Larval development sites of the main Culicoides species (Diptera: Ceratopogonidae) in northern Europe and distribution of coprophilic species larvae in Belgian pastures
Culicoides; Bluetongue disease; Larval ecology; Vectors; Cow dung; Spatial distribution
Abstract :
[en] 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.
Disciplines :
Entomology & pest control Veterinary medicine & animal health
Author, co-author :
Zimmer, Jean-Yves ; Université de Liège - ULiège > Sciences agronomiques > Entomologie fonctionnelle et évolutive
Brostaux, Yves ; Université de Liège - ULiège > Sciences agronomiques > Statistique, Inform. et Mathém. appliquée à la bioingénierie
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 :
Larval development sites of the main Culicoides species (Diptera: Ceratopogonidae) in northern Europe and distribution of coprophilic species larvae in Belgian pastures
Anon. New disease. Report of the South African cattle and sheep disease commission. Report 16 1876, 189-194.
AOAC Official Methods of Analysis 1990, Assoc. Off. Anal. Chem., Arlington, VA. 15th ed.
Baldet T., Delécolle J.-C., Cêtre-Sossah C., Mathieu B., Meiswinkel R., Gerbier G. Indoor activity of Culicoides associated with livestock in the bluetongue virus (BTV) affected region of Northern France during autumn 2006. Prev. Vet. Med. 2008, 87(1-2):84-97.
Bishop A.L., McKenzie H.J., Barchia I.M., Murison R., Spohr L.J. Positions of juvenile stages of Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae) and of four other flies in bovine dung. Aust. J. Entomol. 1996, 35:209-212.
Blackwell A., King F.C. The vertical distribution of Culicoides impunctatus larvae. Med. Vet. Entomol. 1997, 11:45-48.
Blackwell A., Lock K.A., Marshall B., Boag B., Gordon S.C. The spatial distribution of larvae of Culicoides impunctatus biting midges. Med. Vet. Entomol. 1999, 13:362-371.
Blanton F.S., Wirth W.W. The sand flies (Culicoides) of Florida (Diptera: Ceratopogonidae). Arthropods of Florida and Neighboring Land Areas 1979, vol. 10. Florida Department of Agriculture and Consumer Services, 204 pp.
Borkent A. World Species of Biting Midges (Diptera: Ceratopogonidae) 2014, http://wwx.inhs.illinois.edu/files/9913/9144/3328/CeratopogonidaeCatalog.pdf.
Braverman Y., Galun R., Ziv M. Breeding sites of some Culicoides species (Diptera, Ceratopogonidae) in Israel. Mosq. News 1974, 34:303-308.
Braverman Y., Mumcuoglu K. Newly emerged nulliparous Culicoides imicola Kieffer (Diptera: Ceratopogonidae) with pigmented abdomen. Vet. Parasitol. 2009, 160:356-358.
Buxton P.A. British Diptera associated with fungi. III. Flies of all families reared from about 150 species of fungi. Entomol. Monogr. Mag. 1960, 96:61-94.
Campbell M.M., Kettle D.S. Some factors involved in Culicoides brevitarsis Kieffer finding and ovipositing in dung. Aust. J. Zool. 1976, 24:75-85.
Carpenter S., McArthur C., Selby R., Ward R., Nolan D.V., Mordue Luntz A.J., Dallas J.F., Tripet F., Mellor P.S. Experimental infection studies of UK Culicoides species midges with bluetongue virus serotypes 8 and 9. Vet. Rec. 2008, 163:589-592. 10.1136/vr.163.20.589.
Carpenter S., Mellor P.S., Torr S.J. Control techniques for Culicoides biting midges and their application in the U.K. and northwestern Palaearctic. Med. Vet. Entomol. 2008, 22:175-187.
Chaker E. Contribution à l'étude de la morphologie et de la diagnose des larves de Culicoides (Diptera, Ceratopogonidae) 1983, (Thèse d'Université), Université Louis Pasteur de Strasbourg, Sciences pharmaceutiques, Strasbourg, France, 229 pp.
