Determination of Mixed Virus Infection in Honey Bees from Erzurum, Türkiye

Year 2023, , 66 - 71, 27.09.2023

Zeynep Selvitopi Gözde Büşra Eroğlu

https://doi.org/10.46810/tdfd.1257690

Cited By: 1

Abstract

Honey bees are the most important pollinators of agricultural products and provide pollination. Especially the worker bees, which make up the majority of the honey bee population, produce products with high economic value such as honey, pollen, propolis, royal jelly, bee venom, and beeswax. Mass deaths are observed in honey bees grown in Erzurum province, where beekeeping activities are carried out intensively in the Eastern Anatolia region of Türkiye. Epidemic diseases seen in honey bees in Erzurum have a very negative effect on the development and progress of beekeeping activities. Most of the diseases that cause epidemics in bees and cause sudden death and colony loss are of viral origin. In this study, viral pathogens that cause death in honey bees in Erzurum province were investigated and it was determined that two honeybee viruses, the black queen cell virus (BQCV), and the deformed wing virus, caused intense epidemics. In addition, phylogenetic analyzes revealed that all BQCV isolates found in this study clustered quite far from BQCV isolates previously isolated from Turkiye, while DWV isolates clustered close to Hakkari and Lithuania isolates.

Keywords

Honey bee viruses, Black queen cell virus, Deformed wing virus, Colony collapse

Supporting Institution

TUBITAK

Project Number

2209-A undergraduate research project

Thanks

This study was financially supported by the Tubitak 2209-A undergraduate research project conducted by Zeynep Selvitopi.

