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47
S.T. Yong, M. Mardhati, I.J. Farahiyah, S. Noraini and H.K. Wong
J. Trop. Agric. and Fd. Sc. 46(1)(2018): 47 – 55
Article history
Received: 22.12.16
Accepted: 18.12.17
Authors' full names: Yong Su Ting, Mardhati Mohammad, Farahiyah Ilyana Jamaludin, Noraini
Samat and Wong Hee Kum
E-mail: yongsuting@mardi.gov.my
©Malaysian Agricultural Research and Development Institute 2018
Replacement of shmeal in feather meal-based diet and its effects
on tilapia growth performance and on water quality parameters
(Penggantian mil ikan dalam makanan yang berasaskan tepung bulu ayam dan
kesannya terhadap perkembangan tumbesaran tilapia dan parameter kualiti air)
S.T. Yong1, M. Mardhati1, I.J. Farahiyah1, S. Noraini1 and H.K. Wong1
1Animal Science Research Centre, MARDI Headquarters, Persiaran MARDI-UPM, 43400 Serdang,
Selangor, Malaysia.
Abstract
A 16-week feeding trial was conducted to observe the growth performance
of red hybrid tilapia (Oreochromis sp.) fed two levels (10% and 15%)
of feather meal, which replaced 92% and 100% of shmeal in the diets.
Also, the water quality parameters in the recirculating water system were
determined weekly. The triplicate groups of tilapia were fed twice daily with
isoenergetic diets (13.0 MJ/kg) containing 29% digestible protein (isonitrogenous).
The sh with an average size of 37 g were reared for 16 weeks in circular
polytanks with total volume of 1 m3 in a recirculating water culture system. It is
worth highlighting that the weight gain, specic growth rate and feed conversion
ratio of red tilapia fed 10% and 15% feather meal were signicantly better
(p <0.05) than the control (major protein sources from soybean meal, sh meal
and corn gluten meal). Apart from that, all the water parameters were within
the optimum range of water quality for tilapia growth. Small but signicant
differences (p <0.05) in pH, water temperature, NH3 and NH4+ were observed
between the feather meal fed treatments and the control. This study revealed that
up to 15% of feather meal can be included into the sh diet with good growth
performance and feed conversion ratio. Moreover, it was found that feather meal
can completely replace shmeal in tilapia diets.
Keywords: feather meal, tilapia, sh nutrition, growth, water quality
Introduction
Feather meal (FeM) is one of the rendered
protein ingredients that is commonly used
in sh feeds at levels of 3 – 7% (Bureau
2010). However, sh feed manufacturers are
reluctant to use higher levels of feather meal
in their feeds due to signicant variability in
the quality and nutritive value of different
batches of feather meal (Bureau 2010).
Some academic and commercial-scale trials
have reported excellent performance in sh
with feeds containing greater than 12%
feather meal. However, some trials reported
relatively poor performance of feed with
high levels of feather meal (Bureau 2010)
and the source of discrepancies among
the results of different trials was unclear.
It is worth noting that cooking time
and pressure inuenced the digestibility
of feather meal. Variations in the raw
materials incorporated and in processing
methods and conditions can culminate in
48
Replacement of shmeal in feather meal-based
a big variability in the nutrient prole of
different batches of this ingredient, and
problems will be faced in accurate feed
formulation (Bureau et al. 2000; Bureau
2010; Wong and Mardhati 2010). According
to Guimaraes et al. (2008), FeM has 78.5%
apparent protein digestibility with an
average apparent amino acid availability of
79.7% for Oreochromis niloticus. Fuertes
et al. (2014) reported that during the rst
80 days of intensive rearing 8.2% of FeM
(15% replacement of shmeal protein) can
be included in extruded diets for juvenile
Pacifastacus leniusculus without impairing
growth or feed conversion. Bureau et al.
(2000) pointed out that an inclusion of up
to 15% of feather meal provides about 20%
of total digestible protein (DP) in the diet
was possible without affecting the growth,
feed efciency, nitrogen or energy gains of
rainbow trout.
