European Journal of Wildlife Research

, Volume 59, Issue 6, pp 833–845 | Cite as

Past and present trophic position and decadal changes in diet of Yellow-legged Gull in the Azores Archipelago, NE Atlantic

  • Patrícia I. Pedro
  • Jaime A. Ramos
  • Verónica C. Neves
  • Vítor H. Paiva
Original Paper


This study evaluates the trophic position of adult Yellow-legged Gulls Larus michahellis atlantis resident in the Azores archipelago in the past (1921–1928) and in the present (2009–2010), and analyses the decadal variation in the diet of breeding birds from the 1990s to the 2000s for three main colonies (Topo Islet, Baixo Islet and Mistério da Prainha). Using mixing models, we compared stable isotope signatures of nitrogen and carbon in adult breast feathers between birds from 1921 to 1928 (held in museum collections) and 2009 to 2010, jointly with both isotopic signatures of their main prey groups (fish, goose barnacles (Lepas anatifera), seabirds, mammals and refuse). The diet of breeding birds was analysed using pellets collected in 1989, 1995, 1996, 2004, 2009 and 2010. Stable isotopes analysis (SIA) results were in accordance with the results provided from the analysis of pellets, showing a relatively recent and significant change in the diet of adult gulls. In particular, SIA revealed a significant decrease in the trophic position of Yellow-legged Gulls in the Azores, over the last 89 years in response to the decrease in the consumption of seabirds and fish and, an increase in the consumption of marine invertebrates (goose barnacles) and refuse. The analysis of pellets confirmed the significant decrease in the fish ingested, whereas the ingestion of lower trophic level prey (i.e. goose barnacles, mammals and refuse) increased. Both methods reflect the feeding plasticity and opportunistic foraging behavior of this species, and are in accordance with patterns described for continental Europe.


Azores Trophic position Diet Plasticity Refuse Yellow-legged Gulls 


  1. Arcos JM, Oro D, Sol D (2001) Competition between the yellow-legged gull Larus cachinnans and Audouin’s gull Larus audouinii associated with commercial fishing vessels: the influence of season and fishing fleet. Mar Biol 139:807–816CrossRefGoogle Scholar
  2. Arcos JM, Ruiz X, Bearhop S, Furness RW (2002) Mercury levels in seabirds and their fish prey at the Ebro Delta (NW Mediterranean): the role of trawler discards as a source of contamination. Mar Ecol Prog Ser 232:281–290CrossRefGoogle Scholar
  3. Bearhop S, Phillips RA, Thompson DR, Waldron S, Furness RW (2000) Variability in mercury concentrations of Great Skuas Catharacta skua: the influence of colony diet and trophic status inferred from stable isotope signatures. Mar Ecol Prog Ser 195:261–268CrossRefGoogle Scholar
  4. Bearhop S, Furness RW, Hilton GM, Votier SC, Waldron S (2003) A forensic approach to understanding diet and habitat use from stable isotope analysis of (avian) claw material. Funct Ecol 17:270–275CrossRefGoogle Scholar
  5. BirdLife International (2013) Species factsheet: Larus michahellis. Accessed 15 April 2013
  6. Blokpoel H, Scharf WC (1991) The ring-billed gull in the great lakes of North America. In: Bell BP, Cossee RO, Flux JEC, Heather BD, Hitchmough RA, Robertson CJR, Williams MJ (eds) Acta 20 Congressus Internationalis Ornithologici, vol 4, New Zealand Ornithological Congress Trust Board. Wellington, New Zealand, pp 2372–2377Google Scholar
  7. Blokpoel H, Spaans AL (1991) Introductory remarks: superabundance in gulls: causes, problems and solutions. In: Bell BP, Cossee RO, Flux JEC, Heather BD, Hitchmough RA, Robertson CJR, Williams MJ (eds) Acta 20 Congressus Internationalis Ornithologici, vol 4, New Zealand Ornithological Congress Trust Board. Wellington, New Zealand, pp 2359–2361Google Scholar
  8. Blokpoel H, Tessier GD (1992) Control of ring-billed gulls and herring gulls nesting at urban and industrial sites in Ontario, 1987–1990. Proceedings Eastern Wildlife Damage Control Conference 5:51–57Google Scholar
