Skip to main content

Patch use and vigilance by sympatric lemmings in predator and competitor-driven landscapes of fear

Abstract

Prey living in risky environments can adopt a variety of behavioral tactics to reduce predation risk. In systems where predators regulate prey abundance, it is reasonable to assume that differential patterns of habitat use by prey species represent adaptive responses to spatial variation in predation. However, patterns of habitat use also reflect interspecific competition over habitat. Collared (Dicrostonyx groenlandicus) and brown (Lemmus trimucronatus) lemmings represent such a system and possess distinct upland tundra versus mesic meadow habitat preferences consistent with interspecific competition. Yet, we do not know whether this habitat preference might also reflect differences in predation risk or whether the two species differ in their behavioral tactics used to avoid predation. We performed experiments where we manipulated putative predation risk perceived by lemmings by increasing protective cover in upland and meadow habitats while we recorded lemming activity and behavior. Both lemming species preferentially used cover more than open patches, but Dicrostonyx was more vigilant than Lemmus. Both species also constrained their activity to protective patches in upland and meadow habitats, but during different periods of the day. Use of cover and vigilance were independent of habitat, suggesting that both species live in a fearsome but flattened landscape of fear at Walker Bay (Nunavut, Canada), and that their habitat preference is a consequence of competition rather than predation risk. Future studies aiming to map the contours of fear in multi-prey–predator systems should consider how predation and competition interact to modify prey species’ habitat preference, patch use, and vigilance.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Ale SB, Morris DW, Dupuch A, Moore DE (2011) Habitat selection and the scale of ghostly coexistence among Arctic rodents. Oikos 120:1191–1200

    Article  Google Scholar 

  2. Angerbjörn A, Tannerfeldt M, Erlinge S (1999) Predator–prey relations: lemmings and arctic foxes. J Anim Ecol 68:34–49

    Article  Google Scholar 

  3. Bates D, Maechler M, Bolker B (2011) Lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42

  4. Batzli GO (1993) Food selection by lemmings. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, New York, pp 281–301

    Google Scholar 

  5. Batzli GO, Pitelka FA, Cameron GN (1983) Habitat use by lemmings near Barrow, Alaska. Holarctic Ecol 6:255–262

    Google Scholar 

  6. Beauchamp G (2008) What is the magnitude of the group-size effect on vigilance? Behav Ecol 19:1361–1368

    Article  Google Scholar 

  7. Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47

    Article  Google Scholar 

  8. Brown JS (1999) Vigilance, patch use and habitat selection: foraging under predation risk. Evol Ecol Res 1:49–77

    Google Scholar 

  9. Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014

    Article  Google Scholar 

  10. Brown JS, Kotler BP (2007) Foraging and the ecology of fear. In: Stephens DW, Brown JS, Ydenberg RC (eds) Foraging behavior and ecology. University of Chicago Press, Chicago, pp 437–480

    Google Scholar 

  11. Brown JS, Morgan RA, Dow BD (1992) Patch use under predation risk: II. A test with fox squirrels, Sciurus niger. Ann Zool Fenn 29:311–318

    Google Scholar 

  12. Brown JS, Laundré JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399

    Article  Google Scholar 

  13. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  14. China V, Kotler BP, Shefer N, Brown JS, Abramsky Z (2008) Density-dependent habitat and patch use in gerbils: consequences of safety in numbers? Isr J Ecol Evol 54:373–388

    Article  Google Scholar 

  15. Dall SRX, Kotler BP, Bouskila A (2001) Attention, apprehension and gerbils searching in patches. Ann Zool Fenn 38:15–23

    Google Scholar 

  16. Devereux CL, Whittingham MJ, Fernandez-Juricic E, Vickery JA, Krebs JR (2006) Predator detection and avoidance by starlings under differing scenarios of predation risk. Behav Ecol 17:303–309

    Article  Google Scholar 

  17. Dupuch A, Dill LM, Magnan P (2009) Testing the effects of resource distribution and inherent habitat riskiness on simultaneous habitat selection by predators and prey. Anim Behav 78:705–713

    Article  Google Scholar 

  18. Dupuch A, Morris DW, Ale SB, Wilson DJ, Moore DE (2013) Landscapes of fear or competition? Predation did not alter habitat choice by Arctic rodents. Oecologia (published online, doi: 10.1007/s00442-013-2792-7)

  19. Eccard JA, Liesenjohann T (2008) Foraging decisions in risk-uniform landscapes. PloS ONE 3:e3438

    PubMed Central  PubMed  Article  Google Scholar 

  20. Embar K, Kotler BP, Mukherjee S (2011) Risk management in optimal foragers: the effect of sightlines and predator type on patch use, time allocation, and vigilance in gerbils. Oikos 120:1657–1666

    Article  Google Scholar 

  21. Gauthier G, Bêty J, Giroux J-F, Rochefort L (2004) Trophic interactions in a high arctic snow goose colony. Integr Comp Biol 44:119–129

