Mouthparts of the bumblebee (Bombus terrestris) exhibit poor acuity for the detection of pesticides in nectar.

Bees are important pollinators of agricultural crops, but their populations are at risk when pesticides are used. One of the largest risks bees face is poisoning of floral nectar and pollen by insecticides. Studies of bee detection of neonicotinoids have reported contradictory evidence about whether bees can taste these pesticides in sucrose solutions and hence avoid them. Here, we use an assay for the detection of food aversion combined with single-sensillum electrophysiology to test whether the mouthparts of the buff-tailed bumblebee (Bombus terrestris) detect the presence of pesticides in a solution that mimicked the nectar of oilseed rape (Brassica napus). Bees did not avoid consuming solutions containing concentrations of imidacloprid, thiamethoxam, clothianidin, or sulfoxaflor spanning six orders of magnitude, even when these solutions contained lethal doses. Only extremely high concentrations of the pesticides altered spiking in gustatory neurons through a slight reduction in firing rate or change in the rate of adaptation. These data provide strong evidence that bumblebees cannot detect or avoid field-relevant concentrations of pesticides using information from their mouthparts. As bees rarely contact floral nectar with other body parts, we predict that they are at high risk of unwittingly consuming pesticides in the nectar of pesticide-treated crops.

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.

Epidemiological waves - Types, drivers and modulators in the COVID-19 pandemic.

Introduction: A discussion of 'waves' of the COVID-19 epidemic in different countries is a part of the national conversation for many, but there is no hard and fast means of delineating these waves in the available data and their connection to waves in the sense of mathematical epidemiology is only tenuous. Methods: We present an algorithm which processes a general time series to identify substantial, significant and sustained periods of increase in the value of the time series, which could reasonably be described as 'observed waves'. This provides an objective means of describing observed waves in time series. We use this method to synthesize evidence across different countries to study types, drivers and modulators of waves. Results: The output of the algorithm as applied to epidemiological time series related to COVID-19 corresponds to visual intuition and expert opinion. Inspecting the results of individual countries shows how consecutive observed waves can differ greatly with respect to the case fatality ratio. Furthermore, in large countries, a more detailed analysis shows that consecutive observed waves have different geographical ranges. We also show how waves can be modulated by government interventions and find that early implementation of NPIs correlates with a reduced number of observed waves and reduced mortality burden in those waves. Conclusion: It is possible to identify observed waves of disease by algorithmic methods and the results can be fruitfully used to analyse the progression of the epidemic.

Temporal responses of bumblebee gustatory neurons to sugars.

The sense of taste permits the recognition of valuable nutrients and the avoidance of potential toxins. Previously, we found that bumblebees have a specialized mechanism for sensing sugars whereby two gustatory receptor neurons (GRNs) within the galeal sensilla of the bees' mouthparts exhibit bursts of spikes. Here, we show that the temporal firing patterns of these GRNs separate sugars into four distinct groups that correlate with sugar nutritional value and palatability. We also identified a third GRN that responded to stimulation with relatively high concentrations of fructose, sucrose, and maltose. Sugars that were nonmetabolizable or toxic suppressed the responses of bursting GRNs to sucrose. These abilities to encode information about sugar value are a refinement to the bumblebee's sense of sweet taste that could be an adaptation that enables precise calculations of the nature and nutritional value of floral nectar.

Chronic exposure to insecticides impairs honeybee optomotor behaviour.

Honeybees use wide-field visual motion information to calculate the distance they have flown from the hive, and this information is communicated to conspecifics during the waggle dance. Seed treatment insecticides, including neonicotinoids and novel insecticides like sulfoxaflor, display detrimental effects on wild and managed bees, even when present at sublethal quantities. These effects include deficits in flight navigation and homing ability, and decreased survival of exposed worker bees. Neonicotinoid insecticides disrupt visual motion detection in the locust, resulting in impaired escape behaviors, but it had not previously been shown whether seed treatment insecticides disrupt wide-field motion detection in the honeybee. Here, we show that sublethal exposure to two commonly used insecticides, imidacloprid (a neonicotinoid) and sulfoxaflor, results in impaired optomotor behavior in the honeybee. This behavioral effect correlates with altered stress and detoxification gene expression in the brain. Exposure to sulfoxaflor led to sparse increases in neuronal apoptosis, localized primarily in the optic lobes, however there was no effect of imidacloprid. We propose that exposure to cholinergic insecticides disrupts the honeybee's ability to accurately encode wide-field visual motion, resulting in impaired optomotor behaviors. These findings provide a novel explanation for previously described effects of neonicotinoid insecticides on navigation and link these effects to sulfoxaflor for which there is a gap in scientific knowledge.

Neonicotinoid and sulfoximine pesticides differentially impair insect escape behavior and motion detection.

