Performance, egg quality and serum parameters of Japanese quails fed diet
supplemented with Spirulina platensis
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5857
PERFORMANCE, EGG QUALITY AND SERUM
PARAMETERS OF JAPANESE QUAILS FED DIET
SUPPLEMENTED WITH SPIRULINA PLATENSIS
Sibel Canogullari Dogan1,*,Mikail Baylan2, Zeynep Erdogan3, Gulsen Copur Akpinar4,Altug Kucukgul5, Vesile Duzguner6
1Omer Halisdemir University, Ayhan Şahenk Agricultural Sciences and Technologies Faculty, Department of Animal Production and Technologies, Nigde, Turkey
2Cukurova University,Agriculture Faculty, Department of Animal Production, Adana, Turkey
3Trakya University, Vocational Collage of Arda, Department of Food Processing, Aysekadin Campus, Edirne, Turkey 4Mustafa Kemal University, Agriculture Faculty, Department of Animal Production, Hatay, Turkey 5Mustafa Kemal University,Faculty of Veterinary Medicine, Department of Biochemistry, Hatay, Turkey
6Ardahan University, School of Health Sciences, Ardahan, Turkey
ABSTRACT
This experiment was conducted to evaluate the influence of Spirulina platensis on growth performance, egg quality and some serum parameters of laying Japanese quails. For this experiment, 100 ten weeks-old, female Japanese quails (Coturnix coturnix Japonica) with similar body weight were caged individually and were randomly divided into four groups of 25 quails each. Quails were fed diets supplemented with 0 (control), 0.5, 1.0 and 2.0% Spirulina platensis for 8 weeks.
Spirulina platensis addition did not affect feed
conversion ratio, feed intake, egg production, egg weight, shape index, eggshell thickness and haugh unit, significantly (P>0.05). However, there were significant differences (P<0.05) in final body weight, yolk index, albumen index and eggshell weight of experimental groups. There were significant differences (P<0.05) between groups in low density lipoprotein (LDL cholesterol) and high density lipoprotein (HDL cholesterol) concentrations. The LDL cholesterol concentration decreased while HDL cholesterol concentration increased with the increased supplementation of Spirulina platensis.
Spirulina platensis supplementation also decreased
plasma total cholesterol and trigyliceride levels between groups numerically but not statistically (P>0.05). The mean egg yolk cholesterol levels dropped by 19.65 and 18.93% in the 1.0 or 2.0%
Spirulina platensis supplemented groups compared
with control group. In conclusion, Spirulina algae can be used safely in laying quails diets with important effects on serum parameters and egg yolk cholesterol.
KEYWORDS:
egg quality, japanese quails, performance, serum parameters, spirulina platensis
INTRODUCTION
Spirulina is a type of multicellular and
filamentous cyanobacterium which can colonize environments that are unsuitable for many other organisms, forming populations in freshwater and brackish lakes and some marine environments, mainly alkaline saline lakes [1]. Spirulina has a history of human consumption dating as far back as
the 16th century, where it has been reported that
Aztecs harvested algal biomass resembling Spirulina to be consumed as part of their diet [2]. Spirulina is generally regarded as a rich source of protein, vitamins, essential amino acids, minerals, essential fatty acids like γ-linolenic acids (GLA) and antioxidant pigment like carotenoids [3,4]. Spirulina has a level of 62 % amino acid content and it is also regarded as the world’s richest natural source of
vitamin B12 and contains a whole spectrum of natural
mixed carotene and xanthophyll phyto pigments which together with phycocyanin, seem to be related to its antioxidant activity. In addition, highly unsaturated fatty acid (e.g., eicosapentaenoic acid, arachidonic acid and docosahexaenoic acid) content is of major importance [5]. Therefore spirulina is gaining more attention because of its nutritional and various medicinal properties [6,7,8].
