Replacement of fish meal with poultry by-product meal in diets formulated for the humpback grouper, Cromileptes altivelis

Replacement of fish meal with poultry by-product meal in diets formulated for the humpback grouper, Cromileptes altivelis

Available online at www.sciencedirect.com Aquaculture 273 (2007) 118 – 126 www.elsevier.com/locate/aqua-online Replacement of fish meal with poultry...

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Available online at www.sciencedirect.com

Aquaculture 273 (2007) 118 – 126 www.elsevier.com/locate/aqua-online

Replacement of fish meal with poultry by-product meal in diets formulated for the humpback grouper, Cromileptes altivelis Rossita Shapawi a,⁎, Wing-Keong Ng b , Saleem Mustafa a a

Borneo Marine Research Institute, Universiti Malaysia Sabah, Locked Bag 2073, 88999 Kota Kinabalu, Sabah, Malaysia b Fish Nutrition Laboratory, School of Biological Sciences, Universiti Sains Malaysia, Penang 11800, Malaysia Received 26 July 2007; received in revised form 14 September 2007; accepted 14 September 2007

Abstract An eight-week feeding trial was conducted to examine the possibility of replacing fish meal with poultry by-product meal (PBM) at high inclusion levels in the diets of the humpback grouper, Cromileptes altivelis, a carnivorous marine tropical fish. Six isolipidic (12%) and isoproteic (50%), experimental diets were formulated to contain graded levels of PBM. Fish meal protein was replaced with a feed-grade PBM at 50, 75 or 100% level (FPBM50, FPBM75, FPBM100, respectively), or a pet food grade PBM at 75 or 100% replacement level (PPBM75 and PPBM100, respectively). The control diet contained Danish fish meal as the sole protein source. The experimental diets were fed close to apparent satiation, twice a day to triplicate groups of humpback grouper fingerlings (12.4 ± 0.2 g). The grouper fingerlings were randomly distributed into groups of 15 fish in cylindrical cages (61 cm depth and 43 cm diameter) and placed in a 150-ton seawater polyethylene tank. Except for fish fed the FPBM100 diet, growth performance, survival, and feed utilization efficiency for fish fed PBM-based diets were not significantly lower (P N 0.05) compared to fish fed the control diet. The PBM source and dietary level did not significantly affect (P N 0.05) the hepato- and visero-somatic indices or the condition factor of fish. Dry matter and protein apparent digestibility coefficients (ADC) of the diets decreased with increasing dietary PBM, and ranged from 64.3–71.5% and 86.2 to 91.2%, respectively. High values (91.7 to 96.7%) for lipid ADC were observed in all diets, with no significant differences among dietary treatments. Whole-body moisture and lipid contents of the fish were not affected by the inclusion of PBM in the diets. With the exception of fish fed the FPBM100 diet, whole-body protein of fish fed the PBM-based diets was slightly higher than that of fish fed the control diet. There was a trend of increased whole-body ash with the increase in dietary levels of PBM. The results from this study indicate that good quality terrestrial PBM can successfully replace more than half the protein from marine fish meal in the diets for humpback grouper. However, total replacement of fish meal with PBM might be constrained by lowered nutrient digestibility and limiting essential amino acids, especially lysine and methionine. © 2007 Elsevier B.V. All rights reserved. Keywords: Grouper; Fish meal; Poultry by-product meal; Growth; Amino acid; Nutrient digestibility

1. Introduction

⁎ Corresponding author. Tel.: +6088 320000x2598; fax: +6088 320261. E-mail address: [email protected] (R. Shapawi). 0044-8486/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2007.09.014

Grouper farming, especially in Southeast Asia, is still heavily dependent on feeding with trash fish. The demand for trash fish is increasing steadily despite decreasing prey fish stocks in the world's oceans (FAO,

