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The Size But not the Symmetry of the Wings of Eulaema nigrita Lepeletier (Apidae: Euglossini) is Affected by Human-Disturbed Landscapes in the Brazilian Cerrado Savanna

  • Ecology, Behavior and Bionomics
  • Published:
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Abstract

Among other human-related activities, habitat loss and fragmentation are currently ranked as the most important environmental features affecting the persistence of animal and plant populations in landscapes, as well as the maintenance of ecological processes and services. Since these processes are also capable of affecting the ontogenetic development of species inhabiting those landscapes, here we measured the wing veins of male Eulaema nigrita Lepeletier (Apidae: Euglossini) bees in order to evaluate whether the bees sampled in agriculture (AG) areas suffer higher fluctuating asymmetry (FA) than those sampled in Cerrado (CE) areas in the Brazilian state of Goiás. We believe that individuals sampled in CE areas would be less asymmetric than those sampled in AG areas, given a potential higher exposure of these specimens to environmental stresses (mostly pesticides). However, we did not observe a significant trend in the FA measures we obtained, although three wing measures were bigger for bees from CE areas. The lack of significant effects of FA may be related to inherent bionomic features of E. nigrita. For instance, given their high individual dispersal abilities, the individuals we analyzed may have developed in different areas than those where they were sampled. Their generalist feeding behavior may also have given them a higher resistance to environmental perturbations, buffering the normal development of immatures even in areas with local high environmental stress. Nonetheless, higher death rates of individuals from anthropic areas may also have killed the developing immatures of E. nigrita before they reached adulthood consequently equalizing our sampled estimates.

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References

  • Ackerman JD (1983) Diversity and seasonality of male Euglossine bees (Hymenoptera: Apidae) in Central Panamá. Ecology 64:274–283

    Article  Google Scholar 

  • Babbitt GA (2006) Inbreeding reduces power-law scaling in the distribution of fluctuating asymmetry: an explanation of the basis of developmental instability. Heredity 97:258–268

    Article  CAS  PubMed  Google Scholar 

  • Batalha MA, Martins FR (2004) Reproductive phenology of the Cerrado plant community in Emas National Park. Aust J Bot 52:149–161

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bots J, Breuker CJ, Van Kerkhove A, Van Dongen S, De Bruyn L, Van Gossum H (2009) Variation in flight morphology in a female polymorphic damselfly: intraspecific, intrasexual, and seasonal differences. Can J Zool 87:86–94

    Article  Google Scholar 

  • Brosi BJ (2009) The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biol Conserv 142:414–423

    Article  Google Scholar 

  • Campos LAO, Silveira FA, Oliveira ML, Abrantes CVM, Morato EF, Melo GAR (1989) Utilização de armadilhas para a captura de machos de Euglossini (Hymenoptera, Apoidea). Rev Bras Zool 6:621–626

    Article  Google Scholar 

  • Carvalho FMV, De Marco JP, Ferreira LG (2009) The Cerrado into-pieces: habitat fragmentation as a function of landscape use in the savannas of central Brazil. Biol Conserv 142:1392–1403

    Article  Google Scholar 

  • Chang XL, Zhai BP, Liu XD, Wang M (2007) Effects of temperature stress and pesticide exposure on fluctuating asymmetry and mortality of Copera annulata (selys) (Odonata: Zygoptera) larvae. Ecotoxicol Environ Saf 67:120–127

    Article  CAS  PubMed  Google Scholar 

  • Chapin FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Díaz S (2000) Consequences of changing biodiversity. Nature 405:234–242

    Article  CAS  PubMed  Google Scholar 

  • Clarke G (1995) The genetic basis of developmental stability. II. Asymmetry of extreme phenotypes revisited. Am Nat 148:708–725

    Article  Google Scholar 

  • Córdoba-Aguilar A (1995) Fluctuating asymmetry in paired and unpaired damselfly males Ischnura denticollis (Burmeister) (Odonata: Coenagrionidae). J Ethol 13:129–132

    Article  Google Scholar 

  • De Block M, Campero M, Stocks R (2008) Developmental costs of rapid growth in a damselfly. Ecol Entomol 33:313–318

    Article  Google Scholar 

  • Dressler RL (1982) Biology of the orchid bees (Euglossini). Annu Rev Ecol Syst 13:373–394

    Article  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Graham JH, Raz S, Hel-Or H, Nevo E (2010) Fluctuating asymmetry: methods, theory, and applications. Symmetry 2:466–540

    Article  Google Scholar 

  • Henry M, Beguin M, Requier F, Rollin O, Odoux JF, Aupinel P, Aptel J, Tchamitchian S, Decourtye A (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336:348–350

    Article  CAS  PubMed  Google Scholar 

  • Hoffman AA, Woods RE, Collins E, Wallin K, White A, McKenzie JA (2005) Wing shape versus asymmetry as an indicator of changing environmental conditions in insects. Aust J Entomol 44:233–243