Spirulina can be considered as a nutritional
supplement that has various health benefits for humans, and a feed supplement for animals having economic benefits [8,9]. Spirulina platensis's lipid extracts present a promising potential as an accessible and safe alternative to synthetic antioxidants and antimicrobials [10]. Colla et al. [11] showed that the potential of biomass Spirulina to decrease the serum levels of total cholesterol and to increase the serum levels of HDL-cholesterol, considered as a protective factor against the development of atherosclerosis.
Spirulina or its extracts have
5858 [14]. Spirulina has been shown to be an effective means of altering chicken product quality to meet consumer preferences. For instance, the total cholesterol content of eggs can be lowered by including Spirulina into layer hen diets [15]. This is mainly due to Spirulina’s high antioxidant and
omega-3polyunsaturated fatty acids (PUFA)
contents that enriches the nutritional value of eggs at the expense of cholesterol content [15,16]. Egg yolk colour has also been found to intensify linearly with increased dietary Spirulina levels [15, 17]. The effect of Spirulina on yolk color is attributed to its high level content of zeaxanthin, xanthophylls and other carotenoid pigments, particularly β-carotene, which accumulate into the yolk [18,19].
However, there are few researches about the usage of Spirulina as a feed supplement in laying Japanese quails. The aim of this work is to study the effects of dietary Spirulina platensis as a feed supplement on egg quality, performance and serum parameters in laying Japanese quails.
MATERIALS AND METHODS
Animals, Diets and Feeding Treatments. A hundred of 10-weeks old female Japanese quails (Coturnix coturnix Japonica) with similar body weight were randomly divided to four groups, each comprising of 25 quails. The birds were individually maintained in 16 x 26 x 25 cm cages in a well-ventilated room with artificial illumination for 16 hours/day. Water and feed were available for ad
libitum consumption.
The isocaloric and isonitrogenous experimental diet was formulated to meet the nutrient requirements for laying quails [20]. The ingredients and composition of the diet (200 g crude protein and
2800 kcal ME kg–1) are presented in Table 1. Diets
were supplemented with 0 (control), 0.5, 1.0 or 2.0% level of Spirulina platensis. The experiment was conducted for 8 weeks.
TABLE 1
Composition of experimental diets (%)
Spirulina platensis in diet (%)
0 0.5 1.0 2.0 Maize 35.024 34.923 34.820 34.619 Soybean Meal 15.000 15.000 15.000 15.000 Sunflower Meal 10.800 10.741 10.670 10.541 Full-Fat Soybean 10.000 10.000 10.000 10.000 Maize Gluten 7.153 6.681 6.209 5.266 Wheat Bran 4.188 4.417 4.646 5.105 Spirulina Powder 0.000 0.500 1.000 2.000 Vegetable Oil 7.957 7.930 7.957 8.010 Limestone 8.547 8.465 8.382 8.217 Salt 0.300 0.300 0.300 0.300 Choline chloride 0.235 0.235 0.235 0.235 Soda 0.177 0.140 0.104 0.031 DCP-18 0.098 0.100 0.103 0.107 Lysine Sulphate 0.159 0.149 0.138 0.116
Methionine
0.103 0.114 0.125 0.148 Vitamin Premix* 0.200 0.200 0.200 0.200 Mineral Premix** 0.100 0.100 0.100 0.100Calculated nutrient content, %
ME (kcal/kg) 2800 2800 2800 2800 Crude Protein, % 20 20 20 20 Crude Fiber, % 4 4 4 4 Calcium 3.5 3.5 3.5 3.5
Available
phosphorus