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2006). In order to sustain the rapidly expanding marine fish farming in Southeast Asia, more farmers are using commercial formulated feeds in the feeding of captive groupers. However, available commercial feeds for tropical marine carnivorous fish are based mainly on fish meal as the dietary protein source. Total global fish meal production has remained relatively static over the past quarter century (FAO, 2006). The limited supply coupled with increasing demand for fish meal has greatly inflated the cost of this commodity. Therefore, finding suitable protein sources as alternatives to fish meal is critical in the commercial culture of carnivorous fish species, especially for fish such as the humpback grouper, Cromileptes altivelis, that require high protein (50%) in their diets (Williams et al., 2004). Poultry by-product meals (PBM) are rendered byproducts from the poultry processing industry. They are produced in many parts of the world, including the Southeast Asia region, which accounts for approximately one-quarter of the global poultry trade (FAO, 2004). It has high potential to be incorporated in the diet of carnivorous fish species such as groupers due to its high protein content and lower price compared to fish meal. In addition, studies on the apparent digestibility of PBM revealed that this product is well-digested by several fish species (Bureau et al., 1999; Yang et al., 2006). Back in 1980s–1990s, PBM was only able to replace fish meal at a level not exceeding 50%. Tremendous improvement has been achieved in recent years when PBM was reported to be able to replace fish meal at higher levels of up to 100% (Nengas et al., 1999; Takagi et al., 2000; Gaylord and Rawles, 2005). The improved performance of PBM was mainly due to the improved quality of the product through the use of more advanced processing technology (Bureau et al., 1999). As far as we know, there is currently no published information on the use of PBM in the diets of humpback groupers. In the present study, PBM of two origins and grades (local-feed grade and imported-pet food grade) were incorporated in the diets of humpback grouper at a level of 50–100%, and compared with a fish meal-based diet for the effects on growth, feed efficiency, body composition and nutrient digestibility. 2. Materials and methods 2.1. Ingredients and experimental diets Six experimental diets were formulated to be isolipidic (12% crude lipid) and isonitrogenous (50% crude protein). Diet 1 (FM) was the control diet with Danish fish meal as the only protein source. Diets 2-4 were formulated to replace fish meal with a locally sourced feed-grade PBM (Dindings Ltd., Malaysia) at 50% (FPBM50), 75% (FPBM750) or 100%

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(FPBM100), respectively. In Diets 5 and 6, 75% (PPBM75) and 100% (PPBM100) of fish meal, respectively, were replaced by an imported pet food grade PBM [National Renderers Association (NRA), USA]. The chemical and amino acid composition of fish meal and the two grades of PBM are as listed in Table 1. All experimental diets, except diets FPBM100 and PPBM100, were formulated to have 6% fish oil which originated from added fish oil and residual oil in fish meal. Poultry fat (NRA, USA) was used to make up the total lipid level so as to maintain similar dietary fatty acid profiles. Diets FPBM100 and PPBM100 contained slightly lower levels of fish oil compared to other diets due to the residual fat present in added PBM. Chromic oxide (1%) was added to determine the apparent digestibility coefficient (ADC) of the diets. The diets were prepared by mixing all dry ingredients in a mixer and subsequently adding the wet ingredients to form a moist dough. The dough was screw-pressed through a 3 mm die and the strands of feeds formed were air-dried overnight. Diets were kept refrigerated at 4 °C when not being fed. The ingredient composition of the experimental diets is shown in Table 2. 2.2. Fish management Humpback grouper, C. altivelis fingerlings were obtained from a local fish hatchery. Fish of mean initial body weight 12.4 ± 0.2 g were randomly distributed into groups of 15 fish in cylindrical cages (61 cm depth and 43 cm diameter; total of 18 cages), and placed in a 150-ton seawater polyethylene tank, supplied with aeration. Water quality parameters (temperature, salinity, pH, and dissolved oxygen) during the experimental period were 28.6 ± 0.7 °C, 32.6 ± 1.8 mg L− 1, 7.8 ± 0.2, and 6.3 ± 0.1 mg L− 1 respectively. Fish were acclimatized to the experimental cages for two weeks and fed the control diet before the start of the experiment. The experimental diets were fed close to apparent satiation by hand twice a day to triplicate groups of humpback grouper fingerlings. Fish were individually weighed at the start and end of feeding trials, and bulk-weighed fortnightly. The feeding trial was conducted for eight weeks. 2.3. Fecal collection Upon completion of the feeding trial, remaining fish from the same treatments were pooled, divided into duplicate sets and transferred into 12 fiberglass tanks (300 L) with a flowthrough system. Filtered seawater with a flow rate of 3 L/min and adequate aeration were supplied to the culture system. The fish were fed to apparent satiation twice a day at 0800 and 1630 h. After one week acclimatization in the new culture system, feces were collected by carefully siphoning the tank bottom. One hour after each feeding, the rearing tanks were scrubbed and cleaned to remove uneaten feed and fecal residues. Fresh and intact strand of feces were siphoned out carefully 2 h after feeding, rinsed with distilled water, dried on filter paper and immediately frozen (Lin et al., 2004). Daily fecal samples from each tank were pooled until sufficient weight was available for chemical analyses.