It is of utmost importance to have
accurate characterisation of the nutritive
value of FeM in order to optimise its use
in sh feeds. Developing methodological
approaches and rapid screening tests to
effectively differentiate feather meals of
different nutritive values should be a priority
for the rendering and aquaculture feed
industry (Bureau 2010). Notably, feeds can
account for 50 to 80% (Ng 2009) of the
operational costs of aquaculture production
and Malaysia is very dependent on imported
soybean and shmeal as protein sources
in its aquaculture industry. Generally,
protein ingredients account for more than
two-thirds of the sh diet cost. Sustainable
alternatives to replace the feed source need
to be identied and produced due to the
declining global production of shmeal.
It is practical and economical to focus on
further developing downstream processing
and increasing the production of FeM and
poultry offal meal as protein sources for the
aquaculture industry since there is a highly
developed status of poultry production in the
country and many poultry processing plants
(Wong and Mardhati 2010). The objectives
of the present study were to evaluate the
effects of completely replacing shmeal with
hydrolyzed FeM-based diets on the growth
performance and feed conversion ratio
(FCR) of tilapia and to determine the effects
on water quality parameters.
Materials and method
Experimental treatments
A total of 315 red hybrid tilapia
(Oreochromis sp.) male ngerlings with
a mean initial body weight of 37 g were
purchased from a hatchery in Selangor. Prior
to the feeding trial, the sh were adapted
to the experimental system for 2 weeks.
Then, they were randomly divided into
3 treatments and three replications with 35
sh per replication. The sh were fed one
of the three treatment (Table 1) diets: (a)
control diet, (b) 10% inclusion of hydrolysed
feather meal (FeM) and (c) 15% inclusion of
hydrolysed FeM, replacing 92% and 100%
of shmeal in the diets.
Diet preparation
The hydrolysed FeM had nutrient content
of 13.8 MJ/kg digestible energy and
606 g/kg digestible crude protein. The
experimental diets were formulated to be
isoenergetic, 13 MJ/kg digestible energy
(DE) and isonitrogenous, 29% digestible
protein (DP). The nutrient compositions of
the diets are tabulated in Table 2. By means
of using the National Research Council
(NRC) nutrient requirements of sh and
shrimp (NRC 2011) as a guide, the least cost
formulation diets were formulated to meet
the minimum specications for tilapia. The
minimum specications were as follows:
DE 13.0 MJ/kg, DP 29%, crude fat 8%,
available phosphorus 0.40%, calcium 0.70%,
digestible (D)-arginine 1.20%, D-histidine
0.50%, D-isoleucine 1.00%, D-leucine
1.90%, D-lysine 1.60%, D-methionine
0.70%, D-methionine + cystine 1.00%,
D-phenylalanine 1.10%, D-threonine
1.10%, D-tryptophan 0.30% and D-valine
1.10%. The complete feed was produced
as extruded oating pellets. A pulveriser
[(Teck Seng Agricultural Sdn Bhd (TSASB)]
49
S.T. Yong, M. Mardhati, I.J. Farahiyah, S. Noraini and H.K. Wong
Table 1. Composition of diet ingredients (as-fed basis)
Ingredient A (% in diet) B (% in diet) C (% in diet)
Soybean meal 44.26 40.55 34.23
Fish meal 12.30 1.0 0.00
Feather meal 0.00 10.00 15.00
Corn 10.71 12.65 13.57
Corn gluten meal 10.00 10.00 8.97
Cassava starch 15.00 15.00 15.00
Palm oil 5.50 5.50 5.50
Wheat pollard 0.00 2.56 4.80
Dicalcium phosphate 1.41 1.15 1.06
Calcium carbonate 0.640 0.77 0.82
DL-methionine 0.162 0.294 0.331
L-lysine HCl 0.000 0.327 0.454
L-threonine 0.0150 0.186 0.259
Vitamin concentrate* 0.010 0.010 0.010
*Vitamin concentrate providing per kg of ration at 1kg/tonne inclusion: 6,700,000 IU/kg
vitamin A, 1,350,000 IU/kg vitamin D, 67 g/kg vitamin E, 3.4 g/kg vitamin K3, 6.7 g/kg
vitamin B1, 10 g/kg vitamin B2, 8 g/kg vitamin B6, 13.5 mg/kg vitamin B12, 53.0 g/kg
