Mammalian mycophagy: A global review of ecosystem interactions between mammals and fungi.

The consumption of fungi by animals is a significant trophic interaction in most terrestrial ecosystems, yet the role mammals play in these associations has been incompletely studied. In this review, we compile 1 154 references published over the last 146 years and provide the first comprehensive global review of mammal species known to eat fungi (508 species in 15 orders). We review experimental studies that found viable fungal inoculum in the scats of at least 40 mammal species, including spores from at least 58 mycorrhizal fungal species that remained viable after ingestion by mammals. We provide a summary of mammal behaviours relating to the consumption of fungi, the nutritional importance of fungi for mammals, and the role of mammals in fungal spore dispersal. We also provide evidence to suggest that the morphological evolution of sequestrate fungal sporocarps (fruiting bodies) has likely been driven in part by the dispersal advantages provided by mammals. Finally, we demonstrate how these interconnected associations are widespread globally and have far-reaching ecological implications for mammals, fungi and associated plants in most terrestrial ecosystems. Citation: Elliott TF, Truong C, Jackson S, Zúñiga CL, Trappe JM, Vernes K (2022). Mammalian mycophagy: a global review of ecosystem interactions between mammals and fungi. Fungal Systematics and Evolution 9: 99-159. doi: 10.3114/fuse.2022.09.07.

New and Interesting Fungi. 5.

Nine new genera, 17 new species, nine new combinations, seven epitypes, three lectotypes, one neotype, and 14 interesting new host and / or geographical records are introduced in this study. New genera: Neobarrmaelia (based on Neobarrmaelia hyphaenes), Neobryochiton (based on Neobryochiton narthecii), Neocamarographium (based on Neocamarographium carpini), Nothocladosporium (based on Nothocladosporium syzygii), Nothopseudocercospora (based on Nothopseudocercospora dictamni), Paracamarographium (based on Paracamarographium koreanum), Pseudohormonema (based on Pseudohormonema sordidus), Quasiphoma (based on Quasiphoma hyphaenes), Rapidomyces (based on Rapidomyces narthecii). New species: Ascocorticium sorbicola (on leaves of Sorbus aucuparia, Belgium), Dactylaria retrophylli (on leaves of Retrophyllum rospigliosii, Colombia), Dactylellina miltoniae (on twigs of Miltonia clowesii, Colombia), Exophiala eucalyptigena (on dead leaves of Eucalyptus viminalis subsp. viminalis supporting Idolothrips spectrum, Australia), Idriellomyces syzygii (on leaves of Syzygium chordatum, South Africa), Microcera lichenicola (on Parmelia sulcata, Netherlands), Neobarrmaelia hyphaenes (on leaves of Hyphaene sp., South Africa), Neobryochiton narthecii (on dead leaves of Narthecium ossifragum, Netherlands), Niesslia pseudoexilis (on dead leaf of Quercus petraea, Serbia), Nothocladosporium syzygii (on leaves of Syzygium chordatum, South Africa), Nothotrimmatostroma corymbiae (on leaves of Corymbia henryi, South Africa), Phaeosphaeria hyphaenes (on leaves of Hyphaene sp., South Africa), Pseudohormonema sordidus (on a from human pacemaker, USA), Quasiphoma hyphaenes (on leaves of Hyphaene sp., South Africa), Rapidomyces narthecii (on dead leaves of Narthecium ossifragum, Netherlands), Reticulascus parahennebertii (on dead culm of Juncus inflexus, Netherlands), Scytalidium philadelphianum (from compressed air in a factory, USA). New combinations: Neobarrmaelia serenoae, Nothopseudocercospora dictamni, Dothiora viticola, Floricola sulcata, Neocamarographium carpini, Paracamarographium koreanum, Rhexocercosporidium bellocense, Russula lilacina. Epitypes: Elsinoe corni (on leaves of Cornus florida, USA), Leptopeltis litigiosa (on dead leaf fronds of Pteridium aquilinum, Netherlands), Nothopseudocercospora dictamni (on living leaves of Dictamnus albus, Russia), Ramularia arvensis (on leaves of Potentilla reptans, Netherlands), Rhexocercosporidium bellocense (on leaves of Verbascum sp., Germany), Rhopographus filicinus (on dead leaf fronds of Pteridium aquilinum, Netherlands), Septoria robiniae (on leaves of Robinia pseudoacacia, Belgium). Lectotypes: Leptopeltis litigiosa (on Pteridium aquilinum, France), Rhopographus filicinus (on dead leaf fronds of Pteridium aquilinum, Netherlands), Septoria robiniae (on leaves of Robinia pseudoacacia, Belgium). Neotype: Camarographium stephensii (on dead leaf fronds of Pteridium aquilinum, Netherlands). Citation: Crous PW, Begoude BAD, Boers J, Braun U, Declercq B, Dijksterhuis J, Elliott TF, Garay-Rodriguez GA, Jurjevic Z, Kruse J, Linde CC, Loyd A, Mound L, Osieck ER, Rivera-Vargas LI, Quimbita AM, Rodas CA, Roux J, Schumacher RK, Starink-Willemse M, Thangavel R, Trappe JM, van Iperen AL, Van Steenwinkel C, Wells A, Wingfield MJ, Yilmaz N, Groenewald JZ (2022) New and Interesting Fungi. 5. Fungal Systematics and Evolution 10: 19-90. doi: 10.3114/fuse.2022.10.02.

