Araştırma Makalesi
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İsrail Akut Arı Felci Virüsü’nün Türkiye’de Koloni Kayıplı Arılıklardaki Yaygınlığı

Yıl 2023, Cilt: 23 Sayı: 1, 105 - 114, 19.05.2023

Dilek Muz Mustafa Necati Muz

https://doi.org/10.31467/uluaricilik.1265816

Öz

Bal arıları bitkisel tozlaşma ve biyoçeşitliliğin devamında vazgeçilmez polinatör böceklerdir. Ayrıca bal, propolis, polen arısütü gibi ürünleriyle tıbbi öneme sahiptirler. Ani arı ölümleri ve koloni çöküş bozukluğu (CCD) koloni sağlığının sürdürülebilirliğini tehdit eder. Bal arısı virüsleri, parazit ve patojenleri koloni kayıplarını ve CCD-benzeri problemleri tetikler. Bu araştırmada 2011- 2021 yılları arasında Türkiye’de farklı eko-coğrafik bölgelerdeki 16 ilde ani arı ölümleri, koloni kayıpları ve CCD yaşanan arılıklarda Israil akut arı felci virüsünün (IAPV) varlığı ve yaygınlığının tespiti amaçlanmıştır. Örnekler patojenlerinin IAPV ile bir arada bulunması açısından test edildi. Örneklenen arılıklar arı patojenlerinden Akut arı felci virüsü, Siyah kraliçe arı virüsü, Kronik arı felci virüsü, Deforme kanat virüsü, Kaşmir arı virüsü, Lake Sinai virüsü, Sakbrood virüs, Varroa akarları ve Nosema sp. yönünden analiz edildi. Arı virüsleri için patojen spesifik RT-PCR testleri kullanıldı. Örneklenen arılıkların %97,5’i en az bir patojen yönünden pozitif bulunurken, IAPV pozitifliği %52,5 olarak tespit edildi. Araştırma sonuçlarına göre, koloni kaybı ve CCD-benzeri problemler yaşanan arılıklarda IAPV’nin yaygınlığının önceki raporlara kıyasla daha yüksek olduğu belirlendi. IAPV pozitif arılıklarda farklı türlerdeki virüsler, Nosema sp. ve varroa enfestasyonuna rastlanıldığı tespit edildi. Sonuçlar IAPV ile birlikte çoklu patojen pozitifliğinin koloni kayıplarında etkili olabileceğini düşündürmektedir.

