Your PDF has successfully downloaded.

You may be interested in finding more content on these topics:


You are not currently logged in.

Access JSTOR through your library or other institution:


Log in through your institution.

Burst Swimming in Areas of High Flow: Delayed Consequences of Anaerobiosis in Wild Adult Sockeye Salmon

Nicholas J. Burnett, Scott G. Hinch, Douglas C. Braun, Matthew T. Casselman, Collin T. Middleton, Samantha M. Wilson and Steven J. Cooke
Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches
Vol. 87, No. 5 (September/October 2014), pp. 587-598
DOI: 10.1086/677219
Stable URL:
Page Count: 12
  • Download PDF
  • Add to My Lists
  • Cite this Item
We're having trouble loading this content. Download PDF instead.


AbstractWild riverine fishes are known to rely on burst swimming to traverse hydraulically challenging reaches, and yet there has been little investigation as to whether swimming anaerobically in areas of high flow can lead to delayed mortality. Using acoustic accelerometer transmitters, we estimated the anaerobic activity of anadromous adult sockeye salmon (Oncorhynchus nerka) in the tailrace of a diversion dam in British Columbia, Canada, and its effects on the remaining 50 km of their freshwater spawning migration. Consistent with our hypothesis, migrants that elicited burst swimming behaviors in high flows were more likely to succumb to mortality following dam passage. Females swam with more anaerobic effort compared to males, providing a mechanism for the female-biased migration mortality observed in this watershed. Alterations to dam operations prevented the release of hypolimnetic water from an upstream lake, exposing some migrants to supraoptimal, near-lethal water temperatures (i.e., 24°C) that inhibited their ability to locate, enter, and ascend a vertical-slot fishway. Findings from this study have shown delayed post–dam passage survival consequences of high-flow-induced burst swimming in sockeye salmon. We highlight the need for studies to investigate whether dams can impose other carryover effects on wild aquatic animals.

Notes and References

This item contains 71 references.

