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Aquaculture InternationalJournal of the European AquacultureSociety ISSN 0967-6120 Aquacult IntDOI 10.1007/s10499-014-9806-2
Feeding frequency influences growth,feed consumption and body compositionof juvenile rock bream (Oplegnathusfasciatus)
Sung-Yong Oh & B. A. Venmathi Maran
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Feeding frequency influences growth, feed consumptionand body composition of juvenile rock bream(Oplegnathus fasciatus)
Sung-Yong Oh • B. A. Venmathi Maran
Received: 4 March 2014 / Accepted: 9 June 2014� Springer International Publishing Switzerland 2014
Abstract The influence of feeding frequency on growth, feed consumption and body
composition of juvenile rock bream (Oplegnathus fasciatus) was investigated for 70 days
under an ambient water temperature (mean = 22.1 �C) in sea cages at Tongyeong, in the
southern part of Korea. A total of 600 juveniles were used in this experiment, from which
50 juveniles (initial mean body weight 11.6 g) per cage were randomly distributed to 12
cages. They were hand-fed to satiation with a commercial diet (42.5 % protein and 21.2 kJ/g
energy) at one of four different feeding frequency trials (one, two, three, and four meals per
day) with triplicates. At the end of the experiment, the mean final weight of fish fed one, two,
three and four meals per day were 46.3, 54.5, 60.7 and 60.1 g, respectively. The fish fed three
and four meals per day showed the highest specific growth and feeding rates. The feed
conversion ratio was not significantly (P [ 0.05) affected by the feeding frequency. The
extent of size variation in weight significantly (P \ 0.05) decreased with the increase of
feeding frequency. The maximum feed intake of fish appeared at the first meal (08:30) of
each treatment. As feeding frequency increased, lipid and energy contents also increased
significantly (P \ 0.05), but ash content decreased (P \ 0.05). The total nitrogen waste
output of fish was not significantly (P [ 0.05) affected by the feeding frequency. We con-
clude that the optimum feeding frequency aimed at optimized growth of juvenile rock bream
weighing from 10 to 60 g reared in sea cages is three meals per day under our experimental
conditions including particular diet and temperature.
Keywords Oplegnathus fasciatus � Feeding optimization � Feed intake � Aquaculture �South Korea
S.-Y. Oh � B. A. V. Maran (&)Marine Ecosystem Research Division, Korea Institute of Ocean Science and Technology,Ansan P.O. Box 29, Seoul 425-600, Koreae-mail: [email protected]; [email protected]
S.-Y. OhDepartment of Marine Biology, Korea University of Science and Technology, Daejeon, Korea
123
Aquacult IntDOI 10.1007/s10499-014-9806-2
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Introduction
An optimized feeding regime for maximal growth of fish is an important aspect for
commercial fish farming (Cho et al. 2003; Silva et al. 2007; Hafs et al. 2012; Oh et al.
2013). In relation to that, fish are commonly overfed by fish farmers without determining
the satiation point. This could easily lead to an increase in production costs and poor
environmental factors including water quality (Lee et al. 2000a; Cho et al. 2003; Biswas
et al. 2006). On the other hand, if fish are fed insufficiently, their growth is reduced and
size variation is enhanced (Jobling 1983; Wang et al. 1998; Lawrence et al. 2012).
Therefore, for successful fish culture, some economical feeding regimes need to be
developed to save feed costs without causing growth retardation and profit reduction (Silva
et al. 2007; Oh et al. 2013).
Feeding frequency plays a major role in regulating feed consumption, growth, and food
waste of fish (Wang et al. 1998, 2007; Xie et al. 2011). It is therefore important to
determine the optimal feeding frequency in order to (1) improve fish production, (2)
produce fish of uniform sizes, (3) minimize water pollution and (4) optimize economical
benefit (Wang et al. 1998; Kubitza and Lovshin 1999; Dwyer et al. 2002; Zhou et al. 2003;
Biswas et al. 2006; Kucuk et al. 2013). However, the influence of feeding frequency on fish
growth is depending on experimental species, size, feed composition, rearing conditions
and other factors (Wang et al. 1998; Lee et al. 2000a, b; Cho et al. 2003; Xie et al. 2011).
