Skip to main content
SpringerLink
Log in

Exposure to Urine of Canids and Felids, but not of Herbivores, Induces Defensive Behavior in Laboratory Rats

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Predator odors induce defensive behavior in many prey species. For various reasons, studies carried out up to now have been unable to establish whether predator odor recognition is innate or not. Mostly, only particular odors or wild-living (i.e., experienced) test animals have been used in these studies, restricting the conclusiveness of the observations. In the present study, the behavioral effects of exposure to different predator odors on predator odor-naive laboratory male rats were compared with the effects of different nonpredator odors and of a no-odor control stimulus. Results show that exposure to urine of canids and felids, but not of herbivores or conspecifics, induce defensive behaviors. Taken together, the study provides support for the hypothesis that there is an innate recognition of predator odors in laboratory rats.

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

Similar content being viewed by others

References

  • Amo, L., López, P. and Martín, J. 2004. Trade-offs in the choice of refuges by common wall lizards: Do thermal costs affect preferences for predator-free refuges? Can. J. Zool. 82:897–901.

    Article  Google Scholar 

  • Apfelbach, R., Blanchard, C. D., Blanchard, R. J., Hayes, R. A. and Mcgregor, I. S. 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 

  • Berton, F., Vogel, E. and Belzung, C. 1998. Modulation of mice anxiety in response to cat odor as a consequence of predators diet. Physiol. Behav. 65:247–254.

    Article  PubMed  CAS  Google Scholar 

  • Blanchard, R. J. and Blanchard, D. C. 1971. Defensive reactions in the albino rat. Learn. Motiv. 2:351–362.

    Article  Google Scholar 

  • Blanchard, R. J. and Blanchard, D. C. 1990. Anti-predator defense as models of animal fear and anxiety, pp. 89–108, in P. F. Brain, S. Parmigiani, and R. J. Blanchard (eds.). Fear and Defence. Church and Harwood Academic, New York.

    Google Scholar 

  • Blanchard, R. J., Blanchard, D. C., Rodgers, J., and Weiss, S. M. 1990a. The characterization and modeling of antipredator defensive behavior. Neurosci. Biobehav. Rev. 14:463–472.

    Article  PubMed  CAS  Google Scholar 

  • Blanchard, R. J., Blanchard, D. C., Weiss, S. M., and Meyer, S. 1990b. The effects of ethanol and diazepam on reactions to predatory odors. Pharmacol. Biochem. Behav. 35:775–780.

    Article  PubMed  CAS  Google Scholar 

  • Blanchard, D. C., Griebel, G., and Blanchard, R. J. 2003a. The Mouse Defense Test Battery: Pharmacological and behavioral assays for anxiety and panic. Eur. J. Pharmacol. 463:97–116.

    Article  PubMed  CAS  Google Scholar 

  • Blanchard, D. C., Markham, C., Yang, M., Hubbard, D., Madarang, E., and Blanchard, R. J. 2003b. Failure to produce conditioning with low-dose trimethylthiazoline or cat feces as unconditioned stimuli. Behav. Neurosci. 117:360–368.

    Article  PubMed  CAS  Google Scholar 

  • Burwash, M. D., Tobin, M. E., Woolhouse, A. D., and Sullivan, T. P. 1998. Laboratory evaluation of predator odors for eliciting an avoidance response in roof rats (Rattus rattus). J. Chem. Ecol. 24:49–65.

    Article  CAS  Google Scholar 

  • Campbell, T., Lin, S., Devries, C., and Lambert, K. 2003. Coping strategies in male and female rats exposed to multiple stressors. Physiol. Behav. 78:495–504.

    Article  PubMed  CAS  Google Scholar 

  • Carobrez, A. P., Teixeira, K. V., and Graeff, F. G. 2001. Modulation of defensive behavior by periaqueductal gray NMDA/glycine-B receptor. Neurosci. Biobehav. Rev. 25:697–709.

    Article  PubMed  CAS  Google Scholar 

  • Dickman, C. R. 1992. Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73:313–322.

