John N. Klironomos

Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity

The functioning and stability of terrestrial ecosystems are determined by plant biodiversity and species composition. However, the ecological mechanisms by which plant biodiversity and species composition are regulated and maintained are not well understood. These mechanisms need to be identified to ensure successful management for conservation and restoration of diverse natural ecosystems. Here we show, by using two independent, but complementary, ecological experiments, that below-ground diversity of arbuscular mycorrhizal fungi (AMF) is a major factor contributing to the maintenance of plant biodiversity and to ecosystem functioning. At low AMF diversity, the plant species composition and overall structure of microcosms that simulate European calcareous grassland fluctuate greatly when the AMF taxa that are present are changed. Plant biodiversity, nutrient capture and productivity in macrocosms that simulate North American old-fields increase significantly with increasing AMF-species richness. These results emphasize the need to protect AMF and to consider these fungi in future management practices in order to maintain diverse ecosystems. Our results also show that microbial interactions can drive ecosystem functions such as plant biodiversity, productivity and variability.

VARIATION IN PLANT RESPONSE TO NATIVE AND EXOTIC ARBUSCULAR MYCORRHIZAL FUNGI

High variability in plant-growth response to the presence of different mycorrhizal fungi can be a major determinant of local plant species diversity. Multiple species of arbuscular mycorrhizal fungi can coexist in terrestrial ecosystems, and co-occurring plants can differ in their response to colonization by these different fungi. However, the range of mycorrhizal plant-growth responses that can occur within communities has not been determined. In the present study, I crossed a large number of plant and fungal species that co-occur to determine the range of responses that can exist within an ecosystem. I also crossed exotic fungal isolates vs. local plant isolates and local fungal isolates vs. exotic plant isolates to determine whether the range of plant growth responses differs when using foreign genotypes. The data indicate that plant growth responses to mycorrhizal inoculation within an ecosystem can range from highly parasitic to highly mutualistic. In this study, the direction and magnitude of the response depended on the combination of plant and fungal species. No plant did best with the same fungal isolate. The range of responses was greatest when using local plants and fungi. Whereas parasitic and mutualistic responses were also detected when using foreign plant or fungal genotypes, the range of responses was significantly reduced, as was the relative frequency of positive responses. Overall, this study suggests that, within ecosystems, arbuscular mycorrhizal fungi can function along a continuum from parasitism to mutualism, and that extreme responses are more common when using locally adapted plants and fungi. This high variation in plant growth response may be a large contributor to plant species coexistence and the structure of plant communities.

Influence of Phylogeny on Fungal Community Assembly and Ecosystem Functioning

Ecology seeks to explain species coexistence and its functional consequences, but experimental tests of mechanisms that simultaneously account for both processes are difficult. We used an experimental mycorrhizal plant system to test whether functional similarity among closely related species (phylogenetic conservatism) can drive community assembly and ecosystem functioning. Communities were constructed with the same number of fungal species, but after 1 year of growth, realized species richness was highest where the starting species were more distantly related to each other. Communities with high realized species richness also stimulated plant productivity more than those with low realized species richness. Our findings suggest that phylogenetic trait conservatism can promote coexistence because of reduced competition between distinct evolutionary lineages and enhance ecosystem function because of functional complementarity among those same lineages.

Invasive Plant Suppresses the Growth of Native Tree Seedlings by Disrupting Belowground Mutualisms

The impact of exotic species on native organisms is widely acknowledged, but poorly understood. Very few studies have empirically investigated how invading plants may alter delicate ecological interactions among resident species in the invaded range. We present novel evidence that antifungal phytochemistry of the invasive plant, Alliaria petiolata, a European invader of North American forests, suppresses native plant growth by disrupting mutualistic associations between native canopy tree seedlings and belowground arbuscular mycorrhizal fungi. Our results elucidate an indirect mechanism by which invasive plants can impact native flora, and may help explain how this plant successfully invades relatively undisturbed forest habitat.

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.

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.

