Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

A historical perspective of niche differentiation between two top predators in the Uruguayan coastal area

Florencia Artecona A , Maite De María A * , Leandro Bergamino B and Diana Szteren https://orcid.org/0000-0002-7632-0866 A C
+ Author Affiliations
- Author Affiliations

A Laboratorio de Zoología Vertebrados, Dpto de Ecología y Evolución, Facultad de Ciencias, Universidad de la República, Iguá 4225, Montevideo 11400, Uruguay.

B Centro Universitario Regional del Este, sede Rocha, Ruta nacional 9, intersección con ruta 15, Uruguay.

C Corresponding author. Email: diana@fcien.edu.uy

Wildlife Research 46(2) 136-144 https://doi.org/10.1071/WR17188
Submitted: 29 December 2017  Accepted: 17 November 2018   Published: 25 February 2019

Abstract

Context: As top predators, marine mammals play a key role consuming in different trophic levels and the trophic niche characterization may help to understand how species utilize and share resources . On the coast of the Río de la Plata and the South-west Atlantic, the South American sea lion (Otaria flavescens) and the franciscana dolphin (Pontoporia blainvillei) are two important predators.

Aims: The present study investigated potential trophic overlap of both species by measuring stable carbon (δ13C) and nitrogen (δ15N) isotopes over two periods: historical (1959–79) and recent (2002–15) on the Uruguayan coast.

Methods: Bone samples of P. blainvillei and O. flavescens were used to determine the isotopic niche using the Stable Isotope Bayesian Ellipses in R (SIBER) analysis.

Key results: The isotopic niche did not overlap between species in any period. δ15N was higher in O. flavescens in both periods (20.29‰ ± 0.73 in the historical and 19.95‰ ± 1.0 in the recent period), indicating that it feeds at a higher trophic level than P. blainvillei. The δ13C was also significantly higher in O. flavescens than in P. blainvillei during the two periods (O. flavescens: –11.43 ± 0.6‰ historic, –12.72 ± 0.4‰ recent, and P. blainvillei: –12.69 ± 1.1‰ historic, –13.84 ± 1.3‰ recent). The isotopic niche areas of P. blainvillei in recent and historic periods confirmed they forage in 2 distinct environments, marine and estuarine, with low isotopic overlap. This overlap was higher in the recent period.

Conclusions and Implications: O. flavescens and both P. blainvillei groups were segregated in both periods, with a higher overlap in the recent. These species appear to reduce competition by using different resources in the same coastal habitat. O. flavescens preferentially feeds on benthic fish and showed wider trophic amplitude in both periods, whereas P. blainvillei has a more coastal–pelagic diet and included a greater variability of resources in its diet. The differences between species trophic niches can still be detected after both marine mammals species abundance has declined and after the development of fisheries.

Additional keywords: stable isotopes, Pontoporia blainvillei, Otaria flavescens, SIBER analysis.


References

Ambrose, S. H. (1990). Preparation and characterization of bone and tooth collagen for isotopic analysis. Journal of Archaeological Science 17, 431–451.
Preparation and characterization of bone and tooth collagen for isotopic analysis.Crossref | GoogleScholarGoogle Scholar |

Arim, M., Bozinovic, F., and Marquet, P. (2007). On the relationship between trophic position, body mass and temperature: reformulation the energy limitation hypothesis. Oikos 116, 1524–1530.
On the relationship between trophic position, body mass and temperature: reformulation the energy limitation hypothesis.Crossref | GoogleScholarGoogle Scholar |

Aurioles-Gamboa, D., and Camacho-Ríos, F. J. (2007). Diet and feeding overlap of two otariids, Zalophus californianus and Arctocephalus townsendi: implications to survive environmental uncertainty. Aquatic Mammals 33, 315–326.
Diet and feeding overlap of two otariids, Zalophus californianus and Arctocephalus townsendi: implications to survive environmental uncertainty.Crossref | GoogleScholarGoogle Scholar |

Bassoi, M. (2005). Feeding ecology of franciscana dolphin, Pontoporia blainvillei (Cetacea: Pontoporiidae), and oceanographic processes on the Southern Brazilian coast. Ph.D. Thesis, University of Southampton, UK.

