Nationwide Screening for Bee Viruses and Parasites in Belgian Honey Bees.

[en] The health of honey bees is threatened by multiple factors, including viruses and parasites. We screened 557 honey bee (Apis mellifera) colonies from 155 beekeepers distributed all over Belgium to determine the prevalence of seven widespread viruses and two parasites (Varroa sp. and Nosema sp.). Deformed wing virus B (DWV-B), black queen cell virus (BQCV), and sacbrood virus (SBV) were highly prevalent and detected by real-time RT-PCR in more than 95% of the colonies. Acute bee paralysis virus (ABPV), chronic bee paralysis virus (CBPV) and deformed wing virus A (DWV-A) were prevalent to a lower extent (between 18 and 29%). Most viruses were only present at low or moderate viral loads. Nevertheless, about 50% of the colonies harbored at least one virus at high viral load (>10(7) genome copies/bee). Varroa mites and Nosema sp. were found in 81.5% and 59.7% of the honey bee colonies, respectively, and all Nosema were identified as Nosema ceranae by real time PCR. Interestingly, we found a significant correlation between the number of Varroa mites and DWV-B viral load. To determine the combined effect of these and other factors on honey bee health in Belgium, a follow up of colonies over multiple years is necessary.

Disciplines :

Veterinary medicine & animal health

Author, co-author :

Matthijs, Severine

De Waele, Valérie

Vandenberge, Valerie

Verhoeven, Bénédicte

Evers, Jacqueline

Brunain, Marleen

Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appl. aux sc. vétér.

De Winter, Paul J. J.

Roels, Stefan

de Graaf, Dirk C.

De Regge, Nick

Language :

English

Title :

Nationwide Screening for Bee Viruses and Parasites in Belgian Honey Bees.

Publication date :

2020

Journal title :

Viruses

eISSN :

1999-4915

Publisher :

