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Breeding suppression in the bank vole as antipredatory adaptation in a predictable environment

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Summary

In northern Fennoscandia, microtine rodent populations fluctuate cyclically. The environment of an individual vole can be considered to be predictable when the risks of predation and intra- and interspecific competition change with the cycle, such that both are high during the population highs of voles. The risk of predation is also high during the vole crash. After the crash, the vole population is characterized by low intra- and interspecific competition and low predation pressure. The main predators affecting voles during the crash are the small mustelids, least weasel and stoat. The density of these specialist predators declines drastically during the winter after the vole crash. We studied experimentally the impact of the perceived presence of stoats on the breeding and mating behaviour of voles. In a series of breeding experiments with bank voles,Clethrionomys glareolus, both old and young females suppressed breeding when exposed to the odour of stoats,Mustela erminea. The weights of females decreased in both experimental and control groups, but more among the voles under odour exposition. It seems that females actively avoided copulations under high predation risk and that breeding suppression is mediated by a change in female mating behaviour. There was no change in male behaviour or physical condition between the experimental and control treatments. An alternative mechanism for the observed breeding suppression could be the one caused by decreased feeding in females mediated with low energy intake which does not allow breeding. Regardless of its mechanism, delay of breeding should increase the probability of non-breeding females to survive to the next breeding season. The females surviving the crash should gain a strong selective advantage in a predator-free environment of the subsequent breeding season, which could explain the adaptive function of this antipredatory strategy.

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References

  • Abrahams, M.V. and Dill, L.M. (1989) A determination of the energetic equivalence of the risk of predation.Ecology 70, 999–1007.

    Google Scholar 

  • Bondrup-Nielsen, S. and Ims, R.A. (1986) Reproduction and spacing behaviour of females in a peak density population ofClethrionomys glareolus.Holact. Ecol. 9, 109–12.

    Google Scholar 

  • Brown, J.S. (1988) Patch use as an indicator of habitat preference, predation risk, and competition.Behav. Ecol Soc. 22, 37–47.

    Google Scholar 

  • Brown, J.S., Kotler, B.P., Smith, R.J. and Wirz, W.O. II (1988) The effect of owl predation on the foraging behaviour of heteromyid rodents.Oecologia 76, 408–15.

    Google Scholar 

  • Bruce, H.M. (1959) An exteroceptive block to pregnancy in the mouse.Nature 184, 105.

    PubMed  Google Scholar 

  • Bujalska, G. (1973) The role of spacing behaviour among females in the regulation of reproduction in the bank vole.J. Reprod. Fertil. Suppl. 19, 465–74.

    PubMed  Google Scholar 

  • Calder, C.J. and Gorman, M.L. (1991) The effects of red foxVulpes vulpes faecal odours on the feeding behaviour of Orkney volesMicrotus arvalis.J. Zool. 224, 599–606.

    Google Scholar 

  • Cassini, M.H. (1991) Foraging under predation risk in the wild guinea pigCavia aperea.Oikos 61, 1–6.

    Google Scholar 

  • Crowl, T.A. and Cowich, A.P. (1990) Predator-induced life-history shifts in a freshwater snail.Science 247, 949–51.

    Google Scholar 

  • Cushing, B.S. (1984) A selective preference by least weasels for oestrous versus dioestrous urine of prairie deer mice.Anim. Behav. 32, 1263–5.

    Google Scholar 

  • Cushing, B.S. (1985) Estrous mice and vulnerability to weasel predation.Ecology,66, 1976–8.

    Google Scholar 

  • Endler, J.A. (1987) Predation, light intesity and courtship behaviour inPoecilia reticulata (Pisces: Poeciliidae).Anim. Behav. 35, 1376–85.

    Google Scholar 

  • Getz, L.L., Dluzen, D. and McDermott, J.L. (1983) Suppression of reproductive maturation in malesimulated virgin femaleMicrotus by a female urinary chemosignal.Behav. Processes 8, 59–64.

