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Energy allocation and feeding ecology of juvenile chum salmon (Oncorhynchus keta) during transition from freshwater to saltwater

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Abstract

Pacific salmon (Oncorhynchus spp.) populations near their northern range extent in the Arctic-Yukon-Kuskokwim region of Alaska have undergone major changes in population trajectory and illuminated the lack of basic information on juvenile ecology. This study fills information gaps on the early life history of chum salmon at northern latitudes. Energy allocation was examined in the context of distribution, feeding intensity, and diet during a critical life history period for a single cohort of juvenile chum salmon (O. keta) as they transition from freshwater to saltwater in Kuskokwim Bay from mid-May to early June. Juvenile chum salmon were primarily captured in the river mouth and plume. Energy density (kJ g−1 dry mass) was related to fork length, timing (day-of-year), and capture location in a general additive model. The smallest fish had slightly higher energy densities, but the change in energy density with fish size was minimal and consistent with allocating energy toward somatic growth rather than lipid storage. Fish captured earlier had higher energy density, likely reflecting the presence of residual yolk lipids during early migration. Fish captured in the river mouth and plume had higher energy densities. Feeding intensity was highest among small fish captured later within the river plume. Diet was dominated by surface prey (insects and calanoid copepods) rather than epibenthic harpacticoid copepods as commonly observed. These results provide the first data on energy allocation of juvenile chum salmon during a critical life history phase and suggest that somatic growth is prioritized over storing lipid at saltwater entry.

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References

  • Andrews AG, Farley EV, Moss JH, Murphy JM, Husoe EF (2009) Energy density and lenght of juvenile pink salmon Oncorhynchus gorbuscha in the Eastern Bering Sea from 2004 to 2007: A period of relatively warm and cool sea surface temperatures. N Pac Anadromous Fish Comm 5:183–189

    Google Scholar 

  • Anthony J (2000) Lipid content and energy density of forage fishes from the northern Gulf of Alaska. J Exp Mar Bio Ecol 248:53–78. https://doi.org/10.1016/S0022-0981(00)00159-3

    Article  PubMed  CAS  Google Scholar 

  • Bailey JE, Wing BL, Mattson CR (1975) Zooplankton abundance and feeding habits of fry of pink salmon, Oncorhynchus gorbuscha, and chum salmon, Oncorhynchus keta, in Traitors Cove, Alaska, with speculations on the carrying capacity of the area. Fish Bull 73:846–861

    Google Scholar 

  • Bakkala R (1970) Synopsis of biological data on the chum salmon, Oncorhynchus keta Walbaum (1792). FAO Fisheries Synopsis No. 41, U.S. Fish and Wildlife Service Circular 315, Washington, DC

  • Ball JR, Esler D, Schmutz JA (2007) Proximate composition, energetic value, and relative abundance of prey fish from the inshore eastern Bering Sea: implications for piscivorous predators. Polar Biol 30:699–708. https://doi.org/10.1007/s00300-006-0227-1

    Article  Google Scholar 

  • Bax N (1983) Early marine mortality of marked juvenile chum salmon (Oncorhynchus keta) released into Hood Canal, Puget Sound, Washington, in 1980. Can J Fish Aquat Sci 40:426–435. https://doi.org/10.1139/f83-061

    Article  Google Scholar 

  • Beamish RJ, Mahnken C (2001) A critical size and period hypothesis to explain natural regulation of salmon abundance and the linkage to climate and climate change. Prog Oceanogr 49:423–437. https://doi.org/10.1016/S0079-6611(01)00034-9

    Article  Google Scholar 

  • Beauchamp DA (2009) Bioenergetic ontogeny: linking climate and mass-specific feeding to life-cycle growth and survival of salmon. Am Fish Soc Symp 70:1–19

    Google Scholar 

  • Bieniek PA, Bhatt US, Rundquist LA et al (2011) Large-scale climate controls of interior Alaska river ice breakup. J Clim 24:286–297. https://doi.org/10.1175/2010JCLI3809.1

    Article  Google Scholar 

  • Biro PA, Post JR, Abrahams MV (2005) Ontogeny of energy allocation reveals selective pressure promoting risk-taking behaviour in young fish cohorts. Proc R Soc B 272:1443–1448. https://doi.org/10.1098/rspb.2005.3096

    Article  PubMed  Google Scholar 

  • Blain BJ, Hansen TR, Taylor DV, Liller ZW (2016) Salmon escapement monitoring in the Kuskokwim Area, 2015. Alaska Department of Fish and Game, Fishery Data Series No. 16–23, Anchorage, Alaska

