The Presence and Distribution of Nosemosis Disease in Turkey

Year 2019, , 71 - 84, 23.04.2020

Onur Tosun , Çağrı Bekircan , Hilal Baki

https://doi.org/10.35206/jan.688866

Cited By: 1

Abstract

Nosemosis is one of the most important bee diseases causing economic losses in beekeeping, which is one of the significant reasons for Colony Collapse Disorder (CCD) in the world. Nosema apis and Nosema ceranae, the microsporidian species, are the main causative agents of Nosemosis in honey bees worldwide. This disease causes digestive system disorders, a decrease in the average life of bees and colony losses. In this review, the general characteristics of Nosemosis disease, and information about the situation in Turkey are given.

Keywords

Honey bees, Microsporidia, Nosemosis, Nosema apis, Nosema ceranae

References

• Aydın, L., Gülegen, E. & Çetinbas, H. (2001a). Prevalence of Nosema apis in Southern Marmara region. XVII. Apimondia 28. October. 1 November Durban, South Africa.
• Aydın, L., Gülegen, E. & Çetinbas, H. (2001b). Bursa yöresi bal arılarında Nosema apis’in yaygınlıgı. 3. Bee Congress (1- 3 November 2001). Çukurova University. Faculty of Agriculture. Adana.
• Aydın, L., Çakmak, İ., Güleğen, E. & Korkut, M. (2003). Güney Marmara Bölgesi Arı Hastalıkları ve Zararlıları Anket Sonuçları. Uludağ bee journal, 1, 37-40.
• Aydin, L., Cakmak, I., Gulegen, E.& Wells, H. (2005). Honey bee Nosema disease in the Republic of Turkey. Journal of Apicultural Research, 44, 196–197.
• Bailey, L. (1967). Nosema apis and dysentery of the honey bee, Journal of Apicultural Research, 6, 121–125.
• Başar, E. (1990). Ülkemizdeki bal arılarında (Apis mellifera) Acarapis woodi ve Nosema apis parazitlerinin araştırılması, (Master Thesis) Available from Council of Higher Education and Theses Center. (Thesis No. 8505)
• Becnel, J. J., Takvorian, P. M. & Cali, A. (2014). Checklist of available generic names forMicrosporidia with type species and type hosts. In L. M. Weiss & J. J. Becnel Wiley (Eds.), Microsporidia Pathogens of Opportunity (pp. 671–686). Blackwell Press.
• Bourgeois, A. L., Rinderer, T. E., Beaman, L. D. & Danka, R. G. (2010). Genetic detection and quantification of Nosema apis and N. ceranae in the honey bee. Journal of Invertebrate Pathology, 103, 53–58.
• Brenna, E., Traver, B. E., Matthew, R., Williams, M. R., Richard, D. & 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.
• Campbell, J., Kessler, B., Mayack, C. & Naug D. (2010). Behavioural fever in infected honeybees: parasitic manipulation or coincidental benefit?, Parasitology, 137, 1487–1491.
• Cengiz, M. M., Genç, F. (2001). Erzurum arıcılığının yapısal analizi. Türkiye 3. Bee Congress (1- 3 November 2001). Çukurova University. Faculty of Agriculture. Adana.
• Chen, Y. P. & Huang, Z. Y. (2010). Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia, Apidologie, 41, 364–374.
• Chen, Y. P., Evans, J. D., Murphy, C., Gutell, R., Zuker, M., Gundensen-Rındal, D. & Pettıs, J. S. (2009a). Morphological, Molecular, and Phylogenetic Characterization of Nosema ceranae, a Microsporidian Parasite Isolated from the European Honey Bee, Apis mellifera, J. Eukaryot. Microbiol., 56, 2, 142–147.
• Chen, Y., Evans, J. D., Zhou, L., Boncristiani, H., Kimura, K., Xiao, T., Litkowski, A. M. & Pettis, J. S. (2009b). Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees, Journal of Invertebrate Pathology, 101, 204–209.