Anahtar Kelimeler

IAPV Bal Arısı Virüsleri CCD Koloni Kaybı Türkiye

Kaynakça

  • Amiri E, Seddon G, Zuluaga Smith W, Strand MK, Tarpy DR, Rueppell O. Israeli Acute Paralysis Virus: Honey Bee Queen–Worker Interaction and Potential Virus Transmission Pathways. Insects. 2019; 10(1):9.
  • Berenyi O, Bakonyi T, Derakhshifar I, Koglberger H, Nowotny N. Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl. Environ. Microbiol. 2006; 72 (4): 2414–20.
  • Berthoud H, Imdorf A, Haueter M, Radloff S, Neumann P. Virus infections and winter losses of honey bee colonies (Apis mellifera). J. Apicult. Res. 2010; 49, 60–65.
  • Botias C, Martín-Hernández R, Barrios L, Meana A, Higes M. Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet. Res. 2013; 44, 25.
  • Chen Y, Zhao Y, Hammond J, Hsu HT, Evans J, Feldlaufer M. Multiple virus infections in the honey bee and genome divergence of honey bee viruses. J. Invertebr Pathol. 2004 Oct-Nov;87(2-3):84-93.
  • Chen Y, Pettis JS, Feldlaufer MF. Detection of multiple viruses in queens of the honey bee Apis mellifera L. J. Invertebr. Pathol. 2005; 90: 118–121.
  • Chen YP, Pettis JS, Corona M, Chen WP, Li CJ, Spivak M, Visscher PK, DeGrandi-Hoffman G, Boncristiani H, Zhao Y, vanEngelsdorp D, Delaplane K, Solter L, Drummond F, Kramer M, Lipkin WI, Palacios G, Hamilton MC, Smith B,
  • Huang SK, Zheng HQ, Li JL, Zhang X, Zhou AF, Wu LY, Zhou JZ, Lee ML, Teixeira EW, Li ZG, Evans JD. Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health. PLoS Pathog. 2014;31;10(7): e1004261. doi: 10.1371/journal.ppat.1004261.
  • Cornman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D, Pettis JS, vanEngelsdorp D, Evans JD. Pathogen webs in collapsing honey bee colonies, PLoS ONE, 2012; 7: e43562
  • Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M, Geiser DM, Martinson V, vanEngelsdorp D, Kalkstein AL, Drysdale A, Hui J, Zhai J, Cui L, Hutchison SK, Simons JF, Egholm M,
  • Pettis JS, Lipkin WI. A metagenomic survey of microbes in honey bee colony collapse disorder. Science. 2007; 12;318(5848):283-7. doi: 10.1126/science.
  • Çagirgan AA, Yildirim Y, Usta A. The investigation of Israil acute bee paralysis virus, sacbrood virus, kashmir bee virus and chronic bee paralysis virus in honeybees (Apis mellifera). Eurasian J Vet Sci 2020; 36:2, 96-10. doi:10.15312/EurasianJVetSci.2020.265.
  • Çağirgan AA, Yazici Z. The prevalence of seven crucial honeybee viruses using multiplex RT-PCR and their phylogenetic analysis. Turkish Journal of Veterinary and Animal Sciences, 2021; 45, 44-55. https://doi.org/10.3906/vet-2004-139.
  • Çakmak İ. Bal arısı koloni kayıpları ve çözüm yolları. Ordu Arıcılık Araştırma Dergisi, 2012; 4(7):3-8.
  • Çakmak I. Türkiye’de Arıcılık ve Güncel Koloni Kayıpları. Uludağ Arıcılık Dergisi, 2016;16 (1),31-48. DOI:10.31467/uluaricilik379276.
  • De Miranda JR, Cordoni G, Budge G. The Acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J. Invertebr. Pathol. 2010; 103: 30–47.
  • De Miranda JR, Ribiere CY, Gauthier ML. Varroa and Viruses. In Varroa– still a problem in the 21st century? Carreck NL, editor. Cardiff: IBBA. 2011; 11–31.
  • Del Nozal MJ, Mayo R, Bernal JL. Honeybee colony collapse due to Nosema ceranae in Professional apiaries. Environ. Microbiol. Rep. 2009;1: 110–113.
  • Di Prisco G, Pennacchio F, Caprio E, Boncristiani HF, Evans JD, Chen Y. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J Gen Virol., 2011; 92: 151–155.
  • Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C, Büchler R, Berg S, Ritter W, Mühlen W, Gisder S, Meixner M, Liebig G, Rosenkranz P. The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie, 2010; 41, 332–352. https://doi.org/10.1051/apido/2010014
  • Güller A, Kurt Z. Occurrence and Molecular Phylogeny of Economically Relevant Viruses Infecting Honey Bees (Apis mellifera L.) of Bingöl Province, Turkey. Journal of apicultural science, 2021; 66, 85-96. doi: 10.2478/jas-2022-0006
  • Gülmez Y, Bursalı A, Tekin S. Molecular detection and characterization of deformed wing virus (DWV) in honeybees (Apis mellifera L.) and mite (Varroa destructor) in Turkey. African Journal of Biotechnology, 2009; 8(16):3698-3702.
  • Gümüşova-Okursoy S, Albayrak H, Kurt M, Yazıcı Z. Prevalence of three honey bee viruses in Turkey. Veterınarskı Arhıv, 2010; 80 (6): 779-785.
