ABSTRACT
This study was conducted to determine the effect of bee pollen inclusion on the performance and gut morphology of Ross 308 broiler chickens. A total of 240-day-old chicks (120 males and 120 females) were allocated to 4 treatments in a randomized complete block design (RCBD) with sex as a block. Each experimental group was replicated 3 times with 10 chicks per replicate, with an average weight of 40 ± 5g per bird. Body weight and feed intake were measured on a weekly basis to calculate the feed conversion ratio. Gut morphology was measured on days 21 and 42. Data were analysed using the General Linear Model procedures of the Statistical Analysis System.Bee pollen inclusion in starter diets had an effect (p<0.05) on body weight and live weight gain of male Ross 308 broiler chickens. The different inclusion levels of bee pollen had an effect (p<0.05) on the gut morphology of Ross 308 broiler chickens. The ileum lengths of female broiler chickens were significantly wider (p<0.05) in comparison with male chickens. This may suggest that bee pollen inclusion has a beneficial effect on broiler chickens gut morphology during the early stages of development. It can be concluded that natural substances such as bee pollen can be a possible feed additive to replace synthetic antibiotics, since such compounds are essential for the growth and development of poultry gut.
Keywords:
Antibiotics; bee pollen; body weight; broiler chickens; gut morphology
INTRODUCTION
Chicken production has a major impact on employment and income, being an important aspect of food security for the people of Africa (Ngongolo et al., 2018Ngongolo KE, Sigala E, Mtoka S. Community poultry project for conserving the wildlife species in Magombera forest, Tanzania. Asian Journal of Research in Agriculture and Forestry 2018;2(4);1-7.). Soon after chick hatching, chicks start feeding on solid feeds while they depend on the remaining yolk on their body (Sklan, 2003Sklan D. Fat and carbohydrate use in post hatch chicks. Poultry Science 2003;82:117-22.). This process results in weight loss after hatching (Willemsen et al., 2010Willemsen H, Debonne M, Swennen Q, Everaert N, Careghl C, Han H, et al. Delay in feed access and spread of hatch:importance of early nutrition. Poultry Science Journal 2010;66:177-88.). Chicks require diets that help meet their nutrient requirements to avoid weight loss after hatching, with the main goal of achieving their full growth potential (Gous, 2010Gous RM. Nutritional limitations on growth and development in poultry. Livestock Science 2010;130:25-32.). Antibiotics have been used to improve feed utilization in chickens (Rosen,1996Rosen GD. The nutritional effects of tetracyclines in broiler feeds. Proceeding of the Worlds Poultry Congress; 1996 Sept 2-5; New Delhi, India. New Delhi: World’s Poultry Science Association; 1996. p.141-8.). However, the use of antibiotics as growth promoters has been banned in many countries, thus there is a need to find safe additives that will have no adverse effects on the health of animals, humans, and the environment (Zhang et al., 2005Zhang X, Habib FK, Ross M, Burger U, Lewenstein A, Rose K, et al. Isolation and characterization of a cyclic hydroxamic acid from a pollen extract, which inhibits cancerous cell growth in vitro. Journal of Medical Chemistry 2005;38:735-8.). In some countries, bee pollen is considered medicinal (Brindza et al., 2010Brindza J, Gróf J, Bacigálová K, Ferianc P, Tóth D. Pollen microbial colonization and food safety. Acta Chimica Slovaca 2010;3:95-102.). Honeybees collect pollen from different plants and it is mixed with their digestive enzymes (Kalafova et al., 2014Kalafova A, Hascik P, Petruska P, Tušimova E, Cupka P, Kovacik A, et al. Effect of bee pollen in chicken diet on selected parameters of mineral profile. Acta Fytotechnica Zootechnica 2014;17(3):90-2.). Bee pollen is a rich source of protein, essential amino acids, oils, vitamins, minerals, enzymes, and carbohydrates (Xu et al., 2009). Some studies revealed that bee pollen can be used as a growth promoter and immune system stimulator in broiler chickens (Wang et al., 2005). Phenolic constituents and antioxidants in bee pollen have been identified as possible growth promoters in chickens and rabbits (Saric et al., 2009Šarić A, Balog T, Sobočanec S, Kušić B, Šverko V, Rusak G. Antioxidant effects of flavonoid from Croatian Cystus incanus L. rich bee pollen. Food and Chemical Toxicology 2009;47:547-54.). Amino acids, vitamins, and trace elements of bee pollen stimulate the early development, proliferation, and differentiation of intestinal cells. The environments for intestinal microbial ecosystems are also improved (Dias et al., 2013). Several studies have shown the