Skip to main content

Toxicity of insecticides used in the Brazilian melon crop to the honey bee Apis mellifera under laboratory conditions

Abstract

This study aimed at evaluating the toxicity of insecticides used in melon crop (Cucumis melo L.) on adults of Apis mellifera L. (Hymenoptera: Apidae) under laboratory conditions. Three ways of exposure were used: direct spraying, feeding with insecticide contaminated diet, and contact with sprayed leaves. Bees were exposed to the insecticides abamectin, acetamiprid, cartap chloride, chlorfenapyr, cyromazin, deltamethrin, thiamethoxam, flufenoxuron, and pyriproxyfen at the highest dosages recommended by the manufacturers for the melon crop in Brazil. Results indicated that, regardless of how the bees were exposed to insecticides, thiamethoxam, abamectin, and chlorfenapyr were extremely toxic to adults of A. mellifera. Acetamiprid, deltamethrin, and cartap chloride were most toxic when directly sprayed on the bees. Cyromazin and pyriproxyfen caused low mortality rates to A. mellifera, whereas flufenoxuron caused moderate mortality when fed to adult bees.

This is a preview of subscription content, access via your institution.

Figure 1.
Figure 2.
Figure 3.

References

  1. Abbott, W.S. (1925) A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18(2), 265–267

    CAS  Google Scholar 

  2. Baptista, A.P.M., Carvalho, G.A., Carvalho, S.M., Carvalho, C.F., Bueno Filho, J.S.S. (2009) Toxicidade de produtos fitossanitários utilizados em citros para Apis mellifera. Cienc. Rural 39(4), 955–961

    CAS  Article  Google Scholar 

  3. Barnett, E.A., Charlton, A.J., Fletcher, M.R. (2007) Incidents of bee poisoning with pesticides in the United Kingdom, 1994–2003. Pest Manag. Sci. 63(11), 1051–1057

    CAS  PubMed  Article  Google Scholar 

  4. Bernal, J., Garrido-Bailón, E., Del Nozal, M.J., González-Porto, A.V., Martín-Hernández, R., et al. (2010) Overview of pesticide residues in stored pollen and their potential effect on bee colony (Apis mellifera) losses in Spain. J. Econ. Entomol. 103(6), 1964–1971

    CAS  PubMed  Article  Google Scholar 

  5. Blacquiere, T., Smagghe, G., Gestel, C.A.M.V., Mommaerts, V. (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21(4), 973–992

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  6. Carvalho, S.M., Carvalho, G.A., Carvalho, C.F., Bueno Filho, J.S.S., Baptista, A.P.M. (2009) Toxicidade de acaricidas/inseticidas empregados na citricultura para a abelha africanizada Apis mellifera L. 1758 (Hymenoptera: Apidae). Arq. Inst Biol 76(4), 597–606

    Google Scholar 

  7. Cresswell, J.E., Desneux, N., Vanengelsdorp, D. (2012) Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill’s epidemiological criteria. Pest Manag. Sci. 68(6), 819–827

    CAS  PubMed  Article  Google Scholar 

  8. Desneux, N., Decourtye, A., Delpuech, J. (2007) The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106

    CAS  PubMed  Article  Google Scholar 

  9. Devine, G.J., Furlong, M.J. (2007) Insecticide use: contexts and ecological consequences. Agr. Hum. Values 24(3), 281–306

    Article  Google Scholar 

  10. Eto, M. (1990) Biochemical mechanisms of insecticidal activities. Chem. Plant Protect. 6, 65–107

    CAS  Article  Google Scholar 

  11. Fletcher, M., Barnett, L. (2003) Bee poisoning incidents in the United Kingdom. B. Insectol. 56(1), 141–145

    Google Scholar 

  12. Freitas, B.M., Imperatriz-Fonseca, V.L., Medina, L.M., Kleinert, A.M.P., Galleto, L., et al. (2009) Diversity, threats and conservation of native bees in the Neotropics. Apidologie 40(3), 332–346

    Article  Google Scholar 

  13. Friedel, G., McDonell, P.A. (1985) Cyromazine inhibits reproduction and larval development of the Australian sheep blow fly (Diptera: Calliphoridae). J. Econ. Entomol. 78(4), 868–873

    CAS  PubMed  Google Scholar 

  14. Gallai, N., Salles, J.M., Settele, J., Vaissière, B.E. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68(3), 810–821

    Article  Google Scholar 

  15. Guimarães, J. A., Braga Sobrinho, R., Azevedo, F. R., Araujo, E. L., Terão, D., Mesquita, A. L. M. (2008) Manejo integrado de pragas do meloeiro, in: Braga Sobrinho, R., Guimarães, J. A., Freitas, J. A. D., Terão, D. (Eds.), Produção Integrada de Melão. EMBRAPA Agroindustria Tropical, pp. 183–199

  16. Henry, M., Beguin, M., Requier, F., Rollin, O., Odoux, J.F., et al. (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336(6079), 348–350

    CAS  PubMed  Article  Google Scholar 

  17. IBGE (Brazilian Institute of Geography and Statistics) (2012) Temporary crop (online). http://www.ibge.gov.br/estadosat/ (accessed on 19 November 12)

  18. Iwasa, T., Motoyama, N., Ambrose, J.T., Roe, R.M. (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot. 23(5), 371–378

    CAS  Article  Google Scholar 

  19. Johnson, R.M., Ellis, M.D., Mullin, C.A., Frazier, M. (2010) Pesticides and honey bee toxicity – USA. Apidologie 41(3), 312–331

