Nutrient requirements of marine food fish cultured in Southeast Asia

ELSEVIER

Aquaculture

151 (1997) 283-313

Nutrient requirements of marine food fish cultured in Southeast Asia Mali Boonyaratpalin Department of Fisheries, Jarujak,

’

Bangkok 10900, Thailand

Abstract The culture of marine and brackish-water fish has gained increased importance in the aquaculture industry, particularly in Southeast Asia. As feed accounts for the major portion of rearing costs, nutritional adequacy and cost-effectiveness is critical to the industry. This review will focus on the nutritional requirements of tropical marine food fish that include seabass (Lutes calcurifer), grouper (Epinephelus sp.), milkfish (Chums chums) and rabbitfish (Siganus sp.). Culture practices of marine fish in Southeast Asia with special reference to Thailand will also be described. 0 1997 Elsevier Science B.V. Keywords: Fish nutrition; sp.

Nutrient requirements;

Lazes calcarifer;

Epinephelus sp.; Chums chanos; Siganus

1. Introduction This review paper covers the work done on the general nutrition, nutritional requirements, food and feeding of economically important tropical marine finfish cultured in Southeast Asia. The finfish reviewed include the Asian seabass (Lutes calcarifer), grouper ( EpinepheZus spp.), milkfish (Chums chanos) and rabbitfish (Siganus spp.). This review paper discusses each species individually and provides a total summary of the work carried out to date on the different aspects of nutrition on the above mentioned economically important marine finfish. Much emphasis has been placed on the nutritional requirements of seabass as it is the most popular cultured fish having a high table value. Although the grouper is an equally important table fish, more research on its nutrition needs to be conducted, likewise, information on the nutrition of rabbitfish is scant. Extensive research has been done on the milkfish which is a very

’ Director Feed Quality Control and Development

Division.

OO448486/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved PII SOO44-8486(96)01497-4

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M. Boonyararpalin/Aquaculture

important table fish in the Philippines, owing to its bony nature.

2. Asian seabass

151 (1997) 283-313

although not preferred in countries

like Thailand

L&es calcarifer

2.1. Introduction Asian seabass, also called giant sea perch or barramundi in Australia, is an economically important food fish and sport fish in the tropical and subtropical areas of the western Pacific and Indian Ocean. Seabass are a fast growing fish, attaining marketable size within 8 months, generally with a growth rate of 1 kg per year, with acceptable white flesh and commanding a high market price. Seabass also have many characteristics that are favorable for coastal aquaculture, that is, they grow well in water of high turbidity and varying salinities, and can tolerate rough handling and crowded conditions of net-cage culture. Furthermore, they can be easily tamed for aquaculture and accept feeding by humans. Seabass have been cultured in Hong Kong, Indonesia, Malaysia, Philippines, Singapore, Taiwan, and Thailand for many years. Data published by SEAFDEC (1992) show that seabass production was 167, 2267, 1953, 779, 1438 and 1215 t in Hong Kong, Indonesia, Malaysia, Philippines, Taiwan and Thailand, respectively, in 1990. Three methods of spawning are used in Thailand for the mass production of seabass fry. Artificial fertilization involves catching spawners in estuaries and stripping the females and males for eggs and milt. The fertilized eggs are then transported to the hatchery for subsequent incubation. Induced spawning by hormone injection is practiced where natural spawning in tanks does not take place or when an early spawning is needed. Natural spawning in tanks is the easiest and best method for commercial-scale seabass seed production. This is because it produces the largest quantity of eggs, of the highest quality and for a prolonged period (Maneewongsa et al., 1981; Masuo, 1986). Larval rearing is one of the most important steps after seed production. Salinity should be considered at this stage to avoid high mortality and maintain high production. Salinity should be between 25 and 30 ppt for larvae, fry and food organism culture. During the first 15 days, salinity is maintained at about 20-28 ppt. Fry can tolerate freshwater when they attain a size of 4.5 mm total length, but growth is reduced. Fish grow well both in seawater and freshwater when they reach a size of 13.9 to 17.7mm. Temperature during larval rearing has a great effect on health and survival of seabass. Increasing water temperature has been shown to prevent or reduce the incidence of feeble, slender larvae that refuse food and float on the water surface and mass mortality of 15-22-day-old larvae. Survival increases from 11.39 to 66.45% when temperature is increased from 27-29°C to 34-35°C (Ruangpanit and Kongkumnerd, 1992). The food and feeding method are the most important factors affecting growth, health, size variation, and survival of seabass larvae and fry. Rotifers are the most suitable food for larvae at the early stages of rearing. Microcrustacean ( Artemia and Moina) are usually fed once fry reach 4mm in size.

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Seabass are cannibalistic, therefore grading of fry is of prime importance. The first grading is done when the larvae are 12-15 days old, at this time the size variation is already great and the smaller ones can tolerate handling stress (Pechmanee and Watanabe, 1984). After the first grading, subsequent grading is done every 3-5 days. The first grading is done using a double net made of plastic mosquito net with a 2mm mesh size. The smaller fish pass through the net and are left in the tank and the larger ones are retained and transferred to a separate tank. The second grading is done using a bucket with pores through which fry of a certain size can pass. Till the fish are 30 days old, five buckets with gradually increasing pore sizes are used in succession, 3.2, 4.8, 6.4, 9.5 and 12.7mm. The grow-out phase involves the rearing from fingerling (10cm) to marketable size. The marketable size in central Thailand is 500-800 g. This size commands a better price than smaller or larger sized fish. However, the marketable size in southern Thailand is 600-800 to 1200-2000g. The culture period varies from 5 to 8 months (for 500-8OOg fish) to as much as 12-20 months for larger fish. Seabass are cultured in ponds and net cages. Production yields range from 0.87 to 0.91 kgme3 per crop in ponds to as high as 35-40 kgmm3 per crop in net cages.

2.2. Nutrient requirements

2.2.1. Protein requirements The dietary protein requirement of seabass was initially estimated to be 45-55% (Cuzon, 1988). This study involved feeding four practical diets containing 35-55% crude protein mainly from Norwegian fish meal and a control diet containing 52% crude protein consisting of fish meal and fish protein concentrate. The protein-to-energy ratio was held constant at about 140 mg protein per kcal or 7.1 kcal g- ’ of protein. The highest growth rate was obtained with the control diet. Sakaras et al. (1988) evaluated six practical diets with three dietary protein levels of 45, 50, and 55% and two lipid levels of 10 and 15% at each protein level in 7.47g seabass. Fish were fed to satiation twice daily for 8 weeks. The best growth rate, feed conversion, protein retention, and protein efficiency ratios were observed in fish fed the diet containing 50% crude protein, 15% lipid and 7.33 kcalg-’ of protein. In a subsequent study, fish fed a diet containing 45% crude protein and 18% lipid had the highest growth rate (Sakaras et al., 1989). The optimum dietary protein level is usually higher for larval and fry stages and lower for the grow-out stage. The optimal dietary protein level for grow-out seabass has been reported to be 40-45% crude protein in diets containing 12% lipid (Wong and Chou, 1989). Animal proteins such as fish meal and squid meal are the best protein sources and the most readily accepted by seabass. The replacement of 5% fish-meal with an equal amount of squid-meal in a seabass fingerling diet improved growth and feed efficiency by 11.44 and 13.3%, respectively (Chungyampin and Boonyaratpalin, 1988). No information is available on the essential amino acid requirements of seabass, however, it has been shown that excessive dietary tyrosine results in kidney disease (Boonyaratpalin et al., 1990).

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2.2.2. Lipid requirement The optimum dietary lipid level for seabass fingerlings was found to be 15 and 18% at protein levels of 50 and 45%, respectively (Sakaras et al., 1988, 1989). Tucker et al. (1988) found that when 9-628 seabass were fed similar diets containing 9.3 and 12.9% fat, growth was similar but feed conversion was significantly lower with the 12.9% fat diet. Seabass were fed a series of six dry diets containing lo-16.9% fat, and 20-60% fish meal, the diet containing the most fish meal (60%) and fat (16.9%) produced the best feed conversion (0.89), however, a diet containing 20% fish meal and 13.4% fat gave practically the same results. Borlongan and Parazo (1991) found that growth and survival rates of seabass fry fed a diet containing 4.5% cod liver oil and 4.5% soybean oil were highest, followed by those fed cod liver oil alone and soybean oil alone. Fry growth and survival rates were low in fish fed a coconut oil diet and lowest in fish fed a diet containing no lipid supplement. The fatty acid profiles of the fry were influenced by the fatty acid composition of the dietary lipid. Signs of essential fatty acid (EFA) deficiency were observed in seabass fingerlings after being fed a diet containing 0.46% n-3 highly unsaturated fatty acids (HUFA) for 2 weeks. The initial deficiency sign was a reddening of the fins and skin, which was followed by other deficiency signs, such as abnormal eyes, a shock syndrome, loss of appetite, poor growth and swollen, pale livers. Fish fed a diet containing 0.88% n-3 HUFA also showed slight EFA deficiency, such as reddening of fins and skin. Fish fed a diet containing 1.72% n-3 HUFA, approximately 13% of the dietary lipid, had the best growth rate and showed no signs of EFA deficiency (Buranapanidgit et al., 1988). In a subsequent study, six fish meal and casein diets containing levels of n-3 HUFA ranging from 1 to 2% of the diet were fed for 10 weeks. Dietary n-3 HUFA levels were adjusted using squid liver oil. No difference in growth, feed efficiency, or mortality was detected and no signs of EFA deficiency were observed (Buranapanidgit et al., 1989). The results of the two studies indicate that the dietary n-3 HUFA requirement for seabass fingerlings is 1.O to 1.7% of the diet. 2.2.3. Carbohydrate requirement The natural foods of seabass are high in protein, so it is assumed that they do not utilize carbohydrates well. It was observed that when small amounts of starch, up to 10% was added to diets lacking in carbohydrate, growth improved, however when higher levels (27%) were included, growth was depressed. Therefore, until further research is conducted, it would be reasonable to suggest that total available carbohydrate content of feeds for seabass fingerlings not exceed 20% (Boonyaratpalin, 1988). 2.2.4. Vitamins requirement Not all vitamins appear to be essential in practical seabass feeds, even though they are required for normal metabolic functions. Some vitamins may be synthesized by seabass in sufficient quantities to meet requirements or may be present in adequate amounts in the practical feed ingredients. Vitamin requirements depend upon size of fish, stage of sexual maturity, growth rate, environmental conditions and dietary nutrient interrelations. The vitamin requirements of seabass seem to decrease as fish size increases (Boonyaratpalin et al., 1989b). The addition of a vitamin mix to trash fish fed to seabass fingerlings increased

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growth rate from 9.36 to 23.48 g and reduced the feed conversion ratio from 7.44 to 3.83 during a 9 week rearing period (Phromkhuntong et al., 1987). The vitamin requirements for seabass have been established for young fish by supplementing both practical and semipurified diets with various levels of a specific vitamin. The requirements have been based on the minimum dietary vitamin level that will support maximum growth or maximum tissue storage and prevent deficiency signs. No differences in weight gain, feed efficiency and total mortality were observed when seabass were fed practical diets without the addition of choline, niacin, inositol or vitamin E (Boonyaratpalin et al., 1988). Similarly, no differences in growth rate, feed efficiency, or survival were observed in seabass fingerlings fed practical diets without supplemental pyridoxine and pantothenic acid (Pimoljinda and Boonyaratpalin, 1989). Lower weight gain and feed efficiency were observed in fish fed diets without supplemental thiamin and riboflavin after 60 days. Fish fed diets without added vitamin C had normal growth rates for about 15 days after which growth ceased and deficiency signs, such as poor appetite, loss of equilibrium, gill hemorrhage, and scoliosis, developed. Severe mortality occurred after 45 days and all vitamin C-deficient fish died within 60 days. Two studies have been conducted to determine the quantitative vitamin C requirement of seabass fingerlings (Boonyaratpalin et al., 1989a,b). The first study involved feeding practical diets supplemented with 0, 500, 1000, 1500, 2000 and 2500mg crystalline vitamin C per kg of diet to seabass in freshwater for 10 weeks. The best growth rates were observed in fish fed diets containing 1OOOmg vitamin C per kg or higher. In the second study, fish were fed practical diets containing 0, 500, 700, 900, I 100, 2500, and 5000 mg vitamin C per kg diet in seawater for 8 weeks. Fish fed diets with vitamin C levels of 500 or more mg kg-’ of diet had satisfactory growth rates, with only slight vitamin C deficiency signs being observed in fish fed the 500mg crystalline vitamin C per kg diet. The vitamin C content of liver and kidney increased with the increase in dietary vitamin C levels. In conclusion, the minimum level of supplemental crystalline vitamin C required for normal growth of seabass fingerlings in seawater was 500mg kg- ’ diet, and a supplemental level of 1100mg kg-’ diet was required for normal tissue storage. The dietary vitamin C supplementation levels for seabass are relatively high compared to channel catfish and salmon (Helland et al., 1991; Wilson, 1991). This is likely due to the instability of the crystalline vitamin C used in this experiment. Two derivatives of ascorbic acid, which are more stable than the parent compound (crystalline L-ascorbic acid), have been tested and shown to have antiscorbutic activity in seabass. These include L-ascorbyl-2- monophosphate (Boonyaratpalin et al., 1992) and L-ascorbic acid-glucose (M. Boonyaratpalin, unpublished data, 1993). Ascorbyl-2 monophosphate-Mg and ascorbic acid-glucose are stable to the heating process typical of feed manufacturing and are bioavailable for seabass. A dietary level of 30mg ascorbyl-2 monophosphate per kg diet or 25 mg ascorbic acid-glucose per kg of diet (equivalent to 12.6 or 13.0mg ascorbic acid per kg diet, respectively) has been shown to be required for normal growth and prevention of deficiency signs. Seabass fed vitamin-C-deficient diets develop the following gross deficiency signs: poor appetite; poor growth; dark coloration; fin erosion; bleeding gills; loss of equilibrium; pop eye; shortened operculum; detached isthmus; scoliosis; lordosis; broken back

