Marine Biology

, Volume 159, Issue 6, pp 1197–1207 | Cite as

Parent–offspring dietary segregation of Cory’s shearwaters breeding in contrasting environments

  • Hany Alonso
  • José P. Granadeiro
  • Vitor H. Paiva
  • Ana S. Dias
  • Jaime A. Ramos
  • Paulo Catry
Original Paper

Abstract

In pelagic seabirds, who often explore distant food resources, information is usually scarce on the level of trophic segregation between parents and their offspring. To investigate this issue, we used GPS tracking, stable isotopes and dietary information of Cory’s shearwaters Calonectris diomedea breeding in contrasting environments. Foraging trips at Selvagem Grande (an oceanic island) mainly targeted the distant African coast, while at Berlenga island (located on the continental shelf), shearwaters foraged mainly over nearby shelf waters. The degree of isotopic segregation between adults and chicks, based on δ13C, differed markedly between the two sites, indicating that adult birds at Selvagem fed their chicks with a mixture of shelf and offshore pelagic prey but assimilated more prey captured on coastal shelf waters. Isotopic differences between age classes at Berlenga were much smaller and may have resulted from limited dietary segregation or from age-related metabolic differences. The diet of shearwaters was also very different between the two colonies, with offshore pelagic prey only being detected at Selvagem Grande. Our findings suggest that spatial foraging constraints influence resource partitioning between pelagic seabirds and their offspring and can lead to a parent–offspring dietary segregation.

