, Volume 189, Issue 2, pp 487–500 | Cite as

Habitat use of sympatric prey suggests divergent anti-predator responses to recolonizing gray wolves

  • Justin A. DellingerEmail author
  • Carolyn R. Shores
  • Apryle Craig
  • Michael R. Heithaus
  • William J. Ripple
  • Aaron J. Wirsing
Community ecology – original research


The non-consumptive effects of predators on prey are now widely recognized, but the need remains for studies identifying the factors that determine how particular prey species respond behaviorally when threatened with predation. We took advantage of ongoing gray wolf (Canis lupus) recolonization in eastern Washington, USA, to contrast habitat use of two sympatric prey species—mule (Odocoileus hemionus) and white-tailed (O. virginianus) deer—at sites with and without established wolf packs. Under the hypothesis that the nature and scale of responses by these ungulates to wolf predation risk depend on their divergent flight tactics (i.e., modes of fleeing from an approaching predator), we predicted that (1) mule deer would respond to wolves with coarse-scale spatial shifts to rugged terrain favoring their stotting tactic; (2) white-tailed deer would manage wolf risk with fine-scale shifts toward gentle terrain facilitating their galloping tactic within their current home range. Resource selection functions based on 61 mule deer and 59 white-tailed deer equipped with GPS radio-collars from 2013 to 2016 revealed that habitat use for each species was altered by wolf presence, but in divergent ways that supported our predictions. Our findings add to a growing literature highlighting flight behavior as a viable predictor of prey responses to predation risk across multiple ecosystem types. Consequently, they suggest that predators could initiate multiple indirect non-consumptive effects in the same ecosystem that are transmitted by divergent responses of sympatric prey with different flight tactics.


Canis lupus Galloping Mule deer Non-consumptive effects Odocoileus hemionus O. virginianus Predation risk Stotting White-tailed deer 



We are grateful to the Colville Tribes Fish and Wildlife Department, and especially to E. Krausz and R. Whitney, for permission to access their lands, guidance, logistical support, and comments on an earlier version of the manuscript. We also thank the Okanogan-Wenatchee National Forest, and especially M. Marsh, for guidance and logistical support. Field assistance was provided by M. Bianco, K. Ebenhoch, J. Fournier, A. Smethurst, K. Perensovich, S. Stark, C. Montgomerie, B. Woodruff, I. Hull, C. Whitney, and TC Walker. Valuable field training was provided by W. Myers and J. Kujala.

Author contribution statement

AJW, MRH, and WJR originally conceptualized the study. JAD, CRS, and AC contributed to fieldwork. JAD analyzed the data and led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.


This project was carried out under NSF DEB grants 1145902 (AJW) and 1145522 (MRH). Additional funding was provided by the Safari Club International Foundation, Conservation Northwest, the Washington Department of Fish and Wildlife (Aquatic Lands Enhancement Account, ALEA: AJW and JAD), the University of Washington Student Technology Fee (STF: CRS and JAD) program, and the University of Washington USEED program (AJW, JAD, CRS, and AC).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

442_2018_4323_MOESM1_ESM.docx (256 kb)
Supplementary material 1 (DOCX 256 kb)


