alternative dietary protein sources for farmed tilapia, oreochromis spp

Ž .Aquaculture 179 1999 149–168

Alternative dietary protein sources for farmedtilapia, Oreochromis spp.

Abdel-Fattah M. El-Sayed )

Oceanography Department, Faculty of Science, UniÕersity of Alexandria, Alexandria, Egypt

Abstract

Tilapia are widely cultured in the tropical and subtropical regions of the world and constitutethe third largest group of farmed finfish, only after carps and salmonids, with an annual growthrate of about 11.5%. Global production of farmed tilapia has increased more than three-fold since1984, from 186,544 m.t. to 659,000 m.t., representing about 4.48% of total farmed finfish in 1995,with a value of US$925 million. Feeding represents over 50% of the operational costs of

Ž .aquaculture. The shortage in world production of fish meal the main conventional protein source ,coupled with increased demand for fish meal in feeds for livestock and poultry is likely to reducethe dependence on fish meal as a single protein source in aquafeeds. Therefore, fish nutritionistshave made several attempts to partially or totally replace fish meal with less expensive, locallyavailable protein sources. The present review presents alternative dietary protein sources fortilapia, with emphasis on fishery by-products, terrestrial animal by-products, oilseed plants,aquatic plants, single cell proteins, grain legumes, plant protein concentrates and cereal by-prod-ucts. The nutritive values, inclusion levels, constraints and economic evaluation of these sourcesare discussed. q 1999 Elsevier Science B.V. All rights reserved.

Keywords: Tilapia; Aquaculture; Nutrition; Feed; Protein sources

1. Introduction

Tilapia culture has been practiced since the beginning of human history. For example,Žancient Egyptians raised tilapia for human consumption about 2000–2500 BC Chimits,

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( )A.-F.M. El-SayedrAquaculture 179 1999 149–168150

.1957; Bardach et al., 1972 . Currently, tilapia culture is widely practiced in manytropical and subtropical regions of the world. More than 22 tilapia species are being

Ž .cultured worldwide. However, Nile tilapia Oreochromis niloticus , Mozambique tilapiaŽ . Ž .O. mossambicus , blue tilapia O. aureus , O. macrochir, O. hornorum, O. galilaeus,Tilapia zillii and T. rendalli are the most commercially cultured tilapia species.

Tilapia are the third largest group of farmed finfish species, only after carpsŽ 6 . Ž 6 Ž .10.37=10 m.t. and salmonids 0.94=10 m.t. FAO, 1997 , with an average annualgrowth rate of about 11.5%. In addition, Nile tilapia was the 6th most cultured finfishspecies in the world in 1995 with a total production of 473,641 m.t. and an averagecompound growth rate of about 12% per annum since 1986. The global production offarmed tilapia has increased more than three-fold since 1984, from 186,544 m.t. to659,000 m.t., representing 4.48% of total farmed finfish in 1995, with a value of

Ž . Ž .US$925 million Tacon, 1997 Fig. 1 . About 650,000 m.t. or 98.6% of farmed tilapiaŽ .were produced in developing countries in 1995 Fig. 2 with Asia alone producing about

Ž .84% of this amount FAO, 1997 .Fish feeding represents over 50% of operating costs in intensive aquaculture, with

protein being the most expensive dietary source. The development of commercialŽ .aquafeeds has been traditionally based on fish meal FM as the main protein source due

Ž .to its high protein content and balanced essential amino acid EAA profile. FM is alsoŽ .an excellent source of essential fatty acids EFA , digestible energy, minerals and

vitamins. Therefore, it is no surprise that FM is the most expensive protein source inŽ .animal and aquaculture feeds Tacon, 1993 . The shortage in global FM production

coupled with increased demand and competition for its use in livestock and poultryfeeds has further increased FM prices. It is evident, on the long-run, that manydeveloping countries will be unable to depend on FM as a major protein source inaquafeeds. Therefore, several attempts have been made to partially or totally replace FMwith less expensive, locally available protein sources.

Ž .Fig. 1. World production of farmed tilapia during 1986–1995. Source: FAO 1997 .

( )A.-F.M. El-SayedrAquaculture 179 1999 149–168 151

Ž . Ž .Fig. 2. Tilapia production 1000 m.t. and percentage by country in 1995. Source: FAO 1997 .

Ž .El-Sayed and Tacon 1997 shed some light on fish-meal replacers in tilapia feeds.The present review presents further information on alternatives to fish meal, whichinclude fishery by-products, terrestrial animal by-products, oilseed plants, aquatic plants,single cell proteins, grain legumes, plant protein concentrates and cereal by-products.The nutritive values, quality, inclusion levels, constraints, and economic feasibility ofthese sources are discussed. The tested and recommended inclusion levels are summa-rized in Appendix A.

2. Animal protein sources

2.1. Fishery by-products

With the exception of fish silage, little attention has been given to the commercialŽpotential of fishery by-products including fish protein concentrate and hydrolysates,

Ž . .shrimp meal SM , krill meal and squid meal as partial or total protein sources forŽ .tilapia. Toledo et al. 1987 reported that shrimp head meal was incorporated into blue

tilapia diets up to 15% level with no adverse effects on fish performance. MansourŽ . Ž . Ž .1998 and El-Sayed 1998 found that shrimp meal 50% CP can be used as a total FM

Ž .alternative for fingerling red tilapia O. niloticus=O. hornorum and Nile tilapia,respectively, without significant loss in weight gain and feed efficiency.

