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Type: Article
Published: 2024-01-25
Page range: 124-133
Abstract views: 209
PDF downloaded: 6

Geometric morphometrics of the wings of Amazonian species of Melipona (Illiger, 1806) (Hymenoptera: Apidae)

Instituto Tecnológico Vale—Desenvolvimento Sustentável; R. Boaventura da Silva 955; 66055 090; Belém; Pará; Brazil
Instituto Tecnológico Vale—Desenvolvimento Sustentável; R. Boaventura da Silva 955; 66055 090; Belém; Pará; Brazil
Instituto Tecnológico Vale—Desenvolvimento Sustentável; R. Boaventura da Silva 955; 66055 090; Belém; Pará; Brazil; Pós-Graduação em Biologia (Zoologia); PPGCB; Departamento de Sistemática e Ecologia; Universidade Federal da Paraíba (UFPB); 58059-900; João Pessoa; PB; Brazil; Museu Paraense Emílio Goeldi; MPEG; Pós-graduação em Biodiversidade e Evolução; Av. Magalhães Barata; 376; 66040.170; Belém; Pará; Brazil
Universidade de São Paulo; Instituto de Biociências. Rua do Matão; trav 14; 321; Butantã; 05508090; São Paulo; SP; Brasil
Hymenoptera geometric morphometrics uruçu bees taxonomic classification

Abstract

Identifying and classifying species of stingless Neotropical bees is not a trivial task and requires the help of taxonomists and substantial study and training time. Also, there is a lack of taxonomically useful characters to differentiate among the megadiverse Neotropical group of stingless bees, and to recognize variation. Based on that, we have been testing alternatives to a character-based, efficient taxonomic determination of stingless bees, and herein we performed exploratory analyses of wing shape variation using geometric morphometrics. Thus, we built a data set of photographs of the right anterior wing of 1628 individuals belonging to 11 species in the genus Melipona (Illiger 1806) taken from collection material deposited in entomological collections. We then conducted a Procrustes analysis, followed by a Principal Component Analysis (PCA) and by a Canonical Variable Analyses (CVA). The two first principal components of the PCA accounted for 68% of the variation of the wing shape, and the ordination displayed by the first component separated species of the subgenus Melikerria from the others. In the CVA, the first two canonical axes explained 88% of the wing shape variation found among species, and Melikerria appears as a separate group, apart from the other subgenera in the first canonical axis. Along the second axis species belonging to Eomelipona and Michmelia, and among the Michmelia species, and its species group fuliginosa formed well-separated clusters. The wing shape variation of Melipona supports the recognition of subgenera as currently proposed for Melipona.

 

