Abstract
Evidence suggests that 5–15% of the vast pool of soil carbon stored in northern permafrost ecosystems could be emitted as greenhouse gases by 2100 under the current path of global warming. However, direct measurements of changes in soil carbon remain scarce, largely because ground subsidence that occurs as the permafrost soils begin to thaw confounds the traditional quantification of carbon pools based on fixed depths or soil horizons. This issue is overcome when carbon is quantified in relation to a fixed ash content, which uses the relatively stable mineral component of soil as a metric for pool comparisons through time. We applied this approach to directly measure soil carbon pool changes over five years in experimentally warmed and ambient tundra ecosystems at a site in Alaska where permafrost is degrading due to climate change. We show a loss of soil carbon of 5.4% per year (95% confidence interval: 1.0, 9.5) across the site. Our results point to lateral hydrological export as a potential pathway for these surprisingly large losses. This research highlights the potential to make repeat soil carbon pool measurements at sentinel sites across the permafrost region, as this feedback to climate change may be occurring faster than previously thought.
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Data availability
All the data and metadata associated with this manuscript are deposited in the Long Term Ecological Research (LTER) Network Information System Data Portal at https://portal.lternet.edu/nis/home.jsp (https://doi.org/10.6073/pasta/894ec9847bc365347775d3aaba44a50210.6073/pasta/894ec9847bc365347775d3aaba44a502, https://doi.org/10.6073/pasta/f502d8fe1a2e1d6c6b035c198af04f3e and https://doi.org/10.6073/pasta/b559d2650efe99ccabb2a58d9d8819ab).
References
Schuur, E. A. G. et al. Climate change and the permafrost carbon feedback. Nature 520, 171–179 (2015).
Hugelius, G. et al. Estimated stocks of circumpolar permafrost carbon with quantified uncertainty ranges and identified data gaps. Biogeosciences 11, 6573–6593 (2014).
Ping, C. L., Jastrow, J. D., Jorgenson, M. T., Michaelson, G. J. & Shur, Y. L. Permafrost soils and carbon cycling. Soil 1, 147–171 (2015).
Schaefer, K., Lantuit, H., Romanovsky, V. E., Schuur, E. A. G. & Witt, R. The impact of the permafrost carbon feedback on global climate. Environ. Res. Lett. 9, 085003 (2014).
Elberling, B. et al. Long-term CO2 production following permafrost thaw. Nat. Clim. Change 3, 890–894 (2013).
Sistla, S. A. et al. Long-term warming restructures Arctic tundra without changing net soil carbon storage. Nature 497, 615–618 (2013).
Mack, M. C., Schuur, E. A. G., Bret-Harte, M. S., Shaver, G. R. & Chapin, F. S. III Ecosystem carbon storage in Arctic tundra reduced by long-term nutrient fertilization. Nature 431, 440–443 (2003).
Strauss, J. et al. The deep permafrost carbon pool of the Yedoma region in Siberia and Alaska. Geophys. Res. Lett. 40, 6165–6170 (2013).
Jorgenson, M. T. & Osterkamp, T. E. Response of boreal ecosystems to varying modes of permafrost degradation. Can. J. For. Res. 35, 2100–2111 (2005).
Grønlund, A., Hauge, A., Hovde, A. & Rasse, D. P. Carbon loss estimates from cultivated peat soils in Norway: a comparison of three methods. Nutr. Cycl. Agroecosys. 81, 157–167 (2008).
Rogiers, N., Conen, F., Furger, M., Stöckli, R. & Eugster, W. Impact of past and present land-management on the C-balance of a grassland in the Swiss Alps. Glob. Change Biol. 14, 2613–2625 (2008).
Natali, S. M., Schuur, E. A. G., Webb, E. E., Hicks Pries, C. E. & Crummer, K. G. Permafrost degradation stimulates carbon loss from experimentally warmed tundra. Ecology 95, 602–608 (2014).
Schuur, E. A. G. et al. The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459, 556–559 (2009).
Romanovsky, W. E. et al. Permafrost. Arctic Report Card http://www.arctic.noaa.gov/reportcard (2012).
Osterkamp, T. E. Characteristics of the recent warming of permafrost in Alaska. J. Geophys. Res. 112, F02S02 (2007).
Jones, M. C. et al. Rapid carbon loss and slow recovery following permafrost thaw in boreal peatlands. Glob. Change Biol. 23, 1109–1127 (2017).
Shaver, G. R. et al. Global warming and terrestrial ecosystems: a conceptual framework for analysis. Bioscience 50, 871–882 (2000).
Salmon, V. G. et al. Nitrogen availability increases in a tundra ecosystem during five years of experimental permafrost thaw. Glob. Change Biol. 22, 1927–1941 (2016).
Schmidt, M. W. I. et al. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56 (2011).
Lehmann, J. & Kleber, M. The contentious nature of soil organic matter. Nature 528, 60–68 (2015).
Baldock, J. A. & Skjemstad, J. O. Role of the soil matrix and minerals in protecting natural organic materials against biological attack. Org. Geochem. 31, 697–710 (2000).
Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).
Webb, E. E. et al. Increased wintertime CO2 loss as a result of sustained tundra warming. J. Geophys. Res. Biogeosci. 121, 249–265 (2016).
Schädel, C. et al. Potential carbon emissions dominated by carbon dioxide from thawed permafrost soils. Nat. Clim. Change 6, 950–953 (2016).
Olefeldt, D., Turetsky, M. R., Crill, P. M. & McGuire, A. D. Environmental and physical controls on northern terrestrial methane emissions across permafrost zones. Glob. Change Biol. 19, 589–603 (2013).
Vonk, J. E. & Gustafsson, O. Permafrost–carbon complexities. Nat. Geosci. 2, 598–600 (2013).
