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Polar Biology

, Volume 41, Issue 6, pp 1175–1186 | Cite as

Ontogeny, tissue, and species but not sex influence stable isotopic values of three albatross species

  • Maëlle Connan
  • Bo Bonnevie
  • Christopher McQuaid
Original Paper

Abstract

The use of indirect dietary markers, including stable isotopes, has immensely improved our knowledge of seabird trophic ecology throughout their annual cycle. Important aspects include differences in trophic niche between adults and chicks at the intra- and inter-specific levels and tissue-dependent differentiation in chicks. Using stable isotopic niche as a proxy for trophic ecology, we investigated how three closely related albatross species co-exist in the sub-Antarctic Prince Edward Islands. The effects of age, sex, tissue, and species on the isotopic niche were observed for Grey-headed Thalassarche chrysostoma, Sooty Phoebetria fusca, and Light-mantled Phoebetria palpebrata Albatrosses breeding on Marion Island. At the end of chick-rearing, carbon and nitrogen stable isotope values differed according to age, tissue, and species but not the sex of either adults or chicks. A complex pattern was revealed as the three species exhibited contrasting results. For example, values for δ13C or δ15N of chick blood could be depleted, enriched or similar relative to that of adults, depending on species. Stable isotope differences between blood and feathers likely reflect differences in their amino acid composition, while adult/chick differences will relate to their different physiological needs and diet. The results indicate that co-existence of the three species on the island is facilitated through resource partitioning among species in terms of foraging areas and in the trophic levels at which adults feed for themselves and their chicks. This work brings new insights into the effect of intrinsic factors on the foraging ecology of marine top predators.

Keywords

Thalassarche chrysostoma Phoebetria palpebrata Phoebetria fusca Prince Edward Islands Southern Ocean 

Notes

Acknowledgements

The authors thank PG Ryan, MGW Jones, B Dyer, and L Clokie for their valuable advices in the field. Isotope samples were analysed by I Newton at the Stable Light Isotope Laboratory of the University of Cape Town under the supervision of J Lanham. Funding and logistical support was provided by the Department of Environmental Affairs and Tourism through the South African National Antarctic Program and administered by the National Research Foundation. This work is based on research supported by the South African Research Chairs Initiative of the Department of Science and Technology and the National Research Foundation. The authors thank Prof Piepenburg, Prof Quillfeldt, and an anonymous reviewer for their valuable comments on an earlier version of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international guidelines for the care and use of animals were followed. All procedures performed during the study were in accordance with the ethical standards of Rhodes University and were undertaken under an ethics clearance granted by its Animal Ethics committee.