Conraths F., Eschbaumer M., Freuling C., Gethmann J., Hoffmann B., Kramer M., Probst C., Staubach C., Beer M. Bluetongue disease: an analysis of the epidemic in Germany 2006-2009. Arthropods as Vectors of Emerging Diseases, Parasitology Research Monographs 2012, 103-135. Springer, Berlin, Heidelberg. H. Mehlhorn (Ed.).
Cribb B.W., Brei B., Ridley A.W., Merritt D.J. Occurrence of immature Culicoides molestus (Skuse) (Diptera: Ceratopogonidae) in relation to habitat characteristics. Aust. J. Entomol. 2003, 42:114-118.
De Regge N., Deblauwe I., De Deken R., Vantieghem P., Madder M., Geysen D., Smeets F., Losson B., van den Berg T., Cay A.B. Detection of Schmallenberg virus in different Culicoides spp. by real-time RT-PCR. Transbound. Emerg. Dis. 2012, 10.1111/tbed.12000.
Delécolle J.-C. Nouvelle contribution à l'étude systématique et iconographique des espèces du genre Culicoides (Diptera: Ceratopogonidae) du Nord-Est de la France 1985, (Thèse d'Université), Université Louis Pasteur de Strasbourg, UFR des Sciences de la Vie et de la Terre, Strasbourg, France, 238 pp.
Dijkstra E., Van der Ven I.J.K., Meiswinkel R., Hölzel D.R., Van Rijn P.A., Meiswinkel R. Culicoides chiopterus as a potential vector of bluetongue virus in Europe. Vet. Rec. 2008, 162:422. 10.1136/vr.162.13.422-a.
Downes J.A. Habits and life-cycle of Culicoides nubeculosus (Meigen). Nature 1950, 166:510-511.
Dyce A.L. The recognition of nulliparous and parous Culicoides (Diptera: Ceratopogonidae) without dissection. J. Aust. Entomol. Soc. 1969, 8:11-15.
Dzhafarov S.M. Biting midges (Diptera: Heleidae) of Transcaucasus (Morphology, Biology, Ecology, Geographical Distribution and Harmfulness, Control, Fauna of the Genera Culicoides, Leptoconops and Lasiohelea) 1976, Franklin Book Programs, Cairo, 260 pp.
Elbers A.R.W., Meiswinkel R., van Weezep E., Sloet van Oldruitenborgh-Oosterbaan M.M., Kooi E.A. Schmallenberg virus in Culicoides spp. biting midges, the Netherlands, 2011. Emerg. Infect. Dis. 2013, 19:106-109.
Falconi C., López-Olvera J.R., Gortázar C. BTV infection in wild ruminants, with emphasis on red deer: a review. Vet. Microbiol. 2011, 151(3-4):209-219.
Foxi C., Delrio G. Larval habitats and seasonal abundance of Culicoides biting midges found in association with sheep in northern Sardinia, Italy. Med. Vet. Entomol. 2010, 24:199-209.
Glushchenko N.P., Mirzaeva A.G. Larval habitats and species composition of bloodsucking midges (Diptera: Ceratopogonidae) in mountain landscapes of South Siberia and the Russian Far East. Russ. Entomol. J. 2008, 17(1):63-70.
Goetghebuer M. Le genre Culicoides (Diptères, Cératopogonidés) et ses représentants en Belgique. Biol. Jaarb. 1952, 19:185-191.
Gonzalez M., Lopez S., Mullens B.A., Baldet T., Goldarazena A. A survey of Culicoides developmental sites on a farm in northern Spain, with a brief review of immature habitats of European species. Vet. Parasitol. 2013, 191:81-93.
Harrup L.E., Gubbins S., Barber J., Denison E., Mellor P.S., Purse B.V., Carpenter S. Does covering of farm-associated Culicoides larval habitat reduce adult populations in the United Kingdom?. Vet. Parasitol. 2013, 10.1016/j.vetpar.2013.11.028.
Harrup L.E., Purse B.V., Golding N., Mellor P.S., Carpenter S. Larval development and emergence sites of farm-associated Culicoides in the United Kingdom. Med. Vet. Entomol. 2013, 27:441-449.
Havelka P. Ceratopogonidae. Limnofauna Europaea 1978, 441-458. Gustav Fischer Verlag, Stuttgart. J. Illies (Ed.).
