The Role Of Viral And Parasitic Factors In Bee Colony Losses İn Iğdır Province

Öz

Colony losses in honey bees; It is caused by many factors such as care and feeding errors, pesticides, bee diseases and pests, global warming and stress. Viral and some parasitic infections, which are among the bee diseases, can cause significant economic losses in bee holdings and, from time to time, colony extinction. In this study, the role of viral and parasitic factors in colony losses observed in honey bee enterprises engaged in beekeeping and making their living from this activity in Iğdır province was investigated. For this purpose, seven viral agents in 64 bee farms with colony loss; Acute bee paralysis virus (ABPV), Chronic bee paralysis virus (CBPV), Black queen cell virus (BQCV), Deformed wing virus (DWV), Sacbrood bee virus (SBV), Cashmere bee virus (KBV), Israel acute bee paralysis virus (IAPV) and two parasitic agents; Examined for Nosema apis/cerana and Varroa. For this purpose, samples of 64 bee farms with colony loss in the spring of 2021 were analyzed. ABPV, BQCV, CBPV, DWV, KBV, SBV and IAPV factors were found to be 1.56%, 76.56%, 4.68%, 50%, 1.56%, 81.25%,20.31%, respectively, in honey bee enterprises with colony loss. Nosema cerana was positive at a rate of 60.93%, and N.apise was not found. In addition, in any of the bee farms with colony loss, Varroa sp. not detected. As a result, it is thought that mixed infections are seen in bee holdings with colony loss and these mixed infections are thought to be effective in colony losses.

Anahtar Kelimeler

• nosemosis
• türkiye
• Igdır
• colony loss
• bee viruses

Iğdır İlinde Görülen Arı Kolonisi Kayıplarında Viral ve Paraziter Etkenlerin Rolü

Öz

Bal arılarında görülen koloni kayıplarında bakım ve beslenme hataları, pestisitler, arı hastalıkları ve zararlıları, küresel ısınma ve stres gibi birçok faktör rol oynamaktadır. Arı hastalıkları arasında yer alan viral ve paraziter enfeksiyonlar arı işletmelerinde önemli ekonomik kayıplara ve zaman zaman da kolonilerin sönmesine neden olabilmektedir. Bu çalışmada, Iğdır ilinde bulunan, koloni kaybı geçmişi olan 64 işletme belirlenmiş, bu işletmeleride görülen koloni kayıplarında viral, paraziter ve mikrosporodial etkenlerin rolü araştırılmıştır. Bu amaçla yedi viral etken; Akut arı felci virusu (Acute Bee Paralysis Virus-ABPV), kronik arı felci virusu (Cronic Bee Paralysis Virus-CBPV), siyah kraliçe hücre virusu (Black Queen Cell Virus-BQCV), deforme kanat virusu (Deforme Wing Virus-DWV), torba çürüklüğü virusu (SacBrood Virus-SBV), Kaşmir arı virusu (Kashmir Bee Virus-KBV), İsrail akut arı felci virusu (Israeli Acute Paralysis Virus-IAPV) ile nosemosis ve varroasis yönünden incelenmiştir. Araştırma sonunda viral etkenlerden ABPV, BQCV, CBPV, DWV, KBV, SBV ve IAPV sırasıyla %1.56, %76.56, %4.68, %50, %1.56, %81.25, %20.31 oranlarında; mikrosporodial hastalıklardan nosemosis % 60.93 oranında bulunmuştur. Nosemosise neden olan etken Nosema ceranae olarak belirlenmiştir. Ayrıca koloni kaybı gözlenen arı işletmelerinin hiçbirinde Varroa sp. tespit edilmemiştir. Sonuç olarak, koloni kaybı gözlenen arı işletmelerinde miks enfeksiyonların görüldüğü ve bu görülen miks enfeksiyonların koloni kayıplarında etkili olabileceği düşünülmektedir.