• Cox-Foster, D. L., Conles, S., Holmes, E. C., Palacios, G., Evans, J. D., Moran, N. A., Quan, P. L., … Lıpkın, W. I. (2007). Ametagonic survey of microbes in honey bee colony collapse disorder. Science, 318(5848): 283-287.
• Czekońska, K. (2000). The influence of Nosema apis on young honeybee queens and transmission of the disease from queens to workers. Apidologie, 31, 701–706.
• Çakmak, İ., Aydın, L., Seven, S. & Korkut, M. (2003a). Güney Marmara bölgesinde arıcılık anket sonuçları, Uludağ bee journal, 3, 1, 31-36.
• Çakmak, İ, Aydın, L. & Güleğen, A. E. (2003b). Güney Marmara Bölgesinde balarısı zararlıları ve hastalıkları. Uludağ bee journal, 1, 33-35.
• Doğaroğlu, M. (2009). Modern Arıcılık Teknikleri,, Türkmenler Matbaacılık, Tekirdağ.
• Fenoy, S., Rueda, C., Higes, M., Martín-Hernandez, M. & del Aguila, C. (2009). High-Level Resistance of Nosema ceranae, a Parasite of the Honeybee, to Temperature and Desiccation. Applıed and Environmental Microbiology, 75, 21, 6886–6889.
• Fries, I. (1993). Nosema apis - A parasite in the honey bee colony, Bee World, 74, 5–19.
• Fries, I. (2010). Nosema ceranae in European honey bees (Apis mellifera), Journal of Invertebrate Pathology, 103, 73–79.
• Fries, I., Feng, F., Silva, A. D., 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.
• Fries, I., Martín, R., Meana, A., García-Palencia, P. & Higes, M. (2006). Natural infections of Nosema ceranae in European honey bees, J. Apic. Res., 45, 230–233.
• Giray, T., Kence, M., Oskay, D., Döke, M. A., Kence, A. (2010). Colony losses in Turkey and causes of bee deaths, Apidologie 41, 451-453.
• Gül, A., Kutlu, M. A. (2009). Bingöl ili ve ilçelerinde görülen bal arısı hastalık ve zararlılarının belirlenmesi üzerine bir çalışma. 3. Bingöl Sempozyumu Kitapçığı, Bingöl.
• Güner, B. G., Ertürk, Ö. & Yaman, M. (2019). Characterisation of a Turkish Isolate of Nosema ceranae Fries et al., 1996 (Microsporidia) Recorded in Populations of Apis mellifera L. in Turkey. Acta Zoologica Bulgarica, 71 (2), 279-284
• Higes, M., Martin, R. & Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honey bees in Europe, Journal of Invertebrate Pathology, 92, 93-95.
• Higes, M., Garcia-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., Nozal, M. J. … Meana, A. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse, Environmental Microbiology, 10, 10, 2659–2669.
• Huang, Z. (2012). Effects of Nosema on Honey Bee Behavior and Physiology. Retrieved March 20 2019 from http://www.extension.org/pages/60674/effects-of-nosema-on-honey-bee-behavior-and-physiology. in text reference: e.g. (Huang, 2012).
• Huang, W. F., Jiang, J. H., Chen, Y. W. & Wang, C. H. (2007). A Nosema ceranae isolate from the honey bee Apis mellifera, Apidologie, 38, 30-37.
• Ivgın Tunca, R., Oskay, D., Gosterit, A. & Tekin O. K. (2016). Does Nosema ceranae Wipe Out Nosema apis in Turkey?. Iran J Parasitol, 11, 2, 259-264.
• Keskin, N., Basar, E., Saraçbası, T. (1996). Türkiye’nin bazı yörelerindeki bal arılarında (Apis mellifera L.) Nosema hastalıgı. Hacettepe Fen ve Müh. Bil. Derg. 17: 25 – 35.
• Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., Chinh, T. X., … 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.
• Kutlu, M. A. & Kaftanoglu, O. (1990). A study on the distribution and infection rate of nosema (Nosema apis ) disease of adult honey bees (Apis mellifera L .). Cukurova University, Institute of Natural and Applied Sciences, J. Sci. Eng. 4 (2), 141–149