Literature Cited
  • ['Andrew F.J. and G.H. Geen. 1958. Sockeye salmon and pink salmon investigations at the Seton Creek hydroelectric installation. Int Pac Salmon Fish Comm Prog Rep 4. 74 pp.']
  • ['Barton K. 2012. MuMIn: multi-model inference. R package, version 1.7.11.']
  • ['Beacham T.D., M. Lapointe, J.R. Candy, K.M. Miller, and R.E. Withler. 2004. DNA in action: rapid application of DNA variation to sockeye salmon fisheries management. Conserv Genet 5:411–416.']
  • ['Black E.C. 1958. Hyperactivity as a lethal factor in fish. J Fish Board Can 15:573–586.']
  • ['Black E.C., N.J. Bosomworth, and G.E. Docherty. 1966. Combined effect of starvation and severe exercise on glycogen metabolism of rainbow trout, Salmo gairdneri. J Fish Res Board Can 23:1461–1463.']
  • ['Brett J.R. 1995. Energetics. Pp. 3–68 in C. Groot, L. Margolis, and W.C. Clarke, eds. Physiological ecology of Pacific salmon. UBC Press, Vancouver.']
  • ['Brown D.D., R. Kays, M. Wikelski, R. Wilson, and A.P. Klimley. 2013. Observing the unwatchable through acceleration logging of animal behavior. Anim Biotelem 1:20. doi:10.1186/2050-3385-1-20.']
  • ['Brown R.S., D.R. Geist, and M.G. Mesa. 2006. Use of electromyogram telemetry to assess swimming activity of adult Chinook salmon migrating past a Columbia River dam. Trans Am Fish Soc 135:281–287.']
  • ['Bunt C.M. 2001. Fishway entrance modifications enhance fish attraction. Fish Manag Ecol 8:95–105.']
  • ['Bunt C.M., T. Castro-Santos, and A. Haro. 2011. Performance of fish passage structures at upstream barriers to migration. River Res Appl 28:457–478.']
  • ['Burgetz I.J., A. Rojas-Vargas, S.G. Hinch, and D.J. Randall. 1998. Initial recruitment of anaerobic metabolism during submaximal swimming in rainbow trout (Oncorhynchus mykiss). J Exp Biol 201:2711–2721.']
  • ['Burnett N.J., S.G. Hinch, M.R. Donaldson, N.B. Furey, D.A. Patterson, D.W. Roscoe, and S.J. Cooke. 2013a. Alterations to dam-spill discharge influence sex-specific activity, behavior and passage success of migrating adult sockeye salmon. Ecohydrology. doi:10.1002/eco.1440.']
  • ['Burnett N.J., K.M. Stamplecoskie, J.D. Thiem, and S.J. Cooke. 2013b. Comparison of detection efficiency among three sizes of half duplex passive integrated transponders using manual tracking and fixed antenna arrays. N Am J Fish Manag 33:7–13.']
  • ['Burnham K.P. and D.R. Anderson. 2002. Pp. 1–515 in Model selection and multimodel inference. Springer, New York.']
  • ['Castro-Santos T., A. Cotel, and P.W. Webb. 2009. Fishway evaluations for better bioengineering: an integrative approach. Pp. 557–575 in A. Haro, K.L. Smith, R.A. Rulifson, C.M. Moffit, R.J. Klauda, M.J. Dadswell, R.A. Cunjak, J.E. Cooper, K.L. Beal, and T.S. Avery, eds. Challenges for diadromous fishes in a dynamic global environment. American Fisheries Society Symposium, Bethesda, MD.']
  • ['Caudill C.C., W.R. Daigle, M.L. Keefer, C.T. Boggs, M.A. Jepson, B.J. Burke, R.W. Zabel, T.C. Bjornn, and C.A. Peery. 2007. Slow dam passage in adult Columbia River salmonids associated with unsuccessful migration: delayed negative effects of passage obstacles or condition-dependent mortality. Can J Fish Aquat Sci 64:979–995. ']
  • ['Clay C.H. 1995. Design of fishways and other fish facilities. 2nd ed. Lewis, Boca Raton, FL.']
  • ['Cooke S.J., G.T. Crossin, D.A. Patterson, K. English, S.G. Hinch, J.L. Young, R. Alexander, M.C. Healey, G. Van Der Kraak, and A.P. Farrell. 2005. Coupling non-invasive physiological and energetic assessments with telemetry to understand inter-individual variation in behavior and survivorship of sockeye salmon: development and validation of a technique. J Fish Biol 67:1342–1358.']
  • ['Cooke S.J. and S.G. Hinch. 2013. Improving the reliability of fishway attraction and passage efficiency estimates to inform fishway engineering, science, and practice. Ecol Eng 58:123–132.']
  • ['Crossin G.T. and S.G. Hinch. 2005. A non-lethal method for assessing the somatic energy content of freely migrating adult Pacific salmon. Trans Am Fish Soc 134:184–191.']
  • ['Crossin G.T., S.G. Hinch, S.J. Cooke, D.W. Welch, D.A. Patterson, S.R.M. Jones, A.G. Lotto, et al. 2008. Exposure to high temperature influences the behavior, physiology, and survival of sockeye salmon during spawning migration. Can J Zool 86:127–140.']
  • ['Crossin G.T., S.G. Hinch, A.P. Farrell, D.A. Higgs, and M.C. Healey. 2004. Somatic energy of sockeye salmon at the onset of upriver migration a comparison among ocean climate regimes. Fish Oceanogr 29:22–33.']
  • ['Dingle H. 1996. Migration: the biology of life on the move. Oxford University Press, New York.']
