Advertisement

How urbanization affects multiple dimensions of biodiversity in tropical butterfly assemblages

  • Cristiano Agra Iserhard
  • Leandro Duarte
  • Noemy Seraphim
  • André Victor Lucci Freitas
Original Paper
Part of the following topical collections:
  1. Urban Biodiversity

Abstract

We evaluated how the taxonomic, phylogenetic and functional diversities of butterflies and their community-weighted traits are affected by urbanization in the southeastern Brazilian Atlantic Forest. For this purpose, a dataset of Nymphalidae species distributed across 15 urban, semiurban, and rural fragments was analyzed. Urbanization was defined by a set of environmental variables. Furthermore, the total area of each fragment was also considered in the analyses but did not influence the results, in which disturbance level and patch connectivity drove the environmental variation across the urban matrix. Species diversity increased towards the more connected fragments, while phylogenetic and functional diversity did not vary in relation to urbanization. A high forewing:hindwing ratio and the frequency of tiger-like wings were positively related to the urban fragments, while a low forewing:hindwing ratio and iridescent wings were related to the semiurban and rural fragments. The suitability of highly interconnected rural habitats for the maintenance of butterfly diversity was corroborated as expected. Nonetheless, our results also showed that semiurban fragments preserved the ecologically relevant traits of butterflies related to forested habitats, expressed in butterfly groups possibly linked with dispersal capability to avoid predation. Careful management of semiurban fragments and urban landscaping, including highly structured and native vegetation outside urban parks, may increase the functional and taxonomic diversities or at least maintain the current levels of functionality in the urban matrix. Thus, it is possible to preserve the biological diversity of native fauna and flora and recover relevant ecosystem services, ensuring the conservation of Neotropical urban centers.

Keywords

Functional traits Phylogenetic diversity Semiurban sites Taxonomic diversity Urban ecology 

