Skip to main content
Log in

Characteristics of Nosema ceranae infection in Serbian honey bee colonies

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

Abstract

The incidence, symptoms and consequences of Nosema ceranae infection were monitored in 200 honey bee colonies in Serbia over 5 years (2008–2012) to reveal if they display characteristics described for nosemosis type C. Continual high frequency of N. ceranae-positive colonies was recorded within each study year, ranging from 73 to 98 %. A seasonal pattern in N. ceranae incidence was observed over 4 years (2008–2011). Symptoms traditionally attributed to Nosema apis infection were observed in the majority of N. ceranae-infected colonies, both among surviving and those that died. These symptoms could not serve as predictive markers for colony losses, as they were significantly more frequently observed among surviving colonies in 2010, 2011 and 2012. No clear association between N. ceranae infection and colony losses was affirmed neither during the winter nor during the summer season. Thus, N. ceranae infection in Serbian bees do not fit the characteristics for nosemosis type C.

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.

Figure 1.
Figure 2.

Similar content being viewed by others

References

  • Alaux, C., Brunet, J.L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., Brillard, J., Baldy, A., Belzunces, L.P., Le Conte, Y. (2010) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12, 774–782

    Article  PubMed  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). Environ. Microbiol. 11, 2284–2290

    Article  PubMed  Google Scholar 

  • Bacandritsos, N., Granato, A., Budge, G., Papanastasiou, I., Roinioti, E., Caldon, M., Falcaro, C., Gallina, A., Mutinelli, F. (2010) Sudden deaths and colony population decline in Greek honey bee colonies. J. Invertebr. Pathol. 105, 335–340

    Article  PubMed  CAS  Google Scholar 

  • Bailey, L. (1955) The epidemiology and control of Nosema disease of the honey bee. Ann. Appl. Biol. 43, 379–389

    Article  CAS  Google Scholar 

  • Bailey, L. (1967) Nosema apis and dysentery of the honey bee. J. Apic. Res. 6, 121–125

    Google Scholar 

  • Botías, C., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A., Martínez-Salvador, A., De La Rúa, P., Meana, A., Higes, M. (2012) Critical aspects of the Nosema spp. diagnostic sampling in honey bee (Apis mellifera L.) colonies. Parasitol. Res. 110, 2557–2561

    Article  PubMed  Google Scholar 

  • Bourgeois, A.L., Rinderer, E.T., Beaman, D.L., Danka, G.R. (2010) Genetic detection and quantification of Nosema apis and N. ceranae in the honey bee. J. Invertebr. Pathol. 103, 53–58

    Article  PubMed  CAS  Google Scholar 

  • Bromenshenk, J.J., Henderson, C.B., Wick, C.H., Stanford, M.F., Zulich, A.W., et al. (2010) Iridovirus and microsporidian linked to honey bee colony decline. PLoS One 5, e13181

    Article  PubMed  Google Scholar 

  • Burgher-MacLellan, K.L., Williams, G.R., Shutler, D., MacKenzie, K., Rogers, R.E.L. (2010) Optimization of duplex real-time PCR with melting-curve analysis for detecting the microsporidian parasites Nosema apis and Nosema ceranae in Apis mellifera. Can. Entomol. 142, 271–283

    Article  Google Scholar 

  • Chaimanee, V., Chantawannakul, P., Chen, Y., Evans, J.D., Pettis, J.S. (2012) Differential expression of immune genes of adult honey bee (Apis mellifera) after inoculated by Nosema ceranae. J. Insect Physiol. 58, 1090–1095

    Article  PubMed  CAS  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 

  • Chen, Y.P., Evans, J.D., Murphy, C., Gutell, R., Zuker, M., Gundensen-Rindal, D., Pettis, J.S. (2009) Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. J. Eukaryot. Microbiol. 56, 142–147

    Article  PubMed  CAS  Google Scholar 

  • COLOSS workshop (2009). Conclusions, Proc. Workshop “Nosema disease: lack of knowledge and work standardization” (COST Action FA0803) Guadalajara. http://www.coloss.org/news/nosema-workshop-proceedings-online. Accessed 20 Nov 2009

  • Cox-Foster, D.L., Conlan, S., Holmes, E.C., Palacios, G., Evans, J.D., et al. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283–287

    Article  PubMed  CAS  Google Scholar 

  • Dainat, B., Evans, J.D., Chen, Y.P., Gauthier, L., Neumann, P. (2012) Predictive markers of honey bee colony collapse. PLoS One 7, e32151

