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Scholars
Journa ls

  

African Journal of Agricultural Marketing ISSN: 2375-1061 Vol. 12 (3), pp. 001-010, March, 2024. Available 
online at www.internationalscholarsjournals.org © International Scholars Journals 

 

Author(s) retain the copyright of this article. 
 

 

Full Length Research Paper 

 

Assessing the suitability of soybean meal as a 
protein source for Argyrosomus Regius (Asso, 

1801) (Sciaenidae): A nutritional evaluation 
 

Jorge Velazco-Vargas, Silvia Martínez-Llorens, Miguel Jover Cerda and Ana 
Tomás-Vidal 

 
Research Group in Aquatic Resources, Institute of Animal Science and Technology, 

Polytechnic University of Valencia, Valencia, Spain. 
 

Accepted 12 December, 2023 
 
The meagre (Argyrosomus regius) is a carnivorous fish which requires diets with higher protein content, causing 
an increment in diets cost. A way to diminish this cost is to use vegetable meals like soybean meal (SB). So the 
aim of this trial was to determine the optimum inclusion level of defatted soybean meal in experimental diets for 
this species. 800 fishes (165 g) were distributed in 8 tanks, two replicates per treatment. Four isoproteic (50% CP) 
and isolipidic (17% Cl) diets were formulated with four levels of soybean meal inclusion, 0, 15, 30 and 45%. The 
trial lasted 107 days. Meagre fed diets 15 and 30% obtained the highest final weight. There were no significant 
differences among treatments in the feed conversion rate (FCR) and the protein efficiency (PER). According to the 
quadratic regression, the optimum SB inclusion to maximize thermal growth coefficient (TGC) was 26.4% and for 
FCR was 27.6%. No significant differences were observed in energy, protein and amino acid retention among 
diets. The inclusion of SB in meagre diets can generate a decrease in the use of fish meal and in turn reduce the 
cost of producing meagre Mediterranean aquaculture industry. 

 
Key words: Argyrosomus regius, fish meal replacement, defatted soybean meal, economic analysis. 

 
INTRODUCTION 

 
The species belonging to the Scianidae family and 
selected for this present experiment is Argyrosomus 
regius known as Meagre, is a good candidate for the  
diversification on commercial aquaculture in 
Mediterranean and Eastern Atlantic for its good flesh and 
growth rate (El-Shebly et al., 2007; Roo et al., 2010).  

The meagre produced in floating cages has shown 
good management (Jiménez et al., 2005) and high 
growth rate, reaching 1 kg in 10 to 13 months (Calderón 
et al., 1997; Roo et al., 2010). Limited information about 
the optimal feeding nutritional require-ements of meagre 
is available, it only exists a recent study of dietary lipid 
requirements (Chatzifotis et al., 2010). Likewise the 
effects of different levels of plant proteins on the on  
 
 

 
*Corresponding author. E-mail: atomasv@dca.upv.es Tel: 34- 
96-3879752. Fax: 34-96-3877439. 

 
 
 

 
growing of meagre have been studied very recently 
(Estévez et al., 2010).  

Increase of aquaculture production around the world 
depends upon the development of sustainable protein 
sources to replace fish meal in aquafeeds. Fish meal is 
generally incorporated at levels between 30 and 60% in 
feeds for carnivorous marine fish (Wang et al., 2006a). 
Aquaculture production demands more and more 
alternative proteins to substitute fish meal. These meals 
should not have good amino acids profiles, but also lower 
prices than fish meal to reduce the production cost. The 
alternative meals should be highly digestible protein 
sources of plant and/or animal origin that support similar 
fish performance and concurrently have no adverse 
effects upon the environment (Murray et al., 2010). 
Defatted soybean meal (standard toasted and solvent-
extracted, SB) is the most used vegetable meal in 
aquafeeds, because is a widely available, economical 
protein source with relatively high digestible protein and 



2 

 

 
 
 

 

energy contents and good amino acid profile (Wang et 
al., 2006b). The use of defatted soybean protein as a 
dietary protein has been examined for many commercial 
important marine fish species such as cobia 
(Rachycentron canadum) (Zhou et al., 2005), 
Mediterranean yellowtail (Seriola dumerili) (Tomás et al., 
2005), European sea bass (Dicentrarchus labrax) (Tibaldi 
et al., 2006), Sharpsnout seabream (Diplodus puntazzo) 
(Hernández et al., 2007) and gilthead sea bream (Sparus 
aurata) (Martínez-Llorens et al., 2009).  

Soybean meal has a different acceptance in other 
carnivorous sciaenid species, both qualitatively and 
quantitatively, but there is no information available on 
meagre. In the Sciaenidae family, SB meal has been 
tested in different species; Nibea miichthioides has a 
limited ability to utilize SB as a protein source in practical 
feeds (Wang et al., 2006b) and Sciaenops ocellatus 
gained much weight with diets containing 50% of protein 
from soybean meal (McGoogan and Gatlin III, 1997; 
Reigh and Ellis, 1992). These results indicate a 
considerable variation in the ability of different species of 
the same family to utilize SB protein as an alternative to 
fish protein in the diet.  

The aim of this trial was to determinate the optimum 
inclusion level of deffated soybean meal (SB) in 
experimental diets for meagre (A. regius), to maximize 
growth, feed efficiency parameters and amino acid 
retention and relate it with economic analysis. 
 

