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Occurrence, detection, and quantification of economically important viruses in healthy and unhealthy honey bee (Hymenoptera: Apidae) colonies in Canada

Published online by Cambridge University Press:  20 May 2015

Suresh D. Desai ,
Santosh Kumar  and
Robert W. Currie
Suresh D. Desai*
Affiliation:
Department of Entomology, University of Manitoba, R3T 2N2 Winnipeg, Canada
Santosh Kumar
Affiliation:
Department of Plant Science, University of Manitoba, R3T 2N2 Winnipeg, Canada Agriculture and Agri-Food Canada, Brandon Research Centre, 2701 Grand Valley Road, Box 1000A, R.R. #3, Brandon, R7A 5Y3 Manitoba, Canada
Robert W. Currie
Affiliation:
Department of Entomology, University of Manitoba, R3T 2N2 Winnipeg, Canada
*
1 Corresponding author (e-mail: [email protected]).
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Abstract

The occurrence, quantification, and distribution patterns of deformed wing virus (DWV) and sacbrood virus (SBV), (family Iflaviridae); black queen cell virus (BQCV), Israeli acute paralysis virus (IAPV), Kashmir bee virus (KBV), and acute bee paralysis virus (ABPV) (family Dicistroviridae), and chronic bee paralysis virus (CBPV) (unclassified), were characterised in 80 “healthy” honey bee (Apis mellifera Linnaeus; Hymenoptera: Apidae) colonies and 23 “unhealthy” colonies by employing reverse transcription polymerase chain reaction (RT-PCR) for virus identification and quantitative real-time polymerase chain reaction (qPCR) for quantification. All seven viruses were common but the most prevalent viruses were DWV, followed by BQCV and IAPV. For most viruses, prevalence in surviving but unhealthy colonies in spring did not differ from that of healthy baseline colony levels in fall suggesting spring prevalence level would not be a useful metric for diagnosis of factors contributing to colony loss. Sacbrood virus was the only virus that was more prevalent in unhealthy colonies from Manitoba, Canada than in healthy from colonies across Canada but did not differ from healthy colonies within Manitoba. Multiple infections were ubiquitous with a few colonies having simultaneous infection with as many as five viruses. Among the three viruses quantified by qPCR, DWV had the highest relative concentrations in pooled samples of worker bees. Deformed wing virus was the only virus within healthy colonies that differed in fall concentration among provinces and was at high levels in unhealthy colonies. Black queen cell virus was positively correlated with IAPV across all samples. Our study provides the first major baseline study of viruses in Canadian honey bees.

Type
Behaviour & Ecology
Information
The Canadian Entomologist , Volume 148 , Issue 1 , February 2016 , pp. 22 - 35
Copyright
© Entomological Society of Canada 2015 

