Pakistan J. Zool., vol. 51(4), pp 1489-1496, 2019. DOI: http://dx.doi.org/10.17582/journal.pjz/2019.51.4.1489.

1496

Hydrolyzed Chicken Feather Meal as Protein

Source for Red Tilapia (Oreochromis sp.)
Aquafeeds
Nursinatrio and Rudy Agung Nugroho*
Animal Physiology, Development and Molecular Laboratory, Department of Biology,
Faculty of Mathematics and Natural Sciences, Mulawarman University, Indonesia

ABSTRACT Article Information

Received 03 March 2018
An 84-day feeding trial was conducted to determine the effects of Hydrolyzed Chicken Feather Meal Revised 22 May 2018
(HCFM) supplementation on the growth, feed efficiency, survival rate and carcass composition of red Accepted 20 July 2018
tilapia (Oreochromis sp). A group of red tilapias (initial weight 24.09 ± 0.05 g) were fed 3, 6, 9 and 12% Available online 15 May 2019
HCFM as a supplement and compared to a control group without supplementation. After 84 days, growth
Authors’ Contribution
parameters such as body weight gain (BWG), average weekly gain (AWG), daily weight gain (DWG), N surveyed the location and collected
specific growth rate (SGR), feed conversion ratio (FCR), feed efficiency (FE), protein efficiency ratio the data. N and RAN analyzed the
(PER), survival rate (SR) and carcass proximate of red tilapia were measured. The results showed that data and wrote the manuscript.
HCFM up to 12% could be used as supplementation and showed positive effects on all growth parameters.
Supplementation of HCFM above 6% in the red tilapia diet increased the protein and fat content of red Key words
tilapia’s carcass. The highest survival was found on red tilapia fed 9% HCFM supplementation in the diet. Hydrolyzed chicken feather meal,
The current study also found that supplementation of HCFM in the diet is possible for red tilapia without Growth parameters, Oreochromis sp.,
Carcass composition, Survival rate.
impairing growth, feed intake, survival rate or carcass composition. Altogether, the results suggest that
HCFM is an optional ingredient which can be used as an alternative for fish meal in aquafeed for red
tilapia.

INTRODUCTION been found to have considerable economic potential to

replace FM. Chicken feathers can be used for animal feed

F ish meal (FM) plays an important role as an ingredient

for fish feed (Caruso, 2015) and is known as a prime
protein source of high quality and is a very digestible
because they have high protein content, which comprises
80–90% dry matter and exceeds the raw protein content of
soybean meal (42.5%) and fish meal (66.5%). Moreover,
feed ingredient (Miles and Chapman, 2006; Tantikitti proximate analysis of chicken feathers found the following
et al., 2016). Approximately 30% of total fish caught compositions: crude lipid (0.83%), crude fiber (2.15%),
are converted to FM and fish oil (Barroso et al., 2014). crude protein (82.36%), ash (1.49%), NFE (1.02%) and
However, there is a limitation in the production of FM moisture content (12.33%) whereas ultimate analyses
due to an increasing price of this source (FAO, 2010; resulted in carbon (64.47%), nitrogen (10.41%), oxygen
García-Romero et al., 2014; Kurbanov et al., 2015). (22.34%) and sulphur (2.64%) (Tesfaye et al., 2017).
Although FM is still a favourite among fish farmers, the However, chicken feather meal only has the digestibility
search for potential alternative ingredients has become a of dry and organic matter in vitro, respectively at 5.8% and
well-recognized priority for sustainable development of 0.7% because it has a fiber-shaped protein type (fibrous
the aquaculture industry. The use of poultry to replace protein). Thus, chicken feathers must be hydrolyzed to
FM that is often scarce, expensive, of limited availability, improve digestibility (Bureau et al., 1999) and can be
and which leads to high fish production costs provides an used as a protein source in fish diets such as red tilapia
alternative approach and has been gaining momentum. (Oreochromis sp.). Previous research noted that the used
Replacing FM with cheaper ingredients such as of poultry by product has been conducted in some fish
chicken feather meal is a priority for nutrition research. research such as Koi fish, Anabas testudines (Bloch)
Chicken feather is waste from slaughterhouses that has (Bhaskar et al., 2015), golden pompano (Trachinotus
ovatus) (Wang et al., 2017) and juveniles of European
* Corresponding author: rudyagung.nugroho@fmipa. seabass (Dicentrarchus labrax) (Campos et al., 2017).
unmul.ac.id However, there has been limited research on the effects of
0030-9923/2019/0004-1489 $ 9.00/0 dietary HCFM as a protein source on the growth, survival
Copyright 2019 Zoological Society of Pakistan and feed efficiency of red tilapia.
1490 Nursinatrio and R.A. Nugroho

