Journal of Chemical Ecology

, Volume 42, Issue 2, pp 127–138 | Cite as

Measurements of Chlorpyrifos Levels in Forager Bees and Comparison with Levels that Disrupt Honey Bee Odor-Mediated Learning Under Laboratory Conditions

  • Elodie Urlacher
  • Coline Monchanin
  • Coraline Rivière
  • Freddie-Jeanne Richard
  • Christie Lombardi
  • Sue Michelsen-Heath
  • Kimberly J. Hageman
  • Alison R. Mercer
Article

Abstract

Chlorpyrifos is an organophosphate pesticide used around the world to protect food crops against insects and mites. Despite guidelines for chlorpyrifos usage, including precautions to protect beneficial insects, such as honeybees from spray drift, this pesticide has been detected in bees in various countries, indicating that exposure still occurs. Here, we examined chlorpyrifos levels in bees collected from 17 locations in Otago, New Zealand, and compared doses of this pesticide that cause sub-lethal effects on learning performance under laboratory conditions with amounts of chlorpyrifos detected in the bees in the field. The pesticide was detected at 17 % of the sites sampled and in 12 % of the colonies examined. Amounts detected ranged from 35 to 286 pg.bee−1, far below the LD50 of ~100 ng.bee−1. We detected no adverse effect of chlorpyrifos on aversive learning, but the formation and retrieval of appetitive olfactory memories was severely affected. Chlorpyrifos fed to bees in amounts several orders of magnitude lower than the LD50, and also lower than levels detected in bees, was found to slow appetitive learning and reduce the specificity of memory recall. As learning and memory play a central role in the behavioral ecology and communication of foraging bees, chlorpyrifos, even in sublethal doses, may threaten the success and survival of this important insect pollinator.