Bearhop, S., Adams, C., Waldron, 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.
Determining trophic niche width: a novel approach using stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |

Bergamino, L., Szteren, D., and Lercari, D. (2012). Trophic impacts of marine mammals and seabirds in the Rio de la Plata Estuary and the nearshore oceanic ecosystem. Estuaries and Coasts 35, 1571–1582.
Trophic impacts of marine mammals and seabirds in the Rio de la Plata Estuary and the nearshore oceanic ecosystem.Crossref | GoogleScholarGoogle Scholar |

Bligh, E. G., and Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 379, 911–917.

Boecklen, W. J., Yarnes, C. T., Cook, B. A., and James, A. C. (2011). On the use of stable isotopes in trophic ecology. Annual Review of Ecology Evolution and Systematics 42, 411–440.
On the use of stable isotopes in trophic ecology.Crossref | GoogleScholarGoogle Scholar |

Botta, S., Secchi, E. R., Rogers, T. L., Prado, J. H., de Lima, R. C., Carlini, P., and Negrete, J. (2018). Isotopic niche overlap and partition among three Antarctic seals from the western Antarctic Peninsula. Deep-sea Research. Part II, Topical Studies in Oceanography 149, 240–249.
Isotopic niche overlap and partition among three Antarctic seals from the western Antarctic Peninsula.Crossref | GoogleScholarGoogle Scholar |

Botto, F., Gaitán, E., Mianzan, H., Acha, M., Giberto, D., Schiariti, A., and Iribarne, O. (2011). Origin of resources and trophic pathways in large SW Atlantic estuary: an evaluation using stable isotopes. Estuarine, Coastal and Shelf Science 92, 70–77.
Origin of resources and trophic pathways in large SW Atlantic estuary: an evaluation using stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Bowen, W. D. (1997). Role of marine mammals in aquatic ecosystems. Marine Ecology Progress Series 158, 267–274.
Role of marine mammals in aquatic ecosystems.Crossref | GoogleScholarGoogle Scholar |

Bueno, C., Brugnoli, E., Bergamino, L., Muniz, P., García-Rodríguez, F., and Figueira, R. (2018). Anthropogenic and natural variability in the composition of sedimentary organic matter of the urbanised coastal zone of Montevideo (Río de la Plata). Marine Pollution Bulletin 126, 197–203.
Anthropogenic and natural variability in the composition of sedimentary organic matter of the urbanised coastal zone of Montevideo (Río de la Plata).Crossref | GoogleScholarGoogle Scholar | 29421089PubMed |

Burton, R. K., and Koch, P. L. (1999). Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds. Oecologia 119, 578–585.
Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds.Crossref | GoogleScholarGoogle Scholar | 28307717PubMed |

Cappozzo, H. L. (2002). South American sea lion Otaria flavescens. In ‘Encyclopedia of Marine Mammals’. (Eds W. F Perrin, B. Wursig and J. G. M. Thewissen.) pp. 1143–1146. (Academic Press: San Diego, CA.)

Casper, R., Gales, N., Hindell, M., and Robinson, S. (2006). Diet estimation based on an integrated mixed prey feeding experiment using Artocephalus seals. Journal of Experimental Marine Biology and Ecology 328, 228–239.
Diet estimation based on an integrated mixed prey feeding experiment using Artocephalus seals.Crossref | GoogleScholarGoogle Scholar |

Chase, J. M., and Leibold, M. A. (Eds) (2003). ‘Ecological Niches: Linking Classical and Contemporary Approaches.’ (University of Chicago Press: Chicago, IL.)

Christensen, J. T., and Richardson, K. (2008). Stable isotope evidence of long-term changes in the North Sea food web structure. Marine Ecology Progress Series 368, 1–8.
Stable isotope evidence of long-term changes in the North Sea food web structure.Crossref | GoogleScholarGoogle Scholar |

Costa-Urrutia, P., Abud, C., Secchi, E. R., and Lessa, E. P. (2012). Population genetic structure and social kin associations of Franciscana dolphin, Pontoporia blainvillei. The Journal of Heredity 103, 92–102.
Population genetic structure and social kin associations of Franciscana dolphin, Pontoporia blainvillei.Crossref | GoogleScholarGoogle Scholar | 22013080PubMed |

