Despite decades of research on plant drought tolerance, the physiological mechanisms by which trees succumb to drought are still under debate. We report results from an experiment designed to ...separate and test the current leading hypotheses of tree mortality. We show that piñon pine (Pinus edulis) trees can die of both hydraulic failure and carbon starvation, and that during drought, the loss of conductivity and carbohydrate reserves can also co‐occur. Hydraulic constraints on plant carbohydrate use determined survival time: turgor loss in the phloem limited access to carbohydrate reserves, but hydraulic control of respiration prolonged survival. Our data also demonstrate that hydraulic failure may be associated with loss of adequate tissue carbohydrate content required for osmoregulation, which then promotes failure to maintain hydraulic integrity.
This study describes results of the first test of the leading, but controversial, hypotheses regarding how trees die during drought. Our results show that all of the hypothesized mortality mechanisms can occur in trees of the same, relatively isohydric species, but both the progress of symptoms and survival time during drought may vary with individual trees even in similar environmental conditions. The mortality process seems to be controlled by hydraulic limitations on carbohydrate transport and utilization, which determines plant survival time.
Ecosystem models have difficulty predicting plant drought responses, partially from uncertainty in the stomatal response to water deficits in soil and atmosphere. We evaluate a ‘supply–demand’ theory ...for water-limited stomatal behavior that avoids the typical scaffold of empirical response functions. The premise is that canopy water demand is regulated in proportion to threat to supply posed by xylem cavitation and soil drying.
The theory was implemented in a trait-based soil–plant–atmosphere model. The model predicted canopy transpiration (E), canopy diffusive conductance (G), and canopy xylem pressure (P
canopy) from soil water potential (P
soil) and vapor pressure deficit (D).
Modeled responses to D and P
soil were consistent with empirical response functions, but controlling parameters were hydraulic traits rather than coefficients. Maximum hydraulic and diffusive conductances and vulnerability to loss in hydraulic conductance dictated stomatal sensitivity and hence the iso- to anisohydric spectrum of regulation. The model matched wide fluctuations in G and P
canopy across nine data sets from seasonally dry tropical forest and piñon–juniper woodland with < 26% mean error.
Promising initial performance suggests the theory could be useful in improving ecosystem models. Better understanding of the variation in hydraulic properties along the root–stem–leaf continuum will simplify parameterization.
Drought‐induced forest mortality is an increasing global problem with wide‐ranging consequences, yet mortality mechanisms remain poorly understood. Depletion of non‐structural carbohydrate (NSC) ...stores has been implicated as an important mechanism in drought‐induced mortality, but experimental field tests are rare. We used an ecosystem‐scale precipitation manipulation experiment to evaluate leaf and twig NSC dynamics of two co‐occurring conifers that differ in patterns of stomatal regulation of water loss and recent mortality: the relatively desiccation‐avoiding piñon pine (Pinus edulis) and the relatively desiccation‐tolerant one‐seed juniper (Juniperus monosperma). Piñon pine experienced 72% mortality after 13–25 months of experimental drought and juniper experienced 20% mortality after 32–47 months. Juniper maintained three times more NSC in the foliage than twigs, and converted NSC to glucose and fructose under drought, consistent with osmoregulation requirements to maintain higher stomatal conductance during drought than piñon. Despite these species differences, experimental drought caused decreased leaf starch content in dying trees of both species (P < 0.001). Average dry‐season leaf starch content was also a good predictor of drought‐survival time for both species (R² = 0.93). These results, along with observations of drought‐induced reductions to photosynthesis and growth, support carbon limitation as an important process during mortality of these two conifer species.
The ability of plants to supply water to their leaves is intimately associated with survival. Water supply to leaves depends on maintaining an intact water column in the xylem from the roots to ...shoots. Because this hydraulic pathway is under tension, it is vulnerable to breakage through the induction of air emboli (cavitation). Although the physiological benefit of resistance to water-stress-induced xylem cavitation for desiccation tolerance is clear, there is considerable interspecific variation within and across climates. To understand the adaptive significance of this variation and the potential trade-off with water transport, we compiled a database of 167 species from 50 seed plant families and examined relationships among resistance to xylem cavitation, water transport capacity (as determined by the specific conductivity of xylem Ks), and climate. Relationships were evaluated using standard cross-species correlations (r). Because inferences about the adaptive significance of these correlations can be biased by the potential similarity of closely related species, we also analyzed our data using phylogenetically independent contrast correlations (PIC) calculated over a range of alternate seed plant phylogenies. Resistance to cavitation, expressed as the xylem tension at which 50% of hydraulic conductivity was lost (Ψ50), ranged from -0.18 to -9.9 MPa for angiosperms and from -1.5 to -14.1 MPa for conifers. Conifers were most resistant to cavitation, with mean Ψ5080% more negative than angiosperms. In contrast, Kswas 270% higher in angiosperms than conifers. Across all species, cavitation resistance increased with decreasing mean annual precipitation. However, significant phylogenetically independent contrast correlations between Ψ50and annual precipitation were found within the evergreen angiosperms and conifers but not in the deciduous angiosperms. Thus, the adaptive significance of increased resistance to cavitation as a mechanism of drought tolerance may be of primary importance in evergreen angiosperms and conifers. In contrast, analysis of independent contrasts indicated that Ksincreased with decreasing rainfall in deciduous angiosperms, whereas there was no association between Ksand water availability for evergreen angiosperms and conifers. These results suggest that the evolution of increased Ksmay be a critical adaptation to water limitation in deciduous angiosperms. Although there was a significant cross-species correlation between Ψ50and Ks, this relationship was not supported by the independent contrast correlation, suggesting that the evolutionary basis for a trade-off between cavitation resistance and water transport capacity is weak.
