Rare but widespread: A systematic revision of the truffle-forming genera Destuntzia and Kjeldsenia and the formation of a new genus, Hosakaea.

Here we present the results of taxonomic and systematic study of the rare truffle-forming genera Destuntzia and Kjeldsenia. Truffle-forming fungi are difficult to study due to their reduced morphological features and their cryptic, hypogeous fruiting habits. The rare occurrence of Destuntzia and Kjeldsenia further compounds these difficulties due to the lack of adequate material for study. Recent forays in North Carolina and Tennessee recovered new specimens of another rarely collected fungus, Octaviania purpurea. Morphological and phylogenetic analysis revealed that Octaviania purpurea is a member of the genus Destuntzia, and this led us to reevaluate the taxonomic status and systematic relationships of other Destuntzia species. We performed a multilocus phylogenetic analysis of Destuntzia specimens deposited in public fungaria, including all available type material, and environmental sequences from animal scat and soil. Our analyses indicate that Destuntzia is a member of the family Claustulaceae within the order Phallales and is a close relative of Kjeldsenia. Results of our phylogenetic analysis infer that three species originally described in the genus Destuntzia are members of the genus Kjeldsenia. We propose three new combinations in Kjeldsenia to accommodate these species as well as a new combination in Destuntzia to accommodate Octaviania purpurea. We also describe a new genus in Claustulaceae, Hosakaea, to accommodate a closely affiliated species, Octaviania violascens. Finally, we transfer the genus Destunzia into the family Claustulaceae and emend the description of the family. The newly proposed combinations in Destuntzia and Kjeldsenia significantly expand the known geographic ranges of both genera. The data from metabarcode analysis of scat and soil also reveal several additional undescribed species that expand these ranges well beyond those suggested by basidiomata collections. Systematic placement of Destuntzia in the saprotrophic order Phallales suggests that this genus is not ectomycorrhizal, and the ecological implications of this systematic revision are discussed.

Wind and small mammals are complementary fungal dispersers.

Following a disturbance, dispersal shapes community composition as well as ecosystem structure and function. For fungi, dispersal is often wind or mammal facilitated, but it is unclear whether these pathways are complementary or redundant in the taxa they disperse and the ecosystem functions they provide. Here, we compare the diversity and morphology of fungi dispersed by wind and three rodent species in recently harvested forests using a combination of microscopy and Illumina sequencing. We demonstrate that fungal communities dispersed by wind and small mammals differ in richness and composition. Most wind-dispersed fungi are wood saprotrophs, litter saprotrophs, and plant pathogens, whereas fungi dispersed in mammal scat are primarily mycorrhizal, soil saprotrophs, and unspecified saprotrophs. We note substantial dispersal of truffles and agaricoid mushrooms by small mammals, and dispersal of agaricoid mushrooms, crusts, and polypores by wind. In addition, we find mammal-dispersed spores are larger than wind-dispersed spores. Our findings suggest that wind- and small-mammal-facilitated dispersal are complementary processes and highlight the role of small mammals in dispersing mycorrhizal fungi, particularly following disturbances such as timber harvest.

The underappreciated role of rodent generalists in fungal spore dispersal networks.

Animals are often the primary dispersers of seeds and fungal spores. Specialist species that consume fruits or fungal fruiting bodies (sporocarps) as their main food source are thought to play a more important role in dispersal networks compared to generalist species. However, dispersal networks are often based on occurrence data, overlooking the influence of animal abundance and dispersal effectiveness on network interactions. Using rodent-mycorrhizal fungi networks, we determined how diet specialization and abundance influence the role of rodent species in dispersing fungal spores in temperate forests of northern New Hampshire, USA. We tracked the interactions of five rodent species and 34 fungal taxa over a 3-yr period across hardwood, mixed, and softwood forest stands. We accounted for fluctuations in rodent abundance and differences in the number of spores dispersed in rodent scat. Myodes gapperi, a fungal specialist, dispersed a more diverse spore community than rodent generalists and was consistently the most important disperser in forest types with high fungal availability. Nevertheless, during years when generalist species such as Tamias striatus and Peromyscus maniculatus reached high abundance, their relative importance (species strength) in networks approached or even surpassed that of M. gapperi, particularly in forest types where M. gapperi was less common and fungal availability was low. Increased numbers of generalists enhanced network interaction diversity and the number of fungal taxa dispersed, the timing of which was coincident with seedling establishment following masting, a stage when inoculation by mycorrhizal fungi is critical for growth and survival. Our findings suggest that although specialists play key roles in dispersing mycorrhizal fungal spores, generalists play a heretofore underappreciated role.

