Bees and other pollinators often encounter pesticides while collecting nectar and pollen from agricultural crops. Widely used to protect crops, pesticides are toxic to insects and have contributed to population declines in all bee species.

One way that bees might be able to avoid pesticides is using their incredibly good sense of taste, which can detect subtle differences between sugary solutions. Therefore, if pesticides taste bitter to them, bumblebees may be able to avoid feeding treated crops. However, it was not clear if bees can taste pesticides. Previous studies investigating whether they can taste a group of pesticides called “neonicotinoids” gave contradictory results. Furthermore, explicit behavioural tests of their ability to taste pesticides had not been performed.

To shed light on this, Parkinson et al. compared the responses of neurons within structures used for detecting taste in bumblees eating a pure sugar solution with those eating a solution containing pesticides. Experiments with a group of pesticides known as ‘cholinergic’ showed that neuron responses were the same whether the sugar solution contained pesticides or not. Secondly, by looking at bumblebee feeding behaviour, Parkinson et al. found that bees offered both pure and pesticide-laced sugar solutions would still drink the pesticide solution, even when it was toxic enough to make them very ill or kill them. This was the case regardless of which pesticide was used.

The experiments showed that bumblebees cannot use their sense of taste to avoid drinking pesticide-laced nectar, which is an important finding for policymakers making decisions about the use of pesticides on agricultural crops. It is possible that bees simply have a poor sense of bitter taste. However, in the future, these methods could be used to identify a compound that tastes bad to bees. Including such a compound in pesticides, could deter bees from feeding on pesticide-treated crops that do not require pollination, and help to restore their declining populations.

Insect pollination is a critical ecosystem service. The most economically valuable pollinators are bees (Calderone, 2012; Garibaldi et al., 2013; Huang and An, 2018), especially domesticated bees that secure crop yield and quality (Meehan et al., 2011). In agricultural ecosystems, however, insecticides are widely used to protect crop yields (Klein et al., 2007). Using insecticides impacts the health and survival of bees, contributing to the recent population declines of all bee species (Goulson et al., 2015; Potts et al., 2016; Van der Sluijs et al., 2013; Vanbergen et al., 2013). Hundreds of studies have shown that exposure to sublethal concentrations of neonicotinoid pesticides (i.e. imidacloprid, IMD, thiamethoxam, TMX, and clothianidin, CLO) in food impairs foraging behaviour, homing and orientation behaviour, and olfactory learning and memory (e.g. Gill et al., 2012; Henry et al., 2012; Parkinson et al., 2022a; Schneider et al., 2012b; Williamson et al., 2014; Wright et al., 2015). Most studies administer pesticides in sugar solutions; bees consume the solution, and then a change in behaviour or performance is recorded. If bees could detect and avoid pesticides in food, however, these substances could be used to defend crops against pests without risk to bees. Only a few have explicitly tested whether bees can taste and avoid neonicotinoid pesticides in nectar (Arce et al., 2018; Kessler et al., 2015; Muth et al., 2020), but the conclusions of these studies are contradictory. In addition, other compounds that affect cholinergic signalling in the insect nervous system, such as sulfoxaflor, have been proposed as alternatives to neonicotinoids, but whether or not these compounds can be detected by the bee’s sense of taste has not previously been tested.

Insects detect non-volatile compounds (i.e. tastants) through activation of GRNs in contact chemosensilla on mouthparts, antennae, and tarsi which express receptor proteins that bind with specific types of ligands (e.g. sugars, non-nutrient ‘bitter’ compounds, salts, etc.; Wright, 2016). When a taste receptor binds with its ligand, this sets off a signal transduction cascade that results in depolarisation of the neuron (Dethier, 1976). For example, several types of receptors tuned to bitter substances are expressed in a specialized subset of GRNs (Weiss et al., 2011). When these GRNs spike in response to stimulation, feeding reflexes are inhibited (French et al., 2015). Bitter compound detection is also accomplished by the inactivation of sugar-sensing GRNs (French et al., 2015). For compounds which are potentially toxic, simultaneous activation of GRNs that directly inhibit feeding reflexes and silencing of GRNs that activate feeding make it possible to form a rapid response in reaction to contact (Wright, 2016). Thus, we expected that if bees could detect neonicotinoids as bitter compounds, we would see activation of bitter-sensing GRNs and/or inactivation of sugar-sensing GRNs. Previously, we observed that stimulation of the mouthpart’s galeal sensilla with neonicotinoids in water did not elicit spikes from any GRNs, nor did we see a reduction in the rate of firing of sugar-sensing GRNs in the sensilla when stimulated with a mixture of sucrose and neonicotinoid compound (Kessler et al., 2015).

