JOURNAL OF THE Vol. 45, No.

4
WORLD AQUACULTURE SOCIETY August, 2014
doi: 10.1111/jwas.12127

Apparent Protein and Energy Digestibility and Amino Acid

Availability 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, Avenida
Colombo, 5790 Paraná, Brazil

Valéria R. B. Furuya and Wilson M. Furuya1

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

Abstract
Meat 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) of
dry matter, crude protein, and gross energy, and apparent availability coefficients (AAC) of essential
and 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 energy
and test diets containing a 70:30 mixture of the reference diet and MBM were used with 5 g/kg Cr2 O3
as an external indicator. ADC of dry matter, gross energy, and crude protein in MBM samples were
42.9–76.2%, 71.6–89.1%, and 49.4–86.9%, respectively. MBM-400, 430, and 460 showed higher dry
matter, gross energy, and crude protein ADC than that by MBM-340 and 370. All AAs in MBM-460
showed AAC of EAA > 90%, while the value for MBM-430 was >85%, except arginine (82.1%) and
lysine (84.8%). High ADC of energy, crude protein, and AAC in MBM-430 and 460 indicate good
potential as quantitative AA sources. Besides the low AA quality of MBM-340, 370, and 400, their
utilization is limited by low digestible energy and high ash, which should be considered in the production
of least-cost, well-balanced, and sustainable diets for tilapia.

Aquaculture feeds are among the most costly
animal feeds on the market because of their
high contents of expensive ingredients and lev-
els of processing used. As global fish farming
increases, the need for balanced “least-cost”
diets increases in importance. In many coun-
tries, fish meal is an expensive protein source in
aquafeed for tilapia, and evaluating alternatives
to fish meal is an international research priority.
To improve the cost-effectiveness of feeds, fish
meal has been replaced by lower-cost protein
sources with adequate contents of amino acids
(AAs) to sustain comparable feed intake, feed
efficiency, growth, and health in fish. Meat and
bone meal (MBM) is a dried and rendered prod-
uct of mammalian tissue consisting of animal
1 Corresponding author.
© Copyright by the World Aquaculture Society 2014
offal, bones, blood, head parts, lean tissues, and
fat (Traylor et al. 2005). Large quantities of
MBM are produced in Brazil as a result of the
intensive production of poultry, pigs, and cattle,
and because it is a good source of protein and
AAs for fish (Guimarães et al. 2008). Current
European Union legislation restricts the use of
MBM in animal feeds (Buckley et al. 2012),
and characterization of the protein and AA
contents in MBM must be provided when it is
used in aquafeed. MBM varies in composition
and quality (Gibb et al. 1992) because of the
damage caused during rendering and variability
in the source of raw material rendered (Knabe
et al. 1989).
Recent evidence shows that AAs are not
only cell signaling molecules, but also regulate
gene expression and protein phosphorylation

