Sulfoxaflor: A New Promising Insecticide in the Global Control of Dengue and Zika Vector Aedes aegypti (Diptera: Culicidae) Mosquito

Transcription

1 Advances in Environmental Biology, 10(3) March 2016, Pages: AENSI Journals Advances in Environmental Biology ISSN EISSN Journal home page: Sulfoxaflor: A New Promising Insecticide in the Global Control of Dengue and Zika Vector Aedes aegypti (Diptera: Culicidae) Mosquito 1 Mohamed Ahmed Ibrahim Ahmed and 2,3 Christoph Franz Adam Vogel 1 Plant Protection Department, Faculty of Agriculture, Assiut University, Assiut 71526, Egypt. 2 Center for Health and the Environment, 3 Environmental Toxicology Department, University of California, Davis, CA 95616, USA Address For Correspondence: Mohamed Ahmed, Plant Protection Department, Faculty of Agriculture, Assiut University, Assiut 71526, Egypt. Phone: ; Fax: ; maiaf2000@gmail.com This work is licensed under the Creative Commons Attribution International License (CC BY). Received 12 February 2016; Accepted 28 April 2016; Available online 24 May 2016 ABSTRACT Background: Sufloximines are new class of insecticides that are effective against certain insect pests. Sulfoxaflor is the initial sulfoximine compound that demonstrates precise mode of action by acting on the insect nicotinic acetylcholine receptors (nachrs). Detailed understanding of the potency of sulfoxaflor against mosquitoes is a substantial approach in vector control. Objective: To evaluate the toxicological efficacy of sulfoxaflor compared with selected neonicotinoid pesticides on fourth instar of Aedes aegypti larvae and adults. Further, we assessed the synergistic actions of piperonyl butoxide (PBO) and two octopamine receptor agonists, chlordimeform (CDM) and amitraz (AMZ), on sulfoxaflor insecticide against fourth instar and adults of Aedes aegypti. Results: Sulfoxaflor showed significant toxic effects on fourth instar larvae and adults of Aedes aegypti; however, in combination with piperonyl butoxide (PBO), chlordimeform (CDM), and amitraz (AMZ), the toxicity of sulfoxaflor was increased substantially as determined by the synergistic ratio (SR 50) assessed after 24, 48, and 72-h exposure. Among the tested synergists, AMZ increased the potency of sulfoxaflor on both fourth instar larvae and adults the most. Conclusion: Sulfoxaflor proved to be an effective tool in controlling Aedes aegypti. Thus, sulfoxaflor is an auspicious prospect for the control of Aedes aegypti mosquito, which spreads dengue fever and other diseases. KEYWORDS: Aedes aegypti, Sulfoxaflor, Mosquito control, Octopamine receptor agonists, Piperonyl butoxide, Neonicotinoids INTRODUCTION The development of resistance to neonicotinoid insecticides has constituted a major challenge in the control of Aedes aegypti L. [1-5]. Aedes aegypti, also known as the yellow fever mosquito, is known to spread dengue fever, chikungunya, yellow fever viruses, and other diseases around the world especially Zika virus which is an impact issue worldwide [6,7]. The increasing resistance of mosquitoes to conventional insecticide classes, including the neonicotinoid class, has led to a renewed interest in discover new insecticide tools and pest control strategies [8-14]. Sulfoxaflor is structurally related to sulfoximines, a new class of insecticide developed by Dow AgroSciences to control a broad range of sap-feeding insect pests, such as aphids and whiteflies, with resistance to other insecticides [15,16]. Importantly, sulfoxaflor acts on insect nicotinic acetylcholine receptors (nachrs) in the insect nervous system [17]. More interestingly, sulfoxaflor is not metabolized by cytochrome P450 monooxygenases involved in the detoxification of many classes of insecticides (e.g., neonicotinoids and spynosyns). This is due to sulfoxaflor lacking of the amine nitrogen that present in neonicotinoids, which is related to N-alkyl-hydroxylation/N-dealkylation as structure activity relationships (SAR) of sufloxaflor [18]. Copyright 2016 by authors and Copyright, American-Eurasian Network for Scientific Information (AENSI Publication).