• Kutlu, M., A. & Ekmen, F. (2003). Bingöl yöresi bal arılarında (Apis mellifera L.) Nosema hastalığının varlığı ve enfeksiyon oranı, Teknik Arıcılık, 79, 24-26.
• Kutlu, M., A. & Gazioğlu, A. (2008). Bingöl İli Bal Arılarında (Apis mellifera L.) Nosema (Nosematosis) Hastalığının Yaygınlığı, 2.Bingöl sempozyumu, 25-27 Temmuz 2008, Bingöl.
• Malone, L. A. & Gatehouse, H. S. (1998). Effects of Nosema apis Infection on Honey Bee (Apis mellifera) Digestive Proteolytic Enzyme Activity, Journal of Invertebrate Pathology, 71, 169–174.
• Malone, L. A., Gatehouse, H. S. & Tregidga, E. (2001). Effects of Time, Temperature, and Honey on Nosema apis (Microsporidia: Nosematidae), a Parasite of the Honeybee, Apis mellifera (Hymenoptera: Apidae), Journal of Invertebrate Pathology, 77, 258–268.
• Martín-Hernańdez, 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.
• Martín-Hernández, R., Meana, A., García-Palencıa, P., Marín, P., Botías, C., Garrıdo-Baılón, E., Barrıos, L. & Hıges, M. (2009). Effect of temperature on the biotic potential of honey bee microsporidia, Applied and Environmental Microbiology, 75, 2554-2557.
• Mayack, C. & Naug, D. (2009). Energetic stress in the honey bee Apis mellifera from Nosema ceranae infection, Journal of Invertebrate Pathology, 100, 185-188.
• Muz, D. & Muz M. N. (2009). Survey of the occurrence of Deformed Wing Virus and multiple parasites of queens (Apis mellifera L.) in apiaries with collapsed colonies in Hatay, Turkey. Journal of Apicultural Research, 48, 3, 204-208
• Muz, M. N., Girisgin, A. O., Muz, D. & Aydin, L. (2010). Molecular detection of Nosema ceranae and Nosema apis infections in Turkish apiaries with collapsed colonies. Journal of Apicultural Research and Bee World 49(4): 342.
• Muz, M. N., Solmaz, H., Yaman, M. & Karakavuk, M. (2012). Kış Salkımı Erken Bozulan Arı Kolonilerinde Paraziter ve Bakteriyel Patojenler, The Journal of the Faculty of Veterinary Medicine University of Yüzüncü Yıl, 23 (3), 147 – 150.
• Naug, D. & Gibbs, A. (2009). Behavioural changes mediated by hunger in honey bees infected with Nosema ceranae, Apidologie, 40, 595-599.
• Oğuz, B., Karapınar, Z., Dinçer, E. & Değer 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 doi:10.3906/vet-1604-92
• OIE. (2008). Manual Of Diagnostic Tests And Vaccines For Terrestrial Animals, Chapter 2.2.4., Nosemosis of honey bees, Volume 1, 410-414. 2008.
• Özbilgin, N., Alatas, İ., Balkan, C., Öztürk, A. & Karaca, Ü. (1999). Ege bölgesi arıcılık işletmelerinin teknik ve ekonomik baslıca karakteristiklerinin belirlenmesi. Anadolu. 9 (1): 149-170.
• Özkırım, A. & Keskin, N. (2001). A survey of Nosema apis of honey bees (Apis mellifere L.) producing the famous Anzer honey in Turkey, Z. Naturforsch. 56, 918-919.
• Özkırım, A., Shiesser, A. & Keskin, N. (2019). Dynamics Of Nosema Apis And Nosema Ceranae Co-Infection Seasonally In Honey Bee (Apis Mellifera L.) Colonies. J. APIC. SCI.. 63. 1 DOI 10.2478/JAS-2019-0001
• 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.
• Paxton, R. J., Klee, J., Korpella, 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.
• Sıralı, R. & Doğaroğlu, M. (2005). Trakya Bölgesi Arı Hastalıkları ve Zararlıları Üzerine Anket Sonuçları, Uludağ bee journal, 5, 71-78.
• Somerville, D. & Hornitzky, M. (2007). Nosema disease, September 2007. Retrieved March 20 2019 from http//www.dpi.nsw.gov.au__dataassetspdf_file0003177519nosema-disease.pdf. in text reference: e.g. (Somerville & Hornitzky, 2012).
