The impact of anthropogenic food subsidies on a generalist seabird during nestling growth

J. Lenzi, I. González-Bergonzoni, E. Machín, B. Pijanowski, E. Flaherty

Research output: Contribution to journalArticle


Anthropogenic food subsidies, such as refuse, are an important driver of animal population changes and gulls heavily forage on this food source. Foraging on refuse during the rearing period could affect the acquisition of resources with potential demographic consequences. Using conventional diet analysis and stable isotopes of δ13C and δ15N of blood of Kelp Gull (Larus dominicanus) nestlings, we studied the variation of the chick growth in response to foraging on refuse on a reproductive colony in the Rio de la Plata Estuary in Uruguay. Using Bayesian mixing models on isotopic data, we estimated the proportion and variation of natural food and refuse in the diet of nestlings. Then, we modelled the variation between the mean posterior densities of the food sources and their standard deviation with the nestling morphometric measurements of different sizes. We found that refuse was gradually delivered to Kelp Gull nestlings during the chick rearing period. Additionally, variation of refuse incorporated into nestling tissues increased with nestlings' size. We propose that parents use more isotopically unique food sources during the nestling growth thereby increasing isotopic diversity. This study highlights the need to improve the current waste management system, which is being reviewed in Uruguay. We believe that decision makers should consider the results of this study, which show that refuse is directly impacting coastal ecosystems through mechanisms poorly explored by the environmental sciences. © 2019 Elsevier B.V.
Original languageEnglish
Pages (from-to)546-553
Number of pages8
JournalScience of the Total Environment
Publication statusPublished - 2019
Externally publishedYes


Bibliographical note

Export Date: 20 June 2019


Correspondence Address: Lenzi, J.; Centro de Investigación y Conservación Marina - CICMAR, Avenida Giannattasio Km 30.5, Uruguay; email:

Funding details: Agencia Nacional de Investigación e Innovación

Funding details: Fondo Nacional de Desarrollo Científico, Tecnológico y de Innovación Tecnológica, 11160601

Funding details: Department of Forestry and Natural Resources, Purdue University

Funding details: California Health Care Safety Net Institute

Funding text 1: Thanks to Franco Teixeira de Mello and Alejandro D'Anatro for affording the stable isotope analysis. To Pablo Viera, Ernesto Venini, Matías Barrios, Luis Martínez, and Héctor López for their support during fieldwork activities. To Ilda Gómez, Hebert Gallegos, Rodrigo Barreiro, Armada Nacional Naval, and Servicio de Balizamiento de la Armada for their great support with logistics. Dirección Nacional de Medio Ambiente (DINAMA) and Dirección Nacional de Recursos Acuáticos (DINARA) for the research permits. To Purdue Animal Care and Use Committee for the animal ethics training and permit (protocol number 1706001591). To Idea Wild and Birders' Exchange for providing laboratory and field equipment. To Fernando Campos-Medina and the Fondecyt project no. 11160601 for the support and collaboration during this research. To Verónica Campos for comments and insights of an earlier version of the manuscript. IGB was financially supported by the national system for researchers (SNI) of the National Agency for Research and Innovation (ANII) and the graduate school PEDECIBA in Uruguay. Comments on earlier drafts by Jeffrey Lucas helped to improve the quality of the paper. JL was partially supported by the Department of Forestry and Natural Resources at Purdue University and by a Fulbright-ANII Fellowship. We would like to thank the two anonymous referees that contributed to improve this manuscript.

