Fungal communities associated with acorn woodpeckers and their excavations

Wood-decay fungi soften wood, putatively providing opportunities for woodpeckers to excavate an otherwise hard substrate, yet the fungal community composition in tree cavities and the specificity of these relationships is largely unknown. We used high-throughput amplicon sequencing of the fungal ITS2 region to examine the fungal communities associated with acorn woodpeckers (Melanerpes formicivorus) and their cavities in mature valley oak (Quercus lobata) and blue oak (Q. douglasii) trees in an oak savannah of central coastal California, USA. Acorn woodpeckers and their excavations harbored over 1500 fungal taxa, including more than 100 putative wood-decay fungi. The fungal communities found on the birds were more similar to those found in excavated cavities than those found in trees without excavated holes. These results suggest that symbiotic associations between acorn woodpeckers and fungi are highly diverse, with low specificity. Symbiotic associations between cavity-excavators and fungi are likely more common and widespread than previously thought.     

Effect of tree host species on fungal community composition in a tropical rain forest in Panama

Abstract.  To determine whether host species influence the composition of fungal communities, the ascomycetes and basidiomycetes present on three tree species ( Prioria copaifera (Fabaceae), Quararibea asterolepis (Bombacaceae), and Trichilia tuberculata (Meliaceae)) were sampled on the 50-ha Forest Dynamics Project plot in lowland moist tropical forest on Barro Colorado Island, Panama. The most abundant fungal morphotypes of both ascomycetes and basidiomycetes were generalists found on all three hosts, but detrended correspondence analysis revealed distinct differences in fungal community composition among host trees. These differences among hosts were constant across census years. Randomization tests revealed that there were significantly fewer host-generalist fungi than expected for ascomycetes but not for basidiomycetes. These results indicate that host composition plays a role in structuring both ascomycete and basidiomycete fungal communities, but that the most successful fungal morphotypes are capable of colonizing multiple host species.     

Endophytes dominate fungal communities in six-year-old veteranisation wounds in living oak trunks

Old trees are rare in the landscape, as are many of their associated species. Veteranisation is a method by which attempts are made to create microhabitats, otherwise found only in old trees, in younger trees at an earlier stage than would occur naturally. Here, we analysed the early fungal succession in 6 y-old veteranisation wounds in ca. 100 y old living oak trunks by DNA-barcoding of the wood at eight sites in Sweden and Norway. We hypothesised basidiomycetes would be most abundant, and exposed sapwood and heartwood would select for different communities. We identified 686 fungal taxa, mainly ascomycetes, with a large overlap in species composition and surprisingly similar species richness, i.e. 325 vs. 308–360, between intact and different types of damaged wood, respectively. Endophytes continued to be present and common in damaged wood. The results demonstrate that damage to sapwood and heartwood partly select for different fungi and that 6 y is too early to evaluate if veteranisation can positively favour fungi of conservation interest.     

Do increases in the availability of standing dead trees affect the abundance,nest-site use,and niche partitioning of great spotted and middle spotted woodpeckers in riverine forests?

Standing dead trees may be a limited resource for woodpeckers in managed forests, especially for species that rely on dead wood for their nest or roost cavity, and as foraging sites. Effective conservation strategies for woodpeckers require a detailed knowledge of species’ responses to dead wood availability. To investigate the importance of standing dead wood (snags) for the abundance and nest-site use of the great spotted woodpecker Dendrocopos major and middle spotted woodpecker Leiopicus medius in mature riverine forests, we compared the responses of birds between two periods—before mass mortality, and during a pulse in standing dead trees. The density of standing dead trees available for cavity excavation by the great spotted woodpecker and the middle spotted woodpecker increased significantly during the study period: 37-fold and 4-fold, respectively. Temporal trends in the abundance of both woodpecker species from 2000 to 2015 were not significant. Great spotted woodpeckers were significantly more likely to use dead trees and places with wounds in species other than oak and ash during the outbreak period than in the pre-outbreak period. Middle spotted woodpeckers were significantly less likely to excavate cavities in tree species other than oak and ash in the outbreak period, but dead trees were more likely selected. An interspecific comparison suggests that the probability of a nest-hole having been excavated by a middle spotted woodpecker increased with a nest-hole sited in ash, in a dead tree, in a limb/branch, and decreased with a nest-hole in a closed forest. These findings suggest that woodpecker species, especially weak excavators, may benefit from an increase in dead wood availability leading to nest niche shifts into more favorable substrates for cavity excavation. However, a strong increase in dead wood availability does not modify the general pattern of niche partitioning between great spotted and middle spotted woodpeckers. Conservation plans for the specialized middle spotted woodpecker must consider the preference for dead and decaying trees. The decreasing number of large ashes and oaks, and the lack of natural regeneration of the latter species, may negatively affect the middle spotted woodpecker in the future.     

