Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T21:59:43.008Z Has data issue: false hasContentIssue false
  • English
  • Français

Trophic ecology of the blue shark (Prionace glauca) based on stable isotopes (δ13C and δ15N) and stomach content

Published online by Cambridge University Press:  08 September 2015

Sandra Berenice Hernández-Aguilar ,
Ofelia Escobar-Sánchez ,
Felipe Galván-Magaña  and
Leonardo Andrés Abitia-Cárdenas
Sandra Berenice Hernández-Aguilar
Affiliation:
Centro de Investigaciones Biológicas del Noroeste, S.C., Mar Bermejo #195, Col. Playa Palo de Santa Rita, A.P. 128, La Paz, Baja California Sur, 23090, México
Ofelia Escobar-Sánchez
Affiliation:
Universidad Autónoma de Sinaloa-Facultad de Ciencias del Mar. Paseo Claussen s/n, Col. Los Pinos, Mazatlán, Sinaloa, 82000, México
Felipe Galván-Magaña*
Affiliation:
Instituto Politécnico Nacional. Centro Interdisciplinario de Ciencias Marinas . Av. Instituto Politécnico Nacional s/n, La Paz, Baja California Sur, 23096, México
Leonardo Andrés Abitia-Cárdenas
Affiliation:
Instituto Politécnico Nacional. Centro Interdisciplinario de Ciencias Marinas . Av. Instituto Politécnico Nacional s/n, La Paz, Baja California Sur, 23096, México
*
Correspondence should be addressed to:F. Galván-Magaña, Instituto Politécnico Nacional. Centro Interdisciplinario de Ciencias Marinas . Av. Instituto Politécnico Nacional s/n, La Paz, Baja California Sur, 23096, México email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Occupying the upper levels of trophic webs and thus regulating prey at lower levels, sharks play an important role in the trophic structure and energy dynamics of marine ecosystems. In recent years, the removal of these individuals from upper trophic levels as a result of overfishing has negatively affected ecosystems. We analysed the diet of blue sharks (Prionace glauca) caught off the west coast of Baja California Sur, Mexico, during the months of February–June in 2001, 2005 and 2006. We employed both stomach content and stable isotope analyses as each method provides distinct yet important information regarding the role of blue sharks in marine food webs, allowing us to estimate the relative contribution of different prey items to this predator's diet. Of the 368 stomachs analysed, 210 contained food (57%) and 158 (43%) were empty. Based on stomach contents and the index of relative importance (IRI), the pelagic red crab (Pleuroncodes planipes) was the most important prey, followed by the squids Gonatus californiensis (34.1%) and Ancistrocheirus lesueurii (10.4%). The mean (±SD) values for δ15N (16.48 ± 0.94‰) and δ13C (−18.48 ± 0.63‰) suggest that blue sharks prefer feeding in oceanic waters. The trophic level based on stomach content analysis was 4.05, while that based on the stable isotope analysis was 3.8, making blue sharks top consumers in the marine ecosystem of Baja California Sur, Mexico.

