Abstract
During the last century, the human footprint on natural ecosystems has increased strongly and human-altered habitats such as urban and agricultural areas have extended globally. Despite their negative impacts on biodiversity, these habitats offer unique opportunities to study how native species respond to novel environmental conditions. Here, we studied phenotypic divergence associated with colonization of human-altered habitats in the Speckled wood (Pararge aegeria). We reared butterflies of woodland, urban and agricultural origins under common garden conditions and we measured boldness and activity at the adult stage. Both behavioural traits were repeatable at the individual level (i.e. personality traits), but we found weak evidence for ecotype-related differences in mean boldness and activity. In line with urban areas being stressful habitats, we found that boldness and activity traits correlate in urban butterflies, while we found no such syndrome in woodland and agricultural butterflies. Our results show that urbanization can alter some aspects of personality in an insect species, but they do not support the prediction that anthropogenic habitats favour boldness.
Significance statement
Human activities such as urbanization and intensive agriculture strongly alter terrestrial ecosystems and they are among the most significant threats to biodiversity. To tolerate human-dominated landscapes, many vertebrate species show behavioural shifts towards bold personalities, but similar responses remain rather overlooked in invertebrate taxa. Here, we studied the progeny of woodland, agricultural and urban Speckled woods reared under common garden conditions and we assessed their personality. We found little evidence for differences in personality traits among landscape types, but the behavioural syndrome linking boldness and activity was detected only in urban butterflies. This shows that urbanization can indeed shape some aspects of personality in invertebrates.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data set generated and analysed during the current study is available from the corresponding author on reasonable request.
References
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
Allendorf FW, Hard JJ (2009) Human-induced evolution caused by unnatural selection through harvest of wild animals. Proc Natl Acad Sci 106:9987–9994. https://doi.org/10.1073/pnas.0901069106
Baxter-Gilbert J, Riley JL, Whiting MJ (2019) Bold New World: urbanization promotes an innate behavioral trait in a lizard. Behav Ecol Sociobiol 73:105. https://doi.org/10.1007/s00265-019-2713-9
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
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
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
Brans KI, Engelen JMT, Souffreau C, De Meester L (2018) Urban hot-tubs: local urbanization has profound effects on average and extreme temperatures in ponds. Landsc Urban Plan 176:22–29. https://doi.org/10.1016/j.landurbplan.2018.03.013
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
Charmantier A, Demeyrier V, Lambrechts M, Perret S, Grégoire A (2017) Urbanization Is Associated with Divergence in Pace-of-Life in Great Tits. Urbanization is associated with divergence in pace-of-life in great tits Front Ecol Evol 5:5. https://doi.org/10.3389/fevo.2017.00053
Concepción ED, Moretti M, Altermatt F, Nobis MP, Obrist MK (2015) Impacts of urbanisation on biodiversity: the role of species mobility, degree of specialisation and spatial scale. Oikos 124:1571–1582. https://doi.org/10.1111/oik.02166
Diamond SE, Chick LD, Perez A, Strickler SA, Zhao C (2018) Evolution of plasticity in the city: urban acorn ants can better tolerate more rapid increases in environmental temperature. Conserv Physiol 6:1–12. https://doi.org/10.1093/conphys/coy030
Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54. https://doi.org/10.1111/1365-2656.12013
Dingemanse NJ, Dochtermann NA, Nakagawa S (2012) Defining behavioural syndromes and the role of ‘syndrome deviation’ in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548. https://doi.org/10.1007/s00265-012-1416-2
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
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
Ellis EC, Goldewijk KK, Siebert S et al (2010) Anthropogenic transformation of the biomes, 1700 to 2000. Glob Ecol Biogeogr 19:589–606. https://doi.org/10.1111/j.1466-8238.2010.00540.x
