Detection and replication of deformed wing virus and black queen cell virus in parasitic mites, Varroa destructor, from Iranian honey bee (Apis mellifera) colonies

References

• Abou Kubaa, R., Molinatto, G., Solaiman Khaled, B., Daher-Hjaij, N., Heinoun, Kh., & 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.
   Web of Science ®Google Scholar
• Anguiano-Baez, R., Guzman-Novoa, E., Hamiduzzaman, M. M., Espinosa-Montaño, L. G., & Correa-Benítez, A. (2016). Varroa destructor (Mesostigmata: Varroidae) parasitism and climate differentially influence the prevalence, levels and overt infections of deformed wing virus in honey bees (Hymenoptera: Apidae). Journal of Insect Science, 16(1), 44. doi:10.1093/jisesa/iew029
   PubMed Web of Science ®Google Scholar
• Aubert, M., Ball, B., Fries, I., Moritz, R. F. A., Milani, N., & Bernardinelli, I. (2008). Virologyand the honey bee. Luxembourg: European Commission.
   Google Scholar
• Azari, P., Özkan Koca, A., & Kandemir, I. (2014). Honey bee colony losses in Iran: Results of a survey between 2006 and 2011. Bee World, 91, 75–79. CrossRef][https://doi.org/10.1080/0005772X.2014.11417610]
   Google Scholar
• 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. doi:10.1128/AEM.67.5.2384-2387.2001
   PubMed Web of Science ®Google Scholar
• Berthoud, H., Imdorf, A., Haueter, M., Radloff, S., & Neumann, P. (2010). Virus infections and winter losses of honey bee colonies (Apis mellifera). Journal of Apicultural Research, 49(1), 60–65. doi:10.3896/IBRA.1.49.1.08
   Web of Science ®Google Scholar
• Bokaie, S., Sharifi, L., & Mehrabadi, M. (2014). Prevalence and epizootical aspects of varroasis in Golestan Province, Northern Iran. Journal of Arthropod-Borne Diseases, 8(1), 102–107.
   PubMed Web of Science ®Google Scholar
• Chen, Y., Evans, J., & Feldlaufer, M. (2006). Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. Journal of Invertebrate Pathology, 92(3), 152–159. doi:10.1016/j.jip.2006.03.010
   PubMed Web of Science ®Google Scholar
• Chen, Y., Zhao, Y., Hammond, J., Hsu, H., Evans, J., & Feldlaufer, M. (2004). Multiplevirus infections in the honey bee and genome divergence of honey bee viruses. Journal of Invertebrate Pathology, 87(2–3), 84–93. doi:10.1016/j.jip.2004.07.005
   PubMed Web of Science ®Google Scholar
• Chen, Y. P., Higgins, J. A., & Feldlaufer, M. F. (2005). Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.). Applied and Environmental Microbiology, 71(1), 436–441. doi:10.1128/AEM.71.1.436-441.2005
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1126/science.1146498
   PubMed Web of Science ®Google Scholar
• Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L., & Neumann, P. (2012). Predictive markers of honey bee colony collapse. PLoS ONE, 7(2), e32151. doi:10.1371/journal.pone.0032151
   PubMed Web of Science ®Google Scholar
• Dainat, B., & Neumann, P. (2013). Clinical of deformed wing virus infection are predictive markers for honey bee colony losses. Journal of Invertebrate Pathology, 112(3), 278–280. doi:10.1016/j.jip.2012.12.009
   PubMed Web of Science ®Google Scholar
• de Miranda, J. R., & Genersch, E. (2010). Deformed wing virus. Journal of Invertebrate Pathology, 103, 48–61. doi:10.1016/j.jip.2009.06.012
   PubMed Web of Science ®Google Scholar
• Di Prisco, G., Pennacchio, F., Caprio, E., Boncristiani, 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. doi:10.1099/vir.0.023853-0
   PubMed Web of Science ®Google Scholar
• Emsen, B., Hamiduzzaman, M. M., Goodwin, P. H., & Guzman-Novoa, E. (2015). Lower virus infections in Varroa destructor-infested and uninfested brood and adult honey bees Apis mellifera) of a low mite population growth colony compared to a high mite population growth colony. PLoS ONE, 10(2), e0118885. doi:10.1371/journal.pone.0118885
   PubMed Web of Science ®Google Scholar
• Fedorova, A. A., Azzami, K., Ryabchikova, E. I., Spitsyna, Y. E., Silnikov, V. N., Ritter, W., … Zenkova, M. A. (2011). Inactivation of a non-enveloped RNA virus by artificial ribonucleases: Honey bees and acute bee paralysis virus as a new experimental model for in vivo antiviral activity assessment. Antiviral Research, 91(3), 267–277. doi:10.1016/j.antiviral.2011.06.011
   PubMed Web of Science ®Google Scholar
• Food and Agriculture Organization of the United Nations (FAO). (2017). Production of beehives in Iran. Retrieved from http://www.fao.org/faostat/en/#data/QA/visualize
   Google Scholar
• Genersch, E., & Aubert, M. (2010). Emerging and re-emerging viruses of the honey bee (Apis mellifera). Veterinary Research, 41(6), 54–55. doi:10.1051/vetres/2010027
   PubMed Web of Science ®Google Scholar
• Genersch, E., Yue, C., Fries, I., & de Miranda, J. R. (2006). Detection of deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. Journal of Invertebrate Pathology, 91(1), 61–63. doi:10.1016/j.jip.2005.10.002
   PubMed Web of Science ®Google Scholar
• Ghorani, M., Madadgar, O., Langeroudi, A. G., Rezapanah, M., Nabian, S., Akbarein, H., … Forsi, M. (2017). The first comprehensive molecular detection of six honey bee viruses in Iran in 2015–2016. Archives of Virology, 162(8), 2287–2291. doi:10.1007/s00705-017-3370-9
   PubMed Web of Science ®Google Scholar
• Gisder, S., Aumeier, P., & Genersch, E. (2009). Deformed wing virus: Replication and viral load in mites (Varroa destructor). Journal of Genetic Virology, 90(2), 463–467.
