Environmental enrichment reduces maladaptive risk-taking behavior in salmon reared for conservation

Biological Conservation

Volumn 144, Issue 7, 2011, Pages 1972-1979

  Roberts, L J ^a   Taylor, J ^b   Garcia De Leaniz, C ^a  

^a SWANSEA UNIVERSITY   (United Kingdom)

^b ENVIRONMENT AGENCY   (United Kingdom)

Author keywords

Anti predatory behavior; Boldness; Captive breeding; Environmental enrichment; Maladaptation; Salmonid conservation

Indexed keywords

ADAPTIVE RADIATION; ANTIPREDATOR DEFENSE; BEHAVIORAL ECOLOGY; CAPTIVE BREEDING; CONSERVATION MANAGEMENT; FISHERY MANAGEMENT; HATCHING; JUVENILE; NUTRITIONAL STATUS; PERFORMANCE ASSESSMENT; PREDATOR-PREY INTERACTION; REARING; RISK FACTOR; SALMONID; SURVIVAL; WILD POPULATION;

PISCES; SALMO SALAR; SALMONIDAE;

EID: 79957634217     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2011.04.017     Document Type: Article

References (82)

1. Alberts A.C. Behavioral considerations of headstarting as a conservation strategy for endangered Caribbean rock iguanas. Applied Animal Behavioural Science 2007, 102:380-391.
2. Allan J.D., Abell R., Hogan Z., Revenga C., Taylor B.W., Welcomme R.L., Winemiller K. Overfishing of inland waters. BioScience 2005, 55:1041-1051.
3. Alvarez D., Nicieza A.G. Predator avoidance behaviour in wild and hatchery-reared brown trout: the role of experience and domestication. Journal of Fish Biology 2003, 63:1565-1577.
4. Aprahamian M.W., Martin Smith K., McGinnity P., McKelvey S., Taylor J. Restocking of salmonids - opportunities and limitations. Fisheries Research 2003, 62:211-227.
5. Araki H., Berejikian B.A., Ford M.J., Blouin M.S. Fitness of hatchery-reared salmonids in the wild. Evolutionary Applications 2008, 1:342-355.
6. Armstrong D.P., Seddon P.J. Directions in reintroduction biology. Trends in Ecology and Evolution 2007, 23:20-25.
7. Berejikian B.A., Smith R.J.F., Tezak E.P., Schroder S.L., Knudsen C.M. Chemical alarm signals and complex hatchery rearing habitats affect antipredator behavior and survival of chinook salmon (Oncorhynchus tshawytscha) juveniles. Canadian Journal of Fisheries and Aquatic Sciences 1999, 56:830-838.
8. Berejikian B.A., Tezak E.P., Riley S.C., Larae A.L. Competitive ability and social behaviour of juvenile steelhead reared in enriched and conventional hatchery tanks and a stream environment. Journal of Fish Biology 2001, 59:1600-1613.
9. Berejikian B.A., Tezak E.P., LaRae A.L. Innate and enhanced predator recognition in hatchery-reared chinook salmon. Environmental Biology of Fishes 2003, 67:241-251.
10. Bleakley B.H., Parker D.J., Brodie E.D.I. Nonadditive effects of group membership can lead to additive group phenotypes for anti-predator behaviour of guppies, Poecilia reticulata. Journal of Evolutionary Biology 2007, 20:1375-1384.
11. Blumstein D.T., Fernández-Juricic E. The emergence of conservation behavior. Conservation Biology 2004, 18:1175-1177.
12. Blumstein D.T., Mari M., Daniel J.C., Ardron J.G., Griffin A.S., Evans C.S. Olfactory predator recognition: wallabies may have to learn to be wary. Animal Conservation 2002, 5:87-93.
13. Braithwaite V.A., Salvanes A.G.V. Environmental variability in the early rearing environment generates behaviourally flexible cod: implications for rehabilitating wild populations. Proceeding of the Royal Society of London B: - Biological Sciences 2005, 272:1107-1113.
14. Bremner-Harrison S., Prodohl P.A., Elwood R.W. Behavioural trait assessment as a release criterion: boldness predicts early death in a reintroduction programme of captive-bred swift fox (Vulpes velox). Animal Conservation 2004, 7:313-320.
15. Brockmark S., Johnsson J.I. Reduced hatchery rearing density increases social dominance, postrelease growth, and survival in brown trout (Salmo trutta). Canadian Journal of Fisheries and Aquatic Sciences 2010, 67:288-295.