Keywords

Food habitssharksstomach contentsstable isotopesMexican Pacific
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 7 , November 2016 , pp. 1403 - 1410
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abitia-Cárdenas, L.A., Galván-Magaña, F. and Rodríguez-Romero, J. (1997) Food habits and energy values of prey of striped marlin, Tetrapturus audax, off the coast of Mexico. Fishery Bulletin 95, 360–368.Google Scholar
Amaratunga, T. (1983) The role of cephalopods in the marine ecosystem. Advances in assessment of world cephalopods resources. FAO Fisheries Technical Paper 231, 379–415.Google Scholar
Aurioles-Gamboa, D., Castro-González, M.I. and Pérez-Flores, R. (1994) Annual mass strandings of pelagic red crabs, Pleuroncodes planipes (Crustacea: Anomura: Galatheidae), in Bahia Magdalena, Baja California Sur, Mexico. Fishery Bulletin 92, 464–470.Google Scholar
Blanco-Parra, M.P., Galván-Magaña, F., Marquez-Farías, J.F. and Niño-Torres, C.A. (2011) Feeding ecology and trophic level of the banded guitarfish, Zapteryx exasperata, inferred from stable isotopes and stomach contents analysis. Environmental Biology of Fishes 95, 65–77.Google Scholar
Boecklen, W.J., Yarnes, C.T., Cook, B.A. and James, A.C. (2011) On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution and Systematic 42, 411–440.Google Scholar
Bornatowski, H. and Schwingel, P.R. (2008) Feeding and reproduction of the blue shark, Prionace glauca (Linnaeus, 1758), off Southeastern and Southern Brazil. Arquivos de Ciências do Mar 41, 98–103.Google Scholar
Carrera-Fernández, M., Galván-Magaña, F. and Ceballos-Vázquez, P. (2010) Reproductive biology of the blue shark Prionace glauca (Chondrichthyes: Carcharhinidae) off Baja California Sur, México. Aqua, International Journal of Ichthyology 16, 101–110.Google Scholar
Caut, S., Angulo, E. and Courchamp, F. (2008) Caution on isotopic model use for analyses of consumer diet. Canadian Journal of Zoology 86, 438–445.Google Scholar
Christensen, V. and Pauly, D. (1992) Ecopath II – A software for balancing steady-state ecosystem models and calculating network characteristics. Ecological Modelling 61, 169–185.Google Scholar
Cortés, E. (1999) Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56, 707–717.Google Scholar
Dambacher, J.M., Young, J.W., Olson, R.J., Allain, V., Galván-Magaña, F., Lansdell, M.J., Bocanegra-Castillo, N., Alatorre-Ramírez, V., Cooper, S.P. and Duffy, L.M. (2010) Analyzing pelagic food webs leading to top predators in the Pacific Ocean: a graph-theoretic approach. Progress in Oceanography 86, 152–165.Google Scholar
DeNiro, J. and Epstein, S. (1978) Influence of the diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.Google Scholar
Erhardt, E.B. (2009) SISUS: Stable isotope sourcing using sampling. Retrieved 2009. http://statacumen.com/sisus/.Google Scholar
Escobar-Sánchez, O., Abitia-Cárdenas, L.A. and Galván-Magaña, F. (2006) Food habits of the Pacific angel shark Squatina californica in the southern Gulf of California, Mexico. Cybium 30(suppl.), 91–97.Google 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 Marine Biological Association 83, 1347–1350.Google Scholar
Fry, B. (2006) Stable isotope ecology. New York, NY: Springer.Google Scholar
Fry, B. and Parker, P.L. (1979) Animal diet in Texas seagrass meadows: δ13C evidence for the importance of benthic plants. Estuarine and Coastal Marine Science 8, 499–509.Google Scholar
Froese, R. and Pauly, D. (2015) FishBase. World Wide Web electronic publication. www.fishbase.org, version (02/2015).Google Scholar
Galvan-Magaña, F., Polo-Silva, C., Hernández-Aguilar, S.B., Sandoval-Londoño, A., Ochoa-Díaz, M.R., Aguilar-Castro, N., Castañeda-Suárez, D., Cabrera-Chávez-Costa, A., Baigorrí-Santacruz, A., Torres-Rojas, Y.E. and Abitia-Cárdenas, L.A. (2013) Shark predation on cephalopods in the Mexican and Ecuadorian Pacific Ocean. Deep-Sea Research Part II. Topical Studies in Oceanography 95, 52–62.Google Scholar
Henderson, A.C., Dunne, J. and Flannery, K. (2001) Observations on the biology and ecology of the blue shark in the North-East Atlantic. Journal of Fish Biology 58, 1347–1358.Google Scholar
Hoyos, L., Marquin, G. and Valle, S. (1991) Ecología trófica de Prionace glauca ‘tintorera’, de la costa central del Perú. Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos. http://www.unmsm.edu.pe/biologia/reunion/c1dir606.htm [accessed 15 December 2009]Google Scholar
Hyslop, E. (1980) Stomach contents analysis. A review of methods and their application. Journal of Fish Biology 17, 411–429.Google Scholar
Kim, S.L., Casper, D.R., Galván-Magaña, F., Ochoa-Díaz, R., Hernández-Aguilar, S.B. and Koch, P.L. (2012) Carbon and nitrogen discrimination factors for elasmobranch soft tissues based on a long-term controlled feeding study. Environmental Biology of Fishes 95, 37–52.Google Scholar
Krebs, C. 1989 Ecological methodology. New York, NY: Harper & Row.Google Scholar
