TY - JOUR
AU - Brown, Michelle, Q
AB - Abstract The peridomestic anthropophilic Aedes aegypti L. (Diptera: Culicidae) is originated from the wild zoophilic subspecies Aedes aegypti formosus in sub-Saharan Africa, and currently has a broad distribution in human-modified environments of the tropics and subtropics worldwide. In California, breeding populations were initially detected in 2013 in the cities of Fresno, Madera, and San Mateo, and now can be found in 188 cities of 12 counties in the state. Recent genetic studies suggest that this species invaded California on multiple occasions from several regions of the United States and northern Mexico prior to initial detection. As an invasive species and vector for numerous arboviruses, Ae. aegypti is a primary target of surveillance and control in California. In southern California city of Montclair, a population was identified in September 2015, from which a short-term colony was established in an insectary. The susceptibility of this field population to commonly used pesticides with various modes of action, including 15 formulations against larvae and four against adults, was determined, in reference to a susceptible laboratory colony of the same species. No resistance was shown to most pesticides tested. However, tolerance or reduced susceptibility to spinosad, spinetoram, diflubezuron, and fipronil was detected, and modest levels of resistance to pyriproxyfen (resistance ratio = 38.7-fold at IE50 and 81.5-fold at IE90) was observed. Results are discussed based on the field usage and modes of action of the pesticides tested. Strategic selection and application of pesticides against this population of Ae. aegypti in the urban environments should be taken into consideration. Aedes aegypti, resistance, susceptibility, larvicide, adulticide The peridomestic anthropophilic yellow fever mosquito Aedes (Stegomyia) aegypti L. or Aedes aegypti aegypti, from an evolutionary point of view, is originated from the wild zoophilic subspecies Aedes aegypti formosus from sub-Saharan Africa (Powell and Tabachnick 2013) and is widely distributed in human-modified environments in the tropics and subtropics worldwide. This species serves as an important vector for arboviruses such as chikungunya, dengue, Mayaro, Rift Valley fever, yellow fever, and Zika viruses (Weaver and Reisen 2010, Long et al. 2011, Musso and Gubler 2016). Aedes aegypti was likely brought to the Americas by European slave ships during the 15th to 17th centuries (Powell and Tabachnick 2013). In the United States, Ae. aegypti populations are distributed throughout most of the southern states, especially below the 33° north latitude line (Hahn et al. 2016). In California, breeding populations were initially detected in 2013 in the cities of Fresno, Madera, and San Mateo and are now found in 188 cities of 12 counties in the state (Porse et al. 2015, Metzger et al. 2017, CDPH 2018). Genetic studies suggest that this species invaded California on multiple occasions from several regions of the United States and northern Mexico with the aid of humans prior to initial detection (Pless et al. 2017). As an important vector of arboviruses and a major nuisance species, Ae. aegypti is a primary target of surveillance and control in California and elsewhere. Unfortunately, frequent exposure of Ae. aegypti populations to pesticides for other pestiferous arthropods in urban and agricultural areas has led to increased pesticide tolerance and difficulty in controlling this species (Poupardin et al. 2008, Marcombe et al. 2012, WHO 2014, Corbel et al. 2017, Moyes et al. 2017). On 22 September 2015, a female Ae. aegypti was first discovered in a gravid trap at a residence in Montclair, CA, during routine surveillance for Culex mosquitoes. The origin of this female mosquito was unknown as to whether it was an independent introduction or had spread from an earlier invasion. A short-term colony was established in an insectary using subsequent larval collections from this residence. In our study, we investigated this Ae. aegypti population’s pesticide susceptibility profile and resistance development to a variety of off-the-shelf pesticides used for the control of immature and adult arthropods. Fifteen pesticide formulations (13 active ingredients) currently registered to control mosquito larvae or other urban pest species were assayed against larval stages, and four pesticide formulations (four pyrethroids and one organophosphate) were assayed against the adult stage of this Ae. aegypti population. Results are discussed based on modes of action of the pesticides tested. Strategic selection and application of pesticides against specific populations of Ae. aegypti in urban environments are warranted. Materials and Methods Mosquitoes Approximately 200 early and late instar larvae were collected from the infested residence in Montclair, CA on 23 September 2015. Specimens were confirmed to be Ae. aegypti from third and fourth instar larvae from the field collections. Collected larvae were reared to adults and then propagated to F1 and F2 generations. The third or fourth instar larvae were used in cup bioassays on 15 pesticide formulations against larvae, while 3–5-d-old female adults were challenged in bottle bioassays against four adulticide formulations. A susceptible population provided by the Navy Entomology Center of Excellence (Jacksonville, FL) was also bioassayed under the same conditions for resistance ratio calculations. Pesticides The pesticides used to evaluate larval susceptibility of the Ae. aegypti field population were off-the-shelf products, including seven biological pesticide formulations of microbial origins (Bacillus thuringiensis subsp. israelensis, Lysinibacillus sphaericus, a combination of Bti and L. sphaericus, spinosad, spinetoram, and abamectin); four insect growth regulators (IGRs) (methoprene, pyriproxyfen, diflubenzuron and novaluron); and one from each of organophosphate (temephos), neonicotinoid (imidacloprid), phenylpyrazoles (fipronil), and oxadiazine (indoxacarb). The adult susceptibility to four pyrethroids (permethrin, resmethrin, prallethrin and sumethrin, with or without piperonyl butoxide, PBO) and one organophosphate (malathion) was also evaluated. The detailed information of these products including active ingredients and manufacturers are provided