Eötvös CB, Magura T, Lövei GL (2018) A meta-analysis indicates reduced predation pressure with increasing urbanization. Landsc Urban Plan 180:54–59. https://doi.org/10.1016/j.landurbplan.2018.08.010
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
Evans KL, Gaston KJ, Frantz AC, Simeoni M, Sharp SP, McGowan A, Dawson DA, Walasz K, Partecke J, Burke T, Hatchwell BJ (2009) Independent colonization of multiple urban centres by a formerly forest specialist bird species. Proc R Soc B Biol Sci 276:2403–2410. https://doi.org/10.1098/rspb.2008.1712
Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J stat Softw 33:1–22. https://doi.org/10.18637/jss.v033.i02
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
Hobbs RJ, Higgs E, Harris JA (2009) Novel ecosystems: implications for conservation and restoration. Trends Ecol Evol 24:599–605. https://doi.org/10.1016/j.tree.2009.05.012
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
Kaiser A, Merckx T, Van Dyck H (2018) Urbanisation and sex affect the consistency of butterfly personality across metamorphosis. Behav Ecol Sociobiol 72:188. https://doi.org/10.1007/s00265-018-2616-1
Kaiser A, Merckx T, Van Dyck H (2019a) Behavioural repeatability is affected by early developmental conditions in a butterfly. Anim Behav 157:219–226. https://doi.org/10.1016/j.anbehav.2019.08.006
Kaiser A, Merckx T, Van Dyck H (2019b) Personality traits influence contest outcome, and vice versa, in a territorial butterfly. Sci Rep 9:2778. https://doi.org/10.1038/s41598-019-39155-9
Kern EMA, Langerhans RB (2018) Urbanization drives contemporary evolution in stream fish. Glob Chang Biol 24:3791–3803. https://doi.org/10.1111/gcb.14115
Koolhaas J, Korte S, De Boer S et al (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935. https://doi.org/10.1016/S0149-7634(99)00026-3
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
Luniak M, Mulsow R, Walasz K (1990) Urbanization of the European blackbird – expansion and adaptations of urban population. In: Luniak M (ed) Urban ecological studies in central and Eastern Europe. International Symposium Warsaw, Poland, pp 187–200
McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176. https://doi.org/10.1007/s11252-007-0045-4
Merckx T, Kaiser A, Van Dyck H (2018a) Increased body size along urbanization gradients at both community and intraspecific level in macro-moths. Glob Chang Biol 24:3837–3848. https://doi.org/10.1111/gcb.14151
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 (2018b) Body-size shifts in aquatic and terrestrial urban communities. Nature 558:113–116. https://doi.org/10.1038/s41586-018-0140-0
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
Merckx T, Van Dyck H (2007) Habitat fragmentation affects habitat-finding ability of the speckled wood butterfly, Pararge aegeria L. Anim Behav 74:1029–1037. https://doi.org/10.1016/j.anbehav.2006.12.020
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
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
Niemelä PT, Dingemanse NJ (2014) Artificial environments and the study of ‘adaptive’ personalities. Trends Ecol Evol 29:245–247. https://doi.org/10.1016/j.tree.2014.02.007
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
Parris KM (2016) Ecology of urban environments. Wiley-Blackwell, Chichester, UK
Piano E, Souffreau C, Merckx T, Baardsen LF, Backeljau T, Bonte D, Brans KI, Cours M, Dahirel M, Debortoli N, Decaestecker E, de Wolf K, Engelen JMT, Fontaneto D, Gianuca AT, Govaert L, Hanashiro FTT, Higuti J, Lens L, Martens K, Matheve H, Matthysen E, Pinseel E, Sablon R, Schön I, Stoks R, van Doninck K, van Dyck H, Vanormelingen P, van Wichelen J, Vyverman W, de Meester L, Hendrickx F (2020) Urbanization drives cross-taxon declines in abundance and diversity at multiple spatial scales. Glob Chang Biol 26:1196–1211. https://doi.org/10.1111/gcb.14934
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: https://www.R-project.org/
Ramírez-Restrepo L, MacGregor-Fors I (2017) Butterflies in the city: a review of urban diurnal Lepidoptera. Urban Ecosyst 20:171–182. https://doi.org/10.1007/s11252-016-0579-4
Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio PO (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc B Biol Sci 365:4051–4063. https://doi.org/10.1098/rstb.2010.0208
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
Rivkin LR, Santangelo JS, Alberti M, Aronson MFJ, de Keyzer CW, Diamond SE, Fortin MJ, Frazee LJ, Gorton AJ, Hendry AP, Liu Y, Losos JB, MacIvor JS, Martin RA, McDonnell MJ, Miles LS, Munshi-South J, Ness RW, Newman AEM, Stothart MR, Theodorou P, Thompson KA, Verrelli BC, Whitehead A, Winchell KM, Johnson MTJ (2019) A roadmap for urban evolutionary ecology. Evol Appl 12:384–398. https://doi.org/10.1111/eva.12734
