Abstract
Sticky traps were mounted on heifers and sheep to assess Culicoides spp. (Diptera: Ceratopogonidae) host preference. Initially, four coloured 200-cm2 sticky traps (white, clear, yellow and blue) were attached to the backs of each of ten Friesian heifers that were released into open pasture for 24 h, repeated on six occasions. More Obsoletus group Culicoides were caught on the white and clear traps than on the yellow and blue. Trap position on the right or left flank also affected midge catch, probably due to heifer orientation in the field. Next, six Friesian heifers and six Charollais hoggets each had one clear and one white sticky strap attached to their backs for one 24-h period per week, repeated for 24 weeks. Overall, Obsoletus group Culicoides comprised 91.8 % (n = 5, 955) of the midge catch but there was no evidence of host preference, either discounting or including host live weight in the analyses. However, Pulicaris group Culicoides did demonstrate a significant host preference for sheep, providing that the analysis was adjusted for live weight. On heifers, the Pulicaris group comprised 7.5 % of biting midges caught, whereas on hoggets, it comprised 12.7 %.
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References
Allan SA, Day JF, Edman JD (1987) Visual ecology of biting flies. Ann Rev Entomol 32(1):297–314
Augot D, Sauvage F, Jouet D, Simphal E, Veuille M, Couloux A, Kaltenbach ML, Depaquit J (2010) Discrimination of Culicoides obsoletus and Culicoides scoticus, potential bluetongue vectors, by morphometrical and mitochondrial cytochrome oxidase subunit I analysis. Infect Genet Evol 10(5):629–637. doi:10.1016/j.meegid.2010.03.016
Bartsch S, Bauer B, Wiemann A, Clausen P-H, Steuber S (2009) Feeding patterns of biting midges of the Culicoides obsoletus and Culicoides pulicaris groups on selected farms in Brandenburg, Germany. Parasitol Res 105(2):373–380. doi:10.1007/s00436-009-1408-y
Begall S, Červený J, Neef J, Vojtěch O, Burda H (2008) Magnetic alignment in grazing and resting cattle and deer. Proc Natl Acad Sci U S A 105(36):13451–13455. doi:10.1073/pnas.0803650105
Blackwell A, Mordue AJ, Mordue W (1994) Identification of bloodmeals of the Scottish biting midge, Culicoides impunctatus, by indirect enzyme-linked immunosorbent assay (ELISA). Med Vet Entomol 8(1):20–24. doi:10.1111/j.1365-2915.1994.tb00378.x
Boorman J (2011) A short key to British Culicoides of veterinary importance. http://www.culicoides.net/taxonomy/identification-keys/UK01-1. Accessed 03.07.12
Braverman Y (1988) Preferred landing sites of Culicoides species (Diptera: Ceratopogonidae) on a horse in Israel and its relevance to summer seasonal recurrent dermatitis (sweet itch). Equine vet J 20(6):426–429. doi:10.1111/j.2042-3306.1988.tb01566.x
Braverman Y, Rechtman S, Frish A, Braverman R (2003) Dynamics of biting activity of C. imicola (Diptera: Ceratopogonidae) during the year. Israel J Vet Med 58(2–3):46–56
Brugger K, Rubel F (2013) Characterizing the species composition of European Culicoides vectors by means of the Koppen-Geiger climate classification. Parasit Vectors 6(1):333. doi:10.1186/1756-3305-6-333
Carpenter S, Szmaragd C, Barber J, Labuschagne K, Gubbins S, Mellor P (2008) An assessment of Culicoides surveillance techniques in northern Europe: have we underestimated a potential bluetongue virus vector? J Appl Ecol 45(4):1237–1245. doi:10.1111/j.1365-2664.2008.01511.x
Charlwood JD, Lopes J (1980) The age-structure and biting behaviour of Stomoxys calcitrans (L.) (Diptera: Muscidae) from Manaus, Brazil. Bull Ent Res 70(4):549–555. doi:10.1017/S0007485300007847
Clausen PH, Stephan A, Bartsch S, Jandowsky A, Hoffmann-Köhler P, Schein E, Mehlitz D, Bauer B (2009) Seasonal dynamics of biting midges (Diptera: Ceratopogonidae, Culicoides spp.) on dairy farms of Central Germany during the 2007/2008 epidemic of bluetongue. Parasitol Res 105(2):381–386. doi:10.1007/s00436-009-1417-x
Conraths FJ, Eschbaumer M, Freuling C, Gethmann J, Hoffmann B, Kramer M, Probst C, Staubach C, Beer M (2012) Bluetongue disease: an analysis of the epidemic in Germany 2006–2009. In: Mehlhorn H (ed) Arthropods as vectors of emerging diseases. Springer, pp 103-135