Such inconsistency suggests that the effect of feeding frequency on fish growth should be
analyzed in detail before practical suggestions are made for the daily practice.
The rock bream Opleganthus fasciatus (Temminck & Schlegel, 1844) is one of the most
popular and economically important fish in the marine aquaculture in Korea and Japan
because of its high market value and meat quality (Wang et al. 2003; Biswas et al. 2008;
Lim and Lee 2009). In Korea, the annual aquaculture production was ranged from 711 to
902 metric tons between 2010 and 2011 (MFAFF 2012). The hatchery-reared juveniles are
commonly cultured in sea cages, especially in the southern part of Korea until their growth
up to market size. A little attention has been paid to optimizing feeding management such
as feeding frequency in rock breams. Recently, in western Japan, researchers tried to
determine the most efficient feeding interval and photoperiod for the optimal growth of
rock bream (Biswas et al. 2010). A few more studies focused on the nutritional aspects to
improve the feed efficiency of rock bream (Wang et al. 2003; Lim and Lee 2009). Hence,
in this study, we investigated the effects on growth, size variation and feed consumption in
juvenile rock bream subjected to various feeding frequencies in order to determine opti-
mum feeding frequency for species reared in sea cages. To see the effect of feeding
frequency on the body composition and the nitrogen waste of the juveniles, we also
investigated the temporal changes in chemical attributes such as protein, lipid, energy, ash
and moisture contents.
Materials and methods
Experimental fish and conditions
The juveniles of O. fasciatus were obtained from a private hatchery (Shinyangsusan,
Tongyeong, Korea). All juveniles were transferred to a floating sea cage (10 9 10 9 6 m)
at Tongyeong Marine Living Resources Research & Conservation Center (TMRC) and
acclimated for 1 month. During acclimation, fish were hand-fed on a commercial diet of
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dry pellets (Aller Aqua Co., Christiansfeld, Denmark: 11.4 % moisture, 42.5 % crude
protein, 9.4 % crude lipid, 8.0 % ash and 21.2 kJ/g energy) to apparent satiation twice
daily.
During the feeding trial, water temperature, salinity, pH and dissolved oxygen were
monitored every day. Water temperature was maintained at 22.1 ± 1.7 �C. Salinity ranged
from 30.1 to 34.4 psu; dissolved oxygen was greater than 6.8 mg/L; and pH ranged from
8.0 to 8.3 throughout the experiment.
Experimental design and management
After acclimation, a total of 600 juveniles were divided into 4 groups from 12 numbers of
cages, and each group was randomly assigned to one of four different feeding frequency
trials. Each feeding frequency group consisted of 3 replicates with 50 juveniles [initial
body weight: 11.6 ± 0.1 g (mean ± SE, n = 12)] per cage (0.7 9 1.0 9 1.0 m). We
provided every day: (A) one meal at 08:30, (B) two meals at 08:30 and 17:30, (C) three
meals at 08:30, 13:00 and 17:30 and (D) four meals at 08:30, 11:30, 14:30 and 17:30,
respectively. During the experimental period, fish in all feeding treatment groups were fed
by hand on commercial dry pellets (same as during the acclimation period). Pellets were
dropped into each cage until the fish stopped to eat, and the container of the pellets was
weighed before the first feeding and after the last feeding in a day to record the daily
amount of feed that fish actually consumed. The feeding trial lasted for 70 days.
At the beginning and the end of the experiment, all the fish in each cage were fasted for
a day to empty their gut and then anaesthetized with 2-phenoxyethanol (Sigma, St. Louis,
MO, USA) solution (150 mg/L) to minimize stress before body weight measurements were
taken individually. Prior to measurement, the fish were dried by blotting with a paper towel
and then weighed to the nearest 0.1 g.