Several studies conducted on the use of fish silage as a FM replacer in tilapia feedsŽ .showed varying, but promising, results. For example, Lapie and Bigueras-Benitez 1992

Ž .found that the growth of Nile tilapia fed formic acid preserved fish silage FFS blendedwith FM at 1:1 ratio was similar to that of fish fed a FM-based diet. When FFS:FM ratio


was increased to 3:1, growth performance was significantly reduced, presumably due toacidity of the diet and high proportion of free amino acids in fish silage. It has beensuggested that acidity reduces diet acceptance and affects protease activity in fish gutsŽ . ŽHardy et al., 1983 , while free amino acids may depress fish appetite Wilson et al.,

. Ž .1984 . Similarly, Fagbenro 1994 fed Nile tilapia a 30% CP FM-based diet and dietsŽ . Ž .containing blended lactic acid fermented fish silage LFS 1:1, wrw with soybean

Ž . Ž . Ž .meal SBM , poultry by-product meal PBM , hydrolyzed feather meal HFM or meatŽ .and bone meal MBM in a recirculated tank system for 10 weeks. No significant

differences in growth, digestibility, hemoglobin and hematocrit contents were found.Ž .Furthermore, Fagbenro et al. 1994 found that up to 75% of FM protein was

Ž .successfully replaced by dried, blended LFS:soybean meal 1:1 incorporated in diets fedto all male Nile tilapia fingerlings.

Ž .Fagbenro and Jauncey 1993 found that LFS could be stored at 308C for 6 monthswith little change in the quality and nitrogen loss. They also found that protein autolysisin LFS was directly related to prevailing temperature. In addition, LFS had very good

Žwater stability and low nitrogen loss regardless of the binder used Fagbenro and.Jauncey, 1995 . Apparent dry matter, protein and lipid digestibilities determined in O.

Žmossambicus and Nile tilapia fed LFS-based diets were also excellent Hossain et al.,.1992; Fagbenro and Jauncey, 1994, 1995, respectively . It is evident, therefore, that fish

silage has a good potential as a protein source for tilapia.

2.2. Terrestrial animal by-products

ŽThe terrestrial animal by-products poultry by-product meal PBM, blood meal BM,.hydrolyzed feather meal HFM and meat and bone meal MBM have high protein

Ž .contents and good EAA profiles Tacon, 1993 . However, they may be deficient in oneŽor more of the EAA. The most limiting EAA in these by-products are lysine Lys; PBM,

. Ž . Ž . ŽHFM , isoleucine Ile; BM and methionine Met; MBM, BM, HFM NRC, 1983;.Tacon and Jackson, 1985 . If the proper ratio between these by-products is maintained in

the diet, the EAA imbalances can be overcome and the quality of such a diet is likely toŽ .improve Davies et al., 1989 .

Terrestrial animal by-products have been extensively studied as FM alternatives inŽ .tilapia feeds, with varying results. Tacon et al. 1983 found that hexane-extracted MBM

Ž .or MBM:BM 4:1 supplemented with Met successfully replaced up to 50% of FMprotein in 45% CP diets fed to Nile tilapia fry for 6 weeks. HFM supplemented with

Ž . Ž .Met, histidine His and Lys could replace only 30% of FM protein Tacon et al., 1983 .Ž .Davies et al. 1989 found that optimum MBMrBM ratios could effectively replace up

to 75% of FM in diets fed to O. mossambicus fry for 7 weeks. Furthermore, dietsŽ .containing MBM or high MBMrBM ratios 3:1 and 2:3 were superior to FM even at a

100% substitution level. When BM was used as total replacement of FM, fish growthŽ . Ž .was still comparable to the control diet. Mansour 1998 and El-Sayed 1998 found that

red tilapia and Nile tilapia, respectively, efficiently utilized MBM and PBM as singledietary protein sources while BM produced significantly retarded growth rates and feedefficiency.


Results so far on the use of HFM as a protein source for tilapia have beenŽ . Ž . Ž .contradictory. Tacon et al. 1983 , Viola and Zohar 1984 and Davies et al. 1989

found that Nile tilapia fry, Mozambique tilapia and all male tilapia hybrids, respectively,fed HFM-based diets exhibited poor performance, presumably due to poor digestibility

Ž .and EAA profile of HFM. In addition, Bishop and Watts 1994 found that Nile tilapiaŽ .fry fed HFM, PBM and a combination of both 50:50 exhibited lower growth rates

accompanied with pathological signs of vitamin deficiencies including flesh trans-parency with yellow–brown coloration, lack of scale thickening and muscle develop-ment and vascular rupture in the superficial vessels of the caudal and pectoral fins.

Ž .However, Bishop and Watts 1994 concluded that these sources may represent low costFM replacers for Nile tilapia, if a vitamin mix and a plant fiber were added. On the

Ž . Ž .contrary, Falaye 1982 and Bishop et al. 1995 found that the growth of Nile tilapiafingerlings and fry fed HFM as a replacement of FM and FMqMBM up to 50 and 66%levels, respectively, was similar to that of fish fed FM-based diets. Rodriguez-Serna et

Ž . Žal. 1996 found that commercial defatted animal by-product meal ABM; a combination. Ž . Ž .of BM, MBM, HFM and FM , with soybean SB oil or SB oilq fish oil 1:1

successfully replaced up to 75% of FM in diets fed to Nile tilapia fry for 7 weeks in aclosed water system. In addition, ABM supplemented with SB oil, completely replacedFM in the control diet with no adverse effects on fish performance. Similarly, GaberŽ .1996 found that the growth of Nile tilapia fingerlings fed a combination of PBM andHFM as a protein source replacing FM up to 40% level was better than that of those fedthe control diet. The author suggested that this protein source could totally replace FMin Nile tilapia diets.

