Structural Changes in the Male Reproductive Tract of the Stingless Bee Scaptotrigona xanthotricha Moure 1950 (Meliponini, Apidae) During Sexual Maturation

Authors

DOI:

https://doi.org/10.13102/sociobiology.v67i4.5513

Keywords:

Hymenoptera, metamorphosis, reproduction, seminal vesicle, vasa deferentia

Abstract

Stingless bees are social insects widely distributed in the Neotropical region but the loss of habitats and the increased use of pesticides in agriculture have threatened the bee populations. Thus, the knowledge of the biology of these insects, including reproductive biology is important for their conservation and management. This study describes the morphological changes in the male reproductive tract during the sexual maturation in the stingless bee Scaptotrigona xanthotricha (Moure 1950). The reproductive tract was investigated under light microscopy from young pupae to 22 days old adults. The male reproductive organs in S. xanthotricha are a pair of testes, each with four follicles, pair of vasa deferentia with enlarged region forming the seminal vesicle that open in an ejaculatory duct. In the male reproductive system of these bees there is no structure that can be recognized as accessory glands as seen in insects in general. From brown-eyed pupae to newly-emerged adults, the epithelia of the seminal vesicles and post-vesicular vasa deferentia have prismatic cells that release secretion to the organs lumen. In 5-days old adults the testes undergo degeneration, the seminal vesicles filled with secretion and spermatozoa, and the epithelium has cubic cells rich in inclusions in the basal region suggesting that this is the age in which males reach the sexual maturation. Structural modifications in the reproductive tract during sexual maturation are discussed concerning the reproductive biology of Meliponini.

Downloads

Download data is not yet available.

Author Biographies

Vinícius Albano Araujo, Universidade Federal do Rio de Janeiro

Instituto de Biodiversidade e Sustentabilidade (NUPEM) -  Professor

José Eduardo Serrão, Universidade Federal de Viçosa Professor

Departamento de Biologia Celular - Professor

Yasmine Antonini, Universidade Federal de Ouro Preto

Departamento de Biodiversidade Evolução e Meio Ambiente, Instituto de Ciências Exatas e Biológicas - Professor

Lucimar Gomes Dias, Universidad de Caldas

Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas y Naturales, Grupo de investigación Bionat - Professor

José Lino Neto, Universidade Federal de Viçosa

Departamento de Biologia Geral - Professor

References

Araújo, V.A., Zama, U., Neves, C.A., Dolder, H., Lino-Neto, J. (2005). Ultrastructural, histological and histochemical characteristics of the epithelial wall of the seminal vesicle of mature males of Scaptotrigona xanthotricha Moure (Hymenoptera, Apidae, Meliponini). Journal of Morphological Science, 22: 129-136.

Boomsma, J.J., Baer, B., Heinze, J. (2005). The evolution of male traits in social insects. Annual Review of Entomoloy, 50: 395-420. doi: 10.1146/annurev.ento.50.071803.130416. DOI: https://doi.org/10.1146/annurev.ento.50.071803.130416

Brito, B., Zama, U., Dolder, H., Lino-Neto, J. (2010). New characteristics of the male reproductive system in the Meliponini bee, Friesella schrottkyi (Hymenoptera: Apidae): histological and physiological development during sexual maturation. Apidologie, 41: 203-215. doi: 10.1051/apido/2009071. DOI: https://doi.org/10.1051/apido/2009071

Brosi, B.J., Daily, G.C., Chamberlain, C.P., Mills, M. (2009). Detecting changes in habitat-scale bee foraging in a tropical fragmented landscape using stable isotopes. Forest Ecology Management, 258: 1846-1855. doi: 10.1016/j.foreco.2009.02.027. DOI: https://doi.org/10.1016/j.foreco.2009.02.027

Camargo, C.A. (1984). Spematozoa numbers and migration to the seminal vesicles in haploid and diploid males of Melipona quadrifasciata Lep. Journal of Apicultural Research, 23: 15-17. doi: 10.1080/00218839.1984.11100602. DOI: https://doi.org/10.1080/00218839.1984.11100602

Camargo, J.M.F. (2013). Historical biogeography of the Meliponini (Hymenoptera, Apidae, Apinae) of the Neotropical Region. In P. Vit., S.R.M. Pedro & D.W. Roubik (Eds.), PotHoney: A legacy of stingless bees (pp. 19-34). New York: Springer. DOI: https://doi.org/10.1007/978-1-4614-4960-7_2