  9. Blokpoel H, Tessier GD, Andress RA (1997) Successfull restoration of the Ice Island common tern colony requires on-going control of ring-billed gulls. Colon Waterbirds 20:98–101CrossRefGoogle Scholar
  10. Bond A, Jones IL (2009) A practical introduction to stable-isotope analysis for seabird biologists: approaches, cautions and caveats. Mar Ornith 37:183–188Google Scholar
  11. Bosch M, Oro D, Ruiz X (1994) Dependence of Yellow-legged Gull Larus cachinnans on food from human activity in two western Mediterranean colonies. Avocetta 18:135–139Google Scholar
  12. Bosch M, Oro D, Cantos FJ, Zabala M (2000) Short-term effects of culling on the ecology and population dynamics of the yellow-legged gull. J Appl Ecol 37:369–385CrossRefGoogle Scholar
  13. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453CrossRefGoogle Scholar
  14. Ceia FR, Phillips RA, Ramos JA et al (2012) Short- and long-term consistency in the foraging niche of wandering albatrosses. Mar Biol 159:1581–1591. doi:10.1007/s00227-012-1946-1 CrossRefGoogle Scholar
  15. Cherel Y, Hobson KA, Hassani S (2005) Isotopic discrimination between food and blood and feathers of captive penguins: Implications for dietary studies in the wild. Physiol Biochem Zool 78:106–115PubMedCrossRefGoogle Scholar
  16. Christel I, Navarro J, del Castillo M, Cama A, Ferrer X (2012) Foraging movements of Audouin’s gull (Larus audouinii) in the Ebro Delta, NW Mediterranean: a preliminar satellite-tracking study. Estuar Coast Shelf S 96:257–261CrossRefGoogle Scholar
  17. Cohen DM, Inada T, Iwamoto T, Scialabba N (1990) Gadiform fishes of the world (order Gadiformes). An annotated and illustrated catalogue of cods, hakes, grenadiers and other gadiform fishes known to date. FAO Fisheries Synopsis, no. 125, vol. 10. FAO, Rome, p 442Google Scholar
  18. Cooper J, Baccetti N, Belda EJ et al (2003) Seabird mortality from longline fishing in the Mediterranean Sea and Macaronesian waters: a review and a way forward. Sci Mar 67(Supplement 2):57–64Google Scholar
  19. Dalerum F, Angerbjorn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658. doi:10.1007/s00442-005-0118-0 PubMedCrossRefGoogle Scholar
  20. Development Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  21. Dolbeer RA (1990) Ornithology and integrated pest management: red-winged Blackbirds Agelaius phoeniceus and corn. Ibis 132:309–322CrossRefGoogle Scholar
  22. Dolbeer RA, Belant JL, Bernhardt GE (1997) Aerial photography techniques to estimate populations of Laughing Gull nests in Jamaica Bay, New York, 1992–1995. Col Wat 20:8–13CrossRefGoogle Scholar
  23. Duffy DC, Jackson S (1986) Diet studies of seabirds: a review of methods. Colon Waterbirds 9:1–17CrossRefGoogle Scholar
  24. Duhem C, Vidal E, Legrand J, Tatoni T (2003) Opportunistic feeding responses of the Yellow-legged Gull Larus michahellis to accessibility of refuse dumps. Bird Study 50:61–67CrossRefGoogle Scholar
  25. Duhem C, Roche P, Vidal E, Tatoni T (2008) Effects of anthropogenic food resources on yellow-legged gull colony size on Mediterranean islands. Pop Ecol 50:91–100CrossRefGoogle Scholar
  26. Ellis JC (2005) Marine birds on land: a review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecol 181:227–241CrossRefGoogle Scholar
  27. Ferns PN, Mudge GP (2000) Abundance, diet and Salmonella contamination of gulls feeding at sewage outfalls. Water Res 34:2653–2660CrossRefGoogle Scholar
  28. Finney SK, Harris MP, Keller LF et al (2003) Reducing the density of breeding gulls influences the pattern of recruitment of immature Atlantic puffins Fratercula arctica to a breeding colony. Biol Conserv 40:545–552Google Scholar
  29. Forero MG, Hobson KA, Bortolotti GR et al (2002) Food resource utilization by the Magellanic penguin evaluated through stable-isotope analysis: segregation by sex and age and influence on offspring quality. Mar Ecol Prog Ser 234:289–299CrossRefGoogle Scholar
