, Volume 24, Issue 9, pp 2017–2025 | Cite as

Sublethal imidacloprid effects on honey bee flower choices when foraging

  • Ahmed Karahan
  • Ibrahim Çakmak
  • John M. Hranitz
  • Ismail Karaca
  • Harrington Wells


Neonicotinoids, systemic neuro-active pesticides similar to nicotine, are widely used in agriculture and are being investigated for a role in honey bee colony losses. We examined one neonicotinoid pesticide, imidacloprid, for its effects on the foraging behavior of free-flying honey bees (Apis mellifera anatoliaca) visiting artificial blue and white flowers. Imidacloprid doses, ranging from 1/5 to 1/50 of the reported LD50, were fed to bees orally. The study consisted of three experimental parts performed sequentially without interruption. In Part 1, both flower colors contained a 4 μL 1 M sucrose solution reward. Part 2 offered bees 4 μL of 1.5 M sucrose solution in blue flowers and a 4 μL 0.5 M sucrose solution reward in white flowers. In Part 3 we reversed the sugar solution rewards, while keeping the flower color consistent. Each experiment began 30 min after administration of the pesticide. We recorded the percentage of experimental bees that returned to forage after treatment. We also recorded the visitation rate, number of flowers visited, and floral reward choices of the bees that foraged after treatment. The forager return rate declined linearly with increasing imidacloprid dose. The number of foraging trips by returning bees was also affected adversely. However, flower fidelity was not affected by imidacloprid dose. Foragers visited both blue and white flowers extensively in Part 1, and showed greater fidelity for the flower color offering the higher sugar solution reward in Parts 2 and 3. Although larger samples sizes are needed, our study suggests that imidacloprid may not affect the ability to select the higher nectar reward when rewards were reversed. We observed acute, mild effects on foraging by honey bees, so mild that storage of imidacloprid tainted-honey is very plausible and likely to be found in honey bee colonies.


