Aquacult Int (2009) 17:507–521 DOI 10.1007/s10499-008-9220-8
Growth performance, feed utilization, and body composition of Nile tilapia (Oreochromis niloticus L.) fed with differently heated soybean-meal-based diets Mohamed Salah Azaza Æ Wassim Kammoun Æ Abdelwaheb Abdelmouleh Æ Mohamed Mejdeddine Kraı¨em
Received: 8 February 2008 / Accepted: 8 September 2008 / Published online: 25 September 2008 Ó Springer Science+Business Media B.V. 2008
Abstract This study was undertaken in order to determine the effect of feeding heattreated, defatted soybean meal (SBM) on growth, feed utilization, and body composition of Nile tilapia (Oreochromis niloticus). A control diet (SBM0) of 378 g kg-1 crude protein with 18.4 kJ g-1 gross energy was formulated, and three diets identical to the basal diet were autoclaved for 10, 20, or 30 min. The autoclaved diets were named SBM10, SBM20, and SBM30, respectively. Each diet treatment was applied to triplicate groups of 30 fish (2.45 ± 0.03 g) per tank (120 l). The fish were hand fed to satiation four times daily for 45 days. At the end of the feeding trial the fish fed with the SBM30 diet had significantly (P \ 0.05) higher weight gain and protein efficiency ratio than those fed with the other diets. No feed-related mortality was observed during the whole experimental period. Heating SBM for 30 min reduced trypsin inhibitor activity (TIA) and increased apparent protein digestibility (APD), and indicated significant differences (P \ 0.05) among various treatments. No significant differences were found in carcass moisture, lipid, and ash of fish fed with different experimental diets. An increase in the body protein content of fish fed with diet SBM30 was significantly (P \ 0.05) higher than in all other experimental groups. The results of this study seem to indicate that autoclaving the SBM for 30 min improved its nutritional value in practical feeds for Nile tilapia fingerlings. Keywords Heat treatment Soybean meal Trypsin inhibitor Growth performance Digestibility Oreochromis niloticus Abbreviations SBM Soybean meal TIA Trypsin inhibitor activity APD Apparent protein digestibility ANFs Anti-nutritional factors HSI Hepatosomatic index FCR Feed conversion ratio M. S. Azaza (&) W. Kammoun A. Abdelmouleh M. M. Kraı¨em National Institute of Marine Sciences and Technologies, 2025 Salammbo, Tunisia e-mail:
[email protected]
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MS 222 FM MM NFE GE CMC PDI NSI SGR BWG FCR FI PER SR ESM IBW FBW SR RGW
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Tricaine methane sulfonate Fish meal Maize meal Nitrogen free extract Gross energy Carboxymethylcellulose Protein dispersibility index Nitrogen solubility index Specific growth rate Body weight gain per day Feed conversion ratio Feed intake Protein efficiency ratio Survival rate Standard error of means Initial body weight Final body weight Survival rates Relative growth weight
Introduction From 1995 to 2005, total aquaculture production increased by an average of 7.3% annually, and total production is expected to increase dramatically at least until 2015 (FAO 2007). Fishmeal is a major dietary ingredient used in compounded aquafeeds. In 2006, the aquaculture sector consumed about 3.06 million tonnes of fishmeal (Tacon et al. 2006). However, world fish meal production is not expected to increase further (Tacon 2007). Therefore, in order to develop sustainable, economical, and viable aquaculture production, alternate sources of high-quality proteins must be identified to replace unavailable highcost fish meal. Soybean protein is one of the most promising plant proteins identified as a fish meal substitute and its production has continued to increase over the past 25 years (Biswas et al. 2007). Numerous studies on the utilization of soybean meal (SBM) as partial or complete replacement for fishmeal in fish feeds have been conducted during recent decades for many commercially important fish species such as rainbow trout (Heikkinen et al. 2006; Escaffre et al. 2007; Barrows et al. 2007), sharptooth catfish, (Imorou Toko et al. 2007), Nile tilapia (Azaza et al. 2005; Fasakin et al. 2005), Atlantic salmon (Refstie et al. 2000, 2005), European and Asian seabass (Tantikitti et al. 2005; Tibaldi et al. 2006), Indian carp (Jose et al. 2006), and some new candidate species for aquaculture, for example yellowtail (Tomas et al. 2005), sole (Bonaldo et al. 2006), cuneate drum (Wang et al. 2006), and sharpsnout sea bream (Herna´ndez et al. 2007). The main limitations in the use of SBM are attributed to the low level of methionine and the presence of anti-nutritional factors (ANFs). SBM is known to contain several ANFs, for example protease inhibitors, lectins, phytic acid, saponins, phytoestrogens, antivitamins, and allergens (Francis et al. 2001). It is well documented that ANFs in a diet of raw or inadequately heated soybean meal adversely affect various animals (Hoffmann et al. 2003; Machado et al. 2008) including fish (Viola et al. 1983; Peres et al. 2003; Barrows et al.
