Bee pollen supplementation in diets for rabbit does and growing rabbits

Suplementação com pólen apícola em dietas para coelhas e coelhos em crescimento

ANIMAL PRODUCTION

Bee pollen supplementation in diets for rabbit does and growing rabbits

Suplementação com pólen apícola em dietas para coelhas e coelhos em crescimento

Daisa Mirelle Borges Dias^I; Maria Cristina de Oliveira^I,*; Diones Montes da Silva^I; Nadielli Pereira Bonifácio^I; Daniel da Cunha Claro^I; Wilson Aparecido Marchesin^II

^IUniversidade de Rio Verde, Rua Sen. Martins Borges, 269, 75901-340, Rio Verde, Goiás, Brazil

^IICooperativa Agroindustrial dos Produtos Rurais do Sudoeste Goiano, Rio Verde, Goiás, Brazil

ABSTRACT

It was evaluated the effects of bee pollen (BP) on the doe and kits productivity and on the carcass and organs of the rabbits. Twenty White New Zealand does and their kits were used in a randomized block design, with four treatments and five blocks, in a factorial arrangement 2 x 2 with two supplementation levels for the doe and for the kits after the weaning. BP supplementation for the does did not influence (p > 0.05) the doe and kit productivity during the lactation, except by the kits survival rate (p < 0.003), the total (p < 0.002) and daily (p < 0.001) milk production that increased in supplemented doe. BP supplementation for the doe and/or kits did not affect (p > 0.05) the rabbit performance from the weaning until the slaughter age, the slaughter weight, carcass characteristics, except by the spleen and small intestine weights, higher in supplemented rabbits. It was not recommended that BP supplementation for does and/or rabbits for not improving the rabbit productive performance.

Keywords: alimentary additive, rabbit nutrition, bee product.

RESUMO

Os efeitos do pólen apícola (PA) sobre a produtividade de coelhas e láparos e sobre a carcaça e órgãos dos coelhos foram avaliados. Foram utilizadas 20 coelhas Nova Zelândia Branco e seus láparos em delineamento em blocos ao acaso, com quatro tratamentos e cinco blocos, em arranjo fatorial 2 x 2 com dois níveis de suplementação para a coelha e para os láparos após o desmame. A suplementação com PA para as coelhas não influenciou (p > 0,05) a produtividade da coelha e dos láparos durante a lactação, exceto pela taxa de sobrevivência dos láparos (p < 0,003) e a produção total (p < 0,002) e diária (p < 0,001) de leite que aumentou nas coelhas suplementadas. A suplementação para as coelhas e/ou láparos não afetou (p > 0,05) o desempenho dos coelhos do desmame até a idade ao abate, o peso ao abate, características da carcaça, exceto pelos pesos do baço e intestino delgado, maiores em coelhos suplementados. Não foi recomendada a suplementação com PA para coelhas e/ou láparos por não melhorar o desempenho produtivo.

Palavras-chave: aditivo alimentar, nutrição de coelhos, produto apícola.

Introduction

Bee pollen (BP) production started modestly in Brazil at the end of the 1980s. Nowadays, the favorable market for natural products, complementary to the diets or with therapeutics effects, is stimulating and promoting the improvement of the bee productive chain (BARRETO et al., 2005).

BP is an agglomerate of flower pollen collected from several plant sources by the bees and mixed with nectar and secretions from the hypofaryngean glands (CARPES et al., 2008) and is a rich source of proteins, essential amino acids, containing more than 51% polyunsaturated fatty acids, and 39% are linolenic acid, 20% palmitic acid, and 13% linoleic acid; more than 12 vitamins, 28 minerals, 11 enzymes or coenzymes, 11 carbohydrates, mainly glucose, fructose and sucrose, besides flavonoids, carotenoids and phytosterols (ATTIA et al., 2011a).

Amino acids can be found in its composition such as histidine, leucine, isoleucine, tryptophan, valine, lysine, and others) and vitamins of the B complex, A, C, D and K₃. BP also contains antibiotic substances, active on the coli bacilli species and on certain species of the Proteus and Salmonella genera, and antioxidant substances (BASTOS et al., 2003).

Amino acids, vitamins and trace elements of BP are nutritionally beneficial for improving intestinal absorption due the stimulus to the development, proliferation and differentiation of intestinal cells and because they improve the environmental conditions for the intestinal microbial ecosystem. BP can also improve the cell immune response, the antibody production speed, and reinforce the immunological system (SONG et al., 2005).