Notes

Acknowledgements

AVLF thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Grant 303834/2015-3), the National Science Foundation (DEB-1256742) and Fundação de Amparo a Pesquisa do Estado de São Paulo (Grants 2011/50225-3 and 2012/50260-6). LDSD research activities have been supported by the CNPq Productivity Fellowship (Grant 307886/2015-8). This publication is part of the Rede Nacional de Pesquisa e Conservação de Lepidópteros SisBiota-Brasil/CNPq (563332/2010-7). CAI, LDSD and AVLF research activities have been developed in the context of the Institutos Nacionais de Ciência e Tecnologia in Ecology, Evolution and Biodiversity Conservation (EECBio), supported by MCTIC/CNPq (Proc. 465610/2014-5) and Fundação de Amparo a Pesquisa do Estado de Goiás.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Barbaro L, van Halder I (2009) Linking bird, carabid beetle and butterfly life-history traits to habitat fragmentation in mosaic landscapes. Ecography 32:321–333CrossRefGoogle Scholar
  2. Betts CR, Wootton RJ (1988) Wing shape and flight behaviour in butterflies (Lepidoptera: Papilionoidea and Hesperioidea): a preliminary analysis. J Exp Biol 138:271–288Google Scholar
  3. Bivand R, Piras G (2015) Comparing implementations of estimation methods for spatial econometrics. J Stat Softw 63:1–36Google Scholar
  4. Blair RB (1999) Birds and butterflies along an urban gradient: surrogate taxa for assessing biodiversity? Ecol Appl 9:164–170CrossRefGoogle Scholar
  5. Blair RB, Launer AE (1997) Butterfly diversity and human land use: species assemblages along an urban gradient. Biol Conserv 80:113–125CrossRefGoogle Scholar
  6. Blomberg SP, Garland T, Ives AR, Crespi B (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745CrossRefPubMedGoogle Scholar
  7. Bonebrake TC, Ponisio LC, Boggs CL, Ehrlich PR (2010) More than just indicators: a review of tropical butterfly ecology and conservation. Biol Conserv 143:1831–1841CrossRefGoogle Scholar
  8. Brower AVZ, Wahlberg N, Ogawa JR, Boppré M, Vane-Wright RI (2010) Phylogenetic relationships among genera of danaine butterflies (Lepidoptera: Nymphalidae) as implied by morphology and DNA sequences. Syst Biodivers 8:75–89CrossRefGoogle Scholar
  9. Brown KS (1972) Maximizing daily butterfly counts. J Lepid Soc 26:183–196Google Scholar
  10. Brown KS, Freitas AVL (2002) Butterfly communities of urban forest fragments in Campinas, São Paulo, Brazil: structure, instability, environmental correlates, and conservation. J Insect Conserv 6:217–231CrossRefGoogle Scholar
  11. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67CrossRefGoogle Scholar
  12. Cheverud JM, Dow MM, Leutenegger W (1985) The quantitative assessment of phylogenetic constraints in comparative analyses: sexual dimorphism in body weight among primates. Evolution 39:1335–1351CrossRefPubMedGoogle Scholar
  13. Debastiani VJ, Duarte LDS (2014) PCPS—an R-package for exploring phylogenetic eigenvectors across metacommunities. Front Biogeogr 6:144–148CrossRefGoogle Scholar
  14. Debastiani VJ, Pillar VD (2012) SYNCSA—R tool for analysis of metacommunities based on functional traits and phylogeny of the community components. Bioinformatics 28:2067–2068CrossRefPubMedGoogle Scholar
  15. Devictor V, Mouillot D, Meynard C, Jiguet F, Thuiller W, Mouquet N (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 13:1030–1040PubMedGoogle Scholar
  16. DeVries PJ (1987) The butterflies of Costa Rica and their natural history: Papilionidae, Pieridae, and Nymphalidae. Princeton University Press, PrincetonGoogle Scholar
  17. DeVries PJ, Penz CM, Hill RI (2010) Vertical distribution, flight behaviour and evolution of wing morphology in Morpho butterflies. J Anim Ecol 79:1077–1085CrossRefPubMedGoogle Scholar
  18. Diniz-Filho JAF, Sant’Ana CER, Bini LM (1998) An eigenvector method for estimating phylogenetic inertia. Evolution 52:1247–1262CrossRefPubMedGoogle Scholar
  19. Diniz-Filho JAF, Cianciaruso MV, Rangel TF, Bini LM (2011) Eigenvector estimation of phylogenetic and functional diversity. Funct Ecol 5:735–744CrossRefGoogle Scholar
  20. Diniz-Filho JAF, Bini LM, Rangel TF, Morales-Castilla I, Olalla-Tárraga MA, Rodríguez MA, Hawkins BA (2012) On the selection of phylogenetic eigenvectors for ecological analyses. Ecography 35:239–249CrossRefGoogle Scholar
  21. Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930CrossRefGoogle Scholar
  22. Doucet SM, Meadows MG (2009) Iridescence: a functional perspective. J R Soc Interface 6:115–132CrossRefGoogle Scholar
  23. Duarte LDS, Debastiani VJ, Freitas AVL, Pillar VD (2016) Dissecting phylogenetic fuzzy weighting: theory and application in metacommunity phylogenetics. Methods Ecol Evol 7:937–946CrossRefGoogle Scholar
