Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
REVIEW

Stable isotope analysis as a tool for elasmobranch conservation research: a primer for non-specialists

D. S. Shiffman A B F , A. J. Gallagher A B , M. D. Boyle C , C. M. Hammerschlag-Peyer D and N. Hammerschlag A B E
+ Author Affiliations
- Author Affiliations

A Leonard and Jayne Abess Center for Ecosystem Science and Policy, University of Miami, PO Box 248202, Coral Gables, FL 33 124, USA.

B RJ Dunlap Marine Conservation Program, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33 149, USA.

C Pacific Shark Research Center, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, CA 95 039, USA.

D Florida International University, 3000 NE 151st Street, North Miami, FL 33 181, USA.

E Rosenstiel School of Marine and Atmospheric Sciences, 4600 Rickenbacker Causeway, Miami, FL 33 149, USA.

F Corresponding author. Email: David.Shiffman@gmail.com

Marine and Freshwater Research 63(7) 635-643 https://doi.org/10.1071/MF11235
Submitted: 24 October 2011  Accepted: 30 April 2012   Published: 2 July 2012

Abstract

Many elasmobranch species are undergoing population declines on a global scale; however, implementation of effective conservation and management strategies is hindered, to a large extent, by a lack of sufficient data on diet, life history and behaviour. This work is a primer of how stable isotope analysis can be used as a cost-effective, relatively simple tool for examining resource use patterns (e.g. diet, habitat) and generating relevant data in support of science-based elasmobranch conservation and management. Specifically, isotopes can resolve the feeding niches of elasmobranchs, detect ontogenetic trophic shifts and calculate relative diet breadth of different species. Stable isotope analysis can also be employed to investigate the extent of anthropogenic impacts on diet or to infer the source of toxins affecting elasmobranchs. Additionally, this tool can be used to study migration patterns and habitat usage. Depending on the tissue analysed, this technique can also be non-lethal and minimally invasive. The limitations of stable isotope analysis are discussed, and recommendations for future work are presented.

Additional keywords: dietary analysis, ecotoxicology, food web analysis, individual diet specialisation, migration.


References

Arrington, A., Winemiller, K., Loftus, W., and Akin, S. (2002). How often do fishes ‘run on empty’? Ecology 83, 2145–2151.

Beaudoin, C. P., and Prepas, E. E. (1999). Individual specialization and trophic adaptability of northern pike (Esox lucius): an isotope and dietary analysis. Oecologia 120, 386–396.
Individual specialization and trophic adaptability of northern pike (Esox lucius): an isotope and dietary analysis.Crossref | GoogleScholarGoogle Scholar |

Ben-David, M., Flynn, R. W., and Schell, D. M. (1997). Annual and seasonal changes in diets of martens: evidence from stable isotope analysis. Oecologia 111, 280–291.
Annual and seasonal changes in diets of martens: evidence from stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |

Benhamou, S. (2004). How to reliably estimate the tortuosity of an animal’s path: straightness, sinuosity, or fractal dimension? Journal of Theoretical Biology 229, 209–220.
How to reliably estimate the tortuosity of an animal’s path: straightness, sinuosity, or fractal dimension?Crossref | GoogleScholarGoogle Scholar |

Bolnick, D. I., Svanback, R., Fordyce, J. A., Yang, L. H., Davis, J. M., and Hulsey, C. D. (2003). The ecology of individuals: incidence and implications of individual specialization. American Naturalist 161, 1–28.
The ecology of individuals: incidence and implications of individual specialization.Crossref | GoogleScholarGoogle Scholar |

Bolnick, D. I., Svanback, R., Araujo, M. S., and Persson, L. (2007). Comparative support for the niche variation hypothesis that more generalized populations are also more heterogeneous. Proceedings of the National Academy of Sciences of the United States of America 104, 10 075–10 079.
Comparative support for the niche variation hypothesis that more generalized populations are also more heterogeneous.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvVGnt7Y%3D&md5=00efe61511f8113c666aa76cb0639cb8CAS |

Bolnick, D. I., Amarasekare, P., Araujo, M. S., Burger, R., Levine, J. M., Novak, M., Rudolf, V. H., Schreiber, S. J., Urban, M. C., and Vasseur, D. A. (2011). Why intraspecific trait variation matters in community ecology. Trends in Ecology & Evolution 26, 183–192.
Why intraspecific trait variation matters in community ecology.Crossref | GoogleScholarGoogle Scholar |

Borrell, A., Aguilar, A., Gazo, M., Kumarran, R. P., and Cardona, L. (2011). Stable isotope profiles in whale shark (Rhincodon typus) suggest segregation and dissimilarities in the diet depending on sex and size. Environmental Biology of Fishes 92, 559–567.
Stable isotope profiles in whale shark (Rhincodon typus) suggest segregation and dissimilarities in the diet depending on sex and size.Crossref | GoogleScholarGoogle Scholar |