in Table 1. Table 1. Pesticides tested for susceptibility profile of Aedes aegypti L. originated from field collections in Montclair, CA Category Products Active ingredients Concentration (%) Manufacturers Pesticides against larvae Pesticides of microbial origins VectoBac WDG Bacillus thuringiensis israelensis (B.t.i.) 51.2 Valent BioSciences Corp., Libertyville, IL. WVBti SG3 B.t.i. 4.3 West Valley MVCD, Ontario, CA VectoLex WDG L. sphaericus 37.4 Valent BioSciences Corp., Libertyville, IL. VectoMax CG B.t.i. + L. sphaericus 4.5 + 2.7 Valent BioSciences Corp., Libertyville, IL. Natular G30 Spinosad 2.5 Clarke, St. Charles, IL. Radiant Spinetoram 11.7 Dow AgroSciences LLC, Indianapolis, IN Advance 375A Abamectin B1 0.011 BASF Corp., St. Louis, MO Insect growth regulators (IGR) Altosid liquid larvicide Methoprene 5.0 Wellmark International, Schaumburg, IL NyGuard IGR Pyriproxyfen 10.0 MGK, Minneapolis, MN Dimilin 25W Diflubenzuron 25.0 Chemtura Corp., Middlebury, CT Mosquiron 0.12CRD Novaluron 0.12 Makhteshim Agan NA Inc., Raleigh, NC Organophosphate Skeeter Abate Temephos 5.0 Clarke, St. Charles, IL Neonicotinoid ImidaPro 4SC Imidacloprid 40.7 Agrisel USA, Inc., Suwanee, GA Phenylpyrazole Taurus SC Fipronil 9.1 CSI Control Solutions, Inc., Pasadena, TX Oxadiazine Advion RIFA bait Indoxacarb 0.045 DuPont, Wilmington, DE Pesticides against adults Pyrethroids Permethrin (technical) Permethrin 99.5 ChemServices, West Chester, PA Scourge 18 + 54 Resmethrin + PBO 18.0 + 54.0 Bayer, Research Triangle, NC Aquaduet Prallethrin + Sumethrin + PBO 1.0 + 5.0 + 5.0 Clarke, St. Charles, IL Spectracide Malathion 50.0 Spectracide, St. Louis, MO Category Products Active ingredients Concentration (%) Manufacturers Pesticides against larvae Pesticides of microbial origins VectoBac WDG Bacillus thuringiensis israelensis (B.t.i.) 51.2 Valent BioSciences Corp., Libertyville, IL. WVBti SG3 B.t.i. 4.3 West Valley MVCD, Ontario, CA VectoLex WDG L. sphaericus 37.4 Valent BioSciences Corp., Libertyville, IL. VectoMax CG B.t.i. + L. sphaericus 4.5 + 2.7 Valent BioSciences Corp., Libertyville, IL. Natular G30 Spinosad 2.5 Clarke, St. Charles, IL. Radiant Spinetoram 11.7 Dow AgroSciences LLC, Indianapolis, IN Advance 375A Abamectin B1 0.011 BASF Corp., St. Louis, MO Insect growth regulators (IGR) Altosid liquid larvicide Methoprene 5.0 Wellmark International, Schaumburg, IL NyGuard IGR Pyriproxyfen 10.0 MGK, Minneapolis, MN Dimilin 25W Diflubenzuron 25.0 Chemtura Corp., Middlebury, CT Mosquiron 0.12CRD Novaluron 0.12 Makhteshim Agan NA Inc., Raleigh, NC Organophosphate Skeeter Abate Temephos 5.0 Clarke, St. Charles, IL Neonicotinoid ImidaPro 4SC Imidacloprid 40.7 Agrisel USA, Inc., Suwanee, GA Phenylpyrazole Taurus SC Fipronil 9.1 CSI Control Solutions, Inc., Pasadena, TX Oxadiazine Advion RIFA bait Indoxacarb 0.045 DuPont, Wilmington, DE Pesticides against adults Pyrethroids Permethrin (technical) Permethrin 99.5 ChemServices, West Chester, PA Scourge 18 + 54 Resmethrin + PBO 18.0 + 54.0 Bayer, Research Triangle, NC Aquaduet Prallethrin + Sumethrin + PBO 1.0 + 5.0 + 5.0 Clarke, St. Charles, IL Spectracide Malathion 50.0 Spectracide, St. Louis, MO View Large Table 1. Pesticides tested for susceptibility profile of Aedes aegypti L. originated from field collections in Montclair, CA Category Products Active ingredients Concentration (%) Manufacturers Pesticides against larvae Pesticides of microbial origins VectoBac WDG Bacillus thuringiensis israelensis (B.t.i.) 51.2 Valent BioSciences Corp., Libertyville, IL. WVBti SG3 B.t.i. 4.3 West Valley MVCD, Ontario, CA VectoLex WDG L. sphaericus 37.4 Valent BioSciences Corp., Libertyville, IL. VectoMax CG B.t.i. + L. sphaericus 4.5 + 2.7 Valent BioSciences Corp., Libertyville, IL. Natular G30 Spinosad 2.5 Clarke, St. Charles, IL. Radiant Spinetoram 11.7 Dow AgroSciences LLC, Indianapolis, IN Advance 375A Abamectin B1 0.011 BASF Corp., St. Louis, MO Insect growth regulators (IGR) Altosid liquid larvicide Methoprene 5.0 Wellmark International, Schaumburg, IL NyGuard IGR Pyriproxyfen 10.0 MGK, Minneapolis, MN Dimilin 25W Diflubenzuron 25.0 Chemtura Corp., Middlebury, CT Mosquiron 0.12CRD Novaluron 0.12 Makhteshim Agan NA Inc., Raleigh, NC Organophosphate Skeeter Abate Temephos 5.0 Clarke, St. Charles, IL Neonicotinoid ImidaPro 4SC Imidacloprid 40.7 Agrisel USA, Inc., Suwanee, GA Phenylpyrazole Taurus SC Fipronil 9.1 CSI Control Solutions, Inc., Pasadena, TX Oxadiazine Advion RIFA bait Indoxacarb 0.045 DuPont, Wilmington, DE Pesticides against adults Pyrethroids Permethrin (technical) Permethrin 99.5 ChemServices, West Chester, PA Scourge 18 + 54 Resmethrin + PBO 18.0 + 54.0 Bayer, Research Triangle, NC Aquaduet Prallethrin + Sumethrin + PBO 1.0 + 5.0 + 5.0 Clarke, St. Charles, IL Spectracide Malathion 50.0 Spectracide, St. Louis, MO Category Products Active ingredients Concentration (%) Manufacturers Pesticides against larvae Pesticides of microbial origins VectoBac WDG Bacillus thuringiensis israelensis (B.t.i.) 51.2 Valent BioSciences Corp., Libertyville, IL. WVBti SG3 B.t.i. 4.3 West Valley MVCD, Ontario, CA VectoLex WDG L. sphaericus 37.4 Valent BioSciences Corp., Libertyville, IL. VectoMax CG B.t.i. + L. sphaericus 4.5 + 2.7 Valent BioSciences Corp., Libertyville, IL. Natular G30 Spinosad 2.5 Clarke, St. Charles, IL. Radiant Spinetoram 11.7 Dow AgroSciences LLC, Indianapolis, IN Advance 375A Abamectin B1 0.011 BASF Corp., St. Louis, MO Insect growth regulators (IGR) Altosid liquid larvicide Methoprene 5.0 Wellmark International, Schaumburg, IL NyGuard IGR Pyriproxyfen 10.0 MGK, Minneapolis, MN Dimilin 25W Diflubenzuron 25.0 Chemtura Corp., Middlebury, CT Mosquiron 0.12CRD Novaluron 0.12 Makhteshim Agan NA Inc., Raleigh, NC Organophosphate Skeeter Abate Temephos 5.0 Clarke, St. Charles, IL Neonicotinoid ImidaPro 4SC Imidacloprid 40.7 Agrisel USA, Inc., Suwanee, GA Phenylpyrazole Taurus SC Fipronil 9.1 CSI Control Solutions, Inc., Pasadena, TX Oxadiazine Advion RIFA bait Indoxacarb 0.045 DuPont, Wilmington, DE Pesticides against adults Pyrethroids Permethrin (technical) Permethrin 99.5 ChemServices, West Chester, PA Scourge 18 + 54 Resmethrin + PBO 18.0 + 54.0 Bayer, Research Triangle, NC Aquaduet Prallethrin + Sumethrin + PBO 1.0 + 5.0 + 5.0 Clarke, St. Charles, IL Spectracide Malathion 50.0 Spectracide, St. Louis, MO View Large Bioassays Cup