Journal of Ethology

, Volume 35, Issue 1, pp 101–108 | Cite as

Personality and urbanization: behavioural traits and DRD4 SNP830 polymorphisms in great tits in Barcelona city

  • Sepand Riyahi
  • Mats Björklund
  • Fernando Mateos-Gonzalez
  • Juan Carlos Senar
Article

Abstract

Most examples of adaptation to the urban environment relate to plasticity processes rather than to natural selection. Personality, however, defined as consistent individual differences in behaviour related to exploration, caution, and neophobia, is a good behavioural candidate character to study natural selection in relation to the urban habitat due to its heritable variation. The aim of this paper was to analyse variation in personality by comparing urban and forest great tits Parus major using standard tests of exploratory behaviour and boldness. We studied personality in 130 wild great tits captured in Barcelona city and nearby forests and found that urban birds were more explorative and bolder towards a novel object than forest birds. Genotype frequencies of the DRD4 SNP830 polymorphism, a gene region often associated with personality variation, varied significantly between forest and urban birds. Behavioural scores, however, were not correlated with this polymorphism in our population. Exploration scores correlated to boldness for forest birds but not for urban birds. Our findings suggest that the novel selection pressures of the urban environment favour the decoupling of behavioural traits that commonly form behavioural syndromes in the wild.

Keywords

Parus major Urban Boldness Exploratory behaviour Candidate gene 

Notes

Acknowledgments

We thank Alexandre Roulin for comments on an earlier version of the paper. This work was supported by funds from the Ministry of Economy and Competitivity, Spanish Research Council (CGL2012-38262 and CGL2016-79568-C3-3-P) (to J. C. S.), a research grant from the British Ornithology Union (to S. R.), and a FPI BES-2007-16320 grant to F. M. G. (Spanish Ministry of Science and Technology). We thank the Institute of Parks and Gardens for allowing us to sample birds in the Barcelona city parks, Leopoldo Gil for allowing us to sample birds in Can Catà forest area, and the Institut Botànic de Barcelona, especially Alfonso Susanna, for allowing us to use their molecular labs. We also thank Lluïsa Arroyo, Ferrán Bustos and Emilio Pagani-Núñez for their help in the field and in captivity work, and David Carrasco and Carolyn Newey for help with the English. Captive birds were handled with the permission of the Departament d’Agricultura, Generalitat de Catalunya (licences 2012-SF/518, 2013-SF/677 and 2014-SF/090).

