Anders Dahlberg

Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest

Forest Fungi Boreal forest is one of the worlds major biomes, dominating the subarctic northern latitudes of Europe, Asia, and America. The soils of boreal forest function as a net sink in the global carbon cycle and, hitherto, it has been thought that organic matter in this sink primarily accumulates in the form of plant remains. Clemmensen et al. (p. 1615; see the Perspective by Treseder and Holden) now show that most of the stored carbon in boreal forested islands in Sweden is in fact derived from mycorrhizal mycelium rather than from plant litter. Biochemical and sequencing studies show that carbon sequestration is regulated by functional and phylogenetic shifts in the mycorrhizal fungal community. The results will need to be explicitly considered in models of the role of the boreal forest in the global carbon cycle. Reservoirs of carbon in boreal forest soils are revisited in an island chronosequence, using modeling and molecular approaches. [Also see Perspective by Treseder and Holden] Boreal forest soils function as a terrestrial net sink in the global carbon cycle. The prevailing dogma has focused on aboveground plant litter as a principal source of soil organic matter. Using 14C bomb-carbon modeling, we show that 50 to 70% of stored carbon in a chronosequence of boreal forested islands derives from roots and root-associated microorganisms. Fungal biomarkers indicate impaired degradation and preservation of fungal residues in late successional forests. Furthermore, 454 pyrosequencing of molecular barcodes, in conjunction with stable isotope analyses, highlights root-associated fungi as important regulators of ecosystem carbon dynamics. Our results suggest an alternative mechanism for the accumulation of organic matter in boreal forests during succession in the long-term absence of disturbance.

Ectomycorrhizal fungal communities in late‐successional Swedish boreal forests, and their composition following wildfire

This study was conducted to evaluate the effects of wildfires on ectomycorrhizal (EM) fungal communities in Scots pine (Pinus sylvestris) stands. Below‐ and above‐ground communities were analysed in terms of species richness and evenness by examining mycorrhizas and sporocarps in a chronosequence of burned stands in comparison with adjacent unburned late‐successional stands. The internal transcribed spacer (ITS)‐region (rDNA) of mycobionts from single mycorrhizas was digested with three restriction enzymes and compared with an ITS–restriction fragment length polymorphism (RFLP) reference database of EM sporocarps. Spatial variation seemed to be more prominent than the effects of fire on the EM fungal species composition. Most of the common species tended to be found in all sites, suggesting that EM fungal communities show a high degree of continuity following low‐intensity wildfires. Species richness was not affected by fire, whereas the evenness of species distributions of mycorrhizas was lower in the burned stands. The diversity of EM fungi was relatively high considering that there were only three EM tree species present in the stands. In total, 135 EM taxa were identified on the basis of their RFLP patterns; 66 species were recorded as sporocarps, but only 11 of these were also recorded as mycorrhizas. The species composition of the below‐ground community of EM fungi did not reflect that of the sporocarps produced. EM fungal species present in our ITS–RFLP reference database accounted for 54–99% of the total sporocarp production in the stands, but only 0–32% of the mycorrhizal abundance.

Carbon sequestration is related to mycorrhizal fungal community shifts during long‐term succession in boreal forests

Boreal forest soils store a major proportion of the global terrestrial carbon (C) and below-ground inputs contribute as much as above-ground plant litter to the total C stored in the soil. A better understanding of the dynamics and drivers of root-associated fungal communities is essential to predict long-term soil C storage and climate feedbacks in northern ecosystems. We used 454-pyrosequencing to identify fungal communities across fine-scaled soil profiles in a 5000 yr fire-driven boreal forest chronosequence, with the aim of pinpointing shifts in fungal community composition that may underlie variation in below-ground C sequestration. In early successional-stage forests, higher abundance of cord-forming ectomycorrhizal fungi (such as Cortinarius and Suillus species) was linked to rapid turnover of mycelial biomass and necromass, efficient nitrogen (N) mobilization and low C sequestration. In late successional-stage forests, cord formers declined, while ericoid mycorrhizal ascomycetes continued to dominate, potentially facilitating long-term humus build-up through production of melanized hyphae that resist decomposition. Our results suggest that cord-forming ectomycorrhizal fungi and ericoid mycorrhizal fungi play opposing roles in below-ground C storage. We postulate that, by affecting turnover and decomposition of fungal tissues, mycorrhizal fungal identity and growth form are critical determinants of C and N sequestration in boreal forests.

