Evidence of within-species specialization by soil microbes and the implications for plant community diversity.

Microbes are thought to maintain diversity in plant communities by specializing on particular species, but it is not known whether microbes that specialize within species (i.e., on genotypes) affect diversity or dynamics in plant communities. Here we show that soil microbes can specialize at the within-population level in a wild plant species, and that such specialization could promote species diversity and seed dispersal in plant communities. In a shadehouse experiment in Panama, we found that seedlings of the native tree species, Virola surinamensis (Myristicaceae), had reduced performance in the soil microbial community of their maternal tree compared with in the soil microbial community of a nonmaternal tree from the same population. Performance differences were unrelated to soil nutrients or to colonization by mycorrhizal fungi, suggesting that highly specialized pathogens were the mechanism reducing seedling performance in maternal soils. We then constructed a simulation model to explore the ecological and evolutionary consequences of genotype-specific pathogens in multispecies plant communities. Model results indicated that genotype-specific pathogens promote plant species coexistence-albeit less strongly than species-specific pathogens-and are most effective at maintaining species richness when genetic diversity is relatively low. Simulations also revealed that genotype-specific pathogens select for increased seed dispersal relative to species-specific pathogens, potentially helping to create seed dispersal landscapes that allow pathogens to more effectively promote diversity. Combined, our results reveal that soil microbes can specialize within wild plant populations, affecting seedling performance near conspecific adults and influencing plant community dynamics on ecological and evolutionary time scales.

Resistance Genes Affect How Pathogens Maintain Plant Abundance and Diversity.

AbstractSpecialized pathogens are thought to maintain plant community diversity; however, most ecological studies treat pathogens as a black box. Here we develop a theoretical model to test how the impact of specialized pathogens changes when plant resistance genes (R-genes) mediate susceptibility. This work synthesizes two major hypotheses: the gene-for-gene model of pathogen resistance and the Janzen-Connell hypothesis of pathogen-mediated coexistence. We examine three scenarios. First, R-genes do not affect seedling survival; in this case, pathogens promote diversity. Second, seedlings are protected from pathogens when their R-gene alleles and susceptibility differ from those of nearby conspecific adults, thereby reducing transmission. If resistance is not costly, pathogens are less able to promote diversity because populations with low R-gene diversity suffer higher mortality, putting those populations at a disadvantage and potentially causing their exclusion. R-gene diversity may also be reduced during population bottlenecks, creating a priority effect. Third, when R-genes affect survival but resistance is costly, populations can avoid extinction by losing resistance alleles, as they cease paying a cost that is unneeded. Thus, the impact pathogens can have on tree diversity depends on the mechanism of plant-pathogen interactions. Future empirical studies should examine which of these scenarios most closely reflects the real world.

When and where plant-soil feedback may promote plant coexistence: a meta-analysis.

Plant-soil feedback (PSF) theory provides a powerful framework for understanding plant dynamics by integrating growth assays into predictions of whether soil communities stabilise plant-plant interactions. However, we lack a comprehensive view of the likelihood of feedback-driven coexistence, partly because of a failure to analyse pairwise PSF, the metric directly linked to plant species coexistence. Here, we determine the relative importance of plant evolutionary history, traits, and environmental factors for coexistence through PSF using a meta-analysis of 1038 pairwise PSF measures. Consistent with eco-evolutionary predictions, feedback is more likely to mediate coexistence for pairs of plant species (1) associating with similar guilds of mycorrhizal fungi, (2) of increasing phylogenetic distance, and (3) interacting with native microbes. We also found evidence for a primary role of pathogens in feedback-mediated coexistence. By combining results over several independent studies, our results confirm that PSF may play a key role in plant species coexistence, species invasion, and the phylogenetic diversification of plant communities.

Host-specific effects of soil microbial filtrates prevail over those of arbuscular mycorrhizae in a fragmented landscape.

