JOURNAL OF THE Vol. 39, No.

1
WORLD AQUACULTURE SOCIETY February, 2008

Use of a Compound Protein Source as a Replacement for Fish Meal

in Diets of Large Yellow Croaker, Pseudosciaena crocea R.
LU ZHANG1, KANGSEN MAI2, QINGHUI AI, QINGYUAN DUAN, CHUNXIAO ZHANG,
HUITAO LI, AND BEIPING TAN
The Key Laboratory of Mariculture (Ministry of Education), Ocean University of China,
5 Yushan Road, Qingdao 266003, China

Abstract
A feeding trial was conducted to evaluate the potential of a compound protein source (CPS) as
a replacement of fish meal (FM) in diets for large yellow croaker, Pseudosciaena crocea R. The CPS
was made of soybean meal, meat and bone meal, peanut meal, and rapeseed meal (4:3:2:1 in weight)
by adding crystalline L-methionine (0.77%), L-lysine (0.95%), and L-isoleucine (0.44%) to ensure the
essential amino acid (EAA) contents of CPS diets to reach or exceed those of FM diet. Six iso-
nitrogenous and isoenergetic diets (Diets 1–6) were formulated to contain 0, 9, 18, 27, 36, and 45%
CPS replacing 0, 13, 26, 39, 52, and 65% FM protein, respectively. Triplicate groups of 180 fish
(initial average 1.88 6 0.01 g) were fed diets to apparent satiation by hand twice daily for 8 wk in
floating sea cages (1.0 3 1.0 3 1.5 m). The water temperature ranged from 26.5 to 29.5 C, the
salinity from 25 to 28&, and the dissolved oxygen content was approximately 7 mg/L during the
experimental period. The results showed that specific growth rate (SGR) and feed efficiency ratio
(FER) of fish fed Diets 2 and 3 were not significantly different from those of fish fed control diet (Diet
1). However, SGR and FER of fish fed Diets 4–6 were significantly lower compared with control
group (P , 0.05). The whole-body proximate analysis showed that protein significantly decreased
with increasing dietary CPS levels (P , 0.05), while the whole-body lipid, ash, and moisture showed
no significant differences among dietary treatments. Methionine, cystine, and lysine contents of the
whole body were significantly influenced by dietary CPS level (P , 0.05), while other EAA contents
showed no significant differences. Results of the present study indicated that CPS could replace about
26% FM protein in diets for the large yellow croaker on crude protein basis without adverse effect
on growth.

The protein contents in commercial fish diets
range from 30% to more than 50% by dry
weight, which are much higher than those of
domestic animals. This is because of limited
ability to use dietary carbohydrate as an energy
source for most of the fish, thus requiring a much
higher percentage of protein in the diet (NRC
1993). The development of commercial aqua-
feeds has been traditionally based on fish meal
(FM) as the main protein source. While inten-
sive aquaculture continues to expand, so does
the requirement for high-quality protein sources
(Barlow 1989; Hardy 1996). However, the global
FM production has been decreasing greatly in
recent years, which results in the increase of
1 Present address: Zhanjiang Yuehai Feed Co. Ltd. R&D
Center, 22 Airport Road, Xiashan District, Zhanjiang
524017, China.
2 Corresponding authors.
Ó Copyright by the World Aquaculture Society 2008
the market price for fish. Hence, finding alter-
native protein sources to replace FM in the diet
has become the focus of research from the
viewpoint of producing a stable supply of com-
mercial diets at a low price.
Many studies have shown considerable suc-
cess in partial or total replacement of FM with
soybean meal (SBM) or other soybean products
in diets for various fish species (Reinitz 1980;
Mohsen and Lovell 1990; Vivyakarn et al. 1992;
Arndt et al. 1999). Rapeseed meal (RM), peanut
meal (PM), pea seed meal, and lupin seed meal
were also potential substitutes for FM and have
been the objects of a few studies (Yrukowski
et al. 1978; Gomes and Kaushik 1989; McCurdy
and March 1992; Gomes et al. 1995). The use of
the animal proteins has been focused on the
meat and bone meal (MBM) and poultry by-
product meal (Flower 1991; Murai 1992; Davies
et al. 1998; Webster et al. 2000; Millamena

