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Home , Humpback grouper, Marbled grouper, Serranidae, Tiger grouper

Introduction

Groupers are territorial predatory reef that are widely distributed throughout the tropical and subtropical seas of the world, and notably, those of the Indo-Pacific region. A very diverse group of fish comprising more than 90 in five main genera of the family , they are highly prized in the live reef fish markets of Hong Kong and Singapore where they fetch from US$10-12/kg for orange-spot coioides, US$40-50/kg for coral trout spp to more than US$80/kg for Cromileptes altivelis (Sim, 2005). Targeting of spawning aggregations and destructive fishing practices such as the use of cyanide and explosives have resulted in these fish being severely depleted in the wild.

A major impediment to production of has been the limited supply of fry. While a significant industry has been established in South East Asia based on wild- capture fry, only the lower value estuarine species such as orange-spot grouper and Epinephelus malabaricus are caught in any significant numbers. Fry of the higher value, -dwelling species such as coral trout and humpback grouper are seldom caught other than as incidental catches by those targeting the aquarium trade. Until recently, commercial hatchery-production of grouper fry has been very Market-size coral trout, Plectropomus leopardus, difficult with survival rates to metamorphosis typically less Photo credit: SY Sim, NACA than 5%. Advances in grouper hatchery technology (Rimmer et al., 2004; Sim et al., 2005a) are now overcoming this Trash fish still the preferred feed for groupers bottleneck. Fry of many grouper species, including orange- spot, (Epinephelus fuscoguttatus) and humpback grouper, Throughout the Asia-Pacific region, the traditional are becoming more readily available for aquaculture grow-out. and still preferred method of culturing groupers, is to feed them on low-value fresh fish ('trash fish'). Trash fish that is fresh, properly prepared and carefully managed can be a very good, and often inexpensive, source of food for carnivorous marine fish such as groupers. Sadly, this is often not the case and even in well managed systems, the feeding of trash fish can have negative financial, environmental and social impacts 'triple bottom line' consequences. There are three main concerns: depletion of fish stocks and the resultant increased competition between man and aquaculture for a dwindling (and more expensive) supply of wild fish, adverse environmental impacts associated with the feeding of trash fish and spread of diseases to wild and cultured fish.

The demand for low-value fish in the region has steadily increased with continued expansion of mariculture. Satisfying this demand has caused a severe problem of over- fishing, not only of the traditionally-fished stocks, but also of Market-size orange spotted grouper, Epinephelus coioides those fish and invertebrates closer to the bottom of marine food Photo credit: SY Sim, NACA chains. Many stocks in SE Asia are reported to be

