Letter | Published:

Carbon balance of Arctic tundra under increased snow cover mediated by a plant pathogen

Nature Climate Change volume 1, pages 220223 (2011) | Download Citation

Abstract

Climate change is affecting plant community composition1 and ecosystem structure, with consequences for ecosystem processes such as carbon storage2,3,4. Climate can affect plants directly by altering growth rates1, and indirectly by affecting predators and herbivores, which in turn influence plants5,6,7,8,9. Diseases are also known to be important for the structure and function of food webs10,11,12,13,14. However, the role of plant diseases in modulating ecosystem responses to a changing climate is poorly understood15,16. This is partly because disease outbreaks are relatively rare and spatially variable, such that that their effects can only be captured in long-term experiments. Here we show that, although plant growth was favoured by the insulating effects of increased snow cover in experimental plots in Sweden, plant biomass decreased over the seven-year study. The decline in biomass was caused by an outbreak of a host-specific parasitic fungus, Arwidssonia empetri, which killed the majority of the shoots of the dominant plant species, Empetrum hermaphroditum, after six years of increased snow cover. After the outbreak of the disease, instantaneous measurements of gross photosynthesis and net ecosystem carbon exchange were significantly reduced at midday during the growing season. Our results show that plant diseases can alter and even reverse the effects of a changing climate on tundra carbon balance by altering plant composition.

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References

  1. 1.

    et al. Plant community responses to experimental warming across the tundra biome. Proc. Natl Acad. Sci. USA 103, 1342–1346 (2006).

  2. 2.

    et al. Role of land-surface changes in arctic summer warming. Science 310, 657–660 (2005).

  3. 3.

    et al. Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431, 440–443 (2004).

  4. 4.

    et al. 2009. Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460, 616–620 (2009).

  5. 5.

    & Opposing plant community responses to warming with and without herbivores. Proc. Natl Acad. Sci. USA 105, 12353–12357 (2008).

  6. 6.

    et al. Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456, 946–948 (2008).

  7. 7.

    et al. Herbivores inhibit climate-driven shrub expansion on the tundra. Glob. Change Biol. 15, 2681–2693 (2009).

  8. 8.

    et al. Ecological dynamics across the arctic associated with recent climate change. Science 325, 1355–1358 (2009).

  9. 9.

    , & Habitat type determines herbivory controls over CO2 fluxes in a warmer arctic. Ecology 89, 2103–2116 (2008).

  10. 10.

    , , & Complex biotic interactions drive long-term vegetation change in a nitrogen enriched boreal forest. Ecosystems 12, 1204–1211 (2009).

  11. 11.

    , , & Pathogen-induced reversal of native dominance in a grassland community. Proc. Natl Acad. Sci. USA 104, 5473–5478 (2009).

  12. 12.

    et al. A disease-mediated trophic cascade in the Serengeti and its implications for ecosystem C. PLoS Biol. 7, e1000210 (2009).

  13. 13.

    et al. Predator disease out-break modulates top-down, bottom-up and climatic effects on herbivore population dynamics. Ecol. Lett. 9, 383–389 (2006).

  14. 14.

    , & Response of plant pathogens and herbivores to a warming experiment. Ecology 85, 2570–2581 (2004).

  15. 15.

    et al. Global change shifts vegetation and plant–parasite interactions in a boreal mire. Ecology 88, 454–464 (2007).

  16. 16.

    et al. Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2163 (2002).

  17. 17.

    Om den olikformiga snöbeteckningens inflytande på  vegetationen i Sarekfjällen. Bot. Not 5, 241–268 (1902).

  18. 18.

    & A review of snow manipulation experiments in arctic and alpine ecosystems. Polar Res. 29, 95–109 (2010).

  19. 19.

    , & Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities. Soil Biol. Biochem. 36, 217–227 (2004).

  20. 20.

    & Deepened snow alters soil microbial nutrient limitations in arctic birch hummock tundra. Appl. Soil Ecol. 39, 210–222 (2008).

  21. 21.

    , , , & Winter warming events damage sub-Arctic vegetation: Consistent evidence from an experimental manipulation and a natural event. J. Ecol. 97, 1408–1415 (2009).

  22. 22.

    & Understory vegetation as a forest ecosystem driver: Evidence from northern Swedish boreal forest. Front. Ecol. Environ. 3, 421–428 (2005).

  23. 23.

    et al. Parasitic fungus mediates change in nitrogen-exposed boreal forest vegetation. J. Ecol. 90, 61–67 (2002).

  24. 24.

    , & Vegetation responses in Alaskan arctic tundra after 8 years of summer warming and winter snow manipulation experiment. Glob. Change Biol. 11, 537–552 (2005).

  25. 25.

    , & Annual CO2 flux in dry and moist arctic tundra: Field responses to increases in summer temperatures and winter snow depth. Clim. Change 44, 139–150 (2000).

  26. 26.

    & Deeper snow enhances winter respiration from both plant-associated and bulk soil carbon pools in birch hummock tundra. Ecosystems 10, 419–431 (2007).

  27. 27.

    et al. The importance of winter in annual ecosystem respiration in the high arctic: Effects of snow depth in two vegetation types. Polar Res. 29, 58–74 (2010).

  28. 28.

    Impact of grazing and neighbour removal on a heath plant community transplanted onto a snowbed site, NW Finnish Lapland. Oikos 81, 359–367 (1998).

  29. 29.

    , & Facilitation and competition on gradients in alpine plant communities. Ecology 82, 3295–3308 (2001).

  30. 30.

    The Non-Lichenized Pyrenomycetes of Sweden (Lund, SBT-förlaget, 1992).

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Acknowledgements

The Abisko Scientific Research Station provided accommodation, laboratory facilities and funding during the periods of field work. The study was supported by grants from the Centre for Environmental Research in Umeå  (CMF) and The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning to J.O. and NER/A/S/2001/00460 from the Natural Environment Research Council, UK, to R.B.

Author information

Affiliations

  1. Department of Ecology and Environmental Science, Umeå University, SE-901 87 Umeå, Sweden

    • Johan Olofsson
    • , Lars Ericson
    •  & Mikaela Torp
  2. Department of Ecology, Swedish University of Agricultural Sciences, Box 7044, SE-750 07 Uppsala, Sweden

    • Mikaela Torp
  3. Finnish Forest Research Institute, Rovaniemi Research Station, FIN-96301 Rovaniemi, Finland

    • Sari Stark
  4. School of Biological and Biomedical Sciences, Centre for Ecosystem Science, University of Durham, Durham DH1 3LE, UK

    • Robert Baxter

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Contributions

R.B. initiated the field experiment and managed it together with J.O. S.S. carried out the soil analyses. R.B. and J.O. were together responsible for all other field measurements. M.T. contributed to the field work. J.O., L.E. and R.B. outlined the scope of the study and linked various components. J.O. carried out the statistical analyses and wrote the manuscript, to which all authors contributed with discussions and text.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Johan Olofsson.

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DOI

https://doi.org/10.1038/nclimate1142

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