Contents Summary1I.Introduction2II. Consequences of vegetation mortality3III.Global patterns of mortality3IV.Hypotheses on mechanisms of drought‐related mortality4V.Evidence for hypothesized mechanisms5VI.Implications of future climate on hypothesized mortality mechanisms13VII.Conclusions15Acknowledgements15References15 Summary Severe droughts have been associated with regional‐scale forest mortality worldwide. Climate change is expected to exacerbate regional mortality events; however, prediction remains difficult because the physiological mechanisms underlying drought survival and mortality are poorly understood. We developed a hydraulically based theory considering carbon balance and insect resistance that allowed development and examination of hypotheses regarding survival and mortality. Multiple mechanisms may cause mortality during drought. A common mechanism for plants with isohydric regulation of water status results from avoidance of drought‐induced hydraulic failure via stomatal closure, resulting in carbon starvation and a cascade of downstream effects such as reduced resistance to biotic agents. Mortality by hydraulic failure per se may occur for isohydric seedlings or trees near their maximum height. Although anisohydric plants are relatively drought‐tolerant, they are predisposed to hydraulic failure because they operate with narrower hydraulic safety margins during drought. Elevated temperatures should exacerbate carbon starvation and hydraulic failure. Biotic agents may amplify and be amplified by drought‐induced plant stress. Wet multidecadal climate oscillations may increase plant susceptibility to drought‐induced mortality by stimulating shifts in hydraulic architecture, effectively predisposing plants to water stress. Climate warming and increased frequency of extreme events will probably cause increased regional mortality episodes. Isohydric and anisohydric water potential regulation may partition species between survival and mortality, and, as such, incorporating this hydraulic framework may be effective for modeling plant survival and mortality under future climate conditions.

Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk

Wood density (D ), an excellent predictor of mechanical properties, is typically viewed in relation to support against gravity, wind, snow, and other environmental forces. In contrast, we show the surprising extent to which variation in D and wood structure is linked to support against implosion by negative pressure in the xylem pipeline. The more drought-tolerant the plant, the more negative the xylem pressure can become without cavitation, and the greater the internal load on the xylem conduit walls. Accordingly, D was correlated with cavitation resistance. This trend was consistent with the maintenance of a safety factor from implosion by negative pressure: conduit wall span (b) and thickness (t) scaled so that (t/b) was proportional to cavitation resistance as required to avoid wall collapse. Unexpectedly, trends in D may be as much or more related to support of the xylem pipeline as to support of the plant.

1515Plant, Cell and Environment (1999) 22, 1515-1526 g sm , maximum stomatal conductance for water vapour; J S , sap flux density; k/A L , leaf-specific hydraulic conductance; LAI, leaf area index; DY S-L , water potential difference between soil and leaf. INTRODUCTIONAs the vapour pressure deficit between leaf and air (D) increases, stomata generally respond by partial closure (Lange et al. 1971). In most cases, stomatal conductance (g s ) decreases exponentially with increasing D (Massman & Kaufmann 1991; McCaughey & Iacobelli 1994; Monteith 1995). The stomatal closure response to increasing D generally results in a non-linear increase in transpiration rate (per unit leaf area, E) to a plateau and in some cases a decrease at high D (Jarvis 1980; Monteith 1995;Pataki, Oren & Smith 1999). By avoiding high E that would otherwise be caused by increasing D, stomatal closure avoids the corresponding decline in plant water potential (Saliendra, Sperry & Comstock 1995). It is a reasonable premise that the closure response evolved to prevent excessive dehydration and physiological damage.It is established that the cue for the closure response is linked to E rather than D (Mott & Parkhurst 1991) and is therefore fundamentally a feedback response to water loss from the leaf tissue. The only known mechanism by which the plant can sense E is a change in the water potential (or its proxy, relative water content) of cells in the leaf. However, the identity of these cells, and the details of the signal transduction are unknown. Nevertheless, these results argue for an analysis of stomatal responses to D from the standpoint of the regulation of E (Monteith 1995) and water potential (Saliendra et al. 1995).In this paper, we focus on the sensitivity of the stomatal response to D, where sensitivity refers to the magnitude of the reduction in g s with increasing D. While most plants exhibit a decline in g s with D, there is considerable variation at the intra-and interspecific levels in the sensitivity of the response (e.g. Whitehead, Okali & Fasehun 1981;Aphalo & Jarvis 1991; McNaughton & Jarvis 1991). It is commonly observed that greater sensitivity is associated with a higher g s at low D (Kaufmann 1982; McNaughton & Jarvis 1991;Yong, Wong & Farquhar 1997). Here we test the generality of this relationship for data obtained by both porometric and sap flux methods across a variety of species ABSTRACTResponses of stomatal conductance (g s ) to increasing vapour pressure deficit (D) generally follow an exponential decrease described equally well by several empirical functions. However, the magnitude of the decrease -the stomatal sensitivity -varies considerably both within and between species. Here we analysed data from a variety of sources employing both porometric and sap flux estimates of g s to evaluate the hypothesis that stomatal sensitivity is proportional to the magnitude of g s at low D (£ 1 kPa). To test this relationship we used the function g s = g sref -m · lnD where m is the stomatal sensitivity and g sref = g s a...

Abstract. Hydraulic conductivity of the xylem is computed as the quotient of mass fiow rate and pressure gradient. Measurements on excised plant stems can be difficult to interpret because of timedependent reductions in fiow rate, and because of variable degrees of embolism. Using Acer saccharum Marsh, stems, we found that certain perfusing solutions including dilute fixatives (e.g. 0.05% formaldehyde) and acids with pH below 3 (e.g. 10 mol m~^ oxalic) prevent long-term decline in conductivity. Xylem embolism can be quantified by expressing the initial conductivity as a percentage of the maximum obtained after fiow-impeding air emboli have been removed by repeated high-pressure (175 kPa) fiushes. Correlation between microbial contatnination and declining conductivity suggests that long-tenn (>4h) declines are caused by microbial growth within the vessels. Unpredictable trends in short-term (<4h) measurements may be caused by movements of air emboli in vessels and/or particulate matter.

ABSTRACT

Summary Recent decades have been characterized by increasing temperatures worldwide, resulting in an exponential climb in vapor pressure deficit (VPD). VPD has been identified as an increasingly important driver of plant functioning in terrestrial biomes and has been established as a major contributor in recent drought‐induced plant mortality independent of other drivers associated with climate change. Despite this, few studies have isolated the physiological response of plant functioning to high VPD, thus limiting our understanding and ability to predict future impacts on terrestrial ecosystems. An abundance of evidence suggests that stomatal conductance declines under high VPD and transpiration increases in most species up until a given VPD threshold, leading to a cascade of subsequent impacts including reduced photosynthesis and growth, and higher risks of carbon starvation and hydraulic failure. Incorporation of photosynthetic and hydraulic traits in ‘next‐generation’ land‐surface models has the greatest potential for improved prediction of VPD responses at the plant‐ and global‐scale, and will yield more mechanistic simulations of plant responses to a changing climate. By providing a fully integrated framework and evaluation of the impacts of high VPD on plant function, improvements in forecasting and long‐term projections of climate impacts can be made.

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of droughtinduced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function