Anahtar Kelimeler

• Türkiye
• Iğdır
• koloni kaybı
• arı virüsleri
• Nosemosis

Kaynakça

1. Allen, M.F., Ball, B.V. (1996). The incidence and World distribution of honey bee viruses. Bee World. 77: 141–162. Anderson, D. (2005). Triggering virus replication in honey bees, Bee Research And Virus in Europe. In Proceedings of the meeting in Sophia-Antipolis (France) (Vol. 24, p. 26).
2. Anonim, (2022). Hayvansal üretim istatikleri (Erişim Linki: https://www.tuik.gov.tr/, https://data.tuik.gov.tr/Kategori/GetKategori?p=Tarim-111). (Erişim Tarihi: 21.09.2022.
3. Aubert, M., Ball, B., Fries, I., Moritz, R., Milani N, Bernardinelli A. (2008). Virology and the Honey Bee. Belgium ,ISBN 92-79-00:586-3.
4. Aydın S. 2020. Malatya ve Elazığ illerindeki arı viruslerinin RT-PCR yöntemi ile tespiti ve Moleküler karakterizasyonlarının yapılması (MTÖ Üniversitesi).Yüksek lisans tezi(Basılmamış). Erişim adresi: https://tez.yok.gov.tr/UlusalTezMerkezi
5. Aydin, L., Güleğen, E., Çakmak, İ., & Girişgin, A. (2007). The occurrence of Varroa destructor Anderson and Trueman, 2000 on honey bees (Apis mellifera) in Turkey. Turkish Journal of Veterinary & Animal Sciences, 31(3), 189-191.
6. Baker, A., & Schroeder, D. (2008). Occurrence and genetic analysis of picorna-like viruses infecting worker bees of Apis mellifera L. populations in Devon, South West England. Journal of invertebrate pathology, 98(2), 239-242.
7. Balkaya İ, Kaplan H, Güven E, Avcıoğlu H, 2016.(b)Türkiye’de Görülen Bal Arısı (Apis mellifera) Hastalıkları. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, 11(3): 339-347.
8. Balkaya, İ., Kaplan, H., Güven, E., Avcıoğlu, H. (2016)(a). Erzurum yöresi arıcılarının karşılaştıkları bal arısı hastalıkları. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, 11(3), 273-281.

