, Volume 41, Supplement 3, pp 246–255 | Cite as

Ecosystem Response to Climatic Change: The Importance of the Cold Season

  • Stef Bokhorst
  • Jarle W. Bjerke
  • Hans Tømmervik
  • Catherine Preece
  • Gareth K. Phoenix


Winter climate and snow cover are the important drivers of plant community development in polar regions. However, the impacts of changing winter climate and associated changes in snow regime have received much less attention than changes during summer. Here, we synthesize the results from studies on the impacts of extreme winter weather events on polar heathland and lichen communities. Dwarf shrubs, mosses and soil arthropods were negatively impacted by extreme warming events while lichens showed variable responses to changes in extreme winter weather events. Snow mould formation underneath the snow may contribute to spatial heterogeneity in plant growth, arthropod communities and carbon cycling. Winter snow cover and depth will drive the reported impacts of winter climate change and add to spatial patterns in vegetation heterogeneity. The challenges ahead lie in obtaining better predictions on the snow patterns across the landscape and how these will be altered due to winter climate change.


Autumn Empetrum nigrum Icing Snow Snow mould Winter 



We would like to thank Terry V. Callaghan for all the excellent ideas and suggestions during the fieldwork and discussions at Abisko that shaped the work presented here, and his support for the project while director of ANS. This research was supported by a Leverhulme Trust (UK) grant to GKP and TVC, by a grant from the Research Council of Norway awarded to JWB (Contract Nos. 171542/V10 and 216434/E10), by ATANS grants (EU Transnational Access Programme) to JWB, GKP and SB and by the Netherlands Polar Programme (NPP-NWO 851.20.016). This article was improved by the constructive comments of two anonymous reviewers.


