Jean-Yves Zimmer

Breeding sites of bluetongue vectors in northern Europe

SIR, — Bluetongue has recently been spreading in northern Europe, starting in Belgium and the Netherlands in August 2006. In 2006 there were 695 outbreaks in Belgium (399 sheep farms and 296 cattle farms). In 2007, according to data provided by the Federal Agency for the Safety of the Food Chain

Breeding sites of bluetongue virus vectors, belgium.

To the Editor: Bluetongue (BT) is an emerging disease of ruminants in northern Europe (1,2). This disease was reported in August 2006 in the Netherlands and a few days later in Belgium. In 2006, animals in the Netherlands, Belgium, and Germany were affected. In contrast to 2006, when BT virus (BTV) was identified in ≈2,000 enclosures on farms, BTV was identified in >40,000 farm buildings containing ruminants in 2007; many infected animals had severe disease. In addition, the virus expanded its range to include large areas of France, Denmark, the United Kingdom, Switzerland, and the Czech Republic (2). In 2008, BTV serotype 8 (BTV-8) continued its spread across Europe and showed virulence in France where 26,925 BTV-8 outbreaks were reported (3). This observation indicates possible overwintering of the vector from year to year. However, the mechanism of overwintering is not clear. The biting midges responsible for transmission of BTV in northern Europe belong to the genus Culicoides, but only few species are vectors of this virus (2). During the winter of 2006–2007, Losson et al. (1) monitored the presence of biting midges inside farm buildings. Zimmer et al. (4) observed potential vectors of BTV inside a sheepfold during the winter of 2007–2008 and in farm buildings in 2008. These authors suggested that Culicoides spp. may be more abundant indoors than outdoors when animals are kept in these buildings. Breeding sites of bluetongue vector species have been found near farms (silage residues) (5) and in neighboring meadows (overwintering cattle dung and silt along a pond) (5,6) but not inside sheds. We conducted a study on 5 cattle farms in Belgium during February–October 2008. Three samplings were performed: the first in late February, the second in mid-June, and the third in late October. Soil samples (15 biotopes) were collected inside cowsheds. These samples were incubated at 24°C to enable adult midges to emerge. All Culicoides specimens were identified by sex and to the species level by using the morphologic key of Delecolle (7). Among 15 soil biotopes obtained from farm buildings, only 1 showed the emergence of adult Culicoides biting midges. At a cattle farm in Spy (50°28′31′′N, 4°40′39′′E), we found that dried dung adhering to walls inside animal enclosures and used animal litter was a breeding site for the C. obsoletus/scoticus complex (Table). Only 25% of emerging Culicoides midges were females. Table Culicoides species obtained from dried dung samples inside a cowshed, Spy, Belgium, 2008 We observed that C. obsoletus/scoticus complex midges are more prevalent in soil samples with a high carbon:nitrogen (C:N) index; this index indicates the amount of organic matter in soil. C:N indices between 15 and 30 support production of humus and ensure good microbial growth. In addition, larvae of Culicoides spp. feed on organic material and microorganisms in soil (8). Our observations suggest that biting midges can complete their life cycle in animal enclosures. This finding is consistent with the high capture rates of nulliparous (empty and unpigmented abdomens) (9) adult midges observed when suction light traps (Onderstepoort Veterinary Institute, Onderstepoort, South Africa) were used on cattle farms during April–May 2007 (4). We identified a breeding site for the primary BTV vector in a cowshed in northern Europe (10). Vectors feed on blood, overwinter inside cowsheds (1), lay eggs, and larvae develop under such conditions. These observations could explain the persistence of BTV from year to year despite fairly harsh winters. Hygienic measures on farms could reduce midge populations and improve efficacy of vaccination campaigns against BT in Europe. We strongly recommend that such integrated control strategies be evaluated. Removal of residual animal feed and feces on farms and of material from silage structures and sheds, particularly deposits of manure adhering to walls of sheds and used litter, are simple and inexpensive measures that should be implemented. However, their success will depend on active participation by farmers.

Chemical composition of silage residues sustaining the larval development of the Culicoides obsoletus/Culicoides scoticus species (Diptera: Ceratopogonidae)

Culicoides (Diptera: Ceratopogonidae) are biological vectors of bluetongue virus (BTV). Bluetongue is a viral disease that affects domestic and wild ruminants. Since its recent emergence in northern Europe, this disease has caused considerable economic losses to the sheep and cattle industry. The biotopes, and more particularly the chemical characteristics which are suitable for larval development of the main vector species, are still relatively unknown. This study shows that the larvae of biting midges belonging to the species Culicoides obsoletus and Culicoides scoticus are able to breed in different types of silage residue (maize, grass, sugar beet pulp and their combinations). The chemical composition of substrates strongly influences the presence of the immature stages of these biting midges. Higher lignin and insoluble fibre contents seem to favour their presence and could play the role of a physical support for semi-aquatic larvae. In contrast, higher concentrations of magnesium and calcium are negatively correlated with the presence of these two species. These data will help to locate and monitor the breeding sites of these species and could contribute to the control of these insects on farms.

