Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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.

Data availability

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

References

  1. van Mantgem, P. J. et al. Widespread increase of tree mortality rates in the western United States. Science 323, 521–524 (2009).

    Article  Google Scholar 

  2. Peng, C. et al. A drought-induced pervasive increase in tree mortality across Canada’s boreal forests. Nat. Clim. Chang. 1, 467–471 (2011).

    Article  Google Scholar 

  3. Brienen, R. J. et al. Long-term decline of the Amazon carbon sink. Nature 519, 344–348 (2015).

    Article  Google Scholar 

  4. Klein, T., Cahanovitc, R., Sprintsin, M., Herr, N. & Schiller, G. A nation-wide analysis of tree mortality under climate change: forest loss and its causes in Israel 1948–2017. For. Ecol. Manag. 432, 840–849 (2019).

    Article  Google Scholar 

  5. Yu, K. et al. Pervasive decreases in living vegetation carbon turnover time across forest climate zones. Proc. Natl Acad. Sci. USA 116, 24662–24667 (2019).

    Article  Google Scholar 

  6. Hubau, W. et al. Asynchronous carbon sink saturation in African and Amazonian tropical forests. Nature 579, 80–87 (2020).

    Article  Google Scholar 

  7. Kharuk, V. I. et al. Climate-driven conifer mortality in Siberia. Glob. Ecol. Biogeogr. 30, 543–556 (2021).

    Article  Google Scholar 

  8. Breshears, D. D. et al. Regional vegetation die-off in response to global-change-type drought. Proc. Natl Acad. Sci. USA 102, 15144–15148 (2005).

    Article  Google Scholar 

  9. Lewis, S. L., Brando, P. M., Phillips, O. L., van der Heijden, G. M. & Nepstad, D. The 2010 amazon drought. Science 331, 554 (2011).

    Article  Google Scholar 

  10. Ruthrof, K. X. et al. Subcontinental heat wave triggers terrestrial and marine, multi-taxa responses. Sci. Rep. 8, 13094 (2018).

    Article  Google Scholar 

  11. Senf, C. et al. Canopy mortality has doubled in Europe’s temperate forests over the last three decades. Nat. Commun. 9, 4978 (2018).

    Article  Google Scholar 

  12. Schuldt, B. et al. A first assessment of the impact of the extreme 2018 summer drought on Central European forests. Basic Appl. Ecol. 45, 86–103 (2020).

    Article  Google Scholar 

  13. Kannenberg, S. A., Driscoll, A. W., Malesky, D. & Anderegg, W. R. Rapid and surprising dieback of Utah juniper in the southwestern USA due to acute drought stress. For. Ecol. Manag. 480, 118639 (2021).

    Article  Google Scholar 

  14. 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, 1–55 (2015).

    Article  Google Scholar 

  15. Powers, J. S. et al. A catastrophic tropical drought kills hydraulically vulnerable tree species. Glob. Change Biol. 26, 3122–3133 (2020).

    Article  Google Scholar 

  16. Werner, W. L. Canopy dieback in the upper montane rain forests of Sri Lanka. GeoJournal 17, 245–248 (1988).

    Article  Google Scholar 

  17. Feldpausch, T. R. et al. Amazon forest response to repeated droughts. Glob. Biogeochem. Cycles 30, 964–982 (2016).

    Article  Google Scholar 

  18. Esquivel-Muelbert, A. et al. Tree mode of death and mortality risk factors across Amazon forests. Nat. Commun. 11, 5515 (2020).

    Article  Google Scholar 

  19. Werner, R. A. & Holsten, E. H. Mortality of white spruce during a spruce beetle outbreak on the Kenai Peninsula in Alaska. Can. J. For. Res. 13, 96–101 (1983).

    Article  Google Scholar 

  20. Suarez, M. L., Ghermandi, L. & Kitzberger, T. Factors predisposing episodic drought-induced tree mortality in Nothofagus: site, climatic sensitivity and growth trends. J. Ecol. 92, 954–966 (2004).

    Article  Google Scholar 

  21. Swemmer, A. M. Locally high, but regionally low: the impact of the 2014–2016 drought on the trees of semi-arid savannas, South Africa. Afr. J. Range Forage Sci. 37, 31–42 (2020).

    Article  Google Scholar 

  22. Michaelian, M., Hogg, E. H., Hall, R. J. & Arsenault, E. Massive mortality of aspen following severe drought along the southern edge of the Canadian boreal forest. Glob. Chang Biol. 17, 2084–2094 (2011).

    Article  Google Scholar 

  23. Kharuk, V. I. et al. Climate-induced mortality of Siberian pine and fir in the Lake Baikal Watershed, Siberia. For. Ecol. Manag. 384, 191–199 (2017).

    Article  Google Scholar 

  24. Kharuk, V. I., Ranson, K. J., Oskorbin, P. A., Im, S. T. & Dvinskaya, M. L. Climate induced birch mortality in Trans-Baikal lake region, Siberia. For. Ecol. Manag. 289, 385–392 (2013).

    Article  Google Scholar 

  25. Crouchet, S. E., Jensen, J., Schwartz, B. F. & Schwinning, S. Tree mortality after a hot drought: distinguishing density-dependent and -independent drivers and why it matters. Front. For. Glob. Change 2, 21 (2019).

    Article  Google Scholar 

  26. Breshears, D. D. et al. The critical amplifying role of increasing atmospheric moisture demand on tree mortality and associated regional die-off. Front. Plant Sci. 4, 266 (2013).

    Article  Google Scholar 

  27. Grossiord, C. et al. Plant responses to rising vapor pressure deficit. New Phytol. 226, 1550–1566 (2020).

    Article  Google Scholar 

  28. Trenberth, K. E. et al. Global warming and changes in drought. Nat. Clim. Chang. 4, 17–22 (2014).

    Article  Google Scholar 

  29. Williams, A. P. et al. Temperature as a potent driver of regional forest drought stress and tree mortality. Nat. Clim. Chang. 3, 292–297 (2013).

