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  • Review Article
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Mechanisms of woody-plant mortality under rising drought, CO2 and vapour pressure deficit

Nature Reviews Earth & Environment volume 3, pages 294–308 (2022)Cite this article

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Abstract

Drought-associated woody-plant mortality has been increasing in most regions with multi-decadal records and is projected to increase in the future, impacting terrestrial climate forcing, biodiversity and resource availability. The mechanisms underlying such mortality, however, are debated, owing to complex interactions between the drivers and the processes. In this Review, we synthesize knowledge of drought-related tree mortality under a warming and drying atmosphere with rising atmospheric CO2. Drought-associated mortality results from water and carbon depletion and declines in their fluxes relative to demand by living tissues. These pools and fluxes are interdependent and underlay plant defences against biotic agents. Death via failure to maintain a positive water balance is particularly dependent on soil-to-root conductance, capacitance, vulnerability to hydraulic failure, cuticular water losses and dehydration tolerance, all of which could be exacerbated by reduced carbon supply rates to support cellular survival or the carbon starvation process. The depletion of plant water and carbon pools is accelerated under rising vapour pressure deficit, but increasing CO2 can mitigate these impacts. Advancing knowledge and reducing predictive uncertainties requires the integration of carbon, water and defensive processes, and the use of a range of experimental and modelling approaches.

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Fig. 1: Changing tree mortality and climate variables.
Fig. 2: The interconnected mortality process.
Fig. 3: Mechanisms that lead towards mortality.
Fig. 4: The linkage between woody plant’s defence systems and biotic attack.
Fig. 5: Simulated whole-plant hydraulic failure during drought-associated mortality.
Fig. 6: Trait acclimation can reduce mortality likelihood.

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Data availability

All data from the simulations can be obtained from the lead author.

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Acknowledgements

The authors thank C. Körner for thoughtful advice, D. Basler for providing the CH2018 data on future climate projections for Switzerland and B. Roskilly, the Montgomery Laboratory and A. Castillo for feedback on figures. N.G.M. and C.X. were supported by the Department of Energy, Office of Science project Next Generation Ecosystem Experiment–Tropics (NGEE-Tropics). G.S. was supported by the NSFBII-Implementation (2021898). D.T.T. acknowledges support from the Australian Research Council (ARC) (DP0879531, DP110105102, LP0989881, LP140100232). M.G.D.K. acknowledges support from the ARC Centre of Excellence for Climate Extremes (CE170100023), the ARC Discovery Grant (DP190101823) and the NSW Research Attraction and Acceleration Program. C.G. was supported by the Swiss National Science Foundation (PZ00P3_174068). M.Mencuccini and J.M.-V. were supported by the Spanish Ministry of Science and Innovation (MICINN, CGL2017-89149-C2-1-R). A.T.T. acknowledges funding from NSF grant 2003205, the USDA National Institute of Food and Agriculture, Agriculture and Food Research Initiative Competitive Grants Program no. 2018-67012-31496 and the University of California Laboratory Fees Research Program award no. LFR-20-652467. W.M.H. was supported by the NSF GRFP (1-746055). A.M.T. and H.D.A. were supported by the NSF Division of Integrative Organismal Systems, Integrative Ecological Physiology Program (IOS-1755345, IOS-1755346). H.D.A. also received support from the USDA National Institute of Food and Agriculture (NIFA), McIntire-Stennis Project WNP00009 and Agriculture and Food Research Initiative award 2021-67013-33716. D.D.B. was supported by NSF (DEB-1550756, DEB-1824796, DEB-1925837), USGS SW Climate Adaptation Science Center (G18AC00320), USDA NIFA McIntire-Stennis ARZT 1390130-M12-222 and a Murdoch University Distinguished Visiting Scholar award. D.S.M. was supported by NSF (IOS-1444571, IOS-1547796). R.S.O. acknowledges funding from NERC-FAPESP 19/07773-1. W.R.L.A. was supported by the David and Lucille Packard Foundation, NSF grants 1714972, 1802880 and 2003017, and USDA NIFA AFRI grant no. 2018-67019-27850. R.S.O. acknowledges funding from NERC-FAPESP 19/07773-1. B.E.M. is supported by an Australian Research Council Laureate Fellowship (FL190100003). A.S. was supported by a Bullard Fellowship (Harvard University) and the University of Montana.

