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Health-dependent vulnerability to predation affects escape responses of unguarded chinstrap penguin chicks

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Abstract

Predators may select more often to attack the more vulnerable prey or those with an inferior health status. Thus, prey should be able to assess their own vulnerability to predation and modify their antipredatory behavior accordingly. When approached by predator skuas, unguarded penguin chicks flee short distances, and usually aggregate in dense packs, but there is a clear interindividual variability in their responses under similar conditions. We hypothesized that this variability in escape responses might be related to the perceived vulnerability to predation of each individual chick. We simulated predator attacks to chinstrap penguin chicks and analyzed the sources of variation in their escape response, such as the presence of adults or the density of other chicks, and the sex, age, body condition, and health status of responding chicks. Chicks allowed shorter approach distances when they had a better health condition (i.e., a greater T-cell-mediated immunity, CMI), when they were younger, and when the density of adults around was higher. Sex and density of other chicks were not important. Similarly, chicks fled from the experimenter to longer distances when they had a lower CMI and when the density of adults was lower. Therefore, escape characteristics of chicks depended on the presence of adults that can deter predators and on the health-dependent vulnerability of chicks.

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References

  • Besnard A, Gimenez O, Lebreton JD (2002) A model for the evolution of crèching behaviour in gulls. Evol Ecol 16:489–503

    Article  Google Scholar 

  • Blanco DE, Yorio P, Boersma PD (1996) Feeding behaviour, size asymmetry, and food distribution in Magellanic penguin (Spheniscus magellanicus) chicks. Auk 113:496–498

    Google Scholar 

  • Blumstein DT (2003) Flight initiation distance in birds is dependent on intruder starting distance. J Wildl Manage 67:852–857

    Article  Google Scholar 

  • Brinkhof MWG, Heeb P, Kolliker M, Richner H (1999) Immunocompetence of nestling great tits in relation to rearing environment and parentage. Proc R Soc Lond B 266:2315–2322

    Article  Google Scholar 

  • Burger J, Gochfeld M (1981) Discrimination of the threat of direct versus tangential approach to the nest by incubating herring and great black-backed gulls. J Comp Physiol Psychol 95:676–684

    Article  Google Scholar 

  • Caraco T, Martindale S, Pulliam HR (1980) Avian time budgets and distance to cover. Auk 97:872–875

    Google Scholar 

  • Cohn LA (1997) Glucocorticoids as immunosuppressive agents. Sem Vet Med Surg Small Anim 12:150–156

    CAS  Google Scholar 

  • Crawley MJ (1993) GLIM for ecologists. Blackwell, Oxford, UK

    Google Scholar 

  • Cresswell W (1994a) Flocking is an effective anti-predation strategy in redshanks, Tringa totanus. Anim Behav 47:433–442

    Article  Google Scholar 

  • Cresswell W (1994b) Song as a pursuit-deterrent signal, and its occurrence relative to other anti-predation behaviours of skylark (Alauda arvensis) on attack by merlins (Falco columbarius). Behav Ecol Sociobiol 34:217–223

    Article  Google Scholar 

  • Cresswell W, Quinn JL (2004) Faced with a choice, sparrowhawks more often attack the more vulnerable prey group. Oikos 104:71–76

    Article  Google Scholar 

  • Creswell W, Hilton GM, Ruxton GD (2000) Evidence for a rule governing the avoidance of superfluous escape flights. Proc R Soc Lond B 267:733–737

    Article  Google Scholar 

  • Davis LS (1982) Crèching behaviour of Adèlie penguin chicks (Pygoscelis adeliae). NZ J Zool 9:279–286

    Google Scholar 

  • Ellegren H (1996) First gene on the avian W chromosome (CHD) provides a tag for universal sexing of non-ratite birds. Proc R Soc Lond B 263:1635–1641

    Article  CAS  Google Scholar 

  • Emslie SD, Karnovsky N, Trivelpiece W (1995) Avian predation at penguin colonies on King George Island, Antarctica. Wilson Bull 107:317–327

