Sivas İli Örneklerinde Bal Arısı Hastalıkları ve Parazitlerin Yaygınlığının Belirlenmesi

Year 2024, Volume: 21 Issue: 5, 1148 - 1160

Arif Bozdeveci , Rahşan Koç Akpınar , Şengül Alpay Karaoğlu

https://doi.org/10.33462/jotaf.1419608

Abstract

Bal arıları, Apis mellifera L. (Hymenoptera: Apidae), doğal ortamdaki tarım ürünleri ve bitkilerin en önemli tozlayıcılarıdır. Bal arıları doğadaki ve tarımsal üretimdeki bu rolleri nedeniyle ekosistemin önemli bir bileşenidir. Arı çiftliklerinde bakteriyel, fungal, viral ve paraziter faktörler bal arısı koloni kayıplarının en önemli nedenleri arasında yer almaktadır. Bal arısı hastalıkları (bakteriyel, fungal ve viral) ve parazitleri Türkiye'de arıcılığın gelişmesini ve üretim verimliliğini sınırlayan en önemli faktörler arasında yer almaktadır. Bakteriyel ve fungal etkenlerin neden olduğu hastalıkların yanı sıra viral etkenlerin neden olduğu hastalıklar da oldukça çeşitlidir. Virüsler, özellikle de karışık enfeksiyonlar koloni kayıplarına neden olur ve bal arısı kolonilerinin azalmasındaki en önemli faktörlerdir. Bu çalışmada Sivas ilinde koloni kayıpları olan şüpheli örneklerde bal arısı patojenlerinin (Nosema ceranae, Varroa destructor, Paenibacillus larvae ve dokuz virüs) varlığı ve yaygınlığı araştırılmıştır. Bu amaçla larva ve ergin arılarda mikroskobik, mikrobiyolojik ve moleküler yöntemlerle araştırmalar yapılmıştır. Sonuçlar Sivas ilinden alınan örneklerde en sık görülen viral patojenlerin sırasıyla Deformed Wing Virus (%70), Apis mellifera filamentous virus (%60), Black Queen Cell Virus (%60), Sacbrood Virus (%55) ve Varroa destructor virus-1 (%40) olduğunu göstermiştir. Bazı örneklerde viral etkenlerin ikili (%17.5), üçlü (%30), dörtlü (%22.5) ve hatta beşli (%17.5) birlikteliği olduğu görülmüştür. Viral enfeksiyon/varroa birlikteliği oranı %50 olarak belirlenmiştir. İncelenen örneklerde Nosema spor varlığı %22.5, P. larvae pozitiflik oranı ise %12.5 olduğu belirlenmiştir. Arı hastalıkları dağılımının ortaya çıkarılması arıcılara hastalıklarla mücadele ve önlem alma konusunda yardımcı olacaktır. Bu çalışma ile Türkiye'nin Sivas ilinde ilk kez AmFV ve Varroa destructor-1 virüsünün varlığını gösterilmiştir.

Keywords

Apis mellifera L., Bal arısı patojenleri, Virus, Varroa destructor, Sivas

Ethical Statement

Bu çalışma için etik kuruldan izin alınmasına gerek yoktur.

Supporting Institution

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Thanks

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Determination of The Prevalence of Honey Bee Diseases and Parasites in Samples from Sivas Province

Abstract

Honey bees, Apis mellifera L. (Hymenoptera: Apidae), are the most important pollinators of agricultural products and plants in the natural environment. Honeybees are an important ecosystem component due to their role in nature and agricultural production. Bacterial, fungal, viral, and parasitic factors in bee farms are among the most important causes of honey bee colony losses. Honey bee diseases (bacterial, fungal and viral) and parasites are among the most important factors limiting beekeeping development and production efficiency in Türkiye. In addition to diseases caused by bacterial and fungal agents, diseases caused by viral agents are very diverse. Viruses, especially mixed infections, cause colony losses and are the most important factors in the decline of honey bee colonies. In this study the presence and prevalence of honey bee pathogens (Varroa destructor, Nosema ceranae, Paenibacillus larvae, and nine viruses) in suspicious samples with colony losses were investigated in Sivas province. For this purpose, microscopic, microbiological, and molecular methods were investigated on larvae and adult bee. The results showed that the most common viral pathogens in samples from Sivas province were Deformed Wing Virus (70%), Apis mellifera Filamentous Virus (60%), Black Queen Cell Virus (60%), Sacbrood Virus (55%) and Varroa destructor virus-1 (40%), respectively. In some samples, it was observed that there was a double (17.5%), triple (30%), quadruple (22.5%), or even quintuple (17.5%) association of viral agents. The viral infection/varroa coexistence rate was determined to be 50%. It was determined that 22.5% of the samples examined contained Nosema spores, while 12.5% were positive for P. larvae. Revealing the distribution of bee diseases will help beekeepers in disease-fighting and taking measures. This study showed the presence of the AmFV and the Varroa destructor virüs-1 in the Sivas province of Türkiye for the first time.

