Journal of Applied Animal Research

ISSN: 0971-2119 (Print) 0974-1844 (Online) Journal homepage: http://www.tandfonline.com/loi/taar20

The effects of dietary bee pollen on lipid

peroxidation and fatty acids composition of
Japanese quails (Coturnix coturnix japonica) meat
under different stocking densities

Pınar Tatlı Seven, Aslıhan Sur Arslan, İsmail Seven & Zehra Gökçe

To cite this article: Pınar Tatlı Seven, Aslıhan Sur Arslan, İsmail Seven & Zehra Gökçe (2016)
The effects of dietary bee pollen on lipid peroxidation and fatty acids composition of Japanese
quails (Coturnix coturnix japonica) meat under different stocking densities, Journal of Applied
Animal Research, 44:1, 487-491, DOI: 10.1080/09712119.2015.1091339

To link to this article: http://dx.doi.org/10.1080/09712119.2015.1091339

© 2015 Taylor & Francis

Published online: 18 Oct 2015.

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 JOURNAL OF APPLIED ANIMAL RESEARCH, 2016
VOL. 44, NO. 1, 487–491
http://dx.doi.org/10.1080/09712119.2015.1091339

The effects of dietary bee pollen on lipid peroxidation and fatty acids composition of
Japanese quails (Coturnix coturnix japonica) meat under different stocking densities
Pınar Tatlı Sevena, Aslıhan Sur Arslana, İsmail Sevenb and Zehra Gökçec
a
Animal Nutrition and Nutritional Disease Department, Faculty of Veterinary Medicine Elazig, University of Firat, Elazığ, Turkey; bVocation School of
Sivrice, University of Firat, Elazig, Turkey; cFaculty of Science, Department of Biology, University of Firat, Elazig, Turkey

ABSTRACT ARTICLE HISTORY

The objective of this study was to investigate the effects of supplementation of bee pollen (1 g/kg) to the Received 13 March 2014
basal diet on lipid peroxidation and the fatty acids composition of Japanese quails under different Accepted 28 April 2015
stocking densities. Hundred and sixty Japanese quails were divided into 3 treatment groups each with
KEYWORDS
four replicates consisting of 8 birds in control group and 16 birds in the other groups. Experimental Quail; stocking density; lipid
groups were arranged as Control (160cm2/quail without supplementation), high stocking density (HSD) peroxidation; fatty acids; bee
(80 cm2/quail without supplementation), and POL (80 cm2/quail and 1g/kg bee pollen). Plasma pollen
Malondialdehyde level in the HSD group was significantly higher than those of Control and POL
Downloaded by [187.121.187.145] at 20:13 31 January 2016

groups (P < .01). The catalase activity in blood of Control and POL groups was significantly higher than
those of the HSD group(P < .01). In the HSD group the total polyunsaturated fatty acid (PUFA) ratio was
lowered in all tissues. Increased PUFA ratios were observed in breast muscle and kidney tissue
(P < .001), leg muscle (P < .05) and liver (P < .01) tissue in pollen-supplemented quails compared with
the other groups. The n–6 PUFA ratio of breast muscle, kidney tissue (P < .001) and liver tissue (P < .01)
was higher in the POL group than the other groups. As a result, the present study suggests that bee
pollen supplementation to 1 g/kg diet had potential protective activity on lipid peroxidation and tissue
fatty acid composition of quails reared under HSD. In all groups, the bee pollen consumption increased
PUFA levels in tissues, especially n-6 PUFA.

Introduction causes MDA (Malondialdehyde) generation (Simsek et al.

