Root herbivory indirectly affects above‐ and below‐ground community members and directly reduces plant performance

Abstract

Summary There is a widespread recognition that above‐ and below‐ground organisms are linked through their interactions with host plants that span terrestrial subsystems. In addition to direct effects on plants, soil organisms such as root herbivores can indirectly alter interactions between plants and other community members, with potentially important effects on plant growth and fitness. We manipulated root herbivory by Acalymma vittatum in Cucumis sativus to determine indirect effects on arbuscular mycorrhizal fungi, leaf herbivory, the leaf pathogen downy mildew and pollinators. We also manipulated pollen receipt by plants to determine whether root herbivory reduced plant reproduction through changes in pollinator visitation. Overall, root herbivory had strong net negative effects on plant growth and fitness, with 34% reductions in both leaf and fruit production by high root damage levels relative to control, despite reduced infection by downy mildew. High root herbivory also reduced floral visitation by 39%, apparently due to lower flower production, as flower size and scent were unaffected. Above‐ground herbivory was not affected by root herbivores. Although root herbivory reduced pollinator visits, pollen receipt manipulations had no effect on fruit set, indicating that reduced pollinator service did not affect plant reproduction. Synthesis. Root herbivory had indirect effects on a range of community members, including mutualists and antagonists both above‐ and below‐ground. Although reduced pathogen infection associated with root herbivory would be expected to benefit plants, root herbivory had an overall strong negative effect on plant growth and reproduction, indicating that direct negative effects over‐rode any potential indirect benefits.