0
Views
0
CrossRef citations to date
0
Altmetric
Original research article

Exploring the impact of protein diets on the honey bee (Apis mellifera L): a study on intestinal tissue health and royal jelly protein level

, ORCID Icon, & ORCID Icon
Received 18 Jul 2023, Accepted 30 Mar 2024, Published online: 24 Jul 2024

References

  • Al-Ghamdi, A. A. K., Al-Khaibari, A. M., & Omar, M. O. (2011). Consumption rate of some proteinic diets affecting hypopharyngeal glands development in honeybee workers. Saudi Journal of Biological Sciences, 18(1), 73–77. https://doi.org/10.1016/j.sjbs.2010.10.001
  • Almeida-Dias, J. M., Morais, M. M., Francoy, T. M., Pereira, R. A., Turcatto, A. P., & 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
  • Barker, R. J. (1977). Some carbohydrates found in pollen and pollen substitutes are toxic to honey bees. The Journal of Nutrition, 107(10), 1859–1862. https://doi.org/10.1093/jn/107.10.1859
  • Bocquet, M., & Tosi, S. (2022). A New coloss task force: Bee nutrition. Bee World, 99(1), 35–36. https://doi.org/10.1080/0005772X.2021.2000692
  • Bouchebti, S., Wright, G. A., & Shafir, S. (2022). Macronutrient balance has opposing effects on cognition and survival in honey bees. Functional Ecology, 36(10), 2558–2568. https://doi.org/10.1111/1365-2435.14143
  • Branchiccela, B., Castelli, L., Corona, M., Díaz-Cetti, S., Invernizzi, C., Martínez de la Escalera, G., Mendoza, Y., Santos, E., Silva, C., Zunino, P., & Antúnez, K. (2019). Impact of nutritional stress on the honeybee colony health. Scientific Reports, 9(1), 10156–10166. https://doi.org/10.1038/s41598-019-46453-9
  • Bryś, M. S., Skowronek, P., & Strachecka, A. (2021). Pollen diet—Properties and impact on a bee colony. Insects, 12(9), 798–806. https://doi.org/10.3390/insects12090798
  • Daniele, G., & Casabianca, H. (2012). Sugar composition of French royal jelly for comparison with commercial and artificial sugar samples. Food Chemistry, 134(2), 1025–1029. https://doi.org/10.1016/j.foodchem.2012.03.008
  • Elaidy, W., & Zedan, S. (2011). Effects of pollen substitute on food consumption, morphometric characters, and midgut histochemistry of Apis mellifera workers. Egyptian Journal of Experimental Biology (Zoology), 7(2), 361–369.
  • Gad, A. (1951). The head capsule for brood measurement in a honey bee colony. American Bee Journal, 3, 20–21.
  • Hagedorn, H. H., & Moeller, F. E. (1968). Effect of the age of pollen used in pollen supplements on their nutritive value for the honeybee. i. effect on thoracic weight, development of hypopharyngeal glands, and brood rearing. Journal of Apicultural Research, 7(2), 89–95. https://doi.org/10.1080/00218839.1968.11100195
  • Han, X., Sun, Y., Huangfu, B., He, X., & Huang, K. (2023). Ultra-high-pressure passivation of soybean agglutinin and safety evaluations. Food Chemistry: X, 18, 100726–100735. https://doi.org/10.1016/j.fochx.2023.100726
  • Haydak, M. H. (1949). Causes of deficiency of soybean flour as a pollen substitute for honeybees. Journal of Economic Entomology, 42(4), 573–579. https://doi.org/10.1093/jee/42.4.573
  • Hoover, S. E., Lynae, P., & Kearns, J. D. (2022). Consumption of supplemental Spring protein feeds by Western honey bee (Hymenoptera: Apidae) colonies: Effects on colony growth and pollination potential. Journal of Economic Entomology, 115(2), 417–429. https://doi.org/10.1093/jee/toac006
  • Keller, I., Fluri, P., & Imdorf, A. (2005). Pollen nutrition and colony development in honey bees: Part I. Bee World, 86(1), 3–10. https://doi.org/10.1080/0005772X.2005.11099641
  • Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage. Nature, 227(5259), 680–685. https://doi.org/10.1038/227680a0
  • Lercker, G., Caboni, M. F., Vecchi, M. A., Sabatini, A. G., & Nanetti, A. (1992). Caratterizzazione dei principali costituenti della gelatina reale. Apicoltura, 8(8), 27–37.
  • Li, C., Xu, B., Wang, Y., Feng, Q., & Yang, W. (2012). Effects of dietary crude protein levels on development, antioxidant status, and total midgut protease activity of honey bee (Apis mellifera ligustica). Apidologie, 43(5), 576–586. https://doi.org/10.1007/s13592-012-0126-0
  • Loidl, A., & Crailsheim, K. (2001). Free fatty acids digested from pollen and triolein in the honeybee (Apis mellifera carnica Pollmann) midgut. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology, 171(4), 313–319. https://doi.org/10.1007/s003600100178
  • Manning, R., Rutkay, A., Eaton, L., & Dell, B. (2007). Lipid-enhanced pollen and lipid-reduced flour diets and their effect on the longevity of honey bees (Apis mellifera L.). Australian Journal of Entomology, 46(3), 251–257. https://doi.org/10.1111/j.1440-6055.2007.00598.x
  • Mukherjee, R., Chakraborty, R., & Dutta, A. (2016). Role of fermentation in improving nutritional quality of soybean meal - A review. Asian-Australasian Journal of Animal Sciences, 29(11), 1523–1529. https://doi.org/10.5713/ajas.15.0627
  • Omar, E. M., & Amro, A. M. (2023). Improving pollen substitutes to maintain development and hemolymph parameters of honey bees (Apis mellifera L.) during pollen dearth periods. Journal of Apicultural Research, 62(4), 777–786. https://doi.org/10.1080/00218839.2023.2229111
  • Pan, L., Liu, J., Farouk, M. H., Qin, G., Bao, N., Zhao, Y., & Sun, H. (2021). Anti-nutritional characteristics and mechanism of soybean agglutinin. Biocell, 45(3), 451–459. https://doi.org/10.32604/biocell.2021.014289
  • Panettieri, V., Chatzifotis, S., Messina, C. M., Olivotto, I., Manuguerra, S., Randazzo, B., Ariano, A., Bovera, F., Santulli, A., Severino, L., & Piccolo, G. (2020). Honey bee pollen in meagre (Argyrosomus regius) juvenile diets: Effects on growth, diet digestibility, intestinal traits, and biochemical markers related to health and stress. Animals: An Open Access Journal from MDPI, 10(2), 231–247. https://doi.org/10.3390/ani10020231
  • Pang, C., Dong, K., Guo, Y., Ding, G., Lu, Y., Guo, Z., Wu, J., & Huang, J. (2022). Effects of three types of pollen on the growth and development of honey bee larvae (Hymenoptera, Apidae). Frontiers in Ecology and Evolution, 10, 1–11. https://doi.org/10.3389/fevo.2022.870081
  • Paray, B. A., Kumari, I., Hajam, Y. A., Sharma, B., Kumar, R., Albeshr, M. F., Farah, M. A., & Khan, J. M. (2021). Honeybee nutrition and pollen substitutes: A review. Saudi Journal of Biological Sciences, 28(1), 1167–1176. https://doi.org/10.1016/j.sjbs.2020.11.053
  • Ricigliano, V. A., Cank, K. B., Todd, D. A., Knowles, S. L., & Oberlies, N. H. (2022). Metabolomics-guided comparison of pollen and microalgae-based artificial diets in honey bees. Journal of Agricultural and Food Chemistry, 70(31), 9790–−9801. https://doi.org/10.1021/acs.jafc.2c02583
  • Ricigliano, V. A., Fitz, W., Copeland, D. C., Mott, B. M., Maes, P., Floyd, A. S., Dockstader, A., & Anderson, K. E. (2017). The impact of pollen consumption on honey bee (Apis mellifera) digestive physiology and carbohydrate metabolism. Archives of Insect Biochemistry and Physiology, 96(2), 1–14. https://doi.org/10.1002/arch.21406
