Abstract
Southern rockhopper penguins (Eudyptes chrysocome chrysocome) have experienced severe population declines across their distribution area, potentially in response to bottom-up effects following elevated sea surface temperatures, changes in the food web and prey availability. We conducted stable isotope analysis to compare trophic levels and distribution patterns in the non-breeding period over three consecutive years, and between males and females, using egg membranes, blood cells and feathers of parent birds. Tissues representing the non-breeding season had lower δ13C values than prey sampled around the Falklands and red blood cells from breeding rockhopper penguins. In contrast, δ15N values were higher in red blood cells from the end of winter compared to those from the breeding season and compared to feathers. This indicated that rockhopper penguins left the Falkland Island area in the non-breeding season and foraged either around Burdwood Bank further south, or over the Patagonian Shelf. In winter, only males took more prey of higher trophic level than females. Inter-annual differences in isotopic values partly correlated with sea surface temperatures. However, as prey isotope samples were collected only in 1 year, inter-annual differences in penguin isotopic values may result from different foraging sites, different prey choice or different isotopic baseline values. Our study highlights the potential for stable isotope analyses to detect seasonal and gender-specific differences in foraging areas and trophic levels, while stressing the need for more sampling of isotopic baseline data.
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References
Beardall J, Stojkovic S, Larsen S (2009) Living in a high CO2 world: impacts of global climate change on marine phytoplankton. Plant Ecol Divers 2:191–205
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 75:451–458
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 311:157–164
Beaulieu M, Spee M, Lazin D, Ropert-Coudert Y, Le Maho Y, Ancel A, Raclot T (2010) Ecophysiological response of Adélie penguins facing an experimental increase in breeding constraints. J Exp Biol 213:33–39
Behrenfeld MJ, O’Malley RT, Siegel DA, McClain CR, Sarmiento JL, Feldman GC, Milligan AJ, Falkowski PG, Letelier RM, Boss ES (2006) Climate-driven trends in contemporary ocean productivity. Nature 444:752–755
Birdlife International (2010) Rockhopper penguins. A plan for research and conservation to investigate and address population changes. In: Proceedings of an international workshop, Edinburgh, 3–5 June 2008
Boersma PD, Stokes DL, Strange IJ (2002) Applying ecology to conservation: tracking breeding penguins at New Island South Reserve, Falkland Islands. Aquatic Conserv Mar Freshw Ecosyst 12:63–74
Bost CA, Thiebot JB, Pinaud D, Cherel Y, Trathan PN (2009) Where do penguins go during the inter-breeding period? Using geolocation to track the winter dispersion of the macaroni penguin. Biol Lett 5:473–476
Carleton S, de Rio C (2005) The effect of cold-induced increased metabolic rate on the rate of 13C and 15 N incorporation in house sparrows (Passer domesticus). Oecologia 144:226–232
Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Delta N-15 and Delta C-13): the effect of diet isotopic values and applications for diet reconstruction. J Applied Ecol 46:443–453
Cherel Y, Hobson KA, Bailleul FR, Groscolas R (2005a) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888
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 78:106–115
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
Cherel Y, Hobson KA, Guinet C, Vanpe 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