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Table 1 Nutrient composition of dietary ingredients (% dry matter) Proximate composition Ingredients b

FM FPBM d PPBM e

Moisture 8.91 4.44 3.12

Ash

Crude lipid

14.60 12.67 15.52

Crude protein

8.65 10.91 10.11

72.05 69.25 67.58

NFE a

Fiber c

ND 0.49 ND

4.70 6.68 6.79

Amino acid composition

FM

FPBM

PPBM

Aspartic acid Glutamic acid Serine Glycine Histidine Arginine Threonine Alanine Proline Tyrosine Valine Methionine Cystine Isoleucine Leucine Phenylalanine Tryptophan Lysine

6.37 12.34 3.13 6.30 1.62 5.05 3.38 4.83 3.12 1.94 4.05 2.07 0.60 3.66 6.11 3.48 0.69 5.67

4.58 9.47 3.94 7.57 1.48 6.00 3.15 4.33 5.51 2.12 4.14 1.43 1.70 3.10 5.55 3.30 0.62 3.51

4.87 10.11 2.72 7.51 1.57 5.64 2.70 4.51 4.66 1.80 3.30 1.76 0.87 2.80 4.99 2.84 0.63 4.12

a b c d e

NFE, Nitrogen-free extract = 100 − (% ash + % protein + % lipid + % fiber). FM, Danish fishmeal. ND, not detected. Feed-grade poultry by-products (Dindings Ltd., Malaysia). Pet food-grade poultry by-products (National Renderers Assosiation, Inc., USA).

2.4. Sample collection and analysis At the beginning of the feeding trial, 10 fish were sampled and frozen at −86 °C for subsequent whole-body proximate analysis. At the end of the feeding trial, all fish were starved for 24 h to ensure that there is no food in the digestive tract. Commercial anesthetic (α-methylquinoline) was used to anesthetize the fish before taking the weight and length measurements at the beginning and end of trial. Samples of liver and viscera from fish in each cage were excised and weighed to assess hepatosomatic index (HSI) and viserosomatic index (VSI). Five fish from each cage were killed and stored at −86 °C for subsequent whole-body composition analysis. Dry matter, ash, crude protein, crude lipid, and crude fiber analysis of diets and whole-body fish were conducted following established methods described in AOAC International (1997). Chromic oxide of diets and feces were determined following the method of Furukawa and Tsukahara (1966). 2.5. Amino acid analysis Ingredient and diet samples were hydrolysed in duplicate with 6 N HCl at 110 °C for 24 h, and derivatized with AccQ reagent (6aminoquinolyl-N-hydroxysuccinimdyl carbamite) before chro-

matographic separation using an AccQ⁎Tag™ reversed phase (3.9 × 150 mm) analytical column (Waters®). The amino acid analysis was performed on a HPLC system which consisted of two 510 solvent delivery, a 474 scanning fluorescence detector (wavelength excitation 250 nm, emission 395 nm) and a 717plus autosampler (Waters®). Chromatographic peaks were integrated, identified and quantified with Millennium Software Version 3.20 (Waters®) by comparing it to known standards (Amino Acid Standard H, Pierce, Rockford, IL). Methionine and cystine were determined from the same method of acid hydrolysis after treatment with performic acid oxidation. Tryptophan was determined by a fluorescence detector (wavelength excitation 285 nm, emission 345 nm) using the reverse phase HPLC technique (C18 analytical column) after sample preparation using alkaline digestion (Alaiz, 2004). 2.6. Digestibility calculation and statistical analysis Apparent digestibility coefficients (ADCs) for dry matter, crude protein, and crude lipid of the diets were determined with the following equations (Cho and Kaushik, 1990): ADC of dry matter ðkÞ ¼ 100 ½1  ðk dietary chromic oxide=fecal chromic oxideÞ

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ADC of nutrient ðkÞ ¼ 100  ½1  ðk fecal nutrient=k dietary nutrientÞ ðk dietary chromic oxide=fecal chromic oxideÞ

level of PBM. Cystine concentrations increased concomitant with dietary levels of FPBM and to a smaller extent, PPBM.