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2007). It has also been demonstrated that adequately heated SBM has the potential to improve its nutritive value (Peres et al. 2003), the digestibility of nutrients (Haard et al. 1996; Arndt et al. 1999), feed conversion efficiency and growth (Abel et al. 1980; Balogun and Ologhobo 1989), and reproductive performance of fish (Adewumi 2006; Adewumi et al. 2006). Thus, heat treatments denaturing the inhibitor protein are used to make soybean suitable for feeding fish. However, overheated SBM is undesirable because this may reduce the availability of protein, reduce protein digestibility or cause loss of essential amino acids (Plakas et al. 1988; Deng et al. 2005). Thus, careful control of heating conditions is required to optimise the nutritive value of this ingredient. Nile Tilapia, Oreochromis niloticus, has often been regarded as an excellent fish species for culture in many parts of the world, where compound feeds constitute significant portions of the operating cost. SBM is the most commonly used feedstuff in feeds for omnivorous fish species such as tilapia and catfish (Lovell 1988; NRC 1993). Optimum use of this material for fish nutrition can, however, be achieved only after destruction of the growth inhibitor content by heat treatment for a suitable time. No studies have yet examined the effects of heat treatment of defatted SBM on the growth performance of tilapia. Therefore, the first objective of this study was to examine the growth performance, feed utilization efficiency, and body composition of Nile tilapia fingerlings fed on diets containing differently heated defatted SBM. The second objective was to evaluate whether different chemical tests on diets with high soybean meal content could be used to predict their nutritive values and subsequent expected growth performance of Nile tilapia.
Materials and methods Fish and experimental conditions Three hundred and sixty five-week-old uniform-sized fish (2.45 ± 0.03 g; ±SE, n = 360) were obtained from brood stock held at the National Institute of Marine Sciences and Technologies (INSTM), Fish-culture Research Station, Bechima-Gabes, Tunisia. Fry were removed gently from the mouths of females and were maintained in a 1.5 m3 tank until they reached a body weight of approximately 2–3 g. Fish were randomly stocked in 12 batches of 30 fish each, in 120-l cylindroconical fibreglass tanks. Three replicate tanks per dietary treatment were used. Each tank was part of an open circulated system with a common water reservoir. The tanks were supplied with water from a geothermal source after undergoing a cooling in a large storage tank. In all 15 tanks, water was constantly equally replaced by continuous flow at a rate of 2–4 l min-1 tank-1. A photoperiod of a 12-h light, 12-h dark cycle was provided. In addition, the tanks were siphoned daily, before the first feeding, to remove faecal material, and they were thoroughly scrubbed and completely flushed fortnightly, when fish were removed for weighing. Fish were acclimatized to experimental conditions for 10 days prior to the feeding trial during which they received a control diet (SBM0). Within this period, all dead or apparently stressed fish were replaced with animals of similar sizes. At the beginning of the experimental feeding trial, each diet was assigned randomly to three tanks. The fish were hand fed to apparent satiation (i.e., until the first feed item was refused) four times daily (08:00, 11:00, 14:00 and 17:00 h). Daily feed consumption was obtained for each tank by weighing the feed at the start and end of each day. To avoid excess feeding, food was
