The Feeding Effect of Invert Sugar and Sucrose Solutions on The Quality of Produced Honey and The Performance of Honey Bee Colonies Overwintering

Yıl 2026, Cilt: 23 Sayı: 2, 691 - 702, 16.03.2026

Mostafa Abdella , Salah H. Rateb , Mohammed M. Khodairy , Eslam M. Omar

https://doi.org/10.33462/jotaf.1694942

https://izlik.org/JA23FP23FF

Öz

Sugar nutrition is essential for managing and maintaining healthy honey bee colonies, especially during nectar scarcity. This study aimed to evaluate the use of invert sugar as a nectar substitute, comparing its impact on the quality of stored honey and colony performance during overwintering to that of a traditional sucrose solution commonly used by beekeepers. Two separate field experiments were carried out. The first experiment took place in the spring under both isolated and free-flying conditions to assess the quality of honey caused by artificial feeding. Sealed honey was collected and analyzed to determine the percentage of sucrose, glucose, fructose and HMF. Also, the pollen density in honey samples was evaluated as another detector for honey quality. The second experiment was conducted during the winter and nectar scarcity to evaluate the effects of the two supplemental sugar feedings on the overwintering performance of honey bee colonies. We measured the sealed brood and the bee bread areas to indicate the colony's growth and development. The results showed that colonies fed sucrose solutions produced honey that fulfilled standard specifications regardless of whether they were placed under an insulator or free-flying colonies, with sugar percentages and HMF levels that comply with standard specifications and no significant difference in sugar content with honey collected from colonies provided with invert sugar. In contrast, colonies provided with invert sugar had higher HMF values in the produced honey when it was the only sugar source under isolation. However, when the colonies were fed invert sugar during the winter, they became more active in collecting pollen, which increased brood rearing and made them more ready for the beginning of the active season. Because it increases pollen-collecting activity, Invert sugar can be considered as a suitable sugar supplement to honey. It may be more successful than sucrose during periods of overwintering and nectar scarcity, resulting in more brood being raised and better preparation is made before the active season. However, care should be taken because overuse at times when natural nectar sources are available could increase the HMF level in the produced honey, causing low-quality honey production.

Anahtar Kelimeler

Carbohydrate , Nutrition , Nectar scarcity , Honey quality , Winter losses

Etik Beyan

There is no need to obtain permission from the ethics committee for this study.

Teşekkür

The authors thank the beekeepers who maintain Assiut University's Faculty of Agriculture apiary for their support. We also thank Prof. Dr. Mohamed Omar for his guidance and Prof. Dr. Youssef M. Omar for his help with his Economic Entomology lab.

