- Email: [email protected]
Advances in the development of microdiets for gilthead seabream, Sparus aurata: a review
Aquaculture 194 Ž2001. 107–121 www.elsevier.nlrlocateraqua-online
Advances in the development of microdiets for gilthead seabream, Sparus aurata: a review W. Koven a,) , S. Kolkovski b, E. Hadas a , K. Gamsiz c , A. Tandler a a
c
Israel Oceanographic and Limnological Research, The National Center for Mariculture, P.O. Box 1212, Eilat 88112, Israel b Fisheries WA, Fremantle Maritime Centre, 1 Fleet Street, Fremantle, WA 6160, Australia Department of Aquaculture, Faculty of Fisheries, Ege UniÕersity, 35100 BornoÕa, Izmir, Turkey Received 4 February 2000; received in revised form 18 August 2000; accepted 18 August 2000
Abstract The performance of microdiets ŽMDs. for larvae of marine fish is frequently improved when they are co-fed with Artemia. This suggests that nutritional factors in the live food are positively influencing the ingestion, digestion and assimilation of the MD. This paper reviews recent advances in MD development on the gilthead seabream with special emphasis on studies that isolated, identified and tested these live food factors in MD with the aim of improving their performance. MD ingestion rates in gilthead seabream larvae increased up to 120% when the fish were exposed to the visual and chemical stimuli of various concentrations of Artemia nauplii. The free amino acids ŽFAA. alanine, glycine and arginine and the compound betaine were identified from the Artemia rearing medium as metabolites, which stimulated this larval response. Similarly, MD supplemented with phospholipids ŽPL., particularly phosphatidylcholine ŽPC., stimulated feeding activity and was consumed up to 45% better in young larval seabream. Moreover, dietary PC appears to have in parallel andror in tandem a postprandial enhancing effect on lipoprotein synthesis, resulting in improved transport of dietary lipids from the mucosa of the digestive tract to the body tissues.
)
Corresponding author. Tel.: q972-7-6361443; fax: q972-7-6375761. E-mail address: [email protected] ŽW. Koven..
0044-8486r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 Ž 0 0 . 0 0 5 0 1 - 9
108
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
Live food may also contribute exogenous enzymes to the digestion process or provide factors that stimulate larval pancreatic secretions or activate gut zymogens. Seabream larvae ingesting MD supplemented with porcine pancreatic extract Ž0.05% DW diet. showed a 30% increase in assimilation and demonstrated significantly Ž P - 0.05. improved growth. Older seabream larvae showed 6.75 times more radioactivity in tissue lipids when fed 14C-triacylglycerol ŽTAG.-labeled MD supplemented with porcine lipase, while younger larvae demonstrated no improved assimilation. Factors in live Artemia may influence digestion by stimulating an endocrine response. This was shown when Artemia consumed by seabream larvae elicited a 300% increase in the level of the digestive hormone bombesin compared to levels in larvae given only a MD. On the other hand, liposomes containing the FAA methionine ingested by halibut juveniles elicited higher levels of the digestive hormone cholecystokinin ŽCCK. compared to juveniles ingesting liposomes containing physiological saline or fish extract. These studies suggested that mobilizing the native endocrine factors associated with the feeding and digestive processes could improve MD performance in gilthead seabream and other species by maximizing its utilization. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Co-feeding; Microdiets; Attractants; Ingestion rate; Digestion; Assimilation; Gilthead seabream larvae; Endocrine response
1. Introduction Rotifers Ž Brachionus plicatilis . and Artemia nauplii are used extensively worldwide as the dominant live food for the larval stages of both freshwater and marine species with a commercial potential. However, the cost in infrastructure, labor and energy to mass culture these zooplankters represent a significant outlay in investment and running costs. Moreover, the provision of live food is characteristically plagued with variable supply and nutritional quality ŽSorgeloos, 1980; Watanabe et al., 1983.. Consequently, a great deal of interest has been generated to develop an off-the-shelf artificial larval microdiet ŽMD. as an economic live food alternative. Moreover, MD offer the opportunity to introduce nutrients into the larvae that are not available in the live feed ŽRosenlund et al., 1997.. However, larviculture based on MD has proved to be an elusive goal as solving the dual complexities of the evolving nutrient requirements of the larvae and the technology necessary to provide a suitably sized, attractive and digestible food particle for the larvae, has been daunting. Although weaning the larvae from Artemia onto an MD can be achieved at metamorphosis Ž0.5–0.75 g. in many species ŽDabrowski, 1984; Foscarini, 1988; Hardy, 1989., the early introduction of prepared diets as the sole replacement for live food has met with limited success ŽAdron et al., 1974; Barnabe, ´ 1976; Kanazawa et al., 1982; Appelbaum and Van Damme, 1988; Walford et al., 1991.. Early on, workers realized that the poor performance of MD is related to the variable acceptance and attraction of the inert particle for the larvae compounded by inadequate ingestion, digestion and assimilation. Tandler and Kolkovski Ž1991. found that Sparus aurata larvae consumed an experimental MD at about one tenth the rate of feeding live food Ždry weight. which was sufficient as a maintenance ration but could not support good larval growth and survival.
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
109
2. The enigma of co-feeding suggests nutritional factors in the live food are lacking in MD Despite the poor performance of MDs when used exclusively to rear marine fish larvae, results were markedly improved when a MD was co-fed with live Artemia nauplii ŽCorneillie et al., 1989; Fermin and Bolıvar, 1991; Marte and Duray, 1991; ` Tandler and Kolkovski, 1991; Fernandez-Dıaz and Yufera, 1997; Rosenlund et al., ´ ´ ´ 1997.. In seabream larvae, there is a general preference for live food over an inert diet when both are offered simultaneously ŽFernandez-Dıaz ´ ´ et al., 1994.. However, an increase in the ingestion rate of MD in the presence of live food suggests that the zooplankters are stimulating a physiological response in the larvae resulting in improved MD acceptance. This point was illustrated clearly in a co-feeding study by Kolkovski et al. Ž1997a., where gilthead seabream larvae demonstrated an ingestion rate of a 14 C-labeled MD that was positively correlated with the concentration of 3 H-labeled nauplii in the rearing medium up to 9 nauplii mly1 ŽFig. 1.. On the other hand, increasing the concentration to 12 and 15 nauplii mly1 resulted in the ingestion rate of the Artemia continuing to rise significantly from 6.5 to 8 nauplii larvaey1 hy1 , whereas the MD ingestion rate fell from 3 to 1 mg MD larvaey1 hy1 . The diminishing effect of co-feeding above a certain nauplii concentration was presumably due to the attraction of the live food eclipsing the acceptance of the MD. In order to begin to isolate the Artemia factors responsible for the co-feeding phenomenon, Kolkovski et al. Ž1997c. tested the effect of supplementing various extracted Artemia fractions in the MD. These authors found that the addition of
Fig. 1. Ingestion rates of a 14 C MD ŽI. and 3 H Artemia nauplii Žq. given as a combined ration to 20-day-old gilthead seabream larvae Žfrom Kolkovski et al., 1997a..
110
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
Artemia nauplii neutral and polar lipid classes or a non-lipid fraction, separately and in combination, significantly increased MD assimilation by 10–20% in 22-day-old larvae. However, this effect of supplemented fractions diminished with age where only the addition of whole Artemia nauplii or combined Artemia fractions in the MD increased MD assimilation significantly Ž P - 0.05. in 34-day-old larvae. These findings indicated that nutritional and other unidentified factors present in the nauplii, but absent in inert preparations, were positively influencing the ingestion and assimilation of the MD. Clearly, the identification of these factors in live food and their implementation in MD development would contribute to the performance of inert feeds. 3. The modes of influence of dietary factors in Artemia on MD ingestion, digestion and assimilation The above findings suggest three possible modes of influence by Artemia nauplii on the ingestion, digestion and assimilation of MD during co-feeding: Ž1. the influence of MD on ingestion by stimulating feeding activity through visual and chemical stimuli; Ž2. the influence of the biochemical composition of the nauplii on larval digestion and assimilation; Ž3. the influence of dietary factors that influence both feeding activity as well as digestion and assimilation. Kolkovski et al. Ž1997a. found that the MD ingestion rates in seabream larvae, when exposed to the visual and chemical stimuli of various concentrations of Artemia nauplii, increased up to 120% as compared to ingestion rates in larvae that were offered the MD alone ŽFig. 2.. Moreover, both visual and chemical stimuli were found to work synergistically ŽFig. 2.. On the other hand, the magnitude of
Fig. 2. Percent increase of MD ingestion in 20-day-old larvae Žcompared to the control treatment. as a function of visual and chemical Artemia stimuli originating from different Artemia concentrations. The control treatment was larval MD ingestion rate in the absence of Artemia stimuli Žfrom Kolkovski et al., 1997c..
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
111
the influence of these stimuli decreased in older larvae. Since visual acuity as well as neural and olfactory development proceeds with larval age ŽBlaxter, 1968., it is reasonable to assume that the dependence on rudimentary visual and chemical stimulation of the larva by the prey will decrease ŽFernald, 1993. as the larva develops its hunting prowess.
4. The influence of factors in live food on larval MD feeding activity The free amino acids ŽFAA. alanine, glycine and arginine and the ammonium base compound betaine were identified as chemical stimuli of gilthead seabream larvae from the 14 metabolites found in the Artemia-rearing medium ŽKolkovski et al., 1997a.. This was concluded by monitoring the effect of the removal of each of the 14 metabolites on MD ingestion rate in 20-day larvae ŽFig. 3.. Those metabolites absent in the medium and causing a reduction in the MD digestion rate were considered feeding stimulants. In addition and consistent with the previous findings, the degree of influence of these FAAs and betaine on larval ingestion rate, when added to the water at concentrations equivalent to their levels in the rearing medium, was shown to be age-dependent ŽKolkovski et al., 1997b.. The FAA alanine and glycine as well as betaine were incorporated into a w14 Cx labelled MD based on the gelatin-Arabic gum encapsulation of liposomes in a recent study at the National Center of Mariculture ŽNCM.. The MD was tested in 7-day-old gilthead seabream larvae and the ingestion rate measured in the presence or absence of rotifers Ž Brachionus rotundiformis.. In the absence of rotifers, larvae tended to ingest more Ž P ) 0.05. MD incorporating FAA together with the intact protein bovine serum
Fig. 3. The effect of the removal of each of the 14 metabolites in the water medium on MD ingestion rates in 20-day-old larvae Žcompared to the control treatment.. The control was MD ingestion rate in the absence of the metabolites. Bars having the same superscript are not significantly Ž P - 0.05. different from each other Žfrom Kolkovski et al., 1997a..