    Article  Google Scholar 

  • Hogg ID, Eadie JM, Williams DD, Turner D (2001) Evaluating fluctuating asymmetry in a stream-dwelling insect as an indicator of low-level thermal stress: a large-scale field experiment. J Appl Ecol 38:1326–1339

    Article  Google Scholar 

  • Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171:203–205

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter IF, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313

    Article  PubMed Central  PubMed  Google Scholar 

  • Klink CA, Machado RB (2005) Conservation of the Brazilian Cerrado. Conserv Biol 19:707–713

    Article  Google Scholar 

  • Leite GLD, Veloso RVS, Zanúncio JC, Fernandes LA, Almeida CIM (2006) Phenology of Caryocar brasiliense in the Brazilian cerrado regions. For Ecol Manag 236:286–294

    Article  Google Scholar 

  • Markow TA (1995) Evolutionary ecology and developmental instability. Annu Rev Entomol 40:105–120

    Article  CAS  Google Scholar 

  • McGarigal K, Marks BJ (1995) FRAGSTATS: spatial pattern analysis program for quantifying landscape structure. USDA For. Serv Gen Tech Rep

  • McGeoch MA (1998) The selection, testing and application of terrestrial insects as bioindicators. Biol Rev Camb Philos Soc 73:181–201

    Article  Google Scholar 

  • MEA (2005) Millenium ecosystem assessment. ecosystems and human well-being: scenarios. Island Press, Washington, DC, 137p

    Google Scholar 

  • Moura DC, Schlindwein C (2009) Mata ciliar do Rio São Francisco como biocorredor para Euglossini (Hymenoptera: Apidae) de florestas tropicais úmidas. Neotrop Entomol 38:281–284

    Article  PubMed  Google Scholar 

  • Nemésio A (2011) Euglossa marianae sp. n. (Hymenoptera: Apidae): a new orchid bee from the Brazilian Atlantic Forest and the possible first documented local extinction of a forest-dependent orchid bee. Zootaxa 2892:59–68

    Google Scholar 

  • Neves EL, Viana BF (1999) Comunidade de machos de Euglossinae (Hymenoptera: Apidae) das matas ciliares da margem esquerda do médio Rio São Francisco, Bahia. An Soc Entomol Bras 28:201–210

    Article  Google Scholar 

  • Oliveira ML (2006) Três novas espécies de abelhas da Amazônia pertencentes ao gênero Eulaema Lepeletier, 1841 (Hymenoptera: Apidae: Euglossini). Acta Amazon 36:121–128

    Article  Google Scholar 

  • Palmer AR (1994) Fluctuating asymmetry analyses: a primer. Developmental instability: its origins and evolutionary implications. Kluwer, Dordrecht, pp 335–364

    Book  Google Scholar 

  • Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst 17:391–421

    Article  Google Scholar 

  • Peruquetti RC (2003) Variação do tamanho corporal de machos de Eulaema nigrita Lepeletier (Hymenoptera, Apidae, Euglossini). Resposta materna à flutuação de recursos? Rev Bras Zool 2:207–212

    Article  Google Scholar 

  • Peruquetti RC, Campos LAO, Coelho CDP, Abrantes CVM, Lisboa LCO (1999) Abelhas Euglossini (Apidae) de áreas de Mata Atlântica: Abundância, riqueza e aspectos biológicos. Rev Bras Zool 16:101–118

    Article  Google Scholar 

  • Pinto NS, Juen L, Cabette HSR, De Marco P (2012) Fluctuating asymmetry and wing size of Argia tinctipennis Selys (Zygoptera: Coenagrionidae) in relation to riparian forest preservation status. Neotrop Entomol 41:178–185

    Article  CAS  PubMed  Google Scholar 

  • Pokorny T, Loose D, Dyker G, Quezada-Euán JJG, Eltz T (2015) Dispersal ability of male orchid bees and direct evidence for long-range flights. Apidologie 46:224–237

    Article  Google Scholar 

  • Ramalho AV, Gaglianone MC, Oliveira ML (2009) Comunidades de abelhas Euglossina (Hymenoptera, Apidae) em fragmentos de Mata Atlântica no Sudeste do Brasil. Rev Bras Entomol 53:95–101

    Article  Google Scholar 

  • Raw A (1989) The dispersal of Euglossine bees between isolated patches of eastern Brazilian wet forest (Hymenoptera, Apidae). Rev Bras Entomol 33:103–107

    Google Scholar 

  • Rohlf FJ (2006) tpsDig version 2.1. Ecology & Evolution. SUNY, Stony Brook University, New York

    Google Scholar 

  • Roubik DW, Hanson PE (2004) Orchid bees of tropical America: biology and field guide, 1st ed. INBio, San José, 370p

  • Roulston TH, Cane JH (2000) The effect of diet breadth and nesting ecology on body size variation in bees (Apiformes). J Kansas Entomol Soc 73:129–142

