JOURNAL OF THEWORLD AQUACULTURE SOCIETY

Vol. 45, No. 4August, 2014

doi: 10.1111/jwas.12127

Apparent Protein and Energy Digestibility and Amino AcidAvailability of Commercial Meat and Bone Meal for Nile Tilapia,

Oreochromis niloticus

Tadeu O. Xavier, Mariana Michelato, and Luiz V. O. Vidal

Programa de Pós-Graduação em Zootecnia, Universidade Estadual de Maringá, AvenidaColombo, 5790 Paraná, Brazil

Valéria R. B. Furuya and Wilson M. Furuya1

Departamento de Zootecnia, Universidade Estadual de Ponta Grossa, Avenida CarlosCavalcanti, 4748, 84030-900 Paraná, Brazil

AbstractMeat and bone meal (MBM) is an excellent source of amino acids (AAs) for fish but its proximate

composition varies according to its origin and processing. Apparent digestibility coefficients (ADC) ofdry matter, crude protein, and gross energy, and apparent availability coefficients (AAC) of essentialand nonessential AAs (EAA and NEAA, respectively) in MBM containing various levels of crude protein(MBM-340, 370, 400, 430, and 460 g/kg) were determined for juvenile Nile tilapia (Oreochromis niloticus,32.7± 4.5 g). A reference diet containing 351.9 g/kg crude protein and 4541.1 kcal/kg of gross energyand test diets containing a 70:30 mixture of the reference diet and MBM were used with 5 g/kg Cr2O3as an external indicator. ADC of dry matter, gross energy, and crude protein in MBM samples were42.9–76.2%, 71.6–89.1%, and 49.4–86.9%, respectively. MBM-400, 430, and 460 showed higher drymatter, gross energy, and crude protein ADC than that by MBM-340 and 370. All AAs in MBM-460showed AAC of EAA> 90%, while the value for MBM-430 was >85%, except arginine (82.1%) andlysine (84.8%). High ADC of energy, crude protein, and AAC in MBM-430 and 460 indicate goodpotential as quantitative AA sources. Besides the low AA quality of MBM-340, 370, and 400, theirutilization is limited by low digestible energy and high ash, which should be considered in the productionof least-cost, well-balanced, and sustainable diets for tilapia.

Aquaculture feeds are among the most costlyanimal feeds on the market because of theirhigh contents of expensive ingredients and lev-els of processing used. As global fish farmingincreases, the need for balanced “least-cost”diets increases in importance. In many coun-tries, fish meal is an expensive protein source inaquafeed for tilapia, and evaluating alternativesto fish meal is an international research priority.To improve the cost-effectiveness of feeds, fishmeal has been replaced by lower-cost proteinsources with adequate contents of amino acids(AAs) to sustain comparable feed intake, feedefficiency, growth, and health in fish. Meat andbone meal (MBM) is a dried and rendered prod-uct of mammalian tissue consisting of animal

1 Corresponding author.

offal, bones, blood, head parts, lean tissues, andfat (Traylor et al. 2005). Large quantities ofMBM are produced in Brazil as a result of theintensive production of poultry, pigs, and cattle,and because it is a good source of protein andAAs for fish (Guimarães et al. 2008). CurrentEuropean Union legislation restricts the use ofMBM in animal feeds (Buckley et al. 2012),and characterization of the protein and AAcontents in MBM must be provided when it isused in aquafeed. MBM varies in compositionand quality (Gibb et al. 1992) because of thedamage caused during rendering and variabilityin the source of raw material rendered (Knabeet al. 1989).

Recent evidence shows that AAs are notonly cell signaling molecules, but also regulategene expression and protein phosphorylation

© Copyright by the World Aquaculture Society 2014

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440 XAVIER ET AL.

cascades. Besides their functions as buildingblocks of proteins and polypeptides, some AAsregulate key metabolic pathways necessary formaintenance, growth, reproduction, and healthof fish (Wu 2013). Based on new research, appar-ent availability coefficients (AAC) of essentialand nonessential AAs (EAA and NEAA, respec-tively) should be considered in formulating bal-anced diets to improve fish performance andhealth. An optimal balance among AAs is impor-tant for whole-body homeostasis.