Apis mellifera Foraging behavior Neonicotinoids 


  1. Abramson CI, Wells PH, Wenner A, Wells H (2012) Odor, learning and behavior. In: Florio RM (ed) Bees, biology, threats and colonies. Nova Science Publishers Inc, New York, pp 125–145Google Scholar
  2. Abramson CI, Cakmak I, Duell ME, Bates-Albers LM, Zuniga EM, Pendegraft L, Barnett A, Cowo CL, Warren JJ, Albritton-Ford AC, Barthell JF, Hranitz JM, Wells H (2013) Feature-positive and feature-negative learning in honey bees. J Exp Biol 216:224–229CrossRefGoogle Scholar
  3. Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:915–918CrossRefGoogle Scholar
  4. Aizen MA, Garibaldi LA, Cunningham SA, Klein AM (2009) How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann Bot 103:1579–1588CrossRefGoogle Scholar
  5. Aliouane Y, el Hassani AK, Gary V, Armengaud C, Lambin M, Gauthier M (2009) Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior. Environ Toxicol Chem 28:113–122CrossRefGoogle Scholar
  6. Allsopp MH, de Lange WJ, Veldtman R (2008) Valuing insect pollination services with cost of replacement. PLoS One. doi:10.1371/journal.pone.0003128 Google Scholar
  7. Amaya-Marquez M, Hill PS, Abramson CI, Wells H (2014) Honey bee location- and time-linked memory use in novel foraging situations: floral color dependency. Insects 5(1):243–269. doi:10.3390/insects5010243 CrossRefGoogle Scholar
  8. Arena M, Sgolastra F (2014) A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23:324–334CrossRefGoogle Scholar
  9. Avarques-Weber A, Giurfa M (2013) Conceptual learning by miniature brains. Proc Biol Sci 280:20131907CrossRefGoogle Scholar
  10. Blacquière T, Smagghe G, Vangestel CAM, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973–992. doi:10.1007/s10646-012-0863-x CrossRefGoogle Scholar
  11. Bonmatin JM, Marchand PA, Charvet R, Moineau I, Bengsh ER, Colin ME (2005) Quantification of imidacloprid uptake in maize crops. J Agric Food Chem 53:5336–5341CrossRefGoogle Scholar
  12. Breeze TD, Bailey AP, Balcombe KG, Potts SG (2011) Pollination services in the UK: how important are honeybees? Agric Ecosyst Environ 142:137–143CrossRefGoogle Scholar
  13. Breeze TD, Vaissiere BE, Bommarco R, Petanidou T, Seraphides N, Kozak L, Scheper J, Biesmeijer JC, Kleijn D, Gyldenkaerne S, Moretti M, Holzschuh A, Steffan-Dewenter I, Stout JC, Paertel M, Zobel M, Potts SG (2014) Agricultural policies exacerbate honeybee pollination service supply-demand mismatches across Europe. PLoS One. doi:10.1371/journal.pone.0082996 Google Scholar
  14. Brittain CA, Vighi M, Bommarco R, Settele J, Potts SG (2010) Impacts of a pesticide on pollinator species richness at different spatial scales. Basic Appl Ecol 11:106–115CrossRefGoogle Scholar
  15. Bryden J, Gill RJ, Mitton RAA, Raine NE, Jansen VAA (2013) Chronic sublethal stress causes bee colony failure. Ecol Lett 16:1463–1469CrossRefGoogle Scholar
  16. Cakmak I, Sanderson C, Blocker TD, Pham LL, Checotah S, Norman AA, Harader-Pate BK, Reidenbaugh T, Nenchev P, Barthell JF, Well H (2009) Different solutions by bees to a foraging problem. Anim Behav 77(5):1273–1280CrossRefGoogle Scholar
  17. Calderone NW (2012) Insect pollinated crops, insect pollinators and US Agriculture: trend analysis of aggregate data for the period 1992–2009. PLoS One. doi:10.1371/journal.pone.0037235 Google Scholar
  18. Carreck N, Ratnieks F (2014) The dose makes the poison: have “field realistic” rates of exposure of bees to neonicitinoid insecticides been overestimated in laboratory studies? J Apic Res 53(5):607–614CrossRefGoogle Scholar
  19. 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 47:387–395CrossRefGoogle Scholar
  20. Cressey D (2013) Europe debates risk to bees. Nature 496:408CrossRefGoogle Scholar
  21. Cresswell JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20:149–157CrossRefGoogle Scholar
  22. Cresswell JE, Desneux N, vanEngelsdorp D (2012a) Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill’s epidemiological criteria. Pest Manag Sci 68:819–827CrossRefGoogle Scholar
  23. Cresswell JE, Page CJ, Uygun MB, Holmbergh M, Li Y, Wheeler JG, Laycock I, Pook CJ, de Ibarra NH, Smirnoff N, Tyler CR (2012b) Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology 115:365–371CrossRefGoogle Scholar
  24. Dag A (2009) Interaction between pollinators and crop plants: the Israeli experience. Isr J Plant Sci 57:231–242CrossRefGoogle Scholar
  25. de Lange WJ, Veldtman R, Allsopp MH (2013) Valuation of pollinator forage services provided by Eucalyptus cladocalyx. J Environ Manag 125:12–18CrossRefGoogle Scholar
  26. 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 59:269–278CrossRefGoogle Scholar
  27. Decourtye A, Devillers J, Aupinel P, Brun F, Bagnis C, Fourrier J, Gauthier M (2011) Honeybee tracking with microchips: a new methodology to measure the effects of pesticides. Ecotoxicology 20(2):429–437CrossRefGoogle Scholar
  28. DeGrandi-Hoffman G, Sammataro D, Simonds R (2012) Are agrochemicals present in high fructose corn syrup fed to honey bees (Apis mellifera L.)? J Apic Res 51:371–372CrossRefGoogle Scholar
  29. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106CrossRefGoogle Scholar
  30. Devillers J, Decourtye A, Budzinski H, Pham-Delegue MH, Cluzeau S, Maurin G (2003) Comparative toxicity and hazards of pesticides to Apis and non-Apis bees: a chemometrical study. SAR QSAR Environ Res 14:389–403CrossRefGoogle Scholar
  31. 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:e0118748CrossRefGoogle Scholar
  32. Feltham H, Park K, Goulson D (2014) Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23:317–323CrossRefGoogle Scholar
  33. Fischer J, Muller T, Spatz AK, Greggers U, Grunewald B, Menzel R (2014) Neonicotinoids interfere with specific components of navigation in honeybees. PLoS One. doi:10.1371/journal.pone.0091364 Google Scholar
