Underwater Noise Induces Cognitive Impairments in Resource-Directed Exploratory Behaviors in Black Rockfish (Sebastes schlegelii) via Disruption of the Microbiota–Gut–Brain and Hypothalamic–Pituitary–Interrenal Axes

The unprecedented expansion of human activities has led to increasing global underwater noise pollution, but its effects on fish behavior and cognition, which are fundamental for learning, decision-making, and survival, as well as the underlying physiological mechanisms remain poorly understood. Here, we exposed juvenile black rockfish (Sebastes schlegelii) to four noise levels for 50 days. The results showed that medium and high noise levels (110 and 130 dB re 1 μPa root mean square (RMS)) significantly impaired growth and induced learning and memory-related deficits in T-maze tests, as evidenced by reduced spatial preference and altered swimming patterns. Noise exposure doubled malondialdehyde levels in the brains and livers of fish, indicating severe lipid peroxidation. Moreover, noise exposure induced dysregulation of the hypothalamic–pituitary–interrenal (HPI) axis, leading to a sustained stress-inflammatory state that further propagated systemic disturbances, including significant alterations in gut microbiota and metabolite profiles. Consistently, the level of N-acetyl-L-leucine, a key microbial-derived metabolite, was reduced in the brain and gut microbial metabolites, suggesting impaired autophagy function. Collectively, these effects may have contributed to neuronal injury and ultimately resulted in behavioral deficits. These findings highlight the critical role of the HPI and “microbiota–gut–brain” axes in mediating noise-induced behavioral changes in a marine fish.