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PMID: 29950621 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Triggers of tree mortality under drought.

Nature ·Vol. 558 ·No. 7711 ·2018-00-00 ·Pages 531-539

Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE

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.

MeSH Terms
Acclimatization/physiology Droughts Natural Disasters Stress, Physiological/physiology Trees/anatomy & histology,genetics,physiology Water/metabolism,physiology Xylem/metabolism
Chemicals
Water
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Choat Brendan
Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales, Australia. b.choat@westernsydney.edu.au.
Brodribb Timothy J
School of Biological Sciences, University of Tasmania, Hobart, Tasmania, Australia.
Brodersen Craig R
School of Forestry and Environmental Studies, Yale University, New Haven, CT, USA.
Duursma Remko A
Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales, Australia.
López Rosana
Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales, Australia. | PIAF, INRA, Université Clermont Auvergne, Clermont-Ferrand, France.
Medlyn Belinda E
Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales, Australia.
References (133)
133 references, click to expand
  1. Forests and climate change: forcings, feedbacks, and the climate benefits of forests.
    Bonan, G. B. Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320, 1444–1449 (2008). PMID: 18556546 DOI
  2. A large and persistent carbon sink in the world's forests.
    Pan, Y. et al. A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011). PMID: 21764754 DOI
  3. Zhu, Z. et al. Greening of the Earth and its drivers. Nat. Clim. Change 6, 791–795 (2016). DOI
  4. Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise.
    Keenan, T. F. et al. Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499, 324–327 (2013). PMID: 23842499 DOI
  5. Projected land photosynthesis constrained by changes in the seasonal cycle of atmospheric CO2.
    Wenzel, S., Cox, P. M., Eyring, V. & Friedlingstein, P. Projected land photosynthesis constrained by changes in the seasonal cycle of atmospheric CO2. Nature 538, 499–501 (2016). PMID: 27680704 DOI
  6. Climate extremes and the carbon cycle.
    Reichstein, M. et al. Climate extremes and the carbon cycle. Nature 500, 287–295 (2013). PMID: 23955228 DOI
  7. Trenberth, K. E. et al. Global warming and changes in drought. Nat. Clim. Change 4, 17–22 (2014). DOI
  8. Tyree, M. T. & Zimmermann, M. H. Xylem Structure and the Ascent of Sap (Springer, New York, 2002).
  9. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality.
    Adams, H. D. et al. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat. Ecol. Evol. 1, 1285–1291 (2017). PMID: 29046541 DOI
  10. Kursar, T. A. et al. Tolerance to low leaf water status of tropical tree seedlings is related to drought performance and distribution. Funct. Ecol. 23, 93–102 (2009). DOI
  11. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?
    McDowell, N. et al. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol. 178, 719–739 (2008). This study introduces a theoretical framework for understanding physiological mechanisms that underpin drought-induced mortality in trees. PMID: 18422905 DOI
  12. Hydraulic failure defines the recovery and point of death in water-stressed conifers.
    Brodribb, T. J. & Cochard, H. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol. 149, 575–584 (2009). This study quantitatively links hydraulic failure thresholds to whole-plant mortality. PMID: 19011001 DOI
  13. Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees.
    Urli, M. et al. Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol. 33, 672–683 (2013). PMID: 23658197 DOI
  14. Shoot desiccation and hydraulic failure in temperate woody angiosperms during an extreme summer drought.
    Nardini, A., Battistuzzo, M. & Savi, T. Shoot desiccation and hydraulic failure in temperate woody angiosperms during an extreme summer drought. New Phytol. 200, 322–329 (2013). PMID: 23593942 DOI
  15. Chaparral Shrub Hydraulic Traits, Size, and Life History Types Relate to Species Mortality during California's Historic Drought of 2014.
    Venturas, M. D. et al. Chaparral shrub hydraulic traits, size, and life history types relate to species mortality during California’s historic drought of 2014. PLoS ONE 11, e0159145 (2016). PMID: 27391489 DOI
  16. The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off.
    Anderegg, W. R. et al. The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proc. Natl Acad. Sci. USA 109, 233–237 (2012). PMID: 22167807 DOI
  17. Shoot dieback during prolonged drought in Ceanothus (Rhamnaceae) chaparral of California: a possible case of hydraulic failure.
