Plant productivity response to inter- and intra-symbiont diversity: Mechanisms, manifestations and meta-analyses.

Symbiont diversity can have large effects on plant growth but the mechanisms generating this relationship remain opaque. We identify three potential mechanisms underlying symbiont diversity-plant productivity relationships: provisioning with complementary resources, differential impact of symbionts of varying quality and interference between symbionts. We connect these mechanisms to descriptive representations of plant responses to symbiont diversity, develop analytical tests differentiating these patterns and test them using meta-analysis. We find generally positive symbiont diversity-plant productivity relationships, with relationship strength varying with symbiont type. Inoculation with symbionts from different guilds (e.g. mycorrhizal fungi and rhizobia) yields strongly positive relationships, consistent with complementary benefits from functionally distinct symbionts. In contrast, inoculation with symbionts from the same guild yields weak relationships, with co-inoculation not consistently generating greater growth than the best individual symbiont, consistent with sampling effects. The statistical approaches we outline, along with our conceptual framework, can be used to further explore plant productivity and community responses to symbiont diversity, and we identify critical needs for additional research to explore context dependency in these relationships.

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.

Nitrogen-fixing symbiotic bacteria act as a global filter for plant establishment on islands.

Island biogeography has classically focused on abiotic drivers of species distributions. However, recent work has highlighted the importance of mutualistic biotic interactions in structuring island floras. The limited occurrence of specialist pollinators and mycorrhizal fungi have been found to restrict plant colonization on oceanic islands. Another important mutualistic association occurs between nearly 15,000 plant species and nitrogen-fixing (N-fixing) bacteria. Here, we look for evidence that N-fixing bacteria limit establishment of plants that associate with them. Globally, we find that plants associating with N-fixing bacteria are disproportionately underrepresented on islands, with a 22% decline. Further, the probability of N-fixing plants occurring on islands decreases with island isolation and, where present, the proportion of N-fixing plant species decreases with distance for large, but not small islands. These findings suggest that N-fixing bacteria serve as a filter to plant establishment on islands, altering global plant biogeography, with implications for ecosystem development and introduction risks.

Perennial, but not annual legumes synergistically benefit from infection with arbuscular mycorrhizal fungi and rhizobia: a meta-analysis.

Many plant species simultaneously interact with multiple symbionts, which can, but do not always, generate synergistic benefits for their host. We ask if plant life history (i.e. annual vs perennial) can play an important role in the outcomes of the tripartite symbiosis of legumes, arbuscular mycorrhizal fungi (AMF), and rhizobia. We performed a meta-analysis of 88 studies examining outcomes of legume-AMF-rhizobia interactions on plant and microbial growth. Perennial legumes associating with AMF and rhizobia grew larger than expected based on their response to either symbiont alone (i.e. their response to co-inoculation was synergistic). By contrast, annual legume growth with co-inoculation did not differ from additive expectations. AMF and rhizobia differentially increased phosphorus (P) and nitrogen (N) tissue concentration. Rhizobium nodulation increased with mycorrhizal fungi inoculation, but mycorrhizal fungi colonization did not increase with rhizobium inoculation. Microbial responses to co-infection were significantly correlated with synergisms in plant growth. Our work supports a balanced plant stoichiometry mechanism for synergistic benefits. We find that synergisms are in part driven by reinvestment in complementary symbionts, and that time-lags in realizing benefits of reinvestment may limit synergisms in annuals. Optimization of microbiome composition to maximize synergisms may be critical to productivity, particularly for perennial legumes.

Rapid adaptation (or not) in restored plant populations.

Mismatches between the traits of a colonizing population and a novel habitat can generate strong selection, potentially resulting in rapid adaptation. However, for most colonization events, it can be difficult to detect rapid adaptation or distinguish it from nonadaptive evolutionary changes. Here, I take advantage of a replicated prairie restoration experiment to compare recently established plant populations in two closely located restored prairies to each other and to their shared source population to test for rapid adaptation. Using a reciprocal transplant experiment six years after the populations were established, I found that one restored plant population showed evidence of adaptation, outperforming the other restored population when grown at its home site. In contrast, I detected no evidence for adaptation at the other site. These findings demonstrate that while rapid adaptation can occur in colonizing plant populations, it may not be the rule. Better understanding of when adaptation may or may not occur in these contexts may help us use evolution to our advantage, potentially improving establishment of desirable species in restored habitats.

Evolution in novel environments: Do restored prairie populations experience strong selection?