Terrestrial animal by-product silage has been successfully used as a protein source forŽ . Ž .tilapia. Belal et al. 1995 fed O. niloticus fingerlings 10.8 g test diets containing

Ž .0–20% chicken offal silage COS , made from chicken viscera, as a replacement of FM.They found that the growth and body composition of fish fed COS up to 20% level weresimilar to that of fish fed a FM based diet. However, higher inclusion levels of COSshould have been tested in order to determine the proper inclusion level for Nile tilapia.

A number of studies have considered animal manures as a feed source for tilapia.Ž .Alhadhrami and Yousif 1994 found that camel and cow manures could be successfully

Ž .included in blue tilapia diets 35% CP at 10 and 20% levels, respectively. Similarly,Ž . Ž .Abdelghany et al. 1997 reported that up to 20% of SBM in test diets 30% CP fed to

Ž .blue tilapia fingerlings initial weight 3.14 g could be replaced with poultry manureŽ .meal PMM with no significant reduction in fish growth.

Most of the previous studies were short-term, indoor, and conducted in closedsystems. Therefore, long-term evaluation of animal by-products as protein sources for

Žtilapia should be conducted in practical culture systems ponds, outdoor tanks and.cages . In this regard, long-term evaluation of BM as a FM replacer for Nile tilapia

Ž . Ž .fingerlings 3 g reared in cages was conducted for 120 days Otubusin, 1987 . Theauthor found that BM levels exceeding 50% of FM protein resulted in a significantreduction in fish growth, while 10% level was the most efficient. Similarly, Viola and

Ž .Zohar 1984 reported that up to 50% of FM could be successfully replaced by PBM.Ž .More recently, El-Sayed 1998 found that BM used as a sole protein source in practical

diets for Nile tilapia reared in outdoor concrete tanks for 150 days resulted in a sharp


reduction in fish performance. Similar results were reported on red tilapia fingerlingsŽ .Mansour, 1998 .

3. Plant protein sources

3.1. Oilseed plants

3.1.1. Soybean mealSBM is the best plant protein source in terms of protein content and EAA profile.

Ž .However, it is limiting in sulfur containing AA Met, Lys, Cys , and contains manyŽ .endogenous antinutrients including protease trypsin inhibitor, phytohaemagglutinin and

anti-vitamins. Many of these factors can be destroyed or inactivated during thermalŽ .processing Tacon, 1993 .

Many studies have considered SBM as a partial or total FM alternative for tilapia,with varying results. SBM could replace between 67 and 100% of FM, depending onfish species and size, dietary protein level, SBM source and processing methods andculture systems employed. Prepressed, solvent extracted SBM, with or without Metsupplementation successfully replaced up to 75% of FM in test diets fed to Nile tilapia

Ž . Ž .fry Pantha, 1982; Tacon et al., 1983 , O. mossambicus Jackson et al., 1982 and 67%Ž .in case of tilapia hybrids Shiau et al., 1989 . It appears from these results that tilapia

may gain little or no benefits from supplementing SBM with the limiting EAA. InŽ . Ž .support, Viola and Arieli 1983 and Teshima and Kanazawa 1988 reported that

supplementing tilapia diets with crystalline EAA did not improve fish performance.Minerals, rather than limiting EAA, may be the limiting factors in the efficient

Ž .utilization of SBM for tilapia. Viola et al. 1986, 1988 found that the growth of tilapiaŽ .hybrids O. niloticus=O. aureus fed a SBM-based diet supplemented with Lys, Met,

Ž .oil and dicalcium phosphate DCP was similar to that of fish offered a FM-based diet.Furthermore, the non-inclusion of the limiting EAA to SBM-based diet did not result inany growth retardation, while SBM supplemented with 3% DCP and oil completelyreplaced FM without any adverse effects on fish growth. The authors concluded thatphosphorus was the limiting factor in SBM. The lack of benefit of EAA supplementation

Ž .has also been reported with other oilseed plants El-Sayed, 1987, 1990 .The inclusion level of SBM in tilapia feeds is affected by dietary protein level. Davis

Ž .and Stickney 1978 found that the inclusion of SBM at 15% dietary protein impairedgrowth of blue tilapia, while at 36% protein, SBM could totally replace FM in the dietswithout significant retardation in fish performance. The authors suggested that thenutritional value of the feeds was different at low protein levels and became similar atthe highest protein level and the EAA level in the 36% CP SBM based diet was above

Ž .the fish requirement. Moreover, Viola et al. 1994a,b found that the addition of Lys toSBM-based diets fed to tilapia hybrids was ineffective at 25 and 30% dietary protein. At35% CP, reducing the Lysrprotein ratio impaired fish growth.

However, contradicting results were obtained with O. niloticus=O. aureus hybridsŽ .by Shiau et al. 1989 . The authors found that at 24% dietary protein level, 67% of FM


could be replaced with SBM, while at 32% protein level, replacing FM with 30% SBMsignificantly decreased fish growth and feed efficiency, due to poor amino acid balance

Ž .and the presence of trypsin inhibitor Shiau et al., 1987 . The addition of dietary Met tothe level in the control diet significantly improved fish growth.

