Abstract
Habitat fragmentation and ecosystem changes have the potential to affect animal populations in different ways. To effectively monitor these changes, biomonitoring tools have been developed and applied to detect changes in population structure and/or individual traits that reflect such changes. Fluctuating asymmetry (FA) represents random deviations from perfect symmetry in bilateral traits from perfect symmetry in response to genetic and/or environmental stresses. In this study, we evaluated the use of FA as a tool to monitor stress caused by forest fragmentation and edge formation, using the tropical butterfly M. helenor (Nymphalidae) as a model species. We collected adult butterflies from three fragments of Atlantic Forest in Brazil encompassing both edge and interior habitats. Four wing traits (wing length, wing width, ocelli area, and ocelli diameter) were evaluated. Butterflies captured at edge sites exhibited higher FA values for wing length and wing width compared to those captured at interior sites, whereas traits related to ocelli did not show differences between the two habitat types. Our results suggest that the differences in abiotic and biotic conditions between forest interior and edges can act as a source of stress, impacting the symmetry of flight-related traits. On the other hand, as ocelli are crucial for butterfly camouflage and counter-predator strategies, our results indicate that this trait may be more conserved. By employing FA, we identified trait-specific responses to habitat fragmentation, thus suggesting its potential as a biomarker for environmental stress that can be used in butterflies to monitor habitat quality and change.
Graphical Abstract
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 of this study are available from the corresponding author upon reasonable request.
References
Abaga NOZ, Alibert P, Dousset S et al (2011) Insecticide residues in cotton soils of Burkina Faso and effects of insecticides on fluctuating asymmetry in honey bees (Apis mellifera Linnaeus). Chemosphere 83(4):585–592. https://doi.org/10.1016/j.chemosphere.2010.12.021
Adamski P, Witkowski ZJ (2002) Increase in fluctuating asymmetry during a population extinction: the case of the apollo butterfly Parnasius apollo frankenbergeri in the Pieniny Mts. Biologia Bratislava 57:597–601
Aleixo A (1999) Effects of selective logging on a bird community in the Brazilian Atlantic Forest. The Condor 101, 537–548. https://doi.org/10.2307/1370183
Alves-Silva E, Santos JC, Cornelissen T (2018) How many leaves are enough? The influence of sample size on estimates of plant developmental instability and leaf asymmetry. Ecol Indic 89:912–924. https://doi.org/10.1016/j.ecolind.2017.12.060
Anciães M, Marini MÂ (2000) The effects of fragmentation on fluctuating asymmetry on passerine birds of Brazilian tropical forests. J Appl Ecol 37:1013–1028. https://doi.org/10.1046/j.1365-2664.2000.00554.x
Arroyo-Rodríguez V, Fahrig L, Tabarelli M et al (2020) Designing optimal human-modified landscapes for forest biodiversity conservation. Ecol Lett 23(9):1404–1420. https://doi.org/10.1111/ele.13535
Barlow J, Overal WL, Araujo IS et al (2007) The value of primary, secondary and plantation forests for fruit-feeding butterflies in the Brazilian Amazon. J Appl Ecol 44:1001–1012. https://doi.org/10.1111/j.1365-2664.2007.01347.x
Beasley DAE, Bonisoli-Alquati A, Mousseau TA (2013) The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: a meta-analysis. Ecol Indic 30:218–226. https://doi.org/10.1016/j.ecolind.2013.02.024
Benítez HA (2013) Assessment of patterns of fluctuating asymmetry and sexual dimorphism in carabid body shape. Neotrop Entomol 42:164–169. https://doi.org/10.1007/s13744-012-0107-z
