title: Eliminating host-mediated effects demonstrates Bt maize producing Cry1F has no adverse effects on the parasitoid Cotesia marginiventris.
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.
authors.affiliation: Department of Entomology, Cornell University, New York State Agricultural Experiment Station (NYSAES), Geneva, NY, USA.
authors.forename: Jun-Ce
authors.initials: JC
authors.lastname: Tian
authors.forename: Xiang-Ping
authors.initials: XP
authors.lastname: Wang
authors.forename: Li-Ping
authors.initials: LP
authors.lastname: Long
authors.forename: Jörg
authors.initials: J
authors.lastname: Romeis
authors.forename: Steven E
authors.initials: SE
authors.lastname: Naranjo
authors.forename: Richard L
authors.initials: RL
authors.lastname: Hellmich
authors.forename: Anthony M
authors.initials: AM
authors.lastname: Shelton
mesh_terms: D000818:Animals; D000083722:Bacillus thuringiensis Toxins; D001426:Bacterial Proteins / Q000235:genetics / Q000633:toxicity*; D001681:Biological Assay; D004731:Endotoxins / Q000235:genetics / Q000633:toxicity*; D005298:Fertility / Q000187:drug effects; D006460:Hemolysin Proteins / Q000235:genetics / Q000633:toxicity*; D007305:Insecticide Resistance / Q000235:genetics; D008136:Longevity / Q000187:drug effects; D012744:Sex Ratio; D018411:Spodoptera / Q000187:drug effects / Q000469:parasitology*; D014863:Wasps / Q000187:drug effects* / Q000502:physiology; D003313:Zea mays / Q000235:genetics* / Q000382:microbiology
chemical_list: D000083722:Bacillus thuringiensis Toxins; D001426:Bacterial Proteins; D004731:Endotoxins; D006460:Hemolysin Proteins; C030956:insecticidal crystal protein, Bacillus Thuringiensis
references.citation: Environ Entomol. 2009 Dec;38(6):1533-8
references.pmid: 20021746
references.citation: J Insect Physiol. 2004 May;50(5):435-43
references.pmid: 15121457
references.citation: Nat Biotechnol. 2006 Jan;24(1):63-71
references.pmid: 16404399
references.citation: Nat Biotechnol. 2013 May;31(5):386-7
references.pmid: 23657387
references.citation: Transgenic Res. 2005 Apr;14(2):133-44
references.pmid: 16022385
references.citation: Science. 2007 Jun 8;316(5830):1475-7
references.pmid: 17556584
references.citation: Transgenic Res. 2009 Jun;18(3):317-22
references.pmid: 19357987
references.citation: PLoS One. 2013;8(3):e60125
references.pmid: 23544126
references.citation: J Econ Entomol. 2010 Aug;103(4):1031-8
references.pmid: 20857709
references.citation: J Econ Entomol. 2013 Jun;106(3):1103-11
references.pmid: 23865173
references.citation: Transgenic Res. 2012 Dec;21(6):1303-10
references.pmid: 22373893
references.citation: PLoS One. 2008 May 07;3(5):e2118
references.pmid: 18461164
references.citation: Annu Rev Entomol. 2002;47:845-81
references.pmid: 11729093
references.citation: Proc Natl Acad Sci U S A. 2011 Aug 23;108(34):14037-42
references.pmid: 21844358
references.citation: PLoS One. 2011 Mar 01;6(3):e17606
references.pmid: 21390253
references.citation: PLoS One. 2008 May 28;3(5):e2284
references.pmid: 18523682
references.citation: Environ Entomol. 2009 Apr;38(2):293-306
references.pmid: 19389277
references.citation: Annu Rev Entomol. 2002;47:501-33
references.pmid: 11729083
references.citation: J Econ Entomol. 2009 Dec;102(6):2011-25
references.pmid: 20069826
references.citation: Transgenic Res. 2011 Feb;20(1):1-22
references.pmid: 20938806
references.citation: Nat Biotechnol. 2008 Feb;26(2):203-8
references.pmid: 18259178
references.citation: J Econ Entomol. 2004 Oct;97(5):1603-11
references.pmid: 15568349