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Oecologia

, Volume 157, Issue 4, pp 725–734 | Cite as

Foraging patterns of voles at heterogeneous avian and uniform mustelid predation risk

  • Jana A. EccardEmail author
  • Jyrki Pusenius
  • Janne Sundell
  • Stefan Halle
  • Hannu Ylönen
Behavioral Ecology - Original Paper

Abstract

Temporal variation of antipredatory behavior and a uniform distribution of predation risk over refuges and foraging sites may create foraging patterns different from those anticipated from risk in heterogenous habitats. We studied the temporal variation in foraging behavior of voles exposed to uniform mustelid predation risk and heterogeneous avian predation risk of different levels induced by vegetation types in eight outdoor enclosures (0.25 ha). We manipulated mustelid predation risk with weasel presence or absence and avian predation risk by reducing or providing local cover at experimental food patches. Foraging at food patches was monitored by collecting giving-up densities at artificial food patches, overall activity was automatically monitored, and mortality of voles was monitored by live-trapping and radiotracking. Voles depleted the food to lower levels in the sheltered patches than in the exposed ones. In enclosures with higher avian predation risk caused by lower vegetation height, trays were depleted to lower levels. Unexpectedly, voles foraged in more trays and depleted trays to lower levels in the presence of weasels than in the absence. Weasels match their prey’s body size and locomotive abilities and therefore increase predation risk uniformly over both foraging sites and refuge sites that can both be entered by the predator. This reduces the costs of missing opportunities other than foraging. Voles changed their foraging strategy accordingly by specializing on the experimental food patches with predictable returns and probably reduced their foraging in the matrix of natural food source with unpredictable returns and high risk to encounter the weasel. Moreover, after 1 day of weasel presence, voles shifted their main foraging activities to avoid the diurnal weasel. This behavior facilitated bird predation, probably by nocturnal owls, and more voles were killed by birds than by weasels. Food patch use of voles in weasel enclosures increased with time. Voles had to balance the previously missed feeding opportunities by progressively concentrating on artificial food patches.

Keywords

Antipredatory behavior Avian predation Bank voles Mustelid predation Predator Facilitation Predator interaction Temporal variation 

Notes

Acknowledgments

We want to thank our helpers in the field—Raisa Tiilikainen, Felix von Blanckenhagen, John Loehr, Miina Kovanen and Anne Mähönen. The Konnevesi Research Station provided excellent background support and working environment. Burt Kotler and Chris Whelan kindly commented on an earlier version of the manuscript. The study was carried out with permission from the Board for Animal Experiments of the University of Jyväskylä (Permission #5/7.2.2000) and the weasel maintenance by the permission of the Ministry of the Environment of Finland (No 1/5722/96) The study was supported by the Academy of Finland (project No:s 208478, 68726 and 44887, 44878 in Finnish Centre of Excellence Programs).

