Escaping herbivory through chemical novelty? Field performance and herbivore attack of the cardenolide-producing crucifer plant Erysimum cheiranthoides

Abstract

Plants in the Brassicaceae produce glucosinolates as potent defenses against generalist herbivores, but many specialists can tolerate or deactivate these compounds. As a potential counter-adaptation, plants in the genus Erysimum evolved novel cardenolide defenses alongside ancestral glucosinolates. Here we grew the dually defended E. cheiranthoides and the phenologically similar Rhamnospermum nigrum in agricultural fields surrounded by Brassicaceae crops and monitored herbivore communities, leaf damage, and plant performance of focal plants over two seasons. In the second year, we additionally manipulated herbivore density and plant competition to identify direct and indirect effects on plant fitness. Both plant species were attacked by a diverse community of specialist herbivores, but most herbivores strongly preferred R. nigrum, reaching higher densities and causing intense damage that suppressed growth of these plants. A similar herbivore community attacked dually-defended E. cheiranthoides, but herbivores occurred at lower densities, caused less damage, and had no negative effect on growth. Consequently, herbivore suppression through pesticide application increased R. nigrum growth but provided no benefit to E. cheiranthoides. In fact, for E. cheiranthoides growing under heterospecific competition, pesticide application reduced growth due to increased competition by R. nigrum. Our results agree with a successful escape of E. cheiranthoides from herbivory, as even though plants are still attacked when herbivores are abundant, these herbivores caused little damage and caused no reduction in fitness. However, the escape from herbivory has likely come at loss of competitive ability when herbivore pressure is low, which would explain why despite its key innovation, E. cheiranthoides has been unable to gain dominance in any plant community.