Keywords

Apis mellifera L., Honey bee pathogens, Virus, Varroa destructor, Sivas

Ethical Statement

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

Supporting Institution

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Thanks

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References

• Akpınar, R., Bozdeveci, A. and Çelik, S. (2023). Diagnosis of American Foulbrood in honey bees and honeycomb in the Central and Eastern Black Sea region. Fırat University Veterinary Journal of Health Sciences, 37(3): 245-250.
• Anjum, S. I, Shah, A. H, Azim, M. K., Yousuf, M. J, Khan, S. and Khan, S. N. (2015). Prevalence of American Foulbrood disease of honeybee in North-West Pakistan. Biotechnology & Biotechnological Equipment, 29(4): 659-665.
• Avcı, O., Oz, M. E. and Dogan M. (2022). Silent threat in honey bee colonies: infection dynamics and molecular epidemiological assessment of black queen cell virus in Turkey. Archives of Virology, 167: 1499–1508.
• Aydın, S. and Oksal, H. (2023). Prevalence and molecular characterization of deformed wing, acute bee paralysis and black queen cell viruses ınfecting honey bees and varroa mites. Journal of Apicultural Science, 67(1):73-86.
• Bailey, L. (1982). Viruses of honeybees. Bee World, 63(4): 165-173.
• Beaurepaire, A., Piot, N., Doublet, V., Antunez, K., Campbell, E., Chantawannakul, P., Chejanovsky, N., Gajda, A., Heerman, M., Panziera, D., Smagghe, G., Yañez, O., de Miranda, J. R. and Dalmon, A. (2020). Diversity and global distribution of viruses of the western honey bee. Apis mellifera. Insects, 11(4): 239. https://doi.org/10.3390/insects11040239
• Benjeddou, M., Leat, N., Allsopp, M. and Davison, S. (2001). Detection of Acute Bee Paralysis Virus and Black Queen Cell Virus from honeybees by reverse transcriptase PCR. Applied and Environmental Microbiology, 67(5): 2384–2387.
• Bordin, F., Zulian, L., Granato, A., Caldon, M., Colamonico, R., Toson, M., Trevisan, L., Biasion, L. and Mutinelli, F. (2022). Presence of known and emerging honey bee pathogens in apiaries of Veneto Region (Northeast of Italy) during Spring 2020 and 2021. Applied Science, 12(4):2134.
• Çağırgan, A. and Yazıcı, Z. (2021). The prevalance of seven crucial honeybee virüses using Multiplex RT-PCR and their phylogenetic analysis, Turkish Journal of Veterinary & Animal Sciences, 45(1): 44-55.
• Chen, Y. P., Pettis, J. S., Collins, A. and Feldlaufer, M. F. (2006). Prevalence and transmission of honeybee viruses. Applied and Environmental Microbiology, 72(1): 606-611.
• Chioveanu, G., Ionescu, D. and Mardare, A. (2004). Control of Nosemosis-treatment with Protofil. Apiacta, 39:31–38.
• D'Alvise, P., Seeburger, V., Gihring, K., Kieboom, M. and Hasselmann, M. (2019). Seasonal dynamics and co-occurrence patterns of honey bee pathogens revealed by high-throughput RT-qPCR analysis. Ecology and Evolution, 9(18): 10241–10252.
• Doğanay, A. and Aydın, L. (2017). Honey Bee, Breeding, Products, Health. 1st edition. Bursa Dora Yayınevi, Bursa, Türkiye.
• Gajger, I., Kolodziejek, J., Bakonyi, T. and Nowotny, N. (2014). Prevalence and distribution patterns of seven different honeybee viruses in diseased colonies: a case study from Croatia. Apidologie, 45: 701-706.
• Gauthier, L., Ravallec, M., Tournaire, M., Cousserans, F., Bergoin, M., Dainat, B. and de Miranda, J. R. (2011). Viruses associated with ovarian degeneration in Apis mellifera L. queens. PLoS ONE, 6: e0016217.
• Gauthier, L., Cornman, S., Hartmann, U., Cousserans, F., Evans, J. D., de Miranda, J. R. and Neumann, P. (2015). The Apis mellifera Filamentous Virus Genome. Viruses, 7(7): 3798–3815. https://doi.org/10.3390/v7072798
• Gebremedhn, H., Deboutte, W., Schoonvaere, K., Demaeght, P., De Smet, L., Amssalu, B., Matthijnssens, J. and de Graaf, D. C. (2020). Metagenomic approach with the NetoVIR enrichment protocol reveals virus diversity within Ethiopian honey bees (Apis mellifera simensis). Viruses, 12: 1218.
