Skip to main content
Log in

Paleodietary changes by penguins and seals in association with Antarctic climate and sea ice extent

  • Review
  • Oceanology
  • Published:
Chinese Science Bulletin

Abstract

Positioned near the top of the food web, the dietary composition of Antarctic penguins and seals can be an excellent indicator of the regional food web and thus the status of the marine ecosystem. The dietary composition of modern penguins and seals has been well investigated; a long-term time series of data on penguin and seal diets, however, are rare. Such data, especially any predating the initiation of human harvesting of fish, whales and seals in Antarctica, are crucial for understanding and predicting responses of regional marine food webs to natural climate changes. Here we review recent progress on research of paleodietary change in Antarctic penguins and seals, specifically the Adélie penguin (Pygoscelis adeliae) and Antarctic fur seal (Arctocephalus gazella). These studies indicate that the dietary changes of penguins correspond quite well with fluctuations in climate and sea ice extent during the Holocene. The depleted δ 15N ratios found in modern Adélie penguins support the “krill surplus hypothesis” in relation to historic human depletion of krill-eating fish, seals and whales.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Furness RW, Camphuysen CJ (1997) Seabirds as monitors of the marine environment. ICES J Mar Sci 54:726–737

    Article  Google Scholar 

  2. Nicol S, Worby A, Leaper R (2008) Changes in the Antarctic sea ice ecosystem: potential effects on krill and baleen whales. Mar Freshwater Res 59:361–382

    Article  Google Scholar 

  3. 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  Google Scholar 

  4. Laws RM (1977) Seals and whales of the Southern Ocean. Phil Trans R Soc B 279:81–96

    Article  Google Scholar 

  5. Reid K, Davis D, Staniland IJ (2006) Spatial and temporal variability in the fish diet of Antarctic fur seal (Arctocephalus gazella) in the Atlantic sector of the Southern Ocean. Can J Zool 84:1025–1037

    Article  Google Scholar 

  6. Wilson RP (1984) An improved stomach pump for penguins and other seabirds. J Field Ornithol 55:109–112

    Google Scholar 

  7. Reid K (1995) The diet of Antarctic fur seals (Arctocephalus gazella Peters 1875) during winter at South Georgia. Antarct Sci 7:241–249

    Article  Google Scholar 

  8. Emslie SD, Fraser W, Smith RC et al (1998) Abandoned penguin colonies and environmental change in the Palmer Station area, Anvers Island, Antarctic Peninsula. Antarct Sci 10:257–268

    Article  Google Scholar 

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

    Article  Google Scholar 

  10. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    Article  Google Scholar 

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

    Article  Google Scholar 

  12. Iverson SJ, Arnould JPY, Boyd IL (1997) Milk fatty acid signatures indicate both major and minor shifts in the diet of lactating Antarctic fur seals. Can J Zool 75:188–197

    Article  Google Scholar 

  13. Deagle BE, Chiaradia A, McInnes J et al (2010) Pyrosequencing faecal DNA to determine diet of little penguins: is what goes in what comes out? Conserv Genet 11:2039–2048

    Article  Google Scholar 

  14. Bearhop S, Furness RW, Hilton GM et al (2003) A forensic approach to understanding diet and habitat use from stable isotope analysis of (avian) claw material. Funct Ecol 17:270–275

    Article  Google Scholar 

  15. Sun LG, Emslie SD, Huang T et al (2013) Vertebrate records in polar sediments: biological responses to past climate change and human activities. Earth Sci Rev 126:147–155

    Article  Google Scholar 

  16. 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 Progr Ser 329:281–287

    Article  Google Scholar 

  17. Ambrose SH (1986) Stable carbon and nitrogen isotope analysis of human and animal diet in Africa. J Hum Evol 15:707–731

    Article  Google Scholar 

  18. Hu YW, Shang H, Tong HW et al (2009) Stable isotope dietary analysis of the Tianyuan 1 early modern human. Proc Natl Acad Sci USA 106:10971–10974

    Article  Google Scholar 

  19. Si Y, Lü EG, Li X et al (2013) Exploration of human diets and populations from the Yanghai Tombs, Xinjiang. Chin Sci Bull (Chinese Ver) 58:1422–1429 (in Chinese)

    Article  Google Scholar 

  20. Fry B (1988) Food web structure on Georges Bank from stable C, N, and S isotopic compositions. Limnol Oceangr 33:1182–1190

