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Effects of partial and complete replacement of fish meal protein with a soya protein on growth performance of black-chinned tilapia Sarotherodon melanotheron (Rüppell 1852) in tank culture

A R Koumi, B C Atsé*, K A Otchoumou** and P Kouamé 

Université d’Abobo-Adjamé Abidjan, UFR, Sciences et Technologies des Aliments (STA), 02 BP 801 Abidjan 02 (Côte d’Ivoire)

*Centre de Recherches Océanologiques (CRO), BP V 18 Abidjan (Côte d’Ivoire)
**Université de Cocody Abidjan, UFR Biosciences, 04 BP 322 Abidjan 04 (Côte d’Ivoire)

atse_boua_celestin@hotmail.com

Abstract 

A growth trial was conducted to feed juveniles black-chinned tilapia Sarotherodon melanotheron isonitrogenous diets for 6 months. Three diets containing crude protein (35 %) replacing 0 % (FD), 50 % (MD), and 100 % (SD) of the fish protein with similar percentage of soya protein were formulated. Fish were fed daily at 5 % body weight with three experimental diets.

 

After 6 months, final body weight, values of growth performance and feed utilization parameters were not significantly differed from the fish fed in all experimental diets. The highest viscerosomatic index was obtained with fish fed SD. Ash content showed a decreasing trend with an increasing soya protein level in formulated diets. An increase of the carcass protein content was observed in fish fed FD and MD. The carcass fat and energy contents of fish were high in fish fed SD.

 

These results suggest that Sarotherodon melanotheron  fed soya protein diets exhibited comparable growth with those fish fed fish protein diet. Therefore, results indicate the lower protein and higher fat contents of fish carcass were associated with soya protein diets. In add, the formulation of soya protein diet for black-chinned tilapia reduces the need of fish meal in diet.

Key words: diet utilization, proximate composition, Sarotherodon melanotheron, soybean meal


Introduction

Sarotherodon melanotheron (Rüppell 1852) is one of the major fish species that is frequently caught in West African coastal waters (Teugels and Falk 2000). Fishery statistics show that Sarotherodon melanotheron  represents 51 % of commercial catches in Lake Ayame in Ivory Coast (Gourène et al 1999). Several studies including the aquaculture potential (Legendre et al 1989), ecological studies (Koné and Teugels 1999, 2003), morphometric studies (Falk et al 2000), and use of agricultural products in growth performance (Ouattara et al 2005) were realized. These studies showed that Sarotherodon melanotheron  exhibited a good adaptation to pure freshwater conditions but presented a lower weight gain and higher feed conversion ratio with the formulated food. In other way, tilapias (Low-McConnell 2000) usually and Sarotherodon melanotheron  (Koné and Teugels 2003) especially are herbivorous fish, but most formulated feeds for tilapia are similar to those of omnivorous fishes in that they contain significant levels of animal protein such as fish meal protein (Hughes and Handwerker 1993).

 

Fish meal is an ideal protein source for fish and presents a good palatability and a high nutritional quality (El-Saidy and Gaber 2002; Siddhuraju and Becker 2003). However, the increasing cost of fish meal has restricted its use as a protein source for fry diets (Siddhuraju and Becker 2003). In other hand, the use of fish meal entrains phosphorus pollution (Bergheim et al 1984; Cho and Bureau 1997; Sugiura et al 2000) and shows instability in world fish meal production which gives the global needs for fish oil and fish meal for aquaculture (FAO 2002).

 

In this context, research efforts have been directed to identify novel alternative and economically viable protein sources to totally or partially replace fish meal in the fish feed. One of possible alternatives will be an increased use of plant proteins in fish feeds. Among the plant protein sources considered in aquaculture diets, soybean meal is the most widely used in ingredients. It has been preferentially used for replace fish meal due to its higher protein content (48 – 50 %), relatively well balanced amino acid profile, reasonable price and steady supply (NRC 1993; Storebakken et al 2000; Goda et al 2007). However, soybean meal contains approximately 30 % indigestible carbohydrates and several compounds that may disturb the digestive process (Storebakken et al 2000). So, it‘s important to study the nutritional value of combination of plant protein in order to replace fish meal in fish diets.

 

Therefore, the purpose of this study was to evaluate the growth, feed utilization, economic value, and carcass composition of black-chinned tilapia Sarotherodon melanotheron fed diets containing partial or total substitution of soya protein for the fish protein.

 

Materials and methods 

Experimental diets

 

Three experimental diets were formulated to be isonitrogenous in terms of crude protein (35 %). The proximate composition of the ingredients prior to diet formulation and those of experimental diets were given in Tables 1 and 2.


