1. Biotic agent demographics
This hypothesis suggests that drought drives changes in demographics of mortality agents such as insects and pathogens, which subsequently drive forest mortality independently or in conjunction with drought-induced changes in host plant physiological condition. This hypothesis derives from the frequent observation that a temporal correlation exists between drought and outbreaks of insects (White, 1984; Mattson & Haack, 1987; Waring & Cobb, 1992; Clancy et al., 1995; Shaw et al., 2005; Fettig et al., 2007) and pathogens (Houston, 1987; Manion, 1991). Predictions suggest population demographics such as growth rates and reproduction of biotic mortality agents will be exacerbated by climate change largely as a result of increased temperatures (Ayres & Lombardero, 2000; Logan et al., 2003; Gan, 2004; Tran et al., 2007). Empirical evidence and models suggest that drought associated with unusually warm weather will have an impact on many characteristics of insect population dynamics, including intrinsic population growth rate, the number of generations produced per year, synchrony of key developmental phases, winter mortality, and geographic range (Ungerer et al., 1999; Logan & Bentz, 1999; Ayres & Lombardero, 2000; Simberloff, 2000; Logan & Powell, 2001; Logan et al., 2003; Hicke et al., 2006). Droughts may also affect insect and pathogen populations by influencing the abundance of key predators and mutualists (Ayres & Lombardero, 2000); the direction and magnitude of such effects are largely unknown. It is unlikely that drought will be beneficial to all insects that kill trees, or in all locations. For example, outbreaks of western spruce budworm in the southwestern USA are positively related to wet spring weather, negatively related to dry spring weather, and unrelated to temperature (Swetnam & Lynch, 1993). Likewise, the synchrony of insect emergence with temperature may have negative consequences for insect population growth at low elevations but positive impacts on population growth at higher elevations (Hicke et al., 2006). Overall, warm droughts may increase the intensity of outbreaks of biotic mortality agents independent of concomitant changes in tree physiological condition related to drought, although the specific dynamics may vary by agent.
Drought-related mortality does not always include an obvious biotic mortality agent (Lloret et al., 2004) and thus the biotic agents demographics hypothesis can explain, at most, only a portion of observed mortality. However, plants treated with insecticides often survive outbreaks of insects (Hastings et al., 2001; Grosman & Upton, 2006; Romme et al., 2006), indicating that biotic agents play a significant role in mortality. A prediction consistent with observations is that changes in demographics of biotic mortality agents must overlay changes in host plant physiological conditions to cause widespread mortality events (Berryman, 1976; Christiansen et al., 1987).
2. Plant water relations
A review of plant regulation of water use is needed to consider the mechanisms of hydraulic failure and carbon starvation. In particular, it is critical to understand the structural and physiological mechanisms by which plants prevent evapotranspiration (E) from exceeding critical rates (Ecrit) that result in xylem water potentials associated with hydraulic and symplastic failure (Ψcrit). Furthermore, the impacts of Ecrit avoidance on photosynthesis and subsequent dependency on stored carbohydrate reserves are critical to understanding carbon starvation (Cowan & Farquhar, 1977; Katul et al., 2003). In this section we review plant water relations in the context of avoidance of Ecrit and Ψcrit, introduce a modeling framework for investigation of such regulation, and then investigate hypotheses regarding hydraulic failure and carbon starvation using the model and existing evidence from our piñon–juniper case study and the broader literature.
To maintain tissue hydration and photosynthesis, plants must replace water lost through E. As described by the cohesion tension theory, E generates tension that pulls water from the soil through the plant to the crown, where it diffuses to the atmosphere. Thus, E can be explicitly described via the steady-state formulation of the soil–plant–atmosphere hydraulic continuum (modified from Whitehead & Jarvis, 1981; Whitehead, 1998):
- E = Kl (Ψs − Ψl − hpwg) (Eqn 1)
In this corollary to Darcy's law, Kl is leaf-specific hydraulic conductance of the soil-plant continuum, Ψs and Ψl are soil and leaf water potentials, respectively, and hpwg is the gravitational pull on a water column of height h and density pw. The tension difference across the plant (Ψs – Ψl) increases in proportion to E as long as Kl remains constant, for example no cavitation occurs. This mechanism is efficient because metabolic energy is not used to lift water to the crown. However, E has an upper limit (Ecrit) because increasing tension causes decreased Kl as a result of air entry through pit pores into conduits, thereby initiating cavitation (nucleation of vaporization) and producing an embolized, or air-filled conduit (Fig. 4). In other words, hydraulic failure occurs when E exceeds the critical Ψ, Kl approaches zero, and the plant can no longer move water. The Ψcrit value causing 100% cavitation varies widely among species (Pockman et al., 1995; Pockman & Sperry, 2000; Maherali et al., 2004) and is thought to be a function of interconduit pit structure (Pittermann et al., 2005). An example of vulnerability to cavitation in stems and roots of piñon and juniper is presented in Fig. 4 (Linton et al., 1998). Roots tend to be more vulnerable than stems, which may serve the advantage of protecting the more energetically costly stem tissues from cavitation (Sperry & Ikeda, 1997; Sperry et al., 2002).