possible potential bee pollen has on the growth performance in chicken production (Attia et al., 2014Attia YA, El-Hanoun AM, Bovera F, Monastra G, El-Tahawy WS, Habiba HI. Growth performance, carcass quality, biochemical and haematological traits and immune response of growing rabbits as affected by different growth promoters. Journal of Animal Physiology and Animal Nutrition 2014;98(1):128-39.; Hosseini et al. 2016Hosseini SM, Vakili Azghandi M, Ahani S, Nourmohammad 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 Feed Science 2016;25(1):45-51.; Zafarnejad et al., 2016Zafarnejad K, Afzali N, Rajabzadeh M. Effect of bee glue on growth performance and immune response of broiler chickens. Journal of Applied Animal Research 2016;45:1-5.). This type of natural substance can promote gut health, and digestibility, while also decreasing pathogens in poultry (Duarte et al., 2014Duarte CRA, Eyng C, Murakami AE, Santos TC. Intestinal morphology and activity of digestive enzymes in broilers fed crude propolis. Canadian Journal of Animal Science 2014;94:105-14.). A clear perspective on bee pollen as an alternative to synthetic antibiotics in poultry production is necessary. Therefore, this study was conducted to determine the effect of bee pollen inclusion on the performance and gut morphology of Ross 308 broiler chickens.
MATERIALS AND METHODS
Study site
The study was conducted at the University of Limpopo, Animal Unit, Limpopo Province, South Africa. The University of Limpopo lies at latitude 27.55ºS and longitude 24.77ºE. The mean ambient temperature around the study area is 28ºC during winter and 36ºC during summer (Shiringani, 2007Shiringani RP. Effect of planting date and location on phenology, yield and yield components among cowpea selected cowpea varieties [dissertation]. Mankweng (ZA): University of Limpopo, South Africa; 2007; p.20-73.).
The experimental procedures were conducted in accordance with the University of Limpopo (UL) Ethics committee, reference number: AREC/06/2020:PG.
Experimental procedures and design
A total of 240-day-old chicks (120 males and 120 females) were allocated to 4 treatments in a randomized complete block design (RCBD) with sex as a block. Each experimental group was replicated 3 times with 10 chicks per replicate, with an average weight of 40 ± 5g per bird. Bee pollen inclusion levels were 0, 4, 8, or 12 g/kg DM feed (Table 1). Bee pollen used in the current study was purchased from a company in Tzaneen, Polokwane. Bee pollen was dried in a well-ventilated laboratory to obtain a constant weight and milled into powder through a 1 mm sieve by using a hammer mill, before being added to the formulated diets (Table 2 and Table 3). After 21 days, the chickens remained in their treatment groups. This experiment lasted for 42 days, and feed and water were provided ad libitum throughout the experimental period.
Data collection
Live weights were determined at the start of the experiment and then weekly. Feed intake per chicken was determined by calculating the difference between the weight of feed offered and the weight of feed leftover, and the difference was then divided by the total number of chickens in the pen. Feed intake and weight gain were used to calculate the feed conversion ratio (McDonald et al., 2010McDonald P, Edwards RA, Greenhalgh JFD, Morgan CA. Animal nutrition. 6th ed. London: Pearsoned Education; 2010.).
At the ages of 21 and 42 days, 3 chickens per replicate were slaughtered using the cervical dislocation method to determine gut organ weights and lengths, and gut organ digesta pH. Before the slaughter, each chicken was weighed using an electronic weighing balance. Afterwards, carcasses were put inside a bucket containing hot water for a few seconds, subsequently being taken out. Carcasses were then put on a table for hand defeathering. They were cut open at the abdominal site and the digestive tracts were removed from the abdominal cavities. The carcass weight of each chicken was measured only at the age of 42 days, after slaughter. The gastrointestinal tract, small intestine, caeca, and large intestine lengths were determined using a tape measure (Kokoszyński et al., 2017Kokoszyński D , Biegniewska M , Wilkanowska A, Saleh M, Bernacki Z , Stęczny K, et al. Body morphometry and development of the digestive system of grey partridge (Perdix perdix) depending on age and gender. Revista Brasileira de Ciência Avícola 2017;19(4).). The pH of gut contents (crop, proventriculus, gizzard, ileum, caecum, and colon) was measured using a digital pH meter (Crison, Basic 20 pH meter). Breast, drumstick, thigh, crop, proventriculus, gizzard, small intestine, caeca, and large intestine weights were measured using an electronic weighing balance.