Nile tilapia, Oreochromis niloticus, is anomnivorous fish and is considered to be oneof the most important aquaculture species intropical and subtropical countries (El-Sayed2006). Determination of nutrient digestibilityor availability is the first step in evaluatingthe potential of a feedstuff in diets for aqua-culture species (Allan et al. 2000). A betterunderstanding of the AACs of AAs in MBM isrequired to formulate cost-effective, low-wastediets that meet minimum requirements withoutoversupplementing essential AAs. Data on AAavailability of MBM have been reported fortilapia (Guimarães et al. 2008), but additionalstudies are needed because complex interac-tions between sample origin, quantity of bones,and processing methods produce variability inthe proximate and nutritional value of MBM.Thus, this study aimed to evaluate the apparentdigestibility coefficient (ADC) and AAC ofEAA and NEAA of five MBMs commonly usedin commercial feeds for Nile tilapia.

Material and Methods

Feed Ingredients and Diet Preparation

A reference diet containing 352 g/kg crudeprotein, 4541.1 kcal/kg of gross, and 5 g/kgchromic oxide (Cr2O3) was used as external inertmarker (Table 1) and was formulated to meetthe minimum dietary requirements for tilapia(NRC 2011; Tables 2 and 3). The macroingredi-ents were thoroughly mixed and ground using ahammer mill with 0.8-mm screen. Microingredi-ents were manually added to the mixture duringa second mixing cycle. Five commercial sam-ples of MBM were selected according to crudeprotein level to provide a wide range of chemical

Table 1. Formulation and composition of the referencediets (g/kg).

Ingredient g/kg Diet

Corn flour 336.8Soybean meal 437.0Poultry by-product meala 149.5Corn starch 29.9Dicalcium phosphate 19.9Soybean oil 14.9Ascorbic acid phosphate (350 g/kg) 1.0Choline chloride 1.0Vitamin and mineral premixb 5.0Chromium oxide (Cr2O3) 5.0

aIndustry Farima, Tupãci, Paraná, Brazil. Composition:Crude protein, 670 g/kg; dry matter, 948 g/kg; ash, 131 g/kg;gross energy, 4744 kcal/kg.

bComposition (IU or mg/kg of diet): Vitamin A (retinylpalmitate), 1,200,000 IU; vitamin D3 (cholecalciferol),200,000 IU; vitamin E (dl-α-tocopherol), 12,000 mg;vitamin K3 (menadione), 2400 mg; vitamin B1 (thiamineHCl), 4800 mg; vitamin B2 (riboflavin), 4800 mg; vitaminB6 (pyridoxine HCl), 4000 mg; vitamin B12 (cyanocobal-amin), 4.8 mg; folic acid, 1200 mg; d-calcium pantothenate,12,000 mg; vitamin C (ascorbic acid), 48,000 mg; d-biotin,48 mg; choline chloride, 65,000 mg; niacin, 24,000 mg;ferrous sulfate (FeSO4 ⋅H2O ⋅ 7H2O), 10,000 mg; cop-per sulfate (CuSO4 ⋅ 7H2O), 600 mg; manganous sulfate(MnSO4 ⋅H2O), 4000 mg; zinc sulfate (ZnSO4 ⋅ 7H2O),6000 mg; cobalt sulfate (CoSO4 ⋅ 4H2O), 2 mg; sodiumselenite (Na2SeO3), 20 mg; butylated hydroxytoluene(BHT), 15 mg; butylated hydroxyanisole (BHA), 15 mg.

composition (Table 2) and were obtained froma bovine slaughterhouse and from boning andbutcher’s waste. The residues were classified,milled, boiled for 1.5 h in a digester at 90 PSI.The material was then depressurized, excess liq-uid was drained, and drying process was initiatedwith variable pressure in the open digester. Afterthat, MBM was removed from the digester andsieved through a fine mesh to remove fat, andthen pressed to remove remaining fat (Butolo2010). The MBM was provided by NutronIndustries and was classified according to crudeprotein content (g/kg) as MBM-340, 370, 400,430, and 460 on a dry matter basis (Table 4).

Each test diet was composed of 70% refer-ence diet and 30% of the MBM sample. Allingredients were ground through a sieve with500-μm mesh. The test ingredients were handmixed in a Y-mixer (TE 200/5, Tecnal, Piraci-caba, SP, Brazil) and extruded at 99–105 C in

NUTRITIONAL VALUE OF MEAT AND BONE MEAL FOR NILE TILAPIA 441

Table 2. Analyzed proximate composition of thereference diet (g/kg dry matter) fed to Nile tilapia.a

Composition g/kg Diet

Dry matter 909.3± 0.1Crude proteinb 351.9± 2.1Gross energy (kcal/kg) 4541.1± 101.4Crude fiber 37.4± 0.8Ether extract 72.1± 0.6Calcium 13.7± 0.6Total phosphorus 8.8± 0.1

aValues are M±SD of duplicate analyses.bCrude protein=N× 6.25.