    Davis, S. D. et al. Shoot dieback during prolonged drought in Ceanothus (Rhamnaceae) chaparral of California: a possible case of hydraulic failure. Am. J. Bot. 89, 820–828 (2002). PMID: 21665682 DOI
  18. The interdependence of mechanisms underlying climate-driven vegetation mortality.
    McDowell, N. G. et al. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol. Evol. 26, 523–532 (2011). PMID: 21802765 DOI
  19. Elevated [CO2] does not ameliorate the negative effects of elevated temperature on drought-induced mortality in Eucalyptus radiata seedlings.
    Duan, H. et al. Elevated [CO2] does not ameliorate the negative effects of elevated temperature on drought-induced mortality in Eucalyptus radiata seedlings. Plant Cell Environ. 37, 1598–1613 (2014). PMID: 24372529 DOI
  20. Allen, C. D., Breshears, D. D. & McDowell, N. G. On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6, 129 (2015). DOI
  21. Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought.
    Carnicer, J. et al. Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proc. Natl Acad. Sci. USA 108, 1474–1478 (2011). PMID: 21220333 DOI
  22. Europe-wide reduction in primary productivity caused by the heat and drought in 2003.
    Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 (2005). PMID: 16177786 DOI
  23. The 2010 Amazon drought.
    Lewis, S. L., Brando, P. M., Phillips, O. L., van der Heijden, G. M. F. & Nepstad, D. The 2010 Amazon drought. Science 331, 554 (2011). PMID: 21292971 DOI
  24. Progressive forest canopy water loss during the 2012-2015 California drought.
    Asner, G. P. et al. Progressive forest canopy water loss during the 2012–2015 California drought. Proc. Natl Acad. Sci. USA 113, E249–E255 (2016). PMID: 26712020 DOI
  25. Tree mortality from an exceptional drought spanning mesic to semiarid ecoregions.
    Moore, G. W. et al. Tree mortality from an exceptional drought spanning mesic to semiarid ecoregions. Ecol. Appl. 26, 602–611 (2016). PMID: 27209798 DOI
  26. USDA Forest Service Pacific Southwest Region. Aerial Detection Surveys Report: Summary for May 15–19 Report No. fseprd506698 (USDA Forest Service, 2016).
  27. Allen, C. D. et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For. Ecol. Manage. 259, 660–684 (2010). This study summarizes forest mortality events associated with drought and heat over the last four decades. DOI
  28. Duke, N. C. et al. Large-scale dieback of mangroves in Australia’s Gulf of Carpentaria: a severe ecosystem response, coincidental with an unusually extreme weather event. Mar. Freshw. Res. 68, 1816–1829 (2017). DOI
  29. Drought sensitivity of the Amazon rainforest.
    Phillips, O. L. et al. Drought sensitivity of the Amazon rainforest. Science 323, 1344–1347 (2009). PMID: 19265020 DOI
  30. Effect of 7 yr of experimental drought on vegetation dynamics and biomass storage of an eastern Amazonian rainforest.
    da Costa, A. C. L. et al. Effect of 7 yr of experimental drought on vegetation dynamics and biomass storage of an eastern Amazonian rainforest. New Phytol. 187, 579–591 (2010). PMID: 20553386 DOI
  31. The ecology, distribution, conservation and management of large old trees.
    Lindenmayer, D. B. & Laurance, W. F. The ecology, distribution, conservation and management of large old trees. Biol. Rev. Camb. Philos. Soc. 92, 1434–1458 (2016). PMID: 27383287 DOI
  32. Slatyer, R. O. Plant–Water relationships (Academic, New York, 1967).
  33. Debenedetti, P. G. Metastable Liquids: Concepts and Principles (Princeton Univ. Press, Princeton, 1996).
  34. Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots.
