Letter | Published:

Death from drought in tropical forests is triggered by hydraulics not carbon starvation

Nature volume 528, pages 119122 (03 December 2015) | Download Citation


Drought threatens tropical rainforests over seasonal to decadal timescales1,2,3,4, but the drivers of tree mortality following drought remain poorly understood5,6. It has been suggested that reduced availability of non-structural carbohydrates (NSC) critically increases mortality risk through insufficient carbon supply to metabolism (‘carbon starvation’)7,8. However, little is known about how NSC stores are affected by drought, especially over the long term, and whether they are more important than hydraulic processes in determining drought-induced mortality. Using data from the world’s longest-running experimental drought study in tropical rainforest (in the Brazilian Amazon), we test whether carbon starvation or deterioration of the water-conducting pathways from soil to leaf trigger tree mortality. Biomass loss from mortality in the experimentally droughted forest increased substantially after >10 years of reduced soil moisture availability. The mortality signal was dominated by the death of large trees, which were at a much greater risk of hydraulic deterioration than smaller trees. However, we find no evidence that the droughted trees suffered carbon starvation, as their NSC concentrations were similar to those of non-droughted trees, and growth rates did not decline in either living or dying trees. Our results indicate that hydraulics, rather than carbon starvation, triggers tree death from drought in tropical rainforest.

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  1. 1.

    et al. in Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds , , , , et al.) (Cambridge Univ. Press, 2013)

  2. 2.

    et al. The projected timing of climate departure from recent variability. Nature 502, 183–187 (2013)

  3. 3.

    et al. Climate extremes and the carbon cycle. Nature 500, 287–295 (2013)

  4. 4.

    , , & Projected strengthening of Amazonian dry season by constrained climate model simulations. Nat. Clim. Chang. 5, 656–660 (2015)

  5. 5.

    , , , & Research frontiers in drought-induced tree mortality: crossing scales and disciplines. New Phytol. 205, 965–969 (2015)

  6. 6.

    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)

  7. 7.

    et al. Drought impact on forest carbon dynamics and fluxes in Amazonia. Nature 519, 78–82 (2015)

  8. 8.

    , , , & Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat. Clim. Chang. 4, 710–714 (2014)

  9. 9.

    , , , & Mortality of large trees and lianas following experimental drought in an Amazon forest. Ecology 88, 2259–2269 (2007)

  10. 10.

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

  11. 11.

    et al. Drought effects on litterfall, wood production and belowground carbon cycling in an Amazon forest: results of a throughfall reduction experiment. Philos. Trans. R. Soc. B 363, 1839–1848 (2008)

  12. 12.

    et al. Ecosystem respiration and net primary productivity after 8–10 years of experimental through-fall reduction in an eastern Amazon forest. Plant Ecol. Divers. 7, 7–24 (2014)

  13. 13.

    et al. Threshold responses to soil moisture deficit by trees and soil in tropical rain forests: insights from field experiments. Bioscience 65, 882–892 (2015)

  14. 14.

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

  15. 15.

    Senescence, ageing and death of the whole plant. New Phytol. 197, 696–711 (2013)

  16. 16.

    , & Drought-related tree mortality: addressing the gaps in understanding and prediction. New Phytol. 207, 28–33 (2015)

  17. 17.

    et al. Drought’s legacy: multiyear hydraulic deterioration underlies widespread aspen forest die-off and portends increased future risk. Glob. Chang. Biol. 19, 1188–1196 (2013)

  18. 18.

    et al. After more than a decade of soil moisture deficit, tropical rainforest trees maintain photosynthetic capacity, despite increased leaf respiration. Glob. Chang. Biol. (2015)

  19. 19.

    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)

  20. 20.

    et al. Global convergence in the vulnerability of forests to drought. Nature 491, 752–755 (2012)

  21. 21.

    , & Carbon dynamics in trees: feast or famine? Tree Physiol. 32, 764–775 (2012)

  22. 22.

    Carbon limitation in trees. J. Ecol. 91, 4–17 (2003)

  23. 23.

    et al. Size-mediated ageing reduces vigour in trees. Ecol. Lett. 8, 1183–1190 (2005)

  24. 24.

    , , & Stomatal penetration by aqueous solutions – an update involving leaf surface particles. New Phytol. 196, 774–787 (2012)

  25. 25.

    & Foliar uptake of water by wet leaves of Sloanea woollsii, an australian subtropical rain-forest tree. Aust. J. Bot. 43, 157–167 (1995)

  26. 26.

    , & Foliar uptake of fog water and transport belowground alleviates drought effects in the cloud forest tree species, Drimys brasiliensis (Winteraceae). New Phytol. 199, 151–162 (2013)

  27. 27.

    , & Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol. 201, 1086–1095 (2014)

  28. 28.

    et al. Do global change experiments overestimate impacts on terrestrial ecosystems? Trends Ecol. Evol. 26, 236–241 (2011)

  29. 29.