The contradiction among researchers regarding the use of SBM as a protein sourcefor fish may be related to the quality and processing of SBM, fish species and size andculture systems. For example, it has been reported that the processing method of SBM

Ž .has a significant effect on its nutritive value. Wassef et al. 1988 found that thegermination and defattening of SBM reduced the activity of protease inhibitors. HeatingSBM helps rupture the cellulose membrane surrounding the cell and release the cell

Ž .contents making them more available Tacon and Jackson, 1985 . Heating also inacti-Ž .vates and destroys the antinutritional factors found in SBM Liener, 1980 . Wee and Shu

Ž .1989 found that the quality of full-fat SBM boiled at 1008C for 1 h was improved andŽtrypsin inhibitor activity decreased for Nile tilapia. However, El-Sayed et al. unpub-

.lished data found that full-fat SBM contained traces of protease inhibitors even afterŽ .thermal treatments at 2008C for 10 min or soaking for 3 days, leading to an increase in

Ž .trypsin secretion to compensate for the reduced activity in Nile tilapia.Mixing SBM with an animal protein source may improve its quality for tilapia.

Ž .Sadiku and Jauncey 1995a substituted FM in diets for Nile tilapia with soybean flour:Ž .poultry meat meal SBF:PMM; 25:75, 50:50 and 75:25 blends at 3 substitution levels

Ž .25, 50 and 75% and found that best growth rates and feed efficiency were achieved at75:25 blend at 25% replacement. The best lipid and protein digestibility and amino acid

Žavailability were also obtained in the 75:25 SBM:PMM ratio diet Sadiku and Jauncey,.1995b .

3.1.2. Cottonseed mealrcakeŽ . Ž .Cottonseed meal CSM and cake CSC are among the most available plant protein

sources in the world. Besides being relatively cheap, CSM contains good proteinŽ . Žcontents 26–54%, depending on processing methods and amino acid profile FAO,

.1983 . However, it contains relatively low levels of Cys, Lys and Met in addition to itsŽ .high content of gossypol a phenolic antinutrient compound which may limit the use of

CSM in animal feeds.Results on the use of CSM and CSC as protein sources for tilapia have been

Ž . Ž .controversial. For example, Ofojekwu and Ejike 1984 and Robinson et al. 1984found that O. niloticus and O. aureus fed CSC and CSM-based diets, respectively, grewat slower rates compared to fish fed FM-based diets. The authors attributed the poorperformance to the gossypol and cyclopropionic acids contained in glanded and gland-less CSM, respectively. However, it was noted that glandless CSM was better utilized

Ž .than glanded CSM Robinson et al., 1984 .On the contrary, prepressed, solvent extracted CSM was successfully used as a single

Ž .dietary protein source for O. mossambicus Jackson et al., 1982 and Nile tilapiaŽ .El-Sayed, 1990 . On the other hand, about 50% CSM successfully replaced SBM in

Ž .diets fed to tilapia hybrids reared in floating cages Viola and Zohar, 1984 , while T.zillii grew reasonably well on diets containing 80% CSM protein as a replacement of

Ž .caseinrgelatin protein El-Sayed, 1987 .


In addition to the use of CSC as a protein source in commercial pelleted feeds fortilapia, it can be used as a single feed ingredient or a source of fertilizer in semi-inten-sive tilapia culture, increasing natural food production within fish ponds. MiddendorpŽ . Ž . Ž .1995a , Middendorp and Huisman 1995 found that CSC 42% CP used as the onlyfeed input for Nile tilapia reared in earthen ponds, fertilized with cattle manure for 100

Ždays, resulted in a sharp increase in fish weight from 88 g to 303 and 321 g, at feeding.rates of 3 and 6% of fish weightsrday, respectively . Manure fertilization alone resulted

in negative growth rates. In addition, mixing CSC with brewery waste as feed inputs forŽ .the fish, had negative effects on fish growth Middendorp, 1995b .

3.1.3. Other oilseed by-productsOther oilseed by-products, including groundnut, sunflower, rapeseeds, sesame seeds,

copra, macadamia and palm kernel, may have a good potential as protein sources fortilapia. Despite their good protein contents and EAA profiles, little attention has been

Ž .given to these sources. Jackson et al. 1982 evaluated groundnut cake, sunflower meal,rapeseed meal and copra meal as protein sources in 30% CP diets fed to O. mossambi-cus for 7–9 weeks. They found that 25, 75, 75 and 50% of these sources, respectively,could effectively replace FM protein without significant retardation in fish performance.

Ž .However, Davies et al. 1990 found that only 15% rapeseed meal could effectivelyreplace FMrSBM in O. mossambicus diets, while higher levels resulted in poor growth

Ž .and feed efficiency, due to the high content of glucosinolate antinutrient in rapeseed.Ž .El-Sayed 1987 evaluated the effects of replacing caseinrgelatin protein by sesame

seed protein on T. zillii fingerlings. Fish fed sesame seed diets exhibited poor perfor-mance and showed pathological signs including hemorrhage and red spots in the mouth

Ž .and at the base of the fins even at the lowest sesame seed level 25% . Since the sesameseeds were low in Lys and zinc, the diets were re-evaluated after addition of Lys or zincor both. Fish growth increased and the pathological signs disappeared when either Lysor zinc was added to the diets. Therefore, Lys or zinc met the requirement of one or theother supporting the argument that certain minerals rather than EAA deficiency may bethe limiting factor in sesame seeds.

Ž .Fagbenro 1988 compared the use of defatted cocoa cake as a direct feed for T.Ž .guineensis initial weight 52 g in fertilized ponds. He found that fish fed with cocoa

cake grew 72.6% as well as fish fed with a 38.5% CP commercial diet. In addition,Ž .Pezzato et al. 1996 found that inclusion of up to 20% cocoa meal in fingerling Nile

tilapia diets did not affect fish growth rates, but resulted in pathological changes in fishliver and behavioral disturbances, that could have been related to the presence ofalkaloids in cocoa meal.