    Google Scholar 

  • Fernández-Juricic E, Jiménez MD, Lucas E (2002) Factors affecting intra- and inter-specific variations in the difference between alert distances and flight distances for birds in forested habitats. Can J Zool 80:1212–1220

    Article  Google Scholar 

  • Fitzgibbon CD (1990) Why do hunting cheetahs prefer male gazelles? Anim Behav 40:837–845

    Article  Google Scholar 

  • Frid A, Dill LM (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11

    Google Scholar 

  • Funston PJ, Mills MGL, Biggs HC (2001) Factors affecting the hunting success of male and female lions in the Kruger National Park. J Zool 253:419–431

    Article  Google Scholar 

  • Gamallo A, Villanua A, Trancho G, Fraile A (1986) Stress adaptation and adrenal activity in isolated and crowded rats. Physiol Behav 36:217–221

    Article  PubMed  CAS  Google Scholar 

  • Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546

    Article  PubMed  CAS  Google Scholar 

  • Hunter S (1991) The impact of avian predator scavengers on king penguins Aptenodytes patagonicus chicks at Marion Island. Ibis 133:343–350

    Article  Google Scholar 

  • Jackson S, Wilson RP (2002) The potential costs of flipper-bands to penguins. Funct Ecol 16:141–148

    Article  Google Scholar 

  • Jones RB, Beuving G, Blokhuis HJ (1988) Tonic immobility and heterophil/lymphocyte responses of the domestic fowl to corticosterone infusion. Physiol Behav 42:249–253

    Article  PubMed  CAS  Google Scholar 

  • Laiolo P, Tella JL, Carrete M, Serrano D, López G (2004) Distress calls may honestly signal bird quality to predators. Proc R Soc Lond B 271:S513–S515 (Suppl)

    Article  Google Scholar 

  • Lawless RM, Buttemer WA, Astheimer LB, Kerry KR (2001) The influence of thermoregulatory demand on contact crèching behaviour in Adèlie Penguin chicks. J Therm Biol 26:555–562

    Article  Google Scholar 

  • Le Bohec C, Gauthier-Clerc M, Le Maho Y (2005) The adaptive significance of crèches in the king penguin. Anim Behav 70:527–538

    Article  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeteable repeatabilities: a common mistake. Auk 104:116–121

    Google Scholar 

  • Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive and ecological perspectives. Adv Stud Behav 27:215–290

    Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Lindström KM, Van de Veen IT, Lagault BA, Lundström JO (2003) Activity and predator escape performance of common greenfinches Carduelis chloris infected with Sindbis virus. Ardea 91:103–111

    Google Scholar 

  • Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503–510

    Google Scholar 

  • López P, Hawlena D, Polo V, Amo L, Martín J (2005) Sources of individual shy-bold variations in antipredatory behaviour of male Iberian rock-lizards. Anim Behav 69:1–9

    Article  Google Scholar 

  • Martín J, López P (2000) Fleeing to unsafe refuges: effects of conspicuousness and refuge safety on the escape decisions of the lizard Psammodromus algirus. Can J Zool 78:265–270

    Article  Google Scholar 

  • Martín J, de Neve L, Fargallo JA, Polo V, Soler M (2004) Factors affecting the escape behavior of juvenile chinstrap penguins, Pygoscelis antarctica, in response to human disturbance. Polar Biol 27:775–781

    Article  Google Scholar 

  • Møller AP, Erritzøe J (2000) Predation against birds with low immunocompetence Oecologia 122:500–504

    Article  Google Scholar 

  • Moreno J, Carrascal LM, Sanz JJ, Amat JA, Cuervo JJ (1994) Hatching asynchrony, sibling hierarchies and brood reduction in the chinstrap penguin Pygoscelis antarctica. Polar Biol 14:21–30

    Article  Google Scholar 

  • Moreno J, DeLeon 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 

  • Norman FI, McFarlane RA, Ward SJ (1994) Carcasses of Adèlie penguins as a food source for south polar skuas: some preliminary observations. Wilson Bull 106:26–34

