CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Emu   
  A Journal of BirdLife Australia
blank image Search
blank image blank image
blank image
  Advanced Search

Journal Home
About the Journal
Editorial Structure
Online Early
Current Issue
Just Accepted
All Issues
Special Issues
Research Fronts
Rowley Reviews
Virtual Issues
Sample Issue
For Authors
General Information
Submit Article
Author Instructions
Open Access
Awards and Prizes
For Referees
Referee Guidelines
Review an Article
Annual Referee Index
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates
Library Recommendation

red arrow Complete Archive
blank image
With the complete digital archive of Emu now online, we have selected some of the most interesting and significant papers for readers to access freely.

blue arrow e-Alerts
blank image
Subscribe to our Email Alert or RSS feeds for the latest journal papers.

red arrow Connect with BirdLife
blank image
facebook TwitterIcon LinkedIn

red arrow Connect with CP
blank image
facebook twitter logo LinkedIn


Article << Previous     |     Next >>   Contents Vol 116(3)

Assessing the trophic niche of South American Terns integrating conventional and isotopic methods

Alejandro J. Gatto A C and Pablo Yorio A B

A Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Boulevard Brown 2915, U9120ACV, Puerto Madryn, Chubut, Argentina.
B Wildlife Conservation Society, Amenabar 1595, Piso 2, Oficina 19, C1426AKC, Ciudad de Buenos Aires, Argentina.
C Corresponding author. Email: alegatto@cenpat-conicet.gob.ar

Emu 116(3) 230-240 http://dx.doi.org/10.1071/MU15010
Submitted: 24 January 2014  Accepted: 29 October 2015   Published: 7 March 2016

PDF (417 KB) $25
 Export Citation

Conventional dietary studies combined with stable isotope analysis allowed the characterisation of the trophic niche of South American Terns (Sterna hirundinacea) breeding in Argentina. Direct observation of prey deliveries during mate- and chick-provisioning showed that the diet of South American Terns comprised at least 18 prey items, mainly pelagic schooling fish with smaller proportions of marine invertebrates. Argentine Anchovy (Engraulis anchoita) was the main fish prey. Adults delivered a higher proportion of fish and smaller prey to their chicks than to their mates. Analysis of stable isotope ratios in blood samples, using Bayesian stable isotope mixing models, indicated that adult Terns used a higher proportion of marine invertebrates for self-feeding than for mate- or chick-provisioning. Analyses of stable isotopes ratios in blood samples from chicks were consistent with the determination of diet from direct observation, and indicated differences from adults in both the proportion of different prey in the diet and trophic niche. In addition, isotopic niche analysis showed that chicks had a significantly higher trophic position compared with self-feeding adults during both mate-provisioning and chick stages. The results highlight the importance of combining stable isotope and conventional methods to adequately assess the food requirements of a population during the breeding season.

Additional keywords: breeding diet, isotopic niche, Patagonia, prey provisioning, self-feeding, Sterna hirundinacea.


Agresti, A. (2002). ‘Categorical Data Analysis.’ (John Wiley & Sons: Hoboken, NJ.)

Alfaro, M., Mauco, L., Norbis, W., and Lima, M. (2011). Temporal variation on the diet of the South American Tern (Sterna hirundinacea, Charadriiformes:Laridae) on its wintering grounds. Revista Chilena de Historia Natural (Valparaiso, Chile) 84, 451–460.
CrossRef |

Barrett, R. T., Camphuysen, K. (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, 1675–1691.
CrossRef |

Barrett, R. T., Anker-Nilssen, T., Rikardsen, F., Valde, K., Røv, N., and Vader, W. (1987). The food, growth and fledging success of Norwegian Puffin chicks Fratercula arctica in 1980–1983. Ornis Scandinavica 18, 73–83.
CrossRef |

Bearhop, S., Waldron, S., Votier, S. C., and Furness, R. W. (2002). Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiological and Biochemical Zoology 75, 451–458.
CrossRef | CAS | PubMed |

Bearhop, S., Adams, C. E., Waldron, S., Fuller, R. A., and Macleod, H. (2004). Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73, 1007–1012.
CrossRef |

Bodey, T. W., Ward, E. J., Phillips, R. A., McGill, R. A. R., and Bearhop, S. (2014). Species versus guild level differentiation revealed across the annual cycle by isotopic niche examination. Journal of Animal Ecology 83, 470–478.
CrossRef | PubMed |

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.
CrossRef |

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.
CrossRef | PubMed |

Bradstreet, M. S. W., and Brown, R. G. B. (1985). Feeding ecology of the Atlantic Alcidae. In ‘The Atlantic Alcidae’. (Eds D. N. Nettleship and T. R.Birkhead.) pp. 264–318. (Harcourt Brace Jovanovich: Toronto.)

