A Seasonal Perspective of Nosemosis; the Presence of Nosema spp. in Honeybee Colonies During Summer Months in Ankara, Turkey

Öz

Nosemosis is known as a serious disease of adult honey bees, Apis mellifera L. (Hymenoptera: Apidae) caused by Nosema apis and N. ceranae which are obligate intracellular microsporidian parasites. The parasites infect the epithelial cells of honey bee ventriculum and lead to critical changes in midgut mucosa that cause digestive and metabolic disorders. Accordingly, the infestation causes the death of adult honey bees and leads to great economic losses for beekeeping industry worldwide. Seasonal patterns of nosemosis are consistent and mostly observed in the spring or autumn months, with the highest spore counts and viability. The aim of this work was to evaluate the seasonality of nosemosis in the light of previous literature and specifically investigate the presence of Nosema spp. during the summer season including June, July, and August from various locations in Ankara. Honey bee individuals were collected from 80 apiaries located in 14 different areas in Ankara. The samples were analyzed from pools of ten adult honey bees per population using digestion methods. Before analysis, the anesthesia was induced by cold (30 sec, -80 ℃) on the bees. According to obtained data, 12 out of 80 (15%) sampled apiaries were infected with Nosema spp. spores. Infected apiaries were mainly located in the central and north parts of Ankara. Results show nosemosis might be detrimental to honey bee colonies and its productivity in the summer months. Therefore, the treatment might be needed when infections of Nosema spp. reach to an infectious level even in summer.

Anahtar Kelimeler

• Apis mellifera L.
• Nosema spp.
• Seasonal effect
• Summer
• Ankara

Kaynakça

1. Adl, S. M., Simpson, A. G., Farmer, M. A., Andersen, R. A., Anderson, O. R., Barta, J. R., ... & Taylor, M. F. (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology, 52(5), 399-451.
2. Aydin, L., Gulegen, E., & Cetinbas H. (2001). Prevalence of Nosema apis in Southern Marmara Region in Turkey. Proceeding of 37th Apimondia Congress, Durban, South-Africa. 363-378. ISBN: 0-620-27768-8.
3. Basar, E. (1990). Ülkemizdeki bal arılarında(Apis mellifera) Acarapis woodi ve Nosema apis parazitlerinin araştırılması. (Publication No. 8505). [Master Thesis, Hacettepe University]. https://tez.yok.gov.tr/UlusalTezMerkezi/tezDetay.jsp?id=ayfNPbohfu9KEy40W1Nk4w&no=ayfNPbohfu9KEy40W1Nk4w.
4. Brenna, E., Traver, B. E., Matthew, R., Williams, M. R., Richard, D., & Fell, R. D. (2012). “Comparison of with inHive Sampling and Seasonal Activity of Nosema ceranae in Honey Bee Colonies.” Journal of Invertebrate Pathology, 109(2), 187-93.
5. Ceylan, A., Özgenç, Ö., Erhan, F., Sevin, S., & Yarsan, E. (2019). Nosemosis’ in (Nosematosis) bal arısı (Apis mellifera) midesine etkileri üzerine histokimyasal gözlemler. Veteriner Hekimler Derneği Dergisi, 91(2), 98-103.
6. Cox-Foster, D. L., Conlan, S., Holmes, E. C., Palacios, G., Evans, J. D., Moran, N. A., ... & Lipkin, W. I. (2007). A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318(5848), 283-287.
7. Fries, I., Feng, F., da Silva, A., Slemenda, S. B., & Pieniazek, N. J. (1996). Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). European Journal of Protistology, 32(3), 356-365.
8. Fries, I., Martin, R., Meana, A., García-Palencia, P., & Higes, M. (2006). Natural infections of Nosema ceranae in European honey bees. Journal of Apicultural Research, 45(4), 230-233.

