, Volume 161, Issue 2, pp 253–265

Nonlinear effects of winter sea ice on the survival probabilities of Adélie penguins

  • Tosca Ballerini
  • Giacomo Tavecchia
  • Silvia Olmastroni
  • Francesco Pezzo
  • Silvano Focardi
Population Ecology - Original Paper


The population dynamics of Antarctic seabirds are influenced by variations in winter sea ice extent and persistence; however, the type of relationship differs according to the region and the demographic parameter considered. We used annual presence/absence data obtained from 1,138 individually marked birds to study the influence of environmental and individual characteristics on the survival of Adélie penguins Pygoscelis adeliae at Edmonson Point (Ross Sea, Antarctica) between 1994 and 2005. About 25% of 600 birds marked as chicks were reobserved at the natal colony. The capture and survival rates of Adélie penguins at this colony increased with the age of individuals, and five age classes were identified for both parameters. Mean adult survival was 0.85 (SE = 0.01), and no effect of sex on survival was evident. Breeding propensity, as measured by adult capture rates, was close to one, indicating a constant breeding effort through time. Temporal variations in survival were best explained by a quadratic relationship with winter sea ice extent anomalies in the Ross Sea, suggesting that for this region optimal conditions are intermediate between too much and too little winter sea ice. This is likely the result of a balance between suitable wintering habitat and food availability. Survival rates were not correlated with the Southern Oscillation Index. Low adult survival after a season characterized by severe environmental conditions at breeding but favorable conditions during winter suggested an additional mortality mediated by the reproductive effort. Adélie penguins are sensitive indicators of environmental changes in the Antarctic, and the results from this study provide insights into regional responses of this species to variability in winter sea ice habitat.


Age dependence Capture–mark–recapture Life history Population dynamics Southern Oscillation Index 


  1. Ainley DG (2002) The Adélie penguin. Bellwether of climate change. Columbia University Press, New YorkGoogle Scholar
  2. Ainley DG, LeResche RE, Sladen WJL (1983) Breeding biology of the Adélie penguin. University of California, BerkeleyGoogle Scholar
  3. Ainley DG, Nur R, Woehler EJ (1995) Factors affecting the distribution and size of pygoscelid penguin colonies in the Antarctic. Auk 112:171–182Google Scholar
  4. Ainley DG, Clarke ED, Arrigo KR, 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–1990s. Antarct Sci 17:171–182CrossRefGoogle Scholar
  5. Ainley D, Ballard G, Ackley S, Blight LK, Eastman JT, Emslie SD, Lescroel A, Olmastroni S, Towsend SE, Tynan CT, Wilson P, Woehler E (2007) Opininon: paradigm lost, or top-down forcing no longer significant in the Antarctic marine ecosystem? Antarct Sci 19:283–290CrossRefGoogle Scholar
  6. Barbraud C, Weimerskirch H (2001) Emperor penguins and climate change. Nature 411:183–186PubMedCrossRefGoogle Scholar
  7. Baroni C, Orombelli G (1994) Abandoned penguin rookeries as Holocene paleoclimatic indicators in Antarctica. Geology 22:23–26CrossRefGoogle Scholar
  8. Burnham KP, Anderson (2002) Selection and multi-inference. A practical information–theoretic approach. Springer, New YorkGoogle Scholar
  9. Catchpole EA, Morgan BJT, Coulson JN, Freeman SN, Albon SD (2000) Factors influencing soay sheep survival. Appl Stat 49:453–472Google Scholar