Tilapia are generally placed as the second most were measured daily with a routine thermometer, an HM-7
commonly used aquaculture fish in the world (Fitzsimmons, pH meter (pH 110, Eutech Instrument Cyberscan, Thermo
2010) and reached more than 5,000,000 metric tons of Scientific, Illinois, USA) and a DO meter (YSI 550A
global production in 2016 (Fitzsimmons, 2016). As one Clandon, Ohio, USA). Nitrate, nitrite and ammonium
of the important species in Indonesia aquaculture, the were measured and recorded weekly using chemical test
production of tilapia has also increased gradually in some kits (Rochelle Salt Solution and Nessler Reagent, HACH,
Indonesian regions such as South Sumatera, West Java and Loveland, Colorado, USA).
East Kalimantan (Widiarti, 2015). Meanwhile, red tilapia
are one of the most popular freshwater and economically Diet preparation
important food fish, and have high protein levels (Nakphet All raw materials for control and test diets were
et al., 2017; Pauly and Zeller, 2017; Roslan et al., 2014). prepared, weighed and mixed with a Getra mixer (B20-F
Red tilapia can be cultivated with several advantages volume 20 L Series R10240, China). A pelleting machine
such as rapid growth, ease of breeding and resistance was used to obtain wet strands that were of 3 mm diameter.
to pests and diseases as well as being able to adapt to Both control and test diets were dried in an oven (30ºC),
environmental changes; they are popular for both local allowed to cool at room temperature, and stored at 27ºC
and export markets. The production of red tilapia can be throughout the experimental period. Determination of
accelerated by providing feed containing high quality feed composition proximate analysis including dry matter,
nutrients in accordance with the requirements of fish to crude protein, crude fat and ash was performed. The
increase growth in shorter time periods. compositions of the control and test diets are shown in
To evaluate growth performance and health of fish, Table I.
various physiological tools such as body weight gain
(BWG), average weekly gain (AWG), daily weight gain Table I.- Ingredient and proximate composition of
(DWG), specific growth rate (SGR) (Nur et al., 2017; control and trial diets.
Yusup and Nugroho, 2017), feed conversion ratio (FCR)
(Fum et al., 2017), feed efficiency (FE) (Moutinho et al., Ingredients Types of diet with hydrolyzed feathers
2017), protein efficiency ratio (PER) (Azaza et al., 2015), meal inclusion
survival rate (Cai et al., 2015) and carcass proximate Control 3% 6% 9% 12%
(Aryani et al., 2017) have been successfully used. Thus, Corn 26.00 23.00 20.00 17.00 14.00
the current study was designed to evaluate the effects of Wheat by product 18.01 18.00 18.00 18.00 18.00
dietary HCFM as a protein source on the growth, feed Soybean meal 17.64 18.31 18.65 19.00 20.20
efficiency, survival rate and carcass composition of red Sunflower meal 5.30 5.30 5.30 5.30 5.30
tilapia. Cassava starch 7.20 7.20 7.20 7.20 7.20
HCFM 0.00 3.00 6.00 9.00 12.00
MATERIALS AND METHODS Animal protein* 18.00 17.34 17.03 16.71 15.41
Fish meal 3.00 3.00 3.00 3.00 3.00
Animals and experimental setup
Mix oil 1.75 1.72 1.66 1.60 1.66
Three-month-old red tilapia (n=900) (average initial
Vitamin mix 0.25 0.25 0.25 0.25 0.25
weight 24.09 ± 0.05 g) were provided from local fish
Proximate composition (%)
breeding sources in Cirata, Cianjur West Java (Indonesia)
Dry matter 90.8 91.6 91.4 91.8 90.9
and acclimated at PT Suri Tani Pemuka, Cianjur West
Java, Indonesia for one week. The fish were then randomly Crude protein 35.5 36.0 36.7 37.4 37.4
distributed into five experimental groups, namely control Crude fat 5.1 5.2 5.0 4.8 4.6
and four diets supplied with 3, 6, 9 and 12% of HCFM. Ash 11.1 9.5 9.3 9.3 9.4
Each experimental group was in triplicate with 50 fish per *
Animal protein: Bone meal and blood meal.
replicate being 15 experimental pond cages. These cages
were randomly assigned to each group dietary treatment. Sampling and analytical procedure
The daily feed was divided into five parts (8, 10, 12 am, Body weights (BW) of fish from each tank were
2 and 4 pm) by using at satiation method. The fish were recorded at weeks 4, 8 and 12 of the experiment. At the end
fed until apparent satiation and the feeding experiment of the experiment, BWG, AWG, DWG, SGR (Nur et al.,
lasted for 84 days. To quantify the exact feed intake, 2017; Yusup and Nugroho, 2017), FCR (Fum et al., 2017),
refused feed was siphoned out immediately, dried and FE (Moutinho et al., 2017), PER (Azaza et al., 2015) and
weighed. Temperature, pH and dissolved oxygen (DO) SR (Cai et al., 2015) were measured.
1491 Growth Evaluation of Red Tilapia Fed Hydrolyzed Chicken Feather Meal 1491