Dry matter of feeds, bee pollen, feed refusals, faeces, and meat were determined by drying the samples in the oven for 24 hours at a temperature of 105ºC AOAC (2012). Neutral and acid detergent fibre contents of feed and faeces were determined according to Van Soest et al. (1991Van Soest PJ, Robertson JB, Lewis BA. Methods for dietary fibre, neutral detergent fibre, and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science 1991;74:3583-97.). Ash contents of feeds, bee pollen, faeces, and meat samples were determined by ashing the sample at 600ºC in a muffle furnace overnight. Ash was analysed for calcium, magnesium, phosphorus, potassium, sodium, zinc, iron, copper, and manganese AOAC (2012). Nitrogen contents of feed and meat samples were determined by the Kjeldahl method AOAC (2012). The gross energy values of feeds and faeces were determined using a bomb calorimeter AOAC (2012). A full analysis for faeces and feeds was performed at the Pietermaritzburg Laboratory, Kwa-Zulu Natal, South Africa according to AOAC (2012).
Data analysis
Data was analysed using the General Linear Model (GLM) procedures of the statistical analysis of variance SAS (2012) to detect dietary treatment effects. The statistical model Yijk= µ + Ti + Bj + (TB)ij + eijkwas applied, where Yijk = the observation on feed intake, digestibility, live weight, gut morphology, carcass characteristics, feed conversion ratio, and mortality due to dietary treatment effects; µ = the overall mean; Ti = the ith effect of bee pollen inclusion in starter diets; Bj =sex as a block factor; (TB)ij = interaction between bee pollen inclusion and sex; and eijk = the residual effect (error). Where significant differences were observed, mean separation was conducted using Tukey test at a 5% level of significance (SAS, 2012). The responses to bee pollen inclusion levels observed in optimal feed intake, live weight, growth rate, digestibility, feed conversion ratio, metabolisable energy, gut morphology, and carcass characteristics were modelled using the quadratic equation (SAS 20012).
RESULTS
The growth performance of broiler chickens aged one to 21 and 22 to 42 days (Table 4) was analysed. Between the age of one and 21 days, bee pollen inclusion level had no effect (p>0.05) on diet DM intake, growth rate, and FCR of male and female Ross 308 broiler chickens. Similarly, bee pollen inclusion levels had no effect (p>0.05) on the live weight of male Ross 308 broiler chickens aged 21 days. However, the bee pollen inclusion level affected (p<0.05) the live weight of female Ross broiler chickens aged 21 days. Female Ross 308 broiler chickens on a diet with 8g/kg bee pollen per kg DM feed had higher (p<0.05) live weights than those with 0, 4, or 12 g of bee pollen per kg DM. Bee pollen inclusion level had no effect (p>0.05) on the diet DM intake and FCR values of male Ross 308 broiler chickens aged 42 days.
The results in Table 6 show that there was no effect (p>0.05) on the gastrointestinal tract (GIT), duodenum, jejunum, caeca, and ileum lengths of male Ross 308 broiler chickens aged 21 days. Moreover, at the age of 22-42, bee pollen inclusion had no effect (p>0.05) on the gastrointestinal tract (GIT), duodenum, jejunum, caeca, and ileum lengths of male Ross 308 broiler chickens. However, bee pollen inclusion had an effect (p<0.05) on the ileum lengths of female broiler chickens at 21 days, and an effect (p<0.05) on the GIT and duodenum lengths of female broilers at the age of 42 days.