    Article  Google Scholar 

  • Dickman, C. R. and Doncaster, C. P. 1984. Responses of small mammals to red fox (Vulpes vulpes) odour. J. Zool. 204:521–531.

    Article  Google Scholar 

  • Dielenberg, R. A. and McGregor, I. S. 2001. Defensive behavior in rats towards predatory odors: A review. Neurosci. Biobehav. Rev. 25:597–609.

    Article  PubMed  CAS  Google Scholar 

  • Edut, S. and Eilam, D. 2003. Rodents in open space adjust their behavioral response to the different risk levels during barn-owl attack. BMC Ecol. 3:10–22.

    Article  PubMed  Google Scholar 

  • Eilam, D., Dayan, T., Ben-Eliyahu, S., Schulman, I. I., Shefer, G., and Hendrie, C. A. 1999. Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Anim. Behav. 58:1085–1093.

    Article  PubMed  Google Scholar 

  • Epple, G., Mason, J. R., Nolte, D. L., and Campbell, D. L. 1993. Effects of predator odors on feeding in the mountain beaver (Aplodontia rufa). J. Mammol. 74:715–722.

    Article  Google Scholar 

  • Farmer-Dougan, V., Chandrashekar, S., Stutzman, D., Bradham, K., and Dougan, J. D. 2005. Fox urine as an aversive stimulus: Modification of a passive avoidance task. J. Gen. Psychol. 132:313–320.

    Google Scholar 

  • Fendt, M. and Fanselow, M. S. 1999. The neuroanatomical and neurochemical basis of conditioned fear. Neurosci. Biobehav. Rev. 23:743–760.

    Article  PubMed  CAS  Google Scholar 

  • Fendt, M., Endres, T., Lowry, C. A., Apfelbach, R., and McGregor, I. S. 2005. TMT-induced autonomic and behavioral changes and the neural basis of its processing. Neurosci. Biobehav. Rev. 29:1145–1156.

  • Gese, E. M. and Ruff, R. L. 1997. Scent-marking by coyotes, Canis latrans: The influence of social and ecological factors. Anim Behav. 54:1155–1166.

    Article  PubMed  Google Scholar 

  • Glowacinski, Z. and Profus, P. 1997. Potential impact of wolves Canis lupus on prey populations in eastern Poland. Biol. Cons. 80:99–106.

    Article  Google Scholar 

  • Goldyn, B., Hromada, M., Surmacki, A., and Tryjanowski, P. 2003. Habitat use and diet of the red fox Vulpes vulpes in an agricultural landscape in Poland. Z. Jagdwiss. 49:191–200.

    Article  Google Scholar 

  • Hendrie, C. A. 1991. The calls of murine predators activate endogenous analgesia mechanisms in laboratory mice. Physiol. Behav. 49:569–573.

    Article  PubMed  CAS  Google Scholar 

  • Hendrie, C. A., Weiss, C., and Eilam, D. 1996. Exploration and predation models of anxiety: Evidence from laboratory and wild species. Pharmacol. Biochem. Behav. 54:13–20.

    Article  PubMed  CAS  Google Scholar 

  • Hirsch, S. M. and Bolles, R. C. 1980. On the ability of prey to recognize predators. Z. Tierpsychol. 54:71–84.

    Google Scholar 

  • Kats, L. B. and Dill, L. M. 1998. The scent of death: Chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394.

    Google Scholar 

  • Labra, A. and Niemeyer, H. M. 2004. Variability in the assessment of snake predation risk by Liolaemus lizards. Ethology 110:649–662.

    Article  Google Scholar 

  • Markham, C. M., Blanchard, D. C., Canteras, N. S., Cuyno, C. D., and Blanchard, R. J. 2004. Modulation of predatory odor processing following lesions to the dorsal premammillary nucleus. Neurosci. Lett. 372:22–26.

    Article  PubMed  CAS  Google Scholar 

  • McGregor, I. S., Schrama, L., Ambernoon, P., and Dielenberg, R. A. 2002. Not all ‘predator odours’ are equal: Cat odour but not 2,4,5 trimethylthiazoline (TMT; fox odour) elicits specific defensive behaviours in rats. Behav. Brain Res. 129:1–16.