112
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
albumin ŽBSA. than larvae feeding on MD containing only BSA, or larvae feeding on this MD and simultaneously exposed to added alanine, glycine and betaine in the water column ŽFig. 4.. As expected, in the presence or rotifers there was a reduction in the ingestion rate of all the MD. However, the ingestion rate in larvae feeding on the diet based on the liposome encapsulation of the FAA was significantly Ž P - 0.05. better than the other MD treatments, suggesting that the supplementation of the Artemia FAA stimulated a feeding response even in the presence of rotifers. These findings are consistent with work carried out on salmonids ŽHughes, 1990., weatherfish, abalone and yellowtail ŽHarada et al., 1987; Harada, 1992. where FAA and betaine were also found to be effective attractants. Knutsen Ž1992. found that chemical stimuli have a significant effect on the behavior of turbot and sole larvae at the start of exogenous feeding. An increased swimming activity was associated with Artemia nauplii concentration in Pleuronectes platessa larvae ŽWyatt, 1972; Munk and Kiorboe, 1985. and in response to extracts of Balanus nauplii and the amino acids glycine and L-proline in the larvae of herring Ž Clupea harengus L.; Dempsey, 1978.. Therefore, it is not surprising that these metabolites play an important role in feeding stimulation in
Fig. 4. The ingestion rate of larvae, in the presence and absence of rotifers, when fed with MDs encapsulating liposomes containing BSA only, or BSA and selected FAA Ž BSAq FAA., or BSA only together with the FAA dissolved separately in the water ŽBSAqFAA.. Ingestion rate values having different letters were significantly Ž P - 0.05. different.
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
113
marine fish larvae. However, the level of their presence and the potency of other possible attractants in larval feeding stimulation have yet to be determined.
5. The influence of dietary phospholipids (PL) on larval MD feeding activity Studies carried out at the NCM demonstrated that dietary PL, particularly phosphatidylcholine ŽPC., stimulate early larval feeding activity but did not elicit the same response in older larvae ŽKoven et al., 1993, 1998; Hadas, 1998.. This age-dependent effect is likely a function of the ontogeny of the developing digestive tract which characterizes the larvae of marine teleosts. These authors found that larvae fed with PC-supplemented MD demonstrated up to 35% higher Ž P - 0.05. ingestion rates compared to the non-PL control in 21–26-day-old gilthead larvae, although this effect had diminished in 28–31-day-old larvae ŽHadas, 1998; Koven et al., 1998.. These findings were consistent irrespective of the presence or absence of a double bond in the PL fatty acid moiety ŽKoven et al., 1998.. Furthermore, larvae fed on PC-supplemented MD markedly Ž P - 0.05. outperformed larvae ingesting an MD supplemented with phosphatidylethanolamine ŽPE., the other main membrane PL ŽFig. 5.. This suggests that the active chemical group in PC stimulating feeding activity was the trimethyl grouping of the nitrogen moiety of choline, as this is the sole difference between these two phosphoglycerides. The choline trimethyl grouping is also found in the known fish feed attractant betaine ŽMackie and Mitchell, 1985.. In fact, Harada et al. Ž1987.
Fig. 5. The effect on ingestion rate in 22-day-old seabream larvae when the MD is supplemented with PC with a saturated or mono-unsaturated fatty acid moiety and PE with a saturated fatty acid moiety. The control was larvae fed with non-supplemented MD. Those ingestion rates having the same letter were not significantly Ž P - 0.05. different Žfrom Hadas, 1998..
114
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
reported that this chemical group explained the attraction of PC in yellowtail and showed that replacing the hydrogens in the nitrogen moiety of the PE head alcohol with methyl groupings enhanced its attraction to the fish.
6. The age-dependent influence of dietary PL on larval assimilation The growth-promoting effect of dietary PL, particularly lecithin, for marine fish larvae is well documented ŽKanazawa et al., 1981, 1983a,b, 1985; Teshima et al., 1987; Geurden et al., 1997.. As this benefit may affect the early juvenile stages ŽPoston, 1990a,b., the appetite stimulating properties of dietary PC cannot entirely explain the influence of this dietary PL and suggests that post prandial physiological influences are occurring in parallel andror in tandem. Kolkovski Ž1995. found that PC and lyso-PC supplementation effectively improved the assimilation of MD in 20-day-old seabream larvae. In support of this, Koven et al. Ž1993. showed a significant effect of dietary lecithin on the incorporation of labeled free fatty acid ŽFFA. in body neutral and PL in 21–45-day-old larvae ŽFig. 6.. This was particularly pronounced during early larval development Ž21-day-old larvae. where fish fed on PL-supplemented MD assimilated 6.75 times more 14 C-label than the control non-PL MD.
Fig. 6. Comparison between the effects of dietary lecithin and lipase on larval w14 Cx oleic acid incorporation with age. Effect was measured as the times Ž=. increase in fatty acid absorption in larvae fed on lecithin MD compared to the non-lecithin MD control and larvae fed on lipase MD compared to larvae fed on non-lipase MD control Žfrom Koven et al., 1993..
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
115
The literature suggests two main hypotheses to explain the postprandial benefit of this dietary supplement. One theory contends that dietary PL may be an important factor in the production of lipoproteins and cellular components when the developing fish possess a limited ability for PL synthesis ŽKanazawa et al., 1985; Teshima et al., 1987.. Alternatively, dietary PL, in the absence of sufficient levels of bile salts during early development, may enhance the assimilation of ingested fats by acting as temporary emulsifiers ŽMeyers, 1985; Kanazawa, 1993; Koven et al., 1993.. However, the accumulating evidence from studies on various fish species and crustaceans ŽCoutteau et al., 1997. indicate a central role for dietary PL in lipoprotein synthesis and lipid transport and not as an effective surfactant facilitating lipid digestion. This line of thought was supported by recent findings on gilthead seabream which suggested that dietary PL contributes to lipoprotein production, thereby enhancing the efficiency of lipid transport from the enterocytes lining the digestive tract to the body tissues ŽHadas, 1998.. These results were from trials on 28-day-old seabream larvae where the appetite stimulating effect of dietary PC, mentioned earlier, was no longer significant. Despite similar ingestion rates, larvae fed on w14 Cx-labeled PC-supplemented MD retained only 22% of its absorbed radioactivity in the tissues of the digestive tract, compared to 44% of the absorbed radioactivity found in the tissues of the digestive tract of larvae fed with the non-PL control ŽHadas, 1998.. Moreover, 57% of the radioactivity in the digestive tract of the control larvae was in the triacylglycerol ŽTAG. and FFA fraction compared to 12.5% in larvae feeding on the PC diet ŽHadas, 1998.. The accumulation of neutral lipid in the tissues of the digestive tract of larvae fed on non-PC MD reinforces the conclusion that insufficient lipoprotein synthesis and the subsequent delayed fatty acid transport to the body tissues were occurring. These findings were substantiated by Salhi et al. Ž1999. who found a high incidence of lipid vacuoles in the intestinal mucosa of fish fed a low polar lipid diet, suggesting a reduction in the lipid transport rate from the enterocytes to the blood circulation. Similarly, in freshwater species, Fontagne´ et al. Ž1998. reported that a dietary PL deficiency in larval carp caused an accumulation of fat droplets in the enterocytes of the anterior intestine, whereas diets supplemented with PC from hen egg yolk or soybean prevented intestinal steatosis. Conversely, larvae fed on diets containing the PL, phosphatidylinositol, exhibited intestinal steatosis. These authors concluded as well that dietary PC is necessary for the synthesis of very low-density lipoproteins ŽVLDL. or chylomicrons which are involved in the mobilization of dietary lipids into the body tissues, thereby preventing epithelial steatosis.
7. Do exogenous digestive enzymes influence MD digestion and assimilation? Another mechanism how live food may directly enhance MD digestion and assimilation is by contributing their own enzymes to facilitate the digestion process until the larva’s own alimentary systems is fully differentiated and developed ŽDabrowski and Glogowski, 1977a,b; Lauff and Hofer, 1984.. In support of this, Kolkovski et al. Ž1993. found in gilthead seabream larvae ingesting MD supplemented with a porcine pancreatic extract Ž0.05%., a 30% increase in assimilation and significantly Ž P - 0.05. improved growth. Koven et al. Ž1993. tested the effect of an MD supplemented with porcine lipase
116
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
on the assimilation of dietary w14 Cx glycerol trioleate in various ages of larval seabream. The results showed a 3.42 times increase in radioactivity in the tissue lipids of older larvae fed on lipase MD while no lipase effect was observed in younger seabream fed with the same treatment. The lipase effect in the less developed larvae may have been masked by the inability to absorb the sudden excess of w14 Cx breakdown from the lysis of the dietary labeled TAG. Although these studies showed a supplemented enzyme effect on larval digestion and assimilation, they did not support the hypothesis that live food are directly contributing enzymes to the larval digestion process. In fact, Moyano et al. Ž1996. found no evidence of rotifers or Artemia supplying proteases for digestion in various ages of seabream larvae. Zambonino and Cahu Ž1994. claimed as well that enzyme contribution from live food to the larval digestive process was minimal. In support of this, Cahu et al. Ž1995. reported that the Artemia contribution to total trypsin activity of 20-day-old European seabrass larvae was not more than 5%. In seabass and seabream, a general increase in enzyme activity observed between days 3 and 6 coincided with the mouth opening, suggesting it was genetically determined and independent of food intake ŽSarasquete et al., 1995; Cahu and Zambonino Infante, 1994; Moyano et al., 1996.. However, enzyme activities can be a function of the nature of the diet in older larvae. Higher specific activities, except for trypsin, were found in whole body homogenates of seabass larvae ingesting an MD compared to larvae feeding on live food ŽZambonino and Cahu, 1994.. On the other hand, larvae fed with inert feed demonstrated poorer growth than larvae ingesting Artemia, suggesting that nutrient factors in the zooplankters may have affected its ingestion, digestibility and assimilation. In fact, the products of live prey autolysis, possibly including neurohormonal factors ŽChan and Hale, 1992., may stimulate secretions of trypsinogen and other enzymes from the pancreas andror activate gut zymogens ŽLe Ruyet et al., 1993; Zambonino and Cahu, 1994; Moyano et al., 1996.. In other words, although a direct and significant contribution of enzymes by the live food to larval digestion has not been demonstrated, ingested zooplankters may instead be releasing post-prandial factors that stimulate enzyme secretion.