20 Aqua Feeds: Formulation & Beyond, Volume 2 Issue 2 2005 10 to 30% below the levels of three decades ago (Williams, 2002). The feeding of trash fish itself is a significant source of pollution. Feed losses associated with feeding trash fish to carnivorous fish are four times greater than feeding pelleted feeds. However, this may be an underestimate. New (1996) cites a 1991 study in Hong Kong where 45,000 t of trash fish were needed to produce just 3,000 t of high-value food fish in marine cages i.e., a FCR of 15:1. Where trash fish is carefully fed, as for example under experimental conditions, FCRs for cage-cultured groupers can be as good as 3.5:1 on a wet basis. However, under practical farming conditions, FCRs are more typically 6:1 and up to 17:1 (Tacon et al., 1991). An often ignored consequence of feeding trash fish is the likelihood of it being a direct or indirect source of introduced disease. Of particular concern are viral diseases such as viral nervous necrosis (VNN), bacterial infections, particularly by Vibrio and Streptococci, and parasites. While the main mode of VNN transmission is vertical from the egg, horizontal transmission from other infected fish, including trash fish, is also a real threat. Too often, the nutritional inadequacy of the trash fish, Fingerlings of humpback grouper, Cromileptes altivelis especially where spoilage occurs prior to it being fed, is a real, Photo credit: SY Sim, NACA but generally unrecognized problem that results in slow growth, poor FCRs and lower survival. flow to ensure fish have well oxygenated water. Fingerlings of 25-75 mm (14 g/fish) are stocked at 100-150 fish/m2 and cannibalism reduced by grading the fish every one to two weeks until they are 125-150 mm (30-80 g/fish). At this size, the fish are transferred from nursery cages into production cages where stocking density is typically 50-60 fish/m2 initially, reducing to about 10-20 fish/m2 for fish of 500+ g. Another, but less common, culture system is to use brackish water ponds, often reclaimed shrimp ponds of any size up to about 0.5 ha. This culture system is suitable for estuary species such as orange-spot or marbled groupers but has not proved very successful for true marine groupers such as tiger or humpback. For brackish water pond culture, newly introduced fingerlings are restricted to a small netted enclosure of the pond for several weeks while being trained to the feeding method. The fish are then let out of the enclosure to free-range in the pond. Groupers are fed to apparent satiation during the day with feeding frequency decreasing as the size of the fish increases. Farmers check cages and ponds daily to remove uneaten food and to adjust feeding rate so as to minimize food wastage. Broodstock of humpback grouper, Cromileptes altivelis Guidelines for the amount and frequency of feeding trash fish Photo credit: SY Sim, NACA or compounded (pelleted or extruded) dry feeds are given in Table 1. The preferred harvest size of farmed groupers is 600 g Farming practices to 1.2 kg, depending on the market. Under farm conditions, orange-spot and will reach weights of 600 g in Groupers are most commonly farmed using knotless nylon or about 6-8 months and 1-1.2 kg in about 12 months after being polyethylene net sea cages, typically as a raft of floating cages, stocked as 100 mm fingerlings. Survival rates after 100 mm each of 2 to 5 m sides and 2-3 m deep. Where possible, cages are size are typically 85% or better. situated in channels where there is deep water and good tidal Table 1: Guidelines1 for feeding trash fish or compounded (pelleted) dry feeds to Epinephelus species of groupers

Daily feeding rate (% of average body weight) Fish size (g) Number of feeds/day Trash fish Dry feed

1-5 20 20 10 4 3-5 5-25 20 15 4 2 2-3 25-100 15 10 2 1.5 2 100-200 10 8 1.5 1.2 1-2 > 200 6 4 1 0.8 1

1 The amount of food to be given and the frequency of feeding must be carefully monitored and adjusted for each farm situation,. The feeding schedule in the table should only be used as a guide. For slow growing species such as humpback grouper (C. altivelis), the amount to feed should be reduced by about a half.

Aqua Feeds: Formulation & Beyond, Volume 2 Issue 2 2005 21 Preparation of trash fish for feeding to groupers Farm-made pellet feeds for groupers Photo credit: SY Sim, NACA Photo credit: SY Sim, NACA

Table 2: The dry matter, crude protein and energy apparent digestibility coefficients (mean ± SD) determined with groupers for selected ingredients available in SE Asia

Digestibility (%)1 Feed ingredient Dry Matter Crude Protein Energy

Marine product Acetes shrimp meal (72% CP) 76.0 ±4.00 95.0 ±0.72 Fish meal (Chilean, 65% CP) 83.6 ±3.09 98.0 ±0.07 Fish meal (local, 45% CP) 59.1 ±1.23 82.4 ±1.99 77.2 ± 1.91

