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"Bever, James D."
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The missing link in grassland restoration: arbuscular mycorrhizal fungi inoculation increases plant diversity and accelerates succession
by
Koziol, Liz
,
Nuñez, Martin
,
Bever, James D.
in
Abundance
,
anthropogenic activities
,
Anthropogenic factors
2017
Summary Because soil microbial communities are often altered by anthropogenic disturbance, successful plant community restoration may require the restoration of beneficial soil microbes, such as arbuscular mycorrhizal (AM) fungi. Recent evidence suggests that later successional grassland species are more strongly affected by AM fungi relative to early successional plants and that late successional plants consistently benefit from some AM fungi but not other AM fungal species. Many of these late successional species are also often missing in restorations despite being heavily seeded. To assess the effects of AM fungal composition within grassland restorations, we inoculated plots with six different AM fungal community treatments including one of four different AM fungal species isolated from a prairie, a mixture of all four fungal species, and a non‐inoculated control. AM fungi were introduced by planting 16 different inoculated nurse plants into replicated plots. We also seeded the restoration with a diverse, 54 species prairie seed mixture. We found that AM fungal inoculation drove plant community composition; plots inoculated with certain AM fungal treatments were dominated by desirable prairie plants, whereas plots inoculated with other AM fungal species and the non‐inoculated control were dominated by non‐desirable plants including weeds and exotic species. Specifically, we found that many early successional species established well regardless of AM fungal inoculation, whereas the establishment and growth of many late successional species was strongly dependent on the presence of specific AM fungal species. Many conservative late successional species did not occur without inoculation. Overall, total plant community richness, diversity, and Floristic Quality Index were all significantly improved with AM fungal inoculation, whereas we observed that non‐desirable plant abundance was significantly greater in the non‐inoculated plots. Synthesis and applications. Our results suggest that the lack of late successional establishment reported in many previous restorations may be due to ineffective arbuscular mycorrhizal fungal communities at these sites. We conclude that the reintroduction of arbuscular mycorrhizal fungi from reference prairie environments could improve restoration outcomes by promoting plant diversity and richness, especially for desirable later successional plant species, while simultaneously inhibiting less desirable weedy plants. Our results suggest that the lack of late successional establishment reported in many previous restorations may be due to ineffective arbuscular mycorrhizal fungal communities at these sites. We conclude that the reintroduction of arbuscular mycorrhizal fungi from reference prairie environments could improve restoration outcomes by promoting plant diversity and richness, especially for desirable later successional plant species, while simultaneously inhibiting less desirable weedy plants.
Journal Article
Maintenance of Plant Species Diversity by Pathogens
by
Alexander, Helen M.
,
Mangan, Scott A.
,
Bever, James D.
in
Biodiversity
,
Coexistence
,
Ecological succession
2015
We present strong evidence that pathogens play a critical role in structuring plant communities and maintaining plant diversity. Pathogens mediate plant species coexistence through trade-offs between competitive ability and resistance to pathogens and through pathogen specialization. Experimental tests of individual plant-pathogen interactions, tests of feedback through host-specific changes in soil communities, and field patterns and field experimentation consistently identify pathogens as important to plant species coexistence. These direct tests are supported by observations of the role of pathogens in generating the productivity gains from manipulations of plant diversity and by evidence that escape from native pathogens contributes to success of introduced plant species. Further work is necessary to test the role of pathogen dynamics in large-scale patterns of plant diversity and range limits, the robustness of coexistence to coevolutionary dynamics, the contribution of different pathogens, and the role of pathogens in plant succession.
Journal Article
Preferential allocation, physio‐evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts
2015
The common occurrence of mutualistic interactions between plants and root symbionts is problematic. As the delivery of benefit to hosts involves costs to symbionts, symbionts that provide reduced benefit to their host are expected to increase in frequency. Plants have been shown to allocate preferentially to the most efficient symbiont and this preferential allocation may stabilize the mutualism. I construct a general model of the interactive feedbacks of host preferential allocation and the dynamics of root symbiont populations to evaluate the stability of nutritional mutualisms. Preferential allocation can promote the evolution of mutualism even when the cost to the symbiont is very large. Moreover, the physiological plasticity of preferential allocation likely leads to coexistence of beneficial and nonbeneficial symbionts. For arbuscular mycorrhizal fungi, which facilitate plant uptake of phosphorus (P), the model predicts greater P transfer from these fungi per unit carbon invested with decreasing concentrations of soil P and with increasing concentrations of atmospheric CO₂, patterns that have been observed in laboratory and field studies. This framework connects physiological plasticity in plant allocation to population processes that determine mutualism stability and, as such, represents a significant step in understanding the stability and environmental patterns in mutualism.
