Environmental Biology of Fishes

, Volume 101, Issue 3, pp 383–401 | Cite as

Rearing environment influences boldness and prey acquisition behavior, and brain and lens development of bull trout

  • William R. Brignon
  • Martin M. Pike
  • Lars O. E. Ebbesson
  • Howard A. Schaller
  • James T. Peterson
  • Carl B. Schreck


Animals reared in barren captive environments exhibit different developmental trajectories and behaviors than wild counterparts. Hence, the captive phenotypes may influence the success of reintroduction and recovery programs for threatened and endangered species. We collected wild bull trout embryos from the Metolius River Basin, Oregon and reared them in differing environments to better understand how captivity affects the bull trout Salvelinus confluentus phenotype. We compared the boldness and prey acquisition behaviors and development of the brain and eye lens of bull trout reared in conventional barren and more structurally complex captive environments with that of wild fish. Wild fish and captive reared fish from complex habitats exhibited a greater level of boldness and prey acquisition ability, than fish reared in conventional captive environments. In addition, the eye lens of conventionally reared bull trout was larger than complex reared captive fish or same age wild fish. Interestingly, we detected wild fish had a smaller relative cerebellum than either captive reared treatment. Our results suggest that rearing fish in more complex captive environments can create a more wild-like phenotype than conventional rearing practices. A better understanding of the effects of captivity on the development and behavior of bull trout can inform rearing and reintroduction programs though prediction of the performance of released individuals.


Boldness behavior Behavioral development Behavioral plasticity Brain development Eye development Species conservation Species recovery Bull trout 



The authors declare no conflict of interest. We would like to thank Dr. Jeffrey Jolley, Greg Silver, Dr. Kari Dammerman, Dr. Robert Mason, Dr. Jason Dunham, and Dr. Jacob Raber for thoughtful reviews of the manuscript. Dr. Matt Mesa provided productive discussion on study design. Rob Chitwood, Olivia Hakanson, and Rachel Palmer provided animal husbandry. References to trade names do not imply endorsement by the U.S. Government. The findings and conclusions in this manuscript are those of the author and do not necessarily represent the views of the U.S. Fish and Wildlife Service.


  1. Araki H, Berejikian BA, Ford MJ, Blouin MS (2008) Fitness of hatchery-reared salmonids in the wild. Evol Appl 1(2):342–355. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Armstrong JB, Bond MH (2013) Phenotype flexibility in wild fish: Dolly Varden regulate assimilative capacity to capitalize on annual pulsed subsidies. J Anim Ecol 82(5):966–975. CrossRefPubMedGoogle Scholar
  3. Baumgartner JV, Bell MA, Weinberg PH (1988) Body form differences between the Enos Lake species pair of threespine sticklebacks (Gasterosteus aculeatus complex). Can J Zool 66(2):467–474. CrossRefGoogle Scholar
  4. Berejikian BA, Tezak EP, Flagg TA, LaRae AL, Kummerow E, Mahnken CV (2000) Social dominance, growth, and habitat use of age-0 steelhead (Oncorhynchus mykiss) grown in enriched and conventional hatchery rearing environments. Can J Fish Aquat Sci 57(3):628–636. CrossRefGoogle Scholar
  5. Berejikian BA, Tezak EP, Riley SC, LaRae AL (2001) Competitive ability and social behaviour of juvenile steelhead reared in enriched and conventional hatchery tanks and a stream environment. J Fish Biol 59(6):1600–1613. CrossRefGoogle Scholar
