Skip to main content
SpringerLink
Log in

Nosema ceranae and RNA viruses in European and Africanized honeybee colonies (Apis mellifera) in Uruguay

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

Abstract

Nosema ceranae is one of the causative agents of Nosemosis, a severe disease that affects the honeybee Apis mellifera. The aim of the present work was to compare N. ceranae and RNA virus infections in Africanized bees (hybrid of Apis mellifera scutellata and A. m. mellifera) and European (Italian) bees (A. m. ligustica) under field conditions. Africanized and Italian healthy colonies were relocated to an Eucalyptus grandis plantation, a place where colonies inevitably acquire Nosemosis. Fifteen and 30 days after that, all colonies presented N. ceranae spores although Africanized bees were less infected than Italian bees. Sacbrood virus (SBV) and Black queen cell virus (BQCV) were detected in both races of bees, although Africanized bees presented a lower level of BQCV infection than Italian bees. At the end of the flowering period, Africanized colonies had a larger honeybee population and produced more honey than Italian colonies. These results suggest that Africanized bees may be able to limit N. ceranae and BQCV infections within the colony, and that this may allow them to be more productive.

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

Figure 1.
Figure 2.
Figure 3.
Figure 4.

Similar content being viewed by others

References

  • Antúnez, K., D`Alessandro, B., Corbella, E., Zunino, P. (2005) Detection of chronic bee paralysis virus and acute bee paralysis virus in Uruguayan honeybees. J. Invertebr. Pathol 90, 69–72

    Article  PubMed  Google Scholar 

  • Antúnez, K., D’Alessandro, B., Corbella, E., Ramallo, G., Zunino, P. (2006) Honeybee viruses in Uruguay. J. Invertebr. Pathol 93, 67–70

    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 

  • Aurori, C.M., Dezmirean, D.S., Marghitas, L.A., Moritz, R.F.A. (2011) Nosema apis and N. ceranae in Western honeybee (Apis mellifera) – geographical distribution and current methods of diagnosis. Animal Science and Biotechnologies, Bulletin UASVM, pp. 63–70

  • 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  CAS  PubMed  Google Scholar 

  • Bailey, L., Ball, B.V. (1991) Honey bee pathology. Academic, London

    Google Scholar 

  • Bailey, L., Ball, B.V., Perry, J.N. (1983) Association of viruses with two protozoal pathogens of the honey bee. Ann. Appl. Biol 103, 13–20

    Article  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) The growing prevalence of Nosema cearanae in honey bees in Spain, an emerging problem for the last decade. Res. Vet. Sc. 93, 150–155

    Article  Google Scholar 

  • Botías, C., Martín-Hernández, R., Barrios, L., Meana, A., Higes, M. (2013) Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet. Res . doi:10.1186/1297-9716-44-25

    PubMed  Google Scholar 

  • Bowen-Walker, P., Martin, S.J., Gunn, A. (1999) The transmission of Deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J. Invertebr. Pathol 73, 101–106

    Article  PubMed  Google Scholar 

  • Burgett, M., Shorney, S., Cordara, J., Gardiol, G., Sheppard, W.S. (1995) The present status of Africanized honey bees in Uruguay. Am. Bee J 135, 328–330

    Google Scholar 

  • Calderon, R.A., van Veen, J.W., Sommeijer, M.J., Sanchez, L.A. (2010) Reproductive biology of Varroa destructor in Africanized honey bees (Apis mellifera). Exp. Appl. Acarol 50, 281–297

    Article  CAS  PubMed  Google Scholar 

  • Collet, T., Ferreira, K.M., Arias, M.C., Soares, A.E.E., Del Lama, M.A. (2006) Genetic structure of Africanized honeybee populations (Apis mellifera L.) from Brazil and Uruguay viewed through mitochondrial DNA COI–COII patterns. Heredity 97, 329–335

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  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  CAS  PubMed Central  PubMed  Google Scholar 

  • de Miranda, J.R., Cordoni, G., Budge, G. (2010) The Acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex. J. Invertebr. Pathol 103(Suppl 1), S30–47

    Article  PubMed  Google Scholar 

  • Dietz, A. (1992) Honey bees of the world. In: Graham, J.M. (ed.) The hive and the honey bee, pp. 23–71. Dadant, Hamilton, Illinois

    Google Scholar 

  • Diniz, N.M., Soares, A.E.G., Sheppard, W.S., Del Lama, M.A. (2003) Genetic structure of honeybee populations from southern Brazil and Uruguay. Gen. Mol. Res 26, 47–52