Figure 4. The percentage loss of conductivity of excised root (connected circles) and stem (unconnected circles) segments of piñon (open circles) and juniper (closed circles) as a function of xylem pressure. These ‘vulnerability curves’ were obtained by the air-injection method (Linton et al., 1998).
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Hydraulic failure also occurs within soils and is functionally similar to xylem cavitation. The hydraulic conductance of soils is a function of texture, water content, hydraulic conductivity, and water table depth. Greater tension is required to pull water through fine-textured soils because of their small pore sizes, and thus fine-textured soils have lower conductance than sandy soils when water is abundant. However, fine-textured soils retain hydraulic conductance longer and at more negative water potentials than coarse-textured soils because the low conductance of fine soils results in slower water loss to transpiration and drainage (Sperry et al., 1998). Therefore, during drought we expect greater hydraulic failure in coarse-textured soil. Depth to water table also has an impact on plant hydraulics by limiting or allowing plants to obtain water during periods of drought (Dawson, 1996; Franks et al., 2007). To compensate for coarse-textured soils or inaccessible water tables, plants may increase their soil-to-root, or rhizosphere conductance via adjusting fine root density (Ewers et al., 2000; Hacke et al., 2000), fine root hydraulic conductance (McElrone et al., 2007) rooting depth, and other root characteristics (Stirzaker & Passioura, 1996).
Plant avoidance of hydraulic failure can be conceptualized using models of the soil–plant–atmosphere continuum. Such models can then be used as the basis for predictions of mortality related to water stress. The relationship between E and Ψl can be modeled based on the hydraulic properties of soil and xylem, root distribution, and root-shoot allocation (Sperry et al., 1998, 2002; Fig. 5). When E is zero, Ψl equilibrates with bulk soil water potential (Fig. 5a). As E increases, Ψl drops (Fig. 5, solid line a–c). For every unit increase in E, the drop in water potential becomes progressively greater because cavitation and rhizosphere drying reduce Kl of the flow path. If E increases past Ecrit, and hence Ψ exceeds Ψcrit, then hydraulic failure will occur (e.g. when the soil-plant Kl falls to zero, Fig. 5c). As drought decreases soil water potential within the rooting zone, hydraulic failure occurs at progressively lower values of E (Fig. 5, compare dashed drought trajectory b–d with a–c). If hydraulic failure is caused by xylem cavitation within stems, Ψcrit corresponds to the pressure where 100% cavitation occurs (e.g. −6.9 MPa in piñon stems; Fig. 4). Drying of the rhizosphere may drive hydraulic failure at more positive Ψcrit because roots and soils are typically more vulnerable than stems (Fig. 4). This does not mean that roots or soils will always be the location of hydraulic failure, however, because stems can reach much more negative water potentials as a result of their longer hydraulic path length (McDowell et al., 2002a; Sperry et al., 2002); hence trees that have reached their maximum height may be particularly vulnerable.
Figure 5. Modeled transpiration per unit leaf area as a function of leaf water potential for a plant with relatively abundant soil moisture (solid line) and the same plant with reduced soil moisture availability (dashed line). Letters are referenced within the text.
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Using this hydraulic framework we can predict hydraulic failure during drought by plotting the decline in Ecrit as a function of soil water potential (Fig. 6). When the soil water potential reaches Ψcrit, Ecrit is zero and no further water can be extracted (Fig. 6, ‘extraction limit’). The actual water use must fall within this envelope (Fig. 6, ‘realized transpiration’); if the transpiration threshold is exceeded, hydraulic failure results. Plants maintain E below Ecrit over long time periods (e.g. years to centuries) via adjustment of structural features that allow maximum water uptake relative to demand by the plant crown, and over short time periods (e.g. diurnal cycles) via crown-level stomatal conductance (Gs) (Tyree & Sperry, 1988; Sperry et al., 1998).
Figure 6. Modeled transpiration per unit leaf area as a function of soil water potential. The solid line represents the transpiration threshold beyond which hydraulic failure occurs, and the dashed line represents realized transpiration, with the difference between the two lines representative of a hydraulic margin of safety.
