Occurrence and Molecular Phylogeny of Economically Relevant Viruses Infecting Honey Bees (Apis mellifera L.) of Bingöl Province, Turkey

Abou-Kubaa, R., Molinatto, G., Khaled, B.S., Daher-Hjaij, N., Heinoun, K., Saponari, M. (2018). First detection of black queen cell virus, Varroa destructor macula-like virus, Apis mellifera filamentous virus and Nosema ceranae in Syrian honey bees Apis mellifera syriaca. Bulletin of Insectology, 71(2), 217–224. Abou-KubaaR. MolinattoG. KhaledB.S. Daher-HjaijN. HeinounK. SaponariM. 2018 First detection of black queen cell virus, Varroa destructor macula-like virus, Apis mellifera filamentous virus and Nosema ceranae in Syrian honey bees Apis mellifera syriaca Bulletin of Insectology 71 2 217 224 Search in Google Scholar

Anderson, D.L. (1984). A comparison of serological techniques for detecting and identifying honeybee viruses. Journal Invertebrate Pathology, 44, 233–243. https://doi.org/10.1016/0022-2011(84)90019-3 AndersonD.L. 1984 A comparison of serological techniques for detecting and identifying honeybee viruses Journal Invertebrate Pathology 44 233 243 https://doi.org/10.1016/0022-2011(84)90019-3 10.1016/0022-2011(84)90019-3 Search in Google Scholar

Antunez, K., Anido M., Garrido-Bailon, E., Botias, C., Zunino, P., Martínez-Salvador, A.,…Higes, M. (2012). Low prevalence of honeybee viruses in Spain during 2006 and 2007. Research in Veterinary Science, 93, 1441–1445. https://doi.org/10.1016/j.rvsc.2012.03.006 AntunezK. AnidoM. Garrido-BailonE. BotiasC. ZuninoP. Martínez-SalvadorA. HigesM. 2012 Low prevalence of honeybee viruses in Spain during 2006 and 2007 Research in Veterinary Science 93 1441 1445 https://doi.org/10.1016/j.rvsc.2012.03.006 10.1016/j.rvsc.2012.03.006 Search in Google Scholar

Avalos, J., Rosero, H., Maldonado, G., Reynaldi, F.J. (2019). Honey bee louse (Braula schmitzi) as a honey bee virus vector. Journal Apicultural Research, 58(3), 427–429. https://doi.org/10.1080/00218839.2019.1565726 AvalosJ. RoseroH. MaldonadoG. ReynaldiF.J. 2019 Honey bee louse (Braula schmitzi) as a honey bee virus vector Journal Apicultural Research 58 3 427 429 https://doi.org/10.1080/00218839.2019.1565726 10.1080/00218839.2019.1565726 Search in Google Scholar

Bacandritsos, N., Granato, A., Budge, G., Papanastasiou, I., Roinioti, E., Caldon, M.,… Mutinelli, F. (2010). Sudden deaths and colony population decline in Greek honey bee colonies. Journal of Invertebrate Pathology, 105, 335–340. https://doi.org/10.1016/j.jip.2010.08.004 BacandritsosN. GranatoA. BudgeG. PapanastasiouI. RoiniotiE. CaldonM. MutinelliF. 2010 Sudden deaths and colony population decline in Greek honey bee colonies Journal of Invertebrate Pathology 105 335 340 https://doi.org/10.1016/j.jip.2010.08.004 10.1016/j.jip.2010.08.004 Search in Google Scholar

Bailey, L., Gibbs, A.J., Woods, R.D. (1964). Sacbrood virus of the larval honeybee (Apis mellifera L.). Virology, 23, 425–429. https://doi.org/10.1016/0042-6822(64)90266-1 BaileyL. GibbsA.J. WoodsR.D. 1964 Sacbrood virus of the larval honeybee (Apis mellifera L.) Virology 23 425 429 https://doi.org/10.1016/0042-6822(64)90266-1 10.1016/0042-6822(64)90266-1 Search in Google Scholar

