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Urbanisation and sex affect the consistency of butterfly personality across metamorphosis

  • Aurélien KaiserEmail author
  • Thomas Merckx
  • Hans Van Dyck
Original Article

Abstract

Animal behaviour may change with age, when young individuals experience different environments from adults. However, the role of ontogeny in personality traits is still open to debate and it is not clear whether individual differences in behaviour are maintained across important ontogenetic changes such as metamorphosis. Here, we repeatedly quantified personality in rural and urban populations of the speckled wood butterfly (Pararge aegeria) at the larval, pupal and adult stages. We detected significant repeatability at all life stages, showing that personality is already present at the immature stages. We found no evidence for landscape-related differences in personality traits, but adult males were bolder and more active than adult females. Adults also became bolder with trial sequence, suggesting habitation to the experimental procedure. Urbanisation, together with sex, affected relationships among larval and adult personality traits. More active larvae with short latencies resulted in more explorative adults. However, this was the case in males of urban origin only, and we detected no such correlation in females or in rural males. We suggest that harsh conditions prevailing in cities may lead to stronger trait integration across metamorphosis but also that these urbanisation-related selective pressures may act differently on males and females.

Significance statement

In many taxa, metamorphosis marks the transition between the juvenile and the adult stages. During this crucial developmental step, morphology and physiology are deeply remodelled, which may have important consequences for the behaviour of individuals. Although personality has emerged as a hot topic in behavioural ecology, little is known about the consequences of metamorphosis for personality stability. We studied rural and urban speckled wood butterflies at the immature and adult stages to examine whether insect personality is retained over metamorphosis. Sexes differed regarding boldness and activity, but rural and urban butterflies behaved similarly. Nevertheless, urbanisation affected relationships among larval and adult personality traits. Some larval and adult traits correlated in urban males, whereas this was not the case in females or in rural males. This suggests that urbanisation may alter trait combinations across metamorphosis, but this in a sex-specific manner.

Keywords

Behavioural syndrome Global change Lepidoptera Ontogeny Sexual differences 

Notes

Acknowledgements

AK is a research fellow with the Belgian Fund of Scientific Research F.S.R.-FNRS. The research was supported by ARC grant no. 10/15-031 (UCL) and IAP grant no. P7/04 ‘SPEEDY-project’ of the Belgian Science Policy Office BELSPO and by PDR-grant T.0188.14 of the F.R.S.-FNRS Fund both to HVD. This is publication number BRC 397 of the Biodiversity Research Centre (ELI/ELIB, UCL).

