Investigation of Susceptibility Levels of Culex pipiens L. (Diptera: Culicidae) Populations to Synthetic Pyrethroids in Antalya Province of Turkey

  • Önder Ser Malaria Control Unit, Antalya Provincial Directorate of Health, Antalya, Turkey
  • Huseyin Cetin Department of Biology, Faculty of Science, Akdeniz University, Antalya, Turkey
Keywords: Antalya, Culex pipiens, Mosquito, Resistance, Synthetic pyrethroid


Background: Culex pipiens L. (Diptera: Culicidae) is an important vector of several pathogens. This mosquito is widely distributed throughout the world. We aimed to determine the susceptibility levels of Cx. pipiens populations to some synthetic pyrethroid insecticides in Antalya, Turkey.Methods: The immature stages of mosquitoes were collected from eight locations in Alanya, Döşemealtı, Kemer, Kumluca, and Manavgat districts of Antalya between Apr and Oct of 2017. Adult susceptibility tests were carried out according to a modified version of the Centers for Disease Control and Prevention bottle bioassay. In the tests, the World Health Organization recommended diagnostic doses; permethrin (0.75%), etofenprox (0.5%), deltamethrin (0.05%) and lambda-cyhalothrin (0.05%) were used.Results: As a result of the susceptibility tests, deltamethrin was the least effective insecticide and it caused 58.78–97.56% mortalities on Cx. pipiens populations while permethrin was the most effective substance that caused 100% mortality on all populations. While all of the tested populations were found susceptible to permethrin, and possible resistant or resistant to deltamethrin. Etofenprox and lambda-cyhalothrin led to 91.54–100% and 93.1–100% mortali­ties, respectively.Conclusion: The possible resistance or resistance to deltamethrin in all the areas is caused by the widespread use of this chemical against pests in agriculture and public health applications for long-term. Moreover, a concordance was found between resistance levels and the intensity of pesticide application in agriculture and public health, and organic and chemical pollution levels in the sampled habitats.


Oter K, Tuzer E (2014) Composition of mosquito species (Diptera: Culicidae) in Istanbul. J Fac Vet Med Istanbul Univ. 40(2): 249-259.

Ser O, Cetin H (2015) Toxicity of mosquito larvicides on non-target mosquito predator insect, backswimmer (Notonecta sp.). Fresen Environ Bull. 24(1): 311-316.

Akiner MM, Simsek FM, Caglar SS (2009) Insecticide resistance of Culex pipiens (Diptera: Culicidae) in Turkey. J Pestic Sci. 34(4): 259-264.

Taskin BG, Dogaroglu T, Kilic S, Dogac E, Taskin V (2016) Seasonal dynamics of insecticide resistance, multiple resistance, and morphometric variation in field populations of Culex pipiens. Pestic Biochem Physiol. 129: 14–27.

Aldemir A, Bosgelmez A (2006) Population dynamics of adults and immature stages of mosquitoes (Diptera:Culicidae) in Gölbaşı district, Ankara. Turk J Zool. 30: 9-17.

Simsek FM (2006) Seasonal frequency and relative density of larval populations of mosquito species (Diptera: Culicidae) in Şanlıurfa province, Turkey. Turk J Zool. 30: 383-392.

Biskin Z, Inci A, Yildirim A, Duzlu O (2010) The prevalence of mosquito (Diptera: Culicidae) species around Felahiye district of Kayseri. Erciyes University Journal of Health Sciences. 19(2): 133-139.

Muslu H, Kurt O, Ozbilgin A (2011) Evaluation of mosquito species (Diptera: Culicidae) identified in Manisa province according to their breeding sites and seasonal differences. Turk J Parasitol. 35: 100-104.

Alten B, Bellini R, Caglar SS, Simsek FM, Kaynas S (2000) Species composition and seasonal dynamics of mosquitoes in the Belek region of Turkey. J Vector Ecol. 25(2): 146-154.

Cetin H, Yanikoglu A (2004) Mosquito (Diptera: Culicidae) species, their breeding sites and some biological aspects of dominant species Culex pipiens, L. in Antalya, Turkey. Turk entomol derg-Tu. 28(4): 283-294.

Akiner MM, Eksi E (2015) Evaluation of insecticide resistance and biochemical mechanisms of Culex pipiens L. in four localities of east and middle mediterranean basin in Turkey. Int J Mosq Res. 2(3): 39-44.

David J-P, Ismail HM, Chandor-Proust A, Paine MJI (2013) Role of cytochrome P450s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Phil Trans R Soc B. 368: 20120429.

Liu N (2015) Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol. 7(60): 537-559.

Ser O, Cetin H (2016) The use of pesticides in vector control. Turkiye Klinikleri J Vet Sci Pharmacol Toxicol-Special Topics. 2(2): 26-34.

Becker N, Petric D, Zgomba M, Boaseâ C, Dahl C, Madonâ M, Kaiser A (2010) Mosquitoes and Their Control. Vol. 2. Springer-Verlag, Berlin Heidelberg.

