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One of the fundamental problems all plants face is acquiring and transporting water from the soil to the leaves, to replace water lost to the atmosphere during photosynthesis. This continuous column of water can come under tension as a result of low water availability at the roots or high evaporative demand at the leaf; thus dry soil or dry air compounds the challenge of water transport. Our understanding of the hydraulic traits that contribute to plant water relations has been greatly enhanced by research in mediterranean-type environments (MTEs). Because of the annual period of low rainfall characteristic of the MTE climate, the role of soil drought in particular has been the focus of many studies. A suite of covarying physiological and anatomical traits have been identified that describe the diversity of hydraulic strategies within these communities (e.g. Martinez-Vilalta et al., 2002; Filella & Penuelas, 2003; Ackerly, 2004b; Jacobsen et al., 2007). Much of this variation is associated with differences in minimum seasonal water potential; species that experience greater water deficit, as a result of shallow rooting or other factors, tend to have higher wood density, more drought-resistant xylem, and associated traits.
The occurrence of morphologically similar shrub vegetation in semiarid but nonMTE climates provides an opportunity to examine more closely the adaptive significance of traits governing plant water use. In California, chaparral shrubs experience a MTE of high summer temperatures and high vapor pressure deficit (VPD) during the annual period of soil water deficit. By contrast, vegetation in central Mexico experiences a summer rain regime; accordingly, the annual period of soil water deficit coincides with cooler, winter months (Valiente-Banuet et al., 1998). Comparisons between these two communities provide an opportunity to examine the consequences of the seasonal timing of soil drought. Those traits that are shared between these communities may be adaptive in seasonally dry environments in general, and not specific to the unique MTE climate type (Valiente-Banuet et al., 1998); those that differ provide insight into how the timing of soil drought, and specifically its interaction with atmospheric drought, influences plant hydraulic function.
A comparison of dry-season hydraulic strategies between a chaparral community in Santa Barbara, California, and a Mexican shrub community (‘mexical’) in Tehuacan revealed a strong correlation between species hydraulic capacity and the extent of drought experienced: within each site, species with lower whole-plant hydraulic conductance experienced more negative minimum seasonal water potential. However, while the slope of this functional relationship was similar, there was a significant shift in the elevation of the relationship between sites: whole-plant hydraulic conductance was higher in Santa Barbara relative to Tehuacan at a given minimum seasonal water potential (Bhaskar, 2006). Higher whole-plant conductance in Santa Barbara may be part of a hydraulic strategy to allow maintenance of gas exchange under the confluence of both high VPD and high soil water deficit. Under higher evaporative demand, greater water transport to the leaves may be required to prevent excessive diurnal and seasonal declines in leaf water potential (Maherali & DeLucia, 2000, 2001;Addington et al., 2006).
If the MTE climate, with simultaneous atmospheric and soil droughts, imposes a selective pressure for higher leaf hydraulic supply, the differences observed at the community level should also be reflected in evolutionary divergences between related species across this climate contrast. Here we studied patterns of hydraulic trait evolution in all available pairs of closely related species between these taxonomically similar shrub communities (see Valiente-Banuet et al., 1998). Each pair represents an independent divergence into the contrasting environments, and thus we can compare the magnitude and direction of differences in a particular trait across all species pairs in relation to climate as well as to other traits (Felsenstein, 1985).
This paper addresses two objectives. Our first goal was to test for repeated evolutionary divergences in hydraulic traits associated with the timing of atmospheric drought. The community-level pattern focused on variation in whole-plant hydraulic conductance, which integrates the entire conducting pathway from soil through the xylem to the leaves; in this study we examined in greater detail the components of the pathway, specifically leaf-specific and stem-specific conductivity. We predicted that higher conductivity would be adaptive under higher VPD, and thus greater in species in Santa Barbara compared with their relatives in Tehuacan.
Our second objective was to examine evolutionary associations between hydraulic traits that represent broadly observed interspecific functional relationships. Trait correlations observed across taxonomically diverse species may imply an adaptive relationship; however, they do not necessarily reflect coordinated evolutionary change in those traits. For example, when the cross-species correlation between leaf size and leaf life-span among extant taxa was analyzed using phylogenetically independent contrasts (PICs), the trait association was seen to be driven largely by one instance of coordinated change during the split between angiosperms and conifers (Ackerly & Reich, 1999); thus, within lineages, those leaf traits do not appear to be coevolving. Similarly, there is evidence that shared ancestry can also have a large influence on cross-species hydraulic trait relationships (Maherali et al., 2006). Therefore, we used PICs to test for correlated evolutionary change between traits, as evidence of an adaptive association. We tested whether higher leaf-specific conductivity was achieved through coordinated evolutionary shifts in stem-specific conductivity and the leaf area to sapwood area ratio. We also tested whether the evolution of increased conductivity was associated with decreased resistance to embolism, and finally whether divergences in resistance to embolism were correlated with divergences in wood density and minimum seasonal water potentials.
