Login | Register

Growth rate and retention of learned predator cues by juvenile rainbow trout: faster-growing fish forget sooner


Growth rate and retention of learned predator cues by juvenile rainbow trout: faster-growing fish forget sooner

Brown, Grant E. and Ferrari, Maud C. O. and Malka, Patrick H. and Oligny, Marie-Anne and Romano, Matthew and Chivers, Douglas P. (2011) Growth rate and retention of learned predator cues by juvenile rainbow trout: faster-growing fish forget sooner. Behavioral Ecology and Sociobiology, 65 (6). pp. 1267-1276. ISSN 0340-5443

PDF - Accepted Version

Official URL: http://dx.doi.org/10.1007/s00265-011-1140-3


Under conditions of spatial and/or temporal variability in predation risk, prey organisms often rely on acquired predator recognition to balance the trade-offs between energy intake and risk avoidance. The question of ‘for how long’ should prey retain this learned information is poorly understood. Here, we test the hypothesis that the growth rate experienced by prey should influence the length of the ‘memory window’. In a series of laboratory experiments, we manipulated growth rate of juvenile rainbow trout and conditioned them to recognize a novel predator cue. We subsequently tested for learned recognition either 24 h or 8 days post-conditioning. Our results suggest that trout with high versus low growth rates did not differ in their response to learned predator cues when tested 24 h post-conditioning. However, trout on a high growth rate exhibited no response to the predator cues after 8 days (i.e. did not retain the recognition of the predator odour), whereas trout on a lower growth rate retained a strong recognition of the predator. Trout that differed in their growth rate only after conditioning did not differ in their patterns of retention, demonstrating growth rate after learning does not influence retention. Trout of different initial sizes fed a similar diet (percent body mass per day) showed no difference in retention of the predator cue. Together, these data suggest that growth rate at the time of conditioning determines the ‘memory window’ of trout. The implications for threat-sensitive predator avoidance models are described.

Divisions:Concordia University > Faculty of Arts and Science > Biology
Item Type:Article
Authors:Brown, Grant E. and Ferrari, Maud C. O. and Malka, Patrick H. and Oligny, Marie-Anne and Romano, Matthew and Chivers, Douglas P.
Journal or Publication:Behavioral Ecology and Sociobiology
Date:18 January 2011
Keywords:Acquired predator recognition – Memory window – Antipredator behaviour – Salmonids – Growth rate – Trade-offs
ID Code:7634
Deposited On:06 Jun 2011 15:08
Last Modified:06 Jun 2011 15:08
Adriaenssens B, Johnsson JI (2011) Shy trout grow faster: exploring links between personality and fitness-related traits in the wild. Behav Ecol. doi:10.1093/beheco/arq185

Alsop DH, Wood CM (1997) The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykiss). J Exp Biol 200:2337–2346

Berejikian BA, Smith RJF, Tezak PE, Schroder SL, Knusden CM (1999) Chemical alarm signals and complex hatchery rearing habitats affect antipredator and survival of chinook salmon (Oncorhynchus tshawytscha) juveniles. Can J Fish Aquat Sci 56:830–838

Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368

Bishop TD, Brown JA (1992) Threat-sensitive foraging by larval threespine sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 31:133–138

Brown GE (2003) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish 4:227–234

Brown C, Laland KN (2001) Social learning and life skills training for hatchery reared fish. J Fish Biol 59:471–493

Brown GE, Smith RJF (1997) Conspecific skin extracts elicit antipredator responses in juvenile rainbow trout (Oncorhynchus mykiss). Can J Zool 75:1916–1922

Brown GE, Smith RJF (1998) Acquired predator recognition in juvenile rainbow trout (Oncorhynchus mykiss): conditioning hatchery-reared fish to recognize chemical cues of a predator. Can J Fish Aquat Sci 55:611–617

Brown GE, Bongiorno T, DiCapua DM, Ivan LI, Roh E (2006) Effects of group size on the threat-sensitive response to varying concentrations of chemical alarm cues by juvenile convict cichlids. Can J Zool 84:1–8

