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The investigation of Culicoides (Diptera: Ceratopogonidae) species and Bluetongue virus and Schmallenberg virus in Northwest Türkiye

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Abstract

Culicoides biting midges (Diptera: Ceratopogonidae) act as mechanical and biological vectors of arboviruses and are crucial in the global spread of these viruses. This study investigated the diversity of distribution of Culicoides species and the presence of Bluetongue virus (BTV) and Schmallenberg virus (SBV) in Tekirdağ province in Northwest Türkiye. The fourteen Culicoides species, such as Culicoides newsteadi, Culicoides schultzei, Culicoides nubeculosus comp., Culicoides punctatus, Culicoides circumscriptus, Culicoides obsoletus comp., Culicoides gejgelensis, Culicoides festivipennis, Culicoides longipennis, Culicoides spp., Culicoides pulicaris, Culicoides picturatus, Culicoides odiatus, Culicoides kurensis, and Culicoides flavipulicaris, were detected. Culicoides newsteadi, C. odiatus, and C. pulicaris were the most abundant species. Phylogenetic analyses of Culicoides species’ ITS-1 gene region were performed. A pool of C. festivipennis was positive for SBV RNA, while the BTV genomic materials was not found in the qPCR analysis. This is the first report of the presence/detection of SBV in Culicoides species in Türkiye. The survey of bioecological and epizootiological aspects of vector species is essential in implementing effective control measures for arboviral infections.

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References

  • Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J. 1990. Basic local alignment search tool. Journal of Molecular Biology 215:403-410.

    Article  CAS  Google Scholar 

  • Azkur, A.K., Albayrak, H., Rişvanlı, A., Pestil, Z., Ozan, E., Yılmaz, O., Tonbak, S., Cavunt, A., Kadı, H., Macun, H.C., Acar, D., Özenç, E., Alpaslan, S., Bulut, H., 2013. Antibodies to Schmallenberg virus in domestic livestock in Türkiye, Tropical Animal Health Production https://doi.org/10.1007/s11250-013-0415-2.

  • Balenghien, T., Pagesc, N., Goffredod, M., Carpentere, S., Augotf, D., Jacquiera, E., Talaverac, S., Monacod, F., Depaquitf, J., Grilleta, C., Pujolsc, J., Sattag, G., Kasbarif, M., Setier-Rioh, M.L., Izzod, F., Alkani, C., Delecollek, J.C., Quagliad, M., Charreli, R., Polcid, A., Breardl, E., Federicid, V., Cetre-Sossaha, C., Garros, C. 2014. The emergence of Schmallenberg virus across Culicoides communities and ecosystems in Europe. Preventive Veterinary Medicine, https://doi.org/10.1016/j.prevetmed.2014.03.007

  • Bobeva, A., Zehtindjiev, P., Bensch, S., Radrova, J. 2013. A survey of biting midges of the genus Culicoides Latreille, 1809 (Diptera: Ceratopogonidae) in NE Bulgaria, with respect to transmission of avian haemosporidians. Acta Parasitologica, 58:585–91. https://doi.org/10.2478/s11686-013-0185-z

    Article  Google Scholar 

  • Bobeva, A., Zehtindjiev, P., Ilieva, M., Dimitrov, D., Mathis, A., Bensch, S., 2015. Host preferences of ornithophilic biting midges of the genus Culicoides in the Eastern Balkans. Medical and Veterinary Entomology, 29(3): 290-296. https://doi.org/10.1111/mve.12108

    Article  CAS  Google Scholar 

  • Bosnic, S., Beck, R., Listes, E., Lojkic, I., Savini, G., Roic, B., 2015. Bluetongue virus in Oryx antelope (Oryx leucoryx) during the quarantine period in 2010 in Croatia. Veterinaria Italiana, 51:139–143. https://doi.org/10.12834/VetIt.385.1795.2

  • Carpenter, S., Groschup, M.H., Garros, C., Felippe-Bauer, M.L., Purse, B.V. 2013. Culicoides biting midges, arboviruses and public health in Europe. Antiviral Research, 100(1):102-13. https://doi.org/10.1016/j.antiviral

  • Carlson, C.J., Albery, G.F., Merow, C., Trisos, C.H., Zipfel, C.M., Eskew, E.A., Olival, K.J., Ross, N., Bansal, S. 2022. Climate change increases cross-species viral transmission risk. Nature, 607, 555–562. https://doi.org/10.1038/s41586-022-04788-w

    Article  CAS  Google Scholar 

  • Centre-Sossah, C., Baldet, T., Delecolle, J.C., Mathieu, B., Perin, A., Grillet, C., Albina, E. 2004. Molecular detection of Culicoides spp. and Culicoides imicola, the principal vector of bluetongue (BT) and African horse sickness (AHS) in Africa and Europe. Veterinary Research, 35: 325–37. https://doi.org/10.1051/vetres:2004015

    Article  CAS  Google Scholar 

  • Chiang, C.L., Reeves, W.C. 1962. Statistical estimation of virus infection rates in mosquito vector populations. American Journal of Hygiene, 75, 377-391.

