The importance of plant ontogeny for tri-trophic interactions

Plant-herbivore-natural enemy interactions can vary markedly in space and time. Yet, most studies assessing changes in plant defensive traits, and their consequences for higher trophic levels, have been conducted at single host plant developmental stages. The goal of this study was to assess the extent to which resource allocation constraints throughout plant development (i.e. ontogeny) influence the expression of plant constitutive and herbivore-induced defensive traits and their effects on plant-herbivore-natural enemy interactions. A series of experiments using multiple developmental stages of Plantago lanceolata (Plantaginaceae), and a specialist herbivore, the Buckeye butterfly, Junonia coenia (Nymphalidae), were performed. Results showed that investment in constitutive chemical (iridoid glycosides) and physical defenses significantly increased, while leaf water and nitrogen concentrations decreased with plant age. Moreover, plant age significantly influenced the ability of P. lanceolata to tolerate or induce defenses after damage. Ontogenetic changes in plant growth rate and allelochemical synthesis helped to explain why induction was mostly achieved earlier during plant development, whereas compensatory growth showed the opposite pattern. In contrast, extrinsic factors such as frequency and intensity of damage failed to modify age-dependent responses to leaf damage. Finally, ontogenetic patterns in P. lanceolata defensive traits significantly influenced tri-trophic interactions. Oviposition tests showed that Buckeye butterflies significantly preferred younger ontogenetic stages, laying 60% more eggs on juvenile than on reproductive plants. In turn, caterpillars feeding on juvenile plants showed faster growth and increased digestive efficiency, yet they acquired two to five times less sequestered defenses, suggesting that J. coenia predation risk should decrease with host plant age. However, higher sequestered iridoid glycosides decreased larval immunocompetence by up to 30%, suggesting higher susceptibility to parasitoid attack as host plants age increases. Thus, I demonstrated for the first time that ontogenetic patterns in plant defensive traits, mediated by caterpillar performance and palatability, can alter the strength of the top-down control of herbivores. This study improves our understanding of the role of ontogenetic variation in plant quality and defenses for tri-trophic interactions, providing a framework for testing hypotheses related to the evolution of plant defenses and the context dependency of bottom-up and top-down controls shaping herbivore population dynamics