High dietary arachidonic acid levels affect the process of eye migration and head shape in pseudoalbino Senegalese sole Solea senegalensis early juveniles

Abstract

The effect of high dietary levels of arachidonic acid (ARA) on the eye migration and cranial bone remodelling processes in Senegalese sole Solea senegalensis early juveniles (age: 50 days post hatch) was evaluated by means of geometric morphometric analysis and alizarin red staining of cranial skeletal elements. The incidence of normally pigmented fish fed the control diet was 99·1 ± 0·3% (mean ± s.e.), whereas it was only 18·7 ± 7·5% for those fed high levels of ARA (ARA-H). The frequency of cranial deformities was significantly higher in fish fed ARA-H (95·1 ± 1·5%) than in those fed the control diet (1·9 ± 1·9%). Cranial deformities were significantly and negatively correlated with the incidence of normally pigmented animals (r² = -0·88, P < 0·001, n = 16). Thus, fish displaying pigmentary disorders differed in the position of their eyes with regard to the vertebral column and mouth axes, and by the interocular distance and head height, which were shorter than in fish not displaying pigmentary disorders. In addition to changes in the positioning of both eyes, pseudoalbino fish showed some ARA-induced osteological differences for some of the skeletal elements from the splanchnocranium (e.g. right premaxillary, dentary, angular, lacrimal, ceratohyal and branchiostegal rays) and neurocranium (e.g. sphenotic, left lateral ethmoid and left frontal) by comparison to normally pigmented specimens. Pseudoalbino fish also had teeth in both lower and upper jaws. This is the first study in Pleuronectiformes that describes impaired metamorphic relocation of the ocular side eye, the right eye in the case of S. senegalensis, whereas the left eye migrated into the ocular side almost normally.

The effects of dietary arachidonic acid on bone in flatfish larvae: the last but not the least of the essential fatty acids

“…In Senegalese sole early juveniles fed graded dietary ARA levels (0, 4.5, 10% TFA) during the Artemia feeding period, the incidence of skeletal deformities was low and ranged between 35.7 and 46.2% (Boglino et al., 2012b) in comparison to other studies in this species where skeletal deformities ranged from 40 to 85% of cultured fish (Gavaia et al., , ; Fernández et al., ; Boglino et al., 2012a, ). For the determination of the incidence of skeletal deformities in the caudal fin complex, the fusion of the hypurals 3 and 4 was not considered as a skeletal deformity in the study of Boglino et al.…”

“…The skeleton of Senegalese sole early juveniles fed high dietary ARA levels (7% TFA) during the Artemia feeding phase (8–50 days post hatching, dph) tended to have less mineralization in comparison with those animals fed lower dietary doses of ARA (4.5% TFA) (Boglino et al., 2012b). A second study evaluating the effects of dietary ARA on this species has shown that Senegalese sole early juveniles fed high dietary ARA levels from mouth opening to 50 dph (ARA levels: 10.2 and 7.1% TFA during the rotifer and Artemia feeding phases, respectively) presented reduced mineralization of some skeletal tissues of the neurocranium (anterior margin of the sphenotic, lateral left ethmoid and left frontal bones), as well as cranial anomalies associated to the remodelling process occurring in the cranial region during metamorphosis (Boglino et al., ). Under the above‐mentioned experimental conditions, increasing dietary ARA levels might have disrupted the n–6/n–3 PUFA ratio, particularly the ARA/EPA ratio, leading to unbalanced proportions of PGE 2 and PGE 3 that might be responsible for the reduced bone mineralization.…”

“…For instance, Atlantic salmon Salmo salar fed high n–6/n–3 PUFA ratios (from 3.8 to 6.0) showed a reduction in mineralization of their vertebrae that was associated with increased levels of PGE 2 in blood (Berge et al., ). Although PGE levels were not measured in the first study evaluating the effects of dietary ARA on Senegalese sole skeletogenesis (Boglino et al., 2012b), recent data from the same authors indicated that high dietary levels of ARA might have increased PGE 2 production that lead to a reduction in bone ossification (Boglino et al., ). In this recent study, high levels of PGE 2 might have increased the activity of cyclooxygenase (COX2) in osteoblasts, resulting in a decrease of their proliferation and an increase of their differentiation rates, which might have affected the mineralization of some cranial bones and also resulted in the alteration of some skeletal elements during the sensitive period of cranial remodelling occurring during metamorphosis, as reported previously in developing mice (Greenblatt et al., ).…”

“…To date, most studies dealing with the effect of dietary EFA levels on skeletogenesis in fish have focused their investigation on the role of DHA and EPA (Villeneuve et al., ; Kjørsvik et al., ; Roo et al., ; Dâmaso‐Rodrigues et al., ; Boglino et al., 2012a; Izquierdo et al., ), but only a few have focused on investigating the effects of ARA on bone during fish larval development (Boglino et al., 2012b, ). ARA is the major precursor for eicosanoids synthesis, enhancing the immune system and resistance to stress, among other important physiological processes (Bell and Sargent, ), and it directly competes with EPA for the enzymes involved in prostaglandin biosynthesis.…”

“…In Senegalese sole, skeletal deformities may affect up to 80% of the hatchery reared fish, whereas field studies have shown that wild Senegalese sole larvae showed a low incidence of skeletal deformities (19%) than those found in hatchery reared fish, indicating a selective mortality of wild deformed fish and/or an effect of aquaculture‐related rearing conditions in the development of skeletal deformities in this species (Gavaia et al., ). Therefore, skeletogenesis, as well as the processes of pigmentation and eye migration occurring during metamorphosis, have been studied in detail from an aquaculture point of view (Power et al., ; Gavaia et al., ; Fernández and Gisbert, ; Boglione et al., ,b), as well as the role that different nutrients play on the above‐mentioned developmental processes (Villalta et al., , ; Fernández et al., ; Fernández and Gisbert, ; Boglino et al., 2012b; c, Boglino et al., ; Darias et al., ).…”