Marine Biology

, 163:18 | Cite as

Intra-annual variation in the foraging ecology of the endangered endemic Barau’s Petrel (Pterodroma baraui) from Réunion Island, south-western Indian Ocean: insights from a multifaceted approach

  • D. K. Danckwerts
  • C. D. McQuaid
  • M. Connan
  • M. J. Smale
  • M. Le Corre
  • L. Humeau
  • S. Kaehler
  • C. C. Juhasz
  • S. Orlowski
  • J. Tourmetz
  • S. Jaquemet
Original paper


Population modelling for one of Réunion Island’s endemic seabirds, the Barau’s Petrel (Pterodroma baraui), has highlighted its vulnerability to extinction. Conservation action demands information on its biology during different stages of its life cycle. Whilst most aspects of the species’ terrestrial ecology have been studied, at-sea information is scarce and frequently contradictory. In this context, we combine three complementary techniques to provide new information on the trophic ecology of the Barau’s Petrel and to augment recent telemetry data. Colonies were visited periodically through a single breeding season and samples gathered from adults, downy chicks, and fledglings, permitting intra-annual comparisons within and among ontogenetic stages. Stomach contents consisted mostly of accumulated cephalopod beaks, whereas structures from other molluscs, fishes, and arthropods were rare. Variations in carbon stable isotopes matched the patterns of adult foraging behaviour, as described using telemetry, and wide variation in nitrogen isotope values indicated dietary opportunism. Finally, the total fatty acid composition of blood differed greatly among adults, further suggesting opportunistic feeding; however, consistently low incidences of long-chain monounsaturated and n-3 fatty acids indicated little importance of fish. These results offer additional insight into the Barau’s Petrels’ trophic ecology are in concordance with recent telemetry data and will assist in preliminary assessment of the threats to the species whilst foraging. We also illustrate the value of an integrated approach to diet determination for endangered species, where hyper-ethical approaches need to be considered, and when isotope and fatty acid baseline data are not available and are not logistically attainable.


Western Indian Ocean Breeding Stage Total Fatty Acid Composition Cephalopod Beak Cephalopod Prey 
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.



The first author would like to personally thank Pierre Laporte, Clémence Hollinger, and Olivier Tressens for their extreme patience and help with sampling and Dr. Eleonora Puccinelli for her assistance with the fatty acid extraction and analysis. We also recognise and are thankful to our editor and anonymous reviewer for comments on previous versions of the manuscript and for the support of La Société d’Etudes Ornithologiques de La Réunion, Parc National de La Réunion, and InnoVenton—The Nelson Mandela Metropolitan University, Institute of Chemical Technology, South Africa. This publication is based upon research supported by the French Embassy in South Africa, and the South African Research Chairs Initiative of the Department of Science and Technology and the National Research Foundation. All procedures performed in this study were in accordance with the ethical standards of the institutions and practices through which it was conducted (Reference Number ZOOL-01-2013).

Supplementary material

227_2015_2810_MOESM1_ESM.pdf (407 kb)
Supplementary material, containing detailed descriptions of the molecular sexing, stomach content, and FASA methodological approaches as well as the complete TFA compositions of whole blood, is available as an electronic supplement to this article. (PDF 408 kb)


