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Orchid bees (Apidae, Euglossini) from Oil Palm Plantations in Eastern Amazon Have Larger but Not Asymmetrical Wings

  • Ecology, Behavior and Bionomics
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Abstract

Phenotypic variation in both morphology and symmetry of individuals may appear due to environmental stress caused by land-use changes. Here, we evaluated fluctuating asymmetry (FA) and wing size variations of two orchid bee species, Euglossa ignita Smith, 1874 and Eulaema meriana (Olivier, 1789), comparing 11 wing traits. We sampled the individuals from legal reserves (LR), areas of permanent protection (APP), and oil palm plantations (PALM) in Eastern Amazonia. We calculated FA as the absolute difference between the wing measurements made in the right and left wings of specimens and both species’ wing size. We corrected each FA measure for possible directional asymmetry bias by subtracting the mean value of the mean FA signed difference to each FA measure. We compared FA and the size of each wing trait of each species between land-use types using one-way ANOVAs. We found no effect of FA between land-use types, but we observed individuals of both species from PALM areas having larger wings than those from LR areas. Our results demonstrate that there seems to be a pressure exerted by land-use change associated with palm oil cultivation favoring individuals with larger wings, although both species had shown substantial permeability of oil palm.

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References

  • Alves SAO, Amaral WAN, Horbach MA, Antiqueira LMOR, Dias IFS (2013) Indicadores de Sustentabilidade da Agroindústria do dendê no estado do Pará. Energia na Agricultura 28(4):240–246

    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 

  • 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 

  • Benami E, Curran LM, Cochrane M, Venturieri A, Franco R, Kneipp J, Swartos A (2018) Oil palm land conversion in Pará, Brazil, from 2006–2014: evaluating the 2010 Brazilian Sustainable Palm Oil Production Program. Environ Res Lett 13:034037

    Article  Google Scholar 

  • Bolfe EL, Batistella M (2011) Análise florística e estrutural de sistemas silviagrícolas em Tome-Acú, Pará. Pesquisa Agropecuária Brasileira 46:1139–1147

    Article  Google Scholar 

  • Brasil (2012) Lei n° 12.651 de 15 de Maio de 2012. Diário Oficial da República Federativa do Brasil, Poder Legislativo, Brasília, DF. http://www.planalto.gov.br/ccivil_03/_ato2011-2014/2012/lei/l12651.htm. Accessed 6 June 2018

  • Brito TF, Phifer CC, Knowlton JL, Fiser CM, Becker NM, Barros FC, Contrera FAL, Maués MM, Juen L, Montag LFA, Webster CR, Flaspohler DJ, Santos MPD, Silva DP (2017) Forest reserves and riparian corridors help maintain orchid bee (Hymenoptera: Euglossini) communities in oil palm plantations in Brazil. Apidologie 48(5):575–587

    Article  CAS  Google Scholar 

  • Brito TF, Contrera FAL, Phifer CC, Knowlton JL, Brasil LS, Maués MM, Silva DP (2018) Effects of habitat type change on taxonomic and functional composition of orchid bees (Apidae: Euglossini) in the Brazilian Amazon. J Insec Conserv. 22(3–4):451–463

    Article  Google Scholar 

  • Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). J Kans Entomol Soc 60:145–147

    Google Scholar 

  • Clarke GM (1993) Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality. Environ Pollut 82:207–211

    Article  CAS  PubMed  Google Scholar 

  • Costa CP, Francoy TM (2017) The impact of different phytophysiognomies on the composition of orchid bee communities (Hymenoptera: Apidae: Euglossini) in the Atlantic Forest in Brazil. Ann Entomol Soc Am 110(3):255–262

    Google Scholar 

  • Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, New York, p 306

    Google Scholar 

  • Cunha EJ, Montag LFA, Juen L (2015) Oil palm crops effects on environmental integrity of Amazonian streams and Heteropteran (Hemiptera) species diversity. Ecol Indic 52:422–429

    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 

  • De Palma A, Kuhlmann M, Roberts SPM, Potts SG, Börger L, Hudson LN, Lysenko I, Newbold T, Purvis A (2015) Ecological traits affect the sensitivity of bees to land-use pressures in European agricultural landscapes. J Appl Ecol 52:1567–1577

    Article  PubMed  PubMed Central  Google Scholar 

  • Del Lama SN, Lopes IF, Del Lama MA (2002) Genetic variability and level of differentiation among Brazilian wood stork populations. Biochem Genet 40:87–99

    Article  PubMed  Google Scholar 

  • Delgado-Acevedo A, Restrepo C (2008) The contribution of habitat loss to changes in body size, allometry, and bilateral asymmetry in two Eleutherodactylus frogs from Puerto Rico. Conserv Biol 22(3):773–782

