Skip to main content

Advertisement

Log in

Dominant predator odour triggers caution and eavesdropping behaviour in a mammalian mesopredator

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Mesopredators need to satisfy their energetic requirements while avoiding potentially lethal encounters with apex predators. Predators release odours into the environment through natural processes, and many antipredator adaptations are induced by the detection of these scents. We tested whether a mesopredator adjusted its behaviour when it encountered dominant predator odour in an outdoor arena. Eighteen wild-captured stoats (Mustela erminea) were exposed to the body odour of three predators: two previously encountered sympatric apex predators [cat (Felis catus) and ferret (Mustela furo)] and a novel apex predator (African wild dog (Lycaon pictus)). Foraging areas were created that varied in perceived risk, based on the presence or absence of predator odour. Detection of kairomones (chemical cues from predators) triggered cautious inspection and altered the mesopredator’s foraging activity. However, in contrast to our predictions, dominant predator odour was an attractant rather than a deterrent; food was consumed earlier in foraging areas with apex predator odour than in unscented controls. Sympatric predator odour elicited the most pronounced behavioural changes, with stoats cautiously approaching, but readily investigating, the odour source. Ferret odour stimulated the most marked changes. Mesopredators may benefit from exploitative eavesdropping as detection of predator odour primes antipredator behaviours, avoids the energetic cost of unnecessary flight and may also help a mesopredator to locate resources. This experiment highlights the role of odour in the assessment of risk and its capacity to alter foraging behaviour by a subordinate member of a predator guild.

Significance statement

A predator encounters a myriad of scents when foraging, which can then be used to make inferences about its environment. In an outdoor arena, we tested behavioural responses of stoats to the odour of three dominant predators. Upon detecting the scent of a co-evolved predator (cat or ferret), stoats increased their cautious behaviour, but contrary to our initial prediction, they were attracted to the odour; food was consumed earlier in foraging areas with co-evolved predator odour than in unscented areas, or areas with the scent of a novel predator (African wild dog). Mesopredators ‘eavesdropped’ on the olfactory communication system of larger predators to reduce an encounter risk while obtaining food resources. Our results have practical applications for wildlife management and also increase our understanding of the role of scent communication in predator assemblages.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Albone ES, Shirley SG (1984) Mammalian semiochemistry: the investigation of chemical signals between mammals. John Wiley & Sons Ltd, Chichester

    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 

  • Bergstrom DM, Lucieer A, Kiefer K, Wasley J, Belbin L, Pedersen TK, Chown SL (2009) Indirect effects of invasive species removal devastate World Heritage Island. J Appl Ecol 46:73–81

    Article  Google Scholar 

  • Blanchard DC, Blanchard R, Rodgers R (1991) Risk assessment and animal models of anxiety. In: Olivier B, Mos J, Slangen J (eds) Animal models in psychopharmacology. Springer, New York, pp 117–134

    Chapter  Google Scholar 

  • Blanchard DC, Griebel G, Blanchard RJ (2003) Conditioning and residual emotionality effects of predator stimuli: some reflections on stress and emotion. Prog Neuro-Psychopharmacol 27:1177–1185

    Article  Google Scholar 

  • Blumstein DT, Mari M, Daniel JC, Ardron JG, Griffin AS, Evans CS (2002) Olfactory predator recognition: wallabies may have to learn to be wary. Anim Conserv 5:87–93

    Article  Google Scholar 

  • Brinck C, Erlinge S, Sandell M (1983) Anal sac secretion in mustelids: a comparison. J Chem Ecol 9:727–745

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Clapperton BK (1989) Scent-marking behaviour of the ferret, Mustela furo. Anim Behav 38:436–446

    Article  Google Scholar 

  • Clapperton BK, Phillipson SM, Woolhouse AD (1994) Field trials of slow-release synthetic lures for stoats (Mustela erminea) and ferrets (Mustela furo). New Zeal J Zool 21:279–284