    CAS  Google Scholar 

  • Dağalp, S.B., Dik, B., Doğan, F., Farzani, T.A., Ataseven, V.S., Kırmızı, G.A., Şahinkesen, İ., Özkul, A. 2021. Akabane virus infection in Eastern Mediterranean Region in Türkiye: Culicoides (Diptera: Ceratopogonidae) as possible vector. Tropical Animal Health and Production 53: 231. https://doi.org/10.1007/s11250-021-02661-y

    Article  Google Scholar 

  • Deniz, A., Öncel, T., Patakakis, A.J. 2010. Trakya bölgesi’nde (Türkiye) Culicoides Latreille, 1809 (Diptera: Ceratopogonidae) tür kompozisyonu. Kafkas University Veterinary Faculty Journal, 16: 1057-1060

    Google Scholar 

  • De Regge, N., Deblauwe, I., De Deken, R., Vantieghem, P., Madder, M., Gey-sen, D., Smeets, F., Losson, B., van den Berg, T., Cay, A.B. 2012. Detection of Schmallenberg virus in different Culicoides spp. by real-time RT-PCR. Transboundary Emerging Diseases, 59, 471–475. https://doi.org/10.1111/tbed.12000

    Article  CAS  Google Scholar 

  • Dik, B., Yagcı, Ş., Linton, Y.M. 2006. A review of species diversity and distribution of Culicoides Latreille, 1809 (Diptera: Ceratopogonidae) in Türkiye. Journal of Natural History, 40 (32–34): 1947–67. https://doi.org/10.1080/00222930601046634

  • Dik, B., Yavru, S., Uslu, U., Yapıcı, O., Esin, E. 2012. Determination of Culicoides species (Diptera: Ceratopogonidae) and suspect vectors of Epizootic Haemorrhagic Disease virus and Bluetongue virus in Culicoides specimens by RT-PCR in southern and western Anatolia. Revue de Medecine Veteterinaire, 163 (11): 505-510.

    Google Scholar 

  • Dik, B., Muz, D., Uslu, U., Muz, M. 2014. The Geographical Distribution and First Molecular Analysis of Culicoides Latreille (Diptera: Ceratopogonidae) species in Southern and South-Eastern Türkiye during 2012 Outbreak of Bovine Ephemeral Fever. Parasitologia Research, 113: 4225–4232. https://doi.org/10.1007/s00436-014-4098-z

    Article  CAS  Google Scholar 

  • Doceul, V., Lara, E., Sailleau, C., Belbis, G., Richardson, J., Bréard, E., Viarouge, C., Dominguez, M., Hendrikx, P., Calavas, D., Desprat, A., Languille, J., Comtet, L., Pourquier, P., Eléouët, J.F., Delmas, B., Marianneau, P., Vitour, D., Zientara, S. 2013. Epidemiology, molecular virology and diagnostics of Schmallenberg virus, an emerging orthobunyavirus in Europe. Veterinary Research, 15;44(1):31. https://doi.org/10.1186/1297-9716-44-31.

  • Doğan, F., Dik, B., Dağalp, S.B., Farzani, T.A., Ataseven, V.S., Acar, G., Şahinkesen, İ., Özkul, A. 2022. Prevalance of Schmallenberg orthobunyavirus (SBV) infection in sampled ruminants in Türkiye’s Eastern Mediterranean region between 2015 and 2017. Research in Veterinary Science 145: 63-70. https://doi.org/10.1016/j.rvsc.2022.02.013

    Article  CAS  Google Scholar 

  • Elbers, A.R., Meiswinkel, R., van Weezep, E., van Oldruitenborgh- Oosterbaan, M.M., Kooi, E.A. 2013. Schmallenberg virus in Culicoides spp. biting midges, the Netherlands, 2011. Emerging Infection Diseases, 19(1): 106–109. https://doi.org/10.3201/eid1901.121054

