Ankara Üniversitesi Veteriner Fakültesi Dergisi
Research Article
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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

Year 2022, Volume: 69 Issue: 3, 303 - 311, 30.06.2022

Ayşegül USTA Yakup YILDIRIM

https://doi.org/10.33988/auvfd.824882

Abstract

Viruses are one of the most potential risk factors that negatively affect the different life stages of honey bees. This study was conducted to determine the presence of infections caused by the deformed wing virus (DWV), black queen cell virus (BQCV), and acute bee paralysis virus (ABPV) in honey bees in the beekeeping regions of Burdur, along with obtaining information about their prevalence in this particular region. In our study, the adult bees were taken from 31 different beehives and comb samples that had different honey bee breeds and were sampled randomly from 15 beekeeping areas within the region. The collected samples were analyzed using the reverse transcriptase-polymerase chain reaction (RT-PCR), and the prevalence of DWV, BQCV, and ABPV infections were determined to be 74.19% (23/31), 25.81%, (8/31) and 74.19% (23/31), respectively. In this study, the distribution of positive samples and the rates of multiple infections were determined in the colonies. Of the positive honey bee samples, 12 (%38.71) were detected only for one virus, 9 (%29.03) were positive for two viruses (DWV-ABPV) and 8 (%25.81) were positive for all three viruses. In the present study, the presence of the three bee viruses that caused significant damage to the colonies by multiple infections in the Burdur region was determined with RT-PCR. To our knowledge, this is the first report of three mentioned bee infections in honey bees in the Burdur region. The revealed epidemiological conditions lead to the conclusion that serious measures are needed to control these infections in this region.

Keywords

Acute bee paralysis virus, black queen cell virus, deformed wing virus, honey bee, RT-PCR

