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Bee pollen improves productivity of laying Japanese quails

Pólen apícola melhora a produtividade de codornas Japonesas em postura

SUMMARY

This study aimed to evaluate the effects of bee pollen (BP) on the performance of laying Japanese quails and egg quality. A total of 60 quails were used in a completely randomized experimental design with four treatments (0%, 0.5%, 1%, and 1.5% BP inclusion in diets) and five replicates. At the end of the study, productive performance and egg quality were evaluated; 160 eggs were maintained at different temperatures based on a completely randomized design and factorial arrangement (4 × 2), with four BP levels (cited above) and two storage temperatures (room temperature and refrigeration) for 14 days, totaling eight treatments with four replicates. BP levels did not influence (P> 0.05) feed conversion; however, daily feed intake, laying rate, egg mass, and weight and percentage of albumen increased. Yolk percentage decreased due to the augmentation of BP in diets. There was no effect (P> 0.05) of interaction of storage temperature × BP levels on egg quality, except with regard to the Haugh unit. BP supplementation resulted in higher egg weight and index of yolk and albumen. Refrigerated eggs had better internal quality than normal eggs. BP inclusion in diets of Japanese quails improved bird performance and the quality of fresh and stored eggs.

Keywords:
animal nutrition; additive; bee product; egg production; poultry feeding

RESUMO

Este estudo teve como objetivo avaliar o efeito do pólen apícola sobre o desempenho de codornas Japonesas em postura e sobre a qualidade dos ovos. Foram usadas 160 codornas em delineamento completamente casualizado com quatro tratamentos (0%, 0,5%, 1%, e 1,5% de pólen apícola nas dietas) e cinco repetições. Ao fim do estudo, o desempenho e a qualidade dos ovos foram avaliados. Posteriormente, 160 ovos foram mantidos em temperaturas diferentes em delineamento completamente casualizado e arranjo fatorial 4 × 2, com quatro níveis de pólen apícola (citados acima) e duas temperaturas de armazenamento (ambiente e refrigeração) por 14 dias, totalizando oito tratamentos com cinco repetições. Os níveis de pólen apícola não influenciaram (P>0,05) a conversão alimentar, entretanto o consumo diário de ração, a taxa de postura, a massa de ovo e peso e porcentagem de albúmen aumentaram e a porcentagem de gema diminuiu com o aumento do pólen apícola nas dietas. Não houve efeito (P>0,05) da interação temperatura de armazenamento × níveis de pólen apícola sobre a qualidade dos ovos, exceto pela unidade Haugh. A suplementação com pólen apícola resultou em maior peso de ovo e de índices de gema e de albúmen. Ovos refrigerados tinham melhor qualidade interna. A inclusão de pólen apícola nas dietas de codornas Japonesas melhorou o desempenho e a qualidade de ovos frescos e armazenados.

Palavras-chave:
aditivo; alimentação de aves; nutrição animal; produção de ovos; produto apícola

INTRODUCTION

Bee pollen (BP) has therapeutic assets, such as antioxidant (Kocot et al., 2018KOCOT, J.; KIEŁCZYKOWSKA, M.; LUCHOWSKA-KOCOT, D.; KURZEPA, J.; MUSIK, I. Antioxidant potential of propolis, bee pollen, and royal jelly: possible medical application. Oxidative Medicine and Cellular Longevity, v. 2018, 7074209, 2018.), antibacterial (Karadal et al., 2018KARADAL, F.; ONMAZ, N.H.; ABAY, S.; YILDIRIM, Y.; AL, S.; TATYUZ, I.; AKCAY, A. A study of antibacterial and antioxidant activities of bee products: propolis, pollen and honey samples. Ethiopian Journal of Health Development, v. 32, n. 2, p. 116-122, 2018.), and immunomodulatory properties (Nascimento & Luz, 2018NASCIMENTO, A.M.C.B.; LUZ JR, G.E. Bee pollen properties: uses and potential pharmacological applications - a review. Journal of Analytical & Pharmaceutical Research, v. 7, n. 5, p. 513-515, 2018.), as well as a high nutritive value, with 25.66% carbohydrates, 2.22-4.03% ash, 2.28-10.81% fat, and 19.59-37.63% protein. In addition, BP has vitamins and minerals, such as K, Ca, and Mg, and is rich in essential fatty acids, and amino acids (histidine, leucine isoleucine, tryptophan, valine, and lysine) (Rebelo et al., 2016REBELO, K.S.; FERREIRA, A.G.; CARVALHO-ZILSE, G.A. Physicochemical characteristics of pollen collected by Amazonian stingless bees. Ciência Rural, v. 46, n. 5, p. 927-932, 2016.; Negrão & Orsi, 2018NEGRÃO, A.F.; ORSI, R.O. Harvesting season and botanical origin interferes in production and nutritional composition of bee pollen. Anais da Academia Brasileira de Ciências, v. 90, n. 1, p. 325-332, 2018.; Taha et al., 2019TAHA, EL-K.A.; AL-KAHTANI, S.; TAHA, R. Protein content and amino acids composition of bee-pollens from major floral sources in Al-Ahsa, eastern Saudi Arabia. Saudi Journal of Biological Sciences, v. 26, n. 2, p. 232-237, 2019.).