Poultry meat is consumed because of possessing extremely low
lipid content and high concentrations of polyunsaturated fatty
acid (PUFA)) (Yan & Kim 2013. Fatty acid composition of the diet
is a significant factor due to its affecting the fatty acid compo-
sition of the skeletal muscle of poultry that consume these diets
(Dalkilic et al. 2009). Natural supplements have been widely
used in the general population for health and well-being, and
potential therapy on certain disease and conditions (Kennedy
2005; Wang et al. 2007). In this regard, bee pollen is widely
used as a natural supplement, as it contains most of the essen-
tial elements needed for growth and developments in human
beings and animals (Bell et al. 1983; Orzaez et al. 2002; Hascik
et al. 2012). Bee pollen contains essential amino acids, proteins,
unsaturated fatty acids, anthocyanins, ferulic acids, pantothenic
acid, vitamins, minerals such as iron, manganese and zinc, and
trace elements (Campos et al. 2003; Mutsauers et al. 2005). Also
it contains significant amounts of flavonoids, carotenoids and
phytosterols (Campos et al. 2003). Flavonoids are polyphenolic
substances. Polyphenols have strong antioxidant capacity. They
are capable of scavenging free radical due to metal chelation
properties (Campos et al. 2003; Abdella et al. 2009; Teixeria
et al. 2010). Stocking density has been defined as the number
of birds being reared in a given housing area (Thaxton et al.
2006). It is an important environmental factor just like tempera-
ture, humidity, etc. (Faitarone et al. 2005; Celik et al. 2010).
Stocking density may enhance oxidative destruction and
2009). It has been reported in some studies (Seven et al. 2011;
Khalil & El-Sheikh 2012) that pollen has antioxidant effects
against lipid peroxidation caused by free radicals.
The aim of the present study was to determine the effects of
bee pollen on lipid peroxidation and fatty acids composition of
Japanese quails (Coturnix coturnix japonica) reared under differ-
ent stocking densities.
Material and methods
Animals and sampling
One hundred and sixty 3-day-old Japanese quails (Coturnix
coturnix japonica) were allocated to 3 treatment groups each
with 4 replicates consisting of 8 animals in the control and 16
animals in the other treatment groups. All of birds were
placed into cages with an internal dimension of 40×32 cm.
While quails in control group were reared at 160 cm2/quail,
both high stocking density (HSD) and bee pollen groups were
reared at 80 cm2/quail. The quails were fed with starter diets
for 21 days (Table 1). At 22nd day of experiment, experimental
groups were randomly divided into three groups and fed with
finisher diets for a period of 21 days. The pollen was obtained
from a commercial firm in Turkey. The experimental groups
were designed as no supplementing to finisher diet under
optimum stocking density (Control-C); no supplementing to fin-
isher diet under HSD; supplementing of 1g/kg bee pollen to

