Variation in reactions to aposematic prey is common among conspecific individuals of bird predators. It may result from different individual experience but it also exists among naive birds. This variation may possibly be explained by the effect of personality--a complex of correlated, heritable behavioural traits consistent across contexts. In the great tit (Parus major), two extreme personality types have been defined. 'Fast' explorers are bold, aggressive and routine-forming; 'slow' explorers are shy, non-aggressive and innovative. Influence of personality type on unlearned reaction to aposematic prey, rate of avoidance learning and memory were tested in naive, hand-reared great tits from two opposite lines selected for exploration (slow against fast). The birds were subjected to a sequence of trials in which they were offered aposematic adult firebugs (Pyrrhocoris apterus). Slow birds showed a greater degree of unlearned wariness and learned to avoid the firebugs faster than fast birds. Although birds of both personality types remembered their experience, slow birds were more cautious in the memory test. We conclude that not only different species but also populations of predators that differ in proportions of personality types may have different impacts on survival of aposematic insects under natural conditions.

Department of Zoology Faculty of Science Charles University Vinicná 7 128 44 Praha 2 Czech Republic

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Aldrich J. R.1988Chemical ecology of the Heteroptera. Ann. Rev. Entomol. 33, 211–238 (doi:10.1146/annurev.en.33.010188.001235) DOI

Arnold K. E., Ramsay S. L., Donaldson C., Adam A.2007Parental prey selection affects risk-taking behaviour and spatial learning in avian offspring. Proc. R. Soc. B 274, 2563–2569 (doi:10.1098/rspb.2007.0687) PubMed DOI PMC

Benus R. F., den Daas S., Koolhaas J. M., van Oortmerssen G. A.1990Routine formation and flexibility in social and non-social behaviour of aggressive and non-aggressive male mice. Behaviour 112, 176–193 (doi:10.1163/156853990X00185) DOI

Boogert N. J., Reader S. M., Laland K. N.2006The relation between social rank, neophobia and individual learning in starlings. Anim. Behav. 72, 1229–1239 (doi:10.1016/j.anbehav.2006.02.021) DOI

Brower L. P.1988Avian predation on the monarch butterfly and its implications for mimicry theory. In Mimicry and the evolutionary process (ed. Brower L. P.), pp. 4–6 Chicago, IL: University of Chicago Press

Brydges N. M., Colegrave N., Heathcote R. J. P., Braithwaite V. A.2008Habitat stability and predation pressure affect temperament behaviours in populations of three-spined sticklebacks. J. Anim. Ecol. 77, 229–235 (doi:10.1111/j.1365-656.2008.01343.x) PubMed DOI

Carere C., van Oers K.2004Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress. Physiol. Behav. 82, 905–912 (doi:10.1016/j.physbeh.2004.07.009) PubMed DOI

Carere C., Groothuis T. G. G., Möstl E., Daan S., Koolhaas J. M.2003aFecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress. Horm. Behav. 43, 540–548 (doi:10.1016/S0018-506X(03)00065-5) PubMed DOI

Carere C., Havekes R., Oorebeek M., Koolhaas J. M., Groothuis T. G. G.2003b. Food finding abilities in two lines of great tits (Parus major) selected for different ‘personalities’. Personalities as epigenetic suites of traits. A study on a passerine Bird (C. Carere). PhD dissertation, University of Groningen, pp. 42–56

Coleman K., Wilson D. S.1998Shyness and boldness in pumpkinseed sunfish: individual differences are context-specific. Anim. Behav. 56, 927–936 (doi:10.1006/anbe.1998.0852) PubMed DOI

Drent P. J., van Oers K., van Noordwijk A. J.2003Realized heritability of personalities in the great tit (Parus major). Proc. R. Soc. Lond. B 270, 45–51 (doi:10.1098/rspb.2002.2168) PubMed DOI PMC

Dugatkin L. A., Alfieri M. S.2003Boldness, behavioural inhibition and learning. Ethol. Ecol. Evol. 15, 43–49

Endler J. A., Mappes J.2004Predator mixes and the conspicuousness of the aposematic signal. Am. Nat. 163, 232–247 PubMed

Exnerová A., Landová E., Štys P., Fuchs R., Prokopová M., Cehláriková P.2003Reactions of passerine birds to aposematic and non-aposematic firebugs (Pyrrhocoris apterus; Heteroptera). Biol. J. Linn. Soc. 78, 517–525 (doi:10.1046/j.0024-4066.2002.00161.x) DOI

Exnerová A., Svádová K., Štys P., Barcalová S., Landová E., Prokopová M., Fuchs R., Socha R.2006Importance of colour in the reaction of passerine predators to aposematic prey: an experiment with mutants of Pyrrhocoris apterus (Heteroptera). Biol. J. Linn. Soc. 88, 143–153 (doi:10.1111/j.1095-8312.2006.00611.x) DOI

Exnerová A., Štys P., Fučíková E., Veselá S., Svádová K., Prokopová M., Jarošík V., Fuchs R., Landová E.2007Avoidance of aposematic prey in European tits (Paridae): learned or innate? Behav. Ecol. 18, 148–156 (doi:10.1093/beheco/arl061) DOI

Exnerová A., Svádová K., Fousová P., Fučíková E., Ježová D., Niederlová A., Kopečková M., Štys P.2008European birds and aposematic Heteroptera: review of comparative experiments. Bull. Insectol. 61, 163–165

Farine J. P., Bonnard O., Brossut R., Le Quere J. L.1992Chemistry of defensive secretion in nymphs and adults of firebug, Pyrrhocoris apterus L. (Heteroptera, Pyrrhocoridae). J. Chem. Ecol. 8, 1673–1682 PubMed