References

  1. Adams, D.C., Rohlf, F.J. & Slice, D.E. (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71 (1), 5–16. https://doi.org/10.1080/11250000409356545
  2. Adams, D.C., Rohlf, F.J. & Slice, D.E. (2013) A field comes of age: geometric morphometrics in the 21st century. Hystrix, 24 (1), 7.
  3. Baylac, M., Villemant, C. & Simbolotti, G. (2003) Combining geometric morphometrics with pattern recognition for the investigation of species complexes. Biological Journal of the Linnean Society, 8 (1), 89–98. https://doi.org/10.1046/j.1095-8312.2003.00221.x
  4. Bonatti, V., Simões, Z.L., Franco, F.F. & Francoy, T.M. (2014) Evidence of at least two evolutionary lineages in Melipona subnitida (Apidae, Meliponini) suggested by mtDNA variability and geometric morphometrics of forewings. Naturwissenschaften, 101 (1), 17–24. https://doi.org/10.1007/s00114-013-1123-5
  5. Brown, M.J. & Paxton, R.J. (2009) The conservation of bees: a global perspective. Apidologie, 40 (3), 410–416. https://doi.org/10.1051/apido/2009019
  6. Bueno, F.G.B., Kendall, L., Alves, D.A., Tamara, M.L., Heard, T., Latty, T. & Gloag, R. (2023) Stingless bee floral visitation in the global tropics and subtropics. Global Ecology and Conservation, e02454. https://doi.org/10.1016/j.gecco.2023.e02454
  7. Camargo, J.M. & Pedro, S.R. (2008) Revisão das espécies de Melipona do grupo fuliginosa (Hymenoptera, Apoidea, Apidae, Meliponini). Revista Brasileira de Entomologia, 52, 411-427. https://doi.org/10.1590/S0085-56262008000300014
  8. Camargo, J.M.F. & Pedro, S.R.M. (2013) Meliponini Lepeletier, 1836. In: Moure, J. S., Urban, D. & Melo, G.A.R. (Eds.), Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region. Sociedade Brasileira de Entomologia, pp. 272–578. Available from: http://www.moure.cria.org.br/catalogue (accessed 30 April 2023)
  9. Combey, R., Teixeira, J.S., Bonatti, V., Kwapong, P. & Francoy, T.M. (2013) Geometric morphometrics reveals morphological differentiation within four African stingless bee species. Annals of Biological Research, 4 (11), 93–103.
  10. Cortopassi-Laurino, M., Imperatriz-Fonseca, V.L., Roubik, D.W., Dollin, A., Heard, T., Aguilar, I., Venturieri, G.C., Eardley, C. & Nogueira-Neto, P. (2006) Global meliponiculture: challenges and opportunities. Apidologie, 37 (2), 275–292. https://doi.org/10.1051/apido:2006027
  11. Costa, L. (2019) Guia Fotográfico de Identificação de Abelhas Sem Ferrão, para resgate em áreas de supressão florestal. Instituto Tecnológico Vale, Belém, 99 pp.
  12. De Meulemeester, T., Michez, D., Aytekin, A.M. & Danforth, B.N. (2012) Taxonomic affinity of halictid bee fossils (Hymenoptera: Anthophila) based on geometric morphometrics analyses of wing shape. Journal of Systematic Palaeontology, 10 (4), 755–764. https://doi.org/10.1080/14772019.2011.628701
  13. dos Santos, C.F., Souza dos Santos, P.D., Marques, D.M., da-Costa, T. & Blochtein, B. (2019) Geometric morphometrics of the forewing shape and size discriminate Plebeia species (Hymenoptera: Apidae) nesting in different substrates. Systematic Entomology, 44 (4), 787–779. https://doi.org/10.1111/syen.12354
  14. Francisco, F.O., Nunes-Silva, P., Francoy, T.M., Wittmann, D., Imperatriz-Fonseca, V.L., Arias, M.C.& Morgan, E.D. (2008) Morphometrical, biochemical and molecular tools for assessing biodiversity. An example in Plebeia remota (Holmberg, 1903) (Apidae, Meliponini). Insectes Sociaux, 55 (3), 231–237. https://doi.org/10.1007/s00040-008-0992-7
  15. Francoy, T.M., Wittmann, D., Drauschke, M., Müller, S., Steinhage, V., Bezerra-Laure, M.A., De Jong, D. & Gonçalves, L.S. (2008) Identification of Africanized honey bees through wing morphometrics: two fast and efficient procedures. Apidologie, 39 (5), 488–494. https://doi.org/10.1051/apido:2008028
  16. Francoy, T.M. & Imperatriz-Fonseca, V.L. (2010) A morfometria geométrica de asas e a identificação automática de espécies de abelhas. Oecologia Australis, 14 (1), 317–321. https://doi.org/10.4257/oeco.2010.1401.20
  17. Francoy, T.M., Grassi, M.L., Imperatriz-Fonseca, V.L., de Jesús May-Itzá, W. & Quezada-Euán, J.J. (2011). Geometric morphometrics of the wing as a tool for assigning genetic lineages and geographic origin to Melipona beecheii (Hymenoptera: Meliponini). Apidologie, 42 (4), 499. https://doi.org/10.1007/s13592-011-0013-0
  18. Francoy, T.M., de Faria Franco, F. & Roubik, D.W. (2012) Integrated landmark and outline-based morphometric methods efficiently distinguish species of Euglossa (Hymenoptera, Apidae, Euglossini). Apidologie, 43 (6), 609–617. https://doi.org/10.1007/s13592-012-0132-2
  19. Freitas, B.M., Imperatriz-Fonseca, V.L., Medina, L.M., Kleinert, A.D.M.P., Galetto, L., Nates-Parra, G. & Quezada-Euán, J.J.G. (2009) Diversity, threats and conservation of native bees in the Neotropics. Apidologie, 40 (3), 332–346. https://doi.org/10.1051/apido/2009012