  • Hails RS, Ball BV, Genersch E. Infection strategies of insect viruses M. Aubert, B.V. Ball, I. Fries, R. F. A. Moritz, N. Milani, I. Bernardinelli (Eds.), Virology and the Honey Bee, European Communities (2008), pp.255-275
  • Ivgin-Tunca R, Oskay D, Gosterit A, Tekin OK. Does Nosema ceranae Wipe Out Nosema apis in Turkey? Iran J Parasitol. 2016;11(2):259-264.
  • Kalaycı G, Cagirgan AA, Kaplan M, Pekmez K, Beyazit A, Ozkan B, Arslan F. The Role of Viral and Parasitic Pathogens Affected By Colony Losses in Turkish Apiaries. Journal of Kafkas University Faculty of Veterinary Medicine, 2020; 26(5), 671-677. https://doi.org/10.9775/kvfd.2020.24154.
  • Kartal S, Ivgin Tunca R, Özgül O, Karabağ K, koç H. Microscopic and Molecular Detection of Nosema sp. İn the Southwest Aegean Region. Uludağ Arıcılık Dergisi, 2021; 21 (1),8-20. DOI:10.31467/uluaricilik.880380.
  • Maori E, Lavi S, Mozes-Koch R, Gantman Y, Peretz Y, Edelbaum O, Tanne E, Sela I. Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: Evidence for diversity due to intra- and inter-species recombination. J. Gen. Virol. 2007; 88: 3428–3438.
  • Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE, Powel M, Nikaido S, Schroeder DC. Global honey bee viral landscape altered by a parasitic mite. Science, 2012; 336: 1304–1306.
  • Martín-Hernández R, Meana A, Prieto L, Salvador AM, Garrido-Bailon E, Higes M. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl. Environ. Microbiol. 2007; 73: 6331–6338.
  • McMenamin AJ, Genersch E. Honey bee colony losses and associated viruses. Curr Opin Insect Sci. 2015; 8:121-129. doi: 10.1016/j.cois.2015.01.015.
  • Muz MN. Bal arılarında ani koloni sönmesi. T Parazitol Derg. 2008; 32 (3): 271-275.
  • Muz D, Muz MN. Survey of the occurrence of Deformed Wing Virus and multiple parasites of queens (Apis mellifera L.) in apiaries with collapsed colonies in Hatay, Turkey. J. Apicult. Res., 2009; 48(3):204-208.
  • Muz MN. Girişgin AO, Muz D, Aydin L. Molecular detection of Nosema ceranae and Nosema apis infections in Turkish apiaries with collapsed colonies. J. Apicult. Res., 2010; 49(4): 342-344.
  • Muz D, Muz MN. A molecular epidemiological study of black queen cell virüs in honeybees (Apis mellifera) of Turkey: the first genetic characterization and phylogenetic analysis of field viruses. Apidologie, 2018; 49: 1-12. https://doi.org/10.1007/s13592-017-0531-5
  • Muz D, Muz MN. Bal Arılarının Viral Hastalıkları, Tanı ve Tedavisi Özdemir N, editör. Veteriner Arı Sağlığı ve Apiterapi, 2021; 1: 24-36
  • Muz D, Muz MN. Investigation of Honeybee Colony Losses in Thrace Region, 4th International Eurasian Conference on Science, Engineering and Technology (EurasianSciEnTech 2022) December 14-16, 2022.
  • Ostroverkhova NV, Konusova OL, Kucher AN, Kireeva TN, Rosseykina SA. Prevalence of the Microsporidian Nosema spp. in Honey Bee Populations (Apis mellifera) in Some Ecological Regions of North Asia. Veterinary Sciences. 2020; 7(3):111. https://doi.org/10.3390/vetsci7030111
  • Özkırım A, Schiesser A. Israeli acute paralysis virus (IAPV) in Turkish bees. J. Apicult. Res., 2013; 52(2): 56-57. Palacios G, Hui J, Quan PL, Kalkstein A, Honkavuori KS, Bussetti AV, Conlan S, Evans J, Chen YP, vanEngelsdorp D,
  • Efrat H, Pettis J, Cox-Foster D, Holmes EC, Briese T, Lipkin WI. Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. J Virol. 2008; 82(13):6209-17. doi: 10.1128/JVI.00251-08.
  • Rüstemoğlu M, Sipahioğlu HM. Occurrence and prevalence of six honey bee viruses in Hakkâri (Turkey) and their genomic divergence. Munis Entomology & Zoology, 2019; 14 (2): 574-583]
  • Stoltz D, Shen XR, Boggis C, Sisson G. Molecular diagnosis of Kashmir bee virus infection, Journal of Apicultural Research. 1995; 34:3, 153-160
  • Tosun O, Yaman M. 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, 2016; 5(11): 513-522., Doi: 10.17265/2162-5263/2016.11.001
  • Ütük AE, Pişkin FC, Girişgin AO, Selçuk O, Aydın L. Microscopic and molecular detection of Nosema spp. in honeybees of Turkey. Apidologie, 2016; 47:267–271. DOI: 10.1007/s13592-015-0394-6.
  • VanEngelsdorp D, Underwood R, Caron D, Hayes JJ. An estimate of managed colony losses in the winter of 2006–2007: A report commissioned by the apiary inspectors of America. Am Bee J. 2007; 147: 599–603
  • Williams GR, Tarpy DR, Vanengelsdorp D, Chauzat MP, Cox-Foster DL. Colony collapse disorder in context. Bioessays, 2010; 32: 845–846.

