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A multiple basis for insecticide resistance in a strain of Culex quinquefasciatus (Diptera: Culicidae) from Muheza, Tanzania, studied as resistance declined

Published online by Cambridge University Press:  10 July 2009

A. Khayrandish
Affiliation:
Department of Environmental Biology, University of Manchester, UK
R.J. Wood*
Affiliation:
Department of Environmental Biology, University of Manchester, UK
*
Dr Roger J. Wood, Manchester University, Department of Environmental Biology, Williamson Building, Manchester M13 9PL, UK

Abstract

Evidence from observing resistance in decline in fourth instar larvae of the multiple resistant MUHEZA strain of Culex quinquefasciatus Say from Tanzania (MUHEZA), showed that the major mechanisms for chlorpyrifos and propoxur resistance were different. Resistance to chlorpyrifos declined more than 400-fold (from an initial resistance ratio (RR) of 14285) while resistance to propoxur remained stable for at least 30 generations of laboratory culture. Significant synergism was found between propoxur and piperonyl butoxide (PB), propoxur and s,s,s-tributyl trithiophosphate (DEF), and permethrin and PB, but antagonism occurred between chlorpyrifos and PB, and no synergism between chlorpyrifos and DEF. Nine esterase isozymes active against naphthyl acetates on polyacrylamide gel electrophoresis (PAGE), were identified, four (A2, A3, B2, B3) showing polymorphism in activity, with very intense expression at one or other position in more than 32% of larvae, and null expression in less than 30%. The frequency of intense bands and of nulls both declined as resistance declined. A selected substrain (MUHEZA-fb), breeding true for A2, A3, B2 and B3 at the standard level of activity, showed almost stable chlorpyrifos resistance (RR=1428–1785) for approximately 35 generations. In mass larval assays of in vitro sensitivity of acetylcholinesterase (AChE) to propoxur, the I50 in MUHEZA was 950-fold greater than in a reverted resistant strain (RANGOON). Single larval assays indicated an AChE resistance allele (AceR) at frequency 0.43. PAGE of AChE revealed nine isozymes in MUHEZA and five in RANGOON, three of which were in common. It is concluded that propoxur resistance was due principally to AceR with a minor influence from oxidases and non-specific esterases, while chlorpyrifos resistance was due to an interaction between AceR and non-specific esterases, the latter exerting the dominant effect.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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References

