, Volume 176, Issue 1, pp 69–80 | Cite as

Testing the risk of predation hypothesis: the influence of recolonizing wolves on habitat use by moose

  • Kerry L. Nicholson
  • Cyril Milleret
  • Johan Månsson
  • Håkan Sand
Behavioral ecology - Original research


Considered as absent throughout Scandinavia for >100 years, wolves (Canis lupus) have recently naturally recolonized south-central Sweden. This recolonization has provided an opportunity to study behavioral responses of moose (Alces alces) to wolves. We used satellite telemetry locations from collared moose and wolves to determine whether moose habitat use was affected by predation risk based on wolf use distributions. Moose habitat use was influenced by reproductive status and time of day and showed a different selection pattern between winter and summer, but there was weak evidence that moose habitat use depended on predation risk. The seemingly weak response may have several underlying explanations that are not mutually exclusive from the long term absence of non-human predation pressure: intensive harvest by humans during the last century is more important than wolf predation as an influence on moose behavior; moose have not adapted to recolonizing wolves; and responses may include other behavioral adaptations or occur at finer temporal and spatial levels than investigated.


Anti-predator behaviour Foraging trade-offs Habitat shift Landscape of risk Trophic cascade Resource selection 



We are indebted to J.M. Arnemo, and P. Ahlqvist, who captured and handled the wolves and to P. Grängstedt who captured the moose. We would like to thank H. Andrén, J. López-Bao, P. Krausman, and M. Kohl for their thoughtful insights, statistical interpretation and discussions about this work. Financial support was given from the Swedish Environmental Protection Agency, and two private foundations Marie-Claire Cronstedts Stiftelse and Carl Tryggers Stiftelse. The study was performed in compliance with the Swedish Committee of Animal Welfare (Permit C281/6 & C315/6).

Supplementary material

442_2014_3004_MOESM1_ESM.png (263 kb)
Supplementary material 1 (PNG 263 kb)
442_2014_3004_MOESM2_ESM.png (199 kb)
Supplementary material 2 (PNG 198 kb)
442_2014_3004_MOESM3_ESM.docx (23 kb)
Supplementary material 3 (DOCX 24 kb)


