Research Article
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Year 2024, Volume: 9 Issue: 1, 254 - 260, 12.06.2024

Abstract

References

  • Amiri, E., Meixner, M., Nielsen, S. L., & Kryger, P. (2015). Four categories of viral infection describe the health status of honey bee colonies. PLoS ONE, 10(10), 10–12. https://doi.org/10.1371/journal.pone.0140272
  • Antúnez, K., D’Alessandro, B., Corbella, E., Ramallo, G., & Zunino, P. (2006). Honeybee viruses in Uruguay. Journal of Invertebrate Pathology, 93(1), 67–70. https://doi.org/10.1016/j.jip.2006.05.009
  • Benjeddou, M., Leat, N., Allsopp, M., & Davison, S. (2001). Detection of Acute Bee Paralysis Virus and Black Queen Cell Virus from Honeybees by Reverse Transcriptase PCR. Applied and Environmental Microbiology,67(5), 2384–2387. https://doi.org/10.1128/AEM.67.5.2384-2387.2001
  • Berényi, O., Bakonyi, T., Derakhshifar, I., Köglberger, H., & Nowotny, N. (2006). Occurrence of six honeybee viruses in diseased Austrian apiaries. Applied and Environmental Microbiology, 72(4), 2414–2420. https://doi.org/10.1128/AEM.72.4.2414-2420.2006
  • Çağirgan, A. A., & Yazici, Z. (2021). The prevalence of seven crucial honeybee viruses using multiplex RT-PCR and their phylogenetic analysis. Turkish Journal of Veterinary and Animal Sciences, 45(1), 44–55. https://doi.org/10.3906/VET-2004-139
  • Cagirgan, A. A., Yildirim, Y., & Usta, A. (2020). Phylogenetic analysis of deformed wing virus, black queen cell virus and acute bee paralysis viruses in Turkish honeybee colonies. Medycyna Weterynaryjna, 76(8), 480–484. https://doi.org/10.21521/mw.6437
  • Chen, Y., Pettis, J. S., & Feldlaufer, M. F. (2005). Detection of multiple viruses in queens of the honey bee Apis mellifera L. Journal of Invertebrate Pathology, 90(2), 118–121. https://doi.org/10.1016/j.jip.2005.08.005
  • de Miranda, J. R., & Fries, I. (2008). Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). Journal of Invertebrate Pathology, 98(2), 184–189. https://doi.org/10.1016/j.jip.2008.02.004
  • Fanelli, A., & Tizzani, P. (2020). Spatial and temporal analysis of varroosis from 2005 to 2018. Research in Veterinary Science, 131(January), 215–221. https://doi.org/10.1016/j.rvsc.2020.04.017
  • Forgách, P., Bakonyi, T., Tapaszti, Z., Nowotny, N., & Rusvai, M. (2008). Prevalence of pathogenic bee viruses in Hungarian apiaries: Situation before joining the European Union. Journal of Invertebrate Pathology, 98(2), 235–238. https://doi.org/10.1016/j.jip.2007.11.002
  • Francis, R. M., Nielsen, S. L., & Kryger, P. (2013). Varroa-Virus Interaction in Collapsing Honey Bee Colonies. PLoS ONE, 8(3). https://doi.org/10.1371/journal.pone.0057540
  • Gela, A., Atickem, A., Bezabeh, A., Woldehawariat, Y., & Gebresilassie, A. (2023). Insights into varroa mite (Varroa destructor) infestation levels in local honeybee (Apis mellifera) colonies of Ethiopia. Journal of Applied Entomology, 147(9), 798–808. https://doi.org/10.1111/jen.13171
  • Gülmez, Y., Bursali, A., & Tekin, Ş. (2009). 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, 8(16), 3698–3702.
  • Gumusova, S. O., Albayrak, H., Kurt, M., & Yazici, Z. (2010). Prevalence of three honey bee viruses in Turkey. Veterinarski Arhiv, 80(6), 779–785.
  • Hua, T., Chantawannakul, P., Tsai, C. L., & Yeh, W. Bin. (2023). Genetic Profile of the Parasitic Varroan Mite Varroa destructor (Arachnida: Mesostigmata: Varroidae) in Taiwan: a New Taiwanese Haplotype Intermediate Between the Highly Virulent Russian and Less Virulent Japanese Types Identified in the Honey Bee Host Ap. Zoological Studies, 62, 1–12. https://doi.org/10.6620/ZS.2023.62-11
  • ICTV. (2022). International Commitee on Taxonomy of Viruses. Available at https://ictv.global/taxonomy/. Date of Access: 24.04.2024
  • Kalayci, G., Cagirgan, A. A., Kaplan, M., Pekmez, K., Beyazit, A., Ozkan, B., Yesiloz, H., & Arslan, F. (2020). The role of viral and parasitic pathogens affected by colony losses in Turkish apiaries. Kafkas Universitesi Veteriner Fakultesi Dergisi, 26(5), 671–677. https://doi.org/10.9775/kvfd.2020.24154
  • Karapinar, Z., Oǧuz, B., Dinçer, E., & Öztürk, C. (2018). Phylogenetic analysis of black queen cell virus and deformed wing virus in honeybee colonies infected by mites in Van, Eastern Turkey. Medycyna Weterynaryjna, 74(7), 460–465. https://doi.org/10.21521/mw.5990