8. Dietary factors in live food influencing digestion by stimulating an endocrine response It is well documented that nutrients such as FAAs and FFAs entering the mammalian digestive tract stimulate an endocrine response that controls digestion and nutrient assimilation as well as influencing feeding behavior and food intake. Bombesin and cholecystokinin ŽCCK., which are pituitary neuropeptides, are an integral part of this gastro-entero-pancreatic endocrine system and have also been reported, or their binding sites, in adult fish ŽBatten et al., 1990; Thorndyke and Holmgren, 1990; Moons et al., 1992; Himick and Peter, 1994a,b.. Bombesin influences digestion by activating the peristaltic movement of the gut and the release of HCl as well as increasing blood circulation to the gut wall ŽMcDonald et al., 1979.. CCK triggers secretion of pancreatic lipases and proteases as well as the contraction of the gall bladder ŽVander et al., 1998..
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
117
The question proposed was if these digestive hormones in developing larvae can be triggered by nutrient factors present in live food that are absent in MD. Kolkovski et al. Ž1997a,b,c., comparing the post prandial stimulation of bombesin in live food and MD, found the level of bombesin increased by 300% when Artemia nauplii were given as the sole food to seabream larvae, compared to levels that were found in larvae offered only a MD. However, the nutrient factors in Artemia responsible for eliciting this endocrine response remain unclear. On the other hand, a post-prandial CCK response was tested in 60-day-old juvenile Atlantic halibut by injecting various liposome treatments into the gut ŽKoven et al., unpublished.. The aqueous phases of the liposome treatments contained one of the following: physiological saline, codfish extract ŽReiber and Son, Bergen, Norway. or the FAA methionine. Codfish extract is a commercial product where 27% of the protein is in an FAA form. Methionine was selected as it is one of the main rate-limiting amino acids for protein synthesis in larvae feeding on Artemia ŽTonheim et al., 2000.. The CCK response was highest in larvae ingesting liposomes containing the FAA methionine compared to larvae injected with the other liposome treatments ŽI. Rønnestad, C. Rojas and R.N. Finn, personal communication, 1999.. These findings suggested that digestive endocrine mechanisms existing in higher vertebrates are similar to those in young fish and that specific FAA in the digestive tract may be required to trigger an endocrine response. Moreover, FAA pools in the live prey of the larvae may be mobilizing native endocrine factors to complete the digestive process in the developing and not fully functional larval digestive tract.
9. Microdiet prototype for gilthead seabream The inability of MD to stimulate an optimal digestive response may explain why they are generally poorly digested and, in extreme cases, may cause blockages of the digestive tract ŽWalford et al., 1991.. However, a recent study reported that the capacity of gilthead seabream to digest encapsulated diets depended on the thickness and rigidity of the capsule coating ŽFernandez-Dıaz 1995.. These authors found, during ´ ´ and Yufera, ´ larval feeding, that thin-walled and soft gelatin microcapsules were more easily degraded than those encapsulated with a harder, thicker and more resistant material. This may suggest that despite the presence of the requisite digestive enzymes ŽMoyano et al., 1996., sufficient quantities of these enzymes were not mobilized by the ingestion of the MD, resulting in the ability to hydrolyze only a less resistant gelatin shell. An improved new version of this MD prototype was recently reported to give comparable growth and survival in 8–15-day-old seabream larvae compared to those feeding on rotifers, suggesting a promising tool for further nutritional research ŽYufera et al., 1999.. ´
10. Conclusion The present review contends that it is insufficient to base MD development on simply imitating the proximate composition of the live food. For optimal MD attraction,
118
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
digestion and assimilation, specific nutrient factors found in live Artemia, which elicit a physiological response in the larvae, should be incorporated in inert feeds. Future MD research should continue to define, isolate and understand the interdependence of those factors in live food that stimulate feeding activity visually and chemically, influence larval digestion, assimilation and transport of nutrients. Special emphasis should be focused on the very promising area of endocrine hormonal control of feeding and digestive enzyme secretion. This could be the primary trigger for digestive processes, which maximize the utilization of MD.
References Adron, J.W., Blair, A., Cowey, C.B., 1974. Rearing of plaice Ž Pleuronectes platessa. larvae to metamorphosis using an artificial diet. Fish. Bull. 72, 353–357. Appelbaum, S., Van Damme, P., 1988. The feasibility of using exclusively dry diet for rearing of Israeli Clarias gariepinus ŽBurchell. larvae and fry. J. Appl. Ichthyol. 4, 105–110. Barnabe, ´ G., 1976. Elevage larvaire du loup Ž Dicentarchus labrax L.; Pisces, Serranidae. l’aide d’alimentsec compose. ´ Aquaculture 9, 237–252. Batten, T.F.C., Camere, M.L., Moons, L., Vandesande, F., 1990. Comparative distribution of neuropeptide-immunoreactive systems in the brain of the greenmolly, Poecillia latipinna. J. Comp. Neurol. 302, 893–919. Blaxter, J.H.S., 1968. Light intensity, vision and feeding in young plaice. J. Exp. Mar. Biol. Ecol. 2, 293–307. Cahu, C.L., Zambonino Infante, J.L., 1994. Early weaning of sea bass Ž Dicentrarchus labrax . larvae with a compound diet: effect on digestive enzymes. Comp. Biochem. Physiol. 109A, 213–222. Cahu, C.L., Zambonino, J.L., Le Gall, M.M., Quazuguel, P., 1995. Early weaning of seabass: are digestive enzymes limiting? In: Lavens, P., Sorgeloos, P., Jaspers, E., Ollevier, F. ŽEds.., Larvi ’91 Fish and Crustacean Larviculture Symposium, 3–7 September 1995, Gent, Belgium. Eur. Aquacult. Soc., Spec. Pub., vol. 15, pp. 268–275, Gent, Belgium. Chan, C.B., Hale, E., 1992. Effect of somatostatin on intragastric pressure and smooth muscle contactility of the rainbow trout walbaum. J. Fish Biol. 40, 545–556. Corneillie, S., Ollevier, F., Carrascosa, M., Peci, F., Rendon, A., 1989. Reduction of the use of Artemia nauplii by early feeding of sea bream larvae Ž Sparus aurata. with dry food. In: Billard, R., De Pauw, N. ŽEds.., Conference, 2–4 October 1989, Bordeaux, France. Eur. Aquacult. Soc., Spec. Publ., vol. 10, pp. 73–74. Coutteau, P., Geurden, I., Camara, M.R., Bergot, P., Sorgeloos, P., 1997. Review on the dietary effects of phospholipids in fish and crustacean larviculture. Aquaculture 155, 149–164. Dabrowski, K., 1984. The feeding of fish larvae: present Astate of the artB and perspectives. Reprod., Nutr., Dev. 24, 807–833. Dabrowski, K., Glogowski, J., 1977a. Studies on the proteolytic enzymes of invertebrates constituting the food. Hydrobiologia 52, 171–174. Dabrowski, K., Glogowski, J., 1977b. Studies on the role of exogenous proteolytic enzymes in digestive processes in fish. Hydrobiologia 54, 129–134. Dempsey, C.H., 1978. Chemical stimuli as a factor in feeding and intraspecific behaviour of herring larvae Ž Clupea harengus .. J. Mar. Biol. Assoc. U. K. 58, 739–747. Fermin, A.C., Bolıvar, M.E.C., 1991. Larval rearing of Philippine freshwater catfish, Clarias macrocephalus ` ŽGunthr., fed live zooplankton and artificial diet: a preliminary study. Bamidgeh 43, 87–94. Fernald, R.D., 1993. Vision. In: Evans, D.H. ŽEd.., The Physiology of Fishes. CRC Press, Boca Raton, FL, USA, pp. 161–190. Fernandez-Dıaz, M., 1995. Capacity of gilthead seabream, Sparus aurata L., larvae to break down ´ ´ C., Yufera, ´ dietary microcapsules. Aquaculture 134, 269–278. Fernandez-Dıaz, M., 1997. Detecting growth in gilthead seabream, Sparus aurata L., larvae fed ´ ´ C., Yufera, ´ microcapsules. Aquaculture 153, 93–102.
