Digestive physiology of marine fish larvae: Hormonal control and processing capacity for proteins, peptides and amino acids
Introduction
The major function of the digestive system is to digest/degrade macronutrients from feedstuff into a form that can be easily absorbed, in order to supply dietary nutrients to the body tissues. Most marine fish larvae, including target species for aquaculture, hatch from small, mostly pelagic eggs, and their digestive tracts are still developing at the onset of exogenous feeding. The adult-type of digestive system, including a functional (acid-producing) stomach, is acquired during metamorphosis, weeks to months after first feeding depending on species. The larval-type gut has a processing capacity (capability to degrade and absorb dietary nutrients) that can support very high growth rates, providing that suitable feed is available. Important progress has been made on the development of formulated starter feeds that result in high survival and growth, combined with a low incidence of malformations, but their success still depends on a co-supply of live food organisms (Yúfera et al., 2000). A thorough understanding of digestive function and processing capacity from the onset of exogenous feeding will provide a better basis for the formulation of larval specific diets for marine species.
Section snippets
Hormonal control-involvement of cholecystokinin
Digestion is a complex, but closely orchestrated process, involving enzyme and fluid secretions and motility, culminating in absorption and evacuation. In mammalian systems, these processes have been extensively studied and they are known to be controlled and optimized by the nervous and endocrine systems, as well as by luminal factors, implicating neurotransmitters, hormones, paracrine-, signal transduction- and transcription- factors. The available data on hormonal regulation of the
Processing capacity of the larval digestive system
The digestion of ingested diet ultimately culminates in the absorption of nutrients and in the evacuation of the unabsorbed fraction. The efficiency of the digestive process will depend on many factors, including species, stage of development, diet type, among others. This review will focus mainly on the processing capacity for proteins, peptides and AA in marine fish larvae. Amino acids are crucial substrates for anabolic and catabolic processes associated with protein accretion and growth (
Modelling the digestive and metabolic processing of protein and AA
The use of tracer studies has resulted in a better understanding of AA metabolism in fish larvae (e.g., Conceição et al., 2003, Rønnestad et al., 2003). However, the interpretation of information from tracer studies is often difficult, as data are normally expressed on a percentage basis. In addition, these studies usually compare a limited number of body compartments in a few time points (e.g., Aragão et al., 2004, Morais et al., 2004a, Morais et al., 2004b). Modelling is a holistic approach
Amino acid and peptide transporters
As discussed above, the proteolytic capacity of the gut may be the limiting factor for the absorption rates of ingested proteins into the systemic circulation. However, very little data exist that focus on this relationship and almost nothing is known regarding the mechanisms and ontogenetic changes of protein, peptide and FAA absorption in fish. In general, absorption involves many processes, some of them overlapping. The brush border membrane of the enterocytes in adults express numerous AA
Acknowledgements
I.R. acknowledge continuous support from the Research Council of Norway (165203/S40, 174229/S40, 175021/D15) and a study leave grant from the University of Bergen to the University of Algarve, Faro Portugal.
References (109)
- et al.
Duodenal acidification and intra-arterial injection of CCK8 increase gallbladder motility in the rainbow trout, Oncorhynchus mykiss
Gen. Comp. Endocrinol.
(1992) - et al.
Absorption, assimilation and catabolism of individual free amino acids by larval Atlantic halibut (Hippoglossus hippoglossus)
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.
Regulatory peptides in gastric endocrine cells of the rainbow trout Oncorhynchus mykiss: general distribution and colocalizations
Tissue Cell
(1994) - et al.
Hormonal regulation of the fish gastrointestinal tract
Comp. Biochem. Physiol., A
(2004) - et al.
Substitution of live food by formulated diets in marine fish larvae
Aquaculture
(2001) - et al.
Protein hydrolysate vs. fish meal in compound diets for 10-day old sea bass Dicentrarchus labrax larvae
Aquaculture
(1999) - 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.
A preliminary model for dynamic simulation of growth in fish larvae: application to the African catfish (Clarias gariepinus) and turbot (Scophthalmus maximus)
Aquaculture
(1998) - et al.
Amino acid requirements of fish larvae and post-larvae: new tools and recent findings
Aquaculture
(2003)
Biological actions of cholecystokinin
Peptides
The smallest vertebrates, teleost fish, can utilize synthetic dipeptide-based diets
J. Nutr.
Radiolabeling of proteins by reductive alkylation with [14C]formaldehyde and sodium cyanoborohydride
Anal. Biochem.