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and body curvature. Haemoglobin, red blood cells, white blood cells, serum protein and tissue hydroxyproline were reduced in vitamin C deficient fish. Pathological changes included distortion of gill filaments, hyperplasia and club-shaped formation of secondary lamella. Livers of affected seabass showed severe fatty tissue degeneration. Muscle degeneration and hemorrhage of the skin were usually associated with vitamin C deficient-fish. The role that ascorbic acid plays in disease resistance and/or immune system of seabass remains unclear. An example of a semipurified diet that has been used in vitamin studies for seabass fingerlings is presented in Table 1. When this diet was used to determine the pyridoxine requirement, the results indicated that 5 mg of pyridoxine per kg of diet was required for normal growth and 1Omg of pyridoxine per kg of diet was needed for normal lymphocyte levels (Wanakowat et al., 1989). Boonyaratpalin and Wanakowat (1993) fed seabass with semi-purified diets which were deficient in several vitamins for 10 weeks. Thiamin deficiency induced substantial post-handling shock and high mortality. Fish fed diets lacking riboflavin exhibited deficiency signs including anorexia, erratic swimming and cataracts. Pantothenic acid deficiency signs included ventral fin hemorrhage and erosion, hemorrhage around the operculum and isthmus, clubbed gill and high mortality. Inositol deficiency led to poor growth, abnormal mouth and head bone formation in a few individuals. Vitamin E deficiency resulted in dark coloration and muscular atrophy and increased susceptibility to bacterial skin disease infection. In a quantitative pantothenic requirement study, fish were fed semi-purified diets containing 0, 15, 30, 60

Table 1 Example of a semi-purified

diet for seabass (Wanakowat

et al., 19891

Ingredient

Percentage

Casein (vitamin free) Gelatin Cod liver oil Soybean oil Gelatinized starch Carboxymethyl cellulose Cellulose Vitamin mixture a McCollum’s salt mixture b Amino acid mixture ’ Water (ml)

50 10 6 3 5 8 5 2 4 I 80

a To contain as mg lOOg-’ dry diet: thiamin-HCl, 5; riboflavin, 20; choline chloride, 500; nicotinic acid, 75; calcium-d-pantothenate, 50; pyridoxine.HCl, 5; inositol, 200; biotin, 0.5; folic acid, 1.5; vitamin B,,, 0.1; menadione, 4.0; alpha-tocopheryl acetate, 40; vitamin A, 1000 IU; vitamin D,, 200 IU; BHT, 1.0; ascorbic acid, 100. b McColIum’s salt mixture No. 185 plus trace elements fg lOOg_’ mineral mixture): calcium lactate, 32.708; K,PO,, 23.98g; CaHPO,.2H,O, 13.588; MgS04.7H,0, 13.2Og; Na,HP0,.2H_,O, 8.72g; NaCl, 4.35g; ferric citrate, 2.97g; ZnS0,.7H20, 0.3g; CoCl,-6H,O, 1OOmg; MnSO,.HzO, 80mg; Kl, 15mg; AlCls6H,O, 15mg; CuCl,, 1Omg. 0.6; L-arginine.HCl, 1.3; L-cystine, 0.7; ’ Amino acid mixture, (g lOOg_’ d ry diet): L-phenylalanine, L-tryptophan, 0.2; L-histidine.HCl.H,O, 0.2; DL-alanine,l.3; L-aspattic acid.Na, 1.O; L-valine, 0.7; L-lysine HCl, 0.6; glycine, 0.4.

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and 90mg of calcium d-pantothenate per kg for 12 weeks. Results showed that fish fed no supplementary calcium d-pantothenate ceased growing after 2 weeks and total mortality occurred within 6 weeks. This semipurified diet has also been used to determine the importance of certain vitamins and to document their deficiency signs in seabass as summarized in Table 2 (Boonyaratpalin et al., 1993a). The dietary requirement of seabass fingerlings (2.7 to 3O.Og) for pantothenic acid is 15 mg kg-’ diet for normal growth, feed efficiency and survival but the requirement for maximum tissue storage is 90 mg kg-’ diet. Fish fed the pantothenate-deficient diet exhibit poor appetite, poor growth, poor feed efficiency, total mortality in 6 weeks, hemorrhages and clubbed gills (Boonyaratpalin et al., 1993b). 2.2.5. Mineral requirements As seabass do not readily accept purified diets, mineral requirements have not been adequately evaluated. Experiments on the optimum level of supplemental mineral mix UPS XII and the effect of micro minerals and calcium lactate on the growth of seabass fingerlings were done by feeding five fish-meal and casein-based diets containing either 0, 2, or 4% UPS XII mineral mix, 4% macro minerals, or 4% calcium lactate-free micro minerals (Porn-ngam et al., 1989). The results indicated that the diet containing 2% UPS

Table 2 Vitamin requirements and deficiency signs (Boonyaratpalin 1989a,b, 1990, 1992, 1993a,b; Wanakowat et al., 1989)

and Wanakowat,

1993; Boonyaratpalin

Vitamin

Requirement (mg kg- ’ diet)

Deficiency

Thiamin Riboflavin Pyridoxine Pantotheni c acid

Ra R 5-10 b 15-90 b

Poor growth, substantial post-handling shock, high mortality Erratic swimming, cataracts Avoidance of schooling, erratic spiral mortality, convulsions Ventral tin hemorrhage and erosion, hemorrhage acid around operculum and isthmus, mortality in 5-6 weeks

Nicotinic acid Biotin Inositol Choline Folic acid Ascorbic acid

NA NA R NA NA 700 ’ 25-30

Vitamin Vitamin Vitamin Vitamin

NA NA R NA

A D E K

signs

Poor growth, abnormal

d

bone formation

Bleeding gill and distortion of gill filament and hyperplasia, short operculum, short snout, exophthalmia, short body, loss of equilibrium, scoliosis, lordosis, broken back, pop-eye, fatty liver, muscle degeneration and hemorrhage, low blood parameters and low tissue hydroxyproline

Muscular atrophy, susceptible

a Required but quantitative requirement not established. b For maximum tissue storage. ’ For crystalline vitamin C. d For ascorbyl-2-monophosphate-Mg or ascorbic acid glucose. NA: no information available.

to disease

et al.,

290 Table 3 Summary

M. Boonyaratpalin /Aquaculture

of nutrient requirement

151 (1997) 283-313

of seabass

Nutrient

Requirement

References

Protein (% diet) DE/P (kcalg-’ ) Lipid (% diet) n-3 HUFA (% diet) Pyridoxine (mg kg- ’ diet) Pantothenic acid (mg kg- ’ diet) Ascorbic acid (mg kg- ’ ) Phosphorus (% diet)

40-50 6.8-7.33 13-16 l-l.7 5 “-10 b 15 “-90 b 700 c-13 d 0.65

Cuzon, 1988 Tucker et al., 1988; Sakaras et al., 1988 Cuzon et al., 1990; Tucker et al., 1988 Buranapanidgit et al., 1989 Wanakowat et al., 1989 Boonyaratpalin et al., 1993b Boonyaratpalin et al., 1989b, 1992 Boonyaratpalin and Phongmaneerat, 1990

a For growth. b For maximum tissue storage. ’ When crystalline vitamin C is used. d When L-ascorbyl-2-monophosphate-Mg

or ascorbic

acid glucose is used.

XII mineral mix gave optimum growth and that seabass appear to obtain adequate macro minerals from their water supply or practical feedstuffs. Deletion of calcium lactate from the macro mineral mix reduced growth slightly (12%) but not statistically significant. An experiment on the effects of 0, 0.5, 1.O and 2.0% monosodium phosphate supplemented in fish-meal-based diets showed that the growth of seabass fed a diet with 0.5% monosodium phosphate supplementation was superior to the growth of fish fed diets containing the other phosphate levels. However, 1.0% monosodium phosphate supplementation gave the best feed efficiency and protein efficiency ratio. Considering the phosphorous available in the fish meal, the total available phosphorus requirement of seabass was estimated to be 0.55-0.65% (Boonyaratpalin and Phongmaneerat, 1990). The nutrient requirements of seabass are summarized in Table 3. Medicated feeds can be prepared using any type and any formulation with the appropriate chemical or drug incorporated into the formula prior to processing or pelleting. In Thailand, extruded feeds are commonly top-dressed with medications immediately after extrusion or soaked in medicated water just before feeding.

2.2.6. Feeds and feeding Seabass are mid-water column feeders and do not feed either at the surface or bottom, preferring soft, moist feed. Therefore, extruded floating feeds are usually soaked in freshwater until they become saturated, slow sinking pellets. However, successful use of dry pelleted feeds for the culture of seabass in cages has been reported by Sakaras (1990). Though moist pellets are inexpensive and easier for the farmer to process, a binder is required. The most commonly used binder is cooked starch. Although extruded feeds are easy to use, they are expensive when compared to other types of feeds owing to high manufacturing costs and because an excess of heat-sensitive vitamins must be added to the feed. The feed conversion ratio of extruded feed or moist feed is 1.2:l.O (dry weight basis). Traditional feed or trash fish supplemented with vitamins is recommended to farmers

M. Boonyaratpalin/Aquaculture Table 4 Growth, feed conversion and survival (Phromkhuntong et al., 1987)

of seabass

Feed

Weight

151 (1997) 283-313

fed trash fish with and without Feed conversion

291

vitamins

supplementation Survival

Initial

Final

Trash fish

1.48

9.36

7.44

95.00

Trashjish + vitamin mix + folic-free vitamin mix + niacin-free vitamin mix + vitamin C-free vitamin mix a

1.34 1.26 1.25 1.37

23.48 20.49 20.39 16.5

3.82 3.91 4.02 4.81

100.00 99.50 99.50 99.50

a Recommended

fat coated vitamin C for moist feed.

who can obtain fresh trash fish easily and at a low cost. The growth and feed conversion ratios of seabass fed trash fish feed is about 4: 1 (Table 4). A feed formulation (Table 5) has been recommended to farmers which has been well accepted and is based on the results of research carried out by the Department of Fisheries in Thailand. Tacon et al. (1991) found that seabass fed fresh and moist pellets (frozen fish: dry diet-40:60) displayed the best growth response whereas dry pellets alone gave unsatisfactory growth owing to lower feed intake. The reason was not clear but may have been due to the quality of ingredients or lack of some nutrients such as vitamins in the diet. However, feed formulations, vitamin and mineral mixes that are recommended for salmon should also give satisfactory results for seabass. Seabass are typically fed on a percentage of the standing crop weight. Feeding rates are affected by fish size and typically, smaller fish will feed more in relation to their size than larger fish. Table 6 provides suggested feeding rate guides for small seabass. Satiation feeding is recommended for seabass culture because of the cannibalistic and aggressive characteristics of the fish. Feeding the fish slowly to satiation will result in more even growth in the fish population, minimizing mortality owing to cannibalism and the need for frequent grading. Tucker et al. (1988) found that when 74- 150 g seabass

Table 5 Example of practical

diet for seabass (Boonyaratpalin,

1988)

Ingredient

Percentage

Fish meal Rice bran Vitamins Minerals Gelatinized starch Ascorbic acid Marine fish oil Vegetable oil Water

70 12.40 1 2 10 0.10 1.50 3 40-50

M. Boonyaratpalin/Aquaculture

292 Table 6 Suggested

feeding rates for small seabass (Boonyaratpalin,

Fish size (g)

Feeding frequency

1.8-5.4 5.5-11.5 11.6-19.2 19.3-27.9 28.0-45.0 > 74

2-3 2-3 2 2 2 1

(times per day)

151 (1997) 283-313

1988) Feeding rate (% body weight per day) 7.18 5.70 4.59 3.90 3.50

were fed one or two meals a day, daily growth rate was similar but daily ration and feed conversion were significantly lower with one meal per day.