439
440 XAVIER ET AL.
cascades. Besides their functions as building
blocks of proteins and polypeptides, some AAs
regulate key metabolic pathways necessary for
maintenance, growth, reproduction, and health
of fish (Wu 2013). Based on new research, appar-
ent availability coefficients (AAC) of essential
and nonessential AAs (EAA and NEAA, respec-
tively) should be considered in formulating bal-
anced diets to improve fish performance and
health. An optimal balance among AAs is impor-
tant for whole-body homeostasis.
Nile tilapia, Oreochromis niloticus, is an
omnivorous fish and is considered to be one
of the most important aquaculture species in
tropical and subtropical countries (El-Sayed
2006). Determination of nutrient digestibility
or availability is the first step in evaluating
the potential of a feedstuff in diets for aqua-
culture species (Allan et al. 2000). A better
understanding of the AACs of AAs in MBM is
required to formulate cost-effective, low-waste
diets that meet minimum requirements without
oversupplementing essential AAs. Data on AA
availability of MBM have been reported for
tilapia (Guimarães et al. 2008), but additional
studies are needed because complex interac-
tions between sample origin, quantity of bones,
and processing methods produce variability in
the proximate and nutritional value of MBM.
Thus, this study aimed to evaluate the apparent
digestibility coefficient (ADC) and AAC of
EAA and NEAA of five MBMs commonly used
in commercial feeds for Nile tilapia.
Material and Methods
Feed Ingredients and Diet Preparation
A reference diet containing 352 g/kg crude
protein, 4541.1 kcal/kg of gross, and 5 g/kg
chromic oxide (Cr2 O3 ) was used as external inert
marker (Table 1) and was formulated to meet
the minimum dietary requirements for tilapia
(NRC 2011; Tables 2 and 3). The macroingredi-
ents were thoroughly mixed and ground using a
hammer mill with 0.8-mm screen. Microingredi-
ents were manually added to the mixture during
a second mixing cycle. Five commercial sam-
ples of MBM were selected according to crude
protein level to provide a wide range of chemical
Table 1. Formulation and composition of the reference
diets (g/kg).
Ingredient g/kg Diet
Corn flour 336.8
Soybean meal 437.0
Poultry by-product meala 149.5
Corn starch 29.9
Dicalcium phosphate 19.9
Soybean oil 14.9
Ascorbic acid phosphate (350 g/kg) 1.0
Choline chloride 1.0
Vitamin and mineral premixb 5.0
Chromium oxide (Cr2 O3 ) 5.0
a Industry Farima, Tupãci, Paraná, Brazil. Composition:
Crude protein, 670 g/kg; dry matter, 948 g/kg; ash, 131 g/kg;
gross energy, 4744 kcal/kg.
b Composition (IU or mg/kg of diet): Vitamin A (retinyl
palmitate), 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 (thiamine
HCl), 4800 mg; vitamin B2 (riboflavin), 4800 mg; vitamin
B6 (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 ⋅ H2 O ⋅ 7H2 O), 10,000 mg; cop-
per sulfate (CuSO4 ⋅ 7H2 O), 600 mg; manganous sulfate
(MnSO4 ⋅ H2 O), 4000 mg; zinc sulfate (ZnSO4 ⋅ 7H2 O),
6000 mg; cobalt sulfate (CoSO4 ⋅ 4H2 O), 2 mg; sodium
selenite (Na2 SeO3 ), 20 mg; butylated hydroxytoluene
(BHT), 15 mg; butylated hydroxyanisole (BHA), 15 mg.
composition (Table 2) and were obtained from
a bovine slaughterhouse and from boning and
butcher’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 initiated
with variable pressure in the open digester. After
that, MBM was removed from the digester and
sieved through a fine mesh to remove fat, and
then pressed to remove remaining fat (Butolo
2010). The MBM was provided by Nutron
Industries and was classified according to crude
protein 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. All
ingredients were ground through a sieve with
500-μm mesh. The test ingredients were hand
mixed 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 the tilapia (GIFT strain, n = 180; mass, 32.65 ± 4.52
reference diet (g/kg dry matter) fed to Nile tilapia.a g) were obtained from the Aquaculture Labo-
Composition g/kg Diet ratory and were randomly distributed into 12
cylindrical, 120-L fiberglass aquaria (15 fish per
Dry matter 909.3 ± 0.1
Crude proteinb 351.9 ± 2.1 aquarium) connected to a closed recirculation
Gross energy (kcal/kg) 4541.1 ± 101.4 system. The system consisted of three 500-L
Crude fiber 37.4 ± 0.8 reservoir tanks. Oxygen was maintained at
Ether extract 72.1 ± 0.6 5 ± 1 mg/L throughout the experimental period
Calcium 13.7 ± 0.6
using blowers and diffusers that supplied air to
Total phosphorus 8.8 ± 0.1
a Values
each aquarium and to storage tanks. A natural
are M ± SD of duplicate analyses.
b Crude photoperiod of 12-h L : 12-h D occurred during
protein = N × 6.25.
the experimental period. Before the beginning
of the digestibility assay, fish were acclimated
Table 3. Analyzed essential and nonessential amino to the laboratory conditions for 4 wk and were
acids composition of the reference diet (g/kg dry matter) fed hand-fed a commercial extruded diet (Pirá Ideal
to Nile tilapia.a
Tilápias; Guabi, Campinas, SP, Brazil) con-
Amino acid g/kg Diet taining 320 g/kg crude protein, until apparent
Essential amino acids
satiety. Fish were fed the respective diets to
Lysine (%) 16.3 ± 0.1 apparent satiation twice daily for 7 d prior to