  • Elmas, A., Aslan, Ö., Şahna, K.C. 2018. Sivas Yöresindeki Koyunlarda Schmallenberg Virus Enfeksiyonunun Seroprevalansının Belirlenmesi. Harran Üniversity Veterinary Faculty Journal, 7(1): 56-59

    Google Scholar 

  • Ertürk, A., Tatar, N., Kabakli, O., Incoglu, S., Cizmeci, S., Barut, F. 2004. The Current Situation Of Bluetongue in Türkiye. Veterinaria Italiana, 40 (3): 137–40

    Google Scholar 

  • Goffredo, M., Monaco, F., Capelli, G., Quaglia, M., Federici, V., Catalani, M., Montarsi, F., Polci, A., Pinoni, C., Calistri, P., Savini, G. 2013. Schmallenberg virus in Italy: a retrospective survey in Culicoides stored during the bluetongue Italian surveillance program. Preventive Veterinary Medicine, 111, 230–236. https://doi.org/10.1016/j.prevetmed.2013.05.014

    Article  CAS  Google Scholar 

  • Gomulski, L.M., Meiswinkel, R,, Delécolle, J.C., Goffredo, M., Gasperi, G. 2005. Phylogenetic relationships of the subgenus Avaritia Fox, 1955 including Culicoides obsoletus (Diptera: Ceratopogonidae) in Italy based on internal transcribed spacer 2 ribosomal DNA sequences. Systemic Entomology, 30:619–31. https://doi.org/10.1111/j.1365-3113.2005.00286.x

  • Hall, T.A. 1999. BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

  • Hoffmann, B., Scheuch, M., Höper, D., Jungblut, R., Holsteg, M., Schirrmeier, H., Eschbaumer, M., Goller, K.V., Wernike, K., Fischer, M., Breithaupt, A., Mettenleiter, T.C., Beer, M. 2012. Novel orthobunyavirus in Cattle, Europe. Emerging Infection Diseases. https://doi.org/10.3201/eid1803.111905

  • Kęsik-Maliszewska, J., Larska, M., Collins, Á.B., Rola, J. 2019. Post-Epidemic Distribution of Schmallenberg Virus in Culicoides Arbovirus Vectors in Poland. Viruses,11:447. https://doi.org/10.3390/v11050447

    Article  CAS  Google Scholar 

  • Kluiters, G., Swales, H., Baylis, M. 2015. Local dispersal of palaearctic Culicoides biting midges estimated by mark-release-recapture. Parasite and Vector 8: 86. 10.1186/s13071-015-0658-z

  • Korkmaz, C., Alten, B., Erol, U., Deniz, A. 2021. Updated checklist of Culicoides Latreille (Diptera: Ceratopogonidae) of Turkey with ten new records. J Vector Ecology, 46(2):124–136. https://doi.org/10.52707/1081-1710-46.2.124.

  • Kumar S, Stecher G, Li M, Knyaz C,Tamura K 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35:1547-1549

    Article  CAS  Google Scholar 

  • Larska, M., Lechowski, L., Grochowska, M., Zmudzinski, J.F. 2013. Detection of the Schmallenberg virus in nulliparous Culicoides obsoletus/scoticus complex and C. punctatus—the possibility of transovarial virus transmission in the midge population and of a new vector. Veterinary Microbiology, 166: 467–473. https://doi.org/10.1016/j.vetmic.2013.07.015

    Article  Google Scholar 

  • Macun, H.C., Azkur, A.K., Kalender, H., Erat, S. 2017. Kırıkkale'de yetiştirilen koyunlarda Schmallenberg virüs seroprevalansı ve bazı coğrafi özelliklerle ilişkisi. Ankara University Veterinary Faculty Journal, 64: 93-97

    Google Scholar 

  • Mathieu, B., Perrin, A., Baldet, T., Delécolle, J.C., Albina, E., Cêtre-Sossah, C. 2007. Molecular identification of Western European species of obsoletus complex (Diptera: Ceratopogonidae) by an internal transcribed spacer-1 rDNA multiplex polymerase chain reaction assay. Journal of Medical Entomology, 44:1019–25. https://doi.org/10.1603/0022-2585(2007)44[1019:miowes]2.0.co;2

    Article  CAS  Google Scholar 

  • Mathieu, B., Garros, C., Balenghien, T., Candolfi, E., Delecolle, J.C., Cetre-Sossah, C. 2020. A phylogenetic analysis of the biting midges belonging to Culicoides Latreille (Diptera: Ceratopogonidae) subgenus Avaritia using molecular data. Parasites and Vectors, 13:243. https://doi.org/10.1186/s13071-020-04111-4

