Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

14C evidence that millennial and fast-cycling soil carbon are equally sensitive to warming

Abstract

The Arctic is expected to shift from a sink to a source of atmospheric CO2 this century due to climate-induced increases in soil carbon mineralization1. The magnitude of this effect remains uncertain, largely because temperature sensitivities of organic matter decomposition2,3 and the distribution of these temperature sensitivities across soil carbon pools4 are not well understood. Here, a new analytical method with natural abundance radiocarbon was used to evaluate temperature sensitivities across soil carbon pools. With soils from Utqiaġvik (formerly Barrow), Alaska, an incubation experiment was used to evaluate soil carbon age and decomposability, disentangle the effects of temperature and substrate depletion on carbon mineralization, and compare temperature sensitivities of fast-cycling and slow-cycling carbon. Old, historically stable carbon was shown to be vulnerable to decomposition under warming. Using radiocarbon to differentiate between slow-cycling and fast-cycling carbon, temperature sensitivity was found to be invariant among pools, with a Q10 of ~2 irrespective of native decomposition rate. These findings suggest that mechanisms other than chemical recalcitrance mediate the effect of warming on soil carbon mineralization.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Change over time in CO2 production and \(\mathrm{\Delta}^{14}{\mathrm{C}}_{\mathrm{CO}_2}\) during sequential soil incubations.
Fig. 2: Effects of temperature and incubation time on CO2 production rate.
Fig. 3: Effects of temperature and incubation time on active-pool and passive-pool CO2 production rates.

Similar content being viewed by others

Data availability

All data generated and analysed in this study are archived in the Next-Generation Ecosystem Experiments (NGEE-Arctic) data repository49 and can be accessed at https://doi.org/10.5440/1418852.

References

  1. Koven, C. D. et al. Permafrost carbon-climate feedbacks accelerate global warming. Proc. Natl Acad. Sci. USA 108, 14769–14774 (2011).

    Article  CAS  Google Scholar 

  2. Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).

    Article  CAS  Google Scholar 

  3. Koven, C. D., Lawrence, D. M. & Riley, W. J. Permafrost carbon−climate feedback is sensitive to deep soil carbon decomposability but not deep soil nitrogen dynamics. Proc. Natl Acad. Sci. USA 112, 3752–3757 (2015).

  4. Knorr, W., Prentice, I. C., House, J. I. & Holland, E. A. Long-term sensitivity of soil carbon turnover to warming. Nature 433, 298–301 (2005).

    Article  CAS  Google Scholar 

  5. Hugelius, G. et al. Estimated stocks of circumpolar permafrost carbon with quantified uncertainty ranges and identified data gaps. Biogeosciences 11, 6573–6593 (2014).

    Article  Google Scholar 

  6. Schuur, Ea. G. et al. Climate change and the permafrost carbon feedback. Nature 520, 171–179 (2015).

    Article  CAS  Google Scholar 

  7. Jorgenson, M. T., Shur, Y. L. & Pullman, E. R. Abrupt increase in permafrost degradation in Arctic Alaska. Geophys. Res. Lett. 33, L02503 (2006).

  8. Osterkamp, T. E. & Romanovsky, V. E. Evidence for warming and thawing of discontinuous permafrost in Alaska. Permafr. Periglac. Process. 10, 17–37 (1999).

    Article  Google Scholar 

  9. Schuur, E. A. et al. The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459, 556–559 (2009).

    Article  CAS  Google Scholar 

  10. Hicks Pries, C. E., Schuur, E. A. G. & Crummer, K. G. Thawing permafrost increases old soil and autotrophic respiration in tundra: partitioning ecosystem respiration using δC and ∆14C. Glob. Change Biol. 19, 649–661 (2013).

    Article  Google Scholar 

  11. Jones, C. D., Cox, P. & Huntingford, C. Uncertainty in climate–carbon-cycle projections associated with the sensitivity of soil respiration to temperature. Tellus B 55, 642–648 (2003).

    Google Scholar 

  12. Trumbore, S. Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol. Appl. 10, 399–411 (2000).

    Article  Google Scholar 

  13. Lützow, Mv et al. Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—a review. Eur. J. Soil Sci. 57, 426–445 (2006).

    Article  Google Scholar 

  14. Conant, R. T. et al. Temperature and soil organic matter decomposition rates – synthesis of current knowledge and a way forward. Glob. Change Biol. 17, 3392–3404 (2011).

