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Body size and its correlates in fruit-feeding butterflies in a seasonal environment

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Abstract

Introduction

Body-size covaries with many species’ traits, with implications for population and ecosystem-level patterns. Body size and seasonality of a species may covary if, for certain body sizes and optimal resource availability, meet the larger energy requirements of large-bodied species, are restricted to a narrow temporal window.

Aim/methods

Here, we examine the relationship between body size and seasonality of fruit-feeding butterflies in the Cerrado, as well as its association with larval diet breadth and synchrony with fruit phenology.

Results

Relative to smaller-bodied clades, the adults within larger clades were less abundant, more generalized in their larval diet-breadth, more seasonal, and synchronized with fruit phenology.

Discussion

Body-size covaries with species traits that are sensitive to anthropogenic drivers. In the Cerrado realm, Brazil, larger-bodied butterflies tend to be more temporally specialized and more synchronized with food plants—therefore, more vulnerable to climate-driven changes in phenology (i.e., fruiting season).

Implications for insect conservation

To account for climate driven changes in synchrony with resources in the Cerrado, conservation should continue to focus on preserving habitat, especially corridors between savannah and gallery forests, so that resources are diverse and sufficiently abundant to sustain populations. Results from our study suggest that to conserve larger-bodied nymphalids, habitat restoration projects should prioritize seed sources that will maximize interaction diversity. This may not only be achieved by planting a diversity of native host plants but also cultivars that offset seasonal changes in the timing of flushing or fruiting.

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Data availability

All data are available in the supplementary material.

References

  • Agostinelli C, Lund U (2017) R package ‘circular’: Circular Statistics. R package version 0.4–93. URL: https://CRAN.R-projet.org/projects/circular.

  • Batalha MA, Mantovani W (2000) Reproductive phenological patterns of cerrado plant species at the Pé-de-Gigante Reserve (Santa Rita do Passa Quatro, SP, Brazil): a comparison between the herbaceous and woody floras. Rev Bras Biol 60:129–145

    Article  CAS  PubMed  Google Scholar 

  • Beccaloni GW, Hall SK, Viloria AL, Robinson GS (2008) Catalogue of the hostplants of the Neotropical Butterflies/Catálogo de las plantas huésped de las mariposas Neotropicales. In: Zaragoza TM (ed) Monografias the natural history museum. Instituto Venezolano de Investigaciones Científicas, Zaragoza, p 536

    Google Scholar 

  • Blomberg SP, Garland-Jr T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745

    PubMed  Google Scholar 

  • Brito MRM, Lion MB, Oliveira IF, Cardoso MZ (2021) Butterflies on the dry edge of the Atlantic forest: water availability determines community structure at the Northern limit of Atlantic Forest. Insect Conservation and Diversity 14:476–491

    Article  Google Scholar 

  • Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Carreira JYO (2021) Dinâmica temporal de borboletas tropicais. Ph.D. Dissertation, University of Campinas, Campinas, São Paulo.

  • Damuth J (1981) Population density and body size in mammals. Nature 290:699–700

    Article  Google Scholar 

  • Davis RB et al (2013) Degree of specialization is related to body size in herbivorous insects: a phylogenetic confirmation. Evolution 67(2):583–589

    Article  PubMed  Google Scholar 

  • DeVries PJ, Walla TR, Greeney HF (1999) Species diversity in spatial and temporal dimensions of fruit-feeding butterflies from two Ecuadorian rainforests. Biol J Lin Soc 68:333–353

    Article  Google Scholar 

  • DeVries PJ, Hamm CA, Fordyce JA (2016) A standardized sampling protocol for fruit-feeding butterflies (Nymphalidae). In: Larsen TH (ed) Core standardized methods for rapid biological field assessment. Conservation International, Arlington, pp 140–148

    Google Scholar 

  • Diamond SE, Frame AM, Martin RA, Buckley LB (2011) Species’ traits predict phenological responses to climate change in butterflies. Ecology 92(1):005–1012