niacin, 26.5 g/kg pantothenic acid, 3.3 g/kg folic acid, 335 mg/kg biotin, 135 g/kg inositol
and 105 g/kg vitamin C
Table 2. Calculated nutrient composition in experimental diets
Nutrient A BC
Digestible energy (MJ/kg) 13.00 13.00 13.00
Digestible protein (%) 29.00 29.00 29.00
Crude fat (%) 8.05 8.37 8.57
Calcium (%) 0.70 0.70 0.70
Available phosphorus (%) 0.40 0.40 0.40
Crude fat (%) 8.05 8.37 8.57
D-arginine (%) 1.935 1.802 1.710
D-histidine (%) 0.732 0.627 0.562
D-isoleucine (%) 1.306 1.124 1.034
D-leucine (%) 2.752 2.606 2.480
D-lysine (%) 1.670 1.600 1.600
D-methionine (%) 0.700 0.700 0.700
D-methionine + cystine (%) 1.075 1.287 1.384
D-phenylalanine (%) 1.503 1.380 1.282
D-threonine (%) 1.100 1.100 1.100
D-tryptophan (%) 0.310 0.261 0.231
D-valine (%) 1.378 1.234 1.163
D = digestible
50
Replacement of shmeal in feather meal-based
was utilised for particle size reduction of the
various feed ingredients, which were then
thoroughly mixed in a mixer before cooking
and extrusion (up to 150 °C) of the pellets
using a laboratory-scale extruder (TSASB).
After the extrusion process, the pellets
were coated with the vitamin concentrate
(Peterlabs Sdn. Bhd.) mixed in sh oil using
a coating machine (TSASB).
Growth study
The sh were fed the experimental diets
with a total of 3% (1st 8 weeks) and 2%
(2nd 8 weeks) of the sh biomass twice a
day at 9.00 am and 4.00 pm. Every two
weeks, the amount of feed was adjusted
according to the last live body weight
determined by weighing. The experiment
was performed in polyethylene tanks, with
total volume of 1 m3 each and equipped
with a semi-closed water recirculating
aquaculture system (RAS). The RAS system
was equipped with a nitrication unit and
a sedimentation unit. Stocking density in
sh tanks was 28 L/sh. All experimental
tanks were supplied with air through an
aeration system. A 30% volume of water in
the sh tanks was replaced with clean water
weekly. The feeding trial was conducted
for 16 weeks.
Data recording
Temperature, pH, concentration of
dissolved oxygen (DO2), NH3 and NH4+
were measured weekly between 8.00 and
9.00 in the morning prior to partial water
replacement. A thermometer and a pH
meter (model Corning 345) were used
to measure the water temperature and
pH. Water quality (DO2, NH4+ and NH3)
determinations were carried out using a YSI
model 56 oxygen meter (Yellow Spring
Instruments Co., USA). Fish weight and
feed intake were measured fortnightly
during water quality measurements, while
mortality was recorded daily (if any). The
following formula was used to calculate
specic growth rate (SGR):
SGR
(% body weight
gain/day)
= (logn nal sh weight – logn initial sh weight)
––––––––––––––––––––––––––––––––––––––– x 100
time interval
Statistical analysis
The data of the present study were analyzed
using analysis of variance using the ANOVA
procedure of the SAS software (SAS 2000)
and the mean values were compared using
the LSD test.
Results and discussion
Growth performance of sh
A steady increase (Figure 1 and 2) was
observed with regards to the growth and
feed intake among tilapia over the 16 - week
period. The 10% FeM diet gave the best
nal sh weight, weight gain, SGR and
FCR (p <0.05) compared to the control and
the 15% FeM diets (Table 3 and Table 4).
Also, tilapia that were fed with 15% FeM
diet performed better than the control for
nal sh weight, weight gain, SGR and FCR
(p <0.05). The 15% FeM diet (Table 1) did
not include any shmeal; besides protein
from FeM, other major protein sources
were from plant sources such as soybean
and corn gluten meals. The signicantly
better (p <0.05) growth performance and
FCR for the 15% FeM diet compared to
the control diet suggested that higher FeM
inclusion levels are possible if the decient
amino acids in FeM are substituted for
synthetic sources.
