Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Biologia

12 Issues per year


IMPACT FACTOR 2016: 0.759
5-year IMPACT FACTOR: 0.803

CiteScore 2017: 0.86

SCImago Journal Rank (SJR) 2017: 0.299
Source Normalized Impact per Paper (SNIP) 2017: 0.544

Online
ISSN
1336-9563
See all formats and pricing
More options …
Volume 67, Issue 3

Issues

Prevalence of honeybee viruses in the Czech Republic and coinfections with other honeybee disease

Stepan Ryba
  • Biodiversity Research Group, Department of Zoology, Faculty of Science, Charles University in Prague, Vinicna 7, CZ-12488, Prague, Czech Republic
  • Bee Research Institute at Dol, Libcice n. Vlt, Czech Republic
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Dalibor Titera
  • Bee Research Institute at Dol, Libcice n. Vlt, Czech Republic
  • Faculty of Agrobiology, Food and Natural Resources, Department of Zoology and Fisheries, Czech University of Life Science, Prague, Czech Republic
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Iva Schodelbauerova-Traxmandlova / Pavel Kindlmann
  • Biodiversity Research Group, Department of Zoology, Faculty of Science, Charles University in Prague, Vinicna 7, CZ-12488, Prague, Czech Republic
  • Global Change Research Centre, Academy of Sciences of the CR, Prague, Czech Republic
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2012-04-18 | DOI: https://doi.org/10.2478/s11756-012-0038-5

Abstract

Six bee viruses, which occur in Apis mellifera, were monitored in the Czech Republic between 2006 and 2009. Samples of larvae and pupae collected from hives where American foulbrood was detected were screened for bee viruses and in the 125 samples of larvae, there was no confirmed case of a larva infected with both American foulbrood and a bee virus. Of 145 samples infected with the protozoan Nosema apis, there were 23 cases of coinfections with the BQCV virus, 18 with the DWV virus and 11 with the ABPV virus. All coinfections with three or four viruses were also statistically significant apart from the one between ABPV with CBPV and DWV. The PCA ordination diagram indicates that BQCV occurs mainly with Nosema apis and DWV mainly with ABPV.

Keywords: Nosema apis; Nosema ceranae; Paenibacillus; DWV; ABPV; BQCV; SBV; KBV; CBPV

  • [1] Alippi A.M., Lopez A.C. & Aguilar O.M. 2004. A PCR-based method that permits specific detection of Paenibacillus larvae subsp. larvae, the cause of American Foulbrood of honey bees, at the subspecies level. Lett. Appl. Microbiol. 39(1): 25–33. DOI: 10.1111/j.1472-765X.2004.01535.x http://dx.doi.org/10.1111/j.1472-765X.2004.01535.xCrossrefGoogle Scholar

  • [2] Bailey L. 1955. The infection of the ventriculus of the adult honeybee by Nosema apis (Zander). Parasitology 45: 86–94. DOI: 10.1017/S0031182000027451 http://dx.doi.org/10.1017/S0031182000027451Google Scholar

  • [3] Bailey L. 1967. The incidence of virus diseases in the honey bee. Ann. Appl. Biol. 60(1): 43–48. DOI: 10.1111/j.1744-7348.1967.tb05920.x http://dx.doi.org/10.1111/j.1744-7348.1967.tb05920.xCrossrefGoogle Scholar

  • [4] Bailey L. 1976. Viruses attacking the honey bee. Adv. Virus. Res. 20: 271–304. DOI: 10.1016/S0065-3527(08)60507-2 http://dx.doi.org/10.1016/S0065-3527(08)60507-2CrossrefGoogle Scholar

  • [5] Bakonyi T., Derakhshifar I., Grabensteiner E. & Nowotny N. 2003. Development and evaluation of PCR assays for the detection of Paenibacillus larvae in honey samples: comparison with isolation and biochemical characterization. Appl. Environ. Microbiol. 69(3): 1504–1510. DOI: 10.1128/AEM.69.3.1504-1510.2003 http://dx.doi.org/10.1128/AEM.69.3.1504-1510.2003CrossrefGoogle Scholar