Table 3. Analyzed essential and nonessential aminoacids composition of the reference diet (g/kg dry matter) fedto Nile tilapia.a

Amino acid g/kg Diet

Essential amino acidsLysine (%) 16.3± 0.1Methionine 5.4± 0.1Threonine 11.7± 0.1Arginine 21.1± 0.2Histidine 6.5± 0.1Isoleucine 11.8± 0.1Leucine 21.8± 0.2Phenylalanine 13.5± 0.3Phenylalanine+ tyrosine 9.5± 0.2Valine 12.6± 0.2

Nonessential amino acidsAspartic acid 2.8± 0.1Cystine 3.6± 0.1Glycine 16.0± 0.1Glutamic acid 46.4± 0.3Serine 13.4± 0.2Tyrosine 9.5± 0.2

aValues are M±SD of three replicates analyses.

an experimental single-screw extruder (Extrutec,Riberião Preto, SP, Brazil) through 1-mm dieand dehydrated in a forced convection oven(TE 391-1; Tecnal) at 55 C for 48 h. The feedwas stored at 5 C until laboratory analyses anddigestibility trials were conducted.

Fish, Experimental Conditions, and SampleCollection

The digestibility assay was carried outat the Aquaculture Laboratory (CODA-PAR/Universidade Estadual de Maringá) fromDecember 2011 to March 2012. Juvenile Nile

tilapia (GIFT strain, n= 180; mass, 32.65± 4.52g) were obtained from the Aquaculture Labo-ratory and were randomly distributed into 12cylindrical, 120-L fiberglass aquaria (15 fish peraquarium) connected to a closed recirculationsystem. The system consisted of three 500-Lreservoir tanks. Oxygen was maintained at5± 1 mg/L throughout the experimental periodusing blowers and diffusers that supplied air toeach aquarium and to storage tanks. A naturalphotoperiod of 12-h L : 12-h D occurred duringthe experimental period. Before the beginningof the digestibility assay, fish were acclimatedto the laboratory conditions for 4 wk and werehand-fed a commercial extruded diet (Pirá IdealTilápias; Guabi, Campinas, SP, Brazil) con-taining 320 g/kg crude protein, until apparentsatiety. Fish were fed the respective diets toapparent satiation twice daily for 7 d prior tofecal collection. Feces were collected using themodified Guelph system and fish managementfollowed the protocol previously described byGuimarães et al. (2008).

Chemical Analysis

Dry matter and ash analysis of ingredients,diets, and feces were performed according tostandard methods of AOAC (2005). Moisturecontent was determined by drying samples inan oven (TE-391-1; Tecnal) at 105 C until con-stant weight was reached. Nitrogen content wasdetermined using a micro-Kjeldahl apparatus(Tecnal) and crude protein was estimated bymultiplying the nitrogen content by 6.25 (Silvaand Queiroz 2004). Lipid content was deter-mined by ether extraction in a multi-unit Soxhlet(TE-188/6; Tecnal) extraction apparatus for 16 h.Ash was determined by combusting dry sam-ples in a muffle furnace (TE-1100-1P; Tecnal)at 550 C for 6 h. Gross energy was determinedby adiabatic bomb calorimetric (Parr 1266; ParrInstruments Co., Moline, IL, USA). AAs wereanalyzed by the Ajinomoto do Brasil Indús-tria e Comércio de Alimentos Animal NutritionDivision (São Paulo, SP, Brazil) by hydrolyz-ing 0.3 mg sample in 1 mL 6 N HCl for 22 h.The obtained sample was diluted in 0.02 NHCl and injected in an automatic AA analyzer

442 XAVIER ET AL.

Table 4. Nutrient and energy composition of meat and bone meal (MBM) samples on a dry matter basis.a

MBM samples Dry matter (g/kg) GE (kcal/kg) Crude protein (g/kg) Crude fat (g/kg) Ash (g/kg)

MBM-340 936.4± 0.2 3218.6± 27.6 336.9± 1.5 89.9± 1.2 426.4± 1.1MBM-370 941.5± 1.2 3449.6± 36.5 374.0± 0.2 106.0± 2.9 396.2± 1.6MBM-400 948. 6± 2.5 3664.0± 36.8 401.7± 1.2 115.7± 1.5 367.7± 1.3MBM-430 952.5± 0.9 3967.5± 23.9 434.8± 6.0 131.6± 0.6 338.3± 1.7MBM-460 956.4± 0.2 4186.5± 48.3 463.8± 3.6 144.6± 0.6 309.1± 1.2

aValues are M±SD of three replicate analyses. Crude protein=N× 6.25.

