Skip to main content
Log in

Social organization of the voleClethrionomys rufocanus and its demographic and genetic consequences: A review

  • Special Feature
  • Published:
Researches on Population Ecology

Abstract

Recent findings on the relationship between social interaction and demographic process in the gray-sided voleClethrionomys rufocanus are reviewed with reference to the findings in other microtine rodents. Social behavior was particularly focused on spacing and dispersal, and their effects on population dynamics are discussed. Female territoriality can limit a population abundance as a density-dependent factor, although its regulatory effect is controversial. Female philopatry and male-biased dispersal should bring about the clumped distribution of female relatives and genetically random distribution of males during the breeding season. The sexual difference in dispersal patterns can contribute to the mating behavior of the vole; promiscuous mating and low frequency of incestuous mating. However, effects of social structure, including kinship, on reproduction and survival of individuals still remains to be clarified. Molecular markers may help to solve these issues and provide new field of population ecology in microtine rodents.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abe, H. (1976) Population structure and reproductive activity ofClethrionomys rufocanus bedfordiae (Thomas) in a wind shelterbelt of the Ishikari Plain, Hokkaido.Journal of the Mammalogical Society of Japan 7: 17–30.

    Google Scholar 

  • Berger, P. J., N. C. Negus and M. Day (1987) Recognition of kin and avoidance of inbreeding in the montane vole,Microtus montanus.Journal of Mammalogy 78: 1182–1186.

    Google Scholar 

  • Berteaux, D., J.-M. Bergeron, D. W. Thomas and H. Lapierre (1996) Solitude versus gregariousness: do physical benefits drive the choice in overwintering meadow voles?Oikos 76: 330–336.

    Google Scholar 

  • Bjornstad, O. N., S. Champely, N. C. Stenseth and T. Saitoh (1996) Cyclicity and stability of grey-sided voles,Clethrionomys rufocanus, of Hokkaido: spectral and principal components analyses.Philosophical Transactions of the Royal Society of London B 351: 867–875.

    Google Scholar 

  • Bjørnstad, O. N., N. C. Stenseth and T. Saitoh (1998a) Synchrony and scaling in dynamics of voles and mice in northern Japan.Ecology (in press).

  • Bjornstad, O. N., H. P. Andreassen and R. A. Ims (1998b) Effects of habitat patchness and connectivity on the spatial ecology of the root voleMicrotus oeconomus.Journal of Animal Ecology 67: 127–140.

    Google Scholar 

  • Bondrup-Nielsen, S. (1986) Investigation of spacing behaviour ofClethrionomys gapperi by experimentation.Journal of Animal Ecology 55: 269–280.

    Google Scholar 

  • Bondrup-Nielsen, S. and F. Karlsson (1985) Movements and spatial patterns in populations ofClethrionomys species: a review.Annales Zoologici Fennici 22: 385–392.

    Google Scholar 

  • Boonstra, R. (1989) Life history variation in maturation in fluctuating meadow vole populations (Microtus pennsylvanicus).Oikos 54: 265–274.

    Google Scholar 

  • Boonstra, R. and F. H. Rodd (1983) Regulation of breeding density inMicrotus pennsylvanicus.Journal of Animal Ecology 52: 757–780.

    Google Scholar 

  • Boonstra, R. and I. Hogg (1988) Friends and strangers: a test of the Charnov-Finerty Hypothesis.Oecologia 77: 95–100.

    Google Scholar 

  • Boonstra, R., C. J. Krebs, M. S. Gaines, M. L. Johnson and I. T. M. Craine (1987) Natal philopatry and breeding systems in voles (Microtus spp.).Journal of Animal Ecology 56: 655–673.

    Google Scholar 

  • Bowen, B. S. (1982) Temporal dynamics of microgeographic structure of genetic variation inMicrotus californicus.Journal of Mammalogy 63: 625–638.

    Google Scholar 

  • Boyd, S. K. and A. R. Blaustein (1985) Familiarity and inbreeding avoidance in the gray-tailed vole (Microtus canicaudus).Journal of Mammalogy 66: 348–352.

    Google Scholar 

  • Bujalska, G. (1970) Reproduction stabilizing elements in an island population ofClethrionomys glareolus (Schreber, 1780).Acta Theriologica 15: 381–412.