  1. Aerts, R., and F.S. Chapin. 2000. The mineral nutrition of wild plants revisited: A re-evaluation of processes and patterns. Advances in Ecological Research 30: 1–67.CrossRefGoogle Scholar
  2. Benedict, J.B. 1991. Experiments on lichen growth. 2 Effects of a seasonal snow cover. Arctic and Alpine Research 23: 189–199.CrossRefGoogle Scholar
  3. Berg, M.P., M. Stoffer, and H.H. van den Heuvel. 2004. Feeding guilds in Collembola based on digestive enzymes. Pedobiologia 48: 589–601.CrossRefGoogle Scholar
  4. Bjerke, J.W. 2009. Ice encapsulation protects rather than disturbs the freezing lichen. Plant Biology 11: 227–235.CrossRefGoogle Scholar
  5. Bjerke, J.W. 2011. Winter climate change: Ice encapsulation at mild subfreezing temperatures kills freeze-tolerant lichens. Environmental and Experimental Botany 72: 404–408.CrossRefGoogle Scholar
  6. Bjerke, J.W., and H. Tømmervik. 2008. Observerte skader på nordnorske planter i løpet av vår og sommer 2006: omfang og mulige årsaker. Blyttia 66: 90–96. (In Norwegian).Google Scholar
  7. Bjerke, J.W., S. Bokhorst, M. Zielke, T.V. Callaghan, F.W. Bowles, and G.K. Phoenix. 2011. Contrasting sensitivity to extreme winter warming events of dominant sub-Arctic heathland bryophyte and lichen species. Journal of Ecology 99: 1481–1488.CrossRefGoogle Scholar
  8. Bokhorst, S., A. Huiskes, P. Convey, and R. Aerts. 2007a. The effect of environmental change on vascular plant and cryptogam communities from the Falkland Islands and the Maritime Antarctic. BMC Ecology 715. doi: 10.1186/1472-6785-1187-1115
  9. Bokhorst, S., C. Ronfort, A. Huiskes, P. Convey, and R. Aerts. 2007b. Food choice of Antarctic soil arthropods clarified by stable isotope signatures. Polar Biology 30: 983–990.CrossRefGoogle Scholar
  10. Bokhorst, S., A.H.L. Huiskes, P. Convey, P.M.V. Bodegom, and R. Aerts. 2008. Climate change effects on soil arthropod communities from the Falkland Islands and the Maritime Antarctic. Soil Biology and Biochemistry 40: 1547–1556.CrossRefGoogle Scholar
  11. Bokhorst, S., J.W. Bjerke, H. Tømmervik, T.V. Callaghan, and G.K. Phoenix. 2009. Winter warming events damage sub-Arctic vegetation: Consistent evidence from an experimental manipulation and a natural event. Journal of Ecology 97: 1408–1415.CrossRefGoogle Scholar
  12. Bokhorst, S., J.W. Bjerke, M. Davey, K. Taulavouri, E. Taulavuori, K. Laine, T.V. Callaghan, and G.K. Phoenix. 2010. Impacts of extreme winter warming events on plant physiology in a sub-Arctic heath community. Physiologia Plantarum 140: 128–140.CrossRefGoogle Scholar
  13. Bokhorst, S., J.W. Bjerke, L. Street, T.V. Callaghan, and G.K. Phoenix. 2011a. Impacts of multiple extreme winter warming events on sub-Arctic heathland: Phenology, reproduction, growth, and CO2 flux responses. Global Change Biology 17: 2817–2830.CrossRefGoogle Scholar
  14. Bokhorst, S., A.H.L. Huiskes, P. Convey, B.J. Sinclair, M. Lebouvier, B. van de Vijver, and D.H. Wall. 2011b. Microclimate impacts of passive warming methods in Antarctica: Implications for climate change studies. Polar Biology 34: 1421–1435.CrossRefGoogle Scholar
  15. Bokhorst, S., G.K. Phoenix, J.W. Bjerke, T.V. Callaghan, F. Huyer-Brugman, and M.P. Berg. 2012. Extreme winter warming events more negatively impact small rather than large soil fauna: Shift in community composition explained by traits not taxa. Global Change Biology 18: 1152–1162.CrossRefGoogle Scholar
  16. Callaghan, T.V., L.O. Bjorn, Y. Chernov, T. Chapin, T.R. Christensen, B. Huntley, R.A. Ims, M. Johansson, et al. 2004. Responses to projected changes in climate and UV-B at the species level. AMBIO 33: 418–435.Google Scholar
  17. Callaghan, T.V., M. Johansson, R.D. Brown, P.Y. Groisman, N. Labba, V. Radionov, R.S. Bradley, S. Blangy, et al. 2011. Multiple effects of changes in arctic snow cover. AMBIO 40: 32–45.CrossRefGoogle Scholar
  18. Christensen, J.H., B. Hewitson, A. Busuioc, A. Cheng, X. Gao, I. Held, R. Jones, R.K. Kolli, et al. 2007. Regional climate projections. In Climate change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change, eds. S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, and H.L. Miller, 847–940. Cambridge: Cambridge University Press.Google Scholar