Diversity and abundance of resupinate thelephoroid fungi as ectomycorrhizal symbionts in Swedish boreal forests.

Resupinate thelephoroid fungi (hereafter called tomentelloid fungi) have a world‐wide distribution and comprise ≈70 basidiomycete species with inconspicuous, resupinate sporocarps. It is only recently that their ability to form ectomycorrhizas (EM) has been realized, so their distribution, abundance and significance as mycobionts in forest ecosystems is still largely unexplored. In order to provide baseline data for future ecological studies of tomentelloid fungi, we explored their presence and abundance in nine Swedish boreal forests in which the EM communities had been analysed. Phylogenetic analyses were used to compare the internal transcribed spacer of nuclear ribosomal DNA (ITS rDNA) sequence data obtained from mycobionts on single ectomycorrhizal tips with that obtained from sporocarps of identified tomentelloid fungi. Five species of Tomentella and one species of Pseudotomentella were identified as ectomycorrhizal fungi. The symbiotic nature of Tomentella bryophila, T. stuposa, T. badia and T. atramentaria is demonstrated for the first time. T. stuposa and Pseudotomentellatristis were the most commonly encountered tomentelloid fungi, with the other species, including T. sublilacina, only being recorded from single stands. Overall, tomentelloid fungi were found in five of the studies, colonizing between 1 and 8% of the mycorrhizal root tips. Two of the five sites supported several tomentelloid species. Tomentelloid fungi appear to be relatively common ectomycorrhizal symbionts with a wide distribution in Swedish coniferous forests. The results are in accordance with accumulating data that fungal species which lack conspicuous sporocarps may be of considerable importance in EM communities.

Effects of Plant Litter Species Composition and Diversity on the Boreal Forest Plant-Soil System

Although most plant products eventually enter the below-ground subsystem as plant litter, relatively little is known about the effects of plant litter diversity or composition on ecosystem processes and no study has considered the responses of plant growth to these factors. We conducted an experiment in which humus substrate was collected from three field sites in the boreal forest of northern Sweden. Litter was then placed on the humus surface, and the litter used consisted of monocultures of Empetrum hermaphroditum (dwarf shrub), Betula pendula (tree), and Pleurozium schreberi (feather moss), as well as mixtures containing all the possible (two-way and three-way) combinations of these species: the experiment was maintained in out-door conditions. Although decomposition rates of this surface-placed litter differed between species few effects of litter mixing on litter mass loss were apparent. Added litter of Pinus sylvestris litter broke down most slowly when placed in E. hermaphrodnum litter but sometimes showed elevated decomposition rates when placed in some of the multiple species litter mixes. Soil microbial biomass and activity was lowest when plant litter was absent, but as long as plant litter was present on the humus surface the species composition and diversity of the litter was irrelevant. There were few effects of litter treatments on growth of seedlings of either B. pendula or P. sylvestris planted into the humus. However, for one site there were significant effects of mixing litter of P. sclueberi and E. hermaphroditum in reducing growth of both seedling species. Litter treatments generally did not alter the competitive balance between B. pendula and P. sylvestris seedlings when grown together but for all sites litter treatments had significant effects on the overall intensity of competition, and mixing of litter of B. pendula and P. sehreheri had significant non-additive effects on competition intensity for two of the three sites. The abundance of mycorrhizae on seedlings was only weakly related to litter treatment but there were some positive effects of litter mixing on one of the most abundant mycorrhizal morphotypes on both species of seedlings for one of the sites. Our results suggest that litter presence was important in influencing a range of above ground and below ground properties and processes. In some instances individual species effects and litter mixing effects were also important but few general patterns emerged, and the nature of significant effects tended to be idiosyneratic. Ultimately our results show that plant litter has important afterlife effects which need to be considered in order to develop a more complete understanding of how biodiversity affects ecosystems.