Kaynakça

• Abdella, M., Rateb, S. H., Khodairy, M. M. and Omar, E. M. (2024). Sucrose, glucose, and fructose preference in honeybees and their effects on food digestibility. Apidologie, 55(6): 77.
• Adalina, Y., Mulyati, A. H., Oktasari, D. and Prayoga, P. (2024). Physico-chemical properties of multifloral honey Apis dorsata and monofloral honey of bees Apis mellifera. IOP Conference Series: Earth and Environmental Science, 1315(1): 012065. https://doi.org/10.1088/1755-1315/1315/1/012065
• Alghamdi, B. A., Alshumrani, E. S., Saeed, M. S. B., Rawas, G. M., Alharthi, N. T., Baeshen, M. N., Helmi, N. M., Alam, M. Z. and Suhail, M. (2020). Analysis of sugar composition and pesticides using HPLC and GC–MS techniques in honey samples collected from Saudi Arabian markets. Saudi Journal of Biological Sciences, 27(12): 3720-3726.‏ https://doi.org/10.1016/j.sjbs.2020.08.018
• Aljohar, H. I., Maher, H. M., Albaqami, J., Al-Mehaizie, M., Orfali, R., Orfali, R. and Alrubia, S. (2018). Physical and chemical screening of honey samples available in the Saudi market: An important aspect in the authentication process and quality assessment. Saudi Pharmaceutical Journal, 26(7): 932-942.
• Anklam, E. (1998). A review of the analytical methods to determine the geographical and botanical origin of honey. Food Chemistry, 63(4): 549-562.
• Barker, R. J., and Lehner, Y. (1974). Acceptance and sustenance value of naturally occurring sugars fed to newly emerged adult workers of honey bees (Apis mellifera L.). Journal of Experimental Zoology, 187(2): 277-285.
• Bertelli, D., Lolli, M., Papotti, G., Bortolotti, L., Serra, G. and Plessi, M. (2010). Detection of honey adulteration by sugar syrups using one-dimensional and two-dimensional high-resolution nuclear magnetic resonance. Journal of Agricultural and Food Chemistry, 58(15): 8495-8501.
• Bogdanov, S., Ruoff, K. and Oddo, L. P. (2004). Physico-chemical methods for the characterisation of unifloral honeys: a review. Apidologie, 35(Suppl. 1): 4-17.
• Brodschneider, R., and Crailsheim, K. (2010). Nutrition and health in honey bees. Apidologie, 41(3): 278-294.
• Cavdar, S., Yıldız, O., Şahin, H., Karahalil, F. and Kolaylı, S. (2013). Comparison of physical and biochemical characteristics of different quality of Turkish honey. Ukrainian Bee Journal, 13(2): 55-62.
• Ceksteryte, V. and Racys, J. (2006). The quality of syrups used for bee feeding before winter and their suitability for bee wintering. Journal of Apicultural Science, 50(1): 5-14.‏
• Chefrour, C., Draiaia, R., Tahar, A., and Ait Kaki, Y. (2009). Physicochemical characteristics and pollen spectrum of some north-east Algerian honeys. African Journal of Food, Agriculture, Nutrition and Development, 9(5), 1164–1179. https://www.ajol.info/index.php/ajfand/article/view/45101
• FAO/WHO (2001). Codex Alimentarius: Standard for honey (Codex Stan 12-1981, Rev. 1 (1987), Rev. 2 (2001)). Rome: Food and Agriculture Organization of the United Nations and World Health Organization, Rome, Italy.
• Consonni, R., Cagliani, L. R., and Cogliati, C. (2013). Geographical discrimination of honeys by saccharides analysis. Food Control, 32(2): 543-548.
• Cordella, C., Militão, J. S., Clément, M. C., Drajnudel, P. and Cabrol-Bass, D. (2005). Detection and quantification of honey adulteration via direct incorporation of sugar syrups or bee-feeding: preliminary study using high-performance anion exchange chromatography with pulsed amperometric detection (HPAEC-PAD) and chemometrics. Analytica Chimica Acta, 531(2): 239-248.
• Cotte, J. F., Casabianca, H., Giroud, B., Albert, M., Lheritier, J. and Grenier-Loustalot, M. F. (2004). Characterization of honey amino acid profiles using high-pressure liquid chromatography to control authenticity. Analytical and Bioanalytical Chemistry, 378(5): 1342-1350.
• Dietemann, V., Nazzi, F., Martin, S. J., Anderson, D. L., Locke, B., Delaplane, K. S., Wauquiez, Q., Tannahill, C., Frey, E., Ziegelmann, B., Rosenkranz, P., Ellis, J. D., Hatjina, F., Conte, Y. L., Neumann, P. and Pettis, J. S. (2013). Standard methods for varroa research. Journal of Apicultural Research, 52(1): 1-54. https://doi.org/10.3896/IBRA.1.52.1.09
