, Volume 44, Issue 4, pp 367–381 | Cite as

Comparative morphology of the head glands in species of Protepeolini and Emphorini (Hymenoptera: Apidae)

  • Gerónimo L. Galvani
  • Beatriz P. SettembriniEmail author
Original article


The tribe Protepeolini is formed by parasitic bees with Leiopodus being the only genus of the tribe. Protepeolini bees parasitize the nests of members of the tribe Emphorini. Secretions of the head glands are important to the biology of bees as they may act as chemical signals in parasitism strategies. In this paper, we describe the morphology and histoarchitecture of head glands in three Protepeolini species and compare them with those of their Emphorini hosts. Mandibular and hypopharingeal glands were identified , but no head salivary glands were observed. Only parasitic species displayed sexual dimorphism in the morphology of mandibular glands, with males showing well-developed secretory portions and a characteristic organization of the secretory tissue which was previously unknown in bees. The possible role of mandibular head glands is discussed in relationship to behavioral parameters of Leiopodus.


Protepeolini Emphorini head glands immunocytochemistry 



The authors thank Dr. Arturo H. Roig-Alsina for helpful comments on the MS. Thanks are also due to Fabian Tricarico (SEM-MACN) and Patricia Bustingorry for technical assistance.


  1. Cane, J.H. (1986) Predator deterrence by mandibular gland secretions of bees (Hymenoptera: Apoidea). J. Chem. Ecol. 12, 1295–1309CrossRefGoogle Scholar
  2. Cane, J.H., Tengö, J.O. (1981) Pheromonal cues direct mate-seeking behaviors of male Colletes cunicularius (Hymenoptera: Colletidae). J. Chem. Ecol. 7, 427–436CrossRefGoogle Scholar
  3. Cane, J.H., Gerdin, S., Wife, G. (1983) Mandibular gland secretions of solitary bees (Hymenoptera: Apoidea): potential for nest cell disinfection. J. Kansas Entomol. Soc. 56, 199–204Google Scholar
  4. Cruz Landim, C. (1967) Estudo comparativo de algumas glándulas das abelhas (Hymenoptera, Apoidea) e respectivas implicações evolutivas. Arq. Zool. Sao Paulo 15, 177–290Google Scholar
  5. Cruz Landim, C. (2008) Glãndulas mandibulares p315-324. In: Abelhas-Morfologia e Função de Sistemas. UNESPGoogle Scholar
  6. Cruz Landim, C., Gracioli-Vitti, L.F., Abdalla, F.C. (2011) Ultrastuctural studies of the mandibular gland of Melipona quadrifasciata Lepeletier, 1836 (Apidae, Meliponini): a comparison between workers and queens. J. Apic. Res. 50, 306–315CrossRefGoogle Scholar
  7. Cruz Landim, C., Ferreira Caliman, M.J., Gracioli-Vitti, L.F., Zucchi, R. (2012) Correlation between mandibular gland secretion and cuticular hydrocarbons in the stingless bee Melipona quadrifasciata. Genet. Mol. Res. 11, 966–977PubMedCrossRefGoogle Scholar
  8. Deseyn, J., Billen, J. (2005) Age-dependent morphology and ultrastructure of the hypopharyngeal gland of Apis mellifera workers (Hymenoptera, Apidae). Apidologie 36, 49–57CrossRefGoogle Scholar
  9. do Amaral, J.B., Machado-Santelli, G.M. (2008) Salivary system in leaf-cutting ants (Atta sexdens rubropilosa Forel, 1908) castes: a confocal study. Micron 39, 535–540CrossRefGoogle Scholar
  10. Duffield, R.M., Simon-Jordan, C., Riddick, E.W., Wheeler, J.W. (1990) Exocrine secretions of bees X. 3,7-Dimethyldeca-2,6-dien-1,10-diol: a sex-specific compound from Nomada annulata (Hymenoptera: Anthophoridae). J. Chem. Ecol. 16, 1069–1076CrossRefGoogle Scholar
  11. Fortunato, A., Turillazzi, S., Delfino, G. (2000) Ectal mandibular gland in Polistes dominulus (Christ) (Hymenoptera, Vespidae): ultrastructural modifications over the secretory cycle. J. Morphol. 244, 45–55PubMedCrossRefGoogle Scholar
  12. Goettler, W., Strohm, E. (2008) Mandibular glands of European beewolves, Philanthus triangulum (Hymenoptera, Crabronidae). Arthropod Struct. Dev. 37, 363–371PubMedCrossRefGoogle Scholar
  13. Gracioli, L.F., Silva de Moraes, R.L.M., Cruz-Landim, C. (2004) Ultrastructural aspects of the mandibular gland of Melipona bicolor Lepeletier, 1836 (Hymenoptera: Apidae, Meliponini) in the castes. Micron 35, 331–336PubMedCrossRefGoogle Scholar
  14. Gracioli-Vitti, L., Abdalla, F., Cruz-Landim, C. (2004) Caracterização das glândulas mandibulares nas diferentes classes de adultos de Scaptotrigona postica Latreille (Hymenoptera: Apidae). Neotrop. Entomol. 33, 703–708CrossRefGoogle Scholar
