Host plant chemistry enhances herbivore cellular immunity with differential effectiveness against two parasitoid species

Insect herbivores must simultaneously balance bottom-up effects of plant defensive chemistry and the top-down effects of natural enemies. At the intersection of these effects are herbivore immune systems, an herbivore trait that has largely been overlooked in studies of plant-insect interactions. Counter to the majority of studies showing that herbivores feeding on plants containing higher levels of toxins are immunocompromised, we demonstrate that Pieris rapae caterpillars feeding on more toxic host plants have enhanced cellular immunity at the cost of reduced growth rates and body size. However, whether enhanced immune systems are effective defense against parasitoids depends on parasitoid identity. Whereas enhanced immunity provided increased protection against the parasitoid Cotesia glomerata, it did not provide protection against C. rubecula that suppressed and evaded the host's immune system. Our study demonstrates that both herbivore immunity and species identity of trophic participants are crucial in determining the structure of multitrophic interactions.