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Does maternal captivity of wild, migratory sockeye salmon influence offspring performance?

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Abstract

The environment females experience during sexual maturation can have cascading effects on offspring. For free-swimming populations of wild fish, ecological factors including predation and competition are known to alter offspring phenotype. For wild-caught fish targeted for stock enhancement, logistical factors, such as the widespread practice of holding fish in captivity/confinement, also have the potential to modify offspring phenotype. Understanding how maternal captivity affects offspring, in comparison to offspring reared from fish that have matured in the wild, is an important but relatively understudied aspect of fish culture. We examined egg and offspring traits for wild-caught female sockeye salmon reared in captivity during the final stages of sexual maturation or captured on spawning grounds following in-river maturation. Compared to females that matured in-river, captive females had smaller eggs and offspring in poorer body condition. These same offspring did however swim for longer durations. These results suggest that maternal captivity prior to spawning elicits intergenerational phenotypic change. Whether captivity-induced maternal effects are maladaptive/reduce offspring fitness will be dependent upon the environment in which offspring are being released into (e.g. captive or wild). Intergenerational effects of short-term captivity of wild fish may be a contributing mechanism mediating the success of fisheries supplementation programmes.

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References

  • Alvarez, D. & A. G. Nicieza, 2003. Predator avoidance behaviour in wild and hatchery-reared brown trout: the role of experience and domestication. Journal of Fish Biology 63: 1565–1577.

    Article  Google Scholar 

  • Baker, M. R., K. S. Gobush & C. H. Vynne, 2013. Review of factors influencing stress hormones in fish and wildlife. Journal for Nature Conservation 21: 309–318.

    Article  Google Scholar 

  • Braun, D. C., D. A. Patterson & J. D. Reynolds, 2013. Maternal and environmental influences on egg size and juvenile life-history traits in Pacific salmon. Ecology and Evolution 3: 1727–1740.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradford, M. J., J. Lovy, D. A. Patterson, D. J. Speare, W. R. Bennett, A. R. Stobbart & C. P. Tovey, 2010. Parvicapsula minibicornis infections in gill and kidney and the premature mortality of adult sockeye salmon (Oncorhynchus nerka) from Cultus Lake, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 67: 673–683.

    Article  Google Scholar 

  • Brett, J. R., 1964. The respiratory metabolism and swimming performance of young sockeye salmon. Journal of the Fisheries Board of Canada 21: 1183–1226.

    Article  Google Scholar 

  • Brooks, S., C. R. Tyler & J. P. Sumpter, 1997. Egg quality in fish: what makes a good egg? Reviews in Fish Biology and Fisheries 7: 387–416.

    Article  Google Scholar 

  • Campbell, P. M., T. G. Pottinger & J. P. Sumpter, 1994. Preliminary evidence that chronic confinement stress reduces the quality of gametes produced by brown and rainbow trout. Aquaculture 120: 151–169.

    Article  Google Scholar 

  • Christie, M. R., M. L. Marine, R. A. French & M. S. Blouin, 2012. Genetic adaptation to captivity can occur in a single generation. Proceedings of the National Academy of Sciences 109: 238–242.

    Article  CAS  Google Scholar 

  • Clearwater, S. J. & N. W. Pankhurst, 1997. The response to capture and confinement stress of plasma cortisol, plasma sex steroids and vitellogenic oocytes in the marine teleost, red gurnard. Journal of Fish Biology 50: 429–441.

    Article  CAS  Google Scholar 

  • Crossin, G. T., S. G. Hinch, A. P. Farrell, D. A. Higgs, A. G. Lotto, J. D. Oakes & M. C. Healey, 2004. Energetics and morphology of sockeye salmon: effects of upriver migratory distance and elevation. Journal of Fish Biology 65: 788–810.

