Advertisement

Learned Recognition by Zebrafish and Other Cyprinids

  • Brian D. Wisenden
Protocol
Part of the Neuromethods book series (NM, volume 52)

Abstract

Antipredator behavior is triggered by a combination of internal proximate mechanisms (anatomical receptors and the physiological processes that regulate their function) and external environmental cues that signal the context and timing of when behavior is likely to be effective. Responses to some external environmental triggers, such as the presence of conspecific chemical alarm cue, are governed strictly by genetic templates. Other external environmental triggers are learned through a special type of associative learning called releaser-induced recognition learning. Zebrafish are one of several model systems upon which this body of literature has been developed. Minnows (including zebrafish) associate danger with any novel stimulus (visual, chemical, or auditory) that is correlated with the presence of chemical alarm cue released from damaged epithelial tissue of conspecifics. Alarm cue is released only in the context of predation and serves as a reliable external environmental trigger for associating novel stimuli with predation risk. Minnows use learned recognition to learn about predator identity and about the chemical alarm cues of ecologically similar heterospecifics. Learning also occurs when alarm cues are released indirectly through the digestive tract of the predator. Behavioral and chemical responses to disturbance can also facilitate learned recognition. Learned recognition is an ideal system with which to study the molecular mechanisms that underlie the cognitive processes of learning and memory. Collectively, this suggests that zebrafish are a very promising model organism for future study.

Key words

Antipredator behavior predator response alarm cue environmental cues conditioned stimulus unconditioned stimulus releaser-induced recognition learning learned recognition associative learning memory 

