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Mechanisms of Behavioural Change in Urban Animals: The Role of Microevolution and Phenotypic Plasticity

  • Ana Catarina Miranda
Chapter

Abstract

A key question in evolutionary behavioural ecology is how species cope with changes in their environments. In the last centuries, humans have caused dramatic changes in our planet that have affected the way many animals behave. In order to live in cities, most animals are forced to adjust their behaviour and life histories to the new urban habitat. While growing evidence reports behavioural differences between rural and urban conspecifics as common and cross-taxonomical, the mechanisms underlying such differences in behaviour remain largely unknown. Recent research using animals with limited experience of their natural urban or rural environments points to the existence of intrinsic differences in behaviour between rural and urban conspecifics. This suggests that phenotypic plasticity might not be the only mechanism explaining behavioural differences between rural and urban individuals and that differences in individually consistent behavioural traits could also be the result of microevolution in the urban environment.

Knowing that urbanization is and will continue to be a major environmental challenge to most living organisms, it is urgent to understand the mechanisms allowing animals to cope with our urbanizing world. In this chapter, I focus on the existence of different behavioural phenotypes between rural and urban animals and on the possible mechanisms leading to such behavioural differences.

Keywords

Animal personalities Anthropogenic environmental change Behavioural syndromes Colonization Microevolution Phenotypic plasticity Urbanization 

Notes

Acknowledgements

I thank the editors, Enrique Murgui and Marcus Hedblom, for the kind invitation to contribute to this book.

