Prevalence and seasonality of Nosema species in Québec honey bees

Canadian Entomologist

Volumn 144, Issue 4, 2012, Pages 577-588

  Copley, T R ^a   Chen, H ^a   Giovenazzo, P ^b   Houle, E ^c   Jabaji, S H ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c Centre de Recherche en Science Animale de Deschambault   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; DISEASE INCIDENCE; DISEASE PREVALENCE; EPIDEMIOLOGY; HONEYBEE; PARASITE INFESTATION; PARASITE PREVALENCE; POLYMERASE CHAIN REACTION; PROTOZOAN; SEASONALITY; SPORE;

CANADA; QUEBEC [CANADA];

APIDAE; APIS; APIS MELLIFERA; BACTERIA (MICROORGANISMS); HYMENOPTERA; MICROSPORIDIA; NOSEMA; NOSEMA APIS; NOSEMA CERANAE;

EID: 84864693948     PISSN: 0008347X     EISSN: 19183240     Source Type: Journal    
DOI: 10.4039/tce.2012.46     Document Type: Article

References (43)

1. Anderson, D.L. and Giacon, H. 1992. Reduced pollen collection by honey bee (Hymenoptera: Apidae) colonies infected with Nosema apis and sacbrood virus. Journal of Economic Entomology, 85: 47-51.
2. Antúnez, K., Martín Hernández, R., Prieto, L., Meana, A., Zunino, P., and Higes, M. 2009. Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology, 11: 2284-2290.
3. Bailey, L. 1955. The epidemiology and control of Nosema disease of the honey bee. Annals of Applied Biology, 43: 379-389.
4. Bourgeois, A., Rinderer, T., Beaman, L., and Danka, R. 2010. Genetic detection and quantification of Nosema apis and N. ceranae in the honey bee. Journal of Invertebrate Pathology, 103: 53-58.
5. Canadian Association of Professional Apiculturalists. 2008. CAPA statement on honey bee losses in Canada (2008). Canadian Association of Professional Apiculturalists. Available from http://www.capabees.com/main/files/ pdf/canwintlossnewrev. pdf accessed 2 February 2012.
6. Chauzat, M.P., Higes, M., Martín-Hernández, R., Meana, A., Cougoule, N., and Faucon, J.P. 2007. Presence of Nosema ceranae in French honey bee colonies. Journal of Apicultural Research, 46: 127-128. (Pubitemid 47112853)
7. Chen, Y., Evans, J., Murphy, C., Gutell, R., Zuker, M., Gundensen Rindal, D., et al. 2009a. Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. Journal of Eukaryotic Micrbiology, 56: 142-147.
8. Chen, Y., Evans, J., Smith, I., and Pettis, J. 2008. Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology, 97: 186-188.
9. Chen, Y., Evans, J., Zhou, L., Boncristiani, H., Kimura, K., Xiao, T., et al. 2009b. Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. Journal of Invertebrate Pathology, 101: 204-209.
10. Chen, Y., Higgins, J., and Feldlaufer, M. 2005. Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honey bee (Apis mellifera L.). Applied and Environmental Microbiology, 71: 436-441. (Pubitemid 40116299)
11. de Graaf, D., Raes, H., Sabbe, G., De Rycke, P., and Jacobs, F. 1994. Early development of Nosema apis (Microspora: Nosematidae) in the midgut epithelium of the honey bee (Apis mellifera). Journal of Invertebrate Pathology, 63: 74-81.
12. Doull, K.M. and Cellier, K. 1961. A survey of the incidence of Nosema disease (Nosema apis Zander) of the honey bee in South Australia. Journal of Insect Pathology, 3: 280-288.
13. Franzen, C. 2008. Microsporidia: a review of 150 years of research. The Open Parasitology Journal, 2: 1-34.
14. Fries, I. 1988. Infectivity and multiplication of Nosema apis Z. in the ventriculus of the honey bee. Apidologie, 19: 319-328.
15. Fries, I. 2010. Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology, 103: S73-S79.
16. Fries, I., Ekbohm, G., and Villumstad, E. 1984. Nosema apis, sampling techniques and honey yield. Journal of Apicultural Research, 23: 102-105.
17. Fries, I., Feng, F., daSilva, A., Slemenda, S.B., and Pieniazek, N.J. 1996. Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee, Apis cerana (Hymenoptera, Apidae). European Journal of Protistology, 32: 356-365. (Pubitemid 26380633)
18. Fries, I., Martin, R., Meana, A., Garcia-Palencia, P., and Higes, M. 2006. Natural infections of Nosema ceranae in European honey bees. Journal of Apicultural Research, 45: 230-233. (Pubitemid 46086022)
19. Giersch, T., Berg, T., Galea, F., and Hornitzky, M. 2009. Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie, 40: 117-123.
20. Gisder, S., Hedtke, K., Mockel, N., Frielitz, M., Linde, A., and Genersch, E. 2010. Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Applied and Environmental Microbiology, 76: 3032-3038.