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offered with great care by giving small amounts of food at a time to ensure that fish ate all the food particles offered. The feed particle size was 1.5 mm in the first period of the trial; pellets were crumbled and sieved to furnish particles with graded diameters which were used according to fish size. To monitor growth and general health condition, all fish in each tank were individually weighed at two-week intervals during the 45-day trial, after being anaesthetized with tricaine methane sulfonate (MS 222) (50 mg l-1). Dead fish were removed every day from each rearing tank and weighed to calculate feed conversion ratio (FCR). At the beginning of the feeding trial, a pooled sample of 21 fish was randomly collected to serve as an initial carcass sample. At the end of the trials, seven fish were randomly collected from each tank (n = 21, for each treatment diet) for final carcass analysis. Sampled fish were killed by lowering the body temperature in a freezer, homogenized, stored in sealed polyethylene bags, and frozen (-20°C) for subsequent whole-body composition analyses. The livers of 30 other fish randomly taken from each treatment were removed, weighed individually, and used to calculate hepatosomatic index (HSI). For water quality control, temperature and dissolved oxygen were measured daily using a combined digital oxythermometer (WTW/OXI 96), and analyses of total nitrite and nitrate were performed on a weekly basis to ensure that water quality remained well within the limits recommended for Nile tilapia culture. Water-quality data were not significantly different among the experimental tanks, ranging from 29.1 to 30.6°C, 4.4 to 6.2 mg l-1, 0.004 to 0.01 mg l-1, and 0.01–0.6 mg l-1, for temperature, dissolved oxygen, nitrite (NO2-N), and total ammonia-N (NH3-N ? NH4?-N), respectively. Feed formulation and pellet preparation The diets contained local marine fish meal (FM), soybean meal (SBM), and maize meal (MM). All ingredients were ground to a fine powder using a laboratory hammer mill and sieved to pass through a 0.25-mm sieve. FM, SBM, and MM were obtained from commercial suppliers. Prior to feed formulation, proximate compositions of these ingredients were determined (Table 1). On the basis of the nutrient composition of the ingredients (Table 1), a practical feed (380 g kg-1 crude protein and 18.5 kJ g-1 gross energy) which had previously been demonstrated to support good growth performance was formulated according to Azaza et al. (2005) and served as a control diet (SBM0). Three other experimental diets were prepared. They were identical to the control diet, except that the SBM was completely replaced by SBM autoclaved for 10, 20, or 30 min. In the rest of the text, these are termed as SBM10, SBM20, and SBM30. Control diet (SBM0) represented the diet compounded with non-heat-treated soybean meal. Heat treatment of SBM was performed by placing the meal in an oven, already at 110°C and 1.05 kg cm-2; trays contained SBM 4 cm deep. All dietary ingredients were ground and mixed with vitamin–mineral premix and soybean oil in a food mixer (model CAM A30). Water was added gradually until a desirable paste-like consistency was reached then the mix was pelleted through 2.5 mm holes in a kitchen meat grinder (model amb TC22SL) and sun-dried. The dry pieces of feed were then stored in a freezer at -20°C, in polythene bags, until required. Before feeding, the dried diets were crushed and graded to furnish suitable particle sizes. Diet samples were subjected to proximate composition analysis, the results of which are presented in Table 2.
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Aquacult Int (2009) 17:507–521 Table 1 Proximate composition (g kg-1 dry matter basis) and essential amino acid profile of feed ingredients included in test dietsa
511
DSBM
Means of two replicate samples
b
Nitrogen-free extract: 1 - (% lipid ? % moisture ? % protein ? % fibre ? % ash)
c
Calculated using the factors: carbohydrates, 4.1 kcal g-1; protein, 5.5 kcal g-1 and lipids, 9.1 kcal g-1(New 1987), and transformed to kJ using the factor 4.184 d
Essential amino acids
862.2
Dry matter (in original matter)
889.6
914.7
Crude protein
435.0
472.1
78.4
Crude lipid
13.8
16.2
14.3
Crude fibre
66.0
09.5
65.9
Ash
58.0
281.4
13.2
316.8
135.5
689.4
Gross energy (kJ g-1)c
a
MM
Nutrient contents
NFEb
DSBM, defatted soybean meal; FM, fishmeal; MM, maize meal
FM
15.89
13.80
Calcium
0.3
06.3
14.17 0.03
Phosphorus
0.7
3.9
0.2
Lysine
27.9
50.5
1.7
Valine
14.1
39.1
3.0
Leucine
35.3
46.2
8.0
Histidine
9.8
14.8
1.7
Arginine
34.8
31.5
3.0
Threonine
16.8
33.2
2.0
EAAd
Isoleucine
16.1
21.1
2.5
Methionine ? cysteine
10.8
23.1
2.8
6.9
9.1
0.6
18.3
27.3
5.8
Tryptophan Phenylalanine