Benítez HA, Lemic D, Püschel TA et al (2018) Fluctuating asymmetry indicates levels of disturbance between agricultural productions: an example in Croatian population of Pterostichus melas melas (Coleptera: Carabidae). Zool Anz 276:42–49. https://doi.org/10.1016/j.jcz.2018.07.003
Bossart JL, Opuni-Frimpong E (2009) Distance from edge determines fruit feeding butterfly community diversity in Afrotropical forest fragments. Environ Entomol 38:43–52. https://doi.org/10.1603/022.038.0107
Brown KS Jr, Freitas AVL (2000) Atlantic Forest butterflies: indicators for landscape conservation. Biotropica 32(4b):934–956. https://doi.org/10.1111/j.1744-7429.2000.tb00631.x
Chang X, Zhai B, Liu X et al (2007) Effects of temperature stress and pesticide exposure on fluctuating asymmetry and mortality of Copera annulata (Selys). Ecotoxicol Environ Saf 67:120–127. https://doi.org/10.1016/j.ecoenv.2006.04.004
Cramer P (1776) De uitlandsche Kapellen voorkomende in de drie Waereld-Deelen Asia, Africa en America. Papillons exotiques des trois parties du monde l’Asie, l’Afrique et l’Amérique. Amsterdam, S. J. Baalde; Utrecht. Barthelemy Wild and J. Van Schoonhoven Comp (8):133–155
CLB S’a, Ribeiro DB, Garcia LC et al (2014) Fruit-feeding butterfly communities are influenced by restoration age in tropical forests. Restor Ecol 22(4):480–485. https://doi.org/10.1111/rec.12091
Crespi B, Vanderkist B (1997) Fluctuating asymmetry in vestigial and functional traits of a haplodiploid insect. Heredity 79:624–630. https://doi.org/10.1038/hdy.1997.208
DeCoster G, Van Dongen S, Malaki P et al (2013) Fluctuating asymmetry and environmental stress: understanding the role of trait history. PLoS One 8(3):e57966. https://doi.org/10.1371/journal.pone.0057966
Despland E, Humire R, Martín SS (2012) Species richness and phenology of butterflies along an altitude gradient in the desert of Northern Chile. Arct Antarct Alp Res 44:423–431. https://doi.org/10.1657/1938-4246-44.4.423
DeVries PJ (1987) The butterflies of costa rica and their natural history. Princeton University Press, Princeton
DeVries PJ (1988) Stratification of fruit-feeding nymphalid butterflies in a Costa Rican Rainforest. J Res Lepid 26:98–108
DeVries PJ, Murray D, Lande R (1997) Species diversity in vertical, horizontal, and temporal dimensions of a fruit-feeding butterfly community in an Ecuadorian rainforest. Biol J Linn Soc 62:343–364. https://doi.org/10.1006/bijl.1997.0155
DeVries PJ, Penz CM, Hill RI (2010) Vertical distribution, flight behaviour and evolution of wing morphology in Morpho butterflies. J Anim Ecol 79:1077–1085. https://doi.org/10.1111/j.1365-2656.2010.01710.x
DeVries PJ, Hamm CA, Fordyce JA (2016) A standardized sampling protocol for fruit-feeding butterflies (Nymphalidae). In: Larsen, T. H. Core (ed) Standardized methods for rapid biological field assessment. Conservation International Arlington, VA. pp. 140–148
Diaz M, Pulido FJ, Moller AP (2004) Herbivore effects on developmental instability and fecundity of holm oaks. Oecologia 139:224–234. https://doi.org/10.1007/s00442-004-1491-9
Ellers J, Bax M, Van Alphen JJM (2001) Seasonal changes in female size and its relation to reproduction in the parasitoid Asobara tabida. Oikos 92:309–214. https://doi.org/10.1034/j.1600-0706.2001.920213.x
Falconer DS (1981) Introduction to quantitative genetics, 2nd edn, New York, Longman, p 386
Fermon H, Waltert M, Muhlenberg M (2003) Movement and vertical stratification of fruitfeeding butterflies in a managed West African rainforest. J. Insect Conserv 7:7–19. https://doi.org/10.1023/A:1024755819790
Fermon H, Waltert M, Vane-Wright RI et al (2005) Forest use and vertical stratification in fruit-feeding butterflies of Sulawesi, Indonesia: impacts for conservation. Biodivers Conserv 14:333–350. https://doi.org/10.1007/s10531-004-5354-9
