Journal of Ethology

, Volume 37, Issue 1, pp 47–58 | Cite as

Personality influences habituation behaviour in ungulates

  • Rob FoundEmail author


The habituation of wildlife to humans is a growing global problem that damages ecological integrity and threatens public safety, but the behavioural processes underlying habituation have rarely been explicitly tested in large animals. These processes are also likely influenced by animal personality. I used three personality traits to delineate a gradient of “shy” to “bold” personality types in captive elk (Cervus canadensis). I then attempted to habituate elk using either food attractants paired with inactive human presence, or with human approaches but no food attractants. Both food and approach treatments significantly reduced elk wariness, as measured by mean flight response distances, while elk in a control pen showed no change. During approach treatments bolder elk showed significantly larger reductions in wariness than shyer elk, but personality had no influence on wariness reductions after food conditioning. My results demonstrate that habituation can be proactive, whereby animals overcome wariness as a way to reap rewards, but can also be reactive, whereby animals can be forced to habituate through the repeated exposure to negative stimuli to which wariness responses are energetically costly. I showed that changes in optimality decisions surrounding risk and reward are influenced by the personalities of individual animals.


Elk Human-wildlife conflict Learning Individual variation Wariness Ecological integrity 



I would like to thank Amberlane Farm and the Bulten family, Colleen St. Clair, the Alberta Elk Commission, Parks Canada (Banff and Jasper), the Alberta Conservation Association, the Animal Behavior Society, the Alberta Sports, Parks, Recreation and Wildlife Foundation, the Canadian Circumpolar Institute, the Northern Alberta Chapter of Safari Club International, and the Natural Sciences and Engineering Research Council.


