Behavioral Ecology and Sociobiology

, Volume 65, Issue 6, pp 1267–1276 | Cite as

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

  • Grant E. Brown
  • Maud C. O. Ferrari
  • Patrick H. Malka
  • Marie-Anne Oligny
  • Matthew Romano
  • Douglas P. Chivers
Original Paper

Abstract

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.

Keywords

Acquired predator recognition Memory window Antipredator behaviour Salmonids Growth rate Trade-offs 

Notes

Acknowledgements

We wish to thank Drs. James Grant and Robert Weladji for comments on earlier versions of this manuscript and Matthew Murphy and Asra Toobie for assistance in the laboratory. All work reported herein was conducted in accordance with Concordia University Animal Research Ethics Protocol number AC-2008-BROW. Financial support was provided by Concordia University and the Natural Sciences and Engineering Research Council of Canada to GEB and the University of Saskatchewan and NSERC to DPC and an NSERC Postdoctoral Fellowship to MCOF.

References

  1. 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
  2. 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 200:2337–2346PubMedGoogle Scholar
  3. 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 56:830–838CrossRefGoogle Scholar
  4. Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368PubMedCrossRefGoogle Scholar
  5. Bishop TD, Brown JA (1992) Threat-sensitive foraging by larval threespine sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 31:133–138CrossRefGoogle Scholar
  6. Brown GE (2003) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish 4:227–234Google Scholar
  7. Brown C, Laland KN (2001) Social learning and life skills training for hatchery reared fish. J Fish Biol 59:471–493CrossRefGoogle Scholar
  8. Brown GE, Smith RJF (1997) Conspecific skin extracts elicit antipredator responses in juvenile rainbow trout (Oncorhynchus mykiss). Can J Zool 75:1916–1922CrossRefGoogle Scholar
  9. 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 55:611–617CrossRefGoogle Scholar
  10. 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 84:1–8CrossRefGoogle Scholar
  11. 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 63:699–706CrossRefGoogle Scholar
  12. 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 79:552–562CrossRefGoogle Scholar
  13. Brydges NM, Heathcote RJP, Braithwaite VA (2008) Habitat stability and predation pressure influence learning and memory in populations of three-spined sticklebacks. Anim Behav 75:935–942CrossRefGoogle Scholar
  14. Chivers DP, Smith RJF (1998) Chemical alarm signaling in aquatic predator-prey systems: a review and prospectus. Écoscience 5:338–352Google Scholar
  15. Cuthill IC, Kacelnik A, Krebs JR, Haccou P, Iwasa Y (1990) Starlings exploiting patches: the effect of recent experience on foraging decisions. Anim Behav 40:625–640CrossRefGoogle Scholar
  16. Darwish TL, Mirza RS, Leduc AOHC, Brown GE (2005) Acquired recognition of novel predator odour cocktails by juvenile glowlight tetras. Anim Behav 70:83–89CrossRefGoogle Scholar
  17. 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 20:1096–1105CrossRefGoogle Scholar
  18. 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 144:889–906CrossRefGoogle Scholar
  19. Feary DA, McCormick MI, Jones GP (2009) Growth of reef fishes in response to live coral cover. J Exp Mar Biol Ecol 373:45–49CrossRefGoogle Scholar
  20. Ferrari MCO, Chivers DP (2006) Learning threat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information? Anim Behav 71:19–26CrossRefGoogle Scholar
  21. 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 70:777–784CrossRefGoogle Scholar
  22. Ferrari MCO, Sih A, Chivers DP (2009) The paradox of risk allocation: a review and prospectus. Anim Behav 78:579–585CrossRefGoogle Scholar
  23. 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 277:2205–2210CrossRefGoogle Scholar
  24. 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 93:560–569PubMedCrossRefGoogle Scholar
  25. 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 12:745–750PubMedCrossRefGoogle Scholar
  26. 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 64:1117–1123CrossRefGoogle Scholar
  27. Grubb TC Jr, Pravosudov VV (1994) Toward a general theory of energy management in wintering birds. J Avian Biol 25:255–260CrossRefGoogle Scholar