• Doner, L. W. (1977). The sugars of honey a review. Journal of the Science of Food and Agriculture, 28(5): 443-456. ‏ Egyptian Organization for Standardization and Quality Control (EOS). (2005). Egyptian standard No. 355: Honey and methods of analysis – Part 1: Honey. Cairo, Egypt: Egyptian Organization for Standardization and Quality Control, Egypt.
• El Sohaimy, S. A., Masry, S. H. D. and Shehata, M. G. (2015). Physicochemical characteristics of honey from different origins. Annals of Agricultural Sciences, 60(2): 279-287.
• Elflein, L. and Raezke, K. P. (2008). Improved detection of honey adulteration by measuring differences between 13C/12C stable carbon isotope ratios of protein and sugar compounds with a combination of elemental analyzer - isotope ratio mass spectrometry and liquid chromatography - isotope ratio mass spectrometry ( 13C-EA/LC-IRMS). Apidologie, 39(5): 574-587.
• Farag, R. and Rag, A. F. M. (2020). Sugars profile of citrus (Citrus spp.) honey for quality determination. Egyptian Academic Journal of Biological Sciences. A, Entomology, 13(1): 41-46. ‏ Frizzera, D., Del Fabbro, S., Ortis, G., Zanni, V., Bortolomeazzi, R., Nazzi, F. and Annoscia, D. (2020). Possible side effects of sugar supplementary nutrition on honey bee health. Apidologie, 51: 594-608.
• Geslin, B., Aizen, M. A., Garcia, N., Pereira, A. J., Vaissière, B. E., and Garibaldi, L. A. (2017). The impact of honey bee colony quality on crop yield and farmers’ profit in apples and pears. Agriculture, Ecosystems and Environment, 248: 153-161. ‏ Goodwin, R. M. (1997). Feeding sugar syrup to honey bee colonies to improve pollination: a review. Bee World, 78(2): 56-62.‏
• Guler, A., Kocaokutgen, H., Garipoglu, A. V., Onder, H., Ekinci, D. and Biyik, S. (2014). Detection of adulterated honey produced by honeybee (Apis mellifera L.) colonies fed with different levels of commercial industrial sugar (C3 and C4 plants) syrups by the carbon isotope ratio analysis. Food Chemistry, 155: 155-160. ‏ Haydak, M. H. (1970). Honey bee nutrition. Annual Review of Entomology, 15(1): 143-156.
• Herbert Jr, E. W., Shimanuki, H. and Caron, D. (1977). Optimum protein levels required by honey bees (Hymenoptera, Apidae) to initiate and maintain brood rearing. Apidologie, 8(2): 141-146.
• Hermosı́n, I., Chicon, R. M. and Cabezudo, M. D. (2003). Free amino acid composition and botanical origin of honey. Food chemistry, 83(2): 263-268. ‏ Jeffree, E. P. (1958). A shaped wire grid for estimating quantities of brood and pollen in combs. Bee World, 39(5): 115-118. ‏ Juan-Borrás, M., Domenech, E., Hellebrandova, M. and Escriche, I. (2014). Effect of country origin on physicochemical, sugar and volatile composition of acacia, sunflower and tilia honeys. Food Research International, 60: 86-94. ‏ Kamal, M. M., Rashid, M. H. U., Mondal, S. C., El Taj, H. F. and Jung, C. (2019). Physicochemical and microbiological characteristics of honey obtained through sugar feeding of bees. Journal of Food Science and Technology, 56: 2267-2277.
• Kanelis, D., Liolios, V., Tananaki, C. and Rodopoulou, M. A. (2022). Determination of the carbohydrate profile and invertase activity of adulterated honeys after bee feeding. Applied Sciences, 12(7): 3661.
• Kekeçoğlu, M., Gürcan, E. and Soysal, M. (2007). The Status of Beekeeping for Honey Production in Turkey. Journal of Tekirdag Agricultural Faculty, 4(2): 227-236. (In Turkish)
• Kerkvliet, J. D., Shrestha, M., Tuladhar, K., and Manandhar, H. (1995). Microscopic detection of adulteration of honey with cane sugar and cane sugar products. Apidologie, 26(2): 131-139.
• Kowalski, S., Lukasiewicz, M., Duda-Chodak, A. and Zięć, G. (2013). 5-Hydroxymethyl-2-Furfural (HMF) – Heat-Induced Formation, Occurrence in Food and Biotransformation - a Review. Polish Journal of Food and Nutrition Sciences, 63(4): 207–225. https://doi.org/10.2478/v10222-012-0082-4
• Li, S., Shan, Y., Zhu, X., Zhang, X. and Ling, G. (2012). Detection of honey adulteration by high fructose corn syrup and maltose syrup using Raman spectroscopy. Journal of Food Composition and Analysis, 28(1): 69-74. ‏ Lieux, M. H. (1972). A melissopalynological study of 54 Louisiana (USA) honeys. Review of Palaeobotany and Palynology, 13(2): 95-124.