3. Grouper

Epinephelus

sp.

3. I. Introduction Grouper is the most popular maricultured fish in Southeast Asia and in certain parts of the Middle East, namely, Kuwait. Live fish have a high market demand and fetch high prices in Hong Kong. The red grouper, Epinephelus akaara, is a highly preferred species as it symbolizes good fortune in Hong Kong and is served at wedding dinners, (Tseng and Ho, 1988). E. a k aara is a very slow growing grouper in comparison to E. tauuina, which is widely cultured in Asian countries. Groupers are sluggish fish and in their natural habitat are often found to be resting in rocky cervices, or at the bottom of cages when they are cultured. Therefore, in a culture environment, suspended material such as used automobile tires or pipes will help increase the resting surface area. This sluggish characteristic of grouper helps save energy for growth, thereby resulting in increased feed efficiency and reduced feeding frequency. Groupers are marine fish and can withstand salinity ranging from 15 to 45 ppt. They can also withstand exposure to freshwater for about 15min. The optimum culture temperature ranges from 22-28°C. When the temperature is below 15°C the fish do not feed. The grouper is euryphagous, showing greater preference for crustacea and live food than for fish and dead organisms (Randall, 1965). Longly and Hildebrand (1941) reported that Epinephelus morio feed indifferently during the day or night. E. akaara favours feeding just before sunset whereas cultured red groupers exhibit a special feeding behaviour. The fish can be trained to know when they will be fed. When they sense the sound of chopping of trash fish or knocking on a wooden plank, they gather at the cage edge. As the fish are of a suspicious nature, they watch for food but do not move. However, if attempts to approach the food are made by one, all the fish will immediately attack it violently sometimes injuring themselves in the process. Groupers usually eat one to three pieces of minced trash fish then disperse away

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immediately. No attempts are made to eat any food which falls to the net bottom, no matter how hungry they are. Owing to this special feeding behaviour, groupers are generally mix-cultured with sea bream which act as scavengers and stimulate the groupers to feed. E. tuuuina is a hermaphrodite (gynandrous); males are generally absent in the smaller length-classes. The sexually mature males are large, more than 740mm in standard length at the age of 9 or more years. However, the process of sex reversal has been accelerated where 3-year-old females were turned into males by oral application of methyltestosterone (Chen et al., 1977). Groupers are potentially important aquaculture species since they are fast growing, accept dry pellet feed, can be successfully spawned in captivity, have high feed efficiency and very high market value. However, there are certain draw backs in areas such as larval rearing and the lack of nutrient requirement data. Trash fish is the most common feed used in the cage culture of grouper, but increasing price, shortage of supply, variable quality and poor feed conversion ratios indicates that trash fish is not a nutritionally adequate and economical diet. Thus, it is important to develop a balanced feed formulation for this species, otherwise large scale production of grouper may be hampered. 3.2. Nutrient requirements The dietary protein requirements for carnivorous marine species like grouper are normally high. The level of dietary protein which produced maximum weight gain for grouper (Epinephelus tuuoina) was estimated to be around 50% (Teng et al., 1977). However, it was suggested that 40% protein was the most economical level based on the formulation. Sukhawongs et al. (1978) conducted experiments in which two sizes of EpinepheEus tuuvinu (20-30 g and 60-70 g body weight) were fed diets with varying levels of protein (30, 40, 45 and 50%). The best weight gain was observed at 50% dietary protein level. An optimum dietary protein level of 47-60% for Epinephelus tuwinu was also reported by El-Dakour and George (1982). Teng (1979) found that 40% dietary protein was the optimum level for Epinephelus sulmoides (formerly cited as E. tuuuinu). Wongsomnuk et al. (1978) observed a trend for a higher protein requirement of smaller-sized fish which was similar to that of other fish species. Teng et al. (1978) determined the optimum dietary protein level for 65-170 g estuarine grouper (E. sulmoides) fed to satiation with moist diets having sun-dried tuna muscle as the protein source to be 40% on a dry matter basis. The dietary energy of the 40% protein diet was 3302 kcal kg- ’ on a dry weight basis which was calculated, based on energy values of 3.9, 8.0, and 1.6 kcalg-’ for protein, lipid and carbohydrate, respectively, giving a P:E ratio of 121 mg of protein per kcal. The best diet had a lipid content of 13.5% dry weight basis. The optimum protein:energy ratios reported for Epinephelus tuuvinu weighing 60130 g was about 94 mg kcal- ’ GE, and 142 and 162 mg kcal - ’ DE for E. muluburicus and E. striutus, respectively as cited by Tucker (1991). New (1987) reported that the optimum dietary lipid level of grouper was about 14% in the diet.

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3.3. Vitamin and mineral requirements Vitamin C is the only vitamin that has been studied in grouper, E. tauuina (Boonyaratpalin et al., 1993b). A study was conducted to determine the effects of vitamin C in the form of L-ascorbyl 2-phosphate-Mg on feeding rate, growth, feed efficiency, % hydroxyproline of protein, survival, and deficiency signs in juvenile grouper, E. tauuina. A practical diet was supplemented with 0, 30, 60, and 100mg of L-ascorbyl 2-phosphate-Mg per kg of dry diet. The experiment was carried out for 16 weeks in aquaria. The feeding rate, growth, feed efficiency, % hydroxyproline of protein and survival of fish fed the diet without supplemental L-ascorbyl 2-phosphate-Mg were significantly lower (P < 0.05) compared with other treatments. Fish fed the diet without supplemental L-ascorbyl 2-phosphate-Mg showed deficiency signs, such as loss of appetite, short snout, erosion of the opercula and fins, hemorrhaging eyes and fins, exophthalmia, swollen abdomen, abnormal skull, falling pharyngobranchials, severe emaciation, scoliosis and lordosis. The minimum level of L-ascorbyl 2 phosphate-Mg required for normal growth was 30mg kg-’ dry diet. No published information is available for mineral and other nutrient requirements. 3.4. Feeds and feeding The traditional feed for grouper in floating net cages is trash fish, similar to sea bass. Presently, a commercial slow sinking, extruded feed is available in some Asian countries: this commercial feed is believed to contain not less than 43% crude protein, not less than 6% fat, not more than 16% ash, 3% fibre and 12% moisture. Practical feed formulations based on availability of local feed ingredients (Tables 7 and 8) have been recommended by Kanazawa (1984) and Tacon and Rausin (19891, respectively. Experimental feeds for seabass were successfully used by grouper in the vitamin C requirement experiment (Boonyaratpalin et al., 1993b). Chua and Teng (1978) conducted a three month study on the effect of feeding

Table I Composition

of a formulated

diet for grouper

and seabass (Kanazawa,

1984)

Ingredient

Percentage

Fish meal Meat and bone meal Soybean meal Sesame cake meal, expellar Groundnut meal, expellar Ricebran, solvent extracted Leaf meal Tapioca Vitamin and mineral mixture Soybean or corn oil Squid or pollack liver oil BHT Ethoxwuin

34 10 15 5 5 10 5 8 1 4 3 0.02 0.015

M. Boonyaratpalin/Aquaculture Table 8 Composition

of formulated

test diets for grouper (Tacon and Rausin,

Ingredient

295

19891

Formulation 1

Brown fish-meal Shrimp head meal Squid liver powder Suehiro UCF Wheat middlings Wheat flour Zeolite Fish oil Soy lecithin Choline chloride (50%) Vitamin premix AGJT/Fl Mineral premix AGJT/Fl Total

151 (1997) 283-313

75

a b

8.6 IO 5 4.2 0.75 0.40 0.33 0.037 100.067

2 66 5 5 5 3 10 0.75 3.8 0.75 0.40 0.33 0.037 100.067

* Vitamin premix AGJT/Fl supplies per kilogram of dry diet: vitamin A, 4000 IU; vitamin D,, 2000 IU; vitamin E, 200mg; vitamin K,, 8 mg; thiamin, 32 mg; riboflavin, 40mg; pyridoxine, 32 mg; pantothenic acid, 120mg; nicotinic acid, 160mg; biotin, 0.4mg; folic acid, 8mg; vitamin B,,, 0.04 mg; inositol, 300 mg; vitamin C, 8OOmg. ’ Mineral premix AGJT/Fl supplies per kilogram of dry diet: iron, 30mg; zinc, 50mg; manganese, 25mg; copper, 3 mg; cobalt, 0.5 mg; iodine, 3 mg; trivalent chromium, 0.25 mg; selenium, O.lOmg.

frequency on growth of young E. tauvina cultured in floating net cages. Seven feeding frequencies in the order of one feeding in 5 days, 4 days, 3 days, 2 days and 1 day, two feedings daily and three feedings daily was studied. Optimal growth, good feed conversion ratio as well as higher survival rate were observed in the treatment fed to satiation with one feeding every 2 days. Weight gain was substantially reduced in treatments fed to satiation with one feeding every 5, 4, and 3 days. No enhancement in growth was observed when the feeding frequencies were increased to two or three feedings daily. The fact that feed conversion ratios were similar in fish fed to satiation with one feeding in 5, 4, 3, and 2 days suggests feed intake to be important as a growth limiting factor. Total feed intake was appreciable in fish fed once in 2 days. Feed intake was found to be closely related to the amount of feed remaining in the stomach, intake being maximal when the stomach was empty. The food deprivation time of grouper is about 36 h at which time over 95% of the feed is digested at water temperature of 30 f 1°C. Hence, feeding the fish at 48 h intervals, i.e. once every 2 days, greatly enhanced maximum intake and efficient utilization of the feed. Dawes (1930), Moore (194 I> and Hickling ( 1962) have reported that if a second meal was taken too soon after the first, or if fish accept too much food, digestion may be less efficient. The effect of food ration on growth and yield of grouper raised in floating net-cages has been investigated. The optimum ration given on alternate days was 5% body weight which gave the best mean fish weight, uniform condition factor with time, relatively good survival rate, and best feed efficiency. The maintenance, optimum and maximum food rations were 1.41, 5.75, and 9.0% body weight, respectively. The fish were more uniform in size when fed 5-8% body weight. Although the yields at the end of the

296

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151 (1997) 283-313

experiment and one of weight was 5% of body

were higher with higher ration rate, the difference between a ration of 5% 9.1% body weight was 26.8-33.6%, while that between 5% and 2% body 596%. For economic production, the feeding rate should be approximately weight supplied every 2 days (Chua and Teng, 1982).