(Hitachi L-888, Tokyo, Japan). Recovery hydrol-ysis was performed in 4 N methanesulfonic acidfor analysis of tryptophan and in performicacid for recovery of sulfur AAs. Chromic oxide(Cr2O3) was determined by inductively cou-pled plasma-atomic emission spectrophotometry(ICP-AES; Vista-MPX, Varian, Palo Alto, CA,USA) after perchloric acid digestion, using themodified technique described by Furukawa andTsukahara (1966).

Calculations and Statistical Analyses

The ADC of protein and energy and the AACof EAA and NEAA in the diets were calcu-lated according to Maynard and Loosli (1969)as follows: ADC or AAC (%)= (100 – [%chromium in feed/% chromium in feces]× [%crude protein or AA in feces/% crude pro-tein or AAs in feed]× 100). ADC and AACavailability in the MBM samples werecalculated according to NRC (2011) as fol-lows: ADC or AAA of test ingredient (%)=ADCtest diet + [(ADCtest diet – ADCreference diet)×(0.7×Dreference/0.3×Dingredient)], whereDreference and Dingredient are the percentages ofnutrients or kcal/g gross energy of the referencediet and ingredient, respectively. All results areexpressed as M± SD. The data were subjectedto one-way ANOVA followed by Duncan’s mul-tiple range test using SPSS 13.0 for Windows(SPSS Inc., Chicago, IL, USA). A significancelevel of 5% was used for all comparisons.

Results

The proximate composition of the five MBMsamples is shown in Table 4. Dry matter, grossenergy, and crude fat contents increased and ashdecreased as crude protein content increased.

The quantities of EAAs and NEAAs in MBMfollowed the variation observed in crude proteinlevels (Table 5). The ADC values for dry matter,gross energy, and crude protein in MBM samplesare provided in Table 6. ADC of dry matter inthe samples ranged from 42.9 to 76.2% and thehighest values were observed in MBM-43 and46, which were significantly different (P< 0.05)from the other samples. The ADC of dry mat-ter in MBM-340, 370, 400, and 430 did not dif-fer significantly. ADC of gross energy in theMBM samples ranged from 72 to 89% andthe ADC of gross energy was higher (P< 0.05)in MBM-460 compared to that observed inMBM-340 and 370. All MBM samples eval-uated in this study contained ADC of grossenergy >70%, and >80% in MBM-430 (80%)and MBM-450 (89%). ADC of crude proteinranged from 49 to 87%, and MBM-460 exhib-ited the highest ADC of crude protein whileMBM-340 showed the lowest (P< 0.05). OnlyMBM-460 showed ADC of crude protein >80%(Table 6).

Table 7 shows the AACs of MBM samplesfed to Nile tilapia. EAA and NEAA availabil-ity did not reflect the ADC of crude proteinamong MBM samples. The only AAs for whichAAC did not differ significantly among MBMsamples were cystine and tyrosine. No sig-nificant differences in aspartic acid, cysteine,glutamic acid, isoleucine, methionine, pheny-lalanine, threonine, and valine availability wereobserved among MBM-400, 430, and 460.All AAs in MBM-460 showed AAC >90%,except for alanine (89.4%) and glycine (89.1%),while MBM-430 showed AAC >80% exceptfor alanine (89.4%) and glycine (77%). InMBM-340 and 370 AAC was <80%, except forhistidine, cystine, and tyrosine.

NUTRITIONAL VALUE OF MEAT AND BONE MEAL FOR NILE TILAPIA 443

Table 5. Analyzed essential (EAA) and nonessential (NEAA) amino acid (AA) composition of meat and bone meal(MBM) samples (g/kg dry matter).a

AA MBM-340 MBM-370 MBM-400 MBM-430 MBM-460

EAAArg 31.6± 0.1 30.70± 0.1 31.2± 0.1 34.5± 0.2 36.8± 0.1His 4.9± 0.1 6.1± 0.1 7.2± 0.2 8.30± 0.1 8.6± 0.1Ile 9.1± 0.2 9.6± 0.1 10.8± 0.2 12.7± 0.1 14.2± 0.1Leu 19.1± 0.2 21.6± 0.2 24.1± 0.35 27.0± 0.2 303± 0.2Lys 18.4± 0.1 19.7± 0.2 23.0± 0.1 24.1± 0.1 27.5± 0.2Met 5.9± 0.2 6.2± 0.1 6.4± 0.2 7.3± 0.1 8.8± 0.1Phe 12.7± 0.1 13.2± 0.1 14.37± 0.3 15.6± 0.1 19.4± 0.3Thr 10.7± 0.1 11.9± 0.1 13.1± 0.2 14.7± 0.1 16.8± 0.2Val 13.0± 0.1 14.3± 0.1 16.4± 0.3 18.2± 0.1 20.4± 0.3