    Article  CAS  Google Scholar 

  • Mehlhorn, H., Walldorf, V., Klimpel, S., Schaub, G., Kiel, E., Liebisch, G., Liebisch, A., Werner, D., Bauer, C., Clausen, H., Bauer, B., Geier, M., Batza, H., Conraths, F., Hoffmann, B., Beer, M. 2009. Bluetongue disease in Germany (2007–2008): monitoring of entomological aspects. Parasit Research, 105:313–319

    Article  Google Scholar 

  • Mellor, P.S., Boorman, J., Baylis, M. 2000. Culicoides Biting Midges: their role as arbovirus vectors. Annual Review Entomology, 45: 307–40. https://doi.org/10.1146/annurev.ento.45.1.307

    Article  CAS  Google Scholar 

  • Mellor, P.S., Wittmann, E.J. 2002. Bluetongue virus in the mediterranean basin 1998–2001. Veterinary Journal, 164(1): 20–37. https://doi.org/10.1053/tvjl.2002.0713

    Article  CAS  Google Scholar 

  • Mertens, P.P.C., Maan, S., Samuel, A., Attoui, H. 2004. Orbivirus, Reoviridae. In Virus Taxonomy VIIIth Report of ICTV, pp 466–483. Edited by Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA. Elsevier/Academic Press, London

  • Özkul , A., Ertürk, A., Çalışkan, E., Saraç, F., Ceylan, Ç., Mertens, P., Kabaklı, Ö., Dınçer, E., Çızmeci, Ş. 2009. Segment 10 Based Molecular Epidemiology Of Bluetongue Virus (MDV) İsolates From Türkiye:1999–2001.. Virus, https://doi.org/10.1016/J.Virusres.2009.02.007

  • Pudar, D., Petric, D., Allène, X., Alten, B., Ayhan, N., Cvetkovikj, A., Garros, C., Goletic, T., Gunay, F., Hlavackova, K., Cupina, A.I., Kavran, M., Lestinova, T., Mathieu, B., Mikov, O., Pajovic, I., Rakotoarivony, I., Stefanovska, J., Vaselek, S., Zuko, A., Balenghien, T. 2018. An update of the Culicoides (Diptera: Ceratopogonidae) checklist for the Balkans. Parasite and Vectors 11: 462. https://doi.org/10.1186/s13071-018-3051-x

    Article  Google Scholar 

  • Purse, B.V., Carpenter, S., Venter, G.J., Bellis, G. & Mullens, B.A. 2015. Bionomics of temperate and tropical Culicoides midges: Knowledge gaps and consequences for transmission of Culicoides-borne viruses. Annual Review of Entomology, 60, 373-392. https://doi.org/10.1146/annurev-ento-010814-020614

    Article  CAS  Google Scholar 

  • Rasmussen, L.D., Kristensen, B., Kirkeby, C., Rasmussen, T.B., Belsham, G.J., Bodker, R., Botner, A. 2012. Culicoides as vectors of Schmallenberg virus. Emerging Infection Diseases, 18: 1204–1206. https://doi.org/10.3201/eid1807.120385

    Article  CAS  Google Scholar 

  • Roy, P. 2017. Bluetongue virus structure and assembly. Current Opinion In Virology, 24, 115–123.

    Article  CAS  Google Scholar 

  • Sarvasova, A., Kocišová, A., Halán, M., Delécolle, J.C., Mathieu, B. 2014. Morphological and molecular analysis of the genus Culicoides (Diptera: Ceratopogonidae) in Slovakia with five new records. Zootaxa, 3872: 541–560. https://doi.org/10.11646/zootaxa.3872.5.6

  • Schwenkenbecher, J.M., Mordue, A.J., Piertney, S.B. 2009. Phylogenetic analysis indicates that Culicoides dewulfi should not be considered part of the Culicoides obsoletus complex. Bulletin Entomological Research, 99:371–5. 10.1017/S0007485308006391

  • Segard, A., Gardes, L., Jacquier, E., Grillet, C., Mathieu, B., Rakotoarivony, I., Setier-Rio ML, Chavernac D, Cêtre-Sossah C, Balenghien T, Garros C. 2018. Schmallenberg virus in Culicoides Latreille (Diptera: Ceratopogonidae) populations in France during 2011-2012 outbreak. Transbound Emerg Disease, 65(1):e94–e103. https://doi.org/10.1111/tbed.12686