Bailey, L., & Woods, R.D. (1977). Two more small RNA viruses from honey bees and further observations on sacbrood and acute bee paralysis viruses. Journal of General Virology, 37, 175–182. https://doi.org/10.1099/0022-1317-37-1-175 BaileyL. WoodsR.D. 1977 Two more small RNA viruses from honey bees and further observations on sacbrood and acute bee paralysis viruses Journal of General Virology 37 175 182 https://doi.org/10.1099/0022-1317-37-1-175 10.1099/0022-1317-37-1-175 Search in Google Scholar

Baker, A.C., & Schroeder, D.C. (2008). Occurrence and genetic analysis of picorna-like viruses infecting worker bees of Apis mellifera L. populations in Devon, South West England. Journal Invertebrate Pathology, 98, 239–242. https://doi.org/10.1016/j.jip.2008.02.010 BakerA.C. SchroederD.C. 2008 Occurrence and genetic analysis of picorna-like viruses infecting worker bees of Apis mellifera L. populations in Devon, South West England Journal Invertebrate Pathology 98 239 242 https://doi.org/10.1016/j.jip.2008.02.010 10.1016/j.jip.2008.02.01018359042 Search in Google Scholar

Bakonyi, T., Farkas, R., Szendroi, A., Dobos-Kovacs, M., Rusvai, M. (2002). Detection of acute bee paralysis virus by RT-PCR in honey bee and Varroa destructor field samples: rapid screening of representative Hungarian apiaries. Apidologie, 33, 63–74. https://doi.org/10.1051/apido:2001004 BakonyiT. FarkasR. SzendroiA. Dobos-KovacsM. RusvaiM. 2002 Detection of acute bee paralysis virus by RT-PCR in honey bee and Varroa destructor field samples: rapid screening of representative Hungarian apiaries Apidologie 33 63 74 https://doi.org/10.1051/apido:2001004 10.1051/apido:2001004 Search in Google Scholar

Benjeddou, M., Leat, N., Allsopp, M., Davison, S. (2001). Detection of Acute Bee Virus and Black Queen Cell Virus from honeybees by reverse transcriptase. Applied and Environmental Microbiology, 67, 2384–2387. https://doi.org/10.1128/aem.67.5.2384-2387.2001 BenjeddouM. LeatN. AllsoppM. DavisonS. 2001 Detection of Acute Bee Virus and Black Queen Cell Virus from honeybees by reverse transcriptase Applied and Environmental Microbiology 67 2384 2387 https://doi.org/10.1128/aem.67.5.2384-2387.2001 10.1128/AEM.67.5.2384-2387.20019288411319129 Search in Google Scholar

Berényi, O., Bakonyi, T., Derakhshifar, I., Köglberger, H., Nowotny, N. (2006). Occurrence of six honeybee viruses in diseased Austrian apiaries. Applied and Environmental Microbiology, 72(4), 2414–2420. https://doi.org/10.1128/AEM.72.4.2414-2420.2006 BerényiO. BakonyiT. DerakhshifarI. KöglbergerH. NowotnyN. 2006 Occurrence of six honeybee viruses in diseased Austrian apiaries Applied and Environmental Microbiology 72 4 2414 2420 https://doi.org/10.1128/AEM.72.4.2414-2420.2006 10.1128/AEM.72.4.2414-2420.2006144902716597939 Search in Google Scholar

Bonning, B.C. (2009). The Dicistroviridae: An emerging family of invertebrate viruses. Virologica Sinica, 24, 415–427. https://doi.org/10.1007/s12250-009-3044-1 BonningB.C. 2009 The Dicistroviridae: An emerging family of invertebrate viruses Virologica Sinica 24 415 427 https://doi.org/10.1007/s12250-009-3044-1 10.1007/s12250-009-3044-1 Search in Google Scholar

Bravi, M.E., Avalos, J., Rosero, H., Maldonado, G., Reynaldi, F.J., Genchi-García, M.L. (2020). Short communication: Molecular detection of honeybee viruses in Ecuador. Spanish Journal of Agricultural Research, 18(1), e05SC02. https://doi.org/10.5424/sjar/2020181-15779 BraviM.E. AvalosJ. RoseroH. MaldonadoG. ReynaldiF.J. Genchi-GarcíaM.L. 2020 Short communication: Molecular detection of honeybee viruses in Ecuador Spanish Journal of Agricultural Research 18 1 e05SC02 https://doi.org/10.5424/sjar/2020181-15779 10.5424/sjar/2020181-15779 Search in Google Scholar

