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Aquaculture 179 1999.

149168

Alternative dietary protein sources for farmed


tilapia, Oreochromis spp.
)
Abdel-Fattah M. El-Sayed
Oceanography Department, Faculty of Science, Uniersity of Alexandria, Alexandria, Egypt

Abstract

Tilapia are widely cultured in the tropical and subtropical regions of the world and constitute
the third largest group of farmed finfish, only after carps and salmonids, with an annual growth
rate of about 11.5%. Global production of farmed tilapia has increased more than three-fold since
1984, 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
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 reduce
the dependence on fish meal as a single protein source in aquafeeds. Therefore, fish nutritionists
have made several attempts to partially or totally replace fish meal with less expensive, locally
available protein sources. The present review presents alternative dietary protein sources for
tilapia, 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 sources
are 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,
ancient Egyptians raised tilapia for human consumption about 20002500 BC Chimits,

)
Tel.: q20-3-420-3858; fax: q20-3-491-1794; E-mail: amelsayed@alex.eun.eg

0044-8486r99r$ - see front matter q 1999 Elsevier Science B.V. All rights reserved.
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150 A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168

1957; Bardach et al., 1972.. Currently, tilapia culture is widely practiced in many
tropical and subtropical regions of the world. More than 22 tilapia species are being
cultured worldwide. However, Nile tilapia Oreochromis niloticus ., Mozambique tilapia
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 carps
10.37 = 10 6 m.t.. and salmonids 0.94 = 10 6 m.t. FAO, 1997., with an average annual
growth rate of about 11.5%. In addition, Nile tilapia was the 6th most cultured finfish
species in the world in 1995 with a total production of 473,641 m.t. and an average
compound growth rate of about 12% per annum since 1986. The global production of
farmed tilapia has increased more than three-fold since 1984, from 186,544 m.t. to
659,000 m.t., representing 4.48% of total farmed finfish in 1995, with a value of
US$925 million Tacon, 1997. Fig. 1.. About 650,000 m.t. or 98.6% of farmed tilapia
were produced in developing countries in 1995 Fig. 2. with Asia alone producing about
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 commercial
aquafeeds has been traditionally based on fish meal FM. as the main protein source due
to its high protein content and balanced essential amino acid EAA. profile. FM is also
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 in
animal and aquaculture feeds Tacon, 1993.. The shortage in global FM production
coupled with increased demand and competition for its use in livestock and poultry
feeds has further increased FM prices. It is evident, on the long-run, that many
developing countries will be unable to depend on FM as a major protein source in
aquafeeds. Therefore, several attempts have been made to partially or totally replace FM
with less expensive, locally available protein sources.

Fig. 1. World production of farmed tilapia during 19861995. Source: FAO 1997..
A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168 151

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

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, which
include 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 of
these 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 commercial
potential of fishery by-products including fish protein concentrate and hydrolysates,
shrimp meal SM., krill meal and squid meal. as partial or total protein sources for
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. Mansour
1998. and El-Sayed 1998. found that shrimp meal 50% CP. can be used as a total FM
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 feeds
showed varying, but promising, results. For example, Lapie and Bigueras-Benitez 1992.
found that the growth of Nile tilapia fed formic acid preserved fish silage FFS. blended
with FM at 1:1 ratio was similar to that of fish fed a FM-based diet. When FFS:FM ratio
152 A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168

was increased to 3:1, growth performance was significantly reduced, presumably due to
acidity of the diet and high proportion of free amino acids in fish silage. It has been
suggested that acidity reduces diet acceptance and affects protease activity in fish guts
Hardy et al., 1983., while free amino acids may depress fish appetite Wilson et al.,
1984.. Similarly, Fagbenro 1994. fed Nile tilapia a 30% CP FM-based diet and diets
containing blended lactic acid fermented fish silage LFS. 1:1, wrw. with soybean
meal SBM., poultry by-product meal PBM., hydrolyzed feather meal HFM. or meat
and bone meal MBM. in a recirculated tank system for 10 weeks. No significant
differences in growth, digestibility, hemoglobin and hematocrit contents were found.
Furthermore, Fagbenro et al. 1994. found that up to 75% of FM protein was
successfully replaced by dried, blended LFS:soybean meal 1:1. incorporated in diets fed
to all male Nile tilapia fingerlings.
Fagbenro and Jauncey 1993. found that LFS could be stored at 308C for 6 months
with little change in the quality and nitrogen loss. They also found that protein autolysis
in LFS was directly related to prevailing temperature. In addition, LFS had very good
water stability and low nitrogen loss regardless of the binder used Fagbenro and
Jauncey, 1995.. Apparent dry matter, protein and lipid digestibilities determined in O.
mossambicus 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

