Skip to main content
SpringerLink
Log in

Extra-pair paternity and intraspecific brood parasitism in the Gentoo Penguin (Pygoscelis papua) on Elephant Island, Antarctica

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Recent studies have shown that many species of apparently monogamous birds engage in extra-pair copulation (EPC). Penguins have intense shared parental care for their young, and thus have been considered monogamous. The present study aimed to assess the reproductive system of the gentoo penguin (Pygoscelis papua) on Elephant Island, Antarctica, by evaluating extra-pair paternity (EPP) and intraspecific brood parasitism (IBP). Our data revealed high rates of EPC, with approximately 48.75% of chicks originating from EPP, corresponding to 72.5% of nests. IBP was found for ~ 17% of the gentoo penguin nests, a behavior previously recorded only for Magellanic penguins (~ 6%). The reasons for these behaviors are not clear, as increased genetic diversity or sex bias of offspring was not found. Thus, social and ecological aspects could be more important for determining the costs and benefits of EPP. Other genetic and ecological aspects must be investigated in future studies, such as genetic compatibility of the immune system or fluctuations of the EPP rate due to environmental conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahmed S, Hart T, Dawson DA, Horsburgh GJ, Trathan PN, Rogers AD (2009) Isolation and characterization of macaroni penguin (Eudyptes chrysolophus) microsatellite loci and their utility in other penguin species (Spheniscidae, AVES). Mol Ecol Resour 9:1530–1535. https://doi.org/10.1111/j.1755-0998.2009.02710.x

    Article  CAS  PubMed  Google Scholar 

  • Akçay E, Roughgarden J (2007) Extra-pair paternity in birds: review of the genetic benefits. Evol Ecol Res 9:855–868

    Google Scholar 

  • Arnold KE, Owens IPF (2002) Extra-pair paternity and egg dumping in birds: life history, parental care and the risk of retaliation. Proc R So B 269:1263–1269

    Article  Google Scholar 

  • Baião PC, Parker PG (2009) No evidence of extra-pair fertilization in red-footed boobies (Sula sula). Waterbirds 32:179–182. https://doi.org/10.1675/063.032.0122

    Article  Google Scholar 

  • Bertellotti M, Tella JL, Godoy JA, Blanco G, Forero MG, Donázar JA, Ceballos O (2002) Determining sex of magellanic penguins using molecular procedures and discriminant functions. Waterbirds 25:479–484. https://doi.org/10.1675/1524-4695

    Article  Google Scholar 

  • Billing TM, Guay PJ, Peucker AJ, Mulder RA (2007) Isolation and characterization of polymorphic microsatellite loci for the study of paternity and population structure in the little penguin Eudyptula minor. Mol Ecol Notes 7:425–427. https://doi.org/10.1111/j.1471-8286.2006.01607.x

    Article  CAS  Google Scholar 

  • Birdlife International (2016) Pygoscelis papua. The IUCN Red List of Threatened Species 2016: e.T22697755A93637402. Available at https://doi.org/10.2305/IUCN.UK.20163.RLTS.T22697755A93637402. Accessed 07 May 2018

  • Birkhead TR, Møller AP (1992) Sperm competition in birds. Evolutionary causes and consequences. Academic press, San Diego

    Google Scholar 

  • Birkhead TR, Møller AP (1993) Female control of paternity. Trends Ecol Evol 8:100–104

    Article  CAS  Google Scholar 

  • Black C, Collen B, Johnston D, Hart T (2016) Why huddle? Ecological drivers of chick aggregations in gentoo penguins, Pygoscelis papua, across latitudes. PLoS ONE 11(2):e0145676. https://doi.org/10.1371/journal.pone.0145676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Burg TM, Croxall JP (2006) Extrapair paternities in black-browed Thalassarche melanophris, grey-headed T. chrysostoma and wandering albatrosses Diomedea exulans at South Georgia. J Avian Biol 37:331–338

    Article  Google Scholar 

  • Calderón L, Svagelj WS, Quintana F, Lougheed SC, Tubaro PL (2012) No evidence of extra-pair paternity or intraspecific brood parasitism in the Imperial Shag Phalacrocorax atriceps. J Ornithol 153:399–404. https://doi.org/10.1007/s10336-011-0754-6

    Article  Google Scholar 

  • Charmantier A, Blondel J, Perret P, Lambrechts MM (2004) Do extra-pair paternities provide genetic benefits for female blue tits Parus caeruleus? J Avian Biol 35:524–532. https://doi.org/10.1111/j.0908-8857.2004.03296.x

