Brown, Grant E. and Ferrari, Maud C. O. and Malka, Patrick H. and Russo, Stephanie and Tressider, Michelle and Chivers, Douglas P. (2011) Generalization of predators and nonpredators by juvenile rainbow trout: learning what is and is not a threat. Animal Behaviour, 81 (6). pp. 1249-1256. ISSN 00033472
- Accepted Version
Official URL: http://dx.doi.org/10.1016/j.anbehav.2011.03.013
Learned recognition of novel predators allows prey to respond to ecologically relevant threats. Prey could minimize the costs associated with learning the identity of both predators and nonpredators by making educated guesses on the identity of a novel species based on their similarities with known predators and nonpredators, a process known as generalization. Here, we tested whether juvenile rainbow trout, Oncorhynchus mykiss, have the ability to generalize information from a known predator (experiment 1) or a known harmless species (experiment 2) to closely related but novel species. In experiment 1, we taught juvenile trout to recognize a predatory pumpkinseed sunfish, Lepomis gibbosus, by pairing pumpkinseed odour with conspecific alarm cues or a distilled water control. We then tested the trout for a response to pumpkinseeds and to novel longear sunfish, Lepomis megalotis (same genus as pumpkinseed), rock bass, Ambloplites rupestris (same family as pumpkinseed) or yellow perch, Perca flavescens (different family). Trout showed strong learned recognition of pumpkinseed and longear sunfish odour and a weak learned response to rock bass odour but no recognition of yellow perch. In experiment 2, we used latent inhibition to teach juvenile trout that pumpkinseeds were harmless. During subsequent predator learning trials, trout did not learn to recognize pumpkinseed or longear sunfish odour as potential threats, but they did learn that rock bass and yellow perch were threatening. Taken together, these results demonstrate that juvenile rainbow trout can generalize learned recognition of both predator and nonpredator odours based on the phylogenetic relatedness of predators.
|Divisions:||Concordia University > Faculty of Arts and Science > Biology|
|Authors:||Brown, Grant E. and Ferrari, Maud C. O. and Malka, Patrick H. and Russo, Stephanie and Tressider, Michelle and Chivers, Douglas P.|
|Journal or Publication:||Animal Behaviour|
|Digital Object Identifier (DOI):||10.1016/j.anbehav.2011.03.013|
|Keywords:||acquired predator recognition; alarm cue; generalization; latent inhibition; rainbow trout; threat-sensitive trade-off|
|Deposited By:||DANIELLE DENNIE|
|Deposited On:||06 Jun 2011 15:24|
|Last Modified:||24 Aug 2016 21:26|
Acquistapace et al., 2003 P. Acquistapace, B.A. Hazlett and F. Gherardi, Unsuccessful predation and learning of predator cues by crayfish, Journal of Crustacean Biology 23 (2003), pp. 364–370.
Akins et al., 1994 C.K. Akins, M. Domjan and G. Gutiérrez, Topography of sexually conditioned behavior in male Japanese quail (Coturnix japonica) depends on the CS–US interval, Journal of Experimental Psychology: Animal Behavior Processes 20 (1994), pp. 199–209.
Allen et al., 2002 M.T. Allen, L. Chelius, V. Masand, M.A. Gluck, C.E. Myers and G. Schnirman, A comparison of latent inhibition and learned irrelevance pre-exposure effects in rabbit and human eyeblink conditioning, Integrative Physiology and Behavioral Science 37 (2002), pp. 188–214.
Barco et al., 2010 A. Barco, M. Claremont, D.G. Reid, R. Houart, P. Bouchet, S.T. Williams, C. Cruaud, A. Couloux and M. Oliverio, A molecular phylogenetic framework for the Muricidae, a diverse family of carnivorous gastropods, Molecular Phylogenetics and Evolution 56 (2010), pp. 1025–1039.
Berejikian et al., 2003 B.A. Berejikian, E.P. Tezak and A.L. LaRae, Innate and enhanced predator recognition in hatchery-reared Chinook salmon, Environmental Biology of Fishes 67 (2003), pp. 241–251.