The perils of plasticity: dual resource pulses increase facilitation but destabilize populations of small‐bodied cavity‐nesters

Resource pulses within structured communities can lead to changes in the ecological roles of community members, particularly for species that exhibit plasticity in resource use. The red‐breasted nuthatch Sitta canadensis is a facultative excavating cavity‐nester that forages on seeds and insects, thus exhibits plasticity in both nesting habits and diet. In a long‐term study of cavity‐nesting vertebrates, we used point counts, and nest and vegetation surveys to examine the effects of two resource pulses of mountain pine bark beetle prey Dendroctonus ponderosae and tree cavities via excavator populations, on population densities and cavity reuse of red‐breasted nuthatches, from 1997–2006. We observed a doubling in mean nut‐hatch densities from 0.12 to 0.24 individuals ha^?1 then a collapse later in the decade to 50% below endemic levels (0.06 individuals ha^?1). These regional fluctuations were positively correlated with densities of trees recently infected by bark beetles. Because nuthatches range over large areas in winter, this regional correlation suggests that populations responded to the increase in winter food supply. At the site scale, general linear mixed effects models showed that nuthatch populations increased following years of high densities of downy woodpeckers Picoides pubescens, suggesting that downy woodpeckers were important facilitators, via cavity excavation. Type of nesting cavity used by nuthatches varied during the pulse, such that the use of existing cavities (in lieu of excavation) increased on sites that had harboured downy woodpecker nests in the previous year. We conclude that increased densities of cavity excavators allowed facultative excavators to increase their reuse of cavities, which may have contributed to the dramatic increases in nuthatch populations. However, nuthatch populations collapsed after the boom suggesting that this dual resource pulse may have destabilized populations by enabling densities to reach unsustainable levels. Thus, plasticity in resource use can have serious costs as well as benefits.     

Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie

Symbiotic associations between plants and arbuscular mycorrhizal (AM) fungi are ubiquitous in many herbaceous plant communities and can have large effects on these communities and ecosystem processes. The extent of species-specificity between these plant and fungal symbionts in nature is poorly known, yet reciprocal effects of the composition of plant and soil microbe communities is an important assumption of recent theoretical models of plant community structure. In grassland ecosystems, host plant species may have an important role in determining development and sporulation of AM fungi and patterns of fungal species composition and diversity. In this study, the effects of five different host plant species [Poa pratensis L., Sporobolus heterolepis (A. Gray) A. Gray, Panicum virgatum L., Baptisia bracteata Muhl. ex Ell., Solidago missouriensis Nutt.] on spore communities of AM fungi in tallgrass prairie were examined. Spore abundances and species composition of fungal communities of soil samples collected from patches within tallgrass prairie were significantly influenced by the host plant species that dominated the patch. The AM fungal spore community associated with B. bracteata showed the highest species diversity and the fungi associated with Pa. virgatum showed the lowest diversity. Results from sorghum trap cultures using soil collected from under different host plant species showed differential sporulations of AM fungal species. In addition, a greenhouse study was conducted in which different host plant species were grown in similar tallgrass prairie soil. After 4 months of growth, AM fungal species composition was significantly different beneath each host species. These results strongly suggest that AM fungi show some degree of host-specificity and are not randomly distributed in tallgrass prairie. The demonstration that host plant species composition influences AM fungal species composition provides support for current feedback models predicting strong regulatory effects of soil communities on plant community structure. Differential responses of AM fungi to host plant species may also play an important role in the regulation of species composition and diversity in AM fungal communities. Received: 29 January 1999 / Accepted: 20 October 1999     

Delving into the dark ecology: A continent-wide assessment of patterns of composition in soil fungal communities from Australian tussock grasslands

Soil fungi play essential roles in many terrestrial processes, but our knowledge of the forces governing fungal distribution and community composition along broad-scale environmental gradients is still limited. In this study, we explored biogeographic distribution and composition of soil fungal communities associated with 62 tussock grasslands across different regions of Australia. Climatic parameters had only a limited correlation with fungal community structure, while edaphic variables and spatial distance were significantly associated with changes in fungal community composition. We also observed high variations in composition among fungal assemblages from different ecological regions, suggesting some regional endemism in these communities. The discrete distribution of fungi in soil was further confirmed by indicator analysis, which identified distinct indicator operational taxonomic units associated with grasslands from different climatic regions. Finally, fungi with flexible trophic interactions had a central role in the network architecture of both arid and temperate communities. Taken together, the results from our study confirm the prominent role of soil physico-chemical status and geographic location in determining fungal biogeographic patterns over large scales in Australia.     

Occurrence of fungi in combs of fungus-growing termites (Isoptera: Termitidae, Macrotermitinae)

Fungus-growing termites cultivate their mutualistic basidiomycete Termitomyces species on a substrate called a fungal comb. Here, the Suicide Polymerase Endonuclease Restriction (SuPER) method was adapted for the first time to a fungal study to determine the entire fungal community of fungal combs and to test whether fungi other than the symbiotic cultivar interact with termite hosts. Our molecular analyses show that although active combs are dominated by Termitomyces fungi isolated with direct Polymerase Endonuclease Restriction - Denaturing Gradient Gel Electrophoresis (PCR-DGGE), they can also harbor some filamentous fungi and yeasts only revealed by SuPER PCR-DGGE. This is the first molecular evidence of the presence of non-Termitomyces species in active combs. However, because there is no evidence for a species-specific relationship between these fungi and termites, they are mere transient guests with no specialization in the symbiosis. It is however surprising to notice that termite-associated Xylaria strains were not isolated from active combs even though they are frequently retrieved when nests are abandoned by termites. This finding highlights the implication of fungus-growing termites in the regulation of fungi occurring within the combs and also suggests that they might not have any particular evolutionary-based association with Xylaria species.     

Diversity and ecology of soil fungal communities in rubber plantations

Monoculture rubber cultivation and its intensive associated human activities are known to have a negative impact on the biodiversity, ecology, and biological conservation of the ecosystems in which they occur. These negative impacts include changes to the biodiversity and function of soil fungal communities, which contribute towards nutrient cycling and interact with other organisms in belowground ecosystems, and may be pathogens. Despite the important role of soil fungi in rubber plantations, these communities have been poorly studied. In this paper, we review the existing literature on the diversity and ecology of belowground fungi in rubber plantations. Various groups of soil fungi, including saprobes, symbionts, and pathogens are discussed. Additionally, the role of plantation management is discussed in the context of both pathogenic soil fungi and the promotion of beneficial soil fungi. Management practices include clone selection, tree age and planting density, application of chemicals, and intercropping systems. Our review shows the strong need for further research into the effects of monoculture rubber plantations on soil fungal communities, and how we can best manage these systems in the future, in order to create a more sustainable approach to rubber production.     

The effects of grazing history,soil properties and stand structure on the communities of saprotrophic fungi in wood-pastures

Wood-pastures are threatened anthropogenic biotopes that provide habitat for an extensive group of species. Here we studied the effect of management, grazing intensity, time since abandonment, historical land-use intensity, soil properties and stand conditions on communities of saprotrophic fungi in wood-pastures in Central Finland. We found that the proportion of broadleaved trees and soil pH are the major drivers in the communities of saprotrophic fungi in these boreal wood-pastures. In addition, tree species richness, soil moisture, historical land-use intensity and time since abandonment affected the communities of saprotrophic fungi. Current management or grazing intensity did not have a clear effect on saprotrophic fungal species richness, although dung-inhabiting fungal species richness was highest at intermediate to high grazing intensity. Obviously, there were many more dung-inhabiting fungal species on grazed than on abandoned sites. Our study highlights the conservation value of wood-pastures as hotspots of saprotrophic fungi.     