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
119
Fernandez-Dıaz, M., 1994. Feeding behaviour and prey size selection of gilthead ´ ´ C., Pascual, E., Yufera, ´ seabream, Sparus aurata, larvae fed on inert and live food. Mar. Biol. 118, 323–328. Fontagne, ´ S., Geurden, I., Escaffre, A.-M., Bergot, P., 1998. Histological changes induced by dietary phospholipids in intestine and liver of common carp Ž Cyprinus carpio L.. larvae. Aquaculture 161, 213–223. Foscarini, R., 1988. A review: intensive farming for red sea bream Ž Pagrus major . in Japan. Aquaculture 72, 191–246. Geurden, I., Coutteau, P., Sorgeloos, P., 1997. Effect of a dietary phospholipid supplementation on growth and fatty acid composition of European sea bass Ž Dicentrarchus labrax L.. and turbot Ž Scophthalmus maximus L.. juveniles from weaning onwards. Fish Physiol. Biochem. 16, 259–272. Hadas, E., 1998. The influence of dietary phospholipids on feeding rate and absorption of fatty acids in the larvae of the gilthead seabream Ž Sparus aurata.. MSc Thesis. The Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel, 62 pp. Harada, K., 1992. Effect of attractant and repellent mixtures on behavior of the oriental weatherfish Misgurnus anguillicaudatus. Nippon Suisan Gakkaishi 58, 1427–1430. Harada, K., Eguchi, A., Kuosaki, Y., 1987. Feeding attraction activities in the combinations of amino acids and other compounds of abalone, oriental weatherfish and yellowtail. Nippon Suisan Gakkaishi 53, 1483–1489. Hardy, R.W., 1989. Diet preparation. In: Halver, J.E. ŽEd.., Fish Nutrition. 2nd edn. Academic Press, San Diego, CA, USA, pp. 476–544. Himick, B.A., Peter, R.E., 1994a. Bombesin acts to suppress feeding behavior and alter serum growth hormone in gold fish. Physiol. Behav. 55, 65–72. Himick, B.A., Peter, R.E., 1994b. CCKrgastrin-like immunoreactivity in brain and gut, and CCK suppression of feeding in goldfish. Am. J. Physiol. 267, R841–R851. Hughes, G., 1990. Effects of aqueous amino acid solutions on the feed intake of juvenile Atlantic salmon. Salmonid 13, 13–14. Kanazawa, A., 1993. Essential phospholipids of fish and crustaceans. In: Kaushik, S.J., Luaquet, P. ŽEds.., Fish Nutrition in Practice. Biarritz, France, 24–27 June 1993. Les Colloques, vol. 61. INRA, Paris, France, pp. 519–530. Kanazawa, A., Teshima, S., Inamori, S., Iwashita, T., Nagao, A., 1981. Effects of phospholipids on growth, survival rate and incidence of malformation in the larval ayu. Mem. Fac. Fish., Kagoshima Univ. 30, 301–309. Kanazawa, A., Teshima, S., Inamori, S., Sumida, S., Iwashita, T., 1982. Rearing of larval red sea bream and ayu with artificial diets. Mem. Fac. Fish., Kagoshima Univ. 31, 183–192. Kanazawa, A., Teshima, S., Kobayashi, T., Takae, M., Iwashita, T., Uehara, R., 1983a. Necessity of dietary phospholipids for growth of the larval ayu. Mem. Fac. Fish., Kagoshima Univ. 32, 115–120. Kanazawa, A., Teshima, S., Inamori, S., Matsubara, H., 1983b. Effects of dietary phospholipids on growth of the larval red seabream and knife jaw. Mem. Fac. Fish., Kagoshima Univ. 32, 109–114. Kanazawa, A., Teshima, S., Sakamoto, M., 1985. Effects of dietary bonito–egg phospholipids and some phospholipids on growth and survival of the larval ayu, Plecoglossus altiÕelis. J. Appl. Ichthyol. 1, 165–170. Knutsen, J.A., 1992. Feeding behavior of north sea turbot Scophthalmus maximus and dover sole Solea solea larvae elicited by chemical stimuli. Mar. Biol. 113, 543–548. Kolkovski, S., 1995. The mechanism of action of live food on utilization of microdiets in gilthead seabream Sparus aurata larvae. PhD Thesis, The Hebrew University, Jerusalem, 120 pp. Kolkovski, S., Tandler, A., Kissil, G.Wm., Gertler, A., 1993. The effect of dietary exogenous digestive enzymes on ingestion, assimilation, growth and survival of gilthead seabream Ž Sparus aurata, Sparidae, Linnaeus. larvae. Fish Physiol. Biochem. 12, 203–209. Kolkovski, S., Arieli, A., Tandler, A., 1997a. Visual and chemical cues stimulate microdiet ingestion in gilthead seabream, Sparus aurata, larvae. Aquacult. Int. 5, 527–536. Kolkovski, S., Tandler, A., Izquierdo, M.S., 1997b. The effects of live food and dietary digestive enzymes on the efficiency of microdiets for seabass Ž Dicentrarchus labrax . larvae. Aquaculture 148, 313–322. Kolkovski, S., Koven, W.M., Tandler, A., 1997c. The mode of action of Artemia in enhancing utilization of microdiet by gilthead seabream Sparus aurata larvae. Aquaculture 155, 193–205.
120
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
Koven, W.M., Kolkovski, S., Tandler, A., Kissil, G.Wm., Sklan, D., 1993. The effect of dietary lecithin and lipase as a function of age, on n-9 fatty acid incorporation in the tissue lipids of Sparus aurata larvae. Fish Physiol. Biochem. 10, 357–364. Koven, W.M., Parra, G., Kolkovski, S., Tandler, A., 1998. The effect of dietary phosphatidylcholine and its constituent fatty acids on microdiet ingestion and fatty acid absorption rate in gilthead seabream, Sparus aurata, larvae. Aquacult. Nutr. 4, 39–45. Lauff, M., Hofer, R., 1984. Proteolytic enzymes in fish developed and the importance of dietary enzymes. Aquaculture 37, 335–346. Le Ruyet, J.P., Alexandre, J.C., Thebaud, L., Mugnier, C., 1993. Marine fish larvae feeding: formulated diets ´ or live prey? J. World Aquacult. Soc. 24, 211–224. Mackie, A.M., Mitchell, A.I., 1985. Identification of gustatory feeding stimulants for fish applications in aquaculture. In: Cowey, C.B., Mackie, A.M., Bell, J.G. ŽEds.., Nutrition and Feeding in Fish. Academic Press, London, UK, pp. 177–189. Marte, C.L., Duray, M.N., 1991. Microbound larval feed as supplement to live food for milkfish Ž Chanos chanos Forsskal. larvae. In: Lavens, P., Sorgeloos, P., Jaspers, E., Ollevier, F. ŽEds.., Larvi ’91 Fish and Crustacean Larviculture Symposium, 3–7 September 1995, Gent, Belgium. Eur. Aquacult. Soc., Spec. Publ., vol. 15, pp. 175–177, Gent, Belgium. McDonald, T.J., Jornvale, H., Nilsson, G., Vagne, M., Ghatei, M., Bloom, S.R., Mutt, V., 1979. Characterization of gastrin releasing peptide from porcine non-antral gastric tissue. Biochem. Biophys. Res. Commun. 90, 227. Meyers, S.P., 1985. Importance of lipid, lecithin in aquatic diets examined. Feedstuffs 23, 20–21, ŽSeptember.. Moons, L., Batten, T.F., Vandesande, F., 1992. Comparative distribution of substance P ŽSP. and cholecystokinin ŽCCK. binding sites and immunoreactivity in the brain of the sea bass Ž Dicentrarchus labrax .. Gen. Comp. Endocrinol. 73, 270–283. Moyano, F.J., Dıaz, ´ M., Alarcon, ´ Sarasquete, M.C., 1996. Characterization of digestive enzyme activity during larval development of gilthead seabream Ž Sparus aurata.. Fish Physiol. Biochem. 15, 121–130. Munk, P., Kiorboe, T., 1985. Feeding behavior and swimming activity of larval herring Clupea harengus in relation to density of copepod nauplii. Mar. Ecol.: Prog. Ser. 24, 15–21. Poston, H.A., 1990a. Performance of rainbow trout fry fed supplemental soy lecithin and choline. Prog. Fish-Cult. 52, 218–225. Poston, H.A., 1990b. Effect of body size on growth, survival and chemical composition of Atlantic salmon fed soy lecithin and choline. Prog. Fish-Cult. 52, 226–230. Rosenlund, G., Stoss, J., Talbot, C., 1997. Co-feeding marine fish larvae with inert and live diets. Aquaculture 155, 183–191. Salhi, M., Hernandez-Cruz, C.M., Bessonart, M., Izquierdo, M.S., Fernandez-Palacios, H., 1999. Effect of ´ ´ different dietary polar lipid levels on gut and liver histological structure of gilthead seabream Ž Sparus aurata. larvae. Aquaculture 179, 253–263. Sarasquete, M.C., Polo, A., Yufera, M., 1995. Histology and histochemistry of the development of the ´ digestive system of larval gilthead seabream, Sparus aurata L. Aquaculture 130, 79–92. Sorgeloos, P., 1980. The use of the brine shrimp in aquaculture. In: Persoone, G., Sorgeloos, P., Roels, O., Jaspers, E. ŽEds.., The Brine Shrimp Artemia. Ecology, Culturing and Use in Aquaculture, vol. 3. Universal Press, Wetteren, Belgium, pp. 25–46. Tandler, A., Kolkovski, S., 1991. Rates of ingestion and digestibility as limiting factors in the successful use of microdiets in Sparus aurata larval rearing. In: Lavens, P., Sorgeloos, P., Jaspers, E., Ollevier, F. ŽEds.., Larvi ’91 Fish and Crustacean Larviculture Symposium, 3–7 September 1995, Gent, Belgium. Eur. Aquacult. Soc., Spec. Publ., vol. 15, pp. 169–171, Gent, Belgium. Teshima, S., Kanazawa, A., Horinouchi, K., Yamasaki, S., Hirata, H., 1987. Phospholipids of the rotifer, prawn and larval fish. Nippon Suisan Gakkaishi 53, 609–615. Thorndyke, M., Holmgren, S., 1990. Bombesin potentiates the effect of acetylcholine on isolated strips of fish stomach. Regul. Pept. 30, 125–135. Tonheim, S.K., Koven, W., Rønnestad, I., 2000. Enrichment of Artemia with free methionine. Aquaculture Žin press.. Vander, A., Sherman, J., Luciano, D., 1998. Human Physiology: the Mechanisms of Body Function. 7th edn. WCB McGraw-Hill, Boston, MA, USA, 818 pp.
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
121
Walford, J., Lim, T.M., Lam, T.J., 1991. Replacing live food with microencapsulated diets in the rearing of seabass Ž Lates calcarifer . larvae: do the larvae ingest and digest protein-membrane microcapsules? Aquaculture 92, 225–235. Watanabe, T., Kitajima, C., Fujita, S., 1983. Nutritional values of live organisms used in Japan for mass propagation of fish: a review. Aquaculture 34, 115–143. Wyatt, T., 1972. Some effects of food on the growth and behaviour of plaice larvae. Mar. Biol. 14, 210–216. Yufera, M., Pascual, E., Fernandez-Dıaz, ´ ´ ´ C., 1999. A highly efficient microencapsulated food for rearing early larvae of marine fish. Aquaculture 177, 249–256. Zambonino, J.L., Cahu, C., 1994. Development and response to a diet change of some digestive enzymes in sea bas Ž Dicentrarchus labrax . larvae. Fish Physiol. Biochem. 12, 399–408.