    Google Scholar 

  • Bujalska, G. (1973) The role of spacing behavior among females in the regulation of reproduction in the bank vole.Journal of Reproduction and Fertility 19 Supplement: 465–474.

    Google Scholar 

  • Bujalska, G. (1975) Reproduction and mortality of bank voles and the changes in the size of an island population.Acta Theriologica 20: 41–56.

    PubMed  CAS  Google Scholar 

  • Bujalska, G. (1985) Regulation of female maturation inClethrionomys species, with special reference to an island population ofC. glareolus.Annales Zoologici Fennici 22: 331–342.

    Google Scholar 

  • Bujalska, G. (1995a) Peak numbers ofClethrionomys glareolus (Schreber, 1780) and the mechanisms involved.Polish Ecological Studies 21: 397–411.

    Google Scholar 

  • Bujalska, G. (1995b) Winter survival in an island population of the bank vole.Polish Ecological Studies 21: 423–433.

    Google Scholar 

  • Bujalska, G. and L. Griim (1989) Social organization of the bank vole (Clethrionomys glareolus, Schreber 1780): a model.Oecologia 80:70–81.

    Google Scholar 

  • Burrough, P. A. (1995) Spatial aspects of ecological data. pp. 213–251.In R. H. G. Jongman, C. ter Braak, J. F. and O. F. R. van Tongeren (eds.)Data analysis in community and landscape ecology. Cambridge University Press, New York.

    Google Scholar 

  • Charlesworth, B.D., M. T. Morgan and B. Charlesworth (1993) Mutation accumulation in finite outbreeding and inbreeding population.Genetical Research 61: 39–56.

    Google Scholar 

  • Clarke, J. R. and F. V. Clulow (1973) The effect of successive mating upon bank vole (Clethrionomys glareolus) and vole (Microtus agrestis) ovaries. pp. 160–170.In H. Peters (ed.)The development and maturation of the ovary and its functions. Excerpta Medica Int. Congr. Ser., Amsterdam (cited in Clulow et al. 1982).

    Google Scholar 

  • Chepko-Sade, B. D. and Z. T. Halpin (1987)Mammalian Dispersal Patterns. The University of Chicago Press, Chicago.

    Google Scholar 

  • Clulow, F. V., E. A. Franchetto and P. E. Langford (1982) Pregnancy failure in the red-backed vole,Clethrionomys gapperi.Journal of Mammalogy 63: 499–500.

    Google Scholar 

  • Clutton-Brock, T. H. (1989) Female transfer and inbreeding avoidance in social mammals.Nature 337: 70–72.

    PubMed  CAS  Google Scholar 

  • Cockburn, A. (1988)Social behaviour in fluctuating populations. Croom Helm, London.

    Google Scholar 

  • Cockburn, A., M. P. Scott and D. J. Scotts (1985) Inbreeding avoidance and male-biased natal dispersal inAntechinus spp. (Marsupialia: Dasyuridae).Animal Behaviour 33: 908–915.

    Google Scholar 

  • dos Santos, E. M., H. P. Andreassen and R. A. Ims (1995) Differential inbreeding tolerance in two geographically distinct strains of root volesMicrotus oeconomus.Ecography 18: 238–247.

    Google Scholar 

  • Dewa, H. (1975) Seasonal variation of daily activity rhythms in snow season.Research Bulletin of College Experimental Forests Hokkaido University 22: 105–120 (in Japanese with English summary).

    Google Scholar 

  • Dobson, F. S. (1982) Competition for mates and predominant juvenile male dispersal in mammals.Animal Behaviour 30: 1183–1192.

    Google Scholar 

  • Ferkin, M. H. (1988) The effect of familiarity on social interactions in meadow voles,Microtus pennsylvanicus: a laboratory and field study.Animal Behaviour 36: 1816–1822.

    Google Scholar 

  • Ferkin, M. H. (1990) Kin recognition and social behavior in microtine rodents. pp. 11–24.In R. H. Tamarin, R. S. Ostfeld, S. R. Pugh and G. Bujalska (eds.)Social systems and population cycles in voles. Birkhäuser Verlag, Basel.

