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Peay KG, Schubert MG, Nguyen NH, Bruns TD.. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21: 4122-4136

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Abstract

Dispersal plays a prominent role in most conceptual models of community assembly. However, direct measurement of dispersal across a whole community is difficult at ecologically relevant spatial scales. For cryptic organisms, such as fungi and bacteria, the scale and importance of dispersal limitation has become a major point of debate. We use an experimental island biogeographic approach to measure the effects of dispersal limitation on the ecological dynamics of an important group of plant symbionts, ectomycorrhizal fungi. We manipulated the isolation of uncolonized host seedlings across a natural landscape and used a range of molecular techniques to measure the dispersal rates of ectomycorrhizal propagules and host colonization. Some species were prolific dispersers, producing annual spore loads on the order of trillions of spores per km(2). However, fungal propagules reaching host seedlings decreased rapidly with increasing distance from potential spore sources, causing a concomitant reduction in ectomycorrhizal species richness, host colonization and host biomass. There were also strong differences in dispersal ability across species, which correlated well with the predictable composition of ectomycorrhizal communities associated with establishing pine forest. The use of molecular tools to measure whole community dispersal provides a direct confirmation for a key mechanism underlying island biogeography theory and has the potential to make microbial systems a model for understanding the role of dispersal in ecological theory.

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... In settings in which patches of high-severity fire are homogeneous and large, plant (Tomback et al. 1990, Turner et al. 2003, Pansing et al. 2020) and fungal (Peay et al. 2012) species from the regional pool that are adapted to longdistance dispersal may gain advantage. Propagules may also disperse from sources within burned patches, according to a few general mechanisms. ...
... Fungi and obligate seeder plants recovering far in the interior of burned patches are likely to do so more slowly than those established near burn perimeters as burn patch size increases (table 1). Even long-distance-dispersing ectomycorrhizal fungi are unlikely to disperse farther than ten kilometers (Peay et al. 2012). ...
... In addition, certain plant and fungal taxa produce more propagules, disperse farther or colonize at a higher rate than others (Tomback et al. 1990, Vander Wall and Longland 2004, Peay et al. 2012. Therefore, increased fire frequency and increased size of patches of high severity may confer relative advantages to taxa with rapid reproductive maturity (e.g., Picea mariana) or long distance propagule dispersal (e.g., Pteridium aquilinum, Suillus pungens). ...
Article
Many forest species are adapted to long-interval, high-severity fires, but the intervals between severe fires are decreasing with changes in climate, land use, and biological invasions. Although the effects of changing fire regimes on some important recovery processes have previously been considered, the consequences for the dispersal of propagules (plant seeds and fungal spores) in forest communities have not. We characterize three mechanisms by which changing fire regimes disrupt propagule dispersal in mesic temperate, boreal, and high-elevation forests: reduced abundance and altered spatial distributions of propagule source populations, less effective dispersal of propagules by wind, and altered behavior of animal dispersers and propagule predators. We consider how disruptions to propagule dispersal may interact with other factors that are also influenced by fire regime change, potentially increasing risk of forest conversion. Finally, we highlight urgent research topics regarding how dispersal limitation may shape twenty-first century forest recovery after stand-replacing fire.
... Here, we addressed this question by using a spatial gradient consisting of seventeen field sites at Point Reyes National Seashore in California, United States to determine how fungal community assembly affects wood decomposition across scales ( Figure S1). The sites range in their proximity to coastal pine forests from immediately adjacent to approximately 5.5 km away, and prior research has shown that dispersal limitation of spores sourced from forests is a primary driver of fungal community assembly across the gradient (Peay & Bruns, 2014;Peay et al., 2012;Smith et al., 2018). We allowed pine wood blocks to decompose in the field for a year at each study site, pairing each replicate with an equivalent wood decay microcosm incubated in the laboratory for the same duration. ...
... Animal exclusion cages were built out of chicken wire as by Peay et al. (2012) at 17 sites ranging in distance from P. muricata forests from directly adjacent (0.25 m) to approximately 5.5 km ( Figure S1). Sixteen of these sites have appeared in other work (Peay & Bruns, 2014;Peay et al., 2012;Smith et al., 2018); one was repositioned closer to the forest edge relative to prior studies. ...
... Animal exclusion cages were built out of chicken wire as by Peay et al. (2012) at 17 sites ranging in distance from P. muricata forests from directly adjacent (0.25 m) to approximately 5.5 km ( Figure S1). Sixteen of these sites have appeared in other work (Peay & Bruns, 2014;Peay et al., 2012;Smith et al., 2018); one was repositioned closer to the forest edge relative to prior studies. While immediately adjacent sites are likely to be influenced both biotically and abiotically by forest, all other sites are located in coastal scrub. ...
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Decomposition has historically been considered a function of climate and substrate but new research highlights the significant role of specific micro‐organisms and their interactions. In particular, wood decay is better predicted by variation in fungal communities than in climate. Multiple links exist: interspecific competition slows decomposition in more diverse fungal communities, whereas trait variation between different communities also affects process rates. Here, we paired field and laboratory experiments using a dispersal gradient at a forest‐shrubland ecotone to examine how fungi affect wood decomposition across scales. We observed that while fungal communities closer to forests were capable of faster decomposition, wood containing diverse fungal communities decomposed more slowly, independent of location. Dispersal‐driven stochasticity in small‐scale community assembly was nested within large‐scale turnover in the regional species pool, decoupling the two patterns. We thus find multiple distinct links between microbes and ecosystem function that manifest across different spatial scales. Wood decay is better predicted by variation in fungal communities than climate, but multiple links exist: interspecific competition slows decomposition in diverse communities and variation in traits also constrains process rates. We paired field and laboratory experiments using a forest‐shrubland ecotone and discovered that while fungal communities closer to forests were capable of faster decomposition, wood containing diverse fungal communities decomposed more slowly. Stochastic small‐scale community assembly is nested within large‐scale turnover in the regional species pool, decoupling the trends and creating multiple significant links between fungi and decomposition varying not just quantitatively but qualitatively with scale.
... For instance, in ectomycorrhizal fungi, production is estimated at billions to trillions of spores (i.e. tiny propagules) per km 2 (Peay et al. 2012). Despite limited knowledge of the dispersal • Connectivity affects passive dispersal through the effect of connectivity on dispersal vectors • Active dispersal might be affected by connectivity but at a short spatial scale owing to the short dispersal distance ...
... • Define what we consider hotpots for microorganisms • Establish connectivity at multiple spatial scales to account for the range of scales of microorganism response to habitat fragmentation • Test the microbial rescue effect due to corridor implementation • Consider host and its microbiota as a single entity for corridor implementation of microorganisms, it appears that the production of so many propagules is offset by the fact that the vast majority of spores fall close to their emission source (Galante et al. 2011) and by the very low probability of achieving viable germination (Peay et al. 2012). Lastly, microorganisms usually have a short generation time ranging from minutes to at the most, a few days. ...
... Response patterns to connectivity have been reported to be mixed. Positive effects of connectivity have been found for the transport of microorganisms in hydrological networks (Lindström and Bergström 2005) and on richness in ectomycorrhizal fungi (Peay et al. 2012). Increased similarity in fungal species composition in tree roots was found in connected patches compared to disconnected patches in a lava-fragmented landscape (Vannette et al. 2016). ...
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Because of land use changes, a worldwide decrease in biodiversity is underway, mostly driven by habitat degradation and fragmentation. Increasing landscape connectivity (i.e. the degree to which the landscape facilitates movement between habitat patches) has been proposed as a key landscape‐level strategy to counterbalance the negative effects of habitat fragmentation. A robust theoretical and methodological framework has been developed for the concept of connectivity, and an increasing body of empirical evidence supports the relevance of connectivity for biodiversity. However, the framework was built ignoring species that represent the dominant proportion of biodiversity on earth: microorganisms. The extent to which the existing conceptual and methodological frameworks on connectivity can be applied to microorganisms remain unknown. We reviewed existing evidence and analyzed methods to test the influence of connectivity on microorganisms. We included all types of microorganisms, from symbiotic to pathogenic and free‐living microorganisms, across all ecosystems. We describe the effect of connectivity on microorganism populations and communities, and identify the limitations and large gaps in current knowledge. Microorganisms can differ from macroorganisms in their response to connectivity due to short (distance less than a meter) dispersal distance of some groups, longer time lag of microorganisms response (possibly accompanied by evolutionary processes) and host association. The latter relies on tight interactions and feedback effects that drive microbial‐landscape relationships and lead to possible coadaptation processes. Incorporating the connectivity concept in microbial community assembly rules to preserve the diversity of microbial communities and the ecosystem services they provide could be a crucial step forward in the face of pressing global changes.