NEAAAla 34.2± 0.3 34.6± 0.1 35.5± 0.1 37.4± 0.3 38.7± 0.1Asp 26.7± 0.1 28.54± 0.3 30.7± 0.1 34.1± 0.1 36.9± 0.1Cys 1.8± 0.1 2.05± 0.2 2.56± 0.1 2.90± 0.1 3.16± 0.1Glu 46.0± 0.1 48.9± 0.4 52.1± 0.1 55.8± 0.1 60.4± 0.1Gly 77.7± 0.1 75.9± 0.1 74.8± 0.1 76.9± 0.1 77.9± 0.1Ser 15.0± 0.1 15.8± 0.1 16.9± 0.3 18.3± 0.1 19.9± 0.3Tyr 6.8± 0.1 6.6± 0.1 7.2± 0.1 9.2± 0.1 9.9± 0.1

aValues are M±SD of three replicate analyses.

Table 6. Apparent digestibility coefficients (ADC) of dry matter (DM), gross energy (GE), and crude protein (CP) of fivemeat and bone meal (MBM) samples for Nile tilapia feed.a

ADC (%) MBM-340 MBM-370 MBM-400 MBM-430 MBM-460 P

DM 42.9± 2.4b 44.5± 8.9b 52.4± 9.1b 58.5± 7.5b 76.2± 5.0a 0.001GE 71.6± 8.0b 72.5± 1.6b 78.8± 6.6ab 80.4± 4.2ab 89.1± 4.3a 0.016CP 49.4± 5.2d 58.8± 2.4cd 65.2± 4.7c 76.1± 4.0b 86.9± 1.7a 0.0002

aValues are M±SD of two replicates. Means with different letters within a column differed significantly (P< 0.05).

Discussion

The proximate and AA composition of the fiveMBM samples indicated that gross energy, crudeprotein, crude fat, and AA contents increasedwith increasing ash contents. The compositionand AAC of MBM varies according to thetype of tissues rendered and any heat damageincurred during rendering; rendered productsare considered as low-value components ofanimal carcasses and are used to supply AAsfor fast-growing animals (Buckley et al. 2012).Generally, bone content in MBM decreasesthe quantity of protein and AAs (Gibb et al.1992). Variability in ADC and AAC in MBMis influenced by differences in hair, bones, andcollagen, and by differences in rendering timeand temperature (Aderibigbe and Church 1983).Overheating during processing and inclusionof hair and collagen also causes variation in

nutritional value among MBM products, andash content is negatively related to digestibilityof crude protein in Nile tilapia (Guimarães et al.2008). MBM has been used as a potential sourceof phosphorus in plant protein-based diets forNile tilapia (Suloma et al. 2013).

The ADC values for dry matter, gross energy,and crude protein obtained here for MBM-430are in agreement with other studies that evalu-ated MBM products with higher crude proteincontent. Zhou et al. (2008) evaluated bovineMBM (494 kg/kg crude protein, 4015.3 kcal/kggross energy, 115 g/kg crude fat, and 264 kg/kgash) for bluntnose black bream, Megalobramaamblycephala, and found similar values forADC of dry matter (55%), gross energy (78%),and crude protein (78%). For largemouth bass,Micropterus salmoides, Masagounder et al.(2009) reported similar ADC of dry matter(58%) and crude protein (72%) in MBM

444 XAVIER ET AL.

Table 7. Apparent availability coefficients (AAC) of essential (EAA) and nonessential (NEAA) amino acids (%1) of meatand bone meal (MBM) samples for Nile tilapia.1