Cavity construction by reintroduced populations of Red‐cockaded Woodpeckers (Dryobates borealis)

Although species reintroduction attempts are now common, monitoring of reintroduction attempts rarely extends beyond initial population establishment. This short timespan likely fails to document long‐term population stability, subtle changes in behavior, and the potentially larger effects that some reintroduced species may have on other species. The Red‐cockaded Woodpecker (RCW; Dryobates borealis) is an important habitat specialist and ecosystem engineer that excavates cavities in living trees. Excavation of natural RCW cavities can take years to complete, but they also persist for many years and are used by many other species. We quantified characteristics of cavity trees excavated by RCWs (n = 44) in two populations that were reintroduced to unoccupied areas more than 10 years earlier. We measured features associated with heartwood rot and used generalized linear mixed effects regression to determine whether these features differed for trees selected for cavity excavation compared with random neighboring trees. We also assessed population trends for cavity‐nesting species that commonly used RCW cavities on one of the sites. Height of first live limb was the only factor distinguishing natural RCW cavity trees from control trees. Four of six cavity‐nesting species monitored increased significantly following RCW establishment. The increases may relate to the many natural and artificial cavities created during the reintroduction effort. Future reintroductions of the RCW should lead to successful natural cavity excavation if sufficiently large trees with smaller live crowns are present. Future efforts may also benefit the broader community of cavity‐nesting birds.     

Community composition and diversity of Neotropical root‐associated fungi in common and rare trees

Interactions between plants and root‐associated fungi can affect the assembly, diversity, and relative abundances of tropical plant species. Host–symbiont compatibility and some degree of host specificity are prerequisites for these processes to occur, and these prerequisites may vary with host abundance. However, direct assessments of whether specificity of root‐associated fungi varies with host abundance are lacking. Here, in a diverse tropical forest in Los Tuxtlas, Mexico, we couple DNA metabarcoding with a sampling design that controls for host phylogeny, host age, and habitat variation, to characterize fungal communities associated with the roots of three confamilial pairs of host species that exhibit contrasting (high and low) relative abundances. We uncovered a functionally and phylogenetically diverse fungal community composed of 1,038 OTUs (operational taxonomic units with 97% genetic similarity), only 14 of which exhibited host specificity. Host species was a significant predictor of fungal community composition only for the subset of OTUs composed of putatively pathogenic fungi. We found no significant difference in the number of specialists associating with common versus rare trees, but we found that host abundance was negatively correlated with the diversity of root fungal communities. This latter result was significant for symbiotrophs (mostly arbuscular mycorrhizal fungi) and, to a lesser extent, for pathotrophs (mostly plant pathogens). Thus, root fungal communities differ between common and rare trees, which may impact the strength of conspecific negative density dependence. Further studies from other tropical sites and host lineages are warranted, given the role of root‐associated fungi in biodiversity maintenance.     

Soil fungal communities are compositionally resistant to drought manipulations – Evidence from culture-dependent and culture-independent analyses

Current environmental change predictions forecast intensified drought conditions. It is becoming increasingly evident that plant communities are sensitive to drought and that soil-inhabiting microbial communities vary along precipitation gradients. However, the drought sensitivity of microbial communities in general and that of soil fungi in particular remains unclear, even though understanding their responses to adverse environmental conditions is vital for better understanding of ecosystem service provisioning. We sampled soils at two sites with established experiments that imposed extreme, chronic drought to assess fungal community responses. We analyzed fungal communities using both culture-dependent and -independent tools and MiSeq-sequenced communities from colony forming units (CFU-PCR) on a drought simulating medium and from environmental DNA (ePCR), to compare the conclusions derived from these two methods. Our data from the two approaches consistently indicate that the composition of fungal communities is not affected by the drought treatment, whereas – based on the CFU-PCR but not ePCR data – their richness and diversity increased under drought conditions at the more mesic of the two sites. Further, based on the direct comparisons of CFU-PCR and ePCR, we estimate that more than 10% of the fungal community and more than 20% of the ascomycetes were culturable. We conclude that although recent research indicates that plant and bacterial communities respond to drought, fungal community responses are more variable, particularly in experiments that impose chronic drought under field conditions.     