Fucikova E., Drent P. J., Smits N., van Oers K.2009Handling stress as a measurement of personality in great tit nestlings (Parus major). Ethology 115, 366–374 (doi:10.1111/j.1439-0310.2009.01618.x) DOI

Garamszegi L. Z., Eens M., Török J.2008Birds reveal their personality when singing. PLoS ONE 3, e2647 (doi:10.1371/journal.pone.0002647) PubMed DOI PMC

Greenberg R.1990Ecological plasticity, neophobia, and resource use in birds. Stud. Avian Biol. 13, 431–437

Greenberg R.2003The role of neophobia and neophilia in the development of innovative behaviour of birds. In Animal innovation (eds Reader S. M., Laland K. N.), pp. 175–196 Oxford, UK: Oxford University Press

Jones R. B., Mills A. D., Faure J. M.1991Genetic and experiential manipulation of fear-related behavior in Japanese quail chicks (Coturnix coturnix japonica). J. Comp. Psychol. 105, 15–24 (doi:10.1037/0735-7036.105.1.15) PubMed DOI

Korsten P., et al. In press Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations. Mol. Ecol. PubMed

Lindström L., Alatalo R. V., Mappes J.1999Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey. Behav. Ecol. 10, 317–322 (doi:10.1093/beheco/10.3.317) DOI

Marchetti C., Drent P. J.2000Individual differences in the use of social information in foraging by captive great tits. Anim. Behav. 60, 131–140 (doi:10.1006/anbe.2000.1443) PubMed DOI

Marples N. M., Kelly D. J.1999Neophobia and dietary conservatism: two distinct processes? Evol. Ecol. 13, 641–653 (doi:10.1023/A:1011077731153) DOI

Marples N. M., Roper T. J., Harper D. G. C.1998Responses of wild birds to novel prey: evidence of dietary conservatism. Oikos 83, 161–165 (doi:10.2307/3546557) DOI

Marples N. M., Kelly D. J., Thomas R. J.2005The evolution of warning coloration is not paradoxical. Evolution 59, 933–940 PubMed

Marples N. M., Quinlan M., Thomas R. J., Kelly D. J.2007Deactivation of dietary wariness through experience of novel food. Behav. Ecol. 18, 803–810 (doi:10.1093/beheco/arm053) DOI

MathSoft 1997S-plus 4. Guide to statistics: data analysis Seattle, WA: MathSoft Inc

Mettke-Hofmann C., Ebert C., Schmidt T., Steiger S., Stieb S.2005Personality traits in resident and migratory warbler species. Behaviour 42, 1363–1381

Ruxton G. D., Sherratt T. N., Speed M. P.2004Avoiding attack New York, NY: Oxford University Press

Sih A., Bell A. M., Johnson J. C., Ziemba R. E.2004Behavioural syndromes: an integrative overview. Q. Rev. Biol. 79, 241–277 PubMed

Sillén-Tullberg B.1985Higher survival of an aposematic than of a cryptic form of a distasteful bug. Oecologia 67, 411–415 (doi:10.1007/BF00384948) PubMed DOI

Sillén-Tullberg B., Wiklund C., Järvi T.1982Aposematic coloration in adults and larvae of Lygaeus equestris and its bearing on Müllerian mimicry: an experimental study on predation on living bugs by the great tit Parus major. Oikos 39, 131–136 (doi:10.2307/3544476) DOI

Sneddon L. U.2003The bold and the shy: individual differences in rainbow trout. J. Fish Biol. 62, 971–975 (doi:10.1046/j.1095-8649.2003.00084.x) DOI

Socha R., Němec V.1992Pteridine analysis in five body-colour mutations of Pyrrhocoris apterus (Heteroptera, Pyrrhocoridae). Acta Entomol. Bohemoslov. 89, 195–203

Svádová K., Exnerová A., Štys P., Landová E., Valenta J., Fučíková A., Socha R.2009Role of different colours of aposematic insects in learning, memory and generalization of naive bird predators. Anim. Behav. 77, 327–336 (doi:10.1016/j.anbehav.2008.09.034) DOI

van Oers K., Drent P. J., de Goede P., van Noordwijk A. J.2004aRealized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc. R. Soc. Lond. B 271, 65–73 (doi:10.1098/rspb.2003.2518) PubMed DOI PMC

van Oers K., de Jong G., Drent P. J., van Noordwijk A. J.2004bGenetic correlations of avian personality traits: correlated response to artificial selection. Behav. Genet. 34, 611–619 (doi:10.1007/s10519-004-5588-z) PubMed DOI

van Oers K., Klunder M., Drent P. J.2005Context dependence of avian personalities: risk-taking behavior in a social and a non-social situation. Behav. Ecol. 16, 716–723 (doi:10.1093/beheco/ari045) DOI

Verbeek M. E. M., Drent P. J., Wiepkema P. R.1994Consistent individual differences in early exploratory behaviour of male great tits. Anim. Behav. 48, 1113–1121 (doi:10.1006/anbe.1994.1344) DOI

Verbeek M. E. M., Boon A., Drent P. J.1996Exploration, aggressive behaviour and dominance in pair-wise confrontations of juvenile male great tits. Behaviour 133, 945–963 (doi:10.1163/156853996X00314) DOI

Webster S. J., Lefebvre L.2001Problem solving and neophobia in a columbiform-passeriform assemblage in Barbados. Anim. Behav. 62, 23–32 (doi:10.1006/anbe.2000.1725) DOI