    Article  Google Scholar 

  30. Xu, C. et al. Increasing impacts of extreme droughts on vegetation productivity under climate change. Nat. Clim. Chang. 9, 948–953 (2019).

    Article  Google Scholar 

  31. Dore, M. H. Climate change and changes in global precipitation patterns: what do we know? Environ. Int. 31, 1167–1181 (2005).

    Article  Google Scholar 

  32. Ukkola, A. M., De Kauwe, M. G., Roderick, M. L., Abramowitz, G. & Pitman, A. J. Robust future changes in meteorological drought in CMIP6 projections despite uncertainty in precipitation. Geophys. Res. Lett. 31, e2020GL087820 (2020).

    Google Scholar 

  33. Breshears, D. D. et al. Underappreciated plant vulnerabilities to heat waves. New Phytol. 231, 32–39 (2021).

    Article  Google Scholar 

  34. Adams, H. D. et al. Temperature response surfaces for mortality risk of tree species with future drought. Environ. Res. Lett. 12, 115014 (2017).

    Article  Google Scholar 

  35. McDowell, N. G. et al. Multi-scale predictions of massive conifer mortality due to chronic temperature rise. Nat. Clim. Chang. 6, 295–300 (2016).

    Article  Google Scholar 

  36. Keenan, T. F. et al. Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499, 324–327 (2013).

    Article  Google Scholar 

  37. Walker, A. P. et al. Integrating the evidence for a terrestrial carbon sink caused by increasing atmospheric CO2. New Phytol. 229, 2413–2445 (2020).

    Article  Google Scholar 

  38. Long, S. P. Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: has its importance been underestimated? Plant Cell Environ. 14, 729–739 (1991).

    Article  Google Scholar 

  39. Hickler, T. et al. CO2 fertilization in temperate FACE experiments not representative of boreal and tropical forests. Glob. Change Biol. 14, 1531–1542 (2008).

    Article  Google Scholar 

  40. Baig, S., Medlyn, B. E., Mercado, L. & Zaehle, S. Does the growth response of woody plants to elevated CO2 increase with temperature? A model-oriented meta-analysis. Glob. Change Biol. 21, 4303–4319 (2015).

    Article  Google Scholar 

  41. Peñuelas, J. et al. Shifting from a fertilization-dominated to a warming-dominated period. Nat. Ecol. Evol. 1, 1438–1445 (2017).

    Article  Google Scholar 

  42. Belmecheri, S. et al. Precipitation alters the CO2 effect on water-use efficiency of temperate forests. Glob. Change Biol. 27, 1560–1571 (2021).

    Article  Google Scholar 

  43. Duffy, K. A. et al. How close are we to the temperature tipping point of the terrestrial biosphere? Sci. Adv. 7, eaay1052 (2021).

    Article  Google Scholar 

  44. De Kauwe, M. G., Medlyn, B. E. & Tissue, D. T. To what extent can rising [CO2] ameliorate plant drought stress? New Phytol. 231, 2118–2124 (2021).

    Article  Google Scholar 

  45. Martınez-Vilalta, J., Piñol, J. & Beven, K. A hydraulic model to predict drought-induced mortality in woody plants: an application to climate change in the Mediterranean. Ecol. Model. 155, 127–147 (2002).

    Article  Google Scholar 

  46. 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).

    Article  Google Scholar 

  47. McDowell, N. G. et al. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol. Evol. 26, 523–532 (2011).

    Article  Google Scholar 

  48. Adams, H. D. et al. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat. Ecol. Evol. 1, 1285–1291 (2017).

    Article  Google Scholar 

  49. Fisher, R. et al. Assessing uncertainties in a second-generation dynamic vegetation model caused by ecological scale limitations. New Phytol. 187, 666–681 (2010).

    Article  Google Scholar 

  50. McDowell, N. G. et al. Evaluating theories of drought-induced vegetation mortality using a multimodel–experiment framework. New Phytol. 200, 304–321 (2013).

    Article  Google Scholar 

  51. Anderegg, W. R. L. et al. Hydraulic diversity of forests regulates ecosystem resilience during drought. Nature 561, 538–541 (2018).

    Article  Google Scholar 

  52. 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).

    Article  Google Scholar 

  53. Kennedy, D. et al. Implementing plant hydraulics in the community land model, version 5. J. Adv. Model. Earth Syst. 11, 485–513 (2019).

    Article  Google Scholar 

  54. Koven, C. D. et al. Benchmarking and parameter sensitivity of physiological and vegetation dynamics using the Functionally Assembled Terrestrial Ecosystem Simulator (FATES) at Barro Colorado Island, Panama. Biogeosciences 17, 3017–3044 (2020).

    Article  Google Scholar 

  55. Anderegg, W. R., Kane, J. M. & Anderegg, L. D. Consequences of widespread tree mortality triggered by drought and temperature stress. Nat. Clim. Chang. 3, 30–36 (2013).

    Article  Google Scholar 

  56. Hartmann, H. et al. Research frontiers for improving our understanding of drought-induced tree and forest mortality. New Phytol. 218, 15–28 (2018).

    Article  Google Scholar 

  57. Adams, H. D. et al. Ecohydrological consequences of drought- and infestation-triggered tree die-off: insights and hypotheses. Ecohydrology 5, 145–159 (2012).

    Article  Google Scholar 

  58. Bearup, L. A., Maxwell, R. M., Clow, D. W. & McCray, J. E. Hydrological effects of forest transpiration loss in bark beetle-impacted watersheds. Nat. Clim. Chang. 4, 481–486 (2014).

    Article  Google Scholar 

  59. Bennett, K. E. et al. Climate-driven disturbances in the San Juan River sub-basin of the Colorado River. Hydrol. Earth Syst. Sci. 22, 709–725 (2018).

    Article  Google Scholar 

  60. Lutz, J. A. & Halpern, C. B. Tree mortality during early forest development: a long-term study of rates, causes, and consequences. Ecol. Monogr. 76, 257–275 (2006).