Table 7 represents the effect of bee pollen inclusion level on the gut organ weights (g) of Ross 308 broiler chickens aged 21 and 42 days. Female and male Ross 308 broiler chickens aged 21 days with 0, 4, 8, or 12 g of bee pollen per kg DM had similar (p>0.05) crop, gizzard, and liver weights. However, male Ross 308 broiler chickens had heavier (p<0.05) proventriculus, small intestines, and large intestines. Bee pollen inclusion had no effect (p>0.05) on the caecum and large intestine weights of male Ross 308 broiler chickens aged 42 days. However, bee pollen inclusion affected (p<0.05) the gizzard, crop, proventriculus, liver, and small intestine weights of male Ross 308 broiler chickens aged 42 days.Male Ross 308 broiler chickens with 12 g of bee pollen per kg DM had heavier (p<0.05) crop, proventriculus, and liver weights than those on diets with 0, 4, or 8 g of bee pollen per kg DM.There were positive and significant relationships (p<0.05) between bee pollen inclusion levels and the liver and small intestine weights of male Ross 308 broiler chickens aged 42 days.
DISCUSSION
In the present study, bee pollen inclusion had no effect on diet DM intake, growth rate, and FCR of male and female broiler chickens aged one to 21 days. Similarly, bee pollen inclusion levels in starter diets had no effect on the live weight of male broilers aged 21 days. However, the current study is inconsistent with that of (Liu et al., 2010Liu G, Yan W, Zeng Z. Application of bee pollen on the Gallus feed. Bee Journal 2010;3:22-9.; Attia et al., 2011Attia YA, AL-Hanoun A, Bovera F. Effect of different levels of bee pollen on performance and blood profile of New Zealand White bucks and growth performance of their offspring during summer and winter months. Journal of Animal Physiology and Animal Nutrition 2011;95:17-26.; Hascik et al., 2012Haščík P, Elimam I, Garlík J, Kačániová M, Čuboň J, Bobko M, et al. Impact of bee pollen as feed supplements on the body weight of broiler Ross 308. African Journal of Biotechnology 2012;11(89):15596-9.; Eyng et al., 2014Eyng C, Murakami AE, Duarte CRA, Santos TC. Effect of dietary supplementation with an ethanolic extract of propolis on broiler intestinal morphology and digestive enzyme activity. Journal of Animal Physiology and Animal Nutrition 2014;98:393-401.), who observed improved diet intake and live weights after including bee pollen in broiler diets. The improved performance may be due to the high nutrition found in bee pollen, consequently making it a suitable feed supplement for chickens (Hascik et al., 2017). Thus, bee pollen could be included in broiler diets without any effect on chicken performance.
Bee pollen inclusion did not affect the GIT, duodenum, caeca, and large intestine lengths of female Ross 308 broiler chickens aged 21 days. However, it positively affected the large intestine lengths of males as well as the jejunum and ileum lengths of female broilers. Similar results were obtained by Hascik et al. (2017Haščík P, Pavelková A, Bobko M, Trembecka L, Elimam I, Capcarovo M. The effect of bee pollen in chicken diet. World’s Poultry Science Journal 2017;1-7.) and Hashmi et al. (2012Hashmi MS, Haščík P, Eliman I, Garlík J, Bobko M, Kačániová M. Effects of Bee Pollen on the Technical and Allocative Efficiency of Meat Production of Ross 308 Broiler. International Journal of Poultry Science 2012;11:689-95.). This could have been due to amino acids, vitamins, minerals, and coenzymes, which are important for digestibility and cell growth (Wang et al., 2007Wang J, Li S, Wang Q, Xin B, Wang H. Trophic effect of bee pollen on small intestine in broiler chickens. Journal of Medicine Food 2007;10:276-80.).
The inclusion of bee pollen had no effect on the gizzard, liver, and caecum weights of male broilers as well as the crop, proventriculus, liver, and large intestine weights of females aged 21 days. Similar observations were made by Zeedan et al. (2017Zeedan KH, Battaa II, El-Neney AM, Abuoghaba AAAA, El-Kholy KH. Effect of bee pollen at difefferentlevels as natural additive on immunity and productive performance in rabbit males. Egypt Poultry Science 2017;37:213-23). However, bee pollen inclusion positively affected the crop, proventriculus, small intestine, and large intestine weights of male chickens aged 21 days. Moreover, it also improved the gizzard, small intestine, and caecum weights of female broilers. This is in agreement with Fazayeli-Rad et al. (2015Fazayeli-Rad AR, Afzali N, Asghari MR. Effect of bee pollen on intestinal morphometry and selected blood parameters in broiler chicks. Proceedings of the 20th European Symposium on Poultry Nutrition; 2015 Aug 24-27; Prague, Czech Republic. 2015. Prague: AGROLEX; 2015.) and Hascik et al. (2013Haščík P, Elimam I, Garlík J, Kačániová M, Čuboň J, Bobko M, et al. The effect of bee pollen as dietary supplement on meat chemical composition for broiler Ross 308. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 2013;61:71-6.). Nonetheless, there is limited information on the gut organ weights of broiler chickens.
