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Feeding habits of the short-finned squid Illex coindetii in the western Mediterranean Sea using combined stomach content and isotopic analysis

Published online by Cambridge University Press:  09 December 2015

Francisco Martínez-Baena*
Affiliation:
Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta, 37-49, 08003 Barcelona, Spain
Joan Navarro
Affiliation:
Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta, 37-49, 08003 Barcelona, Spain Department of Conservation Biology, Estación Biológica de Doñana (EBD-CSIC), Avenida Américo Vespucio s/n, Sevilla 41092, Spain
Marta Albo-Puigserver
Affiliation:
Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta, 37-49, 08003 Barcelona, Spain
Isabel Palomera
Affiliation:
Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta, 37-49, 08003 Barcelona, Spain
Rigoberto Rosas-Luis
Affiliation:
Departamento Central de Investigación, Universidad Laica ‘Eloy Alfaro’ de Manabí, Manta, Manabí, Ecuador
*
Correspondence should be addressed to: F. Martínez-Baena, Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta, 37-49, 08003 Barcelona, Spain email: [email protected]

Abstract

The ommastrephid squid, Illex coindetii, is one of the most abundant cephalopods in the Mediterranean Sea and an important predator in the ecosystem. In the present study, we examined the diet habits of I. coindetii in the north-western Mediterranean Sea by combining two complementary approaches: stomach content and stable isotopic analyses. Specifically, we examined whether the diet differed between sizes and seasons. Stomach content results indicated that the diet of I. coindetii was composed of 35 prey items including four major groups; namely the crustaceans Pasiphaea sivado, Amphipods, squid of the Order Teuthida, and pelagic and mesopelagic fish. Differences were found among different ontogenetic sizes: juvenile individuals fed mainly on crustaceans (%IRI = 77.59), whereas adult individuals fed on a wider range of prey items, including the shrimp P. sivado (%IRI = 33.21), the amphipod Anchylomera blossevillei (%IRI = 0.91), the decapod Plesionika sp. (%IRI = 0.19), the carangid Trachurus trachurus (%IRI = 0.34) and some Myctophids species (%IRI = 0.21). Differences were also found between seasons in the year. In winter, crustaceans were the main prey items, whereas in summer the diversity of prey was higher, including fish, crustaceans and molluscs. Similar to the stomach contents, stable isotopic results indicated differences among sizes. δ15N values were higher in adult squids than in juveniles because they fed on prey at higher trophic levels. In conclusion, this study indicates that feeding habits of I. coindetii vary seasonally and ontogenetically. These feeding variations may be associated with trophic competence scenarios based on size, and also with the availability and abundance of prey throughout the year.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Albo-Puigserver, M., Navarro, J., Coll, M., Aguzzi, J., Cardona, L. and Sáez-Liante, R. (2015) Feeding ecology and trophic position of three sympatric demersal chondrichthyes in the Northwestern Mediterranean. Marine Ecology Progress Series 524, 255268.Google Scholar
Anderson, M., Gorley, R. and Clarke, K. (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: Primer-E.Google Scholar
Barría, C., Coll, M. and Navarro, J. (2015) Unravelling the ecological role and trophic relationships of uncommon and threatened elasmobranchs in the western Mediterranean Sea. Marine Ecology Progress Series 539, 225240.CrossRefGoogle Scholar
Caddy, J.F. and Rodhouse, P.G. (1998) Cephalopod and groundfish landings: evidence for ecological change in global fisheries? Reviews in Fish Biology and Fisheries 8, 431444.CrossRefGoogle Scholar
Cailliet, G.M. (1976) Several approaches to the feeding ecology of fishes. In Simenstad, C.A. and Lipovsky, S.J. (eds) Fish Food Habits Studies, 1st Pacific Northwest Technical Workshop Proceedings. Astoria, OR, 13–15 October. University of Washington, Washington Sea-Grant Publications, Seattle, pp. 113.Google Scholar