0.38 0.38 0.38 0.38 Methionine 0.48 0.49 0.49 0.50 Met &Cys 0.84 0.84 0.84 0.84 Lysine 1.00 1.00 1.00 1.00 Sodium 0.18 0.18 0.18 0.18 Potassium 0.82 0.82 0.82 0.82*Each kg of vitamin premix contains: 15 000 000 IU retinol; 5 000 000 IU cholecalciferol; 100 000 IU tocopherol; 5 000 IU phytonadione; 4 000 IU thiamine; 10 000 IU riboflavin; 5 000 IU pantothenic acid; 30 IU cyanocobalamin 50.000 mg l-ascorbic acid; 60 000 mg niacin; 18.000 mg calcium d-pantothenate; 2 000 mg folic acid; 250 mg biotin
**Each kg of mineral premix contains: 100 000 mg manganese; 80 000 mg iron; 100 000 mg zinc; 10 000 mg copper; 200 mg cobalt; 1 500 mg iodine 200 mg selenium
5859 TABLE 2
Effect of Spirulina platensis on the performance of Japanese quail
Spirulina platensis Supplementation (%)
Parameters 0 0.5 1.0 2.0 P
Initial Body Weight (g) 358.80±6.317 358.91±6.215 358.20±6.055 358.04±6.333 1.000
Final Body Weight (g) 383.68±7.101ab 398.04±11.625a 381.40±6.115ab 371.48±8.166b 0.180
Feed conversion ratio 3.18±0.068 3.14±0.042 3.07±0.042 3.12±0.043 0.463
(kg feed kg egg-1) Feed intake 2252.7±46.59 2276.05±48.50 2223.10±36.86 2281.43±48 0.795 ( g/bird/8 wk) Egg number (n) 1264 1268 1266 1280 Egg weight 13.97±0.102 14.21±0.076 14.17±0.094 14.06±0.096 0.260 (g/bird/8 wk) Egg production (%) 92.12±0.84 90.57±0.87 90.88±0.96 92.35±1.03 0.439
ab: Means with the different superscript within row are significantly different (P<0.05).
Growth Parameters. Laying quails were weighed at the beginning and end of the experiment. Feed consumption was recorded weekly and feed efficiency was calculated during the 8-weeks of experimental period. The value of feed efficiency was calculated as kg feed/kg of egg. Eggs were collected weighed daily. Egg production was calculated on a hen/day basis. Mortality was recorded as it occurred.
Throughout the experimental period, 12 eggs were collected from each group on weekly basis to determine the egg traits. The length, width and weight of each egg were recorded followed by the measurement of height of the thickest part of the albumen and yolk. The overall width and length were measured by using a compass. A calibrated micrometer was used for measuring the thickness of the eggshell, reported as the mean of three different sides, as mm.
The yolk index (YI) was calculated as follows:
YI= h w
Where h is the length and w the width, in mm.
The albumen index (AI) was calculated as follows:
2
/
)
(
100
w
l
h
x
AI
With h = height, l = length and w = width (in mm)
The Haugh unit (HU) values (8) were calculated by the formula:
37 . 0
7
.
1
57
.
7
log(
100
h
G
HU
)h = height of albumen (mm), G = weight of egg (g). Egg Yolk Cholesterol and Serum Analysis. Ten eggs were collected from each experimental group in the middle and at the end of the experiment to determine their cholesterol concentrations. Eggs were hard-boiled to separate the yolk. Cooked yolk weights were recorded. Cooked yolk was extracted
and subsequently analyzed for cholesterol
concentration on a per yolk basis. The cholesterol
content of the egg yolk was determined using the methods of Biochemical Analysis and Food Analysis [21].
Ten quails were randomly selected at the end of the experiment to determine serum parameters. Blood samples were collected into tubes containing EDTA, which acts as an anticoagulant. Plasma samples were separated by centrifugation at 2 000 rpm for 10 minutes. The total cholesterol, triglyceride, HDL and LDL concentrations in serum
were measured using a Shimadzu 1200
spectrophotometer and kits and calibrators from Diasis Diagnostic Systems (Turkey).
Statistical analysis. Data were statistically analyzed using the One Way ANOVA procedure of SPSS (release 17) with Duncan’s Multiple Range Test to identify the significant differences between the means.
