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 aIsrael 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
c
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
Ž .
The performance of microdiets MDs 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
Ž .
amino acids FAA alanine, glycine and arginine and the compound betaine were identified from the Artemia rearing medium as metabolites, which stimulated this larval response. Similarly, MD
Ž . Ž .
supplemented with phospholipids PL , particularly phosphatidylcholine PC , 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.
Ž .
E-mail address: [email protected] W. Koven .
0044-8486r01r$ - see front matterq2001 Elsevier Science B.V. All rights reserved.
Ž .
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
Ž .
MD supplemented with porcine pancreatic extract 0.05% DW diet showed a 30% increase in
Ž .
assimilation and demonstrated significantly P-0.05 improved growth. Older seabream larvae
14 Ž .
showed 6.75 times more radioactivity in tissue lipids when fed C-triacylglycerol TAG -labeled MD supplemented with porcine lipase, while younger larvae demonstrated no improved assimila-tion.
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
Ž .
levels of the digestive hormone cholecystokinin CCK 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.q2001 Elsevier
Science B.V. All rights reserved.
Keywords: Co-feeding; Microdiets; Attractants; Ingestion rate; Digestion; Assimilation; Gilthead seabream
larvae; Endocrine response
1. Introduction
Ž .
Rotifers 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
Ž .
supply and nutritional quality Sorgeloos, 1980; Watanabe et al., 1983 . Consequently, a great deal of interest has been generated to develop an off-the-shelf artificial larval
Ž .
microdiet MD as an economic live food alternative. Moreover, MD offer the opportu-nity 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
Ž . Ž
metamorphosis 0.5–0.75 g in many species Dabrowski, 1984; Foscarini, 1988; Hardy, .
1989 , the early introduction of prepared diets as the sole replacement for live food has Ž
met with limited success Adron 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
Ž .
assimilation. Tandler and Kolkovski 1991 found that Sparus aurata larvae consumed
Ž .
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
Ž
nauplii Corneillie 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
Ž .
when both are offered simultaneously Fernandez-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 etŽ .
al. 1997a , where gilthead seabream larvae demonstrated an ingestion rate of a
14
C-labeled MD that was positively correlated with the concentration of 3H-labeled
y1 Ž .
nauplii in the rearing medium up to 9 nauplii ml Fig. 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 1mg 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
Ž .
phenomenon, Kolkovski et al. 1997c tested the effect of supplementing various extracted Artemia fractions in the MD. These authors found that the addition of
14 Ž . 3 Ž .
Fig. 1. Ingestion rates of a C MD I and H Artemia nauplii q given as a combined ration to
Ž .
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
Ž .
MD assimilation significantly 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 Ž .
the ingestion, digestion and assimilation of MD during co-feeding: 1 the influence of Ž . MD on ingestion by stimulating feeding activity through visual and chemical stimuli; 2 the influence of the biochemical composition of the nauplii on larval digestion and
Ž .
assimilation; 3 the influence of dietary factors that influence both feeding activity as
Ž .
well as digestion and assimilation. Kolkovski et al. 1997a 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
Ž .
in larvae that were offered the MD alone Fig. 2 . Moreover, both visual and chemical
Ž .
stimuli were found to work synergistically Fig. 2 . On the other hand, the magnitude of
Ž .
Fig. 2. Percent increase of MD ingestion in 20-day-old larvae compared to the control treatment as a function of visual and chemical Artemia stimuli originating from different Artemia concentrations. The control
Ž .
the influence of these stimuli decreased in older larvae. Since visual acuity as well as
Ž .
neural and olfactory development proceeds with larval age Blaxter, 1968 , it is reasonable to assume that the dependence on rudimentary visual and chemical
stimula-Ž .
tion of the larva by the prey will decrease Fernald, 1993 as the larva develops its hunting prowess.
4. The influence of factors in live food on larval MD feeding activity
Ž .
The free amino acids FAA alanine, glycine and arginine and the ammonium base compound betaine were identified as chemical stimuli of gilthead seabream larvae from
Ž .
the 14 metabolites found in the Artemia-rearing medium Kolkovski et al., 1997a . This was concluded by monitoring the effect of the removal of each of the 14 metabolites on
Ž .
MD ingestion rate in 20-day larvae Fig. 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 ..
w14 x The FAA alanine and glycine as well as betaine were incorporated into a C labelled MD based on the gelatin-Arabic gum encapsulation of liposomes in a recent
Ž .
study at the National Center of Mariculture NCM . The MD was tested in 7-day-old gilthead seabream larvae and the ingestion rate measured in the presence or absence of
Ž .
rotifers Brachionus rotundiformis . In the absence of rotifers, larvae tended to ingest
Ž .
more 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
Ž .
20-day-old larvae compared to the control treatment . The control was MD ingestion rate in the absence of the
Ž . Ž
metabolites. Bars having the same superscript are not significantly P-0.05 different from each other from
.
Ž .
albumin BSA 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
Ž .
column Fig. 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
Ž .
based on the liposome encapsulation of the FAA was significantly 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.
Ž .
These findings are consistent with work carried out on salmonids Hughes, 1990 ,
Ž .
weatherfish, abalone and yellowtail Harada et al., 1987; Harada, 1992 where FAA and
Ž .
betaine were also found to be effective attractants. Knutsen 1992 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
Ž
nauplii concentration in Pleuronectes platessa larvae Wyatt, 1972; Munk and Kiorboe, .
1985 and in response to extracts of Balanus nauplii and the amino acids glycine and
Ž .
