Skip to main content
Log in

Seasonal prey switching in non-breeding gentoo penguins related to a wintertime environmental anomaly around South Georgia

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Information is needed on how anomalous environmental conditions affect important Antarctic ecological sentinels during the winter. Using a non-invasive method (scats), the diet of non-breeding gentoo penguins Pygoscelis papua at Bird Island, South Georgia, was examined during the winter of 2009 when local environmental conditions were abnormal (e.g. warmer sea surface waters). Scats were collected every 2 weeks from May until October 2009 (N = 168); the diet was dominated by the amphipod Themisto gaudichaudii by frequency of occurrence (77.5% of the samples) and by number (70.5% of the total individuals). By mass, different species of crustaceans (T. gaudichaudii and Antarctic krill Euphausia superba) and fish (Champsocephalus gunnari, Lepidonotothen larseni and Pseudochaenichthys georgianus) were the most important in different periods. Numerically, prey switching occurred at the end of winter, when E. superba became more abundant in the penguins’ diets in late September and early October (austral spring), when sea surface temperatures became colder. T. gaudichaudii is sub-optimal prey for gentoo penguins and its consumption most likely reflects a lack of E. superba in local waters. The consumption of T. gaudichaudii and fish, in place of E. superba, was probably insufficient for the penguins to maintain a body condition suitable for reproduction, contributing to the observed late commencement of breeding (i.e. 2–3 weeks) that year. Our results highlight the sensitivity of gentoo penguin populations to variations in environmental conditions, particularly in terms of how these conditions affect the availability of preferred dietary items and potential follow-on effects in the subsequent breeding season.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adams NJ, Klages NT (1987) Seasonal variation in the diet of king penguin Aptenodytes patagonicus at Sub-Antarctic Marion Island. J Zool 212:303–324

    Article  Google Scholar 

  • Atkinson A, Ward P, Hunt BPV, Pakhomov EA, Hosie GW (2012) An overview of Southern Ocean zooplankton data: abundance, biomass, feeding and functional relationships. CCAMLR Sci 19:171–218

    Google Scholar 

  • Barrett RT et al (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691. https://doi.org/10.1093/icesjms/fsm152

    Article  Google Scholar 

  • BirdLife_International (2016) Pygoscelis papua. The IUCN Red List of Threatened Species 2016: eT22697755A93637402:

  • Bocher P, Cherel Y, JP L, Mayzaud P, Razouls S, Jouventin P (2001) Amphipod-based food web: Themisto gaudichaudii caught in nets and by seabirds in Kerguelen waters, southern Indian Ocean. Mar Ecol Prog Ser 223:261–276

    Article  Google Scholar 

  • Boltovskoy D (1999) South Atlantic zooplankton. Backhuys Publishers, Leiden

    Google Scholar 

  • Bost CA, Koubbi P, Genevois F, Ruchon L, Ridoux V (1994) Gentoo penguin Pygoscelis papua diet as an indicator of planktonic availability in the Kerguelen Islands. Polar Biol 14:147–153

    Article  Google Scholar 

  • Bowen W, Iverson S (2013) Methods of estimating marine mammal diets: a review of validation experiments and sources of bias and uncertainty. Mar Mammal Sci 29:719–754

    Google Scholar 

  • CCAMLR (2014) CCAMLR Ecosystem Monitoring Program (CEMP) Standard Methods. CCAMLR, Hobart. https://www.ccamlr.org/en/document/science/cemp-standard-methods

  • Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package-I-One-table methods. R News 4:5–10

    Google Scholar 

  • Cimino MA, Moline MA, Fraser WR, Patterson-Fraser DL, Oliver MJ (2016) Climate-driven sympatry may not lead to foraging competition between congeneric top-predators. Sci Rep 6:18820

    Article  CAS  PubMed Central  Google Scholar 

  • Clarke MR (1996) Cephalopods as prey.III.Cetaceans. Phil Trans R Soc Lond B 351:1053–1065

    Article  Google Scholar 

  • Clausen AP, Pütz K (2003) Winter diet and foraging range of gentoo penguins (Pygoscelis papua) from Kidney Cove, Falkland Islands. Polar Biol 26:32–40

    Google Scholar 

  • Constable AJ et al (2014) Change in Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biota. Glob Chang Biol 20:3004–3025

    Article  Google Scholar 

  • Croxall JP, Prince PA (1980) The food of gentoo penguins Pygoscelis papua and macaroni penguins Eudyptes chrysolophus at South Georgia. Ibis 122:245–253

