Keywords: N. apis, A. mellifera, microscope, parasite, bee, infection, histology.


Honey bees (Apis mellifera) host a wide range of parasites, some of which are known to cause dramatic colony losses, as reported in recent years. To counter parasite threats, honey bees have an efficient immune system. Because immune responses are predicted to impose significant physiological costs on infected individuals, they are expected to interact with other life traits that ultimately affect the productivity and fitness of the entire bee colony. Here we tested whether the initial onset of infection adversely affects the gut of worker bees, which is quite an organ of all living organisms and affects all major functions, peristalsis, absorption of nutrients, etc. To do this, we artificially infected young worker bees with the worldwide pathogen Nosema apis, which is recognized and destroyed by the honey bee's immune system. We compared their survival and behavior compared to uninfected individuals from the same apiary and even from the same bee colony. The way of life of social hymenoptera insects, like all ants, as well as some bees and wasps, leads to the fact that related individuals live in close proximity to each other within the bee colony, which creates very favorable conditions for parasites to spread and reproduce. It is well known that bees contain a wide range of different parasites, such as viruses, bacteria, fungi, protozoa, as well as arachnids or other insects that can pose a serious threat to bees. Social insects also have individual innate immune systems, and an individual's ability to fight off parasites is central to the survival of the bee colony. These consist of a mechanical response against large parasites (through processes such as encapsulation and melanization) within cells, as well as a humoral response mediated by antimicrobial peptides, proteins, and other cytotoxic compounds. The activation and use of such defense mechanisms is a complex function and is assumed to compromise other life features of the insect. For example, immune activation can reduce the survival of infected worker bees and affect their reproduction by directing their energy reserves to immunity. A trade-off between immunity and other features of the life cycle is also present in mothers. N. apis infections are often phenotypically expressed by dysentery and increased levels of insect hunger, leading to increased honey and sugar consumption. N. apis is generally referred to as a low-virulence parasite, and the parasite's spores are indeed recognized and destroyed by the honey bee's immune system. Despite the fact that now the Nosema microsporidia is spreading practically all over the world to its definitive host, the mechanisms of its influence on the body of bees, the pathogenesis of the causative agent and how bees react are not sufficiently studied. Therefore, it was decided to conduct a broad characterization at the histological level. The study of the tissues of the intestinal epithelium can explain the early mortality of bees when affected by nosemosis. A study of the bee gut, which is an interesting model system for studying insect defense responses.


1. Alaux, C., Brunet, J. L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., ... & Le Conte, Y. (2010). Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environmental microbiology, 12(3), 774-782.
2. Alaux, C., Folschweiller, M., McDonnell, C., Beslay, D., Cousin, M., Dussaubat, C., ... & Le Conte, Y. (2011). Pathological effects of the microsporidium Nosema ceranae on honey bee queen physiology (Apis mellifera). Journal of invertebrate pathology, 106(3), 380-385.
3. Antúnez, K., Martín‐Hernández, R., Prieto, L., Meana, A., Zunino, P., & Higes, M. (2009). Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental microbiology, 11(9), 2284-2290.
4. Buchon, N., Broderick, N. A., Poidevin, M., Pradervand, S., & Lemaitre, B. (2009). Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell host & microbe, 5(2), 200-211.
5. Costa, C., Tanner, G., Lodesani, M., Maistrello, L., & Neumann, P. (2011). Negative correlation between Nosema ceranae spore loads and deformed wing virus infection levels in adult honey bee workers. Journal of Invertebrate Pathology, 108(3), 224-225.
6. Dussaubat, C., Brunet, J. L., Higes, M., Colbourne, J. K., Lopez, J., Choi, J. H., Martín-Hernández, R., Botías, C., Cousin, M., McDonnell, C., Bonnet, M., Belzunces, L. P., Moritz, R. F., Le Conte, Y., & Alaux, C. (2012). Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PloS one, 7(5), e37017.
7. Fenoy, S., Rueda, C., Higes, M., Martín-Hernández, R., & Del Aguila, C. (2009). High-level resistance of Nosema ceranae, a parasite of the honeybee, to temperature and desiccation. Applied and environmental microbiology, 75(21), 6886-6889.
8. Forsgren, E., & Fries, I. (2010). Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Veterinary parasitology, 170(3-4), 212-217.
9. Fries, I. (2010). Nosema ceranae in European honey bees (Apis mellifera). Journal of invertebrate pathology, 103, S. 73-S79.
10. Genersch, E., von Der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Büchler, R., ... & Rosenkranz, P. (2010). The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie, 41(3), 332-352.
