Plant species with higher chemical defences enhance herbivore cellular immunity with differential effectiveness against two parasitoid species

Abstract Insect herbivores simultaneously experience 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, herbivore traits that have largely been overlooked in studies of plant‐insect interactions. Most previous studies have demonstrated compromised immunity of herbivores that feed on plants with higher defensive chemistry. Many studies have used embedded microfilaments or silica beads as proxies for parasitoid eggs. Yet, parasitoids may evade or suppress host immune responses by injecting venom and calyx fluid, or through modifications of their egg surface structure, necessitating studies that include all three trophic levels to obtain a complete picture of how plant traits may modulate herbivore immunity. Here, we examined the effect of host plant species that differ in glucosinolate (anti‐herbivore compounds produced by plants in the Brassicaceae) concentrations on the immune status of an herbivore and its consequences for two species of parasitoids with different life history traits. We found that larvae of the butterfly Pieris rapae that fed on field mustard Brassica rapa, which contain 52‐fold higher glucosinolate concentrations than collards B. oleracea, attained lower body weights and experienced prolonged development to adulthood. Yet, caterpillars that fed on B. rapa had enhanced cellular immunity, as measured by total and differential haemocyte counts as well as melanization capacity, compared to larvae that fed on B. oleracea. In turn, the likelihood that at least some eggs in clutches of the gregarious endoparasitoid Cotesia glomerata would be encapsulated, leading to a reduction in brood size, were three times greater when their host caterpillars fed on B. rapa compared to B. oleracea. Interestingly, eggs of the solitary endoparasitoid Cotesia rubecula were rarely encapsulated irrespective of the host plant on which their host caterpillar fed. Therefore, our results suggest that plant defence metabolites can influence the expression of herbivore immunity, but the effectiveness of this response strongly depends on the identity of the parasitoid and its ability to evade the caterpillar immune response, and possibly the evolution of these trophic interactions in non‐native systems. Read the free Plain Language Summary for this article on the Journal blog.