... If plant-to-plant transfer is identified as the primary source of foliar fungi, it may still reflect either local or regional source-sink networks. Tracking fungal movement across all relevant scales is challenging, but limited direct measurements of aerial dispersal suggest that local fungal communities are the result of a combination of shortand long-distance dispersal [12][13][14]. This indicates that studies across multiple spatial scales will be necessary to understand source-sink dynamics in foliar fungi. ...
... The primary drivers of source-sink dynamics in foliar fungal endophyte communities were local, in line with our expectations. Evidence is accumulating that dispersal limitation is an important determinant of local to regional fungal community assembly, based on a small number of direct measurements [12,37] and more common distance-decay patterns [8,38,39]. For example, experimental plantings and spore traps demonstrated that ectomycorrhizal fungal richness declined rapidly with increasing distance from a large contiguous patch of source hosts [12]. ...
... Evidence is accumulating that dispersal limitation is an important determinant of local to regional fungal community assembly, based on a small number of direct measurements [12,37] and more common distance-decay patterns [8,38,39]. For example, experimental plantings and spore traps demonstrated that ectomycorrhizal fungal richness declined rapidly with increasing distance from a large contiguous patch of source hosts [12]. Based on aerial sampling, fungal spore size may also limit the transmissibility of specific taxa [13,14], but see [40]. ...
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Microbial communities, like their macro-organismal counterparts, assemble from multiple source populations and by processes acting at multiple spatial scales. However, the relative importance of different sources to the plant microbiome and the spatial scale at which assembly occurs remains debated. In this study, we analyzed how source contributions to the foliar fungal microbiome of a C4 grass differed between locally abundant plants and soils across an abiotic gradient at different spatial scales. Specifically, we used source-sink analysis to assess the likelihood that fungi in leaves from Panicum hallii came from three putative sources: two plant functional groups (C4 grasses and dicots) and soil. We expected that physiologically similar C4 grasses would be more important sources to P. hallii than dicots. We tested this at ten sites in central Texas spanning a steep precipitation gradient. We also examined source contributions at three spatial scales: individual sites (local), local plus adjacent sites (regional), or all sites (gradient-wide). We found that plants were substantially more important sources than soils, but contributions from the two plant functional groups were similar. Plant contributions overall declined and unexplained variation increased as mean annual precipitation increased. This source-sink analysis, combined with partitioning of beta-diversity into nestedness and turnover components, indicated high dispersal limitation and/or strong environmental filtering. Overall, our results suggest that the source-sink dynamics of foliar fungi are primarily local, that foliar fungi spread from plant-to-plant, and that the abiotic environment may affect fungal community sourcing both directly and via changes to host plant communities.
... Estimates suggest that only about 2 % of spores from wind-dispersed basidiomycete species travel beyond 5.2 m of the parent sporocarps (Li 2005), while about 5 % of spores travel beyond one metre (Galante et al. 2011). Among ectomycorrhizal fungi, density and diversity of winddispersed spores decrease with distance from forest edges, with few spores detected at distances over 1 km from the forest edge (Peay et al. 2012). Once landed, spores must find suitable substrates (for saprophytic species) or hosts (for mycorrhizal and parasitic species) to germinate. ...
... For sexual reproduction, individuals need to meet nearby compatible genetic strains. Therefore, spores landing closer to their parent sporocarps have a greater probability of finding suitable habitat and mating types (Kytöviita 2000, Peay et al. 2012, Horton 2017; however, proximity to the parent may also reduce the genetic diversity (thus the adaptability and resilience) of the species in the area. For example, low genetic diversity detected in populations of the hypogeous commercial truffle Tuber melanosporum is likely due to difficulties in long-distance spore dispersal (Taschen et al. 2016). ...
Article
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The consumption of fungi by animals is a significant trophic interaction in most terrestrial ecosystems, yet the role mammals play in these associations has been incompletely studied. In this review, we compile 1 154 references published over the last 146 years and provide the first comprehensive global review of mammal species known to eat fungi (508 species in 15 orders). We review experimental studies that found viable fungal inoculum in the scats of at least 40 mammal species, including spores from at least 58 mycorrhizal fungal species that remained viable after ingestion by mammals. We provide a summary of mammal behaviours relating to the consumption of fungi, the nutritional importance of fungi for mammals, and the role of mammals in fungal spore dispersal. We also provide evidence to suggest that the morphological evolution of sequestrate fungal sporocarps (fruiting bodies) has likely been driven in part by the dispersal advantages provided by mammals. Finally, we demonstrate how these interconnected associations are widespread globally and have far-reaching ecological implications for mammals, fungi and associated plants in most terrestrial ecosystems.
... 17 Dispersal limitation has been shown to have strong impacts on diversity patterns of mycorrhizal fungi and consequently on their plant hosts. 12,13,18,19 Many mycorrhizal fungi produce fruiting bodies to disperse their spores. Most fruiting bodies that grow above ground (mushrooms) shoot their spores into the air and rely on wind to disperse them. ...
... 22 Although aboveground mushrooms shoot their spores into the air, most spores travel only a few meters from their source, so long-distance dispersal is relatively rare. 19,23 Animal-facilitated spore dispersal through consumption, called mycophagy, is an important process that increases the chances that mycorrhizal fungi, both mushrooms and truffles, will colonize the roots of young plants. [23][24][25] Birds are widely recognized as important dispersal vectors of seeds and are crucial for plant establishment in new locations, 26 but we know almost nothing about the importance of birds for fungal dispersal. ...
... Soil fungal communities are highly influenced by differences in soil physico-chemical properties and vegetation features such as host type or stand structure (i.e., niche processes; Větrovský et al., 2019). However, previous studies have found that geographical distance (i.e., neutral processes; Green and Bohannan, 2006) can have a primary role in shaping fungal community structure (Peay et al., 2012;Bahram et al., 2013;Peay and Bruns, 2014). Nevertheless, both niche and neutral processes have been described as extremes of a continuum, whereas biological communities are usually located somewhere between these two theoretical extremes (Gravel et al., 2006), raising the need to determine the relative importance of each process on soil fungal community assembly in different ecosystems (Cao et al., 2019). ...
... There is a consensus that changes in soil physico-chemical properties, particularly the availability of nutrients such as N and P (Read and Perez-Moreno, 2003), shape soil fungal communities at global (Tedersoo et al., 2014), regional (Kivlin et al., 2014) and fine spatial scales (Glassman et al., 2015). Our results at regional scale agree with this given that mycorrhizal and saprophytic communities were primarily influenced by site-specific soil properties but also by geographical distance (i.e., dispersal limitation; Peay et al., 2012;Peay and Bruns, 2014). However, only a small proportion of compositional variation in this study was explained by the tree host (i.e., Pinus species) and stand structural variables. ...
Article
Soil fungi are fundamental drivers of forest ecosystem processes. Soil physico-chemical parameters and vegetation features such as host type or stand structure can affect soil fungal communities. However, there is a lack of comprehensive studies describing the relative importance of niche processes (soil physico-chemistry and forest structural drivers) versus neutral processes (geographical distance) driving soil fungal community assemblages, especially in less-studied drought-prone ecosystems such as Mediterranean forests. In this study, we performed Pacific Biosciences sequencing of internal transcribed spacer 2 amplicons to characterize the soil fungal community composition and diversity of 42 forests dominated by either pure Pinus nigra, Pinus halepensis or Pinus sylvestris or a P. nigra–P. halepensis or P. nigra–P. sylvestris mixture. Our specific aims were to identify and disentangle the relative importance of the main soil characteristics and the spatial and forest structural factors that accounted for the greatest proportion of fungal community variation along a regional gradient in the Mediterranean Pre-Pyrenees. Soil parameters accounted for the greatest significant proportion of the total variance in the overall fungal community (25%), and in the mycorrhizal (23%) and saprotrophic (22%) communities, while geographical distance accounted for 14% of the variance in the overall fungal community, 7% in the mycorrhizal and 22% in the saprotrophic communities. Conversely, forest structure did not significantly affect the soil fungal community, as fungal composition and diversity did not differ significantly among the pine hosts. Moreover, pH, followed by P and the C:N ratio explained the largest differences in the composition of the overall fungal community and in the mycorrhizal fungal community. By contrast, the largest proportion of differences in saprotrophic composition were explained by geographical distance, closely followed by the C:N ratio and N. Our results show that, in these Mediterranean pine forests, soil parameters are the most important driving forces shaping soil fungal communities at the regional scale given that ectomycorrhizal and saprotrophic fungi were more influenced by soil physico-chemical parameters or geographical distance than by Pinus species or forest structural variables. Finally, P content in soils also emerged as a significant factor driving differences in mycorrhizal communities.
... However, bacteria exhibited significantly lower βNTI than fungi (Fig. 1A), indicating greater importance of homogenous selection in structuring bacterial communities and greater importance of neutral processes in structuring fungal communities, which has also been previously reported [13,17]. Specifically, fungal communities were primarily structured by dispersal limitation (Fig. 1C), possibly attributed to the large proportion of dispersal-limited mycorrhizal taxa (~30% of sequences) present in these soils (Fig. S8) [18]. The importance of homogeneous selection in structuring bacterial communities is consistent with the strong and well-known relationships between bacterial communities and specific soil properties (e.g., pH, N availability) [3,4]. ...