  1. Allan EL, Ambrose ST, Richoux NB, Froneman PW (2010) Determining spatial changes in the diet of nearshore suspension-feeders along the South African coastline: stable isotope and fatty acid signatures. Estuar Coast Shelf Sci 87:463–471. doi: 10.1016/j.ecss.2010.02.004 CrossRefGoogle Scholar
  2. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  3. Balestrieri A, Remonti L, Prigioni C (2011) Assessing carnivore diet by faecal samples and stomach contents: a case study with Alpine red foxes. Cent Eur J Biol 6(2):283–292. doi: 10.2478/s11535-010-0106-1 Google Scholar
  4. Barrett RT, Camphuysen KCJ, Anker-Nilssen T, Chardine JW, Furness RW, Garthe S, Hüppop O et al (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691. doi: 10.1093/icesjms/fsm152 CrossRefGoogle Scholar
  5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  6. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188CrossRefGoogle Scholar
  7. Bester AJ, Priddel D, Klomp NI (2010) Diet and foraging behaviour of the Providence Petrel Pterodroma solandi. Mar Ornithol 39:163–172Google 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. Booth JM, McQuaid CD (2013) Northern rockhopper penguins prioritise future reproduction over chick provisioning. Mar Ecol Prog Ser 486:289–304. doi: 10.3354/meps10371 CrossRefGoogle Scholar
  10. Brooks TM, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Rylands AB, Konstant WR, Flick P et al (2002) Habitat loss and extinction in the hotspots of biodiversity. Conserv Biol 16(4):909–923. doi: 10.1046/j.1523-1739.2002.00530.x CrossRefGoogle Scholar
  11. Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mammal Sci 22(4):759–801. doi: 10.1111/j.1748-7692.2006.00079.x CrossRefGoogle Scholar
  12. Catry T, Ramos JA, Jaquemet S, Faulquier L, Berlincourt M, Hauselmann A, Pinet P et al (2009) Comparative foraging ecology of a tropical seabird community of the Seychelles, western Indian Ocean. Mar Ecol Prog Ser 374:259–272. doi: 10.3354/meps07713 CrossRefGoogle Scholar
  13. Cherel Y (2008) Isotopic niches of emperor and Adéilie penguins in Adéilie Land, Antarctica. Mar Biol 154:813–821. doi: 10.1007/s00227-008-0974-3 CrossRefGoogle Scholar
  14. Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005a) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888CrossRefGoogle Scholar
  15. Cherel Y, Hobson KA, Hassani S (2005b) 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
  16. Cherel Y, Hobson KA, Guinet C, Vanpe C (2007) Stable isotopes document seasonal changes in trophic niche and winter foraging individual specialization in diving predators from the Southern Ocean. J Anim Ecol 76(4):826–836CrossRefGoogle Scholar
  17. 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 366:281–291. doi: 10.3354/meps07587 CrossRefGoogle Scholar
  18. Clarke MR (1986) A handbook for the identification of cephalopod beaks. Clarendon Press, OxfordGoogle Scholar
  19. Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143. doi: 10.1111/j.1442-9993.1993.tb00438.x CrossRefGoogle Scholar
  20. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, PlymouthGoogle Scholar
  21. 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. doi: 10.3354/meps290277 CrossRefGoogle Scholar
  22. 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 497:259–272. doi: 10.3354/meps10606 CrossRefGoogle Scholar
  23. Croxall JP, Reid K, Prince PA (1999) Diet, provisioning and productivity responses of marine predators to differences in availability of Antarctic krill. Mar Ecol Prog Ser 177:115–131. doi: 10.3354/meps177115 CrossRefGoogle Scholar