References

  1. Ansorge IJ, Lutjeharms JRE (2002) The hydrography and dynamics of the ocean environment of the Prince Edward Islands (Southern Ocean). J Mar Syst 37:107–127CrossRefGoogle Scholar
  2. Awkerman JA, Hobson KA, Anderson DJ (2007) Isotopic (δ15N and δ13C) evidence for intersexual foraging differences and temporal variation in habitat use in waved Albatrosses. Can J Zool 85:273–279CrossRefGoogle Scholar
  3. Barrett R, Camphuysen KCJ, Anker-Nilssen T, Chardine JW, Furness WR, Grarthe 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. Berruti A (1979) The breeding biologies of the Sooty albatrosses Phoebetria fusca and P. palpebrata. Emu 79:161–175CrossRefGoogle Scholar
  5. BirdLife International (2016) IUCN red list for birds. http://www.birdlife.org. Accessed 9 Jan 2016
  6. Burger AE, Shaffer SA (2008) Perspectives in ornithology: application of tracking and data-logging technology in research and conservation of seabirds. Auk 125:253–264CrossRefGoogle Scholar
  7. Burke CM, Montevecchi WA, Regular PM (2015) Seasonal variation in parental care drives sex-specific foraging by a monomorphic seabird. PLoS ONE 10:e0141190CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cameron-MacMillan ML, Walsh CJ, Wilhelm SI, Storey AE (2007) Male chicks are more costly to rear than females in a monogamous seabird, the common murre. Behav Ecol 18:81–85CrossRefGoogle Scholar
  9. 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
  10. Ceia FR, Phillips RA, Ramos JA, Cherel Y, Vieira RP, Richard P, Xavier JC (2012) Short- and long-term consistency in the foraging niche of wandering Albatrosses. Mar Biol 159:1581–1591CrossRefGoogle Scholar
  11. Ceia FR, Ramos JA, Phillips RA, Cherel Y, Jones DC, Vieira RP, Xavier JC (2015) Analysis of stable isotope ratios in blood of tracked wandering albatrosses fails to distinguish a δ13C gradient within their winter foraging areas in the southwest Atlantic Ocean. Rapid Commun Mass Spectrom 29:2328–2336CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chambers GK, Moeke C, Steel R, Trueman JWH (2009) Phylogenetic analysis of the 24 named albatross taxa based on full mitochondrial cytochrome b DNA sequences. Notornis 56:82–94Google Scholar
  13. Cheah CC, Hansen IA (1970) Stomach oil and tissue lipids of the petrels Puffinus pacificus and Pterodroma macroptera. Int J Biochem 1:203–208CrossRefGoogle Scholar
  14. 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
  15. Cherel Y, Ridoux V (1992) Prey species and nutritive value of food fed during summer to king penguin Aptenodytes patagonicus chicks at possession island, crozet archipelago. Ibis 134:118–127CrossRefGoogle Scholar
  16. Cherel Y, Ducatez S, Fontaine C, Richard P, Guinet C (2008) Stable isotopes reveal the trophic position and mesopelagic fish diet of female southern elephant seals breeding on the Kerguelen Islands. Mar Ecol Prog Ser 370:239–247CrossRefGoogle Scholar
  17. Cherel Y, Fontaine C, Richard P, Labat J-P (2010) Isotopic niches and trophic levels of myctophid fishes and their predators in the southern ocean. Limnol Oceanogr 55:324–332CrossRefGoogle Scholar
  18. Cherel Y, Jaquemet S, Maglio A, Jaeger A (2014) Differences in δ13C and δ15N values between feathers and blood of seabird chicks: implications for non-invasive isotopic investigations. Mar Biol 161:229–237CrossRefGoogle Scholar
  19. Clarke A, Prince PA (1976) The origin of stomach oil in marine birds: analyses of the stomach oil from six species of subantarctic Procellariiform birds. J Exp Mar Biol Ecol 23:15–30CrossRefGoogle Scholar
  20. Connan M, Kelly CMR, McQuaid CD, Bonnevie BT, Barker NP (2011) Morphological versus molecular identification of Sooty (Phoebetria fusca) and Light-mantled (P. palpebrata) albatross chicks. Polar Biol 34:791–798CrossRefGoogle Scholar
