Marine Biology

, 164:39

Long-term variability in the diet and reproductive performance of penguins at Bird Island, South Georgia

  • Claire M. Waluda
  • Simeon L. Hill
  • Helen J. Peat
  • Philip N. Trathan
Original paper

Abstract

Inter-annual variability in diet during crèche (December to February) over 22 years (1989–2010) was examined for gentoo penguins Pygoscelis papua breeding at Bird Island, South Georgia (54°00′S, 38°03′W). Overall, diets comprised 51% crustaceans and 49% fish by mass. Crustaceans were present in 89% of samples and were the main prey (>50% by mass) in 10 years of the study. Antarctic krill Euphausia superba were present in 85% of all diet samples. Fish were present in 79% of samples and were the main prey in 12 years, with Champsocephalus gunnari and Lepidonotothen larseni the most frequently recorded species, in 51 and 33% of samples, respectively. The energy or mass of krill in the diet was the most reliable predictor of breeding success (the number of chicks fledged per breeding pair); the correlation between model-predicted and observed values was 0.58. We compared annual patterns of gentoo penguin diet variability with those of macaroni penguins Eudyptes chrysolophus breeding at the same location. Our results suggest that the availability of krill is a key source of diet variability for both species, but their diets indicate that gentoo penguins are generalist predators (feeding on pelagic and bentho-pelagic prey), while macaroni penguins are krill specialists (feeding on pelagic prey). Differences in the response to variability in key prey species is an important factor separating the ecological niches of these two sympatric krill predators.

Keywords

Gentoo penguin Macaroni penguin Diet Krill Fish South Georgia Ecosystem monitoring 