    Article  Google Scholar 

  15. Hartley, I. P. & Ineson, P. Substrate quality and the temperature sensitivity of soil organic matter decomposition. Soil Biol. Biochem. 40, 1567–1574 (2008).

    Article  CAS  Google Scholar 

  16. Craine, J. M., Fierer, N. & McLauchlan, K. K. Widespread coupling between the rate and temperature sensitivity of organic matter decay. Nat. Geosci. 3, 854–857 (2010).

    Article  CAS  Google Scholar 

  17. Feng, X. & Simpson, M. J. Temperature responses of individual soil organic matter components. J. Geophys. Res. Biogeosci. 113, G03036 (2008).

    Google Scholar 

  18. Townsend, A. R., Vitousek, P. M., Desmarais, D. J. & Tharpe, A. Soil carbon pool structure and temperature sensitivity inferred using CO2 and 13CO2 incubation fluxes from five Hawaiian soils. Biogeochemistry 38, 1–17 (1997).

    Article  CAS  Google Scholar 

  19. Fang, C., Smith, P., Moncrieff, J. B. & Smith, J. U. Similar response of labile and resistant soil organic matter pools to changes in temperature. Nature 433, 57–59 (2005).

    Article  CAS  Google Scholar 

  20. Gillabel, J., Cebrian-Lopez, B., Six, J. & Merckx, R. Experimental evidence for the attenuating effect of SOM protection on temperature sensitivity of SOM decomposition. Glob. Change Biol. 16, 2789–2798 (2010).

    Article  Google Scholar 

  21. Dioumaeva, I. et al. Decomposition of peat from upland boreal forest: temperature dependence and sources of respired carbon. J. Geophys. Res. Atmos. 107, 8222 (2002).

    Article  Google Scholar 

  22. Kleber, M. et al. Old and stable soil organic matter is not necessarily chemically recalcitrant: implications for modeling concepts and temperature sensitivity. Glob. Change Biol. 17, 1097–1107 (2011).

    Article  Google Scholar 

  23. Reichstein, M. et al. Temperature sensitivity of decomposition in relation to soil organic matter pools: critique and outlook. Biogeosciences 2, 317–321 (2005).

    Article  CAS  Google Scholar 

  24. Bradford, M. A. et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11, 1316–1327 (2008).

    Article  Google Scholar 

  25. Tang, J. & Riley, W. J. Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions. Nat. Clim. Change 5, 56–60 (2015).

    Article  CAS  Google Scholar 

  26. Lupascu, M., Welker, J. M., Xu, X. & Czimczik, C. I. Rates and radiocarbon content of summer ecosystem respiration in response to long-term deeper snow in the High Arctic of NW Greenland. J. Geophys. Res. Biogeosci. 119, 2013JG002494 (2014).

    Article  Google Scholar 

  27. Vaughn, L. J. S. & Torn, M. S. Radiocarbon measurements of ecosystem respiration and soil pore-space CO2 in Utqiaġvik (Barrow), Alaska. Earth Syst. Sci. Data. 10, 1943–1957 (2018).

    Article  Google Scholar 

  28. Friedlingstein, P. et al. Climate–carbon cycle feedback analysis: results from the C4MIP model intercomparison. J. Clim. 19, 3337–3353 (2006).

    Article  Google Scholar 

  29. German, D. P., Marcelo, K. R. B., Stone, M. M. & Allison, S. D. The Michaelis–Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study. Glob. Change Biol. 18, 1468–1479 (2012).

    Article  Google Scholar 

  30. Min, K., Lehmeier, C. A., Ballantyne, F., Tatarko, A. & Billings, S. A. Differential effects of pH on temperature sensitivity of organic carbon and nitrogen decay. Soil Biol. Biochem. 76, 193–200 (2014).

    Article  CAS  Google Scholar 

  31. Bockheim, J. G., Everett, L. R., Hinkel, K. M., Nelson, F. E. & Brown, J. Soil organic carbon storage and distribution in Arctic tundra, Barrow, Alaska. Soil Sci. Soc. Am. J. 63, 934–940 (1999).

    Article  CAS  Google Scholar 

  32. Billings, W. D. & Peterson, K. M. Vegetational change and ice-wedge polygons through the thaw-lake cycle in Arctic Alaska. Arct. Alp. Res. 4, 413–432 (1980).

  33. Brown, J, Miller, P. C, Tieszen, L. L. & Bunnell, F. An Arctic Ecosystem: The Coastal Tundra at Barrow, Alaska (Hutchinson and Ross, 1980).

