Investigation of the prevalence of varroasis and nosemosis in honey bees in Aksaray, Türkiye

Year 2025, Volume: 10 Issue: 2, 92 - 99, 31.08.2025

Neslihan Sürsal Simsek , Emrah Simsek

https://doi.org/10.31797/vetbio.1628717

Abstract

Varroa destructor and Nosema species (N. ceranae and N. apis) are significant and widespread honey bee (Apis mellifera) parasites responsible for substantial colony losses and reduced productivity worldwide. Numerous studies have assessed the prevalence of these parasites in honey bees across various provinces of Türkiye. In the present study, we aimed to determine the presence and prevalence of V. destructor and Nosema species in honeybees within Aksaray province, Türkiye, using both conventional and molecular methods. For this purpose, 50 hives from 10 apiaries were sampled between July and November 2020 and between April and June 2021. These hives were examined for the presence of the aforementioned parasites. The results revealed that 94% of the hives were infested with Varroa mites. A total of 686 Varroa sp. mites were collected from infested hives. The average number of mites per hive was 13.7 (ranging from 7 to 38 mites). However, Nosema spores were not detected in the samples using either microscopic or molecular analyses. In conclusion, this study demonstrates that V. destructor is prevalent in apiaries in Aksaray province and may pose a significant threat to honey bee populations.

Keywords

Aksaray , Apis mellifera , Nosema spp. , Türkiye , Varroa destructor

Ethical Statement

As honey bee is an invertebrate organism, no ethical committee approval was necessary.

Supporting Institution

This work was supported by the Aksaray University Research Fund [grant numbers, 2020/024].