... Greater homogenizing dispersal in reference soil bacteria (Fig. 1B) may be attributed to greater age and stability of the reference forests. In fungi, greater dispersal limitation in reference soils (Fig. 1C) may again reflect vegetation differences, which promote greater abundance of dispersallimited mycorrhizae in reference sites vs. disturbed sites (36 and 25% of sequences, respectively, Fig. S8) [18]. ...
Article
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Land use change has long-term effects on the structure of soil microbial communities, but the specific community assembly processes underlying these effects have not been identified. To investigate effects of historical land use on microbial community assembly, we sampled soils from several currently forested watersheds representing different historical land management regimes (e.g., undisturbed reference, logged, converted to agriculture). We characterized bacterial and fungal communities using amplicon sequencing and used a null model approach to quantify the relative importance of selection, dispersal, and drift processes on bacterial and fungal community assembly. We found that bacterial communities were structured by both selection and neutral (i.e., dispersal and drift) processes, while fungal communities were structured primarily by neutral processes. For both bacterial and fungal communities, selection was more important in historically disturbed soils compared with adjacent undisturbed sites, while dispersal processes were more important in undisturbed soils. Variation partitioning identified the drivers of selection to be changes in vegetation communities and soil properties (i.e., soil N availability) that occur following forest disturbance. Overall, this study casts new light on the effects of historical land use on soil microbial communities by identifying specific environmental factors that drive changes in community assembly.
... 17 Dispersal limitation has been shown to have strong impacts on diversity patterns of mycorrhizal fungi and consequently on their plant hosts. 12,13,18,19 Many mycorrhizal fungi produce fruiting bodies to disperse their spores. Most fruiting bodies that grow above ground (mushrooms) shoot their spores into the air and rely on wind to disperse them. ...
... 22 Although aboveground mushrooms shoot their spores into the air, most spores travel only a few meters from their source, so long-distance dispersal is relatively rare. 19,23 Animal-facilitated spore dispersal through consumption, called mycophagy, is an important process that increases the chances that mycorrhizal fungi, both mushrooms and truffles, will colonize the roots of young plants. [23][24][25] Birds are widely recognized as important dispersal vectors of seeds and are crucial for plant establishment in new locations, 26 but we know almost nothing about the importance of birds for fungal dispersal. ...
Article
Dispersal is a key process that impacts population dynamics and structures biotic communities. Dispersal limitation influences the assembly of plant and microbial communities, including mycorrhizal fungi and their plant hosts. Mycorrhizal fungi play key ecological roles in forests by feeding nutrients to plants in exchange for sugars, so the dispersal of mycorrhizal fungi spores actively shapes plant communities. Although many fungi rely on wind for spore dispersal, some fungi have lost the ability to shoot their spores into the air and instead produce enclosed belowground fruiting bodies (truffles) that rely on animals for dispersal. The role of mammals in fungal spore dispersal is well documented, but the relevance of birds as dispersal agents of fungi has been understudied, despite the prominence of birds as seed dispersal vectors. Here, we use metagenomics and epifluorescence microscopy to demonstrate that two common, widespread, and endemic Patagonian birds, chucao tapaculos (Scelorchilus rubecula) and black-throated huet-huets (Pteroptochos tarnii), regularly consume mycorrhizal fungi and disperse viable spores via mycophagy. Our metagenomic analysis indicates that these birds routinely consume diverse mycorrhizal fungi, including many truffles, that are symbiotically associated with Nothofagaceae trees that dominate Patagonian forests. Epifluorescence microscopy of fecal samples confirmed that the birds dispersed copious viable spores from truffles and other mycorrhizal fungi. We show that fungi are a common food for both bird species and that this animal-fungi symbiosis is widespread and ecologically important in Patagonia. Our findings indicate that birds may also act as cryptic but critical fungal dispersal agents in other ecosystems.
... Airborne dispersion of spores is generally effective at short distances, covering scarce meters from the sporocarps (Horton 2017). However, particularly for those EMF species that produce epigeous sporocarps, the production of a large number of spores could increase the chances of reaching further sites and accumulate in time (Galante et al., 2011;Peay et al., 2012;Hayward et al., 2015b). Suillus species, for example, are known to produce a large number of sporocarps: 300-1000 kg dry weight/ha per year (Hedger 1986, Chapela et al. 2001. ...
... Although visitors generally stay near the coast without entering to the forest interior, soil with viable EMF propagules can be carried on their shoes or in other artifacts introduced to the islets. Dispersion strongly determines the EMF community assembly (Peay et al., 2012;Vašutová et al., 2019), so distances reached by each form of dispersal will strongly condition the invasion chances of native stands. ...
Article
Positive interactions between non-native species can accelerate their invasion rate and exacerbate their impacts. This has been shown for non-native mammals that disperse invasive ectomycorrhizal fungi (EMF), in turn facilitating the invasion of non-native tree species. Mammal-mediated dispersion is assumed to be the main mechanism of EMF long distance dispersal, being particularly critical for truffle-like EMF species. We asked whether the absence of non-native mammals is an obstacle for Pinaceae invasion given the lack of invasive EMF being dispersed. We studied EMF species colonization and Pseudotsuga menziesii (Douglas-fir) trees’ growth in soil from mainland sites where non-native mammals are highly abundant, and lake islets in which they have been historically absent. Contrary to what we expected, we found invasive EMF, including truffle-like species, in sites where invasive mammals have been historically absent. Douglas-fir trees grew equally well and had the same EMF colonization in soil from mainland and islets. Alternative mechanisms of EMF dispersal, such as saltation, bird dispersal, or human dispersal, can be involved in their arrival to native stands. The presence of invasive EMF makes native sites vulnerable to Pinaceae invasion, even in the absence of mammalian dispersers.
... Actually, the small subset of EcM fungal communities was suggested to form propagule banks in the mature forests (Taylor and Bruns 1999;Glassman et al. 2015). Because competitive interactions among fungal species cannot occur in the absence of EcM host plants, the community compositions of both transition zone and artificial plantation forest types are expected to be determined mainly by spore dispersal (Ashkannejhad and Horton 2006;Peay et al. 2012), longevity , and dormancy (Bruns et al. 2009). All four of the dominant OTUs appear to produce durable propagules (i.e., sclerotia or dormant spores). ...
... Spore dispersal limitation is likely an important factor in decreased EcM fungal colonization as distance from EcM forest edges increases, as observed in both soil bioassays and in situ surveys (Nuñez et al. 2009;Hayward et al. 2015). Airborne spores produced by fruiting bodies of epigeous EcM fungi can be dispersed over several kilometers, but the spore load decreases considerably with increasing distance from forest edges (Galante et al. 2011;Peay et al. 2012). Unlike epigeous fungal spores, dispersal of hypogeous fungal spores is limited by the home range of animal vectors. ...
Article
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Ectomycorrhizal (EcM) fungal spores play an important role in seedling establishment and forest regeneration, especially in areas where compatible host tree species are absent. However, compared to other Pinaceae trees with a wide distribution, limited information is available for the interaction between the endangered Pseudotsuga trees and EcM fungi, especially the spore bank. The aim of this study was to investigate EcM fungal spore bank communities in soil in remnant patches of Japanese Douglas-fir (Pseudotsuga japonica) forest. We conducted a bioassay of 178 soil samples collected from three P. japonica forests and their neighboring arbuscular mycorrhizal artificial plantations, using the more readily available North American Douglas-fir (Pseudotsuga menziesii) as bait seedlings. EcM fungal species were identified by a combination of morphotyping and DNA sequencing of the ITS region. We found that EcM fungal spore banks were present not only in P. japonica forests but also in neighboring plantations. Among the 13 EcM fungal species detected, Rhizopogon togasawarius had the second highest frequency and was found in all plots, regardless of forest type. Species richness estimators differed significantly among forest types. The community structure of EcM fungal spore banks differed significantly between study sites but not between forest types. These results indicate that EcM fungal spore banks are not restricted to EcM forests and extend to surrounding forest dominated by arbuscular mycorrhizal trees, likely owing to the durability of EcM fungal spores in soils.
... & Gris. Considering the vicinity of sources of ECM fungal propagules and the dispersal abilities of ECM propagules [17], we assumed that natural diversified ECM inoculums would not be a limiting factor for nursery saplings being colonised by the variety of established ECM fungi. However, the conditions in nurseries, i.e., confined space, highly fertile soil, the occasional use of fungicides and abundant watering, prevent ectomycorrhizal interactions [18,19], and mostly involve opportunistic species with high dispersal abilities [20][21][22]. ...
