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A MICROSCOPY AND MOLECULAR STUDIES OF NOSEMA CERANAE INFECTION IN MAZANDARAN PROVINCE OF IRAN

Yıl 2021, Cilt: 21 Sayı: 2, 198 - 205, 11.11.2021
https://doi.org/10.31467/uluaricilik.991579

Öz

Nosema ceranae as a fungal parasite has been reported from the Apis mellifera in all continents. It causes reduced longevity, depopulation, decreased production, and colony losses in honeybee colonies. This study aimed to determine the prevalence of N.ceranae in the apiaries of Mazandaran province. In this study, we randomly selected 320 hives from thirty-two apiaries and collected twenty old honeybees from the apiaries. The collected samples were examined by microscopy and molecular methods. The results of the microscopic examinations showed that 78.12% of apiaries were infected with Nosema spp. In addition, N. ceranae was identified 84.37% of apiaries by PCR, while no samples were infected by N. apis. Blast analysis of the sequenced samples confirmed the presence of N. ceranae infection in the apiaries. Based on the obtained results, a high frequency of N.ceranae was detected in apiaries in Mazandaran province.

Destekleyen Kurum

The Vice President Research and Technology of Ferdowsi University of Mashhad

Proje Numarası

VPRTFM- 3/43533

Kaynakça

  • Ansari, MJ., Al-Ghamdi, A., Nuru, A., Khan, KA., Alattal, Y. 2017. Geographical distribution and molecular detection of Nosema ceranae from indigenous honey bees of Saudi Arabia. Saudi J Biol Sci. 24(5):983-991. DOI: 10.1016/j.sjbs.2017.01.054.
  • Bailey, L., Ball, BV. 1981. Honey Bee Pathology. Academic Press, London.
  • 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. Vet. Hung. 63(3):358-69. DOI: 10.1556/004.2015.034.
  • 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. Parasitol Res 115(1):175-81. DOI: 10.1007/s00436-015-4733-3.
  • Fenoy, S., Rueda, C., Higes, M., Martín-Hernández, R., del Aguila, C. 2009. High-level resistance of Nosema ceranae, a parasite of the honeybee, to temperature and desiccation. Appl. Environ. Microbiol. 75(21):6886-6889. doi:10.1128/AEM.01025-0918.
  • Fries, I. 2010. Nosema ceranae in European honey bees (Apis mellifera) J. Invertebr. Pathol. 103(1): S73-S79.DOI: 10.1016/j.jip.2009.06.017.
  • Fries, I., Feng, F., Silva, AD., Slemenda, SB., Pieniazek, NJ. 1996. Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae) Europ. J. Protistol. 32(3):356–365.
  • Glavinic, U., Stevanovic, J., Ristanic, M., Rajkovic, M., Davitkov, D., Lakic, N., & Stanimirovic, Z. 2021. Potential of Fumagillin and Agaricus blazei Mushroom Extract to Reduce Nosema ceranae in Honey Bees. Insects, 12(4), 282. https://doi.org/10.3390/insects12040282
  • Gisder, S., Hedtke, K., Möckel, N., Frielitz, MC., Linde, A., Genersch, E. 2010. Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Appl. Environ. Microbiol. 76(9):3032–3038. DOI: 10.1128/AEM.03097-09.
  • Higes, M., Martín, R., Meana, A. 2006. Nosema ceranae, a new microsporidian parasite in honey bees in Europe. J. Invert. Pathol. 92 (2):93–95.
  • Ivgin Tunca, R., Oskay, D., Gosterit, A., Tekin, OK. 2016. Does Nosema ceranae wipeout Nosema apis in Turkey? Ir. J. Parasitol, 11(2): 259-264.
  • Kazembeyki, MA. 2003. Society, Politics and Economics in Mazandaran, Iran, Routledge Cruzon, London.
  • Khezri, M., Moharrami, M., Modirrousta, H., Torkaman, M., Salehi, S., Rokhzad, B., Khanbabi, H. 2018. Molecular detection of Nosema ceranae in the apiaries of Kurdistan province, Iran. Vet. Res. Forum 9(3):273–278. DOI: 10.30466/vrf.2018.32086.
  • Klee, J., Besana, AM., Genersch, E., Gisder. S., Nanetti, A., Tam, DQ., Chinh, TX., Puerta, F., Ruz, JM, Kryger, P., Message, D., Hatjina, F., Korpela, S., Fries, I., Paxton, RJ. 2007. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera, J. Invertebr. Pathol. 96(1): 1-10. DOI: 10.1016/j.jip.2007.02.014.
