Skip to main content

Advertisement

Log in

Stable isotopes reveal Holocene changes in the diet of Adélie penguins in Northern Victoria Land (Ross Sea, Antarctica)

  • Behavioral ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Adélie penguin (Pygoscelis adeliae) modern and fossil eggshells and guano samples collected from ornithogenic soils in Terra Nova Bay (Victoria Land, Ross Sea) were processed for carbon and nitrogen isotopic ratios with the aim of detecting past penguin dietary changes. A detailed and greatly expanded Adélie penguin dietary record dated back to 7,200 years BP has been reconstructed for the investigated area. Our data indicate a significant dietary shift between fish and krill, with a gradual decrease from past to present time in the proportion of fish compared to krill in Adélie penguin diet. From 7,200 to 2,000 years BP, δ13C and δ15N values indicate fish as the most eaten prey. The dietary contribution of lower-trophic prey in penguin diet started becoming evident not earlier than 2,000 years BP, when the δ13C values reveal a change in the penguin feeding behavior. Modern eggshell and guano samples reveal a major dietary contribution of krill but not a krill-dominated diet, since δ13C values remain much too high if krill prevail in the diet. According to the Holocene environmental background attested for Victoria Land, Adélie penguin dietary shifts between fish and krill seem to reflect penguin paleoecological responses to different paleoenvironmental settings with different conditions of sea-ice extension and persistence. Furthermore, Adélie penguin diet appears to be particularly affected by environmental changes in a very specific period within the breeding season, namely the egg-laying period when penguin dietary and feeding habit shifts are clearly documented by the δ13C of eggshell carbonate.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ainley DG (2002) The Adélie penguin: bellwether of climate change. Columbia University Press, New York

    Google Scholar 

  • Ainley DG, Wilson PR, BartonKJ Ballard G, Nur N, Karl B (1998) Diet and foraging effort of Adélie penguins in relation to pack-ice conditions in the southern Ross Sea. Polar Biol 20:311–319

    Article  Google Scholar 

  • Ainley DG, Ballard G, Barton KJ, Karl BJ, Rau GH, Ribic CA, Wilson PR (2003) Spatial and temporal variation of diet within a presumed metapopulation of Adélie penguins. Condor 105:95–106

    Article  Google Scholar 

  • Ainley DG, Clarke ED, Arrigo K, Fraser WR, Kato A, Barton KJ, Wilson PR (2005) Decadal-scale changes in the climate and biota of the Pacific sector of the Southern Ocean, 1950s to the 1990s. Antarct Sci 17:171–182

    Article  Google Scholar 

  • Arrigo KR, van Dijken GL, Ainley DG, Fahnestock MA, Markus T (2002) Ecological impact of a large Antarctic iceberg. Geophys Res Lett 29:1104

    Article  Google Scholar 

  • Astheimer LB, Grau CR (1985) The timing and energetic consequences of egg formation in the Adélie penguin. Condor 87:256–268

    Article  Google Scholar 

  • Baroni C, Hall BL (2004) A new Holocene relative sea-level curve for Terra Nova Bay, Victoria Land, Antarctica. J Quat Sci 19:377–396

    Article  Google Scholar 

  • Baroni C, Orombelli G (1991) Holocene raised beaches at Terra Nova Bay, Victoria Land, Antartica. Quat Res 36:157–177

    Article  CAS  Google Scholar 

  • Baroni C, Orombelli G (1994a) Abandoned penguin rookeries as Holocene paleoclimatic indicators in Antarctica. Geology 22:23–26

    Article  Google Scholar 

  • Baroni C, Orombelli G (1994b) Holocene glacier variations in Terra Nova bay area (Victoria Land, Antartica). Antarct Sci 6:497–505

    Article  Google Scholar 

  • Berkman PA, Forman SL (1996) Pre-bomb radiocarbon and the reservoir correction for calcareous marine species in the Southern Ocean. Geophys Res Lett 23:363–366

    Article  CAS  Google Scholar 

  • Croxall JP, Trathan PN, Murphy EJ (2002) Environmental change and Antarctic seabird populations. Science 297:1510–1514

    Article  CAS  PubMed  Google Scholar 

  • de Bruyn M, Hall BL, Chauke LF, Baroni C, Koch PL, Rus Hoelzel A (2009) Rapid response of a marine mammal species to holocene climate and habitat change. PLoS Genet 5(7):e1000554. doi:10.1371/journal.pgen.1000554

  • DeNiro MJ, Epstein S (1978) Influences of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42(5):495–506

    Article  CAS  Google Scholar 

  • Emmerson L, Southwell C (2008) Sea ice cover and its influence on Adélie enguin reproductive performance. Ecology 89:2096–2102

    Article  PubMed  Google Scholar 

  • Emslie SD, Patterson WP (2007) Abrupt shift in δ13C and δ15N values in Adélie penguin eggshell in Antarctica. Proc Natl Acad Sci USA 104:11666–11669

    Article  CAS  PubMed  Google Scholar 

  • Emslie SD, Woehler EJ (2005) A 9000-year record of Adélie penguin occupation and diet in the Windmill Islands, East Antarctica. Antarct Sci 17:57–66

    Article  Google Scholar 

  • Emslie SD, Coats L, Licht K (2007) A 45, 000 year record of Adélie penguins and climate change in the Ross Sea, Antarctica. Geology 35:61–64

    Article  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  • Hall BL (2009) Holocene glacial history of Antarctica and the sub-Antarctic islands. Quat Sci Rev 28:2213–2230