De Deken G, Madder M, Deblauwe I, De Clercq K, Fassotte C, Losson B, Haubruge E, De Deken R (2008) Vector monitoring at Belgian outbreak sites during the bluetongue epidemic of 2006. Prev Vet Med 87(1):64–73. doi:10.1016/j.prevetmed.2008.06.006
Doceul V, Lara E, Sailleau C, Belbis G, Richardson J, Breard E, Viarouge C, Dominguez M, Hendrikx P, Calavas D, Desprat A, Languille J, Comtet L, Pourquier P, Eleouet J-F, Delmas B, Marianneau P, Vitour D, Zientara S (2013) Epidemiology, molecular virology and diagnostics of Schmallenberg virus, an emerging orthobunyavirus in Europe. Vet Res 44(1):31. doi:10.1186/1297-9716-44-31
Dyce A (1969) The recognition of nulliparous and parous Culicoides (Diptera: Ceratopogonidae) without dissection. J Aust Entomol 8(1):11–15
Fredeen FJH (1961) A trap for studying the attacking behaviour of black flies, Simulium arcticum Mall. Canad Entomol 93(01):73–78
Garigliany M-M, Bayrou C, Kleijnen D, Cassart D, Jolly S, Linden A, Desmecht D (2012) Schmallenberg virus: A new Shamonda/Sathuperi-like virus on the rise in Europe. Antiviral Res 95(2):82–87. doi:10.1016/j.antiviral.2012.05.014
Garros C, Gardès L, Allène X, Rakotoarivony I, Viennet E, Rossi S, Balenghien T (2011) Adaptation of a species-specific multiplex PCR assay for the identification of blood meal source in Culicoides (Ceratopogonidae: Diptera): applications on Palaearctic biting midge species, vectors of Orbiviruses. Infect Genet Evol 11(5):1103–1110
Garros C, Mathieu B, Balenghien T, Cêtre-Sossah C, Delécolle J-C (2010) Suggesting synonymies? Comments on Kiehl et al. (2009) “The European vectors of Bluetongue virus: are there species complexes, single species or races in Culicoides obsoletus and C. pulicaris detectable by sequencing ITS-1, ITS-2 and 18S-rDNA?”. Parasitol Res 107(3):731–734. doi:10.1007/s00436-010-1921-z
Gerry AC, Monteys VSI, Vidal JOM, Francino O, Mullens BA (2009) Biting rates of Culicoides midges (Diptera: Ceratopogonidae) on sheep in northeastern Spain in relation to midge capture using UV light and carbon dioxide-baited traps. J Med Entomol 46(3):615–24. doi:10.1603/033.046.0329
Gibson G, Torr SJ (1999) Visual and olfactory responses of haematophagous Diptera to host stimuli. Med Vet Entomol 13(1):2–23. doi:10.1046/j.1365-2915.1999.00163.x
Gubbins S, Carpenter S, Baylis M, Wood JLN, Mellor PS (2008) Assessing the risk of bluetongue to UK livestock: uncertainty and sensitivity analyses of a temperature-dependent model for the basic reproduction number. J R Soc Interface 5(20):363–371. doi:10.1098/rsif.2007.1110
Henni LH, Sauvage F, Ninio C, Depaquit J, Augot D (2014) Wing geometry as a tool for discrimination of Obsoletus group (Diptera: Ceratopogonidae: Culicoides) in France. Infect Genet Evol 21(0):110–117
Humphreys JG, Turner EC (1973) Blood-feeding activity of female Culicoides (Diptera: Ceratopogonidae). J Med Entomol 10(1):79–83
Kettle DS (1951) The spatial distribution of Culicoides impunctatus Goet. under woodland and moorland conditions and its flight range through woodland. Bull Ent Res 42(02):239–291
Kiehl E, Walldorf V, Klimpel S, Al-Quraishy S, Mehlhorn H (2009) The European vectors of Bluetongue virus: are there species complexes, single species or races in Culicoides obsoletus and C. pulicaris detectable by sequencing ITS-1, ITS-2 and 18S-rDNA? Parasitol Res 105(2):331–336. doi:10.1007/s00436-009-1414-0
Kirkeby C, Bødker R, Stockmarr A, Lind P, Heegaard PMH (2013) Quantifying dispersal of European Culicoides (Diptera: Ceratopogonidae) vectors between farms using a novel mark-release-recapture technique. PLoS One 8(4):e61269. doi:10.1371/journal.pone.0061269
Lassen S, Nielsen S, Skovgård H, Kristensen M (2011) Molecular identification of bloodmeals from biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasitol Res 108(4):823–829. doi:10.1007/s00436-010-2123-4
Lillie TH, Marquardt WC, Jones RH (1981) The flight range of Culicoides variipennis (Diptera: Ceratopogonidae). Canad Entomol 113(05):419–426