Carneiro, L.S.C., Teixeira, S.A.M.V., Gonçalves, W.G., Fernandes, K.M., Zanuncio, J.C., SERRÃO, J.E. (2018). Histochemistry, immunohistochemistry and cytochemistry of the anterior midgut region of the stingless bee Melipona quadrifasciata and honey bee Apis mellifera (Hymenoptera: Apidae). Micron, 113: 41-47. doi: 10.1016/j.micron.2018.06.017. DOI: https://doi.org/10.1016/j.micron.2018.06.017

Chen, P.S. (1984). The functional morphological and biochemistry of insect male acessory glands and their secretions. Annual Review of Entomology, 29: 233-255. doi: 10.1146/annurev.en.29.010184.001313. DOI: https://doi.org/10.1146/annurev.en.29.010184.001313

Colonello, N.A., Hartfelder, K. (2005). She's my girl - male accessory gland products and their function in the reproductive biology of social bees. Apidologie, 36: 231-244. doi: 10.1051/apido:2005012. DOI: https://doi.org/10.1051/apido:2005012

Cortopassi-Laurino, M., Imperatriz-Fonseca, V.L., Roubik, D.W., Dollin, A., Heard, T., Aguilar, I. (2006). Global meliponiculture: challenges and opportunities. Apidologie, 37: 275-292. doi: 10.1051/apido:2006027. DOI: https://doi.org/10.1051/apido:2006027

Cortopassi-Laurino, M., Nogueira-Neto, P. (2016). Abelhas sem ferrão do Brasil. São Paulo: Editora da Universidade de São Paulo, 123 p.

Cruz-Landim, C. (2001). Organization of the cysts in bee (Hymenoptera: Apidae) testes: number of spermatozoa per cyst. Iheringia, 91: 183-189. doi: 10.1590/S0073-47212001000200025. DOI: https://doi.org/10.1590/S0073-47212001000200025

Cruz-Landim, C., Dallacqua, R.P. (2002). Testicular reabsorption in adult males of Melipona bicolor bicolor Lepeletier (Hymenoptera, Apidae, Meliponini). Cytologia, 67:145-151. doi: 10.1508/cytologia.67.145. DOI: https://doi.org/10.1508/cytologia.67.145

Custodio, T., Comtois, P., Araujo, A.C. (2017). Reproductive biology and pollination ecology of Triplaris gardneriana (Polygonaceae): a case of ambophily in the Brazilian Chaco. Plant Biology, 19: 504-514. doi: 10.1111/plb.12554. DOI: https://doi.org/10.1111/plb.12554

Dallacqua, R.P., Cruz-Landim, C. (2003). Ultrastructure of the ducts of the reproductive tract of males of Melipona bicolor bicolor Lepeletier (Hymenoptera, Apinae, Meliponini). Anatomy, Histolology and Embryology, 32: 276-281. doi: 10.1046/j.1439-0264.2003.00484.x. DOI: https://doi.org/10.1046/j.1439-0264.2003.00484.x

Del Sarto, M.C.L., 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/s13592-014-0281-6ff. DOI: https://doi.org/10.1007/s13592-014-0281-6

Den Boer, S.P.A., Boomsma, J.B.B. (2009). Honey bee males and queens use glandular secretions to enhance sperm viability before and after storage. Journal of Insect Physiology, 55: 538-543. doi: 10.1016/j.jinsphys.2009.01.012. DOI: https://doi.org/10.1016/j.jinsphys.2009.01.012

Dos Santos, S.A.B., Roselino, A.C., Bego, L.R. (2008). Pollination of Cucumber, Cucumis sativus L. (Cucurbitales: Cucurbitaceae), by the stingless bees Scaptotrigona aff. depilis Moure and Nannotrigona testaceicornis Lepeletier (Hymenoptera: Meliponini) in greenhouses. Neotropical Entomology, 37: 506-512. doi: 10.1590/S1519-566X2008000500002. DOI: https://doi.org/10.1590/S1519-566X2008000500002

Dumser, J.B. (1980). The regulation of spermatogenesis in insects. Annual Review of Entomology, 25: 341-369. doi: 10.1146/annurev.en.25.010180.002013. DOI: https://doi.org/10.1146/annurev.en.25.010180.002013

Ferreira, A., Abdalla, F.C., Kerr, W.E., Cruz-Landim, C. (2004). Comparative anatomy of the male reproductive internal organs of 51 species of bees. Neotropical Entomology, 33: 569-576. doi: 10.1590/S1519-566X2004000500005. DOI: https://doi.org/10.1590/S1519-566X2004000500005