References

  • Allen MF, Ball BV (1996): The incidence and World distribution of honey bee viruses. Bee World, 77, 141–162.
  • Anderson D (2005): Triggering virus replication in honey bees. Bee Research And Virus in Europe. 24-26. In: Proceedings of the meeting in Sophia-Antipolis, France.
  • Antúnez K, D’Alessandro B, Corbella E, et al (2006): Honey bee viruses in Uruguay. J Invertebrat Pathol, 93, 67-70.
  • Bailey L, Ball BV, Perry JN (1983): Association of viruses with two protozoal pathogens of the honey bee. Ann of Appl Biol, 103, 13-20.
  • Bailey L, Woods RD (1977): Two more small RNA viruses from honey bees and further observations on sacbrood and acute bee-paralysis viruses. J Gen Virol, 37, 175-182.
  • Baker AC, Schroeder DC (2008): Occurrence and genetic analysis of picorna-like viruses infecting worker bees of Apis mellifera L. populations in Devon, South West England. J Invertebr Pathol, 98, 239-242.
  • Berényi O, Bakonyi T, Derakhshifar I, et al (2006): Occurrence of six honey bee viruses in diseased Austrian apiaries. Appl Environ Microbiol, 72, 2414-2420.
  • Chantawannakul P, Ward L, Boonham N, et al (2006): A scientific note on the detection of honey bee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Thai honey bee (Apis mellifera) apiary. J Invertebr Pathol, 91, 69-73.
  • Chen YP, Evans J, Feldlaufer M (2006): Horizontal and vertical transmission of viruses in the honey bee (Apis mellifera). J Invertebr Pathol, 92,152-159.
  • Çağırgan AA (2018): Ege Bölgesinde Virus Nedenli Arı Hastalıklarının Multipleks Polimeraz Zincir Reaksiyonu İle Araştırılması. Doktora Tezi. Ondokuz Mayıs Üniversitesi Sağlık Bilimleri Enstitüsü, Samsun.
  • De Jong D, De Jong PH, Gonçalves LS (1982): Weight loss and other damage to developing worker honey bees from infestation with Varroa jacobsoni. J Apic Res, 21, 165-167.
  • De Miranda JR, Cordoni G, Budge G (2010): The Acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J Invertebr Pathol, 103, 30–47.
  • Erganiş O (1993): Veteriner Epidemiyoloji (Temel Bilgiler). 74-79. Mimoza Yayınları:16, Sağlık Bilimleri Dizisi: 2, Konya.
  • Fievet J, Tentcheva D, Gauthier G, et al (2006): Localization of deformed wing virus infection in queen and drone Apis mellifera L. Virol J, 3, 16.
  • Gajger I, Kolodziejek J, Bakonyi T, et al (2014): Prevalence and distribution patterns of seven different honey bee viruses in diseased colonies: a case study from Croatia. Apidologie, 45, 701-706.
  • Garigliany M, Agrebi NE, Franssen M, et al (2018): Moku virus detection in honey bees Belgium, 2018. Wiley Transbound Emerg Dis, 66, 43-46.
  • Gülmez Y, Bursalı A, Tekin Ş (2009): First molecular detection and characterization of Deforme dwing virus (DWV) in honey bee (Apis melifera) in Turkey. African J Biotechnol, 8, 3698-3702.
  • Gümüşova SO, Albayrak H, Kurt M, et al (2010): Prevalence of three honey bee viruses in Turkey. Veterinarski Arhiv, 80, 779-785.
  • Haddad N, Brake M, Migdadi H, et al (2008): First detection of honey bee viruses in jordan by Rt-Pcr. Jordan J Agricul Sci, 4, 3.
  • Kalaycı G, Cagırgan AA, Kaplan M, et al (2020): The Role of Viral and Parasitic Pathogens Affected By Colony Losses in Turkish Apiaries. Kafkas Univ Vet Fak Derg, 26, 671-677.
  • Karapınar Z, Oğuz B, Dinçer E, et al (2018): Phylogenetic analysis of black queen cell virus and deformed wing virus in honey bee colonies infected by mites in Van, Eastern Turkey. Med Weter, 74, 460-465.
  • Khongphinitbunjong K, De Guzman LI, Tarver MR, et al (2015): Interactions of Tropilaelaps mercedesae, honey bee viruses and immune response in Apis mellifera. J Apic Res, 54, 40-47.
  • Kovac H, Crailsheim K (1988): Life span of Apis mellifera Carnica Pollm. infested by Varroa jacobsoni in relation to season and extent of infestation. J Apic Res, 27, 230-238.
  • Kubaa RA, Molınatto G, Khaled BS, et al (2018): First detection of black queen cell virus, Varroa destructor macula-like virus, Apis mellifera filamentous virus and Nosema ceranae in Syrian honey bees Apis mellifera syriaca. Bull Insectology, 71, 217-224.
  • Lanzi G, De Miranda JR, Boniotti MB, et al (2006): Molecular and biological characterization of deformed wing virus of honey bees (Apis mellifera L). J Virology, 80, 4998-5009.
