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Marine Biology

, 165:168 | Cite as

Foraging strategies of a generalist seabird species, the yellow-legged gull, from GPS tracking and stable isotope analyses

  • Roberto F. Mendes
  • Jaime A. Ramos
  • Vitor H. Paiva
  • Joana G. Calado
  • Diana M. Matos
  • Filipe R. Ceia
Original paper

Abstract

Generalist and opportunistic species, such as the yellow-legged gull Larus michahellis, can feed on a wide variety of food from both marine and terrestrial origins. This work evaluates the potential foraging strategies (terrestrial, mix and marine) of the yellow-legged gull during the breeding season, in Berlenga (39°24′55″N, 9°30′28″W) and Deserta (36°57′45″N, 7°53′29″W) Islands, Portugal, across 2011–2016. Stable isotope analyses (δ13C and δ15N) of plasma and blood cells were performed to estimate the proportion of individuals pursuing each strategy based on discrimination analyses. For that, GPS loggers were used to assess individual foraging destinations. Overall, this study discriminated well the foraging strategies adopted by gulls through stable isotope analyses (estimated error of 16.7%). Results indicated a variation in foraging strategies across years and between colonies. As expected, this variation was influenced by oceanographic conditions and availability of marine food sources nearby the colonies. The isotopic niche of yellow-legged gulls pursuing a marine strategy was much smaller than the niche of gulls with a terrestrial strategy, but surprisingly only slight smaller than the niche of gulls pursuing a mixed strategy. Gulls adopting a terrestrial strategy fed on a wide variety of foods, which greatly influenced the amplitude of the isotopic values, and respective isotopic niche width. On the other hand, gulls adopting a mix strategy might be very selective in the consumption of foods, taking great advantage of their potential plasticity on both marine and terrestrial environments. This study highlights an overall preference for the marine and mix strategies in yellow-legged gulls.

Notes

Acknowledgements

We would like to thank the Instituto da Conservação da Natureza e Florestas (ICNF) for permits and logistical support (lodging) to conduct this work. Special thanks to the wardens, Paulo Crisóstomo and Eduardo Mourato (Reserva Natural das Berlengas) and Silverio (Parque Natural da Ria Formosa). GPS loggers were financed by the EU INTERREG project FAME: The Future of the Atlantic Marine Environment (2009-1/089) and by LIFE + Berlenga (LIFE13 NAT/PT/000458). VHP, JGC and FRC acknowledge their Grants (SFRH/BPD/85024/2012; PD/BD/127991/2016 and SFRH/BPD/95372/2013, respectively) attributed by the Foundation for Science and Technology (FCT; Portugal) and the European Social Fund (POPH, EU). This study benefited from the strategic program of MARE, financed by FCT (MARE—UID/MAR/04292/2013). We thank the two reviewers for their useful comments on the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed and all necessary approvals have been obtained by the ‘Institute for Nature Conservation in Portugal (ICNF)’, which include the deployment of data loggers and collection of blood samples—Permits nos. 152/2011/CAPT, 101/2012/CAPT, 99/2013/CAPT, 203/2014/CAPT, 169/2015/CAPT, 133/2016/CAPT.

Supplementary material

227_2018_3421_MOESM1_ESM.pdf (1.5 mb)
Supplementary material 1 (PDF 1546 kb)