    Google Scholar 

  • Ferkin, M. H. and T. F. Rutka (1990) Mechanisms of sibling recognition in meadow voles.Canadian Journal of Zoology 68: 609–613.

    Google Scholar 

  • Frank, F. (1957) The causality of microtine cycles in Germany.Journal of Wildlife Management 21: 113–121.

    Google Scholar 

  • Gaines, M. S. and L. R. McClenaghan, Jr. (1980) Dispersal in small mammals.Annual Reviews of Ecology and Systematics 11: 163–196.

    Google Scholar 

  • Gaines, M.S., C. L. Baker and A. M. Vivas (1979) Demographic attributes of dispersing southern bog lemmings (Synaptomys cooperi) in eastern Kansas.Oecologia 40: 91–101.

    Google Scholar 

  • Gavish, L., J. E. Hofmann and L. L. Getz (1984) Sibling recognition in the prairie vole,Microtus ochrogaster.Animal Behaviour 32: 362–366.

    Google Scholar 

  • Getz, L. L., B. McGuire, T. Pizzuto, J. E. Hofmann and B. Frase (1993) Social organization of the prairie vole (Microtus ochrogaster).Journal of Mammalogy 74: 44–58.

    Google Scholar 

  • Gilbert, B. S., C. J. Krebs, D. Talarico and D. B. Cichowski (1986) DoClethrionomys rutilus females suppress maturation of juvenile females?Journal of Animal Ecology 55: 543–552.

    Google Scholar 

  • Gliwicz, J. (1989) Individuals and populations of the bank vole in optimal, suboptimal and insular habitats.Journal of Animal Ecology 58: 237–247.

    Google Scholar 

  • Hamilton, W. D. (1964) The genetical evolution of social behavior. I and II.Journal of theoretical Biology 7: 1–52.

    PubMed  CAS  Google Scholar 

  • Hayes, J. P., J. R. Speakman and P. A. Racey (1992) The contributions of local heating and reducing exposed surface area to the energetic benefits of huddling by short-tailed field voles (Microtus agrestis).Physiological Zoology 65: 742–762.

    Google Scholar 

  • Heske, E. J. and S. Bundrup-Nielsen (1990) Why spacing behaviour does not stabilize density in cyclic populations of microtine rodents.Oecologia 83: 91–98.

    Google Scholar 

  • Hestbeck, J. B. (1982) Population regulation of cyclic mammals: the social fence hypothesis.Oikos 39: 157–163.

    Google Scholar 

  • Hewitt, G. M. and R. K. Butlin (1997) Causes and consequences of population structure. pp. 456.In J. R. Krebs and N. B. Davies (eds.)Behavioural ecology. An evolutionary approach, 4th edn. Blackwell Science, Oxford.

    Google Scholar 

  • Hinde, R. A. (1956) The biological significance of the territories of birds.Ibis 98: 340–369.

    Google Scholar 

  • Ims, R. A. (1987a) Male spacing systems in microtine rodents.American Naturalist 130: 475–484.

    Google Scholar 

  • Ims, R. A. (1987b) Responses in spatial organization and behaviour to manipulations of the food resource in the voleClethrionomys rufocanus.Journal of Animal Ecology 56: 585–596.

    Google Scholar 

  • Ims, R. A. (1988) Spatial clumping of sexually receptive females induces space sharing among male voles.Nature 335: 541–543.

    PubMed  CAS  Google Scholar 

  • Ims, R. A. (1989) Kinship and origin effects on dispersal and space sharing inClethrionomys rufocanus.Ecology 70: 607–616.

    Google Scholar 

  • Ims, R. A. (1990) Determinants of natal dispersal and space use in grey-sided voles,Clethrionomys rufocanus: a combined field and laboratory experiment.Oikos 57: 106–113.

    Google Scholar 

  • Ims, R. A. (1994) Litter sex ratio variation in laboratory colonies of two geographically distinct strains of the root voleMicrotus oeconomus.Ecography 17: 141–146.

    Google Scholar 

  • Ims, R. A. (1997) Determinants of geographic variation in growth and reproductive traits in the root vole.Ecology 78: 461–470.

