Skip to main content
Log in

Threat-sensitive generalization of predator recognition by larval amphibians

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

Abstract

Despite the importance of acquired predator recognition in mediating predator–prey interactions, we know little about the specific characteristics that prey use to distinguish predators from non-predators. Recent experiments with mammals and fish indicate that some prey lacking innate predator recognition have the ability to display anti-predator responses upon their first encounter with those predators if they are similar to predators that the prey has recently learned to recognize. This phenomenon is referred to as generalization of predator recognition. In this experiment, we documented for the first time that larval amphibians (woodfrog, Rana sylvatica) have the ability to generalize the recognition of known predators to closely related novel predators. Moreover, we demonstrated that this ability is dependent on the level of risk associated with the known predator. When red-bellied newt, Cynops pyrrhogaster (known predator), was paired with simulated low risk, tadpoles displayed fright responses to newts and novel tiger salamanders, Ambystoma tigrinum, but not to novel African clawed frogs, Xenopus laevis. However, when the newt was paired with simulated high risk, tadpoles generalized their responses to both tiger salamanders and African clawed frogs. Larval anurans seem to have a wider generalization frame than other animals.

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

Similar content being viewed by others

References

  • 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 

  • Chivers DP, Mirza RS (2001) The importance of predator-diet cues in the responses of larval woodfrogs to fish and invertebrate predators. J Chem Ecol 27:45–51

    Article  PubMed  CAS  Google Scholar 

  • Chivers DP, Smith RJF (1994a) 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 (1994b) 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, 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 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

  • Ferrari MCO, Chivers DP (2008) Cultural learning of predators in mixed species assemblages: the effects of tutor-to-observer ratio. Anim Behav 75:1921–1925

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ferrari MCO, Kapitania-Kwok T, Chivers DP (2006) The role of learning in the development of threat-sensitive predator avoidance: the use of predator cue concentration by fathead minnows. Behav Ecol Sociobiol 60:522–527

    Article  Google Scholar 

  • Ferrari MCO, Gonzalo A, Messier F, Chivers DP (2007a) Generalization of learned predator recognition: an experimental test and framework for future studies. Proc R Soc B 274:1853–1859

    Article  PubMed  Google Scholar 

  • Ferrari MCO, Messier F, Chivers DP (2007b) First documentation of cultural transmission of predator recognition by larval amphibians. Ethology 113:621–627

    Article  Google Scholar 

  • Ferrari MCO, Messier F, Chivers DP (2007c) Degradation of alarm cues under natural conditions: risk assessment by larval amphibians. Chemoecology 17:263–266

    Article  Google Scholar 

  • Ferrari MCO, Messier F, Chivers DP (2008a) Can prey exhibit threat-sensitive generalization of predator recognition? Extending the Predator Recognition Continuum Hypothesis. Proc R Soc B 275:1811–1816

    Article  PubMed  Google Scholar 

  • Ferrari MCO, Messier F, Chivers DP (2008b) Threat-sensitive learning by the larval mosquito Culex restuans. Behav Ecol Sociobiol 62:1079–1083

    Article  Google Scholar 

  • Griffin AS, Evans CS (2003) Social learning of antipredator behaviour in a marsupial. Anim Behav 66:485–492

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Guirlanda S, Enquist M (2003) A century of generalization. Anim Behav 66:15–36

    Article  Google Scholar 

  • Hazlett BA (2003) Predator recognition and learned irrelevance in the crayfish Orconectes virilis. Ethology 109:765–780

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Herzog M, Hopf S (1984) Behavioural responses to species-specific warning calls in infant squirrel monkeys reared in social isolation. Am J Primatol 7:99–106

    Article  Google Scholar 

  • Kesavaraju B, Damal K, Juliano SA (2007) Threat-sensitive behavioral responses to concentrations of water-borne cues from predation. Ethology 113:199–206

    Article  PubMed  Google Scholar 

  • Kiesecker JM, Blaustein AR (1997) Population differences in responses of red-legged frogs (Rana aurora) to introduced bullfrogs (Rana catesbeiana). Ecology 78:1753–1760

    Google Scholar 

  • Mathis A, Smith RJF (1993) Fathead minnows, Pimephales promelas, learn to recognize northern pike, Esox lucius, as predators on the basis of chemical stimuli from minnows in the pike's diet. Anim Behav 46:645–656

    Article  Google Scholar 

  • Mathis A, Chivers DP, Smith RJF (1996) Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning. Anim Behav 51:185–201

    Article  Google Scholar 

  • Mineka S, Cook M (1988) Social learning and the acquisition of snake fear in monkeys. In: Zentall TR, BGJr G (eds) Social learning: psychological and biological perspectives. Erlbaum, Hillsdale, pp 51–73

    Google Scholar 

  • Mirza RS, Ferrari MCO, Kiesecker JM, Chivers DP (2006) Responses of American toad tadpoles to predation cues: behavioural response thresholds, threat-sensitivity and acquired predation recognition. Behaviour 143:887–889

    Article  Google Scholar 

  • Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In Black AH, Prokasy WF (eds), Classical Conditioning II. Appleton-Century-Crofts, pp. 64–99

  • 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 B 274:175–182

    Article  PubMed  Google Scholar 

  • Stephens DW (1991) Change, regularity and value in the evolution of animal learning. Behav Ecol 2:77–89

    Article  Google Scholar 

  • Vieth W, Curio E, Ernst U (1980) The adaptive significance of avian mobbing. III. Cultural transmission of enemy recognition in blackbirds: cross-species tutoring and properties of learning. Anim Behav 28:1217–1229

    Article  Google Scholar 

  • Wisenden BD, Millard MC (2001) Aquatic flatworms use chemical cues from injured conspecifics to assess predation risk and to associate risk with novel cues. Anim Behav 62:761–766

    Article  Google Scholar 

  • Woody DR, Mathis A (1998) Acquired recognition of chemical stimuli from an unfamiliar predator: associative learning by adult newts, Notophthalmus viridescens. Copeia 1998:1027–1031

    Article  Google Scholar 

Download references

Acknowledgements

We thank Peter Bednekoff and the anonymous reviewers for their constructive comments on our manuscript. We thank Jean and Glen Chivers for their help and support and for letting us invade their home and wetlands for the duration of our field season. We thank the Biology Department of the U of S for providing the predators. Research funding was provided to F. Messier and D. Chivers through the Natural Sciences and Engineering Research Council of Canada. All work reported was in accordance with the Animal Care Committee Protocol # 20060014 from University of Saskatchewan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maud C. O. Ferrari.

Additional information

Communicated by P. Bednekoff

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ferrari, M.C.O., Brown, G.E., Messier, F. et al. Threat-sensitive generalization of predator recognition by larval amphibians. Behav Ecol Sociobiol 63, 1369–1375 (2009). https://doi.org/10.1007/s00265-009-0779-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-009-0779-5

Keywords

Navigation