Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality.
TL;DR: Evidence is provided for a relationship between hydraulic regulation of water status and carbohydrate depletion during terminal drought and the role that duration of drought plays in facilitating carbohydrate consumption.
Abstract: Summary
Plant survival during drought requires adequate hydration in living tissues and carbohydrate reserves for maintenance and recovery. We hypothesized that tree growth and hydraulic strategy determines the intensity and duration of the ‘physiological drought’, thereby affecting the relative contributions of loss of hydraulic function and carbohydrate depletion during mortality.
We compared patterns in growth rate, water relations, gas exchange and carbohydrate dynamics in three tree species subjected to prolonged drought.
Two Eucalyptus species (E. globulus, E. smithii) exhibited high growth rates and water-use resulting in rapid declines in water status and hydraulic conductance. In contrast, conservative growth and water relations in Pinus radiata resulted in longer periods of negative carbon balance and significant depletion of stored carbohydrates in all organs. The ongoing demand for carbohydrates from sustained respiration highlighted the role that duration of drought plays in facilitating carbohydrate consumption.
Two drought strategies were revealed, differentiated by plant regulation of water status: plants maximized gas exchange, but were exposed to low water potentials and rapid hydraulic dysfunction; and tight regulation of gas exchange at the cost of carbohydrate depletion. These findings provide evidence for a relationship between hydraulic regulation of water status and carbohydrate depletion during terminal drought.
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TL;DR: This work focuses on the current understanding of tree hydraulic performance under drought, the identification of physiological thresholds that precipitate mortality and the mechanisms of recovery after drought, and the potential application of hydraulic thresholds to process-based models that predict mortality.
Abstract: Severe droughts have caused widespread tree mortality across many forest biomes with profound effects on the function of ecosystems and carbon balance. Climate change is expected to intensify regional-scale droughts, focusing attention on the physiological basis of drought-induced tree mortality. Recent work has shown that catastrophic failure of the plant hydraulic system is a principal mechanism involved in extensive crown death and tree mortality during drought, but the multi-dimensional response of trees to desiccation is complex. Here we focus on the current understanding of tree hydraulic performance under drought, the identification of physiological thresholds that precipitate mortality and the mechanisms of recovery after drought. Building on this, we discuss the potential application of hydraulic thresholds to process-based models that predict mortality.
811 citations
TL;DR: It is shown 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.
Abstract: 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 pinon 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.
624 citations
Cites background from "Drought response strategies define ..."
...Recent evidence contrasting three species across the iso-anisohydry continuum strongly supported this hypothesis (Mitchell et al. 2013)....
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TL;DR: Conceptual and mathematical models of NSC dynamics, recent observations and experiments at the organismal scale, and advances in plant physiology that have provided a better understanding of the dynamics of woody plant NSC are reviewed.
Abstract: Nonstructural carbon (NSC) provides the carbon and energy for plant growth and survival. In woody plants, fundamental questions about NSC remain unresolved: Is NSC storage an active or passive process? Do older NSC reserves remain accessible to the plant? How is NSC depletion related to mortality risk? Herein we review conceptual and mathematical models of NSC dynamics, recent observations and experiments at the organismal scale, and advances in plant physiology that have provided a better understanding of the dynamics of woody plant NSC. Plants preferentially use new carbon but can access decade-old carbon when the plant is stressed or physically damaged. In addition to serving as a carbon and energy source, NSC plays important roles in phloem transport, osmoregulation, and cold tolerance, but how plants regulate these competing roles and NSC depletion remains elusive. Moving forward requires greater synthesis of models and data and integration across scales from -omics to ecology.
512 citations
Cites background from "Drought response strategies define ..."
...Don) and two fast-growing Eucalyptus species showed depleted NSC for Pinus but not Eucalyptus (86)....
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...Consequences of resource limitation for recovery from repeated defoliation in Eucalyptus globulus Labilladière....
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...A recent drought experiment using one conservative-growing species (Pinus radiata D. Don) and two fast-growing Eucalyptus species showed depleted NSC for Pinus but not Eucalyptus (86)....
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...For several months after a defoliation event, young Eucalyptus plants did not experience carbon limitation (5), and repeated defoliation events (spaced by several years of canopy recovery) led to an accumulation of NSC in Pinus nigra Arnold (96)....
