Breeding sites and species association of the main Bluetongue and Schmallenberg virus vectors, the Culicoides species (Diptera: Ceratopogonidae), in northern Europe
[en] 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.
Disciplines :
Veterinary medicine & animal health Entomology & pest control
Author, co-author :
Zimmer, Jean-Yves ; Université de Liège - ULiège > Sciences agronomiques > Entomologie fonctionnelle et évolutive
Losson, Bertrand ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Parasitologie et pathologie des maladies parasitaires
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Epidémiologie et analyse des risques appl. aux sc. vétér.
Haubruge, Eric ; Université de Liège - ULiège > Vice-Recteur de Gembloux Agro Bio Tech
Francis, Frédéric ; Université de Liège - ULiège > Sciences agronomiques > Entomologie fonctionnelle et évolutive
Language :
English
Title :
Breeding sites and species association of the main Bluetongue and Schmallenberg virus vectors, the Culicoides species (Diptera: Ceratopogonidae), in northern Europe
Bishop AL, McKenzie HJ, Barchia IM, Harris AM. 1996. Effect of temperature regimes on the development, survival and emergence of Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae) in bovine dung. Australian Journal of Entomology. 35:361-368.
Buxton PA. 1960. British Diptera associated with fungi. III. Flies of all families reared from about 150 species of fungi. Entomologists' Monthly Magazine. 96:61-94.
Carpenter S, McArthur C, Selby R, Ward R, Nolan DV, Mordue Luntz AJ, Dallas JF, Tripet F, Mellor PS. 2008. Experimental infection studies of UK Culicoides species midges with bluetongue virus serotypes 8 and 9. Veterinary Record. 163:589-592.
Chaker E. 1983. Contribution à l'étude de la morphologie et de la diagnose des larves de Culicoides (Diptera, Ceratopogonidae) [thèse de Doctorat es Sciences Pharmaceutiques (Diplôme d'Etat)]. Université Louis Pasteur de Strasbourg, no. 56, 229 p.
Delécolle JC. 1985. Nouvelle contribution à l'étude systématique et iconographique des espèces du genre Culicoides (Diptera, Ceratopogonidae) du Nord-Est de la France [thèse de Doctorat d'Université]. Université Louis Pasteur de Strasbourg, no. 293, 238 p.
Delécolle JC, de La Rocque S. 2002. Contribution à l'étude des Culicoides de Corse. Liste des espèces recensées en 2000/2001 et redescription du principal vecteur de la fièvre catarrhale ovine : C. imicola Kieffer, 1913 (Diptera, Ceratopogonidae). Bulletin de la Société entomologique de France. 107:371-379.
De Regge N, Deblauwe I, De Deken R, Vantieghem P, Madder M, Geysen D, Smeets F, Losson B, van den Berg T, Cay AB. 2012. Detection of Schmallenberg virus in different Culicoides spp. by real-time RT-PCR. Transboundary and Emerging Diseases. 59:471-475.
Du Toit RM. 1944. The transmission of blue-tongue and horse sickness by Culicoides. Onderstepoort Journal of Veterinary Science and Animal Industry. 19:7-16.
Dzhafarov SM. 1976. Biting midges (Diptera: Heleidae) of Transcaucasus (morphology, biology, ecology, geographical distribution and harmfulness, control, fauna of the genera Culicoides, Leptoconops and Lasiohelea). Cairo: Franklin Book Programs. 525 p.
Foxi C, Delrio G. 2010. Larval habitats and seasonal abundance of Culicoides biting midges found in association with sheep in northern Sardinia, Italy. Medical and Veterinary Entomology. 24:199-209.
Glukhova VM. 1967. On the technique of collecting and cultivation of larvae of bloodsucking midges (Diptera, Ceratopogonidae). Parazitologiya. 1:171-175.
Glukhova VM. 1977. On the subgenera classification of the genus Culicoides Latreille 1809 (Diptera, Ceratopogonidae) considerating morphological structures of larvae. Parazitologiya. 27:112-118.
Glushchenko NP, Mirzaeva AG. 2008. Larval habitats and species composition of bloodsucking midges (Diptera: Ceratopogonidae) in mountain landscapes of South Siberia and the Russian Far East. Russian Entomological Journal. 17:63-70.