Ž .The growth of Nile tilapia fingerlings mean weight 2.5 g fed up to 60% palm kernelŽ .meal was similar to that of fish fed a FM-based diet Omoregie and Ogbemudia, 1993 .

Ž .Similarly, Deoliveira et al. 1997 found that the growth of fingerling Nile tilapia fedŽ .varying levels of African palm kernel meal 0–35% for 120 days was not adversely

affected.Ž .Macadamia press cake MC was successfully used as a protein source for tilapia.

Ž . Ž .Fagbenro 1993 found that the growth of monosex T. guineensis fed MC 33.4% CP inconcrete tanks for 180 days was similar to those offered a commercial 35.5% CP diet.


ŽOn the contrary, when MC replaced SBM in test diets fed to Nile tilapia mean weight.10 g at levels exceeding 50%, for 100 days, fish growth and protein digestibility were

Ž .significantly reduced Balogun and Fagbenro, 1995 . However, feed utilization effi-ciency was not affected by dietary treatments. Once again, the low price of MC favors itas a promising alternative plant protein source for tilapia.

3.2. Aquatic plants

Studies have been conducted on the use of aquatic plants in tilapia feeds, withŽ .varying, and sometimes, conflicting results. For example, El-Sayed 1992 evaluated

ŽAzolla pinnata a freshwater fern having a symbiotic relationship with nitrogen fixing.cyanobacteria Anabaena azollae as a FM replacer for Nile tilapia fingerlings and adults

respectively, at 0–100% substitution levels. He found that fish fed with Azolla pinnataŽ .showed extremely poor performance even at the lowest inclusion level 25% . Similar

Ž .results were reported on O. niloticus Almazan et al., 1986 and T. rendalli fed A.Ž . Ž .microphylla Micha et al., 1988 . In contrast, Naegel 1997 found that up to 30% of

FM-based diet fed to Nile tilapia could be successfully replaced with dried azolla meal.Ž .Moreover, Santiago et al. 1988a reported that a diet containing up to 42% of A.

pinnata produced better growth rates of Nile tilapia fry than did the control FM diet.Since fish fry require higher protein and energy levels than adults, the ‘‘estimated’’

Ž .digestible energy of 250 kcalr100 g reported by Santiago et al. 1988a appears too lowto support optimum performance of Nile tilapia fry which require about 400 kcalr100 gŽ . ŽEl-Sayed and Teshima, 1992 . Therefore, other factors such as negative effects from

.the FM used may have led to the poor performance of fish fed the control FM diet inŽ .the study of Santiago et al. 1988a .

Ž .Fresh duckweed family: Lemnaceae is a good food source for tilapia, as it containsŽ .about 35–45% CP with good AA and mineral profiles Mbagwu et al., 1990 . Skillicorn

Ž . Žet al., 1993 reported that the production of Nile tilapia fed duckweed Lemna and.Wolffia as a single nutritional input in earthen ponds in Bangladesh reached 7.5 m.t.

hay1 yeary1. Furthermore the authors suggested that with better pond management andstocking density, the production can exceed 10 m.t. hay1 yeary1. Duckweed is also a

Ž .good FM alternative for tilapia. Mbagwu et al. 1990 found that when fingerlingSarotherodon galilaeus were fed with a 33% CP diet containing duckweed as a partialprotein source, they exhibited better growth and feed utilization than those fed a 40% CP

Ž . Ž .standard diet. Similarly, Arrivillaga 1994 and Essa 1997 found that Wolffia andŽ .Lemna, respectively, replaced up to 50% of commercial feeds 35% CP of Nile tilapia

without adverse effects on fish growth and body composition.Ž .Appler 1985 found that up to 20% of FM could be replaced by another aquatic plant

Hydrodictyon reticulatum in diets fed to O. niloticus and T. zillii without adverseŽ Ž .effects on fish growth. Chiayvareesajja et al. 1990 fed moist diets containing dry

Ž .coontail Ceratophyllum demersum , rice bran and FM at ratios of 4:3:1 and 4:2:2 toŽ .Nile tilapia mean weight 88–111 g reared in floating cages for 90 days. They found

Ž .that 4:3:1 ratio was most appropriate. In another study, 3 levels 20, 30 and 40% ofŽ .coontail and chuut-nuu Eleocharis ochrostachys were included in Nile tilapia diets atŽ . Ž .3 dietary protein levels 16, 25 and 35% for 11 weeks Klinnavee et al., 1990 . At the


same protein level, fish fed plant diets grew at similar rates, while the growth increasedwith increasing dietary protein level. A diet containing either plant at 35% CP producedthe best performance and least costrkg fish produced. When juvenile and adult O.aureus were fed diets containing Elodea trifoliata, Muyriophyllum spicatum and

Ž .Potamogeton gramineous, they lost weight at 15 or 258C Okeyo, 1988 . However, EssaŽ . Ž .1997 found that up to 25% of commercial Nile tilapia feed 35% CP could bereplaced with P. pectinatus or C. demersum.

3.3. Grain legumes and plant protein concentrates

Several studies have included leguminous or cereal plants and by-products as partialŽ .replacements for FM in tilapia feeds. Leucaena leaf meal LLM, 30% CP has been

evaluated as a protein source for tilapia, with somewhat conflicting results. PantasticoŽ .and Baldia 1979, 1980 reported improved growth of O. niloticus and O. mossambicus

Ž .fed diets containing 100% LLM. On the contrary, Jackson et al. 1982 and Wee andŽ .Wang 1987 found that levels exceeding 25% LLM in 30% CP diets resulted in a

significant reduction in growth and feed utilization efficiency of O. mossambicus andNile tilapia fingerling, respectively. Similarly, the growth performance of Nile tilapia

Ž . Žbroodstock Santiago et al., 1988b and the production of O. aureus fry Badawy et al.,.1995 were retarded by increasing LLM in the diets above 40 and 15%, respectively.