Heilbron D.C. Zero-altered and other regression models for count data with added zeros. Biometr. J. 1994, 36(5):531-547.
Hendry G., Godwin G. Biting midges in Scottish forestry: a costly irritant or a trivial nuisance?. Scot. Forest. 1988, 42:113-119.
Herder V., Wohlsein P., Peters M., Hansmann F., Baumgärtner W. Salient lesions in domestic ruminants infected with the emerging so-called Schmallenberg virus in Germany. Vet. Pathol. 2012, 49:588-591.
Hoffmann B., Bauer B., Bauer C., Bätza H.J., Beer M., Clausen P.-H., Geier M., Gethmann J.M., Kiel E., Liebisch G., Liebisch A., Mehlhorn H., Schaub G.A., Werner D., Conraths F.J. Monitoring of putative vectors of bluetongue virus serotype 8, Germany. Emerg. Infect. Dis. 2009, 15:1481-1484. 10.3201/eid1509.090562.
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. Novel orthobunyavirus in cattle, Europe, 2011. Emerg. Infect. Dis. 2012, 18(3):469-472. 10.3201/eid1803.111905.
Kettle D.S. The spatial distribution of Culicoides impunctatus Goet. under woodland and moorland conditions and its flight range through woodland. Bull. Entomol. Res. 1951, 42:239-291.
Kettle D.S. The bionomics and control of Culicoides impunctatus Goetghebuer (Diptera: Ceratopogonidae), an early attempt (1945-1958) to control this intractable pest. Mem. Entomol. Soc. Wash. 1962, 18:134-139.
Kettle D.S. Biology and bionomics of bloodsucking Ceratopogonids. Annu. Rev. Entomol. 1977, 22:33-51.
Kettle D.S., Lawson J.W.H. The early stages of British midges Culicoides Latreille (Diptera: Ceratopogonidae) and allied genera. Bull. Entomol. Res. 1952, 43:421-467.
Kirkeby C., Bodker R., Stockmarr A., Enoe C. Association between land cover and Culicoides (Diptera: Ceratopogonidae) breeding sites on four Danish cattle farms. Entomol. Fenn. 2009, 20(4):228-232.
Konurbayev E.O. Biting Midges (Diptera: Heleidae) of the Issyk-kul depression in Kirghizia. Entomol. Rev. 1965, 44:75-78.
Kremer M. Contribution à l'étude du genre Culicoides Latreille, particulièrement en France. Encyclopédie entomologique: Série A, Travaux généraux, 39 1965, Edition Lechevalier, Paris, 299 pp.
Kremer M., Hirtzel C., Molet B. Résultats préliminaires d'une étude écologique des Culicoides de Sansouires de Camargue. Ann. Parasitol. Hum. Comp. 1974, 49:653-656.
Lühken R., Kiel E., Steinke S. Impact of mechanical disturbance on the emergence of Culicoides from cowpats. Parasitol. Res. 2014, 10.1007/s00436-014-3766-3.
Magnon G.J., Hagan D.V., Kline D.L., Linley J.R. Habitat characteristics and phenology of larval Culicoides spp. (Diptera: Ceratopogonidae) from a Georgia salt marsh. Environ. Entomol. 1990, 19:1068-1074.
Mehlhorn H., Walldorf V., Klimpel S., Schaub G., Kiel E., Focke R., Liebisch G., Liebisch A., Werner D., Bauer C., Clausen H., Bauer B., Geier M., Hörbrand T., Bätza H.J., Conraths F.J., Hoffmann B., Beer M. Bluetongue disease in Germany (2007-2008): monitoring of entomological aspects. Parasitol. Res. 2009, 105:313-319.
Mehlhorn H., Al-Rasheid K.A.S., Al-Quraishy S., Abdel-Ghaffar F. Research and increase of expertise in arachno-entomology are urgently needed. Parasitol. Res. 2012, 110(1):259-265.
Meiswinkel R., Baldet T., De Deken R., Takken W., Delécolle J.-C., Mellor P.S. The 2006 outbreak of bluetongue in northern Europe - the entomological perspective. Prev. Vet. Med. 2008, 87:55-63. 10.1016/j.prevetmed.2008.06.005.