Larval development sites of the main Culicoides species (Diptera: Ceratopogonidae) in northern Europe and distribution of coprophilic species larvae in Belgian pastures.

Some Culicoides species of biting midges (Diptera: Ceratopogonidae) are biological virus vectors worldwide and have indeed been associated with outbreaks of important epizoonoses in recent years, such as bluetongue and Schmallenberg disease in northern Europe. These diseases, which affect domestic and wild ruminants, have caused considerable economic losses. Knowledge of substrates suitable for Culicoides larval development is important, particularly for the main vector temperate species. This study, realized during two years, aimed to highlight the larval development sites of these biting midge species in the immediate surroundings of ten Belgian cattle farms. Moreover, spatial distribution of the coprophilic Culicoides larvae (C. chiopterus and C. dewulfi) within pastures was studied with increasing distance from farms along linear transects (farm-pasture-woodland). A total of 4347 adult specimens belonging to 13 Culicoides species were obtained by incubation of 2131 soil samples belonging to 102 different substrates; 18 of these substrates were suitable for larval development. The Obsoletus complex (formed by two species) was observed in a wide range of substrates, including silage residues, components of a chicken coop, dung adhering to walls inside stables, leftover feed along the feed bunk, a compost pile of sugar beet residues, soil of a livestock trampling area, and decaying wood, while the following served as substrates for the other specimens: C. chiopterus, mainly cow dung; C. dewulfi, cow dung and molehill soil; C. circumscriptus, algae; C. festivipennis, algae and soil in stagnant water; C. nubeculosus, algae and silt specifically from the edge of a pond; C. punctatus, mainly wet soil between silage reserves; C. salinarius, algae; and C. stigma, algae and wet soil between silage reserves. We also recorded significantly higher densities of coprophilic larvae within pastures in cow dung located near forests, which is likely due to the localization of potential hosts; the presence of these larvae within cow dung is, however, uninfluenced by relative distance from farms. A better knowledge of the microhabitats of Culicoides biting midges and their spatial distribution may allow the development of targeted species-specific vector control strategies, and may help to prevent the creation of new larval development sites.

Reintroduction of the invasive mosquito species Aedes albopictus in Belgium in July 2013.

Since its first report in 2000, the invasive mosquito Aedes albopictus was not found any more during the different entomological inspections performed at its place of introduction in Belgium between 2001 and 2012. In July 2013, one adult male was captured at the same site (a platform of imported used tires located in Vrasene, Oost-Vlaanderen Province), during a monitoring using CO2-baited trap. This finding suggests the reintroduction of the species in Belgium via the used tire trade.

Are bogs reservoirs for emerging disease vectors? Evaluation of culicoides populations in the Hautes Fagnes Nature Reserve (Belgium).

Several species of Culicoides (Diptera: Ceratopogonidae) biting midges serve as biological vectors for the bluetongue virus (BTV) and the recently described Schmallenberg virus (SBV) in northern Europe. Since their recent emergence in this part of the continent, these diseases have caused considerable economic losses to the sheep and cattle industries. Much data is now available that describe the distribution, population dynamics, and feeding habits of these insects. However, little is known regarding the presence of Culicoides in unusual habitats such as peaty marshes, nor their potential vector capacity. This study evaluated Culicoides biting midges present in the bogs of a Belgian nature reserve compared to those residing at a nearby cattle farm. Culicoides were trapped in 2011 at four different sites (broadleaved and coniferous forested areas, open environments, and at a scientific station) located in the Hautes Fagnes Nature Reserve (Belgium). An additional light trap was operated on a nearby cattle farm. Very high numbers of biting midges were captured in the marshy area and most of them (70 to 95%) were Culicoides impunctatus, a potential vector of BTV and other pathogens. In addition, fewer numbers of C. obsoletus/C. scoticus species, C. chiopterus, and C. dewulfi were observed in the bogs compared to the farm. The wet environment and oligotrophic nature of the soil were probably responsible for these changes in the respective populations. A total of 297,808 Culicoides midges belonging to 27 species were identified during this study and 3 of these species (C. sphagnumensis, C. clintoni and C. comosioculatus) were described in Belgium for the first time.

Ecologie et distribution des espèces de Culicoides Latreille 1809 (Diptera: Ceratopogonidae) à proximité d’une exploitation bovine en Belgique

Résumé La Maladie de la Langue bleue est une maladie non contagieuse qui affecte les ruminants domestiques et sauvages. Depuis son extension au Nord de l’Europe en 2006, cette épizootie virale a engendré des pertes économiques considérables sur le cheptel ovin et bovin. Les vecteurs biologiques du virus de la FCO (BTV) sont des moucherons appartenant au genre Culicoides. De nombreuses inconnues subsistent encore sur leur biologie, physiologie, écologie et distribution. Cette étude montre que ces moucherons piqueurs sont bien plus abondants au niveau de la ferme que dans les prairies avoisinantes; ces dernières présentent toutefois une plus grande diversité spécifique. C’est ainsi que la possibilité de migration entre la prairie et la ferme est émise pour les espèces C. chiopterus et C. dewulfi. Tant pour la ferme que pour la prairie, les femelles sont beaucoup plus représentées que les mâles. L’observation de la physiologie de celles-ci est réalisée tout au long de l’étude.

