Biological responses in Musca domestica to fipronil and chlorfenapyr exposures
Keywords:
life cycle parameters; response to insecticides; sublethal effects; transgenerational insecticidal effects; Diptera
Abstract
Insect populations exist under acute and chronic exposures to lethal and sublethal insecticide concentrations. Among the sublethal effects of insecticides on insects are reductions in life span, development rates, population growth, fertility, fecundity, changes in sex ratio, deformities, changes in behaviour, feeding, searching, and oviposition. These effects may differ depending on the modes of action of insecticides, their doses, and developmental stage of application. This study evaluated the life-history parameters in Musca domestica Linnaeus, 1758 (Diptera:Muscidae) strains that were exposed to two insecticides (fipronil and chlorfenapyr) with different modes of action at sublethal concentrations in each generation up to tenth. Two approaches to each insecticide’s exposure were used in this study, particularly in one approach, only adults M. domestica were exposed to fipronil or chlorfenapyr and in another approach, only larvae were exposed to each insecticide. The susceptibility of adult flies to these insecticides was assessed by resistance ratio based on results of non-choice feeding bioassays. Fipronil exposure at the sublethal concentration in each generation did not affect the susceptibility of adult M. domestica (in the tenth generation) to fipronil. The resistance ratio values revealed tolerance to chlorfenapyr in adults of M. domestica strains that were exposed to this insecticide, independent of the approach used to insecticide exposure. Most of the life-history parameters (such as durations of separate developmental stages, the emergence duration, the adult emergence ratio, the female ratio, and the number of eggs per female per day) of the second, fourth, sixth, eighth, and tenth generations of the insecticide-exposed strains were similar to those of the control strain. At the same time, the sublethal effects of both insecticides fipronil and chlorfenapyr prolonged the larval duration (1.63–2.22 times) and the number of days from egg to adult (1.18–1.39 times) compared to the control strain. Further studies are needed to investigate a possible genetic variability in M. domestica in response to exposure of parental generation to sublethal doses of fipronil and chlorfenapyr.References
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Ali, E., Liao, X., Yang, P., Mao, K. K., Zhang, X. L., Shakeel, M., Salim, A. M. A., Wan H., & Li J. (2017). Sublethal effects of buprofezin on development and reproduction in the white-backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Scientific Reports, 7, 16913.
Ameen, A., Kaakeh, W., & Bennett, G. W. (2000). Integration of chlorfenapyr into a management program for German cockroach (Dictyoptera: Blattellidae). Journal of Agricultural and Urban Entomology, 17, 135–142.
Baena-Díaz, F., Martínez-Morales, I., Gil-Pérez, Y., & González-Tokman, D. (2018). Trans-generational effects of ivermectin exposure in dung beetles. Chemosphere, 202, 637–643.
Bantz, A., Camon, J., Froger, J. A., Goven, D., & Raymond, V. (2018). Exposure to sublethal doses of insecticide and their effects on insects at cellular and physiological levels. Current Opinion in Insect Science, 30, 73–78.
Benelli, G., Pavela, R., Giordani, C., Casettari, L., Curzi, G., Cappellacci, L., Petrelli, R., & Maggi, F. (2018). Acute and sub-lethal toxicity of eight essential oils of commercial interest against the filariasis mosquito Culex quinquefasciatus and the housefly Musca domestica. Industrial Crops and Products, 112, 668–680.
Buczkowski, G., Scharf, M. E., Ratliff, C. R., & Bennett, G. W. (2005). Efficacy of simulated barrier treatments against laboratory colonies of pharaoh ant. Journal of Economic Entomology, 98, 485–492.
Byford, R. L., Craig, M. E., & Crosby, B. L. (1992). A review of ectoparasites and their effect on cattle production. Journal of Animal Science, 70(2), 597–602.
Casida, J. E., & Durkin, K. A. (2013). Neuroactive insecticides: Targets, selectivity, resistance, and secondary effects. Annual Review of Entomology, 58, 99–117.
de França, S. M., Breda, M. O., Barbosa, D. R. S., Araujo, A. M. N., & Guedes, C. A. (2017). The sublethal effects of insecticides in insects. In: Shields, V. D. C. (Ed.). Biological control of pest and vector insects. IntechOpen, London.
Delpuech, J.-M., & Delahaye, M. (2013). The sublethal effects of deltamethrin on Trichogramma behaviors during the exploitation of host patches. Science of the Total Environment, 447, 274–279.
