Invertebrate Microbiology

Prevalence and Seasonal Variations of Six Bee Viruses in Apis mellifera L. and Varroa destructor Mite Populations in France

Diana Tentcheva, Laurent Gauthier, Nathalie Zappulla, Benjamin Dainat, François Cousserans, Marc Edouard Colin, Max Bergoin
DOI: 10.1128/AEM.70.12.7185-7191.2004

Article Figures & Data

Figures

  • FIG. 1.
    FIG. 1.

    Distribution of the 36 apiaries where samples were collected in France. The reference numbers of the apiaries are indicated.

  • FIG. 2.
    FIG. 2.

    Frequencies of bee virus infections in samples of adult bees (A) and pupae (B) collected from 360 colonies. The data are expressed as percentages. The detection of DWV, SBV, CBPV, ABPV, BQCV, or KBV in the spring, summer, and autumn in the same colony is referred to as stable. Viral infections that were detected once or twice during the year in the same colony are referred to as variable. Not detected refers to colonies in which virus was not detected at any time of the year.

  • FIG. 3.
    FIG. 3.

    Percentages of apiaries in which 0 to 10 colonies were infected by DWV, SBV, BQCV, or ABPV at the adult or larval stage.

  • FIG. 4.
    FIG. 4.

    Seasonal variation of viral infection rates in honey bee colonies.

  • FIG. 5.
    FIG. 5.

    Prevalence of viral infections in V. destructor samples.

Tables

  • TABLE 1.

    Primers used for PCR diagnosis

    VirusForward primerReverse primerLength (bp)aReference
    DWVTTTGCAAGATGCTGTATGTGGGTCGTGCAGCTCGATAGGAT39530
    SBVGGATGAAAGGAAATTACCAGCCACTAGGTGATCCACACT426
    CBPVAGTTGTCATGGTTAACAGGATACGAGTCTAATCTTAGCACGAAAGCCGAG45527
    ABPVTGAGAACACCTGTAATGTGGACCAGAGGGTTGACTGTGTG452
    BQCVGGACGAAAGGAAGCCTAAACACTAGGAAGAGACTTGCACC424
    KBVGATGAACGTCGACCTATTGATGTGGGTTGGCTATGAGTCA39329
    TMVbAAAAACAGTCCCCAACTTCCAAGGAGGATTCTCTCGCTGT600

    • ↵a Length of DNA fragment amplified.

    • ↵b TMV, tobacco mosaic virus.

  • TABLE 2.

    Seasonal variation of DWV, SBV, ABPV, BQCV, CBPV, and KBV in bee and Varroa samples from 36 apiaries