4. Milkfish

Chanos chanos

4. I. Introduction Milkfish, or Chanos are known as bangus in the Philippines, is an economically important and popular food and bait fish in Southeast Asia. Milkfish is widely distributed throughout the tropical and sub tropical region of the Indian and Pacific Ocean (Chen, 1976). It is extensively cultured in the Philippines, Indonesia and Taiwan. Chanos is best suited for culture because of its efficient use of natural food, using whatever food is available in the environment (Kumagai and Bagarinao, 1981) which results in faster growth than in any other herbivorous fish. Milkfish have other characteristics that favour coastal aquaculture. They can tolerate and adapt to salinity changes from 0 to 150 ppt (Crear, 1980) and are resistant to disease and handling. Although milkfish are a very tasty table food, they are very bony. A manual deboning technique has been developed in the Philippines. The culture of milkfish on a large scale is carried out in the Philippines, Indonesia and Taiwan. Milkfish farming is generally believed to have started in Indonesia at least 500 years ago, (Schuster, 1952). It was introduced to the Philippines and Taiwan in the 16th century (Ling, 1977). Milkfish is the single most important species produced through aquaculture in these countries. In 1983, almost 32000 t of milkfish were produced annually from 16000 ha or farmed milkfish which contributed to 18.88% of total aquaculture production in Taiwan (Taiwan Fisheries Bureau, 1983). In the Philippines, milkfish is the major culture species and the annual yields from freshwater pens and brackish-water ponds are increasing steadily (Sampson, 1984). In Indonesia, milkfish is a high value food fish. Throughout these countries, the general practice of milkfish farming is in shallow brackish-water pond systems or by a fertilization culture method, however, the yields vary considerably. The average annual production in Taiwan is about 2000 kg ha-’ (Liao and Chen, 1986) as compared to only 870 kg ha-’ in the Philippines (Sampson, 1984) and 450kghaa’ in Indonesia (Chong et al., 1984). These differences in production are mainly attributed to management skills. Besides, being cultured in brackish-water ponds, milkfish have been extensively grown in freshwater pens in Laguna de Bay in the Philippines with an annual yield of about 4 t ha ’ (Camacho and Macalincag-Lagua, 1988). The deep water pond culture or feeding culture method has been developed and improved in Taiwan, where the unit productivity may reach 12 000 kg ha-’ (Huang, 1981). In recent years, many milkfish farmers have started culturing other high-value species such as shrimp. However, longline fishery demand for baitfish has encouraged some milkfish farmers in Taiwan to specialize in fingerling production for baitfish. Thus, in

M. Boonyaratpalin/Aquaculture Table 9 Dietary protein requirements

297

151 (1997) 283-313

of milkfish

Fish size (8)

Protein requirement

0.01-0.035 0.04 0.5-0.8 2.8

52-60 40 30-40 42.8

(% of diet)

References Camacho and Bien (1983) Lim et al. (1979) Pascual(1984) Coloso et al. (1988)

recent years, milkfish farming in brackish-water areas has become less attractive compared to shrimp farming (Liao and Chen, 1986).

when

4.2. Nutrient requirements 4.2.1. Protein and amino acid requirements Studies show that milkfish fry (40mg initial weight) require 40% dietary protein for maximum growth, feed efficiency and high survival (Lim et al., 1979). This value is much lower than the recommended protein level of about 52-60% by Camacho and Bien (1983) (Table 9). Studies on the protein-energy requirement showed that 30-40% dietary protein, 10% lipid and 25% carbohydrate was required by milkfish fingerlings weighing OS-0.8g (Pascual, 1984). The dietary protein requirement of milkfish juveniles of 22Sg initial weight was 42.8% and the optimal metabolizable energy to protein ratio was 9.10-9.29 (Coloso et al., 1988). Milkfish can be assumed to require the same 10 essential amino acids (EAA) as other species. Leucine, lysine and arginine are most likely to be the first limiting amino acids since they occurred in high concentration in the amino acid pattern of protein from the whole body of milkfish juveniles (Coloso et al., 1983) (Table 10). This pattern can also be used as a basis for estimating milkfish requirements for the essential amino acids

Table 10 Amino acid composition Amino acid

and A/E

ratios of milkfish protein (Coloso et al., 1988)

Milkfish muscle Amino acid (g lOOg_’

Arginine Histidine Isoleucine Leucine Lysine Methionine Half-cystine Phenylalanine Tyrosine Threonine Tryptophan Valine a A/E

protein)

A/E

4.23 2.5 4.4 7.94 7.9 2.3 1.14 4.35 3.06 4.69 1.06 4.81

ratios are (each EAA/total

EAA including

12.4 4.95 8.73 15.8 15.6 4.58 2.25 8.62 6.08 9.31 2.11 9.55 half-cystine

+ tyrosine) X 100

ratio a

298 Table 11 Quantitative

M. Boonyararpalin/Aquaculture

amino acid requirement

151 (1997) 283-313

of milkfish

lOOg_’ protein)

Amino acid

Requirement

Arginine Histidine Isoleucine Leucine Lysine Methionine and cystine Methionine and cystine Methionine and cystine Phenylalanine and Tyrosine Phenylalanine and Tyrosine Threonine Tryptophan Valine

5.25 (2.10/40) a 2.0 (0.80/40) 4.0 (1.80/45) 5.1 (2.3/45) 4.0 (2.0/50) 2.50 (1.0/40) and 0.75 (0.3/40) 2.7 (0.98/36) and 0.78 (0.28/36) 1.5 (0.54/3) and 4.1 (1.48/36) 4.22 (1.90/45) and 1.00 (0.45/45) 2.80 (1.26/45) and 2.66 (1.20/45) 4.5 (1.80/40) 0.63 (0.3 l/49) 3.55 (1.60/45)

(g

a In parentheses, the numerators are the requirement are the percentage of total protein in the diet.

expressed

Reference Borlongan, 1991 Borlongan and Coloso, 1992 Borlongan and Coloso, 1992 Borlongan and Coloso, 1992 Borlongan and Benitez, 1990 Borlongan and Coloso, 1992 Sastrillo and Chiu-Chem, 1992 Sastrillo and Chiu-Chem, 1992 Borlongan, 1992a Borlongan, 1992a Borlongan, 199 1 Coloso et al., 1992 Borlongan and Coloso, 1992

as a percentage

of diet and the denominators

when the quantitative requirement for at least one essential amino acid is known (Cowey and Tacon, 1981; Jauncey et al., 1983; Santiago, 1985). Dietary essential amino acid requirements (as a percentage of dietary protein; Tables 11 and 12) of milkfish juveniles are as follows: arginine, 5.25; histidine, 2.0; isoleucine, 4.0; leucine, 5.1; lysine, 4.0; methionine, 2.5 (cystine 0.75); phenylalanine 4.22, (tyrosine, 1.0) or 2.8 (tyrosine, 2.66); threonine, 4.5; tryptophan, 0.63; valine 3.55 (Borlongan and Benitez, 1990; Borlongan, 1991, 1992a; Borlongan and Coloso, 1992; Coloso et al., 1992; Sastrillo and Chiu-Chem, 1992). However, the EAA requirements of milkfish do not completely agree with requirements of other fish species. The

Table 12 Comparison of requirements of milkfish (Chinos chinos) species expressed as a percentage of dietry protein

for 10 essential amino acids with those of other fish

Amino acid

Milkfish a

Japanese eel b

Red dmmC

Common carpb

Channel catfish b

Chinook salmon b

Arginine Histidine Isoleucine Leucine Lysine Methionine + cystine Phenylalanine + tyrosine Threonine Tryptophan Valine

5.2 2.0 4.0 5.1 4.0 3.2 5.2 4.5 0.6 3.6

4.5 2.1 4.0 5.3 5.3 3.2 5.8 4.0 1.1 4.0

3.7 1.7 2.9 4.7 4.4 3.0 4.5 2.8 0.8 3.1

4.3 2.1 2.5 3.3 5.7 3.1 6.5 3.9 0.8 3.6

4.3 1.5 2.6 3.5 5.1 2.3 5.0 2.0 0.5 3.0

6.0 1.8 2.2 3.9 5.0 4.0 5.1 2.2 0.5 3.2

a Borlongan and Coloso, 1992. b National Research Council, 1983. ’ Moon and Gatlin, 1991.

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299

threonine requirement is high compared to that of most other species. Similarly, the requirement for branched chain amino acid (leucine, isoleucine and valine) is high compared to that of other species. The lysine requirement is lower than that of most fish species. For the total basic amino acid (arginine, lysine and histidine), the value for milkfish is similar to that of most fish species. The EAA requirement pattern correlates well with the EAA pattern of milkfish tissue protein (Coloso et al., 1988 cited in Borlongan and Coloso, 1992). The requirement levels of arginine, leucine, lysine, tryptophan and valine were lower than those found in milkfish tissue proteins, but those for the other EAAs were similar. Protein constitutes the most expensive component of fish diets. Milkfish feed lower on the food chain, thus this information is important in formulating artificial feeds where an expensive animal protein can be partially replaced by cheaper plant proteins. Milkfish like other species utilize protein of animal origin better than plant proteins. Among animal proteins, fish meal and meat and bone meal have higher nutritive value than shrimp-head meal. Among plant feedstuffs, only soybean meal gave an acceptable growth and survival rate, and was superior to copra and L.eucena Zeucocephalu meals (Samsi, 1979). Studies on the feasibility of using soybean meal to replace fish meal as a protein source for milkfish have indicated that up to 61% of fish meal can be replaced by soybean meal with a methionine supplement without any adverse effect on milkfish growth and feed conversion (Shiau et al., 1988). Alava and Lim (1988) reported that soybean meal in artificial diets can be replaced by corn gluten meal. Meat and bone meal can be substituted for shrimp head meal. The control diet had 30% fish meal, 16% shrimp head meal and 20% soybean meal. Digestibility of protein in milkfish reared in seawater could be divided into three groups: the most digestible (gelatin), moderately digestible (casein, defatted soybean meal and fish meal) and the least digestible (15. Zeucocephalu meal). No such distinct groups as observed in seawater were evident in freshwater milkfish, although gelatin was still the most digestible protein and L. leucocephulu meal the least (Table 13). There was an apparent increase in digestibility as a function of fish size for casein, fish meal, and defatted soybean meal but not for gelatin and leaf meal. Digestibility of all

Table 13 True-protein al., 1986)

digestibility

Feedstuff

of some feedstuffs

by two sizes of milkfish

and seawater

Protein digestibility Freshwater

Casein Gelatin Soybean meal Fish meal Leaf meal a Unrealistic

in freshwater

value.

Seawater

6Og

175g

6Og

175g

83 94 69 70 39

88 93 92 73 42

49 99 54 55 31

65 98 59 70 -10”

(Ferraris et

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M. Boonyaratpalin/Aquaculture

feedstuffs tested was consistently gelatin (Ferraris et al., 1986).

151 (1997) 283-313

lower in seawater compared

to freshwater

except for

4.3. Lipid requirements The dietary requirement of 0.83 g mean body weight milkfish fingerlings for lipid (cod liver oil) is about 7-10% (Alava and de la Cruz, 1983). This is similar to recommended dietary levels of 8-10% lipid from corn oil and cod liver oil (1: 1 ratio) for milkfish fry (Carnacho and Bien, 1983). Histology of the milkfish livers showed that cellular and structural integrity was maintained when diets contained about 7-10% dietary lipid (Alava and de la Cruz, 1983). Lipid levels lower than 7% resulted in decreased granulation and loss of nuclei of liver cells. Dietary lipid exceeding 10% caused minor disruption of hepatocytes owing to formation of large lipid vacuoles, loss of hepatic cord with development of fibrous tissues, and occurrence of pyknotic nuclei (Alava and de la Cruz, 1983). With the use of purified test diets, Bautista and de la Cruz (1983) found that growth and survival of milkfish (1.6 g body weight) fed diets containing linoleic and linolenic acids were significantly higher than those of fish fed lipid-free diets or diets with 7% lauric acid. Although higher growth was attained by fish fed a diet with 1% linolenic acid, growth and survival of fish fed with linoleic and linolenic acids were not significantly different. Fatty acid analysis revealed that the lipid-free diet and the diet with lauric acid increased the level of monoenoic acids in the fish while diets with linoleic and linolenic acids decreased the monoenes and increased the level of longchained polyunsaturated fatty acids. Results suggest that both linoleic and linolenic acids are effective in promoting high growth and survival rates in milkfish (Bautista and de la Cruz, 1983). Hence, cod liver oil (high in linolenic acid) and corn oil (high in linoleic acid) are good sources of lipid for milkfish fry and fingerlings. There are indications that milkfish have the ability to use linoleic and linolenic acids as precursors for the biosynthesis of long-chain polyunsaturated fatty acids of the n-6 and n-3 series (Gorriceta, 1982; Villegas et al., 1983). The essential fatty acid (EFA) requirement of milkfish was examined in a 12-week feeding trial using purified diets at a water temperature of 28-29°C and salinity of 32 ppt. The test diets contained varying levels of 18:0 (triglyceride form, TG), 18:3 n-3, 18:2 n-6 and n-3 highly unsaturated fatty acids (n-3 HUFA). Milkfish juveniles were starved for 7 days and than fed a lipid-free diet for 30 days before the initiation of feeding trials. Low growth and feed efficiency together with higher mortalities were observed in fish fed the lipid-free diet as well as in those on the EFA-deficient diet. Supplementation of 2% 18:2 n-6 to the tristearin-based diet did not improve growth rate of milkfish as effectively as feeding with n-3 fatty acids. The highest weight gain was obtained in milkfish fed a combination of 5% 18:0 + 1.0% 18:3 n-3 + 0.5% 205 n-3 + 0.5% 22:6 n-3 although the supplementation of 2% 18:3 n-3 alone or combination of 0.5% 20:5 n-3 + 0.5% 22~6 n-3 to the tristearin-based diets was also effective in improving of growth. Thus, n-3 fatty acids, such as 18:3 n-3 and n-3 HUFA were nutritionally more important than 18:2 n-6 for milkfish. This shows that n-3 HUFA was more efficiently utilized compared to 18:3 n-3 and a combination of 18:3 n-3 and n-3 HUFA gave the best performance. The fatty acid composition of the polar lipids from

