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:

Warming-related increases in soil CO2 efflux are explained by increased below-ground carbon flux

Subjects

Abstract

The universally observed exponential increase in soil-surface CO2 efflux (‘soil respiration’; FS) with increasing temperature has led to speculation that global warming will accelerate soil-organic-carbon (SOC) decomposition1, reduce SOC storage, and drive a positive feedback to future warming2. However, interpreting temperature–FS relationships, and so modelling terrestrial carbon balance in a warmer world, is complicated by the many sources of respired carbon that contribute to FS (ref. 3) and a poor understanding of how temperature influences SOC decomposition rates4. Here we quantified FS, litterfall, bulk SOC and SOC fraction size and turnover, and total below-ground carbon flux (TBCF) across a highly constrained 5.2 °C mean annual temperature (MAT) gradient in tropical montane wet forest5. From these, we determined that: increases in TBCF and litterfall explain >90% of the increase in FS with MAT; bulk SOC and SOC fraction size and turnover rate do not vary with MAT; and increases in TBCF and litterfall do not influence SOC storage or turnover on century to millennial timescales. This gradient study shows that for tropical montane wet forest, long-term and whole-ecosystem warming accelerates below-ground carbon processes with no apparent impact on SOC storage.

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

Figure 1: The effects of mean annual temperature (MAT) on the components of total below-ground carbon flux (TBCF).
Figure 2: Mean residence time (MRT) and soil organic carbon (SOC) storage do not vary with mean annual temperature (MAT).
Figure 3: The relationship between short-range order (SRO) aluminium (Al) and the mean residence time (MRT) for soil organic carbon (SOC) for the four sampled depths in tropical montane wet forest in Hawaii.
Figure 4: Our test of ecosystem response to increasing mean annual temperature (MAT) supports the hypothesis that nearly all of the temperature-driven increase in soil-surface CO2 efflux is derived from increased total below-ground carbon flux (TBCF) and secondarily from increased litterfall both resulting from an anticipated increase in stand-level net primary productivity with warming.

Similar content being viewed by others

References

  1. Bond-Lamberty, B. & Thomson, A. Temperature-associated increases in the global soil respiration record. Nature 464, 579–582 (2010).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Kuzyakov, Y. Sources of CO2 efflux from soil and review of partitioning methods. Soil Biol. Biochem. 38, 425–448 (2006).

    Article  CAS  Google Scholar 

  4. Conant, R. 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 

  5. Litton, C. et al. The magnitude and variability of soil-surface CO2 efflux increase with temperature in Hawaiian tropical montane wet forests. Soil Biol. Biochem. 43, 2315–2323 (2011).

    Article  CAS  Google Scholar 

  6. IPCC, in Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.) 1–18 (Cambridge Univ. Press, 2007).

  7. Bonan, G. Forests and climate change: Forcings, feedbacks, and the climate benefits of forests. Science 320, 1444–1449 (2008).

    Article  CAS  Google Scholar 

  8. Giardina, C. & Ryan, M. Evidence that decomposition rates of organic carbon in mineral soil do not vary with temperature. Nature 404, 858–861 (2000).

    Article  CAS  Google Scholar 

  9. Baldocchi, D. et al. FLUXNET: A new tool to study the temporal and spatial variability of ecosystem-scale carbon dioxide, water vapor, and energy flux densities. Bul. Am. Meteorol. Soc. 82, 2415–2434 (2001).

    Article  Google Scholar 

  10. Luyssaert, S. et al. CO2 balance of boreal, temperate, and tropical forests derived from a global database. Glob. Change Biol. 13, 2509–2537 (2007).

    Article  Google Scholar 

  11. Litton, C. & Giardina, C. Belowground carbon flux and partitioning: Global patterns and response to temperature. Funct. Ecol. 22, 941–954 (2008).

    Article  Google Scholar 

  12. Binkley, D. & Fisher, R. Ecology and Management of Forest Soils 347 (Wiley, 2012).

    Google Scholar 

  13. Crow, S. E. et al. Sources of plant-derived carbon and stability of soil organic matter: Implications for global change. Glob. Change Biol. 15, 2003–2019 (2009).

    Article  Google Scholar 

  14. Kuzyakov, Y. Priming effects: Interactions between living and dead organic matter. Soil Biol. Biochem. 42, 1363–1371 (2010).

    Article  CAS  Google Scholar 

  15. Sayer, E. et al. Soil carbon release enhanced by increased tropical forest litterfall. Nature Clim. Change 1, 304–307 (2011).

    Article  CAS  Google Scholar 

  16. Dalias, P., Anderson, J. M., Bottner, P. & Coûteaux, M. M. Temperature responses of carbon mineralization in conifer forest soils from different regional climates incubated under standard laboratory conditions. Glob. Change Biol. 6, 181–192 (2001).

    Article  Google Scholar 

  17. Melillo, J. et al. Soil warming carbon–nitrogen interactions and carbon–nitrogen budgets. Proc. Natl Acad. Sci. USA 108, 9508–9512 (2011).

    Article  CAS  Google Scholar 

  18. Giardina, C., Binkley, D., Ryan, M. & Fownes, J. Belowground carbon cycling in a humid tropical forest decreases with fertilization. Oecologia 139, 545–550 (2004).

