Ovary Activation in Virgin Queens of Plebeia lucii Moure (Hymenoptera: Meliponini)

Authors

  • Ana Paula Pereira Raimundo Federal University of Viçosa, Vicosa-MG, Brazil
  • Natan Martins Silva Federal University of Viçosa, Vicosa-MG, Brazil
  • Jaqueline Amorim Pereira Federal University of Viçosa, Vicosa-MG, Brazil
  • Amanda Martins da Cruz Souza Federal University of Viçosa, Vicosa-MG, Brazil
  • Jullie Anne Pereira Farias Federal University of Viçosa, Vicosa-MG, Brazil
  • José Cola Zanuncio Federal University of Viçosa, Vicosa-MG, Brazil
  • José Eduardo Serrão Federal University of Viçosa, Vicosa-MG, Brazil

DOI:

https://doi.org/10.13102/sociobiology.v72i3.11653

Keywords:

Stingless bees, histology, morphology, vitellarium, pre-copulation

Abstract

Stingless bees (Meliponini) are commonly used in meliponiculture and pollination. In colonies of Plebeia lucii Moure (Hymenoptera: Meliponini), a single queen undergoes changes in hormone profiles, as well as physiological, behavioral, transcriptional, and morphological modifications, particularly after copulation. Among these changes, some bee species exhibit ovary activation in virgin queens before mating. However, few studies have described the reproductive system of virgin queens of Meliponini. The colony’s dynamics depend on the queen, making an understanding of its reproductive biology essential for effective management of this species. This study aimed to determine whether ovary activation occurs before mating in virgin queens of P. lucii. Three virgin queens of P. lucii were collected from royal chambers of different colonies, and their ovaries were analyzed using light microscopy. Each virgin queen possessed two ovaries, each composed of four meroistic polytrophic ovarioles containing a terminal filament, a germarium, and a vitellarium. Oocytes in early developmental stages, spherical in shape and with well-developed nurse cells, were observed in these ovarioles, along with nurse and oocytic chambers in the vitellarium. Additionally, vitellogenesis was observed in the vitellarium, characterized by the formation of elliptical oocytes, yolk accumulation, and the degeneration of adjacent nurse cells. These findings indicate that ovary activation occurs before mating in virgin queens of P. lucii.

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References

Aamidor, S.E., Cardoso-Júnior, C.A.M., Harianto, J., Nowell, C.J., Cole, L., Oldroyd, B.P. & Ronai, I. (2022). Reproductive plasticity and oogenesis in the queen honey bee (Apis mellifera). Journal of Insect Physiology, 136: 104347.

Assis, M.Q., Dohanik, V.T., Oliveira, L.L., Zanuncio, J.C. & Serrão, J.E. (2019). Evidence for a transcellular route for vitellogenin transport in the telotrophic ovary of Podisus nigrispinus (Hemiptera: Pentatomidae). Scientific Reports, 9: 16441.

Baptistella, A.R., Souza, C.C.M., Santana, W.C. & Soares, A.E.E. (2014). Techniques for the in vitro production of queens in stingless bees (Apidae, Meliponini). Sociobiology, 59: 297-310.

Barbiéri, C. & Francoy, T.M. (2020). Theoretical model for interdisciplinary analysis of human activities: meliponiculture as an activity that promotes sustainability. Ambiente e Sociedade, 23: e00202.

Berger, B. & Cruz-Landim, C. (2012). Ovarian ultrastructure in virgin queens of Apis mellifera L. narcotized by CO2. Micron, 43: 832-838.

Bueno, F.G.B., Hajjar, R., Colin, T., Buchmann, G., Latty, T. & Gloag, R. (2023a). Virgin queen behaviour and controlled mating in the stingless bee Tetragonula carbonaria (Meliponini). Insectes Sociaux, 70: 17-27.

Bueno, F.G.B., Santos, C.F., Otesbelgue, A., Menezes, C., Van Veen, J., Blochtein, B., Gloag, R., Heard, T., Imperatriz-Fonseca, V.L. & Alves, D.A. (2023b). The queens of the stingless bees: from egg to adult. Insectes Sociaux, 70: 43-57.

Büning, J. (1994). The insect ovary. Dordrecht: Springer, 400 p.

Church, S.H., Medeiros, B.A.S., Donoughe, S., Márquez Reyes, N.L. & Extavour, C.G. (2021). Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution. Proceedings of the Royal Society B, 288: 20210150.

Cruz-Landim, C. (2000). Ovarian development in Meliponine bees (Hymenoptera: Apidae): the effect of queen presence and food on worker ovary development and egg production. Genetics and Molecular Biology, 23: 83-88.