    Rodriguez-Dominguez, C. M., Carins Murphy, M. R., Lucani, C. & Brodribb, T. J. Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots. New Phytol. 218, 1025–1035 (2018). PMID: 29528498 DOI
  35. Scholander, P. F., Hammel, H. T., Bradstreet, E. D. & Hemmingsen, E. A. Sap pressure in vascular plants. Science 148, 339–346 (1965).
  36. Hochberg, U. et al. Stomatal closure, basal leaf embolism and shedding protect the hydraulic integrity of grape stems. Plant Physiol. (2017).
  37. Plant resistance to drought depends on timely stomatal closure.
    Martin-StPaul, N., Delzon, S. & Cochard, H. Plant resistance to drought depends on timely stomatal closure. Ecol. Lett. 20, 1437–1447 (2017). The absolute limit at which stomata must close to avoid mortality under drought is described. PMID: 28922708 DOI
  38. Tree hydraulic traits are coordinated and strongly linked to climate-of-origin across a rainfall gradient.
    Li, X. et al. Tree hydraulic traits are coordinated and strongly linked to climate-of-origin across a rainfall gradient. Plant Cell Environ. 41, 646–660 (2018). PMID: 29314083 DOI
  39. The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions?
    Leigh, A., Sevanto, S., Close, J. D. & Nicotra, A. B. The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions? Plant Cell Environ. 40, 237–248 (2017). PMID: 28026874 DOI
  40. Powles, S. B. Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol. 35, 15–44 (1984). DOI
  41. Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality.
    Mitchell, P. J. et al. Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytol. 197, 862–872 (2013). PMID: 23228042 DOI
  42. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses.
    Sevanto, S., McDowell, N. G., Dickman, L. T., Pangle, R. & Pockman, W. T. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ. 37, 153–161 (2014). PMID: 23730972 DOI
  43. A general ecophysiological framework for modelling the impact of pests and pathogens on forest ecosystems.
    Dietze, M. C. & Matthes, J. H. A general ecophysiological framework for modelling the impact of pests and pathogens on forest ecosystems. Ecol. Lett. 17, 1418–1426 (2014). PMID: 25168168 DOI
  44. Kerstiens, G. Cuticular water permeability and its physiological significance. J. Exp. Bot. 47, 1813–1832 (1996). DOI
  45. Transpiration in response to variation in microclimate and soil moisture in southeastern deciduous forests.
    Oren, R. & Pataki, D. E. Transpiration in response to variation in microclimate and soil moisture in southeastern deciduous forests. Oecologia 127, 549–559 (2001). PMID: 28547493 DOI
  46. Reversible Leaf Xylem Collapse: A Potential "Circuit Breaker" against Cavitation.
    Zhang, Y.-J., Rockwell, F. E., Graham, A. C., Alexander, T. & Holbrook, N. M. Reversible leaf xylem collapse: a potential “circuit breaker” against cavitation. Plant Physiol. 172, 2261–2274 (2016). PMID: 27733514 DOI
  47. Aquaporin-mediated changes in hydraulic conductivity of deep tree roots accessed via caves.
    McElrone, A. J. et al. Aquaporin-mediated changes in hydraulic conductivity of deep tree roots accessed via caves. Plant Cell Environ. 30, 1411–1421 (2007). PMID: 17897411 DOI
  48. Leaf hydraulics.
    Sack, L. & Holbrook, N. M. Leaf hydraulics. Annu. Rev. Plant Biol. 57, 361–381 (2006). PMID: 16669766 DOI
  49. Mechanical Failure of Fine Root Cortical Cells Initiates Plant Hydraulic Decline during Drought.
    Cuneo, I. F., Knipfer, T., Brodersen, C. R. & McElrone, A. J. Mechanical failure of fine root cortical cells initiates plant hydraulic decline during drought. Plant Physiol. 172, 1669–1678 (2016). PMID: 27621427 DOI
  50. Water storage capacitance and xylem tension in isolated branches of temperate and tropical trees.
    Borchert, R. & Pockman, W. T. Water storage capacitance and xylem tension in isolated branches of temperate and tropical trees. Tree Physiol. 25, 457–466 (2005). PMID: 15687094 DOI
  51. Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery.