On day 69, the amount of feed consumed by the fish in each experimental cage at each
meal was measured to determine daily feed consumption patterns within the four feeding
frequency groups.
Chemical analysis
Chemical body composition was determined at the beginning and at the end of the
experiment. Thirty fish at the beginning of the experiment and 15 fish in each cage at the
end of the experiment were randomly sampled and stored at -30 �C for the analysis of
proximate body composition. Chemical composition of the experimental diet and fish were
analyzed according to the standard method (AOAC 1995). Crude protein content was
determined by the Kjeldahl method using an Auto Kjeldahl System (Foss Tecator, Hog-
anas, Sweden). Moisture content was measured by oven drying at 105 �C for 24 h. Crude
lipid was determined by the ether-extraction method, and ash content was determined by a
muffle furnace at 600 �C for 3 h. Energy content was determined by a bomb calorimeter
(PARR 1351, Moline, IL, USA).
Calculations and statistical analysis
Specific growth rate (SGR), feeding rate (FR), feed conversion ratio (FCR), protein
retention efficiency (PRE), energy retention efficiency (ERE), and total nitrogen waste
output (TNW) were calculated as follows:
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SGR ð%=day) ¼ 100� ½ln Wf=Nfð Þ�ln Wi=Nið Þ�=t
FR ð% body weight=day) ¼ 100 � D= Wf þWi þWdð Þ=2½ �=t ðOh et al: 2013Þ
FCR ¼ D= Wf�Wi þWdð Þ
PRE ð% ) ¼ 100� ðWfnf �Wi � Cni þWd � CniÞ= D� Cndð Þ ðWang et al: 2007Þ
ERE ð%Þ ¼ 100� ðWfef �Wi � Cei þWd � CeiÞ= D� Cedð Þ ðBiswas et al: 2010Þ
TNW ðgN=kg fish gain) ¼ 1;000� f D� Cndð Þ � ð1�PRE=100Þ=½ðWf�WiÞ � 6:25�gðWang et al: 2007Þ
where Wf and Wi are total final and initial weights (g), Wd is total body weight of the dead
fish, t is the experimental duration (d), Nf and Ni are final and initial numbers of fish, D is
the total amount of the consumed feed on a g-dry weight basis during t days, Cni (%) and
Cnf (%) are protein content in the whole fish body at the beginning and at the end of the
experiment, and Cnd (%) is protein content in the feed. Cei (%) and Cef (%) are energy
content in the whole fish body at the beginning and at the end of the experiment, and Ced
(%) is energy content in the feed.
The coefficient of variation (CV) of the initial (CVi) or final (CVf) weight was used to
determine the inter-individual variation among the fish in each cage: CVi
(%) = 100 9 (standard deviation of the initial weight/mean initial weight of the fish in
each cage) and CVf (%) = 100 9 (standard deviation of the final weight/mean final
weight of the fish in each cage).
Data associated with final body weight, SGR, FR, FCR, PRE, ERE, TNW, CV, feed
consumption and body protein, lipid, ash, moisture and energy contents were subjected to
one-way ANOVA followed by a Duncan’s multiple range test (P \ 0.05) with a 95 %
significance level to compare the means when differences occurred, except feed con-
sumption of fish with two meals daily was subjected to a t test to evaluate the daily feed
consumption pattern. Levene’s test was used to check homogeneity of variance, and
percent data were arcsine-transformed before ANOVA and t test. All statistical analyses
were carried out using an SPSS program (SPSS Michigan Avenue, Chicago, IL, USA). The
data presented are mean ± SE of three replications.