  1. Abramsky Z, Rosenzweig ML, Subach A (2002) The costs of apprehensive foraging. Ecology 83:1330–1340CrossRefGoogle Scholar
  2. Alexandersson H, Andersson T (1995) Nederbörd och åska [Precipitation and thunderstorms]. In: Raab B, Vedin H (eds) Klimat, sjöar och vattendrag [Climate, lakes and rivers] SNA Bokfö rlaget Bra böcker (in Swedish.), Höganäs, Sweden, pp 76–90Google Scholar
  3. Arnemo JM, Kreeger TJ, Soveri T (2003) Chemical immobilization of free-ranging moose. Alces 39:243–253Google Scholar
  4. Arnemo JM et al (2007) Biomedical protocols for free-ranging brown bears, gray wolves, wolverines and lynx. Norwegian School of Veterinary Science, NorwayGoogle Scholar
  5. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Management 74:1175–1178CrossRefGoogle Scholar
  6. Barton K (2012) MuMIn: Multi-model inference, 1.7.11 edn. R package version 1.7.11Google Scholar
  7. Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classes, 0.999999-0 edn. R package version 0.999999-0Google Scholar
  8. Berger J (1999) Anthropogenic extinction of top carnivores and interspecific animal behaviour: implications of the rapid decoupling of a web involving wolves, bears, moose and ravens. Proc R Soci Lond Ser B Biol Sci 266:2261–2267CrossRefGoogle Scholar
  9. Berger J, Swenson JE, Persson IL (2001) Recolonizing carnivores and naïve prey: conservation lessons from pleistocene extinctions. Science 291:1036–1039PubMedCrossRefGoogle Scholar
  10. Bjørneraas K, Van Moorter B, Rolandsen CM, Herfindal I (2010) Screening global positioning system location data for errors using animal movement characteristics. J Wildl Manage 74:1361–1366CrossRefGoogle Scholar
  11. Bjørneraas K et al (2011) Moose Alces alces habitat use at multiple temporal scales in a human-altered landscape. Wildl Biol 17:44–54CrossRefGoogle Scholar
  12. Bjørneraas K, Herfindal I, Solberg E, Sæther B-E, Moorter B, Rolandsen C (2012) Habitat quality influences population distribution, individual space use and functional responses in habitat selection by a large herbivore. Oecologia 168:231–243PubMedCentralPubMedCrossRefGoogle Scholar
  13. Blumstein DT, Daniel JC (2005) The loss of anti-predator behaviour following isolation on islands. Proc R Soci B Biol Sci 272:1663–1668CrossRefGoogle Scholar
  14. Brown JS (1992) Patch use under predation risk: I. Models and Predictions: Annales Zoologici Fennici 29:301–309Google Scholar
  15. Brown JS, Laundré JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399CrossRefGoogle Scholar
  16. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer-Verlang, New YorkCrossRefGoogle Scholar
  17. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer-Verlag, New YorkGoogle Scholar
  18. Byers JA (1998) American pronghorn: social adaptations and the ghosts of predators past. University of Chicago Press, ChicagoGoogle Scholar
  19. Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecolo Model 197:516–519CrossRefGoogle Scholar
  20. Calenge C, Dufour A, Maillard D (2005) K-select analysis: a new method to analyse habitat selection in radio-tracking studies. Ecol Model 186:143–153CrossRefGoogle Scholar
  21. Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, ChicagoGoogle Scholar
  22. Cederlund GN, Okarma H (1988) Home range and habitat use of adult female moose. J Wildl Manage 52:336–343CrossRefGoogle Scholar
  23. Cederlund GN, Sand H (1991) Population dynamics and yield of a moose population without predators. Alces 27:31–40Google Scholar
  24. Christianson D, Creel S (2008) Risk effects in elk: sex-specific responses in grazing and browsing due to predation risk from wolves. Behav Ecol 19:1258–1266CrossRefGoogle Scholar
  25. Ciuti S, Bongi P, Vassale S, Apollonio M (2006) Influence of fawning on the spatial behaviour and habitat selection of female fallow deer (Dama dama) during late pregnancy and early lactation. J Zool 268:97–107CrossRefGoogle Scholar
  26. Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201PubMedCrossRefGoogle Scholar
