Environmental variability in the early rearing environment generates behaviourally flexible cod: implications for rehabilitating wild populations
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The release of hatchery-reared fishes for restoring threatened and endangered populations is one of the most controversial issues in applied ecology. A central issue has been to determine whether releases cause extinction of local wild populations. This may arise either through domesticated or non-local fishes hybridizing with wild fishes, or through inappropriate behavioural interactions; for example, many hatchery fishes show exaggerated aggressive and competitive behaviour and out-compete wild counterparts. The impact of the impoverished hatchery environment in shaping behaviour is only now receiving attention. Attempts to counteract hatchery-related behavioural deficiencies have utilized intensive training programmes shortly before the fishes are released. However, we show here that simple exposure to variable spatial and foraging cues in the standard hatchery environment generates fishes with enhanced behavioural traits that are probably associated with improved survival in the wild. It appears that fishes need to experience a varying and changeable environment to learn and develop flexible behaviour. Using variable hatchery rearing environments to generate suitable phenotypes in combination with a knowledge of appropriate local genotypes, rehabilitation of wild fishes is likely to succeed, where to date it has largely failed.
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Environmental enrichment increases foraging behaviour in fish.
“Environmental enrichment | Reduces anxiety [196,197], stress [196,197], and abnormal repetitive behaviour [198–200]. Reduces susceptibility to epilepsy [201] and osteoarthritis [202] and modifies the pathology of neurological disorders [203]. Increases foraging behaviour in fish [204].”
From Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 2.0 (2020) · cites this paper as [204]
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- Allen C.B, Celikel T, Feldman D.E. Long-term depression induced by sensory deprivation during cortical map plasticity in vivo. Nat. Neurosci. 2003;6:291–299. doi: 10.1038/nn1012. [DOI] [PubMed] [Google Scholar] · DOI
- Berejikian B.A. The effects of hatchery and wild ancestry and experience on the relative ability of steelhead trout fry (Oncorhynchus mykiss) to avoid a benthic predator. Can. J. Fish. Aquat. Sci. 1995;52:2476–2482. [Google Scholar]
- Bredy T.W, Humpartzoomian R.A, Cain D.P, Meaney M.J. Partial reversal of the effect of maternal care on cognitive function through environmental enrichment. Neuroscience. 2003;118:571–576. doi: 10.1016/s0306-4522(02)00918-1. [DOI] [PubMed] [Google Scholar] · DOI
- Brown C, Laland K. Social learning and life skills training for hatchery reared fish. J. Fish Biol. 2001;59:471–493. [Google Scholar]
- Brown G.E, Smith R.J.F. 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. 1998;55:611–617. [Google Scholar]
- Brown C, Davidson T, Laland K. Environmental enrichment and prior experience improve foraging behaviour in hatchery-reared Atlantic salmon. J. Fish Biol. 2003;63(Suppl. 1):187–196. [Google Scholar]
- Dulvy N.K. Extinction vulnerability in marine populations. Fish Fish. 2003;4:25–64. [Google Scholar]
- Einum S, Fleming I.A. Genetic divergence and interactions in the wild among native, farmed and hybrid Atlantic salmon. J. Fish Biol. 1997;50:634–651. [Google Scholar]
- Ellis T, Hughes R.N, Howell B.R. Artificial dietary regime may impair subsequent foraging behaviour of hatchery-reared turbot released into natural environment. J. Fish Biol. 2002;61:252–264. [Google Scholar]
- Ersbak K, Haase B.L. Nutritional deprivation after stocking as a possible mechanism leading to mortality in stream-stocked brook trout. North Am. J. Fish. Manage. 1983;3:142–151. [Google Scholar]
- Fleming I.A, Einum S. Experimental tests of genetic divergence of farmed from wild Atlantic salmon due to domestication. ICES J. Mar. Sci. 1997;54:1051–1063. [Google Scholar]
- Godin J.-G. Evading predators. In: Godin J.-G, editor. Behavioural ecology of teleost fish. Oxford University Press; Oxford: 1997. pp. 191–236. [Google Scholar]
- Gomez-Pinilla F, So V, Kesslak J.P. Spatial learning & physical activity contribute to the induction of fibroblast growth factor: neural substrates for increased cognition associated with exercise. Neuroscience. 1998;85:53–61. doi: 10.1016/s0306-4522(97)00576-9. [DOI] [PubMed] [Google Scholar] · DOI
