Skip to main content
SpringerLink
Log in

Stable isotope dynamics in elasmobranch fishes

  • Primary research paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abelson, P. H. & T. C. Hoering, 1961. Carbon isotope fractionation in formation of amino acids by photosynthetic organisms. Proceedings of the National Academy of Sciences of the United States of America 47: 623–632.

    Article  CAS  PubMed  Google Scholar 

  • Baker, R., P. Blanchfield, M. Paterson, R. Flett & L. Wesson, 2004. Evaluation of nonlethal methods for the analysis of mercury in fish tissue. Transactions of the American Fisheries Society 133: 568–576.

    Article  CAS  Google Scholar 

  • Bearhop, S., M. A. Teece, S. Waldron & R. W. Furness, 2000. Influence of lipid and uric acid on δ13C and δ15N values of avian blood: implications for trophic studies. The Auk 117: 504–507.

    Article  Google Scholar 

  • Best, P. B. & D. M. Schell, 1996. Stable isotopes in southern right whale (Eubalaena australis) baleen as indicators of seasonal movements, feeding and growth. Marine Biology 124: 483–494.

    Article  Google Scholar 

  • Bligh, E. G. & W. J. Dyer, 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37: 911–917.

    CAS  PubMed  Google Scholar 

  • Boag, B., R. Neilson & C. Scrimgeour, 2006. The effect of starvation on the planarian Arthurdendyus triangulatus (Tricladida: Terricola) as measured by stable isotopes. Biology and Fertility of Soils 43: 267–270.

    Article  Google Scholar 

  • Brill, R., P. Bushnell, S. Schroff, R. Seifert & M. Galvin, 2008. Effects of anaerobic exercise accompanying catch-and-release fishing on blood-oxygen affinity of the sandbar shark (Carcharhinus plumbeus, Nardo). Journal of Experimental Marine Biology and Ecology 354: 132–143.

    Article  Google Scholar 

  • Burton, R. & P. Koch, 1999. Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds. Oecologia 119: 578–585.

    Article  Google Scholar 

  • Cain, D., C. Harms & A. Segars, 2004. Plasma biochemistry reference values of wild-caught southern stingrays (Dasyatis americana). Journal of Zoo and Wildlife Medicine 35: 471–476.

    Article  PubMed  Google Scholar 

  • Carey, F. G. & J. M. Teal, 1969. Mako and porbeagle – warm-bodied sharks. Comparative Biochemistry and Physiology 28: 199–204.

    Article  CAS  PubMed  Google Scholar 

  • Carpenter, K. E., 2002. The living marine resources of the Western Central Atlantic. FAO, Rome: 2127 pp.

    Google Scholar 

  • Casey, J., H. Pratt & C. Stillwell, 1985. Age and growth of the sandbar shark (Carcharhinus plumbeus) from the Western North Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 42: 963–975.

    Article  Google Scholar 

  • Cherel, Y., K. Hobson, F. Bailleul & R. Groscolas, 2005. Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86: 2881–2888.

    Article  Google Scholar 

  • Cortés, E., 1999. Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56: 707–717.

    Article  Google Scholar 

  • Demirhan, S. & K. Seyhan, 2007. Life history of spiny dogfish, Squalus acanthias (L. 1758), in the southern Black Sea. Fisheries Research 85: 210–216.

    Article  Google Scholar 

  • Denis, W., 1922. The non-protein organic constituents in the blood of marine fish. The Journal of Biological Chemistry 54: 693–700.

    CAS  Google Scholar 

  • Domi, N., J. M. Bouquegneau & K. Das, 2005. Feeding ecology of five commercial shark species of the Celtic Sea through stable isotope and trace metal analysis. Marine Environmental Research 60: 551–569.

    Article  CAS  PubMed  Google Scholar 

  • Doucett, R. R., R. K. Booth, G. Power & R. S. McKinley, 1999. Effects of the spawning migration on the nutritional status of anadromous Atlantic salmon (Salmo salar): insights from stable-isotope analysis. Canadian Journal of Fisheries and Aquatic Sciences 56: 2172–2180.

    Article  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 

  • Estrada, J. A., A. N. Rice, M. E. Lutcavage & G. B. Skomal, 2003. Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis. Journal of the Marine Biological Association of the United Kingdom 83: 1347–1350.

    Article  CAS  Google Scholar 

  • Estrada, J. A., A. N. Rice, L. J. Natanson & G. B. Skomal, 2006. Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87: 829–834.

    Article  PubMed  Google Scholar 

  • Fisk, A. T., S. A. Tittlemier, J. L. Pranschke & R. J. Norstrom, 2002. Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks. Ecology 83: 2162–2172.

    Article  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.

    CAS  Google Scholar 

  • Fry, B., D. M. Baltz, M. C. Benfield, J. W. Fleeger, A. Gace, H. L. Haas & Z. J. Quiñones-Rivera, 2003. Stable isotope indicators of movement and residency for brown shrimp (Farfantepenaeus aztecus) in coastal Louisiana marshscapes. Estuaries 26: 82–97.