    Article  Google Scholar 

  • Clausen AP, Putz K (2002) Recent trends in diet composition and productivity of Gentoo, Magellanic and rockhopper penguins in the Falkland Islands. Aquat Conserv Mar Freshw Ecosyst 12:51–61

    Article  Google Scholar 

  • Clutton-Brock TM (1986) Sex ratio variation in birds. Ibis 128:317–329

    Article  Google Scholar 

  • Davis CA, Orange JP, Bussche RAVD, Elmore D, Fuhlendorf SD, Carroll JM, Tanner EP, Leslie DM Jr (2017) Extrapair paternity and nest parasitism in two sympatric quail. Auk 134:811–882. https://doi.org/10.1642/AUK-16-162.1

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, New York

    Book  Google Scholar 

  • Geffen E, Yom-Tov Y (2001) Factors affecting the rates of intraspecific nest parasitism among Anseriformes and Galliformes. Anim Behav 62:1027–1038

    Article  Google Scholar 

  • Gilbert G, Gibbons DW, Evans J (1998) Bird Monitoring methods: a manual of techniques for key UK species. RSPB, Bedfordshire

    Google Scholar 

  • Gray EM (1997) Female red-winged blackbirds accrue material benefits from copulating with extra-pair males. Anim Behav 53:625–639

    Article  Google Scholar 

  • Griffith SC, Owens IP, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212. https://doi.org/10.1046/j.1365-294X.2002.01613.x

    Article  CAS  PubMed  Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    Article  CAS  Google Scholar 

  • Herman RW, Valls FCL, Hart T, Petry MV, Trivelpiece WZ, Polito MJ (2017) Seasonal consistency and individual variation in foraging strategies differ among and within Pygoscelis penguin species in the Antarctic Peninsula region. Mar Biol 164:1–13. https://doi.org/10.1139/cjz-2019-0032

    Article  CAS  Google Scholar 

  • Indykiewicz P, Podlaszczuk P, Minias P (2018) Extra-pair paternity in the black-headed gull: is it exceptional among colonial waterbirds? Behaviour 154:1081–1099. https://doi.org/10.1163/1568539X-00003459

    Article  Google Scholar 

  • Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Res 10:551–555. https://doi.org/10.1111/j.1755-0998.2009.02787.x

    Article  Google Scholar 

  • Jouventin P, Charmantier A, Dubois MP, Jarne P, Bried J (2007) Extra-pair paternity in the strongly monogamous Wandering Albatross Diomedea exulans has no apparent benefits for females. Ibis 149:67. https://doi.org/10.1111/j.1474-919X.2006.00597.x78

    Article  Google Scholar 

  • Kempenaers B, Verheyen GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus ): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492

    Article  Google Scholar 

  • Kempenaers B, Congdon B, Boag P, Robertson RJ (1999) Extrapair paternity and egg hatchability in tree swallows: evidence for the genetic compatibility hypothesis? Behav Ecol 10:304–311

    Article  Google Scholar 

  • Kokko H (2001) Fisherian and ‘‘good genes’’ benefits of mate choice: how (not) to distinguish between them. Ecol Lett 4:322–326

    Article  Google Scholar 

  • Lescroel A, Ridoux V, Bost CA (2004) Spatial and Temporal variation in the diet of Gentoo Penguin (Pygoscelis papua) at Kerguelen Island. Pol Bio 27:206–216. https://doi.org/10.1007/s00300-003-0571-3

    Article  Google Scholar 

  • Lynch HL (2013) The gentoo penguin (Pygoscelis papua). In: Borboroglu PG, Boersma PD (eds) Biology and conservation of the world’s penguins. University of Washington Press, Seattle

    Google Scholar 

  • Marasco ACM, Morgante JS, Barrinuevo M, Frere E, Dantas GPM (2020) Molecular evidence of extra-pair paternity and intraspecific brood parasitism by the Magellanic Penguin (Spheniscus magellanicus). J Ornithol 161:125–135. https://doi.org/10.1007/s10336-019-01720-4

    Article  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  CAS  Google Scholar 

  • Minias P, Wojczulanis-Jakubas K, Rutkowski R, Kaczmarek K, Janiszewski T (2016) Spatial patterns of extra-pair paternity in a waterbird colony: separating the effects of nesting density and nest site location. Behav Ecol Sociobiol 70:369–376. https://doi.org/10.1007/s00265-015-2056-0

