Post-embryonic Development of the Seminal Vesicle in the Stingless Bee Melipona quadrifasciata Lepeletier, 1836 (Apidae: Meliponini)

Ríudo de Paiva Ferreira, Hugo de Azevedo Werneck, Juliana Malta, Aparecida das Dores Teixeira, Lucio Antonio de Oliveira Campos, José Eduardo Serrão

Abstract


The male accessory glands of stingless bees (Apidae: Meliponini) are absent and the morphology of their seminal vesicle indicate probable secretory function by this organ. This study investigated the post-embryonic development of the seminal vesicles in males of the stingless bee Melipona quadrifasciata by histology and histochemistry. White-eyed pupae, pink-eyed pupae, brown-eyed pupae, black-eyed pupae, newly emerged and sexually mature males were studied. Seminal vesicle has a wall with a single layered epithelium onto a thin basement membrane, followed by a well-developed muscle layer. The epithelium is polarized in the pupal stage with basal cell region strongly positive for glucoconjugates and carbohydrates. The seminal vesicle has an enlarged lumen from the young pupal stages with luminal content increasing gradually with glucoconjugates along the pupal development. In the newly emerged and mature males, the histochemical tests to carbohydrates were negative. In the sexually mature males, spermatozoa clusters are embedded by the glucoconjugates content of the seminal vesicle lumen. In conclusion, the seminal vesicle of M. quadrifasciata has a secretory function during the pupal stage and in newly emerged males, whereas in adult males this organ stores the spermatozoa.

.

Keywords


Hymenoptera, reproductive system, male accessory glands

Full Text:

PDF

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 Scaptotrigona xanthotricha Moure males (Hymenoptera, Apidae, Meliponini). Brazilian Journal of Morphological Sciences, 22: 193–201.

Baer, B. & Boomsma, J. J. (2004). Male reproductive investment and queen mating frequency in fungus growing ants. Behavioral Ecology, 15: 426-432. doi: 10.1093/beheco/arh025

Baer, B., Maile, R., Schmid-Hempel, P., Morgan, E. D. & Jones, G. R. (2000). Chemistry of a mating plug in bumblebees. Journal of Chemical Ecology, 26: 1869-1875. doi: 10.1023/A:100559670

Bancroft, J. D. & Gamble, M. (2008). Theory and prctice of histological techniques. London: Churchill Livingstone, , 725 p.

Blum, M. S., Bumgarner, J. E. & Tauber III, S. (1967). Composition and possible significance of fatty acids in lipids classes of honeybee serum. Journal of Insect Physiology, 13: 1301-1308.

Blum, M. S, Glowska, Z. & Tauber III S. (1962). Chemistry of the drone honeybee reproductive system. II. Carbohydrates in the reproductive organs and semen. Annals of the Entomological Society of America, 55: 135-139.

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

Brito, P., 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

Chapman, R. F. (2013). The Insects: Structure and Function. Cambridge University Press, 959 p.

Chen, P. S. (1984). The functional morphology and biochemistry of insect male accessory glands and their secretions. Annual Review of Entomology, 29: 233-255.

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

Cruz-Landim, C. & Cruz-Höfling, M. A. (1969). Electron microscope observations on honeybee seminal vesicles (Apis mellifera adansonii, Hymenoptera, Apidae). Papéis Avulsos de Zoologia, 22: 145-151.

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

Cruz-Landim, C., 2009. Abelhas: Morfologia e Função. São Paulo: Editora Unesp. 407 p.

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), Anatomia Histologia Embryologia, 32: 276–281. doi: 10.1046/j.1439-0264.2003.00484

den Boer S.P.A., Boomsma, J. & Baer, B. (2009). Honeybee 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

den Boer S.P.A., Sturup, M., Boomsma, J. & Baer, B. (2015). The ejaculatory biology of leafcutter ants. Journal of Insect Physiology, 74: 56-62. doi: 10.1016/j.jinsphys.2015.02.006

Fausto, A. M, Gambellini, A. R., Taddei, A. R., Maroli, M. & Mazzini, M. (2000). Ultrastructure of the vesicle of Phlebotomus perniciosus Newstead (Diptera, Psychodidae). Tissue and Cell, 32: 228-237. doi: 10.1054/tice.2000.0110

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

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

Gillot, C. (1988). Arthropoda-Insecta. in Adiyodi, K. G. & Adiyodi, R. G. (Eds), Reproductive Biology of Invertebrates (pp. 319-371). New York: Wiley press.

Gorshkov, V., Blenau, W., Koeniger, G., Römpp, A., Vilcinskas, A. & Spengler, B. (2015). Protein and Peptide Composition of Male Accessory Glands of Apis mellifera Drones Investigated by Mass Spectrometry. PLoS ONE 10: e0125068.

doi:10.1371/journal.pone.0125068.

Junqueira, L. C. U. & Junqueira, M. M. S. (1983). Técnicas básicas de citologia e histologia. São Paulo: Editora Santos, 123 p.

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

Lopes, D. M., Tavares, M. G. & Campos, L. A. O. (2003). Sperm utilization by Melipona quadrifasciata Lepeletier (Hymenoptera, Apidae) queens subjected to multiple mating. Insectes Sociaux, 50: 387-389. doi:10.1007/s00040-003-0694-0

Moreira J., Zama U. & Lino-Neto J. (2004). Release, behavior and phylogenetic significance of spermatozoa in bundles in the seminal vesicle during sexual maturation in Aculeata (Hymenoptera). Brazilian Journal of Morphological Sciences, 21: 185-189.

Stefanini, M. C. & De Martino, Zamboni, L. (1967). Fixation of ejaculated spermatozoa for electron microscopy. Nature, 216: 173–174. doi: 10.1038/216173a0

Snodgrass, R.E. (1935). Principles of insect morphology. New York and London: McGraw-Hill Book Company, Inc, 667 p.

Sawarkar, A. B. & Tembhare, D. B. (2014). Development and secretory nature of seminal vesicle during sexual maturation in Indian honeybee, Apis cerana indica F. (Hymenoptera: Apidae). Journal of Entomology and Zoology Studies, 2: 105-109.

Tozetto, S. O., Bitondi, M. M. G., Dallacqua, R. P. & Simões, Z. L. P. (2007). Protein profiles of testes, seminal vesicles and accessory glands of honeybee pupae and their relation to the ecdysteroid titer. Apidologie, 38: 1-11. doi: 10.1051/apido:2006045

Viana, M. V. C., de Carvalho, C. A. L., Sousa, H. A. C., Francisco, A. K. & Waldschmidt, A. M. (2015). Mating frequency and maternity of males in Melipona mondury (Hymenoptera: Apidae). Insectes Sociaux, 62: 491-495. doi: 10.1007/s00040-015-0428-0




DOI: http://dx.doi.org/10.13102/sociobiology.v66i2.3431

Refbacks

  • There are currently no refbacks.


JCR Impact Factor 2018: 0.604