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Drought impact on forest carbon dynamics and fluxes in Amazonia

Abstract

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.

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Figure 1: Impact of drought on carbon fluxes.
Figure 2: Impact of drought on carbon allocation.
Figure 3: Estimated impact of drought on the basin-wide flux of CO2.

References

  1. 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)

    ADS  CAS  PubMed  Article  Google Scholar 

  2. Gloor, M. et al. Intensification of the Amazon hydrological cycle over the last two decades. Geophys. Res. Lett. 40, 1729–1733 (2013)

    ADS  Article  Google Scholar 

  3. Solomon, S. et al. (eds) Climate Change 2007: The Physical Science Basis (Cambridge Univ. Press, 2007)

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

    ADS  CAS  PubMed  Article  Google Scholar 

  5. Gatti, L. V. et al. Drought sensitivity of Amazonian carbon balance revealed by atmospheric measurements. Nature 506, 76–80 (2014)

    ADS  CAS  PubMed  Article  Google Scholar 

  6. Franklin, O. et al. Modeling carbon allocation in trees: a search for principles. Tree Physiol. 32, 648–666 (2012)

    CAS  PubMed  Article  Google Scholar 

  7. 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)

    PubMed  Article  Google Scholar 

  8. 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)

    Article  CAS  Google Scholar 

  9. Xu, L. A. et al. Widespread decline in greenness of Amazonian vegetation due to the 2010 drought. Geophys. Res. Lett. 38, L07402 (2011)

    ADS  Article  Google Scholar 

  10. Saatchi, S. et al. Persistent effects of a severe drought on Amazonian forest canopy. Proc. Natl Acad. Sci. USA 110, 565–570 (2013)

    ADS  CAS  PubMed  Article  Google Scholar 

  11. Saleska, S. R., Didan, K., Huete, A. R. & da Rocha, H. R. Amazon forests green-up during 2005 drought. Science 318, 612 (2007)

    ADS  CAS  PubMed  Article  Google Scholar 

  12. Phillips, O. L. et al. Changes in the carbon balance of tropical forests: evidence from long-term plots. Science 282, 439–442 (1998)

    ADS  CAS  PubMed  Article  Google Scholar 

  13. 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)

    CAS  PubMed  Article  Google Scholar 

  14. 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)

    ADS  Article  CAS  Google Scholar 

  15. 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)

    CAS  PubMed  Article  Google Scholar 

  16. 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)

    ADS  PubMed  Article  Google Scholar 

  17. Dietze, M. C. et al. Nonstructural carbon in woody plants. Annu. Rev. Plant Biol. 65, 667–687 (2014)

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  19. 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 

  20. 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)

    Article  Google Scholar 

  21. 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)

    Article  Google Scholar 

  22. 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)

    Article  Google Scholar 

  23. 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)

    Article  Google Scholar 

  24. 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)

  25. 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)

    ADS  Article  Google Scholar 

  26. 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)

    PubMed  Article  Google Scholar 

  27. 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)

    CAS  PubMed  Article  Google Scholar 

  28. 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)

    CAS  PubMed  Article  Google Scholar 

  29. Hikosaka, K. & Anten, N. P. R. An evolutionary game of leaf dynamics and its consequences for canopy structure. Funct. Ecol. 26, 1024–1032 (2012)

    Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  31. Doughty, C. E. & Goulden, M. L. Seasonal patterns of tropical forest leaf area index and CO2 exchange. J. Geophys. Res. 113, G00b06 (2008)

    Google Scholar 

  32. 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)

    Article  Google Scholar 

  33. 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)

    Article  Google Scholar 

  34. 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)

    ADS  Article  Google Scholar 

  35. 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)

    Article  Google Scholar 

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

    ADS  Article  Google Scholar 

  37. Quesada, C. A. et al. Soils of Amazonia with particular reference to the RAINFOR sites. Biogeosciences 8, 1415–1440 (2011)

    ADS  CAS  Article  Google Scholar 

  38. Lehmann, J., Kern, D. C., Glaser, B. & Woods, W. I. Amazonian Dark Earths: Origin, Properties, Management (Kluwer Academic, 2003)

    Book  Google Scholar 

  39. 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)

    ADS  PubMed  Article  Google Scholar 

  40. 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)

    ADS  CAS  PubMed  Article  Google Scholar 

  41. Doughty, C. E. An in situ leaf and branch warming experiment in the Amazon. Biotropica 43, 658–665 (2011)

    Article  Google Scholar 

  42. 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)

    Article  Google Scholar 

  43. 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)

    ADS  CAS  PubMed  Article  Google Scholar 

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

    ADS  CAS  PubMed  Article  Google Scholar 

  45. Martin, A. R. & Thomas, S. C. A reassessment of carbon content in tropical trees. PLoS ONE 6, e23533 (2011)

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. 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)

    Google Scholar 

  47. Malhi, Y. et al. Comprehensive assessment of carbon productivity, allocation and storage in three Amazonian forests. Global Change Biol. 15, 1255–1274 (2009)

    ADS  Article  Google Scholar 

  48. 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)

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Contributions

C.E.D., Y.M. and D.B.M. designed and implemented the study. Y.M. conceived the GEM network, C.E.D., D.B.M., C.A.J.G. and Y.M. implemented it, and O.L.P. contributed to its development. C.E.D. analysed the data. C.E.D., C.A.J.G., F.F.A., D.G., W.H.H., J.E.S., A.A., M.C.C., A.C.L.C., T.F., A.M., W.R. and O.L.P. collected the data. C.E.D. wrote the paper with contributions from Y.M., O.L.P., P.M. and D.B.M.

Corresponding author

Correspondence to Christopher E. Doughty.

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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.

Source data

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.

Source data

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.

Source data

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.

Source data

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. ad, 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). eh, 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.

Source data

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.

Source data

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.

Source data

Extended Data Table 1 Methods for intensive monitoring of net primary production and photosynthesis
Extended Data Table 2 Methods for intensive monitoring of autotrophic and heterotrophic respiration
Extended Data Table 3 Data analysis techniques for intensive study of carbon dynamics

Supplementary information

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)

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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

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