The effect of larval cigarette exposure on the life history of the major malaria vector Anopheles arabiensis (Diptera: Culicidae)

REFERENCES

• Agumba, S., Gimnig, J.E., Ogonda, L., Ombok, M., Kosgei, J., Munga, S., Guyah, B., Omondi, S. & Ochomo, E. 2019. Diagnostic dose determination and efficacy of chlorfenapyr and clothianidin insecticides against Anopheles malaria vector populations of western Kenya. Malaria Journal, 18: 243.
   PubMed Web of Science ®Google Scholar
• Antonio-Nkondjio, C., Fossog, B.T., Ndo, C., Djantio, B.M., Togouet, S.Z., Awono-Ambene, P., Costantini, C., Wondji, C.S. & Ranson, H. 2011. Anopheles gambiae distribution and insecticide resistance in the cities of Douala and Yaounde (Cameroon): influence of urban agriculture and pollution. Malaria Journal, 10: 154.
   PubMed Web of Science ®Google Scholar
• Awolola, T.S., Oduola, A.O., Obansa, J.B., Chukwurar, N.J. & Unyimadu, J.P. 2007. Anopheles gambiae s.s. breeding in polluted water bodies in urban Lagos, southwestern Nigeria. Journal of Vector Borne Diseases, 44: 241–244.
   PubMedGoogle Scholar
• Azrag, R.S. & Mohammed, B.H. 2018. Anopheles arabiensis in Sudan: a noticeable tolerance to urban polluted larval habitats associated with resistance to Temephos. Malaria Journal, 17: 204.
   PubMed Web of Science ®Google Scholar
• Balawanth, R., Ba, I., Qwabe, B., Gast, L., Maharaj, R., Raman, J., Graffy, R., Shandukani, M. & Moonasar, D. 2019. Assessing Kwa-Zulu-Natal’s progress towards malaria elimination and its readiness for sub-national verification. Malaria Journal, 18: 108.
   PubMed Web of Science ®Google Scholar
• Barnes, K.G., Weedall, G.D., Ndula, M., Irving, H., Mzihalowa, T., Hemingway, J. & Wondji, C.S. 2017. Genomic footprints of selective sweeps from metabolic resistance to pyrethroids in African malaria vectors are driven by scale up of insecticide-based vector control. PLOS Genetics, 13: e1006539.
   PubMed Web of Science ®Google Scholar
• Belz, R.G. & Duke, S.O. 2014. Herbicides and plant hormesis. Pest Management Science, 70: 698–707.
   PubMed Web of Science ®Google Scholar
• Brito, I.P., Tropaldi, L., Carbonari, C.A. & Velini, E.D. 2018. Hormetic effects of glyphosate on plants. Pest Management Science, 74: 1064–1070.
   PubMed Web of Science ®Google Scholar
• Brogdon, W.G. & McAllister, J.C. 1998a. Insecticide resistance and vector control. Emerging Infectious Diseases, 4: 605–645.
   PubMed Web of Science ®Google Scholar
• Brogdon, W.G. & McAllister, J.C. 1998b. Simplification of adult mosquito bioassays through use of time-mortality determinations in glass bottles. Journal of the American Mosquito Control Association, 14: 159–164.
   PubMed Web of Science ®Google Scholar
• Calafat, A.M., Polzin, G.M., Saylor, J., Richter, P., Ashley, D.L. & Watson, C.H. 2004. Determination of tar, nicotine, and carbon monoxide yields in the mainstream smoke of selected international cigarettes. Tobacco Control, 13: 45–51.
   PubMed Web of Science ®Google Scholar
• Casida, J.E. 2018. Neonicotinoids and other insect nicotinic receptor competitive modulators: progress and prospects. Annual Review of Entomology, 63: 125–144.
   PubMed Web of Science ®Google Scholar
• Chege, G.M. & Beier, J.C. 1990. Effect of Plasmodium falciparum on the survival of naturally infected afrotropical Anopheles (Diptera: Culicidae). Journal of Medical Entomology, 27: 454–458.
   PubMed Web of Science ®Google Scholar
• Coon, K.L., Vogel, K.J., Brown, M.R. & Strand, M.R. 2014. Mosquitoes rely on their gut microbiota for development. Molecular Ecology, 23: 2727–2739.