Keywords

Chlorpyrifos Honey bee Appetitive learning Memory specificity Field measurements 

References

  1. Al-Naggar Y, Codling G, Vogt A, Naiem E, Mona M et al (2015) Organophosphorus insecticides in honey, pollen and bees (Apis mellifera L.) and their potential hazard to bee colonies in Egypt. Ecotoxicol Environ Saf 114:1–8CrossRefPubMedGoogle Scholar
  2. Avarguès-Weber A, de Brito Sanchez MG, Giurfa M, Dyer AG (2010) Aversive reinforcement improves visual discrimination learning in free-flying honeybees. PLoS One 5:e15370CrossRefPubMedPubMedCentralGoogle Scholar
  3. Balbuena M, Tison L, Hahn M, Greggers U, Menzel R et al (2015) Effects of sub-lethal doses of glyphosate on honeybee navigation. J Exp Biol 218:2799–2805CrossRefPubMedGoogle Scholar
  4. Bates D, Maechler M, Bolker, B (2012) lme4: linear mixed-effects models using S4 classes. R package version 0.999999–0Google Scholar
  5. Blacquière T, Smagghe G, Gestel C, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973–992CrossRefPubMedPubMedCentralGoogle Scholar
  6. Celli G, Maccagnani B (2003) Honey bees as bioindicators of environmental pollution. Bull Insect 56:137–139Google Scholar
  7. Cutler GC, Purdy J, Giesy JP, Solomon KR (2014) Risk to pollinators from the use of chlorpyrifos in the United States. Rev Environ Contam Toxicol 231:219–265PubMedGoogle Scholar
  8. Davie-Martin CL, Hageman KJ, Chin Y-PP (2013) An improved screening tool for predicting volatilization of pesticides applied to soils. Environ Sci Technol 47:868–876CrossRefPubMedGoogle Scholar
  9. De Stefano LA, Stepanov II, Abramson CI (2014) The first order transfer function in the analysis of agrochemical data in honey bees (Apis mellifera L.): Proboscis extension reflex (PER) studies. Insects 5:167–198CrossRefPubMedPubMedCentralGoogle Scholar
  10. Decourtye A, Armengaud C, Renou M, Devillers J, Cluzeau S et al (2004a) Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pestic Biochem Physiol 78:83–92CrossRefGoogle Scholar
  11. Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delègue M-H (2004b) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57:410–419CrossRefPubMedGoogle Scholar
  12. Decourtye A, Devillers J, Genecque E, Le Menach K, Budzinski H et al (2005) Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch Environ Contam Toxicol 48:242–250CrossRefPubMedGoogle Scholar
  13. Dobson HEM (2006) Relationship between floral fragrance composition and type of pollinator. In: Pichersky E, Dudareva N (eds.). Biology of floral scent. CRC Press 2006, pp 147–198Google Scholar
  14. Dötterl S, Vereecken N (2010) The chemical ecology and evolution of bee–flower interactions: a review and perspectives. Can J Zool 88:668–697CrossRefGoogle Scholar
  15. EFSA (European Food Safety Authority) (2014) Conclusion on the peer review of the pesticide human health risk assessment of the active substance chlorpyrifos. EFSA J 12:3640Google Scholar
  16. El-Hassani AK, Dacher M, Gary V, Lambin M, Gauthier M et al (2008) Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Arch Environ Contam Toxicol 54:653–661. doi:10.1007/s00244-007-9071-8 CrossRefPubMedGoogle Scholar
  17. EPA (Environmental Protection Agency) (2015) Chlorpyrifos: Revised human health risk assessment. Environmental Protection Agency, USAGoogle Scholar
  18. Farina WM, Grüter C, Díaz PC (2005) Social learning of floral odours inside the honeybee hive. Proc Biol Sci 272:1923–1928CrossRefPubMedPubMedCentralGoogle Scholar
  19. Farina W, Grüter C, Acosta L, Cabe S (2006) Honeybees learn floral odors while receiving nectar from foragers within the hive. Naturwissenschaften 94:55–60CrossRefPubMedGoogle Scholar
  20. Feltham H, Park K, Goulson D (2014) Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23:317–323CrossRefPubMedGoogle Scholar
  21. Fischer J, Müller T, Spatz A-K, Greggers U, Grünewald B et al (2014) Neonicotinoids interfere with specific components of navigation in honeybees. Plos One 9:e91364CrossRefPubMedPubMedCentralGoogle Scholar
  22. Friesen LJ (1973) The search dynamics of recruited honey bee Apis mellifera. Biol Bull 144:107–131CrossRefGoogle Scholar
  23. Gauthier M, Grünewald B (2012) Neurtransmitter systems in the honeybee brain: Functions in learning and memory. In: Galizia CG, Eisenhardt D, Giurfa M (eds) Honeybee neurobiology and behavior. Springer Verlag, Heidelberg, pp 155–169CrossRefGoogle Scholar
  24. Gil M, de Marco R (2005) Olfactory learning by means of trophallaxis in Apis mellifera. J Exp Biol 208:671–680CrossRefPubMedGoogle Scholar
  25. Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105–108CrossRefPubMedPubMedCentralGoogle Scholar
