Sublethal, Behavioral, and Developmental Effects of the Neonicotinoid Pesticide Imidacloprid on Larval Wood Frogs (Rana sylvatica)

Abstract

Imidacloprid, a neonicotinoid pesticide, is used to prevent the spread of the hemlock woolly adelgid, currently affecting Eastern Hemlock trees across North America. When the pesticide is sprayed directly onto soil around infested trees (soil drenching), it can run off into aquatic systems, with potential negative effects on biota. Simultaneously, climate change may lead to faster pool drying, which acts as an additional stressor for sensitive species such as amphibians. We evaluated the sublethal effects of imidacloprid (10 ppb), and interaction with shorter hydroperiods on the larval behavior, growth, and survival of a model organism, the wood frog (Rana sylvatica). We performed 3 behavioral experiments evaluating swimming speed, time spent swimming, and distance the larvae swam. We found that larvae raised in 10 ppb imidacloprid or shorter hydroperiod did not differ in their swimming time, distance, and speed from nonexposed larvae. Naïve larvae exposed for 20 min to 10-to 500-ppb concentrations also showed similar performance to nonexposed larvae. However, when we applied a stimulus halfway through each experiment, we found that larvae exposed to 10 ppb imidacloprid (short and long term) swam shorter distances and spent less time swimming, suggesting that imidacloprid exposure may slow reaction time, potentially increasing the risk of predation. To minimize impacts on pool-breeding amphibians, imidacloprid application to combat the invasive hemlock woolly adelgid should use trunk injection and avoid soil drenching.

Effects of a Neonicotinoid Insecticide and Population Density on Behavior and Development of Wood Frogs (Rana sylvatica)

“…They suggested that neonicotinoids may impair the natural functioning of the hypothalamic-pituitary-adrenal (HPA) stress axis, which could impair amphibians' ability to respond to stressors in their environment. Lee-Jenkins and Robinson (2018) and Sweeney et al (2021) found, for instance, that chronic exposure of wood frog tadpoles to 10 µg/L imidacloprid may compromise juvenile frogs' ability to perceive and/or respond to predator threats.…”

“…They suggested that neonicotinoids may impair the natural functioning of the hypothalamic–pituitary–adrenal (HPA) stress axis, which could impair amphibians' ability to respond to stressors in their environment. Lee‐Jenkins and Robinson (2018) and Sweeney et al (2021) found, for instance, that chronic exposure of wood frog tadpoles to 10 µg/L imidacloprid may compromise juvenile frogs' ability to perceive and/or respond to predator threats. Similarly, Sievers et al (2018) found that spotted marsh frog tadpoles exposed to imidacloprid and iron–imidacloprid mixtures failed to perceive and avoid predator cues after acute (24 h) exposures to concentrations of 0.25 and 0.5 µg/L.…”

Toxicity and genotoxicity of imidacloprid in the tadpoles of Leptodactylus luctator and Physalaemus cuvieri (Anura: Leptodactylidae)

“…This was expected from the concentrations used in the present study (3–300 µg L −1 ), which were mostly below the LC 50 thresholds (82–366 mg L −1 ) reported for other amphibian species (reviewed by Gibbons et al 44 ). The imidacloprid concentrations used in this study may nevertheless be representative of the levels of contamination found typically in surface water in agricultural areas 45 , and appear not to cause mortality but showed different chronic effects in other aquatic vertebrate species, such as R. sylvatica , exposed to 10–500 µg L −1 (cited as ppm) of the insecticide 43 , and the fish Pimephales promelas (10 µg L−1) 46 .…”

“…While an insecticide based on imidacloprid and lambda-cyhalothrin caused 100% morality of Amietophrynus regularis at doses from 0.05 mg L −1 39 Low levels (e.g., environmental levels 40 – 42 ) have seldom been studied in amphibians. A recent study found that the application of a halfway stimulus in Rana sylvatica exposed to low doses of imidacloprid (10 µg L −1 ) demonstrated that the larvae swam shorter distances and spent less time swimming 43 , suggesting that imidacloprid exposure may delay the reaction, potentially increasing the risk of predation 43 .…”

Carryover effects of pesticide exposure and pond drying on performance, behavior, and sex ratios in a pool breeding amphibian

“…Therefore, forest amphibians breeding in temporary pools may be affected during both aquatic and terrestrial stages. Low imidacloprid concentrations have sublethal effects on non‐target organisms in aquatic systems (Goulson, 2013; Sweeney et al., 2021), while effects on terrestrial organisms have not been widely documented (van Meter et al., 2015).…”