Morphometric Changes in Three Species of Euglossini (Hymenoptera: Apidae) in Response to Landscape Structure


  • Mariléa Ribeiro Universidade Estadual de Feira de Santana
  • Willian Moura Aguiar Universidade Estadual de Feira de Santana
  • Lorena Andrade Nunes Universidade Estadual de Feira de Santana
  • Lazaro da Silva Carneiro Universidade Estadual de Feira de Santana



Agroforestry system, Atlantic Forest, environmental stress, fragmentation, geometric morphometrics, solitary bee


Fragmentation and expansion of agricultural activities are sufficient factors for strongly impacting the biodiversity. Thus, sustainable practices of land use, such as agroforestry systems, are adopted with proposal of improving environmental quality and restore ecological processes. In flying insects, fragmentation may cause changes in the wing shape and size. Therefore, we evaluated the wing size and shape of three species of Euglossini (Eulaema atleticana Nemésio, Euglossa cordata (Linnaeus) and Euglossa ignita Smith) at response to landscape structure. The analysed specimens were collected in five areas, four forest areas with strong anthropic influence and an agroforestry system area. The results of the wing shape analysis have showed that the individuals of the three collected species within the agroforestry system diverge significantly (p<0.05) from those collected in the other areas. On the wings of Eg. cordata and Eg. ignita, differences in shape have occurred mainly in the medial region, which actively participates in the individual's flying ability. The wing size has showed meaningful difference only to the population of Eg. ignita (p=0,005). For Eg. cordata and El. atleticana, there was a significant correlation (r<0.05) between the morphometric data and the landscape metrics, which shows a close relationship between these species and the forest cover. The wing shape and size pursue an important function for the individual's ability in the environment, such as dispersion capacity and fertility rate, respectively. We concluded that the morphometric differences can reveal the existence of environmental stress for the biodiversity, therefore, contribute for environmental quality monitoring studies.


Adams, D.C., Rohlf F.J. & Slice E.D. (2004). Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology 71:5-16

Aguiar, W. M., Sofia, S.H, Melo, G.A.R. & Gaglianone, M.C. (2015). Changes in orchid bee communities across forest-agroecosystem boundaries in Forest Atlantic Forest landscapes. Environmental Entomology 44: 1465-1471. doi: 10.1093/ee/nvv130

Aguiar, W.M. & Gaglianone, M.C. (2008). Comunidade de abelhas Euglossina (Hymenoptera: Apidae) em remanescentes de mata Estacional Semidecidual sobre Tabuleiro no estado do Rio de Janeiro. Neotropical Entomology 37:118–125

Bai.Y, Ma, L.B., Xu, S.Q. & Wang, G.H. (2015). A geometric morphometric study of the wing shapes of Pieris rapae (Lepidoptera:Pieridae) from the Qinling Mountains and adjacent regions: an environmental and distance-based consideration. Florida Entomological Society 98:162-169. doi:10.1653/024.098.0128

Benítez, H., Briones, R. & Jerez, V. (2008). Asimetria fluctuante en dos poblaciones de Ceroglossus chilensis (Eschscholtz, 1829) (Coleoptera: Carabidae) en el agroecosistema Pinus radiata D. don Region Del Bio-Bio, Chile. Gayana 72:131-139

Benjamin, F.E., Reilly, J.R. & Winfree, R. (2014). Pollinator body size mediates the scale at which land use drives crop pollination services. Journal of Applied Ecology 51:440–449. doi: 10.1111/1365-2664.12198

Bennett, A.F. & Saunders, D.A. (2010). Habitat fragmentation and landscape change. In: Sodhi NS, Ehrlich PR (Eds.), Conservation Biology for All (pp.88-106) Oxford: Oxford.

University Press.

Bookstein, F.L. (1989). Principal warps, thin-plate splines and the decomposition of deformations. IEEE Transactions on Pattern Analysis and Machine Intelligence 11:567-585

Brosi, B.J. (2009). The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biological Conservation 142:414-423. doi:10.1016/j.biocon.2008.11.003

Cardinael, R., Chevallier, T., Cambou, A., Béral, C., Barthès, B.G., Dupraz, C. et al. (2017). Increased soil organic carbon stocks under agroforestry: A survey of six different sites in France. Agriculture, Ecosystems and Environment 236:243-255. doi: 10.1016/j.agee.2016.12.011

Chown, S.L. & Gaston, K.J. (2010). Body size variation in insects: a macroecological perspective. Biological Reviews 85:139-169