    Choat, B., Brodersen, C. R. & McElrone, A. J. Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery. New Phytol. 205, 1095–1105 (2015). PMID: 25385085 DOI
  52. Visual quantification of embolism reveals leaf vulnerability to hydraulic failure.
    Brodribb, T. J. et al. Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytol. 209, 1403–1409 (2016). PMID: 26742653 DOI
  53. Tyree, M. T., Cochard, H., Cruiziat, P., Sinclair, B. & Ameglio, T. Drought-induced leaf shedding in walnut: evidence for vulnerability segmentation. Plant Cell Environ. 16, 879–882 (1993). DOI
  54. Rood, S. B., Patiño, S., Coombs, K. & Tyree, M. T. Branch sacrifice: cavitation-associated drought adaptation of riparian cottonwoods. Trees 14, 248–257 (2000). DOI
  55. Noninvasive Measurement of Vulnerability to Drought-Induced Embolism by X-Ray Microtomography.
    Choat, B. et al. Noninvasive measurement of vulnerability to drought-induced embolism by X-ray microtomography. Plant Physiol. 170, 273–282 (2016). PMID: 26527655 DOI
  56. Aridity drove the evolution of extreme embolism resistance and the radiation of conifer genus Callitris.
    Larter, M. et al. Aridity drove the evolution of extreme embolism resistance and the radiation of conifer genus Callitris. New Phytol. 215, 97–112 (2017). PMID: 28378882 DOI
  57. The evolution of water transport in plants: an integrated approach.
    Pittermann, J. The evolution of water transport in plants: an integrated approach. Geobiology 8, 112–139 (2010). PMID: 20156293 DOI
  58. Toward an index of desiccation time to tree mortality under drought.
    Blackman, C. J. et al. Toward an index of desiccation time to tree mortality under drought. Plant Cell Environ. 39, 2342–2345 (2016). A process-based approach is used to model desiccation time to mortality in trees under drought. PMID: 27093688 DOI
  59. The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought.
    Bartlett, M. K., Klein, T., Jansen, S., Choat, B. & Sack, L. The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proc. Natl Acad. Sci. USA 113, 13098–13103 (2016). PMID: 27807136 DOI
  60. Global convergence in the vulnerability of forests to drought.
    Choat, B. et al. Global convergence in the vulnerability of forests to drought. Nature 491, 752–755 (2012). Global synthesis demonstrating a convergence in tree hydraulic safety margins across forest biomes. PMID: 23172141 DOI
  61. Maherali, H., Pockman, W. T. & Jackson, R. B. Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85, 2184–2199 (2004). DOI
  62. Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer.
    Lens, F. et al. Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol. 190, 709–723 (2011). PMID: 21054413 DOI
  63. The relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit membrane form and function.
    Pittermann, J. et al. The relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit membrane form and function. Plant Physiol. 153, 1919–1931 (2010). PMID: 20551212 DOI
  64. Leaf hydraulic vulnerability influences species' bioclimatic limits in a diverse group of woody angiosperms.
    Blackman, C. J., Brodribb, T. J. & Jordan, G. J. Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms. Oecologia 168, 1–10 (2012). PMID: 21744163 DOI
  65. Coordination of physiological traits involved in drought-induced mortality of woody plants.
    Mencuccini, M., Minunno, F., Salmon, Y., Martínez-Vilalta, J. & Hölttä, T. Coordination of physiological traits involved in drought-induced mortality of woody plants. New Phytol. 208, 396–409 (2015). PMID: 25988920 DOI
  66. Reich, P. B. The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J. Ecol. 102, 275–301 (2014). DOI
  67. Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe.