    Article  PubMed  CAS  Google Scholar 

  • Ellis, J.D., Evans, J.D., Pettis, J. (2010) Colony losses, managed colony population decline, and colony collapse disorder in the United States. J. Apic. Res. 49, 134–136

    Article  Google Scholar 

  • Fernández, J.M., Puerta, F., Cousinou, M., Dios-Palomares, R., Campano, F., Redondo, L. (2012) Asymptomatic presence of Nosema spp. in Spanish commercial apiaries. J. Invertebr. Pathol. 111, 106–110

    Article  PubMed  Google Scholar 

  • Forsgren, E., Fries, I. (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet. Parasitol. 170, 212–217

    Article  PubMed  Google Scholar 

  • Fries, I. (2010) Nosema ceranae in European honey bees (Apis mellifera). J. Invertebr. Pathol. 103, S73–S79

    Article  PubMed  Google Scholar 

  • Fries, I., Forsgren, E. (2008) Undersökning av spridningen av Nosema ceranae i Sverige. Investigation of the distribution of Nosema ceranae in Sweden Bitidningen 107, januari/februari, pp. 26–27 (in Swedish)

  • Fries, I., Raina, S. (2003) American foulbrood (Paenibacillus larvae larvae) and African honey bees (Apis mellifera scutellata). J. Econ. Entomol. 96, 1641–1646

    Article  PubMed  Google Scholar 

  • Fries, I., Ekbohm, G., Villumstad, E. (1984) Nosema apis, sampling techniques and honey yield. J. Apic. Res. 23, 102–105

    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

    Article  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 

  • Genersch, E., von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., et al. (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41, 332–352

    Article  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 

  • Gisder, S., Hedtke, K., Möckel, N., Frielitz, M.-C., Linde, A., Genersch, E. (2010) Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Appl. Environ. Microb. 76, 3032–3038

    Article  CAS  Google Scholar 

  • Hamiduzzaman, M.M., Guzman-Novoa, E., Goodwin, P.H. (2010) A multiplex PCR assay to diagnose and quantify Nosema infections in honey bees (Apis mellifera). J. Invertebr. Pathol. 105, 151–155

    Article  PubMed  Google Scholar 

  • Hedtke, K., Jensen, P.M., Jensen, A.B., Genersch, E. (2011) Evidence for emerging parasites and pathogens influencing outbreaks of stress-related diseases like chalkbrood. J. Invertebr. Pathol. 108, 167–173

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

    Article  PubMed  Google Scholar 

  • Higes, M., Martín-Hernández, R., Meana, A. (2010a) Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41, 375–392

    Article  Google Scholar 

  • Higes, M., Martín-Hernández, R., Martínez-Salvador, A., Garrido-Bailón, E., González-Porto, A.V., Meana, A., Bernal, J.L., del Nozal, M.J., Bernal, J. (2010b) A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environ. Microbiol. Rep. 2, 243–250

    Article  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

    Article  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 

  • Klee, J., Besana, A.M., Genersch, E., Gisder, S., Nanetti, A., et al. (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 

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

    Article  Google Scholar 

  • Martín-Hernández, R., Meana, A., García-Palencia, P., Marín, P., Botías, C., Garrido-Bailón, E., Barrios, L., Higes, M. (2009) Effect of temperature on the biotic potential of honeybee microsporidia. Appl. Environ. Microb. 75, 2554–2557

    Article  Google Scholar 

  • Martín-Hernández, R., Botías, C., Garrido Bailón, E., Martínez-Salvador, A., Prieto, L., Meana, A., Higes, M. (2011a) Microsporidia infecting Apis mellifera: coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environ. Microbiol. 14, 2127–2138

    Article  PubMed  Google Scholar 

  • Martín-Hernández, R., Botías, C., Barrios, L., Martínez-Salvador, A., Meana, A., Mayack, C., Higes, M. (2011b) Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitol. Res. 109, 605–612

    Article  PubMed  Google Scholar 

  • Mayack, C., Naug, D. (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J. Invertebr. Pathol. 100, 185–188

    Article  PubMed  Google Scholar 

  • Meana, A., Martín-Hernández, R., Higes, M. (2010) The reliability of spore counts to diagnose Nosema ceranae infections in honey bees. J. Apic. Res. 49, 212–214

    Article  Google Scholar 

  • Muñoz, I., Stevanovic, J., Stanimirovic, Z., De la Rúa, P. (2012) Genetic variation of Apis mellifera from Serbia inferred from mitochondrial analysis. J. Apic. Sci. 56, 59–69