Lo Iacono G, Robin CA, Newton JR, Gubbins S, Wood JLN (2013) Where are the horses? With the sheep or cows? Uncertain host location, vector-feeding preferences and the risk of African horse sickness transmission in Great Britain. J R Soc Interface 10(83):20130194. doi:10.1098/rsif.2013.0194
Logan JG, Cook JI, Mordue AJ, Kline DL (2010) Understanding and exploiting olfaction for the surveillance and control of Culicoides biting midges. In: Takken W, Knols BGJ (eds) Olfaction in vector-host interactions, vol 2 of Ecology and control of vector-borne diseases. Wageningen Academic Publishers, Wageningen, pp 217–246
Mathieu B, Perrin A, Baldet T, Delécolle JC, Albina E, Cêtre-Sossah C (2007) Molecular identification of western European species of Obsoletus complex (Diptera: Ceratopogonidae) by an internal transcribed spacer-1 rDNA multiplex polymerase chain reaction assay. J Med Entomol 44(6):1019–1025
McCall P, Trees A (1993) Onchocerciasis in British cattle: a study of the transmission of Onchocerca sp. in North Wales. J Helminthol 67(2):123–135
Mehlhorn H, Walldorf V, Klimpel S, Schaub G, Kiel E, Focke R, Liebisch G, Liebisch A, Werner D, Bauer C (2009) Bluetongue disease in Germany (2007–2008): monitoring of entomological aspects. Parasitol Res 105(2):313–319. doi:10.1007/s00436-009-1416-y
Meiswinkel R, Baldet T, De Deken R, Takken W, Delecolle JC, Mellor PS (2008) The 2006 outbreak of bluetongue in northern Europe—the entomological perspective. Prev Vet Med 87(1–2):55–63. doi:10.1016/j.prevetmed.2008.06.005
Mellor PS, Pitzolis G (1979) Observations on breeding sites and light trap collections of Culicoides during an outbreak of bluetongue in Cyprus. Bull Ent Res 69(2):229–234. doi:10.1017/S0007485300017697
Mellor PS, Boned J, Hamblin C, Graham S (1990) Isolations of African horse sickness virus from vector insects made during the 1988 epizootic in Spain. Epidemiol Infect 105(2):447–454. doi:10.1017/S0950268800048020
Mellor PS, Boorman J, Baylis M (2000) Culicoides biting midges: their role as arbovirus vectors. Ann Rev Entomol 45(1):307–340
Muñoz-Muñoz F, Talavera S, Carpenter S, Nielsen SA, Werner D, Pagès N (2014) Phenotypic differentiation and phylogenetic signal of wing shape in western European biting midges, Culicoides spp., of the subgenus Avaritia. Med Vet Entomol Epub. doi:10.1111/mve.12042
Nevill EM (1978) The use of cattle to protect sheep from bluetongue infection. J S Afr Vet Assoc 49(2):129–130
Nielsen BO (1971) Some observations on biting midges (Diptera: Ceratopogonidae) attacking grazing cattle in Denmark. Entomol Scand 2(2):94–98
Nielsen SA, Kristensen M (2011) Morphological and molecular identification of species of the Obsoletus group (Diptera: Ceratopogonidae) in Scandinavia. Parasitol Res 109(4):1133–1141. doi:10.1007/s00436-011-2357-9
Nielsen BO, Nielsen SA, Jespersen JB (1988) The fauna of Diptera visiting tethered heifers in Danish pastures. Ent Meddr 56(2):79–88
Ninio C, Augot D, Delecolle JC, Dufour B, Depaquit J (2011) Contribution to the knowledge of Culicoides (Diptera: Ceratopogonidae) host preferences in France. Parasitol Res 108(3):657–663. doi:10.1007/s00436-010-2110-9
Nolan DV, Carpenter S, Barber J, Mellor PS, Dallas JF, Piertney SB (2007) Rapid diagnostic PCR assays for members of the Culicoides obsoletus and Culicoides pulicaris species complexes, implicated vectors of bluetongue virus in Europe. Vet Microbiol 124(1):82–94. doi:10.1016/j.vetmic.2007.03.019
Perrin A, Cetre-Sossah C, Mathieu B, Baldet T, Delecolle JC, Albina E (2006) Phylogenetic analysis of Culicoides species from France based on nuclear ITS1-rDNA sequences. Med Vet Entomol 20(2):219–228. doi:10.1111/j.1365-2915.2006.00616.x
Peterson RD, Meyer HJ (1982) Seasonal activity of male face flies (Diptera: Muscidae) in North Dakota. Environ Entomol 11(4):884–888
Pettersson E, Bensch S, Ander M, Chirico J, Sigvald R, Ignell R (2013) Molecular identification of bloodmeals and species composition in Culicoides biting midges. Med Vet Entomol 27(1):104–112. doi:10.1111/j.1365-2915.2012.01038.x
Saegerman C, Berkvens D, Mellor PS (2008) Bluetongue epidemiology in the European Union. Emerg Infec Dis 14(4):539–544