    Anderegg, W. R. et al. Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc. Natl Acad. Sci. USA 113, 5024–5029 (2016). PMID: 27091965 DOI
  68. Death from drought in tropical forests is triggered by hydraulics not carbon starvation.
    Rowland, L. et al. Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature 528, 119–122 (2015). PMID: 26595275
  69. Limited genetic variability and phenotypic plasticity detected for cavitation resistance in a Mediterranean pine.
    Lamy, J.-B. et al. Limited genetic variability and phenotypic plasticity detected for cavitation resistance in a Mediterranean pine. New Phytol. 201, 874–886 (2014). PMID: 24180459 DOI
  70. How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction?
    Schuldt, B. et al. How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction? New Phytol. 210, 443–458 (2016). PMID: 26720626 DOI
  71. Climate influences the leaf area/sapwood area ratio in Scots pine.
    Mencuccini, M. & Grace, J. Climate influences the leaf area/sapwood area ratio in Scots pine. Tree Physiol. 15, 1–10 (1995). PMID: 14966005 DOI
  72. Magnani, F., Mencuccini, M. & Grace, J. Age-related decline in stand productivity: the role of structural acclimation under hydraulic constraints. Plant Cell Environ. 23, 251–263 (2000). DOI
  73. Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates.
    Maherali, H. & DeLucia, E. H. Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates. Tree Physiol. 20, 859–867 (2000). PMID: 11303576 DOI
  74. Hydraulic adjustment of Scots pine across Europe.
    Martínez-Vilalta, J. et al. Hydraulic adjustment of Scots pine across Europe. New Phytol. 184, 353–364 (2009). Comprehensive study of intra-specific variation in hydraulic traits across a broad climatic gradient. PMID: 19674333 DOI
  75. Genotypic variability and phenotypic plasticity of cavitation resistance in Fagus sylvatica L. across Europe.
    Wortemann, R. et al. Genotypic variability and phenotypic plasticity of cavitation resistance in Fagus sylvatica L. across Europe. Tree Physiol. 31, 1175–1182 (2011). PMID: 21989814 DOI
  76. Hogg, E. H., Brandt, J. P. & Kochtubajda, B. Growth and dieback of aspen forests in northwestern Alberta, Canada, in relation to climate and insects. Can. J. For. Res. 32, 823–832 (2002). DOI
  77. What plant hydraulics can tell us about responses to climate-change droughts.
    Sperry, J. S. & Love, D. M. What plant hydraulics can tell us about responses to climate-change droughts. New Phytol. 207, 14–27 (2015). PMID: 25773898 DOI
  78. Recent advances in tree hydraulics highlight the ecological significance of the hydraulic safety margin.
    Delzon, S. & Cochard, H. Recent advances in tree hydraulics highlight the ecological significance of the hydraulic safety margin. New Phytol. 203, 355–358 (2014). PMID: 24661229 DOI
  79. Anderegg, W. R. L. et al. Tree mortality predicted from drought-induced vascular damage. Nat. Geosci. 8, 367–371 (2015). DOI
  80. McDowell, N. G. et al. Multi-scale predictions of massive conifer mortality due to chronic temperature rise. Nat. Clim. Change 6, 295–300 (2016). DOI
  81. Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit.
    Brodribb, T. J., Bowman, D. J. M. S., Nichols, S., Delzon, S. & Burlett, R. Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit. New Phytol. 188, 533–542 (2010). PMID: 20673281 DOI
  82. Meinzer, F. C., Johnson, D. M., Lachenbruch, B., McCulloh, K. A. & Woodruff, D. R. Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct. Ecol. 23, 922–930 (2009). DOI
  83. Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework.
    McDowell, N. G. et al. Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework. New Phytol. 200, 304–321 (2013). PMID: 24004027 DOI
  84. Gustafson, E. J. & Sturtevant, B. R. Modeling forest mortality caused by drought stress: implications for climate change. Ecosystems 16, 60–74 (2013). DOI
  85. Mitchell, P. J. et al. An ecoclimatic framework for evaluating the resilience of vegetation to water deficit. Glob. Chang. Biol. 22, 1677–1689 (2016). DOI
  86. O’Sullivan, O. S. et al. Thermal limits of leaf metabolism across biomes. Glob. Chang. Biol. 23, 209–223 (2017). DOI
  87. Empirical and process-based approaches to climate-induced forest mortality models.
    Adams, H. D. et al. Empirical and process-based approaches to climate-induced forest mortality models. Front. Plant Sci. 4, 438 (2013). PMID: 24312103
  88. Christoffersen, B. O. et al. Linking hydraulic traits to tropical forest function in a size-structured and trait-driven model (TFS v.1-Hydro). Geosci. Model Dev. 9, 4227–4255 (2016). DOI
  89. Diversity in plant hydraulic traits explains seasonal and inter-annual variations of vegetation dynamics in seasonally dry tropical forests.