  15. Grasso, D.A., Romani, R., Castracani, C., Visicchio, R., Mori, A., Isidoro, N., Le Moli, F. (2004) Mandible associated glands in queens of the slave-making ant Polyergus rufescens (Hymenoptera, Formicidae). Insect. Soc. 51, 74–80CrossRefGoogle Scholar
  16. Hefetz, A., Eickwort, G.C., Blum, M.S., Cane, J., Bohart, G.E. (1982) A comparative study of the exocrine products of cleptoparasitic bees (Holcopasites) and their hosts (Calliopsis) (Hymenoptera: Anthophoridae, Andrenidae). J. Chem. Ecol. 8, 1389–1397CrossRefGoogle Scholar
  17. Heselhaus, F. (1922) Die Hautdrüsen der Apiden und verwandter formen. Zool. Jahrb. Jena Abt. f. Anat. 49, 369–464Google Scholar
  18. Jarau, S., Hrncir, M., Zucchi, R., Barth, F.G. (2004) A stingless bee uses labial gland secretions for scent trail communication (Trigona recursa Smith 1863). J. Comp. Physiol. A 190, 233–239CrossRefGoogle Scholar
  19. Kroiss, J., Lechner, K., Strohm, E. (2010) Male territoriality and mating system in the European beewolf Philanthus triangulum F. (Hymenoptera: Crabronidae): evidence for a “hotspot” lek polygyny. J. Ethol. 28, 295–304CrossRefGoogle Scholar
  20. Lensky, Y.P., Cassier, C., Notkin, M., Delorme-Joulie, C., Levlnsohn, M. (1985) Pheromonal activity and fine structure of the mandibular glands of honeybee drones (Apis mellifera L.). J. Insect Physiol. 31, 265–276CrossRefGoogle Scholar
  21. Nedel, J.D. (1960) Morphologie und physiologie der mandibeldrüse. Z. Morphol. Ökol. Tiere 49, 139–183CrossRefGoogle Scholar
  22. Niculita, H., Billen, J., Keller, L. (2008) Comparative morphology of cephalic exocrine glands among castes of the black ant Lasius niger. Arthropod Struct. Dev. 36, 135–141CrossRefGoogle Scholar
  23. Noirot, C., Quennedey, A. (1974) Fine structure of insect epidermal glands. Annu. Rev. Entomol. 19, 61–80CrossRefGoogle Scholar
  24. Reichle, C., Aguilar, I., Ayasse, M., Jarau, S. (2011) Stingless bees (Scaptotrigona pectoralis) learn foreign trail pheromones and use them to find food. J. Comp. Physiol. A. Neuroethol. Sens. Neural B. 147, 243–249CrossRefGoogle Scholar
  25. Roig-Alsina, A., Rozen Jr., J.G. (1994) Revision of the cleptoparasitic bee tribe Protepeolini, including biologies and immature stages. Am. Mus. Novit. 3099, 1–27Google Scholar
  26. Settembrini, B.P. (1984) The compound eyes of Triatoma infestans and Rhodnius prolixus (Hemiptera: Reduviidae). J. Med. Entomol. 21, 477–479Google Scholar
  27. Settembrini, B.P., Galvani, G.L., Villar, M.J. (2008) Localization of cholecystokinin-like immunoreactivity in the central nervous system of Triatoma infestans (Insecta: Heteroptera). Tissue Cell 40, 51–60PubMedCrossRefGoogle Scholar
  28. Simpson, J. (1960) The functions of the salivary glands of Apis mellifera. J. Insect Physiol. 4, 107–121CrossRefGoogle Scholar
  29. Šobotnik, J., Kalinková, B., Cahlíková, L., Weyda, F., Ptáček, V., Valterová, I. (2008) Age-dependent changes in structure and function of the male labial glands in Bombus terrestris. J. Insect Physiol. 54, 204–214PubMedCrossRefGoogle Scholar
  30. Tengö, J., Bergstrom, G. (1977) Cleptoparasitism and odor mimetism in bees: do Nomada males imitate the odor of Andrena females? Science 196, 1117–1119PubMedCrossRefGoogle Scholar
  31. Vallet, A., Cassier, P., Lensky, Y. (1991) Ontogeny of the fine structure of the mandibular glands of the honeybee (Apis mellifera L.) workers and the pheromonal activity of 2-heptanone. J. Insect Physiol 37, 789–804CrossRefGoogle Scholar
  32. Vinson, S.B., Williams, H.J., Frankie, G.W., Wheeler, J.W., Blum, M.S., Coville, R.E. (1982) Mandibular glands of male Centris adani (Hymenoptera; Anthophoridae): their morphology, chemical constituents and function in scent marking and territorial behavior. J. Chem. Ecol. 8, 319–327CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France 2012

Authors and Affiliations

  • Gerónimo L. Galvani
    • 1
    • 2
  • Beatriz P. Settembrini
    • 1
    • 2
    Email author
  1. 1.Museo Argentino de Ciencias NaturalesCiudad de Buenos AiresArgentina
  2. 2.Facultad de Ciencias BiomédicasUniversidad AustralPilarArgentina

Personalised recommendations