Whenever appropriate, one-way ANOVA was used to compare the growth performance, feed utilization efficiency, body indices, whole-body proximate composition, and ADC. Homogeneity of variances was tested with Levene's test and multiple comparisons among treatments were performed with a Tukey HSD post-hoc test. Significance level was set at P b 0.05. Statistical package SPSS v.11.0 for Windows was used for all statistical analyses.

Good growth of humpback grouper fingerlings was observed in the present study. The highest percentage weight gain (156.7%) and specific growth rate (SGR, 1.7%/d) were attained by fish fed the PPBM75 diet (Table 4). The percentage weight gain and SGR of fish fed FPBM100 were significantly lower (P b 0.05) than that of fish fed the other experimental diets. Fish fed up to 75% FPBM and 100% PPBM replacement of fish meal did not show any significant decrease in growth performance. No significant difference was detected in the total feed intake of fish fed the various experimental diets (P N 0.05). Feed conversion ratio (FCR) ranged from 1.1 to 1.5. The FCR of fish fed FPBM100 was significantly lower (P b 0.05) compared to fish fed the FM, FPBM50, FPBM75, PPBM75, or PPBM100 diets. Both protein efficiency ratio (PER) and net protein utilization (NPU) were lowest in fish fed FPBM100. Survival was high (97 to 100%) and was not dependant on diet.

3. Results 3.1. Nutrient composition of protein sources and experimental diets The proximate and amino acid composition of dietary ingredients and experimental diets are shown in Tables 1 and 3, respectively. Both FPBM and PPBM contained high protein level (67–69%) and moderate level of crude lipid (about 10%). The Danish fish meal used in the present study contained 72% crude protein and 8.7% crude lipid. Both methionine and lysine appeared to be the limiting essential amino acids in the PBM ingredients when compared to fish meal. All experimental diets had similar levels of crude protein and crude lipid. Crude fiber, ash, nitrogen-free extract, and moisture ranged from 0.5–1.8%, 13.2–14.7%, 20.6–23.0%, and 11.3–12.1%, respectively. The amino acid composition of experimental diets reflected the amino acid composition of dietary protein sources. Methionine and lysine contents of the experimental diets decreased with the increasing inclusion

3.2. Growth and feed utilization efficiency

3.3. Body indices and proximate composition Condition factor (CF), hepatosomatic index (HSI), and viscerosomatic index (VSI) were not significantly different (P N 0.05) among dietary treatments (Table 4). The whole-body moisture and lipid contents ranged from 68.7 to 71.9% and 5.0 to 6.0%, respectively, and was not affected by dietary PBM inclusion (Table 5). However, there were significant differences in terms of whole-body protein and ash contents of the groupers fed the different experimental diets. It was observed that incorporation of PBM in the diets increased the whole-

Table 2 Ingredient composition of experimental diets (g/100 g diet) Diet a Ingredient

FM

FPBM50

FPBM75

FPBM100

PPBM75

PPBM100

Danish fish meal b Poultry by-product meal c Corn starch Fish oil Poultry fat d Vitamin premix e Mineral premix f Carboxymethyl cellulose Dicalcium phosphate Chromic oxide Alpha-cellulose

69.4 0.0 13.5 0.0 6.0 3.0 2.0 1.5 1.0 1.0 2.6

34.7 36.1 12.7 3.0 2.1 3.0 2.0 1.5 1.0 1.0 2.9

17.3 54.2 12.3 4.5 0.1 3.0 2.0 1.5 1.0 1.0 3.1

0.0 72.2 11.9 4.1 0.0 3.0 2.0 1.5 1.0 1.0 3.2

17.3 55.5 12.2 4.5 0.4 3.0 2.0 1.5 1.0 1.0 1.6

0.0 74.0 11.7 4.5 0.0 3.0 2.0 1.5 1.0 1.0 1.3

a FM = fish meal control diet; FPBM50, FPBM75, FPBM100 = feed-grade poultry by-product meal replacing 50, 75, or 100% replacement of dietary fish meal; PPBM75, PPBM100 = pet food-grade poultry by product meal replacing 75 or 100% of dietary fish meal. b,c Refer to Table 1 for nutrient content. d Product of National Renderers Association, Inc., USA. e,f Vitamin mix and mineral mix are based on Ng et al. (2000), as-used basis.