References

  1. Baduini CL, Hyrenbach KD (2003) Biogeography of procellariiform foraging strategies: does ocean productivity influence provisioning? Mar Ornithol 31:101–112Google Scholar
  2. Baird PH (1991) Optimal foraging and intraspecific competition in the tufted puffin. Condor 93:503–515CrossRefGoogle Scholar
  3. Barrett RT, Camphuysen CJ, Anker-Nilssen T, Chardine JW, Furness RW, Garthe S, Hüppop O, Leopold MF, Montevecchi WA, Veit RR (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691CrossRefGoogle Scholar
  4. Bearhop S, Teece MA, Waldron S, Furness RW (2000) Influence of lipid and uric acid on δ13C and δ15N values of avian blood: implications for trophic studies. Auk 117:504–507CrossRefGoogle Scholar
  5. Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458CrossRefGoogle 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 73:1007–1012CrossRefGoogle Scholar
  7. Bearhop S, Phillips RA, McGill R, Cherel Y, Dawson DA, Croxall JP (2006) Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar Ecol Prog Ser 311:157–164CrossRefGoogle Scholar
  8. Benson J, Suryan RM, Piatt JF (2003) Assessing chick growth from a single visit to a seabird colony. Mar Ornithol 31:181–184Google Scholar
  9. 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
  10. Bond AL, McClelland GTW, Jones IL, Lavers JL, Kyser TK (2010) Stable isotopes confirm community patterns in foraging among Hawaiian Procellariiformes. Waterbirds 33:50–58CrossRefGoogle Scholar
  11. Bugoni L, McGill RAR, Furness RW (2008) Effects of preservation methods on stable isotope signatures in bird tissues. Rapid Commun Mass Spectrom 22:2457–2462CrossRefGoogle Scholar
  12. Catard A, Weimerskirch H, Cherel Y (2000) Exploitation of distant Antarctic waters and close shelf-break waters by white-chinned petrels rearing chicks. Mar Ecol Prog Ser 194:249–261CrossRefGoogle Scholar
  13. Catry P, Matias R, Vicente L, Granadeiro JP (2009) Brood-guarding behaviour in Cory’s shearwaters Calonectris diomedea. J Ornithol 150:103–108CrossRefGoogle Scholar
  14. Chaurand T, Weimerskirch H (1994) The regular alternation of short and long foraging trips in the Blue petrel Halobaena caerulea: a previously undescribed strategy of food provisioning in a pelagic seabird. J Anim Ecol 63:275–282CrossRefGoogle Scholar
  15. Cherel Y, Hobson KA (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser 329:281–287CrossRefGoogle Scholar
  16. Cherel Y, Hobson KA, Hassani S (2005a) Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiol Biochem Zool 78:106–115CrossRefGoogle Scholar
  17. Cherel Y, Hobson KA, Weimerskirch H (2005b) Using stable isotopes to study resource acquisition and allocation in procellariiform seabirds. Oecologia 145:533–540CrossRefGoogle Scholar
  18. Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005c) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888CrossRefGoogle Scholar
  19. Cherel Y, Le Corre M, Jaquemet S, Ménard F, Richard P, Weimerskirch H (2008) Resource partitioning within a tropical seabird community: new information from stable isotopes. Mar Ecol Prog Ser 366:281–291CrossRefGoogle Scholar
  20. Cramp S, Simmons KE (1977) Handbook of the birds of Europe, the Middle East and North Africa, vol 1. Oxford University Press, OxfordGoogle Scholar
  21. Dänhardt A, Fresemann T, Becker PH (2011) To eat or to feed? Prey utilization of Common Terns Sterna hirundo in the Wadden Sea. J Ornithol 152:347–357CrossRefGoogle Scholar
  22. Davenport R, Neuer S, Helmke P, Perez-Marrero J, Llinas O (2002) Primary productivity in the northern Canary Islands region as inferred from SeaWiFS imagery. Deep Sea Res II 49:3481–3496CrossRefGoogle Scholar
  23. Davoren GK, Burger AE (1999) Differences in prey selection and behaviour during self-feeding and chick provisioning in rhinoceros auklets. Anim Behav 58:853–863CrossRefGoogle Scholar
  24. Duffy DC, Jackson S (1986) Diet studies of seabirds: a review of methods. Colon Waterbirds 9:1–17CrossRefGoogle Scholar
  25. Einoder LD, Page B, Goldsworthy SD, De Little SC, Bradshaw CJA (2011) Exploitation of distant Antarctic waters and close neritic waters by short-tailed shearwaters breeding in South Australia. Aust Ecol 36:461–475CrossRefGoogle Scholar
  26. Forero MG, Gonzalez-Solis J, Hobson KA, Doncazar JA, Bertellotti M, Blanco G, Bortolotti GR (2005) Stable isotopes reveal trophic segregation by sex and age in the southern giant petrel in two different food webs. Mar Ecol Prog Ser 296:107–113CrossRefGoogle Scholar
  27. Granadeiro JP (1991) The breeding biology of Cory’s shearwater Calonectris diomedea borealis on Berlenga Island, Portugal. Seabird 13:30–33Google Scholar
  28. Granadeiro JP, Silva MA (2000) The use of otoliths and vertebrae in the identification and size-estimation of fish in predator-prey studies. Cybium 24:383–393Google Scholar
