Effects of dietary supplementation with natural carotenoid sources on growth performance and skin coloration of fancy carp, Cyprinus carpio L ...
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Iranian Journal of Fisheries Sciences 19(1) 167-181 2020
DOI: 10.22092/ijfs.2019.118784.
Effects of dietary supplementation with natural carotenoid
sources on growth performance and skin coloration of fancy
carp, Cyprinus carpio L.
Ninwichian P.1*; Chookird D.1; Phuwan N.1
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Received: August 2015 Accepted: August 2017
Abstract
We evaluated the effects of natural carotenoid sources on the growth performance and
skin pigmentation of Cyprinus carpio. Samples with mean initial weight of 51.235.04
g were fed with four experimental diets in quadruplicate for 8 weeks: A control diet
without carotenoid supplementation and three other diets with three different kinds of
natural carotenoid sources, Phafia rhodozyma, Paracoccus sp., and Haematococcus
pluviallis, at a level of 45 mg kg-1 total carotenoids. The growth and feed utilization
efficiency did not significantly differ between the dietary treatments (p>0.05). The
lightness (L*) in the red zone of the fish on the control diet tend to increase
significantly from the other treatments (p168 Ninwichian et al., Effects of dietary supplementation with natural carotenoid sources on…
Introduction xanthophylls, have been incorporated
Fancy carp (Cyprinus carpio L.) is one into fish diets for color enhancement
of the globally most popular ornamental (Gouveia et al., 2003; Kalinowski et al.,
fish species, and a wide variety of 2005; Kurnia et al., 2007; Yeşilayer et
colors and patterns have been classified al., 2011; Yuangsoi et al., 2011; Liu et
for this species (Tamadachi, 1990; al., 2014; Yi et al., 2014; Sornsupharp
Blasiola, 1995; Gomelsky et al., 1996). et al., 2015; Boonyapakdee et al.,
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The fancy carp with a white body and a 2015). However, the use of syntetic
red marking is one of the most popular carotenoids may have negative impacts,
among the color types (Kuroki, 1981; such as environmental deterioration and
Tamadachi, 1990). The skin carcinogenic effects, and they tend to
pigmentation of fancy carp is the most have a high cost (El-Baky et al., 2007;
important quality parameter Gupta et al., 2007; Sun et al., 2012;
determining the market value and Teimouri et al., 2013), so recent efforts
consumer acceptability. A frequent have emphasized the potential use of
problem found in fancy carp culture is coloring agents from alternative natural
that, the fish tend to lose their color as sources, such as fairy shrimps (Seidgar,
if fading when maintained in captivity, 2015; Seidgar et al., 2016), beetroots
and this decreases their market value (Devi et al., 2016) to replace the
(Yuangsoi et al., 2010). Therefore, syntetic chemicals. In prior studies the
several studies have been focused on natural compounds derived from red
improving the fish skin coloration. yeast, marine bacteria, and green algae,
Various factors were contributed to the were efficient as synthetic carotenoids
color intensity of aquatic animals, such for improving the skin pigmentation in
as the source and type of pigments, several ornamental fish species,
water temperature, brightness, feeding including goldfish (Carassius auratus)
rate, diet composition, species, size and (Gouveia et al., 2003; Xu et al., 2006),
physiological conditions (Leng and Li, Kenyi cichlids (Maylandia lombardoi)
2006). However, carotenoids that are (Karadal et al., 2017), and tomato
lipid-soluble pigments are the most clownfish (Amphiprion frenatus)
effective and consistent means to (Hekimoglu et al., 2017). Therefore, the
enhance the skin coloration in objective of the present study was to
ornamental fishes (García-Chavarría evaluate the effects of Phafia
and Lara-Flores, 2013). Since fishes are rhodozyma, Paracoccus sp., and
incapable of syntesizing carotenoids de Haematococcus pluviallis, as natural
novo in their body, so these pigments sources of carotenoids, on the growth,
must be supplied in the diet (Johnson feeding efficientcy and skin
and An, 1991; Gouveia et al., 2003; pigmentation of C. carpio. In addition,
Gupta et al., 2007). A variety of the total carotenoid concentrations
carotenoids from both natural and deposited in the skin, scales and serum
synthetic sources, such as astaxanthin, were also investigated. In case such
cantaxanthin, -carotene, lutein and natural carotenoid supplemented dietsIranian Journal of Fisheries Sciences 19(1) 2020 169
were effective on improving the skin The fish and their rearing conditions
pigmentation of fancy carp, the costs Mixed sex fancy carp were obtained
and concerns from using synthetic from a commercial fish farm in
carotenoids could be reduced without Nakornpatom province, Thailand.