  1. Andreatta M, Pauli P (2015) Appetitive vs. aversive conditioning in humans. Front Behav Neurosci 9:128CrossRefPubMedPubMedCentralGoogle Scholar
  2. Atwell JW, Cardoso GC, Whittaker DJ, Campbell-Nelson S, Robertson KW, Ketterson ED (2012) Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation. Behav Ecol 23:960–969CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bejder L, Samuels A, Whitehead H, Finn H, Allen S (2009) Impact assessment research: use and misuse of habituation, sensitization and tolerance in describing wildlife responses to anthropogenic stimuli. Mar Ecol Prog Ser 395:177–185CrossRefGoogle Scholar
  4. Berger J (2004) The last mile: how to sustain long-distance migration in mammals. Conserv Biol 18:320–331CrossRefGoogle Scholar
  5. Blanchard BM, Knight RR (1991) Movements of Yellowstone grizzly bears. Biol Cons 58:41–67CrossRefGoogle Scholar
  6. Blumstein DT (2016) Habituation and sensitization: new thoughts about old ideas. Anim Behav 120:255–262CrossRefGoogle Scholar
  7. Box HO, Gibson KR (1999) Mammalian social learning: comparative and ecological perspectives. Cambridge University Press, LondonGoogle Scholar
  8. Boyce MS (1991) Migratory behavior and management of elk (Cervus elaphus). Appl Anim Behav Sci 29:239–250CrossRefGoogle Scholar
  9. Ciuti S, Northrup JM, Muhly TB, Simi S, Musiani M, Pitt JA, Boyce MS (2012) Effects of humans on behaviour of wildlife exceed those of natural predators in a landscape of fear. PLOS One 7(11):e50611CrossRefPubMedPubMedCentralGoogle Scholar
  10. Clutton-Brock J (1992) The process of domestication. Mamm Rev 22:79–85CrossRefGoogle Scholar
  11. Conover M (2002) Resolving human-wildlife conflicts: the science of wildlife damage management. Lewis, Boca RatonGoogle Scholar
  12. Davis H, Heslop E (2004) Habituation of hissing by Madagascar hissing cockroaches (Gromphadorhina portentosa): evidence of discrimination between humans? Behav Proc 67:539–543CrossRefGoogle Scholar
  13. Desforges MF, Wood-Gush DGM (1975) A behavioural comparison of domestic and Mallard ducks habituation and flight reactions. Anim Behav 23:692–697CrossRefGoogle Scholar
  14. Domjan M (2010) The principles of learning and behavior, 6th edn. Wadsworth, BelmontGoogle Scholar
  15. Doran-Sheehy DM, Derby AM, Greer D, Mongo P (2007) Habituation of Western gorillas: the process and factors that influence it. Am J Primatol 69:1354–1369CrossRefPubMedGoogle Scholar
  16. Driscoll CA, MacDonald DW, O’Brien SJ (2009) From wild animals to domestic pets, an evolutionary view of domestication. Proc Natl Acad Sci 109:9971–9978CrossRefGoogle Scholar
  17. Ensminger AL, Westneat DF (2012) Individual and sex differences in habituation and neophobia in house sparrows (Passer domesticus). Ethology 118:1085–1095CrossRefGoogle Scholar
  18. Ferrari MCO, Elvidge CK, Jackson CD, Chivers DP, Brown GE (2010) The responses of prey fish to temporal variation in predation risk: sensory habituation or risk assessment? Behav Ecol. CrossRefGoogle Scholar
  19. Found RF, St. Clair CC (2016) Behavioural syndromes predict loss of migration in wild elk. Anim Behav 115:35–46CrossRefGoogle Scholar
  20. Found RF, St. Clair CC (2017) Ambidextrous ungulates have more flexible behaviour, bolder personalities and migrate less. R Soc Open Sci 4:160958. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Found RF, St. Clair CC (2018) Elk personality and response to management. J Wildl Manage. CrossRefGoogle Scholar
  22. Frair JL, Merrill EH, Allen JR, Boyce MS (2007) Know thy enemy: experience affects elk translocation success in risky landscapes. J Wildl Manage 71:541–554CrossRefGoogle Scholar
  23. Gates C, Hudson RJ (1978) Energy costs of locomotion in wapiti. Acta Theriol 23:365–370CrossRefGoogle Scholar
  24. Geist V (1982) Adaptive behavioural strategies. In: Thomas JW, Toweill DE (eds) Elk of North America: ecology and management. Stackpole, HarrisburgGoogle Scholar
  25. Gilbert PE, Piogovsky E, Brushfield AM, Luu TT, Tolentino JC, Renteria AF (2009) Age-related changes in associative learning for olfactory and visual stimuli in rodents. Ann NY Acad Sci 1170:718–724CrossRefPubMedGoogle Scholar
  26. Goldberg JF, Hebblewhite M, Bardsley J (2014) Consequences of a refuge for the predator-prey dynamics of a wolf-elk system in Banff National Park, Alberta, Canada. PLoS One 9(3):e91417. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636CrossRefPubMedGoogle Scholar
  28. Hebblewhite M, Merrill E (2009) Trade-offs between predation risk and forage differ between migrant strategies in a migratory ungulate. Ecology 90:3445–3454CrossRefPubMedGoogle Scholar
  29. Houston AI, McNamara JM (2014) Foraging currencies, metabolism and behavioural routines. J Anim Ecol 83:30–40CrossRefPubMedGoogle Scholar
  30. Koolhaas JM, de Boer SF, Buwalda B, van Reenan K (2007) Individual variation in coping with stress: a multidimensional approach of ultimate and proximate mechanisms. Brain Behav Evol 70:218–226CrossRefPubMedGoogle Scholar
  31. Laundre JW, Hernandez 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
  32. Li C, Monclus R, Maul TL, Jiang Z, Blumstein DT (2011) Quantifying human disturbance on antipredator behavior and flush initiation distance in yellow-bellied marmots. Appl Anim Behav Sci 129:146–152CrossRefGoogle Scholar