 
MATERIALS AND METHODS 
 
Experimental setup 
 
The trial was conducted in 8 octagonal concrete tanks (4000 L) 
inside a recirculated seawater system at the aquaculture laboratory 
of Animal Science Department at the Polytechnic University of 
Valencia, (Valencia, Spain). The tanks were set up in a marine 

water recirculation system (65 m
3
 of capacity) with a rotary 

mechanic filter and a gravity biofilter of around 6 m
3
 capacity. All 

tanks were equipped with aeration and water was heated by a heat 
pump installed in the system. The equipments used to control water 
parameters were an oxy-meter (OxyGuard, Handy Polaris V 1.26), 

a refractometer with 0 to 100 g L
-1

 range (Zuzi, A67410) and a kit 
using the colorimetric method to determinate nitrate, ammonia and 
nitrite concentrations. The kits were obtained from AquaMerck 
(Merck KGaA, Darmstadt, Germany). During the trial, the water 

temperature (23 ± 1° C) and dissolved oxygen (7 ± 0.5 mg L
-1

) were 

measured daily. Salinity (33 ± 1 g L
-1

), pH (7.3 ± 0.5), NH4
+
 (0.0 mg 

L
-1

), NO2
-
 (0.34 ± 0.2 mg L

-1
) and NO3

-
 (46.1 ± 3.7 mg L

-1
) were 

measured three times a week. Photoperiod was natural throughout 
the experimental period, and all tanks had similar lighting 
conditions. 
 
 
Fish and experimental design 
 
The fish were transported to the experimental facilities of 
Polytechnic University of Valencia from a commercial hatchery 
localized in France. The fish were acclimated to the experimental 
conditions and fed a commercial diet (47% of crude protein (CP), 
20% of crude lipid (CL), 5.8% Ash and 1.5% crude fibre (CF), 

 
 
 
 

 
Skretting, Spain.  

A group of 800 fishes, 165 g in mean weight, were distributed in 
8 tanks; two replicates per treatment were randomly selected. The 
experiment finished when fish doubled the initial weight. All fishes 
were weighed every 5 to 6 weeks, approximately. Previously, fish 

were anaesthetised with 30 mg L
−1

 of clove oil (Guinama
®

, 
Valencia, Spain) containing 87% of eugenol. The fishes were not 
fed for 24 h before weighing.  

The trial lasted 107 days (from December 2009 to March 2010). 
At the beginning, 16 fishes per tank and the end 10 fishes per tank, 
were slaughtered by a thermoshock in a melting ice bath, to 
determine body composition and biometric parameters and were 
stored at -30°C to determine proximate and amino acid body 
composition. 

 

Diets and feeding 
 
Four isoproteic (50% CP) and isolipidic diets (17% Cl) were 
formulated using commercial ingredients (Table 1), in which 
defatted SB was included at 0, 15, 30 and 45% (Table 2). Diets 
were prepared by cooking-extrusion processing with a semi-
industrial twin-screw extruder (CLEXTRAL BC-45, St. Etienne, 
France). Processing conditions were as follows: 100 rpm speed 
screw, 110°C temperature, 30 to 40 atm pressure and 3 and 6 mm 
diameter pellets, according to fish size. Each experimental diet was 
tested in duplicate tanks. Fishes were fed by hand twice a day to 
apparent satiation from Monday to Saturday. Pellets were 
distributed slowly, allowing all fishes to eat. 

 

Proximate composition and amino acid analysis 
 
Chemical analyses of the dietary ingredients were determined prior 
to diet formulation. Diets and their ingredients as well as the whole 
fishes were analysed according to AOAC (1990) procedures: Dry 
matter (105°C to constant weight), ash (incinerated at 550°C to 
constant weight), crude protein (N × 6.25) by the Kjeldahl method 
after an acid digestion (Kjeltec 2300 Auto Analyser, Tecator 
Höganas, Sweden), crude lipid extracted with methyl-ether (Soxtec 
1043 extraction unit, Tecator) and crude fibre by acid and basic 
digestion (Fibertec System M., 1020 Hot Estractor, Tecator). All 
analyses were performed in triplicate.  

The amino acid content in diets and whole body were determined 
after acid hydrolysis with HCL 6N at 110°C for 23 h. as previously 
described Bosch et al. (2006), through a Waters (Milford, MA, USA) 
HPLC system consisting of two pumps (Mod. 515, Waters), an 
autosampler (Mod. 717, Waters), a fluorescence detector (Mod. 
474, Waters) and a temperature control module. Aminobutyric acid 
was added as internal standard after hydrolysation. The amino 
acids were derivatised with AQC (6-aminoquinolyl-N-
hydroxysuccinimidyl carbamate) and separated with a C-18 
reverse-phase column Waters Acc. Tag (150 mm × 3.9 mm). 
Methionine and Cystine were determined separately as methionine 
sulphone and cysteic acid respectively after performic acid 
oxidation followed by acid hydrolysis. 

 

Economic analysis 
 
The price of each diet was determined by multiplying the respective 
contributions of each feed ingredient by their respective costs per kg 
and summing the values obtained for all the ingredients in each of the 
formulated diets. The used raw material prices were the average prices 
in FAO GLOBEFISH (January, 2010), Instituto Técnico y de Gestión 
Ganadero, S.A and “Mercados Agroalimentarios” (Official FOB prices). 

The price of each ingredient (January, 2011) was: Fish meal=1.38 € kg
-

1
; Defatted soybean meal= 



3 

 

  
 
 

 
Table 1. Proximate composition of ingredients used in experimental diets.  

 
 Ingredient Fish meal, herring Wheat Soybean meal 

 International Feed Nº (5-02-000) (4-05-268) (5-04-604) 

 Dry matter (%) 91.9 87.7 89.35 

 Crude protein (% DM) 72.4 10.6 45.28 

 Crude lipid (% DM) 9.6 1.5 1.61 

 Crude fibre (% DM) 0.3 4.2 5.6 

 Ash (% DM) 15.8 1.6 7.7 

 NFE (% DM)
*
 1.9 82.1 39.81 

 
*NFE was calculated as = 100 - %CP - %CL - %Ash - %CF. 