Advances in the development of microdiets for gilthead seabream, Sparus aurata: a review W. Koven a,) , S. Kolkovski b, E. Hadas a , K. Gamsiz c , A. Tandler a a
c
Israel Oceanographic and Limnological Research, The National Center for Mariculture, P.O. Box 1212, Eilat 88112, Israel b Fisheries WA, Fremantle Maritime Centre, 1 Fleet Street, Fremantle, WA 6160, Australia Department of Aquaculture, Faculty of Fisheries, Ege UniÕersity, 35100 BornoÕa, Izmir, Turkey Received 4 February 2000; received in revised form 18 August 2000; accepted 18 August 2000
Abstract The performance of microdiets ŽMDs. for larvae of marine fish is frequently improved when they are co-fed with Artemia. This suggests that nutritional factors in the live food are positively influencing the ingestion, digestion and assimilation of the MD. This paper reviews recent advances in MD development on the gilthead seabream with special emphasis on studies that isolated, identified and tested these live food factors in MD with the aim of improving their performance. MD ingestion rates in gilthead seabream larvae increased up to 120% when the fish were exposed to the visual and chemical stimuli of various concentrations of Artemia nauplii. The free amino acids ŽFAA. alanine, glycine and arginine and the compound betaine were identified from the Artemia rearing medium as metabolites, which stimulated this larval response. Similarly, MD supplemented with phospholipids ŽPL., particularly phosphatidylcholine ŽPC., stimulated feeding activity and was consumed up to 45% better in young larval seabream. Moreover, dietary PC appears to have in parallel andror in tandem a postprandial enhancing effect on lipoprotein synthesis, resulting in improved transport of dietary lipids from the mucosa of the digestive tract to the body tissues.
)
Corresponding author. Tel.: q972-7-6361443; fax: q972-7-6375761. E-mail address: [email protected] ŽW. Koven..
0044-8486r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 Ž 0 0 . 0 0 5 0 1 - 9
108
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
Live food may also contribute exogenous enzymes to the digestion process or provide factors that stimulate larval pancreatic secretions or activate gut zymogens. Seabream larvae ingesting MD supplemented with porcine pancreatic extract Ž0.05% DW diet. showed a 30% increase in assimilation and demonstrated significantly Ž P - 0.05. improved growth. Older seabream larvae showed 6.75 times more radioactivity in tissue lipids when fed 14C-triacylglycerol ŽTAG.-labeled MD supplemented with porcine lipase, while younger larvae demonstrated no improved assimilation. Factors in live Artemia may influence digestion by stimulating an endocrine response. This was shown when Artemia consumed by seabream larvae elicited a 300% increase in the level of the digestive hormone bombesin compared to levels in larvae given only a MD. On the other hand, liposomes containing the FAA methionine ingested by halibut juveniles elicited higher levels of the digestive hormone cholecystokinin ŽCCK. compared to juveniles ingesting liposomes containing physiological saline or fish extract. These studies suggested that mobilizing the native endocrine factors associated with the feeding and digestive processes could improve MD performance in gilthead seabream and other species by maximizing its utilization. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Co-feeding; Microdiets; Attractants; Ingestion rate; Digestion; Assimilation; Gilthead seabream larvae; Endocrine response
1. Introduction Rotifers Ž Brachionus plicatilis . and Artemia nauplii are used extensively worldwide as the dominant live food for the larval stages of both freshwater and marine species with a commercial potential. However, the cost in infrastructure, labor and energy to mass culture these zooplankters represent a significant outlay in investment and running costs. Moreover, the provision of live food is characteristically plagued with variable supply and nutritional quality ŽSorgeloos, 1980; Watanabe et al., 1983.. Consequently, a great deal of interest has been generated to develop an off-the-shelf artificial larval microdiet ŽMD. as an economic live food alternative. Moreover, MD offer the opportunity to introduce nutrients into the larvae that are not available in the live feed ŽRosenlund et al., 1997.. However, larviculture based on MD has proved to be an elusive goal as solving the dual complexities of the evolving nutrient requirements of the larvae and the technology necessary to provide a suitably sized, attractive and digestible food particle for the larvae, has been daunting. Although weaning the larvae from Artemia onto an MD can be achieved at metamorphosis Ž0.5–0.75 g. in many species ŽDabrowski, 1984; Foscarini, 1988; Hardy, 1989., the early introduction of prepared diets as the sole replacement for live food has met with limited success ŽAdron et al., 1974; Barnabe, ´ 1976; Kanazawa et al., 1982; Appelbaum and Van Damme, 1988; Walford et al., 1991.. Early on, workers realized that the poor performance of MD is related to the variable acceptance and attraction of the inert particle for the larvae compounded by inadequate ingestion, digestion and assimilation. Tandler and Kolkovski Ž1991. found that Sparus aurata larvae consumed an experimental MD at about one tenth the rate of feeding live food Ždry weight. which was sufficient as a maintenance ration but could not support good larval growth and survival.
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
109
2. The enigma of co-feeding suggests nutritional factors in the live food are lacking in MD Despite the poor performance of MDs when used exclusively to rear marine fish larvae, results were markedly improved when a MD was co-fed with live Artemia nauplii ŽCorneillie et al., 1989; Fermin and Bolıvar, 1991; Marte and Duray, 1991; ` Tandler and Kolkovski, 1991; Fernandez-Dıaz and Yufera, 1997; Rosenlund et al., ´ ´ ´ 1997.. In seabream larvae, there is a general preference for live food over an inert diet when both are offered simultaneously ŽFernandez-Dıaz ´ ´ et al., 1994.. However, an increase in the ingestion rate of MD in the presence of live food suggests that the zooplankters are stimulating a physiological response in the larvae resulting in improved MD acceptance. This point was illustrated clearly in a co-feeding study by Kolkovski et al. Ž1997a., where gilthead seabream larvae demonstrated an ingestion rate of a 14 C-labeled MD that was positively correlated with the concentration of 3 H-labeled nauplii in the rearing medium up to 9 nauplii mly1 ŽFig. 1.. On the other hand, increasing the concentration to 12 and 15 nauplii mly1 resulted in the ingestion rate of the Artemia continuing to rise significantly from 6.5 to 8 nauplii larvaey1 hy1 , whereas the MD ingestion rate fell from 3 to 1 mg MD larvaey1 hy1 . The diminishing effect of co-feeding above a certain nauplii concentration was presumably due to the attraction of the live food eclipsing the acceptance of the MD. In order to begin to isolate the Artemia factors responsible for the co-feeding phenomenon, Kolkovski et al. Ž1997c. tested the effect of supplementing various extracted Artemia fractions in the MD. These authors found that the addition of
Fig. 1. Ingestion rates of a 14 C MD ŽI. and 3 H Artemia nauplii Žq. given as a combined ration to 20-day-old gilthead seabream larvae Žfrom Kolkovski et al., 1997a..
110
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
Artemia nauplii neutral and polar lipid classes or a non-lipid fraction, separately and in combination, significantly increased MD assimilation by 10–20% in 22-day-old larvae. However, this effect of supplemented fractions diminished with age where only the addition of whole Artemia nauplii or combined Artemia fractions in the MD increased MD assimilation significantly Ž P - 0.05. in 34-day-old larvae. These findings indicated that nutritional and other unidentified factors present in the nauplii, but absent in inert preparations, were positively influencing the ingestion and assimilation of the MD. Clearly, the identification of these factors in live food and their implementation in MD development would contribute to the performance of inert feeds. 3. The modes of influence of dietary factors in Artemia on MD ingestion, digestion and assimilation The above findings suggest three possible modes of influence by Artemia nauplii on the ingestion, digestion and assimilation of MD during co-feeding: Ž1. the influence of MD on ingestion by stimulating feeding activity through visual and chemical stimuli; Ž2. the influence of the biochemical composition of the nauplii on larval digestion and assimilation; Ž3. the influence of dietary factors that influence both feeding activity as well as digestion and assimilation. Kolkovski et al. Ž1997a. found that the MD ingestion rates in seabream larvae, when exposed to the visual and chemical stimuli of various concentrations of Artemia nauplii, increased up to 120% as compared to ingestion rates in larvae that were offered the MD alone ŽFig. 2.. Moreover, both visual and chemical stimuli were found to work synergistically ŽFig. 2.. On the other hand, the magnitude of
Fig. 2. Percent increase of MD ingestion in 20-day-old larvae Žcompared to the control treatment. as a function of visual and chemical Artemia stimuli originating from different Artemia concentrations. The control treatment was larval MD ingestion rate in the absence of Artemia stimuli Žfrom Kolkovski et al., 1997c..
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
111
the influence of these stimuli decreased in older larvae. Since visual acuity as well as neural and olfactory development proceeds with larval age ŽBlaxter, 1968., it is reasonable to assume that the dependence on rudimentary visual and chemical stimulation of the larva by the prey will decrease ŽFernald, 1993. as the larva develops its hunting prowess.
4. The influence of factors in live food on larval MD feeding activity The free amino acids ŽFAA. alanine, glycine and arginine and the ammonium base compound betaine were identified as chemical stimuli of gilthead seabream larvae from the 14 metabolites found in the Artemia-rearing medium ŽKolkovski et al., 1997a.. This was concluded by monitoring the effect of the removal of each of the 14 metabolites on MD ingestion rate in 20-day larvae ŽFig. 3.. Those metabolites absent in the medium and causing a reduction in the MD digestion rate were considered feeding stimulants. In addition and consistent with the previous findings, the degree of influence of these FAAs and betaine on larval ingestion rate, when added to the water at concentrations equivalent to their levels in the rearing medium, was shown to be age-dependent ŽKolkovski et al., 1997b.. The FAA alanine and glycine as well as betaine were incorporated into a w14 Cx labelled MD based on the gelatin-Arabic gum encapsulation of liposomes in a recent study at the National Center of Mariculture ŽNCM.. The MD was tested in 7-day-old gilthead seabream larvae and the ingestion rate measured in the presence or absence of rotifers Ž Brachionus rotundiformis.. In the absence of rotifers, larvae tended to ingest more Ž P ) 0.05. MD incorporating FAA together with the intact protein bovine serum
Fig. 3. The effect of the removal of each of the 14 metabolites in the water medium on MD ingestion rates in 20-day-old larvae Žcompared to the control treatment.. The control was MD ingestion rate in the absence of the metabolites. Bars having the same superscript are not significantly Ž P - 0.05. different from each other Žfrom Kolkovski et al., 1997a..