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The long-term structural adjustments that maintain homeostasis between water supply, water demand, and plant metabolism (Whitehead & Jarvis, 1981; Cinnirella et al., 2002; Katul et al., 2003; Bréda et al., 2006) may all play a role in the survival or mortality of plants during drought. These adjustments are influenced over decadal time scales in response to climate, plant size, edaphic properties such as soil texture and depth, and stand density (Maherali & DeLucia, 2001; McDowell et al., 2002a, 2006; Sperry et al., 2002; Mencuccini, 2003). Long-term homeostasis was originally defined mathematically by Whitehead & Jarvis (1981) as a steady-state derivation of Darcy's law similar to Eqn 1:
- (Eqn 2)
where ks is saturated permeability of the conducting path, As is sapwood area, Al is leaf area, h is height, η is the viscosity of water, and ΔΨ is Ψs − Ψl − hpwg (Eqn 1). Although Eqn 2 is a simplification of the plant hydraulic system (Domec et al., 2007), it has proven remarkably accurate (Whitehead, 1998; Oren et al., 1999; Schäfer et al., 2000; McDowell et al., 2002a, 2005; Phillips et al., 2002; Barnard & Ryan, 2003). Furthermore, the structural adjustments included in Eqn 2 are consistent with the Sperry et al. (1998) model (Addington et al., 2006). Taken together, homeostatic factors from Eqns 1 and 2 that have been empirically documented include: (i) vulnerability of xylem conductance to low water potentials (see Fig. 4) (Pockman & Sperry, 2000; Ogle & Reynolds, 2002; Maherali et al., 2004); (ii) xylem permeability (Pothier et al., 1989; McElrone et al., 2004); (iii) refilling of cavitated elements (Sperry et al., 1987; Borghetti et al., 1991; Holbrook & Zwieniecki, 1999; Tyree et al., 1999; Salleo et al., 2004; West et al., 2007a); (iv) the soil-to-leaf water potential gradient (Hacke et al., 2000; McDowell et al., 2002a; Barnard & Ryan, 2003); (v) vertical distribution of root density as a function of soil water availability (VanSplunder et al., 1996; Volaire et al., 1998; Ewers et al., 2000; Hacke et al., 2000; Lloret et al., 2004; West et al., 2007b); (vi) ratio of root absorbing area to leaf area (Ewers et al., 2000; Hacke et al., 2000; Magnani et al., 2000); (vii) ratio of sapwood area to leaf area (Mencuccini & Bonosi, 2001; McDowell et al., 2002b, 2006; Barnard & Ryan, 2003); (viii) leaf shedding (Tyree et al., 1993; Suarez et al., 2004; Hultine et al., 2006); (ix) height (McDowell et al., 2005; Addington et al., 2006); and (x) capacitance (water storage, Goldstein et al., 1998; Phillips et al., 2003). Others, such as osmotic regulation of leaf turgor (Kozlowski & Pallardy, 2002), foliar water absorption (Breshears et al., 2008), aquaporin mediation of hydraulic conductance (McElrone et al., 2007) and cellular desiccation tolerance (Gaff, 1971; Dace et al., 1998; Sherwin et al., 1998), may also play a role in drought tolerance or avoidance. Each of these factors may strongly impact the likelihood of plants to survive or succumb to drought. For example, the observation that tall trees tend to die is consistent with Eqns 1 and 2 because height constrains Kl and E such that the margin of safety is reduced. Likewise, the observation that seedlings often die is consistent with their having insufficient soil-to-root Kl during drought.
Note that differences in structural parameters between our case study species, piñon and juniper, are consistent with Eqn 2 with respect to susceptibility to drought-related mortality. Relative to piñon, juniper has more cavitation-resistant xylem (Fig. 4), lower leaf area to sapwood area ratio (Grier et al., 1992), lower leaf area to root area ratio (West et al., 2008), a larger water potential gradient from soil to leaf (Lajtha & Barnes, 1991; West et al., in press), and is shorter (2.7 vs 5.6 m at Mesita del Buey New Mexico).
Over diurnal timescales, plants maintain E below Ecrit through stomatal closure. Plants reduce Gs in response to increasing E (Mott & Parkhurst, 1991), with the degree of closure linked to Ψcrit that causes embolism (Sperry et al., 2002). Gs is in turn regulated not only by water supply and demand, and their impact on E, but also by plant structural adaptations that impact the supply or demand for water, for example rooting volume or leaf area, respectively (Eqn 2). While reducing Gs serves the benefit of reducing water loss, it has the cost of reducing CO2 diffusion from the atmosphere to the site of carboxylation, and thereby constraining photosynthetic CO2 uptake (Cowan & Farquhar, 1977). As we show, this balance between water loss and CO2 uptake may partition plants between survival, hydraulic failure or carbon starvation during drought.
