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

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.

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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).

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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.

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Authors

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.

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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
Extended Data Table 2 Analysis of the effect of tree dbh on xylem P50
Extended Data Table 3 Individual tree mortality by genus

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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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