Reduced caterpillar damage can benefit plant bugs in Bt cotton

Authors: EISENRING, MICHAEL - Agroscope; Naranjo, Steven; BACHER, S - Agroscope; Abbott, Angelique; MEISSLE, M - Agroscope; ROMEIS, J - Agroscope

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/10/2019
Publication Date: 2/27/2019
Citation: Eisenring, M., Naranjo, S.E., Bacher, S., Abbott, A.L., Meissle, M., Romeis, J. 2019. Reduced caterpillar damage can benefit plant bugs in Bt cotton. Scientific Reports. 9:2727.

Interpretive Summary: In some production systems using Bt crops there has been increasing issues with pest insects which are not affected by the Bt insecticidal proteins. In Bt cotton, pests such as plant bugs have increased in importance in some parts of the world. Several factors may influence these patterns, among them the benefits that plant bugs might derive from reduced caterpillar damage on Bt cotton. This reduced damage was found to reduce the production of some of the cotton plant’s inherent defensive compounds (gossypol and other terpenoids), therefore enhancing the plants susceptibility to other herbivores. We found that nymphs of the plant bug Lygus hesperus were negatively affected if they feed on plants sprayed with the defense-triggering phytohormone jasmonic acid (JA) or damaged by Bt tolerant Spodoptera exiga caterpillars. Nymph performance was furthermore affected by food source (cotton squares/ bolls) and the interaction of food source with plant type (Bt/non-Bt cotton). We further found that JA-sprayed plants showed increased levels of terpenoids in feeding structures whereas L. hesperus damage led to no increase of terpenoids. However, feeding assays on artificial diets spiked with gossypol revealed that L. hesperus was not negatively affected indicating that other inherent cotton defense compounds might be responsible for the patterns observed on plants. Overall, this study demonstrates that the absence of plant-mediated competition between herbivores may be an important additional factor contributing to differential populations of sucking bugs in Bt crops.

Technical Abstract: Bt cotton was genetically modified to produce insecticidal proteins targeting Lepidopteran pests and is therefore only minimally affected by caterpillar damage. This could lead to reduced levels of inherent, systemically inducible defensive compounds in Bt cotton which might benefit other important cotton herbivores such as plant bugs. We studied the effects of plant defense induction on the performance of the plant bug Lygus hesperus by caging nymphs on different food sources bolls/squares) of Bt and non-Bt cotton which were either undamaged, damaged by Bt tolerant caterpillars, or treated with jasmonic acid (JA). Terpenoid induction patterns of JA-treated and L. hesperus-damaged plants were characterized for different plant structures and artificial diet assays using purified terpenoids (gossypol/ heliocide H1/4) were conducted. Nymphs were negatively affected if kept on plants damaged by caterpillars or sprayed with JA. Performance of nymphs was increased if they fed on squares and by the Bt-trait which had a positive effect on boll quality as food. In general, JA-sprayed plants (but not L. hesperus infested plants) showed increased levels of terpenoids in the plant structures analyzed which was especially pronounced in Bt cotton. Nymphs were not negatively affected by terpenoids in artificial diet assays indicating that other inducible cotton responses are responsible for the found negative effects on L. hesperus. Overall, genetically engineered plant defenses can benefit plant bugs by releasing them from plant-mediated indirect competition with lepidopterans which might contribute to increasing numbers of hemipterans in Bt cotton.