References

  1. Adams CE, Lindsey KJ, Ash SJ (2006) Urban wildlife management. CRC, New YorkGoogle Scholar
  2. Balen JHV (1967) The significance of variations in body weight and wing length in the Great Tit, Parus major. Ardea 55:1–59Google Scholar
  3. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evolut Biol 18:464–473CrossRefGoogle Scholar
  4. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834CrossRefPubMedGoogle Scholar
  5. Björklund M, Ruiz I, Senar JC (2010) Genetic differentiation in the urban habitat: the great tits (Parus major) of the parks of Barcelona city. Biol J Linn Soc 99:9–19CrossRefGoogle Scholar
  6. Bókony V, Kulcsár A, Tóth Z, Liker A (2012) Personality traits and behavioral syndromes in differently urbanized populations of house sparrows (Passer domesticus). PLoS One 7:e36639CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brown C (2012) Experience and learning in changing environments. In: Candolin U, Wong BBM (eds) Behavioural responses to a changing world: mechanisms and consequences. Oxford University Press, Oxford, pp 46–60CrossRefGoogle Scholar
  8. Budaev SV (1997) The statistical analysis of behavioural latency measures. ISCP Newslett 14:1–4Google Scholar
  9. Carere C, Drent PJ, Privitera L, Koolhaas JM, Groothuis TGG (2005) Personalities in great tits, Parus major: stability and consistency. Anim Behav 70:795–805CrossRefGoogle Scholar
  10. Cole EF, Quinn JL (2012) Personality and problem-solving performance explain competitive ability in the wild. Proc R Soc B Biol Sci 279:1168–1175CrossRefGoogle Scholar
  11. Cole EF, Cram DL, Quinn JL (2011) Individual variation in spontaneous problem-solving performance among wild great tits. Anim Behav 81:491–498CrossRefGoogle Scholar
  12. Development Core Team R (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  13. Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184CrossRefGoogle Scholar
  14. Dingemanse NJ, Both C, Drent PJ, Van Oers K, Van Noordwijk AJ (2002) Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim Behav 64:929–938CrossRefGoogle Scholar
  15. Dingemanse NJ, Both C, Van Noordwijk AJ, Rutten AJ, Drent PJ (2003) Natal dispersal and personalities in great tits (Parus major). Proc R Soc Lond B 270:741–747CrossRefGoogle Scholar
  16. Drent PJ, Van Oers K, Van Noordwijk AJ (2003) Realized heritability of personalities in the great tit (Parus major). Proc R Soc Lond B 270:45–51CrossRefGoogle Scholar
  17. Evans KL (2010) Individual species and urbanisation. In: Gaston KJ (ed) Urban ecology. Cambridge University Press, Cambridge, pp 53–87CrossRefGoogle Scholar
  18. Evans KL, Gaston KJ, Sharp SP, McGowan A, Hatchwell BJ (2009) The effect of urbanisation on avian morphology and latitudinal gradients in body size. Oikos 118:251–259CrossRefGoogle Scholar
  19. Evans J, Boudreau K, Hyman J (2010a) Behavioural syndromes in urban and rural populations of song sparrows. Ethology 116:588–595Google Scholar
  20. Evans KL, Hatchwell BJ, Parnell M, Gaston KJ (2010b) A conceptual framework for the colonisation of urban areas: the blackbird Turdus merula as a case study. Biol Rev 85:643–667PubMedGoogle Scholar
  21. Fidler AE, van Oers K, Drent PJ, Kuhn S, Mueller JC, Kempenaers B (2007) Drd4 gene polymorphisms are associated with personality variation in a passerine bird. Proc R Soc Lond B 274:1685–1691CrossRefGoogle Scholar
  22. Finke MD (2002) Complete nutrient composition of commercially raised invertebrates used as food for insectivores. Zoo Biol 21:269–285CrossRefGoogle Scholar
  23. Garroway CJ, Sheldon BC (2013) Urban behavioural adaptation. Mol Ecol 22:3430–3432CrossRefPubMedGoogle Scholar
  24. Gaston KJ (2010) Urban ecology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  25. Hahs AK, Evans KL (2015) Expanding fundamental ecological knowledge by studying urban ecosystems. Funct Ecol 29:863–867CrossRefGoogle Scholar
  26. Hasegawa M, Ligon RA, Giraudeau M, Watanabe M, McGraw KJ (2014) Urban and colorful male house finches are less aggressive. Behav Ecol 25:641–649CrossRefGoogle Scholar
  27. Jenni L, Winkler R (1994) Moult and ageing of European Passerines. Academic, LondonGoogle Scholar
  28. Karlsson Green K, Eroukhmanoff F, Harris S, Pettersson LB, Svensson EI (2016) Rapid changes in genetic architecture of behavioural syndromes following colonization of a novel environment. J Evolut Biol 29:144–152CrossRefGoogle Scholar
  29. Korsten P, Mueller JC, Hermannstadter C, Bouwman KM, Dingemanse NJ, Drent PJ, Liedvogel M, Matthysen E, Van Oers K, Van Overveld T, Patrick SC, Quinn JL, Sheldon BC, Tinbergen JM, Kempenaers B (2010) Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations. Mol Ecol 19:832–843CrossRefPubMedGoogle Scholar
  30. Korsten P, van Overveld T, Adriaensen F, Matthysen E (2013) Genetic integration of local dispersal and exploratory behaviour in a wild bird. Nat Commun 4:2362CrossRefPubMedGoogle Scholar
  31. Krebs JR (1982) Territorial defence in the great tit (Parus major): do residents always win? Behav Ecol Sociobiol 11:185–194CrossRefGoogle Scholar
  32. Lubjuhn T (1998) Effects of blood sampling in great tits. J Field Ornithol 69:595–602Google Scholar
  33. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sunderland, MAGoogle Scholar
  34. Macleod R, Gosler AG, Cresswell W (2005) Diurnal mass gain strategies and perceived predation risk in the great tit Parus major. J Anim Ecol 74:956–964CrossRefGoogle Scholar
  35. Marchetti C, Drent PJ (2000) Individual differences in the use of social information in foraging by captive great tits. Anim Behav 60:131–140CrossRefPubMedGoogle Scholar