The BP composition is very variable and depends on the local harvest and plant source and consists of 75.9 – 98.31% dry matter, 97.9% organic matter, 1.5 – 4.8% ash, 15.04 – 27.69% crude protein, 3.6 – 14% fats, and 68.1% total carbohydrates (BASTOS et al., 2003; FUNARI et al., 2005; CARPES et al., 2009; MODRO et al., 2009). The BP mineral composition (mg 100 g^-1) is comprised of P (346 – 710), Ca (85 – 260), Na (93 – 358) K (465 – 670), Mg (77 – 82) (BELL et al., 1983; FUNARI et al., 2005; CARPES et al., 2009), along with Se (2100 ppm), Fe (114 ppm), Zn (88 ppm), Cu (15 ppm), and Mn (32 ppm) (FUNARI et al., 2005).

However, its use as an additive in animal feeding is only incipient and reports in the literature are scarce. In studies with swine, Zeng et al. (2004) noted that BP included in the diets improved the amino acid profile of the pig meat. Wang and Cheng (2005) evaluated the inclusion of BP (1, 2, 3, 4 and 5%) in diets for growing and finishing pigs and reported that the 4 and 5% levels improved the daily weight gain and the feed: gain ratio of the animals.

Evaluating 1.5% BP inclusion in diets for broilers, Song et al. (2005) reported that the intestinal cells were longer in the three small intestine segments until the three first weeks of life, and there was no difference after this period. Wang et al. (2007) used 1.5% BP in broiler diets and demonstrated that the BP had a trophic effect in the small intestine and, consequently, promoted the growth of the birds.

Attia et al. (2011a) evaluated the use of 100, 200 and 300 mg BP kg^-1 body weight (BW) for rabbit does and verified that the dose of 200 mg kg^-1 resulted in a higher conception rate, a lower number of service conception rates, a higher litter size, and higher milk production compared to the control group.

Thus, the present study was carried out to evaluate the effects of BP administration to does and/or rabbits, on the doe nursing efficiency, the productive performance, and on the carcass characteristics in slaughtered rabbits.

Material and methods

Twenty multiparous 2.6 years old New Zealand White does were individually allocated in cages (0.8 x 0.75 x 0.67 m, length, width and height, respectively), with ceramic feeder and drinker. The mean weight of the does was 4048 ± 118 g and all of them had seven to nine kits. The does fed ad libitum a commercial pellet feed (17% crude protein, 15% crude fiber, 1.11% calcium, 0.77% phosphorus, 0.90% lysine, 0.63% methionine + cysteine, and 2300 kcal kg^-1 digestible energy). The determined composition of the BP used was, in %, 3.83 moisture, 22.97 crude protein, 0.39 calcium, 0.99 phosphorus, 3.14 mineral matter and 1.71 fats, in addition to 3953 kcal kg^-1 crude energy and pH 4.68.

The experimental design before the weaning was in randomized blocks with two treatments and 10 replications, with two supplementation levels for the rabbit does (0 and 1 g) and, after weaning, a randomized block design in a 2 x 2 factorial arrangement was used with two supplementation levels for the rabbit does (0 and 1 g) and two supplementation levels for the kits after weaning (0 and 1 g), with four treatments and five replications. In both cases, the replications were carried out at different times of the year, from October 2011 to February 2012. The treatments consisted of BP supplementation levels for the does and kits as a water suspension. The BP was provided from one week before until one week after the mating for the does, once a day during the two weeks, and later twice a week throughout the lactation period. BP was provided twice a week for the kits from the weaning up to the slaughter age. The BP was given by insulin syringe in the oral cavity.

The rabbit does were mated with non-treated adult New Zealand White male rabbits 20 days after kindling using mother-litter separation. Each doe was subjected to two services within 30 minutes by the same buck, in the morning and in the afternoon. Each doe was transferred to the buck's cage for mating and after copulation; she was returned to her cage. The rabbit does that failed to become pregnant were discarded from the experiment. Pregnancy was diagnosed by abdominal palpation at day 11 after service.

On the next day postpartum, the doe was separated from the litter and she was taken to the nest only once a day, in the morning, for 15 – 20 minutes, to nurse the kits. At this moment, the doe was weighed before and after the nursing to determine, by difference, the total milk production (ATTIA et al., 2011a).

The following traits were measured: daily feed intake for the does throughout the lactation period and for the kits from the birth to weaning. The total, daily and by kit milk yield, the litter size at birth, kit survival rate until weaning, kit body weight at birth and 35 days of age, weight gain at 35 days, feed conversion ratio of kits from birth until 35 days of age. The total milk production was divided by the number of kits of each doe to determine the milk yield per kit. The kit feed conversion ratio was calculated considering the total feed intake and the milk intake of each kit. The kits were weaned at 35 days.