  10. Chastel O, Weimerskirch H, Jouventin P (1993) High annual variability in reproductive success and survival of an Antarctic seabird, the Snow Petrel Pagodroma nivea: a 27-year study. Oecologia 94:278–285Google Scholar
  11. Choquet R, Reboulet AM, Pradel R, Gimenez O, Lebreton JD (2005a) M-SURGE 1.7: user’s manual. CEFE/CNRS, MontpellierGoogle Scholar
  12. Choquet R, Reboulet AM, Pradel R, Gimenez O, Lebreton JD (2005b) U-CARE 2.2: user’s manual. CEFE, MontpellierGoogle Scholar
  13. Clarke J, Emmerson LM, Townsed A, Kerry KR (2003) Demographic characteristics of the Adélie penguin population on Béchervaise Island after 12 years of study. CCAMLR Sci 10:53–74Google Scholar
  14. Clutton-Brock TH (ed) (1988) Reproductive success. University of Chicago Press, ChicagoGoogle Scholar
  15. Coulson T, Catchpole EA, Albon SD, Morgan BJT, Pemberton JM, Clutton-Brock TH, Crawley MJ, Grenfell BT (2001) Age, sex, density, winter weather and population crashes in Soay sheep. Science 292:1528–1531PubMedCrossRefGoogle Scholar
  16. Crespin L, Harris MP, Lebreton JD, Frederiksen M, Wanless S (2006) Recruitment to a seabird population depends on environmental factors and on population size. J Anim Ecol 75(1):228–238PubMedCrossRefGoogle Scholar
  17. Croxall JP, Nicol S (2004) Management of Southern Ocean fisheries: global forces and future sustainability. Antarct Sci 16:569–584CrossRefGoogle Scholar
  18. Croxall J, Trathan P, Murphy EJ (2002) Environmental change and antarctic seabird populations. Science 297:1510–1514PubMedCrossRefGoogle Scholar
  19. Davis LS, Boersma PD, Court GS (1996) Satellite telemetry of the winter migration of Adélie penguins (Pygoscelis adeliae). Polar Biol 16:221–225CrossRefGoogle Scholar
  20. Davis LS, Harcourt RG, Brasdshaw CJA (2001) The winter migration of Adélie penguins breeding in the Ross Sea sector of Antarctica. Polar Biol 24:593–597CrossRefGoogle Scholar
  21. Davis SE, Nager RG, Furness RW (2005) Food availability affects adult survival as well as breeding success of parasitic jaegers. Ecology 86:1047–1056CrossRefGoogle Scholar
  22. Drent RH, Dann S (1980) The prudent parent: energetic adjustment in avian breeding. Ardea 68:225–252Google Scholar
  23. Dugger KM, Ballard G, Ainley DG, Barton KJ (2006) Effects of flipper bands on foraging behavior and survival of Adélie penguins (Pygoscelis adeliae). Auk 123:858–869CrossRefGoogle Scholar
  24. Emmerson L, Southwell C (2008) Sea ice cover and its influence on Adélie penguin reproductive performance. Ecology 89(8):2096–2102PubMedCrossRefGoogle Scholar
  25. Emslie SD, Coats L, Licht K (2007) A 45,000 year record of Adelie penguins and climate change in the Ross Sea, Antarctica. Geology 35(1):61–64CrossRefGoogle Scholar
  26. Erikstad KE, Fauchald P, Tveraa T, Steen H (1998) On the cost of reproduction in long-lived birds: the influence of environmental variability. Ecology 79:1781–1788CrossRefGoogle Scholar
  27. Ferreyra G, Schloss I, Demers S (2004) Rôle de la glace saisonnière dans la dynamique de l’écosystème marin de l’Antarctique: impact potentiel du changement climatique global. Vertigo 5:1–11Google Scholar
  28. 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 12:411–423CrossRefGoogle Scholar
  29. Fraser WR, Trivelpiece WZ (1996) Factors controlling the distribution of seabirds: winter–summer heterogeneity in the distribution of Adélie penguin populations. In: Hoffmann E, Ross R, Quetin L (eds) Foundations for ecological research west of the Antarctic Peninsula. American Geophysical Union, Washington, pp 257–272Google Scholar