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Table 3 Nutrient composition of experimental diets (% dry matter) Diet a Proximate composition

FM

FPBM0

FPBM75

FPBM100

PPBM75

PPBM100

Moisture Ash Crudelipid Crude protein Crudefiber NFE b

11.3 14.0 12.6 49.9 0.5 23.0

11.5 13.4 12.8 50.2 0.8 22.9

11.4 13.4 12.4 51.8 1.5 20.9

12.1 13.2 12.1 52.4 1.8 20.6

11.6 14.4 12.3 51.0 0.8 21.5

11.6 14.7 12.0 50.5 1.3 21.6

Amino acid composition Aspartic acid Glutamic acid Serine Glycine Histidine Arginine Threonine Alanine Proline Tyrosine Valine Methionine Cystine Isoleucine Leucine Phenylalanine Tryptophan Lysine a b

4.43 8.55 2.12 3.99 1.11 3.17 2.26 3.29 2.07 1.01 2.70 1.47 0.37 2.38 4.03 2.16 0.45 3.96

4.13 7.88 2.52 5.05 1.22 3.39 2.25 3.24 2.90 1.27 2.73 1.13 0.71 2.26 3.92 2.33 0.44 3.25

3.90 7.48 2.55 5.21 1.11 3.79 2.17 3.30 3.55 1.22 2.92 1.01 0.79 2.27 4.01 2.18 0.43 2.99

3.66 7.51 3.05 5.40 1.16 3.94 2.25 3.29 3.99 1.38 3.02 0.87 1.08 2.27 4.05 2.39 0.44 2.72

4.00 8.03 2.04 5.54 1.26 3.92 2.07 3.48 3.37 1.23 2.59 1.22 0.55 2.18 3.83 2.06 0.45 3.45

3.63 7.49 1.95 6.15 1.32 4.08 1.99 3.38 3.63 1.16 2.39 1.13 0.56 2.01 3.61 2.10 0.45 2.99

Refer to Table 2 for diet designations. NFE, Nitrogen-free extract = 100 − (% ash + % protein + % lipid + % fiber).

body ash content. Except in fish fed FPBM100, whole-body protein of the fish fed PBM-based diets were higher than in fish fed the control diet. 3.4. Apparent digestibility coefficients There were significant differences (P b 0.05) in the ADC for dry matter and crude protein among the experimental diets (Table 6). Dry matter ADC was highest in FM, followed by diets PPBM75, FPBM50, PPBM100, FBM75, and FPBM100. ADC for crude protein was highest in diet FM and lowest in diet FPBM100. No significant differences were seen in terms of crude lipid digestibility among the various experimental diets (P N 0.05).

4. Discussion The results of the present study demonstrated that fish meal can be replaced with a significant amount of PBM in the diet of humpback grouper without adverse effects on growth performance and feed utilization. In view of the high protein requirement of humpback groupers, the findings of the present study are considered important. In addition, humpback groupers

are slow-growing species, which takes a longer time to reach marketable size compared with other grouper species (Usman et al., 2005). This longer culture period definitely implies a higher requirement for feed input and cost of maintenance. PBM is a cheaper source of protein compared with fish meal and is available in large quantities, especially in poultry producing regions. Therefore, feed costs can be substantially reduced with the inclusion of greater quantities of PBM in the diets of humpback grouper and possibly in the diets of other tropical marine carnivorous cultured fish species. The replacement of fish meal with poultry byproducts had been previously reported by several researchers for various fish species. However, very limited information is available on the use of poultry byproducts in grouper diets. Usman et al. (2007) reported that poultry offal silage meal was able to replace 37% of fish meal protein in the diets of the tiger grouper, Epinephelus fascoguttatus, without any adverse effects on fish productivity. The much lower percentage of fish meal replacement as reported by Usman et al. (2007) compared to the present study was probably due to the differences in the quality of poultry by-products used.

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Table 4 Growth performance, feed efficiency and body indices of humpback grouper fingerlings fed poultry by-product meal-based diets for eight weeks Diet1

Final weight (g) Weight gain (%) SGR (%/d)2 Total feed intake3 FCR4 PER5 NPU6 CF7 HSI8 VSI9