Mellor P.S., Pitzolis G. Observations on breeding sites and light trap collections of Culicoides during an outbreak of bluetongue in Cyprus. Bull. Entomol. Res. 1979, 69:229-234.
Mellor P.S., Booman J., Baylis M. Culicoides biting midges: their role as arbovirus vectors. Annu. Rev. Entomol. 2000, 45:307-340. 10.1146/annurev.ento.45.1.307.
Mellor P.S., Wittmann E.J. Bluetongue virus in the Mediterranean basin, 1998-2001. Vet. J. 2002, 164:20-37.
Mullen G.R., Hribar L.J. Biology and feeding behavior of ceratopogonid larvae (Diptera: Ceratopogonidae) in North America. Bull. Soc. Vector Ecol. 1988, 13:60-81.
Murray W.S. Investigations on the bionomics of Culicoides obsoletus (Meigen) and other biting midges at Mount Solon, Virginia. Mosq. News 1957, 17(2):77-82.
Ninio C., Augot D., Dufour B., Depaquit J. Emergence of Culicoides obsoletus from indoor and outdoor breeding sites. Vet. Parasitol. 2011, 183:125-129.
Peeters A. Country Pasture/Forage Resource Profile for Belgium 2010, FAO, AGPC, Rome. http://www.fao.org/ag/agp/AGPC/doc/Counprof/Belgium/belgium.htm.
Rasmussen L.D., Kristensen B., Kirkeby C., Rasmussen T.B., Belsham G.J., Bødker R., Bøtner A. Culicoids as vectors of Schmallenberg virus. Emerg. Infect. Dis. 2012, 18(7):1204-1206. 10.3201/eid1807.120385.
Rigot T., Vercauteren Drubbel M., Delécolle J.-C., Gilbert M. Farms, pastures and woodlands: the fine-scale distribution of Palearctic Culicoides spp. biting midges along an agro-ecological gradient. Med. Vet. Entomol. 2013, 27:29-38.
Saegerman C., Berkvens D., Mellor P.S. Bluetongue epidemiology in the European Union. Emerg. Infect. Dis. 2008, 14:539-544.
Saegerman C., Berkvens D., Mellor P.S., Dal Pozzo F., Porter S., Zientara S. Fièvre catarrhale ovine: l'Europe au carrefour de l'enzootie. Point Vét. 2008, 290:41-47.
Satta G., Goffredo M., Sanna S., Vento L., Cubeddu G.P., Mascherpa E. Field disinfestation trials against Culicoides in north-west Sardinia. Vet. Ital. 2004, 40(3):329-335.
Schmidtmann E.T., Bobian R.J., Belden R.P. Soil chemistries define aquatic habitats with immature populations of the Culicoides variipennis complex (Diptera: Ceratopogonidae). J. Med. Entomol. 2000, 37:58-64.
Schmidtmann E.T. Testing the relationship between dissolved salts in aquatic habitats and immature populations of the C. variipennis complex (Diptera: Ceratopogonidae). Environ. Entomol. 2006, 35:1154-1160.
Smith W.W., Varnell J.H. Hydrogen ion concentration (pH) as related to the occurrence and abundance of tree-holes dwelling Culicoides spp. in northern Florida. Mosq. News 1967, 27:519-521.
Sperlova A., Zendulkova D. Bluetongue: a review. Vet. Med. Czech. 2011, 56:430-452.
Takken W., Verhulst N., Scholte E.J., Jacobs F., Jongema Y., van Lammeren R. The phenology and population dynamics of Culicoides spp. in different ecosystems in The Netherlands. Prev. Vet. Med. 2008, 87(1-2):41-54.
Thiry E., Saegerman C., Guyot H., Kirten P., Losson B., Rollin F., Bodmer M., Czaplicki G., Toussaint J.F., De Clercq K., De Dochy J.M., Dufey J., Gilleman J.L., Messeman K. Bluetongue in northern Europe. Vet. Rec. 2006, 159:327. 10.1136/vr.159.10.327.
Uslu U., Dik B. Vertical distribution of Culicoides larvae and pupae. Med. Vet. Entomol. 2006, 20:350-352.
Uslu U., Dik B. Description of breeding sites of Culicoides species (Diptera: Ceratopogonidae) in Turkey. Parasite 2007, 14:173-177.
