Skip to main content
Log in

Variability in Juvenile English Sole Condition Relative to Temperature and Trophic Dynamics Along an Oregon Estuarine Gradient

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Many benthic fish and invertebrates, including the flatfish English sole (Parophrys vetulus), utilize estuaries as nursery habitat during their juvenile life stage. Regions within an estuary differ with respect to salinity, temperature, oxygen, and organic inputs, highlighting the complexity of nursery habitat and the need to assess multiple habitats within a single estuary. To determine the effect of variable estuarine habitat on juvenile English sole, we examined morphometric and energetic (lipid) condition, fatty acids, and stable isotopes (13C and 15N) of wild-caught juveniles from upriver and downriver habitats within the Yaquina Bay, Oregon estuary. Downriver-caught fish exhibited higher energetic condition, which may be attributed to cooler temperatures and the marine-sourced carbon that typified that region’s food web. Conversely, individuals from the upriver habitat exhibited higher morphometric condition. This may be due in part to the warmer temperatures upriver that have been observed to promote growth and suppress lipid storage in other marine species. Our findings highlight the important but variable contribution of both upriver and downriver habitats to English sole early life history.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amara, R., and R. Galois. 2004. Nutritional condition of metamorphosing sole: Spatial and temporal analyses. Journal of Fish Biology 64: 1–17.

    Article  Google Scholar 

  • Amara, R., T. Meziane, C. Gilliers, G. Hermel, and P. Laffargue. 2007. Growth and condition indices in juvenile sole Solea solea measured to assess the quality of essential fish habitat. Marine Ecology Progress Series 351: 201–208.

    Article  Google Scholar 

  • Barss, W.H. 1976. The English sole. Informational report 76–1, Oregon Department of Fish and Wildlife.

  • Beck, M.W., K.L. Heck Jr., K.W. Able, D.L. Childers, D.B. Eggleston, B.M. Gillanders, B. Halpern, C.G. Hays, K. Hoshino, T.J. Minello, R.J. Orth, P.F. Sheridan, and M.P. Weinstein. 2001. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51 (8): 633–641.

    Article  Google Scholar 

  • Bell, M.V., and J.R. Dick. 1991. Molecular species composition of the major diacyl glycerophospholipids from muscle, liver, retina and brain of cod (Gadus morhua). Lipids 26 (8): 565–573.

    Article  CAS  Google Scholar 

  • Bergamino, L., and T. Dalu. 2014. Evidence of spatial and temporal changes in sources of organic matter in estuarine sediments: Stable isotope and fatty acid analyses. Hydrobiologia 732 (1): 133–145.

    Article  CAS  Google Scholar 

  • Boehlert, G.W., and B.C. Mundy. 1987. Recruitment dynamics of metamorphosing English sole (Parophrys vetulus) to Yaquina Bay, Oregon. Estuarine, Coastal and Shelf Science 25 (3): 261–281.

    Article  Google Scholar 

  • Bosley, K.M., L.A. Copeman, B.R. Dumbauld, and K.L. Bosley. 2017. Identification of burrowing shrimp food sources along an estuarine gradient using fatty acid analysis and stable isotope ratios. Estuaries and Coasts 40 (4): 1113–1130.

    Article  CAS  Google Scholar 

  • Brown, C.A., and J.H. Power. 2011. Historic and recent patterns of dissolved oxygen in the Yaquina estuary (Oregon, USA): Importance of anthropogenic activities and oceanic conditions. Estuarine, Coastal and Shelf Science 92 (3): 446–455.

    Article  CAS  Google Scholar 

  • Budd, P.L. 1940. State of California Department of Natural Resources Division of fish and game bulletin no. 56, development of the eggs and early larvae of six California fishes.

  • Budge, S.M., S.J. Iverson, and H.N. Koopman. 2006. Studying trophic ecology in marine ecosystems using fatty acids: A primer on analysis and interpretation. Marine Mammal Science 22 (4): 759–801.

    Article  Google Scholar 

  • Copeman, L.A., and C.C. Parrish. 2003. Marine lipids in a cold coastal ecosystem: Gilbert Bay, Labrador. Marine Biology 143 (6): 1213–1227.

    Article  CAS  Google Scholar 

  • Copeman, L.A., B.J. Laurel, K.M. Boswell, A.L. Sremba, K. Klinck, R.A. Heintz, J.J. Vollenweider, T.E. Helser, and M.L. Spencer. 2015. Ontogenetic and spatial variability in trophic biomarkers of juvenile saffron cod (Eleginus gracilis) from the Beaufort, Chukchi and Bering Seas. Polar Biology: 1–18.