  • Leat N, Ball B, Govan V, et al (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.
  • Levin S, Sela N, Erez T, et al (2019): New Viruses from the Ectoparasite Mite Varroa destructor Infesting Apis mellifera and Apis cerana. Viruses, 11, 94.
  • Maramorosch K, Shatkin A (2007): Honey bee viruses. Advances in Virus Research, Academic Press, 33-80.
  • Molineri AI, Pacini A, Giacobino A, et al (2017): Prevalence of honey bee (Apis mellifera) viruses in temperate and subtropical regions from Argentina. Rev Argent Microbiol, 49, 166-173.
  • Moore PA, Wilson ME, Skinner JA (2015): Honey bee viruses, the deadly Varroa Mite Associates. Bee Health, 19, 2015.
  • Nielsen SL, Nicolaisen M, Kryger P (2008): Incidence of Acute bee paralysis virus, Black queen cell virus, Chronic bee paralysis virus, Deformed wing virus, Kashmir bee virus and Sacbrood virus in honey bees (Apis mellifera) in Denmark. Apidologie, 39, 310-314.
  • Oğuz B, Karapınar Z, Dinçer E, et al (2017): Molecular detection of Nosema spp. and black queen-cell virus in honey bees in Van Province, Turkey. Turk J Vet Anim Sci, 41, 221-227.
  • Roberts JMK, Anderson DL, Durr PA (2017): Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honey bee viral landscapes and colony losses. Sci Rep, 7, 6925.
  • Rodríguez M, Vargas M, Antúnez K, et al (2014): Prevalence and phylogenetic analysis of honey bee viruses in the Biobío Region of Chile and their association with other honey bee pathogens. Chilean J Agricu, 74, 170-177.
  • Rodriguez M, Vargas M, Gerding M, et al (2012): Viral infeciton and Nosema ceranae in honey bees in Chile. J Apicul Res, 51, 285-287.
  • Rüstemoğlu M (2015): Hakkari İli Bal Arılarında (Apis Mellifera L.) Görülen Önemli Arı Viruslarının RT-PCR Yöntemi İle Araştırılması Ve Moleküler Karakterizasyonlarının Yapılması. Doktora Tezi. Van Yüzüncü Yıl Üniversitesi Fen Bilimleri Enstitüsü, Van.
  • Sanpa S, Chantawannakul P (2009): Survey of six bee viruses using RT-PCR in Northern Thailand. J Invertebr Pathol, 100, 116-119.
  • Schatton-Gadelmayer K, Engels W (1988): Hamolymphproteine und Korpergewicht frischgeschlupfter Bienen-Arbeiterinnen nach unterschiedlich starker Parasitierung durch Brutmilben. Entomol Gen, 14, 93-101.
  • Sguazza GH, Reynaldi FJ, Galosi CM, et al (2013): Simultaneous detection of bee viruses by multiplex PCR. J Virol Methods, 194, 102-106.
  • Shimanuki H, Calderone NW, Knox DA (1994): Parasitic mite syndrome: The symptoms. Am Bee J, 134, 827-828.
  • Shumkova R, Neov B, Sirakova D, et al (2018): Molecular detection and phylogenetic assessment of six honey bee viruses in Apis mellifera L. colonies in Bulgaria. Peer J, 20, 6:e5077.
  • Spurny R, Pridal A, Pálková L, et al (2017): Virion structure of black queen cell virus, a common honey bee pathogen. J Virol, 91, e02100-16.
  • Tapaszti Z, Forgach P, Kovágó C, et al (2009): Genetic analysis and phylogenetic comparison of Black queen cell virus genotypes. Vet Microbial, 139, 227-234.
  • Tentcheva D, Gauthier L, Zappulla N, et al (2004): Prevalence and Seasonal Variations of Six Bee Viruses in Apis mellifera L. and Varroa destructor Mite Populations in France. Appl Environ Microbiol, 7185-7191.
  • Valles SM, Chen YP, Firth AE, et al (2017): ICTV virus taxonomy profile: iflaviridae. J Gen Virolo, 98, 527–528.
  • Valles SM, Chen YP, Firth AE, et al (2017): ICTV virus taxonomy profile: dicistroviridae. J Gen Virolo, 98, 355–356.
  • Wang M, Bi J, Wang L, et al (2016): Prevalence of Four Common Bee RNA Viruses in Eastern Bee Populations in Yunnan Province, China. J Veterinar Sci Technol, 7, 1.
  • Weinberg KP, Madel G (1985): The inxuence of the mite Varroa jacobsoni Oud. on the protein concentration and hemolymph volume of the blood of the worker bees and drones of the honey bee, Apis mellifera. Apidologie, 16, 421-436.
  • Yang X, Cox-Foster DL (2005): Impact of an ectoparasite on the immuni and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Natl Acad Sci, 102, 7470-7475.
  • Yue C, Genersch E (2005): RT-PCR analysis of Deformed wing virus (DWV) in honey bees (Apis mellifera) and mites (Varroa destructor). J Gen Virol, 86, 3419-3424.