    Article  Google Scholar 

  61. Clark, J. S. et al. The impacts of increasing drought on forest dynamics, structure, and biodiversity in the United States. Glob. Change Biol. 22, 2329–2352 (2016).

    Article  Google Scholar 

  62. McDowell, N. G. et al. Pervasive shifts in forest dynamics in a changing world. Science 368, eaaz9463 (2020).

    Article  Google Scholar 

  63. Waring, K. M. et al. Modeling the impacts of two bark beetle species under a warming climate in the southwestern USA: ecological and economic consequences. Environ. Manag. 44, 824–835 (2009).

    Article  Google Scholar 

  64. Barigah, T. S. et al. Water stress-induced xylem hydraulic failure is a causal factor of tree mortality in beech and poplar. Ann. Bot. 112, 1431–1437 (2013).

    Article  Google Scholar 

  65. Guadagno, C. R. et al. Dead or alive? Using membrane failure and chlorophyll a fluorescence to predict plant mortality from drought. Plant Physiol. 175, 223–234 (2017).

    Article  Google Scholar 

  66. Hammond, W. M. et al. Dead or dying? Quantifying the point of no return from hydraulic failure in drought-induced tree mortality. New Phytol. 223, 1834–1843 (2019).

    Article  Google Scholar 

  67. Sapes, G. et al. Plant water content integrates hydraulics and carbon depletion to predict drought-induced seedling mortality. Tree Physiol. 39, 1300–1312 (2019).

    Article  Google Scholar 

  68. Mantova, M., Menezes-Silva, P. E., Badel, E., Cochard, H. & Torres-Ruiz, J. M. The interplay of hydraulic failure and cell vitality explains tree capacity to recover from drought. Physiol. Plant. 172, 247–257 (2021).

    Article  Google Scholar 

  69. Kono, Y. et al. Initial hydraulic failure followed by late-stage carbon starvation leads to drought-induced death in the tree Trema orientalis. Commun. Biol. 2, 8 (2019).

    Article  Google Scholar 

  70. Preisler, Y. et al. Seeking the “point of no return” in the sequence of events leading to mortality of mature trees. Plant Cell Environ. 44, 1315–1328 (2020).

    Article  Google Scholar 

  71. Allen, C. D. et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For. Ecol. Manag. 259, 660–684 (2010).

    Article  Google Scholar 

  72. Bennett, A. C. et al. Resistance of African tropical forests to an extreme climate anomaly. Proc. Natl Acad. Sci. USA 118, e2003169118 (2021).

    Article  Google Scholar 

  73. McDowell, N. G. & Allen, C. D. Darcy’s law predicts widespread forest mortality under climate warming. Nat. Clim. Chang. 5, 669–672 (2015).

    Article  Google Scholar 

  74. Stephenson, N. L. & van Mantgem, P. J. Forest turnover rates follow global and regional patterns of productivity. Ecol. Lett. 8, 524–531 (2005).

    Article  Google Scholar 

  75. Zhu, K. C. et al. Dual impacts of climate change: forest migration and turnover through life history. Glob. Change Biol. 20, 251–264 (2014).

    Article  Google Scholar 

  76. Jump, A. S. et al. Structural overshoot of tree growth with climate variability and the global spectrum of drought-induced forest dieback. Glob. Change Biol. 23, 3742–3757 (2017).

    Article  Google Scholar 

  77. Trugman, A. T. et al. Tree carbon allocation explains forest drought-kill and recovery patterns. Ecol. Lett. 21, 1552–1560 (2018).

    Article  Google Scholar 

  78. Hartmann, H. et al. Climate change risks to global forest health – emergence of unexpected events of elevated tree mortality world-wide. Annu. Rev. Plant Biol. https://doi.org/10.1146/annurev-arplant-102820-012804 (2022).

    Article  Google Scholar 

  79. Manion, P. D. Tree Disease Concepts (Prentice-Hall, 1981)

  80. Brodribb, T. J. Learning from a century of droughts. Nat. Ecol. Evol. 4, 1007–1008 (2020).

    Article  Google Scholar 

  81. Anderegg, W. R. et al. Tree mortality from drought, insects, and their interactions in a changing climate. New Phytol. 208, 674–683 (2015).

    Article  Google Scholar 

  82. Huang, J. et al. Tree defence and bark beetles in a drying world: carbon partitioning, functioning and modelling. New Phytol. 225, 26–36 (2019).

    Article  Google Scholar 

  83. Martinez-Vilalta, J., Anderegg, W. R., Sapes, G. & Sala, A. Greater focus on water pools may improve our ability to understand and anticipate drought-induced mortality in plants. New Phytol. 223, 22–32 (2019).

    Article  Google Scholar 

  84. 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).

    Article  Google Scholar 

  85. Johnson, D. M. et al. Co-occurring woody species have diverse hydraulic strategies and mortality rates during an extreme drought. Plant Cell Environ. 41, 576–588 (2018).

    Article  Google Scholar 

  86. Cochard, H. A new mechanism for tree mortality due to drought and heatwaves. Peer Community J. 1, e36 (2021).

    Article  Google Scholar 

  87. Duursma, R. A. et al. On the minimum leaf conductance: its role in models of plant water use, and ecological and environmental controls. New Phytol. 221, 693–705 (2019).

    Article  Google Scholar 

  88. Beckett, R. P. Pressure–volume analysis of a range of poikilohydric plants implies the existence of negative turgor in vegetative cells. Ann. Bot. 79, 145–152 (1997).

    Article  Google Scholar 

  89. Ding, Y., Zhang, Y., Zheng, Q. S. & Tyree, M. T. Pressure–volume curves: revisiting the impact of negative turgor during cell collapse by literature review and simulations of cell micromechanics. New Phytol. 203, 378–387 (2014).

    Article  Google Scholar 

  90. Sperry, J. S., Adler, F. R., Campbell, G. S. & Comstock, J. P. Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell Environ. 21, 347–359 (1998).

