Skip to main content

Advertisement

Log in

A comprehensive review of the phenology of Pygoscelis penguins

  • Review
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Phenology, the study of stages within the life cycles of plants and animals, has served as a proxy for weather and climate throughout human history, but has only recently become its own field of environmental science. Phenological constraints are particularly demanding in avian species because of the necessity of matching chick provisioning with high food abundance, while allocating time for migration. Within avian species, seabird phenology is of particular interest because many seabird species exhibit colonial breeding behaviour. Penguins, representing roughly 90 % of the biomass in the Southern Ocean, are well studied in the context of population dynamics, prey abundance, and phenology. Here I review the annual cycles of Pygoscelis penguins, a genus including gentoo (Pygoscelis papua), chinstrap (Pygoscelis antarctica), and Adélie (Pygoscelis adeliae) penguins, to better understand what is known about their phenology, what causes known changes, and how their phenology influences fitness. Major differences exist between species, particularly in relation to winter migration, incubation shifts, and the timing of breeding. Even with the numerous studies examining phenology in Pygoscelis penguins, large gaps in our understanding of plasticity in the annual cycle remain. In particular, certain phases are neglected because they are logistically difficult to record or have erroneously been ignored. In addition, temporally, large gaps exist in our understanding of phenology, where studies have not been updated in over 20 years at a particular field site. Because phenology does vary greatly between years, depending on the colony, when possible, researchers should strive to update phenological records by recording the dates of phases each year.

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

Similar content being viewed by others

References

  • Abbott CC (1860) The penguins of the Falkland Islands. Ibis 2:336–338

    Article  Google Scholar 

  • Ainley DG (1978) Activity patterns and social behavior of non-breeding Adelie penguins. Condor 80:138–146

    Article  Google Scholar 

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

    Google Scholar 

  • Ainley DG, LeResche RE (1973) The effects of weather and ice conditions on breeding in Adelie penguins. Condor 75:235–255

    Article  Google Scholar 

  • Ainley DG, Schlatter RP (1972) Chick raising ability in Adélie penguins. Auk 89:559–566

    Google Scholar 

  • Ainley DG, LeResche RE, Sladen WJL (1983) Breeding biology of the Adelie penguin. University of California Press, Berkeley

    Google Scholar 

  • Alcock J (1993) Animal behavior: an evolutionary approach. Sinauer Associates, Sunderland

    Google Scholar 

  • Ancel A, Beaulieu M, Gilbert C (2013) The different breeding strategies of penguins: a review. C R Biol 336:1–12

    Article  PubMed  Google Scholar 

  • Angelier F, Bost CA, Giraudeau M, Bouteloup G, Dano S, Chastel O (2008) Corticosterone and foraging behavior in a diving seabird: the Adélie penguin, Pygoscelis adeliae. Gen Comp Endocrinol 156:134–144

    Article  CAS  PubMed  Google Scholar 

  • Ashmole NP (1963) The regulation of numbers of tropical oceanic birds. Ibis 103b:458–473

    Article  Google Scholar 

  • Bagshawe T (1938) Notes on the habits of the gentoo and ringed or Antarctic penguins. Trans Zool Soc Lond 24:185–306

    Article  Google Scholar 

  • Barbosa A, Moreno J, Potti J, Merino S (1997) Breeding group size, nest position and breeding success in the chinstrap penguin. Polar Biol 18:410–414

    Article  Google Scholar 

  • Barbraud C, Weimerskirch H (2006) Antarctic birds breed later in response to climate change. Proc Natl Acad Sci USA 103:6248–6251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beaulieu M, Dervaux A, Thierry A-M, Lazin D, Le Maho Y, Ropert-Coudert Y, Spée M, Raclot T, Ancel A (2010) When sea-ice clock is ahead of Adélie penguins clock. Funct Ecol 24:93–102

    Article  Google Scholar 

  • Beebee TJC (1995) Amphibian breeding and climate. Nature 374:219–220

    Article  CAS  Google Scholar 

  • Bird Life International (2015) Species factsheet: Pygoscelis antarcticus. http://www.birdlife.org. 06 May 2015

  • Biuw M, Lydersen C, Nico de Bruyn PJ, Arriola A, Hofmeyr GGJ, Kritzinger P, Kovacs KM (2009) Long-range migration of a chinstrap penguin from Bouvetøya to Montagu Island, South Sandwich Islands. Antarct Sci 22:157

    Article  Google Scholar 

  • Boersma PD (1976) An ecological and behavioral study of the Galapagos penguin. Living Bird 15:43–93

    Google Scholar 

  • Boersma PD (2008) Penguins as marine sentinels. Bioscience 58:597–607

    Article  Google Scholar 

  • Boersma PD, Rebstock GA (2014) Climate change increases reproductive failure in Magellanic penguins. PLoS ONE 9:e85602