Botto, F., Gaitan, E., Mianzan, H., Acha, M., Giberto, D., Schiariti, A., and Iribarne, O. (2011). Origin of resources and trophic pathways in a large SW Atlantic estuary: an evaluation using stable isotopes. Estuarine, Coastal and Shelf Science 92, 70–77.
Origin of resources and trophic pathways in a large SW Atlantic estuary: an evaluation using stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Bowen, G. J., and Revenaugh, J. (2003). Interpolating the isotopic composition of modern meteoric precipitation. Water Resources Research 39, 1299–1312.
Interpolating the isotopic composition of modern meteoric precipitation.Crossref | GoogleScholarGoogle Scholar |

Boyle, M. D., Ebert, D. A., and Cailliet, G. M. (2012). Stable isotope analysis of a deep sea benthic fish assemblage: evidence of an enriched benthic food web. Journal of Fish Biology 80, 1485–1507.
Stable isotope analysis of a deep sea benthic fish assemblage: evidence of an enriched benthic food web.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38rksVOqsg%3D%3D&md5=efe8a66b04f65e089df2b3f320b2c1a3CAS |

Brunnschweiler, J. M., Quieroz, N., and Sims, D. W. (2010). Oceans apart? Short-term movements and behavior of adult bull sharks Carcharhinus leucas in Atlantic and Pacific Oceans determined from pop-off satellite archival tagging. Journal of Fish Biology 77, 1343–1358.
Oceans apart? Short-term movements and behavior of adult bull sharks Carcharhinus leucas in Atlantic and Pacific Oceans determined from pop-off satellite archival tagging.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbjvV2isQ%3D%3D&md5=ea218947d13b88454d2cdaf655a11043CAS |

Bugoni, L., McGill, R., and Furness, R. W. (2010). The importance of pelagic longline fishery discards for a seabird community determined through stable isotope analysis. Journal of Experimental Marine Biology and Ecology 391, 190–200.
The importance of pelagic longline fishery discards for a seabird community determined through stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |

Carlisle, A. B., Kim, S. L., Semmens, B. X., Madigan, D. J., Jorgensen, S. J., Perle, C. R., Anderson, S. D., Chapple, T. K., Kanive, P. E., and Block, B. A. (2012). Using stable isotope analysis to understand the migration and trophic ecology of Northeastern Pacific white sharks. PLoS ONE 7, e30492.
Using stable isotope analysis to understand the migration and trophic ecology of Northeastern Pacific white sharks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtFWitrg%3D&md5=49e5b2065227f96f618bbd543015a337CAS |

Carlson, J. K., Ribera, M. M., Conrath, C. L., Heupel, M. R., and Burgess, G. H. (2010). Habitat use and movement patterns of bull sharks Carcharhinus leucas determined using pop-up satellite archival tags. Journal of Fish Biology 77, 661–675.
| 1:STN:280:DC%2BC3cjktFOntg%3D%3D&md5=b313db2e08e2928f75e47f5c0777bac4CAS |

Cherel, Y., Phillips, R. A., Hobson, K. A., and McGill, R. (2006). Stable isotope evidence of diverse species-specific and individual wintering strategies in seabirds. Biology Letters 2, 301–303.
Stable isotope evidence of diverse species-specific and individual wintering strategies in seabirds.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28jhtVOktQ%3D%3D&md5=eebc165527c922bba13b151af7270afeCAS |

Cherel, Y., Hobson, K. A., Guinet, C., and Vanpe, C. (2007). Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean. Journal of Animal Ecology 76, 826–836.

Cortes, E. (1999). Standardized diet and trophic levels of sharks. ICES Journal of Marine Science 56, 707–717.
Standardized diet and trophic levels of sharks.Crossref | GoogleScholarGoogle Scholar |

Creel, S., and Christianson, D. (2008). Relationships between direct predation and risk effects. Trends in Ecology & Evolution 23, 194–201.
Relationships between direct predation and risk effects.Crossref | GoogleScholarGoogle Scholar |

Davenport, S. R., and Bax, N. J. (2002). A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Canadian Journal of Fisheries and Aquatic Sciences 59, 514–530.
A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen.Crossref | GoogleScholarGoogle Scholar |

DeNiro, M. J., and Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.
Influence of diet on the distribution of carbon isotopes in animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXls1WrsbY%3D&md5=ade4fa89b82da73ad8e6fea7e38179abCAS |

DeNiro, M. J., and Epstein, S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.
Influence of diet on the distribution of nitrogen isotopes in animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktVGmtLw%3D&md5=91fb3d34cfd50525524407925d4fe3a0CAS |

