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Long-term warming restructures Arctic tundra without changing net soil carbon storage

Nature volume 497, pages 615–618 (2013)Cite this article

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Abstract

High latitudes contain nearly half of global soil carbon, prompting interest in understanding how the Arctic terrestrial carbon balance will respond to rising temperatures1,2. Low temperatures suppress the activity of soil biota, retarding decomposition and nitrogen release, which limits plant and microbial growth3. Warming initially accelerates decomposition4,5,6, increasing nitrogen availability, productivity and woody-plant dominance3,7. However, these responses may be transitory, because coupled abiotic–biotic feedback loops that alter soil-temperature dynamics and change the structure and activity of soil communities, can develop8,9. Here we report the results of a two-decade summer warming experiment in an Alaskan tundra ecosystem. Warming increased plant biomass and woody dominance, indirectly increased winter soil temperature, homogenized the soil trophic structure across horizons and suppressed surface-soil-decomposer activity, but did not change total soil carbon or nitrogen stocks, thereby increasing net ecosystem carbon storage. Notably, the strongest effects were in the mineral horizon, where warming increased decomposer activity and carbon stock: a ‘biotic awakening’ at depth.

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Figure 1: A canonical discriminant analysis plot reveals the loss of trophic heterogeneity across soil horizons in the greenhouse treatment relative to control conditions.
Figure 2: A discontinuous record of the difference between greenhouse treatment and control soil.

References

  1. Tarnocai et al. Soil organic carbon pools in the northern circumpolar permafrost region. Glob. Biogeochem. Cycles 23, GB2023 (2009)

    Article  ADS  Google Scholar 

  2. 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)

    Article  ADS  CAS  Google Scholar 

  3. Sturm, M. et al. Winter biological processes could help convert arctic tundra to shrubland. Bioscience 55, 17–26 (2005)

    Article  Google Scholar 

  4. Shaver, G. R. et al. Carbon turnover in Alaskan tundra soils: effects of organic matter quality, temperature, moisture and fertilizer. J. Ecol. 94, 740–753 (2006)

    Article  CAS  Google Scholar 

  5. Hobbie, S. E. & Chapin, F. S. The response of tundra plant biomass, aboveground production, nitrogen, and CO2 flux to experimental warming. Ecology 79, 1526–1544 (1998)

    Google Scholar 

  6. Oberbauer, S. F. et al. Tundra CO2 fluxes in response to experimental warming across latitudinal and moisture gradients. Ecol. Monogr. 77, 221–238 (2007)

    Article  Google Scholar 

  7. Natali, S. M., Schuur, E. A. G. & Rubin, R. L. Increased plant productivity in Alaskan tundra as a result of experimental warming of soil and permafrost. J. Ecol. 100, 488–498 (2012)

    Article  Google Scholar 

  8. Hodkinson, I. D. et al. Global change and Arctic ecosystems: conclusions and predictions from experiments with terrestrial invertebrates on Spitsbergen. Arct. Alp. Res. 30, 306–313 (1998)

    Article  Google Scholar 

  9. Deslippe, J. R., Hartmann, M., Simard, S. W. & Mohn, W. W. Long-term warming alters the composition of Arctic soil microbial communities. FEMS Microbiol. Ecol. 82, 303–315 (2012)

    Article  CAS  Google Scholar 

  10. McKane, R. B. et al. Climatic effects on tundra carbon storage inferred from experimental data and a model. Ecology 78, 1170–1187 (1997)

    Article  Google Scholar 

  11. Myers-Smith, I. H. et al. Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ. Res. Lett. 6, 045509 (2011)

    Article  ADS  Google Scholar 

  12. Rustad, L. E. et al. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562 (2001)

    Article  ADS  CAS  Google Scholar 

  13. Blok, D. et al. The response of Arctic vegetation to the summer climate: relation between shrub cover, NDVI, surface albedo and temperature. Environ. Res. Lett. 6, 035502 (2011)

    Article  ADS  Google Scholar 

  14. Sullivan, P. F. et al. Climate and species affect fine root production with long-term fertilization in acidic tussock tundra near Toolik Lake, Alaska. Oecologia 153, 643–652 (2007)

    Article  ADS  Google Scholar 

  15. Clemmensen, K. E., Michelsen, A., Jonasson, S. & Shaver, G. R. Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytol. 171, 391–404 (2006)

    Article  Google Scholar 

  16. Wallenstein, M. D., McMahon, S. & Schimel, J. Bacterial and fungal community structure in Arctic tundra tussock and shrub soils. FEMS Microbiol. Ecol. 59, 428–435 (2007)

    Article  CAS  Google Scholar 

  17. Oades, J. M. Soil organic matter and structural stability: mechanisms and implications for management. Plant Soil 76, 319–337 (1984)

    Article  CAS  Google Scholar 

  18. Loya, W. M., Johnson, L. C. & Nadelhoffer, K. J. Seasonal dynamics of leaf- and root-derived C in arctic tundra mesocosms. Soil Biol. Biochem. 36, 655–666 (2004)

    Article  CAS  Google Scholar 

  19. Lavoie, M., Mack, M. C. & Schuur, E. A. G. Effects of elevated nitrogen and temperature on carbon and nitrogen dynamics in Alaskan arctic and boreal soils. J. Geophys. Res. 116, G03013 (2011)

    Article  ADS  Google Scholar 

  20. Six, J., Bossuyt, H., Degryze, S. & Denef, K. A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res. 79, 7–31 (2004)