• Grupe, A. C II. and Quandt C.A. (2020). A growing pandemic: A review of Nosema parasites in globally distributed domesticated and native bees. PLOS Pathogens, 16(6): e1008580. https://doi.org/10.1371/journal.ppat.1008580
• Güller, A. and Kurt, Z. (2022). Occurrence and molecular phylogeny of economically relevant viruses infecting honey bees (Apis mellifera L.) of Bingöl Province, Turkey. Journal of Apicultural Science, 66(1): 85-96.
• Gümüşova, S., Albayrak, H., Yazıcı, Z. and Kurt, M. (2010). Prevalence of three honey bee viruses in Turkey. Veterinarski Arhiv, 80(6): 779-785.
• Hartmann, U., Forsgren, E., Charrière, J. D., Neumann, P. and Gauthier L. (2015). Dynamics of Apis mellifera Filamentous Virus (AmFV) infections in honey bees and relationships with other parasites. Viruses, 7: 2654–2667.
• Hou, C., Li, B., Deng, S., Chu, Y. and Diao, Q. (2017). Diagnosis and distribution of the Apis mellifera Filamentous Virus (AmFV) in honey bees (Apis mellifera) in China. Insectes Sociaux, 64(4): 597–603.
• Karapinar, Z., Oğuz, B., Dincer, E. and Ozturk, C. (2018). Phylogenetic analysis of black queen cell virus and deformed wing virus in honeybee colonies infected by mites in Van, Eastern Turkey. Medycyna Weterynaryjna, 74(7): 460-465.
• Kartal, S., İvgin Tunca, R., Özgül, O., Karabağ, K. and Koç, H. (2021). Microscopic and molecular detection of Nosema sp. in the Southwest Aegean Region. Uludag Bee Journal, 21(1): 8-20.
• Koç, H., Ergün, A. and Kartal, F. (2020). Problems and solution suggestions of honey producers in Sivas province. Journal of International Social Science Education, 6(2): 327-362.
• Köseman, A., Şeker, İ., Karlıdağ, S. and Aygen, S. (2017). Beekeeping Activities II: The evaluaton of beekeeping activities in terms of beekeeper preferences, production quality and bee diseases in Malatya. Journal of Tekirdag Agricultural Faculty, 14(2):54-63.
• Mayack, C. and Hakanoğlu, H. (2022). Honey Bee pathogen prevalence and interactions within the Marmara region of Turkey. Veterinary Sciences, 9(10): 573.
• Molineri, A. I., Pacini, A., Giacobino, A., Bulacio-Cagnolo, N., Aignasse, A., Zago, L., Fondevila, N., Ferrufino, C., Merke, J., Orellano, E., Bertozzi, E., Pietronave, H. and Signorini, M. L. (2017). Prevalence of honey bee (Apis mellifera) viruses in temperate and subtropical regions from Argentina. Revista Argentina de Microbiología 49(2): 166-173.
• Nanetti, A., Bortolotti, L. and Cilia, G. (2021). Pathogens spillover from honey bees to other Arthropods. Pathogens, 10(8): 1044. https://doi.org/10.3390/pathogens10081044
• OIE (2018). Manual of diagnostic tests and vaccines for terrestrial animals. Chapter 3.2.2. American foulbrood of honey bees (infection of honey bees with Paenibacillus larvae: 719-735.
• OIE (2021). Manual of Standards for Diagnostic Tests and Vaccines for Terrestrial Animals, Chapter 3.2.7. Varroosis of honey bees (infestation of honey bees with Varroa spp.), (version adapted in 2021): 1-14.
• Oliver, R. (2020). Refining the mite wash: Part 3 dislodgement, precipitation, and separation. American Bee Journal, 160: 1013.
• Özgör, E., Güzerin, E. and Keskin, N. (2015). Determination and comparison of Nosema apis and Nosema ceranae in terms of geographic and climatic factors. Hacettepe Journal of Biology and Chemistry, 43(1): 9-15.
• Palacios, G., Hui, J., Quan, P. L., Kalkstein, A., Honkavuori, K. S., Bussetti, A. V., Conlan, S., Evans, J., Chen, Y. P., vanEngelsdorp, D., Efrat, H., Pettis, J., Cox-Foster, D., Holmes, E. C., Briese, T. and Lipkin, W.I. (2008). Genetic analysis of Israel Acute Paralysis Virus: distinct clusters are circulating in the United States. Journal of Virology, 82 (13): 620917.