  • [6] Bakonyi T., Farkas R., Szendroi A., Dobos-Kovacs M. & Rusvai M. 2002. Detection of acute bee paralysis virus by RT-PCR in honey bee and Varroa destructor field samples: rapid screening of representative Hungarian apiaries. Apidologie 33(1): 63–74. DOI: 10.1051/apido:2001004 http://dx.doi.org/10.1051/apido:2001004CrossrefGoogle Scholar

  • [7] Blanchard P., Olivier V., Iscache A.L., Celle O., Schurr F., Lallemand P. & Ribiere M. 2008. Improvement of RTPCR detection of chronic bee paralysis virus (CBPV) required by the description of genomic variability in French CBPV isolates. J. Invertebr. Pathol. 97(2): 182–185. DOI: 10.1016/j.jip.2007.07.003 http://dx.doi.org/10.1016/j.jip.2007.07.003CrossrefWeb of ScienceGoogle Scholar

  • [8] Bourgeois A.L., Rinderer T.E., Beaman L.D. & Danka R.G. 2010. Genetic detection and quantification of Nosema apis and N. ceranae in the honey bee. J. Invertebr. Pathol. 103(1): 53–58. DOI: 10.1016/j.jip.2009.10.009 http://dx.doi.org/10.1016/j.jip.2009.10.009Web of ScienceCrossrefGoogle Scholar

  • [9] de Graaf D.C., Alippi A.M., Brown M., Evans J.D., Feldlaufer M., Gregorc A., Hornitzky M., Pernal S.F., Schuch D.M., Titera D., Tomkies V. & Ritter W. 2006. Diagnosis of American foulbrood in honey bees: a synthesis and proposed analytical protocols. Lett. Appl. Microbiol. 43(6): 583–590. DOI: 10.1111/j.1472-765X.2006.02057.x http://dx.doi.org/10.1111/j.1472-765X.2006.02057.xCrossrefGoogle Scholar

  • [10] Dobbelaere W., de Graaf D.C., Reybroeck W., Desmedt E., Peeters J.E. & Jacobs F.J. 2001. Disinfection of wooden structures contaminated with Paenibacillus larvae subsp. larvae spores. J. Appl. Microbiol. 91(2): 212–216. DOI: 10.1046/j.1365-2672.2001.01376.x http://dx.doi.org/10.1046/j.1365-2672.2001.01376.xCrossrefGoogle Scholar

  • [11] Forsgren E. & Fries I. 2010. Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet. Parasitol. 170(3–4): 212–217. DOI: 10.1016/j.vetpar.2010.02.010 http://dx.doi.org/10.1016/j.vetpar.2010.02.010Web of ScienceCrossrefGoogle Scholar

  • [12] Fries I., Martin R., Meana A., Garcia-Palencia P. & Higes M. 2006. Natural infections of Nosema ceranae in European honey bees. J. Apicult. Res. 45(4): 230–233. DOI: 10.3896/IBRA.1.45.4.13 http://dx.doi.org/10.3896/IBRA.1.45.4.13CrossrefGoogle Scholar

  • [13] Genersch E. 2005. Development of a rapid and sensitive RT-PCR method for the detection of deformed wing virus, a pathogen of the honeybee (Apis mellifera). Vet. J. 169(1): 121–123. DOI: 10.1016/j.tvjl.2004.01.004 http://dx.doi.org/10.1016/j.tvjl.2004.01.004CrossrefGoogle Scholar

  • [14] Govan V.A., Allsopp M.H. & Davison S. 1999. A PCR detection method for rapid identification of Paenibacillus larvae. Appl. Environ. Microbiol. 65(5): 2243–2245. Google Scholar

  • [15] Higes M., Esperon F. & Sanchez-Vizcaino J.M. 2007. Short communication. First report of black queen-cell virus detection in honey bees (Apis mellifera) in Spain. Spanish J. Agricult. Res. 5(3): 322–325. Google Scholar

  • [16] Higes M., Martin-Hernandez R., Botias C., Bailon E.G., Gonzalez-Porto A.V., Barrios L., Del Nozal M.J., Bernal J.L., Jimenez J.J., Palencia P.G. & Meana A. 2008. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 10(10): 2659–2669. DOI: 10.1111/j.1462-2920.2008.01687.x http://dx.doi.org/10.1111/j.1462-2920.2008.01687.xCrossrefWeb of ScienceGoogle Scholar