    Google Scholar 

  • Ims, R. A. and H. P. Andreassen (1991) Does kinship influence space use and dispersal in male grey-sided voles?Oikos 62: 216–220.

    Google Scholar 

  • Ishibashi, Y., T. Saitoh, S. Abe and M.C. Yoshida (1995) Polymorphic microsatellite DNA markers in the grey red-backed voleClethrionomys rufocanus bedfordiae.Molecular Ecology 4: 127–128.

    PubMed  CAS  Google Scholar 

  • Ishibashi, Y., T. Saitoh, S. Abe and M. C. Yoshida (1997) Sex-related spatial kin structure in a spring population of grey-sided volesClethrionomys rufocanus as revealed by mitochondrial and microsatellite DNA analyses.Molecular Ecology 6: 63–71.

    PubMed  CAS  Google Scholar 

  • Ishibashi, Y., T. Saitoh, S. Abe and M. C. Yoshida (1998) Kinrelated social organization in a winter population of the voleClethrionomys rufocanus.Researches on Population Ecology 40:51–59.

    Google Scholar 

  • Itô, Y. (1978)Comparative ecology, 2nd edn. Iwanami-shoten, Tokyo (in Japanese). English version (edited and translated by J. Kikkawa) was published in 1980. Cambridge University Press, Cambridge.

  • Kalela, O. (1957) Regulation of reproduction rate in subarctic populations of the voleClethrionomys rufocanus (Sund.).Annales Academiae Scientiarum Fennicae, Series A IV, Biologica 34: 1–60.

    Google Scholar 

  • Kaneko, Y., K. Nakata, T. Saitoh, N. C. Stenseth and O. N. Bjørnstad (1998) The biology of the voleClethrionomys rufocanus: a review.Researches on Population Ecology 40: 21–37.

    Google Scholar 

  • Karlsson, A. F. (1988) Social organization of a low density spring population of the bank vole,Clethrionomys glareolus.Oikos 52: 19–26.

    Google Scholar 

  • Kawata, M. (1985a) Mating system and reproductive success in a spring population of the red-backed vole,Clethrionomys rufocanus bedfordiae.Oikos 45: 181–190.

    Google Scholar 

  • Kawata, M. (1985b) Sex differences in the spatial distribution of genotypes in the red-backed vole,Clethrionomys rufocanus bedfordiae.Journal of Mammalogy 66: 384–387.

    Google Scholar 

  • Kawata, M. (1987) Pregnancy failure and suppression by female-female interaction in enclosed populations of the red-backed vole,Clethrionomys rufocanus bedfordiae.Behavioral Ecology and Sociobiology 20: 89–97.

    Google Scholar 

  • Kawata, M. (1988) Mating success, spatial organization, and male characteristics in experimental field populations of the red-backed vole,Clethrionomys rufocanus bedfordiae.Journal of Animal Ecology 57: 217–235.

    Google Scholar 

  • Kawata, M. (1989) Growth and dispersal timing in male red-backed volesClethrionomys rufocanus bedfordiae.Oikos 54: 220–226.

    Google Scholar 

  • Kawata, M. (1990) Fluctuating populations and kin interaction in mammals.Trends in Ecology and Evolution 5: 17–20.

    Google Scholar 

  • Kawata, M. (1997) Exploitative competition and ecological effective abundance.Ecological Modelling 94: 125–137.

    Google Scholar 

  • Koskela, E., T. Mappes and H. Ylönen (1997) Territorial behaviour and reproductive success of bank voleClethrionomys glareolus females.Journal of Animal Ecology 66: 341–349.

    Google Scholar 

  • Krebs, J. R. (1971) Territory and breeding density in the great tit,Parus major L.Ecology 52: 1–22.

    Google Scholar 

  • Krebs, J. R. and N. B. Davies (1987)An introduction to behavioural ecology, 2nd edn. Blackwell Scientific Publications, Oxford.

    Google Scholar 

  • Krebs, C. J. (1996) Population cycles revisited.Journal of Mammalogy 77: 8–24.

    Google Scholar 

  • Lacy, R. C. (1997) Importance of genetic variation to the viability of mammalian populations.Journal of Mammalogy 78: 320–335.