   PubMed Web of Science ®Google Scholar
• Dagg, K., Irish, S., Wiegand, R.E., Shililu, J., Yewhalaw, D. & Messenger, L.A. 2019. Evaluation of toxicity of clothianidin (neonicotinoid) and chlorfenapyr (pyrrole) insecticides and cross-resistance to other public health insecticides in Anopheles arabiensis from Ethiopia. Malaria Journal, 18: 49.
   PubMed Web of Science ®Google Scholar
• Dandalo, L.C., Brooke, B.D., Munhenga, G., Lobb, L.N., Zikhali, J., Ngxongo, S.P., Zikhali, P.M., Msimang, S., Wood, O.R., Mofokeng, M., Misiani, E., Chirwa, T. & Koekemoer, L.L. 2017. Population dynamics and Plasmodium falciparum (Haemosporida: Plasmodiidae) infectivity rates for the malaria vector Anopheles arabiensis (Diptera: Culicidae) at Mamfene, KwaZulu-Natal, South Africa. Journal of Medical Entomology, 54: 1758–1766.
   PubMed Web of Science ®Google Scholar
• Darriet, F. & Chandre, F. 2013. Efficacy of six neonicotinoid insecticides alone and in combination with deltamethrin and piperonyl butoxide against pyrethroid-resistant Aedes aegypti and Anopheles gambiae (Diptera: Culicidae). Pest Management Science, 69: 905–910.
   PubMed Web of Science ®Google Scholar
• Dieng, H., Rajasaygar, S., Ahmad, A.., Rawi, C.S., Ahmad, H., Satho, T., Miake, F., Zuharah, W.F., Fukumitsu, Y., Saad, A.R., Abdul Hamid, S., Vargas, R.E., Ab Majid, A.H., Fadzly, N., ABU KASSIM, N.F., Hashim, N.A., Abd Ghani, I., Abang, F.B. & Abubakar, S. 2014. Indirect effects of cigarette butt waste on the dengue vector Aedes aegypti (Diptera: Culicidae). Acta Tropica, 130: 123–130.
   PubMed Web of Science ®Google Scholar
• Dieng, H., Saifur, R.G., Ahmad, A.H., Rawi, C.S., Boots, M., Satho, T., Zuharah, W.F., Fadzly, N., Althbyani, A., Miake, F., Jaal, Z. & Abubakar, S. 2011. Discarded cigarette butts attract females and kill the progeny of Aedes albopictus. Journal of the American Mosquito Control Association, 27: 263–271.
   PubMed Web of Science ®Google Scholar
• Finney, D.J. 1952. Probit Analysis. 2nd ed., New York, Cambridge University Press.
   Google Scholar
• Fongnikin, A., Houeto, N., Agbevo, A., Odjo, A., Syme, T., N’Guessan, R. & Ngufor, C. 2020. Efficacy of Fludora® Fusion (a mixture of deltamethrin and clothianidin) for indoor residual spraying against pyrethroid-resistant malaria vectors: laboratory and experimental hut evaluation. Parasites & Vectors, 13: 466.
   PubMed Web of Science ®Google Scholar
• Hancock, P.A., Hendriks, C.J.M., Tangena, J.A., Gibson, H., Hemingway, J., Coleman, M., Gething, P.W., Cameron, E., Bhatt, S. & Moyes, C.L. 2020. Mapping trends in insecticide resistance phenotypes in African malaria vectors. PLOS Biology, 18: e3000633.
   PubMed Web of Science ®Google Scholar
• Hemingway, J. 2014. The role of vector control in stopping the transmission of malaria: threats and opportunities. Philosophical Transactions of the Royal Society B: Biological Sciences, 369: 20130431.
   PubMed Web of Science ®Google Scholar
• Hemingway, J., Beaty, B.J., Rowland, M., Scott, T.W. & Sharp, B.L. 2006. The Innovative Vector Control Consortium: improved control of mosquito-borne diseases. Trends in Parasitology, 22: 308–312.