Methionine 5.4 ± 0.1 fecal collection. Feces were collected using the
Threonine 11.7 ± 0.1 modified Guelph system and fish management
Arginine 21.1 ± 0.2 followed the protocol previously described by
Histidine 6.5 ± 0.1
Isoleucine 11.8 ± 0.1
Guimarães et al. (2008).
Leucine 21.8 ± 0.2
Phenylalanine 13.5 ± 0.3 Chemical Analysis
Phenylalanine + tyrosine 9.5 ± 0.2
Valine 12.6 ± 0.2 Dry matter and ash analysis of ingredients,
Nonessential amino acids diets, and feces were performed according to
Aspartic acid 2.8 ± 0.1 standard methods of AOAC (2005). Moisture
Cystine 3.6 ± 0.1
Glycine 16.0 ± 0.1
content was determined by drying samples in
Glutamic acid 46.4 ± 0.3 an oven (TE-391-1; Tecnal) at 105 C until con-
Serine 13.4 ± 0.2 stant weight was reached. Nitrogen content was
Tyrosine 9.5 ± 0.2 determined using a micro-Kjeldahl apparatus
a Values are M ± SD of three replicates analyses. (Tecnal) and crude protein was estimated by
multiplying the nitrogen content by 6.25 (Silva
and Queiroz 2004). Lipid content was deter-
an experimental single-screw extruder (Extrutec, mined by ether extraction in a multi-unit Soxhlet
Riberião Preto, SP, Brazil) through 1-mm die (TE-188/6; Tecnal) extraction apparatus for 16 h.
and dehydrated in a forced convection oven Ash was determined by combusting dry sam-
(TE 391-1; Tecnal) at 55 C for 48 h. The feed ples in a muffle furnace (TE-1100-1P; Tecnal)
was stored at 5 C until laboratory analyses and at 550 C for 6 h. Gross energy was determined
digestibility trials were conducted.
by adiabatic bomb calorimetric (Parr 1266; Parr
Instruments Co., Moline, IL, USA). AAs were
Fish, Experimental Conditions, and Sample analyzed by the Ajinomoto do Brasil Indús-
Collection tria e Comércio de Alimentos Animal Nutrition
The digestibility assay was carried out Division (São Paulo, SP, Brazil) by hydrolyz-
at the Aquaculture Laboratory (CODA- ing 0.3 mg sample in 1 mL 6 N HCl for 22 h.
PAR/Universidade Estadual de Maringá) from The obtained sample was diluted in 0.02 N
December 2011 to March 2012. Juvenile Nile HCl 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)
MBM-340 936.4 ± 0.2 3218.6 ± 27.6
MBM-370 941.5 ± 1.2 3449.6 ± 36.5
MBM-400 948. 6 ± 2.5 3664.0 ± 36.8
MBM-430 952.5 ± 0.9 3967.5 ± 23.9
MBM-460 956.4 ± 0.2 4186.5 ± 48.3
a Values 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 acid
for analysis of tryptophan and in performic
acid for recovery of sulfur AAs. Chromic oxide
(Cr2 O3 ) was determined by inductively cou-
pled plasma-atomic emission spectrophotometry
(ICP-AES; Vista-MPX, Varian, Palo Alto, CA,
USA) after perchloric acid digestion, using the
modified technique described by Furukawa and
Tsukahara (1966).
Calculations and Statistical Analyses
The ADC of protein and energy and the AAC
of 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 AAC
availability in the MBM samples were
calculated 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 )], where
Dreference and Dingredient are the percentages of
nutrients or kcal/g gross energy of the reference
diet and ingredient, respectively. All results are
expressed as M ± SD. The data were subjected
to one-way ANOVA followed by Duncan’s mul-
tiple range test using SPSS 13.0 for Windows
(SPSS Inc., Chicago, IL, USA). A significance
level of 5% was used for all comparisons.
Results
The proximate composition of the five MBM
samples is shown in Table 4. Dry matter, gross
energy, and crude fat contents increased and ash
decreased as crude protein content increased.
Crude protein (g/kg) Crude fat (g/kg) Ash (g/kg)
336.9 ± 1.5 89.9 ± 1.2 426.4 ± 1.1
374.0 ± 0.2 106.0 ± 2.9 396.2 ± 1.6
401.7 ± 1.2 115.7 ± 1.5 367.7 ± 1.3
434.8 ± 6.0 131.6 ± 0.6 338.3 ± 1.7
463.8 ± 3.6 144.6 ± 0.6 309.1 ± 1.2
The quantities of EAAs and NEAAs in MBM
followed the variation observed in crude protein
levels (Table 5). The ADC values for dry matter,
gross energy, and crude protein in MBM samples
are provided in Table 6. ADC of dry matter in
the samples ranged from 42.9 to 76.2% and the
highest values were observed in MBM-43 and
46, 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 the
MBM samples ranged from 72 to 89% and
the ADC of gross energy was higher (P < 0.05)
in MBM-460 compared to that observed in
MBM-340 and 370. All MBM samples eval-
uated in this study contained ADC of gross
energy >70%, and >80% in MBM-430 (80%)
and MBM-450 (89%). ADC of crude protein
ranged from 49 to 87%, and MBM-460 exhib-
ited the highest ADC of crude protein while
MBM-340 showed the lowest (P < 0.05). Only
MBM-460 showed ADC of crude protein >80%
(Table 6).
Table 7 shows the AACs of MBM samples
fed to Nile tilapia. EAA and NEAA availabil-
ity did not reflect the ADC of crude protein
among MBM samples. The only AAs for which
AAC did not differ significantly among MBM
samples were cystine and tyrosine. No sig-
nificant differences in aspartic acid, cysteine,
glutamic acid, isoleucine, methionine, pheny-
lalanine, threonine, and valine availability were
observed 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% except
for alanine (89.4%) and glycine (77%). In
MBM-340 and 370 AAC was <80%, except for
histidine, 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