    Google Scholar 

  • Hanski, I., Hansson, L. and Henttonen, H. (1991) Specialist predators, generalist predators, and the microtine rodent cycle.J. Anim. Ecol. 60, 353–67.

    Google Scholar 

  • Hanski, I., Turchin, P., Korpimäki, E. and Henttonen, H. (1993) Population oscillations of boreal rodents: regulation by mustelid predators leads to chaos.Nature 364, 232–5.

    PubMed  Google Scholar 

  • Hansson, L. and Henttonen, H. (1988) Rodent dynamics as community process.Trends Ecol. Evol 3, 195–200.

    Google Scholar 

  • Heikkilä, J., Kaarsalo, K., Mustonen, O. and Pekkarinen, P. (1993) Influence of predation risk on early development and maturation in three species ofClethrionomys voles.Ann. Zool. Fennici 30, 153–161.

    Google Scholar 

  • Henttonen, H., Oksanen, T., Jortikka, A. and Haukisalmi, V. (1987) How much do weasels shape microtine cycles in the northern Fennoscandian taiga?Oikos 50, 353–65.

    Google Scholar 

  • Huntingford, F.A. (1984) Some ethical issues raised by studies of predation and aggression.Anim. Behav. 32, 210–15. Appendix added 1992.

    Google Scholar 

  • Ims, R.A. (1988) Spatial clumping of sexually receptive females induces space sharing among male voles.Nature 335, 541–3.

    PubMed  Google Scholar 

  • Jedrzejewski, W. and Jedrzejewska, B. (1990) Effect of a predator's visit on the spatial distribution of bank voles: experiments with weasels.Can. J. Zool. 68, 660–6.

    Google Scholar 

  • Kaarsalo, K. and Wallgren, H. (1989) Inhibition of pregnancy and its effects on ovarian follicles inClethrionomys rutilus females exposed to conspecific males and to males ofC. rufocanus. Fifth International Theriological Congress, Rome, 1989, Abstracts, p. 572.

  • Kaczmarski, F. (1966) Bioenergetics of pregnancy and lactation in the bank vole.Acta Theriol. 11, 409–17.

    Google Scholar 

  • Koponen, T. (1970) Age structure in sedentary and migratory populations of the Norwegian lemming,Lemmus lemmus (L.), at Kilpisjärvi in 1960.Ann. Zool. Fenn. 7, 141–87.

    Google Scholar 

  • Korpimäki, E., Norrdahl, K. and Rinta—Jaskari, T. (1991) Response of stoats and least weasels to fluctuating food abundances: is the low phase of the vole cycle due to mustelid predation?Oecologia 88, 552–61.

    Google Scholar 

  • Kotler, B.P., Brown, J.S., Slotow, R.H., Goodfriend, W.L. and Strauss, M. (1993) The influence of snakes on the foraging behaviour of gerbils.Oikos 67, 309–16.

    Google Scholar 

  • Lima, S.L. and Dill, L.M. (1990) Behavioural decisions made under the risk of predation: a review and prospectus.Can. J. Zool. 68, 619–40.

    Google Scholar 

  • Lima, S.L., Valone, T.J. and Caraco, T. (1985) Foraging efficiency — predation risk trade-off in the gray squirrel.Anim. Behav. 33, 155–65.

    Google Scholar 

  • Lombardi, J.R. and Whitsett, J.M. (1980) Effects of urine from conspecifics on sexual maturation in female prairie deermice,Peromyscus maniculatus bairdii.J. Mammal. 61, 766–8.

    PubMed  Google Scholar 

  • McIntosh, T.K. and Drickamer, L. (1977) Excreted urine, bladder urine, and the delay of sexual maturation in female house mice.Anim. Behav. 25, 999–1004.

