James D. Bever

Host-Dependent Sporulation and Species Diversity of Arbuscular Mycorrhizal Fungi in a Mown Grassland

1 In laboratory microcosm experiments, co-occurring plant species were found to support very different rates of sporulation of arbuscular mycorrhizal (AM) fungi. These differences were not affected by the time of harvest, suggesting that they reflect host-dependent differences in fungal growth rates, rather than host-dependent timing of sporulation. 2 Spore counts in field soil and estimates from sorghum trap cultures showed that the association of AM fungi with particular host plants in the field was positively correlated with the sporulation rates observed on those hosts in the microcosm experiments. 3 The AM fungal species richness observed at the field site was high relative to estimates made in previous studies. 23 distinct species of AM fungi were found, seven of which have not been previously described. 4 The host-dependence of the relative growth rates of fungal populations may play an important role in the maintenance of fungal species diversity.

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.

Plant-soil feedbacks: The past, the present and future challenges

Summary Plant–soil feedbacks is becoming an important concept for explaining vegetation dynamics, the invasiveness of introduced exotic species in new habitats and how terrestrial ecosystems respond to global land use and climate change. Using a new conceptual model, we show how critical alterations in plant–soil feedback interactions can change the assemblage of plant communities. We highlight recent advances, define terms and identify future challenges in this area of research and discuss how variations in strengths and directions of plant–soil feedbacks can explain succession, invasion, response to climate warming and diversity-productivity relationships. While there has been a rapid increase in understanding the biological, chemical and physical mechanisms and their interdependencies underlying plant–soil feedback interactions, further progress is to be expected from applying new experimental techniques and technologies, linking empirical studies to modelling and field-based studies that can include plant–soil feedback interactions on longer time scales that also include long-term processes such as litter decomposition and mineralization. Significant progress has also been made in analysing consequences of plant–soil feedbacks for biodiversity-functioning relationships, plant fitness and selection. To further integrate plant–soil feedbacks into ecological theory, it will be important to determine where and how observed patterns may be generalized, and how they may influence evolution. Synthesis. Gaining a greater understanding of plant–soil feedbacks and underlying mechanisms is improving our ability to predict consequences of these interactions for plant community composition and productivity under a variety of conditions. Future research will enable better prediction and mitigation of the consequences of human-induced global changes, improve efforts of restoration and conservation and promote sustainable provision of ecosystem services in a rapidly changing world.

GRASSROOTS ECOLOGY: PLANT–MICROBE–SOIL INTERACTIONS AS DRIVERS OF PLANT COMMUNITY STRUCTURE AND DYNAMICS

A growing body of research on plant-microbe interactions in soil is con- tributing to the development of a new, microbially based perspective on plant community ecology. Soil-dwelling microorganisms are diverse, and interactions with plants vary with respect to specificity, environmental heterogeneity, and fitness impact. Two microbial pro- cesses that may exert key influences on plant community structure and dynamics are mi- crobial mediation of niche differentiation in resource use and feedback dynamics between the plant and soil community. The niche differentiation hypothesis is based on observations that soil nutrients occur in different chemical forms, that different enzymes are required for plant access to these nutrients, and that soil microorganisms are a major source of these enzymes. We predict that plant nutrient partitioning arises from differential associations of plant species with microbes able to access different nutrient pools. Feedback dynamics result from changes in the soil community generated by the specificity of response in plant- microbe interactions. We suggest that positive feedback between plants and soil microbes plays a central role in early successional communities, while negative feedback contributes both to species replacements and to diversification in later successional communities. We further suggest that plant-microbe interactions in the soil are an important organizing force for large-scale spatial gradients in species richness. The relative balance of positive feedback (a homogenizing force) and negative feedback (a diversifying force) may contribute to observed latitudinal (and altitudinal) diversity patterns. Empirical tests of these ideas are needed, but a microbially based perspective for plant ecology promises to contribute to our understanding of long-standing issues in ecology, and to reveal new areas of future research.

Rooting theories of plant community ecology in microbial interactions.

Predominant frameworks for understanding plant ecology have an aboveground bias that neglects soil micro-organisms. This is inconsistent with recent work illustrating the importance of soil microbes in terrestrial ecology. Microbial effects have been incorporated into plant community dynamics using ideas of niche modification and plant-soil community feedbacks. Here, we expand and integrate qualitative conceptual models of plant niche and feedback to explore implications of microbial interactions for understanding plant community ecology. At the same time we review the empirical evidence for these processes. We also consider common mycorrhizal networks, and propose that these are best interpreted within the feedback framework. Finally, we apply our integrated model of niche and feedback to understanding plant coexistence, monodominance and invasion ecology.

Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism.

Mutualisms, beneficial interactions between species, are expected to be unstable because delivery of benefit likely involves fitness costs and selection should favour partners that deliver less benefit. Yet, mutualisms are common and persistent, even in the largely promiscuous associations between plants and soil microorganisms such as arbuscular mycorrhizal fungi. In two different systems, we demonstrate preferential allocation of photosynthate by host plants to the more beneficial of two AM fungal symbionts. This preferential allocation could allow the persistence of the mutualism if it confers sufficient advantage to the beneficial symbiont that it overcomes the cost of mutualism. We find that the beneficial fungus does increase in biomass when the fungi are spatially separated within the root system. However, in well-mixed fungal communities, non-beneficial fungi proliferate as expected from their reduced cost of mutualism. Our findings suggest that preferential allocation within spatially structured microbial communities can stabilize mutualisms between plants and root symbionts.

Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit.

