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Innate threat-sensitive foraging: black-tailed deer remain more fearful of wolf than of the less dangerous black bear even after 100 years of wolf absence

  • Behavioral ecology - Original research
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Abstract

Anti-predator behaviors often entail foraging costs, and thus prey response to predator cues should be adjusted to the level of risk (threat-sensitive foraging). Simultaneously dangerous predators (with high hunting success) should engender the evolution of innate predator recognition and appropriate anti-predator behaviors that are effective even upon the first encounter with the predator. The above leads to the prediction that prey might respond more strongly to cues of dangerous predators that are absent, than to cues of less dangerous predators that are actually present. In an applied context this would predict an immediate and stronger response of ungulates to the return of top predators such as wolves (Canis lupus) in many parts of Europe and North America than to current, less threatening, mesopredators. We investigated the existence of innate threat-sensitive foraging in black-tailed deer. We took advantage of a quasi-experimental situation where deer had not experienced wolf predation for ca. 100 years, and were only potentially exposed to black bears (Ursus americanus). We tested the response of deer to the urine of wolf (dangerous) and black bear (less dangerous). Our results support the hypothesis of innate threat-sensitive foraging with clear increased passive avoidance and olfactory investigation of cues from wolf, and surprisingly none to black bear. Prey which have previously evolved under high risk of predation by wolves may react strongly to the return of wolf cues in their environments thanks to innate responses retained during the period of predator absence, and this could be the source of far stronger non-consumptive effects of the predator guild than currently observed.

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References

  • Amo L, López P, Martín J, Fox SF (2004) Chemosensory recognition and behavioral responses of wall lizards, Podarcis muralis, to scents of snakes that pose different risks of predation. Copeia 3:691–696

    Article  Google Scholar 

  • Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144

    Article  PubMed  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 

  • Blumstein D (2002) Moving to suburbia: ontogenetic and evolutionary consequences of life on predator-free islands. J Biogeogr 29:685–692

    Article  Google Scholar 

  • Blumstein DT (2006) The multi-predator hypothesis and the evolutionary persistence of antipredator behavior. Ethology 112:209–217

    Article  Google Scholar 

  • Blumstein DT, Bitton A, DaVeiga J (2006) How does the presence of predators influence the persistence of antipredator behavior? J Theor Biol 239:460–468

    Article  PubMed  Google Scholar 

  • Blumstein DT, Barrow L, Luterra M (2008) Olfactory predator discrimination in yellow-bellied marmots. Ethology 114:1135–1143

    Article  Google Scholar 

  • Boitani L (2003) Wolf conservation and recovery. In: Mech D, Boitani L (eds) Wolves. Behavior, ecology and conservation. University of Chicago Press, Chicago, pp 317–340

    Google Scholar 

  • Botham MS, Kerfoot CJ, Louca V, Krause J (2006) The effects of different predator species on antipredator behavior in the Trinidadian guppy, Poecilia reticulata. Naturwissenschaften 93:431–439

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Brown GE, Ferrari MCO, Chivers DP (2011) Learning about danger: chemical alarm cues and threat-sensitive assessment of predation risk by fishes. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior. Blackwell, Oxford, p 472

    Chapter  Google Scholar 

  • Bytheway JP, Carthey AJR, Banks PB (2013) Risk versus reward: how predators and prey respond to aging olfactory cues. Behav Ecol Sociobiol 67:715–725

    Article  Google Scholar 

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

    Google Scholar 

  • Coss RG (1999) Effects of relaxed selection on the evolution of behavior. In: Foster SA, Endler JA (eds) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, New York, pp 181–208

    Google Scholar 

  • Coss RG, Ramakrishnan U (2000) Perceptual aspects of predator recognition by wild bonnet macaques (Macaca radiata). Behaviour 137:315–335

    Article  Google Scholar 

  • Cowan IMcT (1956) What and where are the mule and black-tailed deer? In: Taylor WP (ed) The deer of North America. Stockpole, Wildlife Management Institute, Washington, pp 335–359

    Google Scholar 

  • Curio E (1993) Proximate and developmental aspects of antipredator behavior. Adv Stud Behav 22:135–238

    Article  Google Scholar 

  • Darimont CT, Price MHH, Winchester NN, Gordon-Walker J, Paquet PC (2004) Predators in natural fragments: foraging ecology of wolves in British Columbia’s central and north coast archipelago. J Biogeogr 31:1867–1877

    Article  Google Scholar 

  • Durand J, Legrand A, Tort M, Thiney A, Michniewicz RJ, Coulon A, Aubret F (2012) Effects of geographic isolation on anti-snakes responses in the wall lizard, Podarcis muralis. Amphib-Reptil 33:199–206

    Article  Google Scholar 

  • Fendt M (2006) Exposures to urine of canids or felids, but not of herbivores, induces defensive behavior in laboratory rats. J Chem Ecol 32:2617–2627

    Article  CAS  PubMed  Google Scholar 

  • Golumbia T, Bland L, Moore K, Bartier P (2008) History and current status of introduced vertebrates on Haida Gwaii. Lessons from the Islands Introduced species and what they tell us about how ecosystems work. In: Gaston AJ, Golumbia TE, Martin J-L, Sharpe ST (eds) Proceedings from the Research Group on Introduced Species 2002 symposium, Queen Charlotte City, Queen Charlotte Islands, British Columbia. Canadian Wildlife Service, Environment Canada, Ottawa, pp 8–31

    Google Scholar 

  • Gonzalo A, López P, Martín J (2008) Avoidance responses to scents of snakes that pose different risks of predation by adult natterjack toads, Bufo calamita. Can J Zool 86:928–932

    Article  Google Scholar 

  • Griffin AS (2004) Social learning about predators: a review and prospectus. Learn Behav 32:131–140