Dellicour, S., Gerard, M., Prunier, J.G., Dewulf, A., Kuhlmann, M. & Michez, D. (2017). Distribution and predictors of wing shape and size variability in three sister species of solitary bees. PLoS ONE. doi:10.1371/journal.pone.0173109

Dressler, R.L. (1982). Biology of the orchid bees (Euglossini). Annual Review of Ecology, Evolution, and Systematics 13:373-394

Francoy, T.M., Franco, F.F. & Roubik, D.W. (2012). Integrated landmark and outline-based morphometric methods efficiently distinguish species of Euglossa (Hymenoptera, Apidae, Euglossini). Apidologie 43:609-617. doi: 10.1007/s13592-012-0132-2

Freiria, G.A., Garófalo, C.A. & Del Lama, M.A. (2017). The primitively social behavior of Euglossa cordata (Hymenoptera, Apidae, Euglossini): a view from the perspective of kin selection theory and models of reproductive skew. Apidologie. doi: 10.1007/s13592-017-0496-4

Ghosh, S.M., Testa, N.D. & Shingleton, A.W. (2013).Temperature-size rule is mediated by thermal plasticity of critical size in Drosophila melanogaster. Proceedings of the Royal Society Biological Sciences 280:1-8. doi:

IBGE (Instituto Brasileiro de Geografia e Estatística). (2012). Manual técnico da vegetação brasileira. IBGE, Rio de Janeiro, 271p

Jauker, B., Krauss, J., Jauker, F. & Steffan-Dewenter, I. (2013). Linking life history traits to pollinator loss in fragmented calcareous grasslands. Landscape Ecology 28:107–120. doi: 10.1007/s10980-012-9820-6

Johansson, F., Soderquist, M. & Bokma, F. (2009). Insect wing shape evolution: independent effects of migratory and mate guarding flight on dragonfly wings. Biological Journal of the Linnean Society 97:362–372

Hammer, O., Harper, D.A.T. & Ryan, P.D. (2001). PAST: Paleontological Statistics software package for education and data analysis. Paleontologia Electronica 4:1-9

Hill, J.D., Thomas, C.D., Lewis, O.T. (1999). Flight morphology in fragmented populations of a rare British butterfly, Hesperia comma. Biological Conservation 87:277-283

Kennedy, C.M., Lonsdorf, E., Neel, M.C., Williams, N.M., Ricketts, T.H., Winfree, R. et al. (2013). A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecology Letters 16: 584-599. doi: 10.1111/ele.12082

Kingsolver, J.G. & Huey, R.B. (2008). Size, temperature, and fitness: three rules. Evolutionary Ecology Research 10:251-268

Klingenberg, C.P. (2008). MORPHOJ. Faculty of Life Scienses, University of Manchester, UK. Version (2008). Disponível em: Acesso em: 09 set. 2015

Kremen, C., Williams, N.M. & Thorp, R.W. (2002). Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Sciences, USA 99:16812–16816. doi:10.1073pnas.262413599

Mcgarical, K. & Ene, E. (2013). Fragstats 4.2: A spatial pattern analysis program for categorical maps. Copyright

Matos, M.C.B., Sousa-Souto, L., Almeida, R.S. & Teodoro, A.V. (2013). Contrasting patterns of species richness and composition of solitary wasps and bees (Insecta-Hynenoptera) according to land use. Biotropa 45:73-79. doi: 10.1111/j.1744-7429.2012.00886.x

Merckx, T. & Van Dyck, H. (2006). Landscape structure and phenotypic plasticity in flight morphology in the butterfly Pararge aegeria. Oikos 113:226-232

Moczek, A.P. (2010). Phenotypic plasticity and diversity in insects. Philosophical Transactions of the Royal Society 365:593-603.doi: 10.1098/rstb.2009.0263

Monteiro, L.R. & Reis, S.F. (1999). Princípios de morfometria geométrica. Ribeirão Preto: Holos, 198 p

Nascimento, A., Fischer, C.M., Pierini, C., Fischer, F., Rocha, L., Matos, L.B. et al. (2007) Baixo Sul da Bahia: uma proposta de desenvolvimento territorial. Salvador: CIAGS/UFBA, 224 p

Nemésio A (2009) Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa. New Zeland: Magnolia Press, 242 p

Neves, C.M.L., Carvalho, C.A.L., Souza, A.V. & Lima Junior, C.A. (2012). Morphometric Characterization of a Population of Tetrapedia diversipes in Restricted Areas in Bahia, Brazil (Hymenoptera: Apidae). Sociobiology 59:767-782