Dennard, S. T., McMeans, B. C., and Fisk, A. T. (2009). Preliminary assessment of Greenland halibut diet in Cumberland Sound using stable isotopes. Polar Biology 32, 941–945.
Preliminary assessment of Greenland halibut diet in Cumberland Sound using stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Domi, N., Bouquegneau, J. M., and Das, K. (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.
Feeding ecology of five commercial shark species of the Celtic Sea through stable isotope and trace metal analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtFCqsbk%3D&md5=58a14b8322fdac8abf73af5c27cb7d4fCAS |

Drymon, J. M., Powers, S. P., and Carmichael, R. P. (2011). Trophic plasticity in the Atlantic sharpnose shark from the north central Gulf of Mexico. Environmental Biology of Fishes , .
Trophic plasticity in the Atlantic sharpnose shark from the north central Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |

Dulvy, N. K., Baum, J. K., Clarke, S., Compagno, L. J., Cortes, E., Domingo, A., Fordham, S., Fowler, S., Francis, M. P., Gibson, C., Martinez, J., Musick, J. A., Soldo, A., Stevens, J. D., and Valenti, S. (2008). You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays. Aquatic Conservation: Marine and Freshwater Ecosystems 18, 459–482.
You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays.Crossref | GoogleScholarGoogle Scholar |

Dunton, K. H., Saupe, S. M., Golikov, N., and Schell, D. M. (1989). Trophic relationships and isotopic gradients among arctic and subarctic marine fauna. Marine Ecology Progress Series 56, 89–97.
Trophic relationships and isotopic gradients among arctic and subarctic marine fauna.Crossref | GoogleScholarGoogle Scholar |

Estrada, J. A., Rice, A. N., Lutcavage, M. E., and Skomal, G. B. (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.
Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpslWjurg%3D&md5=2ff7dcf4031cf4d3a4742f797d3ec19eCAS |

Estrada, J. A., Rice, A. N., Natanson, L. J., and Skomal, G. B. (2006). Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87, 829–834.
Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks.Crossref | GoogleScholarGoogle Scholar |

Fisk, A. T., Tittlemier, S. A., Pranschke, J. L., and Norstrom, R. J. (2002). Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks. Ecology 83, 2162–2172.
Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks.Crossref | GoogleScholarGoogle Scholar |

Fourqurean, J. W., Escorcia, S. P., Anderson, W. T., and Zieman, J. C. (2005). Spatial and seasonal variability in elemental content, δC13, and δN15 of Thalassia testudinum from South Florida and its implications for ecosystem studies. Estuaries 28, 447–461.
Spatial and seasonal variability in elemental content, δC13, and δN15 of Thalassia testudinum from South Florida and its implications for ecosystem studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslSmtb4%3D&md5=54b07885f409bb5c9adb06a7285cdadfCAS |

Fourqurean, J. W., Marba, N., Duarte, C. M., Diaz-Almela, E., and Ruiz-Halpern, S. (2007). Spatial and temporal variation in the elemental and stable isotopic content of the seagrasses Posidonia oceanic and Cymodocea nodosa from the Illes Balears, Spain. Marine Biology 151, 219–232.
Spatial and temporal variation in the elemental and stable isotopic content of the seagrasses Posidonia oceanic and Cymodocea nodosa from the Illes Balears, Spain.Crossref | GoogleScholarGoogle Scholar |

France, R. L. (1995). Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes. Limnology and Oceanography 40, 1310–1313.
Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes.Crossref | GoogleScholarGoogle Scholar |

Fry, B. (1981). Natural stable carbon isotope tag traces Texas shrimp migrations. Fish Bulletin 79, 337–345.

Gallagher, A. J., and Hammerschlag, N. (2011). Global shark currency: the distribution, frequency, and economic value of shark ecotourism. Current Issues in Tourism 4, 797–781.
Global shark currency: the distribution, frequency, and economic value of shark ecotourism.Crossref | GoogleScholarGoogle Scholar |

Gallagher, A. J., Kyne, P. K., and Hammerschlag, N. (2012). Ecological risk assessment and its application to elasmobranch conservation and management. Journal of Fish Biology 80, 1727–1748.
Ecological risk assessment and its application to elasmobranch conservation and management.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38njvFalsg%3D%3D&md5=d30e3f410f5766d594d6f86649e1bd9fCAS |

Gelsleichter, J., Manire, C. A., Szabo, N. J., Cortes, E., Carlson, J., and Lombardi-Carlson, L. (2005). Organochlorine concentrations in Bonnethead sharks (Sphyrna tiburo) from four Florida Estuaries. Archives of Environmental Contamination and Toxicology 48, 474–483.
Organochlorine concentrations in Bonnethead sharks (Sphyrna tiburo) from four Florida Estuaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVaisrg%3D&md5=560655b7392eea84c899651f0f129e68CAS |

Grubbs, R. (2010). Ontogenetic shifts in movement and habitat use. In ‘Sharks and their Relatives II: Biodiversity, Adaptive Physiology, and Conservation’. (Eds J. C. Carrier, J. A. Musick and M. R. Heithaus.) pp. 319–350. (CRC Press: Boca Raton, FL.)