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Borboroglu PG, Boersma PD (2013) Penguins: natural history and conservation. University of Washington Press, Seattle

    Google Scholar 

  • Bost CA, Clobert J (1992) Gentoo penguin Pygoscelis papua: factors affecting the process of laying a replacement clutch. Acta Oecol 13:593–605

    Google Scholar 

  • Bost CA, Jouventin P (1990a) Evolutionary ecology of gentoo penguins (Pygoscelis papua). In: Davis LS, Darby JT (eds) Penguin biology. Penguin Biology Academic, San Diego, pp 85–112

    Google Scholar 

  • Bost CA, Jouventin P (1990b) Laying asynchrony in Gentoo penguins on Crozet Islands: causes and consequences. Ornis Scand 21:63–70

    Article  Google Scholar 

  • Bost CA, Jouventin P (1991) The breeding performance of the Gentoo penguin Pygoscelis papua at the northern edge of its range. Ibis 133:14–25

    Article  Google Scholar 

  • Both C, Van Turnhout CAM, Bijlsma RG, Siepel H, Van Strien AJ, Foppen RPB (2009) Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc R Soc B Biol Sci 277:1259–1266

    Article  Google Scholar 

  • Carlini AR, Coria NR, Santos MM, Bujan SM (2005) The effect of Chinstrap penguins on the breeding performance of Adélie penguins. Folia Zool 54:147–158

    Google Scholar 

  • Cendron J (1953) La mue du manchot Adélie adulte. Alauda, Amsterdam

    Google Scholar 

  • Chambers LE, Altwegg R, Barbraud C, Barnard P, Beaumont LJ, Crawford RJM, Durant JM, Hughes L, Keatley MR, Low M (2013) Phenological changes in the Southern Hemisphere. PLoS ONE 8:e75514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chappell MA, Shoemaker VH, Janes DN, Bucher TL, Maloney SK (1993) Diving behavior during foraging in breeding Adélie penguins. Ecology 74:1204–1215

    Article  Google Scholar 

  • Charnov EL, Krebs JR (1974) On clutch-size and fitness. Ibis 116:217–219

    Article  Google Scholar 

  • Chesalin M, Naveen R, Lynch H, Bullock I, Rider M, Miller A, Forrest S, Dagit R, Dykyy I, Timofeyev V (2009) Long-term changes in populations of seabirds on Petermann Island and surrounding islands in Graham Land, Antarctic Peninsula. Mar Ecol J VIII:5–13

    Google Scholar 

  • Clarke WE (1906) Ornithological results of the Scottish National Antarctic Expedition—II. On the birds of the South Orkney Islands. Ibis 48:145–187

    Article  Google Scholar 

  • Clarke J, Kerry K, Irvine L, Phillips B (2002) Chick provisioning and breeding success of Aélie penguins at Béchervaise Island over eight successive seasons. Polar Biol 25:21–30

    Article  Google Scholar 

  • Clarke J, Kerry K, Fowler C, Lawless R, Eberhard S, Murphy R (2003) Post-fledging and winter migration of Adélie penguins Pygoscelis adeliae in the Mawson region of East Antarctica. Mar Ecol Prog Ser 248:267–278

    Article  Google Scholar 

  • Cobley ND, Shears JR (1999) Breeding performance of gentoo penguins (Pygoscelis papua) at a colony exposed to high levels of human disturbance. Polar Biol 21:355–360

    Article  Google Scholar 

  • Conroy JWH, Darling OHS, Smith HG (1975a) The annual cycle of the chinstrap penguin Pygoscelis antarctica on Signy Island, South Orkney Islands. In: Stonehouse B (ed) The biology of penguins. Macmillan, London, pp 353–362

    Chapter  Google Scholar 

  • Conroy JWH, White MG, Furse JR, Bruce G (1975b) Observations on the breeding biology of the chinstrap penguin, Pygoscelis antarctica, at Elephant Island, South Shetland Islands. Ibis 127:84–99

    Google Scholar 

  • Cowan AN (1979) Ornithological studies at Casey, Antarctica, 1977–1978. Aust J Ecol 4:69–90

    Google Scholar 

  • Crawford RJM, Cooper J, Du Toit M, Greyling MD, Hanise B, Holness CL, Keith DG, Nel JL, Petersen SL, Spencer K (2003) Population and breeding of the gentoo penguin Pygoscelis papua at Marion Island, 1994/95–2002/03. Afr J Mar Sci 25:463–474

    Article  Google Scholar 

  • Crawford RJM, Makhado AB, Upfold L, Dyer BM (2008) Mass on arrival of rockhopper penguins at Marion Island correlated with breeding success. Afr J Mar Sci 30:185–188

    Article  Google Scholar 

  • Crick HQP, Sparks TH (1999) Climate change related to egg-laying trends. Nature 399:423–423

    Article  CAS  Google Scholar 

  • Croxall J, Davis L (1999) Penguins: paradoxes and patterns. Mar Ornithol 27:1–12