EAA
Arg 31.6 ± 0.1 30.70 ± 0.1 31.2 ± 0.1 34.5 ± 0.2 36.8 ± 0.1
His 4.9 ± 0.1 6.1 ± 0.1 7.2 ± 0.2 8.30 ± 0.1 8.6 ± 0.1
Ile 9.1 ± 0.2 9.6 ± 0.1 10.8 ± 0.2 12.7 ± 0.1 14.2 ± 0.1
Leu 19.1 ± 0.2 21.6 ± 0.2 24.1 ± 0.35 27.0 ± 0.2 303 ± 0.2
Lys 18.4 ± 0.1 19.7 ± 0.2 23.0 ± 0.1 24.1 ± 0.1 27.5 ± 0.2
Met 5.9 ± 0.2 6.2 ± 0.1 6.4 ± 0.2 7.3 ± 0.1 8.8 ± 0.1
Phe 12.7 ± 0.1 13.2 ± 0.1 14.37 ± 0.3 15.6 ± 0.1 19.4 ± 0.3
Thr 10.7 ± 0.1 11.9 ± 0.1 13.1 ± 0.2 14.7 ± 0.1 16.8 ± 0.2
Val 13.0 ± 0.1 14.3 ± 0.1 16.4 ± 0.3 18.2 ± 0.1 20.4 ± 0.3
NEAA
Ala 34.2 ± 0.3 34.6 ± 0.1 35.5 ± 0.1 37.4 ± 0.3 38.7 ± 0.1
Asp 26.7 ± 0.1 28.54 ± 0.3 30.7 ± 0.1 34.1 ± 0.1 36.9 ± 0.1
Cys 1.8 ± 0.1 2.05 ± 0.2 2.56 ± 0.1 2.90 ± 0.1 3.16 ± 0.1
Glu 46.0 ± 0.1 48.9 ± 0.4 52.1 ± 0.1 55.8 ± 0.1 60.4 ± 0.1
Gly 77.7 ± 0.1 75.9 ± 0.1 74.8 ± 0.1 76.9 ± 0.1 77.9 ± 0.1
Ser 15.0 ± 0.1 15.8 ± 0.1 16.9 ± 0.3 18.3 ± 0.1 19.9 ± 0.3
Tyr 6.8 ± 0.1 6.6 ± 0.1 7.2 ± 0.1 9.2 ± 0.1 9.9 ± 0.1
a Values 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 five
meat 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 0.001
GE 71.6 ± 8.0b 72.5 ± 1.6b 78.8 ± 6.6ab 80.4 ± 4.2ab 89.1 ± 4.3a 0.016
CP 49.4 ± 5.2d 58.8 ± 2.4cd 65.2 ± 4.7c 76.1 ± 4.0b 86.9 ± 1.7a 0.0002
a Values are M ± SD of two replicates. Means with different letters within a column differed significantly (P < 0.05).