Cremer, M., Pinheiro, P., and Simoes-Lopes, P. (2012). Prey consumed by Guiana dolphin Sotalia guianesis (Cetacea, Delphinidae) and franciscana dolphin Pontoporia blainvillei (Cetacea, Pontoporiidae) in an estuarine environment in southern Brazil. Iheringia. Série Zoologia 102, 131–137.
Prey consumed by Guiana dolphin Sotalia guianesis (Cetacea, Delphinidae) and franciscana dolphin Pontoporia blainvillei (Cetacea, Pontoporiidae) in an estuarine environment in southern Brazil.Crossref | GoogleScholarGoogle Scholar |

Crespo, E. A. (2002). Franciscana Pontoporia blainvillei. In ‘Encyclopedia of Marine Mammals’. (Eds W. F. Perrin, B. Wursig and J. G. M. Thewissen.) pp. 482–485. (Academic Press: San Diego, CA.)

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.
The effect of anthropogenic CO2 on the carbon isotope composition of marine phytoplankton.Crossref | GoogleScholarGoogle Scholar |

Defeo, O., Horta, S., Carranza, A., Lercari, D., De Alava, A., Gómez, J., Lozoya, J. C., Martínez, G., and Celentano, E. (2009). ‘Hacia un manejo ecosistémico de pesquerías: Áreas Marinas Protegidas en Uruguay.’ (Facultad de Ciencias-DINARA: Montevideo, Uruguay.)

Defeo, O., Puig, P., Horta, S., and de Alava, A. (2011). Coastal fisheries of Uruguay. In ‘Coastal Fisheries of Latin America and the Caribbean’. (Eds S. Salas, R. Chuenpagdee, A. Charles and J.C. Seijo.) pp. 354–384. FAO Fisheries and Aquaculture Technical Paper No. 544. (FAO: Rome.)

DeNiro, M. J., and Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.
Influence of diet on the distribution of carbon isotopes in animals.Crossref | GoogleScholarGoogle Scholar |

DeNiro, M. J., and Epstein, S. (1981). Isotopic composition of cellulose from aquatic organisms. Geochimica et Cosmochimica Acta 45, 1885–1894.
Isotopic composition of cellulose from aquatic organisms.Crossref | GoogleScholarGoogle Scholar |

Denuncio, P., Paso Viola, M. N., Machovsky-Capuska, G. E., Raubenheimer, D., Blasina, G., Machado, R., Polizzi, P., Gerpe, M., Cappozzo, H. L., and Rodríguez, D. H. (2017). Population variance in prey, diets and their macronutrient composition in an endangered marine predator, the franciscana dolphin. Journal of Sea Research 129, 70–79.
Population variance in prey, diets and their macronutrient composition in an endangered marine predator, the franciscana dolphin.Crossref | GoogleScholarGoogle Scholar |

Di Beneditto, A. P. M., and Monteiro, L. R. (2016). Isotopic niche of two coastal dolphins in a tropical marine area: specific and age class comparisons. Journal of the Marine Biological Association of the United Kingdom 96, 853–858.
Isotopic niche of two coastal dolphins in a tropical marine area: specific and age class comparisons.Crossref | GoogleScholarGoogle Scholar |

Di Beneditto, A. P. M., De Souza, C. M. M., Amaral, H., and Rezende, C. E. (2011). Use of multiple tools to assess the feeding preference of coastal dolphins. Marine Biology 158, 2209–2217.
Use of multiple tools to assess the feeding preference of coastal dolphins.Crossref | GoogleScholarGoogle Scholar |

Emerson, B. C., and Gillespie, R. G. (2008). Phylogenetic analysis of community assembly and structure over space and time. Trends in Ecology & Evolution 23, 619–630.
Phylogenetic analysis of community assembly and structure over space and time.Crossref | GoogleScholarGoogle Scholar |

Estes, J. (2009). Ecological effects of marine mammals. In ‘Encyclopedia of Marine Mammals’. 2nd edn. (Eds W. Perrin, B. Würsig and J. Thewissen.) pp. 357–361. (Elsevier: Amsterdam.)