2 172 Mohamed Ahmed Ibrahim Ahmed et al, 2016 To date, the potential toxicity of sulfoxaflor on mosquitoes has not been reported. The current study provides the first toxicological efficacy data on sulfoxaflor compared with selected neonicotinoid pesticides on fourth instar of Aedes aegypti larvae. Furthermore, to increase the toxicity of sulfoxaflor, we evaluate the synergistic actions of piperonyl butoxide (PBO) and two octopamine receptor agonists, chlordimeform (CDM) and amitraz (AMZ), on sulfoxaflor insecticide against fourth instar and adults of Aedes aegypti were assessed with the purpose of finding a new insecticide devoid of mosquito resistance. MATERIAL AND METHODS Mosquitoes: The FIELD strain (Fresno, CA) of Aedes aegypti was obtained from the laboratory of Dr. Thomas W. Scott, University of California, Davis, and was used for all experiments. The rearing regime was described recently by Ahmed and Vogel (2015) [2]. All procedures were reviewed by the Institutional Review Board (IRB) of the University of California, Davis. Chemicals: Sulfoxaflor (99.4%) was purchased from Chem Services (West Chester, PA, USA). Piperonyl butoxide (PBO: 99%), chlordimeform (CDM: 99.8%), amitraz (AMZ: 96.8%), thiamethoxam (99.5%), dinotefuran (99.5%), acetamiprid (99.5%), and imidacloprid (99.5%) were purchased from Sigma-Aldrich Co. (St. Louis, MO, USA). Larval Bioassays: Twenty-four instars larvae of uniform size were placed in 140-ml glass cups containing 99 ml of distilled water and 1 ml of insecticide (in acetone) solution. Only 1 ml of acetone was added for controls. Larvae were considered dead if they could not reach the surface of the water or they were unresponsive to touching with a probe. Based on the slow-acting nature of some of these insecticides, mortality was determined after 24, 48, and 72-h of exposure. Adult Bioassays: Adult bioassays were conducted in glass jars (600 ml) with an internal surface area of 65 cm 2 and treated with 1 ml of insecticide solution. For control, the internal surface was treated with only 1 ml of acetone. The treatments were coated evenly on the inner walls of the glass jars. Acetone was allowed to evaporate for 30 min. Then 20 adults (5-7 days old post-emergence) per glass jar were placed inside, and the opening was covered with double layered white mesh cheesecloth. Adults were considered dead if they were ataxic. As performed in the larvae bioassays, mortality was determined after 24, 48, and 72-h of exposure. Synergistic Action Bioassay: The synergistic action bioassay was conducted as described above for both larvae and adult bioassays. Controls received only acetone and were run concurrently with each series of tests. For both bioassays, each series of synergistic action tests was carried out by testing the lethal actions of varying concentrations of a test insecticide alone or co-administered with 10 µg/ml of PBO, CDM, or AMZ dissolved in 1 ml of acetone. After the addition of the insecticides, the test solution was stirred briefly to ensure uniform mixture for larvae bioassays and, for adult bioassays, the test solution was allowed to evaporate for 30 min. Initial tests indicated that 10 µg/ml of PBO was the maximum sublethal concentration at which mortality was not observed. However, our previous study on CDM and AMZ demonstrated that a concentration of 10 µg/ml did not cause mortality during the 72-h test period on fourth instar larvae of Aedes aegypti [5]. Further, at least five concentrations were used for all bioassays, and every bioassay was held at 25 o C. Percentage mortality was recorded after 24, 48, and 72-h exposure. Statistical Analysis: The corrected mortality was calculated according to Abbott's formula [19]. Bioassay data (LC 50 and 95% CL values) were analyzed using IBM SPSS Statistics Desktop, V22.0 (SPSS Inc., Chicago, IL). A synergistic action was determined to be significant at P 0.05 when the 95% CIs for the LC 50 values for larvae or adults exposed to insecticide alone did not overlap with those for larvae exposed to insecticide plus synergist mixtures. Synergistic ratio (SR) was calculated by dividing the LC 50 value of the test insecticide by that of the LC 50 obtained by the combined treatment with insecticide plus synergist. Figures were generated using GraphPad Prism 6.01 software (San Diego, CA, USA). Further, toxicity index calculated as [(LC 50 of the most toxic tested compound/lc 50 of the tested compound) 100].