Discussion nutritional value among MBM products, and

The proximate and AA composition of the five
MBM samples indicated that gross energy, crude
protein, crude fat, and AA contents increased
with increasing ash contents. The composition
and AAC of MBM varies according to the
type of tissues rendered and any heat damage
incurred during rendering; rendered products
are considered as low-value components of
animal carcasses and are used to supply AAs
for fast-growing animals (Buckley et al. 2012).
Generally, bone content in MBM decreases
the quantity of protein and AAs (Gibb et al.
1992). Variability in ADC and AAC in MBM
is influenced by differences in hair, bones, and
collagen, and by differences in rendering time
and temperature (Aderibigbe and Church 1983).
Overheating during processing and inclusion
of hair and collagen also causes variation in
ash content is negatively related to digestibility
of crude protein in Nile tilapia (Guimarães et al.
2008). MBM has been used as a potential source
of phosphorus in plant protein-based diets for
Nile tilapia (Suloma et al. 2013).
The ADC values for dry matter, gross energy,
and crude protein obtained here for MBM-430
are in agreement with other studies that evalu-
ated MBM products with higher crude protein
content. Zhou et al. (2008) evaluated bovine
MBM (494 kg/kg crude protein, 4015.3 kcal/kg
gross energy, 115 g/kg crude fat, and 264 kg/kg
ash) for bluntnose black bream, Megalobrama
amblycephala, and found similar values for
ADC 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 meat
and 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 0.0008
His 79.2 ± 5.7b 80.3 ± 2.4b 86.1 ± 3.7ab 87.8 ± 0.5ab 92.9 ± 3.9a 0.005
Ile 71.8 ± 7.9c 74.2 ± 4.1bc 86.2 ± 10.0abc 89.7 ± 5.2ab 92.3 ± 3.4a 0.01
Leu 72.0 ± 7.3c 76.4 ± 1.6bc 87.2 ± 6.6ab 91.9 ± 0.8a 94.2 ± 1.5a 0.0004
Lys 74.3 ± 3.5c 74.7 ± 4.8bc 80.6 ± 4.7bc 84.8 ± 0.7ab 93.6 ± 3.6a 0.0004
Met 74.0 ± 1.7b 74.9 ± 7.2b 80.9 ± 7.0ab 88.5 ± 1.2a 91.2 ± 1.3a 0.0029
Phe 74.1 ± 8.7c 76.4 ± 3.6bc 87.7 ± 5.5ab 92.2 ± 0.8a 95.3 ± 1.7a 0.001
Thr 75.0 ± 2.9b 83.6 ± 9.1ab 90.3 ± 6.2a 91.2 ± 1.8a 94.7 ± 1.2a 0.0062
Val 70.6 ± 7.5b 72.9 ± 3.7b 84.1 ± 8.4ab 88.7 ± 4.2a 93.3 ± 3.0a 0.002
Ala 52.8 ± 3.2c 55.7 ± 6.9c 69.7 ± 6.2b 78.4 ± 2.2ab 89.4 ± 1.8a 0.0009
Asp 68.3 ± 3.1b 71.5 ± 6.4b 83.6 ± 5.6a 87.0 ± 0.7a 93.7 ± 3.8a 0.0001
Cys 85.6 ± 1.3 87.6 ± 10.6 92.7 ± 12.3 91.6 ± 3.2 93.8 ± 2.9 0.64
Glu 69.5 ± 3.1b 70.5 ± 5.9b 84.2 ± 4.6a 88.3 ± 0.6a 94.1 ± 3.2a 0.0004
Gly 53.3 ± 3.8c 54.9 ± 5.6c 67.4 ± 6.7b 77.0 ± 1.3b 89.1 ± 1.2a 0.0006
Ser 68.7 ± 3.0c 71.8 ± 6.5c 84.5 ± 4.9b 88.0 ± 1.4ab 95.5 ± 2.4a 0.0005
Tyr 91.4 ± 7.7 95.3 ± 9.5 99.0 ± 4.6 100.3 ± 0.5 103.5 ± 1.1 0.18
M 71.7 ± 9.7 74.3 ± 10.0 83.7 ± 8.0 88.0 ± 5.6 93.6 ± 3.2 –
1 Values 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 gross
energy, and 199 g/kg ash). For Nile tilapia,
Guimarães et al. (2008) determined ADC of
crude protein of 78% in MBM (473 g/kg crude
protein, 3132 kcal/kg gross energy, and 413 g/kg
ash). However, the ADC of crude protein
and gross energy in MBM-460 in this study
approximated the values of those parameters
(87 and 94%, respectively) obtained for striped
surubim, Pseudoplatystoma reticulatum, (Silva
et al. 2013); besides the carnivorous habit of
this species, the proximate composition of the
MBM (449 g/kg crude protein, 3656.8 kcal/kg
gross energy, 127 g/kg crude lipid, and 340 g/kg
ash) was close to that of the MBM-460 used
in this study. Here, only MBM-460 showed
similar ADC of crude protein to that of red fish
meal described for omnivorous pacu, Piaractus
mesopotamicus (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 for