Multidisciplinary Digital Publishing Institute (MDPI), Switzerland

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 03 September 2020

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Bibliography

Jacques, A.; Laurent, M.; Ribière-Chabert, M.; Saussac, M.; Bougeard, S.; Budge, G.E.; Hendrikx, P.; Chauzat, M.P. A pan-European epidemiological study reveals honey bee colony survival depends on beekeeper education and disease control. PLoS ONE 2017. [CrossRef] [PubMed]
Genersch, E.; Von Der Ohe, W.; Kaatz, H.; Schroeder, A.; Otten, C.; Büchler, R.; Berg, S.; Ritter, W.; Mühlen, W.; Gisder, S.; et al. The German bee monitoring project: A long term study to understand periodically high winter losses of honey bee colonies. Apidologie 2010, 41, 332-352. [CrossRef]
Porrini, C.; Mutinelli, F.; Bortolotti, L.; Granato, A.; Laurenson, L.; Roberts, K.; Gallina, A.; Silvester, N.; Medrzycki, P.; Renzi, T.; et al. The status of honey bee health in Italy: Results from the nationwide bee monitoring network. PLoS ONE 2016, 11, 1-22. [CrossRef] [PubMed]
Charrière, J.D.; Neumann, P. Surveys to estimate winter losses in Switzerland. J. Apic. Res. 2010, 49, 132-133. [CrossRef]
Spleen, A.M.; Lengerich, E.J.; Rennich, K.; Caron, D.; Rose, R.; Pettis, J.S.; Henson, M.; Wilkes, J.T.; Wilson, M.; Stitzinger, J.; et al. A national survey of managed honey bee 2011-12 winter colony losses in the United States: Results from the Bee Informed Partnership. J. Apic. Res. 2013, 52, 44-53. [CrossRef]
Highfield, A.C.; El Nagar, A.; Mackinder, L.C.M.; Noël, L.M.L.J.; Hall, M.J.; Martin, S.J.; Schroeder, D.C. Deformed wing virus implicated in overwintering honeybee colony losses. Appl. Environ. Microbiol. 2009. [CrossRef]
Berthoud, H.; Imdorf, A.; Haueter, M.; Radloff, S.; Neumann, P. Virus infections and winter losses of honey bee colonies (Apis mellifera). J. Apic. Res. 2010, 49, 60-65. [CrossRef]
Iqbal, J.; Mueller, U. Virus infection causes specific learning deficits in honeybee foragers. Proc. R. Soc. B Biol. Sci. 2007, 274, 1517-1521. [CrossRef]
McMenamin, A.J.; Genersch, E. Honey bee colony losses and associated viruses. Curr. Opin. Insect Sci. 2015. [CrossRef]
Dainat, B.; Evans, J.D.; Chen, Y.P.; Gauthier, L.; Neumanna, P. Dead or alive: Deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Appl. Environ. Microbiol. 2012, 78, 981-987. [CrossRef]
Beaurepaire, A.; Piot, N.; Doublet, V.; Antunez, K.; Campbell, E.; Chantawannakul, P.; Chejanovsky, N.; Gajda, A.; Heerman, M.; Panziera, D.; et al. Diversity and Global Distribution of Viruses of the Western Honey Bee, Apis mellifera. Insects 2020, 11, 239. [CrossRef] [PubMed]
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.; et al. Standard methods for virus research in Apis mellifera. J. Apic. Res. 2013, 52, 1-56. [CrossRef]
Chen, Y.; Evans, J.; Feldlaufer, M. Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J. Invertebr. Pathol. 2006, 92, 152-159. [CrossRef] [PubMed]
Amiri, E.; Meixner, M.D.; Kryger, P. Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Sci. Rep. 2016, 6, 1-7. [CrossRef] [PubMed]
Chen, Y.; Pettis, J.S.; Evans, J.D.; Kramer, M.; Feldlaufer, M.F. Transmission of Kashmir bee virus by the ectoparasitic mite Varroa destructor. Apidologie 2004, 35, 441-448. [CrossRef]
Shen, M.; Yang, X.; Cox-Foster, D.; Cui, L. The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology 2005, 342, 141-149. [CrossRef]
Gisder, S.; Aumeier, P.; Genersch, E. Deformed wing virus: Replication and viral load in mites (Varroa destructor). J. Gen. Virol. 2009, 90, 463-467. [CrossRef]
Di Prisco, G.; Pennacchio, F.; Caprio, E.; Boncristiani, H.F.; Evans, J.D.; Chen, Y. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J. Gen. Virol. 2011, 92, 151-155. [CrossRef]
Ball, B.V.; Allen, M.F. The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni. Ann. Appl. Biol. 1988, 113, 237-244. [CrossRef]