  6. Berejikian BA, Gable J, Vidergar D (2011) Effectiveness and trade-offs associated with hydraulic egg collections from natural salmon and steelhead redds for conservation hatchery programs. Trans Am Fish Soc 140(3):549–556. CrossRefGoogle Scholar
  7. Bowmaker JK (2011) Photoreceptors and visual pigments. In: Farrell AP, Stevens ED, Cech JJ, Richards JG (eds) Encyclopedia of fish physiology: from genome to environment. Academic Press, Maryland Heights, pp 110–130. CrossRefGoogle Scholar
  8. Broglio C, Rodríguez F, Salas C (2003) Spatial cognition and its neural basis in teleost fishes. Fish Fish 4(3):247–255. CrossRefGoogle Scholar
  9. Broglio C, Gómez A, Durán E, Salas C, Rodríguez F (2011) Brain and cognition in teleost fish. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior. Wiley-Blackwell, New York, pp 325–358. CrossRefGoogle Scholar
  10. Brown C, Braithwaite VA (2004) Size matters: a test of boldness in eight populations of the poeciliid Brachyraphis episcopi. Anim Behav 68(6):1325–1329. CrossRefGoogle Scholar
  11. Brown C, Day RL (2002) The future of stock enhancements: lessons for hatchery practice from conservation biology. Fish Fish 3(2):79–94. CrossRefGoogle Scholar
  12. Brown C, Davidson T, Laland K (2003) Environmental enrichment and prior experience of live prey improve foraging behaviour in hatchery-reared Atlantic salmon. J Fish Biol 63(s1):187–196. CrossRefGoogle Scholar
  13. Brown C, Burgess F, Braithwaite VA (2007) Heritable and experiential effects on boldness in a tropical poeciliid. Behav Ecol Sociobiol 62(2):237–243. CrossRefGoogle Scholar
  14. Brown AD, Sisneros JA, Jurasin T, Nguyen C, Coffin AB (2013) Differences in lateral line morphology between hatchery-and wild-origin steelhead. PLoS One 8(3):e59162. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New YorkGoogle Scholar
  16. Burns JG, Rodd FH (2008) Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task. Anim Behav 76(3):911–922. CrossRefGoogle Scholar
  17. Burns G, Saravanan A, Rodd FH (2009) Rearing environment affects the brain size of guppies: lab-reared guppies have smaller brains than wild-caught guppies. Ethology 115(2):122–133. CrossRefGoogle Scholar
  18. Cochran-Biederman JL, Wyman KE, French WE, Loppnow GL (2015) Identifying correlates of success and failure of native freshwater fish reintroductions. Conserv Biol 29(1):175–186. CrossRefPubMedGoogle Scholar
  19. Conroy MJ, Peterson JT (2013) Decision making in natural resource management: a structured, adaptive approach. Wiley-Blackwell, New York. CrossRefGoogle Scholar
  20. Currens KP, Sharpe CS, Hjort R, Schreck CB, Li HW (1989) Effects of different feeding regimes on the morphometrics of Chinook salmon (Oncorhynchus tshawytscha) and rainbow trout (O. mykiss). Copeia 3:689–695CrossRefGoogle Scholar
  21. Davis RE, Northcutt RG (1983) Fish Neurobiology, Vol 1 and 2. University of Michigan Press, Ann ArborGoogle Scholar
  22. Devlin RH, Vandersteen WE, Uh M, Stevens ED (2012) Genetically modified growth affects allometry of eye and brain in salmonids. Can J Zool 90(2):193–202. CrossRefGoogle Scholar
  23. Dickens MJ, Delehanty DJ, Romero LM (2010) Stress: an inevitable component of animal translocation. Biol Conserv 143(6):1329–1341. CrossRefGoogle Scholar
  24. Ebbesson LOE, Braithwaite VA (2012) Environmental effects on fish neural plasticity and cognition. J Fish Biol 81(7):2151–2174. CrossRefPubMedGoogle Scholar