Year 2022, Volume: 69 Issue: 3, 303 - 311, 30.06.2022

Ayşegül USTA Yakup YILDIRIM

https://doi.org/10.33988/auvfd.824882

Abstract

References

  • Allen MF, Ball BV (1996): The incidence and World distribution of honey bee viruses. Bee World, 77, 141–162.
  • Anderson D (2005): Triggering virus replication in honey bees. Bee Research And Virus in Europe. 24-26. In: Proceedings of the meeting in Sophia-Antipolis, France.
  • Antúnez K, D’Alessandro B, Corbella E, et al (2006): Honey bee viruses in Uruguay. J Invertebrat Pathol, 93, 67-70.
  • Bailey L, Ball BV, Perry JN (1983): Association of viruses with two protozoal pathogens of the honey bee. Ann of Appl Biol, 103, 13-20.
  • Bailey L, Woods RD (1977): Two more small RNA viruses from honey bees and further observations on sacbrood and acute bee-paralysis viruses. J Gen Virol, 37, 175-182.
  • Baker AC, Schroeder DC (2008): Occurrence and genetic analysis of picorna-like viruses infecting worker bees of Apis mellifera L. populations in Devon, South West England. J Invertebr Pathol, 98, 239-242.
  • Berényi O, Bakonyi T, Derakhshifar I, et al (2006): Occurrence of six honey bee viruses in diseased Austrian apiaries. Appl Environ Microbiol, 72, 2414-2420.
  • Chantawannakul P, Ward L, Boonham N, et al (2006): A scientific note on the detection of honey bee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Thai honey bee (Apis mellifera) apiary. J Invertebr Pathol, 91, 69-73.
  • Chen YP, Evans J, Feldlaufer M (2006): Horizontal and vertical transmission of viruses in the honey bee (Apis mellifera). J Invertebr Pathol, 92,152-159.
  • Çağırgan AA (2018): Ege Bölgesinde Virus Nedenli Arı Hastalıklarının Multipleks Polimeraz Zincir Reaksiyonu İle Araştırılması. Doktora Tezi. Ondokuz Mayıs Üniversitesi Sağlık Bilimleri Enstitüsü, Samsun.
  • De Jong D, De Jong PH, Gonçalves LS (1982): Weight loss and other damage to developing worker honey bees from infestation with Varroa jacobsoni. J Apic Res, 21, 165-167.
  • De Miranda JR, Cordoni G, Budge G (2010): The Acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J Invertebr Pathol, 103, 30–47.
  • Erganiş O (1993): Veteriner Epidemiyoloji (Temel Bilgiler). 74-79. Mimoza Yayınları:16, Sağlık Bilimleri Dizisi: 2, Konya.
  • Fievet J, Tentcheva D, Gauthier G, et al (2006): Localization of deformed wing virus infection in queen and drone Apis mellifera L. Virol J, 3, 16.
  • Gajger I, Kolodziejek J, Bakonyi T, et al (2014): Prevalence and distribution patterns of seven different honey bee viruses in diseased colonies: a case study from Croatia. Apidologie, 45, 701-706.
  • Garigliany M, Agrebi NE, Franssen M, et al (2018): Moku virus detection in honey bees Belgium, 2018. Wiley Transbound Emerg Dis, 66, 43-46.
  • Gülmez Y, Bursalı A, Tekin Ş (2009): First molecular detection and characterization of Deforme dwing virus (DWV) in honey bee (Apis melifera) in Turkey. African J Biotechnol, 8, 3698-3702.
  • Gümüşova SO, Albayrak H, Kurt M, et al (2010): Prevalence of three honey bee viruses in Turkey. Veterinarski Arhiv, 80, 779-785.
  • Haddad N, Brake M, Migdadi H, et al (2008): First detection of honey bee viruses in jordan by Rt-Pcr. Jordan J Agricul Sci, 4, 3.
  • Kalaycı G, Cagırgan AA, Kaplan M, et al (2020): The Role of Viral and Parasitic Pathogens Affected By Colony Losses in Turkish Apiaries. Kafkas Univ Vet Fak Derg, 26, 671-677.
  • Karapınar Z, Oğuz B, Dinçer E, et al (2018): Phylogenetic analysis of black queen cell virus and deformed wing virus in honey bee colonies infected by mites in Van, Eastern Turkey. Med Weter, 74, 460-465.
  • Khongphinitbunjong K, De Guzman LI, Tarver MR, et al (2015): Interactions of Tropilaelaps mercedesae, honey bee viruses and immune response in Apis mellifera. J Apic Res, 54, 40-47.
  • Kovac H, Crailsheim K (1988): Life span of Apis mellifera Carnica Pollm. infested by Varroa jacobsoni in relation to season and extent of infestation. J Apic Res, 27, 230-238.
  • Kubaa RA, Molınatto G, Khaled BS, et al (2018): First detection of black queen cell virus, Varroa destructor macula-like virus, Apis mellifera filamentous virus and Nosema ceranae in Syrian honey bees Apis mellifera syriaca. Bull Insectology, 71, 217-224.