Harrup LE, Purse BV, Golding N, Mellor PS, Carpenter S. 2013. Larval development and emergence sites of farm-associated Culicoides in the United Kingdom. Medical and Veterinary Entomology. doi:10.1111/mve.12006.
Hendry G, Godwin G. 1988. Biting midges in Scottish forestry: a costly irritant or a trivial nuisance? Scottish Forestry. 42: 113-119.
Herder V, Wohlsein P, Peters M, Hansmann F, Baumgärtner W. 2012. Salient lesions in domestic ruminants infected with the emerging so-called Schmallenberg virus in Germany. Veterinary Pathology. 49:588-591.
Hoffmann B, Bauer B, Bauer C, Bätza H-J, Beer M, Clausen P-H, Geier M, Gethmann JM, Kiel E, Liebisch G, Liebisch A, Mehlhorn H, Schaub GA, Werner D, Conraths FJ. 2009. Monitoring of putative vectors of bluetongue virus serotype 8, Germany. Emerging Infectious Diseases. 15:1481-1484.
Hoffmann B, Scheuch M, Höper D, Jungblut R, Holsteg M, Schirrmeier H, Eschbaumer M, Goller KV, Wernike K, Fischer M, Breithaupt A, Mettenleiter TC, Beer M. 2012. Novel Orthobunyavirus in cattle, Europe, 2011. Emerging Infectious Diseases. 18:469-472.
Hutcheon D. 1902. Malarial catarrhal fever of sheep. Veterinary Record. 14:629-633.
Kettle DS. 1962. The bionomics and control of Culicoides and Leptoconops (Diptera, Ceratopogonidae = Heleidae). Annual Review of Entomology. 7:401-418.
Kettle DS, Lawson JWH. 1952. The early stages of British biting midges Culicoides Latreille (Diptera: Ceratopogonidae) and allied genera. Bulletin of Entomological Research. 43:421-467.
Kirkeby C, Bodker R, Stockmarr A, Enoe C. 2009. Association between land cover and Culicoides (Diptera: Ceratopogonidae) breeding sites on four Danish cattle farms. Entomologica Fennica. 20:228-232.
KremerM, Hirtzel C, Molet B. 1974. Résultats préliminaires d'une étude écologique des Culicoides de Sansouires de Camargue. Annales de Parisitologie Humaine et Comparée. 49:653-656.
Kremer M, Rieb J-P, Rebholtz C. 1978. Ecology of the ceratopogonids of the Alsace plain. I. The genus Culicoides in the humid soils of the Ried. Annales de Parasitologie Humaine et Comparée. 53:101-115.
Linley JR, Adams GM. 1972. Ecology and behaviour of immature Culicoides melleus. Bulletin of Entomological Research. 62:113-127.
Linley JR, Kettle DS. 1964. A description of the larvae and pupae of Culicoides furens Poey, and Culicoides hoffmani Fox (Diptera, Ceratopogonidae). Annals and Magazine of Natural History. 7:129-149.
Losson B, Mignon B, Paternostre J, Madder M, De Deken R, De Deken G, Deblauwe I, Fassotte C, Cors R, Defrance T, Delécolle J-C, Baldet T, Haubruge E, Frédéric F, Bortels J, Simonon G. 2007. Biting midges overwintering in Belgium. Veterinary Record. 160:451-452.
Mehlhorn H, Walldorf V, Klimpel S, Jahn B, Jaeger F, Eschweiler J, Hoffmann B, Beer M. 2007. First occurrence of Culicoides obsoletus-transmitted Bluetongue virus epidemic in Central Europe. Parasitology Research. 101:219-228.
Meiswinkel R, Baldet T, De Deken R, Takken W, Delécolle JC, Mellor PS. 2008. The 2006 outbreak of bluetongue in northern Europe-The entomological perspective. Preventive Veterinary Medicine. 87:55-63.
Minitab Inc. 2006. Minitab Statistical Software, Release 15 for Windows. State College, PA, USA.
Murray WS. 1957. Investigations on the bionomics of Culicoides obsoletus (Meigen) and other biting midges at Mount Solon, Virginia. Mosquito News. 17:77-82.