  25. Fernald RD (2015) Social behaviour: can it change the brain? Anim Behav 103:259–265. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Fernö A, Huse G, Jakobsen PJ, Kristiansen TS, Nilsson J (2011) Fish behaviour, learning, aquaculture and fisheries. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior. Wiley-Blackwell, New York, pp 359–404. CrossRefGoogle Scholar
  27. Gonda A, Välimäki K, Herczeg G, Merilä J (2012) Brain development and predation: plastic responses depend on evolutionary history. Biol Lett 8(2):249–252. CrossRefPubMedGoogle Scholar
  28. Hairston NG, Li KT, Easter SS (1982) Fish vision and the detection of planktonic prey. Science 218(4578):1240–1242. CrossRefPubMedGoogle Scholar
  29. Hargis WJ (1991) Disorders of the eye in finfish. Annu Rev Fish Dis 1:95–117. CrossRefGoogle Scholar
  30. Healy SD, Rowe C (2007) A critique of comparative studies of brain size. Proc R Soc B Biol Sci 274(1609):453–464. CrossRefGoogle Scholar
  31. Hosmer DW, Lemeshow S (2000) Applied logistic regression. Wiley Interscience, New York. CrossRefGoogle Scholar
  32. Jeffery WR (2001) Cavefish as a model system in evolutionary developmental biology. Dev Biol 231(1):1–12. CrossRefPubMedGoogle Scholar
  33. Jonsson B, Jonsson N (2014) Early environment influences later performance in fishes. J Fish Biol 85(2):151–188. CrossRefPubMedGoogle Scholar
  34. Kihslinger RL, Nevitt GA (2006) Early rearing environment impacts cerebellar growth in juvenile salmon. J Exp Biol 209(3):504–509. CrossRefPubMedGoogle Scholar
  35. Kihslinger RL, Lema SC, Nevitt GA (2006) Environmental rearing conditions produce forebrain differences in wild Chinook salmon Oncorhynchus tshawytscha. Comp Biochem Physiol-Part A: Mol Integr Physiol 145(2):145–151. CrossRefGoogle Scholar
  36. Kleiman DG (1996) Reintroduction programs. In: Kleiman DG, Allen M, Thompson K, Lumpkin S, Harris H (eds) Wild mammalian captivity: principles and techniques. University of Chicago Press, Chicago, pp 297–305Google Scholar
  37. Kröger RHH (2011) Physiological optics in fishes. In: Farrell AP, Stevens ED, Cech JJ, Richards JG (eds) Encyclopedia of fish physiology: from genome to environment. Academic Press, Maryland Heights, pp 102–109. CrossRefGoogle Scholar
  38. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68(4):619–640. CrossRefGoogle Scholar
  39. López JC, Broglio C, Rodríguez F, Thinus-Blanc C, Salas C (2000) Reversal learning deficit in a spatial task but not in a cued one after telencephalic ablation in goldfish. Behav Brain Res 109(1):91–98. CrossRefPubMedGoogle Scholar
  40. Lorenzen K (2014) Understanding and managing enhancements: why fisheries scientists should care. J Fish Biol 85(6):1807–1829. CrossRefPubMedGoogle Scholar
  41. Lorenzen K, Beveridge M, Mangel M (2012) Cultured fish: integrative biology and management of domestication and interactions with wild fish. Biol Rev 87(3):639–660. CrossRefPubMedGoogle Scholar
  42. Marchetti MP, Nevitt GA (2003) Effects of hatchery rearing on brain structures of rainbow trout, Oncorhynchus mykiss. Environ Biol Fish 66(1):9–14. CrossRefGoogle Scholar
  43. MBTSG (Montana Bull Trout Scientific Group) (1996) The role of stocking in bull trout recovery. Montana Bull Trout Restoration Team, HelenaGoogle Scholar
  44. McNeil WJ (1964) A method of measuring mortality of pink salmon eggs and larvae. Fish Bull 63:575–588Google Scholar
  45. McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): morphological and genetic evidence for a species pair in Enos Lake, British Columbia. Can J Zool 62(7):1402–1408. CrossRefGoogle Scholar
  46. Metcalfe NB, Taylor AC, Thorpe JE (1995) Metabolic rate, social status and life-history strategies in Atlantic salmon. Anim Behav 49(2):431–436. CrossRefGoogle Scholar