Bishop et al. (1996) reported that the
growth of Oreochromis niloticus fry was
not compromised by replacing 9.9% of the
total diet with feather meal. This result is
comparable to the ndings from Chor et
al. (2013). However, Chor et al. (2013)
evaluated several levels (9.86, 19.71, 29.57,
39.42 and 49.28%) of FeM to replace
Danish sh meal as the sole protein source.
It was revealed that catsh that were fed the
control diet had signicantly better weight
gain, specic growth rate and feed intake
than those fed with diets containing FeM.
Apart from that, they also reported that FeM
supplementation at 9.86% was comparable
SGR (% body weight gain/day) = (logn nal sh weight – logn initial sh weight)
––––––––––––––––––––––––––––– X 100%
time interval
51
S.T. Yong, M. Mardhati, I.J. Farahiyah, S. Noraini and H.K. Wong
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250
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150
100
50
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Fish weight (g)
0246 8 10
Weeks
12 14 16
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Figure 1. Effect of feeding feather meal-based
diets on sh growth
24 6 8 10 12 14 16
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Figure 2. Effect of feeding feather meal-based
diets on feed intake
Table 3. Effects of feather meal-based diets on sh weight gain and SGR
Treatment Initial sh weight (g) Final sh weight (g) Weight gain/sh (g) SGR (%)
A 36.67 ± 0.67a 220.95 ± 2.69a 184.29 ± 3.08a 1.60 ± 0.03a
B36.67 ± 0.67a 247.60 ± 2.692c 210.95 ± 2.43c 1.70 ± 0.02c
C 37.14 ± 0.00a 236.19 ± 2.69b 199.05 ± 2.69b 1.65 ± 0.01b
Data values are the mean and standard deviation at the end of 16 weeks; SGR = specic growth rate
(%). Mean values within a column and bearing different letters are signicantly different from one
another according to the LSD test (p < 0.05)
Table 4. Effects of feather meal-based diets on
sh feed intake and FCR
Treatment Feed intake/sh (g) FCR
A 271.78 ± 2.96a 1.47 ± 0.03c
B280.95 ± 3.68a 1.33 ± 0.00a
C 279.07 ± 5.69a 1.40 ± 0.04b
Data values are the mean and standard deviation
at the end of 16 weeks; FCR = feed conversion
ratio. Mean values within a column and bearing
different letters are signicantly different from
one another according to the LSD test (p < 0.05)
to the control for survival rate and FCR.
However, high sh mortality and retarded
growth were observed in the 19.71 – 49.28%
FeM-supplemented diets. Catsh mortality
increased with the increase of FeM inclusion
with mortality ranging from 11.1 – 62.2%
with FeM supplementation. As compared to
the present study, there was no mortality in
all the treatments (10 and 15% FeM) and
this may be due to the difference in quality
of FeM between the studies. The growth,
feed efciency, nitrogen or energy gains
of rainbow trout were not affected by the
inclusion of up to 15% FeM (Bureau 2000).
Higher FeM usage was reported by Sulomo
et al. (2014) as they observed that FeM
inclusion up to 19.8% in Nile tilapia diets
did not compromise growth and protein
utilization. A very high shmeal inclusion
of 22% was observed and in comparison to
the present study, only 0 and 1% of shmeal
inclusion for the FeM-based diets were
observed.
Water quality
Referring to the results presented in Table 5,
the mean range values for DO2 (mg/L) for
all treatments were within the optimum
and not signicantly different between
treatments (p >0.05). There were signicant
differences (p <0.05) in pH and temperature
(Table 5) between treatments. Nevertheless,
the pH and temperature ranges were within
the optimum. It is noteworthy that the
means and range of values for DO2, pH and
temperature (Figures 3, 4 and 5) were within
the optimal range for tilapia production
(Pillay and Kutty 2005, Mjoun et al.
2010). Weekly DO2 data (Figure 3) for the
treatments during weeks 9, 11 and 12 were
below 5.0 mg/L and closer to 3.0 mg/L,
52
Replacement of shmeal in feather meal-based
although these relatively lower values were
still within the acceptable range for tilapia
production (Mjoun et al. 2010).