AAC MBM-340 MBM-370 MBM-400 MBM-430 MBM-460 P

Arg 66.6± 5.9c 67.9± 2.6c 75.1± 5.7bc 82.1± 1.3ab 91.7± 2.2a 0.0008His 79.2± 5.7b 80.3± 2.4b 86.1± 3.7ab 87.8± 0.5ab 92.9± 3.9a 0.005Ile 71.8± 7.9c 74.2± 4.1bc 86.2± 10.0abc 89.7± 5.2ab 92.3± 3.4a 0.01Leu 72.0± 7.3c 76.4± 1.6bc 87.2± 6.6ab 91.9± 0.8a 94.2± 1.5a 0.0004Lys 74.3± 3.5c 74.7± 4.8bc 80.6± 4.7bc 84.8± 0.7ab 93.6± 3.6a 0.0004Met 74.0± 1.7b 74.9± 7.2b 80.9± 7.0ab 88.5± 1.2a 91.2± 1.3a 0.0029Phe 74.1± 8.7c 76.4± 3.6bc 87.7± 5.5ab 92.2± 0.8a 95.3± 1.7a 0.001Thr 75.0± 2.9b 83.6± 9.1ab 90.3± 6.2a 91.2± 1.8a 94.7± 1.2a 0.0062Val 70.6± 7.5b 72.9± 3.7b 84.1± 8.4ab 88.7± 4.2a 93.3± 3.0a 0.002Ala 52.8± 3.2c 55.7± 6.9c 69.7± 6.2b 78.4± 2.2ab 89.4± 1.8a 0.0009Asp 68.3± 3.1b 71.5± 6.4b 83.6± 5.6a 87.0± 0.7a 93.7± 3.8a 0.0001Cys 85.6± 1.3 87.6± 10.6 92.7± 12.3 91.6± 3.2 93.8± 2.9 0.64Glu 69.5± 3.1b 70.5± 5.9b 84.2± 4.6a 88.3± 0.6a 94.1± 3.2a 0.0004Gly 53.3± 3.8c 54.9± 5.6c 67.4± 6.7b 77.0± 1.3b 89.1± 1.2a 0.0006Ser 68.7± 3.0c 71.8± 6.5c 84.5± 4.9b 88.0± 1.4ab 95.5± 2.4a 0.0005Tyr 91.4± 7.7 95.3± 9.5 99.0± 4.6 100.3± 0.5 103.5± 1.1 0.18M 71.7± 9.7 74.3± 10.0 83.7± 8.0 88.0± 5.6 93.6± 3.2 –

1Values are M± SD of three replicates. Means with different letters within a column differed significantly (P< 0.05).

(467 g/kg crude protein, 4039.2 kcal/kg grossenergy, and 199 g/kg ash). For Nile tilapia,Guimarães et al. (2008) determined ADC ofcrude protein of 78% in MBM (473 g/kg crudeprotein, 3132 kcal/kg gross energy, and 413 g/kgash). However, the ADC of crude proteinand gross energy in MBM-460 in this studyapproximated the values of those parameters(87 and 94%, respectively) obtained for stripedsurubim, Pseudoplatystoma reticulatum, (Silvaet al. 2013); besides the carnivorous habit ofthis species, the proximate composition of theMBM (449 g/kg crude protein, 3656.8 kcal/kggross energy, 127 g/kg crude lipid, and 340 g/kgash) was close to that of the MBM-460 usedin this study. Here, only MBM-460 showedsimilar ADC of crude protein to that of red fishmeal described for omnivorous pacu, Piaractusmesopotamicus (91%, Fernandes et al. 2004),Nile tilapia (89%, Guimarães et al. 2008), car-nivorous black bream (82%, Zhou et al. 2008),and striped surubim (83%, Silva et al. 2013).

In this study, mean AAC obtained forMBM-400 (84%) was similar to that describedby Guimarães et al. (2008) for Nile tilapia usingMBM with 473 g/kg crude protein but containedmore ash (413 g/kg) than MBM-400 (368 g/kg).The mean AAC in MBM-430 (88%) wascomparable to the mean value (89%) obtained

in fish meal (574 g/kg crude protein, 89 g/kgcrude lipid, 338 g/kg ash). However, the meanAAC in MBM-460 was slightly higher (94%)than the value obtained in poultry byproducts(91%) by Guimarães et al. (2008), and higherthan that obtained for EAA in Peruvian fishmeal (88%) or Nile tilapia (Davies et al. 2011).Lysine is known as a limiting AA in MBMproducts (Klemesrud et al. 1997) because ofits susceptibility to damage during thermalprocessing. However, in this study, the AACof lysine from each MBM did not differ fromthat of other EAAs and was similar to resultsobserved by Guimarães et al. (2008).

