Temporal variation in production and nutritional value of pollen used in the diet of Apis mellifera L. in a seasonal semideciduous forest
DOI:
https://doi.org/10.13102/sociobiology.v66i2.2879Keywords:
Bee flora, Bee nutrition, Bee pollen, Beekeeping, Nutrition, Pollen production.Abstract
The flora of mountain formations in the Caatinga biome is composed predominantly by semi-deciduous species with representatives of both Atlantic and Amazon forest. Information on the potential for bee pollen production of these species is limited. In this study we evaluated the potential of production, the temporal variation, the botanical origin and the nutritional value of bee pollen produced in a seasonal semideciduous forest in northeastern Brazil. We identified a total of 252 flowering plant species throughout the year. The diet of Apis mellifera consisted of 74 pollen types distributed in 58 genera and 27 families. We identified two production peaks of bee pollen, the highest occurring in the rainy season. Nutritional value considering crude protein, carbohydrates, lipids and mineral matter changed over the study period, with influence of rainfall on the dry matter level. Some taxonomic groups of plants showed a strong relationship with nutrients, suggesting that although the diet of A. mellifera is broadly diversified, this species devoted most of its pollen foraging effort on the genus Mimosa and the palm tree species of Attalea speciosa. The results show that the seasonal semideciduous forest of the mountain range in the Northeast Brazil presents plant species: Mimosa caesalpiniifolia, Baccharis trinervis, Mimosa tenuiflora Myracrodruom urundeuva, Cecropia pachystachya, Attalea speciosa, with high nutritional level and potential for the pollen production.
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Almeida-Muradian L. B., Pamplona L. C., Coimbra S. & Barth O. M. (2005). Chemical composition and botanical evaluation of dried bee pollen pellets. Journal of Food Composition and Analysis, 18: 105-111. doi: 10.1016/j.jfca.2003.10.008.
Alves, R.F. & Santos F.A.R. (2014). Plant sources for bee pollen load production in Sergipe, northeast Brazil. Palynology, 38: 90-100. doi: 10.1080/01916122.2013.846280
AOAC, Association of Official Analytical Chemists. (1990). Official methods of analysis. 15. ed. Vol. I. AOAC, Arlington. 684 p.
Araujo-Filho, J.A. (2013). Manejo Pastoril Sustentável da caatinga. Pernambuco Cidade Gráfica e Editora LTDA, 200p
Arruda V.A.S.D., Pereira A.A.S., Estevinho L.M. & Almeida-Muradian L.B.D. (2013). Presence and stability of B complex vitamins in bee pollen using different storage conditions. Food and Chemical Toxicology, 51: 143-148. doi: 10.1016/j.fct.2012.09.019
Avni, D., Hendriksma H.P., Dag A., Uni Z. & Shafir S. (2014). Nutritional aspects of honey bee-collected pollen and constraints on colony development in the eastern Mediterranean, Journal of Insect Physiology, 69: 65-73. doi: 10.1016/j.jinsphys.2014.07.001
Barreto, L.M.R.C., Funari S.R.C. & Orsi R.O. (2005). Composição e qualidade do pólen apícola proveniente de sete estados brasileiros e do Distrito Federal, Boletim de Indústria Animal, 62: 167-175.
Barreto, L.M.R.C., Funari S.R.C., Orsi, R.O. & Dib A.P. (2006). Produção de pólen no Brasil, Taubaté. Cabral Editora e Livraria Universitária, 99 p
Barth, O.M. (1970). Análise microscópica de algumas amostras de mel. 1. Pólen dominante. Anais da Academia Brasileira de Ciências, 42: 351-366.
Bauermann, S.G., Radaeski J.N., Evaldt A.C.P., Queiroz E.P., Mourelle D., Prieto A.R. & Silva C.I. (2013). Pólen nas angiospermas: diversidade e evolução, Canoas: ULBRA, 214p
Blochtein, B., Freitas S.W., Ribeiro M.F., Vidal M.F. & Cavalcante M.C. (2010). Aspectos da biologia floral, visitantes florais e sucesso reprodutivo de Mimosa caesalpiniifolia (Benth) em Limoeiro do Norte, Ceará, Brasil, in: Serpa A.S.P, Costa C.A., El-Hani C.N., Ramacciotti D.E.L., Filho J.T.C., Novaes A.B. (Eds.), Biologia e Ecologia da Polinização, (pp. 137-146). Bahia: EDUFBA.