    Google Scholar 

  • Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26

    Article  Google Scholar 

  • Penteriani V, Viñuela 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 

  • Pole A, Gordon IJ, Gorman ML (2003) African wild dogs test the ‘survival of the fittest’ paradigm. Proc R Soc Lond B 270:57 (Suppl)

    Article  Google Scholar 

  • Quinn JL, Cresswell W (2004) Predator hunting behaviour and prey vulnerability. J Anim Ecol 73:143–154

    Article  Google Scholar 

  • Quinn JL, Cresswell W (2005) Personality, anti-predation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour 142:1377–1402

    Article  Google Scholar 

  • Roberts G (1996) Why individual vigilance declines as group size increases? Anim Behav 51:1077–1086

    Article  Google Scholar 

  • Smith ME, Belk MC (2001) Risk assessment in western mosquitofish (Gambusia affinis): do multiple cues have additive effects? Behav Ecol Sociobiol 51:101–107

    Article  Google Scholar 

  • Smith KG, Hunt JL (2004) On the use of spleen mass as a measure of avian immune system strength. Oecologia 138:28–31

    Article  PubMed  Google Scholar 

  • Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572

    Article  Google Scholar 

  • Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc Lond B 272:2627–2634

    Article  Google Scholar 

  • Tella JL, Forero MG, Bertellotti M, Donázar JA, Blanco G, Ceballos O (2001) Offspring body condition and immunocompetence are negatively affected by high breeding densities in a colonial sea bird: a multiscale approach. Proc R Soc Lond B 268:1–7

    Article  Google Scholar 

  • Temple SA (1986) Do predators always capture substandard individuals disproportionately from prey populations? Ecology 68:669–674

    Article  Google Scholar 

  • Van Heezik Y, Seddon PJ (1990) Effect of human disturbance on beach groups of jackass penguins. S Afr J Wildl Res 20:89–93

    Google Scholar 

  • Vega-Redondo F, Hasson O (1993) A game-theoretic model of predator–prey signaling. J Theor Biol 162:309–319

    Article  Google Scholar 

  • Viñuela J, Amat JA, Ferrer M (1995) Nest defence of nesting chinstrap penguins (Pygoscelis antarctica) against intruders. Ethology 99:323–331

    Google Scholar 

  • Viñuela J, Moreno J, Carrascal LM, Sanz JJ, Amat JA, Ferrer M, Belliure J, Cuervo JJ (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 

  • Williams TD (1995) The penguins. Oxford University Press, Oxford, UK

    Google Scholar 

  • Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Stud Behav 16:229–249

    Article  Google Scholar 

  • Yorio P, Boersma PD (1992) The effects of human disturbance on Magellanic penguin Spheniscus magellanicus behaviour and breeding success. Bird Conserv Int 2:161–173

    Article  Google Scholar 

  • Young E (1994) Skua and penguin. Cambridge University Press, Cambridge, UK

    Google Scholar 

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Acknowledgements

We thank JL Tella and JL Quinn for the helpful comments on the manuscript. This study was based on the Spanish Army Base “Gabriel de Castilla”; transport to and from Deception Island was provided by the Spanish Navy ship “Las Palmas”. We thank the cooperation offered by all participants in the Spanish Antarctic campaign 2002/2003 and especially to JC, the “man with long sideburns”, for his persistent companionship. Financial support was provided by the Spanish Antarctic Program, MCYT project BOS 2001-3170. The manipulations and experimental procedures were approved by the Scientific Committee for Antarctic Research (SCAR).

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Authors and Affiliations

  1. Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, C.S.I.C., José Gutiérrez Abascal 2, 28006, Madrid, Spain

    J. Martín, L. de Neve, V. Polo & J. A. Fargallo

  2. Departamento de Biología Animal y Ecología, Facultad de Ciencias, Universidad de Granada, 18071, Granada, Spain

    M. Soler

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  1. J. Martín
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Correspondence to J. Martín.

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Communicated by C. Brown

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Martín, J., de Neve, L., Polo, V. et al. Health-dependent vulnerability to predation affects escape responses of unguarded chinstrap penguin chicks. Behav Ecol Sociobiol 60, 778–784 (2006). https://doi.org/10.1007/s00265-006-0221-1

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