The 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
contents and good EAA profiles Tacon, 1993.. However, they may be deficient in one
or more of the EAA. The most limiting EAA in these by-products are lysine Lys; PBM,
HFM., 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 to
improve Davies et al., 1989..
Terrestrial animal by-products have been extensively studied as FM alternatives in
tilapia feeds, with varying results. Tacon et al. 1983. found that hexane-extracted MBM
or MBM:BM 4:1. supplemented with Met successfully replaced up to 50% of FM
protein in 45% CP diets fed to Nile tilapia fry for 6 weeks. HFM supplemented with
Met, histidine His. and Lys could replace only 30% of FM protein Tacon et al., 1983..
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, diets
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 growth
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 single
dietary protein sources while BM produced significantly retarded growth rates and feed
efficiency.
A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168 153

Results so far on the use of HFM as a protein source for tilapia have been
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
and EAA profile of HFM. In addition, Bishop and Watts 1994. found that Nile tilapia
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 yellowbrown coloration, lack of scale thickening and muscle develop-
ment and vascular rupture in the superficial vessels of the caudal and pectoral fins.
However, Bishop and Watts 1994. concluded that these sources may represent low cost
FM replacers for Nile tilapia, if a vitamin mix and a plant fiber were added. On the
contrary, Falaye 1982. and Bishop et al. 1995. found that the growth of Nile tilapia
fingerlings and fry fed HFM as a replacement of FM and FM q MBM up to 50 and 66%
levels, respectively, was similar to that of fish fed FM-based diets. Rodriguez-Serna et
al. 1996. found that commercial defatted animal by-product meal ABM; a combination
of BM, MBM, HFM and FM., with soybean SB. oil or SB oil q fish oil 1:1.
successfully replaced up to 75% of FM in diets fed to Nile tilapia fry for 7 weeks in a
closed water system. In addition, ABM supplemented with SB oil, completely replaced
FM in the control diet with no adverse effects on fish performance. Similarly, Gaber
1996. found that the growth of Nile tilapia fingerlings fed a combination of PBM and
HFM as a protein source replacing FM up to 40% level was better than that of those fed
the control diet. The author suggested that this protein source could totally replace FM
in Nile tilapia diets.
Terrestrial animal by-product silage has been successfully used as a protein source for
tilapia. Belal et al. 1995. fed O. niloticus fingerlings 10.8 g. test diets containing
020% 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 were
similar to that of fish fed a FM based diet. However, higher inclusion levels of COS
should 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.
Alhadhrami and Yousif 1994. found that camel and cow manures could be successfully
included in blue tilapia diets 35% CP. at 10 and 20% levels, respectively. Similarly,
Abdelghany et al. 1997. reported that up to 20% of SBM in test diets 30% CP. fed to
blue tilapia fingerlings initial weight 3.14 g. could be replaced with poultry manure
meal PMM. with no significant reduction in fish growth.
Most of the previous studies were short-term, indoor, and conducted in closed
systems. Therefore, long-term evaluation of animal by-products as protein sources for
tilapia 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
fingerlings 3 g. reared in cages was conducted for 120 days Otubusin, 1987.. The
author found that BM levels exceeding 50% of FM protein resulted in a significant
reduction in fish growth, while 10% level was the most efficient. Similarly, Viola and
Zohar 1984. reported that up to 50% of FM could be successfully replaced by PBM.
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
154 A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168