NOVEL WEAPONS: INVASIVE PLANT SUPPRESSES FUNGAL MUTUALISTS IN AMERICA BUT NOT IN ITS NATIVE EUROPE

Why some invasive plant species transmogrify from weak competitors at home to strong competitors abroad remains one of the most elusive questions in ecology. Some evidence suggests that disproportionately high densities of some invaders are due to the release of biochemicals that are novel, and therefore harmful, to naive organisms in their new range. So far, such evidence has been restricted to the direct phytotoxic effects of plants on other plants. Here we found that one of North Americas most aggressive invaders of undisturbed forest understories, Alliaria petiolata (garlic mustard) and a plant that inhibits mycorrhizal fungal mutualists of North American native plants, has far stronger inhibitory effects on mycorrhizas in invaded North American soils than on mycorrhizas in European soils where A. petiolata is native. This antifungal effect appears to be due to specific flavonoid fractions in A. petiolata extracts. Furthermore, we found that suppression of North American mycorrhizal fungi by A. petiolata corresponds with severe inhibition of North American plant species that rely on these fungi, whereas congeneric European plants are weakly affected. These results indicate that phytochemicals, benign to resistant mycorrhizal symbionts in the home range, may be lethal to naïve native mutualists in the introduced range and indirectly suppress the plants that rely on them.

Breaking New Ground: Soil Communities and Exotic Plant Invasion

Abstract As exotic plant species invade ecosystems, ecologists have been attempting to assess the effects of these invasions on native communities and to determine what factors influence invasion processes. Although much of this work has focused on aboveground flora and fauna, structurally and functionally diverse soil communities also can respond to and mediate exotic plant invasions. In numerous ecosystems, the invasion of exotic plant species has caused major shifts in the composition and function of soil communities. Soil organisms, such as pathogenic or mutualistic fungi, have direct effects on the establishment, growth, and biotic interactions of exotic plants. An integrated understanding of how aboveground and belowground biota interact with exotic plants is necessary to manage and restore communities invaded by exotic plant species.

Microbial ecology of biological invasions

Invasive microbes, plants and animals are a major threat to the composition and functioning of ecosystems; however, the mechanistic basis of why exotic species can be so abundant and disruptive is not well understood. Most studies have focused on invasive plants and animals, although few have considered the effects of invasive microbes, or interactions of invasive plant and animal species with microbial communities. Here, we review effects of invasive plants on soil microbial communities and discuss consequences for plant performance, plant community structure and ecosystem processes. In addition, we briefly discuss effects of invasive soil microbes on plant communities, which has been less well studied, and effects of invasive animals on soil decomposers and ecosystem functioning. We do this by considering each of three important functional groups of microbes, namely soil microbial parasites and pathogens, mutualistic symbionts and decomposers. We conclude that invasive plants, pathogenic and symbiotic soil microbes will have strongest effects on the abundance of individual species, community diversity and ecosystem functioning. Invasive decomposer microbes probably have little impact, because of limited specificity and great functional redundancy. However, invasive plants and animals can have major effects on microbial decomposition in soil. We propose that understanding, predicting and counteracting consequences of enhanced global homogenization of natural communities through introducing exotic plants, animals and microbes will require future studies on how pathogenic, symbiotic and decomposer soil microbes interact, how they are influenced by higher trophic level organisms and how their combined effects are influencing the composition and functioning of ecosystems.

Plant coexistence mediated by arbuscular mycorrhizal fungi

Recent research has indicated the importance of arbuscular mycorrhizal fungi (AMF) in mediating plant coexistence. Coarse-scale studies compare the effects of the presence versus absence of AMF on plant coexistence, a phenomenon that is most relevant in early successional ecosystems where AMF are patchily distributed. By contrast, fine-scale studies investigate interactions that might occur once AMF have developed more fully within ecosystems, and most plants come into contact with AMF. Whereas coarse-scale effects are well understood, our understanding of fine-scale factors is just developing, as a result of investigations into AMF‐ plant specificity, AMF species richness, shared mycelial networks, and plant‐AMF feedback effects. Further research into these areas will provide a better understanding of factors that mediate plant species co-existence and, ultimately, the maintenance of biodiversity within plant communities. The term ‘coexistence’ has been used by ecologists to describe a balanced mixture of species in a biotic community. Such coexistence is a biological riddle, because the tendency towards competitive exclusion should favour a monoculture. Theories attempting to explain plant coexistence have focused on either interactions among species, such as competitive balance [1–3], or the avoidance of interaction among species [4,5]. Non-interaction theories have traditionally examined the role of spatial segregation and disturbance in promoting or suppressing plant coexistence. Agent-mediated coexistence is a non-interaction theory proposed as a mechanism for maintaining multi-species assemblages in plant communities [6,7]. When the ‘agent’ is a pathogen or a predator, it can reduce the ability of a plant to compete for resources if the tissues affected are involved in resource gathering (root or leaf). Often, the effects of pathogens and predators can be density dependent, in that the most abundant host plant species loses more tissue than do less abundant plant species. As a result, less abundant plant species experience reduced competition, lessening their chance of competitive exclusion, and thus promoting species coexistence within plant communities.