References: Akaike, H., Information theory as an extension of the maximum likelihood principle (1973) Proceedings of the Second International Symposium on Information Theory, Akademiai Kiado, Budapest, pp. 267-281. , B.N. Petrov F. Csaki; Annett, C.A., Pierotti, R., Chick hatching as a trigger for dietary switching in the Western Gull (1989) Colonial Waterbirds, 12, pp. 4-11; Annett, C.A., Pierotti, R., Long-term reproductive output in Western gulls: consequences of alternate tactics in diet choice (1999) Ecology, 80, pp. 288-297; Anza, I., Vidal, D., Laguna, C., Díaz-Sánchez, S., Sánchez, S., Chicote, Á., Florín, M., Mateo, R., Eutrophication and bacterial pathogens as risk factors for avian botulism outbreaks in wetlands receiving effluents from urban wastewater treatment plants (2014) Appl. Environ. Microbiol., 80, pp. 4251-4259; Barrett, R.T., Camphuysen, K.C.J., Anker-Nilssen, T., Chardine, J.W., Furness, R.W., Garthe, S., Hüppop, O., Veit, R.R., Diet studies of seabirds: a review and recommendations (2007) ICES, 64, pp. 1675-1691; Bearhop, S., Adams, C.E., Waldron, S., Fuller, R.A., Macleod, H., Determining trophic niche width: a novel approach using stable isotope analysis (2004) J. Anim. Ecol., 73, pp. 1007-1012; Belant, J.L., Seamans, T.W., Gabrey, S.W., Ickes, S.K., Importance of landfills to nesting herring gulls (1993) Condor, 95, pp. 817-830; Bertellotti, M., Yorio, P., Spatial and temporal patterns in the diet of the Kelp Gull in Patagonia (1999) Condor, 101, pp. 790-798; Brousseau, P., Lefebvre, J., Giroux, J.-F., Diet of ring-billed Gull chicks in urban and non-urban colonies in Quebec (1996) Colonial Waterbirds, 19, pp. 22-30; Bugoni, L., McGill, R.A., Furness, R.W., Effects of preservation methods on stable isotope signatures in bird tissues (2008) Rapid Commun. Mass Spectrom., 22, pp. 2457-2462; Burger, J., Foraging behavior in gulls: differences in method, prey, and habitat (1988) Colonial Waterbirds, 11, pp. 9-23; Burgues, M.F., Ecología trófica de la Gaviota Cocinera (Larus dominicanus) en Isla de las Gaviotas (Montevideo, Uruguay). Tesina de grado. Licenciatura en Ciencias. Biológicas. Profundización en Ecología (2015), p. 40. , Facultad de Ciencias, Universidad de la República Montevideo, Uruguay; Campioni, L., Granadeiro, J.P., Catry, P., Niche segregation between immature and adult seabirds: does progressive maturation play a role? (2015) Behav. Ecol., 27, pp. 426-433; Ceia, F.R., Phillips, R.A., Ramos, J.A., Cherel, Y., Vieira, R.P., Richard, P., Xavier, J.C., Short-and long-term consistency in the foraging niche of wandering albatrosses (2012) Mar. Biol., 159, pp. 1581-1591; Ceia, F.R., Paiva, V.H., Fidalgo, V., Morais, L., Baeta, A., Crisóstomo, P., Mourato, E., Ramos, J.A., Annual and seasonal consistency in the feeding ecology of an opportunistic species, the yellow-legged gull Larus michahellis (2014) Mar. Ecol. Prog. Ser., 497, pp. 273-284; Coulson, R., Coulson, G., Population change among Pacific, Kelp and Silver gulls using natural and artificial feeding sites in south-eastern Tasmania (1998) Wildl. Res., 25, pp. 183-198; Davoren, G., Burger, A., Differences in prey selection and behaviour during self-feeding and chick provisioning in Rhinoceros Auklets (1999) Anim. Behav., 58, pp. 853-863; Duhem, C., Vidal, E., Roche, P., Legrand, J., How is the diet of yellow-legged Gull chicks influenced by parents' accessibility to landfills? (2005) Waterbirds, 28, pp. 46-52; Emslie, S.D., Karnovsky, N., Trivelpiece, W., Avian predation at penguin colonies on King George Island, Antarctica (1995) Wilson Bulletin, 107, pp. 317-327; Favero, M., Silva, M., How important are pelagic preys for the kelp gull during chick-rearing at the South Shetland Islands? (1998) Polar Biol., 