In a two choice assay, we unexpectedly found that when bees were given a choice between sucrose solution and sucrose containing field-relevant doses of IMD and TMX over a 24 hr period, the bees choose the neonicotinoid solution (Kessler et al., 2015). This could indicate that bees find neonicotinoid pesticides phagostimulatory, like sugars. However, we also failed to find evidence that neonicotinoid pesticides in water elicited spikes in any galeal GRNs including the nutrient/sugar sensing neurons. For this reason, we concluded that bees could not taste neonicotinoids in nectar or on their own in water. This conclusion, however, has been challenged by a study in free-flying B. terrestris foragers (Arce et al., 2018). They found that free-flying bumblebees preferred specific concentrations of solutions laced with TMX, but only after a period of at least 10 days of feeding on the solutions (Arce et al., 2018). In this study, the location of the solutions was randomised, forcing a choice at the point of feeding. These authors concluded that the only way bees could solve this problem was if they used their sense of taste to identify the preferred solution, arguing that further work needed to be done to identify the mechanism for sensation. Subsequently, however, another study in a different species of bumblebees (B. impatiens) using methods similar to ours reported that bees are neither attracted nor deterred from consuming sugar solutions containing neonicotinoids, consistent with the idea that they cannot detect the pesticides (Muth et al., 2020). Thus, whether or not bumblebees can taste neonicotinoids in food remains unresolved.

Bees have highly specialized mechanisms for encoding sugars which are different to those reported for any other insect species. For example, in bumblebee galeal sensilla, stimulation with sugars produces coherent spiking in 2 GRNs which burst in response to stimulation with high-value saccharide compounds (Miriyala et al., 2018; Parkinson et al., 2022b). We recently discovered that bumblebees also highly value the monosaccharide, fructose, and have a GRN tuned to detect it (Parkinson et al., 2022b). It is possible that changes to the burst pattern of firing could indicate that the presence of a compound such as a neonicotinoid in food. Furthermore, the type of sugar used to stimulate the sensilla could influence whether bees could taste neonicotinoids (Parkinson et al., 2022b). We also know that the labial palps are critical to toxin detection in other insect species (Chapman and Sword, 1993), and could house additional GRNs sensitive to bitter compounds like pesticides. Our previous work on neonicotinoid taste used sucrose to stimulate the galeal sensilla and did not analyse how pesticides might alter the burst structure of the galeal GRN response to sugars or test the labial palps. Clearly, deeper investigations could determine whether the mouthparts GRNs possess novel gustatory mechanisms for pesticide detection and provide critical information about the risk to bees of consuming the nectar of pesticide-defended crops in the field. They would also elucidate novel mechanisms for the detection of bitter compounds.

Here, we use a combination of sensitive behavioural assays and electrophysiology to test in detail whether bumblebee mouthparts have mechanisms to detect pesticides in nectar. Feeding assays using freely moving foragers make it possible to assess if bees detect and avoid potential toxins in food (Ma et al., 2016). To definitively test whether bumblebees detect neonicotinoids on their mouthparts, we quantified the structure of feeding when the mouthparts of freely-moving bumblebees (B. terrestris) were stimulated with nectar-like solutions containing pesticides over a 2 min period (Ma et al., 2016). We specifically tested a mixture of primarily fructose and glucose that mimicked the nectar of oilseed rape (Brassica napus) with field-relevant concentrations of neonicotinoids. In addition, we comprehensively tested these solutions on the gustatory receptor neurons in the A-type sensilla on the galea and the labial palps of the bees’ mouthparts using electrophysiology to determine whether sensilla in multiple locations are able to detect neonicotinoids (IMD, CLO, and TMX) and the previously untested sulfoxamine pesticide, sulfoxaflor (SFX). The burst-spiking of the galeal GRNs was analysed for changes to structure and compared to the GRN response to the bitter compound, quinine (QUI), which has been reported previously to be a feeding deterrent to bees (Ma et al., 2016; Wright et al., 2010).

For the first time, we report how populations of GRNs on the bee’s mouthparts respond to stimulation with putatively bitter compounds. We verified that bees do not have mechanisms on their mouthparts that enable them to taste neonicotinoids or sulfoxaflor when these compounds are present in nectar. Neonicotinoids and sulfoxaflor did not change the bursting of sugar-sensing neurons in the galea, nor did they elicit or inhibit spikes in labial palp neurons. Strikingly, we show that bumblebees do not avoid drinking OSR nectar solutions even when very high concentrations of common pesticides are present. Very high concentrations of these pesticides could produce a small but measurable reduction in the spiking of sugar-sensing GRNs, but these compounds never elicited spikes on their own. What’s more, these small changes in the rate of spiking did not translate into features that the clustering algorithm could use to differentiate pesticide laced stimuli from the control OSR solution. From these data, we conclude that the buff-tailed bumblebee’s mouthparts do not have mechanisms for the detection and avoidance of common cholinergic pesticides in nectar.

