Abstract. Biotic interactions play primary roles in major theories of the distribution and abundance of species, yet the nature of these biotic interactions can depend upon the larger ecological community. Leguminous plants, for example, commonly associate with both arbuscular mycorrhizal fungi (AMF) and rhizobia bacteria, and the pairwise interactions may depend upon the presence or identity of the third partner. To determine if the dynamics of plant-AMF and plant-rhizobia interactions are affected by the alternate symbiont, we manipulated the presence and identity of each symbiont, as well as levels of the nutrients supplied by each symbiont (nitrogen and phosphorus), on the growth of prairie legume Amorpha canescens. We found strong synergistic effects of AMF and rhizobia inoculation on plant biomass production that were independent of nutrient levels. AMF and rhizobia responses were each influenced by the other, but not in the same direction. AMF infection increased root nodule number and mass, but rhizobia inoculation decreased AMF hyphal colonization of roots. The relative benefits of each combination of symbionts depended upon phosphorus level. The effect of nitrogen was also contingent on the biotic environment where nitrogen addition decreased nodulation, but this decrease was reduced with coinfection by AMF. Our results demonstrate a strong contingency on the co-occurrence of AMF and rhizobia for the long-term fitness of A. canescens, and suggest that the belowground community is critical for the success of this species in tallgrass prairies.

In nature, plants often associate with multiple symbionts concurrently, yet the effects of tripartite symbioses are not well understood. We expected synergistic growth responses from plants associating with functionally distinct symbionts. In contrast, symbionts providing similar benefits to a host may reduce host plant growth. We reviewed studies investigating the effect of multiple interactions on host plant performance. Additionally, we conducted a meta-analysis on the studies that performed controlled manipulations of the presence of two microbial symbionts. Using response ratios, we investigated the effects on plants of pairs of symbionts (mycorrhizal fungi, fungal endophytes, and nitrogen-fixers). The results did not support the view that arbuscular mycorrhizal (AM) fungi and rhizobia should interact synergistically. In contrast, we found the joint effects of fungal endophytes and arbuscular mycorrhizal fungi to be greater than expected given their independent effects. This increase in plant performance only held for antagonistic endophytes, whose negative effects were alleviated when in association with AM fungi, while the impact of beneficial endophytes was not altered by infection with AM fungi. Generalizations from the meta-analysis were limited by the substantial variation within types of interactions and the data available, highlighting the need for more research on a range of plant systems.

Plants simultaneously associate with multiple microbial symbionts throughout their lifetimes. To address the question of whether the effects of simultaneous symbionts are contingent on the specific identities, we conducted a greenhouse experiment manipulating the presence and identities of arbuscular mycorrhizal fungi (AMF) and fungal endophytes on the shared host grass Elymus hystrix. Each plant host was inoculated with one of two AMF species having varying effects on host growth, or a sterile soil control. Further, we used naturally occurring endophyte‐infected (E+) and uninfected (E–) individuals from two populations of the endophyte Epichloë elymi that varied in their interaction with E. hystrix. We then measured responses of plants, AMF, and fungal endophytes. Overall, we found that the combined effects of AMF and fungal endophytes on plant growth were additive, reflecting the mutualistic quality of each symbiont independently interacting with host plants. However, fungal endophyte infection differentially altered hyphal colonization of the two AMF species and the identity of the coinfecting AMF species affected fungal endophyte fitness traits. The results of this study demonstrate that the outcome of interspecific symbiotic interactions varies with partner identity such that the effects of simultaneous symbioses can not be generalized.