Plant-soil interactions have been shown to determine plant community composition in a wide range of environments. However, how plants distinctly interact with beneficial and detrimental organisms across mosaic landscapes containing fragmented habitats is still poorly understood. We experimentally tested feedback responses between plants and soil microbial communities from adjacent habitats across a disturbance gradient within a human-modified tropical montane landscape. In a greenhouse experiment, two components of soil microbial communities were amplified; arbuscular mycorrhizal fungi (AMF) and a filtrate excluding AMF spores from the soils of pastures (high disturbance), coffee plantations (intermediate disturbance), and forest fragments (low disturbance), using potted seedlings of 11 plant species common in these habitats (pasture grass, coffee, and nine native species). We then examined their effects on growth of these same 11 host species with reciprocal habitat inoculation. Most plant species received a similar benefit from AMF, but differed in their response to the filtrates from the three habitats. Soil filtrate from pastures had a net negative effect on plant growth, while filtrates from coffee plantations and forests had a net positive effect on plant growth. Pasture grass, coffee, and five pioneer tree species performed better with the filtrate from "away" (where these species rarely occur) compared to "home" (where these species typically occur) habitat soils, while four shade-tolerant tree species grew similarly with filtrates from different habitats. These results suggest that pastures accumulate species-specific soil enemies, while coffee plantations and forests accumulate beneficial soil microbes that benefit pioneer native plants and coffee, respectively. Thus, compared to AMF, soil filtrates exerted stronger habitat and host-specific effects on plants, being more important mediators of plant-soil feedbacks across contrasting habitats.

An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest.

Tropical forests are renowned for their high diversity, yet in many sites a single tree species accounts for the majority of the individuals in a stand. An explanation for these monodominant forests remains elusive, but may be linked to mycorrhizal symbioses. We tested three hypotheses by which ectomycorrhizas might facilitate the dominance of the tree, Oreomunnea mexicana, in montane tropical forest in Panama. We tested whether access to ectomycorrhizal networks improved growth and survival of seedlings, evaluated whether ectomycorrhizal fungi promote seedling growth via positive plant-soil feedback, and measured whether Oreomunnea reduced inorganic nitrogen availability. We found no evidence that Oreomunnea benefits from ectomycorrhizal networks or plant-soil feedback. However, we found three-fold higher soil nitrate and ammonium concentrations outside than inside Oreomunnea-dominated forest and a correlation between soil nitrate and Oreomunnea abundance in plots. Ectomycorrhizal effects on nitrogen cycling might therefore provide an explanation for the monodominance of ectomycorrhizal tree species worldwide.

Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest.

The accumulation of species-specific enemies around adults is hypothesized to maintain plant diversity by limiting the recruitment of conspecific seedlings relative to heterospecific seedlings. Although previous studies in forested ecosystems have documented patterns consistent with the process of negative feedback, these studies are unable to address which classes of enemies (for example, pathogens, invertebrates, mammals) exhibit species-specific effects strong enough to generate negative feedback, and whether negative feedback at the level of the individual tree is sufficient to influence community-wide forest composition. Here we use fully reciprocal shade-house and field experiments to test whether the performance of conspecific tree seedlings (relative to heterospecific seedlings) is reduced when grown in the presence of enemies associated with adult trees. Both experiments provide strong evidence for negative plant-soil feedback mediated by soil biota. In contrast, above-ground enemies (mammals, foliar herbivores and foliar pathogens) contributed little to negative feedback observed in the field. In both experiments, we found that tree species that showed stronger negative feedback were less common as adults in the forest community, indicating that susceptibility to soil biota may determine species relative abundance in these tropical forests. Finally, our simulation models confirm that the strength of local negative feedback that we measured is sufficient to produce the observed community-wide patterns in tree-species relative abundance. Our findings indicate that plant-soil feedback is an important mechanism that can maintain species diversity and explain patterns of tree-species relative abundance in tropical forests.

Restoration age affects microbial-herbaceous plant interactions in an oak woodland.