  34. Wainwright, H. M. et al. Identifying multiscale zonation and assessing the relative importance of polygon geomorphology on carbon fluxes in an Arctic tundra ecosystem. J. Geophys. Res. Biogeosci. 120, 788–808 (2015).

    CAS  Google Scholar 

  35. Sloan, V. L. et al. Plant Community Composition and Vegetation Height, Barrow, Alaska, Ver. 1 (Carbon Dioxide Information Analysis Center, 2014).

  36. Newman, B. D. et al. Microtopographic and depth controls on active layer chemistry in Arctic polygonal ground. Geophys. Res. Lett. 42, 1808–1817 (2015).

    Article  CAS  Google Scholar 

  37. Graven, H. D., Guilderson, T. P. & Keeling, R. F. Methods for high-precision14C AMS measurement of atmospheric CO2 at LLNL. Radiocarbon 49, 349–356 (2007).

    Article  CAS  Google Scholar 

  38. Stuiver, M. & Polach, H. A. Discussion reporting of 14C data. Radiocarbon 19, 355–363 (1977).

    Article  Google Scholar 

  39. Torn, M., Swanston, C., Castanha, C. & Trumbore, S. in Biophysico-Chemical Processes Involving Natural Nonliving Organic Matter in Environmental Systems (eds Sinesi, N. et al.) 219–272 (John Wiley, 2009).

  40. Reimer, P. J. et al. IntCal13 and Marine13 Radiocarbon Age Calibration Curves 0–50,000 Years cal BP. Radiocarbon 55, 1869–1887 (2013).

    Article  CAS  Google Scholar 

  41. Nydal, R. & Lövseth, K. Carbon-14 Measurements in Atmospheric CO 2 from Northern and Southern Hemisphere Sites, 1962–1993 (Oak Ridge National Lab., Oak Ridge Inst. for Science and Education, 1996).

  42. Graven, H. D., Guilderson, T. P. & Keeling, R. F. Observations of radiocarbon in CO2 at seven global sampling sites in the Scripps flask network: analysis of spatial gradients and seasonal cycles. J. Geophys. Res. Atmos. 117, D02303 (2012).

    Google Scholar 

  43. Loya, W. M. et al. Pulse-labeling studies of carbon cycling in arctic tundra ecosystems: Contribution of photosynthates to soil organic matter. Glob. Biogeochem. Cycles 16, 1101 (2002).

    Article  Google Scholar 

  44. Dennis, J. G. Distribution patterns of belowground standing crop in arctic tundra at barrow, Alaska. Arct. Alp. Res. 9, 113 (1977).

    Article  Google Scholar 

  45. Billings, W. D., Peterson, K. M. & Shaver, G. R. in Vegetation and Production Ecology of an Alaskan Arctic Tundra (ed. Tieszen, L. L.) 415–434 (Springer New York, 1978).

  46. Sierra, C. A., Müller, M., Metzler, H., Manzoni, S. & Trumbore, S. E. The muddle of ages, turnover, transit, and residence times in the carbon cycle. Glob. Change Biol. 23, 1763–1773 (2017).

    Article  Google Scholar 

  47. Bates, D., Maechler, M., Bolker, B. M. & Walker, S. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7. (2014).

  48. Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest: Tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R package version 2.0-11. (2014).

  49. Vaughn, L. J. S. & Torn, M. S. Radiocarbon in CO2 and Soil Organic Matter from Laboratory Incubations, Barrow, Alaska, 2012. (Next Generation Ecosystem Experiments Arctic Data Collection, Oak Ridge National Laboratory, U.S. Department of Energy, 2018).

Download references

Acknowledgements

This research was conducted through the Next-Generation Ecosystem Experiments (NGEE-Arctic) project, which is supported by the Office of Biological and Environmental Research in the US Department of Energy Office of Science.

Author information

Authors and Affiliations

Authors

Contributions

L.J.S.V. and M.S.T. designed the soil collection and incubation procedure, L.J.S.V. collected data and designed the analysis with guidance from M.S.T., and L.J.S.V. prepared the manuscript with contributions from M.S.T.

Corresponding authors

Correspondence to Lydia J. S. Vaughn or Margaret S. Torn.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figures 1–12 and Supplementary Tables 1–5.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vaughn, L.J.S., Torn, M.S. 14C evidence that millennial and fast-cycling soil carbon are equally sensitive to warming. Nat. Clim. Chang. 9, 467–471 (2019). https://doi.org/10.1038/s41558-019-0468-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41558-019-0468-y

This article is cited by

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology