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Feeding habits and trophic level of the smooth hammerhead shark, Sphyrna zygaena (Carcharhiniformes: Sphyrnidae), off Ecuador

Published online by Cambridge University Press:  13 July 2018

Colombo Estupiñán-Montaño ,
Luis Cedeño-Figueroa ,
José F. Estupiñán-Ortiz ,
Felipe Galván-Magaña ,
Alejandro Sandoval-Londoño ,
David Castañeda-Suarez  and
Carlos J. Polo-Silva
Colombo Estupiñán-Montaño
Affiliation:
Fundación Alium Pacific, Carrera 26 No. 5C–13, Cali, Colombia Servicio Nacional de Aprendizaje, Centro Agroindustrial y Pesquero de la Costa Pacífica, La Chiricana km 21, Tumaco, Colombia
Luis Cedeño-Figueroa
Affiliation:
Facultad Ciencias del Mar, Universidad Laica “Eloy Alfaro” de Manabí, Manta, Ecuador
José F. Estupiñán-Ortiz
Affiliation:
Fundación Alium Pacific, Carrera 26 No. 5C–13, Cali, Colombia
Felipe Galván-Magaña*
Affiliation:
Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n, La Paz, Baja California Sur, C.P. 23096, Mexico
Alejandro Sandoval-Londoño
Affiliation:
Fundación Alium Pacific, Carrera 26 No. 5C–13, Cali, Colombia Corporación Académica Ambiental, Universidad de Antioquia, Calle 70 No. 52-21, Medellín, Colombia
David Castañeda-Suarez
Affiliation:
Facultad de Ciencias Naturales e Ingeniería, Programa de Biología Marina, Universidad de Bogotá Jorge Tadeo Lozano, Santa Marta, Colombia
Carlos J. Polo-Silva
Affiliation:
Facultad de Ciencias Naturales e Ingeniería, Programa de Biología Marina, Universidad de Bogotá Jorge Tadeo Lozano, Santa Marta, Colombia
*
Correspondence should be addressed to: F. Galván-Magaña, Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n, La Paz, Baja California Sur, C.P. 23096, Mexico email: [email protected]
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Abstract

As apex predators, sharks are known to play an important role in marine food webs. Detailed information on their diet and trophic level is however needed to make clear inferences about their role in the ecosystem. A total of 335 stomachs of smooth hammerhead sharks, Sphyrna zygaena, were obtained from commercial fishing vessels operating in the Ecuadorian Pacific between January and December 2004. A total of 53 prey items were found in the stomachs. According to the Index of Relative Importance (%IRI), cephalopods were the main prey (Dosidicus gigas, Sthenoteuthis oualaniensis, Ancistrocheirus lesueurii and Lolliguncula [Loliolopsis] diomedeae). Sphyrna zygaena was thus confirmed to be a teutophagous species. The estimated trophic level of S. zygaena was between 4.6 and 5.1 (mean ± SD: 4.7 ± 0.16; males: 4.7; females: 4.8). Levin's index (BA) was low (overall: 0.07; males: 0.08; females: 0.09), indicating a narrow trophic niche. We found that sharks <150 cm in total length consumed prey of coastal origin, whereas sharks ≥150 cm foraged in oceanic waters and near the continental shelf. The analyses indicate that S. zygaena is a specialized predator consuming mainly squids.

Keywords

DietEcuadorontogenytop predatorfood webseasonal variations
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 3 , May 2019 , pp. 673 - 680
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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References