    Google Scholar 

  • Duarte LDS, Debastiani VJ, Carlucci MB, Diniz-Filho JAF (2014) Analyzing community-weighted trait means across environmental gradients: should phylogeny stay or should it go? Ecology 99:385–398

    Article  Google Scholar 

  • 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 99:385–398

    Article  PubMed  Google Scholar 

  • Ferreira BHS, da Rosa OM, Mariano Fernandes RA, Fujizawa Nacagava VA, Arguelho BA, Ribeiro DB, Pott A, Damasceno Junior GA, Garcia LC (2023) Flowering and fruiting show phenological complementarity in both trees and non-trees in mosaic-burnt floodable savanna. J Environ Manag 337:117665. https://doi.org/10.1016/j.jenvman.2023.117665

    Article  Google Scholar 

  • Fischer K, Kirste M (2017) Temperature and humidity acclimation increase desiccation resistance in the butterfly Bicyclus anyanana. Entomol Exper Appl 166:289–297

    Article  Google Scholar 

  • Fonseca M (2004) Fitossociologia e similaridade florística entre trechos de Cerrado sentido restrito em interflúvio e em vale no Jardim Botânico de Brasília. Acta Bot Bras 18:19–29

    Article  Google Scholar 

  • Fountain-Jones NM, Baker SC, Jordan GJ (2015) Moving beyond the guild concept: develo** a practical functional trait framework for terrestrial beetles. Ecol Entomol 40:1–13

    Article  Google Scholar 

  • Freire-Jr GBF, Diniz IR (2015) Temporal dynamics of fruit-feeding butterflies (Lepidoptera: Nymphalidae) in two habitats in a Brazilian environment. Florida Entomol 98:1207–1216

    Article  Google Scholar 

  • Freire-Jr GB, Nascimento AR, Malinov IK, Diniz IR (2014) Temporal occurrence of two Morpho butterflies (Lepidoptera: Nymphalidae): influence of weather and food resources. Environ Entomol 43(2):274–282

    Article  Google Scholar 

  • Freire-Jr GB, Silva T, Oliveira H, Collier C, Rodrigues HP, Dias JP, Santos JP, Marini-Filho OJ, Freitas AVL, Smilanich A, Dyer LA, Diniz IR (2021a) Good things come in larger packages: size matters for fruit-feeding butterfly dispersal and diet breadth. Diversity 12:664. https://doi.org/10.3390/d13120664

    Article  Google Scholar 

  • Freire-Jr GB, Ribeiro DB, Santos AC, Silva T, Dias JP, Rodrigues HP, Diniz IR (2021b) Horizontal and vertical variation in the structure of fruit-feeding butterfly (Nymphalidae) assemblages in the Brazilian Cerrado. Insect Conser Diver 14:1–10. https://doi.org/10.1111/icad.12547

    Article  Google Scholar 

  • Freitas AVL, Iserhard CA, Santos JP, Carreira JYO, Ribeiro DB, Melo DHA, Rosa AHB, Marini-Filho OJ, Accacio GM, Uehara-Prado M (2014) Studies with butterfly bait traps: an overview. Rev Colomb De Entomol 40:209–218

    Google Scholar 

  • Fundação Biodiversitas (2003) Lista da fauna brasileira ameaçada de extinção. Fundação Biodiversitas, Belo Horizonte, Brazil. Available from http://www.biodiversitas.org.br/

  • Gerhold P, Cahill-Jr JF, Winter M, Bartish IV, Prinzing A (2015) Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better). Funct Ecol 29:600–614

    Article  Google Scholar 

  • Gillespie MAK, Birkemoe T, Sverdrup-Thygeson A (2017) Interactions between body size, abundance, seasonality and phenology in forest beetles. Ecol Evol 7:1091–1100

    Article  PubMed  PubMed Central  Google Scholar 

  • Graça MB, Pequeno PACL, Franlin E, Morais JW (2017) Coevolution between flight morphology, vertical stratification and sexual dimorphism: what can we learn from tropical butterflies? J Evol Biol 30:1862–2187

    Article  PubMed  Google Scholar 

  • Green DM, Middleton J (2013) Body size varies with abundance, not climate, in an amphibian population. Ecography 36(8):947–955