The inclusion of bee pollen tended to improve the growth rate and live weight of female Ross 308 broiler chickens aged 22 to 42 days. Similar results were reported by Hascik et al. (2017Haščík P, Pavelková A, Bobko M, Trembecka L, Elimam I, Capcarovo M. The effect of bee pollen in chicken diet. World’s Poultry Science Journal 2017;1-7.) and Hascik et al. (2013), who observed that bee pollen inclusion in the diets improved the diet intake, digestibility, and live weights of broiler chickens.
The present study showed that there was an effect of bee pollen supplementation on the FCR of male Ross 308 broiler chickens. This is similar to the observations made by Fazayeli-Rad et al. (2015Fazayeli-Rad AR, Afzali N, Asghari MR. Effect of bee pollen on intestinal morphometry and selected blood parameters in broiler chicks. Proceedings of the 20th European Symposium on Poultry Nutrition; 2015 Aug 24-27; Prague, Czech Republic. 2015. Prague: AGROLEX; 2015.), who observed that the addition of BP in diets significantly improved the FCR values of Ross 308 male broiler chickens.
In the present study, bee pollen increased the GIT and duodenum lengths of Ross 308 female broiler chickens. These results are similar to those reported by Fazayeli-Rad et al. (2015Fazayeli-Rad AR, Afzali N, Asghari MR. Effect of bee pollen on intestinal morphometry and selected blood parameters in broiler chicks. Proceedings of the 20th European Symposium on Poultry Nutrition; 2015 Aug 24-27; Prague, Czech Republic. 2015. Prague: AGROLEX; 2015.), who observed increased sizes of the GIT and intestine of broiler chickens, which could have been due to the increased digestive enzyme caused by the adaptation effect in broiler chickens.
The inclusion of bee pollen in the present study increased the crop, proventriculus, gizzard, liver, and small intestine weights. Amerah et al. (2009Amerah AM, Ravindran V, Lentle RG. Influence of insoluble fibre and whole wheat inclusion on the performance, digestive tract development and ileal microbiota profile of broiler chickens. British Poultry Science 2009;50:366-75.) reported that gizzard volume increases in weight when diets contain structural components. This may have been the reason why the gizzard was affected. Bee pollen contains several components that are important for biological activities, such as phenols and flavonoids (Rzepecka-Stojko et al., 2015). Fazayeli-Rad et al. (2015Fazayeli-Rad AR, Afzali N, Asghari MR. Effect of bee pollen on intestinal morphometry and selected blood parameters in broiler chicks. Proceedings of the 20th European Symposium on Poultry Nutrition; 2015 Aug 24-27; Prague, Czech Republic. 2015. Prague: AGROLEX; 2015.) and Hashmi et al. (2012Hashmi MS, Haščík P, Eliman I, Garlík J, Bobko M, Kačániová M. Effects of Bee Pollen on the Technical and Allocative Efficiency of Meat Production of Ross 308 Broiler. International Journal of Poultry Science 2012;11:689-95.) observed similar results in liver weights of broiler chickens, reporting that treated livers were heavier than those in the control group. These findings may suggest that the antioxidant properties of flavonoids positively impact the alimentary canal of broilers. Sarikaya et al. (2018Sarikaya Y, Tufan T, Bolacali M. Effects of dietary addition of pollen on growth performance and carcass traits of Japanese quail. Harran Üniversitesi Veteriner Fakültesi Dergisi 2018;7(1):26-31.) observed no statistical differences amongst groups in terms of weights of the liver, gizzard, intestines, as well as in the lengths of intestines, when including bee pollen in quail diets at the 0.025% and 0.50% levels.
