Skip to main content
SpringerLink
Log in

Critical aspects of the Nosema spp. diagnostic sampling in honey bee (Apis mellifera L.) colonies

  • Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Nosemosis is one of the most widespread of the adult honey bee diseases and causes major economic losses to beekeepers. Two microsporidia have been described infecting honey bees worldwide, Nosema apis and Nosema ceranae, whose seasonality and pathology differ markedly. An increasing prevalence of microsporidian infections in honey bees has been observed worldwide during the last years. Because nosemosis has detrimental effects on both strength and productivity of the infected colonies, an accurate and reliable method to evaluate the presence of Nosema in honey bee colonies is needed. In this study a high degree of variability in the detection of microsporidia depending on the random subsample analyzed was found, suggesting that both sample size and the time of collection (month and day of sampling) notably affect the diagnosis.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

References

  • Alaux C, Brunet JL, Dussaubat C, Mondet F, Tchamitchan S, Cousin M, Brillard J, Baldy A, Belzunces LP, Le Conte Y (2010) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol 12(3):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(3):335–340

    Article  PubMed  CAS  Google Scholar 

  • Borneck R, Viry A, Martín-Hernández R, Higes M (2010) Honey bee colony losses in the Jura Region, France and related pathogens. J Apicult Res and Bee World 49(4):334–336

    Article  Google Scholar 

  • Bourgeois L, Beaman LD, Rinderer TE (2011) Preservation and processing methods for molecular genetic detection and quantification of Nosema ceranae. Sci Bee Cult 3(1):1–5

    Google Scholar 

  • Bromenshenk JJ, Henderson CB, Wick CH, Stanford MF, Zulich AW, Jabbour RE, Deshpande SV, McCubbin PE, Seccomb RA, Welch PM, Williams T, Firth DR, Skowronski E, Lehmann MM, Bilimoria SL, Gress J, Wanner KW, Cramer RA Jr (2010) Iridovirus and microsporidian linked to honey bee colony decline. PLoS One 5(10):e13181

    Article  PubMed  Google Scholar 

  • Chen YP, Huang ZY (2010) Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie 41(3):364–374

    Article  CAS  Google Scholar 

  • Chen YP, Evans JD, Zhou L, Boncristiani H, Kimura K, Xiao T, Litkowski AM, Pettis JS (2009) Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J Invertebr Pathol 101(3):204–209

    Article  PubMed  Google Scholar 

  • Farrar CL (1947) Nosema losses in package bees as related to queen supersedure and honey yields. J Econ Entomol 40:333–338

    PubMed  CAS  Google Scholar 

  • Fries I (1988) Infectivity and multiplication of Nosema apis Z. in the ventriculus of the honey bee. Apidologie 19:319–328

    Article  Google Scholar 

  • Furgala B, Munssen EC (1990) Protozoa. In: Morse RA, Nowogrodzki R (eds.) Honey bee pests, predators and diseases. 2nd edn. Cornell University Press, Ithaca, NY, pp. 48–64

    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

    Google Scholar 

  • Gisder S, Hedtke K, Möckel N, Frielitz MC, 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 Microbiol 76(9):3032–3038

    Article  PubMed  CAS  Google Scholar 

  • Heintz C, Ribotto M, Ellis M, Delaplane K (2011) Best management practices (BMPs) for beekeepers pollinating California’s agricultural crops. Managed Pollinator CAP Coordinated Agricultura Project, Bee Cult., March 2011: 17–19

  • Higes M, Meana A, Suárez M, Llorente J (1999) Negative long-term effects on bee colonies treated with oxalic acid against Varroa jacobsoni Oud. Apidologie 30:289–292

    Article  CAS  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, 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-Hernández R, Botías C, Garrido-Bailón E, González-Porto AV, Barrios L, Nozal M, Bernal JL, Jiménez JJ, 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, González-Porto AV, García-Palencia P, Meana A, Del Nozal MJ, Mayo R, Bernal JL (2009) Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ Microbiol Rep 1:110–113

    Article  Google Scholar 

  • Higes M, Martín-Hernández R, Meana A (2010) Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41(3):375–392

    Article  Google Scholar 

  • Hornitzky M (2008) Nosema disease. Literature review and three year survey of beekeepers, Part 2. Rural Industries Research and Development Corporation, NSW Department of Primary Industries, Australian Government. https://rirdc.infoservices.com.au/downloads/08-006. Accessed on 1 August 2011