    PubMed  Article  Google Scholar 

  22. Gauthier G, Berteaux D, Krebs CJ, Reid D (2009) Arctic lemmings are not simply food limited—a comment on Oksanen et al. Evol Ecol Res 11:483–484

    Google Scholar 

  23. Gilg O, Hanski I, Sitller B (2003) Cyclic dynamics in a simple vertebrate predator–prey community. Science 302:866–868

    CAS  PubMed  Article  Google Scholar 

  24. Gilg O, Sittler B, Sabard B, Hurstel A, Sane R, Delattre P, Hanski I (2006) Functional and numerical responses of four lemming predators in high arctic Greenland. Oikos 113:193–216

    Article  Google Scholar 

  25. Grand TC, Dill LM (1997) The energetic equivalence of cover to juvenile coho salmon (Oncorhynchus kisutch): ideal free distribution theory applied. Behav Ecol 8:437–447

    Article  Google Scholar 

  26. Hammond JI, Luttbeg B, Sih A (2007) Predator and prey space use: dragonflies and tadpoles in an interactive game. Ecology 88:1525–1535

    PubMed  Article  Google Scholar 

  27. Hanski I, Hentonnen H (1996) Predation on competing rodent species: a simple explanation to complex patterns. J Anim Ecol 65:220–232

    Article  Google Scholar 

  28. Heithaus MR, Wirsing AJ, Frid A, Dill LM (2007) Behavioral indicators in marine conservation: lessons from a pristine seagrass ecosystem. Isr J Ecol Evol 53:355–370

    Article  Google Scholar 

  29. Holt RD (1977) Predation, apparent competition and the structure of prey communities. Theor Popul Biol 12:197–229

    CAS  PubMed  Article  Google Scholar 

  30. Holt RD, Kotler BP (1987) Short-term apparent competition. Am Nat 130:412–430

    Article  Google Scholar 

  31. Hugie DM, Dill LM (1994) Fish and game: a game theoretic approach to habitat selection by predators and prey. J Fish Biol 45:151–169

    Google Scholar 

  32. Kotler BP (1997) Patch use by gerbils in a risky environment: manipulating food and safety to test four models. Oikos 78:274–282

    Article  Google Scholar 

  33. Kotler BP, Brown JS, Hasson 0 (1991) Owl predation on gerbils: the role of body size, illumination, and habitat structure on rates of predation. Ecology 72:2249–2260

    Article  Google Scholar 

  34. Kotler BP, Blaustein L, Brown JS (1992) Predator facilitation: the combined effect of snakes and owls on the foraging behavior of gerbils. Ann Zool Fenn 29:2249–226

    Google Scholar 

  35. Kotler BP, Brown JS, Mukherjee S, Berger-Tal O, Bouskila A (2010) Moonlight avoidance in gerbils reveals a sophisticated interplay among time allocation, vigilance and state-dependent foraging. Proc Roy Soc Lond B 277:1469–1474

    Article  Google Scholar 

  36. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, New York

    Google Scholar 

  37. Krebs CJ (1964) The lemming cycle at Baker Lake, Northwest Territories, during 1959–1962. Arctic Institute of North America Technical Paper 15:1–104

  38. Krebs CJ (2011) Of lemmings and snowshoe hares: the ecology of northern Canada. Proc Roy Soc Lond B 278:481–489

    Article  Google Scholar 

  39. Laundré JW, Hernández L, Altendorf KB (2001) Wolves, elk & bison: reestablishing the “landscape of fear” in Yellowstone National Park USA. Can J Zool 79:1401–1409

    Article  Google Scholar 

  40. Laundré JW, Hernández L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7

    Article  Google Scholar 

  41. Legagneux P, Gauthier G, Berteaux D, Bêty J, Cadieux M-C, Bilodeau F, Bolduc E, McKinnon L, Tarroux A, Therrien J-F, Morissette L, Krebs CJ (2012) Disentangling trophic relationships in a high arctic tundra ecosystem through food web modeling. Ecology 93:1707–1716

    CAS  PubMed  Article  Google Scholar 

  42. Morris DW (2005a) Habitat-dependent foraging in a classic predator–prey system: a fable from snowshoe hares. Oikos 109:239–254

    Article  Google Scholar 

  43. Morris DW (2005b) Paradoxical avoidance of enriched habitats: have we failed to appreciate omnivores? Ecology 86:2568–2577

    Article  Google Scholar 

  44. Morris DW (2009) Apparent predation risk: tests of habitat selection theory reveal unexpected effects of competition. Evol Ecol Res 11:209–225

    Google Scholar 

  45. Morris DW, Dupuch A (2012) Habitat change and the scale of habitat selection: shifting gradients used by coexisting Arctic rodents. Oikos 121:783–789

    Article  Google Scholar 

  46. Morris DW, Davidson DL, Krebs CJ (2000) Measuring the ghost of competition: insights from density-dependent habitat selection on the coexistence and dynamics of lemmings. Evol Ecol Res 2:41–67

    Google Scholar 

  47. Morris DW, Dupuch A, Halliday WD (2012) Climate-induced habitat selection predicts future evolutionary strategies of lemmings. Evol Ecol Res 14:689–705

