Escaping herbivory through chemical novelty? Field performance and herbivore attack in the cardenolide-producing crucifer plantErysimum cheiranthoides

Abstract

Abstract1.Plants in the Brassicaceae produce glucosinolates as potent defences against generalist herbivores, but many specialists have evolved the ability to tolerate or even deactivate these compounds. As a possible co-evolutionary response to attack by specialists, plants in the genusErysimumgained the ability to produce cardenolide defences in addition to glucosinolates.2.We grew the dually defendedE. cheiranthoidesand the glucosinolate-defendedBrassica nigraside-by-side in agricultural fields surrounded by other Brassicaceae crops. Over the course of two field seasons, we monitored focal plants to characterise their associated herbivore community, and we quantified herbivore damage and measured plant growth. In the second year, we additionally manipulated herbivore density and plant competition to identify direct and indirect effects on plant fitness.3.Both plant species were attacked by a diverse community of specialist herbivores already present on surrounding Brassicaceae crops. Most herbivores strongly favouredB. nigra, reaching higher densities and causing intense damage that largely suppressed growth of this plant. The same herbivores attackedE. cheiranthoides, but at much lower densities that caused little damage and did not impact plant growth.4.In accordance with differential susceptibilities to herbivores, herbivore removal benefittedB. nigraby reducing damage and increasing plant growth, while it had no positive effect onE. cheiranthoides. In fact, herbivore removal had an indirect negative effect onE. cheiranthoideswhen growing in conspecific pairs, as these plants suffered from increased competition by previously herbivore-suppressedB. nigra.Synthesis: Our results agree with a successful escape ofE. cheiranthoidesfrom specialist herbivory, as even though plants are still attacked when herbivores are abundant, these herbivores cause little damage and cause no reduction in fitness. However, the escape from herbivory has likely come at loss of competitive ability in the absence of herbivores, which would explain why despite its key innovation,E. cheiranthoideshas been unable to gain dominance in any plant community.