    Article  Google Scholar 

  21. Cai DL, Li HY, Tang QS et al (2005) The foundation of successive trophic chart for food webs in the ecosystem of the Yellow and East China Seas: the result from carbon and nitrogen stable isotope techniques. Sci China Ser C Life Sci 35:123–130

    Google Scholar 

  22. Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mammal Sci 26:509–572

    Google Scholar 

  23. Ramos R, Gonzalez-Solis J (2012) Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Front Ecol Environ 10:258–266

    Article  Google Scholar 

  24. Mizutani H, Kabaya Y, Wada E (1985) Ammonia volatilization and penguin rookery high 15N/14N ratio in Antarctica. Geochem J 19:323–327

    Article  Google Scholar 

  25. Mizutani H, Hasegawa H, Wada E (1986) High nitrogen isotope ratio for soils of seabird rookeries. Biogeochemistry 2:221–247

    Article  Google Scholar 

  26. Lorenzini S, Baroni C, Fallick AE et al (2010) Stable isotopes reveal Holocene changes in the diet of Adélie penguins in Northern Victoria Land (Ross Sea, Antarctica). Oecologia 164:911–919

    Article  Google Scholar 

  27. Huang T, Sun LG, Long NY et al (2013) Penguin tissue as a proxy for relative krill abundance in East Antarctica during the Holocene. Sci Rep 3:2807

    Google Scholar 

  28. Huang T, Sun LG, Wang YH et al (2014) Transport of nutrients and contaminants from ocean to island by emperor penguins from Amanda Bay, East Antarctic. Sci Total Environ 468–469:578–583

    Article  Google Scholar 

  29. Liu XD, Sun LG, Yin XB et al (2004) Paleoecological implications of the nitrogen isotope signatures in the sediments amended by Antarctic seal excrements. Prog Nat Sci 14:786–792

    Article  Google Scholar 

  30. Huang T, Sun LG, Stark J et al (2011) Relative changes in krill abundance inferred from Antarctic Fur Seal. PLoS One 6:e27331

    Article  Google Scholar 

  31. Emslie SD, Polito MJ, Patterson WP (2013) Stable isotope analysis of ancient and modern gentoo penguin egg membrane and the krill surplus hypothesis in Antarctica. Antarct Sci 25:213–218

    Article  Google Scholar 

  32. Cavallerano EJ (2005) Temporal diagenetic alternations in Adélie penguin eggshells throughout the late Holocene of Antarctica. M.Sc. Thesis, University of North Carolina Wilmington

  33. DeNiro MJ (1985) Post-mortem preservation and alternation of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 317:806–809

    Article  Google Scholar 

  34. Price TD, Blitz J, Burton JH (1992) Diagenesis in prehistoric bone: problems and solutions. J Archaeol Sci 19:513–530

    Article  Google Scholar 

  35. Polito MJ, Reiss CS, Trivelpiece WZ et al (2013) Stable isotopes identify an ontogenetic niche expansion in Antarctic krill (Euphausia superba) from the South Shetland Islands, Antarctica. Mar Biol 160:1311–1323

    Article  Google Scholar 

  36. Wilson EA (1907) Aves in British National Antarctic Expedition Report 1901–1904. Nat Hist 2:1–121

    Google Scholar 

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

    Google Scholar 

  38. Endo Y, Asari H, Watanuki Y et al (2002) Biological characteristics of euphausiids preyed upon by Adélie penguins in relation to sea-ice conditions in Lützow-Holm Bay, Antarctica. Polar Biol 25:730–738

    Google Scholar 

  39. Casaux R, Baroni A, Carlini A (1998) The diet of the Antarctic fur seal Arctocephalus gazella at Harmony Point, Nelson Island, South Shetland Islands. Polar Biol 20:424–428

    Article  Google Scholar 

  40. Ainley DG, Ballard G, Barton KJ et al (2003) Spatial and temporal variation of diet within a presumed metapopulation of Adélie Penguins. Condor 105:95–106

    Article  Google Scholar 

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

    Article  Google Scholar 

  42. Lorrain A, Graham B, Menard F et al (2009) Nitrogen and carbon isotope values of individual amino acids: a tool to study foraging ecology of penguins in the Southern Ocean. Mar Ecol Progr Ser 391:293–306