References

  1. Adams RA, Lengas BJ, Bekoff M (1987) Variations in avoidance responses to humans by black-tailed prairie dogs (Cynomys ludovicianus). J Mammal 68:686–689. doi: 10.2307/1381606 CrossRefGoogle Scholar
  2. Adkins-Regan E (2005) Hormones and animal social behavior. Princeton University Press, PrincetonGoogle Scholar
  3. Araya-Ajoy YG, Dingemanse NJ (2013) Characterizing behavioural “characters”: a conceptual and statistical framework. Proc R Soc B 2014 281 20132645. doi: 10.1098/rspb.2013.2645
  4. Arnfield AJ (2003) Two decades of urban climate research: a review of turbulence, exchanges of energy and water, and the urban heat island. Int J Climatol 23:1–26. doi: 10.1002/joc.859 CrossRefGoogle Scholar
  5. Ashlee McGiffin AL (2013) Tolerance of human approaches by Common Mynas along an urban-rural gradient. Emu 113:154. doi: 10.1071/MU12107 CrossRefGoogle Scholar
  6. Atwell JW, Cardoso GC, Whittaker DJ et al (2012) Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation. Behav Ecol 23:960–969. doi: 10.1093/beheco/ars059 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Badyaev AV (2005) Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc Biol Sci 272:877–886. doi: 10.1098/rspb.2004.3045 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bateman PW, Fleming PA (2012) Big city life: carnivores in urban environments. J Zool 287:1–23. doi: 10.1111/j.1469-7998.2011.00887.x CrossRefGoogle Scholar
  9. Baudains TP, Lloyd P (2007) Habituation and habitat changes can moderate the impacts of human disturbance on shorebird breeding performance. Anim Conserv 10:400–407. doi: 10.1111/j.1469-1795.2007.00126.x CrossRefGoogle Scholar
  10. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473. doi: 10.1111/j.1420-9101.2004.00817.x CrossRefPubMedGoogle Scholar
  11. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834. doi: 10.1111/j.1461-0248.2007.01081.x CrossRefPubMedGoogle Scholar
  12. Boake CRB (1989) Repeatability: its role in evolutionary studies of mating behavior. Evol Ecol 3:173–182. doi: 10.1007/BF02270919 CrossRefGoogle Scholar
  13. 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:e36639. doi: 10.1371/journal.pone.0036639 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bowers MA, Breland B (1996) Foraging of gray squirrels on an urban-rural gradient: use of the gud to assess anthropogenic impact. Ecol Appl 6:1135. doi: 10.2307/2269597 CrossRefGoogle Scholar
  15. Brearley G, McAlpine C, Bell S, Bradley A (2012) Influence of urban edges on stress in an arboreal mammal: a case study of squirrel gliders in southeast Queensland, Australia. Landsc Ecol 27:1407–1419. doi: 10.1007/s10980-012-9790-8 CrossRefGoogle Scholar
  16. Buchanan KL, Partecke J (2012) The endocrine system: can homeostasis be maintained in a changing world? In: Candolin U, Wong BBM (eds) Behavioural responses to a changing world: mechanisms and consequences. Oxford University Press, Oxford, pp 145–158Google Scholar
  17. Candler S, Bernal XE (2015) Differences in neophobia between cane toads from introduced and native populations. Behav Ecol 26:97–104. doi: 10.1093/beheco/aru162 CrossRefGoogle Scholar
  18. Carere C, Maestripieri D (2013) Animal personalities – behavior, physiology, and evolution. University of Chicago Press, Chicago, ILCrossRefGoogle Scholar
  19. Carrete M, Tella JL (2011) Inter-individual variability in fear of humans and relative brain size of the species are related to contemporary urban invasion in birds. PLoS One 6:e18859. doi: 10.1371/journal.pone.0018859 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Carrete M, Tella JL (2013) High individual consistency in fear of humans throughout the adult lifespan of rural and urban burrowing owls. Sci Rep. doi: 10.1038/srep03524 PubMedGoogle Scholar
  21. Case TJ (1996) Global patterns in the establishment and distribution of exotic birds. Biol Conserv 78:69–96. doi: 10.1016/0006-3207(96)00019-5 CrossRefGoogle Scholar
  22. Chamberlain DE, Cannon AR, Toms MP et al (2009) Avian productivity in urban landscapes: a review and meta-analysis. Ibis 151:1–18. doi: 10.1111/j.1474-919X.2008.00899.x CrossRefGoogle Scholar
  23. Chapman T, Rymer T, Pillay N (2012) Behavioural correlates of urbanisation in the Cape ground squirrel Xerus inauris. Naturwissenschaften 99:893–902. doi: 10.1007/s00114-012-0971-8 CrossRefPubMedGoogle Scholar
  24. Clucas B, Marzluff JM (2012) Attitudes and actions toward birds in urban areas: human cultural differences influence bird behavior. Auk 129:8–16. doi: 10.1525/auk.2011.11121 CrossRefGoogle Scholar