    Article  Google Scholar 

  • Fisheries and Oceans Canada. 2015. Evaluation of the Salmonid Enhancement Program. Final Report March 2015 6B167. http://www.dfo-mpo.gc.ca/ae-ve/evaluations/13-14/6B167-Evaluation_Salmonid_Enhancement_Program_Mar2015-eng.html [Accessed February 12, 2016].

  • Dunn, G. A., C. P. Morgan & T. L. Bale, 2011. Sex-specificity in transgenerational epigenetic programming. Hormones and Behavior 59: 290–295.

    Article  PubMed  Google Scholar 

  • de Jesus, E. G. T. & T. Hirano, 1992. Changes in whole body concentrations of cortisol, thyroid hormones, and sex steroids during early development of the chum salmon, Oncorhynchus keta. General and Comparative Endocrinology 85: 55–61.

    Article  PubMed  Google Scholar 

  • Eaton, L., E. J. Edmonds, T. B. Henry, D. L. Snellgrove & K. A. Sloman, 2015. Mild maternal stress disrupts associative learning and increases aggression in offspring. Hormones and behavior 71: 10–15.

    Article  CAS  PubMed  Google Scholar 

  • Ellis, T., R. N. Hughes & B. R. Howell, 2002. Artificial dietary regime may impair subsequent foraging behaviour of hatchery-reared turbot released into the natural environment. Journal of Fish Biology 61: 252–264.

    Article  Google Scholar 

  • Faleiro, F. & L. Narciso, 2013. The disadvantages of mating outside home: how breeding in captivity affects the reproductive success of seahorses? Journal of Sea Research 78: 85–90.

    Article  Google Scholar 

  • Groot, C. & L. Margolis, 1991. Pacific Salmon Life Histories. UBC Press, Vancouver.

    Google Scholar 

  • Hilborn, R. & J. Winton, 1993. Learning to enhance salmon production: lessons from the Salmonid Enhancement Program. Canadian Journal of Fisheries and Aquatic Sciences 50: 2043–2056.

    Article  Google Scholar 

  • Johnsson, J. I., S. Brockmark & J. Näslund, 2014. Environmental effects on behavioural development consequences for fitness of captive-reared fishes in the wild. Journal of Fish Biology 85: 1946–1971.

    Article  CAS  PubMed  Google Scholar 

  • Keeley, E. R. & J. W. Grant, 2001. Prey size of salmonid fishes in streams, lakes, and oceans. Canadian Journal of Fisheries and Aquatic Sciences 58: 1122–1132.

    Article  Google Scholar 

  • Lambert, Y. & A. Thorsen, 2003. Integration of captive and wild studies to estimate egg and larval production of fish stocks. Journal of Northwest Atlantic Fisheries Science 33: 71–79.

    Article  Google Scholar 

  • Li, M. & J. F. Leatherland, 2013. The implications for aquaculture practice of epigenomic programming of components of the endocrine system of teleostean embryos: lessons learned from mammalian studies. Fish and Fisheries 14: 528–553.

    Article  Google Scholar 

  • Lindqvist, C., A. M. Janczak, D. Nätt, I. Baranowska, N. Lindqvist, A. Wichman, J. Lundeberg, J. Lindberg, P. A. Torjesen & P. Jensen, 2007. Transmission of stress-induced learning impairment and associated brain gene expression from parents to offspring in chickens. PLoS ONE 2: e364.

    Article  PubMed  PubMed Central  Google Scholar 

  • Love, O. P. & T. D. Williams, 2008. The adaptive value of stress-induced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness. The American Naturalist 172: E135–E149.

    Article  PubMed  Google Scholar 

  • Ma, H., G. M. Weber, M. A. Hostuttler, H. Wei, L. Wang & J. Yao, 2015. MicroRNA expression profiles from eggs of different qualities associated with post-ovulatory ageing in rainbow trout (Oncorhynchus mykiss). BMC Genomics 16: 1.

