Skip to main content
Log in

Foraging plasticity of breeding Northern Rockhopper Penguins, Eudyptes moseleyi, in response to changing energy requirements

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

Abstract

During the breeding season, seabirds must balance the changing demands of self- and off-spring provisioning with the constraints imposed by central-place foraging. Recently, it was shown that Northern Rockhopper Penguins at Tristan da Cunha in the South Atlantic Ocean switch diet from lower to higher trophic level prey throughout their breeding cycle. Here, we investigated if this switch is reflected in their foraging behaviour, using time-depth recorders to study the diving behaviour of 27 guard and 10 crèche birds during the breeding season 2010 at Tristan da Cunha and obtaining complementary stomach contents of 20 birds. While no significant effects of breeding stage were detected on any foraging trip or dive parameters, stage/prey had a significant effect on feeding dive parameters, with dive duration, bottom time, and maximum depth explaining the majority of the dissimilarity amongst categories. We verified the previously shown dietary shift from zooplankton and cephalopods during the guard stage to a higher-energy fish-based diet during the crèche stage, which was reflected in a change in dive behaviour from shorter, shallower to longer, deeper dives. This prey switching behaviour may reflect preferential selection to account for the increased physiological needs of chicks or simply mirror changes in local prey abundance. Nonetheless, we show that Northern Rockhopper Penguins demonstrate behavioural plasticity as a response to their changing energy requirements, which is a critical trait when living in a spatio-temporally heterogeneous environment. This ability is likely to be particularly important under extrinsic constraints such as long-term environmental change.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ainley DG, Ballard G, Barton KJ, Karl BJ, Rau GH, Ribic A, Wilson PR (2003) Spatial and temporal variation of diet within a presumed meta-population of Adélie penguins. Condor 105:95–106

    Article  Google Scholar 

  • Anderson M, Gorley RN, Clarke RK (2008) Permanova + for primer: guide to software and statistical methods. Plymouth Marine Laboratory, Plymouth

    Google Scholar 

  • Boersma PD, Rebstock GA, García-Borboroglu P (2015) Marine protection is needed for Magellanic penguins in Argentina based on long-term data. Biol Cons 182:197–204

    Article  Google Scholar 

  • Booth JM (2011) Trophic ecology of breeding northern rockhopper penguins, Eudyptes Moseleyi, at Tristan da Cunha, South Atlantic Ocean. Dissertation, Rhodes University

  • Booth JM, McQuaid CD (2013) Northern rockhopper penguins prioritise future reproduction over chick provisioning. Mar Ecol Prog Ser 486:289–304

    Article  Google Scholar 

  • Bost CA, Handrich Y, Butler PJ, Fahlman 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 

  • Box GE, Jenkins GM, Reinsel GC (1994) Time series analysis: forecasting and control, 3rd edn. Prentice Hall, New Jersey

    Google Scholar 

  • Breslow NE, Clayton DG (1993) Approximate inference in generalized linear mixed models. J Am Stat Assoc 88:9–25

    Google Scholar 

  • Brown CR (1987) Energy requirements for growth and maintenance in macaroni and rockhopper penguins. Polar Biol 8:95–102

    Article  Google Scholar 

  • Charassin JB, Bost CA, Pütz K, Lage J, Dahier T, Zorn T, Le Maho Y (1998) Foraging strategies of incubating and brooding King penguins Aptenodytes patagonicus. Oecologia 114(2):194–201

    Article  Google Scholar 

  • Cherel Y, Tremblay Y, Guinard E, Georges JY (1999) Diving behaviour of female Northern rockhopper penguins Eudyptes chrysocome moseleyi during the brooding period at Amsterdam Island (Southern Indian Ocean). Mar Biol 134:375–385

    Article  Google Scholar 

  • Cherel Y, Hobson KA, Guinet C, Vanpe C (2007) Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean. J Anim Ecol 76:826–836

    Article  PubMed  Google Scholar 

  • Clarke KR, Gorley RN (2006) Primer v6: user manual/tutorial. PRIMER-E Ltd, Plymouth

    Google Scholar 

  • Crossin GT, Takahashi A, Sakamoto KQ, Trathan PN, Williams TD (2015) Habitat selection by foraging macaroni penguins correlates with hematocrit, an index of aerobic condition. Mar Ecol Prog Ser 530:163–176

    Article  Google Scholar 

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

    Google Scholar 

  • Cuthbert R (2013) Northern Rockhopper Penguin Eudyptes moseleyi. In: Gracia-Borboroglu P, Boersma PD (eds) Penguins: natural history and conservation. University of Washington Press, Seattle