Khambay BPS, Jewess PJ (2010) Pyrethroids. In: Gilbert LI, Gill SS (Eds): Insect Control Biological and Synthetic Agents. Academic Press, London, pp. 1-29.

Coats JR (1990) Mechanisms of toxic action and structure-activity relationships for organochlorine and synthetic pyrethroid insecticides. Environ Health Perspect. 87: 255-262.

Schleier III JJ, Peterson RKD (2011) Pyrethrins and Pyrethroid Insecticides. In: López Ó, Fernández-Bolaños JG (Eds): Green Trends in Insect Control. Royal Society of Chemistry, Cambridge, pp. 94-131.

World Health Organization (WHO) (2013) Test Procedures for Insecticide Resistance Monitoring in Malaria Vector Mosquitoes. WHO press, Geneva.

Thatheyus AJ, Selvam ADG (2013) Synthetic pyrethroids: toxicity and biodegradation. Appl Ecol Env Res. 1(3): 33-36.

Harbach RE (1985) Pictorial keys to the genera of mosquitoes, subgenera of Culex and the species of Culex (Culex) occurring in Southwestern Asia and Egypt, with a note on the subgeneric placement of Culex deserticola (Diptera: Culicidae). Mosquito Systematics. 17(2): 83-107.

Samanidou-Voyadjoglou A, Harbach RE (2001) Keys to the adult female mosquitoes (Culicidae) of Greece. Eur Mosq Bull. 10: 13-20.

Brogdon WG, Chan A (2010) Guidelines for Evaluating Insecticide Resistance in Vectors Using The CDC Bottle Bioassay/Methods in Anopheles Research, Vol. 2. CDC Technical Report, Atlanta.

World Health Organization (WHO) (2006) Guidelines for Testing Mosquito Adulticides for Indoor Residual Spraying and Treatment of Mosquito Nets. WHO press, Geneva.

Owusu HF, Jančáryová D, Malone D, Müller P (2015) Comparability between insecticide resistance bioassays for mosquito vectors: time to review current methodology? Parasite Vectors. 8: 357.

Abbott WS (1925) A method of computing the effectiveness of an insecticide.

J Econ Entomol. 18: 265-267.

Ranson H, N’guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V (2011) Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 27(2): 91-98.

Pittendrigh BR, Margam VM, Walters KRJr, Steele LD, Olds BP, Sun L, Huesing J, Lee SH, Clark JM (2014) Understanding Resistance and Induced Responses of Insects to Xenobiotics and Insecticides in The Age of “Omics” and Systems Biology. In: Onstad DW (Ed): Insect Resistance Management, Biology, Economics, and Prediction, Vol. 2. Academic Press (Elsevier), Amsterdam, pp. 55-98.

Corbel V, N’guessan R (2013) Distribution, Mechanisms, Impact and Management of Insecticide Resistance in Malaria Vectors: A Pragmatic Review. In: Manguin S (Ed): Anopheles Mosquitoes-new Insights into Malaria Vectors. InTech, Rijeka, pp. 579-633.

Bowman DD (2014) Georgis’parasitology for Veterinarians, Vol. 10. Elsevier, St. Louis, Missouri.

Diabate A, Baldet T, Chandre F, Akogbeto M, Guiguemde TR, Darriet F, Brengues C, Guillet P, Hemingway J, Small GJ, Hougard JM (2002) The role of agricultural use of insecticides in resistance to pyrethroids in Anopheles gambiae S.L. in Burkina Faso. Am J Trop Med Hyg. 67(6): 617-622.

Mittal PK, Adak T, Singh OP, Raghavendra K, Subbarao SK (2002) Reduced susceptibility to deltamethrin in Anopheles culicifacies sensu lato, in Ramnathapuram district, Tamil Nadu–selection of a pyrethroid-resistant strain. Curr Sci. 82(2): 185-188.

Nkya TE, Akhouayri I, Poupardin R, Batengana B, Mosha F, Magesa S, Kisinza W, David J-P (2014) Insecticide resistance mechanisms associated with different environments in the malaria vector Anopheles gambiae: a case study in Tanzania. Malar J. 13: 28.

Luleyap U, Kasap H (2000) Insecticide resistance in malaria vector An. sacharovi. Turk J Biol. 24: 437-460.

Corbel V, N’guessan R, Brengues C, Chandre F, Djogbenou L, Martin T, Akogb´Eto M, Hougard JM, Rowland M (2007) Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop. 101: 207-216.

Kioulos I, Kampouraki A, Morou E, Skavdisc G, Vontasb J (2014) Insecticide resistance status in the major West Nile virus vector Culex pipiens from Greece. Pest Manag Sci. 70: 623-627.

Gorouhi MA, Vatandoost H, Oshaghi MA, Raeisi A, Enayati AA, Mirhendi H, Hanafi-Bojd AA, Abai MR, Salim-Abadi Y, Rafi F (2016) Current susceptibility status of Anopheles stephensi (Diptera: Culicidae) to different imagicides in a malarious area, Southeastern Iran. J Arthropod Borne Dis. 10(4): 493-500.

