Elsevier

Aquaculture

Volume 268, Issues 1–4, 22 August 2007, Pages 82-97
Aquaculture

Digestive physiology of marine fish larvae: Hormonal control and processing capacity for proteins, peptides and amino acids

https://doi.org/10.1016/j.aquaculture.2007.04.031Get rights and content

Abstract

For the majority of marine fish larvae a fully developed digestive tract, including gastric digestion, is acquired weeks to months (depending on species) after onset of exogenous feeding. Still, the processing capacity (capability to degrade and absorb dietary nutrients) of the larval gut is sufficient to support fast larval growth by digesting prey naturally available in the sea. However, the physiological constraints of the gut with respect to digestion of cultivated live prey and particularly formulated starter feeds still remain to be elucidated. This paper reviews some recent findings in the areas of control and efficiency of digestive function of marine fish larvae. For studies on the hormonal control, the peptide hormone cholecystokinin (CCK) has been targeted, since it is believed to play an important role in controlling digestion in vertebrates. Recent work on the processing capacity include studies of the digestibility and transfer kinetics of macronutrients from live prey and experimental work on absorption of protein, peptides and free amino acids from the lumen of the digestive tract into the tissues of larval fish and how this changes during ontogeny. The molecular and in vitro characterization of transporters is currently being integrated with ongoing in vivo studies.

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)

  • J.N. Crawley et al.

    Biological actions of cholecystokinin

    Peptides

    (1994)
  • K. Dabrowski et al.

    The smallest vertebrates, teleost fish, can utilize synthetic dipeptide-based diets

    J. Nutr.

    (2003)
  • D. Dottavio-Martin et al.

    Radiolabeling of proteins by reductive alkylation with [14C]formaldehyde and sodium cyanoborohydride

    Anal. Biochem.

    (1978)
  • S. Einarsson et al.

    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.

    (1997)
  • H.J. Fyhn

    1st feeding of marine fish larvae — are free amino acids the source of energy

    Aquaculture

    (1989)
  • S. Helland et al.

    Free amino acid and protein content in the planktonic copepod Temora longicornis compared to Artemia franciscana

    Aquaculture

    (2003)
  • H. Jensen et al.

    Identification and distribution of CCK-related peptides and mRNAs in the rainbow trout, Oncorhynchus mykiss

    Biochim. Biophys. Acta

    (2001)
  • A.H. Johnsen

    Phylogeny of the cholecystokinin/gastrin family

    Front. Neuroendocrinol.

    (1998)
  • Y. Kamisaka et al.

    Ontogeny of cholecystokinin (CCK)-immunoreactive cells in the digestive tract of Atlantic halibut, Hippoglossus hippoglossus, larvae

    Gen. Comp. Endocrinol.

    (2001)
  • Y. Kamisaka et al.

    Distribution of cholecystokinin-immunoreactive cells in the digestive tract of the larval teleost, ayu, Plecoglossus altivelis

    Gen. Comp. Endocrinol.

    (2003)
  • Y. Kamisaka et al.

    Cholecystokinin mRNA in Atlantic herring, Clupea harengus — molecular cloning, characterization, and distribution in the digestive tract during the early life stages

    Peptides

    (2005)
  • S.J. Kaushik

    Nutrient requirements, supply and utilisation in the context of carp culture

    Aquaculture

    (1995)
  • S. Kolkovski

    Digestive enzymes in fish larvae and juveniles — implications and applications to formulated diets

    Aquaculture

    (2001)
  • T. Kurokawa et al.

    Development of cholecystokinin and pancreatic polypeptide endocrine systems during the larval stage of Japanese flounder, Paralichthys olivaceus

    Gen. Comp. Endocrinol.

    (2000)
  • T. Kurokawa et al.

    Identification of gastrin and multiple cholecystokinin genes in teleost

    Peptides

    (2003)
  • A. Kvåle et al.

    Leaching properties of three different micropaticulate diets and preference of the diets in cod (Gadus morhua L.) larvae

    Aquaculture

    (2006)
  • X. Lin et al.

    Brain regulation of feeding behavior and food intake in fish

    Comp. Biochem. Physiol.

    (2000)
  • F.S. Luizi et al.

    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

    (1999)
  • E. McLean et al.

    Gastrointestinal delivery of peptide and protein drugs to aquacultured teleosts

    Aquaculture

    (1999)
  • S. Morais et al.

    A method for radiolabeling Artemia with applications in studies of food intake, digestibility, protein and amino acid metabolism in larval fish

    Aquaculture

    (2004)
  • K. Murakami et al.

