Abstract

Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity1. One primary cause of productivity loss and plant mortality during drought is hydraulic failure2,3,4. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (<1 megapascal) hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe5,6. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk7,8.

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References

  1. 1.

    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)

  2. 2.

    & Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol. 149, 575–584 (2009)

  3. 3.

    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)

  4. 4.

    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)

  5. 5.

    et al. The Copenhagen Diagnosis: Updating the World on the Latest Climate Science (Elsevier, 2009)

  6. 6.

    et al. Detection of human influence on twentieth-century precipitation trends. Nature 448, 461–465 (2007)

  7. 7.

    & Amazonian rain forests and drought: response and vulnerability. New Phytol. 187, 553–557 (2010)

  8. 8.

    et al. Drought sensitivity of the amazon rainforest. Science 323, 1344–1347 (2009)

  9. 9.

    et al. Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447, 80–82 (2007)

  10. 10.

    & Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. Am. J. Bot. 87, 1287–1299 (2000)

  11. 11.

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

  12. 12.

    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)

  13. 13.

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

  14. 14.

    & Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 329, 940–943 (2010)

  15. 15.

    Tropical forests and the changing earth system. Phil. Trans. R. Soc. B 361, 195–210 (2006)

  16. 16.

    , & Sustained and significant negative water pressure in xylem. Nature 378, 715–716 (1995)

  17. 17.

    & Vulnerability of xylem to cavitation and embolism. Annu. Rev. Plant Phys. Mol. Bio. 40, 19–38 (1989)

  18. 18.

    , & Size and function in conifer tracheids and angiosperm vessels. Am. J. Bot. 93, 1490–1500 (2006)

  19. 19.

    , & Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85, 2184–2199 (2004)

  20. 20.

    , , & Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding. Plant Cell Environ. 33, 2101–2111 (2010)

  21. 21.

    , , & Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell Environ. 21, 347–359 (1998)

  22. 22.

    , & Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105, 293–301 (1996)

  23. 23.

    , , , & Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct. Ecol. 23, 922–930 (2009)

  24. 24.

    , , , & The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. Plant Physiol. 154, 1088–1095 (2010)

  25. 25.

    , , , & Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit. New Phytol. 188, 533–542 (2010)

  26. 26.

    , & The hydraulic architecture of Pinaceae—a review. Plant Ecol. 171, 3–13 (2004)

  27. 27.

    , , & Hydraulic architecture of deciduous and evergreen dry rainforest tree species from north-eastern Australia. Trees 19, 305–311 (2005)

  28. 28.

    , , , & in Size- and Age-Related Changes in Tree Structure and Function Vol. 4 (eds et al.). 341–361 (Springer, 2011)

  29. 29.

    et al. Uniform selection as a primary force reducing population genetic differentiation of cavitation resistance across a species range. PLoS ONE 6, e23476 (2011)

  30. 30.

    et al. Genotypic variability and phenotypic plasticity of cavitation resistance in Fagus sylvatica L. across Europe. Tree Physiol. 31, 1175–1182 (2011)

Download references

Acknowledgements

We thank the ARC-NZ Vegetation Function Network for hosting the original working group from which the data set was compiled. We are grateful to the Alexander von Humboldt Foundation for supporting B.C. during preparation of the manuscript.

Author information

Author notes

    • Brendan Choat
    •  & Steven Jansen

    These authors contributed equally to this work.

Affiliations

  1. University of Western Sydney, Hawkesbury Institute for the Environment, Richmond, New South Wales 2753, Australia

    • Brendan Choat
  2. Ulm University, Institute for Systematic Botany and Ecology, Albert-Einstein-Allee 11, 89081 Ulm, Germany

    • Steven Jansen
  3. University of Tasmania, School of Plant Science, Private Bag 55, Hobart, Tasmania 7001, Australia

    • Tim J. Brodribb
  4. INRA, UMR547 PIAF, F-63100 Clermont-Ferrand, France

    • Hervé Cochard
  5. Clermont Université, Université Blaise Pascal, UMR547 PIAF, F-63000 Clermont-Ferrand, France