loss of the market value, which depends Before these fish were transported to
on the pigmentation. conduct the feeding experiments at
Prince of Songkla University, Surat
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Materials and methods Thani campus, Thailand, they were first
Experimental diets raised in an earthen pond and fed with a
Four different experimental diets were commercial fancy carp diet. Before
used during the experimental period for starting the experiment on campus, the
8 weeks. A commercial herbivorous fish were fed with a control diet for 2
fish diet (Starfeed 5931TM, Charoen weeks to acclimatize them to the
Pokphand Foods Public Company rearing system, and to equalize
Limited, Thailand) without additional carotenoid contents in their bodies. A
pigment was used as the baseline or total of 256 individual fish with an
control diet. The three other diets were initial mean weight of 51.235.04 g
formulated to contain 45 mg kg-1 total were randomly divided into 16 indoor
carotenoids from three different natural tanks (300 L each) at a stocking density
pigment source, namely, P. rhodozyma of 16 fish per tank. Each group of fish
(Brineshrimpdirect Co., Ltd., USA), were stocked in a 75×75×60 cm3 indoor
Paracoccus sp. (Brineshrimpdirect Co., tank, and the freshwater flush rate was
Ltd., USA), and H. pluvialis 0.5 L min-1. Each dietary treatment was
(NaturoseTM, Cyanotech corporation, randomly assigned to four of the tanks,
USA). The supplement pigments were for four replicate treatment groups. The
in powder form, and were coated onto fish were fed their assigned
the surface of the basal diet by first experimental diets by hand three times
completely mixing with egg white (100 a day (8:00, 12:00, and 16:00) at the
g kg-1) and spreading evenly, while the feeding rate of 3% of their body weight
control diet was only coated with egg for 8 weeks. The amount of feed was
white. All the experimental feeds were adjusted every 2 weeks after the fish
air dried, stored in re-sealable bags at had been weighed. The mortality and
-20C, and kept away from light and the amount of feed used were recorded
moisture throughout the experiment. daily. During the feeding trial, the fish
The proximate analysis of the control were reared under natural photoperiod.
diet, amount of supplemented pigments The water temperature ranged from 26
and total carotenoid concentrations of to 28.5C, the dissolved oxygen was in
the experimental diets are given in the range from 7 to 10 mg L-1, and the
Tables 1 and 2. pH was 6.5-7.0; these parameters were
monitored daily. At the end of the
experiment, the fish were individually
weighed. The observations were used to170 Ninwichian et al., Effects of dietary supplementation with natural carotenoid sources on…
calculate the growth, the survival, and and then sacrificed with an overdose of
the feeding efficiency of fancy carp clove oil solution. A 300 µl blood
during the 8-week trial. sample was collected from each
individual, from the caudal vein with a
Skin color measurement 1 ml non-heparinized disposable
At the beginning and every 2 weeks syringe fitted with a 0.7×25 mm
after feeding experiment, a total of 3 disposable needle. The blood samples
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individual fish from each tank were for each replicate tank were pooled into
randomly selected and anesthetized a single tube, and allowed to clot on ice
using clove oil solution, to measure the before centrifugation at 300 g for 10
coloration on red and white zones of the min to separate out the serum. The
fish skin using a tristimulus colorimeter serum (200 µl per replication) was
(SC80B, Sino Age Development transferred to an empty tube and
Technology Ltd., Beijing, China). The vortexed with 400 µl of ethanol for 30s,
color was assessed in terms of L*, a*, before 800 µl of petroleum ether was
and b*, where L* represents the added to the mixture and vortexed for 1
lightness with range from 0 for black to min. The petroleum ether was then
100 for white. The +a* expresses red separated by centrifugation at 300 g for
while -a* indicates green, and +b* 10 min (White et al., 2002). The
represents yellow while -b* indicates absorbance of the supernatant was
blue, in accordance with the measured at 450 nm using a UV-visible
recommendations of the International spectrophotometer (U2900; Toshiba,
Commission on Illumination (The Tokyo, Japan). The total carotenoid
International Commission on concentration was estimated using the
Illumination (CIE), 1977). The hue (H) specific extinction coefficient E1%, 1cm=
and the chroma (C*) values were 2,500 with Beer Lambert’s law (Britton
calculated from a* and b*. The Hº is an et al., 1995).
