Connecting the multiple dimensions of global soil fungal diversity.

How the multiple facets of soil fungal diversity vary worldwide remains virtually unknown, hindering the management of this essential species-rich group. By sequencing high-resolution DNA markers in over 4000 topsoil samples from natural and human-altered ecosystems across all continents, we illustrate the distributions and drivers of different levels of taxonomic and phylogenetic diversity of fungi and their ecological groups. We show the impact of precipitation and temperature interactions on local fungal species richness (alpha diversity) across different climates. Our findings reveal how temperature drives fungal compositional turnover (beta diversity) and phylogenetic diversity, linking them with regional species richness (gamma diversity). We integrate fungi into the principles of global biodiversity distribution and present detailed maps for biodiversity conservation and modeling of global ecological processes.

Holarctic Species in the Pluteus podospileus Clade: Description of Six New Species and Reassessment of Old Names.

We studied the taxonomy of Pluteus podospileus and similar species using morphological and molecular (nrITS, TEF1-α) data, including a detailed study of the type collections of P. inflatus var. alneus, Pluteus minutissimus f. major, and P. granulatus var. tenellus. Within the P. podospileus complex, we phylogenetically confirmed six species in Europe, five in Asia, and eight in North America. Based on our results, we recognize P. seticeps as a separate species occurring in North America, while P. podospileus is limited to Eurasia. We describe six new species and a new variety: P. absconditus, P. fuscodiscus, P. gausapatus, P. inexpectatus, P. millsii, and P. notabilis and its variety, P. notabilis var. insignis. We elevate Pluteus seticeps var. cystidiosus to species rank as Pluteus cystidiosus. Based on the holotype of P. inflatus var. alneus, collections of P. inflatus identified by Velenovský, and several modern collections, we resurrect the name P. inflatus. Based on molecular analyses of syntypes of Pluteus minutissimus f. major and a holotype of Pluteus granulatus var. tenellus, we synonymize them under P. inflatus. We also increase our knowledge about the morphology and distribution of P. cutefractus.

Symbiotic status alters fungal eco-evolutionary offspring trajectories.

Despite host-fungal symbiotic interactions being ubiquitous in all ecosystems, understanding how symbiosis has shaped the ecology and evolution of fungal spores that are involved in dispersal and colonization of their hosts has been ignored in life-history studies. We assembled a spore morphology database covering over 26,000 species of free-living to symbiotic fungi of plants, insects and humans and found more than eight orders of variation in spore size. Evolutionary transitions in symbiotic status correlated with shifts in spore size, but the strength of this effect varied widely among phyla. Symbiotic status explained more variation than climatic variables in the current distribution of spore sizes of plant-associated fungi at a global scale while the dispersal potential of their spores is more restricted compared to free-living fungi. Our work advances life-history theory by highlighting how the interaction between symbiosis and offspring morphology shapes the reproductive and dispersal strategies among living forms.

Global patterns in endemicity and vulnerability of soil fungi.

Fungi are highly diverse organisms, which provide multiple ecosystem services. However, compared with charismatic animals and plants, the distribution patterns and conservation needs of fungi have been little explored. Here, we examined endemicity patterns, global change vulnerability and conservation priority areas for functional groups of soil fungi based on six global surveys using a high-resolution, long-read metabarcoding approach. We found that the endemicity of all fungi and most functional groups peaks in tropical habitats, including Amazonia, Yucatan, West-Central Africa, Sri Lanka, and New Caledonia, with a negligible island effect compared with plants and animals. We also found that fungi are predominantly vulnerable to drought, heat and land-cover change, particularly in dry tropical regions with high human population density. Fungal conservation areas of highest priority include herbaceous wetlands, tropical forests, and woodlands. We stress that more attention should be focused on the conservation of fungi, especially root symbiotic arbuscular mycorrhizal and ectomycorrhizal fungi in tropical regions as well as unicellular early-diverging groups and macrofungi in general. Given the low overlap between the endemicity of fungi and macroorganisms, but high conservation needs in both groups, detailed analyses on distribution and conservation requirements are warranted for other microorganisms and soil organisms.

Distance decay 2.0 - A global synthesis of taxonomic and functional turnover in ecological communities.