Cagirgan, A.A., Yildirim, Y., Usta, A. (2020). Phylogenetic analysis of deformed wing virus, black queen cell virus and acute bee paralysis viruses in Turkish honeybee colonies. Medicine Veterinary, 76(8), 480–484. https://doi.org/10.21521/mw.6437 CagirganA.A. YildirimY. UstaA. 2020 Phylogenetic analysis of deformed wing virus, black queen cell virus and acute bee paralysis viruses in Turkish honeybee colonies Medicine Veterinary 76 8 480 484 https://doi.org/10.21521/mw.6437 10.21521/mw.6437 Search in Google Scholar

Cagirgan, A., & Yazici, Z. (2021). The prevalence of seven crucial honeybee viruses using multiplex RT-PCR and their phylogenetic analysis. Turkish Journal of Veterinary and Animal Sciences, 45, 44–55. https://doi.org/10.3906/vet-2004-139. CagirganA. YaziciZ. 2021 The prevalence of seven crucial honeybee viruses using multiplex RT-PCR and their phylogenetic analysis Turkish Journal of Veterinary and Animal Sciences 45 44 55 https://doi.org/10.3906/vet-2004-139. 10.3906/vet-2004-139 Search in Google Scholar

Chen, Y., Zhao, Y., Hammond, J., Hsu, H.T., Evans, J., Feldlaufer, M. (2004). Multiple virus infections in the honey bee and genome divergence of honey bee viruses. Journal of Invertebrate Pathology, 87(2–3), 84–93. https://doi.org/10.1016/j.jip.2004.07.005 ChenY. ZhaoY. HammondJ. HsuH.T. EvansJ. FeldlauferM. 2004 Multiple virus infections in the honey bee and genome divergence of honey bee viruses Journal of Invertebrate Pathology 87 2–3 84 93 https://doi.org/10.1016/j.jip.2004.07.005 10.1016/j.jip.2004.07.00515579317 Search in Google Scholar

Chen, Y., Evans, J.D., Feldlaufer M. (2006). Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera L. Journal of Invertebrate Pathology, 92, 152–159. https://doi.org/10.1016/j.jip.2006.03.010 ChenY. EvansJ.D. FeldlauferM. 2006 Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera L Journal of Invertebrate Pathology 92 152 159 https://doi.org/10.1016/j.jip.2006.03.010 10.1016/j.jip.2006.03.01016793058 Search in Google Scholar

Chen, G., Wu, Y., Deng, J., Wen, Z., Wang, S., Chen, Y.,…Zheng, H. (2021). Seasonal variation of viral infections between the eastern honey bee (Apis cerana) and the western honey bee (Apis mellifera). Microbiology Open, 10(1), e1162. https://doi.org/10.1002/mbo3.1162 ChenG. WuY. DengJ. WenZ. WangS. ChenY. ZhengH. 2021 Seasonal variation of viral infections between the eastern honey bee (Apis cerana) and the western honey bee (Apis mellifera) Microbiology Open 10 1 e1162 https://doi.org/10.1002/mbo3.1162 10.1002/mbo3.1162786287333650796 Search in Google Scholar

Choe, S.E., Nguyen, T.T., Hyun, B.H., Noh, J.H., Lee, H.S., Lee, C.H., Kang, S.W. (2012). Genetic and phylogenetic analysis of South Korean sacbrood virus isolates from infected honey bees (Apis cerena). Veterinary Microbiology, 157, 32–40. https://doi.org/10.1016/j.vetmic.2011.12.007 ChoeS.E. NguyenT.T. HyunB.H. NohJ.H. LeeH.S. LeeC.H. KangS.W. 2012 Genetic and phylogenetic analysis of South Korean sacbrood virus isolates from infected honey bees (Apis cerena) Veterinary Microbiology 157 32 40 https://doi.org/10.1016/j.vetmic.2011.12.007 10.1016/j.vetmic.2011.12.00722221381 Search in Google Scholar