    Article  PubMed  PubMed Central  Google Scholar 

  • Møller AP, Ninni P (1998) Sperm competition and sexual selection: a meta-analysis of paternity studies of birds. Behav Ecol Sociobiol 43:345–358

    Article  Google Scholar 

  • Mulder RA, Dunn PO, Cockburn RA, Lazenby-Cohen KA, Howell MJ (1994) Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proc R Soc Lond B 255:223–229

    Article  Google Scholar 

  • Orr HA (2009) Fitness and its role in evolutionary genetics. Nat Rev Genet 10:531–539. https://doi.org/10.1038/nrg2603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58

    Article  CAS  Google Scholar 

  • Petrie M, Møller AP (1991) Laying eggs in others´nests: intraspecific brood parasitim in birds. Trends Ecol Evol 6:315–320

    Article  CAS  Google Scholar 

  • Petry MV, Valls FCL, Petersen ES, Finger JVG, Krüger L (2018) Population trends of seabirds at Stinker Point. Antarctic Science, Elephant Island. https://doi.org/10.1017/S0954102018000135

    Book  Google Scholar 

  • Pilastro A, Pezzo F, Olmastroni S, Callegarin C, Corsolini S, Focardi S (2001) Extrapair paternity in the Adelie penguin. Ibis 143:681–684

    Article  Google Scholar 

  • Polito MJ, Trivielpiece WZ (2008) Transition to independence and evidence of extended parental care in the Gentoo penguin (Pygoceslis papua). Mar Biol 154:231–240. https://doi.org/10.1007/s00227-008-0919-x

    Article  Google Scholar 

  • Roeder AD, Marshall RK, Mitchelson AJ, Visagathilagar T, Ritchie PA, Love DR, Pakai TJ, McPartlan HC, Murray ND, Robinson NA, Kerry KR, Lambert DM (2001) Gene flow on the ice: genetic differentiation among Adélie penguin colonies around Antarctica. Mol Ecol 10:1645–1656

    Article  CAS  Google Scholar 

  • Sambrook J, Russel DW (2001) Molecular cloning. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schwartz MK, Boness DJ, Schaeff CM, Majluf P, Perry EA, Fleischer RC (1999) Female-solicited extrapair matings in Humboldt penguins fail to produce extrapair fertilizations. Behav Ecol 10:242–250

    Article  Google Scholar 

  • St Clair CC, Waas JR, St Clair RC, Boag PT (1995) Unfit mothers? Maternal infanticide in royal penguins. Anim Behav 50:1177–1185

    Article  Google Scholar 

  • St Clair CC, McLean IG, Murie JO, Phillipson SM, Studholme BJS (1999) Fidelity to nest site and mate in Fiordland Crested penguins Eudyptes pachyrhynchus. Mar Ornithol 27:37–41

    Google Scholar 

  • Stonehouse BS (1970) Geographic variation in gentoo penguins Pygoscelis papua. Ibis 112:52–57

    Article  Google Scholar 

  • Trivelpiece WS, Trivelpiece SG (1990) Courtship period of Adelie, Gentoo and Chinstrap penguins. In: Davis LS, Darby JT (eds) Penguin biology. Academic Press, San Diego, pp 113–127

    Google Scholar 

  • Valls FCL, Petry MV (2014) Niche overlap of Spheniscidae on Elephant Island, Antarctic. Annual activity report. Editora Cubo, São Carlos, São Paulo

    Google Scholar 

  • Vianna JA, Noll D, Dantas GPM, Petry MV, Barbosa A, González-Acuña D, Le Bohec C, Bonadonna F, Poulin E (2017a) Marked phylogeographic structure of Gentoo penguin reveals an ongoing diversification process along the Southern Ocean. Mol Phylogenet Evol 107:486–498. https://doi.org/10.1016/j.ympev.2016.12.003

    Article  PubMed  Google Scholar 

  • Vianna JA, Noll D, Mura-Jornet I, Valenzuela-Guerra P, González-Acuña D, Navarro C, Dantas GPM (2017b) Comparative genome-wide polymorphic microsatellite markers in Antarctic penguins through next generation sequencing. Genet Mol Biol 40:676–687. https://doi.org/10.1590/1678-4685-gmb-2016-0224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webster MS, Westneat DF (1998) The use of molecular markers to study kinship in birds: techniques and questions. In: DeSalle R, Schierwater B (eds) Molecular Approach for Ecology and Evolution. Birkhäuser, Basel, pp 7–35. https://doi.org/10.1007/978-3-0348-8948-3-1