Brown GE, Macnaughton CJ, Elvidge CK, Ramnarine I, Godin J-GJ (2009a) Provenance and threat-sensitive predator avoidance patterns in wild-caught Trinidadian guppies. Behav Ecol Sociobiol 63:699–706

Brown GE, Harvey MC, Leduc AOHC, Ferrari MCO, Chivers DP (2009b) Social context, competitive interactions and the dynamic nature of antipredator responses of juvenile rainbow trout. J Fish Biol 79:552–562

Brydges NM, Heathcote RJP, Braithwaite VA (2008) Habitat stability and predation pressure influence learning and memory in populations of three-spined sticklebacks. Anim Behav 75:935–942

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

Cuthill IC, Kacelnik A, Krebs JR, Haccou P, Iwasa Y (1990) Starlings exploiting patches: the effect of recent experience on foraging decisions. Anim Behav 40:625–640

Darwish TL, Mirza RS, Leduc AOHC, Brown GE (2005) Acquired recognition of novel predator odour cocktails by juvenile glowlight tetras. Anim Behav 70:83–89

Dunlap AS, McLinn CM, MacCormick HA, Scott ME, Kerr B (2009) Why some memories do not last a lifetime: dynamic long-term retrieval in changing environments. Behav Ecol 20:1096–1105

Eiben B, Persons M (2007) The effect of prior exposure to predator cues on chemically-mediated defensive behavior and survival in the wolf spider Rabidosa rabida (Aranae: Lycosidae). Behaviour 144:889–906

Feary DA, McCormick MI, Jones GP (2009) Growth of reef fishes in response to live coral cover. J Exp Mar Biol Ecol 373:45–49

Ferrari MCO, Chivers DP (2006) Learning threat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information? Anim Behav 71:19–26

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

Ferrari MCO, Sih A, Chivers DP (2009) The paradox of risk allocation: a review and prospectus. Anim Behav 78:579–585

Ferrari MCO, Brown GE, Bortolotti GR, Chivers DP (2010) Linking predator risk and uncertainty to adaptive forgetting: a theoretical framework and empirical test using tadpoles. Proc R Soc Lond B 277:2205–2210

Fitting S, Booze RM, Gilbert CA, Mactutus CF (2008) Effects of chronic adult dietary restriction on spatial learning in the aged F344 x BN hybrid F1 rat. Physiol Behav 93:560–569

Gonzalo A, López P, Martín J (2009) Learning, memory and apparent forgetting of chemical cues from new predators by Iberian green frog tadpoles. Anim Cogn 12:745–750

Gonzalo A, López P, Martin J (2010) Risk level of chemical cues determines retention of recognition of new predators in Iberian green frog tadpoles. Behav Ecol Sociobiol 64:1117–1123

Grubb TC Jr, Pravosudov VV (1994) Toward a general theory of energy management in wintering birds. J Avian Biol 25:255–260

Griffin AS (2004) Social learning about predators: a review and prospectus. Learn Behav 32:131–140

Hawkins LA, Armstrong JD, Magurran AE (2007) A test of how predator conditioning influence survival of hatchery-reared Atlantic salmon, Salmo salar, in restocking programmes. Fish Manage Ecol 14:291–293

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

Hirvonen H, Ranta E, Rita H, Peuhkuri N (1999) Significance of memory properties in prey choice decisions. Ecol Model 115:177–189

Kamunde C, Wood CM (2003) The influence of ration size on copper homeostasis during sublethal dietary copper exposure in juvenile rainbow trout, Oncorhynchus mykiss. Aquat Toxicol 62:235–254

Kerr B, Feldman MW (2003) Carving the cognitive niche: optimal learning strategies in homogeneous and heterogeneous environments. J Theor Biol 220:169–188

Kotler BP (1992) Behavioural resource depression and decaying perceived risk of predation in two species of coexisting gerbils. Behav Ecol Sociobiol 30:239–244