    Article  Google Scholar 

  91. Rodriguez-Dominguez, C. M. & Brodribb, T. J. Declining root water transport drives stomatal closure in olive under moderate water stress. New Phytol. 225, 126–134 (2020).

    Article  Google Scholar 

  92. Carminati, A. & Javaux, M. Soil rather than xylem vulnerability controls stomatal response to drought. Trends Plant Sci. 25, 868–880 (2020).

    Article  Google Scholar 

  93. Maseda, P. H. & Fernandez, R. J. Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J. Exp. Bot. 57, 3963–3977 (2006).

    Article  Google Scholar 

  94. Plaut, J. A. et al. Hydraulic limits preceding mortality in a piñon–juniper woodland under experimental drought. Plant Cell Environ. 35, 1601–1617 (2012).

    Article  Google Scholar 

  95. Creek, D. et al. Xylem embolism in leaves does not occur with open stomata: evidence from direct observations using the optical visualization technique. J. Exp. Bot. 71, 1151–1159 (2020).

    Article  Google Scholar 

  96. Choat, B. et al. Triggers of tree mortality under drought. Nature 558, 531–539 (2018).

    Article  Google Scholar 

  97. Hammond, W. M. & Adams, H. D. Dying on time: traits influencing the dynamics of tree mortality risk from drought. Tree Physiol. 39, 906–909 (2019).

    Article  Google Scholar 

  98. Körner, C. No need for pipes when the well is dry — a comment on hydraulic failure in trees. Tree Physiol. 39, 695–700 (2019).

    Article  Google Scholar 

  99. Machado, R. et al. Where do leaf water leaks come from? Trade-offs underlying the variability in minimum conductance across tropical savanna species with contrasting growth strategies. New Phytol. 229, 1415–1430 (2021).

    Article  Google Scholar 

  100. Burghardt, M. & Riederer, M. in Biology of the Plant Cuticle (eds Riederer, M. & Müller, C.) 292–311 (Blackwell, 2006).

  101. Billon, L. M. et al. The DroughtBox: a new tool for phenotyping residual branch conductance and its temperature dependence during drought. Plant Cell Environ. 43, 1584–1594 (2020).

    Article  Google Scholar 

  102. Wolfe, B. T. Bark water vapour conductance is associated with drought performance in tropical trees. Biol. Lett. 16, 20200263 (2020).

    Article  Google Scholar 

  103. Martín-Gómez, P., Serrano, L. & Ferrio, J. P. Short-term dynamics of evaporative enrichment of xylem water in woody stems: implications for ecohydrology. Tree Physiol. 37, 511–522 (2017).

    Google Scholar 

  104. Arend, M. et al. Rapid hydraulic collapse as cause of drought-induced mortality in conifers. Proc. Natl Acad. Sci. USA 118, e2025251118 (2021).

    Article  Google Scholar 

  105. Wang, W. et al. Mortality predispositions of conifers across western USA. New Phytol. 229, 831–844 (2020).

    Article  Google Scholar 

  106. Christiansen, E., Waring, R. H. & Berryman, A. A. Resistance of conifers to bark beetle attack: searching for general relationships. For. Ecol. Manag. 22, 89–106 (1987).

    Article  Google Scholar 

  107. Bigler, C., Bräker, O. U., Bugmann, H., Dobbertin, M. & Rigling, A. Drought as an inciting mortality factor in Scots pine stands of the Valais, Switzerland. Ecosystems 9, 330–343 (2006).

    Article  Google Scholar 

  108. Richardson, A. D. et al. Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytol. 197, 850–861 (2013).

    Article  Google Scholar 

  109. Meinzer, F. C. et al. Dynamics of water transport and storage in conifers studied with deuterium and heat tracing techniques. Plant Cell Environ. 29, 105–114 (2006).

    Article  Google Scholar 

  110. McDowell, N. G., Allen, C. D. & Marshall, L. Growth, carbon-isotope discrimination, and drought-associated mortality across a Pinus ponderosa elevational transect. Glob. Change Biol. 16, 399–415 (2010).

    Article  Google Scholar 

  111. Kane, J. M. & Kolb, T. E. Importance of resin ducts in reducing ponderosa pine mortality from bark beetle attack. Oecologia 164, 601–609 (2010).

    Article  Google Scholar 

  112. Ferrenberg, S., Kane, J. M. & Mitton, J. B. Resin duct characteristics associated with tree resistance to bark beetles across lodgepole and limber pines. Oecologia 174, 1283–1292 (2014).

    Article  Google Scholar 

  113. Cailleret, M. et al. A synthesis of radial growth patterns preceding tree mortality. Glob. Change Biol. 23, 1675–1690 (2017).

    Article  Google Scholar 

  114. Muller, B., Pantin, F., Génard, M., Turc, O., Freixes, S., Piques, M. & Gibon, Y. Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J. Exp. Bot. 62, 1715–1729 (2011).

    Article  Google Scholar 

  115. Yu, S. Cellular and genetic responses of plants to sugar starvation. Plant Physiol. 121, 687–693 (1999).

    Article  Google Scholar 

  116. Koster, K. L. & Leopold, A. C. Sugars and desiccation tolerance in seeds. Plant Physiol. 88, 829–832 (1988).

    Article  Google Scholar 

  117. Sapes, G., Demaree, P., Lekberg, Y. & Sala, A. Plant carbohydrate depletion impairs water relations and spreads via ectomycorrhizal networks. New Phytol. 229, 3172–3183 (2021).

    Article  Google Scholar 

  118. Hoekstra, F. A., Golovina, E. A. & Buitink, J. Mechanisms of plant desiccation tolerance. Trends Plant Sci. 6, 431–438 (2001).

    Article  Google Scholar 

  119. Van den Ende, W. & Valluru, R. Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J. Exp. Bot. 60, 9–18 (2009).

    Article  Google Scholar 

  120. Matros, A., Peshev, D., Peukert, M., Mock, H.-P. & Ende, W. Vden Sugars as hydroxyl radical scavengers: proof-of-concept by studying the fate of sucralose in Arabidopsis. Plant J. 82, 822–839 (2015).