Digestibility measurements For digestibility measurements, the same four experimental diets were tested following the growth trial. Fish were fed the same four experimental diets as in the growth trial except that 0.5% chromic oxide (Cr2O3) was added to each diet as an inert marker. Fish were fed according to the feeding schedule for the growth trial for 3 days before any samples were collected. The apparent digestibility coefficients of crude protein (ADCcrude protein) and dry matter (ADCdry matter) were measured in the diets using an indirect method. Faeces were collected 10 h after the first feeding using the dissection method described by Ferna´ndez et al. (1996). After collection, faecal samples were lyophilized, finely ground, and frozen at -20°C until analysis. Faeces collected from 15 fishes from each tank were pooled into one sample per tank. Apparent digestibility of test diets was calculated by use of the formulae: ADCDry matter ð%Þ ¼ 100ð1 ð% Cr2 O3 in diet=% Cr2 O3 in faecesÞÞ: ADCNutrient ð%Þ ¼ 100ð1 ðð% Cr2 O3 in dietÞð% nutrient in faecesÞ= ð% Cr2 O3 in faecesÞð% nutrient in dietÞÞ: Chemical analysis Crude protein (N-Kjeldahl method, with 6.25 nitrogen to protein conversion factor), total lipids (extraction by Soxhlet method), crude fibre (extraction with H2SO4 and NaOH), dry
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Aquacult Int (2009) 17:507–521 Composition and proximate analysis of the experimental diets
Ingredient (g kg-1)
Experimental diets SBM0
SBM10
SBM20
SBM30
Fish meal
240
240
240
240
Non-heated SBM
500
–
–
–
SBM heated for 10 min
–
500
–
–
SBM heated for 20 min
–
–
500
–
SBM heated for 30 min
–
–
–
500
Maize meal
200
200
200
200
Soybean oil
40
40
40
40
CMC (binder)a
10
10
10
10
Vitamin–mineral mixb
5
5
5
5
Chromic oxide
5
5
5
5
Proximate analyses (g kg-1 dry matter) Moisture Crude protein
87.5
106.7
98.5
94.1
378.1
364.9
366.8
375.3
Crude lipid
57.8
61.1
65.7
61.8
Crude fibre
66.6
70.9
58.4
68.9
Ash
41.6
56.0
44.4
60.9
431.4
403.4
429.2
402.0
18.7
18.0
18.5
18.3
Lysine
26.1
24.8
26.5
22.9
Valine
16.5
18.3
15.0
16.2
Leucine
29.4
27.1
25.8
28.6
Histidine
9.1
11.2
8.9
10.3
Arginine
24.2
22.9
25.0
23.1
Threonine
15.9
13.1
14.4
15.3
Isoleucine
13.5
11.2
13.7
12.9
Methionine ? cysteine
10.7
9.4
11.3
10.1
Carbohydrate (by difference) Gross energy (kJ g-1) EAA (g kg-1diet)
Tryptophan Phenylalanine
4.4
3.3
6.1
5.3
17.0
19.3
17.6
18.7
a
CMC = carboxymethylcellulose
b
Vitamin premix and mineral premix were described in Azaza et al. (2008)
matter (oven drying at 105°C, 24 h), and ash (muffle furnace, oven incineration at 550°C, 24 h) analyses were performed on the individual dietary ingredients and diets, and at the beginning and end of the experiment on experimental fish, using standard AOAC (1990) methodology. Samples were analysed in triplicate. Gross energy (GE) was calculated on the basis of the conversion factors: carbohydrate (as NFE) 4.1 kcal g-1, protein 5.5 kcal g-1, and fat 9.1 kcal g-1 (New 1987). The amino acid content of ingredients and experimental diets was determined using a Beckman amino acid analyser (Beckman 3600 Fullerton, CA, USA) after acid hydrolysis (6 N HCl, 110°C, 24 h). Tryptophan was determined colorimetrically after hydrolyzing samples in NaOH (4.2 N NaOH) (Basha and
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513
Roberts 1977). The chromic oxide content of the feed and faecal samples was estimated in triplicate by the method of Furukawa and Tsukahara (1966) using the acid-digestion technique (nitric acid and perchloric acid). Diets were analysed for trypsin inhibitor activity (TIA) by the enzymatic method, with Na-benzoyl-DL-arginine-p-nitroanilide (D,L-BApNA) as enzyme substrate, according to Hammerstrand et al. (1981). Trypsin inhibitor activity is expressed as trypsin units inhibited (TIU). One trypsin unit is arbitrarily defined as an increase of 0.01 absorbance units at 400 nm per 10 ml of the reaction mixture under the experimental conditions. Protein dispersibility index (PDI) and nitrogen solubility index (NSI) were determined for each experimental diet using AOCS (1983) methodology (American Oil Chemists Society, Official Methods Ba 10–65 and Ba 11–65, respectively). Evaluation of growth parameters Growth-performance indicators measured were the specific growth rate (SGR, % weight