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Review Article

A 200-year history of arctic and alpine fungi in North America: Early sailing expeditions to the molecular era

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Pages 323-340 | Received 02 Mar 2020, Accepted 11 May 2020, Published online: 09 Jul 2020

ABSTRACT

Mushrooms and other fleshy fungi are important components of arctic and alpine habitats where they enhance nutrient uptake in plants and replenish poor soils through decomposition. Here we assemble the 200-year (1819–2019) record of their discovery in North America, beginning with early Arctic sailing expeditions, followed by intense taxonomic studies, and concluding with the molecular era, all of which highlight the difficulty of exhaustively revealing their biodiversity in these extreme, cold-dominated habitats. Compiled biogeographic data reveal that a majority of arctic fungi have large intercontinental distributions with disjunct alpine populations. A newly compiled checklist of 170 species of Basidiomycota in fifty-one genera and twenty families in the Rocky Mountain alpine zone provides current baseline data prior to expected environmental shifts.

Introduction

Alpine fungi exist at high elevations above treeline on mountaintops and plateaus, and their arctic counterparts occur beyond trees at high latitudes. In the Northern Hemisphere, fungi in these cold-dominated regions make up the ecologically important arcto-alpine mycota. These fungi exist as mutualists that enhance nutrient uptake in alpine plants; as decomposers that replenish nutrients in poor alpine soils; and as pathogens that affect alpine plant populations (Körner Citation1999; Haselwandter Citation2007). Those Basidiomycota that produce mushrooms or other kinds of visible fleshy fruiting bodies (i.e., basidiomes) are the focus of this review (); the crust-like thelephoroids and Sebacinales are not covered. At treeline, all trees are associated with ectomycorrhizal fungi (Körner Citation2012), many of which produce basidiomes; above and beyond the trees, Salix, Betula, and Dryas are the primary ectomycorrhizal hosts (Cripps and Eddington Citation2005; ), although there are potential associations with Bistorta, Kobresia, and Helianthemum. In these habitats, cold-loving fungal decomposers fruit on bryophytes, willow branches, and soil; ascolichens attach themselves to rocks or soil; and basidiolichens exist on mud flats in association with algae (Dahlberg and Bültmann Citation2013). Without these fungi, plant life would be sparser in the cold-dominated arctic–alpine biome that covers 8 percent of the Earth (Körner Citation1995).

The story of the discovery of alpine mushrooms as scientific entities began in Europe, where significant knowledge has been amassed over decades. The father of alpine mycology, Jules Favre, spent twenty-one years examining the mushrooms above treeline in the Swiss National Park, hiking to higher elevations to collect specimens (Favre Citation1955; Horak Citation1993; reviewed in Brunner et al. Citation2017). Other mycologists soon followed his example in the high Alps, Pyrenees, and Carpathians, including Bon (Citation1985, Citation1987, Citation1991, Citation1993), Kühner (Citation1975), Lamoure (Citation1982), Horak (Citation1987a, 1987b), Senn-Irlet (Citation1987), Graf (Citation1994), Peintner and Moser (Citation1996), Jamoni (Citation1995, Citation2008), Bizio (Citation1995, Citation1997), Ronikier (Citation2008), and Corriol (Citation2008). In North America, research has lagged behind, and no comprehensive review of the history and current knowledge of the diversity of alpine and arctic mushrooms has been compiled for this continent.

Greenland is considered part of North America, however, and arctic and alpine mushrooms in Greenland have been studied extensively (Lange Citation1957; Peterson Citation1977; Knudsen and Borgen Citation1982; Borgen Citation2006; Borgen, Elborne, and Knudsen Citation2006), and the data have been summarized in “Arctic and Alpine Mycology 6” (Boertmann and Knudsen Citation2006); these data are excluded from this work. Similarly, there has been significant research on the mushrooms inhabiting the arctic islands of Svalbard (Gulden, Jenssen, and Stordal Citation1985; Skifte Citation1989; Gulden and Torkelsen Citation1996) and Iceland (Christiansen Citation1941; Hallgrimsson Citation1998), and this information is similarly excluded.

Early expeditions to the Canadian Arctic (1819–1940)

Early exploration to discover fungi in cold climates in North America focused on Canada, where sailing ships provided access to remote Arctic lands to discover macrofungi (Linder Citation1947; Savile Citation1963; Estey Citation1994; Redhead and Baillargeon Citation1999; Väre Citation2017). During the nineteenth century, Arctic expeditions exploring the polar regions of North America were funded by wealthy businessmen or were supported by government agencies (Berkeley Citation1878; Rostrup and Simmons Citation1906; Lind Citation1910; Dearness Citation1923; Nares Citation2011). Botanical collections were of primary interest to scientifically minded individuals on these early expeditions. Nicholas Polunin summarizes the various accounts of these collectors in Botany of the Canadian Eastern Arctic, parts I and II (Polunin Citation1940, Citation1947). Historically, mycologists began investigating arctic fungi by examining the dried vascular plant material brought back by botanists for attached saprophytic or parasitic fungi (Linder Citation1947; Savile Citation1963). Occasionally, collectors brought back large, fleshy fungi from these expeditions; however, these were usually not identifiable due to improper handling and storage (Linder Citation1947; Savile Citation1963).

Starting in 1819, Captain William Edward Parry led two ships through the Canadian Archipelago on what would later be deemed the most successful attempt to find the Northwest Passage. The ships wintered at Melville Island, and in 1820 officers of the voyage collected Cantharellus lobatus (now called Arrhenia lobata) (), Lycoperdon pratense (a puffball), and fifteen species of lichens on the island (Brown Citation1823). According to Redhead and Baillargeon (Citation1999), these two collections are the earliest published record of any agaric in Canada. Other Arctic expeditions followed, and their findings on the larger fleshy fungi are summarized in . Many of the taxa are known today under different names.

Figure 1. Fleshy fruiting bodies of Rocky Mountain alpine fungi. (a) Arrhenia lobata, decomposer on Salix. (b) Rhizomarasmius epidryas, decomposer on Dryas octopetala. (c) Galerina, decomposer on moss. (d) Lichenomphalia basidiolichen. (e) Melampsora epitea, rust pathogen on Salix reticulata. (f) Lactarius lanceolatus, ectomycorrhizal with S. reticulata. (g) Russula nana, ectomycorrhizal with dwarf Salix. (h) Cortinarius absarokensis, a North American ectomycorrhizal endemic

Figure 1. Fleshy fruiting bodies of Rocky Mountain alpine fungi. (a) Arrhenia lobata, decomposer on Salix. (b) Rhizomarasmius epidryas, decomposer on Dryas octopetala. (c) Galerina, decomposer on moss. (d) Lichenomphalia basidiolichen. (e) Melampsora epitea, rust pathogen on Salix reticulata. (f) Lactarius lanceolatus, ectomycorrhizal with S. reticulata. (g) Russula nana, ectomycorrhizal with dwarf Salix. (h) Cortinarius absarokensis, a North American ectomycorrhizal endemic

Figure 2. (a) Typical North American alpine habitat, Beartooth Plateau, Rocky Mountains. (b) Alpine bog. (c) Betula nana, ectomycorrhizal. (d) Salix arctica, ectomycorrhizal. (e) Salix reticulata, ectomycorrhizal

Figure 2. (a) Typical North American alpine habitat, Beartooth Plateau, Rocky Mountains. (b) Alpine bog. (c) Betula nana, ectomycorrhizal. (d) Salix arctica, ectomycorrhizal. (e) Salix reticulata, ectomycorrhizal

Captain Sir John Franklin’s second overland expedition (1825–1827) crossed through the Canadian Arctic via the Northwest Territories and reached the Arctic Ocean (Berkeley Citation1839; Väre Citation2017). John Richardson, a surgeon on board, made fungal collections that were eventually placed in the prestigious herbarium of Sir William Jackson Hooker, who became director of the Herbarium at Kew (Great Britain) in 1841 (Desmond Citation1995), and these are reported in Rev. Miles Joseph Berkeley’s (Citation1839) paper on exotic fungi.

Franklin and 129 men were lost when two ships went down traversing the last unknown sections of the Northwest Passage around 1845 (Neatby and Mercer Citation2008); arctic fungi were collected on two expeditions funded by Lady Jane Franklin for the purpose of finding her husband’s lost remains. The search expedition led by Admiral Edward Belcher in 1852 set out with at least four ships, and only one returned. David Lyall, a physician and naturalist with the returning ship, again reported Cantharellus lobatus (now called Arrhenia lobata) in 1853 at Wellington Channel (Polunin Citation1940). This was the first confirmed collection (based on preserved material) of A. lobata from North America, and it was placed in the Herbarium at Kew (Redhead Citation1984b). The last expedition that set out to search for Franklin’s party in 1857 was led by Sir Francis Leopold M’Clintock; this was in the yacht Fox, a boat purchased by Lady Franklin (M’Clintock Citation1860). David Walker, a surgeon and naturalist, collected five basidiomycetes and one ascomycete (Hooker Citation1860; ). Walker’s collections were given to Sir Joseph Dalton Hooker, who passed them on to Berkeley (Hooker Citation1860). Berkeley subsequently published on twenty-six species (twenty-three species from Arctic Canada and three from Greenland) of Basidiomycota and Ascomycota collected during the Arctic Expedition from 1875 to 1876 (Berkeley Citation1878; ).