Results
The experimental results revealed that survival rate was 96.2 ± 0.6 % (mean ± SE,
n = 12) and not significantly (P [ 0.05) affected by the feeding frequency. Final body
weight, SGR, FR and FCR of juvenile rock bream fed at different feeding frequencies for
70 days are presented in Table 1. Final body weight, SGR and FR of the fish fed three and
four meals per day were significantly (P \ 0.05) higher than those of fish fed one and two
meals per day, but were not significantly (P [ 0.05) different between three and four meals
per day. There were no significant (P [ 0.05) differences in FCR among the treatments fed
at different feeding frequencies, although the treatment fed three meals per day had a
relatively low FCR compared with the treatments fed one, two and four meals per day.
At the beginning of the experiment, size variation (i.e., CVi = 7.2 %) in fish weight
among the treatments had no significant (P [ 0.05) difference (Table 1). However, at the
end of the experiment, the CVf in fish weight of four meals per day (CVf = 9.2 %) was
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Ta
ble
1In
itia
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dfi
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GR
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ple
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ays
Tre
atm
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Init
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wei
gh
t(g
/fish
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inal
wei
ght
(g/fi
sh)
SG
R(%
/day
)F
R(%
/day
)F
CR
CV
i(%
)C
Vf
(%)
1m
eal/
day
11
.9±
0.2
46
.3±
0.5
a1
.95
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a2
.24
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11.8
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4.5
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1.3
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.2±
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11
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eals
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.7c
2.3
9±
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1.2
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27
.2±
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9.8
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11.3
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.6c
2.3
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2.5
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1.3
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17
.2±
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9.2
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.4a
Val
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(mea
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ith
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t(P
\0
.05
)
Aquacult Int
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significantly (P \ 0.05) lower than those in fish weight of one (CVf = 11.1 %) and two
(CVf = 11.0 %) meals per day. But, this was not significantly (P [ 0.05) different from
that of fish fed three meals (CVf = 9.8 %) per day.
Daily feed consumption patterns of fish fed with different feeding frequencies showed a
similar tendency among the treatments (Fig. 1). The feed consumption of fish fed two,
three and four meals per day was significantly (P \ 0.05) higher at the feeding time of
08:30 than at other feeding times. Fish fed three or four meals per day consumed similar
feed amounts at each feeding time except at 08:30.
At the end of the feeding trial, chemical attributes (protein, lipid, ash, moisture and
energy contents), PRE, ERE and TNW of rock bream were calculated (Table 2). The body
composition was increased for crude protein and lipid from initial to final sampling in all
treatments. However, it was decreased for moisture and ash contents. Contents of moisture
and crude protein of the whole body of rock bream were not significantly (P [ 0.05)
affected by the feeding frequency. However, fish fed one meal per day showed a signifi-
cantly (P \ 0.05) higher ash content and lower crude lipid, energy and ERE than fish fed
two, three and four meals per day. There were no significant (P [ 0.05) differences in
crude lipid, ash and energy contents among the fish fed at two, three and four meals per
day. The PRE and TNW of fish was not significantly (P [ 0.05) affected by the feeding
frequency, although the fish fed at three meals per day had a relatively high PRE and low
TNW.
Discussion
The enhanced growth and feeding rates of fish experiencing increased feeding frequency
were demonstrated by several studies (Jobling 1983; Ruohonen et al. 1998; Zhou et al.
2003; Wang et al. 2007). In the present study, we could reveal that SGR and FR of juvenile
rock bream were significantly increased with up to three meals per day. At the same time, a
further increase in feeding (i.e., four meals per day) did not enhance the growth rate of
juveniles.