day-1), body weight gain per day (BWG, g day-1), feed conversion ratio (FCR), feed intake (FI, g day-1), protein efficiency ratio (PER), and survival rate (SR). These indicators were calculated as: SGR = 100 (Ln (final body weight) - Ln (initial body weight))/time (days); FCR = dry feed intake (g)/wet weight gain (g); PER = wet weight gain (g)/protein intake (g); percent survival (%) = (Final fish number/initial fish number) 9 100. Statistical analysis All data were subjected to a one-way analysis of variance (ANOVA) using the general linear model of Statistica Version 5.1 (Statsoft, Tulsa, USA). When the ANOVA identified differences among groups, multiple comparisons among means were tested using Duncan’s multiple-range tests (DMRT). Tank mean values were considered units of observation for statistical tests, and mean values were considered significantly different when P \ 0.05. Values throughout the text are expressed as mean ± standard error of means for three replicates (ESM, n = 3) unless otherwise specified.
Results Feed quality The formulation and chemical composition of experimental diets are given in Table 2. In each experimental diet, data on the essential amino acid composition were adequate to meet the amino acid requirements of tilapia. Compared with untreated SBM-based diet, the essential amino acid content of diets was not negatively affected by heat treatments of SBM under our conditions. Autoclaving SBM for 30 min significantly decreased the TIA, PDI, and NSI values from 3.91 TIU mg-1, 69.39%, and 67.12% to 0.17 TIU mg-1, 22.51%, and 19.94%, respectively, suggesting improvement of soybean meal quality (Table 3).
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Table 3 TIA and ADCs of protein and dry matter of experimental diets containing defatted soybean meal heated for different time periods Experimental diets
TIA (TIU mg-1)
PDI (%)
NSI (%)
ADCs (%) Protein
SBM0 SBM10 SBM20 SBM30
Dry matter
3.91 ± 1.31a
69.39 ± 1.11a
67.12 ± 1.94a
82.29 ± 2.33a
69.98 ± 1.67a
a
b
b
a
68.03 ± 0.95a
a
71.12 ± 1.22b
b
75.96 ± 1.08c
3.93 ± 2.66
b
3.14 ± 1.54
c
0.17 ± 0.01
57.97 ± 0.94
c
48.54 ± 1.67
d
22.51 ± 1.21
51.44 ± 0.83
c
36.78 ± 1.22
d
19.94 ± 1.08
84.06 ± 1.14 85.86 ± 2.49 92.38 ± 1.55
TIU per mg of sample, one trypsin unit is defined as an increase in absorption of 0.01 at 400 nm Values are mean ± SEM. Means in the same column with different superscripts were significantly different (DMRT, P \ 0.05)
Growth performance and diet utilization efficiency Growth rates and diet utilization of Nile tilapia fingerlings are summarized in Fig. 1 and Tables 3 and 4. There was no feed rejection during the experiment, and the acceptability of the diets seemed similar. Fish mortality was recorded in all replicates of the treatments; no feedrelated mortality was observed during the entire period of the experiment (45 days). TIA in the experimental diets decreased with an increase in the duration of heat treatment of SBM. Fish fed with the control diet, containing the unheated soybean meal, SBM10, and SBM20 diets grew at a significantly slower rate than fish fed with the diet containing SBM autoclaved for 30 min. The SGR and PER values reflected a similar pattern. Fish fed different diets consumed similar amounts of food. By contrast FCR was significantly improved for fish fed with 30-min-autoclaved SBM based diet and similar trends to those for growth response described above were observed; fish fed with the SBM30 diet had a FCR of 1.32 compared with 1.61 and 1.63 for the fish fed with diets SBM0 and SBM10, respectively. Both protein and dry matter digestibilities were the highest in the SBM30 diet group and were the lowest in the unheated SBM-based diet group (Table 4). Whole-body composition Carcass proximate composition values of the fish at the beginning and end of the 45-day experimental period are shown in Table 5. No significant differences were found in the whole-body composition of fingerlings of Nile tilapia either between dietary treatments or between initial and final fish, except for the protein content of fish fed the SBM30 diet, which was significantly (P \ 0.05) higher than in other groups. There were no significant (P [ 0.05) differences among HSI across treatments (Table 5).