Ferreira, R.D., Werneck, H.A., Malta, J., Teixeira, A.D., Campos, L.A.O., Serrão, J.E. (2019). Post-embryonic development of the seminal vesicle in the stingless bee Melipona quadrifasciata Lepeletier, 1836 (Apidae: Meliponini). Sociobiology, 66: 287-292. doi: 10.13102/sociobiology.v66i2.3431 DOI: https://doi.org/10.13102/sociobiology.v66i2.3431

Freitas, B.M., Imperatriz-Fonseca, V.L., Medina, L.M., Kleinert, A.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: 332-346. doi: 10.1051/apido/2009012. DOI: https://doi.org/10.1051/apido/2009012

Fuessl, M., Reinders, J., Oefner, P.J., Heinze, J., Schrempf, A. (2014). Selenophosphate synthase in the male accessory glands of an insect without selenoproteins. Journal of Insect Physiology, 71: 46-51. doi: 10.1016/j.jinsphys.2014.09.012. DOI: https://doi.org/10.1016/j.jinsphys.2014.09.012

Gillot, C. (2003). Male accessory gland secretions: Modulators of female reproductive physiology and behavior. Annual Review of Entomology, 48: 163-184. doi: 10.1146/annurev.ento.48.091801.112657. DOI: https://doi.org/10.1146/annurev.ento.48.091801.112657

Goulson, D., Nicholls, E., Botias, C., Rotheray, E.L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347: 1255957. doi: 10.1126/science.1255957. DOI: https://doi.org/10.1126/science.1255957

Guimarães-Cestaro, L., Martins, M.F., Martínez, L.C., Alves, M.F., Guidugli-Lazzarini, K.R., Nocelli, R.C.F., Malaspina, O., Serrão, J.E., Teixeira, E.W. (2020) Occurrence of virus, microsporidia, and pesticide residues in three species of stingless bees (Apidae: Meliponini) in the field. The Science of Nature, 107:16. doi: 10.1007/s00114-020-1670-5. DOI: https://doi.org/10.1007/s00114-020-1670-5

Happ, G.M. (1992). Maturation of the male reproductive system and its endocrine regulation. Annual Review of Entomology, 37: 303-320. doi: 10.1146/annurev.en.37.010192.001511. DOI: https://doi.org/10.1146/annurev.en.37.010192.001511

Heinze, J., Holldoler, B. (1993). Fighting for a harem of queens: physiology of reproduction in Cardiocondyla male ants. Proceedings of the National Academy of Sciences, 90: 8412-8414. doi: 10.1073/pnas.90.18.8412. DOI: https://doi.org/10.1073/pnas.90.18.8412

Junqueira, L.C.U., Junqueira, M.M.S. (1983). Técnicas Básicas de Citologia e Histologia. São Paulo: Livraria Editora Santos,123p.

Kerr, W.E. (1948). Estudos sobre o gênero Melipona. Anais da Escola Superior de Agricultura Luiz de Queiroz, 5:181-276. doi: 10.1590/S0071-12761948000100005. DOI: https://doi.org/10.1590/S0071-12761948000100005

Kerr WE, Carvalho GA, Silva AC, Assis MGP (2001) Aspectos pouco mencionados da biodiversidade amazônica. Parcerias Estratégicas, 6: 20-41.

Lima, M.A.P., Lino-Neto, J., Campos, L.A.O. (2006). Sexual maturation in Melipona mondury males (Apidae: Meliponini). Journal of Morphological Sciencie, 23: 369-375.

Lino-Neto, J., Araújo, V.A., Dolder, M.A. (2008). Inviability of the spermatids with little cytoplasm in bees (Hymenoptera, Apidae). Sociobiology, 51: 163-172.

