Using field-evolved resistance to Cry1F maize in a lepidopteran pest to demonstrate no adverse effects of Cry1F on one of its major predators

Authors: TIAN, JUN-CE TIAN - Cornell University; COLLINS, HILDA - Cornell University; ROMEIS, JORG - Agroscope; Naranjo, Steven; Hellmich Ii, Richard; SHELTON, ANTHONY - Cornell University

Submitted to: Transgenic Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/19/2012
Publication Date: 2/29/2012
Citation: Tian, J., Collins, H.L., Romeis, J., Naranjo, S.E., Hellmich II, R.L., Shelton, A.M. 2012. Using field-evolved resistance to Cry1F maize in a lepidopteran pest to demonstrate no adverse effects of Cry1F on one of its major predators. Transgenic Research. 21(6):1303-1310.

Interpretive Summary: Transgenic crops producing the target-specific insecticidal proteins of Bacillus thuringiensis (Bt) have been widely adopted and cultivated on millions of hectares globally. However, there remain concerns about the ecological risk associated with these crops, specifically the risk to non-target organisms. Insects that provide biological control services are typically exposed to the Bt proteins through the prey they consume that have fed on the Bt crop (tri-trophic interaction). A common problem in evaluating tri-trophic exposure is that the prey is often harmed by the Bt protein and thus it is impossible to separate the effects of prey quality from Bt toxicity on the natural enemy. Here we take advantage of a prey insect (Spodoptera frugiperda) that has developed resistance to the Cry1F Bt protein and is unharmed when feeding on this type of Bt maize. We allowed the prey to feed on both Bt and non-Bt maize and then provided these prey to a common predator, ladybird beetle, Coleomegilla maculata. Duration of larval and pupal stages, adult weight and female fecundity of C. maculata were not different when they were fed resistant S. frugiperda larvae reared on either Bt or non-Bt maize leaves during over two generations. Immunoassays and insect-sensitive bioassays confirmed that C. maculata were exposed to bioactive Cry1F protein. The Cry1F protein had no effect on C. maculata larvae, even though larvae contained 20-32 ng /g by fresh weight of the protein. Overall, our results demonstrated that Cry1F protein did not affect important fitness parameters of one of S. frugiperda’s major predators and that the Bt protein did not accumulate but was strongly diluted when transferred during trophic interactions. This study clearly documents no adverse impact of Cry1F Bt maize on a common and important insect predator.

Technical Abstract: Spodoptera frugiperda (JE Smith) represents the first documented case of field evolved resistance to a genetically engineered crop expressing an insecticidal protein from Bacillus thuringiensis (Bt). In this case it was Cry1F-expressing maize (Mycogen 2A517). The ladybird beetle, Coleomegilla maculata (DeGeer), is a common and abundant predator that suppresses pest populations in maize and many other cropping systems. Its larvae and adults are polyphagous, feeding on aphids, thrips, lepidopteran eggs and larvae, as well as plant tissues. Thus, C. maculata may be exposed to Bt proteins expressed in genetically engineered crops by several pathways. Using Cry1F-resistant S. frugiperda larvae as prey, we evaluated the potential impact of Cry1F-expressing maize on several fitness parameters of C. maculata over two generations. Using Cry1F resistant prey removed any potential prey-mediated effects. Duration of larval and pupal stages, adult weight and female fecundity of C. maculata were not different when they were fed resistant S. frugiperda larvae reared on either Bt or control maize leaves during both generations. ELISA and insect-sensitive bioassays showed C. maculata were exposed to bioactive Cry1F protein. The insecticidal protein had no effect on C. maculata larvae, even though larvae contained 20-32 ng of Cry1F/g by fresh weight. Over all, our results demonstrated that the Cry1F protein did not affect important fitness parameters of one of S. frugiperda’s major predators and that Cry1F protein did not accumulate but was strongly diluted when transferred during trophic interactions.