    Article  Google Scholar 

  • Mandelman, J. W. & M. A. Farrington, 2007. The physiological status and mortality associated with otter-trawl capture, transport, and captivity of an exploited elasmobranch, Squalus acanthias. ICES Journal of Marine Science 64: 122–130.

    CAS  Google Scholar 

  • Marçalo, A., P. Pousão-Ferreira, L. Mateus, J. H. Duarte Correia & Y. Stratoudakis, 2008. Sardine early survival, physical condition and stress after introduction to captivity. Journal of Fish Biology 72: 103–120.

    Article  Google Scholar 

  • McCormick, M. I., 2006. Mothers matter: crowding leads to stressed mothers and smaller offspring in marine fish. Ecology 87: 1104–1109.

    Article  PubMed  Google Scholar 

  • McGhee, K. E., L. M. Pintor, E. L. Suhr & A. M. Bell, 2012. Maternal exposure to predation risk decreases offspring antipredator behaviour and survival in threespined stickleback. Functional Ecology 26: 932–940.

    Article  PubMed  PubMed Central  Google Scholar 

  • Meylan, S., D. B. Miles & J. Clobert, 2012. Hormonally mediated maternal effects, individual strategy and global change. Philosophical Transactions of the Royal Society B: Biological Sciences 367: 1647–1664.

    Article  Google Scholar 

  • Molony, B. W., R. Lenanton, G. Jackson & J. Norriss, 2003. Stock enhancement as a fisheries management tool. Reviews in Fish Biology and Fisheries 13: 409–432.

    Article  Google Scholar 

  • Mommer, B. C. & A. M. Bell, 2014. Maternal experience with predation risk influences genome-wide embryonic gene expression in threespined sticklebacks (Gasterosteus aculeatus). PLoS ONE 9: e98564.

    Article  PubMed  PubMed Central  Google Scholar 

  • Murchie, K. J., S. E. Danylchuk, C. E. Pullen, E. Brooks, A. D. Shultz, C. D. Suski, A. J. Danylchuk & S. J. Cooke, 2009. Strategies for the capture and transport of bonefish, Albula vulpes, from tidal creeks to a marine research laboratory for long-term holding. Aquaculture Research 40: 1538–1550.

    Article  Google Scholar 

  • Naish, K. A., J. E. Taylor, P. S. Levin, T. P. Quinn, J. R. Winton, D. Huppert & R. Hilborn, 2007. An evaluation of the effects of conservation and fishery enhancement hatcheries on wild populations of salmon. Advances in Marine Biology 53: 61–194.

    Article  PubMed  Google Scholar 

  • Pankhurst, N. W. & D. F. Sharples, 1992. Effects of capture and confinement on plasma cortisol concentrations in the snapper, Pagrus auratus. Marine and Freshwater Research 43: 345–355.

    Article  CAS  Google Scholar 

  • Patterson, D. A., J. S. Macdonald, S. G. Hinch, M. C. Healey & A. P. Farrell, 2004a. The effect of exercise and captivity on energy partitioning, reproductive maturation and fertilization success in adult sockeye salmon. Journal of Fish Biology 64: 1039–1059.

    Article  Google Scholar 

  • Patterson, D. A., H. Guderley, P. Bouchard, J. S. Macdonald & A. P. Farrell, 2004b. Maternal influence and population differences in activities of mitochondrial and glycolytic enzymes in emergent sockeye salmon (Oncorhynchus nerka) fry. Canadian Journal of Fisheries and Aquatic Sciences 61: 1225–1234.

    Article  CAS  Google Scholar 

  • Pottinger, T. G. & T. R. Carrick, 1999. Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. General and Comparative Endocrinology 116: 122–132.

    Article  CAS  PubMed  Google Scholar 

  • Portz, D. E., C. M. Woodley & J. J. Cech, 2006. Stress-associated impacts of short-term holding on fishes. Reviews in Fish Biology and Fisheries 16: 125–170.

