ReviewImproving growth potential in Senegalese sole (Solea senegalensis) through dietary protein
Introduction
Senegalese sole is a robust fast-growing species mostly reared in Portugal and Spain and more recently in France and Italy (FEAP, 2016). The larviculture protocols were successfully established by Dinis et al., 1999, and are nowadays fairly standardized, with post-larvae being routinely produced with good growth and at high survival rates (Morais et al., 2016). However, until recently, some problems have hampered a more successful juvenile production, such as difficulties in weaning, variable growth rates and large size dispersion, which might be related to suboptimal rearing or nutritional conditions during early life stages (Morais et al., 2016).
Due to a growing knowledge on Senegalese sole physiology and recent technological developments, sole production is going through an important expansion: total production of farmed sole has risen from 68 to 1457 t in the period 2007–2015 in Europe (FEAP, 2016). This will inevitably lead to an increase in the demand for high quality juvenile production. This prospective scenery makes it urgent to increase Senegalese sole larvae and juvenile quality, which may be pursued by improving early larvae nutrition.
Live feed nutritional composition is considered as sub-optimal for Senegalese sole larvae on what concerns protein quality (Aragão et al., 2004a, Aragão et al., 2004b) and that has been suggested as a possible cause for the variable growth rates. Using a microdiet to supplement live feed in a co-feeding regime or an earlier weaning have been pointed as possible solutions to overcome the inadequacy of the commonly cultivated zooplantonic species to sole nutritional needs (Engrola et al., 2009). In order to do so, a suitable microdiet must be developed to meet these larvae nutritional needs.
The basis for formulating a commercial microdiet to be introduced from an early stage (first feeding) to Senegalese sole have been set mostly in the last 15 years (reviewed by Conceição et al., 2007; Morais et al., 2016; Engrola et al., 2018; Pinto et al., 2018). Recent projects have largely contributed to the development of commercial microdiets for several flatfish species that showed to be suitable for a successful weaning of Senegalese sole post-larvae (Portuguese projects MICALA, 2010–2012 13,380/QREN, SOLEAWIN 2014–2015 310,305/FEP/71, and EPISOLE PTDC/MAR/110547/2009). A sudden weaning may be achieved at 25-30DAH, and the only significant remaining problem is a large size dispersion. So, there is room for improving the current commercial microdiets and anticipate sudden weaning or to eventually supplement or even definitely replace live feeds at mouth opening.
Section snippets
The role of protein synthesis
Fish growth is mainly driven by protein deposition (Houlihan et al., 1995; Shearer, 1994) and maximal protein deposition and associated carcass lean growth rate determine the nutrient requirements for growth (Schinckel and de Lange, 1996).
Protein deposition or accretion is the net result of the dynamic balance between protein synthesis and protein degradation, in a process called protein turnover (Millward et al., 1975). Protein turnover is the continuous renewal and cycling of tissue proteins
Somatic growth potential and muscle growth
Fish larvae have an allometric growth, with the relative contribution of white muscle increasing throughout development when compared to other tissues, such as liver and the digestive tract (Dabrowski, 1986). Therefore, the efficiency of protein retention and synthesis in skeletal muscle is probably a major determinant of larvae dietary AA requirements throughout development. In fact, skeletal muscle protein deposition was suggested to greatly contribute to overall growth in fish and fish
Dietary protein and epigenetics
It has been recently suggested that an epigenetic event could promote differential gene expression and modulate Senegalese sole muscle growth in response to different rearing temperatures (Campos et al., 2013a). Epigenetic events induce potentially reversible modification of DNA, though not involving modification in the underlying DNA sequence (Berger et al., 2009). Such events occur throughout life and can be influenced by external factors (Anderson et al., 2012). Thus, external effects on the
Dietary effect on protein metabolism and somatic growth
Different diet formulation strategies have been employed to meet the IAA requirements of Senegalese sole larvae so to improve their capacity to utilize and deposit protein throughout metamorphosis and maximize growth potential. In Canada et al. (2016a), dietary protein quality was manipulated by adjusting the dietary AA profile to the larval body AA profile, through a 4% supplementation with encapsulated CAA (Fig.1). This strategy had a positive short-term effect on sole larvae capacity to