83
84 ZHANG ET AL.
2002). Although alternative protein sources
showed considerable potential in replacement
of FM, they also associated with negative qual-
ities such as low protein content, less than ideal
amino acid balance, presence of antinutritional
factors (ANFs), and high proportion of fiber or
ash.
Most studies were conducted on the replace-
ment of FM with single protein source in various
fish species. A little information is available on
the combined use of a few plant and/or animal
proteins to replace FM protein. Watanabe and
PongManeerat (1993) put forward that further
improvements in the use of plant meals were
likely to involve their combination with other
protein sources rather than single one. Watanabe
et al. (1997) also suggested that the studies on
the replacement of FM and use of a combination
of different protein sources have been found to
be worth alternative.
Large yellow croaker is a popular food fish
and an important aquaculture species in China
because of its delicious meat, fast growth, effi-
cient feed conversion, and high market value.
However, a main constraint to the culture of
large yellow croaker is the limited supply of
trash fish that is presently the main feed source
for grow-out production. To develop nutrition-
ally balanced feeds for this fish, a few of our
previous studies have been published on the
nutrient requirements and digestive physiology
of it (Duan et al. 2001; Ma et al. 2005; Mai
et al. 2005, 2006a, 2006b; Ai et al. 2006; Li
et al. 2007).
In our previous work, we found that large
yellow croaker could use SBM and MBM
efficiently (Mai et al. 2005, 2006a, 2006b; Ai
et al. 2006), but it had difficulty using PM and
RM (Li et al. 2007). To develop a cost-effective
diet, a compound protein source (CPS) was
made. Judging from the data of our previous
work and some literatures on protein replace-
ment, the CPS was made of SBM, MBM, PM,
and RM (4:3:2:1 in weight) by adding crystal-
line l-methionine, l-lysine, and l-isoleucine to
ensure the essential amino acid (EAA) contents
of CPS diets to reach or exceed those of the FM
diet. The present study was undertaken to eval-
uate the effect of dietary incorporation of the
CPS on the growth performance and body com-
position in large yellow croaker so as to develop
commercial feed with less FM for large yellow
croaker.
Materials and Methods
Experimental Diets
The CPS was made of SBM, MBM, PM, and
RM (4:3:2:1 in weight) by adding crystalline
L-methionine (0.77%), L-lysine (0.95%), and
L-isoleucine (0.44%) to ensure the EAA con-
tents in CPS diets to reach or exceed those of
the FM diet, calculated based on the NRC
(1993) data. Six isonitrogenous (crude protein
43%) and isoenergetic (gross energy 20 kJ/g
dry matter) diets were formulated (Table 1),
with FM varying between 48.8 and 17.1%. Six
levels of CPS (0, 9, 18, 27, 36, and 45%) were
incorporated into experimental diets to replace
0, 13, 26, 39, 52, and 65% FM protein (Diets
1–6). Diet 1 with FM as the main protein source
was used as a control.
Ingredients were ground into fine powder
through 220-mm mesh. All the ingredients were
thoroughly mixed with fish oil, and water was
added to produce stiff dough. The dough was
then made into pellets using the cold extrusion
process with a twin-screw extruder model (F-26
(II), South China University of Technology,
China) and dried for about 12 h in a ventilated
oven at 50 C until the moisture contents were
below 10%. After drying, the diets were broken
up and sieved into proper pellet size. The sizes
of pellets were 1.5 3 3.0 mm and 2.5 3
4.0 mm. All diets were sealed in bags and stored
at 15 C until used.
Experimental Procedure
The experimental fish were obtained from
a commercial farm in Ningbo, China. Prior to
the feeding trial, the fish were reared in floating
sea cages (3.0 3 3.0 3 3.0 m), and the fish fed
the control diet (Diet 1) for 2 wk to acclimate to
the experimental diet and rearing conditions. At
the start of the experiment, the fish were fasted
for 24 h and weighed after being anesthetized
with eugenol (1:10,000) (Shanghai Reagent
Corp, China). Juvenile fish of similar size (mean
 USE OF CPS AS A REPLACEMENT FOR FM 85

TABLE 1. Composition and proximate analysis of the experimental diets with graded CPS (% dry weight).