Choi, N.R., Jung, C., Lee, D.W. (2015). Optimization of detection of black queen cell virus from Bombus terrestris via real-time PCR. Journal of Asia-Pacific Entomology, 18(1), 9–12. https://doi.org/10.1016/j.aspen.2014.10.010 ChoiN.R. JungC. LeeD.W. 2015 Optimization of detection of black queen cell virus from Bombus terrestris via real-time PCR Journal of Asia-Pacific Entomology 18 1 9 12 https://doi.org/10.1016/j.aspen.2014.10.010 10.1016/j.aspen.2014.10.010 Search in Google Scholar

de Miranda, J., Gauthier, L., Ribière, M., Chen, Y. (2011). Honey Bee Viruses and Their Effect on Bee and Colony Health. Contemporary Topics in Entomology, 71–102. https://doi.org/10.1201/b11318-9 de MirandaJ. GauthierL. RibièreM. ChenY. 2011 Honey Bee Viruses and Their Effect on Bee and Colony Health Contemporary Topics in Entomology 71 102 https://doi.org/10.1201/b11318-9 10.1201/b11318-8 Search in Google Scholar

de Miranda, J.R., Bailey, L., Ball, B.V., Blanchard, P., Budge, G.E., Chejanovsky, N., ….. van der Steen, J.J.M. (2013). Standard methods for virus research in Apis mellifera. Journal of Apicultural Research, 52(4), 1–56. https://doi.org/10.3896/IBRA.1.52.4.22 de MirandaJ.R. BaileyL. BallB.V. BlanchardP. BudgeG.E. ChejanovskyN. van der SteenJ.J.M. 2013 Standard methods for virus research in Apis mellifera Journal of Apicultural Research 52 4 1 56 https://doi.org/10.3896/IBRA.1.52.4.22 10.3896/IBRA.1.52.4.22 Search in Google Scholar

Eyer, M., Chen, Y.P., Schäfer, M.O., Pettis, J., Neumann, P. (2009). Small hive beetle, Aethina tumida, as a potential biological vector of honeybee viruses. Apidologie, 40, 419–428. https://doi.org/10.1051/apido:2008051 EyerM. ChenY.P. SchäferM.O. PettisJ. NeumannP. 2009 Small hive beetle, Aethina tumida, as a potential biological vector of honeybee viruses Apidologie 40 419 428 https://doi.org/10.1051/apido:2008051 10.1051/apido:2008051 Search in Google Scholar

Foissac, L., Gentit, P., Svanetia-Dumas, L., Dulucq, M.J., Candresse, T. (2001). Polyvalent detection of fruit tree tricho, capillo, and foveaviruses by nested RT-PCR using degenerated and inosine containing primers (pdo rt-pcr). Acta Horticulturae, 550, 37–43. https://doi.org/10.17660/ActaHortic.2001.550.2 FoissacL. GentitP. Svanetia-DumasL. DulucqM.J. CandresseT. 2001 Polyvalent detection of fruit tree tricho, capillo, and foveaviruses by nested RT-PCR using degenerated and inosine containing primers (pdo rt-pcr) Acta Horticulturae 550 37 43 https://doi.org/10.17660/ActaHortic.2001.550.2 10.17660/ActaHortic.2001.550.2 Search in Google Scholar

Glover, R.H., Adams, I.P., Budge, G., Wilkins, S., Boonham, N. (2011). Detection of honey bee (Apis mellifera) viruses with an oligonucleotide microarray. Journal of Invertebrate Pathology, 107(3), 216–219. https://doi.org/10.1016/j.jip.2011.03.004 GloverR.H. AdamsI.P. BudgeG. WilkinsS. BoonhamN. 2011 Detection of honey bee (Apis mellifera) viruses with an oligonucleotide microarray Journal of Invertebrate Pathology 107 3 216 219 https://doi.org/10.1016/j.jip.2011.03.004 10.1016/j.jip.2011.03.00421419132 Search in Google Scholar

Grabensteiner, E., Ritter, W., Carter, M.J., Davison, S., Pechhacker, H., Kolodziejek, J.,…Nowotny, N. (2001). Sacbrood virus of the honeybee (Apis mellifera): rapid identification and phylogenetic analysis using reverse transcription-PCR. Clinical and Diagnostic Laboratory Immunology, 8, 93–104. https://doi.org/doi.org/10.1128/CDLI.8.1.93-104.2001 GrabensteinerE. RitterW. CarterM.J. DavisonS. PechhackerH. KolodziejekJ. NowotnyN. 2001 Sacbrood virus of the honeybee (Apis mellifera): rapid identification and phylogenetic analysis using reverse transcription-PCR Clinical and Diagnostic Laboratory Immunology 8 93 104 https://doi.org/doi.org/10.1128/CDLI.8.1.93-104.2001 10.1128/CDLI.8.1.93-104.20019601611139201 Search in Google Scholar

