In comparison with social learning about food, social learning about predators has received little attention. Yet such research is of potential interest to students of animal cognition and conservation biologists. I summarize evidence for social learning about predators by fish, birds, eutherian mammals, and marsupials. I consider the proposal that this phenomenon is a case of S-S classical conditioning and suggest that evolution may have modified some of the properties of learning to accommodate for the requirements of learning socially about danger. I discuss some between-species differences in the properties of socially acquired predator avoidance and suggest that learning may be faster and more robust in species in which alarm behavior reliably predicts high predatory threat. Finally, I highlight how studies of socially acquired predator avoidance can inform the design of prerelease antipredator training programs for endangered species.
Arcediano, F., &Miller, R. R. (2002). Some constraints for models of timing: A temporal coding hypothesis perspective.Learning & Motivation,33, 105–123.
Berejikian, B. A., Smith, R. J. F., Tezak, E. P., Schroder, S. L., &Knudsen, C. M. (1999). Chemical alarm signals and complex hatchery rearing habitats affect antipredator behavior and survival of chinook salmon (Oncorhynchus tshawytscha) juveniles.Canadian Journal of Fisheries & Aquatic Sciences,56, 830–838.
Berger, J., Swenson, J. E., &Persson, I.-L. (2001). Recolonizing carnivores and naive prey: Conservation lessons from Pleistocene extinctions.Science,291, 1036–1039.
Brown, C., &Laland, K. (2001). Social learning and life skills training for hatchery reared fish.Journal of Fish Biology,59, 471–493.
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.Environmental Biology of Fishes,49, 89–96.
Cheney, D. L., &Seyfarth, R. M. (1990).How monkeys see the world. Chicago: University of Chicago Press.
Chivers, D. P., Brown, G. E., &Smith, R. J. F. (1995). Acquired recognition of chemical stimuli from pike,Esox lucius, by brook sticklebacks,Culaea inconstans (Osteichthyes, Gasterosteidae).Ethology,99, 234–242.
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.
Chivers, D. P., &Smith, R. J. F. (1994a). Fathead minnows,Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish.Animal Behaviour,48, 597–605.
Chivers, D. P., &Smith, R. J. F. (1994b). Intra- and interspecific avoidance of areas marked with skin extract from brook sticklebacks (Culaea inconstans) in a natural habitat.Journal of Chemical Ecology,20, 1517–1524.
Chivers, D. P., &Smith, R. J. F. (1994c). The role of experience and chemical alarm signalling in predator recognition by fathead minnows,Pimephales promelas.Journal of Fish Biology,44, 273–285.
Chivers, D. P., &Smith, R. J. F. (1995a). Chemical recognition of risky habitats is culturally transmitted among fathead minnows,Pimephales promelas (Osteichthyes, Cyprinidae).Ethology,99, 286–296.
Chivers, D. P., &Smith, R. J. F. (1995b). Free-living fathead minnows rapidly learn to recognize pike as predators.Journal of Fish Biology,46, 949–954.
Chivers, D. P., &Smith, R. J. F. (1998). Chemical alarm signalling in aquatic predator-prey systems: A review and prospectus.Écoscience,5, 338–352.
Conover, M. R. (1987). Acquisition of predator information by active and passive mobbers in ring-billed gull colonies.Behaviour,102, 41–57.
Conover, M. R., &Perito, J. J. (1981). Response of starlings to distress calls and predator models holding conspecific prey.Zeitschrift für Tierpsychologie,57, 163–172.
Cook, M., &Mineka, S. (1989). Observational conditioning of fear to fear-relevant versus fear-irrelevant stimuli in rhesus monkeys.Journal of Abnormal Psychology,98, 448–459.
Cook, M., &Mineka, S. (1990). Selective associations in the observational conditioning of fear in rhesus monkeys.Journal of Experimental Psychology: Animal Behavior Processes,16, 372–389.
Cook, M., Mineka, S., Wolkenstein, B., &Laitsch, K. (1985). Observational conditioning of snake fear in unrelated rhesus monkeys.Journal of Abnormal Psychology,94, 591–610.