References

• [1] Ruttner F. Biogeography and Taxonomy of Honeybees. 1th ed. Berlin, Germany: Springer; 1988.
• [2] Dietemann V, Pflugfelder J, Anderson D, Charrière JD, Chejanovsky N, Dainat B, ... & Neumann P. Varroa destructor: research avenues towards sustainable control. Journal of Apicultural Research. 2012; 51:125-132.
• [3] Dogaroglu M. Modern arıcılık. Anadolu Matbaa ve Ambalaj San. Tic. Ltd. Şti. İstanbul; 1999.
• [4] Antunez K, D’Alessandro B, Corbella E, Ramallo G, Zunino P. Honey bee viruses in Uruguay. Journal of Invertebrate Pathology. 2006;93:67–70.
• [5] De Miranda JR, Bailey L, Ball BV, Blanchard P, Budge GE, Chejanovsky N, et al. Standard methods for virus research in Apis mellifera. Journal Of Apicultural Research. 2013;52:1-56.
• [6] Berenyi O, Bakonyi T, Derakhshifar I, Koglberger H, Nowotny N. Occurrence of six honeybee viruses in diseased Austrian apiaries. Applied and environmental microbiology. 2006;72(4):2414-2420.
• [7] Galbraith DA, Zachary LF, Allyson MR, Axel B, Maryann F, Mary WG, et al. Investigating the Viral Ecology of Global Bee Communities with High-Throughput Metagenomics. Scientific Reports. 2018;8:1-14.
• [8] McMenamin AJ, Flenniken ML. Recently identified bee viruses and their impact on three bee pollinators. Current Opinion Insect Science. 2018;26:120–129.
• [9] Schoonvaere K, De Smet L, Smagghe G, Vierstraete A, Braeckman BP, de Graaf DC. Study of the Metatranscriptome of Eight Social and Solitary Wild Bee Species Reveals Novel Viruses and Bee Parasites. Published in Front. Microbiol. Biology, Medicine Frontiers in Microbiology. 2018;9:1-12.
• [10] Eroglu GB. Phylogeographic Relationship of Honey Bee Dicistroviruses. Bee World. 2022;99(3):99-102.
• [11] Eroglu GB. RNA Viruses in Honey Bees. In: Erdemir F, Ayar MK, editors. Distinguished Research from Different Disciplines. Gelenbevi Scientific Research Journal Announcements; 2022. p. 133-147.
• [12] Beaurepaire A, Piot N, Doublet V, Antunez K, Campbell E, Chantawannakul P, et al. Diversity and global distribution of viruses of the western honey bee, Apis mellifera. Insects. 2020;11(4), 239.
• [13] Gülmez Y, Bursalı A, Tekin S. First 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).
• [14] Gümüşova SO, Albayrak H, Kurt M, Yazıcı Z. Prevalence of three honey bee viruses in Turkey. Veterinarski Arhiv. 2010;80:779-785.
• [15] Rüstemoğlu M, Sipahioğlu HM. Occurrence and prevalence of six honey bee viruses in Hakkari (Turkey) and their genomic divergence. Munis Entomology & Zoology. 2019;14(2):574-583.
• [16] Rüstemoğlu M, Sipahioğlu HM. Occurrence and molecular characterization of acute bee paralysis virus (ABPV) in honeybee (Apis mellifera) colonies in Hakkari province. Yuzuncu Yıl University Journal of Agricultural Science. 2016;26(2):174-182
• [17] Blazyte-Cereskiene L, Skrodenyte-Arbaciauskiene V, Radziute S, Cepulyte-Rakauskiene R, Apsegaite V, Buda V. A three-year survey of honey bee viruses in Lithuania. Journal of Apicultural Research. 2016;55(2):176-184.
• [18] Güller A, Usta M, Cakar G, Kurt Z. Molecular characterization of Deformed wing viruses identified in honeybee (Apis mellifera L.) colonies in Erzincan province of Turkey. European Journal of Science and Technology. 2021;(27):186-192.
• [19] Karapınar Z, Oguz B, Dincer E, Oztürk C. Phylogenetic analysis of black queen cell virus and deformed wing virus in honeybee colonies infected by mites in Van, Eastern Turkey. Praca oryginaina. 2018;74(7):460-465.
• [20] Mazzei M, Carrozza ML, Luisi E, Forzan M, Giusti M, Sagona S, et al. Infectivity of DWV associated to flower pollen: experimental evidence of a horizontal transmission route. PLoS one. 2014;9(11):e113448.
• [21] Forsgren E, De Miranda JR, Isaksson M, Wei S, Fries I. Deformed wing virus associated with Tropilaelaps mercedesae infesting European honey bees (Apis mellifera). Experimental and Applied Acarology. 2009;47:87-97.
• [22] Fung E, Hill K, Hogendoorn K, Hingston AB, Glatz RV. Co-occurrence of RNA viruses in Tasmanian-introduced bumble bees (Bombus terrestris) and honey bees (Apis mellifera). Apidologie. 2018;49:243-251.
• [23] Ravoet J, De Smet L, Meeus I, Smagghe G, Wenseleers T, de Graaf DC. Widespread occurrence of honey bee pathogens in solitary bees. Journal of Invertebrate Pathology. 2014;122:55-58.
• [24] Mazzei M, Cilia G, Forzan M, Lavazza A, Mutinelli F, Felicioli A. Detection of replicative Kashmir bee virus and Black queen cell virus in Asian hornet Vespa velutina (Lepelieter 1836) in Italy. Scientific Reports. 2019;9(1):10091.
• [25] Abou Kubaa R, Molinatto G, Khaled B, Daher-Hjaij N, Heinoun K, Saponari M. 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. Insectol. 2018;71:217-224.
• [26] Traiyasut P, Mookhploy W, Kimura K, Yoshiyama M, Khongphinitbunjong K, Chantawannakul P. First detection of honey bee viruses in wax moth. Chiang Mai J. Sci. 2016;43(4).