In the present experiments, we expected that if neonicotinoids and sulfoxaflor could be tasted by bees, they would exhibit the same responses in GRNs produced by other non-nutrient compounds (i.e. bitter responses). For this reason, we were mainly testing for the reduction of GRN spiking caused by the suppression of sugar-sensing GRNs, as all of the ‘bitter’ compounds we tested were presented to the sensilla in OSR nectar (a mixture of primarily fructose and glucose). The known bitter compound, QUI, clearly suppressed the activity of sugar-sensing GRNs in both labial palps and the galea, but it did not measurably alter the burst pattern of firing of the galeal GRNs. Importantly, our new data were able to confirm that field-relevant concentrations of pesticides did not significantly alter the pattern or rate of spiking of galeal or labial palp GRNs towards a nectar solution.

We used a clustering algorithm that integrated input from all the sensilla we recorded from over a 1 s time interval with every stimulus to identify whether population-level input made it possible to differentiate the stimuli. Although we were able to measure small but significant reduction in the responses of both labial palp and galeal neurons caused by the high concentrations (100 µM) of IMD, SFX, and TMX, this effect was not sufficient for the clustering algorithm to form classes of distinct stimuli for the OSR-pesticide mixtures. This is similar to what we observed for 0.1 mM QUI; although a small change in firing was detected, the clustering algorithm did not differentiate it from OSR. It is worth noting that the OSR background solutions in both cases were different: in the behavioural experiments the concentration of OSR was an average value of that naturally found in nectar. Our physiology experiments were performed using a 10% dilution of this solution. Different solutions were used because it was not possible to record from neurons with such a concentrated sugar solution, and in behavioural experiments, most bumblebees do not find 10% OSR sufficiently phagostimulatory to feed.

Our electrophysiological recordings are the first to report GRN responses from the bumblebee’s labial palps. The labial palps in other insects such as locusts are used to detect both phagostimulants and deterrant compounds (Blaney and Chapman, 1970), so we might have rationally expected to observe labial palp GRNs that spike in response to QUI and cholinergic pesticides, but we did not. This could indicate that on the mouthparts, bitter compounds are only detected through the suppression of sugar-sensing GRNs (de Brito Sanchez et al., 2005).

It is interesting to note that in the case of all bitter compounds tested, the output of the clustering algorithm matched the behaviour of the bees, as the bees did not reject any of the pesticide solutions or the 0.1 mM QUI solution after the first feeding bout. This could indicate that that small differences detected at the sensory periphery do not translate into a sufficient signal across the whole population of gustatory neurons to produce an aversion to foods containing potential toxins. Bumblebees did drink less overall of the 0.1 mM QUI solution compared to OSR, however the amount of time they spent in contact with the feeding solution was the same. This suggests that, while 0.1 mM QUI is not immediately aversive to bumblebees (i.e. by taste), they can integrate negative post-ingestive feedback within a 2-min feeding period. Compounds reach the hemolymph of honeybees within 30 s of ingestion (Simcock et al., 2018), and quinine causes malaise-like symptoms (Ayestaran et al., 2010; Hurst et al., 2014), so it is feasible that the bumblebees in our behavioural assay factored in post-ingestive feedback while consuming 0.1 mM QUI. Unfortunately, when fed high concentrations of pesticides, post-ingestive feedback did not prevent bumblebees from consuming potentially lethal doses. For example, the LD50 for TMX in Bombus terrestris is approximately 6 ng/bee (Siviter et al., 2022), and bumblebees in our assay consumed a median amount of 3.5 ng of TMX when dissolved at 100 uM in OSR.

Our data also indicate that gustatory coding is more than the presence or absence of spikes arising from GRNs tuned to detect particular tastants. In bumblebees, it is clear that the pattern of spiking itself conveys information which is a feature that enables the brain to distinguish gustatory stimuli (Parkinson et al., 2022b). This supports the idea that encoding of gustatory stimuli is accomplished by the whole population of GRNs on a given body part (e.g. the proboscis) as was observed in multichannel recordings from the adult hawkmoth maxillary nerve (Reiter et al., 2015). Thus, activity across the mouthparts GRN population that includes temporal input over time is likely to be used by the brain to differentiate taste stimuli and to facilitate the valuation of food quality. Our new data testing the difference between a nectar stimulus composed of a mixture of sugars (OSR) and sucrose clearly illustrates this. The changes in the rate of bursting and spiking in the galeal and labial palps were sufficient for the clustering algorithm to classify sucrose and OSR as separate stimuli. Although our behavioural assay did not show a difference, we would not expect it to, as it is an assay developed to study food rejection behaviour by bees, not differences in phagostimulation.