Signaling from below: rodents select for deeper fruiting truffles with stronger volatile emissions.

Many plant and fungal species use volatile organic compounds (VOCs) as chemical signals to convey information about the location or quality of their fruits or fruiting bodies to animal dispersers. Identifying the environmental factors and biotic interactions that shape fruit selection by animals is key to understanding the evolutionary processes that underpin chemical signaling. Using four Elaphomyces truffle species, we explored the role of fruiting depth, VOC emissions, and protein content in selection by five rodent species. We used stable isotope analysis of nitrogen (δ15 N) in truffles to estimate fruiting depth, proton-transfer-reaction mass spectrometry to determine volatile emission composition, and nitrogen concentrations to calculate digestible protein of truffles. We coupled field surveys of truffle availability with truffle spore loads in rodent scat to determine selection by rodents. Despite presumably easier access to the shallow fruiting species, E. americanus (0.5-cm depth) and E. verruculosus (2.5-cm depth), most rodents selected for truffles fruiting deeper in the soil, E. macrosporus (4.1-cm depth) and E. bartlettii (5.0-cm depth). The deeper fruiting species had distinct VOC profiles and produced significantly higher quantities of odiferous compounds. Myodes gapperi (southern red-backed vole), a fungal specialist, also selected for truffles with high levels of digestible protein, E. verruculosus and E. macrosporus. Our results highlight the importance of chemical signals in truffle selection by rodents and suggest that VOCs are under strong selective pressures relative to protein rewards. Strong chemical signals likely allow detection of truffles deep within the soil and reduce foraging effort by rodents. For rodents that depend on fungi as a major food source, protein content may also be important in selecting truffles.

Pulsed resource availability changes dietary niche breadth and partitioning between generalist rodent consumers.

Identifying the mechanisms that structure niche breadth and overlap between species is important for determining how species interact and assessing their functional role in an ecosystem. Without manipulative experiments, assessing the role of foraging ecology and interspecific competition in structuring diet is challenging. Systems with regular pulses of resources act as a natural experiment to investigate the factors that influence the dietary niches of consumers. We used natural pulses of mast-fruiting of American beech (Fagus grandifolia) to test whether optimal foraging or competition structure the dietary niche breadth and overlap between two congener rodent species (Peromyscus leucopus and P. maniculatus), both of which are generalist consumers. We reconstructed diets seasonally over a 2-year period using stable isotope analysis (δ13C, δ15N) of hair and of potential dietary items and measured niche dynamics using standard ellipse area calculated within a Bayesian framework. Changes in niche breadth were generally consistent with predictions of optimal foraging theory, with both species consuming more beechnuts (a high-quality food resource) and having a narrower niche breadth during masting seasons compared to nonmasting seasons when dietary niches expanded and more fungi (a low-quality food source) were consumed. In contrast, changes in dietary niche overlap were consistent with competition theory, with higher diet overlap during masting seasons than during nonmasting seasons. Overall, dietary niche dynamics were closely tied to beech masting, underscoring that food availability influences competition. Diet plasticity and niche partitioning between the two Peromyscus species may reflect differences in foraging strategies, thereby reducing competition when food availability is low. Such dietary shifts may have important implications for changes in ecosystem function, including the dispersal of fungal spores.

Elaphomyces species (Elaphomycetaceae, Eurotiales) from Bartlett Experimental Forest, New Hampshire, USA.

We describe five new species of Elaphomyces from Bartlett Experimental Forest, New Hampshire, USA (E. americanus, E. bartlettii, E. macrosporus, E. oreoides, and E. remickii) and revise the description of a sixth previously published species (E. verruculosus). Of the five new species, E. bartlettii and E. remickii are only known from New Hampshire whereas E. americanus, E. macrosporus, and E. oreoides are widely distributed in eastern North America. Elaphomyces verruculosus is the most widespread and abundant Elaphomyces species in eastern North America with a distribution extending from eastern Canada south to northeastern Mexico. All six Elaphomyces species are putatively associated with Tsuga canadensis, a tree species in regional decline. For five of the six Elaphomyces species, we report partially consumed ascomata or rodent fecal samples containing spores, indicating that small mammals play a key role in dispersing these Elaphomyces species and that the Elaphomyces are an important part of the small mammals' diet.