  21. Connan M, McQuaid CD, Bonnevie BT, Smale MJ, Cherel Y (2014) Combined stomach content, lipid and stable isotope analyses reveal spatial and trophic partitioning among three sympatric albatrosses from the Southern Ocean. Mar Ecol Prog Ser 497:259–272CrossRefGoogle Scholar
  22. Cooper J, Klages NTW (1995) The diets and dietary segregation of sooty albatrosses (Phoebetria spp.) at subantarctic marion island. Antarct Sci 7:15–23CrossRefGoogle Scholar
  23. Corbisier TN, Petti MAV, Skowronski RSP, Brito TAS (2004) Trophic relationships in the nearshore zone of martel inlet (King George Island, Antarctica): δ13C stable-isotope analysis. Polar Biol 27:75–82CrossRefGoogle Scholar
  24. Crossin GT, Phillips RA, Lattin CR, Romero LM, Bordeleau X, Harris CM, Love OP, Williams TD (2017) Costs of reproduction and carry-over effects in breeding albatrosses. Antarct Sci 29:155–164CrossRefGoogle Scholar
  25. Cucherousset J, Villéger S (2015) Quantifying the multiple facets of isotopic diversity: new metrics for stable isotope ecology. Ecol Indic 56:152–160CrossRefGoogle Scholar
  26. Dalerum F, Angerbjörn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658CrossRefPubMedGoogle Scholar
  27. DeNiro MJ, Epstein S (1976) You are what you eat (plus a few per mill): the carbon isotope cycle in food chains. Geol Soc Am Bull 8:834–835Google Scholar
  28. Durgadoo JV, Ansorge IJ, Lutjeharms JRE (2010) Oceanographic observations of eddies impacting the Prince Edward Islands, South Africa. Antarc Sci 22:211–219CrossRefGoogle Scholar
  29. Evans Ogden LJ, Hobson KA, Lank DB (2004) Blood isotopic (δ13C and δ15N) turnover and diet-tissue fractionation factors in captive dunlin (Calidris alpina pacifica). Auk 121:170–177CrossRefGoogle Scholar
  30. François R, Altabet MA, Goericke R (1993) Changes in the δ13C of surface water particulate organic matter across the subtropical convergence in the SW Indian Ocean. Global Biogeochem Cy 7:627–644CrossRefGoogle Scholar
  31. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121CrossRefGoogle Scholar
  32. Hanson NN, Wurster CM, Bird MI, Reid K, Boyd IL (2009) Intrinsic and extrinsic forcing in life histories: patterns of growth and stable isotopes in male Antarctic fur seal teeth. Mar Ecol Prog Ser 388:263–272CrossRefGoogle Scholar
  33. Hayward A, Gillooly JF (2011) The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS ONE 6:e16557CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hilton GM, Thompson DR, Sagar PM, Cuthbert RJ, Cherel Y, Bury SJ (2006) A stable isotopic investigation into the causes of decline in a sub-Antarctic predator, the rockhopper penguin Eudyptes chrysocome. Glob Change Biol 12:611–625CrossRefGoogle Scholar
  35. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188CrossRefGoogle Scholar
  36. Hobson KA, Gibbs HL, Gloutney ML (1997) Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotope analysis. Can J Zool 75:1720–1723CrossRefGoogle Scholar
  37. 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 80:595–602CrossRefPubMedGoogle Scholar
  38. Jaeger A, Blanchard P, Richard P, Cherel Y (2009) Using carbon and nitrogen isotopic values of body feathers to infer inter- and intra-individual variations of seabird feeding ecology during moult. Mar Biol 156:1233–1240CrossRefGoogle Scholar
  39. Jaeger A, Connan M, Richard P, Cherel Y (2010a) Use of stable isotopes to quantify seasonal changes of trophic niche and levels of population and individual specialisation in seabirds. Mar Ecol Prog Ser 401:269–277CrossRefGoogle Scholar
  40. Jaeger A, Lecomte VJ, Weimerskirch H, Richard P, Cherel Y (2010b) Seabird satellite tracking validates the use of latitudinal isoscapes to depict predators’ foraging areas in the Southern Ocean. Rapid Commun Mass Spectro 24:3456–3460CrossRefGoogle Scholar