In degraded ecosystems, soil microbial communities (SMCs) may influence the outcomes of ecological restoration. Restoration practices can affect SMCs, though it is unclear how variation in the onset of restoration activities in woodlands affects SMCs, how those SMCs influence the performance of hard-to-establish woodland forbs, and how different woodland forbs shape SMCs. In this study, we quantified soil properties and species abundances in an oak woodland restoration chronosequence (young, intermediate, and old restorations). We measured the growth of three woodland forb species when inoculated with live whole-soil from young, intermediate, or old restorations. We used DNA metabarcoding to characterize SMCs of each inoculum treatment and the soil after conditioning by each plant species. Our goals were to (1) understand how time since the onset of restoration affected soil abiotic properties, plant communities, and SMCs in a restoration chronosequence, (2) test growth responses of three forb species to whole-soil inoculum from restoration sites, and (3) characterize changes in SMCs before and after conditioning by each forb species. Younger restored woodlands had greater fire-sensitive tree species and lower concentrations of soil phosphorous than intermediate or older restored woodlands. Bacterial and fungal soil communities varied significantly among sites. Forbs exhibited the greatest growth in soil from the young restoration. Each forb species developed a unique soil microbial community. Our results highlight how restoration practices affect SMCs, which can in turn affect the growth of hard-to-establish forb species. Our results also highlight that the choice of forb species can alter SMCs, which could have long-term potential consequences for restoration success.

Complex facilitation and competition in a temperate grassland: loss of plant diversity and elevated CO2 have divergent and opposite effects on oak establishment.

Encroachment of woody vegetation into grasslands is a widespread phenomenon that alters plant community composition and ecosystem function. Woody encroachment is often the result of fire suppression, but it may also be related to changes in resource availability associated with global environmental change. We tested the relative strength of three important global change factors (CO(2) enrichment, nitrogen deposition, and loss of herbaceous plant diversity) on the first 3 years of bur oak (Quercus macrocarpa) seedling performance in a field experiment in central Minnesota, USA. We found that loss of plant diversity decreased initial oak survival but increased overall oak growth. Conversely, elevated CO(2) increased initial oak seedling survival and reduced overall growth, especially at low levels of diversity. Nitrogen deposition surprisingly had no net effect on survival or growth. The magnitude of these effects indicates that long-term woody encroachment trends may be most strongly associated with those few individuals that survive, but grow much larger in lower diversity patches. Further, while the CO(2) results and the species richness results appear to describe opposing trends, this is due only to the fact that the natural drivers are moving in opposite directions (decreasing species richness and increasing CO(2)). Interestingly, the mechanisms that underlie both patterns are very similar, increased CO(2) and increased species richness both increase herbaceous biomass which (1) increases belowground competition for resources and (2) increases facilitation of early plant survival under a more diverse plant canopy; in other words, both competition and facilitation help determine community composition in these grasslands.

Above- and belowground interactions drive habitat segregation between two cryptic species of tropical trees.

In the lowlands of central Panama, the Neotropical pioneer tree Trema micrantha (sensu lato) exists as two cryptic species: "landslide" Trema is restricted to landslides and road embankments, while "gap" Trema occurs mostly in treefall gaps. In this study, we explored the relative contributions of biotic interactions and physical factors to habitat segregation in T. micrantha. Field surveys showed that soils from landslides were significantly richer in available phosphorus and harbored distinct arbuscular mycorrhizal fungal (AMF) communities compared to gap soils. Greenhouse experiments designed to determine the effect of these abiotic and biotic differences showed that: (1) both landslide and gap species performed better in sterilized soil from their own habitat, (2) the availability of phosphorus and nitrogen was limiting in gap and landslide soils, respectively, (3) a standardized AMF inoculum increased performance of both species, but primarily on gap soils, and (4) landslide and gap species performed better when sterilized soils were inoculated with the microbial inoculum from their own habitat. A field experiment confirmed that survival and growth of each species was highest in its corresponding habitat. This experiment also showed that browsing damage significantly decreased survival of gap Trema on landslides. We conclude that belowground interactions with soil microbes and aboveground interactions with herbivores contribute in fundamental ways to processes that may promote and reinforce adaptive speciation.