Table 1.  Proximate composition of the feed ingredients ( dry matter, %) and cost

Proximate analysis

Fish meal

Soybean meal

Cotton seed meal

Wheat bran

Corn flour

Crude protein

59.53

45.5

32.2

16.7

10.8

Crude fat

8.6

5.1

3.9

3.7

5.2

Crude ash

20.4

7.2

6.2

5.1

1.7

Crude fibre

--

4.5

18.8

9.1

3.3

Cost a (Cfa/kg)

400

170

100

50

80

aPrice in CFA pound: 100 CFA = 0.15 $ based on 2006 exchange prices in Ivory Coast



Table 2.  Formulation and proximate composition of the experimental diets

 

 

Experimental diets

FD

MD

SD

Ingredients, g/kg-1

 

 

 

Corn flour

100

100

100

Fish meal

380

190

-

Soybean meal

-

248

500

Wheat bran

340

222

120

Cottonseed meal

150

200

240

Fish oil

10

5

-

Soya oil

-

5

10

Lysine

-

5

5

Methionine

-

5

5

Vitamin and mineral premixa

20

20

20

Total

1000

1000

1000

Proximate analysis, % on dry matter basisb

 

 

Moisture

10.8

10.7

10.5

Crude protein

35.5

35.6

35.6

Total nitrogen

5.7

5.7

5.7

Crude fat

9.2

8.3

12.9

Ash

12.1

9.5

7.4

Crude fibre

8.4

8.4

8.8

Nitrogen-free extractc

23.3

27.5

24.8

Gross energy, kJg diet-1 d

15.5

15.9

17.2

Cost, CFA kg-1 e

260

225

195

aVitamin and mineral mixture each 1-kg of mixture contains: 4800 I.U. Vit A, 2400 IU cholecalciferol (vit. D), 40g Vit E, 8g Vit K, 4.0g Vit B12 , 4.0g Vit B2, 6g Vit B6, 4.0g pantothenic acid, 8.0g nicotinic acid, 400 mg folic acid, 20 mg Biotin, 200 mg Choline, 4g Copper, 0.4g Iodine, 12g Iron, 22g Manganese, 22g Zinc, 0.04g Selenium. Folic acid, 1.2 mg; niacin, 12 mg; D-calcium pantothenate , 26 mg; pyridoxine HCL, 6 mg; riboflavin, 7.2 mg; thiamine HCL, 1.2 mg; sodium chloride (NaCL, 39% Na, 61% Cl), 3077 mg; ferrous sulphate (FeSO47H2O, 20% Fe), 65 mg; manganese sulphate (MnSO4, 36% Mn), 89 mg; zinc sulphate (ZnSO4.7H2O, 40% Zn), 150mg; copper sulphate (CuSO4.5H2O, 25% Cu), 28 mg; potassium iodide (KI, 24% K, 76% I), 11 mg: Celite AW521 (acid-washed diatomaceous earth moisture-silica), 1000mg.

bValues represent the mean of three replicates.

cNitrogen-free extract = 100 – (% moisture + % protein + % fat + % fibre + % ash).

dGross energy = (22.2 x protein + 38.9 x fat + 17.2 x nitrogen-free extract).

ePrice in CFA pound: 100 CFA = 0.15 $ based on 2006 exchange prices in Ivory Coast.


Fish meal protein was replaced by soya protein on the basis of crude protein as follows: fish diet (FD) = 0 % soya protein replaced fish protein; Mixture diet (MD) = 50 % soya protein replaced fish protein; soya diet (SD) = 100 % soya protein replaced fish protein in diet. To balance for lysine and methionine, 0.5 % of each was added to soya protein diets, and 2 % premix vitamin and mineral supplemented each diet formulated. The energy values were calculated using the gross energy values for the macro nutrients (Luquet and Moreau 1989). The cost of each diet was determined by multiplying the respective contributions of each diet ingredients by their respective cost per kilogram and summing the values thus obtained for all the ingredients. The experimental diets, were dried, broken into suitable sizes and stored at -20 °C until use.