  20. Galaschi-Teixeira J.S., Falcon T., Ferreira-Caliman M.J., Witter S. & Francoy T.M. (2018) Morphological, chemical, and molecular analyses differentiate populations of the subterranean nesting stingless bee Mourella caerulea (Apidae: Meliponini). Apidologie, 49 (3), 367–377. https://doi.org/10.1007/s13592-018-0563-5
  21. Giannini, T.C., Alves, D.A., Alves, R., Cordeiro, G.D., Campbell, A.J., Awade, M. & Imperatriz-Fonseca, V.L. (2020) Unveiling the contribution of bee pollinators to Brazilian crops with implications for bee management. Apidologie, 51, 406–421. https://doi.org/10.1007/s13592-019-00727-3
  22. Klingenberg, C.P. (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular ecology resources, 11 (2), 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
  23. Klingenberg, C.P. & McIntyre, G.S. (1998) Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution, 52 (5), 1363–1375 https://doi.org/10.1111/j.1558-5646.1998.tb02018.x
  24. Klingenberg, C.P., Badyaev, A.V., Sowry, S.M. & Beckwith, N.J. (2001) Inferring developmental modularity from morphological integration: analysis of individual variation and asymmetry in bumblebee wings. The American Naturalist, 157 (1), 11–23. https://doi.org/10.1086/317002
  25. Maués, M.M., Boscolo, D., Carvalho, C.A.L., Elias, M.A.S., Ferreira-Caliman, M.J., Gaglianone, M.C. & Imperatriz-Fonseca, V.L. (2019) Bees of Brazil: a review of their diversity, geographic distribution and natural history. The Journal of Basic and Applied Zoology, 80 (1), 1–23.
  26. Melo, G.R. (2021) A new subgenus of the stingless bee genus Melipona (Hymenoptera, Apidae), with a key to the subgenera1. Acta Biológica Paranaense, 50 (1–4), 33–38. https://doi.org/10.5380/abp.v50i1-4.83177
  27. Michener, C.D. (2007) The bees of the world. 2nd Edition. Johns Hopkins University Press, Baltimore, 992 pp. https://doi.org/10.56021/9780801885730
  28. Ndungu, N.N., Kiatoko, N., Ciosi, M., Salifu, D., Nyansera, D., Masiga, D. & Raina, S.K. (2017) Identification of stingless bees (Hymenoptera: Apidae) in Kenya using morphometrics and DNA barcoding. Journal of Apicultural Research, 56 (4), 341–353. https://doi.org/10.1080/00218839.2017.1327939
  29. Ndungu, N., Vereecken, N.J., Gerard, M., Kariuki, S., Kati, L.K., Youbissi, A. & Nkoba, K. (2023) Can the shape of the wing help in the identification of African stingless bee species?(Hymenoptera: Apidae: Meliponini) Wing geometric morphometrics: a tool for african stingless bee taxonomy. International Journal of Tropical Insect Science, 43 (2), 749–759. https://doi.org/10.1007/s42690-023-00980-1
  30. Pedro, S.R. (2014) The stingless bee fauna in Brazil (Hymenoptera: Apidae). Sociobiology, 61 (4), 348–354. https://doi.org/10.13102/sociobiology.v61i4.348-354
  31. Potts, S.G., Imperatriz-Fonseca, V., Ngo, H.T., Aizen, M.A., Biesmeijer, J.C., Breeze, T.D. & Viana, B.F. (2016) Safeguarding pollinators and their values to human well-being. Nature, 540 (7632), 220–229. https://doi.org/10.1038/nature20588
  32. Ramírez, S.R., Nieh, J.C., Quental, T.B., Roubik, D.W., Imperatriz-Fonseca, V.L. & Pierce, N.E. (2010) A molecular phylogeny of the stingless bee genus Melipona (Hymenoptera: Apidae). Molecular Phylogenetics and Evolution, 56 (2), 519–525. https://doi.org/10.1016/j.ympev.2010.04.026
  33. Rasmussen, C. & Cameron, S.A. (2009) Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biological Journal of the Linnean Society, 99 (1), 206–232. https://doi.org/10.1111/j.1095-8312.2009.01341.x
  34. Rattanawannee, A., Chanchao, C. & Wongsiri, S. (2010) Gender and species identification of four native honey bees (Apidae: Apis) in Thailand based on wing morphometric analysis. Annals of the Entomological Society of America, 103 (6), 965–970. https://doi.org/10.1603/AN10070
  35. Rohlf, F.J. & Marcus, L.F. (1993) A revolution in morphometrics. Trends in Ecology & Evolution, 8 (4), 129–132. https://doi.org/10.1016/0169-5347(93)90024-J
  36. Rohlf, F.J. (2015) The tps series of software. Hystrix, 26 (1), 9–12.
  37. Silveira, F.A., Melo, G.A. & Almeida, E.A. (2002) Abelhas brasileiras. Sistemática e Identificação. Fundação Araucária, Belo Horizonte, 253 pp.
  38. Vijayakumar K., Jayaraj K.R. (2013) Geometric morphometry analysis of three species of stingless bees in India. International Journal for Life Sciences and Educational Research, 1 (2) 91–95.
  39. Wappler T., De Meulemeester T., Murat Aytekin A., Michez D. & Engel M.S. (2012) Geometric morphometric analysis of a new Miocene bumble bee from the Randeck Maar of southwestern Germany (Hymenoptera: Apidae). Systematic Entomology, 37 (4), 784–792. https://doi.org/10.1111/j.1365-3113.2012.00642.x