  27. Creel S, Winnie J, Maxwell B, Hamlin K, Creel M (2005) Elk alter habitat selection as an antipredator response to wolves. Ecology 86:3387–3397CrossRefGoogle Scholar
  28. Creel S, Winnie JA Jr, Christianson D, Liley S (2008) Time and space in general models of antipredator response: tests with wolves and elk. Anim Behav 76:1139–1146CrossRefGoogle Scholar
  29. Dussault C, Ouellet JP (2004) Behavioural responses of moose to thermal conditions in the boreal forest. Ecoscience 11:321–328Google Scholar
  30. Dussault C, Ouellet JP, Courtois R, Huot J, Breton L, Jolicoeur H (2005) Linking moose habitat selection to limiting factors. Ecography 28:619–628CrossRefGoogle Scholar
  31. Edwards J (1983) Diet shifts in moose due to predator avoidance. Oecologia 60:185–189CrossRefGoogle Scholar
  32. Eriksen A et al (2011) Activity patterns of predator and prey: a simultaneous study of GPS-collared wolves and moose. Anim Behav 81:423–431CrossRefGoogle Scholar
  33. Fortin D, Beyer HL, Boyce MS, Smith DW, Duchesne T, Mao JS (2005) Wolves influence elk movements: behavior shapes a trophic cascade in Yellowstone National Park. Ecology 86:1320–1330CrossRefGoogle Scholar
  34. Frair JL, Fieberg J, Hebblewhite M, Cagnacci F, DeCesare NJ, Pedrotti L (2010) Resolving issues of imprecise and habitat-biased locations in ecological analyses using GPS telemetry data. Philosophical Transactions R Soci B Biol Sci 365:2187–2200CrossRefGoogle Scholar
  35. Frid A, Dill LM (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11Google Scholar
  36. Gaillard JM et al (2010) Habitat-performance relationships: finding the right metric at a given spatial scale. Philosophical Transactions R Soci B Biol Sci 365:2255–2265CrossRefGoogle Scholar
  37. Garrott RA, White PJ, Rotella JJ (2008) Chapter 23 The Madison Headwaters elk herd: transitioning from bottom–up regulation to top–down limitation. In: Robert A. Garrott PJW, Fred GRW (eds) Terrestrial ecology, vol Volume 3. Elsevier, pp 489–517Google Scholar
  38. Gervasi V et al (2011) Predicting the potential demographic impact of predators on their prey: a comparative analysis of two carnivore–ungulate systems in Scandinavia. J Anim Ecol 81:443–454PubMedCrossRefGoogle Scholar
  39. Gervasi V, Sand H, Zimmerman B, Mattisson J, Wabakken P, Linnell JDC (2013) Decomposing risk: landscape structure and wolf behavior generate different predation patterns in two sympatric ungulates. Ecol Appl 23:1722–1734Google Scholar
  40. Girard I, Ouellet JP, Courtois R, Dussault C, Breton L (2002) Effects of sampling effort based on GPS telemetry on home-range size estimations. J Wildl Manage 66:1290–1300CrossRefGoogle Scholar
  41. Haglund B (1968) De stora rovdjurens vintervanor II. Viltrevy 5:213–361Google Scholar
  42. Hebblewhite M, Merrill E (2007) Multiscale wolf predation risk for elk: does migration reduce risk? Oecologia 152:377–387PubMedCrossRefGoogle Scholar
  43. Hebblewhite M, Pletscher DH, Paquet PC (2002) Elk population dynamics in areas with and without predation by recolonizing wolves in Banff National Park, Alberta. Can J Zool 80:789–799CrossRefGoogle Scholar
  44. Hernández L, Laundré JW (2005) Foraging in the ‘landscape of fear’ and its implications for habitat use and diet quality of elk Cervus elaphus and bison Bison bison. Wildl Biol 11:215–220CrossRefGoogle Scholar
  45. Hunter LTB, Skinner JD (1998) Vigilance behaviour in African ungulates: the role of predation pressure. Behav 135:195–211CrossRefGoogle Scholar
  46. Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65–71CrossRefGoogle Scholar
  47. Kauffman MJ, Brodie JF, Jules ES (2010) Are wolves saving Yellowstone’s aspen? A landscape-level test of a behaviorally mediated trophic cascade. Ecology 91:2742–2755PubMedCrossRefGoogle Scholar
  48. Kunkel KE, Pletscher DH (2000) Habitat factors affecting vulnerability of moose to predation by wolves in southeastern British Columbia. Can J Zool 78:150–157CrossRefGoogle Scholar