ISRAEL ACUTE BEE PARALYSIS VIRUS PREVALENCE IN APIARIES WITH COLONY LOSS IN TÜRKİYE

Yıl 2023, Cilt: 23 Sayı: 1, 105 - 114, 19.05.2023

Dilek Muz Mustafa Necati Muz

https://doi.org/10.31467/uluaricilik.1265816

Öz

Honeybees are indispensable pollinator insects for vegetative pollination and biodiversity. Moreover, they serve medicinal importance with products such as honey, propolis, pollen, and royal jelly. Sudden bee deaths and colony collapse disorder (CCD) threaten the sustainability of colony health. Honeybee viruses, parasites, and pathogens trigger colony losses and CCD. This study investigated the presence and prevalence of Israeli acute bee paralysis virus (IAPV) in apiaries with sudden bee deaths, colony losses, and CCD-like problems in 16 provinces in different eco-geographic regions of Türkiye between 2011- 2021. Samples were tested for the coexistence of honeybee pathogens with IAPV. The sampled apiaries were evaluated for other bee pathogens such as Acute bee paralysis virus, Black queen bee virus, Chronic bee paralysis virus, Deformed wing virus, Kashmir bee virus, Lake Sinai virus, Sacbrood virus, Varroa mites, and Nosema sp. analyzed. Pathogen-specific RT-PCR assay was used for bee viruses. IAPV positivity was found to be 52.5% in apiaries. 97.5% of the sampled apiaries were positive for at least one pathogen. According to the results of this study, the presence of IAPV in apiaries suffering from colony loss and CCD-like problems was higher than in previous reports, and viruses of different species, Nosema sp., and varroa infestation were found to be frequently encountered. The results suggest that the coexistence of IAPV and multiple pathogens may be effective in colony losses.