bioassay on pesticides against larvae Bioassays were conducted as described previously (Su and Mulla 2004; Su et al. 2018a,b). To prepare the bioassay treatment, the emulsifiable concentrate (EC) formulations such as Radiant SC, Altosid liquid larvicide, NyGuard IGR, ImidaPro 4SC and Taurus SC, were suspended in tap water by gentle mixing. Small granules, as in VectoBac WDG, WV Bti SG3, VectoLex WDG, Natular G30, Advance 375A Ant Bait and Advion RIFA Bait, or wettable powders, as in Dimilin 25W, were suspended in tap water by vigorous shaking. Large granular materials of VectoMax CG, or pellets of Skeeter Abate, were pulverized in a coffee grinder (Hamilton Beach Custom Grind, Southern Pines, NC) at the maximum speed under intermittent mode, then suspended in tap water by vortexing for 3 min. For briquets, such as Mosquiron 0.12CRD, fine pieces were shaved off using a razor blade, and suspended in tap water by vortexing for 5 min (Vortex Mixer VX100, Labnet International, Inc., Edison, NJ) (Su et al. 2018a,b). Four to five concentrations resulting in approximately 5–95% mortality, plus untreated controls were used in the bioassay, with three replicates at each concentration. Twenty-five larvae were placed in 100 ml tap water in a 120-ml disposable Styrofoam cup in each replicate. In bioassays on Bti, a combination of Bti and L. sphaericus, spinetoram, abamectin, temephos, imidacloprid, fipronil and indoxacarb, late third instar larvae were used, and larval mortality was recorded at 24 h post-treatment. Early third instar larvae were used in bioassays on L. sphaericus, and larval mortality was recorded at 48 h post-treatment. In bioassays using diflubenzuron and novaluron, early third instar larvae were used, and results were recorded at 72 h post-treatment. Moribund larvae were read as dead. In bioassays of methoprene and pyriproxyfen, late fourth instar larvae were used, and mortality was read when all treated individuals emerged as adults, died prior to emergence or emerged incompletely. Three drops of 10% rabbit chow pellet suspension were added to each cup as larval food in all bioassays, except those treated with methoprene and pyriproxyfen where a small piece (approximately 100 mg) of a rabbit pellet was added to each bioassay cup to support larval development until pupation. A reference laboratory colony of the same species was assayed under the same conditions for susceptibility comparison (Su et al. 2018a,b). Bottle bioassay on pesticides against adults Bottle bioassays were conducted as described previously (Brogdon and McAllister 1998; Su et al. 2018a,b). Briefly, technical permethrin (99.9% purity, Chem Service, West Chester, PA) was dissolved in HPLC grade acetone (EMD Millipore, Temecula, CA), and serial dilutions were made to coat the interior of 250-ml glass bottle (Uline, Pleasant Prairie, WI) at 30 μg/bottle. The coating doses for other test materials were Scourge (resmethrin/PBO = 25/75 μg/bottle), AquaDuet (prallethrin/sumethrin/PBO = 0.5/2.5/2.5 μg/bottle), and Specttracide (malathion = 150 μg/bottle). The coating in each bottle was performed using 1 ml acetone to ensure even coverage for all test materials. An automatic roller (Fisher Scientific, Fisher Scientific, Hampton, NH) placed in a chemical fume hood (Hemco, Independence, MO) was used to ensure the evenness of the coating. Bottles for untreated control were coated by acetone only. All coated bottle surfaces were dried in the hood. Twenty-five of 3–5-d-old female mosquitoes were aspirated into each bottle. Mortality was read at 5, 10, 15, 30, 45, 60, 90, and 120 min. Three replicates were made. Mortality referred to individuals that did not show any movements of the body or appendages. Moribund ones were also read as dead. Bioassays were conducted at 25 ± 1°C and relative humidity of 50–60%. Bottle bioassays were also conducted under the same conditions on a reference laboratory colony of the same species for calculation of resistance ratios (RRs). Data Analysis The dose–mortality data in cup bioassays were analyzed using POLO-PC Probit Analysis (LeOra Software 1987) to generate LC50, LC90, their respective 95% confidence intervals (CIs), slope of the concentration–response line and data heterogeneity (χ2/df). Time–mortality data from the bottle bioassays were analyzed according to Throne et al. (1995) for calculations of LT50 and LT90 and their 95% CI and other parameters. Resistance ratios were calculated by LC (LT)Field/LC (LT)Lab. The significance in susceptibility levels and RRs were determined by separated 95% CIs of LC or LT levels between the field population and laboratory colony (Su et al. 2018a,b). Results Susceptibility to Pesticides Against Larvae Among the seven pesticide formulations of microbial origins, tolerance or reduced susceptibility to spinosad and spinetoram was observed at the LC50 levels, where the RRs were 2.19-fold to spinosad and 2.85-fold to spinetoram. This field population was highly susceptible to Bti, a combination of Bti and L. sphaericus, and abamectin, where the RRs ranged from 0.42 to 1.59-fold at LC50 and 0.22 to 1.66-fold at LC90. A greater than 3.75 ppm of VectoLex WDG was observed at LC50 levels, and LC90 was not measurable within the test range for both field and laboratory populations (Tables 2 and 3). Table 2. Susceptibility of larval Aedes aegypti L. originated from field collections in Montclair, CA to commonly used pesticides against larvae Pesticides Tested Aedes aegypti (F1-2)† Laboratory reference colony LC50 (ppm) (95% CI) LC90 (ppm) (95% CI) Slope χ2/df LC50 (ppm) (95% CI) LC90 (ppm) (95% CI) Slope χ2/df** B.t.i. (VectoBac WDG, 51.2%) 0.078 (0.048–0.128) 0.198 (0.122–0.857) 3.15 ± 0.30 2.05 0.088 (0.079–0.098) 0.152 (0.133–0.185) 5.43 ± 0.63 0.11 B.t.i. (WV SG3, 4.3%) 0.468 (0.405–0.534) 1.231 (1.031–1.564) 3.05 ± 0.31 0.66 0.373 (0.227–0.530) 0.929 (0.637–2.108) 3.24 ± 0.31 3.18 L. sphaericus (VectoLex WDG, 37.4%) >3.75 n/a n/a n/a >3.75 n/a n/a n/a B.t.i. + L. sphaericus (VectoMax FG, 4.5% + 2.7%) 0.875 (0.561–1.243) 1.853 (1.293–4.596) 3.94 ± 0.41 1.53 0.552 (0.397–0.828) 1.113 (0.762–2.896) 4.21 ± 0.42 3.14 Spinosad (Natular G30, 2.5%) 2.28 × 10−2 (2.00–2.60 × 10−2) 5.11 × 10−2 (4.30–6.41 × 10−2) 3.66 ± 0.33 0.25 1.04 × 10−2 (6.88 × 10−3–1.60 × 10−2) 2.19 × 10−2 (1.47–9.27 × 10−2) 3.96 ± 0.48 1.53 Spinetoram (Radiant, 11.7%) 1.47 × 10−2 (1.29–1.66 × 10−2) 3.35 × 10−2 (2.88–4.07 × 10−2) 3.59 ± 0.33 0.13 5.15 × 10−3 (3.51–7.49 × 10−3) 1.10 × 10−2 (7.49 × 10−3–3.08 × 10−2) 3.90 ± 0.43 1.31 Abamectin (Advance 375A, 0.011%) 1.20 × 10−2 (1.02–1.42 × 10−2) 4.06 × 10−2 (3.15–5.80 × 10−2) 2.42 ± 0.24 0.49 2.85 × 10−2 (1.89–5.32 × 10−2) 1.84 × 10−1 (6.50 × 10−2–8.87 × 10−1) 1.94 ± 0.26 1.67 Methoprene* (Altosid Liquid Larvicide, 5%) 5.04 × 10−3 (3.78–6.91 × 10−3) 4.05 × 10−2 (2.53–7.76 × 10−2) 1.42 ± 0.13 0.80 1.51 × 10−3 (9.49 × 10−4–2.13 × 10−3) 1.05 × 10−2 (7.15 × 10−3–1.84 × 10−2) 1.52 ± 0.20 0.61 Pyriproxyfen* (NyGuard IGR, 10%) 1.20 × 10−3 (9.01 × 10−4–1.70 × 10−3) 9.94 × 10−3 (5.83 × 10−3–2.15 × 10−2) 1.40 ± 0.14 0.37 3.10 × 10−5 (2.50–3.90 × 10−5) 1.22 × 10−4 (9.70 × 10−5–1.63 × 10−4) 2.17 ± 0.42 0.46 Diflubenzuron (Dimilin 25WP, 25%) 4.71 × 10−3 (3.96–5.62 × 10−3) 1.51 × 10−2 (1.20–2.06 × 10−2) 2.53 ± 0.22 0.13 1.63 × 10−3 (9.10 × 10−4–2.43 × 10−3) 2.42 × 10−2 (1.40–6.22 × 10−2) 1.10 ± 0.18 0.71 Novaluron (Mosquiron 0.12CRD, 0.12%) 1.34 × 10−3 (9.01 × 10−4–1.92 × 10−3) 3.59 × 10−3 (2.41–7.43 × 10−3) 2.98 ± 0.26 1.06 9.73 × 10−4 (8.50 × 10−4–1.12 × 10−3) 3.20 × 10−3 (2.54–4.37 × 10−3) 2.48 ± 0.26 0.89 Temephos (Skeeter Abate, 5%) 0.009 (0.007–0.010) 0.021 (0.018–0.027) 3.30 ± 0.35 0.44 0.009 (0.008–0.010) 0.016 (0.013–0.020) 5.59 ± 0.75 0.43 Imidacloprid (ImadPro 4SC, 40.7%) 0.106 (0.065–0.174) 0.320 (0.190–0.877) 2.66 ± 0.22 1.44 0.151 (0.125–0.181) 0.412 (0.330–0.550) 2.94 ± 0.28 0.18 Fipronil (Taurus SC, 9.1%) 7.18 × 10−3 (6.35–8.30 × 10−3) 1.93 × 10−2 (1.52–2.73 × 10−2) 2.98 ± 0.37 0.29 2.58 × 10−3 (2.14–3.37 × 10−3) 8.69 × 10−3 (5.95 × 10−3–1.56 × 10−2) 2.44 ± 0.34 0.55 Indoxacarb (Advion RIFA bait, 0.045%) 0.095 (0.063–0.144) 0.317 (0.198–0.728) 2.45 ± 0.21 2.18 0.100 (0.075–0.127) 0.327 (0.251–0.459) 2.48 ± 0.27 0.49 Pesticides Tested Aedes aegypti (F1-2)† Laboratory reference colony LC50 (ppm) (95% CI) LC90 (ppm) (95% CI) Slope χ2/df LC50 (ppm) (95% CI) LC90 (ppm) (95% CI) Slope χ2/df** B.t.i. (VectoBac WDG, 51.2%) 0.078 (0.048–0.128) 0.198 (0.122–0.857) 3.15 ± 0.30 2.05 0.088 (0.079–0.098) 0.152 (0.133–0.185) 5.43 ± 0.63 0.11 B.t.i. (WV SG3, 4.3%) 0.468 (0.405–0.534) 1.231 (1.031–1.564) 3.05 ± 0.31 0.66 0.373 (0.227–0.530) 0.929 (0.637–2.108) 3.24 ± 0.31 3.18 L. sphaericus (VectoLex WDG, 37.4%) >3.75 n/a n/a n/a >3.75 n/a n/a n/a B.t.i. + L. sphaericus (VectoMax FG, 4.5% + 2.7%) 0.875 (0.561–1.243) 1.853 (1.293–4.596) 3.94 ± 0.41 1.53 0.552 (0.397–0.828) 1.113 (0.762–2.896) 4.21 ± 0.42 3.14 Spinosad (Natular G30, 2.5%) 2.28 × 10−2 (2.00–2.60 × 10−2) 5.11 × 10−2 (4.30–6.41 × 10−2) 3.66 ± 0.33 0.25 1.04 × 10−2 (6.88 × 10−3–1.60 × 10−2) 2.19 × 10−2 (1.47–9.27 × 10−2) 3.96 ± 0.48 1.53 Spinetoram (Radiant, 11.7%) 1.47 × 10−2 (1.29–1.66 × 10−2) 3.35 × 10−2 (2.88–4.07 × 10−2) 3.59 ± 0.33 0.13 5.15 × 10−3 (3.51–7.49 × 10−3) 1.10 × 10−2 (7.49 × 10−3–3.08 × 10−2) 3.90 ± 0.43 1.31 Abamectin (Advance 375A, 0.011%) 1.20 × 10−2 (1.02–1.42 × 10−2) 4.06 × 10−2 (3.15–5.80 × 10−2) 2.42 ± 0.24 0.49 2.85 × 10−2 (1.89–5.32 × 10−2) 1.84 × 10−1 (6.50 × 10−2–8.87 × 10−1) 1.94 ± 0.26 1.67 Methoprene* (Altosid Liquid Larvicide, 5%) 5.04 × 10−3 (3.78–6.91 × 10−3) 4.05 × 10−2 (2.53–7.76 × 10−2) 1.42 ± 0.13 0.80 1.51 × 10−3 (9.49 × 10−4–2.13 × 10−3) 1.05 × 10−2 (7.15 × 10−3–1.84 × 10−2) 1.52 ± 0.20 0.61 Pyriproxyfen* (NyGuard IGR, 10%) 1.20 × 10−3 (9.01 × 10−4–1.70 × 10−3) 9.94 × 10−3 (5.83 × 10−3–2.15 × 10−2) 1.40 ± 0.14 0.37 3.10 × 10−5 (2.50–3.90 × 10−5) 1.22 × 10−4 (9.70 × 10−5–1.63 × 10−4) 2.17 ± 0.42 0.46 Diflubenzuron (Dimilin 25WP, 25%) 4.71 × 10−3 (3.96–5.62 × 10−3) 1.51 × 10−2 (1.20–2.06 × 10−2) 2.53 ± 0.22 0.13 1.63 × 10−3 (9.10 × 10−4–2.43 × 10−3) 2.42 × 10−2 (1.40–6.22 × 10−2) 1.10 ± 0.18 0.71 Novaluron (Mosquiron 0.12CRD, 0.12%) 1.34 × 10−3 (9.01 × 10−4–1.92 × 10−3) 3.59 × 10−3 (2.41–7.43 × 10−3) 2.98 ± 0.26 1.06 9.73 × 10−4 (8.50 × 10−4–1.12 × 10−3) 3.20 × 10−3 (2.54–4.37 × 10−3) 2.48 ± 0.26 0.89 Temephos (Skeeter Abate, 5%) 0.009 (0.007–0.010) 0.021 (0.018–0.027) 3.30 ± 0.35 0.44 0.009 (0.008–0.010) 0.016 (0.013–0.020) 5.59 ± 0.75 0.43 Imidacloprid (ImadPro 4SC, 40.7%) 0.106 (0.065–0.174) 0.320 (0.190–0.877) 2.66 ± 0.22 1.44 0.151 (0.125–0.181) 0.412 (0.330–0.550) 2.94 ± 0.28 0.18 Fipronil (Taurus SC, 9.1%) 7.18 × 10−3 (6.35–8.30 × 10−3) 1.93 × 10−2 (1.52–2.73 × 10−2) 2.98 ± 0.37 0.29 2.58 × 10−3 (2.14–3.37 × 10−3) 8.69 × 10−3 (5.95 × 10−3–1.56 × 10−2) 2.44 ± 0.34 0.55 Indoxacarb (Advion RIFA bait, 0.045%) 0.095 (0.063–0.144) 0.317 (0.198–0.728) 2.45 ± 0.21 2.18 0.100 (0.075–0.127) 0.327 (0.251–0.459) 2.48 ± 0.27 0.49 †Field collected from Montclair, CA. *Lethal results were read as inhibition of emergence (IE); ** Data heterogeneity. View Large Table 2. Susceptibility of larval Aedes aegypti L. originated from field collections in Montclair, CA to commonly used pesticides against larvae Pesticides Tested Aedes aegypti (F1-2)† Laboratory reference colony LC50 (ppm) (95% CI) LC90 (ppm) (95% CI) Slope χ2/df LC50 (ppm) (95% CI) LC90 (ppm) (95% CI) Slope χ2/df** B.t.i. (VectoBac WDG, 51.2%) 0.078 (0.048–0.128) 0.198 (0.122–0.857) 3.15 ± 0.30 2.05 0.088 (0.079–0.098) 0.152 (0.133–0.185) 5.43 ± 0.63 0.11 B.t.i. (WV SG3, 4.3%) 0.468 (0.405–0.534) 1.231 (1.031–1.564) 3.05 ± 0.31 0.66 0.373 (0.227–0.530) 0.929 (0.637–2.108) 3.24 ± 0.31 3.18 L. sphaericus (VectoLex WDG, 37.4%) >3.75 n/a n/a n/a >3.75 n/a n/a n/a B.t.i. + L. sphaericus (VectoMax FG, 4.5% + 2.7%) 0.875 (0.561–1.243) 1.853 (1.293–4.596) 3.94 ± 0.41 1.53 0.552 (0.397–0.828) 1.113 (0.762–2.896) 4.21 ± 0.42 3.14 Spinosad (Natular G30, 2.5%) 2.28 × 10−2 (2.00–2.60 × 10−2) 5.11 × 10−2 (4.30–6.41 × 10−2) 3.66 ± 0.33 0.25 1.04 × 10−2 (6.88 × 10−3–1.60 × 10−2) 2.19 × 10−2 (1.47–9.27 × 10−2) 3.96 ± 0.48 1.53 Spinetoram (Radiant, 11.7%) 1.47 × 10−2 (1.29–1.66 × 10−2) 3.35 × 10−2 (2.88–4.07 × 10−2) 3.59 ± 0.33 0.13 5.15 × 10−3 (3.51–7.49 × 10−3) 1.10 × 10−2 (7.49 × 10−3–3.08 × 10−2) 3.90 ± 0.43 1.31 Abamectin (Advance 375A, 0.011%) 1.20 × 10−2 (1.02–1.42 × 10−2) 4.06 × 10−2 (3.15–5.80 × 10−2) 2.42 ± 0.24 0.49 2.85 × 10−2 (1.89–5.32 × 10−2) 1.84 × 10−1 (6.50 × 10−2–8.87 × 10−1) 1.94 ± 0.26 1.67 Methoprene* (Altosid Liquid Larvicide, 5%) 5.04 × 10−3 (3.78–6.91 × 10−3) 4.05 × 10−2 (2.53–7.76 × 10−2) 1.42 ± 0.13 0.80 1.51 × 10−3 (9.49 × 10−4–2.13 × 10−3) 1.05 × 10−2 (7.15 × 10−3–1.84 × 10−2) 1.52 ± 0.20 0.61 Pyriproxyfen* (NyGuard IGR, 10%) 1.20 × 