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Evaluating the relative importance of intrinsic and extrinsic factors on the foraging activity of top predators: a case study on female little penguins

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Abstract

A complex interaction of biotic and abiotic factors influences animal foraging activity. It is often difficult to understand which factors may affect animals’ foraging and how it is affected. For instance, whereas the effect of sexual dimorphism on foraging activity has been reported in several species, little is known of the complex interactions between variables acting at a finer scale, e.g. the variability of body mass within a sex. Evaluating the importance of these finer scale factors is also essential to the understanding of foraging behaviour. We propose here a simple approach by applying principal component analysis (PCA) in a novel way to examine relationships between biotic and abiotic factors affecting foraging behaviour of top predators. We studied female little penguins (Eudyptula minor) of known age, carrying miniature accelerometers during the guard stage of breeding. Surprisingly, the body mass of the females did not influence any of the foraging parameters, but females foraging later in the breeding season dived shallower and more often, showing a strong correlation with laying date. Similarly, the diving effort of females was greater with increasing chick age within the same breeding stage. These results indicate that for female little penguin, the relationship between changes in prey availability and hunting effort can change at a fine scale, within a breeding stage. Therefore, any analysis of little penguin foraging behaviour during breeding should consider the timing in relation to the breeding season. We encourage researchers to develop the use of this PCA approach as it could help clarify the complexity of the underlying mechanisms determining foraging activity and we propose that it should be used as a first step of foraging behaviour analysis, before examining a particular relationship.

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References

  • Barbraud C, Weimerskirch H (2005) Environmental conditions and breeding experience affect costs of reproduction in blue petrels. Ecology 86:682–692. doi:10.1890/04-0075

    Article  Google Scholar 

  • Barrett RT, Furness RW (1990) The prey and diving depth of seabirds on Hornøy, north Norway after a decrease in Barents Sea capelin stock. Ornis Scand 21:179–186

    Article  Google Scholar 

  • Beck CA, Bowen WD, McMillan JI (2003) Sex differences in the diving behaviour of a size-dimorphic capital breeder: the grey seal. Anim Behav 64:1–13

    Google Scholar 

  • Bethge P, Nicol S, Culik BM, Wilson RP (1997) Diving behaviour and energetics in breeding little penguins (Eudyptula minor). J Zool 242:483–502

    Article  Google Scholar 

  • Boyd IL, Reid K, Bevani RM (1995) Swimming speed and location of time during the dive cycle in Antarctic fur seals. Anim Behav 50:769–784

    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 

  • Chiaradia A, Nisbet I (2006) Plasticity in parental provisioning and chick growth in little penguins Eudyptula minor in years of high and low breeding success. Ardea 2:257–270

    Google Scholar 

  • Chiaradia A, Costalunga A, Kerry K (2003) The diet of little penguins Eudyptula minor at Phillip Island, Victoria, following the 1995 mass mortality of one of their main prey, the pilchard Sardinops sagax. Emu 103:43–48

    Article  Google Scholar 

  • Chiaradia A, Ropert-Coudert Y, Kato A, Mattern T, Yorke J (2007) Diving behaviour of little penguins from four colonies across their whole distribution range: bathymetry affecting diving effort and fledging success. Mar Biol 151:1535–1542

    Article  Google Scholar 

  • Collins M, Cullen JM, Dann P (1999) Seasonal and annual foraging movements of little penguins from Phillip Island, Victoria. Wildl Res 26:705–721

    Article  Google Scholar 

  • Croxall J, Davis R, O’Connell M (1988) Diving patterns in relation to diet of gentoo and macaroni penguins at South Georgia. Condor 90:157–167

    Article  Google Scholar 

  • Dann P (1992) Distribution, population trends and factors influencing the population size of little penguins Eudyptula minor on Phillip Island, Victoria. Emu 91:263–272

    Article  Google Scholar 

  • Dann P, Cullen JM, Jessop RE (1995) The cost of reproduction in little penguins. In: Dann P, Norman FI, Reilly P (eds) The penguins: ecology and management. Surrey, Beatty & Sons, Sydney, pp 39–55

