Reduced Honeybee Pollen Foraging under Neonicotinoid Exposure: Exploring Reproducible Individual and Colony Level Effects in the Field Using AI and Simulation

Honeybees (Apis mellifera) are important
pollinators. Their foraging behaviors are essential to colony sustainability.
Sublethal exposure to pesticides such as neonicotinoids can significantly
disrupt these behaviors, in particular pollen foraging. We investigated
the effects of sublethal doses of the neonicotinoid imidacloprid on
honeybee foraging, at both individual and colony levels, by integrating
field experiments with artificial intelligence (AI)-based monitoring
technology and mechanistic simulations using the BEEHAVE model. Our
results replicated previous findings, which showed that imidacloprid
selectively reduces pollen foraging at the colony level, with minimal
impact on nectar foraging. Individually marked exposed honeybees exhibited
prolonged pollen foraging trips, reduced pollen foraging frequency,
and instances of drifting pollen foraging trips, likely due to impaired
cognitive functions and altered metabolism. These behavioral changes
at the individual level corroborated the previous model predictions
derived from BEEHAVE, which highlights the value of combining experimental
and simulation approaches to disentangle underlying mechanisms through
which sublethal effects on individual foragers scale up to impact
colony dynamics. Our findings have implications for future pesticide
risk assessment, as we provide a robust feeding study design for evaluating
pesticide effects on honeybee colonies and foraging in real landscapes,
which could improve the realism of higher-tier ecological risk assessment.