Skip to main content

Advertisement

SpringerLink
Log in

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

  • Behavioral ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abramsky Z, Rosenzweig ML, Subach A (2002) The costs of apprehensive foraging. Ecology 83:1330–1340

    Article  Google Scholar 

  • 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 76–90

  • Arnemo JM, Kreeger TJ, Soveri T (2003) Chemical immobilization of free-ranging moose. Alces 39:243–253

    Google Scholar 

  • Arnemo JM et al (2007) Biomedical protocols for free-ranging brown bears, gray wolves, wolverines and lynx. Norwegian School of Veterinary Science, Norway

    Google Scholar 

  • Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Management 74:1175–1178

    Article  Google Scholar 

  • Barton K (2012) MuMIn: Multi-model inference, 1.7.11 edn. R package version 1.7.11

  • Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classes, 0.999999-0 edn. R package version 0.999999-0

  • 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 266:2261–2267

    Article  CAS  Google Scholar 

  • Berger J, Swenson JE, Persson IL (2001) Recolonizing carnivores and naïve prey: conservation lessons from pleistocene extinctions. Science 291:1036–1039

    Article  CAS  PubMed  Google Scholar 

  • 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 74:1361–1366

    Article  Google Scholar 

  • Bjørneraas K et al (2011) Moose Alces alces habitat use at multiple temporal scales in a human-altered landscape. Wildl Biol 17:44–54

    Article  Google Scholar 

  • 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 168:231–243

    Article  PubMed Central  PubMed  Google Scholar 

  • Blumstein DT, Daniel JC (2005) The loss of anti-predator behaviour following isolation on islands. Proc R Soci B Biol Sci 272:1663–1668

    Article  Google Scholar 

  • Brown JS (1992) Patch use under predation risk: I. Models and Predictions: Annales Zoologici Fennici 29:301–309

    Google Scholar 

  • 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 

  • Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer-Verlang, New York

    Book  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer-Verlag, New York

    Google Scholar 

  • Byers JA (1998) American pronghorn: social adaptations and the ghosts of predators past. University of Chicago Press, Chicago

    Google Scholar 

  • Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecolo Model 197:516–519

    Article  Google Scholar 

  • Calenge C, Dufour A, Maillard D (2005) K-select analysis: a new method to analyse habitat selection in radio-tracking studies. Ecol Model 186:143–153

    Article  Google Scholar 

  • Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago

    Google Scholar 

  • Cederlund GN, Okarma H (1988) Home range and habitat use of adult female moose. J Wildl Manage 52:336–343

    Article  Google Scholar 

  • Cederlund GN, Sand H (1991) Population dynamics and yield of a moose population without predators. Alces 27:31–40

    Google Scholar 

  • Christianson D, Creel S (2008) Risk effects in elk: sex-specific responses in grazing and browsing due to predation risk from wolves. Behav Ecol 19:1258–1266

    Article  Google Scholar 

  • 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 268:97–107

    Article  Google Scholar 

  • Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201

    Article  PubMed  Google Scholar 

  • Creel S, Winnie J, Maxwell B, Hamlin K, Creel M (2005) Elk alter habitat selection as an antipredator response to wolves. Ecology 86:3387–3397

    Article  Google Scholar 

  • 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 76:1139–1146

    Article  Google Scholar 

  • Dussault C, Ouellet JP (2004) Behavioural responses of moose to thermal conditions in the boreal forest. Ecoscience 11:321–328

    Google Scholar 

  • Dussault C, Ouellet JP, Courtois R, Huot J, Breton L, Jolicoeur H (2005) Linking moose habitat selection to limiting factors. Ecography 28:619–628

    Article  Google Scholar 

  • Edwards J (1983) Diet shifts in moose due to predator avoidance. Oecologia 60:185–189

    Article  Google Scholar 

  • Eriksen A et al (2011) Activity patterns of predator and prey: a simultaneous study of GPS-collared wolves and moose. Anim Behav 81:423–431

    Article  Google Scholar 

  • 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 86:1320–1330

    Article  Google Scholar 

  • 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 365:2187–2200

    Article  Google Scholar 

  • Frid A, Dill LM (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11

    Google Scholar 

  • Gaillard JM et al (2010) Habitat-performance relationships: finding the right metric at a given spatial scale. Philosophical Transactions R Soci B Biol Sci 365:2255–2265

    Article  Google Scholar 

  • 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 489–517

  • 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 81:443–454

    Article  PubMed  Google Scholar 

  • 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 23:1722–1734

  • 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 66:1290–1300

    Article  Google Scholar 

  • Haglund B (1968) De stora rovdjurens vintervanor II. Viltrevy 5:213–361

    Google Scholar 

  • Hebblewhite M, Merrill E (2007) Multiscale wolf predation risk for elk: does migration reduce risk? Oecologia 152:377–387

    Article  PubMed  Google Scholar 

  • 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 80:789–799

    Article  Google Scholar 

  • 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 11:215–220

    Article  Google Scholar 

  • Hunter LTB, Skinner JD (1998) Vigilance behaviour in African ungulates: the role of predation pressure. Behav 135:195–211

    Article  Google Scholar 

  • Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65–71

    Article  Google Scholar 

  • Kauffman MJ, Brodie JF, Jules ES (2010) Are wolves saving Yellowstone’s aspen? A landscape-level test of a behaviorally mediated trophic cascade. Ecology 91:2742–2755