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301

the whole body of milkfish juveniles fed the various test diets was influenced by the composition of the dietary fatty acids (Borlongan, 1992b). Signs of essential fatty acid deficiency were growth depression, increased level of monoenic acids, decreased level of polyunsaturated fatty acids, liver abnormalities such as lipid infiltration in the blood vessels and cellular swelling (Bautista and de la Cruz, 1983) fin erosion and darkening of the upper pigmented surface one or two days prior to death (Borlongan, 1992b). Milkfish reared in seawater had a significantly higher content of phospholipids compared to those reared in freshwater (Borlongan, 1992b). Phospholipid content ranged from 21 to 26% in organs of fish reared in seawater and a level of 13-21% for fish reared in freshwater. The gills had lower levels of phospholipids for fish reared in freshwater. Comparison of fatty acid patterns of total lipids from various organs of fish reared in freshwater and seawater showed similar patterns in the livers, intestine and depot fat. However, marked differences were noted in fatty acid patterns of the gills and kidneys. The gill from seawater reared fish contained large quantities of unsaturated fatty acids (72.5%) and much lower quantities of saturated fatty acids (27.5%). The opposite was observed in freshwater samples where the gills contained larger quantities of saturated fatty acid (84.9%) than unsaturated fatty acid (15.0%). Information on lipid composition of fish can be used to make references about dietary requirements (Castell, 1979). This observation of the effect of salinity on fatty acid composition may indicate that milkfish reared in seawater may have a higher requirement for 3-n fatty acid than freshwater reared milkfish. Further studies are necessary to determine the specific lipid and essential fatty acid requirement of milkfish under various salinity conditions. 4.4. Other nutrients The carbohydrate requirement of milkfish has not been studied. However, like other fish, milkfish may not have a specific dietary carbohydrate requirement, but probably use carbohydrate as an energy source more efficiently than coldwater fish. Diets containing up to 35% dextrin have been used successfully in experiments designed to determine other nutrient requirements. Commercial feeds in Taiwan used for pond feeding contain 45% or more of total carbohydrate. Very little is know about the vitamin and mineral requirements of milkfish. Nevertheless, various vitamin and mineral premixes, such as those intended for the coldwater fish, chinook salmon (Halver, 1957) and for other warm-water fishes (National Research Council, 1977) have been used for milkfish (Lee and Liao, 1976; Lim et al., 1979; Santiago et al., 1983; Piedad-Pascual, 1983) with satisfactory results. 4.5. Feed and feeding Lee and Liao (1976) developed a purified diet for milkfish which resulted in acceptable growth rates. Vitamin-free casein (about 60% of the diet) supplemented with 0.5% L-tryptophan supported better growth rates than a combination of casein and gelatin for young milkfish of 1.7 g body weight. Soybean oil (10% of diet) was better as a lipid source than shark liver oil. Vitamin and mineral mixtures were added to the diet at 4 and lo%, respectively, as recommended by Halver (1957) for chinook salmon. This

302

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Table 14 Example of a 40% crude protein diet for milkfish (Alava and Lim, 1988) Ingredient

% in diet

Anchovy fish meal Shrimp head meal Soybean meal Ricebran Wheat flour Cod-liver oil Vitamin mix a Mineral mix b

30.0 16.0 20.0 11.5 15.0 3.0 1.0 3.5

a Complete vitamin mix for warm-water fish. b One-half the amount of mineral mix for purified warm-water

fish diets.

purified diet also contained dextrin as the carbohydrate source and a high level of carboxymethyl cellulose (10%) as a binder. Teshima et al. (1984) also developed a purified diet for milkfish fingerlings. They found that a higher growth rate occurred when a diet containing 35% casein and 15% gelatin, supplemented with 0.5% methionine and 0.5% tryptophan was fed at 30-50% of fish biomass twice daily. Efforts have been made to develop artificial diets for milkfish using available information on milkfish feeding habits and nutrient requirements along with information derived from other species. Practical feeds for fry have been formulated and used for fish grown in freshwater (Santiago et al., 1983, 1989) and seawater (Alava and Lim, 1988). An example of a practical diet formula for milkfish fry is given in Table 14. Commercial feeds used at present for semi-intensive pond culture in Taiwan contain more than 24% crude protein, more than 3% lipid, less than 16% ash and less than 6.5% fiber (Jettanalin, J., personal communication, 1993). Since milkfish is an efficient feeder and feeds at the bottom of the food chain, natural pond food makes a valuable contribution to its nutrient uptake. Thus, these diets are assumed to be sufficient for satisfactory milkfish growth. A model formula of a practical pond feed for milkfish and milkfish broodstock are presented in Tables 15 and 16, respectively. According to Schuster (19601, milkfish in all stages of life feed during the daytime. Banno (1980) also found that wild milkfish fry feed during daylight hours (06:00- 19:OO) Table 15 Model formula of a practical

pond (26% protein) feed for milkfish (Lim, 1991)

Ingredient

% in diet

Fish meal, anchovy or menhaden Soybean meal 48% protein Grains or grain by product Pellet binder ’ Dicalcium phosphate Vitamin premix b Mineral premix ’

8.0 31.5 56.0 2.0 1.5 0.5 0.5

a Pellet binder may be hemicellulose or lignin sulfonate. b Vitamin mix for supplemental diets for warm-water fish. ’ Mineral mix for practical diets for warm-water fish.

M. Boonyaratpalin/Aqwculture Table 16 Composition

151 (1997) 283-313

of a 36% crude protein diet for milkfish broodstock

(Lim, 1991)

Ingredient

% in diet

Fish meal: anchovy or menhaden Soybean meal Wheat meal Corn meal Fish oil Dicalcium phosphate Vitamin premix a Mineral premix b

22.0 35.0 15.0 20.9 4.6 1.0 1.0 0.5

a Complete vitamin mix for warm-water fish. b Mineral mix for practical diets for warm-water

303

fish.

with most of the feeding activity occurring between 07:OO and 13:OOh. Kawamura and Hara (1980) demonstrated that milkfish fry depend primarily on vision during feeding. The ability to take limited amounts of food in the dark increased with size and age. This increase may be attributed to a gradual development of chemical and auditory sensory mechanisms. Subsequent studies showed that although older milkfish (2-3 kg) feed day and night, significantly higher feeding activity occurred during the day (Kawamura and Castillo, 1981). Tampi (1958) suggested that the adult milkfish in the sea feeds by browsing. Several studies have shown that milkfish from the fry to adult stage can be reared successfully on artificial diets. Before the development of artificial diets, during the one-to-two-week holding period, milkfish fry were fed hard boiled egg yolk. A shift from natural food to an artificial diet has been successful in hatchery produced larvae (Duray and Bagarinao, 1984). Fifteen-day-old larvae which were reared on rotifers prior to the experiment were fed six commercial and experimental diets with Artemia nauplii as a control. Survival rate of the larvae fed the artificial diets was comparable to, or significantly higher than, the survival rates of larvae fed with the Artemia nauplii. Although mean body weights were highest for larvae fed the Artemia, mean condition factor and standard lengths were not significantly different among the treatments. Feeding rate for milkfish is affected by size, water quality, feeding frequency and nutrient density of the diets, especially energy content. As with other fish, feed consumption rate of milkfish is inversely related to fish size. For example, with a diet containing 40% protein and 3450 kcal of ME per kg, a daily feeding rate of 20% of biomass is optimum for 7.7mg milkfish fry reared under laboratory conditions (Lim, 1978). For fish averaging 0.60 g, feeding at 9% of the body weight resulted in a 130% increase in weight gain over a 5% feeding rate (Chiu et al., 1987). In a pond environment where natural food is abundant, milkfish grown to marketable size are fed with commercial pellets containing 23-27% protein at a daily rate of 3-4% of body weight (Benitez, 1984). Milkfish, like most other species benefit from multiple daily feedings. The growth and feed efficiency of 0.6g fingerlings fed at 5 or 9% body weight increased by about 20% when the feeding frequency was increased from four to eight times daily (Chiu et

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I51 (1997) 283-313

al., 1987). Under pond conditions, milkfish are normally fed two to three times daily (Liao and Chen, 1986). Feed is offered to fish by hand or by automatic feeders. The latter is commonly used in Taiwan. Automatic feeders equipped with two pipes extending toward the pond are installed on the dikes. The feeders contain devices that can be adjusted to deliver measured quantities of feed at given time intervals. Variable results were obtained when artificial diets were fed to milkfish in shallow water ponds. Pelleted feeds (37.4% crude protein) considerably increased fish production as compared to lab-lab or plankton as the main food for the milkfish (Fortes, 1984). However, commercial chick starter pellets (21% crude protein) when used as a supplemented diet for milkfish fingerlings (16.3 g body weight) did not significantly increase growth, survival or production in fertilized ponds (Otubusin and Lim, 1985). Milkfish fed diets containing 42% crude protein, 13.1% crude fat and 33.2% nitrogen-free extract during the last month of culture were heavier (141 g) than unfed fish (1OOg) in experiment one (dry season) but had similar weights (44 and 41 g) in experiment two (rainy season). This suggests that feeding milkfish was not profitable during the cooler months. Undoubtedly, the effectiveness of an artificial diet in enhancing fish production is influenced by factors such as the nutrition quality of the diet, stocking rate or fish biomass, level of fertilization or natural food production and water temperature (Pascual et al., 1991).

5. Siganids

Sganus

spp.

5.1. Introduction The rabbitfish, family Siganidae, is considered to be an excellent food fish in many parts of the world especially in the eastern Mediterranean and Indo-Pacific regions (Lam, 1974). Rabbitfish hold particular promise for marine aquaculture development by virtue of their herbivorous/omnivorous feeding habits and consequent ability to feed low on the aquatic food chain (Tacon et al., 1990). Of the rabbitfish species, S. argenteus, S. canialiculatus, S. guttatus, S. javus and S. rivalutus are good candidates for culture because of their high tolerance to environmental factors, rough handling and crowding (Carumbana and Luchavez, 1979). During culture, growth of rabbitfish may be fast in some periods and slow in others. Horstmann (1975) reported the highest growth rate of 5.0-6.5 g per week for all the rabbitfish species. In nature, rabbitfish feed on algae, resulting in suboptimum growth and inconsistent production. In captivity, however, rabbitfish can be trained to readily accept artificial feeds, making them feasible to be grown on a commercial scale (Parazo, 1990). 5.2. Nutrient requirements 5.2.1. RabbitjGh larvae Hara et al. (1986) suggested that S. guttatus larval require 53-59% crude protein in commercial diets whereas 40% crude protein was adequate during hatchery production as had previously been suggested by Juario et al. (1985). However, in these studies, a comparison of survival and growth performance of rabbitfish larvae fed artificial diets

