Feeding and migration habits of white shark Carcharodon carcharias (Lamniformes: Lamnidae) from Isla Guadalupe inferred by analysis of stable isotopes δ15N and δ13C;Hábitos alimenticios y migratorios del tiburón blanco Carcharodon carcharias (Lamniformes: Lamnidae) de Isla Guadalupe inferidos por el análisis de isótopos estables de δ15N and δ13C

Revista de Biologia Tropical

Volumn 62, Issue 2, 2014, Pages 637-647

  Jaime Rivera, Mario ^a   Caraveo Patiño, Javier ^a   Hoyos Padilla, Mauricio ^b   Galván Magaña, Felipe ^c  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS DEL NOROESTE   (Mexico)

^b Pelagios Kakunja A C   (Mexico)

^c INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

Author keywords

Feeding habits; Isla Guadalupe; Mixing models; Pinnipeds; Stable isotopes; White shark

Indexed keywords

CARBON; NITROGEN;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; FEEDING BEHAVIOR; METABOLISM; PHYSIOLOGY; POPULATION MIGRATION; SHARK; SKELETAL MUSCLE;

ANIMAL MIGRATION; ANIMALS; CARBON ISOTOPES; FEEDING BEHAVIOR; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; NITROGEN ISOTOPES; SHARKS;

EID: 84901054485     PISSN: 00347744     EISSN: 22152075     Source Type: Journal    
DOI: 10.15517/rbt.v62i2.7767     Document Type: Article

References (58)