16. Brockmark S., Adriaenssens B., Johnsson J.I. Less is more: density influences the development of behavioural life skills in trout. Proceedings of the Royal Society of London B: Biological Sciences 2010, 277:3035-3043.
17. Brown G.E. Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish and Fisheries 2003, 4:227-234.
18. Brown C., Day R.L. The future of stock enhancements: lessons for hatchery practice from conservation biology. Fish and Fisheries 2002, 3:79-94.
19. Brown G.E., Godin J.G.J. Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish. Animal Behaviour 1999, 57:475-481.
20. Brown C., Jones F., Braithwaite V. In situ examination of boldness-shyness traits in the tropical poeciliid (Brachyraphis episcope). Animal Behaviour 2005, 70:1003-1009.
21. Budaev S.V. The statistical analysis of behavioural latency measures. ISCP Newsletter 1997, 14:1-4.
22. Chivers D.P., Smith R.J.F. Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience 1998, 5:338-352.
23. Coleman K., Wilson D.S. Shyness and boldness in pumpkinseed sunfish: individual differences are context-specific. Animal Behaviour 1998, 56:927-936.
24. Cusato M.B., Morrow M.E. Fear in the captive-bred Attwater's prairie chicken as an indicator of postrelease survival. International Journal of Comparative Psychology 2003, 16:95-110.
25. Dawkins M.S. Behaviour as a tool in the assessment of animal welfare. Zoology 2003, 106:383-387.
26. Deverill J.I., Adams C.E., Bean C.W. Prior residence, aggression and territory acquisition in hatchery-reared and wild brown trout. Journal of Fish Biology 1999, 55:868-875.
27. Ellis, T., Nash, R.D.M., 1998. Predation on wild-0-group flatfishes by released and wild turbot (Scophthalmus maximus). In: Stocking and Introduction of Fish. Fishing News Books, Oxford, pp. 319-326.
28. Farmed Animals Welfare Council (FAWC), 1996. Report on the Welfare of Farmed Fish. Surrey.
29. Fernö A., Järvi T. Domestication genetically alters the anti-predator behavior of anadromous brown trout (Salmo trutta) - a dummy predator experiment. Nordic Journal of Freshwater Research 1998, 74:95-100.
30. Ferrari M.C.O., Trowell J.J., Brown G.E., Chivers D.P. The role of learning in the development of threat-sensitive predator avoidance by fathead minnows. Animal Behaviour 2005, 70:777-784.
31. Ferrari M.C.O., Vavrek M.A., Elvidge C.K., Fridman B., Chivers D.P., Brown G.E. Sensory complementation and the acquisition of predator recognition by salmonid fishes. Behavioural Ecology and Sociobiology 2008, 63:113-121.
32. Fischer J., Lindenmayer D.B. An assessment of the published results of animal relocations. Biological Conservation 2000, 96:1-11.
33. Fleming I.A., Agustsson T., Finstad B., Johnsson J.I., Björnsson B.T. Effects of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 2002, 59:1323-1330.
34. Garner J.P. Stereotypes and other abnormal repetitive behaviours: potential impacts of validity, reliability and replicability of scientific outcomes. ILAR Journal 2005, 46:106-117.
35. Griffin A.S., Blumstein D.T., Evans C.S. Training captive-bred or translocated animals to avoid predators. Conservation Biology 2000, 14:1317-1326.
36. Griffin A.S., Evans C.S., Blumstein D.T. Learning specificity in acquired predator recognition. Animal Behaviour 2001, 62:577-589.
37. Halverson M.A. Stocking trends: a quantitative review of governmental fish stocking in the United States, 1931 to 2004. Fisheries 2009, 33:69-75.
38. Henderson J.N., Letcher B.H. Predation on stocked Atlantic salmon (Salmo salar) fry. Canadian Journal of Fisheries and Aquatic Sciences 2003, 60:32-42.
39. Hoyle I., Oidtmann B., Ellis T., Turnbull J., North B., Nikolaidis J., Knowles T.G. A validated microscopic key to assess fin damage in rainbow trout (Oncorhynchus mykiss). Aquaculture 2007, 270:142-148.