  • Copeman, L.A., B.J. Laurel, M. Spencer, and A. Sremba. 2017. Temperature impacts on lipid allocation among juvenile gadid species at the Pacific Arctic-boreal interface: An experimental laboratory approach. Marine Ecology Progress Series 566: 183–198.

    Article  CAS  Google Scholar 

  • Copeman, L., C. Ryer, M. Spencer, M. Ottmar, P. Iseri, A. Sremba, J. Wells, and C. Parrish. 2018. Benthic enrichment by diatom-sourced lipid promotes growth and condition in juvenile Tanner crabs around Kodiak Island, Alaska. Marine Ecology Progress Series 597: 161–178.

    Article  CAS  Google Scholar 

  • Cowey, C.B., J.M. Owen, J.W. Adron, and C. Middleton. 1976. Studies on the nutrition of marine flatfish. The effect of different dietary fatty acids on the growth and fatty acid composition of turbot (Scophthalmus maximus). British Journal of Nutrition 36 (3): 479–486.

    Article  CAS  Google Scholar 

  • Cushing, D.H. 1989. A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified. Journal of Plankton Research 11 (1): 1–13.

    Article  Google Scholar 

  • Dalsgaard, J., M. St John, G. Kattner, D. Muller-Navarra, and W. Hagen. 2003. Fatty acid trophic markers in the pelagic marine environment. Advances in Marine Biology 46: 225–340.

    Article  Google Scholar 

  • De Ben, W.A., W.D. Clothier, G.R. Ditsworth, and D.J. Baumgartner. 1990. Spatio-temporal fluctuations in the distribution and abundance of demersal fish and epibenthic crustaceans in Yaquina Bay, Oregon. Estuaries 13 (4): 469–478.

    Article  Google Scholar 

  • Escalas, A., F. Ferraton, C. Paillon, G. Vidy, F. Carcaillet, C. Salen-Picard, F. Le Loc’h, P. Richard, and A.M. Darnaude. 2015. Spatial variations in dietary organic matter sources modulate the size and condition of fish juveniles in temperate lagoon nursery sites. Estuarine, Coastal and Shelf Science 152: 78–90.

    Article  CAS  Google Scholar 

  • Folch, J., M. Lees, and G.H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226: 497–509.

    CAS  Google Scholar 

  • Fraser, A.J. 1989. Triacylglycerol content as a condition index for fish, bivalve, and crustacean larvae. Canadian Journal of Fisheries and Aquatic Sciences 46 (11): 1868–1873.

    Article  CAS  Google Scholar 

  • Fry, B., and E.B. Sherr. 1984. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contributions in Marine Science 27: 13–47.

    CAS  Google Scholar 

  • Gunderson, D.R., D.A. Armstrong, Y. Shi, and R.A. McConnaughey. 1990. Patterns of estuarine use by juvenile English sole (Parophrys vetulus) and Dungeness crab (Cancer magister). Estuaries 13: 55–71.

    Article  Google Scholar 

  • Hogue, E.W., and A.G. Carey Jr. 1982. Feeding ecology of 0-age flatfishes at a nursery ground on the Oregon coast. Fishery Bulletin 80: 555–565.

    Google Scholar 

  • Howe, E.R., and C.A. Simenstad. 2015. Using stable isotopes to discern mechanisms of connectivity in estuarine detritus-based food webs. Marine Ecology Progress Series 518: 13–29.

    Article  Google Scholar 

  • Huyer, A., P.A. Wheeler, T. Strub, R.L. Smith, R. Letelier, and P.M. Kosro. 2007. The Newport line off Oregon—Studies in the north East Pacific. Progress in Oceanography 75 (2): 126–160.

    Article  Google Scholar 

  • Islam, S., and M. Tanaka. 2006. Spatial variability in nursery functions along a temperate estuarine gradient: Role of detrital versus algal trophic pathways. Canadian Journal of Fisheries and Aquatic Sciences 63 (8): 1848–1864.

    Article  Google Scholar 

  • Kelly, J.R., and R.E. Scheibling. 2012. Fatty acids as dietary tracers in benthic food webs. Marine Ecology Progress Series 446: 1–22.

    Article  CAS  Google Scholar 

  • Kerambrun, E., F. Henry, K. Rabhi, and R. Amara. 2014. Effects of chemical stress and food limitation on the energy reserves and growth of turbot, Scophthalmus maximus. Environmental Science and Pollution Research 21 (23): 13488–13495.

