaf water status and cell turgor [
1]. Maintenance of leaf turgor is critical to the continuance of growth and gas exchange in the face of declining water availability [
2,
3,
4]. The water potential at zero turgor or turgor loss point (π
tlp) and the corresponding relative water content helps to define the operating water potentials over which plants actively regulate water status and is often lower in species with greater dehydration tolerance [
1,
5]. Plants actively accumulate solutes in order to lower their osmotic potential during water deficit, thereby sustaining turgor and prolonging water uptake [
6]. Similarly, leaves with highly elastic tissues reduce steep declines in cell turgor because their cells contain more water at full turgor and can sustain larger declines in volume [
1]. Pressure-volume relationships are routinely used to estimate these key parameters of leaf physiology [
7] and are often interpreted as indicators of species drought tolerance
i.e., the ability to maintain physiological function at low water status [
8,
9].
A large body of work has documented the significance of leaf turgor maintenance traits that enable survival and growth under a range of habitats and climates (see [
10] and references therein). The water potential corresponding to zero turgor has been shown to be similar to the point at which stomata close as evidenced by studies involving four tropical [
11] and three temperate species [
12] and represents an important trait in defining plant hydraulic strategies [
13]. Global analyses show that π
tlp can vary 3-fold between crop and native arid-land species and lower π
tlp appears to be associated with drier environments [
10]. These leaf water relations traits have also been shown to correlate with leaf structural attributes in dry [
14] and wet habitats [
15], indicating either a direct functional link between leaf water management and leaf construction or co-selection for structural and physiological leaf traits. Differences in the ability of species to access and manage water within a particular habitat,
i.e., their ecohydrologic niche, also drives a significant amount of variation in species responses to water deficit and associated traits such as π
tlp. While meta-analyses by Bartlett
et al. [
10] demonstrated a decline in π
tlp with increasing aridity across different biomes, it is unclear how the relative contribution of climatic water availability (across a species climatic envelope) as opposed to local habitat factors and species water management strategies influence patterns in leaf water relations, specifically π
tlp. Assessing the significance of both climatic and habitat water availability in driving variation in π
tlp may help to clarify role of turgor maintenance in defining species distributions at both the landscape and regional scales.
Until recently, the influence of functional traits such as π
tlp on species distributional limits has been unclear and species distribution modelling has relied predominately on the known presence and/or absence of species based observations of their occurrence [
16]. The inclusion of definitive functional attributes that can link a species climatic niche back to relevant physiological or ecological thresholds offers much promise in better utilising the rapidly improving species databases and high resolution climate data. This may be achieved by gaining a better understanding of how particular traits or clusters of traits control plant performance and survival under stressful (or non-stressful) conditions and how these traits vary within and between species with respect to their observed climatic envelope and their ability to access and regulate water within the landscape. In the context of water deficit and heat stress, such analyses would help clarify the extent to which a trait plays an adaptive role in defining species distribution and vegetation function. This information will assist in characterising species sensitivity within existing and new environments, making it possible to quantify the likely impact associated with exposure from future climates.
Australia is a predominately water-limited environment and its vegetation has been shaped by water availability [
17,
18]. The long history of water relations research in Australia provides a unique data resource and opportunity to test the adaptive significance of leaf water relations traits across well delineated aridity and temperature gradients. This study tests the hypothesis that π
tlp is a key adaptation to water stress and lower values of π
tlp enable survival in drier and warmer environments. Specifically, we addressed the following questions: (1) Which climatic indices, derived from a species observed climatic niche (including the middle and tail regions of this distribution), are more closely associated with variation in π
tlp among Australian species? (2) What is the significance of species habitat water availability or ecohydrologic niche and associated leaf water relations traits in modulating adaptation to drier and warmer climates?
4. Discussion
We compiled a database of species leaf water relations that spanned almost 50 years of plant water relations research in Australia and covered a considerable range of vegetation and plant functional types across the Australian continent. In this study, key climatic indices were extracted from different middle and tail regions of species climatic envelopes in order to assess the role of aridity and high temperature as selection pressures on leaf water relations among a large group of species (n = 174). By also evaluating the influence of habitat water availability across these climatic gradients, our study builds on a growing body of work that links key functional traits to a species habitat and climatic range and strengthens efforts to predict shifts in forest distribution and function under a changing climate.
A significant proportion of the variability in π
tlp was explained by climatic indices based on precipitation (MAP) or climatic water deficit (MAPD). This observation supports the finding of Bartlett
et al. [
10,
23] and others [
25] that π
tlp is an adaptive trait whereby a lower π
tlp allows species to tolerate increased aridity in terms of lower precipitation and/or increased evaporative demand. Furthermore, the relationship between π
tlp and MAPD was also maintained among the eucalypt spp. (
n = 47) in the database, supporting the suggestion that turgor maintenance traits explain much of the distribution of the dominant genus in forests across Australia [
26]. However, our study furthers our understanding of leaf physiological adaptations to climate by showing a significant interaction between maximum temperature (MHMT) and MAP in influencing variation in leaf turgor maintenance (
R2 = 0.35). This result indicates an important role for high temperature in modulating π
tlp among species. There is likely to be strong selection for low π
tlp in dry climates with high summer temperatures given the potential for additional heat stress if turgor loss triggers stomatal closure. High temperature stress is amplified under water stress when leaf cooling via transpiration ceases after stomatal closure [
27]. This could trigger leaf or whole-tree mortality if leaf temperatures exceed ambient air temperatures and reach critical temperatures for maintaining cell function [
28,
29]. It remains to be tested whether π
tlp also co-varies with those leaf traits associated with resistance to high temperature stress. These data support recent studies that highlight the strong interaction of drought and high temperature stress in affecting tree functioning and survival in Australia [
21] and globally [
30]. Our findings demonstrate a role of both aridity and high temperature in controlling leaf water relations and π
tlp presumably because conditions of high evaporative demand and high temperature exert strong selection pressure on species to adequately regulate their physiology over a given range of leaf water potentials and temperatures.