RESULTS AND DISCUSSION
Layer Performance. The effects of Spirulina
platensis on the performance of laying quails are
shown in Table 2. The supplementation of Spirulina
platensis had no significant effect (P>0.05) on feed
conversion ratio, feed intake, egg number, egg weight and egg production. In agreement with the present study, Ross and Dominy [17], reported that growth of the chicks fed with the spirulina diets (0, 1.5, 3.0, 6.0, or 12.0% of spirulina) was not different from that of the chicks receiving the control diet. Same researchers used Japanese quail to test the effects of 0, 1.5, 3.0, 6.0, and 12.0 % of Spirulina on growth and egg production of the F1 generation of dams. They reported that there were no significant differences due to the Spirulina content in any of the parameters studied. Venkataraman et al. [22] also explained that Spirulina platensis did not affect the performance of broilers. In contrast to our study Mariey et al. [14] showed that birds fed with 0, 0.10, 0.15 or 0.20% Spirulina-diets achieved superior
5860 TABLE 3
Effect of Spirulina platensis on the quality of quail eggs Spirulina platensis Supplementation (%)
Parameters 0 0.5 1.0 2.0 P Shape Index 76.78±0.408 77.22±0.375 76.70±0.393 76.88±0.439 0.808 Haugh Unit 98.18±0.449 97.43±0.587 97.40±0.475 97.09±0.617 0.534 Yolk Index 47.48±0.322ab 47.52±0.408ab 46.78±0.356b 48.45±0.436a 0.024 Albumen Index 17.02±0.401a 15.77±0.369b 15.09±0.271b 15.71±0.396b 0.002 Eggshell thickness (mm) 0.199±0.002 0.201±0.002 0.198±0.002 0.207±0.002 0.062 Eggshell Weight (g) 1.55±0.022b 1.64±0.017a 1.63±0.022a 1.68±0.0.15a 0.000
ab: Means with the different superscript within row are significantly different (P<0.05).
significantly means of egg production rate, daily egg mass and feed conversion ratio to those of the control group. Kaod [23] investigated the effects of dietary supplementations of prebiotic (Lactose and Myco) and Spirulina platensis on broiler performance and found that body weights, average daily weight gain, carcass yield percentage and feed conversion rate were significantly (P<0.05) increased by the dietary inclusion of the prebiotic and Spirulina platensis as compared to the control diet fed broilers.
The effects of Spirulina platensis on the egg traits of laying quails are shown in Table 3. The results show that inclusion of Spirulina platensis had no significant effect (P>0.05) on egg shape index and Haugh unit. However, there were significant differences (P<0.05) in egg albumen index, egg yolk index, egg shell thickness and egg shell weight. The effect of dietary Spirulina platensis on egg traits had been reported previously by Zahroojian et al. [24]. In contrast to the present study Zahroojian et al. [24] reported that the supplementation of Spirulina
platensis had no significant effect (P>0.05) on egg
traits when laying hens were fed 0, 1.5, 2.0 and 2.5%
Spirulina platensis. Mariey et al. [14], Hasin et al.
[25] and Ross and Dominy [17] also observed no significant differences in egg quality characteristics with Spirulina supplemented diets.
Egg shell weight increased with increasing level of Spirulina supplementation (P<0.05). This may be due to the effects of high calcium content of
Spirulina [26]. Williamson and Burkitt [27]
explained that the calcium content of Spirulina is 26 times folder that of milk.
Egg Yolk Cholesterol. Egg yolk cholesterol concentrations per gram of yolk decreased (P<0.05)
with 1.0 or 2.0% Spirulina platensis
supplementation to diet (Table 4). These results indicate that, compared with a control diet, the mean egg yolk cholesterol levels dropped by 19.65 and 18.93% in the 1.0 or 2.0 % Spirulina platensis supplemented diets. Mariey et al. [14 ] reported that there were significant (P<0.05) reductions in yolk cholesterol as the level of dietary Spirulina was increased. This reduction in cholesterol contents may be related to their lower levels in blood plasma of hens fed the Spirulina-containing diets. Sujatha
and Narahari [15 ] also reported that the total cholesterol content of eggs can be lowered by including Spirulina into layer hen rations. This is mainly due to Spirulina’s high antioxidant and omega-3 polyunsaturated fatty acids (PUFA) contents that enriches the nutritional value of eggs at the expense of cholesterol content (Sujatha and Narahari, 2011). In contrast to our study Zahroojian et al. [24] reported that the supplementation of
Spirulina platensis had no significant effect (P>0.05)
on egg yolk cholesterol when laying hens were fed with 0, 1.5, 2.0 and 2.5% levels of Spirulina
platensis.
