Finding support for theoretical tradeoffs in xylem structure and function

‘It is notable, then, when a study comes along that challenges our fundamental assumptions and urges a research community to re-evaluate the interpretation of certain methods and metrics.’ In 2004, Baas et al. clearly outlined a set of hypotheses to help explain the functional roles of xylem in woody plants and the assumed tradeoffs that should exist between resistance to embolism (i.e. safety), conductive efficiency, and mechanical strength (Fig. 1). When this ‘tradeoff triangle’ was proposed, xylem vulnerability curves (i.e. the measured percent loss of hydraulic conductivity for a given xylem sap tension), and the point at which 50% of hydraulic conductivity is lost (P50), were acknowledged as being useful indicators for characterizing woody plants within specific habitats, and for predicting a species’ response to drought. More recently, the point at which plants lose 88% of their hydraulic conductivity (P88) appears to be a good indicator of the physiological tipping point for many woody plants. Beyond that threshold the probability of recovering from such a drought event is marginal (Urli et al., 2013). If we accept P50, or other points on the vulnerability curve (e.g. P12 or P88), as suitable metrics for characterizing xylem safety, then one could argue that the Gleason et al. study suggests selection may not result in a tradeoff between safety and efficiency in stems. Indeed, as the authors note, over 50% of the studies aimed at finding such a tradeoff have failed. At least two distinct possibilities arise from this study: we have not been looking for the safety–efficiency tradeoff in the right plant structures, and/or our methods or theory are flawed and in need of revision. Gleason et al. have focused on the most readily available traits, and rightly so; safety and efficiency are well-studied and widely reported. While they found a weak relationship between safety and efficiency in stems, should this finding surprise us? The stem is but one tissue among many along the hydraulic pathway from the soil to the atmosphere. Selection is acting at all points along this pathway simultaneously and may more strongly influence tissues other than the stem (e.g. Zimmermann, 1978). We may not see such tradeoffs in the stem because structural support of the photosynthetic and reproductive tissues is deeply integrated into stem anatomy. The largest conduit diameters are commonly found in lianas, where xylem is thought to be released from the structural constraints that govern the xylem of freestanding woody plants. So, stems may not be the best tissue for studying these compromises, and analyzing these broad traits based on plant functional type (e.g. structural parasites) may provide an alternative perspective for interpreting available datasets. A more integrative approach that examines the coordination of traits among different plant structures will prove to be a fruitful path for future research. For example, the coordination between stem and leaf hydraulic strategies may help to explain much of the variation observed by Gleason et al. and may better explain ecological and evolutionary patterns (Skelton et al., 2015). Better integration of measurements from along the entire hydraulic pathway would require the measurement of more tissue types, but also the development of standardized measurement protocols (e.g. the Prometheus Wiki; http://prometheuswiki.publish.csiro.au). We must also consider which measurements may be the most useful and informative. For example, hydraulic conductance (as opposed to conductivity) may more accurately describe the water flux through functional xylem to distal organs and, thus, may better predict downstream physiology (Brodribb & Feild, 2000). Vulnerability curves are inherently valuable, but gain significant predictive power when coupled with the scale and return frequency of episodic drought events where natural selection might be acting most strongly. If, as Delzon & Cochard (2014) suggest, extreme drought events are needed to push plants to P50 and P88, embolism formation and spread may not be routine in plants, and those dangerous regions of the vulnerability curve are not particularly relevant during nondrought conditions. Additions to the list of desirable traits for future meta-analyses that might help to explain the variance presented by Gleason et al. would include capacitance in its different forms (Meinzer et al., 2009), safety margins, and water potential values that induce stomatal closure or incipient plasmolysis. These traits would provide an even greater environmental and ecological context for examining the hypothesized safety–efficiency tradeoff. But even safety margins and a revised interpretation of vulnerability curves will not fully disentangle the safety–efficiency tradeoff, as there are more ‘safety’ mechanisms utilized by plants than resistant conduits. Drought-induced leaf shedding and embolism repair are two of the many strategies that allow plants to avoid or recover from dangerous water potentials. For example, many species shed their leaves before entering the risky region of the vulnerability curve (Sobrado, 1997). Similarly, if a species is capable of refilling embolized xylem conduits (Brodersen & McElrone, 2013), then P12 or P50 could be largely irrelevant if we assume that those plants quickly recover when significant xylem tensions are relieved. Thus, without a more rigorously defined environmental, physiological, and phenological context, teasing apart the meaning of the trends presented by Gleason et al. will be challenging. The possibility also exists that there are yet unmeasured xylem traits that could be better indicators of hydraulic safety. Xylem network redundancy and connectivity are notoriously difficult to study because of the small scale and complexity of conduit organization (Brodersen, 2013), yet those traits appear to have a significant influence over water distribution and the spread of drought-induced embolism (Zanne et al., 2006; Loepfe et al., 2007; Lee et al., 2013). While a highly interconnected xylem network is more efficient at rerouting water around blockages, that benefit comes at the cost of increased probability of embolism spread between conduits, and illustrates a different manifestation of the safety–efficiency compromise. Hydraulic segmentation, or sectoriality, also appears to act at the stem level (Schenk et al., 2008), where systemic embolism spread is confined by the physical separation of the water-conducting pathway into discrete units. This study also highlights some particularly interesting areas for future work. In particular, the authors were able to identify several plant groups where a safety–efficiency tradeoff appears to exist (e.g. Acer). With Acer as a model system, Lens et al. (2010) have provided a glimpse into the structure and function of some of the woody species of this genus, where selection has apparently acted more strongly on the xylem traits that allow for a safety–efficiency tradeoff to be revealed using current metrics among the studied species. The question then is: why Acer? What about its evolutionary history and speciation have allowed it to have the anatomical plasticity within the stem xylem of 10 Acer species to explore such a broad region of the safety–efficiency morphospace with clear tradeoffs, while other plant groups have not? Targeted sampling within phylogenetic clades will likely be an efficient strategy for elucidating these tradeoffs. There is a strong and growing movement to understand how plants will respond to climate change, and how future environmental conditions may push species beyond their physiological thresholds (Allen et al., 2010). Given that plant water transport plays an integral role in landscape water and carbon budgets, it has become increasingly evident that plant biologists should establish a set of physiologically based traits and environmental thresholds that are predictive and meaningful for modelers. The implications of Gleason et al. have highlighted the need for an integrated, whole-plant approach to studying physiological plant ecology, as well as the complex challenges that lie ahead.