  • Khalifa, S. A. M., Elshafiey, E. H., Shetaia, A. A., El-Wahed, A. A. A., Algethami, A. F., Musharraf, S. G., Alajmi, M. F., Zhao, C., Masry, S. H. D., Abdel-Daim, M. M., Halabi, M. F., Kai, G., Al Naggar, Y., Bishr, M., Diab, M. A. M., & El-Seedi, H. R. (2021). Overview of bee pollination and its economic value for crop production. Insects, 12(8), 1–23. https://doi.org/10.3390/insects12080688
  • Lanzi, G., de Miranda, J. R., Boniotti, M. B., Cameron, C. E., Lavazza, A., Capucci, L., Camazine, S. M., & Rossi, C. (2006). Molecular and Biological Characterization of Deformed Wing Virus of Honeybees (Apis mellifera L.) . Journal of Virology, 80(10), 4998–5009. https://doi.org/10.1128/jvi.80.10.4998-5009.2006
  • Leat, N., Ball, B., Govan, V., & Davison, S. (2000). Analysis of the complete genome sequence of black queen-cell virus, a picorna-like virus of honey bees. Journal of General Virology, 81(8), 2111–2119. https://doi.org/10.1099/0022-1317-81-8-2111
  • Li, Z., Chen, Y., Zhang, S., Chen, S., Li, W., Yan, L., Shi, L., Wu, L., Sohr, A., & Su, S. (2013). Viral Infection Affects Sucrose Responsiveness and Homing Ability of Forager Honey Bees, Apis mellifera L. PLoS ONE, 8(10), 1–10. https://doi.org/10.1371/journal.pone.0077354
  • 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. https://doi.org/10.3896/IBRA.1.48.3.09
  • Nazzi, F., & Pennacchio, F. (2018). Honey bee antiviral immune barriers as affected by multiple stress factors: A novel paradigm to interpret colony health decline and collapse. Viruses, 10(4). https://doi.org/10.3390/v10040159
  • Oguz, B., Karapinar, Z., Dinçer, E., & Deĝer, 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(2), 221–227. https://doi.org/10.3906/vet-1604-92
  • Roberts, J. M. K., Anderson, D. L., & Durr, P. A. (2017). Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Scientific Reports, 7, 6925. https://doi.org/10.1038/s41598-017-07290-w
  • Rodríguez, M., Vargas, M., Gerding, M., Navarro, H., & Antúnez, K. (2012). Viral infection and Nosema ceranae in honey bees (Apis mellifera ) in Chile Viral infection and Nosema ceranae in honey bees (Apis mellifera) in Chile. Journal of apicultural research, 51, 285-287. https://doi.org/10.3896/IBRA.1.51.3.12
  • Shojaei, A., Nourian, A., Khanjani, M., & Mahmoodi, P. (2023). The first molecular characterization of Lake Sinai virus in honey bees (Apis mellifera) and Varroa destructor mites in Iran. Journal of Apicultural Research, 62(5), 1176–1182. https://doi.org/10.1080/00218839.2021.1921467
  • Smeele, Z. E., Baty, J. W., & Lester, P. J. (2023). Effects of Deformed Wing Virus-Targeting dsRNA on Viral Loads in Bees Parasitised and Non-Parasitised by Varroa destructor. Viruses, 15(11). https://doi.org/10.3390/v15112259
  • Tang, J., Ji, C., Shi, W., Su, S., Xue, Y., Xu, J., Chen, X., Zhao, Y., & Chen, C. (2023). Survey Results of Honey Bee Colony Losses in Winter in China (2009–2021). Insects, 14(6), 1–18. https://doi.org/10.3390/insects14060554
  • Tentcheva, D., Gauthier, L., Zappulla, N., Dainat, B., Cousserans, F., Colin, M. E., & Bergoin, M. (2004). Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Applied and Environmental Microbiology, 70(12), 7185–7191. https://doi.org/10.1128/AEM.70.12.7185-7191.2004
  • Tlak Gajger, I., Kolodziejek, J., Bakonyi, T., & Nowotny, N. (2014). Prevalence and distribution patterns of seven different honeybee viruses in diseased colonies: a case study from Croatia. Apidologie, 45(6), 701–706. https://doi.org/10.1007/s13592-014-0287-0
  • Usta, A., & Yildirim, 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 Universitesi Veteriner Fakultesi Dergisi, 69(3), 303–311. https://doi.org/10.33988/auvfd.824882
  • Usta, A., & Yıldırım, Y. (2020). Bal Arılarının Viral Hastalıkları. Cukurova University, Agriculture Faculty, 1(35), 57–66. https://doi.org/10.36846/cjafs.2020.18
  • Woodford, L., Sharpe, G., Highet, F., & Evans, D. J. (2023). All together now: Geographically coordinated miticide treatment benefits honey bee health. Journal of Applied Ecology, 60(5), 790–802. https://doi.org/10.1111/1365-2664.14367