3. Isohydry and anisohydry
Plants fall into two categories across the continuum of stomatal regulation of water status, labeled isohydric and anisohydric regulation (Tardieu, 1993; Tardieu & Simonneau, 1998). Isohydric plants reduce Gs as soil water potential decreases and atmospheric conditions dry, maintaining a relatively constant midday Ψl regardless of drought conditions. Anisohydric species, by contrast, allow midday Ψl to decline as soil Ψ declines with drought. Piñon is a good example of isohydric regulation, maintaining leaf water potentials at c. −2.0 MPa despite severe soil drying (Fig. 7, and see Lajtha & Barnes, 1991; Williams & Ehleringer, 2000; West et al., 2008; Breshears et al., in press). Although no specific thresholds and ranges of isohydric control are generalized in the literature, isohydric behavior has been observed in temperate hardwoods, C4 grasses, Australasian and neotropical trees, and other species of gymnosperms (Tardieu & Davies, 1992; Loewenstein & Pallardy, 1998a,b; Tardieu & Simonneau, 1998; Niinemets et al., 1999; Bonal & Guehl, 2001; Fisher et al., 2006). Anisohydric plants maintain higher Gs for a given Ψl than isohydric species, effectively allowing Ψl to decline with decreasing soil water potential (Fig. 8, Barnes, 1986). Anisohydric behavior has been observed across the same diversity of plant groups: species such as juniper, sugar maple (Acer saccharum), sunflower (Helianthus annuus), and eucalyptus (Eucalyptus gomphocephala) allow a greater Ψl range than isohydric species (Loewenstein & Pallardy, 1998a,b; Tardieu & Simonneau, 1998; Franks et al., 2007; West et al., 2008). Anisohydric species tend to occupy more drought-prone habitats compared with isohydric species and have xylem that is more resistant to negative water potentials (see Fig. 4). There are, however, exceptions to these generalizations and many comparative studies and syntheses (Pockman & Sperry, 2000; Maherali et al., 2004) have not specifically characterized species as isohydric or anisohydric. Anisohydric vs isohydric regulation of water status may be a critical factor in the regulation of survival and mortality during drought (Fig. 3).
Figure 7. (a) Midday (11 : 00–13 : 00 h) leaf water potential for piñon (open circles) and juniper (closed circles); and (b) daily precipitation (left axis, bars) and soil water content at 20 cm (right axis, filled symbols) at Mesita del Buey near Los Alamos, New Mexico. Bars in (a) are standard errors. Water potential was measured via pressure chamber within 5 min of twig collection, and consisted of two twigs per individual and five individuals per species per time period. Soil water content was measured via neutron probe.
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Figure 8. Stomatal conductance vs leaf water potential for piñon (open circles) and juniper (closed circles) at Mesita del Buey, Los Alamos, New Mexico. Data from Barnes (1986).
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It is important to clarify that relating the hydraulic framework to plant mortality is based on the premise that whole-plant hydraulic failure will cause death. This premise may be false in cases of resprouting, xylem refilling, or if cells are desiccation-tolerant. Resprouting has been observed following cavitation-induced shoot dieback in shrubs (Davis et al., 2002; Sperry & Hacke, 2002), mesic hardwoods (Tyree et al., 1993), and riparian trees (Horton et al., 2001). A benefit of reducing leaf area via shoot dieback is the resulting improvement in water status of the remaining foliage and subsequent survival of the individual (Tyree & Sperry, 1989; Davis et al., 2002; Bréda et al., 2006). Resprouters may die during drought, however, if persistent hydraulic failure leads to carbon starvation that prevents growth of new stems. Refilling of cavitated elements may occur in some species when drought is relieved by precipitation, although the mechanisms and frequency of refilling remain debated (Sperry et al., 1987; Borghetti et al., 1991; Holbrook & Zwieniecki, 1999; Tyree et al., 1999; Salleo et al., 2004; West et al., 2007a). Refilling has been observed in piñon but not juniper (West et al., 2007a). Desiccation-tolerant cells, such as the live cells of mosses, ferns, seeds and pollen of higher plants, and of resurrection plants (e.g. Xerophyta), can withstand complete drying, and upon wetting they regain complete physiological function (Gaff, 1971; Dace et al., 1998; Sherwin et al., 1998). This ancestral trait is rare amongst vascular plants (Oliver et al., 2000); however, a lesser degree of cellular drought tolerance is common (Kozlowski & Pallardy, 2002). As plants have become larger and more complex, water transport has become more limiting to survival than cell physiology and so vegetative cells may have lost their capacity to tolerate air-drying (Oliver et al., 2000). Based on evidence for correlations between cellular desiccation limits and hydraulic transport limits (Brodribb et al., 2003), cellular drought tolerance may be as colimiting as hydraulics in determining plant physiological limits.