Castro, J.J. and Hernández-García, V. (1995) Ontogenetic changes in mouth structures, foraging behavior and habitat use of Scomber japonicus and Illex coindetii . Scientia Marina 59, 347355.Google Scholar
Caut, S., Angulo, E. and Courchamp, F. (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443453.Google Scholar
Cherel, Y. and Hobson, K.A. (2005) Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids. Proceedings of the Royal Society of London, Series B 272, 16011607.Google Scholar
Cherel, Y., Ridoux, V., Spitz, J. and Richard, P. (2009) Stable isotopes document the trophic structure of a deep-sea cephalopod assemblage including giant octopod and giant squid. Biology Letters 5, 364367.Google Scholar
Clarke, M.R. (1986) A handbook for the identification of cephalopod beaks. Oxford: Clarendon Press.Google Scholar
Clarke, M.R. and Kristensen, T.R. (1980) Cephalopods beaks from the stomachs of two northern bottlenosed whales (Hyperoodon ampullatus). Journal of the Marine Biological Association of the United Kingdom 60, 151156.Google Scholar
Coll, M., Navarro, J., Olson, R.J. and Christensen, V. (2013a) Assessing the trophic position and ecological role of squids in marine ecosystems by means of food-web models. Deep Sea Research II: Tropical Studies in Oceanography 95, 2136.Google Scholar
Coll, M., Navarro, J. and Palomera, I. (2013b) Ecological role, fishing impact, and management options for the recovery of a Mediterranean endemic skate by means of food web models. Biological Conservation 157, 108120.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, 726738.Google Scholar
Costalago, D., Navarro, J., Álvarez-Calleja, I. and Palomera, I. (2012) Ontogenetic and seasonal changes in feeding habits and trophic levels of two small pelagic fish species. Marine Ecology Progress Series 460, 169181.CrossRefGoogle Scholar
Guerra, Á., Rodríguez-Navarro, A.B., González, Á.F., Romanek, C.S., Álvarez-Lloret, P. and Pierce, G.J. (2010) Life-history traits of the giant squid Architeuthis dux revealed from stable isotope signatures recorded in beaks. ICES Journal of Marine Sciences 67, 14251431.Google Scholar
Jereb, P. and Ragonese, S. (1995) An outline of the biology of the squid Illex coindetii in the Sicilian Channel (Central Mediterranean). Journal of the Marine Biological Association of the United Kingdom 75, 373390.CrossRefGoogle Scholar
Keller, S., Quetglas, A., Valls, M., Ordines, F., de Mesa, A., Olivar, M. Pilar and Massutí, E. (2012) Are pelagic cephalopods in the Mediterranean as abundant as suggests the stomach contents of their predators? CIAC 2012 Symposium. Abstracts: 93.<Corrected to: ‘Olivar M. Pilar’>>Google Scholar
Kelly, J.F. (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78, 127.Google Scholar
Layman, C., Araujo, M.S., Boucek, R., Hammerschlag-Peyer, C.M., Harrison, E., Jud, Z.R., Matich, P., Rosenblatt, A.E., Vaudo, J.J., Yeager, L.A., Post, D.M. and Bearhop, S. (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews 87, 545562.Google Scholar
Logan, J.M. and Lutcavage, M.E. (2010) Reply to Hussey et al.: the requirement for accurate diet-tissue discrimination factors for interpreting stable isotopes in sharks. Hydrobiologia 654, 712.Google Scholar
Navarro, J., Coll, M., Somes, C. and Olson, R.J. (2013) Trophic niche of squids: insights from isotopic data in marine systems worldwide. Deep Sea Research II: Tropical Studies in Oceanography 95, 93102.Google Scholar
Navarro, J., López, L., Coll, M., Barría, C. and Sáez-Liante, R. (2014) Short- and long-term importance of small sharks in the diet of the rare deep-sea shark Dalatias licha . Marine Biology 161, 16971707.CrossRefGoogle Scholar
Nesis, K. (1987) Cephalopods of the world. Squids, cuttlefishes, octopuses, and allies. Neptune City, NJ: T.H.F. Publications.Google Scholar
Omori, M. (1974) The biology of pelagic shrimps in the ocean. Advances in Marine Biology 12, 233324.Google Scholar
Parnell, A.C., Inger, R., Bearhop, S. and Jackson, A.L. (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5(3), e9672.CrossRefGoogle Scholar
Parnell, A.C. and Jackson, A.L. (2013) SIAR: stable isotope analysis in R. SIAR: stable isotope analysis in R. R Package version, 3.Google Scholar
