In 2005 and 2010 the Amazon basin experienced two strong droughts1, driven by shifts in the tropical hydrological regime2 possibly associated with global climate change3, as predicted by some global models3. Tree mortality increased after the 2005 drought4, and regional atmospheric inversion modelling showed basin-wide decreases in CO2 uptake in 2010 compared with 2011 (ref. 5). But the response of tropical forest carbon cycling to these droughts is not fully understood and there has been no detailed multi-site investigation in situ. Here we use several years of data from a network of thirteen 1-ha forest plots spread throughout South America, where each component of net primary production (NPP), autotrophic respiration and heterotrophic respiration is measured separately, to develop a better mechanistic understanding of the impact of the 2010 drought on the Amazon forest. We find that total NPP remained constant throughout the drought. However, towards the end of the drought, autotrophic respiration, especially in roots and stems, declined significantly compared with measurements in 2009 made in the absence of drought, with extended decreases in autotrophic respiration in the three driest plots. In the year after the drought, total NPP remained constant but the allocation of carbon shifted towards canopy NPP and away from fine-root NPP. Both leaf-level and plot-level measurements indicate that severe drought suppresses photosynthesis. Scaling these measurements to the entire Amazon basin with rainfall data, we estimate that drought suppressed Amazon-wide photosynthesis in 2010 by 0.38 petagrams of carbon (0.23–0.53 petagrams of carbon). Overall, we find that during this drought, instead of reducing total NPP, trees prioritized growth by reducing autotrophic respiration that was unrelated to growth. This suggests that trees decrease investment in tissue maintenance and defence, in line with eco-evolutionary theories that trees are competitively disadvantaged in the absence of growth6. We propose that weakened maintenance and defence investment may, in turn, cause the increase in post-drought tree mortality observed at our plots.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Stand characteristics modulate secondary growth responses to drought and gross primary production in Pinus halepensis afforestation
European Journal of Forest Research Open Access 24 December 2022
Emerging signals of declining forest resilience under climate change
Nature Open Access 13 July 2022
Forest fragmentation impacts the seasonality of Amazonian evergreen canopies
Nature Communications Open Access 17 February 2022
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Get just this article for as long as you need it
Prices may be subject to local taxes which are calculated during checkout
Lewis, S. L., Brando, P. M., Phillips, O. L., van der Heijden, G. M. F. & Nepstad, D. The 2010 Amazon drought. Science 331, 554 (2011)
Gloor, M. et al. Intensification of the Amazon hydrological cycle over the last two decades. Geophys. Res. Lett. 40, 1729–1733 (2013)
Solomon, S. et al. (eds) Climate Change 2007: The Physical Science Basis (Cambridge Univ. Press, 2007)
Phillips, O. L. et al. Drought sensitivity of the Amazon rainforest. Science 323, 1344–1347 (2009)
Gatti, L. V. et al. Drought sensitivity of Amazonian carbon balance revealed by atmospheric measurements. Nature 506, 76–80 (2014)
Franklin, O. et al. Modeling carbon allocation in trees: a search for principles. Tree Physiol. 32, 648–666 (2012)
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)
Nepstad, D. C. et al. The effects of partial throughfall exclusion on canopy processes, aboveground production, and biogeochemistry of an Amazon forest. J. Geophys. Res. 107 (D20). 8085 (2002)
Xu, L. A. et al. Widespread decline in greenness of Amazonian vegetation due to the 2010 drought. Geophys. Res. Lett. 38, L07402 (2011)
Saatchi, S. et al. Persistent effects of a severe drought on Amazonian forest canopy. Proc. Natl Acad. Sci. USA 110, 565–570 (2013)
Saleska, S. R., Didan, K., Huete, A. R. & da Rocha, H. R. Amazon forests green-up during 2005 drought. Science 318, 612 (2007)
Phillips, O. L. et al. Changes in the carbon balance of tropical forests: evidence from long-term plots. Science 282, 439–442 (1998)
Meir, P., Metcalfe, D. B., Costa, A. C. L. & Fisher, R. A. The fate of assimilated carbon during drought: impacts on respiration in Amazon rainforests. Phil. Trans. R. Soc. B 363, 1849–1855 (2008)