Coss, R. G. (1978). Perceptual determinants of gaze aversion by the lesser mouse lemur (Microcebus murinus): The role of two facing eyes.Behaviour,64, 248–270.
Csányi, V. (1985). Ethological analysis of predator avoidance by the paradise fish (Macropodus opercularis L.): I. Recognition and learning of predators.Behaviour,92, 227–240.
Curio, E. (1988). Cultural transmission of enemy recognition by birds. In T. R. Zentall & B. G. Galef, Jr. (Eds.),Social learning: Psychological and biological perspectives (pp. 75–97). Hillsdale, NJ: Erlbaum.
Curio, E. (1993). Proximate and developmental aspects of antipredator behavior.Advances in the Study of Behavior,22, 135–238.
Curio, E., Ernst, U., &Vieth, W. (1978). The adaptive significance of avian mobbing: II. Cultural transmission of enemy recognition in blackbirds: Effectiveness and some constraints.Zeitschrift für Tierpsychologie,48, 184–202.
Dunham, K. M. (1997). Population growth of mountain gazellesGazella gazella reintroduced to Central Arabia.Biological Conservation,81, 205–214.
Galef, B. G., Jr. (1996). Social enhancement of food preferences in Norway rats: A brief review. In C. M. Heyes & B. G. Galef, Jr. (Eds.),Social learning in animals: The roots of culture (pp. 49–64). New York: Academic Press.
Galef, B. G., Jr., &Durlach, P. J. (1993). Absence of blocking, overshadowing, and latent inhibition in social enhancement of food preferences.Animal Learning & Behavior,21, 214–220.
Galef, B. G., Jr., &Whiskin, E. E. (2001). Interaction between social and individual learning in food preferences of Norway rats.Animal Behaviour,62, 41–46.
Gšz, H. (1941). Über den Art- und Individualgeruch bei Fischen.Zeitschrift für vergleichende Physiologie,29, 1–45.
Griffin, A. S. (2003). Training tammar wallabies to respond to predators: Linking experimental psychology to conservation.International Journal of Comparative Psychology,16, 111–129.
Griffin, A. S., Blumstein, D. T., &Evans, C. S. (2000). Training captive-bred or translocated animals to avoid predators.Conservation Biology,14, 1317–1326.
Griffin, A. S., &Evans, C. S. (2003). Social learning of antipredator behaviour in a marsupial.Animal Behaviour,66, 485–492.
Griffin, A. S., Evans, C. S., &Blumstein, D. T. (2002). Selective learning in a marsupial.Ethology,108, 1103–1114.
Hall, D., &Suboski, M. D. (1995). Visual and olfactory stimuli in learned release of alarm reactions by zebra danio fish (Brachydanio rerio).Neurobiology of Learning & Memory,63, 229–240.
Hall, K. R. L. (1968). Social learning in monkeys. In P. C. Jay (Ed.),Primates: Studies in adaptation and variability (pp. 383–397). New York: Holt, Rinehart & Winston.
Hauser, M. D. (1988). How infant vervet monkeys learn to recognize starling alarm calls: The role of experience.Behaviour,105, 187–201.
Herzog, M., &Hopf, S. (1984). Behavioral responses to species-specific warning calls in infant squirrel monkeys reared in social isolation.American Journal of Primatology,7, 99–106.
Heyes, C. M. (1994). Social learning in animals: Categories and mechanisms.Biological Review,69, 207–231.
Howell, B. R. (1994). Fitness of hatchery-reared fish for survival in the sea.Aquaculture & Fisheries Management,25(Suppl. 1), 3–17.
Huebner, D. K., Lentz, J. L., Wooley, M. J., &King, J. E. (1979). Responses to snakes by surrogate- and mother-reared squirrel monkeys.Bulletin of the Psychonomic Society,14, 33–36.
Järvi, T., &Uglem, I. (1993). Predator training improves the antipredator behaviour of hatchery reared Atlantic salmon (Salmo salar) smolt.Nordic Journal of Freshwater Research,68, 63–71.