    Article  Google Scholar 

  43. Beaulieu M, Ropert-Coudert Y, Le Maho Y et al (2010) Foraging in an oxidative environment: relationship between delta C-13 values and oxidative status in Adélie penguins. Proc R Soc B 277:1087–1092

    Article  Google Scholar 

  44. Polito MJ, Trivelpiece WZ, Karnovsky NJ et al (2011) Integrating stomach content and stable isotope analyses to quantify the diets of pygoscelid penguins. PLoS One 6:e26642

    Article  Google Scholar 

  45. Cherel Y, Hobson KA, Guinet C et al (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  Google Scholar 

  46. Green K, Johnstone G (1988) Changes in the diet of Adélie penguins breeding in East Antarctica. Aust Wildlife Res 15:103–110

    Article  Google Scholar 

  47. Puddicombe RA, Johnstone GW (1988) The breeding season diet of Adélie penguins at the Vestfold Hills, East Antarctica. Hydrobiologia 165:239–253

    Article  Google Scholar 

  48. Fraser WR, Hofmann EE (2003) A predator’s perspective on causal links between climate change, physical forcing and ecosystem. Mar Ecol Prog Ser 265:1–15

    Article  Google Scholar 

  49. Emslie SD, McDaniel JD (2002) Adélie penguin diet and climate change during the middle to late Holocene in northern Marguerite Bay, Antarctic Peninsula. Polar Biol 25:222–229

    Google Scholar 

  50. Polito M, Emslie SD, Walker W (2002) A 1000-year record of Adélie penguin diets in the southern Ross Sea. Antarct Sci 14:327–332

    Article  Google Scholar 

  51. Lorenzini S, Olmastroni S, Pezzo F et al (2009) Holocene Adélie penguin diet in Victoria Land, Antarctica. Polar Biol 32:1077–1086

    Article  Google Scholar 

  52. Ainley DG, Wilson PR, Barton KJ et al (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 

  53. 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 

  54. Ainley DG, Hobson KA, Crosta X et al (2006) Holocene variation in the Antarctic coastal food web: linking delta D and delta C-13 in snow petrel diet and marine sediments. Mar Ecol Progr Ser 306:31–40

    Article  Google Scholar 

  55. Emslie SD, Patterson WP (2007) Abrupt recent shift in delta C-13 and delta N-15 values in Adélie penguin eggshell in Antarctica. Proc Natl Acad Sci USA 104:11666–11669

    Article  Google Scholar 

  56. Hodgson DA, Johnston NM (1997) Inferring seal populations from lake sediments. Nature 387:30–31

    Article  Google Scholar 

  57. Sun LG, Xie ZQ, Zhao JL (2000) Palaeoecology—a 3,000-year record of penguin populations. Nature 407:858

    Article  Google Scholar 

  58. Sun LG, Liu XD, Yin XB et al (2004) A 1500-year record of Antarctic seal populations in response to climate change. Polar Biol 27:495–501

    Article  Google Scholar 

  59. Liu XD, Nie YG, Sun LG et al (2013) Eco-environmental implications of elemental and carbon isotope distributions in ornithogenic sediments from the Ross Sea region Antarctica. Geochim Cosmochim Acta 117:99–114

    Article  Google Scholar 

  60. Arrigo KR, Worthen D, Schnell A et al (1998) Primary production in Southern Ocean waters. J Geophys Res 103:15587–15600

    Article  Google Scholar 

  61. Parkinson CL (2004) Southern Ocean sea ice and its wider linkages: insights revealed from models and observations. Antarct Sci 16:387–400

    Article  Google Scholar 

  62. Arrigo KR (2013) Sea ice ecosystems. Annu Rev Mar Sci 6:13.1–13.29

    Google Scholar 

  63. Loeb V, Siegel V, HolmHansen O et al (1997) Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387:897–900

    Article  Google Scholar 

  64. Atkinson A, Siegel V, Pakhomov E et al (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–103

    Article  Google Scholar 

  65. Nicol S, Pauly T, Bindoff NL et al (2000) Ocean circulation off east Antarctica affects ecosystem structure and sea-ice extent. Nature 406:504–507

    Article  Google Scholar 

  66. Gille ST (2002) Warming of the Southern Ocean since the 1950s. Science 295:1275–1277

    Article  Google Scholar 

  67. Ducklow HW, Baker K, Martinson DG et al (2007) Marine pelagic ecosystems: the West Antarctic Peninsula. Phil Trans R Soc B 362:67–94