Insect nervous systems offer unique advantages for studying interactions between sensory systems and behavior, given their complexity with high tractability. By examining the neural coding of salient environmental stimuli and resulting behavioral output in the context of environmental stressors, we gain an understanding of the effects of these stressors on brain and behavior and provide insight into normal function. The implication of neonicotinoid (neonic) pesticides in contributing to declines of nontarget species, such as bees, has motivated the development of new compounds that can potentially mitigate putative resistance in target species and declines of nontarget species. We used a neuroethologic approach, including behavioral assays and multineuronal recording techniques, to investigate effects of imidacloprid (IMD) and the novel insecticide sulfoxaflor (SFX) on visual motion-detection circuits and related escape behavior in the tractable locust system. Despite similar LD50 values, IMD and SFX evoked different behavioral and physiological effects. IMD significantly attenuated collision avoidance behaviors and impaired responses of neural populations, including decreases in spontaneous firing and neural habituation. In contrast, SFX displayed no effect at a comparable sublethal dose. These results show that neonics affect population responses and habituation of a visual motion detection system. We propose that differences in the sublethal effects of SFX reflect a different mode of action than that of IMD. More broadly, we suggest that neuroethologic assays for comparative neurotoxicology are valuable tools for fully addressing current issues regarding the proximal effects of environmental toxicity in nontarget species.

Neural conduction, visual motion detection, and insect flight behaviour are disrupted by low doses of imidacloprid and its metabolites.

While neonicotinoid insecticides impair visually guided behaviours, the effects of their metabolites are unknown and measurements of environmental concentrations of neonicotinoids, typically lower than those required to elicit toxic effects, tend to exclude metabolites. Here we examined the contributions of imidacloprid and two of its metabolites, imidacloprid-olefin and 5-hydroxy-imidacloprid, on neural conduction velocity, visual motion detection and flight in the locust (Locusta migratoria) using a combination of electrophysiological and behavioural assays. We show reduced visual motion detection and impaired flight behaviour following treatment of metabolite concentrations equal to sublethal doses of the parent compound. Additionally, we show for the first time that imidacloprid and its metabolites result in a decrease in conduction velocity along an unmyelinated axon. We suggest that secondary effects of the insecticide on the biophysical properties of the axon may result in decreased neural conduction. As these metabolites display neurotoxicity similar to the parent compound they should be considered when quantifying environmental concentrations.

Three-dimensional shape and velocity changes affect responses of a locust visual interneuron to approaching objects.

Adaptive collision avoidance behaviours require accurate detection of complex spatiotemporal properties of an object approaching in an animal's natural, three-dimensional environment. Within the locust, the lobula giant movement detector and its postsynaptic partner, the descending contralateral movement detector (DCMD), respond robustly to images that emulate an approaching two-dimensional object and exhibit firing rate modulation correlated with changes in object trajectory. It is not known how this pathway responds to visual expansion of a three-dimensional object or an approaching object that changes velocity, both of which represent natural stimuli. We compared DCMD responses with images that emulate the approach of a sphere with those elicited by a two-dimensional disc. A sphere evoked later peak firing and decreased sensitivity to the ratio of the half size of the object to the approach velocity, resulting in an increased threshold subtense angle required to generate peak firing. We also presented locusts with an approaching sphere that decreased or increased in velocity. A velocity decrease resulted in transition-associated peak firing followed by a firing rate increase that resembled the response to a constant, slower velocity. A velocity increase resulted in an earlier increase in the firing rate that was more pronounced with an earlier transition. These results further demonstrate that this pathway can provide motor circuits for behaviour with salient information about complex stimulus dynamics.

A sublethal dose of a neonicotinoid insecticide disrupts visual processing and collision avoidance behaviour in Locusta migratoria.

Neonicotinoids are known to affect insect navigation and vision, however the mechanisms of these effects are not fully understood. A visual motion sensitive neuron in the locust, the Descending Contralateral Movement Detector (DCMD), integrates visual information and is involved in eliciting escape behaviours. The DCMD receives coded input from the compound eyes and monosynaptically excites motorneurons involved in flight and jumping. We show that imidacloprid (IMD) impairs neural responses to visual stimuli at sublethal concentrations, and these effects are sustained two and twenty-four hours after treatment. Most significantly, IMD disrupted bursting, a coding property important for motion detection. Specifically, IMD reduced the DCMD peak firing rate within bursts at ecologically relevant doses of 10 ng/g (ng IMD per g locust body weight). Effects on DCMD firing translate to deficits in collision avoidance behaviours: exposure to 10 ng/g IMD attenuates escape manoeuvers while 100 ng/g IMD prevents the ability to fly and walk. We show that, at ecologically-relevant doses, IMD causes significant and lasting impairment of an important pathway involved with visual sensory coding and escape behaviours. These results show, for the first time, that a neonicotinoid pesticide directly impairs an important, taxonomically conserved, motion-sensitive visual network.