    Google Scholar 

  • Lambin, X. (1994) Natal philopatry, competition for resources, and inbreeding avoidance in Townsend’s voles (Microtus townsendii).Ecology 75: 224–235.

    Google Scholar 

  • Lambin, X. and C. J. Krebs (1991a) Spatial organization and mating systemof Microtus townsendii.Behavioral Ecology and Sociobiology 28: 353–363.

    Google Scholar 

  • Lambin, X. and C. J. Krebs (1991b) Can changes in female relatedness influence microtine population dynamics?Oikos 61: 126–132.

    Google Scholar 

  • Lambin, X. and C. J. Krebs (1993) Influence of female relatedness on the demography of Townsend’s vole populations in spring.Journal of Animal Ecology 62: 536–550.

    Google Scholar 

  • Lambin, X. and C. Mathers (1997) Dissipation of kin discrimination in Orkney voles,Microtus arvalis orcadensis: a laboratory study.Annales Zoologici Fennici 34: 23–30.

    Google Scholar 

  • Lambin, X. and N. G. Yoccoz (1998) The impact of population kin-structure on nestling survival in Townsend’s voles,Microtus townsendii.Journal of Animal Ecology 67: 1–16.

    Google Scholar 

  • Lande, R. (1994) Risk of population extinction from new deleterious mutations.Evolution 48: 1460–1469.

    Google Scholar 

  • Lidicker, W. Z., Jr. (1985) Dispersal. pp. 420–454.In R. H. Tamarin (ed.)Biology of New World Microtus. The American Society of Mammalogists, No. 8.

  • Lynch, M., J. Conery and R. Bürger (1995) Mutation meltdowns in sexual populations.Evolution 48: 1067–1080.

    Google Scholar 

  • Madison, D. M. (1984) Group nesting and its ecological and evolutionary significance in overwintering microtine rodents. pp. 267–274.In J. F. Merritt (ed.)Winter ecology of small mammals. Carnegie Museum of Natural History, Pittsburgh.

    Google Scholar 

  • Madison, D. M. (1985) Activity rhythms and spacing. pp. 373–418.In R. H. Tamarin (ed.)Biology of New World Microtus. The American Society of Mammalogists, No. 8.

  • Madison, D. M. and W. J. McShea (1987) Seasonal changes in reproductive tolerance, spacing, and social organization in meadow voles: a microtine model.American Zoologist 27: 899–908.

    Google Scholar 

  • Madison, D. M., R. W. FitzGerald and W. J. McShea (1984) Dynamics of social nesting in overwintering meadow voles (Microtus pennsylvanicus): possible consequences for population cycling.Behavioral Ecology and Sociobiology 15: 9–17.

    Google Scholar 

  • Mappes, T., H. Ylönen and J. Viitala (1995) Higher reproductive success among kin groups of bank voles (Clethrionomys glareolus).Ecology 76: 1276–1282.

    Google Scholar 

  • Maruyama, T. and M. Kimura (1980) Genetic variability and effective population size when local extinction and recolonization of subpopulations are frequent.Proceedings of the National Academy of Sciences of the USA 77: 6710–6714.

    PubMed  Google Scholar 

  • Mazurkiewicz, M. and E. Rajska (1975) Dispersion of young bank voles form their place of birth.Acta Theriologica 20: 71–81.

    Google Scholar 

  • McGuire, B. and L. L. Getz (1995) Communal nesting in prairie voles (Microtus ochrogaster): an evaluation of costs and benefits based on patterns of dispersal and settlement.Canadian Journal of Zoology 73: 383–391.

    Google Scholar 

  • McShea, W. J. (1990) Social tolerance and proximate mechanisms of dispersal among winter groups of meadow voles,Microtus pennsylvanicus.Animal Behaviour 39: 346–351.

    Google Scholar 

  • Morse, D. H. (1980)Behavioral mechanism in ecology. Harvard University Press, Cambridge.

    Google Scholar 

  • Nakata, K. (1989) Regulation of reproduction rate in a cyclic population of the red-backed vole,Clethrionomys rufocanus bedfordiae.Researches on Population Ecology 31: 185–209.

    Google Scholar 

  • Ostfeld, R. S. (1985) Limiting resources and territoriality in microtine rodents.American Naturalist 126: 1–15.

