Skip to main content
Log in

Morphology of mandibular and intramandibular glands in workers and virgin queens of Melipona scutellaris

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

The interactions of insect societies are associated with chemical signals released by the exocrine glands that control some insect behaviors. Exocrine glands can be classified into different classes: class I release substances that cross the body cuticle and class III glands that have a conducting canal. This study compares the morphology of intramandibular and mandibular glands in virgin queens of different ages, as well as in nurses and forager workers of Melipona scutellaris. We have found the occurrence of two types of glands inside the mandible; glands of class I, corresponding to a well-developed epithelium, secretory only in virgin queens, and glands of class III. On the other hand, mandibular glands have been found to be well-developed in workers and queens and they also have high amounts of mitochondria and smooth endoplasmic reticulum. Together, these data show that the mandibular and intramandibular glands of M. scutellaris virgin queens have morphological features that indicate the synthesis of compounds that are lipid in nature. Furthermore, both glands have a similar developmental degree in newly emerged and 7-day-old ones.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5

Similar content being viewed by others

References

  • Abdalla, F.C., Cruz-Landim, C. (2002) Glândulas Exócrinas das Abelhas. Funpec-RPP, São Paulo. 2002

    Google Scholar 

  • Armbruster, L., Levy, M., Mathieu, M.N., Bautz, A.M. (1986) Acid phosphatase activity in the hemolymph, hemocytes, fat body and salivary glands during larval and prepupal development in Caliphora erythrocephala (Diptera, Caliphoridae). Comp. Biochem. Physiol. 84, 349–354

    Google Scholar 

  • Blomquist, G.J., Howard, R.W. (2003) Pheromone biosynthesis in social insects. In G. Blomquist and R. Vogt (eds), Insect Pheromone Biochemistry and Molecular Biology, Academic Press, Columbia.

  • Cahliková, L., Hovorka, O., Ptacek, V., Valterova, I. (2004) Exocrine gland secretions of virgin queens of five bumblebee species (Hymenoptera, Apidae, Bombini). Zeitschrif. Naturwis. C 59, 582–589

    Google Scholar 

  • Costa-Leonardo, M. (1978) Glândulas intramandibulares em abelhas sociais. Ciênc. Cult. 30, 835–838

    Google Scholar 

  • Costa-Leonardo, M. (1981) Ultra-estrutura do ciclo secretor das mandíbulas de operárias de Apis mellifera L. (Hymenoptera, Apidae). Rev. Bras. Zool. 41, 307–316

    Google Scholar 

  • Cruz-Landim, C. (1967) Estudo comparativo de algumas glândulas de abelhas (Hymenoptera, Apoidea) e respectivas implicações evolutivas. Arq. Zool. São Paulo 15, 177–290

    Article  Google Scholar 

  • Cruz-Landim, C. (1994) Polimorfismo na ocorrência das glândulas exócrinas nas abelhas (Hymenoptera, Apidae). In: Encontro Sobre Abelhas, Ribeirão Preto, Brazil 8, 118-129.

  • Cruz-Landim, C. (2009) Abelhas, Morfologia e Função de Sistemas. Editora Unesp, São Paulo

    Google Scholar 

  • Cruz-Landim, C., Gracioli-Vitti, L.F., Abdalla, F.C. (2011) Ultrastructure of the intramandibular gland of workers and queens of the stingless bee, Melipona quadrifasciata. J. Insect Sci. 11, 107

    PubMed Central  PubMed  Google Scholar 

  • Cruz-Lopez, L., Malo, E.A., Morgan, E.D., Rincon, M., Guzmán, M., Rojas, J.C. (2005) Mandibular gland secretion of Melipona beecheii, chemistry and behavior. J. Chem. Ecol. 31, 1621–1632

    Article  CAS  PubMed  Google Scholar 

  • Cruz-Lopez, L., Aguilar, S., Malo, E.A., Rincon, M., Guzman, M., Rojas, J.C. (2007) Electroantennogram and behavioral responses of workers of the stingless bee Oxytrigona mediorufa to mandibular gland volatiles. Ent. Exp. Appl. 123, 43–47

