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Spatial variation in the foraging behaviour of the Galapagos sea lions (Zalophus wollebaeki) assessed using scat collections and stable isotope analysis

Published online by Cambridge University Press:  03 December 2013

Diego Páez-Rosas  and
David Aurioles-Gamboa
Diego Páez-Rosas*
Affiliation:
Universidad San Francisco de Quito (USFQ) and Galapagos Science Center, Galapagos, Ecuador Programa PROMETEO-SENESCYT, Secretaria Nacional de Educación Superior, Ciencia, Tecnología e Innovación Quito, Ecuador Parque Nacional Galápagos, Unidad Técnica San Cristóbal, Islas Galápagos, Ecuador
David Aurioles-Gamboa
Affiliation:
Laboratorio de Ecología de Pinnípedos “Burney J. Le Boeuf”, Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, La Paz, B.C.S., México
*
Correspondence shold be addressed to: Diego Páez-Rosas, Universidad San Francisco de Quito, Av. Alsacio Northia s/n, frente Playa Mann, Isla San Cristóbal, Galapagos, Ecuador email: [email protected].
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Abstract

This study focuses on the comparative analysis of variables related to the trophic niche plasticity in the Galapagos sea lion (Zalophus wollebaeki). There is great concern regarding the future of this species, so study of the diet and the way these animals obtain their food is useful to understand and predict their survival possibilities in the long term. The combined use of scat analysis and stable isotopes helps to determine foraging habits of this species in greater detail. The objective of the study was to assess the feeding habits of Z. wollebaeki and its space–time variation. The scat analysis (n = 200) gave as a result space–time changes in the foraging strategies of this species. The isotopic values (n = 80) showed differences in relation to foraging grounds (δ13C: P = 0.001), but also suggested an apparent stability in the trophic level of their diet (δ15N: P = 0.084). These results constitute a relevant finding in the evolutionary behaviour of the species, showing that Z. wollebaeki has developed a high degree of plasticity in its foraging habits that may improve its survival in a highly demanding ecosystem in terms of limited and fluctuating resources.

Keywords

foraging behaviourtrophic nichescat analysisstable isotopesGalapagos IslandsZalophus wollebaeki
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 94 , Issue 6 , September 2014 , pp. 1099 - 1107
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