    Article  Google Scholar 

  • Clout M, Karl B, Pierce R, Robertson H (1995) Breeding and survival of New Zealand pigeons Hemiphaga novaeseelandiae. Ibis 137:264–271

    Article  Google Scholar 

  • Crooks KR, Soulé ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Dielenberg RA, McGregor IS (2001) Defensive behavior in rats towards predatory odors: a review. Neurosci Biobehav Rev 25:597–609

    Article  CAS  PubMed  Google Scholar 

  • Dowding J, Elliott M (2003) Ecology of stoats in a South island braided river valley. New Zealand Department of Conservation, Wellington

    Google Scholar 

  • Erlinge S, Sandell M (1988) Coexistence of stoat, Mustela erminea, and weasel, M. nivalis: social dominance, scent communication, and reciprocal distribution. Oikos 53:242–246

    Article  Google Scholar 

  • Ferrari MC, Trowell JJ, Brown GE, Chivers DP (2005) The role of learning in the development of threat-sensitive predator avoidance by fathead minnows. Anim Behav 70:777–784

    Article  Google Scholar 

  • Ferrero DM, Lemon JK, Fluegge D et al (2011) Detection and avoidance of a carnivore odor by prey. Proc Natl Acad Sci U S A 108:11235–11240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garvey PM, Glen AS, Pech RP (2015) Foraging ermine avoid risk: behavioural responses of a mesopredator to its interspecific competitors in a mammalian guild. Biol Invasions 17:1771–1783

    Article  Google Scholar 

  • Gorman ML, Trowbridge BJ (1989) The role of odor in the social lives of carnivores. In: Gittleman JL (ed) Carnivore behavior, ecology, and evolution. Cornell University Press, Ithaca, pp 57–88

    Chapter  Google Scholar 

  • Griffin AS, Evans CS, Blumstein DT (2001) Learning specificity in acquired predator recognition. Anim Behav 62:577–589

    Article  Google Scholar 

  • Harrington LA, Harrington AL, Macdonald DW (2009) The smell of new competitors: the response of American mink, Mustela vison, to the odours of otter, Lutra lutra and polecat. M Putorius Ethol 115:421–428

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Higginson AD, McNamara JM, Houston AI (2012) The starvation-predation trade-off predicts trends in body size, muscularity, and adiposity between and within taxa. Am Nat 179:338–350

    Article  PubMed  Google Scholar 

  • Hughes NK, Korpimäki E, Banks PB (2010) The predation risks of interspecific eavesdropping: weasel-vole interactions. Oikos 119:1210–1216

    Article  Google Scholar 

  • Hurst JL (2005) Scent marking and social communication. In: McGregor PK (ed) Animal communication networks. Cambridge University Press, Cambridge, pp 219–243

    Chapter  Google Scholar 

  • Hurst JL, Gray SJ, Davey P, Young D, Corbishley J, Dawson C (1997) Social interaction alters attraction to competitor’s odour in the mouse Mus spretus Lataste. Anim Behav 54:941–953

    Article  PubMed  Google Scholar 

  • Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394

    Google Scholar 

  • King CM, Powell RA (2007) The natural history of weasels and stoats: ecology, behaviour and management, 2nd edn. Oxford University Press, New York

    Book  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 

  • Lledo P-M, Gheusi G, Vincent J-D (2005) Information processing in the mammalian olfactory system. Physiol Rev 85:281–317

    Article  PubMed  Google Scholar 

  • Masini C, Sauer S, Campeau S (2005) Ferret odor as a processive stress model in rats: neurochemical, behavioral, and endocrine evidence. Behav Neurosci 119:280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Donnell CFJ (1996) Predators and the decline of New Zealand forest birds: an introduction to the hole‐nesting bird and predator programme. New Zeal J Zool 23:213–219

    Article  Google Scholar 

  • Palomares F, Caro TM (1999) Interspecific killing among mammalian carnivores. Am Nat 153:492–508