CONCLUSIONS
During each phase, dietary treatments had similar nutrient content levels that met the nutrient requirements of the broiler chickens. Thus, any differences in responses must have been due to the bee pollen that was supplemented in broiler diets. The effect of bee pollen in starter diets of Ross 308 broiler chickens at 12g/kg resulted in better live weights. There was a positive and significant relationship between bee pollen inclusion in the starter diet and live weights of male Ross broiler chickens aged 42 days. Therefore, it can be concluded that bee pollen has a positive effect on the gut of chickens, which was shown through the increased lengths and weights of the gut organs. The results of this study show that the inclusion level of 12g/kg of bee pollen had a significant effect on the gut of the chickens. It is suggested that further studies are conducted to support this finding.
ACKNOWLEDGEMENTS
The authors would like to acknowledge the financial assistance of the National Research Foundation (NRF) (grant number 129049)and VLIR-UOS (grant number ZIUS2016AP21).
REFERENCES
- Amerah AM, Ravindran V, Lentle RG. Influence of insoluble fibre and whole wheat inclusion on the performance, digestive tract development and ileal microbiota profile of broiler chickens. British Poultry Science 2009;50:366-75.
- AOAC. Offical methods of analysis. 19th ed. Arlington: AOAC International; 2012.
- Attia YA, Abd Al-Hamid AE, Ibrahim MS, Al-Harthi MA, Bovera F, El-Naggar A. Productive performance, biochemical and hematological traits of broiler chickens supplemented with propolis, bee pollen and mannan oligosaccharides continuously or intermittently. Livestock Science 2014;164:87-95.
- Attia YA, AL-Hanoun A, Bovera F. Effect of different levels of bee pollen on performance and blood profile of New Zealand White bucks and growth performance of their offspring during summer and winter months. Journal of Animal Physiology and Animal Nutrition 2011;95:17-26.
- Attia YA, El-Hanoun AM, Bovera F, Monastra G, El-Tahawy WS, Habiba HI. Growth performance, carcass quality, biochemical and haematological traits and immune response of growing rabbits as affected by different growth promoters. Journal of Animal Physiology and Animal Nutrition 2014;98(1):128-39.
- Brindza J, Gróf J, Bacigálová K, Ferianc P, Tóth D. Pollen microbial colonization and food safety. Acta Chimica Slovaca 2010;3:95-102.
- Dias DMD, Oliveria MC de, Silva DM da, Barifacio NP, Cunha Claro D da, Marchesin WA. Bee pollen supplementation in diets for rabbit does and growing rabbits. Acta Scientiarum Animal Science 2013;35:425-30.
- Duarte CRA, Eyng C, Murakami AE, Santos TC. Intestinal morphology and activity of digestive enzymes in broilers fed crude propolis. Canadian Journal of Animal Science 2014;94:105-14.
- Eyng C, Murakami AE, Duarte CRA, Santos TC. Effect of dietary supplementation with an ethanolic extract of propolis on broiler intestinal morphology and digestive enzyme activity. Journal of Animal Physiology and Animal Nutrition 2014;98:393-401.
- Fazayeli-Rad AR, Afzali N, Asghari MR. Effect of bee pollen on intestinal morphometry and selected blood parameters in broiler chicks. Proceedings of the 20th European Symposium on Poultry Nutrition; 2015 Aug 24-27; Prague, Czech Republic. 2015. Prague: AGROLEX; 2015.
- Gous RM. Nutritional limitations on growth and development in poultry. Livestock Science 2010;130:25-32.
- Haščík P, Elimam I, Garlík J, Kačániová M, Čuboň J, Bobko M, et al. Impact of bee pollen as feed supplements on the body weight of broiler Ross 308. African Journal of Biotechnology 2012;11(89):15596-9.
- Haščík P, Elimam I, Garlík J, Kačániová M, Čuboň J, Bobko M, et al. The effect of bee pollen as dietary supplement on meat chemical composition for broiler Ross 308. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 2013;61:71-6.
- Hascik P, Garlik J, Kacaniova M, Cubon J, Mellen M, Mihok M, et al. Sensory evaluation of meat chickens Ross 308 after application of propolis in their nutrition. Journal of Microbiology, Biotechnology and Food Sciences 2011;1(2):172-86.
- Haščík P, Pavelková A, Bobko M, Trembecka L, Elimam I, Capcarovo M. The effect of bee pollen in chicken diet. World’s Poultry Science Journal 2017;1-7.
