A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees

Abstract

Honey bees provide important pollination services to crops and wild plants. The agricultural use of systemic insecticides, such as neonicotinoids, may harm bees through their presence in pollen and nectar, which bees consume. Many studies have tested the effects on honey bees of imidacloprid, a neonicotinoid, but a clear picture of the risk it poses to bees has not previously emerged, because investigations are methodologically varied and inconsistent in outcome. In a meta-analysis of fourteen published studies of the effects of imidacloprid on honey bees under laboratory and semi-field conditions that comprised measurements on 7073 adult individuals and 36 colonies, fitted dose–response relationships estimate that trace dietary imidacloprid at field-realistic levels in nectar will have no lethal effects, but will reduce expected performance in honey bees by between 6 and 20%. Statistical power analysis showed that published field trials that have reported no effects on honey bees from neonicotinoids were incapable of detecting these predicted sublethal effects with conventionally accepted levels of certainty. These findings raise renewed concern about the impact on honey bees of dietary imidacloprid, but because questions remain over the environmental relevance of predominantly laboratory-based results, I identify targets for research and provide procedural recommendations for future studies.

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

Fig. 1
Fig. 2

References

  1. Alghamdi A, Dalton L, Phillis A, Rosato E, Mallon EB (2008) Immune response impairs learning in free-flying bumble-bees. Biol Lett 4:479–481

    CAS  Article  Google Scholar 

  2. Aupinel P, Fortini D, Michaud B, Marolleau F, Tasei JN, Odoux JF (2007) Toxicity of dimethoate and fenoxycarb to honey bee brood (Apis mellifera), using a new in vitro standardized feeding method. Pest Manag Sci 63:1090–1094

    CAS  Article  Google Scholar 

  3. Bailey J, Scott-Dupree C, Harris R, Tolman J, Harris B (2005) Contact and oral toxicity to honey bees (Apis mellifera) of agents registered for use for sweet corn insect control in Ontario, Canada. Apidologie 36:623–633

    CAS  Article  Google Scholar 

  4. 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 75:2027–2033

    CAS  Article  Google Scholar 

  5. Bonmatin JM, Marchand PA, Charvet R, Moineau I, Bengsch ER, Colin ME (2005) Quantification of imidacloprid uptake in maize crops. J Agric Food Chem 53:5336–5341

    CAS  Article  Google Scholar 

  6. 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 Insectol 56:63–67

    Google Scholar 

  7. BVL (2010) Bundesamt für Verbraucherschutz und Lebensmittelsicherheit. http://www.bvl.bund.de/cln_007/nn_496790/sid_DC14916176B10F16C97BA780A40B2F2B/EN/08__PresseInfothek__engl/01__Presse__und__Hintergrundinformationen/2009__02__09__pi__Maissaatgut__Mesurol__en.html__nnn=true. Accessed 12 July 2010

  8. 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 47:387–395

    CAS  Article  Google Scholar 

  9. Crawley M (2007) The R book. Wiley, Chichester

    Google Scholar 

  10. Cresswell JE (1999) The influence of nectar and pollen availability on pollen transfer by individual flowers of oil-seed rape (Brassica napus) when pollinated by bumblebees (Bombus lapidarius). J Ecol 87:670–677

    Article  Google Scholar 

  11. Croft B (1990) Arthropod biological control agents and pesticides. Wiley, New York

    Google Scholar 

  12. Cutler GC, Scott-Dupree CD (2007) Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. J Econ Entomol 100:765–772

    CAS  Article  Google Scholar 

  13. de Jong FMW, de Snoo GR, van de Zande JC (2008) Estimated nationwide effects of pesticide spray drift on terrestrial habitats in the Netherlands. J Environ Manag 86:721–730

    Article  Google Scholar 

  14. Decourtye A, Lacassie E, Pham-Delegue MH (2003) Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Manag Sci 59:269–278

    CAS  Article  Google Scholar 

  15. Decourtye A et al (2004a) Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pestic Biochem Physiol 78:83–92

    CAS  Article  Google Scholar 

  16. Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delegue MH (2004b) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57:410–419