  • Lanzi G, De Miranda JR, Boniotti MB, et al (2006): Molecular and biological characterization of deformed wing virus of honey bees (Apis mellifera L). J Virology, 80, 4998-5009.
  • Leat N, Ball B, Govan V, et al (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.
  • Levin S, Sela N, Erez T, et al (2019): New Viruses from the Ectoparasite Mite Varroa destructor Infesting Apis mellifera and Apis cerana. Viruses, 11, 94.
  • Maramorosch K, Shatkin A (2007): Honey bee viruses. Advances in Virus Research, Academic Press, 33-80.
  • Molineri AI, Pacini A, Giacobino A, et al (2017): Prevalence of honey bee (Apis mellifera) viruses in temperate and subtropical regions from Argentina. Rev Argent Microbiol, 49, 166-173.
  • Moore PA, Wilson ME, Skinner JA (2015): Honey bee viruses, the deadly Varroa Mite Associates. Bee Health, 19, 2015.
  • Nielsen SL, Nicolaisen M, Kryger P (2008): Incidence of Acute bee paralysis virus, Black queen cell virus, Chronic bee paralysis virus, Deformed wing virus, Kashmir bee virus and Sacbrood virus in honey bees (Apis mellifera) in Denmark. Apidologie, 39, 310-314.
  • Oğuz B, Karapınar Z, Dinçer E, et al (2017): Molecular detection of Nosema spp. and black queen-cell virus in honey bees in Van Province, Turkey. Turk J Vet Anim Sci, 41, 221-227.
  • Roberts JMK, Anderson DL, Durr PA (2017): Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honey bee viral landscapes and colony losses. Sci Rep, 7, 6925.
  • Rodríguez M, Vargas M, Antúnez K, et al (2014): Prevalence and phylogenetic analysis of honey bee viruses in the Biobío Region of Chile and their association with other honey bee pathogens. Chilean J Agricu, 74, 170-177.
  • Rodriguez M, Vargas M, Gerding M, et al (2012): Viral infeciton and Nosema ceranae in honey bees in Chile. J Apicul Res, 51, 285-287.
  • Rüstemoğlu M (2015): Hakkari İli Bal Arılarında (Apis Mellifera L.) Görülen Önemli Arı Viruslarının RT-PCR Yöntemi İle Araştırılması Ve Moleküler Karakterizasyonlarının Yapılması. Doktora Tezi. Van Yüzüncü Yıl Üniversitesi Fen Bilimleri Enstitüsü, Van.
  • Sanpa S, Chantawannakul P (2009): Survey of six bee viruses using RT-PCR in Northern Thailand. J Invertebr Pathol, 100, 116-119.
  • Schatton-Gadelmayer K, Engels W (1988): Hamolymphproteine und Korpergewicht frischgeschlupfter Bienen-Arbeiterinnen nach unterschiedlich starker Parasitierung durch Brutmilben. Entomol Gen, 14, 93-101.
  • Sguazza GH, Reynaldi FJ, Galosi CM, et al (2013): Simultaneous detection of bee viruses by multiplex PCR. J Virol Methods, 194, 102-106.
  • Shimanuki H, Calderone NW, Knox DA (1994): Parasitic mite syndrome: The symptoms. Am Bee J, 134, 827-828.
  • Shumkova R, Neov B, Sirakova D, et al (2018): Molecular detection and phylogenetic assessment of six honey bee viruses in Apis mellifera L. colonies in Bulgaria. Peer J, 20, 6:e5077.
  • Spurny R, Pridal A, Pálková L, et al (2017): Virion structure of black queen cell virus, a common honey bee pathogen. J Virol, 91, e02100-16.
  • Tapaszti Z, Forgach P, Kovágó C, et al (2009): Genetic analysis and phylogenetic comparison of Black queen cell virus genotypes. Vet Microbial, 139, 227-234.
  • Tentcheva D, Gauthier L, Zappulla N, et al (2004): Prevalence and Seasonal Variations of Six Bee Viruses in Apis mellifera L. and Varroa destructor Mite Populations in France. Appl Environ Microbiol, 7185-7191.
  • Valles SM, Chen YP, Firth AE, et al (2017): ICTV virus taxonomy profile: iflaviridae. J Gen Virolo, 98, 527–528.
  • Valles SM, Chen YP, Firth AE, et al (2017): ICTV virus taxonomy profile: dicistroviridae. J Gen Virolo, 98, 355–356.
  • Wang M, Bi J, Wang L, et al (2016): Prevalence of Four Common Bee RNA Viruses in Eastern Bee Populations in Yunnan Province, China. J Veterinar Sci Technol, 7, 1.
  • Weinberg KP, Madel G (1985): The inxuence of the mite Varroa jacobsoni Oud. on the protein concentration and hemolymph volume of the blood of the worker bees and drones of the honey bee, Apis mellifera. Apidologie, 16, 421-436.
  • Yang X, Cox-Foster DL (2005): Impact of an ectoparasite on the immuni and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Natl Acad Sci, 102, 7470-7475.
  • Yue C, Genersch E (2005): RT-PCR analysis of Deformed wing virus (DWV) in honey bees (Apis mellifera) and mites (Varroa destructor). J Gen Virol, 86, 3419-3424.