    Google Scholar 

  • Croxall JP, Prince PA (1979) Antarctic seabird and seal monitoring studies. Polar Rec 19:573–595

    Article  Google Scholar 

  • Croxall JP, McCann TS, Prince PA, Rothery P (1988) Reproductive performance of seabirds and seals at South Georgia and Signy Island, South Orkney Islands, 1976–1987: Implications for Southern Ocean monitoring studies. Antarctic Ocean and resources variability. In: Sahrhage D (ed) Antarctic ocean and resources variability. Springer, New York, pp 261–285

    Chapter  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 

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

    Article  CAS  PubMed  Google Scholar 

  • Croxall JP, Butchart SHM, Lascelles B, Stattersfield AJ, Sullivan B, Symes A, Taylor P (2012) Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv Int 22:1–34

    Article  Google Scholar 

  • Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–293

    Article  Google Scholar 

  • Davis LS (1982a) Creching behaviour of Adelie penguin chicks (Pygoscelis adeliae). N Z J Zool 9:279–285

    Article  Google Scholar 

  • Davis LS (1982b) Timing of nest relief and its effect on breeding success in Adelie penguins (Pygoscelis adeliae). Condor 84:178–183

    Article  Google Scholar 

  • Davis LS, Boersma PD (1996) Satellite telemetry of the winter migration of Adélie penguins (Pygoscelis adeliae). Polar Biol 16:221–225

    Article  Google Scholar 

  • Davis LS, McCaffrey FT (1986) Survival analysis of eggs and chicks of Adélie penguins (Pygoscelis adeliae). Auk 103:379–388

    Google Scholar 

  • Davis L, Harcourt R, Bradshaw C (2001) The winter migration of Adelie penguins breeding in the Ross Sea sector of Antarctica. Polar Biol 24:593–597

    Article  Google Scholar 

  • Despin B (1972) Note préliminaire sur Le Manchot Papou Pygoscelis papua de l’Ile de la Possession (Archipel Crozet). L’Oiseau et RFO 42:69–83

    Google Scholar 

  • Downes MC, Ealey EHM, Gwynn AM, Young PS (1959) The birds of Heard Island. Antarctic Division, Department of External Affairs, ANARE Reports Series B, vol 1, pp 7–34

  • Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252

    Google Scholar 

  • Ducklow HW, Baker K, Martinson DG, Quetin LB, Ross RM, Smith RC, Stammerjohn SE, Vernet M, Fraser W (2007) Marine pelagic ecosystems: the west Antarctic Peninsula. Philos Trans R Soc B 362:67–94

    Article  Google Scholar 

  • Dunn P (2004) Breeding dates and reproductive performance. Adv Ecol Res 35:69–87

    Article  Google Scholar 

  • Dunn MJ, Silk JRD, Trathan PN (2011) Post-breeding dispersal of Adélie penguins (Pygoscelis adeliae) nesting at Signy Island, South Orkney Islands. Polar Biol 34:205–214

    Article  Google Scholar 

  • Durant JM, Hjermann DØ, Anker-Nilssen T, Beaugrand G, Mysterud A, Pettorelli N, Stenseth NC (2005) Timing and abundance as key mechanisms affecting trophic interactions in variable environments. Ecol Lett 8:952–958

    Article  Google Scholar 

  • Durant JM, Hjermann D, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283

    Article  Google Scholar 

  • Emmerson L, Pike R, Southwell C (2011) Reproductive consequences of environment-driven variation in Adélie penguin breeding phenology. Mar Ecol Prog Ser 440:203–216

    Article  Google Scholar 

  • Falla RA (1937) Birds. B.A.N.Z.A.R. Expedition Committee, Adelaide

    Google Scholar 

  • Fargallo JA, Polo V, De Neve L, Martín J, Dávila JA, Soler M (2006) Hatching order and size-dependent mortality in relation to brood sex ratio composition in chinstrap penguins. Behav Ecol 17:772–778

    Article  Google Scholar 

  • Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691

    Article  CAS  PubMed  Google Scholar 

  • Forrest J, Miller-Rushing AJ (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philos Trans R Soc B 365:3101–3112

    Article  Google Scholar 

  • Franks SJ, Weis AE (2008) A change in climate causes rapid evolution of multiple life-history traits and their interactions in an annual plant. J Evol Biol 21:1321–1334

    Article  CAS  PubMed  Google Scholar 

  • Fraser WR, Trivelpiece WZ (1996) Factors controlling the distribution of seabirds: winter-summer heterogeneity in the distribution of adélie penguin populations. In: Ross RM, Hofmann EE, Quetin LB (eds) Foundations for ecological research west of the Antarctic Peninsula. American Geophysical Union, Washington, pp 257–272

    Chapter  Google Scholar 

  • Furse C (1979) Elephant Island: an Antarctic expedition. Harrell Books, Anacortes