France, R. L. (1995). Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Marine Ecology Progress Series 124, 307–312.
Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications.Crossref | GoogleScholarGoogle Scholar |

Francey, R. J., Allison, C. E., Etheridge, D. M., Trudinger, C. M., Enting, I. G., Leuenberger, M., and Steele, L. P. (1999). A 1000-year high precision record of δ13C in atmospheric CO2. Tellus B 51, 170–193.
A 1000-year high precision record of δ13C in atmospheric CO2.Crossref | GoogleScholarGoogle Scholar |

Franco-Trecu, V., Aurioles-Gamboa, D., Arim, M., and Lima, M. (2012). Prepartum and postpartum trophic segregation between sympatrically breeding female Arctocephalus australis and Otaria flavescens. Journal of Mammalogy 93, 514–521.
Prepartum and postpartum trophic segregation between sympatrically breeding female Arctocephalus australis and Otaria flavescens.Crossref | GoogleScholarGoogle Scholar |

Franco-Trecu, V., Aurioles-Gambia, D., and Inchausti, P. (2014). Individual trophic specialisation and niche segregation explain the contrasting population trends of two sympatric otariids. Marine Biology 161, 609–618.
Individual trophic specialisation and niche segregation explain the contrasting population trends of two sympatric otariids.Crossref | GoogleScholarGoogle Scholar |

Franco-Trecu, V., Drago, M., Baladán, C., García-Olazábal, M. D., Crespo, E. A., Cardona, L., and Inchausti, P. (2015). Postharvesting population dynamics of the South American sea lion (Otaria byronia) in the southwestern Atlantic. Marine Mammal Science 31, 963–978.
Postharvesting population dynamics of the South American sea lion (Otaria byronia) in the southwestern Atlantic.Crossref | GoogleScholarGoogle Scholar |

Franco-Trecu, V., Drago, M., Costa, P., Dimitriadis, C., and Passadore, C. (2017). Trophic relationships in apex predators in an estuary system: a multiple-method approximation. Journal of Experimental Marine Biology and Ecology 486, 230–236.
Trophic relationships in apex predators in an estuary system: a multiple-method approximation.Crossref | GoogleScholarGoogle Scholar |

Garreaud, R. D., Vuille, M., Compagnucci, R., and Marengo, J. (2009). Present-day South American climate. Palaeogeography, Palaeoclimatology, Palaeoecology 281, 180–195.
Present-day South American climate.Crossref | GoogleScholarGoogle Scholar |

Gianelli, I., and Defeo, O. (2017). Uruguayan fisheries under an increasingly globalized scenario: long-term landings and bioeconomic trends. Fisheries Research 190, 53–60.
Uruguayan fisheries under an increasingly globalized scenario: long-term landings and bioeconomic trends.Crossref | GoogleScholarGoogle Scholar |

Giménez, J., Cañada, A., Ramírez, F., Afán, I., García-Tiscar, S., Fernandéz-Maldonado, C., Castillo, J., and Stephanis, R. (2018). Living apart together: niche partitioning among Alboran Sea cetaceans. Ecological Indicators 95, 32–40.
Living apart together: niche partitioning among Alboran Sea cetaceans.Crossref | GoogleScholarGoogle Scholar |

Gómez-Erache, M., Conde, M. D., and Villarmarzo, R. (Eds) (2010). ‘The Sustainability of Integrated Management in the Coastal Zone of Uruguay.’ (ECOPLATA/IDRC: Montevideo, Uruguay.)

Heithaus, M. R., Frid, A., Wirsing, A. J., and Worm, B. (2008). Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution 23, 202–210.
Predicting ecological consequences of marine top predator declines.Crossref | GoogleScholarGoogle Scholar |

Hobson, K. A., Piatt, J. F., and Pitocchelli, J. (1994). Using stable isotopes to determine seabird trophic relationships. Journal of Animal Ecology 63, 786–798.
Using stable isotopes to determine seabird trophic relationships.Crossref | GoogleScholarGoogle Scholar |

Jackson, A., Inger, R., Parnell, A., and Bearhop, S. (2011). Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80, 595–602.
Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses in R.Crossref | GoogleScholarGoogle Scholar | 21401589PubMed |

Jaureguizar, A., and Milessi, A. (2008). Assessing the sources of the fishing down marine food web process in the Argentinean–Uruguayan Common Fishing Zone. Scientia Marina 72, 25–36.

