Differential Toxicity of Pyrethroid and Organophosphate Insecticides to the Honey Bee, Apis Mellifera and the Yellow Fever Mosquito, Aedes Aegypti
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DIFFERENTIAL TOXICITY OF PYRETHROID AND ORGANOPHOSPHATE INSECTICIDES TO THE HONEY BEE, APIS MELLIFERA AND THE YELLOW FEVER MOSQUITO, AEDES AEGYPTI HUSSEIN SANCHEZ-ARROYO1, ROBERTO M. PEREIRA2, RUI-DE XUE3, BETTINA A. MOSER2, AND PHILIP G. KOEHLER2 1Colegio de Postgraduados, México 2University of Florida/Department of Entomology & Nematology, Gainesville, FL 3Anastasia Mosquito Control District, 120 EOC Drive, St. Augustine, FL Subject Editor: Keira Lucas ABSTRACT Six insecticide active ingredients (AIs) and five commercial insecticide formulations were applied by topical application and onto filter paper strips to determine differential toxicity toAedes aegypti (L.) and Apis mellifera (L.), and to evaluate their potential use in future insecticide resistance monitoring surveys. For topical application, 0.1 or 1 µl of the technical insecticide solution was applied to the Ae. aegypti and A. mellifera thorax, respectively. For insecticide-impregnated strips the insecticide amount varied, according with the commercial formulation. By topi- cal application deltamethrin was the most toxic AI (LD50 = 0.057 µg/g) to Ae. aegypti and prallethrin was least toxic (LD50 = 19.42 µg/g). For A. mellifera, the most toxic AIs were deltamethrin (LD50 = 0.013 µg/g) and bifenthrin (LD50 = 0.156 µg/g); and the least toxic was chlorpyrifos (LD50 = 3.246 µg/g). When the insecticide-impregnated papers method was used, Mosquitomist Two (chlorpyrifos 24.6%) was the most toxic insecticide for Ae. aegypti (LC50= 0.024 2 2 µg/cm ), and Aqualuer (permethrin 20.6%, PBO 20.6%) was least toxic (LC50= 0.408 µg/cm ). For A. mellifera the 2 most toxic commercial insecticide formulations were Talstar (bifenthrin 7.9%; LC50= 0.288 µg/cm ) and Mosqui- 2 tomist Two (LC50= 0.299 µg/cm ), with no significant differences, and the least toxic commercial formulation was 2 Deltagard (deltamethrin 2.0%; LC50= 15.084 µg/cm ). By topical application, more than 28 times of chlorpyrifos was needed to obtain the same mortality in A. mellifera as in Ae. aegypti. When using the insecticide-impregnated paper method, more than 206 times of Deltagard was needed to obtain the same mortality in A. mellifera as in Ae. aegypti. Even though Mosquitomist Two was the most toxic insecticide for both insect species, the honey bees were >12 times more tolerant to this insecticide, compared with the mosquitoes. Key words: Aedes aegypti, Apis mellifera, insecticides, toxicity, topical application, insecticide-impregnated papers, mosquito control INTRODUCTION Zika have been reported from several states in the United States, including Florida. The Aedes aegypti (L.), the yellow fever mos- Chikungunya and Yellow fever viruses are quito, is an important vector of numerous not currently present in the United States, human arboviral diseases including den- but the risk of (re)introduction is possible gue, Zika, chikungunya and yellow fevers due to infected travelers and the presence of (CDC 2020a, 2020 b, 2020c, 2020d). Den- Ae. aegypti (FDOH 2020a, 2020b). gue, Chikungunya, and Yellow fever viruses About two-thirds of the crops traded on may cause long-lasting severe symptoms the world market depend on pollinator ser- and death. The illness caused by Zika virus vices (Klein et al. 2007). Honey bees, Apis is usually mild but may cause serious brain mellifera (L.), are the most valuable pollina- defects including microcephaly in unborn tors for agricultural crops and the elevated babies. Local transmissions of dengue and loss rates of managed honey bee colonies 70 Sanchez-Arroyo et al.: Insecticide toxicity 71 threaten the pollination services they pro- ture, Center for Medical, Agricultural, and vide (Bruckner et al. 2018, Klein et at. 2007, Veterinary Entomology (USDA CMAVE) in López-Uribe and Simone-Finstrom 2019). Gainesville, FL, USA. Pupae and emerging For that reason, there is global concern adults were maintained in adult colony cag- about the decline of honey bee populations es in an environmental chamber at 26+2°C which is attributed to a range of factors such (79+3°F), 50-80% RH and a photoperiod as “Colony Collapse Disorder” (Williams et of 12:12 (Light:Dark). Apis mellifera were al. 2010), pathogens, and pesticides (Osti- obtained from an apiary managed accord- guy et al. 2019). Since worker honey bees ing to common practices for North Central can forage up to 12 km around their hive Florida by the Honey Bee Research and Ex- and reach urban areas (Beekman and Rat- tension Laboratory, Entomology and Nem- nieks 2000), they can be exposed to insecti- atology Department, University of Florida, cides used in public health to manage mos- Gainesville, FL, USA. Female adult Ae. ae- quitoes. Ae. aegypti is closely associated with gypti were collected 3-4 days after they had urban and suburban domestic habits (Jan- emerged from the pupal stage and used sen and Beebe 2010), and insecticides are for the insecticide assays. Female adult regularly applied to control them (Farook worker A. mellifera were at least 3 days old et al. 2018). Some studies concluded that and collected from three separate hives by barrier or ground insecticide applications shaking off adults crawling on hive frames. to control host-seeking mosquitoes may Throughout the experiments, adult Ae. also affect nontarget insects such as honey aegypti and A. mellifera were provided with bees (Qualls et al. 2010, Drake et al. 2016). 