Toxic and behavioral effects to Carabidae of seed treatments used on Cry3Bb1- and Cry1Ab/c-protected corn

Most transgenic corn seed is now treated with systemic neonicotinoid insecticides. To address potential direct nontarget effects of these combined technologies, 16 Carabidae species from 10 genera (Agonum, Amara, Anisodactylus, Bembidion, Chlaenius, Harpalus, Patrobus, Poecilus, Pterostichus, and Scarites) field-collected from corn were directly exposed to Bacillus thuringiensis (Bt) Cry toxin-laden pollens and seed treatments in feeding and defined-dose bioassays. All adults readily fed on field or sweet corn pollens that expressed coleopteran-specific Cry3Bb1 or lepidopteran-targeting Cry1Ab/c, and no significant toxicity was observed. Adult survivorship ranged from 47 d for the predator Pterostichus melanarius (Illiger) to a year for the more omnivorous Scarites quadriceps Chaudoir, feeding solely on pollen containing 30-90 microgram Cry3Bb1/g and water. In contrast, commercial doses of neonicotinoid seed treatments (imidacloprid, thiamethoxam, or clothianidin) elicited nearly complete mortality for 18 carabid species in 4-d bioassays containing corn seedlings. Carabid consumption of fungicide-only (fludioxonil plus mefenoxam) seed treatments was generally observed within 1 d, compared with a 2-d latency on neonicotinoid treatments, suggesting an antifeedant effect of the insecticide. In microcosm bioassays containing a corn seedling and five prey, clothianidin seed treatments killed adult western corn rootworm, Diabrotica virgifera virgifera LeConte and S. quadriceps, although the smaller Harpalus pensylvanicus (DeGeer) was more tolerant. We conclude that the neonicotinoid/fungicide seed treatments, and not Cry3Bb1 or CryIAb/c, are a major direct mortality factor for ground beetles. Field studies are needed to determine population and community level effects on Carabidae when these transgenic and seed-treatment technologies are combined.