Abstract
BackgroundCulicoides biting midges (Diptera: Ceratopogonidae) are responsible for the biological transmission of internationally important arboviruses of livestock. In 2011, a novel Orthobunyavirus was discovered in northern Europe causing congenital malformations and abortions in ruminants. From field studies, Culicoides were implicated in the transmission of this virus which was subsequently named Schmallenberg virus (SBV), but to date no assessment of susceptibility to infection of field populations under standardised laboratory conditions has been carried out. We assessed the influence of membrane type (chick skin, collagen, Parafilm M®) when offered in conjunction with an artificial blood-feeding system (Hemotek, UK) on field-collected Culicoides blood-feeding rates. Susceptibility to infection with SBV following blood-feeding on an SBV-blood suspension provided via either (i) the Hemotek system or via (ii) a saturated cotton wool pledglet was then compared. Schmallenberg virus susceptibility was defined by RT-qPCR of RNA extractions of head homogenates and related to Culicoides species and haplotype identifications based on the DNA barcode region of the mitochondrial cytochrome c oxidase 1 (cox1) gene.ResultsCulicoides blood-feeding rates were low across all membrane types tested (7.5% chick skin, 0.0% for collagen, 4.4% Parafilm M®, with 6029 female Culicoides being offered a blood meal in total). Susceptibility to infection with SBV through membrane blood-feeding (8 of 109 individuals tested) and pledglet blood-feeding (1 of 94 individuals tested) was demonstrated for the Obsoletus complex, with both C. obsoletus (Meigen) and C. scoticus Downes & Kettle susceptible to infection with SBV through oral feeding. Potential evidence of cryptic species within UK populations was found for the Obsoletus complex in phylogenetic analyses of cox1 DNA barcodes of 74 individuals assessed from a single field-site.ConclusionsMethods described in this study provide the means to blood-feed Palaearctic Culicoides for vector competence studies and colonisation attempts. Susceptibility to SBV infection was 7.3% for membrane-fed members of the subgenus Avaritia and 1.1% for pledglet-fed. Both C. obsoletus and C. scoticus were confirmed as being susceptible to infection with SBV, with potential evidence of cryptic species within UK Obsoletus complex specimens, however the implications of cryptic diversity in the Obsoletus complex on arbovirus transmission remains unknown.
Highlights
Culicoides biting midges (Diptera: Ceratopogonidae) are responsible for the biological transmission of internationally important arboviruses of livestock
Effect of membrane type on blood-feeding A total of 6029 Culicoides were used in the experiments to investigate the effect of membrane type on Culicoides blood-feeding rates: 4681 specimens of the Obsoletus complex including the morphologically cryptic C. obsoletus (Meigen) and C. scoticus Downes & Kettle; 157 C. dewulfi; 4 C. chiopterus; 127 C. pulicaris (L.); 138 C. punctatus (Meigen), 4 C. impunctatus Goetghebuer; 321 C. achrayi
This study has developed artificial blood-feeding techniques for Culicoides in the UK and demonstrated susceptibility to infection with Schmallenberg virus (SBV) in multiple haplotypes of C. obsoletus and C. scoticus under laboratory conditions
Summary
Culicoides biting midges (Diptera: Ceratopogonidae) are responsible for the biological transmission of internationally important arboviruses of livestock. Culicoides biting midges (Diptera: Ceratopogonidae) were suspected as the primary biological vectors of SBV prior to direct study of transmission in the field, due to their involvement in the BTV epidemic in northwestern Europe 5 years earlier [12], and the close phylogenetic relationship of SBV with other Culicoides-borne orthobunyaviruses [1, 13] This hypothesis was confirmed by a series of field-based trials in Belgium, the Netherlands and France that detected significant quantities of SBV RNA in Culicoides collected in close proximity to livestock [14,15,16,17,18], while failing to detect virus in mosquitoes [19]. Techniques to assess the probability of field transmission of SBV by Culicoides and mosquitoes were standardised using colony lines of Culicoides sonorensis Wirth & Jones and Culicoides nubeculosus (Meigen) infected using artificial membrane-based techniques [20, 21]
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