  • Brett J (1995) Energetics. In: Groot C, Margolis L, Clarke WC (eds) Physiological ecology of Pacific salmon. University of British Columbia Press, Vancouver, pp 1–68

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Chittenden CM, Jensen JLA, Ewart D et al (2010) Recent salmon declines: a result of lost feeding opportunities due to bad timing? PLoS ONE 5:e12423. https://doi.org/10.1371/journal.pone.0012423

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dauvin J, Dodson JJ (1990) Relationship between feeding incidence and vertical and longitudinal distribution of rainbow smelt larvae (Osmerus mordax) in a turbid well-mixed estuary. Mar Ecol Prog Ser 60:1–12

    Article  Google Scholar 

  • De Robertis A, Ryer CH, Veloza A, Brodeur RD (2003) Differential effects of turbidity on prey consumption of piscivorous and planktivorous fish. Can J Fish Aquat Sci 60:1517–1526. https://doi.org/10.1139/f03-123

    Article  Google Scholar 

  • De Robertis A, Morgan CA, Schabetsberger RA et al (2005) Columbia River plume fronts. II. Distribution, abundance, and feeding ecology of juvenile salmon. Mar Ecol Prog Ser 299:33–44

    Article  Google Scholar 

  • Dunmall KM, Reist JD, Carmack EC, et al (2013) Pacific Salmon in the Arctic: harbingers of change. In Mueter FJ, Dickson DMS, Huntington HP, et al. Responses of Arctic marine ecosystems to climate change. Alaska Sea Grant, University of Alaska Fairbanks https://doi.org/10.4027/ramecc.2013.07

  • Dunmall KM, Mochnacz NJ, Zimmerman CE et al (2016) Using thermal limits to assess establishment of fish dispersing to high-latitude and high-elevation watersheds. Can J Fish Aquat Sci 73:1–9. https://doi.org/10.1139/cjfas-2016-0051

    Article  Google Scholar 

  • Estensen J, Molyneaux D, Bergstrom D (2009) Kuskokwim River Chinook and chum salmon stock status and Kuskokwim area fisheries; a report to the Alaska Board of Fisheries. Alaska Department of Fish and Game, Special Publication No. 09–21, Anchorage, Alaska

  • Farley EV, Moss JH (2009) Growth rate potential of juvenile chum salmon on the eastern Bering Sea shelf: an assessment of salmon carrying capacity. N Pac Anadromous Fish Comm 5:265–277

    Google Scholar 

  • Feller R, Kaczynski V (1975) Size selective predation by juvenile chum salmon (Oncorhynchus keta) on epibenthic prey in Puget Sound. J Fish Res Board Can 32:1419–1429. https://doi.org/10.1139/f75-161

    Article  Google Scholar 

  • Fergusson EA, Sturdevant MV, Orsi JA (2010) Effects of starvation on energy density of juvenile chum salmon (Oncorhynchus keta) captured in marine waters of Southeastern Alaska. Fish Bull 108:218–225

    Google Scholar 

  • Fujiwara M, Highsmith R (1997) Harpacticoid copepods: potential link between inbound adult salmon and outbound juvenile salmon. Mar Ecol Prog Ser 158:205–216. https://doi.org/10.3354/meps158205

    Article  Google Scholar 

  • Fukuwaka M, Suzuki T (1998) Role of a riverine plume as a nursery area for chum salmon Oncorhynchus keta. Mar Ecol Prog Ser 173:289–297

    Article  Google Scholar 

  • Gregory RS, Levings CD (1998) Turbidity reduces predation on migrating juvenile Pacific salmon. Trans Am Fish Soc 127:275–285

    Article  Google Scholar 

  • Healey MC (1979) Detritus and juvenile salmon production in the Nanaimo Estuary: I. Production and feeding rates of juvenile chum salmon (Oncorhynchus keta). J Fish Res Board Can 36:488–496. https://doi.org/10.1139/f79-072

    Article  Google Scholar 

  • Healey MC (1982) Timing and relative intensity of size-selective mortality of juvenile chum salmon (Oncorhynchus keta) during early sea life. Can J Fish Aquat Sci 952–957

  • Heintz RA, Siddon EC, Farley EV, Napp JM (2013) Correlation between recruitment and fall condition of age-0 pollock (Theragra chalcogramma) from the eastern Bering Sea under varying climate conditions. Deep Res Part II 94:150–156. https://doi.org/10.1016/j.dsr2.2013.04.006

    Article  Google Scholar 

  • Hillgruber N, Zimmerman CE (2009) Estuarine ecology of juvenile salmon in western Alaska: a review. Am Fish Soc Symp 70:183–199