Based on these beneficial properties, BP may improve the use and absorption of nutrients leading to a better productive performance in animals, such as better weight gain, feed intake and feed conversion in quails (Babaei et al., 2016BABAEI, S.; RAHIMI, S.; TORSHIZI, M.A.K.; TAHMASEBI, G.; MIRAN, S.N.K. Effects of propolis, royal jelly, honey and bee pollen on growth performance and immune system of Japanese quails. Veterinary Research Forum, v. 7, n. 1, p. 13-20, 2016.; Desoky & Kamel, 2018DESOKY, A.A.; KAMEL, N.N. Egg production performance, blood biochemical and immunological response of laying Japanese quail fed diet supplemented with própolis and bee pollen. Egyptian Journal of Nutrition and Feeds, v. 21, n. 2, p. 549-557, 2018.), laying hens (Demir & Kaya, 2020DEMIR, Z.; KAYA, H. Effect of bee pollen supplemented diet on performance, egg quality traits and some serum parameters of laying hens. Pakistan Journal of Zoology, v. 52, n. 2, p. 549-555, 2020.), and broiler chickens (Hosseini et al., 2016HOSSEINI, S.M.; AZGHANDI, M.V.; AHANI, S.; NOURMOHAMMADI, R. Effect of bee pollen and propolis (bee glue) on growth performance and biomarkers of heat stress in broiler chickens reared under high ambient temperature. Journal of Animal and Feed Science, v. 25, n. 1, p. 45-51, 2016.).

The internal quality of the egg can be affected by nutrition and the relative humidity and temperature at which the eggs are stored, inter alia (Figueiredo et al., 2013FIGUEIREDO, T.C.; VIEGAS, R.P.; LARA, L.J.C.; BAIÃO, N.C.; SOUZA, M.R.; HENEINE, L.G.D.; CANÇADO, S.V. Bioactive amines and internal quality of comercial eggs. Poultry Science, v. 92, n. 5, p. 1376-1384, 2013.). According to Feddern et al. (2017)FEDDERN, V.; PRÁ, M.C.D.; MORAES, R.; NICOLOSO, R.S.; COLDEBELLA, A.; ABREU. P.G. Egg quality assessment at different storage conditions, seasons and laying hen strains. Ciência e Agrotecnologia, v. 41, n. 3, p. 322-333, 2017., from pasture to consumer table, physicochemical changes occur in yolk and/or albumen that may modify flavor, freshness, and palatability in eggs.