    CAS  Article  Google Scholar 

  20. Kagabu, S. (1997) Chloronicotinyl insecticides: discovery, application and future perspective. Reviews in Toxicology 1, 75–129

    CAS  Google Scholar 

  21. Kearns, C.A., Inouye, D.W. (1997) Pollinators, flowering plants and conservation biology. BioScience 47(5), 297–307

    Article  Google Scholar 

  22. Klein, A.M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., et al. (2007) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B: Biol. Sci. 274(1608), 303–313

    Article  Google Scholar 

  23. Lautenbach, S., Seppelt, R., Liebscher, J., Dormann, C.F. (2012) Spatial and temporal trends of global pollination benefit. PLoS ONE . doi:10.1371/journal.pone.0035954

    PubMed  PubMed Central  Google Scholar 

  24. Laurino, D., Porporato, M., Patetta, A., Manino, A. (2011) Toxicity of neonicotinoid insecticides to honey bees: laboratory tests. B. Insectol. 64(1), 107–113

    Google Scholar 

  25. Malerbo-Souza, D.T., Nogueira-Couto, R.H., Couto, L.A. (2003) Pollination in orange sweet crop (Citrus sinensis L. Osbeck, var. Pera-Rio). Braz. J. Vet. Res. and Anim Sci 40(4), 237–242

    Google Scholar 

  26. Marçon, P. G. (2011) Modo de ação de inseticidas e acaricidas (online). http://www.irac-br.org.br/arquivos/mododeacao.doc (accessed on 10 January 11)

  27. McGregor, S.E. (1976) Insect pollination of cultivated crop plants. Agriculture Handbook. Agricultural Reserch Service, USDA, Washington

    Google Scholar 

  28. Nica, D., Bianu, E., Chioveanu, G. (2004) A case of acute intoxication with deltamethrin in bee colonies in Romania. Apiacta 39(1), 71–77

    Google Scholar 

  29. Ollerton, J., Winfree, R., Tarrant, S. (2011) How many flowering plants are pollinated by animals? Oikos 120(3), 321–326

    Article  Google Scholar 

  30. Pinheiro, J.N., Freitas, B.M. (2010) Efeitos letais dos pesticidas agrícolas sobre polinizadores e perspectivas de manejo para os agroecossistemas brasileiros. Oecol. Aust. 14(1), 266–281

    Article  Google Scholar 

  31. Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., et al. (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25(6), 345–353

    PubMed  Article  Google Scholar 

  32. R Development Core Team (2010) R: A language and environment for statistical computing (online). http://www.R-project.org/ (accessed on 08 December 10)

  33. Ramirez-Romero, R., Chaufaux, J., Pham-Delègue, M. (2005) Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie 36(4), 601–611

    CAS  Article  Google Scholar 

  34. Rhodes, J., Scott, M. (2006) Pesticides: a guide to their effects on honey bees. NSW Department of Primary Industries: Primefacts 149

  35. Sousa, R.M., Aguiar, O.S., Freitas, B.M., Neto, A.A.S., Pereira, T.F.C. (2009) Requerimentos de polinização do meloeiro (Cucumis melo L.) no município de Acaraú – CE – Brasil. Revista Caatinga 22(1), 238–242

    Google Scholar 

  36. Therneau, T., Lumley, T. (2010) Survival: survival analysis, including penalised likelihood (online). http://CRAN.R-project .org/package = survival (accessed on 08 December 10)

  37. Thompson, H.M. (2003) Behavioural effects of pesticides in bees – their potential for use in risk assessment. Ecotoxicology 12(1–4), 317–330

    CAS  PubMed  Article  Google Scholar 

  38. Thomazoni, D., Soria, M.F., Kodama, C., Carbonari, V., Fortunato, R.P., et al. (2009) Selectivity of insecticides for adult workers of Apis mellifera (Hymenoptera: Apidae). Rev. Colomb. Entomol. 35(2), 173–176

    CAS  Google Scholar 

  39. Van Engelsdorp, D., Meixner, M.D. (2010) A historical review of managed honey bee populations in Europe and United States and the factors that may affect them. J. Invertebr. Pathol. . doi:10.1016/j.jip.2009.06.011

    Google Scholar 

  40. Ware, G.W., Whitacre, D.M. (2004) The Pesticide Book, 6th edn. Meister Media Worldwide, Willoughby

    Google Scholar 

Download references

Acknowledgments

We would like to thank Jacquelinne A. M. Araujo (Master Student—Plant Science/UFERSA) for her help in the laboratory and Carter R. Miller (PhD in Horticulture—Pennsylvania State University) for his valuable comments on an earlier version of the manuscript. Financial support was provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) through a Ph.D. fellowship to the first author.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Carlos E. S. Bezerra.

Additional information

Toxicité des insecticides utilisés en cultures de melon au Brésil vis-à-vis de l’abeille Apis mellifera , en conditions de laboratoire

Conservation / mortalité / organisme non-cible / pollinisateur / traitement phytosanitaire

Toxizität von im brasilianischen Melonenanbau eingesetzten Insektiziden für die Honigbiene Apis mellifera unter Laborbedingungen

Schutz / Mortalität / Nicht-Ziel Organismen / Bestäubung / Pflanzengesundheitsbehandlung

Manuscript editor: Monique Gauthier

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Costa, E.M., Araujo, E.L., Maia, A.V.P. et al. Toxicity of insecticides used in the Brazilian melon crop to the honey bee Apis mellifera under laboratory conditions. Apidologie 45, 34–44 (2014). https://doi.org/10.1007/s13592-013-0226-5

Download citation

Keywords

  • conservation
  • mortality
  • nontarget organisms
  • pollinator
  • phytosanitary treatment