• Paxton, R. J., Schäfer, M. O., Nazzi, F., Zanni, V., Annoscia, D., Marroni, F., Bigot, D., Laws-Quinn, E. R., Panziera, D., Jenkins, C. and Shafiey, H. (2022). Epidemiology of a major honey bee pathogen, deformed wing virus: potential worldwide replacement of genotype A by genotype B. International Journal for Parasitology: Parasites and Wildlife 18: 157–171. https://doi.org/10.1016/j.ijppaw.2022.04.013
• Pernal, S. F. and Clay, H. (2013). American foulbrood. Honey Bee Diseases and Pests. 3rd ed. Beaverlodge, Alberta, Canada: Canadian Association of Professional Apiculturists; 5-10.
• Quintana, S., Brasesco, C., Porrini, L. P., Di Gerónimo, V., Eguaras, M. J. and Maggi, M. (2021). First molecular detection of Apis mellifera filamentous virus (AmFV) in honey bees (Apis mellifera) in Argentina. Journal of Apicultural Research, 60(1):111-114.
• Ryabov, E. V., Childers, A. K., Chen, Y., Madella, S., Nessa, A., van Engelsdorp, D. and Evans, J. (2017). Recent spread of Varroa destructor virus-1, a honey bee pathogen, in the United States. Scientific Reports, 7(1): 17447. https://doi.org/10.1038/s41598-017-17802-3
• Salkova, D. and Gurgulova, K. (2022). Detection of Varroa destructor mite and Nosema spp. in bee samples from Bulgaria Bee Studies, 14 (1): 21-26.
• Sguazza, G. H., Reynaldi, F. J., Galosi, C. M. and Pecoraro, M.R. (2013). Simultaneous detection of bee viruses by multiplex PCR. Journal of Virological Methods, 194(1-2): 102–106. https://doi.org/10.1016/j.jviromet.2013.08.003
• Şık, Z., Atıcı, E.G., Altıntaş, Ö., Elitok, Y. and Şen, S. (2022). Frequency of American Foulbrood in honeybees: 2015-2020 Data of the Veterinary Control Central Research Institute in Turkey. Etlik Veteriner Mikrobiyoloji Dergisi, 33(2):15-20.
• Steinhauer, N., Kulhanek, K., Antúnez, K., Human, H., Chantawannakul, P. and Chauzat, M. P. (2018). Drivers of colony losses. Current Opinion in Insect Science, 26: 142–148.
• Stoltz, D., Shen, X. R., Boggis, C. and Sisson, G. (1995). Molecular diagnosis of Kashmir bee virus infection. Journal of Apicultural Research, 34(3): 153-160.
• Tel, O. Y., Ötkün, S., Güllü Yücetepe, A. G., Gürbilek, S. E. and Keskin, O. (2021). Molecular identification of nosemosis agents in honeybees found in Siirt and Sanliurfa. Turkish Journal of Agricultural and Natural Sciences, 8(4): 995-1000.
• Tentcheva, D., Gauthier, L., Zappulla, N., Dainat, B., Cousserans, F., Colin, M. E. and Bergoin, M. (2004). Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Applied and Environmental Microbiology, 70(12): 7185-7191.
• Tozkar, C. Ö., Kence, M., Kence, A., Huang, Q. and Evans, J. D. (2015). Metatranscriptomic analyses of honey bee colonies. Frontiers in Genetics, 19(6): 100. https://doi.org/10.3389/fgene.2015.00100
• Usta, A. and Yildirim, Y. (2022). Investigation of deformed wing virus, black queen cell virus, and acute bee paralysis virus infections in honey bees using reverse transcriptase-polymerase chain reaction (RT-PCR) method. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 69(3): 303-311.
• Yaman, M., Yarılgaç, Ş., Güner, B. G. and Ertürk, Ö. (2015). Presence of nosemosis in honeybees (Apis mellifera) in Ordu province. Turkish Journal of Parasitology, 39: 47-51.
• Yañez, O., Piot, N., Dalmon, A., de Miranda, J. R., Chantawannakul, P., Panziera, D., Amiri, E., Smagghe, G., Schroeder, D. and Chejanovsky, N. (2020). Bee Viruses: Routes of infection in Hymenoptera. Frontiers in Microbiology, 11: 943. https://doi.org/10.3389/fmicb.2020.00943
• Yang, D., Wang, J., Wang, X., Deng, F., Diao, Q., Wang, M., Hu, Z. and Hou, C. (2022). Genomics and proteomics of Apis mellifera filamentous virus isolated from honeybees in China. Virologica Sinica, 37(4): 483–490. https://doi.org/10.1016/j.virs.2022.02.007
• Yilmaz, F., Öztürk, S., Kuvanci, A., Kayaboynu, Ü., Karataş, Ü., Kaya, S., Derebaşi, E. and Buldağ, M. (2018). Epidemiology of Nosema apis and Nosema ceranae in Eastern Black Sea Region. Bee Studies, 10(2): 34-44.
• Yüzbaşioğlu, 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. https://doi.org/10.33462/jotaf.863430