Skip to main content
SpringerLink
Log in

How age and sex drive the foraging behaviour in the king penguin

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

Abstract

As predicted by life history theory, once recruited into the breeding population and with increasing age, long-lived animals should be able to manage more efficiently the conflict between self-maintenance and reproduction. Consequently, breeding performances should improve with age before stabilizing at a certain level. Using temperature–depth recorders and isotopic analysis, we tested how age affects the foraging behaviour of king penguin Aptenodytes patagonicus during one trip in the chick-rearing phase. Depending on sex and age, king penguins expressed two different foraging strategies. Older birds gained more daily mass per unit body mass than younger ones. Older females conducted shorter trips, dived deeper and performed more prey pursuits. They also had higher blood levels of δ15N than younger individuals and males indicating sex- and age-specific dietary regimes. However, we found no differences in carbon isotopic signature, suggesting that individuals exploited the same foraging areas independently of sex and age. Our results suggest that king penguins are able to increase the quantity of energy extracted with increasing age and that such a strategy is sex-related. Our study is the first to reveal of an interaction between age and sex in determining foraging efficiency in king penguins.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

  • Awkerman JA, Hobson KA, Anderson DJ (2007) Isotopic (δ15N and δ13C) evidence for intersexual foraging differences and temporal variation in habitat use in waved albatrosses. Can J Zool 85:273–279

    Article  Google Scholar 

  • Bannasch R, Wilson RP, Culik B (1994) Hydrodynamic aspects of design and attachment of a back-mounted device in penguins. J Exp Biol 194:83–96

    Google Scholar 

  • Barrat A (1976) Quelques aspects de la biologie et de l’écologie du manchot royal Aptenodytes patagonicus des Iles Crozet. Comité National Français des Recherches Antarctiques 40:107–147

    Google Scholar 

  • Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458

    Article  CAS  Google Scholar 

  • Bost C-A, Georges J-Y, Guinet C, Cherel Y, Putz K, Charrassin J-B, Handrich Y, Zorn T, Large J, LeMaho Y (1997) Foraging habitat and food intake of satellite-tacked king penguins during the austral summer at Crozet Archipelago. MEPS 150:21–33

    Article  Google Scholar 

  • Bost C-A, Handrich Y, Butler P, Falhman A, Halsey LG, Woakes AJ, Ropert-Coudert Y (2007) Changes in dive profiles as an indicator of feeding success in king and Adélie penguins. Deep-Sea Res II 54:248–255

    Article  Google Scholar 

  • Brandt CA (1984) Age and hunting success in the brown pelican—influences of skill and patch choice on foraging efficiency. Oecologia 62(1):132–137

    Article  Google Scholar 

  • Burnham KP, Anderson DR (1998) Model selection and inference: a practical–theoric approach. Springer, New York

    Book  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Charrassin JB, Bost C-A (2001) Utilisation of the oceanic habitat by king penguins over the annual cycle. MEPS 221:285–297

    Article  Google Scholar 

  • Charrassin JB, Bost C-A, Pütz K, Lage J, Dahier T, Zorn T, Le Maho Y (1998) Foraging strategies of incubating and brooding king penguin, Aptenodytes patagonicus. Oecologia 114:194–201

    Article  Google Scholar 

  • Charrassin JB, Le Maho Y, Bost C-A (2002) Seasonal changes in the diving parameters of king penguins (Aptenodytes patagonicus). Mar Biol 141:581–589

    Article  Google Scholar 

  • 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 134:118–127

    Article  Google Scholar 

  • Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005) Nutrition, physiology and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888

    Article  Google Scholar 

  • Cherel Y, Fontaine C, Richard P, Labat J-P (2010) Isotopic niches and trophic levels of myctophid fishes and their predator in the Southern Ocean. Limnol Oceanogr 55:324–332

    Article  CAS  Google Scholar 

  • Clarke J, Kerry K (1998) Implanted transponders in penguins: implantation, reliability, and long term effects. J Field Ornithol 69:149–159