Royauté R, Buddle CM, Vincent C (2015) Under the influence: sublethal exposure to an insecticide affects personality expression in a jumping spider. Funct Ecol 29:962–970. https://doi.org/10.1111/1365-2435.12413
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
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
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. https://doi.org/10.3389/fevo.2017.00163
Sepp T, McGraw KJ, Kaasik A, Giraudeau M (2018) A review of urban impacts on avian life-history evolution: does city living lead to slower pace of life? Glob Chang Biol 24:1452–1469. https://doi.org/10.1111/gcb.13969
Serruys M, Van Dyck H (2014) Development, survival, and phenotypic plasticity in anthropogenic landscapes: trade-offs between offspring quantity and quality in the nettle-feeding peacock butterfly. Oecologia 176:379–387. https://doi.org/10.1007/s00442-014-3016-5
Seto KC, Guneralp B, Hutyra LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc Natl Acad Sci 109:16083–16088. https://doi.org/10.1073/pnas.1211658109
Settele J, Kudrna O, Harpke A et al (2008) Climatic Risk Atlas of European Butterflies. In: Climatic risk atlas of European butterflies. Pensoft, Sofia-Moscow
Shochat E, Warren P, Faeth S et al (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191. https://doi.org/10.1016/j.tree.2005.11.019
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
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
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378. https://doi.org/10.1016/j.tree.2004.04.009
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
Sprau P, Mouchet A, Dingemanse NJ (2017) Multidimensional environmental predictors of variation in avian forest and city life histories. Behav Ecol 28:59–68. https://doi.org/10.1093/beheco/arw130
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
Sullivan AP, Bird DW, Perry GH (2017) Human behaviour as a long-term ecological driver of non-human evolution. Nat Ecol Evol 1:0065. https://doi.org/10.1038/s41559-016-0065
Talloen W, Van Dyck H, Lens L (2004) The cost of melanization: butterfly wing coloration under environmental stress. Evolution 58:360–366. https://doi.org/10.1111/j.0014-3820.2004.tb01651.x
Tüzün N, Müller S, Koch K, Stoks R (2017a) 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
Tüzün N, Op de Beeck L, Brans KI et al (2017b) Microgeographic differentiation in thermal performance curves between rural and urban populations of an aquatic insect. Evol Appl 10:1067–1075. https://doi.org/10.1111/eva.12512
Urszán TJ, Garamszegi LZ, Nagy G, Hettyey A, Török J, Herczeg G (2015) No personality without experience? A test on Rana dalmatina tadpoles. Ecol Evol 5:5847–5856. https://doi.org/10.1002/ece3.1804
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
Verbeek MEM, Boon A, Drent PJ (1996) Exploration, aggressive behaviour and dominance in pair-wise confrontations of juvenile male great tits. Behaviour 133:945–963. https://doi.org/10.1163/156853996X00314
Winchell KM, Reynolds RG, Prado-Irwin SR, Puente-Rolón AR, Revell LJ (2016) Phenotypic shifts in urban areas in the tropical lizard Anolis cristatellus. Evolution 70:1009–1022. https://doi.org/10.1111/evo.12925
Acknowledgements
We thank two anonymous reviewers for their constructive comments, and Camille Turlure for help with catching and rearing butterflies. This is publication number BRC 363 of the Biodiversity Research Centre (ELI/ELIB, UCLouvain).
Funding
AK is a research fellow with the Belgian Fund of Scientific Research F.S.R.-FNRS. The research was supported by PDR grant FNRS PDR T.0188.14 and an ARC research grant of Fédération Wallonie-Bruxelles and UCLouvain (ARC-grant 17/22–086) to HVD.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
Our experimental protocol complies with all institutional guidelines at UCLouvain and the F.R.S.-FNRS on invertebrate research. No permit was necessary to perform the experiments described in the study.
Additional information
Communicated by J. C Choe
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 4249 kb)
Rights and permissions
About this article
Cite this article
Kaiser, A., Merckx, T. & Van Dyck, H. An experimental test of changed personality in butterflies from anthropogenic landscapes. Behav Ecol Sociobiol 74, 86 (2020). https://doi.org/10.1007/s00265-020-02871-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-020-02871-8