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

Behavioral Ecology and Sociobiology

Volumn 65, Issue 6, 2011, Pages 1267-1276

  Brown, Grant E ^a   Ferrari, Maud C O ^c   Malka, Patrick H ^a   Oligny, Marie Anne ^a   Romano, Matthew ^a   Chivers, Douglas P ^b  

^a Dept of Electrical and Computer Engineering   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

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

Indexed keywords

ANTIPREDATOR DEFENSE; AVOIDANCE REACTION; BODY SIZE; DIET; GROWTH RATE; HYPOTHESIS TESTING; JUVENILE; LABORATORY METHOD; LEARNING; PREDATION RISK; RECOGNITION; SALMONID; TRADE-OFF;

ONCORHYNCHUS MYKISS; SALMONIDAE;

EID: 79956093748     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-011-1140-3     Document Type: Article

References (58)

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