    Google Scholar 

  • Cottin M, Kato A, Thierry A-M, Le Maho Y, Raclot T, Ropert-Coudert Y (2011) Does corticosterone affect diving behavior of male Adélie penguins? A preliminary experimental study. Ornithol Sc 10:1–9

    Article  Google Scholar 

  • Daunt F, Wanless S, Harris MP, Money L, Monaghan P (2007) Older and wiser: improvements in breeding success are linked to better performance in European shags. Funct Ecol 21:561–567

    Article  Google Scholar 

  • DeForest LN, Gaston AJ (1996) The effect of age on timing of breeding and reproductive success in the thick-billed murre. Ecol 77(5):1501–1511

    Google Scholar 

  • Descamps S, Gauthier-Clerc M, Gendner J-P, Le Maho Y (2002) The annual breeding cycle of unbanded king penguins Aptenodytes patagonicus on Possession Island (Crozet). Avian Sci 2:87–98

    Google Scholar 

  • Forero MG, Hobson KA, Bortolotti GR, Donazar JA, Bertellotti M, Blanco G (2002) Food resource utilisation by the Magellanic penguin evaluated through stable-isotope analysis: segregation by sex and age and influence on offspring quality. MEPS 234:289–299

    Article  Google Scholar 

  • Forero MG, González-Solís J, Hobson KA, Doncazar JA, Bertellotti M, Blanco G, Bortolotti GR (2005) Stable isotopes reveal trophic segregation by sex and age in the southern giant petrel in two different food webs. MEPS 296:107–113

    Article  Google Scholar 

  • Forslund P, Pärt T (1995) Age and reproduction in birds-hypotheses and tests. Tree 10:374–378

    Google Scholar 

  • Froget G, Gauthier-Clerc M, Le Maho Y, Handrich Y (1998) Is penguin banding harmless? Polar Biol 20:406–413

    Article  Google Scholar 

  • Gentry RL, Kooyman GL (1986) Methods of dive analysis. In: Gentry RL, Kooyman GL (eds) Fur seals: maternal strategies on land and at sea. Princeton University Press, New Jersey, pp 28–40

    Google Scholar 

  • González-Solís J, Croxall P, Wood AG (2000) Sexual dimorphism and sexual segregation in foraging strategies of northern giant petrels Macronectes halli during incubation. Oikos 90:390–398

    Article  Google Scholar 

  • Goutte A, Antoine E, Weimerskirch H, Chastel O (2010) Age and the timing of breeding in a long-lived bird: a role for stress hormones? Func Ecol 24:1007–1016

    Article  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 

  • Hanuise N, Bost C-A, Huin W, Auber A, Halsey LG, Handrich Y (2010) Measuring foraging activity in a deep-diving bird: comparing wiggles, oesophageal temperatures and beak-opening angles as proxies of feeding. J Exp Biol 213:3874–3880

    Article  Google Scholar 

  • Hobson KA, Clark RG (1993) Turnover of 13C in cellular and plasma fractions of blood: implications for nondestructive sampling in avian dietary studies. Auk 110:638–641

    Article  Google Scholar 

  • Hobson KA, Gibbs HL, Gloutney ML (1997) Preservation of blood and tissue samples for stable-carbon and stable nitrogen analysis. Can J Zool 75:1720–1723

    Article  CAS  Google Scholar 

  • Kato A, Watanuki Y, Shaughnessy P, Le Maho Y, Naito Y (1999) Intersexual differences in the diving behaviour of foraging subantarctic cormorant (Phalacrocorax albiventer) and Japanese cormorant (P. filamentosus). Comptes rendu de l’Académie des Sciences Serie III Sciences de la Vie Life Sci 322:557–562

    CAS  Google Scholar 

  • Kato A, Watanuki Y, Nishiumi I, Kuroki M, Shaughnessy P, Naito Y (2000) Variation in foraging and parental behavior of King Cormorants. Auk 117:718–730

    Google Scholar 

  • Kato A, Ropert-Coudert Y, Gremillet D, Cannell B (2006) Locomotion and foraging strategy in foot-propelled and wing-propelled shallow-diving seabirds. MEPS 308:293–301

