Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter October 18, 2018

Detection of two Microsporidia pathogens of the European honey bee Apis Mellifera (Insecta: Apidae) in Western Siberia

Yuri S. Tokarev, Zimfira Y. Zinatullina, Anastasiya N. Ignatieva, Oksana N. Zhigileva, Julia M. Malysh and Yulia Y. Sokolova
From the journal Acta Parasitologica

Abstract

Two species of microsporidia, Nosema apis and Nosema ceranae, occur regularly and cause significant losses in apiculture throughout the world. N. ceranae is thought to be an emerging pathogen of the European honey bee which is replacing N. apis. Microscopic analysis of honey bees collected in Tyumen region, South-Western Siberia, suggested presence of two microsporidial pathogens slightly differing in spore size and shape. PCR detection using species-specific primer sets 312APIS and 218MITOC followed by PCR product sequencing confirmed the diagnosis of N. apis and N. ceranae, respectively. Microsporidia were present in private apiaries through 2008-2010, and among 21 colonies from 7 localities, two colonies were infected with both pathogens, while infections with N. apis only were detected in 8, and with N. ceranae only in 13 colonies. These data suggest that N. ceranae is widely spread in South-Western Siberia alongside with N. apis and is able to persist in the regions with average January temperatures below –18°C.

Acknowledgements

The research is supported by Russian Scientific Foundation, grant No. 16-14-00005.

References

Bacandritsos N., Granato A., Budge G., Papanastasiou I., Roinioti E., Caldon M. et al. 2010. Sudden deaths and colony population decline in Greek honey bee colonies. Journal of Invertebrate Pathology, 105, 335–340. org/10.1016/j.jip.2010.08.004Search in Google Scholar

Cepero A., Ravoet J., Gómez-Moracho T., Bernal J.L., Del Nozal M.J., Bartolomé C. et al. 2014. Holistic screening of collapsing honey bee colonies in Spain: a case study. BMC Research Notes, 7, 649. org/10.1186/1756-0500-7-649Search in Google Scholar

Chen Y., Evans J.D., Smith I.B., Pettis J.S. 2008. Nosema ceranae is a long-present and wide-spread microsporidean infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology, 97, 186–188. org/10.1016/j.jip.2007.07.010Search in Google Scholar

Emsen B, Guzman-Novoa E, Hamiduzzaman MM, Eccles L, Lacey B, Ruiz-Pérez RA, Nasr M. 2016. Higher prevalence and levels of Nosema ceranae than Nosema apis infections in Canadian honey bee colonies. Parasitology Research. 115, 175–181. 10.1007/s00436-015-4733-3Search in Google Scholar PubMed

Fries I. 2010. Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology, 103, S73–S79. org/10.1016/j.jip.2009.06.017Search in Google Scholar

Gisder S, Hedtke K, Möckel N, Frielitz NC, Linde A, Genersch E. 2010. Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Applied and Environmental Microbiology, 76, 3032–303810.1128/AEM.03097-09Search in Google Scholar PubMed PubMed Central

Invernizzi C., Abuda C., Tomasco I., Harriet J., Ramallo G., Campá J. et al. 2009. Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. Journal of Invertebrate Pathology, 101, 150–153. org/10.1016/j.jip.2009.03.006Search in Google Scholar

Ivgin Tunca R., Oskay D., Gosterit A., Tekin O.K. 2016. Does Nosema ceranae Wipe Out Nosema apis in Turkey? Iranian Journal of Parasitology, 11, 259–264.Search in Google Scholar

Kasprzak S., Topolska G. 2007. Nosema ceranae (Eukaryota: Fungi: Microsporea) — nowy pasożyt pszczoły miodnej Apis mellifera L. Wiadomosci Parazytologiczne, 53, 281–284. (In Polish)Search in Google Scholar

Klee J., Besana A., Genersch E., Gisder S., Nanetti A., Tam D.Q. et al. 2007. Widespread dispersal of the microsporidium Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology, 96, 1– 10. org/10.1016/j.jip.2007.02.014Search in Google Scholar