Consumer demand for natural products that can prevent the deterioration of animal-origin food has increased (Mitterer-Daltoé et al., 2020MITTERER-DALTOÉ, M.; BORDIM, J.; LISE, C.; BREDA, L.; CASAGRANDE, M.; LIMA, V. Consumer awareness of food antioxidants. Synthetic vs. natural. Food Science and Technology, 2020. Ahead of print. Available at < https://www.scielo.br/pdf/cta/2020nahead/0101-2061-cta-fst15120.pdf> Access on Sep 07, 2020.
https://www.scielo.br/pdf/cta/2020nahead...
). Lipid oxidation caused by free radicals is one of the main mechanisms of quality deterioration (Yilmaz et al., 2017YILMAZ, S.; SEVEN, T.; KAYA, E. Effects of propolis, royal jelly, bee pollen and ronozyme supplementation in diets of Japanese quails (Coturnix coturnix japonica) on yolk lipid peroxidation. International Journal of Veterinary Health Science & Research, v. 5, n. 5, p. 183-189, 2017.). Several studies have been carried out to evaluate the effect of natural antioxidants in laying diets (Cimrin et al., 2019CIMRIN, T.; AVSAROGLU, M.D.; IVGIN, T.R.; KANDIR, S.; AYASAN, T. Effects of the dietary supplementation of layer diets with natural and synthetic antioxidant additives on yolk lipid peroxidation and fatty acid composition of eggs stored at different temperatures and duration. Brazilian Journal of Poultry Science, v. 21, n. 2, p. 1-8, 2019.) to prevent egg deterioration. BP may have a beneficial effect on the quality of eggs because it contains antioxidant substances, such as flavonoids, carotenoids, and phenolic compounds (Feas et al., 2012FEAS, X.; VÁZQUEZ-TATO, M.P.; ESTEVINHO, L.; SEIJAS, J.A.; IGLESIAS, A. Organic bee pollen: botanical origin, nutritional value, bioactive compounds, antioxidant activity and microbiological quality. Molecules, v. 17, n. 1, p. 8359-8377, 2012.; Karadal et al., 2018KARADAL, F.; ONMAZ, N.H.; ABAY, S.; YILDIRIM, Y.; AL, S.; TATYUZ, I.; AKCAY, A. A study of antibacterial and antioxidant activities of bee products: propolis, pollen and honey samples. Ethiopian Journal of Health Development, v. 32, n. 2, p. 116-122, 2018.).

The effects of storage temperature on egg quality are well known and the effects of antioxidant compounds on the quality of eggs stored for different lengths of time and/or temperatures have been studied (Baylan et al., 2011BAYLAN, M.; CANOGULLRI, S.; AYASAN, T.; COPUR, G. Effects of dietary selenium source, storage time, and temperature on the quality of quail eggs. Biological Trace Element Research, v. 143, n. 2, p. 957-964, 2011.; Al-Harthi, 2014AL-HARTHI, M.A. The effect of natural and synthetic antioxidants on performance, egg quality and blood constituents of laying hens grown under high temperature. Italian Journal of Animal Science, v. 13, n. 2, p. 444-449, 2014.; Cimrin et al., 2019CIMRIN, T.; AVSAROGLU, M.D.; IVGIN, T.R.; KANDIR, S.; AYASAN, T. Effects of the dietary supplementation of layer diets with natural and synthetic antioxidant additives on yolk lipid peroxidation and fatty acid composition of eggs stored at different temperatures and duration. Brazilian Journal of Poultry Science, v. 21, n. 2, p. 1-8, 2019.). However, research regarding the use of BP as an antioxidant for improving egg quality is scarce.

This present research was carried out to evaluate the effects of BP on the productive performance of laying Japanese quail and on the internal quality of fresh eggs or eggs stored under different temperatures up to 14 days after laying.

MATERIALS AND METHODS

The experimental protocol was approved by the Ethics Committee on Animal Use (protocol number 01/12; April 19, 2012) of the Universidade de Rio Verde.

One hundred and sixty Japanese quail (Coturnix japonica), with an initial age of 50 days, were used for 84 days in a completely randomized design with four treatments and five replicates. Treatments consisted of BP inclusion in quail diets (0%, 0.5%, 1%, and 1.5% BP) (Table 1). Diets were formulated to meet the nutritional requirements of laying quail (Rostagno et al., 2011ROSTAGNO, H.S.; ALBINO, L.F.T.; DONZELE, J.L.; GOMES, P.C.; OLIVEIRA, R.F.; LOPES, D.C.; FERREIRA, A.S.; BARRETO, S.L.T.; EUCLIDES, R.F. 2011. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais de aves e suínos. 3. Ed. Viçosa: UFV, 2011.) and were provided ad libitum, twice a day. The BP used had a moisture content of 3.83%, crude protein content of 22.97%, gross energy content of 3953 kcal/kg, calcium content of 0.39%, phosphorus content of 0.99%, mineral ash content of 3.14%, fat content of 1.71%, and a pH of 4.68.

Table 1
Composition of the experimental diets

The light program was initiated on the fortieth day of age, with exposure of 14 h of light daily and a weekly increase of 30 min until reaching 17 h of daily light exposure, which was kept until the end of the experimental period.