References

  1. Alonso H, Almeida A, Granadeiro JP, Catry P (2015) Temporal and age-related dietary variations in a large population of yellow-legged gulls Larus michahellis: implications for management and conservation. Eur J Wildl Res 61:819–829.  https://doi.org/10.1007/s10344-015-0958-9 CrossRefGoogle Scholar
  2. Annett C, Pierotti R (1999) Long-term reproductive output in western gulls: consequences of alternate tactics in diet choice. Ecology 80:288–297CrossRefGoogle Scholar
  3. Arcos J, 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 139:807–816.  https://doi.org/10.1007/s002270100651 CrossRefGoogle Scholar
  4. Arizaga J, Jover L, Aldalur A, Cuadrado JF, Díez E, Crespo A (2013) Trophic ecology of a resident yellow-legged gull (Larus michahellis) population in the Bay of Biscay. Mar Environ Res 87–88:19–25CrossRefGoogle Scholar
  5. Arizaga J, Aldalur A, Herrero A, Cuadrado JF, Díez E, Crespo A (2014) Foraging distances of a resident yellow-legged gull (Larus michahellis) population in relation to refuse management on a local scale. Eur J Wildl Res 60:171–175.  https://doi.org/10.1007/s10344-013-0761-4 CrossRefGoogle Scholar
  6. Bearhop S, Adams CE, Waldron S, Fuller RA, Macleod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012.  https://doi.org/10.1111/j.0021-8790.2004.00861.x CrossRefGoogle Scholar
  7. Bécares J, García-Tarrasón M, Villero D, Bateman S, Jover L, García-Matarranz V, Sanpera C, Arcos JM (2015) Modelling terrestrial and marine foraging habitats in breeding Audouin’s gulls Larus audouinii: timing matters. PLoS One 10:e0120799.  https://doi.org/10.1371/journal.pone.0120799 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bond AL, Jones IL (2009) A practical introduction to stable-isotope analysis for seabird biologists: approaches, cautions and caveats. Mar Ornithol 37:183–188Google Scholar
  9. Bouten W, Baaij EW, Shamoun-Baranes J, Camphuysen KC (2013) A flexible GPS tracking system for studying bird behaviour at multiple scales. J Ornithol 154:571–580.  https://doi.org/10.1007/s10336-012-0908-1 CrossRefGoogle Scholar
  10. Calado JG, Matos DM, Ramos JA, Moniz F, Ceia FR, Granadeiro JP, Paiva VH (2018) Seasonal and annual differences in the foraging ecology of two gull species breeding in sympatry and their use of fishery discards. J Avian Biol.  https://doi.org/10.1111/jav.01463 CrossRefGoogle Scholar
  11. Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519.  https://doi.org/10.1016/j.ecolmodel.2006.03.017 CrossRefGoogle Scholar
  12. Caron-Beaudoin É, Gentes M, Patenaude-Monette M, Hélie JF, Giroux JF, Verreault J (2013) Combined usage of stable isotopes and GPS-based telemetry to understand the feeding ecology of an omnivorous bird, the ring-billed gull (Larus delawarensis). Can J Zool 91:689–697.  https://doi.org/10.1139/cjz-2013-0008 CrossRefGoogle Scholar
  13. Ceia FR, Paiva VH, Fidalgo V, Morais L, Baeta A, Crisóstomo P, Mourato E, Garthe S, Marques JC, Ramos JA (2014) Annual and seasonal consistency in the feeding ecology of an opportunistic species, the yellow-legged gull (Larus michahellis). Mar Ecol Prog Ser 497:273–284.  https://doi.org/10.3354/meps10586 CrossRefGoogle Scholar
  14. 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 78:106–115.  https://doi.org/10.1086/425202 CrossRefPubMedGoogle Scholar
  15. Corman A-M, Mendel B, Voigt CC, Garthe S (2016) Varying foraging patterns in response to competition? A multicolony approach in a generalist seabird. Ecol Evol 6:974–986.  https://doi.org/10.1002/ece3.1884 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Duhem C, Vidal E, Legrand J, Tatoni T (2003) Opportunistic feeding responses of the yellow-legged gull Larus michahellis to accessibility of refuse dumps: the gulls adjust their diet composition and diversity according to refuse dump accessibility. Bird Study 50:61–67.  https://doi.org/10.1080/00063650309461291 CrossRefGoogle Scholar
