skip to main content


Title: Global imprint of mycorrhizal fungi on whole-plant nutrient economics
Mycorrhizal fungi are critical members of the plant microbiome, forming a symbiosis with the roots of most plants on Earth. Most plant species partner with either arbuscular or ectomycorrhizal fungi, and these symbioses are thought to represent plant adaptations to fast and slow soil nutrient cycling rates. This generates a second hypothesis, that arbuscular and ectomycorrhizal plant species traits complement and reinforce these fungal strategies, resulting in nutrient acquisitive vs. conservative plant trait profiles. Here we analyzed 17,764 species level trait observations from 2,940 woody plant species to show that mycorrhizal plants differ systematically in nitrogen and phosphorus economic traits. Differences were clearest in temperate latitudes, where ectomycorrhizal plant species are more nitrogen use- and phosphorus use-conservative than arbuscular mycorrhizal species. This difference is reflected in both aboveground and belowground plant traits and is robust to controlling for evolutionary history, nitrogen fixation ability, deciduousness, latitude, and species climate niche. Furthermore, mycorrhizal effects are large and frequently similar to or greater in magnitude than the influence of plant nitrogen fixation ability or deciduous vs. evergreen leaf habit. Ectomycorrhizal plants are also more nitrogen conservative than arbuscular plants in boreal and tropical ecosystems, although differences in phosphorus use are less apparent outside temperate latitudes. Our findings bolster current theories of ecosystems rooted in mycorrhizal ecology and support the hypothesis that plant mycorrhizal association is linked to the evolution of plant nutrient economic strategies.  more » « less
Award ID(s):
1638575 1638577
NSF-PAR ID:
10130237
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
116
Issue:
46
ISSN:
0027-8424
Page Range / eLocation ID:
23163 to 23168
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The maintenance of tree diversity has been explained by multiple mechanisms. One of the most thoroughly studied is conspecific negative density dependence, in which specialist plant enemies reduce survivorship of seeds, seedlings or saplings located near adult conspecifics. Although there is much support that conspecific negative density dependence occurs in temperate forests, only a subset of the species investigated thus far exhibit this recruitment pattern. It remains unclear what drives differential susceptibility to conspecifics among tree species. Previous investigators have considered shade tolerance and mycorrhizal type (arbuscular mycorrhizal vs. ectomycorrhizal association) as two traits that might explain differential susceptibility to conspecific negative density dependence.

    Here, we test whether these two plant traits predict susceptibility of tree saplings to conspecific negative density dependence in a temperate hardwood forest using three responses: spatial point patterns of saplings, sapling growth and sapling survival.

    Spatial patterns of saplings indicate that shade tolerant species are less sensitive to conspecifics than shade intolerant species, but show no differences based on mycorrhizal type. Conversely, shade tolerant saplings exhibit reduced growth, but not survival, when located in areas with high conspecific density. We interpret this finding in light of the conservative functional strategies of shade tolerant species, which typically have low leaf nitrogen levels and slower growth to divert resources to tissue defence against enemies. We found an effect of mycorrhizal type interacting with adult conspecific density, where arbuscular mycorrhizal species show a greater reduction in growth than ectomycorrhizal species in areas dense with conspecifics.

    Synthesis. We conclude that the shade tolerance level and the mycorrhizal type of temperate forest saplings may influence how their growth and survival respond to the adult conspecific trees in their neighbourhoods.

     
    more » « less
  2. Summary

    Arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF) produce contrasting plant–soil feedbacks, but how these feedbacks are constrained by lithology is poorly understood.

    We investigated the hypothesis that lithological drivers of soil fertility filter plant resource economic strategies in ways that influence the relative fitness of trees with AMF or EMF symbioses in a Bornean rain forest containing species with both mycorrhizal strategies.

    Using forest inventory data on 1245 tree species, we found that although AMF‐hosting trees had greater relative dominance on all soil types, with declining lithological soil fertility EMF‐hosting trees became more dominant. Data on 13 leaf traits and wood density for a total of 150 species showed that variation was almost always associated with soil type, whereas for six leaf traits (structural properties; carbon, nitrogen, phosphorus ratios, nitrogen isotopes), variation was also associated with mycorrhizal strategy. EMF‐hosting species had slower leaf economics than AMF‐hosts, demonstrating the central role of mycorrhizal symbiosis in plant resource economies.