• Soysal, M. İ. & Gürcan, E. K. (2005). Tekirdağ İli Arı Yetiştiriciliği Üzerine Bir Araştırma. Journal of Tekirdag Agricultural Faculty, 2(2): 161-165.
• Suwannapong, G., Maksong, S., Seanbualuang, P. & Benbow, M. E. (2010). Experimental infection of red dwarf honeybee, Apis florea, with Nosema ceranae, Journal of Asia-Pacific Entomology, 13, 361–364.
• Şimşek, H. (2005). Elazığ yöresi bal arılarında bazı parazit ve mantar hastalıklarının araştırılması, Veterinary journal of Ankara University, 52, 123-126.
• Şimşek, H., Dilgin, N. & Gültekin, İ. (2001). Elazığ yöresinde bulunan arı işletmelerinde nosematosisin yaygınlığı, Journal of Etlik Veterinary Microbiology, 12, 49-51.
• Topcu, B. & Arslan, M. Ö. (2004). Kars yöresindeki bal arılarında nosemosis’in yaygınlığı, Uludağ bee journal, 11 2004, 164-170.
• Tosun, O. (2012). Bal Arılarında (Apis mellifera L., 1758) Nosemosis (Nosematosis) Hastalığının Doğu Karadeniz Bölgesinde Bulunan Arı Kolonilerindeki Varlığı, Dağılımı ve Hastalık Etkenlerinin Karakterizasyonu, (Master’s Thesis) Available from Council of Higher Education and Theses Center. (Thesis No. 312164)
• Tosun, O. & Yaman, M. (2016). The Effects of Temperature And Humidity Around The Beehives on The Distribution of Nosema ceranae, and also Geographical and Seasonal Activity of The Infection İn The Eastern Black Sea Region of Turkey. Journal of Environmental Science and Engineering B, 5(11), 513-522., Doi: 10.17265/2162-5263/2016.11.001
• Tuik. 2017. Retrieved February 12 2020 from http://www.tuik.gov.tr/VeriBilgi.do?tb_id=46&ust_id=13.%20Hayvanc%C4%B1l%C4%B1k%20istatistikleri.%2013%20A%C4%9Fustos%202011. in text reference: e.g. (TUIK. 2017).
• Tutkun, E. & İnci, A. (1992). Bal Arısı Hastalıkları ve Tedavi Yöntemleri (Teshisten Tedaviye). Demircioglu Matbaacılık. Ankara.
• Uygur, S. Ö. & Girişgin, A. O. (2008). Bal Arısı Hastalık Ve Zararlıları, Uludağ Arıcılık Dergisi, 8, 4, 130-142.
• Ütük, A. E., Pişkin, F. Ç. & Kurt, M. (2010). Türkiye’de Nosema ceranae’nin ilk moleküler tanısı, Veterinary journal of Ankara University, 57, 275-278.
• Ütük, A. E., Pişkin, F. C., Girişgin, A. O., Selçuk O. & Aydın L. (2016). Microscopic and molecular detection of Nosema spp. in honeybees of Turkey. Apidologie (2016) 47:267–271. DOI: 10.1007/s13592-015-0394-6
• Webster, T. C., Pomper, K. W., Hunt, G., Thacker, E. M. & Jones, S. C. (2004). Nosema apis infection in worker and queen Apis mellifera, Apidologie, 35, 49–54.
• Webster, T. C., Thacker, E. M., Pomper, K., Lowe, J.& Hunt, G. (2008). Nosema apis infection in honey bee (Apis mellifera) queens, Journal of Apıcultural Research, 47, 1, 53-57.
• Williams, G. R., Shafer, A. B. A., Rogers, R. E. L., Shutler, D. & Stewart, D. T. (2008a). First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA., Journal of Invertebrate Pathology, 97, 189–192.
• Williams, G. R., Sampson, M. A., Shutler, D. & Rogers, R. E. L. (2008b). Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)?, Journal of Invertebrate Pathology,99, 342–344.
• Whitaker J., Szalanski A. L. & Kence M. (2011). Molecular detection of Nosema ceranae and N. apis from Turkish honey bees, Apidologie, 42:174–180.
• Yalçınkaya, A., Keskın, N. & Özkırım, A. (2009).After Colony Losses in Hatay and Adana Regıon of Turkey the Investıgatıon of Honey Bee Dıseases. Apimonia Fransa 32009.
• Yaşar, N., Güler, A., Yesiltas, H. B., Bulut, G., Gökçe, M. (2002). Karadeniz bölgesi arıcılıgının genel yapısının belirlenmesi. Mellifera. 2-3: 15-24.