Environmental Drivers of Culicoides Phenology: How Important Is Species-Specific Variation When Determining Disease Policy?

Abstract

Since 2006, arboviruses transmitted by Culicoides biting midges (Diptera: Ceratopogonidae) have caused significant disruption to ruminant production in northern Europe. The most serious incursions involved strains of bluetongue virus (BTV), which cause bluetongue (BT) disease. To control spread of BTV, movement of susceptible livestock is restricted with economic and animal welfare impacts. The timing of BTV transmission in temperate regions is partly determined by the seasonal presence of adult Culicoides females. Legislative measures therefore allow for the relaxation of ruminant movement restrictions during winter, when nightly light-suction trap catches of Culicoides fall below a threshold (the ‘seasonally vector free period’: SVFP). We analysed five years of time-series surveillance data from light-suction trapping in the UK to investigate whether significant inter-specific and yearly variation in adult phenology exists, and whether the SVFP is predictable from environmental factors. Because female vector Culicoides are not easily morphologically separated, inter-specific comparisons in phenology were drawn from male populations. We demonstrate significant inter-specific differences in Culicoides adult phenology with the season of Culicoides scoticus approximately eight weeks shorter than Culicoides obsoletus. Species-specific differences in the length of the SVFP were related to host density and local variation in landscape habitat. When the Avaritia Culicoides females were modelled as a group (as utilised in the SFVP), we were unable to detect links between environmental drivers and phenological metrics. We conclude that the current treatment of Avaritia Culicoides as a single group inhibits understanding of environmentally-driven spatial variation in species phenology and hinders the development of models for predicting the SVFP from environmental factors. Culicoides surveillance methods should be adapted to focus on concentrated assessments of species-specific abundance during the start and end of seasonal activity in temperate regions to facilitate refinement of ruminant movement restrictions thereby reducing the impact of Culicoides-borne arboviruses.

A first estimation of Culicoides imicola and Culicoides obsoletus/Culicoides scoticus seasonality and abundance in Europe

“…In Northern Europe, most Culicoides species overwinter in the fourth larval stage and although live adult specimen can be found in stables during winter, their numbers seems to be insufficient to drive BTV outbreaks (Searle et al 2014). In Southern Europe, Culicoides, as a group, are probably active throughout the year in some warm winter areas.…”

Blood-feeding, susceptibility to infection with Schmallenberg virus and phylogenetics of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom

“…Within northwestern Europe, the Culicoides fauna on farms and stables are dominated by species classified within the subgenus Avaritia [18,22,23]. Until recently four species within this subgenus have been identified within this region and are commonly referred to as the Obsoletus group, despite a lack of monophyly: Culicoides obsoletus (Meigen) and Culicoides scoticus Downes & Kettle; Culicoides dewulfi Goetghebuer and Culicoides chiopterus (Meigen) [24][25][26].…”

Field sampling methods for mosquitoes, sandflies, biting midges and ticks

“…To obtain data that are comparable, the VectorNet Culicoides group has mostly carried out studies based on a longitudinal design. Climate, livestock density and land cover have been demonstrated as drivers of Culicoides seasonality and species composition [51,52]. An efficient strategy to assess abundance with a relatively small number of collection sites is to use latitudinal and altitudinal transects to sample different classes of livestock and land cover.…”