Investigation of the Relationship Between Nosema spp. and Black Queen Cell Virus in Honey Bees in Türkiye

Aykut Zerek; Ipek Erdem; Murat Şevik

doi:10.13102/sociobiology.v73i2.12648

Authors

Aykut Zerek Department of Parasitology, Veterinary Faculty, Hatay Mustafa Kemal University, Antakya, 31060 Hatay, Türkiye
Ipek Erdem Department of Parasitology, Veterinary Faculty, Hatay Mustafa Kemal University, Antakya, 31060 Hatay, Türkiye
Murat Şevik Department of Virology, Veterinary Faculty, Necmettin Erbakan University, Ereğli, 42310 Konya, Türkiye

DOI:

https://doi.org/10.13102/sociobiology.v73i2.12648

Keywords:

Honey bee, Black queen cell virus (BQCV), Nosema ceranae, genetic characterization, Türkiye

Abstract

Significant losses in honey bee colonies have been reported worldwide, largely due to pathogens affecting bee health. Among these, Nosema species and Black queen cell virus (BQCV) are particularly prominent. This study aimed to determine the prevalence of Nosema spp. and BQCV in honey bees, investigate the genetic diversity of BQCV, and assess Nosema spp. and BQCV potential association. Adult honey bee samples were collected from 62 randomly selected apiaries in Hatay Province, Türkiye. Nosema spp. were detected and identified at the species level using a multiplex PCR assay, while BQCV was detected by a one-step real-time RT-PCR assay. BQCV was found in 21.0% of the apiaries, and Nosema ceranae infection in 48.4%. Co-infection occurred in 8.1% of the apiaries. No significant association was observed between N. ceranae and BQCV positivity. However, shared use of beekeeping equipment among hives was significantly associated with both pathogens. Phylogenetic analysis of the BQCV helicase gene revealed that isolates identified in this study clustered with Asian-origin sequences, suggesting the circulation of different BQCV genotypes in Türkiye. These findings provide insight into pathogen prevalence and co-occurrence in honey bee colonies. Further studies are warranted to characterize BQCV genotypes and to explore the relationship between Nosema spp. and BQCV in Türkiye in greater detail.

Downloads

Download data is not yet available.

References

Abdi, K., Ben Said, M., Crotti, E., Masmoudi, A.S. & Cherif, A. (2023). The promise of probiotics in honeybee health and disease management. Archives of Microbiology, 205: 73.

Aizen, M.A. & Harder, L.D. (2009). The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Current Biology, 19: 915-918.

Akpınar, R.K., Gürler, A.T., Bölükbaş, C.S., Kaya, S., Arslan, S., Aydın, C., Türlek, Ş.Ö., Çelik, S.N., Beyazıt, A., Öncel, T., Erol, U., Çiftci, A.T., Bastem, Z., Ünal, H.H., Şenel, M., Bozdeveci, A., Karaoğlu, Ş.A., Yaldız, M., Güven, G., Küçükoğlu, B. & Kurt, M. (2024). Prevalence and phylogenetic network analysis of Nosema apis and Nosema ceranae isolates from honeybee colonies in Türkiye. Acta Parasitologica, 69: 1538-1546.

Al Naggar, Y. & Paxton, R.J. (2020). Mode of transmission determines the virulence of Black queen cell virus in adult honey bees, posing a future threat to bees and apiculture. Viruses, 12: 535.

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). Environmental Microbiology, 12: 774-782.

Avci, O., Oz, M.E. & Dogan, M. (2022). Silent threat in honey bee colonies: Infection dynamics and molecular epidemiological assessment of Black queen cell virus in Turkey. Archives of Virology, 167: 1499–1508.

Aydın, L., Doğanay, A., Oruç, H.H., Yeşilbağ, K., Bakırcı, S., Girişgin, O.A., Güneş, N., Muz, M.N., Borum, A.E. & Güneş, M.E. (2017). Bal arısı yetiştiriciliği, ürünleri, hastalıkları. Bursa: Dora Basım-Yayın Dağıtım Ltd. Şti.

Bailey, E. (1975). Biochemistry of insect flight. In D.J. Candy & B.A. Kilby (Eds.), Insect Biochemistry and Function. London: Chapman and Hall.

Bailey, L., & Woods, R.D. (1977). Two more small RNA viruses from honey bees and further observations on sacbrood and acute bee paralysis viruses. Journal of General Virology, 37: 175-182.

Bailey, L., Ball, V.B. & Perry, J.N. (1983). Association of viruses with two protozoal pathogens of the honey bee. Annals of Applied Biology, 103: 13-20.

Barnett, E.A., Charlton, A.J. & Fletcher, M.R. (2007). Incidents of bee poisoning with pesticides in the United Kingdom, 1994–2003. Pest Management Science, 63: 1051-1057.