Table 1. Mushrooms and fleshy fungi collected during early North American Arctic expeditions, 1819–1931. Names and authorities as reported

In 1904, Pier A. Saccardo, Charles H. Peck, and William Trelease published a list of all known fungi in Alaska, including those collected by Trelease on the Harriman Alaska Expedition of 1899 (Trelease Citation1904). Three new species of arctic microfungi were described and four other arctic species were collected from Point Barrow (Saccardo, Peck, and Trelease Citation1904). In 1906, Emil Rostrup began careful examination of botanical collections made by Herman George Simmons during the second voyage of the Fram Expedition (1898–1902). These were collected on Ellesmere Island in Northern Canada, and eight new species of fungi were found on the dried plant specimens (Rostrup and Simmons Citation1906; ). The Gjoa expedition under Captain Roald Amundsen from 1903 to 1906 visited King Point on the Yukon Coast and King William Island. Fungal collections were observed on leaves and stems by Jens Lind (Citation1910), who noted the difficulty of identifying fungi that were deformed by the cold temperatures and exposed habitats of the Arctic, a problem still facing mycologists today. In 1909, the American agrostologist Albert S. Hitchcock traveled through the Alaskan interior looking at various grasses. He collected arctic uredineous rust fungi near Nome, which he shared with Joseph C. Arthur (Arthur Citation1911).

In 1923, John Dearness of London, Ontario, examined over a hundred fungi collected by the naturalists of the Southern Party from the Canadian Arctic expeditions (Dearness Citation1923; ). He noted the wide host range and relative lack of parasitic fungi, only recording three rusts (Pucciniales) and one smut (Ustilaginales). However, Savile (Citation1963) explained these low numbers by pointing out that botanists avoid diseased plants in order to secure the best collections, leading early mycologists to underestimate parasitic fungal abundance in arctic environments. Dearness returned to the Basidiomycota after a half-century pause and focused on the fleshy fungi of southern Baffin Island (Dearness Citation1928). One of the last true Arctic expeditions was the Oxford Exploration Club’s 1931 excursion to Akpatok Island, after which Nicholas Polunin (Citation1934) published a list of the twenty-four fungi he collected (). With a majority of Arctic North America mapped out and explored, expeditions began tapering off; however, detailed investigations of the fungi in these regions were just beginning.

Morphological studies of Arctic fleshy fungi

Up until the 1950s, little detailed research had focused on the mushrooms and other fleshy fungi (Ascomycota and Basidiomycota) in the Arctic. In 1908, Elias J. Durand first confirmed Geoglossaceae (earth tongues) in arctic and subarctic regions of North America when he identified Mitrula gracilis in Labrador and Newfoundland (Durand Citation1908); others would also study Geoglossaceae in arctic regions (Mains Citation1955; Kankainen Citation1969). Durand noted that M. gracilis also had been collected in Greenland (Durand Citation1908) and appeared to have a wide distribution in arctic regions. Hugh S. Spence and Otto E. Jennings investigated the fleshy fungi of the Northwest Territories and on Southampton Island, respectively, and found species in the ectomycorrhizal genera Boletus, Cortinarius, Hydnum, Hygrophorus, Lactarius, and Russula, along with the saprobic genera Calvatia, Psathyrella, and Tubaria, some of which were from arctic habitats (Spence Citation1932; Jennings Citation1936). David H. Linder (Citation1947) summarized the current knowledge regarding fungi found in the Canadian eastern Arctic, coming to some conclusions that were ahead of his time. Linder recognized that fungi found in arctic habitats appeared to have circumpolar distributions and shared similarities with their alpine counterparts at lower latitudes. He also noted the parallels between distributions of arctic–alpine fungi and flowering plants, indicating that the study of fungi may substantiate theories concerning distributions of phanerogams.

During the 1950s several mycologists began focusing on fungi in Northern Canada and Alaska. Edith K. Cash compiled a list of all known fungi and Myxomycetes in Alaska, which consisted of 843 species names that included plant parasites, saprobic micromycetes, and basidomycetes collected in the northern arctic regions of the state (Cash Citation1953). Howard E. Bigelow studied collections secured by government biological survey parties that included Arctic collections in the Tricholomataceae (Bigelow Citation1959), and he contributed knowledge on arctic Omphalina in Alaska and Canada (Bigelow Citation1970). In the 1960s, research was also expanding to include ecological investigations in arctic regions. Sprague and Lawrence (Citation1959, Citation1959–1960, Citation1960) published a three-part series with the goal of understanding the effects of deglaciation on pedological, botanical, and fungal development. Japanese mycologist Yosio Kobayasi and his team arrived in Point Barrow, Alaska, on 1 August 1965 and began three weeks of exploration in the region. They primarily isolated fungi from soil, dung, water (water molds), plant material, animal bones, and insects (in an unsuccessful search for Trichomycetes). However, they reported several species of larger fleshy fungi, including two Ascomycota (Peziza species) and forty-nine Basidiomycota in Hygrophoraceae, Tricholomataceae, Amanitaceae, Agaricaceae, Coprinaceae, Strophariaceae, Cortinariaceae, Boletaceae, Russulaceae, and Lycoperdaceae (Kobayasi et al. Citation1967). Like Kobayasi, John A. Parmelee primarily studied micromycetes in the Canadian Arctic; however, his work also expanded our knowledge of larger mycorrhizal fungi on central Baffin Island (Parmelee Citation1969).

Toward the end of the 1960s, Orson K. Miller Jr., a mycologist trained under Alexander Smith, became interested in arctic fungi after visits to Alaska with Robert L. Gilbertson in 1967 and 1968 (Cripps Citation2010). Miller’s interest in arctic fungi would last for the next thirty years, and he inspired several students and colleagues to examine the understudied fungi in these remote regions. Miller published three papers on Gasteromycetes (puffballs) from the Yukon territory and adjacent Alaska; he was considered an expert on this group (Miller Citation1968, Citation1969; Miller et al. Citation1980). Miller then turned his attention to the arctic and subarctic agarics (gilled mushrooms) of Canada and Alaska, publishing on Coprinus with Roy Watling (Watling and Miller Citation1971); Omphalina, Laccaria, and Coprinus with David F. Farr (Farr and Miller Citation1972); and Melanoleuca with Linnea S. Gillman (Gillman and Miller Citation1977). Miller’s student, Gary Laursen, spent most of his career in Alaska, and he and Miller published on arctic and alpine agarics in Alaska and Canada (Miller, Laursen, and Murray Citation1973; Miller, Laursen, and Calhoun Citation1974; Laursen, Miller, and Bigelow Citation1976) and on the function, distribution, and known plant associates of mycorrhizal fungi of the Alaskan tundra (Miller and Laursen Citation1978; Miller Citation1982b). Laursen and Harold H. Burdsall Jr. reported the first hypogeous fungus from the Alaskan tundra, Geopora cooperi, in ectomycorrhizal association with Salix alaxensis (Laursen and Burdsall Citation1976). Rau (Citation1977), another Miller student, studied fungi in decomposing litter from tundra plants near Barrow, Alaska, and student Robert Antibus reported on the ectomycorrhizal fungi with Salix rotundifolia (Antibus et al. Citation1981).

In the 1980s, the agaric genera Lactarius, Cortinarius, and family Hygrophoraceae in the Alaskan Arctic tundra were studied by Laursen and Joseph Ammirati (Ammirati and Laursen Citation1982; Laursen and Ammirati Citation1982a; Laursen, Ammirati, and Farr Citation1987a). Miller contributed to a review of the current taxonomic understanding of arctic fungi at Point Barrow, Alaska (Bunnell et al. Citation1980); he then went on to study the fleshy fungi of the subarctic tundra of Alaska and the Yukon (Miller Citation1982b, Citation1987), Marasmius epidryas with Scott Redhead (Redhead et al. Citation1982), Phaeogalera and Galerina with European mycologist Egon Horak (Horak and Miller Citation1992), Cystoderma (Miller Citation1993), and Hebeloma (Miller Citation1998). Miller’s in-depth knowledge of arctic fungi provided him with the basis to recognize the large intercontinental distribution of some fungal species (Miller, Laursen, and Farr Citation1982). Later he focused on three Hebeloma species in the alpine tundra of Colorado, recognizing that these species were also present in the arctic tundra of Europe (Miller and Evenson Citation2001).

While Miller and colleagues were exploring the Alaskan tundra, Canadian mycologist Scott Redhead provided clarification for the arctic species Gerronema pseudogrisella (Redhead Citation1980), published a detailed overview of Arrhenia in arctic North America (Redhead Citation1984b), studied agarics in wetlands of Canada (Redhead 1984a), and briefly recounted early agaricology for each Canadian territory, which included information on early arctic fungal collections (Redhead and Baillargeon Citation1999). Redhead (Citation1989) also focused on the biogeographical patterns of Canadian fungi and noted that fungal species found in the high Arctic and in alpine habitats appeared to have intercontinental distributions that match arctic and alpine floristic patterns. Around the same time, Hutchinson, Summerbell, and Malloch (Citation1988) noticed that a majority of the fungi they collected in Northern Quebec were also represented in arctic regions of Greenland and Northern Europe (Gulden, Jenssen, and Stordal Citation1985; Bresinksy Citation1987; Watling Citation1987). The observations of Durand (Citation1908), Linder (Citation1947), Miller, Laursen, and Farr (Citation1982), Redhead (Citation1984b), and Hutchinson, Summerbell, and Malloch (Citation1988) supported the hypothesis that a majority of arctic fungi have large intercontinental distributions with disjunct distributions in the alpine, an idea that would continue to dominate arctic and alpine mycological and botanical research.