angular measure of the visible colors in Skin and scales from the red and the
the electromagnetic spectrum, with 0, white zones were collected from three
30º, and 60º assigned to red, orange and individuals per replication for
yellow hue, respectively. The C* evaluating the total carotenoid
represents the intensity of a given color. concentrations. Samples representing
The transforms used were Hº= arctan each replicate tank were pooled
(b*/a*) and C*= (Hunt, separately for the white and the red
skin, and the scales, into re-sealable
1977).
bags covered with aluminium foil that
were stored at -20ºC until further
Sampling procedure and total
analysis. The total carotenoid analysis
carotenoid analysis
of the fish skin and the scales followed
At the end of the feeding trial, three
the method of Britton et al. (1995), with
individual fish from each replicate tank
minor modifications. Briefly, the
were first used for color measurement
sample was accurately weighed to 1.00Iranian Journal of Fisheries Sciences 19(1) 2020 171
g fresh weight, and homogenized in Results
acetone using a small mortar and a Treatment effects on growth and feed
pestle until the sample appeared utilization efficiency
colorless. After homogenizing, the solid The effects of the experimental diets on
debris have been removed out by the growth performance and feed
filtering through a small pad of cotton utilization efficiency were shown in
wool. The filtered mixture was Table 3. There were no significant
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transferred to a separating funnel and an differences in WG, SGR, FCR or PER
equal volume of diethyl ether was between the treatments (p>0.05). The
added. After that, the mixture was average WG values, relative to initial
mixed gently, then two volumes of weight, across the experimental diets
water were added to the mixture, gently were in the range from 0.69 to 0.84.
mixed and set aside for a while until the The SGR values varied from 0.95 to
mixture was separated into two phases. 1.31. The FCR ranging from 2.4 to 3.11
The upper phase was collected, then the was related to the PER, from 1.69 to
maximum absorbance was determined 2.15. The survival rates by treatment
over the wavelength range 350-550 nm. were between 92% and 96%.
The maximum absorbance value (
max) was used to estimate the total Treatment effects on the body color
carotenoid concentration using the intensity
specific extinction coefficient E1%, The effects of experimental diets on the
1cm=2,500 (Britton et al., 1995). lightness (L*), redness (a*), yellowness
(b*), hue (Hº), and chroma (C*) values
Statistical analysis of fancy carp were shown in Table 4
All results are presented as meanSE. and in Figs. 1 and 2. There were no
All the data were subjected to a one- significant differences in the L*, a*,
way analysis of variance (ANOVA) and b* values for the red zone between
using SPSS 15.0 for Windows, and the dietary treatment groups at the
Tukey’s test was used to determine beginning of the experiment (p>0.05)
significant differences between (Fig. 1). The L* for the red zone of fish
individual means used in assessing the fed with the control diet tended to
total carotenoids in experimental diets increase during the feeding trial, and by
and the effects of the dietary treatments. the end of the experiment it was
The differences were considered significantly higher than the other
statistically significant when p172 Ninwichian et al., Effects of dietary supplementation with natural carotenoid sources on…
sp. (22.32±1.50), and H. pluvialis Total carotenoid contents of
(21.73±1.34), respectively (Fig. 1B). integuments and serum
Moreover, the b* values of the red zone Effects of the experimental diets on the
showed no significant differences total carotenoid deposition in the fish
between the dietary treatments skin, the scales and the serum were
throughout the trial (p>0.05) (Fig. 1C). presented in Table 5. Samples of both
In terms of the white zone, no white skin and scales showed no
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significant differences in the L*, a*, significant effects, while the carotenoid
and b* values were observed between concentrations in the red skin and scales
the dietary treatment groups at the had significant differences between the
beginning of the experiment (p>0.05) experimental diets. The diet with H.