Dietary effect on protein metabolism and somatic growth
In Canada et al. (2017), dietary protein complexity was manipulated to improve its digestibility, by including protein hydrolysates with different molecular weights. When comparing a diet mostly based on native protein sources (Intact), a diet mostly based on low MW peptides (<5KDa, HighH), and a diet mostly based on polypeptides ranging from 5 to 70 KDa (PartH), the later promoted growth in metamorphosing larvae (Canada et al., 2017) (Fig.4), which digestive system is still very immature, with
Conclusions
Manipulating dietary protein quality upon different concepts or dietary protein complexity had different effects on the development of the larvae capacity to utilize and retain protein for growth purposes. Changing either the dietary IAA/DAA ratio or protein complexity exerted a strong influence on sole larvae muscle development, by inducing changes in the myogenic processes that were reflected on somatic growth potential. The dietary induced changes in myogenesis were variable: either delayed
Acknowledgements
This work was funded by the Project EPISOLE (FCT) [PTDC/MAR/110547/2009], through project UID/Multi/04326/2013 (Portugal) from FCT (Portugal), and by the project MICALA — I&DT Co-Promoção No. 13380 (Portugal, supported by POAlgarve 21, QREN and European Union). P. Canada was supported by FCT grant SFRH/BD/82149/2011. S. Engrola was supported by FCT investigator grant IF/00482/2014/CP1217/CT0005 funded by the European Social Fund, the Operational Programme Human Potential and the Foundation for
Conflict of interest
The authors declare that they have no conflict of interest.
References (124)
- et al.
Skeletal Muscle Cellularity and Expression of Myogenic Regulatory Factors and Myosin Heavy Chains in Rainbow Trout (Oncorhynchus mykiss): Effects of Changes in Dietary Plant Protein Sources and Amino Acid Profiles. Comparative Biochemistry and Physiology. Part a, Molecular & Integrative Physiology
(2010) - et al.
Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation
J. Nutr. Biochem.
(2012) - et al.
Amino acid pools of rotifers and Artemia under different conditions: nutritional implications for fish larvae
Aquaculture
(2004) - et al.
Estimated amino acid requirements during early ontogeny in fish with different life styles: gilthead seabream (Sparus aurata) and Senegalese sole (Solea senegalensis)
Aquaculture
(2004) - et al.
A balanced dietary amino acid profile improves amino acid retention in post-larval Senegalese sole (Solea senegalensis)
Aquaculture
(2004) - et al.
Expression and activities of pancreatic enzymes in developing sea bass larvae (Dicentrarchus labrax) in relation to intact and hydrolyzed dietary protein; involvement of cholecystokinin
Aquaculture
(2004) - et al.
Thermal conditions during larval pelagic phase influence subsequent somatic growth of Senegalese sole by modulating gene expression and muscle growth dynamics
Aquaculture
(2013) - et al.
Incubation temperature induces changes in muscle cellularity and gene expression in Senegalese sole (Solea senegalensis)
Gene
(2013) - et al.
The supplementation of a microdiet with crystalline indispensable amino-acids affects muscle growth and the expression pattern of related genes in Senegalese sole (Solea senegalensis) larvae
Aquaculture
(2016) - et al.
Dietary protein complexity modulates growth, protein utilisation and the expression of protein digestion-related genes in Senegalese sole larvae
Aquaculture
(2017)
Larval dietary protein complexity affects the regulation of muscle growth and the expression of DNA methyltransferases in Senegalese sole
Aquaculture
Solubility and peptide profile affect the utilization of dietary protein by common carp (Cyprinus carpio) during early larval stages
Aquaculture
Metabolic budgets for lysine and glutamate in unfed herring (Gluea harengus) larvae
Aquaculture
A new method to estimate the relative bioavailability of individual amino acids in fish larvae using C-NMR spectroscopy. Comparative biochemistry and physiology
Biochemistry & molecular biology.
Amino acid requirements of fish larvae and post-larvae: new tools and recent findings
Aquaculture
Nutritional physiology during development of Senegalese sole (Solea senegalensis)
Aquaculture
The effect of dietary indispensable amino acid imbalances on feed intake: is there a sensing of deficiency and neural signaling present in fish?