    Article  Google Scholar 

  68. Schofield O, Ducklow HW, Martinson DG et al (2010) How do polar marine ecosystems respond to rapid climate change? Science 328:1520–1523

    Article  Google Scholar 

  69. Ainley DG, Ballard G, Dugger KM (2006) Competition among penguins and cetaceans reveals trophic cascades in the western Ross Sea, Antarctica. Ecology 87:2080–2093

    Article  Google Scholar 

  70. Agnew DJ (1997) Review—the CCAMLR Ecosystem Monitoring Programme. Antarct Sci 9:235–242

    Article  Google Scholar 

  71. Denis D, Crosta X, Schmidt S et al (2009) Holocene productivity changes off Adélie Land (East Antarctica). Paleoceanography 24:PA3207

    Article  Google Scholar 

  72. Emslie SD, Berkman PA, Ainley DG et al (2003) Late-Holocene initiation of ice-free ecosystems in the southern Ross Sea, Antarctica. Mar Ecol Progr Ser 262:19–25

    Article  Google Scholar 

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

    Article  Google Scholar 

  74. Hall BL, Hoelzel AR, Baroni C et al (2006) Holocene elephant seal distribution implies warmer-than-present climate in the Ross Sea. Proc Natl Acad Sci USA 103:10213–10217

    Article  Google Scholar 

  75. Everson E (2000) Krill: biology, ecology and fisheries. Blackwell Science, London

    Book  Google Scholar 

  76. Smith RIL, Simpson HW (1987) Early nineteenth century sealers’ refuges on Livingston Island, South Shetland Islands. Br Antarct Surv Bull 74:49–72

    Google Scholar 

  77. Boyd IL (1993) Pup production and distribution of breeding Antarctic fur seals (Arctocephalus gazella) at South Georgia. Antarct Sci 5:17–24

    Article  Google Scholar 

  78. Jabour J (2008) Successful conservation-then what? The de-listing of Arctocephalus fur seal species in Antarctica. J Int Wildl Law Pol 11:1–29

    Article  Google Scholar 

  79. Yang QC, Sun LG, Kong DM et al (2010) Variation of Antarctic seal population in response to human activities in 20th century. Chin Sci Bull 55:1084–1087

    Article  Google Scholar 

  80. Huang J, Sun L, Wang X et al (2011) Ecosystem evolution of seal colony and the influencing factors in the 20th century on Fildes Peninsula, West Antarctica. J Environ Sci 23:1431–1436

    Article  Google Scholar 

  81. Croxall JP, Callaghan T, Cervellati R et al (1992) Southern Ocean environmental changes: effects on seabird, seal and whale populations. Phil Trans R Soc B 338:319–328

    Article  Google Scholar 

  82. Ainley DG, Blight LK (2009) Ecological repercussions of historical fish extraction from the Southern Ocean. Fish Fish 10:13–38

    Article  Google Scholar 

  83. Marschoff ER, Barrera-Oro ER, Alescio NS et al (2012) Slow recovery of previously depleted demersal fish at the South Shetland Islands, 1983–2010. Fish Res 125:206–213

    Article  Google Scholar 

  84. Sladen WJL (1964) The distribution of the Adelie and chinstrap penguins. Biologie Antarctique. Hermann, Paris, pp 359–365

    Google Scholar 

  85. 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

    Google Scholar 

  86. Tierney M, Emmerson L, Hindell M (2009) Temporal variation in Adélie penguin diet at Bechervaise Island, east Antarctica and its relationship to reproductive performance. Mar Biol 156:1633–1645

    Google Scholar 

  87. Ainley D, Ballard G, Blight LK et al (2010) Impacts of cetaceans on the structure of Southern Ocean food webs. Mar Mamm Sci 26:482–498

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by National Natural Science Foundation of China (41106162 and 40730107), the Chinese Polar Environment Comprehensive Investigation and Assessment Programmes (CHINARE2014-04-01 and CHINARE2014-02-01) and the Open Research Fund from SOA Key Laboratory for Polar Science in China (KP201207).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Liguang Sun.

About this article

Cite this article

Huang, T., Sun, L., Wang, Y. et al. Paleodietary changes by penguins and seals in association with Antarctic climate and sea ice extent. Chin. Sci. Bull. 59, 4456–4464 (2014). https://doi.org/10.1007/s11434-014-0300-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11434-014-0300-z

Keywords

Navigation