Skip to main content
Log in

The effects of four crop protection products on the morphology and ultrastructure of the hypopharyngeal gland of the European honeybee, Apis mellifera

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

Abstract

This study describes the impact of sublethal doses of 4 pesticides on size and morphology of the honeybee worker’s hypopharyngeal glands. This gland plays an essential role in brood care by young workers, and thus colony growth. Contaminating 7 day old caged bees, we sampled after 1 day and 1 week for Captan-, Imidacloprid- and Indoxacarb-treated bees and after 1, 2, 3, 4, 5 and 7 days for Fenoxycarb-treated bees. The glands’ acini 1 week post-treatment were all significantly smaller in treated bees. However, lightand electron microscopy showed hardly any difference between controls and gland cells, treated with Captan, Imidacloprid or Indoxacarb. Yet upon Fenoxycarb-treatment, acini showed a decrease in size, a granular texture and unorganized cytoplasm more quickly than normal. Indeed, after only 7 days, Fenoxycarb-treated glands displayed features typical of the onset of foraging in older bees.

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.

Similar content being viewed by others

References

  • Bortolotti L., Montanari R., Marcelino J., Medrzycki P., Maini S., Porrini C. (2003) Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees, Bull. Insectology 56, 63–67.

    Google Scholar 

  • Buckingham S.D., Lapied B., Le Corronc H., Grolleau F., Sattelle D.B. (1997) Imidacloprid actions on insect neuronal acetylcholine receptors, J. Exp. Biol. 200, 2685–2692.

    PubMed  CAS  Google Scholar 

  • Chauzat M.P., Faucon J.P., Martel A.C., Lachaize J., Cougoule N., Aubert M. (2006). Survey of Pesticide Residues in Pollen Loads Collected by Honey Bees in France, J. Econ. Entomol. 99, 253–262.

    Article  PubMed  CAS  Google Scholar 

  • Cruz Landim C. da, Hadek R. (1969) Ultrastructure of Apis mellifera hypopharyngeal gland, Proc. 6th Int. Congr. IUSSI, Bern, pp. 121–130.

  • Decourtye A., Armengaud C., Renou M., Devillers J., Cluzeau S., Gauthier M., Delegue M.H.P. (2004) Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.), Pest. Biochem. Physiol. 78, 83–92.

    Article  CAS  Google Scholar 

  • Deseyn J., Billen J. (2005) Age-dependent morphology and ultrastructure of the hypopharyngeal gland of Apis mellifera workers (Hymenoptera, Apidae), Apidologie 36, 49–57.

    Article  Google Scholar 

  • Dhadialla T.S., Carlson G.R., Le D.P. (1998) New insecticides with ecdysteroidal and juvenile hormone activity, Annu. Rev. Entomol. 43, 545–569.

    Article  PubMed  CAS  Google Scholar 

  • El Hassani A.K., Dacher M., Gary V., Lambin M., Gauthier M., Armengaud C. (2008) Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera), Arch. Environ. Contam. Toxicol. 54, 653–661.

    Article  PubMed  Google Scholar 

  • Faucon J.-P., Mathieu L., Ribiere M., Martel A.-C., Drajnudel P., Zeggane S., Aurieres C., Aubert M.F.A. (2002) Honey bee winter mortality in France in 1999 and 2000, Bee World 83, 14–23.

    Google Scholar 

  • Furquim K.C.S., Camargo-Mathias M.I., Silva de Moraes R.L.M. (2004) Morphological modifications induced by an artificial diet on the hypopharyngeal glands of Apis mellifera (Hymenoptera, Apidae) during their degenerative process, Sociobiology 43, 45–49.

    Google Scholar 

  • Haynes K.F. (1988) Sublethal effects of neurotoxic insecticides on insect behavior, Annu. Rev. Entomol. 33, 149–168.

    Article  PubMed  CAS  Google Scholar 

  • Hrassnigg N., Crailsheim K. (1998) Adaptation of hypopharyngeal gland development to the brood status of honeybee (Apis mellifera L.) colonies, J. Insect Physiol. 44, 929–939.

    Article  PubMed  CAS  Google Scholar 

  • Lapied B., Grolleau F., Sattelle D.B. (2001) Indoxacarb, an oxadiazine insecticide, blocks insect neuronal sodium channels, Br. J. Pharmacol. 132, 587–595.