 

 

0.321 € kg
-1

; Wheat meal=0.154 € kg
-1

; Fish oil=0.780 € kg
-1

; Vit-

Min Mix=7.50 € kg
-1

.  
The Economic Conversion Ratio (ECR) was used to evaluate the 

diets from an economic point of view and it was calculated following 
the expression: 
 
ECR (€ kg

-1
 fish) = feed conversion ratio (kg diet kg

-1
fish) × price of 

diet (€ kg
-1

diet)] 

 

Statistical analysis 
 
Growth data and nutritive parameters were treated using multifactor 
analysis of variance (ANOVA), introducing the initial live weight as 
covariate (Snedecor and Cochran, 1971). Newman-Keuls test was 
used to assess specific differences among diets at a significance 
levels of P < 0.05 significance levels (Statgraphics, Statistical 
Graphics System, Version Plus 5.1, Herndon, Virginia, USA).  

Quadratic regression analyses were applied, where specific 
growth rate (SGR) and feed conversion ratio (FCR) were a function 
of soybean meal (SB) dietary level using the expression: 
 

Y=a + b(SB) + c(SB)
2
 

 
Optimum soybean meal dietary level was obtained by deriving this 
equation and equalising to zero. All experiments were carried out 
according to the rules or protocols of the Animal Welfare 
Commission at the Polytechnic University of Valencia. 
 

 

RESULTS 
 
The composition of test diets including dry matter, CP, 
CL, ash and gross energy (GE) was similar (Table 2). 
The essential amino acid (EAA) profiles of the diets were 
variable (Table 2), Arg, His, Met, Phe and Thr decreased 
according to SB increased in the diets and the opposite 
trend was observed in the Iso and Leu content. The Lys 
content was similar in all diet. In relation to non essential 
amino acids (NEAA), the dietary content of Asp and Glu 
were increased according to dietary level of SB. The 
relation EAA/NEAA also diminished with dietary soybean 
meal level until 0.86.  

No significant difference was observed in final survival 
(that it was around 84% ± 10.61). The meagre did not 

present adaptation problems nor exhibit stress behaviour. 
At the end of the trial,  a  significant  effect  of  soybean 

 
 

 

meal inclusion was observed on fish growth (Table 3). 
Meagre fed diets 15 and 30 obtained the highest final 
weight (380 and 385 g, respectively). The final weight of 
fish fed diet 45 was also higher (360 g), than fish fed diet 
0 (333 g). Likewise, fish fed diet 15 and 30 obtained 
significantly higher Thermal Growth Coefficient (TGC) 

(3.10 × 10
-3

 and 3.15 × 10
-3

, respectively) than fish fed 

45 diet (2.87 × 10
-3

) and fish fed the 0 diet that obtained 

the lowest TGC (2.56 × 10
-3

).  
Regarding nutritional parameters, the daily feed intake, 

the feed conversion rate (FCR) and the protein efficiency 
(PER) ratio were not different for all the diets (Table 3).  

With the aim to determining the SB dietary levels that 
maximize the fish growth, a second-order polynomial 
regression analysis was assessed and the equation that 
describes the relationship between TGC and the dietary 
SB level is expressed in Figure 1. Based on the above 
polynomial equation, the point maximum of this quadratic 
curve is the dietary SB level to maximize the TGC (26.4% 
SB). Likewise, Figure 1 shows the second-polynomial 
regression between FCR and dietary level SB and the SB 
level that obtain the minimum FCR resulted 27.6% SB.  

Biometric parameters and body composition were not 
affected by experimental diets (Table 4). Significant 
differences were not observed in whole body 
composition. The energy retention (GEE) results are 
similar in all tested diets with values between 24 and 
25.7%. Neither, significant differences were observed 
among diets in the efficiency of protein (CPE), between 
27.6 and 30.6%. 

The ingestion of essential amino acids (expressed as g 

AA × 100g
-1

 of fish and day) did not showed significant 
differences with the diets (Figure 2). Overall, the Met 

intake was the lowest (from 0.8 to 1.24 g AA × 100g
-1

 of 
fish and day) followed by the His intake (from 1.9 to 2.1g 

AA × 100g
-1

 of fish and day) and the Lys and Leu intake 
were higher than the others amino acids intake (upper to 

3 g AA × 100g
-1

 of fish and day in the four experimental 
diets). Figure 3 shows the retention efficiency (%) of 
essential amino acids of fishes fed with the experimental 
diets at the end of the experiment. The His was the 
amino acids with the lowest retention efficiency (25% of 
average) and the Thr presented the highest retention 



4 

 

 
 
 

 
Table 2. Formula and proximate composition of the 
experimental diets.  