Bisset, J. A., Rodrigues, M. M., Diaz, C., Ortiz, E., Marquetti, M. C. and Hemingway, J.. (1990) The mechanisms of organophosphate and carbamate resistance in Culex quinquefasciatus (Diptera: Culicidae) from Cuba. Bulletin of Entomological Research 80, 245250.CrossRefGoogle Scholar
Bonning, B. C., Hemingway, J., Romi, R. and Majori, G.. (1991) Interaction of insecticide resistance genes in field populations of Culex pipiens (Diptera: Culicidae) from Italy in response to changing insecticide selection pressure. Bulletin of Entomological Research 81, 510.CrossRefGoogle Scholar
Brown, A. W. A.. (1961) Negatively correlated insecticide resistance. Bulletin of the Entomological Society of America 7, 619.CrossRefGoogle Scholar
Curtis, C. F.. & Pasteur, N.. (1981) Organophosphate resistance in vector populations of the complex of Culex pipiens L. Bulletin of Entomological Research 71, 153161.CrossRefGoogle Scholar
Davis, G. A.. (1968) Metabolic behaviour of isozymes of acetylcholinesterase. Nature 220, 227280.CrossRefGoogle ScholarPubMed
Edwards, J. S. & Gomez, D.. (1966). Bound acetylcholinesterase in central nervous system of Acheta domesticus (L.) (Orthoptera). Insect Physiology 12, 10611066.CrossRefGoogle ScholarPubMed
Eldefrawi, M.E., Tripathi, R.K.. & O'Brien, R.D.. (1970). Acetylcholinesterase isozymes from the housefly brain. Biochemica Biophysica Acta 212, 308314.CrossRefGoogle ScholarPubMed
Hassall, K.A.. (1990). The biochemistry and use of pesticides. 2nd edn. 536 pp. London, MacMillian.CrossRefGoogle Scholar
Heilbronn, E.. (1962). Purification of cholinesterase from horse serum. Biochemica Biophysica Acta 58, 222230.CrossRefGoogle ScholarPubMed
Hemingway, J., Smith, C., Jayawardena, K.G.I.. & Herath, P.R.J.. (1986). Field and laboratory detection of the altered acetylcholinesterase resistance genes which confer organophosphate and carbamate resistance in mosquitoes (Diptera: Culicidae). Bulletin of Entomological Research 76, 559565.CrossRefGoogle Scholar
Jiang, Jialiang.; Chen, Quiaoyun Hou.; Negjun; Zhang, Zhaoyuan.. (1984). Comparison of glutathione and glutathione-S-transferase in dipterex-resistant and susceptibleCulex pipiens pallens Coq. Kunchong Xuebao 27, 248253.Google Scholar
Khayrandish, A.. (1991). Genetical and biochemical investigation of multiple insecticide resistance in mosquitoes of the Culex pipiens complex (Diptera: Culicidae). PhD Thesis University of Manchester, UK.Google Scholar
Khayrandish, A., & Wood, R.J.. (1993). Organophosphorus insecticide resistance in a new strain of Culex quinquefasciatus (Diptera: Culicidae) from Tanga, Tanzania. Bulletin of Entomological Research 83, 6774.CrossRefGoogle Scholar
Knowles, C.D. & Arurkar, S.K.. (1969). Acetylcholinesterase polymorphism in the face fly (Diptera: Muscidae). Journal of the Kansas Entomology Society 42, 3945.Google Scholar
Litchfield, J.J.. & Wilcoxon, F.. (1949). A simplified-method of evaluating dose effect experiments. Journal of Pharmacological and Experimental Therapeutics 96, 99113.Google ScholarPubMed
Magnin, M., Marboutin, E. & Pasteur, N.. (1988). Insecticide resistance in Culex quinquefasciatus (Diptera: Culicidae) in West Africa. Journal of Medical Entomology 25, 99104.CrossRefGoogle ScholarPubMed
Main, A.R.. (1969). Kinetic evidence of multiple reversible cholinesterases based on inhibition by organophosphates. Journal of Biological Chemistry 244, 829840.CrossRefGoogle ScholarPubMed
Oppenoorth, F.J.. (1985). Biochemistry and genetics of insecticide resistance. pp. 731773 in Kerkut, G.A.. & Gilbert, L.I.. (eds) Comprehensive insect physiology biochemistry and pharmacology. Insect Control 12, Oxford, Pergamon Press.Google Scholar
Priester, T.M.. & Georghiou, G.P.. (1979) Inheritance of resistance to permethrin in Culex pipens quinquefasciatus. Journal of Economic Entomology 72, 124127.CrossRefGoogle Scholar
Priester, T.M.. & Georghiou, G.P.. (1980). Penetration of permethrin and knockdown in larvae of pyrethroid-resistant and susceptible strains of southern house mosquito. Journal of Economic Entomology 73, 165167.CrossRefGoogle Scholar
Qiaoyun, Chen., Jiang, Kia-liang., Huang Gang-Tang, Zhen-hua., Liu, Wei-de. (1980) Mechanism of resistance to organophosphate in Culex pipiens pallens. From symposium on Pesticides and environment, Academica Sinica, Shanghai, 11 1980.Google Scholar
Quenouille, M.H.. (1950) Introductory statistics. 248 pp. London, Pergamon press.Google Scholar
Ranasinghe, L.E. & Georghiou, G.P.. (1979). Comparative modification of insecticide resistance in Culex pipiens fatigans Wied. by selection with temephos/synergist combination. Pesticide Science 10, 502508.CrossRefGoogle Scholar
Raymond, M., Pasteur, N., Fournier, D., Cuany, A., Bergè, J. & Magnin, M.. (1985) Le gène d'une acetylcholinesterase insensible aux propoxur determine la résistance du Culex pipiens L. a cet insecticide. Comptes Rendus Academie des Sciences Paris Ser 3, 509512.Google Scholar
Raymond, M., Pasteur, N., Fournier, D., Bride, J.M., Cuany, A., Bergé, J. & Magnin, M.. (1986) Identification of resistance mechanisms in Culex pipiens (Diptera: Culicidae) from southern France: insensitive acetylcholinesterase and detoxifying esterase. Journal of Economic Entomology 79, 14521458.CrossRefGoogle Scholar
Shrivastava, S.P., Georghiou, G.P., Metcalf, R.L. & Fukuto, T.R.. (1970) Carbamate resistance in mosquitoes: the metabolism of propoxur by susceptible and resistant larvae of Culex pipiens fatigans. Bulletin of the World Health Organization 42, 931942.Google Scholar
Tang, Z.H. & Li, Y.G.. (1984) Further studies on effect of some synergists on OP-resistant mosquito (Culex pipiens pallens Coq.). Contributions of the Shanghai Institute of Entomology 4, 121126.Google Scholar
Tang, Z.H. & Wood, R.J.. (1986) Comparative study of resistance to organophosphate and carbamate insecticides in four strains of the Culex pipiens L. complex (Diptera: Culicidae). Bulletin of Entomological Research 76, 505511.CrossRefGoogle Scholar
Tang, Z.H., Wood, R.J. & Cammack, S.L.. (1990) Acetylcholinesterase activity in organophosphorus and carbamate resistant and susceptible strain of the Culex pipiens complex. Pesticide Biochemistry and Physiology 37, 192199.CrossRefGoogle Scholar
White, G.B.. (1971) The present importance of domestic mosquitoes (Culex pipiens fatigans) in East Africa and recent steps towards their control. East African Medical Journal 48, 266274.Google ScholarPubMed
Wood, R.J., Pasteur, N. & Sinègre, G.. (1984) Carbamate and organophosphate resistance in Culex pipiens L. (Diptera: Culicidae) in southern France and the significance of Est-3A. Bulletin of Entomological Research 74, 677687.CrossRefGoogle Scholar
WHO (1975) Instructions for determining the susceptibility or resistance of mosquito larvae to insecticides. World Health Organization unpublished document WHO/VBC/75.583.Google Scholar