  17. Duhem C, Roche P, Vidal E, Tatoni T (2008) Effects of anthropogenic food resources on yellow-legged gull colony size on Mediterranean islands. Popul Ecol 50:91–100.  https://doi.org/10.1007/s10144-007-0059-z CrossRefGoogle Scholar
  18. Enners L, Schwemmer P, Corman A-M, Voigt CC, Garthe S (2018) Intercolony variations in movement patterns and foraging behaviors among herring gulls (Larus argentatus) breeding in the eastern Wadden Sea. Ecol Evol 8:7529–7542.  https://doi.org/10.1002/ece3.4167 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Forero MG, Hobson KA (2003) Using stable isotopes of nitrogen and carbon to study seabird ecology: applications in the Mediterranean seabird community. Sci Mar 67:23–32CrossRefGoogle Scholar
  20. García-Tarrasón M, Sanpera C, Jover L, Costantini D (2014) Levels of antioxidants in breeding female Audouin’s gulls and their deposition in eggs across different environments. J Exp Mar Bio Ecol 453:116–122.  https://doi.org/10.1016/j.jembe.2014.01.012 CrossRefGoogle Scholar
  21. García-Tarrasón M, Bécares J, Bateman S, Arcos JM, Jover L, Sanpera C (2015) Sex-specific foraging behavior in response to fishing activities in a threatened seabird. Ecol Evol 5:2348–2358.  https://doi.org/10.1002/ece3.1492 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Garthe S, Schwemmer P, Paiva VH, Corman A-M, Fock HO, Voigt CC, Adler S (2016) Terrestrial and marine foraging strategies of an opportunistic seabird species breeding in the Wadden Sea. PLoS One 11:e0159630.  https://doi.org/10.1371/journal.pone.0159630 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13 C in tissues. Condor 94(1):181–188CrossRefGoogle Scholar
  24. Isaksson N, Evans TJ, Shamoun-Baranes J, Åkesson S (2016) Land or sea? Foraging area choice during breeding by an omnivorous gull. Mov Ecol 4:11.  https://doi.org/10.1186/s40462-016-0078-5 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602CrossRefGoogle Scholar
  26. Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48CrossRefGoogle Scholar
  27. Mañosa S, Oro D, Ruiz X (2004) Activity patterns and foraging behavior of Audouin’s gulls en the Ebro Delta, NW Mediterranean. Sci Mar 68:605–614CrossRefGoogle Scholar
  28. Matos DM, Ramos JA, Calado JG, Ceia FR, Hey J, Paiva VH (2018) How fishing intensity affects the spatial and trophic ecology of two gull species breeding in sympatry? ICES J Mar Sci fsy096:1–16.  https://doi.org/10.1093/icesjms/fsy096 CrossRefGoogle Scholar
  29. Monticelli D, Ramos JA, Quartly GD (2007) Effects of annual changes in primary productivity and ocean indices on breeding performance of tropical roseate terns in the western Indian Ocean. Mar Ecol Prog Ser 351:273–286.  https://doi.org/10.3354/meps07119 CrossRefGoogle Scholar
  30. Moreno R, Jover L, Munilla I, Velando A, Sanpera C (2010) A three-isotope approach to disentangling the diet of a generalist consumer: the yellow-legged gull in northwest Spain. Mar Biol 157:545–553.  https://doi.org/10.1007/s00227-009-1340-9 CrossRefGoogle Scholar
  31. Munilla I (1997) Henslow’s swimming crab (Polybius henslowii) as an important food for yellow-legged gulls (Larus cachinnans) in NW Spain. ICES J Mar Sci 54:631–634.  https://doi.org/10.1006/jmsc.1997.0249 CrossRefGoogle Scholar
  32. Newsome S, Rio C, Bearhop S, Phillips D (2007) A niche for isotopic ecology. Front Ecol Environ 5(8):429–436.  https://doi.org/10.1890/060150.01 CrossRefGoogle Scholar
  33. Osterback A-MK, Frechette DM, Hayes SA, Shaffer SA, Moore JW (2015) Long-term shifts in anthropogenic subsidies to gulls and implications for an imperiled fish. Biol Conserv 191:606–613.  https://doi.org/10.1016/j.biocon.2015.07.038 CrossRefGoogle Scholar