Ciancio JE, Pascual MA, Botto F, Frere E, Iribarne O (2008) Trophic relationships of exotic anadromous salmonids in the southern Patagonian Shelf as inferred from stable isotopes. Limn Oceanogr 53:788–798
Clarke A, Murphy EJ, Meredith MP, King JC, Peck LS, Barnes DKA, Smith RC (2007) Climate change and the marine ecosystem of the western Antarctic Peninsula. Phil Trans R Soc B 362:149–166
Cooper J, Brown CR, Gales RP, Hindell MA, Klages NTW, Moors PJ, Pemberton D, Ridoux KR, Thompson KR, Van Heezik YM (1990) Diets and dietary segreation of crested penguins (Eudyptes). In: Davies LS, Darby JT (eds) Penguin Biology. Academic Press, San Diego, pp 131–156
Croxall JP, Prince PA, Baird A, Ward P (1985) The diet of the southern rockhopper penguin Eudyptes chrysocome chrysocome at Beauchene Island, Falkland-Islands. J Zool 206:485–496
Cunningham DM, Moors PJ (1994) The decline of Rockhopper penguins Eudyptes chrysocome at Campbell Island, Southern Ocean and the influence of rising sea temperatures. Emu 94:27–36
Davis LS, Renner M (2003) Penguins. Yale University Press, New Haven and London
Forero MG, Hobson KA, Bortolotti GR, Donazar JA, Bertellotti M, Blanco G (2002) Food resource utilisation by the Magellanic penguin evaluated through stable-isotope analysis: segregation by sex and age and influence on offspring quality. Mar Ecol Prog Ser 234:289–299
Gladbach A, McGill RAR, Quillfeldt P (2007) Foraging areas of Wilson’s storm-petrel Oceanites oceanicus in the breeding and inter-breeding period determined by stable isotope analysis. Polar Biol 30:1005–1012
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 12:611–625
Hirons AC, Schell DM, Finney BP (2001) Temporal records of delta C-13 and delta N-15 in North Pacific pinnipeds: inferences regarding environmental change and diet. Oecologia 129:591–601
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326
Hobson KA (2007) An isotopoic exploration of the potential of avian tissues to track changes in terrestrial and marine ecosystems. In: Dawson TE, Siegwolf TW (eds) Stable isotopes as indicators of ecological change, 1st edn. Elsevier Academic Press, London, pp 129–144
Hobson KA (2008) Isotopic tracking of migrant wildlife. In: Michener RH, Lajtha K (eds) Stable isotopes in ecology and environmental science. Blackwell Publishing Ltd., Oxford, pp 155–175
Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I. Turnover of 13C in tissues. Condor 94:181–188
Huin N (2003) Falkland Island Seabird Monitoring Programme Annual Report 2002/03. Falklands Conservation
Iglesias-Rodriguez MD, Halloran PR, Rickaby REM, Hall IR, Colmenero-Hidalgo E, Gittins JR, Green DRH, Tyrrell T, Gibbs SJ, von Dassow P, Rehm E, Armbrust EV, Boessenkool KP (2008) Phytoplankton calcification in a high-CO2 world. Sci 320:336–340
Jaeger A, Cherel Y (2011) Isotopic investigation of contemporary and historic changes in penguin trophic niches and carrying capacity of the Southern Indian Ocean. PLoS ONE 6:e16484
Jennings S, Pinnegar JK, Polunin NVC, Boon TW (2001) Weak cross-species relationships between body size and trophic level belie powerful size-based trophic structuring in fish communities. J Anim Ecol 70:934–944
Jenouvrier S, Barbraud C, Weimerskirch H (2005) Long-term contrasted responses to climate of two Antarctic seabird species. Ecology 86:2889–2903
Kato A, Watanuki Y, Nishiumi I, Kuroki M, Shaughnessy P, Naito Y (2000) Variation in foraging and parental behavior of king cormorants. Auk 117:718–730
Keymer IF, Malcolm HM, Hunt A, Horsley DT (2001) Health evaluation of penguins (Sphenisciformes) following mortality in the Falklands (South Atlantic). Dis Aquat Org 45:159–169
Knox GA (2006) Biology of the Southern Ocean. CRC Press Taylor & Francis Group, Boca Raton
Lyster S (1986) Penguin mortality in the Falklands. Oryx 20:206–207