Soil microbes drive the classic plant diversity-productivity pattern.

Ecosystem productivity commonly increases asymptotically with plant species diversity, and determining the mechanisms responsible for this well-known pattern is essential to predict potential changes in ecosystem productivity with ongoing species loss. Previous studies attributed the asymptotic diversity-productivity pattern to plant competition and differential resource use (e.g., niche complementarity). Using an analytical model and a series of experiments, we demonstrate theoretically and empirically that host-specific soil microbes can be major determinants of the diversity-productivity relationship in grasslands. In the presence of soil microbes, plant disease decreased with increasing diversity, and productivity increased nearly 500%, primarily because of the strong effect of density-dependent disease on productivity at low diversity. Correspondingly, disease was higher in plants grown in conspecific-trained soils than heterospecific-trained soils (demonstrating host-specificity), and productivity increased and host-specific disease decreased with increasing community diversity, suggesting that disease was the primary cause of reduced productivity in species-poor treatments. In sterilized, microbe-free soils, the increase in productivity with increasing plant species number was markedly lower than the increase measured in the presence of soil microbes, suggesting that niche complementarity was a weaker determinant of the diversity-productivity relationship. Our results demonstrate that soil microbes play an integral role as determinants of the diversity-productivity relationship.

Globally, plant-soil feedbacks are weak predictors of plant abundance.

Plant-soil feedbacks (PSFs) have been shown to strongly affect plant performance under controlled conditions, and PSFs are thought to have far reaching consequences for plant population dynamics and the structuring of plant communities. However, thus far the relationship between PSF and plant species abundance in the field is not consistent. Here, we synthesize PSF experiments from tropical forests to semiarid grasslands, and test for a positive relationship between plant abundance in the field and PSFs estimated from controlled bioassays. We meta-analyzed results from 22 PSF experiments and found an overall positive correlation (0.12 ≤  r ¯  ≤ 0.32) between plant abundance in the field and PSFs across plant functional types (herbaceous and woody plants) but also variation by plant functional type. Thus, our analysis provides quantitative support that plant abundance has a general albeit weak positive relationship with PSFs across ecosystems. Overall, our results suggest that harmful soil biota tend to accumulate around and disproportionately impact species that are rare. However, data for the herbaceous species, which are most common in the literature, had no significant abundance-PSFs relationship. Therefore, we conclude that further work is needed within and across biomes, succession stages and plant types, both under controlled and field conditions, while separating PSF effects from other drivers (e.g., herbivory, competition, disturbance) of plant abundance to tease apart the role of soil biota in causing patterns of plant rarity versus commonness.

Specificity between Neotropical tree seedlings and their fungal mutualists leads to plant-soil feedback.

A growing body of evidence obtained largely from temperate grassland studies suggests that feedbacks occurring between plants and their associated soil biota are important to plant community assemblage. However, few studies have examined the importance of soil organisms in driving plant-soil feedbacks in forested systems. In a tropical forest in central Panama, we examined whether interactions between tree seedlings and their associated arbuscular mycorrhizal fungi (AMF) lead to plant-soil feedback. Specifically, do tropical seedlings modify their own AMF communities in a manner that either favors or inhibits the next cohort of conspecific seedlings (i.e., positive or negative feedback, respectively)? Seedlings of two shade-tolerant tree species (Eugenia nesiotica, Virola surinamensis) and two pioneer tree species (Luehea seemannii, Apeiba aspera) were grown in pots containing identical AMF communities composed of equal amounts of inoculum of six co-occurring AMF species. The different AMF-host combinations were all exposed to two light levels. Under low light (2% PAR), only two of the six AMF species sporulated, and we found that host identity did not influence composition of AMF spore communities. However, relative abundances of three of the four AMF species that produced spores were influenced by host identity when grown under high light (20% PAR). Furthermore, spores of one of the AMF species, Glomus geosporum, were common in soils of Luehea and Eugenia but absent in soils of Apeiba and Virola. We then conducted a reciprocal experiment to test whether AMF communities previously modified by Luehea and Apeiba differentially affected the growth of conspecific and heterospecific seedlings. Luehea seedling growth did not differ between soils containing AMF communities modified by Luehea and Apeiba. However, Apeiba seedlings were significantly larger when grown with Apeiba-modified AMF communities, as compared to Apeiba seedlings grown with Luehea-modifed AMF communities. Our experiments suggest that interactions between tropical trees and their associated AMF are species-specific and that these interactions may shape both tree and AMF communities through plant-soil feedback.