L-proline in the larvae of herring 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
Ž .
liposomes containing BSA only, or BSA and selected FAA BSAqFAA , or BSA only together with the FAA
Ž .
dissolved separately in the water BSAqFAA . Ingestion rate values having different letters were significantly
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
phos-Ž .
phatidylcholine PC , stimulate early larval feeding activity but did not elicit the same
Ž .
response in older larvae Koven 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
Ž .
PC-supplemented MD demonstrated up to 35% higher P-0.05 ingestion rates compared to the non-PL control in 21–26-day-old gilthead larvae, although this effect
Ž .
had diminished in 28–31-day-old larvae Hadas, 1998; Koven et al., 1998 . These findings were consistent irrespective of the presence or absence of a double bond in the
Ž .
PL fatty acid moiety Koven et al., 1998 . Furthermore, larvae fed on PC-supplemented
Ž .
MD markedly P-0.05 outperformed larvae ingesting an MD supplemented with
Ž . Ž .
phosphatidylethanolamine PE , the other main membrane PL Fig. 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
Ž . Ž .
feed attractant betaine Mackie and Mitchell, 1985 . In fact, Harada et al. 1987
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
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 Ž
larvae is well documented Kanazawa et al., 1981, 1983a,b, 1985; Teshima et al., 1987;
. Ž
Geurden et al., 1997 . As this benefit may affect the early juvenile stages Poston, .
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
Ž .
occurring in parallel andror in tandem. Kolkovski 1995 found that PC and lyso-PC supplementation effectively improved the assimilation of MD in 20-day-old seabream
Ž .
larvae. In support of this, Koven et al. 1993 showed a significant effect of dietary
Ž .
lecithin on the incorporation of labeled free fatty acid FFA in body neutral and PL in
Ž .
21–45-day-old larvae Fig. 6 . This was particularly pronounced during early larval
Ž .
development 21-day-old larvae where fish fed on PL-supplemented MD assimilated 6.75 times more14C-label than the control non-PL MD.
w14 x
Fig. 6. Comparison between the effects of dietary lecithin and lipase on larval C oleic acid incorporation
Ž .
with age. Effect was measured as the times = 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
Ž .
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
Ž .
a limited ability for PL synthesis Kanazawa 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
Ž .
emulsifiers Meyers, 1985; Kanazawa, 1993; Koven et al., 1993 . However, the accumu-Ž
lating evidence from studies on various fish species and crustaceans Coutteau 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
Ž .
from the enterocytes lining the digestive tract to the body tissues Hadas, 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
w14 x
ingestion rates, larvae fed on C -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
Ž .
non-PL control Hadas, 1998 . Moreover, 57% of the radioactivity in the digestive tract
Ž .
of the control larvae was in the triacylglycerol TAG and FFA fraction compared to
Ž .
12.5% in larvae feeding on the PC diet Hadas, 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
Ž .
et al. 1999 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 au-thors concluded as well that dietary PC is necessary for the synthesis of verylow-den-Ž .
sity lipoproteins VLDL 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 assimila-tion is by contributing their own enzymes to facilitate the digesassimila-tion process until the
Ž
larva’s own alimentary systems is fully differentiated and developed Dabrowski and
. Ž .
Glogowski, 1977a,b; Lauff and Hofer, 1984 . In support of this, Kolkovski et al. 1993 found in gilthead seabream larvae ingesting MD supplemented with a porcine pancreatic
Ž . Ž .
extract 0.05% , a 30% increase in assimilation and significantly P-0.05 improved
Ž .
w14 x
on the assimilation of dietary C 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
w14 x
masked by the inability to absorb the sudden excess of C 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.
Ž .
various ages of seabream larvae. Zambonino and Cahu 1994 claimed as well that enzyme contribution from live food to the larval digestive process was minimal. In
Ž .
support of this, Cahu et al. 1995 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
deter-Ž
mined and independent of food intake Sarasquete 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
Ž .
larvae feeding on live food Zambonino 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
neurohor-Ž .
monal factors Chan and Hale, 1992 , may stimulate secretions of trypsinogen and other Ž
enzymes from the pancreas andror activate gut zymogens Le 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
Ž .
cholecystokinin CCK , which are pituitary neuropeptides, are an integral part of this gastro-entero-pancreatic endocrine system and have also been reported, or their binding
Ž
sites, in adult fish Batten 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
Ž .
circulation to the gut wall McDonald et al., 1979 . CCK triggers secretion of pancreatic
Ž .
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.
Ž .
Kolkovski et al. 1997a,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
Ž .
liposome treatments into the gut Koven 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
Ž .
feeding on Artemia Tonheim et al., 2000 . The CCK response was highest in larvae ingesting liposomes containing the FAA methionine compared to larvae injected with
Ž
the other liposome treatments I. Rønnestad, C. Rojas and R.N. Finn, personal communi-.
cation, 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
Ž .
digestive tract Walford et al., 1991 . However, a recent study reported that the capacity of gilthead seabream to digest encapsulated diets depended on the thickness and rigidity
Ž .
of the capsule coating Fernandez-Dıaz and Yufera, 1995 . These authors found, during
´
´
´
larval feeding, that thin-walled and soft gelatin microcapsules were more easily de-graded than those encapsulated with a harder, thicker and more resistant material. ThisŽ
may suggest that despite the presence of the requisite digestive enzymes Moyano 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,
Ž .
suggesting a promising tool for further nutritional research Yufera et al., 1999 .
´
10. Conclusion
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.
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