  25. Cooke AS (1980) Observations on how close certain passerine species will tolerate an approaching human in rural and suburban areas. Biol Conserv 18:85–88. doi: 10.1016/0006-3207(80)90072-5 CrossRefGoogle Scholar
  26. Daniels G, Kirkpatrick J (2016) Ecology and conservation of Australian urban and exurban avifauna. In: Murgui E, Hedblom M (eds) Ecology and conservation of birds in urban environments. Springer, Heidelberg, pp 343–370Google Scholar
  27. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54. doi: 10.1111/1365-2656.12013 CrossRefPubMedGoogle Scholar
  28. Dingemanse NJ, Wright J, Kazem AJN et al (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138. doi: 10.1111/j.1365-2656.2007.01284.x CrossRefPubMedGoogle Scholar
  29. Dominoni DM (2016) Ecological effects of light pollution: how can we improve our understanding using light loggers on individual animals. In: Murgui E, Hedblom M (eds) Ecology and conservation of birds in urban environments. Springer, Heidelberg, pp 251–270Google Scholar
  30. Dominoni DM, Helm B, Lehmann M et al (2013) Clocks for the city: circadian differences between forest and city songbirds. Proc R Soc B Biol Sci 280:20130593. doi: 10.1098/rspb.2013.0593 CrossRefGoogle Scholar
  31. Edelaar P, Bolnick DI (2012) Non-random gene flow: an underappreciated force in evolution and ecology. Trends Ecol Evol 27:659–665. doi: 10.1016/j.tree.2012.07.009 CrossRefPubMedGoogle Scholar
  32. Engelhardt SC, Weladji RB (2011) Effects of levels of human exposure on flight initiation distance and distance to refuge in foraging eastern gray squirrels (Sciurus carolinensis). Can J Zool 89:823–830. doi: 10.1139/Z11-054 CrossRefGoogle Scholar
  33. Evans J, Boudreau K, Hyman J (2010) Behavioural syndromes in urban and rural populations of song sparrows. Ethology 116:588–595. doi: 10.1111/j.1439-0310.2010.01771.x Google Scholar
  34. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman, Essex, EnglandGoogle Scholar
  35. Fokidis HB, Orchinik M, Deviche P (2009) Corticosterone and corticosteroid binding globulin in birds: relation to urbanization in a desert city. Gen Comp Endocrinol 160:259–270. doi: 10.1016/j.ygcen.2008.12.005 CrossRefPubMedGoogle Scholar
  36. French SS, Fokidis HB, Moore MC (2008) Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) across an urban-rural gradient. J Comp Physiol B 178:997–1005. doi: 10.1007/s00360-008-0290-8 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Gaston KJ (2010) Urban ecology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  38. Gleditsch J (2016) The role of invasive plant species in urban avian conservation. In: Murgui E, Hedblom M (eds) Ecology and conservation of birds in urban environments. Springer, Heidelberg, pp 413–424Google Scholar
  39. Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates of phenotypic change in wild animal populations. Mol Ecol 17:20–29. doi: 10.1111/j.1365-294X.2007.03428.x CrossRefPubMedGoogle Scholar
  40. Houghtaling K, Kight S (2006) Turn alternation in response to substrate vibration by terrestrial isopods, Porcellio laevis (Isopoda: Oniscidea) from rural and urban habitats in New Jersey, USA. Entomol News 117:149–154. doi: 10.3157/0013-872X(2006)117[149:TAIRTS]2.0.CO;2 CrossRefGoogle Scholar
  41. Johnsen TS (1998) Behavioural correlates of testosterone and seasonal changes of steroids in red-winged blackbirds. Anim Behav 55:957–965. doi: 10.1006/anbe.1997.0642 CrossRefPubMedGoogle Scholar
  42. Józkowicz A, Górska-Kłęk L (1996) Activity patterns of the mute swans Cygnus olor wintering in rural and urban areas: a comparison. Acta Ornithol 31:45–51Google Scholar
  43. Kekkonen J (2016) Pollutants in urbanized areas – direct and indirect effects on bird populations. In: Murgui E, Hedblom M (eds) Ecology and conservation of birds in urban environments. Springer, Heidelberg, pp 227–250Google Scholar
  44. Kenney SP, Knight RL (1992) Flight distances of black-billed magpies in different regimes of human density and persecution. Condor 94:545–547. doi: 10.2307/1369231 CrossRefGoogle Scholar
  45. Kitchen K, Lill A, Price M (2010) Tolerance of human disturbance by urban magpie-larks. Aust Field Ornithol 27:1–9Google Scholar
  46. Klausnitzer B (1989) Verstädterung von Tieren. A. Ziemsen, Wittenberg LutherstadtGoogle Scholar