Feed intake, laying rate, egg mass, feed conversion, and egg quality were evaluated. All the eggs laid in the three last days of the experimental period were used to determine egg weight and pH, yolk and albumen weight, percentage, quality related indices, and eggshell thickness. Yolk and albumen height and diameter were measured using a manual caliper, and the values were used to obtain their indices. Ten eggs of each replicate were used to determine the specific weight in saline solutions of a density of 1.050 to 1.100 g/cm3.

Eggshells were washed and dried in air for later measurements (weight and thickness). Eggshell thickness was measured at three different points (on both poles and on the lateral part) with a digital caliper with 0.01 mm precision. The Haugh unit (HU) was obtained using the formula: HU = 100 × log (H-1.7 × P0.37 + 7.6), where H is the albumen height (mm) and P is the egg weight (g).

The results of productivity and egg quality were submitted to an analysis of variance and means were compared by the Tukey test at 5% probability using the software, SISVAR (Ferreira, 2011FERREIRA. D.F. Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia, v. 35, n. 6, p. 1039-1042, 2011.).

At the end of the experiment, 160 eggs were used for evaluating the effects of BP on the quality of eggs stored at room temperature or in the fridge for 14 days, in a completely randomized design and factorial arrangement (4 × 2), with four BP levels and two storage temperatures, ambient (29 °C ± 0.8 °C) and refrigeration (5 °C ± 0.6 °C), totaling eight treatments with four replicates. Egg weight, pH, yolk and albumen weight, percentage, and quality indices, and Haugh unit were evaluated as mentioned above. Data obtained with stored eggs were also submitted to an analysis of variance, and when the F test was significant for BP levels or BP × storing temperature, means were compared using the Tukey test at 5% probability using the software SISVAR (Ferreira, 2011FERREIRA. D.F. Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia, v. 35, n. 6, p. 1039-1042, 2011.).

RESULTS AND DISCUSSION

Feed conversion, kg/kg or kg/dozen eggs, was not affected (P > 0.05) by the treatments; however, daily feed intake, laying rate, and egg mass increased (P < 0.05) as BP levels increased in quail diets up to 1-1.5% (Table 2).

Table 2
Egg production performance of Japanese quail fed diets with bee pollen (BP)

Higher feed intake was reflected in better laying rate and egg mass. According to Peric et al. (2009)PERIC, L.; ZIKIC, D.; LUKIC, M. Application of alternative growth promoters in broiler production. Biotechnolgy in Animal Husbandry, v. 25, n. 5-6, p. 387-397, 2009., BP is an appetite stimulant, and this effect was also reported by Hosseini et al. (2016)HOSSEINI, S.M.; AZGHANDI, M.V.; AHANI, S.; NOURMOHAMMADI, R. Effect of bee pollen and propolis (bee glue) on growth performance and biomarkers of heat stress in broiler chickens reared under high ambient temperature. Journal of Animal and Feed Science, v. 25, n. 1, p. 45-51, 2016., who verified higher feed intake by broilers supplemented with BP, which resulted in higher nutrient ingestion. Babaei et al. (2016)BABAEI, S.; RAHIMI, S.; TORSHIZI, M.A.K.; TAHMASEBI, G.; MIRAN, S.N.K. Effects of propolis, royal jelly, honey and bee pollen on growth performance and immune system of Japanese quails. Veterinary Research Forum, v. 7, n. 1, p. 13-20, 2016. noted that the addition of 5 g/kg BP was beneficial in improving Japanese quail performance. Canogullari et al. (2009)CANOGULLARI, S.; BAYLAN, M.; SAHINLER, N.; SAHIN, A. Effects of propolis and pollen supplementations on growth performance and body components of Japanese quail (Coturnix coturnix japonica). Archiv fur Geflügelkunde, v. 73, n. 3, p. 173-178, 2009. also supplemented Japanese quail with BP and did not observe effects on the productive performance, but the authors noted that feed intake increased with 1% and 2% BP inclusion in diets. These positive effects could be due to the nutritive value of BP, acting as a good source of fat, unsaturated fatty acids, proteins, essential amino acids, minerals, and carbohydrates (Abdelnour et al., 2019ABDELNOUR, S.A.; ABD EL-HACK, M.E.; ALAGAWANY, M.; FARAG, M.R.; ELNESR, S.S. Beneficial impacts of bee pollen in animal production, reproduction and health. Journal of Animal Physiology and Animal Nutrition, v. 103, n. 2, p. 477-484, 2019.).