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versus live food was not made. Recently, Parazo (1991) conducted a feeding trial, using artificial feeds (125 pm) with graded protein levels in comparison with Artemia nauplii for S. guttutus larvae. Larvae performed equally well on all artificial feeds while Artemia fed larvae exhibited poor growth and low survival. This was probably due to suboptimum feeding rate and/or to Artemia quality being nutritional deficient. It was concluded that an artificial feed with 40% protein was sufficient for rabbitfish larvae. Few studies have been done on the energy requirement or the ability of rabbitfish larvae to utilize various energy sources. Parazo (1991) found that rabbitfish larvae utilized carbohydrate more efficiently than seabass and grouper larvae. Inclusion of 37% carbohydrate in rabbitfish feeds did not adversely affect larval growth and did not alter fish carcass protein content. Parazo (1991) was successful in feeding up to 10% cod liver oil in experimental diets for rabbitfish larvae. It was postulated by Parazo, that the fish are capable of utilizing dietary fat and carbohydrate to the extent of sparing protein for growth and recommended a total energy content of 3900 kcal kg-’ in rabbitfish larval feeds. Essential fatty acid requirements of larval siganids are still not known. However, Watanabe et al. (1983) reported suboptimum growth and development of siganid larvae fed Artemiu which contained low levels of polyunsaturated fatty acids. Improved growth of S. guttatus larvae was observed by Sorgeloos et al. (1988) when the Artemia were given enrichment diets. 5.3. Fry Soletchnik (1984) found that feed intake of rabbitfish fry was affected by dietary energy. S. guttatus consumed low amounts of high energy feed and resulted in low growth and feed efficiency. Soletchnik (1984) recommended that feeds for optimum growth of rabbitfish fry should contain total energy about 3700 kcal kg- ’ , 33% protein, 10% fat and 20% ash. In another study with S. guttutus fry, Parazo (1990) observed that growth rate of fish increased with protein and energy levels. It was recommended that feeds containing 35% protein and 3832 kcal/kg should be economical for S. guttatus fry. Despite the similar findings for the protein requirement in the above-mentioned studies, reported protein requirements may vary for rabbitfish species. For S. jams, better growth was obtained with feeds containing 35-46% protein (Basyari and Tanaka, 1989). Fry of S. canaliculatus had poor growth rates when fed low protein diets but showed rapid growth when fed diets containing 58% protein (Basyari and Tanaka, 1989). 5.3.1. Rabbit&h grow-out Nutritional recommendations for rabbitfish in a grow-out system were elucidated by means of feed comparisons. Grow-out trials were carried out in earthen ponds and floating cages. Tacon et al. (1990) evaluated seven different diets fed to S. canaliculatus held in floating cages for 100 days. They found that the best growth and feed efficiency was observed for rabbitfish fed a diet containing 31% crude protein 8% lipid and 38% carbohydrate. These results agreed with other studies reported earlier by Bwathondi (1982) and Ismael et al. (1986). Success in using feeds with protein content below 30% for rabbitfish has also been reported in earthen ponds with natural food. Emata (1991)

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reported that a supplemental diet containing 26% protein promoted higher growth of rabbitfish in ponds than fish fed diets containing 21% protein. This is due to the fact that rabbitfish are opportunistic omnivores, capable of feeding on amphipods, copepods, sponges, Foraminifera, crustaceans and brittle stars (Bwathondi, 1982). 5.3.2. Rabbitfish broodstock Soletchnik (1984) suggested that 5. guttutus broodstock should be maintained on a diet with low energy, low protein and high ash content. The recommended maintenance feed contained 17% protein, 5% fat, 42% NFE, 36% ash and fiber and total energy of 2800 kcal kg-‘. For spawning purposes, the fish should be fed a diet with 40% protein, 5% fat, 36% NIX, 19% ash and fiber and total energy of 3500 kcal kg-‘. Lipids are important in promoting spawning frequency, viable eggs and larval survival. A single female spawned for four successive months when fed with a diet with 10% pollack or cod liver oil (Hara et al., 1986). Diets rich in cod liver oil alone or in combination with soybean lecithin induced repeated spawning for 13 consecutive months. Cod liver oil at 18% in the formulated diets fed to broodstock of S. guttutus resulted in more eggs spawned and better larval survival than for those fed lower lipid diets (Anon, 1988). 5.3.3. Feed and feeding Larvae of rabbitfish start to consume exogenous food, mainly zooplankton, after day three of hatching (Bagarinao, 1986). The provision of suitable food during this period is needed for the larvae to survive. Soh and Lam (1973) observed that siganid larvae did not feed on green algae and died of starvation. Feeding with Brachionus (less than 90 p) at lo-20 individuals per ml improved the survival rate of first-feeding larvae (Duray, 1986). I n t h e h a t c h ery, rabbitfish larvae are fed with Brachionus, Artemia nauplii and artificial diets (May et al., 1974; Hara et al., 1986). The use of artificial diets for rearing siganid larvae poses some difficulties associated with particle size requirement, acceptability and digestibility, feed distribution and water quality problems. Finely powdered (40- 100 pm) artificial feeds have been tried with limited success. However, a successfully tested artificial diet (Table 17) for larval rabbitfish has recently been recommended by Parazo (199 1).

Table 17 Example of a feed formulation

for larval rabbitfish

(Parazo,

1991)

Ingredient

%

Shrimp meal Fish meal Squid meal Bread flour Cod-liver oil Vitamin mix Mineral mix Kappa-carraget BHT Cellulose

14.50 14.50 13.40 37.60 7.10 3.0 2.0 5.0 0.05 2.85

man

M. Boonyaratpalin/Aquaculture Table 18 Example of a feed formulation

for grow-out

Ingredient

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307

rabbitfish %

Formula I (Tacon et al., 1990) Brown fish meal Soybean meal Wheat middlings Wheat flour Fish oil Soybean oil Choline chloride (50%) Vitamin premix

22.0 25.0 38.55 10.0 2.0 2.0 0.25 0.20

Formula 2 (Abu Hassan et al., 1984) Fish meal Soybean meal Groundnut meal Rice bran Copra cake meal Leaf meal Wheat flour Corn meal Vitamin mix

15.0 25.0 5.0 26.5 10.0 5.0 8.0 5.0 0.5

While rabbitfish larvae are zooplankton feeders, the fry and adults are primarily herbivorous (Suyehiro, 1942). They feed by nibbling on the marine vegetation, often browsing in schools with heads directed downward (Munro, 1967). In captivity, rabbitfish become omnivorous, ingesting algae and a variety of feedstuffs, e.g. fish scraps, mussel and shrimp meat, rice bran, chicken and rabbit pellets (Van Westernhagen, 1974). This makes it easy to feed rabbitfish with artificial dry diets. Diets for grow-out rabbitfish are similar in composition to those for cultured omnivorous fish with a protein content of 30% (Conrad, 1987; Tacon et al., 1990). Examples of formulations which have been found to be suitable for rabbitfish are shown in Table 18.

Acknowledgements I would like to thank the following individuals for their kind and unselfish assistance in preparing this paper. To I. Csavas, C.B. Santiago, C. Lim and I.G. Borlongan-for providing, despite my requesting them at such short notice, the various references, literature and information used in this review; to G. Rao, A. Sermwatanakul, W. Jantrarotai, J. Phonmaneerat for helping me identify and focus on the relevant and specific information; and to R. Udomlarp for her very patient assistance in assembling and processing the manuscript into its present form.

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References Abu Hassan, I., Sayuthi S. and Chaim, C.S., 1984. Fabrication of feed suitable for smallholder aquaculture. FAO, Rome, FI:DP/MAL/77/008 Field Documents 2: pp. 261-278. Alava, V.R. and de la Cruz, M.C., 1983. Quantitative dietary fat requirement of Chinos chanos fingerlings in a controlled environment. Presented at the 2nd International Milkfish Aquaculture Conference, 4-8 October, Iloilo, Philippines. Alava, V.R. and Lim, C., 1988. Artificial diets for milktish, Chanos chanos (Forsskal), fry reared in sea water. Aquaculture, 71: 339. Anon, 1988. Reproductive performance of hatchery-bred .Siganus gutfatus broodstock fed different levels of fat. Annual Report of Aquaculture Department. SEAFDEC No. 3. Bagarinao, T., 1986. Yolk resorption, onset of feeding and survival potential of larvae of three tropical marine fish species reared in the hatchery. Mar. Biol., 91: 449-459. Banno, J.E., 1980. The food and feeding habit of the milkfish fry Chinos chanos (Forsskal) collected from the habitats along the coast of Hamtik, Antique. MS. Thesis. University of the Philippines in the Visayas, Iloilo, 77 pp. Basyari, A. and Tanaka, H., 1989. Studies on rearing of rabbitfish-1. Effect of different protein level on the growth of Siganus jams. Scientific report of Mariculture Research and Development Project (ATA-192) in Indonesia, no. 85, pp. 10-16. Bautista, M.N. and de la Cruz, M.C., 1983. Effects of dietary linoleic and linolenic acids on growth, survival, fatty acid composition, and liver histology of milkfish fingerlings. Paper presented during the 2nd International Milkfish Aquaculture Conference, 4-8 October, Iloilo City. Benitez, L.V. 1984., Milkfish nutrition. In: J.V. Juario, R.P. Ferraris, and L.V. Benitez (Editors), Advances in Milkfish Biology and Culture. Island Publishing House Inc., Metro, Manila, Philippines, pp. 133-143. Boonyaratpalin, M., 1988. Seabass feed. In: Manual for Training Provincial Fisheries Officers. Prachuab Khiri Khan Coastal Aquaculture Research and Development Center, Thailand, 21 pp. (in Thai). Boonyaratpalin, M. and Phongmaneerat, J., 1990. Requirement of seabass for dietary phosphorus. Technical Paper No. 4. National Institute of Coastal Aquaculture, Thailand, 20 pp. (in Thai). Boonyaratpalin, M. and Wanakowat, J., 1993. Effect of thiamine, riboflavin, panthothenic acid and inositol on growth, feed efficiency and mortality of juvenile seabass. In: S.J. Kaushik and P. Luquet (Editors), Fish Nutrition in Practice, Bjarritz (France) 1991. INRA, Paris, pp. 819-828. Boonyaratpalin, M., Unprasert, N., Kosutharak, P., Chumsungnern, S. and Sothana, W., 1988. Effect of choline, niacin, inositol, and vitamin E on the growth, feed efficiency and survival of seabass fingerling in freshwater. Technical Paper No. 7. National Institute of Coastal Aquaculture, Department of Fisheries, Thailand, 22 pp. (in Thai). Boonyaratpalin, M., Unprasert, N., Kosutharak, P., Sothana, W. and Chumsungnem, S., 1989a. Effect of different levels of vitamin C added in diet on growth, feed efficiency and survival rate of seabass. Technical Paper No. 6. National Institute of Coastal Aquaculture, Department of Fisheries, Thailand, 21 pp. (in Thai). Boonyaratpalin, M., Unprasert, N. and Buranapanidgit, J., 1989b. Optimal supplementary vitamin C level in seabass fingerling diet. In: M. Takeda and T. Watanabe (Editors), The Current Status of Fish Nutrition in Aquaculture. Tokyo University of Fisheries, Tokyo, Japan, pp. 149-157. Boonyaratpalin, S., Fryer, J.L., Hedrick, R.P., Supamattaya, K., Direkbusamkom, S. and Jadesadakraisom, U., 1990. Development of kidney disease and occurrence of pathogens in seabass (Lams calcarifer) fed two different diets, Technical Paper No. 8. National Institute of Coastal Aquaculture, Department of Fisheries, Thailand, 13 pp. Boonyaratpalin, M., Boonyaratpalin, S. and Supamattaya, K., 1992. Ascorbyl-phosphate-Mg as a dietary vitamin C source for seabass (Lares calcarifer). Presented at the 3rd Asian Fisheries Forum, 26-30 October 1992, Singapore. Boonyaratpalin, M., Wanakowat, J. and Borisut, C., 1993a. L-ascorbyl 2-phosphate-Mg as a dietary vitamin C source for grouper. Presented at the Seminar on Fisheries 1993, Department of Fisheries, Thailand, 16-17 September 1993. Boonyaratpalin, M., Wanakowat, J. and Hangsapreurke, K., 1993b. Pantothenic acid requirement of seabass. Presented at the 5th Asian Fish Nutrition Workshop, 27-31 January 1993, Thailand.

