Morphocytometric Analysis of Phagocytic Cells in the Hemolymph of Clinically Healthy Adult Honey Bees Exposed to Non-Ionizing Electromagnetic Radiation
Keywords:
Apis mellifera, electromagnetic field exposure (EMF), hemocytes, phagocytic cellsAbstract
The aim of this study was to evaluate the effects of non-ionizing electromagnetic fields on immune status by assessing morphocytometric changes in phagocytic cells from the hemolymph of bees involved in the cellular immune response. The analysis also examined the relationship between these changes, the distribution of electromagnetic power density, and the distance from the emission source. The results showed significant variations in radiation power density as a function of distance, with the highest values recorded at intermediate distances, particularly around 300 m, where both elevated levels and pronounced variability were observed. Hemolymph analysis of nurse bees (7–45 days old) collected from apiaries located near sources of non-ionizing electromagnetic radiation revealed a significant decrease in the proportion of phagocytic cell types, namely granulocytes (10%), macrocytes (2%), microcytes (13%), plasmocytes (29%) and spindle-shaped cells (1%), compared with transport stress. The decrease in the proportion of phagocytic cells observed in bees exposed to non-ionizing electromagnetic radiation may be associated with alterations in cellular immune activity, suggesting a possible effect of electromagnetic stress. Statistical analysis further demonstrated significant differences between the experimental and control groups, reflected in a significant increase in the percentages of granulocytes, microcytes, and plasmocytes in the experimental group compared with the control group.
References
Richardson R. T., Ballinger M. N., Qian F., Christman J. W., Johnson R. M. (2018). Morphological and Functional Characterization of Honey Bee, Apis mellifera, Hemocyte Cell Communities Apidologie, 49(3), 397–410. doi: 10.1007/s13592-018-0566-2
Levitt, B. B., Lai, H. C., & Manville, A. M. (2022). Effects of non-ionizing electromagnetic fields on flora and fauna, Part 2 impacts: how species interact with natural and man-made EMF. Reviews on Environmental Health, 37(3), 327-406.
Vilić, M., Žura Žaja, I., Tkalec, M., Tucak, P., Malarić, K., Popara, N., & Gajger, I. T. (2024). Oxidative Stress Response of Honey Bee Colonies (Apis mellifera L.) during Long-Term Exposure at a Frequency of 900 MHz under Field Conditions. Insects, 15(5), 372.
Taric E., Glavinic U., Vejnovic B., et al. (2020). Oxidative Stress, Endoparasite Prevalence and Social Immunity in Bee Colonies Kept Traditionally vs. Those Kept for Commercial Purposes Insects, 11(5), 266. doi: 10.3390/insects11050266Migdał, P.,.
Sapcaliu, A., Pavel, C., Savu, V., Căuia, E., Matei, M., & Rădoi, I. (2010). Biochemical and Cytological Investigations on Haemolymph of Apis Mellifera Carpathica Bee in Stressful Conditions. Bulletin of the University of Agricultural Sciences & Veterinary Medicine Cluj-Napoca. Animal Science & Biotechnologies, 67.
Thielens, A., Greco, M. K., Verloock, L., Martens, L., & Joseph, W. (2020). Radio-frequency electromagnetic field exposure of western honey bees. Scientific reports, 10(1), 461.
Koziorowska, A., Depciuch, J., Białek, J., Woś, I., Kozioł, K., Sadło, S., & Piechowicz, B. (2020). Electromagnetic field of extremely low frequency has an impact on selected chemical components of the honeybee. Polish Journal of Veterinary Sciences, 23(4).
Migdał, P., Plotnik, M., Bieńkowski, P., Berbeć, E., Latarowski, K., Białecka, N., & Murawska, A. (2025). The Influence of an Electromagnetic Field at a Radiofrequency of 900 MHz on the Behavior of a Honey Bee. Agriculture, 15(12), 1266.
Mallinson, V. J., Woodburn, F. A., & O’Reilly, L. J. (2025). Weak anthropogenic electric fields affect honeybee foraging. iScience, 28(6).
Van Steenkiste, D., Raes, H., Jacobs, F. (1988). Hemocytes of adult honey bees (Apis mellifera). Annales de la Société Royale Zoologique de Belgique, 118, 234–235.
