Antennal Sensilla of Workers of Melipona quadrifasciata anthidioides Lepeletier (Apidae, Meliponini) Removing and non-Removing Dead Brood: Morphology, Morphometry and Quantity
DOI:
https://doi.org/10.13102/sociobiology.v72i4.11823Keywords:
hygienic bee, olfactory system, stingless bee, unhygienic beeAbstract
The sophisticated chemical communication of bees allows the natural control of pathogens and diseases in the colony, through hygienic behavior (HB), in which dead or sick brood are removed, improving colony health. In this study, we investigated the morphology, morphometry and quantity of sensilla of workers of Melipona quadrifasciata anthidioides, removing and non-removing dead brood in the HB test. From the micrographs obtained through scanning electron microscopy, the sensilla trichodea (STr), basiconic (SBa), placodea (SPl), coeloconic (SCo), campaniform (SCa), ampullacea (SAm), cetica (SCe), chaetica (SCha), and its subtypes were morphologically characterized. We highlight the identification of sensilla STr 7, setae (SSe), placodea 2 (SPl 2), Bohm's bristles (BhB) and branched bristles (BB), not previously reported in this species. Morphometry indicates that removing workers have a longer average length of the antenna and its segments than non-removing bees, as well as the length of the SCo, SPl 1, SSe, STr 1, STr 2, STr 3 and STr 4 sensilla. Regarding the quantification of sensilla, there was no significant difference between the groups. Considering that chemical stimuli incite bee HB, sensilla may play a fundamental role in hygienic bee lineages, and there is a need to further explore this relationship to understand bee HB.
Downloads
References
Addinsoft. (2019). XLSTAT statistical and data analysis solution. Long Island, NY.
Arathi, H.S., Burns, I. & Spivak, M. (2000). Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioural repertoire of hygienic bees. Ethology, 106: 365-379.
Azevedo, D.O., Matiello-Guss, C.P., Rönnau, M., Zanuncio, J.C. & Serrão, J.E. (2008). Post-embryonic development of the antennal sensilla in Melipona quadrifasciata anthidioides (Hymenoptera: Meliponini). Microscopy Research and Technique, 71: 196-200.
Bigio, G., Schürch, R. & Ratnieks, F.L.W. (2013). Hygienic behaviour in honey bees (Hymenoptera: Apidae): effects of brood, food, and time of the year. Journal of Economic Entomology, 106: 2280-2285.
Carvalho, W.J., Fujimura, P.T., Bonetti, A.M., Goulart, L.R., Cloonan, K., Silva, N.M. & Leal, W.S. (2017). Characterization of antennal sensilla, larvae morphology and olfactory genes of Melipona scutellaris stingless bee. PloS One, 12: e0174857.
Chen, H.H., Zhao, Y.X. & Kang, L. (2003). Antennal sensilla of grasshoppers (Orthoptera: Acrididae) in relation to food preferences and habits. Journal of Biosciences, 28: 743-752.
Cruz-Landim, C. (2009). Abelhas: morfologia e função de sistemas. São Paulo: Editora UNESP, 408p.
Dohanik, V.T., Souza, E.A., Lisboa, L.C.O., Zanuncio, J.C. & Serrão, J.E. (2017). Development of antennal sensilla of Tetragonisca angustula Latreille, 1811 (Hymenoptera: Meliponini) during pupation. Brazilian Journal of Biology, 77: 284-288.
Elgar, M.A., Zhang, D., Wang, Q., Wittwer, B., Thi Pham, H., Johnson, T.L., Freelance, C.B. & Coquilleau, M. (2018). Focus: ecology and evolution: insect antennal morphology: the evolution of diverse solutions to odorant perception. The Yale Journal of Biology and Medicine, 91: 457-469.
Evans, J.V. & Shutler, D. (2023). The importance of Apis mellifera olfaction to social immunity. Journal of Apicultural Research, 64: 150-158.
Fialho, M.D.C.Q., Guss-Matiello, C.P., Zanuncio, J.C., Campos, L.A.O. & Serrão, J.E. (2014). A comparative study of the antennal sensilla in corbiculate bees. Journal of Apicultural Research, 53: 392-403.
Frasnelli, E., Anfora, G., Trona, F., Tessarolo, F. & Vallortigara, G. (2010). Morpho-functional asymmetry of the olfactory receptors of the honeybee (Apis mellifera). Behavioural Brain Research, 209: 221-225.
Gebremedhn, H., Claeys Bouuaert, D., Asperges, M., Amssalu, B., De Smet, L. & de Graaf, D.C. (2023). Expression of molecular markers of resilience against Varroa destructor and bee viruses in Ethiopian honey bees (Apis mellifera simensis) focussing on olfactory sensing and the RNA Interference Machinery. Insects, 14: 436.
Gramacho, K.P. & Spivak, M. (2003). Differences in olfactory sensitivity and behavioral responses among honey bees bred for hygienic behavior. Behavioral Ecology and Sociobiology, 54: 472-479.
Gramacho, K.P., Gonçalves, L.S., Stort, A.C. & Noronha, A.B. (2003). Is the number o antennal plate organs (sensilla placodea) greater in hygienic than in nonhygienic Africanized honey bees? Genetics and Molecular Research, 2: 309-316.