(Fig. 2). During the feeding trial, the L* pluvialis gave the highest carotenoid
for the white zone of fish fed with the levels in both red skin (53.05±1.77) and
control diet tended to decrease and by scales (35.60±0.69), while the control
the end of the feeding trial, it was the group had the lowest levels (pIranian Journal of Fisheries Sciences 19(1) 2020 173
red scales with R2=0.90, while such decrease in Hº of the red scales with
change in deposition matched a R2=0.92 (p174 Ninwichian et al., Effects of dietary supplementation with natural carotenoid sources on…
Table 5: Effects of the different diets on the total carotenoid concentration in the skin,
the scales, and the serum of fancy carp, after 8 weeks of treatment
Total carotenoids Dietary supplement
(mg kg-1) Control P. rhodozyma Paracoccus sp. H. pluvialis
a a a
White skin 10.75±1.58 12.88±0.85 11.68±1.68 13.56±1.62a
Red skin 42.15±0.13b 49.45±2.24ab 52.73±4.95a 53.05±1.77a
White scales 5.21±0.51a 5.63±1.21a 5.24±0.73a 4.79±0.60a
Red scales 26.27±2.17b 35.07±0.90a 33.20±2.32ab 35.60±0.69a
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Serum (µg ml-1) 1.07±0.03a 1.50±0.13a 1.51±0.14a 1.30±0.16a
Data represent as mean±SE. Different superscripts in the same row indicated significant
differences at pIranian Journal of Fisheries Sciences 19(1) 2020 175
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Figure 2: The mean values of L*, a*, and b* on the white
skin zone for the four experimental diets observed at
0, 2, 4, 6, and 8 weeks. Different capital letters
indicate significance with p176 Ninwichian et al., Effects of dietary supplementation with natural carotenoid sources on…
(Sparus aurata) (Gomes et al., 2002), of pigment supplementation in the feed
red porgy (Pagrus pagrus) (Chatzifotis caused a slight decrease in redness on
et al., 2005; Kalinowski et al., 2005), the skin over the first 4 weeks, followed
goldfish (Yeşilayer et al., 2011) and by a significant drop over the rest of the
large yellow croaker (Larimichthys trial. During carotenoid suspension, the
croceus) (Yi et al., 2014). However, in fish cannot synthesize carotenoids in
some studies a dietary carotenoid their body. Therefore, the initial
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supplement improved the growth and carotenoid contents continuously
feed utilization efficiency in fish (Liang decreased, due to utilization in
et al., 2012; Sun et al., 2012). intermediary metabolism and other
functions, and this affected the skin
Effects of carotenoid supplemented redness. A similar result to this study
diets on color parameters has been reported by Yuangsoi et al.
The color parameters have been widely (2010), who also observed that
used to quantify fish skin coloration. In carotenoid suspension decreased the
this study the inclusion of natural redness of fish skin. We note that, in
pigment in the diets significantly our case, it took at least ten weeks for a
improved skin pigmentation. The fish significant drop in the skin
fed with P. rhodozyma containing diet pigmentation, appearing as faded color.
had the highest a* and C*, and the The b* value indicates the purity of
lowest L* and Hº in the red zone, while white skin, with higher b*
the control group had the lowest a* and corresponding to more yellowness. The
C* and the highest L* and Hº. fish fed with P. rhodozyma in the diet
Interestingly, the red zone a* values of did not significantly differ from the
fish fed with the control diet tended to other treatment groups in the b* value.
