Register      Login
Emu Emu Society
Journal of BirdLife Australia
RESEARCH ARTICLE

Pelagic or benthic prey? Combining trophic analyses to infer the diet of a breeding South American seabird, the Red-legged Cormorant, Phalacrocorax gaimardi

Annick Morgenthaler A C , Ana Millones A , Patricia Gandini A B and Esteban Frere A B
+ Author Affiliations
- Author Affiliations

A Centro de Investigaciones de Puerto Deseado, Universidad Nacional de la Patagonia Austral, Av. Prefectura s/n, cc 238 (9050), Puerto Deseado, Santa Cruz, Argentina.

B Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Av. Prefectura s/n, cc 238 (9050), Puerto Deseado, Santa Cruz, Argentina.

C Corresponding author. Email: annick.morgenthaler@gmail.com

Emu 116(4) 360-369 https://doi.org/10.1071/MU15101
Submitted: 27 September 2015  Accepted: 3 June 2016   Published: 19 July 2016

Abstract

The available information about the feeding habits and preferences of the Red-legged Cormorant (Phalacrocorax gaimardi) generally suggests that this near-threatened South American cormorant is a sedentary benthic forager that also incorporates pelagic prey in its diet. In order to describe the dietary composition and assess the importance of certain prey types (pelagic vs benthic), we studied the diet of this cormorant on the Argentine Atlantic coast during four breeding seasons, using a combined technique of conventional diet assessment (pellets) and stable isotope analysis. Our results show that the Red-legged Cormorant forages mainly on pelagic and demersal–pelagic prey. Results of both techniques showed the main prey to be the Patagonian Sprat, a small high-energy-content pelagic forage fish, and the Patagonian Squid, a low-energy-content demersal–pelagic invertebrate. We also found an overall low prey diversity and important interannual variation for the main prey types, as well as variation between the different breeding stages. This study therefore contributes new and unambiguous information about the Red-legged Cormorant’s use of trophic resources and suggests that the combination of a conventional technique with stable isotope analysis provides a solid framework for this seabird diet assessment.

Additional keywords: Argentina, mixing model, Patagonia, shag, stable isotope analysis, trophic ecology.


References

Barrett, R. T., Camphuysen, K., Anker-Nilssen, T., Chardine, J. W., Furness, R. W., Garthe, S., Hislop, 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, 1675–1691.
Diet studies of seabirds: a review and recommendations.Crossref | GoogleScholarGoogle Scholar |

BirdLife International (2012). Phalacrocorax gaimardi. The IUCN Red List of Threatened Species 2012: e.T22696898A38025856. Available at: http://dx.doi.org/10.2305

Bond, A. L., and Diamond, A. W. (2011). Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecological Applications 21, 1017–1023.
Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors.Crossref | GoogleScholarGoogle Scholar | 21774408PubMed |

Bond, A. L., and Jones, I. L. (2009). A practical introduction to stable-isotope analysis for seabird biologists: approaches, cautions and caveats. Marine Ornithology 37, 183–188.

Boschi, E. E., Fischbach, C. E., and Iorio, M. I. (1992). Catálogo ilustrado de los crustáceos estomatópodos y decapodos marinos de Argentina. Frente Marítimo 10, 7–94.

Bovcon, N. D., Cochia, P. D., and Gosztonyi, A. E. (2007). Guía para el reconocimiento de los peces capturados por buques pesqueros monitoreados con observadores a bordo. Publicación especial de la Secretaría de Pesca de la Provincia del Chubut, Rawson, Argentina.

Bugoni, L., McGill, R. A., and Furness, R. W. (2008). Effects of preservation methods on stable isotope signatures in bird tissues. Rapid Communications in Mass Spectrometry 22, 2457–2462.
Effects of preservation methods on stable isotope signatures in bird tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVehtbjP&md5=c1d047c1c671cb63b4dd7b5a735e0065CAS | 18642324PubMed |

Casaux, R. J., Favero, M., Barrera-Oro, E. R., and Silva, P. (1995). Feeding trial on an Imperial Cormorant Phalacrocorax atriceps: preliminary results on fish intake and otolith digestion. Marine Ornithology 23, 101–106.