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

3. Plant protein sources

3.1. Oilseed plants

3.1.1. Soybean meal


SBM is the best plant protein source in terms of protein content and EAA profile.
However, it is limiting in sulfur containing AA Met, Lys, Cys., and contains many
endogenous antinutrients including protease trypsin. inhibitor, phytohaemagglutinin and
anti-vitamins. Many of these factors can be destroyed or inactivated during thermal
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 on
fish species and size, dietary protein level, SBM source and processing methods and
culture systems employed. Prepressed, solvent extracted SBM, with or without Met
supplementation successfully replaced up to 75% of FM in test diets fed to Nile tilapia
fry Pantha, 1982; Tacon et al., 1983., O. mossambicus Jackson et al., 1982. and 67%
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. In
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
utilization of SBM for tilapia. Viola et al. 1986, 1988. found that the growth of tilapia
hybrids O. niloticus= O. aureus . fed a SBM-based diet supplemented with Lys, Met,
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 in
any growth retardation, while SBM supplemented with 3% DCP and oil completely
replaced FM without any adverse effects on fish growth. The authors concluded that
phosphorus was the limiting factor in SBM. The lack of benefit of EAA supplementation
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
and Stickney 1978. found that the inclusion of SBM at 15% dietary protein impaired
growth of blue tilapia, while at 36% protein, SBM could totally replace FM in the diets
without significant retardation in fish performance. The authors suggested that the
nutritional value of the feeds was different at low protein levels and became similar at
the highest protein level and the EAA level in the 36% CP SBM based diet was above
the fish requirement. Moreover, Viola et al. 1994a,b. found that the addition of Lys to
SBM-based diets fed to tilapia hybrids was ineffective at 25 and 30% dietary protein. At
35% CP, reducing the Lysrprotein ratio impaired fish growth.
However, contradicting results were obtained with O. niloticus= O. aureus hybrids
by Shiau et al. 1989.. The authors found that at 24% dietary protein level, 67% of FM
A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168 155

could be replaced with SBM, while at 32% protein level, replacing FM with 30% SBM
significantly decreased fish growth and feed efficiency, due to poor amino acid balance
and the presence of trypsin inhibitor Shiau et al., 1987.. The addition of dietary Met to
the level in the control diet significantly improved fish growth.
The contradiction among researchers regarding the use of SBM as a protein source
for fish may be related to the quality and processing of SBM, fish species and size and
culture systems. For example, it has been reported that the processing method of SBM
has a significant effect on its nutritive value. Wassef et al. 1988. found that the
germination and defattening of SBM reduced the activity of protease inhibitors. Heating
SBM helps rupture the cellulose membrane surrounding the cell and release the cell
contents making them more available Tacon and Jackson, 1985.. Heating also inacti-
vates and destroys the antinutritional factors found in SBM Liener, 1980.. Wee and Shu
1989. found that the quality of full-fat SBM boiled at 1008C for 1 h was improved and
trypsin 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 after
thermal treatments at 2008C for 10 min. or soaking for 3 days, leading to an increase in
trypsin secretion to compensate for the reduced activity. in Nile tilapia.
Mixing SBM with an animal protein source may improve its quality for tilapia.
Sadiku and Jauncey 1995a. substituted FM in diets for Nile tilapia with soybean flour:
poultry meat meal SBF:PMM; 25:75, 50:50 and 75:25 blends. at 3 substitution levels
25, 50 and 75%. and found that best growth rates and feed efficiency were achieved at
75:25 blend at 25% replacement. The best lipid and protein digestibility and amino acid
availability were also obtained in the 75:25 SBM:PMM ratio diet Sadiku and Jauncey,
1995b..

3.1.2. Cottonseed meal r cake


Cottonseed meal CSM. and cake CSC. are among the most available plant protein
sources in the world. Besides being relatively cheap, CSM contains good protein
contents 2654%, depending on processing methods. and amino acid profile FAO,
1983.. However, it contains relatively low levels of Cys, Lys and Met in addition to its
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
controversial. For example, Ofojekwu and Ejike 1984. and Robinson et al. 1984.
found that O. niloticus and O. aureus fed CSC and CSM-based diets, respectively, grew
at slower rates compared to fish fed FM-based diets. The authors attributed the poor
performance to the gossypol and cyclopropionic acids contained in glanded and gland-
less CSM, respectively. However, it was noted that glandless CSM was better utilized
than glanded CSM Robinson et al., 1984..
On the contrary, prepressed, solvent extracted CSM was successfully used as a single
dietary protein source for O. mossambicus Jackson et al., 1982. and Nile tilapia
El-Sayed, 1990.. On the other hand, about 50% CSM successfully replaced SBM in
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
caseinrgelatin protein El-Sayed, 1987..
156 A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168

In addition to the use of CSC as a protein source in commercial pelleted feeds for
tilapia, 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. Middendorp
1995a., Middendorp and Huisman 1995. found that CSC 42% CP. used as the only
feed input for Nile tilapia reared in earthen ponds, fertilized with cattle manure for 100
days, 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 for
the fish, had negative effects on fish growth Middendorp, 1995b..