  • Lotfi, A., Jamshidi, R., Aghdam Shahryar, H., Yousefkhani, M. 2009.The prevalence of nosemosis in honey bee colonies in Arasbaran region (Northwestern Iran). J. Agri Environ. Sci. 5(2): 255-257.
  • McCallum, R. Olmstead, S. Shaw, J. Glasgow, K. 2020. Evaluating efficacy of Fumagilin-B® against Nosemosis and tracking seasonal trends of Nosema spp. in Nova Scotia Honey bee colonies. J.Apic. Sci.2020.64(2):277-286.
  • Martín-Hernández, R., Meana, A., Prieto, L., Salvador, AM., Garrido-Bailón, E., Higes, M. 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl. Environ. Microbiol. 73:6331-6338. DOI: 10.1128/AEM.00270-07.
  • 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. Pol. J. Vet. Sci. 14(3):385-91. DOI: 10.2478/v10181-011-0058-z.
  • Mohammadian, B., Bokaie, S., Moharrami, M., Nabian, S., Forsi, M. 2018. Distribution of Nosema spp. in climatic regions of Iran. Vet Res Forum. 9(3):259–263. DOI: 10.30466/vrf.2018.32082.
  • Moradi, M. 2019. Survey of Thymus volgaris ethanolic effects on the Nosema parasite in honeybee. Iranian. H. Sci.Tech .9 (17): 24-32.
  • Moshverinia, A., Abedi, V., Safaie, H. 2012. A survey of Nosema apis infection in apiaries of North Khorasan province, Iran. Ir. J Vet Sci Tech 4: 25-30. DOI: 10.22067/veterinary.v4i2.17418.
  • Nabian, S., Ahmadi, K., Shirazi, MN., Gerami Sadeghian, A. 2011. First detection of Nosema ceranae, a microsporidian protozoon of European honeybees (Apis mellifera) in Iran. Ir.J.Parasitol. 6: 89-95. PMID: 22347302.
  • OIE. 2019. Manual for diagnostic tests and vaccines for terrestrial animals, Nosemosis of honey bees, Paris.
  • Papini, R., Mancianti, F., Canovai, R., Cosci, F., Rocchigiani, G., Benelli, G., Canale, A. 2017. Prevalence of the microsporidian Nosema ceranae in honeybee (Apis mellifera) apiaries in Central Italy. Saudi. J. Biol. Sci. 24 (5):979-982. DOI: 10.1016/j.sjbs.2017.01.010.
  • Petrie A., Watson P. 2006. Statistic for veterinary and animal science. Blackwell Oxford.
  • Razmaraii, N., Karimi, H. 2010. A survey of Nosema disease of honey bee (Apis mellifera) in East Azarbaijan province of Iran. J. Anim.Vet. Adv. 9: 879-882. DOI: 10.3923/javaa.2010.879.882.
  • 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. Peer J 31;6:e4252. DOI: 10.7717/peerj.4252.
  • Stevanovic, J., Stanimirovic, Z., Genersch, E., Kovacevic, SR., 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.
  • Tavassoli, M., Eiganinejad, S., Alizadeh-Asl, S. 2009. A survey on Nosema apis infection in apiaries of Urmia, North-West of Iran. Ir. J. Vet. Sci. Tech. 1(1): 35-40.
  • Thursfield, MV.1986. Veterinary epidemiology, Butterworth, Guilford, London.
  • Tokarev, YS., Huang, WF, Solter, LF., Malysh, JM., Becnel, JJ., Vossbrinck, CR. 2020. A formal redefinition of the genera Nosema and Vairimorpha (Microsporidia: Nosematidae) and reassignment of species based on molecular phylogenetics. J.Inver. Pathol. 169: 107279, doi.org/10.1016/j.jip.2019.107279.
  • Van den Heever, JP., Thompson, TS., Curtis, JM., Ibrahim, A., Pernal, SF.2014. Fumagillin: an overview of recent scientific advances and their significance for apiculture. J. Agric. Food. Chem. 62:2728–37. doi: 10.1021/jf4055374.
  • Webster, TC., Pomper, KW., Gerg, H., Thacker, EM., Jones, SC. 2004. Nosema apis infection in worker and queen Apis mellifera. Apidologie. 35(1): 49–54.
  • Williams, GR., Shutler, D., Little, CM., Burgher MacLellan, KL., Rogers, REL. (2010). The microsporidian Nosema ceranae, the antibiotic Fumagilin B, and western honey bee (Apis mellifera) colony strength. Apidologie 42 (1): 15 22.