The large number of potential interactions between isohydry, anisohydry and parameters within Eqns 1 and 2 highlights that there is a large number of physiological and structural factors that may be adjusted to either tolerate or avoid water stress during drought. However, these factors may also have species or site-specific limits on how far they can be adjusted; these limits may subsequently predispose plants to hydraulic failure. Next we can apply the hydraulic framework to understand the hydraulically based hypotheses of hydraulic failure and carbon starvation.
4. Hydraulic failure
The concept underlying the hydraulic-failure hypothesis is that drought causes the species- and site-specific Ecrit to be surpassed such that the plant irreversibly desiccates. Hydraulic failure occurs in small plants, as seedling mortality has been linked to excessive cavitation in the field (Williams et al., 1997) and drying experiments with potted plants often result in rapid mortality (Sparks & Black, 1999). The limited rooting volume explored by seedlings exposes them to more negative soil water potentials than plants with larger root systems, decreasing soil-to-root Kl and hence the safety margin between realized E and Ecrit (Fig. 6). For mature trees there are numerous anecdotal observations of mortality occurring in the absence of insect or pathogen attack; however, it is unknown if hydraulic failure or another mechanism was the cause of death.
The piñon–juniper comparison provides an interesting contrast with respect to mortality by hydraulic failure. Modeling Ecrit vs Ψsoil using piñon and juniper vulnerability curves (Fig. 4) and soil and plant architecture and water potential data (West et al., 2008) yields the prediction that the anisohydric strategy of juniper makes it more susceptible to hydraulic failure than piñon, because the water-use envelope of juniper is closer to the xylem cavitation threshold (Fig. 9). Continued transpiration by juniper during drought reduced soil water potential to –6.9 MPa, bringing juniper plants close to hydraulic failure (Fig. 9, solid circle compared with Ecrit) and induced an estimated 40–60% embolism in roots and shoots, respectively (West et al., 2007a, 2008; Fig. 4). The species-specific difference in regulation of the hydraulic safety margins occurs in part via differential relationships between leaf water potential and Gs (Fig. 8; Barnes, 1986; Williams & Ehleringer, 2000; West et al., 2008). Although this strategy allows juniper to maintain photosynthetic activity during drought, ultimately it may result in patchy dieback of crowns if drought is prolonged, as has been observed in juniper during the 2000–2002 severe drought in the southwestern USA (authors’ personal observations). Whether this partial dieback can explain whole tree mortality is unknown, but given a drought of sufficient intensity and duration, it seems a logical hypothesis that hydraulic failure may cause whole-plant mortality in anisohydric plants (Fig. 3).
Figure 9. Modeled critical transpiration threshold as a function of soil water potential for piñon (dashed line) and juniper (solid line) and observed minimum leaf water potential for each (filled and open symbol, respectively). Data from West et al. (2008). Dotted vertical lines represent the species-specific margins of hydraulic safety, which are 0.05 and 0.01 mmol m−2 s−1 for piñon and juniper, respectively.
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By contrast, the isohydric behavior of piñon prevents excessive cavitation even during extreme drought, making it unlikely to be a victim of hydraulic failure. Piñons lose only an estimated 5–40% of their xylem conductivity (all in their root systems) because stomatal closure keeps xylem water potentials above −2.5 MPa during drought (Figs 7–9). Safety margins from hydraulic failure are relatively large (Fig. 9, compare open circle with Ecrit). Of course, this control of cavitation in piñon comes at the price of negligible gas exchange, which leads to the carbon-starvation hypothesis, which we discuss in the next section.
A notable insight that emerges from the hydraulic framework is that although isohydric species appear more vulnerable to embolism (Fig. 4), isohydric plants should actually be less likely to experience hydraulic failure because they close their stomata rather than risk cavitation. Anisohydric plants instead have higher rates of gas exchange during drought, but risk greater cavitation as a consequence (Fig. 10). Both isohydric and anisohydric species are capable of carbon starvation or hydraulic failure; however, the isohydric species will probably maintain Ψl above its hydraulic failure threshold until carbon starvation occurs (Fig. 10, thick line) and will only reach hydraulic failure if the drought is sufficiently intense to force whole-system cavitation via xylem equilibration with severely dry soil. By contrast, the anisohydric species will allow Ψl to approach (or even surpass, e.g. Fig. 9) its cavitation threshold, thus allowing a longer time period before zero carbon assimilation and hence a longer time period before carbon starvation occurs. However, the closer proximity that the anisohydric species has to its cavitation threshold increases the risk of catastrophic hydraulic failure if drought intensity continues to increase, particularly because it maintains Ψl in realms where both soil moisture release curves and cavitation response curves (i.e. Fig. 4) are steep, such that small changes in water availability can have very large impacts on water potential.