    Article  Google Scholar 

  121. Rolland, F., Baena-González, E. & Sheen, J. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57, 675–709 (2006).

    Article  Google Scholar 

  122. Ramel, F., Sulmon, C., Bogard, M., Couée, I. & Gouesbet, G. Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol. 9, 28 (2009).

    Article  Google Scholar 

  123. Fine, P. V. A. et al. The growth–defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87, S150–S162 (2006).

    Article  Google Scholar 

  124. Huot, B., Yao, J., Montgomery, B. L. & He, S. Y. Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7, 1267–1287 (2014).

    Article  Google Scholar 

  125. Ouédraogo, D.-Y., Mortier, F., Gourlet-Fleury, S., Freycon, V. & Picard, N. Slow-growing species cope best with drought: evidence from long-term measurements in a tropical semi-deciduous moist forest of Central Africa. J. Ecol. 101, 1459–1470 (2013).

    Article  Google Scholar 

  126. de la Mata, R., Hood, S. & Sala, A. Insect outbreak shifts the direction of selection from fast to slow growth rates in the long-lived conifer Pinus ponderosa. Proc. Natl Acad. Sci. USA 114, 7391–7396 (2017).

    Article  Google Scholar 

  127. Roskilly, B., Keeling, E., Hood, S., Giuggiola, A. & Sala, A. Conflicting functional effects of xylem pit structure relate to the growth-longevity trade-off in a conifer species. Proc. Natl Acad. Sci. USA 116, 15282–15287 (2019).

    Article  Google Scholar 

  128. Snyder, K. A. & Williams, D. G. Defoliation alters water uptake by deep and shallow roots of Prosopis velutina (Velvet Mesquite). Funct. Ecol. 17, 363–374 (2003).

    Article  Google Scholar 

  129. Eyles, A., Pinkard, E. A. & Mohammed, C. Shifts in biomass and resource allocation patterns following defoliation in Eucalyptus globulus growing with varying water and nutrient supplies. Tree Physiol. 29, 753–764 (2009).

    Article  Google Scholar 

  130. Hillabrand, R. M., Hacke, U. G. & Lieffers, V. J. Defoliation constrains xylem and phloem functionality. Tree Physiol. 39, 1099–1108 (2019).

    Article  Google Scholar 

  131. Landhäusser, S. M. & Lieffers, V. J. Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees 26, 653–661 (2012).

    Article  Google Scholar 

  132. Poyatos, R., Aguadé, D., Galiano, L., Mencuccini, M. & Martínez-Vilalta, J. Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine. New Phytol. 200, 388–401 (2013).

    Article  Google Scholar 

  133. Cardoso, A. A., Batz, T. A. & McAdam, S. A. Xylem embolism resistance determines leaf mortality during drought in Persea americana. Plant Physiol. 182, 547–554 (2020).

    Article  Google Scholar 

  134. Mencuccini, M. et al. Leaf economics and plant hydraulics drive leaf:wood area ratios. New Phytol. 224, 1544–1556 (2019).

    Article  Google Scholar 

  135. Cochard, H., Pimont, F., Ruffault, J. & Martin-St Paul, N. SurEau: a mechanistic model of plant water relations under extreme drought. Ann. Forest Sci. 78, 1–23 (2021).

    Article  Google Scholar 

  136. Yin, M. C. & Blaxter, J. H. S. Temperature, salinity tolerance, and buoyancy during early development and starvation of Clyde and North Sea herring, cod, and flounder larvae. J. Exp. Mar. Biol. Ecol 107, 279–290 (1987).

    Article  Google Scholar 

  137. Cahill, G. F. Jr. Fuel metabolism in starvation. Annu. Rev. Nutr. 26, 1–22 (2006).

    Article  Google Scholar 

  138. Yandi, I. & Altinok, I. Irreversible starvation using RNA/DNA on lab-grown larval anchovy, Engraulis encrasicolus, and evaluating starvation in the field-caught larval cohort. Fish. Res. 201, 32–37 (2018).

    Article  Google Scholar 

  139. Smith, A. M. & Stitt, M. Coordination of carbon supply and plant growth. Plant Cell Environ. 30, 1126–1149 (2007).

    Article  Google Scholar 

  140. Schädel, C., Richter, A., Blöchl, A. & Hoch, G. Hemicellulose concentration and composition in plant cell walls under extreme carbon source–sink imbalances. Physiol. Plant. 139, 241–255 (2010).

    Google Scholar 

  141. Tsamir-Rimon, M. et al. Rapid starch degradation in the wood of olive trees under heat and drought is permitted by three stress-specific beta amylases. New Phytol. 229, 1398–1414 (2020).

    Article  Google Scholar 

  142. McLoughlin, F. et al. Autophagy plays prominent roles in amino acid, nucleotide, and carbohydrate metabolism during fixed-carbon starvation in maize. Plant Cell 32, 2699–2724 (2020).

    Article  Google Scholar 

  143. Quirk, J., McDowell, N. G., Leake, J. R., Hudson, P. J. & Beerling, D. J. Increased susceptibility to drought-induced mortality in Sequoia sempervirens (Cupressaceae) trees under Cenozoic atmospheric carbon dioxide starvation. Am. J. Bot. 100, 582–591 (2013).

    Article  Google Scholar 

  144. 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).

    Article  Google Scholar 

  145. Tomasella, M., Petrussa, E., Petruzzellis, F., Nardini, A. & Casolo, V. The possible role of non-structural carbohydrates in the regulation of tree hydraulics. Int. J. Mol. Sci. 21, 144 (2020).

    Article  Google Scholar 

  146. Gaylord, M. L. et al. Drought predisposes piñon–juniper woodlands to insect attacks and mortality. New Phytol. 198, 567–578 (2013).

    Article  Google Scholar 

  147. Dickman, L. T., McDowell, N. G., Sevanto, S., Pangle, R. E. & Pockman, W. T. Carbohydrate dynamics and mortality in a piñon-juniper woodland under three future precipitation scenarios. Plant Cell Environ. 38, 729–739 (2015).