    & in Ecosystems and sustainable development IV (eds , , , & , ) Vol. 2, 1113–1121 (WIT Press, 2003)

  30. 30.

    et al. The response of an Eastern Amazonian rain forest to drought stress: results and modelling analyses from a throughfall exclusion experiment. Glob. Chang. Biol. 13, 2361–2378 (2007)

  31. 31.

    , , , & Evaluating climatic and soil water controls on evapotranspiration at two Amazonian rainforest sites. Agric. For. Meteorol. 148, 850–861 (2008)

  32. 32.

    et al. Improved allometric models to estimate the aboveground biomass of tropical trees. Glob. Chang. Biol. 20, 3177–3190 (2014)

  33. 33.

    et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009)

  34. 34.

    et al. Data from: Towards a worldwide wood economics spectrum. Dryad Digital Repository. (2009)

  35. 35.

    et al. Branch xylem density variations across the Amazon Basin. Biogeosciences 6, 545–568 (2009)

  36. 36.

    et al. Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia 145, 87–99 (2005)

  37. 37.

    et al. Tree height integrated into pantropical forest biomass estimates. Biogeosciences 9, 3381–3403 (2012)

  38. 38.

    et al. Shifts in plant respiration and carbon use efficiency at a large-scale drought experiment in the eastern Amazon. New Phytol. 187, 608–621 (2010)

  39. 39.

    et al. The sensitivity of wood production to seasonal and interannual variations in climate in a lowland Amazonian rainforest. Oecologia 174, 295–306 (2014)

  40. 40.

    , , , & How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ. 37, 153–161 (2014)

  41. 41.

    , , & How reliable is the double-ended pressure sleeve technique for assessing xylem vulnerability to cavitation in woody angiosperms? Physiol. Plant. 142, 205–210 (2011)

  42. 42.

    et al. Genotypic variability in vulnerability of leaf xylem to cavitation in water-stressed and well-irrigated sugarcane. Plant Physiol. 100, 1020–1028 (1992)

  43. 43.

    & Mixed-Effects Models in S and S-PLUS (Springer, 2000)

  44. 44.

    , , , & Evidence from Amazonian forests is consistent with isohydric control of leaf water potential. Plant Cell Environ. 29, 151–165 (2006)

  45. 45.

    et al. Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecol. Lett. 17, 324–332 (2014)

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This work was supported by UK NERC grant NE/J011002/1 to P.M. and M.M., CNPQ grant 457914/2013-0/MCTI/CNPq/FNDCT/LBA/ESECAFLOR to A.C.L.D., and ARC grant FT110100457 to P.M. It was previously supported by NERC NER/A/S/2002/00487, NERC GR3/11706, EU FP5-Carbonsink and EU FP7-Amazalert to P.M. and J.G., and by grant support to Y.M. from NERC NE/D01025X/1 and the Gordon and Betty Moore Foundation. L.R., M.M. and P.M. would also like to acknowledge support from S. Sitch, Y. Salmon and B. Christoffersen. The authors would also like to thank three anonymous referees for their useful comments.

Author information


  1. School of GeoSciences, University of Edinburgh, Edinburgh EH9 3FF, UK

    • L. Rowland
    • , O. J. Binks
    • , J. Grace
    • , M. Mencuccini
    •  & P. Meir
  2. Centro de Geosciências, Universidade Federal do Pará, Belém 66075-110, Brazil

    • A. C. L. da Costa
    •  & A. A. R. Oliveira
  3. School of Geography, University of Leeds, Leeds LS2 9JT, UK

    • D. R. Galbraith
  4. Instituto de Biologia, UNICAMP, Campinas 13.083-970, Brazil

    • R. S. Oliveira
  5. The University of Cambridge, Cambridge CB2 1TN, UK

    • A. M. Pullen
  6. Environmental Change Institute, The University of Oxford, Oxford OX1 3QY, UK

    • C. E. Doughty
    •  & Y. Malhi
  7. Department of Physical Geography and Ecosystem Science, Lund University, Lund S-223 62, Sweden

    • D. B. Metcalfe
  8. EMBRAPA Amazônia Oriental, Belém 66095-903, Brazil

    • S. S. Vasconcelos
  9. Museu Paraense Emílio Goeldi, Belém 66077-830, Brazil

    • L. V. Ferreira
  10. ICREA at CREAF, 08193 Cerdanyola del Vallés, Spain

    • M. Mencuccini
  11. Research School of Biology, Australian National University, Canberra, Australian Capital Territory 2601, Australia

    • P. Meir


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L.R., P.M., A.C.L.D. and M.M. designed and implemented the research. P.M. conceived and led the experiment and this study. L.R. led recent measurements; all authors contributed to data collection, led by A.C.L.D.; L.R. analysed the data with M.M., P.M., O.J.B. and A.M.P.; L.R. wrote the paper with P.M. and M.M., with contributions from all authors.

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The authors declare no competing financial interests.

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Correspondence to L. Rowland.

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