... Indeed, nursery conditions, i.e., confined space, high soil fertility and abundant watering, significantly influence mycorrhizal interactions resulting in the selection of opportunistic ECM species and contribute to low ECM fungal diversity [51,52]. In the absence of any inoculation practices, we can assume that, at the end of the nursery stage, the T. calobuxus ECM fungal community was composed of ruderal species, which are easily dispersed by spores [17,40] and mostly adapted to survive in nursery conditions. Our observations of ECM diversity associated with T. calobuxus before planting were consistent with the observations reported by these authors. ...
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We investigated the suitability of Acacia spirorbis Labill., a tropical ectomycorrhizal (ECM) tree, as a nurse plant to improve the growth of Tristaniopsis calobuxus Brongn. & Gris seedlings for the restoration of nickel mines in New Caledonia. Rehabilitation of nickel mines in New Caledonia is a major concern. In such harsh soil conditions, ectomycorrhizal (ECM) symbiosis is important for tree growth, survival, and resistance. To improve ecological restoration in New Caledonia, new technical itineraries have undergone experimentation using ECM as a plant nurse, allowing ECM saplings to rapidly acquire a wide range of ECM fungi. We transplanted ECM seedlings of Tristani-opsis calobuxus from the nursery to bare ferralitic soils harbouring some scattered 12-year-old Acacia spirorbis to be used as ECM nurse plants. Using molecular characterisation of ITS rDNA, we char-acterised ECM fungal communities of A. spirorbis and of T. calobuxus saplings at transplanting time and 13 months later. We observed changes in the composition of fungal communities of T. calobuxus with an increase in diversity, notably the appearance of operational taxonomic units (OTUs) affiliated with /russulaceae, /boletus and /pisolithus-scleroderma and a decrease in ubiquitous nursery orders such as /sebacinales and /helotiales. We also observed a higher number of shared OTUs between T. calobuxus and A. spirorbis. The vicinity of A. spirorbis enabled diversification and adaptation of the T. calobuxus ECM fungal community. These results led us to recommend A. spirorbis as a good nurse tree candidate in the framework of ecological restoration of mine sites.
... 21 ). We therefore expect EEM and ORC fungi to be better able to establish on islands prior to their hosts compared to AM fungi, and EEM and orchid plant species to be less impacted by the mycorrhizal filter than AM plant species 22 . ...
... Our analyses support the hypothesis that dispersal limitation of AM fungi on distant islands is a stronger limiting factor in plant colonization of islands than the higher specificity of EEM associations. While there is empirical evidence of dispersal limitation of symbionts being important to both EEM and AM plant species 22,[33][34][35] , our work suggests that AM plants are more susceptible to symbiont dispersal limitation. Limited AM fungal dispersal to islands is supported by analyses of AM fungal composition showing differential AM fungal species abundances on islands compared to mainland regions 32 . ...
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Plant colonization of islands may be limited by the availability of symbionts, particularly arbuscular mycorrhizal (AM) fungi, which have limited dispersal ability compared to ectomycorrhizal and ericoid (EEM) as well as orchid mycorrhizal (ORC) fungi. We tested for such differential island colonization within contemporary angiosperm floras worldwide. We found evidence that AM plants experience a stronger mycorrhizal filter than other mycorrhizal or non-mycorrhizal (NM) plant species, with decreased proportions of native AM plant species on islands relative to mainlands. This effect intensified with island isolation, particularly for non-endemic plant species. The proportion of endemic AM plant species increased with island isolation, consistent with diversification filling niches left open by the mycorrhizal filter. We further found evidence of humans overcoming the initial mycorrhizal filter. Naturalized floras showed higher proportions of AM plant species than native floras, a pattern that increased with increasing isolation and land-use intensity. This work provides evidence that mycorrhizal fungal symbionts shape plant colonization of islands and subsequent diversification.
... This result was almost in agreement with the observation by Wang et al. (2020), who presented that fungi exhibited smaller taxonomic beta diversity without significant differences across islands under the processes of homogenizing dispersal and drift; however, these small difference in beta diversity may be because null model falsely produced non-significant βNTI values for fungi due to the uncertain in fungal phylogeny, therefore, a caution should be paid when interpreting the fungal phylogenetic turn over using this model. A smaller effect of dispersal on the fungal community was also observed and corroborated in previous studies (Prevost-Boure et al., 2014;Glassman et al., 2017), which speculated that the fungal spores could transfer across regions via wind or water currents, even though the fungi were suggested to be dispersal limited in other cases (Peay et al., 2012;Talbot et al., 2014). ...
Article
The long-standing challenge in microbial ecology is to quantify the relative importance of deterministic and stochastic processes in controlling the community structures through space and time. Deterministic processes are important when the environmental selection and species interactions are strong, whereas stochastic processes may dominate when there is large number of neutral births, death, speciation of microorganism. The existing studies are still lacking in understanding how these two processes structure microbial communities in an ecosystem whose environmental gradients change sharply at a very short geographic scale, such as in the fresh-saltwater transition zone. Here, we investigated the bacterial and fungal assembly processes in topsoil (0–10 cm) in a wetland transect with fresh-saltwater transition zone in the Yellow River Estuary (YRE), China, by calculating beta-mean-nearest taxon distance (βMNTD), beta nearest taxon index (βNTI) and Raup–Crick index. We found that stochastic processes primarily shaped the two communities. The bacterial assembly was controlled by homogenizing dispersal and dispersal limitation within and across the wetland transect, respectively. The fungal assembly, on the other hand, was mostly regulated by undominated processes, which are processes induced by weak selection/dispersal, diversification, and drift. Dispersal limitation had more pronounced effects on the bacterial diversity and cooccurrence in comparison with the effects of undominated processes on the fungal community. Nevertheless, environmental factors, such as pH, salinity and C/N, explained ∼30% (p < 0.01) of compositional variations with more explanatory power for bacteria than fungi. Our study highlights the different types of stochastic processes in regulating bacterial and fungal communities along the short natural environmental gradients.
... Efforts have also been made to classify AM fungi into edaphophilic or rhizophilic guilds related to differential allocation to soil hyphae or root colonization, respectively, and how that relates to mycorrhizal function [35,36]. In EcM fungi, previous work has defined mycorrhizal traits as differences in morphology and physiology of mycelial [37] and reproductive structures [38] that produce differences in species' capacity for carbon storage, enzymatic activity, nutrient uptake and translocation, dispersal, and habitat colonization [27,[39][40][41][42]. Alternatively, plantcentric perspectives have shown how mycorrhizal symbioses explain significant variation in plant life history strategies [43] and multivariate root trait space [44], accounting for different C-S-R and resource utilization strategies of plants across the globe. ...
Article
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Traits are inherent properties of organisms, but how are they defined for organismal networks such as mycorrhizal symbioses? Mycorrhizal symbioses are complex and diverse belowground symbioses between plants and fungi that have proved challenging to fit into a unified and coherent trait framework. We propose an inclusive mycorrhizal trait framework that classifies traits as morphological, physiological, and phenological features that have functional implications for the symbiosis. We further classify mycorrhizal traits by location – plant, fungus, or the symbiosis – which highlights new questions in trait-based mycorrhizal ecology designed to charge and challenge the scientific community. This new framework is an opportunity for researchers to interrogate their data to identify novel insights and gaps in our understanding of mycorrhizal symbioses.
... Similarly, Chen et al. (2020a) showed that dispersal limitation played an important role in distribution patterns of the fungal communities in sediments along large rivers, which was supported by the lower immigration rate. This lower immigration rate is probably due to geographic barriers and special fungal propagules (spores and mycelia) (Peay et al., 2012). Meanwhile, the unknown environmental factors with spatial structure may also contribute to this phenomenon. ...
Article
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Inland river basins include critical habitats and provide various ecosystem services in extremely arid lands. However, we know little about the distribution patterns of soil fungal communities in these river basins. We investigated the distribution patterns of soil fungal communities from the riparian oasis zone (ROZ) to the circumjacent desert zone (CDZ) at the lower reaches of the Heihe River. The results indicated that soil fungal communities were mainly dominated by the phyla Ascomycota and Basidiomycota across all samples. The dominant soil fungi taxa were significantly different between ROZ and CDZ habitats at both the phylum and genus levels. Fungal alpha diversity was mainly affected by spatial factors and plant functional traits, and Pearson correlation analysis revealed that fungal alpha diversity was more closely related to plant functional traits than soil properties. Furthermore, fungal community structure was best explained by spatial factors and plant attributes (including plant diversity and plant functional traits). Together, our findings provide new insights into the significance of spatial factors and plant attributes for predicting distributions of fungal communities in arid inland river basins, which will help us better understand the functions and services of these ecosystems. This article is protected by copyright. All rights reserved.