A basic tenet of ecology is that negative feedback on abundance plays an important part in the coexistence of species within guilds. Mutualistic interactions generate positive feedbacks on abundance and therefore are not thought to contribute to the maintenance of diversity. Here, I report evidence of negative feedback on plant growth through changes in the composition of their mutualistic fungal symbionts, arbuscular mycorrhizal (AM) fungi. Negative feedback results from asymmetries in the delivery of benefit between plant and AM fungal species in which the AM fungus that grows best with the plant Plantago lanceolata is a poor growth promoter for Plantago. Growth of Plantago is, instead, best promoted by the AM fungal species that accumulate with a second plant species, Panicum sphaerocarpon. The resulting community dynamic leads to a decline in mutualistic benefit received by Plantago, and can contribute to the coexistence of these two competing plant species.

MAINTENANCE OF DIVERSITY WITHIN PLANT COMMUNITIES: SOIL PATHOGENS AS AGENTS OF NEGATIVE FEEDBACK

The effect of soil pathogens on plant communities was investigated using four old-field perennial plant species and five isolates of a pathogenic oomycete in the genus Pythium. These Pythium strains were isolated from the roots of two of the plant species, Danthonia spicata and Panicum sphaerocarpon, used in a previous experiment on the consequences of changes in the soil community on plant growth. In this previous experiment, Danthonia and Panicum changed the soil community in a manner that reduced their growth relative to that of a third plant species, Anthoxanthum odoratum. In the current experiments, we found that inoculation with Pythium reduced overall plant mass and root: shoot ratios, but Danthonia and Panicum were more susceptible to the presence of Pythium than the other two plant species, Anthoxanthum and Plantago lanceolata. In addition, Pythium ac- cumulates at different rates on different plant species, with a greater than tenfold higher population observed in association with Panicum compared to Anthoxanthum. The results of these experiments suggest that the accumulation of species-specific soil pathogens could account for the previous observation of negative feedback on plant growth through changes in the soil community. As negative feedback may act to maintain plant species diversity within a community, these results suggest that soil pathogens may themselves contribute to the maintenance of plant species diversity.

LOCAL ADAPTATION IN THE LINUM MARGINALE–MELAMPSORA LINI HOST-PATHOGEN INTERACTION

Abstract The potential for local adaptation between pathogens and their hosts has generated strong theoretical and empirical interest with evidence both for and against local adaptation reported for a range of systems. We use the Linum marginale—Melampsora lini plant‐pathogen system and a hierarchical spatial structure to investigate patterns of local adaptation within a metapopulation characterised by epidemic dynamics and frequent extinction of pathogen populations. Based on large sample sizes and comprehensive cross‐inoculation trials, our analyses demonstrate strong local adaptation by Melampsora to its host populations, with this effect being greatest at regional scales, as predicted from the broader spatial scales at which M. lini disperses relative to L. marginale. However, there was no consistent trend for more distant pathogen populations to perform more poorly. Our results further show how the coevolutionary interaction between hosts and pathogens can be influenced by local structure such that resistant hosts select for generally virulent pathogens, while susceptible hosts select for more avirulent pathogens. Empirically, local adaptation has generally been tested in two contrasting ways: (1) pathogen performance on sympatric versus allopatric hosts; and (2) sympatric versus allopatric pathogens on a given host population. In situations where no host population is more resistant or susceptible than others when averaged across pathogen populations (and likewise, no pathogen population is more virulent or avirulent than others), results from these tests should generally be congruent. We argue that this is unlikely to be the case in the metapopulation situations that predominate in natural host‐pathogen interactions, thus requiring tests that control simultaneously for variation in plant and pathogen populations.

Direct and Interactive Effects of Enemies and Mutualists on Plant Performance: a Meta-Analysis

Plants engage in multiple, simultaneous interactions with other species; some (enemies) reduce and others (mutualists) enhance plant performance. Moreover, effects of different species may not be independent of one another; for example, enemies may compete, reducing their negative impact on a plant. The magnitudes of positive and negative effects, as well as the frequency of interactive effects and whether they tend to enhance or depress plant performance, have never been comprehensively assessed across the many published studies on plant-enemy and plant-mutualist interactions. We performed a meta-analysis of experiments in which two enemies, two mutualists, or an enemy and a mutualist were manipulated factorially. Specifically, we performed a factorial meta-analysis using the log response ratio. We found that the magnitude of (negative) enemy effects was greater than that of (positive) mutualist effects in isolation, but in the presence of other species, the two effects were of comparable magnitude. Hence studies evaluating single-species effects of mutualists may underestimate the true effects found in natural settings, where multiple interactions are the norm and indirect effects are possible. Enemies did not on average influence the effects on plant performance of other enemies, nor did mutualists influence the effects of mutualists. However, these averages mask significant and large, but positive or negative, interactions in individual studies. In contrast, mutualists ameliorated the negative effects of enemies in a manner that benefited plants; this overall effect was driven by interactions between pathogens and belowground mutualists (bacteria and mycorrhizal fungi). The high frequency of significant interactive effects suggests a widespread potential for diffuse rather than pairwise coevolutionary interactions between plants and their enemies and mutualists. Pollinators and mycorrhizal fungi enhanced plant performance more than did bacterial mutualists. In the greenhouse (but not the field), pathogens reduced plant performance more than did herbivores, pathogens were more damaging to herbaceous than to woody plants, and herbivores were more damaging to crop than to non-crop plants (suggesting evolutionary change in plants or herbivores following crop domestication). We discuss how observed differences in effect size might be confounded with methodological differences among studies.