Embryonic Exposure to Thiamethoxam Reduces Survival and Alters Neurobehavior of Fathead Minnows

Abstract

Thiamethoxam is a commonly used neonicotinoid insecticide that acts as a nicotinic acetylcholine receptor (nAChR) agonist. Although vertebrates are less sensitive to neonicotinoid insecticides than invertebrates, some neonicotinoids have been shown to cause neurobehavioral changes in larval fishes. In the present study, we examine the neurobehavioral toxicity of acute and chronic exposure to environmentally relevant concentrations of thiamethoxam in fathead minnows at two different life stages. Whereas acute exposure of embryos to thiamethoxam does not appear to stimulate spontaneous contractions within 1 min, chronic exposure of embryos to 1.57 µg or more thiamethoxam/L caused increased mortality as well as a subtle increase in spontaneous contraction frequency (SCF), which was negatively correlated with early hatching success. Chronic exposure of embryos to 155 µg thiamethoxam/L impaired predator escape response, and chronic exposure to 0.02–14.61 µg thiamethoxam/L impaired foraging efficiency of some fish. Fathead minnows exposed to thiamethoxam beginning post hatch did not experience changes to measured health or neurobehavioral indicators. Taken together, our findings indicate that embryonic life stages are more sensitive to thiamethoxam exposure than later larval life stages. Because early exposure to thiamethoxam can cause deficits in predatory escape behaviors and may impair foraging success, further study of the potential direct and nondirect impacts of thiamethoxam on wild fish populations is warranted. Environ Toxicol Chem 2022;41:1276–1285. © 2022 SETAC

Chronic Exposure to Environmentally Relevant Concentrations of Imidacloprid Impact Survival and Ecologically Relevant Behaviors of Fathead Minnow Larvae

“…Interestingly, reduced embryonic motor activity (SCF) was correlated with premature hatching, which contradicts the idea that increased SCF may be necessary for hatching (Woynárovich & Horváth, 1980). Exposure to similar concentrations of another neonicotinoid, thiamethoxam, did not alter SCF in fathead minnow (Victoria, Hein, et al, 2022) or zebrafish embryos (Victoria, Duffy, et al, 2022), but lower embryonic motor activity was also correlated with an increased proportion of fathead minnow embryos that hatched (Victoria, Hein, et al, 2022). It is possible that fathead minnows are hatching early in an attempt to escape exposure to IM.…”

“…Behavioral indicators for nAChR activation were used in conjunction with modeling. We hypothesized that acute exposure to IM leading to overactivation of the nAChR would increase SCF and, if the affinity were strong enough, would lead to paralysis (as seen with nicotine; Victoria, Duffy, et al, 2022). As described previously in the Impacts on predator escape response section, embryos were placed in 1 ml of standard culture water under a dissecting microscope attached to a Nikon 80i camera set at 43 fps (maximum possible speed) with the NIS Elements software (Nikon Instruments).…”

“…Another behavioral response that could be altered by an nAChR agonist is the predator escape response (C-start response). After 8 days of IM exposure, predator escape activity was assessed as described by Victoria, Duffy, et al (2022) using vibrational stimulus to initiate the response. A Nikon SMZ800 dissecting microscope with an attached Photron camera set at 1000 frames/s (fps) was used to capture the response.…”

Binary mixtures of imidacloprid and thiamethoxam do not appear to cause additive toxicity in fathead minnow larvae (Pimephales promelas)

“…In Wisconsin (U.S.A), the presence of these neonicotinoid insecticides in various surface and drinking water sources has raised concerns, with IM detected in surface waters in the range 0.05–0.08 µg IM/L and TM detected in surface waters at 0.057–2.78 μg TM/L ( DATCP, 2018 ). Their high specificity for the invertebrate nicotinic acetylcholine receptor (nAChR) was thought to limit their effects on vertebrates ( Yamamoto et al, 1998 ); however, several studies demonstrate their toxicity in fish ( Beggel et al, 2012 ; Gibbons et al, 2015 ; Thompson, 2020 ; Victoria et al, 2022a ; Victoria et al, 2022b ). Taken together, this suggests that fish, and aquatic ecosystems in general, may be at risk from exposure to mixtures of these insecticides ( Anderson et al, 2015b ; Sánchez-Bayo et al, 2016 ).…”

“…Our previous work showed that individually, IM and TM cause subtle toxicity in fathead minnow larvae ( Victoria et al, 2022a ; Jeninga et al, 2023 ). Here, we used fathead minnow ( Pimephales promelas ) to test the hypothesis that embryo larval exposure to binary mixtures of IM and TM that include environmentally relevant concentrations would be more toxic than exposure to either pesticide alone.…”