- Grand T.C, Grant J.W.A. Spatial predictability of resources and the ideal free distribution in convict cichlids, Cichlasoma nigrofasciatum. Anim. Behav. 1994;48:909–919. [Google Scholar]
- Hossain M.A.R, Tanaka M, Masuda R. Predator–prey interaction between hatchery-reared Japanese flounder juvenile, Paralichthys olivaceus, and sandy shore crab, Matuta lunaris: daily rhythms, anti-predator conditioning and starvation. J. Exp. Mar. Biol. Ecol. 2002;267:1–14. [Google Scholar]
- Hunter S.A, Bay M.S, Martin M.L, Hatfield J.S. Behavioural effects of environmental enrichment on harbour seals (Phoca vitulina concolor) and grey seals (Halichoerus grypus) Zool. Biol. 2002;21:375–387. [Google Scholar]
- Hutchings J.A. Collapse and recovery of marine fishes. Nature. 2000;406:882–885. doi: 10.1038/35022565. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
- Johnsson J.I, Abrahams M.V. Interbreeding with domestic strain increases foraging under threat of predation in juvenile steelhead trout (Oncorhynchus mykiss)—an experimental study. Can. J. Fish. Aquat. Sci. 1991;48:243–247. [Google Scholar]
- Kempermann G, Gast D, Gage F.H. Neuroplasticity in old age: sustained five-fold induction of hippocampal neurogenesis by long term environmental enrichment. Ann. Neurol. 2002;52:135–143. doi: 10.1002/ana.10262. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
- Krause J, Loader S.P, McDermott J, Ruxton G.D. Refuge use by fish as a function of body length-related metabolic expenditure and predation risks. Proc. R. Soc. B. 1998;265:2373–2379. [Google Scholar]
- McGinnity P, Stone C, Taggart J.B, Cooke D, Cotter D, Hynes R, McCamley C, Cross T, Ferguson A. Genetic impact of escaped farmed Atlantic salmon (Salmo salar) on native populations: use of DNA profiling to assess freshwater performance of wild, farmed, and hybrid progeny in a natural environment. ICES J. Mar. Sci. 1997;54:998–1008. [Google Scholar]
- McGinnity P, et al. Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proc. R. Soc. B. 2003;270:2443–2450. doi: 10.1098/rspb.2003.2520. doi:10.1098/rspb.2003.2520 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- McLaughlin R.L, Grant J.W.A, Kramer D.L. Individual variation and alternative patterns of foraging movements in recently emerged brook charr (Salvelinus fontinalis) Behaviour. 1992;120:286–301. [Google Scholar]
- Mirza R.S, Chivers D.P. Predator-recognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies. Can. J. Zool. 2000;78:2198–2208. [Google Scholar]
- Myers R.A, Levin S.A, Lande R, James F, Murdoch W.W, Paine R.T. Hatcheries and endangered salmon. Science. 2004;303:1980. doi: 10.1126/science.1095410. [DOI] [PubMed] [Google Scholar] · DOI
- Nordeide J.T, Fosså J.H, Salvanes A.G.V, Smedstad O.M. Testing if year-class strength of coastal cod, Gadus morhua L., can be determined at the juvenile stage. Aquat. Fish. Manage. 1994;25(Suppl. 1):101–116. [Google Scholar]
- Odling-Smee L, Braithwaite V.A. The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback. Anim. Behav. 2003;65:701–707. [Google Scholar]
- Olla B.L, Davis M.W, Ryer C.H. Behavioural deficits in hatchery-reared fish: potential effects on survival following release. Aquat. Fish. Manage. 1994;25(Suppl. 1):19–34. [Google Scholar]
- Olla B.L, Davis M.W, Ryer C.H. Understanding how the hatchery environment represses or promotes the development of behavioural survival skills. Bull. Mar. Sci. 1998;62:531–550. [Google Scholar]
- Papaj D.R. Interpopulation differences in host preference and the evolution of learning in the butterfly, Battus philenor. Evolution. 1986;40:518–530. doi: 10.1111/j.1558-5646.1986.tb00504.x. [DOI] [PubMed] [Google Scholar] · DOI
- Pauly D, Christensen V, Guénette S, Pitcher T, Sumaila U.R, Walters C.J, Watson R, Zeller D. Towards sustainability in world fisheries. Nature. 2002;418:689–695. doi: 10.1038/nature01017. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
- Pickering A.D, Pottinger T.G. Stress response and disease resistance in salmonid fish: effects of chronic elevation of plasma cortisol. Fish Physiol. Biochem. 1989;7:253–258. doi: 10.1007/BF00004714. [DOI] [PubMed] [Google Scholar] · DOI
- Rabin L.A. Maintaining behavioural diversity in captivity for conservation: natural behaviour management. Anim. Welf. 2003;12:85–94. [Google Scholar]
- Ryer C.H, Olla B.L. Growth depensation and aggression in laboratory reared coho salmon: the effect of food distribution and ration size. J. Fish Biol. 1996;48:686–694. [Google Scholar]
- Ryer C.H, Olla B.L. Altered search speed and growth: social versus independent foraging in two pelagic juvenile fishes. Mar. Ecol. Prog. Ser. 1997;153:273–281. [Google Scholar]