    Article  Google Scholar 

  21. Anisimov, O., a, Shiklomanov, N. I. & Nelson, F. E. Global warming and active-layer thickness: results from transient general circulation models. Glob. Planet. Change 15, 61–77 (1997)

    Article  ADS  Google Scholar 

  22. Hobbie, S. E., Gough, L. & Shaver, G. R. Species compositional differences on different-aged glacial landscapes drive contrasting responses of tundra to nutrient addition. J. Ecol. 93, 770–782 (2005)

    Article  Google Scholar 

  23. Deslippe, J. R., Hartmann, M., Mohn, W. W. & Simard, S. W. Long-term experimental manipulation of climate alters the ectomycorrhizal community of Betula nana in Arctic tundra. Glob. Change Biol. 17, 1625–1636 (2011)

    Article  ADS  Google Scholar 

  24. Fahnestock, J. T., Jones, M. H. & Welker, J. M. Wintertime CO2 efflux from Arctic soils: implications for annual carbon budgets. Glob. Biogeochem. Cycles 13, 775–779 (1999)

    Article  ADS  CAS  Google Scholar 

  25. Pollierer, M. M., Langel, R., Körner, C., Maraun, M. & Scheu, S. The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol. Lett. 10, 729–736 (2007)

    Article  Google Scholar 

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

    Article  ADS  Google Scholar 

  27. Oechel, W. C. et al. Recent change of Arctic tundra ecosystems from a net carbon dioxide sink to a source. Nature 361, 520–523 (1993)

    Article  ADS  Google Scholar 

  28. 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 (2004)

    Article  ADS  CAS  Google Scholar 

  29. Fierer, N. & Schimel, J. P. Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biol. Biochem. 34, 777–787 (2002)

    Article  CAS  Google Scholar 

  30. Bloem, J. Fluorescent staining of microbes for total direct counts. Mol. Microbial Ecol. Manual 1–12 (1995)

  31. West, A. W. & Sparling, G. P. Modifications to the substrate-induced respiration method to permit measurement of microbial biomass in soils of differing water contents. J. Microbiol. Methods 5, 177–189 (1986)

    Article  CAS  Google Scholar 

  32. Anderson, J. P. E. & Domsch, K. H. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol. Biochem. 10, 215–221 (1978)

    Article  CAS  Google Scholar 

  33. Beck, T. et al. An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biol. Biochem. 29, 1023–1032 (1997)

    Article  CAS  Google Scholar 

  34. Brookes, P. C., Landman, A., Prudenmaltese, G. & Jenkinson, D. S. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 17, 837–842 (1985)

    Article  CAS  Google Scholar 

  35. Frey, S., Elliott, E. & Paustian, K. Bacterial and fungal abundance and biomass in conventional and no-tillage agroecosystems along two climatic gradients. Soil Biol. Biochem. 31, 573–585 (1999)

    Article  CAS  Google Scholar 

  36. Ilic, B. et al. Single cell detection with micromechanical oscillators. J. Vac. Sci. Technol. B 19, 2825–2828 (2001)

    Article  CAS  Google Scholar 

  37. Darbyshire, J. F., Wheatley, R. E., Greaves, M. P. & Inkson, R. H. E. A rapid micromethod for estimating bacterial and protozoan populations in soil. Rev. Ecol. Biol. Sol 11, 465–475 (1974)

    Google Scholar 

  38. Gough, L., Moore, J. C., Shaver, G. R., Simpson, R. T. & Johnson, D. R. Above- and belowground responses of arctic tundra ecosystems to altered soil nutrients and mammalian herbivory. Ecology 93, 1683–1694 (2012)

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by a DOE Global Change Education Program Graduate Fellowship, a Leal Anne Kerry Mertes scholarship, and Explorer’s Club grant to S.A.S., NSF OPP-1023524 to J.P.S., NSF OPP-0425606 and NSF OPP-0909441 to J.C.M., NSF OPP-0425827 and NSF OPP-0909507 to L.G., and the Arctic LTER program NSF-DEB 1026843 to G.R.S. We thank J. Laundre for temperature and thaw depth data. We also thank three anonymous reviewers, C. D’Antonio, J. King, and S. Viswanathan for comments that greatly improved this manuscript.

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Authors and Affiliations

  1. Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, 93108, California, USA

    Seeta A. Sistla & Joshua P. Schimel

  2. Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, 80523, Colorado, USA

    John C. Moore & Rodney T. Simpson

  3. Department of Ecosystem Science and Sustainability, Colorado State University, Fort Collins, 80523, Colorado, USA

    John C. Moore

  4. Department of Biology, University of Texas at Arlington, Arlington, 76019, Texas, USA

    Laura Gough

  5. The Ecosystems Center, Marine Biological Laboratory, Woods Hole, 02543, Massachusetts, USA

    Gaius R. Shaver

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  1. Seeta A. Sistla
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Contributions

S.A.S., J.C.M., L.G., J.P.S. and G.R.S. conceived the study and designed scientific objectives. J.C.M. and R.T.S. collected the soil food web data, L.G. and G.R.S. collected the plant data, S.A.S. and J.P.S. collected the soil chemistry data. S.A.S., J.C.M., L.G. and R.T.S. carried out statistical analyses. S.A.S. wrote the paper. J.P.S., J.C.M., L.G. and G.R.S. provided textual edits and all authors commented on the analysis and presentation of the data.

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Correspondence to Seeta A. Sistla.

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The authors declare no competing financial interests.

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Sistla, S., Moore, J., Simpson, R. et al. Long-term warming restructures Arctic tundra without changing net soil carbon storage. Nature 497, 615–618 (2013). https://doi.org/10.1038/nature12129

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