  28. Griffin AS (2004) Social learning about predators: a review and prospectus. Learn Behav 32:131–140PubMedCrossRefGoogle Scholar
  29. 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 14:291–293CrossRefGoogle Scholar
  30. Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58CrossRefGoogle Scholar
  31. Hirvonen H, Ranta E, Rita H, Peuhkuri N (1999) Significance of memory properties in prey choice decisions. Ecol Model 115:177–189CrossRefGoogle Scholar
  32. 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 62:235–254PubMedCrossRefGoogle Scholar
  33. Kerr B, Feldman MW (2003) Carving the cognitive niche: optimal learning strategies in homogeneous and heterogeneous environments. J Theor Biol 220:169–188PubMedCrossRefGoogle Scholar
  34. Kotler BP (1992) Behavioural resource depression and decaying perceived risk of predation in two species of coexisting gerbils. Behav Ecol Sociobiol 30:239–244CrossRefGoogle Scholar
  35. Kraemer PJ, Golding JM (1997) Adaptive forgetting in animals. Psych Bull Rev 4:480–491CrossRefGoogle Scholar
  36. 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 60:1223–1230CrossRefGoogle Scholar
  37. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  38. 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 166–188Google Scholar
  39. Mackney PA, Hughes RN (1995) Foraging behaviour and memory window in sticklebacks. Behaviour 132:1241–1253CrossRefGoogle Scholar
  40. Mangel M (1990) Dynamic information in uncertain and changing worlds. J Theor Biol 146:317–332PubMedCrossRefGoogle Scholar
  41. Martel G, Dill LM (1993) Feeding and aggressive behaviours in juvenile coho salmon (Oncorhynchus kisutch) under chemically-mediated risk of predation. Behav Ecol Sociobiol 32:365–370CrossRefGoogle Scholar
  42. McNamara JM, Houston AI (1987) Memory and the efficient use of information. J Theor Biol 125:385–395PubMedCrossRefGoogle Scholar
  43. Mirza RS, Chivers DP (2000) Predator-recognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies. Can J Zool 78:2198–2208CrossRefGoogle Scholar
  44. Nilsson PA, Brönmark C (2000) Prey vulnerability to a gape-limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88:539–546CrossRefGoogle Scholar
  45. 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 268:363–368CrossRefGoogle Scholar
  46. 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 116:515–522PubMedCrossRefGoogle Scholar
  47. Reinhardt UG, Healey MC (1999) Season- and size-dependent risk taking in juvenile coho salmon: experimental evaluation of asset protection. Anim Behav 57:923–933PubMedCrossRefGoogle Scholar
  48. Roitberg BD, Zimmermann K, Hoffmeister TS (2010) Dynamic response to danger in a parasitoid wasp. Behav Ecol Sociobiol 64:627–637CrossRefGoogle Scholar
  49. Shettleworth SJ, Plowright CMS (1992) How pigeons estimate rates of prey encounter. J Exp Psych: Anim Behav Proc 18:219–235CrossRefGoogle Scholar
  50. 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 73:567–577CrossRefGoogle Scholar
  51. Skow CD, Jakob EM (2006) Jumping spiders attend to context during learned avoidance of aposematic prey. Behav Ecol 17:34–40CrossRefGoogle Scholar
  52. Speed MP (2000) Warning signals, receiver psychology and predator memory. Anim Behav 60:269–278PubMedCrossRefGoogle Scholar
  53. 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 18:255–261CrossRefGoogle Scholar
  54. Werner EE, Gilliam JF, Hall DJ, Mittlebach GG (1983) An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540–1548CrossRefGoogle Scholar
  55. 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 61:2144–2150CrossRefGoogle Scholar
  56. White KG (2001) Forgetting functions. Anim Learn Behav 29:193–207CrossRefGoogle Scholar
  57. Wixted JT (2004) The psychology and neuroscience of forgetting. Ann Rev Psychol 55:235–269CrossRefGoogle Scholar
  58. Zhao X, Ferrari MCO, Chivers DP (2006) Threat-sensitive learning of predator odours by a prey fish. Behaviour 143:1103–1121CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Grant E. Brown
    • 1
  • Maud C. O. Ferrari
    • 3
  • Patrick H. Malka
    • 1
  • Marie-Anne Oligny
    • 1
  • Matthew Romano
    • 1
  • Douglas P. Chivers
    • 2
  1. 1.Department of BiologyConcordia UniversityMontrealCanada
  2. 2.Department of BiologyUniversity of SaskatchewanSaskatoonCanada
  3. 3.Department of Environmental Science and PolicyUniversity of California, DavisDavisUSA

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