Resurrecting the genus Geomorium: Systematic study of fungi in the genera Underwoodia and Gymnohydnotrya (Pezizales) with the description of three new South American species.

Molecular phylogenetic analyses have addressed the systematic position of several major Northern Hemisphere lineages of Pezizales but the taxa of the Southern Hemisphere remain understudied. This study focuses on the molecular systematics and taxonomy of Southern Hemisphere species currently treated in the genera Underwoodia and Gymnohydnotrya. Species in these genera have been identified as the monophyletic /gymnohydnotrya lineage, but no further research has been conducted to determine the evolutionary origin of this lineage or its relationship with other Pezizales lineages. Here, we present a phylogenetic study of fungal species previously described in Underwoodia and Gymnohydnotrya, with sampling of all but one described species. We revise the taxonomy of this lineage and describe three new species from the Patagonian region of South America. Our results show that none of these Southern Hemisphere species are closely related to Underwoodia columnaris, the type species of the genus Underwoodia. Accordingly, we recognize the genus Geomorium described by Spegazzini in 1922 for G. fuegianum. We propose the new family, Geomoriaceae fam. nov., to accommodate this phylogenetically and morphologically unique Southern Hemisphere lineage. Molecular dating estimated that Geomoriaceae started to diverge from its sister clade Tuberaceae c. 112 MYA, with a crown age for the family in the late Cretaceous (c. 67 MYA). This scenario fits well with a Gondwanan origin of the family before the split of Australia and South America from Antarctica during the Paleocene-Eocene boundary (c. 50 MYA).

Balsamia (Sequestrate Helvellaceae, Ascomycota) in western North America.

Balsamia, a hypogeous, sequestrate genus in the Helvellaceae, has been characterized variously as having three to eight species in North America, and these have been considered either different from or conspecific with European species. No available modern systematic treatment of Balsamia exists to allow for accurate identification at the species level. We sequenced DNA from recent western North American Balsamia collections, assessed relationships by sequence similarity, and identified molecular taxonomic units. From these data, we determined which matched descriptions and types of named species. ITS sequences supported 12 Balsamia species in western North America, five originally described by Harkness and Fischer and seven new species that we describe here. No sequences from Balsamia collections in western North America were nested among those of European species. We found no clear evidence for separation of Balsamia into multiple genera.

Erratum to: A worldwide nomenclature revision of sequestrate Russula species: FUSE 1: 229-242 (2018). doi.org/10.3114/fuse.2018.01.10.

Two corrections are needed to our revision of sequestrate Russula nomenclature (Elliott & Trappe 2018). Decisions are based on the International Code of Nomenclature for algae, fungi, and plants (Turland et al. 2018), hereafter referred to as the "Shenzhen Code". We present them in the same format as the original publication to facilitate comparison of the corrections with the previous publication.

A worldwide nomenclature revision of sequestrate Russula species.