Diets (substitute level of FM protein)

Ingredients (%) Diet 1 (0%) Diet 2 (13%) Diet 3 (26%) Diet 4 (39%) Diet 5 (52%) Diet 6 (65%)
FM 48.8 42.4 36.1 29.7 23.4 17.1
CPS1 0.0 9.0 18.0 27.0 36.0 45.0
Squid viscera meal 5.0 5.0 5.0 5.0 5.0 5.0
Beer yeast meal 3.5 3.5 3.5 3.5 3.5 3.5
Menhaden fish oil 2.0 2.0 2.0 2.0 2.0 2.0
Soybean oil 3.0 3.0 3.0 3.0 3.0 3.0
Lecithin 3.0 3.0 3.0 3.0 3.0 3.0
Wheat meal 29.6 26.9 24.3 21.6 19.0 16.3
Sodium alginate 1.0 1.0 1.0 1.0 1.0 1.0
Mineral premix2 2.0 2.0 2.0 2.0 2.0 2.0
Vitamin premix3 2.0 2.0 2.0 2.0 2.0 2.0
Mold inhibitor4 0.1 0.1 0.1 0.1 0.1 0.1
Ethoxyquin 0.05 0.05 0.05 0.05 0.05 0.05
Proximate analysis
Crude protein (% DM) 43.3 43.9 43.2 43.1 43.5 43.2
Crude lipid (% DM) 12.4 12.0 12.3 12.1 12.1 12.3
Ash (% DM) 11.3 11.7 11.9 12.3 12.4 12.8
Moisture (%) 9.3 9.6 9.3 9.5 9.4 9.4
Gross energy (kJ/g DM) 20.5 20.3 20.3 20.3 20.2 20.1
Total phosphorus content (%)5 1.61 1.58 1.56 1.53 1.50 1.48
CPS 5 compound protein source; DM 5 dry matter; FM 5 fish meal.
1 CPS: made of soybean meal, meat and bone meal, peanut meal, and rapeseed meal (4:3:2:1 in weight) by adding 0.77%

L-methionine, 0.95% L-lysine, and 0.44% L-isoleucine.

2 Mineral premix (mg or g/kg diet): NaF, 2 mg; KI, 0.8 mg; CoCl
6H O (1%), 50 mg; CuSO
5H O, 10 mg;
2 2 4 2
FeSO4
H2O, 80 mg; ZnSO4
H2O, 50 mg; MnSO4
H2O, 60 mg; MgSO4
7H2O, 1200 mg; Ca (H2PO4)2
H2O, 3000 mg;
NaCl, 100 mg; and Zoelite, 15.447 g.
3 Vitamin premix (mg or g/kg diet): thiamin, 25 mg; riboflavin, 45 mg; pyridoxine HCl, 20 mg; vitamin B , 0.1 mg;
12
vitamin K3, 10 mg; inositol, 800 mg; pantothenic acid, 60 mg; niacin acid, 200 mg; folic acid, 20 mg; biotin, 1.20 mg;
retinol acetate, 32 mg; cholecalciferol, 5 mg; alpha-tocopherol, 120 mg; ascorbic acid, 2000 mg; choline chloride,
2500 mg; ethoxyquin, 150 mg; and wheat middling, 14.012 g.
4 Mold inhibitor: contained 50% calcium propionic acid and 50% fumaric acid.
5 Calculated based on the NRC (1993) data.