Anahtar Kelimeler

IAPV Honeybee Viruses CCD Colony Losses Türkiye

Kaynakça

  • Amiri E, Seddon G, Zuluaga Smith W, Strand MK, Tarpy DR, Rueppell O. Israeli Acute Paralysis Virus: Honey Bee Queen–Worker Interaction and Potential Virus Transmission Pathways. Insects. 2019; 10(1):9.
  • Berenyi O, Bakonyi T, Derakhshifar I, Koglberger H, Nowotny N. Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl. Environ. Microbiol. 2006; 72 (4): 2414–20.
  • Berthoud H, Imdorf A, Haueter M, Radloff S, Neumann P. Virus infections and winter losses of honey bee colonies (Apis mellifera). J. Apicult. Res. 2010; 49, 60–65.
  • Botias C, Martín-Hernández R, Barrios L, Meana A, Higes M. Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet. Res. 2013; 44, 25.
  • Chen Y, Zhao Y, Hammond J, Hsu HT, Evans J, Feldlaufer M. Multiple virus infections in the honey bee and genome divergence of honey bee viruses. J. Invertebr Pathol. 2004 Oct-Nov;87(2-3):84-93.
  • Chen Y, Pettis JS, Feldlaufer MF. Detection of multiple viruses in queens of the honey bee Apis mellifera L. J. Invertebr. Pathol. 2005; 90: 118–121.
  • Chen YP, Pettis JS, Corona M, Chen WP, Li CJ, Spivak M, Visscher PK, DeGrandi-Hoffman G, Boncristiani H, Zhao Y, vanEngelsdorp D, Delaplane K, Solter L, Drummond F, Kramer M, Lipkin WI, Palacios G, Hamilton MC, Smith B,
  • Huang SK, Zheng HQ, Li JL, Zhang X, Zhou AF, Wu LY, Zhou JZ, Lee ML, Teixeira EW, Li ZG, Evans JD. Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health. PLoS Pathog. 2014;31;10(7): e1004261. doi: 10.1371/journal.ppat.1004261.
  • Cornman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D, Pettis JS, vanEngelsdorp D, Evans JD. Pathogen webs in collapsing honey bee colonies, PLoS ONE, 2012; 7: e43562
  • Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M, Geiser DM, Martinson V, vanEngelsdorp D, Kalkstein AL, Drysdale A, Hui J, Zhai J, Cui L, Hutchison SK, Simons JF, Egholm M,
  • Pettis JS, Lipkin WI. A metagenomic survey of microbes in honey bee colony collapse disorder. Science. 2007; 12;318(5848):283-7. doi: 10.1126/science.
  • Çagirgan AA, Yildirim Y, Usta A. The investigation of Israil acute bee paralysis virus, sacbrood virus, kashmir bee virus and chronic bee paralysis virus in honeybees (Apis mellifera). Eurasian J Vet Sci 2020; 36:2, 96-10. doi:10.15312/EurasianJVetSci.2020.265.
  • Çağirgan AA, Yazici Z. The prevalence of seven crucial honeybee viruses using multiplex RT-PCR and their phylogenetic analysis. Turkish Journal of Veterinary and Animal Sciences, 2021; 45, 44-55. https://doi.org/10.3906/vet-2004-139.
  • Çakmak İ. Bal arısı koloni kayıpları ve çözüm yolları. Ordu Arıcılık Araştırma Dergisi, 2012; 4(7):3-8.
  • Çakmak I. Türkiye’de Arıcılık ve Güncel Koloni Kayıpları. Uludağ Arıcılık Dergisi, 2016;16 (1),31-48. DOI:10.31467/uluaricilik379276.
  • De Miranda JR, Cordoni G, Budge G. The Acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J. Invertebr. Pathol. 2010; 103: 30–47.
  • De Miranda JR, Ribiere CY, Gauthier ML. Varroa and Viruses. In Varroa– still a problem in the 21st century? Carreck NL, editor. Cardiff: IBBA. 2011; 11–31.
  • Del Nozal MJ, Mayo R, Bernal JL. Honeybee colony collapse due to Nosema ceranae in Professional apiaries. Environ. Microbiol. Rep. 2009;1: 110–113.
  • Di Prisco G, Pennacchio F, Caprio E, Boncristiani HF, Evans JD, Chen Y. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J Gen Virol., 2011; 92: 151–155.
  • Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C, Büchler R, Berg S, Ritter W, Mühlen W, Gisder S, Meixner M, Liebig G, Rosenkranz P. The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie, 2010; 41, 332–352. https://doi.org/10.1051/apido/2010014
  • Güller A, Kurt Z. Occurrence and Molecular Phylogeny of Economically Relevant Viruses Infecting Honey Bees (Apis mellifera L.) of Bingöl Province, Turkey. Journal of apicultural science, 2021; 66, 85-96. doi: 10.2478/jas-2022-0006
  • Gülmez Y, Bursalı A, Tekin S. Molecular detection and characterization of deformed wing virus (DWV) in honeybees (Apis mellifera L.) and mite (Varroa destructor) in Turkey. African Journal of Biotechnology, 2009; 8(16):3698-3702.
  • Gümüşova-Okursoy S, Albayrak H, Kurt M, Yazıcı Z. Prevalence of three honey bee viruses in Turkey. Veterınarskı Arhıv, 2010; 80 (6): 779-785.
  • Hails RS, Ball BV, Genersch E. Infection strategies of insect viruses M. Aubert, B.V. Ball, I. Fries, R. F. A. Moritz, N. Milani, I. Bernardinelli (Eds.), Virology and the Honey Bee, European Communities (2008), pp.255-275
  • Ivgin-Tunca R, Oskay D, Gosterit A, Tekin OK. Does Nosema ceranae Wipe Out Nosema apis in Turkey? Iran J Parasitol. 2016;11(2):259-264.