 
 

Ingredients (g kg
−1

) 
 Diet  

 

 0 15 30 45  

  
 

 Fish meal, herring (5-02-000) 660 576 493 407 
 

 Soybean meal (5-04-604) 0 150 300 450 
 

 Wheat (4-05-268) 216 144 70 0 
 

 Fish oil (7-08-048) 104 110 117 123 
 

 Vitamin–mineral Mix 20 20 20 20 
 

 Analysed composition (% dry weight)    
 

 Dry matter 91.9 91.31 90.09 90.41 
 

 Crude protein (%CP) 50.43 50.13 50 50.98 
 

 Crude lipid (%CL) 17.78 17.94 18.09 17.42 
 

 Ash (%) 11.17 11.22 10.95 10.55 
 

 Crude fibre (%CF) 1.11 1.62 2.12 2.64 
 

 Calculated values     
 

 NFE 
*
 19.51 19.09 18.84 18.41 

 

 GE (MJ kg
−1

) 
†
 22.57 22.48 22.34 22.36 

 

 CP/GE (g MJ
−1

) 22.35 22.3 22.38 22.8 
 

 Essential amino acid content calculated (g 100
-1

g)  
 

 Arginine 4.19 4.13 4.07 4.00 
 

 Histidine 1.82 1.75 1.68 1.61 
 

 Isoleucine 2.43 2.44 2.45 2.46 
 

 Leucine 3.90 3.92 3.94 3.95 
 

 Lysine 3.00 3.00 3.01 3.00 
 

 Methionine 1.10 1.04 0.99 0.92 
 

 Phenylalanine 3.38 3.29 3.21 3.11 
 

 Threonine 2.45 2.39 2.33 2.27 
 

 Valine 2.66 2.65 2.64 2.62 
 

 Non essential amino acid content calculated (g 100
-1

 g) 
 

 Alanine 3.03 2.94 2.84 2.74 
 

 Aspartate 4.31 4.59 4.87 5.14 
 

 Cystine 0.73 0.72 0.71 0.69 
 

 Glutamine 6.66 7.09 7.51 7.93 
 

 Glycine 3.65 3.48 3.31 3.13 
 

 Proline 4.93 4.60 4.27 3.92 
 

 Serine 2.09 2.14 2.20 2.25 
 

 Tyrosine 2.41 2.28 2.16 2.03 
 

 EAA/NEAA 0.90 0.88 0.87 0.86 
  

*NFE  calculated:  100-%CP-%CL-%Ash-%CF.  
†
GE:  Gross energy: 

Calculated using: 23.9 kJ g
−1

 proteins, 39.8 kJ g
−1

 lipids and 17.6 kJ 

g
−1

 carbohydrates. 
 
 
(around of 35%) following by Arg (34%) and Lys and 
Met32%). There were no significant differences of amino 
acids efficiency retention among diets. Ratio between dietary 
EAA level of experimental diets and EAA in the carcass was 

calculated (expressed as %EAAdiet/%EAAfish) and the 

results are shown in Figure 5. The His presented the upper 
value of this ratio (upper to 130%), and Arg, Lys, Met and 
Thr presented the ratio below to 100%. No differences were 

observed in ratio %EAAdiet/%EAAfish in relation to diets, with 

a exception of Met that presented 

 
 
 
 

 

the lowest ratio in diet 30 and 45 and the highest in the 0 
diet.  

Regarding to economic analyses of the diets, the cost 
of diets was reduced with the increase of soybean meal 
in diets (Table 5). Significant differences were showed in 
the economic conversion ratio (ECR) that was higher in 
control diet (diet 0) than in the others diets. 
 

 

DISCUSSION 

 

The results of this present trial show that the meagre 

exhibits a high growth, with TGC around 3.00 ×10
-3

, greater 

than other marine species such as gilthead sea bream with 

TGC average of 1.72 ×10
-3

 (Mayer et al., 2008) and others 

scianids as Argyrosomus japonicus (Pirozzi et al., 2009) 

feed with commercials diets (1.46 × 10
-3

). Likewise the TGC 

in present trial were also higher that TGC recalculated by 
the growth results obtained by Calderón et al. (1997) with A. 

regius feeding with pelletized diets (2.02 × 10
-3

), Estevez et 

al. (2010) feeding A. regius with experimental diet with 

extruded commercial diet (1.73 × 10
-3

) and by El-Shebly et 

al. (2007) (1.78 × 10
-3

) with feed based in tilapia and 

shrimp. The diets with 15 or 30% of SB obtained the best 

final weight and TGC (385 g and 3.15 × 10
-3

, respectively) 

but the optimum soybean inclusion in diets for A. regius was 
27% for both, growth and feed conversion. Figure 4 shows 
the TGC obtained in this experiment compared with different 
marine species that were feeding with different levels of 
plant proteins in diets. Despite the fact that knowledge of 
meagre nutrition is limited there are a few feeding studies in 
fishes of the scianids family. The studies made by Wang et 
al. (2006b) recommended soybean meal dietary level below 
10% (40% of fish meal substitution) in diets for cuneate 
drum, since exceeding this level produced a detriment in the 
fish growth. Higher levels of dietary soybean meal were 
recommended for other scianids as Sciaenops ocelatus, for 
example McGoogan and Gatlin III (1997) obtained a good 
growth results when soybean meal was included at 66% in 
diets and in the same species, Reigh and Ellis (1992) also 
observed that the 70% of soybean meal dietary inclusion did 
not affected negatively to fish growth. Regarding to replaces 
fish meal with a vegetable protein mixtures, Estevez et al. 
(2010) fed A. regius with four experimental diets with two 
inclusion levels (42 and 52%, those represented the 315 
and 38% of total protein of diets) of mixture plant protein 
(soy cake, corn gluten, soy protein concentrate and 
sunflower cake) with or without fish protein hydrolysates and 
observed that the fish growth was significantly reduced by 
the inclusion of plant protein, although the growth of fish fed 
diets with 42% of plant protein dietary inclusion obtained 
similar growth to fish fed control diet. The quadratic 
regression analysis was recommended by Shearer (2000) 
because it was used to obtain optimum levels of ingredients 
or nutrients 



5 

 

  
 
 

 
Table 3. Main performances of meagre fed increasing levels of dietary soybean meal.  