Santiago-Alarcon D, Havelka P, Schaefer HM, Segelbacher G (2012) Bloodmeal analysis reveals avian P lasmodium infections and broad host preferences of Culicoides (Diptera: Ceratopogonidae) vectors. PLoS One 7(2):e31098. doi:10.1371/journal.pone.0031098
Scheffer EG, Venter GJ, Labuschagne K, Page PC, Mullens BA, MacLachlan NJ, Osterrieder N, Guthrie AJ (2012) Comparison of two trapping methods for Culicoides biting midges and determination of African horse sickness virus prevalence in midge populations at Onderstepoort, South Africa. Vet Parasitol 185(2–4):265–273. doi:10.1016/j.vetpar.2011.09.037
Schmidtmann ET, Jones CJ, Gollands B (1980) Comparative host-seeking activity of Culicoides (Diptera: Ceratopogonidae) attracted to pastured livestock in central New York State, USA. J Med Entomol 17(3):221–231
Szmaragd C, Wilson AJ, Carpenter S, Wood JL, Mellor PS, Gubbins S (2010) The spread of bluetongue virus serotype 8 in Great Britain and its control by vaccination. PLoS One 5(2):e9353. doi:10.1371/journal.pone.0009353
Takken W, Verhulst N, Scholte E, Jacobs F, Jongema Y, van Lammeren R (2008) The phenology and population dynamics of Culicoides spp. in different ecosystems in the Netherlands. Prev Vet Med 87(1–2):41–54. doi:10.1016/j.prevetmed.2008.06.015
Thompson GM, Jess S, Murchie AK (2013) Differential emergence of Culicoides (Diptera: Ceratopogonidae) from on-farm breeding substrates in Northern Ireland. Parasitology 140(06):699–708. doi:10.1017/S0031182012002016
Townley P, Baker K, Quinn P (1984) Preferential landing and engorging sites of Culicoides species landing on a horse in Ireland. Equine vet J 16(2):117–120
van der Rijt R, van den Boom R, Jongema Y, van Oldruitenborgh-Oosterbaan MMS (2008) Culicoides species attracted to horses with and without insect hypersensitivity. Vet J 178(1):91–97. doi:10.1016/j.tvjl.2007.07.005
Velthuis AGJ, Saatkamp HW, Mourits MCM, de Koeijer AA, Elbers ARW (2010) Financial consequences of the Dutch bluetongue serotype 8 epidemics of 2006 and 2007. Prev Vet Med 93(4):294–304. doi:10.1016/j.prevetmed.2009.11.007
Viennet E, Garros C, Lancelot R, Allene X, Gardes L, Rakotoarivony I, Crochet D, Delecolle J-C, Moulia C, Baldet T, Balenghien T (2011) Assessment of vector/host contact: comparison of animal-baited traps and UV-light/suction trap for collecting Culicoides biting midges (Diptera: Ceratopogonidae), vectors of Orbiviruses. Parasit Vectors 4(1):119
Viennet E, Garros C, Gardès L, Rakotoarivony I, Allène X, Lancelot R, Crochet D, Moulia C, Baldet T, Balenghien T (2013) Host preferences of Palaearctic Culicoides biting midges: implications for transmission of orbiviruses. Med Vet Entomol 27(3):255–266. doi:10.1111/j.1365-2915.2012.01042.x
Wilson AJ, Mellor PS (2009) Bluetongue in Europe: past, present and future. Phil Trans R Soc B 364(1530):2669–2681. doi:10.1098/rstb.2009.0091
Acknowledgments
We would like to extend our appreciation to the staff of AFBI Hillsborough for providing the animals and site for this experiment. In particular, we thank Andrew Brown for his helpful assistance and positive attitude. We value the help of Sam Clawson, Ian Rea, Ivan Forsythe and John Anderson in collecting and processing trap samples. An anonymous reviewer corrected terminology and presentation. We thank the Department of Agriculture and Rural Development, Northern Ireland, for funding this research as part of its post-graduate agricultural and food studentship and ongoing vector surveillance programmes.
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All experiments were conducted on a research farm by staff trained and experienced in large-animal handling. There are no conflicts of interest to state.
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Thompson, G.M., Jess, S., Gordon, A.W. et al. Sticky-trapping biting midges (Culicoides spp.) alighting on cattle and sheep: effects of trap colour and evidence for host preference. Parasitol Res 113, 3085–3094 (2014). https://doi.org/10.1007/s00436-014-3974-x
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DOI: https://doi.org/10.1007/s00436-014-3974-x