    Article  Google Scholar 

  • Guarino GSE, Walter TMB (2005) Fitossociologia de dois trechos inundáveis de Matas de Galeria no Distrito Federal, Brasil. Acta Bot Bras 19:431–442

    Article  Google Scholar 

  • Hill GM, Kawahara AY, Daniels JC, Bateman GC, Scheffers BR (2021) Climate change effects on animal ecology: butterflies and moths as a case study. Biol Rev 5:2113–2126

    Article  Google Scholar 

  • Hjalmarsson A, Bergsten J, Monaghan MT (2015) Dispersal is linked to habitat use in 59 species of water beetles (Coleoptera: Adephaga) on Madagascar. Ecography 38:732–739

    Article  Google Scholar 

  • Hofmann GS, Cardoso MF, Alves RJ, Weber EJ, Barbosa AA, de Toledo PM, de Oliveira LF (2021) The Brazilian Cerrado is becoming hotter and drier. Glob Change Biol 27(17):4060–4073

    Article  CAS  Google Scholar 

  • Holm S, Davis RB, Javoiš J, Õunap E, Kaasik A, Molleman F, Tammaru T (2016) A comparative perspective on longevity: the effect of body size dominates over ecology in moths. J Evol Biol 29(12):2422–2435

    Article  CAS  PubMed  Google Scholar 

  • ** Y, Qian H (2019) V.PhyloMaker: an R package that can generatively large phylogenies for vascular plants. Ecography 42:1353–1359

    Article  Google Scholar 

  • Kembel S, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2020) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  Google Scholar 

  • Landler L, Ruxton GD, Malkemper EP (2020) Grouped circular data in biology: advice for effectively implementing statistical procedures. Behav Ecol Sociobiol. https://doi.org/10.1007/s00265-020-02881-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewinsohn TM, Freitas AVL, Prado PI (2005) Conservation of terrestrial invertebrates and their habitats in Brazil. Conserv Biol 19(3):640–645. https://doi.org/10.1111/j.1523-1739.2005.00682.x

    Article  Google Scholar 

  • Lourenço GM, Soares GR, Santos TP, Dáttilo W, Freitas AVL, Ribeiro SP (2019) Equal but different: natural ecotones are dissimilar to anthropic edges. PLoS ONE. https://doi.org/10.1371/journal.pone.0213008

    Article  PubMed  PubMed Central  Google Scholar 

  • Marquis RJ, Morais HC, Diniz IR (2002) Interactions among cerrado plants and their herbivores: unique or typical? The Cerrados of Brazil: ecology and natural history of a Neotropical savanna. Columbia University Press, New York, pp 306–328

    Google Scholar 

  • Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717

    Article  PubMed  Google Scholar 

  • Miller-Rushing AJ, Hoye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc London b: Biol Sci 365:3177–3186

    Article  PubMed  Google Scholar 

  • Morais HC, Diniz IR, Silva DMS (1999) Caterpillar seasonality in a Central Brazilian Cerrado. Rev Biol Trop 47:1025–1033

    Google Scholar 

  • Morellato LPC, Talora DC, Takahasi A, Benke CC, Romera EC, Ziparro B (2000) Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32:811–823

    Article  Google Scholar 

  • Morellato L, Patricia C, Alberti LF, Irene L (2010) Applications of circular statistics in plant phenology: a case studies approach. Phenological research. Springer, Dordrecht

    Google Scholar 

  • Morse DR, Lawton JH, Dodson MM, Williamson MH (1985) Fractal dimension of vegetation and the distribution of arthropod body lengths. Nature 314:731–733

    Article  Google Scholar 

  • Nobre CEB, Iannuzzi L, Schlindwein C (2012) Seasonality of fruit-feeding butterflies (Lepidoptera, Nymphalidae) in a Brazilian semiarid area. ISRN Zool 2012:1–8

    Article  Google Scholar 

  • Paradis E, Schliep K (2019) ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528

    Article  CAS  PubMed  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary reponses to recent climate change. Ann Rev Ecol Evol Syst 37:637–369

