Location: Crop Protection and Management ResearchTitle: Pest tradeoffs in technology: Reduced damage by caterpillars in Bt cotton benefits aphids.) Author
Submitted to: Proceedings of the Royal Society B
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/12/2013
Publication Date: 2/18/2013
Publication URL: http://www.dx.doi.org/10.1098/rspb.2013.0042
Citation: Hagenbucher, S., Wackers, F.L., Wettstein, F.E., Olson, D.M., Ruberson, J.R., Romeis, J. 2013. Pest tradeoffs in technology: Reduced damage by caterpillars in Bt cotton benefits aphids. Proceedings of the Royal Society B. 280:1471-2954. Interpretive Summary: The rapid adoption of genetically engineered (GE) plants that express insecticidal Cry proteins derived from Bacillus thuringiensis (Bt) has raised concerns about their potential impact on non-target organisms. Particular concern lies with the possibility that herbivores insensitive to the Bt toxin might develop (secondary) pest status in Bt crops, and a number of studies have now reported increased levels of secondary pests in Bt crops. While this threatens to compromise the sustainable use of the transgenic varieties, the underlying mechanisms remain poorly understood. Secondary pest problems have largely been attributed to the reduced use of broad spectrum chemical insecticides against the target pests but also to changes in plant growth or morphology as well to other unintended transformation-related effects. Here, we propose that herbivore-inducible secondary metabolites may represent an important additional mechanism. We show that, because of effective suppression of Bt-sensitive lepidopteran herbivores, Bt cotton contains reduced levels of induced terpenoid aldehydes. We also show that changes in the overall level of these defensive secondary metabolites are associated with improved performance of a Bt-insensitive herbivore, the aphid Aphis gossypii, under glasshouse and field conditions. This study identifies a novel, indirect interaction between insecticidal Bt toxins and inherent plant resistance that explains secondary pest outbreaks in Bt crops. Identification of this mechanism increases our understanding of how insect-resistant crops impact herbivore communities and helps underpin the sustainable use of transgenic varieties and effective management of resistance development in the target pest populations.
Technical Abstract: A number of studies have now reported increased levels of non Bt-targeted secondary pests in Bt crops. We carried out a series of greenhouse and field experiments comparing aphid populations on Bt-and non Bt-cotton that were damaged by the Bt-targeted caterpillar, Heliothis virescens. We found in both greenhouse and field studies that Bt-cotton had no caterpillar damage after 7 days whereas non-Bt cotton was heavily damaged by the caterpillar. The constitutive terpenoids levels did not differ between Bt and non Bt-cotton, but induced levels of terpenoids were higher in the non Bt-cotton. Bt and non-Bt cotton plants did not differ in their capacity for terpenoid production as confirmed in an experiment in which plant terpenoids were induced by application of jasmonic acid. Aphid populations were similar on Bt and non Bt-cotton that had no caterpillar damage. However, aphid populations were significantly reduced on the non-Bt cotton compared to the Bt-cotton. Our results show that effective suppression of target herbivores by Bt cotton translates into a decrease in the level of induced terpenoids, leaving plants more susceptible to herbivores not targeted by the Bt toxins.