Supplementary material

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References

  1. Alberti M (2015) Eco-evolutionary dynamics in an urbanizing planet. Trends Ecol Evol 30:114–126.  https://doi.org/10.1016/j.tree.2014.11.007 CrossRefPubMedGoogle Scholar
  2. Alberti M, Marzluff J, Hunt VM (2017) Urban driven phenotypic changes: empirical observations and theoretical implications for eco-evolutionary feedback. Philos Trans R Soc B Biol Sci 372:20160029.  https://doi.org/10.1098/rstb.2016.0029 CrossRefGoogle Scholar
  3. Alcalay Y, Barkae ED, Ovadia O, Scharf I (2014) Consequences of the instar stage for behavior in a pit-building antlion. Behav Process 103:105–111.  https://doi.org/10.1016/j.beproc.2013.11.009 CrossRefGoogle Scholar
  4. Álvarez M, Munguira ML, Martínez-Ibáñez MD (2014) Comparative study of the morphology of stridulatory organs of the Iberian lycaenid butterfly pupae (Lepidoptera). J Morphol 275:414–430.  https://doi.org/10.1002/jmor.20224 CrossRefPubMedGoogle Scholar
  5. Amat I, Desouhant E, Gomes E, Moreau J, Monceau K (2018) Insect personality: what can we learn from metamorphosis? Curr Opin Insect Sci 27:46–51.  https://doi.org/10.1016/j.cois.2018.02.014 CrossRefPubMedGoogle Scholar
  6. Anderson BB, Scott A, Dukas R (2016) Social behavior and activity are decoupled in larval and adult fruit flies. Behav Ecol 27:820–828.  https://doi.org/10.1093/beheco/arv225 CrossRefGoogle Scholar
  7. Baker RL, Forbes MRL, Proctor HC (1992) Sexual differences in development and behaviour of larval Ischnura verticalis (Odonata: Coenagrionidae). Can J Zool 70:1161–1165.  https://doi.org/10.1139/z92-162 CrossRefGoogle Scholar
  8. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473.  https://doi.org/10.1111/j.1420-9101.2004.00817.x CrossRefPubMedGoogle Scholar
  9. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834.  https://doi.org/10.1111/j.1461-0248.2007.01081.x CrossRefPubMedGoogle Scholar
  10. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783.  https://doi.org/10.1016/j.anbehav.2008.12.022 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bergerot B, Merckx T, Van Dyck H, Baguette M (2012) Habitat fragmentation impacts mobility in a common and widespread woodland butterfly: do sexes respond differently? BMC Ecol 12:5.  https://doi.org/10.1186/1472-6785-12-5 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bink FA (1992) Atlas van de Dagvlinders van Noordwest-Europa. Schuyt & Co, Haarlem, NLGoogle Scholar
  13. Blackiston DJ, Silva Casey E, Weiss MR (2008) Retention of memory through metamorphosis: can a moth remember what it learned as a caterpillar? PLoS One 3:e1736.  https://doi.org/10.1371/journal.pone.0001736 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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.  https://doi.org/10.1371/journal.pone.0036639 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Bonier F, Martin PR, Sheldon KS, Jensen JP, Foltz SL, Wingfield JC (2007) Sex-specific consequences of life in the city. Behav Ecol 18:121–129.  https://doi.org/10.1093/beheco/arl050 CrossRefGoogle Scholar
  16. Brakefield PM, Shreeve TG, Thomas JA (1992) Avoidance, concealment, and defence. In: Dennis RLH (ed) The ecology of butterflies in Britain. Oxford University Press, Oxford, UK, pp 93–119Google Scholar
  17. Brodin T (2009) Behavioral syndrome over the boundaries of life—carryovers from larvae to adult damselfly. Behav Ecol 20:30–37.  https://doi.org/10.1093/beheco/arn111 CrossRefGoogle Scholar
  18. Brommer JE, Kluen E (2012) Exploring the genetics of nestling personality traits in a wild passerine bird: testing the phenotypic gambit. Ecol Evol 2:3032–3044.  https://doi.org/10.1002/ece3.412 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Carrete M, Tella JL (2017) Behavioral correlations associated with fear of humans differ between rural and urban burrowing owls. Front Ecol Evol 5:54.  https://doi.org/10.3389/fevo.2017.00054 CrossRefGoogle Scholar