  49. Latombe G, Fortin D, Parrott L (2014) Spatio-temporal dynamics in the response of woodland caribou and moose to the passage of grey wolf. J Anim Ecol 83:185–198PubMedCrossRefGoogle Scholar
  50. Laundré JW, Hernández L, Altendorf KB (2001) Wolves, elk, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, U.S.A. Can J Zool 79:1401–1409CrossRefGoogle Scholar
  51. Lavsund S, Nygrén T, Solberg EJ (2003) Status of moose populations and challenges to moose management in Fennoscandia. Alces 39:109–130Google Scholar
  52. Liberg O, Bergström R, Kindberg J, von Essen H (2010) Ungulates and their management in Sweden. In: Apollonio M, Andersen R, Putman R (eds) European ungulates and their management in the 21st century. Cambridge University Press, UK, p 618Google Scholar
  53. Liberg O et al (2011) Monitoring of wolves in ScandinaviaGoogle Scholar
  54. Lima SL (1995) Back to the basics of anti-predatory vigilance: the group-size effect. Anim Behav 49:11–20CrossRefGoogle Scholar
  55. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  56. Lönnberg E (1934) Bidrag till vargens historia i Sverige. Kungliga Vetenskapsakademins skrifter i naturskyddsärenden 26:1–33Google Scholar
  57. Lykkja ON, Solberg EJ, Herfindal I, Wright J, Rolandsen CM, Hanssen MG (2009) The effects of human activity on summer habitat use by moose. Alces 45:109–124Google Scholar
  58. Månsson J (2009) Environmental variation and moose Alces alces density as determinants of spatio-temporal heterogeneity in browsing. Ecography 32:601–612CrossRefGoogle Scholar
  59. Månsson J, Andrén H, Sand H (2011) Can pellet counts be used to accurately describe winter habitat selection by moose Alces alces? Eur J Wildl Res 57:1017–1023CrossRefGoogle Scholar
  60. Mao JS et al (2005) Habitat selection by elk before and after wolf reintroduction in Yellowstone National Park. J Wildl Manag 69:1691–1707CrossRefGoogle Scholar
  61. Martin J, Basille M, Van Moorter B, Kindberg J, Allaine D, Swenson JE (2010) Coping with human disturbance: spatial and temporal tactics of the brown bear (Ursus arctos). Can J Zool 88:875–883CrossRefGoogle Scholar
  62. Mech LD, Smith DW, Murphy KM, MacNulty (2001) Winter severity and wolf predation on a formerly wolf-free elk herd. J Wildl Manag 65:998–1003CrossRefGoogle Scholar
  63. Metz MC, Smith DW, Vucetich JA, Stahler DR, Peterson RO (2012) Seasonal patterns of predation for gray wolves in the multi-prey system of Yellowstone National Park. J Anim Ecol 81:553–563PubMedCrossRefGoogle Scholar
  64. Mohr CO (1947) Table of equivalent populations of North American small mammals. Am Midl Nat 37:223–249CrossRefGoogle Scholar
  65. Neumann W, Ericsson G, Dettki H, Arnemo JM (2011) Effect of immobilizations on the activity and space use of female moose (Alces alces). Can J Zool 89:1013–1018CrossRefGoogle Scholar
  66. Olsson M, Cox J, Larkin J, Widén P, Olovsson A (2011) Space and habitat use of moose in southwestern Sweden. Eur J Wildl Res 57:241–249CrossRefGoogle Scholar
  67. Pettorelli N, Vik JO, Mysterud A, Gaillard JM, Tucker CJ, Stenseth NC (2005) Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends Ecol Evol 20:503–510PubMedCrossRefGoogle Scholar
  68. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509CrossRefGoogle Scholar
  69. R Development Core Team (2010) R: A language and environment for statistical computing, R Foundation for Statistical Computing, 2.11.1 edn, Vienna, AustriaGoogle Scholar
  70. Ripple WJ, Beschta RL (2004) Wolves and the ecology of fear: can predation risk structure ecosystems? Bioscience 54:755–766CrossRefGoogle Scholar
  71. Robinson B, Hebblewhite M, Merrill E (2010) Are migrant and resident elk (Cervus elaphus) exposed to similar forage and predation risk on their sympatric winter range? Oecologia 164:265–275PubMedCrossRefGoogle Scholar
  72. Rönnegård L, Sand H, Andrén H, Månsson J, Pehrson Å (2008) Evaluation of four methods used to estimate population density of moose Alces alces. Wildl Biol 14:358–371CrossRefGoogle Scholar
  73. Sæther BE, Engen S, Lande R (1996) Density-dependence and optimal harvesting of fluctuating populations. Oikos 76:40–46CrossRefGoogle Scholar