Kelly, J. F. (2000). Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78, 1–27.
Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology.Crossref | GoogleScholarGoogle Scholar |

Layman, C. A., Arrington, D. A., Montaña, C. G., and Post, D. M. (2007). Can stable isotope ratios provide community-wide measures of trophic structure? Ecology 88, 42–48.
Can stable isotope ratios provide community-wide measures of trophic structure?Crossref | GoogleScholarGoogle Scholar | 17489452PubMed |

Layman, C. A., Araujo, M. S., Boucek, R., Harrison, E., Jud, Z. R., Matich, P., Hammerschlag-Peyer, C. M., Rosenblatt, A. E., Vaudo, J. J., Yeager, L. A., Post, D., and Bearhop, S. (2012). Applying stable isotopes to examine food web structure: an overview of analytical tools. Biological Reviews of the Cambridge Philosophical Society 87, 545–562.
Applying stable isotopes to examine food web structure: an overview of analytical tools.Crossref | GoogleScholarGoogle Scholar | 22051097PubMed |

Lercari, D., Vögler, R., Milessi, A., Jaureguizar, A., and Velazco, G. (2014). Trophic models in the Southwestern Atlantic Ocean: evaluating structure and functioning of coastal ecosystem. In ‘Ecopath 30 Years Conference Proceedings: Extended Abstracts’. (Eds J. Steenbeek, C. Piroddi, M. Coll, J. J. Heymans, S. Villasante and V. Christensen.) pp. 75–77. Fisheries Centre Research Reports 22(3). (Fisheries Centre, University of British Columbia: Canada.)

Lorenzo, M. I., Defeo, O., Roshan Moniri, N., and Zylich, K. (2016). Uruguay. In ‘Global Atlas of Marine Fisheries: A Critical Appraisal of Catches and Ecosystem’. (Eds D. Pauly and D. Zeller.) pp. 439. (Island Press: Washington, DC.)

Madin, E. M., Dill, L. M., Ridlon, A. D., Heithaus, M. R., and Warner, R. R. (2016). Human activities change marine ecosystems by altering predation risk. Global Change Biology 22, 44–60.
Human activities change marine ecosystems by altering predation risk.Crossref | GoogleScholarGoogle Scholar | 26448058PubMed |

Marrero, A., Tuduri, A., Pérez, L., Cuña, C., Muniz, P., Lopes Figueira, R. C., Michaelovitch de Mahiques, M., Alves de Lima, P., Pittauerova, D., Hanebuth, T., and García-Rodríguez, F. (2014). Cambios históricos en el aporte terrígeno de la cuenca del Río de la Plata sobre la plataforma interna uruguaya. Latin American Journal of Sedimentology and Basin Analysis 21, 165–179.

Mauas, P. J., Flamenco, E., and Buccino, A. P. (2008). Solar forcing of the stream flow of a continental scale South American river. Physical Review Letters 101, 168501.
Solar forcing of the stream flow of a continental scale South American river.Crossref | GoogleScholarGoogle Scholar | 18999720PubMed |

Menafra, R., Conde, D., Roche, I., Gorfinkiel, D., Píriz, C., Baliero, W., Biasco, E., Fossati, M., Lorenzo, E., Cortazzo, R., and Fournier, R. (2009). Challenges and perspectives for integrated coastal management in Uruguay. Ocean Yearbook 23, 403–432.
Challenges and perspectives for integrated coastal management in Uruguay.Crossref | GoogleScholarGoogle Scholar |

Mendez, M., Rosenbaum, H. C., and Bordino, P. (2008). Conservation genetics of the franciscana dolphin in Northern Argentina: population structure, by-catch impacts, and management implications. ‎ Conservation Genetics 9, 419–435.
Conservation genetics of the franciscana dolphin in Northern Argentina: population structure, by-catch impacts, and management implications. ‎Crossref | GoogleScholarGoogle Scholar |

Mianzan, H., Lasta, C., Acha, E., Guerrero, R., Macchi, G., and Bremec, C. (2001). The Rio de la Plata estuary, Argentina–Uruguay. In ‘Coastal Marine Ecosystems of Latin America’. (Eds U. Seeliger and B. Kjerfve.) pp. 185–204. (Springer Verlag: Heidelberg, Germany.)

Michener, R., and Kaufman, L. (2007). Stable isotope ratio as tracers in marine food webs: an update. In ‘Stable Isotopes in Ecology and Environmental Science’. 2nd edn. (Eds R. Michener and K. Lajtha.) pp. 238–282. (Blackwell: Oxford, UK.)

