Advertisement

Ecotoxicology

, Volume 26, Issue 9, pp 1199–1206 | Cite as

Lethal and sublethal effects, and incomplete clearance of ingested imidacloprid in honey bees (Apis mellifera)

  • Francisco Sánchez-BayoEmail author
  • Luc Belzunces
  • Jean-Marc Bonmatin
Article

Abstract

A previous study claimed a differential behavioural resilience between spring or summer honey bees (Apis mellifera) and bumble bees (Bombus terrestris) after exposure to syrup contaminated with 125 µg L−1 imidacloprid for 8 days. The authors of that study based their assertion on the lack of body residues and toxic effects in honey bees, whereas bumble bees showed body residues of imidacloprid and impaired locomotion during the exposure. We have reproduced their experiment using winter honey bees subject to the same protocol. After exposure to syrup contaminated with 125 µg L−1 imidacloprid, honey bees experienced high mortality rates (up to 45%), had body residues of imidacloprid in the range 2.7–5.7 ng g−1 and exhibited abnormal behaviours (restless, apathetic, trembling and falling over) that were significantly different from the controls. There was incomplete clearance of the insecticide during the 10-day exposure period. Our results contrast with the findings reported in the previous study for spring or summer honey bees, but are consistent with the results reported for the other bee species.

Keywords

Neonicotinoids Pesticides Bees Chronic exposure Residues Detoxification 

Notes

Funding

This study was only supported by the recurrent funding of the respective research organisms of the authors.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Alkassab AT, Kirchner WH (2016) Impacts of chronic sublethal exposure to clothianidin on winter honeybees. Ecotoxicology 25(5):1000–1010CrossRefGoogle Scholar
  2. Arena M, Sgolastra F (2014) A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23(3):324–334CrossRefGoogle Scholar
  3. Bacandritsos N, Granato A, Budge G, Papanastasiou I, Roinioti E, Caldon M, Falcaro C, Gallina A, Mutinelli F (2010) Sudden deaths and colony population decline in Greek honey bee colonies. J Invertebr Pathol 105(3):335–340CrossRefGoogle Scholar
  4. Blacquière T, Smagghe G, van Gestel C, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21(4):973–992CrossRefGoogle Scholar
  5. Bonmatin JM, Moineau I, Charvet R, Fleche C, Colin ME, Bengsch ER (2003) A LC/APCI-MS/MS method for analysis of imidacloprid in soils, in plants, and in pollens. Anal Chem 75(9):2027–2033CrossRefGoogle Scholar
  6. Bortolotti L, Sabatini AG, Mutinelli F, Astuti M, Lavazza A, Piro R, Tesoriero D, Medrzycki P, Sgolastra F, Porrini C (2009) Spring honey bee losses in Italy. Julius-Kuhn-Archiv 423:148–152Google Scholar
  7. Calatayud-Vernich P, Calatayud F, Simó E, Suarez-Varela MM, Picó Y (2016) Influence of pesticide use in fruit orchards during blooming on honeybee mortality in 4 experimental apiaries. Sci Total Environ 541:33–41CrossRefGoogle Scholar
  8. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA, Berenbaum MR, Feyereisen R, Oakeshott JG (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol 15(5):615–636CrossRefGoogle Scholar
  9. Colin ME, Bonmatin JM, Moineau I, Gaimon C, Brun S, Vermandere JP (2004) A method to quantify and analyze the foraging activity of honey bees: relevance to the sublethal effects induced by systemic insecticides. Arch Environ Contam Toxicol 47(3):387–395CrossRefGoogle Scholar
  10. Crailsheim K (1986) Dependence of protein metabolism on age and season in the honeybee (Apis mellifica carnica Pollm). J Insect Physiol 32(7):629–634CrossRefGoogle Scholar
  11. Cresswell J (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20(1):149–157CrossRefGoogle Scholar
  12. Cresswell JE, Page CJ, Uygun MB, Holmbergh M, Li Y, Wheeler JG, Laycock I, Pook CJ, de Ibarra NH, Smirnoff N et al. (2012) Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology 115(6):365–371CrossRefGoogle Scholar
  13. Cresswell JE, Robert F-XL, Florance H, Smirnoff N (2014) Clearance of ingested neonicotinoid pesticide (imidacloprid) in honey bees (Apis mellifera) and bumblebees (Bombus terrestris). Pest Manag Sci 70(2):332–337CrossRefGoogle Scholar
  14. Decourtye A, Lacassie E, Pham-Delègue M-H (2003) Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Manag Sci 59(3):269–278CrossRefGoogle Scholar
  15. Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106CrossRefGoogle Scholar