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.
To test the hypothesis that drought predisposes trees to insect attacks, we quantified the effects of water availability on insect attacks, tree resistance mechanisms, and mortality of mature piñon ...pine (Pinus edulis) and one-seed juniper (Juniperus monosperma) using an experimental drought study in New Mexico, USA.
The study had four replicated treatments (40 × 40 m plot/replicate): removal of 45% of ambient annual precipitation (H2O−); irrigation to produce 125% of ambient annual precipitation (H2O+); a drought control (C) to quantify the impact of the drought infrastructure; and ambient precipitation (A).
Piñon began dying 1 yr after drought initiation, with higher mortality in the H2O− treatment relative to other treatments. Beetles (bark/twig) were present in 92% of dead trees. Resin duct density and area were more strongly affected by treatments and more strongly associated with piñon mortality than direct measurements of resin flow. For juniper, treatments had no effect on insect resistance or attacks, but needle browning was highest in the H2O− treatment.
Our results provide strong evidence that ≥ 1 yr of severe drought predisposes piñon to insect attacks and increases mortality, whereas 3 yr of the same drought causes partial canopy loss in juniper.
The effects of short‐term drought on soil microbial communities remain largely unexplored, particularly at large scales and under field conditions. We used seven experimental sites from two ...continents (North America and Australia) to evaluate the impacts of imposed extreme drought on the abundance, community composition, richness, and function of soil bacterial and fungal communities. The sites encompassed different grassland ecosystems spanning a wide range of climatic and soil properties. Drought significantly altered the community composition of soil bacteria and, to a lesser extent, fungi in grasslands from two continents. The magnitude of the fungal community change was directly proportional to the precipitation gradient. This greater fungal sensitivity to drought at more mesic sites contrasts with the generally observed pattern of greater drought sensitivity of plant communities in more arid grasslands, suggesting that plant and microbial communities may respond differently along precipitation gradients. Actinobateria, and Chloroflexi, bacterial phyla typically dominant in dry environments, increased their relative abundance in response to drought, whereas Glomeromycetes, a fungal class regarded as widely symbiotic, decreased in relative abundance. The response of Chlamydiae and Tenericutes, two phyla of mostly pathogenic species, decreased and increased along the precipitation gradient, respectively. Soil enzyme activity consistently increased under drought, a response that was attributed to drought‐induced changes in microbial community structure rather than to changes in abundance and diversity. Our results provide evidence that drought has a widespread effect on the assembly of microbial communities, one of the major drivers of soil function in terrestrial ecosystems. Such responses may have important implications for the provision of key ecosystem services, including nutrient cycling, and may result in the weakening of plant–microbial interactions and a greater incidence of certain soil‐borne diseases.
Direct and indirect effects of drought and environmental conditions on bacterial community composition and microbial activity.
Global climate change is projected to produce warmer, longer, and more frequent droughts, referred to here as "global change-type droughts", which have the potential to trigger widespread tree ...die-off. However, drought-induced tree mortality cannot be predicted with confidence, because long-term field observations of plant water stress prior to, and culminating in, mortality are rare, precluding the development and testing of mechanisms. Here, we document plant water stress in two widely distributed, co-occurring species, piñon pine (Pinus edulis) and juniper (Juniperus monosperma), over more than a decade, leading up to regional-scale die-off of piñon pine trees in response to global change-related drought. Piñon leaf water potentials remained substantially below their zero carbon assimilation point for at least 10 months prior to dying, in contrast to those of juniper, which rarely dropped below their zero-assimilation point. These data suggest that piñon mortality was driven by protracted water stress, leading to carbon starvation and associated increases in susceptibility to other disturbances (eg bark beetles), a finding that should help to improve predictions of mortality during drought.
Drought‐related tree mortality occurs globally and may increase in the future, but we lack sufficient mechanistic understanding to accurately predict it. Here we present the first field assessment of ...the physiological mechanisms leading to mortality in an ecosystem‐scale rainfall manipulation of a piñon–juniper (Pinus edulis–Juniperus monosperma) woodland. We measured transpiration (E) and modelled the transpiration rate initiating hydraulic failure (Ecrit). We predicted that isohydric piñon would experience mortality after prolonged periods of severely limited gas exchange as required to avoid hydraulic failure; anisohydric juniper would also avoid hydraulic failure, but sustain gas exchange due to its greater cavitation resistance. After 1 year of treatment, 67% of droughted mature piñon died with concomitant infestation by bark beetles (Ips confusus) and bluestain fungus (Ophiostoma spp.); no mortality occurred in juniper or in control piñon. As predicted, both species avoided hydraulic failure, but safety margins from Ecrit were much smaller in piñon, especially droughted piñon, which also experienced chronically low hydraulic conductance. The defining characteristic of trees that died was a 7 month period of near‐zero gas exchange, versus 2 months for surviving piñon. Hydraulic limits to gas exchange, not hydraulic failure per se, promoted drought‐related mortality in piñon pine.
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