  47. Knight RL, Grout DJ, Temple SA (1987) Nest-defense behavior of the American crow in urban and rural areas. Condor 89:175–177. doi: 10.2307/1368772 CrossRefGoogle Scholar
  48. Lehrer EW, Schooley RL, Whittington JK (2012) Survival and antipredator behavior of woodchucks (Marmota monax) along an urban–agricultural gradient. Can J Zool 90:12–21. doi: 10.1139/z11-107 CrossRefGoogle Scholar
  49. Liker A, Bókony V (2009) Larger groups are more successful in innovative problem solving in house sparrows. Proc Natl Acad Sci USA 106:7893–7898. doi: 10.1073/pnas.0900042106 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lourenço PM, Silva A, Santos CD et al (2008) The energetic importance of night foraging for waders wintering in a temperate estuary. Acta Oecol 34:122–129. doi: 10.1016/j.actao.2008.04.005 CrossRefGoogle Scholar
  51. Lowry H, Lill A, Wong BBM (2011) Tolerance of auditory disturbance by an avian urban adapter, the noisy miner. Ethology 117:490–497. doi: 10.1111/j.1439-0310.2011.01902.x CrossRefGoogle Scholar
  52. Lowry H, Lill A, Wong BBM (2013) Behavioural responses of wildlife to urban environments. Biol Rev Camb Philos Soc 88:537–549. doi: 10.1111/brv.12012 CrossRefPubMedGoogle Scholar
  53. Magle S, Zhu J, Crooks KR (2005) Behavioral responses to repeated human intrusion by black-tailed prairie dogs (Cynomys ludovicianus). J Mammal 86:524–530. doi: 10.1644/1545-1542(2005)86[524:BRTRHI]2.0.CO;2 CrossRefGoogle Scholar
  54. Martin LB, Fitzgerald L (2005) A taste for novelty in invading house sparrows, Passer domesticus. Behav Ecol 16:702–707. doi: 10.1093/beheco/ari044 CrossRefGoogle Scholar
  55. Mccleery RA (2009) Changes in fox squirrel anti-predator behaviors across the urban–rural gradient. Landsc Ecol 24:483–493. doi: 10.1007/s10980-009-9323-2 CrossRefGoogle Scholar
  56. McGlothlin JW, Jawor JM, Ketterson ED (2007) Natural variation in a testosterone‐mediated trade‐off between mating effort and parental effort. Am Nat 170:864–875. doi: 10.1086/522838 PubMedGoogle Scholar
  57. 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 19:2634–2644. doi: 10.1111/gcb.12258 CrossRefGoogle Scholar
  58. Møller AP (2008) Flight distance of urban birds, predation, and selection for urban life. Behav Ecol Sociobiol 63:63–75. doi: 10.1007/s00265-008-0636-y CrossRefGoogle Scholar
  59. Møller AP, Ibáñez-Álamo JD (2012) Escape behaviour of birds provides evidence of predation being involved in urbanization. Anim Behav 84:341–348. doi: 10.1016/j.anbehav.2012.04.030 CrossRefGoogle Scholar
  60. Møller AP, Tryjanowski P (2014) Direction of approach by predators and flight initiation distance of urban and rural populations of birds. Behav Ecol. doi: 10.1093/beheco/aru073 Google Scholar
  61. Mueller JC, Partecke J, Hatchwell BJ et al (2013) Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds. Mol Ecol 22:3629–3637. doi: 10.1111/mec.12288 CrossRefPubMedGoogle Scholar
  62. Papp S, Vincze E, Preiszner B et al (2014) A comparison of problem-solving success between urban and rural house sparrows. Behav Ecol Sociobiol 69:471–480. doi: 10.1007/s00265-014-1859-8 CrossRefGoogle Scholar
  63. Partan SR, Fulmer AG, Gounard MAM, Redmond JE (2010) Multimodal alarm behavior in urban and rural gray squirrels studied by means of observation and a mechanical robot. Curr Zool 56:313–326Google Scholar
  64. Partecke J (2013) Mechanisms of phenotypic responses following colonization of urban areas: from plastic to genetic adaptation. In: Gil D, Brumm H (eds) Avian urban ecology. Oxford University Press, OxfordGoogle Scholar
  65. Partecke J, Van’t Hof TJ, Gwinner E (2005) Underlying physiological control of reproduction in urban and forest-dwelling European blackbirds Turdus merula. J Avian Biol 36:295–305. doi: 10.1111/j.0908-8857.2005.03344.x CrossRefGoogle Scholar
  66. Partecke J, Schwabl I, Gwinner E (2006) Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecology 87:1945–1952. doi: 10.1890/0012-9658(2006)87[1945:SATCUA]2.0.CO;2 CrossRefPubMedGoogle Scholar
  67. Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc B Biol Sci 270:1433–1440. doi: 10.1098/rspb.2003.2372 CrossRefGoogle Scholar
  68. Prosser C, Hudson S, Thompson MB (2006) Effects of urbanization on behavior, performance, and morphology of the garden skink, Lampropholis guichenoti. J Herpetol 40:151–159. doi: 10.1670/38-05A.1 CrossRefGoogle Scholar
  69. Royauté R, Buddle CM, Vincent C (2013) Interpopulation variations in behavioral syndromes of a jumping spider from insecticide-treated and insecticide-free orchards. Ethology. doi: 10.1111/eth.12185 Google Scholar