Bugoni, L., McGill, R. A. R., and Furness, R. W. (2008). Effects of preservation methods on stable isotope signatures in bird tissues. Rapid Communications in Mass Spectrometry 22, 2457–2462.
CrossRef | CAS | PubMed |

Burnham, K. P., and Anderson, D. R. (2002). ‘Model Selection and Multimodel Inference: A Practical Information Theoretic Approach.’ (Springer-Verlag: New York.)

Catry, T., Ramos, J. A., Paiva, V. H., Martins, J., Almeida, A., Palma, J., Andrade, P. J., Peste, F., Trigo, S., and Luís, A. (2006). Intercolony and annual differences in the diet and feeding ecology of Little Tern adults and chicks in Portugal. Condor 108, 366–376.
CrossRef |

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

Cherel, Y., Hobson, K. A., Bailleul, F., and Groscolas, R. (2005). Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86, 2881–2888.
CrossRef |

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.
CrossRef |

Ciancio, J. E., Pascual, M. A., Botto, F., Frere, E., and Iribarne, O. (2008). Trophic relationships of exotic anadromous salmonids in the southern Patagonian Shelf as inferred from stable isotopes. Limnology and Oceanography 53, 788–798.
CrossRef |

Crawford, R. J. M. (2004). Accounting for food requirements of seabirds in fisheries management: the case of the South African purse-seine fishery. African Journal of Marine Science 26, 197–203.
CrossRef |

Crawley, M. J. (2013). ‘The R Book.’ (Wiley: Chichester, UK.)

Cury, P. M., Boyd, I. L., Bonhommeau, S., Anker-Nilssen, T., Crawford, R. J. M., Furness, R. W., Mills, J. A., Murphy, E. J., Österblom, H., Paleczny, M., Piatt, J. F., Roux, J.-P., Shannon, L., and Sydeman, W. J. (2011). Global seabird response to forage fish depletion—one-third for the birds. Science 334, 1703–1706.
CrossRef | CAS | PubMed |

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.
CrossRef | PubMed |

Faraway, J. J. (2006). ‘Extending the Linear Model with R: Generalized Linear, Mixed Effects and Nonparametric Regression Models.’ (Chapman & Hall and CRC Press: Boca Raton, FL.)

Favero, M., Bó, M. S., Silva Rodríguez, M. P., and García-Mata, C. (2000). Food and feeding biology of the South American Tern during the nonbreeding season. Waterbirds 23, 125–129.

Fernández Ajó, A. A., Gatto, A., and Yorio, P. (2011). Patterns of prey provisioning in relation to chick age in the South American Tern (Sterna hirundinacea). Ornitologia Neotropical 22, 361–368.

Forero, M. G., Bortolotti, G. R., Hobson, K. A., Donazar, J. A., Bertellotti, M., and Blanco, G. (2004). High trophic overlap within the seabird community of Argentinean Patagonia: a multiscale approach. Journal of Animal Ecology 73, 789–801.
CrossRef |

Fracasso, H. A. A., Branco, J. O., and Barbieri, E. (2011). A comparison of foraging between the South American and Cabot’s Tern in southern Brazil. Biota Neotropica 11, 189–196.
CrossRef |

Fry, B. (2004). ‘Stable Isotope Ecology.’ (Springer: New York.)

Galván, D. E., Botto, F., Parma, A. M., Bandieri, L., Mohamed, N., and Iribarne, O. O. (2009). Food partitioning and spatial subsidy in shelter-limited fishes inhabiting patchy reefs of Patagonia. Journal of Fish Biology 75, 2585–2605.
CrossRef | PubMed |

García, G. O., Favero, M., and Vassallo, A. I. (2010). Factors affecting kleptoparasitism by gulls in a multi-species seabird colony. Condor 112, 521–529.
CrossRef |

Gatto, A. J., and Yorio, P. (2009). Provisioning of mates and chicks by Cayenne and Royal Terns: resource partitioning in northern Patagonia, Argentina. Emu 109, 49–55.
CrossRef |

Gochfeld, M., and Burger, J. (1996). Family Sternidae (Terns). In ‘Handbook of the Birds of the World. Vol. 3: Hoatzin to Auks’. (Eds J. Del Hoyo, A. Elliott and J. Sargatal.) pp. 624–667. (Lynx Edicions: Barcelona.)

Gotelli, N. J., and Entsminger, G. L. (2010). ‘EcoSim: Null Models Software for Ecology.’ (Acquired Intelligence Inc. & Kesey-Bear: Jericho, VT.)

