Honey Bee Infection Caused by Nosema spp. in Lithuania

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The infection of Lithuanian honey bee colonies by Nosema apis and N. ceranae and the consequences were analysed over a four-year (2011 - 2014) period. Both mono-infection either by N. apis or N. ceranae, and co-infection by both Nosema species, were found. There was a decrease in the percentage of Nosema infected colonies during the four-year study period. There were fewer colonies infected by N. ceranae, whereas the number of colonies with N. apis remained approximately at the same level during the study. The prevalence of both types of Nosema in honey bee colonies varied seasonally, i.e. there was a higher percentage of colonies infected in spring and summer but very rarely was Nosema detected in autumn. Mono-infection by N. apis, and co-infection by both Nosema species, were significantly more often recorded in weak and moderate colonies than in strong colonies. Mono-infection by N. ceranae was more often detected in weak colonies than in moderate and strong colonies, but more often detected in strong than in moderate colonies. A moderate link between a high prevalence of N. ceranae infection and an increased risk for winter colony mortality was observed.

Alaux, C., Folschweiller, M., McDonnell, C., Beslay, D., Cousin, M., Dussaubat, C., Brunet, J.L., Le Conte, Y. (2011). Pathological effects of the microsporidium Nosema ceranae on honey bee queen physiology (Apis mellifera). Journal of Invertebrate Pathology, 106, 380-385. DOI: 10.1016/j.jip.2010.12.005

Anderson, D.L., & Giacon, H. (1992). Reduced pollen collection by honeybee (Hymenoptera, Apidae) colonies infected with Nosema apis and sacbrood virus. Journal of Economic Entomology, 85, 47–51. DOI: 10.1093/jee/85.1.47

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). Environmental Microbiology, 11, 2284–2290. DOI: 10.1111/j.1462-2920.2009.01953.x

Aplinkos būklė 2011. Tik faktai (2012). [Environment State in 2011. The facts]. Aplinkos apsaugos agentūra, Všį Gamtos paveldo fondas, Vilnius.

Blažytė-Čereškienė, L., Skrodenytė-Arbačiauskienė, V., & Būda. V. (2014). Microsporidian parasites of honey bees Nosema ceranae and N. apis in Lithuania: supplementary data on occurrence along Europe. Journal of Apicultural Research, 53(3), 374-376. DOI: 10.3896/IBRA.

Botías, C., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A., Martínez-Salvador, A., Pilar De La Rúa, Meana, A., Higes, M. (2012). The growing prevalence of Nosema ceranae in honey bees in Spain, an emerging problem for the last decade. Research in Veterinary Science, 93, 150-155. DOI: 10.1016/j.rvsc.2011.08.002

Budge, G., Powell, M., Roberts, K., Adams, I., Jones, B., Marris, G., Laurenson, L., Wilkins, S., Pietravalle, S., Brown, M. (2010). What has Nosema got to do with losses? Monitoring both Nosema species in the UK. In Proceedings of the 4th European Conference of Apidology (p. 48). Ankara - Turkey.

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. Journal of Insect Physiology, 58, 1090–1095. DOI: 10.1016/j.jinsphys.2012.04.016

Chauzat, M.-P., Higes, M., Martin-Hernandez, R., Meana, A., Cougoule, N., Faucon, J.P. (2007). Presence of Nosema ceranae in French honey bee colonies. Apidologie, 46, 127–128. DOI: 10.3896/IBRA.

Chauzat, M.-P., Laurent, M., Riviere, M.-P., Saugeon, C., Hendrikx, P., Ribiere-Charbert, M. (2014). A pan-European epidemiological study on honeybee colony losses 2012-2013 - EPILOBEE - 2012-2013. Retrieved October 22, 2014 from, https://ec.europa.eu/food/sites/food/files/animals/live_animals/bees/docs/bee-report_en.pdf

Chauzat, M.-P., Martel, A.-C., Zeggane, S., Drajnudel, P., Schurr, F., Clément, M.-C., Ribière-Chabert, M., Aubert, M., Faucon, J.-P. (2010). A case control study and a survey on mortalities of honey bee colonies (Apis mellifera) in France during the winter of 2005-6. Journal of Apicultural Research, 49, 40−51. DOI: 10.3896/IBRA.