Before the application of molecular techniques, evolutionary relationships between sequestrate genera and their epigeous counterparts in the Russulaceae were unclear. Based on overwhelming evidence now available, personal observations, and consideration of the International Code for Nomenclature of Algae, Fungi and Plants, we combine the overlapping sequestrate generic names Bucholtzia, Cystangium, Elasmomyces, Gymnomyces, Macowanites, and Martellia with the agaricoid genus Russula. This nomenclatural action follows precedents set by earlier mycologists and continues an effort to create clarity in our understanding of the evolutionary affiliations among sequestrate fungi - particularly the Russulaceae. We also provide the first comprehensive list of described sequestrate species of Russula.

Three new black Elaphomyces species (Elaphomycetaceae, Eurotiales, Ascomycota) from eastern North America with notes on selected European species.

We describe three new species of Elaphomyces from eastern North America. Of the three, Elaphomyces loebiae is the rarest, known only from North Carolina and South Carolina, and appears to associate primarily with ectomycorrhizal hardwoods but possibly also with conifers. Elaphomyces cibulae is widely distributed but disjunct from Florida, Mississippi, and North Carolina. Elaphomyces cibulae seems to primarily associate with Quercus species. Elaphomyces mitchelliae has the widest distribution of the three species, from Florida, Maryland, North Carolina, Virginia, and West Virginia, and appears to associate with either ectomycorrhizal hardwoods and/or conifers. In the course of comparing our new Elaphomyces species to previously described European species we discovered that E. persoonii var. minor is conspecific in all essential details with and thus a synonym of E. cyanosporus.

Ecological relationships among hypogeous fungi and trees: inferences from association analysis integrated with habitat modeling.

Association analyses by contingency tables and generalized linear modeling were compared to infer relationships among hypogeous (belowground-fruiting) ectomycorrhizal fungi and potential host tree species from 136 study plots in forested habitats in southeastern mainland Australia. Results from both types of statistical approaches were highly congruent. As with previous experimental studies, no exclusive fungus-host tree associations were identified. However, the likelihood of occurrence of some species of fungi increased significantly in the presence of particular host tree species, suggesting fungal host preference or shared habitat preferences. Similarly, while most associations among fungal species were nonsignificant, a few taxa were more likely to be found in the presence of certain others. These were termed positively associated and are thought to share common climatic and microhabitat requirements or host preferences. In contrast, other combinations of fungal species were negatively associated with one another, perhaps indicating different habitat preferences. Furthermore, the finding that some fungi occurred more frequently in the presence of certain tree species provides a starting point for selection of compatible host-fungus combinations that could be used for forest nursery and restoration applications.

Multiple origins of sequestrate fungi related to Cortinarius (Cortinariaceae).

The aim of the present study was to investigate the phylogeny and evolution of sequestrate fungi (with gastroid or partially exposed basidiomes) in relation to their gilled relatives from the Cortinariaceae (Basidiomycetes). Phylogenetic analyses of 151 ITS sequences from 77 gilled species and 37 sequestrate taxa were performed using maximum parsimony and maximum likelihood methods. Results show that sequestrate basidiome forms occur in all three major ectomycorrhizal lineages of Cortinariaceae: the clades Cortinarius, Hebeloma/Hymenogaster/Naucoria, and Descolea. However, these forms do not appear within the saprobic outgroup Gymnopilus, indicating multiple origins of sequestrate forms from ectomycorrhizal ancestors. Additionally, within the Cortinarius clade sequestrate forms have multiple origins: emergent Cortinarius spp., Thaxterogaster, Quadrispora, Protoglossum, and two Hymenogaster spp. (H. remyi, H. sublilacinus) share common ancestors with Cortinarius spp., but these sequestrate genera are not closely related to each other (with exception of Thaxterogaster and Quadrispora). Hymenogaster sensu stricto, Setchelliogaster, and Descomyces were placed in the two other major clades. Thus, sequestrate taxa evolved independently many times within brown-spored Agaricales. Furthermore, emergent, secotioid, and gastroid forms have evolved independently from each other, and so are not necessarily intermediate forms. After their establishment, these apparently morphologically stable taxa show a tendency to radiate.