  • Huang WF, Jiang JH, Chen YW, Wang CH (2007) A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38:30–37

    Article  Google Scholar 

  • Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, Tam DQ, Chinh TX, Puerta F, Ruz JM, Kryger P, Message D, Hatjina F, Korpela S, Fries I, Paxton RJ (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96(1):1–10

    Article  PubMed  Google Scholar 

  • Le Conte Y, Ellis M, Ritter W (2010) Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie 41(3):353–363

    Article  Google Scholar 

  • Liu TP (1984) Ultrastructure of the midgut of the worker honey bee Apis mellifera heavily infected with Nosema apis. J Invertebr Pathol 44:282–291

    Article  Google Scholar 

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

    Article  PubMed  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 Microbiol 75(8):2554–2557

    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 Apicult Res and Bee World 49(2):212–214

    Article  Google Scholar 

  • Moeller FE (1978) Nosema disease. Its control in honey bee colonies. Department of Agriculture, Washington D.C.N.S. Bulletin No. 1569, 16 pp.

    Google Scholar 

  • OIE (2008) Manual of standards for diagnostic test and vaccines. http://www.oie.int/eng/normes/mmanual/2008.pdf. Accessed 1 August 2011

  • OIE (2010) Meeting of Group Ad Hoc for Honey Bee Health, 25–27 January 2010, París. http://www.oie.int/doc/ged/D7058.PDF. Accessed 1 August 2011

  • OIE (2011a). Listed diseases 2011. http://www.oie.int/en/animal-health-in-the-world/oie-listed-diseases-2011/. Accessed 1 August 2011

  • OIE (2011b) Meeting of the OIE terrestrial animal health standards commission Paris, 1–11 February 2011. http://www.oie.int/fileadmin/Home/eng/Internationa_Standard_Setting/docs/pdf/A_TAHSC_Feb_2011_Part_A.pdf. Accessed 1 August 2011

  • Paxton RJ, 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 

  • Pickard RS, El-Shemy AAM (1989) Seasonal variation in the infection of honeybee colonies with Nosema apis Zander. J Apicult Res 28(2):93–100

    Google Scholar 

  • Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103(1):S96–S119

    Article  PubMed  Google Scholar 

  • Suwannapong G, Maksong S, Seanbualuang P, Benbow ME (2010) Experimental infection of red dwarf honeybee, Apis florea, with Nosema ceranae. J Asia Pac Entomol 13(4):361–364

    Article  Google Scholar 

  • Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24(16):3189–3194

    Article  PubMed  CAS  Google Scholar 

  • Weiser J (1961) Die Mikrosporidien als Parasiten der Insekten. Monogr Angew Entomol 17:1–149

    Google Scholar 

Download references

Acknowledgments

The authors wish to thank E. Garrido Bailón, S. Rodrigo, P. Gaspar, A. Sanz, J. Almagro, J. García, J. Martínez Llana, A. Cepero, V. Albendea, C. Rogerio, T. Corrales, C. Abascal, and S. Sagastume for their technical support. This study was supported by the Junta de Comunidades de Castilla-La Mancha (Consejería de Agricultura and Consejería de Educación), MARM-FEAGA funds (API 06/009) and INCRECYT (FEDER funds).

Author information

Authors and Affiliations

  1. Laboratorio de Patología Apícola, Centro Apícola Regional (CAR), Junta de Comunidades de Castilla La Mancha, San Martín s/n. 19180, Marchamalo, Guadalajara, Spain

    Cristina Botías, Raquel Martín-Hernández & Mariano Higes

  2. Instituto de Recursos Humanos para la Ciencia y Tecnología, INCRECYT (FEDER funds), Parque Científico de Albacete, Albacete, Spain

    Raquel Martín-Hernández

  3. Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040, Madrid, Spain

    Aránzazu Meana

Authors
  1. Cristina Botías
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raquel Martín-Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aránzazu Meana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mariano Higes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cristina Botías.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Botías, C., Martín-Hernández, R., Meana, A. et al. Critical aspects of the Nosema spp. diagnostic sampling in honey bee (Apis mellifera L.) colonies. Parasitol Res 110, 2557–2561 (2012). https://doi.org/10.1007/s00436-011-2760-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-011-2760-2

Keywords

Search

Navigation