Abstract
Recently, we reported a novel mode of action in monarch butterfly (Danaus plexippus) larvae exposed to neonicotinoid insecticides: arrest in pupal ecdysis following successful larval ecdysis. In this paper, we explore arrested pupal ecdysis in greater detail and propose adverse outcome pathways to explain how neonicotinoids cause this effect. Using imidacloprid as a model compound, we determined that final-instar monarchs, corn earworms (Helicoverpa zea), and wax moths (Galleria mellonella) showed high susceptibility to arrested pupal ecdysis while painted ladies (Vanessa cardui) and red admirals (Vanessa atalanta) showed low susceptibility. Fall armyworms (Spodoptera frugiperda) and European corn borers (Ostrinia nubilalis) were recalcitrant. All larvae with arrested ecdysis developed pupal cuticle, but with incomplete shedding of larval cuticle and unexpanded pupal appendages; corn earworm larvae successfully developed into adults with unexpanded appendages. Delayed initiation of pupal ecdysis was also observed with treated larvae. Imidacloprid exposure was required at least 26 h prior to pupal ecdysis to disrupt the molt. These observations suggest neonicotinoids may disrupt the function of crustacean cardioactive peptide (CCAP) neurons, either by directly acting on their nicotinic acetylcholine receptors or by acting on receptors of inhibitory neurons that regulate CCAP activity.
Highlights
We reported a novel mode of action in monarch butterfly (Danaus plexippus) larvae exposed to neonicotinoid insecticides: arrest in pupal ecdysis following successful larval ecdysis
arrested pupal ecdysis (AE) is characterized by a failure to complete the pupal ecdysis process; the pre-ecdysis and initial ecdysis behaviors initiated by ecdysis triggering hormone (ETH) and eclosion hormone (EH)[13] are not a ffected[14]
We describe a unique adverse effect caused by neonicotinoid insecticides in butterflies and moths
Summary
We reported a novel mode of action in monarch butterfly (Danaus plexippus) larvae exposed to neonicotinoid insecticides: arrest in pupal ecdysis following successful larval ecdysis. We report a novel effect of neonicotinoids on the development of butterflies and moths and propose associated AOPs. We characterize a unique adverse outcome, termed arrested pupal ecdysis (AE), which was first reported following neonicotinoid exposure to final instars of the monarch butterfly (Danaus plexippus; Nymphalidae). Larvae died during pupation following topical and dietary exposure to imidacloprid, clothianidin, and thiamethoxam without prior signs of intoxication[14,15] This disruption in the pupal molt occurred at environmentally relevant doses 10 to 100-fold lower than doses that caused larval mortality due to neuronal overstimulation and p aralysis[14,15]. Larval-to-larval molts were not disrupted at doses that caused AE These observations suggest that sublethal neonicotinoid doses (i.e., doses not causing CNS overstimulation) are disrupting neuroendocrine signaling during pupal ecdysis through a novel toxicity pathway.
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