  • Ricigliano, V. A., Williams, S. T., & Oliver, R. (2022). Effects of different artificial diets on commercial honey bee colony performance, health biomarkers, and gut microbiota. BMC Veterinary Research, 18(1), 52–65. https://doi.org/10.1186/s12917-022-03151-5
  • Sanjukta, S., & Rai, A. K. (2016). Production of bioactive peptides during soybean fermentation and their potential health benefits. Trends in Food Science & Technology, 50, 1–10. https://doi.org/10.1016/j.tifs.2016.01.010
  • Smart, M. D., Otto, C. R. V., & Lundgren, J. G. (2019). Nutritional status of honey bee (Apis mellifera L.) workers across an agricultural land-use gradient. Scientific Reports, 9(1), 16252–16261. https://doi.org/10.1038/s41598-019-52485-y
  • Szymas, B., & Przybyl, A. (2007). Midgut histological picture of the honey bee (Apis mellifera L.) following consumption of substitute feeds supplemented with feed additives. Zootechnika, 1(4), 48–56.
  • Szymaś, B., Łangowska, A., & Kazimierczak-Baryczko, M. (2012). Histological structure of the midgut of honey bees (Apis mellifera L.) fed pollen substItutes fortIfIed wIth probIotIcs. Journal of Apicultural Science, 56(1), 5–12. https://doi.org/10.2478/v10289-012-0001-2
  • Tawfik, A. I., Ahmed, Z. H., Abdel-Rahman, M. F., & Moustafa, A. M. (2022). Effect of some bee bread quality on protein content and antioxidant system of honeybee workers. International Journal of Tropical Insect Science, 43(1), 93–105. https://doi.org/10.1007/s42690-022-00888-2
  • Wang, Y., Ma, L. T., Hang, X. B., Yang, W. R., Liu, F., & Xu, B. H. (2014). Digestion of protein of two pollen types in China by the honeybee (Apis mellifera L). Apidologie, 45(5), 590–600. https://doi.org/10.1007/s13592-014-0278-1
  • Wang, W., Tan, Z., Gu, L., Ma, H., Wang, Z., Wang, L., Wu, G., Qin, G., Wang, Y., & Pang, H. (2022). Dynamics changes of microorganisms community and fermentation quality in soybean meal prepared with lactic acid bacteria and Artemisia argyi through fermentation and aerobic exposure processes. Foods (Basel, Switzerland), 11(6), 795–814. https://doi.org/10.3390/foods11060795
  • Wen, Y., Liu, A., Meng, C., Li, Z., & He, P. (2021). Quantification of lectin in soybeans and soy products by liquid chromatography-tandem mass spectrometry. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences, 1185, 122987. https://doi.org/10.1016/j.jchromb.2021.122987
  • Zakaria, M. E. (2010). Effect of the accessory protein feeding on honey bee worker tissues and Hypopharyngeal glands. Egyptian Journal of Agricultural Research, 88(3), 755–765. https://doi.org/10.21608/ejar.2010.188623
  • Zakaria, M., El Sayeh, H. A., Abdel El Azeim, M., & El Dereny, S. (2021). Role of the date palm pollen grains (Phoenix dactylifera l.) in induced antimicropial peptides synthesis and improved the royal jelly protein properties in honey bees. Journal of Plant Protection and Pathology, 12(12), 857–860. https://doi.org/10.21608/jppp.2021.220025
  • Zakaria, M. E., Ghazala, N. E., Zidan, E. W., & Abdel-Aziz, S. Y. (2016). Effeciency of some supplemental protein nutrition process in honey bee colonies in improved properties of the Hypopharyngeal glandular secretion. Egyptian Journal of Agricultural Research, 94(4), 809–819. https://doi.org/10.21608/ejar.2016.153111
  • Zheng, B., Wu, Z., & Xu, B. (2014). The effects of dietary protein levels on the population growth, performance, and physiology of honey bee workers during early spring. Journal of Insect Science (Online), 14(24), 191. https://doi.org/10.1093/jisesa/ieu053

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.