Treatment did not affect egg quality (P > 0.05), except for yolk percentage, which was reduced (P ≤ 0.003), or albumen percentage, which was increased (P ≤ 0.006), as BP levels increased in the diets (Table 3).

Table 3
Characteristics of the eggs of Japanese quail fed diets with different inclusions of bee pollen (BP)

The yolk index is a measure of egg freshness and, as there was no difference in this parameter, it can be stated that BP inclusion did not affect yolk quality in fresh eggs. The reduction in yolk percentage and increase in albumen percentage occurred, possibly due to a higher protein deposition in the albumen. The need for amino acids for albumen synthesis is high, and any increase in this nutrient consumption and/or retention could improve the albumen amount in the egg, thereby decreasing yolk percentage, as demonstrated by Silva et al. (2010)SILVA, M.F.R.; FARIA, D.E.; RIZZOLI, P.W.; SANTOS, A.L.; SAKAMOTO, M.I.; SOUZA, H.R.B. Desempenho, qualidade dos ovos e balanço de nitrogênio de poedeiras comerciais alimentadas com rações contendo diferentes níveis de proteína bruta e lisina. Revista Brasileira de Zootecnia, v. 39, n. 6, p. 1280-1285, 2010., who evaluated diets with 12%, 14%, 16%, and 18% crude protein for laying hens and noted higher protein consumption and higher albumen percentage when dietary protein content was increased.

In addition, BP contains important nutrients necessary for cellular differentiation, which results in trophic effects in the intestinal mucosa that increase the absorption surface (Fazayeli-Rad et al., 2015FAZAYELI-RAD, A.R.; AFZALI, N.; FARHANGFAR, H.; ASGHARI, M.R. 2015. Effect of bee pollen on growth performance, intestinal morphometry and immune status of broiler chicks. European Poultry Science, v. 79, article 86, 2015. Available at http://doi.org/10.1399/eps.2015.86 Access on Jan 20, 2020.
http://doi.org/10.1399/eps.2015.86...
) and improve dietary nutrient use by the animal (Zeedan et al., 2017ZEEDAN, K.; BATTAA, A.M.E.N.; ABUOGHABA, A.A.A.A.; EL-KHOLY K.H. Effect of bee pollen at different levels as natural additives on immunity and productive performance in rabbit males. Egyptian Poultry Science, v. 37, n. 1, p. 213-231, 2017.). Similar results were found by Demir and Kaya (2020)DEMIR, Z.; KAYA, H. Effect of bee pollen supplemented diet on performance, egg quality traits and some serum parameters of laying hens. Pakistan Journal of Zoology, v. 52, n. 2, p. 549-555, 2020.. However, Desoky and Kamel (2018)DESOKY, A.A.; KAMEL, N.N. Egg production performance, blood biochemical and immunological response of laying Japanese quail fed diet supplemented with própolis and bee pollen. Egyptian Journal of Nutrition and Feeds, v. 21, n. 2, p. 549-557, 2018. observed improvements in the shell thickness and yolk index due to BP inclusion (0.2%) in diets of Japanese quail, and Arpásová et al. (2013)ARPÁSOVÁ, H.; KACÁNIOVÁ, M.; GÁLIK, B. The effect of oregano essential oil and pollen on egg production and egg yolk qualitative parameters. Lucrari Stiintifice, v. 46, n. 1 p. 12-16, 2013. did not note differences in egg quality of laying hens fed 0.04% BP in their diets.

BP inclusion increased (P ≤ 0.02) egg and albumen weight, egg pH, yolk and albumen indexes, and eggs stored under ambient temperature had a higher (P ≤ 0.02) pH value, lower yolk, and albumen indexes. However, at 14 days, there was an effect (P < 0.05) of the BP × storing temperature interaction only on the Haugh unit value. Higher values were obtained with BP inclusion of 1-1.5% in diets (Table 4).

Table 4
Characteristics of the eggs of Japanese quail fed diets with bee pollen (BP) stored under room temperature or refrigeration for 14 days

Egg freshness is a quality factor that can be influenced by the storage time and conditions (temperature and relative humidity), and by the egg age. The most common indicators of egg freshness are the height of the air space, albumen pH, aging rate, oxidation intensity of the yolk fats, and Haugh unit (Baylan et al., 2011BAYLAN, M.; CANOGULLRI, S.; AYASAN, T.; COPUR, G. Effects of dietary selenium source, storage time, and temperature on the quality of quail eggs. Biological Trace Element Research, v. 143, n. 2, p. 957-964, 2011.). However, as in any other animal origin product, the egg starts to deteriorate immediately after egg laying.

