Abstract
Globally, neonicotinoids are the most used insecticides, despite their well-documented sub-lethal effects on beneficial insects. Neonicotinoids are nicotinic acetylcholine receptor agonists. Memory, circadian rhythmicity and sleep are essential for efficient foraging and pollination and require nicotinic acetylcholine receptor signalling. The effect of field-relevant concentrations of the European Union-banned neonicotinoids: imidacloprid, clothianidin, thiamethoxam and thiacloprid were tested on Drosophila memory, circadian rhythms and sleep. Field-relevant concentrations of imidacloprid, clothianidin and thiamethoxam disrupted learning, behavioural rhythmicity and sleep whilst thiacloprid exposure only affected sleep. Exposure to imidacloprid and clothianidin prevented the day/night remodelling and accumulation of pigment dispersing factor (PDF) neuropeptide in the dorsal terminals of clock neurons. Knockdown of the neonicotinoid susceptible Dα1 and Dβ2 nicotinic acetylcholine receptor subunits in the mushroom bodies or clock neurons recapitulated the neonicotinoid like deficits in memory or sleep/circadian behaviour respectively. Disruption of learning, circadian rhythmicity and sleep are likely to have far-reaching detrimental effects on beneficial insects in the field.
Highlights
Neonicotinoids are the most used insecticides, despite their well-documented sublethal effects on beneficial insects
The mean lifespan of control flies was 49 days while exposure to a field relevant concentration of 10 μg/L clothianidin causing a reduction to 28 days, imidacloprid and thiamethoxam to 36 days, and thiacloprid, to 39 days (Supplementary Fig. S1)
Field relevant concentrations of imidacloprid, clothianidin and thiamethoxam (10 and 50 μg/L) all reduced locomotor performance, tested via a negative geotaxis climbing assay, whilst thiacloprid had no effect on locomotion at these concentrations (Supplementary Fig. S4)
Summary
Neonicotinoids are the most used insecticides, despite their well-documented sublethal effects on beneficial insects. Neonicotinoids are highly efficacious insecticides they lack specificity, affecting both target pest species such as aphids and non-target beneficial insects, such as bees They share a mechanism of action, being agonists of nicotinic acetylcholine receptors (nAChR), the main neurotransmitter in the insect nervous system. Continued intensive use is likely to have severe consequences on insect species numbers, with knock-on as well as direct effects on the ecosystem, aquatic life, birds and mammals including potential toxicity to h umans[1,12,13,14] This has resulted in the European Union (EU) banning the nitrome neonicotinoids; imidacloprid, clothianidin and thiamethoxam (a prodrug for c lothiandin15) in 2017 followed by the cyanoimine neonicotinoid, thiacloprid in 202016. Neonicotinoids reduced honeybee antennal lobe Ca2+ responses and caused sensory deficits[28], potentially contributing to olfactory memory deficits
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