    CAS  Google Scholar 

  • Franck, P., Garnery, L., Loiseau, A., Oldroyd, B.P., Hepburn, H.R., Solignac, M., Cornuet, J.M. (2001) Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data. Heredity 86, 420–430

    Article  CAS  PubMed  Google Scholar 

  • Fries, I. (1997) Protozoa. In: Morse, R.A., Flottum, K. (eds.) Honey bee pest, predators and diseases, pp. 57–76. The A.I. Root Company, Medina, OH

    Google Scholar 

  • Fries, I. (2010) Nosema ceranae in European honey bees (Apis mellifera). J. Invertebr. Pathol 103(Suppl 1), S73–79

    Article  PubMed  Google Scholar 

  • Fries, I., Feng, F., da Silva, A., Slemenda, S.B., Pieniazek, N.J. (1996) Nosema ceranae sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honeybee Apis cerana (Hymenoptera, Apidae). Eur. J. Protistol 32, 356–365

    Article  Google Scholar 

  • Fries, I., Slemenda, S.B., Da Silva, A., Pieniazek, N.J. (2003) African honey bees (Apis mellifera scutellata) and nosema (Nosema apis) infections. J. Apic. Res 42, 13–15

    Google Scholar 

  • Garnery, L., Franck, P., Baudry, E., Vautrin, D., Cornuet, J., Solignac, M. (1998) Genetic diversity of the west European honey bee (Apis mellifera mellifera and A. m. iberica) I. Mitochondrial DNA. Genet. Sel. Evol 30, S31–S47

    Article  CAS  Google Scholar 

  • Genersch, E., Aubert, M. (2010) Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet. Res 41, 54

    Article  PubMed  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. Microbiol 76, 3032–3038

    Article  CAS  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Higes, M., Martín-Hernández, R., Botías, C., Bailón, E.G., 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 

  • Invernizzi, C., Abud, C., Tomasco, I.H., Harriet, J., Ramallo, G., Campa, 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 

  • Invernizzi, C., Antúnez, K., Campa, J., Harriet, J., Mendoza, Y., Santos, E., Zunino, P. (2011a) Situación sanitaria de las abejas melíferas en Uruguay. Veterinaria 47, 15–27

    Google Scholar 

  • Invernizzi, C., Santos, E., Garcia, E., Daners, G., Di Landro, R., Saadoun, A., Cabrera, C. (2011b) Sanitary and nutritional characterization of honeybee colonies in Eucalyptus grandis plantations. Arch. Zootec 60, 1303–1314

    Article  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). Proc. Natl. Acad. Sci. U.S.A 106, 14790–14795

    Article  CAS  PubMed Central  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 

  • Kukielka, D., Esperon, F., Higes, M., Sanchez-Vizcaino, J.M. (2008) A sensitive one-step real-time RT-PCR method for detection of deformed wing virus and black queen cell virus in honey bee Apis mellifera. J. Virol. Methods 147, 275–281

    Article  CAS  PubMed  Google Scholar 

  • L’Arrivee, J.C.M. (1965) Tolerance of honey bees to nosema disease. J. Invert. Pathol 7, 408–413

    Article  Google Scholar 

  • Malone, L.A., Giacon, H.A., Hunapo, R.J., McIvor, C.A. (1992) Response of New Zealand honey bee colonies to Nosema apis. J. Apicl. Res. 31, 135–140

    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

    Article  Google Scholar 

  • Malone, L.A., Stefanovic, D. (1999) Comparison of the responses of two races of honeybees to infection with Nosema apis Zander. Apidologie 30, 375–382

    Article  Google Scholar 

  • Maori, E., Lavi, S., Mozes-Koch, R., Gantman, Y., Peretz, Y., Edelbaum, O., Tanne, E., Sela, I. (2007) Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra- and inter-species recombination. J. Gen. Virol 88, 3428–3438

    Article  CAS  PubMed  Google Scholar 

  • Martin, S.J. (2001) The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. J. Appl. Ecol 38, 1082–1093

    Article  Google Scholar 

  • Martin, S.J., Medina, L.M. (2004) Africanized honeybees have unique tolerance to Varroa mites. Trends Parasitol 20, 112–114

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Medici, S.K., Sarlo, E.G., Porrini, M.P., Braunstein, M., Eguaras, M.J. (2011) Genetic variation and widespread dispersal of Nosema ceranae in Apis mellifera apiaries from Argentina. Parasitol. Res 110, 859–864

    Article  PubMed  Google Scholar 

  • Mendoza, Y., Harriet, J., Campa, J., Katz, H., Ramallo, G., Díaz-Cetti, S., Invernizzi, C. (2012) Control de Nosema ceranae en colonias de abejas (Apis mellifera) en forestaciones de Eucalyptus grandis. Agrociencia. In press.