Brown, 2003 G.E. Brown, Learning about danger: chemical alarm cues and local risk assessment in prey fishes, Fish and Fisheries 4 (2003), pp. 227–234.
Brown and Chivers, 2005 G.E. Brown and D.P. Chivers, Learning as an adaptive response to predation. In: P. Barbosa and I. Castellanos, Editors, Ecology of Predator–Prey Interactions, Oxford University Press, Oxford (2005), pp. 34–54.
Brown and Smith, 1997 G.E. Brown and R.J.F. Smith, Conspecific skin extracts elicit antipredator responses in juvenile rainbow trout (Oncorhynchus mykiss), Canadian Journal of Zoology 75 (1997), pp. 1916–1922.
Brown and Smith, 1998 G.E. Brown and R.J.F. Smith, Acquired predator recognition in juvenile rainbow trout (Oncorhynchus mykiss): conditioning hatchery-reared fish to recognize chemical cues of a predator, Canadian Journal of Fisheries and Aquatic Sciences 55 (1998), pp. 611–617.
Brown et al., 2006 G.E. Brown, T. Bongiorno, D.M. DiCapua, L.I. Ivan and E. Roh, Effects of group size on the threat-sensitive response to varying concentrations of chemical alarm cues by juvenile convict cichlids, Canadian Journal of Zoology 84 (2006), pp. 1–8.
Brown, 1984 J.A. Brown, Parental care and the ontogeny of predator-avoidance in two species of centrarchid fish, Animal Behaviour 32 (1984), pp. 113–119.
Chandra et al., 2010 S.B.C. Chandra, G.A. Wright and B.H. Smith, Latent inhibition in the honey bee, Apis mellifera: is it a unitary phenomenon?, Animal Cognition 13 (2010), pp. 805–815.
Chivers and Mirza, 2001 D.P. Chivers and R.S. Mirza, Predator diet cues and the assessment of predation risk by aquatic vertebrates: a review and prospectus. In: A. Marchlewska-Koj, J.J. Lepri and D. Müller-Schwarze, Editors, Chemical Signals in Vertebrates. Vol. 9, Kluwer Academic, New York (2001), pp. 227–284.
Crawford et al., 1993 L.L. Crawford, K.S. Holloway and M. Domjan, The nature of sexual reinforcement, Journal of the Experimental Analysis of Behavior 60 (1993), pp. 55–66.
Curio et al., 1978 E. Curio, U. Ernst and W. Vieth, The adaptive significance of avian mobbing: II. Cultural transmission of enemy recognition in blackbirds: effectiveness and some constraints, Zeitschrift für Tierpsychologie 48 (1978), pp. 184–202.
Dalesman et al., 2007a S. Dalesman, S.D. Rundle and P.A. Cotton, Predator regime influences innate anti-predator behaviour in the freshwater gastropod Lymnaea stagnalis, Freshwater Biology 52 (2007), pp. 2134–2140.
Dalesman et al., 2007b S. Dalesman, S.D. Rundle, D.T. Bilton and P.A. Cotton, Phylogenetic relatedness and ecological interactions determine antipredator behavior, Ecology 88 (2007), pp. 2462–2467.
Dall et al., 2005 S.R.X. Dall, L.-A. Giraldeau, O. Olsson, J.M. McNamara and D.W. Stephens, Information and its use by animals in evolutionary ecology, Trends in Ecology & Evolution 20 (2005), pp. 187–193.
Darwish et al., 2005 T.L. Darwish, R.S. Mirza, A.O.H.C. Leduc and G.E. Brown, Acquired recognition of novel predator odour cocktails by juvenile glowlight tetras, Animal Behaviour 70 (2005), pp. 83–89.
Drezner-Levy et al., 2009 T. Drezner-Levy, B.H. Smith and S. Shafir, The effect of foraging specialization on various learning tasks in the honey bee (Apis mellifera), Behavioral Ecology and Sociobiology 64 (2009), pp. 135–148.
Ferrari and Chivers, 2006 M.C.O. Ferrari and D.P. Chivers, The role of latent inhibition in acquired predator recognition by fathead minnows, Canadian Journal of Zoology 84 (2006), pp. 505–509.