Project Number

2020/024

References

• Arıcılık Araştırma Enstitüsü Müdürlüğü. (2023). Arıcılık İstatistikleri. Retrieved 12 December 2024 from https://arastirma.tarimorman.gov.tr/aricilik/Link/2/Aricilik-Istatistikleri
• 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(7), 1499-1508. https://doi.org/10.1007/s00705-022-05458-y
• Aydın, A. (2012). Hakkari yöresinde Varroasis' in yaygınlığı. Yüzüncü Yıl Üniversitesi Veteriner Fakültesi Dergisi, 23(3), 129-130.
• Aydın, L., Doğanay, A., Oruç, H., Yeşilbağ, K., Bakırcı, S., & Girişkin, O. (2017). Bal arısı yetiştiriciliği ürünleri hastalıkları. TR: Dora Basım Yayım Dağıtım, 1, 155-190.
• Aydın, L., Güleğen, E., Çakmak, İ., & Girişgin, A. (2007). The occurrence of Varroa destructor Anderson and Trueman, 2000 on Honey Bees (Apis mellifera) in Turkey. Turkish Journal of Veterinary and Animal Sciences, 31(3), 189-191.
• Aydın, L., Güleğen, E., & Çetinbaş, H. (2001). Bursa yöresi bal arılarında Nosema apis’in (Zander, 1909) yaygınlığı. Bültendif, 17, 6-8.
• Botías, C., Martín-Hernández, R., Meana, A., & Higes, M. (2012). Critical aspects of the Nosema spp. diagnostic sampling in honey bee (Apis mellifera L.) colonies. Parasitology Research, 110(6), 2557-2561. https://doi.org/10.1007/s00436-011-2760-2
• Burnham, A. J. (2019). Scientific advances in controlling Nosema ceranae (Microsporidia) infections in honey bees (Apis mellifera). Frontiers in Veterinary Science, 6, 79. https://doi.org/10.3389/fvets.2019.00079
• Chaimanee, V., Warrit, N., & Chantawannakul, P. (2010). Infections of Nosema ceranae in four different honeybee species. Journal of Invertebrate Pathology, 105(2), 207-210. https://doi.org/10.1016/j.jip.2010.06.005
• Charbonneau, L. R., Hillier, N. K., Rogers, R. E., Williams, G. R., & Shutler, D. (2016). Effects of Nosema apis, N. ceranae, and coinfections on honey bee (Apis mellifera) learning and memory. Scientific Reports, 6(1), 22626. https://doi.org/10.1038/srep22626
• Chemurot, M., De Smet, L., Brunain, M., De Rycke, R., & de Graaf, D. C. (2017). Nosema neumanni n. sp. (Microsporidia, Nosematidae), a new microsporidian parasite of honeybees, Apis mellifera in Uganda. European Journal of Protistology, 61(Pt A), 13-19. https://doi.org/10.1016/j.ejop.2017.07.002
• 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(5848), 283-287. https://doi.org/10.1126/science.1146498
• Çakmak, İ., Aydın, L., & Güleğen, E. A. (2003). Güney Marmara Bölgesinde balarısı zararlı ve hastalıkları. Uludağ Arıcılık Dergisi, 3(2), 33-35.
• Dietemann, V., Pflugfelder, J., Anderson, D., Charrière, J.-D., Chejanovsky, N., Dainat, B., & Neumann, P. (2012). Varroa destructor: research avenues towards sustainable control. Journal of Apicultural Research, 51(1), 125-132. https://doi.org/10.3896/ibra.1.51.1.15
• Dümen, E., Akkaya, H., Öz, G. M., & Sezgin, F. H. (2013). Microbiological and parasitological quality of honey produced in İstanbul. Turkish Journal of Veterinary and Animal Sciences, 37(5), 602-607. https://doi.org/10.3906/vet-1301-46
• El Khoury, S., Rousseau, A., Lecoeur, A., Cheaib, B., Bouslama, S., Mercier, P.-L., Demey, V., Castex, M., Giovenazzo, P., Derome, N. (2018). Deleterious interaction between honey bees (Apis mellifera) and its microsporidian intracellular parasite Nosema ceranae was mitigated by administrating either endogenous or allochthonous gut microbiota strains. Frontiers in Ecology and Evolution, 6, 58. https://doi.org/10.3389/fevo.2018.00058
• FAOSTAT. (2023). Crops and Livestock Products. Retrieved 28 December from https://www.fao.org/faostat/en/#data/QCL
• Forsgren, E., & Fries, I. (2010). Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Veterinary Parasitology, 170(3-4), 212-217. https://doi.org/10.1016/j.vetpar.2010.02.010