Unionised ammonia (NH3) is the
toxic form of ammonia and predominates
when pH is high. NH4+ is relatively
non-toxic (Hargreaves and Tucker 2004)
and predominates when pH is low. The
mean values for unionized NH3 (Table 5)
were within the optimum, ranging from
0.028 – 0.031 mg/L (mean 0.029 mg/L)
for treatment A, 0.019 – 0.021 mg/L
(mean 0.020 mg/L) for treatment B and
0.020 – 0.026 mg/L (mean 0.023 mg/L)
for treatment C. On comparison, unionized
NH3 was signicantly higher (p <0.05)
in treatment A than treatments B and C.
Table 5. Effects of feather meal-based diets on water quality parameters
Treatment DO2 (mg/L) pH Temp (°C) NH3 (mg/L) NH4+ (mg/L)
A 5.44 ± 0.09a 7.29 ± 0.03a 26.28 ± 0.02a 0.029 ± 0.001a 2.22 ± 0.09a
B5.56 ± 0.20a 7.21 ± 0.02b 26.17 ± 0.02b 0.020 ± 0.001b 1.85 ± 0.12b
C 5.23 ± 0.21a 7.13 ± 0.02c 26.01 ± 0.01c 0.0230.003b 2.19 ± 0.23ab
Data values are the mean and standard deviation at the end of 16 weeks; DO2 = dissolved oxygen; Temp
= temperature. Mean values within a column and bearing different letters are signicantly different from
one another according to the LSD test (p < 0.05)
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Concentration of DO2 (mg/L)
10
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6
4
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012 3 45678910 11 1213 141516
Weeks
Figure 3. Effect of feeding feather meal-based
diets on concentration of dissolved oxygen
in water
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Figure 4. Effect of feeding feather meal-based
diets on pH of water
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1 2 3 4 5 6 78910 111213 14 15 16
Temperature (°C)
Weeks
A
B
C
Figure 5. Effecy of feeding meal-based diets on
water temperature
Weekly NH3 values (Figure 6) for weeks
1, 13 and 14 exceeded the optimum
range (Mjoun et al. 2010) for growth, but
recovered and were within the optimum
range in the subsequent weeks. The increase
of NH3 during these weeks may have
been due to overall sh growth and more
protein waste excretion. The declines in
weekly feed intake (Figure 2) were due
to the NH3 increase during these weeks.
When ammonia began to accumulate, sh
responded through reduced feeding activity
and microorganisms use oxygen for the
degradation of undigested feed resulting in
lower DO2 levels. The values for the toxic
NH3 for all the treatments were below the
lower lethal range 0.6 mg/L (Riche and
Garling 2003) and below the 2.0 mg/L level
(Popma and Masser 1999, Riche and Garling
2003, Mjoun et al. 2010) when tilapia began
to die. Toxic NH3 made up 1.29, 1.07 and
1.04% (Table 5) of the total NH3 plus NH4+
for treatments A, B and C, respectively,
which were well below the proportion
of under 10% reported by Hargreaves
and Tucker (2004). Values for ionised
NH4+ (Figure 7 and Table 5) ranged from
2.10 – 2.30 mg/L (mean 2.22 mg/L) for A,
53
S.T. Yong, M. Mardhati, I.J. Farahiyah, S. Noraini and H.K. Wong
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Figure 6. Effect of feeding feather meal-based
diets on water ammonia concentration
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B
C
Figure 7. Effect of feeding feather meal based
diets on water ammonium ion concentration
1.68 – 1.94 mg/L (mean 1.85 mg/L) for B
and 1.90 – 2.46 mg/L (mean 2.19 mg/L)
for C. There was a signicant difference
(p <0.05) in NH4+ values between treatment
A and B. NH4+ is relatively non-toxic and
the weekly NH4+ data reected the weekly
NH3 data.
No detrimental effects on the water
quality in the experimental tanks and on
the performance of the sh as no mortality
recorded with the inclusion of 10 or 15%
hydrolysed feather meal.