    Article  Google Scholar 

  • Croxall JP, Davis RW, Oconnell MJ (1988) Diving patterns in relation to diet of gentoo and macaroni penguins at South Georgia. Condor 90:157–167

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • De Broyer C, Lowry JK, Jazdzewski K, Robert H (2007) Catalogue of the Gammaridean and Corophiidean Amphipoda (Crustacea) of the Southern Ocean, with distribution and ecological data. In: C. DB (ed) Census of Antarctic Marine Life: Synopsis of the Amphipoda of the Southern Ocean. Vol. I., vol 77. Bulletin de l’Institut royal des Sciences naturelles de Belgique, Biologie, pp 1–325

  • Everson I (2000) Krill: biology, ecology and fisheries. Blackwell Science Ltd, Oxford

    Book  Google Scholar 

  • Fielding S et al (2014) Interannual variability in Antarctic krill (Euphausia superba) density at South Georgia, Southern Ocean: 1997–2013. ICES J Mar Sci 71:2578–2588

    Article  Google Scholar 

  • Forcada J, Trathan PN (2009) Penguin responses to climate change in the Southern Ocean. Glob Chang Biol 15:1618–1630

    Article  Google Scholar 

  • Forcada J, Trathan PN, Reid K, Murphy EJ, Croxall JP (2006) Contrasting population changes in sympatric penguin species in association with climate warming. Glob Chang Biol 12:411–423

    Article  Google Scholar 

  • Gutt J et al (2015) The Southern Ocean ecosystem under multiple climate change stresses—an integrated circumpolar assessment. Glob Chang Biol 21:1434–1453

    Article  PubMed Central  Google Scholar 

  • Hecht T (1987) A guide to the otoliths of Southern Ocean fishes. S Afr J Antarct Res 17:2–87

    Google Scholar 

  • Hill S et al. (2009) Multiple indicators suggest a strong ecosystem anomaly at South Georgia in 2009. WG-EMM-09/23:

  • Hill HJ, Trathan PN, Croxall JP, Watkins JL (1996) A comparison of Antarctic krill Euphausia superba caught by nets and taken by macaroni penguins Eudyptes chrysolophus: evidence for selection. Mar Ecol Prog Ser 140:1–11

    Article  Google Scholar 

  • Hill SL et al (2016) Is current management of the Antarctic krill fishery in the Atlantic sector of the Southern Ocean precautionary? CCAMLR Sci 23:31–51

    Google Scholar 

  • Hinke JT, Trivelpiece WZ (2011) Daily activity and minimum food requirements during winter for gentoo penguins (Pygoscelis papua) in the South Shetland Islands, Antarctica. Polar Biol 34:1579–1590

    Article  Google Scholar 

  • Irvine LG (2002) Sex differences in Antarctic krill (Euphausia superba) retrieved from Adelie penguin stomachs: implications for diet analysis. Polar Biol 25:717–720

    Google Scholar 

  • Kane JE (1966) The distribution of Parathemisto gaudichaudii (Guer.), with observations on its life-history in the 0° to 20° E sector in the Southern Ocean. Discov Rep 34:163–198

    Google Scholar 

  • Kato A, Williams TD, Barton TR, Rodwell S (1991) Short-term variation in the winter diet of gentoo penguins Pygoscelis papua at South Georgia during July 1989. Mar Ornithol 19:31–38

    Google Scholar 

  • Kindt R, Coe R (2005) Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre

  • Kirkwood JM (1982) A guide to the Euphausiacea of the Southern Ocean. ANARE Res Notes 1:1–45

    Google Scholar 

  • Kock K-H (1992) Antarctic fish and fisheries. Cambridge University Press, Cambridge

    Google Scholar 

  • Kock K-H, Jones CD (2005) Fish stocks in the southern Scotia arc region—a review and prospects for future research. Rev Fisheries Sci 13:75–108

    Article  Google Scholar 

  • Kock K-H, Wilhelms S, Everson I, Gröger J (1994) Variations in the diet composition and feeding intensity of mackerel icefish Champsocephalus gunnari at South Georgia (Antarctic). Mar Ecol Prog Ser 108:43–57

    Article  Google Scholar 

  • Kock K-H et al (2012) The role of fish as predators of krill (Euphausia superba) and other pelagic resources in the Southern Ocean. CCAMLR Sci 19:115–169