• Fries, I., Wei, H. Z., Shi, W., & Chen, S. J. (1996). Grooming behavior and damaged mites (Varroa jacobsoni) in Apis cerana cerana and Apis mellifera ligustica. Apidologie, 27(1), 3-11. https://doi.org/10.1051/apido:19960101
• Genersch, E. (2010). Honey bee pathology: current threats to honey bees and beekeeping. Applied Microbiology and Biotechnology, 87(1), 87-97. https://doi.org/10.1007/s00253-010-2573-8
• Glenny, W., Cavigli, I., Daughenbaugh, K. F., Radford, R., Kegley, S. E., & Flenniken, M. L. (2017). Honey bee (Apis mellifera) colony health and pathogen composition in migratory beekeeping operations involved in California almond pollination. PloS One, 12(8), e0182814. https://doi.org/10.1371/journal.pone.0182814
• Grupe, A. C., & Quandt, C. A. (2020). A growing pandemic: A review of Nosema parasites in globally distributed domesticated and native bees. PLoS Pathogens, 16(6), e1008580. https://doi.org/https://doi.org/10.1371/journal.ppat.1008580
• Gül, A., & Kutlu, M. (2010). Bingöl ili ve ilçelerinde görülen bal arısı hastalık ve zararlılarının belirlenmesi üzerine bir çalışma. Bingöl Sempozyumu, Bingöl Üniversitesi, 17-19.
• Gürler, A.T., Akpınar, R., Yiğit, S., Kaya, S., Tuygun, T., Aydın, C., Türlek, Ş. Ö., Bölükbaş, C. S., Akçay, A., Bilgiç, Ö. F., Çelik, S. N., Kurt, C., Çetindağ, M., Şimşek, A., Yeşilöz, H., İtik Ekinci, A., Kaplan, S., Korkmaz, Ç., Tuncer, S., Kaymak, S., Deniz, A., Güven, G., Küçükoğlu, B., Yaldız, M., & Kızıltepe Ş. (2024). Investigation of honey bee colonies in terms of mesostigmatid mites in Turkey. Journal of Apicultural Research, 63(2), 350-356. https://doi.org/10.1080/00218839.2024.2309765
• 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(3), 211-217. https://doi.org/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(10), 2659-2669. https://doi.org/10.1111/j.1462-2920.2008.01687.x
• Higes, M., Martín-Hernández, R., Garcia-Palencia, P., Marin, P., & Meana, A. (2009a). Horizontal transmission of Nosema ceranae (Microsporidia) from worker honeybees to queens (Apis mellifera). Environmental Microbiology Reports, 1(6), 495-498. https://doi.org/10.1111/j.1758-2229.2009.00052.x
• Higes, M., Martín-Hernández, R., Garrido-Bailón, E., Botías, C., & Meana, A. (2009b). The presence of Nosema ceranae (Microsporidia) in North African honey bees (Apis mellifera intermissa). Journal of Apicultural Research, 48(3), 217-219. https://doi.org/10.3896/IBRA.1.48.3.12
• Higes, M., Martín-Hernández, R., & Meana, A. (2010). Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie, 41(3), 375-392. https://doi.org/10.1051/apido/2010019
• Huang, W. F., & Solter, L. F. (2013). Comparative development and tissue tropism of Nosema apis and Nosema ceranae. Journal of Invertebrate Pathology, 113(1), 35-41. https://doi.org/10.1016/j.jip.2013.01.001
• Kar, S., Kaya, N., Guven, E., & Karaer, Z. (2006). Use of a new designed container for the detection of Varroa mites in adult bees. Uludag Bee Journal, 6(2), 68-73.
• Kartal, S., Tunca, R. İ., Özgül, O., Karabağ, K., & Koç, H. (2021). Microscopic and molecular detection of Nosema sp. in the Southwest Aegean Region. Uludağ Arıcılık Dergisi, 21(1), 8-20. https://doi.org/10.31467/uluaricilik.880380
• 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), 1-10. https://doi.org/10.1016/j.jip.2007.02.014
• Klein, A.-M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the royal society B: biological sciences, 274(1608), 303-313. https://doi.org/10.1098/rspb.2006.3721
• Koç Akpınar, R., Gürler, A. T., Bölükbaş, C. S., Kaya, S., Arslan, S., Aydın, C., & Öncel, T. (2024). Prevalence and phylogenetic network analysis of Nosema apis and Nosema ceranae isolates from honeybee colonies in Türkiye. Acta Parasitologica, 69(3), 1538-1546. https://doi.org/10.1007/s11686-024-00887-y
