Advertisement

Marine Biology

, Volume 155, Issue 6, pp 637–647 | Cite as

The role of stable isotopes and mercury concentrations to describe seabird foraging ecology in tropical environments

  • Teresa Catry
  • Jaime A. Ramos
  • Matthieu Le Corre
  • Jessica Kojadinovic
  • Paco Bustamante
Original Paper

Abstract

Nitrogen (δ15N) and carbon (δ13C) stable isotopes and contaminants, such as mercury, have been widely used to characterise foraging ecology of temperate and polar seabirds. In this study, for the first time, we used isotopic signatures and mercury levels of feathers and blood of eight tropical seabird species, that forage in a range-gradient between inshore and offshore areas, to describe the foraging habits of a large tropical seabird community (from two neighboring islands of the Seychelles archipelago, western Indian Ocean) during both the breeding and inter-breeding periods. Overall, we found a high overlap in both δ15N and δ13C signatures among species. The high inter-specific overlap in δ15N values was expected, given the similarities in the diet of the species from this community. However, several unexpected results, such as (1) the consistently higher δ15N signatures of white terns (Gygis alba), (2) the large variation in inter-specific differences in δ15N signatures among the sampling groups (season, age, island and tissue) and (3) the consistent low δ15N values of breeding birds during the northwest monsoon (austral summer), suggest that δ15N signatures cannot be used as indicators of seabird trophic levels in this community. The high inter-specific overlap in δ13C signatures and the absence, during the breeding season, of a δ13C gradient that follows the inshore-offshore foraging gradient within the community can be explained by the habitat homogeneity of the Seychelles continental shelf and suggest that birds forage mostly within the limits of this “plateau”. On the other hand, the similarities in δ13C values between the breeding and inter-breeding periods in species that are known to show post-breeding dispersal, strongly support the hypothesis of a lack of latitudinal variation in δ13C signatures of POM in the central Indian Ocean, and the consequent inaccuracy of δ13C values to track seabird movements within this geographic area. Inter-specific differences in mercury levels seem to be related to prey size, while consistent higher mercury concentrations in one of the studied islands suggest different island mercury-backgrounds and possible segregation in foraging areas between the seabirds of the two islands.

Keywords

Mercury Level Western Indian Ocean Body Feather High Mercury Level Sooty Tern 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to acknowledge Island Conservation Society (ICS) and Nature Seychelles for permission to work on Aride and Cousin Islands, respectively. Two anonymous reviewers provide very helpful comments on an early draft of the manuscript. TC was funded by a portuguese doctoral grant from Fundação para a Ciência e Tecnologia (SFRH/BD/16706/2004). This work is part of a regional programme on seabirds as bioindicators of the marine environment, funded by the Western Indian Ocean Marine Science Association (Marine Science for Management Grant, MASMA/AG/2004/04), and by the Agence National pour la Recherche (Program REMIGE-ANR Biodiversité 2005–011). This research was conducted under permission of the Seychelles Bureau of Standards, Republic of Seychelles.

Supplementary material

227_2008_1060_MOESM1_ESM.doc (82 kb)
Supplementary tables (DOC 82 kb)