Nosema ceranae Enfeksiyonunun İran, Mazandaran İlinde Mikroskopik ve Moleküler Çalışması

Yıl 2021, Cilt: 21 Sayı: 2, 198 - 205, 11.11.2021
https://doi.org/10.31467/uluaricilik.991579

Öz

Nosema ceranae, tüm kıtalarda Apis mellifera'dan mantar paraziti olarak rapor edilmiştir. Bal arısı kolonilerinde yaşam süresinin azalmasına, nüfus azalmasına, üretimin azalmasına ve koloni kayıplarına neden olur. Bu çalışmada Mazandaran ili arılıklarında N.ceranae yaygınlığının belirlenmesi amaçlanmıştır. Bu çalışmada, otuz iki arılıktan rastgele 320 kovan seçtik ve arılıklardan yirmi yaşlı bal arısı topladık. Toplanan örnekler mikroskop ve moleküler yöntemlerle incelendi. Mikroskobik incelemelerde arılıkların %78,12'sinin Nosema spp belirlendi. Ayrıca N. ceranae, PCR ile %84.37'sinde tespit edilirken, hiçbir numune N. apis ile enfekte olmamıştır. Sıralı örneklerin gen hizalama analizi sonucunda arılıklarda N. ceranae enfeksiyonunun varlığı doğrulandı. Elde edilen sonuçlara göre Mazandaran ilindeki arılıklarda yüksek oranda N.ceranae tespit edilmiştir.