    Article  Google Scholar 

  • Pavoine S, Baguette M, Stevens VM, Leibold MA, Turlure C, Bonsall MB (2014) Life history traits, but not phylogeny, drive compositional patterns in a butterfly metacommunity. Ecology 95:3304–3313

    Article  Google Scholar 

  • Post E (2019) Time in ecology: a theoretical framework. Princeton University Press

  • Pozo C, Martínez AL, Bouquets JL, Suárez NS, Martínez AM, Fernández IV, Warren DA (2008) Seasonality and phenology of the butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of Mexico’s Calakmul region. Florida Entomol 91:407–422

    Article  Google Scholar 

  • R Development Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Online: “http://www.R-project.org”.

  • Revell LJ (2012) phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  • Ribeiro DB, Freitas AVL (2011) Large-sized insects show stronger seasonality than small-sized ones: a case study of fruit-feeding butterflies. Biol J Linnean Soc 104:820–827

    Article  Google Scholar 

  • Ribeiro DB, Prado P, Brown-Jr KB, Freitas AVL (2010) Temporal diversity and phenology in fruit-feeding butterflies in the Atlantic Forest. Biotropica 6:710–716

    Article  Google Scholar 

  • Rosa AHB, Ribeiro DB, Freitas AVL (2023) How data curation and new geographical records can change the conservation status of threatened brazilian butterflies. J Insect Conserv. https://doi.org/10.1007/s10841-023-00464-0

    Article  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Focus on Bioimage Informatics 9:671–675

    CAS  Google Scholar 

  • Shahabuddin G, Ponte CA (2005) Frugivorous butterfly species in tropical forest fragments: correlates of vulnerability to extinction. Biodivers Conserv 14:1137–1152

    Article  Google Scholar 

  • Silva JM, Bates JM (2002) Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot: the Cerrado, which includes both forest and savanna habitats, is the second largest South American biome, and among the most threatened on the continent. Bioscience 52(3):225–234

    Article  Google Scholar 

  • Silva FAM, Assad EA, Evangelista BA (2008) Caracterização climática do bioma Cerrado. Cerrado Ecol e Flora 1:69–88

    Google Scholar 

  • Silva-Júnior MC, Sarmento TR (2009) Comunidades lenhosas no cerrado sentido restrito em duas posições topográficas na estação ecológica do Jardim Botânico de Brasília, DF, Brasil. Rodriguésia 60:277–294

    Article  Google Scholar 

  • Spaniol RL, Duarte LS, Mendonça-Jr MS, Iserhard CA (2019) Combining functional traits and phylogeny to disentangling Amazonian butterfly assemblages on anthropogenic gradients. Ecosphere 10(8):e02837. https://doi.org/10.1002/ecs2.2837

    Article  Google Scholar 

  • Stevens VM, Trochet A, Dyck HV, Colbert J, Baguete M (2012) How is dispersal integrated in life histories: a quantitative analysis using butterflies. Ecol Lett 15:74–86

    Article  PubMed  Google Scholar 

  • Stireman JO, Dyer LA, Janzen DH, Singer MS, Lill JT, Marquis RJ, Ricklefs RE, Gentry GL, Hallwachs W, Coley PD, Barone JA, Greeney HF, Connahs H, Morais HC, Diniz IR (2005) Climatic umpredictability and parasitism of caterpillars: implications of global warming. PNAS 48:17384–17387

    Article  Google Scholar 

  • Sudta C, Salcido DM, Forister ML, Walla TR, Villarin-Cortez S, Dyer LA (2022) Jack-of-all trades paradigm meets long-term data: generalist herbivores are more widespread and locally less abundant. Ecol Lett 00:1–10

    Google Scholar 

  • Symonds MRE, Blomberg SP (2014) A primer on phylogenetic generalised least squares. In: Garamszegi L (ed) Modern phylogenetic comparative methods and their application in evolutionary biology. Springer, Berlin

    Google Scholar 

  • 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 continuous landscape. Glob Ecol Biogeogr 16:43–54

    Article  Google Scholar 

  • UN Environment World Conservation Monitoring Centre (UNEP-WCMC), International Union for Conservation of Nature (IUCN), National Geographic Society (NGS), “Protected Planet Report 2018” (UNEP-WCMC, IUCN, and NGS, 2018).