    Google Scholar 

  • Cuthbert R, Cooper J, Burle MH, Glass CJ, Glass JP, Glass S, Glass T, Hilton GM, Sommer ES, Wanless RM, Ryan PG (2009) Population trends and conservation status of the Northern Rockhopper penguins Eudyptes moseleyi at Tristan da Cunha and Gough Island. Bird Conserv Int 19:109–120

    Article  Google Scholar 

  • Davis LS, Cuthbert RL (2001) Reproductive ecology of seabirds. In: Steel JH, Thorpe SA, Turekian KK (eds) Encyclopaedia of ocean sciences. Academic Press, London

    Google Scholar 

  • Davoren GK, Montevecchi WA, Anderson JT (2003) Search strategies of a pursuit-diving marine bird and the persistence of prey patches. Ecol Monogr 73:463–481

    Article  Google Scholar 

  • Deagle BE, Gales NJ, Hindell MA (2008) Variability in foraging behaviour of chick-rearing Macaroni penguins Eudyptes chrysolophus. Mar Ecol Prog Ser 359:295–309

    Article  Google Scholar 

  • Dehnhard N, Ludynia K, Masello JF, Voigt CC, McGill RA, Quillfeldt P (2016) Plasticity in foraging behaviour and diet buffers effects of inter-annual environmental differences on chick growth and survival in southern rockhopper penguins Eudyptes chrysocome chrysocome. Polar Biol 39:1627–1641

    Article  Google Scholar 

  • Elliott KH, Woo K, Gaston AJ, Benvenuti S, Dall’Antonia L, Davoren GK, (2008) Seabird foraging behaviour indicates prey type. Mar Ecol Prog Ser 354:289–303. https://doi.org/10.3354/meps07221

    Article  Google Scholar 

  • Elliott KH, Ricklefs RE, Gaston AJ, Hatch SA, Speakman JR, Davoren GK (2013) High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins. PNAS 110:9380–9384

    Article  PubMed  Google Scholar 

  • Gales RP (1987) Validation of the stomach-flushing technique for obtaining stomach contents of penguins. Ibis 129:335–343

    Article  Google Scholar 

  • Gaston AJ (2004) Seabirds: a natural history. Oxford University Press, Oxford

    Google Scholar 

  • Hagihara R, Jones RE, Sheppard JK, Hodgson AJ, Marsh H (2011) Minimizing errors in the analysis of dive recordings from shallow-diving animals. J Exp Mar Biol Ecol 399:173–181

    Article  Google Scholar 

  • Handley JM, Baylis AM, Brickle P, Pistorius P (2016) Temporal variation in the diet of gentoo penguins at the Falkland Islands. Polar Biol 39:283–296

    Article  Google Scholar 

  • Handley JM, Connan M, Baylis AM, Brickle P, Pistorius P (2017) Jack of all prey, master of some: influence of habitat on the feeding ecology of a diving marine predator. Mar Biol 164:82

    Article  Google Scholar 

  • Heath RGM, Randall RM (1985) Growth of Jackass penguin chicks (Spheniscus demersus) hand reared on different diets. J Zool 205:91–105

    Article  Google Scholar 

  • Ichii T, Naganobu M, Ogisima T (1996) Competition between the krill fishery and penguins in the South Shetland Islands. Polar Biol 16:63–70

    Article  Google Scholar 

  • Jansen JK, Russell RW, Meyer WR (2002) Seasonal shifts in the provisioning behavior of chinstrap penguins, Pygoscelis antarctica. Oecologia 131:306–318

    Article  PubMed  Google Scholar 

  • Lack D (1968) Ecological adaptations for breeding in birds. Methuen, London

    Google Scholar 

  • Lescroël A, Bost CA (2005) Foraging under contrasting oceanographic conditions: the Gentoo penguin at Kerguelen Archipelago. Mar Ecol Prog Ser 302:245–261

    Article  Google Scholar 

  • Ludynia K, Roux JP, Jones R, Kemper J, Underhill LG (2010) Surviving off junk: low-energy prey dominates the diet of African penguins Spheniscus demersus at Mercury Island, Namibia, between 1996 and 2009. Afr J Mar Sci 32:563–572

    Article  Google Scholar 

  • Lyver POB, MacLeod CJ, Ballard G, Karl BJ, Barton KJ, Adams J, Ainley DG, Wilson PR (2011) Intra-seasonal variation in foraging behaviour among Adélie penguins (Pygoscelis adeliae) breeding at Cape Hallett Ross Sea Antarctica. Polar Biol 34:49–67

    Article  Google Scholar 

  • MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609

    Article  Google Scholar 

  • Mauchline J (1980) The biology of mysids and euphausiids. Adv Mar Biol 18:1–681

