Toxic plants improve caterpillar immunity against some, but not all, parasites

Enakshi Ghosh, Ryan L. Paul, Paul J. Ode

This is a plain language summary of a Functional Ecology research article which can be found here.

Plants, insect herbivores, and their natural enemies (e.g., predators and parasites) rank among the most abundant and ecologically important species interactions in nearly all terrestrial environments. Insect herbivores, such as caterpillars, face a lot of challenges from below and above. Caterpillars must cope with plant anti-herbivore defenses including chemicals that are toxic or repellent to caterpillars—frequently via detoxification or excretion. At the same time caterpillars must avoid becoming prey to predators or hosts to parasitoids (frequently, parasitic wasps that develop inside their caterpillar hosts). Caterpillars are well-known to employ specialized hemolymph (“blood”) cells that provide immunity against internally developing parasitoid eggs and larva. These immune cells form hardened capsules around parasitoid eggs, resulting in death of the parasitoid from asphyxiation.

Fifth (top) and third (bottom) instar caterpillars of the cabbage white butterfly (Pieris rapae) feeding on a cabbage leaf (credit: Dhaval Vyas)

At the intersection of the bottom-up effects of plant defense chemistry and the top-down effects of parasitoids are caterpillar immune systems, traits that are frequently overlooked in studies of plant-insect interactions. Those studies that have considered caterpillar immune responses have generally found that caterpillars feeding on plants with higher levels of defensive chemistry typically have suppressed immune responses. In these situations, caterpillars feeding on more toxic plants may suffer both reduced survivorship—both from the direct effects on their development success as well as the indirect effects via their suppressed immune systems—resulting in increased mortality from their parasitoids. Interestingly, we show that caterpillars of the cabbage white butterfly (Pieris rapae) enjoy enhanced production of immunity hemocytes. However, enhanced production of hemocytes involved in immunity against parasitoids comes with a cost. Such caterpillars attained smaller body weights and experienced increased development times. Moreover, the enhanced production of immune cells in caterpillars that feed on more toxic host plant does not always translate into increased protection from parasitoids. While caterpillars feeding on more toxic host plants enjoyed enhanced immune responses that increased their protection from the parasitoid Cotesia glomerata, such caterpillars remained equally susceptible to another common parasitoid, C. rubecula. Our study suggests that host plants have a strong impact on the expression of caterpillar immunity; however, the effectiveness against parasitoids strongly depends on parasitoid identity, and its ability to escape caterpillar immunity.  


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