    Article  CAS  Google Scholar 

  • Tonbak, Ş., Azkur, A.K., Pestil, Z., Bıyıklı, E., Abaylı, H., Baydar, E., van der Poel Wim, H.M., Bulut, H. 2016. "Circulation of Schmallenberg virus in Turkey, 2013," Turkish Journal of Veterinary and Animal Sciences, 40:(2) 8. https://doi.org/10.3906/vet-1507-3

  • Turgut, F., Kılıç, A.Y. 2015. The Ceratopogonidae (Insecta: Diptera) fauna of the Central Black Sea Region in Türkiye Turkish Journal Zoology, 39: 1071–1089. https://doi.org/10.3906/zoo-1410-33

  • Turunçoğlu, U.U., Türkeş, M., Bozkurt, D., Önol, B., Şen, Ö.L., Dalfes, H.N. 2018. Climates In: S. Kapur, E. Akça, and H. Günal (eds.), the Soils of Turkey. Springer ISBN 978–3–319–64392–2. pp. 25–44

  • Venter, G.J. 2016. Culicoides spp. (Diptera: Ceratopogonidae) as vectors of bluetongue virus in South Africa - a review. Veterinaria Italiana, 51(4), 325–333. https://doi.org/10.12834/VetIt.505.2436.2

  • Veronesi, E., Henstock, M., Gubbins, S., Batten, C., Manley, R., Barber, J., Hoffmann, B., Beer, M., Attoui, H., Mertens, P.P., Carpenter, S. 2013. Implicating Culicoides biting midges as vectors of schmallenberg virus using semi-quantitative rt-PCR. PLoS ONE, 8: e57747. https://doi.org/10.1371/journal.pone.0057747

  • Walter, S.D., Hildreth, S.W., Beaty B.J. 1980. Estimation of infection rates in populations of organisms using pools of variable size. American Journal Epidemiology, 112, 124-128.

    Article  CAS  Google Scholar 

  • Yavru, S., Dik, B., Bulut, O., Uslu, U., Yapıcı, O., Kale, M., Avcı, O. 2018. New Culicoides vector species for BTV transmission in Central and Central West of Anatolia. Annual Research and Review in Biology, 27 (1): 1-9. 10.9734/ARRB/2018/42170

  • Yılmaz, H., Hoffmann, B., Turan, N., Cizmecigil, U.Y., Richt, J.A., van der Poel, W.H. 2014. Detection and partial sequencing of Schmallenberg virus in cattle and sheep in Türkiye. Vector Borne Zoonotic Diseases, https://doi.org/10.1089/vbz.2013.1451

  • Yıldırım, A., Dik, B., Düzlü, Ö., Onder, Z., Çiloglu, A., Yetişmiş, G., İnci, A. 2019. Genetic diversity of Culicoides species within the Pulicaris complex (Diptera: Ceratopogonidae) in Türkiye inferred from mitochondrial COI gene sequences. Acta tropica, 190: 380-388. https://doi.org/10.1016/j.actatropica.2018.12.005

    Article  Google Scholar 

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Funding

The project was financially supported by Namik Kemal University Scientific Research Projects Coordination Unit (NKUBAP) with the project no. NKUBAP.00.23.AR.14.08.

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  1. Department of Virology, Faculty of Veterinary Medicine, Tekirdag Namık Kemal University, Tekirdağ, Türkiye

    Dilek Muz

  2. Department of Parasitology, Faculty of Veterinary Medicine, Selçuk University, Konya, Türkiye

    Bilal Dik

  3. Department of Parasitology, Faculty of Veterinary Medicine, Tekirdag Namık Kemal University, Tekirdağ, Türkiye

    Mustafa Necati Muz

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All authors contributed to the study’s conception. Dilek Muz and Mustafa Necati Muz designed this study; Dilek Muz, Bilal Dik, and Mustafa Necati Muz participated in the sample collection; Bilal Dik and Mustafa Necati Muz identified the Culicoides species; Dilek Muz and Mustafa Necati Muz carried out the molecular work, analyzed and interpreted the data, and wrote the main manuscript text; and all authors reviewed and edited the manuscript.

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Muz, D., Dik, B. & Muz, M.N. The investigation of Culicoides (Diptera: Ceratopogonidae) species and Bluetongue virus and Schmallenberg virus in Northwest Türkiye. Trop Anim Health Prod 55, 39 (2023). https://doi.org/10.1007/s11250-023-03454-1

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