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. Journal of Invertebrate Pathology, 97, 186–188. DOI: 10.1016/j.jip.2007.07.010

Copley, T.R. & Jabaji, S.H. (2011). Honeybee glands as possible infection reservoirs of Nosema ceranae and Nosema apis in naturally infected forager bees. Journal of Applied Microbiology, 112, 15–24. DOI: 10.1111/j.1365-2672.2011.05192.x

Cox-Foster, D.L., Conlan, S., Holmes, E.C., Palacios, G., Evans, J.D., Moran, N.A., ... Lipkin, W.I. (2007). A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318, 283–287. DOI: 10.1126/science.1146498

Dainat, B., Evans, J.D., Chen, Y.P., Gauthier, L., Neumann, P. (2012). Predictive markers of honey bee colony collapse. PLoS One, 7, e32151. DOI: 10.1371/journal.pone.0032151

Derakhshifar, I., Köglberger, H., Oberlerchner, J., Moosbeckhofer, R. (2009). Incidence of Nosema spp. and colony performance in Austria 2006–2008. In Nosema disease: lack of knowledge and work standardization (COST Action FA0803). Guadalajara – Spain. Retrieved January 25, 2012 from, http://www.coloss.org/news/nosema-workshop-proceedings-online

Dussaubat, C., Maisonnasse, A., Alaux, C. Tchamitchan, S., Brunet, J.L., Plettner, E., Belzunces, L.P., Le Conte, Y. (2010). Nosema spp. infection alters pheromone production in honey bees (Apis mellifera). Journal of Chemical Ecology, 36, 522–525. DOI: 10.1007/s10886-010-9786-2

Ellis, J.D. & Munn, P.A. (2005). The worldwide health status of honey bees. Bee World, 86, 88–101. DOI: 10.1080/0005772X.2005.11417323

Fries, I. (2010). Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology, 103, S73–79. DOI: 10.1016/j.jip.2009.06.017

Fries, I., Ekbohm, G., & Villumstad, E. (1984). Nosema apis, sampling techniques and honey yield. Journal of Apicultural Research, 23, 102–105.

Fries, I., Feng, F., da Silva, A., Slemenda, S.B., Pieniazek, N.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). European Journal of Protistology, 32, 356−365. DOI: 10.1016/S0932-4739(96)80059-9

Gajda, A. & Topolska, G. (2009). Most probable causes of colony losses during the winter of 2008/2009 in Poland. In Proceedings of 5th COLOSS conference (p. 41). Montpellier - France.

Genersch, E., von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Büchler, R., ... Rosenkranz, P. (2010). The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie, 41, 332–352. DOI: 10.1051/apido/2010014

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? Applied and Environmental Microbiology, 76, 3032–3038. DOI: 10.1128/AEM.03097-09

Higes, M., Martín, R., & Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of Invertebrate Pathology, 92, 93–95. DOI: 10.1016/j.jip.2006.02.005

Higes, M., Garcia-Palencia, P., Martin-Hernandez, R., & Meana, A. (2007). Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). Journal of Invertebrate Pathology, 94, 211–217. DOI: 10.1016/j.jip.2006.11.001

Higes, M., Martin-Hernandez, R., Botias, C., Bailon, E.G., Gonzalez-Porto, A.V., Barrios, L., ... Meana, A. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, 10, 2659–2669. DOI: 10.1111/j.1462-2920.2008.01687.x

Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A.V., García-Palencia, P., Meana, A., ... Bernal, J.L. (2009). Honey bee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports, 1, 110–113. DOI: 10.1111/j.1758-2229.2009.00014.x

Invernizzi, C., Abud, C., Tomasco, I.H., Harriet, J., Ramallo, G., Campá, J., ... Mendoza, Y. (2009). Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. Journal of Invertebrate Pathology, 101, 150–153. DOI: 10.1016/j.jip.2009.03.006

Klee, J., Besana, A.M., Genersch, E., Gisder, S., Nanetti, A., Tam, D.Q., ... & Paxton, R.J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology, 96, 1–10. DOI: 10.1016/j.jip.2007.02.014

Korpela, S. (2009). Nosema situation in Finland. In Proceedings of 5th COLOSS conference (p. 48). Montpellier - France.