  • ['Eliason E.J., T.D. Clark, M.J. Hague, L.M. Hanson, Z.S. Gallagher, K.M. Jeffries, M.K. Gale, D.A. Patterson, S.G. Hinch, and A.P. Farrell. 2011. Differences in thermal tolerance among sockeye salmon populations. Science 332:109–112.']
  • ['Eliason E.J., T.D. Clark, S.G. Hinch, and A.P. Farrell. 2013. Cardiorespiratory collapse at high temperature in swimming adult sockeye salmon. Conserv Physiol 1. doi:10.1093/conphys/cot008.']
  • ['Farrell A.P., S.G. Hinch, S.J. Cooke, D.A. Patterson, G.T. Crossin, M. Lapointe, and M.T. Mathes. 2008. Pacific salmon in hot water: applying aerobic scope models and biotelemetry to predict the success of spawning migrations. Physiol Biochem Zool 81:697–708.']
  • ['Gelman A. 2008. Scaling regression inputs by dividing by two standard deviations. Stat Med 27:2865–2873.']
  • ['Gleiss A.C., J.J. Dale, K.N. Holland, and R.P. Wilson. 2010. Accelerating estimates of activity-specific metabolic rate in fishes: testing the applicability of acceleration data-loggers. J Exp Mar Biol Ecol 385:85–91.']
  • ['Grueber C.E., S. Nakagawa, R.J. Laws, and I.G. Jamieson. 2011. Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711.']
  • ['Hague M.J., M.R. Ferrari, J.R. Miller, D.A. Patterson, G.L. Russells, A.P. Farrell, and S.G. Hinch. 2011. Modelling the future hydroclimatology of the lower Fraser River and its impacts on the spawning migration survival of sockeye salmon. Glob Change Biol 17:87–98.']
  • ['Hasler C.T., B. Mossop, D.A. Patterson, S.G. Hinch, and S.J. Cooke. 2012. Swimming activity of migrating Chinook salmon in a regulated river. Aquat Biol 17:47–56.']
  • ['Hinch S.G. and J. Bratty. 2000. Effects of swimming speed and activity pattern on success of adult sockeye salmon migration through an area of difficult passage. Trans Am Fish Soc 129:598–606.']
  • ['Hinch S.G. and P.S. Rand. 1998. Swimming speeds and energy use of upriver migrating sockeye salmon (Oncorhynchus nerka): role of local environment and fish characteristics. Can J Fish Aquat Sci 55:1821–1831.']
  • ['———. 2000. Optimal swimming speeds and forward assisted propulsion: energy conserving behaviors of upriver-migrating salmon. Can J Fish Aquat Sci 57:2470–2478.']
  • ['Hinch S.G., E.M. Standen, M.C. Healey, and A.P. Farrell. 2002. Swimming patterns and behavior of upriver migrating adult pink (Oncorhynchus gorbuscha) and sockeye salmon (O. nerka) salmon as assessed by EMG telemetry in the Fraser River, British Columbia, Canada. Hydrobiologia 165:147–160.']
  • ['Katopodis C. 1992. Introduction to fishway design. Freshwater Institute, Winnipeg.']
  • ['Keefer M.L., C.A. Peery, and M.J. Heinrich. 2008. Temperature-mediated en route migration mortality and travel rates of endangered Snake River sockeye salmon. Ecol Freshw Fish 17:136–145.']
  • ['Kindt R. and R. Coe. 2005. Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre, Nairobi.']
  • ['Laine A. 1995. Fish swimming behavior in Finnish fishways. Pp. 323–328 in S. Komura, ed. Proceedings of the International Symposium on Fishways ’95, Gifu, Japan. Organising Committee for International Symposium on Fishways.']
  • ['Lee C.G., A.P. Farrell, A.G. Lotto, S.G. Hinch, and M.C. Healey. 2003a. Excess post-exercise oxygen consumption in adult sockeye salmon (Oncorhynchus nerka) and coho (O. kisutch) salmon following critical speed swimming. J Exp Biol 206:3253–3260.']
  • ['Lee C.G., A.P. Farrell, A.G. Lotto, M.J. MacNutt, S.G. Hinch, and M.C. Healey. 2003b. The effect of temperature on swimming performance and oxygen consumption in adult sockeye salmon (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. J Exp Biol 206:3239–3251.']
  • ['Martins E.G., S.G. Hinch, D.A. Patterson, M.J. Hague, S.J. Cooke, K.M. Miller, D. Robichaud, K.K. English, and A.P. Farrell. 2012. High river temperature reduces survival of sockeye salmon approaching spawning grounds and exacerbates female mortality. Can J Fish Aquat Sci 69:330–342.']
  • ['Miller K.M., A. Teffer, S. Tucker, S. Li, A.D. Schulze, M. Trudel, F. Juanes, et al. 2014. Infectious disease, shifting climates and opportunistic predators: cumulative factors potentially impacting declining wild salmon populations. Evol Appl. doi:10.1111/eva.12164.']
  • ['Nadeau P.S., S.G. Hinch, K.A. Hruska, L.B. Pon, and D.A. Patterson. 2010. The effects of experimental energy depletion on the physiological condition and survival of adult sockeye salmon (Oncorhynchus nerka) during spawning migration. Environ Biol Fish 88:241–251.']
  • ['Naughton G.P., C.C. Caudill, M.L. Keefer, T.C. Bjornn, L.C. Stuehrenberg, and C.A. Peery. 2005. Late-season mortality during migration of radio-tagged adult sockeye salmon (Oncorhynchus nerka) in the Columbia River. Can J Fish Aquat Sci 62:30–47.']
