Fluctuating Asymmetry in Melipona scutellaris (L.) 1811 (Hymenoptera: Apidae) Associated to Stress due to Transportation of Colonies


  • Brunelle Ramos Andrade
  • Eliaber Barros Santos
  • Lorena Andrade Nunes
  • Andreia Santos do Nascimento
  • Carlos Alfredo Lopes de Carvalho




stingless bee, migrating meliponiculture, shape


Transportation to long distances and handling of colonies can affect development and survival conditions of bees. Our study investigated the stress intensity of individuals of Melipona scutellaris Latreille, 1811, due to transportation of colonies to long distances, within the natural range of the species. We used 746 bee workers. The right and left forewings were removed and measured using 15 landmarks in vein insertions. Individuals were divided into four groups: (1) workers collected at the origin site, (2) workers emerged at the place of destination in pupal stage during transportation, (3) workers emerged at the destination site in the 3rd instar of larval stage during transportation, and (4) workers collected after three months of colony establishment at the destination site. The Procrustes ANOVA showed significant results as well as the presence of Fluctuating Asymmetry (FA) in all treatments for the shape of wings (P<0.01). However, in the comparison of groups using the One-Way ANOVA, only workers that emerged at the destination site in the 3rd instar of larval stage during transportation (Group 3) significantly differentiated (P<0.05) from the others, with a higher FA index. The larval stage underwent more stress due to colony transportation. Beekeepers should take good care of colonies during transportation in order to minimize damages to workers to prevent quality loss of services and products offered by bees.


Download data is not yet available.


Ahn, K., Xie, X., Riddle, J., Pettis, J. & Huang, Z. Y. (2012) Effects of Long Distance Transportation on Honey Bee Physiology. Psyche, 2012: 1-9. doi: 10.1155/2012/193029

Banaszak-Cibicka, W., Fliszkiewicz, M., Langowska, A., Żmihorski, M. (2018). Body size and wing asymmetry in bees along an urbanization gradient. Apidologie, 49: 297-306. doi:10.1007/s13592-017-0554-y

Belsky, J. & Joshi, N.K. (2019). Impact of Biotic and Abiotic Stressors on Managed and Feral Bees. Insects, 10: 1-42. doi:10.3390/insects10080233

Chouvenc, T., Basille, M., Li, H.F. & Su, N.Y. (2014). Developmental instability in incipient colonies of social insects. PLoS One, 9:1-16. doi.org/10.1371/journal.pone. 0113949

Clarke, G. M. (1995). Relationships between developmental stability and fitness: Application for conservation biology. Conserv Biol, 9:18-24. doi: 10.1046/j.1523-1739.1995.09010018.x

Clarke, G.M. (1998). The genetic basic of developmental stability. IV. Individual and population asymmetry parameters. Heredlty, 80: 553-561. doi: 10.1046/j.1365-2540.1998.00326.x

Cranston, P.S. & Gullan P.J. (2017). Insetos: Fundamentos da Entomologia. 5ª ed. Rio de Janeiro: Roca, 460 p

Del Sarto, M.C., Oliveira, E.E., Guedes, R.N.C. & Campos, L.A.O. (2014). Differential insecticide susceptibility of the neotropical stingless bee Melipona quadrifasciata and the honey bee Apis mellifera. Apidologie, 45: 626-636. doi: 10.1007/s13592-014-0281-6

Domingos, H.G.T. & Gonçalves, L.S. (2014). Thermoregulation in bees with emphasis on Apis mellifera. Acta Veterinaria Brasilica, 8: 151-154. doi: 10.21708/avb.2014.8.3.3491

Evgen’ev, M.B., Garbuz, D. & Zatsepina, O. (2014). Heat shock proteins and whole body adaptation to extreme environments. Netherlands: Springer, 212 p

Glenny, G., Cavigli, I., Daughenbaugh, K.F. Radford, R., Kegley, S.E. & Flenniken, M.L. (2017). Honey bee (Apis mellifera) colony health and pathogen composition in migratory beekeeping operations involved in California almond pollination. Plos One, 12: e0182814. doi: 10.1371/journal.pone.0182814