Journal Article
Mycorrhizal feedbacks generate positive frequency dependence accelerating grassland succession
by
Koziol, Liz
,
Bever, James D.
in
Abundance
,
arbuscular mycorrhizal fungi
,
Arbuscular mycorrhizas
2019
1. Plant mutualists including arbuscular mycorrhizal (AM) fungi have been postulated as being important drivers of plant community diversity and succession. Late successional plants have been shown to be more responsive to AM fungi and more sensitive to AM fungal species identity, which could generate positive feedback and potentially accelerate succession. 2. We test the effect of AM fungi on plant diversity and on frequency dependence predicted by positive plant-AM fungi feedback across a successional gradient. We created prairie mesocosms comprised of a majority of early successional, equal abundance, and a majority of late successional plant species. We inoculated these mesocosms and a field restoration experiment with 14 different communities of AM fungi from late successional prairies that varied in levels of species richness. 3. Overall, we found that AM fungi increased plant diversity and this was driven by the response of late successional plant species to mycorrhizae. Our results indicate that AM fungal composition is more important than AM fungal diversity per se. We found that the effect of inoculation with a single species or groups of AM fungi depended on whether those fungi benefited late successional plant species. Early successional plants consistently exhibited negative frequency-dependent growth regardless of fungal composition, while late successional plants demonstrated positive frequency-dependent growth in our mesocosms—but only in the presence of beneficial AM fungal species. These results are consistent with positive plant-mycorrhizal feedbacks accelerating plant community successional trajectories once late successional plants establish. Mesocosm results were mirrored with field inoculation assays where we found that beneficial AM fungi facilitated late successional plant establishment. 4. Synthesis. Our results provide support for beneficial arbuscular mycorrhizal fungi being a primary mechanism for positive plant-soil feedback driving plant community succession, as late successional seedlings grew faster and larger when their neighbours were also late successional plant species when they were associated with beneficial arbuscular mycorrhizal fungi. We found that this positive feedback thereby accelerated succession in mesocosms and in the field.
Journal Article
Mycorrhizal response trades off with plant growth rate and increases with plant successional status
2015
Earlyâsuccessional plant species invest in rapid growth and reproduction in contrast to slow growing lateâsuccessional species. We test the consistency of tradeâoffs between plant life history and responsiveness on arbuscular mycorrhizal fungi. We selected four very earlyâ, seven earlyâ, 11 middleâ, and eight lateâsuccessional plant species from six different families and functional groups and grew them with and without a mixed fungal inoculum and compared root architecture, mycorrhizal responsiveness, and plant growth rate. Our results indicate mycorrhizal responsiveness increases with plant successional stage and that this effect explains more variation in mycorrhizal response than is explained by phylogenetic relatedness. The mycorrhizal responsiveness of individual plant species was positively correlated with mycorrhizal root infection and negatively correlated with average plant mass and the number of root tips per unit mass, indicating that both plant growth rate and root architecture trade off with investment in mycorrhizal mutualisms. Because lateâsuccessional plants are very responsive to mycorrhizal fungi, our results suggest that fungal community dynamics may be an important driver of plant succession.
Journal Article
Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume
by
Larimer, Anna L.
,
Clay, Keith
,
Bever, James D.
in
Amorpha canescens
,
arbuscular mycorrhizal fungi
,
Bacteria
2014
Biotic interactions play primary roles in major theories of the distribution and abundance of species, yet the nature of these biotic interactions can depend upon the larger ecological community. Leguminous plants, for example, commonly associate with both arbuscular mycorrhizal fungi (AMF) and rhizobia bacteria, and the pairwise interactions may depend upon the presence or identity of the third partner. To determine if the dynamics of plantâAMF and plantârhizobia interactions are affected by the alternate symbiont, we manipulated the presence and identity of each symbiont, as well as levels of the nutrients supplied by each symbiont (nitrogen and phosphorus), on the growth of prairie legume Amorpha canescens. We found strong synergistic effects of AMF and rhizobia inoculation on plant biomass production that were independent of nutrient levels. AMF and rhizobia responses were each influenced by the other, but not in the same direction. AMF infection increased root nodule number and mass, but rhizobia inoculation decreased AMF hyphal colonization of roots. The relative benefits of each combination of symbionts depended upon phosphorus level. The effect of nitrogen was also contingent on the biotic environment where nitrogen addition decreased nodulation, but this decrease was reduced with coinfection by AMF. Our results demonstrate a strong contingency on the coâoccurrence of AMF and rhizobia for the longâterm fitness of A. canescens, and suggest that the belowground community is critical for the success of this species in tallgrass prairies.
Journal Article
Dilution of specialist pathogens drives productivity benefits from diversity in plant mixtures
2023
Productivity benefits from diversity can arise when compatible pathogen hosts are buffered by unrelated neighbors, diluting pathogen impacts. However, the generality of pathogen dilution has been controversial and rarely tested within biodiversity manipulations. Here, we test whether soil pathogen dilution generates diversity- productivity relationships using a field biodiversity-manipulation experiment, greenhouse assays, and feedback modeling. We find that the accumulation of specialist pathogens in monocultures decreases host plant yields and that pathogen dilution predicts plant productivity gains derived from diversity. Pathogen specialization predicts the strength of the negative feedback between plant species in greenhouse assays. These feedbacks significantly predict the overyielding measured in the field the following year. This relationship strengthens when accounting for the expected dilution of pathogens in mixtures. Using a feedback model, we corroborate that pathogen dilution drives overyielding. Combined empirical and theoretical evidence indicate that specialist pathogen dilution generates overyielding and suggests that the risk of losing productivity benefits from diversity may be highest where environmental change decouples plant-microbe interactions.