Figure 10. Theoretical predictions of the mechanisms of drought-related mortality for species utilizing isohydric vs anisohydric regulation of water potential. This figure is a more detailed representation of the hypotheses exemplified in Fig. 3, highlighting differences between isohydric (I) and anisohydric (A) functional types. The dashed horizontal line represents the point of hydraulic failure for each functional type. Carbon starvation is hypothesized to occur primarily for isohydric species that close stomata relatively early in a drought (solid isohydric line), initiating the phase of reliance on carbohydrate reserves earlier than anisohydric plants (compare solid isohydric and anisohydric lines). Isohydric species may experience hydraulic failure in cases of severe intensity of drought (dotted isohydric line). Anisohydric species have a more curvilinear response (similar to Fig. 9) and are predicted to maintain positive carbon gain for a longer period than isohydric species, thus prolonging the duration of drought they can withstand before carbon starvation (solid anisohydric line). However, anisohydric species have a smaller margin of safety, thus increasing their likelihood of mortality via hydraulic failure (dotted anisohydric line).
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5. Carbon starvation
The carbon-starvation hypothesis predicts that stomatal closure to prevent desiccation (e.g. by isohydric plants, Figs 8 and 9), causes photosynthetic carbon uptake to diminish to near zero (Fig. 10). Continued demand for carbohydrates to maintain metabolism will deplete carbohydrate reserves, leading eventually to starvation or an inability to fend off attack from biotic agents, whichever comes first (Fig. 3). Similar to the hydraulic-failure hypothesis, the carbon starvation hypothesis lacks direct tests, although variations on this theme have been modeled as a driver of mortality for decades (Waring, 1987; Manion, 1991; Martínez-Vilalta et al., 2002; Guneralp & Gertner, 2007). Empirical evidence supporting a link between carbon availability and mortality is derived from the numerous studies reporting that trees that die have lower stemwood growth rates, increased growth variability, or increased climatic sensitivity, particularly after severe droughts (Kolb & McCormick, 1993; Pedersen, 1998; Demchik & Sharpe, 2000; Ogle et al., 2000; Lloret et al., 2004; Rolland & Lemperiere, 2004; Suarez et al., 2004; Guarin & Taylor, 2005; Bigler et al., 2006). However, still other studies have shown higher growth rates in trees predisposed to die, particularly in oak species (Jenkins & Pallardy, 1995, T. Levanič & N. McDowell, unpublished data). Modeling studies typically support the carbon-starvation hypothesis (Pedersen, 1998; Guneralp & Gertner, 2007), including models that predict carbon starvation initiated by stomatal closure (Martínez-Vilalta et al., 2002).
The primary means of reduced photosynthesis by isohydric species during drought is the constraint on CO2 diffusion into leaf intercellular spaces as a result of stomatal closure (Figs 8 and 9). For example, piñon net photosynthesis is halved at a rhizosphere water potential of −1.0 MPa, and reaches zero at a water potential of −2.3 MPa (Lajtha & Barnes, 1991). However, respiratory consumption of stored carbohydrates continues during drought to maintain plant metabolism, even if growth is zero (Amthor, 2000). Accounting for nocturnal leaf respiration costs, piñon leaf carbon gain reaches zero at approx. −2.0 MPa (Barnes, 1986). If we make the simple assumption that whole-plant respiration consumes 55% of assimilation (Ryan et al., 1994; Waring et al., 1998; Litton et al., 2007) then piñon trees achieve negative whole-plant carbon balance around rhizosphere water potentials of −1.0 MPa. By contrast, making this same 55% assumption, we predict that juniper reaches a zero whole-plant carbon balance at a rhizosphere water potential of c. −3.0 MPa. In effect, this difference allows the anisohydric species to maintain positive carbon gain for a greater duration of the drought (Fig. 10).