    Google Scholar 

  • Gain L (1914) Oiseaux antarctiques. Deuxieme Expédition Antarctique Française, 1908–10. Sciences Naturelles, Paris, pp 1–200

  • Gaston AJ (2004) Seabirds: a natural history. Yale University Press, New Haven

    Google Scholar 

  • Ghys MI, Rey AR, Schiavini A (2008) Population trend and breeding biology of gentoo penguin in Martillo Island, Tierra Del Fuego, Argentina. Waterbirds. Int J Waterbird Biol 31:625–631

    Google Scholar 

  • Gienapp P, Lof M, Reed TE, McNamara J, Verhulst S, Visser M (2013) Predicting demographically sustainable rates of adaptation: can great tit breeding time keep pace with climate change? Philos Trans R Soc B 368:20120289

    Article  Google Scholar 

  • Groscolas R, Jallageas M, Goldsmith A, Assenmacher I (1986) The endocrine control of reproduction and molt in male and female emperor (Aptenodytes forsteri) and adelie (Pygoscelis adeliae) penguins: i. Annual changes in plasma levels of gonadal steroids and LH. Gen Comp Endocrinol 62:43–53

    Article  CAS  PubMed  Google Scholar 

  • Gwynn AM (1953) The egg-laying and incubation periods of rockhopper, macaroni and gentoo penguins. Antarctic Division, Department of External Affairs, Commonwealth of Australia, Melbourne

    Google Scholar 

  • Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916

    Article  CAS  PubMed  Google Scholar 

  • Hinke JT, Polito MJ, Reiss CS, Trivelpiece SG, Trivelpiece WZ (2012) Flexible reproductive timing can buffer reproductive success of Pygoscelis spp. penguins in the Antarctic Peninsula region. Mar Ecol Prog Ser 454:91–104

    Article  Google Scholar 

  • Holdgate MW (1963) Observations of birds and seals at Anvers Island, Palmer Archipelago, in 1956–57. Br Antarct Surv Bull 2:45–51

    Google Scholar 

  • Hunt GL, Stabeno PJ (2002) Climate change and the control of energy flow in the southeastern Bering Sea. Prog Oceanogr 55:5–22

    Article  Google Scholar 

  • IUCN (2015) The IUCN red list of threatened species. Version 2015-3. http://www.iucnredlist.org. Accessed 9 Sept 2014

  • Jablonski B (1987) Diurnal pattern of changes in the number of penguins on land and the estimation of their abundance (Admiralty Bay, King George I., South Shetland Islands). Acta Zool Crac 30:97–118

    Google Scholar 

  • Jenouvrier S (2013) Impacts of climate change on avian populations. Glob Change Bio 19:2036–2057

    Article  Google Scholar 

  • Johnstone GW, Brown DA, Lugg DJ (1973) The biology of the Vestfold Hills, Antarctica. Antarctic Division, Department of Science, Tasmania

    Google Scholar 

  • Kerry K, Clarke J, Else G (1993) The use of an automated weighing and recording system for the study of the biology of adelie penguins (Pygoscelis adeliae) (14th Symposium on Polar Biology). Proc NIPR Symp Polar Biol 6:62–75

    Google Scholar 

  • Körner C, Basler D (2010) Phenology under global warming. Science 327:1461–1462

    Article  PubMed  Google Scholar 

  • Korotkevich ES (1964) Observations on birds during the first wintering of the Soviet Antarctic expedition, 1956–1957. Sov Antarct Exped Inf Bull 1:149–152

    Google Scholar 

  • Krebs JR, Davies NB (2009) Behavioural ecology: an evolutionary approach. Wiley, New York

    Google Scholar 

  • Lack D (1954) The natural regulation of animal numbers. Clarendon Press, Oxford

    Google Scholar 

  • Lambrechts MM, Blondel J, Maistre M, Perret P (1997) A single response mechanism is responsible for evolutionary adaptive variation in a bird’s laying date. Proc Natl Acad Sci USA 94:5153–5155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LaRue MA, Ainley DG, Swanson M, Dugger KM, Phil O, Lyver B, Barton K, Ballard G (2013) Climate change winners: receding ice fields facilitate colony expansion and altered dynamics in an Adélie penguin metapopulation. PLoS ONE 8:e60568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LeResche RE, Sladen WJL (1970) Establishment of pair and breeding site bonds by young known-age adelie penguins (Pygoscelis adeliae). Anim Behav 18:517–526

    Article  Google Scholar 

  • Lescroël A, Bajzak C, Bost C-A (2009) Breeding ecology of the gentoo penguin Pygoscelis papua at Kerguelen Archipelago. Polar Biol 32:1495–1505

    Article  Google Scholar 

  • Levick GM (1914) Antarctic penguins: a study of their social habits. McBride Nast, New York