    Article  Google Scholar 

  148. Ruehr, N. K. et al. Drought effects on allocation of recent carbon: from beech leaves to soil CO2 efflux. New Phytol. 184, 950–961 (2009).

    Article  Google Scholar 

  149. 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).

    Article  Google Scholar 

  150. Hagedorn, F. et al. Recovery of trees from drought depends on belowground sink control. Nat. Plants 2, 16111 (2016).

    Article  Google Scholar 

  151. Hesse, B. D., Goisser, M., Hartmann, H. & Grams, T. E. E. Repeated summer drought delays sugar export from the leaf and impairs phloem transport in mature beech. Tree Physiol. 39, 192–200 (2019).

    Article  Google Scholar 

  152. Wiley, E., Hoch, G. & Landhäusser, S. M. Dying piece by piece: carbohydrate dynamics in aspen (Populus tremuloides) seedlings under severe carbon stress. J. Exp. Bot. 68, 5221–5232 (2017).

    Article  Google Scholar 

  153. Weber, R. et al. Living on next to nothing: tree seedlings can survive weeks with very low carbohydrate concentrations. New Phytol. 218, 107–118 (2018).

    Article  Google Scholar 

  154. Hasanuzzaman, M. & Tanveer, M. (eds) Salt and Drought Stress Tolerance in Plants: Signaling Networks and Adaptive Mechanisms (Springer, 2020)

  155. O’Brien, M. J., Leuzinger, S., Philipson, C. D., Tay, J. & Hector, A. Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat. Clim. Chang. 4, 710–714 (2014).

    Article  Google Scholar 

  156. Nardini, A. et al. Rooting depth, water relations and non-structural carbohydrate dynamics in three woody angiosperms differentially affected by an extreme summer drought. Plant Cell Environ. 39, 618–627 (2016).

    Article  Google Scholar 

  157. Zinselmeier, C., Westgate, M. E., Schussler, J. R. & Jones, R. J. Low water potential disrupts carbohydrate metabolism in maize (Zea mays L.) ovaries. Plant Physiol. 107, 385–391 (1995).

    Article  Google Scholar 

  158. Desprez-Loustau, M.-L., Marçais, B., Nageleisen, L.-M., Piou, D. & Vannini, A. Interactive effects of drought and pathogens in forest trees. Ann. For. Sci. 63, 597–612 (2006).

    Article  Google Scholar 

  159. Oliva, J., Stenlid, J. & Martínez-Vilalta, J. The effect of fungal pathogens on the water and carbon economy of trees: implications for drought-induced mortality. New Phytol. 203, 1028–1035 (2014).

    Article  Google Scholar 

  160. Kolb, T. et al. Drought-mediated changes in tree physiological processes weaken tree defenses to bark beetle attack. J. Chem. Ecol. 45, 888–900 (2019).

    Article  Google Scholar 

  161. Croize, L., Lieutier, F., Cochard, H. & Dreyer, E. Effects of drought stress and high density stem inoculations with Leptographium wingfieldii on hydraulic properties of young Scots pine trees. Tree Physiol. 21, 427–436 (2001).

    Article  Google Scholar 

  162. Wullschleger, S. D., McLaughlin, S. B. & Ayres, M. P. High-resolution analysis of stem increment and sap flow for loblolly pine trees attacked by southern pine beetle. Can. J. For. Res. 34, 387–2393 (2004).

    Article  Google Scholar 

  163. Hubbard, R. M., Rhoades, C. C., Elder, K. & Negron, J. Changes in transpiration and foliage growth in lodgepole pine trees following mountain pine beetle attack and mechanical girdling. For. Ecol. Manag. 289, 312–317 (2013).

    Article  Google Scholar 

  164. Manter, D. K. & Kavanagh, K. L. Stomatal regulation in Douglas fir following a fungal-mediated chronic reduction in leaf area. Trees 17, 485–491 (2003).

    Article  Google Scholar 

  165. Lahr, E. L. & Sala, A. Sapwood stored resources decline in whitebark and lodgepole pines attacked by mountain pine beetles (Coleoptera: Curculionidae). Environ. Entomol. 45, 1463–1475 (2016).

    Article  Google Scholar 

  166. Marler, T. E. & Cascasan, A. N. Carbohydrate depletion during lethal infestation of Aulacaspis yasumatsui on Cycas revoluta. Int. J. Plant Sci. 179, 497–504 (2018).

    Article  Google Scholar 

  167. Hood, S. & Sala, A. Ponderosa pine resin defenses and growth: metrics matter. Tree Physiol. 35, 1223–1235 (2015).

    Google Scholar 

  168. Roth, M., Hussain, A., Cale, J. A. & Erbilgin, N. Successful colonization of lodgepole pine trees by mountain pine beetle increased monoterpene production and exhausted carbohydrate reserves. J. Chem. Ecol. 44, 209–214 (2018).

    Article  Google Scholar 

  169. Raffa, K. F. et al. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. Bioscience 58, 501–517 (2008).

    Article  Google Scholar 

  170. Seidl, R., Schelhaas, M. J., Rammer, W. & Verkerk, P. J. Increasing forest disturbances in Europe and their impact on carbon storage. Nat. Clim. Chang. 4, 806–810 (2014).

    Article  Google Scholar 

  171. Ryan, M. G., Sapes, G., Sala, A. & Hood, S. M. Tree physiology and bark beetles. New Phytol. 205, 955–957 (2015).

    Article  Google Scholar 

  172. Huang, J. et al. Tree defence and bark beetles in a drying world: carbon partitioning, functioning and modelling. New Phytol. 225, 26–36 (2020).

    Article  Google Scholar 

  173. Goodsman, D. W., Lusebrink, I., Landhäusser, S. M., Erbilgin, N. & Lieffers, V. J. Variation in carbon availability, defense chemistry and susceptibility to fungal invasion along the stems of mature trees. New Phytol. 197, 586–594 (2013).