  29. Granadeiro JP, Monteiro LR, Furness RW (1998a) Diet and feeding ecology of Cory’s shearwater Calonectris diomedea in the Azores, north-east Atlantic. Mar Ecol Prog Ser 166:267–276CrossRefGoogle Scholar
  30. Granadeiro JP, Nunes M, Silva MC, Furness RW (1998b) Flexible foraging strategy of Cory’s shearwater, Calonectris diomedea, during the chick-rearing period. Anim Behav 56:1169–1176CrossRefGoogle Scholar
  31. Granadeiro JP, Dias MP, Rebelo R, Santos CD, Catry P (2006) Numbers and population trends of Cory’s Shearwater Calonectris diomedea at Selvagem Grande, northeast Atlantic. Waterbirds 29:56–60CrossRefGoogle Scholar
  32. Grémillet D, Dell’Omo G, Ryan PG, Peters G, Ropert-Coudert Y, Weeks SJ (2004) Offshore diplomacy, or how seabirds mitigate intra-specific competition: a case study based on GPS tracking of cape gannets from neighbouring colonies. Mar Ecol Prog Ser 268:265–279CrossRefGoogle Scholar
  33. Harding AMA, Hobson KA, Walkusz W, Dmoch K, Karnovsky NJ, Van Pelt TI, Lifjeld JT (2008) Can stable isotope (δ13C and δ15N) measurements of little auk (Alle alle) adults and chicks be used to track changes in high-Arctic marine foodwebs? Polar Biol 31:725–733CrossRefGoogle Scholar
  34. Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798CrossRefGoogle Scholar
  35. Hodum PJ, Hobson KA (2000) Trophic relationships among Antarctic fulmarine petrels: insights into dietary overlap and chick provisioning strategies inferred from stable-isotope (δ15N and δ13C) analyses. Mar Ecol Prog Ser 198:273–281CrossRefGoogle Scholar
  36. Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150:447–461CrossRefGoogle Scholar
  37. 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
  38. Lecoq M, Catry P, Granadeiro JP (2011) Population trends of Cory’s shearwaters Calonectris diomedea borealis breeding at Berlenga Islands, Portugal. Airo 20:36–41Google Scholar
  39. Lewis S, Sherratt TN, Hamer KC, Wanless S (2001) Evidence of intra-specific competition for food in a pelagic seabird. Nature 412:816–819CrossRefGoogle Scholar
  40. Machu E, Ettahiri O, Kifani S, Benazzouz A, Makaoui A, Demarcq H (2009) Environmental control of the recruitment of sardines (Sardina pilchardus) over the western Saharan shelf between 1995 and 2002: a coupled physical/biogeochemical modelling experiment. Fish Oceanogr 18:287–300CrossRefGoogle Scholar
  41. Magalhães MC, Santos RS, Hamer KC (2008) Dual-foraging of Cory’s shearwaters in the Azores: feeding locations, behaviour at sea and implications for food provisioning of chicks. Mar Ecol Prog Ser 359:283–293CrossRefGoogle Scholar
  42. Navarro J, González-Solís J (2009) Environmental determinants of foraging strategies in Cory’s shearwaters Calonectris diomedea. Mar Ecol Prog Ser 378:259–267CrossRefGoogle Scholar
  43. Navarro J, González-Solís J, Viscor G (2007) Nutritional and feeding ecology in the Cory’s shearwater (Calonectris diomedea) during breeding. Mar Ecol Prog Ser 351:261–271CrossRefGoogle Scholar
  44. Navarro J, Louzao M, Igual JM, Oro D, Delgado A, Arcos JM, Genovart M, Hobson KA, Forero MG (2009) Seasonal changes in the diet of a critically endangered seabird and the importance of trawling discards. Mar Biol 156:2571–2578CrossRefGoogle Scholar
  45. Orians GH, Pearson NE (1979) On the theory of central place foraging. In: Horn DJ, Mitchell RD, Stairs GR (eds) Analysis of ecological systems. Ohio State University Press, Columbus, pp 154–177Google Scholar
  46. Paiva VH, Geraldes P, Ramírez I, Meirinho A, Garthe S, Ramos JA (2010a) Foraging plasticity in a pelagic seabird species along a marine productivity gradient. Mar Ecol Prog Ser 398:259–274CrossRefGoogle Scholar
  47. Paiva VH, Geraldes P, Ramírez I, Meirinho A, Garthe S, Ramos JA (2010b) Oceanographic characteristics of areas used by Cory’s shearwaters during short and long foraging trips in the North Atlantic. Mar Biol 157:1385–1399CrossRefGoogle Scholar
  48. Paiva VH, Xavier J, Geraldes P, Ramírez I, Meirinho A, Garthe S, Ramos JA (2010c) Foraging ecology of Cory’s shearwaters in different ecological environments of the North Atlantic. Mar Ecol Prog Ser 410:257–268CrossRefGoogle Scholar
  49. Passos C, Navarro J, Giudici A, González-Solís J (2010) Effects of extra mass on the pelagic behavior of a seabird. Auk 127:100–107CrossRefGoogle Scholar
  50. Pedrocchi V, Oro D, González-Solís J (1996) Differences between diet of adult and chick Audouin’s gulls Larus audouinii at the Chafarinas Islands, SW Mediterranean. Ornis Fenn 73:124–130Google Scholar
  51. Phillips RA, Xavier JC, Croxall JP (2003) Effects of satellite transmitters on albatrosses and petrels. Auk 120:1082–1090CrossRefGoogle Scholar
