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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Change history
17 February 2016
A Correction to this paper has been published: https://doi.org/10.1038/nature17177
References
Decourtye, A. & Devillers, J. Ecotoxicity of neonicotinoid insecticides to bees. Adv. Exp. Med. Biol. 683, 85–95 (2010)
Gill, R. J., Ramos-Rodriguez, O. & Raine, N. E. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108 (2012)
Whitehorn, P. R., O'Connor, S., Wackers, F. L. & Goulson, D. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352 (2012)
Department for Environment Food & Rural Affairs. An assessment of key evidence about neonicotinoids and bees. https://www.gov.uk/government/publications/an-assessment-of-key-evidence-about-neonicotinoids-and-bees (2013)
Godfray, H. C. et al. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. Biol. Sci. 281, 20140558 (2014)
Dively, G. P. & Kamel, A. Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. J. Agric. Food Chem. 60, 4449–4456 (2012)
Schmuck, R., Schoning, R., Stork, A. & Schramel, O. Risk posed to honeybees (Apis mellifera l, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag. Sci. 57, 225–238 (2001)
Decourtye, A., Devillers, J., Cluzeau, S., Charreton, M. & Pham-Delegue, M. H. Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol. Environ. Saf. 57, 410–419 (2004)
Fischer, J. et al. Neonicotinoids interfere with specific components of navigation in honeybees. PLoS ONE 9, e91364 (2014)
Henry, M. et al. A common pesticide decreases foraging success and survival in honey bees. Science 336, 348–350 (2012)
Laycock, I., Lenthall, K. M., Barratt, A. T. & Cresswell, J. E. Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21, 1937–1945 (2012); Corrected. 21, 1946 (2012)
Williamson, S. M., Willis, S. J. & Wright, G. A. Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology 23, 1409–1418 (2014)
Carreck, N. L. & Ratnieks, F. L. 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)
Easton, A. H. & Goulson, D. The neonicotinoid insecticide imidacloprid repels pollinating flies and beetles at field-realistic concentrations. PLoS ONE 8, e54819 (2013)
Thompson, H. M., Wilkins, S., Harkin, S., Milnera, S. & Walters, K. F. B. Neonicotinoids and bumblebees (Bombus terrestris): effects on nectar consumption in individual workers. Pest Manag. Sci.. http://dx.doi.org/10.1002/ps.3868 (2014)
Tiedeken, E. J., Stout, J. C., Stevenson, P. C. & Wright, G. A. Bumblebees are not deterred by ecologically relevant concentrations of nectar toxins. J. Exp. Biol. 217, 1620–1625 (2014)
Wright, G. A. et al. Parallel reinforcement pathways for conditioned food aversions in the honeybee. Curr. Biol. 20, 2234–2240 (2010)
Dethier, V. G. The Hungry Fly (Harvard Univ. Press, 1976)
Chapman, R. F., Ascolichristensen, A. & White, P. R. Sensory coding for feeding deterrence in the grasshopper Schistocerca americana. J. Exp. Biol. 158, 241–259 (1991)
Weiss, L. A., Dahanukar, A., Kwon, J. Y., Banerjee, D. & Carlson, J. R. The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258–272 (2011)
de Brito Sanchez, M. G., Giurfa, M., Mota, T. R. D. & Gauthier, M. Electrophysiological and behavioural characterization of gustatory responses to antennal 'bitter' taste in honeybees. Eur. J. Neurosci. 22, 3161–3170 (2005)
Dethier, V. G. & Bowdan, E. The effect of alkaloids on sugar receptors and the feeding-behavior of the blowfly. Physiol. Entomol. 14, 127–136 (1989)
Sanchez, M. G. D. et al. The tarsal taste of honey bees: behavioral and electrophysiological analyses. Front. Behav. Neurosci. 8, 25 (2014)
Singaravelan, N., Nee'man, G., Inbar, M. & Izhaki, I. Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectars. J. Chem. Ecol. 31, 2791–2804 (2005)
Brown, L. A., Ihara, M., Buckingham, S. D., Matsuda, K. & Sattelle, D. B. Neonicotinoid insecticides display partial and super agonist actions on native insect nicotinic acetylcholine receptors. J. Neurochem. 99, 608–615 (2006)