CONTACT Aslıhan Sur Arslan aslihansur01@gmail.com

© 2015 Taylor & Francis
 488 P. T. SEVEN ET AL

Table 1. Ingredient composition and chemical composition of the experimental Table 3. The fatty acid composition of pollen (% fatty acids).
diets (g/kg). Lipid numbers Name (%)
Ingredients Starter Finisher C12:0 Lauric acid 1.00
Maize 539.8 621.3 C14:0 Myristic acid 2.86
Soybean meal (%48) 266.3 – C16:0 Palmitic acid 23.98
Full fat soybean 124.8 276.5 C18:0 Stearic acid 3.57
Poultry meal 25 60 C22:0 Behenic acid 2.47
Soybean oil 9.4 14.3 ΣSFA 33.88
Limestone 11.9 2.9 C161n7 Palmitoleic acid 1.28
Bone meal – 16.5 C181n9 Oleic acid 8.42
Dicalcium phosphate 11.9 – C201n9 Eeicosenoic acid 0.89
Salt 3 2.1 C221n9 Erucic acid 2.89
DL-methionin 2.8 1.3 ΣMUFA 13.48
a
Vitamin–mineral premix 3.5 3.5 C182n6c Linoleic acid 18.93
Lysine 1.6 1.6 C182n6t Linoleic acid 0.32
Calculated content C183n6 Gamma linolenic acid 1.09
ME, kcal/kgc 3300 3030 C183n3 Alfa-linolenic acid 31.53
Dry matter, %b 89.40 90.50 C202n6 Eicosadienoic acid 0.16
b
Crude protein (CP), % 23.62 19.25 C205n3 Eicosapentaenoic acid 0.35
Aether extract, %b 6.1 8.9 ΣPUFA 52.38
Ash, %b 5.1 4.3
b
Crude cellulose, % 5.6 5.0
c
Calcium 10 10.2
Total phosphorusc 5.5 5.6 at −20oC until analyses. They were thawed at +4oC and
homogenized just before analysis.
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a
Vitamin–mineral premix provided per kilogram of diet: retinol, 4,5 mg; cholecal-
ciferol 0.125 mg; Alpha-tocopherol, 100 mg; menadione, 4 mg; thiamine, 3 mg;
riboflavin, 8 mg; niacin, 60 mg; pyridoxine, 5 mg; Ca-Dpantothenate, 18 mg; folic
acid, 2 mg; D-biotin, 0.20 mg; Mn, 100 mg; Zn, 80 mg; Fe, 80 mg; Cu, 8 mg; Co,
8mg; Se, 0.3 mg; Iodine, 1 mg, Mo,1 mg; choline chloride, 500 mg.
b
Analysed (AOAC, 1995).
c
Based on NRC (1994) feed composition tables.
finisher diet under HSD (POL). Corn and soybean meal-based
feeds were formulated to be isonitrogenic and isoenergic
according to the NRC (1994) recommendation. Pollen was
homogeneously mixed carefully to the basal diet. The
ingredients and chemical composition of the diets are
presented in Table 1. Chemical composition of feed
ingredients (dry matter, crude protein, aether extract and ash)
as dried samples was analysed using AOAC (1995)
procedures and crude fibre was determined by the methods
of Crampton and Maynard (1970). The fatty acid compositions
of diet and bee pollen were presented in Table 2 and Table 3,
respectively.
All groups were kept under the same environmental con-
ditions. Photoperiods of 23 h/day during 3–42 days of periods
were maintained. The chicks were raised in a temperature-con-
trolled room at 36°C for the first week. Thereafter, the tempera-
ture was reduced by 3 degrees each week to a minimum of 22
±2°C. Average relative humidity was determined as 65%. Feed
and water were given ad libitum. On 42nd day of the study 6
quails from each group with their body weight near the
group average were weighed and slaughtered. The blood,
breast, leg muscle, liver and kidney samples were collected.
Blood samples were taken into tubes containing anticoagulant
(2% sodium oxalate). The samples were centrifuged at 200 g for
5 min at +4°C; then the plasma was removed immediately and
stored at −20°C until analysed. The tissue samples were stored
Table 2. Fatty acid profiles of diet and feed additives (% fatty acids).
Starter Finisher
SFA 22.58 21.94
MUFA 30.54 21.93
PUFA 46.36 55.81
Note: SFA, saturated fatty acid; MUFA, monounsaturated fatty acid
MDA concentration in plasma, the end product of lipid per-
oxidation was measured according to the method of Satoh
(1978). MDA concentration in plasma was expressed as nmol/
ml. Catalase (CAT) activity was estimated by measuring the
breakdown of H2O2 at 240 nm according to the method of
Aebi, (1984). CAT activity in blood was expressed as kat/hHb.
Extraction of lipids from the tissue (kidney, liver, breast and
leg) samples, experimental diets (starter and finisher) and
pollen samples were performed according to the method by
Hara and Radin (1978). According to this method, 1 g of liver,
kidney and muscle (leg and breast) tissue and diet pollen speci-
mens were broken down in a Micra–D.8 homogeniser for 1 min
with 10 ml hexane isopropanol. The tissue homogenate was
centrifuged at 4500 rpm for 10 min to seperate the tissue
pellet. Fatty acid methyl esters were prepared according to
the methylation method by Christie (1992). Fatty acids in the
lipid extract were converted to methyl esters by 2% sulphuric
acid (v/v) in methanol. Fatty acids were analysed in SHIMADZU
GC 17 ver. 3 gas chromatography. A 25 cm-long MACHERY-
NAGEL (Germany) capillary colon with a 0.25 µm internal diam-
eter and a PERMABOND 25 µ film thickness was used in
analyses.
Statistical analysis
After normality test, Shapiro-Wilk, the data were subjected to
analysis of variance, significant differences were further sub-
jected to Duncan’s multiple range test (SPSS 2006). The
results were considered as significant when P values were
lower than 0.05.
Results and discussion
The PUFA ratio of pollen was higher than those of monounsatu-
rated fatty acid (MUFA) and saturated fatty acid (SFA) (Table 3).
Pollen
Dietary bee pollen supplementation showed positive effects on
33.88
13.48 stress, reducing lipid peroxidation due to antioxidant sub-
52.38 stances in its structure (Campos et al. 2003) and increasing
the PUFA level in some tissues due to high PUFA content in
 JOURNAL OF APPLIED ANIMAL RESEARCH 489