    Article  CAS  Google Scholar 

  • Koenker, B.L., L.A. Copeman, and B.J. Laurel. 2018. Impacts of temperature and food availability on the condition of larval Arctic cod (Boreogadus saida) and walleye Pollock (Gadus chalcogrammus). ICES Journal of Marine Science. 75 (7): 2370–2385. https://doi.org/10.1093/icesjms/fsy052.

    Article  Google Scholar 

  • Krygier, E.E., and W.G. Pearcy. 1986. The role of estuarine and offshore nursery areas for young English sole (Parophrys vetulus Girard) of Oregon. Fishery Bulletin 84: 119–132.

    Google Scholar 

  • Litz, M.N.C., R.D. Brodeur, R.L. Emmett, S.S. Heppell, R.S. Rasmussen, L. O’Higgins, and M.S. Morris. 2010. Effects of variable oceanographic conditions on forage fish lipid content and fatty acid composition in the northern California current. Marine Ecology Progress Series 405: 71–85.

    Article  CAS  Google Scholar 

  • Litzow, M.A., K.M. Bailey, F.G. Prahl, and R. Heintz. 2006. Climate regime shifts and reorganization of fish communities: The essential fatty acid limitation hypothesis. Marine Ecology Progress Series 315: 1–11.

    Article  CAS  Google Scholar 

  • Lu, Y., S.A. Ludsin, D.L. Fanslow, and S.A. Pothoven. 2008. Comparison of three microquantity techniques for measuring total lipids in fish. Canadian Journal of Fisheries and Aquatic Sciences 65 (10): 2233–2241.

    Article  CAS  Google Scholar 

  • MacPherson, J.C., J.G. Pavlovich, and R.S. Jacobs. 1998. Phospholipid composition of the granular amebocyte from the horseshoe crab, Limulus polyphemus. Lipids 33 (9): 931–940.

    Article  CAS  Google Scholar 

  • Mayzaud, P., J.P. Chanut, and R.G. Ackman. 1989. Seasonal changes of the biochemical composition of marine particulate matter with special reference to fatty acids and sterols. Marine Ecology Progress Series 56: 189–204.

    Article  CAS  Google Scholar 

  • Meng, L., C. Gray, B. Taplin, and E. Kupcha. 2000. Using winter flounder growth rates to assess habitat quality in Rhode Island’s coastal lagoons. Marine Ecology Progress Series 201: 287–299.

    Article  Google Scholar 

  • Miller, J.A., W.T. Peterson, L.A. Copeman, X. Du, C.A. Morgan, and M.N.C. Litz. 2017. Temporal variation in the biochemical ecology of lower trophic levels in the northern California current. Progress in Oceanography 155: 1–12.

    Article  Google Scholar 

  • Parrish, C.C. 1987. Separation of aquatic lipid classes by chromarod thin-layer chromatography with measurement by Iatroscan flame ionization detection. Canadian Journal of Fisheries and Aquatic Sciences 44 (4): 722–731.

    Article  CAS  Google Scholar 

  • Parrish, C.C. 2013. Lipids in marine ecosystems. ISRN Oceanography 2013: 1–16.

    Article  CAS  Google Scholar 

  • Pepin, P., and J.F. Dower. 2007. Variability in the trophic position of larval fish in a coastal pelagic ecosystem based on stable isotope analysis. Journal of Plankton Research 29 (8): 727–737.

    Article  CAS  Google Scholar 

  • Peterson, B.J., and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18 (1): 293–320.

    Article  Google Scholar 

  • Post, D.M., C.A. Layman, D.A. Arrington, G. Takimoto, J. Quattrochi, and C.G. Montaña. 2007. Getting to the fat of the matter: Models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152 (1): 179–189.

    Article  Google Scholar 

  • Rooper, C.N., D.R. Gunderson, and D.A. Armstrong. 2003. Patterns in use of estuarine habitat by juvenile English sole (Pleuronectes vetulus) in four eastern North Pacific estuaries. Estuaries 26 (4B): 1142–1154.

    Article  Google Scholar 

  • Rosenberg, A.A. 1982. Growth of juvenile English sole, Parophrys vetulus, in estuarine and open coastal nursery grounds. Fishery Bulletin 80: 245–252.

    Google Scholar 

  • Ryer, C.H., B.J. Laurel, and A.W. Stoner. 2010. Testing the shallow-water refuge hypothesis in flatfish nurseries. Marine Ecology Progress Series 415: 275–282.

    Article  Google Scholar 

  • Ryer, C.H., K.S. Boersma, and T.P. Hurst. 2012. Growth and distributional correlates of behavior in three co-occurring juvenile flatfishes. Marine Ecology Progress Series 460: 183–193.