  1. Atwood TC, Gese EM, Kunkel KE (2009) Spatial partitioning of predation risk in a multiple predator-multiple prey system. J Wildl Manag 73:876–884CrossRefGoogle Scholar
  2. Benson JF (2013) Improving rigour and efficiency of use-availability habitat selection analyses with systematic estimation of availability. Methods Ecol Evol 4:244–251CrossRefGoogle Scholar
  3. Beyer HL (2015) Geospatial modelling environment (Version URL: Accessed 10 Jan 2018
  4. Bonar M, Manseau M, Geisheimer J, Bannatyne T, Lingle S (2016) The effect of terrain and female density on survival of neonatal white-tailed deer and mule deer fawns. Ecol Evol 6:4387–4402CrossRefPubMedGoogle Scholar
  5. Bowyer RT (1987) Coyote group size relative to predation on mule deer. Mammalia 51:515–526CrossRefGoogle Scholar
  6. Boyce MS, Vernier PR, Nielsen SE, Schmiegelow FK (2002) Evaluating resource selection functions. Ecol Modelling 157:281–300CrossRefGoogle Scholar
  7. Catano LB, Rojas MC, Malossi RJ, Peters JR, Heithaus MR, Fourqurean JW, Burkepile DE (2016) Reefscapes of fear: predation risk and reef heterogeneity interact to shape herbivore foraging behavior. J Anim Ecol 85:146–156CrossRefPubMedGoogle Scholar
  8. Clausnitzer RR, Zamora BA (1987) Forest habitat types of the Colville Indian Reservation. Pullman, Washington State University. Department of Forestry and Range Management, WashingtonGoogle Scholar
  9. Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201CrossRefPubMedGoogle Scholar
  10. Creel S, Schutte P, Christianson D (2014) Effects of predation risk on group size, vigilance, and foraging behavior in an African ungulate community. Behav Ecol 25:773–784CrossRefGoogle Scholar
  11. Crowell MM, Shipley LA, Camp MJ, Rachlow JL, Forbey JS, Johnson TR (2016) Selection of food patches by sympatric herbivores in response to concealment and distance from a refuge. Ecol Evol 6:2865–2876CrossRefPubMedGoogle Scholar
  12. Dellinger JA, Proctor C, Steury TD, Kelly MJ, Vaughan MR (2013) Habitat selection of a large carnivore, the red wolf, in a human-altered landscape. Biol Conserv 157:324–330CrossRefGoogle Scholar
  13. Dellinger JA, Shores CR, Marsh M, Heithaus MR, Ripple WJ, Wirsing AJ (2018) Impacts of recolonizing gray wolves (Canis lupus) on survival and mortality in two sympatric ungulates. Can J Zool 96:760–768CrossRefGoogle Scholar
  14. Dorresteijn I, Schultner J, Nimmo DG, Fischer J, Hanspach J, Kuemmerle T, Kehoe L, Ritchie EG (2015) Incorporating anthropogenic effects into trophic ecology: predator-prey interactions in a human-dominated landscape. Proc R Soc B 282:20151602CrossRefPubMedGoogle Scholar
  15. Ford AT, Goheen JR (2015) Trophic cascades by large carnivores: a case for strong inference and mechanism. Trend Ecol Evol 30:725–735CrossRefGoogle Scholar
  16. 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
  17. Geist V (1981) Behavior: adaptive strategies in mule deer. In: Wallmo OC (ed) Mule and black-tailed deer of North America. University of Nebraska Press, Lincoln, pp 157–224Google Scholar
  18. Gervasi V, Sand H, Zimmermann 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 23:1722–1734CrossRefPubMedGoogle Scholar
  19. Haulton SM, Porter WF, Rudolph BA (2001) Evaluating 4 methods to capture white-tailed deer. Wildl Soc Bull 29:255–264Google Scholar
  20. Hebblewhite M, Merrill EH, McDonald TL (2005) Spatial decomposition of predation risk using resource selection functions: an example in a wolf-elk predator-prey system. Oikos 111:101–111CrossRefGoogle Scholar
  21. Heithaus MR, Wirsing AJ, Burkholder D, Thomson J, Dill LM (2009) Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics. J Anim Ecol 78:556–562CrossRefPubMedGoogle Scholar
  22. Heithaus MR, Wirsing AJ, Dill LM (2012) The ecological importance of intact top-predator populations: a synthesis of 15 years of research in a seagrass ecosystem. Mar Freshw Res 63:1039–1050CrossRefGoogle Scholar