    Article  Google Scholar 

  • Parsons MH, Blumstein DT (2010) Familiarity breeds contempt: kangaroos persistently avoid areas with experimentally deployed dingo scents. PLoS ONE 5:e10403

    Article  PubMed  PubMed Central  Google Scholar 

  • Peake TM (2005) Eavesdropping in communication networks. In: McGregor PK (ed) Animal communication networks. Cambridge University Press, Cambridge, pp 13–37

    Chapter  Google Scholar 

  • Preisser EL, Bolnick DI, Bernard 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 (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org/

    Google Scholar 

  • Ratz H (2000) Movements by stoats (Mustela erminea) and ferrets (M. furo) through rank grass of yellow‐eyed penguin (Megadyptes antipodes) breeding areas. New Zeal J Zool 27:57–69

    Article  Google Scholar 

  • Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998

    Article  PubMed  Google Scholar 

  • Schemnitz SD (2005) Capturing and handling wild animals. In: Bookhout TA (ed) Research and management techniques for wildlife and habitats. The Wildlife Society, Bethesda, pp 106–124

    Google Scholar 

  • Schoeppner NM, Relyea RA (2009) Interpreting the smells of predation: how alarm cues and kairomones induce different prey defences. Funct Ecol 23:1114–1121

    Article  Google Scholar 

  • Sih A (1980) Optimal behavior: can foragers balance two conflicting demands? Science 210:1041–1043

    Article  CAS  PubMed  Google Scholar 

  • Sih A, Bolnick DI, Luttbeg B et al (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621

    Article  Google Scholar 

  • Staples LG (2010) Predator odor avoidance as a rodent model of anxiety: learning-mediated consequences beyond the initial exposure. Neurobiol Learn Mem 94:435–445

    Article  PubMed  Google Scholar 

  • Takahashi LK, Nakashima BR, Hong H, 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 

  • Ward AJ, Mehner T (2010) Multimodal mixed messages: the use of multiple cues allows greater accuracy in social recognition and predator detection decisions in the mosquitofish, Gambusia holbrooki. Behav Ecol: 1315–1320

  • Ward J, Macdonald D, Doncaster C (1997) Responses of foraging hedgehogs to badger odour. Anim Behav 53:709–720

    Article  Google Scholar 

  • Wyatt TD (2010) Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J Comp Physiol 196:685–700

    Article  CAS  Google Scholar 

  • Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

We wish to thank Kay Clapperton, Anne Gaskett, Elaine Murphy, Catherine Price and Grant Morriss for their advice at the outset of the experiment. Thanks to Mick Clout, Manpreet Dhami, Grant Norbury, Phil Cowan and the two anonymous reviewers for their helpful comments on the manuscript. Thanks to Guy Forrester for his statistical advice. We would also like to thank Mike Wehner, Samantha Brown and Jane Arrow for their expert husbandry at the animal facility at Landcare Research. This work was supported by Core funding to Landcare Research from the Ministry of Business, Innovation and Employment’s Science and Innovation Group (contract CO9X09009), with additional support through the University of Auckland Doctoral Scholarship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patrick M. Garvey.

Ethics declarations

Pen trials were carried out within all the necessary guidelines and were in accordance with the relevant animal welfare regulations. We received ethical clearance from the Landcare Research Animal Ethics Committee (AEC approval number 12/06/01)

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Communicated by E. Korpimäki

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM. 1

(DOCX 17 kb)

ESM. 2

(DOCX 17 kb)

ESM. 3

(DOCX 17 kb)

ESM. 4

(DOCX 19 kb)

Video 1

(WMV 34294 kb)

Video 2

(WMV 9169 kb)

Video 3

(WMV 170326 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garvey, P.M., Glen, A.S. & Pech, R.P. Dominant predator odour triggers caution and eavesdropping behaviour in a mammalian mesopredator. Behav Ecol Sociobiol 70, 481–492 (2016). https://doi.org/10.1007/s00265-016-2063-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-016-2063-9

Keywords

Navigation