Dupuis, J. P., Gauthier, M. & Raymond-Delpech, V. 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)
Palmer, M. J. et al. Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nat. Commun. 4, 1634 (2013)
Decourtye, A. et al. Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pestic. Biochem. Physiol. 78, 83–92 (2004)
Williamson, S. M. & Wright, G. A. Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J. Exp. Biol. 216, 1799–1807 (2013)
Feltham, H., Park, K. & Goulson, D. Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23, 317–323 (2014)
Paoli, P. P. et al. Nutritional balance of essential amino acids and carbohydrates of the adult worker honeybee depends on age. Amino Acids 46, 1449–1458 (2014)
Bitterman, M. E., Menzel, R., Fietz, A. & Schafer, S. Classical-conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97, 107–119 (1983)
Whitehead, A. T. & Larson, J. R. Ultrastructure of the contact chemoreceptors of Apis mellifera L. (Hymenoptera: Apidae). Int. J. Insect Morphol. Embryol. 5, 301–315 (1976)
Hodgson, E. S., Lettvin, J. Y. & Roeder, K. D. Physiology of a primary chemoreceptor unit. Science 122, 417–418 (1955)
Marion-Poll, F. & van der Pers, J. Un-filtered recordings from insect taste sensilla. Entomol. Exp. Appl. 80, 113–115 (1996)
Hiroi, M., Meunier, N., Marion-Poll, F. & Tanimura, T. Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J. Neurobiol. 61, 333–342 (2004)
Meunier, N., Marion-Poll, F., Rospars, J. P. & Tanimura, T. Peripheral coding of bitter taste in Drosophila. J. Neurobiol. 56, 139–152 (2003)
Pohorecka, K. 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)
Stoner, K. A. & Eitzer, B. D. Using a hazard quotient to evaluate pesticide residues detected in pollen trapped from honey bees (Apis mellifera) in Connecticut. PLoS ONE 8, e77550 (2013)
Byrne, F. V. 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)
Larson, J. L., Redmond, C. T. & Potter, D. A. Assessing insecticide hazard to bumble bees foraging on flowering weeds in treated lawns. PLoS ONE 8, e66375 (2013)
Pilling, E., Campbell, P., Coulson, M., Ruddle, N. & Tornier, I. 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)
The Food and Environment Research Agency. Effects of Neonicotinoid Seed Treatments on Bumble Bee Colonies Under Field Conditionshttp://fera.co.uk/ccss/documents/defraBumbleBeeReportPS2371V4a.pdf (fera, 2013)
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
Authors and Affiliations
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.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Extended data figures and tables
Extended Data Figure 1 The proportion of bees surviving after 24 h in the two-choice assay.
Data from Fig. 1. a, Bumblebees given a choice between sucrose and sucrose laced with 1,000 nM TMX or CLO were less likely to survive after 24 h (lreg: IMD: χ42 = 4.36, P = 0.359; TMX: χ42 = 62.3, P < 0.001; CLO: χ42 = 79.7, P < 0.001). b, Honeybees given a choice between sucrose and sucrose laced with 1,000 nM TMX or CLO were less likely to survive after 24 h (lreg: IMD: χ42 = 5.18, P = 0.269; TMX: χ42 = 577, P < 0.001; CLO: χ42 = 243, P < 0.001). Cohort (cov) accounted for a significant portion of the variance in survival for all three treatment groups (lreg: IMD: χ12 = 22.0, P < 0.001; TMX: χ12 = 32.4, P < 0.001; CLO: χ12 = 70.2, P < 0.001). Sample sizes are the same as in Fig. 1. *P < 0.05 in least squares post hoc comparisons against sucrose in each treatment
Extended Data Figure 2 Antennal proboscis extension response (PER) and mouthparts assay of honeybees to solutions containing neonicotinoids.
a, Stimulation of the antennae with 1 M sucrose solutions containing neonicotinoids did not affect the elicitation of PER. b, Honeybees did not refuse to consume solutions containing neonicotinoids; only one bee in the CLO treatments failed to drink the solutions. n = 40 per neonicotinoid treatment for antennal stimuli and n = 10 for each concentration of each neonicotinoid for the mouthparts taste assay. Bees were randomly selected from 2 colonies.