Ferrari and Chivers, 2009 M.C.O. Ferrari and D.P. Chivers, Latent inhibition of predator recognition by embryonic amphibians, Biology Letters 5 (2009), pp. 160–162.
Ferrari et al., 2005 M.C.O. Ferrari, J.J. Trowell, G.E. Brown and D.P. Chivers, The role of learning in the development of threat-sensitive predator avoidance by fathead minnows, Animal Behaviour 70 (2005), pp. 777–784.
Ferrari et al., 2006 M.C.O. Ferrari, T. Kapitania-Kwok and D.P. Chivers, The role of learning in the development of threat-sensitive predator avoidance: the use of predator cue concentration by fathead minnows, Behavioral Ecology and Sociobiology 60 (2006), pp. 522–527.
Ferrari et al., 2007 M.C.O. Ferrari, A. Gonzalo, F. Messier and D.P. Chivers, Generalization of learned predator recognition: an experimental test and framework for future studies, Proceedings of the Royal Society B 274 (2007), pp. 1853–1859.
Ferrari et al., 2008 M.C.O. Ferrari, F. Messier and D.P. Chivers, Can prey exhibit threat-sensitive generalization of predator recognition? Extending the predator recognition continuum hypothesis, Proceedings of the Royal Society B 275 (2008), pp. 1811–1816.
Ferrari et al., 2009 M.C.O. Ferrari, G.E. Brown, F. Messier and D.P. Chivers, Threat-sensitive generalization of predator recognition by larval amphibians, Behavioral Ecology and Sociobiology 63 (2009), pp. 1369–1375.
Ferrari et al., 2010 M.C.O. Ferrari, B.D. Wisenden and D.P. Chivers, Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus, Canadian Journal of Zoology 88 (2010), pp. 698–724.
Gall and Brodie, 2009 B.G. Gall and E.D. Brodie Jr., Behavioral avoidance of injured conspecific and predatory chemical stimuli by larvae of the aquatic caddisfly Hesperophylax occidentalis, Canadian Journal of Zoology 87 (2009), pp. 1009–1015.
Gonzalo et al., 2009 A. Gonzalo, P. López and J. Martin, Risk level of chemical cues determines retention of recognition of new predators in Iberian green frog tadpoles, Behavioral Ecology and Sociobiology 64 (2009), pp. 1117–1123.
Griffin et al., 2001 A.S. Griffin, C.S. Evans and D.T. Blumstein, Learning specificity in acquired predator recognition, Animal Behaviour 62 (2001), pp. 577–598.
Gyssels and Stoks, 2006 F. Gyssels and R. Stoks, Behavioral responses to fish kairomones and autotomy in a damselfly, Journal of Ethology 24 (2006), pp. 79–83.
Helfman, 1989 G.S. Helfman, Threat-sensitive predator avoidance in damselfish-trumpetfish interactions, Behavioral Ecology and Sociobiology 24 (1989), pp. 47–58.
Kim et al., 2011 J.-W. Kim, J.L.A. Wood, J.W.A. Grant and G.E. Brown, Acute and chronic increases in predation risk affect the territorial behaviour of juvenile Atlantic salmon in the wild, Animal Behaviour 81 (2011), pp. 93–99.
Langerhans and DeWitt, 2002 R.B. Langerhans and T.J. DeWitt, Plasticity constrained: over-generalized induction cues cause maladaptive phenotypes, Evolutionary Ecology Research 4 (2002), pp. 857–870.
Leduc et al., 2004 A.O.H.C. Leduc, M.C.O. Ferrari, J.M. Kelly and G.E. Brown, Learning to recognize novel predators under weakly acidic conditions: the effects of reduced pH on acquired predator recognition by juvenile rainbow trout (Oncorhynchus mykiss), Chemoecology 14 (2004), pp. 107–112.
Lima, 1998 S.L. Lima, Nonlethal effects in the ecology of predator–prey interactions: what are the ecological effects of anti-predator decision-making?, Bioscience 48 (1998), pp. 25–34.