   PubMed Web of Science ®Google Scholar
• Grabensteiner, E., Bakonyi, T., Ritter, W., Pechhacker, H., & Nowotny, N. (2007). Development of a multiplex RT-PCR for the simultaneous detection of three viruses of the honeybee (Apis mellifera L.): Acute bee paralysis virus, Black queen cell virus and Sacbrood virus. Journal of Invertebrate Pathology, 94(3), 222–225. doi:10.1016/j.jip.2006.11.006
   PubMed Web of Science ®Google Scholar
• Guzman-Novoa, E. (2016). Colony collapse disorder and other threats to honey bees. In: S. Cork, D. C. Hall, & K. Liljebjelke (Eds.), One health case studies: Addressing complex problems in a changing world. Sheffield: 5M Publishing Ltd.
   Google Scholar
• Guzman-Novoa, E., Hamiduzzaman, M. M., Correa-Benítez, A., Espinosa-Montaño, L. G., & Uribe-Rubio, J. L. (2013). A scientific note on the first detection of black queen cell virus in honey bees (Apis mellifera) in Mexico. Apidologie, 44(4), 382–384. doi:10.1007/s13592-012-0191-4
   Web of Science ®Google Scholar
• Guzman-Novoa, E., Hamiduzzaman, M. M., Espinosa-Montano, L. G., Correa-Benítez, A., Anguiano-Baez, R., & Ponce-Vázquez, R. (2012). First detection of four viruses in honey bee (Apis mellifera) workers with and without deformed wings and Varroa destructor in Mexico. Journal of Apicultural Research, 51(4), 342–346. doi:10.3896/IBRA.1.51.4.08
   Web of Science ®Google Scholar
• Haddad, N. J., Noureddine, A., Al-Shagour, B., Loucif-Ayad, W., El-Niweiri, M. A. A., Anaswah, E., … de Miranda, J. R. (2017). Distribution and variability of deformed wing virus of honeybees (Apis mellifera) in the Middle East and North Africa. Insect Science, 24(1), 103–113. doi:10.1111/1744-7917.12277
   PubMed Web of Science ®Google Scholar
• Hamiduzzaman, M. M., Guzman-Novoa, E., Goodwin, P. H., Reyes-Quintana, M., Koleoglu, G., Correa-Benítez, A., & Petukhova, T. (2015). Differential responses of Africanized and European honey bees (Apis mellifera) to viral replication following mechanical transmission or Varroa destructor parasitism. Journal of Invertebrate Pathology, 126, 12–20. doi:10.1016/j.jip.2014.12.004
   PubMed Web of Science ®Google Scholar
• Holland, J. J., De La Torre, J. C., Clarke, D. K., & Duarte, E. (1991). Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. Journal of Virology, 65(6), 2960–2967.
   PubMed Web of Science ®Google Scholar
• Kevan, P. G., Hannan, M. A., Ostiguy, N., & Guzman-Novoa, E. (2006). A summary of the varroa-virus disease complex in honey bees. American Bee Journal, 146, 694–697.
