Virus status, varroa levels, and survival of 20 managed honey bee colonies monitored in luxembourg between the summer of 2011 and the spring of 2013

Journal of Apicultural Science

Volumn 59, Issue 1, 2015, Pages 59-73

  Clermont, Antoine ^a   Pasquali, Matias ^a   Eickermann, Michael ^a   Kraus, François ^b   Hoffmann, Lucien ^a   Beyer, Marco ^a  

^a LUXEMBOURG INSTITUTE OF SCIENCE AND TECHNOLOGY   (Luxembourg)

^b Administration des Services Techniques de l'Agriculture   (Luxembourg)

Author keywords

Apis mellifera; Honey bee colony mortality; Honey bee viruses; Varroa destructor; Varroa virus interactions

Indexed keywords

ACARI; ACUTE BEE PARALYSIS VIRUS; APIS MELLIFERA; APOIDEA; BLACK QUEEN CELL VIRUS; CHRONIC BEE PARALYSIS VIRUS; DEFORMED WING VIRUS; KASHMIR BEE VIRUS; SACBROOD VIRUS; VARROA; VARROA DESTRUCTOR; VARROA DESTRUCTOR VIRUS 1;

EID: 84930351256     PISSN: 16434439     EISSN: None     Source Type: Journal    
DOI: 10.1515/jas-2015-0005     Document Type: Article

References (36)