Effect of exogenous cholecystokinin on the discharge of the gallbladder and the secretion of trypsin and chymotrypsin from the pancreas of the Atlantic salmon, Salmo salar L.
Comp. Biochem. Physiol.
1st feeding of marine fish larvae — are free amino acids the source of energy
Aquaculture
Free amino acid and protein content in the planktonic copepod Temora longicornis compared to Artemia franciscana
Aquaculture
Identification and distribution of CCK-related peptides and mRNAs in the rainbow trout, Oncorhynchus mykiss
Biochim. Biophys. Acta
Phylogeny of the cholecystokinin/gastrin family
Front. Neuroendocrinol.
Ontogeny of cholecystokinin (CCK)-immunoreactive cells in the digestive tract of Atlantic halibut, Hippoglossus hippoglossus, larvae
Gen. Comp. Endocrinol.
Distribution of cholecystokinin-immunoreactive cells in the digestive tract of the larval teleost, ayu, Plecoglossus altivelis
Gen. Comp. Endocrinol.
Cholecystokinin mRNA in Atlantic herring, Clupea harengus — molecular cloning, characterization, and distribution in the digestive tract during the early life stages
Peptides
Nutrient requirements, supply and utilisation in the context of carp culture
Aquaculture
Digestive enzymes in fish larvae and juveniles — implications and applications to formulated diets
Aquaculture
Development of cholecystokinin and pancreatic polypeptide endocrine systems during the larval stage of Japanese flounder, Paralichthys olivaceus
Gen. Comp. Endocrinol.
Identification of gastrin and multiple cholecystokinin genes in teleost
Peptides
Leaching properties of three different micropaticulate diets and preference of the diets in cod (Gadus morhua L.) larvae
Aquaculture
Brain regulation of feeding behavior and food intake in fish
Comp. Biochem. Physiol.
Further description of the development of digestive organs in Atlantic halibut (Hippoglossus hippoglossus) larvae, with notes on differential absorption of copepod and Artemia prey
Aquaculture
Gastrointestinal delivery of peptide and protein drugs to aquacultured teleosts
Aquaculture
A method for radiolabeling Artemia with applications in studies of food intake, digestibility, protein and amino acid metabolism in larval fish
Aquaculture
Degradation of proteins with blocked amino-groups by cytosolic proteases
Biochem. Biophys. Res. Commun.
Molecular cloning and expression of cDNA encoding brain preprocholecystokinin in goldfish
Peptides
Growth factor regulation of enterocyte nutrient transport during intestinal adaptation
Am. J. Surg.
Latency, duration and dose response relationships of amino acid effects on human muscle protein synthesis
J. Nutr.
Free amino acids are absorbed faster and assimilated more efficiently than protein in postlarval Senegal sole (Solea senegalensis)
J. Nutr.
In vivo studies of digestion and nutrient assimilation in marine fish larvae
Aquaculture
The supply of amino acids during early feeding stages of marine fish larvae: a review of recent findings
Aquaculture
A new method for force-feeding larval fish
Aquaculture
In vivo incorporation of [U]-14C-amino acids: an alternative protein labelling procedure for use in examining larval digestive physiology
Aquaculture
Pre-hydrolysis improves utilisation of dietary protein in the larval teleost Atlantic halibut (Hippoglossus hippoglossus) L.)
J. Exp. Mar. Biol. Ecol.
Molecular and functional characterisation of the zebrafish (Danio rerio) PEPT1-type peptide transporter
FEBS Lett.
Neuropeptides and the control of food intake in fish
Gen. Comp. Endocrinol.
Intestinal growth and differentiation in zebrafish
Mech. Dev.
Slow and fast dietary proteins differently modulate postprandial protein accretion
Proc. Natl. Acad. Sci. U. S. A.
Maturation of the pancreatic and intestinal digestive functions in sea bass (Dicentrarchus labrax): effect of weaning with different protein sources
Fish Physiol. Biochem.
First feeding common carp larvae on diets with high levels of protein hydrolysates
Aquac. Int.
Assessment of dry matter and protein digestibility of selected raw ingredients by discus fish (Symphysodon aequifasciata) using in vivo and in vitro methods
Aquac. Nutr.
Utilization of dietary amino acids in fish larvae: towards an explanatory model
Fast growth, protein turnover and costs of protein metabolism in yolk-sac larvae of the African catfish (Clarias gariepinus)
Fish Physiol. Biochem.
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