    Article  Google Scholar 

  174. Wiley, E., Rogers, B. J., Hodgkinson, R. & Landhäusser, S. M. Nonstructural carbohydrate dynamics of lodgepole pine dying from mountain pine beetle attack. New Phytol. 209, 550–562 (2016).

    Article  Google Scholar 

  175. Netherer, S. et al. Do water-limiting conditions predispose Norway spruce to bark beetle attack? New Phytol. 205, 1128–1141 (2015).

    Article  Google Scholar 

  176. Rissanen, K. et al. Drought effects on carbon allocation to resin defences and on resin dynamics in old-grown Scots pine. Environ. Exp. Bot. 185, 104410 (2021).

    Article  Google Scholar 

  177. Gershenzon, J. Metabolic costs of terpenoid accumulation in higher plants. J. Chem. Ecol. 20, 1281–1328 (1994).

    Article  Google Scholar 

  178. Navarro, L. et al. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr. Biol. 1, 650–655 (2008).

    Article  Google Scholar 

  179. Fox, H. et al. Transcriptome analysis of Pinus halepensis under drought stress and during recovery. Tree Physiol. 38, 423–441 (2018).

    Article  Google Scholar 

  180. Caretto, S., Linsalata, V., Colella, G., Mita, G. & Lattanzio, V. Carbon fluxes between primary metabolism and phenolic pathway in plant tissues under stress. Int. J. Mol. Sci. 16, 26378–26394 (2015).

    Article  Google Scholar 

  181. Franceschi, V. R., Krokene, P., Christiansen, E. & Krekling, T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol. 167, 353–376 (2005).

    Article  Google Scholar 

  182. Suárez-Vidal, E. et al. Drought stress modifies early effective resistance and induced chemical defences of Aleppo pine against a chewing insect herbivore. Environ. Exp. Bot. 162, 550–559 (2019).

    Article  Google Scholar 

  183. Hood, S., Sala, A., Heyerdahl, E. K. & Boutin, M. Low-severity fire increases tree defense against bark beetle attacks. Ecology 96, 1846–1855 (2015).

    Article  Google Scholar 

  184. Zhao, S. & Erbilgin, N. Larger resin ducts are linked to the survival of lodgepole pine trees during mountain pine beetle outbreak. Front. Plant Sci. 10, 1459 (2019).

    Article  Google Scholar 

  185. Kichas, N. E., Hood, S. M., Pederson, G. T., Everett, R. G. & McWethy, D. B. Whitebark pine (Pinus albicaulis) growth and defense in response to mountain pine beetle outbreaks. For. Ecol. Manag. 457, 117736 (2020).

    Article  Google Scholar 

  186. Gaylord, M. L., Kolb, T. E. & McDowell, N. G. Mechanisms of piñon pine mortality after severe drought: a retrospective study of mature trees. Tree Physiol. 35, 806–816 (2015).

    Article  Google Scholar 

  187. Anderegg, W. et al. Tree mortality predicted from drought-induced vascular damage. Nat. Geosci. 8, 367–371 (2015).

    Article  Google Scholar 

  188. De Kauwe, M. G. et al. Identifying areas at risk of drought-induced tree mortality across South-Eastern Australia. Glob. Change Biol. 26, 5716–5733 (2020).

    Article  Google Scholar 

  189. Sperry, J. S. et al. The impact of rising CO2 and acclimation on the response of US forests to global warming. Proc. Natl Acad. Sci. USA 116, 25734–25744 (2019).

    Article  Google Scholar 

  190. Medlyn, B. E. et al. Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. New Phytol. 149, 247–264 (2001).

    Article  Google Scholar 

  191. Klein, T. & Ramon, U. Stomatal sensitivity to CO2 diverges between angiosperm and gymnosperm tree species. Funct. Ecol. 33, 1411–1424 (2019).

    Article  Google Scholar 

  192. Paudel, I. et al. Elevated CO2 compensates for drought effects in lemon saplings via stomatal downregulation, increased soil moisture, and increased wood carbon storage. Environ. Exp. Bot. 148, 117–127 (2018).

    Article  Google Scholar 

  193. Bobich, E. G., Barron-Gafford, G. A., Rascher, K. G. & Murthy, R. Effects of drought and changes in vapour pressure deficit on water relations of Populus deltoides growing in ambient and elevated CO2. Tree Physiol. 30, 866–875 (2010).

    Article  Google Scholar 

  194. Gimeno, T. E., McVicar, T. R., O’Grady, A. P., Tissue, D. T. & Ellsworth, D. S. Elevated CO2 did not affect the hydrological balance of a mature native Eucalyptus woodland. Glob. Change Biol. 24, 3010–3024 (2018).

    Article  Google Scholar 

  195. Nowak, R. S. et al. Elevated atmospheric CO2 does not conserve soil water in the mojave desert. Ecology 85, 93–99 (2004).

    Article  Google Scholar 

  196. Schäfer, K. V., Oren, R., Lai, C. T. & Katul, G. G. Hydrologic balance in an intact temperate forest ecosystem under ambient and elevated atmospheric CO2 concentration. Glob. Change Biol. 8, 895–911 (2002).

    Article  Google Scholar 

  197. Novick, K. A., Katul, G. G., McCarthy, H. R. & Oren, R. Increased resin flow in mature pine trees growing under elevated CO2 and moderate soil fertility. Tree Physiol. 32, 752–763 (2012).

    Article  Google Scholar 

  198. Li, X. M. et al. Temperature alters the response of hydraulic architecture to CO2 in cotton plants (Gossypium hirsutum). Environ. Exp. Bot. 172, 104004 (2020).

    Article  Google Scholar 

  199. Li, W. et al. The sweet side of global change–dynamic responses of non-structural carbohydrates to drought, elevated CO2 and nitrogen fertilization in tree species. Tree Physiol. 38, 1706–1723 (2018).

    Google Scholar 

  200. 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).