Eremina, O. Y. (2017). Khlorfenapir – perspektivnyо insektitsid iz gruppy pirrolov dlya bor’by s rezistentnymi sinantropnymi nasekomymi [Chlorfenapyr – promising pyrrole insecticide for combating resistant synanthropic insects]. Pest-Management, 101, 41–49 (in Russian).
Eremina, O. Y., Olekhnovich, E. I., Olifer, V. V., Ibragimkhalilova, I. V., Gevorkyan, I. S., Bendrysheva, S. N., & Sarvin, B. A. (2016). Issledovanie rezistentnosti ryzhikh tarakanov k fipronilu [Investigation of Blattella germanica resistance to fipronil]. Dezinfektsionnoe Delo, 96(2), 33–42 (in Russian).
Farooq, M., & Freed, S. (2018). Mortality, biological, and biochemical response of Musca domestica (Diptera: Muscidae) to selected insecticides. Journal of Entomological Science, 53, 27–45.
Förster, M., Klimpel, S., Mehlhorn, H., Sievert, K., Messler, S., & Pfeffer, K. (2007). Pilot study on synanthropic flies (e.g. Musca, Sarcophaga, Calliphora, Fannia, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitology Research, 101, 243–246.
Guglielmone, A. A., Volpogni, M. M., Scherling, N., Cobeñas, M. M., Mangold, A. J., Anziani, O. S., Loppolo, M., & Doscher, M. (2000). Chlorfenapyr ear tags to control Haematobia irritans (L.) (Diptera: Muscidae) on cattle. Veterinary Parasitology, 93(1), 77–82.
Haynes, K. F. (1988). Sublethal effects of neurotoxic insecticides on insect behavior. Annual Review Entomology. 33, 149–168.
Kozak, V. M., Romanenko, E. R., & Brygadyrenko, V. V. (2020). Influence of herbicides, insecticides and fungicides on food consumption and body weight of Rossiulus kessleri (Diplopoda, Julidae). Biosystems Diversity, 28(3), 272–280.
Kristensen, M., Jespersen, J. B., & Knorr, M. (2004). Cross-resistance potential of fipronil in Musca domestica. Pest Management Science, 60, 894–900.
Lalouette, L., Pottier, M. A., Wycke, M. A., Boitard, C., Bozzolan, F., Maria, A., Demondion, E., Chertemps, T., Lucas, P., Renault, D., Maibeche, M., & Siaussat, D. (2016). Unexpected effects of sublethal doses of insecticide on the peripheral olfactory response and sexual behavior in a pest insect. Environmental Science and Pollution Research, 23, 3073–3085.
Leontieva, T. L., Syrtlanova, L. A., & Benkovskaya, G. V. (2016). Razvitie ustojchivosti k insektitsidam u koloradskogo zhuka na territorii Respubliki Bashkortostan [Development of Colorado potato beetle resistance to insecticides on the territory of the Republic of Bashkortostan]. Vestnik Bashkirskogo Gosudarstvennogo Agrarnogo Universiteta, 38(2), 11–14 (in Russian).
Levchenko, M. A., & Silivanova, E. A. (2015). Effektivnost’ insektitsidnykh primanochnykh sostavov dlya bor’by s mukhami [The effectiveness of insecticidal bait compositions for houseflies control]. Vestnik Veterinarii, 73(2), 23–26 (in Russian).
Müller, C. (2018). Impacts of sublethal insecticide exposure on insects – facts and knowledge gaps. Basic and Applied Ecology, 30, 1–10.
Müller, T., Römer, C. I., & Müller, C. (2019). Parental sublethal insecticide exposure prolongs mating response and decreases reproductive output in offspring. Journal of Applied Ecology, 56, 1528–1537.
N’Guessan, R., Boko, P., Odjo, A., Akogbeto, M., Yates, A., & Rowland, M. (2007). Chlorfenapyr: A pyrrole insecticide for the control of pyrethroid or DDT resistant Anopheles gambiae (Diptera: Culicidae) mosquitoes. Acta Tropica, 102, 69–78.
N’Guessan, R., Boko, P., Odjo, A., Knols, B., Akogbeto, M., & Rowland, M. (2009). Control of pyrethroid‐resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes with chlorfenapyr in Benin. Tropical Medicine and International Health, 14, 389–395.
Qayyum, M. A., Wakil, W., Arif, M. J., Sahi, S. T., Saeed, N. A., & Russell, D. A. (2015). Multiple resistances against formulated organophosphates, pyrethroids, and newer-chemistry insecticides in populations of Helicoverpa armigera (Lepidoptera: Noctuidae) from Pakistan. Journal of Economic Entomology, 108(1), 286–293.
