Using resistant prey demonstrates that Bt plants producing Cry1Ac, Cry2Ab and Cry1F have no negative effects on Geocoris punctipes and Orius insidiosus

Authors: TIAN, J - Cornell University; LONG, L - Cornell University; WANG, X - Cornell University; Naranjo, Steven; ROMEIS, J - Agroscope; Hellmich Ii, Richard; WANG, P - Cornell University; SHELTON, A - Cornell University

Submitted to: Environmental Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/20/2013
Publication Date: 2/1/2014
Publication URL: http://handle.nal.usda.gov/10113/58419
Citation: Tian, J.C., Long, L.P., Wang, X.P., Naranjo, S.E., Romeis, J., Hellmich, R.L., Wang, P., Shelton, A.M. 2014. Using resistant prey demonstrates that Bt plants producing Cry1Ac, Cry2Ab and Cry1F have no negative effects on Geocoris punctipes and Orius insidiosus. Environmental Entomology. 43:242-251.

Interpretive Summary: Transgenic cotton and maize 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. Of particular interest are non-target organisms that supply valuable ecosystem services such as natural enemies of pest insects. 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 itself 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 cultures of two prey insects (cabbage looper and fall armyworm) that have been selected to be resistant to multiple Bt Cry proteins in two crop plants. Larvae of these species were fed Bt cotton or maize or non-Bt plants and then exposed to nymphs and adults of Geocoris punctipes (big-eyed bugs) and Orius insidiosus (insidious flower bug), two important and cosmopolitan predators that are abundant in cotton, maize and many other crops. Fitness parameters (larval survival, development time, adult fecundity, mass and survival) of these two predators were assessed over two generations. There were no differences in any of the fitness parameters regardless if the predator consumed prey that had in turn consumed Bt or non-Bt plants. Assays confirmed that the prey consumed by the predator contained Cry proteins and that these proteins were transferred to the predators. These studies confirm that Cry1Ac, Cry2Ab and Cry1F do not pose a hazard to big-eyed bugs or insidious flower bugs at field realistic concentrations. This study also demonstrates the power of using resistant hosts when assessing the risk of genetically modified plants on non-target organisms. 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: Geocoris punctipes (Say) and Orius insidiosus (Say) are generalist predators found in a wide range of crops, including cotton (Gossypium hirsutum L.) and maize (Zea mays L.), where they provide important biological control services by feeding on an array of pests including eggs and small larvae of lepidopteran caterpillars. A high percentage of cotton and maize in the USA and several other countries are transgenic cultivars that produce one or more of the insecticidal Cry proteins of Bacillus thuringiensis Berliner (Bt). Here we quantify effects of three Cry proteins on the life history of these predators over two generations when they are exposed to these Cry proteins indirectly through their prey. To eliminate the confounding prey quality effects that can be introduced by Bt susceptible prey, we used Cry1Ac/Cry2Ab-resistant Trichoplusia ni (Hübner) and Cry1F-resistant Spodoptera frugiperda (J.E. Smith) in a series of tri-trophic studies. Survival, development, adult mass, fecundity and fertility were similar when predators consumed larvae feeding on Cry1Ac/Cry2Ab cotton or Cry1F maize compared with prey feeding on isogenic or near-isogenic cotton or maize. Repeated exposure of the same initial cohort over a second generation also resulted in no differences in life history traits when feeding on non-Bt or Bt fed prey. ELISA showed that predators were directly exposed to Bt Cry proteins from their prey and that these proteins became increasingly diluted as they moved up the food chain. Results show a clear lack of effect of three common and widespread Cry proteins on these two important predator species. The use of resistant insects to eliminate prey quality effects provides for a more robust and meaningful assessment of exposure and hazard.