Airborne DNA reveals predictable spatial and seasonal dynamics of fungi.

Fungi are among the most diverse and ecologically important kingdoms in life. However, the distributional ranges of fungi remain largely unknown as do the ecological mechanisms that shape their distributions1,2. To provide an integrated view of the spatial and seasonal dynamics of fungi, we implemented a globally distributed standardized aerial sampling of fungal spores3. The vast majority of operational taxonomic units were detected within only one climatic zone, and the spatiotemporal patterns of species richness and community composition were mostly explained by annual mean air temperature. Tropical regions hosted the highest fungal diversity except for lichenized, ericoid mycorrhizal and ectomycorrhizal fungi, which reached their peak diversity in temperate regions. The sensitivity in climatic responses was associated with phylogenetic relatedness, suggesting that large-scale distributions of some fungal groups are partially constrained by their ancestral niche. There was a strong phylogenetic signal in seasonal sensitivity, suggesting that some groups of fungi have retained their ancestral trait of sporulating for only a short period. Overall, our results show that the hyperdiverse kingdom of fungi follows globally highly predictable spatial and temporal dynamics, with seasonality in both species richness and community composition increasing with latitude. Our study reports patterns resembling those described for other major groups of organisms, thus making a major contribution to the long-standing debate on whether organisms with a microbial lifestyle follow the global biodiversity paradigms known for macroorganisms4,5.

Global Spore Sampling Project: A global, standardized dataset of airborne fungal DNA.

Novel methods for sampling and characterizing biodiversity hold great promise for re-evaluating patterns of life across the planet. The sampling of airborne spores with a cyclone sampler, and the sequencing of their DNA, have been suggested as an efficient and well-calibrated tool for surveying fungal diversity across various environments. Here we present data originating from the Global Spore Sampling Project, comprising 2,768 samples collected during two years at 47 outdoor locations across the world. Each sample represents fungal DNA extracted from 24 m3 of air. We applied a conservative bioinformatics pipeline that filtered out sequences that did not show strong evidence of representing a fungal species. The pipeline yielded 27,954 species-level operational taxonomic units (OTUs). Each OTU is accompanied by a probabilistic taxonomic classification, validated through comparison with expert evaluations. To examine the potential of the data for ecological analyses, we partitioned the variation in species distributions into spatial and seasonal components, showing a strong effect of the annual mean temperature on community composition.

Spatial trade-offs between ecological and economical sustainability in the boreal production forest.

Economically-oriented forestry aims to sustain timber harvest revenues, while ecologically-oriented management supplies suitable habitat for species using deadwood as primary habitat. As these objectives are conflicting, planning for economic and ecological sustainability involves compromise and trade-offs. We analyze the spatial trade-offs between the economic value from timber harvesting and the volume of deadwood in the boreal forest. We assess these trade-offs from three perspectives: (1) landscape characteristics, affected by conservation strategies; (2) forest management promoting either economic or ecological values; (3) uncertainty in inventory errors undermining the estimate of the two sustainability objectives. To reveal the tradeoffs between the forest economic and ecological values we simulated and optimized a production landscape in Finland 30 years into the future accounting for uncertainty in biomass and deadwood inventories. We found that, with a limited reduction in timber harvesting (7%), (i) the amount of deadwood increased more in non-aggregated (45%) than in aggregated (16%) stands, (ii) constraining stands in adjacent areas further increased deadwood (21%) respect to the matrix and (iii) 7% of connected stand area harbored ≥20 m3/ha deadwood supporting survival of near-threatened species. Our results demonstrate that the structure of the landscape for biodiversity can be improved with limited economic losses. However, improving habitat configuration requires larger economic losses than only increasing habitat amount, but its ecological benefits are larger both for common and red-listed species. We found that management oriented towards stand aggregation not only creates connected areas with high deadwood of high value biodiversity but also improves the value of the whole matrix by decreasing intensive timber harvesting and energy wood collection. Finally, we found that uncertainties alter the estimate of the potential of the forest landscape to supply deadwood, and this can affect the choice of management actions to allocate over the landscape. To conclude, our results demonstrate the trade-offs between economic forest use and conservation are affected differently by landscape characteristics, forest management and uncertainty in inventory errors. As such these drivers should be considered when optimizing the forest for multiple uses.

Quantifying trade-offs between ecological gains, economic costs, and landowners' preferences in boreal mire protection.

Private land often encompasses biodiversity features of high conservation value, but its protection is not straightforward. Commonly, landowners' perspectives are rightfully allowed to influence conservation actions. This unlikely comes without consequences on biodiversity or other aspects such as economic considerations, but these consequences are rarely quantitatively considered in decision-making. In the context of boreal mire protection in Finland, we report how acknowledging landowners' resistance to protection changes the combination of mires selected to conservation compared to ignoring landowners' opinions. Using spatial prioritization, we quantify trade-offs arising between the amount of landowners' resistance, protected biodiversity, and financial costs in different conservation scenarios. Results show that the trade-offs cannot be fully avoided. Nevertheless, we show that the systematic examination of the trade-offs opens up options to alleviate them. This can promote the evaluation of different conservation policy outcomes, enabling better-informed conservation decisions and more effective and socially sustainable allocation of conservation resources.