    Google Scholar 

  48. Oksanen L (1983) Trophic exploitation and arctic phytomass patterns. Am Nat 122:45–52

    Google Scholar 

  49. Oksanen T, Oksanen L, Dahgren J, Olofsson J (2008) Arctic lemmings, Lemmus spp. and Dicrostonyx spp.: integrating ecological and evolutionary perspectives. Evol Ecol Res 10:415–434

    Google Scholar 

  50. Oksanen T, Oksanen L, Dahlgren J, Olofsson J, Kyrö K (2009) On the implications of currently available data on population fluctuations of arctic lemmings—reply to Gauthier et al. Evol Ecol Res 11:485–487

    Google Scholar 

  51. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2012) nlme: linear and nonlinear mixed effects models. R package version 3.1–105. URL: http://cran.r-project.org/web/packages/nlme. Accessed 6 July 2012

  52. Pitelka FA, Batzli GO (1993) Distribution, abundance and habitat use by lemmings on the north slope of Alaska. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, New York, pp 213–236

  53. Predavec M, Krebs CJ (2000) Microhabitat utilization, home ranges, and movement patterns of the collared lemming (Dicrostonyx groenlandicus) in the central Canadian Arctic. Can J Zool 78:1885–1890

    Google Scholar 

  54. Pulliam HR (1973) On the advantages of flocking. Theor Biol 38:419–422

    CAS  Article  Google Scholar 

  55. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, URL http://www.R-project.org/. Accessed 1 Jan 2011

  56. Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086

    Article  Google Scholar 

  57. Rodgers AR, Lewis MC (1986) Diet selection in Arctic lemmings (Lemmus sibiricus and Dicrostonyx groenlandicus): demography, home range, and habitat use. Can J Zool 64:2717–2727

    Article  Google Scholar 

  58. Schmidt NM, Berg TB, Forchhammer MC, Hendrichsen DK, Kyhn LA, Meltofte H, Hoye TT (2008) Vertebrate predator–prey interactions in a seasonal environment. Adv Ecol Res 40:345–370

    Google Scholar 

  59. Sekhon JS (2011) Multivariate and propensity score matching software with automated balance optimization: the matching package for R. J Stat Softw 42:1–52

    Google Scholar 

  60. Slotow R, Coumi N (2000) Vigilance in bronze mannikin groups: the contributions of predation risk and intra-group competition. Behaviour 137:565–578

    Article  Google Scholar 

  61. Treves A (2000) Theory and method in studies of vigilance and aggregation. Anim Behav 60:711–722

    PubMed  Article  Google Scholar 

  62. van der Merwe M, Brown JS (2008) Mapping the landscape of fear of the cape ground squirrel (Xerus inauris). J Mammal 89:1162–1169

    Article  Google Scholar 

  63. Watson A (1956) Ecological notes on the lemmings Lemmus trimucronatus and Dicrostonyx groenlandicus in Baffin Island. J Anim Ecol 25:289–301

    Article  Google Scholar 

  64. Werner EE, Gilliam JF, Hall DF, Mittelbach GG (1983) An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540–1548

    Article  Google Scholar 

  65. Wilson DJ, Bromley RG (2001) Functional and numerical responses of predators to cyclic lemming abundances: effects on loss of goose nests. Can J Zool 79:525–532

    Article  Google Scholar 

  66. Wilson DJ, Krebs CJ, Sinclair ARE (1999) Limitation of collared lemming populations during a population cycle. Oikos 87:382–398

    Article  Google Scholar 

Download references

Acknowledgments

We thank Canada’s International Polar Year program “Arctic Wildlife Observatories Linking Vulnerable EcoSystems”, Natural Sciences and Engineering Research Council, Department of Indian and Northern Affairs, Northern Scientific Training Program, and Polar Continental Shelf Project (Natural Resources Canada), for financial and logistical support. We also thank Lakehead University’s Northern Studies Committee and Canada’s Summer Career Placements program for student support and the Government of Nunavut for permission and facilities to conduct this research. Our tests of predation’s effects on lemming habitat use benefitted from the assistance and cooperation of G. Gauthier, S. Vijayan, M. Moses, and R.W. Buchkowski. This contribution was improved by candid and helpful comments by B. Kotler and an anonymous referee. We thank you.

Ethical standards

All experiments complied with animal utilization protocols certified by the Lakehead University Animal Care Committee.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Douglas W. Morris.

Additional information

Communicated by E. Korpimäki

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 227 kb)

ESM 2

(DOC 60 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dupuch, A., Morris, D.W. & Halliday, W.D. Patch use and vigilance by sympatric lemmings in predator and competitor-driven landscapes of fear. Behav Ecol Sociobiol 68, 299–308 (2014). https://doi.org/10.1007/s00265-013-1645-z

Download citation

Keywords

  • Activity pattern
  • Antipredator behavior
  • Competition
  • Dicrostonyx
  • Lemmus
  • Predation risk