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Footnotes

Subject editor: Justin Schmidt

References

Ai, H., Yan, X., and Han, R. 2012. Occurrence and prevalence of seven bee viruses in Apis mellifera and Apis cerana apiaries in China. Journal of Invertebrate Pathology, 109: 160–164.Google Scholar
Aizen, M.A. and Harder, L.D. 2009. The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Current Biology, 19: 915–918.Google Scholar
Allen, M.F. and Ball, B.V. 1995. Characterisation and serological relationships of strains of Kashmir bee virus. Annals of Applied Biology, 126: 471–484.Google Scholar
Allen, M.F. and Ball, B.V. 1996. The incidence and world distribution of honey bee viruses. Bee World, 77: 141–162.Google Scholar
Aubert, M., Ball, B., Fries, I., Moritz, R., Milani, N., and Bernardinelli, I. 2008. Virology and the honey bee. European Commission Directorate-General for Research, Brussells, Belgium.Google Scholar
Bailey, L. and Ball, B.V. 1991. Honey bee pathology. Academic Press, San Diego, California, United States of America.Google Scholar
Bailey, L., Ball, B.V., and Perry, J.N. 1983. Association of viruses with two protozoal pathogens of the honey bee. Annals of Applied Biology, 103: 13–20.Google Scholar
Bailey, L. and 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.Google Scholar
Ball, B.V. and Allen, M.F. 1988. The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni . Annals of Applied Biology, 113: 237–244.Google Scholar
Ball, B.V. and Bailey, L. 1997. Viruses. In Honey bee pests predators and diseases. Edited by R.A. Morse and K. Flottum. AI Root Co., Medina, Ohio, United States of America. Pp. 11–31.Google Scholar
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: 2384–2387.Google Scholar
Berényi, O., Bakonyi, T., Derakhshifar, I., Koglberger, H., and Nowotny, N. 2006. Occurrence of six honeybee viruses in diseased Austrian apiaries. Applied and Environmental Microbiology, 72: 2414–2420. doi:10.1128/aem.72.4.2414-2420.2006.Google Scholar
Berényi, O., Bakonyi, T., Derakhshifar, I., Koglberger, H., Topolska, G., Ritter, W., et al. 2007. Phylogenetic analysis of deformed wing virus genotypes from diverse geographic origins indicates recent global distribution of the virus. Applied and Environmental Microbiology, 73: 3605–3611. doi:10.1128/aem.00696-07.Google Scholar
Blanchard, P., Schurr, F., Celle, O., Cougoule, N., Drajnudel, P., Thiery, R., et al. 2008. First detection of Israeli acute paralysis virus (IAPV) in France, a dicistrovirus affecting honeybees (Apis mellifera). Journal of Invertebrate Pathology, 99: 348–350. doi:10.1016/j.jip.2008.07.006.Google Scholar
Canada Honey Council. 2012. Overview of the Canadian apiculture industry [online]. Canadian Honey Council. Available from http://www.honeycouncil.ca/cdn_apiculture_overview.php [accessed 26 March 2012].Google Scholar
Canadian Association of Professional Apiculturalists. 2013. CAPA statement on honey bees losses in Canada 2013 [online]. In Canadian Association of Professional Apiculturists. Available from http://capabees.org/content/uploads/2013/06/2013-CAPA-Statement-on-Colony-Losses-final.pdf [accessed 12 February 2014].Google Scholar
Carey, G. 2012. Quantitative Methods in Neuroscience. University of Colorado, Boulder, Colorado, United States of America. Available at: http://psych.colorado.edu/~carey/qmin/qmin.php [accessed 20 September 2013].Google Scholar
Chantawannakul, P., Ward, L., Boonham, N., and 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: 69–73. doi:10.1016/j.jip.2005.11.001.Google Scholar
Chen, Y.P., Higgins, J.A., and 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: 436–441. doi:10.1128/aem.71.1.436-441.2005.Google Scholar
Chen, Y.P., Pettis, J.S., Collins, A., and Feldlaufer, M.F. 2006. Prevalence and transmission of honeybee viruses. Applied and Environmental Microbiology, 72: 606–611. doi:10.1128/aem.72.1.606-611.2006.Google Scholar
Chen, Y.P., Pettis, J.S., Corona, M., Chen, W.P., Li, C.J., Spivak, M., et al. 2014. Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health. Public Library of Science Pathogens, 10: e1004261.Google Scholar
Chen, Y.P. and Siede, R. 2007. Honey bee viruses. Advances in Virus Research, 70: 33–80.Google Scholar
Chen, Y.P., Smith, I.B., Collins, A.M., Pettis, J.S., and Feldlaufer, M.F. 2004a. Detection of deformed wing virus infection in honey bees, Apis mellifera L., in the United States. American Bee Journal, 144: 557–559.Google Scholar
Chen, Y.P., Zhao, Y., Hammond, J., Hsu, H.T., Evans, J., and Feldlaufer, M. 2004b. Multiple virus infections in the honey bee and genome divergence of honey bee viruses. Journal of Invertebrate Pathology, 87: 84–93. doi:10.1016/j.jip.2004.07.005.Google Scholar