The great variability in MBM as a replacementfor fish meal in fish diets is also related to parti-cle size distribution and energy content (Forsteret al. 2003), and to heat damage to lysine thatoccurs during the rendering process (Opstvedtet al. 1984). However, positive effects of MBMmay be obtained because of its good palatability,which can increase feed intake (Yang et al.2004). The ADC of crude protein decreasedwith increases in MBM content, and appearedto have been related to the high ash content, asa negative relationship between ADCCP anddietary ash content was previously observed ingibel carp by Zhang et al. (2006). The proteinquality of aquafeed ingredients is usually the

NUTRITIONAL VALUE OF MEAT AND BONE MEAL FOR NILE TILAPIA 445

leading factor affecting fish growth (Köprücüand Özdemir 2005), and protein quality dependson the AA profile and availability. Deficiencyof an EAA results in poor utilization of dietaryCP and reduces growth and feed efficiency (Lee2002). In this study, apparent EAA and NEAAavailability did not follow trends similar tothe ADC of crude protein, and knowledge ofindividual AA availability of particular MBMproducts should be considered to achieve for-mulation of more appropriate, economical, andenvironmentally sustainable diets for fish. Inthis study, dry matter, gross energy, and crudeprotein ADC and AAC of MBM were relatedmarkedly and negatively to ash content. MBMwas shown to be a potential source of protein,AAs, energy, and minerals in fish diets, and alow-cost alternative feed ingredient that couldbe used without compromising fish performancein gibel carp, Carassius auratus gibelio (Yanget al. 2004; Zhang et al. 2006); drum, Nibeamiichthioides (Guo et al. 2007); channel catfish,Ictalurus punctatus (Lochmann et al. 2012); andNile tilapia (Suloma et al. 2013).

In conclusion, this study has shown that forNile tilapia, the highest ADC crude proteinavailability was observed in MBM contain-ing 460 g/kg of crude protein. ADC and AACof AA tended to be negatively related to ashcontent, suggesting that MBM containing 340and 400 g/kg crude protein could be consid-ered in formulating nutritionally balanced,cost-effective diets for sustainable tilapiaproduction, but that these products are notpromising sources of protein and AAs.

Acknowledgments

Ajinomoto Animal Nutrition – Animal Nutri-tion Division, São Paulo, SP, Brazil, assistedwith the AA analyses. This study was funded byConselho Nacional de Pesquisa e Desenvolvi-mento Científico – CNPq, Brasília, DF, Brazil.We also thank Luiz Edivaldo Pezzato and JoséEurico Possebon Cyrino for their assistance inthis study.

Literature CitedAderibigbe, A. O. and D. C. Church. 1983. Feather and hair

meals for ruminants. I. Effect of degree of processing on

utilization of feather meal. Journal of Animal Science56:1198–1207.

Allan, G. L., S. Parkinson, M. A. Booth, D. A. J. Stone, S.J. Rowland, J. Frances, and R. Warner-Smith. 2000.Replacement of fish meal in diets for Australian silverperch, Bidyanus bidyanus: I. Digestibility of alternativeingredients. Aquaculture 186:293–310.

AOAC (Association of Official Analytical Chemists).2005. Official methods of analysis of AOAC Inter-national edition. AOAC International, Gaithersburg,Maryland, USA.

Buckley, M., K. E. H. Penkman, T. J. Wess, S. Reaney, andM. J. Collins. 2012. Protein and mineral characteriza-tion of rendered meat and bone meal. Food Chemistry134:1267–1278.

Butolo, J. E. 2010. Qualidade de Ingredientes na Alimen-tação Animal. Colégio Brasileiro de Nutrição Animal,Campinas, Brazil.

Davies, S. J., A. A. Abdel-Warith, and A. Gouveia. 2011.Digestibility characteristics of selected feed ingredientsfor developing bespoke diets for Nile tilapia culturein Europe and North America. Journal of the WorldAquaculture Society 42:388–398.

El-Sayed, A. F. M. 2006. Tilapia culture. CABI Publishing,Wallingford, Connecticut, USA.

Fernandes, J. B. K., R. Lochmann, and F. A. Bocane-gra. 2004. Apparent digestible energy and nutrientdigestibility coefficients of diet ingredients for pacuPiaractus brachypomus. Journal of the World Aquacul-ture Society 35:237–244.

Forster, I. P., W. Dominy, L. Obaldo, and A. G. J. Tacon.2003. Rendered meat and bone meals as ingredients ofdiets for shrimp Litopenaeus vannamei (Boone, 1931).Aquaculture 219:655–670.

Furukawa, A. and H. Tsukahara. 1966. On the aciddigestion method for the determination of chromicoxide as an index substance in the study of digestibilityof fish feed. Nippon Suisan Gakkaishi 32:502–506.

Gibb, D. J., T. J. Klopfenstein, and M. H. Sindt. 1992.Combinations of rendered protein meals for growingcalves. Journal of Animal Science 70:2581–2589.

