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.

Taxonomic imbalances in animal sleep studies

“…Arthropods alone count for more than 3/4 of studies in invertebrates, representing 27% of these references. These results can be explained by the discovery and description of sleep in an insect model, the fruit fly (Drosophila melanogaster), at the beginning of the 21st century (Hendricks et al, 2000), which paved the way to numerous studies addressing sleep in this same insect, but also in the honey bee (Apis mellifera), another insect very often studied until recently (Tackenberg et al, 2020;Vázquez et al, 2020). This trend is confirmed our literature searches on Google Scholar: fruit flies and honey bees are by far the arthropods for which the study of sleep is the most often mentioned, with respectively 372,000 and 117,000 references (Arthropods: 549,900 references) found by the search engine.…”

“…However, these consequences could have a large-scale impact if they involve insects providing essential ecosystem services such as pollination. Actually, in populations of Apis mellifera, the feeders synchronize their activity with the workers', so the disruption of the circadian rhythms of the latter could greatly affect the organization of the hive (Tackenberg et al, 2020) and ultimately reduce the efficiency of pollinating bees. This hypothesis justifies the importance of studying sleep in species other than vertebrates and suggests that arthropods will be the subject of more studies on this topic in the following years, thus contributing to the reduction of the taxonomic bias in favor of other animals which was initiated at the beginning of the 21st century.…”

“…Moreover, the numerous sleep deprivation experiments carried out on rats and bees showed that, in both mammals and insects, rest is essential for the proper functioning of the brain since all the tested individuals suffered from impaired cognitive performances (learning difficulties, inability to form new memories, space perception issues, etc.) (Helfrich-Förster, 2018;Kayser et al, 2015;Keene and Duboue, 2018;Tackenberg et al, 2020).…”

“…The artificial lighting of cities and the tendency of bitumen to retain heat are therefore likely to disrupt the sleep of insects in the long term. To boot, the noise and vibrations generated by human activities (Tougeron and Abram, 2017) and the use of pesticides such as neonicotinoids (Tackenberg et al, 2020;Tasman et al, 2020) or glyphosate (Vázquez et al, 2020) in agrosystems can also cause a significant shift in their circadian rhythms. Consequently, urban sprawl and land artificialization could be at the origin of serious disturbances in the behaviour of insects, which would ultimately have a detrimental impact across ecosystems.…”

Neonicotinoids and Varroa mites force the extending of longevity in a bee colony during overwintering to forget

“…NNs can adversely affect the immunity of queen bees and cause the re-development of the disease 10 ; they disrupt the circadian rhythms and sleep of honeybees and can impair honeybee navigation, time memory and social communication 11 ; acetamiprid adversely affects memory-related properties in honeybees, homing ability and expression levels of memory-related genes 12 . NNs reduce the mating frequency of queens, resulting in a decrease in the genetic diversity of working bees, which can adversely affect colony vitality 13 ; imidacloprid damages the development of the nervous system in areas responsible for both the sense of smell and vision in the larval stage of honeybees, inhibiting the activity of honeybees 14 .…”