Nitrogen-Fixing Rhizobia Affect Multitrophic Interactions in the Field

Virtually all plants employ direct and indirect defenses against herbivores. While it is known that plant defenses can be affected by belowground symbiotic microbes under controlled conditions, studies showing these multitrophic interactions in nature are surprisingly scarce. Here we tested for effects of rhizobia on insect attraction and direct defense (cyanogenesis) in wild lima bean ( Phaseolus lunatus ) plants in Costa Rica. We performed bioassays with rhizobia-inoculated (R+) and rhizobia-free (R-) potted plants distributed among native lima bean communities at two spatially separated field sites (450 km apart) and in two field seasons. Without affecting overall plant size, rhizobia altered leaf chemistry (cyanogenesis and soluble leaf nitrogen) and ultimately insect communities visiting the plants. Natural herbivorous chrysomelid beetles were strongly attracted to R + plants, while natural enemies, ants and parasitoid wasps, preferred R- plants resulting in a particularly high herbivore:carnivore ratio on R + plants. This suggests that symbiotic microbes mediate trophic interactions by influencing both direct and indirect plant defenses against herbivores. Our results show that rhizobia affect the plant defensive phenotype and have cascading effects on plant-insect interactions in nature.