  24. Croxall JP, Butchart SHM, Lascelles B, Stattersfield AJ, Sullivan B, Symes A, Taylor P (2012) Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv Int 22:1–34. doi: 10.1017/S0959270912000020 CrossRefGoogle Scholar
  25. Dalsgaard J, St John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment: a review. Adv Mar Biol 46:227–340. doi: 10.1016/S0065-2881(03)46005-7 Google Scholar
  26. De Lecea AM, Cooper R, Omarjee A, Smit AK (2011) The effects of preservation methods, dyes and acidification on the isotope values (δ15N and δ13C) of two zooplankton species from the KwaZulu-Natal Bight, South Africa. Rapid Commun Mass Spectrom 25(13):1853–1861. doi: 10.1002/rcm.5051 CrossRefGoogle Scholar
  27. Dell RK (1952) The recent Cephalopoda of New Zealand. Dom Mus Bull 16:1–157Google Scholar
  28. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506. doi: 10.1016/0016-7037(78)90199-0 CrossRefGoogle Scholar
  29. Drent R, Daan S (1980) The prudent parent: energetic adjustment in avian breeding. Ardea 68:225–252Google Scholar
  30. Dumont Y, Russell JC, Lecomte V, Le Corre M (2010) Conservation of endangered endemic seabirds within a multi-predator context: the Barau’s Petrel in Réunion Island. Nat Resour Model 23:381–436. doi: 10.1111/j.1939-7445.2010.00068.x CrossRefGoogle Scholar
  31. Faulquier L, Fontaine R, Vidal E, Salamolard M, Le Corre M (2009) Feral Cats Felis catus Threaten the Endangered Endemic Barau’s Petrel Pterodroma baraui at Reunion Island (Western Indian Ocean). Waterbirds 32:330–336. doi: 10.1675/063.032.0213 CrossRefGoogle Scholar
  32. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226(1):497–509Google Scholar
  33. Furness BL, Laugksch RC, Duffy DC (1984) Cephalopod beaks and studies of seabird diets. Auk 101:619–620Google Scholar
  34. Garcia LV (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos 105(3):657–663. doi: 10.1111/j.0030-1299.2004.13046.x CrossRefGoogle Scholar
  35. Hamer KC, Schrieber EA, Burger J (2002) 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, pp 217–262Google Scholar
  36. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9Google Scholar
  37. Harper PC (1987) Feeding behaviour and other notes on 20 species of Procellariiformes at sea. Notornis 34(3):169–192Google Scholar
  38. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94(1):181–188. doi: 10.2307/1368807 CrossRefGoogle Scholar
  39. Hobson KA, Clark RG (1993) Turnover of 13C in cellular and plasma fractions of blood: implications for non-destructive sampling in avian dietary studies. Auk 110:638–641CrossRefGoogle Scholar
  40. Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analysis of diet. Condor 95(2):388–394CrossRefGoogle Scholar
  41. Hyslop E (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17(4):411–429. doi: 10.1111/j.1095-8649.1980.tb02775.x CrossRefGoogle Scholar
  42. Imber MJ (1973) The food of Grey-faced Petrels (Pterodroma macroptera gouldi (Hutton)), with special reference to diurnal migration of their prey. J Anim Ecol 42:645–662. doi: 10.2307/3130 CrossRefGoogle Scholar
  43. Imber MJ, Jolly JN, Brooke MDL (1995) Food of three sympatric gadfly petrel (Pterodroma spp.) breeding on the Pitcairn Islands. Biol J Linn Soc 56(12):233–240. doi: 10.1111/j.1095-8312.1995.tb01087.x CrossRefGoogle Scholar
  44. Jaquemet S, Potier M, Cherel Y, Kojadinovic J, Bustamante P, Richard P, Catry T et al (2008) Comparative foraging ecology and ecological niche of a superabundant tropical seabird: the sooty tern Sterna fuscata in the southwest Indian Ocean. Mar Biol 155(5):505–520. doi: 10.1007/s00227-008-1049-1 CrossRefGoogle Scholar
  45. Jereb P, Roper CFE (2010) Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. Vol. 2. Myopsid and Oegopsid Squids. FAO Species Catalogue for Fishery Purposes. No 4, vol 2. FAO, RomeGoogle Scholar