Several Finnish mycologists visited arctic habitats in North America. Heli Heikkila and Paavo Kallio from Finland showed Omphalina to be one of the most common agaric genera in the arctic habitats of Northern Canada (Heikkila and Kallio Citation1966, Citation1969), and Kallio (Citation1980) surveyed the subarctic fungi of Schefferville, noting similarities to Finnish species. Seppo Huhtinen (Citation1982, Citation1985) reported on the Pezizales and Helotiales in Northern Labrador and Quebec, finding sixteen new species of these Ascomycota in North America. Finnish mycologists Esteri Ohenoja and Martti Ohenoja made trips to the Canadian Arctic, more specifically to Hudson Bay in 1971 and 1974 (Northwest Territories and Manitoba). Working independently and in collaboration with various authors, they studied Lactarius (Ohenoja and Ohenoja Citation1993); Inocybe (Ohenoja, Vauras, and Ohenoja Citation1998); Marasmius epidryas (Redhead et al. Citation1982); Ascomycota in Finland, noting that some distributions extended into North America (Ohenoja Citation1975); and fungal diversity at Rankin Inlet (Ohenoja Citation1972). They subsequently summarized their findings, primarily of agarics in the Canadian Arctic (Ohenoja and Ohenoja Citation2010), in Arctic and Alpine Mycology 8 (Cripps and Ammirati Citation2010). Norwegian mycologist Gro Gulden contributed knowledge on arctic and alpine species of Lepista from Alaska (Gulden Citation1983) and Galerina from Schefferville, Quebec (Noordeloos and Gulden Citation1992).

International Symposia on Arctic and Alpine Mycology (1980–2020)

On 16 August 1980, during the fruiting period for arctic and alpine fungi, an esteemed group of twenty-five mycologists from nine countries met at the Naval Arctic Research station in Point Barrow, Alaska. The First International Symposium on Arcto-Alpine Mycology (ISAM) was organized by acting president Gary Laursen. Many arctic and alpine mycologists were in attendance, including Savile, Miller, Kobayasi, Moser, Lamoure, Lange, Knudsen, and Horak. The symposium’s goal was to better understand fungi in arctic and alpine ecosystems, and the weeklong meeting produced valuable taxonomic information regarding the fungal community at Point Barrow (Laursen and Ammirati Citation1982a, Citation1982b). The format of the meeting consisted of several days of collecting fungi in the field followed by evening lectures to discuss proposed contributions to the proceedings. Because of the relative lack of knowledge on arcto–alpine fungi, the first ISAM focused on determining which fungi were present in these habitats. Fungal taxonomy would continue to dominate subsequent meetings.

After the first ISAM, it was decided that a select group of professional arctic and alpine mycologists would meet every four years in various countries to advance the knowledge of arctic and alpine fungi. At the end of each symposium, a representative would be selected to organize and act as sitting president for the next meeting. The format of the first ISAM has persisted through all ten symposia over thirty-six years, and more than one hundred different researchers have been involved in ISAM since its inception (Gulden and Høiland Citation2008; Cripps and Ammirati Citation2010). Each ISAM was held at an iconic arctic or alpine location, and all have improved our understanding of fungi in these environments. summarizes the research published in each proceedings that contributes information on arctic and alpine mycology in North America. The eleventh symposium is scheduled to be held in the Altai Mountains of Russia in 2021, with hosts Victor Muhkin and Anton Shiryaev.

Alpine mushrooms of the Rocky Mountains

Many mycologists have focused their attention on arctic fungi in Alaska and Canada over the last century, but little attention was paid to the alpine fungi in the mountainous regions of the continent. At the beginning of the twentieth century, researchers began reporting fleshy fungi from the Rockies (Overholtz Citation1919; Kauffman Citation1921; Seaver and Shope Citation1930; Solheim Citation1949; Smith Citation1975); however, no substantial research on true alpine fungi above treeline took place until the 1980s. Meinhard Moser, an Austrian mycologist, made several collecting trips to North America and visited alpine habitats in Yellowstone National Park, the Beartooth Plateau in Montana and Wyoming, and the Windriver Mountains of Wyoming. Moser primarily described Cortinarius species from these regions, including the endemic C. absarokensis, but he also reported the iconic Russula nana () for the first time from the Rocky Mountain alpine (Moser and McKnight Citation1987; Moser Citation1993; Moser, McKnight, and Sigl Citation1994; Moser, McKnight, and Ammirati Citation1995). Redhead (Citation1984b) reported Arrhenia lobata from Colorado after examining several of Alexander H. Smith’s collections from the Rocky Mountain alpine; A. lobata, usually growing on moss, is a common arctic–alpine species known from the Alps, Greenland, and Iceland; this species was previously referred to as Cantharellus lobatus on early Arctic expeditions.

Research into the fleshy fungi of alpine regions in North America, and especially the Rocky Mountains, was about to increase substantially. In 1996, Monique Gardes and Anders Dahlberg published a review on the diversity of mycorrhizal fungi in arctic and alpine regions. They observed the roots of mycorrhizal plant hosts and provided an overview of the mycorrhizal fungal genera present. Gardes and Dahlberg (Citation1996) studied various mycorrhizal associations, including arbuscular mycorrhizae, dark septate fungi, ectomycorrhizae, and ericoid mycorrhizas. The occurrence of these mycorrhizal types is variable, and certain arctic–alpine plants lack mycorrhizal associations completely (Gardes and Dahlberg Citation1996). In general terms, Gardes and Dahlberg identified the known mycorrhizal associations in cold-dominated environments as a potential model for understanding the evolution of mycorrhizal symbioses. They outlined future research questions requiring investigation and focused on the potential use of molecular tools to answer questions about fungal diversity and on mycorrhizal community structure and dynamics. Their review set the stage for future research into mycorrhizal fungi in alpine areas, especially for the Rocky Mountains.

A National Science Foundation–funded survey of alpine fungi in the Rocky Mountains commenced in 1999, led by Cathy Cripps and Egon Horak. They were the first to survey alpine fungi in the Rocky Mountains on a large scale, and their work focused on the central and southern regions. That same year, they presented a preliminary report on mushrooms in the Rocky Mountain alpine zone at the International Botanical Congress (Cripps and Horak Citation1999) and later disseminated information on alpine ectomycorrhizal species of Amanita, Inocybe, Russula, Lactarius, and Hebeloma at subsequent conferences (Cripps and Horak Citation2002; Cripps Citation2003; Cripps and Horak Citation2005, Citation2007; Cripps, Horak, and Mohatt Citation2008). This led to a paper that explored the diversity of Amanita in the Rocky Mountain alpine (Cripps and Horak Citation2010). A review paper on the mycorrhizal status of alpine plants, including those of the Beartooth Plateau, reported that 68 percent of alpine vascular plant species form mycorrhizal associations; the paper covered ecto-, arbuscular, ericoid, and arbutoid mycorrhizae, with arbuscular associations being the most common (Cripps and Eddington Citation2005). For decomposers, the well-known arcto-alpine fungus Arrhenia auriscalpium was reported in Colorado at the highest elevation (3,650 m) and the furthest latitude (39° N) south recorded for the fungus (Cripps and Horak Citation2006).

A preliminary list of alpine fungi in the Rocky Mountains was published in the proceedings of the seventh ISAM (Cripps and Horak 2008). It was estimated that at least 75 percent of the mushroom-producing fungi in the Rocky Mountain alpine appeared to be known from other arctic–alpine environments and that 25 percent were potentially endemic. Based on these findings, the most diverse mycorrhizal families in the Rocky Mountain alpine zone were reported to be the Cortinariaceae, Inocybaceae, and Hymenogastraceae (Hebeloma). It was hypothesized that the diverse geology, habitat, and mesic conditions of the southern Rockies led to more variation in habitat and thus greater fungal diversity than observed further north in Wyoming and Montana (Cripps and Horak 2008). However, the diversity of fungi that do not fruit aboveground was not assessed. Studies have shown that some, such as the Sebacinales, Cenococcum, and thelephoroids, can be dominant on roots in the alpine Alps (Ryberg, Larsson, and Molau Citation2009) and in the Arctic (Timling et al. Citation2014).

The molecular era

Early in the twenty-first century, molecular DNA methods became cheaper and easier to use, providing researchers with a powerful and independent way to verify taxonomic determinations based on morphology and to confirm intercontinental distributions. The nuclear ribosomal internal transcribed spacer (ITS) region eventually became commonly used as a universal DNA barcode marker for fungi (Schoch et al. Citation2012). Several of Cripps’ students investigated the fungi in the Rocky Mountain alpine zone using this method, focusing primarily on ectomycorrhizal genera. The genus Laccaria was investigated in the Rockies by Todd Osmundson (Osmundson, Cripps, and Mueller Citation2005). Phylogenetic analysis of the ITS region of ribosomal DNA, along with morphological and cultural data, revealed five species in the Rocky Mountain alpine zone. Laccaria laccata var. pallidifolia and L. nobilis were confirmed for the first time in alpine habitats and L. pseudomontana was described as new to science. The distribution, morphology, and phylogenetics of the genus Lactarius in the Rocky Mountain alpine zone was tackled by Ed Barge. Six species were reported, one new to science (Lactarius pallidomarginata), and all but the new endemic were molecularly confirmed using ITS/RPB2 sequence data to have intercontinental distributions in arctic–alpine regions (Barge and Cripps Citation2016; Barge, Cripps, and Osmundson Citation2016). It was hypothesized that species distributions may have been shaped by glaciation during the various ice ages, joint migration with host plants, and long-distance dispersal. The diversity of Russula in the Rocky Mountain alpine zone was examined by Chance Noffsinger using molecular (ITS/RPB2), morphological, and ecological data. Ten species were determined to be present, including the well-known Russula nana, R. laccata, and R. subrubens; all but a species near R. pascua were confirmed to have intercontinental distributions in arctic–alpine habitats (Noffsinger Citation2020). Additional molecular and morphological analyses have investigated the ectomycorrhizal genera Hebeloma (Becker, Eberhardt, and Vesterholt Citation2010; Cripps et al. Citation2019), Cortinarius (Peintner Citation2008), and Inocybe (Cripps, Larsson, and Horak Citation2010; Larsson, Vauras, and Cripps Citation2014, Citation2018; Cripps, Larsson, and Vauras Citation2020) in the Rocky Mountain alpine zone. All of these molecular studies have confirmed intercontinental distributions and disjunct populations of numerous alpine species, with the exception of Osmundson, Cripps, and Mueller (Citation2005), where only North American collections were examined.