initial weight 1.88 6 0.01 g) were randomly as-
signed to 18 floating sea cages (1.0 3 1.0 3
1.5 m), and each cage was stocked with 180 fish.
Each diet was randomly assigned to triplicate
cages. To prevent the waste of dietary pellets,
fish were slowly hand-fed little by little till
apparent satiation on the basis of visual observa-
tion of fish-feeding behavior, twice daily at 0500
and 1730 h, respectively. The feeding trial
lasted for 8 wk, for Week 1–4, 1.5-mm pellets
were fed; thereafter, 2.5-mm pellets were fed
until the end of the experiment. During this
period, the number and weight of dead fish were
recorded. The water temperature fluctuated
from 26.5 to 29.5 C, salinity from 25 to 28&,
and dissolved oxygen was approximately
7 mg/L. At the end of the experiment, the fish
were fasted for 24 h and fish in each cage were
weighed and counted.
Measurement and Analysis
In each cage, 20 fish at the start and 10 fish at
the termination were randomly sampled and
stored frozen ( 20 C) for the analysis of proxi-
mate whole-body composition. Proximate anal-
ysis of diets and fish were performed according
to the standard methods of AOAC (1995): dry
matter after drying in an oven at 105 C until
constant weight, crude protein (N 3 6.25) by
Kjeldhal method after acid digestion, lipid by
ether extraction using Soxhlet, ash content
by cineration in a muffle furnace at 600 C
for 12 h, and gross energy by direct combustion
in an oxygen bomb calorimeter (Parr 1281;
86 ZHANG ET AL.

Moline, IL, USA). For amino acid analysis
(except for methionine and cystine), feeds were
freeze-dried and then hydrolyzed with 6N HCl
at 110 C for 24 h, and the chromatographic sep-
aration and analysis of the amino acids were
performed after orthophthaldehyde (Sigma,
St. Louis, MO, USA) derivation using reverse-
phase high-performance liquid chromatography
(HP1100; Agilent, Palo Alto, CA, USA) fol-
lowed by the modified procedure of Gardner
and Miller (1980). While for methionine and cys-
tine, the samples were oxidized with performic
acid at 10 C for 3 h to obtain methionine sul-
fone and cysteic acid and then freeze-dried
twice with deionized water. The freeze-dried in-
gredients were hydrolyzed and analyzed as the
process of other amino acids. To evaluate the
effect of dietary treatments on the amino acid
profile of the whole fish body, at the end of the
feeding trial, three fish from each cage were col-
lected, cut into small pieces, pooled, and
homogenized. Their amino acid profiles were
analyzed as described above.
Calculation and Statistical Analysis
The following parameters were calculated as
follows:
Specific growth rate (SGR) (% /d) 5 100 3 (ln
Wf ln Wi)/t and feed efficiency ratio (FER) 5
wet weight gain (g)/dry diet fed (g). Where
Wf and Wi were final and initial fish weights
and t is the experimental duration in days.
One-way ANOVA was used to determine the
significance between means. Normality and
homogeneity of variance were confirmed (SPSS
10.0), and comparison between means was ana-
lyzed by Tukey test. Significant level was cho-
sen at P , 0.05.
Results
Survivals, feed consumption, SGR, and FER
were shown in Table 2. Survival showed a de-
creasing trend (96.7–92.2%) with the increasing
dietary CPS levels, but no significant differen-
ces were observed. Feed consumption of fish
fed Diets 1–3 were between 3800 and 3900 g,
higher than Diets 4–6 (between 3500 and
3600 g), but no significant differences were
found between the six diets. SGR of fish fed
Diets 1–3 were all above 3.5 and showed no sig-
nificant differences, meanwhile fish fed Diets
4–6 all showed inferior SGR (lower than 3.2)
(P , 0.05). FER of fish fed Diets 1–3 showed
no significant differences, while fish fed Diets
4–6 all showed significant lower FER than the
control (P , 0.05).
Whole-body compositions of the cultured fish
are shown in Table 3. The protein contents of
fish fed Diets 1–3 (ranged from 16. 0 to 16.1%)
were significantly higher than those of fish
fed Diets 4–6 (ranged from 14.4 to 14.8%)
(P , 0.01). Whole-body lipid (ranged from 4.6
to 5.2%), moisture (ranged from 75.8 to 77.5%),
and ash (ranged from 4.7 to 5.1%) showed no

TABLE 2. Survival, final weight, feed consumption, SGR, and FER of large yellow croaker fed the experimental diets with
graded CPS for 8 wk.1