Soil pathogen dilution can improve plant production. Here, the authors combine an empirical and theoretical approaches finding that specialist pathogens suppress yield in monocultures while pathogen dilution drives yield benefits in diverse plant communities.
Journal Article
The Plant Microbiome and Native Plant Restoration
by
SCHULTZ, PEGGY A.
,
BAUER, JONATHAN T.
,
BEVER, JAMES D.
in
anthropogenic activities
,
Anthropogenic factors
,
Arbuscular mycorrhizas
2018
Ecological restoration efforts can increase the diversity and function of degraded areas. However, current restoration practices cannot typically reestablish the full diversity and species composition of remnant plant communities. We present evidence that restoration quality can be improved by reintroducing key organisms from the native plant microbiome. In particular, root symbionts called arbuscular mycorrhizal fungi are crucial in shaping grassland communities, but are sensitive to anthropogenic disturbance, which may pose a problem for grassland restoration. In the present article, we highlight the conceptual motivation and empirical evidence evaluating native mycorrhizal fungi, as opposed to commercial fungi. Reintroduction of the native microbiome and native mycorrhizal fungi improves plant diversity, accelerates succession, and increases the establishment of plants that are often missing from restored communities. The example of mycorrhizal fungi serves to illustrate the value of a more holistic view of plant communities and restoration that embraces the intricacies and dynamics of native microbial communities.
Journal Article
Biogeography of arbuscular mycorrhizal fungi (Glomeromycota): a phylogenetic perspective on species distribution patterns
by
Stürmer, Sidney L
,
Bever, James D
,
Morton, Joseph B
in
Arbuscular mycorrhizas
,
Biogeography
,
Climatic zones
2018
Information on the biogeography of arbuscular mycorrhizal fungi (AMF) is important because this group of obligately symbiotic soil microbes is a ubiquitous and functionally critical component of terrestrial ecosystems. In this paper, we utilize a biogeography database summarizing data on AMF species distribution linked to geographic and environmental conditions to describe global distribution patterns and interpret these patterns within a phylogenetic perspective. The data were obtained from accessions in living culture collections (INVAM, CICG), species descriptions, and other published literature from 1960 to 2012. The database contains 7105 records, 6396 of them from 768 published papers and the remaining 709 from culture accessions. Glomeromycotan species were recorded in all seven continents, 87 countries, 11 biogeographical realms, and 14 biomes. The distribution of families differed among climatic zones and continents, but they, together with all genera, appear to be cosmopolitan. Distribution of AMF species shows a slight decrease from low to high latitudes, but this decrease is steeper in the southern than in the northern hemisphere. A total of 189 species is shared between ancient supercontinents Gondwana and Laurasia and 78 species are common to all climatic zones. Ninety-five species (43% of the total) have known cosmopolitan distribution, including members of all genera except Redeckera. Some species have disjunct distribution and 26% of species have been registered from only one continent. Data on AMF distribution challenge the “Everything is everywhere” hypothesis in favor of the “moderate endemicity model” for species distribution. Data from this study provide a foundation to formulate and test hypotheses of biogeographic patterns and processes in Glomeromycota.
Journal Article
Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function
by
Tanya E. Cheeke
,
Edward R. Brzostek
,
James D. Bever
in
arbuscular mycorrhizal (AM) fungi
,
Bacteria - metabolism
,
biogeochemical cycles
2017
While it is well established that plants associating with arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) fungi cycle carbon (C) and nutrients in distinct ways, we have a limited understanding of whether varying abundance of ECM and AM plants in a stand can provide integrative proxies for key biogeochemical processes.
We explored linkages between the relative abundance of AM and ECM trees and microbial functioning in three hardwood forests in southern Indiana, USA. Across each site’s ‘mycorrhizal gradient’, we measured fungal biomass, fungal: bacterial (F: B) ratios, extracellular enzyme activities, soil carbon: nitrogen ratio, and soil pH over a growing season.
We show that the percentage of AM or ECM trees in a plot promotes microbial communities that both reflect and determine the C to nutrient balance in soil. Soils dominated by ECM trees had higher F: B ratios and more standing fungal biomass than AM stands. Enzyme stoichiometry in ECM soils shifted to higher investment in extracellular enzymes needed for nitrogen and phosphorus acquisition than in C-acquisition enzymes, relative to AM soils.
Our results suggest that knowledge of mycorrhizal dominance at the stand or landscape scale may provide a unifying framework for linking plant and microbial community dynamics, and predicting their effects on ecological function.
Journal Article