MBM-400 (84%) was similar to that described
by Guimarães et al. (2008) for Nile tilapia using
MBM with 473 g/kg crude protein but contained
more ash (413 g/kg) than MBM-400 (368 g/kg).
The mean AAC in MBM-430 (88%) was
comparable to the mean value (89%) obtained
in fish meal (574 g/kg crude protein, 89 g/kg
crude lipid, 338 g/kg ash). However, the mean
AAC in MBM-460 was slightly higher (94%)
than the value obtained in poultry byproducts
(91%) by Guimarães et al. (2008), and higher
than that obtained for EAA in Peruvian fish
meal (88%) or Nile tilapia (Davies et al. 2011).
Lysine is known as a limiting AA in MBM
products (Klemesrud et al. 1997) because of
its susceptibility to damage during thermal
processing. However, in this study, the AAC
of lysine from each MBM did not differ from
that of other EAAs and was similar to results
observed by Guimarães et al. (2008).
The great variability in MBM as a replacement
for fish meal in fish diets is also related to parti-
cle size distribution and energy content (Forster
et al. 2003), and to heat damage to lysine that
occurs during the rendering process (Opstvedt
et al. 1984). However, positive effects of MBM
may be obtained because of its good palatability,
which can increase feed intake (Yang et al.
2004). The ADC of crude protein decreased
with increases in MBM content, and appeared
to have been related to the high ash content, as
a negative relationship between ADCCP and
dietary ash content was previously observed in
gibel carp by Zhang et al. (2006). The protein
quality of aquafeed ingredients is usually the
 NUTRITIONAL VALUE OF MEAT AND BONE MEAL FOR NILE TILAPIA
leading factor affecting fish growth (Köprücü
and Özdemir 2005), and protein quality depends
on the AA profile and availability. Deficiency
of an EAA results in poor utilization of dietary
CP and reduces growth and feed efficiency (Lee
2002). In this study, apparent EAA and NEAA
availability did not follow trends similar to
the ADC of crude protein, and knowledge of
individual AA availability of particular MBM
products should be considered to achieve for-
mulation of more appropriate, economical, and
environmentally sustainable diets for fish. In
this study, dry matter, gross energy, and crude
protein ADC and AAC of MBM were related
markedly and negatively to ash content. MBM
was shown to be a potential source of protein,
AAs, energy, and minerals in fish diets, and a
low-cost alternative feed ingredient that could
be used without compromising fish performance
in gibel carp, Carassius auratus gibelio (Yang
et al. 2004; Zhang et al. 2006); drum, Nibea
miichthioides (Guo et al. 2007); channel catfish,
Ictalurus punctatus (Lochmann et al. 2012); and
Nile tilapia (Suloma et al. 2013).
In conclusion, this study has shown that for
Nile tilapia, the highest ADC crude protein
availability was observed in MBM contain-
ing 460 g/kg of crude protein. ADC and AAC
of AA tended to be negatively related to ash
content, suggesting that MBM containing 340
and 400 g/kg crude protein could be consid-
ered in formulating nutritionally balanced,
cost-effective diets for sustainable tilapia
production, but that these products are not
promising sources of protein and AAs.
Acknowledgments
Ajinomoto Animal Nutrition – Animal Nutri-
tion Division, São Paulo, SP, Brazil, assisted
with the AA analyses. This study was funded by
Conselho Nacional de Pesquisa e Desenvolvi-
mento Científico – CNPq, Brasília, DF, Brazil.
We also thank Luiz Edivaldo Pezzato and José
Eurico Possebon Cyrino for their assistance in
this study.
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