Guimarães, I. G., L. E. Pezzato, and M. M. Barros.2008. Amino acid availability and protein digestibilityof several protein sources for Nile tilapia, Oreochromisniloticus. Aquaculture Nutrition 14:396–404.

Guo, J., Y. Wang, and D. P. Bureau. 2007. Inclusion ofrendered animal ingredients as fishmeal substitutes inpractical diets for cuneate drum, Nibea miichthioides(Chu, Lo et Wu). Aquaculture Nutrition 13:81–87.

Klemesrud, M. J., T. J. Klopfenstein, A. J. Lewis, D. H.Shain, and D. W. Herold. 1997. Limiting amino acidsin meat and bone and poultry by-product meals. Journalof Animal Science 75:3294–3300.

Knabe, D. A., D. C. LaRue, E. J. Gregg, G. M. Martinez,and T. D. Tanksley. 1989. Apparent digestibility ofnitrogen and amino acids in protein feedstuffs by grow-ing pigs. Journal of Animal Science 67:441–458.

Köprücü, K. and Y. Özdemir. 2005. Apparentdigestibility of selected feed ingredients for Nile

446 XAVIER ET AL.

tilapia (Oreochromis niloticus). Aquaculture 250:308–316.

Lee, S.-M. 2002. Apparent digestibility coefficients of var-ious feed ingredients for juvenile and grower rockfish(Sebastes schlegeli). Aquaculture 207:79–95.

Lochmann, R., C. Engle, G. Kumar, M. H. Li, J. L. Avery,B. G. Bosworth, and C. S. Tucker. 2012. Multi-batchcatfish production and economic analysis using alter-native (low-cost) diets with corn gluten feed and tra-ditional diets with meat and bone meal. Aquaculture366-367:34–39.

Masagounder, K., J. D. Firman, R. S. Hayward, S. Sun,and P. B. Brown. 2009. Apparent digestibilities of com-mon feedstuffs for bluegill Lepomis macrochirus andlargemouth bass Micropterus salmoides using individ-ual test ingredients. Aquaculture Nutrition 15:29–37.

Maynard, L. A. and J. K. Loosli. 1969. Animal nutrition.McGraw-Hill Book Company, New York, New York,USA.

NRC. 2011. Nutrient requirements of fish and shrimp. TheNational Academy Press, Washington, DC, USA.

Opstvedt, J., R. Miller, R. W. Hardy, and J. Spinelli.1984. Heat-induced changes in sulfhydryl groups anddisulfide bonds in fish protein and their effect on proteinand amino acid digestibility in rainbow trout (Salmogairdneri). Journal of Agricultural and Food Chemistry32:929–935.

Silva, D. and A. Queiroz. 2004. Análise de alimentos(Métodos químicos e biológicos). 3a Edição, Viçosa,MG. Universidade Federal de Viçosa 57:76.

Silva, T. S. C., G. V. Moro, T. B. A. Silva, J. K. Dairiki, andJ. E. P. Cyrino. 2013. Digestibility of feed ingredientsfor the striped surubim Pseudoplatystoma reticulatum.Aquaculture Nutrition 19:491–498.

Suloma, A., R. Mabroke, and E. El-Haroun. 2013. Meatand bone meal as a potential source of phosphorus inplant-protein-based diets for Nile tilapia (Oreochromisniloticus). Aquaculture International 21:375–385.

Traylor, S. L., G. L. Cromwell, and M. D. Linde-mann. 2005. Bioavailability of phosphorus in meatand bone meal for swine. Journal of Animal Science83:1054–1061.

Wu, G. 2013. Amino acids: biochemistry and nutrition. CRCPress, Boca Raton, Florida, USA.

Yang, Y., S. Xie, Y. Cui, W. Lei, X. Zhu, and Y. Yu. 2004.Effect of replacement of dietary fish meal by meat andbone meal and poultry by-product meal on growth andfeed utilization of gibel carp, Carassius auratus gibelio.Aquaculture Nutrition 10:289–294.

Zhang, S., S. Xie, X. Zhu, W. Lei, Y. Yang, and M. Zhao.2006. Meat and bone meal replacement in diets for juve-nile gibel carp (Carassius auratus gibelio): effects ongrowth performance, phosphorus and nitrogen loading.Aquaculture Nutrition 12:353–362.

Zhou, Z., Z. Ren, H. Zeng, and B. Yao. 2008. Apparentdigestibility of various feedstuffs for bluntnose blackbream Megalobrama amblycephala Yih. AquacultureNutrition 14:153–165.