decrease during the trial, while the Meanwhile, the L* values on the red
carotenoid supplementation maintained zone of fish fed with dietary pigments
or improved skin redness. The were significantly lower than the fish
continuous decrease in the skin redness fed with the control diet, especially so
of the fish fed with the control diet may with the P. rhodozyma diet. This is
be explained by the effects of probably related to the progressive
carotenoid suspension in a control accumulation of carotenoid pigments in
group. Since the fish had been raised in the red zone. Similar results with
an earthen pond, which contained a decreasing L* during carotenoid
variety of phytoplanktons, and fed with supplementation have been reported in
a commercial fancy carp diet for a long rainbow trout (Oncorhynchus mykiss)
period of time before they were used in (Teimouri et al., 2013) and large yellow
the experiment. Thus, fish had croaker (L. croceus) (Yi et al., 2014).
accumulated carotenoids from Furthermore, Pérez-Escalante et al.
phytoplanktons and mainly from the (2012) and Liu et al. (2014) have been
commercial fancy carp diet, prior to the reported that carotenoid
dietary treatments of the trial. The loss supplementation may stimulateIranian Journal of Fisheries Sciences 19(1) 2020 177
chromatophore production and increase Carotenoid accumulation in fish skin,
the pigment granules in scales and serum
chromatophores, thus ultimately The efficiency of carotenoid deposition
increasing the fish coloration. in some specific tissues, organs or
Additionally, these chromatophore specific positions of the fish skin is
quantities on the fish tissues were dependent on various factors, including
dependent on the body zone (Pérez- the fish species, the carotenoid sources,
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Escalante et al., 2012). quantities of chromatophores, and the
Overall, the fish fed with P. distribution pattern and carotenoid
rhodozyma in the diet had the most deposition capacity (Barbosa et al.,
redness in their skin color among all the 1999; Liang et al., 2012; Pérez-
dietary treatments. This indicates that Escalante et al., 2012; Liu et al., 2014;
the fish may utilize P. rhodozyma more Yi et al., 2014). In our results, there
efficiently than the other experimental was no significant difference for
diets to improve skin pigmentation. carotenoid accumulations in the skin,
Such effects may be the result of cell scales, or serum among fish fed with
wall disruption of P. rhodozyma before carotenoid supplemented diets. This
inclusion into the fish feed which suggested that these dietary pigments
enhance carotenoid bioavailability, and had a similar accumulation of
facilitate digestion and assimilation by carotenoids. When we considered the
the digestive tract. A similar total carotenoid concentrations across
explanation has been reported by all dietary treatments, the carotenoids
Johnson et al. (1980) who demonstrate were more deposited in the skin than in
that trout fed with fully disrupted yeast the scales, as well as more in the red
showed more improvement in their than in the white zones. These results
pigmentation than those fed with only were in agreement with the study of
partially disrupted red yeast. Moreover, Liang et al. (2012) who state that
since carotenoid in P. rhodozyma is carotenoids in fancy carp were mainly
accumulated in the lipid droplets of deposited in the skin more than in the
cytoplasmic membranes (Johnson and scales. The possible explanation for
An, 1991), these lipid droplets may these observations is that the deposition
improve the absorption of the lipid capacity of carotenoids and the
soluble pigments as reported by presence of chromatophores may be
Guerden et al. (1998). The cell wall higher in the skin than in the scales and
disruption and the lipid droplets of P. also may be higher in the red than in the
rhodozyma therefore may increase white zones. Besides the factors
carotenoid absorption in fancy carp, mentioned above, the number of
leading to the most improvement in the adipose cells and the fat deposition
skin redness as observed in the current levels in the fish may also affect the
study. efficiency of carotenoid deposition as
described by Qiufen et al. (2012). In
addition, Mahboob et al. (2014)178 Ninwichian et al., Effects of dietary supplementation with natural carotenoid sources on…
reported that the fat content in C. the Aquatic Animal Biotechnology
carprio is higher in the skin than in the Research Center, Faculty of Science
scales. These suggested that the fat and Industrial Technology, Prince of
content of the skin may facilitate the Songkla University, Surat Thani
accumulation of lipid soluble pigments, Campus, Thailand.
leading to more carotenoid deposition
in the skin than in the scales as References
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