Hammerschlag, N., and Sulikowski, J. (2011). Killing for conservation: the need for alternatives to lethal sampling of apex-predatory sharks. Endangered Species Research 14, 135–140.
Killing for conservation: the need for alternatives to lethal sampling of apex-predatory sharks.Crossref | GoogleScholarGoogle Scholar |

Hammerschlag, N., Gallagher, A. J., and Lazarre, D. M. (2011). A review of shark satellite tagging studies. Journal of Experimental Marine Biology and Ecology 386, 125–132.

Hammerschlag-Peyer, C. M., and Layman, C. A. (2010). Intrapopulation variation in habitat use by two abundant coastal fish species. Marine Ecology Progress Series 415, 211–220.
Intrapopulation variation in habitat use by two abundant coastal fish species.Crossref | GoogleScholarGoogle Scholar |

Harrington, R. R., Kennedy, B. P., Chamberlain, C. P., Blum, J. D., and Folt, C. L. (1998). δ15N enrichment in agricultural catchments: field patterns and applications to tracking Atlantic salmon (Salmo salar). Chemical Geology 147, 281–294.
δ15N enrichment in agricultural catchments: field patterns and applications to tracking Atlantic salmon (Salmo salar).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjslGlsLg%3D&md5=1c5e4298e3cc43395c80b0cd0a3e0c03CAS |

Heithaus, M. R., Frid, A., Wirsing, A. J., and Worm, B. (2008). Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution 23, 202–210.
Predicting ecological consequences of marine top predator declines.Crossref | GoogleScholarGoogle Scholar |

Heupel, M., and Simpfendorfer, C. (2010). Science or slaughter: need for lethal sampling of sharks. Conservation Biology 24, 1212–1218.
Science or slaughter: need for lethal sampling of sharks.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M%2Fps1Srtw%3D%3D&md5=d737d7c7f2f1bbb069c2d20fc887bf13CAS |

Hobson, K. A. (1999). Tracing origins and migration of wildlife using stable isotopes: a review. Wildlife Research 120, 314–326.

Hobson, K. A., and Clark, R. W. (1992). Assessing avian diets using stable isotopes. 1: Turnover over 13C in tissues. The Condor 94, 181–188.
Assessing avian diets using stable isotopes. 1: Turnover over 13C in tissues.Crossref | GoogleScholarGoogle Scholar |

Hobson, K. A., Hughes, K. D., and Ewins, P. J. (1997). Using stable isotope analysis to identify endogenous and exogenous sources of nutrients in eggs of migratory birds: applications to Great Lakes contaminants research. The Auk 114, 467–478.

Hostynek, J. J., and Maibach, H. I. (2006). Skin penetration by metal compounds with special reference to copper. Toxicology Mechanisms and Methods 16, 245–265.
Skin penetration by metal compounds with special reference to copper.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlyitLo%3D&md5=eac87fba3bca4e7ab79462b3f00c2225CAS |

Hussey, N. E., Brush, J., McCarthy, I. D., and Fisk, A. T. (2010a). δ15N and δ13C diet-tissue discrimination factors for large sharks under semi-controlled conditions. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 155, 445–453.
δ15N and δ13C diet-tissue discrimination factors for large sharks under semi-controlled conditions.Crossref | GoogleScholarGoogle Scholar |

Hussey, N. E., MacNeil, M. A., and Fisk, A. T. (2010b). The requirement for accurate diet-tissue discrimination factors for interpreting stable isotopes in sharks: comment on stable isotope dynamics in elasmobranch fishes. Hydrobiologia 654, 1–5.
The requirement for accurate diet-tissue discrimination factors for interpreting stable isotopes in sharks: comment on stable isotope dynamics in elasmobranch fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqt7zO&md5=bf94bc79008aa2f18faf426b3de5ccecCAS |

Hussey, N. E., Dudley, S. F., McCarthy, I. D., Cliff, G., and Fisk, A. T. (2011). Stable isotope profiles of large marine predators: viable indicators of trophic position, diet, and movement in sharks? Canadian Journal of Fisheries and Aquatic Sciences 68, 2029–2045.
Stable isotope profiles of large marine predators: viable indicators of trophic position, diet, and movement in sharks?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xns12htA%3D%3D&md5=02ec5626b94e46d1f6769d2892300bfeCAS |

