One mechanism proposed to explain high species diversity in tropical systems is strong negative conspecific density dependence (CDD), which reduces recruitment of juveniles in proximity to conspecific adult plants. Although evidence shows that plant-specific soil pathogens can drive negative CDD, trees also form key mutualisms with mycorrhizal fungi, which may counteract these effects. Across 43 large-scale forest plots worldwide, we tested whether ectomycorrhizal tree species exhibit weaker negative CDD than arbuscular mycorrhizal tree species. We further tested for conmycorrhizal density dependence (CMDD) to test for benefit from shared mutualists. We found that the strength of CDD varies systematically with mycorrhizal type, with ectomycorrhizal tree species exhibiting higher sapling densities with increasing adult densities than arbuscular mycorrhizal tree species. Moreover, we found evidence of positive CMDD for tree species of both mycorrhizal types. Collectively, these findings indicate that mycorrhizal interactions likely play a foundational role in global forest diversity patterns and structure.
Soil microbes impact plant community structure and diversity through plant–soil feedbacks. However, linking the relative abundance of plant pathogens and mutualists to differential plant recruitment remains challenging. Here, we tested for microbial mediation of pairwise feedback using a reciprocal transplant experiment in a lowland tropical forest in Panama paired with amplicon sequencing of soil and roots. We found evidence that plant species identity alters the microbial community, and these changes in microbial composition alter subsequent growth and survival of conspecific plants. We also found that greater community dissimilarity between species in their arbuscular mycorrhizal and nonpathogenic fungi predicted increased positive feedback. Finally, we identified specific microbial taxa across our target functional groups that differentially accumulated under conspecific settings. Collectively, these findings clarify how soil pathogens and mutualists mediate net feedback effects on plant recruitment, with implications for management and restoration.
more » « less- Award ID(s):
- 1738041
- NSF-PAR ID:
- 10473989
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology
- Volume:
- 105
- Issue:
- 1
- ISSN:
- 0012-9658
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
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Abstract Plant–soil feedbacks (PSFs) drive plant community diversity via interactions between plants and soil microbes. However, we know little about how frequently PSFs affect plants at the seed stage, and the compositional shifts in fungi that accompany PSFs on germination.
We conducted a pairwise PSF experiment to test whether seed germination was differentially impacted by conspecific versus heterospecific soils for seven grassland species. We used metagenomics to characterize shifts in fungal community composition in soils conditioned by each plant species. To investigate whether changes in the abundance of certain fungal taxa were associated with multiple PSFs, we assigned taxonomy to soil fungi and identified putative pathogens that were significantly more abundant in soils conditioned by plant species that experienced negative or positive PSFs.
We observed negative, positive, and neutral PSFs on seed germination. Although conspecific and heterospecific soils for pairs with significant PSFs contained host‐specialized soil fungal communities, soils with specialized microbial communities did not always lead to PSFs. The identity of host‐specialized pathogens, that is, taxa uniquely present or significantly more abundant in soils conditioned by plant species experiencing negative PSFs, overlapped among plant species, while putative pathogens within a single host plant species differed depending on the identity of the heterospecific plant partner. Finally, the magnitude of feedback on germination was not related to the degree of fungal community differentiation between species pairs involved in negative PSFs.
Synthesis . Our findings reveal the potential importance of PSFs at the seed stage. Although plant species developed specialized fungal communities in rhizosphere soil, pathogens were not strictly host‐specific and varied not just between plant species, but according to the identity of plant partner. These results illustrate the complexity of microbe‐mediated interactions between plants at different life stages that next‐generation sequencing can begin to unravel. -
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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. -
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Abstract While microorganisms are recognized for driving belowground processes that influence the productivity and fitness of plant populations, the vast majority of bacteria and fungi in soil belong to a seed bank consisting of dormant individuals. However, plant performance may be affected by microbial dormancy through its effects on the activity, abundance, and diversity of soil microorganisms. To test how microbial seed banks influence plant‐soil interactions, we purified recombinant resuscitation promoting factor (Rpf), a bacterial protein that terminates dormancy. In a factorially designed experiment, we then applied the Rpf to soil containing field mustard (
Brassica rapa ), an agronomically important plant species. Plant biomass was ~33% lower in the Rpf treatment compared to plants grown with an unmanipulated microbial seed bank. In addition, Rpf reduced soil respiration, decreased bacterial abundance, and increased fungal abundance. These effects of Rpf on plant performance were accompanied by shifts in bacterial community composition, which may have diluted mutualists or resuscitated pathogens. Our findings suggest that changes in microbial seed banks may influence the magnitude and direction of plant‐soil feedbacks in ways that affect above‐ and belowground biodiversity and function. -
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Abstract Seedling recruitment can be strongly affected by the composition of nearby plant species. At the neighborhood scale (on the order of tens of meters), adult conspecifics can modify soil chemistry and the presence of host microbes (pathogens and mutualists) across their combined canopy area or rooting zones. At local or small spatial scales (on the order of one to few meters), conspecific seed or seedling density can influence the strength of intraspecific light and resource competition and also modify the density‐dependent spread of natural enemies such as pathogens or invertebrate predators. Intrinsic correlation between proximity to adult conspecifics (i.e., recruitment neighborhood) and local seedling density, arising from dispersal, makes it difficult to separate the independent and interactive factors that contribute to recruitment success. Here, we present a field experiment in which we manipulated both the recruitment neighborhood and seedling density to explore how they interact to influence the growth and survival of
Dryobalanops aromatica , a dominant ectomycorrhizal tree species in a Bornean tropical rainforest. First, we found that both local seedling density and recruitment neighborhood had effects on performance ofD .aromatica seedlings, though the nature of these impacts varied between growth and survival. Second, we did not find strong evidence that the effect of density on seedling survival is dependent on the presence of conspecific adult trees. However, accumulation of mutualistic fungi beneath conspecifics adults does facilitate establishment ofD .aromatica seedlings. In total, our results suggest that recruitment near adult conspecifics was not associated with a performance cost and may have weakly benefitted recruiting seedlings. Positive effects of conspecifics may be a factor facilitating the regional hyperabundance of this species. Synthesis: Our results provide support for the idea that dominant species in diverse forests may escape the localized recruitment suppression that limits abundance in rarer species.
