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Ontogeny and morphology of the bulbus, part of the male reproductive organ in Apis mellifera carnica (Hymenoptera, Apidae)

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Abstract

The bulbus is a part of the unique functional penis (endophallus) in the genus Apis and was studied in Apis mellifera drones. The bulbus consists of a thin cuticular membrane, covered by four different epithelia (dorsal epithelium, anterior epithelium, ventral epithelium I and ventral epithelium II). One day before eclosion, pupae have no sclerotised plates in the bulbus lumen. In emerging drones, however, the lumen contains tanned plate-like structures, the chitin plates, subjacent are small droplets. The chitin plates are connected to each other by a transparent matrix. They consist of globular sclerotized structures which are connected by a network of fibrils. In young adult drones, the dorsal and lateral epithelia consist of highly columnar gland cells which decrease in thickness from the age of 6–12 days from 140 to 20 μm. The ultrastructural analysis combined with histochemistry shows that the gland cells secrete proteinaceous droplets towards the lumen which pass through the cuticle and the pores of the chitin plates and accumulate in the matrix. In sexually mature drones, all secretions have merged to a rigid connective substance, which extends laterally as a thin tapering membrane. The ventral epithelia I and II have no secretory function. The ventral epithelium II has a mucus-like content and several invaginations towards the lumen of the bulbus which enables widening of the bulbus orifice to discharge the bulbus secretions filled with viscous mucus via the cervix into the queen during the mating process.

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References

  • Bancroft, J.D., Gamble, M. (2008) Theory and practice of histological techniques, 6th edn. Churchill Livingstone, Philadelphia

    Google Scholar 

  • Colonello, N.A., Hartfelder, K. (2003) Protein content and pattern during mucus gland maturation and its ecdysteroid control in honeybee drones. Apidologie 34, 1–10

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gary N.E. (1969) Mating behaviour of the honeybee. Proc. XXII Int. Beekeep. Congr., 413–414

  • Gillott, C. (1988) Arthropoda–Insecta. In: Adiyodi, K.G., Adiyodi, R.G. (eds.) Reproductive biology of invertebrates, vol. 3, pp. 319–471. Wiley, Chichester

    Google Scholar 

  • Gillott, C. (1996) Male insect accessory glands: functions and control of secretory activity. Invertebr. Repr. Dev. 30, 199–205

    Article  CAS  Google Scholar 

  • Gillott, C. (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu. Rev. Entomol. 48, 163–184

    Article  PubMed  CAS  Google Scholar 

  • Koeniger, G. (1984) Funktionsmorphologische Befunde bei der Kopulation der Honigbiene (Apis mellifera L.). Apidologie 15, 189–204

    Article  Google Scholar 

  • Koeniger, G. (1986) Mating sign and multiple mating in the honeybee. Bee World 67, 141–150

    Google Scholar 

  • Koeniger, G. (1990) The role of the mating sign in honeybees Apis mellifera L.: does it hinder or promote multiple mating? Anim. Behav. 39, 444–449

    Article  Google Scholar 

  • Koeniger, G., Hänel, H. (1996) The bulbus gland of drones (Apis mellifera L.). Pszcz. Zesz. Nauk. 2, 45–54

    Google Scholar 

  • Koeniger, G., Hänel, H., Wissel, M., Herth, W. (1996) Cornual gland in the honeybee drone (Apis mellifera L.): structure and secretion. Apidologie 27, 145–156

    Article  Google Scholar 

  • Koeniger, G., Koeniger, N., Mardan, M., Otis, G., Wongsiri, S. (1991) Comparative anatomy of male genital organs in the genus Apis. Apidologie 22, 539–552

    Article  Google Scholar 

  • Leopold, R.A. (1976) The role of male accessory glands in insect reproduction. Annu. Rev. Entomol. 21, 199–221

    Article  Google Scholar 

  • Moors, L., Billen, J. (2009) Age-dependent morphology and ultrastructure of the cornua glands in drones of Apis mellifera. Apidologie 40, 600–607

    Article  Google Scholar 

  • Moors, L., Spaas, O., Koeniger, G., Billen, J. (2005) Morphological and ultrastructural changes in the mucus glands of Apis mellifera drones during pupal development and sexual maturation. Apidologie 36, 245–254

    Article  Google Scholar 

  • Patinawin, S., Wongsiri, S. (1993) Male genitalia of honeybees in Asian apiculture. Proc. 1st Int. Conf. Asian Honeybees and Bee Mites, Bangkok, Thailand. Wicwas Press, Cherhire, CT, USA, pp. 110–116

  • Snodgrass, R.E. (1941) The male genitalia of Hymeno-ptera. Smithsonian Institution, Washington

    Google Scholar 

  • Snodgrass, R.E. (1956) Anatomy of the honey bee. Comstock Publ. Assoc. Cornell. Univ. Press, Ithaca

    Google Scholar 

  • Winston, M.L. (1987) The biology of the honey bee. Harvard University Press, Cambridge

    Google Scholar 

  • Wolfner, M.F. (1997) Tokens of love: functions and regulation of Drosophila melanogaster male accessory gland products. Insect Biochem. Mol. Biol. 27, 179–192

    Article  PubMed  CAS  Google Scholar 

  • Woyke, J. (1956) Anatomo-physiological changes in queen-bees returning from mating flights and the process of multiple mating. Bull. Acad. Polon. Sci. 4, 81–87

    Google Scholar 

  • Woyke, J. (1958a) The process of mating in the honeybee. Pszcz. Zesz. Nauk. 2, 1–42

    Google Scholar 

  • Woyke, J. (1958b) The histological structure of the reproductive organs of the drone. Publ. Sect. Agr. Sylv. 19, 38–50

    Google Scholar 

  • Woyke, J., Ruttner, F. (1958) An anatomical study of the mating process in the honeybee. Bee World 39, 3–18

    Google Scholar 

  • Woyke, J. (2008) Why the eversion of the endophallus of honey bee drone stops at the partly everted stage and significance of this. Apidologie 39, 627–636

    Article  Google Scholar 

  • Zander, E. (1916) Die postembryonale Entwicklung des Geschlechtsapparates der Drohne (Apis mellifica L.). Z. Angew. Ent. 3, 7–20

    Article  Google Scholar 

  • Zander, E. (1922) Der Bau der Biene. E. Ulmer, Stuttgart

    Google Scholar 

Download references

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Correspondence to Johan Billen.

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Manuscript editor: Klaus Hartfelder

Ontogénie et morphologie du bulbe, partie de l’organe reproducteur mâle chez Apis mellifera carnica (Hymenoptera, Apidae)

Morphologie / ontogénie / ultrastructure / bulbe / endophallus / abeille / mâle

Entwicklung und Morphologie des Bulbus, eines Teils des männlichen Reproduktionstrakts von Apis mellifera carnica (Hymenoptera, Apidae)

Morphologie / Entwicklung / Ultrastruktur / BUlbus / Endophallus / Honigbiene / Drohn

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Moors, L., Koeniger, G. & Billen, J. Ontogeny and morphology of the bulbus, part of the male reproductive organ in Apis mellifera carnica (Hymenoptera, Apidae). Apidologie 43, 201–211 (2012). https://doi.org/10.1007/s13592-011-0094-9

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  • DOI: https://doi.org/10.1007/s13592-011-0094-9

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