REFERENCES

Anderson, M.J. (2001) Permutation tests for univariate or multivariate analysis of variance and regression. Canadian Journal of Fisheries and Aquatic Sciences 58, 626–639.Google Scholar
Avendaño-Alvarez, J.O., Pérez-España, H., Salas-Monreal, D. and Garcia-Rodríguez, E. (2013) Captures and diet of three shark species in the Veracruz reef system. Open Journal of Marine Science 3, 66–73.Google Scholar
Bass, A.J., D'Aubrey, J.D. and Kistnasamy, N. (1975) Sharks of the east coast South Africa. III. The families Carcharhinidae (excluding Mustelus and Carcharhinus) and Sphyrnidae. Oceanographic Research Institute Investigational Report 38, 1–100.Google Scholar
Bigelow, H.B. and Schroeder, W. (1948) Fishes of the western North Atlantic. Part I: lancelets, Cyclostomes, Sharks. Memoir Sears Foundation for Marine Research 1, 1–576.Google Scholar
Bizzarro, J.J., Robinson, H.J., Rinewalt, C.S. and Ebert, D.A. (2007) Comparative feeding ecology of four sympatric skate species off central California, USA. Environmental Biology of Fishes 80, 197–220.Google Scholar
Bornatowski, H., Braga, R.R., Abilhoa, V. and Corrêa, M.F.M. (2014a) Feeding ecology and trophic comparisons of six shark species in a coastal ecosystem off southern Brazil. Journal of Fish Biology 85, 246–263.Google Scholar
Bornatowski, H., Costa, L., Roberte, M.C. and da Pina, J.V. (2007) Hábitos alimentares de tubarões-martelo jovens, Sphyrna zygaena (Carcharhiniformes: Sphyrnidae), no litoral sul do Brasil. Biota Neotropica 7, 213–216.Google Scholar
Bornatowski, H., Navia, A.F., Braga, R.R., Abilhoa, V. and Corrêa, M.F.M. (2014b) Ecological importance of sharks and rays in a structural food web analysis in southern Brazil. ICES Journal of Marine Science 71, 1586–1592.Google Scholar
Braga, R.R., Bornatowski, H. and Vitule, J.R.S. (2012) Feeding ecology of fishes: an overview of worldwide publications. Reviews in Fish Biology and Fisheries 22, 915–929.Google Scholar
Casper, B.M., Domingo, A., Gaibor, N., Heupel, M.R., Kotas, E., Lamónaca, A.F., Pérez-Jimenez, J.C., Simpfendorfer, C., Smith, W.D., Stevens, J.D., Soldo, A. and Vooren, C.M. (2005) Sphyrna zygaena. The IUCN red list of threatened species 2005. e.T39388A10193797. Available at http://dx.doi.org/10.2305/IUCN.UK.2005.RLTS.TT39388A10193797.en.Google Scholar
Colwell, R.K. (2013) EstimateS: statistical estimation of species richness and shared species from simple (Software and User's Guide), Version 9.10. University of Connecticut, USA- URL. Available at http://viceroy.eeb.uconn.edu/estimates.Google Scholar
Compagno, L.J.V. (1984) FAO species catalogue. Sharks of the world. An annotated and illustrated catalogue of shark species known date. Part 1–2. Volume 4. Hexanchiformes to Carcharhiniformes. FAO Fisheries Synopsis 125. Rome: FAO.Google Scholar
Cortés, E. (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54, 726–738.Google Scholar
Cortés, E. (1999) Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56, 707–717.Google Scholar
Dulvy, N.K., Baum, J.K., Clarke, S., Compagno, L.J.V., Cortés, E., Domingo, A., Fordham, S., Fowler, S., Francis, M.P., Gibson, C., Martínez, 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.Google Scholar
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.Google Scholar
Estupiñán-Montaño, C., Cedeño-Figueroa, L.G. and Galván-Magaña, F. (2009) Feeding habits of the scalloped hammerhead shark Sphyrna lewini (Griffith & Smith, 1834) (Chondrichthyes) in the Ecuadorian Pacific. Revista de Biología Marina y Oceanografía 44, 379–386.Google Scholar
Froese, R. and Pauly, D. (eds) (2015) FishBase. World Wide Web electronic publication. Available at http://www.fishbase.org, Version (09/2015).Google Scholar