    Google Scholar 

  • Hillgruber N, Zimmerman CE, Burril SE, Haldorson LJ (2007) Early marine ecology of juvenile chum salmon in Kuskokwim Bay, western Alaska. Report to the North Pacific Research Board, Anchorage, Alaska

  • Hislop JRG, Harris MP, Smith JGM (1991) Variation in the calorific value and total energy content of the lesser sandeel (Ammodytes marinus) and other fish preyed on by seabirds. J Zool 224:501–517. https://doi.org/10.1111/j.1469-7998.1991.tb06039.x

    Article  Google Scholar 

  • Hyslop E (1980) Stomach contents analysis: a review of methods and their applications. J Fish Biol 17:411–429

    Article  Google Scholar 

  • Iwata M, Komatsu S (1984) Importance of estuarine residence for adaptation of chum salmon (Oncorhynchus keta) fry to seawater. Can J Fish Aquat Sci 41:744–749. https://doi.org/10.1139/f84-086

    Article  Google Scholar 

  • John M, MacDonald J, Harrison PJ et al (1992) The Fraser River plume: some preliminary observations on the distribution of juvenile salmon, herring, and their prey. Fish Oceanogr 1:153–162. https://doi.org/10.1111/j.1365-2419.1992.tb00034.x

    Article  Google Scholar 

  • Kaczynski VW, Feller RJ, Clayton J (1973) Trophic analysis of juvenile pink and chum salmon (Oncorhynchus gorbuscha and O. keta) in Puget Sound. J Fish Res Board Can 30:1003–1008. https://doi.org/10.1139/f73-164

    Article  Google Scholar 

  • Kaeriyama M (2008) Ecosystem-based sustainable conservation and management of Pacific salmon. In: Tsukamoto K, Kawamura T, Takeuchi T, et al. (eds) Proceedings of 5th World Fisheries Congress. Terra Pub, Japan, pp 371–380

  • Kruger C, Zimmerman CE (eds) (2009) Pacific salmon: ecology and management of Western Alaska’s populations. American Fisheries Society Symposium, 70, Bethesda, Maryland

  • Lawson JW (1998) Important prey species of marine vertebrate predators in the northwest Atlantic: proximate composition and energy density. Mar Ecol Prog Ser 164:13–20

    Article  Google Scholar 

  • Linderman JCJ, Bergstrom DJ (2009) Kuskokwim management area: salmon escapement, harvest, and management. Am Fish Soc Symp 70:541–599

    Google Scholar 

  • MacFarlane RB (2010) Energy dynamics and growth of Chinook salmon (Oncorhynchus tshawytscha) from the Central Valley of California during the estuarine phase and first ocean year. Can J Fish Aquat Sci 67:1549–1565. https://doi.org/10.1139/F10-080

    Article  Google Scholar 

  • Malick MJ, Cox SP, Mueter FJ, Peterman RM (2015) Linking phytoplankton phenology to salmon productivity along a north–south gradient in the Northeast Pacific Ocean. Can J Fish Aquat Sci 72:697–708

    Article  CAS  Google Scholar 

  • Manzer J (1969) Stomach contents of juvenile Pacific salmon in Chatham Sound and adjacent waters. J Fish Res Board Can 26:2219–2223

    Article  Google Scholar 

  • Martin DJ, Glass D, Whitus C, et al (1986) Distribution, seasonal abundance, and feeding dependencies of juvenile salmon and non-salmonid fishes in the Yukon River Delta. Final Report Outer Continental Shelf Environmental Assessment Program. https://doi.org/10.1007/s13398-014-0173-7.2

  • Mason J (1974) Behavioral ecology of chum salmon fry (Oncorhynchus keta) in a small estuary. J Fish Res Board Can 31:83–92

    Article  Google Scholar 

  • Merritt M, Raymond J (1983) Early life history of chum salmon in the Noatak River and Kotzebue Sound. Alaska Department of Fish and Game, Division of Fisheries Rehabilitation, Enhancement, and Development Report, Juneau, Alaska

  • Molyneaux D, Brodersen A, Shelden C (2010) Salmon age, sex and length catalog for the Kuskokwim area, 2009. Alaska Department of Fish and Game, Division of Commercial Fisheries, Regional Information Report 3A10-05, Anchorage, Alaska

  • Montevecchi WA, Piatt JF (1987) Dehydration of seabird prey during transport to the colony: effects on wet weight energy densities. Can J Zool 65:2822–2824

    Article  Google Scholar 

  • Moss JH, Murphy JM, Farley EV Jr et al (2009) Juvenile pink and chum salmon distribution, diet, and growth in the Northern Bering and Chukchi seas. N Pac Anadromous Fish Comm Bull 5:191–196

