Ontogeny of the digestive system of meagre Argyrosomus regius reared in a mesocosm, and quantitative changes of lipids in the liver from hatching to juvenile
Highlights
► We describe the ontogeny of the digestive system of meagre in relation to feeding. ► Meagre is a fast growing species, developing rapidly its digestive system. ► Changes in the feeding protocol were reflected in larval feeding preferences. ► A new method for liver lipid content was used to identify malnutrition periods. ► The new method was shown to be useful in improving larval rearing protocols.
Introduction
Meagre (Argyrosomus regius) is a scienid species distributed in the Mediterranean Sea, Black Sea and the Atlantic coast of Europe, with maximum reported weight and total length of 103 kg and 182 cm, respectively (Chao, 1986, Quéro and Vayne, 1987). This species inhabits coastal ecosystems near the continental shelf, and can be found in lagoons or river Deltas (Griffiths and Heemstra, 1995) where it spawns in the spring. Flesh quality is considered exceptional and highly nutritious, and the species name regius (i.e., royal) was given because of its highly esteemed flesh quality (Poli et al., 2003).
Meagre has been considered a good species for the diversification of fin-fish aquaculture in the Mediterranean cage-culture industry (Quèmèner, 2002). Growth rates of > 1 kg year− 1 have been reported (Monfort, 2010), which is many-times more than the growth of currently cultured species such as the gilthead seabream (Sparus aurata) and the European sea bass (Dicentrarchus labrax). In addition, meagre mature at a large size > 4 kg (Schuchardt et al., 2007), which is larger than the harvest size, thus avoiding problems of reduced growth associated with maturation. Although meagre fail to undergo oocyte maturation spontaneously in captivity, recently developed hormonal induction methods have proven effective in controlling spawning (Duncan et al., 2012, Fernández-Palacios et al., 2009a, Mylonas et al., 2011) and producing eggs of sufficient quality and quantity for commercial hatchery production. Larvae and juveniles have been reared with similar facilities and methodologies to other marine fishes using rotifers, Artemia nauplii and inert feeds (Estévez et al., 2007, Fernández-Palacios et al., 2007, Fernández-Palacios et al., 2009b, Hernández -Cruz et al., 2007, Roo et al., 2007, Roo et al., 2009, Roo et al., 2010, Vallés and Estévez, 2009). Therefore, the introduction of meagre in commercial aquaculture in the Mediterranean region may contribute positively to the further growth of the industry. Meagre was first produced in 1997 in France, and once juveniles became available outside France, European production grew from 103 mtn in 2003 to 2377 mtn in 2010 (FAO, 2012).
To optimize larval rearing technology, in order to achieve better production results (i.e., higher survival, less variable growth, reduced cannibalism, lower skeletal deformities, better welfare and reduced cost), it is essential to study the ontogeny of the digestive system in relation to the rearing method and employed feeding protocol. The most critical rearing period is during the early developmental stages, especially during the transition from endogenous to exogenous feeding (Watanabe and Kiron, 1994), and during weaning and the transition from live to artificial feeds (Garcia-Ortega et al., 2003, Hamlin et al., 2000). A number of genetically programmed, species-specific morphological and functional changes are observed in the digestive system of fish at the early developmental stages until metamorphosis to juvenile (Zambonino-Infante et al., 2008). However, the ontogeny of the digestive system exhibits significant plasticity, with temperature (Kamler, 2002) and larval rearing protocol (Papadakis et al., 2009) being the most influential environmental factors affecting the appearance and development of the various structures of the digestive system.
Histological examination of the timing of ontogenetic development of the digestive tract and accessory glands is considered the most accurate method for the evaluation of proper function and, thus, nutritional status of fish larvae (Hamlin et al., 2000). For example, hepatocyte morphology and vacuole formation in the cytoplasm are related to the nutritional status of the larvae (Chen et al., 2007, Gisbert et al., 2004a, O'Connell and Paloma, 1981). Understanding the changes of the digestive system occurring during ontogeny under specific rearing conditions is essential and may provide indicators of the nutritional status of the fish during early stages (Chen et al., 2007, Gisber et al., 2008, Treviño et al., 2011). These indicators, then may aid in the identification of periods of malnutrition of the reared organism and provide information for the optimization of commercial rearing technologies and feeding protocols (Zambonino-Infante et al., 2008). Although the ontogeny of the digestive system is basically similar among teleost fishes, the existence of significant species-specific differences related to the timing of appearance and complete functionality of the various structures or organs, makes it necessary to study each potential species in order to develop optimal rearing protocols (Conceição et al., 2007, Gisber et al., 2008, Zambonino-Infante et al., 2008). Such information is not yet available for the meagre.
The aim of the present study was to describe the ontogeny of the digestive system in meagre from hatching to metamorphosis using the mesocosm rearing system, and relate changes occurring in lipid deposition in the liver with the feeding protocol during rearing of meagre using the mesocosm method. The use of the mesocosm is advantageous in fin-fish larval rearing of species with little information of their nutritional requirements (Divanach and Kentouri, 2000, Koumoundouros et al., 2004) as this rearing system is more similar to the natural conditions. It is expected that the obtained information will aid in the improvement of other more intensive commercial larval rearing protocols for this species.
Section snippets
Materials and methods
Larval rearing was performed at the facilities of the Institute of Marine Biology, Biotechnology and Aquaculture of the Hellenic Centre for Marine Research (HCMR), Iraklion, Crete, Greece. Rearing was based on the mesocosm technology (Divanach, 1985, Divanach and Kentouri, 2000, Kentouri, 1985) as described below.
Results
Growth was best described by the equation TL = 0.3711 dah + 2.265 (R2 = 0.9551) between 0 and 17 dah and by the equation TL = 1.2854 dah − 10.047 (R2 = 0.9884) between 17 and 44 dah until the end of the experimental rearing (Fig. 1).
Discussion
The use of the mesocosm rearing system is advantageous in fin-fish larval rearing, especially in species for which little is known of their nutritional requirements (Divanach and Kentouri, 2000, Koumoundouros et al., 2004). Better production results are achieved mainly due to the greater variety of prey items available, coming from the unfiltered sea water that is used to fill the tank initially (Papandroulakis et al., 2004). This variety of zooplankton that grows in a mesocosm in conjunction
Acknowledgments
Financial support for this study has been provided by the Ministry of Education, Lifelong Learning and Religious Affairs, General Secretariat for Research and Technology, Greece under the Call “Cooperation” of the National Strategic Reference Framework 2007–2013 (SYN09-24-424) to CCM, titled “Development of methods for reproduction and rearing of meagre (Argyrosomus regius) as a means for the enhancement of the competitiveness of aquaculture, with the introduction of new species”.
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