  33. Linnell JDC, Odden J, Smith ME, Aanes R, Swenson JE (1999) Large carnivores that kill livestock: do “problem individuals” really exist? Wildl Soc Bull 27:698–705Google Scholar
  34. Lowry H, Lill A, Wong BBM (2013) Behavioural responses of wildlife to urban environments. Biol Rev 88:537–549CrossRefGoogle Scholar
  35. Mackenzie J (2001) The demographic and nutritional benefits of urban habitat use by elk. Thesis, University of GuelphGoogle Scholar
  36. Malo JE, Acebes P, Traba J (2011) Measuring ungulate tolerance to human with flight distance: a reliable visitor management tool? Biol Cons 20:3477–3488CrossRefGoogle Scholar
  37. May R, Landa A, van Dijk J, Linnell JDC, Andersen R (2006) Impact of infrastructure on habitat selection of wolverines Gulo gulo. Wildl Biol 12:285–295CrossRefGoogle Scholar
  38. Messmer TA (2009) Human-wildlife conflicts: emerging opportunities. Hum Wildl Confl 3:10–17Google Scholar
  39. Morrison H (1998) Grain problems in national parks. Pro-Farm 14:44–45Google Scholar
  40. Murray MH, Hill J, Whyte P, St. Clair CC (2016) Urban compost attracts coyotes, contains toxins, and may promote disease in urban-adapted wildlife. EcoHealth 13:2. CrossRefGoogle Scholar
  41. Mysterud A (2013) Ungulate migration, plant phenology, and large carnivores: the times they are a-changin’. Ecology 94:1257–1261CrossRefPubMedGoogle Scholar
  42. Parker GA, Maynard Smith J (1990) Optimality theory in evolutionary biology. Nature 348:27–33CrossRefGoogle Scholar
  43. Pooley S, Barua M, Beinart W, Dickman A, Holmes G, Lorimer J, Loveridge AJ, Macdonald DW, Marvin G, Redpath S, Sillero-Zubriri C, Zimmermann A, Milner-Gulland EJ (2016) An interdisciplinary review of current and future approaches to improving human-predator relations. Conserv Biol 31:513–523CrossRefGoogle Scholar
  44. Price EO (1999) Behavioral development in animals undergoing domestication. Appl Anim Behav Sci 65:245–271CrossRefGoogle Scholar
  45. Proffitt KM, Grigg JL, Hamlin KL, Garrott RA (2009) Contrasting effects of wolves and human hunters on elk behavioral responses to predation risk. J Wildl Manage 73:345–356CrossRefGoogle Scholar
  46. Reale D, Martin J, Coltman DW, Poissant J, Festa-Bianchet M (2009) Male personality, life-history strategies and reproductive success in a promiscuous mammal. J Evol Biol 22:1599–1607CrossRefPubMedGoogle Scholar
  47. Reimers E, Colman JE (2003) Reindeer and caribou (Rangifer tarandus) response towards human activities. Rangifer 26:55–71CrossRefGoogle Scholar
  48. Rodriguez-Prieto I, Martin J, Fernandex-Juricic E (2010) Habituation to low-risk predators improves body condition in lizards. Behav Ecol Sociobiol 64:1937–1945CrossRefGoogle Scholar
  49. Samuni L, Mundry R, Terkel J, Zuberbuhler K, Hobaiter C (2014) Socially learned habituation to human observers in wild chimpanzees. Anim Cogn 17:997–1005CrossRefPubMedGoogle Scholar
  50. Shannon G, Cordes LS, Hardy AR, Angeloni LM, Crooks KR (2014) Behavioral responses associated with a human-mediated predator shelter. PLoS One 9(4):e94630. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289CrossRefGoogle Scholar
  52. Sneddon LU (2003) The bold and the shy: individual differences in rainbow trout. J Fish Biol 62:971–975CrossRefGoogle Scholar
  53. Stankowich T (2008) Ungulate flight responses to human disturbance: a review and meta-analysis. Biol Cons 141:2159–2173CrossRefGoogle Scholar
  54. Tarlow EM, Blumstein DT (2007) Evaluating methods to quantify anthropogenic stressors on wild animals. Appl Anim Behav Sci 102:429–451CrossRefGoogle Scholar
  55. Thompson MJ, Henderson RE (1998) Elk habituation as a credibility challenge for wildlife professionals. Wildl Soc Bull 26:477–483Google Scholar
  56. Vincze E, Papp S, Preiszner B, Seress G, Bokony V, Liker A (2016) Habituation to human disturbance is faster in urban than rural house sparrows. Behav Ecol 27:1304–1313CrossRefGoogle Scholar
  57. Vors LS, Boyce MS (2009) Global declines of caribou and reindeer. Glob Change Biol 15:2626–2633CrossRefGoogle Scholar
  58. Walter WD, Lavelle MJ, Fischer JW, Johnson TL, Hygnstrom SE, VerCauteren KC (2010) Management of damage by elk (Cervus elaphus) in North America: a review. Wildl Res 37:630–646CrossRefGoogle Scholar
  59. Wam HK, Eldegard K, Hjeljord O (2014) Minor habituation to repeated experimental approaches in Scandinavian wolves. Eur J Wildl Res 60:839–842CrossRefGoogle Scholar
  60. Whitaker D, Knight RL (1998) Understanding wildlife responses to humans. Wildl Soc Bull 26:217–312Google Scholar
  61. Wolf ID, Croft DB (2010) Minimizing disturbance to wildlife by tourists approaching on foot or in a car: a study of kangaroos in the Australian rangelands. Appl Anim Behav Sci 126:75–84CrossRefGoogle Scholar
  62. Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Study Behav 16:229–249CrossRefGoogle Scholar
  63. Zala SM, Maattanen I, Penn DJ (2012) Different social-learning strategies in wild and domesticated zebrafish, Danio rerio. Anim Behav 83:1519–1525CrossRefGoogle Scholar

Copyright information

© Japan Ethological Society and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  2. 2.Elk Island National ParkParks CanadaFort SaskatchewanCanada

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