    Article  PubMed  Google Scholar 

  • Graham JH, Shimizu K, Emlem JM, Freeman DC, Merkel J (2003) Growth models and the expected distribution of fluctuating asymmetry. Biol J Linn Soc 80(1):57–65

    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 

  • Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596

    Article  PubMed  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 

  • Klingenberg CK, McIntyre GS (1998) Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with procrustes methods. Evolution 52:1363–1375

    Article  PubMed  Google Scholar 

  • Koehn RK, Bayne BL (1989) Towards a physiological and genetical understanding of the energetics of the stress response. Biol J Linn Soc 37:157–171

    Article  Google Scholar 

  • Koh LP (2008) Can oil palm plantations be made more hospitable for forest butterflies and birds? J Appl Ecol 45:1002–1009

    Article  Google Scholar 

  • Leary RF, Allendorf FW (1989) Fluctuating asymmetry as an indicator of stress: implications for Conservation Biology. Tree 4(7):214–217

    CAS  PubMed  Google Scholar 

  • Leung B, Forbes MR, Houle D (2000) Fluctuating asymmetry as a bioindicator of stress: comparing efficacy involving multiple traits. Am Nat 155:101–115

    Article  PubMed  Google Scholar 

  • Leung B, Knopper L, Mineau P (2003) A critical assessment of the utility of fluctuating asymmetry as a biomarker of anthropogenic stress. In: Polak M (ed) Developmental Instability: Causes and Consequences. Oxford University Press, New York, pp 415–426

    Google Scholar 

  • Lima CBS, Nunes LA, Carvalho CAL, Ribeiro MF, Souza BA, Silva CSB (2016) Morphometric differences and fluctuating asymmetry in Melipona subnitida Ducke 1910 (Hymenoptera: Apidae) in different types of housing. Braz J Biol 76(4):845–850

    Article  CAS  PubMed  Google Scholar 

  • Livingston G, Jha S, Vega A, Gilbert L (2013) Conservation value and permeability of neotropical oil palm landscapes for orchid bees. PLoS One 8:e78523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lucey JM, Hill JK (2011) Spillover of insects from rain forest into adjacent oil palm plantations. Biotropica 44:368–377

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Milet-Pinheiro P, Schlindwein C (2005) Do euglossine males (Apidae, Euglossini) leave tropical rainforest to collect fragrances in sugarcane monocultures? Rev Bras Zool 22(4):853–858

    Article  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(2):281–284

    Article  PubMed  Google Scholar 

  • Moure JS, Melo GAR, Faria Jr LRR (2012) Euglossini Latreille, 1802. In: Moure JS, Urban D, Melo GAR (eds) Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region - online version. Available at http://www.moure.cria.org.br/catalogue

  • Nemésio A (2009) Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic forest. Zootaxa 2041:1–242

    Article  Google Scholar 

  • Nemésio A, Rasmussen C (2011) Nomenclatural issues in the orchid bees (Hymenoptera: Apidae: Euglossina) and an updated catalogue. Zootaxa 3006:1–42

    Article  Google Scholar 

  • Nemésio A, Vasconcelos HL (2013) Beta diversity of orchid bees in a tropical biodiversity hotspot. Biodiv Conserv 22(8):1647–1661

    Article  Google Scholar 

  • Oliveira ML (2007) Catálogo comentado das espécies de abelhas do gênero Eulaema Lepeletier, 1841 (Hymenoptera: Apidae). Lundiana 8(2):113–136

    Google Scholar 

  • Paiva CKS, Faria APJ, Calvão LB, Juen L (2017) Effect of oil palm on the Plecoptera and Trichoptera (Insecta) assemblages in streams of eastern Amazon. Environ Monit Assess 189:393

    Article  PubMed  Google Scholar 

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

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  • Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power of statistical tests. In: Zakharov MV, Graham JH (eds) Developmental stability in natural populations, vol 191. Acta Zoologica Fennica, Finnish Zoological Publishing Board, Helsinki, pp 57–72

    Google Scholar 

  • Parsons PA (2005) Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency. Biol Rev 80:589–610

    Article  PubMed  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 20(2):207–212

    Article  Google Scholar 

  • Pinto NS, Silva DP, Rodrigues JG, De Marco P Jr (2015) 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(5):439–447

    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 

  • Rader R, Bartomeus I, Tylianakis JM, Laliberté E (2014) The winners and losers of land use intensification: pollinator community disassembly is non-random and alters functional diversity. Divers Distrib 20(8):908–917

    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 

  • Rosa JF, Ramalho M, Monteiro D, Silva MD (2015) Permeability of matrices of agricultural crops to Euglossina bees (Hymenoptera, Apidae) in the Atlantic rain Forest. Apidologie 46:691–702

    Article  Google Scholar 

  • Sanseverino AM, Nessimian JL (2008) Larvas de Chironomidae (Insecta: Diptera) em depósitos de folhiço submerso em um riacho de primeira ordem da Mata Atlântica (Rio de Janeiro, Brasil). Rev Bras Entomol 52:95–104