Cherel, Y., Hobson, K. A., and Hassani, S. (2005). Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiological and Biochemical Zoology 78, 106–115.
Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild.Crossref | GoogleScholarGoogle Scholar | 15702469PubMed |

Ciancio, J. E., Pascual, M. A., and Beauchamp, D. A. (2007). Energy density of Patagonian aquatic organisms and empirical predictions based on water content. Transactions of the American Fisheries Society 136, 1415–1422.
Energy density of Patagonian aquatic organisms and empirical predictions based on water content.Crossref | GoogleScholarGoogle Scholar |

Ciancio, J., Botto, F., and Frere, E. (2015). Combining a geographic information system, known dietary, foraging and habitat preferences, and stable isotope analysis to infer the diet of Magellanic Penguins in their austral distribution. Emu 115, 237–246.
Combining a geographic information system, known dietary, foraging and habitat preferences, and stable isotope analysis to infer the diet of Magellanic Penguins in their austral distribution.Crossref | GoogleScholarGoogle Scholar |

Clarke, K. R., and Warwick, R. M. (2001). ‘Changes in Marine Communities: An Approach to Statistical Analysis and Interpretation.’ 2nd edn. (Primer-E Ltd.: Plymouth, UK.)

Cousseau, M. B., and Gru, D. L. (1982). Estudio de edad y crecimiento de la sardina fueguina (Sprattus fuegensis) de las costas de la provincia de Santa Cruz e Islas Malvinas. Revista de Investigación y Desarrollo Pesquero 3, 51–58.

Craig, E. C., Dorr, B. S., Hanson-Dorr, K. C., Sparks, J. P., and Curtis, P. D. (2015). Isotopic discrimination in the Double-crested Cormorant (Phalacrocorax auritus). PLoS ONE 10, e0140946.
Isotopic discrimination in the Double-crested Cormorant (Phalacrocorax auritus).Crossref | GoogleScholarGoogle Scholar | 26473353PubMed |

Davoren, G. K., and Burger, A. E. (1999). Differences in prey selection and behaviour during self-feeding and chick provisioning in rhinoceros auklets. Animal Behaviour 58, 853–863.
Differences in prey selection and behaviour during self-feeding and chick provisioning in rhinoceros auklets.Crossref | GoogleScholarGoogle Scholar | 10512659PubMed |

Derby, C. E., and Lovvorn, J. R. (1997). Comparison of pellets versus collected birds for sampling diets of double-crested cormorants. The Condor 99, 549–553.
Comparison of pellets versus collected birds for sampling diets of double-crested cormorants.Crossref | GoogleScholarGoogle Scholar |

Duffy, D. C. (1990). Seabirds and the 1982–1984 El Niño–southern oscillation. Elsevier oceanography series 52, 395–415.
Seabirds and the 1982–1984 El Niño–southern oscillation.Crossref | GoogleScholarGoogle Scholar |

Frere, E., Quintana, F., and Gandini, P. (2002). Diving behavior of the Red-legged Cormorant in southeastern Patagonia, Argentina. The Condor 104, 440–444.
Diving behavior of the Red-legged Cormorant in southeastern Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |

Frere, E., Quintana, F., and Gandini, P. (2005). Cormoranes de la costa patagónica: estado poblacional, ecología y conservación. El hornero 20, 35–52.