Filgueiras BKC, Melo DHA, Leal IR et al (2016) Fruit-feeding butterflies in edge-dominated habitats: community structure, species persistence and cascade effect. J Insect Conserv 20:539–548. https://doi.org/10.1007/s10841-016-9888-4
Freitas AVL, Leal IR, Uehara-Prado M, Iannuzzi L (2006) Insetos como indicadores de conservação da paisagem. In: Biologia da conservação: essências. Rima, São Carlos, pp 357–384
Freitas AVL, Iserhard CA, Santos JP et al (2014) Studies with butterfly bait traps: an overview. Rev Colom Entomol 40(2):203–212
Freitas AVL, Muniz DG, Carreira JYO et al (2021a) Fruit-feeding butterfly assemblages in a neotropical savanna: assessing phenological patterns using baited traps. J Lep Soc 75(2):88–103. https://doi.org/10.18473/lepi.75i2.a2
Freitas AVL, Santos JP, Rosa AHB, Iserhard CA, Richter A, Siewert RR, Gueratto PE, Carreira JYO, Lourenço GM (2021b) Sampling methods for butterfies (Lepidoptera). In: Santos JC, Fernandes GW (eds) Measuring arthropod biodiversity: a handbook of sampling methods. Springer, pp 101–123
Gallagher RV, Butt N, Carthey AJR et al (2021) A guide to using species trait data in conservation. One Earth 4(7):927–936. https://doi.org/10.1016/j.oneear.2021.06.013
Graça MB, Pequeno PACL, Franklin E et al (2017) Coevolution between flight morfology, vertical stratification and sexual dimorphism: what we can learn about tropical butterflies? J Evol Biol 30(10):1862–1871. https://doi.org/10.1111/jeb.13145
Gueratto PE, Carreira JYO, Santos JP et al (2020) Effects of forest trails on the community structure of tropical butterflies. J Insect Conserv 24:309–319. https://doi.org/10.1007/s10841-019-00199-x
Guilherme DR, Souza JLP, Franklin E et al (2019) Can environmental complexity predict functional trait composition of ground-dwelling ant assemblages? A test across the Amazon Basin. Acta Oecol 99:103434. https://doi.org/10.1016/j.actao.2019.05.004
Haddad NM, Brudwig LA, Clobert J et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1(2):e1500052. https://doi.org/10.1126/sciadv.1500052
Hagen M, Kissling WD, Rasmussen C et al (2012) Biodiversity, species interactions and ecological networks in a fragmented world. In: Bohan D, Dumbrell A, Woodward G, Jackson M (eds) Advances in Ecological Research, 1st edn. Elsevier Ltd, University of Essex, Colchester, UK, pp 89–210
Henriques NR, Cornelissen TG (2019) Wing asymmetry of a butterfly community: is altitude a source of stress? Community Ecol 20(3):252–257. https://doi.org/10.1556/168.2019.20.3.5
Henriques NR, Lourenço GM, Diniz ES, Cornelissen T (2022) Is elevation a strong environmental filter? Combining taxonomy, functional traits and phylogeny of butterflies in a tropical mountain. Ecol Entomol 47:613–625. https://doi.org/10.1111/een.13145
Instituto Brasileiro de Geografia e Estatística – IBGE (2004) Vegetação. https://www.ibge.gov.br/geociencias/informacoes-ambientais/vegetacao.html
Jacquenyn H, Meester LD, Jongejans E et al (2012) Evolutionary changes in plant reproductive traits following habitat fragmentation and their consequences for population fitness. J Ecol 100:76–87. https://doi.org/10.1111/j.1365-2745.2011.01919.x
Jensen BM, Aarnes JB, Murvoll KM et al (2010) Fluctuating asymmetry and hepatic concentrations of persistent organic pollutants are associated in European shag (Phalacrocorax aristotelis) chicks. Sci Total Environ 408:578–585. https://doi.org/10.1111/j.1365-2745.2011.01919.x
Kanegae AP, Lomônaco C (2003) Plasticidade morfológica, reprodutiva e assimetria flutuante de Myzus persicae (Sulzer) (Hemiptera: Aphididae) sob diferentes temperaturas. Neotrop Entomol 32:37–43. https://doi.org/10.1590/S1519-566X2003000100005
Kodandaramaiah U (2011) The evolutionary significance of butterfly eyespots. Behav Ecol 22:1264–1271. https://doi.org/10.1093/beheco/arr123