   PubMed Web of Science ®Google Scholar
• Hemingway, J., Ranson, H., Magill, A., Kolaczinski, J., Fornadel, C., Gimnig, J., Coetzee, M., Simard, F., Roch, D.K., Hinzoumbe, C.K., Pickett, J., Schellenberg, D., Gething, P., Hoppé, M. & Hamon, N. 2016. Averting a malaria disaster: will insecticide resistance derail malaria control? The Lancet, 387: 1785–1788.
   PubMed Web of Science ®Google Scholar
• Hunt, R.H., Brooke, B.D., Pillay, C., Koekemoer, L.L. & Coetzee, M. 2005. Laboratory selection for and characteristics of pyrethroid resistance in the malaria vector Anopheles funestus. Medical and Veterinary Entomology, 19: 271–275.
   PubMed Web of Science ®Google Scholar
• Jeanrenaud, A., Brooke, B.D. & Oliver, S.V. 2020. Second generation effects of larval metal pollutant exposure on reproduction, longevity and insecticide tolerance in the major malaria vector Anopheles arabiensis (Diptera: Culicidae). Parasites & Vectors, 13: 4.
   PubMed Web of Science ®Google Scholar
• Jeanrenaud, A.C.S.N., Brooke, B.D. & Oliver, S.V. 2019. The effects of larval organic fertiliser exposure on the larval development, adult longevity and insecticide tolerance of zoophilic members of the Anopheles gambiae complex (Diptera: Culicidae). PLoS One, 14: e0215552.
   PubMed Web of Science ®Google Scholar
• Jones, C.M., Toe, H.K., Sanou, A., Namountougou, M., Hughes, A., Diabate, A., Dabire, R., Simard, F. & Ranson, H. 2012. Additional selection for insecticide resistance in urban malaria vectors: DDT resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PLoS One, 7: e45995.
   PubMed Web of Science ®Google Scholar
• Kamal, H.A. & Khater, E.I. 2013. Potency and persistence of the bacterial mosquitocide Bacillus sphaericus against culicine mosquitoes under field conditions. Journal of the Egyptian Society of Parasitology, 43: 115–124.
   PubMedGoogle Scholar
• Kaplan, E.L. & Meier, P. 1958. Nonparametric estimation from incomplete observations. Journal of the American Statistical Association, 53: 457–481.
   Web of Science ®Google Scholar
• Kibuthu, T.W., Njenga, S.M., Mbugua, A.K. & Muturi, E.J. 2016. Agricultural chemicals: life changer for mosquito vectors in agricultural landscapes? Parasites & Vectors, 9: 500.
   PubMed Web of Science ®Google Scholar
• Knox, T.B., Juma, E.O., Ochomo, E.O., Pates Jamet, H., Ndungo, L., Chege, P., Bayoh, N.M., N’Guessan, R., Christian, R.N., Hunt, R.H. & 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. Parasites & Vectors, 7: 76.
   PubMed Web of Science ®Google Scholar
• Kruskal, W.H. & Wallis, W.A. 1952. Use of ranks in one-criterion variance analysis. Journal of the American Statistical Association, 47: 583–621.
   Web of Science ®Google Scholar
• Lees, R., Praulins, G., Davies, R., Brown, F., Parsons, G., White, A., Ranson, H., Small, G. & Malone, D. 2019. A testing cascade to identify repurposed insecticides for next-generation vector control tools: screening a panel of chemistries with novel modes of action against a malaria vector. Gates Open Research, 3: 1464.
   PubMedGoogle Scholar
• Mohammadi, D. 2010. Public health insecticide development: a status of hiatus. The Lancet, 376: 1207.
   PubMed Web of Science ®Google Scholar
• Murugan, K., Suresh, U., Panneerselvam, C., Rajaganesh, R., Roni, M., Aziz, A.T., Hwang, J.S., Sathishkumar, K., Rajasekar, A., Kumar, S., Alarfaj, A.A., Higuchi, A. & Benelli, G. 2018. Managing wastes as green resources: cigarette butt-synthesized pesticides are highly toxic to malaria vectors with little impact on predatory copepods. Environmental Science and Pollution Research, 25: 10456–10470.