  47. Metcalfe NB, Valdimarsson SK, Morgan IJ (2003) The relative roles of domestication, rearing environment, prior residence and body size in deciding territorial contests between hatchery and wild juvenile salmon. J Appl Ecol 40(3):535–544. CrossRefGoogle Scholar
  48. Näslund J, Johnsson JI (2016) Environmental enrichment for fish in captive environments: effects of physical structures and substrates. Fish Fish 17(1):1–30. CrossRefGoogle Scholar
  49. Näslund J, Aarestrup K, Thomassen ST, Johnsson JI (2012) Early enrichment effects on brain development in hatchery-reared Atlantic salmon (Salmo salar): no evidence for a critical period. Can J Fish Aquat Sci 69(9):1481–1490. CrossRefGoogle Scholar
  50. Näslund J, Rosengren M, Del Villar D, Gansel L, Norrgård JR, Persson L, Winkowski JJ, Kvingedal E (2013) Hatchery tank enrichment affects cortisol and shelter-seeking in Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 70(4):585–590. CrossRefGoogle Scholar
  51. Northmore D (2011) Optic tectum. In: Farrell AP, Stevens ED, Cech JJ, Richards JG (eds) Encyclopedia of fish physiology: from genome to environment. Academic Press, Maryland Heights, pp 131–142. CrossRefGoogle Scholar
  52. Olla BL, Davis MW (1989) The role of learning and stress in predator avoidance of hatchery-reared Coho salmon (Oncorhynchus kisutch) juveniles. Aquaculture 76(3-4):209–214. CrossRefGoogle Scholar
  53. Olla BL, Davis MW, Ryer CH (1998) Understanding how the hatchery environment represses or promotes the development of behavioural survival skills. Bull Mar Sci 62:531–550Google Scholar
  54. Pakkasmaa S, Ranta E, Piironen J (1998) A morphometric study on four land-locked salmonid species. Ann Zool Fenn 35:131–140Google Scholar
  55. Pankhurst NW, Montgomery JC (1994) Uncoupling of visual and somatic growth in the rainbow trout Oncorhynchus mykiss. Brain Behav Evol 44(3):149–155. CrossRefPubMedGoogle Scholar
  56. Park PJ, Chase I, Bell MA (2012) Phenotypic plasticity of the threespine stickleback Gasterosteus aculeatus telencephalon in response to experience in captivity. Current Zoology 58(1):189–210. CrossRefGoogle Scholar
  57. Rodríguez F, López CJ, Vargas JP, Gómez Y, Broglio C, Salas C (2002) Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. J Neurosci 22(7):2894–2903PubMedGoogle Scholar
  58. Rodríguez F, Durán E, Gómez A, Ocaña FM, Álvarez E, Jiménez-Moya F, Broglio C, Salas C (2005) Cognitive and emotional functions of the teleost fish cerebellum. Brain Res Bull 66(4-6):365–370. CrossRefPubMedGoogle Scholar
  59. Rosset A, Spadola L, Ratib O (2004) OsiriX: an open-source software for navigating in multidimensional DICOM images. J Digit Imaging 17(3):205–216. CrossRefPubMedPubMedCentralGoogle Scholar
  60. Salvanes AG, Moberg O, Ebbesson LO, Nilsen TO, Jensen KH, Braithwaite VA (2013) Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proc R Soc B 280:3113CrossRefGoogle Scholar
  61. Shively D, Allen C, Alsbury T, Bergamini B, Goehring B, Horning T, and Strobel B. 2007. Clackamas River Bull Trout Reintroduction Feasibility Assessment. Published by USDA Forest Service, Mt. Hood National Forest; U.S. Fish and Wildlife Service, Oregon State Office; and Oregon Department of Fish and Wildlife, North Willamette RegionGoogle Scholar
  62. Simões JM, Teles MC, Oliveira RF, Van der Linden A, Verhoye M (2012) A three-dimensional stereotaxic MRI brain atlas of the cichlid fish Oreochromis mossambicus. PLoS One 7(9):e44086. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Sinn DL, Gosling SD, Moltschaniwskyj NA (2008) Development of shy/bold behaviour in squid: context-specific phenotypes associated with developmental plasticity. Anim Behav 75(2):433–442. CrossRefGoogle Scholar