   Web of Science ®Google Scholar
• Koleoglu, G., Goodwin, P. H., Reyes-Quintana, M., Hamiduzzaman, M. M., & Guzman-Novoa, E. (2017). Effect of Varroa destructor, wounding and Varroa homogenate on gene expression in brood and adult honey bees. PLoS ONE, 12(1), e0169669. doi:10.1371/journal.pone.0169669
   PubMed Web of Science ®Google Scholar
• Koleoglu, G. H., Goodwin, P., Reyes-Quintana, M., Hamiduzzaman, M. M., & Guzman-Novoa, E. (2018). Varroa destructor parasitism reduces hemocyte concentrations and prophenol oxidase gene expression in bees from two populations. Parasitology Research, 117, 1175. doi:10.1007/s00436-018-5796-8
   PubMed Web of Science ®Google Scholar
• Le Conte, Y., Ellis, M., & Ritter, W. (2010). Varroa mites and honey bee health: Can Varroa explain part of the colony losses? Apidologie, 41(3), 353–363. doi:10.1051/apido/2010017
   Web of Science ®Google Scholar
• Lotfi, A., & Shahryar, H. A. (2011). Seasonal incidence of some economic bee diseases (varroosis, nosemosis and American foulbrood) in honey bee colonies of northwestern Iran. Uludag Bee Journal, 11, 25–31.
   Google Scholar
• Macedo, P. A., Wu, J., & Ellis, M. D. (2002). Using inert dusts to detect and assess varroa infestations in honey bee colonies. Journal of Apicultural Research, 41(1–2), 3–7. doi:10.1080/00218839.2002.11101062
   Web of Science ®Google Scholar
• Maori, E., Paldi, N., Shafir, S., Kalev, H., Tsur, E., Glick, E., & Sela, I. (2009). IAPV, a bee-affecting virus associated with colony collapse disorder can be silenced by dsRNA ingestion. Insect Molecular Biology, 18(1), 55–60. doi:10.1111/j.1365-2583.2009.00847.x
   PubMed Web of Science ®Google Scholar
• Martin, S. J., Highfield, A. C., Brettell, L., Villalobos, E. M., Budge, G. E., Powell, M., … Schroeder, D. C. (2012). Global honey bee viral landscape altered by a parasitic mite. Science, 336(6086), 1304–1306. doi:10.1126/science.1220941
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1007/s13592-017-0531-5
   Web of Science ®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(3), 310–314. doi:10.1051/apido:2008007
   Web of Science ®Google Scholar
• Omidi-Arjenaki, O., Ebrahimi, R., & Ghanbarian, D. (2016). Analysis of energy input and output for honey production in Iran (2012–2013). Journal of Renewable and Sustainable Energy, 59, 52–957.
   Google Scholar
• Peng, W., Li, J., Boncristiani, H., Strange, J. P., Hamilton, M., & Chen, Y. (2011). Host range expansion of honey bee black queen cell virus in the bumble bee, Bombus huntii. Apidologie, 42(5), 650–658. doi:10.1007/s13592-011-0061-5
   Web of Science ®Google Scholar
• Ramsey, S. D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J. D., Cohen, A., … van Engelsdorp, D. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences, 116(5), 1792–1801. doi:10.1073/pnas.1818371116
   PubMed Web of Science ®Google Scholar
• Rasuli, F., Nazemi-Rafie, J., & Sadeghi, A. (2017). Acute contact toxicity of six pesticides in honeybees (Apis mellifera Meda) in Iran. Journal of Apicultural Science, 61(1), 29–36. doi:10.1515/jas-2017-0003
   Web of Science ®Google Scholar
• 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. doi:10.1080/00218839.1995.11100900
   Web of Science ®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(12), 7185–7191. doi:10.1128/AEM.70.12.7185-7191.2004
   PubMed Web of Science ®Google Scholar
• Van Engelsdorp, D., Evans, J. D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B. K., … Pettis, J. S. (2009). Colony collapse disorder: A descriptive study. PLoS ONE, 4(8), e6481. doi:10.1371/journal.pone.0006481
   PubMed Web of Science ®Google Scholar
• Wilfert, L., Long, G., Leggett, H. C., Schmid-Hempel, P., Butlin, R., Martin, S. J., & Boots, M. (2016). Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science, 351(6273), 594–597. doi:10.1126/science.aac9976
   PubMed Web of Science ®Google Scholar
• Yang, X., & Cox-Foster, D. (2005). Impact of an ectoparasite on the immunity and pathology of an invertebrate host: Evidence for host immunosuppression and viral amplication. Proceedings of the National Academy of Sciences, 102(21), 7470–7475. doi:10.1073/pnas.0501860102
   PubMed Web of Science ®Google Scholar
• Yue, C., & Genersch, E. (2005). RT-PCR analysis of deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). Journal of General Virology, 86(12), 3419–3424. doi:10.1099/vir.0.81401-0
   PubMed Web of Science ®Google Scholar
• Zhang, X., He, S. Y., Evans, J. D., Pettis, J. S., Yin, G., & 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. doi:10.1016/j.jip.2011.09.010
   PubMed Web of Science ®Google Scholar