Letter

Bees prefer foods containing neonicotinoid pesticides

Received:
Accepted:
Published online:

Abstract

The impact of neonicotinoid insecticides on insect pollinators is highly controversial. Sublethal concentrations alter the behaviour of social bees and reduce survival of entire colonies1,2,3. However, critics argue that the reported negative effects only arise from neonicotinoid concentrations that are greater than those found in the nectar and pollen of pesticide-treated plants4. Furthermore, it has been suggested that bees could choose to forage on other available flowers and hence avoid or dilute exposure4,5. Here, using a two-choice feeding assay, we show that the honeybee, Apis mellifera, and the buff-tailed bumblebee, Bombus terrestris, do not avoid nectar-relevant concentrations of three of the most commonly used neonicotinoids, imidacloprid (IMD), thiamethoxam (TMX), and clothianidin (CLO), in food. Moreover, bees of both species prefer to eat more of sucrose solutions laced with IMD or TMX than sucrose alone. Stimulation with IMD, TMX and CLO neither elicited spiking responses from gustatory neurons in the bees’ mouthparts, nor inhibited the responses of sucrose-sensitive neurons. Our data indicate that bees cannot taste neonicotinoids and are not repelled by them. Instead, bees preferred solutions containing IMD or TMX, even though the consumption of these pesticides caused them to eat less food overall. This work shows that bees cannot control their exposure to neonicotinoids in food and implies that treating flowering crops with IMD and TMX presents a sizeable hazard to foraging bees.

  • Subscribe to Nature for full access:

    $199

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    & Ecotoxicity of neonicotinoid insecticides to bees. Adv. Exp. Med. Biol. 683, 85–95 (2010)

  2. 2.

    , & Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108 (2012)

  3. 3.

    , , & Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352 (2012)

  4. 4.

    Department for Environment Food & Rural Affairs. An assessment of key evidence about neonicotinoids and bees. (2013)

  5. 5.

    et al. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. Biol. Sci. 281, 20140558 (2014)

  6. 6.

    & Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. J. Agric. Food Chem. 60, 4449–4456 (2012)

  7. 7.

    , , & Risk posed to honeybees (Apis mellifera l, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag. Sci. 57, 225–238 (2001)

  8. 8.

    , , , & Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol. Environ. Saf. 57, 410–419 (2004)

  9. 9.

    et al. Neonicotinoids interfere with specific components of navigation in honeybees. PLoS ONE 9, e91364 (2014)

  10. 10.

    et al. A common pesticide decreases foraging success and survival in honey bees. Science 336, 348–350 (2012)

  11. 11.

    , , & Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21, 1937–1945 (2012); Corrected. 21, 1946 (2012)

  12. 12.

    , & Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology 23, 1409–1418 (2014)

  13. 13.

    & The dose makes the poison: have “field realistic” rates of exposure of bees to neonicotinoid insecticides been overestimated in laboratory studies?. J. Apic. Res. 53, 607–614 (2014)

  14. 14.

    & The neonicotinoid insecticide imidacloprid repels pollinating flies and beetles at field-realistic concentrations. PLoS ONE 8, e54819 (2013)

  15. 15.

    , , , & Neonicotinoids and bumblebees (Bombus terrestris): effects on nectar consumption in individual workers. Pest Manag. Sci.. (2014)

  16. 16.

    , , & Bumblebees are not deterred by ecologically relevant concentrations of nectar toxins. J. Exp. Biol. 217, 1620–1625 (2014)

  17. 17.

    et al. Parallel reinforcement pathways for conditioned food aversions in the honeybee. Curr. Biol. 20, 2234–2240 (2010)

  18. 18.

    The Hungry Fly (Harvard Univ. Press, 1976)

  19. 19.

    , & Sensory coding for feeding deterrence in the grasshopper Schistocerca americana. J. Exp. Biol. 158, 241–259 (1991)

  20. 20.

    , , , & The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258–272 (2011)

  21. 21.

    , , & Electrophysiological and behavioural characterization of gustatory responses to antennal 'bitter' taste in honeybees. Eur. J. Neurosci. 22, 3161–3170 (2005)

  22. 22.

    & The effect of alkaloids on sugar receptors and the feeding-behavior of the blowfly. Physiol. Entomol. 14, 127–136 (1989)

  23. 23.

    et al. The tarsal taste of honey bees: behavioral and electrophysiological analyses. Front. Behav. Neurosci. 8, 25 (2014)

  24. 24.

    , , & Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectars. J. Chem. Ecol. 31, 2791–2804 (2005)

  25. 25.

    , , , & Neonicotinoid insecticides display partial and super agonist actions on native insect nicotinic acetylcholine receptors. J. Neurochem. 99, 608–615 (2006)

  26. 26.