10−3 (9.01 × 10−4–1.70 × 10−3) 9.94 × 10−3 (5.83 × 10−3–2.15 × 10−2) 1.40 ± 0.14 0.37 3.10 × 10−5 (2.50–3.90 × 10−5) 1.22 × 10−4 (9.70 × 10−5–1.63 × 10−4) 2.17 ± 0.42 0.46 Diflubenzuron (Dimilin 25WP, 25%) 4.71 × 10−3 (3.96–5.62 × 10−3) 1.51 × 10−2 (1.20–2.06 × 10−2) 2.53 ± 0.22 0.13 1.63 × 10−3 (9.10 × 10−4–2.43 × 10−3) 2.42 × 10−2 (1.40–6.22 × 10−2) 1.10 ± 0.18 0.71 Novaluron (Mosquiron 0.12CRD, 0.12%) 1.34 × 10−3 (9.01 × 10−4–1.92 × 10−3) 3.59 × 10−3 (2.41–7.43 × 10−3) 2.98 ± 0.26 1.06 9.73 × 10−4 (8.50 × 10−4–1.12 × 10−3) 3.20 × 10−3 (2.54–4.37 × 10−3) 2.48 ± 0.26 0.89 Temephos (Skeeter Abate, 5%) 0.009 (0.007–0.010) 0.021 (0.018–0.027) 3.30 ± 0.35 0.44 0.009 (0.008–0.010) 0.016 (0.013–0.020) 5.59 ± 0.75 0.43 Imidacloprid (ImadPro 4SC, 40.7%) 0.106 (0.065–0.174) 0.320 (0.190–0.877) 2.66 ± 0.22 1.44 0.151 (0.125–0.181) 0.412 (0.330–0.550) 2.94 ± 0.28 0.18 Fipronil (Taurus SC, 9.1%) 7.18 × 10−3 (6.35–8.30 × 10−3) 1.93 × 10−2 (1.52–2.73 × 10−2) 2.98 ± 0.37 0.29 2.58 × 10−3 (2.14–3.37 × 10−3) 8.69 × 10−3 (5.95 × 10−3–1.56 × 10−2) 2.44 ± 0.34 0.55 Indoxacarb (Advion RIFA bait, 0.045%) 0.095 (0.063–0.144) 0.317 (0.198–0.728) 2.45 ± 0.21 2.18 0.100 (0.075–0.127) 0.327 (0.251–0.459) 2.48 ± 0.27 0.49 Pesticides Tested Aedes aegypti (F1-2)† Laboratory reference colony LC50 (ppm) (95% CI) LC90 (ppm) (95% CI) Slope χ2/df LC50 (ppm) (95% CI) LC90 (ppm) (95% CI) Slope χ2/df** B.t.i. (VectoBac WDG, 51.2%) 0.078 (0.048–0.128) 0.198 (0.122–0.857) 3.15 ± 0.30 2.05 0.088 (0.079–0.098) 0.152 (0.133–0.185) 5.43 ± 0.63 0.11 B.t.i. (WV SG3, 4.3%) 0.468 (0.405–0.534) 1.231 (1.031–1.564) 3.05 ± 0.31 0.66 0.373 (0.227–0.530) 0.929 (0.637–2.108) 3.24 ± 0.31 3.18 L. sphaericus (VectoLex WDG, 37.4%) >3.75 n/a n/a n/a >3.75 n/a n/a n/a B.t.i. + L. sphaericus (VectoMax FG, 4.5% + 2.7%) 0.875 (0.561–1.243) 1.853 (1.293–4.596) 3.94 ± 0.41 1.53 0.552 (0.397–0.828) 1.113 (0.762–2.896) 4.21 ± 0.42 3.14 Spinosad (Natular G30, 2.5%) 2.28 × 10−2 (2.00–2.60 × 10−2) 5.11 × 10−2 (4.30–6.41 × 10−2) 3.66 ± 0.33 0.25 1.04 × 10−2 (6.88 × 10−3–1.60 × 10−2) 2.19 × 10−2 (1.47–9.27 × 10−2) 3.96 ± 0.48 1.53 Spinetoram (Radiant, 11.7%) 1.47 × 10−2 (1.29–1.66 × 10−2) 3.35 × 10−2 (2.88–4.07 × 10−2) 3.59 ± 0.33 0.13 5.15 × 10−3 (3.51–7.49 × 10−3) 1.10 × 10−2 (7.49 × 10−3–3.08 × 10−2) 3.90 ± 0.43 1.31 Abamectin (Advance 375A, 0.011%) 1.20 × 10−2 (1.02–1.42 × 10−2) 4.06 × 10−2 (3.15–5.80 × 10−2) 2.42 ± 0.24 0.49 2.85 × 10−2 (1.89–5.32 × 10−2) 1.84 × 10−1 (6.50 × 10−2–8.87 × 10−1) 1.94 ± 0.26 1.67 Methoprene* (Altosid Liquid Larvicide, 5%) 5.04 × 10−3 (3.78–6.91 × 10−3) 4.05 × 10−2 (2.53–7.76 × 10−2) 1.42 ± 0.13 0.80 1.51 × 10−3 (9.49 × 10−4–2.13 × 10−3) 1.05 × 10−2 (7.15 × 10−3–1.84 × 10−2) 1.52 ± 0.20 0.61 Pyriproxyfen* (NyGuard IGR, 10%) 1.20 × 10−3 (9.01 × 10−4–1.70 × 10−3) 9.94 × 10−3 (5.83 × 10−3–2.15 × 10−2) 1.40 ± 0.14 0.37 3.10 × 10−5 (2.50–3.90 × 10−5) 1.22 × 10−4 (9.70 × 10−5–1.63 × 10−4) 2.17 ± 0.42 0.46 Diflubenzuron (Dimilin 25WP, 25%) 4.71 × 10−3 (3.96–5.62 × 10−3) 1.51 × 10−2 (1.20–2.06 × 10−2) 2.53 ± 0.22 0.13 1.63 × 10−3 (9.10 × 10−4–2.43 × 10−3) 2.42 × 10−2 (1.40–6.22 × 10−2) 1.10 ± 0.18 0.71 Novaluron (Mosquiron 0.12CRD, 0.12%) 1.34 × 10−3 (9.01 × 10−4–1.92 × 10−3) 3.59 × 10−3 (2.41–7.43 × 10−3) 2.98 ± 0.26 1.06 9.73 × 10−4 (8.50 × 10−4–1.12 × 10−3) 3.20 × 10−3 (2.54–4.37 × 10−3) 2.48 ± 0.26 0.89 Temephos (Skeeter Abate, 5%) 0.009 (0.007–0.010) 0.021 (0.018–0.027) 3.30 ± 0.35 0.44 0.009 (0.008–0.010) 0.016 (0.013–0.020) 5.59 ± 0.75 0.43 Imidacloprid (ImadPro 4SC, 40.7%) 0.106 (0.065–0.174) 0.320 (0.190–0.877) 2.66 ± 0.22 1.44 0.151 (0.125–0.181) 0.412 (0.330–0.550) 2.94 ± 0.28 0.18 Fipronil (Taurus SC, 9.1%) 7.18 × 10−3 (6.35–8.30 × 10−3) 1.93 × 10−2 (1.52–2.73 × 10−2) 2.98 ± 0.37 0.29 2.58 × 10−3 (2.14–3.37 × 10−3) 8.69 × 10−3 (5.95 × 10−3–1.56 × 10−2) 2.44 ± 0.34 0.55 Indoxacarb (Advion RIFA bait, 0.045%) 0.095 (0.063–0.144) 0.317 (0.198–0.728) 2.45 ± 0.21 2.18 0.100 (0.075–0.127) 0.327 (0.251–0.459) 2.48 ± 0.27 0.49 †Field collected from Montclair, CA. *Lethal results were read as inhibition of emergence (IE); ** Data heterogeneity. View Large Table 3. Resistance ratios in field-collected Aedes aegypti L. from Montclair, CA to commonly used pesticides against larvae Pesticides tested At LC50 At LC90 B.t.i. (VectoBac WDG, 51.2%) 0.89 1.30 B.t.i. (WV SG3, 4.3%) 1.25 1.33 L. sphaericus (VectoLex WDG, 37.4%) 1.00 n/a B.t.i. + L. sphaericus (VectoMax FG, 4.5% + 2.7%) 1.59 1.66 Spinosad (Natular G30, 2.5%) 2.19* 2.33 Spinetoram (Radiant, 11.7%) 2.85* 3.05 Abamectin (Advance 375A, 0.011%) 0.42 0.22 Methoprene (Altosid Liquid Larvicide, 5%) 3.34* 3.86* Pyriproxyfen (NyGuard IGR, 10%) 38.7* 81.5* Diflubenzuron (Dimilin 25WP, 25%) 2.89* 0.62 Novaluron (Mosquiron 0.12CRD, 0.12%) 1.38 1.12 Temephos (Skeeter Abate, 5%) 1.00 1.31 Imidacloprid (ImadPro 4SC, 40.7%) 0.70 0.78 Fipronil (Taurus SC, 9.1%) 2.78* 2.22 Indoxacarb (Advion RIFA bait, 0.045%) 0.95 0.97 Pesticides tested At LC50 At LC90 B.t.i. (VectoBac WDG, 51.2%) 0.89 1.30 B.t.i. (WV SG3, 4.3%) 1.25 1.33 L. sphaericus (VectoLex WDG, 37.4%) 1.00 n/a B.t.i. + L. sphaericus (VectoMax FG, 4.5% + 2.7%) 1.59 1.66 Spinosad (Natular G30, 2.5%) 2.19* 2.33 Spinetoram (Radiant, 11.7%) 2.85* 3.05 Abamectin (Advance 375A, 0.011%) 0.42 0.22 Methoprene (Altosid Liquid Larvicide, 5%) 3.34* 3.86* Pyriproxyfen (NyGuard IGR, 10%) 38.7* 81.5* Diflubenzuron (Dimilin 25WP, 25%) 2.89* 0.62 Novaluron (Mosquiron 0.12CRD, 0.12%) 1.38 1.12 Temephos (Skeeter Abate, 5%) 1.00 1.31 Imidacloprid (ImadPro 4SC, 40.7%) 0.70 0.78 Fipronil (Taurus SC, 9.1%) 2.78* 2.22 Indoxacarb (Advion RIFA bait, 0.045%) 0.95 0.97 *Significances in RRs were indicated by separate 95% CI at susceptibility levels. View Large Table 3. Resistance ratios in field-collected Aedes aegypti L. from Montclair, CA to commonly used pesticides against larvae Pesticides tested At LC50 At LC90 B.t.i. (VectoBac WDG, 51.2%) 0.89 1.30 B.t.i. (WV SG3, 4.3%) 1.25 1.33 L. sphaericus (VectoLex WDG, 37.4%) 1.00 n/a B.t.i. + L. sphaericus (VectoMax FG, 4.5% + 2.7%) 1.59 1.66 Spinosad (Natular G30, 2.5%) 2.19* 2.33 Spinetoram (Radiant, 11.7%) 2.85* 3.05 Abamectin (Advance 375A, 0.011%) 0.42 0.22 Methoprene (Altosid Liquid Larvicide, 5%) 3.34* 3.86* Pyriproxyfen (NyGuard IGR, 10%) 38.7* 81.5* Diflubenzuron (Dimilin 25WP, 25%) 2.89* 0.62 Novaluron (Mosquiron 0.12CRD, 0.12%) 1.38 1.12 Temephos (Skeeter Abate, 5%) 1.00 1.31 