Our results demonstrated that the optimum feeding frequency for juvenile rock bream
weighing from 10 to 60 g was three meals per day (Tables 1, 2), because at this frequency
the fish had a relatively high SGR, FR, PRE and ERE, but low FCR compared with one,
two and four meals per day. The optimum feeding frequency for fish growth varies largely
depends on the fish species and size. For instance, the juveniles of Korean rockfish (Se-
bastes schlegelii, average initial weight 5.7 g) fed one meal a day grew faster and used feed
more effectively than two meals a day or one meal every 2 days (Lee et al. 2000b). In
contrast, the optimum feeding frequencies of juveniles of yellowtail flounder (Limanda
ferruginea, initial weight 6.8 g), hybrid sunfish (F1 hybrid of female green sunfish Lepomis
cyanellus 9 male bluegill L. macrochirus, initial weight 7.4 g), ayu (Plecoglossus altiv-
elis, initial weight 0.15 g), and gibel carp (Carassius auratus gibelio, initial weight 3.0 g),
were reported to be two meals (Dwyer et al. 2002), three meals (Wang et al. 1998), four
meals (Cho et al. 2003), and 24 meals (Zhou et al. 2003) per day, respectively. Our FCR
result that was not affected by feeding frequency is well agreed with other observations of
Korean rockfish fed moisture pellets (Lee et al. 2000b), channel catfish (Ictalurus punct-
atus) reared in a cage (Webster et al. 1992), mrigal (Cirrhinus mrigala) and rohu (Labeo
rohita) reared in a nursery (Biswas et al. 2006) and flounder (Platichthys flesus luscus)
reared in a indoor tank (Kucuk et al. 2013). These reports indicated that feed consumption
was the growth-limiting factor of fish that experienced various feeding frequencies
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(Andrews and Page 1975). Therefore, enhanced growth in the fish fed three meals per day
in the present study was achieved by the improvement of FR, not by the improvement of
FCR.
0
1
2
3M
ean
feed
con
sum
ptio
n (%
bod
y w
eigh
t)
0
1
2
3
0
1
2
3
0
1
2
3
Time (h)
a
b
a
b ba
bb b
1 meal/d 2 meals/d
3 meals/d 4 meals/d
08:30 11:30 14:30 17:30 08:30 11:30 14:30 17:30
08:30 11:30 14:30 17:30 08:30 11:30 14:30 17:30
Fig. 1 Daily variation in mean feed consumption at four feeding times of juvenile rock bream fed at fourdifferent feeding frequencies. Values (mean ± SE) with different letters are significantly different (n = 3,P \ 0.05)
Table 2 Whole body proximate composition (%, wet weight basis), energy content (kJ/g), protein (PRE)and energy (ENE) retention efficiencies and total nitrogen waste (TNW) of juvenile rock bream Oplegnathusfasciatus fed at four different feeding frequencies for 70 days
Parameters Initial 1 meal/day 2 meals/day 3 meals/day 4 meals/day
Moisture 75.3 ± 0.4 72.4 ± 0.0 73.0 ± 0.4 73.2 ± 0.6 73.3 ± 0.3
Crude protein 16.2 ± 0.1 16.3 ± 0.2 16.3 ± 0.1 16.5 ± 0.4 16.6 ± 0.3
Crude lipid 4.7 ± 0.0 5.7 ± 0.2a 6.2 ± 0.1b 6.4 ± 0.1b 6.2 ± 0.1b
Ash 4.6 ± 0.0 3.8 ± 0.1b 3.3 ± 0.0a 3.4 ± 0.1a 3.4 ± 0.0a
Energy 5.1 ± 0.2 5.5 ± 0.1a 6.6 ± 0.2b 6.6 ± 0.0b 6.5 ± 0.7b
PRE (%) 29.0 ± 0.1 29.5 ± 0.9 30.7 ± 0.5 30.0 ± 0.2
ERE (%) 19.9 ± 0.1a 25.3 ± 0.7b 25.7 ± 0.4b 24.4 ± 0.1b
TNW (gN/kg fish gain) 63.8 ± 0.3 62.6 ± 2.6 60.1 ± 1.3 62.5 ± 0.5
Values (mean ± SE, n = 3) with different superscripts in the same row are significantly different(P \ 0.05)
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In this study, the CV in weight was increased in all treatment groups at the end of the
experiment (CVf) compared with initial (CVi). However, inter-individual size variation
decreased with increasing feeding frequency, which is consistent with some of the previous
studies (Wang et al. 1998; Liu and Liao 1999). Thus, the increase in feeding frequency
from one to four meals per day provided more uniform size in hybrid sunfish (Wang et al.