    Article  CAS  Google Scholar 

  • Dehazan, M., Lensky, Y., Cassier, P. (1989) Effects of queen honeybee (Apis mellifera L.) aging on her attractiveness to workers. Comp. Biochem. Physiol. 93, 777–783

    Article  Google Scholar 

  • Dimitriadis, V.K., Kastritsis, C. (1985) Ultrastructural analysis of the midgut of Dosophila auraria larvae–distribution of alkaline phosphatase, acid phosphatase, leucine aminopeptidase, and glycogen. Cytologia 50, 689–700

    Article  Google Scholar 

  • Engels, W., Engels, E., Francke, W. (1997) Ontogeny of cephalic volatile patterns in queens and mating biology of the Neotropical stingless bee, Scaptotrigona postica. Invertebr. Reprod. Dev. 31, 251–256

    Article  CAS  Google Scholar 

  • Gary, N.E. (1961) Queen honey bee attractiveness as related to mandibular gland secretion. Science 133(346), 1479–1480

    Article  CAS  PubMed  Google Scholar 

  • 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, 331–336

    Article  CAS  PubMed  Google Scholar 

  • Gracioli-Vitti, L.F., Abdalla, F.C., Cruz-Landim, C. (2004a) Caracterização das glândulas mandibulares nas diferentes classes de adultos de Scaptotrigona postica Latreille (Hymenoptera, Apidae). Neotrop. Ent. 33, 703–708

    Article  Google Scholar 

  • Gracioli-Vitti, L.F., Abdalla, F.C., Silva-de-Moraes, R.L.M., Jones, G.R. (2004b) The chemical composition of the mandibular gland secretion of Melipona bicolor (Lepeletier, 1836) (Hymenoptera, Apidae, Meliponini), a comparative study among castes and sexes. J. Braz. Chem. Soc. 15, 777–781

    Article  CAS  Google Scholar 

  • Grasso, D.A., Visicchio, R., Castracani, C., Mori, A., Le Moli, F. (2003) The mandibular glands as a source of sexual pheromones in virgin queens of Polyergus rufescens (Hymenoptera, Formicidae). Ital. J. Zool. 70, 229–232

    Article  Google Scholar 

  • Gregorc, A., Bowen, I.D. (1997) Programmed cell death in honey-bee Apis mellifera larvae midgut. Cell Biol. Int. 21, 151–158

  • Gregorc, A., Bowen I.D. (1998) The histopathological changes in honeybee larvae after infection with Bacillus larvae the causative agent of American foulbrood disease. Cell Biol. Int. 22, 137–144

  • Hora, R.R., Delabie, J.H.C., Santos, C.G., Serrão, J.E. (2010) Glandular epithelium as a possible source of a fertility signal in Ectatomma tuberculatum (Hymenoptera, Formicidae) queens. PlosOne 5, e10219

    Article  Google Scholar 

  • Hrncir, M., Jarau, S., Zucchi, R., Barth, F.G. (2004) On the origin and properties of scent marks deposited at the food source by a stingless bee, Melipona seminigra. Apidologie 35, 3–13

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Jarau, S., Schulz, C.M., Hrncir, M., Francke, W., Zucchi, R., Barth, F.G., Ayasse, M. (2006) Hexyl decanoate, the first trail pheromone compound identified in a stingless bee, Trigona recurs. J. Chem. Ecol. 32, 1555–1564

    Article  CAS  PubMed  Google Scholar 

  • Jarau, S., Veen, V., Aguilar, J.W.I., Ayasse, M. (2009) Virgin queen execution in the stingless bee Melipona beecheii, The sign stimulus for worker attacks. Apidologie 40, 496–507

    Article  Google Scholar 

  • Jimenez, D.R., Gilliam, M. (1990) Ultrastructure of the ventriculus of the honey bee, Apis mellifera, cytochemical localization of acid phosphatase, alkaline phosphatase, and nonspecific esterase. Cell Tiss. Res. 261, 431–443