   PubMed Web of Science ®Google Scholar
• N’Guessan, R., Odjo, A., Ngufor, C., Malone, D. & Rowland, M. 2016. A chlorfenapyr mixture net Interceptor® G2 shows high efficacy and wash durability against resistant mosquitoes in West Africa. PLoS One, 11: e0165925.
   PubMed Web of Science ®Google Scholar
• Nchoutpouen, E., Talipouo, A., Djiappi-Tchamen, B., Djamouko-Djonkam, L., Kopya, E., Ngadjeu, C.S., Doumbe-Belisse, P., Awono-Ambene, P., Kekeunou, S., Wondji, C.S. & Antonio-Nkondjio, C. 2019. Culex species diversity, susceptibility to insecticides and role as potential vector of lymphatic filariasis in the city of Yaoundé, Cameroon. PLOS Neglected Tropical Diseases, 13: e0007229.
   PubMed Web of Science ®Google Scholar
• Ngufor, C., Fongnikin, A., Hobbs, N., Gbegbo, M., Kiki, L., Odjo, A., Akogbeto, M. & Rowland, M. 2020. Indoor spraying with chlorfenapyr (a pyrrole insecticide) provides residual control of pyrethroid-resistant malaria vectors in southern Benin. Malaria Journal, 19: 249.
   PubMed Web of Science ®Google Scholar
• Novotny, T.E., Lum, K., Smith, E., Wang, V. & Barnes, R. 2009. Cigarettes butts and the case for an environmental policy on hazardous cigarette waste. International Journal of Environmental Research and Public Health, 6: 1691–1705.
   PubMed Web of Science ®Google Scholar
• Novotny, T.E. & Slaughter, E. 2014. Tobacco product waste: an environmental approach to reduce tobacco consumption. Current Environmental Health Reports, 1: 208–216.
   PubMedGoogle Scholar
• Oliver, S.V. & Brooke, B.D. 2013. The effect of larval nutritional deprivation on the life history and DDT resistance phenotype in laboratory strains of the malaria vector Anopheles arabiensis. Malaria Journal, 12: 44.
   PubMed Web of Science ®Google Scholar
• Oliver, S.V. & Brooke, B.D. 2017. The effect of elevated temperatures on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). Malaria Journal, 16: 73.
   PubMed Web of Science ®Google Scholar
• Oliver, S.V. & Brooke, B.D. 2018a. The effect of commercial herbicide exposure on the life history and insecticide resistance phenotypes of the major malaria vector Anopheles arabiensis (Diptera: culicidae). Acta Tropica, 188: 152–160.
   PubMed Web of Science ®Google Scholar
• Oliver, S.V. & Brooke, B.D. 2018b. The effect of metal pollution on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). PLoS One, 13: e0192551.
   PubMed Web of Science ®Google Scholar
• Oliver, S.V., Kaiser, M.L., Wood, O.R., Coetzee, M., Rowland, M. & Brooke, B.D. 2010. Evaluation of the pyrrole insecticide chlorfenapyr against pyrethroid resistant and susceptible Anopheles funestus (Diptera: Culicidae). Tropical Medicine & International Health, 15: 127–131.
   PubMed Web of Science ®Google Scholar
• Oxborough, R.M., Seyoum, A., Yihdego, Y., Dabire, R., Gnanguenon, V., Wat’senga, F., Agossa, F.R., Yohannes, G., Coleman, S., Samdi, L.M., Diop, A., Faye, O., Magesa, S., Manjurano, A., Okia, M., Alyko, E., Masendu, H., Baber, I., Sovi, A., Rakotoson, J.D., Varela, K., Abong’o, B., Lucas, B., Fornadel, C. & Dengela, D. 2019. Susceptibility testing of Anopheles malaria vectors with the neonicotinoid insecticide clothianidin; results from 16 African countries, in preparation for indoor residual spraying with new insecticide formulations. Malaria Journal, 18: 264.
   PubMed Web of Science ®Google Scholar
• Raman, J., morris, N., Frean, J., Brooke, B., Blumberg, L., Kruger, P., Mabusa, A., Raswiswi, E., Shandukani, B., Misani, E., Groepe, M.A. & Moonasar, D. 2016. Reviewing South Africa’s malaria elimination strategy (2012–2018): progress, challenges and priorities. Malaria Journal, 15: 438.