Cox-Foster, D.L., Conlan, S., Holmes, E.C., Palacios, G., Evans, J.D., Moran, N.A., et al. 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318: 283–287. doi:10.1126/science.1146498.Google Scholar
Currie, R.W., Pernal, S.F., and Guzman-Novoa, E. 2010. Honey bee colony losses in Canada. Journal of Apicultural Research, 49: 104–106.Google Scholar
Dainat, B., Evans, J.D., Chen, Y.P., Gauthier, L., and Neumann, P. 2012. Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Applied and Environmental Microbiology, 78: 981–987.Google Scholar
DeGrandi-Hoffman, G., Chen, Y., Huang, E., and Huang, M.H. 2010. The effect of diet on protein concentration, hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.). Journal of Insect Physiology, 56: 1184–1191.Google Scholar
De Miranda, J.R., Cordoni, G., and Budge, G. 2010. The acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex. Journal of Invertebrate Pathology, 103: S30–S47. doi:10.1016/j.jip.2009.06.014.Google Scholar
De Miranda, J.R. and Genersch, E. 2010. Deformed wing virus. Journal of Invertebrate Pathology, 103: S48–S61.Google Scholar
Desai, S.D., Eu, Y.J., Whyard, S., and Currie, R.W. 2012. Reduction in deformed wing virus infection in larval and adult honey bees (Apis mellifera L.) by double-stranded RNA ingestion. Insect Molecular Biology, 21: 446–455.Google Scholar
Di Prisco, G., Pennacchio, F., Caprio, E., Boncristiani, H.F. Jr., Evans, J.D., and Chen, Y. 2011. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera . Journal of General Virology, 92: 151–155. doi:10.1099/vir.0.023853-0.Google Scholar
Eischen, F. 1995. Varroa resistance to fluvalinate. American Bee Journal, 135: 815–816.Google Scholar
Ellis, J.D. and Munn, P.A. 2005. The worldwide health status of honey bees. Bee World, 86: 88–101.Google Scholar
Elzen, P.J., Baxter, J.R., Spivak, M., and Wilson, W.T. 1999. Amitraz resistance in varroa: new discovery in North America. American Bee Journal, 139: 362.Google Scholar
Elzen, P.J., Eischen, F.A., Baxter, J.B., Pettis, J., Elzen, G.W., and Wilson, W.T. 1998. Fluvalinate resistance in Varroa jacobsoni from several geographic locations. American Bee Journal, 138: 674–676.Google Scholar
Evans, J.D. and Schwarz, R.S. 2011. Bees brought to their knees: microbes affecting honey bee health. Trends in Microbiology, 19: 614–620.Google Scholar
Gallai, N., Salles, J., Settele, J., and Vaissière, B. 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics, 68: 810–821.Google Scholar
Gauthier, L., Tentcheva, D., Tournaire, M., Dainat, B., Cousserans, F., Colin, M.E., et al. 2007. Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique. Apidologie, 38: 426–435. doi:10.1051/apido:2007026.Google Scholar
Genersch, E., von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Buchler, R., et al. 2010. The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie, 41: 332–352. doi:10.1051/apido/2010014.Google Scholar
Guzman-Novoa, E., Eccles, L., Calvete, Y., McGowan, J., Kelly, P.G., and Correa-Benitez, A. 2010. Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie, 41: 443–450. doi:10.1051/apido/2009076.Google Scholar
Highfield, A.C., El Nagar, A., Mackinder, L.C.M., Noel, L., Hall, M.J., Martin, S.J., et al. 2009. Deformed wing virus implicated in overwintering honeybee colony losses. Applied and Environmental Microbiology, 75: 7212–7220. doi:10.1128/aem.02227-09.Google Scholar
Hou, C., Rivkin, H., Slabezki, Y., and Chejanovsky, N. 2014. Dynamics of the presence of israeli acute paralysis virus in honey bee colonies with colony collapse disorder. Viruses, 6: 2012–2027.Google Scholar
Hunter, W., Ellis, J., van Engelsdorp, D., Hayes, J., Westervelt, D., Glick, E., et al. 2010. Large-scale field application of RNAi technology reducing Israeli acute paralysis virus disease in honey bees (Apis mellifera, Hymenoptera: Apidae). Public Library of Science Pathogens, 6: 1–10. doi:e1001160.Google Scholar
Kojima, Y., Toki, T., Morimoto, T., Yoshiyama, M., Kimura, K., and 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: 895–906. doi:10.1007/s00248-011-9947-z.Google Scholar
Kukielka, D., Perez, A.M., Higes, M., Bulboa, M.D., and Sanchez-Vizcaino, J.M. 2008. Analytical sensitivity and specificity of a RT-PCR for the diagnosis and characterization of the spatial distribution of three Apis mellifera viral diseases in Spain. Apidologie, 39: 607–617. doi:10.1051/apido:2008040.Google Scholar
Locke, B., Forsgren, E., Fries, I., de Miranda, J.R. 2012. Acaricide treatment affects viral dynamics in Varroa destructor-infested honey bee colonies via both host physiology and mite control. Applied and Environmental Microbiology, 78: 227–235. doi:10.1128/aem.06094-11.Google Scholar
Maori, E., Lavi, S., Mozes-Koch, R., Gantman, Y., Peretz, Y., Edelbaum, O., et al. 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: 3428–3438. doi:10.1099/vir.0.83284-0.Google Scholar
