Assessing the risk of insecticide exposures on monarch butterflies
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Abstract
The North American monarch butterfly (Danaus plexippus), an iconic butterfly species, has significantly declined over the last two decades. In December 2020, it was designated as a candidate species under the Endangered Species Act. Conservation of North America’s eastern monarch butterfly population requires establishment of 1.3 to 1.6 billion milkweed (Asclepias spp.) stems in the agricultural landscapes of North Central United States (U.S.). As insecticides are commonly used in this landscape, it is important to assess the risk of insecticide exposure on monarch butterflies. Both foliar and seed treatment insecticide use in North Central U.S. could result in topical and/or dietary exposure to different monarch life stages. Topical and dietary acute and chronic toxicity of six insecticides, encompassing four different modes of action, were studied. Chlorantraniliprole (anthranilic diamide) and beta-cyfluthrin (pyrethroid) were the most toxic while thiamethoxam (neonicotinoid) and chlorpyrifos (organophosphate) were the least toxic. Generally, the larvae and eggs were more sensitive than the adults and pupae. Comparison of toxicity data with modelled and measured environmental insecticide concentrations indicated that foliar applications pose significant risks to monarchs downwind of treated maize or soybean fields. Conversely, seed treatment applications pose little or no risk. The field-scale risk estimates were incorporated into a landscape-scale population model to determine the conservation risks and benefits of establishing milkweed in agricultural landscapes. Toxicity data also were generated for double-stranded RNA (dsRNA) molecules, an emerging class of insecticide products. Monarch larvae were recalcitrant to the dsRNA molecules tested. A review of the literature, including development of species sensitivity distribution models, indicated that while monarch and other lepidopteran larvae were similarly susceptible to the chemical modes of action tested, monarchs were comparatively less susceptible to RNA interference. Finally, a novel mode of action for neonicotinoid insecticides was evaluated. Five of the seven final-instar lepidopteran larvae treated with neonicotinoids failed to expand their pupal appendages and complete pupal ecdysis. Detailed analyses of arrested ecdysis symptomology suggest that neonicotinoids interfere with the function of crustacean cardioactive peptide neurons; adverse outcome pathways for this effect were proposed. Future avenues of research in the field of insect toxicology and risk assessment include the development and use of in vitro and in silico techniques.