Discussion It is well known that for efficient use of dietary ingredients by fish, optimum utilization of energy-yielding nutrients from feed ingredients is essential. Most anti-nutrients can be
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515 40
Fig. 1 Growth curve responses of O. niloticus fed experimental diets for 45 days
SBM0 SBM10
35
SBM20 Mean body weight (g)
30
SBM30
25 20 15 10 5 0 0
15
30
45
Experimental period (days) Growth performance of O. niloticus fed with experimental diets
Table 4 Variables
Experimental diets SBM0
IBW (g) FBW (g)
SBM10 2.51 ± 0.06a
2.47 ± 0.10a
2.49 ± 0.03a
a
a
a
31.43 ± 0.91b
a
91.33 ± 5.42a
a
0.73 ± 0.07b
a
5.90 ± 0.14b
a
1.32 ± 0.04b
a
1.65 ± 0.08b
a
35.39 ± 0.37a
a
90.00 ± 5.24 -1
-1
DWG (g d fish ) -1
SGR (% day ) -1
FCR (g g )
a
0.53 ± 0.06
a
5.22 ± 0.09
a
1.61 ± 0.15
a
PER
1.20 ± 0.04 -1
FI (g day )
SBM30
2.56 ± 0.08a 26.77 ± 1.54
SR (%)
SBM20
a
35.57 ± 0.72
24.89 ± 0.89
a
90.66 ± 6.23
a
0.50 ± 0.08
a
5.09 ± 0.14
a
1.63 ± 0.08
a
1.25 ± 0.18
a
32.67 ± 0.41
26.12 ± 1.13 91.33 ± 5.42 0.52 ± 0.03 5.24 ± 0.10 1.58 ± 0.11 1.24 ± 0.13
34.56 ± 0.25
Data are mean ± SEM of three replicates (n = 3 tanks per diet) IBW, initial body weight; FBW, final body weight; SR, survival rates; DWG, daily weight gain; SGR, specific growth rate; FCR, feed conversion ratio; PER, protein efficiency ratio; FI, feed intake Means within a row having different superscripts were significantly different (DMRT, P \ 0.05)
reduced by physical, chemical, or biochemical treatments, for example inactivation of trypsin inhibitor by heat, reduction of carbohydrate content by methanol extraction, or hydrolysis of phytic acid by phytase. For economic reasons, conventional, heat-treated SBM remains the major soy product in fish feeds (Storebakken et al. 2000). Currently, different soy products obtained by various processing techniques are commercially available. The effectiveness of these products as protein sources for fish depends on the extraction and processing techniques (Kaushik 2007). This paper is the first detailed attempt to investigate the effect of autoclaving defatted SBM in Nile tilapia diets, in which heating SBM for 30 min is recommended before it is
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Table 5 Effect of dietary treatments on the body (whole fish) composition (g kg-1 fresh weight basis) of O. niloticus fingerlings Component (g kg-1)
Initial fish
Final (fish fed diet) SBM10
SBM0 Moisture Crude protein Crude fat Ash
SBM20
SBM30
780.5
730.6 ± 2.64a
731.4 ± 1.56a
728.9 ± 2.39a
726.3 ± 2.74a
136.1
a
a
a
158.2 ± 1.71b
a
86.6 ± 1.79a
a
26.4 ± 1.96a
a
1.44 ± 0.39a
44.2 35.9
HSI
147.3 ± 1.45
a
88.8 ± 2.07
a
31.2 ± 1.91
a
1.51 ± 0.62
144.9 ± 1.19
a
91.6 ± 2.10
a
27.5 ± 1.41
a
1.49 ± 0.83
146.7 ± 2.22 87.5 ± 1.61 32.5 ± 1.49 1.42 ± 0.72
Values are mean ± SEM of three replicates (n = 3 tanks per diet), except for HSI, for which values are mean ± SE (n = 30 fish per treatment) Means in the same row followed by the same superscript letter are not significantly different (DMRT, P [ 0.05) HSI, hepatosomatic index
suitable for use. In this study, the maximum heating time (30 min) was chosen after a preliminary study (unpublished data) in which it was established that heating SBM for 40 min had a negative effect on the amino acid content. In this experiment, feed was offered to visual satiety and there was no significant difference in feed intake among fish fed with others diets. However, this did not result in similar growth performance. Growth rate of fish fed with diet SBM30 was significantly faster than for fish fed with other diets. It thus appears that the growth-limiting effect of insufficiently treated soybean meal based diet was not because of feed palatability, measured by voluntary feed intake. This indicates the presence of a factor, or factors, in the untreated and/or inadequately treated SBM, not present in the adequately processed (autoclaved) SBM, which inhibited growth. The most commonly known and studied antinutritional factors are the inhibitors of protease enzymes, trypsin