Author information

Authors and Affiliations

  1. Atmospheric Sciences and Global Change Division, Pacific Northwest National Laboratory, Richland, WA, USA

    Nate G. McDowell & Alexandria Pivovaroff

  2. School of Biological Sciences, Washington State University, Pullman, WA, USA

    Nate G. McDowell

  3. Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN, USA

    Gerard Sapes

  4. School of the Environment, Washington State University, Pullman, WA, USA

    Henry D. Adams

  5. Department of Geography and Environmental Studies, University of New Mexico, Albuquerque, NM, USA

    Craig D. Allen

  6. School of Biological Sciences, University of Utah, Salt Lake City, UT, USA

    William R. L. Anderegg

  7. Department of Environmental Sciences — Botany, University of Basel, Basel, Switzerland

    Matthias Arend, Günter Hoch & Ansgar Kahmen

  8. School of Natural Resources and the Environment, University of Arizona, Tucson, AZ, USA

    David D. Breshears

  9. School of Natural Sciences, University of Tasmania, Hobart, Tasmania, Australia

    Tim Brodribb

  10. Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales, Australia

    Brendan Choat, Belinda E. Medlyn & David T. Tissue

  11. Université Clermont-Auvergne, INRAE, PIAF, Clermont-Ferrand, France

    Hervé Cochard, Marylou Mantova & José M. Torres-Ruiz

  12. Centre for Research on Ecology and Forestry Applications (CREAF), Bellaterra, Spain

    Miquel De Cáceres, Jordi Martínez-Vilalta & Maurizio Mencuccini

  13. School of Biological Sciences, University of Bristol, Bristol, UK

    Martin G. De Kauwe

  14. ARC Centre of Excellence for Climate Extremes, Sydney, New South Wales, Australia

    Martin G. De Kauwe

  15. Climate Change Research Centre, University of New South Wales, Sydney, New South Wales, Australia

    Martin G. De Kauwe

  16. Plant Ecology Research Laboratory (PERL), École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland

    Charlotte Grossiord

  17. Community Ecology Unit, Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Lausanne, Switzerland

    Charlotte Grossiord

  18. Agronomy Department, University of Florida, Gainesville, FL, USA

    William M. Hammond

  19. Department of Biogeochemical Processes, Max Planck Institute for Biogeochemistry, Jena, Germany

    Henrik Hartmann

  20. Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel

    Tamir Klein

  21. Department of Geography, University at Buffalo, Buffalo, NY, USA

    D. Scott Mackay

  22. Department of Environment and Sustainability, University at Buffalo, Buffalo, NY, USA

    D. Scott Mackay

  23. Universitat Autònoma de Barcelona, Bellaterra, Spain

    Jordi Martínez-Vilalta

  24. Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain

    Maurizio Mencuccini

  25. Department of Life Sciences, University of Trieste, Trieste, Italy

    Andrea Nardini

  26. Department of Plant Biology, University of Campinas — UNICAMP, Campinas, Brazil

    Rafael S. Oliveira

  27. Division of Biological Sciences, University of Montana, Missoula, MT, USA

    Anna Sala

  28. Department of Entomology, University of Wisconsin-Madison, Madison, WI, USA

    Amy M. Trowbridge

  29. Department of Geography, University of California, Santa Barbara, Santa Barbara, CA, USA

    Anna T. Trugman

  30. Department of Biology, University of Central Arkansas, Conway, AR, USA

    Erin Wiley

  31. Earth and Environmental Sciences Division, Los Alamos National Laboratory, Los Alamos, NM, USA

    Chonggang Xu

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  1. Nate G. McDowell
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  2. Gerard Sapes
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Contributions

N.G.M. led the effort to generate this manuscript. G.S. generated the figures. A.P., H.C., M.D.C., M.G.D.K. and D.S.M. conducted the modelling simulations. The authors contributed equally to the generation of ideas and writing of the article.

Corresponding author

Correspondence to Nate G. McDowell.

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The authors declare no competing interests.

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Nature Reviews Earth and Environment thanks Amanda Cardoso, Teresa Gimeno and Atsushi Ishida, who co-reviewed with Shin-Taro Saiki, for their contribution to the peer review of this work.

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Supplementary information

Glossary

Mortality

The irreversible cessation of metabolism and the associated inability to regenerate.

Die-off

Widespread and rapid mortality of a species or community.

Background mortality

Mortality rates in the absence of disturbances.

Droughts

Periods of anomalously low precipitation.

Hydraulic failure

The accumulation of emboli within the sapwood past a threshold after which water transport is irrecoverable.

Threshold

The magnitude or intensity that must be exceeded to cause a reaction or change.

Carbon starvation

The process whereby a limited carbohydrate supply rate impairs maintenance of carbon-dependent metabolic, defence or hydraulic functions.

Process

A series of mechanisms that leads to an end point.

Mechanisms

Systems of parts working together within a process; pieces of the machinery.

Dying

Committed to death; beyond the point of no return; to have passed a threshold beyond which mortality is certain.

Biotic agents

Living organisms — especially fungi, bacteria and insects — that interdependently impact the water and carbon economies of plants.

Meristematic cells

Undifferentiated cells capable of division and formation into new tissues.

Cytorrhysis

Irreparable damage to cell walls after cellular collapse from the loss of internal positive pressure.

Dieback

The partial loss of canopy or root biomass, without whole-plant mortality.

Failure of water relations

Impairment of the interacting water and carbon processes that forces declines in water supply and subsequent dehydration.

Acclimation

Structural or physiological shifts in response to external drivers.

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McDowell, N.G., Sapes, G., Pivovaroff, A. et al. Mechanisms of woody-plant mortality under rising drought, CO2 and vapour pressure deficit. Nat Rev Earth Environ 3, 294–308 (2022). https://doi.org/10.1038/s43017-022-00272-1

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