19, pp. 32-36; Flaherty, E.A., Ben-David, M., Overlap and partitioning of the ecological and isotopic niches (2010) Oikos, 119, pp. 1409-1416; Fry, B., Stable isotope diagrams of freshwater food webs (1991) Ecology, 72, pp. 2293-2297; Fry, B., Alternative approaches for solving underdetermined isotope mixing problems (2013) Mar. Ecol. Prog. Ser., 472, pp. 1-13; González-Bergonzoni, I., Johansen, K.L., Mosbech, A., Landkildehus, F., Jeppesen, E., Davidson, T.A., Small birds, big effects: the Little Auk (Alle alle) transforms high Arctic ecosystems (2017) Proc. R. Soc. B Biol. Sci., 284; Goshu, A.T., Koya, P.R., Derivation of inflection points of nonlinear regression curves-implications to statistics (2013) Am. J. Theor. Appl. Stat., 2, pp. 268-272; Groch, K.R., Cases of harassment by Kelp Gulls (Larus dominicanus) on Right Whales (Eubalaena australis) of southern Brazil (2001) Biotemas, 14, pp. 147-156; Guido, A., Mai, P., Piñeiro, V., Mourelle, D., Souza, M., Machín, E., Zaldúa, N., Lenzi, J., Floristic composition of Isla de las Gaviotas, Río de la Plata estuary, Uruguay (2013) CheckList, 9, pp. 763-770; Hammer, Ø., Harper, D.A.T., Ryan, P.D., PAST: paleontological statistics software package for education and data analysis (2001) Palaeontolia Electronica, 4; Hand, J.L., Southern, W.E., Vermeer, K., Ecology and behavior of gulls (1987) Stud. Avian Biol., 10. , (140 pp.); Hertz, E., Trudel, M., El-Sabaawi, R., Tucker, S., Dower, J.F., Beacham, T.D., Edwards, A.M., Mazumder, A., Hitting the moving target: modelling ontogenetic shifts with stable isotopes reveals the importance of isotopic turnover (2016) J. Anim. Ecol., (3), pp. 681-691; Hobson, K.A., Isotopic ornithology: a perspective (2011) J. Ornithol., 152, pp. 49-66; Hobson, K.A., Clark, R.G., Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation (1992) Condor, 94, pp. 189-197; Hobson, K.A., Piatt, J.F., Pitocchelli, J., Using stable isotopes to determine seabird trophic relationships (1994) J. Anim. Ecol., 63, pp. 786-798; Hone, D.W.E., Benton, M.J., The evolution of large size: how does Cope's Rule work? (2005) Trends in Ecology and Evolution, 20, pp. 4-6; Hoornweg, D., Bhada-Tata, P., What a waste: A global review of solid waste management (2012) Urban Development Series Knowledge Papers, 15, pp. 1-98; Hunt, G.L., Influence of food distribution and human disturbance on the reproductive success of Herring Gulls (1972) Ecology, 53, pp. 1051-1061; Johnson, J.B., Omland, K.S., Model selection in ecology and evolution (2004) Trends Ecol. Evol., 19, pp. 101-108; Karnovsky, N.J., Hobson, K.A., Iverson, S.J., From lavage to lipids: estimating diets of seabirds (2012) Mar. Ecol. Prog. Ser., 451, pp. 263-284; Kelleher, K., Discards in the world's Marine Fisheries. An Update. FAO Fisheries Technical Paper. No. 470 (2005), FAO Rome 131pp; Kurle, C., Koch, P., Tershy, B., Croll, D., The effects of sex, tissue type, and dietary components on stable isotope discrimination factors (Δ13C and Δ15N) in mammalian omnivores (2014) Isot. Environ. Health Stud., 50, pp. 307-321; Lenzi, J., Burgues, M.F., Carrizo, D., Machín, E., (2016), pp. 71-76. , Teixeira-de Mello, F. Plastic ingestion by a generalist seabird on the coast of Uruguay. Mar. Pollut. Bull. 107; Leroux, S.J., Loreau, M., Subsidy hypothesis and strength of trophic cascades across ecosystems (2008) Ecol. Lett., 11, pp. 1147-1156; Lisnizer, N., García-Borboroglu, P., Pascual, M., Yorio, P., Transfer processes drive population dynamics of kelp gull colonies in Patagonia: implications for management strategies (2015) Mar. Biol. Res., 11, pp. 738-746; Ludynia, K., Garthe, S., Luna-Jorquera, G., Seasonal and regional variation in the diet of the Kelp Gull in northern Chile (2005) Waterbirds, 28, pp. 