Michener, C.D. (2007). The bees of the world, 2nd ed. Baltimore: Johns Hopkins University Press, 992p. DOI: https://doi.org/10.56021/9780801885730

Michener, C.D. (2013). The Meliponini. Vit., S.R.M. Pedro & D.W. Roubik (Eds.), PotHoney: A legacy of stingless bees (pp. 3-17). New York: Springer. DOI: https://doi.org/10.1007/978-1-4614-4960-7_1

Nascimento, W.M., Gomes, E.M.L., Batista, E.A., Freitas, R.A. (2012). Influence of pollinators on seed production and quality of carrot and sweet pepper in a greenhouse. Horticultura Brasileira, 30: 494-498. doi: 10.1590/S0102-05362012000300023. DOI: https://doi.org/10.1590/S0102-05362012000300023

Nielsen, A., Reitan, T., Rinvoll, A.W., Brysting, A.K. (2017). Effects of competition and climate on a crop pollinator community. Agriculture Ecosystems & Environment, 246: 253-260. doi: org/10.1016/j.agee.2017.06.006. DOI: https://doi.org/10.1016/j.agee.2017.06.006

Nunes-Silva, P., Hrncir, M., Silva, C.I., Roldão, Y.S., Imperatriz-Fonseca, V.I. (2013). Stingless bees, Melipona fasciculata, as efficient pollinators of egg plant (Solanum melongena) in greenhouses. Apidologie, 44:537-546. doi: 10.1007/s13592-013-0204-yf. DOI: https://doi.org/10.1007/s13592-013-0204-y

Pedro, S.E.M. (2014). The Stingless Bee fauna in Brazil (Hymenoptera: Apidae). Sociobiology, 61: 348-354. doi: 10.13102/sociobiology.v61i4.348-354. DOI: https://doi.org/10.13102/sociobiology.v61i4.348-354

Potts, G.V., Imperatriz-Fonseca, H.T., Ngo, M.A., Aizen, J.C., Biesmeijer, T.D., Breeze, L.V., Dicks, L.A., Garibaldi, R.H., Elle, J.S., Vanberg, A.J. (2016). Safeguarding pollinators and their values to human well-being. Nature, 540: 220-229. doi: 10.1038/nature20588. DOI: https://doi.org/10.1038/nature20588

Roselino, A.C., Santos, S.B., Hrncir, M., Bego, L.R. (2009). Differences between the quality of strawberries (Fragaria x Ananassa) pollinated by the stingless bees Scaptotrigona aff. depilis and Nannotrigona testaceicornis. Genetic Molecular and Research, 8:539-545. doi: 10.4238/vol8-2keer005. DOI: https://doi.org/10.4238/vol8-2kerr005

Schmitz, G., Muller, G. (1991). Structure and function of lamellar bodies, lipid-protein complexes involved in storage and secretion of cellular lipids. Journal Lipid Research 32:1539-1570. DOI: https://doi.org/10.1016/S0022-2275(20)41642-6

Slaa, E.J., Sanchez Chaves, L.A., Malagodi-Braga, K.S., Hofstede, F.E. (2006). Stingless bees in applied pollination: practice and perspectives. Apidologie, 37: 293-315. doi: 10.1051/apido:2006022. DOI: https://doi.org/10.1051/apido:2006022

Snodgrass, R.E. (1978). Anatomy of the honeybees. 3º ed. Londres: Cornel University Press.

Tasei, J., Asano, S., Ohtsubo, T., Kamomae, M., Gotoh, T. (1998). Relationship between aging, mating and sperm production in captive Bombus terrestris. Journal of Apicultural Research, 37: 107-113. doi: 10.1080/00218839.1998.11100962. DOI: https://doi.org/10.1080/00218839.1998.11100962

Wheleer, D.E., Krutzsch, P.H. (1992). Internal reproductive system in adult males of the genus Camponotus (Hymenoptera: Formicidae: Formicinae). Journal of Morphology, 211: 307-317. doi: 10.1002/jmor.1052110308. DOI: https://doi.org/10.1002/jmor.1052110308

Witter, S., Nunes-Silva, P., Lisboa, B.B., Tirelli, F.P., Sattler, A., Hilgert-Moreira, S.B., Blochtein, B. (2015). Stingless bees as alternative pollinators of canola. Journal of Economic Entomology, 108: 880-886. doi: 10.1093/jee/tov096. DOI: https://doi.org/10.1093/jee/tov096

Downloads

Published

2020-12-28

How to Cite

Araujo, V. A., Serrão, J. E., Antonini, Y., Dias, L. G., & Neto, J. L. (2020). Structural Changes in the Male Reproductive Tract of the Stingless Bee Scaptotrigona xanthotricha Moure 1950 (Meliponini, Apidae) During Sexual Maturation. Sociobiology, 67(4), 526–534. https://doi.org/10.13102/sociobiology.v67i4.5513

Issue

Vol. 67 No. 4 (2020)

Section

Research Article - Bees

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:

 

    1. 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.

 

    1. 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.

 

  1. 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).

Most read articles by the same author(s)