40. Huntingford F.A. Implications of domestication and rearing conditions for the behaviour of cultivated fishes. Journal of Fish Biology 2004, 65:122-142.
41. Huntingford F., Adams C. Behavioural syndromes in farmed fish: implications for production and welfare. Behaviour 2005, 142:1207-1221.
42. IUCN, 2008. IUCN Red List of Threatened Species.
43. Jepsen N., Aarestrup K., Økland F., Rasmussen G. Survival of radiotagged Atlantic salmon (Salmo salar L) and trout (Salmo trutta L) smolts passing a reservoir during seaward migration. Hydrobiologia 1998, 371:347-353.
44. Johnsson J.I., Petersson E., Jönsson E., Järvi T., Björnsson B. Growth hormone-induced effects on mortality, energy status and growth: a field study on brown trout (Salmo trutta). Functional Ecology 1999, 13:514-522.
45. Johnsson J.I., Höjesjö J., Fleming I.A. Behavioural and heart rate responses to predation risk in wild and domesticated Atlantic salmon. Canadian Journal of Fisheries and Aquatic Sciences 2001, 58:788-794.
46. Jule K., Leaver L., Lea S. The effects of captive experience on reintroduction survival in carnivores: a review and analysis. Biological Conservation 2008, 141:355-363.
47. Kekäläinen J., Niva T., Huuskonen H.P. Pike predation on hatchery-reared Atlantic salmon smolts in a northern Baltic river. Ecology of Freshwater Fish 2008, 17:100-109.
48. Kihslinger R.L., Nevitt G.A. Early rearing environment impacts cerebellar growth in juvenile salmon. Journal of Experimental Biology 2006, 209:504-509.
49. Koolhaas J.M., Korte S.M., De Boer S.F., Van Der Vegt B.J., Van Reenen C.G., Hopster H., De Jong I.C., Ruis M.A.W., Blokhuis H.J. Coping styles in animals: current status in behavior and stress-physiology. Neuroscience and Biobehavioral Reviews 1999, 23:925-935.
50. Lahti D.C., Johnson N.A., Ajie B.C., Otto S.P., Hendry A.P., Blumstein D.T., Coss R.G., Donohue K., Foster S.A. Relaxed selection in the wild. Trends Ecology and Evolution 2009, 24:487-496.
51. Lee J.S.F., Berejikian B.A. Effects of the rearing environment on average behaviour and behavioural variation in steelhead. Journal of Fish Biology 2008, 72:1736-1749.
52. Lévêque C., Oberdorff T., Paugy D., Stiassny M.L.J., Tedesco P.A. Global diversity of fish (Pisces) in freshwater. Hydrobiologia 2008, 595:545-567.
53. Lima S.L., Dill L.M. Behavioural decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 1990, 68:619-640.
54. Lymbery, P., 2002. In Too Deep - The Welfare of Intensively Farmed Fish. A Compassion in World Farming Report. In: Compassion in World Farming. Petersfield, Hampshire, pp. 1-65.
55. Maloney R.F., McLean I.G. Historical and experimental learned predator recognition in free-living New Zealand robins. Animal Behaviour 1995, 50:1193-1201.
56. Maran T., Põdra M., Põlma M., Macdonald D.W. The survival of captive-born animals in restoration programmes - case study of the endangered European mink Mustela lutreola. Biological Conservation 2009, 142:1685-1692.
57. Marchetti M.P., Nevitt G.A. Effects of hatchery rearing on brain structures of rainbow trout, Oncorhynchus mykiss. Environmental Biology of Fishes 2003, 66:9-14.
58. Mathews F., Orros M., McLaren G., Gelling M., Foster R. Keeping fit on the ark: assessing the suitability of captive-bred animals for release. Biological Conservation 2005, 121:569-577.
59. McDougall P.T., Réale D., Sol D., Reader S.M. Wildlife conservation and animal temperament: causes and consequences of evolutionary change for captive, reintroduced, and wild populations. Animal Conservation 2006, 9:39-48.
60. McLean I.G., Lundie-Jenkins G., Jarman P.J. Teaching an endangered mammal to recognize predators. Biological Conservation 1996, 75:51-62.
61. McLean I.G., Hölzer C., Studholme B.J.S. Teaching predator-recognition to a naïve bird: implications for management. Biological Conservation 1999, 87:123-130.