Serum Parameters. The effects of Spirulina
platensis supplementation on serum parameters of
laying quails are shown in Table 4. Spirulina
platensis supplementation did not significantly affect
plasma cholesterol and triglyceride concentrations (P>0.05). However, compared with a control diet, 0.5, 1.0 or 2.0 % Spirulina platensis reduced plasma triglyceride concentration by 2.08, 17.29 and 18.51% respectively. These results are in line with those obtained by Mariey et al. [14] who reported significant decrease (P<0.05) in blood plasma concentrations of cholesterol, and triglycerides with the supplementation of Spirulina. Nagaoka et al. [13] investigated the hypocholesterolemic action of
Spirulina platensis concentrations (SPC) in rats.
They reported that serum cholesterol concentrations were significantly lower in rats fed SPC than in those fed casein. The hypocholesterolemic action of SPC may involve the inhibition of both jejunal cholesterol absorption and ileal bile acid reabsorption. In another experiment Colla et al. [11] reported that Spirulina has an effect to decrease the serum levels of total cholesterol in rabbits.
The levels of plasma high density lipoprotein (HDL-cholesterol)) concentration in laying quails fed diets containing 0.5, 1.0 and 2.0% Spirulina
platensis were higher than that of the fed with the
control diet (P<0.05). The levels of low density lipoprotein (LDL-cholesterol) concentration in laying quails decreased with Spirulina platenis supplementation. Similarly, Nagaoka et al. [13] reported that the serum HDL cholesterol
5861 TABLE 4
Effect of Spirulina platensis on serum parameters (mg/dl) and egg yolk cholesterol (mg/g)
Spirulina platensis Supplementation (%)
Parameters 0 0.5 1.0 2.0 P
Plasma cholesterol 230.64±16.69 236.39±14.00 204.09±14.66 195.17±20.50 0.259
Plasma triglyceride 516.60±37.44 505.81±30.15 427.27±40.22 420.97±13.76 0.091
HDL 123.47±8.38c 141.14±11.09bc 162.63±7.90ab 168.22±4.89a 0.007
LDL 74.99±11.69 63.25±2.65 54.16±2.15 53.40±1.13 0.072
Egg yolk cholesterol 38.88 ±1.22a 39.43±1.36a 31.24±1.94b 31.52±1.07b 0.000
ab: Means with the different superscript within row are significantly different (P<0.05).
concentration was significantly higher in the group fed SPC than in the casein group in rats.They explained that serum LDL-cholesterol concentration was significantly lower in the group fed with SPC. Colla et al. [11] also reported that HDL-cholesterol concentration decreased in rabbits fed with
Spirulina. They also explained that the decreased t
serum levels of total cholesterol and increased serum levels of HDL-cholesterol, can be considered as a protective factor against atherosclerosis.
CONCLUSION
The results of this study clearly demonstrate that Spirulina platensis has potential benefits as a feed additive in reducing plasma and egg cholesterol concentrations in laying quails. Spirulina platensis up to 2% in diet can be used as a hypocholesterolemic agent in practical laying quail diets when low cholesterol egg is desired in the human diet.
ACKNOWLEDGEMENTS
This research was supported by the Mustafa Kemal University the Scientific Research Projects Unit with 08 V 0102 project number.
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Received: 26.01.2016
Accepted: 08.09.2016
CORRESPONDING AUTHOR Sibel Canogullari Dogan
Omer Halisdemir University, Ayhan Sahenk Agricultural Sciences and Technologies Faculty,
Department of Animal Production and
Technologies, 51240, Nigde, Turkey e mail: sibelcanogullari@gmail.com
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