  16. Dively GP, Embrey MS, Kamel A, Hawthorne DJ, Pettis JS (2015) Assessment of chronic sublethal effects of imidacloprid on honey bee colony health. PLoS One 10(3):e0118748CrossRefGoogle Scholar
  17. Hardstone MC, Scott JG (2010) Is Apis mellifera more sensitive to insecticides than other insects? Pest Manag Sci 66(11):1171–1180CrossRefGoogle Scholar
  18. Hladik ML, Vandever M, Smalling KL (2016) Exposure of native bees foraging in an agricultural landscape to current-use pesticides. Sci Total Environ 542:469–477CrossRefGoogle Scholar
  19. Laycock I, Lenthall K, Barratt A, Cresswell J (2012) Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21(7):1937–1945CrossRefGoogle Scholar
  20. Marletto F, Patetta A, Manino A (2003) Laboratory assessment of pesticide toxicity to bumble bees. Bull Insectol 56(1):155–158Google Scholar
  21. Medrzycki P, Montanari R, Bortolotti L, Sabatini AG, Maini S, Porrini C (2003) Effects of imidacloprid administered in sublethal doses on honey bee behaviour. Laboratory tests. Bull Insectol 56(1):59–62Google Scholar
  22. Meled M, Thrasyvoulou A, Belzunces LP (1998) Seasonal variations in susceptibility of Apis mellifera to the synergistic action of prochloraz and deltamethrin. Environ Toxicol Chem 17(12):2517–2520CrossRefGoogle Scholar
  23. Moffat C, Buckland ST, Samson AJ, McArthur R, Chamosa Pino V, Bollan KA, Huang JTJ, Connolly CN (2016) Neonicotinoids target distinct nicotinic acetylcholine receptors and neurons, leading to differential risks to bumblebees. Sci. Rep 6:24764CrossRefGoogle Scholar
  24. Ramirez-Romero R, Chaufaux J, Pham-Delègue M-H (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):601–611CrossRefGoogle Scholar
  25. Rinkevich FD, Margotta JW, Pittman JM, Danka RG, Tarver MR, Ottea JA, Healy KB (2015) Genetics, synergists, and age affect insecticide sensitivity of the honey bee, Apis mellifera. PLoS One 10(10):e0139841CrossRefGoogle Scholar
  26. Rondeau G, Sánchez-Bayo F, Tennekes HA, Decourtye A, Ramírez-Romero R, Desneux N (2014) Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites. Sci Rep 4:5566CrossRefGoogle Scholar
  27. Sánchez-Bayo F, Goka K (2014) Pesticide residues and bees—a risk assessment. PLoS One 9(4):e94482CrossRefGoogle Scholar
  28. Schmuck R, Schöning R, Stork A, Schramel O (2001) Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag Sci 57(3):225–238CrossRefGoogle Scholar
  29. Suchail S, Debrauwer L, Belzunces LP (2004a) Metabolism of imidacloprid in Apis mellifera. Pest Manag Sci 60(3):291–296CrossRefGoogle Scholar
  30. Suchail S, Guez D, Belzunces LP (2001) Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ Toxicol Chem 20(11):2482–2486CrossRefGoogle Scholar
  31. Suchail S, de Sousa G, Rahmani R, Belzunces LP (2004b) In vivo distribution and metabolisation of 14C-imidacloprid in different compartments of Apis mellifera L. Pest Manag Sci 60(11):1056–1062CrossRefGoogle Scholar
  32. Teeters BS, Johnson RM, Ellis MD, Siegfried BD (2012) Using video-tracking to assess sublethal effects of pesticides on honey bees (Apis mellifera L.). Environ Toxicol Chem 31(6):1349–1354CrossRefGoogle Scholar
  33. Thompson H (2016) Extrapolation of acute toxicity across bee species. Integr Environ Assess Manag 12(4):622–626CrossRefGoogle Scholar
  34. Thompson HM (2001) Assessing the exposure and toxicity of pesticides to bumblebees (Bombus sp.). Apidologie 32:305–321CrossRefGoogle Scholar
  35. Thompson HM, Wilkins S, Harkin S, Milner S, Walters KFA (2015) Neonicotinoids and bumblebees (Bombus terrestris): effects on nectar consumption in individual workers. Pest Manag Sci 71(7):946–950CrossRefGoogle Scholar
  36. Williamson SM, Willis SJ, Wright GA (2014) Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology 23(8):1409–1418CrossRefGoogle Scholar
  37. Yang EC, Chuang YC, Chen YL, Chang LH (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 101(6):1743–1748CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Francisco Sánchez-Bayo
    • 1
    Email author
  • Luc Belzunces
    • 2
  • Jean-Marc Bonmatin
    • 3
  1. 1.School of Life and Environmental Sciences, Biomedical building, The University of SydneyEveleighAustralia
  2. 2.INRA, Laboratoire de Toxicologie EnvironnementaleAvignonFrance
  3. 3.Centre National de la Recherche Scientifique (CNRS), Centre de Biophysique MoléculaireOrléansFrance

Personalised recommendations