In our study, feed intake increased by 13.62% due to the inclusion of 1.5% BP; consequently, nutrient intake was also increased. One of the factors affecting egg weight is daily feed and nutrient intake, mainly protein intake. Egg weight increases with the increase in dietary protein ingestion (Lofti et al., 2018LOFTI, E.; KARIMI, N.; KAVAN, B.P.; SHARIFI, M.R. Influence of different dietary levels of energy and protein on reproductive and post hatch growth performance in Japanese quails. Iranian Journal of Applied Animal Science, v. 8, n. 1, p. 137-145, 2018.). According to Hegab and Hanafy (2019)HEGAB, I.M.; HANAFY, A.M. Effect of egg weight on external and internal qualities, physiological and hatching success of Japanese quail eggs (Coturnix coturnix japonica) Brazilian Journal of Poultry Science, v. 21, n. 3, p. 1-8, 2019. and Yasin and Sultan (2020)YASIN, B.; SULTAN, A. Phenotypic correlations between egg quality traits, albumen pH and ovalbumin levels in four varieties of Japanese quail (Coturnix coturnix japonica). GSC Biological and Pharmaceutical Sciences, v. 10, n. 3, p. 69-75, 2020., heavier eggs are positively correlated with yolk and albumen indices and albumen weight.

Egg pH was higher when BP was included in the diets, probably because heavier eggs, tend to have a greater eggshell surface, and total pore count, leading to higher CO2 losses and consequently, a higher egg pH. This effect was observed by El-Safty (2012)EL-SAFTY, S.A. Effect of egg weight grades, porosity and their interaction on some hatching traits of ostrich eggs. Egyptian Poultry Science, v. 32, n. 4, p. 725-733, 2012. and Hegab and Hanafy (2019)HEGAB, I.M.; HANAFY, A.M. Effect of egg weight on external and internal qualities, physiological and hatching success of Japanese quail eggs (Coturnix coturnix japonica) Brazilian Journal of Poultry Science, v. 21, n. 3, p. 1-8, 2019. in ostrich and Japanese quail eggs, respectively.

Maintenance of the eggs at ambient temperature resulted in higher pH values, and yolk and albumen indices. All these deteriorations in the egg occurred due to ovalbumin degradation, which leads to water formation. This water migrates to the yolk, increasing its weight and percentage. This is one of the buffer system components in the albumen, and the dissociation forms water and CO2. This CO2 is lost through the eggshell pores, causing a pH increase (Eke et al., 2013EKE, M.O.; OLAITAN, N.I.; OCHEFU, J.H. Effect of storage conditions on the quality attributes of shell (table) eggs. Nigerian Food Journal, v. 31, n. 1, p. 18-24, 2013.). These reactions result in a decrease in internal egg quality, as measured by the yolk and albumen indices, as well as the Haugh unit of eggs stored at ambient temperature.

There was an interaction between BP and storage time and this is because BP has antioxidant activity (Karadal et al., 2018KARADAL, F.; ONMAZ, N.H.; ABAY, S.; YILDIRIM, Y.; AL, S.; TATYUZ, I.; AKCAY, A. A study of antibacterial and antioxidant activities of bee products: propolis, pollen and honey samples. Ethiopian Journal of Health Development, v. 32, n. 2, p. 116-122, 2018.) due to the presence of several phenolic compounds in its composition, besides flavonoids and carotenoids (Feas et al., 2012FEAS, X.; VÁZQUEZ-TATO, M.P.; ESTEVINHO, L.; SEIJAS, J.A.; IGLESIAS, A. Organic bee pollen: botanical origin, nutritional value, bioactive compounds, antioxidant activity and microbiological quality. Molecules, v. 17, n. 1, p. 8359-8377, 2012.). The Haugh unit is a function of the height of thick albumen and the weight of the egg. As BP inclusion in the diet improved the egg weight and albumen index, it was expected that the Haugh unit would also improve with the consequent improvement in egg internal quality.