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Despite the difference in rainfall seasonality between Santa Barbara and Tehuacan (Fig. 1), the extent of soil dry-down experienced by species, as indicated by water potentials, did not differ consistently between sites (Table 2). By the end of the dry season, species were more varied within than between sites, spanning a large range of Ψpredawn values, presumably reflecting differences in rooting depths (Fig. 1, Table 2). While disequilibrium between soil and leaf predawn water potentials has been found in some desert shrub species (Donovan et al., 2003), for four of the six California species, the relative ranking of rooting depth established by Hellmers et al. (1955) mirrors the ranking of Ψpredawn in this study.
Evolutionary divergences in hydraulic traits among the six species pairs in this study were expected to be correlated with divergences in precipitation patterns between Santa Barbara and Tehuacan (Fig. 1). However, divergences in KS, a measure of water transport efficiency, were not associated with site. Within both sites there was fourfold variation in KS among genera and, more strikingly, genera generally maintained their relative ranks across the site contrast (Fig. 2a). KS may exhibit conservatism with respect to lineage because of a number of factors, such as stabilizing selection or perhaps lack of selection. Other studies have reported low rates of evolutionary change in wood characteristics and vessel density, which should have consequences for hydraulic transport capacity (Maherali et al., 2006; Preston et al., 2006).
The relative stasis in KS across sites with contrasting seasonality of rainfall raises the general question of what climate variables impose selective pressure on KS. A global meta-analysis by Maherali et al. (2004) revealed a complex relationship between KS and climate, related to life history. In deciduous angiosperms, evolution of increasing KS was correlated with decreasing precipitation, but water availability did not explain variation in KS in evergreen angiosperms or conifers. In fact, evolution of KS within the evergreen angiosperms was not associated with any of the climate parameters included in their study, including atmospheric demand and temperature.
At smaller scales, studies within one or a few lineages comparing congeners of differing water status have generally found no correlation between evolutionary change in KS and site or species water availability (Preston & Ackerly, 2003; Edwards, 2006; Choat et al., 2007; but see Cavender-Bares et al., 2004). Few studies have examined contrast correlations between KS and atmospheric demand (VPD), but within Pereskia no correlation was found (E. J. Edwards, pers. comm.). In this study, we were able to compare a system in which high VPD coincided with maximum soil water deficit vs one in which they were separated seasonally, but by design mean annual rainfall was similar between sites. Consistent with a growing number of studies, we found no pattern of divergence in KS associated with our climate contrast. Thus, the adaptive significance of KS for evergreen angiosperms is unresolved with respect to climate variables.
Under contrasting humidity conditions, intraspecific comparisons have found greater leaf-specific hydraulic conductivity (KL) in tree populations experiencing higher VPD (Maherali & DeLucia, 2001; Cornwell et al., in press). Thus, the coincidence of high atmospheric demand with soil drought in Santa Barbara was expected to result in selective pressure for higher KL relative to Tehuacan. Consistent with this hypothesis, there was a repeated evolutionary shift towards higher KL in Santa Barbara for five out of six pairs. Higher KL in Santa Barbara may be part of a hydraulic strategy to balance leaf water supply with the high evaporative demand during the dry season, when predawn water potential is extremely negative. A highly conductive soil–leaf transport pathway can then prevent excessive drops in end of season leaf water potentials and allow continued carbon gain under high-VPD conditions (see Addington et al., 2006).
The one pair that showed a reversal was Salvia, with higher KL in Tehuacan compared with Santa Barbara. However, Salvia mellifera, the Santa Barbara species, has a distinct leaf phenology which may contribute to the observed reversal. Immediately after the rainy season, S. mellifera produces a cohort of drought-deciduous leaves which are dropped with the onset of the dry season, while side-shoot leaves are maintained (Gill & Mahall, 1986). A seasonal shift towards higher in situ KL has been previously documented in S. mellifera (Kolb & Davis, 1994), which suggests that the reduction in LA:SA during the dry season may be enough to ensure higher leaf water supply to the remaining leaves, even with embolism-induced drops in KS. Hydraulic measurements in this study were conducted under favorable water conditions in spring, and thus by the end of the dry season Salvia may have also had higher leaf conductivity in Santa Barbara, similar to the other pairs.
