Multilevel impact of cocaine on honeybees: From neurochemistry and mitochondrial dysfunction to superorganism

Cocaine abuse remains a serious global problem with far-reaching health, economic, social, and criminal consequences. Therefore, continued research on the mechanisms underlying cocaine effects is highly desirable. Utilizing invertebrate models in this field offers significant practical advantages, while a comparative approach can further broaden the understanding of fundamental physiological principles. This study highlights the honeybee Apis mellifera as a promising model for investigating the effects of single cocaine dose at both the individual and collective/social levels. Our results show that acute cocaine administration triggers a complex array of neurochemical, behavioral, and subcellular-toxic changes, each characterized by distinct temporal dynamics. The 'neurochemical-behavioral' axis manifested through altered biogenic amine levels, which are analogous to the mammalian response. Concurrently, the 'subcellular-toxic' axis, encompasses a cascade of mitochondrial abnormalities, reduced citrate synthase activity, and a compensatory antioxidant response. Furthermore, the impact of a single treatment was assessed by monitoring vibroacoustic signals—a likely manifestation of social communication within the hive—, which exhibited a notable latency compared to the biochemical/ultrastructural alterations at an individual level. These signals may indicate a collective response of colony to the disruption of individual biochemical and structural homeostasis. In essence, our results demonstrate that the honeybee is a compelling supplementary model that offers a promising opportunity to understand both socio-behavioral and molecular mechanisms of cocaine action, with potential implications for drug impact and addiction research. • A single dose of cocaine significantly affects the level of biogenic amines in bees. • Cocaine affects also antioxidant markers, vitellogenins and citrate synthase. • Cocaine induces mitochondrial abnormalities in thoracic muscles. • Cocaine social effect manifests itself through modulation of vibroacoustic signals. • Bees appear to be an alternative model to study mechanisms of cocaine actions.