Proje Numarası

VPRTFM- 3/43533

Kaynakça

  • Ansari, MJ., Al-Ghamdi, A., Nuru, A., Khan, KA., Alattal, Y. 2017. Geographical distribution and molecular detection of Nosema ceranae from indigenous honey bees of Saudi Arabia. Saudi J Biol Sci. 24(5):983-991. DOI: 10.1016/j.sjbs.2017.01.054.
  • Bailey, L., Ball, BV. 1981. Honey Bee Pathology. Academic Press, London.
  • 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. Vet. Hung. 63(3):358-69. DOI: 10.1556/004.2015.034.
  • 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. Parasitol Res 115(1):175-81. DOI: 10.1007/s00436-015-4733-3.
  • Fenoy, S., Rueda, C., Higes, M., Martín-Hernández, R., del Aguila, C. 2009. High-level resistance of Nosema ceranae, a parasite of the honeybee, to temperature and desiccation. Appl. Environ. Microbiol. 75(21):6886-6889. doi:10.1128/AEM.01025-0918.
  • Fries, I. 2010. Nosema ceranae in European honey bees (Apis mellifera) J. Invertebr. Pathol. 103(1): S73-S79.DOI: 10.1016/j.jip.2009.06.017.
  • Fries, I., Feng, F., Silva, AD., Slemenda, SB., Pieniazek, NJ. 1996. Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae) Europ. J. Protistol. 32(3):356–365.
  • Glavinic, U., Stevanovic, J., Ristanic, M., Rajkovic, M., Davitkov, D., Lakic, N., & Stanimirovic, Z. 2021. Potential of Fumagillin and Agaricus blazei Mushroom Extract to Reduce Nosema ceranae in Honey Bees. Insects, 12(4), 282. https://doi.org/10.3390/insects12040282
  • Gisder, S., Hedtke, K., Möckel, N., Frielitz, MC., Linde, A., Genersch, E. 2010. Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Appl. Environ. Microbiol. 76(9):3032–3038. DOI: 10.1128/AEM.03097-09.
  • Higes, M., Martín, R., Meana, A. 2006. Nosema ceranae, a new microsporidian parasite in honey bees in Europe. J. Invert. Pathol. 92 (2):93–95.
  • Ivgin Tunca, R., Oskay, D., Gosterit, A., Tekin, OK. 2016. Does Nosema ceranae wipeout Nosema apis in Turkey? Ir. J. Parasitol, 11(2): 259-264.
  • Kazembeyki, MA. 2003. Society, Politics and Economics in Mazandaran, Iran, Routledge Cruzon, London.
  • Khezri, M., Moharrami, M., Modirrousta, H., Torkaman, M., Salehi, S., Rokhzad, B., Khanbabi, H. 2018. Molecular detection of Nosema ceranae in the apiaries of Kurdistan province, Iran. Vet. Res. Forum 9(3):273–278. DOI: 10.30466/vrf.2018.32086.
  • Klee, J., Besana, AM., Genersch, E., Gisder. S., Nanetti, A., Tam, DQ., Chinh, TX., Puerta, F., Ruz, JM, Kryger, P., Message, D., Hatjina, F., Korpela, S., Fries, I., Paxton, RJ. 2007. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera, J. Invertebr. Pathol. 96(1): 1-10. DOI: 10.1016/j.jip.2007.02.014.
  • Lotfi, A., Jamshidi, R., Aghdam Shahryar, H., Yousefkhani, M. 2009.The prevalence of nosemosis in honey bee colonies in Arasbaran region (Northwestern Iran). J. Agri Environ. Sci. 5(2): 255-257.
  • McCallum, R. Olmstead, S. Shaw, J. Glasgow, K. 2020. Evaluating efficacy of Fumagilin-B® against Nosemosis and tracking seasonal trends of Nosema spp. in Nova Scotia Honey bee colonies. J.Apic. Sci.2020.64(2):277-286.
  • Martín-Hernández, R., Meana, A., Prieto, L., Salvador, AM., Garrido-Bailón, E., Higes, M. 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl. Environ. Microbiol. 73:6331-6338. DOI: 10.1128/AEM.00270-07.
  • 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. Pol. J. Vet. Sci. 14(3):385-91. DOI: 10.2478/v10181-011-0058-z.
  • Mohammadian, B., Bokaie, S., Moharrami, M., Nabian, S., Forsi, M. 2018. Distribution of Nosema spp. in climatic regions of Iran. Vet Res Forum. 9(3):259–263. DOI: 10.30466/vrf.2018.32082.
  • Moradi, M. 2019. Survey of Thymus volgaris ethanolic effects on the Nosema parasite in honeybee. Iranian. H. Sci.Tech .9 (17): 24-32.
  • Moshverinia, A., Abedi, V., Safaie, H. 2012. A survey of Nosema apis infection in apiaries of North Khorasan province, Iran. Ir. J Vet Sci Tech 4: 25-30. DOI: 10.22067/veterinary.v4i2.17418.
  • Nabian, S., Ahmadi, K., Shirazi, MN., Gerami Sadeghian, A. 2011. First detection of Nosema ceranae, a microsporidian protozoon of European honeybees (Apis mellifera) in Iran. Ir.J.Parasitol. 6: 89-95. PMID: 22347302.
  • OIE. 2019. Manual for diagnostic tests and vaccines for terrestrial animals, Nosemosis of honey bees, Paris.
  • Papini, R., Mancianti, F., Canovai, R., Cosci, F., Rocchigiani, G., Benelli, G., Canale, A. 2017. Prevalence of the microsporidian Nosema ceranae in honeybee (Apis mellifera) apiaries in Central Italy. Saudi. J. Biol. Sci. 24 (5):979-982. DOI: 10.1016/j.sjbs.2017.01.010.
  • Petrie A., Watson P. 2006. Statistic for veterinary and animal science. Blackwell Oxford.
  • Razmaraii, N., Karimi, H. 2010. A survey of Nosema disease of honey bee (Apis mellifera) in East Azarbaijan province of Iran. J. Anim.Vet. Adv. 9: 879-882. DOI: 10.3923/javaa.2010.879.882.
  • 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. Peer J 31;6:e4252. DOI: 10.7717/peerj.4252.
  • Stevanovic, J., Stanimirovic, Z., Genersch, E., Kovacevic, SR., 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.
  • Tavassoli, M., Eiganinejad, S., Alizadeh-Asl, S. 2009. A survey on Nosema apis infection in apiaries of Urmia, North-West of Iran. Ir. J. Vet. Sci. Tech. 1(1): 35-40.
  • Thursfield, MV.1986. Veterinary epidemiology, Butterworth, Guilford, London.
  • Tokarev, YS., Huang, WF, Solter, LF., Malysh, JM., Becnel, JJ., Vossbrinck, CR. 2020. A formal redefinition of the genera Nosema and Vairimorpha (Microsporidia: Nosematidae) and reassignment of species based on molecular phylogenetics. J.Inver. Pathol. 169: 107279, doi.org/10.1016/j.jip.2019.107279.
  • Van den Heever, JP., Thompson, TS., Curtis, JM., Ibrahim, A., Pernal, SF.2014. Fumagillin: an overview of recent scientific advances and their significance for apiculture. J. Agric. Food. Chem. 62:2728–37. doi: 10.1021/jf4055374.
  • Webster, TC., Pomper, KW., Gerg, H., Thacker, EM., Jones, SC. 2004. Nosema apis infection in worker and queen Apis mellifera. Apidologie. 35(1): 49–54.
  • Williams, GR., Shutler, D., Little, CM., Burgher MacLellan, KL., Rogers, REL. (2010). The microsporidian Nosema ceranae, the antibiotic Fumagilin B, and western honey bee (Apis mellifera) colony strength. Apidologie 42 (1): 15 22.
Toplam 34 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Veteriner Cerrahi
Bölüm Araştırma Makaleleri
Yazarlar

Ali Shirzadi Bu kişi benim 0000-0002-3803-3727

Gholamreza Razmi 0000-0002-0754-1278

Proje Numarası VPRTFM- 3/43533
Yayımlanma Tarihi 11 Kasım 2021
Kabul Tarihi 19 Ekim 2021
Yayımlandığı Sayı Yıl 2021 Cilt: 21 Sayı: 2

Kaynak Göster

Vancouver Shirzadi A, Razmi G. A MICROSCOPY AND MOLECULAR STUDIES OF NOSEMA CERANAE INFECTION IN MAZANDARAN PROVINCE OF IRAN. U.Arı D.-U.Bee J. 2021;21(2):198-205.

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