Open Access
Review
Issue
Apidologie
Volume 41, Number 3, May-June 2010
Honey bee health
Page(s) 364 - 374
DOI https://doi.org/10.1051/apido/2010021
Published online 16 June 2010
  • Anderson D.L., Giacon H. (1992) Reduced pollen collection by honey bee (Hymenoptera: Apidae) colonies infected with Nosema apis and sacbrood virus, J. Econ. Entomol. 85, 47–51. [Google Scholar]
  • Bailey L. (1981) Honey bee pathology, Academic Press, London, UK, 124 p. [Google Scholar]
  • Bailey L., Ball B.V. (1991) Honey bee pathology, Academic Press, London, 2nd ed. [Google Scholar]
  • Chen Y.P., Evans J.D., Smith J.B., Pettis J.S. (2007) Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States, J. Invertebr. Pathol. 92, 152–159. [CrossRef] [PubMed] [Google Scholar]
  • Chen Y.P., Evans J.D., Murphy C.A., Gutell R., Zuker M., Gundersen-Rindal, D.E., Pettis, J.S. (2009a) Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera, J. Euk. Microb. 56, 142–147. [CrossRef] [Google Scholar]
  • Chen Y.P., Evans J.D., Zhou L., Boncristiani H., Kimura K., Xiao T.G., Litkowski A.M., Pettis J.S. (2009b) Asymmetrical coexistence of Nosema ceranae and N. apis in honey bees, J. Invertebr. Pathol. 101, 204–209. [CrossRef] [PubMed] [Google Scholar]
  • Cornman R.S., Chen Y.P., Schatz M.C., Street C., Zhao Y., Desany B., Egholm M., Hutchison S., Pettis J.S., Lipkin W.I., Evans J.D. (2009) Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees, PLoS Pathol. 5, e100466. [Google Scholar]
  • Cox-Foster D.L., Conlan S., Holmes E., Palacios G., Evans J.D., Moran N.A., Quan P.L., Briese T., Hornig M., Geiser D.M., Martinson V., van Engelsdorp D., Kalkstein A.L., Drysdale A., Hui J., Zhai J., Cui L., Hutchison S.K., Simons J.F., Egholm M., Pettis J.S., Lipkin W.I. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder, Science 318, 283–287. [CrossRef] [PubMed] [Google Scholar]
  • de Graaf D.C., Jacobs E.J. (1991) Tissue specificity of Nosema apis, J. Invertebr. Pathol. 58, 277–278. [CrossRef] [Google Scholar]
  • de Graaf D.C., Raes H., Sabbe G., de Rycke P.H., Jacobs F.J. (1994) Early development of Nosema apis (Microspora : Nosematidae) in the midgut epithelium of the honey bee (Apis mellifera), J. Invertebr. Pathol. 63, 74–81. [CrossRef] [Google Scholar]
  • Fries I. (1989) Observation on the development and transmission of Nosema apis Z. in the ventriculus of the honey bee, J. Apic. Res. 28, 107–117. [Google Scholar]
  • Fries I. (2010) Nosema ceranae in European honey bees (Apis mellifera), J. Invertebr. Pathol. 103, S73–S79. [CrossRef] [PubMed] [Google Scholar]
  • Fries I., Feng F. (1995) Crossinfectivity of Nosema apis in Apis mellifera and Apiscerana. In: Proceedings of the Apimondia 34th International Apicultural Congress, Bucharest, Romania, pp. 151–155. [Google Scholar]
  • Fries I., Feng F., Silva A.D., 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), Eur. J. Protistol. 32, 356–365. [Google Scholar]
  • Fries I., Martín R., Meana A., García-Palencia P., Higes M. (2006) Natural infections of Nosema ceranae in European honey bees, J. Apic. Res. 45, 230–233. [CrossRef] [Google Scholar]
  • Gatehouse H.S., Malone L.A. (1998) The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size, J. Invertebr. Pathol. 71, 97–105. [CrossRef] [PubMed] [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, 117–123. [CrossRef] [EDP Sciences] [Google Scholar]
  • Gilliam M., Shimanuki H. (1967) In vitro phagocytosis of Nosema apis spores by honeybee hemocytes, J. Invertebr. Pathol. 9, 387–389. [CrossRef] [PubMed] [Google Scholar]
  • Goodwin M., Ten Houten A., Perry J., Blackman R. (1990) Cost benefit analysis of using fumagillin to treat Nosema, New Zeal. Beekeeper 208, 11–12. [Google Scholar]
  • Gutell R.R., Noller H.F., Woese C.R. (1986a) Higher order structure in ribosomal RNA, EMBO J. 5, 1111–1113. [PubMed] [Google Scholar]
  • Gutell R.R., Weiser B., Woese C.R., Noller H.F. (1986b) Comparative Anatomy of 16S-like ribosomal RNA, Prog. Nucl. Acid Res. Mol. Biol. 32, 155–216. [CrossRef] [Google Scholar]
  • Hassanein M.H. (1953a) The influence of Nosema apis on the larval honeybee, Ann. Appl. Biol. 38, 844–846. [CrossRef] [Google Scholar]
  • Hassanein M.H. (1953b) Infection with Nosema apis on the activities and longevity of the worker honeybee, Ann. Appl. Biol. 40, 418–423. [CrossRef] [Google Scholar]
  • Higes M., García-Palencía P., Martín-Hernández R., Meana A. (2007) Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia), J. Invertebr. Pathol. 94, 211–217. [CrossRef] [PubMed] [Google Scholar]