Breeding sites and species association of the main Bluetongue and Schmallenberg virus vectors, the Culicoides species (Diptera: Ceratopogonidae), in northern Europe

Summary Several species of Culicoides (Diptera: Ceratopogonidae) biting midges are biological vectors of bluetongue virus (BTV) and, as recently discovered, Schmallenberg virus (SBV) in northern Europe. Since their recent emergence in this part of the continent, these diseases that affect domestic and wild ruminants have caused considerable economic losses to the sheep and cattle industries. The substrates that are suitable for larval development of the main vector species are still relatively unknown. This study assessed all the substrates present in the immediate surroundings of a Belgian cattle farm and aimed to highlight the main breeding sites of these midge species. A total of 1639 immature Culicoides and 1320 adult specimens belonging to 13 species were found in 15 out of the 43 substrates studied: maize silage residues for C. obsoletus/C. scoticus, old overwintered cattle dung in the meadow for C. chiopterus and C. dewulfi, ground of a flooded meadow, green filamentous algae and underlying substrate, silt from a pond, and ground of hollows caused by the crossing of machines on a dirt track for C. festivipennis, silt from a pond for C. nubeculosus, and ground of a flooded meadow for C. lupicaris. Identification of these micro-habitats and the associations among the species they contain could allow their localization and the development of new strategies of vector control, while preventing the creation of new Culicoides larval micro-habitats. Finally, measures designed to reduce larval populations could improve efficacy of vaccination campaigns against BTV in Europe.

Comparaison des populations de Culicoides Latreille 1809 (Diptera : Ceratopogonidae) présentes au sein d’une bergerie belge et d’une prairie ovine associée

Summary Culicoides biting midges (Diptera: Ceratopogonidae) serve as biological vectors for several pathogens, including the Bluetongue virus and the recently described Schmallenberg virus in northern Europe. These diseases have caused considerable direct and indirect economic losses to the sheep and cattle industries. This study undertaken between August and December 2007 on a sheep farm in the Namur province (Belgium) aims to evaluate Culicoides populations present inside a partially opened sheepfold and in a nearby sheep meadow, using light traps. The comparative analysis of insects trapped at 18 dates at regular intervals showed that Culicoides were most abundant inside this livestock building (17,450 midges) than in surrounding meadow (1,121 midges); this meadow had however a greater species diversity. The two species C. obsoletus and C. scoticus constituting the Obsoletus complex predominated for all trappings and females were much more numerous than males. Important capture of engorged females of the Obsoletus complex inside the sheepfold seems to reflect the possibility of an opportunistic endophagous behavior. Maintaining sheep inside livestock buildings in order to reduce the risk of Culicoides bites – and thus of pathogens transmission – however requires to limit biting midge populations which are likely to enter or to develop inside these buildings. Implementation of effective sanitation and hygiene measures against midges present inside farms, as well as establishing of measures to protect livestock against intrusion and improvement of “midge-proofing” of animal housing are therefore highly recommended.

Diversity and ecology survey of mosquitoes potential vectors in Belgian equestrian farms: A threat prevention of mosquito-borne equine arboviruses

Emergence of West Nile Virus was recently recorded in several European countries, which can lead to severe health problems in horse populations. Europe is also at risk of introduction of mosquito-borne equine alphavirus from Americas. Prevention of these arboviruses requires a clear understanding of transmission cycles, especially their vectors. To characterize mosquito fauna, their ecology and identify potential vectors of equine arboviruses in Belgium, entomological surveys of six equestrian farms located in the Wolloon Region were conducted during 2011-2012. The harvest of mosquitoes was based on larval sampling (272 samples from 111 breeding sites) and monthly adults trapping (CO2-baited traps, Mosquito Magnet Liberty Plus). Among 51,493 larvae and 319 adult mosquitoes collected, morphological identification showed the presence of 11 species: Anopheles claviger (Meigen), An. maculipennis s.l. (Meigen), An. plumbeus (Stephens), Culex hortensis (Ficalbi), Cx. territans (Walker), Cx. pipiens s.l. L., Cx. torrentium (Martini), Coquillettidia richiardii (Ficalbi), Culiseta annulata (Schrank), Aedes cantans (Meigen), Ae. geniculatus (Olivier). Molecular identification of Cx. pipiens species complex allowed the detection of three molecular forms, Pipiens (92.3%), Molestus (4.6%) and Hybrid (3.1%). Larvae of Cx. pipiens sl and Cx. torrentium were omnipresent and the most abundant species. Water troughs, ponds and slurry (liquid manure) were the most favorable breeding sites of mosquito larvae. Based upon behavior and ecology of the identified mosquito species, Studied Belgian equestrian farms seem to provide a suitable environment and breeding sites for the proliferation of potential vectors of arboviruses and those being a real nuisance problem for horses and neighboring inhabitants.