Advertisement

Apidologie

, Volume 46, Issue 1, pp 23–34 | Cite as

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

  • Douglas Elias Santos
  • Edmilson Amaral de Souza
  • Carlos Ueira Vieira
  • José Cola Zanuncio
  • José Eduardo SerrãoEmail author
Original article

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.

Keywords

head glands Melipona communication behavior virgin queen 

Notes

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.

References

  1. Abdalla, F.C., Cruz-Landim, C. (2002) Glândulas Exócrinas das Abelhas. Funpec-RPP, São Paulo. 2002Google Scholar
  2. 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, 349–354Google Scholar
  3. 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.Google Scholar
  4. 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, 582–589Google Scholar
  5. Costa-Leonardo, M. (1978) Glândulas intramandibulares em abelhas sociais. Ciênc. Cult. 30, 835–838Google Scholar
  6. Costa-Leonardo, M. (1981) Ultra-estrutura do ciclo secretor das mandíbulas de operárias de Apis mellifera L. (Hymenoptera, Apidae). Rev. Bras. Zool. 41, 307–316Google Scholar
  7. Cruz-Landim, C. (1967) Estudo comparativo de algumas glândulas de abelhas (Hymenoptera, Apoidea) e respectivas implicações evolutivas. Arq. Zool. São Paulo 15, 177–290CrossRefGoogle Scholar
  8. Cruz-Landim, C. (1994) Polimorfismo na ocorrência das glândulas exócrinas nas abelhas (Hymenoptera, Apidae). In: Encontro Sobre Abelhas, Ribeirão Preto, Brazil 8, 118-129.Google Scholar
  9. Cruz-Landim, C. (2009) Abelhas, Morfologia e Função de Sistemas. Editora Unesp, São PauloGoogle Scholar
  10. 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, 107PubMedCentralPubMedGoogle Scholar
  11. 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, 1621–1632PubMedCrossRefGoogle Scholar
  12. 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, 43–47CrossRefGoogle Scholar
  13. Dehazan, M., Lensky, Y., Cassier, P. (1989) Effects of queen honeybee (Apis mellifera L.) aging on her attractiveness to workers. Comp. Biochem. Physiol. 93, 777–783CrossRefGoogle Scholar
  14. 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, 689–700CrossRefGoogle Scholar
  15. 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, 251–256CrossRefGoogle Scholar
  16. Gary, N.E. (1961) Queen honey bee attractiveness as related to mandibular gland secretion. Science 133(346), 1479–1480PubMedCrossRefGoogle Scholar
  17. 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
  18. 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, 703–708CrossRefGoogle Scholar
  19. 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, 777–781CrossRefGoogle Scholar
  20. 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, 229–232CrossRefGoogle Scholar
  21. Gregorc, A., Bowen, I.D. (1997) Programmed cell death in honey-bee Apis mellifera larvae midgut. Cell Biol. Int. 21, 151–158Google Scholar
  22. 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, 137–144Google Scholar
  23. 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, e10219CrossRefGoogle Scholar
  24. 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, 3–13CrossRefGoogle Scholar
  25. Imperatriz-Fonseca, V.L., Zucchi, R. (1995) Virgin queens in stingless bee (Apidae, Meliponinae) colonies, a review. Apidologie 26, 231–244CrossRefGoogle Scholar
  26. 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, 1555–1564PubMedCrossRefGoogle Scholar
  27. 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, 496–507CrossRefGoogle Scholar
  28. 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, 431–443CrossRefGoogle Scholar
  29. 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, 611–618CrossRefGoogle Scholar
  30. Kleinert, M.P., Imperatriz-Fonseca, V.L. (1994) Virgin queens refuges in colonies of Melipona marginata (Apidae, Meliponinae). Rev. Brasil. Biol. 54, 247–251Google Scholar
  31. 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.Google Scholar
  32. 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, 1765–1787PubMedCrossRefGoogle Scholar
  33. 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, 885–890PubMedCrossRefGoogle Scholar
  34. 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, 154–161CrossRefGoogle Scholar
  35. Michener, C.D. (1974) The social behaviour of the bees: a comparative study. Belknap, CambridgeGoogle Scholar
  36. Nedel, O.J. (1960) Morphologie und physiologie der Mandibeldrusse einiger Bienen Arten Apidae. Zeitschr. Morphol. Oekol. Tiere 49, 139–183CrossRefGoogle Scholar
  37. Noirot, C., Quennedey, A. (1991) Glands, gland cells, glandular units: some comments on terminology and classification. Ann. Soc. Ent. Fr. 27, 123–128Google Scholar
  38. Pearse, A.G.E. (1985) Histochemistry Theoretical and applied. J. & A, Churchil, LondonGoogle Scholar
  39. 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, 1323–1327CrossRefGoogle Scholar
  40. 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, 132–137CrossRefGoogle Scholar
  41. Romani, R., Isidoro, N., Riolo, P., Bin, F. (2003) Antennal glands in male bees: structures for sexual communication by pheromones? Apidologie 34, 603–610CrossRefGoogle Scholar
  42. 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, 96–102CrossRefGoogle Scholar
  43. 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, 1–7CrossRefGoogle Scholar
  44. 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, 1153–1162PubMedCrossRefGoogle Scholar
  45. 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, 895–896CrossRefGoogle Scholar
  46. 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, 28–31PubMedCrossRefGoogle Scholar
  47. 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, 213–223Google Scholar
  48. Sledge, M.F., Boscaro, F., Turillazzi, S. (2001) Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav. Ecol. Sociobiol. 49, 401–409CrossRefGoogle Scholar
  49. 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, 1465–1472PubMedCrossRefGoogle Scholar
  50. Stefanini, M., Demartino, C., Zamboni, L. (1967) Fixation of ejaculated spermatozoa for electron microscopy, Nature 216, 173-174.Google Scholar
  51. 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, 237–246CrossRefGoogle Scholar
  52. van Noorden, C.J.F., Frederiks, W.M. (1992) Enzyme histochemistry: a laboratory manual of current methods. Oxford Science Publication, OxfordGoogle Scholar
  53. 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, 1277–1282CrossRefGoogle Scholar
  54. Vasquez, G.M., Schal, C., Silverman, J. (2008) Cuticular hydrocarbons as queen adoption occur in the invasive Argentine ant. J. Exp. Biol. 211, 1249–1256PubMedCrossRefGoogle Scholar
  55. 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, 1043–1056PubMedCrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France 2014

Authors and Affiliations

  • Douglas Elias Santos
    • 1
  • Edmilson Amaral de Souza
    • 2
  • Carlos Ueira Vieira
    • 3
  • José Cola Zanuncio
    • 4
  • José Eduardo Serrão
    • 1
    Email author
  1. 1.Departamento de Biologia GeralUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Departamento de BiologiaUniversidade Federal de ViçosaRio ParanaíbaBrazil
  3. 3.Instituto de Genética e BioquímicaUniversidade Federal de UberlândiaUberlândiaBrazil
  4. 4.Departamento de Biologia AnimalUniversidade Federal de ViçosaViçosaBrazil

Personalised recommendations