62. McPhee M.E. Generations in captivity increases behavioural variations: considerations for captive rearing and behavioural programmes. Biological Conservation 2003, 115:71-77.
63. Olla B.L., Davis M.W., Ryer C.H. Behavioural deficits in hatchery-reared fish: potential effects on survival following release. Aquatic Fisheries Management 1994, 25:19-34.
64. Petersson E., Järvi T. Anti-predator response in wild and sea-ranched brown trout and their crosses. Aquaculture 2006, 253:218-228.
65. Price E.O. Behavioral development in animals undergoing domestication. Applied Animal Behavioral Science 1999, 65:245-271.
66. Rikardsen A.H., Sandring S. Diet and size-selective feeding by escaped hatchery rainbow trout (Oncorhynchus mykiss) (Walbaum). ICES Journal of Marine Science 2006, 63:460-465.
67. Riley S.C., Tatara C.P., Berejikian B.A., Flagg T.A. Behavior of steelhead fry in a laboratory stream is affected by fish density but not rearing environment. North American Journal of Fisheries Management 2009, 29:1806-1818.
68. Seddon P.J., Armstrong D.P., Maloney R.F. Developing the science of reintroduction biology. Conservation Biology 2007, 21:303-312.
69. Shier D.M., Owings D.H. Effects of social learning on predator training and postrelease survival in juvenile black-tailed prairie dogs, Cynomys ludovicianus. Animal Behaviour 2006, 73:567-577.
70. Sneddon L.U. The bold and the shy: individual differences in rainbow trout. Journal of Fish Biology 2003, 62:971-975.
71. Sol D., Timmermans S., Lefebvre L. Behavioural flexibility and invasion success in birds. Animal Behaviour 2002, 63:495-502.
72. Stoinski T.S., Beck B.B. Changes in locomotor and foraging skills in captive-born, reintroduced golden lion tamarins (Leontopithecus rosalia rosalia). American Journal of Primatology 2004, 62:1-13.
73. Sundström L.F., Petersson E., Höjesjö J., Johnsson J.I., Järvi T. Hatchery selection promotes boldness in newly hatched brown trout (Salmo trutta): implications for dominance. Behavioral Ecology 2004, 15:192-198.
74. Sundström L.F., Lõhmus M., Tymchuk W.E., Devlin R.H. Gene-environment interactions influence ecological consequences of transgenic animals. Proceedings of the Natural Academy of Science USA 2007, 104:3889-3894.
75. Tatara C.P., Riley S.C., Scheurer J.A. Environmental enrichment in steelhead (Oncorhynchus mykiss) hatcheries: field evaluation of aggression, foraging, and territoriality in natural and hatchery fry. Canadian Journal of Fisheries and Aquatic Sciences 2008, 65:744-753.
76. Tatara C.P., Riley S.C., Scheurer J.A. Growth, survival, and habitat use of naturally reared and hatchery steelhead fry in streams: effects of an enriched hatchery rearing environment. Transactions of the American Fisheries Society 2009, 138:441-457.
77. Vilhunen S. Repeated antipredator conditioning: a pathway to habituation or to better avoidance?. Journal of Fish Biology 2006, 68:25-43.
78. Vilhunen S., Hirvonen H. Innate antipredatory responses of Arctic char (Salvelinus alpinus) depend on predator species and their diet. Behavioral Ecology and Sociobiology 2003, 55:1-10.
79. Vilhunen S., Hirvonen H., Laakkonen M.V.M. Less is more: social learning of predator recognition requires a low demonstrator to observer ratio in Arctic charr (Salvelinus alpinus). Behavioral Ecology and Sociobiology 2005, 57:275-282.
80. Wilson A.D.M., Stevens E.D. Consistency in context-specific measures of shyness and boldness in rainbow trout (Oncorhynchus mykiss). Ethology 2005, 111:849-862.
81. Wilson D.S., Coleman K., Clark A.B., Biederman L. Shy-bold continuum in pumpkinseed sunfish (Lepomis gibbosus): an ecological study of a psychological trait. Journal of Comparative Psychology 1993, 107:250-260.
82. Wisenden B.D. Olfactory assessment of predation risk in the aquatic environment. Philosophical Transactions of the Royal Society of London B - Biological Sciences 2000, 355:1205-1208.