Galván-Magaña, F., Nienhuis, H.J. and Klimley, A.P. (1989) Seasonal abundance and feeding habits of sharks of the lower Gulf of California, Mexico. California Fish and Game 75, 74–84.Google Scholar
Galván-Magaña, F., Polo-Silva, C., Hernández-Aguilar, S.B., Sandoval-Londoño, A., Ochoa-Díaz, R.M., Aguilar-Castro, N., Castañeda-Suárez, D., Chávez-Costa, A., Baigorrí-Santacruz, Á., Torres-Rojas, Y.E. and Abitia-Cárdenas, A.L. (2013) Shark predation on cephalopods in the Mexican and Ecuadorian Pacific Ocean. Deep-Sea Research II 95, 52–62.Google Scholar
Gonzalez-Pestana, A., Acuña-Perales, N., Coasaca-Cespedes, J., Cordova-Zavaleta, F., Alfaro-Shigueto, J., Mangel, J.C. and Espinoza, P. (2017) Trophic ecology of the smooth hammerhead shark (Sphyrna zygaena) off the coast of northern Peru. Fishery Bulletin 115, 451–459.Google Scholar
Heithaus, M.R., Frid, A., Vaudo, J.J., Worm, B. and Wirsing, A.J. (2010) Unravelling the ecological importance of elasmobranchs. In Carrier, J.C., Musick, J.A. and Heithaus, M.R. (eds) Biology of sharks and their relatives II. Boca Raton, FL: CRC Press, pp. 611–637.Google Scholar
Heithaus, M.R., Frid, A., Wirsing, A.J. and Worm, B. (2008) Predicting ecological consequences of marine top predator declines. Trends in Ecology and Evolution 23, 202–210.Google Scholar
Hobson, K.A. and Welch, H.E. (1992) Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Marine Ecology Progress Series 84, 9–18.Google Scholar
Hyslop, E.J. (1980) Stomach contents analysis – a review of methods and their application. Journal of Fish Biology 17, 411–429.Google Scholar
Jereb, P. and Roper, C.F.E. (2010) Cephalopods of the world. An annotated and illustrated catalogue of cephalopods species known to date. Volume 2. Myopsid and Oegopsid squids. FAO Species Catalogue for Fishery Purposes 4. Rome: FAO.Google Scholar
Kim, S.L., Tinker, M.T., Estes, J.A. and Koch, P.L. (2012) Ontogenetic and among-individual variation in foraging strategies of northeast Pacific white sharks based on stable isotope analysis. PLoS ONE 7, e45068.Google Scholar
Krebs, C.J. (1999) Ecological methodology. New York, NY: Addison Wesley Longman, p. 620.Google Scholar
Loor-Andrade, P., Galván-Magaña, F., Elorriaga-Verplancken, F.R., Polo-Silva, C. and Delgado-Huertas, A. (2015) Population and individual foraging patterns of two hammerhead sharks using carbon and nitrogen stable isotopes. Rapid Communications in Mass Spectrometry 29, 821–829.Google Scholar
Lowe, C.G., Wetherbee, B.M., Crow, G.L. and Tester, A.L. (1996) Ontogenetic dietary shifts and feeding behaviour of the tiger shark, Galeocerdo cuvier, in Hawaiian waters. Environmental Biology of Fishes 47, 203–211.Google Scholar
Lucifora, L.O., Garcia, V.B. and Worm, B. (2011) Global diversity hotspots and conservation priorities for sharks. PLoS ONE 6, e19356.Google Scholar
Marshall, A.D., Kyne, P.M. and Bennett, M.B. (2008) Comparing the diet of two sympatric urolophid elasmobranchs (Trygonoptera testacea Müller & Henle and Urolophus kapalensis Yearsley & Last): evidence of ontogenetic shifts and possible resource partitioning. Journal of Fish Biology 72, 883–898.Google Scholar
Martínez-Ortíz, J., Galván-Magaña, F., Carrera-Fernández, M., Mendoza-Intriago, D., Estupiñán-Montaño, C. and Cedeño-Figueroa, L. (2007) Seasonal abundance of sharks landing in Manta – Ecuador. In Martínez-Ortíz, J.F. and Galván-Magaña, F. (eds) Tiburones en Ecuador: Casos de esudio/Shark in Ecuador: case studies. Manta, Ecuador: EPESPO – PMRC, pp. 9–27.Google Scholar
Myers, R.A., Baum, J.K., Shepherd, T.D., Powers, S.P. and Peterson, C.H. (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850.Google Scholar