In the performance trial, eighty rabbits from treated and non-treated does, with an initial weight of 753 ± 51.40 g were used. The animals (two males and two females) were placed in galvanized cages (0.77 x 0.60 x 0.39 m, length x width x height) with an external feeder and three nipple drinkers. The rabbits were fed ad libitum a commercial pellet feed (cited above).

The kits were weighed at weaning and at 82 days (slaughter age) and the following traits were determined: weaning weight, final weight and daily feed intake, daily weight gain, feed conversion rate and survival rate from weaning until the slaughter age.

At 82 days, the rabbits were food fasted for 8 hours and weighed in order to obtain the slaughter weight. Later, the animals were slaughtered and the carcasses, with no head, feet and viscera, were weighed. Edible viscera, spleen and small intestine were also weighed. The carcass yield and organ relative weight were determined considering the slaughter weight and carcass weight, respectively. The small intestine length was measured and the intestinal density was calculated dividing the intestine weight (g) by its length (m) (ABDEL-FATTAH et al., 2008).

The statistical analysis of the characteristics related to the does and their kits followed the mathematic model comprised by one factor (BP supplementation for the does) and total and daily milk productions were analyzed using the litter size as a co-variable. The other characteristics, after weaning, followed the mathematic model in a 2 x 2 factorial arrangement, as described above. The analyses were performed using the SAEG software and the means were compared by the F test, at 5% probability level.

Results and Discussion

BP supplementation for the does during the mating and lactation period affected (p > 0.05) the doe nursing efficiency (Table 1) and the kit growth performance from birth until weaning (Table 2) due to the higher total (p < 0.002) and daily (p < 0.002) milk production in the does supplemented with BP and higher (p < 0,003) kits survival rate.

The improvement on the total and daily milk production was due to the presence of a high micronutrient content (polyunsatured fatty acids, mineral, vitamins, amino acids, etc.) and protective agents, such as flavonoids, carotenoids, and phenolic constituents in the BP (LEJA et al., 2007; SARIC et al., 2009). Attia et al. (2011a) also reported a higher milk production in does supplemented with 200 mg BP kg^-1 BW. This effect is important because, up to weaning, milk is the main food for young rabbits, even if the intake of solid food begins from 18 to 21 days of age (BOVERA et al., 2009). A higher milk supply for the kits resulted in a better survival rate during the lactation period.

Although does supplemented with BP produced more milk, this effect was not reflected in the body weight, weight gain, feed intake and feed conversion rate of the kits from birth to weaning.

These results are different than those reported by Attia et al. (2011a) that evaluated the effects of BP supplementation of 100, 200 and 300 mg kg^-1 BW for does and noted the does had a lower feed intake up to the 200 mg kg^-1 level. The authors also verified that the litter size and kit body weight at 7, 14, 21 and 28 days of age were higher for the does supplemented with 200 mg BP kg^-1 BW.

BP administration for does and/or weaned rabbits did not affect (p > 0.05) the productive performance (Table 3) and the carcass characteristics (Table 4), except for the spleen and small intestine weights, that were higher in supplemented rabbits.

Although the BP is a substance rich in carbohydrates, proteins, amino acids, fats (60-91% are polyunsatured fatty acids) (WANG et al., 2005), vitamins A, B, C, D, E (MARCHINI et al., 2006) and B complex, minerals, carotenoids and flavonoids (WANG et al., 2005), BP supplementation for the does and/or growing rabbits was not sufficient to improve performance from weaning up to slaughter age. According to Bell et al. (1983), BP is rich in proteins and has a favorable amino acid profile, but their digestibilities are relatively low, that is a limiting factor for its use as a food for humans and monogastrics.

Different results were reported by Attia et al. (2011a) in which kits born of does supplemented with BP showed higher growth rates and lower feed intake from 4 to 8, 9 to 12 and 4 to 12 weeks of age, compared to the control group. As a consequence, the feed conversion rate was also better.

Attia et al. (2011b) observed that the feed efficiency was improved in growing rabbits due to the supplementation of 200 - 500 mg BP kg^-1 BW compared to the unsupplemented control group, during moderate and hot seasons, from weaning to mature age.

Reports about BP effects on the carcass and organ characteristics in rabbits are scarce. Song et al. (2005) and Wang et al. (2007) evaluated the BP effects on the liver and pancreas weights in broilers and noted that their weights were higher in treated broilers, however, Ke et al. (2009), studying the use of 0.2% BP polysaccharides in broiler diets, reported that BP did not influence the carcass yield of the birds.