The hypothesis that carbon starvation, not hydraulic failure, is a likely driver of mortality in isohydric species can be examined by parameterizing Barnes’ (1986) empirical model of leaf carbon gain using measurements of predawn water potential generated from the same field site (Mesita del Buey). Three years of monthly predawn water potential measurements demonstrate that piñon regulates water potential within a much narrower range than juniper (Fig. 11a). By contrast, modeled leaf carbon gain is substantially more variable for piñon than juniper (Fig. 11b), owing to the greater stomatal sensitivity of piñon to water stress (Fig. 8). During the 2000–2002 drought, when piñon experienced region-scale mortality, Breshears et al. (in press) observed that piñon and juniper predawn water potential was below –2.0 MPa for 11 months before observed mortality, effectively precluding carbon gain for a year.
Figure 11. (a) Three years of monthly observations of predawn water potential of piñon (open circles) and juniper (closed circles) from Mesita del Buey, Los Alamos, New Mexico. Twigs were sampled at least 20 min before sunrise and kept in plastic bags until measurement, which took place within 1 h of collection. Samples consisted of two twigs per tree and a minimum of five trees per species per time period. (b) Seasonal leaf carbon gain for piñon and juniper modeled using Barnes (1986) and the predawn water potentials from (a).
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The theory that carbon starvation and hydraulic failure are the dominant mechanisms of mortality for isohydric and anisohydric species, respectively, is further supported when a broader set of plant species is considered. In Fig. 12 we plotted a typical rhizosphere drying curve for a drought period after a precipitation event at time zero. We have overlaid measured Ψ of zero Gs for all isohydric species and Ψ of 100% cavitation for all anisohydric species. These species are described in our literature review from the ‘Isohydry and anisohydry’ section. An assumed time lag of 10 months from zero Gs to carbon starvation is applied uniformly to all isohydric species (from observations of piñon pine; Breshears et al., in press). Figure 12 demonstrates that the isohydry/anisohydry continuum partitions species vulnerability to drought as a function of drought duration. For example, if drought were relieved by precipitation after 10 months, one anisohydric species (sunflower) would have died but all other species would have survived. By contrast, if drought-relieving precipitation did not occur until 15 months then all isohydric species would have died. If the drought were more intense, such that the drying curve were steeper, then the likelihood of more anisohydric species succumbing earlier would increase; and vice versa, if the drought were less intense, such that the drying curve was shallower, proportionally more isohydric species would succumb because they would reach carbon starvation long before anisohydric species reach Ψcrit. Perhaps the most important observation from Fig. 12 is the clear need for information regarding the time required for carbon starvation to occur. Likewise, this analysis points to the need to understand interactions with biotic mortality agents and within-species variation in Ψ of zero Gs (isohydric) and Ψcrit (anisohydric); such variation is known to occur in response to tree height (Yoder et al., 1994; McDowell et al., 2002a; Barnard & Ryan, 2003) or soil texture (Hacke et al., 2000), and may occur in other situations. However, variation in these variables is likely to move species timing of mortality only slightly relative to the larger general pattern of mortality shown in Fig. 12. The patterns in Fig. 12 support the concept that isohydric species are more likely to die of carbon starvation than hydraulic failure, and that partitioning of mortality between isohydric and anishydric plants is a function of drought intensity and duration (Figs 3 and 10).
Figure 12. Theoretical mortality response of isohydric and anisohydric species to drought. The curve illustrates the decline in rhizosphere water potential under a 30 month drought scenario. For isohydric species, the horizontal dotted lines extend from where the Ψleaf at zero Gs crosses the rhizosphere Ψ curve to the date of death via carbon starvation (filled symbols). For anisohydric species, Ψcrit is the Ψstem or Ψleaf at which some portion of the plant xylem experiences Ks = 0, and is plotted on top of the rhizosphere Ψ curve (open symbols). For isohydric species, the length of time until carbon starvation is based on observations of piñon pine (see text). Isohydric species (solid symbols): flowering dogwood (square), tatuba (circle), black elderberry (triangle), piñon pine (diamond). Anisohydric species (open symbols): sunflower (downward triangle), sugar maple (hexagon), eucalyptus (square), juniper (upward triangle). Sources are from the literature review provided in Section V.3, Isohydry and anisohydry.