• Kumova, U. (2003). The controlling methods of Varroa. Marmara Bölgesi 2. Arıcılık Kongresi Bildirileri, 28-30.
• Kutlu, M., & Kaftanoğlu, O. (1988). Ergin Balarısı (Apis mellifera L.) Hastalığı Nosema apis' in dağılımı ve enfeksiyon oranı üzerine bir araştırma [Yüksek Lisans Tezi, Çukurova Üniversitesi, Fen Bilimleri Enstitüsü. Adana].
• 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. https://doi.org/10.1051/apido/2010017
• Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A. M., Garrido-Bailón, E., & Higes, M. (2007). Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73(20), 6331-6338. https://doi.org/10.1128/AEM.00270-07
• Martín‐Hernández, R., Botías, C., Bailón, E. G., Martínez‐Salvador, A., Prieto, L., Meana, A., & Higes, M. (2012). Microsporidia infecting Apis mellifera: coexistence or competition. is Nosema ceranae replacing Nosema apis? Environmental Microbiology, 14(8), 2127-2138. https://doi.org/10.1111/j.1462-2920.2011.02645.x
• Mayack, C., & Hakanoglu, H. (2022). Honey bee pathogen prevalence and interactions within the Marmara Region of Turkey. Veterinary Science, 9(10), 573. https://doi.org/10.3390/vetsci9100573
• McMenamin, A. J., & Genersch, E. (2015). Honey bee colony losses and associated viruses. Current Opinion in Insect Science, 8, 121-129. https://doi.org/10.1016/j.cois.2015.01.015
• Muz, M. N., Solmaz, H., Yaman, M., & Karakavuk, M. (2012). Kış salkımı erken bozulan arı kolonilerinde paraziter ve bakteriyel patojenler. Yüzüncü Yıl Üniversitesi Veteriner Fakültesi Dergisi, 23(3), 147-150.
• Naug, D. (2009). Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation, 142(10), 2369-2372. https://doi.org/10.1016/j.biocon.2009.04.007
• Önk, K., & Kılıç, Y. (2014). Kars yöresindeki bal arılarında varroosis'in yaygınlığı. Uludag Bee Journal, 14(2).
• Özkırım, A. (2018). Beekeeping in Turkey: Bridging Asia and Europe. C. Panuwan, W. Geoffrey & N. Peter (Eds.), Asian beekeeping in the 21st century, (pp.41-69). Springer. https://doi.org/10.1007/978-981-10-8222-1_2
• Özkırım, A., Schiesser, A., & Keskin, N. (2019). Dynamics of Nosema apis and Nosema ceranae co-infection seasonally in honey bee (Apis mellifera L.) colonies. Journal of Apicultural Science, 63(1), 41-48. https://doi.org/10.2478/JAS-2019-0001
• Özüiçli, M., & Aydın, L. (2018). Türkiye bal arılarında ciddi tehlike; nosemosis. Uludağ Üniversitesi Veteriner Fakültesi Dergisi, 37(2), 151-157. https://doi.org/10.30782/uluvfd.419001
• 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. https://doi.org/10.3896/IBRA.1.49.1.11
• Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O., & Kunin, W. E. (2010). Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25(6), 345-353. https://doi.org/10.1016/j.tree.2010.01.007
• Potts, S. G., Imperatriz-Fonseca, V., Ngo, H. T., Aizen, M. A., Biesmeijer, J. C., Breeze, T. D., & Vanbergen, A. J. (2016). Safeguarding pollinators and their values to human well-being. Nature, 540(7632), 220-229. https://doi.org/10.1038/nature20588
• Ramsey, S. D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J. D., Cohen, A., & Ellis, J. D. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences, 116(5), 1792-1801.
• Ratnieks, F. L., & Carreck, N. L. (2010). Ecology. Clarity on honey bee collapse? Science, 327(5962), 152-153. https://doi.org/10.1126/science.1185563
• Roberts, J. M., 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(1), 6925. https://doi.org/10.1038/s41598-017-07290-w
• Rosenkranz, P., Aumeier, P., & Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103, S96-S119. https://doi.org/10.1016/j.jip.2009.07.016
• Seven Çakmak, S., & Çakmak, İ. (2016). Beekeeping and recent colony losses in Turkey. Uludag Bee Journal, 16(1), 31-48.
• Smith, M. L. (2012). The honey bee parasite Nosema ceranae: transmissible via food exchange? PloS One, 7(8), e43319. https://doi.org/10.1371/journal.pone.0043319