Fish meal (sardine, 65% CP) 87.2 ±2.53 85.2 ± 0.90 92.5 ±1.40 Fish meal (tuna, 50% CP) 75.4 ±3.61 76.2 ±1.92 Fish meal (white, 69% CP) 89.2 ±1.69 98.6 ±0.31 Shrimp head meal (50% CP) 58.5 ±3.33 78.0 ±1.32 63.6 ±0.89 Squid meal (71% CP) 99.4 ±0.95 94.2 ±0.21 Terrestrial product Blood meal (ring-dried, 84% CP) 36.9 ± 0.98 15.5 ± 2.01 Blood meal (oven-dried, 84% CP) 48.1 ± 0.85 55.2 ± 1.35 Blood meal (formic, 87% CP)2 67.9 ± 1.63 87.5 ± 0.55 Blood meal (propionic, 84% CP)2 61.7 ± 2.60 84.2 ± 0.69 Meat meal (Australian, 44% CP) 60.8 ± 0.80 98.9 ± 1.32 Meat meal (Philippine, 45% CP) 77.7 ± 0.09 83.8 ± 1.66 Meat solubles (Danish, 73% CP) 99.3 ± 0.45 97.6 ± 0.08 Poultry feather meal (67% CP) 74.3 ± 3.06 81.8 ± 2.58 Terrestrial plant product Corn meal (8% CP) 85.2 ± 2.81 82.9 ± 4.71 Corn gluten meal (56% CP) 94.0 ± 2.03 99.5 ± 0.65 Cowpea meal (white, 24% CP) 74.2 ± 3.14 93.5 ± 1.22 Lucaena (ipil-ipil) meal (19% CP) 56.0 ± 0.04 78.8 ± 2.64 Lupin albus meal (26% CP) 54.1 ± 1.24 97.5 ± 3.65 Palm oil cake meal (11% CP) 45.3 ± 2.37 80.5 ± 1.30 40.4 ± 3.74 Rice bran (11% CP) 22.2 ± 1.52 59.5 ± 1.41 44.3 ± 0.97 Rice bran (14% CP) 68.5 ± 7.02 42.7 ± 5.38 Soybean meal (full-fat, 41% CP) 54.8 ± 2.72 67.2 ± 1.29 51.1 ± 0.89 Soybean meal (solvent-extracted, 75.7 ± 1.98 96.0 ± 0.13 50-54% CP) Wheat flour (9% CP) 72.8 ± 0.85 82.9 ± 1.26 1Mean ± SD. 2Oven-dried blood meal fermented using either formic or propionic acids.

Collaborative grouper feeds research effective, manufactured feeds as an alternative to trash fish. Following several workshops in SE Asia during the mid 1990's, Aquaculture production of grouper from China and an Australian Centre for International Agricultural Research SE Asian countries was only 3000 to 5000 tonnes per annum (ACIAR) project was established to unite the efforts of grouper throughout most of the 1990's. As market demand for live aquaculture researchers in the region in order to accelerate the grouper increased and hatchery-reared fry became more development of grouper farming. Specific aims of the project available, grouper production rapidly expanded in the region were to: (i) improve the growth and survival of grouper larvae and now exceeds 52,000 tonnes (FAO, 2005). Continued during the hatchery phase; (ii) develop grow-out feeds that expansion of grouper and other marine fish aquaculture in the have low environmental impact; and (iii) support NACA's region will place even more pressure on the diminishing supply establishment of an Asia-Pacific Grouper Aquaculture of trash fish and the only long-term solution is to use cost- Network. The grouper network has since been expanded into an

22 Aqua Feeds: Formulation & Beyond, Volume 2 Issue 2 2005 grouper, but this did not greatly alter the dietary nutritional specifications needed to maximize the growth rate of the species.