    Article  PubMed  CAS  Google Scholar 

  • McNaughton, N. and Corr, P. J. 2004. A two-dimensional neuropsychology of defense: Fear/anxiety and defensive distance. Neurosci. Biobehav. Rev. 28:285–305.

    Article  PubMed  Google Scholar 

  • Misslin, R. 2003. The defense system of fear: Behavior and neurocircuitry. Neurophysiol. Clin. 33:55–66.

    Article  PubMed  Google Scholar 

  • Nolte, D. L., Mason, J. R., Epple, G., Aronov, E., and Campbell, D. L. 1994. Why are predator urines aversive to prey? J. Chem. Ecol. 20:1505–1516.

    Article  CAS  Google Scholar 

  • Rosell, F. 2001. Effectiveness of predator odors as grey squirrel repellents. Can. J. Zool. 79:1719–1723.

    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, T. P., Nordstrom, L., and Sullivan, D. S. 1985a. Use of predator odors as repellents to reduce feeding damage by herbivores. I. Showshoe hares (Lepus americanus). J. Chem. Ecol. 11:903–911.

    Article  Google Scholar 

  • Sullivan, T. P., Nordstrom, L., and Sullivan, D. S. 1985b. 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  Google Scholar 

  • Sullivan, T. P., Crump, D., and Sullivan, D. S. 1988. Use of predator odors as repellents to reduce feeding damage by herbivores. III. Montane and meadow voles (Microtus montanus and Microtus pennsylvannicus). J. Chem. Ecol. 14:363–378.

    Article  CAS  Google Scholar 

  • Sullivan, G. M., Apergis, J., Bush, D. E., Johnson, L. R., Hou, M., and Ledoux, J. E. 2004. Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus. Neuroscience 128:7–14.

    Article  PubMed  CAS  Google Scholar 

  • Swihart, R. K., Pignatello, J. J., and Mattina, M. J. I. 1999. Adverse responses of white-tailed deer, Odocoileus virginianus, to predator urines. J. Chem. Ecol. 17:767–777.

    Article  Google Scholar 

  • Takahashi, L. K., Nakashima, B. R., Hong, H., and Watanabe, K. 2005. The smell of danger: A behavioral and neural analysis of predator odor-induced fear. Neurosci. Biobehav. Rev. 29:1157–1167.

    Article  PubMed  Google Scholar 

  • Wiltgen, B. J. and Fanselow, M. S. 2003. A model of hippocampal–cortical–amygdala interactions based on contextual fear conditioning, pp. 83–103, in K. J. Jeffries (ed.) The Neurobiology of Spatial Behavior. Oxford University Press, Oxford.

    Google Scholar 

  • Yamada, K. and Nabeshima, T. 1995. Stress-induced behavioral responses and multiple opioid systems in the brain. Behav. Brain Res. 67:133–145.

    Article  PubMed  CAS  Google Scholar 

  • Zar, J. H. 1999. Biostatistical Analysis. Prentice-Hall, Upper Saddle River, NJ.

    Google Scholar 

Download references

Acknowledgments

The author thanks Daniel Endler, Daniela Schmieder, and Verena Koller for assistance with these experiments, as well as Dr. Björn Siemers for comments on the manuscript.

Author information

Author notes

  1. Markus Fendt

    Present address: Novartis Institutes for Biomedical Research, Neuroscience Research, WSJ-386.3.44, Lichtstrasse 35, 4056, Basel, Switzerland

Authors and Affiliations

  1. Tierphysiologie, Zoologisches Institut, Fakultät für Biologie, Universität Tübingen, Auf der Morgenstelle 28, 72076, Tübingen, Germany

    Markus Fendt

Authors
  1. Markus Fendt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Markus Fendt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fendt, M. Exposure to Urine of Canids and Felids, but not of Herbivores, Induces Defensive Behavior in Laboratory Rats. J Chem Ecol 32, 2617–2627 (2006). https://doi.org/10.1007/s10886-006-9186-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-006-9186-9

Keywords

Search

Navigation