Previously, Arce et al., 2018 reported that B. terrestris were capable of selectively foraging on 30% w/v sucrose solutions containing TMX. This finding confirmed our previous data that honeybees and bumblebees prefer solutions containing TMX (Kessler et al., 2015). Arce et al., 2018 did not observe a preference for or against the solutions containing the neonicotinoids during the initial days of their experiments. We expect that if taste was the mechanism for the preference, the bees would have shown a preference for the TMX solution within the first foraging bout, similar to the time frame of our behavioural assay in this study (2 min). Instead, the authors found that the preference for the TMX solution developed over time. Similarly, in our previous work, we found that individual bees developed a preference for solutions containing TMX if they were confined to feed on a choice between sucrose and sucrose laced with pesticide over longer time period (i.e. 24 hr, Kessler et al., 2015). We concluded that the preference was caused by the pharmacological action of TMX on cholinergic circuits involved in encoding reward in the insect brain (Barnstedt et al., 2016), as we found no electrophysiological evidence to support that bees could taste neonicotinoids (Kessler et al., 2015). This conclusion is consistent with the expectation that a preference resulting from post-ingestive reinforcement caused by amplification of the brain’s response to sugars would be expected to develop following long-term, repeated exposure to a pharmacological compound (Palmer et al., 2013; Wright et al., 2013). If TMX caused bees to associate a higher ‘reward value’ with food found in a particular location, they would learn to return to it in preference over other solutions. Although Arce et al., 2018 switched the feeders between training and testing phases, this may not have been sufficient to rule out the possibility that bees could learn the location of the food within a single feeding bout.

Arce et al., 2018 conducted their experiments using gravity feeders in an enclosed arena, allowing bees to consume solutions ad libitum. Since the feeders did not have visual or olfactory cues, the authors inferred that the bees were capable of tasting the TMX in the solution. However, gravity feeders do not simulate how bees feed on real flowers. These feeders have large openings that allow multiple bees to feed simultaneously, enabling them to contact the solution with all body parts, including the tarsi and antennae. While it is possible that the sensilla on the antennae or tarsi could detect TMX, it seems unlikely given that honeybees have limited bitter detection in these locations, only observed when the sensilla are contacted with concentrations of compounds like QUI that are >1 mM (de Brito Sanchez et al., 2005; de Brito Sanchez et al., 2014). The field-relevant concentrations of the pesticides we tested are between 3–6 orders of magnitude lower in concentration (see Kessler et al., 2015 for review); such dilute concentrations of a bitter compound present in a highly concentrated sugar solution would be difficult for most organisms to detect.

Floral morphology such as corolla length has often co-evolved with particular groups of pollinators with longer mouthparts; a long corolla protects nectar when visitors are efficient and reliable pollinators. In many flowers, nectar is hidden deep within the corolla such that the only contact that bumblebees have with it is via the distal end of the proboscis (also the location where most of the sensilla are). For example, in OSR flowers, nectaries are located at a depth of 5–8 mm (Cresswell et al., 2001) and the nectar cannot be contacted otherwise unless the bee bites through the petals. In addition, bees learn to handle flowers quickly to improve their foraging efficiency (Heinrich, 1976) and even extend the proboscis in anticipation of entering the corolla prior to landing. Thus, they are unlikely to contact nectar using gustatory sensilla on their antennae or tarsi while foraging. For this reason, it is likely that nectar palatability is largely determined by the sensilla on the proboscis.

Data in this manuscript are currently available on Figshare.com at https://doi.org/10.6084/m9.figshare.22005272.v1.

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Author details

1. Rachel H Parkinson

   Department of Biology, University of Oxford, Oxford, United Kingdom

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Visualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-8192-3178

2. Jennifer Scott

   Department of Biology, University of Oxford, Oxford, United Kingdom

   Contribution

   Data curation, Writing – review and editing

   Competing interests

   No competing interests declared

3. Anna L Dorling

   Department of Biology, University of Oxford, Oxford, United Kingdom

   Contribution

   Data curation, Writing – original draft

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0009-0005-4084-0201

4. Hannah Jones

   Department of Life Sciences, Imperial College, London, United Kingdom

   Contribution

   Data curation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9481-8094

5. Martha Haslam

   Department of Biology, University of Oxford, Oxford, United Kingdom

   Contribution

   Data curation

   Competing interests

   No competing interests declared

6. Alex E McDermott-Roberts

   Department of Biology, University of Oxford, Oxford, United Kingdom

   Contribution

   Data curation

   Competing interests

   No competing interests declared

7. Geraldine A Wright

   Department of Biology, University of Oxford, Oxford, United Kingdom

   Contribution

   Conceptualization, Supervision, Funding acquisition, Methodology, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   geraldine.wright@biology.ox.ac.uk

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2749-021X

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