Rehan, A., & Freed, S. (2015). Fitness cost of methoxyfenozide and the effects of its sublethal doses on development, reproduction, and survival of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). Neotropical Entomology, 44(5), 513–520.
Romero, A., Potter, M. F., & Haynes, K. F. (2010). Evaluation of chlorfenapyr for control of the bed bug, Cimex lectularius L. Pest Management Science, 66, 1243–1248.
Rust, M. K., & Saran, R. K. (2006). Toxicity, repellency, and transfer of chlorfenapyr against western subterranean termites (Isoptera: Rhinotermitidae). Journal of Economic Entomology, 99(3), 864–872.
Sparks, T. C., 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.
Tamilselvan, R., Kennedy, J. S., & Suganthi, A. (2021). Sublethal and transgenerational effects of spinetoram on the biological traits of Plutella xylostella (L.) (Lepidoptera: Plutellidae). Ecotoxicology, 30(4), 667–677.
Tang, Q., Xiang, M., Hu, H., An, C., & Gao, X. (2015). Evaluation of sublethal effects of sulfoxaflor on the green peach aphid (Hemiptera: Aphididae) using life table parameters. Journal of Economic Entomology, 108(6), 2720–2728.
Ullah, S., Shah, R. M., & Shad, S. A. (2016). Genetics, realized heritability and possible mechanism of chlorfenapyr resistance in Oxycarenus hyalinipennis (Lygaeidae: Hemiptera). Pesticide Biochemistry and Physiology, 133, 91–96.
Van Leeuwen, T., Stillatus, V., & Tirry, L. (2004). Genetic analysis and cross-resistance spectrum of a laboratory-selected chlorfenapyr resistant strain of two-spotted spider mite (Acari: Tetranychidae). Experimental and Applied Acarology, 32(4), 249–261.
Xu, C., Zhang, Z., Cui, K., Zhao, Y., Han, J., Liu, F., & Mu, W. (2016). Effects of sublethal concentrations of cyantraniliprole on the development, fecundity and nutritional physiology of the black cutworm agrotisipsilon (Lepidoptera: Noctuidae). PLoS One, 11(6), e0156555.
Zhang, S., Zhang, X., Shen, J., Mao, K., You, H., & Li, J. (2016). Susceptibility of field populations of the diamondback moth, Plutella xylostella, to a selection of insecticides in Central China. Pesticide Biochemistry and Physiology, 132, 38–46.
Zhao, Y., Wang, Q., Ding, J., Wang, Y., Zhang, Z., Liu, F., & Mu, W. (2018). Sublethal effects of chlorfenapyr on the life table parameters, nutritional physiology and enzymatic properties of Bradysia odoriphaga (Diptera: Sciaridae). Pesticide Biochemistry and Physiology, 148, 93–102.
Zhu, F., Lavine, L., O’Neal, S., Lavine, M., Foss, C., & Walsh, D. (2016). Insecticide resistance and management strategies in urban ecosystems. Insects, 7, 2.
Ali, E., Liao, X., Yang, P., Mao, K. K., Zhang, X. L., Shakeel, M., Salim, A. M. A., Wan H., & Li J. (2017). Sublethal effects of buprofezin on development and reproduction in the white-backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Scientific Reports, 7, 16913.
Ameen, A., Kaakeh, W., & Bennett, G. W. (2000). Integration of chlorfenapyr into a management program for German cockroach (Dictyoptera: Blattellidae). Journal of Agricultural and Urban Entomology, 17, 135–142.
Baena-Díaz, F., Martínez-Morales, I., Gil-Pérez, Y., & González-Tokman, D. (2018). Trans-generational effects of ivermectin exposure in dung beetles. Chemosphere, 202, 637–643.
Bantz, A., Camon, J., Froger, J. A., Goven, D., & Raymond, V. (2018). Exposure to sublethal doses of insecticide and their effects on insects at cellular and physiological levels. Current Opinion in Insect Science, 30, 73–78.
Benelli, G., Pavela, R., Giordani, C., Casettari, L., Curzi, G., Cappellacci, L., Petrelli, R., & Maggi, F. (2018). Acute and sub-lethal toxicity of eight essential oils of commercial interest against the filariasis mosquito Culex quinquefasciatus and the housefly Musca domestica. Industrial Crops and Products, 112, 668–680.