In general, the inclusion of climate indices based on the dry tails of the species distribution (e.g., MAP and MAPD) did not strengthen the relationship between climatic indices and π
tlp, compared to climate indices derived from the median (
Table 1). It is likely that these climate-trait relationships are maintained at both parts of the distribution because values derived from the median scale linearly with those at the dry or warm tail of the distribution.
This study also elucidates the role of species habitat water availability and water management strategy, in addition to species climatic envelope in driving species leaf water relations. Species that experience lower Ψ
md (and lower Ψ
pd) tended to have lower π
tlp, particularly for those species from more arid environments. Variation in habitat water availability is also reflected in the larger dispersion in π
tlp at observed in MAPD between −50 to −150 mm (
Figure 2). This suggests that increasing aridity drives greater selection pressure for different strategies to exploit a wider range of potential water sources and ecohydrologic niches [
31]. Regulation of water use must also closely align with spatial and temporal patterns in water availability thereby promoting strong divergence in water status, particularly during dry periods [
32]. The tendency for larger trait variation in drier climates is consistent with other drought trait databases such as the global analysis of stem embolism resistance (defined using the water potential at 50 percent loss of hydraulic conductivity), that shows increasing trait variation with climatic water availability [
33]. In this study, climatic water deficit explained only ~ 30% of the variation in π
TLP. These patterns among drought resistance traits indicate the significance of contrasting water management strategies that may diminish the importance of a single trait π
tlp in enabling survival under water deficit. Hence, at the whole plant level, species responses to increasing aridity involves the coordination of multiple traits and provide differential responses to drought and rates of recovery following drought.
Shifts in turgor maintenance are a good example of how alternative strategies may bring about similar outcomes for tolerating low water availability. Osmotic adjustment is widely evaluated in order to compare drought tolerance among differing species and genotypes [
23], however elastic adjustment or increased elasticity (lower ε) can potentially buffer against steep declines in water status [
5,
34]. The relatively weak relationship we observed between differential modes of turgor maintenance; osmotic adjustment and bulk tissue elasticity
versus aridity suggests no consistent shift in determinants of leaf turgor. The negative relationship between π
0 and ε is consistent with the trade-off observed among many species exhibiting either lower elasticity or osmotic potential (less negative) or higher elasticity and osmotic potential [
10,
25,
35]. This trade-off probably originates from a biophysical requirement of tissues and cells to either accumulate solutes accompanied by a decrease in elasticity to avoid cell rupture or increased elasticity without having to incur the cost of producing compatible solutes [
35]. Several studies in dry climates show strong divergence in turgor maintenance patterns among sympatric or closely related species that confer resistance to water deficit [
13,
35,
36].
Intra-specific variation in π
tlp may also drive adaptation across the species distribution. Evidence for systematic variation in π
tlp under well-watered conditions is limited in woody species and most studies included in the database showed non-significant differences in π
tlp among genotypes [
37,
38,
39], whereas variation among genotypes tends to occur in response to seasonal or short-term water deficit suggesting plasticity in ability to adjust π
tlp among genotypes [
39,
40]. Nevertheless patterns in π
tlp presented here would suggest that single parameters of species climatic envelope and corresponding mean trait value provide a fairly robust indication of inter-specific patterns in adaptation to aridity.
5. Conclusions
We showed that among the 174 woody species for which there were data for π
tlp, a large proportion of the variability in π
tlp could be explained by mean annual precipitation or climatic water deficit (precipitation deficit). While similar biome and species-level patterns in π
tlp has been demonstrated in global meta-analyses that considered species aridity values from the study site [
10,
23], our study also confirmed the significance of an interaction between hottest monthly maximum temperature with climatic water availability. This provides evidence for strong selective pressure from both water deficit and high temperature in defining physiological strategies among Australian species. Furthermore, habitat water availability and plant water management patterns as reflected by differences in midday leaf water potential was a slightly better predictor of π
tlp across these gradients in aridity, highlighting the fundamental importance of these factors, in addition to the prevailing climatic conditions, in modulating the operating range over which plants may actively sustain turgor. Further research is required to examine the relationship between turgor maintenance parameters and other traits known to exert strong controls on plant performance under water deficit across a broad range of species, e.g., leaf hydraulic conductance. This study suggests that π
tlp plays a central role in defining plant performance and could be incorporated in species distribution modelling given its responsiveness to climatic and site-based drivers in water availability.