    Xu, X., Medvigy, D., Powers, J. S., Becknell, J. M. & Guan, K. Diversity in plant hydraulic traits explains seasonal and inter-annual variations of vegetation dynamics in seasonally dry tropical forests. New Phytol. 212, 80–95 (2016). PMID: 27189787 DOI
  90. Davi, H. & Cailleret, M. Assessing drought-driven mortality trees with physiological process-based models. Agric. For. Meteorol. 232, 279–290 (2017). DOI
  91. The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis.
    Bartlett, M. K., Scoffoni, C. & Sack, L. The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol. Lett. 15, 393–405 (2012). Data synthesis that links the point at which leaf turgor is lost to drought tolerance in plants. PMID: 22435987 DOI
  92. Change in hydraulic traits of Mediterranean Quercus ilex subjected to long-term throughfall exclusion.
    Limousin, J.-M., Longepierre, D., Huc, R. & Rambal, S. Change in hydraulic traits of Mediterranean Quercus ilex subjected to long-term throughfall exclusion. Tree Physiol. 30, 1026–1036 (2010). PMID: 20621974 DOI
  93. Cavitation, stomatal conductance, and leaf dieback in seedlings of two co-occurring Mediterranean shrubs during an intense drought.
    Vilagrosa, A., Bellot, J., Vallejo, V. R. & Gil-Pelegrín, E. Cavitation, stomatal conductance, and leaf dieback in seedlings of two co-occurring Mediterranean shrubs during an intense drought. J. Exp. Bot. 54, 2015–2024 (2003). PMID: 12885857 DOI
  94. Dahlin, K. M., Ponte, D. D., Setlock, E. & Nagelkirk, R. Global patterns of drought deciduous phenology in semi-arid and savanna-type ecosystems. Ecography 40, 314–323 (2016). DOI
  95. De Kauwe, M. G. et al. Do land surface models need to include differential plant species responses to drought? Examining model predictions across a mesic–xeric gradient in Europe. Biogeosciences 12, 7503–7518 (2015). DOI
  96. Aguadé, D., Poyatos, R., Rosas, T. & Martínez-Vilalta, J. Comparative drought responses of Quercus ilex L. and Pinus sylvestris L. in a montane forest undergoing a vegetation shift. Forests 6, 2505 (2015). DOI
  97. Predawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions.
    Donovan, L., Linton, M. & Richards, J. Predawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions. Oecologia 129, 328–335 (2001). PMID: 28547187 DOI
  98. Nobel, P. S. & Cui, M. Hydraulic conductances of the soil, the root–soil air gap, and the root: changes for desert succulents in drying soil. J. Exp. Bot. 43, 319–326 (1992). DOI
  99. Cloud forest trees with higher foliar water uptake capacity and anisohydric behavior are more vulnerable to drought and climate change.
    Eller, C. B., Lima, A. L. & Oliveira, R. S. Cloud forest trees with higher foliar water uptake capacity and anisohydric behavior are more vulnerable to drought and climate change. New Phytol. 211, 489–501 (2016). PMID: 27038126 DOI
  100. Sinclair, T. R. Model analysis of plant traits leading to prolonged crop survival during severe drought. Field Crops Res. 68, 211–217 (2000). DOI
  101. Manzoni, S., Katul, G. & Porporato, A. A dynamical system perspective on plant hydraulic failure. Wat. Resour. Res. 50, 5170–5183 (2014). DOI
  102. Gentine, P., Guérin, M., Uriarte, M., McDowell, N. G. & Pockman, W. T. An allometry-based model of the survival strategies of hydraulic failure and carbon starvation. Ecohydrology 9, 529–546 (2016). DOI
  103. Waring, R. H. Characteristics of trees predisposed to die. Bioscience 37, 569–574 (1987). DOI
  104. Bréda, N., Huc, R., Granier, A. & Dreyer, E. Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann. For. Sci. 63, 625–644 (2006). DOI
  105. De Micco, V., Balzano, A., Wheeler, E. A. & Baas, P. Tyloses and gums: a review of structure, function and occurrence of vessel occlusions. IAWA J. 37, 186–205 (2016). DOI