Aquaculture
A review on the cultivation potential of Solea senegalensis in Spain and in Portugal
Aquaculture
Co-feeding in Senegalese sole larvae with inert diet from mouth opening promotes growth at weaning
Aquaculture
Parental and early-feeding effects of dietary methionine in rainbow trout (Oncorhynchus mykiss)
Aquaculture
Natural carbon stable isotope ratios as indicators of the relative contribution of live and inert diets to growth in larval Senegalese sole (Solea senegalensis)
Aquaculture
Protein synthesis in fish
Effect of exogenous tryptophan on cannibalism, survival and growth in juvenile grouper, Epinephelus coioides
Aquaculture
Muscle development and growth: potential implications for flesh quality in fish
Aquaculture
Growth performance, muscle structure and flesh quality in out-of-season Atlantic salmon (Salmo salar) smolts reared under two different photoperiod regimes
Aquaculture
A little goes long way: improved growth in Atlantic cod (Gadus morhua) fed small amounts of wild zooplankton
Aquaculture
Circadian rhythmicity and photic plasticity of myosin gene transcription in fast skeletal muscle of Atlantic cod (Gadus morhua)
Mar. Genomics
The nutritional regulation of muscle growth and protein turnover
Aquaculture
The effect of dietary protein replacement by crystalline amino acid on growth and nitrogen utilization of turbot Scophthalmus maximus juveniles
Aquaculture
Can dietary aromatic amino acid supplementation be beneficial during fish metamorphosis?
Aquaculture
Towards an early weaning in Senegalese sole: a historical review
Aquaculture
Epigenetic alterations in the brains of Fisher 344 rats induced by long-term administration of folate/methyl-deficient diet
Brain Res.
Hepatic epigenetic phenotype predetermines individual susceptibility to hepatic steatosis in mice fed a lipogenic methyl-deficient diet
J. Hepatol.
Regulation and functions of myogenic regulatory factors in lower vertebrates. Comparative biochemistry and physiology
Biochemistry & molecular biology.
Muscle growth patterns and regulation during fish ontogeny
Gen. Comp. Endocrinol.
Development of digestive enzymes in larvae of Solea senegalensis, Kaup 1858
Aquaculture
Assessment of protein digestive capacity and metabolic utilisation during ontogeny of Senegalese sole larvae: a tracer study using in vivo produced radiolabelled polypeptide fractions
Aquaculture
Dietary methionine level affects growth performance and hepatic gene expression of GH-IGF system and protein turnover regulators in rainbow trout (Oncorhynchus mykiss) fed plant protein-based diets. Comparative biochemistry and physiology
Biochemistry & molecular biology.
Artemia protein is processed very fast in Solea senegalensis larvae: a dynamic simulation model
Aquaculture
The supply of amino acids during early feeding stages of marine fish larvae: a review of recent findings
Aquaculture
Digestive physiology of marine fish larvae: Hormonal control and processing capacity for proteins, peptides and amino acids
Aquaculture
Oral serotonin administration affects the quantity and the quality of macronutrients selection in European sea bass Dicentrarchus labrax L
Physiol. Behav.
Evaluation of bioavailability of individual amino acids in Diplodus puntazzo larvae: Towards the ideal dietary amino acid profile
Aquaculture
Effect of lysine and tyrosine supplementation in the amino acid metabolism of Diplodus sargus larvae fed rotifers
Aquaculture
Different dietary protein levels affect meagre (Argyrosomus regius) larval survival and muscle cellularity
Aquaculture
Growth characteristics of skeletal muscle tissue in Oreochromis niloticus larvae fed on a lysine supplemented diet
J. Fish Biol.
Growth and multiplication of white skeletal muscle fibres in carp larvae in relation to somatic growth rate
J. Fish Biol.
Early decrease in dietary protein:energy ratio by fat addition and ontogenetic changes in muscle growth mechanisms of rainbow trout: short- and long-term effects
Br. J. Nutr.
Maternal dietary protein restriction and excess affects offspring gene expression and methylation of non-SMC subunits of condensin I in liver and skeletal muscle
Epigenetics
A purified test diet for coho salmon, Oncorhynchus kisutch, fry
Bull. Jpn. Soc. Sci. Fish.
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