The Bt-trait in Cotton Affects Plant-mediated Competition Among Herbivores

Introduction Cotton plants from the genus Gossypium are well defended against arthropod herbivores by a broad range of resistance mechanisms. These include direct mechanisms like trichomes and the production of toxins and indirect mechanisms like the emission of volatiles or extra-floral nectaries to attract and retain natural enemies1. One of the best understood resistance trait of cotton is the terpenoid gossypol and its processor or related compounds1. These terpenoids are highly effective in controlling a broad range of insect pests, from aphids to lepidopterans. Production of the terpenoids is inducible by damage caused by some herbivores (e.g., most species of Lepidoptera) but not by others (e.g., aphids). However, these arthropod resistance mechanisms do not prevent large economic losses due to insect pests2, and cotton was historically one of the most sprayed crops in the world. This has changed with the introduction of Lepidoptera-protected Bt-cotton producing Cry proteins derived from Bacillus thuringiensis (Berliner) (Bt)2. In recent years, increased populations of sap-feeding herbivores were reported in Bt cotton in different parts of the world. In most cases this was reported for plant and stink bugs, but also aphids and whiteflies can profit from Bt cotton. The rise of pests that are not targeted by the Bt trait is commonly explained by the reduction in the application of broad-spectrum insecticides to control pest Lepidoptera2. Other factors that could contribute to the emergence of pests in Bt cotton include the release from competition with lepidopteran pests. This competition could be direct, through resource depletion due to lepidopteran feeding, or caused indirectly by induction of secondary plant compounds due to prior herbivory3. While cases of direct competition between Bt-target and non-target herbivores have been reported4,5, indirect competition was not considered as a mechanism before.