Tropical soils contain one-third of the carbon stored in soils globally1, so destabilization of soil organic matter caused by the warming predicted for tropical regions this century2 could accelerate climate change by releasing additional carbon dioxide (CO2) to the atmosphere3,4,5,6. Theory predicts that warming should cause only modest carbon loss from tropical soils relative to those at higher latitudes5,7, but there have been no warming experiments in tropical forests to test this8. Here we show that in situ experimental warming of a lowland tropical forest soil on Barro Colorado Island, Panama, caused an unexpectedly large increase in soil CO2 emissions. Two years of warming of the whole soil profile by four degrees Celsius increased CO2 emissions by 55 per cent compared to soils at ambient temperature. The additional CO2 originated from heterotrophic rather than autotrophic sources, and equated to a loss of 8.2 ± 4.2 (one standard error) tonnes of carbon per hectare per year from the breakdown of soil organic matter. During this time, we detected no acclimation of respiration rates, no thermal compensation or change in the temperature sensitivity of enzyme activities, and no change in microbial carbon-use efficiency. These results demonstrate that soil carbon in tropical forests is highly sensitive to warming, creating a potentially substantial positive feedback to climate change.
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This study was supported by two fellowships to A.T.N., a European Union Marie-Curie Fellowship FP7-2012-329360 (University of Edinburgh) and a Tupper Fellowship (Smithsonian Tropical Research Institute); a Smithsonian Institution Scholarly Studies Grant to B.L.T. and K. Winter; a UK NERC grant NE/K01627X/1 and an ANU Biology Innovation grant to P.M. We thank O. Acevado, D. Agudo, A. Bielnicka, M. Cano, D. Dominguez, M. Garcia, M. Larsen, B. Martin, M. Montero, S. O’Connor, J. Rodriguez, H. Szczygiel, I. Torres, W. Wcislo, K. Winter and S. J. Wright for their contributions to SWELTR.
The authors declare no competing interests.
Peer review information Nature thanks Eric Davidson and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Extended data figures and tables
a–d, Pictures (a, b) and thermal images (c, d) of a warmed plot. The thermal images show the soil-surface temperature 1 h after the warming structure was switched on (c) and after a period of thermal equilibration of soil (d). The circular heating structure was 3.5 m in diameter and extended to 1.2 m depth, which resulted in an effective heated plot of approximately 5 m diameter and 1.2 m depth. The experiment consisted of five warmed and control plot pairs in total. Image credit: J. Bujan and E.V.
a, b, Soil volumetric moisture content (a) and soil temperature (b), for the period after the warming treatment began (December 2016 to December 2018), partitioned by soil depth (columns) and season (rows). Box plots are standard (Tukey) plots, where the centre line represents the median across the five plots over the study period, the lower and upper hinges represent the first and third quartiles, and whiskers represent + 1.5 the interquartile range. c, d, Temporal patterns in soil volumetric moisture content (c) and soil temperature (d), relative to when the warming treatment began (relative day 0; temperature temporarily increased in warmed plots before this during the testing phase). The points are daily means of soil profile and the error bars represent one standard error of the variation by plot (n = 5). The box (Tukey) plots show the median temporal value over sequential 100-day periods. The shaded areas represent dry seasons (1 January to 1 April). Treatment effects on annual or seasonal soil-profile moisture content were not significant; treatment effects on soil temperature were significant (repeated-measures ANOVA, P < 0.001; Extended Data Table 4).
Extended Data Fig. 3 Relationship between soil CO2 efflux, soil moisture and season, in control and warmed plots.
a, b, Relationship between soil CO2 efflux and soil moisture in warmed (red) and control (blue) plots during the dry (a) and wet (b) seasons. Data were fitted (solid lines) using a quadratic function. c, d, Soil CO2 efflux differences between warmed (red) and control (blue) plots during the dry (c) and wet (d) seasons. Soil CO2 efflux in warmed plots was significantly higher than controls for both dry and wet season, although the difference was greater for the wet season (average difference of 2.8 μmol CO2 m−2 s−1 for the wet season compared to 2.1 μmol CO2 m−2 s−1 for the dry season).
a, b, Data for root-derived (a) and soil-derived (b) sources are for the study period. The error bars for points represent one standard error of the variation across the five plots. The box (Tukey) plots show the median temporal value over 100-day periods. The dotted vertical line is when installation and testing of warming plots began; the dashed vertical line shows when all five warming plots were switched on permanently. The shaded areas represent dry seasons (1 January to 1 April).
a–c, Data are for the study period December 2016 to December 2018. Data are partitioned into annual (a), dry-season (b) and wet-season (c) responses. Soil properties are microbial CUE (ratio, no units), soil-extractable nutrients (NH4, NO3, resin P; mg kg–1), dissolved organic carbon (DOC; mg kg–1), microbial elements (mic C, mic N, mic P; mg kg–1) and activities (Vmax) of extracellular enzymes β-glucosidase (BG-ase), phosphomonoesterase (P-ase), N-acetyl β-glucosaminidase (N-ase) and β-xylanase (Xy-ase) (nmol MU g–1 min–1). The temperature sensitivity of activities of extracellular enzymes (Q10 of Vmax) was determined for α-glucosidase (AG-ase), BG-ase, P-ase, N-ase, Xy-ase and cellobiohydrolase (Cel-ase) (nmol MU g–1 min–1). Significant responses (P < 0.05) are highlighted in bold and underlined. The only significant annual response (a) is for microbial carbon (P = 0.02), although there is also a marginal non-significant response for β-xylanase activity (P = 0.07). The centre line of each box plot represents the median across the five plots over the study period, the lower and upper hinges represent the first and third quartiles, and whiskers represent + 1.5 the interquartile range.
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Nottingham, A.T., Meir, P., Velasquez, E. et al. Soil carbon loss by experimental warming in a tropical forest. Nature 584, 234–237 (2020). https://doi.org/10.1038/s41586-020-2566-4
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