    Article  Google Scholar 

  • Kooyman GL, Cherel Y, Lemaho Y, Croxall JP, Thorson PH, Ridoux V (1992) Diving behavior and energetics during foraging cycles in king penguins. Ecol Monogr 62:143–163

    Article  Google Scholar 

  • Koubbi P, Duhamel G, Herbert C (2001) Seasonal relative abundance of fish larvae inshore at îles Kerguelen, Southern Ocean. Ant Sci 13:385–392

    Article  Google Scholar 

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

    Google Scholar 

  • Le Vaillant M, Wilson RP, Kato A, Saraux C, Hanuise H, Prud’Homme O, Le Maho Y, Le Bohec C, Ropert-Coudert Y (2012) King penguins adjust their diving behaviour with age. J Exp Biol 215:3685–3692

    Article  Google Scholar 

  • Lecomte VJ, Sorci G, Cornet S, Jaeger A, Faivre B, Arnoux E, Gaillard M, Trouvé C, Besson D, Chastel O, Weimerskirch H (2010) Patterns of aging in the long-lived wandering albatross. PNAS 107:6370–6375

    Article  CAS  Google Scholar 

  • Lewis S, Schreiber EA, Daunt F, Schenk GA, Orr K, Adams A, Wanless S, Hamer KC (2005) Sex-specific foraging behavior in tropical boobies: does size matter? Ibis 150:408–414

    Article  Google Scholar 

  • Marchetti K, Price T (1989) Differences in the foraging of juvenile and adult birds: the importance of developmental constraints. Biol Rev 64:51–70

    Article  Google Scholar 

  • Nisbet ICT, Dann P (2009) Reproductive performance of little penguins Eudyptula minor in relation to year, age, pair-bond duration, breeding date and individual quality. J Avian Biol 40:296–308

    Article  Google Scholar 

  • Pärt T (1995) Does breeding experience explain increased reproductive success with age? Proc R Soc B 360:113–117

    Article  Google Scholar 

  • Pärt T (2001) The effects of territory quality on age-dependent reproductive performance in the northern wheatear, Oenanthe oenanthe. Anim Behav 62:379–388

    Article  Google Scholar 

  • Pinet P, Jaquemet S, Phillips RA, Le Corre M (2012) Sex-specific foraging strategies throughout the breeding season in a tropical, sexually monorphic small petrel. Anim Behav 83:979–989

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Team TRDC (2010) nlme: linear and nonlinear mixed effect models. R package version 3.1-102

  • Pütz K, Cherel Y (2005) The diving behaviour of brooding king penguins (Aptenodytes patagonicus) from the Falkland Islands: variation in dive profiles and synchronous underwater swimming provide new insights into their foraging strategies. Mar Biol 147:281–290

    Article  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing [Internet]. Vienna (Austria): R Foundation for Statistical Computing. Available from: http://www.R-project.org

  • Ridoux V (1994) The diets and dietary segregation of seabirds at the subantarctic Crozet Islands. Mar Ornithol 22:1–192

    Google Scholar 

  • Rütz C, Whittingham MJ, Newton I (2006) Age-dependent diet choice in an avian top predator. Proc R Soc B 273:579–586

    Article  Google Scholar 

  • Saraux C, Chiaradia A, Le Maho Y, Ropert-Coudert Y (2011) Everybody needs somebody: unequal parental effort in little penguins. Behav Ecol 22:837–845

    Article  Google Scholar 

  • Schreer JF, Kovacs KM (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75:339–358

    Article  Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Weimerskirch H, Stahl JC, Jouventin P (1992) The breeding biology and population-dynamics of king penguins Aptenodytes patagonica on the Crozet-Islands. Ibis 134:107–117

    Article  Google Scholar 

  • Weimerskirch H, Cherel Y, Cuenot-Chaillet F, Ridoux V (1997) Alternative foraging strategies and resource allocation by male and female wandering albatross. Ecology 78:2051–2063