Mycophagy by small mammals in the coniferous forests of North America: nutritional value of sporocarps of Rhizopogon vinicolor, a common hypogeous fungus.

We evaluated the nutritional value of sporocarps of Rhizopogon vinicolor, a common hypogeous fungus in the coniferous forests of North America, for two small mammal species: the Californian red-backed vole (Clethrionomys californicus) and the northern flying squirrel (Glaucomys sabrinus). Although the nitrogen concentration of sporocarps was high, much of it was in non-protein form or associated with cell walls, suggesting that it may be of low nutritional value or protected from mammalian digestive enzymes. Sporocarps also had high concentrations of cell wall constituents, indicating low availability of digestible energy. When fed a diet of this fungus alone in a controlled feeding experiment both mammal species lost a small amount of body mass. Digestibilities of dry matter, nitrogen, cell wall constituents and energy from sporocarps by both species were lower than the digestibilities of other food types by other similarly sized small mammals. Red-backed voles digested the various components of sporocarps at least as well as the flying squirrels, even though they were almost six-fold smaller in body mass. This observation supports the notion that red-backed voles, like other microtine rodents, have morphological and physiological adaptations of the digestive system that are postulated to permit greater digestion of fibrous diets than predicted on the basis of body size. Despite this, our results re-affirm previous conclusions that hypogeous fungi are only of moderate nutritional value for most small, hindgut-fermenting mammals. Future studies should focus on the importance of mixed-species of fungi in the diet of small mammalian mycophagists.

Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: interactions with soil nitrogen and organic matter.

Plants growing on an environmentally stressed glacier forefront on soil low in N and organic matter have abundant root colonizations by dark-septate fungi. As the plants appeared fit for this severe habitat, it was hypothesized that the dark-septate endophytes were neutral or beneficial rather than detrimental to the plants. To test this hypothesis, we designed a growth-room experiment with Pinus contorta grown on forefront soil inoculated with the dark-septate fungus Phialocephala fortinii in the absence of climatic stress. N and organic matter treatments were included to explore their interaction with the fungal inoculation. P. fortinii colonized roots inter- and intracellularly and occasionally formed microsclerotia. Inoculated plants absorbed significantly more P than noninoculated plants in all combinations of N and organic matter. Without added N, neither inoculation nor organic matter addition improved plant growth or N uptake, showing that N indeed limits plant growth in this substrate. With added N, however, both organic matter addition and inoculation significantly increased total pine biomass and N uptake. The enhanced P uptake by the P. fortinii-inoculated pine as well as the increased pine growth and N uptake in the treatment combining P. fortinii and N appear as typical mycorrhizal responses.

Decomposition of 14 C-labelled substrates by ectomycorrhizal fungi in association with Douglas fir.

Ectomycorrhizas of Pseudotsuga menziesii (Mirb.) Franco were synthesized in pure culture with Cenococcum geophilum Fr., Laccaria bicolor (Maire) Orton, Rhizopogon vinicolor Smith, or Suillus lakei (Murr.) Smith and Thiers. The mycorrhizal plants were grown in sterile vessels with peat/vermiculite plus 14 C labelled hemicellulose, cellulose, Douglas fir needles, or humic polymers as an organic substrate. The sum of the 14 C respired and that found in the seedling after 240 d of growth was used to quantify decomposition of the labelled substrates. All mycobionts released at least 20-30% of the 14 C in hemicellulose and all were able to release 14 C from cellulose and needles, escept L. buolttr, which failed to release 14 C from needles. S. lakei released the largest amount of 14 C from cellulose. C. geophilum, S. lakei and R. filticolor released similar amounts of 14 C from needles. Generally, substrates could be ranked in terms of ease of breakdown by the ectomycorrhizal fungi as follows: humic polymers < needles < cellulose < hemicellulose.

Morphological changes and photosynthate allocation in ageing Hebeloma crustuliniforme (Bull.) Quel. and Laccaria bicolor (Maire) Orton mycorrhizas of Pinus ponderosa Dougl. ex. Laws.