Kalish, H. I. (1967). Strength of fear as a function of the number of acquisition and extinction trials. In R. M. Elliott, G. Lindzey, & K. Mac-Corquodale (Eds.),Foundations of conditioning and learning (pp. 428–439). New York: Appleton-Century-Crofts.
Klopfer, P. H. (1957). An experiment of empathic learning in ducks.American Naturalist,41, 61–63.
Kodric-Brown, A., &Nicoletto, P. F. (2001). Female choice in the guppy (Poecilia reticulata): The interaction between male color and display.Behavioral Ecology & Sociobiology,50, 346–351.
Kramer, G., &von St. Paul, U. (1951). Über angeborenes und erworbenes Feinderkennen beim Gimpel (Pyrrhula pyrrhula L.).Behaviour,3, 243–255.
Kruuk, H. (1976). The biological function of gulls’ attraction towards predators.Animal Behaviour,24, 146–153.
Lima, S. L., &Dill, L. M. (1990). Behavioral decisions made under the risk of predation: A review and prospectus.Canadian Journal of Zoology,68, 619–640.
Lore, R., Blanc, A., &Suedfeld, P. (1971). Empathic learning of a passive-avoidance response in domesticatedRattus norvegicus.Animal Behaviour,19, 112–114.
Lorenz, K. Z. (1952).King Solomon’s ring. New light on animal ways. New York: Crowell.
Lorenz, K. Z. (1969). Innate bases of learning. In K. H. Pribram (Ed.),On the biology of learning (pp. 13–93). New York: Harcourt, Brace & World.
Magurran, A. E. (1989). Acquired recognition of predator odour in the European minnow (Phoxinus phoxinus).Ethology,82, 216–223.
Magurran, A. E. (1999). The causes and consequences of geographic variation in antipredator behavior: Perspectives from fish populations. In S. A. Foster & J. A. Endler (Eds.),Geographic variation in behavior: Perspectives on evolutionary mechanisms (pp. 139–163). Oxford: Oxford University Press.
Maloney, R. F., &McLean, I. G. (1995). Historical and experimental learned predator recognition in free-living New Zealand robins.Animal Behaviour,50, 1193–1201.
Mateo, J. M. (1996). The development of alarm-call response behaviour in free-living juvenile Belding’s ground squirrels.Animal Behaviour,52, 489–505.
Mateo, J. M., &Holmes, W. G. (1997). Development of alarm-call responses in Belding’s ground squirrels: The role of dams.Animal Behaviour,54, 509–524.
Mathis, A., Chivers, D. P., &Smith, R. J. F. (1996). Cultural transmission of predator recognition in fishes: Intraspecific and interspecific learning.Animal Behaviour,51, 185–201.
Maynard, D. J.,Flagg, T. A., &Mahnken, C. V.W. (1995). A review of seminatural culture strategies for enhancing the postrelease survival of anadromous salmonid. In H. L. Schramm, Jr., & R. G. Piper (Eds.),American Fisheries Society Symposium 15 (pp. 307–314). Bethesda, MD.
McLean, I. G., Hölzer, C., &Strudholme, B. J. S. (1999). Teaching predator-recognition to a naive bird: Implications for management.Biological Conservation,87, 123–130.
McLean, I. G., Lundie-Jenkins, G., &Jarman, P. J. (1996). Teaching an endangered mammal to recognise predators.Biological Conservation,75, 51–62.
Mineka, S., &Cook, M. (1986). Immunization against the observational conditioning of snake fear in rhesus monkeys.Journal of Abnormal Psychology,95, 307–318.
Mineka, S., &Cook, M. (1988). Social learning and the acquisition of snake fear in monkeys. In T. R. Zentall & B. G. Galef, Jr. (Eds.),Social learning: Psychological and biological perspectives (pp. 51–73). Hillsdale, NJ: Erlbaum.
Mineka, S., &Cook, M. (1993). Mechanisms involved in the observational conditioning of fear.Journal of Experimental Psychology: General,122, 23–38.