  20. Carter AW, Paitz RT, McGhee KE, Bowden RM (2016) Turtle hatchlings show behavioral types that are robust to developmental manipulations. Physiol Behav 155:46–55.  https://doi.org/10.1016/j.physbeh.2015.11.034
  21. Charmantier A, Demeyrier V, Lambrechts M, Perret S, Grégoire A (2017) Urbanization is associated with divergence in pace-of-life in great tits. Front Ecol Evol 5:1–13.  https://doi.org/10.3389/fevo.2017.00053 CrossRefGoogle Scholar
  22. Chippindale AK, Gibson JR, Rice WR (2001) Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc Natl Acad Sci 98:1671–1675.  https://doi.org/10.1073/pnas.98.4.1671 CrossRefPubMedGoogle Scholar
  23. Cole LR (1959) On the defences of lepidopterous pupae in relation to the oviposition behaviour of certain Ichneumonidae. J Lepid Soc 13:1–10Google Scholar
  24. Consoulas C, Duch C, Bayline RJ, Levine RB (2000) Behavioral transformations during metamorphosis: remodeling of neural and motor systems. Brain Res Bull 53:571–583.  https://doi.org/10.1016/S0361-9230(00)00391-9 CrossRefPubMedGoogle Scholar
  25. Core Team R (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria URL: https://www.R-project.org/ Google Scholar
  26. Debeffe L, Lemaître JF, Bergvall UA, et al (2015) Short- and long-term repeatability of docility in the roe deer: sex and age matter. Anim Behav 109:53–63.  https://doi.org/10.1016/j.anbehav.2015.08.003
  27. Davies NB (1978) Territorial defence in the speckled wood butterfly (Pararge aegeria): the resident always wins. Anim Behav 26:138–147.  https://doi.org/10.1016/0003-3472(78)90013-1 CrossRefGoogle Scholar
  28. Denys C, Schmidt H (1998) Insect communities on experimental mugwort (Artemisia vulgaris L.) plots along an urban gradient. Oecologia 113:269–277.  https://doi.org/10.1007/s004420050378 CrossRefPubMedGoogle Scholar
  29. 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.  https://doi.org/10.1111/j.1365-2656.2007.01284.x CrossRefPubMedGoogle Scholar
  30. Dingemanse NJ, Bouwman KM, van de Pol M, van Overveld T, Patrick SC, Matthysen E, Quinn JL (2012) Variation in personality and behavioural plasticity across four populations of the great tit Parus major. J Anim Ecol 81:116–126.  https://doi.org/10.1111/j.1365-2656.2011.01877.x CrossRefPubMedGoogle Scholar
  31. Downey JC, Allyn AC (1973) Butterfly ultrastructure. I. Sound production and associated abdominal structures in pupae of Lycaenidae and Riodinidae. Bull Allyn Mus 14:1–47Google Scholar
  32. Ducatez S, Baguette M (2016) Inter-individual variation in shivering behaviour in the migratory painted lady Vanessa cardui. Ecol Entomol 41:131–137.  https://doi.org/10.1111/een.12283 CrossRefGoogle Scholar
  33. Ducatez S, Legrand D, Chaput-Bardy A et al (2012) Inter-individual variation in movement: is there a mobility syndrome in the large white butterfly Pieris brassicae? Ecol Entomol 37:377–385.  https://doi.org/10.1111/j.1365-2311.2012.01375.x CrossRefGoogle Scholar
  34. Ducatez S, Humeau A, Congretel M, Fréville H, Baguette M (2014) Butterfly species differing in mobility show different structures of dispersal-related syndromes in the same fragmented landscape. Ecography (Cop) 37:378–389.  https://doi.org/10.1111/j.1600-0587.2013.00365.x CrossRefGoogle Scholar
  35. Evans J, Boudreau K, Hyman J (2010) Behavioural syndromes in urban and rural populations of song sparrows. Ethology 116:588–595.  https://doi.org/10.1111/j.1439-0310.2010.01771.x CrossRefGoogle Scholar
  36. Feltwell J (1982) Large white butterfly: the biology, biochemistry and physiology of Pieris brassicae (Linnaeus). Dr W. Junk Publishers, The HagueGoogle Scholar
  37. Goulet CT, Ingley SJ, Scharf I, Pruitt JN (2016) Thermal effects on survival and reproductive performance vary according to personality type. Behav Ecol 27:1635–1641.  https://doi.org/10.1093/beheco/arw084 CrossRefGoogle Scholar