 

Parameter 
  Diet   

 

0 15 30 45 SEM 
 

 
   

Initial weight (g)  
Final weight (g) 

TGC × 10
-3 *

  
FI (% day

-1
) 

†
 

FCR‡ 

PER
§
 

  
164 166 166 165 3.84 

333
c
 380

a
 385

a
 360

b
 1.2 

2.56
c
 3.10

a
 3.15

a
 2.87

b
 0.144 

0.79 0.90 0.95 0.89 0.03 

1.30 1.34 1.43 1.45 0.05 

1.53 1.49 1.40 1.36 0.05  
  

Means of duplicate groups. Data on the same row not sharing a common superscript letter are significantly 
different different (P < 0.05). SEM: Pooled standard error of the mean. Initial weight was considered as 

covariable for final weight and TGC. *TGC = 1000 x [Final weight (g) 
1/3

− Initial weight (g)
1/3

] /(T°−minimum 

T° to feed). 
†
Feed intake (g100 g fish

-1
day

-1
) FI = 100 × feed consumption (g)/ average biomass (g) × days.  

‡
Feed conversion ratio, FCR = feed offered (g)/ weight gain (g). 

§
Protein efficiency ratio, PER = Weight gain 

(g)/protein offered (g). 
 

 

2.5 
TGC = 2.53x10

-3
+ 4.95544x10

-5
xSB-9,37562x10

-7
xSB

2 26.42 
3.5 

 

r
2
 = 86.91 Optimun SB level 

 

   TGC x 10
-3 

 

FCR    
 

   3 
 

2    
 

   2.5 
 

1.5   
2  

   
 

   FCR 
 

 FCR = 1,93(± 0.19)-0,04 (±0.02)xSB + 72.74x10
-5

 (±43.42x10
-5

) xSB
2 27.64 

TGC  

 r
2
 = 81.66 % Optimun SB level 

 

1   1.5 
 

   
  

 
1 

 
0.5 

 
0.5 

 
 

0                      0 
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 

 
Figure 1. Optimum dietary soybean meal level for TGC and FCR depending on dietary soybean meal obtaining by 
quadratic regression. 

 

 

(Martínez-Llorens et al., 2009; Sánchez et al., 2007). 
According to the polynomial regression showed that the 
dietary soybean meal obtained for a maximum growth 
was 26.4%. Similar results were reported in other marine 
species, such as gilthead sea bream that recommended 
between 20.5% (Martínez-Llorens et al., 2009) and 
30.5% (Martínez-Llorens et al., 2007) of dietary soybean 
meal level for maximum growth, and likewise Tomás et 
al. (2005) recommended from 20 to 30% of defatted 
soybean meal dietary inclusion for maximum growth of 
Seriola dumerili. Chou et al. (2004) for juvenile cobia 
(Rachycentron canadum) estimated by quadratic 
regression a growth optimum at 16.9% replacement of 
fish meal protein by soybean meal protein.  

Although daily feed intake, FCR,  and  PER  do not 

 
 

 

statistically differ between diets, they do not appear so 
close. Daily feed intake of diet 0, in particular, is 13% 
lower than the value recorded for diets 15 and 45, and 
17% lower than diet 30. To provide evidence that the 
may be caused by the nutrient imbalances besides to 
palatability properties of plant proteins.  

In relation to biometric parameters, no effect of diet 
was observed and similar indexes were obtained by Poli 
et al. (2003); 1.04 condition factor, 44% fillets, 6% VSI, 
but the mesenteric fat obtained in present trial (2.4%) 
were higher than the obtained by Poli et al. (2003), and 
the cause of this differences probably could be to that 
meagres in this present experiment not formed gonad. 
There was not significant effect on the whole body 
composition of meagre by the experimental diets and 



6 

 

 
 
 

 
Table 4. Biometric indices and proximate composition (expressed as percentage of wet weight) of A. regius 
fed increasing levels of soybean meal.  

 
 

Parameter 
  Diet   

 

 

0 15 30 45 SEM 
 

  
 

 CF 
*
 1.11 1.18 1.17 1.16 0.02 

 

 VSI (%)
†
 6.12 5.77 5.49 6.02 0.24 

 

 HSI (%)
‡
 1.96 1.6 1.58 1.61 0.11 

 

 MF (%)
§
 2.43 2.53 2.33 2.48 0.16 

 

 DP (%)
¶
 70.33 70.9 70.56 69.17 0.84 

 

 MI (%)
||
 58.76 60.75 58.39 59.39 1.44 

 

 Moisture (%) 74.05 72.62 71.8 71.9 0.55 
 

 Crude Protein (% ww) 17.37 17.95 18.6 17.37 0.37 
 

 Crude Lipid (% ww) 6.5 6.63 6.81 7.64 0.25 
 

 Ash (% ww) 2.45 2.65 3.12 2.57 0.19 
 

 CPE (%)** 29.7 30.4 30.6 27.6 1.83 
 

 GEE (%)
††

 24.0 24.8 25.4 25.7 1.33 
 

 
The data are the mean (n=10) ± SEM. Data in the same row with different superscripts differ at P < 0.05. *Condition 

factor CF = 100 × total weight (g)/total length
3
 (cm). 

†
Viscerosomatic index (%) VSI = 100 x visceral weight (g)/ Fish 

weight (g). 
‡
Hepatosomatic index (%) HIS = 100 × liver weight (g) / Fish weight (g). §Mesenteric fat (%) MF = 100 x 

mesenteric fat weight (g)/fishweight (g). ¶Dressout percentage (%) DP = 100 × [total fish weight (g)-visceral weight  
(g)-head weight (g)]/ fish weight (g). ||Meat index (%) MI = 100 x meat weight (g)/fish weight (g). **Crude protein 

efficiency (%) CPE = Fish protein gain (g) × 100/ protein intake (g). 
††

Gross energy efficiency (%) GEE = Fish energy 
gain (kJ) × 100/energy intake (kJ). 