    Google Scholar 

  • Kokubun N, Takahashi A, Mori Y, Watanabe S, Shin H-C (2010) Comparison of diving behavior and foraging habitat use between Chinstrap and Gentoo Penguins breeding in the South Shetland Islands, Antarctica. Mar Biol 157:811–825

    Article  Google Scholar 

  • Labat J, Mayzaud P, Sabini S (2005) Population dynamics of Themisto gaudichaudii in Kerguelen Island waters, Southern Indian Ocean. Polar Biol 28:776–783

    Article  Google Scholar 

  • Laws RM (2009) Antarctic seals: research methods and techniques. Cambridge University Press, Cambridge

  • Lescroël A, Ridoux V, Bost CA (2004) Spatial and temporal variation in the diet of gentoo penguin (Pygoscelis papua) at Kerguelen Islands. Polar Biol 27:206–216

    Article  Google Scholar 

  • Libertelli MM, Daneri GA, Piatkowski U, Coria NR, Carlini AR (2004) Predation on cephalopods by Pygoscelis papua and Arctocephalus gazella at South Orkney Islands. Polish Polar Res 25:267–274

    Google Scholar 

  • Main CE, Collins MA, Mitchell R, Belchier M (2009) Identifying patterns in the diet of mackerel icefish (Champsocephalus gunnari) at South Georgia using bootstrapped confidence intervals of a dietary index. Polar Biol 32:569–581

    Article  Google Scholar 

  • Mori Y, Boyd IL (2004) Segregation of foraging between two sympatric penguin species: does rate maximisation make the difference? Mar Ecol Prog Ser 275:241–249

    Article  Google Scholar 

  • North AW, Murray AWA (1992) Abundance and diurnal vertical distribution of fish larvae in early spring and summer in fjord at South Georgia. Antarct Sci 4:405–412

    Article  Google Scholar 

  • Pakhomov E, Perissinotto R (1996) Trophodynamics of the hyperiid amphipod Themisto gaudichaudi in the South Georgia region during late austral summer. Mar Ecol Prog Ser 134:91–100

    Article  Google Scholar 

  • Ratcliffe N et al (2014) Love thy neighbour or opposites attract? Patterns of spatial segregation and association among crested penguin populations during winter. J Biogeogr 41:1183–1192

    Article  PubMed Central  Google Scholar 

  • Reid K (1996) A guide to the use of otoliths in the study of predators at South Georgia. British Antarctic Survey, Cambridge

    Google Scholar 

  • Reid K, Croxall JP (2001) Environmental response of upper trophic-level predators reveals a system change in an Antarctic marine ecosystem. Proc R Soc B 268:377–384

    Article  CAS  Google Scholar 

  • Reid K, Measures J (1998) Determining the sex of Antarctic krill Euphausia superba using carapace measurements. Polar Biol 19:145–147

    Article  Google Scholar 

  • Reiss CS et al (2017) Overwinter habitat selection by Antarctic krill under varying sea-ice conditions: implications for top predators and fishery management. Mar Ecol Prog Ser 568:1–16

    Article  CAS  Google Scholar 

  • Smale MJ (1996) Cephalopods as prey. IV. Fishes. Phil Trans R Soc Lond B 351:1067–1081

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Takahashi A et al (2018) Migratory movements and winter diving activity of Adélie penguins in East Antarctica. Mar Ecol Prog Ser 589:227–239

    Article  Google Scholar 

  • Tanton JL, Reid K, Croxall JP, Trathan PN (2004) Winter distribution and behaviour of gentoo penguins Pygoscelis papua at South Georgia. Polar Biol 27:299–303

    Article  Google Scholar 

  • Tarling GA (2003) Sex-dependent diel vertical migration in northern krill Meganyctiphanes norvegica and its consequences for population dynamics. Mar Ecol Prog Ser 260:173–188

    Article  Google Scholar 

  • Tarling G, Cuzin-Roudy J, Thorpe S, Shreeve R, Ward P, Murphy E (2007) Recruitment of Antarctic krill Euphausia superba in the South Georgia region: adult fecundity and the fate of larvae. Mar Ecol Prog Ser 331:161–179

    Article  Google Scholar 

  • Thiebot J-B, Lescroël A, Pinaud D, Trathan PN, Bost C-A (2011) Larger foraging range but similar habitat selection in non-breeding versus breeding sub-Antarctic penguins. Antarct Sci 23:117–126