    • Hervé Cochard
  6. INRA, University of Bordeaux, UMR BIOGECO, 33450 Talence, France

    • Sylvain Delzon
  7. Brown University, Environmental Change Initiative, Box 1951, 167 Thayer Street, Providence, Rhode Island 02912, USA

    • Radika Bhaskar
  8. Universidad Nacional de la Patagonia San Juan Bosco, Departmento de Biología, Facultad de Ciencias Naturales, 9000 Comodoro Rivadavia, Argentina

    • Sandra J. Bucci
  9. James Cook University, School of Marine and Tropical Biology, Townsville, Queensland 4811, Australia

    • Taylor S. Feild
  10. Macquarie University, Department of Biological Sciences, New South Wales 2109, Australia

    • Sean M. Gleason
    • , Mark Westoby
    •  & Ian J. Wright
  11. University of Alberta, Department of Renewable Resources, Edmonton, Alberta T6G 2E3, Canada

    • Uwe G. Hacke
  12. California State University, Department of Biology, Bakersfield, California 93311, USA

    • Anna L. Jacobsen
    •  & R. Brandon Pratt
  13. Naturalis Biodiversity Centre, Leiden University, PO Box 9514, 2300 RA Leiden, The Netherlands

    • Frederic Lens
  14. University of Guelph, Department of Integrative Biology, 50 Stone Road East, Guelph, Ontario N1G 2W1, Canada

    • Hafiz Maherali
  15. CREAF, Cerdanyola del Vallès 08193, Spain

    • Jordi Martínez-Vilalta
  16. Universitat Autònoma Barcelona, Cerdanyola del Vallès 08193, Spain

    • Jordi Martínez-Vilalta
  17. University Innsbruck, Institut für Botank, Sternwartestrasse 15, A-6020 Innsbruck, Austria

    • Stefan Mayr
  18. ICREA at CREAF, Univ Autònoma Barcelona, Cerdanyola del Vallès 08193, Spain

    • Maurizio Mencuccini
  19. University of Edinburgh, School of GeoSciences, Crew Building, West Mains Road, Edinburgh EH9 3JN, UK

    • Maurizio Mencuccini
  20. CSIRO, Ecosystem Sciences, College Road, Sandy Bay, Tasmania 7005, Australia

    • Patrick J. Mitchell
  21. Università di Trieste, Dipartimento di Scienze della Vita, Via L. Giorgieri 10, 34127 Trieste, Italy

    • Andrea Nardini
  22. University of California, Santa Cruz, Department of Ecology and Evolutionary Biology, California 95064, USA

    • Jarmila Pittermann
  23. University of Utah, Department of Biology, 257 South 1400 East, Salt Lake City, Utah 84112, USA

    • John S. Sperry
  24. Missouri Botanical Garden, Center for Conservation and Sustainable Development, St. Louis, Missouri 63166, USA

    • Amy E. Zanne
  25. George Washington University, Department of Biological Sciences, 2023 G Street NW, Washington DC 20052, USA

    • Amy E. Zanne

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Contributions

B.C. and S.J. led the initial working group and coordinated the analysis and write-up of the work. B.C., S.J., T.J.B., H.C., S.D., R.B., S.J.B., T.S.F., S.M.G., U.G.H., A.L.J., F.L., H.M., J.M.-V., S.M., M.M., P.J.M., A.N., J.P., R.B.P., J.S.S., M.W., I.J.W. and A.E.Z. contributed to compilation and organization of the data set and writing of the manuscript. S.M.G. and I.J.W. extracted climate data from the WorldClim and CRU climate databases. H.M., M.M. and J.M.-V. assisted in statistical analyses of the data set.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Steven Jansen.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Figures 1 and 2 and additional references.

Excel files

  1. 1.

    Supplementary Table 1

    This file contains the dataset compiled from published work and unpublished data of the authors, including species names, Ψ50, Ψ88, Ψmin, safety margins, climate data, life form, biome, site data, and the sources of published data.This file was corrected on 23 January 2013 to correct an error in the dataset.

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DOI

https://doi.org/10.1038/nature11688

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