    Article  CAS  Google Scholar 

  • Kerr, W.E., Jungnickel, H., Morgan, E.D. (2004) Workers of the stingless bee Melipona scutellaris are more similar to males than to queens in their cuticular compounds. Apidologie 35, 611–618

    Article  Google Scholar 

  • Kleinert, M.P., Imperatriz-Fonseca, V.L. (1994) Virgin queens refuges in colonies of Melipona marginata (Apidae, Meliponinae). Rev. Brasil. Biol. 54, 247–251

    Google Scholar 

  • Lensky, Y., P. Cassier, Notkin, M., Delorme-Joulie, C. Levinsohn, M. (1985). Pheromonal activity and fine structure of the mandibular glands of honeybee drones (Apis mellifera L.) (Insecta: Hymenoptera: Apidae), J. Ins. Physiol 31, 265-276.

  • Mant, J.B.C., Vereecken, N.J., Schulz, C.M., Francke, W., Schiestl, F.P. (2005) Cuticular hydrocarbons as sex pheromone of the bee Colletes cunicularius and the key to its mimicry by the sexually deceptive orchid. J. Chem. Ecol. 31, 1765–1787

    Article  CAS  PubMed  Google Scholar 

  • Marques-Silva, S., Matiello-Guss, C.P., Delabie, J.H.C., Mariano, C.S.F., Zanuncio, J.C., Serrão, J.E. (2006) Sensilla and secretory glands in the antennae of a primitive ant, Dinoponera lucida (Formicidae, Ponerinae). Microsc. Res. Tech. 69, 885–890

    Article  PubMed  Google Scholar 

  • Martins, L.C.B., Delabie, J.H.C., Zanuncio, J.C., Serrão, J.E. (2013) Post-embryonic development of intramandibular glands in Pachycondyla verenae (Forel) (Hymenoptera: Formicidae) workers. Sociobiology 60, 154–161

    Article  Google Scholar 

  • Michener, C.D. (1974) The social behaviour of the bees: a comparative study. Belknap, Cambridge

    Google Scholar 

  • Nedel, O.J. (1960) Morphologie und physiologie der Mandibeldrusse einiger Bienen Arten Apidae. Zeitschr. Morphol. Oekol. Tiere 49, 139–183

    Article  Google Scholar 

  • Noirot, C., Quennedey, A. (1991) Glands, gland cells, glandular units: some comments on terminology and classification. Ann. Soc. Ent. Fr. 27, 123–128

    Google Scholar 

  • Pearse, A.G.E. (1985) Histochemistry Theoretical and applied. J. & A, Churchil, London

    Google Scholar 

  • Peeters, C., Monnin, T., Malosse, C. (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc. R. Soc. London B - Biol. Sci. 266, 1323–1327

    Article  CAS  Google Scholar 

  • Peters, L., Zhu-Salzman, K., Pankiw, T. (2010) Effect of primer pheromones and pollen diet on the food producing glands of worker honey bees Apis mellifera L. J. Ins. Physiol. 56, 132–137

    Article  CAS  Google Scholar 

  • Romani, R., Isidoro, N., Riolo, P., Bin, F. (2003) Antennal glands in male bees: structures for sexual communication by pheromones? Apidologie 34, 603–610

    Article  Google Scholar 

  • Romani, R., Isidoro, N., Riolo, P.P., Bin, F., Fortunado, A., Beoni, L. (2005) A new role for antennation in paper wasps (Hymenoptera, Vespidae): antennal courtship and sex dimorphic glands in antennomeres. Ins. Soc. 52, 96–102

    Article  Google Scholar 

  • Santos, G., Megiolaro, F.L., Serrão, J.E., Blochtein, B. (2009) Morphology of the head salivary and intramandibular glands of the stingless bee Plebeia emerina (Hymenoptera, Meliponini) workers associated with propolis. Ann. Ent. Soc. Am. 102, 1–7

    Article  Google Scholar 

  • Schorkopf, D.L.P. (2009) Mandibular gland secretions of meliponine worker bees, further evidence for their role in interspecific and intraspecific defence and aggression and against their role in food source signaling. J. Exp. Biol. 212, 1153–1162