  38. Gyuris E, Feró O, Barta Z (2012) Personality traits across ontogeny in firebugs, Pyrrhocoris apterus. Anim Behav 84:103–109.  https://doi.org/10.1016/j.anbehav.2012.04.014
  39. Hardman SI, Dalesman S (2018) Repeatability and degree of territorial aggression differs among urban and rural great tits (Parus major). Sci Rep 8:5042.  https://doi.org/10.1038/s41598-018-23463-7 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hedrick AV, Kortet R (2012) Sex differences in the repeatability of boldness over metamorphosis. Behav Ecol Sociobiol 66:407–412.  https://doi.org/10.1007/s00265-011-1286-z CrossRefGoogle Scholar
  41. Kaiser A, Merckx T, Van Dyck H (2016) The urban heat island and its spatial scale dependent impact on survival and development in butterflies of different thermal sensitivity. Ecol Evol 6:4129–4140.  https://doi.org/10.1002/ece3.2166 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Karl I, Fischer K (2008) Why get big in the cold? Towards a solution to a life-history puzzle. Oecologia 155:215–225.  https://doi.org/10.1007/s00442-007-0902-0 CrossRefPubMedGoogle Scholar
  43. 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 Evol Biol 29:144–152.  https://doi.org/10.1111/jeb.12769 CrossRefPubMedGoogle Scholar
  44. Kralj-Fišer S, Schuett W (2014) Studying personality variation in invertebrates: why bother? Anim Behav 91:41–52.  https://doi.org/10.1016/j.anbehav.2014.02.016 CrossRefGoogle Scholar
  45. Kralj-Fišer S, Hebets EA, Kuntner M (2017) Different patterns of behavioral variation across and within species of spiders with differing degrees of urbanization. Behav Ecol Sociobiol 71:125.  https://doi.org/10.1007/s00265-017-2353-x CrossRefGoogle Scholar
  46. Lagucki E, Burdine JD, McCluney KE (2017) Urbanization alters communities of flying arthropods in parks and gardens of a medium-sized city. PeerJ 5:e3620.  https://doi.org/10.7717/peerj.3620 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lane SM, Briffa M (2017) Boldness is for rookies: prefight boldness and fighting success in a sea anemone. Anim Behav 132:13–20.  https://doi.org/10.1016/j.anbehav.2017.07.012 CrossRefGoogle Scholar
  48. Lapiedra O, Chejanovski Z, Kolbe JJ (2017) Urbanization and biological invasion shape animal personalities. Glob Chang Biol 23:592–603.  https://doi.org/10.1111/gcb.13395 CrossRefPubMedGoogle Scholar
  49. Martin JGA, Réale D (2008) Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. Anim Behav 75:309–318.  https://doi.org/10.1016/j.anbehav.2007.05.026 CrossRefGoogle Scholar
  50. Merckx T, Van Dyck H (2005) Mate location behaviour of the butterfly Pararge aegeria in woodland and fragmented landscapes. Anim Behav 70:411–416.  https://doi.org/10.1016/j.anbehav.2004.12.005 CrossRefGoogle Scholar
  51. Merckx T, Souffreau C, Kaiser A, Baardsen LF, Backeljau T, Bonte D, Brans KI, Cours M, Dahirel M, Debortoli N, de Wolf K, Engelen JMT, Fontaneto D, Gianuca AT, Govaert L, Hendrickx F, Higuti J, Lens L, Martens K, Matheve H, Matthysen E, Piano E, Sablon R, Schön I, van Doninck K, de Meester L, van Dyck H (2018) Body-size shifts in aquatic and terrestrial urban communities. Nature 558:113–116.  https://doi.org/10.1038/s41586-018-0140-0 CrossRefPubMedGoogle Scholar
  52. Miranda AC, Schielzeth H, Sonntag T, Partecke J (2013) Urbanization and its effects on personality traits: a result of microevolution or phenotypic plasticity? Glob Chang Biol 19:2634–2644.  https://doi.org/10.1111/gcb.12258 CrossRefPubMedGoogle Scholar
  53. Monceau K, Moreau J, Richet J, Motreuil S, Moret Y, Dechaume-Moncharmont FX (2017) Larval personality does not predict adult personality in a holometabolous insect. Biol J Linn Soc 120:869–878.  https://doi.org/10.1093/biolinnean/blw015 CrossRefGoogle Scholar
  54. Moran NP, Mossop KD, Thompson RM, Wong BBM (2016) Boldness in extreme environments: temperament divergence in a desert-dwelling fish. Anim Behav 122:125–133.  https://doi.org/10.1016/j.anbehav.2016.09.024 CrossRefGoogle Scholar