Hyslop, E. (1980). Stomach contents analysis: a review of methods and applications. Journal of Fish Biology 17, 411–429.
Stomach contents analysis: a review of methods and applications.Crossref | GoogleScholarGoogle Scholar |

Jackson, A. L., Inger, R., Parnell, A. C., and Bearhop, S. (2011). Comparing isotopic niche widths among and within communities: SIBER- stable isotope Bayesian ellipses in R. Journal of Animal Ecology 80, 595–602.
Comparing isotopic niche widths among and within communities: SIBER- stable isotope Bayesian ellipses in R.Crossref | GoogleScholarGoogle Scholar |

Jardine, T., and Kidd, A. F. (2006). Applications, considerations, and sources of uncertainty when using stable isotope analysis in ecotoxicology. Environmental Science & Technology 40, 7501–7511.
Applications, considerations, and sources of uncertainty when using stable isotope analysis in ecotoxicology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFWnurfK&md5=5beeeb0372212576baff3025285acb7aCAS |

Jennings, S., Greenstreet, S., Hill, L., Piet, G., Pinnegar, J., and Warr, K. J. (2002). Long-term trends in the trophic structure of the North Sea fish community: evidence from stable-isotope analysis, size-spectra and community metrics. Marine Biology 141, 1085–1097.
Long-term trends in the trophic structure of the North Sea fish community: evidence from stable-isotope analysis, size-spectra and community metrics.Crossref | GoogleScholarGoogle Scholar |

Killingley, J. S., and Lutcavage, M. (1983). Loggerhead turtle movements reconstructed from 180 and 13C profiles from commensal barnacle shells. Estuarine, Coastal and Shelf Science 16, 345–349.
Loggerhead turtle movements reconstructed from 180 and 13C profiles from commensal barnacle shells.Crossref | GoogleScholarGoogle Scholar |

Kim, S. L., Casper, D. R., Galván-Magaña, F., Ochoa-Díaz, R., Hernández-Aguilar, S. B., and Koch, P. L. (2011). Carbon and nitrogen discrimination factors for elasmobranch soft tissues based on a long-term controlled feeding study. Environmental Biology of Fishes , .
Carbon and nitrogen discrimination factors for elasmobranch soft tissues based on a long-term controlled feeding study.Crossref | GoogleScholarGoogle Scholar |

Kohler, N. E., and Turner, P. A. (2001). Shark tagging: a review of conventional methods and studies. Environmental Biology of Fishes 60, 191–224.
Shark tagging: a review of conventional methods and studies.Crossref | GoogleScholarGoogle Scholar |

Layman, C. A., and Post, D. M. (2008). Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 89, 2358–2359.
Can stable isotope ratios provide for community-wide measures of trophic structure?Crossref | GoogleScholarGoogle Scholar |

Layman, C. A., Albrey-Arrington, D., Montana, C., and Post, D. M. (2007). Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88, 42–48.
Can stable isotope ratios provide for community-wide measures of trophic structure?Crossref | GoogleScholarGoogle Scholar |

Layman, C. A., Araujo, M. S., Boucek, R., Hammerschlag-Peyer, C. M., Harrison, E., Jud, Z. R., Matich, P., Rosenblatt, A., Vaudo, J. J., and Yeager, L. A. (2012). Applying stable isotopes to examine food web structure: an overview of analytical tools. Biological Reviews of the Cambridge Philosophical Society , .

Logan, J. M., and Lutcavage, M. E. (2010a). Stable isotope dynamics in elasmobranch fishes. Hydrobiologia 644, 231–244.
Stable isotope dynamics in elasmobranch fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvFagt7o%3D&md5=4826f9c5ee2983b1e6b3f9efb262f30aCAS |

Logan, J. M., and Lutcavage, M. E. (2010b). Reply to Hussey et al.: the requirement for accurate diet-tissue discrimination factors for interpreting stable isotopes in sharks. Hydrobiologia 654, 7–12.
Reply to Hussey et al.: the requirement for accurate diet-tissue discrimination factors for interpreting stable isotopes in sharks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqt7zI&md5=fc9ad8d5edd499e08b5ddbfda063edd4CAS |

Lucifora, L. O., Garcia, V. b., Menni, R. C., Escalante, A. H., and Hozbor, N. M. (2009). Effects of body size, age, and maturity stage on diet in a large shark: ecological and applied implications. Ecological Research 24, 109–118.
Effects of body size, age, and maturity stage on diet in a large shark: ecological and applied implications.Crossref | GoogleScholarGoogle Scholar |