    Google Scholar 

  • Ostfeld, R. S. (1990) The ecology of territoriality in small mammals.Trends in Ecology and Evolution 5: 411–415.

    Google Scholar 

  • Ostfeld, R. S. (1992) Do changes in female relatedness determine demographic patterns in microtine rodents?Oikos 65: 531–534.

    Google Scholar 

  • Ostfeld, R. S. and L. L. Klosterman (1990) Microtine social systems, Actaptation, and the comparative method. pp. 35–44.In R. H. Tamarin, R. S. Ostfeld, S. R. Pugh and G. Bujalska (eds.)Social systems and population cycles in voles. Birkhäuser Verlag, Basel.

    Google Scholar 

  • Ostfeld, R. S. and C. D. Canham (1995) Density-dependent process in meadow voles: an experimental approach.Ecology 76: 521–532.

    Google Scholar 

  • Ota, K. (1984)Study on wild murid rodents in Hokkaido. Hokkaido University Press, Sapporo.

    Google Scholar 

  • Petrusewicz, K., G. Bujalska, R. Andrzejewski and J. Gliwicz (1971) Productivity processes in an island population ofClethrionomys glareolus.Annales Zoologici Fennici 8: 127–132.

    Google Scholar 

  • Petrusewicz, K., A. Górecki, W. Grodziński and J. Kozlowski (1983) Productivity and energetics.Acta Theriologica 28 Supplement1: 173–205.

    Google Scholar 

  • Plante, Y., P. T. Boag and B. N. White (1989) Microgeographic variation in mitochondrial DNA of meadow voles (Microtus pennsylvanicus) in relation to population density.Evolution 43: 1522–1537.

    Google Scholar 

  • Pugh, S. R. and R. H. Tamarin (1988) Inbreeding in a population of meadow voles,Microtus pennsylvanicus.Canadian Journal of Zoology 66: 1831–1834.

    Google Scholar 

  • Pugh, S. R. and R. H. Tamarin (1990) A test of the Charnov and Finerty hypothesis of population regulation in meadow voles. pp. 111–120.In R. H. Tamarin, R. S. Ostfeld, S. R. Pugh and G. Bujalska (eds.)Social systems and population cycles in voles. Birkhäuser Verlag, Basel.

    Google Scholar 

  • Pusey, A. E. (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals.Trends in Ecology and Evolution 2: 295–299.

    Google Scholar 

  • Pusey, A. and M. Wolf (1996) Inbreeding avoidance in animals.Trends in Ecology and Evolution 11: 201–206.

    Google Scholar 

  • Robertson, G. P. (1987) Geostatistics in ecology: interpolating with known variance.Ecology 68: 744–748.

    Google Scholar 

  • Saitoh, T. (1981) Control of female maturation in high density populations of the red-backed vole,Clethrionomys rufocanus bedfordiae.Journal of Animal Ecology 50: 79–87.

    Google Scholar 

  • Saitoh, T. (1985) Practical definition of territory and its application to the spatial distribution of voles.Journal of Ethology 3: 143–149.

    Google Scholar 

  • Saitoh, T. (1989a) Communal nesting and spatial structure in an early spring population of the grey red-backed vole,Clethrionomys rufocanus bedfordiae.Journal of the Mammalogical Society of Japan 14: 27–41.

    Google Scholar 

  • Saitoh, T. (1989b) Effects of added food on some attributes of an enclosed vole population.Journal of Mammalogy 70: 772–782.

    Google Scholar 

  • Saitoh, T. (1990) Lifetime reproductive success in reproductively suppressed female voles.Researches on Population Ecology 32: 391–406.

    Google Scholar 

  • Saitoh, T. (1991) The effects and limits of territoriality on population regulation in grey red-backed voles,Clethrionomys rufocanus bedfordiae.Researches on Population Ecology 33: 367–386.

    Google Scholar 

  • Saitoh, T. (1995) Sexual differences in natal dispersal and philopatry of the grey-sided vole.Researches on Population Ecology 37: 49–57.

    Google Scholar 

  • Saitoh, T., N. C. Stenseth and O. N. Bjørnstad (1997) Density dependence in fluctuating grey-sided vole populations.Journal of Animal Ecology 66: 14–24.