... The findings of the present study have important implications with respect to our understanding of the biogeography of ECM fungi. Peay et al. (2012) have previously shown that, as the distance from the spore source increases, the number of spores reach and the consequent probability of ECM fungal colonization declines, suggesting that the dispersal limitation is a crucial factor to determine the distribution of ECM fungi. Nevertheless, our results show host-fungus incompatibility between exotic host plant and native ECM fungi growing in the same area (within ca. ...
Article
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Host specificity may potentially limit the distribution expansion of ectomycorrhizal (ECM) fungi into areas where their original host plants are absent. To test this hypothesis, we investigated whether populations of native ECM fungi may establish in stands of exotic host trees, namely those of the Eucalyptus species, in Japan. ECM fungal communities associated with eucalyptus and surrounding native host species ( Pinus thunbergii and Fagaceae spp.) were investigated at two sites; one site in which eucalyptus and native trees were growing in isolation, and a second site in which these species were mixed. To identify fungal taxa, the nuclear ribosomal internal transcribed spacer region 1 was sequenced for the ECM fungi from the root tips and clustered into operational taxonomic units (OTUs). To confirm whether the retrieved OTUs were native to Japan, they were queried against the entire database of the National Center for Biotechnology Information, UNITE, and GlobalFungi, whereby sampling locations and associated hosts were obtained from sequences with ≥97% similarity. Eucalyptus trees were associated with seven and 12 ECM fungal OTUs, including putatively exotic OTUs in isolated and mixed sites, respectively. Among the 36 and 63 native ECM fungal OTUs detected from native hosts at isolated and mixed sites, only one OTU was shared with eucalyptus at the respective sites. This means that most native ECM fungi in Japan may be incapable of forming an association with exotic Eucalyptus spp. Notably, even ECM fungi associated with both Pinus and Quercus were not detected from eucalyptus, suggesting that host-fungus incompatibility is determined not only by host phylogenetic relatedness but also by host biogeographic affinities. Our findings show that the incompatibility with eucalyptus as well as dispersal limitation may prevent the distribution expansion of native ECM fungi in Japan into the distribution ranges of Eucalyptus spp., where the original hosts are absent.
... In accordance with our results regarding the absence of IBD across our three plots together with positive genetic correlation between individuals within each plot, we suppose that genetic exchange across the sites in our study can be realized via multiple short-distance dispersal events, as already proposed Wang et al. (2015). Moreover, the massive fruit body production related to abundant spore production may contribute to dispersal by wind (Peay et al., 2012) and animals (Johnson, 1996) and enable colonization of new habitats. Ashkannejhad and Horton (2006) found viable spores of Suillus and Rhizopogon spp. in deer fecal pellets. ...
Article
Although Russula ochroleuca is a common ectomycorrhizal (ECM) species in European forests, its reproduction mode, dispersal range, and population structure remains unknown. Altogether, 462 fruit bodies from three spruce forests (two 15 km apart, one 230 km distant from the first two) were analysed using AFLP markers. A mixed mode of reproduction, with several large genets accompanied by a majority of single fruit body genets, was found. Low level of inbreeding (Fis = 0.0021–0.0072), low level of genetic differentiation among subpopulations (PhiPT = 0.037–0.190) and negligible isolation by distance (r = 0.033, P = 0.005) indicates effective spore dispersal and a high level of outcrossing across the sampled area. Finally, we discovered temporal diversification within this species, as evidenced by genetic differentiation between early (August) and late (September) fruiting genotypes.
... The extent to which communities track climate and thereby modify direct effects of climate is a pressing unanswered question in biogeochemistry (Koven 2013). Yet limited dispersal and niche conservatism in at least some microbial communities (Peay et al. 2012) raises the possibility that disturbances, such as climate change, may decouple contemporary controls and result in novel macrosystem patterns (Fig. 1c). There is theoretical and empirical support for macrosystem patterns emerging from such interactions between broad-scale drivers and fine-scale processes (Peters et al. 2007;Heffernan et al. 2014). ...
Article
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Soil organic matter (SOM) stocks, decomposition and persistence are largely the product of controls that act locally. Yet the controls are shaped and interact at multiple spatiotemporal scales, from which macrosystem patterns in SOM emerge. Theory on SOM turnover recognizes the resulting spatial and temporal conditionality in the effect sizes of controls that play out across macrosystems, and couples them through evolutionary and community assembly processes. For example, climate history shapes plant functional traits, which in turn interact with contemporary climate to influence SOM dynamics. Selection and assembly also shape the functional traits of soil decomposer communities, but it is less clear how in turn these traits influence temporal macrosystem patterns in SOM turnover. Here, we review evidence that establishes the expectation that selection and assembly should generate decomposer communities across macrosystems that have distinct functional effects on SOM dynamics. Representation of this knowledge in soil biogeochemical models affects the magnitude and direction of projected SOM responses under global change. Yet there is high uncertainty and low confidence in these projections. To address these issues, we make the case that a coordinated set of empirical practices are required which necessitate (1) greater use of statistical approaches in biogeochemistry that are suited to causative inference; (2) long-term, macrosystem-scale, observational and experimental networks to reveal conditionality in effect sizes, and embedded correlation, in controls on SOM turnover; and (3) use of multiple measurement grains to capture local- and macroscale variation in controls and outcomes, to avoid obscuring causative understanding through data aggregation. When employed together, along with process-based models to synthesize knowledge and guide further empirical work, we believe these practices will rapidly advance understanding of microbial controls on SOM and improve carbon cycle projections that guide policies on climate adaptation and mitigation.
... Studies are showing that spore shape does not affect dispersal distance (Crandall, 2016;Hussein et al., 2013). In contrast, e.g., Peay et al. (2012) and Tulloss (2005) reported that elliptical spores are carried further by wind than round ones. This is corroborated by studies that showed that elliptical spores occur more often in open forests (chaparral) (Botnen et al., 2019) and nutrient-deprived settings (Halbwachs et al., 2017). ...
Chapter
Functional traits are widely recognized as a useful framework for testing mechanisms underlying species community assemblage patterns and ecosystem processes. While botanists have developed this field during the past 20 years, mycology still needs to catch up. Only during recent years, ecological research has begun to recognize the fundamental role of fungi in virtually all ecosystems. For this role, the mechanistic background needs to be uncovered, which is tightly intertwined with fungal functional traits. These traits are of morphological, physiological, and behavioral nature. In this article, current knowledge is presented, and gaps to be closed are analyzed.
... In this system, each tree island could represent a refugia for fungi that associate with Pseudotsuga instead of graminoid arbuscular mycorrhizal fungi in the broader landscape. Because successful fungal spore dispersal decreases with distance from its source (Peay et al., 2012), forest fragmentation could lead to isolated communities prone to priority effects and stochastic assembly. Glassman, Lubetkin, et al. (2017) found that EMF richness increased with tree island size in an alpine community and decreased with distance from the forest (Cline et al., 2005;Grove et al., 2019). ...
Article
1. Fungal communities can influence the productivity, composition, and survival of trees through cycling nutrients, providing resources, and altering pathogens. Thus, shifts in fungal communities could impact forests by altering interactions between trees and their environments. Fungal community composition may be shaped by stochastic and deterministic processes such as dispersal‐limitation, environmental filtering, and partner specificity between trees and fungi. For tree species with large geographic ranges, we expect fungal assembly processes to change with environmental variation across the range of the tree partner. Due to specificity between trees and symbiotic fungi, we expect deterministic to outweigh stochastic processes in root compared with soil fungi. As some tree species have exceptional longevity, we also expected tree age to influence fungal community assembly. 2. We surveyed fungi in four stands of Pseudotsuga menziesii with tree ages up to 800 years along an 1,800 km transect. We sampled roots and soil around 12 P. menziesii in each stand, aged the trees, and sequenced fungal rDNA to determine composition and richness from which we calculated the relative role of deterministic and stochastic assembly processes. We used null models to evaluate the relative importance of deterministic variable and homogenizing selection, and stochastic dispersal‐limitation, drift, and homogenizing dispersal in fungal community assembly. 3. We detected 7,280 amplicon sequence variants with 5,270 associated with soil, 3,887 with roots and 1,877 found across both roots and soils. Deterministic processes dominated root and soil fungal communities at all sites except one where stochastic processes (i.e., dispersal‐limitation and drift) controlled root‐fungi. Despite the dominance of determinism in fungal community assembly, the proportion of processes differed by site. Assembly processes did not vary with tree age. 4.Synthesis Taken together, we suggest that the local environment, water limitation, and partner‐preference between trees and their associated fungi, influence fungal community composition across the range of P. menziesii. We conclude that while fungal communities occurring near P. menziesii are dominated by homogenizing selection, the role of neutral processes still has a minor influence on community assembly and may be important in spatially isolated communities and those with strong gradients of fungal diversity.