Biogeography of Arctic and alpine fungi in North America

In the last decade, there has been a dramatic increase in the number of studies concerned with the biogeography and distribution of arctic fungi in North America. József Geml, a mycologist from Hungary, assessed the biodiversity of Lactarius in arctic tundra and boreal forests of Alaska using 95 and 97 percent ITS sequence similarity. He found strong habitat preference and a high diversity in the genus, noting that species richness appeared to decrease with increasing latitude (Geml et al. Citation2009). However, this study used operational taxonomic units as a proxy for species, which is common in ecological studies but does not clearly delimit species. A few studies have hypothesized that long-distance dispersal might play an important role in the distribution of arctic fungal genera (Geml et al. Citation2012; Timling et al. Citation2014). Others have assessed how mycorrhizal fungi are affected by climate change and a warming Arctic (Deslippe and Simard Citation2011; Deslippe et al. Citation2012; Geml et al. Citation2015, Citation2016; Morgado et al. Citation2015; Semenova et al. Citation2016). The current status of fungal diversity knowledge, especially lichens, was reviewed in Dahlberg and Bültmann (Citation2013). More recently, the taxonomic and ecological structure of larger fleshy fungi in polar deserts of the Northern Hemisphere was addressed by Shiryaev, Zmitrovich, and Ezhov (Citation2018), the cold adaptation strategies of fungi in polar regions was covered by Tsuji and Hoshino (Citation2019), and the upward shifts in fungal fruitings at treeline was reported by Diez et al. (Citation2020).

Biodiversity of alpine mushrooms in North America: Current knowledge

Approximately 170 species in fifty-one genera in twenty families of Basidiomycota are confirmed from alpine areas of North America, primarily from the Rocky Mountains, and data are newly compiled in . Fifty of these have been molecularly confirmed to have an intercontinental distribution in arctic–alpine habitats using ITS/RPB2 sequence data (), and more have been sequenced. Many of these species have also been reported from the North American Arctic, but most are not yet molecularly confirmed (Ohenoja and Ohenoja Citation2010). Of these, 104 are ectomycorrhizal species (61 percent) and 66 are saprophytic species (39 percent). The most species-diverse genera are Cortinarius (35), Inocybe including Mallocybe and Inosperma (27), Hebeloma (16), Russula (10), Lactarius (6), Laccaria (5), Entoloma (5+), and Galerina (8). All are potentially ectomycorrhizal genera except for Galerina and some species of Entoloma (Graf and Brunner Citation1996; Rinaldi, Comandini, and Kuyper Citation2008). Though these often appear to be the most diverse genera in arctic and alpine habitats, as indicated by aboveground structures, it is also possible that there has been collecting bias. Moser intensely collected Cortinarius in the Telamonia group, which was his specialty, and a majority of species listed are in this subgenus. Similarly, Cripps and Horak focused on Inocybe and Hebeloma with Beker and Eberhardt. Cripps’ students, as noted above, intensely searched for Laccaria, Lactarius, and Russula. In addition, eleven species of puffballs in genera Bovista, Bovistella, Calvatia, and Lycoperdon are reported, mostly by Taiga Kasuya of Japan, who attended ISAM 8 on the Beartooth Plateau (Kasuya Citation2010). Also, belowground data were not collected and, as mentioned before, it is possible that Sebacinales, Cenococcum, and thelephoroids could be dominant on roots as is found elsewhere (Ryberg, Larsson, and Molau Citation2009; Timling et al. Citation2014), but it remains to be seen whether this is also true for this part of the Rockies.

At the International Mycological Congress in 2002 in Oslo, Norway, Moser gave a talk titled “How Alpine Are ‘Alpine’ Fungi?,” a question that could be considered for arctic fungi as well (Moser Citation2002). Almost all of the arctic and alpine species in North American that have been sequenced are now confirmed to have intercontinental distributions; they also occur in Svalbard, Greenland, or arctic–alpine Europe. However, a majority of the Inocybe species, half of the Hebelomas, Lactarii, and Russulas listed (), are also reported from subalpine or boreal habitats, sometimes with Salix. Those that associate with dwarf Salix—for example, Lactarius nanus, Russula nana, and some Hebelomas—are more likely to be restricted to arctic and alpine habitats like their hosts. Even the so-called true alpine decomposer Arrhenia auriscalpium has been found below treeline, although it is rare (Cripps and Horak Citation2006). However, ecotypes and populations have not been studied in arctic and alpine fungi using new molecular techniques. Further, because many of the Rocky Mountain collections are not yet sequenced, is likely an underestimate of the diversity.

Table 2. Research in the proceedings of the international symposia on arctic and alpine mycology focused on North American fungi

Table 3. Current list of species of alpine Agaricales, Russulales, Boletales, and Ascomycota from the Rocky Mountains of Colorado, Montana, and Wyoming collected at elevations of ca. 3,000 to 4,200 m

Although new molecular techniques hold the promise of analyzing an entire fungal community in alpine or arctic soils in a timely manner, caution is advised when interpreting the results. Brunner et al. (Citation2017) compared historical morphological data generated by Favre (Citation1955) to data produced using novel high-throughput DNA sequencing techniques on soil cores. He concluded that these new techniques using 97 percent sequence similarity were effective at genus-level identification but often failed to effectively delineate species. The molecular analysis of soil found many species not known from alpine habitats and produced molecular errors that complicated the analyses (chimeric sequence formation, primer bias, etc.). These molecular techniques also have the potential to amplify DNA that may not represent metabolically active members of the soil community. A problem inherent to next-generation sequencing techniques or high-throughput sequencing data is that the length of the DNA fragments that can be sequenced (ca. 300 bp) is small and often not informative enough to delimit species. Further, they do not produce vouchers of fungal collections. Brunner et al. (Citation2017) stressed the importance of improving fungal DNA databases that will make high-throughput DNA sequencing techniques more effective in the future. The best way to improve fungal databases is through detailed taxonomic studies that combine morphological and molecular data, including the sequencing of type material when possible. The taxonomy of arctic and alpine fungi in North America is still poorly understood compared to that in arctic and alpine areas of Europe, but progress is being made. Taxonomic baseline data are necessary for understanding evolutionary, physiological, biogeographical, and climate trends. Research has already shown that climate change is altering arctic and alpine habitats at alarming rates (Serreze and Barry Citation2011; IPCC Citation2014), which highlights the importance of understanding these communities prior to large environmental shifts.

Acknowledgments

We thank Almut Horak and Don Bachman, who have contributed to our alpine mycological endeavors in North America since 1999. We also thank Todd Osmundson, Leslie Eddington, Sara Klingsporn, Angela Imhof, Erin Lonergan, and Ed Barge, who contributed as students to this project.

Disclosure statement

No potential conflict of interest was reported by the authors.

Funding

We acknowledge the National Science Foundation for the original grant (9971210) that initiated the discipline of alpine mycology in the Rocky Mountains. Fieldwork was supported by the John W. Marr Fund provided by the University of Colorado Boulder.