Kraemer PJ, Golding JM (1997) Adaptive forgetting in animals. Psych Bull Rev 4:480–491

Leduc AOHC, Roh E, Brown GE (2009) Effects of acid rainfall on juvenile Atlantic salmon (Salmo salar) antipredator behaviour: loss of chemical alarm function and potential survival consequences during predation. Mar Freshwater Res 60:1223–1230

Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

Lima SL, Steury TD (2005) Perception of predation risk: the foundation of nonlethal predator-prey interactions. In: Castellanos I, Barbosa P (eds) Ecology of predator-prey interactions. Oxford University Press, Oxford, pp 166–188

Mackney PA, Hughes RN (1995) Foraging behaviour and memory window in sticklebacks. Behaviour 132:1241–1253

Mangel M (1990) Dynamic information in uncertain and changing worlds. J Theor Biol 146:317–332

Martel G, Dill LM (1993) Feeding and aggressive behaviours in juvenile coho salmon (Oncorhynchus kisutch) under chemically-mediated risk of predation. Behav Ecol Sociobiol 32:365–370

McNamara JM, Houston AI (1987) Memory and the efficient use of information. J Theor Biol 125:385–395

Mirza RS, Chivers DP (2000) Predator-recognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies. Can J Zool 78:2198–2208

Nilsson PA, Brönmark C (2000) Prey vulnerability to a gape-limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88:539–546

Pravosudov VV, Clayton NS (2001) Effects of demanding foraging conditions on cache retrieval accuracy in food-caching mountain chickadees (Poecile gambeli). Proc R Soc Lond B 268:363–368

Pravosudov VV, Clayton NS (2002) A test of the adaptive specialization hypothesis: population differences in caching, memory and the hippocampus in black-capped chickadees (Poecile atricapilla). Behav Neurosci 116:515–522

Reinhardt UG, Healey MC (1999) Season- and size-dependent risk taking in juvenile coho salmon: experimental evaluation of asset protection. Anim Behav 57:923–933

Roitberg BD, Zimmermann K, Hoffmeister TS (2010) Dynamic response to danger in a parasitoid wasp. Behav Ecol Sociobiol 64:627–637

Shettleworth SJ, Plowright CMS (1992) How pigeons estimate rates of prey encounter. J Exp Psych: Anim Behav Proc 18:219–235

Shier DM, Owings DH (2007) Effects of social learning on predator training and postrelease survival in juvenile black-tailed prairie dogs, Cynomys ludovicianus. Anim Behav 73:567–577

Skow CD, Jakob EM (2006) Jumping spiders attend to context during learned avoidance of aposematic prey. Behav Ecol 17:34–40

Speed MP (2000) Warning signals, receiver psychology and predator memory. Anim Behav 60:269–278

Vavrek MA, Elvidge CK, DeCaire R, Belland B, Jackson CD, Brown GE (2008) Disturbance cues in freshwater prey fishes: do juvenile convict cichlids and rainbow trout respond to ammonium as an ‘early warning’ signal? Chemoecol 18:255–261

Werner EE, Gilliam JF, Hall DJ, Mittlebach GG (1983) An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540–1548

Wisenden BD, Klitzke J, Nelson R, Friedl D, Jacobson PC (2004) Predator-recognition training of hatchery-reared walleye (Stizostedion vitreum) and a field test of a training method using yellow perch (Perca favescens). Can J Fish Aquat Sci 61:2144–2150

White KG (2001) Forgetting functions. Anim Learn Behav 29:193–207

Wixted JT (2004) The psychology and neuroscience of forgetting. Ann Rev Psychol 55:235–269

Zhao X, Ferrari MCO, Chivers DP (2006) Threat-sensitive learning of predator odours by a prey fish. Behaviour 143:1103–1121

All items in Spectrum are protected by copyright, with all rights reserved. The use of items is governed by Spectrum's terms of access.

Repository Staff Only: item control page


Downloads per month over past year

Back to top Back to top