Furness, R. W., and Camphuysen, K. C. (1997). Seabirds as monitors of the marine environment. ICES Journal of Marine Science 54, 726–737.
Seabirds as monitors of the marine environment.Crossref | GoogleScholarGoogle Scholar |

Gandini, P., Frere, E., and Quintana, F. (2005). Feeding performance and foraging area of the Red-legged Cormorant. Waterbirds 28, 41–45.
Feeding performance and foraging area of the Red-legged Cormorant.Crossref | GoogleScholarGoogle Scholar |

Gosztonyi, A. E., and Kuba, L. (1996). Atlas de huesos craneales y de la cintura escapular de peces costeros patagónicos. Informe Técnico del plan de manejo integrado de la zona costera patagónica n°4, Fundación Patagonia Natural, Puerto Madryn, Argentina.

Hansen, J. E. (1999). Estimación de parámetros poblacionales del efectivo de sardina fueguina (Sprattus fuegensis) de la costa continental Argentina. Informe Técnico 27, INIDEP, Mar del Plata, Argentina.

Hobson, K. A., Gloutney, M. L., and Gibbs, H. L. (1997). Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotope analysis. Canadian Journal of Zoology 75, 1720–1723.
Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotope analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntlOisbk%3D&md5=61358a925f1763d757b1219f8b4c4878CAS |

Inger, R., and Bearhop, S. (2008). Applications of stable isotope analyses to avian ecology. The Ibis 150, 447–461.
Applications of stable isotope analyses to avian ecology.Crossref | GoogleScholarGoogle Scholar |

Logan, J. M., Jardine, T. D., Miller, T. J., Bunn, S. E., Cunjak, R. A., and Lutcavage, M. E. (2008). Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. Journal of Animal Ecology 77, 838–846.
Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods.Crossref | GoogleScholarGoogle Scholar | 18489570PubMed |

López-Lanús, B., Grilli, P., Coconier, E., Di Giacomo, A., and Banchs, R. (2008). Categorización de las aves de la Argentina según su estado de conservación. Informe de Aves Argentinas/AOP y Secretaría de Ambiente y Desarrollo Sustentable. Buenos Aires, Argentina.

Menni, R. C., Ringuelet, R. A., and Arambaru, R. H. (1984). Peces marinos de la Argentina y Uruguay. Editorial Hemisferio Sur S.A. Buenos Aires, Argentina.

Millones, A., and Frere, E. (2012). Environmental factors affecting the distribution of the Red-Legged Cormorant in Argentina: a regional scale approach. Waterbirds 35, 230–238.
Environmental factors affecting the distribution of the Red-Legged Cormorant in Argentina: a regional scale approach.Crossref | GoogleScholarGoogle Scholar |

Millones, A., Frere, E., and Gandini, P. (2005). Dieta del cormorán gris (Phalacrocorax gaimardi) en la Ría Deseado, Santa Cruz, Argentina. Ornitologia Neotropical 16, 519–527.

Millones, A., Gandini, P., and Frere, E. (2015). Long-term population trends of the Red-legged Cormorant Phalacrocorax gaimardi on the Argentine coast. Bird Conservation International 25, 234–241.
Long-term population trends of the Red-legged Cormorant Phalacrocorax gaimardi on the Argentine coast.Crossref | GoogleScholarGoogle Scholar |

Nasca, P. B., Gandini, P. A., and Frere, E. (2004). Caracterización de las asociaciones de alimentación multiespecíficas de aves marinas en la Ría Deseado, Santa Cruz, Argentina El hornero 19, 29–36.

Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, H. H., and Wagner, H. (2016). Vegan: community ecology package. R package version 2.3–4. Available at: https://CRAN.R-project.org/package=vegan.

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.
Source partitioning using stable isotopes: coping with too much variation.Crossref | GoogleScholarGoogle Scholar | 20300637PubMed |

Phillips, D. L., and Gregg, J. W. (2001). Uncertainty in source partitioning using stable isotopes. Oecologia 127, 171–179.
Uncertainty in source partitioning using stable isotopes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cvptlClug%3D%3D&md5=ef1a4b2fef0ce6e4ecc65ce17b6f9b70CAS | 24577646PubMed |

Pineda, S. E., Aubone, A., and Brunetti, N. E. (1996). Identificación y morfometría comparada de las mandíbulas de Loligo gahi y Loligo sanpaulensis (Cephalopoda, Loliginidae) del atlántico sudoccidental. Revista de Investigación y Desarrollo Pesquero 10, 85–99.