    CAS  Article  Google Scholar 

  17. DEFRA (2007) Assessment of the risk posed to honeybees by systemic pesticides (Project no. PS2322). Department for Environment, Food and Rural Affairs, London

  18. DEFRA (2009) Agriculture in the United Kingdom 2009. Department of Food, Environment and Rural Affairs, London

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

    CAS  Article  Google Scholar 

  20. El Hassani AK, 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 Toxicl 54:653–661

    CAS  Article  Google Scholar 

  21. Elbert A, Haas M, Springer B, Thielert W, Nauen R (2008) Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci 64:1099–1105

    CAS  Article  Google Scholar 

  22. Faucon JP et al (2005) Experimental study on the toxicity of imidacloprid given in syrup to honey bee (Apis mellifera) colonies. Pest Manag Sci 61:111–125

    CAS  Article  Google Scholar 

  23. Girolami V et al (2009) Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: a novel way of intoxication for bees. J Econ Entomol 102:1808–1815

    CAS  Article  Google Scholar 

  24. Glass GV (1976) Primary, secondary, and meta-analysis of research. Educ Res 5:3–8

    Google Scholar 

  25. Greatti M, Barbattini R, Stravisi A, Sabatini A, Rossi S (2006) Presence of the a.i. imidacloprid on vegetation near corn fields sown with Gaucho® dressed seeds. Bull Insectol 59:99–103

    Google Scholar 

  26. Guez D, Suchail S, Gauthier M, Maleszka R, Belzunces LP (2001) Contrasting effects of imidacloprid on habituation in 7- and 8-day-old honeybees (Apis mellifera). Neurobiol Learn Mem 76:183–191

    CAS  Article  Google Scholar 

  27. Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149

    Article  Google Scholar 

  28. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156

    Article  Google Scholar 

  29. Hoyle M, Hayter KE, Cresswell JE (2007) Effect of pollinator abundance on self-fertilization and gene flow: application to GM canola. Ecol Appl 17:2123–2135

    Article  Google Scholar 

  30. Ihaka R, Gentleman R (1996) A language for data analysis and graphics. J Comput Graph Stat 5:299–314

    Article  Google Scholar 

  31. Iwasa T, Motoyama N, Ambrose JT, Roe RM (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot 23:371–378

    CAS  Article  Google Scholar 

  32. Johnson RM, Evans JD, Robinson GE, Berenbaum MR (2009) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proc Natl Acad Sci USA 106:14790–14795

    CAS  Article  Google Scholar 

  33. Kremen C, Ricketts T (2000) Global perspectives on pollination disruptions. Conserv Biol 14:1226–1228

    Article  Google Scholar 

  34. Lambin M, Armengaud C, Raymond S, Gauthier M (2001) Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee. Arch Insect Biochem Physiol 48:129–134

    CAS  Article  Google Scholar 

  35. Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22:573–580

    CAS  Article  Google Scholar 

  36. Maus C, Gaelle C, Schmuck R (2003) Safety of imidacloprid seed dressings to honey bees: a comprehensive overview and compilation of the current state of knowledge. Bull Insectol 56:51–57

    Google Scholar 

  37. Medrzycki P, Montanari R, Bortolotti L, Sabatini A, Maini S, Porrini C (2003) Effects of imidacloprid administered in sub-lethal doses on honey bee behaviour. Laboratory tests. Bull Insectol 56:59–62

    Google Scholar 

  38. 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 17:2517–2520

    CAS  Google Scholar 

  39. Mommaerts V, Reynders S, Boulet J, Besard L, Sterk G, Smagghe G (2010) Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19:207–215

    CAS  Article  Google Scholar 

  40. Mullin CA et al (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. Plos One 5:e9754

    Article  Google Scholar 

  41. Nauen R, Ebbinghaus-Kintscher U, Schmuck R (2001) Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae). Pest Manag Sci 57:577–586

    CAS  Article  Google Scholar 

  42. Nguyen BK et al (2009) Does imidacloprid seed-treated maize have an impact on honey bee mortality? J Econ Entomol 102:616–623

    CAS  Article  Google Scholar 

  43. Oerke EC, Dehne HW (2004) Safeguarding production—losses in major crops and the role of crop protection. Crop Prot 23:275–285