  52. Phillips RA, Wakefield ED, Croxall JP, Fukuda A, Higuchi H (2009) Albatross foraging behaviour: no evidence for dual foraging, and limited support for anticipatory regulation of provisioning at South Georgia. Mar Ecol Prog Ser 391:279–292CrossRefGoogle Scholar
  53. Pinaud D, Cherel Y, Weimerskirch H (2005) Effect of environmental variability on habitat selection, diet, provisioning behaviour and chick growth in yellow-nosed albatrosses. Mar Ecol Prog Ser 298:295–304CrossRefGoogle Scholar
  54. Pinheiro JC, Bates DM, DebRoy S, Sarkar D, R Development Core Team (2011) nlme: linear and nonlinear mixed effects models. R package version 3.1-102Google Scholar
  55. 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 152:179–189CrossRefGoogle Scholar
  56. Quéro J-C, Porché P, Vayne JJ (2003) Guide des Poissons de l’Atlantique Européen. Delachaux & Niestlé, ParisGoogle Scholar
  57. Ramos JA, Sola E, Monteiro LR, Ratcliffe N (1998) Prey delivered to roseate tern chicks in the Azores. J Field Ornithol 69:419–429Google Scholar
  58. Richoux NB, Jaquemet S, Bonnevie BT, Cherel Y, McQuaid CD (2010) Trophic ecology of grey-headed albatrosses from Marion Island, Southern Ocean: insights from stomach contents and diet tracers. Mar Biol 157:1755–1766CrossRefGoogle Scholar
  59. Roberts JJ, Best BD, Dunn DC, Treml EA, Halpin PN (2010) Marine geospatial ecology tools: an integrated framework for ecological geoprocessing with ArcGIS, Python, R, MATLAB, and C++. Environ Model Softw 25:1197–1207CrossRefGoogle Scholar
  60. Sears J, Hatch SA, O’Brien DM (2009) Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 159:41–48CrossRefGoogle Scholar
  61. Sousa FM, Nascimento S, Casimiro H, Boutov D (2008) Identification of upwelling areas on the sea surface temperature images using fuzzy clustering. Remote Sens Environ 112:2817–2823CrossRefGoogle Scholar
  62. R Development Core Team (2009) R: a language and environment for statistical computing (2.10.1). R Foundation for Statistical Computing, ViennaGoogle Scholar
  63. Thompson DR, Phillips RA, Stewart FM, Waldron S (2000) Low δ13C signatures in pelagic seabirds: lipid ingestion as a potential source of 13C-depleted carbon in the Procellariiformes. Mar Ecol Prog Ser 208:265–271CrossRefGoogle Scholar
  64. Uttley JD, Walton P, Monaghan P, Austin G (1994) The effects of food abundance on breeding performance and adult time budgets of Guillemots Uria aalge. Ibis 136:205–213CrossRefGoogle Scholar
  65. Weimerskirch H (1998) How can a pelagic seabird provision its chick when relying on a distant food resource? Cyclic attendance at the colony, foraging decision and body condition in sooty shearwaters. J Anim Ecol 67:99–109CrossRefGoogle Scholar
  66. Weimerskirch H, Cherel Y (1998) Feeding ecology of short-tailed shearwaters: breeding in Tasmania and foraging in the Antarctic? Mar Ecol Prog Ser 167:261–274CrossRefGoogle Scholar
  67. Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese E (1986) Fishes of the North-eastern Atlantic and the Mediterranean. UNESCO, ParisGoogle Scholar
  68. Williams CT, Buck CL, Sears J, Kitaysky AS (2007) Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds. Oecologia 153:11–18CrossRefGoogle Scholar
  69. Wilson RP (1984) An improved stomach pump for penguins and other seabirds. J Field Ornithol 55:109–112Google Scholar
  70. Wilson RP, Pütz K, Peters G, Culik BM, Scolaro JA, Charrassin JB, Ropert-Coudert Y (1997) Long-term attachment of transmitting and recording devices to penguins and others seabirds. Wildl Soc Bull 25:101–106Google Scholar
  71. Wilson LJ, Daunt F, Wanless S (2004) Self-feeding and chick provisioning diet differ in the common guillemot Uria aalge. Ardea 92:197–208Google Scholar
  72. Xavier JC, Magalhães MC, Mendonça AS, Antunes M, Carvalho N, Machete M, Santos RS, Paiva V, Hamer KC (2011) Changes in diet of Cory’s Shearwaters Calonectris diomedea breeding in the Azores. Mar Ornithol 39:129–134Google Scholar
  73. Ydenberg RC, Welham CVJ, Schmid-Hempel R, Schmid-Hempel P, Beauchamp G (1994) Time and energy constraints and the relationship between currencies in foraging theory. Behav Ecol 5:28–34CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Hany Alonso
    • 1
    • 2
  • José P. Granadeiro
    • 4
  • Vitor H. Paiva
    • 2
  • Ana S. Dias
    • 3
  • Jaime A. Ramos
    • 2
  • Paulo Catry
    • 1
    • 3
  1. 1.Eco-Ethology Research Unit, ISPALisbonPortugal
  2. 2.Department of Life Sciences, Institute of Marine Research (IMAR/CMA)University of CoimbraCoimbraPortugal
  3. 3.Museu Nacional História NaturalUniversidade de LisboaLisbonPortugal
  4. 4.Centro de Estudos do Ambiente e do Mar (CESAM)/Museu Nacional de História NaturalUniversidade de LisboaLisbonPortugal

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