• Spivak, M., Browning, Z., Goblirsch, M., Lee, K., Otto, C., Smart, M., & Wu-Smart, J. (2017). Why does bee health matter? The science surrounding honey bee health concerns and what we can do about it. ICAST Commentary, QTA2017-1.
• Şimşek, H. (2005). Elazığ yöresi bal arılarında bazı parazit ve mantar hastalıklarının araştırılması. Ankara Universitesi Veteriner Fakultesi Dergisi, 52(2), 123-126. https://doi.org/10.1501-Vetfak_0000000030-776487
• Tamali, H., Adjlane, N., & Özkırım, A. (2024). Impact of national beekeeping approaches and structures on Nosema spp. prevalence in honeybee (Apis mellifera L.) colonies. Applied Ecology & Environmental Research, 22(3). http://dx.doi.org/10.15666/aeer/2203_27852795
• Topçu, B., & Arslan, M. Ö. (2004). Kars yöresindeki balarılarında nosemosis’ in yaygınlığı. Uludag Bee Journal, 4(4), 164-170.
• Traver, B. E., & Fell, R. D. (2011). Nosema ceranae in drone honey bees (Apis mellifera). Journal of Invertebrate Pathology, 107(3), 234-236. https://doi.org/10.1016/j.jip.2011.05.016
• Traver, B. E., & Fell, R. D. (2012). Low natural levels of Nosema ceranae in Apis mellifera queens. Journal of Invertebrate Pathology, 110(3), 408-410. https://doi.org/10.1016/j.jip.2012.04.001
• TUIK. (2022). Turkish Statistical Institute Data Portal of Statistics, Agriculture. https://data.tuik.gov.tr/Kategori/GetKategori?p=Agriculture-111 Accessed on 25 August 2022.
• TUIK. (2023). Turkish Statistical Institute Data Portal of Statistics, Agriculture. https://data.tuik.gov.tr/Search/Search?text=ar%C4%B1c%C4%B1l%C4%B1k Accessed on 17 December 2024.
• Tunca, R. İ., & Çimrin, T. (2012). Kırşehir ilinde bal arısı yetiştiricilik aktiviteleri üzerine anket çalışması. Journal of the Institute of Science and Technology, 2(2), 99-108.
• Urbieta-Magro, A., Higes, M., Meana, A., Gomez-Moracho, T., Rodriguez-Garcia, C., Barrios, L., & Martin-Hernandez, R. (2019). The levels of natural Nosema spp. infection in Apis mellifera iberiensis brood stages. International Journal for Parasitology, 49(8), 657-667. https://doi.org/10.1016/j.ijpara.2019.04.002
• Ütük, A. E., Piskin, F. C., Girisgin, A. O., Selcuk, O., & Aydin, L. (2016). Microscopic and molecular detection of Nosema spp. in honeybees of Turkey. Apidologie, 47(2), 267-271. https://doi.org/10.1007/s13592-015-0394-6
• Ütük, A. E., Pişkin, F. Ç., Deniz, A., & Balkaya, İ. (2011). Varroosis ve nosemosis üzerine retrospektif bir çalışma. Etlik Veteriner Mikrobiyoloji Dergisi, 22(1), 11-15.
• Ütük, A. E., Pişkin, F. Ç., & Mitat, K. (2010). First molecular detection of Nosema ceranae in Turkey. Ankara Universitesi Veteriner Fakultesi Dergisi, 57(4), 275-278. https://doi.org/10.1501/Vetfak_0000002439
• Webster, T. (1993). Nosema apis spore transmission among honey bees. American Bee Journal, 133, 869-870.
• Webster, T. C., Thacker, E. M., Pomper, K., Lowe, J., & Hunt, G. (2008). Infection in honey bee (Apis mellifera) queens. Journal of Apicultural Research, 47(1), 53-57. https://doi.org/10.1080/00218839.2008.11101423
• Whitaker, J., Szalanski, A. L., & Kence, M. (2011). Molecular detection of Nosema ceranae and N. apis from Turkish honey bees. Apidologie, 42(2), 174-180. https://doi.org/10.1051/apido/2010045
• Winston, M. L. (1991). The biology of the honey bee. Harvard University Press.
• Yalçınkaya, A. (2008). Hatay ve Adana yöresindeki bal arılarının (Apis mellifera L.) mikrobiyal ve paraziter hastalıklar yönünden incelenmesi [Yüksek Lisans Tezi. Hacettepe Üniv. Fen Bil Ens, Ankara].
• Yalçınkaya, A., & Keskin, N. (2010). The investigation of honey bee diseases after colony losses in Hatay and Adana provinces of Turkey. Mellifera, 10(20), 24-31.
• Zander, E. (1909). Tierische parasiten als krankenheitserreger bei der biene. Münchener Bienenzeitung, 31, 196-204.