Skip to main content
SpringerLink
Log in

The role of learning in the acquisition of threat-sensitive responses to predator odours

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

Abstract

The supposition that prey animals respond to a predator with an intensity that matches the risk posed by the predator is known as the threat-sensitive predator avoidance hypothesis. Many studies have provided support for this hypothesis; yet, few studies have attempted to determine how such abilities are acquired by prey species. In this study, we investigated whether fathead minnows (Pimephales promelas) could learn to recognize an unknown predator (northern pike, Esox lucius) in such a way that they could match the intensity of their antipredator response with the threat posed by the predator. We exposed pike-naïve minnows to conspecific alarm cues paired with either a high or low concentration of pike odor. The following day, both groups were tested for a response to either high or low concentration of pike odor alone. We found that minnows conditioned with alarm cues paired with a given concentration of pike odor subsequently responded with a higher intensity to higher concentrations of pike odor, and with a lower intensity to lower concentrations of pike odor. These results demonstrate that during a single conditioning trial, minnows learn the identity of the predator in a threat-sensitive manner. Minnows use predator odor concentrations that they experience in subsequent interactions to adjust the intensity of their antipredator behavior.

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

Similar content being viewed by others

References

  • Amo L, Lopez P, Martin J (2004) Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges. Anim Behav 67:647–653

    Article  Google Scholar 

  • Anholt BR, Skelly DK, Werner EE (1996) Factors modifying antipredator behavior in larval toads. Herpetologica 52:301–313

    Google Scholar 

  • Berejikian BA, Tezaka EP, LaRaeb AL (2003) Innate and enhanced predator recognition in hatchery-reared chinook salmon. Environ Biol Fishes 67:241–251

    Article  Google Scholar 

  • Brown GE, Smith RJF (1996) Foraging trade-offs in fathead minnows (Pimephales promelas, Osteichthyes, Cyprinidae): acquired predator recognition in the absence of an alarm response. Ethology 102:776–785

    Google Scholar 

  • Brown GE, Chivers DP, Smith RJF (1997) Differential learning rates of chemical versus visual cues from a northern pike by fathead minnows in a natural habitat. Environ Biol Fishes 49:89–96

    Article  Google Scholar 

  • Chivers DP, Mirza RS (2001) Predator diet cues and the assessment of predation risk by aquatic vertebrates: a review and prospectus. In: Marchlewska-Koj DA, Lepri JJ, Müller-Schwarze D (eds) Chemical signals in vertebrates, vol. 9. Plenum, New York, pp 277–284

    Google Scholar 

  • Chivers DP, Smith RJF (1994a) The role of experience and chemical alarm signalling in predator recognition by fathead minnows, Pimephales promelas. J Fish Biol 44:273–285

    Article  Google Scholar 

  • Chivers DP, Smith RJF (1994b) Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish. Anim Behav 48:597–605

    Article  Google Scholar 

  • Chivers DP, Smith RJF (1995) Free-living fathead minnows rapidly learn to recognize pike as predators. J Fish Biol 46:949–954

    Article  Google Scholar 

  • Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator–prey systems: a review and prospectus. Ecoscience 5:338–352

    Google Scholar 

  • Chivers DP, Mirza RS, Bryer PJ, Kiesecker JM (2001) Threat-sensitive predator avoidance by slimy sculpins: understanding the importance of visual versus chemical information. Can J Zool 79:867–873

    Article  Google Scholar 

  • Dahl J, Nilsson PA, Petterson LB (1998) Against the flow: chemical detection of downstream predators in running waters. Proc R Soc Lond B Biol Sci 265:1339–1344

    Article  Google Scholar 

  • Dupuch A, Magnan P, Dill LM (2004) Sensitivity of northern redbelly dace, Phoxinus eos, to chemical alarm cues. Can J Zool 82:407–415

    Article  Google Scholar 

  • Ferrari MCO, Chivers DP (2006) The role of learning in the development of threat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information? Anim Behav 71:19–26

    Article  Google Scholar 

  • Ferrari MCO, Messier F, Chivers DP (in press) The nose knows: minnows determine predator proximity and density through detection of predator odours. Anim Behav

  • Ferrari MCO, 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 

  • Golub JL, Brown GE (2003) Are all signals the same? Ontogenetic change in the response to conspecific and heterospecific chemical alarm signals by juvenile green sunfish (Lepomis cyanellus). Behav Ecol Sociobiol 54:113–118

    Google Scholar 

  • Hartman EJ, Abrahams MV (2000) Sensory compensation and the detection of predators: the interaction between chemical and visual information. Proc R Soc Lond B Biol Sci 267:571–575

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Holomuzki JR, Short TM (1990) Ontogenetic shifts in habitat use and activity in a stream-dwelling isopod. Holarct Ecol 13:300–307