   PubMed Web of Science ®Google Scholar
• Ranson, H., Lissenden, N. 2016. Insecticide resistance in African anopheles mosquitoes: a worsening situation that needs urgent action to maintain malaria control. Trends in Parasitology. 32: 187–196.
   PubMed Web of Science ®Google Scholar
• Samuel, M., Brooke, B.D. & Oliver, S.V. 2020. Effects of inorganic fertilizer on larval development, adult longevity and insecticide susceptibility in the malaria vector Anopheles arabiensis (Diptera: Culicidae). Pest Management Science, 76: 1560–1568.
   PubMed Web of Science ®Google Scholar
• Shapiro, S.S. & Wilk, M.B. 1965. An analysis of variance test for normality (complete samples). Biometrika, 52: 591–611.
   Web of Science ®Google Scholar
• Sparks, T.., Crossthwaite, A.J., Nauen, R., Banba, S., Cordova, D., Earley, F., Ebbinghaus-Kintscher, U., Fujioka, S., Hirao, A., Karmon, D., Kennedy, R., Nakao, T., Popham, H.J.R., Salgado, V., Watson, G.B., Wedel, B.J. & Wessels, F.J. 2020. Insecticides, biologics and nematicides: updates to IRAC’s mode of action classification - a tool for resistance management. Pesticide Biochemistry and Physiology, 167: 104587.
   PubMed Web of Science ®Google Scholar
• Steppuhn, A., Gase, K., Krock, B., Halitschke, R. & Baldwin, I.T. 2004. Nicotine’s defensive function in nature. PLoS Biology, 2: E217.
   PubMed Web of Science ®Google Scholar
• Tabbabi, A., Daaboub, J., Ben Cheikh, R., Laamari, A., Feriani, M., Boubaker, C., Ben Jha, I. & Ben Cheikh, H. 2019. The potential role of urbanization in the resistance to organophosphate insecticide in Culex pipiens pipiens from Tunisia. African Health Sciences, 19: 1368–1375.
   PubMed Web of Science ®Google Scholar
• Talhout, R., Schulz, T., Florek, E., Van Benthem, J., Wester, P. & Opperhuizen, A. 2011. Hazardous compounds in tobacco smoke. International Journal of Environmental Research and Public Health, 8: 613–628.
   PubMed Web of Science ®Google Scholar
• Tchouakui, M., Riveron, J.M., Djonabaye, D., Tchapga, W., Irving, H., Soh Takam, P., Njiokou, F. & Wondji, C.S. 2018. Fitness costs of the glutathione S-Transferase Epsilon 2 (L119F-GSTe2) mediated metabolic resistance to insecticides in the major African malaria vector Anopheles funestus. Genes, 9(12): 645.
   Web of Science ®Google Scholar
• Tukey, J.W. 1949. Comparing individual means in the analysis of variance. Biometrics, 5: 99–114.
   PubMed Web of Science ®Google Scholar
• Venter, N., Oliver, S.V., Muleba, M., Davies, C., Hunt, R.H., Koekemoer, L.L., Coetzee, M. & Brooke, B.D. 2017. Benchmarking insecticide resistance intensity bioassays for Anopheles malaria vector species against resistance phenotypes of known epidemiological significance. Parasites & Vectors, 10: 198.
   PubMed Web of Science ®Google Scholar
• Weedall, G.D., Riveron, J.M., Hearn, J., Irving, H., Kamdem, C., Fouet, C., White, B.J. & Wondji, C.S. 2020. An Africa-wide genomic evolution of insecticide resistance in the malaria vector Anopheles funestus involves selective sweeps, copy number variations, gene conversion and transposons. PLOS Genetics, 16: e1008822.
   PubMed Web of Science ®Google Scholar
• WHO. 2005. Guidelines for laboratory and field testing of mosquito larvicides. [Online] (accessed 27 September 2020).
   Google Scholar
• Yamamoto, I. 1999. Nicotine to nicotinoids: 1962 to 1997. In: Yamamoto, I. & Casida, J.E. (Eds.) Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor. 3–27, Tokyo, Springer-Verlag.
   Google Scholar