    Article  CAS  PubMed  Google Scholar 

  • Schorkopf, D.L.P., Jarau, S., Francke, W., Twele, R., Zucchi, R., Hrncir, M., Schmidt, V.M., Ayasse, M., Barth, F.G. (2007) Spitting out information, Trigona bees deposit saliva to signal resource locations. Proc. R. Soc. London B - Biol. S. 274, 895–896

    Article  Google Scholar 

  • Serrão, J.E., Castro, R.C.A., Zanuncio, J.C., Mariano, C.F., Delabie, J.H.C. (2009) Epidermal glands in the abdomen of a basal ant Dinoponera lucida (Formicidae: Ponerinae. Microsc. Res. Tech. 72, 28–31

    Article  PubMed  Google Scholar 

  • Skelton, H.K., Bowen, I.D. (1987) The cytochemical localization and backscattered electron imaging of acid phosphatase and cell death in the midgut of developing Caliphora vomitoria larvae. Epithelia 1, 213–223

    Google Scholar 

  • Sledge, M.F., Boscaro, F., Turillazzi, S. (2001) Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav. Ecol. Sociobiol. 49, 401–409

    Article  Google Scholar 

  • Smith, R.F., Roubik, D.W. (1983) Mandibular gland of stingless bee (Hymenoptera, Apidae): chemical analysis of their contents and biologic function in two species of Melipona. J. Chem. Ecol. 9, 1465–1472

    Article  CAS  PubMed  Google Scholar 

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

  • Teixeira, A.D., Fialho, M.C.Q., Zanuncio, J.C., Ramalho, F.S., Serrão, J.E. (2013) Degeneration and cell regeneration in the midgut of Podisus nigrispinus (Heteroptera: Pentatomidae) during post-embryonic development. Arthr. Struc. Dev. 42, 237–246

    Article  Google Scholar 

  • van Noorden, C.J.F., Frederiks, W.M. (1992) Enzyme histochemistry: a laboratory manual of current methods. Oxford Science Publication, Oxford

    Google Scholar 

  • van Zweden, J.S., Grueter, C., Jones, S.M., Ratnieks, F.L.W. (2011) Hovering guards of the stingless bee Tetragonisca angustula increase colony defensive perimeter as shown by intra- and inter-specific comparisons. Behav. Ecol. Sociobiol. 65, 1277–1282

    Article  Google Scholar 

  • Vasquez, G.M., Schal, C., Silverman, J. (2008) Cuticular hydrocarbons as queen adoption occur in the invasive Argentine ant. J. Exp. Biol. 211, 1249–1256

    Article  PubMed  Google Scholar 

  • Wossler, T.C., Jones, G.E., Allsoppp, M.H., Hepburn, R. (2006) Virgin queen mandibular gland signals of Apis mellifera capensis change with age and affect honeybee worker responses. J. Chem. Ecol. 32, 1043–1056

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by Brazilian Research Agencies National Council of Research (CNPq) and Minas Gerais State Research Agency (FAPEMIG). Authors are grateful to Nucleus of Microscopy and Microanalysis (UFV) for technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Eduardo Serrão.

Additional information

Morphologie des glandes mandibulaires et intramandibulaires chez les ouvrières et les reines vierges de Melipona scutellaris

Glandes céphaliques / stingless bee / communication / comportement

Morphologie der Mandibeldrüsen und der Intramandibeldrüsen bei Arbeiterinnen und jungfräulichen Königinnen von Melipona scutellaris

Kopfdrüsen / Kommunikation / Verhalten / jungfräuliche Königin

Manuscript editor: James Nieh

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Santos, D.E., de Souza, E.A., Vieira, C.U. et al. Morphology of mandibular and intramandibular glands in workers and virgin queens of Melipona scutellaris . Apidologie 46, 23–34 (2015). https://doi.org/10.1007/s13592-014-0301-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-014-0301-6

Keywords

Navigation