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Magellanic penguins: stomach contents and isotopic profiles to assess the feeding demands of juveniles in a wintering area off Brazil

Published online by Cambridge University Press:  15 October 2014

Ana Paula Madeira Di Beneditto*
Affiliation:
Laboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense, CBB, Av. Alberto Lamego, 2000, Campos dos Goytacazes, RJ 28013-620, Brazil
Roberta Aguiar Dos Santos
Affiliation:
Instituto Chico Mendes de Conservação da Biodiversidade, Centro de Pesquisa e Gestão dos Recursos Pesqueiros do Litoral Sudeste e Sul, Av. Ministro Victor Konder, 303, Itajaí, SC 88301-700, Brazil
Karen Russel Rosa
Affiliation:
Instituto Chico Mendes de Conservação da Biodiversidade, Centro de Pesquisa e Gestão dos Recursos Pesqueiros do Litoral Sudeste e Sul, Av. Ministro Victor Konder, 303, Itajaí, SC 88301-700, Brazil
Salvatore Siciliano
Affiliation:
Fundação Oswaldo Cruz, Escola Nacional de Saúde Pública, Rua Leopoldo Bulhões 1480, 6° andar, sala 611, Manguinhos, Rio de Janeiro, RJ 21041-210, Brazil
*
Correspondence should be addressed to: A.P.M. Di Beneditto, Laboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense, CBB, Av. Alberto Lamego, 2000, Campos dos Goytacazes, RJ 28013-620, Brazil email: anadibeneditto@gmail.com

Abstract

The stomach contents of juvenile Magellanic penguins, Spheniscus magellanicus, stranded along the Atlantic coast (21–23°S) during the extreme mortality event of 2008 were analysed. The isotopic profiles of this species and their prey in a wintering area are presented to identify trophic relationships and to evaluate whether the prey species recovered in the stomach contents were assimilated. The prey groups recorded were molluscs (cephalopods and gastropods), teleost fish, and, to a lesser extent, crustaceans (decapods and isopods). Cephalopods were the most representative prey, and Argonauta nodosa was the most abundant species. Plant remains and solid waste were atypical items found in the stomach contents. The nitrogen isotope (δ15N) values found in this study confirm the higher trophic position of the penguins (14.5‰) relative to their prey (11.7–12.3‰). The carbon isotope (δ13C) measurements of all species are characteristic of marine coastal environments (−18.7 to −16.8‰). A Bayesian approach applied to stable isotope mixing models showed that cephalopods are assimilated to a greater extent than fish. However, the poor nutritional condition of specimens that reach the Brazilian coast, especially at the northern limit of migration (~21°S), indicates that prey ingestion is not sufficient for the maintenance of body weight.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

Baldassin, P., Santos, R.A., Cunha, J.M.M., Werneck, M.R. and Gallo, H. (2010) Cephalopods in the diet of Magellanic penguins on the coast of Brazil. Marine Ornithology 38, 5557.Google Scholar
Barquete, V., Strauss, V. and Ryan, P.G. (2013) Stable isotope turnover in blood and claws: a case study in captive African penguins. Journal of Experimental Marine Biology and Ecology 448, 121127.CrossRefGoogle Scholar
Barrett, R.T., Camphuysen, C.J., Anker-Nilssen, T., Chardine, J.W., Furness, R.W., Garthe, S., Hüppop, O., Leopold, M.F., Montevecchi, W.A. and Veit, R.R. (2007) Diet studies of seabirds: a review and recommendations. ICES Journal of Marine Science 64, 16751691.CrossRefGoogle Scholar