Outcome of interspecific interactions among brown-rot and white-rot wood decay fungi

Abstract Interspecific mycelial interactions among brown-rot fungi resulted in either deadlock or replacement of one fungus by the other. Similarly, most of the brown-rot fungi deadlocked with some or all of the whitre-rot fungi tested, while a few were able to replace some of the white-rot fungi. The results indicate similarities in interspecific mycelial interactions among brown-rot fungi and between brown-rot and white-rot fungi. The results further suggest that some brown-rot fungi are capable of invading and occupying domains within white-rot fungal communities in decaying wood.     

New Lineages of Elaphocordyceps Harboring in Lichen Thalli

All species of Elaphocordyceps parasitize the fungal genus Elaphomyces, except for three species growing on scarabid beetle larvae or cicada nymphs. During our study on the diversity of culturable endolichenic fungi, some Elaphocordyceps species are found widely harboring in lichen thalli. A total of 64 fungal strains belonging to Elaphocordyceps were isolated from 42 lichen samples respectively collected from 5 provinces of China and the Antarctic. Phylogenetic analysis based on ITS nrDNA shows that these endolichenic fungi are possibly heterospecific. The endophytic fungi of plant often provide benefits to their hosts. However, the endolichenic fungi may be parasites or nutrient competitors of the mycobiont, because they have to obtain nutrient components from mycobionts or photobionts. Our study partly proves this hypothesis, since most known species of Elaphocordyceps are parasites of fungi.     

Endophyte communities vary in the needles of Norway spruce clones

Endophytic fungi show no symptoms of their presence but can influence the performance and vitality of host trees. The potential use of endophytes to indicate vitality has been previously realized, but a standard protocol has yet to be developed due to an incomplete understanding of the factors that regulate endophyte communities. Using a culture-free molecular approach, we examined the extent to which host genotype influences the abundance, species richness, and community composition of endophytic fungi in Norway spruce needles. Briefly, total DNA was extracted from the surface-sterilized needles of 30 clones grown in a nursery field and the copy number of the fungal internal transcribed spacer (ITS) region of ribosomal DNA was estimated by quantitative PCR. Fungal species richness and community composition were determined by denaturing gradient gel electrophoresis and DNA sequencing. We found that community structure and ITS copy number varied among spruce clones, whereas species richness did not. Host traits interacting with endophyte communities included needle surface area and the location of cuttings in the experimental area. Although Lophodermium piceae is considered the dominant needle endophyte of Norway spruce, we detected this species in only 33 % of samples. The most frequently observed fungus (66 %) was the potentially pathogenic Phoma herbarum. Interestingly, ITS copy number of endophytic fungi correlated negatively with the richness of ectomycorrhizal fungi and thus potential interactions between fungal communities and their influence on the host tree are discussed. Our results suggest that in addition to environmental factors, endophyte communities of spruce needles are determined by host tree identity and needle surface area.     

Crown dieback events as key processes creating cavity habitat for magellanic woodpeckers

Abstract Woodpeckers are considered keystone species for webs of cavity nesters and habitat and resource specialists that strongly depend on availability of trees suitable for cavity excavation. Most studies carried out in northern hemisphere temperate coniferous forests emphasize the importance of old growth stages of forests or large dead trees as habitat for cavity builders. We present a study of Nothofagus pumilio tree selection by the magellanic woodpecker (Campephilus magellanicus) that incorporates dendroecological data on long‐term growth trends of trees that provides new insights into the processes that create suitable habitat for cavity excavating species. We analysed 351 cavity and neighbouring control trees in terms of age and radial growth patterns, as well as external tree characteristics. In addition, from a subsample of these trees we developed tree‐ring chronologies for each group using standard methods in order to analyse potential differences in radial growth patterns between cavity and non‐cavity trees. Multivariate models that account for differences between paired cavities versus control trees indicated that growth decline and the degree of crown dieback were the primary variables explaining magellanic woodpecker tree selection for cavity building. In contrast to previous work, neither diameter (above a certain threshold) nor age, were important determinants of selection. Furthermore, trees that became present cavity are those that had synchronously declined in radial growth during the 1943–44 and 1956–57 droughts and the 1985–86 massive caterpillar defoliation. Insect outbreaks and extreme climatic events may episodically reduce vigour, induce partial crown mortality, trigger increased fungal attack and heart rot formation at different tree heights on the bole in a group of trees and thus increase availability of soft substrate and their likelihood of cavity excavation by the magellanic woodpecker. These results underscore the importance of drought/biotically‐induced canopy dieback events in creating habitat for woodpeckers and their dependent cavity users.     