  • Wahlberg N, Leneveu J, Kodandaramaiah U, Pena C, Nylin S, Freitas AVL, Brower AVZ (2009) Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proc R Soc Biol Sci 276:4295–4302

    Article  Google Scholar 

  • White EP, Ernest SKM, Kerkhoff AJ, Enquist BJ (2007) Relationships between body size and abundance in ecology. Trends Ecol Evol 22:323–330

    Article  PubMed  Google Scholar 

  • Zanne AE et al (2014) Three keys to the radiation of angiosperms into freezing environments

  • Zhang C, Settele J, Sun W, Wiemes M, Zhang Y, Schweiger O (2019) Resource availability drives trait composition of butterfly assemblages. Oecologia. https://doi.org/10.1007/s00442-019-04454-5

    Article  PubMed  Google Scholar 

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Aknowledgments

Fernando Carvalho, Miguel Marinho, and Nayara F. Araújo helped with fieldwork. University of Brasília provided logistical support. G.B.F.Jr and I.R.D, received a post-doc fellowships from Coordination of Improvement of Higher Education through the Program of Internationalization—CAPES/PrInt (Proc #: CAPES/PrInt—88887.683913/2022), and the National Council for Scientific and Technological Development (CNPq) through the PVE Program and PRONEX CNPq/FAPDF (Proc #: CNPq-303076/2013), respectively. Special thanks to André Lucci Freitas, Lee Dyer, Pedro Constantino, Celso Oliveira, Korynna Rubio, and Andrea Glassmire for hel** us with specimen identification and comments on a previous version of this paper.

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Authors and Affiliations

  1. Department of Biology, Program in Ecology, Evolution and Conservation Biology, EECB, University of Nevada, Reno, NV, 89552, USA

    Geraldo de Brito Freire Jr. & Danielle Salcido

  2. Departamento de Zoologia, Universidade do Paraná, UFPR, Curitiba, PR, 81531-980, Brazil

    Geraldo de Brito Freire Jr. & Hernani F. M. Oliveira

  3. Instituto de Pesquisa Ambiental da Amazônia, Rua Horizontina 104, Canarana, MT, 78640-000, Brazil

    Hernani F. M. Oliveira

  4. Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Campo Grande, MS, 79070-900, Brazil

    Danilo B. Ribeiro & Diogo B. Provete

  5. Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade de Brasília, UnB. Campus Universitário Darcy Ribeiro, Bloco E, Asa Norte, Brasília, DF, 70910-900, Brazil

    Thayane Silva, Joao Paulo Dias, Hanna P. Rodrigues & Ivone R. Diniz

  6. Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Campinas, SP, Brazil

    Jessie P. Santos

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  1. Geraldo de Brito Freire Jr.
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Contributions

GBF, IRD, conceived, designed the experiment and have edited the manuscript. TS, JPD, and HPR performed the fieldwork, JPS, built the phylogenetic tree; DBR, and DP analyzed the statistical analyses. GBF, DMS, and HFMO, wrote the manuscript.

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Correspondence to Geraldo de Brito Freire Jr..

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Appendix S1

Abundance (N); mean vector length (r); Rayleigh test p-value (R.T (p)—(*) mean p ≤ 0.05; (**) p ≤ 0.01; (***) p ≤ 0.001); forewing length (FWL); and diet breadth based on the number of family, genera, species, and phylogenetic relatedness of host plants (Fam/Gen/Spp/Phy, respectively) of fruit-feeding butterfly species captured from July/2012 to June/2013 at Fazenda Água Limpa, Brasília, Brazil.

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Freire, G.d.B., Salcido, D., Oliveira, H.F.M. et al. Body size and its correlates in fruit-feeding butterflies in a seasonal environment. J Insect Conserv 27, 577–587 (2023). https://doi.org/10.1007/s10841-023-00481-z

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