China has the largest number of managed honey bee colonies globally, but there is currently no data on viral infection in diseased A. mellifera L. colonies in China. In particular, there is a lack of data on chronic bee paralysis virus (CBPV) in Chinese honey bee colonies. Consequently, the present study investigated the occurrence and frequency of several widespread honey bee viruses in diseased Chinese apiaries, and we used the reverse transcription-polymerase chain reaction (RT-PCR) assay. Described was the relationship between the presence of CBPV and diseased colonies (with at least one of the following symptoms: depopulation, paralysis, dark body colorings and hairless, or a mass of dead bees on the ground surrounding the beehives). Phylogenetic analyses of CBPV were employed. The prevalence of multiple infections of honey bee viruses in diseased Chinese apiaries was 100%, and the prevalence of infections with even five and six viruses were higher than expected. The incidence of CBPV in diseased colonies was significantly higher than that in apparently healthy colonies in Chinese A. mellifera aparies, and CBPV isolates from China can be separated into Chinese-Japanese clade 1 and 2. The results indicate that beekeeping in China may be threatened by colony decline due to the high prevalence of multiple viruses with CBPV.
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Ai H. Yan X. Han R. (2012) Occurrence and prevalence of seven bee viruses in Apis mellifera and Apis cerana apiaries in China. Journal of Invertebrate Pathology 109(1): 160-164.
Allen M. Ball B. (1996) The incidence and world distribution of the honey bee viruses. Bee World 77: 141-162.
Bacandritsos N. Granato A. Budge G. Papanastasiou I. Roinioti E. Caldon M. Falcaro C. Gallina A. Mutinelli F. (2010) Sudden deaths and colony population decline in Greek honey bee colonies. Journal of Invertebrate Pathology. 105(3): 335-340.
Bailey L. Woods R. D. (1977) Two more small RNA viruses from honeybees and further observations on sacbrood and acute bee-paralysis viruses. The Journal of General Virology 37: 175-182.
Bailey L. Gibbs A. J. Woods R. D. (1963) Two viruses from adult honey bees (Apis mellifera Linnaeus). Virology 21: 390-395.
Ball B. V. (1996) Honeybee viruses: a cause for concern? Bee World 77: 117-119.
Berényi O. Bakonyi T. Derakhshifar I. Köglberger H. Nowotny N. (2006) Occurrence of six honey bee viruses in diseased Austrian apiaries. Applied and Environmental Microbiology 72(4): 2414-2420.
Blanchard P. Schurr F. Olivier V. Celle O. Antùnez K. Bakonyi T. Berthoud H. Haubruge E. Higes M. Kasprzak S. Koeglberger H. Kryger P. Thiéry R. 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.
Celli G. Maccagnani B. (2003) Honey bees as bioindicators of environmental pollution. Bulletin of Insectology 56: 137-139.
Chantawannakul P. Ward L. Boonham N. Brown M. (2006) A scientific note on the detection of honeybee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Thai honeybee (Apis mellifera) apiary. Journal of Invertebrate Pathology. 91(1): 69-73.
Chen Y. P. Evans J. D. Pettis J. S. (2011) The presence of chronic bee paralysis virus infection in honey bees (Apis mellifera L.) in the USA. Journal of Apicultural Research 50(2): 85-86.
Cox-Foster D. L. Conlan S. Holmes E. C. Palacios G. Evans J. D. Moran N. A. Quan P. L. Briese T. Hornig M. Geiser D. M. Martinson V. vanEngelsdorp D. Kalkstein A. L. Drysdale A. Hui J. Zhai J. Cui L. Hutchison S. K. Simons J. F. Eqholm M. Pettis J. S. Lipkin W. I. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318(5848): 283-287.
de Miranda J. Genersch E. (2010) Deformed wing virus. Journal of Invertebrate Pathology 103: S48-S61.
de Miranda J. R. Bailey L. Ball B. V. Blanchard P. Budge G. E. Chejanovsky N. Chen Y. P. Gauthier L. Genersch E. de Graaf D. C. Ribière M. Ryabov E. De Smet L. van der Steen J. J. M. (2013) Standard methods for virus research in Apis mellifera. Journal of Apicultural Research 52:4 1-56.