    Chapter  Google Scholar 

  • Wetzel DP, Westneat DF (2009) Heterozygosity and extra-pair paternity: biased tests result from the use of shared markers. Mol Ecol 18:2010–2021. https://doi.org/10.1111/j.1365-294X.2009.04114.x

    Article  PubMed  Google Scholar 

  • Wetton JH, Parkin DT (1991) An association between fertility and cuckoldry in the house sparrow, Passer domesticus. Proc R Soc Lond B 245:227–233

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Williams TD (1995) Bird families of the world: the penguins. Oxford University Press, Oxford

    Google Scholar 

  • Williams TD, Rodwell S (1992) Annual variation in return rate, mate and nest-fidelity in breeding gentoo and macaroni penguins. Condor 94:636–645

    Article  Google Scholar 

  • Wink M, Dyrcz A (1999) Mating system in birds: a review of molecular studies. Acta Ornith 34:91–109

    Google Scholar 

  • Wojczulanis-Jakubas K, Jakubas D, Øigarden T, Lifjeld JT (2009) Extrapair copulations are frequent but unsuccessful in a highly colonial seabird, the little auk, Alle alle. Anim Behav 77:433–438

    Article  Google Scholar 

  • Yom-Tov Y (2001) An update list and some comments on the occurrence of intraspecific nest parasitism in birds. Ibis 143:133–143

    Article  Google Scholar 

Download references

Acknowledgements

We thank the team from the Laboratório de Ornitologia e Animais Marinhos at the Universidade do Vale do Rio dos Sinos for assistance with field work. Financial support for the analysis in this study was provided by the National Council for Research and Development (CNPq; Process no. 482501/2013-8, 306904/2019-5) and FIP-PUC Minas (2016-S2-11080). Financial support for field work was provided by the National Institute of Science and Technology of Antarctic Environmental Research (INCT-APA) (CNPq Process no. 574018/2008-5), and the Carlos Chagas Research Support Foundation of the State of Rio de Janeiro (FAPERJ; process no. E-16/170023/2008). Logistical support was provided by the Brazilian Secretary of the Inter-Ministry on Marine Resources (SECIRM). We thank Erik Wild for his checking and correcting of the English in this paper, as well as Peter Dann, Grant Ballard and anonymous reviewers who all helped improve the manuscript.

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Biologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais, Av. Dom Jose Gaspar, 500, Prédio 41, Coração Eucarístico, Belo Horizonte, Minas Gerais, Cep:30535-901, Brazil

    Gisele Pires de Mendonça Dantas, Luana Gisele Gonzaga & Alana Silva da Silveira

  2. Programa de Pós-Graduação em Biologia, Laboratório de Ornitologia E Animais Marinhos, Universidade Do Vale Do Rio Dos Sinos, Av. Unisinos, São Leopoldo, State of Rio Grande do Sul, 950, Brazil

    Gabriela Bandasz Werle, Roberta da Cruz Piuco & Maria Virginia Petry

  3. INCT-APA National Institute of Science and Technology of Antarctic Environmental Research, Rio de Janeiro, Brazil

    Maria Virginia Petry

Authors
  1. Gisele Pires de Mendonça Dantas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luana Gisele Gonzaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alana Silva da Silveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gabriela Bandasz Werle
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roberta da Cruz Piuco
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Virginia Petry
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GPMD contributed to the design of the study, sampling, data analysis, and writing of the manuscript text. AS and LGG contributed to the laboratory work and data analysis. MVP, GV, and RCP contributed to the sampling design and field work. All authors contributed to the draft of the manuscript.

Corresponding author

Correspondence to Gisele Pires de Mendonça Dantas.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the Animal Research Ethics Committee CEUA -PUC Minas (0026-2014), and agrees with the Commission for the Conservation of Antarctic Marine Living Resources (CAMMLAR) protocol, and was approved by PROANTAR (Antarctic Brazilian Program).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Mendonça Dantas, G.P., Gonzaga, L.G., da Silveira, A.S. et al. Extra-pair paternity and intraspecific brood parasitism in the Gentoo Penguin (Pygoscelis papua) on Elephant Island, Antarctica. Polar Biol 43, 851–859 (2020). https://doi.org/10.1007/s00300-020-02692-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-020-02692-5

Keywords

Search

Navigation