Plants and their arbuscular mycorrhizal fungal symbionts interact in complex underground networks involving multiple partners. This increases the potential for exploitation and defection by individuals, raising the question of how partners maintain a fair, two-way transfer of resources. We manipulated cooperation in plants and fungal partners to show that plants can detect, discriminate, and reward the best fungal partners with more carbohydrates. In turn, their fungal partners enforce cooperation by increasing nutrient transfer only to those roots providing more carbohydrates. On the basis of these observations we conclude that, unlike many other mutualisms, the symbiont cannot be "enslaved." Rather, the mutualism is evolutionarily stable because control is bidirectional, and partners offering the best rate of exchange are rewarded.
Feedback with soil biota is an important determinant of terrestrial plant diversity. However, the factors regulating plant-soil feedback, which varies from positive to negative among plant species, remain uncertain. In a large-scale study involving 55 species and 550 populations of North American trees, the type of mycorrhizal association explained much of the variation in plant-soil feedbacks. In soil collected beneath conspecifics, arbuscular mycorrhizal trees experienced negative feedback, whereas ectomycorrhizal trees displayed positive feedback. Additionally, arbuscular mycorrhizal trees exhibited strong conspecific inhibition at multiple spatial scales, whereas ectomycorrhizal trees exhibited conspecific facilitation locally and less severe conspecific inhibition regionally. These results suggest that mycorrhizal type, through effects on plant-soil feedbacks, could be an important contributor to population regulation and community structure in temperate forests.
Summary• Arbuscular mycorrhizal fungi (AMF) are important components of terrestrial communities but the basic ecology of individual AMF, including their colonization strategy, remains unclear. The colonizing behaviours of 21 AMF isolates from three families (Acaulosporaceae, Gigasporaceae and Glomaceae) were compared to test for a relationship between AMF taxonomy and colonization strategy.• Both the rate and extent of colonization were considered by measuring percentage root colonization, root fungal biomass, soil hyphal length and soil fungal biomass over 12 wk.• Most Glomaceae isolates colonized roots before Acaulosporaceae and Gigasporaceae isolates. The fastest colonizers were also often the most extensive. Taxonomic differences were apparent in the amount and proportion of fungal biomass found in roots vs in soil. Glomaceae isolates had high root colonization but low soil colonization, Gigasporaceae isolates showed the opposite trend whereas Acaulosporaceae isolates had low root and soil colonization. These results were similar for four different host plants.• The results indicate that the colonizing strategies of AM fungi differ considerably and that this variation is taxonomically based at the family level. Arbuscular mycorrhizal fungal taxonomy therefore has a functional basis.
Ecological theory predicts a positive and asymptotic relationship between plant diversity and ecosystem productivity based on the ability of more diverse plant communities to use limiting resources more fully. This is supported by recent empirical evidence. Additionally, in natural ecosystems, plant productivity is often a function of the presence and composition of mycorrhizal associations. Yet, the effect of mycorrhizal fungi on the relationship between plant diversity and productivity has not been investigated. We predict that in the presence of AMF, productivity will saturate at lower levels of species richness because AMF increase the ability of plant species to utilize nutrient resources. In this study we manipulated old‐field plant species richness in the presence and absence of two species of AMF. We found that in the absence of AMF, the relationship between plant species richness and productivity is positive and linear. However, in the presence of AMF, the relationship is positive but asymptotic, even though the maximum plant biomass was significantly different between the two AMF treatments. This is consistent with the hypothesis that AMF increase the redundancy of plant species in the productivity of plant communities, and indicates that these symbionts must be considered in future investigations of plant biodiversity and ecosystem function.
The diversity of functional and life-history traits of organisms depends on adaptation as well as the legacy of shared ancestry. Although the evolution of traits in macro-organisms is well studied, relatively little is known about character evolution in micro-organisms. Here, we surveyed an ancient and ecologically important group of microbial plant symbionts, the arbuscular mycorrhizal (AM) fungi, and tested hypotheses about the evolution of functional and life-history traits. Variation in the extent of root and soil colonization by AM fungi is constrained to a few nodes basal to the most diverse groups within the phylum, with relatively little variation associated with recent divergences. We found no evidence for a trade-off in biomass allocated to root versus soil colonization in three published glasshouse experiments; rather these traits were positively correlated. Partial support was observed for correlated evolution between fungal colonization strategies and functional benefits of the symbiosis to host plants. The evolution of increased soil colonization was positively correlated with total plant biomass and shoot phosphorus content. Although the effect of AM fungi on infection by root pathogens was phylogenetically conserved, there was no evidence for correlated evolution between the extent of AM fungal root colonization and pathogen infection. Variability in colonization strategies evolved early in the diversification of AM fungi, and we propose that these strategies were influenced by functional interactions with host plants, resulting in an evolutionary stasis resembling trait conservatism.
Plants interact simultaneously with each other and with soil biota, yet the relative importance of competition vs. plant-soil feedback (PSF) on plant performance is poorly understood. Using a meta-analysis of 38 published studies and 150 plant species, we show that effects of interspecific competition (either growing plants with a competitor or singly, or comparing inter- vs. intraspecific competition) and PSF (comparing home vs. away soil, live vs. sterile soil, or control vs. fungicide-treated soil) depended on treatments but were predominantly negative, broadly comparable in magnitude, and additive or synergistic. Stronger competitors experienced more negative PSF than weaker competitors when controlling for density (inter- to intraspecific competition), suggesting that PSF could prevent competitive dominance and promote coexistence. When competition was measured against plants growing singly, the strength of competition overwhelmed PSF, indicating that the relative importance of PSF may depend not only on neighbour identity but also density. We evaluate how competition and PSFs might interact across resource gradients; PSF will likely strengthen competitive interactions in high resource environments and enhance facilitative interactions in low-resource environments. Finally, we provide a framework for filling key knowledge gaps and advancing our understanding of how these biotic interactions influence community structure.
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