    Google Scholar 

  • Moss JH, Murphy JM, Fergusson EA, Heintz RA (2016) Allometric relationships between body size and energy density of juvenile Chinook (Oncorhynchus tshawytscha) and chum (O. keta) salmon across a latitudinal gradient. N Pac Anadromous Fish Comm. https://doi.org/10.23849/npafcb6/161.168

    Article  Google Scholar 

  • Moulton LL (1997) Early marine residence, growth, and feeding by juvenile salmon in northern Cook Inlet, Alaska. Alaska Fish Res Bull 4:154–177

    Google Scholar 

  • Murphy ML, Thedinga JF, Koski KV (1988) Size and diet of juvenile Pacific salmon during seaward migration through a small estuary in southeastern Alaska. Fish Bull 86:213–222

    Google Scholar 

  • Neave F (1966) Salmon of the north Pacific Ocean—part III. A review of the life history of north Pacific salmon. 6. Chum salmon in British Columbia. Int N Pac Fish Comm Bull 18:81–86

    Google Scholar 

  • Neimark LM (1979) Zooplankton ecology of Norton Sound, Alaska. Thesis, University of Alaska Fairbanks

  • Nemeth M, Williams B, Haley B, Kinneen S (2006) An ecological comparison of juvenile chum salmon from two watersheds in Norton Sound, Alaska: migration, diet, estuarine habitat, and fish community assemblage. Final Report for 2003 and 2004 to the Norton Sound Disaster Relief Fund by the Norton Sound Economic Development Corporation and LGL Alaska Research Associates, Inc. Anchorage, Alaska

  • Nielsen JL, Ruggerone GT, Zimmerman CE (2013) Adaptive strategies and life history characteristics in a warming climate: Salmon in the Arctic? Environ Biol Fishes 96:1187–1226. https://doi.org/10.1007/s10641-012-0082-6

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, et al (2016) vegan: Community Ecology Package

  • Orsi JA, Wertheimer AC, Sturdevant MV et al (2004) Juvenile chum salmon consumption of zooplankton in marine waters of southeastern Alaska: a bioenergetics approach to implications of hatchery stock interactions. Rev Fish Biol Fish 14:335–359. https://doi.org/10.1007/s11160-004-3813-8

    Article  Google Scholar 

  • Parker RR (1968) Marine mortality schedules of pink salmon of the Bella Coola River, central British Columbia. J Fish Res Board Can 25:757–794

    Article  Google Scholar 

  • Parker D, Massa J (1991) A comparison of diets and apparent growth rates for juvenile pink and chum salmon collected in Prince William Sound, Alaska. In: Proceedings of the 16th Northeast Pacific Pink and Chum Salmon Workshop. Alaska Sea Grant College Program, Report No. 94-02, pp 1–15

  • Parr Instrument Company (1994) Operating instruction manual: 1425 semimicro bomb calorimeter No. 280MM. Parr Instrument Co., Illinois, USA

  • Post JR, Parkinson E (2001) Energy allocation strategy in young fish: allometry and survival. Ecology 82:1040–1051

    Article  Google Scholar 

  • R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Raymond JA, Skaugstad C (1986) Observations on the emigration of hatchery-produced chum salmon in the Noatak River, Alaska

  • Reese C, Hillgruber N, Sturdevant M et al (2009) Spatial and temporal distribution and the potential for estuarine interactions between wild and hatchery chum salmon (Oncorhynchus keta) in Taku Inlet, Alaska. Fish Bull 107:433–450

    Google Scholar 

  • Robards MD, Anthony JA, Rose GA, Piatt JF (1999) Changes in proximate composition and somatic energy content for Pacific sand lance (Ammodytes hexapterus) from Kachemak Bay, Alaska relative to maturity and season. J Exp Mar Bio Ecol 242:245–258

    Article  Google Scholar 

  • Siddon EC, Heintz RA, Mueter FJ (2013) Conceptual model of energy allocation in walleye pollock (Theragra chalcogramma) from age-0 to age-1 in the southeastern Bering Sea. Deep Sea Res Part II 94:140–149. https://doi.org/10.1016/j.dsr2.2012.12.007

    Article  Google Scholar 

  • Simenstad CA (1981) Juvenile salmonid and baitfish distribution, abundance, and prey resources in selected areas of Grays Harbor, Washington. Final Report to the U.S. Army Corps Engineers, University of Washington, Fish Research Institute Report FRI-UW-8117