 

Experimental procedure

 

Tilapia Sarotherodon melanotheron  juveniles used in this study were obtained from culture pond of Layo Aquaculture Station (5°19’N, 4°19’W; Ivory Coast). Fish were acclimated for two weeks into tanks and fed at 5 % of their body weight with commercial diet containing 30 % - crude protein. The fish were counted and stocked at density of 40 fish per tank (10 fish m-3). Three replicate tanks were constituted for each diet. The fish were fed at ration of 5 % fresh weight three times a day (08:00, 12:00 and 17:00 hours). At the beginning of the experiment, fish were individually weighed and, for the intermediate weighing (once a month), fish were bulk weighed and ration was adjusted accordingly for the subsequent month. At the end of the experiment (180 days) all survival fish were collected and counted from each replicate. Thus individual body weight was recorded and 10 fish were removed from each replicate to chemical composition determination. After collection of chemical analyses samples, fish were sacrificed and dissected carefully to isolate and weight viscera, liver, and gonad for biometric parameters calculation. The growth parameters and nutrient utilization of experimental fish were evaluated as follows:
 

Body weight gain (%) = [(final body weight – initial body weight)/ initial weight] x 100

Specific growth rate (SGR) = (ln final body weight–ln initial body weight)/number of day

Feed conversion ratio (FCR) = dry feed intake (g) / wet weight gain (g)

Protein efficiency ratio (PER) = weight gain (g) / protein intake (g)

Energy retention (ER) = [retained carcass energy / energy intake] x 100

Daily lipid gain (DLG) = retained lipid (g) / biomass gain (kg)/ number of day

Viscerosomatic index (VSI) = 100 x [viscera weight (g)/ body weight (g)]

Hepatosomatic index (HSI) = 100 x [liver weight (g)/ body weight (g)]

Gonadosomatic index (GSI) = 100 x [gonad weight (g)/ body weight (g)]

Cost benefit analyses of the diets were performed according to El -Sayed (1990).

 

Water quality

 

During the experiment, water temperature, dissolved oxygen and pH were recorded daily in each tank. Water temperature and dissolved oxygen were measured using an Oxy meter model WTW OXI 330 and pH by using pH meter model WTW pH 90. Water quality as phosphorus, nitrate-nitrogen and nitrite-nitrogen were recorded at weekly intervals using a spectrometric method (Aminot and Chaussepied 1983).

 

Biochemical analysis

 

The approximate compositions of the feed ingredients, experimental diets and the fish carcasses were analysed using standard methods (AOAC 1995). Moisture content of each sample was determined through a hot-air oven set at 105°C for 24 hours, and ash was measured by incineration at 550°C in a muffle furnace for 24 hours. Crude protein (Nitrogen x 6.25) was determined using micro-kjeldahl method; crude fat was extracted (hexane extraction) using the soxhlet method and crude fibre was quantified by acid digestion followed by ashing the dry residue at 550°C in muffle furnace for 4 hours. The gross energy of samples was determined using the gross energy values for the macronutrients (Luquet and Moreau 1989).

 

Statistical analysis

 

All percentage and ratio values were transformed to arcsin values, and data of weight to logarithm values. Growth data (weight) and fish carcass composition were analysed by using one way analysis of variance (ANOVA). Tukey’s HSD ranking test was used to compare the differences among means. The data of growth performance were analysed by using one way ANOVA and the Duncan multiple ranking test was used to compare the differences among means. The treatment effects were considered to be significant at p ≤ 0.05.

 

Results 

Water quality

 

Water quality characteristics monitored throughout the study period are summarized in Table 3.


Table 3.  Mean water quality parameters recorded in the experiment tanks

Parameters*

Diets

FD

MD

SD

Temperature, °C

27.9 ± 2.7

27.9 ± 2.7

27.9 ± 2.9

pH

6.8 ± 0.7

6.7 ± 0.6

6.8 ± 0.7

DO, mgL-1

4.3 ± 0.3

4.3 ± 0.4

4.3 ± 0.3

NO2N, mgL-1

0.06 ± 0.02

0.05 ± 0.02

0.04 ± 0.02

NO3N, mgL-1

0.27 ± 0.02b

0.24 ± 0.02b

0.15 ± 0.01a

PO43—P, mgL-1

0.40 ± 0.22

0.38 ± 0.19

0.35 ± 0.21

*Values represent the mean of three replicates (mean ± SD). Values in the same row with different superscripts are significantly different (p ≤ 0.05).


The water temperature ranged from 25.2 to 30.8 °C, pH from 6.1 to 7.7, dissolved oxygen from 4.1 to 4.7 mgL-1, nitrite nitrogen from (NO2--N) 0.02 to 0.08 mgL-1, nitrate nitrogen from (NO3-- N) 0.15 to 0.29 mgL-1 and phosphorus (PO43--P) from 0.14 to 0.62 mgL-1. There were no significant differences in the water quality parameters among the treatments during the whole experimental period. Only nitrate nitrogen was significantly affected by the treatments (p < 0.05). The lowest values of nitrate nitrogen were recorded in tanks where fish were fed CD and SD.