References

  1. Adams NJ, Klages NT (1989) Temporal variation in the diet of the gentoo penguin Pygoscelis papua at sub-Antarctic Marion Island. Colon Waterbird 12:30–36CrossRefGoogle Scholar
  2. Agnew DJ (1997) The CCAMLR Ecosystem Monitoring Programme. Antarct Sci 9:235–242CrossRefGoogle Scholar
  3. Agnew DJ (2004) Fishing South. The history and management of South Georgia fisheries. The Penna Press, St AlbansGoogle Scholar
  4. Ainley DG, Blight LK (2009) Ecological repercussions of historical fish extraction from the Southern Ocean. Fish Fish 10:13–38CrossRefGoogle Scholar
  5. Bost CA, Jouventin P (1991) Relationships between fledging weight and food availability in seabird populations: is the gentoo penguin a good model? Oikos 60:113–114CrossRefGoogle Scholar
  6. 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 14:147–153CrossRefGoogle Scholar
  7. Boyd IL (1993) Pup production and distribution of breeding Antarctic fur seals (Artocephalus gazella) at South Georgia. Ant Sci 5:17–24CrossRefGoogle Scholar
  8. Boyd IL, Murray AWA (2001) Monitoring a marine ecosystem using responses of upper trophic level predators. J Anim Ecol 70:747–760CrossRefGoogle Scholar
  9. Brierley AS, Watkins JL, Goss C, Wilkinson MT, Everson I (1999) Acoustic estimates of krill density at South Georgia, 1981–1998. CCAMLR Sci 6:47–57Google Scholar
  10. Brown CR, Klages NT, Adams NJ (1990) Short and medium-term variation in the diets of penguins at Marion Island. S Afr J Ant Res 20:13–20Google Scholar
  11. Burchett MS, Sayers PJ, North AW, White MG (1983) Some biological aspects of the nearshore fish populations at South Georgia. Br Antarct Surv Bull 59:63–74Google Scholar
  12. Cairns DK (1987) Seabirds as indicators of marine food supplies. Biol Oceanogr 5:261–271Google Scholar
  13. CCAMLR (2014) CCAMLR Ecosystem Monitoring Program (CEMP) Standard Methods. CCAMLR, Hobart. https://www.ccamlr.org/en/document/science/cemp-standard-methods Google Scholar
  14. Cherel Y, Ridoux V (1992) Prey species and nutritive value of food fed during summer to King Penguin Aptenodytes patagonica chicks at Possession Island, Crozet Archipelago. Ibis 134:118–127CrossRefGoogle Scholar
  15. Chiaradia A, Forero MG, Hobson KA, Cullen JM (2010) Changes in diet and trophic position of a top predator 10 years after a mass mortality of a key prey. ICES J Mar Sci 67:1710–1720CrossRefGoogle Scholar
  16. Ciancio JE, Pascual MA, Beauchamp DA (2007) Energy density of Patagonian aquatic organisms and empirical predictions based on water content. Trans Am Fish Soc 136:1415–1422CrossRefGoogle Scholar
  17. Clarke A (1980) The biochemical composition of krill, Euphausia superba Dana, from South Georgia. J Exp Mar Biol Ecol 43:221–236CrossRefGoogle Scholar
  18. Clarke MR (1986) A handbook for the identification of cephalopod beaks. Clarendon Press, OxfordGoogle Scholar
  19. Clarke A, Prince PA (1980) Chemical composition and calorific value of food fed to mollymauk chicks Diomedia melanophris and D. chrysostoma at Bird Island, South Georgia. Ibis 122:488–494CrossRefGoogle Scholar
  20. Clarke A, Clarke MR, Holmes LJ, Waters TD (1985) Calorific values and elemental analysis of eleven species of oceanic squids (Mollusca: Cephalopoda). J Mar Biol Ass UK 65:983–986CrossRefGoogle Scholar
  21. Clausen AP, Pütz K (2002) Recent trends in diet composition and productivity of gentoo, magellanic and rockhopper penguins in the Falkland Islands. Aquat Conserv 12:51–61CrossRefGoogle Scholar
  22. Clausen AP, Arkhipkin AI, Laptikhovsky VV, Huin N (2005) What is out there? Diversity in feeding of gentoo penguins (Pygoscelis papua) around the Falkland Islands (Southwest Atlantic). Polar Biol 28:653–662CrossRefGoogle Scholar
  23. Collins MA, Allcock AL, Belchier M (2004) Cephalopods of the South Georgia slope. J Mar Biol Ass UK 84:415–419CrossRefGoogle Scholar
  24. Coria N, Libertelli MM, Casaux R, Darrieu C (2000) Inter-annual variation in the autumn diet of the gentoo penguin at Laurie Island, Antarctica. Waterbirds 23:511–517CrossRefGoogle Scholar
  25. Croxall JP, Prince PA (1980) The food of gentoo penguins Pygoscelis papua and macaroni penguins Eudyptes chrysolophus at South Georgia. Ibis 122:245–253CrossRefGoogle Scholar
  26. Croxall JP, Prince PA (1987) Seabirds as predators on marine resources, especially krill at South Georgia. In: Croxall JP (ed) Seabirds: feeding ecology and role in marine ecosystems. Cambridge University Press, Cambridge, pp 347–368Google Scholar
  27. Croxall JP, McCann TS, Prince PA, Rothery P (1988a) Reproductive performance of seabirds and seals at South Georgia and Signy Island, South Orkney Islands, 1976–1987: implications for Southern Ocean monitoring studies. In: Sahrhage D (ed) Antarctic Ocean and resources variability. Springer-Verlag, Berlin, pp 261–285Google Scholar
  28. Croxall JP, Davis RW, O’Connell MJ (1988b) Diving patterns in relation to diet of gentoo and macaroni penguins at South Georgia. Condor 90:157–167Google Scholar