  36. Marzluff J, Bowman R, Donnelly R (2001) Avian ecology and conservation in an urbanizing world. Kluwer, New YorkCrossRefGoogle Scholar
  37. Miranda AC, Schielzeth H, Sonntag T, Partecke J (2013) Urbanization and its effects on personality traits: a result of microevolution or phenotypic plasticity? Glob Change Biol 19:2634–2644CrossRefGoogle Scholar
  38. Møller AP (2012) Reproductive behaviour. In: Candolin U, Wong BBM (eds) Behavioural responses to a changing world: mechanisms and consequences. Oxford University Press, Oxford, pp 106–118CrossRefGoogle Scholar
  39. Mueller JC, Korsten P, Hermannstaedter C, Feulner T, Dingemanse NJ, Matthysen E, van Oers K, van Overveld T, Patrick SC, Quinn JL, Riemenschneider M, Tinbergen JM, Kempenaers B (2013) Haplotype structure, adaptive history and associations with exploratory behaviour of the DRD4 gene region in four great tit (Parus major) populations. Mol Ecol 22:2797–2809CrossRefPubMedGoogle Scholar
  40. Pagani-Núñez E, Senar JC (2014) Are colorful males of great tits Parus major better parents? Parental investment is a matter of quality. Acta Oecol 55:23–28CrossRefGoogle Scholar
  41. Quinn JL, Patrick SC, Bouwhuis S, Wilkin TA, Sheldon BC (2009) Heterogeneous selection on a heritable temperament trait in a variable environment. J Anim Ecol 78:1203–1215CrossRefPubMedGoogle Scholar
  42. Quinn JL, Cole EF, Patrick SC, Sheldon BC (2011) Scale and state dependence of the relationship between personality and dispersal in a great tit population. J Anim Ecol 80:918–928CrossRefPubMedGoogle Scholar
  43. Reale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev Cam Philos Soc 82:291–318CrossRefGoogle Scholar
  44. Riyahi S, Sánchez-Delgado M, Calafell F, Monk D, Senar JC (2015) Combined epigenetic and intraspecific variation of the DRD4 and SERT genes influence novelty seeking behavior in great tit Parus major. Epigenetics 10:516–525CrossRefPubMedPubMedCentralGoogle Scholar
  45. Roulin A (2013) Ring recoveries of dead birds confirm that darker pheomelanic barn owls disperse longer distances. J Ornithol 154:871–874CrossRefGoogle Scholar
  46. Ryan AM, Partan SR (2014) Urban wildlife behavior. In: McCleery RA, Moorman CE, Peterson MN (eds) Urban wildlife conservation: theory and practice. Springer, Berlin, pp 149–173Google Scholar
  47. Saino N, Romano M, Scandolara C, Rubolini D, Ambrosini R, Caprioli M, Costanzo A, Romano A (2014) Brownish, small and lousy barn swallows have greater natal dispersal propensity. Anim Behav 87:137–146CrossRefGoogle Scholar
  48. Scales J, Hyman J, Hughes M (2011) Behavioral syndromes break down in urban song sparrow populations. Ethology 117:887–895CrossRefGoogle Scholar
  49. Senar JC, Domènech J, Carrascal LM, Moreno E (1997) A funnel trap for the capture of tits. Butll GCA 14:17–24Google Scholar
  50. Senar JC, Conroy MJ, Quesada J, Mateos-Gonzalez F (2014) Selection based on the size of the black tie of the great tit may be reversed in urban habitats. Ecol Evol 4:2625–2632CrossRefPubMedPubMedCentralGoogle Scholar
  51. Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trend Ecol Evol 21:186–191CrossRefGoogle Scholar
  52. Sih A, Kats LB, Maurer EF (2003) Behavioural correlations across situations and the evolution of antipredator behaviour in a sunfish-salamander system. Anim Behav 65:29–44CrossRefGoogle Scholar
  53. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trend Ecol Evol 19:372–378CrossRefGoogle Scholar
  54. Skaug HFD, Nielsen A, Magnusson A, Bolker B (2013) GlmmADMB package, 0.6. 7.1 edn. http://glmmadmb.r-forge.r-project.org/glmmADMB.html. Accessed 28 Sep 2016
  55. Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112CrossRefGoogle Scholar
  56. StatSoft I (2013) Electronic statistics textbook. Tulsa, OK. http://www.statsoft.com/textbook/. Accessed 28 Sep 2016
  57. Svensson L (1992) Identification guide to European passerines. Svensson, StockholmGoogle Scholar
  58. Timm K, Tilgar V, Saag P (2015) DRD4 gene polymorphism in great tits: gender-specific association with behavioural variation in the wild. Behav Ecol Sociobiol 69:729–735CrossRefGoogle Scholar
  59. Torné-Noguera A, Pagani-Núñez E, Senar JC (2014) Great tit (Parus major) breath rate in response to handling stress: urban and forest birds differ. J Orn 155:315–318CrossRefGoogle Scholar
  60. Tschirren B, Bensch S (2010) Genetics of personalities: no simple answers for complex traits. Mol Ecol 19:624–626CrossRefPubMedGoogle Scholar
  61. Tuomainen U, Candolin U (2012) Behavioural responses to human-induced environmental change. Biol Rev 86:640–657CrossRefGoogle Scholar
  62. United Nations DoEaSAPD (2014) World urbanization prospects: the 2014 revision, highlights (ST/ESA/SER.A/352). Department of Economic and Social Affairs/Population Division 3, New YorkGoogle Scholar
  63. Van Oers KV, Drent PJ, Goede P, Van Noordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc Lond B 271:65–73CrossRefGoogle Scholar
  64. Verbeek MEM, Drent PJ, Wiepkema PR (1994) Consistent individual differences in early exploratory behaviour of male great tits. Anim Behav 48:1113–1121CrossRefGoogle Scholar

Copyright information

© Japan Ethological Society and Springer Japan 2016

Authors and Affiliations

  1. 1.Evolutionary and Behavioural Ecology Research UnitNatural History Museum of BarcelonaBarcelonaSpain
  2. 2.Department of Animal Ecology, Evolutionary Biology Centre (EBC)Uppsala UniversityUppsalaSweden
  3. 3.Section of Integrative BiologyUniversity of TexasAustinUSA
  4. 4.Department of Collective Behaviour, Max Planck Institute for OrnithologyUniversity of KonstanzKonstanzGermany

Personalised recommendations