    Google Scholar 

  • Saitoh, T., O. N. Bjørnstad and N. C. Stenseth (1998a) Densitydependence in voles and mice: a comparative study.Ecology (in press).

  • Saitoh, T., N. C. Stenseth and O. N. Bjørnstad (1998b) The population dynamics of the grey-sided vole,Clethrionomys rufocanus, in Hokkaido.Researches on Population Ecology 40: 61–76.

    Google Scholar 

  • Salvioni, M. and W. Z. Lidicker, Jr. (1995) Social organization and space use in California voles: seasonal, sexual, and age-specific strategies.Oecologia 101: 426–438.

    Google Scholar 

  • Sera, W. E. and M. S. Gaines (1994) The effect of relatedness on spacing behavior and fitness of female prairie voles.Ecology 75: 1560–1566.

    Google Scholar 

  • Shield, W. M. (1993) The natural and unnatural history of inbreeding and outbreeding. pp. 143–169.In N. W. Thornhill (ed.)The natural history of inbreeding and outbreeding. The University of Chicago Press, Chicago.

    Google Scholar 

  • Smith, A. T. (1993) The natural history of inbreeding and outbreeding in small mammals. pp. 329–351.In N. W. Thornhill (ed.)The natural history of inbreeding and outbreeding. The University of Chicago Press, Chicago.

    Google Scholar 

  • Stacy, J. E., P. E. Jorde, H. Steen, R. A. Ims, A. Purvis and K. S. Jakobsen (1997) Lack of concordance between mtDNA gene flow and population density fluctuations in the bank vole.Molecular Ecology 6: 751–759.

    PubMed  CAS  Google Scholar 

  • Steen, H. (1994) Low survival of long distance dispersers of the root vole (Microtus oeconomus).Annales Zoologici Fennici 31: 271–274.

    Google Scholar 

  • Steen, H., R. A. Ims and G. A. Sonerud (1996) Spatial and temporal patterns of small-rodent population dynamics at a regional scale.Ecology 77: 2365–2372.

    Google Scholar 

  • Stenseth, N. C. (1985a) Geographic distribution ofClethrionomys species.Annales Zoologici Fennici 22: 215–219.

    Google Scholar 

  • Stenseth, N. C. (1985b) Models of bank vole and wood mouse populations.Symposium of the Zoological Society of London 55: 339–376.

    Google Scholar 

  • Stenseth, N. C. (1985c) Population dynamics consequences of female territoriality in bank voles.Acta Theriologica 28: 445–460.

    Google Scholar 

  • Stenseth, N. C. and R. A. Ims (1993) Population dynamics of lemmings: temporal and spatial variation — an introduction. pp. 61–96.In N. C. Stenseth and R. A. Ims (eds.)The biology of lemmings. Academic Press, London.

    Google Scholar 

  • Stenseth, N. C., O. N. Bjørnstad and W. Falck (1996a) Is spacing behaviour coupled with predation causing the microtine density cycle? A synthesis of current process-oriented and pattern-oriented studies.Proceedings of the Royal Society of London B 263: 1423–1435.

    CAS  Google Scholar 

  • Stenseth, N. C., O. N. Bjørnstad and T. Saitoh (1996b) A gradient from stable to cyclic populations ofClethrionomys rufocanus in Hokkaido, Japan.Proceedings of the Royal Society of London B 263: 1117–1126.

    CAS  Google Scholar 

  • Stenseth, N. C., O. N. Bjørnstad and T. Saitoh (1998) Seasonal forcing on the dynamics ofClethrionomys rufocanus: modeling geographic gradients in population dynamics.Researches on Population Ecology 40: 85–95.

    Google Scholar 

  • Stickel, F. (1954) A comparison of certain methods of measuring ranges of small mammals.Journal of Mammalogy 35: 1–15.

    Google Scholar 

  • Stockley, P., J. B. Searle, D. W. Macdonald and C. S. Jones (1993) Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding.Proceedings of the Royal Society of London B 254: 173–179.

