Influences of diet quality and nursery-habitat complexity on brain development and cognitive performance of brown trout (Salmo trutta L.)

Access to omega-3 long-chain polyunsaturated fatty acids (n-3 LC-PUFA), and the physical and social complexity of habitat have been proposed to influence brain development and cognitive ability. We aimed to investigate how juvenile brown trout mitigate dietary n-3 LC-PUFA deprivation in complex habitats, typical of natal streams, by testing the effects of n-3 LC-PUFA deficiency in diet and habitat complexity on somatic growth, cognitive performance, encephalisation, and n-3 LC-PUFA biosynthesis and nutrient routing capacity. Brown trout were raised from egg for seven months post-hatch on either a high (8.91%) or low (1.79%) n-3 LC-PUFA diet; for the final three months, trout were further divided into complex (heavily ornamented tanks with small, changing, populations) or simple habitats (bare tanks with many, constant, inhabitants). Cognitive abilities including recognition, memory and inference were tested by comparing the times required to establish stable hierarchical relationships in agonistic dyadic trials featuring naïve trout and trials in which one of the trout had previously observed the other. Gas chromatography and compound-specific stable hydrogen isotope analysis revealed increased biosynthesis and routing of n-3 LC-PUFA to the brain among trout on n-3 LC-PUFA-deficient diets. Fed ad libitum, trout did not sacrifice somatic growth to fuel biosynthesis and routing of n-3 LC-PUFA, but dietary deficiency in n‑3 LC-PUFA did lead to smaller brains, and smaller brains were associated with lower cognitive performance. Complex habitats gave rise to trout showing better cognitive performance, and were associated with lower somatic growth, but habitat complexity played only minor roles in encephalisation and the n-3 LC-PUFA composition of brain lipids. We conclude that brown trout can only partially compensate for the paucity of dietary n-3 LC-PUFA, and we suggest that cognitive divergences may play a role in the diversification of life-history variants among brown trout in the wild.