Skip to main content
Log in

Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder

  • Original Article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

Nosema species were determined in honey bees from Balkan countries. A total of 273 Nosema-positive samples were analysed. Duplex PCR and PCR-RFLP with newly designed primers, nos-16S-fw/rv, were used to differentiate between N. apis and N. ceranae. N. apis was detected in only one sample (collected in 2008 in Serbia) and N. ceranae in all the others (N = 272) including 35 older samples from Serbia collected between 2000 and 2005. No co-infection was detected. The results suggest (1) the dominance of N. ceranae infection in all Balkan countries monitored throughout the last three years; (2) the presence of N. ceranae in Serbia at least since 2000, which means that N. ceranae has not recently displaced N. apis; (3) the higher efficacy of PCR-RFLP with newly designed primers, nos-16S-fw/rv, in comparison with duplex PCR (100%:82%, respectively). The prevalence of N. ceranae in Balkan countries was not associated with an increase in nosemosis or colony losses resembling Colony Collapse Disorder (CCD).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ashiralieva A., Genersch E. (2006) Reclassification, genotypes and virulence of Paenibacillus larvae, the etiological agent of American foulbrood in honeybees — a review, Apidologie 37, 411–420.

    Article  Google Scholar 

  • Chauzat M.P., Higes M., Martín-Hernández R., Meana A., Cougoule N., Faucon J.P. (2007) Presence of Nosema ceranae in French honeybee colonies, J. Apic. Res. 46, 127–128.

    Article  Google Scholar 

  • Chen Y., Evans J.D., Smith I.B., Pettis J.S. (2008) Nosema ceranae is a long-present and widespread microsporidean infection of the European honey bee (Apis mellifera) in the United States, J. Invertebr. Pathol. 97, 186–188.

    Article  PubMed  Google Scholar 

  • Cox-Foster D.L., Conlan S., Holmes E.C., 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.H., Cui L.W., 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.

    Article  PubMed  CAS  Google Scholar 

  • De la Rúa P., Jaffé R., Dall’Olio R., Muñoz I., Serrano J.(2009) Biodiversity, conservation and current threats to European honeybees, Apidologie 40, 263–284.

    Article  Google Scholar 

  • Franck P., Garnery L., Solignac M., Cornuet J.M. (2000) Molecular confirmation of a fourth lineage in honey bees from the Near East, Apidologie 31, 167–180.

    Article  CAS  Google Scholar 

  • Fries I. (1997) Protozoa, in: Morse R.A., Flottum K. (Eds.), Honey bee pests, predators and diseases, 3rd ed., A.I. Root Company, Medina, Ohio, USA, pp. 59–76.

    Google Scholar 

  • Fries I., Feng F., da Silva A., Slemenda S.B., Pieniazek 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.

    Article  Google Scholar 

  • Garnery L., Cornuet J.M., Solignac M. (1992) Evolutionary History of the Honey Bee Apis mellifera Inferred from Mitochondrial DNA Analysis, Mol. Ecol. 1, 145–154.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

  • Genersch E., Ashiralieva A., Fries I. (2005) Strainand genotype-specific differences in virulence of Paenibacillus larvae subsp. larvae, a bacterial pathogen causing American foulbrood disease in honeybees, Appl. Environ. Microbiol. 71, 7551–7555.

    Article  PubMed  CAS  Google Scholar 

  • Genersch E., Forsgren E., Pentikäinen J., Ashiralieva A., Rauch S., Kilwinski J., Fries I. (2006) Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies classification, Int. J. Syst. Evol. Microbiol. 56, 501–511.

    Article  PubMed  CAS  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.

    Article  CAS  Google Scholar 

  • Higes M., García-Palencia P., Martín-Hernández R., Meana A. (2007) Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia), J. Invertebr. Pathol. 94, 211–217.

    Article  PubMed  Google Scholar 

  • Higes M., Martín R., Meana A. (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe, J. Invertebr. Pathol. 92, 93–95.

    Article  PubMed  CAS  Google Scholar 

  • Higes M., Martín R., Sanz A., Álvarez N., Sanz A., García-Palencia P., Meana A. (2005) El síndrome de despoblamiento de las colmenas en España. Consideraciones sobre su origen, Vida Apícola 133, 15–21.

    Google Scholar 

  • Higes M., Martín-Hernández R., Botías C., Garrido-Bailón E., González-Porto A.V., Barrios L., Del Nozal M.J., Bernal J.L., Jiménez J.J., García-Palencia P., Meana A. (2008) How natural infection by Nosema ceranae causes honeybee colony collapse, Environ. Microbiol. 10, 2659–2669.

    Article  PubMed  Google Scholar 

  • Higes M., Martín-Hernández R., Garrido-Bailón E., Botías C., Meana A. (2009a) The presence of Nosema ceranae (Microsporidia) in North African honey bees (Apis mellifera intermissa), J. Apic. Res. 48, 217–219.

    Article  Google Scholar 

  • Higes M., Martín-Hernández R., Garrido-Bailón E., González-Porto A.V., García-Palencia P., Meana A., del Nozal M.J., Mayo R., Bernal J.L. (2009b) Honeybee colony collapse due to Nosema ceranae in professional apiaries, Environ. Microbiol. Rep. 1, 110–113.