  74. Sand H, Zimmermann B, Wabakken P, Andren H, Pedersen HC (2005) Using GPS technology and GIS cluster analyses to estimate kill rates in wolf-ungulate ecosystems. Wildl Soc Bull 33:914–925CrossRefGoogle Scholar
  75. Sand H, Wikenros C, Wabakken P, Liberg O (2006a) Cross-continental differences in patterns of predation: will naive moose in Scandinavia ever learn? Proc R Soci B Biol Sci 273:1421–1427CrossRefGoogle Scholar
  76. Sand H, Wikenros C, Wabakken P, Liberg O (2006b) Effects of hunting group size, snow depth and age on the success of wolves hunting moose. Anim Behav 72:781–789CrossRefGoogle Scholar
  77. Sand H, Wabakken P, Zimmermann B, Johansson O, Pedersen HC, Liberg O (2008) Summer kill rates and predation pattern in a wolf–moose system: can we rely on winter estimates? Oecologia 156:53–64PubMedCrossRefGoogle Scholar
  78. Sand H, Wikenros C, Ahlqvist P, Stromseth TH, Wabakken P (2012) Comparing body condition of moose (Alces alces) selected by wolves (Canis lupus) and human hunters: consequences for the extent of compensatory modality. Can J Zool 90:403–412CrossRefGoogle Scholar
  79. Sappington JM, Longshore KM, Thompson DB (2007) Quantifying landscape ruggedness for animal habitat analysis: a case study using bighorn sheep in the Mojave Desert. J Wildl Manage 71:1419–1426CrossRefGoogle Scholar
  80. Smith DW, Peterson RO, Houston DB (2003) Yellowstone after wolves. Bioscience 53:330–340CrossRefGoogle Scholar
  81. Stubsjøen T, Sæther B-E, Solberg EJ, Heim M, Rolandsen CM (2000) Moose (Alces alces) survival in three populations in northern Norway. Can J Zool 78:1822–1830CrossRefGoogle Scholar
  82. Thaker M, Vanak AT, Owen CR, Ogden MB, Niemann SM, Slotow R (2011) Minimizing predation risk in a landscape of multiple predators: effects on the spatial distribution of African ungulates. Ecology 92:398–407PubMedCrossRefGoogle Scholar
  83. Valeix M et al (2009) Behavioral adjustments of African herbivores to predation risk by lions: spatio-temporal variations influence habitat use. Ecology 90:23–30PubMedCrossRefGoogle Scholar
  84. Van Beest FM, Mysterud A, Loe LE, Milner JM (2010) Forage quantity, quality and depletion as scale-dependent mechanisms driving habitat selection of a large browsing herbivore. J Anim Ecol 79:910–922PubMedGoogle Scholar
  85. Vedin H (1995) Lufttemperatur [Air temperature]. In: B. Raab, Vedin H (eds) Klimat, sjöar och vattendrag [Climate, lakes and rivers] SNA Bokfö rlaget Bra böcker (In Swedish.), Höganäs, Sweden, pp 91–97Google Scholar
  86. Vijayan S, Morris DW, McLaren BE (2012) Prey habitat selection under shared predation: tradeoffs between risk and competition? Oikos 121:783–789CrossRefGoogle Scholar
  87. Wabakken P, Sand H, Liberg O, Bjärvall A (2001) The recovery, distribution, and population dynamics of wolves on the Scandinavian peninsula, 1978–1998. Can J Zool 79:710–725CrossRefGoogle Scholar
  88. Wabakken P et al (2011) The wolf in Scandinavia: Status report of the 2009–2010 winter (in Norwegian with English summary). In: 1:2011 On (ed) Oppdragsrapport no., vol. Oppdragsrapport no. 1:2011, Høgskolen i HedmarkGoogle Scholar
  89. Winnie J Jr, Creel S (2007) Sex-specific behavioural responses of elk to spatial and temporal variation in the threat of wolf predation. Anim Behav 73:215–225CrossRefGoogle Scholar
  90. Wirsing AJ, Cameron KE, Heithaus MR (2010) Spatial responses to predators vary with prey escape mode. Anim Behav 79:531–537CrossRefGoogle Scholar
  91. Worton BJ (1989) Kernel methods for estimating the utilization distribution in home range studies. Ecology 70:164–168CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Kerry L. Nicholson
    • 1
  • Cyril Milleret
    • 1
    • 2
  • Johan Månsson
    • 1
  • Håkan Sand
    • 1
  1. 1.Department of EcologyGrimsö Wildlife Research Station, Swedish University of Agricultural SciencesRiddarhyttanSweden
  2. 2.Faculty of Forestry and Wildlife ManagementHedmark University CollegeKoppangNorway

Personalised recommendations