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Differential emergence of Culicoides (Diptera: Ceratopogonidae) from on-farm breeding substrates in Northern Ireland

Published online by Cambridge University Press:  30 January 2013

GEOFFREY M. THOMPSON ,
STEPHEN JESS  and
ARCHIE K. MURCHIE
GEOFFREY M. THOMPSON*
Affiliation:
Queen's University of Belfast, School of Biological Sciences, BT7 1NN, Northern Ireland Agri-Food and Biosciences Institute, Newforge Lane, Belfast, BT9 5PX, Northern Ireland
STEPHEN JESS
Affiliation:
Agri-Food and Biosciences Institute, Newforge Lane, Belfast, BT9 5PX, Northern Ireland
ARCHIE K. MURCHIE
Affiliation:
Agri-Food and Biosciences Institute, Newforge Lane, Belfast, BT9 5PX, Northern Ireland
*
*Corresponding author: F15, Applied Plant Science & Biometrics Division, Agri-Food and Biosciences Institute, Newforge Lane, Belfast, BT9 5PX, Northern Ireland. Tel: 07854368784. E-mail: Geoffrey.Thompson@afbini.gov.uk
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Summary

Biting midges of the genus Culicoides (Diptera: Ceratopogonidae) are vectors of a number of viral diseases worldwide. Following the unforeseen outbreak of bluetongue in northern Europe (2006–2009) there was a need to clarify on-farm breeding substrates utilized by temperate Culicoides spp. Six substrates (cow dung, cow slurry, horse dung, sheep dung, maize silage and soil) were investigated for Culicoides spp. emergence over a 31-week period. Overall, most Obsoletus group Culicoides emerged from the cow dung and the most Pulicaris group Culicoides emerged from the sheep dung. Furthermore, Culicoides of the Obsoletus group were found to be abundant in cow slurry and sheep dung. Temperature played a significant role in the emergence times of adult Culicoides. The Obsoletus group appear to have undergone 3 generations during the experimental period. The sex ratio of emergent Obsoletus group Culicoides was affected by substrate type, with a greater proportion of males emerging from cow dung and slurry compared with the other substrates.

Keywords

Culicoidesdungphenologysex ratio
Type
Research Article
Information
Parasitology , Volume 140 , Issue 6 , May 2013 , pp. 699 - 708
Copyright
Copyright © Cambridge University Press 2013