The use of LLM as a feed input for tilapia is limited by the deficiency of certain EAAŽ . Ž . ŽArg, Thr, Ile, His, Met and the presence of momosine a toxic non protein AA Lim

.and Dominy, 1991 . Therefore, processing LLF may improve its quality as has beenŽ .reported by Wee and Wang 1987 who found that soaking LLF produced better results

Ž .with Nile tilapia than sun-dried or commercial LLM. Osman et al. 1996 reported thatcooked or sun-dried LLM produced better growth of Nile tilapia than did sodiumhydroxide-treated or rumen liquor-incubated LLM.

Other legume seeds have been tested as protein sources for tilapia. Ng and WeeŽ . Ž . Ž .1989 found that the performance of Nile tilapia 14.5 g fed Cassava leaf meal CLMwas reduced with increasing CLM levels in the diets. However, fish growth wassignificantly improved when CLM was supplemented with 0.1% Met. Similarly, when

Ž .the green gram legume Phaseolus aureus was fed to Nile tilapia fry at different dietaryŽprotein levels, the best growth rates were observed at 25% substitution level De Silva

. Ž . Žand Gunasekera, 1989 . Martinez-Palacios et al. 1988 found that jack bean CanaÕalia.ensiformis was a useful partial substitute for FM in O. mossambicus diets at 25%

inclusion level.Ž .Leaf protein concentrate LPC represents another FM replacer with good potential

for the aquafeed industry. The growth of O. mossambicus fingerlings fed purified alfalfaŽ .LPC 69% CP as a replacement of up to 35% of FM protein in a 40% CP diet was

Ž .better than that obtained with the FM-based diet Olvera-Novoa et al., 1990 . In anotherŽ .study, Olvera-Novoa et al. 1997 found that 20–30% of FM in diets fed to Nile tilapia

Ž .fry could be successfully replaced with cowpea Vigna unguiculata protein concentrate.Cereal by-products including maize gluten meal, gluten feed, grain distillers and

brewery waste have been successfully used as protein sources for tilapia. The growth ofNile tilapia fingerlings fed maize distiller grain with soluble, gluten meal and gluten feed


Žas partial protein sources was better than that of fish fed a FM-based diet Wu et al.,. Ž .1994, 1995; Tudor et al., 1995 . In support, Wu et al. 1996 , and Twibell and Brown

Ž . Ž1998 reported excellent growth of O. niloticus and tilapia hybrids O. niloticus=O.. Žaureus , respectively, fed all-plant diets containing corn by-products corn gluten meal,

.corn grain, corn distillers grains and corn gluten feed and SBM as a protein source. PitoŽbrewery waste was evaluated as FM replacer in test diets for T. busumana fry mean

. Žweight 1.5 g at 50 and 100% substitution levels Oduro-Boateng and Bart-Plange,.1988 . The best performance was achieved at 50% inclusion level. However, the authors

recommended pito brewery waste as full replacement for FM in tilapia feeds with greatŽ .economic feasibility. On the other hand, Pouomogne 1995 reported that brewery draff

could be included at 30% in Nile tilapia diets without depressive effects on growth rate.

4. Single-cell proteins

Ž .Single cell proteins SCP are a group of microorganisms including unicellular algae,fungi, bacteria, cyanobacteria, and yeast. Biosynthesis and utilization of SCP by tilapiawithin intensive and semi-intensive farming systems has attracted the attention of manyresearchers. SCP production is a simple, cheap and effective way of producing natural

Ž .fish food. For example, Chamberlain and Hopkins 1994 reported that spraying a sourceof carbon such as wheat bran and cellulose on the surface of pond water with continuous

Ž .aeration, at the optimum carbon:nitrogen ratio 15:1 would increase bacterial growth.Produced bacteria consume the carbon source as energy and reduce ammonia concentra-

Ž .tion through nitrification, while the fish feed on these bacteria Fig. 3 . This approachhas been adopted for O. aureus grown intensively in aerated, circulated tanks as

Ž .reported by Avnimelech and Mokady 1988 . The authors found that SCP producedusing cheap carbon and nitrogen sources, can partially replace expensive commercial

Ž .protein sources in O. aureus feeds. In addition, Avnimelech et al. 1989 found that theŽ .growth of fish fed with SCP was identical to that of those fed a protein-rich 30% CP

diet. Similar results were reported with other tilapia where SCP including bacteria,phytoplankton, detrital biomass, periphytic mats and microbial proteins were success-

Žfully used as protein sources by different tilapia species Moriarty and Moriarty, 1973;

Fig. 3. Production of natural food in tilapia fish ponds.

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168160Ž .Appendix A. Alternative protein sources tested and recommended for tilapia. Levels tested are a substitution of standard dietary protein mainly FM or whole diet.