References

  1. 1.
    Wisenden, B. D. & Stacey, N. E. (2005) Fish semiochemicals and the network concept. In McGregor, P. K. (Ed.) Animal Communication Networks. Cambridge, Cambridge University Press, pp. 540–567.CrossRefGoogle Scholar
  2. 2.
    Suboski, M. D. (1990) Releaser-induced recognition learning. Psychol Rev 97, 271–284.CrossRefGoogle Scholar
  3. 3.
    Suboski, M. D., Bain, S., Carty, A. E., McQuoid, L. M., Seelen, M. I. & Seifert, H. (1990) Alarm reaction in acquisition and social transmission of simulated-predator recognition by zebra danio fish (Brachydanio rerio). J Comp Psychol 104, 101–112.CrossRefGoogle Scholar
  4. 4.
    Göz, H. (1941) Über den Art-und Individualgeruch bei Fischen. Z Vergl Physiol 29, 1–45.CrossRefGoogle Scholar
  5. 5.
    von Frisch, K. (1938) Zur psychologie des Fische-Schwarmes. Naturwissenschaften 26, 601–606.CrossRefGoogle Scholar
  6. 6.
    Dill, L. M. (1974) The escape response of the zebra danio (Brachydanio rerio). I. The stimulus for escape. Anim Behav 22, 711–722.CrossRefGoogle Scholar
  7. 7.
    Gandolfi, G., Classon, L. J. & Rossi, A. C. (1968) The fright reaction of zebra fish. Atti Soc Ital Sci Nat 107, 74–88.Google Scholar
  8. 8.
    Pfeiffer, W. (1977) The distribution of fright reaction and alarm substance cells in fishes. Copeia 1977, 653–665.CrossRefGoogle Scholar
  9. 9.
    Waldman, B. (1982) Quantitative and developmental analysis of the alarm reaction in the zebra danio, Brachydanio rerio. Copeia 1982, 1–9.CrossRefGoogle Scholar
  10. 10.
    Magurran, A. E. (1989) Acquired recognition of predator odour in the European minnow (Phoxinus phoxinus). Ethology 82, 216–223.CrossRefGoogle Scholar
  11. 11.
    Hall, D. & Suboski, M. D. (1995) Visual and olfactory stimuli in learned release of alarm reactions by zebra danio fish (Brachydanio rerio). Neurobiol Learn Mem 63, 229–240.PubMedCrossRefGoogle Scholar
  12. 12.
    Korpi, N. L. & Wisenden, B. D. (2001) Learned recognition of novel predator odour by zebra danios, Danio rerio, following time-shifted presentation of alarm cue and predator odour. Environ Biol Fishes 61, 205–211.CrossRefGoogle Scholar
  13. 13.
    Chivers, D. P. & Smith, R. J. F. (1994a) Fathead minnows (Pimephales promelas) acquire recognition when alarm substance is associated with the sight of unfamiliar fish. Anim Behav 48, 597–605.CrossRefGoogle Scholar
  14. 14.
    Chivers, D. P. & Smith, R. J. F. (1994b) The role of experience and chemical alarm signaling in predator recognition by fathead minnows, Pimephales promelas Rafinesque. J Fish Biol 44, 273–285.CrossRefGoogle Scholar
  15. 15.
    Mathis, A. & Smith, R. J. F. (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.CrossRefGoogle Scholar
  16. 16.
    Wisenden, B. D., Pogatshnik, J., Gibson, D., Bonacci, L., Schumacher, A. & Willett, A. (2008) Sound the alarm: learned association of predation risk with novel auditory stimuli by fathead minnows (Pimephales promelas) and glowlight tetras (Hemigrammus erythrozonus) after single simultaneous pairings with conspecific chemical alarm cues. Environ Biol Fish 81, 141–147.CrossRefGoogle Scholar
  17. 17.
    Ferrari, M. C. O. & Chivers, D. P. (2006a) The role of learning in the acquisition of threat-sensitive responses to predator odors. Behav Ecol Sociobiol 60, 522–527.CrossRefGoogle Scholar
  18. 18.
    Brown, G. E., Chivers, D. P. & Smith, R. J. F. (1997) Differential learning rates of chemical versus visual cues of a northern pike by fathead minnows in a natural habitat. Environ Biol Fish 49, 89–96.CrossRefGoogle Scholar
  19. 19.
    Chivers, D. P. & Smith, R. J. F. (1995a) Free-living fathead minnows rapidly learn to recognize pike as predators. J Fish Biol 46, 949–954.CrossRefGoogle Scholar
  20. 20.
    Leduc, A. O. H. C., Roh, E., Breau, C. & Brown, G. E. (2007) Learned recognition of a novel odour by wild juvenile Atlantic salmon (Salmo salar) under fully natural conditions. Anim Behav 73, 471–477.CrossRefGoogle Scholar
  21. 21.
    Chivers, D. P. & Smith, R. J. F. (1995b) Fathead minnows (Pimephales promelas) learn to recognize chemical stimuli from high-risk habitats by the presence of alarm substance. Behav Ecol 6, 155–158.CrossRefGoogle Scholar
  22. 22.
    Ferrari, M. C. O. & Chivers, D. P. (2006b) The role of latent inhibition in acquired predator recognition in fathead minnows. Can J Zool 84, 505–509.CrossRefGoogle Scholar
  23. 23.
    Ferrari, M. C. O., Gonzalo, A., Messier, F. & Chivers, D. P. (2007) Generalization of learned predator recognition: an experimental test and framework for future studies. Proc R Soc Lond B 274, 1853–1859.CrossRefGoogle Scholar
  24. 24.
    Wisenden, B. D. & Harter, K. R. (2001) Motion, not shape, facilitates association of predation risk with novel objects by fathead minnows (Pimephales promelas). Ethology 107, 357–364.CrossRefGoogle Scholar
  25. 25.
    Chivers, D. P., Mirza, R. S. & Johnston, J. G. (2002) Learned recognition of heterospecific alarm cues enhances survival during encounters with predators. Behaviour 139, 929–938.CrossRefGoogle Scholar
  26. 26.
    Mirza, R. S. & Chivers, D. P. (2003) Fathead minnows learn to recognize heterospecific alarm cues they detect in the diet of a known predator. Behaviour 140, 1359–1369.CrossRefGoogle Scholar
  27. 27.
    Mirza, R. S. & Chivers, D. P. (2001) Learned recognition of heterospecific alarm signals: the importance of a mixed predator diet. Ethology 107, 1007–1018.CrossRefGoogle Scholar
  28. 28.
    Mathis, A., Chivers, D. P. & Smith, R. J. F. (1996) Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning. Anim Behav 51, 185–201.CrossRefGoogle Scholar
  29. 29.
    Wisenden, B. D., Chivers, D. P. & Smith, R. J. F. (1995) Early warning in the predation sequence: a disturbance pheromone in Iowa darters (Etheostoma exile). J Chem Ecol 21, 1469–1480.CrossRefGoogle Scholar
  30. 30.
    Hazlatt, B. A. (1990) Source and nature of disturbance-chemical system in crayfish. J Chem Ecol 16, 2263–2275.CrossRefGoogle Scholar
  31. 31.
    Kiesecker, J. M., Chivers, D. P., Marco, A., Quilchanos, C., Anderson, M. T. & Blaustein, A. R. (1999) Identification of a disturbance signal in larval red-legged frogs Rana aurora. Anim Behav 57, 1295–1300.PubMedCrossRefGoogle Scholar
  32. 32.
    Mirza, R. S. & Chivers, D. P. (2002) Behavioural responses to conspecific disturbance chemicals enhance survival of juvenile brook charr, Salvelinus fontinalis, during encounters with predators. Behaviour 139, 1099–1109.CrossRefGoogle Scholar
  33. 33.
    Wisenden, B. D., Binstock, C. L., Knoll, K. E. & Linke, A. D. (2010) Risk-sensitive information gathering by zebrafish following release of chemical alarm cues. Anim Behav 79, 1101–1107.CrossRefGoogle Scholar
  34. 34.
    Brown, G. E. & Godin, J.-G. J. (1999) Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish. Anim Behav 57, 475–481.PubMedCrossRefGoogle Scholar
  35. 35.
    Mathis, A., Ferrari, M. C. O., Windel, N., Messier, F. & Chivers, D. P. (2008) Learning by embryos and the ghost of predation future. Proc R Soc B 275, 2603–2607.PubMedCrossRefGoogle Scholar
  36. 36.
    Ferrari, M. C. O., Wisenden, B. D. & Chivers, D. P. (2010) Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88, 698–724.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Brian D. Wisenden
    • 1
  1. 1.Biosciences DepartmentMinnesota State University MoorheadMoorheadUSA

Personalised recommendations