    CAS  Google Scholar 

  • Taitt, M. J. and C. J. Krebs (1985) Population dynamics and cycles. pp. 567–620.In R. H. Tamarin (ed.)Biology of New World Microtus. The American Society of Mammalogists, Special Publication No. 8.

  • Tanaka, R. (1953) Home range and territories inClethrionomys population on a peat-bog grassland in Hokkaido.Bulletin of Kochi Women’s College 2: 10–20.

    Google Scholar 

  • Trivers, R. (1985)Social evolution. Benjamin/Cummings Publishing Company, Menlo Park.

    Google Scholar 

  • Viitala, J. (1977) Social organization in cyclic subarctic populations of the volesClethrionomys rufocanus (Sund.) andMicrotus agrestis (L.).Annales Zoologici Fennici 14: 53–93.

    Google Scholar 

  • Viitala, J. and I. Hoffmeyer (1985) Social organization inClethrionomys compared withMicrotus andApodemus: Social odours, chemistry and biological effects.Annales Zoologici Fennici 22: 359–371.

    Google Scholar 

  • Watson, A. and R. Moss (1970) Dominance, spacing behaviour and aggression in relation to population limitation in vertebrates. pp. 167–218.In A. Watson (ed.)Animal populations in relation to their food resources. Blackwell Scientific Publications, Oxford.

    Google Scholar 

  • Webster, A. B. and R. J. Brooks (1981) Social behavior ofMicrotus pennsylvanicus in relation to seasonal changes in demography.Journal of Mammalogy 62: 738–751.

    Google Scholar 

  • West, S. D. and H. T. Dublin (1984) Behavioral strategies of small mammals under winter conditions: solitary or social? pp. 293–298.In J. F. Merritt (ed.)Winter ecology of small mammals. Carnegie Museum of Natural History, Pittsburgh.

    Google Scholar 

  • Wilson, D. S., G. B. Pollock and L. A. Dugatkin (1992) Can altruism evolve in purely viscous populations?Evolutionary Ecology 6: 331–341.

    Google Scholar 

  • Wilson, E. O. (1975)Sociobiology, the new synthesis. Harvard University Press, Cambridge.

    Google Scholar 

  • Wolff, J. O. (1993a) Why are female small mammals territorial?Oikos 68: 364–370.

    Google Scholar 

  • Wolff, J. O. (1993b) What is the role of adults in mammalian juvenile dispersal?Oikos 68: 173–176.

    Google Scholar 

  • Wolff, J. O. (1995) Friends and strangers in vole population cycles.Oikos 73: 411–414.

    Google Scholar 

  • Wolff, J. O. (1997) Population regulation in mammals: an evolutionary perspective.Journal of Animal Ecology 66: 1–13.

    Google Scholar 

  • Wolff, J. O. and W. Z. Lidicker, Jr. (1981) Communal winter nesting and food sharing in taiga voles.Behavioral Ecology and Sociobiology 9: 237–240.

    Google Scholar 

  • Wolff, J. O. and D. M. Cicirello (1991) Comparative paternal and infanticidal behavior of sympatric white-footed mice (Peromyscus leucopus noveboracensis) and deermice (P. maniculatus nubiterrae).Behavioral Ecology 2: 38–45.

    Google Scholar 

  • Wolff, J. O. and E. M. Schauber (1996) Space use and juvenile recruitment in gray-tailed voles in response to intruder pressure and food abundance.Acta Theriologica 41: 35–43.

    Google Scholar 

  • Ylönen, H. and J. Viitala (1987) Social organization and habitat use of introduced populations of the voleClethrionomys rufocanus (Sund) in Central Finland.Zeitschrift für Säugetierkunde 52: 354–363.

    Google Scholar 

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

    Google Scholar 

  • Yoccoz, N. G., K. Nakata, N. C. Stenseth and T. Saitoh (1998) The demography ofClethrionomys rufocanus: from mathematical and statistical models to further field studies.Researches on Population Ecology 40: 107–121.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yasuyuki Ishibashi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ishibashi, Y., Saitoh, T. & Kawata, M. Social organization of the voleClethrionomys rufocanus and its demographic and genetic consequences: A review. Res Popul Ecol 40, 39–50 (1998). https://doi.org/10.1007/BF02765220

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02765220

Key words

Navigation