  34. Paiva VH, Geraldes P, Marques V, Rodríguez R, Garthe S, Ramos JA (2013) Effects of environmental variability on different trophic levels of the North Atlantic food web. Mar Ecol Prog Ser 477:15–28.  https://doi.org/10.3354/meps10180 CrossRefGoogle Scholar
  35. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS One 5(3):e9672.  https://doi.org/10.1371/journal.pone.0009672 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Pinto JG, Raible CC (2012) Past and recent changes in the North Atlantic Oscillation. WIREs Clim Chang 3:79–90.  https://doi.org/10.1002/wcc.150 CrossRefGoogle Scholar
  37. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189.  https://doi.org/10.1007/s00442-006-0630-x CrossRefPubMedGoogle Scholar
  38. Quillfeldt P, McGill R, Furness R (2005) Diet and foraging areas of Southern Ocean seabirds and their prey inferred from stable isotopes: review and case study of Wilson’s storm-petrel. Mar Ecol Prog Ser 295:295–304.  https://doi.org/10.3354/meps295295 CrossRefGoogle Scholar
  39. Ramos R, Ramírez F, Sanpera C, Jover L, Ruiz X (2009a) Diet of yellow-legged gull (Larus michahellis) chicks along the Spanish Western Mediterranean coast: the relevance of refuse dumps. J Ornithol 150:265–272.  https://doi.org/10.1007/s10336-008-0346-2 CrossRefGoogle Scholar
  40. Ramos R, Ramírez F, Sanpera C, Jover L, Ruiz X (2009b) Feeding ecology of yellow-legged gulls Larus michahellis in the western Mediterranean: a comparative assessment using conventional and isotopic methods. Mar Ecol Prog Ser 377:289–297.  https://doi.org/10.3354/meps07792 CrossRefGoogle Scholar
  41. 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 17:338–349.  https://doi.org/10.1111/j.1472-4642.2010.00736.x CrossRefGoogle Scholar
  42. Ramos JA, Pedro P, Matos A, Paiva VH (2013) Relation between climatic factors, diet and reproductive parameters of little terns over a decade. Acta Oecol 53:56–62.  https://doi.org/10.1016/j.actao.2013.09.001 CrossRefGoogle Scholar
  43. Shaffer SA, Cockerham S, Warzybok P, Bradley RW, Jahncle J, Clatterbuck CA, Lucia M, Jelincic JA, Cassell AL, Kelsey EC, Adams J (2017) Population-level plasticity in foraging behavior of western gulls (Larus occidentalis). Mov Ecol 5:27.  https://doi.org/10.1186/s40462-017-0118-9 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Shim JH, Pendall E, Morgan JA, Ojima DS (2009) Wetting and drying cycles drive variations in the stable carbon isotope ratio of respired carbon dioxide in semi-arid grassland. Oecologia 160:321–333.  https://doi.org/10.1007/s00442-009-1302-4 CrossRefPubMedGoogle Scholar
  45. Soldatini C, Riccato F, Torricelli P, Mainardi D (2005) Yellow legged gulls’ diet and foraging locations. In: XV Congr della Soc Ital di Ecol Torino, pp 1–6Google Scholar
  46. Sousa FM, Nascimento S, Casimiro H, Boutov D (2008) Identification of upwelling areas on sea surface temperature images using fuzzy clustering. Remote Sens Environ 112:2817–2823.  https://doi.org/10.1016/j.rse.2008.01.014 CrossRefGoogle Scholar
  47. Stenseth NC, Ottersen G, Hurrell JW, Mysterud A, Lima M, Chan K, Yoccoz NG, Bjørn A (2003) Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond Nils. Proc R Soc London B.  https://doi.org/10.1098/rspb.2003.2415 CrossRefGoogle Scholar
  48. Thorne LH, Conners MG, Hazen EL, Bograd SJ, Antolos M, Costa DP, Shaffer SA (2016) Effects of El Niño-driven changes in wind patterns on North Pacific albatrosses. J R Soc Interface 13:20160196CrossRefGoogle Scholar
  49. Washburn BE, Bernhardt GE, Kutschbach-Brohl L, Chipman RB, Francoeur LC (2013) Foraging ecology of four gull species at a coastal–urban interface. Condor 115:67–76.  https://doi.org/10.1525/cond.2013.110185 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Life Sciences, MARE-Marine and Environmental Sciences CentreUniversidade de CoimbraCoimbraPortugal

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