Kodandaramaiah U, Vallin A, Wikelund C (2009) Fixed eyespot display in a butterfly thwarts attacking birds. Anim Behav 77:1415–1419. https://doi.org/10.1016/j.anbehav.2009.02.018
Lefcheck JS, Bastazini VAG, Griffin JN (2014) Choosing and using multiple traits in functional diversity research. Environ Conserv 42(2):104–107. https://doi.org/10.1017/S0376892914000307
Lens L, Dongen SV, Kark S et al (2002) Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biol Rev Biol Proc 77:27–38. https://doi.org/10.1017/s1464793101005796
Leonard RJ, Wat KKY, McArthur C, Hochuli DF (2018) Urbanisation and wing asymmetry in the western honey bee (Apis mellifera, Linnaeus 1758) at multiple scales. PeerJ 6:e5940. https://doi.org/10.7717/peerj.5940
Lourenço GM, Soares GR, Santos TP et al (2019) Equal but different: natural ecotones are dissimilar to anthropic edges. PLoS One 14:e0213008. https://doi.org/10.1371/journal.pone.0213008
Lourenço GM, Luna P, Guevara R et al (2020) Temporal shifts in butterfly diversity: responses to natural and anthropic forest transitions. J Insect Conserv 24:353–363. https://doi.org/10.1007/s10841-019-00207-0
Lourenço GM, Dátillo W, Ribeiro SP et al (2022) Biological aspects and movements of Neotropical fruit-feeding butterflies. Neotrop Entomol 51:43–53. https://doi.org/10.1007/s13744-021-00913-y
Magrach A, Lawrence WF, Larrinaga AR, Santamaria L (2014) Meta-analysis of the effects of forest fragmentation on interspecific interactions. Conserv Biol 28:1342–1348. https://doi.org/10.1111/cobi.12304
Marini-Filho OJ, Martins RP (2010) Nymphalid butterfly dispersal among forest fragments at Serra da Canastra National Park Brazil. J Insect Conserv 14:401–411. https://doi.org/10.1007/s10841-010-9271-9
Miller DG, Lane J, Senock R (2011) Butterflies as potential bioindicators of primary rainforest and oil palm plantation habitats on New Britain Papua New Guinea. Pac Conserv Biol 17:149–159. https://doi.org/10.1071/PC110149
Mikitová B, Šemeláková M, Panigaj Ľ (2022) Wing morphology and eyespot pattern of Erebia medusa (Lepidoptera, Nymphalidae) vary along an elevation gradient in the Carpathian Mountains. Nota Lepi 45:233–250. https://doi.org/10.3897/nl.45.68624
Moller AP, Thornhill R (1997) A meta-analysis of the heritability of developmental stability. J Evolut Biol 10:1–16. https://doi.org/10.1046/j.1420-9101.1997.10010001.x
Monteiro A (2015) Origin, development, and evolution of butterfly eyespots. Annu Rev Entomol 7(10):253–271. https://doi.org/10.1146/annurev-ento-010814-020942 Epub 2014 Oct 17
Murugesan SN, Connahs H, Matsuoka Y, Monteiro A (2022) Butterfly eyespots evolved via cooption of an ancestral gene-regulatory network that also patterns antennae, legs, and wings. Evolution 119(8):e2108661119. https://doi.org/10.1073/pnas.2108661119
Nascimento AR, Malinov IK, Freire G Jr et al (2020) The temporal dynamics of two Morpho Fabricius, 1807 Species (Lepidoptera: Nymphalidae) are affected differently by fire in the Brazilian Savanna. Environ Entomol 46(6):1449–1454. https://doi.org/10.1093/ee/nvaa128
Nattero J, Piccinali RV, Gaspe MS et al (2019) Fluctuating asymmetry and exposure to pyrethroid insecticides in Triatoma infestans populations in northeastern Argentina. Infect Genet Evol 74:103925. https://doi.org/10.1016/j.meegid.2019.103925
Neves FSN, Madeira BG, Oliveira VHF et al (2008) Insetos como bioindicadores dos processos de regeneração em matas secas. MG-Biota 1:46–53
Nunes LA, De AE, Marchini LC (2015) Fluctuating asymmetry in Apis melífera (Hymenoptera: Apidae) as bioindicator of anthropogenic environments. Rev Biol Trop 63(3):673–682
Palmer RA, Strobeck C (1986) Fluctuating asymmetry: measurement analysis, patterns. Annu Rev Ecol Syst 17:391–421. https://doi.org/10.1146/annurev.es.17.110186.002135