    Article  Google Scholar 

  201. Duan, H. et al. CO2 and temperature effects on morphological and physiological traits affecting risk of drought-induced mortality. Tree Physiol. 38, 1138–1151 (2018).

    Article  Google Scholar 

  202. Zavala, J. A., Nabity, P. D. & DeLucia, E. H. An emerging understanding of mechanisms governing insect herbivory under elevated CO2. Annu. Rev. Entomol. 58, 79–97 (2013).

    Article  Google Scholar 

  203. Kazan, K. Plant-biotic interactions under elevated CO2: a molecular perspective. Environ. Exp. Bot. 153, 249–261 (2018).

    Article  Google Scholar 

  204. Gessler, A., Schaub, M. & McDowell, N. G. The role of nutrients in drought-induced tree mortality and recovery. New Phytol. 214, 513–520 (2017).

    Article  Google Scholar 

  205. Mackay, D. S. et al. Interdependence of chronic hydraulic dysfunction and canopy processes can improve integrated models of tree response to drought. Water Resour. Res. 51, 6156–6176 (2015).

    Article  Google Scholar 

  206. Mackay, D. S. et al. Conifers depend on established roots during drought: results from a coupled model of carbon allocation and hydraulics. New Phytol. 225, 679–692 (2020).

    Article  Google Scholar 

  207. Tai, X. et al. Plant hydraulic stress explained tree mortality and tree size explained beetle attack in a mixed conifer forest. J. Geophys. Res. Biogeosci. 124, 3555–3568 (2019).

    Article  Google Scholar 

  208. Sala, A., Piper, F. & Hoch, G. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol. 186, 274–281 (2010).

    Article  Google Scholar 

  209. Limousin, J. M. et al. Regulation and acclimation of leaf gas exchange in a piñon–juniper woodland exposed to three different precipitation regimes. Plant Cell Environ. 36, 1812–1825 (2013).

    Article  Google Scholar 

  210. Sorek, Y. et al. An increase in xylem embolism resistance of grapevine leaves during the growing season is coordinated with stomatal regulation, turgor loss point and intervessel pit membranes. New Phytol. 229, 1955–1969 (2021).

    Article  Google Scholar 

  211. Hudson, P. J. et al. Impacts of long-term precipitation manipulation on hydraulic architecture and xylem anatomy of piñon and juniper in Southwest USA. Plant Cell Environ. 41, 421–435 (2018).

    Article  Google Scholar 

  212. Warren, J. M., Norby, R. J. & Wullschleger, S. D. Elevated CO2 enhances leaf senescence during extreme drought in a temperate forest. Tree Physiol. 31, 117–130 (2011).

    Article  Google Scholar 

  213. Matusick, G. et al. Chronic historical drought legacy exacerbates tree mortality and crown dieback during acute heatwave-compounded drought. Environ. Res. Lett. 13, 095002 (2018).

    Article  Google Scholar 

  214. Shirley, H. L. Lethal high temperatures for conifers, and the cooling effect of transpiration. J. Agric. Res. 53, 239–258 (1936).

    Google Scholar 

  215. Fisher, R. A. & Koven, C. D. Perspectives on the future of land surface models and the challenges of representing complex terrestrial systems. J. Adv. Model. Earth Syst. 12, e2018MS001453 (2020).

    Article  Google Scholar 

  216. Menzel, A., Sparks, T. H., Estrella, N. & Roy, D. B. Altered geographic and temporal variability in phenology in response to climate change. Glob. Ecol. Biogeogr. 15, 498–504 (2006).

    Article  Google Scholar 

  217. Keenan, T. F. et al. Net carbon uptake has increased through warming-induced changes in temperate forest phenology. Nat. Clim. Chang. 4, 598–604 (2014).

    Article  Google Scholar 

  218. Nakamura, T. et al. Tree hazards compounded by successive climate extremes after masting in a small endemic tree, Distylium lepidotum, on subtropical islands in Japan. Glob. Change Biol 27, 5094–5108 (2021).

    Article  Google Scholar 

  219. Hummel, I. et al. Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol. 154, 357–372 (2010).

    Article  Google Scholar 

  220. Jamieson, M. A., Trowbridge, A. M., Raffa, K. F. & Lindroth, R. L. Consequences of climate warming and altered precipitation patterns for plant-insect and multitrophic interactions. Plant Physiol. 160, 1719–1727 (2012).

    Article  Google Scholar 

  221. Mithöfer, A. & Boland, W. Plant defense against herbivores: chemical aspects. Annu. Rev. Plant Biol. 63, 431–450 (2012).

    Article  Google Scholar 

  222. Netherer, S. et al. Interactions among Norway spruce, the bark beetle Ips typographus and its fungal symbionts in times of drought. J. Pest Sci. 94, 591–614 (2021).

    Article  Google Scholar 

  223. Love, D. M. et al. Dependence of aspen stands on a subsurface water subsidy: implications for climate change impacts. Water Resour. Res. 55, 1833–1848 (2019).

    Article  Google Scholar 

  224. McDowell, N. G. et al. Mechanisms of a coniferous woodland persistence under drought and heat. Environ. Res. Lett. 14, 045014 (2019).

    Article  Google Scholar 

  225. Rozendaal, D. M. et al. Competition influences tree growth, but not mortality, across environmental gradients in Amazonia and tropical Africa. Ecology 101, e03052 (2020).

    Article  Google Scholar 

  226. Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Clim. 27, 511–526 (2014).

    Article  Google Scholar 

  227. CH2018 Project Team. CH2018 — climate scenarios for Switzerland. NCCS https://doi.org/10.18751/Climate/Scenarios/CH2018/1.0 (2018).

    Article  Google Scholar 

  228. McMaster, G. S. & Wilhelm, W. W. Growing degree-days: one equation, two interpretations. Agric. For. Meteorol. 87, 291–300 (1997).

    Article  Google Scholar 

  229. McDowell, N. G. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol. 155, 1051–1059 (2011).

    Article  Google Scholar 

Download references

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

Authors

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.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

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.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s43017-022-00272-1

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing