Arbuscular mycorrhizal fungi mediate how plant herbivory history influences herbivore performance

Herbivore performance is influenced by plant host quality and chemical defences, both of which are influenced by belowground symbionts of plants and herbivory history. The previous herbivory may suppress or facilitate subsequent herbivore performance through changes in plant chemistry and tissue quality. Likewise, arbuscular mycorrhizal fungi (AM fungi) can alter both plant quality and plant responses to aboveground herbivory, as mycorrhizal-mediated alterations of the nutritional budget may alter leaf nutritional quality, chemical profiles, and available leaf surface area. Despite evidence that both herbivory history and AM fungi can independently affect herbivore performance, few studies directly test both at the same time. Here, the role of AM fungi and herbivory history on the performance of a pest insect (Spodoptera frugiperda) on a common forb (Solidago altissima) grown with different AM fungal additions (no AM fungi, single species, multispecies) was directly tested. Evidence that the effect of herbivory history on herbivore performance depended on the AM fungal environment of the plant was found. Specifically, the composition of the AM fungal additions altered the directionality of herbivore performance on plants with and without prior herbivory. Without added AM fungi, herbivores demonstrated a classically suppressed growth rate on grazed plants. With a single species AM fungi added, herbivores performed the same on host plants, regardless of herbivory history. With diverse AM fungi added, herbivore growth increased on grazed plants. Mycorrhizal-mediated changes in plant chemical profiles did not explain herbivore performance. These results emphasise the need for direct tests of mycorrhizal diversity on plant-insect interactions.