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References

REFERENCES

Aurioles-Gamboa, D. and Trillmich, F. (2008) Zalophus wollebaeki. In IUCN Red List of Threatened Species. Available at: www.iucnredlist.org (accessed 8 November 2013).Google Scholar
Aurioles-Gamboa, D., Newsome, S.D., Salazar-Pico, S. and Koch, P.L. (2009) Stable isotope differences between sea lions of the genus Zalophus from the Gulf of California and Galapagos Islands. Journal of Mammology 90, 1410–1420.CrossRefGoogle Scholar
Banks, A.S. (2002) Ambiente Físico. In Danulat, E. and Edgar, G.J. (eds) Reserva Marina de Galápagos. Línea Base de la Biodiversidad. Galápagos, MA: Fundación Charles Darwin y Servicio Parque Nacional Galápagos, pp. 32–46.Google Scholar
Baque-Menoscal, J., Páez-Rosas, D. and Wolff, M. (2012) Hábitos alimentarios de dos peces pelágicos Thunnus albacares y Acanthocybium solandri de la Reserva Marina de Galápagos. Revista de Biología Marina y Oceanografía 47, 1–11.CrossRefGoogle Scholar
Bearhop, S., Colin, E., Adams, S., Fuller, R. and Macleod, H. (2004) Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73, 1007–1012.CrossRefGoogle Scholar
Bidigare, R.R., Fluegge, A., Freeman, K.H., Hanson, K.L., Hayes, J.M., Hollander, H., Jasper, J.D., King, L.L., Laws, E.A., Milder, J., Millero, F.J., Pancost, R., Popp, B.N., Steinbergand, P.A. and Wakeham, G. (1997) Consistent fractionation of 13C in nature and in the laboratory: growth-rate effects in some haptophyte algae. Global Biogeochemical Cycles 11, 279–292.CrossRefGoogle ScholarPubMed
Bligh, G.E. and Dyer, J.W. (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.CrossRefGoogle ScholarPubMed
Canales, M., Saavedra, C., Böhm, G. and Martínez, C. (2003) Investigación y evaluación de stock de anchoveta y sardina española, III y IV Regiones 2004. Research Bulletin. Estación Científica Charles Darwin, 102 pp.Google Scholar
Costa, D.P., Weise, M.J. and Arnould, J.P. (2006) Potential influences of whaling on the status and trends of pinniped populations. In Esters, J.A., Demaster, D.P., Doak, D.F., Williams, T.M. and Brownell, R.L. Jr (eds) Whales, whaling, and ocean ecosystems. Berkeley, CA: University of California Press.Google Scholar
Cullen, J.T., Rosenthal, Y. and Falkowski, P.G. (2001) The effect of anthropogenic CO2 on the carbon isotope composition of marine phytoplankton. Limnology and Oceanography 46, 996–998.CrossRefGoogle Scholar
Dellinger, T. and Trillmich, F. (1999) Fish prey of the sympatric Galapagos fur seals and sea lions: seasonal variation and niche separation. Canadian Journal of Zoology 77, 1204–1216.CrossRefGoogle Scholar
DeNiro, M.J. and Epstein, S. (1978) Influence of the diet on the distribution of carbon isotopes in animals. Geochimica Cosmochimica Acta 42, 495–506.CrossRefGoogle Scholar
DeNiro, M.J. and Epstein, S. (1981) Influence of the diet on the distribution of nitrogen isotopes in animals. Geochimica Cosmochimica Acta 45, 341–353.CrossRefGoogle Scholar
Díaz-Murillo, M.B. (2007) Catálogo de otolitos de peces marinos de las costas adyacentes a Baja California Sur. BSc thesis. Universidad Autónoma de Baja California Sur, La Paz, Mexico.Google Scholar
France, R. (1995) Carbon-13 enrichment in benthic compared to planktonic algae: food web implications. Marine Ecology Progress Series 124, 307–312.CrossRefGoogle Scholar
Fry, B. and Wainright, S.C. (1991) Diatom sources of 13C-rich carbon in marine food webs. Marine Ecology Progress Series 76, 149–157.CrossRefGoogle Scholar
García-Godos, I. (2001) Patrones morfológicos del otolito sagitta de algunos peces óseos del mar peruano. Research Bulletin. Instituto Ciencias Marinas del Perú, 107 pp.Google Scholar
García-Rodríguez, F.J. and Aurioles-Gamboa, D. (2004) Spatial and temporal variations in the diet of the California sea lion (Zalophus californianus) in the Gulf of California, México. Fisheries Bulletin 102, 47–62.Google Scholar
Gentry, R.L. and Kooyman, G.L. (1987) Fur seals: maternal strategies on land and at sea. Princeton, NJ: Princeton University Press.Google Scholar
Graham, B., Koch, P.L., Newsome, S.D., McMahon, K. and Aurioles-Gamboa, D. (2010) Using isoscapes to trace the movement and foraging behaviour of top predators in oceanic ecosystems. In West, J.B., Bowen, G.J., Dawson, T.E., Tu, K.P. (eds). Isoscapes: understanding movement, pattern, and process on Earth through isotope mapping. Berlin: Springer.Google Scholar
Grove, J.S. and Lavenberg, R.J. (1997) The fishes of the Galapagos Islands. Stanford, CA: California University Press.Google Scholar
Harris, M.P. (1969) Breeding seasons of seabirds in the Galapagos Islands. Journal of Zoology 159, 145–165.CrossRefGoogle Scholar
Heath, C.B. (2002) California, Galapagos, and Japanese sea lions Zalophus californianus, Z. wollebaeki, and Z. japonicus. In Perrin, W.F., Wursig, B. and Thiewissen, J.G. (eds) Encyclopedia of marine mammals. London: Academic Press.Google Scholar
Hobson, K.A., Schell, M.D., Renouf, D. and Noseworthy, E. (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Journal of Fisheries and Aquatic Science 53, 528–533.CrossRefGoogle Scholar
Horn, H.S. (1966) Measurement of overlap in comparative ecological studies. American Nature 100, 419–424.CrossRefGoogle Scholar
Kooyman, G.L. and Trillmich, F. (1986) Diving behaviour of Galápagos sea lions. In Gentry, R.L. and Kooyman, G.L. (eds) Maternal investment in otariid seals and walruses. Princeton, NJ: Princeton University Press.Google Scholar