112
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
albumin ŽBSA. than larvae feeding on MD containing only BSA, or larvae feeding on this MD and simultaneously exposed to added alanine, glycine and betaine in the water column ŽFig. 4.. As expected, in the presence or rotifers there was a reduction in the ingestion rate of all the MD. However, the ingestion rate in larvae feeding on the diet based on the liposome encapsulation of the FAA was significantly Ž P - 0.05. better than the other MD treatments, suggesting that the supplementation of the Artemia FAA stimulated a feeding response even in the presence of rotifers. These findings are consistent with work carried out on salmonids ŽHughes, 1990., weatherfish, abalone and yellowtail ŽHarada et al., 1987; Harada, 1992. where FAA and betaine were also found to be effective attractants. Knutsen Ž1992. found that chemical stimuli have a significant effect on the behavior of turbot and sole larvae at the start of exogenous feeding. An increased swimming activity was associated with Artemia nauplii concentration in Pleuronectes platessa larvae ŽWyatt, 1972; Munk and Kiorboe, 1985. and in response to extracts of Balanus nauplii and the amino acids glycine and L-proline in the larvae of herring Ž Clupea harengus L.; Dempsey, 1978.. Therefore, it is not surprising that these metabolites play an important role in feeding stimulation in
Fig. 4. The ingestion rate of larvae, in the presence and absence of rotifers, when fed with MDs encapsulating liposomes containing BSA only, or BSA and selected FAA Ž BSAq FAA., or BSA only together with the FAA dissolved separately in the water ŽBSAqFAA.. Ingestion rate values having different letters were significantly Ž P - 0.05. different.
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
113
marine fish larvae. However, the level of their presence and the potency of other possible attractants in larval feeding stimulation have yet to be determined.
5. The influence of dietary phospholipids (PL) on larval MD feeding activity Studies carried out at the NCM demonstrated that dietary PL, particularly phosphatidylcholine ŽPC., stimulate early larval feeding activity but did not elicit the same response in older larvae ŽKoven et al., 1993, 1998; Hadas, 1998.. This age-dependent effect is likely a function of the ontogeny of the developing digestive tract which characterizes the larvae of marine teleosts. These authors found that larvae fed with PC-supplemented MD demonstrated up to 35% higher Ž P - 0.05. ingestion rates compared to the non-PL control in 21–26-day-old gilthead larvae, although this effect had diminished in 28–31-day-old larvae ŽHadas, 1998; Koven et al., 1998.. These findings were consistent irrespective of the presence or absence of a double bond in the PL fatty acid moiety ŽKoven et al., 1998.. Furthermore, larvae fed on PC-supplemented MD markedly Ž P - 0.05. outperformed larvae ingesting an MD supplemented with phosphatidylethanolamine ŽPE., the other main membrane PL ŽFig. 5.. This suggests that the active chemical group in PC stimulating feeding activity was the trimethyl grouping of the nitrogen moiety of choline, as this is the sole difference between these two phosphoglycerides. The choline trimethyl grouping is also found in the known fish feed attractant betaine ŽMackie and Mitchell, 1985.. In fact, Harada et al. Ž1987.
Fig. 5. The effect on ingestion rate in 22-day-old seabream larvae when the MD is supplemented with PC with a saturated or mono-unsaturated fatty acid moiety and PE with a saturated fatty acid moiety. The control was larvae fed with non-supplemented MD. Those ingestion rates having the same letter were not significantly Ž P - 0.05. different Žfrom Hadas, 1998..
114
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
reported that this chemical group explained the attraction of PC in yellowtail and showed that replacing the hydrogens in the nitrogen moiety of the PE head alcohol with methyl groupings enhanced its attraction to the fish.
6. The age-dependent influence of dietary PL on larval assimilation The growth-promoting effect of dietary PL, particularly lecithin, for marine fish larvae is well documented ŽKanazawa et al., 1981, 1983a,b, 1985; Teshima et al., 1987; Geurden et al., 1997.. As this benefit may affect the early juvenile stages ŽPoston, 1990a,b., the appetite stimulating properties of dietary PC cannot entirely explain the influence of this dietary PL and suggests that post prandial physiological influences are occurring in parallel andror in tandem. Kolkovski Ž1995. found that PC and lyso-PC supplementation effectively improved the assimilation of MD in 20-day-old seabream larvae. In support of this, Koven et al. Ž1993. showed a significant effect of dietary lecithin on the incorporation of labeled free fatty acid ŽFFA. in body neutral and PL in 21–45-day-old larvae ŽFig. 6.. This was particularly pronounced during early larval development Ž21-day-old larvae. where fish fed on PL-supplemented MD assimilated 6.75 times more 14 C-label than the control non-PL MD.
Fig. 6. Comparison between the effects of dietary lecithin and lipase on larval w14 Cx oleic acid incorporation with age. Effect was measured as the times Ž=. increase in fatty acid absorption in larvae fed on lecithin MD compared to the non-lecithin MD control and larvae fed on lipase MD compared to larvae fed on non-lipase MD control Žfrom Koven et al., 1993..
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
115
The literature suggests two main hypotheses to explain the postprandial benefit of this dietary supplement. One theory contends that dietary PL may be an important factor in the production of lipoproteins and cellular components when the developing fish possess a limited ability for PL synthesis ŽKanazawa et al., 1985; Teshima et al., 1987.. Alternatively, dietary PL, in the absence of sufficient levels of bile salts during early development, may enhance the assimilation of ingested fats by acting as temporary emulsifiers ŽMeyers, 1985; Kanazawa, 1993; Koven et al., 1993.. However, the accumulating evidence from studies on various fish species and crustaceans ŽCoutteau et al., 1997. indicate a central role for dietary PL in lipoprotein synthesis and lipid transport and not as an effective surfactant facilitating lipid digestion. This line of thought was supported by recent findings on gilthead seabream which suggested that dietary PL contributes to lipoprotein production, thereby enhancing the efficiency of lipid transport from the enterocytes lining the digestive tract to the body tissues ŽHadas, 1998.. These results were from trials on 28-day-old seabream larvae where the appetite stimulating effect of dietary PC, mentioned earlier, was no longer significant. Despite similar ingestion rates, larvae fed on w14 Cx-labeled PC-supplemented MD retained only 22% of its absorbed radioactivity in the tissues of the digestive tract, compared to 44% of the absorbed radioactivity found in the tissues of the digestive tract of larvae fed with the non-PL control ŽHadas, 1998.. Moreover, 57% of the radioactivity in the digestive tract of the control larvae was in the triacylglycerol ŽTAG. and FFA fraction compared to 12.5% in larvae feeding on the PC diet ŽHadas, 1998.. The accumulation of neutral lipid in the tissues of the digestive tract of larvae fed on non-PC MD reinforces the conclusion that insufficient lipoprotein synthesis and the subsequent delayed fatty acid transport to the body tissues were occurring. These findings were substantiated by Salhi et al. Ž1999. who found a high incidence of lipid vacuoles in the intestinal mucosa of fish fed a low polar lipid diet, suggesting a reduction in the lipid transport rate from the enterocytes to the blood circulation. Similarly, in freshwater species, Fontagne´ et al. Ž1998. reported that a dietary PL deficiency in larval carp caused an accumulation of fat droplets in the enterocytes of the anterior intestine, whereas diets supplemented with PC from hen egg yolk or soybean prevented intestinal steatosis. Conversely, larvae fed on diets containing the PL, phosphatidylinositol, exhibited intestinal steatosis. These authors concluded as well that dietary PC is necessary for the synthesis of very low-density lipoproteins ŽVLDL. or chylomicrons which are involved in the mobilization of dietary lipids into the body tissues, thereby preventing epithelial steatosis.
7. Do exogenous digestive enzymes influence MD digestion and assimilation? Another mechanism how live food may directly enhance MD digestion and assimilation is by contributing their own enzymes to facilitate the digestion process until the larva’s own alimentary systems is fully differentiated and developed ŽDabrowski and Glogowski, 1977a,b; Lauff and Hofer, 1984.. In support of this, Kolkovski et al. Ž1993. found in gilthead seabream larvae ingesting MD supplemented with a porcine pancreatic extract Ž0.05%., a 30% increase in assimilation and significantly Ž P - 0.05. improved growth. Koven et al. Ž1993. tested the effect of an MD supplemented with porcine lipase
116
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
on the assimilation of dietary w14 Cx glycerol trioleate in various ages of larval seabream. The results showed a 3.42 times increase in radioactivity in the tissue lipids of older larvae fed on lipase MD while no lipase effect was observed in younger seabream fed with the same treatment. The lipase effect in the less developed larvae may have been masked by the inability to absorb the sudden excess of w14 Cx breakdown from the lysis of the dietary labeled TAG. Although these studies showed a supplemented enzyme effect on larval digestion and assimilation, they did not support the hypothesis that live food are directly contributing enzymes to the larval digestion process. In fact, Moyano et al. Ž1996. found no evidence of rotifers or Artemia supplying proteases for digestion in various ages of seabream larvae. Zambonino and Cahu Ž1994. claimed as well that enzyme contribution from live food to the larval digestive process was minimal. In support of this, Cahu et al. Ž1995. reported that the Artemia contribution to total trypsin activity of 20-day-old European seabrass larvae was not more than 5%. In seabass and seabream, a general increase in enzyme activity observed between days 3 and 6 coincided with the mouth opening, suggesting it was genetically determined and independent of food intake ŽSarasquete et al., 1995; Cahu and Zambonino Infante, 1994; Moyano et al., 1996.. However, enzyme activities can be a function of the nature of the diet in older larvae. Higher specific activities, except for trypsin, were found in whole body homogenates of seabass larvae ingesting an MD compared to larvae feeding on live food ŽZambonino and Cahu, 1994.. On the other hand, larvae fed with inert feed demonstrated poorer growth than larvae ingesting Artemia, suggesting that nutrient factors in the zooplankters may have affected its ingestion, digestibility and assimilation. In fact, the products of live prey autolysis, possibly including neurohormonal factors ŽChan and Hale, 1992., may stimulate secretions of trypsinogen and other enzymes from the pancreas andror activate gut zymogens ŽLe Ruyet et al., 1993; Zambonino and Cahu, 1994; Moyano et al., 1996.. In other words, although a direct and significant contribution of enzymes by the live food to larval digestion has not been demonstrated, ingested zooplankters may instead be releasing post-prandial factors that stimulate enzyme secretion.