Aim: Understanding the variation in community composition and species abundances (i.e., ß-diversity) is at the heart of community ecology. A common approach to examine ß-diversity is to evaluate directional variation in community composition by measuring the decay in the similarity among pairs of communities along spatial or environmental distance. We provide the first global synthesis of taxonomic and functional distance decay along spatial and environmental distance by analysing 148 datasets comprising different types of organisms and environments. Location: Global. Time period: 1990 to present. Major taxa studied: From diatoms to mammals. Method: We measured the strength of the decay using ranked Mantel tests (Mantel r) and the rate of distance decay as the slope of an exponential fit using generalized linear models. We used null models to test whether functional similarity decays faster or slower than expected given the taxonomic decay along the spatial and environmental distance. We also unveiled the factors driving the rate of decay across the datasets, including latitude, spatial extent, realm and organismal features. Results: Taxonomic distance decay was stronger than functional distance decay along both spatial and environmental distance. Functional distance decay was random given the taxonomic distance decay. The rate of taxonomic and functional spatial distance decay was fastest in the datasets from mid-latitudes. Overall, datasets covering larger spatial extents showed a lower rate of decay along spatial distance but a higher rate of decay along environmental distance. Marine ecosystems had the slowest rate of decay along environmental distances. Main conclusions: In general, taxonomic distance decay is a useful tool for biogeographical research because it reflects dispersal-related factors in addition to species responses to climatic and environmental variables. Moreover, functional distance decay might be a cost-effective option for investigating community changes in heterogeneous environments.

Pluteus insidiosus Complex, Four New Species Described and Pluteus reisneri Resurrected.

We studied the taxonomy of Pluteus insidiosus and similar species using morphological and molecular (nrITS, TEF1-α) data, including a detailed study of the type collection of P. insidiosus. Based on our results, we recognize five species in this group: P. insidiosus sensu stricto and four other taxa: P. assimilatus; P. farensis; P. flavostipitatus; and P. pseudoinsidiosus; described here as new. All these taxa are distinct from each other based on molecular data, but some of them are semi-cryptic based on morphology and co-occur in the Palaearctic region. An additional molecular lineage, phylogenetically separates from the P. insidiosus complex, but with many morphological similarities, was recognized in the molecular phylogenies. Based on the revision of available type collections, the name Pluteus reisneri Velen., was adopted for this Clade. Pluteus reisneri was validly published in 1921, but it has barely been used since its original description. A modern epitype, with molecular data, was selected for P. reisneri.

Automatic Fungi Recognition: Deep Learning Meets Mycology.

The article presents an AI-based fungi species recognition system for a citizen-science community. The system's real-time identification too - FungiVision - with a mobile application front-end, led to increased public interest in fungi, quadrupling the number of citizens collecting data. FungiVision, deployed with a human-in-the-loop, reaches nearly 93% accuracy. Using the collected data, we developed a novel fine-grained classification dataset - Danish Fungi 2020 (DF20) - with several unique characteristics: species-level labels, a small number of errors, and rich observation metadata. The dataset enables the testing of the ability to improve classification using metadata, e.g., time, location, habitat and substrate, facilitates classifier calibration testing and finally allows the study of the impact of the device settings on the classification performance. The continual flow of labelled data supports improvements of the online recognition system. Finally, we present a novel method for the fungi recognition service, based on a Vision Transformer architecture. Trained on DF20 and exploiting available metadata, it achieves a recognition error that is 46.75% lower than the current system. By providing a stream of labeled data in one direction, and an accuracy increase in the other, the collaboration creates a virtuous cycle helping both communities.

First Evidence That Nematode Communities in Deadwood Are Related to Tree Species Identity and to Co-Occurring Fungi and Prokaryotes.

Nematodes represent a diverse and ubiquitous group of metazoans in terrestrial environments. They feed on bacteria, fungi, plants, other nematodes or parasitize a variety of animals and hence may be considered as active members of many food webs. Deadwood is a structural component of forest ecosystems which harbors many niches for diverse biota. As fungi and bacteria are among the most prominent decomposing colonizers of deadwood, we anticipated frequent and diverse nematode populations to co-occur in such ecosystems. However, knowledge about their ability to colonize this habitat is still limited. We applied DNA-based amplicon sequencing (metabarcoding) of the 18S rRNA gene to analyze nematode communities in sapwood and heartwood of decaying logs from 13 different tree species. We identified 247 nematode ASVs (amplicon sequence variants) from 27 families. Most of these identified families represent bacterial and fungal feeders. Their composition strongly depended on tree species identity in both wood compartments. While pH and water content were the only wood properties that contributed to nematodes' distribution, co-occurring fungal and prokaryotic (bacteria and archaea) α- and ß-diversities were significantly related to nematode communities. By exploring thirteen different tree species, which exhibit a broad range of wood characteristics, this study provides first and comprehensive insights into nematode diversity in deadwood of temperate forests and indicates connectivity to other wood-inhabiting organisms.

Detecting flying insects using car nets and DNA metabarcoding.