3.1.3. Other oilseed by-products


Other oilseed by-products, including groundnut, sunflower, rapeseeds, sesame seeds,
copra, macadamia and palm kernel, may have a good potential as protein sources for
tilapia. Despite their good protein contents and EAA profiles, little attention has been
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 79 weeks. They found that 25, 75, 75 and 50% of these sources, respectively,
could effectively replace FM protein without significant retardation in fish performance.
However, Davies et al. 1990. found that only 15% rapeseed meal could effectively
replace FMrSBM in O. mossambicus diets, while higher levels resulted in poor growth
and feed efficiency, due to the high content of glucosinolate antinutrient. in rapeseed.
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
and at the base of the fins even at the lowest sesame seed level 25%.. Since the sesame
seeds were low in Lys and zinc, the diets were re-evaluated after addition of Lys or zinc
or both. Fish growth increased and the pathological signs disappeared when either Lys
or zinc was added to the diets. Therefore, Lys or zinc met the requirement of one or the
other supporting the argument that certain minerals rather than EAA deficiency may be
the limiting factor in sesame seeds.
Fagbenro 1988. compared the use of defatted cocoa cake as a direct feed for T.
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,
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 fish
liver and behavioral disturbances, that could have been related to the presence of
alkaloids in cocoa meal.
The growth of Nile tilapia fingerlings mean weight 2.5 g. fed up to 60% palm kernel
meal was similar to that of fish fed a FM-based diet Omoregie and Ogbemudia, 1993..
Similarly, Deoliveira et al. 1997. found that the growth of fingerling Nile tilapia fed
varying levels of African palm kernel meal 035%. for 120 days was not adversely
affected.
Macadamia press cake MC. was successfully used as a protein source for tilapia.
Fagbenro 1993. found that the growth of monosex T. guineensis fed MC 33.4% CP. in
concrete tanks for 180 days was similar to those offered a commercial 35.5% CP diet.
A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168 157

On 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
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 it
as 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, with
varying, and sometimes, conflicting results. For example, El-Sayed 1992. evaluated
Azolla 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 0100% substitution levels. He found that fish fed with Azolla pinnata
showed extremely poor performance even at the lowest inclusion level 25%.. Similar
results were reported on O. niloticus Almazan et al., 1986. and T. rendalli fed A.
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.
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
digestible energy of 250 kcalr100 g reported by Santiago et al. 1988a. appears too low
to support optimum performance of Nile tilapia fry which require about 400 kcalr100 g
El-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 in
the study of Santiago et al. 1988a..
Fresh duckweed family: Lemnaceae. is a good food source for tilapia, as it contains
about 3545% CP with good AA and mineral profiles Mbagwu et al., 1990.. Skillicorn
et 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 and
stocking density, the production can exceed 10 m.t. hay1 yeary1 . Duckweed is also a
good FM alternative for tilapia. Mbagwu et al. 1990. found that when fingerling
Sarotherodon galilaeus were fed with a 33% CP diet containing duckweed as a partial
protein source, they exhibited better growth and feed utilization than those fed a 40% CP
standard diet. Similarly, Arrivillaga 1994. and Essa 1997. found that Wolffia and
Lemna, respectively, replaced up to 50% of commercial feeds 35% CP. of Nile tilapia
without adverse effects on fish growth and body composition.
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 adverse
effects on fish growth. Chiayvareesajja et al. 1990. fed moist diets containing dry
coontail Ceratophyllum demersum., rice bran and FM at ratios of 4:3:1 and 4:2:2 to
Nile tilapia mean weight 88111 g. reared in floating cages for 90 days. They found
that 4:3:1 ratio was most appropriate. In another study, 3 levels 20, 30 and 40%. of
coontail and chuut-nuu Eleocharis ochrostachys. were included in Nile tilapia diets at
3 dietary protein levels 16, 25 and 35%. for 11 weeks Klinnavee et al., 1990.. At the
158 A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168