 
 

 

  Arg 
 

 3.5  
 

Val 
3.0 

His 
 

 
 

 2.5  
 

 2.0  
 

 1.5  
 

 1.0  
 

Thr 
0.5 

Ile 
 

  
 

 0.0 
0  

  
 

  15 
 

  30 
 

  45 
 

Phe  Leu 
  

 
 
 
 

 

Met Lys 
 

Figure 2. Ingestion of essential amino acids (EAA) in each experimental diet expressed as g 

per 100 g
-1

 of fish and day. Each value is the mean of duplicate groups. Different superscripts 
indicated differ at P < 0.05. 



7 

 

   
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 
Figure 3. Retention efficiency (%) of essential amino acids in A. regius fed with the experimental diets at the end of the experiment. Each 
value is the mean of duplicate groups. Different superscripts indicated differ at P < 0.05. Retention of ingested protein (%) = Fish amino 
acid gain (g)/ ingested amino acids (g) × 100. 

 

 
Table 5. Global results of economic parameters at the end of the experiment.  

 

Parameter 
  Diet   

 

0 15 30 S45 SEM 
 

 
 

Cost of diet (€ kg 
-1

)* 1.18 1.10 1.03 0.95  
 

ECR (€ kg 
-1

) 
†
 2.31

b
 1.50

a
 1.55

a
 1.47

a
 0.06 

 

 
Data in the same row with different superscripts differ at P < 0.05. *Calculated from price of 

ingredients: Fish meal=1.38 € kg
−1

; Soybean meal=0.32 € kg
−1

; Wheat= 0.154 € kg
−1

; Fish 

oil=0.78 € kg
−1

; Vit–Min–AA Mix=7.5 € kg
−1

. 
†
 ECR (€ kg

−1
 fish) = feed conversion ratio (kg diet 

kg
−1

fish)*price of diet (€ kg
−1

 diet). 
 

 

approximately content was 72% of humidity, 17% of CP 
and 7% of lipids. These results demonstrate the excellent 
meat quality that presents the meagre, being the main 
characteristic its lower fat content, representing an 
important parameter of quality for the consumer (Poli et 
al., 2003).  

The detriment of growth in 45 diet could be to several 
factors as the presence of anti nutritional factors in plant 
proteins (Francis et al., 2001; Gatlin III et al., 2007), that 
various effects can also caused the activities reduces of 
alkaline phosphatase and aminopeptidase in meagre 
(Estevez et al., 2010). In addition, the growth could be 
affected by the amino acid deficiencies of diets (Gomez-
Requeni et al., 2004; Peres et al., 2003; Refstie et al., 
2006; Wang et al., 2006b). Following this reasoning, the 
information about amino acids requirements for meagre is 
not available. Nevertheless, a first approach about the 

 
 

 

excess or defect of EAA could be done by estimating 
amino acid retention, which has been carried out in other 
fish species (Peres and Oliva-Teles 2009; Sánchez-
Lozano et al., 2010). In this present experiment, no 
significant effect in amino acid retentions was observed 
with the different diets, but great differences can be 
observed among amino acids, Arg, Lys, Met and Thr 
presented the highest retention and the His the lowest. 
The amino acid efficiency retention and amino acid intake 
is closely related and the reason of the high retention 
was due to the low amino acid intake, if this one is made 
below its requirements. Ratio between EAA profile of 
diets and whole body (Figure 5) could be a good tool to 
estimate the deficiencies as Sánche-Lozano et al. (2009, 
2010) have shown in the sea bream, so, that if this 
relation is less than 100% this amino acid would be 
deficient and if it is greater than 100% it would be in 



8 

 

 
 
 

 

A.regius Sparus aurata N. miichthioides Sciaenops ocellatus 1 Sciaenops ocellatus 2 Seriola dumerili  
 
 
 
 
 
 
 
 
 

T
G

C
 x

 1
0

-3
 

  
3.5  
 

 

3 
 

 

2.5   
 

 

2  
 

 

1.5  
 

 

1  
 

 

0.5 
 

 
0    
0 10 20 30 40 50 60 70 80  

Dietary level (%) 
 

Figure 4. TGC of A. regius in the present trial, compared, Sparus aurata (Martínez-Llorens et al., 2009), N. miichthioides (Wang 
et al., 2006), Sciaenops ocellatus 1 (McGoogan and Gatlin III, 1997), Sciaenops ocellatus 2 (Reigh and Ellis, 1992) and Seriola 
dumerili (Tomás et al., 2005). 

 
 
 
   140             

 

  
6 130       

0 
 

20 40 
 

60  

            
 

  5,5   
ab a           

 

            

a 
   

 

  5 120 b           
 

            

b 
   

 

  
4,5   b           

 

            

b 
   

 

  
4 110 

          0 
 

          b    
 

%EAA              

15 
 

g DAA 
 3,5

diet
 %EAAfish    

a  ab 
     c   

 

 
3 100 

 a 
ab 

       30 
 

100 g fish day  ab         45  

      

b 
      

 

  2,5    ab b    
a 

     
 

  

a 
     

ab 
      

             
 

          

b 
   

 

  2 90      bc  
c 

   
 

  
1,5 

ab ab b            
 

               
 

                
 

  1 80         a    
 

  0,5            
a 

  
 

                
 

  0 70             
 

               
 

   HIS  ARG THR VAL 
Leu 

MET 
Lys 

LYS ILE LEU PHE 
 

     Arg His Ile    Met Phe Thr Val 
 

         Aminoacids     
 

 Figure 5. Ratio between essential amino acids profile of experimental diets and whole body fish expressed as g per 100 g
-1

 of 
 

 protein. Each value is the mean of duplicate groups.  Different superscripts indicated differ at P < 0.05.  
  