    Article  Google Scholar 

  • Sargent, J.R., D.R. Tocher, and J.G. Bell. 2002. The lipids. In Fish nutrition, ed. J.E. Halver and R.W. Hardy, 181–259. San Diego: Academic Press.

    Google Scholar 

  • Sheaves, M., R. Baker, I. Nagelkerken, and M. Connolly. 2015. True value of estuarine and coastal nursery: Incorporating complexity and dynamics. Estuaries and Coasts 38 (2): 401–414.

    Article  Google Scholar 

  • Shilla, D. 2014. Chemical and isotopic composition of estuarine organic matter: Implications for the relative contribution and reactivity of anthropogenic sources of organic matter. Advances in Oceanography and Limnology 5 (2): 164–183.

    Article  CAS  Google Scholar 

  • Siddon, E.C., R.A. Heintz, and F.J. Mueter. 2013. Conceptual model of energy allocation in walleye Pollock (Theragra chalcogramma) from age-0 to age-1 in the southeastern Bering Sea. Deep-Sea Research II 94: 140–149.

    Article  Google Scholar 

  • Sogard, S.M. 1997. Size-selective mortality in the juvenile stages of teleost fishes: A review. Bulletin of Marine Science 60: 1129–1157.

    Google Scholar 

  • Sokal, R.R., and F.J. Rohlf. 1969. Biometry: The principles and practice of statistics in biological research. San Francisco: W.H. Freeman.

    Google Scholar 

  • St. John, M.A., and T. Lund. 1996. Lipid biomarkers: Linking the utilization of frontal plankton biomass to enhanced condition of juvenile North Sea cod. Marine Ecology Progress Series 131: 75–85.

    Article  Google Scholar 

  • Suthers, I.M., A. Fraser, and K.T. Frank. 1992. Comparison of lipid, otolith and morphometric condition indices of pelagic juvenile cod Gadus morhua from the Canadian Atlantic. Marine Ecology Progress Series 84: 31–40.

    Article  Google Scholar 

  • Sweeting, C.J., J. Barry, C. Barnes, N.V.C. Polunin, and S. Jennings. 2007. Effects of body size and environment on diet-tissue δ15N fractionation in fishes. Journal of Experimental Marine Biology and Ecology 340 (1): 1–10.

    Article  CAS  Google Scholar 

  • Twining, C.W., J.T. Brenna, N.G. Hairston Jr., and A.S. Flecker. 2016. Highly unsaturated fatty acids in nature: What we know and what we need to learn. Oikos 125 (6): 749–760.

    Article  CAS  Google Scholar 

  • Vinagre, C., J. Salgado, M.J. Costa, and H.N. Cabral. 2008. Nursery fidelity, food web interactions and primary sources of nutrition of the juveniles of Solea solea and S. senegalensis in the Tagus estuary (Portugal): A stable isotope approach. Estuarine, Coastal and Shelf Science 76 (2): 255–264.

    Article  Google Scholar 

  • Walther, B.D., T.S. Elsdon, and B.M. Gillanders. 2010. Interactive effects of food quality, temperature and rearing time on condition of juvenile black bream Acanthopagrus butcheri. Journal of Fish Biology 76 (10): 2455–2468.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Fredrick Prahl for contributing to the study design and data interpretation, Mara Spencer for creating a map of the study area, and Katelyn Bosley for feedback on fatty acid and stable isotope analyses and interpretation. Thanks to Scarlett Arbuckle, Morgan Bancroft, Scott Heppell, Karolin Klinck, Kathryn Sobocinski, and Angie Sremba for help with laboratory and field work. Thanks also to the Colorado Plateau Stable Isotope Laboratory at Northern Arizona University (CPSIL-NAU) for guidance on stable isotope sample preparation. We would also like to thank Dr. Andrew Thurber and anonymous reviewers for critical feedback on this manuscript.

Funding

This work was partially funded by the Center for Coastal Margin Observation and Prediction (CMOP) through NSF Division of Ocean Science cooperative agreement No. 0424602. Further, scholarship support to Michelle Stowell was provided by the Hatfield Marine Science Center through the Mamie Markham Research Award.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michelle A. Stowell.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Matthew D. Taylor

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stowell, M.A., Copeman, L.A. & Ciannelli, L. Variability in Juvenile English Sole Condition Relative to Temperature and Trophic Dynamics Along an Oregon Estuarine Gradient. Estuaries and Coasts 42, 1955–1968 (2019). https://doi.org/10.1007/s12237-019-00621-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-019-00621-2

Keywords

Navigation