Halley, D. J., Minagawa, M., Nieminen, M., and Gaare, E. (2008). Preservation in 70% ethanol solution does not affect δ13C and δ15N values of Reindeer blood samples – relevance for stable isotope studies of diet. Rangifer 28, 9–12.
CrossRef |

Hobson, K. A., and Clark, R. G. (1992). Assessing avian diets using stable isotopes II: Factors influencing diet-tissue fractionation. Condor 94, 189–197.
CrossRef |

Hobson, K. A., Gibbs, H. L., and Gloutney, M. L. (1997). Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotope analysis. Canadian Journal of Zoology 75, 1720–1723.
CrossRef | CAS |

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

Jackson, A. L., 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.
CrossRef | PubMed |

Jackson, M. C., Donohue, I., Jackson, A. L., Britton, J. R., Harper, D. M., and Grey, J. (2012). Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PLoS One 7, e31757.
CrossRef | CAS | PubMed |

Jaksic, F. M., and Marone, L. (2007). Nicho. In ‘Ecología de Comunidades’. (Eds F. M. Jaksic and L. Marone.) pp. 33–46. (Ediciones Universidad Católica de Chile: Santiago, Chile.)

Karnovsky, N. J., Hobson, K. A., and Iverson, S. J. (2012). From lavage to lipids: estimating diets of seabirds. Marine Ecology Progress Series 451, 263–284.
CrossRef | CAS |

Krebs, C. J. (1999). ‘Ecological Methodology.’ (Benjamin/Cummings & Addison-Wesley Educational Publishers: Menlo Park, CA.)

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

Lisnizer, N., Cotichelli, L., Yorio, P., Basso, N., and Gatto, A. (2014). Using morphometry and molecular markers for sexing South American, Cayenne and Royal Terns breeding in Patagonia, Argentina. Waterbirds 37, 183–190.
CrossRef |

Mariano-Jelicich, R., Silva Rodríguez, M. P., Copello, S., Seco Pon, J. P., Berón, M. P., Mauco, L., Ghys, M. I., and Favero, M. (2011). The diet of the South American Tern: the Argentine Anchovy as key prey in the non-breeding season. Emu 111, 292–296.
CrossRef |

McLeay, L. J., Page, B., Goldsworthy, S. D., Ward, T. M., and Paton, D. C. (2009). Size matters: variation in the diet of chick and adult Crested Terns. Marine Biology 156, 1765–1780.
CrossRef |

Milesi, F., and López de Casenave, J. (2005). El concepto de nicho en la ecología aplicada: del nicho al hecho hay mucho trecho. Ecología Austral 15, 131–148.

Montevecchi, W. A. (1993). Birds as indicators of change in marine prey stocks. In ‘Birds as Monitors of Environmental Change’. (Eds R. W. Furness and J. J. D. Greenwood.) pp. 217–266. (Chapman & Hall: London.)

Moore, J. W., and Semmens, B. X. (2008). Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11, 470–480.
CrossRef | PubMed |

Newsome, S. D., Martínez del Rio, C., Bearhop, S., and Phillips, D. L. (2007). A niche for isotopic ecology. Frontiers in Ecology and the Environment 5, 429–436.
CrossRef |

Nisbet, I. C. T. (1977). Courtship-feeding and clutch size in Common Terns Sterna hirundo. In ‘Evolutionary Ecology’. (Eds B. Stonehouse and C. Perrins.) pp. 101–109. (MacMillan: London.)

Nisbet, I. C. T. (2002). Common Tern (Sterna hirundo). In ‘The Birds of North America’. (Eds A. Poole and F. Gill.) (The Birds of North America, Inc.: Ithaca, NY.)

Parnell, A., and Jackson, A. (2013). SIAR: stable isotope analysis in R. (R package version 4.2). Available at http://CRAN.R-project.org/package=siar [Verified 23 January 2015].

Parnell, A., Inger, R., Bearhop, S., and Jackson, A. L. (2010). Source partitioning using stable isotopes: coping with too much variation. PLoS One 5, e9672.
CrossRef | PubMed |

Phillips, D. L., Inger, R., Bearhop, S., Jackson, A. L., Moore, J. W., Parnell, A. C., Semmens, B. X., and Ward, E. J. (2014). Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92, 823–835.
CrossRef |

Piatt, J. F., Sydeman, W. J., and Wiese, F. (2007). Introduction: a modern role for seabirds as indicators. Marine Ecology Progress Series 352, 199–204.
CrossRef |

Pierotti, R., and Annett, C. A. (1991). Diet choice in the Herring Gull: constraints imposed by reproductive and ecological factors. Ecology 72, 319–328.
CrossRef |

R Development 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/ [Verified 23 January 2015].

Ramos, J. A., Solá, E., Monteiro, L. R., and Ratcliffe, N. (1998). Prey delivered to Roseate Tern chicks in the Azores. Journal of Field Ornithology 69, 419–429.

