The importance of plant ontogeny for tri-trophic interactions

Background/Question/Methods Plant-herbivore-natural enemy interactions have been shown to vary markedly in space and time. However, studies assessing changes in the direction and magnitude of these interactions have traditionally examined the role of spatial variation more than the role of temporal change. Physiological and anatomical constraints during plant ontogeny has been shown to affect the expression of numerous plant traits relevant to higher trophic levels such as nutritional content as well as physical and chemical defenses. Yet, we know little about how these sources of temporal variation can directly and/or indirectly mediate tri-trophic interactions. Here, I explore how ontogenetic variation in plant defenses and nutritional quality can alter tri-trophic interactions: 1) directly through changes in butterfly oviposition choice and caterpillar performance, or 2) indirectly through changes in caterpillar predation risk. To assess these questions, I conducted greenhouse and laboratory work using an ecological model system composed of Ribwort-leaf plantain, Plantago lanceolata (Plantaginaceae), and its specialist herbivore, the Buckeye butterfly (Junonia coenia, Nymphalidae).  Using four distinct plant ontogenetic stages (i.e. seedling, juvenile, reproductive and post-reproductive) I evaluated: butterfly oviposition choice, caterpillar performance (survival rate, growth rate and nutritional indices), caterpillar sequestration rate, and caterpillar immune response to simulated parasitoid eggs.

Results/Conclusions Plant age significantly influenced plant-herbivore interactions both directly and indirectly. Buckeye butterflies greatly preferred younger developmental stages of P. lanceolata over older reproductive stages, laying on average 60% more eggs on seedling and juvenile plants than on reproductive stages. In accordance with the “mother knows best” hypothesis, caterpillars also performed better on young developmental stages. Caterpillars feeding on P. lanceolata seedlings or juvenile plants showed lower mortality rate (p<0.05), faster relative growth rate (p<0.001) and increased digestive efficiency (p<0.001) than those feeding in reproductive and post reproductive hosts. In contrast, caterpillars feeding in younger developmental stages acquired lower levels of sequestered chemical defenses (p<0.001), which can render them more susceptible to predation. Finally, host plant age also altered the ability of a caterpillar to mount an immune response against simulated parasitoid eggs (p<0.01), with caterpillars reared on older life stages showing a compromised immune response compared to those feeding on younger plant age classes. These results demonstrate that changes in plant traits throughout plant development can greatly influence insect herbivores by directly altering herbivore preference and performance and indirectly altering herbivore-natural enemy interactions.