  41. Jaeger A, Jaquemet S, Phillips RA, Wanless RM, Richard P, Cherel Y (2013) Stable isotopes document inter- and intra-specific variation in feeding ecology of nine large southern Procellariiformes. Mar Ecol Prog Ser 490:255–266CrossRefGoogle Scholar
  42. Jennings S, Varsani A, Dugger KM, Ballard G, Ainley DG (2016) Sex-based differences in Adélie penguin (Pygoscelis adeliae) chick growth rates and diet. PLoS ONE 11:e0149090CrossRefPubMedPubMedCentralGoogle Scholar
  43. Jouventin P, Weimerskirch H (1984) L’albatros fuligineux à dos sombre Phoebetria fusca, exemple de stratégie d’adaptation extrême à la vie pélagique. Rev Ecol (Terre Vie) 39:401–427Google Scholar
  44. Karnovsky NJ, Hobson KA, Iverson SJ (2012) From lavage to lipids: estimating diets of seabirds. Mar Ecol Prog Ser 451:263–284CrossRefGoogle Scholar
  45. Kernaléguen L, Cazelles B, Arnould JPY, Richard P, Guinet C, Cherel Y (2012) Long-term species, sexual and individual variations in foraging strategies of fur seals revealed by stable isotopes in whiskers. PLoS ONE 7:e32916CrossRefPubMedPubMedCentralGoogle Scholar
  46. Krüger L, Ramos JA, Xavier JC, Grémillet D, González-Solís J, Petry MV, Phillips RA, Wanless RM, Paiva VH (2018) Projected distribution of Southern Ocean albatrosses, petrels and fisheries as a consequence of climatic change. Ecography 41:195–208CrossRefGoogle Scholar
  47. Lorrain A, Graham B, Ménard F, Popp B, Bouillon S, van Breugel P, Cherel Y (2009) Nitrogen and carbon isotope values of individual amino acids: a tool to study foraging ecology of penguins in the Southern Ocean. Mar Ecol Prog Ser 391:293–306CrossRefGoogle Scholar
  48. Michener RH, Kaufman L (2007) Stable isotope ratios as tracers in marine food webs: An update. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science. Blackwell Publishing Ltd, Singapore, pp 238–282CrossRefGoogle Scholar
  49. Michener R, Lajtha K (2007) Stable isotopes in ecology and environmental science. Blackwell Publishing Ltd, SingaporeCrossRefGoogle Scholar
  50. Mizutani H, Fukuda M, Kabaya Y (1992) δ13C and δ15N enrichment factors of feathers of 11 species of adult birds. Ecology 73:1391–1395CrossRefGoogle Scholar
  51. Nel DC, Nel JL, Ryan PG, Klages NTW, Wilson RP, Robertson G (2000) Foraging ecology of grey-headed mollymawks at Marion Island, southern Indian Ocean, in relation to longline fishing activity. Biol Conserv 96:219–231CrossRefGoogle Scholar
  52. Péron C, Weimerskirch H, Bost C-A (2012) Projected poleward shift of king penguins’ (Aptenodytes patagonicus) foraging range at the Crozet Islands, southern Indian Ocean. Proc R Soc Lond B 279:2515–2523CrossRefGoogle Scholar
  53. Phillips RA, Hamer KC (2000) Postnatal development of northern fulmar chicks, Fulmarus glacialis. Physiol Biochem Zool 73:597–604CrossRefPubMedGoogle Scholar
  54. Phillips RA, Silk JRD, Phalan B, Catry P, Croxall JP (2004) Seasonal sexual segregation in two Thalassarche albatross species: competitive exclusion, reproductive role specialization or foraging niche divergence? Proc R Soc Lond B 271:1283–1291CrossRefGoogle Scholar
  55. Phillips RA, Bearhop S, McGill RAR, Dawson DA (2009) Stable isotopes reveal individual variation in migration strategies and habitat preferences in a suite of seabirds during the nonbreeding period. Oecologia 160:795–806CrossRefPubMedGoogle Scholar
  56. Phillips RA, McGill RAR, Dawson DA, Bearhop S (2011) Sexual segregation in distribution, diet and trophic level of seabirds: insights from stable isotope analysis. Mar Biol 158:2199–2208CrossRefGoogle Scholar
  57. Quillfeldt P, McGill RAR, Furness RW (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 295:295–304CrossRefGoogle Scholar
