Mutualisms in a warming world: How increased temperatures affect the outcomes of multi-mutualist interactions.

In nature, plant species simultaneously interact with many different mutualistic partners. These mutualists may influence one another through direct interference or indirectly by competing for shared reward resources or through alteration of plant traits. Together, these mutualists also may combine to affect plant hosts in ways that may not be predictable based on pairwise interactions. Given that the outcome of mutualistic interactions often depends on environmental conditions, multi-mutualist effects on one another, and their plant hosts may be affected by global changes. Here, we grew focal plants under simulated global warming conditions and manipulated the presence of partner mutualists to test how warming affects the outcome of interactions between focal plants and their partners (nitrogen-fixing rhizobia, ant defenders, and pollinators) and interactions among these partner mutualists. We find that warming alters the fitness benefits plants receive from rhizobium resource mutualists but not ant mutualists and that warming altered plant investment in all mutualists. We also find that mutualist partners interact, often by altering the availability of plant-produced rewards that facilitate interactions with other partners. Our work illustrates that global changes may affect some but not all mutualisms, often asymmetrically (e.g., affecting investment in the mutualist partner but not plant host benefits) and also highlights the ubiquity of interactions between the multiple mutualists associating with a shared host.

Effects of multiple mutualists on plants and their associated arthropod communities.

Although most studies of mutualisms focus on a single partner at a time, host species often associate with multiple mutualist partners simultaneously. Because of potential interactions between mutualists, only studying a single type of mutualism could lead to a biased perspective of mutualism benefit and how mutualisms may scale-up to affect communities. The legume Chamaecrista fasciculata engages in a resource mutualism with nitrogen-fixing rhizobia and also forms symbiotic interactions with ants by providing nectar in exchange for defense against herbivores. Although they provide very different benefits to the plant, both mutualists receive carbon resources from the plant. As a result, these two mutualists are likely to interact, potentially competing for carbon resources or mutually benefitting each other via their positive effects on plant hosts. In a full-factorial field experiment, we explored how rhizobia and ants influence one another, C. fasciculata fitness, and the associated arthropod community. Ants reduced plant allocation to rhizobia, but ants also increased rhizobia contamination of uninoculated plants, suggesting that ants may disperse rhizobia. In turn, rhizobia increased ant abundances, with ants preferentially tending plants with rhizobia. Chamaecrista fasciculata received substantial fitness benefits from rhizobia; in contrast, associating with ants reduced fitness. Additionally, the mutualists interacted to influence the abundance of other arthropods found on the plants. Rhizobia increased arthropod abundances, likely because more nitrogen-rich leaf tissue was more attractive to arthropod herbivores, but ants negated these increases. As these results illustrate, multiple mutualists may interact, influencing each other's abundance and the abundance of other community members.

Quantifying nonadditive selection caused by indirect ecological effects.

In natural biological communities, species interact with many other species. Multiple species interactions can lead to indirect ecological effects that have important fitness consequences and can cause nonadditive patterns of natural selection. Given that indirect ecological effects are common in nature, nonadditive selection may also be quite common. As a result, quantifying nonadditive selection resulting from indirect ecological effects may be critical for understanding adaptation in natural communities composed of many interacting species. We describe how to quantify the relative strength of nonadditive selection resulting from indirect ecological effects compared to the strength of pairwise selection. We develop a clear method for testing for nonadditive selection caused by indirect ecological effects and consider how it might affect adaptation in multispecies communities. We use two case studies to illustrate how our method can be applied to empirical data sets. Our results suggest that nonadditive selection caused by indirect ecological effects may be common in nature. Our hope is that trait-based approaches, combined with multifactorial experiments, will result in more estimates of nonadditive selection that reveal the relative importance of indirect ecological effects for evolution in a community context.

Mutualistic rhizobia reduce plant diversity and alter community composition.

Mutualistic interactions can be just as important to community dynamics as antagonistic species interactions like competition and predation. Because of their large effects on both abiotic and biotic environmental variables, resource mutualisms, in particular, have the potential to influence plant communities. Moreover, the effects of resource mutualists such as nitrogen-fixing rhizobia on diversity and community composition may be more pronounced in nutrient-limited environments. I experimentally manipulated the presence of rhizobia across a nitrogen gradient in early assembling mesocosm communities with identical starting species composition to test how the classic mutualism between nitrogen-fixing rhizobia and their legume host influence diversity and community composition. After harvest, I assessed changes in α-diversity, community composition, ß-diversity, and ecosystem properties such as inorganic nitrogen availability and productivity as a result of rhizobia and nitrogen availability. The presence of rhizobia decreased plant community diversity, increased community convergence (reduced ß-diversity), altered plant community composition, and increased total community productivity. These community-level effects resulted from rhizobia increasing the competitive dominance of their legume host Chamaecrista fasciculata. Moreover, different non-leguminous species responded both negatively and positively to the presence of rhizobia, indicating that rhizobia are driving both inhibitory and potentially facilitative effects in communities. These findings expand our understanding of plant communities by incorporating the effects of positive symbiotic interactions on plant diversity and composition. In particular, rhizobia that specialize on dominant plants may serve as keystone mutualists in terrestrial plant communities, reducing diversity by more than 40%.