    Google Scholar 

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

    Article  Google Scholar 

  • Dunne J, Brose U, Williams RJ, Martinez ND (2005) Modeling of web dynamics: complexity-stability implications. In: Belgrano A, Scharler UM, Dunne J, Ulanowicz RE (eds) Aquatic food webs: an ecosystem approach. Oxford University Press, Oxford, pp 117–129

    Google Scholar 

  • Elliott KH, Woo K, Gaston AJ, Benvenuti S, Antonia LD, Davoren GK (2008) Seabird foraging behaviour indicates prey type. Mar Ecol Prog Ser 354:298–303

    Article  Google Scholar 

  • Ezard THG, Becker PH, Coulson T (2007) The correlation between age, phenotopic traits and reproductive success in common terns (Sterna hirundo). Ecology 88:2496–2504

    Article  Google Scholar 

  • Fedak MA, Lovell P, Grant SM (2001) Two approaches to compressing and interpreting time-depth recorders and satellite-linked data recorders. Mar Mamm Sci 17:94–110

    Article  Google Scholar 

  • Halsey LG, Bost CA, Handrich Y (2007) A thorough and quantified method for classifying seabird diving behaviour. Polar Biol 30:991–1004

    Article  Google Scholar 

  • Holmes DJ, Flückiger R, Austad SN (2001) Comparitive biology of aging in birds: an update. Exp Gerontol 36:869–883

    Article  CAS  Google Scholar 

  • Hussell DJT (1988) Supply and demand in tree swallow broods: a model of parent-offspring food-provisioning interactions in birds. Am Nat 131:175–202

    Article  Google Scholar 

  • Jolliffe IT (1986) Principal component analysis. Springer-Verlag, Berlin

    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

    Article  Google Scholar 

  • Kato A, Watanuki Y, Naito Y (2003) Annual and seasonal changes in foraging site and diving behavior in Adélie penguins. Polar Biol 26:389–395

    Google Scholar 

  • Kato A, Ropert-Coudert Y, Chiaradia A (2008) Regulation of trip duration by an inshore forager, the little penguin (Eudyptula minor), during incubation. Auk 125:588–593

    Article  Google Scholar 

  • Kitaysky AC, Wingfield JC, Piatt JF (2000) Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behav Ecol 2:619–625

    Google Scholar 

  • Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–17

    Google Scholar 

  • Lescroël A, Dugger KM, Ballard G, Ainley DG (2009) Effects of individual quality, reproductive success and environmental variability on survival of a long-lived seabird. J Anim Ecol 78:798–806

    Article  Google Scholar 

  • Limmer B, Becker PH (2009) Improvement in chick provisioning with parental experience in a seabird. Anim Behav 77:1095–1101

    Article  Google Scholar 

  • Link JS (2002) Does food web theory work for marine ecosystems? Mar Ecol Prog Ser 230:1–9

    Article  Google Scholar 

  • Link JS, Stockhausen WT, Methratta ET (2005) Food web theory in marine ecosystems. In: Belgrano A, Scharler UM, Dunne J, Ulanowicz RE (eds) Aquatic food webs: an ecosystem approach. Oxford University Press, Oxford, pp 98–114

    Google Scholar 

  • Lorentsen S-H (1996) Regulation of food provisioning in the Antarctic petrel Thalassoica antarctica. J Anim Ecol 65:381–388

    Article  Google Scholar 

  • Martin K (1995) Patterns and mechanisms for age-dependent reproduction and survival in birds. Am Zool 35:340–348

    Google Scholar 

  • Meijer T, Drent R (1999) Re-examination of the capital and income dichotomy in breeding birds. Ibis 141:399–414

    Article  Google Scholar 

  • Morrison ML, Ralph CJ, Verner J, Jehl JRJ (1990) Avian foraging: theory, methodology, and applications. Stud Avian Biol 13:1–515

    Google Scholar 

  • Nakagawa S, Waas J, Miyazaki M (2001) Heart rate changes reveal that little blue penguin chicks (Eudyptula minor) can use vocal signatures to discriminate familiar from unfamiliar chicks. Behav Ecol Sociobiol 50:180–188