  64. Soares D, Yamamoto Y, Strickler AG, Jeffery WR (2004) The lens has a specific influence on optic nerve and tectum development in the blind cavefish Astyanax. Dev Neurosci 26(5-6):308–317. CrossRefPubMedGoogle Scholar
  65. Sundström LF, Johnsson JI (2001) Experience and social environment influence the ability of young brown trout to forage on live novel prey. Anim Behav 61(1):249–255. CrossRefPubMedGoogle Scholar
  66. Sundström LF, Petersson E, Höjesjö J, Johnsson JI, Järvi T (2004) Hatchery selection promotes boldness in newly hatched brown trout (Salmo trutta): implications for dominance. Behav Ecol 15(2):192–198. CrossRefGoogle Scholar
  67. Taylor EB (1986) Differences in morphology between wild and hatchery populations of juvenile Coho salmon. Prog Fish Cult 48(3):171–176.<171:DIMBWA>2.0.CO;2 CrossRefGoogle Scholar
  68. Teletchea F (2017) Wildlife conservation: is domestication a solution?. Global exposition of wildlife management. InTechGoogle Scholar
  69. Thompson WL, Lee DC (2000) Modeling relationships between landscape-level attributes and snorkel counts of Chinook salmon and steelhead parr in Idaho. Can J Fish Aquat Sci 57(9):1834–1842. CrossRefGoogle Scholar
  70. Tiffan KF, Connor WP (2011) Distinguishing between natural and hatchery Snake River fall Chinook Salmon subyearlings in the field using body morphology. Trans Am Fish Soc 140:21–30Google Scholar
  71. Ullmann JF, Cowin G, Kurniawan ND, Collin SP (2010) A three-dimensional digital atlas of the zebrafish brain. NeuroImage 51(1):76–82. CrossRefPubMedGoogle Scholar
  72. USFWS (U.S. Fish and Wildlife Service). (2015) Recovery plan for the coterminous United States population of bull trout (Salvelinus confluentus). PortlandGoogle Scholar
  73. Wall GL (1963) The vertebrate eye and its adaptive radiation. Haffner Publishing, New YorkGoogle Scholar
  74. Weigel DE, Peterson JT, Spruell P (2003) Introgressive hybridization between native cutthroat trout and introduced rainbow trout. Ecol Appl 13(1):38–50.[0038:IHBNCT]2.0.CO;2 CrossRefGoogle Scholar
  75. West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20(1):249–278. CrossRefGoogle Scholar
  76. Williams DA (1982) Extra-binomial variation in logistic linear models. Appl Stat 31(2):144–148. CrossRefGoogle Scholar
  77. Wilson ADM, McLaughlin RL (2010) Foraging behaviour and brain morphology in recently emerged brook charr, Salvelinus fontinalis. Behav Ecol Sociobiol 64(11):1905–1914. CrossRefGoogle Scholar
  78. Woodward CC, Strange RL (1987) Physiological stress responses in wild and hatchery-reared rainbow trout. Trans Am Fish Soc 116(4):574–579.<574:PSRIWA>2.0.CO;2 CrossRefGoogle Scholar
  79. Zupanc G (2006) Neurogenesis and neuronal regeneration in the adult fish brain. J Comp Physiol A 192(6):649–670. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  • William R. Brignon
    • 1
    • 2
  • Martin M. Pike
    • 3
  • Lars O. E. Ebbesson
    • 4
  • Howard A. Schaller
    • 5
  • James T. Peterson
    • 2
  • Carl B. Schreck
    • 2
  1. 1.Columbia River Fisheries Program OfficeUnited States Fish and Wildlife ServiceVancouverUSA
  2. 2.U.S. Geological Survey, Oregon Cooperative Fish and Wildlife Research Unit, U.S.G.S.Oregon State UniversityCorvallisUSA
  3. 3.Advanced Imaging Research CenterOregon Health and Science UniversityPortlandUSA
  4. 4.Uni Research EnvironmentUniversity of BergenBergenNorway
  5. 5.Fish and Aquatic Conservation ProgramUnited States Fish and Wildlife ServicePortlandUSA

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