Townsend, A. R., Asner, G. P., White, J. W. C. & Tans, P. P. Land use effects on atmospheric C-13 imply a sizable terrestrial CO2 sink in tropical latitudes. Geophys. Res. Lett. 29, 1426 (2002)
Malhi, Y., Doughty, C. & Galbraith, D. The allocation of ecosystem net primary productivity in tropical forests. Phil. Trans. R. Soc. B 366, 3225–3245 (2011)
Wurth, M. K. R., Pelaez-Riedl, S., Wright, S. J. & Korner, C. Non-structural carbohydrate pools in a tropical forest. Oecologia 143, 11–24 (2005)
Dietze, M. C. et al. Nonstructural carbon in woody plants. Annu. Rev. Plant Biol. 65, 667–687 (2014)
Sala, A., Woodruff, D. R. & Meinzer, F. C. Carbon dynamics in trees: feast or famine? Tree Physiol. 32, 764–775 (2012)
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)
Araujo-Murakami, A. et al. The productivity, allocation and cycling of carbon in forests at the dry margin of the Amazon forest in Bolivia. Plant Ecol. Divers. 7, 55–69 (2014)
Doughty, C. E. et al. The production, allocation and cycling of carbon in a forest on fertile terra preta soil in eastern Amazonia compared with a forest on adjacent infertile soil. Plant Ecol. Divers. 7, 41–53 (2014)
Malhi, Y. et al. The productivity, metabolism and carbon cycle of two lowland tropical forest plots in south-western Amazonia, Peru. Plant Ecol. Divers. 7, 85–105 (2014)
Rocha, W. et al. Ecosystem productivity and carbon cycling in intact and annually burnt forest at the dry southern limit of the Amazon rainforest (Mato Grosso, Brazil). Plant Ecol. Divers. 7, 25–40 (2014)
Fenn, K., Malhi, Y., Morecroft, M., Lloyd, C. & Thomas, M. The carbon cycle of a maritime ancient temperate broadleaved woodland at seasonal and annual scales. Ecosystems http://dx.doi.org/10.1007/s10021-014-9793-1 (13 December 2014)
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. Change Biol. 13, 2361–2378 (2007)
Doughty, C. E. et al. Allocation trade-offs dominate the response of tropical forest growth to seasonal and interannual drought. Ecology 95, 2192–2201 (2014)
Lewis, S. L. et al. Concerted changes in tropical forest structure and dynamics: evidence from 50 South American long-term plots. Phil. Trans. R. Soc. B 359, 421–436 (2004)
King, D. A. A model analysis of the influence of root and foliage allocation on forest production and competition between trees. Tree Physiol. 12, 119–135 (1993)
Hikosaka, K. & Anten, N. P. R. An evolutionary game of leaf dynamics and its consequences for canopy structure. Funct. Ecol. 26, 1024–1032 (2012)
McDowell, N. G. et al. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol. Evol. 26, 523–532 (2011)
Doughty, C. E. & Goulden, M. L. Seasonal patterns of tropical forest leaf area index and CO2 exchange. J. Geophys. Res. 113, G00b06 (2008)
Girardin, C. A. J. et al. Productivity and carbon allocation in a tropical montane cloud forest in the Peruvian Andes. Plant Ecol. Divers. 7, 107–123 (2014)
Huasco, W. H. et al. Seasonal production, allocation and cycling of carbon in two mid-elevation tropical montane forest plots in the Peruvian Andes. Plant Ecol. Divers. 7, 125–142 (2014)
Quesada, C. A. et al. Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9, 2203–2246 (2012)
Lopez-Gonzalez, G., Lewis, S. L., Burkitt, M. & Phillips, O. L. ForestPlots.net: a web application and research tool to manage and analyse tropical forest plot data. J. Veg. Sci. 22, 610–613 (2011)
Feldpausch, T. R. et al. Tree height integrated into pantropical forest biomass estimates. Biogeosciences 9, 3381–3403 (2012)
Quesada, C. A. et al. Soils of Amazonia with particular reference to the RAINFOR sites. Biogeosciences 8, 1415–1440 (2011)
Lehmann, J., Kern, D. C., Glaser, B. & Woods, W. I. Amazonian Dark Earths: Origin, Properties, Management (Kluwer Academic, 2003)
Malhi, Y. et al. The linkages between photosynthesis, productivity, growth and biomass in lowland Amazonian forests. Global Change Biol. http://dx.doi.org/10.1111/gcb.12859 (10 January 2015)
Malhi, Y. et al. Exploring the likelihood and mechanism of a climate-change-induced dieback of the Amazon rainforest. Proc. Natl Acad. Sci. USA 106, 20610–20615 (2009)
Doughty, C. E. An in situ leaf and branch warming experiment in the Amazon. Biotropica 43, 658–665 (2011)
da Rocha, H. R. et al. Seasonality of water and heat fluxes over a tropical forest in eastern Amazonia. Ecol. Appl. 14, S22–S32 (2004)