10% and 50% sucrose solution ad libitum, Adding to the challenges faced by mosquito respectively. control districts, Ae. aegypti is becoming in- Active ingredient experiments. The fol- creasingly resistant to pyrethroids (Smith et lowing six commonly used mosquito adul- al. 2016, Estep et al. 2018 Casey et al. 2020), ticidal technical AIs (Sigma-Aldrich, USA) which are the active ingredients (AIs) of were used in the experiments: Phenothrin choice in many adulticides available for (94.6 %), prallethrin (96 %), deltamethrin mosquito control. As such, novel ways are (99.7%), chlorpyrifos (99.3%), permethrin needed to control mosquitoes with minimal (96.7%) and bifenthrin (99.1%). For range- impacts on non-target organisms. finding experiments, 10-fold serial dilutions The first objective of the studies present- in acetone from 1.0x104 - 1.0x10-1 ng/µL ed here was to determine the differential were applied topically onto the thorax of toxicity of one organophosphate and five py- adult female Ae. aegypti and A. mellifera. In- rethroid AIs and one organophosphate and termediate dilutions were included for the four pyrethroid commercial insecticide for- determination of the LD50. mulations for Ae. aegypti and A. mellifera. The For Ae. aegypti, topical toxicity bioassays second objective was to evaluate two bioassay were performed based on the method of methods for potential use in insecticide re- Pridgeon et al. (2008). For each of 5 repli- sistance monitoring surveys. This informa- cate assays per treatment, 10 adult female tion is needed to help evaluate the impact Ae. aegypti were knocked down using CO2 for of insecticide applications on both Ae. aegypti 15 s, and then treated with 0.1 µl of insecti- and A. mellifera. cide preparation using a 5 µl syringe (Ham- ilton Co. Reno NV) with a repeat dispenser MATERIALS AND METHODS (Hamilton PB 600-1). Each group of treated mosquitoes were transferred to a 20-ml scin- Insects rearing and maintenance. Py- tillation vial, which was covered with mesh to rethroid-susceptible Ae. aegypti (ORL1952 prevent escape. Control insects were treated strain) pupae in 473 ml (16 oz) deli cups with acetone only. Mortality was assessed 24 were obtained from colonies maintained at h after exposure to insecticides. The repli- the United States Department of Agricul- cates were performed on different days with 72 Journal of the Florida Mosquito Control Association, Vol. 68, 2021 4-5 doses over the critical portion of the dose of Deltagard or Talstar preparations, or 70 curve for Probit analysis. µl of Duet preparation. Ae. aegypti strips were For A. mellifera, topical toxicity bioassays treated with 32 µl of Mosquitomist Two or were performed based on the method of the Aqualuer, 50 µl of Deltagard or Talstar, or 25 Organization for Economic Co-operation µl of Duet preparations (Sanchez-Arroyo et and Development (OECD 1998). For each al., 2019). The negative control strips were of 6-7 replicate assays per treatment, 10 adult treated with the diluents of the correspond- female workers from three separate hives ing insecticides. were knocked down with CO2 for 20 s and Aedes aegypti were knocked down using then treated with 1.0 µl of insecticide prepa- CO2 for 15 s and transferred to 20-ml scin- ration using a 50 µl syringe (Hamilton Co. tillation vials, which were then covered with Reno NV) with a repeat dispenser (Hamil- mesh secured by rubber bands. Ten females ton PB 600-1). Each group of treated insects were used in each concentration replicate were transferred to a 120-ml Mason jar which and housed in the same vial. After 30 min- was then closed with a lid that was modified utes and complete insect recovery from with glued-in mesh. Negative controls were CO2, an insecticide-treated filter paper strip treated with acetone only. Mortality was as- was introduced to the middle of the scin- sessed 24 h after exposure to insecticides. tillation vial, with both sides available for The replicates were performed on different mosquitoes to rest. The strips remained in days with 4-5 doses over the critical portion the vial for the duration of the experiment. of the dose curve for Probit analysis. Five replicates were carried out on separat- Commercial insecticide experiments. The ed days. following five commercial insecticides were Apis mellifera were knocked down using tested using an insecticide-impregnated pa- CO2 for 20 s and transferred to 120-ml glass per method: Mosquitomist TwoTM (chlorpy- jars which were then secured with a mesh.