- Hashmi MS, Haščík P, Eliman I, Garlík J, Bobko M, Kačániová M. Effects of Bee Pollen on the Technical and Allocative Efficiency of Meat Production of Ross 308 Broiler. International Journal of Poultry Science 2012;11:689-95.
- Hosseini SM, Vakili Azghandi M, Ahani S, Nourmohammad 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 Feed Science 2016;25(1):45-51.
- Kalafova A, Hascik P, Petruska P, Tušimova E, Cupka P, Kovacik A, et al. Effect of bee pollen in chicken diet on selected parameters of mineral profile. Acta Fytotechnica Zootechnica 2014;17(3):90-2.
- Kokoszyński D , Biegniewska M , Wilkanowska A, Saleh M, Bernacki Z , Stęczny K, et al. Body morphometry and development of the digestive system of grey partridge (Perdix perdix) depending on age and gender. Revista Brasileira de Ciência Avícola 2017;19(4).
- Liu G, Yan W, Zeng Z. Application of bee pollen on the Gallus feed. Bee Journal 2010;3:22-9.
- McDonald P, Edwards RA, Greenhalgh JFD, Morgan CA. Animal nutrition. 6th ed. London: Pearsoned Education; 2010.
- Ngongolo KE, Sigala E, Mtoka S. Community poultry project for conserving the wildlife species in Magombera forest, Tanzania. Asian Journal of Research in Agriculture and Forestry 2018;2(4);1-7.
- Rosen GD. The nutritional effects of tetracyclines in broiler feeds. Proceeding of the Worlds Poultry Congress; 1996 Sept 2-5; New Delhi, India. New Delhi: World’s Poultry Science Association; 1996. p.141-8.
- Rzepecka-stojko A, Stojko J, Kurek-górecka A, Górecki M, Kabała-dzik A, Kubina R, Moździerz A, Buszman E. Polyphenols from Bee Pollen:Structure, Absorption, Metabolism and Biological Activity. Molecules 2015;20:21732-21749.
- Šarić A, Balog T, Sobočanec S, Kušić B, Šverko V, Rusak G. Antioxidant effects of flavonoid from Croatian Cystus incanus L. rich bee pollen. Food and Chemical Toxicology 2009;47:547-54.
- Sarikaya Y, Tufan T, Bolacali M. Effects of dietary addition of pollen on growth performance and carcass traits of Japanese quail. Harran Üniversitesi Veteriner Fakültesi Dergisi 2018;7(1):26-31.
- SAS - Statistical Analysis System. User’s guide. Statistical. Version 9.1th ed. Cary; 2012.
- Shiringani RP. Effect of planting date and location on phenology, yield and yield components among cowpea selected cowpea varieties [dissertation]. Mankweng (ZA): University of Limpopo, South Africa; 2007; p.20-73.
- Sklan D. Fat and carbohydrate use in post hatch chicks. Poultry Science 2003;82:117-22.
- Van Soest PJ, Robertson JB, Lewis BA. Methods for dietary fibre, neutral detergent fibre, and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science 1991;74:3583-97.
- Wang J, Li S, Wang Q, Xin B, Wang H. Trophic effect of bee pollen on small intestine in broiler chickens. Journal of Medicine Food 2007;10:276-80.
- Willemsen H, Debonne M, Swennen Q, Everaert N, Careghl C, Han H, et al. Delay in feed access and spread of hatch:importance of early nutrition. Poultry Science Journal 2010;66:177-88.
- Zafarnejad K, Afzali N, Rajabzadeh M. Effect of bee glue on growth performance and immune response of broiler chickens. Journal of Applied Animal Research 2016;45:1-5.
- Zeedan KH, Battaa II, El-Neney AM, Abuoghaba AAAA, El-Kholy KH. Effect of bee pollen at difefferentlevels as natural additive on immunity and productive performance in rabbit males. Egypt Poultry Science 2017;37:213-23
- Zhang X, Habib FK, Ross M, Burger U, Lewenstein A, Rose K, et al. Isolation and characterization of a cyclic hydroxamic acid from a pollen extract, which inhibits cancerous cell growth in vitro. Journal of Medical Chemistry 2005;38:735-8.
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DATA AVAILABILITY STATEMENT
Data of the current study is available from the authors on request.
Publication Dates
-
Publication in this collection
13 Mar 2023 -
Date of issue
2023
History
-
Received
08 Feb 2022 -
Accepted
28 Nov 2022