Bowen-Walker, P.L.; Martin, S.J.; Gunn, A. The Transmission of Deformed Wing Virus between Honeybees (Apis mellifera L.) by the Ectoparasitic Mite Varroa jacobsoni Oud. J. Invertebr. Pathol. 1999, 73, 101-106. [CrossRef]
Genersch, E. Honey bee pathology: Current threats to honey bees and beekeeping. Appl. Microbiol. Biotechnol. 2010, 87, 87-97. [CrossRef] [PubMed]
Ramsey, S.D.; Ochoa, R.; Bauchan, G.; Gulbronson, C.; Mowery, J.D.; Cohen, A.; Lim, D.; Joklik, J.; Cicero, J.M.; Ellis, J.D.; et al. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc. Natl. Acad. Sci. USA 2019, 116, 1792-1801. [CrossRef] [PubMed]
Al Naggar, Y.; Paxton, R.J. Mode of Transmission Determines the Virulence of Black Queen Cell Virus in Adult Honey Bees, Posing a Future Threat to Bees and Apiculture. Viruses 2020, 12, 535. [CrossRef] [PubMed]
Chapter 3.2.4. Nosemosis of honey bees. In OIE Terrestrial Manual; 2018; p. 1833. Available online: https://www.oie.int/standard-setting/terrestrial-manual/access-online/ (accessed on 14 August 2020).
Toplak, I.; Jamnikar Ciglenečki, U.; Aronstein, K.; Gregorc, A. Chronic bee paralysis virus and Nosema ceranae experimental co-infection of winter honey bee workers (Apis mellifera L.). Viruses 2013, 5, 2282-2297. [CrossRef] [PubMed]
Doublet, V.; Natsopoulou, M.E.; Zschiesche, L.; Paxton, R.J. Within-host competition among the honey bees pathogens Nosema ceranae and Deformed wing virus is asymmetric and to the disadvantage of the virus. J. Invertebr. Pathol. 2015, 124, 31-34. [CrossRef] [PubMed]
Doublet, V.; Labarussias, M.; de Miranda, J.R.; Moritz, R.F.A.; Paxton, R.J. Bees under stress: Sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ. Microbiol. 2015, 17, 969-983. [CrossRef]
Nguyen, B.K.; Ribière, M.; VanEngelsdorp, D.; Snoeck, C.; Saegerman, C.; Kalkstein, A.L.; Schurr, F.; Brostaux, Y.; Faucon, J.-P.; Haubruge, E. Effects of honey bee virus prevalence, Varroa destructor load and queen condition on honey bee colony survival over the winter in Belgium. J. Apic. Res. 2011, 50, 195-202. [CrossRef]
De Smet, L.; Ravoet, J.; de Miranda, J.R.; Wenseleers, T.; Mueller, M.Y.; Moritz, R.F.A.; de Graaf, D.C. BeeDoctor, a Versatile MLPA-Based Diagnostic Tool for Screening Bee Viruses. PLoS ONE 2012, 7, e47953. [CrossRef]
Forsgren, E.; Locke, B.; Semberg, E.; Laugen, A.T.; de Miranda, J.R. Sample preservation, transport and processing strategies for honeybee RNA extraction: Influence on RNA yield, quality, target quantification and data normalization. J. Virol. Methods 2017, 246, 81-89. [CrossRef]
Ciglenečki, U.J.; Toplak, I. Development of a real-time RT-PCR assay with TaqMan probe for specific detection of acute bee paralysis virus. J. Virol. Methods 2012, 184, 63-68. [CrossRef]
Chantawannakul, P.; Ward, L.; Boonham, N.; Brown, M. 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. J. Invertebr. Pathol. 2006, 91, 69-73. [CrossRef] [PubMed]
Blanchard, P.; Ribière, M.; Celle, O.; Lallemand, P.; Schurr, F.; Olivier, V.; Iscache, A.L.; Faucon, J.P. Evaluation of a real-time two-step RT-PCR assay for quantitation of Chronic bee paralysis virus (CBPV) genome in experimentally-infected bee tissues and in life stages of a symptomatic colony. J. Virol. Methods 2007, 141, 7-13. [CrossRef] [PubMed]
Schurr, F.; Tison, A.; Militano, L.; Cheviron, N.; Sircoulomb, F.; Rivière, M.P.; Ribière-Chabert, M.; Thiéry, R.; Dubois, E. Validation of quantitative real-time RT-PCR assays for the detection of six honeybee viruses. J. Virol. Methods 2019, 270, 70-78. [CrossRef] [PubMed]
Ward, L.; Waite, R.; Boonham, N.; Fisher, T.; Pescod, K.; Thompson, H.; Chantawannakul, P.; Brown, M. First detection of Kashmir bee virus in the UK using real-time PCR. Apidologie 2007, 38, 181-190. [CrossRef]
Blanchard, P.; Guillot, S.; Antùnez, K.; Köglberger, H.; Kryger, P.; de Miranda, J.R.; Franco, S.; Chauzat, M.P.; Thiéry, R.; Ribière, M. Development and validation of a real-time two-step RT-qPCR TaqMan® assay for quantitation of Sacbrood virus (SBV) and its application to a field survey of symptomatic honey bee colonies. J. Virol. Methods 2014, 197, 7-13. [CrossRef] [PubMed]