    Article  Google Scholar 

  • Gannes, L. Z., D. M. O’Brien & C. Martínez del Rio, 1997. Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78: 1271–1276.

    Article  Google Scholar 

  • Goldstein, L. & R. Forster, 1971. Osmoregulation and urea metabolism in the little skate, Raja erinacea. American Journal of Physiology 220: 742–746.

    CAS  PubMed  Google Scholar 

  • Guelinckx, J., J. Maes, P. Van Den Driessche, B. Geysen, F. Dehairs & F. Ollevier, 2007. Changes in δ13C and δ15N in different tissues of juvenile sand goby Pomatoschistus minutus: a laboratory diet-switch experiment. Marine Ecology Progress Series 341: 205–215.

    Article  CAS  Google Scholar 

  • Hammerschlag, N., 2006. Osmoregulation in elasmobranchs: a review for fish biologists, behaviourists and ecologists. Marine and Freshwater Behaviour and Physiology 39: 209–228.

    Article  CAS  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.

    Article  CAS  Google Scholar 

  • Hobson, K. A., 1999. Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120: 314–326.

    Article  Google Scholar 

  • Hobson, K. A. & R. G. Clark, 1992. Assessing avian diets using stable isotopes I: turnover of 13C in tissues. The Condor 94: 181–188.

    Article  Google Scholar 

  • Hobson, K. A., R. T. Alisaiskas & R. G. Clark, 1993. Stable nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analysis of diet. The Condor 95: 388–394.

    Article  Google 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.

  • Ip, Y., W. Tam, W. Wong & S. Chew, 2005. Marine (Taeniura lymma) and freshwater (Himantura signifer) elasmobranchs synthesize urea for osmotic water retention. Physiological and Biochemical Zoology 78: 610–619.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Kiljunen, M., J. Grey, T. Sinisalo, C. Harrod, H. Immonen & R. I. Jones, 2006. A revised model for lipid-normalizing δ13C values from aquatic organisms, with implications for isotope mixing models. Journal of Applied Ecology 43: 1213–1222.

    Article  CAS  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.

    CAS  Google Scholar 

  • Logan, J., H. Haas, L. Deegan & E. Gaines, 2006. Turnover rates of nitrogen stable isotopes in the salt marsh mummichog, Fundulus heteroclitus, following a laboratory diet switch. Oecologia 147: 391–395.

    Article  PubMed  Google Scholar 

  • Logan, J., T. Jardine, T. Miller, S. Bunn, R. Cunjak & M. Lutcavage, 2008. Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. Journal of Animal Ecology 77: 838–846.

    Article  PubMed  Google Scholar 

  • MacAvoy, S. E., S. A. Macko & G. C. Garman, 2001. Isotopic turnover in aquatic predators: quantifying the exploitation of migratory prey. Canadian Journal of Fisheries and Aquatic Sciences 58: 923–932.

    Article  CAS  Google Scholar 

  • Macko, S. A., W. Y. Lee & P. L. Parker, 1982. Nitrogen and carbon isotope fractionation by two species of marine amphipods – laboratory and field studies. Journal of Experimental Marine Biology and Ecology 63: 145–149.

    Article  Google Scholar 

  • MacNeill, M. A., G. B. Skomal & A. T. Fisk, 2005. Stable isotopes from multiple tissues reveal diet switching in sharks. Marine Ecology Progress Series 302: 199–206.

    Article  Google Scholar 

  • MacNeil, M. A., K. G. Drouillard & A. T. Fisk, 2006. Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Canadian Journal of Fisheries and Aquatic Sciences 63: 345–353.

    Article  CAS  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 

  • Mathew, S., M. Karthikeyan & B. A. Shamasundar, 2002. Effect of water washing of shark (Scoliodon laticaudus) meat on the properties of proteins with special reference to gelation. Nahrung/Food 46: 78–82.

    Article  CAS  Google Scholar 

  • McClelland, J. W. & J. P. Montoya, 2002. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83: 2173–2180.

    Article  Google Scholar 

  • Merson, R. & H. Pratt, 2001. Distribution, movements and growth of young sandbar sharks, Carcharhinus plumbeus, in the nursery grounds of Delaware Bay. Environmental Biology of Fishes 61: 13–24.

    Article  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 

  • Murry, B. A., J. M. Farrell, M. A. Teece & P. M. Smyntek, 2006. Effect of lipid extraction on the interpretation of fish community trophic relationships determined by stable carbon and nitrogen isotopes. Canadian Journal of Fisheries and Aquatic Sciences 63: 2167–2172.

    Article  CAS  Google Scholar 

  • Nakamura, Y., M. Horinouchi, T. Shibuno, Y. Tanaka, T. Miyajima, I. Koike, H. Kurokura & M. Sano, 2008. Evidence of ontogenetic migration from mangroves to coral reefs by black-tail snapper Lutjanus fulvus: stable isotope approach. Marine Ecology Progress Series 355: 257–266.