Cruz-Landim, C., Patrício, K. & Antonialli Jr, W. F. (2006). Cell death and ovarian development in highly eusocial bees (Hymenoptera, Apidae): caste differentiation and worker egg laying. Journal of Morphological Sciences, 23: 27-42.

Cruz-Landim, C., Reginato, R.D. & Imperatriz-Fonseca, V.L. (1997). Variation on ovariole number in Meliponinae (Hymenoptera, Apidae) queen’s ovaries, with comments on ovary development and caste differentiation. Papéis Avulsos de Zoologia, 40: 289-296.

Cullen, G., Delargy, E. & Dearden, P.K. (2024). Development of germline progenitors in larval queen honeybee ovaries. Biology Open, 13: bio060511.

Danforth, B.N., Minckley, R.L. & Neff, J.L. (2019). The solitary bees: biology, evolution, conservation. Princeton University Press.

Dohanik, V.T., Gonçalves, W.G., Oliveira, L.L., Zanuncio, J.C. & Serrão, J.E. (2018). Vitellogenin transcytosis in follicular cells of the honeybee Apis mellifera and the wasp Polistes simillimus. Protoplasma, 255: 1703-1712.

Duell, M.E., Klok, C.J., Roubik, D.W. & Harrison, J.F. (2022). Size-dependent scaling of stingless bee flight metabolism reveals an energetic benefit to small body size. Integrative and Comparative Biology, 62: 1429-1438.

Engel, M.S., Rasmussen, C., Ayala, R., & de Oliveira, F.F. (2023). Stingless bee classification and biology (Hymenoptera, Apidae): a review, with an updated key to genera and subgenera. ZooKeys, 1172: 239.

Gonçalves, R.B. & Brandão, C.R.F. (2008). Diversity of bees (Hymenoptera, Apidae) along a latitudinal gradient in the Atlantic Forest. Biota Neotropica, 8: 51-61.

Grüter, C. (2020). Stingless bees: their behaviour, ecology and evolution. Cham: Springer, 385 p.

Gutzeit, H.O., Zissler, D. & Fleig, R. (1993). Oogenesis in the honeybee Apis mellifera: cytological observations on the formation and differentiation of previtellogenic ovarian follicles. Roux’s Archives of Developmental Biology, 202: 181-191.

Hayworth, M.K., Johnson, N.G., Wilhelm, M.E., Gove, R.P., Metheny, J.D. & Rueppell, O. (2009). Added weights lead to reduced flight behavior and mating success in polyandrous honey bee queens (Apis mellifera). Ethology, 115: 698-706.

Imperatriz-Fonseca, V.L. & Zucchi, R. (1995). Virgin queens in stingless bee (Apidae, Meliponinae) colonies: a review. Apidologie, 26: 231-244.

Kapheim, K.M. (2017). Nutritional, endocrine, and social influences on reproductive physiology at the origins of social behavior. Current Opinion in Insect Science, 22: 62-70.

Kocher, S.D., Richard, F.J., Tarpy, D.R. & Grozinger, C.M. (2008). Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). BMC Genomics, 9: 232.

Macêdo, N.S., Silveira, Z.S., Sousa, A.E.S., Dantas, D.M., Monteiro, A.L.B., Santos, H.S. & Cunha, F.A.B. (2023). Floral visitation, phytochemical and biological activities of bioproducts from Tetragonisca angustula (Hymenoptera, Apidae, Meliponini): a review. Chemistry and Biodiversity, 20: e202301451.

Marques, R.D., Lima, M.A.P., Marques, R.D. & Bernardes, R.C. (2020). A spinosad-based formulation reduces the survival and alters the behavior of the stingless bee Plebeia lucii. Neotropical Entomology, 49: 578-585.

Martins, G.F. & Serrão, J.E. (2004). Changes in the reproductive tract of Melipona quadrifasciata anthidioides (Hymenoptera: Apidae, Meliponini) queen after mating. Sociobiology, 44: 241-254.

Melo, G.A.R. & Costa, M.A. (2009). A new cluster-brood building species of Plebeia (Hymenoptera, Apidae) from eastern Brazil. Revista Brasileira de Entomologia, 53: 77-81.

Melo, G.A.R., Buschini, M.L.T. & Campos, L.A.O. (2001). Ovarian activation in Melipona quadrifasciata queens triggered by mating plug stimulation (Hymenoptera, Apidae). Apidologie, 32: 355-361.

Menezes, C., Vollet-Neto, A. & Fonseca, V.L.I. (2013). An advance in the in vitro rearing of stingless bee queens. Apidologie, 44: 491-500.

Michener, C.D. (2007). The bees of the world. Johns Hopkins University Press.