  19. Colbeck, S.C. 1991. The layered character of snow covers. Reviews of Geophysics 29: 81–96.CrossRefGoogle Scholar
  20. Cornelissen, J.H.C., S.I. Lang, N.A. Soudzilovskaia, and H.J. During. 2007. Comparative cryptogam ecology: A review of bryophyte and lichen traits that drive biogeochemistry. Annals of Botany 99: 987–1001.CrossRefGoogle Scholar
  21. Cunningham, C., N.E. Zimmermann, V. Stoeckli, and H. Bugmann. 2006. Growth response of Norway spruce saplings in two forest gaps in the Swiss Alps to artificial browsing, infection with black snow mold, and competition by ground vegetation. Canadian Journal of Forest Research 36: 2782–2793.CrossRefGoogle Scholar
  22. Dorrepaal, E., R. Aerts, J.H.C. Cornelissen, T.V. Callaghan, and R.S.P. van Logtestijn. 2004. Summer warming and increased winter snow cover affect Sphagnum fuscum growth, structure and production in a sub-arctic bog. Global Change Biology 10: 93–104.CrossRefGoogle Scholar
  23. Elmendorf, S.C., G.H.R. Henry, R.D. Hollister, R.G. Bjork, A.D. Bjorkman, T.V. Callaghan, L.S. Collier, E.J. Cooper, et al. 2012. Global assessment of experimental climate warming on tundra vegetation: Heterogeneity over space and time. Ecology Letters 15: 164–175.CrossRefGoogle Scholar
  24. Filser, J. 2002. The role of Collembola in carbon and nitrogen cycling in soil. Pedobiologia 46: 234–245.Google Scholar
  25. Gaines, S.D., and M.W. Denny. 1993. The largest, smallest, highest, lowest, longest, and shortest—extremes in ecology. Ecology 74: 1677–1692.CrossRefGoogle Scholar
  26. Graae, B.J., I.G. Alsos, and R. Ejrnaes. 2008. The impact of temperature regimes on development, dormancy breaking and germination of dwarf shrub seeds from arctic, alpine and boreal sites. Plant Ecology 198: 275–284.CrossRefGoogle Scholar
  27. Hessl, A.E., and W.L. Baker. 1997. Spruce and fir regeneration and climate in the forest-tundra ecotone of Rocky Mountain National Park, Colorado USA. Arctic and Alpine Research 29: 173–183.CrossRefGoogle Scholar
  28. Hubert, J., M. Zilova, and S. Pekar. 2001. Feeding preferences and gut contents of three panphytophagous oribatid mites Acari: Oribatida. European Journal of Soil Biology 37: 197–208.CrossRefGoogle Scholar
  29. Inouye, D.W. 2000. The ecological and evolutionary significance of frost in the context of climate change. Ecology Letters 3: 457–463.CrossRefGoogle Scholar
  30. Johansson, C., V.A. Pohjola, C. Jonasson, and T.V. Callaghan. 2011. Multi-decadal changes in snow characteristics in sub-Arctic Sweden. AMBIO 40: 566–574.CrossRefGoogle Scholar
  31. Jørgensen, M., L. Østrem, and M. Höglind. 2010. De-hardening in contrasting cultivars of timothy and perennial ryegrass during winter and spring. Grass & Forage Science 65: 38–48.CrossRefGoogle Scholar
  32. Kappen, L. 2000. Some aspects of the great success of lichens in Antarctica. Antarctic Science 12: 314–324.CrossRefGoogle Scholar
  33. Kappen, L., M. Sommerkorn, and B. Schroeter. 1995. Carbon acquisition and water relations of lichens in polar regions—potentials and limitations. Lichenologist 27: 531–545.Google Scholar
  34. Kumpula, J., P. Parikka, and M. Nieminen. 2000. Occurrence of certain microfungi on reindeer pastures in northern Finland during winter 1996–97. Rangifer 20: 3–8.Google Scholar
  35. Maraun, M., S. Migge, M. Schaefer, and S. Scheu. 1998. Selection of microfungal food by six oribatid mite species Oribatida, Acari from two different beech forests. Pedobiologia 42: 232–240.Google Scholar
  36. Matsumoto, N. 2009. Snow molds: A group of fungi that prevail under snow. Microbes and Environments 24: 14–20.CrossRefGoogle Scholar
  37. Olofsson, J., L. Ericson, M. Torp, S. Stark, and R. Baxter. 2011. Carbon balance of Arctic tundra under increased snow cover mediated by a plant pathogen. Nature Climate Change 1: 220–223.CrossRefGoogle Scholar
  38. Parmesan, C., and G. Yohe. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37–42.CrossRefGoogle Scholar