  30. France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Series 124:307–312CrossRefGoogle Scholar
  31. Garthe S, Camphuysen CJ, Furness RW (1996) Amounts of discards by commercial fisheries and their significance as food for seabirds in the North Sea. Mar Ecol Prog Ser 136:1–11CrossRefGoogle Scholar
  32. González-Zevallos D, Yorio P (2006) Seabird use of discards and incidental captures at the Argentine hake trawl fishery in the Golfo San Jorge, Argentina. Mar Ecol Prog Ser 316:175–183CrossRefGoogle Scholar
  33. Gould WJ (1985) Physical Oceanography of the Azores Front. Progr Oceanogr 14:167–190CrossRefGoogle Scholar
  34. Hamer KC, Thompson DR, Rudle AJ, Lewis SA, Stewart FM (1994) Mesopelagic fish eaten by Yellow-legged Herring Gulls Larus argentatus atlantis in the Azores. Seabird 16:30–33Google Scholar
  35. Harris MP, Wanless S (1997) The effect of removing large numbers of gulls Larus spp. on an island population of oystercatchers Haematopus ostralegus: implications for management. Biol Conserv 82:167–171CrossRefGoogle Scholar
  36. Hebert CE, Weseloh DVC, Idrissi A et al (2008) Restoring piscivorous fish populations in the Laurentian Great Lakes causes seabird dietary change. Ecology 89:891–897PubMedCrossRefGoogle Scholar
  37. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197CrossRefGoogle Scholar
  38. Hobson KA, Welch HE (1992) Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Mar Ecol Prog Ser 84:9–18CrossRefGoogle Scholar
  39. Hobson KA, Fisk A, Karnovsky N et al (2002) A stable isotope (δ13C, δ15N) model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants. Deep-Sea Res PT II 49:5131–5150CrossRefGoogle Scholar
  40. INE (2007) Estatísticas da Pesca 2006. Instituto Nacional de Estatística. Direcção-Geral das Pescas e Aquicultura, PortugalGoogle Scholar
  41. Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150:447–461CrossRefGoogle Scholar
  42. Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27CrossRefGoogle Scholar
  43. Kress S (1983) The use of decoys, sound recordings and gull control for re-establishing a tern colony in Maine. Colonial Waterbirds 6:185–196CrossRefGoogle Scholar
  44. Lewis WO, Able KP, Anderson DW et al (1988) Guidelines for the use of wild birds in research. Auk 105(Suppl):1–41Google Scholar
  45. Martínez-Abraín A, Gonzalez-Solís J, Pedrocchi V et al. (2003) Predation, kleptoparasitism and disturbances of yellow-legged gull on Audouin’s gull in three western Mediterranean colonies. In: Mínguez E, Oro D, De Juana E, Martínez-Abraín A (eds) Mediterranean seabirds and their conservation. Sci Mar 67:89–94Google Scholar
  46. Matias R, Catry P (2010) The diet of Atlantic Yellow-legged Gulls (Larus michahellis atlantis) at an oceanic seabird colony: estimating predatory impact upon breeding petrels. Eur J Wildl Res 56:861–869. doi:10.1007/s10344-010-0384-y CrossRefGoogle Scholar
  47. Mizutani H, Fukuda M, Kabaya Y (1992) δ13C and δ15N enrichment factors of feathers of adult birds. Ecology 73:1391–1395CrossRefGoogle Scholar
  48. Monaghan P, Shedden CB, Ensor K, Fricker CR, Girdwood RWA (1985) Salmonella carriage by herring gulls in the Clyde area of Scotland in relation to their feeding ecology. J Appl Ecol 22:669–680CrossRefGoogle Scholar
  49. Monteiro LR (1996) Seabirds as monitors of mercury contamination in the Portuguese Atlantic. PhD Thesis, University of GlasgowGoogle Scholar
  50. Monteiro LR, Ramos JA, Furness RW (1996a) Past and present status and conservation of the seabirds breeding in the Azores Archipelago. Biol Conserv 78:319–328CrossRefGoogle Scholar
  51. Monteiro LR, Ramos JA, Furness RW, del Nevo AJ (1996b) Movements, morphology, breeding, molt, diet and feeding of seabirds in the Azores. Colon Waterbird 19:82–97CrossRefGoogle Scholar
  52. Morais L, Santos C, Vicente L (1998) Population increase of yellow-legged gulls Larus cachinnans breeding on Berlenga Island (Portugal), 1974–1994. Sula 12:27–37Google Scholar
  53. Nelson JS (1984) Fishes of the world, 2nd edn. Wiley-Interscience, New York, p 523Google Scholar