    Google Scholar 

  • Kats LB, Breeding JA, Hanson KM, Smith P (1994) Ontogenetic change in California newts (Taricha torosa) in response to chemical cues from conspecific predators. J North Am Benthol Soc 13:321–325

    Article  Google Scholar 

  • Kelley JL, Magurran AE (2003) Learned predator recognition and antipredator responses in fishes. Fish Fish 4:216–226

    Google Scholar 

  • Kusch RC, Mirza RS, Chivers DP (2004) Making sense of the predator scents: investigating the sophistication of predator assessment abilities of fathead minnows. Behav Ecol Sociobiol 55:551–555

    Article  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 

  • Magurran AE (1989) Acquired recognition of predator odour in the European minnows (Phoxinus phoxinus). Ethology 82:216–233

    Google Scholar 

  • Marcus J, Brown GE (2003) Response of pumpkinseed sunfish to conspecific chemical alarm cues: an interaction between ontogeny and stimulus concentration. Can J Zool 81:1671–1677

    Article  Google Scholar 

  • Mathis A, Smith RJF (1993) Chemical alarm signals increase the survival time in fathead minnows (Pimephales promelas) during encounters with northern pike (Esox lucius). Behav Ecol 4:260–265

    Article  Google Scholar 

  • Mathis A, Vincent F (2000) Differential use of visual and chemical cues in predator recognition and threat-sensitive predator-avoidance responses by larval newts (Notophthalmus viridescens). Can J Zool 78:1646–1652

    Article  CAS  Google Scholar 

  • Mathis A, Chivers DP, Smith RJF (1993) Population differences in responses of fathead minnows (Pimephales promelas) to visual and chemical stimuli from predators. Ethology 93:31–40

    Article  Google Scholar 

  • McIntosh AR, Peckarsky BL, Taylor BW (1999) Rapid size-specific changes in the drift of Baetis bicaudatus (Ephemeroptera) caused by alteration in fish odour concentration. Oecologia 118:256–264

    Article  Google Scholar 

  • Puttlitz MH, Chivers DP, Kiesecker JM, Blaustein AR (1999) Threat-sensitive predator avoidance by larval Pacific treefrogs (Amphibia, Hylidae). Ethology 105:449–456

    Article  Google Scholar 

  • Smith RJF (1999) What good is smelly stuff in the skin? Cross function and cross taxa effects in fish ‘alarm substances’. In: Johnston RE, Müller-Schwarze D, Sorensen PW (eds) Advances in chemical signals in vertebrates. Kluwer, New York, pp 475–488

    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 

  • Wahle RA (1992) Body-size dependent anti-predator mechanisms of the American lobster. Oikos 65:52–60

    Article  Google Scholar 

  • Williams PJ, Brown JA (1991) Developmental changes in foraging—predator avoidance trade-offs in larval lumpfish, Cyclopterus lumpus. Mar Ecol Prog Ser 76:53–60

    Article  Google Scholar 

  • Wisenden BD (2003) Chemically-mediated strategies to counter predation. In: Collin SP, Marshall NJ (eds) Sensory processing in the aquatic environment. Springer, Berlin Heidelberg New York, pp 236–251

    Chapter  Google Scholar 

  • Zhao X, Chivers DP (2005) Response of juvenile goldfish (Carassius auratus) to chemical cues: relationship between response intensity, response duration and the level of predation risk. In: Mason RT, LeMaster M, Müller-Scharze D (eds) Chemical signals in vertebrates, vol 10. Plenum, New York, pp 334–341

    Chapter  Google Scholar 

Download references

Acknowledgements

This work is dedicated to the memory of Dr. Joseph A. Brown who passed away unexpectedly on September 4, 2005. Dr. Brown was a pioneer in fish behavioral ecology. His contribution to science will be sorely missed.

The Natural Sciences and Engineering Research Council of Canada and the University of Saskatchewan provided financial support to D. P. Chivers. All work reported herein was in accordance with the University of Saskatchewan Committee of Animal Care and Supply protocol #19920077.

Author information

Authors and Affiliations

  1. Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK S7N 5E2, Canada

    Maud C. O. Ferrari, Terence Capitania-Kwok & Douglas P. Chivers

Authors
  1. Maud C. O. Ferrari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Terence Capitania-Kwok
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Douglas P. Chivers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maud C. O. Ferrari.

Additional information

Communicated by K. Lindström

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ferrari, M.C.O., Capitania-Kwok, T. & Chivers, D.P. The role of learning in the acquisition of threat-sensitive responses to predator odours. Behav Ecol Sociobiol 60, 522–527 (2006). https://doi.org/10.1007/s00265-006-0195-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0195-z

Keywords

Search

Navigation