    Article  Google Scholar 

  • Hall BL, Baroni C, Denton GH (2004) Holocene relative sea-level history of the Southern Victoria Land Coast, Antarctica. Glob Planet Chang 42:241–263

    Article  Google Scholar 

  • Hall BL, Hoelzel AR, Baroni C, Denton GH, Le Boeuf BJ, Overturf B, Töpf AL (2006) Holocene elephant seal distribution implies warmer-than-present climate in the Ross Sea. Proc Natl Acad Sci USA 103:10213–10217

    Article  CAS  PubMed  Google Scholar 

  • Hobson KA (1995) Reconstructing avian diets using stable-carbon and nitrogen isotope analysis of egg components: patterns of isotopic fractionation and turnover. Condor 97:752–762

    Article  Google Scholar 

  • Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798

    Article  Google Scholar 

  • Ivany LC, Van Simaeys S, Domaci EW, Samson SD (2006) Evidence for an earliest Oligocene ice sheet on the Antarctic Peninsula. Geology 34:377–380

    Article  Google Scholar 

  • Koch PL, Fogel ML, Tuross N (1994) Tracing the diet of fossil animals using stable isotopes. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and environmental science. Blackwell, New York, pp 63–92

    Google Scholar 

  • Lambert DM, Ritchie PA, Millar CD, Holland B, Drummond AJ, Baroni C (2002) Rates of evolution in ancient DNA from Adélie penguins. Science 295:2270–2273

    Article  CAS  PubMed  Google Scholar 

  • Lorenzini S, Olmastroni S, Pezzo F, Salvatore MC, Baroni C (2009) Holocene Adélie penguin diet in Victoria Land, Antarctica. Polar Biol 32:1077–1086

    Article  Google Scholar 

  • Millar CD, Dodd A, Anderson J, Gibb GC, Ritchie PA, Baroni C, Woodhams MD, Hendy MD, Lambert DM (2008) Mutation and evolutionary rates in Adélie penguins from the Antarctic. PLoS Genetics 4:1–9

    Article  Google Scholar 

  • Minagawa M, Wada E (1984) Stepwise enrichment of δ15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140

    Article  CAS  Google Scholar 

  • Mizutani H, Wada E (1988) Nitrogen and carbon isotope ratios in sea bird rookeries and their ecological implications. Ecology 69:340–349

    Article  Google Scholar 

  • Roberts D, van Ommen TD, McMinn A, Morgan V, Roberts JL (2001) Late-Holocene East Antarctic climate trends from ice-core and lake-sediment proxies. The Holocene 11:117–120

    Article  Google Scholar 

  • Schaffner FC, Swart PK (1991) Influence of diet and environmental water on the carbon and oxygen isotopic signatures of seabird eggshell carbonate. Bull Mar Sci 48:23–38

    Google Scholar 

  • Sinclair AJ (1974) Selection of threshold values in geochemical data using probability graphs. J Geochem Explor 3:129–149

    Article  CAS  Google Scholar 

  • StatSoft inc (2005) STATISTICA (Data analysis software system). Version 7.1. 2005. Available in: http://www.statsoft.com

  • Stonehouse B (1970) Recent climatic change in Antarctica suggested from 14C dating of penguin remains. Palaeogeogr Palaeoclimatol Palaeoecol 7:341–343

    Article  Google Scholar 

  • Taylor F, Whitehead J, Domack E (2001) Holocene paleoclimate change in the Antarctic Peninsula: evidence from the diatom, sedimentary and geochemical record. Mar Micropaleontol 41:25–43

    Article  Google Scholar 

  • Ugolini FC (1972) Ornithogenic soils of Antarctica. In: Llano GA (ed) Antarctic terrestrial biology. American Geophysical Union, Antarct Res Ser, vol 20, pp 181–193

  • Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066

    Article  CAS  Google Scholar 

  • Walsh JE (1950) Some nonparametric tests of whether the largest observation of a set are too large or too small. Ann Math Statist 21:583–592

    Article  Google Scholar 

  • Zane L, Marcato S, Bargelloni L, Bortolotto E, Papetti C, Simonato M, Varotto V, Patarnello T (2006) Demographic history and population structure of the Antarctic silverfish Pleuragramma antarcticum. Mol Ecol 15:4499–4511

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was executed under the financial support of the Italian National Program on Antarctic Research (PNRA) and of the PhD School in Earth Sciences of the University of Pisa. Isotopic analyses were performed at the SUERC of East Kilbride (Scotland) and at the IGG-CNR of Pisa (Italy). We particularly thank Julie Dougans and Andrew Tait for their irreplaceable technical support and supervision in stable isotope analyses at SUERC. New radiocarbon dates on penguin remains reported here were performed at the National Ocean Sciences Accelerator Mass Spectrometry Facility (NOSAMS) at the Woods Hole Oceanographic Institution (USA). We finally thank S. McWilliams, D. Ainley and a third anonymous reviewer for their careful readings and constructive suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sandra Lorenzini.

Additional information

Communicated by Scott McWilliams.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 186 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lorenzini, S., Baroni, C., Fallick, A.E. et al. Stable isotopes reveal Holocene changes in the diet of Adélie penguins in Northern Victoria Land (Ross Sea, Antarctica). Oecologia 164, 911–919 (2010). https://doi.org/10.1007/s00442-010-1790-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1790-2

Keywords

Navigation