Uslu U., Dik B. Chemical characteristics of breeding sites of Culicoides species (Diptera: Ceratopogonidae). Vet. Parasitol. 2010, 169:178-184.
Van den Brom R., Luttikholt S.J., Lievaart-Peterson K., Peperkamp N.H., Mars M.H., van der Poel W.H., Vellema P. Epizootic of ovine congenital malformations associated with Schmallenbergvirus infection. Tijdschr. Diergeneeskd. 2012, 137:106-111.
Vandermotten C., Decroly J.-M. Géographie, dans Wallonie. Atouts et références d'une Région 1995, Gouvernement wallon, Namur.
Velthuis A.G., Saatkamp H.W., Mourits M.C., de Koeijer A.A., Elbers A.R. Financial consequences of the Dutch bluetongue serotype 8 epidemics of 2006 and 2007. Prev. Vet. Med. 2010, 93(4):294-304.
Veronesi E., Henstock M., Gubbins S., Batten C., Manley R., Barber J., Hoffmann B., Beer M., Attoui H., Mertens P.P.C., Carpenter S. Implicating Culicoides biting midges as vectors of Schmallenberg virus using semi-quantitative RT-PCR. PLoS ONE 2013, 8(3):e57747. 10.1371/journal.pone.0057747.
Weinburgh H.B., Pratt H.D. Culicoides, Public Health Importance, Biology, Survey, and Control 1962, U.S. Department of Health, Education and Welfare, Public Health Service, Communicable Disease Center, Atlanta, Georgia, 17 pp.
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. Breeding sites of bluetongue vectors in northern Europe. Vet. Rec. 2008, 162:131. 10.1136/vr.162.4.131.
Zimmer J.-Y., Losson B., Saegerman C., Haubruge E. Ecologie et distribution des espèces de Culicoides Latreille 1809 (Diptera: Ceratopogonidae) à proximité d'une exploitation bovine en Belgique. Ann. Soc. Entomol. Fr. 2009, 45(3):393-400.
Zimmer J.-Y., Saegerman C., Losson B., Haubruge E. Breeding sites of bluetongue virus vectors, Belgium. Emerg. Infect. Dis. 2010, 16(3):575-576.
Zimmer J.-Y., Saegerman C., Losson B., Beckers Y., Haubruge E., Francis F. Chemical composition of silage residues sustaining the larval development of the Culicoides obsoletus/Culicoides scoticus species (Diptera: Ceratopogonidae). Vet. Parasitol. 2013, 191:197-201. 10.1016/j.vetpar.2012.08.014.
Zimmer J.-Y., Smeets F., Simonon G., Fagot J., Haubruge E., Francis F., Losson B. Are bogs reservoirs for emerging disease vectors? Evaluation of Culicoides populations in the Hautes Fagnes Nature Reserve (Belgium). PLoS ONE 2013, 8(6):e66893. 10.1371/journal.pone.0066893.
Zimmer J.-Y., Losson B., Saegerman C., Haubruge E., Francis F. Breeding sites and species association of the main bluetongue and Schmallenberg virus vectors, the Culicoides species (Diptera: Ceratopogonidae), in northern Europe. Ann. Soc. Entomol. Fr. 2013, 49(3):335-344.
Zimmer J.-Y., Losson B., Saegerman C., Kirschvink N., Haubruge E., Francis F. Comparaison des populations de Culicoides Latreille 1809 (Diptera: Ceratopogonidae) présentes au sein d'une bergerie belge et d'une prairie ovine associée. Ann. Soc. Entomol. Fr. 2013, 49(4):446-459.
Zimmer J.-Y., Haubruge E., Francis F. Synthèse bibliographique: l'écologie larvaire des culicoïdes (Diptera: Ceratopogonidae). Biotechnol. Agron. Soc. Environ. 2014, 18(2):301-312.
Zimmer J.-Y., Saegerman C., Martinelle L., Losson B., Leroy P., Haubruge E., Francis F. Les porcheries: réservoirs des culicoïdes (Diptera: Ceratopogonidae), vecteurs des virus de la Maladie de la Langue bleue et de Schmallenberg?. Biotechnol. Agron. Soc. Environ. 2014, (in press).
