4.7 Article

Neonicotinoids can cause arrested pupal ecdysis in Lepidoptera

Journal

SCIENTIFIC REPORTS
Volume 11, Issue 1, Pages -

Publisher

NATURE PORTFOLIO
DOI: 10.1038/s41598-021-95284-0

Keywords

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Funding

  1. Henry and Sylvia Richardson Research Incentive Grant from the entomology department at Iowa State University (ISU)
  2. Agriculture and Food Research Initiative Pollinator Health Program from the U.S. Department of Agriculture (USDA) National Institute of Food and Agriculture [2018-67013-27541]
  3. State of Iowa funds

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This study reveals that exposure to neonicotinoid insecticides can disrupt the process of pupal ecdysis in monarch butterfly larvae, possibly by affecting the function of crustacean cardioactive peptide (CCAP) neurons.
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.

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