Plant-microbial-herbivore interactions play a crucial role in the structuring and maintenance of plant communities and biodiversity, yet these relationships are complex. In grassland ecosystems, herbivores have the potential to greatly influence the survival, growth, and reproduction of plants. However, few studies examine interactions of above- and belowground grazing and AM mycorrhizal symbiosis on plant community structure. We established experimental mesocosms containing an assemblage of eight tallgrass prairie grass and forb species in native prairie soil, maintained under mycorrhizal and nonmycorrhizal conditions, with and without native herbivorous soil nematodes, and with and without grasshopper herbivory. Using factorial analysis of variance and principal component analysis, we examined: a) the independent and interacting effects of above- and belowground herbivores on AM symbiosis in tallgrass prairie mesocosms, b) independent and interacting effects of above- and belowground herbivores and mycorrhizal fungi on plant community structure, and c) potential influences of mycorrhizal responsiveness of host plants on herbivory tolerance, and concomitant shifts in plant community composition. Treatment effects were characterized by interactions between AM fungi and both aboveground and belowground herbivores, while herbivore effects were additive. The dominance of mycorrhizal-dependent C₄ grasses in the presence of AMF symbiosis was increased (p < 0.0001) by grasshopper herbivory but reduced (p < 0.0001) by nematode herbivory. Cool-season C₃ grasses exhibited a competitive release in the absence of AMF symbiosis but this effect was largely reversed in the presence of grasshopper herbivory. Forbs showed species-specific responses to both AM fungal inoculation and the addition of herbivores. Biomass of the grazing-avoidant, facultatively mycotrophic forb Brickellia eupatorioides increased (p < 0.0001) in the absence of AMF symbiosis and with grasshopper herbivory, while AMF-related increases in the aboveground biomass of mycorrhizal-dependent forbs Rudbeckia hirta and Salvia azurea were eradicated (p < 0.0001) by grasshopper herbivory. In contrast, nematode herbivory enhanced (p = 0.001) the contribution of Salvia azurea to total biomass.

Synthesis: Our research indicates that AM symbiosis is the key driver of the dominance of C₄ grasses in the tallgrass prairie, with foliar and root herbivory being two mechanisms for the maintenance of plant diversity.

Experimental tallgrass prairie plant communities were constructed and maintained in large mesocosms grown in a greenhouse facility at Kansas State University in Manhattan, KS, USA. Data collected includes end-of-season biomass production and colonization of roots by AM fungi.