  23. Hernandez L, Laundre 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
  24. Jimenez MD, Becker SA (2016) Northern Rocky Mountain Wolf Recovery Program 2015 Interagency Annual Report. US Fish and Wildlife Service, Ecological Services, 585 Shepard Way, Helena, Montana, 59601Google Scholar
  25. Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65–71CrossRefGoogle Scholar
  26. Johnson CJ, Nielsen SE, Merrill EH, McDonald TL, Boyce MS (2006) Resource selection functions based on use-availability data: theoretical motivation and evaluation methods. J Wildl Manag 70:347–357CrossRefGoogle Scholar
  27. Kauffman MJ, Varley N, Smith DW, Stahler DR, MacNulty DR, Boyce MS (2007) Landscape heterogeneity shapes predation in a newly restored predator-prey system. Ecol Lett 10:690–700CrossRefPubMedGoogle Scholar
  28. Kilgo JC, Labisky RF, Fritzen DE (1998) Influences of hunting on the behavior of white-tailed deer: implications for conservation of the Florida panther. Conserv Biol 12:1359–1364CrossRefGoogle Scholar
  29. Kittle AM, Fryxell JM, Desy GE, Hamr J (2008) The scale-dependent impact of wolf predation risk on resource selection by three sympatric ungulates. Oecologia 157:163–175CrossRefPubMedGoogle Scholar
  30. Kuijper DPJ, Bubnicki JW, Churski M, Mols B, Van Hooft P (2015) Context dependence of risk effects: wolves and tree logs create patches of fear in an old-growth forest. Behav Ecol 26:1558–1568CrossRefGoogle Scholar
  31. Kuijper DPJ, Sahlen E, Elmhagen B, Chamaille-Jammes S, Sand H, Lone K, Cromsigt JPGM (2016) Paws without claws? Ecological effects of large carnivores in anthropogenic landscapes. Proc R Soc B 283:20161625. CrossRefPubMedGoogle Scholar
  32. Kunkel K, Pletscher DH (2001) Winter hunting patterns of wolves in and near Glacier National Park, Montana. J Wildl Manag 65:520–530CrossRefGoogle Scholar
  33. 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 83:185–198CrossRefPubMedGoogle Scholar
  34. Laundré JW, Hernández L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7CrossRefGoogle Scholar
  35. Lima SL (2002) Putting predators back into behavioral predator-prey interactions. Trends Ecol Evol 17:70–75CrossRefGoogle Scholar
  36. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  37. Lingle S (2002) Coyote predation and habitat segregation of white-tailed deer and mule deer. Ecology 83:2037–2048CrossRefGoogle Scholar
  38. Lingle S, Pellis S (2002) Fight or flight? Antipredator behavior and the escalation of coyote encounters with deer. Oecologia 131:154–164CrossRefPubMedGoogle Scholar
  39. Lone K, Loe LE, Gobakken T, Linnell JDC, Odden J, Remmen J, Mysterud A (2014) Living and dying in a multi-predator landscape of fear: roe deer are squeezed by contrasting pattern of predation risk imposed by lynx and humans. Oikos 123:641–651CrossRefGoogle Scholar
  40. Makin DF, Chamaille-Jammes S, Shrader AM (2017) Changes in feeding behavior and patch use by herbivores in response to the introduction of a new predator. J Mammal 99:341–350CrossRefGoogle Scholar
  41. Manly BFJ, McDonald LL, Thomas DL, McDonald TL, Erickson WP (2002) Resource selection by animals: statistical analysis and design for field studies, 2nd edn. Kluwer, BostonGoogle Scholar
  42. Martin J, Owen-Smith N (2016) Habitat selectivity influences the reactive responses of African ungulates to encounters with lions. Anim Behav 116:163–170CrossRefGoogle Scholar
  43. Mech LD, Peterson RO (2003) Wolf-prey relations. In: Mech LD, Boitani L (eds) Wolves: behavior, ecology, and conservation. University of Chicago Press, Chicago, IL, USA, pp 131–160CrossRefGoogle Scholar
  44. Middleton AD, Kauffman MJ, McWhirter DE, Cook JG, Cook RC, Nelson AA, Jimenez MD, Klaver RW (2013) Animal migration amid shifting patterns of phenology and predation: lessons from a Yellowstone elk herd. Ecology 94:1245–1256CrossRefPubMedGoogle Scholar