21. Guzman-Novoa, E., Hamiduzzaman, M.M., Arichavaleta-Velasco, M.E., Koleoglu, G., Valizadeh, P., and Correa-Benitez, A. 2011. Nosema ceranae has parasitized Africanized honey bees in Mexico since at least 2004. Journal of Apicultural Research, 50: 167-169.
22. Hamiduzzaman, M., Guzman-Novoa, E., and Goodwin, P. 2010. A multiplex PCR assay to diagnose and quantify Nosema infections in honey bees (Apis mellifera). Journal of Invertebrate Pathology, 105: 151-155.
23. Henriques, N. 2009. Diversity and recombination of rDNA in the microsporidian Nosema ceranae: how reliable is the genotyping? Proceedings of the workshop Nosema disease: lack of knowledge and work standardization (COST Action FA0803), Guadalajara, Spain. Available from http://www.coloss. org/publications/Nosema-Workshop-Proceedings.pdf accessed on 16 November 2011.
24. Higes, M., García-Palencia, P., Martín-Hernández, R., and Meana, A. 2007. Experimental infection of Apis mellifera honey bees with Nosema ceranae (Microsporidia). Journal of Invertebrate Pathology, 94: 211-217. (Pubitemid 46240071)
25. Higes, M., Martín-Hernández, R., Botías, C., Bailón, E., González Porto, A., Barrios, L., et al. 2008. How natural infection by Nosema ceranae causes honey bee colony collapse. Environmental Microbiology, 10: 2659-2669.
26. Higes, M., Martín-Hernández, R., and Meana, A. 2006. Nosema ceranae, a new microsporidian parasite in honey bees in Europe. Journal of Invertebrate Pathology, 92: 93-95.
27. Higes, M., Martín-Hernández, R., and Meana, A. 2010. Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, 41: 375-392.
28. Johnson, M.R., Evans, J.D., Robinson, G.E., and Berenbaum, M.R. 2009. Changes in transcript abundance relating to colony collapse disorder of honey bees (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America, 106: 14790-14795.
29. Keeling, P. and Fast, N. 2002. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Reviews in Microbiology, 56: 93-116. (Pubitemid 35217449)
30. Klee, J., Besana, A., Genersch, E., Gisder, S., Nanetti, A., Tam, D., et al. 2007. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology, 96: 1-10. (Pubitemid 47260581)
31. Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A., Garrido-Bailon, E., and Higes, M. 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73: 6331-6338. (Pubitemid 47623689)
32. Mathis, A. 2000. Microsporidia: emerging advances in understanding the basic biology of these unique organisms. International Journal of Parasitology, 30: 795-804. (Pubitemid 30421125)
33. Pernal, S., Ibrahim, A., and Melathopoulos, A.P. 2010. Integrated management of Nosema and detection of antibiotic residues. Hivelights, 23: 12-18.
34. Runckel, C., Flenniken, M.L., Engel, J.C., Ruby, J.G., Ganem, D., Andino, R., et al. 2011. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. Public Library of Science One, 6: e20656-e20673.
35. Sagastume, S., del Á gulla, C., Martín-Hernandez, R., Higes, M., and Henriques-Gil, N. 2011. Polymorphism and recombination of rDNA in the putatively asexual microsporidian Nosema cernae, a pathogen of honey bees. Environmental Microbiology, 13: 84-95.
36. Traver, B.E. and Fell, R.D. 2011. Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia. Journal of Invertebrate Pathology, 107: 43-49.
37. http://dx.doi.org/10.1016/j.jip.2011.02.003.
38. Troemel, E.R. and Madhani, H.D. 2011. New models of microsporidiosis: infections in zebrafish, C. elegans, and honey bee. PLoS Pathogology, 7: e1001243. doi:10.1371/journal.ppat.1001243.
39. van Engelsdorp, D., Evans, J.D., Saegerman, C., Mullin, C., Haubruge, E., Kim Nguyen, B., et al. 2009. Colony collapse disorder: a descriptive study. Public Library of Science One, 4: e6481.
40. Webster, T., Pomper, K., Hunt, G., Thacker, E., and Jones, S. 2004. Nosema apis infection in worker and queen Apis mellifera. Apidologie, 35: 49-54. (Pubitemid 38143356)
41. Williams, G., Shafer, A., Rogers, R., Shutler, D., and Stewart, D. 2008. First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA. Journal of Invertebrate Pathology, 97: 189-192.
42. Yoshiyama, M. and Kimura, K. 2010. Distribution of Nosema ceranae in the European honey bee, Apis mellifera in Japan. Journal of Invertebrate Pathology, 106: 263-267.
43. Zander, E. 1909. Tierische Parasiten als Krankenheitserreger bei der Biene. Münchener Bienenzeitung, 31: 196-204.