  54. Neves VC, Murdoch N, Furness RW (2006) Population status and diet of the Yellow-legged Gull in the Azores. Arquipélago. Life and Marine Sciences 23A:59–73Google Scholar
  55. Newsome SD, Martínez del Rio C, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Evol 5:429–436Google Scholar
  56. Nolf D (1985) Otolithi piscium. In: Schultz HP (ed) Handbook of Paleoichthyology, vol 10. Fisher, Stuttgart, p 145Google Scholar
  57. Noordhuis R, Spaans AL (1992) Interspecific competition for food between Herring Gull Larus argentatus and Lesser Black-backed Gull L fuscus in the Dutch Wadden Sea area. Ardea 80:115–132Google Scholar
  58. Oro D, Martínez-Abraín A (2007) Deconstructing myths on large gulls and their impact on threatened sympatric waterbirds. Anim Conserv 10:117–126CrossRefGoogle Scholar
  59. Oro D, Bosch M, Ruiz X (1995) Effects of a trawling moratorium on the breeding success of the yellow-legged gull Larus cachinnans. Ibis 137:547–549CrossRefGoogle Scholar
  60. Oro D, de León A, Mínguez E, Furness RW (2005) Estimating predation on breeding European storm-petrels by Yellow-legged Gulls. J Zool (Lond) 265:421–429CrossRefGoogle Scholar
  61. Pajuelo M, Bjorndal KA, Alfaro-Shigueto J et al (2010) Stable isotope variation in loggerhead turtles reveals Pacific–Atlantic oceanographic differences. Mar Ecol Prog Ser 417:277–285CrossRefGoogle Scholar
  62. Paracuellos M, Nevado JC (2010) Culling Yellow-legged Gulls Larus michahellis benefits Audouin’s Gulls Larus audouinii at a small and remote colony. Bird Study 57:26–30CrossRefGoogle Scholar
  63. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672PubMedCrossRefGoogle Scholar
  64. Pérennou C, Sadoul N, Pineau O, Johnson A, Hafner H (1996) Gestion des sites de nidification des oiseaux d’eaux coloniaux. Tour du Valat, ArlesGoogle Scholar
  65. Pham CK, Canha A, Diogo H et al (2013) Total marine fishery catch for the Azores (1950–2010) ICES. J Mar Sci 70(3):564–577. doi:10.1093/icesjms/fst024 Google Scholar
  66. Pingree RD, Garcia-Soto C, Sinha B (1999) Position and structure of the subtropical/Azores Front region from combined Lagrangian and remote sensing (IR/altimeter/SeaWiFS) measurements. J Mar Biol Assoc UK 79:769–792CrossRefGoogle Scholar
  67. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  68. Queró Jean-Claude, Porehe P, Vayne Jean-Jacques (2003) Guide des poissons de l’Atlantique européen. Delachaux et Niestlé S.A., pp 465Google Scholar
  69. Quillfeldt P, Masello JF, McGill RAR, Adams M, Furness R (2010) Moving polewards in winter: a recent change in the migratory strategy of a pelagic seabird? Front Zool 7:15PubMedCrossRefGoogle Scholar
  70. Ramos JA, Sola E, Porteiro FM, Monteiro LR (1998) Prey of Yellow-legged Gull, Roseate Tern and Common Tern in the Azores. Seabird 20:31–40Google Scholar
  71. Ramos R, Ramírez F, Sanpera C, Jover L, Ruiz X (2009) Feeding ecology of yellow-legged gulls Larus michahellis in the western Mediterranean: a comparative assessment using conventional and isotopic methods. Mar Ecol Prog Ser 377:289–297CrossRefGoogle Scholar
  72. Ramos R, Ramírez F, Carrasco JL, Jover L (2011) Insights into the spatiotemporal component of feeding ecology: an isotopic approach for conservation management sciences. Divers Distrib 17:338–349CrossRefGoogle Scholar
  73. Richards SA, Wilson WG (2000) Adaptive feeding across environmental gradients and its effects on population dynamics. Theor Popul Biol 57:377–390PubMedCrossRefGoogle Scholar
  74. Roscales JL, Gómez-Diaz E, Neves V, González-Solíz J (2011) Trophic versus geographic structure in stable signatures of pelagic seabirds breeding in the northeast Atlantic. Mar Ecol Prog Ser 434:1–13. doi:10.3354/meps09211 CrossRefGoogle Scholar
  75. Rutz C, Bijlsma RG (2006) Food-limitation in a generalist predator. P Roy Soc B-Biol Sci 273:2069–2073CrossRefGoogle Scholar
  76. Santos RS, Hawkins S, Monteiro LR, Alves M, Isidro EJ (1995) Marine research, resources and conservation in the Azores. Aquat Conserv 5:311–354CrossRefGoogle Scholar