References

  1. Ainley DG, Ribic CA, Ballard G, Heath S, Gaffney I, Karl BJ et al (2004) Geographic structure of Adélie Penguin populations: overlap in colony-specific foraging areas. Ecol Monogr 74:159–178. doi: 10.1890/02-4073 CrossRefGoogle 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 232:281–290. doi: 10.3354/meps232281 CrossRefGoogle Scholar
  3. Ashmole NP (1963a) The Black Noddy Anous tenuirostris on Ascension Island. Part 1. General biology. Ibis 103b:235–273. doi: 10.1111/j.1474-919X.1962.tb07246.x CrossRefGoogle Scholar
  4. Ashmole NP (1963b) The biology of the wideawake or sooty tern Sterna fuscata on Ascension Island. Ibis 103b:297–351. doi: 10.1111/j.1474-919X.1963.tb06757.x CrossRefGoogle Scholar
  5. Bailey RS (1968) The pelagic distribution of sea-birds in the western Indian Ocean. Ibis 110:493–519. doi: 10.1111/j.1474-919X.1968.tb00060.x CrossRefGoogle Scholar
  6. Ballance LT, Pitman RL (1999) Foraging ecology of tropical seabirds. In: Adams NJ, Slotow RH (eds) Proc 22 Int. Ornithol. Congr., Durban. Johannesburg, BirdLife South Africa, pp 2057–2071Google Scholar
  7. Bearhop S, Phillips RA, Thompson DR, Waldron S, Furness RW (2000a) 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 195:261–268. doi: 10.3354/meps195261 CrossRefGoogle Scholar
  8. Bearhop S, Waldron S, Thompson DR, Furness RW (2000b) Bioamplification of mercury in Great Skua Catharacta skua chicks: the influence of trophic status as determined by stable isotope signatures of blood and feathers. Mar Pollut Bull 40:181–185. doi: 10.1016/S0025-326X(99)00205-2 CrossRefGoogle Scholar
  9. Becker PH, González-Solís J, Behrends B, Croxall J (2002) Feather mercury levels in seabirds at South Georgia: influence of trophic position, sex and age. Mar Ecol Prog Ser 243:261–269. doi: 10.3354/meps243261 CrossRefGoogle Scholar
  10. Braithwaite CJR (1984) Geology of the Seychelles. In: Stoddart DR (ed) Biogeography and ecology of the Seychelles islands. Junk, The HagueGoogle Scholar
  11. Bryan GW (1979) Bioaccumulation of marine pollutants. Philos Trans R Soc Lond B Biol Sci 286:483–505. doi: 10.1098/rstb.1979.0042 CrossRefGoogle Scholar
  12. Burger J, Shukla T, Dixon C, Shukla S, McMahon MJ, Ramos R et al (2001) Metals in feathers of Sooty Tern, White Tern, Gray-backed Tern and Brown Noddy from islands in the North Pacific. Environ Monit Assess 71:71–89. doi: 10.1023/A:1011695829296 CrossRefGoogle Scholar
  13. Burger J, Schreiber EAE, Gochfeld M (1993) Metal in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 5:203–311Google Scholar
  14. Catry T, Ramos JA, Jaquemet S, Faulquier L, Berlincourt M, Hauselmann A, Pinet P, Le Corre M. Comparative foraging ecology of a tropical seabird community of Seychelles, western Indian Ocean. Mar Ecol Prog Ser (in press)Google Scholar
  15. Croxall JP (1987) Seabirds: feeding ecology and role in marine ecosystems. Cambridge University Press, CambridgeGoogle Scholar
  16. Cherel Y, Hobson KA, Weimerskirch H (2000) Using stable-isotope analysis of feathers to distinguish moulting and breeding origins of seabirds. Oecologia 122:155–162. doi: 10.1007/PL00008843 CrossRefGoogle Scholar
  17. Cherel Y, Phillips RA, Hobson KA, McGill R (2006) Stable isotope evidence of diverse species-specific and individual wintering strategies in seabirds. Biol Lett 2:301–303. doi: 10.1098/rsbl.2006.0445 CrossRefGoogle Scholar
  18. Cherel Y, Hobson KA (2007) Geographical variation in carbon isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser 329:281–287. doi: 10.3354/meps329281 CrossRefGoogle Scholar
  19. Diamond AW (1983) Feeding overlap in some tropical and temperate seabird communities. Stud Avian Biol 8:24–46Google Scholar
  20. Diamond A, Prŷs-Jones RP (1986) The biology of terns nesting at Aldabra Atoll, Indian Ocean, with particular reference to breeding seasonality. J Zool 210:527–549CrossRefGoogle Scholar
  21. Dorward DF (1963) The Fairy Tern Gygis alba on Ascension Island. Ibis 103b:365–378. doi: 10.1111/j.1474-919X.1963.tb06759.x CrossRefGoogle Scholar