  • [17] 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. J. Invertebr. Pathol. 91: 69–73. DOI: 10.1016/j.jip.2005.11.001 http://dx.doi.org/10.1016/j.jip.2005.11.001CrossrefGoogle Scholar

  • [18] Chen Y., Evans J. & Feldlaufer M. 2006. Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J. Invertebr. Pathol. 92: 152–159. DOI: 10.1016/j.jip.2006.03.010 http://dx.doi.org/10.1016/j.jip.2006.03.010CrossrefGoogle Scholar

  • [19] Chen Y.P., Evans J.D., Zhou L., Boncristiani H., Kimura K., Xiao T.G., Litkowski A.M. & Pettis J.S. 2009. Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J. Invertebr. Pathol. 101: 204–209. DOI: 10.1016/j.jip.2009.05.012 http://dx.doi.org/10.1016/j.jip.2009.05.012CrossrefGoogle Scholar

  • [20] Chen Y.P. & Siede R. 2007. Honey bee viruses. Adv. Virus. Res. 70: 33–80. DOI: 10.1016/S0065-3527(07)70002-7 http://dx.doi.org/10.1016/S0065-3527(07)70002-7CrossrefWeb of ScienceGoogle Scholar

  • [21] Kukielka D., Esperon F., Higes M. & Sanchez-Vizcaino J.M. 2007. A sensitive one-step real-time RT-PCR method for detection of deformed wing virus and black queen cell virus in honeybee Apis mellifera. J. Virol. Methods. 147(2): 275–281. DOI: 10.1016/j.jviromet.2007.09.008 http://dx.doi.org/10.1016/j.jviromet.2007.09.008CrossrefGoogle Scholar

  • [22] Lanzi G., de Miranda J.R., Boniotti M.B., Cameron C.E., Lavazza A., Capucci L., Camazine S.M. & Rossi C. 2006. Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.). J. Virol. 80(10): 4998–5009. DOI: 10.1128/JVI.80.10.4998-5009.2006 http://dx.doi.org/10.1128/JVI.80.10.4998-5009.2006CrossrefGoogle Scholar

  • [23] Martin-Hernandez R., Meana A., Prieto L., Salvador A.M., Garrido-Bailon E. & Higes M. 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl. Environ. Microbiol. 73(20): 6331–6338. DOI: 10.1128/AEM.00270-07 http://dx.doi.org/10.1128/AEM.00270-07Web of ScienceCrossrefGoogle Scholar

  • [24] Parrella G., Caprio E. & Mazzone P. 2006. Development of improved molecular methods for the detection of deformed wing virus (DWV) in honeybees (Apis mellifera L.) and mites (Varroa destructor Oud.). Commun. Agric. Appl. Biol. Sci. 71(2PtB): 625–629. PMID: 17385533 Google Scholar

  • [25] Paxton R.J., Klee J., Korpela S. & Fries I. 2007. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 38(6): 558–565. DOI: 10.1051/apido:2007037 http://dx.doi.org/10.1051/apido:2007037Web of ScienceCrossrefGoogle Scholar

  • [26] Ribiere M., Lallemand P., Iscache A.L., Schurr F., Celle O., Blanchard P., Olivier V. & Faucon J.P. 2007b. Spread of infectious chronic bee paralysis virus by honeybee (Apis mellifera L.) feces. Appl. Environ. Microbiol. 73(23): 7711–7716. DOI: 10.1128/AEM.01053-07 http://dx.doi.org/10.1128/AEM.01053-07CrossrefWeb of ScienceGoogle Scholar

  • [27] Ribiere M., Triboulot C., Mathieu L., Aurieres C., Faucon J.P. & Pepin M. 2002. Molecular diagnosis of chronic bee paralysis virus infection. Apidologie 33(3): 339–351. DOI: 10.1051/apido:2002020 http://dx.doi.org/10.1051/apido:2002020CrossrefGoogle Scholar

  • [28] Ryba S., Titera D., Haklova M. & Stopka P. 2009. A PCR method of detecting American Foulbrood (Paenibacillus larvae) in winter beehive wax debris. Vet. Microbiol. 139(1–2): 193–196. DOI: 10.1016/j.vetmic.2009.05.009 http://dx.doi.org/10.1016/j.vetmic.2009.05.009CrossrefWeb of ScienceGoogle Scholar

