Effects of fish size and diet adaptation on growth performances and nitrogen utilization of rainbow trout (Oncorhynchus mykiss W.) juveniles given diets based on free and/or protein-bound amino acids
Highlights
► Dietary protein quality depends of the molecular form of the nitrogen in trout. ► This quality is modulated by the ratio of free to protein-bound amino acids. ► Free amino acid utilization depends of juvenile size and diet adaptation. ► Larger fish can tolerated higher free amino acids in their diet than smaller ones. ► Accustomed fish can tolerate higher level of free amino acids in their diet.
Introduction
The quality of dietary protein is an important factor influencing the growth performance of a fish. Dietary protein quality is usually assessed by amino acid (AA) composition, protein digestibility and protein utilization efficiency. Some observations have shown that the molecular form of the ingested nitrogen (free (F) AA, peptides or proteins) affects growth rate, AA absorption kinetics, the degree of whole-body AA oxidation and utilization for protein synthesis in fish as well as in mammals (Collin-Vidal et al., 1994, Dabrowski et al., 2003, Daenzer et al., 2001, Metges et al., 2000, Terjesen et al., 2006, Zhang et al., 2006), raising the question as to whether this variable may also affect protein quality. This question is of great economical and environmental importance in the context of fishmeal shortage, particularly when fishmeal is replaced by AA-deficient proteins that need to be supplemented with free (F) indispensable (I) AA, in order to meet the requirements of the targeted fish species (Cheng et al., 2003, Davies and Morris, 1997, Nang Thu et al., 2007, Nang Thu et al., 2009, National Research Council (NRC), 2011, Watanabe et al., 1997).
Several authors have attempted to define the AA requirements for different fish species (Wilson, 2003). However, in many instances, the observed differences between studies exceeded credibility (Dabrowski and Guderley, 2002). For instance, tryptophane requirements of rainbow trout (Oncorhynchus mykiss) ranged from 0.5 to 1.4% and methionine requirements in salmonids were estimated from 2.2% in rainbow trout to 4.0% in chinook salmon (O. tshawytscha) (Akiyama et al., 1997). Several factors have been proposed to explain these large variations, being either nutritional or methodological (Bodin et al., 2007, Bodin et al., 2009, Rollin et al., 2003a). According to Dabrowski and Guderley (2002), the questionable formulation of test diets to secure acceptability and maximize growth of fish is the single, most important factor resulting in discrepancies observed in published IAA requirements in fish. Diet formulation for IAA requirement are based entirely, or in variable proportions, on synthetic FAA (Bureau and Encarnação, 2006, Dabrowski and Guderley, 2002). This approach, presuming that these FAA are able to sustain close to optimal growth and are utilized with the same efficiency as the AA derived from dietary proteins, has been questioned by several authors (Dabrowski and Guderley, 2002, Nolles et al., 2008, Rollin, 1999). Therefore, it seems that more studies are required to test this hypothesis.
In 1970, Aoe and colleagues started a still ongoing discussion as to whether the nutritional value of FAA and protein of similar AA composition in the diet of rainbow trout is equivalent (Abboudi et al., 2006, Aoe et al., 1970, Barroso et al., 1999, Cowey, 1992, Cowey, 1994, Cowey and Luquet, 1983, Cowey and Walton, 1988, Dabrowski and Guderley, 2002, Dabrowski et al., 2003, Espe and Njaa, 1991, Kim et al., 1991, Rodehutscord et al., 1995, Rollin et al., 2003a, Rollin et al., 2006, Terjesen et al., 2006). Some authors concluded that FAA can replace protein-bound AA in diets of rainbow trout (Murai, 1992, Rodehutscord et al., 1995) while other obtained sometimes dramatically reduced growth performances when intact protein sources were substituted by FAA mixtures equivalent to their AA composition (Barroso et al., 1999, Cowey and Luquet, 1983, Cowey and Walton, 1988, Dabrowski et al., 2003, Terjesen et al., 2006). These contrasting results could possibly be related to differences of dietary FAA level, fish size and development stage as well as diet adaptation to these FAA-rich diets. Here we propose to investigate the effect of those three variables and to optimize the ratio of FAA to protein in experimental diets aimed at examining requirements for individual AA in rainbow trout juveniles.