  30. Gaillard J-M, Yoccoz NG (2004) Temporal variation in survival of mammals: a case of environmental canalization. Ecology 84:3294–3306CrossRefGoogle Scholar
  31. Gaillard J-M, Festa-Bianchet M, Yoccoz NG, Loison A, Toigo C (2000) Temporal variation in fitness components and population dynamics of large herbivores. Annu Rev Ecol Syst 31:367–393Google Scholar
  32. Gloersen P, Campbell WJ, Cavalieri DJ, Comiso JC, Parkinson CL, Zwally HJ (1992) Arctic and Antarctic sea ice, 1978–1987: satellite passive-microwave observations and analysis (NASA SP-511). National Aeronautics and Space Administration, WashingtonGoogle Scholar
  33. Grosbois V, Tavecchia G (2003) Modeling dispersal with capture–recapture data: disentangling decisions of leaving and settlement. Ecology 84:1225–1236Google Scholar
  34. Hadley LG, Rotella JJ, Garrott AR (2007) Influence of maternal characteristics and oceanographic conditions on survival and recruitment probabilities of Weddell seals. Oikos 116:601–613CrossRefGoogle Scholar
  35. Hall BL, Hoelzel AR, Baroni C, Denton GH, Le Boeuf BJ, Overturf B, Topf AL (2006) Holocene elephant seal distribution implies warmer-than-present climate in the Ross Sea. Proc Natl Acad Sci USA 103(27):10213–10217PubMedCrossRefGoogle Scholar
  36. Harris MP, Anker-Nilssen T, McCleery RH, Erikstad KE, Shaw DN, Grosbois V (2005) Effect of wintering area and climate on the survival of adult Atlantic puffins Fratercula arctica in the eastern Atlantic. Mar Ecol Prog Ser 297:283–296CrossRefGoogle Scholar
  37. Hinke JT, Salwicka K, Trivelpiece SG, Watters GM, Trivelpiece WZ (2007) Divergent responses of Pygoscelis penguins reveal a common environmental driver. Oecologia 153:845–855PubMedCrossRefGoogle Scholar
  38. IPCC (2007) Working Group I report: climate change 2007: the physical science basis (Intergovernmental Panel on Climate Change fourth assessment report). Cambridge University Press, CambridgeGoogle Scholar
  39. Jacobsen K-O, Erikstad KE, Saether B-E (1995) An experimental study of the costs of reproduction in the kittiwake Rissa tridactyla. Ecology 76:1636–1642Google Scholar
  40. Jenouvrier S, Barbraud C, Weimerskirch H (2003) Effects of climate variability on the temporal population dynamics of southern fulmars. J Anim Ecol 72:576–587CrossRefGoogle Scholar
  41. Jenouvrier S, Barbraud C, Cazelles B, Weimerskirch H (2005a) Modelling population dynamics of seabirds: importance of the effects of climate fluctuations on breeding proportions. Oikos 108:511–522CrossRefGoogle Scholar
  42. Jenouvrier S, Barbraud C, Weimerskirch H (2005b) Long-term contrasted responses to climate of two Antarctic seabird species. Ecology 86:2289–2903CrossRefGoogle Scholar
  43. Jenouvrier S, Weimerskirch H, Barbraud C, Park Y, Cazelles B (2005c) Evidence of a shift in the cyclicity of Antarctic seabird dynamics linked to climate. Proc R Soc Lond B Biol Sci 272(1566):887–895CrossRefGoogle Scholar
  44. Jenouvrier S, Barbraud C, Weimerskirch H (2006) Sea ice affects the population dynamics of Adélie penguins in Terre Adélie. Polar Biol 29:413–423CrossRefGoogle Scholar
  45. Jenouvrier SP, Caswell H et al (2009) Demographic models and IPCC climate projections predict the decline of an emperor penguin population. Proc Natl Acad Sci USA 106(6):1844–1847PubMedCrossRefGoogle Scholar