    Google Scholar 

  • Nabian, S., Ahmadi, K., Nazem Shirazi, M.H., Gerami Sadeghian, A. (2011) First detection of Nosema ceranae, a microsporidian protozoa of European honeybees (Apis mellifera) in Iran. Iran. J. Parasitol. 6, 89–95

    PubMed  CAS  Google Scholar 

  • OIE (2008) Office International des Epizooties, Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, Chap. 2.2.4., Nosemosis of Honey Bees. http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.02.04_NOSEMOSIS.pdf

  • Paxton, R.J. (2010) Does infection by Nosema ceranae cause Colony Collapse Disorder in honey bees (Apis mellifera)? J. Apic. Res. 49, 80–84

    Article  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

    Article  Google Scholar 

  • RHMZ, Republic Hydrometeorological Sevice of Serbia. http://www.hidmet.gov.rs/index_eng.php

  • Runckel, C., Flenniken, M.L., Engel, J.C., Ruby, J.G., Ganem, D., Andino, R., DeRisi, J.L. (2011) Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One 6, e20656

    Article  PubMed  CAS  Google Scholar 

  • Stanimirovic, Z., Pejovic, D., Stevanovic, J., Vucinic, M., Mirilovic, M. (2002) Investigations of hygienic behaviour and disease resistance in organic beekeeping of two honeybee ecogeographic varieties from Serbia. Acta Vet.-Beograd 52, 169–180

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stanimirovic, Z., Stevanovic, J., Cirkovic, D. (2005b) Behavioural defenses of the honey bee ecotype from Sjenica—Pester against Varroa destructor. Acta Vet.-Beograd 55, 69–82

    Google Scholar 

  • Stevanovic, J., Stanimirovic, Z., Radakovic, M., Kovacevic, R.S. (2010) Biogeographic study of the honey bee (Apis mellifera L.) from Serbia, Bosnia and Herzegovina and Republic of Macedonia based on mitochondrial DNA analyses. Russ. J. Genet. 46, 603–609

    Article  CAS  Google Scholar 

  • Stevanovic, J., Stanimirovic, Z., Genersch, E., Kovacevic, R.S., Ljubenkovic, J., Radakovic, M., Aleksic, N. (2011) Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie 41, 49–58

    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 

  • Tlak Gajger, I.T., Vugrek, O., Grilec, D., Petrinec, Z. (2010) Prevalence and distribution of Nosema ceranae in Croatian honeybee colonies. Vet. Med.-Czech 55, 457–462

    CAS  Google Scholar 

  • Traver, B.E., Fell, R.D. (2011) Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia. J. Invertebr. Pathol. 107, 43–49

    Article  PubMed  Google Scholar 

  • Traver, B.E., Williams, M.R., Fell, R.D. (2012) Comparison of within hive sampling and seasonal activity of Nosema ceranae in honey bee colonies. J. Invertebr. Pathol. 109, 187–193

    Article  PubMed  Google Scholar 

  • vanEngelsdorp, D., Evans, J.D., Saegerman, C., Mullin, C., Haubruge, E., et al. (2009) Colony collapse disorder: a descriptive study. PLoS One 4, e6481

    Article  PubMed  Google Scholar 

  • Vejsnæs, F., Nielsen, S.L., Kryger, P. (2010) Factors involved in the recent increase in colony losses in Denmark. J. Apic. Res. 49, 109–110

    Article  Google Scholar 

  • Vidau, C., Diogon, M., Aufauvre, J., Fontbonne, R., Viguès, B., et al. (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS One 6, e21550

    Article  PubMed  CAS  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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

This study was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (grant No. III 46002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jevrosima Stevanovic.

Additional information

Manuscript editor: David Tarpy

Caractéristiques de l’infection par Nosema ceranae dans les colonies d’abeilles de Serbie

Nosema ceranae / Apis mellifera / nosémose de type C / fèces / maladie de l’abeille

Merkmale der Infektionen mit Nosema ceranae in Bienenvölkern in Serbien

Nosema ceranae / Apis mellifera / Nosemose Typ C / Fäzes

Jevrosima Stevanovic and Predrag Simeunovic contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stevanovic, J., Simeunovic, P., Gajic, B. et al. Characteristics of Nosema ceranae infection in Serbian honey bee colonies. Apidologie 44, 522–536 (2013). https://doi.org/10.1007/s13592-013-0203-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-013-0203-z

Keywords

Navigation