Lucifora, L. O., Garcia, V. B., and Worm, B. (2011). Global diversity hotspots and conservation priorities for sharks. PLoS ONE 6, e19356.
Global diversity hotspots and conservation priorities for sharks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtFWisLY%3D&md5=30c66a1373a8146cba5eff7a7e9a3b51CAS |

MacNeil, M. A., Skomal, G. B., and Fisk, A. T. (2005). Stable isotopes from multiple tissues reveal diet switching in sharks. Marine Ecology Progress Series 302, 199–206.
Stable isotopes from multiple tissues reveal diet switching in sharks.Crossref | GoogleScholarGoogle Scholar |

MacNeil, M. A., Drouillard, K. G., and Fisk, A. T. (2006). Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Canadian Journal of Fisheries and Aquatic Sciences 63, 345–353.
Variable uptake and elimination of stable nitrogen isotopes between tissues in fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivVSgsLw%3D&md5=fe0871b7dd96b7280f052cae96f0a135CAS |

Magurran, A. E. (1986). Individual differences in fish behaviour. In ‘The Behaviour of Teleost Fishes’. (Ed. T. J. Pitcher.) pp. 338–365. (Croom Helm; London.)

Maljković, A., and Côté, I. M. (2011). Effects of tourism-related provisioning on the trophic signatures and movement patterns of an apex predator, the Caribbean reef shark. Biological Conservation 144, 859–865.
Effects of tourism-related provisioning on the trophic signatures and movement patterns of an apex predator, the Caribbean reef shark.Crossref | GoogleScholarGoogle Scholar |

Marra, P. P., Hobson, K. A., and Holmes, R. T. (1998). Linking winter and summer events in a migratory bird by using stable carbon isotopes. Science 282, 1884–1886.
Linking winter and summer events in a migratory bird by using stable carbon isotopes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVWis7w%3D&md5=17901e9fbba880600c4aada681066dd5CAS |

Martinez del Rio, C., Wolf, N., Carleton, S. A., and Gannes, L. Z. (2009). Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84, 91–111.

Matich, P., Heithaus, M. R., and Layman, C. A. (2010). Size-based variation in intertissue comparisons of stable carbon and nitrogen isotopic signatures of bull sharks (Carcharhinus leucas) and tiger sharks (Galeocerdo cuvier). Canadian Journal of Fisheries and Aquatic Sciences 67, 877–885.
Size-based variation in intertissue comparisons of stable carbon and nitrogen isotopic signatures of bull sharks (Carcharhinus leucas) and tiger sharks (Galeocerdo cuvier).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFWitrc%3D&md5=d13c417807ec0247e1ab39625e0f9e31CAS |

Matich, P., Heithaus, M. R., and Layman, C. A. (2011). Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. Journal of Animal Ecology 80, 294–305.
Contrasting patterns of individual specialization and trophic coupling in two marine apex predators.Crossref | GoogleScholarGoogle Scholar |

Matthews, B., and Mazumder, A. (2004). A critical evaluation of intrapopulation variation of δ13C and isotopic evidence of individual specialization. Oecologia 140, 361–371.
A critical evaluation of intrapopulation variation of δ13C and isotopic evidence of individual specialization.Crossref | GoogleScholarGoogle Scholar |

McMeans, B. C., Olin, J. A., and Benz, G. W. (2009). Stable-isotope comparisons between embryos and mothers of a placentatrophic shark species. Journal of Fish Biology 75, 2464–2474.
Stable-isotope comparisons between embryos and mothers of a placentatrophic shark species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXislagsL0%3D&md5=a52ff4286dbf7bb19db9f073b2a2ad4bCAS |

McMeans, B. C., Svavarsson, J., Dennard, S., and Fisk, A. T. (2010). Diet and resource use among Greenland sharks (Somniosus microcephalus) and teleosts sampled in Icelandic waters, using δ13C, δ15N, and mercury. Canadian Journal of Fisheries and Aquatic Sciences 67, 1428–1438.
Diet and resource use among Greenland sharks (Somniosus microcephalus) and teleosts sampled in Icelandic waters, using δ13C, δ15N, and mercury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVKhtr3J&md5=8241368dccee1ae56e95553b16714f4eCAS |

Moore, J. W., and Semmens, B. X. (2008). Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11, 470–480.
Incorporating uncertainty and prior information into stable isotope mixing models.Crossref | GoogleScholarGoogle Scholar |

Nathan, R., Getz, W. M., Revilla, R., Holyoak, M., Kadmon, R., Saltz, D., and Smouse, P. E. (2008). A movement ecology paradigm for unifying organismal movement research. Proceedings of the National Academy of Sciences of the United States of America 105, 19 052–19 059.
A movement ecology paradigm for unifying organismal movement research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFamurfP&md5=1fabdfe209145895e75dd5923eff4b58CAS |

Nelson, C. S., Northcote, T. G., and Hendy, C. H. (1989). Potential use of oxygen and carbon isotopic composition of otoliths to identify migratory and non-migratory stocks of the New Zealand common smelt: a pilot study. New Zealand Journal of Marine and Freshwater Research 23, 337–344.
Potential use of oxygen and carbon isotopic composition of otoliths to identify migratory and non-migratory stocks of the New Zealand common smelt: a pilot study.Crossref | GoogleScholarGoogle Scholar |

Newsome, S. D., del Rio, C. M., Bearhop, S., and Phillips, D. L. (2007). A niche for isotopic ecology. Frontiers in Ecology and the Environment 5, 429–436.