No evidence of systematic pre-emptive loggings after notifying landowners of their lands' conservation potential.

Landowners can intentionally impair biodiversity values occurring on their land to pre-empt biodiversity protection. This often leads to significant negative effects on biodiversity. We studied whether landowners in Finland engaged in pre-emptive loggings after they were notified that their wooded mires are candidate sites for a mire protection program. After the notification, harvesting rates of the candidate wooded mires were significantly lower compared to harvesting rates of similar but non-candidate wooded mires. Annual and monthly harvesting rates indicated that notifying landowners of the conservation potential did not launch systematic pre-emptive logging behavior. Nevertheless, part of the candidate wooded mires were logged, so some landowners place more weight on other values than the biodiversity ones. Pre-emptive behavior has been observed in other studies suggesting that many country- or system-specific factors such as cultural background or level of compensation can affect landowners' behavior.

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.

Give me a sample of air and I will tell which species are found from your region: Molecular identification of fungi from airborne spore samples.

Fungi are a megadiverse group of organisms, they play major roles in ecosystem functioning and are important for human health, food production and nature conservation. Our knowledge on fungal diversity and fungal ecology is however still very limited, in part because surveying and identifying fungi is time demanding and requires expert knowledge. We present a method that allows anyone to generate a list of fungal species likely to occur in a region of interest, with minimal effort and without requiring taxonomical expertise. The method consists of using a cyclone sampler to acquire fungal spores directly from the air to an Eppendorf tube, and applying DNA barcoding with probabilistic species identification to generate a list of species from the sample. We tested the feasibility of the method by acquiring replicate air samples from different geographical regions within Finland. Our results show that air sampling is adequate for regional-level surveys, with samples collected >100 km apart varying but samples collected <10 km apart not varying in their species composition. The data show marked phenology, and thus obtaining a representative species list requires aerial sampling that covers the entire fruiting season. In sum, aerial sampling combined with probabilistic molecular species identification offers a highly effective method for generating a species list of air-dispersing fungi. The method presented here has the potential to revolutionize fungal surveys, as it provides a highly cost-efficient way to include fungi as a part of large-scale biodiversity assessments and monitoring programs.

Grazing and abandonment determine different tree dynamics in wood-pastures.

Wood-pastures are threatened biotopes in which trees and livestock grazing maintain high conservation values. However, browsing may threaten tree regeneration, whereas abandonment leads to tree encroachment. We studied the regeneration of trees in a grazed and abandoned boreal wood-pastures. In grazed sites, the density of young spruces (Picea abies) was high, while the density of young birches (Betula spp.) was very low. Sprucification can be prevented only by removing spruces. The number of young birches and pines (Pinus sylvestris) was correlated with the number of junipers (Juniperus communis), probably because thorny junipers protect palatable seedlings from browsing. In abandoned sites, deciduous trees and spruces regenerated abundantly. In the long term, both grazing and abandonment lead to changes in tree species compositions and low diversity wood-pastures. Landscape scale planning and disturbance dynamics are needed for the creation of new wood-pastures and the maintenance of all pasture types within the landscape.

The role of novel forest ecosystems in the conservation of wood-inhabiting fungi in boreal broadleaved forests.

The increasing human impact on the earth's biosphere is inflicting changes at all spatial scales. As well as deterioration and fragmentation of natural biological systems, these changes also led to other, unprecedented effects and emergence of novel habitats. In boreal zone, intensive forest management has negatively impacted a multitude of deadwood-associated species. This is especially alarming given the important role wood-inhabiting fungi have in the natural decay processes. In the boreal zone, natural broad-leaved-dominated, herb-rich forests are threatened habitats which have high wood-inhabiting fungal species richness. Fungal diversity in other broadleaved forest habitat types is poorly known. Traditional wood pastures and man-made afforested fields are novel habitats that could potentially be important for wood-inhabiting fungi. This study compares species richness and fungal community composition across the aforementioned habitat types, based on data collected for wood-inhabiting fungi occupying all deadwood diameter fractions. Corticioid and polyporoid fungi were surveyed from 67 130 deadwood particles in four natural herb-rich forests, four birch-dominated wood pastures, and four birch-dominated afforested field sites in central Finland. As predicted, natural herb-rich forests were the most species-rich habitat. However, afforested fields also had considerably higher overall species richness than wood pastures. Many rare or rarely collected species were detected in each forest type. Finally, fungal community composition showed some divergence not only among the different habitat types, but also among deadwood diameter fractions. Synthesis and applications: In order to maintain biodiversity at both local and regional scales, conserving threatened natural habitat types and managing traditional landscapes is essential. Man-made secondary woody habitats could provide the necessary resources and serve as surrogate habitats for many broadleaved deadwood-associated species, and thus complement the existing conservation network of natural forests.

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.

Community turnover of wood-inhabiting fungi across hierarchical spatial scales.

