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Trophic ecology of Grey-headed albatrosses from Marion Island, Southern Ocean: insights from stomach contents and diet tracers

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Abstract

During chick-rearing, albatrosses can alternate between long foraging trips that provide the main source of food for the adults and short foraging trips that they use to feed their young. This flexibility in foraging behaviour can lead to differences in diet composition between adults and chicks and implies that they may be vulnerable in different ways to food shortages. The trophic ecology of the Grey-headed albatross Thalassarche chrysostoma was investigated at the sub-Antarctic Prince Edward Islands during the chick-rearing period in April 2006 using a combination of approaches. Diets of adults and chicks were assessed using stable isotope ratios and fatty acid (FA) profiles of blood and/or stomach oils, in addition to stomach contents analysis. Fish from the family Macrouridae and cephalopods (particularly the onychoteuthid Kondakovia longimana) were the primary prey, whereas crustaceans (krill Euphausia superba) represented a smaller proportion of the stomach contents. Stomach oil FA profiles contained more monounsaturated FA than the profiles of plasma, which were richer in saturated FA and arachidonic acid (20:4n-6). There was also a distinct separation of adults from chicks, with higher levels of monounsaturates in chick plasma, and higher saturated FA levels (particularly 16:0) in the adult plasma. Stable carbon isotope ratios of whole blood were similar in adults and chicks, whereas stable nitrogen isotope ratios showed significant enrichment by >1‰ in chicks. The combined FA, stable isotopes and stomach contents analyses suggest clear differences in diet quality between adults and chicks, with chicks feeding at a higher trophic position through feeding more on highly nutritious fish and adults keeping much of the less nutritious zooplankton for themselves.

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References

  • Anderson ORJ, Phillips RA, McDonald RA, Shore RF, McGill RAR, Bearhop S (2009) Influence of trophic position and foraging range on mercury levels within a seabird community. Mar Ecol Prog Ser 375:277–288

    Article  CAS  Google Scholar 

  • Baker AC, Boden BP, Brinton E (1990) A practical guide to the euphausiids of the World. Natural History Museum Publications, London

    Google Scholar 

  • 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 64:1675–1691

    Article  Google Scholar 

  • Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mamm Sci 22:759–801

    Article  Google Scholar 

  • 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 194:249–261

    Article  Google Scholar 

  • Cherel Y (2008) Isotopic niches of emperor and Adélie penguins in Adélie Land, Antarctica. Mar Biol 154:813–821

    Article  Google Scholar 

  • 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 329:281–287

    Article  CAS  Google Scholar 

  • Cherel Y, Klages N (1998) A review of the food of albatrosses. In: Robertson G, Gales R (eds) Albatross biology and conservation. Surrey Beatty, Chipping Nortion, pp 113–136

    Google Scholar 

  • Cherel Y, Weimerskirch H (1999) Spawning cycle of onychoteuthid squids in the southern Indian Ocean: new information from seabird predators. Mar Ecol Prog Ser 188:93–104

    Article  Google Scholar 

  • Cherel Y, Weimerskirch H, Trouvé C (2000) Food and feeding ecology of the neritic-slope forager black-browed albatross and its relationships with commercial fisheries in Kerguelen waters. Mar Ecol Prog Ser 207:183–199

    Article  Google Scholar 

  • Cherel Y, Bocher P, Trouvé C, Weimerskirch H (2002a) Diet and feeding ecology of blue petrels Halobaena caerulea at Iles Kerguelen, Southern Indian Ocean. Mar Ecol Prog Ser 228:283–299

    Article  Google Scholar 

  • Cherel Y, Weimerskirch H, Trouvé C (2002b) Dietary evidence for spatial foraging segregation in sympatric albatrosses (Diomedea spp.) rearing chicks at Iles Nuageuses, Kerguelen. Mar Biol 141:1117–1129

    Article  Google Scholar 

  • 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 78:106–115

    Article  PubMed  Google Scholar 

  • Cherel Y, Hobson KA, Weimerskirch H (2005b) Using stable isotopes to study resource acquisition and allocation in procellariiform seabirds. Oecologia 145:533–540

    Article  CAS  PubMed  Google Scholar 

  • Cherel Y, Hobson KA, Guinet C, Vanpé C (2007) Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean. J Anim Ecol 76:826–836