11. Gisder, S., Hedtke, K., Möckel, N., Frielitz, M. C., Linde, A., & Genersch, E. (2010). Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Applied and environmental microbiology, 76(9), 3032-3038.
12. Ha, E. M., Lee, K. A., Seo, Y. Y., Kim, S. H., Lim, J. H., Oh, B. H., ... & Lee, W. J. (2009). Coordination of multiple dual oxidase–regulatory pathways in responses to commensal and infectious microbes in Drosophila gut. Nature immunology, 10(9), 949-957.
13. Hges, M., Martín-Hernández, R., & Meana, A. (2010). Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, 41(3), 375-392.
14. Huang, Q., Kryger, P., Le Conte, Y., & Moritz, R. F. (2012). Survival and immune response of drones of a Nosemosis tolerant honey bee strain towards N. ceranae infections. Journal of invertebrate pathology, 109(3), 297-302.
15. Huang, W. F., Bocquet, M., Lee, K. C., Sung, I. H., Jiang, J. H., Chen, Y. W., & Wang, C. H. (2008). The comparison of rDNA spacer regions of Nosema ceranae isolates from different hosts and locations. Journal of invertebrate pathology, 97(1), 9-13.
16. Johnson, R. M., Evans, J. D., Robinson, G. E., & Berenbaum, M. R. (2009). Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proceedings of the National Academy of Sciences, 106(35), 14790-14795.
17. Lallès, J. P. (2010). Intestinal alkaline phosphatase: multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutrition reviews, 68(6), 323-332.
18. Martín-Hernández, R., Botías, C., Barrios, L., Martínez-Salvador, A., Meana, A., Mayack, C., & Higes, M. (2011). Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitology research, 109, 605-612.
19. Martín-Hernández, R., Botías, C., Barrios, L., Martínez-Salvador, A., Meana, A., Mayack, C., & Higes, M. (2011). Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitology research, 109, 605-612.
20. Mayack, C., & Naug, D. (2009). Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. Journal of invertebrate pathology, 100(3), 185-188.
21. Meana, A., Martín-Hernández, R., & Higes, M. (2010). The reliability of spore counts to diagnose Nosema ceranae infections in honey bees. Journal of Apicultural Research, 49(2), 212-214.
22. Paxton, R. J. (2010). Does infection by Nosema ceranae cause “Colony Collapse Disorder” in honey bees (Apis mellifera)?. Journal of Apicultural Research, 49(1), 80-84.
23. Pettis, J. S., Vanengelsdorp, D., Johnson, J., & Dively, G. (2012). Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften, 99, 153-158.
24. Ryu, J. H., Ha, E. M., & Lee, W. J. (2010). Innate immunity and gut–microbe mutualism in Drosophila. Developmental & Comparative Immunology, 34(4), 369-376. 25. Stengel, A., & Taché, Y. (2009). Neuroendocrine control of the gut during stress: corticotropin-releasing factor signaling pathways in the spotlight. Annual review of physiology, 71, 219-239.
26. Vidau, C., Diogon, M., Aufauvre, J., Fontbonne, R., Viguès, B., Brunet, J. L., ... & Delbac, F. (2011). Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PloS one, 6(6), e21550.
27. Wang, P., & Hou, S. X. (2010). Regulation of intestinal stem cells in mammals and Drosophila. Journal of cellular physiology, 222(1), 33-37.
28. Warde-Farley, D., Donaldson, S. L., Comes, O., Zuberi, K., Badrawi, R., Chao, P., ... & Morris, Q. (2010). The Gene- MANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic acids research, 38(suppl_2), W214-W220.
29. Wu, J. Y., Smart, M. D., Anelli, C. M., & Sheppard, W. S. (2012). Honey bees (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection. Journal of invertebrate pathology, 109(3), 326-329.
30. Yaremenko, I. A., Syromyatnikov, M. Y., Radulov, P. S., Belyakova, Y. Y., Fomenkov, D. I., Popov, V. N., & Terent'ev, A. O. (2020). Cyclic Synthetic Peroxides Inhibit Growth of Entomopathogenic Fungus Ascosphaera apis without Toxic Effect on Bumblebees. Molecules (Basel, Switzerland), 25(8), 1954.
How to Cite
KisilD. О., & NazarenkoS. М. (2023). PATHOMORPHOLOGICAL CHANGES IN THE INTESTINE OF BEE AND IMMUNE REACTION TO MICROSPORIDIUM NOSEMA APIS. Bulletin of Sumy National Agrarian University. The Series: Veterinary Medicine, (3(62), 44-49.