Neonicotinoid and sulfoximine pesticides differentially impair insect escape behavior and motion detection

Abstract

Insect nervous systems offer unique advantages for studying interactions between sensory systems and behavior, given their complexity with high tractability. By examining the neural coding of salient environmental stimuli and resulting behavioral output in the context of environmental stressors, we gain an understanding of the effects of these stressors on brain and behavior and provide insight into normal function. The implication of neonicotinoid (neonic) pesticides in contributing to declines of nontarget species, such as bees, has motivated the development of new compounds that can potentially mitigate putative resistance in target species and declines of nontarget species. We used a neuroethologic approach, including behavioral assays and multineuronal recording techniques, to investigate effects of imidacloprid (IMD) and the novel insecticide sulfoxaflor (SFX) on visual motion-detection circuits and related escape behavior in the tractable locust system. Despite similar LD50 values, IMD and SFX evoked different behavioral and physiological effects. IMD significantly attenuated collision avoidance behaviors and impaired responses of neural populations, including decreases in spontaneous firing and neural habituation. In contrast, SFX displayed no effect at a comparable sublethal dose. These results show that neonics affect population responses and habituation of a visual motion detection system. We propose that differences in the sublethal effects of SFX reflect a different mode of action than that of IMD. More broadly, we suggest that neuroethologic assays for comparative neurotoxicology are valuable tools for fully addressing current issues regarding the proximal effects of environmental toxicity in nontarget species.

Sublethal exposure to deltamethrin impairs maternal egg care in the European earwig Forficula auricularia

“…Whereas exposure to sublethal doses of pesticides is well known to shape a broad diversity of insect behaviors (Haynes, 1988;Mazzi and Dorn, 2012;Müller, 2018;Parkinson et al, 2020), their effects on maternal egg care remained surprisingly unknown. In this study, we addressed this gap in knowledge by testing whether exposures to different concentrations of deltamethrin (a commonly used pesticide in agriculture and public health fields (Davies et al, 2012;Li et al, 2019;Liao et al, 2018) altered the expression of maternal egg care in the European earwig.…”

“…The absence of effects of maternal exposure to deltamethrin on the egg fate may also suggest that the observed sublethal effects on maternal care are transient and return to a normal level a few days after maternal exposure (a behavior that was not recorded in the present experiment) and/or that impaired maternal care occurring after the eggs have reached half of their development time is not detrimental in absence of natural constraints such as pathogens and predators. In insects, the duration of sublethal effects of pesticides on insect behaviors are difficult to predict, as they strongly depend on the type and dose of pesticide, mode of pesticide exposure, species, and measured behavior (Haynes, 1988;Mazzi and Dorn, 2012;Müller, 2018;Parkinson et al, 2020). Our findings therefore pave the way for follow-up studies disentangling among the formulated hypotheses and investigating the long-lasting effects of deltamethrin on the physiology and behaviors of earwig mothers, as well as the short-and long-term effects of deltamethrin exposure on the impact of impaired egg care under natural conditions.…”

“…Whereas a growing number of studies shed light on the broad diversity of sublethal effects associated with pesticide exposure on insect behaviors (Haynes, 1988;Mazzi and Dorn, 2012;Müller, 2018;Parkinson et al, 2020), their impacts -and the impact of deltamethrin -on maternal care remain unexplored in insects. This is surprising, as maternal care is a common phenomenon in insects and forms the backbone of key insect societies such as in many bees (Klug and Bonsall, 2014;Kramer and Meunier, 2019;Machado and Trumbo, 2018;Wong et al, 2013).…”

Do novel insecticides pose a threat to beneficial insects?

“…B 287: 20201265 impact of chronic sulfoxaflor exposure (5 ppb) on bumblebee foraging performance, although foraging observations were not made during the exposure period [32], so the results are not directly comparable to research with neonicotinoids [19,23]. More recent experiments similarly found no effect of acute sulfoxaflor exposure on locust (Locusta migratoria) behaviour [79], suggesting that the lack of behavioural impairment may hold across insects more broadly.…”

Acute Application of Imidacloprid Alters the Sensitivity of Direction Selective Motion Detecting Neurons in an Insect Pollinator

“…Direct evidence for potential effects on visual processing includes acute exposure to sublethal doses of IMI, which caused increased cell death in the optic lobes of honey bees (de Almeida Rossi et al, 2013). More recently, visually-evoked responses recorded in visual premotor neurons from the locust ventral nerve cord showed impaired burst activity and activity propagation in animals previously injected or orally treated with a sub-lethal dose of IMI or two main secondary metabolites (Parkinson et al, 2017(Parkinson et al, , 2020Parkinson and Gray, 2019). Very recently Martelli and colleagues provided evidence of decreased synaptic transmission as well as phototransduction in photoreceptors of Drosophila chronically treated with imidacloprid (Martelli et al, 2020).…”