Edgar R. C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32(5): 1792-1797.
Feng F. Chen S. J. Xia L. J. Chen M. Fang Q. Y. Gao Y. J. Yin M. B. (1986) Studies on RNA and protein components of chronic bee paralysis virus. Chinese Journal of Virology 2: 175-180.
Jia H. R. Liu J. Z. Wang X. Wu Y. Y. Zhou T. (2014) Occurrence and prevalence of six bee viruses in Beijing. Chinese Journal of Applied Entomology 51: 772-780.
Kajobe R. Marris G. Budge G. Laurenson L. Cordoni G. Jones B. Wilkins S. Cuthbertson A. G. Brown M. A. (2010) First molecular detection of a viral pathogen in Ugandan honey bees. Journal of Invertebrate Pathology 104(2): 153-156.
Kojima Y. Toki T. Morimoto T. Yoshiyama M. Kimura K. Kadowaki T. (2011) Infestation of Japanese native honey bees by tracheal mite and virus from non-native European honey bees in Japan. Microbial Ecology 62(4): 895-906.
Li Z. G. (2014) Molecular detection prevalence and transmission of Israeli acute paralysis virus and its effects on honey bee behaviors. Ph.D. dissertation. Zhejiang University. Hangzhou. 114 pp.
Morimoto T. Kojima Y. Yoshiyama M. Kimura K. Yang Y. Kadowaki T. (2012) Molecular identification of chronic bee paralysis virus infection in Apis mellifera colonies in Japan. Viruses 4(7): 1093-1103.
Olivier V. Blanchard P. Chaouch S. Lallemand P. Schurr F. Celle O. Dubois E. Tordo N. Thiéry R. Houlgatte R. Ribière M. (2008) Molecular characterization and Phylogenetic analysis of chronic bee paralysis virus a honey bee virus. Virus Research 132(1-2): 59-68.
Ribière M. Triboulot C. Mathieu L. Auriéres C. Faucon J. P. Péin M. (2002) Molecular diagnosis of chronic bee paralysis virus infection. Apidologie 33: 339-351.
Ribière M. Lallemand P. Iscache A.L. Schurr F. Celle O. Blanchard P. Olivier V. 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.
Sanpa S. Chantawannakul P. (2009) Survey of six bee viruses using RT-PCR in Northern Thailand. Journal of Invertebrate Pathology 100(2): 116-119.
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.
Shen M. L. Ositiguy C. N. Cox-Foster D. (2005) Intricate transmission routes and interactions between picornalike viruses (Kashmir bee virus and Sacbrood virus) with the honeybee host and the parasitic Varroa mite. Journal of General Virology 86: 2281-2289. SPSS 17.0
SPSS Inc. Chicago IL.
Todd J. H. de Miranda J. R. Ball B. V. (2007) Incidence and molecular characterization of viruses found in dying New Zealand honey bee (Apis mellifera) colonies infested with Varroa destructor. Apidologie 38: 354-367.
vanEngelsdorp D. Hayes J. J. Underwood R. M. Caron R. M. Pettis J. (2011) A survey of managed honey bee colony losses in the USA fall 2009 to winter 2010. Journal of Apicultural Research 50: 1-10.
Vejsnæs F. Nielsen S. L. Kryger P. (2010) Factors involved in the recent increase in colony losses in Denmark. Journal of Apicultural Research 49(1): 109-110.
Yang B. Peng G. Li T. Kadowaki T. (2013) Molecular and phylogenetic characterization of honey bee viruses Nosema microsporidia protozoan parasites and parasitic mites in China. Ecology and Evolution 3(2): 298-311.