Brando, P. M. et al. Abrupt increases in Amazonian tree mortality due to drought–fire interactions. Proc. Natl Acad. Sci. USA 111, 6347–6352 (2014)
Chave, J. et al. Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia 145, 87–99 (2005)
Martin, A. R. & Thomas, S. C. A reassessment of carbon content in tropical trees. PLoS ONE 6, e23533 (2011)
Metcalfe, D. B. et al. Factors controlling spatio-temporal variation in carbon dioxide efflux from surface litter, roots, and soil organic matter at four rain forest sites in the eastern Amazon. J. Geophys. Res. 112, G04001 (2007)
Malhi, Y. et al. Comprehensive assessment of carbon productivity, allocation and storage in three Amazonian forests. Global Change Biol. 15, 1255–1274 (2009)
Chambers, J. Q. et al. Respiration from a tropical forest ecosystem: Partitioning of sources and low carbon use efficiency. Ecol. Appl. 14, S72–S88 (2004)
We thank P. Brando and Tanguro partners for logistical support and advice. This work is a product of the Global Ecosystems Monitoring (GEM) network (http://gem.tropicalforests.ox.ac.uk) and the RAINFOR and ABERG research consortia, and was funded by grants to Y.M. and O.L.P. from the Gordon and Betty Moore Foundation to the Amazon Forest Inventory Network (RAINFOR) and the Andes Biodiversity and Ecosystems Research Group (ABERG), and grants from the UK Natural Environment Research Council (NE/D01025X/1, NE/D014174/1, NE/F002149/1 and NE/J011002/1), the NERC AMAZONICA consortium grant (NE/F005776/1) and the EU FP7 Amazalert (282664) GEOCARBON (283080) projects. Some data in this publication were provided by the Tropical Ecology Assessment and Monitoring (TEAM) Network, a collaboration between Conservation International, the Missouri Botanical Garden, the Smithsonian Institution and the Wildlife Conservation Society, and partly funded by these institutions, the Gordon and Betty Moore Foundation, and other donors. T.R.F. is supported by a National Council for Scientific and Technological Development (CNPq, Brazil) award. P.M. is supported by an ARC fellowship award FT110100457; O.L.P. is supported by an ERC Advanced Investigator Award and a Royal Society Wolfson Research Merit Award; Y.M. is supported by an ERC Advanced Investigator Award and by the Jackson Foundation. C.E.D. acknowledges funding from the John Fell Fund.
The authors declare no competing financial interests.
Extended data figures and tables
Extended Data Figure 1 Comparison of plot-based and flux-based estimates of gross primary productivity (GPP) at six different sites worldwide.
The black line represents 1:1; the dashed line represents a linear fit with a y intercept of 0. Slope = 0.97 ± 0.04, coefficient of determination = 0.61. If the Caxiuanã tower site is removed, then slope = 1.01 ± 0.03 and coefficient of determination = 0.87. Data points are from Manaus, Tapajos, Caxiuanã (Brazil), Wytham Woods (UK) and Lambir Hills (Malaysia). For further details see ref. 39.
Extended Data Figure 2 Climate data for the plots.
a, Cumulative water deficit (CWD) anomaly for six droughted plots (red) and the remaining seven non-droughted plots (black) in 2010, on the basis of data from Skye instruments meteorological stations near each plot. Meteorology stations were set up in either ∼2005 (n = 4) or ∼2009 (n = 4). b, MCWD anomaly for 2010 (the minimum of CWDmean minus CWD2010) for the entire Amazon basin based on TRMM version 7 data (1998–2012). For clarity we do not show MCWD for non-droughted sites for which MCWDanom = 0; this is the maximum potential value because by definition the wettest average month has a CWD value of 0). The arrows depict the site-specific MCWD anomaly for each drought area and average for all drought plots. c, e, Data from Skye instruments meteorological stations from January 2009 to December 2011 near our drought plots for cumulative water deficit (mm per month) (c) and air temperature (°C) (e). d, f, Anomalies for the same variables (mean values are average of all data from ∼2005, ∼2009–2011 or ∼2009–2012). The drought period in our drought sites had a slightly lower average temperature during the drought than during the equivalent months of 2009 (24.6 °C versus 24.7 °C). The bar highlights the approximate period of the 2010 drought in the region based on CWD anomaly. To calculate CWD see ref. 40. Error bars are standard error differences between plots.
Extended Data Figure 3 Leaf-level light-saturated photosynthesis measurements.