9. Benjeddou, M., Leat, N., Allsopp, M., & 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.
10. Berenyi, O., Bakonyi, T., Derakhshifar, I., Köglberger, H., & Nowotny, N. (2006)(b). Occurrence of six honeybee viruses in diseased Austrian apiaries. Applied and environmental microbiology, 72(4), 2414-2420.
11. Berenyi, O., Bakonyi, T., Derakhshifar, I., Köglberger, H., Topolska, G., Ritter, W., ... & Nowotny, N. (2007)(a). Phylogenetic analysis of deformed wing virus genotypes from diverse geographic origins indicates recent global distribution of the virus. Applied and Environmental Microbiology, 73(11), 3605-3611.
12. Beyazıt, A., Akkoca, N., Eskiizmirliler, S., Albayrak, H., Özan, E., Özden, M., ... & Tunalıgil, S. (2012). Ege Bölgesi illerinde önemli arı hastalıklarının yaygınlığının araştırılması. Hayvan Sağlığı Program Değerlendirme Kitapçığı, 366.
13. Blanchard, P., Schurr, F., Olivier, V., Celle, O., Antùnez, K., Bakonyi, T., ... & Ribière, M. (2009). Phylogenetic analysis of the RNA-dependent RNA polymerase (RdRp) and a predicted structural protein (pSP) of the Chronic bee paralysis virus (CBPV) isolated from various geographic regions. Virus Research, 144(1-2), 334-338.
14. Chemurot, M., De Smet, L., Brunain, M., De Rycke, R., & de Graaf, D. C. (2017). Nosema neumanni n. sp.(Microsporidia, Nosematidae), a new microsporidian parasite of honeybees, Apis mellifera in Uganda. European journal of protistology, 61, 13-19.
15. Chen, Y. P., & Siede, R. (2007). Honey bee viruses. Advances in virus research, 70, 33-80.
16. Chen, Y. P., Pettis, J. S., Collins, A., & Feldlaufer, M. F. (2006). Prevalence and transmission of honeybee viruses. Applied and environmental microbiology, 72(1), 606-611.
17. Chen, Y. P., Pettis, J. S., Corona, M., Chen, W. P., Li, C. J., Spivak, M., ... & Evans, J. D. (2014). Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health. PLoS pathogens, 10(7), e1004261.
18. 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.
19. Çağırgan, A. A., & Yazici, Z. (2021). The prevalence of seven crucial honeybee viruses using multiplex RT-PCR and theirphylogenetic analysis. Turkish Journal of Veterinary & Animal Sciences, 45(1), 44-55.
20. Çağırgan, A. A., Yıldırım, Y., & Usta, A. (2020) (b). Phylogenetic Analysis of Deformed Wing Virus, Black Queen Cell Virus and Acute Bee Paralysis Viruses in Turkish Honeybee Colonies. Medycyna Weterynaryjna,, 76:8: 480-484.
21. Çağırgan, A. A., Yıldırım, Y., & Usta, A. (2020)(a). The investigation of Israil acute bee paralysis virus, sacbrood virus, Kashmir bee virus and chronic bee paralysis virus in honeybees (Apis mellifera). Eurasian Journal of Veterinary Sciences, 36(2), 96-101.
22. Çağirgan, A. A. (2018). Ege bölgesinde virus nedenli arı hastalıklarının multipleks polimeraz zincir reaksiyonu ile araştırılması. Ondokuz Mayıs Üniversitesi Sağlık Bilimleri Enstitüsü Veteriner Viroloji Anabilim Dalı. Doktora Tezi. (Basılmış). (Doktora tezi). Erişim adresi: https://tez.yok.gov.tr/UlusalTezMerkezi
23. Çakmak, İ., Aydın, L., & Güleğen, E. (2003). Güney Marmara Bölgesinde balarısı zararlı ve hastalıkları. Uludağ Arıcılık Dergisi, 3(2), 33-35.
24. De Miranda, J. R., Bailey, L., Ball, B. V., Blanchard, P., Budge, G. E., Chejanovsky, N., ... & Van Der Steen, J. J. (2013). Standard methods for virus research in Apis mellifera. Journal of apicultural research, 52(4), 1-56.
25. De Miranda, J. R., Cordoni, G., & Budge, G. (2010). The acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. Journal of invertebrate pathology, 103, S30-S47.
26. De Miranda, J. R., Drebot, M., Tyler, S., Shen, M., Cameron, C. E., Stoltz, D. B., & Camazine, S. M. (2004). Complete nucleotide sequence of Kashmir bee virus and comparison with acute bee paralysis virus. Journal of General Virology, 85(8), 2263-2270.
27. Di Prisco, G., Pennacchio, F., Caprio, E., Boncristiani Jr, H. F., Evans, J. D., & Chen, Y. (2011). Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. Journal of General Virology, 92(1), 151-155.
28. Doğanay, A., Aydın, L. (2017). Bal Arısı Yetiştiriciliği Ürünleri Hastalıkları. 1. Baskı, Bursa: Dora Yayınevi, s: 21-57, 283-343.
29. Ellis, J. D., & Munn, P. A. (2005). The worldwide health status of honey bees. Bee world, 86(4), 88-101.