1. Ainley, D. G., Strong, C. S. Huber, H. R. Lewis, T. J., & Morrell, S. H. (1981). Predation by sharks on pinnipeds at the Farallon Islands. Fishery Bulletin, 78, 941-945.
2. Ainley, D. G., Henderson, R. P., Huber, H. R., Boekelheide, R. J., Allen, S. G., & McElroy, T. L. (1985). Dynamics of white shark/pinniped interactions in the Gulf of the Farallones. Memoirs of the California Academy of Sciences, 9, 109-122.
3. Aurioles-Gamboa, D., & Zavala-González, A. (1994). Algunos factores ecológicos que determinan la distribución y abundancia del lobo marino Zalophus californianus, en el Golfo de California. Ciencias Marinas, 20, 535-553.
4. Ben-David, M., & Schell, D. M. (2001). Mixing models in analyses of diet using multiple stable isotopes: a response. Oecologia, 127,180-184.
5. Bruce, B. (1992). Preliminary observations on the biology of the White Shark, Carcharodon carcharias, in South Australian waters. Marine & Freshwater Research, 43, 1-11.
6. Boggs, C. H., & Ito, R. Y. (1993). Hawaii's pelagic fisheries. Marine Fisheries Review, 55, 69-82.
7. Burton, R. K., & Koch, P. L. (1999). Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds. Oecologia, 119, 578-585.
8. 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., & Block, B. A. (2012). Using Stable Isotope Analysis to Understand the Migration and Trophic Ecology of Northeastern Pacific White Sharks (Carcharodon carcharias). PLoS ONE, 7(2):e30492.
9. Chapple, T. K., Jorgensen, S. J., Anderson, S. D., Kanive, P. E., Klimley, A. P., Botsford, L. W., & Block, B. A. (2011). A first estimate of white shark, Carcharodon carcharias, abundance off Central California. Biology Letters, 7, 581-583.
10. DeNiro, M. J., & Epstein, S. (1981). Influence of the diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta, 45, 341-351.
11. Domeier, M., & Nasby-Lucas, N. (2008). Migration patterns of white sharks Carcharodon carcharias tagged at Isla Guadalupe, Mexico, and identification of an eastern Pacific shared offshore foraging area. Marine Ecology Progress Series, 370, 221-237.
12. Domeier, M. L. (2012). A new Life-History Hypothesis for White Sharks, Carcharodon carcharias, in the Northeastern Pacific. In M. L. Domeier (Eds.), Global Perspectives on the Biology and Life History of the White Shark (pp. 199-223). Florida: CRC Press.
13. Ellis, R., & McCosker, J. E. (1991). Great White Shark. Stanford: Stanford University Press.
14. Estrada, J. A., Rice, A. N., Natanson, L. J., & Skomal, G. B. (2006). Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology, 87, 829-834.
15. Fergusson, I. K., Compagno, L. J. V., & Marks, M. A. (2000). Predation by White Sharks; Carcharodon carcharias; (Chondrichthyes: Lamnidae) Upon Chelonians, with New Records from the Mediterranean Sea and a First Record of the Ocean Sunfish; Mola mola; (Osteichthyes: Molidae) as Stomach Contents. Environmental Biology of Fishes, 5, 447-453.
16. Folch, J., Lees, M., & Stanley, G. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. The Journal of Biological Chemistry 226, 497-509.
17. Gallo-Reynoso, J. P., Figueroa-Carranza, A. L., & Blanco-Parra, M. P. (2004). Shark wounds in the seals of Isla Guadalupe, México. Annual Meeting of the American Elasmobranchs Society. Norman, Oklahoma USA.
18. Galván-Magaña, F., Hoyos-Padilla, E. M., Navarro-Serment, C. J., & Márquez-Farías, F. (2011). Records of white shark, Carcharodon carcharias, in the Gulf of California, Mexico. Marine Biology Records, 3, e111.
19. Graham, B. S., Grubbs, D., Holland, K., & Popp, B. (2007). A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii. Marine Biology, 150, 647-658.
20. Graham, B. S., Koch, P. L., Newsome, S. D., McMahon, K. W., & Aurioles, D. (2010). Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems. In J. B. West, G. Bowen, T. Dawson, & K. Tu (Eds.), Isoscapes: understanding movement, pattern, and process on earth through isotope mapping. (pp. 299-318). New York: Springer-Verlag.
21. Hammerschlag, N., Martin, R. A., & Fallows, C. (2006). Effects of environmental conditions on predator-prey interactions between white sharks (Carcharodon carcharias) and Cape fur seals (Arctocephalus pusillus pusillus) at Seal Island, South Africa. Environmental Biology of Fishes, 76, 341-350.
22. Hobson, K. A., & Clark, R. G. (1992a). Assessing Avian Diets Using Stable Isotopes I: Turnover of 13C in Tissues. The Condor, 94, 181-188.
23. Hobson, K. A., Schell, D. M., Renouf, D., & Noseworthy, E. (1996). Stable carbon and nitrogen fractionation between diet and tissues of captive seals: Implications for dietary reconstructions involving marine mammals. Canadian Journal of Fisheries and Aquatic Sciences, 53, 528-533.
24. Hobson, K. A., & Sease, J. L. (1998). Stable isotope analyses of tooth annuli reveal temporal dietary records: an example using Steller sea lions. Marine Mammal Science, 14, 116-129.
25. Hoyos-Padilla, E. M. (2009). Patrones de movimiento del tiburón blanco (Carcharodon carcharias) en isla Guadalupe, México (Tesis de doctorado, CICIMAR, IPN).
26. Hussey, N. E., Dudley, S. F. J., McCarthy, I. D., Geremy, C., & 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.
27. Itano, D. G. (2000). The reproductive biology of yellowfin tuna (Thunnus albacares) in Hawaiian waters and the western tropic Pacific Ocean: project summary. SOEST 00-01 JIMAR Contribution 00-328. Pelagic Fisheries Research Program, JIMAR, University of Hawaii.
28. Jackson, A. L., Inger, R., Bearhop, S., & Parnell, A. (2009). Erroneous behaviour of MixSIR, a recently published Bayesian isotope mixing model: a discussion of Moore & Semmens (2008). Ecology Letters, 12, E1-E5.
29. Jorgensen, S. J., Reeb, C. A., Chapple, T. K., Anderson, S., Perle, C., Van Sommeran, S. R., Fritz-Cope, C., Brown, A. C., Klimley, A. P., & Block, B. A. (2009). Philopatry and migration of Pacific white sharks. Proceedings of the Royal Society B: Biological Sciences, 277, 679-688.