Kubodera, T., Watanabe, H. and Ichii, T. (2007) Feeding habits of the blue shark, Prionace glauca, and salmon shark, Lamna ditropis, in the transition region of the Western North Pacific. Reviews in Fish Biology and Fisheries 17, 111–124.Google Scholar
Langton, R.W. (1982) Diet overlap between the Atlantic cod Gadus morhua, silver hake Merluccius bilinearis and fifteen other northwest Atlantic finfish. U. S. National Marine Fisheries Service. Fishery Bulletin 80, 745–759.Google Scholar
Liao, C.H., Pierce, C.L. and Larscheid, J.G. (2001) Empirical assessment of indices of prey importance in the diets of predacious fish. Transactions of the American Fisheries Society 130, 583–591.Google Scholar
López, S., Meléndez, R. and Barría, P. (2010) Preliminary diet analysis of the blue shark Prionace glauca in the eastern South Pacific. Revista de Biología Marina y Oceanografía 45(S1), 745–749.Google Scholar
Markaida, U. and Sosa-Nishizaki, O. (2010) Food and feeding habits of the blue shark Prionace glauca caught off Ensenada, Baja California, Mexico, with a review on its feeding. Journal of the Marine Biological Association of the United Kingdom 90, 1–18.Google Scholar
McCord, M. and Campana, S. (2003) A quantitative assessment of the diet of blue shark (Prionace glauca) of Nova Scotia, Canada. Journal of Northwest Atlantic Fisheries Science 32, 57–63.Google Scholar
Michener, R.H. and Schell, D.M. (1994) Stable isotope ratios as tracers in marine aquatic food webs. In Lajtha, K. and Michener, R.H. (eds) Stable isotopes in ecology and environmental science. Oxford: Blackwell Scientific, pp. 138–157.Google Scholar
Nakano, H. and Stevens, J.D. (2008) The biology of the blue shark, Prionace glauca . In Camhi, M., Pikitch, E.K. and Babcock, E. (eds) Sharks of the open ocean. Oxford: Blackwell Scientific, pp. 140–159.Google Scholar
Newsome, S., Martinez del Rio, C., Bearhop, S. and Phillips, D. (2007) A niche for isotopic ecology. Frontiers in Ecology at the Environment 5, 429–436.Google Scholar
Niño-Torres, C.A., Gallo-Reynoso, J.P., Galván-Magaña, F., Escobar-Briones, E. and Macko, S.A. (2006) Isotopic analysis of δ13C, δ15N and δ34S ‘a feeding tale’ in teeth of the long-beaked common dolphin Delphinus capensis . Marine Mammal Science 22, 831–846.Google Scholar
Ochoa-Díaz, M.R. (2009) Espectro trófico del tiburón martillo Sphyrna zygaena (Linnaeus, 1758) en Baja California Sur: aplicación de δ13C y δ15N . MS thesis. CICIMAR-IPN, La Paz, Mexico.Google Scholar
Pardo-Gandarillas, M.C., Duarte, F., Chong, J. and Ibañez, C.M. (2007) Dieta de tiburones juveniles (Linnaeus, 1758) Prionace glauca (Carcharhiniformes: Carcharhinidae) en la zona litoral centro-sur de Chile. Revista de Biología Marina y Oceanografía 42, 362–369.Google Scholar
Phillips, D.L. and Gregg, J.W. (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136, 261–269.Google Scholar
Pinkas, L., Oliphant, S.M. and Iverson, I.L.K. (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. Fishery Bulletin 152, 105.Google Scholar
Polo-Silva, CJ, Galván-Magaña, F. and Delgado-Huertas, A. (2012) Trophic inferences of blue shark (Prionace glauca) in the Mexican Pacific from stable isotope analysis in teeth. Rapid Communications in Mass Spectrometry 26, 1631–1638.CrossRefGoogle ScholarPubMed
Post, D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumption. Ecology 83, 703–718.Google Scholar
Preti, A., Soykan, C.U., Dewar, H., Wells, R.J.D., Spear, N. and Kohin, S. (2012) Comparative feeding ecology of shortfin mako, blue and thresher sharks in the California Current. Environmental Biology of Fishes 95, 127–146.Google Scholar
Rabehagasoa, N., Lorrain, A., Bach, P., Potier, M., Jaquemet, S., Richard, P. and Ménard, F. (2012) Isotopic niches of the blue shark Prionace glauca and the silky shark Carcharhinus falciformis in the southwestern Indian Ocean. Endangered Species Research 17, 83–92.Google Scholar
Richert, J.E. (2007) Trophic ecology of large pelagic fishes in the southern Gulf of California . PhD thesis. University of California, Davis, USA.Google Scholar
Smith, P.E. and Zaret, M.T. (1982) Bias in estimating niche overlap. Ecology 63, 1248–1253.Google Scholar
Stevens, J. (1976) First results of sharks tagging in the northeast Atlantic, 1972–1975. Journal of the Marine Biological Association of the United Kingdom 56, 929–937.Google Scholar
Tricas, T.C. (1979) Relationships of the blue shark, Prionace glauca and its prey species near Santa Catalina Island, California. Fishery Bulletin 77, 175–182.Google Scholar
Vaske-Junior, T. and Rincon-Filho, A. (1998) Stomach content of blue sharks (Prionace glauca) and anequim (Isurus oxyrinchus) from oceanic waters of Southern Brazil. Revista Brasileira de Biologia 58, 445–452.Google Scholar
Velasco-Tarelo, P.M. (2005) Hábitos alimenticios e isótopos de 13C y 15N del tiburón mako Isurus oxyrinchus (Rafinesque, 1810) en la Costa Occidental de Baja California Sur. MS thesis. CICIMAR-IPN, La Paz, Mexico.Google Scholar