    Article  PubMed  Google Scholar 

  • Kunkel KE, Pletscher DH (2000) Habitat factors affecting vulnerability of moose to predation by wolves in southeastern British Columbia. Can J Zool 78:150–157

    Article  Google Scholar 

  • 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 83:185–198

    Article  PubMed  Google Scholar 

  • 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 79:1401–1409

    Article  Google Scholar 

  • Lavsund S, Nygrén T, Solberg EJ (2003) Status of moose populations and challenges to moose management in Fennoscandia. Alces 39:109–130

    Google Scholar 

  • 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 618

    Google Scholar 

  • Liberg O et al (2011) Monitoring of wolves in Scandinavia

  • Lima SL (1995) Back to the basics of anti-predatory vigilance: the group-size effect. Anim Behav 49:11–20

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Lönnberg E (1934) Bidrag till vargens historia i Sverige. Kungliga Vetenskapsakademins skrifter i naturskyddsärenden 26:1–33

    Google Scholar 

  • 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 45:109–124

    Google Scholar 

  • Månsson J (2009) Environmental variation and moose Alces alces density as determinants of spatio-temporal heterogeneity in browsing. Ecography 32:601–612

    Article  Google Scholar 

  • 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 57:1017–1023

    Article  Google Scholar 

  • Mao JS et al (2005) Habitat selection by elk before and after wolf reintroduction in Yellowstone National Park. J Wildl Manag 69:1691–1707

    Article  Google Scholar 

  • 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 88:875–883

    Article  Google Scholar 

  • Mech LD, Smith DW, Murphy KM, MacNulty (2001) Winter severity and wolf predation on a formerly wolf-free elk herd. J Wildl Manag 65:998–1003

    Article  Google Scholar 

  • 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 81:553–563

    Article  PubMed  Google Scholar 

  • Mohr CO (1947) Table of equivalent populations of North American small mammals. Am Midl Nat 37:223–249

    Article  Google Scholar 

  • 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 89:1013–1018

    Article  Google Scholar 

  • Olsson M, Cox J, Larkin J, Widén P, Olovsson A (2011) Space and habitat use of moose in southwestern Sweden. Eur J Wildl Res 57:241–249

    Article  Google Scholar 

  • 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 20:503–510

    Article  PubMed  Google Scholar 

  • Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509

    Article  Google Scholar 

  • R Development Core Team (2010) R: A language and environment for statistical computing, R Foundation for Statistical Computing, 2.11.1 edn, Vienna, Austria

  • Ripple WJ, Beschta RL (2004) Wolves and the ecology of fear: can predation risk structure ecosystems? Bioscience 54:755–766

    Article  Google Scholar 

  • 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 164:265–275

    Article  PubMed  Google Scholar 

  • 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 14:358–371

    Article  Google Scholar 

  • Sæther BE, Engen S, Lande R (1996) Density-dependence and optimal harvesting of fluctuating populations. Oikos 76:40–46

    Article  Google Scholar 

  • 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 33:914–925

    Article  Google Scholar 

  • 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 273:1421–1427

    Article  Google Scholar 

  • 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 72:781–789

    Article  Google Scholar 

  • 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 156:53–64

    Article  PubMed  Google Scholar 

  • 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 90:403–412

    Article  Google Scholar 

  • 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 71:1419–1426

    Article  Google Scholar 

  • Smith DW, Peterson RO, Houston DB (2003) Yellowstone after wolves. Bioscience 53:330–340

    Article  Google Scholar 

  • 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 78:1822–1830

    Article  Google Scholar 

  • 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 92:398–407

    Article  PubMed  Google Scholar 

  • Valeix M et al (2009) Behavioral adjustments of African herbivores to predation risk by lions: spatio-temporal variations influence habitat use. Ecology 90:23–30

    Article  CAS  PubMed  Google Scholar 

  • 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 79:910–922

    PubMed  Google Scholar 

  • 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 91–97

  • Vijayan S, Morris DW, McLaren BE (2012) Prey habitat selection under shared predation: tradeoffs between risk and competition? Oikos 121:783–789

    Article  Google Scholar 

  • 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 79:710–725

    Article  Google Scholar 

  • 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 Hedmark

  • 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 73:215–225

    Article  Google Scholar 

  • Wirsing AJ, Cameron KE, Heithaus MR (2010) Spatial responses to predators vary with prey escape mode. Anim Behav 79:531–537

    Article  Google Scholar 

  • Worton BJ (1989) Kernel methods for estimating the utilization distribution in home range studies. Ecology 70:164–168

    Article  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

  1. Department of Ecology, Grimsö Wildlife Research Station, Swedish University of Agricultural Sciences, 730 91, Riddarhyttan, Sweden

    Kerry L. Nicholson, Cyril Milleret, Johan Månsson & Håkan Sand

  2. Faculty of Forestry and Wildlife Management, Hedmark University College, Evenstad, 2480, Koppang, Norway

    Cyril Milleret

Authors
  1. Kerry L. Nicholson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cyril Milleret
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Johan Månsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Håkan Sand
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kerry L. Nicholson.

Additional information

Communicated by Ilpo Kojola.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nicholson, K.L., Milleret, C., Månsson, J. et al. Testing the risk of predation hypothesis: the influence of recolonizing wolves on habitat use by moose. Oecologia 176, 69–80 (2014). https://doi.org/10.1007/s00442-014-3004-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-3004-9

Keywords

Search

Navigation