9 

 

 
 
 

 

excess. Arg, Lys and Thr were deficient in diets and 
therefore the efficiency retention of these amino acids 
was high. Met was significant different among diets and 
fish fed diet 0 (100% of fish meal) presented the highest  
relation between %EAAdiet/%EAAfish and for reason Met 
efficiency retention increased with soybean meal dietary  
level. In summary, it is necessary to determine the amino 
acids requirement of meagre because, even in the diet 
with the 100% of fish meal, there are amino acids that 
could be deficient, such as Arg, Lys and Thr. From an 
economic point of view, it was clearly improved the ECR 
when fish meal was substituted for soybean meal in the 
diet.  

Then, if the growth and body indices show that diets 15 
and 30% were quite similar, although the cost of the diets 
is not significantly different, the best diet must be 
considered the diet 30 Reigh and Ellis (1992) 
recommended up to 70% of dietary soybean meal for a 
growth of Sciaenops ocelatus, but observed that the 
35.5% soybean level (50% of dietary protein from 
soybean meal) was the most cost-effective diet. The 
soybean meal level for minimum ECR (optimum ECR) in 
diets for Seriola dumerili (Tomás et al., 2005) resulted 
around 20.5% and similar results (Martínez-Llorens et al., 
2007) were obtained for gilthead sea bream (22%). 
 

 

Conclusion 

 

The results obtained in this present trial showed that 30% 
SB inclusion could be an excellent plant meal to 
substitute 25% of fish meal dietary, because no effects on 
growth and feed efficiency parameters were detected and 
in addition improve the profitability of diets. 
 

 

ACKNOWLEDGEMENT 

 

This research was supported by grants from the Planes 
Nacionales de Acuicultura (JACUMAR) in Spain. 
 

 
REFERENCES 
 
Association of official Analytical Chemists, AOAC. (1990). Official 

Methods of Analysis, 15th end. Association of Official Analytical 
Chemists, Arlington, VA, USA. pp. 1298.  

Bosch L, Alegria A, Farré R (2006). Application of the 6-aminoquinolyl-
N-hydroxysuccinimidyl carbamate (AQC), reagent to the RP-HPLC 
determination of amino acids in infant foods. J. Chromatogr. B 
831:176–183.  

Calderón JA, Esteban JC., Carrascosa MA, Ruiz PL, Valera F (1997). 
Estabulación y crecimiento en cautividad de un lote de reproductores 
de corvina (Argyrosomus regius). Actas del VI Congreso Nacional de 
Acuicultura, Cartagena, Spain:365–370.  

Chatzifotis S, Panagiotidou M, Papaioannou N, Pavlidis M, Nengas I, 
Mylonas C (2010). Effect of dietary lipid levels on growth, feed 
utilization, body composition and serum metabolites of meagre 
(Argyrosomus regius) juveniles. Aquaculture 307:65–70.  

Chou RL, Her BY, Su MS, Hwang G, Wu YH, Chen HY (2004). 
Substituting fish meal with soybean meal in diets of juvenile cobia 
Rachycentron canadum. Aquaculture 229:325–333. 

  
  

 
 

 
El-Shebly A, El-Kady MAH, Hussin A, Yeamin Hossain MD (2007). 

Preliminary observations on the pond culture of meagre Argyrosomus 
regius (Asso, 1801) (Sciaenidae) in Egypt. J. Fisheries. Aquatic. Sci. 
2(5):345–352.  

Estévez A, Treviño L, Kotzamanis Y, Karacostas I, Tort L, Gisbert E 
(2010). Effects of different levels of plant proteins on the ongrowing 
of meagre (Argyrosomus regius) juveniles at low temperatures. 
Aquacult. Nutr. 17:e572–e582.  

Francis G, Makkar H, Becker K (2001). Antinutritional factors present in 
plant-derived alternate fish feed ingredients and their effects in fish. 
Aquaculture 199:197–227.  

Gatlin III, D, Barrows F, Bronwn P, Dabrowski K, Gaylord T, Hardy R, 

Herman E, Hu G, Krogdahl A, Nelson R, Overturf K, Rust M, Sealey 
W, Skonberg D, Souza E, Stone D, Wilson R, Wurtele E (2007). 
Expanding the utilization of sustainable plant products in aquafeeds: 
a review. Aquacult. Res. 38:551–579.  

Gómez-Requeni P, Mingarro M, Calduch-Giner J, Médale F, Martin S, 
Houlihan DF, Kaushik S, Pérez-Sánchez J (2004). Protein growth 
performance, amino acid utilisation and somatotropic axis 
responsiveness to fish meal replacement by plant protein sources in 
gilthead sea bream (Sparus aurata). Aquaculture 232:493–510.  

Hernández M, Martínez F, Jover M, García B (2007). Effects of partial 
replacement of fish meal by soybean meal in sharpsnout seabream 
(Diplodus puntazzo) diet. Aquaculture 263:159–167.  

Jiménez MT, Pastor E, Grau A, Alconchel JI, Sánchez R, Cárdenas S 
(2005). Revisión del cultivo de esciénidos en el mundo, con especial 
atención a la corvina Argyrosomus regius (Asso, 1801). Boletín 
Instituto Español de Oceanografía. 21(1-4):169–175.  

Martínez-Llorens S, Moñino AV, Tomás A, Pla M, Jover M (2007). 
Soybean meal as partial dietary replacement for fish meal in gilthead 
sea bream (Sparus aurata) diets: effects on growth, nutritive 
efficiency and body composition. Aquacult. Res. 38:82–90.  