    Book  Google Scholar 

  • Liebezeit JR, Gurney KEB, Budde M, Zack S, Ward D (2014) Phenological advancement in arctic bird species: relative importance of snow melt and ecological factors. Polar Biol 37:1309–1320

    Article  Google Scholar 

  • Lishman G (1985) The comparative breeding biology of Adélie and chinstrap penguins Pygoscelis adeliae and P. antarctica at Signy Island, South Orkney Islands. Ibis 127:84–99

    Article  Google Scholar 

  • Lynch HJ, LaRue MA (2014) First comprehensive census of the Adélie penguin. Auk 131:457–466

    Article  Google Scholar 

  • Lynch HJ, Naveen R, Fagan WF (2008) Censuses of penguin, blue-eyed shag Phalacrocorax atriceps and southern giant petrel Macronectes giganteus populations on the Antarctic Peninsula, 2001–2007. Mar Ornithol 36:83–97

    Google Scholar 

  • Lynch HJ, Fagan WF, Naveen R (2009) Population trends and reproductive success at a frequently visited penguin colony on the western Antarctic Peninsula. Polar Biol 33:493–503

    Article  Google Scholar 

  • Lynch HJ, Naveen R, Trathan PN, Fagan WF (2012a) Spatially integrated assessment reveals widespread changes in penguin populations on the Antarctic Peninsula. Ecology 93:1367–1377

    Article  PubMed  Google Scholar 

  • Lynch HJ, Fagan WF, Naveen R, Trivelpiece SG, Trivelpiece WZ (2012b) Differential advancement of breeding phenology in response to climate may alter staggered breeding among sympatric pygoscelid penguins. Mar Ecol Prog Ser 454:135–145

    Article  Google Scholar 

  • Lyver P et al (2014) Trends in the breeding population of Adélie penguins in the Ross Sea, 1981–2012: a coincidence of climate and resource extraction effects. PLoS ONE. doi:10.1371/journal.pone.0091188

    PubMed  PubMed Central  Google Scholar 

  • Makushok VM (1959) Biological report for 1958. Rept Third Continental Exped 5:115–124

    Google Scholar 

  • Marchant S, Higgins PJ (1990) Handbook of Australian, New Zealand and Antarctic birds, vol 1. Oxford University Press, Oxford

    Google Scholar 

  • Martin TE (1987) Food as a limit on breeding birds: a life history perspective. Ann Rev Ecol Syst 18:453–487

    Article  Google Scholar 

  • Martín J, De Neve L, Polo V, Fargallo J, Soler M (2006) Health-dependent vulnerability to predation affects escape responses of unguarded chinstrap penguin chicks. Behav Ecol Sociobiol 60:778–784

    Article  Google Scholar 

  • Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kübler K, Bissolli P, Og Braslavská, Briede A (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1969–1976

    Article  Google Scholar 

  • Metcalf CJE, Mitchell-Olds T (2009) Life history in a model system: opening the black box with Arabidopsis thaliana. Ecol Lett 12:593–600

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller AK, Trivelpiece WZ (2008) Chinstrap penguins alter foraging and diving behavior in response to the size of their principle prey, Antarctic krill. Mar Biol 154:201–208

    Article  Google Scholar 

  • Montevecchi WA (1993) Birds as indicators of change in marine prey stocks. Springer, New York

    Book  Google Scholar 

  • Moreno J, De Leon A, Fargallo JA, Moreno E (1998) Breeding time, health and immune response in the chinstrap penguin Pygoscelis antarctica. Oecologia 115:312–319

    Article  Google Scholar 

  • Müller-Schwarze D, Müller-Schwarze C (1980) Display rate and speed of nest relief in Antarctic pygoscelid penguins. Auk 97:825–831

    Google Scholar 

  • Murphy RC (1936) Oceanic birds of South America, vol 1. American Museum of Natural History, New York

    Google Scholar 

  • Newton I (2010) The migration ecology of birds. Academic Press, Massachusetts

    Google Scholar 

  • Nicol S, Clarke J, Romaine SJ, Kawaguchi S, Williams G, Hosie GW (2008) Krill (Euphausia superba) abundance and Adélie penguin (Pygoscelis adeliae) breeding performance in the waters off the Béchervaise Island colony, East Antarctica in 2 years with contrasting ecological conditions. Deep Sea Res Part II 55:540–557

    Article  Google Scholar 

  • Nudel’man AV (1966) Soviet Antarctic expeditions 1959–1961. Israel Program for Scientific Translations, Jerusalem

  • Oelke H (1975) Breeding behaviour and success in a colony of Adélie penguins Pygoscelis adeliae) at Cape Crozier, Antarctica. The biology of penguins. Macmillan, London

    Google Scholar 

  • Olmastroni S, Corsolini S, Pezzo F, Focardi S, Kerry K (2000) The first five years of the Italian–Australian joint programme on the Adélie penguin: an overview. Ital J Zool 67:141–145