Spleen weight was higher in rabbits treated with BP from weaning to slaughter age. According to Wang et al. (2005), BP also has nucleic acids that stimulate the natural killer cells and T lymphocyte activities, such as vitamin A and E and microelements, such as Fe, Se, Zn and Mn, which promote the proliferation and differentiation of immune system cells. These results are in agreement with Wang et al. (2005) who included 1.5% BP in broiler feed and noted that the spleen absolute weight increased due to the BP, but not the relative weight. Cheng (2009) studied the effect of BP inclusion (0, 0.5, 1 and 1.5%) in broiler diets and verified that the spleen weight was higher from the 7^th up to 42^nd day of age.

The small intestine weight increased due to the BP supplementation because its cells require amino acids, vitamins, trace elements for their development, proliferation and differentiation and these constituents are also beneficial to the intestinal microbiota. Even though the intestine weight was higher in supplemented rabbits, the intestinal density was not influenced by the BP. This higher weight in the same length means there was an improvement in the intestinal surface for the nutrient absorption (SONG et al., 2005; WANG et al., 2005). Wang et al. (2007) reported that the 1.5% BP in broiler diets did not influence the small intestine length but the authors also verified that the villi and intestinal glands were more developed in treated birds, demonstrating the BP trophic effect on the small intestine.

The small intestine density is an indirect measure of the intestinal mass and function (CROOM et al., 2006), villi dimension (PALO et al., 1995), and intestinal wall thickness (TREVISI et al., 2009). Lower intestinal density might mean lower villi height and width, which results in lower intestinal digestive and absorptive capacities (CORLESS; SELL, 1999).

Conclusion

Bee pollen supplementation for does improved milk production and kit survival rate, but is not recommended for rabbits after weaning due to the lack of positive effect on their productive performance.

Acknowledgements

Our thanks to the CNPq for the scholarship and to the Cooperativa Mista dos Produtores Rurais do Sudoeste Goiano – COMIGO for donating the commercial feed for this experiment.

Received on October 23, 2012.

Accepted on March 26, 2013.