Mineka, S., Davidson, M., Cook, M., &Keir, R. (1984). Observa tional conditioning of snake fear in rhesus monkeys.Journal of Abnormal Psychology,93, 355–372.
Mirza, R. S., &Chivers, D. P. (2000). Predator-recognition training enhances survival of brook trout: Evidence from laboratory and field-enclosure studies.Canadian Journal of Zoology,78, 2198–2208.
Mirza, R. S., &Chivers, D. P. (2001). Learned recognition of heterospecif ic alarm signals: The importance of a mixed predator diet.Ethology,107, 1007–1018.
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.
Palleroni, A. R. (1999).Anti-predator behavior of galliform birds. Unpublished doctoral dissertation, University of California, Davis.
Peters, R. A., Clifford, C. W. G., &Evans, C. S. (2002). Measuring the structure of dynamic visual signals.Animal Behaviour,64, 131–146.
Shettleworth, S. J. (1998).Cognition, evolution, and behavior. New York: Oxford University Press.
Shriner, W. M. (1999). Antipredator responses to a previously neutral sound by free-living adult golden-mantled ground squirrels,Spermophilus lateralis (Sciuridae).Ethology,105, 747–757.
Springer, M. S., Westerman, M., &Kirsch, J. A. W. (1994). Relationships among orders and families of marsupials based on 12S ribosomal DNA sequences and the timing of the marsupial radiation.Journal of Mammalian Evolution,2, 85–115.
Suboski, M. D. (1990). Releaser-induced recognition learning.Psychological Review,97, 271–284.
Suboski, M. D. (1992). Releaser-induced recognition learning by amphibians and reptiles.Animal Learning & Behavior,20, 63–82.
Suboski, M. D., Bain, S., Carty, A. E., McQuoid, L. M., Seelen, M. I., &Seifert, M. (1990). Alarm reaction in acquisition and social transmission of simulated-predator recognition by zebra danio fish (Brachydanio rerio).Journal of Comparative Psychology,104, 101–112.
Trainor, B. C., &Basolo, A. L. (2000). An evaluation of video playback usingXiphophorus helleri.Animal Behaviour,59, 83–89.
van Heezik, Y., Seddon, P. J., &Maloney, R. F. (1999). Helping reintroduced houbara bustards avoid predation: Effective anti-predator training and the predictive value of pre-release behaviour.Animal Conservation,2, 155–163.
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.Animal Behaviour,28, 1217–1229.
von Frisch, K. (1938). Zur Psychologie des Fische-Schwarmes.Naturwissenschaften,26, 601–606.
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.
Wolf, C. M., Griffith, B., Reed, C., &Temple, S. A. (1996). Avian and mammalian translocations: Update and reanalysis of 1987 survey data.Conservation Biology,10, 1142–1154.
Wynne, C. D. L., &McLean, I. G. (1999). The comparative psychology of marsupials.Australian Journal of Psychology,51, 1–6.
Young, S. L., &Fanselow, M. S. (1992). Associative regulation of Pavlovian fear conditioning: Unconditional stimulus intensity, incentive shifts, and latent inhibition.Journal of Experimental Psychology: Animal Behavior Processes,18, 400–413.
Yunker, W. K., Wein, D. E., &Wisenden, B. D. (1999). Conditioned alarm behavior in fathead minnows (Pimephales promelas) resulting from association of chemical alarm pheromone with a nonbiological visual stimulus.Journal of Chemical Ecology,25, 2677–2686.
The author thanks Louis Lefebvre, Jeff Galef, and Douglas Chivers for comments on this paper. A.S.G. is supported by the Swiss National Foundation for Scientific Research.
About this article
Cite this article
Griffin, A.S. Social learning about predators: a review and prospectus. Animal Learning & Behavior 32, 131–140 (2004). https://doi.org/10.3758/BF03196014
- Social Learning
- Alarm Call
- Predator Avoidance
- Fathead Minnow
- Antipredator Behavior