... We predicted that ectomycorrhizal fungi would demonstrate distance decay as a function of dispersal limitation, but that foliar endophytes would demonstrate distance decay as a function of environmental dissimilarity. Our predictions are based on the observations that ectomycorrhizal fungi typically have a limited ability to disperse, often on the scale of only one or a few meters [31][32][33]. In contrast, foliar endophytes seem to have little dispersal limitation at local to regional scales if no physical barriers are present and compatible hosts are available [26,30,34]. ...
Article
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Fungal communities associated with plants often decrease in similarity as the distance between sampling sites increases (i.e., they demonstrate distance decay). In the southwestern USA, forests occur in highlands separated from one another by warmer, drier biomes with plant and fungal communities that differ from those at higher elevations. These disjunct forests are broadly similar in climate to one another, offering an opportunity to examine drivers of distance decay in plant-associated fungi across multiple ecologically similar yet geographically disparate landscapes. We examined ectomycorrhizal and foliar endophytic fungi associated with a dominant forest tree (Pinus ponderosa) in forests across ca. 550 km of geographic distance from northwestern to southeastern Arizona (USA). Both guilds of fungi showed distance decay, but drivers differed for each: ectomycorrhizal fungi are constrained primarily by dispersal limitation, whereas foliar endophytes are constrained by specific environmental conditions. Most ectomycorrhizal fungi were found in only a single forested area, as were many endophytic fungi. Such regional-scale perspectives are needed for baseline estimates of fungal diversity associated with forest trees at a landscape scale, with attention to the sensitivity of different guilds of fungal symbionts to decreasing areas of suitable habitat, increasing disturbance, and related impacts of climate change.
... During tree seedling establishment, successful mycorrhizal colonization from dispersal depends on the presence of spores from the correct mycorrhizal associate (AM or ECM) and the spores being abundant enough to colonize roots (Peay et al., 2012). Additionally, although some tree species are able to establish in open areas, many require microsites where downed woody material or vegetative cover provide shade or protection (Gray & Spies, 1997), making spore dispersal to these microsites particularly important. ...
Article
Animals that disperse plant or fungal propagules following forest disturbances, including timber harvests, play an important role during forest regeneration by dispersing seeds or spores from intact communities to disturbed sites. Determining how complementary or redundant animal species are as dispersers of propagules is key to understanding the stability of dispersal dynamics and informing management practices. Here we examine the functional, temporal, and spatial components of mycorrhizal fungal spore dispersal by small mammals (rodents and shrews) following timber harvest. We tracked the interactions of seven mammal species and 34 fungal taxa composed of two mycorrhizal functional types, arbuscular mycorrhizae (AM) and ectomycorrhizae (ECM), in 11 patch cuts (0.4 ha) distributed across hardwood and mixedwood forest in the northeastern USA. Over a two‐year period directly following harvests, we measured the relative contribution of mammal species to spore dispersal using networks that integrated mammal abundance with spore loads in scat. We also measured species‐specific microhabitat associations. Mammals were complementary in their dispersal of AM and ECM fungal spores. However, within AM dispersal networks, mammals were redundant, with asynchrony in mammal population fluctuations among years leading to changes in the relative importance of mammal species. Comparatively, ECM fungal spore consumption and dispersal was primarily provided by one rodent species (Myodes gapperi), resulting in dispersal networks that were highly specialized. This indicates that AM spore dispersal is more robust to changes in mammal community turnover compared to ECM spore dispersal. Mammal species varied from having no microhabitat associations to associating with a variety of different forest structure and ground cover conditions, indicating that species play different roles from broadcasting spores widely to depositing spores in discrete locations. By preserving microhabitat characteristics that are associated with small mammals in harvested areas, particularly downed wood and patches of pre‐harvest vegetation, forest managers can help maintain dispersal of mycorrhizal fungi.
... By contrast, we found that conspecific versus heterospecific recruitment neighborhoods did not affect overall patterns While we cannot confirm how the fungal communities varied in the absence of molecular sequencing data, we expect that spatial variation is likely driven by differential abundance and composition of mycorrhizal fungi and fungal or Oomycete pathogens between conspecific and heterospecific neighborhoods. This is not unexpected, as other studies have shown decreased abundance of hostspecific pathogens (Augspurger & Wilkinson, 2007;Bagchi et al., 2014;Packer & Clay, 2000) and mycorrhizal fungi (Dickie & Reich, 2005;Peay et al., 2012) away from host trees, along with general coturnover of microbial and plant communities (Peay et al., 2013;Russo et al., 2012). Similarly, in our previous shade-house experimental study at Lambir, EM colonization of dipterocarp seedlings decreased in soils collected from beneath non-dipterocarp hosts, and application of a Captan fungicide significantly reduced EM colonization on the roots of several different species of dipterocarp seedlings, including D. aromatica (Segnitz et al., 2020). ...
Article
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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 of D. 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 of D. 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. We present a rare‐field experiment in which we manipulated both the recruitment neighborhood (whether or not seedlings recruited in proximity to adult conspecifics) and seedling density to explore how they interact to influence the growth and survival of a dominant ectomycorrhizal tree species in a Bornean tropical rainforest. 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 and that ectomycorrhizal fungi play an important role in reducing CNDD for some tropical trees.
... Most red-listed species prefer closed-canopy conditions (Nordén et al. 2013), likely due to the moist microclimate and the buffering impact of the canopy on temperature and moisture extremes. Long-distance dispersal events seem rare (Peay et al. 2012, Golan and Pringle 2017, Abrego et al. 2020, especially for species with thin-walled or hyaline spores (the majority of boreal wood-decomposer fungi) that lose viability when exposed to ultraviolet light during dispersal (Norros et al. 2015). This is in contrast to species with thick-walled or dark spores, such as many pathogens, that may more readily disperse over large distances (Brown and Hovmøller 2002). ...
Technical Report
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In this report, we summarize the current state of knowledge and best estimates of how climate change is expected to impact Norwegian forest ecosystems from now to the year 2100
... Recent studies investigating the ECM fungal community spanning multiple forests varying in host tree species (ranging over hundreds or thousands of kilometres) have revealed that ECM fungal communities can vary across spatially isolated sites, showing spatial pattern (García-Guzmán et al., 2017;Ostonen et al., 2011;Põlme et al., 2013;Rosinger et al., 2018;Roy et al., 2013;Tedersoo et al., 2012). These studies have shown that the main drivers of fungal communities are host species Rosinger et al., 2018;van der Linde et al., 2018;Wu et al., 2018), climate (Jarvis et al., 2013;Miyamoto et al., 2015Miyamoto et al., , 2018 and edaphic factors (Horton et al., 2013;Lilleskov et al., 2002;Truong et al., 2019), as well as dispersal-related processes Peay et al., 2012). Among these, differences in host tree communities are often critical factors that drive variations in ECM fungal community structures. ...
Article
Ectomycorrhizal (ECM) fungal community structures can vary across sites at a regional scale (>1,000 km), affected by abiotic and biotic environments, dispersal abilities of the fungi, or ecological drift, even among forests of the same host tree species. The spatial patterns of such variation may differ among associated host species and their growth environments, but our knowledge about this remains limited. In the present study, we aimed to investigate whether the ECM fungal community structures (i.e. species richness and species composition) at the regional scale and their driving factors vary across hosts. Japan. ECM fungi associated with Fagus crenata and Castanopsis sieboldii. Using DNA metabarcoding of fine roots, the ECM fungal communities of 15 Fagus crenata forests across their distribution range were characterised. The resultant community structure of ECM fungi, as well as the relative effects of edaphic, climatic and spatial factors on community composition were compared with those of 12 Castanopsis sieboldii forests investigated in a previous study. ECM fungal community composition differed between the two Fagaceae hosts. The spatial pattern of ECM fungal community composition also differed between hosts. Specifically, the spatial variation in community composition across sites was smaller in F. crenata forests than in C. sieboldii forests. The spatial pattern of ECM fungal communities of F. crenata forests was explained by climatic and edaphic factors, while that of C. sieboldii forests was explained by spatial and edaphic factors. On a regional scale in Japan, the spatial pattern of ECM fungal communities and its driving factors varied between two Fagaceae host species. Our results provide an example that the difference in associated host leads to the difference in environmental response among ECM fungal communities.
... Although the soil and plant tissue surveys were performed only once, the results suggested that DNA of terrestrial fungi present in the soil and plant tissues at the study site may be recruited into the stream. For these terrestrial fungi, spores and/or mycelial fragments released on land may have entered the stream through air, rainfall and host tissues (Galante et al., 2011;Peay et al., 2012;Voronin, 2014;Chen et al., 2018;Castaño et al., 2019;Redondo et al., 2020). ...