 

Growth performance and feed utilization

 

Data on the growth performance and feed utilization of juveniles Sarotherodon melanotheron  are presented in Table 4.


Table 4.  Growth performance and nutrient utilization of juveniles tilapia Sarotherodon melanotheron fed with experimental diets

Parameters*

Diets

FD

MD

SD

IBW, g

12.3±0.3

11.9±0.5

11.9±0.6

FBW, g

133.8±6.3

125.5±10.6

124.3±9.9

SR, %

84.2±9.5

87.5±4.3

91.7±1.4

BWG, %

985.9±43.9

964.9±61.4

940.4±73.2

SGR, % day-1

1.3 ±0.02

1.3±0.03

1.3±0.04

FCR

2.4±0.7

2.9±0.3

2.4±0.3

PER

1.3±0.4

1.0±0.1

1.2±0.2

ER, %

24.2±0.5a

25.7±1.3a

31.8±0.7b

DLG, gkg-1day1

1.0±0.01a

1.0±0.06a

1.4±0.02b

PC, F.CFA#

580.4±24.2b

643.1±38.4b

449.1± 33.6a

PT , days kg-1

43.5±3.1

46.2±4.3

43.9±3.9

*Values are means ± SD. Values in the same row with different superscripts are significantly different (p ≤ 0.05). IBW = Initial body weight; FBW = Final body weight; SR = Survival rate; BWG = Body weight gain; SGR = Specific growth rate;

FCR = Feed conversion ratio; PER = Protein efficiency ratio; ER = Energy retention;

DLG = Daily lipid gain; PC= Cost per kg of fish produced; PT= Time per kg of fish produced.

# Price in CFA pound: 100 CFA = 0.15 $ based on 2006 exchange prices in Ivory Coast.


At the end of experiment, there were no significant differences in final body weight, survival rate, body weight gain and specific growth rate of fish fed the different experimental diets. Feed conversion and protein efficiency ratios also were not significantly affected (p ≥ 0.05) by dietary proteins substitution. However, fish fed SD showed the highest values (p ≤ 0.05) of energy retention and daily lipid gain. Data on economic performances showed that production cost were higher (p ≤ 0.05) with fish fed MD and FD (Table 4). Contrary production times of fish fed different experimental diet were not differed significantly. Concerning biometric parameters, fish fed SD had a significantly higher viscerosomatic index (VSI) compared to those of fish fed FD and MD. No significant differences (p ≥ 0.05) in hepatosomatique index (HIS) and gonadosomatic index (GSI) were observed among treatments (Table 5).


Table 5.   Viscerosomatic index (VSI), hepatosomatic index (HIS), and gonadosomatic index (GSI) of juveniles tilapia Sarotherodon melanotheron fed with experimental diets

Parameters*

Diets

FD

MD

SD

VSI

5.7±1.0a

6.5±1.0a

7.9±1.1b

HSI

2.1±0.3

1.9±0.3

2.2±0.4

GSI

0.3±0.1

0.2±0.1

0.2±0.1

*Values are means ± SD. Values in the same row with different superscripts are significantly different (p ≤ 0.05)


Carcass composition

 

The carcass proximate composition at the end of the trial for the different experimental groups was presented in Table 6.


Table 6.  Final carcass compositions of juveniles tilapia Sarotherodon melanotheron fed with experimental diets (% on dry matter basis)

 

Parameters*

Diets

FD

MD

SD

Moisture

70.1±4.3

70.1±1.5

67.3±0.8

Ash

20.0±0.5c

18.3±1.1b

16.5±0.1a

Crude protein

58.2±0.4a

58.2±0.3a

54.2±2.2b

Crude fat

16.9±0.7a

16.7±1.2a

23.2±0.2b

Gross energy (kJg-1diet)

20.2±0.04a

20.5±0.2b

22.1±0.2c

*Values are mean ± SD of triplicate analysis. Values in the same row with different superscripts are significantly different (p ≤ 0.05).


No significant differences were found in the carcass moisture of fish fed different experimental diets. In contrast, ash, protein, fat, and energy contents were significantly affected by experimental treatments (p ≤ 0.05). The carcass ash content showed a decreasing trend with increasing soya protein levels in formulated diets. It was the highest in fish fed FD, intermediate in fish fed MD and lowest in fish fed SD. An increase in the carcass protein content was observed in fish fed FD and MD, which was significantly different (p ≤ 0.05) than that observed in fish fed SD. The highest carcass fat and energy contents (p ≤ 0.05) were recorded in fish fed with SD.