Milessi, A., and Jaureguizar, A. (2013). Evolución temporal del nivel trófico medio de los desembarques en la Zona Común de Pesca Argentino-Uruguaya años 1989–2010. Frente Marítimo 23, 83–93.

Naya, D., Vargas, R., and Arim, M. (2000). Análisis preliminar de la dieta del león marino del sur (Otaria flavescens) en Isla de Lobos Uruguay. Boletin de la Sociedad Zoológica del Uruguay 12, 14–21.

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.
A niche for isotopic ecology.Crossref | GoogleScholarGoogle Scholar |

Newsome, S. D., Clementz, M. T., and Koch, P. L. (2010). Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science 26, 509–572.

Páez, E. (2006). Situación de la administración del recurso lobos y leones marinos en Uruguay. In ‘Bases para la conservación y el manejo de la costa uruguaya’. (Eds R. Menafra, L. Rodríguez-Gallego, F. Scarabino and D. Conde.) pp. 577–583. (Vida Silvestre, Sociedad Uruguaya para la Conservación de la Naturaleza: Montevideo, Uruguay.)

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 424, 424–425.
Stable isotopes indicate differing foraging strategies in two sympatric otariids of the Galapagos Islands. ‎Crossref | GoogleScholarGoogle Scholar |

Paso-Viola, M. N., Denuncio, P., Negri, M. F., Rodriguez, D., Bastida, R., and Cappozzo, H. L. (2014). Diet composition of franciscana dolphin Pontoporia blainvillei from southern Buenos Aires, Argentina and its interaction with fisheries. Revista de Biología Marina y Oceanografía 49, 393–400.
Diet composition of franciscana dolphin Pontoporia blainvillei from southern Buenos Aires, Argentina and its interaction with fisheries.Crossref | GoogleScholarGoogle Scholar |

Pauly, D., Trites, A. W., Capuli, E., and Christensen, V. (1998a). Diet composition and trophic levels of marine mammals. ICES Journal of Marine Science 55, 467–481.
Diet composition and trophic levels of marine mammals.Crossref | GoogleScholarGoogle Scholar |

Pauly, D., Christensen, V., Dalsgaard, J., Froese, R., and Torres, F. (1998b). Fishing down marine foods webs. Science 279, 860–863.
Fishing down marine foods webs.Crossref | GoogleScholarGoogle Scholar | 9452385PubMed |

Peterson, B. J., and Fry, B. (1987). Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293–320.
Stable isotopes in ecosystem studies.Crossref | GoogleScholarGoogle Scholar |

Pimm, S. (Ed.) (2002). ‘Food Webs’. 2nd edn. (The University of Chicago Press: Chicago, IL.)

Post, D. (2002). Using stable isotopes to estimate trophic position models, methods and assumptions. Ecology 83, 703–718.
Using stable isotopes to estimate trophic position models, methods and assumptions.Crossref | GoogleScholarGoogle Scholar |

Reeves, R. R., Dalebout, M. L., Jefferson, T. A., Karczmarski, L., Laidre, K., O’Corry-Crowe, G., Rojas-Bracho, L., Secchi, E. R., Slooten, E., Smith, B. D., Wang, J. Y., Zerbini, A. N., and Zhou, K. (2008). Pontoporia blainvillei. In ‘IUCN 2012, IUCN Red List of Threatened Species’. Available at www.iucnredlist.org [Verified December 2018]

Riet-Sapriza, F., Costa, D. P., Franco-Trecu, V., Marin, Y., Chocca, H., González, B., Beathyate, G., Chilvers, B. L., and Huckstadt, L. A. (2013). Foraging behavior of lactating South American sea lions (Otaria flavescens) and spatial–temporal resource overlap with the Uruguayan fisheries. Deep-sea Research. Part II, Topical Studies in Oceanography 88-89, 106–119.
Foraging behavior of lactating South American sea lions (Otaria flavescens) and spatial–temporal resource overlap with the Uruguayan fisheries.Crossref | GoogleScholarGoogle Scholar |

