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

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Abstract

The fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), 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 protein 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.

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Acknowledgments

This project was supported by the Biotechnology Risk Assessment Program Competitive Grant No. 2010-33522-21772 from the USDA National Institute of Food and Agriculture. We thank H. Collins and M. Cheung for technical assistance and Mike Strand for supplying the initial colony of C. marginiventris.

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Authors and Affiliations

  1. Department of Entomology, Cornell University, New York State Agricultural Experiment Station (NYSAES), Geneva, NY, USA

    Jun-Ce Tian, Xiang-Ping Wang, Li-Ping Long & Anthony M. Shelton

  2. State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, China

    Jun-Ce Tian

  3. College of Agriculture, Yangtze University, Jingzhou, Hubei, China

    Xiang-Ping Wang

  4. Rice Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, Guangxi, China

    Li-Ping Long

  5. Agroscope Reckenholz-Tänikon Research Station ART, Zurich, Switzerland

    Jörg Romeis

  6. USDA-ARS, Arid Land Agricultural Research Center, Maricopa, AZ, USA

    Steven E. Naranjo

  7. USDA-ARS, Corn Insects and Crop Genetics Research Unit, Department of Entomology, Iowa State University, Ames, IA, USA

    Richard L. Hellmich

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  1. Jun-Ce Tian
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  2. Xiang-Ping Wang
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  3. Li-Ping Long
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  4. Jörg Romeis
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  5. Steven E. Naranjo
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  6. Richard L. Hellmich
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  7. Anthony M. Shelton
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Correspondence to Anthony M. Shelton.

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Xiang-Ping Wang is a co-first author, equal contribution as first author.

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Tian, JC., Wang, XP., Long, LP. et al. Eliminating host-mediated effects demonstrates Bt maize producing Cry1F has no adverse effects on the parasitoid Cotesia marginiventris . Transgenic Res 23, 257–264 (2014). https://doi.org/10.1007/s11248-013-9748-x

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  • DOI: https://doi.org/10.1007/s11248-013-9748-x

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