  24. Duarte LDS, Debastiani VJ, Carlucci MB, Diniz-Filho JAF (2018) Analyzing community-weighted trait means across environmental gradients: should phylogeny stay or should it go? Ecology 99:385–398CrossRefPubMedGoogle Scholar
  25. Ellis EC, Goldewijk KK, Siebert S, Lightman D, Ramankutty N (2010) Anthropogenic transformation of the biomes, 1700 to 2000. Glob Ecol Biogeogr 19:589–606Google Scholar
  26. Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10CrossRefGoogle Scholar
  27. Finkbeiner SD, Briscoe AD, Reed RD (2014) Warning signals are seductive: relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies. Evolution 68:3410–3420CrossRefPubMedGoogle Scholar
  28. Flynn DFB, Mirotchnick N, Jain M, Palmer MI, Naeem S (2011) Functional and phylogenetic diversity as predictors of biodiversity–ecosystem function relationships. Ecology 92:1573–1581CrossRefPubMedGoogle Scholar
  29. Fritz SA, Purvis A (2010) Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conserv Biol 24:1042–1051CrossRefPubMedGoogle Scholar
  30. Garnier E, Cortez J, Billès G, Navas M-L, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Bellmann A (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637CrossRefGoogle Scholar
  31. Goddard MA, Dougill AJ, Benton TG (2009) Scaling up from gardens: biodiversity conservation in urban environments. TREE 1175:1–9Google Scholar
  32. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, OxfordGoogle Scholar
  33. Hill JK, Hamer KC, Tangah J, Dawood M (2001) Ecology of tropical butterflies in rainforest gaps. Oecologia 128:294–302CrossRefPubMedGoogle Scholar
  34. Iserhard CA, Brown KS, Freitas AVL (2013) Maximized sampling of butterflies to detect temporal changes in tropical communities. J Insect Conserv 17:615–622CrossRefGoogle Scholar
  35. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464CrossRefGoogle Scholar
  36. Kemp DJ (2007) Female butterflies prefer males bearing bright iridescent ornamentation. Proc R Soc Lond B 274:1043–1047CrossRefGoogle Scholar
  37. Kemp DJ, Wiklund C, Van Dyck H (2006) Contest behaviour in the speckled wood butterfly (Pararge aegeria): seasonal phenotypic plasticity and the functional significance of flight performance. Behav Ecol Sociobiol 59:403–411CrossRefGoogle Scholar
  38. Legendre P, Legendre L (2012) Numerical ecology, 3rd edn. Elsevier, AmsterdamGoogle Scholar
  39. Maddison DR, Maddison WP (2010) Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org
  40. Magle SB, Hunt VM, Vernon M, Crooks KR (2012) Urban wildlife research: past, present, future. Biol Conserv 155:23–32CrossRefGoogle Scholar
  41. Magurran AE, McGill BJ (2011) Biological diversity: frontiers in measurement and assessment. Oxford University Press, OxfordGoogle Scholar
  42. Matteson KC, Langellotto GA (2010) Determinates of inner city butterfly and bee species richness. Urban Ecosyst 13:333–347CrossRefGoogle Scholar
  43. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297CrossRefGoogle Scholar
  44. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260CrossRefGoogle Scholar
  45. Nagelkerke NJD (1991) A note on a general definition of the coefficient of determination. Biometrika 78:691–692CrossRefGoogle Scholar
  46. Orme D (2013) The caper package: comparative analysis of phylogenetics and evolution in R. R package version 5:1–36Google Scholar
  47. Papageorgis C (1975) Mimicry in Neotropical butterflies: why are there so many different wing-coloration complexes in one place? Am Sci 63:522–532Google Scholar
  48. Pavoine S, Baguette M, Stevens VM, Leibold MA, Turlure C, Bonsall B (2014) Life history traits, but not phylogeny, drive compositional patterns in a butterfly metacommunity. Ecology 95:3304–3313CrossRefGoogle Scholar
  49. Peña C, Wahlberg N, Weingartner E, Kodandaramaiah U, Nylin S, Freitas AVL, Brower AVZ (2006) Higher level phylogeny of Satyrinae butterflies (Lepidoptera: Nymphalidae) based on DNA sequence data. Mol Phylogenet Evol 40:29–49CrossRefPubMedGoogle Scholar
  50. Penz CM (1999) Higher level phylogeny for the passion-vine butterflies (Nymphalidae, Heliconiinae) based on early stage and adult morphology. Zool J Linn Soc 127:277–344CrossRefGoogle Scholar
  51. Penz CM, Peggie D (2003) Phylogenetic relationships among Heliconiinae genera based on morphology (Lepidoptera: Nymphalidae). Syst Entomol 28:451–479CrossRefGoogle Scholar
  52. Peres-Neto PR, Leibold MA, Dray S (2012) Assessing the effects of spatial contingency and environmental filtering on metacommunity phylogenetics. Ecology 93:S14–S30CrossRefGoogle Scholar
  53. Peres-Neto PR, Dray S, ter Braak CJF (2017) Linking trait variation to the environment: critical issues with community-weighted mean correlation resolved by the fourth-corner approach. Ecography 40:806–816CrossRefGoogle Scholar