References

  1. Abrahams MV, Dill LM (1989) A determination of the energetic equivalence of the risk of predation. Ecology 70:999–1107CrossRefGoogle Scholar
  2. Abramsky Z, Rosenzweig ML, Belmaker J, Bar A (2004) The impact of long-term continuous risk of predation on two species of gerbils Canadian. J Zool 82:464–474Google Scholar
  3. Abramsky Z, Strauss E, Subach A, Kotler BP, Riechmann A (1996) The effect of barn owls (Tyto alba) on the activity and microhabitat selection of Gerbillus allenbi and G. pyramidum. Oecologia 105:313–319CrossRefGoogle Scholar
  4. Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr 79:371–394Google Scholar
  5. Bouskila A (1995) Interactions between predation risk and competition: a field study of kangaroo rats and snakes. Ecology 76:165–178CrossRefGoogle Scholar
  6. Brandt MJ, Lambin X (2005) Summertime activity patterns of common weasels Mustela nivalis vulgaris under differing prey abundances in grassland habitats. Acta Theriol 50:67–79Google Scholar
  7. Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47CrossRefGoogle Scholar
  8. Brown JS, Kotler BP, Smith RJ, Wirtz WOII (1988) The effects of owl predation on the foraging behaviour of heteromyid rodents. Oecologia 76:408–415Google Scholar
  9. Brown JS, Morgan RA, Dow BD (1992) Patch use under predation risk: II A test with fox squirrels, sciurus niger. Ann Zool Fenn 29:311–318Google Scholar
  10. Charnov EL, Orians GH, Hyatt K (1976) Ecological implications of resource depression. Am Nat 110:247–259CrossRefGoogle Scholar
  11. Davidson DL, Morris DW (2001) Density-dependent foraging effort of Deer Mice (Peromyscus maniculatus). Funct Ecol 15:575–583CrossRefGoogle Scholar
  12. Eccard JA, Liesenjohann T (2008) Foraging decisions in risk-uniform landscapes. Plos ONE (under revision)Google Scholar
  13. Halle S (1993) Diel pattern of predation risk in microtine rodents. Oikos 68:510–518CrossRefGoogle Scholar
  14. Halle S (2000) Voles—small graminivores with polyphasic patterns. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals—an ecological approach. Ecological studies, vol 141. Springer, Berlin, pp 191–215Google Scholar
  15. Halle S, Lehmann U (1987) Circadian activity patterns, photoperiodic responses and population cycles in voles. Oecologia 71:568–572CrossRefGoogle Scholar
  16. Halle S, Lehmann U (1992) Cycle-correlated changes in the activity behavior of field voles Microtus agrestis. Oikos 64:489–497CrossRefGoogle Scholar
  17. Hanski I, Henttonen H (1996) Predation on competing rodent species: a simple explanation of complex patterns. J Anim Ecol 65:220–232CrossRefGoogle Scholar
  18. Hassel M-P, May RM (1986) Generalists and specialists natural enemies in insect predator-prey interactions. J Anim Ecol 55:923–940CrossRefGoogle Scholar
  19. Jacob J, Brown JS (2000) Microhabitat use, gibing-ip densities and temporal activity as short- and long-term anti-predator behaviors in common voles. Oikos 91:131–138CrossRefGoogle Scholar
  20. Jedrzejewski W, Jedrzejewska B, Zub K, Nowakowski WK (2000) Activity patterns of radio-tracked weasels Mustela nivalis in Bialowieza National Park (E Poland). Ann Zool Fenn 37:161–168Google Scholar
  21. Korpimäki E, Koivunen V, Hakkarinen H (1996) Microhabitat use and behaviour of voles under weasel and raptor predation risk: predator facilitation? Behav Ecol 7:30–34CrossRefGoogle Scholar
  22. Korpimäki E, Krebs CJ (1996) Predation and population cycles of small mammals. BioScience 46:754–764CrossRefGoogle Scholar
  23. Korpimäki E, Norrdahl K (1989) Avian predation on Mustelids in Europe 1: occurrence and effects on body size variation and life traits. Oikos 55:205–215CrossRefGoogle Scholar
  24. Kotler B, Blaustein L (1995) Titrating food and safety in a heterogeneous environment: when are the risky and safe patches of equal value? Oikos 74:251–258CrossRefGoogle Scholar
  25. Kotler BP, Blaustein L, Brown JS (1992) Predator facilitation: the combined effects of snakes and owls on the foraging behaviour of gerbils. Ann Zool Fenn 29:199–206Google Scholar
  26. Kotler BP, Brown JS, Hasson O (1991) Factors affecting gerbil foraging behavior and rates of owl predation. Ecology 72:2249–2260CrossRefGoogle Scholar
  27. Lima SL (1992) Life in a multi-predator environment: some considerations for anti-predatory vigilance. Ann Zool Fennici 292:217–226Google Scholar
  28. Lima SL (1998a) Non-lethal effects in the ecology of predator–prey interactions. BioScience 48:25–34CrossRefGoogle Scholar
  29. Lima SL (1998b) Stress and decision-making under the risk of predation: recent developments from behavioural, reproductive, and ecological perspectives. Adv Study Behav 27:215–290CrossRefGoogle Scholar
  30. Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredatory behaviour: the predation risk allocation hypothesis. Am Nat 153:649–659CrossRefGoogle Scholar
  31. Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  32. Milinski M, Heller R (1978) Influence of a predator on the optimal foraging behaviour of sticklebacks. Nature 275:642–644CrossRefGoogle Scholar
  33. Norrdahl K, Korpimäki E (1998) Does mobility or sex of voles affect risk of predation by mammalian predators? Ecology 79:226–232CrossRefGoogle Scholar
  34. Pusenius J, Ostfeld RS (2002) Mammalian predator scent, vegetation cover and tree seedling predation by meadow voles. Ecography 25:481–487CrossRefGoogle Scholar
  35. Pusenius J, Ostfeld RS (2000) Effects of stoat’s presence and auditory cues indicating its presence on tree seedling predation by meadow voles. Oikos 91:123–130CrossRefGoogle Scholar
  36. Sih A (1980) Optimal behaviour: can foragers balance two conflicting demands? Science 210:1041–1043PubMedCrossRefGoogle Scholar
  37. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evolut 13:350–355CrossRefGoogle Scholar
  38. Stephens DW, Krebs JR (1996) Foraging theory. Princeton University Press, PrincetonGoogle Scholar
  39. Sundell J, Eccard JA, Tiilikainen R, Ylönen H (2003) Predation rate, prey preference and predator switching: experiments on voles and weasels. Oikos 101:615–623CrossRefGoogle Scholar
  40. Sundell J, Huitu O, Henttonen H, Kaikusalo A, Korpimäki E, Pietiäinen H, Saurola P, Hanski I (2004) Large-scale spatial dynamics of vole populations in Finland revealed by the breeding success of vole-eating avian predators. J Anim Ecol 73:167–178CrossRefGoogle Scholar
  41. Sundell J, Norrdahl K (2002) Body size-dependent refuges in voles: an alternative explanation of the Chitty effect. Ann Zool Fenn 39:325–333Google Scholar
  42. Sundell J, Norrdahl K, Korpimäki E, Hanski I (2000) Functional response of the least weasel, Mustela nivalis nivalis. Oikos 90:501–508CrossRefGoogle Scholar
  43. Ylönen H (1988) Diel activity and demography in an enclosed population of the vole Clethrionomys glareolus (Schreb.). Ann Zool Fenn 25:221–228Google Scholar
  44. Ylönen H, Jacob J, Davis M, 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 99:285–290CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Jana A. Eccard
    • 1
    • 5
    Email author
  • Jyrki Pusenius
    • 2
  • Janne Sundell
    • 3
  • Stefan Halle
    • 4
  • Hannu Ylönen
    • 5
  1. 1.Animal BehaviorUniversity of BielefeldBielefeldGermany
  2. 2.Finnish Game and Fisheries Research InstituteHelsinkiFinland
  3. 3.Department of Biological and Environmental SciencesUniversity of HelsinkiHelsinkiFinland
  4. 4.Institute of EcologyUniversity of JenaJenaGermany
  5. 5.Department of Biological and Environmental Science, Konnevesi Research StationUniversity of JyväskyläJyväskyläFinland

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