Proximate analysis 3% also had significantly higher DWG than control diet.
To calculated carcass composition, fish was Meanwhile, SGR, FCR, FE and PER were not affected by
transformed into meal for a proximate standard test the supplementation of HCFM in the diet of red tilapia
(AOAC, 2005) by using a chemical test and NIRS (Table II). At the end of feeding trial, the lowest survival
automatic machine. Fish were measured for protein and rate was found for red tilapia fed with 12% of HCFM
fat contents. inclusion whereas the highest survival rate was shown for
the red tilapia fed control and 9% HCFM supplementation
Statistical analysis in the diet (Fig. 1).
Results were expressed as mean ± standard error
(SE). Proximate analysis and growth data were objected to
analysis of variance (ANOVA) using IBM SPSS Statistics
22 (SPSS, Inc., USA). Comparisons among treatment
means were carried out by one-way analysis of variance
followed by Duncan’s test. Standard Error (±SE) was
calculated to identify the range of means. Percentage
data were transformed by arc-sine transformation prior
to ANOVA and reversed afterwards. All significant tests
were at P<0.05 levels.

RESULTS

Growth, feed efficiency and survival rate

After 84 days of feeding trial, the BWG and AWG
of red tilapia fed dietary 12% of HCFM supplementation Fig. 1. Survival rate of red tilapia (Oreochromis sp.) with
were significantly higher (P<0.05) than red tilapia fed other different concentrations of hydrolyzed chicken feather
diets. The red tilapia fed dietary HCFM inclusion above meal inclusion (HCFM) for 12 weeks.

Table II.- Growth performance of red tilapia (Oreochromis sp.) with different concentration of hydrolyzed feathers
meal.

Parameters Hydrolyzed feathers meal inclusion

Control 3% 6% 9% 12%
BWG (g/fish) 77.56 ± 0.52a 64.43 ± 0.17b 80.93 ± 0.20c 83.96 ± 0.87c 84.20 ± 0.73d
AWG (g/fish) 6.46 ± 0.44a 5.36 ± 0.89b 6.74 ± 0.16a 6.99 ± 0.72a 7.01 ± 0.60c
DWG (g/fish) 0.92 ± 0.06a 0.76 ± 0.12b 0.96 ± 0.02c 0.99 ± 0.10c 1.00 ± 0.08c
SGR (%/day) 1.70 ± 0.13 1.53 ± 0.31 1.71 ± 0.04 1.78 ± 0.20 1.78 ± 0.17
FCR 1.74 ± 0.04 2.07 ± 0.15 1.86 ± 0.09 1.91 ± 0.16 1.75 ± 0.08
FE (%) 57.64 ± 1.54 48.43 ± 3.44 53.90 ± 2.83 53.24 ± 4.96 57.30 ± 2.86
PER 1.62 ± 0.04 1.35 ± 0.09 1.47 ± 0.07 1.42 ± 0.12 1.53 ± 0.07
Values are Means ± Standar error. Means in the same row having different superscript letters (a, b, c) indicated significant differences (P<0.05). BWG,
body weight gain; AWG, average weight gain; DWG, daily weight gain; SGR, specific growth rate; FCR, feed conversion ratio; FE, feed efficiency, PER,
protein efficiency ratio; SR, survival rate.

Table III.- Proximate analysis of hydrolyzed feathers meal of fish.