References

  • Ammirati, J. F., and G. A. Laursen. 1982. Cortinarii in Alaskan Arctic tundra. In Arctic and Alpine Mycology, The First International Symposium on Arcto-Alpine Mycology, ed. G. A. Laursen and J. F. Ammirati, 282–315. Seattle: University of Washington Press.
  • Antibus, R. K., J. G. Croxdale, O. K. Miller Jr., and A. E. Linkins. 1981. Ectomycorrhizal fungi of Salix rotundifolia. 3. Canadian Journal of Botany 59:2458–65. doi:https://doi.org/10.1139/b81-297.
  • Arthur, J. C. 1911. Some Alaskan and Yukon rusts. The Plant World 14 (10):233–36.
  • Barge, E. G., and C. L. Cripps. 2016. New reports, phylogenetic analysis, and a key to Lactarius Pers. in the Greater Yellowstone Ecosystem informed by molecular data. MycoKeys 15:1–58. doi:https://doi.org/10.3897/mycokeys.15.9587.
  • Barge, E. G., C. L. Cripps, and T. W. Osmundson. 2016. Systematics of the ectomycorrhizal genus Lactarius in the Rocky Mountain alpine zone. Mycologia 108 (2):414–40. doi:https://doi.org/10.3852/15-177.
  • Becker, H. J., U. Eberhardt, and J. Vesterholt. 2010. Hebeloma hiemale Bres. in Arctic/Alpine Habitats. North American Fungi 5:51–65.
  • Berkeley, M. J. 1839. XLII. Descriptions of exotic fungi in the collection of Sir W. J. Hooker, from memoirs and notes of J.F. Klotzsch, with additions and corrections. Journal of Natural History 3 (19):375–401.
  • Berkeley, M. J. 1878. Enumeration of the fungi collected during the Arctic expedition, 1875–76. Journal of the Linnaean Society, Botany 17:13–17. doi:https://doi.org/10.1111/j.1095-8339.1878.tb00453.x.
  • Bigelow, H. E. 1959. Notes of fungi from northern Canada IV. Tricholomataceae. Canadian Journal of Botany 37 (5):769–79. doi:https://doi.org/10.1139/b59-062.
  • Bigelow, H. E. 1970. Omphalina in North America. Mycologia 62 (1):1–32. doi:https://doi.org/10.1080/00275514.1970.12018941.
  • Bizio, E. 1995. Alcune Inocybe più frequenti della zona alpine delle Dolomiti. Rivista di Micologia 38 (2suppl.):1–60.
  • Bizio, E. 1997. Alcune Inocybe più frequenti della zona alpine delle Dolomiti: 2nd contribution. Rivista di Micologia 40 (4):339–62.
  • Boertmann, D., and H. Knudsen. 2006. Arctic and alpine mycology 6. Meddelelser om Grønland, Bioscience 56:1–161.
  • Bon, M. 1985. Stage Mycologie Alpine Lanslebourg (Savoie) du 1 au 3 septembre 1984. Bulletin trimestriel de la fédération mycologique dauphiné-savoie 96:19–25.
  • Bon, M. 1987. Quelques recoltes mycologiques de la zone alpine au 7ème convegno di micologia. Fiera di Primiero (Italie). Micologia Italiana 17 (3):267–70.
  • Bon, M. 1991. Inventaires des espéces récoltees au stage de mycologie alpine. Bulletin trimestriel de la fédération mycologique dauphiné-savoie 122:25–28.
  • Bon, M. 1993. Russules alpine nouvelles ou intéressantes. Bulletin trimestriel de la fédération mycologique dauphiné-savoie 128:20–24.
  • Borgen, T. 2006. Distribution of selected basidiomycetes in oceanic dwarf-scrub heaths in the Paamiut area, low arctic South Greenland. Meddelelser om Grøenland, Bioscience 56:25–36.
  • Borgen, T., S. A. Elborne, and H. Knudsen. 2006. A checklist of the Greenland basidiomycetes. Meddelelser om Grøenland, Bioscience 56:37–59.
  • Bresinksy, A. 1987. Bemerkenswerte Grosspilzfunde in der Bundersrepublik Deutschland. Zeitschrift für Mykologie 53:289–302.
  • Brown, R. 1823. A list of plants collected in Melville Island in the year 1820; by the officers of the voyage of Discovery under the orders of Captain Parry. Chloris Melvilliana, 49. London: Printed by W. Clowes, Northumberland-Court, Strand.
  • Brunner, I., B. Frey, M. Hartmann, S. Zimmermann, F. Graf, L. M. Suz, T. Niskanen, M. I. Bidartondo, and B. Senn-Irlet. 2017. Ecology of alpine macrofungi-combining historical with recent data. Frontiers in Microbiology 8:e2066. doi:https://doi.org/10.3389/fmicb.2017.02066.
  • Bunnell, F. L., O. K. Miller Jr., P. W. Flanagan, and R. E. Benoit. 1980. The microflora: Composition, biomass, and environmental relations. In An Arctic ecosystem. The coastal tundra at Barrow, Alaska. US/IBP synthesis series 120, ed. J. Brown, P. Miller, L. L. Tieszen, and F. L. Bunnell, 255–90.  Stroudsburg, PA: Dowden, Hutchingon and Ross, Inc.
  • Cash, E. K. 1953. A checklist of Alaskan fungi. The Plant Disease Reporter 219:3–70.
  • Christiansen, M. P. 1941. Studies in the larger fungi of Iceland. The Botany of Iceland 3 (2):187–227.
  • Corriol, G. 2008. Checklist of Pyrenean alpine-stage macrofungi. Sommerfeltia 31:29–99. doi:https://doi.org/10.2478/v10208-011-0004-6.
  • Cripps, C. and E. Barge. 2014. Notes on the genus Lactarius from the Rocky Mountain alpine zone in regard to Finnish arctic alpine species. Karstenia 53:29–37.
  • Cripps, C. L. 2003. Interesting distributions of ectomycorrhizal alpine fungi along the Rocky Mountain cordillera. Pacific Grove, CA: Mycological Society of America. July 27–31.
  • Cripps, C. L. 2010. Orson K. Miller Jr., 1930–2006. Mycologia 102 (5):1216–20. doi:https://doi.org/10.3852/10-042.
  • Cripps, C. L., and E. Horak. 1999. Alpine Mycota (Agaricales) Rocky Mountain Tundra, USA: A preliminary report. St. Louis, MO: International Botanical Congress. August 6.
  • Cripps, C. L., and E. Horak. 2002. Alpine species of Lactarius in the Rocky Mountains. Corvallis, OR: Mycological Society of America. June 24–26.
  • Cripps, C. L., and E. Horak. 2005. Amanita in the Rocky Mountain Alpine Zone: Where mycorrhizal mushrooms tower over miniature forests. Hilo, HI: Joint meeting of Japanese Mycological Society and Mycological Society of America. July 30-August 5.
  • Cripps, C. L., and E. Horak. 2006. Arrhenia auriscalpium in arctic-alpine habitats: World distribution, ecology, new reports from the southern Rocky Mountains, USA. In Arctic and alpine mycology 6. Meddelelser  om Grønland, Bioscience 56, ed. D. Boertmann and H. Knudsen, 17–24.
  • Cripps, C. L., and E. Horak. 2007. Alpine agarics with Dryas octopetala (Rosaceae) in arctic-alpine habitats of the Rocky Mountains (USA). Baton Rouge, LA: Mycological Society of American meeting. August 6–9.
  • Cripps, C. L., and E. Horak. 2008. Checklist and ecology of the Agaricales, Russalales and Boletales in the alpine zone of the Rocky Mountains (Colorado, Montana, Wyoming) at 3000–4000 m asl. Sommerfeltia 31:101–23. doi:https://doi.org/10.2478/v10208-011-0005-5.
  • Cripps, C. L., and E. Horak. 2010. Amanita in the Rocky Mountain alpine zone, USA: New records for A. nivalis and A. groenlandica. North American Fungi 5:9–21.
  • Cripps, C. L., E. Horak, and K. Mohatt. 2008. Ectomycorrhizal fungi at alpine treeline in the Rocky Mountains: Baseline data and a review in the context of climate change. MTNCLIME. June 9–12. Consortium for Integrated Climate Change Research in Western Mountains, Silverton, CO.
  • Cripps, C. L., E. Larsson, and E. Horak. 2010. Subgenus Mallocybe (Inocybe) in the Rocky Mountain alpine zone with molecular reference to European arctic-alpine material. North American Fungi 5:97–126.
  • Cripps, C. L., E. Larsson, and J. Vauras. 2020. Nodulose-spored Inocybe from the Rocky Mountain alpine zone molecularly linked to European and type specimens. Mycologia 121 (1):1–21.
  • Cripps, C. L., and J. Ammirati. 2010. Eighth International Symposium on Arctic-Alpine Mycology (ISAM 8), Beartooth Plateau, Rocky Mountains, USA 2008. North American Fungi 5:232.
  • Cripps, C. L., and L. H. Eddington. 2005. Distribution of mycorrhizal types among alpine vascular plant families on the Beartooth Plateau, Rocky Mountains, USA, in reference to large-scale patterns in arctic-alpine habitats. Arctic, Antarctic, and Alpine Research 37 (2):177–88. doi:https://doi.org/10.1657/1523-0430(2005)037[0177:DOMTAA]2.0.CO;2.
  • Cripps, C. L., U. Eberhardt, N. Schütz, H. J. Beker, V. S. Evenson, and E. Horak. 2019. The genus Hebeloma in the Rocky Mountain Alpine Zone. MycoKeys 46:1–54. doi:https://doi.org/10.3897/mycokeys.46.32823.
  • Dahlberg, A., and H. Bültmann. 2013. Fungi. Chapter 10. In Arctic Biodiversity Assessment. Status and Trends in Arctic Biodiversity. Conservation of Arctic Flora and Fauna (CAFF), ed. H. Meltofte, 354–71. Denmark: Narayana Press.
  • Dearness, J. 1923. The fungi of the Arctic Coast of America West of the 100th meridian. Report of the Canadian Arctic Expedition 1913–1918. Volume IV: Botany. Part C: Fungi, 1–24. Ottawa: F. A. Acland.
  • Dearness, J. 1928. Report on fleshy fungi collected in August 1926. In A faunal investigation of southern Baffin Land. National Museum of Canada Bulletin no. 53 Biological Series, ed. J. D. Soper, 120–23. Ottawa: Dept. of Mines and Resources, National Museum of Canada.
  • Deslippe, J. R., M. Hartmann, S. W. Simard, and W. W. Mohn. 2012. Long-term warming alters the composition of Arctic soil microbial communities. FEMS Microbiology Ecology 82 (2):303–15. doi:https://doi.org/10.1111/j.1574-6941.2012.01350.x.