  54. Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758CrossRefPubMedGoogle Scholar
  55. Pillar VD, Duarte LDS (2010) A framework for metacommunity analysis of phylogenetic structure. Ecol Lett 13:587–596CrossRefPubMedGoogle Scholar
  56. Pillar VD, Orlóci L (1996) On randomization testing in vegetation science: multifactor comparisons of relevé groups. J Veg Sci 7:585–592CrossRefGoogle Scholar
  57. Pillar VD, Duarte LDS, Sosinski EE, Joner F (2009) Discriminating trait-convergence and trait-divergence assembly patterns in ecological community gradients. J Veg Sci 20:334–348CrossRefGoogle Scholar
  58. Pinheiro CEG, Freitas AVL (2014) Some possible cases of escape mimicry in Neotropical butterflies. Neotrop Entomol 43:393–398CrossRefPubMedGoogle Scholar
  59. Pinheiro CEG, Freitas AVL, Campos VC, DeVries PJ, Penz CM (2016) Both palatable and unpalatable butterflies use bright colors to signal difficulty of capture to predators. Neotrop Entomol 45:107–113CrossRefPubMedGoogle Scholar
  60. Prinzing A, Reiffers R, Braakhekke WG, Hennekens SM, Tackenberg O, Ozinga WA, Schamineée JHH, van Groenendael JM (2008) Less lineages—more trait variation: phylogenetically clustered plant communities are functionally more diverse. Ecol Lett 8:809–819CrossRefGoogle Scholar
  61. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  62. Ramírez-Restrepo L, MacGregor-Fors I (2017) Butterflies in the city: a review of urban diurnal Lepidoptera. Urban Ecosyst 20:171–182CrossRefGoogle Scholar
  63. Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223CrossRefGoogle Scholar
  64. Rodrigues JJS, Brown KS, Ruszczyk A (1993) Resources and conservation of Neotropical butterflies in urban forest fragments. Biol Conserv 64:3–9CrossRefGoogle Scholar
  65. Rohlf FJ (2001) Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:2143–2160CrossRefPubMedGoogle Scholar
  66. Ruszczyk A (1986) Distribution and abundance of butterflies in the urbanization zones of Porto Alegre Brazil. J Lepid Soc 25:157–178Google Scholar
  67. Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. TREE 21:186–191PubMedGoogle Scholar
  68. Silva-Brandão KL, Wahlberg N, Francini RB, Azeredo-Espin AML, Brown KS, Paluch M, Lees DC, Freitas AVL (2008) Phylogenetic relationships of butterflies of the tribe Acraeini (Lepidoptera, Nymphalidae, Heliconiinae) and the evolution of host plant use. Mol Phylogenet Evol 46:515–531CrossRefPubMedGoogle Scholar
  69. Sing KW, Dong H, Wang WZ, Wilson JJ (2016) Can butterflies cope with city life? Butterfly diversity in a young megacity in southern China. Genome 59:751–761CrossRefPubMedGoogle Scholar
  70. Soga M, Koike S (2012) Relative importance of quantity, quality and isolation of patches for butterfly diversity in fragmented urban forests. Ecol Res 27:265–271CrossRefGoogle Scholar
  71. Summerville KS, Crist TO (2001) Effects of experimental habitat fragmentation on patch use by butterflies and skippers (Lepidoptera). Ecology 5:1360–1370CrossRefGoogle Scholar
  72. Uehara-Prado M, Brown KS, Freitas AVL (2009) Species richness, composition and abundance of fruit-feeding butterflies in the Brazilian Atlantic Forest: comparison between fragmented and a continuous landscape. Glob Ecol Biogeogr 16:43–54CrossRefGoogle Scholar
  73. Wahlberg N, Leneveu J, Kodandaramaiah U, Peña C, Nylin S, Freitas AVL, Brower AVZ (2009) Nymphalid butterflies diversify following near demise at the cretaceous/tertiary boundary. Proc R Soc B 276:4295–4302CrossRefPubMedGoogle Scholar
  74. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505CrossRefGoogle Scholar
  75. Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100CrossRefGoogle Scholar
  76. Weiher E (2011) A primer of trait and functional diversity. In: Magurran AE, McGill BJ (eds) Biological diversity—frontiers in measurement and assessment, 1st edn. Oxford University Press, Oxford, pp 175–193Google Scholar
  77. Willmott KR, Freitas AVL (2006) Higher-level phylogeny of the Ithomiinae (Lepidoptera: Nymphalidae): classification, patterns of larval hostplant colonization and diversification. Cladistics 22:297–368CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Cristiano Agra Iserhard
    • 1
  • Leandro Duarte
    • 2
  • Noemy Seraphim
    • 3
    • 4
  • André Victor Lucci Freitas
    • 4
  1. 1.Programa de Pós-Graduação em Biologia Animal, Departamento de Ecologia, Zoologia e Genética, Instituto de BiologiaUniversidade Federal de PelotasPelotasBrazil
  2. 2.Departamento de EcologiaUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  3. 3.Instituto Federal de Educação, Ciência e Tecnologia de São PauloCampinasBrazil
  4. 4.Departamento de Biologia Animal and Museu de ZoologiaUniversidade Estadual de CampinasCampinasBrazil

Personalised recommendations