Neonicotinoids disrupt circadian rhythms and sleep in honey bees

Abstract

Honey bees are critical pollinators in ecosystems and agriculture, but their numbers have significantly declined. Declines in pollinator populations are thought to be due to multiple factors including habitat loss, climate change, increased vulnerability to disease and parasites, and pesticide use. Neonicotinoid pesticides are agonists of insect nicotinic cholinergic receptors, and sub-lethal exposures are linked to reduced honey bee hive survival. Honey bees are highly dependent on circadian clocks to regulate critical behaviors, such as foraging orientation and navigation, time-memory for food sources, sleep, and learning/memory processes. Because circadian clock neurons in insects receive light input through cholinergic signaling we tested for effects of neonicotinoids on honey bee circadian rhythms and sleep. Neonicotinoid ingestion by feeding over several days results in neonicotinoid accumulation in the bee brain, disrupts circadian rhythmicity in many individual bees, shifts the timing of behavioral circadian rhythms in bees that remain rhythmic, and impairs sleep. Neonicotinoids and light input act synergistically to disrupt bee circadian behavior, and neonicotinoids directly stimulate wake-promoting clock neurons in the fruit fly brain. Neonicotinoids disrupt honey bee circadian rhythms and sleep, likely by aberrant stimulation of clock neurons, to potentially impair honey bee navigation, time-memory, and social communication.

Neonicotinoids disrupt memory, circadian behaviour and sleep

“…The high degree of structural and functional conservation of nAChRs between flies and bees 9 , 50 , 65 , and the conserved lethal and sub-lethal effects of reduced viability, longevity, locomotion, memory, circadian rhythmicity and sleep we show in flies and as reported in bees suggests that the modes of action identified here may also occur in bees 1 , 21 , 23 , 33 , 53 – 56 . Previous work has shown that sub-lethal effects observed in the lab translate to the field, for example neonicotinoid reduced foraging motivation is observed in bumblebees in the lab as well as in free flying colonies in the field 20 , 66 .…”

“…Previous work has shown that sub-lethal effects observed in the lab translate to the field, for example neonicotinoid reduced foraging motivation is observed in bumblebees in the lab as well as in free flying colonies in the field 20 , 66 . Reduced behavioural rhythmicity, shown in honeybees 23 , 33 , bumblebees 21 and here in fruit flies, is likely to reduce the amount of activity carried out in the daytime, reducing pollination and foraging opportunities 67 . The reduction in total sleep and fragmentation of sleep will reduce the quantity of deep sleep achieved, as deep sleep occurs later into the sleep episode 68 .…”

“…The s-LNv dorsal terminals exhibit circadian remodelling, with their terminals being more branched during the day than at night 45 and having higher PDF accumulation in the day than at night 43 , 46 . LNv expression of a GCaMP Ca 2+ reporter showed that 4 µg/l clothiandin caused a transient (~ 1 min) increase in Ca 2+ dependent fluorescence 33 . While similar experiments using a nAChR promoter Gal4 line (which drives expression wherever the endogenous nAChR is expressed) to express GCaMP showed that 2.5 µg/L imidacloprid blocked nAChR agonist (e.g.…”

“…Memory formation is also reliant on circadian rhythms 29 , 30 and sleep 31 , 32 . Work in honeybees and bumblebees has shown that neonicotinioids can reduce behavioural rhythmicity and disrupt sleep behaviour in these important pollinators 21 , 33 . The mode of action of neonicotinoids on circadian rhythmicity and sleep is unknown.…”

The Power of Drosophila melanogaster for Modeling Neonicotinoid Effects on Pollinators and Identifying Novel Mechanisms

“…Similar sensitivities to the different neonicotinoids are seen in Drosophila with the nonbanned thiacloprid being less toxic (Tasman et al, 2020(Tasman et al, , 2021. Furthermore the insecticides seem to act through a similar neuronal mechanism of action, causing initial hyperexcitability of neurons when applied to fly clock neurons in the whole brain (Tackenberg et al, 2020).…”