and chymotrypsin. These inhibitors, known as trypsin inhibitors, can be destroyed by proper heat treatment (Grant 1989). The presence of high levels of these substances in the control, SBM10 and SBM20 diets compared with the SBM30 diet, as shown in Table 3, may contribute to the growth depression noted in this study. Because the particle sizes, moisture content, and temperature used to heat the soybean portions used for compounding the experimental diets were similar throughout the study, the extent to which TIA will be destroyed by heat could only be a function of duration of heating (Carter and Hauler 2000). The different growth performance observed between treatments could be attributed to heating times of soybean component of the diets, which probably correlated with the levels of the inactivated trypsin inhibitor. Growth rates and PER values improved as the TIA of the experimental diets decreased to tolerable levels and the maximum values were achievable only when at least 88% of the TIA was destroyed. In this trial, the growth performance of fingerlings Nile tilapia followed the same pattern, by diet, as the protein digestibility values. Furthermore, linear regression analysis including protein digestibility data and TIA contents revealed approximately 81% (weight gain = 0.72 (CUDprotein) - 37.34; r2 = 0.810; P \ 0.001) and 93% (weight gain = -1.92 (TIA) ? 30.50; r2 = 0.933; P \ 0.001) of variability in total weight gain of Nile tilapia can be explained by the actual digestible protein and TIA contents, respectively. It has been reported that TIA levels of 1.6 mg g-1 or higher in the diet retarded the growth of Nile tilapia, but the fish tolerated and grew well at dietary levels of 0.6 mg TI g-1
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diet (Wee and Shu 1989). Juvenile channel catfish (Ictalurus panctatus) showed the best growth performance when the TIA level of the diet was 2.2 mg g-1 (Wilson and Poe 1985). It seems that below the 2 mg g-1 mark, most cultured fish are able to compensate for the presence of trypsin inhibitor by increasing trypsin production. Krogdahl et al. (1994) observed that rainbow trout were able to partly compensate for TIA action by increasing enzyme secretion and enhancing absorption of protein in the distal parts of the intestine. Rumsey (1991) found little effect on growth or feed intake at TIA levels below 2.0 mg g-1 when feeding rainbow trout at levels of TIA ranging from 1.6 to 51.0 mg g-1. The discrepancy among results regarding the tolerability of ANFs in SBM-based diet for fish may be related to the quality and processing of SBM, variation in diet formulation, and differences in fish size and culture system. Furthermore, fish species can have different tolerance limits to the presence of antinutrients (Francis et al. 2001). In a comparative study on Nile tilapia O. niloticus, gilthead seabream Sparus aurata, and African sole Solea senegalensis, the last had the greatest resistance of sole to protease inhibitors in defatted SBM (Moyano Lopez et al. 1999). A second comparative study between Atlantic salmon and rainbow trout (Refstie et al. 2000) suggested that rainbow trout has a higher tolerance for SBM ‘‘agents’’ causing histopathological changes in the intestinal mucosa than Atlantic salmon, indicating the existence of species-specific differences even within the same family. It has been demonstrated that dietary incorporation of proper-heated SBM improved the growth performance, feed intake, feed efficiency, and reproductive performance of most aquaculture species, namely common carp (Viola et al. 1983), Indian carp (Maity and Patra 2002), channel catfish (Peres et al. 2003; Adewumi 2006), rainbow trout (Olli and Krogdahl 1994), and Atlantic salmon (Olli et al. 1994). Insufficient heating of SBM led to incomplete destruction of trypsin inhibitor and, in turn, to poor growth performance of fish. However, heat treatment can add considerable cost to processing and reduce the availability of other nutrients (Kratzer et al. 1990). Thus, this heating process should