Imidacloprid (ImadPro 4SC, 40.7%) 0.70 0.78 Fipronil (Taurus SC, 9.1%) 2.78* 2.22 Indoxacarb (Advion RIFA bait, 0.045%) 0.95 0.97 Pesticides tested At LC50 At LC90 B.t.i. (VectoBac WDG, 51.2%) 0.89 1.30 B.t.i. (WV SG3, 4.3%) 1.25 1.33 L. sphaericus (VectoLex WDG, 37.4%) 1.00 n/a B.t.i. + L. sphaericus (VectoMax FG, 4.5% + 2.7%) 1.59 1.66 Spinosad (Natular G30, 2.5%) 2.19* 2.33 Spinetoram (Radiant, 11.7%) 2.85* 3.05 Abamectin (Advance 375A, 0.011%) 0.42 0.22 Methoprene (Altosid Liquid Larvicide, 5%) 3.34* 3.86* Pyriproxyfen (NyGuard IGR, 10%) 38.7* 81.5* Diflubenzuron (Dimilin 25WP, 25%) 2.89* 0.62 Novaluron (Mosquiron 0.12CRD, 0.12%) 1.38 1.12 Temephos (Skeeter Abate, 5%) 1.00 1.31 Imidacloprid (ImadPro 4SC, 40.7%) 0.70 0.78 Fipronil (Taurus SC, 9.1%) 2.78* 2.22 Indoxacarb (Advion RIFA bait, 0.045%) 0.95 0.97 *Significances in RRs were indicated by separate 95% CI at susceptibility levels. View Large Of the four IGRs tested, tolerance or low levels of resistance were observed in methoprene with RRs 3.34 to 3.86-fold. Similar tolerance (RR 2.89-fold) was also noticed to diflubenzuron at the LC50 level. However, modest levels of resistance were observed to pyriproxyfen with RRs 38.7- and 81.5-fold at IE50 and IE90 levels, respectively. Among the other pesticides against larval stages, the lower activity was encountered only in fipronil at the LC50 level with RR 2.78-fold (Tables 2 and 3). Susceptibility to Pesticides Against Adults There were no differences in susceptibility to the pyrethroid formulations tested, with or without synergist PBO, as well as the organophosphate malathion, between the field population and laboratory colony. The RRs to the four adulticide formulations ranged from 0.41- to 1.13-fold at LT50 and 0.48- to 1.80-fold at LT90 (Tables 4 and 5). Table 4. Susceptibility of adult Aedes aegypti L. originated from field collections in Montclair, CA to commonly used pesticides against adults Pesticides tested* Aedes aegypti (F1-2)† Laboratory reference colony LT50 (min) (95% CI) LT90 (min) (95% CI) Slope χ2/df* LT50 (min) (95% CI) LT90 (min) (95% CI) Slope χ2/df** Permethrin (Technical 99.0%) 10.3 (4.4–16.5) 32.6 (20.2–95.4) 2.57 ± 0.24 5.98 9.1 (7.1–11.0) 18.1 (14.4–27.3) 4.26 ± 0.33 4.53 Scourge 18 + 54 (18% resmethrin + 54% PBO) 8.0 (4.2–11.5) 16.7 (11.6–46.5) 4.02 ± 0.48 4.55 19.6 (18.1–21.3) 35.1 (31.7–39.8) 5.08 ± 0.38 0.34 Aquaduet (1% Prallethrin + 5% sumethrin + 5% PBO) 11.5 (8.0–15.0) 48.8 (36.1–76.2) 2.04 ± 0.19 1.43 13.2 (11.7–14.9) 42.9 (36.4–52.5) 2.51 ± 0.17 0.74 Malathion (Specttracide, 50%) 10.9 (10.0–11.7) 15.0 (13.7–17.7) 9.14 ± 1.58 0.01 21.2 (19.6–22.9) 29.3 (26.5–34.6) 9.10 ± 0.78 0.11 Pesticides tested* Aedes aegypti (F1-2)† Laboratory reference colony LT50 (min) (95% CI) LT90 (min) (95% CI) Slope χ2/df* LT50 (min) (95% CI) LT90 (min) (95% CI) Slope χ2/df** Permethrin (Technical 99.0%) 10.3 (4.4–16.5) 32.6 (20.2–95.4) 2.57 ± 0.24 5.98 9.1 (7.1–11.0) 18.1 (14.4–27.3) 4.26 ± 0.33 4.53 Scourge 18 + 54 (18% resmethrin + 54% PBO) 8.0 (4.2–11.5) 16.7 (11.6–46.5) 4.02 ± 0.48 4.55 19.6 (18.1–21.3) 35.1 (31.7–39.8) 5.08 ± 0.38 0.34 Aquaduet (1% Prallethrin + 5% sumethrin + 5% PBO) 11.5 (8.0–15.0) 48.8 (36.1–76.2) 2.04 ± 0.19 1.43 13.2 (11.7–14.9) 42.9 (36.4–52.5) 2.51 ± 0.17 0.74 Malathion (Specttracide, 50%) 10.9 (10.0–11.7) 15.0 (13.7–17.7) 9.14 ± 1.58 0.01 21.2 (19.6–22.9) 29.3 (26.5–34.6) 9.10 ± 0.78 0.11 †Field collected from Montclair, CA. *Coating doses: Permethrin (technical) – 30 μg/bottle, Scourge (resmethrin/PBO = 25/75 μg/bottle), AquaDuet (prallethrin/sumethrin/PBO = 0.5/2.5/2.5 μg/bottle), and Specttracide (malathion) – 150 μg/bottle. **Data heterogeneity. View Large Table 4. Susceptibility of adult Aedes aegypti L. originated from field collections in Montclair, CA to commonly used pesticides against adults Pesticides tested* Aedes aegypti (F1-2)† Laboratory reference colony LT50 (min) (95% CI) LT90 (min) (95% CI) Slope χ2/df* LT50 (min) (95% CI) LT90 (min) (95% CI) Slope χ2/df** Permethrin (Technical 99.0%) 10.3 (4.4–16.5) 32.6 (20.2–95.4) 2.57 ± 0.24 5.98 9.1 (7.1–11.0) 18.1 (14.4–27.3) 4.26 ± 0.33 4.53 Scourge 18 + 54 (18% resmethrin + 54% PBO) 8.0 (4.2–11.5) 16.7 (11.6–46.5) 4.02 ± 0.48 4.55 19.6 (18.1–21.3) 35.1 (31.7–39.8) 5.08 ± 0.38 0.34 Aquaduet (1% Prallethrin + 5% sumethrin + 5% PBO) 11.5 (8.0–15.0) 48.8 (36.1–76.2) 2.04 ± 0.19 1.43 13.2 (11.7–14.9) 42.9 (36.4–52.5) 2.51 ± 0.17 0.74 Malathion (Specttracide, 50%) 10.9 (10.0–11.7) 15.0 (13.7–17.7) 9.14 ± 1.58 0.01 21.2 (19.6–22.9) 29.3 (26.5–34.6) 9.10 ± 0.78 0.11 Pesticides tested* Aedes aegypti (F1-2)† Laboratory reference colony LT50 (min) (95% CI) LT90 (min) (95% CI) Slope χ2/df* LT50 (min) (95% CI) LT90 (min) (95% CI) Slope χ2/df** Permethrin (Technical 99.0%) 10.3 (4.4–16.5) 32.6 (20.2–95.4) 2.57 ± 0.24 5.98 9.1 (7.1–11.0) 18.1 (14.4–27.3) 4.26 ± 0.33 4.53 Scourge 18 + 54 (18% resmethrin + 54% PBO) 8.0 (4.2–11.5) 16.7 (11.6–46.5) 4.02 ± 0.48 4.55 19.6 (18.1–21.3) 35.1 (31.7–39.8) 5.08 ± 0.38 0.34 Aquaduet (1% Prallethrin + 5% sumethrin + 5% PBO) 11.5 (8.0–15.0) 48.8 (36.1–76.2) 2.04 ± 0.19 1.43 13.2 (11.7–14.9) 42.9 (36.4–52.5) 2.51 ± 0.17 0.74 Malathion (Specttracide, 50%) 10.9 (10.0–11.7) 15.0 (13.7–17.7) 9.14 ± 1.58 0.01 21.2 (19.6–22.9) 29.3 (26.5–34.6) 9.10 ± 0.78 0.11 †Field collected from Montclair, CA. *Coating doses: Permethrin (technical) – 30 μg/bottle, Scourge (resmethrin/PBO = 25/75 μg/bottle), AquaDuet (prallethrin/sumethrin/PBO = 0.5/2.5/2.5 μg/bottle), and Specttracide (malathion) – 150 μg/bottle. **Data heterogeneity. View Large Table 5. Resistance ratios in field-collected Aedes aegypti L. from Montclair, CA to commonly used pesticides against adults Pesticides tested At LT50 At LC90 Permethrin (Technical 99.0%) 1.13 1.80 Scourge 18 + 54 (18% resmethrin + 54% PBO) 0.41 0.48 AquaDuet (1% prallethrin + 5% sumethrin + 5% PBO) 0.87 1.14 Specttracide (malathion 50%) 0.51 0.51 Pesticides tested At LT50 At LC90 Permethrin (Technical 99.0%) 1.13 1.80 Scourge 18 + 54 (18% resmethrin + 54% PBO) 0.41 0.48 AquaDuet (1% prallethrin + 5% sumethrin + 5% PBO) 0.87 1.14 Specttracide (malathion 50%) 0.51 0.51 View Large Table 5. Resistance ratios in field-collected Aedes aegypti L. from Montclair, CA to commonly used pesticides against adults Pesticides tested At LT50 At LC90 Permethrin (Technical 99.0%) 1.13 1.80 Scourge 18 + 54 (18% resmethrin + 54% PBO) 0.41 