  77. Schwarcz HP (1991) Some theoretical aspects of isotope paleodiet studies. J Archaeol Sci 18:261–275CrossRefGoogle Scholar
  78. Sinclair ARE, Krebs CJ (2003) Complex numerical responses to top-down and bottom-up processes in vertebrate populations. In: Sibly RM, Hone J, Clutton-Brock T (eds) Wildlife population growth rates. Cambridge University Press, CambridgeGoogle Scholar
  79. Smale MJ, Watson G, Hecht T (1995) Otolith atlas of Southern African marine fishes. Ichthyological Monographs, vol 1. JLB Smith Institute of Ichthyology, GrahamstownGoogle Scholar
  80. Smith GC, Carlile N (1993) Methods for population control within a silver gull colony. Wildl Res 20:219–226CrossRefGoogle Scholar
  81. Sol D, Arcos JM, Senar JC (1995) The influence of refuse tips on the winter distribution of Yellow-legged Gulls Larus cachinnans. Bird Study 42:216–221CrossRefGoogle Scholar
  82. Soldatini C, Riccato F, Torricelli P, Mainardi D (2005) Yellow legged gulls’ diet and foraging locations. XV Congresso della Società Italiana di. Ecologia, TorinoGoogle Scholar
  83. Spaans AL (1971) On the feeding ecology of the Herring Gull Larus argentatus Pont. in the northern part of the Netherlands. Ardea 59:73–188Google Scholar
  84. Spaans AL, Coulson JC, Migot P et al (1991) The herring gull in north-west Europe. In: Bell BP, Cossee RO, Flux JEC, Heather BD, Hitchmough RA, Robertson CJR, Williams MJ (eds) Acta 20 Congressus Internationalis Ornithologici, vol 4, New Zealand Ornithological Congress Trust Board. Wellington, New Zealand, pp 2365–2371Google Scholar
  85. SREA (2011) Estimativa da população residente em 1991 e 2011. Accessed 26 March 2013
  86. Thibault J-C, Zotier R, Guyot I, Bretagnolle V (1996) Recent trends in breeding marine birds of the Mediteranean region with special reference to Corsica. Colon Waterbird 19:31–40CrossRefGoogle Scholar
  87. Tucker GM, Heath MF (1994) Birds in Europe: their conservation status. BirdLife International, CambridgeGoogle Scholar
  88. Valladares S, Moreno R, Jover L, Sanpera C (2010) Evaluating cleansing effects on trace elements and stable isotope values in feathers of oiled birds. Ecotoxycology 19:223–227CrossRefGoogle Scholar
  89. Veen J, Hoedmakers K (2005). Synopsis iconographique des otoliths de quelques espèces de poisons des côtes ouest africaines. Wetlands International, pp 40Google Scholar
  90. Vidal E, Médail F, Tatoni T (1998) Is the yellow-legged gull a superabundant bird species in the Mediterranean? Impact on fauna and flora, conservation measures and research priorities. Biodivers Conserv 7:1013–1026CrossRefGoogle Scholar
  91. Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese E (1984) Fishes of the North-eastern Atlantic and the Mediterranean (FNAM), vol 1. UNESCO, Paris, p 510Google Scholar
  92. Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese E (1986) Fishes of the North-eastern Atlantic and the Mediterranean, vols 1 and 3. UNESCO, Paris, p 1473Google Scholar
  93. Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese E (1989) Fishes of the North-eastern Atlantic and the Mediterranean, vol 2. UNESCO, Paris, p 1473Google Scholar
  94. Witt H-H, Crespo J, de Juana E, Varela J (1981) Comparative feeding ecology of Audouin’s Gull Larus audouinii and the Herring gull L. argentatus in the Mediterranean. Ibis 123:519–526CrossRefGoogle Scholar
  95. Yésou P, Beaubrun PC (1995) Le goéland leucophée Larus cachinnans. In: Yeatman-Berthelot D, Jarry G (eds) Nouvel atlas des oiseaux nicheurs de France 1985–1989. S.O.F, Paris, pp 328–329Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Patrícia I. Pedro
    • 1
  • Jaime A. Ramos
    • 1
  • Verónica C. Neves
    • 2
  • Vítor H. Paiva
    • 1
  1. 1.Marine and Environmental Research Center (IMAR/CMA), Department of Life SciencesUniversity of CoimbraCoimbraPortugal
  2. 2.DOP-Department of Oceanography and FisheriesUniversity of AzoresHortaPortugal

Personalised recommendations