30. Formato, G., Giacomelli, A., Olivia, M. A., Aubin, L., Glick, E., Paldi, N., ... & Mutinelli, F. (2011). First detection of Israeli acute paralysis virus (IAPV) in Italy. Journal of apicultural research, 50(2), 176-177.
31. Francis, R. M., Nielsen, S. L., & Kryger, P. (2013). Varroa-virus interaction in collapsing honey bee colonies. PloS one, 8(3), e57540.
32. Francis, R., & Kryger, P. (2012). Single assay detection of acute bee paralysis virus, Kashmir bee virus and Israeli acute paralysis virus. Journal of Apicultural Science, 56(1), 137-146.
33. 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.
34. Gajger, T.I., Kolodziejek, J., Bakonyi, T., & Nowotny, N. (2014). Prevalence and distribution patterns of seven different honeybee viruses in diseased colonies: a case study from Croatia. Apidologie, 45, 701-706.
35. Galbraith, D. A., Fuller, Z. L., Ray, A. M., Brockmann, A., Frazier, M., Gikungu, M. W., ... & Grozinger, C. M. (2018). Investigating the viral ecology of global bee communities with high-throughput metagenomics. Scientific reports, 8(1), 1-11.
36. Garigliany, M., El Agrebi, N., Franssen, M., Hautier, L., & Saegerman, C. (2019). Moku virus detection in honey bees, Belgium, 2018. Transboundary and emerging diseases, 66(1), 43-46.
37. Gauthier, L., Tentcheva, D., Tournaire, M., Dainat, B., Cousserans, F., Colin, M. E., & Bergoin, M. (2007). Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique. Apidologie, 38(5), 426-435.
38. Genersch, E. (2010). Honey bee pathology: current threats to honey bees and beekeeping. Applied microbiology and biotechnology, 87, 87-97.
39. Govan, V. A., Leat, N., Allsopp, M., & Davison, S. (2000). Analysis of the complete genome sequence of acute bee paralysis virus shows that it belongs to the novel group of insect-infecting RNA viruses. Virology, 277(2), 457-463.
40. Gümüşova, O.S., Albayrak, H., Kurt, M., & Yazici, Z. (2010). Prevalence of three honey bee viruses in Turkey. Veterinarski Arhiv, 80(6), 779-785.
41. Gürçay, M., & Kutlu, M. A. Bal Arılarının Önemli Virusları. Uluslararası Gıda Tarım ve Hayvan Bilimleri Dergisi, 2(2), 29-41.
42. Kalaycı, G., Çağırgan, A. A., Pekmez, K., Özkan, B., & Kaplan, M. (2019). Molecular detection and phylogenetic analysis of the honeybee (Apis mellifera) sacbrood virus in Turkey. Turkish Journal of Veterinary & Animal Sciences, 43(4), 551-554.
43. Kalayci, G., Cagirgan, A. A., Kaplan, M., Pekmez, K., Beyazit, A., Ozkan, B., ... & Arslan, F. (2020). The role of viral and parasitic pathogens affected by colony losses in Turkish apiaries. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 26(5).
44. Karapınar, Z., Oğuz, B., Dinçer, E., & Öztürk, C. (2018). Phylogenetic analysis of black queen cell virus and deformed wing virus in honeybee colonies infected by mites in Van, Eastern Turkey. 74 (7): 460-465. Kukielka, Z.D., & Rodríguez, J. M. S. V. (2010). First detection of Israeli acute paralysis virus (IAPV) in Spanish honeybees. Spanish Journal of Agricultural Research, (2), 308-311.
45. Kutlu, M.A., Kaftanoğlu, O. (1990). Ergin bal arısı (Apis mellifera L.) hastalığı Nosema apis’in dağılımı ve enfeksiyon oranı üzerine bir araştırma. Çukurova Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 4(2)41-53 Lanzi, G., De Miranda, J. R., Boniotti, M. B., Cameron, C. E., Lavazza, A., Capucci, L., ... & Rossi, C. (2006). Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.). Journal of virology, 80(10), 4998-5009.
46. Levin, S., Sela, N., Erez, T., Nestel, D., Pettis, J., Neumann, P., & Chejanovsky, N. (2019). New viruses from the ectoparasite mite Varroa destructor infesting Apis mellifera and Apis cerana. Viruses, 11(2), 94.
47. Levitt, A. L., Singh, R., Cox-Foster, D. L., Rajotte, E., Hoover, K., Ostiguy, N., & Holmes, E. C. (2013). Cross-species transmission of honey bee viruses in associated arthropods. Virus research, 176(1-2), 232-240.
48. Li, J., Wang, T., Evans, J. D., Rose, R., Zhao, Y., Li, Z., ... & Chen, Y. (2019). The phylogeny and pathogenesis of sacbrood virus (SBV) infection in European honey bees, Apis mellifera. Viruses, 11(1), 61.
49. Maori, E., Lavi, S., Mozes-Koch, R., Gantman, Y., Peretz, Y., Edelbaum, O., ... & Sela, I. (2007). Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra-and inter-species recombination. Journal of General Virology, 88(12), 3428-3438.
