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Effect of temperature on survival and rate of virogenesis of African horse sickness virus in Culicoides variipennis sonorensis (Diptera: Ceratopogonidae) and its significance in relation to the epidemiology of the disease

  • Martin P. Wellby (a1), Matthew Baylis (a1), Peter Rawlings (a1) and Philip S. Mellor (a1)

Culicoides variipennis sonorensis Wirth & Jones and C. nubeculosus (Meigen) were orally infected with African horse sickness virus (AHSV) type 9 and subsequently incubated at 10, 15, 20 and 25°C (R.H. 80%±10%). A time course of infection rates and virus titres was recorded by assaying flies individually or in pools, and survival rates of flies were also estimated. Survival rates at 10, 15 and 20°C were very similar and 80–90% of flies remained alive after 14 days; at 25°C after the same period survival was reduced to 40%. None of the C. nubeculosus became persistently infected with AHSV, but the virus took longer to clear as the incubation temperature dropped. At temperatures of 10, 15, 20 and 25°C virus was undetectable on days 12, 8, 5, and 4 days post infection (dpi), respectively. In C. v. sonorensis both the infection rate and rate of virogenesis were related to temperature. At 25°C a maximum mean titre of 104.3 TCID50/fly was reached by 9 dpi and the infection rate remained between 60 and 80%. At 20°C virogenesis was slower and a maximum mean titre of 104.3 TCID50/fly was reached only after 23 days; the infection rate was also reduced to 50–70%. At 15°C there was an overall decline in virus titre with time, although between 12 and 15 dpi some pools of flies contained 103.0–104.0 TCID50/fly, demonstrating that virogenesis can occur. The infection rate at this temperature decreased dramatically to 0–15% after 9 dpi. At 10°C there was no detectable virogenesis and all pools tested at 13 dpi were negative. The apparent infection rate dropped to 0–5% between 13 and 35 days post infection. However, when surviving flies were then returned to 25 °C for 3 days the infection rate increased to 15.5%. It therefore appears that at low temperatures the virus does not replicate but infectious virus may persist at a level below that detectable by the usual assay systems. The implications of these findings for the epidemiology of AHS are discussed.