Hepburn, H.R., Radloff, S.E. & Fuchs, S. (1999). Flight machinery dimensions of honeybees, Apis mellifera. Journal of Comparative Physiology B, 169: 107-112. doi: 10.1007/s003600050200

Klingenberg, C.P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11: 353-357. doi: 10.1111/j.1755-0998.2010.02924.x

Klingenberg, C.P. (2015). Analyzing fluctuating asymmetry with geometric morphometrics: concepts, methods, and applications. Symmetry, 7: 843-934. doi: 10.3390/sym7020843

Klingenberg, C.P. & Mcintyre, G.S. (1998). Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution, Lancaster, 52: 1363-1375. doi: 10.2307/2411306

Li, Y., Zhao, Q., Duan, X., Song, C. & Chen, M. (2017). Transcription of four Rhopalosiphum padi (L.) heat shock protein genes and their responses to heat stress and insecticide exposure. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 205: 48-57. doi: 10.1016/j.cbpa.2016.12.021

Lijteroff, R., Lima, L. & Prieri, B. (2008). Uso de líquenes como bioindicadores de contaminación atmosférica em la ciudad de San Luis, Argentina. Revista Internacional de Contaminación Ambiental, 25: 111-120.

Lima, C.B.S., Nunes, L.A., Carvalho, C.A.L., Ribeiro, M.F., Souza, B.A. & Silva, C.S.B. (2016). Morphometric differences and fluctuating asymmetry in Melipona subnitidaDucke 1910 (Hymenoptera: Apidae) in different types of housing. Brazilian Journal of Biology, 76: 845-850. doi: 10.1590/1519-6984.01015

Lu, K., Chen, X., Liu, W. & Zhou, Q. (2016). Identification of a heat shock protein 90 gene involved in resistance to temperature stress in two wing-morphs of Nilaparvata lugens(Stal). Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 197: 1-8. doi: 10.1016/j.cbpa.2016.02.019

Modro, A.F.H., Marchini, L.C., Moreti, A.C.C.C. & Maia, E. (2012). Influence of pollen on the development of Africanized bee colonies (Hymenoptera: Apidae). Sociobiology, 59: 395-405. doi: 10.13102/sociobiology.v59i2.602

Møller, A.P. (1997). Developmental stability and fitness: a review. The American Naturalist, 149: 916-932.Møller, A.P. & Swaddle, J.P. (1997). Asymmetry, developmental stability and evolution. Oxford: Oxford University Press, 302 p

Nunes, L.A., Araújo, E.D. & Marchini, L.C. (2015). Fluctuating asymmetry in Apis mellifera (Hymenoptera: Apidae) as bioindicator of anthropogenic environments. Revista de Biologia Tropical, 63: 673-682. doi: 10.15517/rbt.v63i3.15869

Palmer, A.R. (1994). Fluctuating asymmetry analyses: a primer. In:

Markow, T.A. (Ed.), Developmental instability: its origins and evolutionary implications (pp. 335-364). Dordrecht: Kluwer Academic Publishers.

Palmer, R.A. & Strobeck, C. (2003). Fluctuating asymmetry analyses revisited. In: Polak, M. (Ed.), Developmental instability (DI): causes and consequences (pp. 279- 319). Oxford: University Press.

Parsons, P.A. (1990). Fluctuating asymmetry: An epigenetic measure of stress. Biological reviews of the Cambridge Philosophical Society, 65: 131-145. doi: 10.1111/j.1469-185X.1990.tb01186.x

Paul, S. & Keshan, B. (2016). Ovarian development and vitellogenin gene expression under heat stress in silkworm, Bombyx mori. Psyche, 2016: 1-8. doi: 10.1155/2016/4242317

Pires, C.S.S., Pereira, F.M., Lopes, M.T.R., Nocelli, R.C.F., Malaspina, O., Pettis, J.S. & Teixeira, E.W. (2016). Enfraque-cimento e perda de colônias de abelhas no Brasil: há casos de CCD?. Pesquisa Agropecuária Brasileira, 51: 422-442. doi: 10.1590/S0100-204X2016000500003