The aim of this work was to study the effect of total or partial replacement of cod muscle meal protein, essentially composed of protein-bound AA, by mixtures of FAA of equivalent AA composition on growth performances and nitrogen deposition and utilization in rainbow trout at two juvenile sizes during three feeding periods. The maximum substitution levels that still support reasonable growth or nitrogen utilization efficiency was evaluated for both juvenile sizes at each period.
Section snippets
Experimental diets
Five isonitrogenous (64 g N/kg DM) and isoenergetic (± 18.75 MJ kg/DM) diets (Table 1) were formulated. The dietary N was supplied by gelatin and by cod muscle meal and/or FAA. The cod muscle meal, obtained from a commercial source (Toro Food Division, Rieber and Søn AS, Bergen, Norway), was obtained by freeze-drying muscle of Atlantic cod (Gadus morhua). Its nitrogen content is high (14.7% DM) and was reported earlier to be highly digestible (apparent digestibility of 94.5%) and to provoke high
Growth performances and voluntary feed intake
During the feeding trial, all diets were well accepted by the fish. Mean mortality rate was less than 0.02% per day and was not related to dietary treatments.
Fig. 1A shows the responses for the whole experimental duration of the daily growth coefficient (DGC, % per day) to dietary treatments. Significant differences were observed between diets D0 and D50, D50 and D75 for the larger juveniles and between diets D75 and D100 for both sizes of juvenile. Body weight gain (g/fish) was reduced by 71%
Discussion
The nutritional value of FAA as compared to protein-bound AA is still controversial in fish nutrition for many species (for a review, see Dabrowski and Guderley, 2002) and rainbow trout is not an exception. Some authors concluded that FAA can replace protein-bound AA in experimental diets of rainbow trout (Kim, 1997, Kim et al., 1991, Rodehutscord et al., 1995) while others concluded to sometimes dramatically inferior performances for FAA-rich diets (Aoe et al., 1970, Barroso et al., 1999,
Acknowledgements
The authors thank Marc Michotte for expert technical assistance and the Université catholique de Louvain for funding. The authors wish to thank the two referees for their constructive comments that improved the present manuscript.
References (76)
- et al.
Protein and lysine requirements for maintenance and for tissue accretion in Atlantic salmon (Salmo salar) fry
Aquaculture
(2006) - et al.
The effect of dispensable amino acids on nitrogen and amino acid losses in Atlantic salmon (Salmo salar L) fry fed a protein-free diet
Aquaculture
(2009) - et al.
Growth rate estimates for cultured Atlantic salmon and rainbow trout
Aquaculture
(1987) - et al.
Kinetic behavior and protein expression of hepatic NADPH-production systems during development of rainbow trout (Oncorhynchus mykiss)
Aquaculture
(1999) - et al.
Postprandial kinetics of dietary amino acids are the main determinant of their metabolism after soy or milk protein digestion in humans
The Journal of Nutrition
(2003) - et al.
Effect of lysine supplementation in plant protein-based diets on the performance of rainbow trout (Oncorhynchus mykiss) and apparent digestibility coefficients of nutrients
Aquaculture
(2003) - et al.
Dietary arginine requirement of young rainbow trout (Oncorhynchus mykiss)
Comparative Biochemistry and Physiology
(1992) Nutrition—estimating requirements of rainbow trout
Aquaculture
(1992)Amino acid requirements of fish: a critical appraisal of present values
Aquaculture
(1994)Ontogenic aspects of nutritional requirements in fish
Comparative Biochemistry and Physiology
(1986)
Digestion of protein by rainbow trout (Salmo gairdneri Rich.) and absorption of amino acids within the alimentary tract
Comparative Biochemistry and Physiology
The smallest vertebrate, teleost fish, can utilize synthetic dipeptide-based diets
The Journal of Nutrition
The effect of dietary indispensable amino acid imbalances on feed intake: is there a sensing of deficiency and neural signaling present in fish?