Molecular detection of deformed wing virus, black queen cell virus in honey bees in balıkesir province

Year 2024, Volume: 9 Issue: 1, 254 - 260, 12.06.2024

Abstract

Viral infections are among the risk factors affecting the health of honey bees, which are economically and ecologically important insects. These infections cause large-scale colony losses. The primary threat to the well-being of western honey bees (Apis mellifera) is the ectoparasitic mite Varroa destructor, mainly because of its role as a transmitter of viruses. This study aimed to investigate the presence of deformed wing virus (DWV) and black queen cell virus (BQCV) infections, which cause significant colony losses in honey bees, using the reverse transcriptase polymerase chain reaction (RT-PCR) method. For this purpose, adult bees were taken from 50 hives by random sampling in three different regions of Balıkesir. As a result of the analysis of the samples, the genome positivity of DWV and BQCV infections was determined to be 86% (43/50) and 24% (12/50), respectively. In the study’s bee colonies, multiple infections with both viruses were found at a rate of 18% (9/50). The results obtained revealed that Varroa was not effectively controlled in the colonies, especially in the last month of spring, and accordingly, that viral diseases may occur due to Varroa infestation in the winter months.

Ethical Statement

It has been reported that the Approval of the Local Ethics Committee for Animal Experiments is not required for the study, in accordance with the provisions of Article 4.1 (d) of the ‘Regulation on Working Procedures and Principles of Animal Committees’ published in the Official Gazette No. 28914 on 15.02.2014.