Soil biota increase the likelihood for coexistence among competing plant species.

Theory predicts that stable species coexistence will occur when population growth rates of competitively dominant species are suppressed when at high conspecific density. Although there is now compelling evidence that plant communities exhibit negative density dependence, the relative importance of the underlying processes leading to these patterns is rarely tested. We coupled reciprocal greenhouse and field experiments with community dynamics modeling to untangle the relative importance of soil biota from competition as stabilizing forces to coexistence. We found that (1) plant-soil biotic interactions compared to competitive interactions were stronger stabilizing forces, (2) only the strength of plant-soil biotic interactions was dependent on plant evolutionary history, and (3) the variation in the strength of plant-soil biotic interactions was correlated with relative abundance patterns in an opposite way than was the variation in the strength of competitive interactions. Collectively, our results demonstrate the fundamental role soil biota have in maintaining plant community diversity.

Mutualist and pathogen traits interact to affect plant community structure in a spatially explicit model.

Empirical studies show that plant-soil feedbacks (PSF) can generate negative density dependent (NDD) recruitment capable of maintaining plant community diversity at landscape scales. However, the observation that common plants often exhibit relatively weaker NDD than rare plants at local scales is difficult to reconcile with the maintenance of overall plant diversity. We develop a spatially explicit simulation model that tracks the community dynamics of microbial mutualists, pathogens, and their plant hosts. We find that net PSF effects vary as a function of both host abundance and key microbial traits (e.g., host affinity) in ways that are compatible with both common plants exhibiting relatively weaker local NDD, while promoting overall species diversity. The model generates a series of testable predictions linking key microbial traits and the relative abundance of host species, to the strength and scale of PSF and overall plant community diversity.

Author Correction: Mutualist and pathogen traits interact to affect plant community structure in a spatially explicit model.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Abundance, origin, and phylogeny of plants do not predict community-level patterns of pathogen diversity and infection.

Pathogens have the potential to shape plant community structure, and thus, it is important to understand the factors that determine pathogen diversity and infection in communities. The abundance, origin, and evolutionary relationships of plant hosts are all known to influence pathogen patterns and are typically studied separately. We present an observational study that examined the influence of all three factors and their interactions on the diversity of and infection of several broad taxonomic groups of foliar, floral, and stem pathogens across three sites in a temperate grassland in the central United States. Despite that pathogens are known to respond positively to increases in their host abundances in other systems, we found no relationship between host abundance and either pathogen diversity or infection. Native and exotic plants did not differ in their infection levels, but exotic plants hosted a more generalist pathogen community compared to native plants. There was no phylogenetic signal across plants in pathogen diversity or infection. The lack of evidence for a role of abundance, origin, and evolutionary relationships in shaping patterns of pathogens in our study might be explained by the high generalization and global distributions of our focal pathogen community, as well as the high diversity of our plant host community. In general, the community-level patterns of aboveground pathogen infections have received less attention than belowground pathogens, and our results suggest that their patterns might not be explained by the same drivers.

Prairie plants harbor distinct and beneficial root-endophytic bacterial communities.