  70. Santos CD, Miranda AC, Granadeiro JP et al (2010) Effects of artificial illumination on the nocturnal foraging of waders. Acta Oecol 36:166–172. doi: 10.1016/j.actao.2009.11.008 CrossRefGoogle Scholar
  71. Scales J, Hyman J, Hughes M (2011) Behavioral syndromes break down in urban song sparrow populations. Ethology 117:887–895. doi: 10.1111/j.1439-0310.2011.01943.x CrossRefGoogle Scholar
  72. Schielzeth H, Bolund E, Kempenaers B, Forstmeier W (2011) Quantitative genetics and fitness consequences of neophilia in zebra finches. Behav Ecol 22:126–134. doi: 10.1093/beheco/arq184 CrossRefGoogle Scholar
  73. Schoech SJ, Bowman R, Reynolds SJ (2004) Food supplementation and possible mechanisms underlying early breeding in the Florida scrub-Jay (Aphelocoma coerulescens). Horm Behav 46:565–573CrossRefPubMedGoogle Scholar
  74. Seress G, Bókony V, Heszberger J, Liker A (2011) Response to predation risk in urban and rural house sparrows. Ethology 117:896–907. doi: 10.1111/j.1439-0310.2011.01944.x CrossRefGoogle Scholar
  75. Shochat E, Warren P, Faeth S et al (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191. doi: 10.1016/j.tree.2005.11.019 CrossRefPubMedGoogle Scholar
  76. Shochat E, Lerman SB, Anderies JM et al (2010) Invasion, competition, and biodiversity loss in urban ecosystems. Bioscience 60:199–208. doi: 10.1525/bio.2010.60.3.6 CrossRefGoogle Scholar
  77. Sih A, Stamps J, Yang LH et al (2010) Behavior as a key component of integrative biology in a human-altered world. Integr Comp Biol 50:934–944. doi: 10.1093/icb/icq148 CrossRefPubMedGoogle Scholar
  78. Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4:367–387. doi: 10.1111/j.1752-4571.2010.00166.x CrossRefPubMedPubMedCentralGoogle Scholar
  79. Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112. doi: 10.1016/j.anbehav.2013.01.023 CrossRefGoogle Scholar
  80. St Clair JJH, Garcia-Peña GE, Woods RW, Székely T (2010) Presence of mammalian predators decreases tolerance to human disturbance in a breeding shorebird. Behav Ecol 21:1285–1292. doi: 10.1093/beheco/arq144 CrossRefGoogle Scholar
  81. Sweeney K, Gadd RDH, Hess ZL et al (2013) Assessing the effects of rearing environment, natural selection, and developmental stage on the emergence of a behavioral syndrome. Ethology 119:436–447. doi: 10.1111/eth.12081 CrossRefGoogle Scholar
  82. Thibert-Plante X, Hendry AP (2011) The consequences of phenotypic plasticity for ecological speciation. J Evol Biol 24:326–342. doi: 10.1111/j.1420-9101.2010.02169.x CrossRefPubMedGoogle Scholar
  83. United Nations (2014) World urbanization prospects: the 2014 revision. Department of Economic and Social Affairs, Population Division, United Nations, New YorkGoogle Scholar
  84. Valcarcel A, Fernandez-Juricic E (2009) Antipredator strategies of house finches: are urban habitats safe spots from predators even when humans are around? Behav Ecol Sociobiol 63:673–685. doi: 10.1007/s00265-008-0701-6 CrossRefGoogle Scholar
  85. Van Buskirk J (2012) Behavioural plasticity and environmental change. In: Candolin U, Wong BBM (eds) Behavioural responses to a changing world: mechanisms and consequences. Oxford University Press, Oxford, pp 145–158CrossRefGoogle Scholar
  86. van Oers K, Drent PJ, de Goede P, van Noordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc B Biol Sci 271:65–73. doi: 10.1098/rspb.2003.2518 CrossRefGoogle Scholar
  87. van Oers K, Buchanan KL, Thomas TE, Drent PJ (2011) Correlated response to selection of testosterone levels and immunocompetence in lines selected for avian personality. Anim Behav 81:1055–1061. doi: 10.1016/j.anbehav.2011.02.014 CrossRefGoogle Scholar
  88. Vincze E, Papp S, Preiszner B et al (2014) Does urbanization facilitate individual recognition of humans by house sparrows? Anim Cogn 18:291–298. doi: 10.1007/s10071-014-0799-z CrossRefPubMedGoogle Scholar
  89. Wolf M, van Doorn GS, Weissing FJ (2008) Evolutionary emergence of responsive and unresponsive personalities. Proc Natl Acad Sci USA. doi: 10.1073/pnas.0805473105 Google Scholar

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Authors and Affiliations

  1. 1.Postgraduate Programme in Biodiversity and ConservationUniversidade Federal do MaranhãoSão LuísBrazil
  2. 2.Max Planck Institute for OrnithologyRadolfzellGermany
  3. 3.Department of BiologyUniversity of KonstanzConstanceGermany

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