Novel Insights into Foodborne Microplastics-Enhanced Shoaling Behavior in Marine Korean Rockfish (Sebastes schlegelii) : Energy Deficiency-Driven Gut-Brain Axis Dysregulation

Microplastics (MPs) pollution threatens ocean health, yet their impacts on fish shoaling behavior remain poorly understood. Herein, the effects of foodborne polyethylene terephthalate debris (D-PET), PET fiber (F-PET), and tire wear particles (TWPs) at environmentally relevant concentrations (0.1 and 1 mg g –1 ) on behavioral strategies and energy metabolism-mediated gut-brain axis regulation in Korean rockfish ( Sebastes schlegelii ) were investigated through a 50-day exposure-depuration experiment. MPs induced boldness reduction and hyperactivity, consequently intensifying shoaling behavior in an order of TWPs > F-PET > D-PET, with the interindividual distance decreased by up to 12.14 ± 0.31%. Leachable additives from TWPs, including benzothiazolone, benzothiazole, N,N′ -ditolyl- p -phenylenediamine, and N -1,3-dimethylbutyl- N′ -phenyl- p -phenylenediamine-quinone, were primarily responsible for the shoaling enhancement. MPs induced hepatic mitochondrial dysfunction and apoptosis that disrupted glucose homeostasis and caused systemic energy deficiency, thereby promoting shoaling as an energetically compensatory strategy. The energy imbalance subsequently triggered oxidative neurotoxicity and perturbed serotonergic, cholinergic, dopaminergic, and GABAergic pathways. Moreover, MPs disrupted the intestinal physicochemical barrier, immune function, and reshaped microbiota, exacerbating neurotransmitter disruption via the gut-brain axis. These findings demonstrate that environmentally relevant MPs exposure can enhance fish shoaling through energy deficiency-driven gut-brain axis dysregulation, revealing the mechanisms by which MPs stress can reorganize population-level behavior and thereby expand understanding of the ecological risks posed by contaminants of emerging concerns.