Parameters (%) Hydrolyzed feathers meal inclusion

Control 3% 6% 9% 12%
Crude protein 48.50 ± 0.25a 49.59 ± 0.05a 51.32 ± 0.12b 51.40 ± 0.03b 51.93 ± 0.27c
Crude fat 20.84 ± 0.15a 19.67 ± 0.18a 21.40 ± 0.22b 21.56 ± 0.21b 23.00 ± 0.11c
1492 Nursinatrio and R.A. Nugroho

Fish carcass composition Similarly, no effects on growth performance were found in

Table III shows carcass compositions (%/100 g wet Atlantic salmon (Salmo salar) fed diets with poultry meal
weight basis) of the red tilapia at the five levels of HCFM and blood meal in combination with poultry oil (Hatlen et
supplementation after the 84-day experimental period. al., 2015; Aryani et al., 2017).
Crude protein and crude fat of red tilapia fed 12% HCFM It is assumed that the amount of protein contained in
supplementation showed a high percentage after this 84- the feed that can be digested was sufficient to support fish
day period. growth. Growth may stop and a decrease in body weight
can occur if protein is deficient. Further, protein in the
Water quality parameter body system can be broken down to maintain more critical
Water quality parameters were recorded during the functions such as the immune system (Magnadóttir, 2006;
experiments along with their tolerable limits (Table IV). Uribe et al., 2011). In addition to protein metabolism,
Average temperature, pH, DO, nitrite and TAN for this low fish growth rates can occur due to the amount and
research were found to be at the tolerable limit. characteristics of keratin protein contained in feather meals,
and only a small amount of protein can be absorbed by
Table IV.- Water quality parameters. the body. Moreover, keratin proteins have a strong double
bond that inhibits breakdown by proteolytic enzymes in the
Parameters Mean± SE Tolerable limits digestive tract (Montes-Zarazúa et al., 2015; Sinkiewicz et
Temperature (o C) 22.13 ± 0.17 20.9 – 24.3 al., 2017). Growth values exceeding 1% indicate that the
pH 7.35 ± 0.25 6.5 – 9.0 amount of protein contained in the feed and digested by
the fish is sufficient, providing a balance of essential amino
DO (ppm) 5.70 ± 0.31 3-12
acids in the diet. In addition, specific growth rate is also
Nitrite (ppm) 0.17 ± 0.07 0.5
affected by the balance of nutrients in the diet that can be
TAN (ppm) 0.14 ± 0.02 0.5 digested by fish, particularly the amino acid content. These
results also indicate that the use of HCFM up to 12% is
DISCUSSION still acceptable by red tilapia.
Current findings also found that SGR, FCR, FE
Growth performance and PER of red tilapia fed any level of HCFM were not
Positive effects of growth of red tilapia were observed significantly different to the control. These findings
when fish were fed 12% HCFM in the diet. The body weight showed that a supply with 3–12% of HCFM in the diet of
of red tilapia also increased with the increasing level of red tilapia can be applied with no adverse effects on fish
HCFM. According to Grazziotin et al. (2008), Moritz and growth. This result is in accordance with previous research
Latshaw (2001) and Wiradimadja et al. (2014), chicken noting that replacing FM with other soy protein (33–100%)
feathers contain keratin proteins that have low digestibility. led to no significant difference in growth performance or
However, hydrolysis can increase digestibility to 54–76%. nutrient utilization of rainbow trout, Oncorhynchus mykiss
Further, the absorption of nutrients becomes more optimal (Kaushik et al., 1995). Moreover, protein efficiency
when consumed at high concentrations. This suggests that is influenced by several factors including fish size,
the use of HCFM as a protein source in aquafeeds could physiological functions of fish, feed quality and feeding
replace some other animal protein sources with the same rate. High PER values also indicate a good feed quality
result. This study also found that the 12% of HCFM supply (Cho, 1992; Council, 2011; De Silva and Anderson, 1994).
in the diet of red tilapia for 84 days resulted in higher BWG In addition, HCFM inclusion in the diet up to 12% reflects
(84.20 ± 0.73 g/fish), AWG (7.01 ± 0.60 g/fish) and DWG that the quality of this ingredient can match the value of
(1.00 ± 0.08 g/fish) than the control group. This finding the feed using animal protein meal, which is beneficial
is similar to previous research revealing that replacement because animal protein generally has high prices and
of fish meal by using poultry also increased fish growth materials that compete with human needs.
parameters such as in juvenile Nile tilapia (Oreochromis
niloticus) (Yones and Metwalli, 2016), juveniles of rainbow Survival
trout (Oncorhynchus mykiss) (Barreto-Curiel et al., 2016) Although 12% HCFM inclusion reduced survival of
and Japanese sea bass (Lateolabrax japonicus) (Wang et red tilapia to 92%, this survival rate was at an acceptable
al., 2015). Another current study, however, mentioned that level. This result is similar to past research finding that
poultry used as an FM replacement in the diet of juvenile substituted fish meal using another source of protein in
Black Sea Bass Centropristis striata from 40–90% led to the diet of Clarias gariepinus fingerlings (Djissou et al.,
no significant differences in BWG (Dawson et al., 2018). 2016) led to a high survival rate above 90% or similar
1493 Growth Evaluation of Red Tilapia Fed Hydrolyzed Chicken Feather Meal 1493