    Google Scholar 

  • Sala OE (2000) Global Biodiversity Scenarios for the Year 2100. Science 287:1770–1774

    Article  CAS  PubMed  Google Scholar 

  • Samejima Y, Tsubaki Y (2009) Body temperature and body size affect flight performance in a damselfly. Behav Ecol Sociobiol 64:685–692

    Article  Google Scholar 

  • Sano EE, Rosa R, Brito JLS, Ferreira LG (2008) Mapeamento semidetalhado do uso da terra do Bioma Cerrado. Pesq Agrop Brasileira 43:153–156

    Article  Google Scholar 

  • Sanseverino AM, Nessimian JL (2008) Assimetria flutuante em organismos aquáticos e sua aplicação para avaliação de impactos ambientais. Oecologia Bras 12:382–405

    Google Scholar 

  • Santos ML, Garófalo CA (1994) Nesting biology and nest re-use of Eulaema nigrita (Hymenoptera: Apidae, Euglossini). Insectes Soc 41:99–110

    Article  Google Scholar 

  • Silva DP, De Marco P (2014) No evidence of habitat loss affecting the orchid bees Eulaema nigrita Lepeletier and Eufriesea auriceps Friese (Apidae: Euglossini) in the Brazilian Cerrado Savanna. Neotrop Entomol 43:509–518

    Article  CAS  Google Scholar 

  • Silva MC, Lomônaco C, Augusto SC, Kerr WE (2009) Climatic and anthropic influence on size and fluctuating asymmetry of Euglossine bees (Hymenoptera, Apidae) in a semideciduous seasonal forest reserve. Genet Mol Res 8:730–737

    Article  CAS  PubMed  Google Scholar 

  • Silveira FA, Melo GAR, Almeida EAB (2002) Abelhas brasileiras: sistemática e identificação, 1st ed. Edição do Autor, Belo Horizonte, 253p

  • Souto K, Pereira C, Lomônaco C (2011) Body size, symmetry and abundance of Euxesta stigmatias (loew) and Euxesta sororcula (Wiedemann) (Diptera: Ulidiidae) in a Natural Reserve and in a Guava Orchard in Uberlândia, MG, Brazil. Neotrop Entomol 40:661–668

    Article  CAS  PubMed  Google Scholar 

  • Stewart SS, Vodopich DS (2013) Variation in fluctuating asymmetry among nine damselfly species. Int J Odonatol 16:1–11

    Article  Google Scholar 

  • Tonhasca A Jr, Blackmer JL, Albuquerque GS (2002) Abundance and diversity of Euglossine bees in the Fragmented lndscape of the Brazilian Atlantic forest. Biotropica 34:416–422

    Article  Google Scholar 

  • Tonhasca A Jr, Albuquerque GS, Blackmer JL (2003) Dispersal of euglossine bees between fragments of the Brazilian Atlantic Forest. J Trop Ecol 19:99–102

    Article  Google Scholar 

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336:351–352

    Article  CAS  PubMed  Google Scholar 

  • Wikelski M, Moxley J, Eaton-Mordas A, López-Uribe MM, Holland R, Moskowitz D, Roubik DW, Kays R (2010) Large-range movements of Neotropical orchid bees observed via radio telemetry. PLoS One 5, e10738. doi:10.1371/journal.pone.0010738

    Article  PubMed Central  PubMed  Google Scholar 

  • Winfree R, Bartomeus I, Cariveau DP (2011) Native pollinators in anthropogenic habitats. Annu Rev Ecol Evol Syst 42:1–22

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th ed. Pearson Prentice Hall, New Jersey, 944p

  • Zucchi R, Sakagami SF, Camargo JMF (1969) Biological observations on a neotropical parasocial bee, Eulaema nigrita, with a review on the biology of Euglossinae (Hymenoptera, Apidae). J Fac Sci Hokkaido Univ Ser 4 Zool 17:271–380

    Google Scholar 

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Acknowledgments

We are grateful to Dário Paiva Silva Júnior, Mírian Cristina de Almeida, Fábio Martins Villar de Carvalho, and several other field assistants who helped in the field surveys on which we sampled the specimens of E. nigrita. We also acknowledge both CNPq – Conselho Nacional de Desenvolvimento Científico e Tecnológico and Fundação “O Boticário” de Proteção à Natureza for the resources that allowed us to do this study. Finally, we also thank two anonymous reviewers and the journal’s editors for important and constructive suggestions and comments on previous versions of this manuscript.

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Correspondence to D P Silva.

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Pinto, N.S., Silva, D.P., Rodrigues, J.G. et al. The Size But not the Symmetry of the Wings of Eulaema nigrita Lepeletier (Apidae: Euglossini) is Affected by Human-Disturbed Landscapes in the Brazilian Cerrado Savanna. Neotrop Entomol 44, 439–447 (2015). https://doi.org/10.1007/s13744-015-0316-3

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