  106. Drought and resprouting plants.
    Zeppel, M. J. B. et al. Drought and resprouting plants. New Phytol. 206, 583–589 (2015). PMID: 27283977 DOI
  107. Ecology of sprouting in woody plants: the persistence niche.
    Bond, W. J. & Midgley, J. J. Ecology of sprouting in woody plants: the persistence niche. Trends Ecol. Evol. 16, 45–51 (2001). PMID: 11146144 DOI
  108. Maintenance of xylem Network Transport Capacity: A Review of Embolism Repair in Vascular Plants.
    Brodersen, C. R. & McElrone, A. J. Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Front. Plant Sci. 4, 108 (2013). PMID: 23630539 DOI
  109. Confronting Maxwell's demon: biophysics of xylem embolism repair.
    Zwieniecki, M. A. & Holbrook, N. M. Confronting Maxwell’s demon: biophysics of xylem embolism repair. Trends Plant Sci. 14, 530–534 (2009). PMID: 19726217 DOI
  110. Nardini, A., Savi, T., Trifilò, P. & Lo Gullo, M. A. in Progress in Botany Vol. 79(eds Cánovas, F. et al.) 197–231 (Springer, Cham, 2017).
  111. Dynamics of freeze-thaw embolism in Smilax rotundifolia (Smilacaceae).
    Cobb, A. R., Choat, B. & Holbrook, N. M. Dynamics of freeze–thaw embolism in Smilax rotundifolia (Smilacaceae). Am. J. Bot. 94, 640–649 (2007). PMID: 21636432 DOI
  112. Mechanisms of xylem recovery from winter embolism in Fagus sylvatica.
    Cochard, H., Lemoine, D., Améglio, T. & Granier, A. Mechanisms of xylem recovery from winter embolism in Fagus sylvatica. Tree Physiol. 21, 27–33 (2001). PMID: 11260821 DOI
  113. Spring filling of xylem vessels in wild grapevine.
    Sperry, J. S., Holbrook, N. M., Zimmermann, M. H. & Tyree, M. T. Spring filling of xylem vessels in wild grapevine. Plant Physiol. 83, 414–417 (1987). PMID: 16665259 DOI
  114. Functional repair of embolized vessels in maize roots after temporal drought stress, as demonstrated by magnetic resonance imaging.
    Kaufmann, I. et al. Functional repair of embolized vessels in maize roots after temporal drought stress, as demonstrated by magnetic resonance imaging. New Phytol. 184, 245–256 (2009). PMID: 19563443 DOI
  115. McCully, M. E., Huang, C. X. & Ling, L. E. C. Daily embolism and refilling of xylem vessels in the roots of field-grown maize. New Phytol. 138, 327–342 (1998). DOI
  116. A case-study of water transport in co-occurring ring- versus diffuse-porous trees: contrasts in water-status, conducting capacity, cavitation and vessel refilling.
    Taneda, H. & Sperry, J. S. A case-study of water transport in co-occurring ring- versus diffuse-porous trees: contrasts in water-status, conducting capacity, cavitation and vessel refilling. Tree Physiol. 28, 1641–1651 (2008). PMID: 18765369 DOI
  117. Zwieniecki, M. A. & Holbrook, N. M. Diurnal variation in xylem hydraulic conductivity in white ash (Fraxinus americana L.), red maple (Acer rubrum L.) and red spruce (Picea rubens Sarg.). Plant Cell Environ. 21, 1173–1180 (1998). DOI
  118. The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography.
    Brodersen, C. R., McElrone, A. J., Choat, B., Matthews, M. A. & Shackel, K. A. The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. Plant Physiol. 154, 1088–1095 (2010). First study to utilize synchrotron-based imaging methods for non-destructive visualization of xylem function. PMID: 20841451 DOI
  119. Evidence for Hydraulic Vulnerability Segmentation and Lack of Xylem Refilling under Tension.
    Charrier, G. et al. Evidence for hydraulic vulnerability segmentation and lack of xylem refilling under tension. Plant Physiol. 172, 1657–1668 (2016). PMID: 27613852 DOI
  120. Clearwater, M. J. & Clark, C. J. In vivo magnetic resonance imaging of xylem vessel contents in woody lianas. Plant Cell Environ. 26, 1205–1214 (2003). DOI
  121. Patterns of drought-induced embolism formation and spread in living walnut saplings visualized using X-ray microtomography.