Bisi, T.L., Lepoint, G., Azevedo, A.F., Dorneles, P.R., Flach, L., Das, K., Malm, O. and Lailson-Brito, J. (2012) Trophic relationships and mercury biomagnification in Brazilian tropical coastal food webs. Ecological Indicators 18, 291302.CrossRefGoogle Scholar
Boersma, P.D., Rebstock, G.A., Frere, E. and Moore, S.E. (2009) Following the fish: penguins and productivity in the South Atlantic. Ecological Monographs 79, 5976.CrossRefGoogle Scholar
Brandão, M.L., Braga, K.M. and Luque, J.L. (2011) Marine debris ingestion by Magellanic penguins, Spheniscus magellanicus (Aves: Sphenisciformes), from the Brazilian coastal zone. Marine Pollution Bulletin 62, 22462249.CrossRefGoogle ScholarPubMed
Caut, S., Angulo, E. and Courchamp, F. (2009) Variation in discrimination factors (∧15N and ∧13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443453.CrossRefGoogle Scholar
Cergol, M.C., Saccard, S.A. and Rossi-Wongtschowsk, C.L.D.B. (2002) Fluctuations in the spawning stock biomass and recruitment of the Brazilian sardine (Sardinella brasiliensis): 1977–1997. Revista Brasileira de Oceanografia 50, 1326.CrossRefGoogle Scholar
Cherel, Y., Hobson, K.A., Bailleu, F. and Groscola, R. (2005) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86, 28812888.CrossRefGoogle Scholar
Dantas, G.M., Almeida, V.S., Maracini, P., Serra, S.D., Chame, M., Labarthe, N., Kolesnikovass, C., Siciliano, S., Matias, C.A.R., Moura, J.F., Campos, S.D.E., Mader, A. and Serafini, P.P. (2013) Evidence for northward extension of the winter range of Magellanic penguins along the Brazilian coast. Marine Ornithology 41, 195197.Google Scholar
Di Beneditto, A.P.M., Souza, C.M.M., Kehrig, H.A. and Rezende, C.E. (2011) Use of multiple tools to assess the feeding preference of coastal dolphins. Marine Biology 158, 22092217.CrossRefGoogle Scholar
Fonseca, V.S., Petry, M.V. and Jost, A.H. (2001) Diet of the Magellanic penguin on the coast of Rio Grande do Sul, Brasil. Waterbirds 24, 290293.CrossRefGoogle Scholar
Forero, M.G., Hobson, K.A., Bortolotti, G.R., Donazar, J.A., Bertellotti, M. and Blanco, G. (2002a) Food resource utilisation by the Magellanic penguin evaluated through stable-isotope analysis: segregation by sex and age and influence on offspring quality. Marine Ecology Progress Series 234, 289299.CrossRefGoogle Scholar
Forero, M.G., Tella, J.L., Hobson, K.A., Bertellotti, M. and Blanco, G. (2002b) Conspecific food competition explains variability in colony size: a test in Magellanic penguins. Ecology 83, 34663475.CrossRefGoogle Scholar
Frere, E., Gandini, P. and Lichtschein, V. (1996) Variación latitudinal en la dieta del pinguino de magallanes (Spheniscus magellanicus) en la costa Patagonica, Argentina. Ornitologia Neotropical 7, 3541.Google Scholar
García-Borboroglu, P., Boersma, P.D., Ruoppolo, V., Pinho da Silva, A.R., Corrado, A., Conte-Sena, D., Velozo, R., Myiaji-Kolesnikovas, C., Dutra, G., Maracini, P., Carvalho-do-Nascimento, C., Ramos-Júnior, V., Barbosa, L. and Serra, S. (2010) Magellanic penguin mortality in 2008 along the SW Atlantic coast. Marine Pollution Bulletin 60, 16521657.CrossRefGoogle ScholarPubMed
Haimovici, M. and Perez, J.A.A. (1991) Coastal cephalopod fauna of southern Brazil. Bulletin of Marine Science 49, 221230.Google Scholar
Hobson, K.A., Alisauskas, R.T. and Clark, R.G. (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95, 388394.CrossRefGoogle Scholar
