Possible Dietary Effects of Insect-Based Diets across Zebrafish (Danio rerio) Generations: A Multidisciplinary Study on the Larval Phase

SIMPLE SUMMARY: Fish meal and fish oil represent the optimal ingredients for aquafeed formulation. However, their partial or complete substitution with more sustainable alternatives, like insects, is required for a further development of the aquaculture sector. Nutritional programming through parental feeding may enhance the ability of the progeny to utilize insect-based diets. In the present study, five experimental diets characterized by increasing fish meal substitution levels with full-fat Black Soldier Fly (Hermetia illucens; BSF) prepupae meal (0%, 25%, 50%, 75% and 100%), used for zebrafish broodstock rearing, were provided to the progeny (first filial generation, F1). The effects of BSF-based diets on F1 zebrafish larvae were investigated through a multidisciplinary approach. No significant differences among the experimental groups were observed in terms of growth, hepatic lipid accumulation and gut health. Furthermore, increasing fish meal substitution levels with BSF prepupae meal resulted in a positive modulation of both stress and immune response. Results demonstrated that nutritional programming via broodstock nutrition should be considered a valuable solution to increase the use of insect meal in aquafeeds formulation and improve fish culture sustainability. ABSTRACT: Insects represent a valuable and sustainable alternative ingredient for aquafeed formulation. However, insect-based diets have often highlighted controversial results in different fish species, especially when high inclusion levels were used. Several studies have demonstrated that nutritional programming through parental feeding may allow the production of fish better adapted to use sub-optimal aquafeed ingredients. To date, this approach has never been explored on insect-based diets. In the present study, five experimental diets characterized by increasing fish meal substitution levels with full-fat Black Soldier Fly (Hermetia illucens; BSF) prepupae meal (0%, 25%, 50%, 75% and 100%) were used to investigate the effects of programming via broodstock nutrition on F1 zebrafish larvae development. The responses of offspring were assayed through biometric, gas chromatographic, histological, and molecular analyses. The results evidenced that the same BSF-based diets provided to adults were able to affect F1 zebrafish larvae fatty acid composition without impairing growth performances, hepatic lipid accumulation and gut health. Groups challenged with higher BSF inclusion with respect to fish meal (50%, 75% and 100%) showed a significant downregulation of stress response markers and a positive modulation of inflammatory cytokines gene expression. The present study evidences that nutritional programming through parental feeding may make it possible to extend the fish meal substitution level with BSF prepupae meal in the diet up to almost 100% without incurring the well-known negative side effects of BSF-based diets.