As regards the tilapia aquaculture
in Malaysia, average feeding costs of the
surveyed farms made up almost 63% of the
production cost, while high production cost
was due to the use of commercial tilapia
feeds (Ng et al. 2013). Thus, cheaper feed
ingredients like FeM can help alleviate the
cost of aquaculture production. Gatlin et
al. (2007) and Tacon and Metian (2008)
highlighted on the considerable progress
made in nding substitutes to replace the
diminishing supply of an increasingly
expensive sh meal. The availability of
soybean products (soybean meal and soy
protein concentrate) made them viable
alternatives to shmeal, but whether they
can effectively replace shmeal in sh diets
is still debateable and more research is
required with regards to the issue. Recently,
Figueiredo-Silva et al. (2015) reported on
the almost total replacement of sh meal
with soybean meal in diets for hybrid tilapia
by indicating that methionine + cystine
levels of 15.7 g/kg and 12.5 g/kg in the diets
were able to achieve 95% of maximum sh
weight and protein gain. Hernandez et al.
(2010) reported a complete replacement of
shmeal using animal proteins from porcine
and poultry by-product meals in practical
diets for ngerling Nile tilapia.
Conclusion
The present study found that FeM up to
15% of the total diet could completely
replace shmeal (a diminishing and
unsustainable source) in tilapia diets, giving
good growth and feed conversion ratio
with no detrimental effects on water quality
parameters. It is practical and economical
to produce FeM as a protein source for
the aquaculture industry due to the highly
developed status of poultry production and
many poultry processing plants in Malaysia
(Wong and Mardhati 2010). Apart from
that, developing rapid screening tests to
effectively differentiate feather meals of
different nutritive value (Bureau 2010)
should be a high priority for both the
rendering industry and aquaculture feed
industry due to the wide variation in results
reported for FeM used in aquaculture feed.
Acknowledgements
Our deepest thanks go to the Ministry
of Science, Technology and Innovation
(MOSTI) for the nancial support through
the E-Sciencefund (06-03-08-SF0253) and
Mr. Zainal Abidin Abdul Rahman for his
technical assistance.
54
Replacement of shmeal in feather meal-based
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L.A., Azevedo, P.A. and Cho, C.Y. (2000).
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from different origins as protein sources in
rainbow trout (Oncorhynchus mykiss) diets.
Aquaculture 181: 281 – 291
Bureau, D.P. (2010). Feather meal. Improving
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Abstrak
Satu kajian makanan selama 16 minggu telah dijalankan untuk mengkaji
perkembangan tumbesaran ikan tilapia hibrid merah (Oreochromis sp.) yang
memakan dua peringkat (10% dan 15%) makanan berasaskan tepung bulu
ayam. Makanan ikan yang berasaskan 10% dan 15% tepung bulu ayam dapat
menggantikan mil ikan dalam makanan ikan sebanyak 92% dan 100%. Selain
itu, parameter kualiti air dalam sistem air pengedaran semula juga ditentukan
setiap minggu. Tiga replikasi kumpulan tilapia diberi makan diet isoenergetic
(13.0 MJ/kg) yang mengandungi 29% protein hadam (isonitrogen) sebanyak
dua kali sehari. Ikan dengan saiz purata 37 g telah dipelihara selama 16 minggu
dalam tangki bulat sebesar 1 m3 dalam sistem air pengedaran semula. Adalah
ditekankan bahawa penambahan berat badan, kadar pertumbuhan tertentu dan
nisbah pertukaran makanan ikan tilapia merah yang makan 10% dan 15%
makanan bulu ayam adalah lebih baik (p <0.05) berbanding dengan kawalan
(sumber utama protein adalah daripada tepung kacang soya, tepung ikan dan
tepung gluten jagung). Tambahan pula, semua parameter air adalah dalam julat
optimum kualiti air untuk pertumbuhan tilapia. Perbezaan kecil tetapi signikan
(p <0.05) dalam pH, suhu air, NH3 dan NH4+ telah diperhatikan di antara
rawatan ikan yang makan tepung bulu poultri dan kawalan. Dapatan kajian ini
juga menunjukkan bahawa sehingga 15% tepung bulu ayam boleh dimasukkan
ke dalam diet ikan dengan prestasi pertumbuhan dan nisbah pertukaran
makanan yang baik. Selain itu, didapati juga bahawa makanan bulu ayam boleh
menggantikan tepung ikan dengan sepenuhnya dalam diet tilapia.
Wong, H.K. and Mardhati M. (2010). Protein
sources from poultry processing plants
for aquaculture production. Proceedings
of the 4th International Conference on
Animal Nutrition (ICAN), p. 353 – 356.
Selangor: MARDI