A survey of deformed wing virus and acute bee paralysis virus in honey bee colonies from serbia using real-time RT-PCR

Simeunović, Predrag; Stevanović, Jevrosima; Vidanović, Dejan; Nišavić, Jakov; Radović, Dejan; Stanišić, Ljubodrag; Stanimirović, Zoran

doi:10.2478/acve-2014-0009

Abstract

In this study 55 honey bee colonies from different Serbian regions were monitored for the presence of Deformed Wing Virus (DWV) and Acute Bee Paralysis Virus (ABPV) using TaqMan-based real-time RT-PCR assay. The results revealed the presence of DWV in each sampling location, and ABPV in 10 out of 11 apiaries. High frequency of DWV (76.4%) and ABPV (61.8%) positive samples in asymptomatic colonies can be the consequence of inefficient and postponed Varroa treatment concerning the role of this mite in the transmission and activation of honey bee viruses. The real-time RTPCR technique described in this paper is proved to be the most reliable method for this kind of investigation.

References

1. Genersch E, Aubert M: Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet Res 2010, 41:54.10.1051/vetres/2010027
Search in Google Scholar
2. Chen YP, Siede R: Honey bee viruses. Adv Virus Res 2007, 70:33-80.10.1016/S0065-3527(07)70002-7
Search in Google Scholar
3. Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C, Büchler R, Berg S, Ritter W, Mühlen W, Gisder S, Meixner M, Liebig G, Rosenkranz P: The German bee monitoring project: a long term study to understand periodically high winter losses of honeybee colonies. Apidologie 2010a, 41:332-352.10.1051/apido/2010014
Search in Google Scholar
4. Bailey L, Ball BV, Perry JN: The prevalence of viruses of honey bees in Britain. Ann Appl Biol 1981, 97:109-118.10.1111/j.1744-7348.1981.tb02999.x
Search in Google Scholar
5. Evans JD, Hung AC: Molecular phylogenetics and the classifi cation of honey bee viruses. Arch Virol 2000, 145:2015-2026.10.1007/s00705007003711087089
Search in Google Scholar
6. Gauthier L, Tentcheva D, Tournaire M, Dainat B, Cousserans F, Colin ME, Bergoin M: Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique. Apidologie 2007, 38:426-435.10.1051/apido:2007026
Search in Google Scholar
7. Highfi eld AC, El Nagar A, Mackinder LC, Laure MLN, Hall MJ, Martin SJ, Schroeder DC: Deformed wing virus implicated in overwintering honeybee colony losses. Appl Environ Microb 2009,75:7212-722010.1128/AEM.02227-09278654019783750
Search in Google Scholar
8. Lanzi G, De Miranda JR, Boniotti MB, Cameron CE, Lavazza A, Capucci L, Camazine SM, Rossi C: Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.). J Virol 2006, 80:4998-5009.10.1128/JVI.80.10.4998-5009.2006147207616641291
Search in Google Scholar
9. Knowles NJ, Hovi T, Hyypiä T, King AMQ, Lindberg AM, Pallansch MA, Palmenberg AC, Simmonds P, Skern T, Stanway G, Yamashita T, Zell R: Picornaviridae. In: Virus Taxonomy: Classifi cation and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses. Ed: King AMQ, Adams MJ, Carstens EB, Lefkowitz, EJ. San Diego: Elsevier; 2012, 855-880.
Search in Google Scholar
10. Adams MJ, Lefkowitz EJ, King AMQ, Carstens EB: Recently agreed changes to the statutes of the international committee on taxonomy of viruses. Arch Virol 2013, 1-6.10.1007/s00705-013-1748-x23836392
Search in Google Scholar
11. Nordström S: Distribution of deformed wing virus within honey bee (Apis mellifera) brood cells infested with the ectoparasitic mite Varroa destructor. Exp Appl Acarol 2003, 29:293-302.
Search in Google Scholar