As the case of Salvia illustrates, KL is determined by the interaction between KS and LA:SA; changes in KL can thus be achieved through various combinations of change in the other two traits. Under high VPD, one particular pattern that has been observed in intraspecific studies is higher KL through a combination of higher KS and lower LA:SA (Maherali & DeLucia, 2000, 2001). Of the two traits, LA:SA in particular has been hypothesized to decrease under conditions of increasing evaporative demand, as a means of increasing leaf water supply (Mencuccini & Grace, 1995). If the evolutionary pattern is similar we would expect divergences in KS and LA:SA to be associated with site, as well as negatively correlated with each other. However, in our study, genera varied in how LA:SA differed across sites, and higher KL in Santa Barbara was achieved in different ways (Fig. 2b,c). Additionally, contrast correlations revealed a trend in the opposite direction from that found in intraspecific studies; divergences in KS were generally positively correlated with divergences in LA:SA (Fig. 3a). The outlier, Quercus, has large differences in LA:SA, with no corresponding divergences in KS. The positive association between KS and LA:SA has been found interspecifically (Vander Willigen et al., 2000) and between divergences (Preston & Ackerly, 2003; but see Edwards, 2006). The complicated interplay among the three traits may explain the varying direction of correlation: in some cases higher transport efficiency (KS) may allow maintenance of greater leaf deployment (higher LA:SA), but the resulting KL is dependent on their relative changes.
One widely tested hydraulic relationship is the trade-off between safety and transport efficiency. Interspecific correlations across diverse taxa provide evidence of a weak negative relationship between measures of transport efficiency (conduit diameter or KS) and measures of stem resistance to embolism (PLC50) (Tyree et al., 1994; Maherali et al., 2004; Hacke et al., 2006; Maherali et al., 2006), although at the leaf level conductivity and drought tolerance may be decoupled (Sack et al., 2003). However, evolutionary analyses reveal no significant correlations among trait divergences (Maherali et al., 2004; Maherali et al., 2006; Jacobsen et al., 2007). Similarly, among the six pairs in this study, it appears that evolution of hydraulic transport efficiency (KS) is independent of the evolution of hydraulic resistance (PLC50) (Fig. 3b). Recent work on the mechanism of stem resistance has focused on the role of conduit pit structure and suggests that the anatomical traits that confer increased resistance to embolism may be somewhat decoupled from those that contribute to transport efficiency (Sperry et al., 2005; Wheeler et al., 2005). Because of the number of functionally linked traits that may collectively determine safety and efficiency, selective pressure can operate on distinct aspects of hydraulic architecture, and may explain the weak evolutionary correlation between stem conductivity and embolism resistance.
A tight evolutionary correlation was found between the extent of drought stress experienced in the field (Ψmin) and xylem resistance to embolism (Fig. 3c, inset). Cross-species, this relationship has been found widely (Davis et al., 1999; Pockman & Sperry, 2000), including among the species in this study (Fig. 3c) – evidence of an evolutionary correlation in this study suggests that the balance between Ψmin and resistance is adaptive. This may be consistent with an evolutionary correlation found more broadly across evergreen angiosperms between resistance to embolism and mean annual precipitation – at global scales, Ψmin may scale with mean annual precipitation (Maherali et al., 2004). The cost of low resistance to embolism relative to Ψmin is apparent: high rates of embolism, stomatal shut-down and at the extreme shoot death (Davis et al., 2002); however, the cost of overly resistant xylem is less clear, particularly as no trade-off is seen with conductivity. The construction costs associated with high resistance may partially explain the evolutionary match between Ψmin and PLC50. Across a large number of diverse taxa, greater stem resistance to embolism is associated with higher wood density (Hacke et al., 2001). Similarly, in our study divergences between wood density and PLC50 were positively, although not significantly, associated (Fig. 3d).
In conclusion, we found that the contrast in timing of rainfall had selective consequences for leaf but not sapwood specific conductivity. Variation in KS was largely explained by differences among genera, which were maintained across sites. The majority of genera had higher KL in Santa Barbara, which was achieved through different combinations of change in LA:SA and KS. Interestingly, divergences in KS and LA:SA may be interrelated; a weak positive correlation was found using contrasts. Thus, while the target of selection may be higher KL, there may be underlying coordination between higher transport efficiency and greater deployment of leaf area relative to sapwood area. No evidence was found for an evolutionary trade-off between resistance to embolism and sapwood-specific conductivity, consistent with recent global analyses. Evidence of correlated evolution between Ψmin and PLC50 suggests that the extent of drought experienced in the field has selective consequences for resistance to embolism.
The inclusion of all available pairs in this study revealed a diverse array of hydraulic strategies in both sites, as well as varied evolutionary trajectories across the climatic contrast. Studies of trait evolution in response to the mediterranean-type climate have found similarly heterogeneous responses. In California, some chaparral lineages that predate the origin of the mediterranean climate already possessed traits considered characteristic of MTE, related to fire persistence and leaf morphology, which allowed them to persist once the climate changed (Axelrod, 1989; Herrera, 1992; Valiente-Banuet et al., 1998; Verdu et al., 2003; Ackerly, 2004a; Pausas et al., 2006). Instances where trait evolution does correlate with a change in climate have been found to reflect the biogeographic history of the lineages (Ackerly, 2004a). Thus, both trait evolution and ecological sorting contribute to the observed functional diversity of these communities.