    Article  Google Scholar 

  • Nisbet I, 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 

  • Piatt IJF, Sydeman WJ, Wiese F (2007) Introduction: seabirds as indicators of marine ecosystems. Mar Ecol Prog Ser 352:199–204

    Article  Google Scholar 

  • Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846

    Article  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN: 3-900051-07-0. http://www.R-project.org

  • Ropert-Coudert Y, Grémillet D, Kato A (2006a) Swim speed of free-ranging great cormorants. Mar Biol 149:415–422

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ropert-Coudert Y, Kato A, Chiaradia A (2009) Impact of small-scale environmental perturbations on local marine food resources: a case study of a predator, the little penguin. Proc R Soc B 276:4105–4109

    Article  Google Scholar 

  • Rutz 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 

  • Sakomoto KQ, Sato K, Ishizuka M, Watanuki Y, Takahashi A, Daunt F, Wanless S (2009) Can ethograms be automatically generated using body acceleration data from free-ranging birds? PLoS one 4:e5379. doi:5310.1371/journal.pone.0005379

    Article  Google Scholar 

  • Schreer JF, O’Hara Hines RJ, Kovacs KM (1998) Classification of dive profiles: a comparison of statistical clustering techniques and unsupervised artificial neural networks. J Agric Biol Envir Stat 3:383–404

    Article  Google Scholar 

  • Sydeman WJ, Penniman JF, Penniman TM, Pyle P, Ainley DG (1991) Breeding performance in the western gull: effects of parental age, timing of breeding and year in relation to food availability. J Anim Ecol 60:135–149

    Article  Google Scholar 

  • Takahashi A, Kuroki M, Niizuma Y, Watanuki Y (1999) Parental food provisioning is unrelated to manipulated offspring food demand in a nocturnal single-provisioning alcid, the rhinoceros auklet. J Avian Biol 30:486–490

    Article  Google Scholar 

  • Takahashi A, Watanuki Y, Sato K, Kato A, Arai N, Nishikawa J, Naito Y (2003) Parental foraging effort and offspring growth in Adélie penguins: does working hard improve reproductive success? Funct Ecol 17:590–597

    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 

  • Watanuki Y, Wanless S, Harris M, Lovvorn JR, Miyazaki M, Tanaka H, Sato K (2006) Swim speeds and stroke patterns in wing-propelled divers: a comparison among alcids and a penguin. J Exp Biol 209:1217–1230

    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 27:1042–1054

    Article  Google Scholar 

  • Wilson RP, Pütz K, Bost C-A, Culik BM, Bannasch R, Reins T, Adelung D (1993) Diel dive depth in penguins in relation to diel vertical migration of prey: whose dinner by candlelight? Mar Ecol Prog Ser 94:101–104

    Article  Google Scholar 

  • Wilson RP, Bost CA, Pütz K, Charrassin JB, Culik BM, Adelung D (1997a) Southern rockhopper penguin Eudyptes chrysocome chrysocome foraging at Possession Island. Polar Biol 17:323–329

    Article  CAS  Google Scholar 

  • Wilson RP, Pütz K, Peters G, Culik B, Scolaro JA, Charrassin JB, Ropert-Coudert Y (1997b) Long-term attachment of transmitting and recording devices to penguins and other seabirds. Wildl Soc Bull 25:101–106

    Google Scholar 

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Acknowledgments

We thank P. Fallow for her help in the field, T. P. Nanuk for invaluable input in the manuscript and T. J. Preston for reviewing the manuscript. This work was supported by the BHP-Billiton, the Japan Science Society, the Australian Academy of Science, the University of Strasbourg, the Penguin Foundation and the Japan Society for the Promotion of Science. Field work protocol was approved by the ethics committee of the Phillip Island Nature Park with a research permit issued by the Department of Sustainability and Environment of Victoria, Australia.

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Correspondence to I. Zimmer.

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Communicated by M. E. Hauber.

I. Zimmer, Y. Ropert-Coudert, A. Kato and A. Chiaradia contributed equally to the work.

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Table 2 Summary of the foraging parameters used in the PCA and life history traits of little penguins

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Zimmer, I., Ropert-Coudert, Y., Poulin, N. et al. 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 (2011). https://doi.org/10.1007/s00227-010-1594-2

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