survival rate with control (100%) with respect to juvenile the protein content in the HCFM can be applied to increase
Ussuri catfish Pseudobagrus ussuriensis (Bu et al., 2017). the protein content in fish carcass, in comparison with red
In contrast, study replacement fish meal with soya protein tilapia fed without inclusion of HCFM.
concentrate on snakehead (Channa striata) showed lower
survival rates compared to control (Hien et al., 2017). Water quality
In addition, a previous study on the use of fermented The quality of water plays a pivotal role in the
feather meal as a fish meal replacement on the survival of growth of fish. These water parameters (temperature, pH,
Oreochromis niloticus revealed that the survival of the fish DO, nitrite and TAN) remained within the suitable range
was not affected by any concentration of fermented feather required for red tilapia (Alabaster and Lloyd, 1980; Hepher
meal substitution (Arunlertaree and Moolthongnoi, 2008). et al., 1983), and there were only minor differences among
Hence, complete nutrition in the feed provides energy the treatments. The average water temperature recorded
for the activity and survival of fish. The quality of feed is during the experiment was 22.13± 0.17 oC, which is in
determined by its nutrient content because fish utilize the a tolerable limit for red tilapia (20.9–24.3oC); pH was in
feed to obtain energy in accordance with their needs. a tolerable range (7.35± 0.25), the DO levels recorded
during the experiment were 5.70± 0.31 ppm and TAN was
Diet composition at an acceptable level (0.14± 0.02 ppm) that supports the
Diets were formulated to be optimal for growth life of the red tilapia. Overall, water quality parameters
and survival of red tilapia by inclusion of HCFM up to such as temperature, pH, DO, nitrite and TAN were found
12%, with no significant negative effects on fish growth to be favourable for fish growth and survival during the
performance and survival rate. The inclusion of HCFM trial.
might decrease diet costs, which explains the lower values
of cost for per-kg fish production. The present study CONCLUSION
revealed that diet composition with HCFM inclusion had
higher protein, low fat and ash content than a diet without Based on growth, feed efficiency, survival rate and
HCFM substitution. The higher protein in the diet supports carcass composition, the use of hydrolyzed chicken feather
and affects fish weight. Meanwhile, freshwater fish such meal up to 12 % is possible for red tilapia aquafeed without
as red tilapia often require fatty acids such as 18 carbon impairing growth and feed intake. The carcass composition
n-3 fatty acid and linolenic acid (18:3-n-3), in quantities (crude protein and crude lipid) of red tilapia was recorded
ranging from 0.5 to 1.5% of dry diet (Craig and Helfrich, to be highest at 6% of HCFM inclusion. Further research
2009). As a comparison, previous research suggests that should be conducted to determine the effects of prolonged
hybrid tilapia needs 5% crude fat for minimum growth feeding with current ingredients at high concentration.
and can be increased until 12% of crude fat for maximum
growth (Chou and Shiau, 1996). Further, ash is the result ACKNOWLEDGMENT
of combustion of organic materials in the form of minerals
and the lower ash content indicates that the feed is more The author(s) gratefully thank the Department of
easily digested by the fish. Biology, Faculty of Mathematics and Natural Sciences,
Mulawarman University, Indonesia; Mr Erwin Suwendi
Fish carcass composition and Ai Tety Nurbety from PT Suri Tani Pemuka, the
Generally, tilapia has a protein content of Aquaculture division research and development, and Japfa
approximately 19.04% and a fat content of 19.67–23.00% Comfeed Indonesia for technical and facilities in support
(Foh et al., 2011). The current results determined that red of the research.
tilapia fed 12% HCFM supplementation in the diet had the
highest protein (51.93%) and fat (23.00%) contents. This Statement of conflict of interest
finding is similar to previous research stating that tilapia The authors declare no conflicts of interest regarding
fed with 20% fish meal substitution had significantly the publication of this article.
higher total protein in their muscle compared to tilapia fed
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