Top: light-saturated (1,000 μmol m−2 s−1 irradiance, 25 °C, ambient CO2) leaf gas exchange (μmol m−2 s−1) (means ± s.e.m.) for a drought period (November 2010) and a non-drought period (June 2011) for sunlit branches (cut and rehydrated) on the same ∼20 trees each season distributed evenly through the two (Kenia-A and Kenia-B) 1-ha plots. Asterisks indicate significant differences between the plots: P < 0.05; P < 0.001. Bottom: weekly averaged leaf-level photosynthesis for eight species from three canopy walk-up towers measured at 1,000 μmol m−2 s−1 light and 30 °C between July (the start of the dry season) and November from the Tapajós, Brazil (see ref. 41 for further details and methodology). In the Tapajós the average dry season lasts from about July to about November. Note the lack of a decrease in photosynthesis during the dry season. Over this period, soil moisture decreases from ∼0.45 to 0.40 m3 m−3, most of the decrease that occurs during the dry season42. These data suggest that a large (that is, 50%) sharp decline in leaf-level photosynthesis is not typical during an average dry season and that the declines shown in the table above are probably due to the 2010 drought.
Extended Data Figure 4 A conceptual model with simulated data of the impact of drought on the study sites.
Total photosynthesis (grey dashed line; 100% represents average photosynthesis) decreased during the drought period (vertical bar). Total NPP (grey line, shown as a percentage of total photosynthesis) and growth respiration (Rgrowth) (black dotted line) remained constant, whereas maintenance respiration (Rmaintain) (black line) decreased after NSC stores were depleted. Total NSC stores decreased (we define a negative value as NSC storage) during the drought period (the red line indicates a NSC storage of 0) and then increased at the end of the drought. Red arrows represent the timing of when the basin was a source (up) or a sink (down) of CO2 to the atmosphere based on atmospheric inversion measurements from ref. 5.
Extended Data Figure 5 Impact of drought on carbon allocation for individual plots.
This figure shows similar trends to those in Fig. 2, but with all the plots separated and extended for a further year for Tambopata and Kenia. a–d, Four years of total NPP (Mg C ha−1 per month) (a), percentage allocation to canopy (b), percentage allocation to wood (c) and percentage allocation to fine roots (d) for the two plots in Kenia, Bolivia (black line, Kenia-A; grey line, Kenia-B). e–h, Seasonally detrended anomaly data for the same variables. This data set is explored in detail in ref. 26. i, j, Comparison of four years of wood (i) and root (j) allocation data for two plots in Tambopata, Peru (black lines). Canopy NPP is not shown because LAI data were not processed for the entire 4-year period. k, Three years of woody (brown), fine-root (black) and canopy (red) allocation data for two plots in Tanguro, Brazil (solid line, Tanguro A; dashed line, Tanguro C ). The bar indicates the approximate drought period.
Extended Data Figure 6 Deadwood respiration, branch fall and tree mortality.
a, Respiration from deadwood over a 4-year period from Kenia-A (grey) and Kenia-B (black). b, Branch fall over a 4-year period from Kenia-A (grey) and Kenia-B (black); smoothed values are shown in bold lines; actual values are shown in dashed lines. c, Per-stem mortality rates for Peruvian drought plots (grey line, n = 3; error bars indicate standard errors), Bolivian drought plots (black line, n = 2) and the control plot in Caxiuanã (red line, n = 1). We do not show mortality for the Brazilian drought plots, but a recent paper43 has shown an increase in mortality after drought at these sites. Mortality was marginally significantly higher (P = 0.06; paired 1-tailed t-test, n = 5) during the 2-year period after the drought than in other periods. The bar indicates the approximate period of the drought.
Extended Data Figure 7 Separated components of PCE.
Total PCE (grey solid line), wood and rhizosphere respiration (black solid line), and canopy respiration (red solid line) for the six droughted plots and smoothed 2009 equivalents (stippled lines). This figure shows that the decline in Ra was due to the components measured monthly (wood and rhizosphere respiration) and not to canopy respiration (which was measured only once or twice a year). This does not mean that canopy respiration did not decrease during the drought, only that we did not track canopy respiration sufficiently to measure changes. The bar indicates the approximate period of the drought.
Supplementary Data 1
This file contains the data for drought conditions. (XLSX 57 kb)
Supplementary Data 2
This file contains the data for non-drought conditions. (XLSX 50 kb)
Rights and permissions
About this article
Cite this article
Doughty, C., Metcalfe, D., Girardin, C. et al. Drought impact on forest carbon dynamics and fluxes in Amazonia. Nature 519, 78–82 (2015). https://doi.org/10.1038/nature14213
This article is cited by
Heat and drought impact on carbon exchange in an age-sequence of temperate pine forests
Ecological Processes (2022)
Emerging signals of declining forest resilience under climate change
Forest fragmentation impacts the seasonality of Amazonian evergreen canopies
Nature Communications (2022)
Does asymmetric birch effect phenomenon matter for environmental sustainability of agriculture in Tunisia?
Environment, Development and Sustainability (2022)
Terrestrial carbon sinks in China and around the world and their contribution to carbon neutrality
Science China Life Sciences (2022)
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.