    Article  Google Scholar 

  • Welcker J, Steen H, Harding AMA, Gabrielsen GW (2009) Sex-specific provisioning behaviour in a monorphic seabirb with a biomodal foraging strategy. Ibis 151:502–513

    Article  Google Scholar 

  • Wilson RP (1995) A device for measuring seabird activity at sea. J Avian Biol 26:172–175

    Article  Google Scholar 

  • Wilson RP, Wilson MPT (1989) Tape—a package-attachment technique for penguins. Wildl Soc Bull 17:77–79

    Google Scholar 

  • Wilson RP, Cooper J, Plötz J (1992) Can we determine when marine endotherms feed? A case study seabirds. J Exp Biol 167:267–275

    Google Scholar 

  • Zimmer I, Ropert-Coudert Y, Kato A, Ancel A, Chiaradia A (2011) Does foraging performances change with age in female little penguins (Eudyptula minor). PLoSOne 6:e16098

    CAS  Google Scholar 

Download references

Acknowledgments

Thanks to Paul E. Viblanc for his help in pre-analysing diving data. We are grateful to B. Friess for his help on the Radio Frequency IDentification analysis and H. Gachot-Neveu for sexing birds. Thanks to T. Raclot for his help in delipidating samples, to J.-P. Robin for lyophylizing samples and to P. Richard and G. Guillou for isotopic measurements. We thank all volunteers for their help with field work. This work was supported by the Institut Polaire Français Paul-Emile Victor (Program ECOPHY 137), and by the grants from the Centre National de la Recherche Scientifique, the Fondation Prince Albert II de Monaco (http://www.fpa2.com) and the Fondation des Treilles (to M.L.V.), and the Marie Curie Intra European Fellowship (FP7-PEOPLE-IEF-2008, European Commission; project No 235962) (to C.L.B.).

Ethical note

All procedures employed during animal handling, PIT-tag implantations and data-logger deployments were approved by the Ethical Committee of the French Polar Institute (IPEV Program ECOPHY 137: permits 01/315/AUT issued on the 4 July 2001, 01/322/AUT issued on the 16 August 2001, 2005-191 issued on the 21 November, 2009-57 issued on the 26 August, and 2009-59 issued on the August 29). The handling of individuals was performed without anaesthetic and lasted no longer than 15 min.

Author information

Authors and Affiliations

  1. Institut Pluridisciplinaire Hubert Curien, Université de Strasbourg, 23 rue Becquerel, 67087, Strasbourg, France

    Maryline Le Vaillant, Céline Le Bohec, Onésime Prud’Homme, Yvon Le Maho, Akiko Kato & Yan Ropert-Coudert

  2. CNRS, UMR7178, 23 rue Becquerel, 67037, Strasbourg, France

    Maryline Le Vaillant, Céline Le Bohec, Onésime Prud’Homme, Yvon Le Maho, Akiko Kato & Yan Ropert-Coudert

  3. Centre Scientifique de Monaco, 8 quai Antoine 1er, 98000, Monaco, Principality of Monaco

    Céline Le Bohec

  4. LEA 647 ‘BioSensib’ CSM-CNRS, 8 quai Antoine 1er, 98000, Monaco, Principality of Monaco

    Céline Le Bohec

  5. Nordic Centre for Research on Marine Ecosystems and Resources under Climate Change (NorMER), Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, P.O. Box 1066, Blindern, 0316, Oslo, Norway

    Céline Le Bohec

  6. Australian Antarctic Division, Channel Highway, Kingston, TAS, 7050, Australia

    Barbara Wienecke

Authors
  1. Maryline Le Vaillant
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Céline Le Bohec
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Onésime Prud’Homme
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Barbara Wienecke
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yvon Le Maho
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Akiko Kato
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yan Ropert-Coudert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maryline Le Vaillant.

Additional information

Communicated by S. Garthe.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Le Vaillant, M., Le Bohec, C., Prud’Homme, O. et al. How age and sex drive the foraging behaviour in the king penguin. Mar Biol 160, 1147–1156 (2013). https://doi.org/10.1007/s00227-013-2167-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2167-y

Keywords

Search

Navigation