  46. Kaiser A (1993) A new multi-category classification of subcutaneous fat deposits of songbirds. J Field Ornithol 64(2):246–255Google Scholar
  47. 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. doi: 10.3354/meps293191 CrossRefGoogle Scholar
  48. Käkelä R, Furness RW, Kahle S, Becker PH, Käkelä A (2009) Fatty acid signatures in seabird plasma are a complex function of diet composition: a captive feeding trial with herring gulls. Funct Ecol 23(1):141–149. doi: 10.1111/j.1365-2435.2008.01475.x CrossRefGoogle Scholar
  49. Kempster B, Zanette L, Longstaffe FJ, Macdougall-Shackleton SA, Wingfield JC, Clinchy M (2007) Do stable isotopes reflect nutritional stress? Results from a laboratory experiment on song sparrows. Oecologia 151:365–371CrossRefGoogle Scholar
  50. Kojadinovic J, Le Corre M, Cosson RP, Bustamante P (2007) Trace elements in three marine birds breeding on Réunion island (western Indian Ocean): Part 1—factors influencing their bioaccumulation. Arch Environ Con Tox 52(3):418–430CrossRefGoogle Scholar
  51. Kojadinovic J, Ménard F, Bustamante P, Casson RP, Le Corre M (2008) Trophic ecology of marine birds and pelagic fishes from Réunion Island, as determined by stable isotope analysis. Mar Ecol Prog Ser 361:239–251. doi: 10.3354/meps07355 CrossRefGoogle Scholar
  52. Lavers JL, Bond AL, Hutton I (2014) Plastic ingestion by Flesh-footed Shearwaters (Puffinus carneipes): implications for fledgling body condition and the accumulation of plastic-derived chemicals. Environ Pollut 187:124–129. doi: 10.1016/j.envpol.2013.12.020 CrossRefGoogle Scholar
  53. Le Corre M (2008) Conservation biology: cats, rats and seabirds. Nature 451:134–135. doi: 10.1038/451134a CrossRefGoogle Scholar
  54. Le Corre M, Ollivier A, Ribes S, Jouventin P (2002) Light-induced mortality of petrels: a 4-year study from Réunion Island (Indian Ocean). Biol Cons 105(1):93–102. doi: 10.1016/S0006-3207(01)00207-5 CrossRefGoogle Scholar
  55. Le Corre M, Ghestemme T, Salamolard M, Couzi FX (2003) Rescue of the Mascarene Petrel, a critically endangered seabird of Réunion Island, Indian Ocean. Condor 105(2):387–391. doi: 10.1650/0010-5422(2003)105[0387:ROTMPA]2.0.CO;2 CrossRefGoogle Scholar
  56. Lewis RW (1969) Studies on the stomach oil of marine birds. II. Oils of some procellariiform birds. Comp Biochem Physiol 31:725–731CrossRefGoogle Scholar
  57. Lewison R, Oro D, Godley BJ, Underhill L, Bearhop L, Wilson RP, Ainley D et al (2012) Research priorities for seabirds: improving conservation and management in the 21st century. Endanger Species Res 17:93–121. doi: 10.3354/esr00419 CrossRefGoogle Scholar
  58. Lipinski MR, Jackson S (1989) Surface-feeding on cephalopods by procellariiform seabirds in the southern Benguela region, South Africa. J Zool 218(4):549–563. doi: 10.1111/j.1469-7998.1989.tb04998.x CrossRefGoogle Scholar
  59. Mallory ML, Forbes MR, Ankney CD, Alisauskas RT (2008) Nutrient dynamics and constrains on the pre-laying exodus of High Arctic Northern Fulmars. J Aquat Biol 4:211–223. doi: 10.3354/ab00113 CrossRefGoogle Scholar
  60. McGuill MW, Rowan AN (1989) Biological effects of blood loss: implications for sampling volumes and techniques. ILAR News 31(4):5–20. doi: 10.1093/ilar.31.4.5 CrossRefGoogle Scholar
  61. Ménard F, Benivary HD, Bodin N, Coffineau N, Le Loc’h F, Mison T, Richard P et al (2014) Stable isotope patterns in micronekton from the Mozambique Channel. Deep-Sea Res II 100:153–163. doi: 10.1016/j.dsr2.2013.10.023 CrossRefGoogle Scholar