Riofrío-Lazo, M., and Aurioles-Gamboa, D. (2013). Timing of isotopic integration in marine mammal skull: comparative study between calcified tissues. Rapid Communications in Mass Spectrometry 27, 1076–1082.
Timing of isotopic integration in marine mammal skull: comparative study between calcified tissues.Crossref | GoogleScholarGoogle Scholar | 23592211PubMed |

Rodríguez, D., Rivero, L., and Bastida, R. (2002). Feeding ecology of the franciscana (Pontoporia blainvillei) in marine and estuarine waters of Argentina. The Latin American Journal of Aquatic Mammals 1, 77–94.
Feeding ecology of the franciscana (Pontoporia blainvillei) in marine and estuarine waters of Argentina.Crossref | GoogleScholarGoogle Scholar |

Rooney, N., McCann, K., Gellner, G., and Moore, J. C. (2006). Structural asymmetry and the stability of diverse food webs. Nature 442, 265–269.
Structural asymmetry and the stability of diverse food webs.Crossref | GoogleScholarGoogle Scholar | 16855582PubMed |

Schoener, T. (1974). Resource partitioning in ecological communities. Science 185, 27–39.
Resource partitioning in ecological communities.Crossref | GoogleScholarGoogle Scholar | 17779277PubMed |

Secchi, E. R., Danilewicz, D., and Ott, P. H. (2003). Applying the phylogeographic concept to identify franciscana dolphin stocks: implications to meet management objectives. The Journal of Cetacean Research and Management 5, 61–68.

Segura, A. M., Franco-Trecu, V., Franco-Fraguas, P., and Arim, M. (2015). Gape and energy limitation determine a humped relationship between trophic position and body size. Canadian Journal of Fisheries and Aquatic Sciences 72, 198–205.
Gape and energy limitation determine a humped relationship between trophic position and body size.Crossref | GoogleScholarGoogle Scholar |

Suárez, A., Sanfelice, D., Cassini, M., and Cappozzo, H. (2005). Composition and seasonal variation in the diet of the South American sea lion (Otaria flavescens) from Quequén, Argentina. The Latin American Journal of Aquatic Mammals 4, 163–174.
Composition and seasonal variation in the diet of the South American sea lion (Otaria flavescens) from Quequén, Argentina.Crossref | GoogleScholarGoogle Scholar |

Suess, H. E. (1955). Radiocarbon concentration in modern wood. Science 122, 415–417.
Radiocarbon concentration in modern wood.Crossref | GoogleScholarGoogle Scholar |

Trites, A. W., and Joy, R. (2005). Dietary analysis from fecal samples: how many scats are enough? Journal of Mammalogy 86, 704–712.
Dietary analysis from fecal samples: how many scats are enough?Crossref | GoogleScholarGoogle Scholar |

Varela, J., Rojo-Nieto, E., Sorell, J., and Medina, A. (2018). Using stable isotope analysis to assess trophic relationships between Atlantic bluefin tuna (Thunnus thynnus) and striped dolphin (Stenella coeruleoalba) in the Strait of Gibraltar. Marine Environmental Research 139, 57–63.
Using stable isotope analysis to assess trophic relationships between Atlantic bluefin tuna (Thunnus thynnus) and striped dolphin (Stenella coeruleoalba) in the Strait of Gibraltar.Crossref | GoogleScholarGoogle Scholar | 29754735PubMed |

Vaz-Ferreira, R. (1982). Otaria flavescens, South American sea lion. In ‘FAO Mammals in the Seas IV’. pp. 477–496. (FAO: Rome.)

Vögler, R., Arreguín-Sánchez, F., Lercari, D., del Monte-Luna, P., and Calliari, D. (2015). The effects of long-term climate variability on the trophodynamics of an estuarine ecosystem in southern South America. Ecological Modelling 317, 83–92.
The effects of long-term climate variability on the trophodynamics of an estuarine ecosystem in southern South America.Crossref | GoogleScholarGoogle Scholar |

Whitehead, H., MacLeod, C. D., and Rodhouse, P. (2003). Differences in niche breadth among some teuthivorous mesopelagic marine mammals. ‎ Marine Mammal Science 19, 400–406.
Differences in niche breadth among some teuthivorous mesopelagic marine mammals. ‎Crossref | GoogleScholarGoogle Scholar |

Zar, J. H. (1996). ‘Biostatistical Analysis.’ (Prentice Hall: Upper Saddle River, NJ.)