same protein level, fish fed plant diets grew at similar rates, while the growth increased
with increasing dietary protein level. A diet containing either plant at 35% CP produced
the best performance and least costrkg fish produced. When juvenile and adult O.
aureus were fed diets containing Elodea trifoliata, Muyriophyllum spicatum and
Potamogeton gramineous, they lost weight at 15 or 258C Okeyo, 1988.. However, Essa
1997. found that up to 25% of commercial Nile tilapia feed 35% CP. could be
replaced 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 partial
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. Pantastico
and Baldia 1979, 1980. reported improved growth of O. niloticus and O. mossambicus
fed diets containing 100% LLM. On the contrary, Jackson et al. 1982. and Wee and
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 and
Nile tilapia fingerling, respectively. Similarly, the growth performance of Nile tilapia
broodstock 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 EAA
Arg, 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 been
reported by Wee and Wang 1987. who found that soaking LLF produced better results
with Nile tilapia than sun-dried or commercial LLM. Osman et al. 1996. reported that
cooked or sun-dried LLM produced better growth of Nile tilapia than did sodium
hydroxide-treated or rumen liquor-incubated LLM.
Other legume seeds have been tested as protein sources for tilapia. Ng and Wee
1989. found that the performance of Nile tilapia 14.5 g. fed Cassava leaf meal CLM.
was reduced with increasing CLM levels in the diets. However, fish growth was
significantly improved when CLM was supplemented with 0.1% Met. Similarly, when
the green gram legume Phaseolus aureus . was fed to Nile tilapia fry at different dietary
protein levels, the best growth rates were observed at 25% substitution level De Silva
and Gunasekera, 1989.. Martinez-Palacios et al. 1988. found that jack bean Canaalia
ensiformis. was a useful partial substitute for FM in O. mossambicus diets at 25%
inclusion level.
Leaf protein concentrate LPC. represents another FM replacer with good potential
for the aquafeed industry. The growth of O. mossambicus fingerlings fed purified alfalfa
LPC 69% CP. as a replacement of up to 35% of FM protein in a 40% CP diet was
better than that obtained with the FM-based diet Olvera-Novoa et al., 1990.. In another
study, Olvera-Novoa et al. 1997. found that 2030% of FM in diets fed to Nile tilapia
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 of
Nile tilapia fingerlings fed maize distiller grain with soluble, gluten meal and gluten feed
A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168 159

as partial protein sources was better than that of fish fed a FM-based diet Wu et al.,
1994, 1995; Tudor et al., 1995.. In support, Wu et al. 1996., and Twibell and Brown
1998. reported excellent growth of O. niloticus and tilapia hybrids O. niloticus= O.
aureus ., 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. Pito
brewery waste was evaluated as FM replacer in test diets for T. busumana fry mean
weight 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 great
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

Single cell proteins SCP. are a group of microorganisms including unicellular algae,
fungi, bacteria, cyanobacteria, and yeast. Biosynthesis and utilization of SCP by tilapia
within intensive and semi-intensive farming systems has attracted the attention of many
researchers. SCP production is a simple, cheap and effective way of producing natural
fish food. For example, Chamberlain and Hopkins 1994. reported that spraying a source
of carbon such as wheat bran and cellulose on the surface of pond water with continuous
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-
tion through nitrification, while the fish feed on these bacteria Fig. 3.. This approach
has been adopted for O. aureus grown intensively in aerated, circulated tanks as
reported by Avnimelech and Mokady 1988.. The authors found that SCP produced
using cheap carbon and nitrogen sources, can partially replace expensive commercial
protein sources in O. aureus feeds. In addition, Avnimelech et al. 1989. found that the
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-
fully used as protein sources by different tilapia species Moriarty and Moriarty, 1973;

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


160
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
Source specification. Levels %. tested Levels %. recommended Species weight, g. References
Animal sources:
Shrimp head meal 015 15 O. aureus N.A..U Toledo et al., 1987
Shrimp meal 100 100 O. niloticus 20. El-Sayed, 1998
Shrimp meal 100 100 Red tilapia 9. Mansour, 1998
LFSqSBM 1:1. 075 75 O. niloticus 8. Fagbenro et al., 1994
LFSqSBM or MBM 075 75 O. niloticus 8. Fagbenro, 1994