Hobson, K.A. and Clark, R.G. (1992) Assessing avian diets using stable isotopes 2. Factors influencing diet-tissue fractionation. Condor 94, 189197.CrossRefGoogle Scholar
Hobson, K.A., Schell, 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. Canadian Journal of Fisheries and Aquatic Science 53, 528533.CrossRefGoogle Scholar
Hobson, K.A. and Welch, H.E. (1992) Determination of trophic relationships within a high Arctic food web using δ13C and δ15 N analysis. Marine Ecology Progress Series 84, 918.CrossRefGoogle Scholar
Ivar do Sul, J.A. and Costa, M. F. (2007) Marine debris review for Latin America and the wider Caribbean region: from the 1970s until now, and where do we go from here? Marine Pollution Bulletin 54, 10871104.CrossRefGoogle Scholar
Kempster, B., Zanette, L., LongstaVe, F.J., MacDougall-Shackleton, S.A., WingWeld, J.C. and Clinchy, M. (2007) Do stable isotopes reflect nutritional stress? Results from a laboratory experiment on song sparrows. Oecologia 151, 365371.CrossRefGoogle ScholarPubMed
Lansdell, M. and Young, J. (2007) Pelagic cephalopods from eastern Australia: species composition, horizontal and vertical distribution determined from the diet of pelagic fishes. Review of Fish Biology and Fishery 17, 125138.CrossRefGoogle Scholar
Mäder, A., Sander, M. and Casa, G. Jr. (2010) Ciclo sazonal de mortalidade do pinguim-de-Magalhães, Spheniscus magellanicus influenciado por fatores antrópicos e climáticos na costa do Rio Grande do Sul, Brasil. Revista Brasileira de Ornitologia 18, 228233.Google Scholar
Mai, A.C.G. and Vieira, J.P. (2013) Review and consideration on habitat use, distribution and life history of Lycengraulis grossidens (Agassiz, 1829) (Actinopterygii, Clupeiformes, Engraulididae). Biota Neotropica 13, 121130.CrossRefGoogle Scholar
Michalik, A., McGill, R.A.R., van Noordwijk, H.J., Masello, J.F., Furness, R.W., Eggers, T. and Quillfeldt, P. (2013) Stable isotopes reveal variable foraging behaviour in a colony of the Imperial Shag Phalacrocorax atriceps: differences between ages, sexes and years. Journal of Ornithology 154, 239249.CrossRefGoogle Scholar
Munroe, T.A. and Nizinski, M.S. (2002) Engraulidae. In Carpenter, K. (ed.) The living marine resources of the Western Central Atlantic. Rome: FAO Species Identification Guide for Fishery Purposes, no. 5, pp. 764794.Google Scholar
Oelbermann, K. and Scheu, S. (2002) Stable isotope enrichment (delta N-15 and delta C-13) in a generalist predator (Pardosa lugubris, Araneae : Lycosidae): effects of prey quality. Oecologia 130, 337344.CrossRefGoogle 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, e9672. doi: 10.1371/journal.pone.0009672.CrossRefGoogle ScholarPubMed
Petry, M.V., Fonseca, V.S.S. and Jost, A.H. (2004) Registro de pinguin-de-magalhães (Spheniscus magellanicus) mortos no Rio Grande do Sul. Acta Biologica Leopoldensia 26, 139144.Google Scholar
Petry, M.V., Krüger, L., Fonseca, V.S.S., Brummelhaus, J. and Piuco, R.C. (2009) Diet and ingestion of synthetics by Corys Shearwater Calonectris diomedea off southern Brazil. Journal für Ornithologie 150, 601606.CrossRefGoogle Scholar
Pinkas, L., Oliphant, M. and Iverson, I.L.K. (1971) Food habits of albacore, bluefin tuna and bonito in Californian waters. Fishery Bulletin 152, 1105.Google Scholar
Pinto, M.B.L.C., Siciliano, S. and Di Beneditto, A.P.M. (2007) Stomach contents of the Magellanic penguin Spheniscus magellanicus from the northern distribution limit on the Atlantic coast of Brazil. Marine Ornithology 35, 7778.Google Scholar
Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J. and Montaña, C.G. (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179189.CrossRefGoogle Scholar
R Development Core Team. (2011) R: A language and environment for statistical computing. Reference index version 2.12.2. R Foundation for Statistical Computing, Vienna. www.R-project.org.Google Scholar
Radl, A. and Culik, B.M. (1999) Foraging behaviour and reproductive success in Magellanic Penguins (Spheniscus magellanicus): a comparative study of two colonies in southern Chile. Marine Biology 133, 381393.CrossRefGoogle Scholar
Reis, E.C., Aires, R.M., Moura, J.F., Matias, C.A.R., Tavares, M., Ott, P.H., Siciliano, S. and Lôbo-Hajdu, G. (2011) Molecular sexing of unusually large numbers of Spheniscus magellanicus (Spheniscidae) washed ashore along the Brazilian coast in 2008. Genetics and Molecular Research 10, 37313737.CrossRefGoogle ScholarPubMed
Sala, J.E., Wilson, R.P. and Quintana, F. (2012) How much is too much? Assessment of prey consumption by Magellanic penguins in Patagonian colonies. PLoS ONE 7, e51487. doi: 10.1371/journal.pone.0051487.CrossRefGoogle ScholarPubMed
Santos, R.A. and Haimovici, M. (2002) Cephalopods in the trophic relations off Southern Brazil. Bulletin of Marine Science 71, 753770.Google Scholar
Sartor, S.M. (1986) Incidência de isópodes parasitas (Cymothoidae) em peixes da plataforma continental brasileira. Boletim do Instituto Oceanográfico 34, 112.CrossRefGoogle Scholar
Schmidt, O., Scrimgeour, C.M. and Curry, J.P. (1999) Carbon and nitrogen stable isotope ratios in body tissue and mucus of feeding and fasting earthworms (Lumbricus festivus). Oecologia 118, 915.CrossRefGoogle ScholarPubMed
Silva, R.R., Pereira, J., Tanajura, A.S.C., Lentini, C.A.D., Cirano, M., Boersma, P.D. and Rodrigues, R.R. (2012) Occurrence of Magellanic penguins along the Northeast Brazilian coast during 2008 austral winter. Scientific World Journal, art. 686184, doi: 10.1100/2012/686184.Google ScholarPubMed
StatSoft, Inc. (2007) STATISTICA (data analysis software system), version 8.0. http://www.statsoft.com.Google Scholar
Vidal, E.A.G., Haimovici, M. and Hackbart, V.C.S. (2010) Distribution of paralarvae and small juvenile cephalopods in relation to primary production in an upwelling area off southern Brazil. ICES Journal of Marine Science 67, 13461352.CrossRefGoogle Scholar
Williams, C.T., Buck, C.L., Sears, J. and Kitaysky, A.S. (2007) Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds. Oecologia 153, 1118.CrossRefGoogle ScholarPubMed
Williams, T.D. and Boersma, P.D. (1995) Magellanic penguin. In Williams, T.D. (ed.) Bird families of the world – the penguins. Oxford: Oxford University Press, pp. 249258.Google Scholar
Wilson, R.P., Scolaro, J.A., Grémillet, D., Kierspel, M.A.M., Laurenti, S., Upton, J., Gallelli, H., Quintana, F., Frere, E., Müller, G., Straten, M.T. and Zimmer, I. (2005) How do Magellanic penguins cope with variability in their access to prey? Ecological Monographs 75, 379401.CrossRefGoogle Scholar
Wu, N. (1989) The paper nautilus. Sea Frontiers 35, 9496.Google Scholar
Xavier, J.C., Phillips, R.A. and Cherel, Y. (2011) Cephalopods in marine predator diet assessments: why identifying upper and lower beaks is important. ICES Journal of Marine Science 68, 18571864.CrossRefGoogle Scholar