Article
Investigation of seasonal variation in fungal communities is essential for understanding biodiversity and ecosystem functions. However, the conventional sampling method, with substrate removal and high spatial heterogeneity of community composition, makes surveying the seasonality of fungal communities challenging. Recently, water environmental DNA (eDNA) analysis has been explored for its utility in biodiversity surveys. In this study, we assessed whether the seasonality of fungal communities can be detected by monitoring eDNA in a forest stream. We conducted monthly water sampling in a forest stream over two years and used DNA metabarcoding to identify fungal eDNA. The stream water contained DNA from functionally diverse aquatic and terrestrial fungi, such as plant decomposers, parasites, and mutualists. The variation in the fungal assemblage showed a regular annual periodicity, meaning that the assemblages in a given season were similar, irrespective of the year or sampling. Furthermore, the strength of the annual periodicity varied among functional groups. Our results suggest that forest streams may act as a “trap” for terrestrial fungal DNA derived from different habitats, allowing the analysis of fungal DNA in stream water to provide information about the temporal variation in fungal communities in both the aquatic and the surrounding terrestrial ecosystems. This article is protected by copyright. All rights reserved.
... Yet, many EcM fungi have been shown to be dispersal limited, with around 96% of their spores potentially landing within one meter of where they are released (Galante et al. 2011). In addition, the richness and quantity of EcM spores decreases with increasing distance from habitats dominated by EcM host vegetation (Peay et al. 2012). Nevertheless, in other instances, EcM fungi have been found to be capable of cross continental dispersal (Geml et al. 2012;Tedersoo et al. 2014), suggesting that a combination of dispersal limitation due to distance and host availability, together with environmental filtering, contribute to EcM community assembly (Geml et al. 2008). ...
Chapter
This chapter provides an up-to-date account of fungi and the factors driving their biogeographic patterns, focusing mainly on terrestrial fungi and in particular mycorrhizal fungi due to their more established and studied biogeographic patterns. It also provides some insights into the biogeography of aquatic and animal-associated fungi. It is important to understand the evolutionary history of fungi because this could explain some of their biogeographical patterns, especially with reference to symbioses. The chapter discusses how fungal functions and their interactions with other organisms can affect fungal biogeography. Global environmental change driven by human disturbance, climate change and natural hazards can fundamentally alter the distribution and activity of fungi in time and space, while fungi can buffer or exacerbate the effects of global change on other organism groups.
... Thus, we do not know whether macroecological rules can also explain trait responses in local thermal variability, e.g., mediated via vegetation cover. Finally, on macroecological scales, other processes, than climate, may produce the observed pattern, e.g., dispersal limitation (MacArthur and MacArthur, 1961;Leibold et al., 2004;Vellend, 2010;Peay et al., 2012). Therefore, we investigated Bogert's rule for fruit body-forming fungi along a macroclimatic elevational gradient and assessed vegetation cover as a proxy for local microclimatic variability. ...
Article
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Understanding how species relate mechanistically to their environment via traits is a central goal in ecology. Many macroecological rules were found for macroorganisms, however, whether they can explain microorganismal macroecological patterns still requires investigation. Further, whether macroecological rules are also applicable in microclimates is largely unexplored. Here we use fruit body-forming fungi to understand both aspects better. A recent study showed first evidence for the thermal-melanism hypothesis (Bogert's rule) in fruit body-forming fungi and relied on a continental spatial scale with large grid size. At large spatial extent and grid sizes, other factors like dispersal limitation or local microclimatic variability might influence observed patterns besides the rule of interest. Therefore, we test fungal assemblage fruit body color lightness along a local elevational gradient (mean annual temperature gradient of 7 • C) while considering the vegetation cover as a proxy for local variability in microclimate. Using multivariate linear modeling, we found that fungal fruiting assemblages are significantly darker at lower mean annual temperatures supporting the thermal-melanism hypothesis. Further, we found a non-significant trend of assemblage color lightness with vegetation cover. Our results support Bogert's rule for microorganisms with macroclimate, which was also found for macroorganisms.
... The application of community assembly to fungi has already helped explain community patterns in fungal wood decomposers (Fukami et al. 2010) and AM fungi (Maherali and Klironomos 2012). In addition, priority effects, where early arrival of some taxa alters the success of later arriving taxa, occur in nectar yeasts inhabiting insect-pollinated flowers (Peay et al. 2012) and fungal endophytes following disturbance (Sikes et al. 2016). Trait-based assembly models may be useful in determining post-fire fungal communities, as fire-associated mortality (severity dependent) reduces fungal competition in ways that also shape post-fire community assembly. ...
Article
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Fires occur in most terrestrial ecosystems where they drive changes in the traits, composition, and diversity of fungal communities. Fires range from rare, stand-replacing wildfires to frequent, prescribed fires used to mimic natural fire regimes. Fire regime factors, including burn severity, fire intensity, and timing, vary widely and likely determine how fungi respond to fires. Despite the importance of fungi to post-fire plant communities and ecosystem functioning, attempts to identify common fungal responses and their major drivers are lacking. This synthesis addresses this knowledge gap and ranges from fire adaptations of specific fungi to succession and assembly fungal communities as they respond to spatially heterogenous burning within the landscape. Fires impact fungi directly and indirectly through their effects on fungal survival, substrate and habitat modifications , changes in environmental conditions, and/or physiological responses of the hosts with which fungi interact. Some specific pyrophilous, or "fire-loving," fungi often appear after fire. Our synthesis explores whether such taxa can be considered cosmopolitan, and whether they are truly fire-adapted or simply opportunists adapted to rapidly occupy substrates and habitats made available by fires. We also discuss the possible inoculum sources of post-fire fungi and explore existing conceptual models and ecological frameworks that may be useful in generalizing fungal fire responses. We conclude with identifying research gaps and areas that may best transform the current knowledge and understanding of fungal responses to fire.
... The high host specificity and stress tolerance of R. togasawarius and the dormant properties of the spore banks suggest its importance in the early stage of P. japonica forest regeneration. The establishment of spore banks is expected to be determined by spore dispersal (Peay et al. 2012), but the spore distribution and dispersal distance of R. togasawarius are still poorly understood. ...
Article
Ectomycorrhizal (EcM) fungal spore banks can facilitate seedling establishment where compatible host tree species are absent. Although Rhizopogon togasawarius spore banks play an important role in the early establishment stage of endangered Japanese Douglas-fir (Pseudotsuga japonica) seedlings, the dispersal ecology of this EcM fungus is poorly understood. The objective of this study was to clarify the spatial distribution and dispersal distance of R. togasawarius spore banks that extend inside and outside extant P. japonica forests. We evaluated R. togasawarius spore banks in five remnant forests and neighboring arbuscular mycorrhizal artificial plantations using Douglas-fir (P. menziesii) seedling bioassays. Forty-five to ninety-five surface soils were collected along lines of increasing distance from P. japonica forests to neighboring plantations. In each forest, 60%–84% of the soils collected inside or within 50 m of forest boundaries of P. japonica forests harbored R. togasawarius spore banks. The occurrence of R. togasawarius decreased significantly with increasing distance from the forest boundaries. Moreover, R. togasawarius was detected in samples several hundred meters away from forest boundaries. These results suggest that R. togasawarius has a dispersal capacity to extend the range of the spore banks outside the forest of host trees.
... Given that vicariance is unlikely to be the main mechanism of arrival of the EcM symbiosis to Madagascar, long distance dispersal seems to be the most plausible alternative, and has been proposed for other late-diverging organisms (Renner et al. 2001, Nobre et al. 2010, Kainulainen et al. 2017. Long distance dispersal of EcM fungi is highly variable and across species (Peay et al. 2007(Peay et al. , 2010(Peay et al. , 2012Geml et al. 2012), Wilson et al. (2012) described the ancestral distribution of the Sclerodermatineae as North America-Asia-Southeast Asia; they speculate that taxa extant outside of this range (which includes Madagascar) could be attributed to long-distance dispersal capabilities combined with low host specificity. An ancestral area reconstruction of Amanitaceae, Russulaceae and Boletaceae would help decipher the multiple possibilities for the origin of their EcM habit. ...
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Madagascar is known for its high diversity and endemism of Fauna and Flora, which makes it particularly interesting for research on diversity and evolution. Fungi, however, have been largely overlooked, and whether fungi exhibit the same patterns as animals and plants has yet to be further examined. We collected fungal sporocarps and ectomycorrhizal (EcM) roots during opportunistic surveys in five forests in Madagascar and generated a dataset of fungal Internal Transcribed Spacer (ITS) DNA sequences. We analysed them together with all publicly available fungal ITS DNA sequences. We identified 620 Operational Taxonomic Units (OTUs) from Madagascar, 10% of which contained only sequences from our surveys. We found 292 OTUs belonging to EcM species with /russula-lactarius, /boletus, /tomentella-telephora, /cortinarius and /amanita as the most abundant EcM lineages. Overall, sixty percent of all the fungi and 81% of the EcM species found are endemic to Madagascar. Lastly, we conducted a phylogenetic analysis using all the OTUs in Amanitaceae, Boletaceae and Russulaceae families to elucidate their relative timing of arrival in Madagascar. We found that the EcM species from Madagascar in the three families diverged recently (less than 34 mya), long after the separation of India and Madagascar (88 mya), which is consistent with a dispersal mediated process of arrival on the island. Our study provides the first comprehensive view of the current state of knowledge of EcM fungi in Madagascar represented by molecular data useful for ecological and evolutionary studies.