    Article  Google Scholar 

  • 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, Ross Sea. CCAMLR Sci 11:99–109

    Google Scholar 

  • Otley HM, Clausen AP, Christie DJ, Pütz K (2005) Aspects of the breeding biology of the gentoo penguin Pygoscelis papua at Volunteer Beach, Falkland Islands, 2001/02. Mar Ornithol 32:167–171

    Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  CAS  PubMed  Google Scholar 

  • Paulian P (1953) Pinnipèdes, cétacés, oiseaux des Iles Kerguelen et Amsterdam: mission Kerguelen 1951. Institut Scientifique de Madagascar 8:111–234

    Google Scholar 

  • Penney RL (1968) Molt in the Adelie penguin. Auk 84:61–71

    Article  Google Scholar 

  • Penney RL, Emlen J (1967) Further experiments on distance navigation in the adelie penguin Pygoscelis adeliae. Ibis 109:99–109

    Article  Google Scholar 

  • Penteriani V, Vinuela J, Belliure J, Bustamante J, Ferrer M (2003) Causal and functional correlates of brood amalgamation in the chinstrap penguin Pygoscelis antarctica : parental decision and adult aggressiveness. Polar Biol 26:538–544

    Article  Google Scholar 

  • Perrins CM (1970) The timing of birds breeding seasons. Ibis 112:242–255

    Article  Google Scholar 

  • Polito MJ, Lynch HJ, Naveen R, Emslie SD (2011) Stable isotopes reveal regional heterogeneity in the pre-breeding distribution and diets of sympatrically breeding Pygoscelis spp. penguins. Mar Ecol Prog Ser 421:265–277

    Article  Google Scholar 

  • Potts GR, Coulson JC, Deans IR (1980) Population dynamics and breeding success of the shag, Phalacrocorax aristotelis, on the Farne Islands, Northumberland. J Anim Ecol 49:465–484

    Article  Google Scholar 

  • Pryor ME (1968) The Avifauna of Haswell Island, Antarctica. Antarctic Bird Studies. Am Geophys Union 12:57–82

    Google Scholar 

  • Quetin LB, Ross RM (2001) Environmental variability and its impact on the reproductive cycle of Antarctic krill. Am Zool 41:74–89

    Google Scholar 

  • Quintana RD, Cirelli V (2000) Breeding dynamics of a gentoo penguin Pygoscelis papua population at Cierva Point, Antarctic Peninsula. Mar Ornithol 28:29–35

    Google Scholar 

  • Rand RW (1954) Notes on the birds of Marion Island. Ibis 96:173–206

    Article  Google Scholar 

  • Rand RW (1955) The penguins of Marion Island. Ostrich 26:57–69

    Article  Google Scholar 

  • Reed TE, Jenouvrier S, Visser ME (2013a) Phenological mismatch strongly affects individual fitness but not population demography in a woodland passerine. J Anim Ecol 82:131–144

    Article  PubMed  Google Scholar 

  • Reed TE, Grotan V, Jenouvrier S, Saether BE, Visser ME (2013b) Population growth in a wild bird ss buffered against phenological mismatch. Science 340:488–491

    Article  CAS  PubMed  Google Scholar 

  • Reid BE (1964) The Cape Hallett Adelie penguin rookery-its size, composition, and structure. Dominion Museum, Wellington

    Google Scholar 

  • Reilly PN, Kerle JA (1981) A study of the gentoo penguin. Notornis 28:189–202

    Google Scholar 

  • Richdale LE (1957) A population study of penguins. Clarendon Press, Oxford

    Google Scholar 

  • Roberts B (1940) The breeding behaviour of penguins: with special reference to Pygoscelis papua (Forster). Order of the Trustees of the British Museum, London

    Google Scholar 

  • Rodary D, Wienecke BC, Bost CA (2000) Diving behaviour of Adélie penguins (Pygoscelis adeliae) at Dumont D’Urville, Antarctica: nocturnal patterns of diving and rapid adaptations to changes in sea-ice condition. Polar Biol 23:113–120

    Article  Google Scholar 

  • Rootes DM (1988) The status of birds at Signy Island, South Orkney Islands. Br Antarct Surv B 80:87–119

    Google Scholar 

  • Sapin-Jaloustre J, Bourlière F (1952) Incubation et développement du poussin chez le Manchot Adélie Pygoscelis adeliae. Alauda Rev Int Ornithd 2:65–82

    Google Scholar 

  • Sladen WJ (1953) The Adelie penguin. Nature 171:952–955

    Article  CAS  PubMed  Google Scholar 

  • Sladen W (1958) The pygoscelid penguins. I: Methods of study; II: The Adélie penguin. Falkland Is Depend Surv Sci Rep 1–97

  • Spée M, Beaulieu M, Dervaux A, Chastel O, Le Maho Y, Raclot T (2010) Should I stay or should I go? Hormonal control of nest abandonment in a long-lived bird, the Adélie penguin. Horm Behav 58:762–768