    Article  PubMed  CAS  Google Scholar 

  • Malone L.A., Todd J.H., Burgess E.P.J., Christeller J.T. (2004) Development of hypopharyngeal glands in adult honey bees fed with a Bt toxin, a biotin binding protein and a protease inhibitor, Apidologie 35, 655–664.

    Article  CAS  Google Scholar 

  • Medrzycki P., Montanari R., Bortolotti L., Sabatini A.G., Maini S., Porrini V. (2003) Effects of Imidacloprid administered in sub-lethal doses on honey bee behaviour. Lab tests, Bull. Insectology 56, 59–62.

    Google Scholar 

  • Ohashi K., Natori S., Kubo T. (1997) Change in the mode of gene expression of the hypopharyngeal gland cells with an age-dependent role change of the worker honeybee Apis mellifera L., Eur. J. Biochem. 249, 797–802.

    Article  PubMed  CAS  Google Scholar 

  • Owens R.G. (1969) Metabolism of fungicides and related compounds, Ann. N.Y. Acad. Sci. 160, 114–132.

    Article  PubMed  CAS  Google Scholar 

  • Robinson G.E., Ratnieks F.L.W. (1987) Induction of premature honey bee (Hymenoptera: Apidae) flight by juvenile hormone analogs administered orally or topically, J. Econ. Entomol. 80, 784–787.

    CAS  Google Scholar 

  • Rutz W., Gerig L., Wille H., Lüscher M. (1974) A bioassay for juvenile hormone (JH) effects of insect growth regulators (IGR) on adult worker honeybees, Bull. Soc. Entomol. Suisse 47, 307–313.

    Google Scholar 

  • Sasagawa H., Sasaki M., Okada I. (1989) Hormonal control of the division of labor in adult honeybees (Apis mellifera L.). I. Effect of methoprene on corpora allata and hypopharyngeal gland, and its α-glucosidase activity, Appl. Entomol. Zool. 24, 66–77.

    CAS  Google Scholar 

  • Silva de Moraes R.L.M., Bowen I.D. (2000) Modes of cell death in hypopharyngeal glands of honey bee (Apis mellifera L.), Cell Biol. Int. 24, 737–743.

    Article  PubMed  CAS  Google Scholar 

  • Simpson J., Riedel I.B.M., Wilding N. (1968) Invertase in the hypopharyngeal glands of the honeybee, J. Apic. Res. 7, 29–36.

    CAS  Google Scholar 

  • Suchail S., Guez D., Belzunces L.P. (2001) Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera, Environ. Toxicol. Chem. 20, 2482–2486.

    PubMed  CAS  Google Scholar 

  • Tasei J.N. (2001) Effects of insect growth regulators on honey bees and non-Apis bees. A review, Apidologie 32, 527–545.

    Article  CAS  Google Scholar 

  • Thompson H.M., Wilkins S., Battersby A.H., Waite R.J., Wilkinson D. (2005) The effects of four insect growth-regulating (IGR) insecticides on honeybee (Apis mellifera L.) colony development, queen rearing and drone sperm production, Ecotoxicology 14, 757–769.

    Article  PubMed  CAS  Google Scholar 

  • Thompson H.M., Wilkins S., Battersby A., Waite R.J., Wilkinson D. (2007) Modelling long-term effects of IGRs on honey bee colonies, Pest Manage. Sci. 63, 1081–1084.

    Article  CAS  Google Scholar 

  • Tsurubuchi Y., Kono Y. (2003) Modulation of sodium channels by the oxadiazine insecticide indoxacarb and its N-decarbomethoxylated metabolite in rat dorsal root ganglion neurons, Pest Manage. Sci. 59, 999–1006.

    Article  CAS  Google Scholar 

  • van der Steen J. (2001) Review of the methods to determine the hazard and toxicity of pesticides to bumblebees, Apidologie 32, 399–406.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johan Billen.

Additional information

Manuscript editor: Monique Gauthier

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heylen, K., Gobin, B., Arckens, L. et al. The effects of four crop protection products on the morphology and ultrastructure of the hypopharyngeal gland of the European honeybee, Apis mellifera . Apidologie 42, 103–116 (2011). https://doi.org/10.1051/apido/2010043

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1051/apido/2010043

Keywords

Navigation