12. Tentcheva D, Gauthier L, Jouve S, Canabady- Rochelle L, Dainat B, Cousserans F, Colin ME, Ball BV, Bergoin M: Prevalence and seasonal variations of six bee viruses in Api smellifera L. and Varroa destructor mite populations in France. Appl Environ Microb 2004, 70:7185-7191.10.1128/AEM.70.12.7185-7191.200453517015574916
Search in Google Scholar
13. Berenyi O, Bakonyi T, Derakhshifar I, Köglberger H, Nowotny N: Occurence of six honeybee viruses in diseased Austrian apiaries. Appl Environ Microb 2006, 72:2414-2420.10.1128/AEM.72.4.2414-2420.2006144902716597939
Search in Google Scholar
14. Chantawannakul P, Ward L, Boonham N, Brown M: A scientifi c note on the detection of honeybee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Tai honeybee (Apis mellifera) apiary. J Invertebr Pathol 2006, 91:69-73.10.1016/j.jip.2005.11.00116376930
Search in Google Scholar
15. Forgách P, Bakonyi T, Tapaszti S, Nowotny N, Rusvai M: Prevalence of pathogenic bee viruses in Hungarian apiaries: situation before joining the European Union, J Invertebr Pathol 2008, 98:235-238.10.1016/j.jip.2007.11.00218155230
Search in Google Scholar
16. Ribière M, Ball BV, Aubert M: Natural history and geographic distribution of honey bee viruses, in: Aubert M, Ball BV, Fries I, Moritz RFA, Milani N, Bernardinelli I: Virology and the honey bee, European Communities, Luxembourg: 2008, 15-84.
Search in Google Scholar
17. Williams GR, Rogers REL, Kalkstein AL, Taylor BA, Shutler D, Ostiguy N: Deformed wing virus in western honey bees (Apis mellifera) from Atlantic Canada and the fi rst description of an overtly infected emerging queen. J Invertebr Pathol 2009, 101:77-79.10.1016/j.jip.2009.01.00419373971
Search in Google Scholar
18. Ai H, Yan X, Han R: Occurrence and prevalence of seven bee viruses in Apismellifera and Apis cerana apiaries in China. J Invertebr Pathol 2012, 109:160-164.10.1016/j.jip.2011.10.00622062807
Search in Google Scholar
19. Chen Y, Evans J, Feldlaufer M: Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J Invertebr Pathol 2006, 92:152-159.10.1016/j.jip.2006.03.01016793058
Search in Google Scholar
20. Forsgren E, de Miranda JR, Isaksson M: Deformed wing virus associated with Tropilaelaps mercedesae infesting European honey bees (Apis mellifera). Exp Appl Acarol 2009, 47:87-97.10.1007/s10493-008-9204-418941909
Search in Google Scholar
21. Yue C, Schröder M, Bienefeld K, Genersch E: Detection of viral sequences in semen of honeybees (Apis mellifera): evidence for vertical transmission of viruses through drones. J Invertebr Pathol 2006, 92:105-108.10.1016/j.jip.2006.03.00116630626
Search in Google Scholar
22. Yue C, Schröder M, Gisder S, Genersch E: Vertical transmission routes for deformed wing virus of honeybees (Apis mellifera). J Gen Virol 2007, 88:2329-2336.10.1099/vir.0.83101-017622639
Search in Google Scholar
23. de Miranda JR, Fries I: Venereal and vertical transmission of deformed wing virus in honey bees (Apis mellifera L.). J Invertebr Pathol 2008, 98:184-189. 10.1016/j.jip.2008.02.00418358488
Search in Google Scholar
24. Möckel N, Gisder S, Genersch E: Horizontal transmission of deformed wing virus: Pathological consequences in adult bees (Apis mellifera) depend on the transmission route. J Gen Virol 2011, 92:370-377.10.1099/vir.0.025940-020965988
Search in Google Scholar
25. Yang X, Cox-Foster D: Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology 2007, 134:405.10.1017/S003118200600071017078903
Search in Google Scholar
26. Bailey L, Ball BV: 1991. Honeybee pathology. Academic Press, London, United Kingdom.
Search in Google Scholar
27. Gisder S, Aumeier P, Genersch E: Deformed wing virus (DWV): viral load and replication in mites (Varroa destructor). J Gen Virol 2009, 90:463-467.10.1099/vir.0.005579-019141457