Dietary treatments Survival Final weight Feed consumption SGR

(substitute level of fish meal protein) (%) (g) (g) (% /d) FER
Diet 1 (0%) 96.7 14.28a 3842.8 3.62a 0.73a
Diet 2 (13%) 94.4 14.21a 3861.1 3.61a 0.72a
Diet 3 (26%) 93.9 14.13a 3834.2 3.60a 0.72a
Diet 4 (39%) 92.8 11.17b 3502.5 3.18b 0.62b
Diet 5 (52%) 92.8 11.11b 3594.8 3.17b 0.60b
Diet 6 (65%) 92.2 10.04b 3542.4 2.99b 0.55b
Pooled SEM 0.21 0.45 59.40 0.07 0.18
ANOVA
F value 1.168 22.034 1.804 22.972 13.538
P value 0.379 0.000 0.187 0.000 0.000
CPS 5 compound protein source; SGR 5 specific growth rate; FER 5 feed efficiency ratio.
1 Values are means of three replicate sea cages. Values within the same column sharing a common superscript letters are
not significantly different determined by Tukey test (P . 0.05).
 USE OF CPS AS A REPLACEMENT FOR FM 87

TABLE 3. Whole-body composition of large yellow croaker fed the experimental diets with graded compound protein
source for 8 wk1 (wet weight).

Dietary treatments
(substitute level of fish meal protein) Crude protein (%) Crude lipid (%) Ash (%) Moisture (%)
Diet 1 (0%) 16.0a 5.1 4.0 76.7
Diet 2 (13%) 16.1a 5.2 4.1 75.9
Diet 3 (26%) 16.1a 5.2 3.9 75.8
Diet 4 (39%) 14.5b 4.6 3.8 77.4
Diet 5 (52%) 14.4b 4.8 3.7 77.5
Diet 6 (65%) 14.8b 4.6 4.0 76.1
Pooled SEM 0.2 0.8 0.5 0.2
ANOVA
F value 12.825 4.305 1.411 3.399
P value 0.000 0.053 0.298 0.105
1 Values are means of three replicate sea cages. Values within the same column sharing a common superscript letters are

not significantly different determined by Tukey test (P . 0.05).

significant differences among all dietary treat-
ments. The analysis of amino acids of whole fish
(Table 4) showed that significant deceases were
observed in methionine and lysine contents (P
, 0.05) with the increase of CPS levels in the
experimental diets. There was a decrease trend
in cystine content of whole body with the
increasing dietary CPS levels; however, no sig-
nificant difference can be found in whole-body
cystine content among the fish fed Diets 1–6.
Meanwhile, other EAA contents were not sig-
nificantly influenced by the incorporation levels
of CPS in the experimental diets.
Discussion
The present study demonstrated the potential
of CPS (MBM : SBM : PM : RM 5 4:3:2:1
in weight, adding 0.77% L-methionine, 0.95%
L-lysine, and 0.44% L-isoleucine) for inclusion
in diets of the large yellow croaker. Results of
the study demonstrated that growth of the juvenile
large yellow croaker was not significantly
depressed when diets containing 9 (Diet 2) and
18% (Diet 3) CPS (replace 13 and 26% FM pro-
tein). When the CPS was used to replace 39, 52,
and 65% FM protein (Diets 4–6), growth was sig-
nificantly reduced (P , 0.05). This agreed with
the results obtained by Lim et al. (2004) who re-
ported dehulled SBM could replace FM up to
30% with methionine and lysine supplementation
in fingerling Korean rockfish. Further, a few re-
ports have also been reported on very high
replacement of FM with plant and/or animal pro-
teins supplemented with amino acid in diets of
fishes. Webster et al. (1995) suggested that a
methionine-supplemented diet with an all protein

TABLE 4. Whole-body essential amino acid contents of large yellow croaker fed the experimental diets with graded
compound protein source for 8 wk1 (g/16 g N).