Buczkowski, G., Scharf, M. E., Ratliff, C. R., & Bennett, G. W. (2005). Efficacy of simulated barrier treatments against laboratory colonies of pharaoh ant. Journal of Economic Entomology, 98, 485–492.
Byford, R. L., Craig, M. E., & Crosby, B. L. (1992). A review of ectoparasites and their effect on cattle production. Journal of Animal Science, 70(2), 597–602.
Casida, J. E., & Durkin, K. A. (2013). Neuroactive insecticides: Targets, selectivity, resistance, and secondary effects. Annual Review of Entomology, 58, 99–117.
de França, S. M., Breda, M. O., Barbosa, D. R. S., Araujo, A. M. N., & Guedes, C. A. (2017). The sublethal effects of insecticides in insects. In: Shields, V. D. C. (Ed.). Biological control of pest and vector insects. IntechOpen, London.
Delpuech, J.-M., & Delahaye, M. (2013). The sublethal effects of deltamethrin on Trichogramma behaviors during the exploitation of host patches. Science of the Total Environment, 447, 274–279.
Eremina, O. Y. (2017). Khlorfenapir – perspektivnyо insektitsid iz gruppy pirrolov dlya bor’by s rezistentnymi sinantropnymi nasekomymi [Chlorfenapyr – promising pyrrole insecticide for combating resistant synanthropic insects]. Pest-Management, 101, 41–49 (in Russian).
Eremina, O. Y., Olekhnovich, E. I., Olifer, V. V., Ibragimkhalilova, I. V., Gevorkyan, I. S., Bendrysheva, S. N., & Sarvin, B. A. (2016). Issledovanie rezistentnosti ryzhikh tarakanov k fipronilu [Investigation of Blattella germanica resistance to fipronil]. Dezinfektsionnoe Delo, 96(2), 33–42 (in Russian).
Farooq, M., & Freed, S. (2018). Mortality, biological, and biochemical response of Musca domestica (Diptera: Muscidae) to selected insecticides. Journal of Entomological Science, 53, 27–45.
Förster, M., Klimpel, S., Mehlhorn, H., Sievert, K., Messler, S., & Pfeffer, K. (2007). Pilot study on synanthropic flies (e.g. Musca, Sarcophaga, Calliphora, Fannia, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitology Research, 101, 243–246.
Guglielmone, A. A., Volpogni, M. M., Scherling, N., Cobeñas, M. M., Mangold, A. J., Anziani, O. S., Loppolo, M., & Doscher, M. (2000). Chlorfenapyr ear tags to control Haematobia irritans (L.) (Diptera: Muscidae) on cattle. Veterinary Parasitology, 93(1), 77–82.
Haynes, K. F. (1988). Sublethal effects of neurotoxic insecticides on insect behavior. Annual Review Entomology. 33, 149–168.
Kozak, V. M., Romanenko, E. R., & Brygadyrenko, V. V. (2020). Influence of herbicides, insecticides and fungicides on food consumption and body weight of Rossiulus kessleri (Diplopoda, Julidae). Biosystems Diversity, 28(3), 272–280.
Kristensen, M., Jespersen, J. B., & Knorr, M. (2004). Cross-resistance potential of fipronil in Musca domestica. Pest Management Science, 60, 894–900.
Lalouette, L., Pottier, M. A., Wycke, M. A., Boitard, C., Bozzolan, F., Maria, A., Demondion, E., Chertemps, T., Lucas, P., Renault, D., Maibeche, M., & Siaussat, D. (2016). Unexpected effects of sublethal doses of insecticide on the peripheral olfactory response and sexual behavior in a pest insect. Environmental Science and Pollution Research, 23, 3073–3085.
Leontieva, T. L., Syrtlanova, L. A., & Benkovskaya, G. V. (2016). Razvitie ustojchivosti k insektitsidam u koloradskogo zhuka na territorii Respubliki Bashkortostan [Development of Colorado potato beetle resistance to insecticides on the territory of the Republic of Bashkortostan]. Vestnik Bashkirskogo Gosudarstvennogo Agrarnogo Universiteta, 38(2), 11–14 (in Russian).
Levchenko, M. A., & Silivanova, E. A. (2015). Effektivnost’ insektitsidnykh primanochnykh sostavov dlya bor’by s mukhami [The effectiveness of insecticidal bait compositions for houseflies control]. Vestnik Veterinarii, 73(2), 23–26 (in Russian).
Müller, C. (2018). Impacts of sublethal insecticide exposure on insects – facts and knowledge gaps. Basic and Applied Ecology, 30, 1–10.