 

Discussion 

During the experimental period, water temperature, pH and dissolved oxygen recorded in tank were within the recommended range for tilapia culture (Philippart and Ruwet 1982). Nitrate nitrogen in culture water significantly decrease with increased the levels of soya protein in experimental diets. This element originates mainly from fish feeds (Cho and Bureau 1997). In added, discharge of any element depends on fish growth and the level of the respective element in the diet. The higher levels of nitrate nitrogen obtain in the culture pond when fish fed FD was probably due to the protein content of FD which was above the requirement of this fish. This indicates that excess dietary protein, even though originating from a quality protein source (FM), led to a higher N discharge (Jahan et al 2003).

 

Feeding trials revealed that as much as 100 % of fish protein could be replaced by soya protein supplemented with vitamin and mineral premix without repercussion on Sarotherodon melanotheron  growth performance. As suggested by Watanabe et al (1987), the proper utilization of dietary protein is dependent on the good quality or amino acids balance of the protein sources. The main protein sources used in the experimental diets were from both fish meal and soybean origins. Generally adding high percentages of plant products in fish diets can cause reduced palatability and acceptability, leading to diminish the growth performance and feed utilisation (Watanabe et al 1993, Riche and Garling 2004). Contrary, in this study, the sources and the levels of dietary protein appeared to be relatively unimportant when considering similar results for growth performance values (FBW, BWG, SGR) and feed utilization parameters ( FCR, PER) recorded among fish fed with different diets. A similar result in tilapia (Oreochromis niloticus x Oreochromis aureus) was observed by Shiau et al (1987) when fish were fed diets containing soybean meal protein in substitution with fish meal protein. The present findings also support those of Goda et al (2007) who observed comparable growth and feed utilization of Sarotherodon galilaeus fed soybean meal diet with those fish meal based diet. Since Sarotherodon melanotheron  is herbivorous fish (Koné and Teugels 2003), this could explain the good digestibility, palatability and availability of soybean meal base diets. The feed conversion ratio varying from 2.37 to 2.97 in all experimental groups were found to be good. For Morissens et al (1987), values of FCR inferior to 3.5 is considered to be good for growth. In other studies, good growth and better feed utilization were recorded when Sarotherodon melanotheron  was rearing in extensive culture system “Acadjas-Enclos” with natural periphyton food (Hem et al 1994). Furthermore, culture of Sarotherodon melanotheron  in fertilising pond with these formulated diets (FD, MD and SD) containing 35 % protein could improve perfectly the growth of this fish.

 

Diets were formulated to be least costly and it is apparent that considerable reduction in fish meal level can be achieved without compromising the fish performance. Supplementing soya protein based diets entrained diminution of the diet cost which explains lower values of cost for kg fish production obtained with fish fed SD. Also lower production cost could attributable to the higher level of survival rate obtain in this group.

 

For proximate composition, we observed a significant decrease in ash carcass content with increasing levels of fish meal replacement. The fish meal had high levels of minerals including phosphorus associated with the bone fraction (Sugiura et al 2000), which were highly available and retained for Sarotherodon melanotheron . Our results on ash are similar to those of Chong et al (2003) in Symphysodon aequifasciata and Goda et al (2007) in Sarotherodon galileus. Also total replacement of fish protein by soya protein entrains a decrease of fish carcass protein. Brown et al (1997) had reported a decrease in protein body content of hybrid Morone saxatilis x Morone  chrysops fed diets containing high levels of soybean meal. Similar trend had also been reported by Watanabe and Pongmaneerat (1993) in rainbow trout. However, we observed a significant increase in carcass fat content with increasing levels of soybean meal in diets. This consequently resulted in a similar increase in carcass energy content. Our result of carcass fat is similar to those obtained by Lee et al (2002) with juvenile Ayu Plecoglossus altivelis. Cissé (1996) also showed that the lipid retention was directly associated with dietary fat level in Sarotherodon melanotheron . Nonetheless, these values were correlated with energy retention, daily lipid gain, and viscerosomatic index in the respective dietary group. The high fat and energy retention values in this group, clearly suggest that there were increased lipogenesis with increasing levels of fish meal replacements (Kaushik et al 2004). In add the higher VSI values obtained with fish fed SD may be due to the relatively high lipid deposition in viscera.

 

Conclusions

 

Acknowledgments 

The authors thank the staff of Biochemistry and Food Sciences Laboratory (LaBSA) of University of Cocody (Ivory Coast) for helpful technical assistance. Furthermore, the authors express also their sincere thank to the staff of Layo Aquaculture Station for its assistance concerning growth trials and samplings monitoring. This study is a part of the Oceanology Research Center project and was financed by Ivorian government.

 

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Received 19 March 2008; Accepted 16 April 2008; Published 5 December 2008

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