    Google Scholar 

  • Mori Y (1998) The optimal patch use in divers: optimal time budget and the number of dive cycles during bout. J Theor Biol 190:187–199

    Article  Google Scholar 

  • Orians GH, Pearson NE (1979) On the theory of central place foraging. In: Horn DJ, Mitchell RD, Stairs GR (eds) Analysis of ecological systems. Ohio State University Press, Colombus

    Google Scholar 

  • Pichegru L, Ropert-Coudert Y, Kato A, Takahashi A, Dyer BM, Ryan PG (2011) Diving patterns of female Macaroni penguins breeding on Marion Island, South Africa. Polar Biol 34:945–954

    Article  Google Scholar 

  • Pichegru L, Cook T, Handley J, Voogt N, Watermeyer J, Nupen L, McQuaid CD (2013) Sex-specific foraging behaviour and a field sexing technique for Endangered African penguins. Endangered Species Res 25:255–264

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Core Team R (2009) nlme: linear and nonlinear mixed effects models. R package version 3(1–131):1

    Google Scholar 

  • R Development Core Team. 2010. R: a language and environment for statistical computing

  • Ratcliffe N, Takahashi A, O’Sullivan C, Adlard S, Trathan PN, Harris MP, Wanless S (2013) The roles of sex, mass and individual specialisation in partitioning foraging-depth niches of a pursuit-diving predator. PLoS ONE 8:e79107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ratcliffe N, Crofts S, Brown R, Baylis AM, Adlard S, Horswill C, Venables H, Taylor P, Trathan PN, Staniland IJ (2014) Love thy neighbour or opposites attract? Patterns of spatial segregation and association among crested penguin populations during winter. J Biogeogr 41:1183–1192

    Article  PubMed  PubMed Central  Google Scholar 

  • Raya Rey A, Trathan P, Schiavini A (2007) Inter-annual variation in provisioning behaviour of Southern Rockhopper Penguins Eudyptes chrysocome chrysocome at Staten Island, Argentina. Ibis 149:826–835

    Article  Google Scholar 

  • Raya Rey A, Pütz K, Simeone A, Hiriart-Bertrand L, Reyes-Arriagada R, Riquelme V, Lüthi B (2013) Comparative foraging behaviour of sympatric Humboldt and Magellanic Penguins reveals species-specific and sex-specific strategies. Emu 113:145–153

    Article  Google Scholar 

  • Robson B, Glass T, Glass N, Glass J, Green J, Repetto C, Rodgers G, Ronconi RA, Ryan PG, Swain G, Cuthbert RJ (2011) Revised population estimate and trends for the Endangered Northern Rockhopper Penguin Eudyptes moseleyi at Tristan da Cunha. Bird Conserv Int 21:454–459

    Article  Google Scholar 

  • Ropert-Coudert Y, Kato A, Bost CA, Rodary D, Sato K, Le Maho Y, Naito Y (2002) Do Adélie penguins modify their foraging behaviour in pursuit of different prey? Mar Biol 140:647–652

    Article  Google Scholar 

  • Ropert-Coudert Y, Kato A, Wilson RP, Cannell B (2006) Foraging strategies and prey encounter rate of free-ranging Little penguins. Mar Biol 149:139–148

    Article  Google Scholar 

  • Sala JE, Wilson RP, Quintana F (2012) How much is too much? Assessment of prey consumption by Magellanic penguins in Patagonian colonies. PLoS ONE 7:e51487

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sala JE, Wilson RP, Frere E, Quintana F (2014) Flexible foraging for finding fish: variable diving patterns in Magellanic penguins Spheniscus magellanicus from different colonies. J Ornithol 155:801–817

    Article  Google Scholar 

  • Schiavini A, Raya Rey A (2004) Long days, long trips: foraging ecology of female rockhopper penguins Eudyptes chrysocome chrysocome at Tierra del Fuego. Mar Ecol Prog Ser 275:251–262

    Article  Google Scholar 

  • Stein RW, Williams TD (2013) Extreme intraclutch egg-size dimorphism in Eudyptes penguins, an evolutionary response to clutch-size maladaptation. Am Nat 182:260–270

    Article  PubMed  Google Scholar 

  • Tremblay Y, Cherel Y (2000) Benthic and pelagic dives: a new foraging behaviour in rockhopper penguins. Mar Ecol Prog Ser 204:257–267

    Article  Google Scholar 

  • Tremblay Y, Cherel Y (2003) Geographic variation in the foraging behaviour diet and chick growth of rockhopper penguins. Mar Ecol Prog Ser 251:279–297

    Article  Google Scholar 

  • Tremblay Y, Cherel Y (2005) Spatial and temporal variation in the provisioning behaviour of female rockhopper penguins Eudyptes chrysocome filholi. J Avian Biol 36:135–145