    PubMed  Google Scholar 

  • Magnhagen, C. (1990) Reproduction under predation risk in the sand goby,Potamochistus minutus, and the black goby,Gobius niger: the effect of age and longevity.Behav. Ecol. Soc. 26, 331–5.

    Google Scholar 

  • Magnhagen, C. (1991) Predation risk as a cost of reproduction.Trends Ecol. Evol. 6, 183–6.

    Google Scholar 

  • Massey, A. and Vandenbergh, J.G. (1980) Puberty delay by a urinary cue from female house mouse in feral populations.Science 209, 821–2.

    PubMed  Google Scholar 

  • Milinski, M. and Heller, R. (1978). Influence of a predator on the optimal foraging behaviour of sticklebacks (Gastreolus aculeatus L.).Nature 275, 642–4.

    Google Scholar 

  • Ronkainen, H. and Ylönen, H. (1994) Behaviour of cyclic bank voles under risk of mustelid predation: do females avoid copulations?Oecologia (in press).

  • Sharpe, S.T. and Millar, J.S. (1990) Relocation of nest sites by female deer mice,Peromyscus maniculatus borealis.Can. J. Zool. 68, 2364–7.

    Google Scholar 

  • Sibly, R. and Calow, P. (1984) Direct and absorption costing in the evolution of life cycles.J. Theor. Biol. 111, 463–73.

    PubMed  Google Scholar 

  • Sih, A. (1980) Optimal behavior: can foragers balance two conflicting demands?Science 210, 1041–3.

    Google Scholar 

  • Sih, A. (1982) Foraging strategies and the avoidance of predation by an aquatic insect,Notonecta hoffmanni.Ecology 63, 786–96.

    Google Scholar 

  • Sih, A., Krupa, J. and Travers, S. (1990) An experimental study on the effects of predation risk and feeding regime on the mating behavior of the water strider.Am. Nat. 135, 284–90.

    Google Scholar 

  • Stearns, S.C. and Koella, J.C. (1986) The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size for maturity.Evolution 40, 892–913.

    Google Scholar 

  • Viitala, J. (1987) Social organization ofClethrionomys rutilus (Pall.) at Kilpisjärvi, Finnish Lappland.Ann. Zool. Fenn. 24, 267–73.

    Google Scholar 

  • Watson, M., Clulow, F.V. and Mariotti, F. (1983) Influence of olfactory stimuli on pregnancy of the meadow voleMicrotus pennsylvanicus, in the laboratory.J. Mammal. 64, 706–8.

    Google Scholar 

  • Wing, S.R. (1988) Cost of mating for female insects: risk of predation inPhotinus collustrans (Coleoptera: Lampyridae).Am. Nat. 131, 139–42.

    Google Scholar 

  • Ylönen, H. (1989) Weasels suppress reproduction in cyclic bank volesClethrionomys glareolus.Oikos,55, 138–40.

    Google Scholar 

  • Ylönen, H. (1990) Phenotypic flexibility in the social organization ofClethrionomys. InSocial systems and population cycles in voles (R. H. Tamarin, R.S. Ostfeld, S.R. Pugh and G. Bujalska, eds), pp. 203–12. Birkhäuser, Basel, Boston, Berlin.

    Google Scholar 

  • Ylönen, H., Kojola, T. and Viitala, J. (1988). Changing female spacing behaviour and demography in an enclosed breeding population ofClethrionomys glareolus.Holarct. Ecol. 11, 286–92.

    Google Scholar 

  • Ylönen, H., Jedrzejewska, B., Jedrzejewski, W. and Heikkilä, J. (1992) Antipredatory behaviour ofClethrionomys voles — ‘David and Goliath’ arms race.Ann. Zool. Fenn. 29, 207–16.

    Google Scholar 

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Ylönen, H., Ronkainen, H. Breeding suppression in the bank vole as antipredatory adaptation in a predictable environment. Evol Ecol 8, 658–666 (1994). https://doi.org/10.1007/BF01237848

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