• [27] Yang SA, Gayral P, Zhao H, Wu Y, Jiang X, Wu Y, et al. Occurrence and molecular phylogeny of honey bee viruses in Vespids. Viruses. 2019;12(1):6.
• [28] Murray EA, Burand J, Trikoz N, Schnabel J, Grab H, Danforth BN. Viral transmission in honey bees and native bees, supported by a global black queen cell virus phylogeny. Environmental microbiology. 2019;21(3):972-983.
• [29] Avcı O, Oz ME, Dogan M. Silent threat in honey bee colonies: infection dynamics and molecular epidemiological assessment of black queen cell virus in Turkey. Archives of Virology. 2022;167(7):1499-1508.
• [30] Güller A, Kurt Z. Occurrence and Molecular Phylogeny of Economically Relevant Viruses Infecting Honey Bees (L.) of Bingöl Province, Turkey. Journal of Apicultural Science. 2022;66(1):85-96.
• [31] Anderson DL. Pathogens and queen bees. Aust. Beekeeper. 1993;94:292–296.
• [32] Tentcheva D, Gauthier L, Zappulla N, Dainat B, Cousserans F, Colin ME, et al. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Applied and Environmental Microbiology. 2004;70(12):7185-7191.
• [33] Bailey L, Ball BV. Cultivation and Purification of Bee Viruses. In: Honey Bee Pathology; 1991.
• [34] Allen M, Ball B. The incidence and world distribution of honey bee viruses. Bee World. 1996;77(3):141-162.
• [35] Antunez K, Anido M, Garrido-Bailon E, Botias C, Zunino P, Martinez Salvador A, et al. Low prevalence of honeybee viruses in Spain during 2006 and 2007. Research in Veterinary Science. 2012;93(3):1441-1445.
• [36] Genersch E, Yue C, Fries I, De Miranda JR. Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. Journal of Invertebrate Pathology. 2006; 91(1):61-63.
• [37] Li J, Peng W, Wu J, Strange JP, Boncristiani H, Chen Y. CrossSpecies Infection of Deformed Wing Virus Poses a New Threat to Pollinator Conservation. Journal of Economic Entomology. 2011;104(3):732-739.
• [38] Peng W, Li J, Boncristiani H, Strange JP, Hamilton M, Chen Y. Host range expansion of honey bee Black Queen Cell Virus in the bumble bee, Bombus huntii. Apidologie. 2011;42, 650-658.
• [39] Choe SE, Nguyen LTK, Noh JH, Koh HB, Jean YH, Kweon CH, Kang SW. Prevalence and distribution of six bee viruses in Korean Apis cerana populations. Journal of Invertebrate Pathology. 2012; 109(3):330-333.
• [40] Wang M, Bi J, Wang L, Zhou D, Ma X, Li W, ... He S. Prevalence of four common bee RNA viruses in Eastern bee populations in Yunnan Province, China. Journal of Veterinary Science and Technology. 2016; 7(1).
• [41] Ghorani M, Madadgar O, Langeroudi AG, Rezapanah M, Nabian S, Akbarein H. et al. The first comprehensive molecular detection of six honey bee viruses in Iran in 2015-2016. Archives of Virology. 2017; 162:2287-2291.
• [42] Truong AT, Yoo MS, Seo SK, Hwang TJ, Yoon SS, Cho YS. Prevalence of honey bee pathogens and parasites in South Korea: A five-year surveillance study from 2017 to 2021. Heliyon. 2023; 9(2).
• [43] 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. Journal of Apicultural Research. 2009;48(3):204-208.
• [44] Muz D, Muz MN. A molecular epidemiological study of black queen cell virus in honeybees (Apis mellifera) of Turkey: the first genetic characterization and phylogenetic analysis of field viruses. Apidologie. 2018;49(1):89-100.
• [45] Oğuz B, Karapınar Z, Dinçer E, Değer MS. Molecular detection of Nosema spp. and black queen-cell virusin honeybees in Van Province, Turkey. Turkish Journal of Veterinary & Animal Sciences. 2017;41(2):221-227.
• [46] Kalaycı G, Çağırgan AA, Pekmez K, Özkan B, Kaplan M. Molecular detection and phylogenetic analysis of the honeybee (Apis mellifera) sacbrood virus in Turkey. Turkish Journal of Veterinary & Animal Sciences. 2019; 43(4):551-554.
• [47] Çağırgan AA, Yıldırım Y, Usta A. Phylogenetic analysis of deformed wing virus, black queen cell virus and acute bee paralysis viruses in Turkish honeybee colonies. Medycyna Weterynaryjna. 2020;76(08).
• [48] Kalaycı G, Cağırgan AA, Kaplan M, Pekmez K, Beyazıt A, Özkan B, ... Arslan F. The role of viral and parasitic pathogens affected by colony losses in Turkish apiaries. Kafkas Üniversitesi Veteriner Fakültesi Dergisi. 2020;26(5).
• [49] Aydın S. Detection and of molecular characterizatıon of bee viruses in Malatya and Elazıg provinces (Master thesis). Malatya Turgut Özal University Institute of Graduate Studies Department of Plant Protection; 2020.
• [50] Utkan NG, Eroğlu GB. Molecular identıfıcatıon of microbıal pathogens in honey bees from Amasya. Uludag Bee Journal. 2023;23 (1).
• [51] Eroğlu GB. Detection of honey bee viruses in Vespula germanica: Black queen cell virus and Kashmir bee virus. Biologia 2023;1-5.
• [52] Anderson DL. Pests and pathogens of the honeybee (Apis mellifera L.) in Fiji. Journal of Apicultural Research. 1990; 29(1):53-59.
• [53] 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. Journal of invertebrate pathology. 2004; 87(2-3):84-93.