Grozinger, C.M., & Flenniken, M.L. (2019). Bee viruses: Ecology, pathogenicity, and impacts. Annual Review of Entomology, 64, 205–226. https://doi.org/10.1146/annurev-ento-011118-111942 GrozingerC.M. FlennikenM.L. 2019 Bee viruses: Ecology, pathogenicity, and impacts Annual Review of Entomology 64 205 226 https://doi.org/10.1146/annurev-ento-011118-111942 10.1146/annurev-ento-011118-11194230629896 Search in Google Scholar

Gumusova, S., Albayrak, H., Yazıcı, Z., Kurt, M. (2010). Prevalence of three honey bee viruses in Turkey. Veterinarski Arhiv, 80(6), 779–785. GumusovaS. AlbayrakH. YazıcıZ. KurtM. 2010 Prevalence of three honey bee viruses in Turkey Veterinarski Arhiv 80 6 779 785 Search in Google Scholar

Haddad, N.J., Brake, M., Migdadi, H., de Miranda, J.R. (2008). First detection of honey bee viruses in Jordan by RT-PCR. Jordan Journal of Agricultural Sciences, 4, 242–247. HaddadN.J. BrakeM. MigdadiH. de MirandaJ.R. 2008 First detection of honey bee viruses in Jordan by RT-PCR Jordan Journal of Agricultural Sciences 4 242 247 Search in Google Scholar

Higes, M., Esperon, F., Sanchez-Vizcaino, J.M. (2007). Short communication. First report of Black queen cell virus detection in honey bees (Apis mellifera) in Spain. Spanish Journal of Agricultural Research, 5(3), 322–325. https://doi.org/10.5424/sjar/2007053-263 HigesM. EsperonF. Sanchez-VizcainoJ.M. 2007 Short communication. First report of Black queen cell virus detection in honey bees (Apis mellifera) in Spain Spanish Journal of Agricultural Research 5 3 322 325 https://doi.org/10.5424/sjar/2007053-263 10.5424/sjar/2007053-263 Search in Google Scholar

Highfield, A., Kevill, J., Mordecai, G., Hunt, J., Henderson, S., Sauvard, D.,…Schroeder, D.C. (2020). Detection and Replication of Moku virus in Honey Bees and Social Wasps. Viruses, 12(6), 607. https://doi.org/10.3390/v12060607 HighfieldA. KevillJ. MordecaiG. HuntJ. HendersonS. SauvardD. SchroederD.C. 2020 Detection and Replication of Moku virus in Honey Bees and Social Wasps Viruses 12 6 607 https://doi.org/10.3390/v12060607 10.3390/v12060607735447732498304 Search in Google Scholar

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 and Animal Sciences, 43, 551–554. https://doi.org/10.3906/vet-1811-5 KalaycıG. ÇağırganA.A. PekmezK. ÖzkanB. KaplanM. 2019 Molecular Detection And Phylogenetic Analysis of The Honeybee (Apis mellifera) Sacbrood virus in Turkey Turkish Journal of Veterinary and Animal Sciences 43 551 554 https://doi.org/10.3906/vet-1811-5 10.3906/vet-1811-5 Search in Google Scholar

Kalaycı, 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. Journal of Kafkas University Faculty of Veterinary Medicine, 26(5), 671–677. https://doi.org/10.9775/kvfd.2020.24154 KalaycıG. CagirganA.A. KaplanM. PekmezK. BeyazitA. OzkanB. ArslanF. 2020 The Role of Viral and Parasitic Pathogens Affected By Colony Losses in Turkish Apiaries Journal of Kafkas University Faculty of Veterinary Medicine 26 5 671 677 https://doi.org/10.9775/kvfd.2020.24154 10.9775/kvfd.2020.24154 Search in Google Scholar