Benjeddou, M., Leat, N., Allsopp, M. & Davison, S. (2002). Development of infectious transcripts and genome manipulation of Black queen-cell virus of honey bees. Journal of General Virology, 83: 3139-3146.

Berényi, O., Bakonyi, T., Derakhshifar, I., Köglberger, H. & Nowotny, N. (2006). Occurrence of six honeybee viruses in diseased Austrian apiaries. Applied and Environmental Microbiology, 72: 2414-2420.

Bordin, F., Zulian, L., Granato, A., Caldon, M., Colamonico, R., Toson, M., Trevisan, L., Biasion, L. & Mutinelli, F. (2022). Presence of known and emerging honey bee pathogens in apiaries of Veneto region (Northeast of Italy) during spring 2020 and 2021. Applied Sciences, 12: 2134.

Cagirgan, A.A., Yildirim, Y. & Usta, A. (2020). Phylogenetic analysis of deformed wing virus, Black queen cell virus and acute bee paralysis viruses in Turkish honeybee colonies. Medycyna Weterynaryjna, 76: 480-484.

Chagas, D.B., Monteiro, F.L., Barcelos, L.S., Frühauf, M.I., Ribeiro, L.C., de Lima, M., Hübner, S.O. & Fischer, G. (2020). Black queen cell virus and Nosema ceranae coinfection in Africanized honey bees from southern Brazil. Pesquisa Veterinária Brasileira, 40: 892-897.

Chantawannakul, P., Ward, L., Boonham, N. & Brown, M. (2006). A scientific note on the detection of honeybee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Thai honeybee (Apis mellifera) apiary. Journal of Invertebrate Pathology, 91: 69-73.

Csáki, T., Heltai, M., Markolt, F., Kovács, B., Békési, L., Ladányi, M., Péntek-Zakar, E., Meana, A., Botías, C., Martín-Hernández, R. & Higes, M. (2015). Permanent prevalence of Nosema ceranae in honey bees (Apis mellifera) in Hungary. Acta Veterinaria Hungarica, 63: 358-369.

Doublet, V., Labarussias, M., de Miranda, J.R., Moritz, R.F., & Paxton, R.J. (2015). Bees under stress: Sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environmental Microbiology, 17: 969-983.

Dussaubat, C., Brunet, J.L., Higes, M., Colbourne, J.K., Lopez, J., Choi, J.H., Martín-Hernández, R., Botías, C., Cousin, M., McDonnell, C., Bonnet, M., Belzunces, L.P., Moritz, R.F., Le Conte, Y. & Alaux, C. (2012). Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS One, 7: e37017.

Gajda, A.M., Mazur, E.D., Bober, A.M., & Czopowicz, M. (2021). Nosema ceranae interactions with Nosema apis and Black queen cell virus. Agriculture, 11: 963.

Galajda, R., Valenčáková, A., Sučik, M., & Kandráčová, P. (2021). Nosema disease of European honey bees. Journal of Fungi, 7: 714.

Harju, V.A., Skelton, A., Clover, G.R., Ratti, C., Boonham, N., Henry, C.M., & Mumford, R.A. (2005). The use of real-time RT-PCR (TaqMan) and post-ELISA virus release for the detection of Beet necrotic yellow vein virus types containing RNA 5 and its comparison with conventional RT-PCR. Journal of Virological Methods, 123: 73-80.

Higes, M., García-Palencia, P., Martín-Hernández, R. & Meana, A. (2007). Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). Journal of Invertebrate Pathology, 94: 211-217.

Higes, M., Martín-Hernández, R., Botías, C., Bailón, E. G., González-Porto, A. V., Barrios, L., Del Nozal, M. J., Bernal, J. L., Jiménez, J. J., Palencia, P. G. & Meana, A. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, 10: 2659-2669.

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.

Kandemir, I., Kence, M. & Kence, A. (2000). Genetic and morphometric variation in honey bee (Apis mellifera L.) populations of Turkey. Apidologie, 31: 343-356.

Leat, N., Ball, B., Govan, V. & Davison, S. (2000). Analysis of the complete genome sequence of Black queen-cell virus, a picorna-like virus of honey bees. Journal of General Virology, 81: 2111-2119.

Martín-Hernández, R., Meana, A. & Prieto, L. (2007). Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73: 6331-6338.

Mayack, C., & Hakanoğlu, H. (2022). Honey bee pathogen prevalence and interactions within the Marmara Region of Turkey. Veterinary Sciences, 9: 573.

Mayack, C. & Naug, D. (2009). Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. Journal of Invertebrate Pathology, 100: 185-188.