Feed ingredient digestibility

A prerequisite in formulating nutritionally sound feeds is to know how well each ingredient is digested by the target animal. Standard digestibility procedures were used in the ACIAR project to determine the digestibility of locally- available feed ingredients. Chromic oxide and ytterbium were used as digestibility markers and the digestibility of individual feed ingredients was calculated using substitution procedures: test ingredients were incorporated into the reference diet at substitution rates of either 40% or 30% for animal or plant meals, respectively. Ingredient digestibility data are presented in Table 2. The protein digestibility of marine and terrestrial animal meals was high (above 76%) except for blood meal, Commercial, extruded feeds for grouper culture although ensiling the product with organic acids (Box 1) Photo credit: SY Sim, NACA substantially improved its digestibility. The protein digestibility of terrestrial plant meals was more variable, being poor for rice bran (43-60%) but good for lupin and corn gluten Asia-Pacific Marine Finfish Aquaculture Network meal (almost 100%). (http://www.enaca.org/marinefish). Results of the ACIAR project work have been reported by Rimmer and colleagues Nutrient requirements (Rimmer et al., 2004; Sim et al., 2005a, b). As a result of the ACIAR and other research, we now Eco-friendly grow-out feed for groupers have a good idea about the nutritional requirements of juvenile groupers and the dietary specifications that must be provided if The goal of the feeds component of the ACIAR the fish is to use the feed efficiently and grow well. Being grouper project was to develop compounded grow-out feeds as carnivores, groupers have a natural propensity to use dietary a more-sustainable, lower-polluting and cost-effective protein as the preferred source of metabolic energy. Lipids are alternative to the feeding of trash fish. This was addressed in a efficiently digested, but increasing the dietary lipid content structured way, quantifying information on the nutritive value above 10-15% does not improve growth rate, nor does it enable of available feed ingredients, characterizing the requirements much, if any, of the dietary protein to be spared from being of groupers for key nutrients and demonstrating the cost- oxidized for energy. The higher lipid levels rather depress effectiveness of the compounded feeds. Partners in the appetite and result in fatty fish. Adding dietary lipid in the form collaborative research were 's CSIRO Marine of coconut oil as a rich source of medium chain fatty acids Research, Indonesia's Gondol Research Institute for (chain length of 10 to 14 carbon atoms) accelerated the Mariculture and Maros Research Institute for Coastal oxidation of the absorbed lipid and resulted in severely Aquaculture, and the SEAFDEC laboratory at Iloilo, the depressed appetite and profoundly reduced fish growth (Smith Philippines. The research targeted three grouper species: E. et al., 2005; I.H. Williams et al., unpublished data). Thus, coioides (orange-spot grouper), E. fuscoguttatus (tiger groupers require diets that are high in digestible protein (around grouper) and C. altivelis (humpback grouper). While some 44%, equivalent to about 50-52% crude protein), moderately nutritional differences were observed between the three low in lipid (10-15% total lipid) and which contain no more species, these were comparatively minor. This allows than about 20% of cereal (wheat, rice etc). Recommended nutritional recommendations to be generalized for groupers as dietary specifications for optimal growth of juvenile groupers a whole. However, it should be noted that humpback grouper is are shown in Table 3. a slow growing species compared to tiger or orange-spot Table 3: Recommended nutritional specifications of pelleted feeds for optimal growth of juvenile grouper

Nutrient/energy Specification Comment (as fed)

Moisture (%) < 10 Pellets dry and without mold; few fines in bag; slowly sinking Ash (%) < 13 Crude protein (%) > 50 Should be from high quality protein ingredients Digestible protein (%) > 44 Crude fiber (%) < 3 Total lipid (%) 9 - <15 9-10% is optimal. Higher amounts will produce fatty fish. Above 15% will depress appetite and growth EPA + DHA (%) > 1.5 Vitamin C (mg/kg) > 100 As heat-stable ascorbyl product. Increase to 150 mg/kg for stressful conditions Gross energy (kJ/g)* < 20 Digestible energy (kJ/g) < 16 Protein : energy (g:kJ) > 27 As digestible protein digestible energy * 1 kJ = 0.24 k cal

Aqua Feeds: Formulation & Beyond, Volume 2 Issue 2 2005 23 Fish meal replacement Acknowledgements

The high digestibility of many terrestrial plant and Much of the data reported in this article were animal feed ingredients indicated that they could be used as produced by collaborators in the ACIAR Grouper project partial fish meal replacements in grouper feeds. This has been FIS/97/93 under the direction of Dr Mike Rimmer of the confirmed with laboratory and on-farm experiments. A 4:1 Queensland Department of Primary Industries and Fisheries. combination of meat meal and ring-dried blood meal could In particular I would like to acknowledge Dr Oseni Millamena replace at least 60% of the fish meal protein in the diet of and Perla Eusebio of SEAFDEC, Dr Nyoman Giri and Ketut orange-spot grouper without adversely affecting survival, Suwirya of Gondol, Asda Laining of Maros, Dr Ian Williams of growth or FCR (Millamena, 2002) (Fig 1). Other less University of and David Smith of CSIRO. digestible protein meals such as cowpea, lucaena, soybean Also acknowledged is the coordination role of the Network of meal and shrimp head meal were less useful as fish meal Aquaculture Centres in Asia-Pacific, and in particular the help replacements. of Sih-Yang Sim, in extending the results of this research and

3.5 1.4 providing the photos that have been used in this article. Also, my thanks to all researchers who have contributed to our knowledge on feed development for groupers. 3.0 1.2

) References

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g a FAO, 2005. Fishstat Plus.