3 173 Mohamed Ahmed Ibrahim Ahmed et al, 2016 RESULTS AND DISCUSSION The toxicity of sulfoxaflor in comparison to select neonicotinoids (thiamethoxam, dinotefuran, acetamiprid, and imidacloprid) on fourth instar larvae of Aedes aegypti after 24, 48, and 72- h of exposure is presented in Table 1and Figure 1. Sulfoxaflor was potent insecticide (LC 50 = 135, 108, and 78 ng/ml after 24, 48, and 72-h of exposure, respectively), followed by thiamethoxam (LC 50 = 147, 117, and 81 ng/ml after 24, 48, and 72- h of exposure, respectively). The neonicotinoid insecticide with the lowest toxicity was imidacloprid (LC 50 = 2079, 324, and 208 ng/ml after 24, 48, and 72-h of exposure, respectively). Based on the toxicity index after 24-h exposure by fourth instar larvae (Fig. 1), sulfoxaflor was more toxic than thiamethoxam, dinotefuran, acetamiprid, and imidacloprid by 1.09, 1.54, 4.70, and fold, respectively. Further, thiamethoxam was more toxic than dinotefuran, acetamiprid, and imidacloprid by 1.41, 4.31, and fold, respectively. The same pattern of toxicity was observed after 48 and 72-h of exposure. The toxicity and the synergism of sulfoxaflor alone and in combination with PBO, CDM, and AMZ on fourth instar larvae and adults of Aedes aegypti mosquitoes after 24, 48, and 72-h of exposure are shown in Tables 2-4, respectively. PBO significantly synergized sulfoxaflor, especially for the adult mosquitoes (adult LC 50 value for sulfoxaflor alone was 69, 1.6, ng/cm 2 after 24, 48, 72-h, respectively, while with PBO, the adult LC 50 was 19.2, 0.31, and ng/cm 2 after 24, 48, 72-h, respectively). CDM significantly synergized the toxicity of sulfoxaflor on both fourth instar larvae and adults, although the synergism was stronger on the adults after 48 and 72-h of exposure. AMZ plus sulfoxaflor had the greatest synergism, especially on adults after 72-h of exposure (Table: LC 50 = ng/cm 2 ). Noticeably, synergism was more evident when mosquitoes were cotreated with sulfoxaflor and AMZ rather than with PBO or CDM on both fourth instar larvae and adults; for example, AMZ caused sulfoxaflor to increase its toxicity fold after 48-h and fold after 72-h compared to 24-h on fourth instar larvae (Fig. 2A), while PBO caused sulfoxaflor to increase its toxicity only 2.5-fold after 48-h and 10.2-fold after 72-h (Fig. 2B). Compounds n a Table 1: Toxicity of sulfoxaflor in comparison with select neonicotinoid insecticides on fourth instars of Aedes aegypti after 24, 48, and 72- h exposure b b b LC 50 LC Slope (±SE) 50 LC Slope (±SE) 50 Slope (±SE) After 24-h After 48-h After 72-h Sulfoxaflor (±0.49) 3.7 (±0.20) ( ) (40-432) (38-329) 3.4 (±0.23) Thiamethoxam (±0.32) 4.6 (±0.41) (81-370) (92-272) (61-395) 4.3 (±0.38) Dinotefuran (±0.54) 4.3 (±0.32) ( ) (64-296) (52-411) 4.6 (±0.27) Acetamiprid (±0.37) (±0.25) (±0.46) ( ) ( ) Imidacloprid (±0.26) ( ) ( ) a n = number of larvae tested, including control b Concentration is expressed in ng/ml and the response determined after 24, 48, and 72-h 3.8 (±0.27) (69-497) 208 (73-427) 3.9 (±0.31) There is an urgent need for the continued discovery of new compounds that have unique chemical and physical properties as well as mode of action as pesticide resistance rises. Unfortunately, real and perceived constraints have limited the discovery and development of new chemical compounds in the field of plant protection. However, the agrochemical industry has reacted by developing new effective