0.48 AquaDuet (1% prallethrin + 5% sumethrin + 5% PBO) 0.87 1.14 Specttracide (malathion 50%) 0.51 0.51 Pesticides tested At LT50 At LC90 Permethrin (Technical 99.0%) 1.13 1.80 Scourge 18 + 54 (18% resmethrin + 54% PBO) 0.41 0.48 AquaDuet (1% prallethrin + 5% sumethrin + 5% PBO) 0.87 1.14 Specttracide (malathion 50%) 0.51 0.51 View Large Discussion Since its domestication, the type Ae. aegypti aegypti has been extremely successful in establishing itself around human surroundings. The other genomically indistinguishable, domestic variety Aedes aegypti queenslandensis has overlapping distribution with the type species, while the original wild subspecies remains in sub-Saharan Africa (Powell and Tabachnick 2013, Rašić et al. 2016). Thus far, emerging resistance to all four main classes of neurotoxic insecticides (carbamates, organochlorines, organophosphates, and pyrethroids) as adulticides has been detected in the Americas, Africa, and Asia among the type Ae. aegypti populations, where the target-site mutations and increased insecticide detoxification have both been linked to resistance (WHO 2014, Moyes et al. 2017). Most previous studies were conducted for adulticides. The current studies on Ae. aegypti mostly evaluated pesticide formulations against larval stages, including ones of microbial origins, IGRs and other reduced risk pesticides by US Environmental Protection Agency (U.S. EPA 2018). Although some formulations evaluated in the current study are not currently labeled as mosquito larvicides, mosquitoes can be exposed to them when those products are applied against other arthropod pests in the urban environments, which could compromise the susceptibility of the urban mosquito species to registered larvicides because of interactive resistance mechanism. Considering current patchy distributions and diverse genetic background of Ae aegypti in California (Pless et al. 2017), it is important to establish pesticide susceptibility profiles for individual populations of interest to ensure field efficacy of the products to be used. Among the pesticide formulations of microbial origins, this field-caught population was highly susceptible to Bti, a microbial mosquito larvicide belonging to the IRAC (Insecticide Resistance Action Committee) Group 11 (microbial disruptors of insect midgut membranes and derived toxins). Bti possesses intrinsic characteristics limiting resistance development (Wirth et al. 1997, 2000a,b), hence, resistance to Bti is uncommon regardless of the resistance status of mosquitoes to other pesticides (Su and Cheng 2014b; Su 2016b; Becker et al. 2018; Su et al. 2018a,b), even though resistance to individual crystal toxins can occur easily (Wirth 2010, Stalinski et al. 2014, Su 2016b). As expected, Ae. aegypti belonging to subgenus Stegomyia, was not susceptible to the microbial mosquito larvicide L. sphaericus (Wirth et al. 2000a,b), another IRAC Group 11 pesticide. Despite its high activity against Culex and some other species, primarily due to the nature of the target site for binary toxins (Wirth 2010, Su 2016a), L. sphaericus has a narrow target spectrum against mosquitoes. Lysinibacillus sphaericus is also prone to resistance development in Culex mosquitoes (Su 2016b, Su et al. 2018a,b). The combination of Bti and L. sphaericus is intended to take advantage of these two microbial agents, which is highly effective against Culex and other mosquito species. This combination showed high activity against both field and laboratory Ae. aegypti populations, due to the known synergism between Bti and L. sphaericus (Su and Mulla 2004, Wirth et al. 2004, Sreshty et al. 2011). Tolerance was observed in spinosad and spinetoram as indicated by elevated LC50 levels. Spinosad consisting of spinosyn A and D, and spinetoram consisting of spinosyn J and L are reduced risk pesticides (U.S. EPA 2018), belonging to IRAC Group 5 (nicotinic acetylcholine receptor allosteric modulator). These active ingredients are formulated in Conseve SC (11.6% spinosad), Radiant SC (11.7% spinetoram), and other pesticides to control urban and agricultural pests. This Ae. aegypti population might have been previously exposed to spinosyns in the urban environment in which it was found. Recently, products based on spinosad under trade name Natular have become available for mosquito control; however, they had not been used extensively yet when the Ae. aegypti specimens were collected in 2015. Nevertheless, it is highly recommended to monitor susceptibility to spinosyns in mosquito populations considering the risk of resistance development under sublethal conditions (Su and Cheng 2014a). As a reduced risk pesticide (U.S. EPA 2018), abamectin has been available to control a variety of urban and agricultural pests in bait (Advance 375A, 0.011%) or emulsifiable concentrate (Avid 0.15EC, 2.0%) formulations. This Aedes population was highly susceptible to abamectin, although its exposure history is unknown. The IGRs, including juvenile hormone (JH) mimics, such as the biopesticide methoprene (IRAC Group 7A – JH analog) and the reduced rick pesticide pyriproxyfen (IRAC Group 7C – JH mimic), and chitin synthesis inhibitors (CSIs), such as diflubenzuron and novaluron (IRAC Group 15), are commonly used biorational pesticides. Numerous formulations containing methoprene (Altosid, 0.5–20%), pyriproxyfen (Admiral 10EC, 10%, Admiral Advance, 10%, NyGuard IGR, 10%), or diflubenzuron (Adept, 25%, Advance Termite Bait, 0.25%) are available to control mosquitoes or other pests in urban environment, on pets, or in greenhouses. Novaluron is relatively new to the pest control world (Su et al. 2003). Available products containing novaluron are Pedestal (10%) to control insect pests on ornamentals in greenhouses, shade-houses and nurseries, and Mosquiron (0.12%) to control mosquitoes (Su et al. 2014). With respect to resistance development in mosquitoes to these IGRs, several cases have been reported previously to methoprene in Aedes nigromaculis (Cornel et al. 2000), Aedes taeniorhynchus (Dame et al. 1998), Culex quinquefasciatus (Su and Cheng 2014b), and to diflubenzuron in Culex pipiens (Grigoraki et al. 2017). However, the overall risk of mosquito resistance to methoprene and diflubenzuron is considered to be low (Bellinato et al. 2016, Su 2016b, Lau et al. 2018). It is generally believed that the