Bogdanov, S. (2015). Pollen: Production, Nutrition and Health: A Review, Product Science, [online] http://www.bee-hexagon.net/files/file/fileE/Health/PollenBook2Review.pdf (accessed on 16 December 2015).
Brodschneider, R. & Crailsheim K. (2010). Nutrition and health in honey bees. Apidologie, 41: 278-294. doi: 10.1051/apido/2010012
Carvalho, A.R. (2013). Normas pluviométricas e probabilidade de safra agrícola de sequeiro no Ceará, Fortaleza: Tipografia Íris 224 p.
Colwell, M.J., Williams G.R., Evans R.C. & Shutler D. (2017). Honey bee-collected pollen in agro-ecosystems reveals diet diversity, diet quality, and pesticide exposure. Ecology and Evolution, 7: 7243-7253. doi: 10.1002/ece3.3178
Dimou, M. & Thrasyvoulou A. (2007). Seasonal variation in vegetation and pollen collected by honeybees in Thessaloniki, Greece. Grana, 46: 292-299.
Dobson, H.E.M. (1988). Survey of Pollen and Pollenkitt Lipids - Chemical Cues to Flower Visitors? American Journal of Botany, 75: 170-182.
Erdtman, G. (1960). The acetolized method. A revised description. Svensk Botanisk Tidskrift, 54: 561-564.
Estevinho, L.M., Rodrigues S. & Pereira A.P., Feás X. (2012). Portuguese bee pollen: palynological study, nutritional and microbiological evaluation. International Journal of Food Science and Technology, 47: 429-435. doi: 10.1111/j.1365-2621.2011.02859.x
FUNCEME, Fundação Cearense de Meteorologia e Recursos Hídricos (2012-2013). http://www.funceme.br/index.php/areas/23-monitoramento/meteorol%C3%B3gico/548-gr%C3%A1fico-de-chuvas-dos-postos-pluviom% C3%A9tricos#site (accessed on 11 december 2015)
Hill, P.S., Wells P.H. & Wells H. (1997). Spontaneous flower constancy and learning in honey bees as a function of colour. Animal Behaviour, 54: 615-627. doi: 10.1006/anbe.1996.0467
Komosinska-Vassev, K., Olczyk P., Kaźmierczak J., Mencner L., Olczyk K. (2015). Bee Pollen: Chemical Composition and Therapeutic Aplication, Evidence-Based Complementary and Alternative Medicine, 2015. doi: 10.1155/2015/297425
Köppen, W. (1948). Climatologia: com um estúdio de los climas de latierra, Cidade do México Fundo de Cultura: Economica, 478 p
Krebs, C.J. (1999). Ecological methodology, Benjamin/Cummings, Menlo Park, California: Longman, 620p
Louveaux, J., Maurizio A. & Vorwohl G. (1970). Methods of melissopalynology, Bee World, 51: 25-138.
Louveaux, J., Maurizio A. & Vorwohl G. (1978). Methods of melissopalynology, Bee World, 59: 139-157.
Magurran A.E. (2003). Measuring Biological Diversity. London: Blackwell Publishing Limited, 260 p
Maia-Silva, C., Imperatriz-Fonseca V.L., Silva C.I. & Hrncir, M. (2015). Survival strategies of stingless bees (Melipona subnitida) in an unpredictable environment, the Brazilian tropical dry forest. Apidologie, 46: 631-643. doi: 10.1007/s13592-015-0354-1
Maia-Silva, C., Silva C.I., Hrncir M., Queiroz R.T. & Imperatriz-Fonseca V.L. (2012). Guia de plantas visitadas por abelhas na Caatinga. Fortaleza: Fundação Brasil Cidadão 191p.
Marchini, L.C., Reis V.D.A. & Moreti A.C.C.C. (2006). Composição físico-química de amostras de pólen coletado por abelhas africanizadas Apis mellífera (Hymenoptera: Apidae) em Piracicaba, estado de São Paulo. Ciência Rural, 36: 949-953. doi: 10.1590/S0103-84782006000300034
Melo, A.A.M., Estevinho M.L.M.F., Sattler J.A.G., Souza B.R., Silva-Freitas A., Barth O.M. & Almeida-Muradian L.B. (2015). Effect of processing conditions on characteristics of dehydrated bee-pollen and correlation between quality parameters, LWT-Food Science and Technology, 65:808-815. doi: 10.1016/j.lwt.2015.09.014
Melo, A.A.M., Freitas, A.D.S., Barth, O.M., & Almeida-Muradian, L.B. (2018). Produção, beneficiamento e adequação à legislação do pólen apícola desidratado, produzido no Brasil. Revista Ciência em Extensão, 14: 55-73.