  22. Eisler R (1987) Mercury hazards to fish, wildlife and invertebrates: a synoptic review. Biol Rev Camb Philos Soc 85:1–10Google Scholar
  23. Feare CJ (1981) Breeding schedules and feeding strategies of Seychelles seabirds. Ostrich 32:179–185CrossRefGoogle Scholar
  24. 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
  25. François R, Altabet MA, Goericke R, McCorkle DC, Brunet C, Poisson A (1993) Changes in the δ13C of surface water particulate organic matter across the subtropical convergence in the SW Indian Ocean. Global Biogeochem Cycles 7:627–644. doi: 10.1029/93GB01277 CrossRefGoogle Scholar
  26. González-Sólis J, Sanpera C, Ruiz X (2002) Metals and selenium as bioindicators of geographic and trophic segregation in giant petrels Macronectes spp. Mar Ecol Prog Ser 244:257–264. doi: 10.3354/meps244257 CrossRefGoogle Scholar
  27. Hamer KC, Schreiber EA, Burger J (2001) Breeding biology, life histories, and life history–environment interactions in seabirds. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, FLGoogle Scholar
  28. Harrison CS, Hida TS, Seki MP (1983) Hawaiian seabird feeding ecology. Wildl Monogr 85:1–71Google Scholar
  29. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes. II. Factors influencing diet-tissue fractionation. Condor 94:189–197. doi: 10.2307/1368808 CrossRefGoogle Scholar
  30. Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798. doi: 10.2307/5256 CrossRefGoogle Scholar
  31. Hobson KA, Gibbs HL, Gloutney ML (2005) Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotope analysis. Can J Zool 75:1720–1723. doi: 10.1139/z97-799 CrossRefGoogle Scholar
  32. Hobson KA, Gilchrist G, Falk K (2002) Isotopic investigations of seabirds of the North Water Polynya: contrasting trophic relationships between the eastern and western sectors. Condor 104:1–11. doi: 10.1650/0010-5422(2002)104[0001:IIOSOT]2.0.CO;2 CrossRefGoogle Scholar
  33. Jaquemet S, Le Corre M, Weimerskirch H (2004) Seabird community structure in a coastal tropical environment: importance of associations with sub-surface predators and of Fish Aggregating Devices (FADs). Mar Ecol Prog Ser 268:281–292. doi: 10.3354/meps268281 CrossRefGoogle Scholar
  34. Jaquemet S, Potier M, Cherel Y, Kojadinovic J, Bustamante P, Richard P, Catry T, Ramos JA. Diet and ecological niche of the sooty tern Sterna fuscata in the southwest Indian Ocean. Mar Biol (in press)Google Scholar
  35. Kojadinovic J, Potier M, Le Corre M, Cosson RP, Bustamante P (2006) Mercury content in commercial pelagic fish and its risk assessment in the Western Indian Ocean. Sci Total Environ 366:688–700. doi: 10.1016/j.scitotenv.2006.02.006 CrossRefGoogle Scholar
  36. Kojadinovic J, Le Corre M, Cosson RP, Bustamante P (2007) Trace elements in three marine birds breeding on Reunion Island (Western Indian Ocean). Part 1. Factors influencing their bioaccumulation. Arch Environ Contam Toxicol 52:418–430. doi: 10.1007/s00244-005-0225-2 CrossRefGoogle Scholar
  37. Kojadinovic J, Ménard F, Bustamante P, Cosson RP, Le Corre M (2008) Trophic ecology of marine birds and pelagic fishes from Reunion Island as determined through stable isotope analysis. Mar Ecol Prog Ser 361:239–251. doi: 10.3354/meps07355 CrossRefGoogle Scholar
  38. Massias A, Becker PH (1990) Nutritive value of food and growth in Common Tern Sterna hirundo chicks. Ornis Scand 21:187–194. doi: 10.2307/3676778 CrossRefGoogle Scholar
  39. Ménard F, Lorrain A, Potier M, Marsac F (2007) Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean. Mar Biol (Berl) 153:141–152. doi: 10.1007/s00227-007-0789-7 CrossRefGoogle Scholar
  40. Monteiro LR, Furness RW, Del Nevo AJ (1995) Mercury levels in seabirds from the Azores, Mid-North Atlantic Ocean. Arch Environ Contam Toxicol 28:304–309. doi: 10.1007/BF00213106 CrossRefGoogle Scholar
  41. Monteiro LR, Granadeiro JP, Furness RW (1998) Relationship between mercury levels and diet in Azores seabirds. Mar Ecol Prog Ser 166:259–265. doi: 10.3354/meps166259 CrossRefGoogle Scholar
  42. Monteiro LR, Furness RW (2001) Kinetics, dose–response, excretion and toxicity of methylmercury in free-living Cory’s Shearwater chicks. Environ Toxicol Chem 20:1816–1823. doi: 10.1897/1551-5028(2001)020<1816:KDREAT>2.0.CO;2 PubMedGoogle Scholar