Mariani, F., Maggi, M., Porrini, M., Fuselli, S., Caraballo, G., Brasesco, C., Barrios, C., Principal, J., Martin, E. (2012). Parasitic interactions between Nosema spp. and Varroa destructor in Apis mellifera colonies. Zootecnia Tropical, 30(1), 81-90.

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. Applied and Environmental Microbiology, 73, 6331–6338. DOI: 10.1128/AEM.00270-07

Mayack, C. & Naug, D. (2009). Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. Journal of Invertebrate Pathology, 100, 185–188. DOI: 10.1016/j.jip.2008.12.001

Michalczyk, M., Sokół, R., & Szczerba-Turek, A. (2013). Phylogenetic analysis of Nosema apis and Nosema ceranae small subunit 16S rRNA in honey bees (Apis mellifera) from north-eastern Poland. Medycyna Weterynaryjna, 69: 733-735.

Michalczyk, M., Sokół, R., Szczerba-Turek, A., Bancerz-Kisiel, A. (2011). A comparison of the effectiveness of the microscopic method and the multiplex PCR method in identifying and discriminating the species of Nosema spp. spores in worker bees (Apis mellifera) from winter hive debris. Polish Journal of Veterinary Sciences, 14, 385-391. DOI: 10.2478/v10181-011-0058-z

OIE (2008) Nosemosis of honey bees. OIE Terrestrial Manual.

Paxton, R.J. (2010). Does infection by Nosema ceranae cause Colony Collapse Disorder in honey bees (Apis mellifera)? Journal of Apicultural Research, 49(1), 80-84. DOI: 10.3896/IBRA.

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. DOI: 10.1051/apido:2007037

Pickard, R.S. & El-Shemy, A.A.M. (1989). Seasonal variation in the infection of honeybee colonies with Nosema apis Zander. Journal of Apicultural Research, 28, 93-100.

Ratnieks, F.L.W. & Carreck, N.L. (2010). Clarity on honey bee collapse? Science, 327, 152-153. DOI: 10.1126/science.1185563

Stevanovic, J., Stanimirovic, Z., Genersch, E., Kovacevic, S. R., 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, 42, 49–58. DOI: 10.1051/apido/2010034

Stevanovic, J., Simeunovic, P., Gajic, B., Lakic, N., Radovic, D., Fries, I., Stanimirovic, Z. (2013). Characteristics of Nosema ceranae infection in Serbian honey bee colonies. Apidologie, 44, 522-536. DOI: 10.1007/s13592-013-0203-z

Tapaszti, Z., Forgách, P., Kövágó, C., Békési, L., Bakonyi, T., & Rusvai, M. (2009). First detection and dominance of Nosema ceranae in Hungarian honeybee colonies. Acta Veterinaria Hungarica, 57, 383-388. DOI: 10.1556/AVet.57.2009.3.4

Tlak Gajger, I., Vugrek, O., Grilec, D., Petrinec, Z. (2010). Prevalence and distribution of Nosema ceranae in Croatian honeybee colonies. Veterinární medicína, 55: 457–462.

Topolska, G., Gajda, A., & Hartwig, A. (2008). Polish honey bee colony-loss during the winter of 2007/2008. Journal of Apicultural Science, 52, 95–103.

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. Journal of Invertebrate Pathology, 109, 187-193. DOI: 10.1016/j.jip.2011.11.001

Van Engelsdorp, D., Evans, J.D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B.K., ... Pettis, J.S. (2009). Colony collapse disorder: a descriptive study. PLoS One, 4, e6481. DOI: 10.1371/journal.pone.0006481

Vejsnæs, F., Nielsen, S.L., & Kryger, P. (2010). Factors involved in the recent increase in colony losses in Denmark. Journal of Apicultural Research, 49, 109–110. DOI: 10.3896/IBRA.

Whitaker, J., Szalanski, A.L., & Kence, M. (2011). Molecular detection of Nosema ceranae and N. apis from Turkish honey bees. Apidologie, 42, 174-180. DOI: 10.1051/apido/2010045

Zander, E. (1909). Tierische Parasiten als Krankenheitserreger bei der Biene. Münchener Bienenzeitung, 31: 196-204.

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