M. Boonyaratpalin/Aquaculture

151 (1997) 283-313

309

Borlongan, I.G., 1991. Arginine and threonine requirement of milktish (Chanos chanos Forsskal) juveniles. Aquaculture, 93: 313-322. Borlongan, I.G., 1992a. Dietary requirement of milkfish (Chinos charm Forsskal) juveniles for total aromatic amino acids. Aquaculture, 102: 309-317. Borlongan, LG., 1992b. The essential fatty acid requirement of milkfish (Chanos chanos Forsskal). Fish. Physiol. Biochem., 9: 401-407. Borlongan, I.G. and Benitez, L.V., 1990. Quantitative lysine requirement of milkfish (Chanos chanos Forsskall juveniles. Aquaculture, 87: 341-347. Borlongan, I.G. and Coloso, R.M., 1992. Lipid and fatty acid composition of milkfish (Chanos chanos Forsskal) grown in freshwater and seawater. Aquaculture, 104: 79-89. Borlongan, LG. and Parazo, M.M., 1991. Effect of dietary lipid sources on growth, survival and fatty acid composition of seabass (Lates calcarifer, Blochl fry. Israeli Aquac. Bamidgeh, 43: 95-102. Buranapanidgit, J., Boonyaratpalin, M., Watanabe, T., Pechmanee, T. and Yashiro, R., 1988. Essential fatty acid requirement of juvenile seabass, L.utescalcarifer. Technical Paper No. 3. National Institute of Coastal Aquaculture, Department of Fisheries, Thailand, 21 pp. (in Thai). Buranapanidgit, J., Boonyaratpalin, M. and Kaewninglard, S., 1989. Optimum level of w3HUFA on juvenile seabass, Lutes calcarifer. In: IDRC Fish Nutrition Project Annual Report. Department of Fisheries, Thailand, 23 pp. Bwathondi, P.O.J., 1982. Preliminary investigations on rabbitfish, S&anus canaliculatus cultivations in Tanzania. Aquaculture, 27: 205-210. Camacho, A.S. and Bien, N., 1983. Studies on the nutrient requirement of milktish Chanos chanos (Forsskal). Presented at the Tech. Symposium on Aquaculture, University of the Philippines, 17, 19 February, The Visayas. Camacho, A.S. and Macalincag-Lagua, N., 1988. The Philippines aquaculture industry, In: J.V. Juario and L.V. Benitez (Editors), Perspectives in Aquaculture Development in Southeast Asia and Japan. Aquaculture Dept., SEAFDEC, lloilo, Philippines, 91 pp. Carumbana, E.E. and Luchavez, J.A., 1979. A comparative study of the growth rates of S&anus canaliculatus, Siganus spinus and Siganus guttatus reared under laboratory and semi-natural conditions in Southern Negros Oriental. Philipp. Silliman J., 26: 187-209. Castell, J.D., 1979. Review of lipid requirements of finfish. In: J.E. Halver and K. Tiews (Editors), World Symposium on Finfish Nutrition and Fish Feed Technology, Hamburg, Germany. Heenemann, Berlin, Vol. 1, pp. 59-84. Chen, F.Y., Chow, M., Chao, T.M. and Lim, R. 1977. Artificial spawning and larval rearing of the grouper, Epinephelus tauuina (Forsskal) in Singapore. Singapore J. Pri. lnd., 5(l): 1-21. Chen, T.P., 1976. Aquaculture Practice in Taiwan. Fishing News Books Ltd., Surrey, UK, Chapter 1. Chiu, Y.N., Sumagaysay, N.S., and Sastillo, M.A.S., 1987. Effect of feeding frequency and feeding rate on the growth and feeding efficiency of milkfish Chanos chanos Forsskal, juveniles. Asian Fish. Sci., 1: 27. Chong, K.C., Pocmomo, A. and Kasryno, F., 1984. Economic and technological aspects of the Indonesian milk&h industry. In: J.V. Juario, R.P. Ferraris and L.V., Benitez (Editors), Advances in Milkfish Biology and Culture. Island Publishing House, Manila, 199 pp. Chua, T.E., and Teng, S.K., 1978. effects of feeding frequency on the growth of young estuary grouper, Epinephelus tauuina (Forsskal), cultured in floating cages. Aquaculture, 14: 3 l-47. Chua, T.E. and Teng, S.K., 1982. Effects of food ration on growth, condition factor, food conversion efficiency and net yield of estuary grouper, Epinephelus salmoides (Maxwell), cultured in floating net cages. Aquaculture, 27: 273-283. Chungyampin, S. and Boonyaratpalin, M., 1988. Effect of type of feeds and squid meal on growth of seabass fingerlings, National Institute of Coastal Aquaculture, Songkhla, Thailand, (unpublished data). Coloso, R.M., Tiro, L.B. and Benitez, L.V., 1983. A reference amino acid pattern for milkfish, Chanos chanos juveniles. Paper presented at 2nd International Milkfish Aquaculture Conference, 4-8 October 1983, Iloilo City, Philippines. Coloso, R.M., Benitez, L.V. and Tiro, L.B., 1988. The effect of dietary protein-energy levels on growth and metabolism of milkfish (Chanos chanos Forsskal). Comp. Biochem. Physiol., 89A: 11. Coloso, R.M., Tiro, L.B. and Benitez, L.V., 1992. Requirement for tryptophan by milkfish (Chinos chanos Forsskal) juveniles. Fish Physiol. Biochem., 10: 35-41.

310

M. Boonyaratpalin/Aquaculture

151 (1997) 283-313

Conrad, J., 1987. Rabbitfish and tilapia culture in Saudia Arabia. Aquaculture Magazine. November/December 1987. Cowey, C.B. and A.G.J. Tacon, 1981. Fish nutrition-relevance to invertebrates. Proceedings of 2nd International Conference on Aquaculture Nutrition. Biochemical Approaches to Shellfish Nutrition. 27-29 October 1981, University of Delaware, pp. 13-29. Crear, D., 1980. Observations of the reproductive state of milkfish populations Chanos chanos from hypersaline ponds on Christmas Island (Pacific Ocean). In: J.W. Avault Jr. (Editor), Proceedings of World Mariculture Society, Vol. 21. Louisiana State University, Baton Rouge, 548 pp. Cuzon, Cl., 1988. Preliminary nutritional studies of seabass Lates calcarifer (Bloch) protein and lipid requirements. 19th Annual Conference and Exposition, World Aquaculture Society, Hawaii ‘88 Program and Abstracts, 15 pp. Cuzon, G., Chou, R. and Fuchs, J., 1990. Nutrition of the seabass L&es calcarifer. In: Advances in Tropical Aquaculture. AQUACOP, IFREMER, Actes de Colloques No. 9, pp. 757-763. Dawes, B., 1930. The absorption of fats and lipoids in plaice. J. Mar. Biol. Ass. U.K., 17: 75-102. Duray, M., 1986. Biological evaluation of three phytoplankton species (Chlorella sp,, Tetraselmis sp., Isochrysis galbana) and two zooplankton species (Grassostrea iredali, Branchionua plicatilis) as food for first-feeding Siganus guttutus larvae. Philipp. Sci., 23: 41-49. Duray, M. and Bagarinao, T., 1984. Weaning of hatchery-bred milkfish larvae from live food to artificial diets. Aquaculture, 41: 325-332. El-Dakour, S. and George, K.A., 1982. Growth of hamoor (Epinephelus tauuina) fed on diferent protein: energy ratios. Kuwait Institute of Scientific Research Annual Research Report (1981). pp. 75-77. Emata, A.C., 1991. Milkfish, rabbitfish and mullet studies 1988-1991: a review. A Lecture Note on Aquaculture. Aquaculture Department, SEAFDEC, Tigbauan, Iloilo, Philippines, 15 pp. Ferraris, R.P., Catacutan, M.R., Mabelin, R.L. and Jazul, A.P., 1986. Digestibility in milkfish Chanos chanos (Forsskal): effects of protein source, fish size and salinity. Aquaculture, 59: 93. Fortes, R.D., 1984. Milkfish culture techniques generated and developed by the Brackish Water Aquaculture Center. In: J.V. Juario, R.P. Ferraris and L.V. Benitez (Editors), Advances in Milkfish Biology and Culture. Island Publishing House Inc., Metro, Manila, Philippines, pp. 107-199. Gorriceta, I.R., 1982. Studies on the digestive lipases and lipid composition of milkfish, Chanos chanos Forsskal. MS. Thesis, University of the Philippines System, 56 pp. Halver, J.E., 1957. Nutrition of salmonid fishes III. Water-soluble vitamin and mineral requirements of chinook salmon. J. Nutr., 62: 225-243. Hara, S., Duray, M.N., Parazo, M.M., and Taki, Y., 1986. Year-round spawning and seed production of the rabbitfish, Siganus guttatus. Aquaculture, 59: 259-272. Helland, S., Storebakken, T. and Grisdale-Helland, B., 1991. Atlantic salmon, Salmo salar. In: P. Wilson (Editor), Handbook of Nutrient Requirement of Finfish. CRC Press, London, pp. 13-22. Hickling, C.F., 1962. Fish Culture. Faber and Faber, London, 295 pp. Horstmann, U.. 1975. Some aspects of the mariculture of different siganid species in the Philippines. Philipp. Sci., 12: 5-20. Huang, T.L., 1981. An investigation report of deepwater milkfish culture. China Fish. Mon., 338: 12-15 (in Chinese). Ismael, W., Wahyuni, IS. and Panggabeam, T., 1986. Preliminary study on the combination of feed for siganids. Panelition Perikanan Laut., 10: l-5. Jauncey, K., Tacon, A.G.J. and Jackson, A.J., 1983. The quantitative essential amino acid requirements of Oreochromis (Sarotherodon mossambicus). In: L. Fishelson and Z. Yaron (Compilers), Proceedings of 1st International Symposium on Tilapia in Aquaculture, Nazareth, Israel. Tel Aviv University, Israel. Juario, J.V., Duray, M.N., Duray, V.M., Nacario J.F. and Almendras J.M.E., 1985. Breeding and larval rearing of the rabbitfish, Siganus guttarus (Blach). Aquaculture, 44: 91-101. Kanazawa, A., 1984. Feed formulation for penaeid shrimp, seabass, grouper and rabbitfish culture in malaysia. FAO, Malaysia Coastal Aquaculture Development Project, FI: DP/MAL/77/008, Field Document 2, pp. 61-78. Kawamura, G. and Castillo, A., Jr., 1981. A new device for recording the feeding activities of milkfish. Bull. Jpn. Sot. Sci. Fish., 47: 141.

M. Boonyaratpalin/Aquaculture

151 (1997) 283-313

311

Kawamura, G. and Hara, S., 1980. On the visual feeding of milkfish larvae and juveniles in captivity. Bull. Jpn. Sot. Sci. Fish., 46: 1297. Kumagai, S. and Bagarinao, T.U., 1981. Studies on the habitat and food of juvenile milkfish in the wild. Fish Res. J. Phil. 6(l): l-10. Lam, T.J., 1974. Siganids: their biology and mariculture potential. Aquaculture, 3: 325-354. Lee, D.L. and Liao, I.C., 1976. A preliminary study on the purified test diet for young milkfish Chanos chanos. Proceedings of international Milklish Workshop Conference, 19-22 May, Iloilo, Philippines, pp. 104-120. Liao, LC. and Chen, T.I., 1986. Milkfish culture methods in Southeast Asia. In: C.S. Lee, M.S. Gordon and W.O. Watanabe (Editors), Aquaculture of Milktish (Chanos chanos): State of the Art. The Oceanic Institute, Waimanalo, Hawaii, 209 pp. Lim, C., 1978. Effect of feeding rate on the survival and growth of milkfish (Chinos chinos) fry in a controlled environment. SEAFDEC Aquac. Dept. Q. Res. Rep., 2f4): 17. Lim, C., 1991, Milkfish, Chanos chanos. In: R.P. Wilson (Editor), Handbook of Nutrient Requirements of Fintish. CRC Press, London, pp. 97-104. Lim, C., Sukhawongs and Pascual, F.P. 1979. A preliminary study on the protein requirement of Chaws chanos (Forsskal) in a controlled environment. Aquaculture, 17: 195-201. Ling, S.W., 1977. Aquaculture in Southeast Asia-A Historical Overview. University of Washington Press, Seattle, 108 pp. Longly, W.H. and Hildebrand, S.F., 1941. Systematic catalogue of the fishes of Tortugas, Florida. Carnegie Inst. Washington Publ., 535: 1-331. Maneewongsa, S., Ruangpanit, N., Pechmanee, T and Tattanon, T., 1981. Propagation on seabass (I.&es cakar@r). Contribution No. 1. National Institute of Coastal Aquaculture, Department of Fisheries, 24 pp. (in Thai). Masuo, M., 1986. Technical Manual for Seed Production of Seabass. National Institute of Coastal Aquaculture, Department of Fisheries, 49 pp. May, R.C., Popper, D. and Mcvey, J.R. 1974. Rearing and larval development of Siganus canaliculatus (Park) (Pisces: Siganidae). Micronesica, 10: 285-298. Moon, H.Y. and Gatlin, D.M., 1991. Total sulfur amino acid requirement of juvenile red drum (S&mops ocellatus). Aquaculture, 95: 97-106. Moore, W.G., 1941. Studies on the habits of fishes. Ecol., 22: 91-96. Munro, I.S.R., 1967. Spine-feet, rabbittish (suborder Siganoidei; family Siganidae). In: The Fishes of New Guinea. Port Moresby, New Guinea Department of Agriculture, Stock and Fisheries, pp. 472-479. National Research Council, 1977. Nutrient Requirement of Warmwater Fishes. National Academy Press, Washington, DC, 78 pp. National Research Council, 1983. Nutrient Requirement of Warmwater Fishes and Shellfishes. National Academy Press, Washington, DC, 102 pp. New, M.B., 1987. Feed and Feeding of Fish and Shrimp: A Manual on the Preparation and Presentation of Compound Feeds for Shrimp and Fish in Aquaculture. United Nations Development Program, Food and Agriculture Organization of the United Nations, Rome, pp. 111. Otubusin, S.O. and Lim, C., 1985. The effect of duration of feeding on survival, growth and production of milktish, Chanos chanos (Forsskal) in brackishwater ponds in the Philippines. Aquaculture, 46: 287-292. Parazo, M.M., 1990. Effect of dietary protein and energy level on growth, protein utilization and carcass composition of rabbitfish, Siganus guttatus. Aquaculture, 86: 41-49. Parazo, M.M., 1991. An artificial diet for larval rabbitfish, S&anus guttatus Bloch. In: S. De Silva (Editor), Fish Nutrition Research in Asia. Proceedings of the Fourth Asian Fish Nutrition Workshop. Asian Fishery Society Special Publication 5. Asian Fisheries Society, Manila, Phillippines, pp. 43-48. Pascual, F.P., 1984. The energy-protein requirement of Chanos chanos fingerlings, Poster paper presented at the International Symposium on Feeding and Nutrition in Fish, lo- I3 July, University of Aberdeen. Pascual, F.P., Sumagaysay, N.S. and Borlongan, LG., 1991. Modular method of rearing milkfish with artificial feed. Proceedings of the 4th Asian Fish Nutrition Workshop, pp. 159-167. Piedad-Pascual, F., 1983. Biological evaluation of some practical diets developed for milkfish fingerlings. Poster paper presented during the Second International Milkfish Aquaculture Conference, Iliolo City, Philippines, 408 pp.