Monitoring insects across space and time is challenging, due to their vast taxonomic and functional diversity. This study demonstrates how nets mounted on rooftops of cars (car nets) and DNA metabarcoding can be applied to sample flying insect richness and diversity across large spatial scales within a limited time period. During June 2018, 365 car net samples were collected by 151 volunteers during two daily time intervals on 218 routes in Denmark. Insect bulk samples were processed with a DNA metabarcoding protocol to estimate taxonomic composition, and the results were compared to known flying insect richness and occurrence data. Insect and hoverfly richness and diversity were assessed across biogeographic regions and dominant land cover types. We detected 15 out of 19 flying insect orders present in Denmark, with high proportions of especially Diptera compared to Danish estimates, and lower insect richness and diversity in urbanized areas. We detected 319 species not known for Denmark and 174 species assessed in the Danish Red List. Our results indicate that the methodology can assess the flying insect fauna at large spatial scales to a wide extent, but may be, like other methods, biased towards certain insect orders.

European mushroom assemblages are darker in cold climates.

Thermal melanism theory states that dark-colored ectotherm organisms are at an advantage at low temperature due to increased warming. This theory is generally supported for ectotherm animals, however, the function of colors in the fungal kingdom is largely unknown. Here, we test whether the color lightness of mushroom assemblages is related to climate using a dataset of 3.2 million observations of 3,054 species across Europe. Consistent with the thermal melanism theory, mushroom assemblages are significantly darker in areas with cold climates. We further show differences in color phenotype between fungal lifestyles and a lifestyle differentiated response to seasonality. These results indicate a more complex ecological role of mushroom colors and suggest functions beyond thermal adaption. Because fungi play a crucial role in terrestrial carbon and nutrient cycles, understanding the links between the thermal environment, functional coloration and species' geographical distributions will be critical in predicting ecosystem responses to global warming.

Open-source data reveal how collections-based fungal diversity is sensitive to global change.

PREMISE OF THE STUDY: Fungal diversity (richness) trends at large scales are in urgent need of investigation, especially through novel situations that combine long-term observational with environmental and remotely sensed open-source data. METHODS: We modeled fungal richness, with collections-based records of saprotrophic (decaying) and ectomycorrhizal (plant mutualistic) fungi, using an array of environmental variables across geographical gradients from northern to central Europe. Temporal differences in covariables granted insight into the impacts of the shorter- versus longer-term environment on fungal richness. RESULTS: Fungal richness varied significantly across different land-use types, with highest richness in forests and lowest in urban areas. Latitudinal trends supported a unimodal pattern in diversity across Europe. Temperature, both annual mean and range, was positively correlated with richness, indicating the importance of seasonality in increasing richness amounts. Precipitation seasonality notably affected saprotrophic fungal diversity (a unimodal relationship), as did daily precipitation of the collection day (negatively correlated). Ectomycorrhizal fungal richness differed from that of saprotrophs by being positively associated with tree species richness. DISCUSSION: Our results demonstrate that fungal richness is strongly correlated with land use and climate conditions, especially concerning seasonality, and that ongoing global change processes will affect fungal richness patterns at large scales.

Explaining European fungal fruiting phenology with climate variability.

Here we assess the impact of geographically dependent (latitude, longitude, and altitude) changes in bioclimatic (temperature, precipitation, and primary productivity) variability on fungal fruiting phenology across Europe. Two main nutritional guilds of fungi, saprotrophic and ectomycorrhizal, were further separated into spring and autumn fruiters. We used a path analysis to investigate how biogeographic patterns in fungal fruiting phenology coincided with seasonal changes in climate and primary production. Across central to northern Europe, mean fruiting varied by approximately 25 d, primarily with latitude. Altitude affected fruiting by up to 30 d, with spring delays and autumnal accelerations. Fruiting was as much explained by the effects of bioclimatic variability as by their large-scale spatial patterns. Temperature drove fruiting of autumnal ectomycorrhizal and saprotrophic groups as well as spring saprotrophic groups, while primary production and precipitation were major drivers for spring-fruiting ectomycorrhizal fungi. Species-specific phenology predictors were not stable, instead deviating from the overall mean. There is significant likelihood that further climatic change, especially in temperature, will impact fungal phenology patterns at large spatial scales. The ecological implications are diverse, potentially affecting food webs (asynchrony), nutrient cycling and the timing of nutrient availability in ecosystems.

Fungal spore diversity reflects substrate-specific deposition challenges.

Sexual spores are important for the dispersal and population dynamics of fungi. They show remarkable morphological diversity, but the underlying forces driving spore evolution are poorly known. We investigated whether trophic status and substrate associations are associated with morphology in 787 macrofungal genera. We show that both spore size and ornamentation are associated with trophic specialization, so that large and ornamented spores are more probable in ectomycorrhizal than in saprotrophic genera. This suggests that spore ornamentation facilitates attachment to arthropod vectors, which ectomycorrhizal species may need to reach lower soil layers. Elongated spore shapes are more common in saprotrophic taxa, and genera associated with above ground substrates are more likely to have allantoid (curved elongated) spores, probably to lower the risk of wash out by precipitation. Overall, our results suggest that safe arrival on specific substrates is a more important driver of evolution in spore morphology than dispersal per se.