  • [29] Sammataro D., Gerson U. & Needham G. 2000. Parasitic mites of honey bees: life history, implications, and impact. Annu. Rev. Entomol. 45: 519–548. DOI: 10.1146/annurev.ento.45.1.519 http://dx.doi.org/10.1146/annurev.ento.45.1.519CrossrefGoogle Scholar

  • [30] Shimanuki H., Calderone N.W. & Knox D.A. 1994. Parasitic mite syndrome — the symptoms. Amer. Bee J. 134(12): 827–828. Google Scholar

  • [31] Schmid-Hempel P. 1995. Parasites and social insects. Apidologie 26: 255–271. DOI: 10.1051/apido:19950307 http://dx.doi.org/10.1051/apido:19950307CrossrefGoogle Scholar

  • [32] Stoltz D., Shen X.R., Boggis C. & Sisson G. 1995. Molecular diagnosis of Kashmir bee virus infection. J. Apicult. Res. 34(3): 153–160. Google Scholar

  • [33] ter Braak C.J.F. & Smilauer P. 2002. CANOCO Reference Manual and CanoDraw for Windows User’s Guide: Software for Canonical Community Ordination, Biometris, Wageningen/Českějovice version 4.5. http://www.pri.wur.nl/NR/rdonlyres/1A441CBA-07D6-4981-B9A4-E11F428E1CBF/48050/terBraak2002canoco45manualpermutation.pdf Google Scholar

  • [34] VanEngelsdorp D. & 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. J. Invertebr. Pathol. 103(Suppl.): S80–S95. DOI: 10.1016/j.jip.2009.06.011 http://dx.doi.org/10.1016/j.jip.2009.06.011CrossrefWeb of ScienceGoogle Scholar

  • [35] Webster T.C., Thacker E.M., Pomper K., Lowe J. & Hunt G. 2008. Nosema apis infection in honey bee (Apis mellifera) queens. J. Apicult. Res. 47(1): 53–57. DOI: 10.3896/IBRA.1.47.1.08 http://dx.doi.org/10.3896/IBRA.1.47.1.08CrossrefGoogle Scholar

  • [36] Woyciechowski M. & Krol E. 2001. Worker genetic diversity and infection by Nosema apis in honey bee colonies. Folia Biol. (Krakow) 49(1–2): 107–112. PMID: 11732162 Google Scholar

  • [37] Zhang Q., Ongus J.R., Boot W.J., Calis J., Bonmatin J.M., Bengsch E. & Peters D. 2007. Detection and localisation of picorna-like virus particles in tissues of Varroa destructor, an ectoparasite of the honey bee, Apis mellifera. J. Invertebr. Pathol. 96(2): 97–105. DOI: 10.1016/j.jip.2007.03.019 http://dx.doi.org/10.1016/j.jip.2007.03.019CrossrefWeb of ScienceGoogle Scholar

About the article

Published Online: 2012-04-18

Published in Print: 2012-06-01


Citation Information: Biologia, Volume 67, Issue 3, Pages 590–595, ISSN (Online) 1336-9563, ISSN (Print) 0006-3088, DOI: https://doi.org/10.2478/s11756-012-0038-5.

Export Citation

© 2012 Slovak Academy of Sciences. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Khaliunaa Tsevegmid, Peter Neumann, Orlando Yañez, and Wolfgang Blenau
PLOS ONE, 2016, Volume 11, Number 3, Page e0151164
[2]
Noureddine Adjlane, Benjamin Dainat, Laurent Gauthier, and Vincent Dietemann
Apidologie, 2016, Volume 47, Number 5, Page 631
[3]
Yamandú Mendoza, Karina Antúnez, Belén Branchiccela, Matilde Anido, Estela Santos, and Ciro Invernizzi
Apidologie, 2014, Volume 45, Number 2, Page 224
[4]
Sebastian Gisder and Elke Genersch
Journal of Invertebrate Pathology, 2013, Volume 113, Number 1, Page 1
[5]
Henriette Rasolofoarivao, Johanna Clémencet, Lala Harivelo Raveloson Ravaomanarivo, Dimby Razafindrazaka, Bernard Reynaud, and Hélène Delatte
Experimental and Applied Acarology, 2013, Volume 60, Number 4, Page 521

Comments (0)

Please log in or register to comment.
Log in