Seedlings of Pinus Ponderosa Dougl, ex. Laws were grown in root observation containers. They were inoculated with either Hebeloma crustuliniforme (Bull.) Quel. or Laccaria bicolor (Maire) Orton or left uninoculated (control). Oil a monthly basis starting at the eighth month of a 12-month growing period, roots (mycorrhizal root tips from inoculated plants, non-mycorrhizal from control plants) were traced onto acetate sheets. Each root tip was classified as light, 'intermediate' or 'dark' in colour. Roots initiated between months eight and nine were monitored for the next 90 d. All root tips progressed from light-brown to dark-brown to black for all three treatments. Hebeloma crustuliniforme, and to a lesser extent L. bicolor, retarded this progression relative to the control. At the end of 12 months, seedlings were labelled with 14 CO2 to determine the effects of ectomycorrhizal inoculation on carbon supply to roots of the different morphological categories. The amount of 14 C in 'light'L. bicolor and H. crustuliniforme mycorrhizas was 2.3 and 1.8 times greater, respectively, than that in 'light' control root tips. The amount of 14 C in mycorrhizas of the inoculated treatments and, to a lesser extent, roots of the control seedlings decreased as they progressed from 'light' to 'dark'. It is concluded that pondersa pine seedlings continue to allocate photosynthate to morphologically older roots, perhaps to meet maintenance requirements or to supply carbon for growth and metabolism of extra-matrical hyphae. Such allocation may enhance root longevity, which would have an important influence on tree, forest and soil carbon budgets.

Root endophytes of lupin and some other legumes in Northwestern USA.

Roots of ten species of Lupinus and three other legumes collected from field soils were cleared, stained, and examined for fungal colonization. Three species were not colonized. Nine species were colonized by aseptate hyphae and vesicles attributable to vesicular-arbuscular mycorrhizal fungi. Seven species were sometimes colonized by fungi with septate hyphae, which often formed intracellular sclerotia. The associations observed are compared with previous reports and discussed in relation to legume systematics.

Ectomycorrhizal mediation of competition between coniferous tree species.

To test the effect of ectomycorrhizal fungi (EMF) on interactions between host plants, Pseudotsuga menziesii (Mirb.) Franco and Pinus ponderosa Dougl. ex. Laws., seedlings were grown in replacement series in pasteurized soil with (a) no EMF added, (A) two EMF species added - Rhizopogon vinicolor Smith (specific to Douglas-fir) and R. ochraceorubens Smith (specific to pine), and (c) tour EMF species added - the two Rhizopogon species plus two host generalists, Laccaria laccata (Scop, ex Fr.) Bk. & Br, and Hebeloma crustuliniforme (Bull.) Quel. A replacement series in unpasteurized forest soil also was included. Seedlings without added EMF were colonized by the greenhouse contaminant, Thelephora terrestris. Without added EMF (but with T. terrestris), the tree species mutually inhibited one another, producing Relative Yield Totals significantly < 1; with EMF added, mutual inhibition disappeared. With four EMF species added, Pseudotsuga menziesii seedlings were significantly larger in mixture than in monoculture, with no corresponding decrease in the size of Pinus ponderoso seedlings; this was due solely to seedlings with L. laccata, which apparently enhanced nitrogen (N) and phosphorus (P) uptake by Pseudotsuga menziesii at the expense of luxury consumption by Pinus ponderosa. Graphical analysis suggested that better growth of Pseudotosuga menziesii in mixture with EMF added was related to improved P nitrogen. Both N and P nutrition of Pinus ponderosa was better in mixture with two than no EMF species added; there was no clear nutrient effect with four EMF species added. Results indicate that EMF can reduce competition between plant species and perhaps increase overall community P uptake. However, patterns were specific to both EMF and tree species and were quite different in unpasteurized soils. Hence generalizations about the effects of EMF on plant-plant interactions must be made cautiously.

Fossil mycorrhizae: a case for symbiosis.

Vesicular-arbuscular mycorrhizae are significant in the physiology and ecology of extant vascular plants, and they may also have played a major role in the origin of the vascular land flora. The case for fossil vesicular-arbuscular mycorrhizae rests upon hyphae and chlamydospore-like bodies in several Paleozoic taxa, but fossil arbuscles are unknown to date. Specimens from the Triassic of Antarctica represent the first known occurrence of arbuscles in the fossil record.