Insecticide exposure during brood or early-adult development reduces brain growth and impairs adult learning in bumblebees

Abstract

For social bees, an understudied step in evaluating pesticide risk is how contaminated food entering colonies affects residing offspring development and maturation. For instance, neurotoxic insecticide compounds in food could affect central nervous system development predisposing individuals to become poorer task performers later-in-life. Studying bumblebee colonies provisioned with neonicotinoid spiked nectar substitute, we measured brain volume and learning behaviour of 3 or 12-day old adults that had experienced in-hive exposure during brood and/or early-stage adult development. Micro-computed tomography scanning and segmentation of multiple brain neuropils showed exposure during either of the developmental stages caused reduced mushroom body calycal growth relative to unexposed workers. Associated with this was a lower probability of responding to a sucrose reward and lower learning performance in an olfactory conditioning test. While calycal volume of control workers positively correlated with learning score, this relationship was absent for exposed workers indicating neuropil functional impairment. Comparison of 3-and 12-day adults exposed during brood development showed a similar degree of reduced calycal volume and impaired behaviour highlighting lasting and irrecoverable effects from exposure despite no adult exposure. Our findings help explain how the onset of pesticide exposure to whole colonies can lead to lag-effects on growth and resultant dysfunction.

Pollen source richness may be a poor predictor of bumblebee colony growth

“…However, we found that polyfloral colonies, that had access to a lower amount of crude protein, reared both a lower number and mass of workersparticularly in the latter two weeks of our experiment (a similar pattern was observed for reared males). Producing a smaller and lighter workforce in polyfloral colonies may have implications for colony task performance, given that larger workers appear to show better learning and foraging performances (Goulson et al 2002;Spaethe and Weidenmüller 2002;Jandt et al 2009;Riveros and Gronenberg 2009;Willmer and Finlayson 2014;Smith et al 2020). The lack of any apparent compensatory strategy observed in our study is unlikely to be down to a reduced appetite, as the per capita consumption rate of both sucrose solution and pollen was not significantly different and actually higher on average in polyfloral colonies ( Figures S2-3).…”

Neonicotinoids disrupt memory, circadian behaviour and sleep

“…Therefore, neonicotinoids can act at multiple nAChR synapses in the mushroom body circuit, disrupting the plasticity-relevant signals for memory formation. Furthermore, in bees, field relevant concentrations of neonicotinoids disrupted mushroom body-mediated olfactory memory, electrically inactivated Kenyon cells 22 , decreased their synaptic density 26 and reduced antennal lobe Ca 2+ responses upstream of the mushroom body 27 . Additionally, neonicotinoids have been shown to interrupt mushroom body development 27 , providing a further route for memory disruption.…”

“…Furthermore, in bees, field relevant concentrations of neonicotinoids disrupted mushroom body-mediated olfactory memory, electrically inactivated Kenyon cells 22 , decreased their synaptic density 26 and reduced antennal lobe Ca 2+ responses upstream of the mushroom body 27 . Additionally, neonicotinoids have been shown to interrupt mushroom body development 27 , providing a further route for memory disruption. Our results extend existing data from pollinators showing neonicotinoid disrupt memory by showing for the first time that the disruption is mediated by nAChRs containing Dα1 or Dβ2 subunits in the mushroom body.…”

“…In honeybees, sub-lethal neonicotinoids electrically inactivated 22 and decreased the synaptic density 26 of mushroom body neurons and resulted in disrupted olfactory memory 22 . In bumblebees, exposure during development reduced mushroom body growth, causing learning deficits in adults 27 . Neonicotinoids also reduced honeybee antennal lobe Ca 2+ responses and caused sensory deficits 28 , potentially contributing to olfactory memory deficits.…”

Honeybee gut microbiota modulates host behaviors and neurological processes

“…Moreover, the stimulation of the mAChR of honeybee increases the volume of the mushroom body neuropil, which mimics the reinforcement of cholinergic neurotransmission in foraging bees 73 . A reduced mushroom body calycal growth is also associated with lower learning performance in bumblebees through micro-computed tomography scanning 74 . It would be interesting to investigate whether gut microbes impact the structural changes of the brain in future studies.…”