Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-25T05:16:29.864Z Has data issue: false hasContentIssue false

Prevalence and seasonality of Nosema species in Québec honey bees

Published online by Cambridge University Press:  16 July 2012

T.R. Copley
Affiliation:
Department of Plant Science, McGill University, 21111 Lakeshore, Ste-Anne-de-Bellevue, Quebec, Canada H9X 3V9
H. Chen
Affiliation:
Department of Plant Science, McGill University, 21111 Lakeshore, Ste-Anne-de-Bellevue, Quebec, Canada H9X 3V9
P. Giovenazzo
Affiliation:
Department of Biology, Laval University, Quebec City, Canada
E. Houle
Affiliation:
Centre de recherche en science animale de Deschambault, Deschambault, Quebec, Canada
S.H. Jabaji*
Affiliation:
Department of Plant Science, McGill University, 21111 Lakeshore, Ste-Anne-de-Bellevue, Quebec, Canada H9X 3V9
*
1Corresponding author (e-mail: suha.jabaji@mcgill.ca).

Abstract

Nosemosis is a disease of adult honey bees, Apis mellifera Linnaeus (Hymenoptera: Apidae), caused by two described species of Microsporidia: Nosema ceranae Fries and Nosema apis Zander. The epidemiology of N. apis is well understood; however, little is known about N. ceranae in Canadian apiaries. The following study aimed to determine the seasonal patterns of N. ceranae and N. apis in European honey bees in a Québec, Canada, apiary. Honey bees from six hives were sampled from 2008 to 2010 and the amount of spores quantified by both microscopic spore counts and duplex quantitative polymerase chain reaction (qPCR). Results demonstrated that duplex qPCR was the most sensitive technique and was able to detect N. ceranae in samples confirmed negative for microscopic spore counts and conventional polymerase chain reaction (PCR) detection. Results show that N. ceranae is the more prevalent parasite and was present in 75% of collections as single or mixed infections in the sampled apiary. The prevalence of N. apis was lower representing 29.7% throughout the 3 years of the study, and by 2010 was present only as mixed infections. Seasonal patterns of N. apis were consistent with previously published data with peaks in spring and autumn months, while N. ceranae peak infections varied throughout the 3-year study.

Résumé

La nosémose est une maladie des abeilles domestiques, Apis mellifera Linnaeus (Hymenoptera: Apidae) causée par deux espèces de Microsporidia: Nosema ceranae Fries et Nosema apis Zander. L′épidémiologie de N. apis est bien étudiée, mais très peu est connu de l′épidémiologie de N. ceranae au Canada. Cette étude vise à déterminer les tendances saisonnières de N. ceranae et N. apis dans les abeilles d'un rucher au Québec, Canada. Des abeilles de six ruches ont été échantillonnées entre 2008 et 2010 et la quantité de spores a été quantifiée par des méthodes microscopiques et duplex de qPCR. Les résultats ont démontré que le duplex de qPCR était plus sensible que les méthodes microscopiques et était capable de détecter N. ceranae dans des échantillons qui ont été confirmés négatifs par les méthodes microscopiques. Les résultats ont aussi démontré que N. ceranae est plus répandu que N. apis et est présent dans 75% des échantillons dans le rucher examiné. Nosema apis est moins répandu avec seulement 29.7% des échantillons et était présent en 2010 seulement en tant que co-infections. Les tendances saisonnières de N. apis sont cohérentes avec des données déjà publiées avec des pics au printemps et en automne, cependant les pics de N. ceranae ont été variés pendant la durée de l′étude.