A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168


LFSqPBM or HFM 1:1. 50 50 O. niloticus 8. Fagbenro, 1994
PBM 50 50 Hybrids 195. Viola and Zohar, 1984
PBMqHFM 1040 40 O. niloticus 1.4. Gaber, 1996
MBMqMet 4050 50 O. niloticus 0.011. Tacon et al., 1983
MBM 100 100 O. niloticus 20. El-Sayed, 1998
MBM 100 100 Red tilapia 9. Mansour, 1998
MBMqBM 4:1. 1050 50 O. niloticus 0.01. Tacon et al., 1983
MBM 0100 75 O. mossambicus 1. Davies et al., 1989
MBMqBM 2:3. 0100 100 O. mossambicus 1. Davies et al., 1989
BM 0100 100 O. mossambicus 1. Davies et al., 1989
BM 100 -100 O. niloticus 20. El-Sayed, 1998
BM 100 -100 Red tilapia 9. Mansour, 1998
BM 1050 10 O. niloticus 3.9. Otubusin, 1987
HFM 0100 66 O. niloticus 0.01. Bishop et al., 1995
HFM"EAA 1050 30 O. niloticus 45. Tacon et al., 1983
Animal by-products 0100 100 O. niloticus 0.1. Rodriguez-Serna et al., 1996
Chicken offal silage 020 20 O. niloticus 10.8. Belal et al., 1995

Plant sources
Oilseed plants:
SBM
SBM"Met 75 75 O. niloticus 0.8. Tacon et al., 1983
SBM"Met 0100 100 O. aureus 0.30.5. Davis and Stickney, 1978
SBM 0100 75 O. mossambicus 50. Jackson et al., 1982
SBM"Met 0100 67 Hybrids 4.47. Shiau et al., 1989
Soy protein concentrate 0100 100 O. niloticus 3.2. Abdelghany, 1997
SBMqEAAqDCPqoil 0100 100 Hybrids 84. Viola et al., 1988
SBMqDCPqoil 0100 100 Hybrids 169. Viola et al., 1988
SB flourqPMM 75:25. 2575 25 O. niloticus 7. Sadiku and Jauncey, 1995a

CSM
CSM"lys 100 100 O. niloticus 20. El-Sayed, 1990
CSM 0100 50 O. mossambicus 12. Jackson et al., 1982
CSM 50 50 Hybrids 195. Viola and Zohar, 1984
CSM 0100 80 T. zillii 1.5. El-Sayed, 1987
CSM 1447 ? O. aureus 1.6. Robinson et al., 1984

A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168


Other oil seed by-products
Sesameseed meal 075 25 T. zillii 2.4. El-Sayed, 1987
Groundnut cake 0100 25 O. mossambicus 30. Jackson et al., 1982
Rapeseed meal 1560 15 O. mossambicus 0.3. Davies et al., 1990
Rapeseed meal 075 75 O. mossambicus 13. Jackson et al., 1982
Copra meal 050 2550 O. mossambicus 31. Jackson et al., 1982
Defatted cocoa cake 100 100 T. guineensis 52. Fagbenro, 1988
Defatted cocoa cake 020 20 O. niloticus 9. Pezzato et al., 1996
Palm kernel cake 0100 60 O. niloticus 2.5. Omoregie and Ogbemudia, 1993
Palm kernel cake 035 30 O. niloticus 1.5. Deoliveira et al., 1997
Macadamia press cake 0100 50 O. niloticus 7.512. Balogun and Fagbenro, 1995
Macadamia press cake 100 100 T. guineensis N.A.. Fagbenro, 1993

Aquatic plants
Spirulina 20 20 O. mossambicus 7.5. Chow and Woo, 1990
Spirulina 0100 40 O. mossambicus 0.3. Olvera-Novoa et al., in press
Azolla pinnata 842 42 O. niloticus 0.011. Santiago et al., 1988a
Azolla pinnata 0100 - 25 O. niloticus 440. El-Sayed, 1992
Azolla microphylla 50100 ? O. niloticus 5. Micha et al., 1988
Azolla microphylla 50100 ? T. rendalli 5. Micha et al., 1988
Hydrodictyon 0100 20 O. niloticus 1. Appler, 1985
Hydrodictyon 0100 20 T. zillii 1. Appler, 1985
Eleocharis ochrostachys 2040 2030 O. niloticus 7. Klinnavee et al., 1990
Potamogeton 2550 25 O. niloticus 14.5. Essa, 1997
Ceratopyhllum demersum 2040 2030 O. niloticus 7. Klinnavee et al., 1990

161
Appendix A. continued.

162
Source specification. Levels %. tested Levels %. recommended Species weight, g. References
Ceratopyhllum demersum 2550 25 O. niloticus 14.5. Essa, 1997
Duckweed 0100 50100 Tilapia sp not given. Skillicorn et al., 1993
Source specification. Levels %. tested Levels %. recommended Species weight, g. References

Aquatic plants
Duckweed Wolffia. 075 50 O. niloticus 0.4. Arrivillaga, 1994
Duckweed Lemna. 050 50 O. niloticus 14.5. Essa, 1997