Kevan, P.G., Hannan, M.A., Ostiguy, N., Guzman, E. (2006). A summary of the Varroa-virus disease complex in honeybees. American Bee Journal, 146, 694–697. KevanP.G. HannanM.A. OstiguyN. GuzmanE. 2006 A summary of the Varroa-virus disease complex in honeybees American Bee Journal 146 694 697 Search in Google Scholar

Kutlu, M.A., & Gül, A. (2020). The Colony Losses in Bingol Province (Bee Deaths), Causes and Suggestions. Turkish Journal of Agricultural and Natural Sciences, 7(4), 867–873. https://doi.org/10.30910/turkjans.685088 KutluM.A. GülA. 2020 The Colony Losses in Bingol Province (Bee Deaths), Causes and Suggestions Turkish Journal of Agricultural and Natural Sciences 7 4 867 873 https://doi.org/10.30910/turkjans.685088 10.30910/turkjans.685088 Search in Google Scholar

Li, Z., Huang, S., Huang, W.F., Geng, H., Zhao, Y., Li, M., … Su, S. (2016). A scientific note on detection of honeybee viruses in the darkling beetle (Alphitobius diaperinus, Coleoptera: Tenebrionidae), a new pest in Apis cerana cerana colonies. Apidologie, 47(6), 759–761. https://doi.org/10.1007/s13592-016-0430-1 LiZ. HuangS. HuangW.F. GengH. ZhaoY. LiM. SuS. 2016 A scientific note on detection of honeybee viruses in the darkling beetle (Alphitobius diaperinus, Coleoptera: Tenebrionidae), a new pest in Apis cerana cerana colonies Apidologie 47 6 759 761 https://doi.org/10.1007/s13592-016-0430-1 10.1007/s13592-016-0430-1 Search in Google Scholar

Milićević, V., Radojičić, S., Kureljušić, J., Šekler, M., Nešić, K., Veljović, L., … Radosavljević, V. (2018). Molecular detection of black queen cell virus and Kashmir bee virus in honey. AMB Express, 8(1), 128. https://doi.org/10.1186/s13568-018-0655-7 MilićevićV. RadojičićS. KureljušićJ. ŠeklerM. NešićK. VeljovićL. RadosavljevićV. 2018 Molecular detection of black queen cell virus and Kashmir bee virus in honey AMB Express 8 1 128 https://doi.org/10.1186/s13568-018-0655-7 10.1186/s13568-018-0655-7608148430088183 Search in Google Scholar

Muz, D., & Muz, N.M. (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, 1–12. https://doi.org/10.1007/s13592-017-0531-5 MuzD. MuzN.M. 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 12 https://doi.org/10.1007/s13592-017-0531-5 10.1007/s13592-017-0531-5 Search in Google Scholar

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, 310–314. https://doi.org/10.1051/apido:2008007 NielsenS.L. NicolaisenM. KrygerP. 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 39 310 314 https://doi.org/10.1051/apido:2008007 10.1051/apido:2008007 Search in Google Scholar

Noh, J.H., Reddy, K.E., Choe, S.E., Yoo, M.S., Doan, H.T., Kweon, C.H., … Kang, S.W. (2013). Phylogenetic analysis of black queen cell virus genotypes in South Korea. Virus Gene, 46, 362–368. https://doi.org/10.1007/s11262-012-0859-x NohJ.H. ReddyK.E. ChoeS.E. YooM.S. DoanH.T. KweonC.H. KangS.W. 2013 Phylogenetic analysis of black queen cell virus genotypes in South Korea Virus Gene 46 362 368 https://doi.org/10.1007/s11262-012-0859-x 10.1007/s11262-012-0859-x23239276 Search in Google Scholar

Oğuz, B., Karapınar, Z., Dinçer, E., Değer, M.S. (2018). Molecular detection of Nosema spp. and black queen cell virus in honeybees in Van Province, Turkey. Turkish Journal of Veterinary and Animal Sciences, 41, 221–227. https://doi.org/10.3906/vet-1604-92 OğuzB. KarapınarZ. DinçerE. DeğerM.S. 2018 Molecular detection of Nosema spp. and black queen cell virus in honeybees in Van Province, Turkey Turkish Journal of Veterinary and Animal Sciences 41 221 227 https://doi.org/10.3906/vet-1604-92 10.3906/vet-1604-92 Search in Google Scholar