    Degradation of proteins with blocked amino-groups by cytosolic proteases

    Biochem. Biophys. Res. Commun.

    (1987)
  • P. Peyon et al.

    Molecular cloning and expression of cDNA encoding brain preprocholecystokinin in goldfish

    Peptides

    (1998)
  • E.C. Ray et al.

    Growth factor regulation of enterocyte nutrient transport during intestinal adaptation

    Am. J. Surg.

    (2002)
  • M.J. Rennie et al.

    Latency, duration and dose response relationships of amino acid effects on human muscle protein synthesis

    J. Nutr.

    (2002)
  • I. Rønnestad et al.

    Free amino acids are absorbed faster and assimilated more efficiently than protein in postlarval Senegal sole (Solea senegalensis)

    J. Nutr.

    (2000)
  • I. Rønnestad et al.

    In vivo studies of digestion and nutrient assimilation in marine fish larvae

    Aquaculture

    (2001)
  • I. Rønnestad et al.

    The supply of amino acids during early feeding stages of marine fish larvae: a review of recent findings

    Aquaculture

    (2003)
  • M.B. Rust et al.

    A new method for force-feeding larval fish

    Aquaculture

    (1993)
  • S.K. Tonheim et al.

    In vivo incorporation of [U]-14C-amino acids: an alternative protein labelling procedure for use in examining larval digestive physiology

    Aquaculture

    (2004)
  • S.K. Tonheim et al.

    Pre-hydrolysis improves utilisation of dietary protein in the larval teleost Atlantic halibut (Hippoglossus hippoglossus) L.)

    J. Exp. Mar. Biol. Ecol.

    (2005)
  • T. Verri et al.

    Molecular and functional characterisation of the zebrafish (Danio rerio) PEPT1-type peptide transporter

    FEBS Lett.

    (2003)
  • H. Volkoff et al.

    Neuropeptides and the control of food intake in fish

    Gen. Comp. Endocrinol.

    (2005)
  • K.N. Wallace et al.

    Intestinal growth and differentiation in zebrafish

    Mech. Dev.

    (2005)
  • Y. Boirie et al.

    Slow and fast dietary proteins differently modulate postprandial protein accretion

    Proc. Natl. Acad. Sci. U. S. A.

    (1997)
  • C.L. Cahu et al.

    Maturation of the pancreatic and intestinal digestive functions in sea bass (Dicentrarchus labrax): effect of weaning with different protein sources

    Fish Physiol. Biochem.

    (1995)
  • A.P.C. Carvalho et al.

    First feeding common carp larvae on diets with high levels of protein hydrolysates

    Aquac. Int.

    (1997)
  • A.S.C. Chong et al.

    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.

    (2002)
  • Conceição, L.E.C., 1997. Growth in early life stages of fishes: an explanatory model. PhD thesis, Dept. Fish Culture...
  • L.E.C. Conceição et al.

    Utilization of dietary amino acids in fish larvae: towards an explanatory model

  • L.E.C. Conceição et al.

    Fast growth, protein turnover and costs of protein metabolism in yolk-sac larvae of the African catfish (Clarias gariepinus)

    Fish Physiol. Biochem.

    (1997)
  • Cited by (112)

    • Digestive system ontogeny and the effects of weaning time on larval survival, growth and pigmentation development of orchid dottyback Pseudochromis fridmani

      2022, Aquaculture
      Citation Excerpt :

      Firstly, for precocial fish such as salmonids and wolffish, the stomach is already differentiated at the onset of first feeding (Falk-Petersen and Hansen, 2001; Lazo et al., 2011; Rønnestad et al., 2013; Sahlmann et al., 2015). In contrast, many other marine fish species are altricial, and the functional stomach is often developed late in the larval stage (Govoni et al., 1986; Rønnestad et al., 2013; Rønnestad et al., 2007; Segner et al., 1994). Research on marine foodfish has documented the digestive system ontogeny of diverse pelagic spawning fish (PSF), including cobia Rachycentron canadum (Faulk et al., 2007), coral trout Plectropomus leopardus (Qu et al., 2012), fat snook Centropomus parallelus (Teles et al., 2015), golden pompano Trachinotus ovatus (Ma et al., 2014a), Japanese flounder Paralichthys olivaceus (Khoa et al., 2021b), longfin yellowtail Seriola rivoliana (Teles et al., 2017), meagre Argyrosomus regius (Solovyev et al., 2016), white seabass Atractoscion nobilis (Galaviz et al., 2011), and yellowtail kingfish Seriola lalandi (Chen et al., 2006).

    View all citing articles on Scopus
    View full text