Martínez-Llorens S, Tomás A, Jauralde I, Pla M, Jover M (2009). 
Optimun dietary soybean meal level for maximizing growth and 
nutrient utilization of on-growing gilthead sea bream (Sparus aurata). 
Aquacult. Nutr.15:320–328.  

Mayer P, Estruch V, Blasco J, Jover M (2008). Predicting the growth of 
gilthead sea bream (Sparus aurata L.) farmed in marine cages under 
real production conditions using temperature- and time-dependent 
models. Aquacult. Res. 39:1046–1052.  

McGoogan B, Gatlin III D (1997). Effects of replacing fish meal with 
soybean meal in diets for red drum Sciaenops ocelltus and potential 
for palatability enhancement. J. World Aquacult. Soc. 28:374–385.  

Murray H, Lall S, Rajaselvam R, Boutilier L, Blanchard B, Flight R, 
Colombo S, Mohindra S, Douglas S (2010). A nutrigenomic analysis 
of intestinal response to partial soybean meal replacement in diets for 
juvenile Atlantic halibut, Hippoglossus hippoglossus, L. Aquacult. 
298: 282–293.  

Peres H, Lim C, Klesius P (2003). Nutritional value of heattreated 
soybean meal for channel catfish (Ictalurus punctatus). Aquacult. 
225: 67–82.  

Peres H, Oliva-Teles A (2009). The optimum dietary essential amino 
acids profile for gilthead seabream (Sparus aurata) juveniles. 
Aquaculture 296:81–86.  

Pirozzi I, Booth M, Pankhurst P (2009). The effect of stocking density 
and repeated handling on the growth of juvenile mulloway, 
Argyrosomus japonicus (Temminck, Schlegel 1843). Aquacult. Int. 
17:199–205.  

Poli B, Parisi G, Zampacavallo G, Iurzan F, Mecatti M, Lupi P, Bonelli A 
(2003). Preliminary results on quality changes in reared meagre 
(Argyrosomus regius): body and fillet traits and freshness changes in 
refrigerated commercial-size fish. Aquacult. Int. 11:301–311.  
Refstie  S,  Landsverk  T,  Bakke-McKellep  A,  Ringo  E,  Sundby  A, 

Shearer  K,    Krogdahl  A  (2006).  Digestive  capacity,  intestinal 
morphology,  and  microflora of  1-year  and  2-year  old  Atlantic  cod 

(Gadus  morhua)  fed  standard  or  bioprocessed  soybean  meal.  
Aquaculture 261:269–284.  

Reigh R, Ellis S (1992). Effects of dietary soybean and fish-protein 
ratios on growth and body composition of red drum (Sciaenops 
ocellatus) fed isonitrogenous diets. Aquaculture 104:279–292.  

Roo J, Hernández-Cruz C, Borrero C, Schuchardt D, Fernández-
Palacios H (2010). Effect of larval density and feeding 



10 

 

 
 
 

 
sequence on meagre (Argyrosomus regius; Asso, 1801) larval 
rearing. Aquaculture 302:82–88.  

Sánchez N, Tomás A, Martínez-Llorens S, Nogales S, Blanco J., 
Moñino A, Pla M, Jover M (2007). Growth and economic profit of 
gilthead sea bream (Sparus aurata, L.) fed sunflower meal. 
Aquaculture 272:528–534. 

Sánchez-Lozano N, Martínez-Llorens S, Tomás-Vidal A, Jover Cerdá M 
(2009). Effect of high-level fish meal replacement by pea and rice 
concentrate protein on growth, nutrient utilization and fillet quality in 
gilthead seabream (Sparus aurata, L.). Aquaculture 298:83–89.  

Sánchez-Lozano N, Martínez-Llorens S, Tomás-Vidal A, Jover Cerdá M 
(2010). Amino acid retention of gilthead sea bream (Sparus aurata, 
L.) fed with pea protein concentrate. Aquacult. Nutr. 17:e604–e614.  

Shearer K (2000). Experimental design, statistical analysis and 
modelling of dietary nutrient requirement studies for fish: a critical 
review. Aquacult. Nutr. 6:91–102.  

Snedecor G, Cochran W (1971). Statistical methods. The lowa State 
University Press Ames. lowa, USA. p. 593.  

Tibaldi E, Hakim Y, Uni Z, Tulli F, De Francesco M, Luzzana U, Harpaz 
S (2006). Effects of the partial substitution of dietary fish meal by 
differently processed soybean meals on growth performance, nutrient 
digestibility and activity of intestinal brush border enzymes in the 
European sea bass (Dicentrarchus labrax). Aquaculture 261:182– 
193. 

 
 
 
 

 
Tomás A, De La Gándara F, García-Gomez A, Pérez L, Jover M 

(2005). Utilization of soybean meal as an alternative protein source in 
the Mediterranean yellowtail, Seriola dumerili. Aquacult. Nutr. 11:333-
340.  

Wang Y, Guo J, Bureau D, Cui Z (2006a). Replacement of fish meal by 
rendered animal protein ingredients in feeds for cuneate drum (Nibea 
miichthioides). Aquaculture 252:476–483.  

Wang Y, Kong L, Li C, Bureau D (2006b). Effect of replacing fish meal 
with soybean meal on growth, feed utilization and carcass 
composition of cuneate drum (Nibea miichthioides). Aquaculture 
261:1307–1313.  

Zhou Q, Mai K, Tan B, Liu Y (2005). Partial replacement of fishmeal by 
soybean meal in diets for juvenile cobia (Rachycentron canadum). 
Aquacult. Nutr. 11:175–182. 