  • Higes M., Martín-Hernández R., Botías C., Bailón E.G., González-Porto A.V., Barrios L., del Nozal M.J., Bernal J.L., Jiménez J.J., Palencia P.G., Meana A. (2008) How natural infection by Nosema ceranae causes honey bee colony collapse, Environ. Microbiol. 10, 2659–2669. [CrossRef] [PubMed] [Google Scholar]
  • Higes M., Martín R., Meana A. (2006) Nosema ceranae, a new microsporidian parasite in honey bees in Europe, J. Invertebr. Pathol. 92, 93–95. [CrossRef] [PubMed] [Google Scholar]
  • Huang W.F., Jiang J.H., Chen Y.W., Wang C.H. (2007) A Nosema ceranae isolate from the honeybee Apis mellifera, Apidologie 38, 30–37. [CrossRef] [EDP Sciences] [Google Scholar]
  • Huang W.F., Jiang J.H., Wang C.H. (2005) Nosema ceranae infection in Apis mellifera. 38th Annual Meeting of Society for Invertebrate Pathology, Anchorage, Alaska. [Google Scholar]
  • Huang Z.Y. (2001) Honey bee biology laboratory annual report, http://cyberbee.net/lab/reports/2001.html, (visited Nov. 1, 2009). [Google Scholar]
  • Klee J., Besana A.M., Genersch E., Gisder S., Nanetti A., Tam D.Q., Chinh T.X., Puerta F., Ruz J.M., Kryger P., Message D., Hatjina F., Korpela S., Fries I., Paxton R.J. (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera, J. Invertebr. Pathol. 96, 1–10. [CrossRef] [PubMed] [Google Scholar]
  • Larsson R. (1986) Ultrastructure, function, and classification of microsporidia, in: Corliss J.O., Patterson D.J. (Eds.), Progress in protistology, Vol. 1. Biopress, Bristol, England, pp. 325–390. [Google Scholar]
  • Liu T.P. (1984) Ultrastructure of the midgut of the worker honey Apis mellifera heavily infected with Nosema apis, J. Invertebr. Pathol. 44, 103–105. [CrossRef] [Google Scholar]
  • Liu F., Wang Q., Dai P.L., Wu Y.Y., Song H.K., Zhou T. (2008) Natural stripe of Microsporidia of honeybee in China, Chinese Bull. Entomol. 45, 963–966. [Google Scholar]
  • Malone L.A., Giacon H.A., Newton M.R. (1995) Comparison of the responses of some New Zealand and Australian honey bees (Apis mellifera L) to Nosema apis Z., Apidologie 26, 495–502. [CrossRef] [EDP Sciences] [Google Scholar]
  • Matheson A. (1993) World bee health update, Bee World 74, 176–212. [Google Scholar]
  • Mayack C., Naug D. (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection, J. Invertebr. Pathol. 100, 185–188. [CrossRef] [PubMed] [Google Scholar]
  • Naug D., Gibbs A. (2009) Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae, Apidologie 40, 595–599. [CrossRef] [EDP Sciences] [Google Scholar]
  • Paxton R.J. (2010) Does infection by Nosema ceranae cause « Colony Collapse Disorder » in honey bees (Apis mellifera)? J. Apic. Res. 49, 80–84. [CrossRef] [Google Scholar]
  • 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, 558–565. [CrossRef] [EDP Sciences] [Google Scholar]
  • Plischuk S., Martín-Hernández R., Lucía M., Prieto L., Botías C., Meana A., Abrahamovich A.H., Lange C., Higes M. (2009) South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera), Environ. Microbiol. Reports 1, 131–135. [CrossRef] [Google Scholar]
  • Rinderer T.E., Sylvester H.A. (1978) Variation in response to Nosema apis, longevity, and hoarding behavior in a free-mating population of the honey bee, Ann. Entomol. Soc. Am. 71, 372–374. [Google Scholar]
  • Sokolova Y.Y., Kryukova N.A., Glupov V.V., Fuxa J.R. (2006) Systenostrema alba Larsson 1988 (Microsporidia, Thelohaniidae) in the Dragonfly Aeshna viridis (Odonata, Aeshnidae) from South Siberia: morphology and molecular characterization, J. Euk. Microb. 53, 49–57. [CrossRef] [Google Scholar]
  • vanEngelsdorp D., Evans J.D., Saegerman C., Mullin C., Haubruge E., Nguyen B.K., Frazier M., Frazier J., Cox-Foster D., Chen Y.P., Underwood R., Tarpy D.R., Pettis J.S. (2009) Colony Collapse Disorder: A Descriptive Study, PLoS ONE 4, e6481. [CrossRef] [PubMed] [Google Scholar]
  • Wang D., Moeller F. (1970) The division of labor and queen attendance behavior of Nosema-infected worker honeybees, J. Econ. Entomol. 63, 1539–1541. [Google Scholar]
  • Williams G.R., Shafer A.B.A., Rogers R.E.L., Shutler D., Stewart D.T. (2008) First detection of Nosema ceranae, a microsporidean parasite of European honey bees (Apis mellifera), in Canada and central USA, J. Invertebr. Pathol. 97, 189–192. [CrossRef] [PubMed] [Google Scholar]
  • Zander E. (1909) Tierische Parasiten als Krankenheitserreger bei der Biene, Münchener Bienenzeitung 31, 196–204. [Google Scholar]