Recommended levels are based on biological andror economic evaluation. For details see text

Ž . Ž . Ž . Ž .Source specification Levels % tested Levels % recommended Species weight, g ReferencesAnimal sources:

UŽ .Shrimp head meal 0–15 15 O. aureus N.A. Toledo et al., 1987Ž .Shrimp meal 100 100 O. niloticus 20 El-Sayed, 1998Ž .Shrimp meal 100 100 Red tilapia 9 Mansour, 1998

Ž . Ž .LFSqSBM 1:1 0–75 75 O. niloticus 8 Fagbenro et al., 1994Ž .LFSqSBM or MBM 0–75 75 O. niloticus 8 Fagbenro, 1994

Ž . Ž .LFSqPBM or HFM 1:1 50 50 O. niloticus 8 Fagbenro, 1994Ž .PBM 50 50 Hybrids 195 Viola and Zohar, 1984

Ž .PBMqHFM 10–40 40 O. niloticus 1.4 Gaber, 1996Ž .MBMqMet 40–50 50 O. niloticus 0.011 Tacon et al., 1983Ž .MBM 100 100 O. niloticus 20 El-Sayed, 1998Ž .MBM 100 100 Red tilapia 9 Mansour, 1998

Ž . Ž .MBMqBM 4:1 10–50 50 O. niloticus 0.01 Tacon et al., 1983Ž .MBM 0–100 75 O. mossambicus 1 Davies et al., 1989

Ž . Ž .MBMqBM 2:3 0–100 100 O. mossambicus 1 Davies et al., 1989Ž .BM 0–100 100 O. mossambicus 1 Davies et al., 1989

Ž .BM 100 -100 O. niloticus 20 El-Sayed, 1998Ž .BM 100 -100 Red tilapia 9 Mansour, 1998Ž .BM 10–50 10 O. niloticus 3.9 Otubusin, 1987Ž .HFM 0–100 66 O. niloticus 0.01 Bishop et al., 1995Ž .HFM"EAA 10–50 30 O. niloticus 4–5 Tacon et al., 1983Ž .Animal by-products 0–100 100 O. niloticus 0.1 Rodriguez-Serna et al., 1996Ž .Chicken offal silage 0–20 20 O. niloticus 10.8 Belal et al., 1995

Plant sourcesOilseed plants:SBM

Ž .SBM"Met 75 75 O. niloticus 0.8 Tacon et al., 1983Ž .SBM"Met 0–100 100 O. aureus 0.3–0.5 Davis and Stickney, 1978

Ž .SBM 0–100 75 O. mossambicus 50 Jackson et al., 1982Ž .SBM"Met 0–100 67 Hybrids 4.47 Shiau et al., 1989

Ž .Soy protein concentrate 0–100 100 O. niloticus 3.2 Abdelghany, 1997

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Ž .SBMqEAAqDCPqoil 0–100 100 Hybrids 84 Viola et al., 1988Ž .SBMqDCPqoil 0–100 100 Hybrids 169 Viola et al., 1988

Ž . Ž .SB flourqPMM 75:25 25–75 25 O. niloticus 7 Sadiku and Jauncey, 1995a

CSMŽ .CSM"lys 100 100 O. niloticus 20 El-Sayed, 1990

Ž .CSM 0–100 50 O. mossambicus 12 Jackson et al., 1982Ž .CSM 50 50 Hybrids 195 Viola and Zohar, 1984Ž .CSM 0–100 80 T. zillii 1.5 El-Sayed, 1987

Ž .CSM 14–47 ? O. aureus 1.6 Robinson et al., 1984

Other oil seed by-productsŽ .Sesameseed meal 0–75 25 T. zillii 2.4 El-Sayed, 1987

Ž .Groundnut cake 0–100 25 O. mossambicus 30 Jackson et al., 1982Ž .Rapeseed meal 15–60 15 O. mossambicus 0.3 Davies et al., 1990Ž .Rapeseed meal 0–75 75 O. mossambicus 13 Jackson et al., 1982Ž .Copra meal 0–50 25–50 O. mossambicus 31 Jackson et al., 1982

Ž .Defatted cocoa cake 100 100 T. guineensis 52 Fagbenro, 1988Ž .Defatted cocoa cake 0–20 20 O. niloticus 9 Pezzato et al., 1996Ž .Palm kernel cake 0–100 60 O. niloticus 2.5 Omoregie and Ogbemudia, 1993Ž .Palm kernel cake 0–35 30 O. niloticus 1.5 Deoliveira et al., 1997Ž .Macadamia press cake 0–100 50 O. niloticus 7.5–12 Balogun and Fagbenro, 1995Ž .Macadamia press cake 100 100 T. guineensis N.A. Fagbenro, 1993

Aquatic plantsŽ .Spirulina 20 20 O. mossambicus 7.5 Chow and Woo, 1990Ž .Spirulina 0–100 40 O. mossambicus 0.3 Olvera-Novoa et al., in press

Ž .Azolla pinnata 8–42 42 O. niloticus 0.011 Santiago et al., 1988aŽ .Azolla pinnata 0–100 -25 O. niloticus 4–40 El-Sayed, 1992Ž .Azolla microphylla 50–100 ? O. niloticus 5 Micha et al., 1988Ž .Azolla microphylla 50–100 ? T. rendalli 5 Micha et al., 1988Ž .Hydrodictyon 0–100 20 O. niloticus 1 Appler, 1985

Ž .Hydrodictyon 0–100 20 T. zillii 1 Appler, 1985Ž .Eleocharis ochrostachys 20–40 20–30 O. niloticus 7 Klinnavee et al., 1990Ž .Potamogeton 25–50 25 O. niloticus 14.5 Essa, 1997Ž .Ceratopyhllum demersum 20–40 20–30 O. niloticus 7 Klinnavee et al., 1990

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Ž .Appendix A. continued

Ž . Ž . Ž . Ž .Source specification Levels % tested Levels % recommended Species weight, g ReferencesŽ .Ceratopyhllum demersum 25–50 25 O. niloticus 14.5 Essa, 1997

Ž .Duckweed 0–100 50–100 Tilapia sp not given Skillicorn et al., 1993Ž . Ž . Ž . Ž .Source specification Levels % tested Levels % recommended Species weight, g References