BP inclusion at 1 and 1.5 ppm improved the Haugh unit of eggs stored at ambient temperature, because BP acts as an antioxidant (Kocot et al., 2018KOCOT, J.; KIEŁCZYKOWSKA, M.; LUCHOWSKA-KOCOT, D.; KURZEPA, J.; MUSIK, I. Antioxidant potential of propolis, bee pollen, and royal jelly: possible medical application. Oxidative Medicine and Cellular Longevity, v. 2018, 7074209, 2018.), inhibiting lipid oxidation in the yolk and ovalbumin degradation. These reactions would lead to water and CO2 loss, reducing the egg weight and albumen height, with a consequent increase in pH and a decrease in Haugh unit values, which are internal quality measures of the egg.

Similar results were observed by other authors who worked with eggs stored under different temperatures and/or using additives with antioxidant activity in bird diets (Olobatoke & Mugueta, 2012OLOBATOKE, R.Y.; MULUGETA, S.D. The effect of dietary garlic powder and a low temperature on the physical quality of stored eggs. South African Journal of Animal Science, v. 42, n 5, p. 540-544, 2012.; Arpásová et al., 2013ARPÁSOVÁ, H.; KACÁNIOVÁ, M.; GÁLIK, B. The effect of oregano essential oil and pollen on egg production and egg yolk qualitative parameters. Lucrari Stiintifice, v. 46, n. 1 p. 12-16, 2013.; Al-Harthi, 2014AL-HARTHI, M.A. The effect of natural and synthetic antioxidants on performance, egg quality and blood constituents of laying hens grown under high temperature. Italian Journal of Animal Science, v. 13, n. 2, p. 444-449, 2014.; Lee et al., 2016LEE, M.H.; CHO, E.J.; CHOI, E.S.; SOHN, S.H. The effect of storage period and temperature on egg quality in commercial eggs. Korean Journal of Poultry Science, v. 1, n. 1, p. 31-38, 2016.; Feddern et al., 2017FEDDERN, V.; PRÁ, M.C.D.; MORAES, R.; NICOLOSO, R.S.; COLDEBELLA, A.; ABREU. P.G. Egg quality assessment at different storage conditions, seasons and laying hen strains. Ciência e Agrotecnologia, v. 41, n. 3, p. 322-333, 2017.; Lana et al. 2017LANA, S.R.V.; LANA, G.R.Q.; SALVADOR, E.L.; LANA, A.M.Q.; CUNHA, F.S.A.; MARINHO, A.L. Qualidade de ovos de poedeiras comerciais armazenados em diferentes temperaturas e períodos de estocagem. Revista Brasileira de Saúde e Produção Animal, v. 18, n. 1, p. 140-151, 2017.; Yilmaz et al., 2017YILMAZ, S.; SEVEN, T.; KAYA, E. Effects of propolis, royal jelly, bee pollen and ronozyme supplementation in diets of Japanese quails (Coturnix coturnix japonica) on yolk lipid peroxidation. International Journal of Veterinary Health Science & Research, v. 5, n. 5, p. 183-189, 2017.).

CONCLUSION

The inclusion of BP in the diet of laying Japanese quails may improve their productive performance and the internal quality of fresh eggs while improving the Haugh unit in eggs stored at ambient temperature for 14 days. Storage of eggs under refrigeration improves egg pH, yolk, and albumen indices, resulting in better internal quality of the eggs.

REFERENCES

  • ABDELNOUR, S.A.; ABD EL-HACK, M.E.; ALAGAWANY, M.; FARAG, M.R.; ELNESR, S.S. Beneficial impacts of bee pollen in animal production, reproduction and health. Journal of Animal Physiology and Animal Nutrition, v. 103, n. 2, p. 477-484, 2019.
  • AL-HARTHI, M.A. The effect of natural and synthetic antioxidants on performance, egg quality and blood constituents of laying hens grown under high temperature. Italian Journal of Animal Science, v. 13, n. 2, p. 444-449, 2014.
  • ARPÁSOVÁ, H.; KACÁNIOVÁ, M.; GÁLIK, B. The effect of oregano essential oil and pollen on egg production and egg yolk qualitative parameters. Lucrari Stiintifice, v. 46, n. 1 p. 12-16, 2013.
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Publication Dates

  • Publication in this collection
    15 Feb 2021
  • Date of issue
    2020

History

  • Received
    16 Feb 2020
  • Accepted
    13 Oct 2020
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