  62. Michalik A, McGill RAR, Furness RW, Eggers T, van Noordwijk HJ, Quillfeldt P (2010) Black and white- does melanin change the bulk carbon and nitrogen isotope values of feathers? Rapid Commun Mass Spectrom 24:875–878. doi: 10.1002/rcm.4462 CrossRefGoogle Scholar
  63. Mrosovsky N, Sherry DF (1980) Animal anorexias. Science 207(4433):837–842CrossRefGoogle Scholar
  64. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation. Nature 403:853–858. doi: 10.1038/35002501 CrossRefGoogle Scholar
  65. Nichols DS, Williams D, Dunstan GA, Nichols PD, Volkman JK (1994) Fatty acid composition of Antarctic and temperate fish of commercial interest. Comp Biochem Phys B 107:357–363. doi: 10.1016/0305-0491(94)90059-0 CrossRefGoogle Scholar
  66. Nur N (1986) Is clutch size variation in the blue tit (Parus caeruleus) adaptive? An experimental study. J Anim Ecol 55:983–999CrossRefGoogle Scholar
  67. Nyeland J, Fox AD, Kahlert J, Therkildsen OR (2003) Field methods to assess pectoral muscle mass in moulting geese. Wildl Biol 9:155–159Google Scholar
  68. 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(3):212–220. doi: 10.1017/S0954102002000044 CrossRefGoogle Scholar
  69. Pinet P, Salamolard M, Probst JM, Russell JC, Jaquemet S, Le Corre M (2009) Barau’s Petrel Pterodroma baraui: history, biology and conservation of an endangered endemic petrel. Mar Ornithol 37:107–113Google Scholar
  70. Pinet P, Jaeger A, Cordier E, Potin G, Le Corre M (2011a) Celestial moderation of tropical seabird behaviour. PLoS One 6(11):e27663. doi: 10.1371/journal.pone.0027663 CrossRefGoogle Scholar
  71. Pinet P, Jaquemet S, Pinaud D, Weimerskirch H, Phillips RA, Le Corre M (2011b) Migration, wintering distribution and habitat use of an endangered tropical seabird, Barau’s Petrel (Pterodroma baraui). Mar Ecol Prog Ser 423:291–302. doi: 10.3354/meps08971 CrossRefGoogle Scholar
  72. Pinet P, Jaquemet S, Phillips RA, Le Corre M (2012) Sex-specific foraging strategies throughout the breeding season in a tropical sexually monomorphic small petrel. Anim Behav 83(4):979–989. doi: 10.1016/j.anbehav.2012.01.019 CrossRefGoogle Scholar
  73. Post DM (2002) Using stable isotope to estimate trophic position: models, methods and assumptions. Ecology 83(3):703–718CrossRefGoogle Scholar
  74. Potier M, Marsac F, Cherel Y, Lucas V, Sabatié R, Maury O, Ménard F (2007) Forage fauna in the diet of three large pelagic fishes (lancetfish, swordfish and yellowfin tuna) in the western equatorial Indian Ocean. Fish Res 83:60–72. doi: 10.1016/j.fishres.2006.08.020 CrossRefGoogle Scholar
  75. 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. doi: 10.1007/s002270050418 CrossRefGoogle Scholar
  76. Richoux N, 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 157:1755–1766. doi: 10.1007/s00227-010-1448-y CrossRefGoogle Scholar
  77. Riethmuller M, Jan F, Giloux Y (2011) Plan National d’Actions Pétrel noir de Bourbon, Pseudobulweria atterima. SEOR/Parc National de La Réunion/DIREN RéunionGoogle Scholar
  78. Russell JC, Le Corre M (2009) Introduced mammal impacts on seabirds in the Îles Éparses, Western Indian Ocean. Mar Ornithol 37:121–129Google Scholar
  79. Salamolard M (2007) Plan de conservation du Pétrel de Barau (Pterodroma baraui). Rapport ECOMAR. Réunion University and Société d’Etudes Ornithologiques de la Réunion, RéunionGoogle Scholar
  80. Schramm M (1986) The diet of chicks of Great-winged, Kerguelen and Soft-plumaged Petrels at the Prince Edward Islands. Ostrich 57(1):9–15. doi: 10.1080/00306525.1986.9633632 CrossRefGoogle Scholar
  81. Schreiber EA, Burger J (2002) Seabirds in the marine environment. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, pp 1–15Google Scholar