    Knipfer, T., Brodersen, C. R., Zedan, A., Kluepfel, D. A. & McElrone, A. J. Patterns of drought-induced embolism formation and spread in living walnut saplings visualized using X-ray microtomography. Tree Physiol. 35, 744–755 (2015). PMID: 26063708 DOI
  122. Gas exchange recovery following natural drought is rapid unless limited by loss of leaf hydraulic conductance: evidence from an evergreen woodland.
    Skelton, R. P., Brodribb, T. J., McAdam, S. A. M. & Mitchell, P. J. Gas exchange recovery following natural drought is rapid unless limited by loss of leaf hydraulic conductance: evidence from an evergreen woodland. New Phytol. 215, 1399–1412 (2017). PMID: 28620915 DOI
  123. XYLOGENESIS: INITIATION, PROGRESSION, AND CELL DEATH.
    Fukuda, H. Xylogenesis: initiation, progression, and cell death. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 299–325 (1996). PMID: 15012291 DOI
  124. Davies, W., Metcalfe, J., Lodge, T. & da Costa, A. R. Plant growth substances and the regulation of growth under drought. Funct. Plant Biol. 13, 105–125 (1986).
  125. Liang, E., Balducci, L., Ren, P. & Rossi, S. in Secondary Xylem Biology: Origins, Functions, and Applications (eds Kim, Y.S. et al.) 45–58 (Academic, Cambridge, 2016).
  126. Hartmann, H. Will a 385 million year-struggle for light become a struggle for water and for carbon? – How trees may cope with more frequent climate change-type drought events. Glob. Chang. Biol. 17, 642–655 (2011). DOI
  127. How tree roots respond to drought.
    Brunner, I., Herzog, C., Dawes, M. A., Arend, M. & Sperisen, C. How tree roots respond to drought. Front. Plant Sci. 6, 547 (2015). PMID: 26284083 DOI
  128. Kozlowski, T. & Pallardy, S. Acclimation and adaptive responses of woody plants to environmental stresses. Bot. Rev. 68, 270–334 (2002). DOI
  129. A microtensiometer capable of measuring water potentials below -10 MPa.
    Pagay, V. et al. A microtensiometer capable of measuring water potentials below −10 MPa. Lab Chip 14, 2806–2817 (2014). PMID: 24901287 DOI
  130. Luo, Z. et al. Responses of plant water use to a severe summer drought for two subtropical tree species in the central southern China. J. Hydrol. 8, 1–9 (2016).
  131. Methods for measuring plant vulnerability to cavitation: a critical review.
    Cochard, H. et al. Methods for measuring plant vulnerability to cavitation: a critical review. J. Exp. Bot. 64, 4779–4791 (2013). PMID: 23888067 DOI
  132. SAPFLUXNET: towards a global database of sap flow measurements.
    Poyatos, R. et al. SAPFLUXNET: towards a global database of sap flow measurements. Tree Physiol. 36, 1449–1455 (2016). PMID: 27885171 DOI
  133. Global satellite monitoring of climate-induced vegetation disturbances.
    McDowell, N. G. et al. Global satellite monitoring of climate-induced vegetation disturbances. Trends Plant Sci. 20, 114–123 (2015). PMID: 25500552 DOI
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
DOI
10.1038/s41586-018-0240-x
Email
b.choat@westernsydney.edu.au
Published
2018-00-00
Epub
2018-00-27
Pages
531-539
Language
English
Region
England
NLM ID
0410462
Subset
IM
External Links
PubMed source DOI: 10.1038/s41586-018-0240-x View journal details
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