Apidologie

, Volume 41, Issue 3, pp 364–374 | Cite as

Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia

Open Access
Review Article

Abstract

Globalization has provided opportunities for parasites/pathogens to cross geographic boundaries and expand to new hosts. Nosema disease is one of the most serious adult honey bee diseases and has high prevalence in honey bee colonies. For years, Nosema apis was thought to be the only microsporidian infecting domestic bee colonies. However, recently it was discovered that N. ceranae could cross the species barrier from Asian honey bees (Apis cerana) to European honey bees (Apis mellifera) that are widely used for crop pollination and honey production. Over the last few years, considerable progress has been made in our understanding of Nosema infections in honey bees. This review summarizes previous findings and recent progress in the understanding of Nosema infection of A. mellifera in the USA and Asia, with particular emphasis on the comparative epidemiological, morphological, pathological, and genomic organization of two Nosema species. The prospects of future research and remaining unresolved questions associated with the study of honey bee Nosema diseases are also discussed.

Nosema apis N. ceranae host range distribution morphology pathology genome 

Nosema ceranae, un agent pathogène d’Apis mellifera nouvellement identifié aux États-Unis et en Asie

Nosema apis Nosema ceranae spectre d’hôtes distribution morphologie pathologie génome 

Nosema ceranae, ein neu entdecktes Pathogen von Apis mellifera in den USA und Asien

Zusammenfassung

Nosema ist ein sporenbildender Parasit, der eine ernsthafte Erkrankung der erwachsenen Honigbienen verursacht und von einer Forschergruppe in Zusammenhang mit dem Colony Collapse Disorder (CCD) gebracht wurde. Die Erkrankung wird durch zwei verschiedene Nosema-Arten, N. apis und N. ceranae verursacht. Wir weisen nach, dass N. ceranae der für Bienen in den USA und Asien vorherrschende Erreger ist. Wir präsentieren auch die erste vollständige pathologische, genetische und genomische Analyse dieses Pathogens. Die Informationen aus dieser Arbeit können von anderen Forschern und Sachverständigen genutzt werden, um Bienenvölker auf die Krankheit hin zu untersuchen und um effektive Maßnahmen zu ihrer Bekämpfung zu entwickeln.

Nosema apis N. ceranae Wirtsspektrum Verteilung Morphologie Pathologie Genom 

References

  1. 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
  2. Bailey L. (1981) Honey bee pathology, Academic Press, London, UK, 124 p.Google Scholar
  3. Bailey L., Ball B.V. (1991) Honey bee pathology, Academic Press, London, 2nd ed.Google Scholar
  4. Chen Y.P., Evans J.D., Smith J.B., Pettis J.S. (2007) Nosema ceranae is a long-present and widespread microsporidian infection of the European honey bee (Apis mellifera) in the United States, J. Invertebr. Pathol. 92, 152–159.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.PubMedCrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.PubMedCrossRefGoogle Scholar
  9. de Graaf D.C., Jacobs E.J. (1991) Tissue specificity of Nosema apis, J. Invertebr. Pathol. 58, 277–278.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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
  12. Fries I. (2010) Nosema ceranae in European honey bees (Apis mellifera), J. Invertebr. Pathol. 103, S73-S79.PubMedCrossRefGoogle Scholar
  13. 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
  14. 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
  15. 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.CrossRefGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. Gilliam M., Shimanuki H. (1967) In vitro phagocytosis of Nosema apis spores by honeybee hemocytes, J. Invertebr. Pathol. 9, 387–389.PubMedCrossRefGoogle Scholar
  19. 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
  20. Gutell R.R., Noller H.F., Woese C.R. (1986a) Higher order structure in ribosomal RNA, EMBO J. 5, 1111–1113.PubMedGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. Hassanein M.H. (1953a) The influence of Nosema apis on the larval honeybee, Ann. Appl. Biol. 38, 844–846.CrossRefGoogle Scholar
  23. Hassanein M.H. (1953b) Infection with Nosema apis on the activities and longevity of the worker honeybee, Ann. Appl. Biol. 40, 418–423.CrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. Higes M., Martín R., Meana A. (2006) Nosema ceranae, a new microsporidian parasite in honey bees in Europe, J. Invertebr. Pathol. 92, 93–95.PubMedCrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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
  29. Huang Z.Y. (2001) Honey bee biology laboratory annual report, http://cyberbee.net/lab/reports/2001.html, (visited Nov. 1, 2009).Google Scholar
  30. 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.PubMedCrossRefGoogle Scholar
  31. 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
  32. 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.CrossRefGoogle Scholar
  33. 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
  34. 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.CrossRefGoogle Scholar
  35. Matheson A. (1993) World bee health update, Bee World 74, 176–212.Google Scholar
  36. Mayack C., Naug D. (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection, J. Invertebr. Pathol. 100, 185–188.PubMedCrossRefGoogle Scholar
  37. Naug D., Gibbs A. (2009) Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae, Apidologie 40, 595–599.CrossRefGoogle Scholar
  38. Paxton R.J. (2010) Does infection by Nosema ceranae cause “Colony Collapse Disorder” in honey bees (Apis mellifera)? J. Apic. Res. 49, 80–84.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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
  42. 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.CrossRefGoogle Scholar
  43. 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.PubMedCrossRefGoogle Scholar
  44. 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
  45. 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.PubMedCrossRefGoogle Scholar
  46. Zander E. (1909) Tierische Parasiten als Krankenheitserreger bei der Biene, Münchener Bienenzeitung 31, 196–204.Google Scholar

Copyright information

© Springer S+B Media B.V. 2010

Authors and Affiliations

  1. 1.Bee Research LaboratoryUSDA-ARSBeltsvilleUSA
  2. 2.Department of Entomology, Ecology, Evolutionary Biology and BehaviorMichigan State UniversityEast LansingUSA

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