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References

REFERENCES

Augot, D., Sauvage, F., Jouet, D., Simphal, E., Veuille, M., Couloux, A., Kaltenbach, M. and Depaquit, J. (2010). Discrimination of Culicoides obsoletus and Culicoides scoticus, potential bluetongue vectors, by morphometrical and mitochondrial cytochrome oxidase subunit I analysis. Infection, Genetics and Evolution 10, 629–637.CrossRefGoogle ScholarPubMed
Baldet, T., Delécolle, J., Cetre-Sossah, C., Mathieu, B., Meiswinkel, R. and Gerbier, G. (2008). Indoor activity of Culicoides associated with livestock in the bluetongue virus (BTV) affected region of northern France during autumn 2006. Preventive Veterinary Medicine 87, 84–97.CrossRefGoogle ScholarPubMed
Baylis, M., Parkin, H., Kreppel, K., Carpenter, S., Mellor, P. and McIntyre, K. (2010). Evaluation of housing as a means to protect cattle from Culicoides biting midges, the vectors of bluetongue virus. Medical and Veterinary Entomology 24, 38–45.CrossRefGoogle ScholarPubMed
Bishop, A. L., McKenzie, H. J., Barchia, I. M. and Harris, A. M. (1996 a). 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.CrossRefGoogle Scholar
Bishop, A. L., McKenzie, H. J., Barchia, I. M., Murison, R. and Spohr, L. J. (1996 b). Positions of juvenile stages of Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae) and of four other flies in bovine dung. Australian Journal of Entomology 35, 209–212.CrossRefGoogle Scholar
Blackwell, A., Mordue, A. J., Young, M. R. and Mordue, W. (1992). Bivoltinism, survival rates and reproductive characteristics of the Scottish biting midge, Culicoides impunctatus (Diptera: Ceratopogonidae) in Scotland. Bulletin of Entomological Research 82, 299–306.CrossRefGoogle Scholar
Boorman, J. (2011). A short key to British Culicoides of veterinary importance. Culicoides.NET, http://www.culicoides.net/taxonomy/identification-keys/UK01-1.Google Scholar
Boorman, J. and Goddard, P. (1970 a). Culicoides Latreille (Diptera, Ceratopogonidae) from Pirbright, Surrey. Entomologist's Gazette 21, 205–216.Google Scholar
Boorman, J. and Goddard, P. (1970 b). Observations on the biology of Culicoides impunctatus Goetgh. (Dipt., Ceratopogonidae) in southern England. Bulletin of Entomological Research 60, 189–198.CrossRefGoogle ScholarPubMed
Braverman, Y., Galun, R. and Ziv, M. (1974). Breeding sites of some Culicoides species (Diptera, Ceratopogonidae) in Israel. Mosquito News, 34, 303–308.Google Scholar
Bull, J. J. (1983). Evolution of Sex Determining Mechanisms. The Benjamin/Cummings Publishing Company, Menlo Park, CA, USA.Google Scholar
Campbell, J. A. and Pelham-Clinton, E. (1960). A taxonomic review of the British species of “Culicoides” Latreille (Diptera, Ceratopogonidae). Proceedings of the Royal Society of Edinburgh, Series B (Biology) 67, 181–302.Google Scholar
Campbell, M. M. and Kettle, D. S. (1976). Number of adult Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae) emerging from bovine dung exposed under different conditions in field. Australian Journal of Zoology 24, 75–85.CrossRefGoogle Scholar
Cannon, L. and Reye, E. J. (1966). A larval habitat of the biting midge Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae). Australian Journal of Entomology 5, 7–9.CrossRefGoogle Scholar
Charnov, E. L. (1982). The Theory of Sex Allocation. Princeton University Press, Princeton, NJ, USA.Google ScholarPubMed
Clausen, P. H., Stephan, A., Bartsch, S., Jandowsky, A., Hoffmann-Köhler, P., Schein, E., Mehlitz, D. and 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. Parasitology Research 105, 381–386.CrossRefGoogle ScholarPubMed
Conte, A., Goffredo, M., Ippoliti, C. and Meiswinkel, R. (2007). Influence of biotic and abiotic factors on the distribution and abundance of Culicoides imicola and the Obsoletus Complex in Italy. Veterinary Parasitology 150, 333–344.CrossRefGoogle ScholarPubMed
Cruickshank, J. G. (1997). Soil and Environment: Northern Ireland. DANI/QUB, Belfast, Northern Ireland.Google Scholar
De Deken, G., Madder, M., Deblauwe, I., De Clercq, K., Fassotte, C., Losson, B., Haubruge, E. and De Deken, R. (2008). Vector monitoring at Belgian outbreak sites during the bluetongue epidemic of 2006. Preventive Veterinary Medicine 87, 64–73.CrossRefGoogle ScholarPubMed
Department for Environment Food and Rural Affairs (2012). Schmallenberg Virus. Animal Health and Veterinary Laboratories Agency. http://www.defra.gov.uk/ahvla/files/sci_schmallenberg.pdf.Google Scholar