Plant-soil feedback studies attempt to understand the interplay between composition of plant and soil microbial communities. A growing body of literature suggests that plant species can coexist when they interact with a subset of the soil microbial community that impacts plant performance. Most studies focus on the microbial community in the soil rhizosphere; therefore, the degree to which the bacterial community within plant roots (root-endophytic compartment) influences plant-microbe interactions remains relatively unknown. To determine if there is an interaction between conspecific vs heterospecific soil microbes and plant performance, we sequenced root-endophytic bacterial communities of five tallgrass-prairie plant species, each reciprocally grown with soil microbes from each hosts' soil rhizosphere. We found evidence of plant-soil feedbacks for some pairs of plant hosts; however, the strength and direction of feedbacks varied substantially across plant species pairs-from positive to negative feedbacks. Additionally, each plant species harbored a unique subset of root-endophytic bacteria. Conspecifics that hosted similar bacterial communities were more similar in biomass than individuals that hosted different bacterial communities, suggesting an important functional link between root-endophytic bacterial community composition and plant fitness. Our findings suggest a connection between an understudied component of the root-endophytic microbiome and plant performance, which may have important implications in understanding plant community composition and coexistence.

Negative plant-soil feedbacks are stronger in agricultural habitats than in forest fragments in the tropical Andes.

There is now strong evidence suggesting that interactions between plants and their species-specific antagonistic microbes can maintain native plant community diversity. In contrast, the decay in diversity in plant communities invaded by nonnative plant species might be caused by weakening negative feedback strengths, perhaps because of the increased relative importance of plant mutualists such as arbuscular mycorrhizal fungi (AMF). Although the vast majority of studies examining plant-soil feedbacks have been conducted in a single habitat type, there are fewer studies that have tested how the strength and direction of these feedbacks change across habitats with differing dominating plants. In a fragmented montane agricultural system in Colombia, we experimentally teased apart the relative importance of AMF and non-AMF microbes (a microbial filtrate) to the strength and direction of feedbacks in both native and nonnative plant species. We hypothesized that native tree species of forest fragments would exhibit stronger negative feedbacks with a microbial filtrate that likely contained pathogens than with AMF alone, whereas nonnative plant species, especially a highly invasive dominant grass, would exhibit overall weaker negative feedbacks or even positive feedbacks regardless of the microbial type. We reciprocally inoculated each of 10 plant species separately with either the AMF community or the microbial filtrate originating from their own conspecifics, or with the AMF or microbial filtrate originating from each of the other nine heterospecific plant species. Overall, we found that the strength of negative feedback mediated by the filtrate was much stronger than feedbacks mediated by AMF. Surprisingly, we found that the two nonnative species, Urochloa brizantha and Coffea arabica, experienced stronger negative feedbacks with microbial filtrate than did the native forest tree species, suggesting that species-specific antagonistic microbes accumulate when a single host species dominates, as is the case in agricultural habitats. However, negative feedback between forest trees and agricultural species suggests that soil community dynamics may contribute to the re-establishment of native species into abandoned agricultural lands. Furthermore, our finding of no negative feedbacks among trees in forest fragments may be due to a loss in diversity of those microbes that drive diversity-maintaining processes in intact tropical forests.

Response to Comment on "Plant diversity increases with the strength of negative density dependence at the global scale".

Hülsmann and Hartig suggest that ecological mechanisms other than specialized natural enemies or intraspecific competition contribute to our estimates of conspecific negative density dependence (CNDD). To address their concern, we show that our results are not the result of a methodological artifact and present a null-model analysis that demonstrates that our original findings-(i) stronger CNDD at tropical relative to temperate latitudes and (ii) a latitudinal shift in the relationship between CNDD and species abundance-persist even after controlling for other processes that might influence spatial relationships between adults and recruits.

Response to Comment on "Plant diversity increases with the strength of negative density dependence at the global scale".

Chisholm and Fung claim that our method of estimating conspecific negative density dependence (CNDD) in recruitment is systematically biased, and present an alternative method that shows no latitudinal pattern in CNDD. We demonstrate that their approach produces strongly biased estimates of CNDD, explaining why they do not detect a latitudinal pattern. We also address their methodological concerns using an alternative distance-weighted approach, which supports our original findings of a latitudinal gradient in CNDD and a latitudinal shift in the relationship between CNDD and species abundance.