Interference mechanisms in conifer-Ericaceae-feathermoss communities

In northern boreal forests ground level species occur which may have the capacity to suppress tree seedling regeneration substantially, particularly in late successional stages. We investigated, through an experiment involving sequential manipulations, the effects of three biotic components operating at the ground layer, i.e. aboveground effects of the ericaceous shrub Empetrum hermaphroditum and of the feathermoss species Pleurozium schreberi and the below-ground effects of extramatrical mycorrhizal hyphae, on the seedling establishment, growth and nutrient acquisition of Pinus sylvestris during two growing seasons. Germination and seedling establishment of P. sylvestris were enhanced by reduction of the above ground components of E. hermaphroditum and P. schreberi but were not influenced by temporary disruption of mycorrhizal hyphae. Seedling growth and nitrogen content were, however, significantly increased when hyphal connections were disrupted and above ground influence of P. schreberi and E. hermaphroditum were reduced. Higher shoot:root ratios were also found in seedlings when hyphal connections were disrupted. Seedlings in treatments where P. schreberi was left intact and above ground interference by E. hermaphroditum was reduced had unusually low shoot:root ratios (1.6) after two growing seasons and significantly lower total amounts of nutrients after one growing season than were initially present in the seeds, indicative of a net nutrient drain during the early establishment phase. The experiment could not explain the mechanisms behind this unexpected nutrient drain. Possible rhizosphere interactions immobilizing nutrients and causing seedling nutrient losses are discussed. From the results of this study and other indirect evidence we hypothesize that the three biotic components we investigated could act together to immobilize nutrients and to inhibit tree seedling regeneration and growth in late successional stages of boreal forests.

Patterns of fungal communities among and within decaying logs, revealed by 454 sequencing.

Owing to previous methodological limitations, knowledge about the fine‐scale distribution of fungal mycelia in decaying logs is limited. We investigated fungal communities in decaying Norway spruce logs at various spatial scales at two environmentally different locations in Sweden. On the basis of 454 pyrosequencing of the ITS2 region of rDNA, 1914 operational taxonomic units (OTUs) were detected in 353 samples. The communities differed significantly among logs, but the physical distance between logs was not found to have a significant effect on whether fungal communities had any resemblance to each other. Within a log, samples that were closer together generally had communities that showed more resemblance to each other than those that were further apart. OTUs characteristic for particular positions on the logs could be identified. In general, these OTUs did not overlap with the most abundant OTUs, and their ecological role was often unknown. Only a few OTUs were detected in the majority of logs, whereas numerous OTUs were rare and present in only one or a few logs. Wood‐decaying Basidiomycetes were often represented by higher sequence reads in individual logs than Ascomycete OTUs, suggesting that Basidiomycete mycelia spread out more rapidly when established. OTU richness tended to increase with the decay stage of the sample; however, the known wood decayers were most abundant in less‐decomposed samples. The fungi identified in the logs represented different ecological strategies. Our findings differ from previously published sporocarp studies, indicating that the highly abundant fruiting species may respond to environment in different ways than the rest of the fungal community.

Post-fire legacy of ectomycorrhizal fungal communities in the Swedish boreal forest in relation to fire severity and logging intensity

Swedish foresters are placing increasing reliance in burning of forestland and green tree retention, in order to enhance biodiversity in the Swedish boreal forests. However, much remains to be learned about how to optimise nature conservation goals by different logging and burning procedures. We monitored the survival of ectomycorrhizal (EM) fungi as mycorrhizas, at a clear-cut, a seed tree stand and an uncut stand of Scots pine in central Sweden, with and without burning at two levels of fire severity. The abundance of mycorrhizas and the EM fungal diversity declined with increased logging intensity and with increased depth of burn. Deep burning fires in combination with logging or fire-caused tree mortality can kill much of the existing EM community. Logging intensity, fire intensity and fire severity are all factors that can be manipulated, thus changing the effects on EM fungi and other soil biota.

Population ecology of Suillus variegatus in old Swedish Scots pine forests

Spatial characteristics of Suillus variegatus populations, including the size, distribution and number of genets, were measured in four naturally regenerated stands of Scots pine, Pinus sylvestris in Sweden that were more than 100 years old. In the oldest forest, a continuous tree-layer had been present at least since the last forest fire in 1647. Genets were identified based on somatic incompatibility reactions performed on mycelial cultures from sporocarps. In total, 38 genets were identified from 120 tested sporocarps. The maximal extension of a genet, as reflected by its outermost sporocarps, was 27 m in the oldest stand and ranged between 10 and 17 m in the other stands. On average, genet size was 20 m in the oldest stand and 10 m in the other stands. Other genets were not found within the domains of established genets. The closest detected distance between genets was 1–5 m, and the average distance was 4 m. The number of genets ranged between 56 and 74 ha − at the studied sites. Possible reasons for the high degree of resemblance in characteristics in old forests between S. variegatus , the dominant bolete in mature forests, and S. bovinus when present, more a characteristic for younger forests and only scarcely occurring in older forests, are discussed.

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.