1998). In the case of juvenile gilthead seabream (Sparus auratus), size variation depended
on feeding frequency as well as on dry feed particle size (Goldan et al. 1997). However,
few reports showed that feeding frequency did not affect size variation of juvenile gibel
carp (Zhou et al. 2003), white sturgeon (Acipenser transmontanus) (Cui et al. 1997), and
flounder (Kucuk et al. 2013).
Information on feed consumption pattern is necessary to achieve an optimized feeding
regime for particular fish species (Wang et al. 1998). In the present study, the daily feed
consumption pattern of juvenile rock bream indicated that the greatest ratio of feeding
activity in fish occurred in the morning time (i.e., 08:30) and became more uniform feeding
ratio when fish were fed at higher feeding frequencies (i.e., three or four meals per day)
after maximum feed intake. Similarly, hybrid sunfish (Wang et al. 1998) and flounder
(Kucuk et al. 2013) showed more uniform feeding ratio at higher feeding frequencies, but
maximal feeding activity changed depending on feeding frequency. The fish fed at lower
feeding frequencies daily consumed more feed during each meal (Dwyer et al. 2002). The
ingested ratio related to feeding frequency depends on the stomach volume (Grayton and
Beamish 1977; Jobling 1983; Ruohonen and Grove 1996), feeding intervals (Liu and Liao
1999; Biswas et al. 2010), and gastric evacuation rate (Lee et al. 2000b). The data con-
cerning the daily feed consumption pattern will provide important information associated
with the feeding time and the supplied amounts of feed in each feeding for improved
growth of juvenile rock bream.
The increase in the body lipid content with feeding frequency in the present study is
similar to other fish species (Grayton and Beamish 1977; Kayano et al. 1993; Yao et al.
1994; Lee et al. 2000a, b), but another study with same species did not show any significant
increase in different feeding intervals and photoperiods (Biswas et al. 2010). The surplus
feed ingested by frequent feeding was found to be converted into body lipid in the post-
larvae of ayu (Cho et al. 2003), as well in juvenile flounder (Paralichthys olivaceus) (Lee
et al. 2000a). However, Harpaz et al. (1999) reported that the body lipid content of juvenile
silver perch (Bidyanus bidyanus) was affected by dietary energy levels and not by feeding
frequency.
Commercial fish farming in sea cages is recognized as one of the causes of water
deterioration through TNW originated from uneaten or wasted feed, fecal and metabolites
of cultured fish (Islam 2005; Wang et al. 2007). The nitrogen waste production in fish
farms is directly affected by the feeding regime (Azevedo et al. 1998), which has an
inverse correlation with feed utilization in fish (Wang et al. 2007). Wang et al. (2007)
further suggested that nitrogen waste can be minimized by regulating feeding frequency
and estimated that about 50 g nitrogen waste is released into the water by 1 kg of cuneate
drum (Nibea miichthioides) offered for one meal per day. This amount of nitrogen waste is
comparable with our results with three meals per day (about 60 g).
In this study, based on growth performance, size variation, feed consumption and
nitrogen waste of juvenile rock bream, it is concluded that the optimum feeding frequency
for growth of juvenile rock bream of 10–60 g body weight was three meals per day under
our experimental conditions. In addition, the fish fed with three meals per day produced a
relatively low TNW compared with other feeding frequencies. This also means that three
meals per day provided appropriate intervals for optimal growth of juvenile rock bream. At
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the same time, water pollution was minimized in sea cages, which is essential for an eco-
friendly culture.
Acknowledgments We thank Mr. David Berry for language editing and two anonymous reviewers fortheir constructive comments. We also thank TMRC colleagues for their generous assistance in the field. Thefunding was supported by the Korea Institute of Ocean Science and Technology (KIOST) projects (PO01110and PE99202).
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