Search in Google Scholar
28. de Miranda J, Genersch E: Deformed wing virus. J Invertebr Pathol 2010, 103:48-61.10.1016/j.jip.2009.06.01219909976
Search in Google Scholar
29. Allen MF, Ball BV: The incidence and world distribution of honey bee viruses. Bee World 1996, 77:141-162.10.1080/0005772X.1996.11099306
Search in Google Scholar
30. Ellis JD, Munn PA: The worldwide health status of honey bees. Bee World 2005, 86:88-101.10.1080/0005772X.2005.11417323
Search in Google Scholar
31. Hung ACF, Ball BV, Adams JR, Shimanuki H, Knox DA: A scientifi c note on the detection of American strains of acute paralysis virus and Kashmir bee virus in dead bees in one US honey bee (Apis mellifera L.) colony. Apidologie 1996, 27:55-56.10.1051/apido:19960107
Search in Google Scholar
32. Békési L, Ball BV, Dobos-Kovács M, Bakonyi T, Rusvai M: Occurrence of acute paralysis virus of the honey bee (Apis mellifera) in a Hungarian apiary infested with the parasitic mite Varroa jacobsoni. Acta Vet Hung 1999, 47:319-324.10.1556/avet.47.1999.3.5
Search in Google Scholar
33. Siede R, König M, Büchler R, Failing K, Thiel HJ: A real-time PCR based survey on acute bee paralysis virus in German bee colonies, Apidologie 2008, 39:650-661.10.1051/apido:2008044
Search in Google Scholar
34. Allen MF and Ball BV: Characterization and serological relationships of strains of Kashmir bee virus. Ann Appl Biol 1995, 126:471-484.10.1111/j.1744-7348.1995.tb05382.x
Search in Google Scholar
35. Anderson DL: A comparison of serological techniques for detecting and identifying honeybee viruses. J Invertebr Pathol 1984, 44:233-243.10.1016/0022-2011(84)90019-3
Search in Google Scholar
36. Benjeddou M, Leat N, Allsopp M, Davison S: Detection of acute bee paralysis virus and black queen cell virus from honeybees by reverse transcriptase PCR. Appl Environ Microb 2001 67:2384-2387.10.1128/AEM.67.5.2384-2387.20019288411319129
Search in Google Scholar
37. Kukielka D, Esperón F, Higes M, Sánchez-Vizcaíno JM: A sensitive one-step real-time RTPCR method for detection of deformed wing virus and black queen cell virus in honeybee Apis mellifera. J Virol Methods 2008, 147:275-281.10.1016/j.jviromet.2007.09.00817964669
Search in Google Scholar
38. Nielsen SL, Nicolaisen M, Kryger P: 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 2008, 39:310-314.10.1051/apido:2008007
Search in Google Scholar
39. Jamnikar Ciglenečki U, Toplak I: Development of a real-time RT-PCR assay with TaqMan probe for specifi c detection of acute bee paralysis virus. J Virol Methods 2012, 184:63-68.10.1016/j.jviromet.2012.05.01022609890
Search in Google Scholar
40. de Miranda JR, Cordoni G, Budge G: The acute bee paralysis virus-Kashmir bee virus- Israeli acute paralysis virus complex. J Invertebr Pathol 2010, 10:30-47.10.1016/j.jip.2009.06.01419909972
Search in Google Scholar
41. Stevanovic J, Stanimirovic Z, Genersch E, Kovacevic RS, Ljubenkovic J, Radakovic M, Aleksic N: Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie 2011, 41:49-58.10.1051/apido/2010034
Search in Google Scholar
42. Stevanovic J, Simeunovic P, Gajic B, Lakic N, Radovic D, Fries I, Stanimirovic Z: Characteristics of Nosema ceranae infection in Serbian honey bee colonies. Apidologie 2013, 44:522-536. 10.1007/s13592-013-0203-z
Search in Google Scholar
43. Stanimirović Z, Aleksić N, Stevanović J, Ćirković D, Mirilović M, Đelić N, Stojić V: The infl uence of pulverised sugar dusting on the degree of infestation of honey bee colonies with Varroa destructor. Acta Vet-Beograd 2011, 61:309-325.10.2298/AVB1103309S
Search in Google Scholar