Maori, E., Paldi, N., Shafir, S., Kalev, H., Tsur, E., Glick, E., et al. 2009. IAPV, a bee-affecting virus associated with colony collapse disorder can be silenced by dsRNA ingestion. Insect Molecular Biology, 18: 55–60.Google Scholar
Martin, S.J. 2001. The role of varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. Journal of Applied Ecology, 38: 1082–1093.Google Scholar
Martin, S.J., Highfield, A.C., Brettell, L., Villalobos, E.M., Budge, G.E., Powell, M., et al. 2012. Global honey bee viral landscape altered by a parasitic mite. Science, 336: 1304–1306. doi:10.1126/science.1220941.Google Scholar
Neumann, P. and Carreck, N.L. 2010. Honey bee colony losses. Journal of Apicultural Research, 49: 1–6. doi:10.3896/ibra.1.49.1.01.Google Scholar
Palacios, G., Hui, J., Quan, P.L., Kalkstein, A., Honkavuori, K.S., Bussetti, A.V., et al. 2008. Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. Journal of Virology, 82: 6209–6217. doi:10.1128/jvi.00251-08.Google Scholar
Persico, M., Capasso, M., Persico, E., Svelto, M., Russo, R., Spano, D., et al. 2007. Suppressor of cytokine signaling 3 (SOCS3) expression and hepatitis C virus-related chronic hepatitis: insulin resistance and response to antiviral therapy. Hepatology, 46: 1009–1015. doi:10.1002/hep.21782.Google Scholar
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., and Kunin, W.E. 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution, 25: 345–353. doi:10.1016/j.tree.2010.01.007.Google Scholar
Ribiere, M., Ball, B., and Aubert, M. 2008. Natural history and geographical distribution of honey bee viruses. In Virology and the honey bee. Edited by M. Aubert, B. Ball, I. Fries, R.F. Moritz, N. Milani, and I. Bernardinelli. European Communities, Luxembourg, Luxembourg. Pp. 15–84.Google Scholar
Ribiere, M., Triboulot, C., Mathieu, L., Aurieres, C., Faucon, J.P., and Pepin, M. 2002. Molecular diagnosis of chronic bee paralysis virus infection. Apidologie, 33: 339–351. doi:10.1051/apido:2002020.Google Scholar
SAS. 1999. SAS/STAT user's guide. SAS Institute Inc., Cary, North Carolina, United States of America.Google Scholar
Shen, M.Q., Cui, L.W., Ostiguy, N., and Cox-Foster, D. 2005a. 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: 2281–2289. doi:10.1099/vir.0.80824-0.Google Scholar
Shen, M.Q., Yang, X.L., Cox-Foster, D., and Cui, L.W. 2005b. The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology, 342: 141–149. doi:10.1016/j.virol.2005.07.012.Google Scholar
Snedecor, G. and Cochran, W. 1980. Statistical methods. The Iowa State University Press, Ames, Iowa, United States of America.Google Scholar
Stoltz, D., Shen, X.R., Boggis, C., and Sisson, G. 1995. Molecular diagnosis of Kashmir bee virus infection. Journal of Apicultural Research, 34: 153–160.Google Scholar
Tentcheva, D., Gauthier, L., Bagny, L., Fievet, J., Dainat, B., Cousserans, F., et al. 2006. Comparative analysis of deformed wing virus (DWV) RNA in Apis mellifera and Varroa destructor . Apidologie, 37: 41–50. doi:10.1051/apido:2005057.Google Scholar
Tentcheva, D., Gauthier, L., Zappulla, N., Dainat, B., Cousserans, F., Colin, M.E., et al. 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. doi:10.1128/aem.70.12.7185-7191.2004.Google Scholar
Todd, J.H., De Miranda, J.R., and 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. doi:10.1051/apido:2007021.Google Scholar
Underwood, R.M. and vanEngelsdorp, D. 2007. Colony collapse disorder: have we seen this before? Bee Culture, 35: 13–18.Google Scholar
VanEngelsdorp, D., Evans, J.D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B.K., et al. 2009. Colony collapse disorder: a descriptive study. Public Library of Science One, 4: e6481.Google Scholar
VanEngelsdorp, D., Hayes, J. Jr., Underwood, R.M., and Pettis, J. 2008. A survey of honey bee colony losses in the U.S., Fall 2007 to Spring 2008. Public Library of Science One, 3: e4071.Google Scholar
VanEngelsdorp, D. and Meixner, M.D. 2010. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology, 103: 580–595. doi:10.1016/j.jip.2009.06.011.Google Scholar
VanEngelsdorp, D., Underwood, R., Caron, D., and Hayes, J. Jr. 2007. An estimate of managed colony losses in the winter of 2006–2007: a report commissioned by the apiary inspectors of America. American Bee Journal, 147: 599–603.Google Scholar
Welch, B. 1951. On the comparison of several mean values: an alternative approach. Biometrika, 38: 330–336.Google Scholar
Williams, G.R., Rogers, R.E.L., Kalkstein, A.L., Taylor, B.A., Shutler, D., and Ostiguy, N. 2009. Deformed wing virus in western honey bees (Apis mellifera) from Atlantic Canada and the first description of an overtly-infected emerging queen. Journal of Invertebrate Pathology, 101: 77–79. doi:10.1016/j.jip.2009.01.004.Google Scholar