    Article  Google Scholar 

  • Park, R. & S. Epstein, 1961. Metabolic fractionation of C13 & C12 in plants. Plant Physiology 36: 133–138.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Phillips, D. & J. Gregg, 2001. Uncertainty in source partitioning using stable isotopes. Oecologia 127: 171–179.

    Article  Google Scholar 

  • Pinnegar, J. K. & N. V. C. Polunin, 1999. Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13: 225–231.

    Article  Google Scholar 

  • Post, D. M., 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703–718.

    Article  Google Scholar 

  • Queiroz, N., F. Lima, A. Maia, P. Ribeiro, J. Correia & A. Santos, 2005. Movement of blue shark, Prionace glauca, in the north-east Atlantic based on mark – recapture data. Journal of the Marine Biological Association of the United Kingdom 85: 1107–1112.

    Article  Google Scholar 

  • R Development Core Team, 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

    Google Scholar 

  • Remme, J., W. Larssen, I. Bruheim, P. Saebo, A. Saebo & I. Stoknes, 2006. Lipid content and fatty acid distribution in tissues from Portuguese dogfish, leafscale gulper shark and black dogfish. Comparative Biochemistry and Physiology 143: 459–464.

    PubMed  Google Scholar 

  • Revill, A., J. Young & M. Lansdell, 2009. Stable isotopic evidence for trophic groupings and bio-regionalization of predators and their prey in oceanic waters off eastern Australia. Marine Biology 156: 1241–1253.

    Article  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 

  • Romine, J., R. Grubbs & J. Musick, 2006. Age and growth of the sandbar shark, Carcharhinus plumbeus, in Hawaiian waters through vertebral analysis. Environmental Biology of Fishes 77: 229–239.

    Article  Google Scholar 

  • Sepulveda, C., J. Graham & D. Bernal, 2007. Aerobic metabolic rates of swimming juvenile mako sharks, Isurus oxyrinchus. Marine Biology 152: 1087–1094.

    Article  CAS  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.

    CAS  Google Scholar 

  • Smith, H. S., 1936. The retention and physiological role of urea in the Elasmobranchii. Biological Reviews 11: 49–82.

    Article  CAS  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.

  • Sotiropoulos, M. A., W. M. Tonn & L. I. Wassenaar, 2004. Effects of lipid extraction on stable carbon and nitrogen isotope analyses of fish tissues: potential consequences for food web studies. Ecology of Freshwater Fish 13: 155–160.

    Article  Google Scholar 

  • Steele, K. W. & R. M. Daniel, 1978. Fractionation of nitrogen isotopes by animals – a further complication to use of variations in natural abundance of 15N for tracer studies. Journal of Agricultural Science 90: 7–9.

    Article  CAS  Google Scholar 

  • Steele, S., P. Yancey & P. Wright, 2005. The little skate Raja erinacea exhibits an extrahepatic ornithine urea cycle in the muscle and modulates nitrogen metabolism during low-salinity challenge. Physiological and Biochemical Zoology 78: 216–226.

    Article  CAS  PubMed  Google Scholar 

  • Sulikowski, J., J. Treberg & H. Howell, 2003. Fluid regulation and physiological adjustments in the winter skate, Leucoraja ocellata, following exposure to reduced environmental salinities. Environmental Biology of Fishes 66: 339–348.

    Article  Google Scholar 

  • Suzuki, K., A. Kasai, K. Nakayama & M. Tanaka, 2005. Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analyzing migration. Canadian Journal of Fisheries and Aquatic Sciences 62: 671–678.

    Article  Google Scholar 

  • Sweeting, C., J. Barry, N. Polunin & S. Jennings, 2007a. Effects of body size and environment on diet-tissue δ13C fractionation in fishes. Journal of Experimental Marine Biology and Ecology 352: 165–176.

    Article  Google Scholar 

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

    Article  CAS  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.

    Article  CAS  PubMed  Google Scholar 

  • Vanderklift, M. A. & S. Ponsard, 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136: 169–182.

    Article  PubMed  Google Scholar 

  • Weng, K., D. Foley, J. Ganong, C. Perle, G. Shillinger & B. Block, 2008. Migration of an upper trophic level predator, the salmon shark Lamna ditropis, between distant ecoregions. Marine Ecology Progress Series 372: 253–264.

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Large Pelagics Research Center, Department of Biological Sciences, University of New Hampshire, 46 College Road, Durham, NH, 03824, USA

    John M. Logan & Molly E. Lutcavage

Authors
  1. John M. Logan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Molly E. Lutcavage
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John M. Logan.

Additional information

Handling editor: M. Power

Rights and permissions

Reprints and permissions

About this article

Cite this article

Logan, J.M., Lutcavage, M.E. Stable isotope dynamics in elasmobranch fishes. Hydrobiologia 644, 231–244 (2010). https://doi.org/10.1007/s10750-010-0120-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-010-0120-3

Keywords

Search

Navigation