    ApiaryRegionaDWVSBVCBPVABPVBQCVKBV
    Adults, springAdults, summerAdults, autumnPupae, springPupae, summerPupae, autumnVarroacAdults, springAdults, summerAdults, autumnPupae, springPupae, summerPupae, autumnVarroacAdults, springAdults, summerAdults, autumnPupae, springPupae, summerPupae, autumnVarroacAdults, springAdults, summerAdults, autumnPupae, springPupae, summerPupae, autumnVarroacAdults, springAdults, summerAdults, autumnPupae, springPupae, summerPupae, autumnVarroacAdults, springAdults, summerAdults, autumnPupae, springPupae, summerPupae, autumnVarroac
    910AL−b−+−−−++++++−−−−−−−−−−−+−−−+−−−−−−−−−−−−−−
    333AQ+++−++NA−+−−+−NA−−−−−−NA−−+−−−NA−++−+−NA−−−−−−NA
    497AQ++++++++++++−+−−+−−−−−−−−−−−−−−−−−−−−−−−−−
    878AQ++++++++++++−+−−−−−−−−−−−−−−++−−−−−−−−−−−−
    855AU++++−−+−++−+−+−−−−−−−−−−−−−−+++−−−−−−−−−−−
    649AU+++−+++−++−−+−+−−−−−−−+−++−+−++−−−−−−−−−−−
    208BN+++++++−++−+−+−+−−−−−−++−−−−+++−−−−−−−−−−−
    426BR+++++−+−−−−−−−+−+−−−−−−−−−−−+−−−−−−−−−−−−−
    429BR−−−−−−NA−−−−−−NA−−−−−−NA−−−−−−NA−−−−−−NA−−−−−−NA
    150CA+++−+++−−−−−−−−−−−−−−−−−−−−−+++−−−−−−−−−−−
    746CA+++++++−++−−−−−−−−−−−−+−−+++−++−−−−−−−−−−−
    751CA+++++++−++−+−−++−−−−−−+−−−−−+++−+−−−−−−−−−
    624CE++++++NA++−+−−NA−−+−−−NA−+−−+−NA+++−−−NA−−−−−−NA
    413CE++++++++++−+++−−−−−−−−−−−−−−+++−−−−−−−−−−−
    1005HN++++++++++−−−−−−−−−−−−++−−−−+++−−−−−−−−−−−
    802LO+++−−++++−++−+−−−−−−−−−+−+−++++−−−−−−−−−−
    702LR−++−++NA−−−−−−NA−−+−−−NA−−−−−−NA−−−−−−NA−−−−−−NA
    900LR+++−++++++−+−−−−−−−−−−−−−−−−+++−−−−++−−+−−
    125MP++++++++++++++−−−−−−−−−−−−−−+++−−−−−−−−−−−
    1051MP+++−−+++++−+−−−−−−−−−−−−−−−−+++−+−−−−−−−−−
    1049MP+++−−−NA++−++−NA−−−−−−NA−−−−−−NA+++−−−NA−−−−−−NA
    137MP++++++NA++−+−−NA−−−−−−NA−−−−−−NA+−−−−−NA−−−−−−NA
    814NO+++++NANA−−−−−NANA−++−−NANA−++−−NANA−−−−−NANA−−−−−NANA
    1182PA+−+−++++++++++−−−−−−−−++−++++++−+−−+++−+++
    1196PA+++−−+++++−−−−−−−−−−−−+−−−−−+++−−−−−−−−−−−
    242PC++++++++++−+−−+−+−−−−−−−−−−−+++−−−−−−−−−−−
    28PI++++++++++++−+−−−−−−−+++−−+++++−+−−−−−−−−−
    727PL+++−+++−++−−++−−+−−−−+++−−−+++−−+−−−−−−−−−
    355RA+++−+−NA+++++−NA−−−−−−NA−++−−−NA+++−−−NA+++−−−NA
    626RA+++−++NA++++++NA−−−−−−NA+−−−−−NA+++−−−NA−−−−−−NA
    380RA++++++NA+++++−NA−−−−−−NA++−−−−NA+++−−−NA−−−−−−NA
    992RA++++++NA++−+−−NA−−−−−−NA−++−+−NA++++−−NA−−−−−−NA
    591RA+++−++NA++++++NA−−−−−−NA−−−−−−NA+++−+−NA+++−−−NA
    585RA++++++NA+++−+−NA−−−−−−NA−−+−−−NA+++−−−NA+++−−−NA
    106RA+++++++++−++−−−−−−−−−+++−−+++++−−−−−−−−−−−
    934RA++++++NA+++++−NA−−−−−−NA−−+−−−NA+++−−−NA+++−−−NA
    No. (%) of positive apiaries33 (92)33 (92)35 (97)20 (56)29 (81)29 (83)22 (100)24 (67)31 (86)24 (67)17 (47)23 (64)7 (20)10 (45)4 (11)3 (8)7 (19)00005 (14)15 (42)14 (39)1 (3)6 (17)4 (11)8 (36)28 (78)29 (81)27 (75)1 (3)7 (19)006 (17)6 (17)5 (14)02 (6)1 (3)1 (5)

    • ↵a PA, Provence Alpes Côte d'Azur; LR, Languedoc Roussillon; RA, Rhône Alpes; NO, Nord; MP, Midi Pyrénées; CA, Champagne Ardennes; LO, Lorraine; AU, Auvergne Picardie; BR, Bretagne; PL, Pays de Loire; BN, Basse Normandie; CE, Centre; AL, Alsace; AQ, Aquitaine; HN, Haute Normandie; PC, Poitou Charentes.

    • ↵b −, negative; +, positive; NA, sample not available.

    • ↵c The Varroa samples were collected in August or September.

  • TABLE 3.

    Frequencies of infected apiaries during 2002

    VirusFrequency (%)a
    AdultsPupaeMites
    DWV9794100
    SBV868045
    CBPV2800
    ABPV582336
    BQCV86230
    KBV1765

    • ↵a An apiary was considered positive for DWV, SBV, CBPV, ABPV, BQCV, or KBV if at least 1 of 10 colonies was positive in the spring, summer, or autumn.

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