Physical and social enrichment influences the adaptability-related behaviors of black rockfish Sebastes schlegelii: An effect mediated by social behaviors, HPI axis and neurogenesis

Abstract

Environmental enrichment is a promising method to increase fish ecological fitness in hatchery release and to improve fish welfare in the aquaculture industry. However, little is known about the effects of physical and social enrichment on fish behavioral development and the relevant regulatory mechanisms. To address this knowledge gap, a typical aquaculture fish, black rockfish Sebastes schlegelii, was exposed to contrasting environments (i.e., physically enriched environment vs. barren environment, and socially low-density environment vs. high-density environment) for six weeks. Subsequently, the adaptability-related behaviors and social interactions during the captive period were determined, and stress-related physiological parameters and neurogenesis-related gene markers were measured. In general, the fish from an enriched environment expressed significantly higher sheltering propensity and anti-predator ability while less risk-taking frequency than the fish from a barren environment. And meanwhile, the fish from a low-density environment presented significantly less risk-taking behavior and more anti-predator responses than high-density fish. A structurally barren environment significantly increased fish aggressive frequency and locomotor activity compared with an enriched environment, whereas the social environment did not affect fish social interactions. For physiological status, the hypothalamus-pituitary-interrenal (HPI) axis and corticosteroid receptor system activities of barren fish were significantly higher than those of enriched fish, and meanwhile, the high-density fish also presented significantly higher physiological stress than low-density fish. For neurogenesis processes, an enriched environment did not affect fish brain cell proliferation but increased telencephalon neuronal differentiation ratio and immature neuron number. In contrast, a low-density environment significantly stimulated cell proliferating activity in telencephalon but did not affect brain neuronal differentiation activity. These novel results verified the conspicuous effects of physical and social environments on the adaptability-related behaviors in aquaculture fish, and finally, we proposed a novel regulatory pathway for fish behavioral plasticity, i.e., environmental stimuli - social interactions - HPI axis - corticosteroid receptor system - neurogenesis - adaptability-related behaviors. These results may lay the foundations for restoring fishery resources and for improving fish welfare, add novel knowledge to fish biology and environmental enrichment framework, and help deeply understand the mechanisms of environmental effects on marine animal behaviors.