FM

FPBM50

FPBM75

FPBM100

PPBM75

PPBM100

SEM

31.4a 150.4a 1.7a 20.7 1.1a 1.8a 29.0bc 1.6 1.3 6.3

31.3a 148.9a 1.7a 22.5 1.2a 1.7ab 27.0c 1.6 1.2 6.6

31.0a 154.3a 1.7a 22.5 1.2a 1.6b 31.6ab 1.5 1.3 6.8

26.7b 112.5b 1.4b 21.5 1.5b 1.3c 18.1d 1.5 1.4 6.8

31.7a 156.7a 1.7a 22.6 1.2a 1.7ab 31.8a 1.5 1.3 6.5

30.5a 148.7a 1.7a 20.8 1.1a 1.7ab 31.1ab 1.6 1.3 6.3

0.76 6.68 0.05 0.36 0.06 0.07 2.14 0.03 0.02 0.09

Values are the mean of triplicate groups of 15 fish. Average weight of initial fish was 12.4 ± 0.2 g. Values with different superscripts within row are significantly different (P b 0.05). Weight gain = (final weight − initial weight) × 100/initial weight. 1 Refer to Table 2 for diet designations. 2 Specific growth rate (SGR) = [(ln final weight − ln initial weight) / days] × 100. 3 Total feed intake g dry matter fish-1. 4 Feed conversion ratio (FCR) = feed fed (g) / weight gained (g). 5 Protein efficiency ratio (PER) = wet weight gain (g) / total protein intake (g). 6 Net protein utilization (NPU) = 100 × (final − initial fish body protein) / total protein intake. 7 Condition factor (CF) = [fish weight / (total length)3] × 100. 8 Hepatosomatic index (HSI) = (Liver weigh / body weight) × 100. 9 Viserosomatic index (VSI) = (Viseral weight / body weight) × 100.

Nevertheless, the results of the present study are in agreement with several other studies using different fish species. Steffens (1994) reported that poultry offal meal could be successfully used as the sole animal protein source in diets for salmonids provided amino acid supplementation was used. Good quality PBM can be used without amino acid supplementation to replace 75% of the fish meal in diets for gilthead seabream (Nengas et al., 1999) and up to 100% in red sea bream diets (Takagi et al., 2000) without a significant reduction in growth performance. In gibel carp, Yang et al. (2006) reported that high quality PBM could replace 100%

dietary fish meal without adversely affecting growth performance and feed utilization, but an optimal replacement level of 66.5% was recommended. In contrast, PBM could only replace fish meal at a level of not exceeding 50% in European eel (Gallagher and Degani, 1988), chinook salmon (Fowler, 1991), African catfish (Abdel-Warith et al., 2001), and black sea turbot (Yigit et al., 2006). Apart from fish species differences, the major reason for these variable findings was probably due to the varying quality of the tested PBM, which are significantly influenced by their origin and processing methods used (Dong et al., 1993).

Table 5 Whole-body proximate composition (% wet weight basis) of fingerling humpback grouper fed experimental diets Diet1

Moisture Crude protein Crude lipid Ash 1

FM

FPBM50

FPBM75

FPBM100

PPBM75

PPBM100

SEM

71.9 16.4c 5.8 4.7de

71.5 17.1bc 5.2 4.9d

68.7 18.1a 5.9 5.9a

70.5 15.4d 5.0 5.4b

69.3 17.6ab 6.0 5.0d

70.5 17.5ab 5.2 5.2c

0.50 0.40 0.18 0.17

Refer to Table 2 for diet designations. The whole-body composition of initial fish was 72.1 ± 0.8% moisture, 5.4 ± 0.0% ash, 2.8 ± 0.2 lipid. Values are the mean of triplicate groups of 15 fish. Values with different superscripts within row are significantly different (P b 0.05).

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Table 6 Apparent digestibility coefficient for dry matter, crude protein, and crude lipid of experimental diets Diet1

Dry matter (%) Crude protein (%) Crude lipid (%)

FM

FPBM50

FPBM75

FPBM100

PPBM75

PPBM100

SEM

71.5a 91.2a 93.1

68.2abc 89.4b 93.7

66.2c 87.9c 91.8

64.3c 86.2d 91.7

70.6ab 90.1ab 96.7

67.0bc 89.5b 95.2

1.11 0.72 0.80

1

Refer to Table 2 for diet designations. Values are the mean of triplicate groups of 15 fish. Values with different superscripts within row are significantly different (P b 0.05).