    , & Expression patterns of nicotinic subunits α2, α7, α8, and β1 affect the kinetics and pharmacology of ach-induced currents in adult bee olfactory neuropiles. J. Neurophysiol. 106, 1604–1613 (2011)

  27. 27.

    et al. Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nat. Commun. 4, 1634 (2013)

  28. 28.

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

  29. 29.

    & Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J. Exp. Biol. 216, 1799–1807 (2013)

  30. 30.

    , & Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23, 317–323 (2014)

  31. 31.

    et al. Nutritional balance of essential amino acids and carbohydrates of the adult worker honeybee depends on age. Amino Acids 46, 1449–1458 (2014)

  32. 32.

    , , & Classical-conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97, 107–119 (1983)

  33. 33.

    & Ultrastructure of the contact chemoreceptors of Apis mellifera L. (Hymenoptera: Apidae). Int. J. Insect Morphol. Embryol. 5, 301–315 (1976)

  34. 34.

    , & Physiology of a primary chemoreceptor unit. Science 122, 417–418 (1955)

  35. 35.

    & Un-filtered recordings from insect taste sensilla. Entomol. Exp. Appl. 80, 113–115 (1996)

  36. 36.

    , , & Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J. Neurobiol. 61, 333–342 (2004)

  37. 37.

    , , & Peripheral coding of bitter taste in Drosophila. J. Neurobiol. 56, 139–152 (2003)

  38. 38.

    et al. Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. J. Apic. Sci. 56, 115–134 (2012)

  39. 39.

    & Using a hazard quotient to evaluate pesticide residues detected in pollen trapped from honey bees (Apis mellifera) in Connecticut. PLoS ONE 8, e77550 (2013)

  40. 40.

    et al. Determination of exposure levels of honey bees foraging on flowers of mature citrus trees previously treated with imidacloprid. Pest Manag. Sci. 70, 470–482 (2013)

  41. 41.

    , & Assessing insecticide hazard to bumble bees foraging on flowering weeds in treated lawns. PLoS ONE 8, e66375 (2013)

  42. 42.

    , , , & A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam. PLoS ONE 8, e66375 (2013)

  43. 43.

    The Food and Environment Research Agency. Effects of Neonicotinoid Seed Treatments on Bumble Bee Colonies Under Field Conditions (fera, 2013)

Download references

Acknowledgements

We thank M. Thompson for beekeeping, A. Radcliffe for help with experiments, and C. Rowe, S. Waddell, M. Palmer and N. Millar for comments. This work was funded jointly by a grant from the BBSRC, NERC, the Wellcome Trust, Defra, and the Scottish Government under the Insect Pollinators Initiative (BB/I000143/1) to G.A.W., a Leverhulme Trust research project grant (RPG-2012-708) to G.A.W., a Science Foundation Ireland grant (10/RFP/EOB2842) to J.C.S., a US National Science Foundation Graduate Research Fellowship awarded to E.J.T. (Grant No. 2010097514), and an Irish Research Council's EMBARK Postgraduate Scholarship Scheme grant (RS/2010/2147) to E.J.T.

Author information

Author notes

    • Sébastien C. Kessler
    •  & Erin Jo Tiedeken

    These authors contributed equally to this work.

Affiliations

  1. Institute of Neuroscience, Newcastle University, Newcastle upon Tyne NE2 4HH, UK

    • Sébastien C. Kessler
    • , Kerry L. Simcock
    • , Samantha Softley
    •  & Geraldine A. Wright
  2. Botany Department, Trinity College Dublin, Dublin 2, Ireland

    • Erin Jo Tiedeken
    •  & Jane C. Stout
  3. School of Biology, Newcastle University, Newcastle upon Tyne NE1 7RU, UK

    • Sophie Derveau
  4. Centre for Neural Circuits and Behaviour, Tinsley Building, University of Oxford, Oxford OX1 3SR, UK

    • Jessica Mitchell
  5. Institute of Neuroscience, Newcastle University, Newcastle upon Tyne NE2 4HH, UK

    • Amy Radcliffe

Authors

  1. Search for Sébastien C. Kessler in:

  2. Search for Erin Jo Tiedeken in:

  3. Search for Kerry L. Simcock in:

  4. Search for Sophie Derveau in:

  5. Search for Jessica Mitchell in:

  6. Search for Samantha Softley in:

  7. Search for Amy Radcliffe in:

  8. Search for Jane C. Stout in:

  9. Search for Geraldine A. Wright in:

Contributions

S.C.K. performed the ephys experiments, spike-sorted the ephys data and wrote portions of the manuscript, E.J.T., K.L.S., S.D., J.M., S.S. and A.R. performed the choice experiments, E.J.T. and J.C.S. wrote portions of and edited the manuscript, and G.A.W. designed the experiments, analysed all data, and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Geraldine A. Wright.

Extended data

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.