Intraspecific plant-soil feedback in four tropical tree species is inconsistent in a field experiment.

PREMISE: Soil microbes can influence patterns of diversity in plant communities via plant-soil feedbacks. Intraspecific plant-soil feedbacks occur when plant genotype leads to variations in soil microbial composition, resulting in differences in the performance of seedlings growing near their maternal plants versus seedlings growing near nonmaternal conspecific plants. How consistently such intraspecific plant-soil feedbacks occur in natural plant communities is unclear, especially in variable field conditions. METHODS: In an in situ experiment with four native tree species on Barro Colorado Island (BCI), Panama, seedlings of each species were transplanted beneath their maternal tree or another conspecific tree in the BCI forest. Mortality and growth were assessed at the end of the wet season (~4 months post-transplant) and at the end of the experiment (~7 months post-transplant). RESULTS: Differences in seedling performance among field treatments were inconsistent among species and eroded over time. Effects of field environment were detected at the end of the wet season in two of the four species: Virola surinamensis seedlings had higher survival beneath their maternal tree than other conspecific trees, while seedling survival of Ormosia macrocalyx was higher under other conspecific trees. However, these differences were gone by the end of the experiment. CONCLUSIONS: Our results suggest that intraspecific plant-soil feedbacks may not be consistent in the field for tropical tree species and may have a limited role in determining seedling performance in tropical tree communities. Future studies are needed to elucidate the environmental and genetic factors that determine the incidence and direction of intraspecific plant-soil feedbacks in plant communities.

Arbuscular mycorrhizal fungi influence host infection during epidemics in a wild plant pathosystem.

While pathogenic and mutualistic microbes are ubiquitous across ecosystems and often co-occur within hosts, how they interact to determine patterns of disease in genetically diverse wild populations is unknown. To test whether microbial mutualists provide protection against pathogens, and whether this varies among host genotypes, we conducted a field experiment in three naturally occurring epidemics of a fungal pathogen, Podosphaera plantaginis, infecting a host plant, Plantago lanceolata, in the Åland Islands, Finland. In each population, we collected epidemiological data on experimental plants from six allopatric populations that had been inoculated with a mixture of mutualistic arbuscular mycorrhizal fungi or a nonmycorrhizal control. Inoculation with arbuscular mycorrhizal fungi increased growth in plants from every population, but also increased host infection rate. Mycorrhizal effects on disease severity varied among host genotypes and strengthened over time during the epidemic. Host genotypes that were more susceptible to the pathogen received stronger protective effects from inoculation. Our results show that arbuscular mycorrhizal fungi introduce both benefits and risks to host plants, and shift patterns of infection in host populations under pathogen attack. Understanding how mutualists alter host susceptibility to disease will be important for predicting infection outcomes in ecological communities and in agriculture.

Strain Diversity and Spatial Distribution Are Linked to Epidemic Dynamics in Host Populations.

AbstractThe inherently variable nature of epidemics renders predictions of when and where infection is expected to occur challenging. Differences in pathogen strain composition, diversity, fitness, and spatial distribution are generally ignored in epidemiological modeling and are rarely studied in natural populations, yet they may be important drivers of epidemic trajectories. To examine how these factors are linked to epidemics in natural host populations, we collected epidemiological and genetic data from 15 populations of the powdery mildew fungus, Podosphaera plantaginis, on Plantago lanceolata in the Åland Islands, Finland. In each population, we tracked spatiotemporal disease progression throughout one epidemic season and coupled our survey of infection with intensive field sampling of the pathogen. We found that strain composition varied greatly among populations in the landscape. Within populations, strain composition was driven by the sequence of strain activity: early-active strains reached higher abundances, leading to consistent strain compositions over time. Co-occurring strains also varied in their contribution to the growth of the local epidemic, and these fitness inequalities were linked to epidemic dynamics: a higher proportion of hosts became infected in populations containing strains that were more similar in fitness. Epidemic trajectories in the populations were also linked to strain diversity and spatial dynamics: higher infection rates occurred in populations containing higher strain diversity, while spatially clustered epidemics experienced lower infection rates. Together, our results suggest that spatial and/or temporal variation in the strain composition, diversity, and fitness of pathogen populations are important factors generating variation in epidemiological trajectories among infected host populations.

Facilitative priority effects drive parasite assembly under coinfection.

