The effects of dietary arachidonic acid on Senegalese sole morphogenesis: A synthesis of recent findings

Abstract In this study we evaluated the effects of high dietary arachidonic acid (ARA) levels on prostaglandin \{E2\} (PGE2) and \{E3\} (PGE3) production and their effect on two morphogenetic processes occurring during metamorphosis: the establishment of the juvenile pigmentation pattern and eye migration and remodeling of cranial bones. In this sense, Senegalese sole larvae were fed from 2 to 50 days post-hatch (dph) with live prey enriched with an experimental emulsion containing high levels of \{ARA\} (ARA-H; 10.2 and 7.1% \{TFA\} in enriched rotifer and Artemia, respectively) versus a reference commercial enriching product (Algamac 3050®, AGM; 1.0 and 1.4% \{TFA\} in enriched rotifer and Artemia, respectively). High dietary \{ARA\} levels did not affect larval growth performance at 50 dph, but significantly induced malpigmentation (81.4 ± 7.5%, versus 0.9 ± 0.3% in larvae fed the \{AGM\} diet). This malpigmentation was linked to the higher prostaglandin \{E2\} (PGE2) levels observed in pseudo-albino fish as compared to normally pigmented individuals. The \{PGE2\} levels were higher in normally pigmented specimens fed the ARA-H diet than in those fed the \{AGM\} diet. The effects of \{ARA\} on normally pigmented fish fed the \{AGM\} diet and pseudo-albino specimens fed the ARA-H diet were evaluated by means of the density of melanophores and the texture and image segmentation analyses in the dorsal skin of post-metamorphic fish. The skin of pseudo-albino specimens had a more uniform and homogeneous melanophore pattern than normally pigmented fish. Melanophores in pseudo-albino specimens were less abundant and not so aggregated in patches as they were in normally pigmented ones, whereas their shape differed (round vs. dendritic) suggesting their inability to disperse melanin. In addition, fish fed the ARA-H diet presented a higher percentage of cranial deformities (95.1 ± 1.5%) than those fed the control diet (1.9 ± 1.9%) that was significantly and negatively correlated with the incidence of normally-pigmented animals (R2 = − 0.88, P < 0.001). Cranial deformities in pseudo-albino fish were associated with an impaired migration of the eye from the ocular side (the right eye), whereas the left eye migrated from the blind side into the ocular side almost normally. The effects of high dietary \{ARA\} levels in the eye migration and cranial bone remodeling processes in post-metamorphic larvae were evaluated by means of the staining of cranial skeletal elements. Pseudo-albino fish showed higher interocular distance and head height than normally pigmented individuals, a different disposition of the eyes with regard to the vertebral column and mouth axes, and a distinct osteological development of some skeletal structures from the neuro- and splanchnocranium, in relation to high dietary \{ARA\} contents and high \{PGE2\} production. These results brought new information about possible nutritional forcing factors and physiological mechanisms of pigmentary disorders and impaired eye migration, which are current major bottlenecks in flatfish aquaculture.