359-365; Martinez-Abraín, A., Gonzalez-Solís, J., Pedrocchi, V., Genovart, M., Abella, J.C., Ruiz, X., Jiménez, J., Oro, D., Kleptoparasitism, disturbance and predation of yellow-legged gulls on Audouin's gulls in three colonies in western Mediterranean (2003) Sci. Mar., 67, pp. 89-94; Minagawa, M., Wada, E., Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age (1984) Geochim. Cosmochim. Acta, 48, pp. 1135-1140; Moore, J.W., Semmens, B.X., Incorporating uncertainty and prior information into stable isotope mixing models (2008) Ecol. Lett., 11, pp. 470-480; Moré, E., Ayats, T., Ryan, P.G., Naicker, P.R., Keddy, K.H., Gaglio, D., Witteveen, M., Cerdà-Cuéllar, M., Seabirds (Laridae) as a source of Campylobacter spp., Salmonella spp. and antimicrobial resistance in South Africa (2017) Environ. Microbiol., 19, pp. 4164-4176; Newsome, S.D., Martinez del Rio, C., Bearhop, S., Phillips, D.L., A niche for isotopic ecology (2007) Front. Ecol. Environ., 5, pp. 429-436; Newsome, S.D., Yeakel, J.D., Wheatley, P.V., Tinker, M.T., Tools for quantifying isotopic niche space and dietary variation at the individual and population level (2012) J. Mammal., 93, pp. 329-341; Oro, D., Genovart, M., Tavecchia, G., Fowler, M.S., Martínez-Abraín, A., Ecological and evolutionary implications of food subsidies from humans (2013) Ecol. Lett., 16, pp. 1501-1514; Parnell, A.C., Inger, R., Bearhop, S., Jackson, A.L., Source partitioning using stable isotopes: coping with too much variation (2010) PLoS One, 5; Pedrocchi, V., Oro, D., González-Solís, J., Differences between diet of adult and chick Audouin's gulls Larus audouinii at the Chafarinas Islands, SW Mediterranean (1996) Ornis Fennica, 73, pp. 124-130; Peterson, B.J., Fry, B., Stable isotopes in ecosystem studies (1987) Annu. Rev. Ecol. Syst., 18, pp. 293-320; Petracci, P.F., (2004), pp. 23-28. , La Sala, L.F., Aguerre, G., Pérez, C.H., Acosta, N., Sotelo, M., Pamparana, C. Dieta de la Gaviota Cocinera (Larus dominicanus) durante el período reproductivo en el estuario de Bahía Blanca, Buenos Aires, Argentina. El hornero 19; Pierotti, R., Annett, C.A., Reproductive consequences of dietary specialization and switching in an ecological generalist (1987) Foraging Behavior, pp. 417-442. , A.C. Kamil J.R. Krebs H.R. Pulliam Plenum Press New York and London; Pierotti, R., Annett, C.A., The ecology of Western gulls in habitats varying in degree of urban influence (2001) Avian Ecology and Conservation in an Urbanizing World, pp. 307-329. , J.M. Marzluff R. Bowman R. Donnelly Springer Boston; Plaza, P.I., Lambertucci, S.A., How are garbage dumps impacting vertebrate demography, health, and conservation? (2017) Global Ecology and Conservation, 12, pp. 9-20; Polis, G.A., Anderson, W.B., Holt, R.D., Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs (1997) Annu. Rev. Ecol. Syst., 28, pp. 289-316; Pons, J.M., Effects of changes in the availability of human refuse on breeding parameters in a herring Gull Larus argentatus population in Brittany, France (1992) Ardea, 80, pp. 143-150; Pons, J.M., Migot, P., Life-history strategy of the Herring Gull: changes in survival and fecundity in a popoulation subjected to variours feeding conditions (1995) J. Anim. Ecol., 64, pp. 592-599; Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J., Montana, C.G., Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses (2007) Oecologia, 152, pp. 179-189; R Development Core Team. R, A Language and Environment for Statistical Computing (2018), R Foundation for Statistical Computing Vienna, Austria; Ramos, R., Ramírez, F., Sanpera, C., Jover, L., Ruiz, X., Diet of yellow-legged Gull (Larus michahellis) chicks along the Spanish Western Mediterranean coast: the relevance of refuse dumps (2009) J. Ornithol., 