  82. Sears J, Hatch SA, O’Brien DM (2009) Disentangling effects of growth and nutritional stress on seabird stable isotope ratios. Oecologia 159(1):41–48. doi: 10.1007/s00442-008-1199-3 CrossRefGoogle Scholar
  83. Shirihai H, Pym T, Román MS, Bretagnolle V (2014) The critically endangered Mascarene Petrel Pseudobulweria aterrima: identification and behaviour at sea, historical discovery of breeding sites, and breeding ecology on Réunion, Indian Ocean. Bull Br Orn Club 134(3):194–233Google Scholar
  84. Spear LB, Ainley DG, Walker WA (2007) Foraging dynamics of seabirds in the Eastern Tropical Pacific Ocean. Studies in Avian Biology Series 35: Cooper Ornithological Society, NormanGoogle Scholar
  85. Stahl JC, Bartle JA (1991) Distribution, abundance and aspects of the pelagic ecology of Barau’s Petrel Pterodroma baraui in the south-west Indian Ocean. Notornis 38(3):211–225Google Scholar
  86. Thompson DR, Phillips RA, Stewart FM, Waldron S (2000) Low d13C 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
  87. Tierney M, Nichols PD, Wheatley KE, Hindell MA (2008) Food fatty acids indicate inter- and intra-annual variation in the diet of Adélie Penguins: comparison with stomach content and stable isotope analysis. J Exp Mar Biol Ecol 367:65–74CrossRefGoogle Scholar
  88. Totzke U, Fenske M, Hűppop O, Raabe H, Schach N (1999) The influence of fasting on blood and plasma composition of herring gulls (Larus argentatus). Physiol and Biochem Zool 72(4):426–437CrossRefGoogle Scholar
  89. Uspenski VS (1956) The bird bazaars of Novaya Zemlya. Moscow, U.S.S.R. Acad. Sci. 4th Vol. CWS transl. of Russ. Game ReportsGoogle Scholar
  90. Warham J (1977) The incidence, functions and ecological significance of Petrel stomach oils. Proc New Zeal Ecol Soc 24:84–93Google Scholar
  91. Warham J (1990) The Petrels—their ecology and breeding systems. Academic Press, LondonGoogle Scholar
  92. Warham J, Watts R, Dainty RJ (1976) The composition, energy content and function of the oils of petrel (order, Procellariiformes). J Exp Mar Biol Ecol 23(1):1–13. doi: 10.1016/0022-0981(76)90081-2 CrossRefGoogle Scholar
  93. Weimerskirch H (2002) Seabird demography and its relationship with the marine environment. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, pp 115–136Google Scholar
  94. Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography ecology, evolution and conservation, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  95. Xavier JC, Cherel Y (2009) Cephalopod beak guide for the southern ocean. British Antarctic Survey, CambridgeGoogle Scholar
  96. Young RE, Yeccione M, Mangold KM (2012) Cephalopoda, Cuvier 1797. Octopods, squids, nautiluses, etc. Tree of Life Web project: Accessed 5 Aug 2014

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • D. K. Danckwerts
    • 1
    • 2
  • C. D. McQuaid
    • 1
  • M. Connan
    • 3
  • M. J. Smale
    • 3
    • 4
  • M. Le Corre
    • 2
  • L. Humeau
    • 5
  • S. Kaehler
    • 6
  • C. C. Juhasz
    • 2
  • S. Orlowski
    • 2
  • J. Tourmetz
    • 7
  • S. Jaquemet
    • 2
  1. 1.Coastal Research Group, Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa
  2. 2.UMR ENTROPIE (Université de La Réunion, IRD, CNRS)St Denis Cedex 9, Ile De La RéunionFrance
  3. 3.Zoology DepartmentNelson Mandela Metropolitan UniversityPort ElizabethSouth Africa
  4. 4.Port Elizabeth MuseumHumewoodSouth Africa
  5. 5.UMR C533 PVBMT (Université de La Réunion, IRD, CNRS)St Denis Cedex 9, Ile De La RéunionFrance
  6. 6.IsoEnvironmental cc, Department of BotanyRhodes UniversityGrahamstownSouth Africa
  7. 7.La Société d’Etudes Ornithologiques de La Réunion (SEOR)Saint André, Ile De La RéunionFrance

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