Chronic cadmium exposure impairs flight behavior by dampening flight muscle carbon metabolism in bumblebees

Cadmium pollution affects the global ecosystem because cadmium can be transferred up the food chain. The bumblebee, Bombus terrestris, is an important insect pollinator. Their foraging activity on flowers exposes them to harmful heavy metals, which damages their health and leads to massive population declines. However, the effects of chronic exposure to heavy metals on the flight performance of bumblebees have not yet been characterized. Here, we studied variation in the flight capacity of bumblebees induced by chronic cadmium exposure at field-realistic concentrations using behavioral, physiological, and molecular approaches. Chronic cadmium exposure caused a significant reduction in the duration, distance, and mean velocity of bumblebee flight. Transcriptome analysis showed that the impairment of carbon metabolism and mitochondrial dysfunction in the flight muscle were the primary causes. Physiological, biochemical, and metabolomic analyses validated disruptions in energy metabolism, and impairments in mitochondrial respiratory chain complexes activities. Histological analysis revealed muscle fiber damage and mitochondrial loss. Exogenous decanoic acid or citric acid partially restored sustained flight ability of bumblebees by mitigating muscle fiber damage and increasing energy generation. These findings provide insights into how long-term cadmium stress affects the flight ability of insects and will aid human muscle or exercise-related disease research.