Kasap H, Kasap M, Alptekin D, Luleyap U, Herath PRJ (2000) Insecticide resistance in Anopheles sacharovi Favre in southern Turkey. Bull World Health Organ. 78 (5): 687-692.

Pocquet N, Darriet F, Zumbo B, Milesi P, Thiria J, Bernard V, Toty C, Labbé P, Chandre F (2014) Insecticide resistance in disease vectors from Mayotte: an opportunity for integrated vector management. Parasite Vectors. 7: 299.

Yadouléton A, Badirou K, Agbanrin R, Jost H, Attolou R, Srinivasan R, Padonou G, Akogbéto M (2015) Insecticide resistance status in Culex quinquefasciatus in Benin. Parasite Vectors. 8:17.

Nkya TE, Akhouayi I, Kisinza W, David J-P (2013) Impact of environment on mosquito response to pyrethroid insecticides: facts, evidences and prospects. Insect Biochem Mol Biol. 43: 407-416.

Poupardin R, Reynaud S, Strode C, Ranson H, Vontas J, David J-P (2008) Crossinduction of detoxification genes by environmental xenobiotics and insecticides in the mosquito Aedes aegypti: impact on larval tolerance to chemical insecticides. Insect Biochem Mol Biol. 38(5): 540-551.

Poupardin R, Riaz MA, Jones CM, Chandor-Proust A, Reynaud S, David J-P (2012) Do pollutants affect insecticide-driven gene selection in mosquitoes? Experimental evidence from transcriptomics. Aquat Toxicol. 114-115, 49-57.

Riaz MA, Poupardin R, Reynaud S, Strode C, Ranson H, David J-P (2009) Impact of glyphosate and benzo[a]pyrene on the tolerance of mosquito larvae to chemicalinsecticides. Role of detoxification genes in response to xenobiotics. Aquat Toxicol. 93(1): 61-69.

David J-P, Coissac E, Melodelima C, Poupardin R, Riaz MA, Chandor-Proust A, Reynaud S (2010) Transcriptome response to pollutants and insecticides in the dengue vector Aedes aegypti using next-generation sequencing technology. BMC Genomics. 11 (216).

Riaz MA, Chandor-Proust A, Dauphin-Villemant C, Poupardin R, Jones CM, Strode C, Regent-Kloeckner M, David J-P, Reynaud S (2013) Molecular mechanism sassociated with increased tolerance to the neonicotinoid insecticide imidacloprid in the dengue vector Aedes aegypti. Aquat Toxicol. 126: 326-337.

Ser O (2018) Investigation of susceptibility levels to synthetic pyrethroids of Culex pipiens L. (Diptera: Culicidae) populations in Antalya. [PhD dissertation]. Institute of Natural and Applied Sciences, Akdeniz University, Turkey.

Salim-Abadi Y, Oshaghi MA, Enayati AA, Abai MR, Vatandoost H, Eshraghian MR, Mirhendi H, Hanafi-Bojd AA, Gorouhi MA, Rafi F (2016) High insecticides resistance in Culex pipiens (Diptera: Culicidae) from Tehran, Capital of Iran. J Arthropod Borne Dis. 10(4): 483-492.

Karaağaç SU (2011) Insecticide Resistance. In: Perveen F (Ed): Insecticides–advances in Integrated Pest Management. In Tech, Rijeka, pp. 469-478.

Babayigit MA, Tekbas OF, Cetin H (2014) Public health effects of pesticides used in pest management and precautions for the protection. TAF Prev Med Bull. 13(5): 405-412.

Knox TB, Juma EO, Ochomo EO, Jamet HP, Ndungo L, Chege P, Bayoh NM, N’Guessan R, Christian RN, Hunt RH, Coetzee M (2014) An online tool for mapping insecticide resistance in major Anopheles vectors of human malaria parasites and review of resistance status for the Afrotropical region. Parasite Vectors. 7:76.

World Health Organization (WHO) (2016a) Monitoring and Managing Insecticide Resistance in Aedes Mosquito Populations, Interim Guidance for Entomologists. WHO Press, Geneva.

Yu SJ (2008) The Toxicology and Biochemistry of Insecticides. CRC Press/Taylor & Francis Group, Boca Raton.

World Health Organization (WHO) (2016b) Test Procedures for Insecticide Resistance Monitoring in Malaria Vector Mosquitoes, Vol. 2. WHO Press, Geneva.

Poopathi S, Abidha S (2010) Mosquitocidal bacterial toxins (Bacillus sphaericus and Bacillus thuringiensis serovar israelensis): mode of action, cytopathological effects and mechanism of resistance. J Physiol Pathophysiol. 1(3): 22-38.

How to Cite
Ser Önder, Cetin H. Investigation of Susceptibility Levels of Culex pipiens L. (Diptera: Culicidae) Populations to Synthetic Pyrethroids in Antalya Province of Turkey. J Arthropod Borne Dis. 13(3):243-258.
Original Article