The effects of geographic origin and genotype on fungal diversity of silver birch (Betula pendula)

Soil microbes, especially root symbiotic fungi, often have drastic effects on the successful growth and establishment of plants. While plant intraspecific genetic variation is known to affect many ecosystem processes and functions, the effect it has on root fungal communities has received less attention. To determine the effect plant origin and genotype have on root fungal communities, we used high-throughput amplicon sequencing of ITS-regions to detect fungi from the roots of 64 clonally propagated silver birch (Betula pendula) trees representing four different geographical origins and 16 genotypes, all grown together in a common garden. We found that fungal alpha and beta-diversity but not community composition differ by silver birch genotype. Some birch genotypes are potentially more plastic in terms of their fungal interactions, which could make them more robust against environmental changes and provide a competitive advantage especially in disturbed habitats.     

Comparative analysis of fungal communities in colonies of two leaf-cutting ant species with different substratum preferences

Fungus gardens of leaf-cutting ants harbor diverse alien fungi in addition to their fungal cultivar. Previous work suggested that alien microorganisms are likely derived from the substrata foraged by ant workers and incorporated into the fungus gardens. To test this hypothesis, we sampled 1014 garden fragments from 16 field colonies of Atta sexdens rubropilosa (a dicot-cutting ant) and Atta capiguara (a grass-cutting ant) in Brazil. From a total of 615 fungal isolates recovered, we observed similar diversity of fungi between colonies of both ant species. However, fungal communities differed in composition of taxa between ant colonies. Trichoderma spirale, Trichosporon chiarellii and Penicillium citrinum were prevalent accounting for 18.5%, 12.2% and 11.7% of the total isolates, respectively. As expected, fungal communities clustered in two major groups supporting the hypothesis that plant substratum has an impact on the composition of the alien fungi found in leaf-cutting ant gardens.     

Fungal associates of <Emphasis Type="Italic">Pyrola rotundifolia</Emphasis>, a mixotrophic Ericaceae,from two Estonian boreal forests

Pyrola rotundifolia (Ericaceae, Pyroleae tribe) is an understorey subshrub that was recently demonstrated to receive considerable amount of carbon from its fungal mycorrhizal associates. So far, little is known of the identity of these fungi and the mycorrhizal anatomy in the Pyroleae. Using 140 mycorrhizal root fragments collected from two Estonian boreal forests already studied in the context of mixotrophic Ericaceae in sequence analysis of the ribosomal DNA internal transcribed spacer region, we recovered 71 sequences that corresponded to 45 putative species in 19 fungal genera. The identified fungi were mainly ectomycorrhizal basidiomycetes, including Tomentella, Cortinarius, Russula, Hebeloma, as well as some ectomycorrhizal and/or endophytic ascomycetes. The P. rotundifolia fungal communities of the two forests did not differ significantly in terms of species richness, diversity and nutritional mode. The relatively high diversity retrieved suggests that P. rotundifolia does not have a strict preference for any fungal taxa. Anatomical analyses showed typical arbutoid mycorrhizae, with variable mantle structures, uniseriate Hartig nets and intracellular hyphal coils in the large epidermal cells. Whenever compared, fungal ultrastructure was congruent with the molecular identification. Similarly to other mixotrophic and autotrophic pyroloids in the same forests, P. rotundifolia shares its mycorrhizal fungal associates with surrounding trees that are likely a carbon source for pyroloids.