    Article  PubMed  Google Scholar 

  • Clarke A (1989) Seabirds. In: Ackman RG (ed) Marine biogenic lipids, fats, and oils, vol II. CRC Press, Boca Raton, pp 383–398

    Google Scholar 

  • 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 23:15–30

    Article  CAS  Google Scholar 

  • Connan M, Mayzaud P, Boutoute M, Weimerskirch H, Cherel Y (2005) Lipid composition of stomach oil in a procellariiform seabird Puffinus tenuirostris: implications for food web studies. Mar Ecol Prog Ser 290:277–290

    Article  CAS  Google Scholar 

  • Connan M, Cherel Y, Mabille G, Mayzaud P (2007) Trophic relationships of white-chinned petrels from Crozet Islands: combined stomach oil and conventional dietary analyses. Mar Biol 152:95–107

    Article  CAS  Google Scholar 

  • Drazen JC, Phleger CF, Guest MA, Nichols PD (2009) Lipid composition and diet inferences in abyssal macrourids of the eastern North Pacific. Mar Ecol Prog Ser 387:1–14

    Article  CAS  Google Scholar 

  • Duhamel G, Pruvost P, Capdeville D (1997) By-catch of fish in longline catches off the Kerguelen Islands (division 58.5.1) during the 1995/96 season. CCAMLR Sci 4:175–193

    Google Scholar 

  • Folch J, Lees M, Sloane SG (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Goericke R, Fry B (1994) Variations of marine plankton δ13C with latitude, temperature, and dissolved CO2 in the world ocean. Glob Biogeochem Cycles 8:85–90

    Article  CAS  Google Scholar 

  • Gon O, Heemstra P (1990) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown

    Google Scholar 

  • Hagen W, Kattner G, Tergbrüggen A, Van Vleet ES (2001) Lipid metabolism of the Antarctic krill Euphausia superba and its ecological implications. Mar Biol 139:95–104

    Article  CAS  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: palaeontological statistics software package for education and data analysis. In: Palaeontologia electronica, vol 4, p 9

  • 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 198:273–281

    Article  Google Scholar 

  • Hunter S, Klages NTW (1989) The diet of Grey-headed albatrosses Diomedia chrysostoma at the Prince Edward Islands. South Afr J Ant Res 19:31–33

    Google Scholar 

  • Käkelä R, Käkelä A, Kahle S, Becker PH, Kelly A, Furness RW (2005) Fatty acid signatures in plasma of captive herring gulls as indicators of demersal or pelagic fish diet. Mar Ecol Prog Ser 293:191–200

    Article  Google Scholar 

  • Käkelä A, Crane J, Votier SC, Furness RW, Käkelä R (2006) Fatty acid signatures as indicators of diet in great skuas Stercorarius skua, Shetland. Mar Ecol Prog Ser 319:297–310

    Article  Google Scholar 

  • Käkelä A, Furness RW, Kelly A, Strandberg U, Waldron S, Käkelä R (2007) Fatty acid signatures and stable isotopes as dietary indicators in North Sea seabirds. Mar Ecol Prog Ser 342:291–301

    Article  Google Scholar 

  • Käkelä R, Käkelä A, Martínez-Abraín A, Sarzo B, Louzao M, Gerique C, Villuendas E, Strandberg U, Furness RW, Oro D (2010) Fatty acid signature analysis confirms foraging resources of a globally endangered Mediterranean seabird species: calibration test and application to the wild. Mar Ecol Prog Ser 398:245–258

    Article  Google Scholar 

  • Kattner G, Hagen W, Falk-Petersen S, Sargent JR, Henderson RJ (1996) Antarctic krill Thysanoessa macrura fills a major gap in marine lipogenic pathways. Mar Ecol Prog Ser 134:295–298

    Article  Google Scholar 

  • Lea M-A, Nichols PD, Wilson G (2002) Fatty acid composition of lipid-rich myctophids and mackerel icefish (Champsocephalus gunnari)—Southern Ocean food-web implications. Polar Biol 25:843–854

    Google Scholar 

  • Nel DC, Lutjeharms JRE, Pakhomov EA, Ansorge IJ, Ryan PG, Klages NTW (2001) Exploitation of mesoscale oceanographic features by grey-headed albatross Thalassarche chrysostoma in the southern Indian Ocean. Mar Ecol Prog Ser 217:15–26