For efficient use of conservation resources it is important to determine how species diversity changes across spatial scales. In many poorly known species groups little is known about at which spatial scales the conservation efforts should be focused. Here we examined how the community turnover of wood-inhabiting fungi is realised at three hierarchical levels, and how much of community variation is explained by variation in resource composition and spatial proximity. The hierarchical study design consisted of management type (fixed factor), forest site (random factor, nested within management type) and study plots (randomly placed plots within each study site). To examine how species richness varied across the three hierarchical scales, randomized species accumulation curves and additive partitioning of species richness were applied. To analyse variation in wood-inhabiting species and dead wood composition at each scale, linear and Permanova modelling approaches were used. Wood-inhabiting fungal communities were dominated by rare and infrequent species. The similarity of fungal communities was higher within sites and within management categories than among sites or between the two management categories, and it decreased with increasing distance among the sampling plots and with decreasing similarity of dead wood resources. However, only a small part of community variation could be explained by these factors. The species present in managed forests were in a large extent a subset of those species present in natural forests. Our results suggest that in particular the protection of rare species requires a large total area. As managed forests have only little additional value complementing the diversity of natural forests, the conservation of natural forests is the key to ecologically effective conservation. As the dissimilarity of fungal communities increases with distance, the conserved natural forest sites should be broadly distributed in space, yet the individual conserved areas should be large enough to ensure local persistence.

Bryophyte species richness on retention aspens recovers in time but community structure does not.

Green-tree retention is a forest management method in which some living trees are left on a logged area. The aim is to offer 'lifeboats' to support species immediately after logging and to provide microhabitats during and after forest re-establishment. Several studies have shown immediate decline in bryophyte diversity after retention logging and thus questioned the effectiveness of this method, but longer term studies are lacking. Here we studied the epiphytic bryophytes on European aspen (Populus tremula L.) retention trees along a 30-year chronosequence. We compared the bryophyte flora of 102 'retention aspens' on 14 differently aged retention sites with 102 'conservation aspens' on 14 differently aged conservation sites. We used a Bayesian community-level modelling approach to estimate the changes in bryophyte species richness, abundance (area covered) and community structure during 30 years after logging. Using the fitted model, we estimated that two years after logging both species richness and abundance of bryophytes declined, but during the following 20-30 years both recovered to the level of conservation aspens. However, logging-induced changes in bryophyte community structure did not fully recover over the same time period. Liverwort species showed some or low potential to benefit from lifeboating and high potential to re-colonise as time since logging increases. Most moss species responded similarly, but two cushion-forming mosses benefited from the logging disturbance while several weft- or mat-forming mosses declined and did not re-colonise in 20-30 years. We conclude that retention trees do not function as equally effective lifeboats for all bryophyte species but are successful in providing suitable habitats for many species in the long-term. To be most effective, retention cuts should be located adjacent to conservation sites, which may function as sources of re-colonisation and support the populations of species that require old-growth forests.

Quantifying the indicator power of an indicator species.

Biodiversity indicator species are needed for classifying biotopes and sites for conservation, and a number of methods have been developed for determining indicator species for this purpose. Nevertheless, in addition to site classification, there is sometimes a need to define an indicator species that indicates the occurrence of another species. For example, when a species of interest (target species) is difficult to detect or identify, a reliable indicator species can function as a tool that saves time and money. We derived a method that provides a quantitative measure of the indicator power (IP) of an indicator species for the target species or any species assemblage. We calculated the measure of IP from a presence-absence matrix that covered several sites. The method provided a list of indicator species, the presence of which reliably indicated the presence of another species (e.g., a threatened or rare species in a given area). The IP of the species was highest when the number of shared occurrences between the indicator species and the target species was high and, simultaneously, when the indicator species and the target species occurred separately in only a few cases. The IP was also positively influenced by the number of sites with no occurrences of either the indicator or the target species. Our method can also be used to quantify different types of species occurrence indications. We refer to these types as presence-presence, presence-absence, absence-presence, and absence-absence indications. To clarify the use of the method, we examined the situation with red-listed polypores in White-backed Woodpecker (Dendrocopos leucotos) habitats in Fennoscandia and found some suitable indicator species. Our method provides a new, objective way to evaluate the IP of an indicator species.

Color signals in the black grouse (Tetrao tetrix): signal properties and their condition dependency.

Recent progress in techniques of quantifying between-individual differences of color-based ornaments has revealed undiscovered possibilities for research in sexual selection. We present how the color spectra data can be comprehensively used for studying the importance of sexual ornaments in the black grouse and how these ornaments are related to a male condition. For this, we used both correlative field and experimental data. Field data indicated that older males had more chromatic coloration than yearlings. Blue chroma of males was correlated with male mating success. We experimentally manipulated yearling birds with testosterone implants and found that testosterone-implanted males had impaired expression of several sexual ornaments: 10 months after the implantation, both structural-based blue and carotenoid-based red eye comb coloration were diminished, as well as lyre (tail) length. However, the manipulation did not affect vital traits under natural selection (wing length or body mass). Our data indicate that structural color is an important trait in sexual selection in this lekking species. Importantly, the data also indicate that male sexual ornaments are more susceptible to environmental conditions than the other male traits, thus showing their heightened condition dependency compared with the other traits mediating the honesty of signaling.