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. https://doi.org/10.1016/j.jviromet.2008.06.027 OlivierV. MassouI. CelleO. BlanchardP. SchurrF. RibièreM. GauthierM. 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 https://doi.org/10.1016/j.jviromet.2008.06.027 10.1016/j.jviromet.2008.06.02718674566 Search in Google Scholar

Reynaldi, F.J., Sguazza, G.H., Albicoro, F.J., Pecoraro, M.R., Galosi, C.M. (2013). First molecular detection of co-infection of honey bee viruses in asymptomatic Bombus atratus in South America. Brazilian Journal of Microbiology, 73(4), 797–800. https://doi.org/10.1111/j.1758-2229.2010.00173.x ReynaldiF.J. SguazzaG.H. AlbicoroF.J. PecoraroM.R. GalosiC.M. 2013 First molecular detection of co-infection of honey bee viruses in asymptomatic Bombus atratus in South America Brazilian Journal of Microbiology 73 4 797 800 https://doi.org/10.1111/j.1758-2229.2010.00173.x 10.1590/S1519-69842013000400016 Search in Google Scholar

Rosenkranz, P., Aumeier, P., Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103, 96–119. https://doi.org/10.1016/j.jip.2009.07.016 RosenkranzP. AumeierP. ZiegelmannB. 2010 Biology and control of Varroa destructor Journal of Invertebrate Pathology 103 96 119 https://doi.org/10.1016/j.jip.2009.07.016 10.1016/j.jip.2009.07.01619909970 Search in Google Scholar

Rüstemoğlu, M., & Sipahioğlu, H.M. (2016). Occurrence and molecular characterization of acute bee paralysis virus (ABPV) in honeybee (Apis mellifera) colonies in Hakkari province. Yuzuncu Yil University Journal of Agricultural Sciences, 26, 174–182. RüstemoğluM. SipahioğluH.M. 2016 Occurrence and molecular characterization of acute bee paralysis virus (ABPV) in honeybee (Apis mellifera) colonies in Hakkari province Yuzuncu Yil University Journal of Agricultural Sciences 26 174 182 Search in Google Scholar

Rüstemoğlu, M., & Sipahioğlu, H.M. (2019). Occurrence and prevalence of six honey bee viruses in Hakkari (Turkey) and their genomic divergence. Munis Entomology & Zoology, 14(2), 574–583. RüstemoğluM. SipahioğluH.M. 2019 Occurrence and prevalence of six honey bee viruses in Hakkari (Turkey) and their genomic divergence Munis Entomology & Zoology 14 2 574 583 Search in Google Scholar

Rüstemoğlu, M. (2020). Isolation and Characterization of Two Important Honeybee-Killing Virus Species, Deformed wing virus (DWV) and Black queen cell virus (BQCV) From Messor Concolorants (Hymenoptera: Formicidae). Applied Ecology and Environmental Research, 18, 7407–7415. https://doi.org/10.15666/aeer/1805_74077415 RüstemoğluM. 2020 Isolation and Characterization of Two Important Honeybee-Killing Virus Species, Deformed wing virus (DWV) and Black queen cell virus (BQCV) From Messor Concolorants (Hymenoptera: Formicidae) Applied Ecology and Environmental Research 18 7407 7415 https://doi.org/10.15666/aeer/1805_74077415 10.15666/aeer/1805_74077415 Search in Google Scholar

Schurr, F., Tison, A., Militano, L., Cheviron, N., Sircoulomb, F., Rivière, M.P., … Dubois, E. (2019). Validation of quantitative real-time RT-PCR assays for the detection of six honeybee viruses. Journal of Virological Methods, 270, 70–78. https://doi.org/10.1016/j.jviromet.2019.04.020 SchurrF. TisonA. MilitanoL. ChevironN. SircoulombF. RivièreM.P. DuboisE. 2019 Validation of quantitative real-time RT-PCR assays for the detection of six honeybee viruses Journal of Virological Methods 270 70 78 https://doi.org/10.1016/j.jviromet.2019.04.020 10.1016/j.jviromet.2019.04.02031026560 Search in Google Scholar

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, 102–106. https://doi.org/10.1016/j.jviromet.2013.08.003 SguazzaG.H. ReynaldiF.J. GalosiC.M. PecoraroM.R. 2013 Simultaneous detection of bee viruses by multiplex PCR Journal of Virological Methods 194 102 106 https://doi.org/10.1016/j.jviromet.2013.08.003 10.1016/j.jviromet.2013.08.00323948157 Search in Google Scholar

