Consequences of root herbivory for aboveground plant interactions with herbivores, pollinators, and a fungal pathogen
Plants interact with multiple organisms both above and below the soil surface, and the impacts of these interactions have direct consequences for the plant as well as indirect consequences for the other interactors. Root herbivory can have significant effects on plant growth and reproduction, and it can also influence plant interactions with aboveground herbivores, pollinators, and pathogens. However these indirect effects on aboveground interactions are poorly understood. We examined the impacts of a belowground root herbivore on plant growth and reproduction, leaf herbivory, pollinator behavior, and pathogen infection in an agroecosystem using Cucumis sativus (cucumber). We manipulated early-season root herbivory by applying four densities of Acalymma vittatum (striped cucumber beetle) larvae. We also evaluated the role of pollinators in fruit production and tested for pollen limitation using a hand-pollination treatment.
Early-season root damage had clear negative effects on plant growth and reproduction by reducing plant size, female flower production, and fruit production. Aboveground interactions with pollinators and a pathogen, but not leaf herbivores, were affected by belowground herbivory. Leaf damage was unaffected by root herbivory treatments. Pollinator visitation was significantly lower on plants that received higher numbers of root-feeding larvae, and this pattern was consistent for the two most abundant pollinators, honey bees and Lepidoptera. Infection by downy mildew, an economically important pathogen, was significantly higher on plants that did not receive root herbivores, suggesting that root damage may provide induced resistance against this fungal pathogen. Hand pollination treatments did not affect any response variables, and there were no pollination x herbivory interactions, demonstrating that plants were not pollen-limited in this system. By reducing pollinator visitation, root herbivores may cause reductions in plant reproduction in addition to their direct negative effects of tissue consumption. However, if low to moderate levels of root damage reduce later effects of downy mildew, late-season plant reproduction could be prolonged, increasing overall reproduction (and crop yield for farmers).