8. Dietary factors in live food influencing digestion by stimulating an endocrine response It is well documented that nutrients such as FAAs and FFAs entering the mammalian digestive tract stimulate an endocrine response that controls digestion and nutrient assimilation as well as influencing feeding behavior and food intake. Bombesin and cholecystokinin ŽCCK., which are pituitary neuropeptides, are an integral part of this gastro-entero-pancreatic endocrine system and have also been reported, or their binding sites, in adult fish ŽBatten et al., 1990; Thorndyke and Holmgren, 1990; Moons et al., 1992; Himick and Peter, 1994a,b.. Bombesin influences digestion by activating the peristaltic movement of the gut and the release of HCl as well as increasing blood circulation to the gut wall ŽMcDonald et al., 1979.. CCK triggers secretion of pancreatic lipases and proteases as well as the contraction of the gall bladder ŽVander et al., 1998..
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
117
The question proposed was if these digestive hormones in developing larvae can be triggered by nutrient factors present in live food that are absent in MD. Kolkovski et al. Ž1997a,b,c., comparing the post prandial stimulation of bombesin in live food and MD, found the level of bombesin increased by 300% when Artemia nauplii were given as the sole food to seabream larvae, compared to levels that were found in larvae offered only a MD. However, the nutrient factors in Artemia responsible for eliciting this endocrine response remain unclear. On the other hand, a post-prandial CCK response was tested in 60-day-old juvenile Atlantic halibut by injecting various liposome treatments into the gut ŽKoven et al., unpublished.. The aqueous phases of the liposome treatments contained one of the following: physiological saline, codfish extract ŽReiber and Son, Bergen, Norway. or the FAA methionine. Codfish extract is a commercial product where 27% of the protein is in an FAA form. Methionine was selected as it is one of the main rate-limiting amino acids for protein synthesis in larvae feeding on Artemia ŽTonheim et al., 2000.. The CCK response was highest in larvae ingesting liposomes containing the FAA methionine compared to larvae injected with the other liposome treatments ŽI. Rønnestad, C. Rojas and R.N. Finn, personal communication, 1999.. These findings suggested that digestive endocrine mechanisms existing in higher vertebrates are similar to those in young fish and that specific FAA in the digestive tract may be required to trigger an endocrine response. Moreover, FAA pools in the live prey of the larvae may be mobilizing native endocrine factors to complete the digestive process in the developing and not fully functional larval digestive tract.
9. Microdiet prototype for gilthead seabream The inability of MD to stimulate an optimal digestive response may explain why they are generally poorly digested and, in extreme cases, may cause blockages of the digestive tract ŽWalford et al., 1991.. However, a recent study reported that the capacity of gilthead seabream to digest encapsulated diets depended on the thickness and rigidity of the capsule coating ŽFernandez-Dıaz 1995.. These authors found, during ´ ´ and Yufera, ´ larval feeding, that thin-walled and soft gelatin microcapsules were more easily degraded than those encapsulated with a harder, thicker and more resistant material. This may suggest that despite the presence of the requisite digestive enzymes ŽMoyano et al., 1996., sufficient quantities of these enzymes were not mobilized by the ingestion of the MD, resulting in the ability to hydrolyze only a less resistant gelatin shell. An improved new version of this MD prototype was recently reported to give comparable growth and survival in 8–15-day-old seabream larvae compared to those feeding on rotifers, suggesting a promising tool for further nutritional research ŽYufera et al., 1999.. ´
10. Conclusion The present review contends that it is insufficient to base MD development on simply imitating the proximate composition of the live food. For optimal MD attraction,
118
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
digestion and assimilation, specific nutrient factors found in live Artemia, which elicit a physiological response in the larvae, should be incorporated in inert feeds. Future MD research should continue to define, isolate and understand the interdependence of those factors in live food that stimulate feeding activity visually and chemically, influence larval digestion, assimilation and transport of nutrients. Special emphasis should be focused on the very promising area of endocrine hormonal control of feeding and digestive enzyme secretion. This could be the primary trigger for digestive processes, which maximize the utilization of MD.
References Adron, J.W., Blair, A., Cowey, C.B., 1974. Rearing of plaice Ž Pleuronectes platessa. larvae to metamorphosis using an artificial diet. Fish. Bull. 72, 353–357. Appelbaum, S., Van Damme, P., 1988. The feasibility of using exclusively dry diet for rearing of Israeli Clarias gariepinus ŽBurchell. larvae and fry. J. Appl. Ichthyol. 4, 105–110. Barnabe, ´ G., 1976. Elevage larvaire du loup Ž Dicentarchus labrax L.; Pisces, Serranidae. l’aide d’alimentsec compose. ´ Aquaculture 9, 237–252. Batten, T.F.C., Camere, M.L., Moons, L., Vandesande, F., 1990. Comparative distribution of neuropeptide-immunoreactive systems in the brain of the greenmolly, Poecillia latipinna. J. Comp. Neurol. 302, 893–919. Blaxter, J.H.S., 1968. Light intensity, vision and feeding in young plaice. J. Exp. Mar. Biol. Ecol. 2, 293–307. Cahu, C.L., Zambonino Infante, J.L., 1994. Early weaning of sea bass Ž Dicentrarchus labrax . larvae with a compound diet: effect on digestive enzymes. Comp. Biochem. Physiol. 109A, 213–222. Cahu, C.L., Zambonino, J.L., Le Gall, M.M., Quazuguel, P., 1995. Early weaning of seabass: are digestive enzymes limiting? In: Lavens, P., Sorgeloos, P., Jaspers, E., Ollevier, F. ŽEds.., Larvi ’91 Fish and Crustacean Larviculture Symposium, 3–7 September 1995, Gent, Belgium. Eur. Aquacult. Soc., Spec. Pub., vol. 15, pp. 268–275, Gent, Belgium. Chan, C.B., Hale, E., 1992. Effect of somatostatin on intragastric pressure and smooth muscle contactility of the rainbow trout walbaum. J. Fish Biol. 40, 545–556. Corneillie, S., Ollevier, F., Carrascosa, M., Peci, F., Rendon, A., 1989. Reduction of the use of Artemia nauplii by early feeding of sea bream larvae Ž Sparus aurata. with dry food. In: Billard, R., De Pauw, N. ŽEds.., Conference, 2–4 October 1989, Bordeaux, France. Eur. Aquacult. Soc., Spec. Publ., vol. 10, pp. 73–74. Coutteau, P., Geurden, I., Camara, M.R., Bergot, P., Sorgeloos, P., 1997. Review on the dietary effects of phospholipids in fish and crustacean larviculture. Aquaculture 155, 149–164. Dabrowski, K., 1984. The feeding of fish larvae: present Astate of the artB and perspectives. Reprod., Nutr., Dev. 24, 807–833. Dabrowski, K., Glogowski, J., 1977a. Studies on the proteolytic enzymes of invertebrates constituting the food. Hydrobiologia 52, 171–174. Dabrowski, K., Glogowski, J., 1977b. Studies on the role of exogenous proteolytic enzymes in digestive processes in fish. Hydrobiologia 54, 129–134. Dempsey, C.H., 1978. Chemical stimuli as a factor in feeding and intraspecific behaviour of herring larvae Ž Clupea harengus .. J. Mar. Biol. Assoc. U. K. 58, 739–747. Fermin, A.C., Bolıvar, M.E.C., 1991. Larval rearing of Philippine freshwater catfish, Clarias macrocephalus ` ŽGunthr., fed live zooplankton and artificial diet: a preliminary study. Bamidgeh 43, 87–94. Fernald, R.D., 1993. Vision. In: Evans, D.H. ŽEd.., The Physiology of Fishes. CRC Press, Boca Raton, FL, USA, pp. 161–190. Fernandez-Dıaz, M., 1995. Capacity of gilthead seabream, Sparus aurata L., larvae to break down ´ ´ C., Yufera, ´ dietary microcapsules. Aquaculture 134, 269–278. Fernandez-Dıaz, M., 1997. Detecting growth in gilthead seabream, Sparus aurata L., larvae fed ´ ´ C., Yufera, ´ microcapsules. Aquaculture 153, 93–102.