Rieb J-P. 1982. Contribution à la connaissance de l'écologie et de la biologie des Cératopogonidés (Diptera, Nematocera) [thèse d'Université]. Strasbourg (France): Université Louis Pasteur de Strasbourg, 395 p.
Rieb J-P. 1987. L'estivo-hibernation et le contrôle de la dynamique du cycle évolutif dans le genre Culicoides (Diptères, Cératopogonidés). Vie Milieu. 37:23-37.
Saegerman C, Berkvens D, Mellor PS. 2008. Bluetongue epidemiology in the European Union. Emerging Infectious Diseases. 14:539-544.
Saegerman C, Berkvens D, Mellor PS, Dal Pozzo F, Porter S, Zientara S. 2008. Fièvre catarrhale ovine: l'Europe au Carrefour de l'enzootie. Point Vétérinaire. 290:41-47.
Sperlova A, Zendulkova D. 2011. Bluetongue: a review. Veterinarni Medicina. 56:430-452.
Szmaragd C, Wilson A, Carpenter S, Mertens PPC, Mellor PS, Gubbins S. 2007. Mortality and case fatality during the recurrence of BTV-8 in northern Europe in 2007. Veterinary Record 161:571-572.
Uslu U, Dik B. 2006. Vertical distribution of Culicoides larvae and pupae. Medical and Veterinary Entomology. 20:350-352.
Uslu U, Dik B. 2007. Description of breeding sites of Culicoides species (Diptera: Ceratopogonidae) in Turkey. Parasite. 14: 173-177.
Uslu U, Dik B. 2010. Chemical characteristics of breeding sites of Culicoides species (Diptera: Ceratopogonidae). Veterinary Parasitology. 169:178-184.
Van den Brom R, Luttikholt SJ, Lievaart-Peterson K, Peperkamp NH, Mars MH, van der Poel WH, Vellema P. 2012. Epizootic of ovine congenital malformations associated with Schmallenberg virus infection. Tijdschrift voor Diergeneeskunde. 137:106-111.
Veronesi E, Henstock M, Gubbins S, Batten C, Manley R, Barber J, Hoffmann B, Beer M, Attoui H, Mertens PPC, Carpenter S. 2013. Implicating Culicoides biting midges as vectors of Schmallenberg virus using semi-quantitative RT-PCR. PLoS ONE. 8: e57747. doi:10.1371/journal.pone.0057747.
Weinburgh HB, Pratt HD. 1962. Culicoides, public health importance, biology, survey, and control. US Department of Health, Education and Welfare, Public Health Service, Communicable Disease Center, Atlanta, Georgia.
World Organization for Animal Health. 2006. Bluetongue detected for the first time in Northern Europe. Press release. Aug 23. Available from http://www.oie.int/eng/press/en-060823.htm
Zimmer J-Y, Haubruge E, Francis F, Bortels J, Simonon G, Losson B, Mignon B, Paternostre J, De Deken R, De Deken G, Deblauwe I, Fassotte C, Cors R, Defrance T. 2008. Breeding sites of bluetongue vectors in northern Europe. Veterinary Record. 162:131.
Zimmer J-Y, Losson B, Saegerman C, Haubruge E. 2009. Ecologie et distribution des espèces de Culicoides Latreille 1809 (Diptera : Ceratopogonidae) à proximité d'une exploitation bovine en Belgique. Annales de la Société entomologique de France. 45:393-400.
Zimmer J-Y, Saegerman C, Losson B, Beckers Y, Haubruge E, Francis F. 2013. Chemical composition of silage residues sustaining the larval development of the Culicoides obsoletus/Culicoides scoticus species (Diptera: Ceratopogonidae). Veterinary Parasitology. 191:197-201.
Zimmer J-Y, Saegerman C, Losson B, Haubruge E. 2010. Breeding sites of bluetongue virus vectors, Belgium. Emerging Infectious Diseases. 16:575-576.
Zimmer J-Y, Smeets F, Simonon G, Fagot J, Haubruge E, Francis F, Losson B, 2013. Are bogs reservoirs for emerging disease vectors? Evaluation of Culicoides populations in the Hautes Fagnes Nature Reserve (Belgium). PLoS ONE. 8: e66893. doi:10.1371/journal.pone.0066893.