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Drought may also reduce photosynthesis by other mechanisms, such as loss of leaf turgor (Dreyer et al., 1992; Rodriguez et al., 1993; Kolb & Sperry, 1999) and leaf shedding (Tyree et al., 1993 and citations mentioned earlier). When elevated temperatures accompany drought (Breshears et al., 2005), a nonhydraulic mechanism of reduced photosynthesis may result from the impact of temperature on photosynthetic optima, both on electron transport and Rubisco activity (Berry & Bjorkman, 1980; Sage & Kubien, 2007). For our case study, juniper has a higher temperature optima for peak photosynthesis (21 vs 17°C) and a broader temperature range above which 90% of maximum photosynthesis is sustained (16.5 vs 14.2°C) than does piñon (Barnes, 1986). Adaptation of the biochemical machinery driving photosynthesis to rising temperatures may occur if the temperature rise is consistent and slow, but will be insufficient if temperature extremes happen rapidly and infrequently. Temperature impacts on photosynthesis occur in broadleaf species that have high interception of solar radiation, and may possibly occur in needleleaf species during periods of low wind speed and high radiative load (Kolb & Robberecht, 1996; Martin et al., 1999). Atmospheric conditions that promote high leaf temperatures in needleleaf species are not frequent; however, just a single day of lethal conditions could severely impede future photosynthesis if there are no stored carbohydrates for use in repair of the photosynthetic apparatus, such as during a severe drought. Mesophyll conductance to CO2 also shows temperature optima, and therefore may also be a constraint on photosynthesis under temperature extremes (Diaz-Espejo et al., 2007).
In addition to reductions in carbon uptake there are increases in carbon use for maintenance respiration and perhaps below-ground root production during drought. Carbon allocation to maintenance respiration may increase as a result of elevated temperatures of foliage, sapwood and roots (Amthor, 2000), although acclimation to temperature and drought may occur that would minimize this effect (Bryla et al., 1997; King et al., 2006). During relatively mild droughts, allocation to roots and sapwood may increase to maintain adequate Kl if there are carbohydrates available (Gower et al., 1994; Cinnirella et al., 2002; Kozlowski & Pallardy, 2002).
Carbon starvation may facilitate mortality from biotic agents (Fig. 3) when carbon starvation and the population abundance of these agents are synchronous (Schoeneweiss, 1981; Marçais & Bréda, 2007). This synchrony is mediated by the degree of water stress imposed on the trees. The growth-differentiation balance hypothesis (Herms & Mattson, 1992; Reeve et al., 1995; Stamp, 2003; Fine et al., 2006) predicts a curvilinear relationship between water stress and carbon allocation to resin because moderate water stress impacts photosynthesis slightly but shifts carbon allocation from growth to storage and defensive chemicals. This shift in carbon allocation results in greater resin flow from phloem wounds in moderately stressed compared with nonstressed trees (Lorio, 1986; Dunn & Lorio, 1993). However, severe droughts cause a cessation of carbon allocation to all sinks, including resin defense, when photosynthetic carbon gain is near zero (Christiansen et al., 1987; Waring, 1987; Herms & Mattson, 1992; Lewinsohn et al., 1993; Reeve et al., 1995; Stamp, 2003). Consistent with the carbon-starvation hypothesis, ponderosa pine (Pinus ponderosa) resin flow decreases with stresses that reduce radial growth (Kolb et al., 1998; McDowell et al., 2007). Drought duration is important because stored carbohydrates may temporarily buffer effects on carbon allocation to resin (consistent with Fig. 10). Studies examining carbohydrate content of tissues in relation to drought and mortality are consistent with the idea that reduced carbon storage is associated with susceptibility to biotic mortality agents (Marçais & Bréda, 2007).
Carbon starvation may also facilitate biotic attack via changes in the release of volatile attractants or changes in the quality of forage for biotic agents. The production of ethanol and other volatiles changes during drought in order to preserve cellular function (Kimmerer & Kozlowski, 1982; Tadege et al., 1999) and perhaps as a byproduct of increased tissue temperatures associated with reduced transpiration (Hietz et al., 2005). Such increases in volatile emissions may be used by insects to locate stressed plants (Kelsey, 2001; Kelsey & Joseph, 2003; Manter & Kelsey, 2008). The composition of defensive compounds within plant tissues may also shift during drought, though little conclusive evidence yet exists (Tognetti et al., 1997; Thoss & Byers, 2006). Host palatability may improve or decline during drought, depending in part on soil nutrient availability (Price, 1991; Waring & Cobb, 1992; Warren et al., 1999; Erbilgin & Raffa, 2000; Campo & Dirzo, 2003; Rieske et al., 2003; Hui & Jin, 2004) and phloem thickness (Amman, 1972; Haack et al., 1984; Amman & Pasek, 1986). Lastly, predisposition to biotic agents from carbon starvation may feed back to hydraulic failure as the proximal cause of mortality. For many pine species, bark beetles attack stressed trees and inoculate them with fungi that occludes the xylem, functionally halting transpiration (Larsson et al., 1983; Waring & Pitman, 1985; Lorio, 1986; Christiansen et al., 1987). It remains an open question whether hydraulic failure or carbon starvation per se leads to mortality in these cases (Wullschleger et al., 2004).