Martín-Hernández R., Meana A., Prieto L., Martinez Salvador A., Garrido- Bailón E., Higes M. et al. 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73, 6331–6338. org/10.1128/AEM.00270-07Search in 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. org/10.1051/apido:2007037Search in Google Scholar

Ravoet J., Maharramov J., Meeus I., De Smet L., Wenseleers T., Smagghe G. et al. 2013. Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PLoS One, 8, e72443. org/10.1371/journal.pone.0072443Search in Google Scholar

Retschnig G, Williams GR, Schneeberger A, Neumann P. 2017. Cold ambient temperature promotes Nosema spp. intensity in honey bees (Apis mellifera). Insects. 8, pii: E20. 10.3390/insects8010020Search in Google Scholar PubMed PubMed Central

Ryan N.J., Sutherland G., Coughlan K., Globan M., Doultree J., Marshall J. et al. 1993. A new trichrome-blue stain for detection of microsporidial species in urine, stool, and nasopharyngeal specimens. Journal of Clinical Microbiology, 31, 3264–326910.1128/jcm.31.12.3264-3269.1993Search in Google Scholar PubMed PubMed Central

Sambrook J., Fritsch E., Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New YorkSearch in Google Scholar

Shumkova R, Georgieva A, Radoslavov G, Sirakova D, Dzhebir G, Neov B, Bouga M, Hristov P. 2018.The first report of the prevalence of Nosema ceranae in Bulgaria. PeerJ. 6, e4252. 10.7717/peerj.4252Search in Google Scholar PubMed PubMed Central

Stevanovic J., Schwarz R.S., Vejnovic B., Evans J.D., Irwin, R.E., Glavinic U. et al. 2016. Species-specific diagnostics of Apis mellifera trypanosomatids: A nine-year survey (2007-2015) for trypanosomatids and microsporidials in Serbian honey bees. Journal of Invertebrate Pathology, 139: 6–11. org/10.1016/j.jip.2016.07.001Search in Google Scholar

Stevanovic J., Staminirovic Z., Genersch E., Kovacevic S.R., Ljubenkovic J., Radakovic M. et al. 2011. Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie, 42, 49. org/10.1051/apido/2010034Search in Google Scholar

Tokarev Y.S., Ignatieva A.N., Zinatullina Z.Y. 2010. Molecular detection of Nosema disease. Pchelovodstvo, 5, 18–19 (In Russian)Search in Google Scholar

Vogelstein B., Gillespie D. 1979. Preparative and analytical purification of DNA from agarose. Proceedings of the National Academy of Sciences of the United States of America, 76, 615–61910.1073/pnas.76.2.615Search in Google Scholar PubMed PubMed Central

Weber R., Bryan R.T., Owen R.L., Wilcox C.M., Gorelkin L., Visvesvara G. 1992. Improved light microscopic detection of Microsporida spores in stool and duodenal aspirates. The New England Journal of Medicine, 4, 161–166. org/10.1056/NEJM199201163260304Search in Google Scholar

Yoshiyama M., Kimura K. 2011. Distribution of Nosema ceranae in the European honeybee, Apis mellifera in Japan. Journal of Invertebrate Pathology, 106, 263–267. org/10.1016/j.jip.2010.10.010Search in Google Scholar

Zander E. 1909. Tierische Parasiten als Krankheitserreger bei der Biene. Leipziger Bienenzeitung, 24, 147–150Search in Google Scholar

Zinatullina Z.Y. 2017. Methods of wintering bee colonies in the apiary infected with Nosema ceranae. The Bulletin of Krasnoyarsk State Agrarian University, 124, 40–44. (In Russian)Search in Google Scholar

Zinatullina Z.Y., Ignatieva A.N., Zhigileva O.N., Tokarev Y.S. 2011. "Asian" nosemosis in Russia. Pchelovodstvo, 10, 24–26. (In Russian)Search in Google Scholar

Received: 2018-04-10
Revised: 2018-07-09
Accepted: 2018-07-11
Published Online: 2018-10-18
Published in Print: 2018-12-19

© 2018 W. Stefański Institute of Parasitology, PAS

Scroll Up Arrow