  • Simenstad CA, Fresh KL, Salo EO (1982) The role of Puget Sound and Washington coastal estuaries in the life history of Pacific salmon: an unappreciated function. In: Kennedy V (ed) Estuarine comparisons. Academic Press, New York, pp 343–364

    Chapter  Google Scholar 

  • Stabeno PJ, Kachel NB, Moore SE et al (2012) Comparison of warm and cold years on the southeastern Bering Sea shelf and some implications for the ecosystem. Deep Res Part II Top Stud Oceanogr 65–70:31–45. https://doi.org/10.1016/j.dsr2.2012.02.020

    Article  Google Scholar 

  • Stewart DJ, Weininger D, Rottiers DV, Edsall TA (1983) An energetics model for lake trout, Salvelinus namaycush: application to the Lake Michigan population. Can J Fish Aquat Sci 40:681–698. https://doi.org/10.1139/f83-091

    Article  Google Scholar 

  • Sturdevant MV, Wertheimer AC, Lum J (1996) Diets of juvenile pink and chum salmon in oiled and non-oiled nearshore habitats in Prince William Sound, 1989 and 1990. Am Fish Soc Symp 18:578–592

    CAS  Google Scholar 

  • Sturdevant MV, Fergusson E, Hillgruber N et al (2012) Lack of trophic competition among wild and hatchery juvenile chum salmon during early marine residence in Taku Inlet, Southeast Alaska. Environ Biol Fishes 94:101–116. https://doi.org/10.1007/s10641-011-9899-7

    Article  Google Scholar 

  • Trudel M, Tucker S, Morris JFT et al (2005) Indicators of energetic status in juvenile coho salmon and Chinook salmon. N Am J Fish Manage 25:374–390. https://doi.org/10.1577/M04-018.1

    Article  Google Scholar 

  • Van Pelt T, Piatt J, Lance BK, Roby DD (1997) Proximate composition and energy density of some North Pacific forage fishes. Comp Biochem Physiol Part A 118:1393–1398

    Article  Google Scholar 

  • Varnavsky VS, Kinas NM, Rostomova SA (1993) Development of seawater adaptation in pink salmon, Oncorhynchus gorbuscha, during downstream migration: relationships to temperature and residual yolk. Environ Biol Fishes 36:373–379. https://doi.org/10.1007/BF00012415

    Article  Google Scholar 

  • Vollenweider JJ, Heintz RA, Schaufler L, Bradshaw R (2011) Seasonal cycles in whole-body proximate composition and energy content of forage fish vary with water depth. Mar Biol 158:413–427. https://doi.org/10.1007/s00227-010-1569-3

    Article  PubMed  Google Scholar 

  • Wolfe RJ, Spaeder J (2009) People and salmon of the Yukon and Kuskokwim drainages and Norton Sound in Alaska: Fishery harvests, culture change, and local knowledge systems. In: Pacific salmon: Ecology and management of western Alaska’s populations. American Fisheries Society Symposium, 70, Bethesda, Maryland, pp 349–379

  • Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc 73:3–36

    Article  Google Scholar 

  • Young CD (2009) Shoaling behavior as a tool to understand microhabitat use by juvenile chum salmon, Oncorhynchus keta. MS Thesis, University of Washington, Seattle, Washington

  • Zimmerman C, Mosegaard H (1992) Initial feeding in migratory brown trout (Salmo trutta L.) alevins. J Fish Biol 40:647–650. https://doi.org/10.1111/j.1095-8649.1992.tb02612.x

    Article  Google Scholar 

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Acknowledgements

We are grateful to the North Pacific Research Board (NPRB) for funding this research (Project R0327). We thank Capt. J. Peacock and crew of the chartered vessel F/V Eileen O’Farrel and Capt. B. Wiebe of the chartered vessel F/V Namorada for navigation and use of their boats during our field sampling. In addition, we thank volunteers J. Zutz and M. Blikshteyn for assistance with sampling. Our sincere thanks to D. Cuadra, M. Sturdevant, C. Stark, and W. Park for their generous advice and assistance. E. Siddon, M. Arimitsu, and two anonymous reviewers provide valuable comments on an earlier draft of this manuscript. Fish treatment followed a protocol approved by the University of Alaska Fairbanks Animal Care and Use Committee (IACUC # 03-18). Any use of trade names or products is for descriptive purposes only and does not imply endorsement of the U.S. Government.

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Burril, S.E., von Biela, V.R., Hillgruber, N. et al. Energy allocation and feeding ecology of juvenile chum salmon (Oncorhynchus keta) during transition from freshwater to saltwater. Polar Biol 41, 1447–1461 (2018). https://doi.org/10.1007/s00300-018-2297-2

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