    Article  PubMed  CAS  Google Scholar 

  • Spellerberg IF (1971) Arrival and departure of birds at McMurdo Sound, Antarctica. Emu 71:167–171

    Article  Google Scholar 

  • Spurr E (1975) Breeding of the Adélie penguin Pygoscelis adeliae at Cape Bird. Ibis 117:324–338

    Article  Google Scholar 

  • Stammerjohn SE, Martinson DG, Smith RC, Yuan X, Rind D (2008) Trends in Antarctic annual sea ice retreat and advance and their relation to El Niño–Southern Oscillation and Southern Annular Mode variability. J Geophy Res 113:C03S90. doi:10.1029/2007JC004269

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Stonehouse B (1963) Observations on Adélie penguins (Pygoscelis adeliae) at Cape Royds, Antarctica. In: Proceedings XIIIth international ornithological congress, pp 766–779

  • Taylor RH (1962) The Adélie penguin Pygoscelis adeliae at Cape Royds. Ibis 104:176–204

    Article  Google Scholar 

  • Taylor JR (1985) Ontogeny of thermoregulation and energy metabolism in pygoscelid penguin chicks. J Comp Physiol 155:615–627

    Article  CAS  Google Scholar 

  • Taylor JRE (1986) Thermal insulation of the down and feathers of pygoscelid penguin chicks and the unique properties of penguin feathers. Auk 103:160–168

    Google Scholar 

  • Trathan PN, Garcia-BorborogluP Boersma D, Bost CA, Crawford RJM, Crossin GT, Cuthbert RJ, Dann P, Davis LS, De la Puente S (2014) Pollution, habitat loss, fishing, and climate change as critical threats to penguins. Conserv Biol 29:31–41

    Article  PubMed  Google Scholar 

  • Trivelpiece WZ, Trivelpiece SG (1990) Courtship period of Adélie, gentoo and chinstrap penguins in Penguin Biology. Academic Press, San Diego, pp. 113–127

  • Trivelpiece W, Volkman NJ (1979) Nest-site competition between Adelie and Chinstrap penguins: an ecological interpretation. Auk 96:675–681

    Google Scholar 

  • Trivelpiece WZ, Trivelpiece SG, Volkman NJ (1984) Further insights into nest-site competition between Adelie and chinstrap penguins. Auk 101:882–884

    Article  Google Scholar 

  • Trivelpiece WZ, Trivelpiece SG, Volkman NJ (1987) Ecological segregation of Adelie, gentoo, and chinstrap penguins at King George Island, Antarctica. Ecology 68:351–361

    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. Proc Natl Acad Sci USA 108:7625–7628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tulloch A (1916) Macquarie Island penguins. Emu 16:92–96

    Article  Google Scholar 

  • Vaughan DG, Marshall GJ, Connolley WM, Parkinson C, Mulvaney R, Hodgson DA, King JC, Pudsey CJ, Turner J (2003) Recent rapid regional climate warming on the Antarctic Peninsula. Clim Change 60:243–274

    Article  Google Scholar 

  • Villanueva C, Walker BG, Bertellotti M (2012) A matter of history: effects of tourism on physiology, behaviour and breeding parameters in Magellanic penguins (Spheniscus magellanicus) at two colonies in Argentina. J Ornithol 153:219–228

    Article  Google Scholar 

  • Viñuela J, Moreno J, Carrascal LM, Sanz JJ, Amat JA, Ferrer M, Belliure J, Cuervo J (1996) The effect of hatching date on parental care, chick growth, and chick mortality in the chinstrap penguin Pygoscelis antarctica. J Zool 240:51–58

    Article  Google Scholar 

  • Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B Biol Sci 272:2561–2569

    Article  Google Scholar 

  • Visser ME, Caro SP, Van Oers K, Schaper SV, Helm B (2010) Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philos Trans R Soc B 365:3113–3127

    Article  CAS  Google Scholar 

  • Vleck CM, Vertalino N, Vleck D, Bucher TL (2000) Stress, corticosterone, and heterophil to lymphocyte ratios in free-living Adélie penguins. Condor 102:392–400

    Article  Google Scholar 

  • Volkman NJ, Trivelpiece W (1980) Growth in pygoscelid penguin chicks. J Zool Lond 191:521–530

    Article  Google Scholar 

  • Walker BG, Boersma P, Wingfield JC (2005) Physiological and behavioral differences in Magellanic penguin chicks in undisturbed and tourist-visited locations of a colony. Conserv Biol 19:1571–1577

    Article  Google Scholar 

  • Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  CAS  PubMed  Google Scholar 

  • Watanuki Y (1993) Mortality of eggs and nest attendance pattern in Adelie penguins in Lutzow–Holm Bay. 日本鳥学会誌 42:1–8