  46. Kato A, Ropert-Coudert Y, Nato Y (2002) Changes in Adélie penguin breeding populations in Lutzow-Holm Bay, Antarctica, in relation to sea ice conditions. Polar Biol 25:934–938Google Scholar
  47. Kerry KR, Clarke JR, Else GD (1993) The use of an automated weighing and recording system for the study of the biology of Adélie penguins (Pygoscelis adeliae). NIPR Symp Polar Biol 6:62–75Google Scholar
  48. Kwok R, Comiso JC (2002) Southern Ocean climate and sea ice anomalies associated with the Southern Oscillation. J Clim 15:487–501Google Scholar
  49. Le Bohec C, Durant JM, Gauthier-Clerc M, Stenseth NC, Park YH, Pradel R, Gremillet D, Gendner J-P, Le Maho Y (2008) King penguin population threatened by Southern Ocean warming. Proc Natl Acad Sci USA 105(7):2493–2497Google Scholar
  50. Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modelling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118CrossRefGoogle Scholar
  51. Marrow P, McNamara JM, Houston AI, Stevenson IR, Clutton-Brock TH (1996) State-dependent life history evolution in Soay sheep: dynamic modelling of reproductive scheduling. Philos Trans R Soc Lond B Biol Sci 351(1335):17–32PubMedCrossRefGoogle Scholar
  52. Monaghan P, Uttley JD, Burns MD, Thaine C, Blackwood J (1989) The relationship between food supply, reproductive effort and breeding success in Arctic Terns Sterna paradisea. J Anim Ecol 58:261–274CrossRefGoogle Scholar
  53. Morris WF, Doak DF (2004) Buffering of life-histories against environmental stochasticity: accounting for a spurious correlation between the variabilities of vital rates and their contributions to fitness. Am Nat 165:579–590CrossRefGoogle Scholar
  54. Navarro J, González-Solís J (2007) Experimental increase of flying costs in a pelagic seabird: effects on foraging strategies, nutritional state and chick condition. Oecologia 151:150–160PubMedCrossRefGoogle Scholar
  55. Olmastroni S, Corsolini S, Pezzo F, Focardi S, Kerry K (2000) The first 5 years of the Italian–Australian joint programme on the Adélie penguin: an overview. Ital J Zool 67:141–145CrossRefGoogle Scholar
  56. Olmastroni S, Pezzo F, Volpi V, Focardi S (2004) Effects of weather and sea ice on the reproductive performance of the Adélie penguin at Edmonson Point. CCAMLR Sci 11:99–109Google Scholar
  57. Olsson O, van der Jeugd HP (2002) Survival in king penguins Aptenodytes patagonicus: temporal and sex-specific effects of environmental variability. Oecologia 132:509–516CrossRefGoogle Scholar
  58. Oro D, Jover L, Ruiz X (1996) Influence of trawling activity on the breeding ecology of a threatened seabird, Audouin’s gull Larus audouinii. Mar Ecol Prog Ser 139:19–29CrossRefGoogle Scholar
  59. Parkinson CL (2002) Trends in the length of the Southern Ocean sea ice season, 1979–1999. Ann Glaciol 34:435–440CrossRefGoogle Scholar
  60. Pezzo F, Olmastroni S, Volpi V, Focardi S (2007) Annual variation in reproductive parameters of Adélie penguins at Edmonson Point, Victoria Land, Antarctica. Polar Biol 31:39–45Google Scholar
  61. Pfister CA (1998) Patterns of variance in stage-structured populations: evolutionary predictions and ecological implications. Proc Natl Acad Sci USA 95:213–218Google Scholar
  62. Pradel R, Hines JE, Lebreton J-D, Nichols JD (1997) Capture–recapture survival staking account of transients. Biometrics 53:60–72CrossRefGoogle Scholar
  63. Reid B (1968) An interpretation of the age structure and breeding status of an Adélie penguin population. Notornis 15:193–197Google Scholar