    Article  Google Scholar 

  • Robinson, K. A., S. G. Hinch, G. D. Raby, M. R. Donaldson, D. Robichaud, D. A. Patterson & S. J. Cooke, 2015. Influence of post-capture ventilation assistance on migration success of adult sockeye salmon following capture and release. Transactions of the American Fisheries Society 144: 693–704.

    Article  Google Scholar 

  • Roche, D. P., K. E. McGhee & A. M. Bell, 2012. Maternal predator-exposure has lifelong consequences for offspring learning in threespined sticklebacks. Biology Letters 8: 932–935.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sierra-Flores, R., T. Atack, H. Migaud & A. Davie, 2015. Stress response to anthropogenic noise in Atlantic cod Gadus morhua L. Aquacultural Engineering 67: 67–76.

    Article  Google Scholar 

  • Sopinka, N. M., S. G. Hinch, A. G. Lotto, C. K. Whitney & D. A. Patterson, 2013. Does among-population variation in burst swimming performance of sockeye salmon Oncorhynchus nerka fry reflect early life migrations? Journal of Fish Biology 83: 1416–1424.

    Article  CAS  PubMed  Google Scholar 

  • Sopinka, N. M., S. G. Hinch, C. T. Middleton, J. A. Hills & D. A. Patterson, 2014. Mother knows best, even when stressed? Effects of maternal exposure to a stressor on offspring performance at different life stages in a wild semelparous fish. Oecologia 175: 493–500.

    Article  CAS  PubMed  Google Scholar 

  • Sopinka, N. M., S. G. Hinch, S. J. Healy, P. M. Harrison & D. A. Patterson, 2015. Egg cortisol treatment affects the behavioural response of coho salmon to a conspecific intruder and threat of predation. Animal Behaviour 104: 115–122.

    Article  Google Scholar 

  • Stratholt, M. L., E. M. Donaldson & N. R. Liley, 1997. Stress induced elevation of plasma cortisol in adult female coho salmon (Oncorhynchus kisutch), is reflected in egg cortisol content, but does not appear to affect early development. Aquaculture 158: 141–153.

    Article  CAS  Google Scholar 

  • Taylor, E. B. & J. D. McPhail, 1985. Burst swimming and size-related predation of newly emerged coho salmon Oncorhynchus kisutch. Transactions of the American Fisheries Society 114: 546–551.

    Article  Google Scholar 

  • Uller, T. & M. Olsson, 2006. Direct exposure to corticosterone during embryonic development influences behaviour in an ovoviviparous lizard. Ethology 112: 390–397.

    Article  Google Scholar 

  • Wankowski, J. W. J., 1979. Morphological limitations, prey size selectivity, and growth response of juvenile Atlantic salmon, Salmo salar. Journal of Fish Biology 14: 89–100.

    Article  Google Scholar 

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Acknowledgments

All experimental methods were approved by the University of British Columbia (UBC) Animal Care Committee (#A11 0215) and met the Canadian Council on Animal Care guidelines. The authors thank members of the Pacific Salmon Ecology and Conservation Lab, Chehalis First Nation, DFO Environmental Watch, DFO stock assessment, DFO Cultus Lake Salmon Research Laboratory, and undergraduate volunteers for fish collection and offspring rearing, J. Hills and A. Faure for help with egg cortisol analyses, and G. Raby and two anonymous reviewers for constructive comments on an earlier version of this manuscript. SGH is funded by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery, Strategic and Network (Ocean Tracking Network Canada)  grants. NMS was funded by an NSERC graduate scholarship, and CTM was funded by an NSERC undergraduate student research award.

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Correspondence to N. M. Sopinka.

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Sopinka, N.M., Middleton, C.T., Patterson, D.A. et al. Does maternal captivity of wild, migratory sockeye salmon influence offspring performance?. Hydrobiologia 779, 1–10 (2016). https://doi.org/10.1007/s10750-016-2763-1

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