  • ['Nehlsen W., J.E. Williams, and J.A. Lichatowich. 1991. Pacific salmon at the crossroads: stocks at risk from California, Oregon, Idaho, and Washington. Fisheries 16:4–21.']
  • ['Nilsson C., C.A. Reidy, M. Dynesius, and C. Revenga. 2005. Fragmentation and flow regulation of the world’s large river systems. Science 308:405–408.']
  • ['O’Connor C.M., D.R. Norris, G.T. Crossin, and S.J. Cooke. 2014. Biological carryover effects: linking common concepts and mechanisms in ecology and evolution. Ecosphere 5. doi:10.1890/ES13-00388.1.']
  • ['Patterson D.A., J.S. Macdonald, K.M. Skibo, D. Barnes, I. Guthrie, and J. Hills. 2007. Reconstructing the summer thermal history for the lower Fraser River, 1941 to 2006, and implications for adult sockeye salmon (Oncorhynchus nerka) spawning migration. Can Tech Rep Fish Aquat Sci 2724.']
  • ['Pon L.B., S.G. Hinch, S.J. Cooke, D.A. Patterson, and A.P. Farrell. 2009. Physiological, energetic and behavioural correlates of successful fishway passage of adult sockeye salmon Oncorhynchus nerka in the Seton River, British Columbia. J Fish Biol 74:1323–1336.']
  • ['Preece R.M. and H.A. Jones. 2002. The effect of Keepit Dam on the temperature regime of the Namoi River, Australia. River Res Appl 18:397–414.']
  • ['Priede I.G. 1977. Natural selection for energetic efficiency and the relationship between activity level and mortality. Nature 267:610–611.']
  • ['R Development Core Team. 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.']
  • ['Rand P.S., S.G. Hinch, J. Morrison, M.G.G. Foreman, M.J. MacNutt, J.S. Macdonald, M.C. Healey, A.P. Farrell, and D.A. Higgs. 2006. Effects of river discharge, temperature, and future climates on energetics and mortality of adult migrating Fraser River sockeye salmon. Trans Am Fish Soc 135:655–667.']
  • ['Roscoe D.W., S.G. Hinch, S.J. Cooke, and D.A. Patterson. 2011. Fishway passage and post passage mortality of up-river migrating sockeye salmon in the Seton River, British Columbia. River Res Appl 27:693–705.']
  • ['Rosenberg D.M., P. McCully, and C.M. Pringle. 2000. Global-scale environmental effects of hydrological alterations: introduction. BioScience 50:746–751.']
  • ['Servizi J.A. and J.O. Jensen. 1977. Resistance of adult sockeye salmon to acute thermal shock. Int Pac Salmon Fish Comm Prog Rep 34.']
  • ['Slaney T.L., K.D. Hyatt, T.G. Northcote, and R.J. Fielden. 1996. Status of anadromous salmon and trout in British Columbia and Yukon. Fisheries 21:20–35.']
  • ['Standen E.M., S.G. Hinch, M.C. Healey, and A.P. Farrell. 2002. Energetic costs of migration through the Fraser River Canyon, British Columbia, in adult pink (Oncorhynchus gorbuscha) and sockeye (O. nerka) salmon as assessed by EMG telemetry. Can J Fish Aquat Sci 59:1809–1818.']
  • ['Tierney K.B. and A.P. Farrell. 2004. The relationships between fish health, metabolic rate, swimming performance and recovery in return-run sockeye salmon, Oncorhynchus nerka (Walbaum). J Fish Dis 27:663–671.']
  • ['Videler J.J. 1993. Fish swimming. Chapman & Hall, London.']
  • ['Videler J.J. and D. Weihs. 1982. Energetic advantages of burst-and-coast swimming of fish at high speeds. J Exp Biol 97:169–178.']
  • ['Wagenmakers E.-J. and S. Farrell. 2004. AIC model selection using Akaike weights. Psychon Bull Rev 11:192–196.']
  • ['Webb P.W. 1995. Locomotion. Pp. 69–99 in C. Groot, L. Margolis, and W.C. Clarke, eds. Physiological ecology of Pacific salmon. UBC Press, Vancouver.']
  • ['Weihs D. 1974. Energetic advantages of burst swimming of fish. J Theor Biol 48:215–229.']
  • ['Wilson R.P., C.R. White, F. Quintana, L.G. Halsey, N. Liebsch, G.R. Martin, and P.J. Butler. 2006. Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant. J Anim Ecol 75:1081–1090.']
  • ['Wilson S.M., S.G. Hinch, S.M. Drenner, E.G. Martins, N.B. Furey, D.A. Patterson, D.W. Welch, and S.J. Cooke. 2014. Coastal marine and in-river migration behavior of adult sockeye salmon en route to spawning grounds. Mar Ecol Prog Ser 496:71–84.']
  • ['Wilson S.M., S.G. Hinch, E.J. Eliason, A.P. Farrell, and S.J. Cooke. 2013. Calibrating acoustic acceleration transmitters for estimating energy use by wild adult Pacific salmon. Comp Biochem Physiol A 164:491–498.']
  • ['Wood C.M. 1991. Acid-base and ion balance, metabolism, and their interactions, after exhaustive exercise in fish. J Exp Biol 160:285–308.']
  • ['Wood C.M., J.D. Turner, and M.S. Graham. 1983. Why do fish die after severe exercise? J Fish Biol 22:189–201.']
  • ['Zuur A., E. Ieno, and C. Elphick. 2010. A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14.']