  58. Quillfeldt P, Bugoni L, McGill RAR, Masello JF, Furness RW (2008a) Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies. Mar Biol 155:593–598CrossRefGoogle Scholar
  59. Quillfeldt P, McGill RAR, Masello JF, Weiss F, Strange IJ, Brickle P, Furness RW (2008b) Stable isotope analysis reveals sexual and environmental variability and individual consistency in foraging of thin-billed prions. Mar Ecol Prog Ser 373:137–148CrossRefGoogle Scholar
  60. Quillfeldt P, Masello JF, McGill RAR, Adams M, Furness RW (2010) Moving polewards in winter: a recent change in the migratory strategy of a pelagic seabird? Front Zool 7:15–26CrossRefPubMedPubMedCentralGoogle Scholar
  61. Ramos R, González-Solís J (2012) Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Front Ecol Environ 10:258–266CrossRefGoogle Scholar
  62. Ricketts C, Prince PA (1981) Comparison of growth of Albatrosses. Ornis Scand 12:120–124CrossRefGoogle Scholar
  63. Schoombie S, Crawford RJM, Makhado AB, Dyer BM, Ryan PG (2016) Recent population trends of sooty and light-mantled albatrosses breeding on Marion Island. Afr J Mar Sci 38:119–127CrossRefGoogle Scholar
  64. Schoombie S, Dilley BJ, Davies D, Glass T, Ryan PG (2017) The distribution of breeding Sooty Albatrosses from the three most important breeding sites: gough, Tristan and the Prince Edward Islands. Emu 117:160–169CrossRefGoogle Scholar
  65. Sears J, Hatch SA, O’Brien DM (2009) Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 159:41–48CrossRefPubMedGoogle Scholar
  66. Team RC (2016) A Language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  67. Terauds A, Gales R (2006) Provisioning strategies and growth patterns of Light-mantled Sooty Albatrosses Phoebetria palpebrata on Macquarie Island. Polar Biol 29:917–926CrossRefGoogle Scholar
  68. Trull TW, Armand L (2001) Insights into Southern Ocean carbon export from the δ13C of particles and dissolved inorganic carbon during the SOIREE iron release experiment. Deep-Sea Res II 48:2655–2680CrossRefGoogle Scholar
  69. Warham J (1996) The behaviour, population biology and physiology of the petrels. Academic Press, London and San DiegoGoogle Scholar
  70. Warham J, Watts R, Dainty RJ (1976) The composition, energy content and function of the stomach oils of Petrels (Order, Procellariiformes). J Exp Mar Biol Ecol 23:1–13CrossRefGoogle Scholar
  71. Weimerskirch H, Lys P (2000) Seasonal changes in the provisioning behaviour and mass of male and female wandering albatrosses in relation to the growth of their chick. Polar Biol 23:733–744CrossRefGoogle Scholar
  72. Weimerskirch H, Jouventin P, Stahl JC (1986) Comparative ecology of the six albatross species breeding on the Crozet Islands. Ibis 128:195–213CrossRefGoogle Scholar
  73. Weimerskirch H, Barbraud C, Lys P (2000) Sex differences in parental investment and chick growth in wandering albatrosses: fitness consequences. Ecology 81:309–318CrossRefGoogle Scholar
  74. Whitehead TO, Connan M, Ropert-Coudert Y, Ryan PG (2017) Subtle but significant segregation in the feeding ecology of sympatric penguins during the critical pre-moult period. Mar Ecol Prog Ser 565:227–236CrossRefGoogle Scholar
  75. Xavier JC, Trathan PN, Ceia FR, Tarling GA, Adlard S, Fox D, Edwards EWJ, Vieira RP, Medeiros R, De Broyer C, Cherel Y (2017) Sexual and individual foraging segregation in Gentoo penguins Pygoscelis papua from the Southern Ocean during an abnormal winter. PLoS ONE 12:e0174850CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa
  2. 2.Department of Zoology, Marine Apex Predator Unit, Institute for Coastal and Marine ResearchNelson Mandela UniversityPort ElizabethSouth Africa

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