Guarna, M.M., Melathopoulos, A.P., Huxter, E., Iovinella, I., Parker, R., Stoynov, I., Tam, A., Moon, K-M, Chan, Q.W.T., Pelosi, P., White, R., Pernal, S.F. & Foster, L.J. (2015). A search for protein biomarkers links olfactory signal transduction to social immunity. BMC Genomics, 16:1-16.
Grüter, C. & Keller, L. (2016). Inter-caste communication in social insects. Current Opinion in Neurobiology, 38: 6-11.
Huang, X., Xu, X.L., Li, R.X., Wang, S. & Tian, L.X. (2023). Ultrastructure and distribution of antennal sensilla of Bombus terrestris (Hymenoptera: Apidae). Zoologischer Anzeiger, 302: 239-247.
Jesus, J.N., Chambó, E.D., Silva, G.S., Oliveira, N.T.E. & Carvalho, C.A.L. (2017). Hygienic behavior in Melipona quadrifasciata anthidioides (Apidae, Meliponini). Apidologie, 48: 504-512.
Kaissling, K.E. & Renner, M. (1968). Antennale rezeptoren für queen substance und sterzelduft bei der honigbiene. Zeitschrift fuer Vergleichende Physiologie, 59: 357-361.
Kannan, K., Galizia, C.G. & Nouvian, M. (2022). Olfactory strategies in the defensive behaviour of insects. Insects, 13: 470.
Masterman, R., Smith, B.H. & Spivak, M. (2000). Brood odor discrimination abilities in hygienic honey bees (Apis mellifera L.) using proboscis extension reflex conditioning. Journal of Insect Behavior, 13: 87-101.
McAfee, A., Chapman, A., Iovinella, I., Gallagher-Kurtzke, Y., Collins, T.F., Higo, H., Madilao, L.L., Pelosi, P. & Foster, L.J. (2018). A death pheromone, oleic acid, triggers hygienic behavior in honey bees (Apis mellifera L.) Scientific Reports, 8: 5719.
Mondet, F., Alaux, C., Severac, D., Rohmer, M., Mercer, A.R., Le Conte, Y. (2015) Antennae hold a key to Varroa-sensitive hygiene behaviour in honey bees. Scientific Reports, 5: 10454.
Moraes, R.L.M.S. & Cruz-Landim, C. (1972). Estudo comparativo de órgãos sensoriais em abelhas com diferentes tipos de comunicação. Revista Brasileira de Biologia, 32: 185-196.
Nascimento, M.A., Fernandes-Salomão, T.M. & Martins, G.F. (2013). Estudo comparativo das sensilas antenais de operárias de Melipona scutellaris (Hymenoptera: Apidae) de diferentes altitudes. EntomoBrasilis, 6: 64-67.
Ravaiano, S.V., Ferreira, R.D.P., Campos, L.A.O. & Martins, G.F. (2014). The antennal sensilla of Melipona quadrifasciata (Hymenoptera: Apidae: Meliponini): a study of different sexes and castes. Naturwissenschaften, 101: 603-611.
Ren, C.S., Chang, Z.M., Zu, Z.Y., Han, L., Chen, X.S. & Long, J.K. (2023). Comparison of morphological characteristics of antennae and antennal sensilla among four species of bumblebees (Hymenoptera: Apidae). Insects, 14: 232.
Spivak, M. & Reuter, G.S. (1998). Performance of hygienic honey bee colonies in a comercial apiary. Apidologie, 29: 291-302.
Spivak, M., Masterman, R., Ross, R., Mesce, K. A. (2003) Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. Journal of Neurobiology, 55: 341-354.
Stort, A.C. & Moraes-Alves, M.M.B. (1999). Differences in the number of the antennal sensory structures of males of three honey bee types. Revista Brasileira de Biologia, 59: 161-166.
Swanson, J.A., Torto, B., Kells, S.A., Mesce, K.A., Tumlinson, J.H. & Spivak, M. (2009). Odorants that induce hygienic behavior in honeybees: identification of volatile compounds in chalkbrood-infected honeybee larvae. Journal of Chemical Ecology, 35: 1108-1116.
Van Baaren, J., Boivin, G., Le Lannic, J. & Nénon, J.P. (1999). Comparison of antennal sensilla of Anaphes victus and Anaphes listronoti (Hymenoptera: Mymaridae), egg-parasitoids of Curculionidae. Zoomorphology, 119: 1-8.
Wagoner, K.M., Millar, J.G., Schal, C. & Rueppell, O. (2020). Cuticular pheromones stimulate hygienic behavior in the honey bee (Apis mellifera). Scientific Reports, 10: 7132.
Wilson-Rich, N., Spivak, M., Fefferman, N.H. & Starks, P.T. (2009). Genetic, Individual and Group Facilitation of Disease Resistance in Insect Societies. Annual Review of Entomology, 54: 405-423.
Yan, H., Jafari, S., Pask, G., Zhou, X., Reinber, G. D., Desplan, C. (2020) Evolution, developmental expression and function of odorant receptors in insects. Journal of Experimental Biology, 223: jeb208215.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2025 Jossimara Neiva de Jesus, Johnnatan Duarte de Freitas, Paulo Roberto Ribeiro de Mesquita, Carlos Alfredo Lopes de Carvalho, Frederico de Medeiros Rodrigues, Cândida Maria Lima Aguiar

This work is licensed under a Creative Commons Attribution 4.0 International License.
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).

eISSN 2447-8067









