Less cooperative belowground plant mutualists negatively affect aboveground herbivore growth and survival

Resource mutualists like nitrogen (N)-fixing rhizobia can improve the nutrition of plants available to higher trophic levels. However, there is substantial intraspecific variation in mutualist quality. How this variation in mutualist quality affects higher trophic levels, such as herbivores, is unclear, as high-quality resource mutualists could increase both leaf nutrient content, which should improve herbivore growth, but also plant chemical defenses, which are expected to inhibit herbivore growth. We evaluated the effect of rhizobium strains of varying mutualist quality on the survival and development of a generalist insect herbivore, the beet armyworm (Spodoptera exigua), reared on alsike clover (Trifolium hybridum). We inoculated T. hybridum with cooperative (“high-quality”) and less cooperative (“low-quality”) rhizobia strains, measured plant growth, nutrients, and metabolites, and fed the leaves to S. exigua. We found that high-quality rhizobium strains significantly improved S. exigua survival, but also increased development time compared to low-quality strains. Furthermore, some developmental traits, such as pupal weight and adult wing area, increased in high-quality treatments. Inoculation with strains of varying quality impacted T. hybridum nutrition and phytochemistry, suggesting that both could mediate herbivore responses to mutualist quality. The effects of rhizobium genetic variation on herbivores exceeded the effects of N-fertilization alone: S. exigua fed leaves from uninoculated, fertilized plants had decreased survival compared to caterpillars fed leaves from high-quality partners, implying that N deposition into ecosystems does not fully replace benefits provided by rhizobia to higher trophic levels.