  • MGAP (2010) Decreto presidencial 14-6-2010. Oxcitetraciclina y Fumagilina- Retiro y/o limitación de uso en Uruguay [on line] http://www.mgap.gub.uy (accessed on 12 December 2011)

  • Palacios, G., Hui, J., Quan, P.L., Kalkstein, A., Honkavuori, K.S., et al. (2008) Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. J. Virol 82, 6209–17

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pickard, R.S., El-Shemy, A.A.M. (1989) Seasonal variation in the infection of honeybee colonies with Nosema apis Zander. J. Apic. Res. 28, 93–100

    Google Scholar 

  • R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.

  • 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 

  • Rinderer, T., Sylvester, H., Buco, S., Lancaster, A., Herbert, W., Collins, M., Hellmich, H.L. (1987) Improved simple techniques for identifying Africanized and European honey bees. Apidologie 18, 179–196

    Article  Google Scholar 

  • Rinderer, T.E., Collins, A.M., Brown, M.A. (1983) Heritabilities and correlations of the honey bee: response to Nosema apis, longevity, and alarm response to isopentyl acetate. Apidologie 14, 79–85

    Article  Google Scholar 

  • Rodríguez, M., Vargas, M., Gerding, M., Navarro, H., Antúnez, K. (2012) Viral infection and Nosema ceranae in honey bees (Apis mellifera) in Chile. J. Apic. Res 51, 285–287

    Article  Google Scholar 

  • Ruttner, F. (1988) Biogeography and taxonomy of honeybees. Springer, Berlin

    Book  Google Scholar 

  • Ryba, S., Titera, D., Schodelbauerova-Traxmandlova, I., Kindlmann, P. (2012) Prevalence of honeybee viruses in the Czech Republic and coinfections with other honeybee disease. Biologia 67, 590–595

    Article  Google Scholar 

  • Stoltz, D., Shen, X.R., Boggis, C., Sisson, G. (1995) Molecular diagnosis of Kashmir bee virus infection. J. Apic. Res. 34, 153–160

    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 

  • Vandame, R., Palacio, M.A. (2010) Preserved honey bee health in Latin America: A fragile equilibrium due to low-intensity agriculture and beekeeping? Apidologie 41, 243–255

    Article  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 Central  PubMed  Google Scholar 

  • Walsh, P.S., Metzger, D.A., Higuchi, R. (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506–513

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Winston, M.L., Katz, S.J. (1981) Longevity of cross-fostered honeybee workers of European and Africanized races. Can. J. Zool 59, 1571–1575

    Article  Google Scholar 

  • Winston, M.L., Katz, S.J. (1982) Foraging differences between cross-fostered honeybee workers (Apis mellifera) of European and Africanized races. Behav. Ecol. Sociobiol 10, 125–129

    Article  Google Scholar 

  • Yang, X., Cox-Foster, D.L. (2005) Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc. Natl. Acad. Sci. U.S.A 102, 7470–7475

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Instituto de Investigación Agropecuaria, Ruta 11 Km, 70000, Colonia, Uruguay

    Yamandú Mendoza

  2. Departamento de Microbiología, Instituto de Investigaciones Biológicas Clemente Estable, Avenida Italia 3318, 11600, Montevideo, Uruguay

    Karina Antúnez, Belén Branchiccela & Matilde Anido

  3. Facultad de Ciencias, Iguá 4225, 11400, Montevideo, Uruguay

    Estela Santos & Ciro Invernizzi

Authors
  1. Yamandú Mendoza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karina Antúnez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Belén Branchiccela
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matilde Anido
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Estela Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ciro Invernizzi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karina Antúnez.

Additional information

Manuscript editor: Stan Schneider

Nosema ceranae et virus à ARN dans des colonies d’abeilles européennes et africanisées ( Apis mellifera ) en Uruguay

Nosemose / virus / résistance / haplotypes / abeille

Nosema ceranae und RNA-Viren in europäischen und afrikanisierten Honigbienenvölkern ( Apis mellifera ) in Uruguay

Nosemosis / RNA-Viren / Resistenz / Bienen-Haplotypen

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mendoza, Y., Antúnez, K., Branchiccela, B. et al. Nosema ceranae and RNA viruses in European and Africanized honeybee colonies (Apis mellifera) in Uruguay. Apidologie 45, 224–234 (2014). https://doi.org/10.1007/s13592-013-0241-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-013-0241-6

Keywords

Search

Navigation