  26. Guerrieri F, Schubert M, Sandoz J-CC, Giurfa M (2005) Perceptual and neural olfactory similarity in honeybees. PLoS Biol 3:e60CrossRefPubMedPubMedCentralGoogle Scholar
  27. Guez D, Zhu H, Zhang S, Srinivasan M (2010) Enhanced cholinergic transmission promotes recall in honeybees. J Insect Physiol 56:1341–1348CrossRefPubMedGoogle Scholar
  28. Henry M, Béguin M, Requier F, Rollin O, Odoux J-F et al (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336:348–350CrossRefPubMedGoogle Scholar
  29. Herbert L, Vazquez D, Arenas A, Farina W (2014) Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour. J Exp Biol 217:3457–3464CrossRefPubMedGoogle Scholar
  30. Jaeger T (2008) Categorical data analysis: away from ANOVAs (transformation or not) and towards logit mixed models. J Mem Lang 59:434–446CrossRefPubMedPubMedCentralGoogle Scholar
  31. Johnson R, Ellis M, Mullin C, Frazier M (2010) Pesticides and honey bee toxicity - USA. Apidologie 41:312–331CrossRefGoogle Scholar
  32. Katz EJ, Cortes VI, Eldefrawi ME (1997) Chlorpyrifos, parathion, and their oxons bind to and desensitize a nicotinic acetylcholine receptor: relevance to their toxicities. Toxicol Appl Pharmacol 146:227–236CrossRefPubMedGoogle Scholar
  33. Kessler S, Tiedeken E, Simcock K, Derveau S, Mitchell J et al (2015) Bees prefer foods containing neonicotinoid pesticides. Nature 521:74–76CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kosmidis I (2007) brglm: bias reduction in binary-response GLMsGoogle Scholar
  35. Lambert O, Piroux M, Puyo S, Thorin C, L’Hostis M et al (2013) Widespread occurrence of chemical residues in beehive matrices from apiaries located in different landscapes of western France. PLoS One 8:e67007CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lavin K, Hageman K (2013) Contributions of long-range and regional atmospheric transport on pesticide concentrations along a transect crossing a mountain divide. Environ Sci Technol 17:1390–1398Google Scholar
  37. Lavin K, Hageman K, Marx S, Dillingham P, Kamber B (2012) Using trace elements in particulate matter to identify the sources of semivolatile organic contaminants in air at an alpine site. Environ Sci Technol 46:268–276CrossRefPubMedGoogle Scholar
  38. Lunden J, Mayer D, Johansen C, Shanks C, Eves J (1986) Effects of chlorpyrifos insecticide on pollinators. Am Bee J 126:441–444Google Scholar
  39. Lusebrink I, Girling RD, Farthing E, Newman TA, Jackson CW et al (2015) The effects of diesel exhaust pollution on floral volatiles and the consequences for honey bee olfaction. J Chem Ecol 41:904–912CrossRefPubMedGoogle Scholar
  40. Mackay D, Giesy J, Solomon K (2014) Fate in the environment and long-range atmospheric transport of the organophosphorus insecticide, chlorpyrifos and its oxon. Rev Environ Contam Toxicol 231:35–76PubMedGoogle Scholar
  41. Matsumoto Y, Menzel R, Sandoz J-CC, Giurfa M (2012) Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: a step toward standardized procedures. J Neurosci Methods 211:159–167CrossRefPubMedGoogle Scholar
  42. Ministry for Primary Industries (2012) Food residue surveillance programme 2011–2012 quarterly report. ISBN No: 978-0-478-40047-2Google Scholar
  43. Morzycka B (2002) Simple method for the determination of trace levels of pesticides in honeybees using matrix solid-phase dispersion and gas chromatography. J Chromatogr A 982:267–273CrossRefPubMedGoogle Scholar
  44. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R et al (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One 5:e9754CrossRefPubMedPubMedCentralGoogle Scholar
  45. NZEPA (New Zealand Environmental Protection Authority) (2013) Application for the reassessment of a group of hazardous substances under Section 63 of the Hazardous Substances and New Organisms Act 1996Google Scholar
  46. Palmer MJ, Moffat C, Saranzewa N, Harvey J, Wright GA et al (2013) Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nat Commun 4:1634CrossRefPubMedPubMedCentralGoogle Scholar
  47. Pareja L, Colazzo M, Pérez-Parada A, Niell S, Carrasco-Letelier L et al (2011) Detection of pesticides in active and depopulated beehives in Uruguay. Int J Environ Res Public Health 8:3844–3858CrossRefPubMedPubMedCentralGoogle Scholar
  48. Perry C, Søvik E, Myerscough M, Barron A (2015) Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proc Natl Acad Sci U S A 112:3427–3432CrossRefPubMedPubMedCentralGoogle Scholar
  49. Pohanka M (2011) Cholinesterases, a target of pharmacology and toxicology. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 155:219–223CrossRefPubMedGoogle Scholar
  50. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  51. Racke KD (1993) Environmental fate of chlorpyrifos. Rev Environ Contam Toxicol 131:1–150PubMedGoogle Scholar