  45. Nelson ME, Mech LD (1991) Wolf predation risk associated with white-tailed deer movements. Can J Zool 69:2696–2699CrossRefGoogle Scholar
  46. Nelson EH, Matthews CE, Rosenheim JA (2004) Predators reduce prey population growth by inducing changes in prey behavior. Ecology 85:1853–1858CrossRefGoogle Scholar
  47. Nielson RM, Manly BFJ, McDonald LL, Sawyer H, McDonald TL (2009) Estimating habitat selection when GPS fix success is less than 100%. Ecology 90:2956–2962CrossRefPubMedGoogle Scholar
  48. Oakleaf JK, Murray DL, Oakleaf JR, Bangs EE, Mack CM, Smith DW, Fontaine JA, Jimenez MD, Meier TJ, Niemeyer CC (2006) Habitat selection by recolonizing wolves in the northern Rocky Mountains of the United States. J Wildl Manag 70:554–563CrossRefGoogle Scholar
  49. Padie S, Morellet N, Hewison AJ, Martin JL, Bonnot N, Cargnelutti B, Chamaille-Jammes S (2015) Roe deer at risk: teasing apart habitat selection and landscape constraints in risk exposure at multiple scales. Oikos 124:1536–1546CrossRefGoogle Scholar
  50. Pierce BM, Bowyer RT, Bleich VC (2004) Habitat selection by mule deer: forage benefits or risk of predation? J Wildl Manag 68:533–541CrossRefGoogle Scholar
  51. R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: Accessed 5 Feb 2018
  52. Ripple WJ, Beschta RL (2012) Trophic cascades in Yellowstone: the first 15 years after wolf reintroduction. Biol Conserv 145:205–213CrossRefGoogle Scholar
  53. Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP, Schmitz OJ, Smith DW, Wallach AD, Wirsing AJ (2014) Status and ecological effects of the world’s largest carnivores. Science 343:1241484CrossRefPubMedGoogle Scholar
  54. Robinson HS, Wielgus RB, Gwilliam JC (2002) Cougar predation and population growth of sympatric mule deer and white-tailed deer. Can J Zool 80:556–568CrossRefGoogle Scholar
  55. Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem functioning. Science 319:952–954CrossRefPubMedGoogle Scholar
  56. Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399CrossRefGoogle Scholar
  57. Spence G (2017) Wolf predation on livestock in Washington. Thesis. Washington State University, Pullman, WA, USAGoogle Scholar
  58. Swenson JE (1982) Effects of hunting on habitat use by mule deer on mixed-grass prairie in Montana. Wildl Soc Bull 10:115–120Google Scholar
  59. Thaker MA, Vanak T, 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 92:398–407CrossRefPubMedGoogle Scholar
  60. United States Census Bureau (2016) TIGER/Line Shapefiles. Available from Accessed 5 Jan 2018
  61. United States Geological Survey (2011) National gap analysis program: Accessed 5 Jan 2018
  62. Whittington J, Hebblewhite M, DeCesare NJ, Neufield L, Bradley M, Wilmshurst J, Musiani M (2011) Caribou encounters with wolves increase near roads and trails: a time-to-event approach. J Appl Ecol 48:1535–1542CrossRefGoogle Scholar
  63. Wirsing AJ, Ripple WJ (2011) A comparison of shark and wolf research reveals similar behavioral responses by prey. Front Ecol Environ 9:335–341CrossRefGoogle Scholar
  64. Wirsing AJ, Cameron KE, Heithaus MR (2010) Spatial responses to predators vary with prey escape mode. Anim Behav 79:531–537CrossRefGoogle Scholar
  65. Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Study Behav 16:229–249CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Justin A. Dellinger
    • 1
    • 2
    Email author
  • Carolyn R. Shores
    • 1
  • Apryle Craig
    • 1
  • Michael R. Heithaus
    • 3
  • William J. Ripple
    • 4
  • Aaron J. Wirsing
    • 1
  1. 1.School of Environmental and Forest SciencesUniversity of WashingtonSeattleUSA
  2. 2.Wildlife Investigations LabCalifornia Department of Fish and WildlifeRancho CordovaUSA
  3. 3.Department of Biological SciencesFlorida International UniversityNorth MiamiUSA
  4. 4.Global Trophic Cascades Program, Department of Forest Ecosystems and SocietyOregon State UniversityCorvallisUSA

Personalised recommendations