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TL;DR: In this article, the authors performed a meta-analysis on species' mortality rates across 475 species from 33 studies around the globe to assess which traits determine a species’ mortality risk and found that species-specific mortality anomalies from community mortality rate in a given drought were associated with plant hydraulic traits.
Abstract: Drought-induced tree mortality has been observed globally and is expected to increase under climate change scenarios, with large potential consequences for the terrestrial carbon sink. Predicting mortality across species is crucial for assessing the effects of climate extremes on forest community biodiversity, composition, and carbon sequestration. However, the physiological traits associated with elevated risk of mortality in diverse ecosystems remain unknown, although these traits could greatly improve understanding and prediction of tree mortality in forests. We performed a meta-analysis on species’ mortality rates across 475 species from 33 studies around the globe to assess which traits determine a species’ mortality risk. We found that species-specific mortality anomalies from community mortality rate in a given drought were associated with plant hydraulic traits. Across all species, mortality was best predicted by a low hydraulic safety margin—the difference between typical minimum xylem water potential and that causing xylem dysfunction—and xylem vulnerability to embolism. Angiosperms and gymnosperms experienced roughly equal mortality risks. Our results provide broad support for the hypothesis that hydraulic traits capture key mechanisms determining tree death and highlight that physiological traits can improve vegetation model prediction of tree mortality during climate extremes.
506 citations
TL;DR: Current knowledge about responses of tree roots to drought supports the view that tree roots are well equipped to withstand drought situations and maintain morphological and physiological functions as long as possible.
Abstract: The ongoing climate change is characterized by increased temperatures and altered precipitation patterns In addition, there has been an increase in both the frequency and intensity of extreme climatic events such as drought Episodes of drought induce a series of interconnected effects, all of which have the potential to alter the carbon balance of forest ecosystems profoundly at different scales of plant organization and ecosystem functioning During recent years, considerable progress has been made in the understanding of how aboveground parts of trees respond to drought and how these responses affect carbon assimilation In contrast, processes of belowground parts are relatively underrepresented in research on climate change In this review, we describe current knowledge about responses of tree roots to drought Tree roots are capable of responding to drought through a variety of strategies that enable them to avoid and tolerate stress Responses include root biomass adjustments, anatomical alterations, and physiological acclimations The molecular mechanisms underlying these responses are characterized to some extent, and involve stress signaling and the induction of numerous genes, leading to the activation of tolerance pathways In addition, mycorrhizas seem to play important protective roles The current knowledge compiled in this review supports the view that tree roots are well equipped to withstand drought situations and maintain morphological and physiological functions as long as possible Further, the reviewed literature demonstrates the important role of tree roots in the functioning of forest ecosystems and highlights the need for more research in this emerging field
501 citations
Cites result from "Drought response strategies define ..."
...Mitchell et al. (2013) found a similar result when applying a lethal drought treatment to two eucalypt (Eucalyptus globulus, E. smithii) and one pine (Pinus radiata) species....
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References
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United States Geological Survey1, University of Arizona2, University of Batna3, Oregon State University4, Los Alamos National Laboratory5, Centre national de la recherche scientifique6, Swiss Federal Institute for Forest, Snow and Landscape Research7, Natural Resources Canada8, University of California, Berkeley9, University of Granada10, Northern Research Institute11, Forest Research Institute12, Food and Agriculture Organization13, University of Montana14, Northern Arizona University15
TL;DR: In this paper, the authors present the first global assessment of recent tree mortality attributed to drought and heat stress and identify key information gaps and scientific uncertainties that currently hinder our ability to predict tree mortality in response to climate change and emphasizes the need for a globally coordinated observation system.
5,811 citations
"Drought response strategies define ..." refers background in this paper
...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)....
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...Global analyses of forest vulnerability and droughtrelated 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)....
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...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)....
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TL;DR: A hydraulically based theory considering carbon balance and insect resistance that allowed development and examination of hypotheses regarding survival and mortality was developed, and incorporating this hydraulic framework may be effective for modeling plant survival andortality under future climate conditions.
Abstract: Summary Severe droughts have been associated with regional-scale forest mortality worldwide. Climate change is expected to exacerbate regional mortality events; however, pre- diction 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
3,302 citations
"Drought response strategies define ..." refers background in this paper
...These responses represent very different strategies along the drought response continuum and support predictions of McDowell et al. (2008), whereby the drought conditions and associated physiological adaptations can alter the relative contributions from hydraulic dysfunction and the exhaustion of…...