50. Maramorosch, K., Shatkin, A. (2007). Honey bee viruses. Advances in Virus Research. Academic Press. 33-80
51. Meeus, I., de Miranda, J. R., de Graaf, D. C., Wäckers, F., & Smagghe, G. (2014). Effect of oral infection with Kashmir bee virus and Israeli acute paralysis virus on bumblebee (Bombus terrestris) reproductive success. Journal of Invertebrate Pathology, 121, 64-69.
52. Morawetz, L., Köglberger, H., Griesbacher, A., Derakhshifar, I., Crailsheim, K., Brodschneider, R., & Moosbeckhofer, R. (2019). Health status of honey bee colonies (Apis mellifera) and disease-related risk factors for colony losses in Austria. PloS one, 14(7), e0219293.
53. Mullapudi, E., Přidal, A., Pálková, L., de Miranda, J. R., & Plevka, P. (2016). Virion structure of Israeli acute bee paralysis virus. Journal of Virology, 90(18), 8150-8159.
54. Muz, D., & Muz, M. N. (2018). A molecular epidemiological study of black queen cell virus in honeybees (Apis mellifera) of Turkey: the first genetic characterization and phylogenetic analysis of field viruses. Apidologie, 49(1), 89-100.
55. Muz, M. N., Girisgin, A. O., Muz, D., & Aydin, L. (2010). Molecular detection of Nosema ceranae and Nosema apis infections in Turkish apiaries with collapsed colonies. Journal of Apicultural Research, 49(4), 342-342.
56. Nielsen, S. L., Nicolaisen, M., & Kryger, P. (2008). Incidence of acute bee paralysis virus, black queen cell virus, chronic bee paralysis virus, deformed wing virus, Kashmir bee virus and sacbrood virus in honey bees (Apis mellifera) in Denmark. Apidologie, 39(3), 310-314.
57. Oğuz, B., Karapinar, Z., Dincer, E., & DEĞER, M. S. (2017). Molecular detection of Nosema spp. and black queen-cell virusin honeybees in Van Province, Turkey. Turkish Journal of Veterinary & Animal Sciences, 41(2), 221-227.
58. Olivier, V., Massou, I., Celle, O., Blanchard, P., Schurr, F., Ribière, M., & Gauthier, M. (2008). In situ hybridization assays for localization of the chronic bee paralysis virus in the honey bee (Apis mellifera) brain. Journal of virological methods, 153(2), 232-237.
59. Özkırım, A., & Schiesser, A. (2013). Israeli acute paralysis virus (IAPV) in Turkish bees. Journal of Apicultural Research, 52(2), 56-57.
60. Özüiçli, M., & Aydın, L. (2018). Türkiye bal arılarında ciddi tehlike; nosemosis. Uludağ Üniversitesi Veteriner Fakültesi Dergisi, 37(2), 151-157.
61. Palacios, G. U. S. T. A. V. O., Hui, J. E. F. F. E. R. Y., Quan, P. L., Kalkstein, A. B. B. Y., Honkavuori, K. S., Bussetti, A. V., ... & Lipkin, W. I. (2008). Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. Journal of Virology, 82(13), 6209-6217.
62. Ratnieks, F. L., & Carreck, N. L. (2010). Clarity on honey bee collapse?. Science, 327(5962), 152-153.
63. Reddy, K. E., Yoo, M. S., Kim, Y. H., Kim, N. H., Ramya, M., Jung, H. N., ... & Kang, S. W. (2016). Homology differences between complete Sacbrood virus genomes from infected Apis mellifera and Apis cerana honeybees in Korea. Virus Genes, 52, 281-289.
64. Remnant, E. J., Shi, M., Buchmann, G., Blacquière, T., Holmes, E. C., Beekman, M., & Ashe, A. (2017). A diverse range of novel RNA viruses in geographically distinct honey bee populations. Journal of virology, 91(16), e00158-17.
65. Reynaldi, F. J., Sguazza, G. H., Pecoraro, M. R., Tizzano, M. A., & Galosi, C. M. (2010). First report of viral infections that affect argentine honeybees. Environmental Microbiology Reports, 2(6), 749-751.
66. Reynaldi, F. J., Sguazza, G. H., Tizzano, M. A., Fuentealba, N., Galosi, C. M., & Pecoraro, M. R. (2011). First report of Israeli acute paralysis virus in asymptomatic hives of Argentina. Rev Argent Microbiol, 43(2), 84-6.
67. Ribière, M., Lallemand, P., Iscache, A. L., Schurr, F., Celle, O., Blanchard, P., ... & Faucon, J. P. (2007). Spread of infectious chronic bee paralysis virus by honeybee (Apis mellifera L.) feces. Applied and environmental microbiology, 73(23), 7711-7716.
68. Ribière, M., Olivier, V., & Blanchard, P. (2010). Chronic bee paralysis: a disease and a virus like no other?. Journal of invertebrate pathology, 103, S120-S131.
69. Rodríguez, M., Vargas, M., Gerding, M., Navarro, H., & Antúnez, K. (2012). Viral infection and Nosema ceranae in honey bees (Apis mellifera) in Chile. Journal of Apicultural Research, 51(3), 285-287.