    Article  Google Scholar 

  • Trathan P, Ratcliffe N, Masden E (2012) Ecological drivers of change at South Georgia: the krill surplus, or climate variability. Ecography 35:983–993

    Article  Google Scholar 

  • Trivelpiece WZ, Hinke JT, Miller AK, Reiss CS, Trivelpiece SG, Watters GM (2011) Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. PNAS 108:7625–7628

    Article  CAS  PubMed Central  Google Scholar 

  • Waluda CM, Hill SL, Peat HJ, Trathan PN (2017) Long-term variability in the diet and reproductive performance of penguins at Bird Island, South Georgia. Mar Biol 164:39

    Article  Google Scholar 

  • Watts J, Tarling GA (2012) Population dynamics and production of Themisto gaudichaudii (Amphipoda, Hyperiidae) at South Georgia, Antarctica. Deep-Sea Res II 59:117–129

    Article  Google Scholar 

  • Williams TD (1990) Annual variation in breeding biology of gentoo penguins (Pygoscelis papua) at Bird Island, South Georgia. J Zool 222:247–258

    Article  Google Scholar 

  • Williams TD (1991) Foraging ecology and diet of gentoo penguins Pygoscelis papua at South Georgia during winter and an assessment of their winter krill consumption. Ibis 133:3–13

    Article  Google Scholar 

  • Williams TD (1995) The penguins: Spheniscidae. Oxford University Press, Oxford

    Google Scholar 

  • Williams R, McEldowney A (1990) A guide to the fish otoliths from waters off the Australian Antarctic Territory, Heard and Macquarie Island vol 75. ANARE Research Notes

  • Williams TD, Briggs DR, Croxall JP, Naito Y, Kato A (1992) Diving pattern and performance in relation to foraging ecology in the gentoo penguin Pygoscelis papua. J Zool 227:211–230

    Article  Google Scholar 

  • Williams RL, Goodenough AE, Stafford R (2012) Statistical precision of diet diversity from scat and pellet analysis. Ecol Inf 7:30–34

    Article  Google Scholar 

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

  • Xavier JC, Rodhouse PG, Trathan PN, Wood AG (1999) A Geographical Information System (GIS) atlas of cephalopod distribution in the Southern Ocean. Antarct Sci 11:61–62

    Article  Google Scholar 

  • Xavier JC, Croxall JP, Reid K (2003) Inter-annual variation in the diet of two albatross species breeding at South Georgia: implications for breeding performance. Ibis 145:593–610

    Article  Google Scholar 

  • Xavier JC et al (2013) Seasonal changes in the diet and feeding behaviour of a top predator indicate a flexible response to deteriorating oceanographic conditions. Mar Biol 160:1597–1606

    Article  Google Scholar 

  • Xavier JC, Raymond B, Jones DC, Griffiths H (2016) Biogeography of cephalopods in the Southern Ocean using habitat suitability prediction models. Ecosystems 19:220–247

    Article  CAS  Google Scholar 

  • Xavier JC et al (2017) Sexual and individual foraging segregation in Gentoo penguins Pygoscelis papua from the Southern Ocean during an abnormal winter. PLoS ONE 12:e0174850

    Article  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Marcella Libertelli (Instituto Antárctico Argentino) for aiding the identification of small otoliths, Peter Ward for identifying zooplankton, Karim Erzini and Ian Staniland for guidance and revision and to Derren Fox, Stacey Adler and Ewan Edwards for supporting collecting the samples. Thank you to the editor Dieter Piepenburg and referees for the excellent contributions in improving the manuscript. This study is a contribution to the programs SCAR AnT-ERA, SCAR EGBAMM, ICED Dynamics and to the PROPOLAR (Programa Polar Português). JS was supported by Do*MAR PhD FCT fellowship from Fundação para Ciência e Tecnologia (Portugal). JX was supported by the Investigator FCT program (IF/00616/2013). This study benefited from the strategic program of MARE, financed by FCT (MARE- UID/MAR/04292/2013).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. C. Xavier.

Ethics declarations

Conflict of interest

The authors have no conflict of interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xavier, J.C., Velez, N., Trathan, P.N. et al. Seasonal prey switching in non-breeding gentoo penguins related to a wintertime environmental anomaly around South Georgia. Polar Biol 41, 2323–2335 (2018). https://doi.org/10.1007/s00300-018-2372-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-018-2372-8

Keywords

Navigation