Lima and Dill, 1990 S.L. Lima and L.M. Dill, Behavioral decisions made under the risk of predation: a review and prospectus, Canadian Journal of Zoology 68 (1990), pp. 619–640.
Loy et al., 2006 I. Loy, V. Fenrnández and F. Acebes, Conditioning of tentacle lowering in the snail (Helix aspersa): acquisition, latent inhibition, overshadowing, second-order conditioning and sensory preconditioning, Learning & Behavior 34 (2006), pp. 305–314.
McLean et al., 1996 I.G. McLean, G. Lundie-Jenkins and P.J. Jarma, Teaching an endangered mammal to recognise predators, Biological Conservation 56 (1996), pp. 51–62.
Mathis and Smith, 1993 A. Mathis and R.J.F. Smith, 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, Animal Behaviour 46 (1993), pp. 645–656.
Mery and Kawecki, 2003 F. Mery and T.J. Kawecki, A fitness cost of learning ability in Drosphila melanogaster, Proceedings of the Royal Society B 270 (2003), pp. 2465–2469.
Mery and Kawecki, 2005 F. Mery and T.J. Kawecki, A cost of long-term memory in Drosophila, Science 308 (2005), p. 1148.
Mineka and Cook, 1986 S. Mineka and M. Cook, Immunization against the observational conditioning of snake fear in rhesus monkeys, Journal of Abnormal Psychology 95 (1986), pp. 307–318.
Mirza and Chivers, 2000 R.S. Mirza and D.P. Chivers, Predator-recognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies, Canadian Journal of Zoology 78 (2000), pp. 2198–2208.
Olson et al., 1995 M.H. Olson, G.G. Mittelbach and C.W. Osenberg, Competition between predator and prey: resource: based mechanisms and implications for stage-structured dynamics, Ecology 76 (1995), pp. 1758–1771.
Pollock et al., 2003 M.S. Pollock, D.P. Chivers, R.S. Mirza and B.D. Wisenden, Fathead minnows, Pimephales promelas, learn to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans, Environmental Biology of Fishes 66 (2003), pp. 313–319.
Rankin et al., 2009 C.H. Rankin, T. Abrams, R.J. Barry, S. Bhatnagar, D.F. Clayton, J. Colombo, G. Coppola, M.A. Geyer, D.L. Glanzman and S. Marsland et al., Habituation revisited: an updated and revised description of the behavioral characteristics of habituation, Neurobiology of Learning and Memory 92 (2009), pp. 135–138.
Scott and Crossman, 1973 W.B. Scott and E.J. Crossman, Freshwater fishes of Canada, Fisheries Research Board of Canada Bulletin 184 (1973).
Sih, 1992 A. Sih, Prey uncertainty and the balancing of antipredator and feeding needs, American Naturalist 139 (1992), pp. 1052–1069.
Smith et al., 2008 J.J. Smith, A.O.H.C. Leduc and G.E. Brown, Chemically mediated learning in juvenile rainbow trout. Does predator odour pH influence intensity and retention of acquired predator recognition?, Journal of Fish Biology 72 (2008), pp. 1750–1760.
Stankowich and Coss, 2007 T. Stankowich and R.G. Coss, The re-emergence of felid camouflage with the decay of predator recognition in deer under relaxed selection, Proceedings of the Royal Society B 274 (2007), pp. 175–182.
Vavrek and Brown, 2009 M.A. Vavrek and G.E. Brown, Threat-sensitive responses to disturbance cues in juvenile convict cichlids and rainbow trout, Annales Zoologici Fennici 46 (2009), pp. 171–180.
Vilhunen and Hirvonen, 2003 S. Vilhunen and H. Hirvonen, Innate antipredator response of Arctic charr (Salvelinus alpinus) depends on predator species and their diet, Behavioral Ecology and Sociobiology 55 (2003), pp. 1–10.
Zhao et al., 2006 X. Zhao, M.C.O. Ferrari and D.P. Chivers, Threat-sensitive learning of predator odours by a prey fish, Behaviour 143 (2006), pp. 1103–1121.
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