In the present study, total replacement of fish meal with FPBM had resulted in reduced growth performance and FCR of humpback grouper fingerlings. Similar with the growth trend and FCR, PER and NPU of fish fed FPBM100 diet were significantly lower than that of other fish groups. The lower NPU and PER values were probably due to the reduced growth rate and the lower whole-body protein level of fish fed the FPBM100 diet. Replacement of fish meal with PBM also resulted in decreased PER and NPU in gilthead seabream exhibiting the lowest SGR (Nengas et al., 1999). The reduction in PER due to reduced growth was also observed in black sea turbot (Yigit et al., 2006) and rainbow trout (Steffens, 1994). The amino acid composition of the PBM used in the present study was within the published values for this ingredient (Halver, 1991; Yu, 2006), and it influenced the overall amino acid composition of the experimental diets. Even though the feed-grade PBM contained slightly higher protein content than the pet food-grade PBM, the latter had a better amino acid profile, especially in terms of lysine and methionine levels. It was interesting to note that the cystine concentration in FPBM was about double that found in PPBM but the sparing value of cystine for methionine in grouper is currently not known. Both methionine and lysine appeared to be the limiting amino acids in the experimental diets with 100% PBM dietary protein source in the present study. Methionine and lysine were also reported as the limiting amino acids in pet food-grade PBM when used as the sole source of protein in the diets of hybrid striped bass, Morone chrysops X M. saxatilis (Gaylord and Rawles, 2005). Little is known about the quantitative amino acid requirement for grouper species. However, the essential amino acids (EAA) levels in fish meal were reported to conform with the EAA pattern in the grouper juveniles, Epinephelus coioides (Millamena, 2002). The dietary methionine requirement for growth of juvenile humpback grouper was reported to be 1.18% (2.41% of dietary protein) and 1.16% (2.37% of dietary protein)

based on weight gain data and feed efficiency, respectively (Giri et al., 2005). The optimum dietary methionine requirement for juvenile E. coioides was estimated to be 1.31% of the diet or 2.73% of dietary protein in the presence of 0.26% dietary cystine (Lou et al., 2005). The methionine concentration was 0.87% in the FPBM100 diet and ranged from 1.01–1.47% in the other experimental diets. This might have contributed in part to the poor growth of fish fed FPBM100. Longer-termed feeding trials will be required to determine if a dietary methionine level of below 1% can support the normal growth of humpback grouper fingerlings. The growth performance of fish fed PPBM100 diet was not significantly different compared to fish fed the FM, FPBM50, FPBM75 or PPBM75 diets. The quantitative lysine requirement for humpback grouper is currently not known. Compared to the FM diet, the FPBM100 and PPBM100 diet had 0.96% and 1.24% less lysine, respectively. Supplementation with lysine and methionine in the PBM-based diets for rainbow trout (Gropp et al., 1979) and hybrid striped bass (Gaylord and Rawles, 2005) was reported to produce fish of equivalent growth performance as fish fed fish meal-based diets. The dry matter, protein and lipid ADC for the FPBM100 diet were the lowest among the various diets. This was probably the major contributing factor to the poor growth performance of humpback grouper fingerling fed FBPM100. Protein ADC for the PPBM100 diet were significantly higher compared to the FPBM100 diet. Dry matter and lipid ADC were also numerically higher for the PPBM100 diet. The better nutrient digestibility of the PPBM compared to FPBM allowed higher dietary levels of this ingredient to be included without noticeable growth depression. Dry matter ADC values (64.3–70.6%) for PBM-based diets observed in the present study were comparable to or slightly better than the values reported in PBM-based diets for hybrid striped bass (Rawles et al., 2006) and in gibel carp (Yang et al., 2006), respectively. The dry matter ADC of poultry offal silage meal diets with a lower inclusion