  55. Moran NP, Mossop KD, Thompson RM, Chapple DG, Wong BBM (2017) Rapid divergence of animal personality and syndrome structure across an arid-aquatic habitat matrix. Oecologia 185:55–67.  https://doi.org/10.1007/s00442-017-3924-2 CrossRefPubMedGoogle Scholar
  56. Müller T, Müller C (2015) Behavioural phenotypes over the lifetime of a holometabolous insect. Front Zool 12:S8.  https://doi.org/10.1186/1742-9994-12-S1-S8 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Müller T, Müller C (2017) Phenotype of a leaf beetle larva depends on host plant quality and previous test experience. Behav Process 142:40–45.  https://doi.org/10.1016/j.beproc.2017.05.017 CrossRefGoogle Scholar
  58. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956.  https://doi.org/10.1111/j.1469-185X.2010.00141.x CrossRefPubMedGoogle Scholar
  59. Niemelä PT, Dingemanse NJ (2018) Meta-analysis reveals weak associations between intrinsic state and personality. Proc R Soc B Biol Sci 285:20172823.  https://doi.org/10.1098/rspb.2017.2823 CrossRefGoogle Scholar
  60. Oliver TH, Marshall HH, Morecroft MD, Brereton T, Prudhomme C, Huntingford C (2015) Interacting effects of climate change and habitat fragmentation on drought-sensitive butterflies. Nat Clim Chang 5:941–945.  https://doi.org/10.1038/nclimate2746 CrossRefGoogle Scholar
  61. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318.  https://doi.org/10.1111/j.1469-185X.2007.00010.x CrossRefPubMedGoogle Scholar
  62. Rodrigues AS, Botina L, Nascimento CP, Gontijo LM, Torres JB, Guedes RNC (2016) Ontogenic behavioral consistency, individual variation and fitness consequences among lady beetles. Behav Process 131:32–39.  https://doi.org/10.1016/j.beproc.2016.08.003 CrossRefGoogle Scholar
  63. Royauté R, Buddle CM, Vincent C (2014) Interpopulation variations in behavioral syndromes of a jumping spider from insecticide-treated and insecticide-free orchards. Ethology 120:127–139.  https://doi.org/10.1111/eth.12185 CrossRefGoogle Scholar
  64. Rudin FS, Briffa M (2012) Is boldness a resource-holding potential trait? Fighting prowess and changes in startle response in the sea anemone, Actinia equina. Proc R Soc B Biol Sci 279:1904–1910.  https://doi.org/10.1098/rspb.2011.2418 CrossRefGoogle Scholar
  65. Scales J, Hyman J, Hughes M (2011) Behavioral syndromes break down in urban song sparrow populations. Ethology 117:887–895.  https://doi.org/10.1111/j.1439-0310.2011.01943.x CrossRefGoogle Scholar
  66. Schuett W, Delfs B, Haller R, Kruber S, Roolfs S, Timm D, Willmann M, Drees C (2018) Ground beetles in city forests: does urbanization predict a personality trait? PeerJ 6:e4360.  https://doi.org/10.7717/peerj.4360 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Schweiger O, Dormann CF, Bailey D, Frenzel M (2006) Occurrence pattern of Pararge aegeria (Lepidoptera: Nymphalidae) with respect to local habitat suitability, climate and landscape structure. Landsc Ecol 21:989–1001.  https://doi.org/10.1007/s10980-005-6057-7 CrossRefGoogle Scholar
  68. Scott JA (1974) Lifespan of butterflies. J Res Lepid 12:225–230Google Scholar
  69. Senar JC, Garamszegi LZ, Tilgar V, Biard C, Moreno-Rueda G, Salmón P, Rivas JM, Sprau P, Dingemanse NJ, Charmantier A, Demeyrier V, Navalpotro H, Isaksson C (2017) Urban great tits (Parus major) show higher distress calling and pecking rates than rural birds across Europe. Front Ecol Evol 5:163.  https://doi.org/10.3389/fevo.2017.00163 CrossRefGoogle Scholar
  70. Shochat E, Stefanov WL, Whitehouse MEA, Faeth SH (2004) Urbanization and spider diversity: influences of human modification of habitat structure and productivity. Ecol Appl 14:268–280.  https://doi.org/10.1890/02-5341 CrossRefGoogle Scholar