    Article  Google Scholar 

  44. Petanidou T (2003) Introducing plants for bee-keeping at any cost?—Assessment of Phacelia tanacetifolia as nectar source plant under xeric Mediterranean conditions. Plant Syst Evol 238:155–168

    Google Scholar 

  45. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  Google Scholar 

  46. Ragsdale NN (2006) The role of pesticides in agricultural crop protection. Ann NY Acad Sci 894:199–205

    Article  Google Scholar 

  47. Ramirez-Romero R, Chaufaux J, Pham-Delegue MH (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 36:601–611

    CAS  Article  Google Scholar 

  48. Ramirez-Romero R, Desneux N, Decourtye A, Chaffiol A, Pham-Delegue MH (2008) Does CrylAb protein affect learning performances of the honey bee Apis mellifera L. (Hymenoptera, Apidae)? Ecotoxicol Environ Saf 70:327–333

    CAS  Article  Google Scholar 

  49. Ribbands C (1953) The behaviour and social life of honeybees. Bee Research Association Ltd., London

    Google Scholar 

  50. Riddell CE, Mallon EB (2006) Insect psychoneuroimmunology: immune response reduces learning in protein starved bumblebees (Bombus terrestris). Brain Behav Immun 20:135–138

    CAS  Article  Google Scholar 

  51. Rortais A, Arnold G, Halm MP, Touffet-Briens F (2005) Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36:71–83

    CAS  Article  Google Scholar 

  52. Schmuck R (2004) Effects of a chronic dietary exposure of the honeybee Apis mellifera (Hymenoptera: Apidae) to imidacloprid. Arch Environ Contam Toxicol 47:471–478

    CAS  Article  Google Scholar 

  53. Schmuck R, Schoning R, Stork A, Schramel O (2001) Risk posed to honeybees (Apis mellifera L. Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag Sci 57:225–238

    CAS  Article  Google Scholar 

  54. Seeley TD (1985) Honeybee ecology. Princeton University Press, Princeton

    Google Scholar 

  55. Smirle MJ, Winston ML (1987) Intercolony variation in pesticide detoxification by the honey-bee (Hymenoptera, Apidae). J Econ Entomol 80:5–8

    CAS  Google Scholar 

  56. Suchail S, Guez D, Belzunces LP (2000) Characteristics of imidacloprid toxicity in two Apis mellifera subspecies. Environ Toxicol Chem 19:1901–1905

    CAS  Google Scholar 

  57. 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 20:2482–2486

    CAS  Google Scholar 

  58. Sur R, Stork A (2003) Uptake, translocation and metabolism of imidacloprid in plants. Bull Insectol 56:35–40

    Google Scholar 

  59. Synge AD (1947) Pollen collection by honeybees (Apis mellifera). J Anim Ecol 16:122–138

    Article  Google Scholar 

  60. Thompson HM, Maus C (2007) The relevance of sublethal effects in honey bee testing for pesticide risk assessment. Pest Manag Sci 63:1058–1061

    CAS  Article  Google Scholar 

  61. van Engelsdorp D et al (2009) Colony collapse disorder: a descriptive study. Plos One 4:17

    Google Scholar 

  62. van Engelsdorp D, Hayes J, Underwood RM, Pettis JS (2010) A survey of honey bee colony losses in the United States, fall 2008 to spring 2009. J Apic Res 49:7–14

    Article  Google Scholar 

  63. Wahl O, Ulm K (1983) Influence of pollen feeding and physiological condition on pesticide sensitivity of the honey bee Apis mellifera carnica. Oecologia 59:106–128

    Article  Google Scholar 

  64. Weast RC, Astle MJ (eds) (1982) Handbook of chemistry and physics. CRC, Boca Raton

    Google Scholar 

  65. 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 101:1743–1748

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to James E. Cresswell.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cresswell, J.E. A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20, 149–157 (2011). https://doi.org/10.1007/s10646-010-0566-0

Download citation

Keywords

  • Agrochemicals
  • Ecosystem services
  • Pollination
  • Pollution
  • Sustainability
  • Toxicology