Post, D., Layman, C., Arrington, D., Takimoto, G., Quattrochi, J., and Montaña, C. (2007). Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179–189.
Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses.Crossref | GoogleScholarGoogle Scholar | 17225157PubMed |

R Core Team (2014). ‘R: A Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna, Austria.) Available at: http://www.R-project.org.

Schreiber, R. W., and Clapp, R. B. (1987). Pelecaniform feeding ecology. In ‘Seabirds: Feeding Ecology and Role in Marine Ecosystems’. (Ed. J. P. Croxall.) pp. 173–188. (Cambridge University Press.)

Sears, J., Hatch, S. A., and O’Brien, D. M. (2009). Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 159, 41–48.
Disentangling effects of growth and nutritional status on seabird stable isotope ratios.Crossref | GoogleScholarGoogle Scholar | 18975007PubMed |

Smith, J. A., Mazumder, D., Suthers, I. M., and Taylor, M. D. (2013). To fit or not to fit: evaluating stable isotope mixing models using simulated mixing polygons. Methods in Ecology and Evolution 4, 612–618.
To fit or not to fit: evaluating stable isotope mixing models using simulated mixing polygons.Crossref | GoogleScholarGoogle Scholar |

Suryan, R. M., Irons, D. B., Brown, E. D., Jodice, P. G., and Roby, D. D. (2006). Site-specific effects on productivity of an upper trophic-level marine predator: bottom-up, top-down, and mismatch effects on reproduction in a colonial seabird. Progress in Oceanography 68, 303–328.
Site-specific effects on productivity of an upper trophic-level marine predator: bottom-up, top-down, and mismatch effects on reproduction in a colonial seabird.Crossref | GoogleScholarGoogle Scholar |

Therrien, J. F., Fitzgerald, G., Gauthier, G., and Bêty, J. (2011). Diet–tissue discrimination factors of carbon and nitrogen stable isotopes in blood of Snowy Owl (Bubo scandiacus). Canadian Journal of Zoology 89, 343–347.
Diet–tissue discrimination factors of carbon and nitrogen stable isotopes in blood of Snowy Owl (Bubo scandiacus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntlKgt7g%3D&md5=4a3b72842c7fa5358d7dcd5cdfc7ff9dCAS |

Tramer, E. J. (1969). Bird species diversity: components of Shannon’s formula. Ecology 97, 927–929.
Bird species diversity: components of Shannon’s formula.Crossref | GoogleScholarGoogle Scholar |

Turner, T. F., Collyer, M. L., and Krabbenhoft, T. J. (2010). A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91, 2227–2233.
A general hypothesis-testing framework for stable isotope ratios in ecological studies.Crossref | GoogleScholarGoogle Scholar | 20836444PubMed |

Volpedo, A. V., and Echeverría, D. D. (2000). ‘Catálogo y Claves de Otolitos para la Identificación de Peces del Mar Argentino.’ Vol. 1. (Editorial Dunken.)

Votier, S. C., Bearhop, S., Witt, M. J., Inger, R., Thompson, D., and Newton, J. (2010). Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. Journal of Applied Ecology 47, 487–497.
Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems.Crossref | GoogleScholarGoogle Scholar |

Zavalaga, C. B., Frere, E., and Gandini, P. (2002). Status of the Red-legged Cormorant in Perú: what factors affect distribution and numbers? Waterbirds 25, 8–15.
Status of the Red-legged Cormorant in Perú: what factors affect distribution and numbers?Crossref | GoogleScholarGoogle Scholar |