its structure (Table 3). The dietary PUFA supplementation can
exert benefits on antioxidative status, and alter the animal per-
formance and health (Chen et al. 2012). These results were con-
sidered to be due to the antioxidative capacity (Eraslan et al.
2009) and suitable fatty acids profile of bee pollen (Chen et al.
2012).
Poultry may be need antioxidant effective dietary sup-
plements or enzymes under stress while they only need to
creals-soybean based diets under normal conditions (Tatli
Seven et al. 2008; Kianfar et al. 2013; Makhdum et al. 2013).
Microclimate conditions around the birds deteriorate when
the number of birds per unit of space increases. They move
less and exhibit decreased walking ability, resulting in loco-
motion problems and difficulty accessing feeders and drinkers.
The birds have to spend more time standing than resting, which
results in social anarchy for resting birds. All of these problems
cause physical and physiological stress to the birds (Agarwal
et al. 2003; Seven et al. 2014b). The use of different manage-
ment practices, equipment and several dietary alternatives
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this effect by protecting the hepatocytes from the oxidative
stress and promoted the healing of the liver damage induced
by carbon tetrachloride toxicity. They analysed antioxidant
properties of chesnut bee pollen before the treatment and
determined that the chestnut bee pollen possessed many phe-
nolic compounds, which are the factors of high antioxidant
properties. It was reported that bee pollen supplementation
decreases markers of oxidative stress, enhancing the antioxi-
dant system of animals under stress (Khalil & El-Sheikh 2012).
Lipids mobilize from adipose tissue for increasing energy
needs during stress, especially unsaturated fatty acids
(Mumma et al. 2006). The total PUFA ratio of all tissues was
found to be lower in the HSD group (Table 5). Especially PUFA
ratios of breast and kidney tissue were lower than those in
other groups (P < .001). Lipid peroxidation causes reduction of
PUFA in the phospholipid fraction of the tissues (Morrissey
et al. 1994). Results of Mumma et al. (2006) are consistent
with our results, as given in Table 5. In the present study, the
total SFA ratio of leg muscle was higher in the HSD group

