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Title: Eliminating host-mediated effects demonstrates Bt maize producing Cry1F has no adverse effects on the parasitoid Cotesia marginiventris

Author
item Naranjo, Steven
item TIAN, J.C. - Cornell University
item WANG, X.P. - Cornell University
item LONG, L.P. - Cornell University
item ROMEIS, J. - Agroscope
item HELLMICH, R.L. - US Department Of Agriculture (USDA)
item SHELTON, A.M. - Cornell University

Submitted to: Transgenic Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/31/2013
Publication Date: 6/16/2014
Publication URL: http://handle.nal.usda.gov/10113/58931
Citation: Naranjo, S.E., Tian, J., Wang, X., Long, L., Romeis, J., Hellmich, R., Shelton, A. 2014. Eliminating host-mediated effects demonstrates Bt maize producing Cry1F has no adverse effects on the parasitoid Cotesia marginiventris. Transgenic Research. 23:257-264.

Interpretive Summary: Several transgenic crops producing the insecticidal proteins of Bacillus thuringiensis (Bt) have been widely adopted and were cultivated on nearly 70 million hectares globally in 2012. Despite their target selectivity there remain concerns about the ecological risk associated with these crops, specifically the risk to non-target organisms. Non-target organisms that supply valuable ecosystem like biological pest control are of particular interest. Insects that provide biological control services can be exposed to the Bt proteins through the prey they consume that have in turn fed on the Bt crop (tri-trophic interaction). A common problem in evaluating tri-trophic exposure is that susceptible prey are often sublethally harmed by the Bt protein. This makes it impossible to separate the effects of prey quality from Bt toxicity on the natural enemy. In this study we utilize a prey species (fall armyworm) that has evolved resistance to Bt maize in the field. We used the Cry1F-resistant fall armyworms to evaluate effects of Cry1F on Cotesia marginiventris, an important parasitoids of numerous caterpillar pests, over five generations. Our results clearly demonstrate that Cry1F maize does not affect development, parasitism, survivorship, sex ratio, longevity or fecundity of C. marginiventris when they parasitize Cry1F maize-fed fall armyworms. Furthermore, the level of Cry1F protein in the leaves was strongly diluted when transferred from Bt maize to the host caterpillar and was not detected in larvae, cocoons or adults of the parasitoid. Our results refute previous reports of C. marginiventris being harmed by Bt proteins and suggest that such results were caused by prey-mediated effects due to using Bt-susceptible caterpillar hosts. These results should be useful to governmental regulators, scientists interested in ecological risk assessment and others concerned about the risks of Bt transgenic crops.

Technical Abstract: The fall armyworm, Spodoptera frugiperda, is an important pest of maize in the United States and many tropical areas in the western hemisphere. In 2001, Herculex I ® (Cry1F) maize was commercially planted in the United States to control Lepidoptera, including S. frugiperda. In 2006, a population of S. frugiperda was discovered in Puerto Rico that had evolved resistance to Cry1F maize in the field, making it the first well-documented case of an insect with field resistance to a plant producing proteins from Bacillus thuringiensis (Bt). Using this resistant population, we conducted tri-trophic studies with a natural enemy of S. frugiperda. By using resistant S. frugiperda, we were able to overcome possible prey-mediated effects and avoid concerns about potential differences in laboratory- or field-derived Bt resistance. We used the Cry1F-resistant S. frugiperda to evaluate effects of Cry1F on Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae), a larval endoparasitoid of S. frugiperda, over five generations. Our results clearly demonstrate that Cry1F maize does not affect development, parasitism, survivorship, sex ratio, longevity or fecundity of C. marginiventris when they parasitize Cry1F maize-fed S. frugiperda. Furthermore, the level of Cry1F protein in the leaves was strongly diluted when transferred from Bt maize to S. frugiperda and was not detected in larvae, cocoons or adults of C. marginiventris. Our results refute previous reports of C. marginiventris being harmed by Bt proteins and suggest that such results were caused by prey-mediated effects due to using Bt-susceptible lepidopteran hosts.