- Sacett G.P, Novak M.F.S.X, Kroeker R. Early experience effects on adaptive behavior: theory revisited. Ment. Retard. Dev. Disabil. Res. Rev. 1999;5:30–40. [Google Scholar]
- Salvanes A.G.V. Ocean ranching. In: Steele J, Thorpe S, Turekian K, editors. Encyclopedia of ocean sciences. Academic Press; London: 2001. pp. 1973–1982. [Google Scholar]
- Salvanes A.G.V, Nordeide J. Dominating sublittoral fish species in a west Norwegian fjord and their trophic links to cod (Gadus morhua L.) Sarsia. 1993;78:221–234. [Google Scholar]
- Siegal S, Castellan N.J. 2nd edn. McGraw-Hill Book Company; London: 1988. Nonparametric statistics for the behavioral sciences. [Google Scholar]
- Shumway C.A. A neglected science: applying behaviour to aquatic conservation. Environ. Biol. Fish. 1999;55:183–201. [Google Scholar]
- Sih A, Bell A, Chadwick Johnson J. Behavioural syndromes: an ecological and evolutionary overview. Trends Ecol. Evol. 2004;19:372–378. doi: 10.1016/j.tree.2004.04.009. [DOI] [PubMed] [Google Scholar] · DOI
- Sneddon L.U, Braithwaite V.A, Gentle M.J. Do fish have nociceptors: evidence for the evolution of a vertebrate sensory system. Proc. R. Soc. B. 2003a;270:1115–1121. doi: 10.1098/rspb.2003.2349. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
- Sneddon L.U, Braithwaite V.A, Gentle M.J. Novel object test: examining nociception and fear in the rainbow trout. J. Pain. 2003b;4:431–440. doi: 10.1067/s1526-5900(03)00717-x. [DOI] [PubMed] [Google Scholar] · DOI
- Sundstrøm L.F, Johnsson J.I.J. Experience and social environment influence the ability of young brown trout to forage on live novel prey. Anim. Behav. 2001;61:249–255. doi: 10.1006/anbe.2000.1593. [DOI] [PubMed] [Google Scholar] · DOI
- Sundstrøm L.F, Lohmus M, Johnsson J.I. Investment in territorial defence depends on rearing environment in brown trout (Salmo trutta) Behav. Ecol. Sociobiol. 2003;54:249–255. [Google Scholar]
- Sundstrøm L.F, Lohmus M, Johnsson J, Devlin R.H. Growth hormone transgenic salmon pay for growth potential with increased predation mortality. Proc. R. Soc. B. 2004;271(Suppl.):S350–S352. doi: 10.1098/rsbl.2004.0189. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- Tupper M, Boutilier R.G. Effects of habitat on settlement, growth, and postsettlement survival of Atlantic cod (Gadus morhua) Can. J. Fish. Aquat. Sci. 1995;52:1834–1841. [Google Scholar]
- Underwood A.J. Cambridge University Press; Cambridge: 1997. Experiments in ecology. [Google Scholar]
- Vilhunen S, Hirvonen H. Innate antipredator responses of Arctic char (Salvelinus alpinus) depend on predator species and their diet. Behav. Ecol. Sociobiol. 2003;55:1–10. [Google Scholar]
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Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 2.0
Percie du Sert, N., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., Dirnagl, U., Emerson, M., et al. (2020) · PLOS Biology · doi:10.1371/journal.pbio.3000411 · Cited by 2,677 · see citing works
- Authors
- Braithwaite, V. A., & Salvanes, A. G. V.
- Affiliations
- University of Edinburgh (GB)
- University of Bergen (NO)
- Corresponding author
- Braithwaite, Victoria A
- ORCID
- Salvanes, Anne G.V
- Venue
- Proceedings of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2005-06-02
- Volume
- 272
- Issue
- 1568
- Pages
- 1107-1113
- ISSN
- 0080-4649 (ISSN-L)
- 0962-8452
- 1471-2954
- PMC
- PMC1559818
- OpenAlex
- W2127207276
- Cited by
- 227
- References
- 0
- Citations by year
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- FWCI
- 6.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the Royal Society B Biological Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- NORA - Norwegian Open Research Archives (submittedVersion, other-oa)
- Funders
- Leverhulme Trust
- Norges Forskningsråd
- Topics
- Physical Sciences › Environmental Science › Nature and Landscape Conservation › Fish Ecology and Management Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Physical Sciences › Environmental Science › Nature and Landscape Conservation › Fish biology, ecology, and behavior
- Keywords
- hatchery-reared fish, cod, Gadus morhua, behavioral flexibility, environmental variability, rearing conditions, spatial cues, fish rehabilitation, hybridization, aggression, survival in the wild
- MeSH terms
- Analysis of Variance, Animals, Behavior, Animal, Conservation of Natural Resources, Environment, Escape Reaction, Exploratory Behavior, Feeding Behavior, Fishes, Social Behavior, Stress, Physiological, Aquaculture
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