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level of 5 to 20% ranged from 62.5 to 77.9% in tiger grouper (Usman et al., 2007). Protein ADC (86.2– 90.1%) in PBM-based diets of the present study were comparable to values reported by Takagi et al. (2000) for red sea bream (88.3–93.6%), and slightly better than the values reported by Yang et al. (2006) using gibel carp (81.89–87.39%). High lipid ADC values were observed in all dietary treatments (91.7–96.7%), and these values were not significantly different among dietary treatments. High values for total lipid ADC (91.2 to 95.4%) of poultry offal silage meal diets were also reported in tiger grouper (Usman et al., 2007). In hybrid striped bass, lipid ADC values of PBM diets ranged from 87.0 to 89.9% (Rawles et al., 2006). Williams et al. (2006) reported that humpback grouper was able to use dietary fat efficiently. Replacement of fish meal with PBM did not influence the whole-body moisture and lipid content of groupers in the present study. However, whole-body protein was significantly lower in fish fed FPBM100 than in other fish groups. Whole-body ash tended to increase with the increase of PBM in the diets. This observation was in agreement with Yang et al. (2006), who reported no differences in the whole-body moisture and fat, but a trend of increased protein and ash contents of gibel carp fed increasing level of PBM. In contrast, Nengas et al. (1999) reported significantly lower carcass lipid with increasing dietary PBM in gilthead seabream. Increased whole-body fat of fish fed PBM diets were observed in rainbow trout (Alexis et al., 1985 Steffens, 1994) and chinook salmon (Fowler, 1991). Meanwhile, whole-body composition of red sea bream was not affected by different levels of dietary PBM (Takagi et al., 2000). In the present study, replacement of fish meal with PBM did not affect the CF, HSI, and VSI of the experimental fish. In chinook salmon, there was a tendency for fish fed diets with the highest level of PBM to have lower condition factors than fish fed the lower dietary levels of PBM, but the differences were not always significant (Fowler 1991). Levels of PBM in the diets were reported to influence the HSI of rainbow trout (Steffens, 1994) and red seabream (Takagi et al., 2000). Other than species specific differences, other compounding dietary and environmental factors might be the cause of these differences found in the whole-body composition of various fish fed PBM-based diets. In conclusion, terrestrial PBM can successfully replace more than half of the protein from marine fish meal in the formulated diets for the humpback grouper, a marine carnivorous tropical fish. However, the use of PBM as the sole protein source in the diets of humpback

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grouper might be constrained by lowered nutrient digestibility and limiting essential amino acids. Further research with longer-term feeding trials is currently being carried out to evaluate the nutritive value of PBM for marine fish species. Acknowledgments This study was supported by a fundamental research grant from Universiti Malaysia Sabah and a short-term research grant from Universiti Sains Malaysia. We would like to thank Mr. Ronald Cheong (Dindings Ltd., Malaysia) and Dr. Yu Yu (NRA, Hong Kong) for providing the poultry-by product meals. We are grateful to Dr. Asiah Karim and Mr. Ismail Muit (Department of Veterinary Services, Malaysia) for their assistance in amino acid analysis. References Abdel-Warith, A., Russell, P.M., Davies, S.J., 2001. Inclusion of a commercial poultry by-product meal as a protein replacement of fish meal in practical diets for African catfish Clarias gariepinus (Burchell 1822). Aquacult. Res. 32, 296–305. Alaiz, M., 2004. Determination of tryptophan by high-performance liquid chromatography of alkaline hydrolysates with spectrophotometric detection. Food Chem. 85, 317–320. Alexis, M., Papaparaskeva-Papoutsoglou, E., Theochari, V., 1985. Formulation of practical diets for rainbow trout Salmo gairdneri made by partial or complete substitution of fish meal by poultry-by products and certain plant by-products. Aquaculture 50, 61–73. Association of Official Analytical Chemists International (AOAC) International, 1997. Official Methods of analysis of AOAC International, 16th edn. AOAC International, Arlington, Virginia. Bureau, D.P., Harris, A.M., Cho, C.Y., 1999. Apparent digestibility of rendered animal protein ingredients for rainbow trout. Aquaculture 180, 345–358. Cho, C.Y., Kaushik, S.J., 1990. Nutritional energetics in fish: energy and protein utilization in rainbow trout (Salmo gairdneri). World Rev. Nutr. Diet 61, 132–172. Dong, F.M., Hardy, R.W., Haard, N.F., Barrows, F.T., Rasco, B.A., Fairgrieve, W.T., Forster, I.P., 1993. Chemical composition and protein digestibility of poultry by-product meals for salmonid diets. Aquaculture 116, 149–158. FAO, 2004. EMPRES transboundary animal diseases bulletin no 25, January–June 2004. FAO, 2006. Use of fishery resources as feed inputs to aquaculture development: trends and policy implications. FAO Fisheries Circular, vol. 1018. FAO, Rome. Fowler, L.G., 1991. Poultry by-product meal as a dietary protein source in fall chinook salmon diets. Aquaculture 99, 309–321. Furukawa, A., Tsukahara, H., 1966. On the acid digestion method for the determination of chromic oxide as an index substance in the study of digestibility of fish feed. Bull. Jpn. Soc. Sci. Fish. 32, 502–506. Gallagher, M.L., Degani, G., 1988. Poultry meal and poultry oil as sources of protein and lipid in the diet of European eels (Anguilla anguilla). Aquaculture 73, 177–187.

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