    Article  Google Scholar 

  • Huang W.F., Jiang J.H., Chen Y.W., Wang C.H. (2005) Complete rRNA sequence of the Nosema ceranae from honeybee (Apis mellifera), https://gra103.aca.ntu.edu.tw/gdoc/F90632004a.pdf.

  • Huang W.F., Bocquet M., Lee KC, Sung I.H., Jiang J.H., Chen Y.W., Wang C.H. (2008) The comparison of rDNA spacer regions of Nosema ceranae isolates from different hosts and locations, J. Invertebr. Pathol. 97, 9–13.

    Article  PubMed  CAS  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.

    Article  Google Scholar 

  • Imdorf A., Charrière J.D., Gallmann P. (2006) Mögliche Ursachen für die Völkerverluste der letzten Jahre, Schweiz. Bienenztg. 129, 6–10

    Google Scholar 

  • Invernizzi C., Abud C., Tomasco I.H., Harriet J., Ramallo G., Campá J., Katz H., Gardiol G., Mendoza Y. (2009) Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay, J. Invertebr. Pathol. 101, 150–153.

    Article  PubMed  Google Scholar 

  • Johnson R.M., Evans J.D., Robinson G.E., Berenbaum M.R. (2009) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera), PNAS 106, 14790–14795.

    Article  PubMed  CAS  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.

    Article  PubMed  Google Scholar 

  • Kozmus P., Stevanovic J., Stanimirovic Z., Stojic V., Kulisic Z., Meglic V. (2007) Analysis of mitochondrial DNA in honey bees (Apis mellifera) from Serbia, Acta Vet.-Beograd 57, 465–476.

    Google Scholar 

  • Martín-Hernández R., Meana A., Prieto L., Martínez Salvador A., Garrido-Bailón E., Higes M. (2007) Outcome of colonization of Apis mellifera by Nosema ceranae, Appl. Environ. Microbiol. 73, 6331–6338.

    Article  PubMed  Google Scholar 

  • Meixner M.D., Worobik M., Wilde J., Fuchs S., Koeniger N. (2007) Apis mellifera mellifera in eastern Europe — morphometric variation and determination of its range limits, Apidologie 38, 191–197.

    Article  Google Scholar 

  • OIE (2008) Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, Chap. 2.2.4., Nosemosis of Honey Bees, http://www.oie.int/fr/normes/mmanual/2008/pdf/2.02.04_NOSEMOSIS.pdf.

  • 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.

    Article  Google Scholar 

  • Stanimirovic Z., Stevanovic J., Andjelkovic M. (2005) Chromosomal diversity in Apis mellifera carnica from Serbia, Apidologie 36, 31–42.

    Article  CAS  Google Scholar 

  • Stanimirovic Z., Stevanovic J., Bajic V., Radovic I. (2007) Evaluation of genotoxic effects of fumagillin (dicyclohexylamine) by citogenetic tests in vivo, Mutat. Res. 628, 1–10.

    PubMed  CAS  Google Scholar 

  • Stanimirovic Z., Stevanovic J., Kulic M., Stojic V. (2006) Frequency of chromosomal aberrations in the evaluation of genotoxic potential of dicyclohexylamine (fumagillin) in vivo, Acta Vet.-Beograd 56, 353–366.

    Google Scholar 

  • Stevanovic J., Stanimirovic Z., Pejin I.I., Lazarevic M. (2006) Monitoring of mitotic index and frequency of micronuclei in evaluation of genotoxic potential of fumagillin (dicyclohexylamine) in vivo, Acta Vet.-Beograd 56, 437–448.

    Google Scholar 

  • Stevanovic J., Stanimirovic Z., Radakovic M., Stojic V. (2008) In vitro evaluation of the clastogenicity of fumagillin, Environ. Mol. Mutagen. 49, 594–601.

    Article  PubMed  CAS  Google Scholar 

  • Sušnik S., Kozmus P., Poklukar J., Megliè V. (2004) Molecular characterisation of indigenous Apis mellifera carnica in Slovenia, Apidologie 35, 623–636.

    Article  Google Scholar 

  • Tapaszti Z., Forgách P., Kovágó C., Békési L., Bakonyi T., Rusvai M. (2009) First detection and dominance of Nosema ceranae in Hungarian honeybee colonies, Acta Vet. Hung. 57, 383–388.

    Article  PubMed  Google Scholar 

  • van Engelsdorp D., Evans J.D., Saegerman C., Mullin C., Haubruge E., Nguyen B.K., Frazier M., Frazier J., Cox-Foster D., Chen Y., Underwood R., Tarpy D.R., Pettis J.S. (2009) Colony collapse disorder: a descriptive study, PLoS One 4, e6481.

    Article  Google Scholar 

  • Williams G.R., Shafer A.B.A., Rogers R.E.L., Shutler D., Stewart D.T. (2008a) 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.

    Article  PubMed  Google Scholar 

  • Williams G.R., Sampson MA, Shutler D., Rogers R.E.L. (2008b) Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)? J. Invertebr. Pathol. 99, 342–344.

    Article  PubMed  CAS  Google Scholar 

  • Zander E. (1909) Tierische Parasiten als Krankheitserreger bei der Biene, Münchener Bienenzeitung 31, 196–204.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jevrosima Stevanovic.

Additional information

Manuscript editor: Peter Rosenkranz

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stevanovic, J., Stanimirovic, Z., Genersch, E. et al. Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie 42, 49–58 (2011). https://doi.org/10.1051/apido/2010034

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1051/apido/2010034

Keywords

Navigation