  64. Ribic CA, Chapman E, Fraser WR, Lawson GL, Wiebe PH (2008) Top predators in relation to bathymetry, ice and krill during austral winter in Marguerite Bay, Antarctica. Deep Sea Res Part II Top Stud Oceanogr 55(3–4):485–499CrossRefGoogle Scholar
  65. Russell RW (1999) Comparative demography and life history tactics of seabirds: implications for conservation and marine monitoring. Am Fish Soc Sympos 23:51–76Google Scholar
  66. Saether B-E, Bakke O (2000) Avian life history variation and contribution of demographic traits to the population growth rate. Ecology 81:642–653Google Scholar
  67. Sladen WJL (1978) Sexing penguins by cloacascope. Int Zoo Yearb 18:77–80CrossRefGoogle Scholar
  68. Smith RC, Ainley DG, Baker K, Domack E, Emslie SD, Fraser B, Kennet J, Leventer A, Mosley-Thompson E, Stammerjohn S, Vernet M (1999) Marine ecosystem sensitivity to climate change. Bioscience 49:393–404CrossRefGoogle Scholar
  69. Smith RC, Baker KS, Dierssen HM, Stammerjohn SE, Vernet M (2001) Variability of primary production in an Antarctic marine ecosystem as estimated using a multi-scale sampling strategy. Am Zool 41:40–56CrossRefGoogle Scholar
  70. Smith WOK, Ainley DG, Cattaneo-Vietti R (2007) Trophic interactions within the Ross Sea continental shelf ecosystem. Phil Trans R Soc B 362:95–111Google Scholar
  71. Stearns SC (1992) The evolution of life histories. Chapman and Hall, OxfordGoogle Scholar
  72. Tavecchia G, Minguez E, De Leon A, Louzao M, Oro D (2008) Living close, doing differently: small-scale asynchrony in demographic parameters in two species of seabirds. Ecology 89(1):77–85Google Scholar
  73. Testa JW, Oelhert G, Ainley DG, Bengston JL, Siniff DB, Laws RM, Rounsevell D (1991) Temporal variability in Antarctic marine ecosystems: periodic fluctuations in the phocid seals. Can J Fish Aquat Sci 48:631–639Google Scholar
  74. Trathan PN, Forcada J, Murphy EJ (2007) Environmental forcing and Southern Ocean marine predator populations: effects of climate change and variability. Philos Trans R Soc Lond B 362(1488):2351–2365Google Scholar
  75. Turner (2004) The El Nino–Southern Oscillation and Antarctica—review. Int J Climatol 24:1–31Google Scholar
  76. Tynan C (1998) Ecological importance of the southern boundary of the Antarctic circumpolar current. Nature 392:708–710CrossRefGoogle Scholar
  77. Weimerskirch H (2002) Seabirds demography and its relationship with the marine environment. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, New YorkGoogle Scholar
  78. Williams TD (1995) The penguins. Oxford University Press, OxfordGoogle Scholar
  79. Wilson PR, Ainley DG, Nur N, Jacobs SS, Barton KJ, Ballard G, Comiso JC (2001) Adélie penguin population change in the pacific sector of Antarctica: relation to sea ice extent and the Antarctic circumpolar current. Mar Ecol Prog Ser 213:301–309CrossRefGoogle Scholar
  80. Zwally HJ, Comiso JC, Parkinson CL, Cavalieri DJ, Gloersen P (2002) Variability of Antarctic sea ice 1979–1998. J Geophys Res 107:C5Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Tosca Ballerini
    • 1
    • 3
  • Giacomo Tavecchia
    • 2
  • Silvia Olmastroni
    • 1
  • Francesco Pezzo
    • 1
  • Silvano Focardi
    • 1
  1. 1.Dipartimento di Scienze Ambientali “G. Sarfatti”Università degli Studi di SienaSienaItaly
  2. 2.Institut Mediterrani d’Estudis Avançats (IMEDEA), CSIC-UIBEsporlesSpain
  3. 3.Center for Coastal Physical OceanographyOld Dominion UniversityNorfolkUSA

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