Moure, J.S. (2004). Duas espécies novas de Plebeia Schwarz do Brasil (Hymenoptera, Apidae, Meliponinae). Revista Brasileira de Entomologia, 48: 199-202.

Niño, E.L., Malka, O., Hefetz, A., Tarpy, D.R. & Grozinger, C.M. (2013). Chemical profiles of two pheromone glands are differentially regulated by distinct mating factors in honey bee queens (Apis mellifera L.). PLoS ONE, 8: e78637.

Patrício, K. & Cruz-Landim, C. (2002). Mating influence in the ovary differentiation in adult queens of Apis mellifera L. (Hymenoptera, Apidae). Brazilian Journal of Biology, 62: 641-649.

Ronnau, M., Azevedo, D.O., Fialho, M.C.Q., Gonçlaves, W.G., Zanuncio, J.C. & Serrão, J.E. (2016). Changes in follicular cells architecture during vitellogenin transport in the ovary of social Hymenoptera. Protoplasma, 253: 815-820.

Rossa, L.S., Wolupeck, H.L., Guimarães, T.M., Weber, S.H. & Macedo, R.E.F. (2025). Propolis and geopropolis from stingless bees as sources of natural antioxidant compounds: a systematic review and meta-analysis. Journal of Apicultural Research, 1-13.

Roy, S., Saha, T.T., Zou, Z. & Raikhel, A.S. (2018). Regulatory pathways controlling female insect reproduction. Annual Review of Entomology, 63: 489-511.

Santos, C.F., Santos, P.D.S. & Blochtein, B. (2016). In vitro rearing of stingless bee queens and their acceptance rate into colonies. Apidologie, 47: 539-547.

Santos, C.F., Raguse-Quadros, M., Ramos, J.D., Silva, N.L.G., Carvalho, F.G., Barros, C.A. & Blochtein, B. (2021). Diversidade de abelhas sem ferrão e seu uso como recurso natural no Brasil: permissões e restrições legais consorciadas a políticas públicas. Revista Brasileira de Meio Ambiente, 9: 2-22.

Santos, T.C.A. & Cruz-Landim, C. (2002). Determinação das castas em Scaptotrigona postica (Latreille) (Hymenoptera, Apidae, Meliponini): diferenciação do ovário. Revista Brasileira de Zoologia, 19: 703-714.

Slaa, E.J., Chaves, L.A.S., Malagodi-Braga, K.S. & Hofstede, F.E. (2006). Stingless bees in applied pollination: practice and perspectives. Apidologie, 37: 293-315.

Slessor, K.N., Kaminski, L.A., King, G.G.S. & Winston, M.L. (1990). Semiochemicals of the honeybee queen mandibular glands. Journal of Chemical Ecology, 16: 851-860.

Souza, E.A., Neves, C.A., Campos, L.A.O., Zanuncio, J.C. & Serrão, J.E. (2007). Effect of mating delay on the ovary of Melipona quadrifasciata anthidioides (Hymenoptera: Apidae) queens. Micron, 38: 471-477.

Stefanini, M., Martino, C. & Zamboni, L. (1967). Fixation of ejaculated spermatozoa for electron microscopy. Nature, 216: 173-174.

Tanaka, E.D. & Hartfelder, K. (2004). The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. Arthropod Structure and Development, 33: 431-442.

Toledo-Hernández, E., Peña-Chora, G., Hernández-Velázquez, V.M., Lormendez, C.C., Toribio-Jiménez, J., Romero-Ramírez, Y. & León-Rodríguez, R. (2022). The stingless bees (Hymenoptera: Apidae: Meliponini): a review of the current threats to their survival. Apidologie, 53: 8.

Van Eeckhoven, J. & Duncan, E.J. (2020). Mating status and the evolution of eusociality: oogenesis is independent of mating status in the solitary bee Osmia bicornis. Journal of Insect Physiology, 121: 104003.

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Published

2025-09-12

How to Cite

Raimundo, A. P. P., Silva, N. M., Pereira, J. A., Souza, A. M. da C., Farias, J. A. P., Zanuncio, J. C., & Serrão, J. E. (2025). Ovary Activation in Virgin Queens of Plebeia lucii Moure (Hymenoptera: Meliponini). Sociobiology, 72(3), e11653. https://doi.org/10.13102/sociobiology.v72i3.11653

Issue

Vol. 72 No. 3 (2025)

Section

Research Article - Bees

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Copyright (c) 2025 Ana Paula Pereira Raimundo, Natan Martins Silva, Jaqueline Amorim Pereira, Amanda Martins da Cruz Souza, Jullie Anne Pereira Farias, José Cola Zanuncio, José Eduardo Serrão

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