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

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 (µCT) scanning and
segmentation of multiple brain neuropils showed exposure during either
developmental stage 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. Whilst 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.