Top down and bottom up: Herbivore performance is determined by diet breadth, plant defenses and natural enemies

Although many influential hypotheses in plant-animal interactions address the top-down and bottom-up controls of herbivore populations, the Tri-Trophic Interactions (TTI) Hypothesis is the first to make predictions regarding the simultaneous effects of plant quality, herbivore diet breadth, and natural enemies on herbivore performance.  I present data from laboratory experiments testing components of the TTI hypothesis.  Specifically, I address how plant secondary metabolites and natural enemies interactively determine the performance herbivores.  I focus specifically on native Colorado wildflowers in the genus Penstemon (Plantaginaceae), which are chemically defended by bitter iridoid glycosides (IGs), and their associated lepidopteran herbivores, including the specialist Anicia checkerspot (Euphydryas anicia).  Checkerspot caterpillars were reared on one of two Penstemon species: P. virgatus, which contains the IGs catalpol and scutellarioside, or P. glaber, which contains only catalpol.  Caterpillars from each diet were then used either in bioassays with ant predators (Formica pallidefulva) or in assays to measure their cellular immune response.  The ant bioassays showed that solutions containing caterpillars were unpalatable compared to control solutions and ants generally avoided the checkerspot caterpillars.  Furthermore, ants showed a negative response to pure IGs, which suggest that the IGs were likely responsible for the unpalatability of the caterpillars.  Data from the immune response assays will also be considered in the light of the tradeoffs between protection from predators and protection from parasitoids.  I will discuss the potential implications of different plant chemical defenses on herbivore vulnerability to natural enemies and the role that the novel TTI Hypothesis plays in these interactions.