  • Deslippe, J. R., and S. W. Simard. 2011. Below-ground carbon transfer among Betula nana may increase with warming in Arctic tundra. New Phytologist 192 (3):689–98. doi:https://doi.org/10.1111/j.1469-8137.2011.03835.x.
  • Desmond, R. 1995. Kew: The history of the Royal Botanic Gardens, 150–238. London: The Harvill Press.
  • Diez, J., H. Kauserud, C. Andrew, E. Heegaard, I. Krisai-Greilhuber, B. Senn-Irlet, K. Høiland, S. Egli, and U. Büntgen. 2020. Altitudinal upwards shifts in fungal fruiting in the Alps. Proceedings of the Royal Society B: Biological Sciences 287:20192348. doi:https://doi.org/10.1098/rspb.2019.2348.
  • Durand, E. J. 1908. The Geoglossaceae of North America. Annales Mycologici 6:387–477.
  • Estey, R. H. 1994. Essays on the early history of plant pathology and mycology in Canada, 383. Montreal, QC: McGill-Queen’s University Press.
  • Farr, D. F., and O. K. Miller Jr. 1972. Notes on arctic and subarctic Basidiomycetes. Virginia Journal of Science 23:120.
  • Favre, J. 1955. Les champignons supérieurs de la zone alpine du Parc National Suisse. Resultats des recherches scientifiques enterprises au Parc National Suisse. Ergebnisse der wissenschaftlichen Untersuchungen des schweizerischen National Parks 5:212.
  • Gardes, M., and A. Dahlberg. 1996. Mycorrhizal diversity in Arctic and alpine tundra: An open question. New Phytologist 133 (1):147–57. doi:https://doi.org/10.1111/j.1469-8137.1996.tb04350.x.
  • Geml, J., G. A. Laursen, I. Timling, J. M. McFarland, M. G. Booth, N. Lennon, C. Nusbaum, and D. L. Taylor. 2009. Molecular phylogenetic biodiversity assessment of arctic and boreal ectomycorrhizal Lactarius Pers. (Russulales; Basidiomycota) in Alaska, based on soil and sporocarp DNA. Molecular Ecology 18 (10):2213–27. doi:https://doi.org/10.1111/j.1365-294X.2009.04192.x.
  • Geml, J., I. Timling, C. H. Robinson, N. Lennon, H. C. Nusbaum, C. Brochmann, M. E. Noordeloos, and D. L. Taylor. 2012. An arctic community of symbiotic fungi assembled by long-distance dispersers: Phylogenetic diversity of ectomycorrhizal basidiomycetes in Svalbard based on soil and sporocarp DNA. Journal of Biogeography 39 (1):74–88. doi:https://doi.org/10.1111/j.1365-2699.2011.02588.x.
  • Geml, J., L. N. Morgado, T. A. Semenova, J. M. Welker, M. D. Walker, and E. Smets. 2015. Long-term warming alters richness and composition of taxonomic and functional groups of arctic fungi. FEMS Microbiology Ecology 91 (8):fiv095. doi:https://doi.org/10.1093/femsec/fiv095.
  • Geml, J., T. A. Semenova, L. N. Morgado, and J. M. Welker. 2016. Changes in composition and abundance of functional groups of arctic fungi in response to long-term summer warming. Biology Letters 12 (11):20160503. doi:https://doi.org/10.1098/rsbl.2016.0503.
  • Gillman, L. S., and O. K. Miller Jr. 1977. A study of the boreal, alpine, and arctic species of Melanoleuca. Mycologia 69 (5):927–51. doi:https://doi.org/10.1080/00275514.1977.12020146.
  • Graf, F. 1994. Ecology and sociology of macromycetes in snow-beds with Salix herbacea L. in the alpine valley of Radönt (Grisons, Switzerland). Dissertationes Botanicae 235:242.
  • Graf, F., and I. Brunner. 1996. Natural and synthesized ectomycorrhizas of the alpine dwarf willow Salix herbacea. Mycorrhiza 6:227–35. doi:https://doi.org/10.1007/s005720050130.
  • Gulden, G. 1983. Studies in Lepista (Fr.) W.G. Smith. Section Lepista (Basidiomycotina, Agaricales). Sydowia: Annales mycologici 36:59–73.
  • Gulden, G., and A. E. Torkelsen. 1996. Fungi I. Basidiomycota: Agaricales, Gasteromycetales, Aphyllophorales, Exobadisiales and Tremellales. Skrifter-Norsk Polarinstitutt 198:173–206.
  • Gulden, G., and K. Høiland. 2008. ISAM VII at Finse, Norway, 2005. Sommerfeltia 31:7–16. doi:https://doi.org/10.2478/v10208-011-0002-8.
  • Gulden, G., K. M. Jenssen, and J. Stordal. 1985. Arctic and alpine fungi, Vol. 1, 61. Oslo, Norway: Lubrecht & Cramer Ltd. Soppkonsulenten.
  • Hallgrimsson, H. 1998. Checklist of Icelandic fungi V: Agarics. Natturufraedistornun Islands. Akureyri, Iceland: Akureyri Museum of Natural History.
  • Haselwandter, K. 2007. Mycorrhiza in the alpine timberline ecotone: Nutritional implications. In Trees at their upper limit, ed. G. Wieser and M. Tausz, 57–66. The Netherlands: Springer.
  • Heikkila, H., and P. Kallio. 1966. On the problem of subarctic basidiolichens I. Reports from the Kevo Subarctic Research 3:48–74.
  • Heikkila, H., and P. Kallio. 1969. On the problem of subarctic basidiolichens II. Reports from the Kevo Subarctic Research 4:90–97.
  • Hooker, J. D. 1860. An account of the plants collected by Dr. Walker in Greenland and Arctic America during the expedition of Sir Francis M’Clintock, RN, in the Yacht ‘Fox.’. Botanical Journal of the Linnaean Society 5 (18):79–89.
  • Horak, E. 1987a. Astrosporina in the alpine zone of the Swiss National Park (SNP) and adjacent regions. In Arctic and alpine mycology, ed. G. Laursen, J. Ammirati, and S. A. Redhead, 205–34. ISAM II.
  • Horak, E. 1987b. Revision der von J. Favre aus der Region des Schweizer Nationalparkes beschriebenen alpinen Arten von Cortinarius subgen. Telamonia (Agaricales). Candollea 42:771–803.
  • Horak, E. 1993. Entoloma in the alpine zone of the Alps: 1. Revision of the taxa described by J. Favre (1955). - 2. New records from the Swiss National Park and other locations in the Alps. Bibliotheca Mycologica 150:63–91.
  • Horak, E., and O. K. Miller Jr. 1992. Phaeogalera and Galerina in arctic-subarctic Alaska (USA) and the Yukon Territory (Canada). Canadian Journal of Botany 70 (2):414–33. doi:https://doi.org/10.1139/b92-055.
  • Hoshino, T., N. Tuno, Y. Degawa, T. Kasuya, Y. Yajima, E. Kawahara, and I. Nose. 2018. The 10th International Symposium on Arctic and Alpine Mycology. Mycoscience 30:1–2.
  • Huhtinen, S. 1982. Ascomycetes from central and northern Labrador. Karstenia 22:1–8. doi:https://doi.org/10.29203/ka.1982.206.
  • Huhtinen, S. 1985. Mycoflora of Poste-de-la-Baleine, northern Quebec: Ascomycetes. Le Naturaliste Canadien 112 (4):473–524.
  • Hutchinson, L. J., R. C. Summerbell, and D. W. Malloch. 1988. Additions to the mycota of North America and Quebec: Arctic and boreal species from Schefferville, northern Quebec. Le Naturaliste Canadien 115:39–56.
  • IPCC. 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, R. K. Pachauri and L. A. Meyer, eds]. IPCC, Geneva, Switzerland, 151 pp.
  • Jalink, L. 2010. Additional notes on the Lycoperdaceae of the Beartooth Plateau. North American Fungi 5:173–180.
  • Jamoni, P. G. 1995. Russulaceae della zona alpine. Proposta di chiavi di determinazione per le specie crescent nella zona alpina delle Alpi. Rivista di Micologia 2:75–80.
  • Jamoni, P. G. 2008. Funghi alpini, delle zone alpine superiori e inferiori, 543. Trento: Association Micologica Bresadola, Fondazione centro Studi Micologici.
  • Jennings, O. E. 1936. The exploration of Southampton Island, Hudson Bay. 3. Botany. 1. Algae and fungi. Memoirs of the Carnegie Museum 12 (3):1–4.
  • Kallio, P. 1980. Some observations on the fungi of the central Québec-Labrador peninsula. McGill Subarctic Research Report 30:1–16.
  • Kankainen, E. 1969. On the structure, ecology, and distribution of the species of Mitrula s. lat. Karstenia 9:23–34. doi:https://doi.org/10.29203/ka.1969.56.
  • Kasuya, T. 2010. Lycoperdaceae (Agaricales) on the Beartooth Plateau, Rocky Mountains, USA. North American Fungi 5:159–71.
  • Kauffman, C. H. 1921. The mycological flora of the higher Rockies of Colorado. Papers of the Michigan Academy of Science, Arts and Letters 1:101–50.
  • Knudsen, H., and T. Borgen. 1982. Russulaceae in Greenland. In Arctic and alpine mycology 1, ed. G. A. Laursen and J. F. Ammirati, 216–44. Seattle: University of Washington Press.
  • Kobayasi, Y. 1982. Ecology and distribution of Arctic lower fungi. In Arctic and Alpine Mycology 1, ed. G. A. Laursen and F. J. Ammirati, 16–26. Seattle: University of Washington Press.
  • Kobayasi, Y., H. Hiratsuka, K. Aoshima, R. Korf, M. Soneda, K. Tubaki, and J. Sugiyama. 1967. Mycological studies of the Alaskan Arctic, 138. Osaka: Annual Report of the Institute for Fermentation.
  • Körner, C. 1995. Alpine plant diversity: A global survey and functional interpretations. In Arctic and Alpine Biodiversity: Patterns, causes and ecosystem consequences. Ecological studies 113, ed. F. S. Chapin III and C. Körner, 45–62. New York: Springer-Verlag.
  • Körner, C. 1999. Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems, 338. Berlin: Springer-Verlag.
  • Körner, C. 2012. Alpine treelines, 220. Basel, Switzerland: Springer.
  • Kühner, R. 1975. Agaricales de la zone alpine. Genre Russula Pers. ex SF Gray. Bulletin trimestriel de la Société Mycologique de France 91 (3):314–90.