Ramos, J. A., Maul, A. M., Bowler, J., Monticelli, D., and Pacheco, C. (2004). Laying date, chick provisioning, and breeding success of Lesser Noddies on Aride Island, Seychelles. Condor 106, 887–895.
CrossRef |

Rossell, C. R., Hamilton, C. D., Weber, L. M., and Kress, S. W. (2000). Chick provisioning by Common Terns in the southern Gulf of Maine, USA. Canadian Journal of Zoology 78, 158–160.
CrossRef |

Sanders, H. (1968). Marine benthic diversity: a comparative study. American Naturalist 102, 243–282.
CrossRef |

Schaffner, F. (1986). Trends in Elegant Tern and Northern Anchovy populations in California. Condor 88, 347–354.
CrossRef |

Scolaro, A., Laurenti, S., and Galleli, H. (1996). The nesting and breeding biology of the South American Tern in northern Patagonia. Journal of Field Ornithology 67, 17–24.

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.
CrossRef | PubMed |

Shealer, D. (1998a). Differences in diet and chick provisioning between adult Roseate and Sandwich terns in Puerto Rico. Condor 100, 131–140.
CrossRef |

Shealer, D. (1998b). Size-selective predation by a specialist forager, the Roseate Tern. Auk 115, 519–525.
CrossRef |

Silva Rodríguez, M. P., Favero, M., Berón, M. P., Mariano-Jelicich, R., and Mauco, L. (2005). Ecología y conservación de aves marinas que utilizan el litoral bonaerense como área de invernada. Hornero 20, 111–130.

Skewgar, E., Boersma, P. D., Harris, G., and Caille, G. (2007). Anchovy fishery threat to Patagonian ecosystem. Science 315, 45.
CrossRef | CAS | PubMed |

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.
CrossRef |

Sonntag, N., and Hüppop, O. (2005). Snacks from the depth: summer and winter diet of Common Guillemots Uria aalge around the Island of Helgoland. Atlantic Seabirds 7, 1–4.

Stienen, E. W. M., Van Beers, P. W. M., Brenninkmeijer, A., Habraken, J. M. P. M., Raaijmakers, M. H. J. E., and Van Tienen, P. G. M. (2000). Reflections of a specialist: patterns in food provisioning and foraging conditions in Sandwich Terns Sterna sandvicensis. Ardea 88, 33–49.

Suryan, R. M., Irons, D. B., Kaufman, M., Benson, J., Jodice, P. G. R., Roby, D. D., and Brown, E. D. (2002). Short-term fluctuations in forage fish availability and the effect on prey selection and brood-rearing in the Black-legged Kittiwake Rissa tridactyla. Marine Ecology Progress Series 236, 273–287.
CrossRef |

Taylor, I. R. (1979). Prey selection during courtship feeding in the Common Tern. Ornis Scandinavica 10, 142–144.
CrossRef |

Taylor, I. R. (1983). Effect of wind on the foraging behaviour of Common and Sandwich Terns. Ornis Scandinavica 14, 90–96.
CrossRef |

Thomson, J. A., Heithaus, M. R., Burkholder, D. A., Vaudo, J. J., Wirsing, A. J., and Dill, L. M. (2012). Site specialists, diet generalists? Isotopic variation, site fidelity, and foraging by Loggerhead Turtles in Shark Bay, Western Australia. Marine Ecology Progress Series 453, 213–226.
CrossRef |

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.
CrossRef | PubMed |

Villanueva-Gomila, L., Gatto, A., Cabral, K., and Yorio, P. (2009). Aggression by adult South American Terns toward conspecific chicks. Journal of Field Ornithology 80, 344–350.
CrossRef |

Wambach, E. J., and Emslie, S. D. (2003). Seasonal and annual variation in the diet of breeding, known-age Royal Terns in North Carolina. Wilson Bulletin 115, 448–454.
CrossRef |

Wiens, J. A. (1989). ‘The Ecology of Bird Communities. Vol. 1: Foundations and Patterns.’ (Cambridge University Press: Cambridge, UK.)

Wilson, L., Daunt, F., and Wanless, S. (2004). Self-feeding and chick provisioning diet differ in the Common Guillemot Uria aalge. Ardea 92, 197–208.

Ydenberg, R. C. (1994). The behavioral ecology of provisioning in birds. Ecoscience 1, 1–14.

Yorio, P. (2005). Estado poblacional y de conservación de gaviotines y escúas que se reproducen en el litoral marítimo argentino. Hornero 20, 75–93.

Zabala, S., Bigatti, G., Botto, F., Iribarne, O. O., and Galván, D. E. (2013). Trophic relationships between a Patagonian gastropod and its epibiotic anemone revealed by using stable isotopes and direct observations. Marine Biology 160, 909–919.
CrossRef | CAS |

Subscriber Login

Legal & Privacy | Contact Us | Help


© CSIRO 1996-2016