  29. Croxall JP, Prince PA, Reid K (1997) Dietary segregation of krill-eating South Georgia seabirds. J Zool Lond 242:531–556CrossRefGoogle Scholar
  30. 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 177:115–131CrossRefGoogle Scholar
  31. Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T, Crawford RJM, Furness RW, Mills JA, Murphy EJ, Oesterblom H, Paleczny M, Piatt JF, Roux JP, Shannon L, Sydeman WJ (2011) Global seabird response to forage fish depletion - one-third for the birds. Science 334:1703–1706CrossRefGoogle Scholar
  32. Deagle BE, Gales NJ, Evans K, Jarman SN, Robinson S, Trebilco R, Hindell MA (2007) Studying seabird diet through genetic analysis of faeces: a case study on macaroni penguins (Eudyptes chrysolophus). PLoS one 2(9):e831. doi:10.1371/journal.pone.0000831:1-10 CrossRefGoogle Scholar
  33. Donnelly J, Torres JJ, Hopkins TL, Lancraft TM (1990) Proximate composition of Antarctic mesopelagic fishes. Mar Biol 106:13–23CrossRefGoogle Scholar
  34. Dwyer KS, Buren A, Koen-Alonso M (2010) Greenland halibut diet in the Northwest Atlantic from 1978 to 2003 as an indicator of ecosystem change. J Sea Res 64:427–504CrossRefGoogle Scholar
  35. Fielding S, Watkins JL, Trathan PN, Enderlein P, Waluda CM, Stowasser G, Tarling GA, Murphy EJ (2014) Interannual variability in Antarctic krill (Euphausia superba) density at South Georgia, Southern Ocean: 1997–2013. ICES J Mar Sci. doi:10.1093/icesjms/fsu104 Google Scholar
  36. Handley JM, Baylis AMM, Brickle P, Pistorius P (2016) Temporal variation in the diet of gentoo penguins at the Falkland Islands. Polar Biol 39:283–296CrossRefGoogle Scholar
  37. Hanson JM, Chouinard GA (2002) Diet of Atlantic cod in the southern Gulf of St Lawrence as an index of ecosystem change, 1959–2000. J Fish Biol 60:902–922Google Scholar
  38. Hill SL, Reid K, North AW (2005) Recruitment of mackerel icefish (Champsocephalus gunnari) at South Georgia indicated by predator diets and its relationship with sea surface temperature. Can J Fish Aquat Sci 62:2530–2537CrossRefGoogle Scholar
  39. Jablonski B (1985) The diet of penguins on King George Island, South Shetland Islands. Acta Biol Cracov Zoo 29:177–186Google Scholar
  40. Klages NT, Pemberton D, Gales RP (1990) The diets of king and gentoo penguins at Heard Island. Aust Wildl Res 17:53–60CrossRefGoogle Scholar
  41. Kock K-H, Barrera-Oro ER, Belchier M, Collins MA, Duhamel G, Hanchet S, Pshenichnov L, Welsford D, Williams R (2012) The role of fish as predators of krill (Euphausia superba) and other pelagic resources in the Southern Ocean. CCAMLR Sci 19:115–169Google Scholar
  42. Kokubun N, Takahashi A, Mori Y, Watanabe S, Shin HC (2010) Comparison of diving behavior and foraging habitat use between chinstrap and gentoo penguins breeding in the South Shetland Islands, Antarctica. Mar Biol 157:811–825CrossRefGoogle Scholar
  43. Lea MA, Cherel Y, Guinet C, Nichols PD (2002) Antarctic fur seals foraging in the Polar Frontal Zone: inter-annual shifts in diet as shown from fecal and fatty acid analyses. Mar Ecol Prog Ser 245:281–297CrossRefGoogle Scholar
  44. Lescroël A, Ridoux V, Bost CA (2004) Spatial and temporal variation in the diet of the gentoo penguin (Pygoscelis papua) at Kerguelen Islands. Polar Biol 27:206–216CrossRefGoogle Scholar
  45. Lynch HJ (2012) Gentoo penguin (Pygoscelis papua). In: Borboroglu PG, Boersma PD (eds) Penguins natural history and conservation. University of Washington Press, Seattle, pp 73–88Google Scholar
  46. McInnes JC, Alderman R, Deagle BE, Lea M-A, Raymond B, Jarman SN (2016) Optimised scat collection protocols for dietary DNA metabarcoding in vertebrates. Methods Ecol Evol. doi:10.1111/2041-210X.12677 Google Scholar
  47. Miller AK, Karnovsky NJ, Trivelpiece WZ (2009) Flexible foraging strategies of gentoo penguins Pygoscelis papua over 5 years in the South Shetland Islands, Antarctica. Mar Biol 156:2527–2537CrossRefGoogle Scholar
  48. Miller AK, Kappes MA, Trivelpiece SG, Trivelpiece WZ (2010) Foraging-niche separation of breeding gentoo and chinstrap penguins, South Shetland Islands, Antarctica. Condor 112:683–695CrossRefGoogle Scholar
  49. Piatt JF, Harding AMA, Shultz M, Speckman SG, van Pelt TI, Drew GS, Kettle AB (2007) Seabirds as indicators of marine food supplies: Cairns revisited. Mar Ecol Prog Ser 352:221–234CrossRefGoogle Scholar
  50. Polito MJ, Trivelpiece WZ, Patterson WP, Karnovsky NJ, Reiss C, Emslie SD (2015) Contrasting specialist and generalist patterns facilitate foraging niche partitioning in sympatric populations of Pygoscelis penguins. Mar Ecol Prog Ser 519:221–237CrossRefGoogle Scholar
  51. Pütz K, Ingham RJ, Smith JG, Croxall JP (2001) Population trends, breeding success and diet composition of gentoo Pygoscelis papua, magellanic Spheniscus magellanicus and rockhopper Eudyptes chrysocome penguins in the Falkland Islands. Polar Biol 24:793–807CrossRefGoogle Scholar