compounds that while toxic to insect pests, are respectful to the environmental components. Sulfoxaflor is a new insecticide that acts on nachrs in susceptible insects, yet is classified as a nicotinic acetylcholine receptor agonist [20-22]. Since the efficacy of sulfoxaflor on Aedes aegypti has not been reported, we initially investigated the effect of sulfoxaflor on fourth instar larvae and adults under laboratory conditions. We found that sulfoxaflor showed significant toxicity against fourth instar larvae in comparison with selected neonicotinoid pesticides. Further, the selected neonicotinoid pesticides were shown toxic effects on the larvae stage. Given that PBO, CDM, and AMZ, were important in the metabolism or the enhancement of the toxicity on the selected insecticides. In the presence of the synergists, PBO, CDM, and AMZ, toxicity increased dramatically, especially after 48 and 72 hours of exposure. Furthermore, there was trend of increased synergistic toxicity that was greater on adults than on fourth instar larvae. The synergistic action that occurs via the octopamine receptor was greatest with AMZ and was most apparent after 72 hours of exposure by both fourth instar larvae and adults. These results agree with a previous study that revealed similar toxic effects of the synergists on Aedes aegypti [2,5,23].

4 174 Mohamed Ahmed Ibrahim Ahmed et al, 2016 Fig. 1: Toxicity index of sulfoxaflor in comparison to select neonicotinoid insecticides on fourth instar larvae of Aedes aegypti after 24-h (A), 48-h (B), and 72-h (C) of exposure. Toxicity index = [(LC 50 of the most toxic tested compound/lc 50 of the tested compound) 100]. Table 2: Toxicity and synergism of sulfoxaflor alone or with co-administered synergist on Aedes aegypti fourth instar larvae and adults after 24-h exposure Compounds n a b LC 50 Slope (± SE) SR c On fourth instar larvae Sulfoxaflor ( ) 5.8 (± 0.49) - Sufloxaflor + PBO d (75-234) 3.8 (± 0.55) 1.3 Sufloxaflor + CDM d (44-141) 5.0 (± 0.28) 2.0 * Sufloxaflor + AMZ d (23-79) 4.4 (± 0.24) 3.6 * On adults Sulfoxaflor (29-268) 5.1 (± 0.15) - Sufloxaflor + PBO (11-63) 3.7 (± 0.23) 3.6 * Sufloxaflor + CDM (6-38) 3.2 (± 0.31) 7.8 * Sufloxaflor + AMZ (1-19) 3.8 (± 0.28) 16.3 * a n, number of larvae or adults tested, including control b Concentrations are expressed in ng/ml for fourth instar larvae and ng/cm 2 for adults. The response was determined after 24- h. c SR, synergistic ratio. Calculated by dividing the LC for insecticide by the LC of insecticide + synergist. d Concentration of synergist was 10 µg/ml * SR significantly different from control without synergist (=1.0) at (P 0.05)

5 175 Mohamed Ahmed Ibrahim Ahmed et al, 2016 Table 3: Toxicity and synergism of sulfoxaflor alone or with co-administered synergist on Aedes aegypti fourth instar larvae and adults after 48-h exposure Compounds n a b LC 50 Slope (± SE) SR c On fourth instar larvae Sulfoxaflor (40-432) 3.7 (± 0.20) - Sufloxaflor + PBO d (26-83) 4.8 (± 0.25) 2.5 * Sufloxaflor + CDM d (11-201) 2.6 (± 0.23) 3.5 * Sufloxaflor + AMZ d ( ) 5.1 (± 0.53) 12.1 * On adults Sulfoxaflor ( ) 3.6 (± 0.11) - Sufloxaflor + PBO ( ) 3.4 (± 0.28) 5.2 * Sufloxaflor + CDM ( ) 3.1 (± 0.34) 11.4 * Sufloxaflor + AMZ ( ) 3.7 (± 0.22) 21.8 * a n, number of larvae or adults tested, including control b Concentrations are expressed in ng/ml for fourth instar larvae and ng/cm 2 for adults. The response was determined after 48-h. c