Dietary treatments
(substitute level of
fish meal protein) Arginine Cystine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Valine
Diet 1 (0%) 6.07 0.51a 2.04 4.44 8.64 8.55a 3.26a 4.43 4.82 4.87
Diet 2 (13%) 5.97 0.47ab 2.09 4.35 8.46 8.33b 3.17ab 4.27 4.78 4.81
Diet 3 (26%) 6.08 0.48a 2.12 4.41 8.53 8.39b 3.22ab 4.39 4.77 4.85
Diet 4 (39%) 5.97 0.43ab 2.05 4.46 8.63 8.37b 3.20ab 4.42 4.77 4.82
Diet 5 (52%) 5.89 0.40b 2.01 4.45 8.61 8.33b 3.23ab 4.30 4.70 4.84
Diet 6 (65%) 5.85 0.42ab 2.01 4.44 8.67 8.18c 3.06b 4.38 4.72 4.81
Pooled SEM 0.04 0.09 0.02 0.05 0.04 0.02 0.03 0.05 0.05 0.05
ANOVA
F value 1.476 12.000 0.809 0.810 2.572 23.331 3.617 1.052 0.786 0.503
P value 0.268 0.000 0.565 0.565 0.084 0.000 0.032 0.433 0.579 0.768
1 Values are means of three replicate sea cages. Values within the same column sharing a common superscript letters are

not significantly different determined by Tukey test (P . 0.05).

88 ZHANG ET AL.
source (SBM) could totally replace FM in a diet
for blue catfish without adverse effect on weight
gain or body composition. McGoogan and Gatlin
(1997) grew red drum successfully with diets in
which 90% of FM protein was replaced by
SBM with addition of amino acids. Discrepancies
of these results may be because of fish species,
size and age, genetic differences, feeding regime,
and culture conditions in different experiments.
In consistent with some other studies about
plant and/or animal protein sources, the inverse
relationship was found between inclusion level
and growth (Jackson et al. 1982; Flower 1991;
Reigh and Ellis 1992; Webster et al. 1992). In
this study, the decreased growth probably be-
cause of the deficiencies in available EAAs
and suboptimal EAA balance (NRC 1993). Pro-
tein digestibility generally reflects amino acid
availability. The apparent digestibility coeffi-
cients (ADCs) of protein for SBM, MBM, RM,
and PM (84.5, 78.3, 79.6, and 80.6%) were sig-
nificantly lower than that of FM (92.4%) in
large yellow croaker in our previous work (Li
et al. 2007). Low protein digestibility possibly
explained the decline in growth performance
of juvenile large yellow croaker when SBM,
MBM, RM, and PM were included into the
experimental diets as the alternative protein
sources of FM. Calculated ADC of protein for
CPS was 81.3% based on the data from Li
et al. (2007), which was much lower than that
of FM (92.4%). The lower ADC of protein def-
initely resulted in the lower ADC of EAAs.
Therefore, with the increasing of the CPS levels
in diets, the available EAA contents decreased.
SBM, MBM, PM, and RM have low EAA con-
tents compared with FM. In the present study,
the crystalline lysine, methionine, and isoleu-
cine were added to ensure the EAA contents
of CPS diets to reach or exceed those of FM
diet. However, the CPS with the added crystal-
line amino acids could only replace 26% FM
protein but not even higher as we thought
before. The possible reason is the low ADC of
protein in CPS or leaching of crystalline amino
acids during the feeding. Therefore, the EAAs
contents that the experimental fish can absorb
were insufficient for its growth in high-CPS-
contained groups.
Anti-nutritional factors (ANFs), perhaps, are
the other reasons of the decreased growth of
the fish. ANFs in the plant proteins decreased
ADC of diets (Krogdahl et al. 1994; Olli et al.
1994). Complex dietary and nutrient interac-
tions result from ANFs reduced the scope and
potential for using plant ingredients of different
fish species (Davies et al. 1998). Evidence exists
that high-value marine finfish, including the
flounders, turbot, seabass, and sea bream, are
particularly sensitive to the ANFs contents of
plant ingredients (Francis et al. 2001).
In conclusion, the present study revealed that
26% FM could be replaced by CPS in commer-
cial diet of the large yellow croaker on crude
protein basis without adverse effect on growth
performance. Further evaluation on the ANFs
and the ADC of EAAs for the CPS should be
conducted.
Acknowledgments
The study was supported by the National Key
Technologies R&D Program for the tenth 5-yr
plan of China (grant number: 2001BA505B-
06) and the High-Tech R&D Program of China
(grant number: 2004AA623010). We thank
X. X. Wang, X. W. Liu, J. H. Chen, J. Q. Li,
F. P. Tan, and H. Chen in diet production.
Thanks are also due to J. K. Shentu for all his
help during the experiment.
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