Zhu, Z. & McGuire, A. D. Baseline and Projected Future Carbon Storage and Greenhouse-Gas Fluxes in Ecosystems of Alaska Professional Paper 1826 (USGS, 2016).
Abbott, B. W. & Jones, J. B. Permafrost collapse alters soil carbon stocks, respiration, CH4, and N2O in upland tundra. Glob. Change Biol. 21, 4570–4587 (2015).
Zhang, X. et al. Importance of lateral flux and its percolation depth on organic carbon export in Arctic tundra soil: implications from a soil leaching experiment. J. Geophys. Res. 122, 796–810 (2017).
Tarnocai, C. et al. Soil organic carbon pools in the northern circumpolar permafrost region. Glob. Biogeochem. Cycl. 23, GB2023 (2009).
McGuire, A. D. et al. An assessment of the carbon balance of Arctic tundra: comparisons among observations, process models, and atmospheric inversions. Biogeosciences 9, 3185–3204 (2012).
Soil Survey Staff Keys to Soil Taxonomy (USDA–NRCS, 2014).
Natali, S. et al. Effects of experimental warming of air, soil and permafrost on carbon balance in Alaskan tundra. Glob. Change Biol. 17, 1394–1407 (2011).
Natali, S., Schuur, E. & Rubin, R. Increased plant productivity in Alaskan tundra as a result of experimental warming of soil and permafrost. J. Ecol. 100, 488–498 (2012).
Mauritz, M. et al. Nonlinear CO2 flux response to 7 years of experimentally induced permafrost thaw. Glob. Change Biol. 23, 3646–3666 (2017).
Crowther, T. W. et al. Quantifying global soil carbon losses in response to warming. Nature 540, 104–108 (2016).
Hicks Pries, C. E., Schuur, E. A. G. & Crummer, K. G. Holocene carbon stocks and carbon accumulation rates altered in soils undergoing permafrost thaw. Ecosystems 15, 162–173 (2012).
Schumacher, B. A. Methods for the Determination of Total Organic Carbon (TOC) in Soils and Sediments EPA/600/R-02/069 (US EPA, 2002).
Ellert, B. H., Janzen, H. H., VandenBygaart, A. G. & Bremer, E., in Soil Sampling and Methods of Analysis (eds Carter, M. R. & Gregorich, E. G.) 25–38 (CRC Press, 2007).
Lee, J., Hopmans, J. W., Rolston, D. E., Baer, S. G. & Six, J. Determining soil carbon stock changes: simple bulk density corrections fail. Agric. Ecosyst. Environ. 134, 251–256 (2009).
McBratney, A. B. & Minasny, B. Comment on “Determining soil carbon stock changes: simple bulk density corrections fail”. Agric. Ecosyst. Environ. 136, 185–186 (2010).
IUSS Working Group WRB World Reference Base for Soil Resources 2014 (FAO, 2014).
Kaiser, C. et al. Conservation of soil organic matter through cryoturbation in Arctic soils in Siberia. J. Geophys. Res. 112, G02017 (2007).
Baldock, J. A. & Smernik, R. J. Chemical composition and bioavailability of thermally altered Pinus resinosa (Red pine) wood. Org. Geochem. 33, 1093–1109 (2002).
Simpson, A. J. & Simpson, M. J. in Biophysico-Chemical Processes Involving Natural Nonliving Organic Matter in Environmental Systems (eds Senesi, N., Xing, B. & Huang, P. M.) 589–651 (John Wiley & Sons, 2009).
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009).
Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002).
Ku, H. H. Notes on the use of propagation of error formulas. J. Res. Natl Bur. Stand. C 70C, 263–273 (1966).
R Core Team. R: A language and environment for statistical computing https://d.R-project.org (2015).
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest: Tests in Linear Mixed Effects Models https://CRAN.R-project.org/package=lmerTest (2016).
Barton, K. MuMIn: Multi-Model inference https://CRAN.R-project.org/package=MuMIn (2016).
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).
Wilke, C. O. cowplot: Streamlined Plot Theme and Plot Annotations for ‘ggplot2’ https://CRAN.R-project.org/package=cowplot (2016).
Acknowledgements
This work was based in part on support provided by the following programs: US Department of Energy, Office of Biological and Environmental Research, Terrestrial Ecosystem Science (TES) Program, Award nos DE-SC0006982 and DE-SC0014085; National Science Foundation CAREER program, Award no. 0747195; National Parks Inventory and Monitoring Program; National Science Foundation Bonanza Creek LTER program, Award no. 1026415 and National Science Foundation Office of Polar Programs, Award no. 1203777. In addition, this project received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska Curie grant agreement 654132. We thank L. Barrios (CSIC) and the NAU statistical consulting lab for assistance with the data analysis.
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E.A.G.S. conceived and designed the study. E.A.G.S. and S.M.N. implemented the field experiment. R.B., G.C., K.G.C., J.A.H., M.M., S.M.N., C.P., C.E.H.P., E.P., C.S., E.A.G.S., V.G.S. and E.E.W. performed the field research and/or data analysis. K.G.C., J.A.H., C.P., E.P., M.M., S.M.N. and V.G.S. conducted the laboratory research. C.P., G.C. and M.M. carried out data analyses. C.P., E.A.G.S. and E.P. wrote the article. All authors substantially discussed the results and contributed to editing the manuscript.
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Plaza, C., Pegoraro, E., Bracho, R. et al. Direct observation of permafrost degradation and rapid soil carbon loss in tundra. Nat. Geosci. 12, 627–631 (2019). https://doi.org/10.1038/s41561-019-0387-6
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DOI: https://doi.org/10.1038/s41561-019-0387-6
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