References

  • Amiri, E., Meixner, M., Nielsen, S. L., & Kryger, P. (2015). Four categories of viral infection describe the health status of honey bee colonies. PLoS ONE, 10(10), 10–12. https://doi.org/10.1371/journal.pone.0140272
  • Antúnez, K., D’Alessandro, B., Corbella, E., Ramallo, G., & Zunino, P. (2006). Honeybee viruses in Uruguay. Journal of Invertebrate Pathology, 93(1), 67–70. https://doi.org/10.1016/j.jip.2006.05.009
  • Benjeddou, M., Leat, N., Allsopp, M., & Davison, S. (2001). Detection of Acute Bee Paralysis Virus and Black Queen Cell Virus from Honeybees by Reverse Transcriptase PCR. Applied and Environmental Microbiology,67(5), 2384–2387. https://doi.org/10.1128/AEM.67.5.2384-2387.2001
  • Berényi, O., Bakonyi, T., Derakhshifar, I., Köglberger, H., & Nowotny, N. (2006). Occurrence of six honeybee viruses in diseased Austrian apiaries. Applied and Environmental Microbiology, 72(4), 2414–2420. https://doi.org/10.1128/AEM.72.4.2414-2420.2006
  • Çağirgan, A. A., & Yazici, Z. (2021). The prevalence of seven crucial honeybee viruses using multiplex RT-PCR and their phylogenetic analysis. Turkish Journal of Veterinary and Animal Sciences, 45(1), 44–55. https://doi.org/10.3906/VET-2004-139
  • Cagirgan, A. A., Yildirim, Y., & Usta, A. (2020). Phylogenetic analysis of deformed wing virus, black queen cell virus and acute bee paralysis viruses in Turkish honeybee colonies. Medycyna Weterynaryjna, 76(8), 480–484. https://doi.org/10.21521/mw.6437
  • Chen, Y., Pettis, J. S., & Feldlaufer, M. F. (2005). Detection of multiple viruses in queens of the honey bee Apis mellifera L. Journal of Invertebrate Pathology, 90(2), 118–121. https://doi.org/10.1016/j.jip.2005.08.005
  • de Miranda, J. R., & Fries, I. (2008). Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). Journal of Invertebrate Pathology, 98(2), 184–189. https://doi.org/10.1016/j.jip.2008.02.004
  • Fanelli, A., & Tizzani, P. (2020). Spatial and temporal analysis of varroosis from 2005 to 2018. Research in Veterinary Science, 131(January), 215–221. https://doi.org/10.1016/j.rvsc.2020.04.017
  • Forgách, P., Bakonyi, T., Tapaszti, Z., Nowotny, N., & Rusvai, M. (2008). Prevalence of pathogenic bee viruses in Hungarian apiaries: Situation before joining the European Union. Journal of Invertebrate Pathology, 98(2), 235–238. https://doi.org/10.1016/j.jip.2007.11.002
  • Francis, R. M., Nielsen, S. L., & Kryger, P. (2013). Varroa-Virus Interaction in Collapsing Honey Bee Colonies. PLoS ONE, 8(3). https://doi.org/10.1371/journal.pone.0057540
  • Gela, A., Atickem, A., Bezabeh, A., Woldehawariat, Y., & Gebresilassie, A. (2023). Insights into varroa mite (Varroa destructor) infestation levels in local honeybee (Apis mellifera) colonies of Ethiopia. Journal of Applied Entomology, 147(9), 798–808. https://doi.org/10.1111/jen.13171
  • Gülmez, Y., Bursali, A., & Tekin, Ş. (2009). 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, 8(16), 3698–3702.
  • Gumusova, S. O., Albayrak, H., Kurt, M., & Yazici, Z. (2010). Prevalence of three honey bee viruses in Turkey. Veterinarski Arhiv, 80(6), 779–785.
  • Hua, T., Chantawannakul, P., Tsai, C. L., & Yeh, W. Bin. (2023). Genetic Profile of the Parasitic Varroan Mite Varroa destructor (Arachnida: Mesostigmata: Varroidae) in Taiwan: a New Taiwanese Haplotype Intermediate Between the Highly Virulent Russian and Less Virulent Japanese Types Identified in the Honey Bee Host Ap. Zoological Studies, 62, 1–12. https://doi.org/10.6620/ZS.2023.62-11
  • ICTV. (2022). International Commitee on Taxonomy of Viruses. Available at https://ictv.global/taxonomy/. Date of Access: 24.04.2024
  • Kalayci, G., Cagirgan, A. A., Kaplan, M., Pekmez, K., Beyazit, A., Ozkan, B., Yesiloz, H., & Arslan, F. (2020). The role of viral and parasitic pathogens affected by colony losses in Turkish apiaries. Kafkas Universitesi Veteriner Fakultesi Dergisi, 26(5), 671–677. https://doi.org/10.9775/kvfd.2020.24154
  • Karapinar, Z., Oǧuz, B., Dinçer, E., & Öztürk, C. (2018). Phylogenetic analysis of black queen cell virus and deformed wing virus in honeybee colonies infected by mites in Van, Eastern Turkey. Medycyna Weterynaryjna, 74(7), 460–465. https://doi.org/10.21521/mw.5990
  • Khalifa, S. A. M., Elshafiey, E. H., Shetaia, A. A., El-Wahed, A. A. A., Algethami, A. F., Musharraf, S. G., Alajmi, M. F., Zhao, C., Masry, S. H. D., Abdel-Daim, M. M., Halabi, M. F., Kai, G., Al Naggar, Y., Bishr, M., Diab, M. A. M., & El-Seedi, H. R. (2021). Overview of bee pollination and its economic value for crop production. Insects, 12(8), 1–23. https://doi.org/10.3390/insects12080688