• Louveaux, J., Maurizio, A. and Vorwohl, G. (1978). International commission for bee botany of IUBS. Methods of melissopalynology. Bee Word, 59(4): 139-57.
• Majtan, J., Bucekova, M., Kafantaris, I., Szweda, P., Hammer, K. and Mossialos, D. (2021). Honey antibacterial activity: A neglected aspect of honey quality assurance as functional food. Trends in Food Science and Technology, 118: 870-886. ‏ Melnichuk, I.A. (1964). Autumn sugar feeding and physiology of bees. Pchelovodstvo, 84: 13-15. (In Russian) Nair, P. K. K. (1960). Palynological investigation of Quaternary (Karewa) in Kashmir. Journal of Scientific and Industrial Research, 19C, 145–154.
• Nicolson, S. W., De Veer, L., Köhler, A. and Pirk, C. W. (2013). Honeybees prefer warmer nectar and less viscous nectar, regardless of sugar concentration. Proceedings of the Royal Society B: Biological Sciences, 280(1767): 20131597.‏
• Nisbet, C., Kazak, F. and Ardalı, Y. (2018). Determination of quality criteria that allow differentiation between honey adulterated with sugar and pure honey. Biological Trace Element Research, 186: 288-293. ‏ Omar, E., Abd-Ella, A. A., Khodairy, M. M., Moosbeckhofer, R., Crailsheim, K., and Brodschneider, R. (2017). Influence of different pollen diets on the development of hypopharyngeal glands and size of acid gland sacs in caged honey bees (Apis mellifera). Apidologie, 48(4): 425-436.
• Omar, E. M. and 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.
• Přidal, A., Musila, J. and Svoboda, J. (2023). Condition and Honey Productivity of Honeybee Colonies Depending on Type of Supplemental Feed for Overwintering. Animals, 13(3): 323.
• Pudasaini, R., Dhital, B. and Chaudhary, S., (2020). Nutritional requirement and its role on honeybee: a review. Journal of Agriculture and Natural Resources, 3(2): 321-334.
• Rana, A. and Singh, G. (2024). Artificial diet supplementation: A review for sustainable approach to boost honeybee health: Dearth period and artificial diet for bee health. Journal of Scientific and Industrial Research, 83(8): 914-933.
• Rodríguez-Flores, M. S., Escuredo, O., Míguez, M. and Seijo, M. C. (2019). Differentiation of oak honeydew and chestnut honeys from the same geographical origin using chemometric methods. Food Chemistry, 297: 124979. ‏ Ruiz-Matute, A. I., Soria, A. C., Martínez-Castro, I., and Sanz, M. L. (2007). A new methodology based on GC-MS to detect honey adulteration with commercial syrups. Journal of Agricultural and Food Chemistry, 55(18): 7264-7269. ‏ Saklani, S., and Kumar, N. (2021). Quality Honey Production, Processing and Various Mechanisms for Detection of Adulteration. In: Honey Ed(s): Bera, M. B. CRC Press.
• She, S., Chen, L., Song, H., Lin, G., Li, Y., Zhou, J. and Liu, C. (2019). Discrimination of geographical origins of Chinese acacia honey using complex 13C/12C, oligosaccharides and polyphenols. Food Chemistry, 272: 580-585. ‏ Siddiqui, A. J., Musharraf, S. G. and Choudhary, M. I. (2017). Application of analytical methods in authentication and adulteration of honey. Food Chemistry, 217: 687-698. ‏ Standifer, L. N. (1980). Honey bee nutrition and supplemental feeding. United States Department of Agriculture Agricultural Handbook, 335, 39–45.
• Taylor, M. A., Robertson, A. W., Biggs, P. J., Richards, K. K., Jones, D. F. and Parkar, S. G. (2019). The effect of carbohydrate sources: Sucrose, invert sugar and components of mānuka honey, on core bacteria in the digestive tract of adult honey bees (Apis mellifera). PLoS One, 14(12): e0225845.
• Tsvetanov, T., and Balkanska, R. (2025). How does invert sugar syrup affect sealed worker brood and colony strength in Roger-Delon hives? Bulgarian Journal of Animal Husbandry / Životnov Dni Nauki, 62(2): 21–26. https://agriacad.eu/ojs/index.php/bjah/article/download/2852/2607
• von der Ohe, W. (1994). Unifloral honeys: chemical conversion and pollen reduction. Grana, 33(4-5), 292-294. White, J. W. and Doner, L. W. (1980). Honey Composition and Properties. Beekeeping in the United States Agriculture Handbook, 335: 82-91.‏ U. S. A.
• Yüzbaşıoğlu, R. (2022). Honey consumption of individuals and reasons for preference zara honey that a local product (Sivas Provincial Center District). Journal of Tekirdag Agricultural Faculty, 19(1): 16-27. (In Turkish)