  • Lamoure, D. 1982. Agaricales de la zone alpine du Parc National des Ecrins. Travaux scientifiques du Parc national des Ecrins 2:119–23.
  • Lange, M. 1957. Macromycetes. Part III. I. Greenland Agaricales (Pars.), Macromycetes caeteri. II. Ecological and Plant Geographical Studies 148 (2):1–125.
  • Larsson, E., J. Vauras, and C. L. Cripps. 2014. Inocybe leiocephala, a species with an intercontinental distribution range–disentangling the I. leiocephala–subbrunnea–catalaunica morphological species complex. Karstenia 54:15–39. doi:https://doi.org/10.29203/ka.2014.461.
  • Larsson, E., J. Vauras, and C. L. Cripps. 2018. Inocybe praetervisa group–A clade of four closely related species with partly different geographical distribution ranges in Europe. Mycoscience 59 (4):277–87. doi:https://doi.org/10.1016/j.myc.2017.11.002.
  • Laursen, G., and M. Chmielewski. 1982. The ecological significance of soil fungi in Arctic Tundra. In Arctic and alpine mycology 1, ed. G. A. Laursen and F. J. Ammirati, 432–492. Seattle: University of Washington Press.
  • Laursen, G. A., and H. H. Burdsall Jr. 1976. Notes concerning a new distribution record for Geopora (Pezizales) from Alaskan tundra. Mycotaxon 4 (2):329–30.
  • Laursen, G. A., and J. F. Ammirati. 1982a. Arctic and alpine mycology: First International Symposium on Arctic-Alpine Mycology, 559. Seattle: University of Washington Press.
  • Laursen, G. A., and J. F. Ammirati. 1982b. Citation index to Arctic and alpine mycology. The First International Symposium on Arctic and Alpine Mycology, vol. 84–3, 561–602. University of Alaska-Fairbanks Misc. Pub.
  • Laursen, G. A., J. F. Ammirati, and D. F. Farr. 1987a. Hygrophoraceae from arctic and alpine tundra in Alaska. In Arctic and alpine mycology 2. Environmental science research 34, ed. G. A. Laursen, J. F. Ammirati, and S. A. Redhead, 273–86. New York, NY: Plenum Press.
  • Laursen, G. A., J. F. Ammirati, and S. A. Redhead. 1987b. Arctic and alpine mycology 2. Environmental science research 34, 364. New York, NY: Plenum Press.
  • Laursen, G. A., O. K. Miller Jr., and H. E. Bigelow. 1976. A new Clitocybe from the Alaskan arctic. Canadian Journal of Botany 54 (9):976–80. doi:https://doi.org/10.1139/b76-103.
  • Lind, J. 1910. Fungi (Micromycetes) collected in Arctic North America (King William Land, King Point and Herschell Isl.) by the Gjöa expedition under Captain Roald Amundsen 1904–1906. Videnskabs-Selskabets Skrifter 1. Mathematisk-Naturvidenskabelig Klasse 9. Christiania (Oslo): Jacob Dybwad.
  • Linder, D. H. 1947. Fungi. In Botany of the Canadian Eastern Arctic. Part II: Thallophyta and bryophyta. National Museum of Canada bulletin no. 97 Biological Series no. 26, ed. N. Polunin, 234–96. Ottawa: Dept. of Mines and Resources, National Museum of Canada.
  • Linkins, A., and R. Antibus. 1982. Mycorrhizae of Salix rotundifolia. In Arctic and alpine mycology 1, ed. G. A. Laursen and F. J. Ammirati, 509–531. Seattle: University of Washington Press.
  • M’Clintock, F. L. 1860. The voyage of the “Fox” in the Arctic seas: A narrative of the discovery of the fate of Sir John Franklin and his companions. London: John Murray.
  • Mains, E. B. 1955. North American hyaline-spored species of the Geoglossaceae. Mycologia 47 (6):846–77. doi:https://doi.org/10.1080/00275514.1955.12024501.
  • Miller, O. K., Jr. 1968. Interesting fungi of the St. Elias Mountains, Yukon Territory, and adjacent Alaska. Mycologia 60 (6):1190–203. doi:https://doi.org/10.1080/00275514.1968.12018686.
  • Miller, O. K., Jr. 1969. Notes on gastromycetes of the Yukon Territory and adjacent Alaska. Canadian Journal of Botany 47 (2):247–50. doi:https://doi.org/10.1139/b69-034.
  • Miller, O. K., Jr. 1982a. Higher fungi in Alaskan subarctic tundra and taiga plant communities. In The First International Symposium on Arcto-Alpine Mycology, ed. G. A. Laursen and J. F. Ammirati, 123–49. Seattle: University of Washington Press.
  • Miller, O. K., Jr. 1982b. Mycorrhizae, mycorrhizal fungi and fungal biomass in subalpine tundra at Eagle Summit, Alaska. Holarctic Ecology 5:125–34.
  • Miller, O. K., Jr. 1987. Higher fungi in tundra and subalpine tundra from the Yukon territory and Alaska. In Arctic and alpine mycology 2, ed. G. A. Laursen and J. F. Ammirati, 287–97. New York, NY: Plenum Press.
  • Miller, O. K., Jr. 1993. Observations on the genus Cystoderma in Alaska. In Arctic and alpine mycology 3. Bibliotheca mycologica 150, ed. O. Petrini and G. A. Laursen, 161–69. Berlin-Stuttgart: J. Cramer in der Gebrüder Borntraeger Verlagsbuchhandlung.
  • Miller, O. K., Jr. 1998. Hebeloma in the Arctic and alpine tundra in Alaska. In Arctic and alpine mycology 5. Proceedings of the 5th International Symposium on Arcto-Alpine Mycology. Labytnangi, Russia, ed. V. A. Mukhin and H. Knudsen, 86–97. Yekaterinburg, Russia: Yekaterinburg Publishers.
  • Miller, O. K., Jr., and G. A. Laursen. 1978. Ecto- and ectendo-mycorrhizae of arctic plants at Barrow, Alaska. In Vegetation and production ecology of an Alaskan Arctic tundra. Ecological studies 29, ed. L. L. Tieszen, 229–37. New York, NY: Springer.
  • Miller, O. K., Jr., G. A. Laursen, and B. M. Murray. 1973. Arctic and alpine agarics from Alaska and Canada. Canadian Journal of Botany 51 (1):43–49. doi:https://doi.org/10.1139/b73-007.
  • Miller, O. K., Jr., G. A. Laursen, and D. F. Farr. 1982. Notes on Agaricales from Arctic tundra in Alaska. Mycologia 74 (4):576–91. doi:https://doi.org/10.1080/00275514.1982.12021553.
  • Miller, O. K., Jr., G. A. Laursen, and W. F. Calhoun. 1974. Higher fungi in arctic plant communities. U.S. Tundra Biome Ecosystem Analysis Studies 7:1–7.
  • Miller, O. K., Jr., H. H. Burdsall, G. A. Laursen, and I. B. Sachs. 1980. The status of Calvatia cretacea in arctic and alpine tundra. Canadian Journal of Botany 58 (24):2533–42. doi:https://doi.org/10.1139/b80-295.
  • Miller, O. K., Jr., and V. S. Evenson. 2001. Observations on the alpine tundra species of Hebeloma in Colorado. Gilbertson honorary volume. Harvard Papers in Botany 6:155–62.
  • Morgado, L. N., T. A. Semenova, J. M. Welker, M. D. Walker, E. Smets, and J. Geml. 2015. Summer temperature increase has distinct effects on the ectomycorrhizal fungal communities of moist tussock and dry tundra in Arctic Alaska. Global Change Biology 21 (2):959–72. doi:https://doi.org/10.1111/gcb.12716.
  • Moser, M. and E. Horak. 2006. Agrocybe praemagna; a new alpine species from Colorado, Idaho and Wyoming, Rocky Mountains, USA. In Arctic and alpine mycology 6, ed. D. Boertmann and H. Knudsen, Meddelelser om Grøenland, Bioscience 56:133–138.
  • Moser, M. M. 1993. Studies on North American Cortinarii. III. The Cortinarius flora of dwarf and shrubby Salix associations in the alpine zone of the Windriver Mountains, Wyoming, USA. Sydowia 45:275–306.
  • Moser, M. M. 2002. How alpine are “alpine” fungi? Paper presented at International Mycological Congress (IMC7), August 11–17, Oslo, Norway. http://plantsciences.montana.edu/alpinemushrooms/imc7.html.
  • Moser, M. M., and K. H. McKnight. 1987. Fungi (Agaricales, Russulales) from the alpine zone of Yellowstone National Park and the Beartooth Mountains with special emphasis on Cortinarius. In Arctic and alpine mycology 2, ed. G. A. Laursen and J. F. Ammirati, 299–317. New York, NY: Plenum Press.
  • Moser, M. M., K. H. McKnight, and J. F. Ammirati. 1995. Studies on North American Cortinarii I. New and interesting taxa from the greater Yellowstone area. Mycotaxon 60:301–46.
  • Moser, M. M., K. H. McKnight, and M. Sigl. 1994. The genus Cortinarius (Agaricales) in the Greater Yellowstone Area: Mycorrhizal host associations and taxonomic considerations. In Plants and their environments, Proceedings of the First Biennial Scientific Conference on the Greater Yellowstone Ecosystem, ed. D. G. Despain, 239–46. Denver, CO: US Department of the Interior National Park Service, Natural Resources Publications Office.
  • Mukhin, V. A., and H. Knudsen. 1998. Arctic and alpine mycology 5. Russian Academy of Sciences: Ural Division, 172. Yekaterinburg: Yekaterinburg Publishers.
  • Nares, G. 2011. Narrative of a voyage to the Polar Sea during 1875–6 in HM ships alert and discovery: With notes on the natural history, Vol. 1. Cambridge, UK: Cambridge University Press.
  • Nauta, M. 2010. Notes on Mollisioid Ascomycetes from the Beartooth Plateau, Rocky Mountains, USA. North American Fungi 5:181–186.
  • Neatby, L. H., and K. Mercer. 2008. Sir John Franklin. The Canadian encyclopedia. Historica Canada. Accessed April 9, 2019. https://www.thecanadianencyclopedia.ca/en/article/sir-john-franklin.
  • Noffsinger, C. R. 2020. Systematics of Russula in the Rocky Mountain alpine zone. Ms. Thesis, Montana State University.