  • Lanzi, G., de Miranda, J. R., Boniotti, M. B., Cameron, C. E., Lavazza, A., Capucci, L., Camazine, S. M., & Rossi, C. (2006). Molecular and Biological Characterization of Deformed Wing Virus of Honeybees (Apis mellifera L.) . Journal of Virology, 80(10), 4998–5009. https://doi.org/10.1128/jvi.80.10.4998-5009.2006
  • Leat, N., Ball, B., Govan, V., & Davison, S. (2000). Analysis of the complete genome sequence of black queen-cell virus, a picorna-like virus of honey bees. Journal of General Virology, 81(8), 2111–2119. https://doi.org/10.1099/0022-1317-81-8-2111
  • Li, Z., Chen, Y., Zhang, S., Chen, S., Li, W., Yan, L., Shi, L., Wu, L., Sohr, A., & Su, S. (2013). Viral Infection Affects Sucrose Responsiveness and Homing Ability of Forager Honey Bees, Apis mellifera L. PLoS ONE, 8(10), 1–10. https://doi.org/10.1371/journal.pone.0077354
  • 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. https://doi.org/10.3896/IBRA.1.48.3.09
  • Nazzi, F., & Pennacchio, F. (2018). Honey bee antiviral immune barriers as affected by multiple stress factors: A novel paradigm to interpret colony health decline and collapse. Viruses, 10(4). https://doi.org/10.3390/v10040159
  • Oguz, B., Karapinar, Z., Dinçer, E., & Deĝer, 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(2), 221–227. https://doi.org/10.3906/vet-1604-92
  • Roberts, J. M. K., Anderson, D. L., & Durr, P. A. (2017). Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Scientific Reports, 7, 6925. https://doi.org/10.1038/s41598-017-07290-w
  • Rodríguez, M., Vargas, M., Gerding, M., Navarro, H., & Antúnez, K. (2012). Viral infection and Nosema ceranae in honey bees (Apis mellifera ) in Chile Viral infection and Nosema ceranae in honey bees (Apis mellifera) in Chile. Journal of apicultural research, 51, 285-287. https://doi.org/10.3896/IBRA.1.51.3.12
  • Shojaei, A., Nourian, A., Khanjani, M., & Mahmoodi, P. (2023). The first molecular characterization of Lake Sinai virus in honey bees (Apis mellifera) and Varroa destructor mites in Iran. Journal of Apicultural Research, 62(5), 1176–1182. https://doi.org/10.1080/00218839.2021.1921467
  • Smeele, Z. E., Baty, J. W., & Lester, P. J. (2023). Effects of Deformed Wing Virus-Targeting dsRNA on Viral Loads in Bees Parasitised and Non-Parasitised by Varroa destructor. Viruses, 15(11). https://doi.org/10.3390/v15112259
  • Tang, J., Ji, C., Shi, W., Su, S., Xue, Y., Xu, J., Chen, X., Zhao, Y., & Chen, C. (2023). Survey Results of Honey Bee Colony Losses in Winter in China (2009–2021). Insects, 14(6), 1–18. https://doi.org/10.3390/insects14060554
  • Tentcheva, D., Gauthier, L., Zappulla, N., Dainat, B., Cousserans, F., Colin, M. E., & Bergoin, M. (2004). Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Applied and Environmental Microbiology, 70(12), 7185–7191. https://doi.org/10.1128/AEM.70.12.7185-7191.2004
  • Tlak Gajger, I., Kolodziejek, J., Bakonyi, T., & Nowotny, N. (2014). Prevalence and distribution patterns of seven different honeybee viruses in diseased colonies: a case study from Croatia. Apidologie, 45(6), 701–706. https://doi.org/10.1007/s13592-014-0287-0
  • Usta, A., & Yildirim, 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 Universitesi Veteriner Fakultesi Dergisi, 69(3), 303–311. https://doi.org/10.33988/auvfd.824882
  • Usta, A., & Yıldırım, Y. (2020). Bal Arılarının Viral Hastalıkları. Cukurova University, Agriculture Faculty, 1(35), 57–66. https://doi.org/10.36846/cjafs.2020.18
  • Woodford, L., Sharpe, G., Highet, F., & Evans, D. J. (2023). All together now: Geographically coordinated miticide treatment benefits honey bee health. Journal of Applied Ecology, 60(5), 790–802. https://doi.org/10.1111/1365-2664.14367
There are 35 citations in total.

Details

Primary Language English
Subjects Veterinary Parasitology, Veterinary Virology
Journal Section Research Articles
Authors

Zeynep Karapınar 0000-0002-2743-8948

Mehmet Özüiçli 0000-0003-3415-2582

Publication Date June 12, 2024
Submission Date February 29, 2024
Acceptance Date April 22, 2024
Published in Issue Year 2024 Volume: 9 Issue: 1

Cite

APA Karapınar, Z., & Özüiçli, M. (2024). Molecular detection of deformed wing virus, black queen cell virus in honey bees in balıkesir province. Mediterranean Veterinary Journal, 9(1), 254-260.