Skip to main content
SpringerLink
Log in

Snow evens fragmentation effects and food determines overwintering success in ground-dwelling voles

  • Original Article
  • Published:
Ecological Research

Abstract

Climate instability strongly affects overwintering conditions in organisms living in a strongly seasonal environment and consequently their survival and population dynamics. Food, predation and density effects are also strong during winter, but the effect of fragmentation of ground vegetation on ground-dwelling small mammals is unknown. Here, we report the results of a winter experiment on the effects of habitat fragmentation and food on experimental overwintering populations of bank voles Myodes glareolus. The study was conducted in large outdoor enclosures containing one large, two medium-sized or four small habitat patches or the total enclosure area covered with protective tall-grass habitat. During the stable snow cover of midwinter, only food affected the overwintering success, body condition, trappability and earlier onset of breeding in bank voles. However, after the snow thaw in spring, habitat fragmentation gained importance again, and breeding activities increased the movements of voles in the most fragmented habitat. The use of an open, risky matrix area increased along the habitat fragmentation. Our experiment showed that long-lasting stable snow cover protects overwintering individuals in otherwise exposed and risky ground habitats. We conclude that a stable winter climate and snow cover should even out habitat fragmentation effects on small mammals. However, along prolonged snow-free early winter and in an earlier spring thaw, this means loss of protection by snow cover both in terms of thermoregulation and predation. Thus, habitat cover is important for the survival of small ground-dwelling boreal mammals also during the non-breeding season.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aars J, Ims RA (2002) Intrinsic and climatic determinants of population demography: the winter dynamics of tundra voles. Ecology 83:3449–3456

    Article  Google Scholar 

  • Andreassen HP, Ims RA (2001) Dispersal in patchy vole populations: role of patch configuration, density dependence, and demography. Ecology 82:2911–2926

    Article  Google Scholar 

  • Andreassen HP, Hertzberg K, Ims RA (1998) Space-use responses to habitat fragmentation and connectivity in the root vole Microtus oeconomus. Ecology 79:1223–1235

    Google Scholar 

  • Batzli GO (1983) Responses of arctic rodent populations to nutritional factors. Oikos 40:396–406

    Article  Google Scholar 

  • Bjørnstad ON, Andreassen HP, Ims RA (1998) Effects of habitat patchiness and connectivity on the spatial ecology of the root vole Microtus oeconomus. J Anim Ecol 67:127–140

    Article  Google Scholar 

  • Boutin S (1990) Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can J Zool 68:203–223

    Article  Google Scholar 

  • Bujalska G (1985) Regulation of female maturation in Clethrionomys species, with special reference to an island population of C. glareolus. Ann Zool Fenn 22:331–342

    Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, New York

    Book  Google Scholar 

  • Desy EA, Batzli GO (1989) Effects of food availability and predation on prairie vole demography: a field experiment. Ecology 70:411–421

    Article  Google Scholar 

  • Eccard JA, Ylönen H (2001) Initiation of breeding after winter in bank voles: effects of food and population density. Can J Zool 79:1743–1753

    Article  Google Scholar 

  • Ergon T (2007) Optimal onset of seasonal reproduction in stochastic environments: when should overwintering small rodents start breeding. Ecoscience 14:330–346. doi:10.2980/1195-6860(2007)14[330:OOOSRI]2.0.CO;2

    Google Scholar 

  • Fahrig L, Merriam G (1994) Conservation of fragmented populations. Conserv Biol 8:50–59

    Article  Google Scholar 

  • Fretwell SD, Lucas HL (1970) On territorial behaviour and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheor 19:16–36

    Article  Google Scholar 

  • Groom MJ, Vynne CH (2006) Habitat degradation and loss. In: Groom MJ, Meffe GM, Caroll CR (eds) Principles of conservation biology. Sinauer, Sunderland, pp 173–212

  • Haapakoski M, Ylönen H (2010) Effects of fragmented breeding habitat and resource distribution on behavior and survival of the bank vole (Myodes glareolus). Popul Ecol 52:427–435

    Article  Google Scholar 

  • Haapakoski M, Sundell J, Ylönen H (2012) Predation risk and food: opposite effects on overwintering survival and onset of breeding in a boreal rodent. J Anim Ecol. doi:10.1111/j.1365-2656.2012.02005.x

    PubMed  Google Scholar 

  • Halonen M, Mappes T, Meri T, Suhonen J (2007) Influence of snow cover on food hoarding in Pygmy Owls Glaucidium passerinum. Ornis Fenn 84:105–111

    Google Scholar 

  • Hanski I, Gilpin ME (1997) Metapopulation biology: ecology, genetics, and evolution. Academic Press, London

    Google Scholar 

  • Hanski I, Henttonen H, Korpimaki E, Oksanen L, Turchin P (2001) Small-rodent dynamics and predation. Ecology 82:1505–1520

    Article  Google Scholar 

  • Hansson L (1985) The food of bank voles, food mice and yellow-necked mice. Symp Zool Soc Lond 55:141–168

    Google Scholar 

  • Hoset KS, Le Galliard JF, Gundersen G (2009) Demographic responses to a mild winter in enclosed vole populations. Popul Ecol 51:279–288

    Article  Google Scholar 

  • Huitu O, Jokinen I, Korpimaki E, Koskela E, Mappes T (2007) Phase dependence in winter physiological condition of cyclic voles. Oikos 116:565–577. doi:10.1111/j.2007.0030-1299.15488.x