    Article  Google Scholar 

  19. Schmidt, M. et al. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56 (2011).

    Article  CAS  Google Scholar 

  20. Torn, M. et al. Mineral control of soil organic carbon storage and turnover. Nature 389, 170–173 (1997).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  22. Stewart, C. E., Paustian, K., Conant, R. T., Plante, A. F. & Six, J. Soil carbon saturation: Concept, evidence and evaluation. Biogeochem. 86, 19–31 (2007).

    Article  CAS  Google Scholar 

  23. Cusack, D. et al. The response of heterotrophic activity and carbon cycling to nitrogen additions and warming in two tropical soils. Glob. Change Biol. 16, 2555–2572 (2010).

    Google Scholar 

  24. Phillips, R. et al. Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2 . Ecol. Lett. 15, 1042–1049 (2012).

    Article  Google Scholar 

  25. Sistla, S. et al. Long-term warming restructures Arctic tundra without changing net soil carbon storage. Nature 497, 615–619 (2013).

    Article  CAS  Google Scholar 

  26. Iwashita, D., Litton, C. & Giardina, C. Coarse woody debris carbon pools across a 5.2 °C mean annual temperature gradient in tropical montane wet forest. For. Ecol. Manage. 291, 336–343 (2013).

    Google Scholar 

  27. Fissore, C., Giardina, C. & Kolka, R. Reduced substrate supply limits the temperature response of soil organic carbon decomposition. Soil Biol. Biochem. 67, 306–311 (2013).

    Article  CAS  Google Scholar 

  28. Asner, G. et al. Environmental and biotic controls over aboveground biomass throughout a tropical rain forest. Ecosystems 12, 261–278 (2009).

    Article  Google Scholar 

  29. Sollins, P. et al. Organic C and N stabilization in a forest soil: Evidence from sequential density fractionation. Soil Biol. Biochem. 38, 3313–3324 (2006).

    Article  CAS  Google Scholar 

  30. Courchesne, F. & Turmel, M. Extractable Al, Fe, Mn and Si. in Soil Sampling and Methods of Soil Analysis (eds Carter, M., Soon, Y. & Hendershot, W.) 307–316 (Lewis, 2008).

    Google Scholar 

Download references

Acknowledgements

We thank M. Long, J. Albano, M. Koontz, R. Mosley, J. Johansen, B. Hwang, K. Kinney and K. Kaneshiro for assistance with data collection, C. Fissore for assembling previously published radiocarbon data, T. Giambelluca for assistance with climate analyses, and D. Binkley, M. Busse, P. Selmants and D. Levinson for reviews of earlier versions of the manuscript. We thank the National Science Foundation (C.M.L. and C.P.G.), the College of Tropical Agriculture and Human Resources at the University of Hawaii at Manoa (C.M.L.), the Pacific Southwest Research Station, USDA Forest Service (C.P.G), and the Carnegie Institution for Science (G.P.A.) for funding to establish the study, collect flux data, and process and analyse soil samples. We thank C. Swanston and K. Heckman of the Northern Research Station, USDA Forest Service for funding, preparation and bulk SOC radiocarbon analyses at Lawrence Livermore National Laboratory; P. Reimer and the 14CHRONO Centre for Climate, the Environment, and Chronology, Queen’s University Belfast for radiocarbon analyses of SOC fractions; the USDA Forest Service, the State of Hawaii Department of Land and Natural Resources, Division of Forestry and Wildlife and the Parker Ranch for access to research plots in the Hawaii Experimental Tropical Forest; the US Fish and Wildlife Service for access to plots in Hakalau Forest National Wildlife Refuge. The Carnegie Airborne Observatory is made possible by the Andrew Mellon Foundation, John D. and Catherine T. MacArthur Foundation, Avatar Alliance Foundation, Grantham Foundation for the Protection of the Environment, Mary Anne Nyburg Baker and G. Leonard Baker Jr., and William R. Hearst III.

Author information

Authors and Affiliations

Authors

Contributions

C.M.L. and C.P.G. designed the study and secured funding for flux and stock analyses; C.P.G. secured funding for bulk SOC radiocarbon analyses; S.E.C. secured funding for fraction SOC radiocarbon analyses SRO data collection and analyses; G.P.A. secured funding for LiDAR data collection and analyses; all authors contributed to data interpretation and manuscript preparation; C.M.L. and C.P.G. led collection of flux and stock data; S.E.C. led analysis and interpretation of radiocarbon measurements; S.E.C. led collection, analysis and interpretation of SRO data; G.P.A. led LiDAR-based analyses of forest plots and, with the other authors, plot selection; C.M.L., C.P.G. and S.E.C. drafted figures; C.P.G. wrote the initial draft of the manuscript; all authors discussed and interpreted results, and provided editorial input.

Corresponding author

Correspondence to Christian P. Giardina.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Giardina, C., Litton, C., Crow, S. et al. Warming-related increases in soil CO2 efflux are explained by increased below-ground carbon flux. Nature Clim Change 4, 822–827 (2014). https://doi.org/10.1038/nclimate2322

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate2322

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