Nava, P. and Márquez-Farías, J.F. (2014) Talla de madurez del tiburón martillo, Sphyrna zygaena, capturado en el Golfo de California. Hidrobiológica 24, 129–135.Google Scholar
Navia, A.F., Cortés, E. and Mejía-Falla, P.A. (2010) Topological analysis of the ecological importance of elasmobranch fishes: a food web study on the Gulf of Tortugas, Colombia. Ecological Modelling 221, 2918–2926.Google Scholar
Newman, S.P., Handy, R.D. and Gruber, S.H. (2012) Ontogenetic diet shifts and prey selection in nursery bound lemon sharks, Negaprion brevirostris, indicate a flexible foraging tactic. Environmental Biology of Fishes 95, 115–126.Google Scholar
Pauly, D., Trites, A., Capuli, E. and Christensen, V. (1998) Diet composition and trophic levels of marine mammals. ICES Journal of Marine Science 55, 467–481.Google Scholar
Pauly, D. and Zeller, D. (eds) (2015) Sea Around Us: concepts, design and data. Available at http://www.seaaround.org, Version (06/2016).Google Scholar
Pinkas, L., Oliphant, M.S. and Iverson, I.L.K. (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. California Fish and Game Fishery Bulletin 152, 1–105.Google Scholar
Rosas-Luis, R., Loor-Andrade, P., Carrera-Fernández, M., Pincay-Espinoza, J.E., Vinces-Ortega, C. and Chompoy-Salazar, L. (2015) Cephalopod species in the diet of large pelagic fish (sharks and billfishes) in Ecuadorian waters. Fisheries Research 173, 159–168.Google Scholar
Shiffman, D.S., Gallagher, A.J., Boyle, M.D., Hammerschlag-Peyer, C.M. and Hammerschlag, N. (2012) Stable isotope analysis as a tool for elasmobranch conservation research: a primer for non-specialists. Marine and Freshwater Research 63, 635–643.Google Scholar
Smale, M.J. (1991) Occurrence and feeding of three shark species, Carcharhinus brachyurus, C. obscurus and Sphyrna zygaena, on the Eastern Cape coast of South Africa. South African Journal of Marine Science 11, 31–42.Google Scholar
Smale, M.J. and Cliff, G. (1998) Cephalopods in the diets of four shark species (Galeocerdo cuvier, Sphyrna lewini, S. zygaena, S. mokarran) from Kwazulu-Natal, South Africa. South African Journal of Marine Science 20, 241–253.Google Scholar
Smith, E.P. and Zaret, T.M. (1982) Bias in estimating niche overlap. Ecology 63, 1248–1253.Google Scholar
Stevens, J.D. (1984) Biological observations on sharks caught by sport fishermen off New South Wales. Australian Journal of Marine and Freshwater Research 35, 573–590.Google Scholar
Stevens, J.D., Bonfil, R., Dulvy, N.K. and Walker, P.A. (2000) The effects of fishing on sharks, rays, and chimeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57, 476–494.Google Scholar
Taipe, A., Yamashiro, C., Mariategui, L., Rojas, P. and Roque, C. (2001) Distribution and concentrations of jumbo flying squid (Dosidicus gigas) off the Peruvian coast between 1991 and 1999. Fisheries Research 54, 21–32.Google Scholar
Torres-Rojas, E.Y., Hernández-Herrera, A. and Galván-Magaña, F. (2006) Feeding habits of the scalloped hammerhead shark, Sphyrna lewini, in Mazatlán waters, southern Gulf of California, Mexico. Cybium 30, 85–90.Google Scholar
Torres-Rojas, E.Y., Páez-Osuna, F., Camalich, J. and Galván-Magaña, F. (2015) Diet and trophic level of scalloped hammerhead shark (Sphyrna lewini) from the Gulf of California and Gulf of Tehuantepec, Mexico. Iranian Journal of Fisheries Sciences 14, 767–785.Google Scholar
Wetherbee, B., Gruber, S. and Cortés, E. (1990) Diet, feeding habits, digestion and consumption in sharks, with special reference to the lemon shark, Negaprion brevirostris. In Pratt, H.L. Jr., Gruber, S.H. and Taniuchi, T. (eds) Elasmobranchs as living resources: advances in the biology, ecology, systematics and the status of the fisheries. NOAA Technical Report NMFS 90, 29–47.Google Scholar