312

M. Boonyaratpalin/Aquaculture

151 (1997) 283-313

Pechmanee, T. and Watanabe, T., 1984. Effect of handling on survival in larval stage of seabass, L.utes calcarifer. Report of Thailand and Japan Coastal Aquaculture Research Project, April 1981-March 1984. Japan International Cooperation Agency, pp. 85-92. Phromkhuntong, W., Supamattaya, K. and Jittione, W., 1987. Effect of water soluble vitamins on growth, body composition and histology of seabass. Report of the Aquatic Science Division, Faculty of Natural Resources, Prince of Songkhla University, Thailand, 37 pp. Pimoljinda, T. and Boonyaratpalin, M., 1989. Study on the vitamin requirements of seabass L&es calcarifer Bloch in sea water. Technical Paper No. 3. Phuket Brackishwater Fisheries Station, Department of Fisheries, Thailand, 24 pp. (in Thai). Porn-ngam, N., Chonchuenchob, P. and Boonchum, U., 1989. Dietary mineral requirement in seabass. IDRC Fish Nutrition Project Annual Report. Department of Fisheries, Thailand, 3 pp. Randall, J.E., 1965. Food habits of reef fishes of the West Indies. Stud. Trop. Oceanog., 5: 665-847. Ruangpanit, N. and Kongkumnerd, J., 1992. Study on some potentially suitable factors to prevent and reduce the mass mortality of seabass (Lutes calcarifer). Technical Paper No. 8. National Institute of Coastal Aquaculture, Songkla, Thailand, 12 pp. (in Thai). Sakaras, W., 1990. Experiment on seabass, Z&es calcarifer (Bloch), cultured in cages with dry pellet. Technical Paper No. 5. Rayong Brackishwater Fisheries Station, Thailand, 15 pp. (in Thai). Sakaras, W., Boonyaratpalin, M., Unprasert, N. and Kumpang, P., 1988. Optimum dietary protein energy ratio in seabass feed I. Technical Paper No. 7. Rayong Brackishwater Fisheries Station, Thailand, 20 pp. (in Thai). Sakaras, W., Boonyaratpalin, M. and Unprasert, N., 1989. Optimum dietary protein energy ratio in seabass feed II. Technical Paper No. 8. Rayong Brackish Water Fisheries Station, Thailand, 22 pp. (in Thai). Sampson, E., 1984. The milkfish industry in the Philippines. In: J.V. Juario, R.P. Ferraris and L.V. Benitez (Editors), Advances in Milk&h Biology and Culture. Island Publishing House, Manila, 215 pp. Samsi, S., 1979. Effects of various protein sources on the growth and survival rates of milkfish (Chanos charm Forsskal) fingerlings in a controlled environment. MS. Thesis, University of the Philippines, the Visayas, 42 pp. Santiago, C.B., 1985. Amino acid requirements of Nile tilapia. Ph.D. Dissertation. Auburn University, Alabama, 141 pp. Santiago, C.B., Aldaba, M.B. and Songalia, E.T. 1983. Effect of artificial diets on growth and survival of milkfish fry in freshwater. Aquaculture, 34: 247-252. Santiago, C.B., Pantastico, J.B., Baldia, S.F. and Reyes, OS., 1989. Feeding for milkfish fingerling production in freshwater ponds. Asian Aquac., 11: 1. Sastrillo, M.A.S. and Chiu-Chem, Y.N., 1992. Methionine requirement of milkfish (Chanos chanos Forsskal) juvenile. Asian Fisheries Society, Abstracts: Third Asian Fisheries Forum, p. 96. Schuster, W.H., 1952. Fish culture in brackishwater ponds in Java. Special Publication. Indo-Pacific Fish Council, Vol. 1, 140 pp. Schuster, W.H., 1960. Synopsis of biological data on milkfish Chanos chanos (Forsskal), 1775. FAO Fisheries Biology Synopsis No. 4. Fisheries Division, Biology Branch, FAO, Rome, 60 pp. SEAFDEC, 1992. Fisheries Statistical Bulletin for South China Seas and Asia. Southeast Asian Fisheries Development Center, Bangkok, Thailand. Shiau, S.Y., Pan, B.S., Chen, S. Yu, H.L and Lin, S.L., 1988. Successful use of soybean meal with a methionine supplement to replace fish meal in diets fed to milkfish Chanos chanos Forsskal. J. World Aquac. Sot., 19: 14-19. Soh, C.L. and Lam, T.J., 1973. Induced breeding and early development of the rabbitfish Siganus oramin. Malaysia National Journal, pp. 49-56. Soletchnik, P., 1984. Aspects of nutrition and reproduction in Si,ganus guttatus with emphasis on application to aquaculture. SEAFDEC Aquaculture Department, Iloilo, 75 pp. Sorgeloos, P., Leger P. and Lavens, P., 1988. Improved larval rearing of European and Asian seabass, seabream, mahi-mahi, siganid and milkfish using enrichment diets for Branchionus and Artemia. World Aquac., 19: 78-79. Suyehiro, Y., 1942. A study on the digestive system and feeding habits of fish. Jpn J. Zool., 10: 301-303. Sukhawongs, S., Tanakumchup, N. and Chungyampin, S., 1978. Feeding experiment on artificial diet for

M. Boonyaratpalin/Aquaculture

I51 (1997) 283-313

313

grouper, Epinephelus tauuina in nylon cages. Annual Report of Songkhla Fishery Station Department of Fisheries, pp. 103-l 17. Tacon, A.G.J. and Rausin, N., 1989. Seabass cage culture trial. The food and feeding of seabass Lutes calcarifer, grouper Epinephelus taurina and rabbitfish Siganus canaliculatus in floating netcages. INS/81/008 Technical Paper 13. The National Seafarming Development Center, Lampung, Indonesia, 34 greasy

PP. Tacon, A.G.J., Rausin, N., Kadari, M. and Cornelis, P., 1990. The food and feeding of marine finfish in floating net cages at the National Seafarming Development Centre, Lampung, Indonesia: rabbitfish, S&anus canalicultus (Park). Aquac. Fish. Manage., 21: 375-390. Tacon, A.G.J., Rausin, N., Kadari, M. and Cornelis, P., 1991. The food and feeding of tropical marine fishes in floating net cages: Asian seabass, Lm-es calcarifer (Bloch) and brown-spotted grouper, Epinephelus tauuina (Forsskal). Aquac. Fish. Man. Taiwan Fisheries Bureau, 1983. Fisheries Year Book, Taiwan Area, 1982. Taiwan Fisheries Bureau, Department of Agriculture and Forestry, Provincial Government of Taiwan, Tampi, P.R.S., 1958. On the food of Chanos chanos (Forsskal). Indian J. Fish., 5: 107-l 17. Teng, S.K., 1979. Studies on the culture of the estuary grouper, Epinephelus salmoides, Maxwell (Pisces: Serranidae) in floating net cages. In: M. Divina, V. Zamora et al. (Compilers), Grouper Abstracts, 1987. Brackish Water Aquaculture Information System, SEAFDEC, Philippines, p, 61. Teng, S.K., Chua, T.E. and Lim, P.E., 1977. Preliminary observation on the dietary protein requirement of estuary grouper, Epinephelus tauuina (Forsskal) cultured in floating net cages. In: M. Divina, V. Zamora et al. (Compilers), Grouper Abstracts, 1987. Brackish Water Aquaculture Information System, SEAFDEC, Philippines, p. 60. Teng, S.K., Chua, T.E. and Lim, P.E., 1978. Preliminary observation on the dietary protein requirement of estuary grouper, Epinephelus salmoides, culture in floating net-cages. Aquaculture, 15: 257-272. Teshima, S., Kanazawa, A. and Kawamura, G., 1984. Effects of several factors on growth of milkfish (Chanos chanos Forsskal) fingerlings reared with artificial diets in aquaria. Aquaculture, 37: 39-50. Tseng, W.Y. and Ho, S.K., 1988. Grouper Culture, A Practical Manual. Chien Cheng Publisher, Kaohsiung, People’s Republic of China, 134 pp. Tucker, J.W. Jr., 1991, Marine fish nutrition. In: G.L. Allan and W. Dal1 (Editors), Proceedings of Aquaculture Nutrition Workshop, Salamander Bay, 15-17 April 1991. NSW Fisheries, Brackish Water Fish Culture Research Station, Salamander Bay, Australia. Tucker, J.W., Jr., Mackinnon, M.R., Russell, D.J., O’Brien, J.J. and Cazzola, E., 1988. Growth of juvenile barramundi (kites calcarifer) on dry feeds. Prog. Fish Culturist, 50: 81-85. Villegas, C.T., Millamena, O.M. and Escritor, F., 1983. Growth, survival and fatty acid composition of Charm chanos fry fed Brachionus plicatilis reared on three selected algal diets. Paper presented at the 2nd International Milktish Aquaculture Conference, 4-8 October 1983, Iloilo City, Philippines. Von Westemhagen, H., 1974. Food preferences in cultured rabbitfish (Siganidae). Aquaculture 3: 109-l 17. Wanakowat, J., Boonyaratpalin, M., Pimoljinda, T. and Assavaaree, M., 1989. Vitamin B6 requirement of juvenile seabass Lutescalcarifer. In: M. Takeda and T. Watanabe (Editors), The Current Status of Fish Nutrition in Aquaculture. Tokyo University of Fisheries, Tokyo, Japan, pp. 141-147. Watanabe, T., Kitajima, C., and Fujita, C., 1983. Nutritional values of live organisms used in Japan for mass propagation of fish: a review. Aquaculture, 34: 115-143. Wilson, R., 1991. Channel catfish, Ictalurus punctutus In: P. Wilson (Editors). Handbook of Nutrient Requirement of Finfish. CRC Press, London, 196 pp. Wong, F.J. and Chou, R., 1989. Dietary protein requirements of early grow-out seabass (Lates calcarifer Bloch) and some observations on the performance of two practical formulated feeds, Singapore J. Primary Ind., 17: 134 pp. Wongsomnuk, S., Pamichsuka, P. and Danayadol, Y., 1978. Experiment on nursing of grouper, Epinephelus tauuina (Forsskal) with various mixed feeds. Annual Report of Songkhla Fishery Station Department of Fisheries, pp. 97-102.