Tapaszti, Z., Forgách, P., Kovágó, C., Topolska, G., Nowotny, N., Rusvai, M., Bakonyi, T. (2009). Genetic analysis and phylogenetic comparison of black queen cell virus genotypes. Veterinary Microbiology, 18, 139–227. https://doi.org/10.1016/j.vetmic.2009.06.002 TapasztiZ. ForgáchP. KovágóC. TopolskaG. NowotnyN. RusvaiM. BakonyiT. 2009 Genetic analysis and phylogenetic comparison of black queen cell virus genotypes Veterinary Microbiology 18 139 227 https://doi.org/10.1016/j.vetmic.2009.06.002 10.1016/j.vetmic.2009.06.00219570624 Search in Google Scholar

Tentcheva, D., Gauthier, L., Zappulla, N., Dainat, B., Cousserans, F., Colin, M.E., 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, 7185–7191. https://doi.org/10.1128/aem.70.12.7185-7191.2004 TentchevaD. GauthierL. ZappullaN. DainatB. CousseransF. ColinM.E. BergoinM. 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 7185 7191 https://doi.org/10.1128/aem.70.12.7185-7191.2004 10.1128/AEM.70.12.7185-7191.200453517015574916 Search in Google Scholar

Traiyasut, P., Mookhploy, W., Kimura, K., Yoshiyama, M., Khongphinitbunjong, K., Chantawannakul, P. (2016). First Detection of Honey Bee Viruses in Wax Moth. Chiang Mai Journal of Science, 43, 695–698. TraiyasutP. MookhployW. KimuraK. YoshiyamaM. KhongphinitbunjongK. ChantawannakulP. 2016 First Detection of Honey Bee Viruses in Wax Moth Chiang Mai Journal of Science 43 695 698 Search in Google Scholar

Ullah, A., Tlak-Gajger, I., Majoros, A., Dar, S.A., Khan, S., Kalimullah, … Anjum, S.I. (2021). Viral impacts on honey bee populations: A. review. Saudi Journal of Biological Sciences, 28, 523–530. https://doi.org/10.1016/j.sjbs.2020.10.037 UllahA. Tlak-GajgerI. MajorosA. DarS.A. KhanS. Kalimullah AnjumS.I. 2021 Viral impacts on honey bee populations: A. review Saudi Journal of Biological Sciences 28 523 530 https://doi.org/10.1016/j.sjbs.2020.10.037 10.1016/j.sjbs.2020.10.037778363933424335 Search in Google Scholar

Ünal, H.H., Oruç, H.H., Sezgin, A., Kabil, E. (2010). Determined pesticides after honey bee deaths between 2006 and 2010 in Turkey. Uludag Bee Journal, 10, 118–126. ÜnalH.H. OruçH.H. SezginA. KabilE. 2010 Determined pesticides after honey bee deaths between 2006 and 2010 in Turkey Uludag Bee Journal 10 118 126 Search in Google Scholar

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. https://doi.org/10.1128/AEM.01319-09 WelchA. DrummondF. TewariS. AverillA. BurandJ.P. 2009 Presence and prevalence of viruses in local and migratory honeybees (Apis mellifera) in Massachusetts Applied and Environmental Microbiology 75 24 7862 7865 https://doi.org/10.1128/AEM.01319-09 10.1128/AEM.01319-09279409019854916 Search in Google Scholar

Zhang, X., He, S.Y., Evans, J.D., Pettis, J.S., Yin, G.F., Chen, Y.P. (2012). New evidence that deformed wing virus and black queen cell virus are multi-host pathogens. Journal of Invertebrate Pathology, 109(1), 156–159. https://doi.org/10.1016/j.jip.2011.09.010 ZhangX. HeS.Y. EvansJ.D. PettisJ.S. YinG.F. ChenY.P. 2012 New evidence that deformed wing virus and black queen cell virus are multi-host pathogens Journal of Invertebrate Pathology 109 1 156 159 https://doi.org/10.1016/j.jip.2011.09.010 10.1016/j.jip.2011.09.01022001629 Search in Google Scholar