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M http://www.fao.org/fi/statist/FISOFT/FISHPLUS.asp#General %

D (

Millamena, O.M., 2002. Replacement of fish meal by animal by-

2.0 0.8 g

( R

product meals in a practical diet for grow-out culture of grouper G

R Epinephelus coioides. Aquaculture 204, 75-84. S

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SGR F New, M.B., 1996. Responsible use of aquaculture feeds. Aquaculture 1.5 FCR 0.6 Asia, 1: 3-15. Rimmer, M.A., McBride, S., Williams, K.C., 2004. In: Advances in Grouper Aquaculture. ACIAR monograph 110, Australian Centre 1.0 0.4 for International Agricultural Research, Canberra, Australia. 137 0 10 20 30 40 60 80 100 TF pp. Fish meal protein replacement (%) Sim, S-Y., 2005. Weekly wholesale marine fish prices in Hong Kong. Marine Finfish Aquaculture Network, Network of Aquaculture Fig.1: Comparison of specific growth rate (SGR) and feed conversion Centres in Asia-Pacific, Bangkok, Thailand. ratio (FCR) responses of juvenile orange-spot grouper (E. coioides) fed for 60 days on trash fish (TF) or pelleted feeds in which fish meal http://www.enaca.org/modules/news/index.php?storytopic=14 protein was serially replaced by a 4:1 mixture of meat meal and blood Sim, S-Y., Rimmer, M.A., Toledo, J.D., Sugama, S., Rumengan, I., meal. Data of Millamena (2002). Williams, K.C., Phillips, M.J., 2005a. In: A Guide to Small-scale Marine Finfish Hatchery Technology. NACA Pub. 2005-01, Network of Aquaculture Centres in Asia-Pacific, Bangkok, Thailand. 17 pp. Conclusions Sim, S-Y., Rimmer, M.A., Williams, K.C., Toledo, J.D., Sugama, S., Rumengan, I., Phillips, M.J., 2005b. In: A Practical Guide to Feeds Feeds formulated to meet the fish's requirements of and Feed Management for Cultured Groupers. NACA Pub. 2005- digestible nutrients and not containing excessive amounts of 02, Network of Aquaculture Centres in Asia-Pacific, Bangkok, plant protein meals will enable groupers to grow as well as Thailand. 18 pp. those fed trash fish. Groupers will readily accept compounded Smith, D.M., Williams, I.H., Williams, K.C., Barclay, M.C., dry feeds especially if they are fed these feeds from an early Venables, W.N., 2005. Oxidation of medium-chain and long-chain age, ideally from the late larval development stage. However, fatty acids by polka dot grouper Cromileptes altivelis. Aquacult. Nutr. 11, 41-48. fingerlings taken from the wild or reared on trash fish can be Tacon, A.G.J., Rausin, N., Kadari, M., Cornelis, P., 1991. The food trained to accept dry compounded feed. Switching to and fro and feeding of tropical marine in floating net cages: Asian between feeding trash fish and dry feed is discouraged as the seabass, Lates calcarifer (Bloch) and brown-spotted grouper, training period may cause fish to lose some condition. Further Epinephelus tauvina (Forskal). Aquacult. Fish. Man. 22, 165-182. work is needed to see if the nutritional requirements Williams, M.J., 2002. Asian fisheries in the 21st century: Which way determined for fingerling groupers need to be adjusted as fish to prosperity? (Keynote address to the 6th Asian Fisheries Forum, grow and approach market size of 500-600 g and above. K a o h s i u n g , Ta i w a n N o v e m b e r 2 5 - 2 9 2 0 0 1 ) http://www.compass.com.ph/~afs/mjwkeynote.html

Dr Kevin Williams is a veterinary graduate of U. Queensland and has a PhD from U. Melbourne for amino acid studies in pigs. Much of his 38-year professional career has involved nutritional research, initially with pigs and poultry, and more recently with aquaculture. Since 1992, he has applied the nutritional skills honed in the intensive pig and poultry industries to the aquaculture industry, joining CSIRO's Division of Marine Research in 1995 to lead the aquaculture nutrition group. His current research interests are in the development of feeds for marine finfish, spiny lobsters and tiger shrimp. He has authored more than 100 scientific papers, about half of these relating to aquaculture.

24 Aqua Feeds: Formulation & Beyond, Volume 2 Issue 2 2005