Penido G, Zanzini ACS (2012) Checklist of large and medium-sized mammals of the Estação Ecológica Mata do Cedro, an Atlantic Forest Remnant of central Minas Gerais, Brazil. Checklist 8:712–717. https://doi.org/10.15560/8.4.712
Pinto NS, Juen L, Cabette HSR et al (2012) Fluctuating asymmetry and wing size of Agria tinctipennis Selys (Zigoptera: Coenagrionidae) in relation to riparian forest preservation status. Neotrop Entomol 41:178–185. https://doi.org/10.1007/s13744-012-0029-9
Ribeiro B, Guedes RNC, Côrrea AS et al (2007) Fluctuating asymmetry in insecticide-resistant and insecticide-susceptible strains of the maize weevil, Sitophilus zeamais (Coleoptera: Curculionidae). Arch Environ Contam Toxicol 53:77–83. https://doi.org/10.1007/s00244-006-0162-8
Ribeiro DB, Prado PI, Brown KS Jr et al (2010) Temporal diversity patterns and phenology in fruit-feeding butterflies in the Atlantic Forest. Biotropica 42:710–716. https://doi.org/10.1111/j.1744-7429.2010.00648.x
Ribeiro DB, Batista R, Prado PI et al (2012) The importance of small scales to the fruit-feeding butterfly assemblages in a fragmented landscape. Biodivers Conserv 21:811–827. https://doi.org/10.1007/s10531-011-0222-x
Ribeiro DB, Freitas AVL (2012) The effect of reduced-impact logging on fruit-feeding butterflies in Central Amazon Brazil. J Insect Conserv 16:733–744. https://doi.org/10.1007/s10841-012-9458-3
Rodrigues FMA, Lomônaco C, Christoffersen ML (2009) Habitat partition and variation of size and symmetry of three sympatric species of Alpheus (Decapoda: Caridae) along an intertidal gradient in the southwest Atlantic. J Crust Biol 29:334–342. https://doi.org/10.1651/08-3101.1
Roy CL, Amadori D, Charberet S et al (2021) Adaptative evolution of flight in Morpho butterflies. Science 374(6571):1158–1162. https://doi.org/10.1126/science.abh2620
Ryazanova GI, Polygalov AS (2013) Fluctuating asymmetry of wing venation in damselflies Ischnura elegans (Odonata, Coenagrionidae) and prospects of its use as a biological indicator of ecological quality of fresh-water reservoirs. Mosc Univ Biol Sci Bull 68:195–199. https://doi.org/10.3103/S0096392513040081
Sampaio MV, Bueno VHP, De Conti BF (2008) The effect of the quality and size of host aphid species on the biological characteristics of Aphidius colemani (Hymenoptera: Braconidae, Aphidiinae). Eur J Entomol 105:489–494. https://doi.org/10.14411/eje.2008.063
Sanseverino AM, Nessimian JL (2008) Assimetria flutuante em organismos aquáticos e sua aplicação para avaliação de impactos ambientais. Oecol Aust 12:382–405. https://doi.org/10.4257/oeco.2008.1203.03
Sarre S (1996) Habitat fragmentation promotes fluctuating asymmetry but not morphological divergence in two geckos. Popul Ecol 38:57–64. https://doi.org/10.1007/BF02514971
Schulze CH, Linsenmair E, Fiedler K (2001) Understorey versus canopy: patterns of vertical stratification and diversity among Lepidoptera in a Bornean rain forest. Plant Ecol 153:133–152. https://doi.org/10.1023/A:1017589711553
Shahabuddin G, Terborgh JW (1999) Frugivorous butterflies in Venezuelan forest fragments: abundance, diversity and the effects of isolation. J Trop Ecol 15:703–722. https://doi.org/10.1017/S0266467499001121
Shirey V, Larsen E, Doherty A et al (2022) LepTraits 1.0 A globally comprehensive dataset of butterfly traits. Nature 9:382. https://doi.org/10.1038/s41597-022-01473-5
Spaniol RS, Duarte LDS, Mendonca MDS Jr et al (2019) Combining functional traits and phylogeny to disentangling Amazonian butterfly assemblages on anthropogenic gradient. Ecosphere 10(8):e02837. https://doi.org/10.1002/ecs2.2837
Spaniol R, de MMS, Hartz SM et al (2020) Discolouring the Amazon Rainforest: how deforestation is affecting butterfly coloration. Biodiv Conserv 29(11). https://doi.org/10.1007/s10531-020-01999-3
