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.

  • Letter
  • Published:

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

Nature volume 528, pages 119–122 (2015)Cite this article

Subjects

Abstract

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.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Changes in biomass and mortality rates.
Figure 2: Tree growth of living and dead trees.
Figure 3: Leaf, branch and stem NSC concentrations.
Figure 4: Xylem vulnerability to embolism and predicted loss of xylem hydraulic conductivity as a function of tree diameter (dbh).

Similar content being viewed by others

References

  1. Christensen, J. H. 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 Stocker, T. F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S. K. et al.) (Cambridge Univ. Press, 2013)

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

    Article  CAS  ADS  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  4. Boisier, J. P., Ciais, P., Ducharne, A. & Guimberteau, M. Projected strengthening of Amazonian dry season by constrained climate model simulations. Nat. Clim. Chang. 5, 656–660 (2015)

    Article  ADS  Google Scholar 

  5. Hartmann, H., Adams, H. D., Anderegg, W. R. L., Jansen, S. & Zeppel, M. J. B. Research frontiers in drought-induced tree mortality: crossing scales and disciplines. New Phytol. 205, 965–969 (2015)

    Article  Google Scholar 

  6. 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)

    Article  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  8. 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  ADS  Google Scholar 

  9. Nepstad, D. C., Tohver, I. M., Ray, D., Moutinho, P. & Cardinot, G. Mortality of large trees and lianas following experimental drought in an Amazon forest. Ecology 88, 2259–2269 (2007)

    Article  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  11. Brando, P. M. 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)

    Article  Google Scholar 

  12. da Costa, A. C. L. 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)

    Article  Google Scholar 

  13. Meir, P. 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)

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  16. Meir, P., Mencuccini, M. & Dewar, R. C. Drought-related tree mortality: addressing the gaps in understanding and prediction. New Phytol. 207, 28–33 (2015)

    Article  Google Scholar 

  17. Anderegg, W. R. L. 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)

    Google Scholar 

  18. Rowland, L. 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. 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)

    Article  CAS  ADS  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  21. Sala, A., Woodruff, D. R. & Meinzer, F. C. Carbon dynamics in trees: feast or famine? Tree Physiol. 32, 764–775 (2012)

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Burkhardt, J., Basi, S., Pariyar, S. & Hunsche, M. Stomatal penetration by aqueous solutions – an update involving leaf surface particles. New Phytol. 196, 774–787 (2012)

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  26. Eller, C. B., Lima, A. L. & Oliveira, R. S. 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)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  29. Ruivo, M. L. P. & Cunha, E. C. in Ecosystems and sustainable development IV (eds Tiezzi, E., Brebbia, C. A. & Uso, J.-L. ) Vol. 2, 1113–1121 (WIT Press, 2003)

    Google Scholar 

  30. Fisher, R. A. 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)

    Google Scholar 

  31. Fisher, R. A., Williams, M., Ruivo, M. D., de Costa, A. L. & Meira, P. Evaluating climatic and soil water controls on evapotranspiration at two Amazonian rainforest sites. Agric. For. Meteorol. 148, 850–861 (2008)

    Article  ADS  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  34. Zanne, A. E. et al. Data from: Towards a worldwide wood economics spectrum. Dryad Digital Repository. http://dx.doi.org/10.5061/dryad.234 (2009)

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

    Article  ADS  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

  38. Metcalfe, D. B. 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)

    Article  CAS  Google Scholar 

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

    Article  ADS  Google Scholar 

  40. 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  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  43. Pinheiro, J. C. & Bates, D. M. Mixed-Effects Models in S and S-PLUS (Springer, 2000)

  44. Fisher, R. A., Williams, M., Do Vale, R. L., Da Costa, A. L. & Meir, P. Evidence from Amazonian forests is consistent with isohydric control of leaf water potential. Plant Cell Environ. 29, 151–165 (2006)

    Article  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgements

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

Authors and Affiliations

  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, Cerdanyola del Vallés, 08193, Spain

    M. Mencuccini

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

    P. Meir

Authors
  1. L. Rowland
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. C. L. da Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. R. Galbraith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. S. Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. O. J. Binks
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. A. R. Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. M. Pullen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. C. E. Doughty
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. D. B. Metcalfe
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. S. S. Vasconcelos
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. L. V. Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Y. Malhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. J. Grace
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. M. Mencuccini
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. P. Meir
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to L. Rowland.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Leaf area index change.

Leaf area index (LAI; ratio of leaf area to ground area) for the period of 2001–2014 on the control (black, solid) and TFE (grey, dashed) plots. Error bars show the s.e.m. associated with LAI calculation, which is derived from n = 25 photos per control and TFE plot (see Methods).

Extended Data Figure 2 Seasonal soil water potential.

Average soil water potential (−MPa) in the control and TFE during dry season (July–December, control n = 34 months, TFE n = 40 months) and wet season (January–June control n = 34 months, TFE n = 40 months), calculated form monthly average volumetric soil moisture content data, collected from 2008–2014, using sensors installed 0, 0.5, 1, 2.5 and 4 m below the surface and the necessary van Genuchten parameters previously calculated from soil hydraulics measurements at this site (see Methods). Error bars show s.e.m.

Extended Data Figure 3 Leaf herbivory comparison.

Average percentage loss of leaf area from herbivore attack calculated from leaves collected in litter-traps on the control (n = 3,297) and TFE plot (n = 3,824) from 2010–2014. Error bars show s.e.m and no significant differences were found significant with a P < 0.05 using the Wilcoxon test. A separate analysis of herbivore attack on 13,694 top-canopy living leaves from branches of the 41 trees used for the P50 analysis support these results, also showing no significant differences in percentage herbivory between the control and the TFE (data not shown).

Extended Data Figure 4 Diurnal patterns of Ψl.

Diurnal Ψl measured every 2 h from 6:00 until 18:00 in dry season on trees accessible from the walk up tower. Each box shows the diurnal Ψl against diurnal air vapour pressure deficit (VPD) from one of seven trees accessible on the control (C), or one of four trees accessible on the TFE. Note that a majority of trees demonstrate an inversely correlated (negative) relationship with VPD. Combined separately for each plot, a significant negative linear relationship is observed between Ψl and VPD on the control (R2 = 0.18, P = 0.002) and even more strongly on the TFE (R2 = 0.33, P = 0.001).

Extended Data Table 1 NSC and P50 sample trees
Full size table
Extended Data Table 2 Analysis of the effect of tree dbh on xylem P50
Full size table
Extended Data Table 3 Individual tree mortality by genus
Full size table

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rowland, L., da Costa, A., Galbraith, D. et al. Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature 528, 119–122 (2015). https://doi.org/10.1038/nature15539

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature15539

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced 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