Milfont, M.O., Freitas B.M. & Alves J.E. (2011). Pólen apícola. Manejo para a produção de pólen no Brasil. Viçosa: Editora Aprenda Fácil, 102p
Montero, I. & Tormo R. (1990). Análisis polínico de mieles de cuatro zonas montañosas de Extremadura, Anais Associação de Palinologia. Leng. Esp. 5, 71-78.
Negrão, A.F., Barreto L.M.R.C & Orsi R.O. (2014). Influence of the Collection Season on Production, Size, and Chemical Composition of Bee Pollen Produced by Apis mellifera Journal of Apicultural Science, 58: 5-10. doi:10.2478/jas -2014-0017
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’hara, R.B. & Oksanen, M.J. (2013). Package ‘vegan’. Community ecology package, version, 2.9
Pacheco, Filho A.J.D.S, Verola C.F., Verde L.W.L. & Freitas B.M. (2014). Bee-flower association in the Neotropics: implications to bee conservation and plant pollination, Apidologie, 46: 530-541. doi: 10.1007/s13592-014-0344-8
Pacini, E. & Casadoro G. (1981). Tapetum plastids of Olea europaea L., Protoplasma, 106: 289-296.
R Development Core Team. (2014). R: A language and environment for statistical computing, The R Foundation for Statistical Computing, Viena.
Rebolledo, R., Riquelme M., Huaiquil S., Sepúlveda Ch G & Aguilera A. (2011). Estudio comparativo de laproducción de polen y mielenun sistema de doble reina versus una por colmenaen La Araucanía, Chile. Idesia (Arica), 29: 139-144. doi: 10.4067/S0718-34292011000200018
Santos, F.D.S., Sousa M.B., Nascimento J.E.M., Andrade L.B.S. & Figueiredo M.F. (2014). Flora fanerogâmica do Sítio Santo Inácio, Meruoca-CE, Enciclopédia Biosfera, 10: 3291-3304.
Sattler, J.A.G., Melo I.L.P., Granato D., Araújo E., Freitas A.D.S., Barth O.M., Almeida-Muradian L.B. (2015). Impact of origin on bioactive compounds and nutritional composition of bee pollen from southern Brazil: A screening study, Food Food Research International, 77: 82-91. doi: 10.1016/j.foodres. 2015.09.013
Silva, C.I., Ballestero P.L.O., Palmero A.M., Bauermann S.G., Evaldt A.C.P. & Oliveira P.E. (2010). Catálogo polínico: Palinologia aplicada em estudos de conservação de abelhas do gênero Xylocopa no Triângulo Mineiro. Minas Gerais: EDUFU, 154p
Silva, C.I., Araújo G. & Oliveira P.E.A.M. (2012). Distribuição vertical dos sistemas de polinização bióticos em áreas de cerrado sentido restrito no Triângulo Mineiro, MG, Brasil. Acta Botanica Brasilica, 66: 748-760.
Silva, C.I., Gropdo M., Bauermann S.G., Imperatriz-Fonseca V.L., Saraiva A.M., Queiroz E.P & Garófalo C.A. (2014). Catálogo polínico das plantas usadas por abelhas no Campus da USP de Ribeirão Preto. Ribeirão Preto: Holos, 153p
Sniffen, C.J., O’connor J.D., Van Soest P.J., Fox D.G. & Russel J.B. (1992). A net carbohydrate and protein system for evaluating cattle diets. II. Carbohydrate and protein availability. Jounal of Animal Science, 70: 3562-3577.
Stang, M., Peter G.L.K. & Meijden E.V. (2007). Asymmetric specialization and extinction risk in plant–flower visitor webs: a matter of morphology or abundance? Oecologia, 151: 442-453.
Villanueva M.O., Marquina A.D. & Serrano R.B. Abellán G.B. (2002) The importance of bee-collected pollen in the diet: a study of its composition, International Journal of Food Sciences and Nutrition, 53: 217-224. doi: 10.1080/ 09637480220132832
Villanueva-G, R. & Roubik, D. W. (2004). Why are African honey bees and not European bees invasive? Pollen diet diversity in community experiments. Apidologie, 35: 481-491.
Yang, K., Wu D., Ye X., Liu D., Chen J. & Sun P. (2013) Characterization of chemical composition of bee pollen in China. Journal of Agricultural and Food Chemistry, 61: 708-718. doi: 10.1021/jf304056b
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