    Article  CAS  Google Scholar 

  • Huitu O, Koivula M, Korpimäki E, Klemola T, Norrdahl K (2003) Winter food supply limits growth of northern vole populations in the absence of predation. Ecology 84:2108–2118

    Article  Google Scholar 

  • Ims RA, Rolstad J, Wegge P (1993) Predicting space use responses to habitat fragmentation: can voles Microtus oeconomus serve as an experimental model system (EMS) for capercaillie grouse Tetrao urogallus in boreal forest? Biol Conserv 63:261–268

    Article  Google Scholar 

  • Klemme I, Eccard JA, Ylönen H (2007) Why do female bank voles Clethrionomys glareolus mate multiply? Anim Behav 73:623–628

    Article  Google Scholar 

  • Korslund L, Steen H (2006) Small rodent winter survival: snow conditions limit access to food resources. J Anim Ecol 75:156–166. doi:10.1111/j.1365-2656.2005.01031.x

    Article  PubMed  Google Scholar 

  • Ludwig G, Alatalo RV, Helle P, Linden H, Lindstrom J, Siitari H (2006) Short- and long-term population dynamical consequences of asymmetric climate change in black grouse. Proc R Soc Lond B 273:2009–2016. doi:10.1098/rspb.2006.3538

    Article  Google Scholar 

  • MA (Millennium Ecosystem Assessment) (2005) Ecosystems and human well-being: biodiversity synthesis. World Resources Institute, Washington

    Google Scholar 

  • Millar JS, Gyug LW (1981) Initiation of breeding by northern Peromyscus in relation to temperature. Can J Zool 59:1094–1098

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2010).nlme: linear and nonlinear mixed effects models. R package version 3.1-97

  • R Development Core Team (2010). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/

  • Rolstad J (1991) Consequences of forest fragmentation for the dynamics of bird populations: conceptual issues and the evidence. Biol J Linn Soc 42:149–163

    Article  Google Scholar 

  • Smith JE, Batzli GO (2006) Dispersal and mortality of prairie voles (Microtus ochrogaster) in fragmented landscapes: a field experiment. Oikos 112:209–217. doi:10.1111/j.0030-1299.2006.13431.x

    Article  Google Scholar 

  • Stenseth NC (1985) Geographic distribution of Clethrionomys species. Ann Zool Fenn 22:215–219

    Google Scholar 

  • Stenseth NC, Mysterud A (2002) Climate, changing phenology, and other life history and traits: nonlinearity and match-mismatch to the environment. Proc Natl Acad Sci 99:13379–13381. doi:10.1073/pnas.212519399

    Article  PubMed  CAS  Google Scholar 

  • Viitala J, Hoffmeyer I (1985) Social organization in Clethrionomys compared with Microtus and Apodemus: social odours, chemistry and biological effects. Ann Zool Fenn 22:359–371

    Google Scholar 

  • Visser ME, van Noordwijk AJ, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc R Soc Lond B 265:1867–1870

    Article  Google Scholar 

  • von Blanckenhagen F, Eccard J, Ylönen H (2007) Animal protein as a reproductive constraint in spring reproduction of the bank vole. Ecoscience 14:323–329. doi:10.2980/1195-6860(2007)14[323:APAARC]2.0.CO;2

    Google Scholar 

  • Ylönen H, Mappes T, Viitala J (1990) Different demography of friends and strangers: an experiment on the impact of kinship and familiarity in Clethrionomys glareolus. Oecologia 83:333–337

    Google Scholar 

  • Ylönen H, Viitala J (1985) Social organization of an enclosed winter population of the bank vole Clethrionomys glareolus. Ann Zool Fenn 22:353–358

    Google Scholar 

  • Ylönen H, Kojola T, Viitala J (1988) Changing female spacing behaviour and demography in an enclosed breeding population of Clethrionomys glareolus. Holarct Ecol 11:286–292

    Google Scholar 

  • Ylönen H, Jacob J, Davies MJ, Singleton GR (2002) Predation risk and habitat selection of Australian house mice (Mus domesticus) during an incipient plague: desperate behaviour due to food depletion Oikos 99:285–290. doi:10.1034/j.1600-0706.2002.990208.x

  • Ylönen H, Eccard JA (2004) Does quality of winter food affect spring condition and breeding in; female bank voles (Clethrionomys glareolus)? Ecoscience 11:1–5

    Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

Download references

Acknowledgments

We thank technicians of the Konnevesi Research Station for helping with the food supplementation. Elina Puolakka and Lenka Trebaticka are thanked for their help with snowy trapping sessions. Janne Sundell, Lenka Trebaticka and Annika Opperbeckand Erlend Birkeland Nilsen gave valuable comments on the manuscripts. All the research and vole housing complied with Finnish law, and we recieved permission for animal experimentation at Jyväskylä University, no. 35/31.5.2004.

Author information

Authors and Affiliations

  1. Department of Biological and Environmental Science, Konnevesi Research Station, University of Jyväskylä, P.O. Box 35, 40014, Jyväskylä, Finland

    Marko Haapakoski & Hannu Ylönen

Authors
  1. Marko Haapakoski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hannu Ylönen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marko Haapakoski.

About this article

Cite this article

Haapakoski, M., Ylönen, H. Snow evens fragmentation effects and food determines overwintering success in ground-dwelling voles. Ecol Res 28, 307–315 (2013). https://doi.org/10.1007/s11284-012-1020-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-012-1020-y

Keywords

Search

Navigation