The multi-trophic context of plant defense: ecological and evolutionary implications of variation in milkweeds

Abstract

Plants exhibit great diversity in defense-related traits, such as toxins and spines. Most explanations for this variation assume that such traits are costly because they require resources to produce and maintain; however, controlled experiments frequently fail to document costs of plant defenses. One explanation for this pattern is that ecological context matters. I develop the hypothesis that certain plant traits impose ecological costs in a multi-trophic context because they disrupt predation on herbivores. Because milkweed plants are toxic and harbor specialist herbivores that sequester the toxins to defend themselves against generalist predators, I expect plants to incur ecological costs of defense in this system. I investigate the impact of variation among milkweed species on the ecology and evolution of predators that consume herbivores, testing for costs of defense in a multi-trophic context. I show that plants can strongly impact the preference and performance of some predators and generate patterns consistent with ecological costs of defense. However, I also demonstrate that other traits and processes, such as plant tolerance of herbivory and predator tolerance of plant-derived defense, may have the potential to mitigate such ecological costs. Consequently, ecological costs of defense are unlikely to be fixed but are instead subject to coevolutionary dynamics. As introductions, extinctions, and range shifts change the pool of potentially interacting species, a more predictive understanding of the way individual traits affect, and are affected by, the community context in which they occur will improve our ability to prioritize and manage human impacts on these systems.