Krebs, C.J. (1999) Ecological methodology. Longman, California: Addison Wesley.Google Scholar
Minagawa, M. and Wada, E. (1984) Stepwise enrichment of 15N along food chains. Further evidence and the relation between δ15N and animal age. Geochimica Cosmochimica Acta 48, 1135–1140.CrossRefGoogle Scholar
Montoya, J.P. (2010) Natural abundance of 15N in marine planktonic ecosystems. In Michener, R. and Lajtha, K. (eds) Stable isotopes in ecology and environmental science. London: Blackwell Publishing.Google Scholar
Nelson, J.S. (2006) Fishes of the World, 4th edition. New York: Wiley.Google Scholar
Newsome, S.D., Clementz, M.R. and Koch, P.L. (2010) Using stable isotope biochemistry to study marine mammal ecology. Marine Mammal Science 26, 509–572.Google Scholar
Newsome, S.D., Martinez del Rio, C., Bearhop, S. and Phillips, D.L. (2007) A niche for isotopic ecology. Frontiers in Ecology and the Environment 5, 429–436.CrossRefGoogle Scholar
Osman, L.P., Hucke-Gaete, R., Moreno, C.A. and Torres, D. (2004) Feeding ecology of Antarctic fur seal at Cape Shirreff, South Shetlands, Antarctica. Polar Biology 27, 92–98.CrossRefGoogle Scholar
Páez-Rosas, D. (2011) Ecología trófica de los pinnípedos de las Islas Galápagos: análisis temporal y espacial. PhD thesis. Instituto Politécnico Nacional, La Paz, Mexico.Google Scholar
Páez-Rosas, D. and Aurioles-Gamboa, D. (2010) Alimentary niche partitioning in the Galapagos sea lion, Zalophus wollebaeki. Marine Biology 157, 2769–2781.CrossRefGoogle Scholar
Páez-Rosas, D., Aurioles-Gamboa, D., Alava, J.J. and Palacios, D.M. (2012) Stable isotopes indicate differing foraging strategies in two sympatric otariids of the Galapagos Islands. Journal of Experimental Marine Biology and Ecology 425, 44–52.CrossRefGoogle Scholar
Palacios, D.M., Bograd, S.J., Foley, D.G. and Schwing, F.B. (2006) Oceanographic characteristics of biological hot spots in the North Pacific: a remote sensing perspective. Deep-Sea Research II 53, 250–269.CrossRefGoogle Scholar
Pancost, R.D., Freeman, K.H., Wakeham, S.G. and Robertson, C.Y. (1997) Controls on carbon isotope fractionation by diatoms in the Peru upwelling region. Geochimica Cosmochimica Acta 61, 4983–4991.CrossRefGoogle Scholar
Pak, H. and Zanveld, J.R. (1973) The Cromwell Current on the east side of the Galapagos Islands. Journal of Geophysical Research 78, 4845–7859.CrossRefGoogle Scholar
Porras-Peters, H., Aurioles-Gamboa, D., Koch, P.L. and Cruz-Escalona, V. (2008) Position, breadth and trophic overlap of sea lions (Zalophus californianus) in the Gulf of California. Mexico. Marine Mammal Science 24, 554–576.CrossRefGoogle Scholar
Post, D.M. (2002) Using stable isotopes to estimate trophic position models methods, and assumptions. Ecology 83, 703–718.CrossRefGoogle Scholar
Ruttenberg, B.I., Haupt, A.J., Chiriboga, A.I. and Warner, R.R. (2005) Patterns, causes and consequences of regional variation in the ecology and life history of a reef fish. Oecologia 145, 394–403.CrossRefGoogle ScholarPubMed
Salazar, S.K. (2005) Variación temporal y espacial del espectro trófico del lobo marino de Galápagos. MSc thesis. Instituto Politécnico Nacional, La Paz, Mexico.Google Scholar
Schaeffer, B.A., Morrison, J.M., Kamykowski, D., Feldman, G.C., Xie, L., Liu, Y., Sweet, A., McCulloch, A. and Banks, S. (2008) Phytoplankton biomass distribution and identification of productive habitats within the Galapagos Marine Reserve by MODIS, a surface acquisition system, and in-situ measurements. Remote Sensing of Environmen 112, 3044–3054.CrossRefGoogle Scholar
Schell, D.M., Barnett, B.A. and 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.CrossRefGoogle Scholar
Sigman, D.M., Granger, J., DiFiore, P.J., Lehmann, M.M., Ho, R., Cane, G. and van Geen, A. (2005) Coupled nitrogen and oxygen isotope measurements of nitrate along the eastern North Pacific margin. Global Biogeochemical Cycles 19, GB4022. doi: 10.1029/2005GB002458CrossRefGoogle Scholar
Tieszen, L.L., Boutton, T.W., Tesdahl, K.G. and Slade, N.A. (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57, 32–37.CrossRefGoogle ScholarPubMed
Tollit, D.J., Heaslip, S.G., Deagle, B.E., Iverson, S.J., Joy, R., Rosen, D.A. and Trites, A.W. (2006) Estimating diet composition in sea lions: which technique to choose? In Trites, A.W., Atkinson, S., DeMaster, D.P., Fritz, L.W., Gelatt, T.S., Rea, L.D. and Wynne, K. (eds) Sea lions of the world. Fairbanks, AK: University of Alaska.Google Scholar
Trillmich, F. and Ono, K. (1991) The effects of El Niño on pinniped populations in the eastern Pacific. New York: Springer.CrossRefGoogle Scholar
Trillmich, F. and Wolf, J.B. (2008) Parent-offspring and sibling conflict in Galapagos fur seals and sea lions. Behavioural Ecology and Sociobiology 62, 363–375.CrossRefGoogle Scholar
Vander-Zanden, M.J. and Rasmussen, J.B. (1999) Primary consumer d13C and d15N and the trophic position of acuatic consumers. Ecology 80, 1395–1404.CrossRefGoogle Scholar
Villegas-Amtmann, S., Costa, D., Tremblay, Y., Aurioles-Gamboa, D. and Salazar, S. (2008) Multiple foraging strategies in a marine apex predator, the Galapagos Sea Lion. Marine Ecology Progress Series 363, 299–309.CrossRefGoogle Scholar
Villegas-Amtmann, S., Simmons, S.E., Kuhn, C.E., Huckstadt, L.A. and Costa, D.P. (2011) Latitudinal range influences the seasonal variation in the foraging behaviour of marine top predators. PLoS ONE 6, 23166.CrossRefGoogle ScholarPubMed