Müller, T., Römer, C. I., & Müller, C. (2019). Parental sublethal insecticide exposure prolongs mating response and decreases reproductive output in offspring. Journal of Applied Ecology, 56, 1528–1537.
N’Guessan, R., Boko, P., Odjo, A., Akogbeto, M., Yates, A., & Rowland, M. (2007). Chlorfenapyr: A pyrrole insecticide for the control of pyrethroid or DDT resistant Anopheles gambiae (Diptera: Culicidae) mosquitoes. Acta Tropica, 102, 69–78.
N’Guessan, R., Boko, P., Odjo, A., Knols, B., Akogbeto, M., & Rowland, M. (2009). Control of pyrethroid‐resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes with chlorfenapyr in Benin. Tropical Medicine and International Health, 14, 389–395.
Qayyum, M. A., Wakil, W., Arif, M. J., Sahi, S. T., Saeed, N. A., & Russell, D. A. (2015). Multiple resistances against formulated organophosphates, pyrethroids, and newer-chemistry insecticides in populations of Helicoverpa armigera (Lepidoptera: Noctuidae) from Pakistan. Journal of Economic Entomology, 108(1), 286–293.
Rehan, A., & Freed, S. (2015). Fitness cost of methoxyfenozide and the effects of its sublethal doses on development, reproduction, and survival of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). Neotropical Entomology, 44(5), 513–520.
Romero, A., Potter, M. F., & Haynes, K. F. (2010). Evaluation of chlorfenapyr for control of the bed bug, Cimex lectularius L. Pest Management Science, 66, 1243–1248.
Rust, M. K., & Saran, R. K. (2006). Toxicity, repellency, and transfer of chlorfenapyr against western subterranean termites (Isoptera: Rhinotermitidae). Journal of Economic Entomology, 99(3), 864–872.
Sparks, T. C., 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.
Tamilselvan, R., Kennedy, J. S., & Suganthi, A. (2021). Sublethal and transgenerational effects of spinetoram on the biological traits of Plutella xylostella (L.) (Lepidoptera: Plutellidae). Ecotoxicology, 30(4), 667–677.
Tang, Q., Xiang, M., Hu, H., An, C., & Gao, X. (2015). Evaluation of sublethal effects of sulfoxaflor on the green peach aphid (Hemiptera: Aphididae) using life table parameters. Journal of Economic Entomology, 108(6), 2720–2728.
Ullah, S., Shah, R. M., & Shad, S. A. (2016). Genetics, realized heritability and possible mechanism of chlorfenapyr resistance in Oxycarenus hyalinipennis (Lygaeidae: Hemiptera). Pesticide Biochemistry and Physiology, 133, 91–96.
Van Leeuwen, T., Stillatus, V., & Tirry, L. (2004). Genetic analysis and cross-resistance spectrum of a laboratory-selected chlorfenapyr resistant strain of two-spotted spider mite (Acari: Tetranychidae). Experimental and Applied Acarology, 32(4), 249–261.
Xu, C., Zhang, Z., Cui, K., Zhao, Y., Han, J., Liu, F., & Mu, W. (2016). Effects of sublethal concentrations of cyantraniliprole on the development, fecundity and nutritional physiology of the black cutworm agrotisipsilon (Lepidoptera: Noctuidae). PLoS One, 11(6), e0156555.
Zhang, S., Zhang, X., Shen, J., Mao, K., You, H., & Li, J. (2016). Susceptibility of field populations of the diamondback moth, Plutella xylostella, to a selection of insecticides in Central China. Pesticide Biochemistry and Physiology, 132, 38–46.
Zhao, Y., Wang, Q., Ding, J., Wang, Y., Zhang, Z., Liu, F., & Mu, W. (2018). Sublethal effects of chlorfenapyr on the life table parameters, nutritional physiology and enzymatic properties of Bradysia odoriphaga (Diptera: Sciaridae). Pesticide Biochemistry and Physiology, 148, 93–102.
Zhu, F., Lavine, L., O’Neal, S., Lavine, M., Foss, C., & Walsh, D. (2016). Insecticide resistance and management strategies in urban ecosystems. Insects, 7, 2.
Published
2021-10-20
How to Cite
Shumilova, P. A., Sennikova, N. A., Silivanova, E. A., & Levchenko, M. A. (2021). Biological responses in Musca domestica to fipronil and chlorfenapyr exposures . Regulatory Mechanisms in Biosystems, 12(4), 664-669. https://doi.org/10.15421/022191
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