Pereira, P.H.C., Barros, B., Zemoi, R. and Ferreira, B.P. (2014) Ontogenetic diet changes and food partitioning of Haemulon spp. coral reef fishes, with a review of the genus diet. Reviews in Fish Biology and Fisheries 25, 245260.Google Scholar
Petric, M., Mladineo, I. and Sifner, S.K. (2011) Insight into the short-finned squid Illex coindetii (Cephalopoda: Ommastrephidae) feeding ecology: is there a link between helminth parasites and food composition? Journal of Parasitology 97, 5562.Google Scholar
Pinkas, L., Oliphant, M.S. and Iverson, L.K. (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. Fish Bulletin 152, 1105.Google Scholar
Rasero, M., Gonzalez, A.F., Castro, B.G. and Guerra, A. (1996) Predatory relationships of two sympatric squid, Todaropsis eblanae and Illex coindetii (Cephalopoda: Ommastrephidae) in Galician waters. Journal of the Marine Biological Association of the United Kingdom 76, 7387.Google Scholar
Rodhouse, P. and Nigmatullin, C.M. (1996) Role as consumers. Philosophical Transactions of the Royal Society B: Biological Sciences 351, 10031022.Google Scholar
Rosas-Luis, R., Salinas-Zavala, C.A., Koch, V., del Monte-Luna, P. and Morales-Zárate, M.V. (2008) Importance of the jumbo squid Dosidicus gigas (Orbigny, 1835) in the pelagic ecosystem of the central Gulf of California. Ecological Modellling 218, 149161.Google Scholar
Rosas-Luis, R. and Sánchez, P. (2014) Food and feeding habits of Alloteuthis media in the Western Mediterranean Sea. Marine Biology Research 11, 438442.Google Scholar
Rosas-Luis, R., Villanueva, R. and Sánchez, P. (2014) Trophic habits of the Ommastrephid squid Illex coindetii and Todarodes sagittatus in the Northwestern Mediterranean Sea. Fisheries Research 152, 2128.Google Scholar
Ruiz-Cooley, R.I., Markaida, U., Gendron, D. and Aguiñiga, S. (2006) Stable isotopes in jumbo squid (Dosidicus gigas) beaks to estimate its trophic position: comparison between stomach contents and stable isotopes. Journal of the Marine Biological Association of the United Kingdom 86, 437445.CrossRefGoogle Scholar
Ruiz-Cooley, R.I., Villa, E. and Gould, W. (2010) Ontogenetic variation of δ13C and δ15N recorded in the gladius of the jumbo squid Dosidicus gigas: geographic differences. Marine Ecology Progress Series 399, 187198.Google Scholar
Salat, J. (1996) Review of hydrographic environmental factors that may influence anchovy habitats in the northwestern Mediterranean. Scientia Marina 60 (Suppl. 2), 2132.Google Scholar
Sánchez, P. (1982) Régimen alimentario de Illex coindetii (Verany, 1837) en el mar Catalán. Investigación Pesquera 46, 443449.Google Scholar
Sánchez, P., González, A.F., Jereb, P., Laptikhovsky, V.V., Mangold, K.M., Nigmatullin, Ch.M. and Ragonese, S. (1998) Illex coindetii . In Rodhouse, P.G., Dawe, E.G. and O'Dor, R.K. (eds) Squid recruitment dynamics: The genus Illex as a model, the commercial Illex species and influences on variability. Rome: FAO, FAO Fisheries Technical Paper 376, pp. 5976.Google Scholar
Sánchez, P. and Martin, P. (1993) Population dynamics of the exploited cephalopod species of the Catalan Sea (NW Mediterranean). Scientia Marina 57, 153159.Google Scholar
Smale, M. (1996) Cephalopods as prey. IV. Fishes. Philosophical Transactions of the Royal Society B: Biological Sciences 351, 10671081.Google Scholar
Stergiou, K.I. and Karpouzi, V.S. (2001) Feeding habits and trophic levels of Mediterranean fish. Reviews in Fish Biology and Fisheries 11, 217254.Google Scholar
Stowasser, G., Pierce, G.J., Moffat, C.F., Collins, M.A. and Forsythe, J.W. (2006) Experimental study on the effect of diet on fatty acid and stable isotope profiles of the squid Lolliguncula brevis . Journal of Experimental Marine Biology and Ecology 333, 97114.Google Scholar
Takai, N., Onaka, S., Ikeda, Y., Yatsu, A., Kidokoro, H. and Sakamoto, W. (2000) Geographical variations in carbon and nitrogen stable isotope ratios in squid. Journal of the Marine Biological Association of the United Kingdom 80, 675684.CrossRefGoogle Scholar
Tuset, V.M., Lombarte, A. and Assis, C.A. (2008) Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Scientia Marina 72, 7198.Google Scholar
Zariquiey-Alvarez, R. (1986) Crustáceos Decápodos Ibéricos. Investigación Pesquera 32, 510 pp.Google Scholar