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Changes in temperature and rainfall patterns across many forest and woodland ecosystems are thought to underlie the increasing vulnerability of tree species to drought-related mortality (Allen et al., 2010). Global analyses of forest vulnerability and drought-related mortality events across different biomes suggest that a wide range of forest types are susceptible to periods of extreme temperature and water deficit (Allen et al., 2010; Choat et al., 2012). However, in many cases, mortality rates vary among species or functional types (Pook et al., 1966; Breshears et al., 2005; Fensham & Fairfax, 2007) suggesting strong differences in drought resistance among co-occurring species. Despite major progress on understanding on how water deficit affects plant functioning (Sperry, 2000; Breda et al., 2006; Flexas et al., 2006) the controls on species survival under extreme drought remain poorly resolved and limit our ability to adequately predict future changes in ecosystem structure and function.
Recent syntheses have built on earlier work on drought physiology to describe how mechanisms of mortality are linked to plant capacity to regulate its carbon and water balance under drought conditions of differing intensity and duration (McDowell et al., 2008; Allen et al., 2010). These frameworks suggest that, for any given drought event, both plant hydraulic strategy and meteorological conditions will define the ‘physiological drought’ experienced by the plant. Physiological drought is a function of plant regulation of water-use in response to declining soil water potential and thresholds associated with hydraulic- or carbohydrate-mediated mortality. For example, plants exposed to low-intensity but long-duration droughts may maintain water status above critical water potential thresholds but deplete stored carbohydrates to lethal limits (i.e. carbon starvation). Conversely, under high-intensity drought, incapacity to regulate plant water status above critical thresholds will promote xylem cavitation and death through dehydration (i.e. hydraulic failure). In addition to these drivers, trees often sustain tissue damage from biotic and abiotic agents such as pest outbreaks (Ayres & Lombardero, 2000) and extreme temperatures (De Boeck et al., 2010) that can amplify the impacts of drought. This conceptual framework has been the focus of intense debate within the literature (Adams et al., 2009; McDowell & Sevanto, 2010; Sala et al., 2010) but has not been extensively tested with observational and experimental data.
The processes of hydraulic failure and carbon starvation are intimately linked (McDowell et al., 2011) via the balancing act required to minimize water loss and maximize carbon uptake at the leaf surface. Adjustments in stomatal aperture act to reduce transpiration in response to declining hydraulic conductance and/or reductions in leaf turgor and help plants avoid water potentials that can induce hydraulic failure (Sperry, 2000). At the whole-plant scale, the hydraulic architecture of plants appears to be well coordinated with photosynthetic capacity (Brodribb & Feild, 2000; Santiago et al., 2004; Quentin et al., 2012)., Under favourable growing conditions, higher photosynthetic capacity tends to promote higher growth rates (Poorter et al., 1990; Lambers & Poorter, 1992). Therefore, higher rates of hydraulic conductance may promote high growth rates in trees by maintaining high stomatal conductance (gs), internal [CO2] and carbon gain (Tyree, 2003). However, during protracted periods of water deficit, high hydraulic conductance may also increase plant susceptibility to cavitation (Maherali et al., 2006). Evidence for a growth vs hydraulic safety trade-off is highlighted by relationships between wood density and growth rate (Enquist et al., 1999; Muller-Landau, 2004) and cavitation safety (Hacke et al., 2001). The capacity for rapid growth (i.e. high intrinsic relative growth rates) can reduce carbon allocation to hydraulic safety (e.g. reduced lumen fraction, thicker cell walls), potentially making these species more vulnerable to hydraulic failure during drought.
Maintenance of cell turgor, which is a hydraulically mediated process, plays an important role in regulating the carbon balance of plants. Growth is particularly sensitive to changes in cell turgor and often declines before reductions in leaf photosynthesis in response to drought (Hsiao et al., 1976; Amthor & McCree, 1990) In contrast, respiration tends to be relatively insensitive to drought and does not decline proportionally in response to declining photosynthesis (Atkin & Macherel, 2009; Ayub et al., 2011). As a result, the concentration of nonstructural carbohydrates within plant tissues depends on the balance between carbon supply (i.e. photosynthesis) and carbon demand (i.e. growth and respiration). In the short term, the concentration of nonstructural carbohydrates during drought will increase if reductions in growth precede declines in photosynthesis, a response that has been observed in many species (Tissue & Wright, 1995; Körner, 2003; Ayub et al., 2011). However, if drought is prolonged, reductions in carbon assimilation and subsequent consumption of reserve carbohydrates may occur until a threshold is reached, after which plants may die of carbon starvation (McDowell et al., 2011).
As a result of these trade-offs in hydraulic and carbon dynamics, plants operate along a continuum of responses to drought, which are characterized by varying levels of hydraulic regulation to declining water availability associated with structural and physiological traits (Mitchell et al., 2008; Bartlett et al., 2012). We propose that physiological drought will vary in species with different growth and hydraulic strategies and generate water stress conditions of differing duration and intensity that are associated with mortality processes involving hydraulic failure and carbohydrate starvation. To test this, we compared the magnitude and timing of changes in water relations, gas exchange and carbohydrate dynamics in three tree species with different water use and growth characteristics exposed to a terminal drought treatment. We hypothesized that tight hydraulic regulation of water and carbon uptake reduces the risk of rapid hydraulic failure, but results in increased duration of the physiological drought and promotes depletion of nonstructural carbohydrates.