    Article  Google Scholar 

  • Tremblay Y, Guinard E, Cherel Y (1997) Maximising diving depths of Northern rockhopper penguins (Eudyptes chrysocome moseleyi) at Amsterdam Island. Polar Biol 17:119–122

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Van de Putte A, Flores H, Volckaert F, van Franekar JA (2006) Energy content of Antarctic mesopelagic fishes: implications for the marine food webs. Polar Biol 29:1045–1051

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Random and mixed effects. Springer, New York

    Book  Google Scholar 

  • Weimerskirch H, Doncaster C, Cuenot-Chaillet F (1994) Pelagic seabirds and the marine environment: foraging patterns of wandering albatrosses in relation to prey availability and distribution. Proc R Soc Lond B Biol Sci 255:91–97

    Article  Google Scholar 

  • Whitehead TO, Kato A, Ropert-Coudert Y, Ryan PG (2016) Habitat use and diving behaviour of macaroni Eudyptes chrysolophus and eastern rockhopper E. chrysocome filholi penguins during the critical pre-moult period. Mar Biol 163:19

    Article  Google Scholar 

  • Williams TD, Rothery P (1990) Factors affecting variation in foraging and activity patterns of gentoo penguins (Pygoscelis papua) during the breeding season at Bird Island, South Georgia. J Appl Ecol 1:1042–1054

    Article  Google Scholar 

  • Wilson RP (1985) The Jackass penguin (Spheniscus demersus) as a pelagic predator. Mar Ecol Prog Ser 25:219–227

    Article  Google Scholar 

  • Wilson RP, Ryan PG, Wilson MP (1989) Sharing food in the stomachs of seabirds between adults and chicks – a case for delayed gastric emptying. Comp Biochem Physiol A Physiol 94:461–466

    Article  CAS  Google Scholar 

  • Wilson RP, Ropert-Coudert Y, Kato A (2002) Rush and grab strategies in foraging marine endotherms: the case for haste in penguins. Anim Behav 63:85–95

    Article  Google Scholar 

  • Wilson RP, Scolaro JA, Grémillet D, Kierspel MAM, Laurenti S, Upton J, Galleli H, Quintana F, Frere E, Müller G, Straten MT, Zimmer I (2005) How do Magellanic penguins cope with variability in their access to prey? Ecol Monogr 75:379–401

    Article  Google Scholar 

  • Xavier JC, Trathan PN, Ceia FR, Tarling GA, Adlard S, Fox D, Edwards EW, Vieira RP, Medeiros R, De Broyer C, Cherel Y (2017) Sexual and individual foraging segregation in Gentoo penguins Pygoscelis papua from the Southern Ocean during an abnormal winter. PLoS ONE 12:e0174850

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ydenberg RC, Welham CV, Schmid-Hempel R, Schmid-Hempel P, Beauchamp G (1994) Time and energy constraints and the relationships between currencies in foraging theory. Behav Ecol 5:28–34

    Article  Google Scholar 

  • Zimmer I, Ropert-Coudert Y, Poulin N, Kato A, Chiaradia A (2011) Evaluating the relative importance of intrinsic and extrinsic factors on the foraging activity of top predators: a case study on female little penguins. Mar Biol 158:715–722

    Article  Google Scholar 

Download references

Acknowledgements

This work was carried out under the auspices of the Flagship Species Fund of the Department of Environment, Food and Rural Affairs (DEFRA) and Fauna & Flora International with funding from DEFRA, the Royal Society for the Protection of Birds (RSPB) and other donors under Project FSF-Defra- 10-48. The Department of Environmental Affairs through the South African National Antarctic Programme and the Tristan da Cunha conservation department provided logistical support. Thanks to T. Glass, J. Repetto, G. Swain, C. Repetto, M. Green and K. Green of the Tristan Conservation Department for their support in the field. M. Connan and anonymous reviewers provided helpful comments on an earlier version of this manuscript. This work is based upon research supported by the South African Research Chairs Initiative of the Department of Science and Technology and the National Research Foundation. Funding was provided by SARCHI (Grant Number 64801).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jenny M. Booth.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Animal rights

Full permission for all methods used in this study and access to the penguin colonies were granted by the Tristan da Cunha government. Animal ethics approval was given by Rhodes University Ethics Committee (ZOOL-17-2010). All applicable international and institutional guidelines for the use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Booth, J.M., Steinfurth, A., Fusi, M. et al. Foraging plasticity of breeding Northern Rockhopper Penguins, Eudyptes moseleyi, in response to changing energy requirements. Polar Biol 41, 1815–1826 (2018). https://doi.org/10.1007/s00300-018-2321-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-018-2321-6

Keywords

Navigation