Masello JF, Mundry R, Poisbleau M, Demongin L, Voigt CC, Wikelski M, Quillfeldt P (2010) Diving seabirds share foraging space within and among species. Ecosphere 1:19
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 24:851–1112
Minagawa M, Wada E (1984) Stepwise enrichment of 15 N along food chains: further evidence and the relation between d 15 N and animal age. Geochim Cosmochim Acta 48:1135–1140
Ogden LJE, Hobson KA, Lank DB (2004) Blood isotopic (delta C-13 and delta N-15) turnover and diet- tissue fractionation factors in captive Dunlin (Calidris alpina pacifica). Auk 121:170–177
Oppel S, Powell AN, O’Brien DM (2009) Using eggshell membranes as a non-invasive tool to investigate the source of nutrients in avian eggs. J Ornithol 150:109–115
Owens N (1987) Natural variations in 15 N in the marine environment. Adv Mar Biol 24:389–451
Peterson RG, Whitworth T (1989) The sub-antarctic and polar fronts in relation to deep-water masses through the southwestern Atlantic. J Geophys Res Ocean 94:817–838
Poisbleau M, Demongin L, Strange IJ, Otley H, Quillfeldt P (2008) Aspects of the breeding biology of the southern rockhopper penguin Eudyptes c. chrysocome and new consideration on the intrinsic capacity of the A-egg. Polar Biol 31:925–932
Poisbleau M, Demongin L, Angelier F, Dano S, Lacroix A, Quillfeldt P (2009) What ecological factors can affect albumen corticosterone levels in the clutches of seabirds? Timing of breeding, disturbance and laying order in rockhopper penguins (Eudyptes chrysocome chrysocome). Gen Comp Endocrinol 162:139–145
Poisbleau M, Demongin L, van Noordwijk HJ, Strange IJ, Quillfeldt P (2010) Sexual dimorphism and use of morphological measurements to sex adults, immatures and chicks of rockhopper penguins. Ardea 98:217–227
Pütz K, Ingham RJ, Smith JG, Lüthi BH (2002) Winter dispersal of rockhopper penguins Eudyptes chrysocome from the Falkland Islands and its implications for conservation. Mar Ecol Prog Ser 240:273–284
Pütz K, Clausen AP, Huin N, Croxall JP (2003a) Re-evaluation of historical rockhopper penguin population data in the Falkland Islands. Waterbirds 26:169–175
Pütz K, Smith JG, Ingham RJ, Lüthi BH (2003b) Satellite tracking of male rockhopper penguins Eudyptes chrysocome during the incubation period at the Falkland Islands. J Avian Biol 34:139–144
Pütz K, Rey AR, Huin N, Schiavini A, Pütz A, Luthi BH (2006a) Diving characteristics of southern rockhopper penguins (Eudyptes c. chrysocome) in the Southwest Atlantic. Mar Biol 149:125–137
Pütz K, Rey AR, Schiavini A, Clausen AP, Lüthi BH (2006b) Winter migration of rockhopper penguins (Eudyptes c. chrysocome) breeding in the Southwest Atlantic: is utilisation of different foraging areas reflected in opposing population trends? Polar Biol 29:735–744
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 295:295–304
Quillfeldt P, Strange IJ, Masello JF (2007) Sea surface temperatures and behavioural buffering capacity in thin-billed prions Pachyptila belcheri: breeding success, provisioning and chick begging. J Avian Biol 38:298–308
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 155:593–598
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 373:137–148
Quillfeldt P, McGill RAR, Masello JF, Poisbleau M, van Noordwijk H, Demongin L, Furness RW (2009) Differences in the stable isotope signatures of seabird egg membrane and albumen—implications for non-invasive studies. Rapid Commun Mass Spectrom 23:3632–3636
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
Raya Rey A, Schiavini A (2005) Inter-annual variation in the diet of female southern rockhopper penguin (Eudyptes chrysocome chrysocome) at Tierra del Fuego. Polar Biol 28:132–141
Raya Rey A, Trathan P, Pütz K, Schiavini A (2007a) Effect of oceanographic conditions on the winter movements of rockhopper penguins Eudyptes chrysocome chrysocome from Staten Island, Argentina. Mar Ecol Prog Ser 330:285–295