... Yet, many EcM fungi have been shown to be dispersal limited, with around 96% of their spores potentially landing within one meter of where they are released (Galante et al. 2011). In addition, the richness and quantity of EcM spores decreases with increasing distance from habitats dominated by EcM host vegetation (Peay et al. 2012). Nevertheless, in other instances, EcM fungi have been found to be capable of cross continental dispersal (Geml et al. 2012;Tedersoo et al. 2014), suggesting that a combination of dispersal limitation due to distance and host availability, together with environmental filtering, contribute to EcM community assembly (Geml et al. 2008). ...
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Freshwater ecosystems occupy only 2.3% of Earth's surface, yet they support an excessive portion of the world's most speciose and endemic taxa. They are estimated to harbor 12% of the world's fauna and one third (18,000 species) of the global vertebrate species richness. In this chapter, the author draws together threads of recent theoretical and empirical results and patterns at multiple scales; both may offer a useful roadmap of theoretical background for identifying new paths of investigation and future challenges into the field of freshwater biogeography, which needs to be considered to safeguard the status of aquatic ecosystems. Neotropics and Afrotropics are among the global hotspots of freshwater fish endemism. Recent findings in freshwaters underscore the importance of studying simultaneously historical processes, drainage basin characteristics and local environmental conditions to understand variation in species richness. Freshwater species richness and endemism patterns are the result of climate, productivity and biogeographical history.
... Both genera have been previously recognized as being more dependent on production of spores than on vegetative mycelia in the soil for their reproduction (Redecker et al., 2001;Ishida et al., 2008). This ability to reproduce through propagules in the form of spores and other associated traits confers competitive advantages during the initial stages of forest succession (Nara et al., 2003;Ishida et al., 2008;Kennedy, 2010;Peay et al., 2012;Reverchon et al., 2015). ...
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While forest management impacts the ectomycorrhizal fungi (EMF) community, most of the evidence regarding such effects has been obtained from temperate forests of the Northern Hemisphere and little is known of their prevalence in highly diverse tropical habitats. This study analyzes the responses of the EMF community in managed tropical montane forests in the southern Mexican state of Chiapas. EMF community composition and diversity were evaluated over a 2-year period along a gradient of structural and microclimatic conditions of the forest associated with the stages of a cycle of silvicultural practices (R = release cutting, T = thinning, and F = final regeneration cutting), as well as in a mid-successional unmanaged forest (UF) as a reference system. The silvicultural practices involve varying intensities of tree harvesting (≈ 20% in T to ≈ 80% in F). It is hypothesized that: (1) diversity and composition of EMF communities are influenced by changes in forest conditions, principally as a result of canopy cover alteration due to forest management, and (2) late forest successional conditions are associated to more diverse EMF communities, while more intensive silvicultural practices reduce their diversity. A total of 75 EMF species were recorded. Diversity analysis using Hill numbers showed a close relationship between diversity and forest conditions: total species richness, 0 D = 5.7 ± 0.6 in F up to 11.7 ± 1.3 in UF; richness of abundant species, 1 D = 4.1 ± 0.4 in F up to 7.5 ± 0.4 in UF; richness of very abundant species 2 D = 3.3 ± 0.3 in R up to 5.5 ± 0.3 in UF. Canopy cover (9.8 ± 4% in F and 80.6 ± 5% in UF) was the main factor affecting EMF diversity, mainly due to its influence on herbaceous cover, tree species richness (path analysis, R 2 = 0.32; p < 0.05), and microclimatic variables. Turnover of the most abundant EMF species from the most intensive management practice towards the later successional forest conditions was observed. Late successional conditions allow for maintenance of more diverse EMF communities, while more intensive practices reduce their diversity (p < 0.05, in both cases). Rare fungal species appear to be more vulnerable to highly intensive management , and account for most of the EMF diversity in UF. The results indicate the importance of preserving relatively undisturbed species-rich forest stands near intensively managed stands in order to maintain biological integrity of the EMF community and ecosystem functioning in tropical montane forests.
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The assembly of biological communities depends on deterministic and stochastic processes whose influence varies across spatial and temporal scales. Although ectomycorrhizal (ECM) fungi play a key role in forest ecosystems, our knowledge on ECM community assembly processes and their dependency on spatial scales is still scarce. We analysed the assembly processes operating on ECM fungal communities associated with Cistus albidus L. and Quercus spp. in Mediterranean mixed forests (Southern Spain), for which root tip ECM fungi were characterized by high-throughput sequencing. The relative contribution of deterministic and stochastic processes that govern the ECM fungal community assembly was inferred by using phylogenetic and compositional turnover descriptors across spatial scales. Our results revealed that stochastic processes had a significantly higher contribution than selection on root tip ECM fungal community assembly. The strength of selection decreased at the smallest scale and it was linked to the plant host identity and the environment. Dispersal limitation increased at finer scales, whilst drift showed the opposite pattern likely suggesting a main influence of priority effects on ECM fungal community assembly. This study highlights the potential of phylogeny to infer ECM fungal community responses and brings new insights into the ecological processes affecting the structure and dynamics of Mediterranean forests.
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Root‐colonizing fungi form species‐rich assemblages with key functions in principal ecosystem processes, making them prospectively important players in conservation and applied ecology. Harnessing the processes and services they drive requires a better understanding of their patterns of diversity and community structure, and how these link to function. Here, we search for possible adaptations to contrasting environmental and host conditions, indicative of participation in habitat‐specific processes. We surveyed heathland and grassland habitats across a latitudinal gradient in Western Europe, using a spatially explicit design to assess community variation at scales from centimeters, to thousands of kilometers. Root‐associated fungi assemble into strongly site‐specific communities irrespective of habitat type, shaped by environmental factors and spatial distance operating at different scales, but also by a high level of endemism, likely determined by local stochastic processes such as drift and dispersal limitation at short distances. Despite the high site‐specificity in communities, they are dominated everywhere by a core set of lineages with little preferences toward habitat conditions or host phylogeny. Our results suggest a convergent evolution across phylogenetically distant lineages toward the root‐colonizing habit, and a functional redundancy in strategies for habitat colonization and host interaction. Further efforts are needed to integrate functional trait composition in future community ecology studies of root‐colonizing fungi.
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Aim Current evidence from temperate studies suggests that ectomycorrhizal (ECM) fungi require overland routes for migration because of their obligate symbiotic associations with woody plants. Despite their key roles in arctic ecosystems, the phylogenetic diversity and phylogeography of arctic ECM fungi remains little known. Here we assess the phylogenetic diversity of ECM communities in an isolated, formerly glaciated, high arctic archipelago, and provide explanations for their phylogeographic origins.
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The elevational gradient in plant and animal diversity is one of the most widely documented patterns in ecology and, although no consensus explanation exists, many hypotheses have been proposed over the past century to explain these patterns. Historically, research on elevational diversity gradients has focused almost exclusively on plant and animal taxa. As a result, we do not know whether microbes exhibit elevational gradients in diversity that parallel those observed for macroscopic taxa. This represents a key knowledge gap in ecology, especially given the ubiquity, abundance, and functional importance of microbes. Here we show that, across a montane elevational gradient in eastern Peru, bacteria living in three distinct habitats (organic soil, mineral soil, and leaf surfaces) exhibit no significant elevational gradient in diversity (r 2 , 0.17, P . 0.1 in all cases), in direct contrast to the significant diversity changes observed for plant and animal taxa across the same montane gradient (r 2 . 0.75, P , 0.001 in all cases). This finding suggests that the biogeographical patterns exhibited by bacteria are fundamentally different from those of plants and animals, highlighting the need for the development of more inclusive concepts and theories in biogeography to explain these disparities.
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Models of seed dispersal—a key process in plant spatial dynamics— have played a fundamental role in representing dispersal patterns, investigating disper-sal processes, elucidating the consequences of dispersal for populations and commu-nities, and explaining dispersal evolution. Mechanistic models of seed dispersal have explained seed dispersion patterns expected under different conditions, and illuminated the circumstances that lead to long-distance dispersal in particular. Phenomenological models have allowed us to describe dispersal pattern and can be incorporated into models of the implications of dispersal. Perhaps most notably, population and com-munity models have shown that not only mean dispersal distances but also the entire distribution of dispersal distances are critical to range expansion rates, recruitment pat-terns, genetic structure, metapopulation dynamics, and ultimately community diversity at different scales. Here, we review these developments, and provide suggestions for further research.
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A guide to using S environments to perform statistical analyses providing both an introduction to the use of S and a course in modern statistical methods. The emphasis is on presenting practical problems and full analyses of real data sets.
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