Aquaculture
Whole-body nitrogen and splanchnic amino acid metabolism differ in rats fed mixed diets containing casein or its corresponding amino acid mixture
The Journal of Nutrition
Do Atlantic Salmon (Salmo salar) utilize mixtures of free amino acids to the same extent as intact protein sources for muscle protein synthesis?
Comparative Biochemistry and Physiology
Influence of dietary non-essential amino acid profile on growth performance and amino acid metabolism of Nile tilapia, Oreochromis niloticus (L.)
Comparative Biochemistry and Physiology
The influence of the dietary inclusion of the alkaloid gramine, on rainbow trout (Oncorhynchus mykiss) growth, feed utilisation and gastrointestinal histology
Aquaculture
Nutrition of salmonid fishes. IV. An amino acid test diet for Chinook salmon
The Journal of Nutrition
Re-evaluation of protein and amino acid requirements of rainbow trout (Oncorhynchus mykiss)
Aquaculture
Purified diet development and re-evaluation of the dietary protein requirement of fingerling rainbow trout (Oncorhynchus mykiss)
Aquaculture
Effects of coating and encapsulation of crystalline amino acids on leaching in larval feeds
Aquaculture
Partial replacement of dietary protein nitrogen with dispensable amino acids in diets of Nile tilapia, Oreochromis niloticus
Comparative Biochemistry and Physiology
A high-protein meal exceeds anabolic and catabolic capacities in rats adapted to a normal protein diet
The Journal of Nutrition
Protein nutrition of rainbow trout
Aquaculture
Comparison of the lysine utilization efficiency in different plant protein sources supplemented with l-lysine·HCl in rainbow trout (Oncorhynchus mykiss) fry
Aquaculture
Protein level does not affect the lysine utilization efficiency at marginal lysine intake in growing rainbow trout (Oncorhynchus mykiss) fry
Aquaculture
Reduced growth and feed consumption of Atlantic salmon (Salmo salar L.) fed fish meal made from stale fish is not due to increased content of biogenic amines
Aquaculture
The effect of dietary protein replacement by crystalline amino acid on growth and nitrogen utilization of turbot Scophthalmus maximus juveniles
Aquaculture
Effect of the dietary essential amino acid pattern on growth, feed utilization and nitrogen metabolism of European sea bass (Dicentrarchus labrax)
Aquaculture
Free amino acids can replace protein-bound amino acids in test diets for studies in rainbow trout (Oncorhynchus mykiss)
The Journal of Nutrition
The effects of dietary lipid and strain difference on polyunsaturated fatty acid composition and conversion in anadromous and landlocked salmon (Salmo salar L.) parr
Comparative Biochemistry and Physiology
Free amino acids are absorbed faster and assimilated more efficiently than protein in postlarval Senegal sole (Solea senegalensis)
The Journal of Nutrition
Plasma amino acids in rainbow trout (Oncorhynchus mykiss) fed intact protein or a crystalline amino acid diet
Aquaculture
Coating crystalline methionine with tripalmitin-polyvinyl alcohol slows its absorption in the intestine of Nile tilapia, Oreochromis niloticus
Aquaculture
Optimization of dipeptide–protein mixtures in experimental diet formulations for rainbow trout (Oncorhynchus mykiss) alevins
Aquaculture
Supplemental effects of methionine-enriched plastein in Penaeus japonicus diets
Aquaculture
Influence of feeding diets with and without fish meal by hand and by self-feeders on feed intake, growth and nutrient utilization of juvenile rainbow trout (Oncorhynchus mykiss)
Aquaculture
Determination of the threonine requirement for maintenance in Atlantic salmon (Salmo salar L.) fry with the diet dilution procedure
Aquaculture Nutrition
Cited by (29)
Evaluation of the optimum dietary essential amino acid pattern for adult pacu (Piaractus mesopotamicus)
2021, AquacultureCitation Excerpt :A fixed AA composition of the diet is required to be achieved in AA deletion method based experiments in order to avoid any irregularity in the animal response (Green and Hardy, 2002; Marammazi et al., 2017; Peres and Oliva-Teles, 2009; Wang and Fuller, 1989). The desired AA profile of the experimental diets used in this study was obtained through the combination of crystalline AAs and intact protein which is relatively a practical approach (Ambardekar et al., 2009; Bodin et al., 2012). The specified crystalline AA mix (including both the EAAs and non-EAAs) was used only to guarantee the required nutritional composition.