Stevens M, Hardman CJ, Stubbins CL (2008) Conspicuousness, not eye mimicry, makes eyespots effective anti-predator signals. Behav Ecol 19:525–531. https://doi.org/10.1093/beheco/arm162
Stevens M, Merilaita S (2009) Animal camouflage: current issues and new perspectives. Phil. Trans R Soc B: Biol Sci 364:423–427. https://doi.org/10.1098/rstb.2008.0217
Stork NE, Srivastava DS, Watt AD et al (2003) Butterfly diversity and silvicultural practice in lowland rainforests of Cameroon. Biodivers Conserv 12:387–410. https://doi.org/10.1023/A:1022470308591
Symanski C, Redak RA (2021) Does fluctuating asymmetry of wing traits capture relative environmental stress in a lepidopteran? Ecol Evol 11:1199–1213. https://doi.org/10.1002/ece3.7097
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
Thomas JA (2016) Butterfly communities under threat. Science 353:216–218. https://doi.org/10.1126/science.aaf8838
Tsubaki Y, Matsumoto K (1998) Fluctuating asymmetry and male mating success in a sphragis-bearing butterfly Luehdorfia japonica (Lepidoptera: Papilionidae). J Insect Behav 11:571–582. https://doi.org/10.1023/A:1022371531263
Uehara-Prado M, Brown KS Jr, Freitas AVL (2007) Species richness, composition and abundance of fruit-feeding butterflies in the Brazilian Atlantic Forest: comparison between a fragmented and a continuous landscape. Glob Ecol Biogeogr 16:43–54. https://doi.org/10.1111/j.1466-8238.2006.00267.x
Uehara-Prado M, Fernandes JO, Bello AM et al (2009) Selecting terrestrial arthropods as indicators of small-scale disturbance: a first approach in the Brazilian Atlantic Forest. Biol Conserv 142:1220–1228. https://doi.org/10.1016/j.biocon.2009.01.008
Weller B, Ganzhorn J (2004) Carabid beetle community composition, body size, and fluctuating asymmetry along an urban–rural gradient. Basic Appl Ecol 5:193–201. https://doi.org/10.1078/1439-1791-00220
Windig JJ, Rintamaki WPT, Cassel A et al (2000) How useful is fluctuating asymmetry in rare and abundant Coenonympha butterflies. J Insect Conserv 4:253–261. https://doi.org/10.1023/A:1011332401156
Yuto CMM, Lumogdang L, Tabugo RM (2016) Fluctuating asymmetry as an indicator of ecological stress in Rhinocypha colorata (Odonata: Chlorocyphidae) in Iligan City, Mindanao Philippines. Entomol Appl Sci Lett 3:13–20
Zverev V, Kozlov MV (2021) The fluctuating asymmetry of the butterfly wing pattern does not change along an industrial pollution gradient. Symmetry 13(4):626. https://doi.org/10.3390/sym13040626
Acknowledgements
The authors would like to thank UFMG, ECMVS, CSEC, and UFSJ for support. We gratefully acknowledge the staff of the Instituto Estadual de Florestas (IEF – MG) and Estação Ecológica Estadual Mata do Cedro (ESEC) for allowing us to work in the Station. We want to thank Carla Daniele Guimarães for the collection of the individuals and Letícia Peroli for assistance with illustrations. TP thanks for the research scholarship from Conselho Nacional de Desenvolvimento Científico de Tecnológico (CNPq -142032/2020-4).
Funding
This study was financed in part by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG - APQ371-18), CNPq (307210/2016-2; 313007/2020-9), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/Brazil - Finance Code 001).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by: Matthias Waltert
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 43 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Pignataro, T., Lourenço, G.M., Beirão, M. et al. Wings are not perfect: increased wing asymmetry in a tropical butterfly as a response to forest fragmentation. Sci Nat 110, 28 (2023). https://doi.org/10.1007/s00114-023-01856-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-023-01856-7