    Article  Google Scholar 

  • Nel DC, Ryan PG, Crawford RJM, Cooper J, Huyser OAW (2002) Population trends of albatrosses and petrels at sub-Antarctic Marion Island. Polar Biol 25:81–89

    Google Scholar 

  • Nelson MM, Mooney BD, Nichols PD, Phleger CF (2001) Lipids of Antarctic Ocean amphipods: food chain interactions and the occurrence of novel biomarkers. Mar Chem 73:53–64

    Article  CAS  Google Scholar 

  • Newland C, Field IC, Nichols PD, Bradshaw CJA, Hindell MA (2009) Blubber fatty acid profiles indicate dietary resource partitioning between adult and juvenile southern elephant seals. Mar Ecol Prog Ser 384:303–312

    Article  CAS  Google Scholar 

  • Nichols DS, Williams D, Dunstand GA, Nichols PD, Volkman JK (1994) Fatty acid composition of Antarctic and temperate fish of commercial interest. Comp Biochem Physiol Part B 107:357–363

    Article  Google Scholar 

  • Pakhomov EA, Perissinotto R, McQuaid CD (1994) Comparative structure of the macrozooplankton/micronekton communities of the Subtropical and Antarctic Polar Fronts. Mar Ecol Prog Ser 111:155–169

    Article  Google Scholar 

  • Parrish CC (1999) Determination of total lipid, lipid classes, and fatty acids in aquatic samples. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 4–20

    Google Scholar 

  • Phillips KL, Jackson GD, Nichols PD (2001) Predation on myctophids by the squid Moroteuthis ingens around Macquarie and Heard Islands: stomach contents and fatty acid analyses. Mar Ecol Prog Ser 215:179–189

    Article  CAS  Google Scholar 

  • Phillips KL, Nichols PD, Jackson GD (2002) Lipid and fatty acid composition of the mantle and digestive gland of four Southern Ocean squid species: implications for food-web studies. Antarct Sci 14:212–220

    Article  Google Scholar 

  • Phillips KL, Nichols PD, Jackson GD (2003a) Dietary variation of the squid Moroteuthis ingens at four sites in the Southern Ocean: stomach contents, lipid and fatty acid profiles. J Mar Biol Assoc UK 83:523–534

    Article  Google Scholar 

  • Phillips KL, Nichols PD, Jackson GD (2003b) Size-related dietary changes observed in the squid Moroteuthis ingens at the Falkland Islands: stomach contents and fatty-acid analyses. Polar Biol 26:474–485

    Google Scholar 

  • Phleger CF, Nichols PD, Virtue P (1998) Lipids and trophodynamics of Antarctic zooplankton. Comp Biochem Physiol Part B 120:311–323

    Article  Google Scholar 

  • Raclot T, Groscolas R, Cherel Y (1998) Fatty acid evidence for the importance of myctophid fishes in the diet of king penguins, Aptenodytes patagonicus. Mar Biol 132:523–533

    Article  Google Scholar 

  • Rodhouse PG, Prince PA, Clarke MR, Murray AWA (1990) Cephalopod prey of the Grey-headed albatross Diomedea chrysostoma. Mar Biol 104:353–362

    Article  Google Scholar 

  • Saito H, Kotani Y (2000) Lipids of four boreal species of calanoid copepods: origin of monoene fats of marine animals at higher trophic levels in the grazing food chain in the subarctic ocean ecosystem. Mar Chem 71:69–82

    Article  CAS  Google Scholar 

  • Sakamoto KQ, Takahashi A, Iwata T, Trathan PN (2009) From the eye of the albatrosses: A bird-borne camera shows an association between albatrosses and a killer whales in the Southern Ocean. PLoS One 4(10):e7322

    Article  PubMed  Google Scholar 

  • Sears J, Hatch SA, O’Brien DM (2009) Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 159:41–48

    Article  PubMed  Google Scholar 

  • Smale MJ, Watson G, Hecht T (1995) Otolith atlas of Southern African marine fishes. Ichthyological monographs, vol 1. JLB Smith Institute of Ichthyology, Grahamstown