    Article  CAS  PubMed  Google Scholar 

  • Helfman G (1989) Threat-sensitive predator avoidance in damselfish–trumpetfish interactions. Behav Ecol Sociobiol 24:47–58

    Article  Google Scholar 

  • Herberich E, Sikorski J, Hothorn T (2010) A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PLoS One 5:e9788

    Article  PubMed Central  PubMed  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometr J 50:346–363

    Article  Google Scholar 

  • Hughes NK, Kelley JL, Banks PB (2009) Receiving behaviour is sensitive to risks from eavesdropping predators. Oecologia 160:609–617

    Article  PubMed  Google Scholar 

  • Hunter LTB, Skinner JD (1988) Vigilance behaviour in African ungulates: the role of predation pressure. Behaviour 135:195–211

    Article  Google Scholar 

  • Kelley JL, Evans JP, Ramnarine IW, Magurran AE (2003) Back to school: can antipredator behaviour in guppies be enhanced through social learning? Anim Behav 65:655–662

    Article  Google Scholar 

  • Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Ithohara S, Kikusui T, Mori K, Sakano H (2007) Innate versus learned odour processing in the mouse olfactory bulb. Nature 450:503–510

    Article  CAS  PubMed  Google Scholar 

  • Lathi DC, Johnson NA, Ajie BC, Otto SP, Hendry AP, Blumstein DT, Coss RG, Donohue K, Foster SA (2009) Relaxed selection in the wild. Trends Ecol Evol 24:487–496

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Li C, Yang X, Ding Y, Zhang L, Fang H, Tang S, Jiang Z (2011) Do Père David’s deer lose memories of their ancestral predators? PLoS One 6:e23623

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lima SL (1998) Stress and decisions making under the risk of predation: recent developments from behavioral, reproductive and ecological perspectives. Adv Stud Behav 27:215–290

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Martin J-L, Stockton SA, Allombert S, Gaston AJ (2010) Top-down and bottom-up consequences of unchecked ungulate browsing on plant and animal diversity in temperate forests: lessons from a deer introduction. Biol Invasions 12:353–371

    Article  Google Scholar 

  • Mech LD, Peterson RO (2003) Wolf-prey relations. In: Mech LD, Boitani L (eds) Wolves. Behaviour, ecology and conservation. University of Chicago Press, Chicago, pp 131–160

    Chapter  Google Scholar 

  • Mery F, Burns JG (2010) Behavioral plasticity: an interaction between evolution and experience. Evol Ecol 24:571–583

    Article  Google Scholar 

  • Miller JR, Ament JM, Schmitz OJ (2013) Fear on the move: predator hunting mode predicts variation in prey mortality and plasticity in prey spatial response. J Anim Ecol. doi:10.1111/1365-2656.12111

    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 

  • Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Brashares JS (2009) The rise of the mesopredator. Bioscience 59:779–791

    Article  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. URL http://www.R-project.org/

  • Ritchie EG, Elmhagen B, Glen AS, Letnic M, Ludwig G, McDonald RA (2012) Ecosystem restoration with teeth: what role for predators? Trends Ecol Evol 27:265–271

    Article  PubMed  Google Scholar 

  • Stankowich T, Coss RG (2007) The re-emergence of felid camouflage with the decay of predator recognition in deer under relaxed selection. Proc R Soc Lond Ser B 274:175–182

    Article  Google Scholar 

  • Stapley J (2003) Differential avoidance of snake odours by a lizard: evidence for prioritized avoidance based on risk. Ethology 109:785–796

    Article  Google Scholar 

  • Sullivan TP, Nordstrom LO, Sullivan DS (1985) Use of predator odors as repellents to reduce feeding damage by herbivores. II. Black-tailed deer (Odocoileus hemionus columbianus). J Chem Ecol 11:921–935

    Article  CAS  PubMed  Google Scholar 

  • Swihart RK, Pignatello JJ, Mattina MJI (1991) Aversive responses of white-tailed deer, Odocoileus virginianus, to predator urines. J Chem Ecol 17:767–777

    Article  CAS  PubMed  Google Scholar 

  • Vilhunen S, Hirvonen H (2003) Innate antipredator responses of Arctic charr (Salvelinus alpinus) depend on predator species and their diet. Behav Ecol Sociobiol 55:1–10

    Article  Google Scholar 

  • Webb JK, Du Guo W, Pike DA, Shine R (2009) Chemical cues from both dangerous and non-dangerous snakes elicit antipredator behaviours from a nocturnal lizard. Anim Behav 77:1471–1478

    Article  Google Scholar 

  • Zager P, Beecham J (2006) The role of American black bears and brown bears as predators on ungulates in North America. Ursus 17:95–108

    Article  Google Scholar 

  • Zeileis A (2004) Econometric computing with HC and HAC covariance matrix estimators. J Stat Softw 11:1–17

    Google Scholar 

Download references

Acknowledgments

This work was partially funded by the CNRS and project 2010-BLAN-1718 of the Agence Nationale de la Recherche. We are indebted to members of the Laskeek Bay Society for their support, and to Barb Roswell and Jake and Erin Pattisson for support in the field. The latter, as well as M. Valeix, C. Chamaillé, S. Padié and L. Forbes, made the fieldwork smooth-running and fun. P. Banks and two anonymous reviewers made helpful suggestions which improved the manuscript.

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Correspondence to Simon Chamaillé-Jammes.

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Communicated by Peter Banks.

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Chamaillé-Jammes, S., Malcuit, H., Le Saout, S. et al. Innate threat-sensitive foraging: black-tailed deer remain more fearful of wolf than of the less dangerous black bear even after 100 years of wolf absence. Oecologia 174, 1151–1158 (2014). https://doi.org/10.1007/s00442-013-2843-0

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