Hystad E. M., Salmela H., Amdam G. V., Münch D. (2017). Hemocyte-Mediated Phagocytosis Differs Between Honey Bee (Apis mellifera) Worker Castes. PLoS ONE, 12(9), e0184108. doi: 10.1371/journal.pone.0184108.
Amdam G. V., Aase A. L. T. O., Seehuus S.-C., Kim Fondrk M., Norberg K., Hartfelder K. (2005). Social Reversal of Immunosenescence in Honey Bee Workers. Experimental Gerontology, 40(12), 939–947. doi: 10.1016/j.exger.2005.08.004.
Wilson-Rich N., Dres S. T., Starks P. T. (2008). The Ontogeny of Immunity: Development of Innate Immune Strength in the Honey Bee (Apis mellifera). Journal of Insect Physiology, 54(10–11), 1392–1399.14. Butolo N. P., Azevedo P., Alencar L. D., Malaspina O., Nocelli R. C. F. (2021). Impact of Low Temperatures on the Immune System of Honeybees. Journal of Thermal Biology, 101, 103082. DOI: 10.1016/j.jtherbio.2021.103082.
Migdał, P., Murawska, A., Bieńkowski, P., Strachecka, A., & Roman, A. (2021). Effect of the electric field at 50 Hz and variable intensities on biochemical markers in the honey bee’s hemolymph. Plos one, 16(6), e0252858.
Migdal, P., Bieńkowski, P., Cebrat, M., Berbeć, E., Plotnik, M., Murawska, A., & Latarowski, K. (2023). Exposure to a 900 MHz electromagnetic field induces a response of the honey bee organism on the level of enzyme activity and the expression of stress-related genes. PloS one, 18(5), e0285522.
Migdal, P., Plotnik, M., Bieńkowski, P., Murawska, A., Berbeć, E., Sobkiewicz, P., & Latarowski, K. (2024). Changes in honey bee nutrition after exposure to radiofrequency electromagnetic field. The European Zoological Journal, 91(1), 172-179.
Murawska, A., Migdał, P., Mating, M., Bieńkowski, P., Berbeć, E., & Einspanier, R. (2024). Metabolism gene expression in worker honey bees after exposure to 50Hz electric field-semi-field analysis. Frontiers in Zoology, 21(1), 14.
Shepherd, S., Lima, M. A. P., Oliveira, E. E., Sharkh, S. M., Jackson, C. W., & Newland, P. L. (2018). Extremely low frequency electromagnetic fields impair the cognitive and motor abilities of honey bees. Scientific reports, 8(1), 1-9.
Migdał, P., Berbeć, E., Bieńkowski, P., Plotnik, M., Murawska, A., & Latarowski, K. (2022). Exposure to magnetic fields changes the behavioral pattern in Honeybees (Apis mellifera L.) under laboratory conditions. Animals, 12(7), 855.
Treder, M., Müller, M., Fellner, L., Traynor, K., & Rosenkranz, P. (2023). Defined exposure of honey bee colonies to simulated radiofrequency electromagnetic fields (RF-EMF): Negative effects on the homing ability, but not on brood development or longevity. Science of The Total Environment, 896, 165211.
Molina-Montenegro, M. A., Acuña-Rodríguez, I. S., Ballesteros, G. I., Baldelomar, M., Torres-Díaz, C., Broitman, B. R., & Vázquez, D. P. (2023). Electromagnetic fields disrupt the pollination service by honeybees. Science advances, 9(19), eadh1455.
As, N., Karan, Y., Dizman, S., Sayi, B. C., Kuvanci, A., Cinbirtoğlu, Ş., ... & Şahin, M. E. (2025). An experimental study on the effect of non-ionizing electromagnetic fields on honey bees. Electromagnetic Biology and Medicine, 44(1), 65-78.
OIE - World Organisation for Animal Health, 2008. Terrestrial Code Online Access, 2022 (OIE Manual, ed. 2016; BEE Book ed. 2013).
Wille H., Vecchi Maria A., 1974. Untersuchungen uber die Hamolymphe der Honigbiene (Apis mellifica L.). Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 47, 133-149).
Sapcaliu, A., Pavel, C., Căuia, E., Rădoi, I., Tudor, N., Tudor, P., & Milea, F. (2009). Morpho-cytometric investigations on haemolymph collected from honeybees originated from south of Romania. Bulletin UASVM Animal Science and Biotechnologies, 66 (1-2)/2009. Print ISSN 1843-5262; Electronic ISSN 1843-536X