  52. Raine N, Chittka L (2008) The correlation of learning speed and natural foraging success in bumble-bees. Proc R Soc B 275:803–808CrossRefPubMedPubMedCentralGoogle Scholar
  53. Reinhard J, Srinivasan MV (2009) The role of scents in honey bee foraging and recruitment. In: Jarau S, Hrncir M (eds) Food exploitation by social insects: ecological, behavioral, and theoretical approaches 1. CRC Press/Taylor & Francis Group, Boca Raton, pp 65–182Google Scholar
  54. Roussel E, Carcaud J, Sandoz J-C, Giurfa M (2009) Reappraising social insect behavior through aversive responsiveness and learning. PLoS One 4:e4197CrossRefPubMedPubMedCentralGoogle Scholar
  55. Rundlöf M, Andersson G, Bommarco R, Fries I, Hederström V et al (2015) Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521:77–80CrossRefPubMedGoogle Scholar
  56. Sanchez-Bayo F, Goka K (2014) Pesticide residues and bees—a risk assessment. PLoS One 9:e94482CrossRefPubMedPubMedCentralGoogle Scholar
  57. Scheiner R, Erber J, Page RE (1999) Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.). J Comp Physiol A 185:1–10CrossRefPubMedGoogle Scholar
  58. Scheiner R, Barnert M, Erber J (2003) Variation in water and sucrose responsiveness during the foraging season affects proboscis extension learning in honey bees. Apidologie 34:67–72CrossRefGoogle Scholar
  59. Shahpoury P, Hageman K, Matthaei C, Magbanua F (2013) Chlorinated pesticides in stream sediments from organic, integrated and conventional farms. Environ Pollut 181:219–225CrossRefPubMedGoogle Scholar
  60. Shapira M, Thompson C, Soreq H, Robinson G (2001) Changes in neuronal acetylcholinesterase gene expression and division of labor in honey bee colonies. J Mol Neurosci 17:1–12CrossRefPubMedGoogle Scholar
  61. Solomon KR, Williams WM, Mackay D, Purdy J, Giddings JM et al (2014) Properties and uses of chlorpyrifos in the United States. Rev Environ Contam Toxicol 231:13–34PubMedGoogle Scholar
  62. Stanley DA, Garratt MP, Wickens JB, Wickens VJ, Potts SG et al (2015) Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528:548–550CrossRefPubMedGoogle Scholar
  63. Stevenson J (1978) The acute toxicity of unformolated pesticides to worker honey bees (Apis mellifera L.). Plant Pathol 27:38–40CrossRefGoogle Scholar
  64. Tan K, Chen W, Dong S, Liu X, Wang Y et al (2014) Imidacloprid alters foraging and decreases bee avoidance of predators. PLoS One 9:e102725CrossRefPubMedPubMedCentralGoogle Scholar
  65. van der Sluijs J, Simon-Delso N, Goulson D, Maxim L, Bonmatin J-M et al (2013) Neonicotinoids, bee disorders and the sustainability of pollinator services. Curr Opin Environ Sustain 5:293–305CrossRefGoogle Scholar
  66. Vergoz V, Roussel E, Sandoz J-C, Giurfa M (2007) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS One 2:e288CrossRefPubMedPubMedCentralGoogle Scholar
  67. von Frisch K (1993) The dance language and orientation of bees. Harvard University Press, Cambridge, MACrossRefGoogle Scholar
  68. Watts M (2013) Chlorpyrifos. Pesticide action network Asia and the pacific. Penang, MalaysiaGoogle Scholar
  69. Weick J, Thorn R (2002) Effects of acute sublethal exposure to coumaphos or diazinon on acquisition and discrimination of odor stimuli in the honey bee (Hymenoptera: Apidae). J Econ Entomol 95:227–236CrossRefPubMedGoogle Scholar
  70. Wenner AM, Wells PH, Johnson DL (1969) Honey bee recruitment to food sources: olfaction or language? Science 164:84–86CrossRefPubMedGoogle Scholar
  71. Williamson SM, Wright GA (2013) Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol 216:1799–1807CrossRefPubMedPubMedCentralGoogle Scholar
  72. Williamson S, Moffat C, Gomersall M, Saranzewa N, Connolly C et al (2013) Exposure to acetylcholinesterase inhibitors alters the physiology and motor function of honeybees. Front Physiol 4:13CrossRefPubMedPubMedCentralGoogle Scholar
  73. Wright GA, Schiestl FP (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct Ecol 23:841–851CrossRefGoogle Scholar
  74. Yang E, Chuang Y, Chen Y, Chang L (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 107:1743–1748CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Elodie Urlacher
    • 1
  • Coline Monchanin
    • 1
  • Coraline Rivière
    • 1
  • Freddie-Jeanne Richard
    • 2
  • Christie Lombardi
    • 3
  • Sue Michelsen-Heath
    • 1
  • Kimberly J. Hageman
    • 3
  • Alison R. Mercer
    • 1
  1. 1.University of Otago, Department of ZoologyDunedinNew Zealand
  2. 2.Laboratoire Ecologie et Biologie des intéractions, UMR CNRS 7267, Team Ecologie Evolution SymbioseUniversity of PoitiersPoitiers Cedex 9France
  3. 3.Department of ChemistryUniversity of OtagoDunedinNew Zealand

Personalised recommendations