be kept to a minimum and carefully regulated to minimise the loss of nutritional quality of the feed material; overheated meals are undesirable because overheating may damage proteins and reduce protein digestibility and amino acid availability. Viola et al. (1983) and Plakas et al. (1988) concluded that slightly overheated soybean meal may have inadequate lysine levels, because of availability associated with the Maillard reaction. The optimum heating of SBM for carp was reported to be about 30–90 min at 105°C (Viola et al. 1983). Deng et al. (2005) demonstrated that lysine availability decreased in white sturgeon (Acipenser transmontanus) in feeds heated excessively. Faldet et al. (1992) determined that the total amount of lysine diminishes when soybean seed is cooked at temperatures between 120 and 160°C. Overheating can also lead to racemization of amino acids, with loss in biological activity when the biologically active L-form is converted into the inactive D-form (Hurrell 1984). The data on apparent digestibility in this study confirm the need for heat treatment of SBM to increase protein digestibility, as has been reported for salmonids (Haard et al. 1996; Arndt et al. 1999). It seems that after heating SBM over 30 min the protein portion available for assimilation by the fish increases, which may have contributed to higher protein content in the carcass (Table 5). The adverse effect of dietary incorporation of inadequately heated SBM on digestibility has been attributed mainly to the insoluble complexes formed by trypsin inhibitor and the proteolytic enzymes trypsin and chymotrypsin (Francis et al. 2001). PDI has been demonstrated to be a simple and effective procedure for assessment of the quality of heat-treated soybeans (Hsu and Satter 1995). The nitrogen solubility index is a
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slight modification of the PDI procedure (AOCS 1983), and is used frequently in the foodprocessing industry (Kahn et al. 2003; Zhang and Liu 2005). PDI values of the complete diets in the current study ranged from 22.51% to 69.39%. Barrows et al. (2007) demonstrated that PDI and NSI values of 13.1% and 12.4%, respectively, indicate optimum heating of SBM for rainbow trout. Batal et al. (2000) reported that values less than 45% indicate adequate heat treatment of soybeans for chickens. PDI values reported in this study, however, were not as low as those reported to be optimum by Wang et al. (2004). This may be because of differences in the source of soybeans used in the two studies. Qin et al. (1998) found that the PDI values of Argentinean soybeans responded to time of steam exposure and temperature differently from soybeans of Chinese origin. These authors concluded that soybeans of different origin required different processing conditions to optimize protein properties. Because there were significant effects of SBM heat-treatment time both on chemical indicators (for example TIA, PDI, and NSI) and on biological indicators (for example growth performance, feed utilization efficiency, and digestibility), we can conclude that, under the conditions of this study, TIA, PDI, and NSI are good indicators for providing further insight into nutrient bioavailability and for ascertaining tolerability to certain soyANFs in various fish species. Before it is suitable for use in fish feeds, heat treatment of SBM (autoclaving for 30 min) is recommended as a means of reducing the amount of trypsin inhibitors below the critical levels and of improving growth performance and feed efficiency. Further extensive research is needed on ANFs other than trypsin inhibitors which have been identified as major anti-nutrient factors in SBM, in particular phytic acid, which has the ability to reduce the availability of several minerals and other feed nutrients, and non-starch polysaccharides (NSPs), that restrict the nutritive value of SBM. Acknowledgements The authors thank Elebdelli Kamel and Kalboussi Samir for their excellent technical assistance.
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