Raya Rey A, Trathan P, Schiavini A (2007b) Inter-annual variation in provisioning behaviour of southern rockhopper penguins Eudyptes chrysocome chrysocome at Staten Island, Argentina. Ibis 149:826–835
Riebesell U, Zondervan I, Rost B, Tortell PD, Zeebe RE, Morel FMM (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407:364–367
Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends in Ecol Evol 19:256–263
Schell DM (2000) Declining carrying capacity in the Bering Sea: isotopic evidence from whale baleen. Limnol Oceanogr 45:459–462
Schreer JF, Kovacs KM (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75:339–358
Strange IJ (1982) Breeding ecology of the Rockhopper penguin (Eudyptes crestatus) in the Falkland Islands. Gerfaut 72:137–188
Thompson KR (1989) An assessment of the potential for competition between seabirds and fisheries in the Falkland Islands. Falkland Islands Foundation Project Reports
Thompson KR (1994) Predation on Gonatus antarcticus by Falkland Islands seabirds. Antarct Sci 6:269–274
Tierney M, Southwell C, Emmerson LM, Hindell MA (2008) Evaluating and using stable-isotope analysis to infer diet composition and foraging ecology of Adélie penguins Pygoscelis adeliae. Mar Ecol Prog Ser 355:297–307
Weimerskirch H, Inchausti P, Guinet C, Barbraud C (2003) Trends in bird and seal populations as indicators of a system shift in the Southern Ocean. Antarct Sci 15:249–256
Weiss F, Furness RW, McGill RAR, Strange IJ, Masello JF, Quillfeldt P (2009) Trophic segregation of Falkland Islands seabirds: insights from stable isotope analysis. Polar Biol 32:1753–1763
White RW, Reid JB, Black AD, Gillon KW (1999) Seabird and marine mammal dispersion in the waters around the Falkland Islands 1998–1999. Joint Nature Conservation Committee, Peterborough, UK
White RW, Gillon KW, Black AD, Reid JB (2001) Vulnerable concentrations of seabirds in Falkland Islands waters. Joint Nature Conservation Committee, Peterborough, UK
Williams TD (1995) The penguins. Oxford University Press, Oxford
Wilson RP (1995) Foraging ecology. In: Williams TD (ed) The penguins. Oxford University Press, Oxford, pp 81–106
Wilson RP, Culik B, Spairani HJ, Coria NR, Adelung D (1991) Depth utilization by penguins and gentoo penguin dive patterns. J Ornithol 132:47–60
Acknowledgments
We are grateful to the New Island Conservation Trust for permission to work on the island. We thank Ian, Maria and Georgina Strange, and Dan Birch for their support during the field season. Thanks also to Helen Otley, Falkland Islands Government and British Antarctic Survey for their logistic help. Prey samples were provided by Dr. Paul Brickle, Falkland Islands Government Fisheries Department, fat extracted by Felix Weiss and analysed at SURC, UK, by Dr. Rona McGill, as part of a previous project. We thank Karin Sörgel and Anja Luckner from the IZW for isotope analysis of penguin samples. Dr. Katrin Ludynia helped to create a map of the study area. We would like to thank three anonymous reviewers for helpful comments on this manuscript. Our study was funded by a grant provided by the Deutsche Forschungsgemeinschaft DFG (Qu 148/1-ff) and an Environmental Studies Budget grant from the Falkland Islands Government. All work was approved by the Falkland Islands Government (Environmental Planning Office).
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Dehnhard, N., Voigt, C.C., Poisbleau, M. et al. Stable isotopes in southern rockhopper penguins: foraging areas and sexual differences in the non-breeding period. Polar Biol 34, 1763–1773 (2011). https://doi.org/10.1007/s00300-011-1026-x
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DOI: https://doi.org/10.1007/s00300-011-1026-x