Department of Agriculture and Rural Development (2011). Nitrates Action Programme 2011–2014 and Phosphorus Regulations Guidance Booklet. http://www.dardni.gov.uk/ruralni/nitrates_action_programme_2011-2014_guidance_booklet.pdf.Google Scholar
Dorchin, N. and Freidberg, A. (2004). Sex ratio in relation to season and host plant quality in a monogenous stem-galling midge (Diptera: Cecidomyiidae). Ecological Entomology 29, 677–684.CrossRefGoogle Scholar
Dyce, A. (1969). The recognition of nulliparous and parous Culicoides (Diptera: Ceratopogonidae) without dissection. Australian Journal of Entomology 8, 11–15.CrossRefGoogle Scholar
Dyce, A. and Marshall, B. (1989). An early record of Culicoides species (Diptera: Ceratopogonidae) developing in the dung of game animals in southern Africa. Onderstepoort Journal of Veterinary Research 56, 85.Google Scholar
Dzhafarov, S. M. (1964). Blood-sucking Midges (Diptera, Heleidae) of the Transcaucasus, Akademija Nauk Azerbaidzanskoi SSR, Instituta Zoologicheskiy.Google Scholar
Edwards, P. B. (1982). Laboratory observations on the biology and life cycle of the Australian biting midge Culicoides subimmaculatus (Diptera, Ceratopogonidae). Journal of Medical Entomology 19, 545–552.CrossRefGoogle ScholarPubMed
European Commission (1991). Council Directive 91/676/EEC of 12 December 1991 concerning the protection of waters against pollution caused by nitrates from agricultural sources. http://ec.europa.eu/environment/water/water-nitrates/directiv.html.Google Scholar
European Food Safety Authority (2007). Scientific Opinion of the Scientific Panel on Animal Health and Welfare on the EFSA Selfmandate on bluetongue and occurrence. The EFSA Journal 408, 1–20.Google Scholar
Floate, K. D., Colwell, D. D. and Fox, A. S. (2002). Reductions of non-pest insects in dung of cattle treated with endectocides: a comparison of four products. Bulletin of Entomological Research 92, 471–481.CrossRefGoogle ScholarPubMed
Floate, K. D., Spooner, R. W. and Colwell, D. D. (2001). Larvicidal activity of endectocides against pest flies in the dung of treated cattle. Medical and Veterinary Entomology 15, 117–120.CrossRefGoogle Scholar
Fort Dodge Animal Health (1997). Environmental Assessment – Cydectin moxidectin 0·5% Pour-On for Cattle. http://www.fda.gov/downloads/AnimalVeterinary/DevelopmentApprovalProcess/EnvironmentalAssessments/UCM072383.pdf.Google Scholar
Holmes, P. R. and Boorman, J. P. T. (1987). Light and suction trap catches of Culicoides midges on southern England. Medical and Veterinary Entomology 1, 349–359.CrossRefGoogle ScholarPubMed
Kettle, D. and Lawson, J. (1952). The early stages of British biting midges Culicoides Latreille (Diptera: Ceratopogonidae) and allied genera. Bulletin of Entomological Research 43, 421–467.CrossRefGoogle Scholar
King, B. H. (1993). Sex ratio manipulation by parasitoid wasps. In Evolution and Diversity of Sex Ratio in Insects and Mites (ed. Wrensch, D. L. and Ebbert, M. A.), pp. 418–441. Chapman & Hall, New York, USA.CrossRefGoogle Scholar
Mathieu, B., Perrin, A., Baldet, T., Delécolle, J. C., Albina, E. and 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. Journal of Medical Entomology 44, 1019–1025.CrossRefGoogle ScholarPubMed
McCarthy, T. K., Bateman, A., Nowak, D., Higgins, T., Geraghty, F., Sheehy, E., Kirrane, A., Moran, P. and Lawless, A. (2008). BTV Vector Surveillance 2007–2008, 1st Annual Technical Report. http://www.agriculture.gov.ie/media/migration/animalhealthwelfare/diseasecontrols/bluetonguedisease/BTV_Vector_Surveillance_2007.pdf.Google Scholar
Meiswinkel, R. (1989). Afrotropical Culicoides: a redescription of C. (Avaritia) imicola Kieffer, 1913 (Diptera: Ceratopogonidae) with description of the closely allied C.(A.) bolitinos sp. nov. reared from the dung of the African buffalo, blue wildebeest and cattle in South Africa. Onderstepoort Journal of Veterinary Research 56, 23.Google Scholar
Meiswinkel, R., Baldet, T., De Deken, R., Takken, W., Delecolle, J. C. and Mellor, P. S. (2008 a). The 2006 outbreak of bluetongue in northern Europe–the entomological perspective. Preventive Veterinary Medicine 87, 55–63.CrossRefGoogle ScholarPubMed
Meiswinkel, R., Goffredo, M., Dijkstra, E., Van Der Ven, I., Baldet, T. and Elbers, A. (2008 b). Endophily in Culicoides associated with BTV-infected cattle in the province of Limburg, south-eastern Netherlands, 2006. Preventive Veterinary Medicine 87, 182–195.CrossRefGoogle ScholarPubMed
Mellor, P. S. (2000). Replication of arboviruses in insect vectors. Journal of Comparative Pathology 123, 231–247.CrossRefGoogle ScholarPubMed
