Tritrophic interactions between Bt maize, Spodoptera frugiperda (Lepidoptera: Noctuidae) and Podisus nigrispinus (Hemiptera: Pentatomidae)

Abstract

Insect resistant transgenic plants are important tools for pest control, and risk assessment studies are required to assess their effects on non-target organisms, such as the natural enemies. Tritrophic interactions studies that integrate toxicological and behavioral aspects can provide reliable information of the possible effects of transgenic plants on higher trophic level organisms. In this context, the objective of thisthesis was to study the tritrophic interactions between Bt and non-Bt maize plants, the fall armywormSpodoptera frugiperda (Lepidoptera: Noctuidae) and the predator Podisus nigrispinus (Hemiptera: Pentatomidae). A Bt-resistant population of S. frugiperda to Btmaize was used to evaluate direct effects of the Cry1F toxin on the biology of the predator, excluding indirect effects of low-quality susceptible pests on the biology ofthe predator. It was also evaluated possible effects of the genetic modification of the Bt plants on the volatile emissions and on foraging behavior of the predator P. nigrispinus, for this, constitutive and induced volatile emissions of Bt maize plants were compared with non-Bt plants. Induced plants were treated with larval regurgitant or damaged by Bt-resistant larvae of S. frugiperda that were able to feed on Bt and non-Bt plants equally, avoiding possible changes in the herbivore-induced volatile profiles due to larval feeding behavior. The laboratory and semi-field greenhouse assays showed that the Bt-resistant S. frugiperda were able to damage and survive on Bt maize, without deleterious effects on its biology. The bioassays with the predator P. nigrispinus showed no direct impact on its biology, as evidenced by the high survival rate, normal nymphal development time and average adult weight after exposure to Bt-resistant prey fed on Bt maize. GC-MS analyses revealed that Bt transformation did not result in relevant changes in the constitutive volatile emission nor in that emitted by regurgitant-treated plants. Despite the fact that Bt-resistant S. frugiperda population inflicted similar damage on Bt and non-Bt plants, herbivore-induced volatile blend emitted by Bt plants had a different composition. Herbivore-damaged non-Bt plants emitted fatty acid derivatives and monoterpenes that were absent in the emission of herbivore-damaged Bt plants. Results from olfactometer tests showed that P. nigrispinus did not distinguish among the odours of undamaged and regurgitant-treated plants regardless of the plant genotypes. While the predator oriented preferentially to volatiles from herbivore-damaged over undamaged plants of the non-Bt genotype, the predator did not differentiate blends emitted by undamaged and herbivore-damaged plants of Bt maize. When the predator was exposed to herbivore-induced plant volatiles of Bt and non-Bt plants, P. nigrispinus preferred the latter, suggesting that the qualitative differences found between herbivore-damaged Bt and non-Bt maize plants might be responsible for the differential attractiveness. Given the fact that we used a Bt-resistant herbivore, this is the first report demonstrating that the insertion of Bt into maize genome changes qualitatively plant volatile emissions, in ways that disrupt predator orientation to herbivore-induced plant volatiles. Therefore, Cry1F maizehad no direct effects on the biology of the predatorP. nigrispinus, however may affect its prey-searching behavior.