The influence of diet on the early development of two seahorse species (H. guttulatus and H. reidi): Traditional and innovative approaches
2018, AquacultureCitation Excerpt :Also, copepods are preferred to Artemia nauplii during the first days of development in H. guttulatus (Blanco and Planas, 2015). Differences in the digestion efficiency of live preys mainly depends on their biochemical composition (e.g. nutritional profile) and permeability of the exoskeleton, their digestion and on the developmental stage of fishes (Rainuzzo et al., 1997; Bodin et al., 2012). Previous studies suggested that Artemia is hardly digested by early life stages of fish, including seahorses (Olivotto et al., 2011; Planas et al., 2012; Blanco et al., 2015).
Effects of dietary amino acid patterns on growth, feed utilization and hepatic IGF-I, TOR gene expression levels of hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂) juveniles
2017, AquacultureCitation Excerpt :Proteins also have numerous structural and metabolic functions, and thus protein is an essential component for every type of cell in the body, including muscles, bones, organs, tendons, and ligaments (NRC, 2011). All dietary proteins are not identical in their nutritive value, which is a function of their digestibility and amino acid profile (NRC, 2011), and the quality of dietary protein is usually assessed by amino acid (AA) compositions, protein digestibility and protein utilization efficiency (Bodin et al., 2012). An “ideal protein” has been defined as the amino acid profile that meets exactly the requirement of the animal with no excess or deficit (Wang and Fuller, 1989; Emmert and Baker, 1997), and so defining the ideal dietary amino acid profile has been the focus of a significant number of studies.
Increasing levels of dietary crystalline methionine affect plasma methionine profiles, ammonia excretion, and the expression of genes related to the hepatic intermediary metabolism in rainbow trout (Oncorhynchus mykiss)
2016, Comparative Biochemistry and Physiology Part - B: Biochemistry and Molecular BiologyCitation Excerpt :Fish fed diets meeting their requirement for amino acids have improved nitrogen utilization compare to fish fed amino acid deficient diets (Green and Hardy, 2008). However, the utilization of diets with crystalline amino acids is often still inferior to that of a diet containing only protein-bound amino acids such as a fish meal-based diet (Bodin et al., 2012). An increased understanding on the role of amino acids in the regulation of genes involved in growth and metabolism has been obtained from studies on mammalian species (Fafournoux et al., 2000; Kadowaki and Kanazawa, 2003; Jousse et al., 2004; Avruch et al., 2009), and is rapidly emerging as an independent field of research in fish nutrition (Panserat and Kaushik, 2010).
Graded levels of fish protein hydrolysate in high plant diets for turbot (Scophthalmus maximus): Effects on growth performance and lipid accumulation
2016, AquacultureCitation Excerpt :Only very high levels of fish meal protein replacement by FPH protein reduced the feed utilization. The reduction of feed utilization by FPH could be due to the lower bio-efficacy values of free amino acids contained in protein hydrolysate, which is mainly resulted from the gastrointestinal absorption rate asynchronism between free amino acids and protein-bound amino acids (Espe et al., 1993, 1999; Zarate et al., 1999; Ambardekar et al., 2009; Dabrowski et al., 2010; Bodin et al., 2012; Nunes et al., 2014). However, on the opposite side, high levels of dietary FPH increased the feed intake, which offset its negative effects on feed utilization to some extent.