1. Blanchard P., Guillot S., Antùnez K., Köglberger H., Kryger P., De Miranda J. R., Franco S., Chauzat M.-P., Thiéry R., Ribière M. (2014) 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. Journal of Virological Methods 197: 7–13. DOI: 10.1016/j.jviromet.2013.09.012
2. Chen Y. P., Pettis J. S., Collins A., 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
3. Clermont A., Eickermann M., Kraus F., Georges C., Hoffmann L., Beyer M. (2014) A survey on some factors potentially affecting losses of managed honeybee colonies in Luxembourg over the winters 2010/2011 and 2011/2012. Journal of Apicultural Research 53: 43-56. DOI: 10.3896/IBRA.1.53.1.04
4. Dainat B., Evans J. D., Chen Y. P., Gauthier L., 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. DOI: 10.1128/AEM.06537-11
5. De Graaf D. C., Brunain M., Imberechts H., Jacobs F. J. (2008) First molecular confirmation of deformed wing virus infections of honeybees from a Belgian apiary reveals the presence of black queen cell virus and Varroa destructor virus 1. Vlaams Diergeneeskundig Tijdschrift 77: 101-105.
6. 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., Ribière M., Ryabov E., De Smet L., van der Steen J. J. M. (2013) Standard methods for virus research in Apis mellifera. Journal of Apicultural Research 52: 1-16. DOI: 10.3896/IBRA.1.52.4.22
7. De Smet L., Ravoet J., De Miranda J. R., Wenseleers T., Mueller M. Y., Moritz R. F. A., de Graaf D. C. (2012) BeeDoctor, a versatile MPLA-based diagnostic tool for screening bee viruses. PLoS ONE 7: e47953. DOI: 10.1371/journal.pone.0047953
8. Dwight Z., Palais R., Wittwer C. T. (2011) Umelt: prediction of high-resolution melting curves and dynamic melting profiles of PCR products in a rich web application. Bioinformatics 27: 1019-1020. DOI: 10.1093/bioinformatics/btr065
9. Francis R. M., Kryger P. (2012) Single assay detection of Acute Bee Paralysis Virus, Kashmir Bee Virus and Israeli Acute Paralysis Virus. Journal of Apicultural Science 56: 137-146. DOI: 10.2478/v10289-012-0014-x
10. Francis R. M., Nielsen S. L., Kryger P. (2013) Varroa-virus interaction in collapsing honey bee colonies. PLoS ONE 8: e57540. DOI: 10.1371/journal.pone.0057540
11. Gallai N., Salles J. -M., Settele J., Vaissière B. E. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68: 810-821. DOI: 10.1016/j.ecolecon.2008.06.014
12. Gauthier L., Ravallec M., Tournaire M., Cousserans F., Bergoin M., Dainat B., De Miranda J. R. (2011) Viruses associated with ovarian degeneration in Apis mellifera L. Queens. PLoS ONE 6: e16217. DOI: 10.1371/journal. pone.0016217. DOI: 10.1371/journal.pone.0016217
13. Genersch E. (2010) Honey bee pathology: current threats to honey bees and beekeeping. Applied Microbiology and Biotechnology 87: 87-97. DOI: 10.1007/s00253-010-2573-8
14. 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. (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
15. IBM SPSS Statistics for Windows, Version 19.0 (2010) IBM Corp. Armonk, NY.
16. Kirsanov K. I., Lesovaya E. A., Yakubovskaya M. G., Belitsky G. A. (2010) SYBR Gold and SYBR Green II are not mutagenic in the Ames test. Mutation Research 699: 1-4. DOI: 10.1016/j.mrgentox.2010.04.014
17. Li Z., Chen Y., Zhang S., Chen S., Li W., Yan L., Shi L., Wu L., Sohr A., Su S. (2013) Viral infection affects sucrose responsiveness and homing ability of forager honey bees, Apis mellifera L. PLoS ONE 8: e77354. DOI: 10.1371/journal.pone.0077354
18. 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
19. Moritz R. F. A., Southwick E. E. (1992) Bees as superorganisms. An evolutionary reality. Springer-Verlag. Berlin. 395 pp.
20. Möckel N., Gisder S., Genersch E. (2011) Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route. Journal of General Virology 92: 370-377. DOI: 10.1099/vir.0.025940-0
21. Nicholls C. I., Altieri M. A. (2013) Plant biodiversity enhances bees and other insect pollinators in agroecosystems. A review. Agronomy for Sustainable Development 33: 257-274. DOI: 10.1007/s13593-012-0092-y
22. Pasquali M., Piatti P., Gullinom M. L., Garibaldim A. (2006) Development of a real-time polymerase chain reaction for the detection of Fusarium oxysporum f. sp. basilici from basil seed and roots. Journal of Phytopathology 154: 632-636. DOI: 10.1111/j.1439-0434.2006.01160.x
23. Pohorecka K., Zdańska D, Bober A., Skubida M. (2011) First detection of Israeli Acute Paralysis Virus (IAPV) in Poland and phylogenetic analysis of the isolates. Journal of Apicultural Science 55: 149-159.
24. Potts S. G., Roberts S. P. M., Dean R., Marris G., Brown M. A., Jones H. R., Neumann P., Settele J. (2010) Declines of managed honey bees and beekeepers in Europe. Journal of Apicultural Research 49: 15-22. DOI: 10.3896/IBRA.1.49.1.02
25. Ravoet J., Maharramov J., Meeus I., Wenseleers T., Smagghe G., de Graaf D. C. (2013) Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PLoS ONE 8: e72443. DOI: 10.1371/journal.pone.0072443
26. Rosenkranz P., Aumeier P., Ziegelmann B. (2010) Biology and control of Varroa destructor. Journal of Invertebrate Pathology 103: S96-S119. DOI: 10.1016/j.jip.2009.07.016
27. Runckel C., Flenniken M. L., Engel J. C., Ruby J. G., Ganem D., Andino R., DeRisi J. L. (2011) Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS ONE 6: e20656. DOI: 10.1371/journal. pone.0020656
28. Scharlaken B., de Graaf D. C., Goossens K., Brunain M., Peelman L. J., Jacobs F. J. (2008) Reference gene selection for insect expression studies using quantitative realtime PCR: the head of the honeybee, Apis mellifera, after a bacterial challenge. Journal of Insect Science 8: 33. DOI: 10.1673/031.008.3301
29. Seeley T. D. (1985) Honeybee ecology. A study of adaptation in social life. Princeton University Press, Princeton, NJ, 216 pp.
30. Semkiw P., Skubida P. (2010) Evaluation of the economical aspects of Polish beekeeping. Journal of Apicultural Science 54: 5-15.
31. Sequence Manipulation Suite: DNA Molecular Weight (2004) Available at: http://www.bioinformatics.org/sms2/dna_mw.html
32. Siede R., Derakhshifar I., Otten C., Berényi O., Bakonyi T., Köglberger H., Büchler R. (2005) Prevalence of Kashmir bee virus in central Europe. Journal of Apicultural Research 44 (3): 129-29. DOI: 10.3896/IBRA.1.44.3.09
33. Tentcheva D., Gauthier L., Zapulla N., Dainat B., Cousserans F., Coling M. E., Bergoin M. (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
34. van der Zee R., Brodschneider R., Brusbardis V., Charrière J.-D., Chlebo R., Coffey M. F., Dahle B., Drazic M. M., Kauko L., Kretavicius J., Kristiansen P., Mutinelli F., Otten C., Peterson M., Raudmets A., Santrac V., Seppälä A., Soroker V., Topolska G., Vejsnæs F., Gray A. (2014) Results of international standardised beekeeper surveys of colony losses for winter 2012-2013: analysis of winter loss rates and mixed effects modelling of risk factors for winter loss. Journal of Apicultural Research 53: 19-34. DOI: 10.3896/IBRA.1.53.1.02
35. vanEngelsdorp D., Caron D., Hayes J., Underwood R., Henson K. R. M., Spleen A., Andree M., Snyder R., Lee K., Roccasecca K., Wilson M., Wilkes J., Lengerich E., Pettis J. (2012) A national survey of managed honey bee 2010-11 winter colony losses in the USA: results from the Bee Informed Partnership. Journal of Apicultural Research 51: 115-124. DOI: 10.3896/IBRA.1.51.1.14
36. Winnebeck E. C., Millar C. D., Warman G. R. (2010) Why does insect RNA look degraded? Journal of Insect Science 10: 159. DOI: 10.1673/031.010.14119