Olin, J. A., Hussey, N. E., Fritts, M., Heupel, M. R., Simpfendorfer, C. A., Poulakis, G. R., and Fisk, A. T. (2011). Maternal meddling in neonatal sharks: implications for interpreting stable isotopes in young animals. Rapid Communications in Mass Spectrometry 25, 1008–1016.
| 1:CAS:528:DC%2BC3MXktFWqsb0%3D&md5=f2639627220b65da73059a829e57881aCAS |

Owens, N. J. P. (1988). Natural variations in 15N in the marine environment. Advances in Marine Biology 24, 389–451.
Natural variations in 15N in the marine environment.Crossref | GoogleScholarGoogle Scholar |

Peterson, B., and Fry, B. (1987). Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293–320.
Stable isotopes in ecosystem studies.Crossref | GoogleScholarGoogle Scholar |

Peterson, B. J., and Howarth, R. W. (1987). Sulfur, carbon and nitrogen isotopes used to trace organic matter flow in the salt-marsh estuaries of Sapelo Island, Georgia. Limnology and Oceanography 32, 1195–1213.
Sulfur, carbon and nitrogen isotopes used to trace organic matter flow in the salt-marsh estuaries of Sapelo Island, Georgia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXotFGguw%3D%3D&md5=4bd1dfa7ffa9d791c7476e63a30106b9CAS |

Phillips, D. L. (2001). Mixing models in analyses of diet using multiple stable isotopes: a critique. Oecologia 127, 166–170.
Mixing models in analyses of diet using multiple stable isotopes: a critique.Crossref | GoogleScholarGoogle Scholar |

Phillips, D. L., and Gregg, J. W. (2003). Source partitioning using stable isotopes: coping with too many sources. Oecologia 136, 261–269.
Source partitioning using stable isotopes: coping with too many sources.Crossref | GoogleScholarGoogle Scholar |

Phillips, D. L., Newsome, S. D., and Gregg, J. W. (2005). Combining sources in stable isotope mixing models: alternative methods combining sources alternative methods in stable isotope mixing models. Oecologia 144, 520–527.
Combining sources in stable isotope mixing models: alternative methods combining sources alternative methods in stable isotope mixing models.Crossref | GoogleScholarGoogle Scholar |

Pikitch, E. K., Santora, C., Babcock, E. A., Bakun, A., Bonfil, R., Conover, D. O., Dayton, P., Doukakis, P., Fluharty, D., Beneman, B., Houde, E. D., Link, J., Livingston, P. A., Mangel, M., McAllister, M. K., Pope, J., and Sainsbury, K. J. (2004). Ecosystem-based fishery management. Science 305, 346–347.
Ecosystem-based fishery management.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2czlsVWqsw%3D%3D&md5=7472a3b33ad5ecc6a187161a9f3ff40aCAS |

Pinnegar, J. K., Jennings, S., O’Brien, C. M., and Polunin, N. V. C. (2002). Long-term changes in the trophic level of the Celtic Sea fish community and fish market price distribution. Journal of Applied Ecology 39, 377–390.
Long-term changes in the trophic level of the Celtic Sea fish community and fish market price distribution.Crossref | GoogleScholarGoogle Scholar |

Polunin, N. V. C., Morales-Nin, B., Pawsey, W. E., Cartes, J. E., Pinnegar, J. K., and Moranta, J. (2001). Feeding relationships in Mediterranean bathyal assemblages elucidated by stable nitrogen and carbon isotope data. Marine Ecology Progress Series 220, 13–23.
Feeding relationships in Mediterranean bathyal assemblages elucidated by stable nitrogen and carbon isotope data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpt1Gqu7w%3D&md5=6739a3ef4ea8eb9d73e488785b767fa3CAS |

Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.
Using stable isotopes to estimate trophic position: models, methods, and assumptions.Crossref | GoogleScholarGoogle Scholar |

Post, D. M. (2003). Individual variation in the timing of ontogenetic niche shifts in largemouth bass. Ecology 84, 1298–1310.
Individual variation in the timing of ontogenetic niche shifts in largemouth bass.Crossref | GoogleScholarGoogle Scholar |

