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Bees prefer foods containing neonicotinoid pesticides

A Corrigendum to this article was published on 17 February 2016

This article has been updated


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.

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Figure 1: Foraging-age bees prefer to eat food containing neonicotinoids.
Figure 2: Electrophysiological recordings of the gustatory receptor neurons from the mouthparts of bumblebees and honeybees during stimulation with neonicotinoids.

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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.

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Authors and Affiliations



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

Correspondence to Geraldine A. Wright.

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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.

Extended Data Table 1 Concentrations of neonicotinoids reported in floral nectar
Extended Data Table 2 Generalized linear models for the neonicotinoid choice experiment and total food consumption
Extended Data Table 3 One-sample t-tests against ‘0’ for each treatment of the 24 h behavioural assay
Extended Data Table 4 Comparison of doses consumed by each bee species for each treatment
Extended Data Table 5 Repeated-measures ANOVA

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Kessler, S., Tiedeken, E., Simcock, K. et al. Bees prefer foods containing neonicotinoid pesticides. Nature 521, 74–76 (2015).

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