When populations colonize new habitats, they are likely to experience novel environmental conditions, and as a consequence may experience strong selection. While selection and the resulting evolutionary responses may have important implications for establishment success in colonizing populations, few studies have estimated selection in such scenarios. Here we examined evidence of selection in recently established plant populations in two prairie restorations in close proximity (<15 km apart) using two approaches: (1) we tested for evidence of past selection on a suite of traits in two Chamaecrista fasciculata populations by comparing the restored populations to each other and their shared source population in common gardens to quantify evolutionary responses and (2) we measured selection in the field. We found evidence of past selection on flowering time, specific leaf area, and root nodule production in one of the populations, but detected contemporary selection on only one trait (plant height). Our findings demonstrate that while selection can occur in colonizing populations, resulting in significant trait differences between restored populations in fewer than six generations, evolutionary responses differ across even nearby populations sown with the same source population. Because contemporary measures of selection differed from evolutionary responses to past selection, our findings also suggest that selection likely differs over the early stages of succession that characterize young prairies.

Evolution of increased Medicaco polymorpha size during invasion does not result in increased competitive ability.

Species invading new habitats experience novel selection pressures that can lead to rapid evolution, which may contribute to invasion success and/or increased impact on native community members. Many studies have hypothesized that plants in the introduced range will be larger than those in the native range, leading to increases in competitive ability. There is mixed support for evolution of larger sizes in the introduced range, but few studies have explicitly tested whether evolutionary changes result in decreased competitive responses or increased competitive effects on other species in the community. Here, we show that introduced Medicago polymorpha genotypes produced 14% more aboveground and 41% more belowground biomass than genotypes from the native range, suggesting that evolutionary changes in size occurred after introduction. However, these size differences were only observed in the absence of competition. The competitive effects of introduced and native range genotypes on three species that commonly co-occur with Medicago in invaded regions were remarkably similar. These results suggest that evolutionary increases in size during biological invasions do not necessarily alter the competitive effects of the invader on other community members, but may increase invasion success in disturbed or low competition environments.

Shrubs as ecosystem engineers across an environmental gradient: effects on species richness and exotic plant invasion.

Ecosystem-engineering plants modify the physical environment and can increase species diversity and exotic species invasion. At the individual level, the effects of ecosystem engineers on other plants often become more positive in stressful environments. In this study, we investigated whether the community-level effects of ecosystem engineers also become stronger in more stressful environments. Using comparative and experimental approaches, we assessed the ability of a native shrub (Ericameria ericoides) to act as an ecosystem engineer across a stress gradient in a coastal dune in northern California, USA. We found increased coarse organic matter and lower wind speeds within shrub patches. Growth of a dominant invasive grass (Bromus diandrus) was facilitated both by aboveground shrub biomass and by growing in soil taken from shrub patches. Experimental removal of shrubs negatively affected species most associated with shrubs and positively affected species most often found outside of shrubs. Counter to the stress-gradient hypothesis, the effects of shrubs on the physical environment and individual plant growth did not increase across the established stress gradient at this site. At the community level, shrub patches increased beta diversity, and contained greater rarified richness and exotic plant cover than shrub-free patches. Shrub effects on rarified richness increased with environmental stress, but effects on exotic cover and beta diversity did not. Our study provides evidence for the community-level effects of shrubs as ecosystem engineers in this system, but shows that these effects do not necessarily become stronger in more stressful environments.

Responses to invasion and invader removal differ between native and exotic plant groups in a coastal dune.

The spread of exotic, invasive species is a global phenomenon that is recognized as a major source of environmental change. Although many studies have addressed the effects of exotic plants on the communities they invade, few have quantified the effects of invader removal on plant communities, or considered the degree to which different plant groups vary in response to invasion and invader removal. We evaluated the effects of an exotic succulent, iceplant (Carpobrotus edulis), on a coastal dune plant community in northern California, as well as the community responses to its removal. To assess possible mechanisms by which iceplant affects other plants, we also evaluated its above- and belowground influences on the germination and growth of a dominant exotic annual grass, Bromus diandrus. We found that iceplant invasion was associated with reduced native plant cover as well as increased cover and density of some exotic plants-especially exotic annual grasses. However, iceplant removal did not necessarily lead to a reversal of these effects: removal increased the cover and density of both native and exotic species. We also found that B. diandrus grown in iceplant patches, or in soil where iceplant had been removed, had poorer germination and growth than B. diandrus grown in soil not influenced by iceplant. This suggests that the influence of iceplant on this dune plant community occurs, at least in part, due to belowground effects, and that these effects remain after iceplant has been removed. Our study demonstrates the importance of considering how exotic invasive plants affect not only native species, but also co-occurring exotic taxa. It also shows that combining observational studies with removal experiments can lead to important insights into the influence of invaders and the mechanisms of their effects.