Mellor, P. S. and Pitzolis, G. (1979). Observations on breeding sites and light trap collections of Culicoides during an outbreak of bluetongue in Cyprus. Bulletin of Entomological Research 69, 229–234.CrossRefGoogle Scholar
Mirzaeva, A. G. and Glushchenko, N. P. (1976). Biogeographical-ecological groupings of blood-sucking ceratopogonids (Diptera, Ceratopogonidae) of Siberia. Trudy Biologicheskogo Instituta, Sibirskoe Otdelenie, Akademiya Nauk SSSR 18, 277–290.Google Scholar
Mullens, B. A. and Rutz, D. A. (1983). Development of immature Culicoides variipennis (Diptera, Ceratopogonidae) at constant laboratory temperatures. Annals of the Entomological Society of America 76, 747–751.CrossRefGoogle Scholar
Mullens, B. A., Sarto i Monteys, V. and Przhiboro, A. A. (2008). Mermithid parasitism in Ceratopogonidae: a literature review and critical assessment of host impact and potential for biological control of Culicoides. Russian Entomological Journal 17, 87–113.Google Scholar
Nevill, H., Venter, G., Meiswinkel, R. and Nevill, E. (2010). Comparative descriptions of the pupae of five species of the Culicoides imicola complex (Diptera, Ceratopogonidae) from South Africa. Onderstepoort Journal of Veterinary Research 74, 97–114.Google Scholar
Ninio, C., Augot, D., Dufour, B. and Depaquit, J. (2011). Emergence of Culicoides obsoletus from indoor and outdoor breeding sites. Veterinary Parasitology 183, 125.CrossRefGoogle ScholarPubMed
Nolan, D. V., Carpenter, S., Barber, J., Mellor, P. S., Dallas, J. F. and Piertney, S. B. (2007). Rapid diagnostic PCR assays for members of the Culicoides obsoletus and Culicoides pulicaris species complexes, implicated vectors of bluetongue virus in Europe. Veterinary Microbiology 124, 82–94.CrossRefGoogle ScholarPubMed
Nunamaker, R. A., Brown, S. E., McHolland, L. E., Tabachnick, W. J. and Knudson, D. L. (1999). First-generation physical map of the Culicoides variipennis (Diptera: Ceratopogonidae) genome. Journal of Medical Entomology 36, 771–775.CrossRefGoogle ScholarPubMed
Ode, P. J. and Heinz, K. M. (2002). Host-size-dependent sex ratio theory and improving mass-reared parasitoid sex ratios. Biological Control 24, 31–41.CrossRefGoogle Scholar
Perrin, A., Cetre-Sossah, C., Mathieu, B., Baldet, T., Delecolle, J. C. and Albina, E. (2006). Phylogenetic analysis of Culicoides species from France based on nuclear ITS1-rDNA sequences. Medical and Veterinary Entomology 20, 219–228.CrossRefGoogle ScholarPubMed
Sanders, C. J., Shortall, C. R., Gubbins, S., Burgin, L., Gloster, J., Harrington, R., Reynolds, D. R., Mellor, P. S. and Carpenter, S. (2011). Influence of season and meteorological parameters on flight activity of Culicoides biting midges. Journal of Applied Ecology 48, 1355–1364.CrossRefGoogle Scholar
Takken, W., Verhulst, N., Scholte, E., Jacobs, F., Jongema, Y. and van Lammeren, R. (2008). The phenology and population dynamics of Culicoides spp. in different ecosystems in the Netherlands. Preventive Veterinary Medicine 87, 41–54.CrossRefGoogle ScholarPubMed
Thompson, G. M., Brunt, A., Loye, S., Jess, S. and Murchie, A. K. (in press). A low-cost bucket trap for newly emerged insects. Irish Naturalists' Journal.Google Scholar
Thompson, G. M., Murchie, A. K. and Jess, S. (2011). A review of bluetongue disease and its implications for Ireland. Tearmann: Irish Journal of Agri-Environmental Research, 8, 45–58.Google Scholar
Trukhan, M. N. (1975). The effect of drainage improvement on the fauna and abundance of blood-sucking Ceratopogonidae. Problems of Parasitology. Proceedings of the VIIIth Scientific Conference of Parasitologists of the Ukrainian SSR. Volume 2.: Problemy Parazitologii. Materialy VIII Nauchnoi Konferentsii Parazitologov USSR. Chast' 2, 218–219.Google Scholar
Vaughan, J. A. and Turner, E. C. (1987). Development of immature Culicoides variipennis (Diptera, Ceratopogonidae) from Saltville, Virginia, at constant laboratory temperatures. Journal of Medical Entomology 24, 390–395.CrossRefGoogle Scholar
Wittmann, E. J. and Baylis, M. (2000). Climate change: effects on Culicoides-transmitted viruses and implications for the UK. Veterinary Journal 160, 107–117.CrossRefGoogle ScholarPubMed
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. and Defrance, T. (2008). Breeding sites of bluetongue vectors in northern Europe. Veterinary Record, 162, 131–131.CrossRefGoogle ScholarPubMed
Zimmer, J.-Y., Saegerman, C., Losson, B. and Haubruge, E. (2010). Breeding sites of bluetongue virus vectors, Belgium. Emerging Infectious Diseases 16, 575–576.CrossRefGoogle ScholarPubMed