30. Jorgensen, S. J., Chapple, T. K., Anderson, S., Hoyos, M., Reeb, C., & Block, B. (2012). Connectivity among White Shark Coastal Aggregation Areas in Northeastern Pacific. In M. L. Domeier (Ed.), Global Perspectives on the Biology and Life History of the White Shark (pp. 159-167). Florida: CRC Press.
31. Kennedy, B. P., Blum, J. D., Folt, C. L., & Nislow, K. H. (1997). Natural isotope markers in salmon. Nature, 387, 766-767.
32. Kerr, L. A., Andrews, A. H., Cailliet, G. M., Brown, T. A., & Coale, K. H. (2006). Investigations of Δ14C, δ13C, and δ15N in vertebrae of white shark (Carcharodon carcharias) from the eastern North Pacific Ocean. Environmental Biology of Fishes,77, 337-353.
33. Kim, S. L., Tinker, T., Estes, J. A., & Koch, P. L. (2012a). Ontogenetic and Among-Individual Variation in Foraging Strategies of Northeast Pacific White Sharks Based on Stable Isotope Analysis. PLoS ONE, 7(9), e45068.
34. Kim, S. L., del Rio, C. M. N., Casper, D., & Koch, P. L. (2012b). Isotopic incorporation rates for shark tissues from a long-term captive feeding study. The Journal of Experimental Biology, 215, 2495-2500.
35. Lesage, V., Hammill, M. O., & Kovacs, K. M. (2001). Marine mammals and the community structure of the estuary and gulf of St Lawrence, Canada: evidence from stable isotope analysis. Marine Ecology Progress Series, 210, 203-221.
36. Long, J. D., & Jones, R. (1996). White Shark Predation and Scavening on Cetaceans in the Eastern North Pacific Ocean. In A. P. Klimley & D. G. Ainley (Eds.), Great white sharks: the biology of Carcharodon carcharias (pp. 161-177). San Diego: Academic Press.
37. Malpica-Cruz, L., Herzka, S. Z., Sosa-Nishizaki, O., Lazo, J. P., & Trudel, M. (2012). Tissue-specific isotope trophic discrimination factors and turnover rates in a marine elasmobranch: empirical and modeling results. Canadian Journal of Fisheries and Aquatic Sciences, 69, 551-564.
38. McClellan, C. M., Braun-McNeill, J., Avens, L., Wallace, B. P., & Read, A. J. (2010). Stable isotopes confirm a foraging dichotomy in juvenile loggerhead sea turtles. Journal of Experimental Marine Biology and Ecology, 387, 44-51.
39. Morales-Bojórquez, E., Hernández-Herrera, A., Nevárez-Martínez, M. O., & Díaz-Uribe, J. G. (2012). Population size of the jumbo squid Dosidicus gigas in the central Gulf of California, Mexico, based on markrecapture data. Aquatic Biology, 15, 27-34.
40. Morey, G., Martínez, M., Massutí, E., & Moranta, J. (2003). The Occurrence of White Sharks, Carcharodon carcharias, Around the Balearic Islands (Western Mediterranean Sea). Environmental Biology of Fishes, 68, 425-432.
41. Motta, P. J. (1977). Anatomy and functional morphology of dermal collagen fibres in shark. Copeia, 3, 454-464.
42. Moore, J. W., & Semmens, B. X. (2008). Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters, 11, 470-480.
43. Newsome, S. D., Koch, P. L., Etnier, M. A., & Aurioles-Gamboa, D. (2006). Using carbon and nitrogen isotope values to investigate maternal strategies in northeast Pacific otariids. Marine Mammal Science, 22, 556-572.
44. Okamoto, H., & Bayliff, W. H. (2003). A review of the Japanese longline fishery for tunas and billfishes in the eastern Pacific Ocean, 1993-1997. Inter-american tropical tuna commission bulletin, 22, 221-431.
45. Olson, R. J., Popp, B. N., Graham, B. S., Lopez-Ibarra, G. A., Galván-Magaña, F., Lennert-Cody, C. E., Bocanegra-Castillo, N., Wallsgrove, N. J., Gier, E., Alatorre-Ramirez, V., Balance, L. T., & Fry, B. (2010). Food-web inferences of stable isotope spatial patterns in copepods and yellowfin tuna in the pelagic eastern Pacific Ocean. Progress in Oceanography, 86, 124-138.
46. Parnell, A. C., Inger, R., Bearhop, S., & Jackson, A. L. (2010). Source partitioning using stable isotopes: coping with too much variation. PLoS ONE, 5, e9672.
47. Phillips, D. L., & Gregg, J. W. (2003). Source partitioning using stable isotopes: coping with too many sources. Oecologia, 136, 261-269.
48. Porras-Peters, H., Aurioles-Gamboa, D., Cruz-Escalona, V. H., & Koch, P. L. (2008). Trophic level and overlap of sea lions (Zalophus californianus) in the Gulf of California, Mexico. Marine Mammal Science, 24, 554-576.
49. Post, D., Layman, C., Arrington, D., Takimoto, G., Quattrochi, J., & Montaña, C. (2007). Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia, 152, 179-189.
50. Ruiz-Cooley, R. I., Gendron, D., Aguiñiga, S., Mesnick, S., & Carriquiry, J. D. (2004). Trophic relationships between sperm whales and jumbo squid using stable isotopes of C and N. Marine Ecology Progress Series, 277, 275-283.
51. Schell, D. M., Barnett, B. A., & Vinette, K. A. (1998). Carbon and nitrogen isotope ratios in zooplankton of the Bering, Chukchi and Beaufort seas. Marine Ecology Progress Series, 162, 11-23.
52. Smale, M. J., & Cliff, G. (2012). White sharks and Cephalopod Prey. Indicators of Habitat use? In M. L Domeier (Ed.), Global Perspectives on the Biology and Life History of the White Shark (pp. 51-57). Florida: CRC Press.
53. Tieszen, L. L., Boutton, T. W., Tesdahl, K. G., & Slade, N. A. (1983). Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ13C analysis of diet. Oecologia, 57, 32-37.
54. Tricas, T. C., & McCosker, J. E. (1984). Predatory behaviour of the white shark, Carcharodon carcharias, with notes on its biology. Proceedings of California Academy Science, 43, 221-238.
55. Wcisel, M., Chivelle, W., & Gottfried, M. D. (2010). A potential predation attempt by a great white shark on an Indo-Pacific humpback dolphin. South African Journal of Wildlife Research 40, 184-187.
56. Weng, K., Boustany, A., Pyle, P., Anderson, S., Brown, A., & Block, B. (2007). Migration and habitat of white sharks (Carcharodon carcharias) in the eastern Pacific Ocean. Marine Biology152, 877-894.
57. West, A. G., Goldsmith, G., Brooks, P., & Dawson, T. (2010). Discrepancies between isotope ratio infrared spectroscopy and isotope ratio mass spectrometry for the stable isotope analysis of plant and soil waters. Rapid Communications in Mass Spectrometry 24, 1948-1954.
58. Winn, H. E., Bishoff, W. L., & Tarusky, A. G. (1973). Cytological sexing of Cetacea. Marine Biology 23: 343-346.