• ABDEL-FATTAH, S. A.; EL-SANHOURY, M. H.; EL-MEDNAY, N. M.; ABDEL-AZEEM, F. Thyroid activity, some blood constituents, organs morphology and performance of broiler chicks fed supplemental organic acids. International Journal of Poultry Science, v. 7, n. 3, p. 215-222, 2008.
• ATTIA, Y. A.; AL-HANOUN, A.; EL-DIN, A. E.; BOVERA, F.; SHEWIKA, Y. E. Effect of bee pollen levels on productive, reproductive and blood traits of NZW rabbits. Journal of Animal Physiology and Animal Nutrition, v. 95, n. 3, p. 294-303, 2011a.
• ATTIA, Y. A.; 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 wither months. Journal of Animal Physiology and Animal Nutrition, v. 95, n. 1, p. 17-26, 2011b.
• BARRETO, L. M. R. C.; FUNARI, S. R. C.; ORSI, R. O. Composição e qualidade do pólen apícola proveniente de sete estados brasileiros e do Distrito Federal. Boletim da Indústria Animal, v. 62, n. 2, p. 167-175, 2005.
• BASTOS, D. H. M.; ROCHA, C. I.; CUNHA, I. B. S.; CARVALHO, P. O.; TORRES, E. A. S. Composição e qualidade de pólen apícola comercializado em algumas cidades nos estados de São Paulo e Minas Gerais Brasil. Revista do Instituto Adolfo Lutz, v. 62, n. 3, p. 239-244, 2003.
• BELL, R. R.;  THORNBER, E. J.; SEET, J. L. L.; GROVES, M. T.; HO, N. P.; BELL, D. T. Composition and protein quality of honeybee-collected pollen of Eucalyptus marginata and Eucalyptus calophylla. Journal of Nutrition, v. 113, n.12, p. 2479-2484, 1983.
• CARPES, S. T.; CABRAL, I. S. R.; LUZ, C. F. P.; CAPELETTI, J. P.; ALENCAR, S. M.; MASSON, M. L. Palynological and physicochemical characterizations of Apis mellifera L. bee pollen in the Southern region of Brazil. Journal of Food, Agriculture and Environment, v. 7, n. 3-4, p. 667- 673, 2009.
• CARPES, S. T.; PRADO, A.; MORENO, I. A. M.; MOURÃO, G. B.; ALENCAR, S. M.; MASSON, M. L. Avaliação do potencial antioxidante do pólen apícolaproduzido na região sul do Brasil, Química Nova, v. 31, n. 7, p. 1660-1664, 2008.
• CHENG, Y. Effect of bee pollen on the growth of immune organs of miscellaneous broilers. Animal Husbandry and Feed Science, v. 30, n. 1, p. 23-24, 2009.
• CORLESS, A. B.; SELL, J. L. The effects of delayed access to feed and water on the physical and functional development of the digestive system of young turkeys. Poultry Science, v. 78, n. 8, p. 1158-1169, 1999.
• CROOM, W. J.; DECUBELLIS, J.; COLES, B. A.; DANIEL, L. R.; CHRISTENSEN, V. L. Effect of in ovo peptide YY on the ontogeny of glucose transport in turkey poults. International Journal of Poultry Science, v. 5, n. 2, p. 128-133, 2006.
• FUNARI, S. R. C.; ROCHA, H. C.; SFORCIN, J. M.; FILHO, H. G.; CURI, P. R.; GOMES DIERCKX, S. M. A; FUNARI, A. R. M.; ORSI, R. O. Composições bromatológica e mineral do pólen coletado por abelhas africanizadas (Apis mellifera L.) em Botucatu, Estado de São Paulo. Archivos Latinoamericano de Produccion Animal, v. 11, n. 2, p. 88-93, 2005.
• KE, P.; SUN, H.; GAO, Z. Effect of bee pollen polysaccharide on growth performance of broilers and chemical compositions of muscle. Feed Industry, v. 27, n. 12, p. 36-38, 2009.
• LEJA, M.; MARECZEK, A.; WYZGOLIK, G.; KLEPACZ-BANIAK, J.; CZEKONSKA, K. Antioxidative properties of bee pollen in selected plant species. Food Chemistry, v. 100, n. 1, p. 237-240, 2007.
• MARCHINI, L. C.; REIS, V. D. A.; MORETI, A. C. C. C. Composição fisico-química de amostras de pólen coletado por abelhas africanizadas. Ciência Rural, v. 36, n. 3, p. 949-953, 2006.
• MODRO, A. F. H.; SILVA, I. C.; LUZ, C. F. P.; MESSAGE, D. Analysis of pollen load based on color, physicochemical composition and botanical source. Anais da Academia Brasileira de Ciências, v. 81, n. 2, p. 281-285, 2009.
• PALO, P. E.; SELL, J. L; PIQUER, F. J.; SOTO SATANOVA, M. F.; VILASECA, L. Effect of early nutrient restriction on broiler chicken. Performance and development of gastrointestinal tract. Poultry Science, v. 74, n. 1, p. 88-110, 1995.
• SARIC, A.; BALOG, T.; SOBOCANEC, S.; KUSIC, B.; SVERKO, V.; RUSAK, G.; LIKIC, S.; BUBALO, D.; PINTO, B.; REALI, D.; MAROTTI, T. Antioxidant effects of flavonoid from croatian Cystus incanus L. rich bee pollen. Food and Chemical Toxicology, v. 47, n. 3, p. 547-554, 2009.
• SONG, Y.; WANG, J.; SHENG, L.; SHANG, C. Effect of bee pollen on the development of digestive gland of broilers, China Animal Husbandry and Veterinary Medicine, v. 37, n. 4, p. 14-17, 2005.
• TREVISI, P.; MELCHIOR, D.; MAZZONI, M.; CASINI, L.; DE FILIPPI, S.; MINIERI, L.; LALATTA-COSTERBOSA, G.; BOSI, P. A tryptophan-enriched diet improves feed intake and growth performance of susceptible weanling pigs orally challenged with Escherichia coli K88. Journal of Animal Science, v. 87, n. 1, p. 148-156, 2009.
• WANG, J.; JIN, G. M.; ZHENG, Y.; LI, S.; WANG, H. Effect of bee pollen on development of imune organ of animal. China Journal of Chinese Materia Medica, v. 30, n. 19, p. 1532-1536, 2005.
• WANG, J.; LI, S.; WANG, Q.; XIN, B.; WANG, H. Trophic effect of bee pollen on small intestine in broiler chickens. Journal of Medicinal Food, v. 10, n. 2, p. 276-280, 2007.
• WANG, Q.; CHENG, Q. Effect of bee-pollen on growth performance and meat quality of growing-finishing swine. Journal of Bee, v. 3, n. 1, p. 3-4, 2005.
• ZENG, Z. J.; LI, L.; ZHENG, Y. L.; MAO, F. G.; DUAN, Y. B. A study on the effect of compound preparaions of propolis and pollen on meat quality and flavor. Acta Agriculturae Universitatis Jiangxiensis, v. 26, n. 5, p. 778-780, 2004.

Publication Dates

• Publication in this collection
  12 Nov 2013
• Date of issue
  Dec 2013

History

• Received
  23 Oct 2012
• Accepted
  26 Mar 2013