  43. Monticelli D, Ramos JA, Tavares PC, Bataille B, Lepoint G, Devillers P (2008) Diet and foraging ecology of Roseate Terns and Lesser Noddies breeding sympatrically on Aride Island, Seychelles. Waterbirds (in press)Google Scholar
  44. Nisbet ICT, Montoya JP, Burger J, Hatch JJ (2002) Use of stable isotopes to investigate individual differences in diets and mercury exposures among Common Terns Sterna hirundo in breeding and wintering grounds. Mar Ecol Prog Ser 242:267–274. doi: 10.3354/meps242267 CrossRefGoogle Scholar
  45. Ochoa-acuña H, Sepúlveda MS, Gross TS (2002) Mercury in feathers from Chilean birds: influence of location, feeding strategy and taxonomic affiliation. Mar Pollut Bull 44:340–349. doi: 10.1016/S0025-326X(01)00280-6 CrossRefGoogle Scholar
  46. Paiva VH, Ramos JA, Catry T, Pedro P, Medeiros R, Palma J (2006) Influence of environmental factors and energetic value of food on Little Tern Sterna albifrons chick growth and food delivery. Bird Stud 53:1–11CrossRefGoogle Scholar
  47. Pearson TH (1968) The feeding biology of seabird species breeding on the Farne Islands, Northumberland. J Anim Ecol 37:521–522. doi: 10.2307/3073 CrossRefGoogle Scholar
  48. Schreiber EA, Burger J (2001) Biology of marine birds. CRC Press, Boca Raton, FLCrossRefGoogle Scholar
  49. Shealer D (2001) Foraging behavior and food of seabirds. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, FLGoogle Scholar
  50. Sherwood GD, Rose GA (2005) Stable isotope analysis of some representative fish and invertebrates of the Newfoundland and Labrador continental shelf food web. Estuar Coast Shelf Sci 63:537–549. doi: 10.1016/j.ecss.2004.12.010 CrossRefGoogle Scholar
  51. Spear LB, Ainley DG, Walker WA (2007) Foraging dynamics of seabirds in the eastern tropical Pacific Ocean. Stud Avian Biol 35Google Scholar
  52. Surman CA, Wooller RD (2003) Comparative foraging ecology of five sympatric terns at a sub-tropical island in the eastern Indian Ocean. J Zool (Lond) 259:219–230. doi: 10.1017/S0952836902003047 CrossRefGoogle Scholar
  53. Sydeman WJ, Hobson KA, Pyle P, McLaren EB (1997) Trophic relationships among seabirds in central California: combined stable isotope and conventional dietary approach. Condor 99:327–336. doi: 10.2307/1369938 CrossRefGoogle Scholar
  54. Thompson DR, Furness RW, Barrett RT (1992) Mercury concentrations in seabirds from colonies in the north-east Atlantic. Arch Environ Contam Toxicol 23:383–389. doi: 10.1007/BF00216249 CrossRefGoogle Scholar
  55. Thompson DR, Bearhop S, Speakman JR, Furness RW (1998a) Feathers as a means of monitoring mercury in seabirds: insights from stable isotope analysis. Environ Pollut 101:193–200. doi: 10.1016/S0269-7491(98)00078-5 CrossRefGoogle Scholar
  56. Thompson DR, Furness RW, Monteiro LR (1998b) Seabirds as biomonitors of mercury inputs to epipelagic and mesopelagic marine food chains. Sci Total Environ 213:299–305. doi: 10.1016/S0048-9697(98)00103-X CrossRefGoogle Scholar
  57. Thompson DR, Lilliendahl K, Solmundsson J, Furness RW, Waldron S, Phillips RA (1999) Trophic relationships among six species of Icelandic seabirds as determined through stable isotope analysis. Condor 101:898–903. doi: 10.2307/1370085 CrossRefGoogle Scholar
  58. Thompson DR, Phillips RA, Stewart FM, Waldron S (2000) Low δ13C signatures in pelagic seabirds: lipid ingestion as a potential source of δ13C-depleted carbon in the Procellariiformes. Mar Ecol Prog Ser 208:265–271. doi: 10.3354/meps208265 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Teresa Catry
    • 1
  • Jaime A. Ramos
    • 1
  • Matthieu Le Corre
    • 2
  • Jessica Kojadinovic
    • 2
    • 3
  • Paco Bustamante
    • 3
  1. 1.Institute of Marine Research (IMAR), Department of ZoologyUniversity of CoimbraCoimbraPortugal
  2. 2.Laboratoire ECOMARUniversité de la RéunionSaint Denis message Cedex 9France
  3. 3.Littoral Environnement et Sociétés (LIENSs)UMR 6250 CNRS-Université La RochelleLa Rochelle Cedex 01France

Personalised recommendations