  • Kalaycı G, Cagirgan AA, Kaplan M, Pekmez K, Beyazit A, Ozkan B, Arslan F. The Role of Viral and Parasitic Pathogens Affected By Colony Losses in Turkish Apiaries. Journal of Kafkas University Faculty of Veterinary Medicine, 2020; 26(5), 671-677. https://doi.org/10.9775/kvfd.2020.24154.
  • Kartal S, Ivgin Tunca R, Özgül O, Karabağ K, koç H. Microscopic and Molecular Detection of Nosema sp. İn the Southwest Aegean Region. Uludağ Arıcılık Dergisi, 2021; 21 (1),8-20. DOI:10.31467/uluaricilik.880380.
  • Maori E, Lavi S, Mozes-Koch R, Gantman Y, Peretz Y, Edelbaum O, Tanne E, Sela I. Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: Evidence for diversity due to intra- and inter-species recombination. J. Gen. Virol. 2007; 88: 3428–3438.
  • Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE, Powel M, Nikaido S, Schroeder DC. Global honey bee viral landscape altered by a parasitic mite. Science, 2012; 336: 1304–1306.
  • Martín-Hernández R, Meana A, Prieto L, Salvador AM, Garrido-Bailon E, Higes M. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl. Environ. Microbiol. 2007; 73: 6331–6338.
  • McMenamin AJ, Genersch E. Honey bee colony losses and associated viruses. Curr Opin Insect Sci. 2015; 8:121-129. doi: 10.1016/j.cois.2015.01.015.
  • Muz MN. Bal arılarında ani koloni sönmesi. T Parazitol Derg. 2008; 32 (3): 271-275.
  • Muz D, Muz MN. Survey of the occurrence of Deformed Wing Virus and multiple parasites of queens (Apis mellifera L.) in apiaries with collapsed colonies in Hatay, Turkey. J. Apicult. Res., 2009; 48(3):204-208.
  • Muz MN. Girişgin AO, Muz D, Aydin L. Molecular detection of Nosema ceranae and Nosema apis infections in Turkish apiaries with collapsed colonies. J. Apicult. Res., 2010; 49(4): 342-344.
  • Muz D, Muz MN. A molecular epidemiological study of black queen cell virüs in honeybees (Apis mellifera) of Turkey: the first genetic characterization and phylogenetic analysis of field viruses. Apidologie, 2018; 49: 1-12. https://doi.org/10.1007/s13592-017-0531-5
  • Muz D, Muz MN. Bal Arılarının Viral Hastalıkları, Tanı ve Tedavisi Özdemir N, editör. Veteriner Arı Sağlığı ve Apiterapi, 2021; 1: 24-36
  • Muz D, Muz MN. Investigation of Honeybee Colony Losses in Thrace Region, 4th International Eurasian Conference on Science, Engineering and Technology (EurasianSciEnTech 2022) December 14-16, 2022.
  • Ostroverkhova NV, Konusova OL, Kucher AN, Kireeva TN, Rosseykina SA. Prevalence of the Microsporidian Nosema spp. in Honey Bee Populations (Apis mellifera) in Some Ecological Regions of North Asia. Veterinary Sciences. 2020; 7(3):111. https://doi.org/10.3390/vetsci7030111
  • Özkırım A, Schiesser A. Israeli acute paralysis virus (IAPV) in Turkish bees. J. Apicult. Res., 2013; 52(2): 56-57. Palacios G, Hui J, Quan PL, Kalkstein A, Honkavuori KS, Bussetti AV, Conlan S, Evans J, Chen YP, vanEngelsdorp D,
  • Efrat H, Pettis J, Cox-Foster D, Holmes EC, Briese T, Lipkin WI. Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. J Virol. 2008; 82(13):6209-17. doi: 10.1128/JVI.00251-08.
  • Rüstemoğlu M, Sipahioğlu HM. Occurrence and prevalence of six honey bee viruses in Hakkâri (Turkey) and their genomic divergence. Munis Entomology & Zoology, 2019; 14 (2): 574-583]
  • Stoltz D, Shen XR, Boggis C, Sisson G. Molecular diagnosis of Kashmir bee virus infection, Journal of Apicultural Research. 1995; 34:3, 153-160
  • Tosun O, Yaman M. 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, 2016; 5(11): 513-522., Doi: 10.17265/2162-5263/2016.11.001
  • Ütük AE, Pişkin FC, Girişgin AO, Selçuk O, Aydın L. Microscopic and molecular detection of Nosema spp. in honeybees of Turkey. Apidologie, 2016; 47:267–271. DOI: 10.1007/s13592-015-0394-6.
  • VanEngelsdorp D, Underwood R, Caron D, Hayes JJ. An estimate of managed colony losses in the winter of 2006–2007: A report commissioned by the apiary inspectors of America. Am Bee J. 2007; 147: 599–603
  • Williams GR, Tarpy DR, Vanengelsdorp D, Chauzat MP, Cox-Foster DL. Colony collapse disorder in context. Bioessays, 2010; 32: 845–846.
Toplam 46 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Entomoloji, Ziraat Mühendisliği (Diğer), Veteriner Cerrahi
Bölüm Araştırma Makaleleri
Yazarlar

Dilek Muz 0000-0001-9358-8103

Mustafa Necati Muz

Yayımlanma Tarihi 19 Mayıs 2023
Kabul Tarihi 2 Mayıs 2023
Yayımlandığı Sayı Yıl 2023 Cilt: 23 Sayı: 1

Kaynak Göster

Vancouver Muz D, Muz MN. ISRAEL ACUTE BEE PARALYSIS VIRUS PREVALENCE IN APIARIES WITH COLONY LOSS IN TÜRKİYE. U.Arı D.-U.Bee J. 2023;23(1):105-14.
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