Mendoza, Y., Antúnez, K., Branchiccela, B., Anido, M., Santos, E. & Invernizzi, C. (2014). Nosema ceranae and RNA viruses in European and Africanized honeybee colonies (Apis mellifera) in Uruguay. Apidologie, 45: 224-234.

Milićević, V., Radojičić, S., Kureljušić, J., Šekler, M., Nešić, K., Veljović, L., Maksimović Zorić, J. & Radosavljević, V. (2018). Molecular detection of black queen cell virus and Kashmir bee virus in honey. AMB Express, 8: 128.

Moharrami, M. & Modirrousta, H. (2018). Molecular identification of six honeybee viruses in Iranian apiaries. Archives of Razi Institute, 73: 311-318.

Muz, D. & Muz, M.N. (2018). A molecular epidemiological study of black queen cell virus in honeybees (Apis mellifera) of Turkey: The first genetic characterization and phylogenetic analysis of field viruses. Apidologie, 49: 89-100.

Oguz, B., Karapınar, Z., Dincer, E. & Deger, M.S. (2017). Molecular detection of Nosema spp. and Black queen-cell virus in honeybees in Van Province, Turkey. Turkish Journal of Veterinary and Animal Sciences, 41: 221-227.

Okur Gumusova, S., Albayrak, H., Kurt, M. & Yazici, Z. (2010). Prevalence of three honey bee viruses in Turkey. Veterinarski Arhiv, 80: 779-785.

Palmer, M.N., Smith, D.R. & Kaftanoğlu, O. (2000). Turkish honeybees: Genetic variation and evidence for a fourth lineage of Apis mellifera mtDNA. The Journal of Heredity, 91: 42-66.

Pettis, J.S., Johnson, J. & Dively, G. (2012). Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften, 99: 153-158.

Ramos-Cuellar, A.K., De la Mora, A., Contreras-Escareño, F., Morfín, N., Tapia-González, J.M., Macías-Macías, J.O., Petukhova, T., Correa-Benítez, A. & Guzmán-Novoa, E. (2024). Prevalence and infection intensity of honey bee (Apis mellifera) viral diseases in six regions of the state of Jalisco, Mexico. Revista Mexicana De Ciencias Pecuarias, 15: 471-482.

Retschnig, G., Williams, G.R., Mehmann, M.M., Yañez, O., de Miranda, J.R. & Neumann, P. (2014). Sex-specific differences in pathogen susceptibility in honey bees (Apis mellifera). PLoS One, 9: e85261.

Roberts, J.M.K., Anderson, D.L. & Durr, P.A. (2017). Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Scientific Reports, 7: 6925.

Schittny, D., Yañez, O. & Neumann, P. (2020). Honey bee virus transmission via hive products. Veterinary Sciences, 7: 96.

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.

Soklič, M. & Gregorc, A. (2016). Comparison of the two microsporidia that infect honey bees: A review. Agricultura, 13: 49-56.

Spurny, R., Přidal, A., Pálková, L., Kiem, H.K.T., de Miranda, J.R. & Plevka, P. (2017). Virion structure of Black queen cell virus, a common honeybee pathogen. Journal of Virology, 91: e02100-16.

Tantillo, G., Bottaro, M., Di Pinto, A., Martella, V., Di Pinto, P. & Terio, V. (2015). Virus infections of honeybees Apis mellifera. Italian Journal of Food Safety, 4: 5364.

Tapaszti, Z., Forgách, P., Kovágó, C., Topolska, G., Nowotny, N., Rusvai, M. & Bakonyi, T. (2009). Genetic analysis and phylogenetic comparison of Black queen cell virus genotypes. Veterinary Microbiology, 139: 227-234.

Tentcheva, D., Gauthier, L., Zappulla, N., Dainat, B., Cousserans, F., Colin, M.E. & Bergoin, M. (2004). Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Applied and Environmental Microbiology, 70: 7185-7191.

Tlak Gajger, I., Kolodziejek, J., Bakonyi, T. & Nowotny, N. (2014). Prevalence and distribution patterns of seven different honeybee viruses in diseased colonies: A case study from Croatia. Apidologie, 45: 701-706.

Usta, A. & Yıldırım, Y. (2022). Investigation of deformed wing virus, Black queen cell virus, and acute bee paralysis virus infections in honey bees using reverse transcriptase-polymerase chain reaction (RT-PCR) method. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 69: 303-311.

Ütük, A.E., Pişkin, F.Ç. & Kurt, M. (2010). Türkiye’de Nosema ceranae’nın ilk moleküler tanısı. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 57: 275-278.

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

Zerek, A., Yaman, M. & Dik, B. (2022). Prevalence of nosemosis in honey bees (Apis mellifera L., 1758) of the Hatay province in Turkey. Journal of Apicultural Research, 61: 368-374.