  71. Shreeve TG (1984) Habitat selection, mate location, and microclimatic constraints on the activity of the speckled wood butterfly Pararge aegeria. Oikos 42:371–377.  https://doi.org/10.2307/3544407 CrossRefGoogle Scholar
  72. Shreeve TG (1986) Egg-laying by the speckled wood butterfly (Pararge aegeria): the role of female behaviour, host plant abundance and temperature. Ecol Entomol 11:229–236.  https://doi.org/10.1111/j.1365-2311.1986.tb00298.x CrossRefGoogle Scholar
  73. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277.  https://doi.org/10.1086/422893 CrossRefPubMedGoogle Scholar
  74. Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112.  https://doi.org/10.1016/j.anbehav.2013.01.023 CrossRefGoogle Scholar
  75. Stamps J, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325.  https://doi.org/10.1111/j.1469-185X.2009.00103.x CrossRefPubMedGoogle Scholar
  76. Stanley CR, Mettke-Hofmann C, Preziosi RF (2017) Personality in the cockroach Diploptera punctata: evidence for stability across developmental stages despite age effects on boldness. PLoS One 12:e0176564.  https://doi.org/10.1371/journal.pone.0176564 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Stoffel MA, Nakagawa S, Schielzeth H (2017) rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol 8:1639–1644.  https://doi.org/10.1111/2041-210X.12797 CrossRefGoogle Scholar
  78. Talloen W, Van Dyck H, Lens L (2004) The cost of melanization: butterfly wing coloration under environmental stress. Evolution (N Y) 58:360–366.  https://doi.org/10.1111/j.0014-3820.2004.tb01651.x CrossRefGoogle Scholar
  79. Tanaka Y (1989) Genetic variance and covariance patterns of larval development in the small white butterfly Pieris rapae crucivora Boisduval. Res Popul Ecol (Kyoto) 31:311–324.  https://doi.org/10.1007/BF02513208 CrossRefGoogle Scholar
  80. Travassos MA, Pierce NE (2000) Acoustics, context and function of vibrational signalling in a lycaenid butterfly–ant mutualism. Anim Behav 60:13–26.  https://doi.org/10.1006/anbe.1999.1364 CrossRefPubMedGoogle Scholar
  81. Tüzün N, Debecker S, Op de Beeck L, Stoks R (2015) Urbanisation shapes behavioural responses to a pesticide. Aquat Toxicol 163:81–88.  https://doi.org/10.1016/j.aquatox.2015.04.002 CrossRefPubMedGoogle Scholar
  82. Tüzün N, Müller S, Koch K, Stoks R (2017) Pesticide-induced changes in personality depend on the urbanization level. Anim Behav 134:45–55.  https://doi.org/10.1016/j.anbehav.2017.10.007 CrossRefGoogle Scholar
  83. Van Dyck H, Matthysen E (1998) Thermoregulatory differences between phenotypes in the speckled wood butterfly: hot perchers and cold patrollers? Oecologia 114:326–334.  https://doi.org/10.1007/s004420050454 CrossRefPubMedGoogle Scholar
  84. Vonk J, Weiss A, Kuczaj SA (2017) Personality in nonhuman animals. Springer International Publishing, ChamCrossRefGoogle Scholar
  85. Wexler Y, Subach A, Pruitt JN, Scharf I (2016) Behavioral repeatability of flour beetles before and after metamorphosis and throughout aging. Behav Ecol Sociobiol 70:745–753.  https://doi.org/10.1007/s00265-016-2098-y CrossRefGoogle Scholar
  86. Wilson ADM, Krause J (2012) Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav Ecol 23:1316–1323.  https://doi.org/10.1093/beheco/ars123 CrossRefGoogle Scholar
  87. Wormington JD, Juliano SA (2014) Hunger-dependent and sex-specific antipredator behaviour of larvae of a size-dimorphic mosquito. Ecol Entomol 39:548–555.  https://doi.org/10.1111/een.12129 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Wuerz Y, Krüger O (2015) Personality over ontogeny in zebra finches: long-term repeatable traits but unstable behavioural syndromes. Front Zool 12:S9.  https://doi.org/10.1186/1742-9994-12-S1-S9

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Behavioural Ecology and Conservation Group, Biodiversity Research Centre, Earth and Life InstituteUniversité catholique de Louvain (UCL)Ottignies-Louvain-la-NeuveBelgium

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