Prado-Silva, A., Nunes, L.A, Santos, J.M., Affonso, P.R.A.M. & Waldschmidt, A.M. (2018). Morphogenetic alterations in Melipona quadrifasciata anthidioides (Hymenoptera: Apidae) associated with pesticides. Archives of Environmental Contamination and Toxicology, 74: 627-632. doi: 10.1007/s00244-018-0509-y

Rech, A.R., Agostini, K., Oliveira, P.E.G.M. & Machado, I.C.S. (2014). Biologia da polinização. Rio de Janeiro: Editora Projeto Cultural, 524 p

Rohlf, F.J. (2017a). TpsUtil for Windows version 1.74. Department of Ecology and Evolution, State University of New York, Stony Book. Retrived from: http://life.bio.sunysb.edu/morph/index.html. Access to: 22 Ago. 2017.

Rohlf, F.J. (2017b). TpsDig for Windows version 2.30. Department of Ecology and Evolution, State University of New York, Stony Book. Retrived from: http://life.bio.sunysb.edu/morph/index.html. Access to: 22 Ago. 2017.

Roubik, D.W. (1989). Ecology and natural history of tropical bees. Cambridge: Cambridge University Press, 514 p

Simone-Finstrom, M., Li-Byarlay, H., Huang, M.H., Strand, M.K., Rueppell, O. & Tarpy, D. R. (2016a). Migratory management and environmental conditions affect lifespan and oxidative stress in honey bees. Scientific Reports, 6: 1-10. doi: 10.1038/srep32023

Simone-Finstrom, M., Walz, M. & Tarpy, D.R. (2016b). Genetic diversity confers colony-level benefits due to individual immunity. Biology Letters, 12: 1-4. doi: 10.1098/rsbl.2015.1007

Tarpy, D.R., Lengerich, E.J. & Pettis, J.S. (2013). Idiopathic brood disease syndrome and queen events as precursors of colony mortality in migratory beekeeping operations in the eastern United States. Preventive veterinary medicine, 108: 225-233. doi: 10.1016/j.prevetmed.2012.08.004

Tomkins, J.L. & Kotiaho, J.S. (2001). Fluctuating Asymmetry. In: Encyclopedia of Life Sciences. Macmillan Publishers Ltd., Nature Publishing Group, 1: 1-5. doi: 10.1038/npg.els.0003741

Truman, J.W. & Riddiford, L.M. (2019). The evolution of insect metamorphosis: a developmental and endocrine view. Philosophical Transactions B, 374: 2-12. doi: 10.1098/rstb.2019.0070

vanEngelsdorp, D., Caron, D., Hayes, J., Underwood, R., Henson, M., Rennich, K., Spleen, A., Andree, M., Snyder, R., Lee, K., Roccasecca, K., Wilson, M., Wilkes, J., Lengerich, E. & Pettis, J. (2012). A national survey of managed honey bee 2010-11 winter colony losses in the USA: results from the Bee Informed Partnership. Journal of Apicultural Research, 51: 115-124. doi: 10.3896/IBRA.

Villas-Bôas, J. (2012). Manual tecnológico: Mel de abelhas sem ferrão. Brasília: Instituto Sociedade, População e Natureza, 96 p

Zhu, X., Zhou, S. & Huang, Z.Y. (2014). Transportation and pollination service increase abundance and prevalence of Nosema ceranae in honey bees (Apis mellifera). Journal of Apicultural Research, 53: 469-471. doi: 10.3896/IBRA.




How to Cite

Ramos Andrade, B., Barros Santos, E., Andrade Nunes, L., Santos do Nascimento, A., & Lopes de Carvalho, C. A. (2020). Fluctuating Asymmetry in Melipona scutellaris (L.) 1811 (Hymenoptera: Apidae) Associated to Stress due to Transportation of Colonies. Sociobiology, 67(3), 417–424. https://doi.org/10.13102/sociobiology.v67i3.4987



Research Article - Bees

Most read articles by the same author(s)