Extended Data Figure 3 Young bees avoid solutions containing neonicotinoids.
a, Newly emerged worker bumblebees (n = 30 bees per treatment) and honeybees (n = 20 boxes per treatment) were tested in the behavioural choice assay with 1 nM and 10 nM IMD in sucrose solution as in Fig. 1. Bumblebees avoided consuming both solutions containing IMD (one-sample t-test against 0, 1 nM: P < 0.001, 10 nM: P = 0.001), whereas honeybees avoided only the 1 nM concentration (one-sample t-test against 0, 1 nM: P = 0.003, 10 nM: P = 0.773). Error bars represent ± s.e.m. b, The presence of IMD did not alter the spike frequency of gustatory neurons in the galeal sensilla of newly emerged honeybees (repeated-measures ANOVA, stimulus: F1,47 = 0.207, P = 0.653). Recordings were made from the basiconic sensilla on the galea as in Fig. 2. Boxplots represent the frequencies of responses to 50 mM sucrose or to 50 mM sucrose solutions containing 1 nM or 10 nM IMD. n = 5 bees, 10 sensilla per bee. Boxplots represent the median (black bars), the 1.5 interquartile range (whiskers) and outliers (circles). Stimuli on x axis are in order of presentation during the experiment.
Extended Data Figure 4 Spike-sorted recordings.
Data from four of the honeybees in Fig. 2h. a, To verify that the spike rates we observed in Fig. 2h were not a result in changes in the rates of firing of individual neurons, we spike-sorted recordings from four-honeybees stimulated with sucrose and IMD. b, Spike sorting revealed two potential spiking neurons (units) characterized by different spike amplitudes; both units spiked in response to sucrose stimulation. (This was also observed previously by Wright et al. 201017). One neuron is labelled in green, the other in red. Spike doublets (indicated in pink as ‘d’) where both neurons spiked nearly simultaneously were also observed. c, d, These same two spiking neurons continued to respond when stimulated with sucrose containing 1 μM IMD. e, Boxplots reveal that the rate of spiking was lower on average for one of the neurons (repeated-measures ANOVA, unit: F1,36 = 596, P < 0.001). The rate of firing of both neurons was not affected by IMD concentration (repeated-measures ANOVA, unit: F1,36 = 0.369, P = 0.547). Spikes from additional neurons (units) were not detected, and so we concluded that no other neurons were recruited during stimulation with IMD. ‘S’ indicates stimulation with sucrose. Boxplots represent the median (black bars), the 1.5 interquartile range (whiskers) and outliers (circles). Stimuli on x axis are in order of presentation during the experiment.
PowerPoint slides
Rights and permissions
About this article
Cite this article
Kessler, S., Tiedeken, E., Simcock, K. et al. Bees prefer foods containing neonicotinoid pesticides. Nature 521, 74–76 (2015). https://doi.org/10.1038/nature14414
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature14414
This article is cited by
-
The impact of chronic exposure to field-level thiamethoxam on sunflower visitation and yield for Apis cerana
Apidologie (2024)
-
Diverse cropping systems lead to higher larval mortality of the cabbage root fly (Delia radicum)
Journal of Pest Science (2024)
-
Non-optimal ambient temperatures aggravate insecticide toxicity and affect honey bees Apis mellifera L. gene regulation
Scientific Reports (2023)
-
The influence of sublethal neonicotinoid doses on individual Apis mellifera scutellata thermotolerance
Apidologie (2023)
-
Seed treatment with clothianidin induces changes in plant metabolism and alters pollinator foraging preferences
Ecotoxicology (2023)
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.