Aquatic plantsŽ . Ž .Duckweed Wolffia 0–75 50 O. niloticus 0.4 Arrivillaga, 1994Ž . Ž .Duckweed Lemna 0–50 50 O. niloticus 14.5 Essa, 1997

SCPŽ .Pruteen 50–100 50 Hybrids N.A. Viola and Zohar, 1984

Ž .Eurolysine fodder protein 0–40 -40 O. mossambicus 1.4 Davies and Wareham, 1988Ž .Yeast 20–40 40 O. niloticus N.A Heydarpour, 1987

Grain legumes and plantprotein concentrates

Ž . Ž .Leucaena leaf meal LLM 0–50 -25 O. mossambicus 50 Jackson et al., 1982Ž .LLM 0–100 100 O. mossambicus N.A. Pantastico and Baldia, 1979

Ž .LLM 0–50 15 O. aureus 43–50 Badawy et al., 1995Ž .Cassava leaf meal 20–100 -100 O. niloticus 13.8–15.4 Ng and Wee, 1989Ž .Green gram legume 13–50 25–37 O. niloticus 2.92 De Silva and Gunasekera, 1989

Ž .Jack bean meal 0–35 25 O. mossambicus 0.4–0.9 Martinez-Palacios et al., 1988Ž .Sesbania seed meal 0–35 -10 O. mossambicus 0.3 Olvera-Novoa et al., 1988Ž .Alfalfa LPC 15–55 35 O. mossambicus 0.3 Olvera-Novoa et al., 1990

Ž .Cowpea LPC 0–50 20–30 O. niloticus 0.16 Olvera-Novoa et al., 1997

Ž .Corn gluten feedqSBM 100 100 O. niloticus 30 Wu et al., 1995Ž .Corn glutenqSBM 100 100 O. niloticus 30 Wu et al., 1995

Ž .Corn gluten feed 16–49 30–42 Tilapia 0.4 Wu et al., 1996Ž .Corn distillers’ grains 16–49 35–49 Tilapia 0.4 Wu et al., 1996Ž .Corn co-products 0–100 50 Hybrids 21 Twibell and Brown, 1998

Ž .Pito brewery waste 0–100 100 T. busumana 1.5 Oduro-Boateng and Bart-Plange, 1988Ž .Brewery draff 30 30 O. niloticus 10–100 Pouomogne, 1995

Ž .Coffee pulp 0–30 30 O. aureus 9–50 Bayne et al., 1976Ž .Coffee pulp 0–39 13–26 O. aureus 4–10 Ulloa Rojas and Weerd, 1997

UNot available.


.Shrestha and Knud-Hansen, 1994; Dempster et al., 1995 . Therefore, more attentionŽ .should be given to natural food production SCP in fish ponds especially in developing

countries where tilapia culture is widely practiced.SCP is currently produced on commercial scales and used as a protein source for fish.

Ž . Ž .Viola and Zohar 1984 found that growth of tilapia hybrids O. niloticus=O. aureusŽ .fed commercial SCP Pruteen, 70% CP in cages at 50% substitution level, was similar

to that of those fed a 30% CP FM-based diet. However, fish performance was reducedŽ .when SCP totally replaced FM in the diets. Similarly, Davies and Wareham 1988

found that up to 40% FM in diets of O. mossambicus fry could be replaced with SCPŽ .Eurolysine Fodder Protein; EFP, 64% CP , with no negative effects on fish growth and

Ž .feed utilization. Furthermore, Heydarpour 1987 found that partial replacement of FMwith yeast protein at 20 and 40% level in Nile tilapia diet resulted in a significantreduction in fish growth. However, fish growth was fairly good even at 40% substitutionlevel. Replacement of 20% of a commercial eel diet with Spirulina alga did not affect

Žthe growth, appetite and amylase and protease activities of O. mossambicus Chow and. Ž .Woo, 1990 . Olvera-Novoa et al. in press replaced FM in a control diet fed to O.

mossambicus fry with Spirulina maxima at 0–100% levels. They found that the growthand feed efficiency of fish fed 20–40% Spirulina were similar to that of those fed thecontrol diet.

5. Economic feasibility of fish meal alternatives

Most of the above mentioned works have evaluated FM replacers in tilapia feedsfrom biological and nutritional points of view. Very few studies have considered theeconomic evaluation of feed inputs for tilapia. Some workers have demonstrated thatdespite that most of these feed inputs produced lower biological performance than

Ž .standard control diets, costrbenefit analyses indicated that they were economicallyŽ .better. For example, economic evaluation of cotton seed meal El-Sayed, 1990 , corn

Ž . Žgluten feed and meal Wu et al., 1995 and animal by-product meal Rodriguez-Serna et. Žal., 1996; El-Sayed, 1998 as protein sources for Nile tilapia; brewery waste Oduro-

. Ž .Boateng and Bart-Plange, 1988 for T. busumana and cocoa cake Fagbenro, 1988 forT. guineensis indicated that incidence cost and profit indices of these protein sourceswere better than for FM-based feeds. The authors suggested the use of these sources astotal fish-meal replacers for tilapia.

Acknowledgements

The author thanks the International Center for Advanced Mediterranean AgronomicŽ .Studies-Mediterranean Agronomic Institute of Zaragoza CIHEAM-IAMZ for provid-

ing a travel grant to present this review at the VIII International Symposium on‘‘Nutrition and Feeding of Fish’’ held at Las Palmas De Gran Canaria, Spain, 1–4 June,1998. Thanks are also due to Dr. A. Tacon, Hawaii Oceanographic Institute, USA, forproviding recent references on the subject and for his valuable suggestions.


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