    Google Scholar 

  • Stowasser G, McAllen R, Pierce GJ, Collins MA, Moffat CF, Priede IG, Pond DW (2009a) Trophic position of deep-sea fish—assessment through fatty acid and stable isotope analyses. Deep Sea Res I 56:812–826

    Article  CAS  Google Scholar 

  • Stowasser G, Pond DW, Collins MA (2009b) Using fatty acid analysis to elucidate the feeding habits of Southern Ocean mesopelagic fish. Mar Biol 156:2289–2302

    Article  CAS  Google Scholar 

  • Wang SW, Iverson SJ, Springer AM, Hatch SA (2009) Spatial and temporal diet segregation in northern fulmars Fulmarus glacialis breeding in Alaska: insights from fatty acid signatures. Mar Ecol Prog Ser 377:299–307

    Article  CAS  Google Scholar 

  • 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 23:1–13

    Article  CAS  Google Scholar 

  • Waugh SM, Weimerskirch H, Cherel Y, Shankar U, Prince PA, Sagar PM (1999) Exploitation of the marine environment by two sympatric albatrosses in the Pacific Southern Ocean. Mar Ecol Prog Ser 177:243–254

    Article  Google Scholar 

  • 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 Animal Ecol 67:99–109

    Article  Google Scholar 

  • Weimerskirch H, Chastel O, Ackermann L, Charuande T, Cuénot-Chaillet F, Hindermeyer X, Judas J (1994) Alternate long and short foraging trips in pelagic seabird parents. Anim Behav 47:472–476

    Article  Google Scholar 

  • Weimerskirch H, Ancel A, Calouin M, Zahariev A, Spariari J, Kersten M, Chastel O (2003) Foraging efficiency and adjustment of energy expenditure in a pelagic seabird provisioning its chick. J Animal Ecol 72:500–508

    Article  Google Scholar 

  • Williams CT, Iverson SJ, Buck CL (2008) Stable isotopes and fatty acid signatures reveal age- and stage-dependent foraging niches in tufted puffins. Mar Ecol Prog Ser 363:287–298

    Article  Google Scholar 

  • Wilson G (2004) The lipid composition of Patagonian Toothfish from the Macquarie Island region—ecology and dietary implications within a regional food web. Dissertation, University of Tasmania

  • Xavier JC, Cherel Y (2009) Cephalopod beak guide for the Southern Ocean. British Antarctic Survey, Cambridge, p 129

    Google Scholar 

  • Xavier JC, Croxall JP, Trathan PN, Wood AG (2003) Feeding strategies and diets of breeding grey-headed and wandering albatrosses at South Georgia. Mar Biol 143:221–232

    Article  Google Scholar 

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Acknowledgments

We thank the officers and crew of the S.A. Agulhas for transport to the field site, L. Joassard for processing the stable isotope samples, and M. Connan for comments on an early draft. Funding was provided by the Department of Environmental Affairs and Tourism through the South African National Antarctic Program and administered by the National Research Foundation. Additional funds and facilities from Rhodes University are appreciated. This work is based upon research supported by the South African Research Chairs Initiative of the Department of Science and Technology and National Research Foundation. This field study complied with the current laws of South Africa.

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Authors and Affiliations

  1. Department of Zoology and Entomology, Rhodes University, Grahamstown, 6140, South Africa

    Nicole B. Richoux & Christopher D. McQuaid

  2. Laboratoire d’Ecologie Marine, Université de la Réunion, 15 avenue René Cassin, BP 7151, 97715, Saint Denis, Ile de la Réunion, France

    Sébastien Jaquemet

  3. Information Technology Division, Rhodes University, Grahamstown, 6140, South Africa

    Bo T. Bonnevie

  4. Centre d’Etudes Biologiques de Chizé, UPR 1934 du CNRS, BP 14, 79360, Villiers-en-Bois, France

    Yves Cherel

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  1. Nicole B. Richoux
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Correspondence to Nicole B. Richoux.

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Communicated by S. Garthe.

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Richoux, N.B., Jaquemet, S., Bonnevie, B.T. et al. Trophic ecology of Grey-headed albatrosses from Marion Island, Southern Ocean: insights from stomach contents and diet tracers. Mar Biol 157, 1755–1766 (2010). https://doi.org/10.1007/s00227-010-1448-y

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