Chen, Y.P.; Higgins, J.A.; Feldlaufer, M.F. Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.). Appl. Environ. Microbiol. 2005, 71, 436-441. [CrossRef] [PubMed]
Chen, Y.; Evans, J.D.; Zhou, L.; Boncristiani, H.; Kimura, K.; Xiao, T.; Litkowski, A.M.; Pettis, J.S. Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J. Invertebr. Pathol. 2009, 101, 204-209. [CrossRef]
Traynor, K.S.; Rennich, K.; Forsgren, E.; Rose, R.; Pettis, J.; Kunkel, G.; Madella, S.; Evans, J.; Lopez, D.; vanEngelsdorp, D. Multiyear survey targeting disease incidence in US honey bees. Apidologie 2016, 47, 325-347. [CrossRef]
Ravoet, J.; De Smet, L.; Wenseleers, T.; de Graaf, D.C. Vertical transmission of honey bee viruses in a Belgian queen breeding program. BMC Vet. Res. 2015, 11. [CrossRef]
Schittny, D.; Yañez, O.; Neumann, P. Honey Bee Virus Transmission via Hive Products. Vet. Sci. 2020, 7, 96. [CrossRef]
Mutinelli, F. The spread of pathogens through trade in honey bees and their products (including queen bees and semen): Overview and recent developments. Rev. Sci. Tech. l'OIE 2011, 30, 257-271. [CrossRef] [PubMed]
Shen, M.; Cui, L.; Ostiguy, N.; Cox-Foster, D. Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and Sacbrood virus) with the honeybee host and the parasitic Varroa mite. J. Gen. Virol. 2005, 86, 2281-2289. [CrossRef] [PubMed]
Ravoet, J.; De Smet, L.; Meeus, I.; Smagghe, G.; Wenseleers, T.; de Graaf, D.C. Widespread occurrence of honey bee pathogens in solitary bees. J. Invertebr. Pathol. 2014. [CrossRef] [PubMed]
Genersch, E.; Yue, C.; Fries, I.; De Miranda, J.R. Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J. Invertebr. Pathol. 2006, 91, 61-63. [CrossRef] [PubMed]
Bailes, E.J.; Deutsch, K.R.; Bagi, J.; Rondissone, L.; Brown, M.J.F.; Owen, T. First detection of honey bee viruses in hoverfly (syrphid) pollinators. Biol. Lett. 2016, 14, 20180001. [CrossRef] [PubMed]
Yang, X.; Cox-Foster, D.L. Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification. Proc. Natl. Acad. Sci. USA 2005, 102, 7470-7475. [CrossRef]
Tentcheva, D.; Gauthier, L.; Zappulla, N.; Dainat, B.; Cousserans, F.; Colin, M.E.; Bergoin, M. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl. Environ. Microbiol. 2004, 70, 7185-7191. [CrossRef]
Biesmeijer, K. Report Honeybee Surveillance Program the Netherlands. Naturalis 2016.
Amiri, E.; Meixner, M.; Nielsen, S.L.; Kryger, P. Four categories of viral infection describe the health status of honey bee colonies. PLoS ONE 2015, 10, 10-12. [CrossRef]
Benaets, K.; Van Geystelen, A.; Cardoen, D.; De Smet, L.; de Graaf, D.C.; Schoofs, L.; Larmuseau, M.H.D.; Brettell, L.E.; Martin, S.J.; Wenseleers, T. Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival. Proc. R. Soc. B Biol. Sci. 2017, 284. [CrossRef]
McMenamin, A.J.; Flenniken, M.L. Recently identified bee viruses and their impact on bee pollinators. Curr. Opin. Insect Sci. 2018. [CrossRef]
Natsopoulou, M.E.; McMahon, D.P.; Doublet, V.; Frey, E.; Rosenkranz, P.; Paxton, R.J. The virulent, emerging genotype B of Deformed wing virus is closely linked to overwinter honeybee worker loss. Sci. Rep. 2017, 7, 1-9. [CrossRef] [PubMed]
Ravoet, J.; Maharramov, J.; Meeus, I.; De Smet, L.; Wenseleers, T.; Smagghe, G.; de Graaf, D.C. Comprehensive Bee Pathogen Screening in Belgium Reveals Crithidia mellificae as a New Contributory Factor to Winter Mortality. PLoS ONE 2013, 8. [CrossRef] [PubMed]
Milbrath, M.O.; van Tran, T.; Huang, W.F.; Solter, L.F.; Tarpy, D.R.; Lawrence, F.; Huang, Z.Y. Comparative virulence and competition between Nosema apis and Nosema ceranae in honey bees (Apis mellifera). J. Invertebr. Pathol. 2015, 125, 9-15. [CrossRef] [PubMed]
Natsopoulou, M.E.; McMahon, D.P.; Doublet, V.; Bryden, J.; Paxton, R.J. Interspecific competition in honeybee intracellular gut parasites is asymmetric and favours the spread of an emerging infectious disease. Proc. R. Soc. B Biol. Sci. 2015, 282. [CrossRef] [PubMed]