  • Noordeloos, M., and G. Gulden. 1992. Studies in the genus Galerina from the Shefferville area on the Québec-Labrador Peninsula, Canada. Persoonia-Molecular Phylogeny and Evolution of Fungi 14 (4):625–39.
  • Ohenoja, E. 1972. Preliminary note on the botanical research at Rankin Inlet, 1971. Musk-Ox 10:67.
  • Ohenoja, E. 1975. Leotia, Cudonia, Spathularia and Neolecta (Ascomycetes) in Finland. Annals Botanici Fennici 12:123–30.
  • Ohenoja, E., A. L. Ruotsalainen, and J. Vauras. 2018. Mycological records from ISAM 9, Kevo, Finland. Mycoscience 59 (4):263–67. doi:https://doi.org/10.1016/j.myc.2017.12.003.
  • Ohenoja, E., J. Vauras, and M. Ohenoja. 1998. The Inocybe species found in the Canadian Arctic and west Siberian sub-arctic, with ecological notes. In Arctic and alpine mycology 5. Russian Academy of Sciences: Ural Division, ed. V. A. Mukhin and H. Knudsen, 106–21. Yekaterinburg: Yekaterinburg Publishers.
  • Ohenoja, E., and M. Ohenoja. 1993. Lactarii of the Franklin and Keewatin districts of the Northwest Territories, Arctic Canada. In Arctic and Alpine mycology 3–4, ed. O. Petrini and G. A. Laursen, 179–92. Stuttgart, Berlin: J Cramer.
  • Ohenoja, E., and M. Ohenoja. 2010. Larger fungi of the Canadian arctic. North American Fungi 5:85–96.
  • Osmundson, T. W., C. L. Cripps, and G. M. Mueller. 2005. Morphological and molecular systematics of Rocky Mountain alpine Laccaria. Mycologia 97 (5):949–72. doi:https://doi.org/10.1080/15572536.2006.11832746.
  • Overholtz, L. 1919. Some Colorado fungi. Mycologia 11 (5):245–58. doi:https://doi.org/10.1080/00275514.1919.12016799.
  • Parmelee, J. A. 1969. Fungi of Central Baffin Island. Canadian Field Naturalist 83:48–53.
  • Peintner, U. 2008. Cortinarius alpinus as an example for morphological and phylogenetic species concepts in ectomycorrhizal fungi. Sommerfeltia 31:161–77. doi:https://doi.org/10.2478/v10208-011-0009-1.
  • Peintner, U., and M. Moser. 1996. The mycobiota (Basidiomycetes) of an Alpine Tyrolean Valley. Phyton (Horn Austria) 36 (4):65–82.
  • Peterson, P. M. 1977. Investigations on the ecology and phenology of the macromycetes in the Arctic. Meddelelser  om Grønland, Bioscience 199:2–72.
  • Petrini, O., and G. A. Laursen. 1993. Arctic and alpine mycology 3–4. Bibliotheca Mycologica 150:269.
  • Polunin, N. 1934. The Flora of Akpatok Island, Hudson Strait. Journal of Botany 72:197–204.
  • Polunin, N. 1940. Botany of the Canadian eastern Arctic. Part I. Pteridophyta and Spermatophyta. National Museum of Canada Bulletin No. 92 Biological Series no. 24, 395. Ottawa: Dept. of Mines and Resources, National Museum of Canada.
  • Polunin, N. 1947. Botany of the Canadian Eastern Arctic. Part II: Thallophyta and bryophyta. National Museum of Canada Bulletin No. 97 Biological Series No. 26.  Ottawa: Dept. of Mines and Resources, National Museum of Canada.
  • Rau, T. G. 1977. Fungi in decomposing litter from tundra plants near Barrow, Alaska, 53. Ms. Thesis, Virginia Polytechnic Institute and State University.
  • Redhead, S. A. 1980. Gerronema pseudogrisella. Fungi Canadenses no. 170. Ottawa: Agriculture Canada.
  • Redhead, S. A. 1984a. Additional Agaricales on wetland Monocotyledoneae in Canada. Canadian Journal of Botany 62:1844–51. doi:https://doi.org/10.1139/b84-251.
  • Redhead, S. A. 1984b. Arrhenia and Rimbachia, expanded generic concepts, and a reevaluation of Leptoglossum with emphasis on muscicolous North American taxa. Canadian Journal of Botany 62 (5):865–92. doi:https://doi.org/10.1139/b84-126.
  • Redhead, S. A. 1989. A biogeographical overview of the Canadian mushroom flora. Canadian Journal of Botany 67 (10):3003–62. doi:https://doi.org/10.1139/b89-384.
  • Redhead, S. A., and G. Baillargeon. 1999. Fungal database development and early historical records of mushrooms from Canada. McIlvainea 14 (1):73–82.
  • Redhead, S. A., O. K. Miller Jr., R. Watling, and E. Ohenoja. 1982. Marasmius epidryas. Fungi Canadensis No. 213. Ottawa: Agriculture Canada.
  • Rinaldi, A. C., O. Comandini, and T. W. Kuyper. 2008. Ectomycorrhizal fungal diversity: Separating the wheat from the chaff. Fungal Diversity 33:1–45.
  • Ronikier, A. 2008. Contribution to the biogeography of arctic-alpine fungi: First records in the Southern Carpathians (Romania). Sommerfeltia 31:191–211. doi:https://doi.org/10.2478/v10208-011-0011-7.
  • Ronikier, A. and M. Ronikier. 2010. Biogeographical patterns of arctic-alpine fungi: distribution analysis of Marasmius epidryas, a typical circumpolar species of cold environments. North American Fungi 5: 23–50.
  • Rostrup, E., and H. G. Simmons. 1906. Fungi collected by HG Simmons on the 2nd Norwegian Polar expedition, 1898–1902. In Report of the second Norwegian Arctic Expedition in the “Fram”, 1898–1902 2 (9), 1–10. Oslo: Videnskabs-Selskabet I Kristiania.
  • Ryberg, M., E. Larsson, and U. Molau. 2009. Ectomycorrhizal diversity on Dryas octopetala and Salix reticulata in an alpine cliff ecosystem. Arctic, Antarctic, and Alpine Research 41:506–14. doi:https://doi.org/10.1657/1938-4246-41.4.506.
  • Saccardo, P. A., C. H. Peck, and W. Trelease. 1904. The fungi of Alaska. Harriman Alaska expedition. Cryptogamic Botany 5:44–49.
  • Savile, D. B. O. 1963. Mycology in the Canadian arctic. Arctic 16 (1):17–25. doi:https://doi.org/10.14430/arctic3518.
  • Schoch, C. L., K. A. Seifert, S. Huhndorf, V. Robert, J. L. Spouge, C. A. Levesque, and W. Chen. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Science, USA 109:6241. doi:https://doi.org/10.1073/pnas.1117018109.
  • Seaver, R., and P. F. Shope. 1930. A mycological foray through the mountains of Colorado, Wyoming, and South Dakota. Mycologia 22 (1):1–8. doi:https://doi.org/10.1080/00275514.1930.12016975.
  • Semenova, T. A., L. N. Morgado, J. M. Welker, M. D. Walker, E. Smets, and J. Geml. 2016. Compositional and functional shifts in arctic fungal communities in response to experimentally increased snow depth. Soil Biology & Biochemistry 100:201–09. doi:https://doi.org/10.1016/j.soilbio.2016.06.001.
  • Senn-Irlet, B. I. 1987. Pilze aus der alpinen stufe des Val d’Anniviers (Wallis). Bulletin de la Murithienne 105:87–106.
  • Serreze, M. C., and R. G. Barry. 2011. Processes and impacts of Arctic amplification: A research synthesis. Global and Planetary Change 77 (1–2):85–96. doi:https://doi.org/10.1016/j.gloplacha.2011.03.004.
  • Shiryaev, A. G., I. V. Zmitrovich, and O. N. Ezhov. 2018. Taxonomic and ecological structure of basidial macromycetes biota in polar deserts of the Northern Hemisphere. Contemporary Problems of Ecology 11 (5):458–71. doi:https://doi.org/10.1134/S1995425518050086.
  • Skifte, O. 1989. Russula of the island Bjornoya (Bear Island), Svalbard. Opera Botanica 100:233–39.
  • Smith, A. H. 1975. A field guide to western mushrooms, 280. Ann Arbor: The University of Michigan Press.
  • Solheim, W. 1949. Studies on Rocky Mountain fungi: I. Mycologia 41 (6):623–31.
  • Spence, H. S. 1932. Sub-arctic mushrooms. Canadian Field Naturalist 46:53–54.
  • Sprague, R., and D. B. Lawrence. 1959. The fungi on deglaciated Alaskan terrain of known age. 1. Research Studies Washington State University 27 (3):110–28.
  • Sprague, R., and D. B. Lawrence. 1959–1960. The fungi on deglaciated Alaskan terrain of known age. 2. Research Studies Washington State University 27 (4):214–29.
  • Sprague, R., and D. B. Lawrence. 1960. The fungi of deglaciated Alaskan terrain of known age. 3. Research Studies Washington State University 28 (1):1–20.
  • Stephenson, S. and G. Laursen. 1993. A preliminary report on the distribution and ecology of Myxomycetes in Alaskan tundra. In Arctic and Alpine mycology 3–4, ed. O. Petrini and G. A. Laursen, 251–257, Berlin: J Cramer.
  • Timling, I., D. A. Walker, C. Nusbaum, N. J. Lennon, and D. L. Taylor. 2014. Rich and cold: Diversity, distribution and drivers of fungal communities in patterned-ground ecosystems of the North American Arctic. Molecular Ecology 23:3258–72. doi:https://doi.org/10.1111/mec.12743.
  • Trelease, W. 1904. Vol. V. 13. In: Harriman Alaska expedition, 1899, vol. V. containing cryptogamic Botany of Alaska, by William Trelease. New York: Doubleday, Page & Company.
  • Tsuji, M., and T. Hoshino. 2019. Fungi in polar regions, 146. Florida: CRC Press Taylor and Francis Group.
  • Väre, H. 2017. Finnish botanists and mycologists in the Arctic. Arctic Science 3 (3):525–52. doi:https://doi.org/10.1139/as-2016-0051.
  • Watling, R. 1987. Larger arctic-alpine fungi in Scotland. In Arctic and alpine mycology 2, ed. G. Laursen, J. F. Ammirati, and S. A. Redhead, 17–45. New York, NY: Plenum Press.
  • Watling, R., and O. K. Miller Jr. 1971. Notes on eight species of Coprinus of the Yukon Territory and adjacent Alaska. Canadian Journal of Botany 49 (9):1687–90. doi:https://doi.org/10.1139/b71-237.