has been recommended to alleviate such an environmental (P < .01). Simsek et al. (2009) reported that a lower stocking
stress (Seven et al. 2014b).
The increasing MDA levels in plasma are an indicator of oxi-
dative stress. We determined that the MDA levels in plasma Table 5. Effects of bee pollen on fatty acid profile of muscle and inner organ
tissues under HSD conditions in Japanese quails (% fatty acids).
were significantly higher in the HSD group when compared
Characteristics Stocking Pollen P (Statistical
to the Control and POL groups (P < .01) (Table 4). In the
(%) Control density (HSD) (POL) significance)
present study, HSD decreased blood CAT (P < .01). POL sup-
Breast muscle (M. pectoralisprofundus)
plementation was significantly decreased MDA, while increased PUFA 46.56 ± 42.95 ± 0.90b 49.46 ± ***
CAT (Table 4). Living organisms are able to adapt to oxidative 0.62ab 0.35a
MUFA 21.02 ± 26.07 ± 1.09a 8.95 ± **
stress by inducing the synthesis of antioxidant enzymes and b
1.10 1.28b
damage removal/repair enzymes (Tatli Seven et al. 2009). In SFA 31.61 ± 30.03 ± 0.44 30.88 ± –
the present study, increasing of plasma MDA level and decreas- 0.71 0.98
N3-PUFA 8.38 ± 8.81 ± 0.32 8.58 ± –
ing of blood antioxidant enzymes activities (such as CAT) in the
0.51 0.49
HSD group may be evidence of oxidative stress that caused of N6-PUFA 38.18 ± 34.09 ± 0.65c 40.87 ± ***
HSD (Tatli Seven et al. 2009; Eraslan et al. 2009; Seven et al. 0.52b 0.38a
Leg muscle (M. gastrocnemius)
2014a). POL supplementation partially improves oxidative
PUFA 46.51 ± 44.21 ± 1.05b 45.24 ± *
stress caused by HSD. The present study results were in agree- 1.68a 3.72ab
ment with results of a study related to effect on MDA activity of MUFA 24.96 ± 24.12 ± 1.28 24.15 ± –
1.85 4.52
POL supplementation (Eraslan et al. 2009). Bee products contain
SFA 28.14 ± 31.04 ± 1.06a 30.58 ± **
numerous phenolic compounds (Khalil & El-Sheikh 2012; Feas 1.38b 1.32a
et al. 2012). As a bee product pollen is a good source of N3-PUFA 6.70 ± 6.51 ± 0.34 6.29 ± –
0.68 0.57
healty compounds such as phenolics. Bee pollen might be
N6-PUFA 39.80 ± 37.70 ± 0.87 38.95 ± –
suggested for useful properties in the prevention of disease in 2.48 2.15
which free radicals occur (Feas et al. 2012). Besides, it has Liver
PUFA 40.00 ± 35.08 ± 4.00b 47.39 ± **
been reported that bee pollen has metal chelation properties ab
2.71 1.61a
that react with free radicals (Abdella et al. 2009). Their function MUFA 26.93 ± 31.97 ± 3.67a 20.78 ± *
is to hunt down free radicals and neutralize them. In so doing, 2.20a 1.41b
SFA 30.66 ± 31.60 ± 1.26 31.79 ± –
they not only prevent free radicals from causing damage but
1.13 1.45
also repair any damages (Tatlı Seven et al. 2012). In a recent N3-PUFA 4.79 ± 5.23 ± 0.82 6.85 ± –
study, Yildiz et al. (2013) clearly showed that chesnut bee 0.78 1.74
N6-PUFA 35.21 ± 29.84 ± 3.19b 40.54 ± **
pollen had protective effects against carbon tetrachloride- a
2.91 1.20a
induced hepatic damage in rats. Chestnut bee pollen showed Kidney
PUFA 43.14 ± 34.11 ± 2.32b 45.57 ± ***
0.82a 1.02a
Table 4. Effects of bee pollen on MDA (µg/ml homojenat) and CAT (kat/hHb) MUFA 17.40 ± 19.82 ± 1.83 15.17 ± –
activities. 1.32 1.27
SFA 36.93 ± 43.74 ± 3.0a 35.27 ± *
Control Stocking density (HSD) Pollen (POL) P 1.25b 0.94b
MDA 2.66 ± 0.38c 4.43 ± 0.56a 3.38 ± 0.35b ** N3-PUFA 1.73 ± 1.41 ± 0.48 1.43 ±
CAT 4.12 ± 0.68a 2.60 ± 0.52b 3.46 ± 0.54a ** 0.29 0.56
a,b,c a,b,c
Mean values with different superscripts within a row differ significantly. Mean values with different superscripts with in a row differ significantly.
**P < .01. *P < .05, **P < .01, ***P < .001.
 490 P. T. SEVEN ET AL
density decreased the fat ratio of meat and increased the
protein ratio, total PUFA and n-3, n-6 fatty acid ratio. In accord-
ance with these reports, in the present study it was found that
the PUFA ratios of breast muscle and kidney tissue of the
control group were higher (P < .001) than those of other
groups. Also, total SFA ratio of kidney (P < .05) and leg muscle
(P < .01) tissues was higher in the HSD group than Control in
accordance with Simsek et al. (2009)’s study.
As given in Table 5, PUFA ratios of breast muscle were higher
in the POL than in Control and HSD groups (P < .001). The PUFA
ratio of kidney tissue was significantly higher in the POL than
that of HSD (P<.001). This result was found similar to the
Control group. In the present study, it was determined that
bee pollen had positive effects and increased n-6 PUFA levels.
N-6 PUFA ratios of breast muscle, kidney (P<.001) and liver
(P<.01) tissues were higher in the POL than those in HSD.
Total MUFA ratios of liver tissue were higher in the HSD
group than the pollen group (P < .01).
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Conclusion
In summary, the present study suggested that bee pollen sup-
plementation to 1 g/kg diet had potential protective activity on
lipid peroxidation and tissue fatty acid composition of quails
reared under HSD. Bee pollen supplementation increased
PUFA ratios in the tissues especially n-6 PUFA. Further studies
are needed to comprehensively assess biological activity,
quality and effects on toxicity.
Disclosure statement
No potential conflict of interest was reported by the authors.
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