70. Rüstemoğlu M, 2015. Hakkari İli Bal Arılarında (Apis Mellifera L.) Görülen Önemli Arı Viruslarının RT-PCR Yöntemi İle Araştırılması Ve Moleküler Karakterizasyonlarının Yapılması. Van Yüzüncü Yıl Üniversitesi Fen Bilimleri Enstitüsü, (Basılmış). (Doktora tezi). Erişim adresi: https://tez.yok.gov.tr/UlusalTezMerkezi
71. Rüstemoğlu, M., & Sipahioğlu, H. M. (2016). Occurrence and molecular characterization of acute bee paralysis virus (ABPV) in honeybee (Apis mellifera) colonies in Hakkari province. Yüzüncü Yıl Üniversitesi Tarım Bilimleri Dergisi. 26(2): 174-182.
72. Sguazza, G. H., Reynaldi, F. J., Galosi, C. M., & Pecoraro, M. R. (2013). Simultaneous detection of bee viruses by multiplex PCR. Journal of Virological Methods, 194(1-2), 102-106.
73. Shen M, Yang X, Cox-Foster D, Cui L, 2005a. The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology, 342(1): 141-149.
74. Shen, M., Cui, L., Ostiguy, N., & Cox-Foster, D. (2005)(b). Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite. Journal of General Virology, 86(8), 2281-2289.
75. Shen, M., Yang, X., Cox-Foster, D., & Cui, L. (2005)(a). The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology, 342(1), 141-149.
76. Simon-Delso, N., San Martin, G., Bruneau, E., Minsart, L. A., Mouret, C., & Hautier, L. (2014). Honeybee colony disorder in crop areas: the role of pesticides and viruses. PloS one, 9(7), e103073.
77. Spurny, R., Přidal, A., Pálková, L., Kiem, H. K. T., de Miranda, J. R., & Plevka, P. (2017). Virion structure of black queen cell virus, a common honeybee pathogen. Journal of virology, 91(6), e02100-16.
78. Stoltz, D., Shen, X. R., Boggis, C., & Sisson, G. (1995). Molecular diagnosis of Kashmir bee virus infection. Journal of apicultural research, 34(3), 153-160.
79. Şimşek, H., Dilgin, N., & Gültekin, İ. (2001). Elazığ ve yöresinde bulunan arı işletmelerinde nosematosisin yaygınlığı. Etlik Veteriner Mikrobiyoloji Dergisi, 12(1-2), 49-52.
80. Tentcheva, D., Gauthier, L., Jouve, S., Canabady-Rochelle, L., Dainat, B., Cousserans, F., ... & Bergoin, M. (2004)(a). Polymerase Chain Reaction detection of deformed wing virus (DWV) in Apis mellifera and Varroa destructor. Apidologie, 35(4), 431-439.
81. Tentcheva, D., Gauthier, L., Zappulla, N., Dainat, B., Cousserans, F., Colin, M. E., & Bergoin, M. (2004)(b). 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.
82. Tozkar, C. Ö., Kence, M., Kence, A., Huang, Q., & Evans, J. D. (2015). Metatranscriptomic analyses of honey bee colonies. Frontiers in genetics, 6, 100.
83. Tuncer, P., & Yeşilbağ, K. (2009). Bal arılarının viral hastalıkları. Uludağ Arıcılık Dergisi, 9(4), 149-161.
84. Usta, A., & Yıldırım, Y. (2020). Bal Arılarının Viral Hastalıkları. Çukurova Tarım ve Gıda Bilimleri Dergisi, 35(1), 57-66.
85. Usta, A., & Yıldırım, Y. (2022). Investigation of deformed wing virus, black queen cell virus and acute bee paralysis virus infections by using reverse transcriptase-polymerase chain reaction (RT-PCR) technique in honey bees. Ankara Üniversitesi Veteriner Fakültesi Dergisi.
86. Uygur, Ş. Ö., & Girişgin, A. O. (2008). Bal arısı hastalık ve zararlıları. Uludağ Arıcılık Dergisi, 8(4), 130-142.
87. Valles, S. M., Chen, Y., Firth, A. E., Guérin, D. M. A., Hashimoto, Y., Herrero, S., ... & Consortium, I. R. (2017). ICTV virus taxonomy profile: Iflaviridae. The Journal of general virology, 98(4), 527.
88. Welch, A., Drummond, F., Tewari, S., Averill, A., & Burand, J. P. (2009). Presence and prevalence of viruses in local and migratory honeybees (Apis mellifera) in Massachusetts. Applied and environmental microbiology, 75(24), 7862-7865.
89. Williams, G. R., Tarpy, D. R., Chauzat, M. P., Cox-Foster, D. L., Delaplane, K. S., Neumann, P., ... & Shutler, D. (2010). Colony collapse disorder in context. Bioessays, 32(10), 845.
90. Yan, X., Liu, X. J., Chen, J. H., Zhang, Y., & Han, R. C. (2009). First detection of Israel acute paralysis virus (IAPV) in Apis mellifera (Hymenoptera: Apidae) in China. Sociobiology, 54(1), 95.
91. Yildirim, Y., Çagirgan, A. A., & Usta, A. (2020). Phylogenetic analysis of sacbrood virus structural polyprotein and non-structural RNA dependent RNA polymerase gene: Differences in Turkish strains. Journal of invertebrate pathology, 176, 107459.