Nijhout, H.F. & Callier, V. (2015). Developmental mechanisms of body size an wing-body scaling in insects. Annual Review of Entomology 60:141-156. doi: 10.1146/annurev-ento-010814-020841

Nunes, L.A., Passos, G.B., Carvalho, C.A.L. & Araújo, E.D. (2013). Size and shape in Melipona quadrifasciata anthidioides Lepeletier, 1836 (Hymenoptera; Meliponini). Brazilian Journal of Biology 73:887-893. doi: 10.1590/S1519-69842013000400027

Outomuro, D., Dijkstra, D.B. & Johansson, F. (2013). Habitat variation and wing coloration affect wing shape evolution in dragonflies. Journal of Evolutionary Biology 26:1866-1874. doi: 10.1111/jeb.12203

Pokorny, T., Loose, D., Dyker, G., Quezada-Euán, J.J.G. & Eltz, T. (2014) Dispersal ability of male orchid bees and direct evidence for long-range flights. Apidologie. doi: 10.1007/s13592-014-0317-y

Prudhomme, J., Cassan, C., Hide, M., Toty, C., Rahola, N., Vergnes, B. et al. (2016). Ecology and morphological variations in wings of Phlebotomus ariasi (Diptera: Psychodidae) in the region of Roquedur (Gard France): a geometric morphometrics approach. Parasites and Vectors 578:1-13. doi: 10.1186/s13071-016-1872-z

Reed, T.E., Schindler, D.E. & Waples, R.S. (2011). Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conservation Biology 25:56-63. doi:10.1111/j.1523-1739.2010.01552.x

Renauld, M., Hutchinson, A., Loeb, G., Poveda, K. & Connelly, H. (2016). Landscape simplification constrains adult size in a native ground-nesting bee. PLoS ONE. doi:10.1371/journal.pone.0150946

Richtsmeier, J.T., Deleon, V.B. & Lele, S.R. (2002). The promise of geometric morphometrics. Yeardbook of Physical Anthropology 45: 63-91. doi: 10.1002/ajpa.10174

Rohlf, F.J. (2010). Relative warps-tpsRelw, version 1.49. Department of Ecology and Evolution, State University of New York, Suny at Stony Brook

Rohlf, F.J. (2013). tps Utility program, version 1.60. Department of Ecology and Evolution, State University of New York, Suny at Stony Brook

Rohlf, F.J. (2015). tpsDig2, version 2.18.Department of Ecology and Evolution, State University of New York, Suny at Stony Brook

Silva, M.C., Lomônaco, C., Augusto, S.C. & Kerr, W.E. (2009). Climatic and anthropic influence on size and fluctuating asymmetry of Euglossine bees (Hymenoptera, Apidae) in a semideciduous seasonal forest reserve. Genetics and Molecular Research 8:730-737

Sistla, S.A., Roddy, A.B., Williams, N.E., Kramer, D.B., Stevens, K. & Allison, S.D. (2016). Agroforestry practices promote biodiversity and natural resource diversity in Atlantic Nicaragua. PLoS ONE. doi:10.1371/journal.pone.0162529

Skandalis, D.A., Tattersall, S.P. & Richards, M.H. (2009). Body size and shape of the large Carpenter bee, Xylocopoda virginica (L.) (Hymenoptera: Apidae). Journal of the Kansas Entomological Society 82: 30-42. doi: 10.2317/JKES711.05.1

Torralba, M., Fagerholm, N., Burgess, P.J., Moreno, G. & Plieninger, T. (2016). Do European agroforestry systems enhance biodiversity and ecosystem services? A meta-analysis. Agriculture, Ecosystems and Environment 230:150-161. doi: 10.1016/j.agee.2016.06.002

Wang, J., Ren, C., Cheng, H., Zou, Y., Bughio, M.A. & Li, Q. (2017). Conversion of rainforest into agroforestry and monoculture plantation in China: Consequences for soil phosphorus forms and microbial community. Science of the Total Environment 595:769-778. doi: 10.1016/j.scitotenv.2017.04.012

Whitman, D.W. & Agrawal, A.A. (2009). What is phenotypic plasticity and why is it important? In: Whitman, D.W. & Ananthakrishnan, T.N. (Eds), Phenotypic Plasticity of Insects. (pp.1-63). USA: Science Publishers, Enfield.




How to Cite

Ribeiro, M., Aguiar, W. M., Nunes, L. A., & Carneiro, L. da S. (2019). Morphometric Changes in Three Species of Euglossini (Hymenoptera: Apidae) in Response to Landscape Structure. Sociobiology, 66(2), 339–347.



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