Disentangling the Influence of Water Limitation and Simultaneous above and Belowground Herbivory on Plant Tolerance and Resistance to Stress

Abstract

Plants face multiple biotic and abiotic stressors simultaneously. Many species can tolerate and resist stress, but countermeasures differ between roots and leaves. Since herbivores and environmental conditions modulate costs and benefits of plant defence traits, stress responses are context-dependent. We examined whole-plant tolerance and resistance responses to individual and combined effects of above and belowground herbivory under variable water conditions. We manipulated water availability and access by two common herbivores (Spodoptera exigua caterpillars and Meloidogyne incognita nematodes) to Solanum lycocarpum. Plants were either watered based on historical regional averages or the 30% reduction predicted by IPCC studies. Herbivory treatments included isolated above (AG) and belowground (BG) attacks, simultaneous (AGBG) attacks and no-herbivory controls. We then parameterized generalized linear mixed-effects models with data on plant survival, leaf and root biomass accumulation, root complexity and terpenoid concentration. Foliar herbivory increased terpenoid concentrations in roots relative to no-herbivory plants under control water but decreased concentrations in both roots and leaves under drought. Similarly, root feeders increased concentrations of terpenoids in leaves under control water but decreased concentrations only in roots under drought. Plants challenged with AGBG herbivory had greater whole-plant biomass (i.e. tolerance) and lower total concentrations of defensive compounds (i.e. resistance) than plants exposed to no-herbivore controls, regardless of water conditions. Importantly, the capacity of plants to grow or produce terpenoids changes when herbivory level is considered. In plants exposed to AGBG herbivory, greater nematode infection was related to decreases in whole-plant biomass and marginal increases in total terpenoid concentration. Ultimately, accounting only for individual AG and BG responses would have led to different conclusions and underestimated the magnitude of S. lycocarpum’s compensatory responses. A ‘whole-plant’ approach revealed that belowground herbivory is the primary driver of tolerance in plants surviving moderate water stress. Synthesis. Whole-plant responses to stress in variable environments are complex, and their comprehensive understanding requires accounting for belowground herbivores and root responses.