Details

Primary Language English
Subjects Veterinary
Journal Section Research Article
Authors

Ayşegül USTA
BURDUR MEHMET AKİF ERSOY ÜNİVERSİTESİ, VETERİNER FAKÜLTESİ, VETERİNER PR.
0000-0002-8376-0421
Türkiye

Yakup YILDIRIM
BURDUR MEHMET AKİF ERSOY ÜNİVERSİTESİ, VETERİNER FAKÜLTESİ, VETERİNER PR.
0000-0003-4299-4712
Türkiye

Supporting Institution This research was supported by Burdur Mehmet Akif Ersoy University Scientific Research Projects Unit with project number 0586-YL-19.
Project Number 0586-YL-19
Thanks We thank Dr. A. Anıl Çağırgan and İzmir/Bornova Veterinary Control Institute for their contributions. This study represents part of the thesis submitted by A. Usta to the Virology Department of Veterinary Medicine Faculty of Burdur Mehmet Akif University, Burdur, Turkey, to fulfill the requirements for a master's degree in veterinary medicine.
Publication Date June 30, 2022
Published in Issue Year 2022Volume: 69 Issue: 3

Cite

Bibtex @research article { auvfd824882, journal = {Ankara Üniversitesi Veteriner Fakültesi Dergisi}, issn = {1300-0861}, eissn = {1308-2817}, address = {}, publisher = {Ankara University}, year = {2022}, volume = {69}, number = {3}, pages = {303 - 311}, doi = {10.33988/auvfd.824882}, title = {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}, key = {cite}, author = {Usta, Ayşegül and Yıldırım, Yakup} }
APA 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 (3) , 303-311 . DOI: 10.33988/auvfd.824882
MLA Usta, A. , Yıldırım, Y. "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 (2022 ): 303-311 <http://vetjournal.ankara.edu.tr/en/pub/issue/70947/824882>
Chicago Usta, A. , Yıldırım, Y. "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 (2022 ): 303-311
RIS TY - JOUR T1 - 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 AU - AyşegülUsta, YakupYıldırım Y1 - 2022 PY - 2022 N1 - doi: 10.33988/auvfd.824882 DO - 10.33988/auvfd.824882 T2 - Ankara Üniversitesi Veteriner Fakültesi Dergisi JF - Journal JO - JOR SP - 303 EP - 311 VL - 69 IS - 3 SN - 1300-0861-1308-2817 M3 - doi: 10.33988/auvfd.824882 UR - https://doi.org/10.33988/auvfd.824882 Y2 - 2021 ER -
EndNote %0 Ankara Üniversitesi Veteriner Fakültesi Dergisi 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 %A Ayşegül Usta , Yakup Yıldırım %T 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 %D 2022 %J Ankara Üniversitesi Veteriner Fakültesi Dergisi %P 1300-0861-1308-2817 %V 69 %N 3 %R doi: 10.33988/auvfd.824882 %U 10.33988/auvfd.824882
ISNAD Usta, Ayşegül , Yıldırım, Yakup . "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 / 3 (June 2022): 303-311 . https://doi.org/10.33988/auvfd.824882
AMA Usta A. , Yıldırım Y. 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 Univ Vet Fak Derg. 2022; 69(3): 303-311.
Vancouver Usta A. , Yıldırım Y. 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. 2022; 69(3): 303-311.
IEEE A. Usta and Y. Yıldırım , "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, vol. 69, no. 3, pp. 303-311, Jun. 2022, doi:10.33988/auvfd.824882
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