Stable isotope dynamics in elasmobranch fishes
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Carbon and nitrogen stable isotope analyses have improved our understanding of food webs and movement patterns of aquatic organisms. These techniques have recently been applied to diet studies of elasmobranch fishes, but isotope turnover rates and isotope diet–tissue discrimination are still poorly understood for this group. We performed a diet switch experiment on captive sandbar sharks (Carcharhinus plumbeus) as a model shark species to determine tissue turnover rates for liver, whole blood, and white muscle. In a second experiment, we subjected captive coastal skates (Leucoraja spp.) to serial salinity reductions to measure possible impacts of tissue urea content on nitrogen stable isotope values. We extracted urea from spiny dogfish (Squalus acanthias) white muscle to test for effects on nitrogen stable isotopes. Isotope turnover was slow for shark tissues and similar to previously published estimates for stingrays and teleost fishes with low growth rates. Muscle isotope data would likely fail to capture seasonal migrations or diet switches in sharks, while liver and whole blood would more closely reflect shorter term movement or shifts in diet. Nitrogen stable isotope values of skate blood and skate and dogfish white muscle were not affected by tissue urea content, suggesting that available diet–tissue discrimination estimates for teleost fishes with similar physiologies would provide accurate estimates for elasmobranchs.
KeywordsNitrogen Sharks Trophic Urea 13C 15N
We thank N. Reynolds, N. Carlson, and W.H. Howell and the staff of the University of New Hampshire Coastal Marine Laboratory and R. Bonniwell, M. Luckenbauch, and the staff of the Virginia Institute of Marine Science Eastern Shore Laboratory for providing facilities and logistical support for both captive experiments. We are especially grateful to D. Prillaman, B. Martin, and all of the staff at Blue Ridge Aquaculture of Martinsville, VA for their generous donation of tilapia as well as M. Walsh and the staff of Normandeau Associates, Inc. for providing skates, and R. Campbell and the staff of the Yankee Fisherman’s Cooperative in Seabrook, NH for providing dogfish. We thank R. Brill, P. Bushnell, L. Pace, L. Litherland, C. Speaks, and T. Nania for assistance with shark sampling and husbandry. We thank R. Doucett, A. Ouimette, and the staff of the Colorado Plateau and University of New Hampshire stable isotope laboratories for assistance with isotope analyses. E. Hobbie, A. Ouimette, S. Bean, and two anonymous reviewers provided valuable comments to earlier drafts of this manuscript. This study complies with current U.S. law, and animal handling methods in this study were approved by the University of New Hampshire and College of William and Mary Institutional Animal Care and Use Committees. This study was funded by NOAA grant no. NA04NMF4550391 to M. Lutcavage.
- Carpenter, K. E., 2002. The living marine resources of the Western Central Atlantic. FAO, Rome: 2127 pp.Google Scholar
- Denis, W., 1922. The non-protein organic constituents in the blood of marine fish. The Journal of Biological Chemistry 54: 693–700.Google Scholar
- Dowd, W., R. Brill, P. Bushnell & J. Musick, 2006. Estimating consumption rates of juvenile sandbar sharks (Carcharhinus plumbeus) in Chesapeake Bay, Virginia, using a bioenergetics model. Fishery Bulletin 104: 332–342.Google Scholar
- Fry, B. & E. B. Sherr, 1984. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contributions to Marine Science 27: 13–47.Google Scholar
- Hansen, P. M., 1963. Tagging experiments with the Greenland shark (Somniosus microcephalus (Bloch and Schneider)) in subarea 1. Special Publication – International Commission for the Northwest Atlantic Fisheries 4: 172–175.Google Scholar
- Hesslein, R. H., K. A. Hallard & P. Ramlal, 1993. Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Canadian Journal of Fisheries and Aquatic Sciences 50: 2071–2076.CrossRefGoogle Scholar
- Holm, S., 1979. A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6: 65–70.Google Scholar
- Hussey, N. E., J. Brush, I. D. McCarthy & A. T. Fisk, 2009. δ15N and δ13C diet-tissue discrimination factors for large sharks under semi-controlled conditions. Comparative Biochemistry and Physiology Part A. doi: 10.1016/j.cbpa.2009.09.023.
- Karnaky, J. K. J., 1998. Osmotic and ionic regulation. In Evans, D. H. (ed.), The Physiology of Fishes, 2nd ed. CRC Press LLC, Boca Raton: 157–176.Google Scholar
- Kriss, M. & L. F. Marcy, 1940. The influence of urea ingestion on the nitrogen balance and energy metabolism of rats. The Journal of Nutrition 19: 151–160.Google Scholar
- Martínez del Rio, C. & B. O. Wolf, 2004. Mass-balance models for animal isotopic ecology. In Starck, J. M. & T. Wang (eds), Physiological consequences of feeding. Springer, Berlin/Heidelberg/New York.Google Scholar
- Michener, R. H. & D. M. Schell, 1994. Stable isotope ratios as tracers in marine aquatic food webs. In Lajtha, K. & R. H. Michener (eds), Stable isotopes in ecology and environmental science. Wiley-Blackwell, Oxford: 138–157.Google Scholar
- R Development Core Team, 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
- Robins, C. R. & G. C. Ray, 1986. A Field Guide to Atlantic Coast Fishes of North America. Houghton Mifflin Company, Boston.Google Scholar
- Skomal, G. & L. Natanson, 2003. Age and growth of the blue shark (Prionace glauca) in the North Atlantic Ocean. Fishery Bulletin 101: 627–639.Google Scholar
- Smith, H. S., 1929. The composition of the body fluids of elasmobranchs. Journal of Biological Chemistry 81: 407–419.Google Scholar
- Smith, M., D. Warmolts, D. Thoney & R. Hueter (eds), 2004. The elasmobranch husbandry manual: captive care of sharks, rays and their relatives. Special Publication of the Ohio Biological Survey: 589 pp.Google Scholar
- Treberg, J. R., B. Speers-Roesch, P. M. Piermarini, Y. K. Ip, J. S. Ballantyne & W. R. Driedzic, 2006. The accumulation of methylamine counteracting solutes in elasmobranchs with differing levels of urea: a comparison of marine and freshwater species. The Journal of Experimental Biology 209: 860–870.CrossRefPubMedGoogle Scholar