SR, synergistic ratio. Calculated by dividing the LC for insecticide by the LC of insecticide + synergist. d Concentration of synergist was 10 µg/ml * SR significantly different from control without synergist (=1.0) at (P 0.05) Table 4: Toxicity and synergism of sulfoxaflor alone or with co-administered synergist on Aedes aegypti fourth instar larvae and adults after 72-h exposure Compounds n a b LC 50 Slope (± SE) SR c On fourth instar larvae Sulfoxaflor (38-329) 3.4 (± 0.23) - Sufloxaflor + PBO d ( ) 4.3 (± 1.22) 10.3 * Sufloxaflor + CDM d ( ) 3.1 (± 0.24) 13.7 * Sufloxaflor + AMZ d ( ) 3.7 (± 0.61) 16.3 * On adults Sulfoxaflor ( ) 3.0 (± 0.14) - Sufloxaflor + PBO ( ) 4.2 (± 0.36) 8.3 * Sufloxaflor + CDM ( ) 3.9 (± 0.29) 17.6 * Sufloxaflor + AMZ ( ) 3.6 (± 0.33) 29.6 * a n, number of larvae or adults tested, including control b Concentrations are expressed in ng/ml for fourth instar larvae and ng/cm 2 for adults. The response was determined after 72- h. c SR, synergistic ratio. Calculated by dividing the LC for insecticide by the LC of insecticide + synergist. d Concentration of synergist was 10 µg/ml * SR significantly different from control without synergist (=1.0) at (P 0.05) Synergistic Ratio (SR 50) (A) On fourth instar larvae Sulfoxaflor + PBO Sulfoxaflor + CDM Sulfoxaflor + AMZ Time (h) 35 (B) On adults Synergistic Ratio (SR 50) Time (h) Sulfoxaflor + PBO Sulfoxaflor + CDM Sulfoxaflor + AMZ Fig. 2: Time-dependent changes in the synergistic ratio (SR 50 ) on fourth instar larvae (A) and on adults (B) of Aedes aegypti as calculated from LC 50 values from Tables 4-6 for combined treatments with PBO, CDM, and AMZ as assessed 24, 48, and 72-h after initial exposure.

6 176 Mohamed Ahmed Ibrahim Ahmed et al, 2016 In view of the significant synergism between octopamine receptor agonists and sulfoxaflor, Ahmed et al. (2015) [3] explained that the molecular base of this synergism is likely activation of the OR signaling in the brain of adult Culex pipiens mosquitoes. Interestingly, octopamine causes activation of cyclic adenosine monophosphate (camp) which indicating this basic mechanism does indeed operate in this species. In some insects, elevation of camp by octopamine directly causes the loss of appetite because it likely due to acceleration of the process of energy exhaustion in those affected insects. [3,24]. Sulfoxaflor s potent toxicity has been shown towards many insect pests, in particular, the sap-feeding pests even under field conditions [15,21,25]. In a previous study on Cotton aphids, Aphis gossypii Glover, LC 50 values for sulfoxaflor ranged from 1.01 to 5.85 ppm and 0.92 to 4.13 ppm at 48 and 72 hours, respectively, on collected strains from different cotton fields across the states of Mississippi, Louisiana, Arkansas, Tennessee, and Texas. Sulfoxaflor demonstrated effective control of cotton aphids in areas where thiamethoxam resistance occurred [15]. In another study, Bemisia tabaci developed a very low resistance ratio (RR) to sulfoxaflor compared to imidacloprid (RR up to 1000-fold) and cross-resistance to selected neonicotinoid pesticides [16]. In the same study, no cross-resistance was found between sulfoxaflor and imidacloprid on Trialeurodes vaporariorum. One valuable factor which worth consideration, sulfoxaflor is not metabolized by enzymes such as monooxygenase that are involved in insecticide resistance development, thereby, resulting in the lack of resistance and