44. Gajic B, Radulovic Z, Stevanovic J, Kulisic Z, Vucicevic M, Simeunovic P, Stanimirovic Z: Variability of the honey bee mite Varroa destructor in Serbia based on mtDNA analysis. Exp Appl Acarol 2013, 61:97-105.10.1007/s10493-013-9683-923471517
Search in Google Scholar
45. Kulinčević J, Ball B, Mladjan V: Viruses in honey bee colonies infested with Varroa jacobsoni: fi rst fi ndings in Yugoslavia. Acta Vet-Beograd 1990, 40:37-42.
Search in Google Scholar
46. Petrovic T, Vidanovic D, Stojanov I, Lupulovic D, Lazic G: First molecular detection of six honeybee viruses in Serbian apiaries. Proceedings, 10th International Symposium Modern Trends in Livestock Production, Belgrade, 2 - 4 October, 2013, Institute for Animal Husbandry, Belgrade 2013, 627:639.
Search in Google Scholar
47. Toplak I, Rihtarič D, Ciglenečki UJ, Hostnik P, Jenčič V, Barlič-Maganja D: Detection of six honeybee viruses in clinically affected colonies of Carniolan gray bee (Apis mellifera carnica). Slov Vet Res 2012, 49:89-96.
Search in Google Scholar
48. Mackay, IM: Real-time PCR in the microbiology laboratory. Clin Microbiol Infec 2004, 10:190-212.10.1111/j.1198-743X.2004.00722.x
Search in Google Scholar
49. ANSES: French Agency for Food, Environmental and Occupational Health & Safety Screening for several honeybee viruses using PCR (in-house method) (ABPV, IAPV, KBV, DWV, SBV, BQCV, CBPV). 2011, http://www.anses.fr/en.
Search in Google Scholar
50. Antúnez K, D’Alessandro B, Corbella E, Ramallo G, Zunino P: Honeybee viruses in Uruguay. J Invertebr Pathol 2006, 93:67-70.10.1016/j.jip.2006.05.00916843485
Search in Google Scholar
51. Runckel C, Flenniken ML, Engel JC, Ruby JG, Ganem D, Andino R, DeRisi JL: Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One 2011, 6:e20656.10.1371/journal.pone.0020656311020521687739
Search in Google Scholar
52. Choe SE, Nguyen LTK, Noh JH, Koh HB, Jean YH, Kweon CH, Kang SW: Prevalence and distribution of six bee viruses in Korean Apis cerana populations. J Invertebr Pathol 2012, 109:330-333.10.1016/j.jip.2012.01.00322273697
Search in Google Scholar
53. Chen Y, Zhao Y, Hammond J, Hsu HT, Evans J, Feldlaufer M: Multiple virus infections in the honey bee and genome divergence of honey bee viruses. J Invertebr Pathol 2004, 87:84-93.10.1016/j.jip.2004.07.00515579317
Search in Google Scholar
54. Antúnez K, Anido M, Garrido-Bailon E, Botias C, Zunino P, Martínez-Salvador A, Higes M: Low prevalence of honeybee viruses in Spain during 2006 and 2007. Res Vet Sci 2012, 93:1441-1445.10.1016/j.rvsc.2012.03.00622513127
Search in Google Scholar
55. Grabensteiner E, Ritter W, Carter MJ, Davison S, Pechhacker H, Kolodziejek J, Boecking O, Derakshhifar I, Moosbeckhofer R, Licek E, Nowotny N: Sacbrood virus of the honeybee (Apis mellifera): rapid identifi cation and phylogenetic analysis using reverse transcription- PCR. Clin Diagn Lab Immun 2001, 8:93-104.10.1128/CDLI.8.1.93-104.20019601611139201
Search in Google Scholar
56. Kukielka D, Sánchez-Vizcaíno JM: One-step real-time quantitative PCR assays for the detection and fi eld study of Sacbrood honeybee and Acute bee paralysis viruses. J Virol Methods 2009, 161:240-246.10.1016/j.jviromet.2009.06.01419559729
Search in Google Scholar
57. Blanchard P, Ribière M, Celle O, Lallemand P, Schurr F, Olivier V, Iscache AL, Faucon JP: 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. 10.1016/j.jviromet.2006.11.02117166598
Search in Google Scholar

A survey of deformed wing virus and acute bee paralysis virus in honey bee colonies from serbia using real-time RT-PCR

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