risk of resistance development against pyriproxyfen is even lower than other IGRs after a failure to induce resistance in an organophosphate-resistant Cx. quinquefasciatus colony for 17 generations (Schaefer et al. 1991). Additionally, mosquitoes that have developed resistance to other pesticides such as L. sphaericus, spinosad, permethrin, or methoprene, remained susceptible to pyriproxyfen (Su and Cheng 2014b, Su et al. 2015, 2018a,b). However, a noticeable level of resistance to pyriproxyfen was observed in this field population of Ae. aegypti in Montclair, CA. The small ratio of RR90/RR50, or closer RR50 and RR90 indicated this population was homogenous, i.e., most individuals in this population were resistant to pyriproxyfen. The most commonly used products with pyriproxyfen are Admiral 10EC, Admiral Advance, and NyGuard IGR to control whiteflies and a wide variety of flying and crawling arthropods of urban, household and public health importance, including mosquitoes. It remains unknown how this population developed this significant level of resistance under field conditions. Upon the increasing potential application of pyriproxyfen in mosquito control particularly against invasive Aedes species by autodissemination through oviposition activity (Buckner et al. 2017, Suman et al. 2018) or dusting males (Mains et al. 2015), resistance risk assessment to this promising compound is well warranted. It is important to emphasize that this pyriproxyfen-resistant field Ae. aegypti population remained susceptible to methoprene with negligible levels of tolerance. Methoprene, as a biopesticide, has the same mode of action and belongs to the same general IRAC Group (Group 7A) as pyriproxyfen (Group 7C). Among the commonly used biorational pesticides of microbial or IGR origins against mosquitoes, pyriproxyfen is the most active with the lowest LC levels, the longevity of which warrants to be preserved by resistance management tactics in today’s challenging world of mosquito control. Although this is the first report of resistance to pyriproxyfen in a wild mosquito population, the earliest report in other insects (whiteflies) dates back to 1995 (Ishaaya and Horowitz 1995) where a high level of resistance was recorded in a greenhouse whitefly population after three successive applications of pyriproxyfen. Numerous studies and reports ensued with regard to the evolution (Crowder et al. 2006), inheritance (Horowitz et al. 2003), metabolic mechanisms (Ma et al. 2010, Karatolos et al. 2012), and relevant operational and environmental factors (Crowder et al. 2008) of resistance development in different species of whiteflies, such as Bemisia tabaci (Gennadius) and Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) (Li et al. 2003, Crowder et al. 2007). Other similar reports on arthropods of public health importance were only on the housefly Musca domestica L. (Diptera: Muscidae), where resistance risk, genetic mechanism and cross-resistance spectrum were investigated under laboratory conditions (Zhang and Shono 1997; Zhang et al. 1997, 1998). Among the remaining pesticide formulations tested against larval stages, this Ae. aegypti population was highly susceptible to one of the conventional pesticides, temephos (organophosphate), and two reduced risk pesticides, imidacloprid (neonicotinoid) and indoxacarb (oxadiazine). Tolerance to fipronil (phenylpyrazole) was observed at the LC50 level. Products based on fipronil such as Taurus SC (9.1%), Taurus TRIO G (0.0143%), MaxForce FC (0.01%), etc. are commonly used in household and surroundings against a wide variety of pests of urban and public importance. Mosquito populations have ample opportunity to be exposed to these pesticides, particularly the species closely associated with human dwellings and urban setups, such as Ae. aegypti and Aedes albopictus (Skuse). It is quite common for urban insect populations, particularly houseflies and mosquitoes, to develop various levels of resistance against pyrethroids and other conventional pesticides (Zhu et al. 2016). However, this Aedes population remained susceptible to technical permethrin and the combinations of pyrethroids and PBO. The same also held true for one of the commonly used organophosphates, malathion. Because resistance profiles can be highly population-specific, susceptibility assays are recommended to be conducted in each population of interest. In summary, Ae. aegypti has been an extremely successful invader of urban landscapes and a significant nuisance and vector of arboviruses in the tropics and subtropics worldwide. The biological traits of this species and its close association with human dwellings and activities have contributed to its geographical expansion and spread of the pathogens it transmits. While adulticiding by space sprays is needed to mitigate disease outbreaks, larviciding using biorational pesticides (microbial origins and IGRs) can serve as a sustainable integrated vector management approach in controlling mosquitoes in urban environments. Resistance evolution due to the mode of action, as well as repeated exposure during urban applications against other pests, and improper use of products, have combined to compromise the expected efficacy of insecticide-based mosquito control operations. It is essential to evaluate the potential for resistance development in mosquitoes according to the mode of action, monitor the susceptibility, and implement proper mitigation measures when reduced susceptibility or tolerance in the target population to the pesticides of interest is realized. Acknowledgments The authors are grateful to Dr. Alec Gerry with Department of Entomology, University of California at Riverside (Riverside, CA, USA) for the provision of Radiant SC, and to Dr. Barry Tyler, Pestalto Environmental Health Services Inc. (Hamilton, Ontario, Canada) for supplying Mosquiron 0.12CRD. 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TI - Susceptibility Profile of Aedes aegypti L. (Diptera: Culicidae) from Montclair, California, to Commonly Used Pesticides, With Note on Resistance to Pyriproxyfen
JO - Journal of Medical Entomology
DO - 10.1093/jme/tjz019
DA - 2019-06-27
UR - https://www.deepdyve.com/lp/oxford-university-press/susceptibility-profile-of-aedes-aegypti-l-diptera-culicidae-from-PS4riPYMDi
SP - 1047
VL - 56
IS - 4
DP - DeepDyve
ER -