Mycorrhizal‐herbivore interactions and the competitive release of subdominant tallgrass prairie species

Abstract

Abstract 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 below‐ground grazing and arbuscular mycorrhizal (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 below‐ground herbivores on AM symbiosis in tallgrass prairie mesocosms, (b) independent and interacting effects of above‐ and below‐ground 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 above‐ground and below‐ground herbivores, while herbivore effects were additive. The dominance of mycorrhizal‐dependent C4 grasses in the presence of AM 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 AM 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 AM symbiosis and with grasshopper herbivory, while AM‐related increases in the above‐ground 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 arbuscular mycorrhizal symbiosis is the key driver of dominance of C4 grasses in the tallgrass prairie, with foliar and root herbivory being two mechanisms for maintenance of plant diversity.