crossresistance issues [17]. Given these advantages, sulfoxaflor will be a remarkable pesticide in the global control of Dengue and Zika vector Aedes aegypti mosquito in the future. Conclusion: The results of this study reveal that sulfoxaflor is a new promising insecticide as demonstrated by its high level of potency compared to other select neonicotinoid pesticides. Numerous pests have developed resistance to neonicotinoid pesticides; however, sulfoxaflor has different chemical and biological properties and is also active on a wide range of insect pests. Thus, sulfoxaflor has the potential to be an important component in the field of pest control. Further biochemical and molecular biological investigation will give a better insight in to sulfoxaflor s mode of action, and field experiments are needed to elucidate the promising efficacy of this unique insecticide. ACKNOWLEDGEMENTS The senior author was supported and funded with a grant (SAB 1918) from the Ministry of Higher Education of the Government of Egypt. We are grateful to Prof. Dr. Thomas W. Scott, Department of Entomology and Nematology, University of California, Davis for kindly providing us with Aedes aegypti eggs that were used for this study. REFERENCES [1] Kushwah, R.B., C.L. Dykes, N. Kapoor, T. Adak, O.P. Singh, Pyrethroid-resistance and presence of two knockdown resistance (kdr) mutations, F1534C and a novel mutation T1520I, in Indian Aedes aegypti. PLOS Neglected Tropical Diseases. 9: e3332. [2] Ahmed, M.A.I., C.F.A. Vogel, Synergistic action of octopamine receptor agonists on the activity of selected novel insecticides for control of Dengue vector Aedes aegypti (Diptera: Culicidae) mosquito. Pesticide Biochemistry and Physiology, 120: [3] Ahmed, M.A.I., C.F.A. Vogel, F. Matsumura, Unique biochemical and molecular biological mechanism of synergistic actions of formamidine compounds on selected pyrethroid and neonicotinoid insecticides on the fourth instar larvae of Aedes aegypti (Diptera: Culicidae). Pesticide Biochemistry and Physiology, 120: [4] Liu, N., Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annual Review of Entomology, 60: [5] Ahmed, M.A.I., F. Matsumura, Synergistic actions of formamidine insecticides on the activity of pyrethroids and neonicotinoids against Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology, 49: [6] Ahmed, M.A.I., C.F.A. Vogel, The role of octopamine receptor agonists in the synergistic toxicity of certain insect growth regulators (IGRs) in controlling Dengue vector Aedes aegypti (Diptera: Culicidae) mosquito. Acta Tropica., 155: 1-5. [7] Al-Qahtani, A.A., N. Nazir, M.R. Al-Anazi, S. Rubino, M.N. Al-Ahdal, Zika virus: a new pandemic threat. Journal of infection in developing countries, 10(3): [8] Kaufman, P.E., S.C. Nunez, R.S. Mann, C.J. Geden, M.E. Scharf, Neonicotinoid and pyrethroid insecticide resistance in houseflies (Diptera: Muscidae) collected from Florida dairies. Pest Management Science, 66: [9] Wang, Z., H. Yan, Y. Yang, Y. Wu, Biotype and insecticide resistance status of the whitefly, Bemisia tabaci from China. Pest Management Science, 66:

7 177 Mohamed Ahmed Ibrahim Ahmed et al, 2016 [10] Karatolos, N., I. Denholm, M. Williamson, R. Nauen, K. Gorman, Incidence and characterization of resistance to neonicotinoid insecticides and pymetrozine in the greenhouse whitefly, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae). Pest Management Science, 66: [11] Schuster, D.J., R.S. Mann, M. Toapanta, R. Cordero, S. Thompson, S. Cyman, A. Shurtleff, R.F. Morris II Monitoring neonicotinoid resistance in biotype B of Bemisia tabaci in Florida. Pest Management Science, 66: [12] Srigiriraju, L., P.J. Semtner, J.R. Bloomquist, Monitoring for imidacloprid resistance in the tobaccoadapted form of the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in the eastern United States. Pest Management Science, 66: [13] David, J.P., F. Faucon, A. Chandor-Proust, R. Poupardin, M.A. Riaz, A. Bonin, V. Navratil, S. Reynaud, Comparative analysis of response to selection with three insecticides in the dengue mosquito Aedes aegypti using mrna sequencing. BMC Genomics, 15: 174. [14] Riaz, M.A., A. Chandor-Proust, C. Dauphin-Villemant, R. Poupardin, C.M. Jones, C. Strode, M. Régent- Kloeckner, J.P. David, S. Reynaud, Molecular mechanisms associated with increased tolerance to the neonicotinoid insecticide imidacloprid in the dengue vector Aedes aegypti. Aquatic Toxicology, 126: [15] Gore, J., D. Cook, A. Catchot, B.R. Leonard, S.D. Stewart, G. Lorenz, D. Kerns, Cotton aphid (Heteroptera: Aphididae) susceptibility to commercial and experimental insecticides in the southern United States. Journal of Economic Entomology, 106: [16] Longhurst, C., J.M. Babcock, I. Denholm, K. Gorman, J.D. Thomas, T.C. Sparks, Cross-resistance relationships of the sulfoximine insecticide sulfoxaflor with neonicotinoids and other insecticides in the whiteflies Bemisia tabaci and Trialeurodes vaporariorum. Pest Manag. Sci., 69: [17] Sparks, T.C., G.B. Watson, M.R. Loso, C. Geng, J.M. Babcock, J.D. Thomas, Sulfoxaflor and the sulfoximine insecticides: chemistry, mode of action and basis for efficacy on resistant insects. Pesticide Biochemistry and Physiology, 107: 1-7. [18] Sparks, T.C., G.J. DeBoer, N.X. Wang, J.M. Hasler, M.R. Loso, G.B. Watson, Differential metabolism of sulfoximine and neonicotinoid insecticides by Drosophila melanogaster monooxygenase CYP6G1. Pesticide Biochemistry and Physiology, 103: [19] Abbott, W.S., A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18: [20] Babcock, J.M., C.B. Gerwick, J.X. Huang, M.R. Loso, G. Nakamura, S.P. Nolting, R.B. Rogers, T.C. Sparks, J. Thomas, G.B. Watson, Y. Zhu Biological classification of sulfoxaflor, a novel insecticide. Pest Management Science, 67: [21] Watson, G.B., M.R. Loso, J.M. Babcock, J.M. Hasler, T.J. Letherer, C.D. Young, Y. Zhu, J.E. Casida, T.C. Sparks, Novel nicotinic action of the sulfoximine insecticide sulfoxaflor. Insect Biochemistry and Molecular Biology, 41: [22] Zhu, Y., M.R. Loso, G.B. Watson, T.C. Sparks, R.B. Rogers, J.X. Huang, B.C. Gerwick, J.M. Babcock, D. Kelly, V.B. Hegde, B.M. Nugent, J.M. Renga, I. Denholm, K. Gorman, G.J. DeBoer, J. Hasler, T. Meade, J.D. Thomas, Discovery and characterization of sulfoxaflor, a novel insecticide targeting sap-feeding insects. Journal of Agricultural and Food Chemistry, 59: [23] Paul, A., L.C. Harrington, J.G. Scott, Evaluation of novel insecticides for control of dengue vector Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology, 43: [24] Pratt, S., S.C. Pryor, Dopamine- and octopamine-sensitive adenylate cyclase in the brain of adult Culex pipiens mosquitoes, Cellular and Molecular Neurobiology, 6: [25] Smith, H.A., M.C. Giurcanu, New insecticides for management of tomato yellow leaf curl, a virus vectored by the Silverleaf whitefly, Bemisia tabaci. Journal of Insect Science, 14: 183.