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
119
Fernandez-Dıaz, M., 1994. Feeding behaviour and prey size selection of gilthead ´ ´ C., Pascual, E., Yufera, ´ seabream, Sparus aurata, larvae fed on inert and live food. Mar. Biol. 118, 323–328. Fontagne, ´ S., Geurden, I., Escaffre, A.-M., Bergot, P., 1998. Histological changes induced by dietary phospholipids in intestine and liver of common carp Ž Cyprinus carpio L.. larvae. Aquaculture 161, 213–223. Foscarini, R., 1988. A review: intensive farming for red sea bream Ž Pagrus major . in Japan. Aquaculture 72, 191–246. Geurden, I., Coutteau, P., Sorgeloos, P., 1997. Effect of a dietary phospholipid supplementation on growth and fatty acid composition of European sea bass Ž Dicentrarchus labrax L.. and turbot Ž Scophthalmus maximus L.. juveniles from weaning onwards. Fish Physiol. Biochem. 16, 259–272. Hadas, E., 1998. The influence of dietary phospholipids on feeding rate and absorption of fatty acids in the larvae of the gilthead seabream Ž Sparus aurata.. MSc Thesis. The Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel, 62 pp. Harada, K., 1992. Effect of attractant and repellent mixtures on behavior of the oriental weatherfish Misgurnus anguillicaudatus. Nippon Suisan Gakkaishi 58, 1427–1430. Harada, K., Eguchi, A., Kuosaki, Y., 1987. Feeding attraction activities in the combinations of amino acids and other compounds of abalone, oriental weatherfish and yellowtail. Nippon Suisan Gakkaishi 53, 1483–1489. Hardy, R.W., 1989. Diet preparation. In: Halver, J.E. ŽEd.., Fish Nutrition. 2nd edn. Academic Press, San Diego, CA, USA, pp. 476–544. Himick, B.A., Peter, R.E., 1994a. Bombesin acts to suppress feeding behavior and alter serum growth hormone in gold fish. Physiol. Behav. 55, 65–72. Himick, B.A., Peter, R.E., 1994b. CCKrgastrin-like immunoreactivity in brain and gut, and CCK suppression of feeding in goldfish. Am. J. Physiol. 267, R841–R851. Hughes, G., 1990. Effects of aqueous amino acid solutions on the feed intake of juvenile Atlantic salmon. Salmonid 13, 13–14. Kanazawa, A., 1993. Essential phospholipids of fish and crustaceans. In: Kaushik, S.J., Luaquet, P. ŽEds.., Fish Nutrition in Practice. Biarritz, France, 24–27 June 1993. Les Colloques, vol. 61. INRA, Paris, France, pp. 519–530. Kanazawa, A., Teshima, S., Inamori, S., Iwashita, T., Nagao, A., 1981. Effects of phospholipids on growth, survival rate and incidence of malformation in the larval ayu. Mem. Fac. Fish., Kagoshima Univ. 30, 301–309. Kanazawa, A., Teshima, S., Inamori, S., Sumida, S., Iwashita, T., 1982. Rearing of larval red sea bream and ayu with artificial diets. Mem. Fac. Fish., Kagoshima Univ. 31, 183–192. Kanazawa, A., Teshima, S., Kobayashi, T., Takae, M., Iwashita, T., Uehara, R., 1983a. Necessity of dietary phospholipids for growth of the larval ayu. Mem. Fac. Fish., Kagoshima Univ. 32, 115–120. Kanazawa, A., Teshima, S., Inamori, S., Matsubara, H., 1983b. Effects of dietary phospholipids on growth of the larval red seabream and knife jaw. Mem. Fac. Fish., Kagoshima Univ. 32, 109–114. Kanazawa, A., Teshima, S., Sakamoto, M., 1985. Effects of dietary bonito–egg phospholipids and some phospholipids on growth and survival of the larval ayu, Plecoglossus altiÕelis. J. Appl. Ichthyol. 1, 165–170. Knutsen, J.A., 1992. Feeding behavior of north sea turbot Scophthalmus maximus and dover sole Solea solea larvae elicited by chemical stimuli. Mar. Biol. 113, 543–548. Kolkovski, S., 1995. The mechanism of action of live food on utilization of microdiets in gilthead seabream Sparus aurata larvae. PhD Thesis, The Hebrew University, Jerusalem, 120 pp. Kolkovski, S., Tandler, A., Kissil, G.Wm., Gertler, A., 1993. The effect of dietary exogenous digestive enzymes on ingestion, assimilation, growth and survival of gilthead seabream Ž Sparus aurata, Sparidae, Linnaeus. larvae. Fish Physiol. Biochem. 12, 203–209. Kolkovski, S., Arieli, A., Tandler, A., 1997a. Visual and chemical cues stimulate microdiet ingestion in gilthead seabream, Sparus aurata, larvae. Aquacult. Int. 5, 527–536. Kolkovski, S., Tandler, A., Izquierdo, M.S., 1997b. The effects of live food and dietary digestive enzymes on the efficiency of microdiets for seabass Ž Dicentrarchus labrax . larvae. Aquaculture 148, 313–322. Kolkovski, S., Koven, W.M., Tandler, A., 1997c. The mode of action of Artemia in enhancing utilization of microdiet by gilthead seabream Sparus aurata larvae. Aquaculture 155, 193–205.
120
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
Koven, W.M., Kolkovski, S., Tandler, A., Kissil, G.Wm., Sklan, D., 1993. The effect of dietary lecithin and lipase as a function of age, on n-9 fatty acid incorporation in the tissue lipids of Sparus aurata larvae. Fish Physiol. Biochem. 10, 357–364. Koven, W.M., Parra, G., Kolkovski, S., Tandler, A., 1998. The effect of dietary phosphatidylcholine and its constituent fatty acids on microdiet ingestion and fatty acid absorption rate in gilthead seabream, Sparus aurata, larvae. Aquacult. Nutr. 4, 39–45. Lauff, M., Hofer, R., 1984. Proteolytic enzymes in fish developed and the importance of dietary enzymes. Aquaculture 37, 335–346. Le Ruyet, J.P., Alexandre, J.C., Thebaud, L., Mugnier, C., 1993. Marine fish larvae feeding: formulated diets ´ or live prey? J. World Aquacult. Soc. 24, 211–224. Mackie, A.M., Mitchell, A.I., 1985. Identification of gustatory feeding stimulants for fish applications in aquaculture. In: Cowey, C.B., Mackie, A.M., Bell, J.G. ŽEds.., Nutrition and Feeding in Fish. Academic Press, London, UK, pp. 177–189. Marte, C.L., Duray, M.N., 1991. Microbound larval feed as supplement to live food for milkfish Ž Chanos chanos Forsskal. larvae. In: Lavens, P., Sorgeloos, P., Jaspers, E., Ollevier, F. ŽEds.., Larvi ’91 Fish and Crustacean Larviculture Symposium, 3–7 September 1995, Gent, Belgium. Eur. Aquacult. Soc., Spec. Publ., vol. 15, pp. 175–177, Gent, Belgium. McDonald, T.J., Jornvale, H., Nilsson, G., Vagne, M., Ghatei, M., Bloom, S.R., Mutt, V., 1979. Characterization of gastrin releasing peptide from porcine non-antral gastric tissue. Biochem. Biophys. Res. Commun. 90, 227. Meyers, S.P., 1985. Importance of lipid, lecithin in aquatic diets examined. Feedstuffs 23, 20–21, ŽSeptember.. Moons, L., Batten, T.F., Vandesande, F., 1992. Comparative distribution of substance P ŽSP. and cholecystokinin ŽCCK. binding sites and immunoreactivity in the brain of the sea bass Ž Dicentrarchus labrax .. Gen. Comp. Endocrinol. 73, 270–283. Moyano, F.J., Dıaz, ´ M., Alarcon, ´ Sarasquete, M.C., 1996. Characterization of digestive enzyme activity during larval development of gilthead seabream Ž Sparus aurata.. Fish Physiol. Biochem. 15, 121–130. Munk, P., Kiorboe, T., 1985. Feeding behavior and swimming activity of larval herring Clupea harengus in relation to density of copepod nauplii. Mar. Ecol.: Prog. Ser. 24, 15–21. Poston, H.A., 1990a. Performance of rainbow trout fry fed supplemental soy lecithin and choline. Prog. Fish-Cult. 52, 218–225. Poston, H.A., 1990b. Effect of body size on growth, survival and chemical composition of Atlantic salmon fed soy lecithin and choline. Prog. Fish-Cult. 52, 226–230. Rosenlund, G., Stoss, J., Talbot, C., 1997. Co-feeding marine fish larvae with inert and live diets. Aquaculture 155, 183–191. Salhi, M., Hernandez-Cruz, C.M., Bessonart, M., Izquierdo, M.S., Fernandez-Palacios, H., 1999. Effect of ´ ´ different dietary polar lipid levels on gut and liver histological structure of gilthead seabream Ž Sparus aurata. larvae. Aquaculture 179, 253–263. Sarasquete, M.C., Polo, A., Yufera, M., 1995. Histology and histochemistry of the development of the ´ digestive system of larval gilthead seabream, Sparus aurata L. Aquaculture 130, 79–92. Sorgeloos, P., 1980. The use of the brine shrimp in aquaculture. In: Persoone, G., Sorgeloos, P., Roels, O., Jaspers, E. ŽEds.., The Brine Shrimp Artemia. Ecology, Culturing and Use in Aquaculture, vol. 3. Universal Press, Wetteren, Belgium, pp. 25–46. Tandler, A., Kolkovski, S., 1991. Rates of ingestion and digestibility as limiting factors in the successful use of microdiets in Sparus aurata larval rearing. In: Lavens, P., Sorgeloos, P., Jaspers, E., Ollevier, F. ŽEds.., Larvi ’91 Fish and Crustacean Larviculture Symposium, 3–7 September 1995, Gent, Belgium. Eur. Aquacult. Soc., Spec. Publ., vol. 15, pp. 169–171, Gent, Belgium. Teshima, S., Kanazawa, A., Horinouchi, K., Yamasaki, S., Hirata, H., 1987. Phospholipids of the rotifer, prawn and larval fish. Nippon Suisan Gakkaishi 53, 609–615. Thorndyke, M., Holmgren, S., 1990. Bombesin potentiates the effect of acetylcholine on isolated strips of fish stomach. Regul. Pept. 30, 125–135. Tonheim, S.K., Koven, W., Rønnestad, I., 2000. Enrichment of Artemia with free methionine. Aquaculture Žin press.. Vander, A., Sherman, J., Luciano, D., 1998. Human Physiology: the Mechanisms of Body Function. 7th edn. WCB McGraw-Hill, Boston, MA, USA, 818 pp.
W. KoÕen et al.r Aquaculture 194 (2001) 107–121
121
Walford, J., Lim, T.M., Lam, T.J., 1991. Replacing live food with microencapsulated diets in the rearing of seabass Ž Lates calcarifer . larvae: do the larvae ingest and digest protein-membrane microcapsules? Aquaculture 92, 225–235. Watanabe, T., Kitajima, C., Fujita, S., 1983. Nutritional values of live organisms used in Japan for mass propagation of fish: a review. Aquaculture 34, 115–143. Wyatt, T., 1972. Some effects of food on the growth and behaviour of plaice larvae. Mar. Biol. 14, 210–216. Yufera, M., Pascual, E., Fernandez-Dıaz, ´ ´ ´ C., 1999. A highly efficient microencapsulated food for rearing early larvae of marine fish. Aquaculture 177, 249–256. Zambonino, J.L., Cahu, C., 1994. Development and response to a diet change of some digestive enzymes in sea bas Ž Dicentrarchus labrax . larvae. Fish Physiol. Biochem. 12, 399–408.