Type
Original Article
Copyright
Copyright © Entomological Society of Canada 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, D.L.Giacon, H. 1992. Reduced pollen collection by honey bee (Hymenoptera: Apidae) colonies infected with Nosema apis and sacbrood virus. Journal of Economic Entomology, 85: 4751.Google Scholar
Antúnez, K., Martín Hernández, R., Prieto, L., Meana, A., Zunino, P., Higes, M. 2009. Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology, 11: 22842290.Google Scholar
Bailey, L. 1955. The epidemiology and control of Nosema disease of the honey bee. Annals of Applied Biology, 43: 379389.Google Scholar
Bourgeois, A., Rinderer, T., Beaman, L., Danka, R. 2010. Genetic detection and quantification of Nosema apis and N. ceranae in the honey bee. Journal of Invertebrate Pathology, 103: 5358.CrossRefGoogle Scholar
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].Google Scholar
Chauzat, M.P., Higes, M., Martín-Hernández, R., Meana, A., Cougoule, N., Faucon, J.P. 2007. Presence of Nosema ceranae in French honey bee colonies. Journal of Apicultural Research, 46: 127128.Google Scholar
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: 142147.Google Scholar
Chen, Y., Evans, J., Smith, I., 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: 186188.CrossRefGoogle ScholarPubMed
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: 204209.CrossRefGoogle ScholarPubMed
Chen, Y., Higgins, J., 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: 436441.CrossRefGoogle Scholar
de Graaf, D., Raes, H., Sabbe, G., De Rycke, P., 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: 7481.Google Scholar
Doull, K.M.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: 280288.Google Scholar
Franzen, C. 2008. Microsporidia: a review of 150 years of research. The Open Parasitology Journal, 2: 134.Google Scholar
Fries, I. 1988. Infectivity and multiplication of Nosema apis Z. in the ventriculus of the honey bee. Apidologie, 19: 319328.CrossRefGoogle Scholar
Fries, I. 2010. Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology, 103: S73S79.CrossRefGoogle ScholarPubMed
Fries, I., Ekbohm, G., Villumstad, E. 1984. Nosema apis, sampling techniques and honey yield. Journal of Apicultural Research, 23: 102105.Google Scholar
Fries, I., Feng, F., daSilva, A., Slemenda, S.B., 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: 356365.CrossRefGoogle Scholar
Fries, I., Martin, R., Meana, A., Garcia-Palencia, P., Higes, M. 2006. Natural infections of Nosema ceranae in European honey bees. Journal of Apicultural Research, 45: 230233.Google Scholar
Giersch, T., Berg, T., Galea, F., Hornitzky, M. 2009. Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie, 40: 117123.Google Scholar
Gisder, S., Hedtke, K., Mockel, N., Frielitz, M., Linde, A., 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: 30323038.Google Scholar
Guzman-Novoa, E., Hamiduzzaman, M.M., Arichavaleta-Velasco, M.E., Koleoglu, G., Valizadeh, P., Correa-Benitez, A. 2011. Nosema ceranae has parasitized Africanized honey bees in Mexico since at least 2004. Journal of Apicultural Research, 50: 167169.Google Scholar
Hamiduzzaman, M., Guzman-Novoa, E., Goodwin, P. 2010. A multiplex PCR assay to diagnose and quantify Nosema infections in honey bees (Apis mellifera). Journal of Invertebrate Pathology, 105: 151155.Google Scholar
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].Google Scholar
Higes, M., García-Palencia, P., Martín-Hernández, R., Meana, A. 2007. Experimental infection of Apis mellifera honey bees with Nosema ceranae (Microsporidia). Journal of Invertebrate Pathology, 94: 211217.CrossRefGoogle Scholar
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: 26592669.Google Scholar
Higes, M., Martín-Hernández, R., Meana, A. 2006. Nosema ceranae, a new microsporidian parasite in honey bees in Europe. Journal of Invertebrate Pathology, 92: 9395.Google Scholar
Higes, M., Martín-Hernández, R., Meana, A. 2010. Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, 41: 375392.Google Scholar
Johnson, M.R., Evans, J.D., Robinson, G.E., 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: 1479014795.CrossRefGoogle ScholarPubMed
Keeling, P.Fast, N. 2002. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Reviews in Microbiology, 56: 93116.CrossRefGoogle ScholarPubMed
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: 110.Google Scholar
Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A., Garrido-Bailon, E., Higes, M. 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73: 63316338.Google Scholar
Mathis, A. 2000. Microsporidia: emerging advances in understanding the basic biology of these unique organisms. International Journal of Parasitology, 30: 795804.Google Scholar
Pernal, S., Ibrahim, A., Melathopoulos, A.P. 2010. Integrated management of Nosema and detection of antibiotic residues. Hivelights, 23: 1218.Google Scholar
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: e20656e20673.Google ScholarPubMed
Sagastume, S., del Águlla, C., Martín-Hernandez, R., Higes, M., Henriques-Gil, N. 2011. Polymorphism and recombination of rDNA in the putatively asexual microsporidian Nosema cernae, a pathogen of honey bees. Environmental Microbiology, 13: 8495.Google Scholar
Traver, B.E.Fell, R.D. 2011. Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia. Journal of Invertebrate Pathology, 107: 4349. http://dx.doi.org/10.1016/j.jip.2011.02.003.Google Scholar
Troemel, E.R.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.Google Scholar
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.Google Scholar
Webster, T., Pomper, K., Hunt, G., Thacker, E., Jones, S. 2004. Nosema apis infection in worker and queen Apis mellifera. Apidologie, 35: 4954.Google Scholar
Williams, G., Shafer, A., Rogers, R., Shutler, D., 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: 189192.Google Scholar
Yoshiyama, M.Kimura, K. 2010. Distribution of Nosema ceranae in the European honey bee, Apis mellifera in Japan. Journal of Invertebrate Pathology, 106: 263267.Google Scholar
Zander, E. 1909. Tierische Parasiten als Krankenheitserreger bei der Biene. Münchener Bienenzeitung, 31: 196204.Google Scholar