    At the global scale, climate has been shown to shape forest mycorrhizal composition, but here we show that in communities it depends on soil lithology, suggesting scale‐dependent abiotic factors influence feedbacks underlying the relative fitness of different mycorrhizal strategies.

     
    more » « less
  3. Abstract

    Soil fungi link above‐ and belowground carbon (C) fluxes through their interactions with plants and contribute to C and nutrient dynamics through the production, turnover, and activity of fungal hyphae. Despite their importance to ecosystem processes, estimates of hyphal production and turnover rates are relatively uncommon, especially in temperate hardwood forests. We sequentially harvested hyphal ingrowth bags to quantify the rates of Dikarya (Ascomycota and Basidiomycota) hyphal production and turnover in three hardwood forests in the Midwestern United States, where plots differed in their abundance of arbuscular (AM)‐ vs. ectomycorrhizal (ECM)‐associated trees. Hyphal production rates increased linearly with the percentage of ECM trees and annual production rates were 66% higher in ECM‐ than AM‐dominated plots. Hyphal turnover rates did not differ across the mycorrhizal gradient (plots varying in their abundance of AM vs. ECM trees), suggesting that the greater fungal biomass in ECM‐dominated plots relates to greater fungal production rather than slower fungal turnover. Differences in hyphal production across the gradient aligned with distinctly different fungal communities and activities. As ECM trees increased in dominance, fungi inside ingrowth bags produced more extracellular enzymes involved in degrading nitrogen (N)‐bearing relative to C‐bearing compounds, suggesting greater fungal (and possibly plant) N demand in ECM‐dominated soils. Collectively, our results demonstrate that shifts in temperate tree species composition that result in changes in the dominant type of mycorrhizal association may have strong impacts on Dikarya hyphal production, fungal community composition and extracellular enzyme activity, with important consequences for soil C and N cycling.

     
    more » « less
  4. Druzhinina, Irina S. (Ed.)
    ABSTRACT Trees associating with different mycorrhizas often differ in their effects on litter decomposition, nutrient cycling, soil organic matter (SOM) dynamics, and plant-soil interactions. For example, due to differences between arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) tree leaf and root traits, ECM-associated soil has lower rates of C and N cycling and lower N availability than AM-associated soil. These observations suggest that many groups of nonmycorrhizal fungi should be affected by the mycorrhizal associations of dominant trees through controls on nutrient availability. To test this overarching hypothesis, we explored the influence of predominant forest mycorrhizal type and mineral N availability on soil fungal communities using next-generation amplicon sequencing. Soils from four temperate hardwood forests in southern Indiana, United States, were studied; three forests formed a natural gradient of mycorrhizal dominance (100% AM tree basal area to 100% ECM basal area), while the fourth forest contained a factorial experiment testing long-term N addition in both dominant mycorrhizal types. We found that overall fungal diversity, as well as the diversity and relative abundance of plant pathogenic and saprotrophic fungi, increased with greater AM tree dominance. Additionally, tree community mycorrhizal associations explained more variation in fungal community composition than abiotic variables, including soil depth, SOM content, nitrification rate, and mineral N availability. Our findings suggest that tree mycorrhizal associations may be good predictors of the diversity, composition, and functional potential of soil fungal communities in temperate hardwood forests. These observations help explain differing biogeochemistry and community dynamics found in forest stands dominated by differing mycorrhizal types. IMPORTANCE Our work explores how differing mycorrhizal associations of temperate hardwood trees (i.e., arbuscular [AM] versus ectomycorrhizal [ECM] associations) affect soil fungal communities by altering the diversity and relative abundance of saprotrophic and plant-pathogenic fungi along natural gradients of mycorrhizal dominance. Because temperate hardwood forests are predicted to become more AM dominant with climate change, studies examining soil communities along mycorrhizal gradients are necessary to understand how these global changes may alter future soil fungal communities and their functional potential. Ours, along with other recent studies, identify possible global trends in the frequency of specific fungal functional groups responsible for nutrient cycling and plant-soil interactions as they relate to mycorrhizal associations. 
    more » « less
  5. Recent work suggests mycorrhizal fungi are important drivers of soil organic matter dynamics; however, whether this is a result of the fungi themselves or related traits of their host trees remains unclear. We evaluated how tree mycorrhizal associations and foliar chemistry influence mineral-associated organic matter (MAOM) and particulate organic matter (POM) in temperate forests of northern New England, USA. We measured carbon (C) and nitrogen (N) concentrations and C:N of three soil density fractions beneath six tree species that vary in both mycorrhizal association and foliar chemistry. We found a significant decline in the concentration of MAOM C and N with increasing foliar C:N in soil beneath tree species with arbuscular mycorrhizal (AM), but not ectomycorrhizal (ECM) fungi. The C:N of POM and MAOM was positively associated with the foliar C:N of the dominant tree species in a forest, and MAOM C:N was also higher beneath ECM- rather than AM-associated tree species. These results add to the growing body of support for mycorrhizal fungi as predictors of soil C and N dynamics, and suggest that C concentration in the MAOM fraction is more sensitive to organic matter chemistry beneath AM-associated tree species. Because MAOM decomposition is thought to be less responsive than POM decomposition to changes in soil temperature and moisture, differences in the tendency of AM- vs. ECM-dominated forests to support MAOM formation and persistence may lead to systematic differences in the response of these forest types to ongoing climate change. These data were gathered as part of the Hubbard Brook Ecosystem Study (HBES). The HBES is a collaborative effort at the Hubbard Brook Experimental Forest, which is operated and maintained by the USDA Forest Service, Northern Research Station. 
    more » « less