9. 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.
10. Güzerin, E. (2013). Investigation of Honey Bees (Apis mellifera L. ) in Artvin Region in Terms of Microbial and Parasitic Diseases. [Master Thesis, Hacettepe University]. http://www.openaccess.hacettepe.edu.tr:8080/xmlui/handle/11655/2020?show=full.
11. Higes, M., Martín, R., & Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of invertebrate pathology, 92(2), 93-95.
12. Higes, M., Martín‐Hernández, R., Botías, C., Bailón, E. G., González‐Porto, A. V., Barrios, L., ... & Meana, A. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental microbiology, 10(10), 2659-2669.
13. Higes, M., Juarranz, Á., Dias‐Almeida, J., Lucena, S., Botías, C., Meana, A., ... & Martín‐Hernández, R. (2013a). Apoptosis in the pathogenesis of Nosema ceranae (M icrosporidia:Nosematidae) in honey bees (Apis mellifera). Environmental microbiology reports, 5(4), 530-536.
14. Higes, M., Meana, A., Bartolomé, C., Botías, C., & Martín‐Hernández, R. (2013b). Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environmental microbiology reports, 5(1), 17-29.
15. Kurze, C., Le Conte, Y., Kryger, P., Lewkowski, O., Müller, T., & Moritz, R. F. (2018). Infection dynamics of Nosema ceranae in honey bee midgut and host cell apoptosis. Journal of invertebrate pathology, 154, 1-4.
16. Kutlu, M. A., & Kaftanoğlu, O. (1990). A study on the distribution and infection rate of adult honey bee (Apis mellifera L.) disease Nosema apis. Çukurova University Journal of Science Institute, 4(2), 41-53.
17. Martín-Hernández, R., Meana, A., García-Palencıa, P.,Marín, P., Botías, C., Garrıdo-Baılón, E., ... & Higes, M. (2009). Effect of temperature on the biotic potential of honeybee microsporidia. Applied and Environmental Microbiology, 75(8), 2554-2557.
18. Martín-Hernández, R., Higes, M., Sagastume, S., Juarranz, Á., Dias-Almeida, J., Budge, G. E., ... & Boonham, N. (2017). Microsporidia infection impacts the host cell's cycle and reduces host cell apoptosis. PLoS One, 12(2), e0170183.
19. Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A. M., Garrido-Bailón, E., & Higes, M. (2007). Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and environmental microbiology, 73(20), 6331-6338.
20. Muz, M. N., Solmaz, H., Yaman, M., & Karakavuk, M. (2012). Kış salkımı erken bozulan arı kolonilerinde paraziter ve bakteriyel patojenler. The Journal of the Faculty of Veterinary Medicine University of Yuzuncu Yıl, 23(3), 147-150.
21. Özkırım, A., Schiesser, A., & Keskin, N. (2019). Dynamics of Nosema apis and Nosema ceranae co-infection seasonally in honey bee (Apis mellifera L.) colonies. Journal of Apicultural Science, 63(1), 41-48.
22. Terrestrial Manual of the OIE. (2018). Nosemosis of honey bees, Chapter 3.2.4, pp. 744-49. Paris, France.
23. Pernal, S., Ibrahim, A., & Melathopoulos, A. P. (2010). Integrated management of Nosema and detection of antibiotic residues. Hivelights, 23, 12-18.
24. Smith, M. L. (2012). The honey bee parasite Nosema ceranae: transmissible via food exchange?. PLoS One, 7(8), e43319.
25. Tosun, O., Bekircan, Ç., & Yıldırım, H. B. (2019). The presence and distribution of Nosemosis Disease in Turkey. Journal of Apitherapy and Nature, 2(2), 71-84.
26. Tosun, O., & Yaman, M. (2016). The Effects of Temperature and humidity around the beehives on the distribution of Nosema ceranae, and also geographical and seasonal activity of the infection in the Eastern Black Sea Region of Turkey. Mellifera, 6, 7.
27. Traver, B. E., & Fell, R. D. (2011). Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia. Journal of Invertebrate Pathology, 107(1), 43-49.
28. Tutkun E., & İnci A. (1992). Honeybee pests, diseases and treatment methods (From Diagnosis to Treatment). Demircioglu Printing, Ankara.
29. Tutun, H., Sevin, S., & Cetintav, B. (2020). Effects of different chilling procedures on honey bees (Apis mellifera) for anesthesia. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 67(3), 289-294.
30. Utuk, A. E., Piskin, F. C., Girisgin, A. O., Selcuk, O., & Aydin, L. (2016). Microscopic and molecular detection of Nosema spp. in honeybees of Turkey. Apidologie, 47(2), 267-271.
31. Zander, E. (1909). Tierische Parasiten als Krankheitserreger bei der Biene. MunchenerBienenzeitung, 31, 196–204