Photoinhibition: A link between effects of the environment on eucalyptus leaf chemistry and herbivory

We investigated effects of light and nutrients on whole plant growth, ecophysiology, and leaf chemistry of Eucalyptus nitens seedlings, and the effect of these characteristics on herbivory by common brushtail possums (Trichosurus vulpecula) and red-bellied pademelons (Thylogale billardierii). We compared results of the response of plant secondary chemistry to changes in environmental conditions against two contrasting hypotheses: (1) the carbon:nutrient balance hypothesis (CNBH) and (2) the photoinhibition hypothesis. Nutrient and light levels affected relative growth rate and leaf area ratio of seedlings. Electron transport rates and optimum photochemical efficiencies indicated different rates of carbon fixation between treatments, consistent with levels of chlorophyll and xanthophyll pigments. Nonphotochemical quenching and xanthophylls per unit chlorophyll were negatively correlated with total chlorophyll content. Consistent with the photoinhibition hypothesis, levels of leaf phenolics (flavonols, hydrolyzable tannins, and sideroxylonals) per unit chlorophyll were also negatively correlated with total chlorophyll content. In contrast, phenolic levels on a dry-mass basis were not consistent with predictions of the CNBH; they were better explained as a response to severity of photoinhibition than by reallocation of resources from growth to defense. Total essential oil and cineole levels were positively correlated with nitrogen levels, but there was an interaction in their response to nutrients and light. Thus, levels of essential oils were not well predicted by the CNBH. Sideroxylonal and cineole levels were not correlated, and we hypothesize that different processes and requirements drive their production. Intake of seedlings by possums and pademelons was not directly negatively correlated with levels of hydrolyzable tannins, sideroxylonals, or essential oils. An interaction of the costs of these compounds against benefits of nitrogen levels may explain patterns in intake. We suggest that, while environmentally induced levels of carbon-based plant secondary metabolites have consequences for herbivory, photoinhibition may drive the adjustment of levels of leaf phenolics in response to variation in light and nutrients. This contrasts with the view that these adjustments represent a trade-off in resource allocation between growth and defense.