Rawson, A. J., Bradley, J. P., Teetsov, A., Rice, S. B., Haller, E. M., and Patton, G. W. (1995). A role for airborne particulates in high mercury levels of some cetaceans. Ecotoxicology and Environmental Safety 30, 309–314.
A role for airborne particulates in high mercury levels of some cetaceans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlt1Gmurc%3D&md5=944e224db654fbb7f54e4b27902dec9bCAS |

Revill, A. T., Young, J. W., and Lansdell, M. (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.
Stable isotopic evidence for trophic groupings and bio-regionalization of predators and their prey in oceanic waters off eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Sampson, L., Galvan-Magana, F., de Silva-Davila, R., Aguiniga-Garcia, S., and O’Sullivan, J. B. (2010). Diet and trophic position of the devil rays Mobula thurstoni and Mobula japanica as inferred from stable isotope analysis. Journal of the Marine Biological Association of the United Kingdom 90, 969–976.
Diet and trophic position of the devil rays Mobula thurstoni and Mobula japanica as inferred from stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |

SEDAR (2006). 11 Stock Assessment Report: large coastal shark complex, blacktip, and sandbar sharks. NOAA National Marine Fisheries Service, Highly Migratory Species Division, Silver Spring, MD.

Semeniuk, C. A., Bourgeon, S., Smith, S. L., and Rothley, K. D. (2009). Hematological differences between stingrays at tourist and non-visited sites suggest physiological costs of wildlife tourism. Biological Conservation 142, 1818–1829.
Hematological differences between stingrays at tourist and non-visited sites suggest physiological costs of wildlife tourism.Crossref | GoogleScholarGoogle Scholar |

Shiffman, D. (2011). Feeding ecology of the sandbar shark (Carcharhinus plumbeus) in South Carolina estuaries using δ13C and δ15N stable isotope analysis. MS thesis. College of Charleston.

Shurdak, M. E., and Gruber, S. H. (1989). Gastric evacuation of the lemon shark Negaprion brevirostris under controlled conditions. Journal of Experimental Biology 48, 77–82.

Simpfendorfer, C. A., Heupel, M. R., White, W. T., and Dulvy, N. K. (2011). The importance of research and public opinion to conservation management of sharks and rays: a synthesis. Marine and Freshwater Research 62, 518–527.
The importance of research and public opinion to conservation management of sharks and rays: a synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFantbs%3D&md5=6b4e066265730d330b1b7d87ad1207b8CAS |

Sims, D. W. (2010). Tracking and analysis techniques for understanding free-ranging shark movements and behavior. In ‘Sharks and their Relatives II: Biodiversity, Adaptive Physiology, and Conservation’. (Eds J. Carrier, D. Musick and M. Heithaus.) pp. 341–392. (CRC Press: Boca Raton, FL.)

Solomon, C. T., Cole, J. J., Doucett, R. R., Pace, M. L., Preston, N. D., Smith, L. E., and Weidel, B. C. (2009). The influence of environmental water on the hydrogen stable isotope ratio in aquatic consumers. Oecologia 161, 313–324.
The influence of environmental water on the hydrogen stable isotope ratio in aquatic consumers.Crossref | GoogleScholarGoogle Scholar |

Turner, T. F., Collyer, M. L., and Krabbenhoft, T. J. (2010). A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91, 2227–2233.
A general hypothesis-testing framework for stable isotope ratios in ecological studies.Crossref | GoogleScholarGoogle Scholar |

Vaudo, J., and Heithaus, M. (2011). Dietary niche overlap in a nearshore elasmobranch mesopredator community. Marine Ecology Progress Series 425, 247–260.
Dietary niche overlap in a nearshore elasmobranch mesopredator community.Crossref | GoogleScholarGoogle Scholar |

Vaudo, J. J., Matich, P., and Heithaus, M. R. (2010). Mother-offspring isotope fractionation in two species of placentatrophic sharks. Journal of Fish Biology 77, 1724–1727.
Mother-offspring isotope fractionation in two species of placentatrophic sharks.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbnt1Sitg%3D%3D&md5=60cdef21877a9accc3959840537833f9CAS |

Wolf, N., Carleton, S. A., and Martinez del Rio, C. (2009). Ten years of experimental animal isotope ecology. Functional Ecology 23, 17–26.
Ten years of experimental animal isotope ecology.Crossref | GoogleScholarGoogle Scholar |

Ziegler, H. (1989). Hydrogen isotope fractionation in plant tissues. In ‘Stable Isotopes in Ecological Research’. (Eds P. W. Rundel, J. R. Ehleringer and K. A. Nagy.) pp. 105–123. (Springer: New York.)