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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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)
Mora, C. et al. The projected timing of climate departure from recent variability. Nature 502, 183–187 (2013)
Reichstein, M. et al. Climate extremes and the carbon cycle. Nature 500, 287–295 (2013)
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)
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)
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)
Doughty, C. E. et al. Drought impact on forest carbon dynamics and fluxes in Amazonia. Nature 519, 78–82 (2015)
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)
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)
Phillips, O. L. et al. Drought sensitivity of the Amazon rainforest. Science 323, 1344–1347 (2009)
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)
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)
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)
McDowell, N. G. et al. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol. Evol. 26, 523–532 (2011)
Thomas, H. Senescence, ageing and death of the whole plant. New Phytol. 197, 696–711 (2013)
Meir, P., Mencuccini, M. & Dewar, R. C. Drought-related tree mortality: addressing the gaps in understanding and prediction. New Phytol. 207, 28–33 (2015)
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)
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)
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)
Choat, B. et al. Global convergence in the vulnerability of forests to drought. Nature 491, 752–755 (2012)
Sala, A., Woodruff, D. R. & Meinzer, F. C. Carbon dynamics in trees: feast or famine? Tree Physiol. 32, 764–775 (2012)
Körner, C. Carbon limitation in trees. J. Ecol. 91, 4–17 (2003)
Mencuccini, M. et al. Size-mediated ageing reduces vigour in trees. Ecol. Lett. 8, 1183–1190 (2005)
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)
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)
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)
Fatichi, S., Leuzinger, S. & Körner, C. Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol. 201, 1086–1095 (2014)
Leuzinger, S. et al. Do global change experiments overestimate impacts on terrestrial ecosystems? Trends Ecol. Evol. 26, 236–241 (2011)
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)
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)
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)
Chave, J. et al. Improved allometric models to estimate the aboveground biomass of tropical trees. Glob. Chang. Biol. 20, 3177–3190 (2014)
Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009)
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)
Patiño, S. et al. Branch xylem density variations across the Amazon Basin. Biogeosciences 6, 545–568 (2009)
Chave, J. et al. Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia 145, 87–99 (2005)
Feldpausch, T. R. et al. Tree height integrated into pantropical forest biomass estimates. Biogeosciences 9, 3381–3403 (2012)
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)
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)
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)
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)
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)
Pinheiro, J. C. & Bates, D. M. Mixed-Effects Models in S and S-PLUS (Springer, 2000)
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)
Metcalfe, D. B. et al. Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecol. Lett. 17, 324–332 (2014)
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.
The authors declare no competing financial interests.
Extended data figures and tables
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).
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.
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).
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).
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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
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