    Article  Google Scholar 

  • Shimano Y, Juen L (2016) How oil palm cultivation is affecting mayfly assemblages in Amazon streams. Ann Limnol - Int J Lim 52:35–45

    Article  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(2):730–737

    Article  CAS  PubMed  Google Scholar 

  • Sommer C (1996) Ecotoxicology and developmental stability as an in-situ monitor of adaptation. Ambio 25(5):374–376

    Google Scholar 

  • Soto IM, Carreira VP, Soto EM, Hasson E (2008) Wing morphology and fluctuating asymmetry depend on the host plant in cactophilic Drosophila. J Evol Biol 21:598–609

    Article  CAS  PubMed  Google Scholar 

  • Stewart SS, Vodopich DS (2013) Variation in fluctuating asymmetry among nine damselfly species. Int J Odonatol 16:67–77

    Article  Google Scholar 

  • Storck-Tonon D, Peres CA (2017) Forest patch isolation drives local extinctions of Amazonian orchid bees in a 26 years old archipelago. Biol Conserv 214:270–277

    Article  Google Scholar 

  • Storck-Tonon D, Morato EF, Oliveira ML (2009) Fauna de Euglossina (Hymenoptera: Apidae) na Amazônia Sul-Ocidental, Acre, Brasil. Acta Amaz 39(3):693–706

    Article  Google Scholar 

  • Storck-Tonon D, Morato EF, Melo AWF, Oliveira ML (2013) Orchid bees of forest fragments in Southwestern Amazonia. Biota Neotrop 13(1):133–141

    Article  Google Scholar 

  • Turner EC, Snaddon JL, Ewers RM, Fayle TM, Foster WA (2011) The impact of oil palm expansion on environmental change: putting conservation research in context. In: Bernardes MAS (ed) Environmental impact of biofuels. InTech Press, Rijeka, pp 19–40

    Google Scholar 

  • Viana BF, Melo AMC, Drumond PD (2006) Variação na estrutura do habitat afetando a composição de abelhas e vespas solitárias em remanescentes florestais urbanos de Mata Atlântica no Nordeste do Brasil. Sitientibus Sér Ciên Biol 6(4):282–295

    Article  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Williams NM, Crone EE, Roulston TH, Minckley RL, Packer L, Potts SG (2010) Ecological and life history traits predict bee species responses to environmental disturbances. Biol Conserv 143(10):2280–2291

    Article  Google Scholar 

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Acknowledgements

We thank Agropalma Group for permitting this research on their property. We are grateful to the Embrapa Amazônia Oriental agency for its laboratory support and bee reference collection access. We also thank two independent reviewers for constructive criticisms to a previous version of this manuscript. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–Brasil (CAPES)–Finance Code FAPAC 007/2014, to TFB. We also thank the US National Science Foundation for its support (grant numbers 124344 and DEB–1019928) of this research. DPS was supported by a productivity grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Proc. Number: 304494/2019-4). NSP thanks CNPq for a post-doctoral scholarship (CNPq-Proc. Number: 160656/2019-2).

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Authors and Affiliations

  1. Programa de Pós-Graduação em Zoologia, Universidade Federal do Pará/Museu Paraense Emílio Goeldi, Belém, Pará, Brazil

    Thaline de Freitas Brito

  2. Laboratório de Biologia e Ecologia de Abelhas, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil

    Thaline de Freitas Brito & Felipe A. L. Contrera

  3. Centro Universitário UniAraguaia, Goiânia, Goiás, Brazil

    Nelson S. Pinto

  4. School of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, USA

    Colin C. Phifer

  5. Department of Biology, Wheaton College, Norton, MA, USA

    Jessie L. Knowlton

  6. Laboratório de Entomologia, Embrapa Amazônia Oriental, Belém, Pará, Brazil

    Márcia M. Maués

  7. Departamento de Ciências Biológicas, Instituto Federal Goiano, Urutaí, Goiás, Brazil

    Daniel P. Silva

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  1. Thaline de Freitas Brito
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  2. Nelson S. Pinto
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  6. Márcia M. Maués
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Contributions

Conceptualization: CCP, JLK, DPS, TFB; methodology: CCP, JLK, DPS, TFB; formal analysis and investigation: TFB, NSP; writing—original draft preparation: TFB, DPS; writing—review and editing: CCP, JLK, DPS, NSP, FALC, MMM.

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Correspondence to Thaline de Freitas Brito.

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Brito, T.d.F., Pinto, N.S., Phifer, C.C. et al. Orchid bees (Apidae, Euglossini) from Oil Palm Plantations in Eastern Amazon Have Larger but Not Asymmetrical Wings. Neotrop Entomol 50, 388–397 (2021). https://doi.org/10.1007/s13744-021-00864-4

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