Host individuals are often coinfected with diverse parasite assemblages, resulting in complex interactions among parasites within hosts. Within hosts, priority effects occur when the infection sequence alters the outcome of interactions among parasites. Yet, the role of host immunity in this process remains poorly understood. We hypothesized that the host response to the first infection could generate priority effects among parasites, altering the assembly of later-arriving strains during epidemics. We tested this by infecting sentinel host genotypes of Plantago lanceolata with strains of the fungal parasite Podosphaera plantaginis and measuring susceptibility to subsequent infection during experimental and natural epidemics. In these experiments, prior infection by one strain often increased susceptibility to other strains, and these facilitative priority effects altered the structure of parasite assemblages, but this effect depended on host genotype, host population and parasite genotype. Thus, host genotype, spatial structure and priority effects among strains all independently altered parasite assembly. Using a fine-scale survey and sampling of infections on wild hosts in several populations, we then identified a signal of facilitative priority effects, which altered parasite assembly during natural epidemics. Together, these results provide evidence that within-host priority effects of early-arriving strains can drive parasite assembly, with implications for how strain diversity is spatially and temporally distributed during epidemics.

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.

Species associations structured by environment and land-use history promote beta-diversity in a temperate forest.

Patterns of diversity and community composition in forests are controlled by a combination of environmental factors, historical events, and stochastic or neutral mechanisms. Each of these processes has been linked to forest community assembly, but their combined contributions to alpha and beta-diversity in forests has not been well explored. Here we use variance partitioning to analyze approximately 40,000 individual trees of 49 species, collected within 137 ha of sampling area spread across a 900-ha temperate deciduous forest reserve in Pennsylvania to ask (1) To what extent is site-to-site variation in species richness and community composition of a temperate forest explained by measured environmental gradients and by spatial descriptors (used here to estimate dispersal-assembly or unmeasured, spatially structured processes)? (2) How does the incorporation of land-use history information increase the importance attributed to deterministic community assembly? and (3) How do the distributions and abundances of individual species within the community correlate with these factors? Environmental variables (i.e., topography, soils, and distance to stream), spatial descriptors (i.e., spatial eigenvectors derived from Cartesian coordinates), and land-use history variables (i.e., land-use type and intensity, forest age, and distance to road), explained about half of the variation in both species richness and community composition. Spatial descriptors explained the most variation, followed by measured environmental variables and then by land- use history. Individual species revealed variable responses to each of these sets of predictor variables. Several species were associated with stream habitats, and others were strictly delimited across opposing north- and south-facing slopes. Several species were also associated with areas that experienced recent (i.e., <100 years) human land-use impacts. These results indicate that deterministic factors, including environmental and land-use history variables, are important drivers of community response. The large amount of "unexplained" variation seen here (about 50%) is commonly observed in other such studies attempting to explain distribution and abundance patterns of plant communities. Determining whether such large fractions of unaccounted for variation are caused by a lack of sufficient data, or are an indication of stochastic features of forest communities globally, will remain an important challenge for ecologists in the future.

Testing predictions of the Janzen-Connell hypothesis: a meta-analysis of experimental evidence for distance- and density-dependent seed and seedling survival.

The Janzen-Connell hypothesis proposes that specialist natural enemies, such as herbivores and pathogens, maintain diversity in plant communities by reducing survival rates of conspecific seeds and seedlings located close to reproductive adults or in areas of high conspecific density. Variation in the strength of distance- and density-dependent effects is hypothesized to explain variation in plant species richness along climatic gradients, with effects predicted to be stronger in the tropics than the temperate zone and in wetter habitats compared to drier habitats.We conducted a comprehensive literature search to identify peer-reviewed experimental studies published in the 40+ years since the hypothesis was first proposed. Using data from these studies, we conducted a meta-analysis to assess the current weight of evidence for the distance and density predictions of the Janzen-Connell hypothesis.Overall, we found significant support for both the distance- and density-dependent predictions. For all studies combined, survival rates were significantly reduced near conspecifics compared to far from conspecifics, and in areas with high densities of conspecifics compared to areas with low conspecific densities. There was no indication that these results were due to publication bias.The strength of distance and density effects varied widely among studies. Contrary to expectations, this variation was unrelated to latitude, and there was no significant effect of study region. However, we did find a trend for stronger distance and density dependence in wetter sites compared to sites with lower annual precipitation. In addition, effects were significantly stronger at the seedling stage compared to the seed stage.Synthesis. Our study provides support for the idea that distance- and density-dependent mortality occurs in plant communities world-wide. Available evidence suggests that natural enemies are frequently the cause of such patterns, consistent with the Janzen-Connell hypothesis, but additional studies are needed to rule out other mechanisms (e.g. intraspecific competition). With the widespread existence of density and distance dependence clearly established, future research should focus on assessing the degree to which these effects permit species coexistence and contribute to the maintenance of diversity in plant communities.