  39. Pearce, R.S. 2001. Plant freezing and damage. Annals of Botany 87: 417–424.CrossRefGoogle Scholar
  40. Phoenix, G.K., and J.A. Lee. 2004. Predicting impacts of Arctic climate change: Past lessons and future challenges. Ecological Research 19: 65–74.CrossRefGoogle Scholar
  41. Putkonen, J., and G. Roe. 2003. Rain-on-snow events impact soil temperatures and affect ungulate survival. Geophysical Research Letters 30: 1188. doi: 1110.1029/2002GL016326.CrossRefGoogle Scholar
  42. Riseth, J.A., H. Tømmervik, E. Helander-Renvall, N. Labba, C. Johansson, E. Malnes, J.W. Bjerke, C. Jonsson, et al. 2011. Sámi traditional ecological knowledge as a guide to science: Snow, ice and reindeer pasture facing climate change. Polar Record 47: 202–217.CrossRefGoogle Scholar
  43. Schroeter, B., S.L. Kaplan, F. Schulz, and L.G. Sancho. 2000. Seasonal variation in the carbon balance of lichens in the maritime antarctic: Long-term measurements of photosynthetic activity in Usnea aurantiaco-atra. In Antarctic ecosystems: Models for wider ecological understanding, ed. W. Davidson, C. Howard-Williams, and P. Broady, 258–262. Christchurch: The Caxton Press.Google Scholar
  44. Schmidt, S.K., K.L. Wilson, R.K. Monson, and D.A. Lipson. 2009. Exponential growth of snow molds at sub-zero temperatures: an explanation for high beneath-snow respiration rates and Q 10 values. Biogeochemistry 95: 13–21.CrossRefGoogle Scholar
  45. Schmidt, N.M., C. Baittinger, J. Kollmann, and M.C. Forchhammer. 2010. Consistent dendrochronological response of the Dioecious Salix arctica to variation in local snow precipitation across gender and vegetation types. Arctic, Antarctic, and Alpine Research 42: 471–475.CrossRefGoogle Scholar
  46. Simms, H.R. 1967. On the ecology of Herpotrichia nigra. Mycologia 59: 902–909.CrossRefGoogle Scholar
  47. Sturm, M., J.P. McFadden, G.E. Liston, F.S. Chapin, C.H. Racinem, and J. Holmgren. 2001. Snow-shrub interactions in Arctic tundra: A hypothesis with climatic implications. Journal of Climate 14: 336–344.CrossRefGoogle Scholar
  48. Taub, D.R., and M.T. Lerdau. 2000. Relationship between leaf nitrogen and photosynthetic rate for three NAD-ME and three NADP-ME C-4 grasses. American Journal of Botany 87: 412–417.CrossRefGoogle Scholar
  49. Tolvanen, A. 1997. Recovery of the bilberry Vaccinium myrtillus L. from artificial spring and summer frost. Plant Ecology 1301: 35–39.CrossRefGoogle Scholar
  50. Van Straalen, N.M., and P.C. Rijninks. 1982. The efficiency of Tullgren apparatus with respect to interpreting seasonal changes in age structure of soil arthropod populations. Pedobiologia 24: 197–209.Google Scholar
  51. Walker, D.A., W.D. Billings, and J.G. de Molenaar. 2001. Snow-vegetation interactions in tundra environments. In Snow ecology: An interdisciplinary examination of snow-covered ecosystems, ed. H.G. Jones, J.W. Pomeroy, D.A. Walker, and R.W. Hoham, 266–324. Cambridge: Cambridge University Press.Google Scholar
  52. Wall, D.H., M.A. Bradford, M.G.S. John, J.A. Trofymow, V. Behan-Pelletier, D.D.E. Bignell, J.M. Dangerfield, W.J. Parton, et al. 2008. Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent. Global Change Biology 14: 2661–2677.Google Scholar
  53. Wipf, S., and C. Rixen. 2010. A review of snow manipulation experiments in Arctic and alpine tundra ecosystems. Polar Research 29: 95–109.CrossRefGoogle Scholar
  54. Ye, H.C., D.Q. Yang, and D. Robinson. 2008. Winter rain on snow and its association with air temperature in northern Eurasia. Hydrological Processes 22: 2728–2736.CrossRefGoogle Scholar

Copyright information

© Royal Swedish Academy of Sciences 2012

Authors and Affiliations

  • Stef Bokhorst
    • 1
  • Jarle W. Bjerke
    • 2
  • Hans Tømmervik
    • 2
  • Catherine Preece
    • 3
  • Gareth K. Phoenix
    • 3
  1. 1.Department of Forest Ecology and ManagementSwedish University of Agricultural SciencesUmeåSweden
  2. 2.Norwegian Institute for Nature Research (NINA), FRAM—High North Research Centre on Climate and the EnvironmentTromsöNorway
  3. 3.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK

Personalised recommendations