  34. Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105–119CrossRefGoogle Scholar
  35. Girolami V, Mazzon L, Squartini A, Mori N, Marzaro M, Di Bernardo A, Greatti M, Giorio C, Tapparo A (2009) Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: a novel way of intoxication for bees. J Econ Entomol 102:1808–1815CrossRefGoogle Scholar
  36. Goulson D (2013) Review: an overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50:977–987CrossRefGoogle Scholar
  37. Han P, Niu CY, Lei CL, Cui JJ, Desneux N (2010) Use of an innovative T-tube maze assay and the proboscis extension response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee Apis mellifera L. Ecotoxicology 19:1612–1619CrossRefGoogle Scholar
  38. Hill PSM, Wells PH, Wells H (1997) Spontaneous flower constancy and learning in honey bees as a function of colour. Anim Behav 54:615–627CrossRefGoogle Scholar
  39. 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(5):371–378CrossRefGoogle Scholar
  40. Johnson DL, Wenner AM (1966) A relationship between conditioning and communication in honey bees. Anim Behav 14:261–265CrossRefGoogle Scholar
  41. Kandemir I, Kence M, Kence A (2000) Genetic and morphometric variation in honey bee (Apis mellifera L.) population of Turkey. Apidology 31:343–356CrossRefGoogle Scholar
  42. Kearns C, Inouye D, Waser N (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Syst Evol 29:83–112CrossRefGoogle Scholar
  43. Laycock I, Cotterell KC, O’shea-Wheller TA, Cresswell JE (2014) Effects of the neonicotinoid pesticide thiamethoxam at field-realistic levels on microcolonies of Bombus terrestris worker bumble bees. Ecotoxicol Environ Saf 100:153–158CrossRefGoogle Scholar
  44. Lu C, Warchol KM, Callahan RA (2012) In situ replication of honey bee colony collapse disorder. Bull Insectol 65:99–106Google Scholar
  45. Lu C, Warchol KM, Callahan RA (2014) Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder. Bull Insectol 67:125–130Google Scholar
  46. Menzel R (2001) Searching for he memory trace in mini-brain the honeybee. Learn Mem 8:53–62CrossRefGoogle Scholar
  47. Michener CD (2007) The bees of the world, 2nd edn. The John Hopkins University Press, BaltimoreGoogle Scholar
  48. Potts SG, Petanidou T, Roberts S, O’Toole C, Hulbert A, Willmer P (2006) Plant-pollinator biodiversity and pollination services in a complex Mediterranean landscape. Biol Conserv 129:519–529CrossRefGoogle Scholar
  49. Ramirez-Romero R, Chaufaux J, Pham-Delegue MH (2005) Effects of Cry1Ab prototoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee, Apis mellifera: a comparative approach. Apidologie 36:601–611CrossRefGoogle Scholar
  50. Ramirez-Romero R, Desneux N, Decourtye A, Chaffiol A, Pham-Delegue MH (2008) Does Cry1Ab protein affect learning performances of the honeybee Apis mellifera L. (Hymenoptera, Apidae)? Ecotoxicol Environ Saf 70:327–333CrossRefGoogle Scholar
  51. Rondeau G, Sanchez-Bayo F, Tennekes HA, Decourtye A, Ramırez-Romero R, Desneux N (2013) Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites. Sci Rep 4:5566Google Scholar
  52. 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 36:71–83CrossRefGoogle Scholar
  53. Ruttner F (1988) Biogeography and taxonomy of honey-bees. Springer, BerlinGoogle Scholar
  54. Sall F, Lehman A (1996) JMP IN; SAS institute, Inc. Ducksberry Press, BelmontGoogle Scholar
  55. Sanderson CE, Cook P, Hill PSM, Orozco BS, Abramson CI, Wells H (2013) Nectar quality perception by honey bees (Apis mellifera ligustica). J Comp Psychol 127:341–351CrossRefGoogle Scholar
  56. Sandrock C, Tanadini M, Tanadini LG, Fauser-Misslin A, Potts SG, Neumann P (2014) Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure. PLoS One 9:e103592CrossRefGoogle Scholar
  57. Scholer J, Krischik V (2014) Chronic exposure of imidacloprid and clothianidin reduce queen survival, foraging, and nectar storing in colonies of Bombus impatiens. PLoS One. doi:10.1371/journal.pone.0091573 Google Scholar
  58. Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, CambridgeGoogle Scholar
  59. Sirinivasan M (2010) Honey bees as a model for vision, perception, and cognition. Annu Rev Entomol 55:267–284CrossRefGoogle Scholar
  60. Sokal RR, Rohlf RJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W. H. Freeman and Co, New YorkGoogle Scholar
  61. Stoner KA, Eitzer BD (2012) Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS One. doi:10.1371/journal.pone.0039114 Google Scholar
  62. Von Frisch K (1967) The dance language and orientation of bees. Belknap Press of Harvard University, CambridgeGoogle Scholar
  63. Wells H, Wells PH (1986) Optimal diet, minimal uncertainty and individual constancy in the foraging of honey bees, Apis mellifera. J Anim Ecol 55:881–891CrossRefGoogle Scholar
  64. Wenner AM (1989) Concept-centered versus organism-centered biology. Am Zool 29:1177–1197CrossRefGoogle Scholar
  65. Wenner AM, Wells PH (1990) Anatomy of a controversy: the question of a “language” among bees. Columbia University Press, New YorkGoogle Scholar
  66. Wenner AM, Wells PH, Johnson DL (1969) Honeybee recruitment to food sources: olfaction or language? Science 164:84–86CrossRefGoogle Scholar
  67. Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336:351–352CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Ahmed Karahan
    • 1
  • Ibrahim Çakmak
    • 2
  • John M. Hranitz
    • 3
  • Ismail Karaca
    • 1
  • Harrington Wells
    • 4
  1. 1.Department of Plant ProtectionSuleyman Demirel UniversityIspartaRepublic of Turkey
  2. 2.Beekeeping Development Application and Research Center, MKP MYOUludag UniversityBursaRepublic of Turkey
  3. 3.Department of Biological and Allied Health SciencesBloomsburg UniversityBloomsburgUSA
  4. 4.Department of BiologyUniversity of TulsaTulsaUSA

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