Effects of ensiling on the quality of protein supplements for honey bees Apis mellifera
We developed a nutritious, palatable, and attractive fermented diet as supplementary food for honey bees (Apis mellifera) during periods of natural food scarcity. Two types of commercial silage inoculants were tested; bacteria and a mix of bacteria and fungi were used to ferment a protein-based feed for 7, 14, or 28 days. The positive control consisted of beebread and the negative controls were sucrose solution 50%, w/v) and the unfermented protein diet. These feeds were offered, 4 g each, along with sucrose solution ad libitum, to 60 worker bees confined in plastic cages (seven replicates, 7 days). A pool of 20 bees/cage was collected on the first day (day 0) and on the 7th day of the experiment, for protein quantification by the Bradford method and for the electrophoretic profile of the proteins by SDS-polyacrylamide gel electrophoresis. The diets fermented for 7 days were the most consumed when compared with unfermented protein diet and with beebread. All the bees that ate the fermented feeds (except for the 28-day fermentation period) presented higher titers of protein in the hemolymph when compared with the bees that did not consume any protein food (negative control and day 0). The electrophoretic analysis presented a protein profile compatible with good protein expression in the hemolymph of the bees that consumed the fermented feeds, in comparison with bees that had no access to a protein diet. Consequently, we conclude that fermenting protein supplements with silage inoculants is a viable alternative for producing protein diets that are nutritious and palatable for honey bees.
KeywordsApis mellifera fermentation artificial diets inoculants
The authors thank Dr. David De Jong for reviewing the manuscript. We are also thankful to the Agência Paulista de Tecnologia dos Agronegócios (APTA-SAA, SP), in particular, Dr. Érica Weinstein Teixeira, for providing biological material, and we thank Natucentro for providing artificial diets for bees.
JP, MM, and EE: conceived this research and designed the experiments; MM, GS, and TF: design and interpretation of the data; JP, EE, and GS: experiments and analysis; JP, MM, and TF: writing and revision. All authors read and approved.
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.
- Almeida-Dias, J. M. V; Morais, M.M; Francoy, T.M; Pereira, R.M; Turcatto, A.P and De Jong, D. (2018). Fermentation of a pollen substitute diet with beebread microorganisms increases diet consumption and hemolymph protein levels of honey bees (Hymenoptera: Apidae). Sociobiology 65, (4): 760–765 ( https://doi.org/10.13102/sociobiology.v65i4.3293) Special Issue.CrossRefGoogle Scholar
- Anderson, K.E., Sheehan, T.H., Mott, B.M., Maes, P., Snyder, L., Schwan, M.R., Walton, A., Jones, B.M, Corby-Harris, V. (2013). Microbial ecology of the hive and pollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PLoS One 8 (12) e83125. https://doi.org/10.1371/journal.pone.0083125 CrossRefPubMedPubMedCentralGoogle Scholar
- Behera, S. S., Ray, R. C., & Zdolec, N. (2018). Lactobacillus plantarum with Functional Properties: An Approach to Increase Safety and Shelf-Life of Fermented Foods. Biomed. Res. Int., 9361614. https://doi.org/10.1155/2018/9361614
- Brindza J et al. (2010). Pollen microbial colonization and food safety. Acta Chim. Slov. 3, 95–102.Google Scholar
- Ellis, A.M. and Hayes Jr, G.W. (2009). An evaluation of fresh versus fermented diets for honey bees (Apis mellifera). J. Apic. Res. 48 (3), 215–216. https://doi.org/10.3896/IBRA.22.214.171.124
- Herbert Jr, E.W. (1992) Honey bee nutrition. In ‘The hive and the honeybee’. (Ed. JM Graham). Dadant and Sons: Hamilton, pp. 197–233.Google Scholar
- Herbert Jr, E.W and Shimanuki, H. (1978). Chemical composition and nutritive value of bee-collected and bee-stored pollen. Apidologie 9 (1), 33–40. https://doi.org/10.1051/apido:19780103
- Keady, T.W.J., Steen, R.W.J., Kilpatrick, D.J., Mayne, C.S. (1994). Effects of inoculant treatment on silage fermentation, digestibility and intake by growing cattle. Grass Forage Sci. 49, 284–294. https://doi.org/10.1111/j.1365-2494.1994.tb02003.x CrossRefGoogle Scholar
- Kristensen, N.B., Sloth, K.H., Højberg, O., Spliid, N.H., Jensen, C., Thøgersen, R. (2010). Effects of microbial inoculants on corn silage fermentation, microbial contents, aerobic stability, and milk production under field conditions. Dairy Sci. 93, 3764–3774. https://doi.org/10.3168/jds.2010-3136.CrossRefGoogle Scholar
- Morais, M.M., Turcatto, A.P., Pereira, R.A., Francoy, T.M., Guidugli-Lazzarini, K.R., Gonçalves, L.S., Almeida-Dias, J.M.V., Ellis, J.D., De Jong, D. (2013b). Protein levels and colony development of Africanized and European honey bees fed natural and artificial diets. Genet. Mol. Res. 12 (4), 6915–6922. https://doi.org/10.4238/2013.December.19.10 CrossRefPubMedGoogle Scholar
- Pahlow, G.; Muck, R.E.; Driehuis, F. et al. (2003). Microbiology of ensiling. In: Buxton, D.R.; Muck, R.E.; Harrison, J.H. (Eds.) Silage science and technology. Madison: American Society of Agronomy, Crop Science Society of America, Soil Science Society of America. p. 31–93.Google Scholar
- Schröder, J.J; de Visser, W; Assinck, F.B.T; Velthof, G.L. (2013) Effects of short-term nitrogen supply from livestock manures and cover crops on silage maize production and nitrate leaching. Soil Use and Management 29 (2):151-160.Google Scholar
- Somerville, Doug & Rural Industries Research and Development Corporation (Australia) (2005). Fat bees skinny bees: a manual on honey bee nutrition for beekeepers: a report for the Rural Industries Research and Development Corporation. Rural Industries Research and Development Corporation, Barton.Google Scholar
- Sun, L. et al. (2018). Changes in microbial population and chemical composition of corn stover during field exposure and their evaluation on silage fermentation and in vitro digestibility. Asian Australas. J. Anim. Sci. https://doi.org/10.5713/ajas.18.0514
- Tortora, G. J.; Funke, B.R.; Case, C. L. (2012). Microbiology: An Introduction.10th Edition. Pearson Education, Inc., publishing as Benjamin Cummings, 937 p.Google Scholar
- Winston, M. (2003). The Biology of the Honey Bee. Harvard University Press, 294 p.Google Scholar
- Wright, G.A.; Nicolson, S.W; Shafir, S. (2017). Nutritional physiology and ecology of honey bees. Annu. Rev. Entomol., 63: 327–344. https://doi.org/10.1146/annurev-ento-020117-043423 CrossRefPubMedGoogle Scholar