Are ungulates in forests concerns or key species for conservation and biodiversity? Reply to Boulanger et al. (DOI: 10.1111/gcb.13899).

Increasing species richness of light demanding species in forests may not be a conservation concern if we accept a macroecological and evolutionary baseline for biodiversity. Most of the current biodiversity in Europe has evolved in the Pleistocene or earlier, and in ecosystems markedly influenced by dynamic natural processes, including grazing. Many threatened species are associated with high-light forest environments such as forest glades and edges, as these have strongly declined at least partially due to the decline of large herbivores in European forests. Hence, moderate grazing in forests should be an ecological baseline and conservation target rather than a concern.

Dataset on species incidence, species richness and forest characteristics in a Danish protected area.

The data presented in this article are related to the research article entitled "Restoring hydrology and old-growth structures in a former production forest: Modelling the long-term effects on biodiversity" (A. Mazziotta, J. Heilmann-Clausen, H. H.Bruun, Ö. Fritz, E. Aude, A.P. Tøttrup) [1]. This article describes how the changes induced by restoration actions in forest hydrology and structure alter the biodiversity value of a Danish forest reserve. The field dataset is made publicly available to enable critical or extended analyses.

Citizen science data reveal ecological, historical and evolutionary factors shaping interactions between woody hosts and wood-inhabiting fungi.

Woody plants host diverse communities of associated organisms, including wood-inhabiting fungi. In this group, host effects on species richness and interaction network structure are not well understood, especially not at large geographical scales. We investigated ecological, historical and evolutionary determinants of fungal species richness and network modularity, that is, subcommunity structure, across woody hosts in Denmark, using a citizen science data set comprising > 80 000 records of > 1000 fungal species on 91 genera of woody plants. Fungal species richness was positively related to host size, wood pH, and the number of species in the host genus, with limited influence of host frequency and host history, that is, time since host establishment in the area. Modularity patterns were unaffected by host history, but largely reflected host phylogeny. Notably, fungal communities differed substantially between angiosperm and gymnosperm hosts. Host traits and evolutionary history appear to be more important than host frequency and recent history in structuring interactions between hosts and wood-inhabiting fungi. High wood acidity appears to act as a stress factor reducing fungal species richness, while large host size, providing increased niche diversity, enhances it. In some fungal groups that are known to interact with live host cells in the establishment phase, host selectivity is common, causing a modular community structure.

A fungal perspective on conservation biology.

Hitherto fungi have rarely been considered in conservation biology, but this is changing as the field moves from addressing single species issues to an integrative ecosystem-based approach. The current emphasis on biodiversity as a provider of ecosystem services throws the spotlight on the vast diversity of fungi, their crucial roles in terrestrial ecosystems, and the benefits of considering fungi in concert with animals and plants. We reviewed the role of fungi in ecosystems and composed an overview of the current state of conservation of fungi. There are 5 areas in which fungi can be readily integrated into conservation: as providers of habitats and processes important for other organisms; as indicators of desired or undesired trends in ecosystem functioning; as indicators of habitats of conservation value; as providers of powerful links between human societies and the natural world because of their value as food, medicine, and biotechnological tools; and as sources of novel tools and approaches for conservation of megadiverse organism groups. We hope conservation professionals will value the potential of fungi, engage mycologists in their work, and appreciate the crucial role of fungi in nature.

Population evidence of cryptic species and geographical structure in the cosmopolitan ectomycorrhizal fungus, Tricholoma scalpturatum.

Tricholoma scalpturatum is an ectomycorrhizal fungus that forms symbioses with roots of diverse trees and shrubs. It is commonly encountered in a wide range of habitats, across temperate ecosystems. A previous study has revealed a high genetic diversity at a local scale, and ruderal abilities. To examine genetic structure at a large geographical scale, a total of 164 basidiocarps were collected from 30 populations located in Western Europe, from Spain to Scandinavia. These samples were analyzed by three molecular methods with different levels of resolution: inter-simple sequence repeats (ISSRs), restriction fragment length polymorphisms (RFLPs) in the rDNA internal transcribed spacer (ITS), and ITS sequence analysis. Considerable genetic variation was found, and the morphospecies was separated into two genetic groups that were distinct from each other. The ISSR data and the relatively low percentage value (96%) of shared sequence polymorphisms in the ITS between isolates from the two groups, strongly suggest cryptic species and long-lasting separation. No geographical exclusion was detected for these two widely distributed taxa. However, high estimates of population differentiation were observed in each group, including between populations less than a few kilometers apart. This result provides evidence for limited gene flow and/or founding effects. It also indicates that T. scalpturatum does not constitute a random mating population, and the hypothesis of endemism cannot be excluded for this cosmopolitan wind-dispersed fungus.