150, pp. 265-272; Rey, M., Lorenzo, M.I., Páez, E., Cálculo indirecto del descarte costero (2000), p. 14. , Instituto Nacional de Pesca 14pp. Informe Técnico N° 48; Reynolds, S.J., Ibáñez-Álamo, J.D., Sumasgutner, P., Mainwaring, M.C., Urbanisation and nest building in birds: a review of threats and opportunities (2019) J. Ornithol., pp. 1-20; Rowntree, V., Mcguinness, P., Marshall, K., Payne, R., Sironi, M., Seger, J., Increased harassment of right whales (Eubalaena australis) by kelp gulls (Larus dominicanus) at Peninsula Valdes, Argentina (1998) Marine Mammal Science, 14, pp. 99-115; Silva, M.P., Bastida, R., Darrieu, C., Dieta de la Gaviota Cocinera (Larus dominicanus) en zonas costeras de la Provincia de Buenos Aires, Argentina (2000) Ornitología Neotropical, 11, pp. 331-339; Sironi, M., Rowntree, V.J., Snowdon, C.T., Valenzuela, L., Marón, C., Kelp Gulls (Larus dominicanus) Feeding on Southern Right Whales (Eubalaena australis) at Península Valdés, Argentina: Updated Estimates and Conservation Implications (2009), (International Whaling Commission Document SC/61/BRG19); Smith, J.A., Mazumder, D., Suthers, I.M., Taylor, M.D., To fit or not to fit: evaluating stable isotope mixing models using simulated mixing polygons (2013) Methods Ecol. Evol., 4, pp. 612-618; Sodhi, N.S., Competition in the air: birds versus aircraft (2002) Auk, 119, pp. 587-595; Steenweg, R.J., Ronconi, R.A., Leonard, M.L., Seasonal and age-dependent dietary partitioning between the great black-backed and herring gulls (2011) Condor, 113, pp. 795-805; Stock, B.C., Semmens, B.X., MixSIAR GUI User Manual. Version 3.1 (2016),<doi:10.5281/zenodo.1209993; Thompson, D.R., Lilliendahl, K., Sólmundsson, J., Furness, R.W., Waldron, S., Phillips, R.A., Trophic relationships among six species of Icelandic seabirds as determined through stable isotope analysis (1999) Condor, pp. 898-903; Voorbergen, A., De Boer, W.F., Underhill, L.G., Natural and human-induced predation on cape cormorants at Dyer Island (2012) Bird Conservation International, 22, pp. 82-93; Votier, S.C., Grecian, W.J., Patrick, S., Newton, J., Inter-colony movements, at-sea behaviour and foraging in an immature seabird: results from GPS-PPT tracking, radio-tracking and stable isotope analysis (2011) Mar. Biol., 158, pp. 355-362; Weimerskirch, H., Cherel, Y., Delord, K., Jaeger, A., Patrick, S.C., Riotte-Lambert, L., Lifetime foraging patterns of the wandering albatross: life on the move! (2014) J. Exp. Mar. Biol. Ecol., 450, pp. 68-78; Weiser, E.L., Powell, A.N., Does Garbage in the Diet Improve Reproductive Output of Glaucous Gulls? (2010), 112. , University of California Press Berkeley, CA, ETATS-UNIS; Wilson, R., An improved stomach pump for penquins and other seabirds (1984) Journal of Field Ornithology, 55, pp. 109-112; Wolf, N., Carleton, S.A., Martínez del Rio, C., Ten years of experimental animal isotopic ecology (2009) Funct. Ecol., 23, pp. 17-26; Yeakel, J.D., Bhat, U., Elliott Smith, E.A., Newsome, S.D., Exploring the isotopic niche: isotopic variance, physiological incorporation, and the temporal dynamics of foraging (2016) Front. Ecol. Evol., 4 (1); Yorio, P., Bertellotti, M., Quintana, F., Preference for covered nest sites and breeding success in kelp gulls Larus dominicanus (1995) Mar. Ornithol., 23, pp. 121-128; Yorio, P., Bertellotti, M., Gandini, P., Frere, E., Kelp Gull Larus dominicanus breeding on the argentine coast: population status and relationship with coastal management and conservation (1998) Mar. Ornithol., 26, pp. 11-18; Yorio, P., Branco, J.O., Lenzi, J., Luna-Jorquera, G., Zavalaga, C., Distribution and trends in Kelp Gull (Larus dominicanus) coastal breeding populations in South America (2016) Waterbirds, 39, pp. 114-135

Cite this