  52. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  53. Ratcliffe N, Trathan PN (2011) A review of the diet and at-sea distribution of penguins breeding within the CAMLR convention area. CCAMLR Sci 18:75–114Google Scholar
  54. Reid K, Arnould JPY (1996) The diet of Antarctic fur seals Arctocephalus gazella during the breeding season at South Georgia. Polar Biol 16:105–114CrossRefGoogle Scholar
  55. Reid K, Croxall JP (2001) Environmental response of upper trophic-level predators reveals a system change in an Antarctic marine ecosystem. Proc R Soc Lond B 268:377–384CrossRefGoogle Scholar
  56. Reid K, Hill SL, Diniz TCD, Collins MA (2005a) Mackerel icefish Champsocephalus gunnari in the diet of upper trophic level predators at South Georgia: implications for fisheries management. Mar Ecol Prog Ser 305:153–161Google Scholar
  57. Reid K, Croxall JP, Briggs DR, Murphy EJ (2005b) Antarctic ecosystem monitoring: quantifying the response of ecosystem indicators to variability in Antarctic krill. ICES J Mar Sci 62:366–373Google Scholar
  58. 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 84:1025–1037CrossRefGoogle Scholar
  59. Reid K, Watkins JL, Murphy EJ, Trathan PN, Fielding S, Enderlein P (2010) Krill population dynamics at South Georgia: implications for ecosystem-based fisheries management. Mar Ecol Prog Ser 399:243–252CrossRefGoogle Scholar
  60. Ridoux V (1994) The diets and dietary segregation of seabirds at the Subantarctic Crozet Islands. Mar Ornithol 22:1–192Google Scholar
  61. Robinson SA, Hindell MA (1996) Foraging ecology of gentoo penguins Pygoscelis papua at Macquarie Island during the period of chick care. Ibis 138:722–731CrossRefGoogle Scholar
  62. Rodhouse PG, Prince PA, Clarke MR, Murray AWA (1990) Cephalopod prey of the grey-headed albatross Diomedea chrysostoma. Mar Biol 104:353–362CrossRefGoogle Scholar
  63. Staniland IJ, Boyd IL, Reid K (2007) An energy–distance trade-off in a central-place forager, the Antarctic fur seal (Arctocephalus gazella). Mar Biol 152:233–241CrossRefGoogle Scholar
  64. Stowasser G, Atkinson A, McGill RAR, Phillips RA, Pond DW (2012) Food web dynamics in the Scotia Sea in summer: A stable isotope study. Deep Sea Res II 59–60:208–221Google Scholar
  65. Tierney M, Hindell MA, Goldsworthy S (2002) Energy content of mesopelagic fish from Macquarie Island. Antarct Sci 14:225–230CrossRefGoogle Scholar
  66. Torres JJ, Donnelly J, Hopkins TL, Lancraft TM, Aarset AV, Ainley DG (1994) Proximate composition and overwintering strategies of Antarctic micronektonic crustacea. Mar Ecol Prog Ser 113:221–232CrossRefGoogle Scholar
  67. Trathan PN, Reid K (2009) Exploitation of the marine ecosystem in the sub-Antarctic: historical impacts and current consequences. Pap Proc Roy Soc Tasmania 143:9–14Google Scholar
  68. Trathan PN, Murphy EJ, Forcada J, Croxall JP, Reid K, Thorpe SE (2006) Physical forcing in the southwest Atlantic: ecosystem control. In: Boyd IL, Wanless S, Camphuysen CJ (eds) Top predators in marine ecosystems. Cambridge University Press, Cambridge, pp 28–45CrossRefGoogle Scholar
  69. Trathan PN, Ratcliffe N, Masden EA (2012) Ecological drivers of change at South Georgia: the krill surplus, or climate variability? Ecography 35:983–993CrossRefGoogle Scholar
  70. Vanella FA, Calvo J, Morriconi ER, Aureliano DR (2005) Somatic energy content and histological analysis of the gonads in Antarctic fish from the Scotia Arc. Sci Mar 69:305–316CrossRefGoogle Scholar
  71. Waluda CM, Collins MA, Black AD, Staniland IJ, Trathan PN (2010) Linking predator and prey behaviour: contrasts between Antarctic fur seals and macaroni penguins at South Georgia. Mar Biol 157:99–112CrossRefGoogle Scholar
  72. Waluda CM, Hill SL, Peat HJ, Trathan PN (2012) Diet variability and reproductive performance of macaroni penguins Eudyptes chrysolophus at Bird Island, South Georgia. Mar Ecol Prog Ser 466:261–274CrossRefGoogle Scholar
  73. Williams TD (1990) Annual variation in breeding biology of gentoo penguins Pygoscelis papua at Bird Island, South Georgia. J Zool Lond 222:247–258CrossRefGoogle Scholar
  74. Williams TD (1991) Foraging ecology and diet of gentoo penguins Pygoscelis papua at South Georgia during winter and an assessment of their winter prey consumption. Ibis 133:3–13CrossRefGoogle Scholar
  75. 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 Lond 227:211–230CrossRefGoogle Scholar
  76. Wilson RP (1984) An improved stomach pump for penguins and other seabirds. J Field Ornithol 55:109–112Google Scholar
  77. Wilson RP (2010) Resource partitioning and niche hyper-volume overlap in free-living Pygoscelid penguins. Funct Ecol 24:646–657CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Claire M. Waluda
    • 1
  • Simeon L. Hill
    • 1
  • Helen J. Peat
    • 1
  • Philip N. Trathan
    • 1
  1. 1.British Antarctic SurveyNatural Environment Research CouncilCambridgeUK

Personalised recommendations