    Google Scholar 

  • Whitehead M, Johnstone G, Burton H (1990) Annual fluctuations in productivity and breeding success of Adélie penguins and fulmarine petrels in Prydz Bay, East Antarctica. Antarct Ecosyst. Springer, Berlin, pp 214–223

  • Wilczek AM, Burghardt LT, Cobb AR, Cooper MD, Welch SM, Schmitt J (2010) Genetic and physiological bases for phenological responses to current and predicted climates. Philos Trans R Soc B 365:3129–3147

    Article  CAS  Google Scholar 

  • Williams AJ (1979) Factors affecting time of breeding of Gentoo penguins Pygoscelis papua at Marion Island. Proc Symp Birds Sea Shore 1:979

    Google Scholar 

  • Williams AJ (1980) Aspects of the breeding biology of the Gentoo penguin, Pygoscelis papua [at Marion Island in the Prince Edward archipelago Antarctic areas; Atlantic and Indian Oceans; chick mortality, food availability. Gerfaut 70:283–295

    Google Scholar 

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

    Article  Google Scholar 

  • Wilson D (2009) Causes and benefits of chick aggregations in penguins. Auk 126:688–693

    Article  Google Scholar 

  • Wilson RP, Culik BM, Kosiorek P, Adelung D (1998) The over-winter movements of a chinstrap penguin (Pygoscelis antarctica). Polar Rec 34:107–112

    Article  Google Scholar 

  • Wingfield JC, Hahn TP, Levin R, Honey P (1992) Environmental predictability and control of gonadal cycles in birds. J Exp Zool 261:214–231

    Article  Google Scholar 

  • Winkler DW, Dunn PO, McCulloch CE (2002) Predicting the effects of climate change on avian life-history traits. Proc Natl Acad Sci USA 99:13595–13599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeates GW (1968) Studies on the Adelie penguin at cape Royds 1964–65 and 1965–66. N Z J Mar Freshw Res 2:472–496

    Article  Google Scholar 

  • Yeates GW (1971) Diurnal activity in the Adelie penguin (Pygoscelis adeliae) at Cape Royds, Antarctica. J Nat Hist 5:103–112

    Article  Google Scholar 

  • Zinderen Bakker EM, Winterbottom JM, Dyer RA (1971) Marion and Prince Edward islands: report on the South African Biological and Geological Expedition 1965–1966. CRC Press, Florida

    Google Scholar 

Download references

Acknowledgments

I gratefully acknowledge Drs Tom Hart, Chris Perrins, and Dora Biro for comments on an earlier version of this manuscript and Quark Expeditions and Penguin Lifelines funders for their financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Caitlin E. Black.

Appendix 1: Terminology for each phase within the annual cycle of Pygoscelis penguins. See below for citations supporting these definitions

Appendix 1: Terminology for each phase within the annual cycle of Pygoscelis penguins. See below for citations supporting these definitions

  1. 1.

    Return to colony: The date in which the first adult is seen returning to the rookery. The phase is sometimes expressed as a range of dates beginning when the first individual returns and ending when the majority of birds are present at the colony.

  2. 2.

    Courtship: The time period when copulations are noted at the breeding site.

  3. 3.

    Egg laying: The start of the egg laying period is often referred to as the clutch initiation date (CID) and the majority of studies have measured this date, or the mean of these dates, when examining phenology. These phases end when the second clutch is laid or, in the case of northern sub-Antarctic gentoo populations, when the two-egg clutch is relaid. The phase is sometimes expressed as a range of dates.

  4. 4.

    Incubation: The time period in which the eggs are incubated, beginning when the second egg is laid, and partners alternate incubation shifts. The phase ends when the first egg hatches.

  5. 5.

    Hatching: The hatching period begins when the first egg hatches and ends when the second egg hatches. Studies often only measure the beginning of this phase; in other words, the date in which the first egg hatches.

  6. 6.

    Guard: The period in which chicks are guarded by their parents and stay within the nest boundaries. The phase begins when the second egg hatches and ends when the first chick is unguarded by parents, leaving the nest.

  7. 7.

    Post-guard: This phase commences when the first chick leaves the nest area and is considered unguarded by a parent and ends when chicks depart the colony.

  8. 8.

    Chick moult: The time period in which chicks moult their down feathers, beginning with the first visible moulting individual and ending with the last.

  9. 9.

    Adult moult: The time period in which adults moult their feathers, beginning with the first visible moulting individual and ending with the last.

  10. 10.

    Chick Departure: The date or series of dates when chicks depart the colony, beginning with the first individual departing to sea and ending with the last.

  11. 11.

    Adult Departure: The date or series of dates when adults depart the colony, beginning with the first individual departing to sea and ending with the last.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Black, C.E. A comprehensive review of the phenology of Pygoscelis penguins. Polar Biol 39, 405–432 (2016). https://doi.org/10.1007/s00300-015-1807-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-015-1807-8

Keywords

Navigation