A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168


SCP
Pruteen 50100 50 Hybrids N.A.. Viola and Zohar, 1984
Eurolysine fodder protein 040 - 40 O. mossambicus 1.4. Davies and Wareham, 1988
Yeast 2040 40 O. niloticus N.A. Heydarpour, 1987

Grain legumes and plant


protein concentrates
Leucaena leaf meal LLM. 050 - 25 O. mossambicus 50. Jackson et al., 1982
LLM 0100 100 O. mossambicus N.A.. Pantastico and Baldia, 1979
LLM 050 15 O. aureus 4350. Badawy et al., 1995
Cassava leaf meal 20100 -100 O. niloticus 13.815.4. Ng and Wee, 1989
Green gram legume 1350 2537 O. niloticus 2.92. De Silva and Gunasekera, 1989
Jack bean meal 035 25 O. mossambicus 0.40.9. Martinez-Palacios et al., 1988
Sesbania seed meal 035 -10 O. mossambicus 0.3. Olvera-Novoa et al., 1988
Alfalfa LPC 1555 35 O. mossambicus 0.3. Olvera-Novoa et al., 1990
Cowpea LPC 050 2030 O. niloticus 0.16. Olvera-Novoa et al., 1997
Corn gluten feedqSBM 100 100 O. niloticus 30. Wu et al., 1995
Corn glutenqSBM 100 100 O. niloticus 30. Wu et al., 1995
Corn gluten feed 1649 3042 Tilapia 0.4. Wu et al., 1996
Corn distillers grains 1649 3549 Tilapia 0.4. Wu et al., 1996
Corn co-products 0100 50 Hybrids 21. Twibell and Brown, 1998
Pito brewery waste 0100 100 T. busumana 1.5. Oduro-Boateng and Bart-Plange, 1988
Brewery draff 30 30 O. niloticus 10100. Pouomogne, 1995
Coffee pulp 030 30 O. aureus 950. Bayne et al., 1976
Coffee pulp 039 1326 O. aureus 410. Ulloa Rojas and Weerd, 1997
U
Not available.
A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168 163

Shrestha and Knud-Hansen, 1994; Dempster et al., 1995.. Therefore, more attention
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.
Viola and Zohar 1984. found that growth of tilapia hybrids O. niloticus= O. aureus .
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 reduced
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 SCP
Eurolysine Fodder Protein; EFP, 64% CP., with no negative effects on fish growth and
feed utilization. Furthermore, Heydarpour 1987. found that partial replacement of FM
with yeast protein at 20 and 40% level in Nile tilapia diet resulted in a significant
reduction in fish growth. However, fish growth was fairly good even at 40% substitution
level. Replacement of 20% of a commercial eel diet with Spirulina alga did not affect
the growth, appetite and amylase and protease activities of O. mossambicus Chow and
Woo, 1990.. Olvera-Novoa et al. in press. replaced FM in a control diet fed to O.
mossambicus fry with Spirulina maxima at 0100% levels. They found that the growth
and feed efficiency of fish fed 2040% Spirulina were similar to that of those fed the
control diet.

5. Economic feasibility of fish meal alternatives

Most of the above mentioned works have evaluated FM replacers in tilapia feeds
from biological and nutritional points of view. Very few studies have considered the
economic evaluation of feed inputs for tilapia. Some workers have demonstrated that
despite that most of these feed inputs produced lower biological performance than
standard control. diets, costrbenefit analyses indicated that they were economically
better. For example, economic evaluation of cotton seed meal El-Sayed, 1990., corn
gluten feed and meal Wu et al., 1995. and animal by-product meal Rodriguez-Serna et
al., 1996; El-Sayed, 1998. as protein sources for Nile tilapia; brewery waste Oduro-
Boateng and Bart-Plange, 1988. for T. busumana and cocoa cake Fagbenro, 1988. for
T. guineensis indicated that incidence cost and profit indices of these protein sources
were better than for FM-based feeds. The authors suggested the use of these sources as
total fish-meal replacers for tilapia.

Acknowledgements

The author thanks the International Center for Advanced Mediterranean Agronomic
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, 14 June,
1998. Thanks are also due to Dr. A. Tacon, Hawaii Oceanographic Institute, USA, for
providing recent references on the subject and for his valuable suggestions.
164 A.-F.M. El-Sayedr Aquaculture 179 (1999) 149168

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