Corresponding author
Institute for Animal Health, Ash Road, Pirbright, Woking, Surrey GU24 ONF, UK.
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Bellamy, R.E., Reeves, W.C. & Scrivani, R.P. (1968) Experimental cyclic transmission of St. Louis encephalitis virus in chickens and Culex mosquitoes through a year. American Journal of Epidemiology 87, 484495.
Boorman, J. (1974) The maintenance of laboratory colonies of Culicoides variipennis (Coq.), C. nubeculosus (Mg.) and C. riethi Kieff. (Diptera: Ceratopogonidae). Bulletin of Entomological Research 64, 371377.
Boorman, J., Mellor, P.S., Penn, M. & Jennings, M. (1975) The growth of African horse sickness virus in embryonating hen eggs and the transmission of virus by Culicoides variipennis Coq. (Diptera, Ceratopogonidae). Archives of Virology 47, 343349.
Capela, R., Sousa, C., Pena, I. & Caeiro, V. (1993) Preliminary note on the distribution and ecology of Culicoides imicola in Portugal. Medical and Veterinary Entomology 7, 2326.
Cornel, A.J., Jupp, P.G. & Blackburn, N.K. (1993) Environmental temperature on the vector competence of Culex univittatus (Diptera: Culicidae) for West Nile virus. Journal of Medical Entomology 30, 449456.
Foster, N.M., Jones, R.H. & McCrory, B.R. (1963) Preliminary investigations on insect transmission of bluetongue virus in sheep. American Journal of Veterinary Research 24, 11951199.
Fu, H. (1996) Mechanisms controlling infection of Culicoides biting midges with bluetongue virus. PhD thesis submitted to University of Hertfordshire.
Hamblin, C., Mertens, P.P.C., Mellor, P.S., Burroughs, J.N. & Crowther, J.R. (1991) A serogroup specific enzyme linked immunosorbant assay for the detection and identification of African horse sickness viruses. Journal of Virological Methods 31, 285292.
Hunt, G.J., Tabachnick, W.J. & McKinnon, C.N. (1989) Environmental factors affecting mortality of adult Culicoides variipennis (Diptera: Ceratopogonidae) in the laboratory. Journal of the American Mosquito Control Association 5, 387391.
Jupp, P.G. (1974) Laboratory studies on the transmission of West Nile virus by Culex univittatus Theobald; factors influencing the transmission rate. Journal of Medical Entomology 11, 455458.
Kramer, L.D., Hardy, J.L. & Presser, S.B. (1983) Effect of temperature of extrinsic incubation on the vector competence of Culex tarsalis for Western equine encephalomyelitis virus. American Journal of Tropical Medicine and Hygiene 32, 130139.
Lundström, J.O., Turell, M.J. & Niklasson, B. (1990) Effect of environmental temperature on the vector competence of Culex pipiens and Cx. torrentium for Ockelbo virus. American Journal of Tropical Medicine and Hygiene 43, 534542.
Mellor, P.S. (1971) A membrane feeding technique for infection of Culicoides nubeculosus Mg. and Culicoides variipennis sonorensis Coq. with Onchocerca cervicalis Rail. and Henry. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 199201.
Mellor, P.S. (1993) African horse sickness: transmission and epidemiology. Veterinary Research 24, 199212.
Mellor, P.S. (1994) Epizootiology and vectors of African horse sickness virus. Comparative Immunology, Microbiology and Infectious Diseases 17, 287296.
Mellor, P.S., Boorman, J. & Loke, R. (1974) The multiplication of Main Drain virus in two species of Culicoides (Diptera: Ceratopogonidae). Archiv für die Gesamte Virusforschung 46, 105110.
Mellor, P.S., Boorman, J. & Jennings, M. (1975) The multiplication of African horse sickness virus in two species of Culicoides (Diptera, Ceratopogonidae). Archives of Virology 47, 351356.
Mellor, P.S., Boorman, J.P.T., Wilkinson, P.J. & Martinez-Gomez, F. (1983) Potential vectors of bluetongue and African horse sickness viruses in Spain. Veterinary Record 112, 229230.
Mertens, P.P.C., Burroughs, J.N., Walton, A., Wellby, M.P., Fu, H., O'Hara, R.S. & Mellor, P.S. (1996) Enhanced infectivity of modified bluetongue virus particles for 2 Culicoides vector species, and for 2 insect cell lines. Virology 217, 582593.
Mullens, B.A. & Holbrook, F.R. (1991) Temperature effects on the gonotrophic cycle of Culicoides variipennis (Diptera: Ceratopogonidae). Journal of the American Mosquito Control Association 7, 588591.
Mullens, B.A., Tabachnick, W.J., Holbrook, F.R. & Thompson, L.H. (1995) Effects of temperature on virogenesis of bluetongue virus serotype 11 in Culicoides variipennis sonorensis. Medical and Veterinary Entomology 9, 7176.
Price, D.A. & Hardy, W.T. (1954) Isolation of bluetongue virus from Texas sheep - Culicoides shown to be a vector. Journal of the American Veterinary Medical Association 124, 255258.
Rawlings, P. & Mellor, P.S. (1994) African horse sickness and the overwintering of Culicoides spp. in the Iberian peninsula. Revue Scientifique et Technique de l'Office International des Epizooties 13, 753761.
Rosen, L. (1987) Overwintering mechanisms of mosquito-borne arboviruses in template climates. American Journal of Tropical Medicine and Hygiene 37 (3), 69s76s.
Takahashi, M. (1976) The effect of environmental and physiological conditions of Culex tritaeniorhynchus on the pattern of transmission of Japanese encephalitis virus. Journal of Medical Entomology 13, 275284.
Turell, M.J., Rossi, C.A. & Bailey, C.L. (1985) Effect of extrinsic incubation temperature on the ability of Aedes taeniorhynchus and Culex pipiens to transmit Rift Valley fever virus. American Journal of Tropical Medicine and Hygiene 34, 12111218.
Whitaker, A.M. (1972) Application of cell culture to virology. pp. 73110 in Whitaker, A.M. (Ed.) Tissue and cell culture. Bailliere Tindall.
Zar, J.H. (1984) Biostatistical analysis, 2nd edn.London, Prentice-Hall International.
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Bulletin of Entomological Research
  • ISSN: 0007-4853
  • EISSN: 1475-2670
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