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...Our study shows for the first time that prolonged periods of negative carbon balance during drought causes significant depletion in whole-plant TNC and provides evidence for carbohydrate starvation as a contributing process for mortality, as postulated by McDowell et al. (2008)....
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...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)....
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TL;DR: The results quantify a trigger leading to rapid, drought-induced die-off of overstory woody plants at subcontinental scale and highlight the potential for such die-offs to be more severe and extensive for future global-change-type drought under warmer conditions.
Abstract: Future drought is projected to occur under warmer temperature conditions as climate change progresses, referred to here as global-change-type drought, yet quantitative assessments of the triggers and potential extent of drought-induced vegetation die-off remain pivotal uncertainties in assessing climate-change impacts. Of particular concern is regional-scale mortality of overstory trees, which rapidly alters ecosystem type, associated ecosystem properties, and land surface conditions for decades. Here, we quantify regional-scale vegetation die-off across southwestern North American woodlands in 2002-2003 in response to drought and associated bark beetle infestations. At an intensively studied site within the region, we quantified that after 15 months of depleted soil water content, >90% of the dominant, overstory tree species (Pinus edulis, a pinon) died. The die-off was reflected in changes in a remotely sensed index of vegetation greenness (Normalized Difference Vegetation Index), not only at the intensively studied site but also across the region, extending over 12,000 km2 or more; aerial and field surveys confirmed the general extent of the die-off. Notably, the recent drought was warmer than the previous subcontinental drought of the 1950s. The limited, available observations suggest that die-off from the recent drought was more extensive than that from the previous drought, extending into wetter sites within the tree species' distribution. Our results quantify a trigger leading to rapid, drought-induced die-off of overstory woody plants at subcontinental scale and highlight the potential for such die-off to be more severe and extensive for future global-change-type drought under warmer conditions.
1,992 citations
University of Western Sydney1, University of Ulm2, University of Tasmania3, Institut national de la recherche agronomique4, Blaise Pascal University5, University of Bordeaux6, Brown University7, National University of Patagonia San Juan Bosco8, James Cook University9, Macquarie University10, University of Alberta11, California State University, Bakersfield12, Leiden University13, University of Guelph14, University of Innsbruck15, University of Edinburgh16, Commonwealth Scientific and Industrial Research Organisation17, University of Trieste18, University of California, Santa Cruz19, University of Utah20, George Washington University21, Missouri Botanical Garden22
TL;DR: In this article, the authors 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.
Abstract: 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(1). One primary cause of productivity loss and plant mortality during drought is hydraulic failure(2-4). 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 (<1 megapascal) 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(5,6). 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(7,8).
1,864 citations
TL;DR: The role du couvert dans les echanges avec l'atmosphere is rappele puis integre dans l'analyse des reductions de bilan d'eau and de carbone in 2003 dus a regulation stomatique as discussed by the authors.
Abstract: La secheresse exceptionnelle de 2003 a ete l'occasion de faire le point de nos connaissances sur les mecanismes ecophysiologiques permettant aux arbres de traverser un tel evenement climatique extreme. L'analyse a ete conduite a l'echelle de l'arbre et du peuplement, tandis que l'intensite de la secheresse a ete quantifiee a l'aide d'un calcul de bilan hydrique sur neuf sites forestiers europeens contrastes du reseau CARBOEUROPE. Le role du couvert dans les echanges avec l'atmosphere est rappele puis integre dans l'analyse des reductions de bilan d'eau et de carbone en 2003 dus a la regulation stomatique. Les caracteristiques du complexe sol-racine, important a la fois pour l'acces a la ressource et a l'efficience de son absorption, constituent un des premiers traits d'adaptation a la secheresse. La reponse et les adaptations des especes ont surtout ete analysees en termes de diversite inter-specifique de fonctionnement hydraulique et du couplage entre proprietes hydrauliques et regulation stomatique. Enfin, nous discutons l'hypothese selon la quelle les dysfonctionnements hydrauliques ou les deficits de mise en reserve sont impliques dans les reactions differees de croissance, de developpement, d'induction de deperissement. Par exemple, des mesures de reserves glucidiques dans les troncs de chenes menees en fin d'ete 2003 ont permis de predire l'etat des couronnes des arbres au printemps 2004. Les faibles taux d'amidon etaient associes a une forte mortalite de branches et de jeunes pousses.
1,553 citations
"Drought response strategies define ..." refers background in this paper
...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…...
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