From vaccinus, meaning dun color (i.e. dull grayish brown).

Cortina not observed. Pileus 10–11 mm in diameter, convex, buff to brownish with a hoary coating, rather unicolor, smooth, shiny, tacky; margin turned down, a bit crenulate, faintly striate; edges white. Lamellae adnexed, L = 38 plus lamellulae, buff to milk coffee. Stipe 10 × 3 mm, equal, cream, finely floccose at apex and fibrillose for length, delicate. Context cream. Odor not apparent, but previously noted as raphanoid. Exsiccate: very tiny, brown, not shiny, lamellae not blackening.

Basidiospores yellowish brown, amygdaliform, limoniform, with a snout and small apiculus, distinctly verrucose (O3), with loosening perispore observed in a few spores (P1, P2), dextrinoid (D3), 10–14 × 6–8 µm, on average 12.2 × 7.1 µm, Q = 1.71; some larger spores present –18 × –9 µm. Basidia 27–35 × 7–9 µm, four-spored, possibly a few two-spored because of larger spores present. Cheilocystidia clavate-lageniform, some slightly more swollen at apex, 35–70 × 6–8 µm at apex, 3–5 µm in middle, and 6–10 µm at base, occasionally septate, no thickening observed. Pleurocystidia absent. Epicutis thickness 40–125 µm, with some encrusted hyphae.

Figure 7. 

Hebeloma vaccinum HJB11135 from Swiss alpine zone.

results are based on a single collection of two small basidiomes found in the Colorado alpine with Salix arctica.

U.S.A. COLORADO: San Juan County, San Juan Mountains, Mineral Basin, with Salix arctica, 3320 m, 31 July 2002, CLC1881 (MONT), C. Cripps.

Beker and co-workers (Beker et al. 2016; Eberhardt et al. 2016; including ML ITS analyses) showed that H. vaccinum can be recognized by its ITS region from all species apart from H. cavipes Huijsman, which differs in morphology and ecology. The RM H. vaccinum collection fits in with the diversity found within the species (Fig. 4D) it differs in 0–5 [0] bp from other included members of the species. The intraspecific variation of the included FE members of H. vaccinum is 0–8 [0] bp.

This species is usually described as larger (13–40 mm) than the Rocky Mountain specimens described here. Microscopically, the species has spores that are strongly dextrinoid (D3) with a frequently loosening perispore. The spores and cheilocystidia characteristics (swollen at the apex and at the base but constricted in the middle part) put it in H. sect. Denudata, subsect. Clepsydroida. Hebeloma vaccinum is known to occur in low elevation dunes and woodlands with Salix; it is widespread in Northern Europe. Other arctic-alpine collections are from the European Alps, the Carpathians in Slovakia, and Greenland, always with Salix species (Beker et al. 2016; Eberhardt et al. 2015b). It could be recognized in the Rocky Mountains by its association with dwarf Salix, small size, lack of a veil, and distinct spores and cystidia; compare with H. aurantioumbrinum.

From aurantius, orange and umbrinus, umber.

Cortina absent. Pileus small, 10–20 mm in diameter, convex, slightly conic-convex, appearing smooth, greasy, not hygrophanous, cream, then buff, pinkish buff, orange brown, can be lighter towards margin but not clearly two-toned, somewhat hoary; margin weakly involute, possibly crenate with a white rim. Lamellae deeply indented, deeply sinuate-arcuate, rather distant, L = 25–40 plus lamellulae, cream, then buff, pinkish buff, milk coffee; edges fimbriate, white but graying, drops visible. Stipe 15–28 × 2–3 mm, equal, bit curved, dingy whitish cream but darkening at base to watery brown (in CLC3093), floccose/pruinose for top third and smooth-fibrous below. Context dingy whitish. Odor faint or raphanoid. Exsiccate: pileus buff, lamellae brown; stipe very thin, whitish.

Basidiospores yellowish brown, slightly amygdaliform, with almost obtuse ends, with tiny apiculus, with slight ornamentation (O2), no loosening perispore (P0, P1), slightly dextrinoid (D1, D2), 10–13(–14) × 6–7.5 µm, on average 11.5 × 6.7 µm, Q = 1.72. Basidia 30–35 × 8–10 µm, clavate, two- and four-spored. Cheilocystidia long with swollen apex, clavate-stiptate, occasionally clavate-lageniform, 40–70 × 6–9 µm at apex, 3–5.5 µm in middle, and 3–6.5 µm in base. Pleurocystidia absent. Epicutis thickness 70–100 µm, with some encrusted hyphae.

Figure 8. 

Hebeloma aurantioumbrinum, CLC3093 and CLC1822.

In the alpine with willows Salix glauca, Salix planifolia, and S. arctica, reported from Colorado, Montana and Wyoming.

U.S.A. COLORADO: San Juan/Hinsdale County, San Juan Mountains, Stony Pass, with Salix arctica, 28 July 2002, CLC1822 (MONT), C. Cripps. WYOMING: Park County, Beartooth Plateau. Frozen Lakes with S. planifolia, 14 Aug 2014, CLC3093 (MONT), C. Cripps; WY/MT stateline with S. planifolia, 14 July 2001, CLC1565 (MONT), C. Cripps. Wyoming Creek 6 Aug 2008 with S. arctica and S. glauca, HJB12445, C. Cripps & H.J. Beker; HJB12446, C. Cripps; HJB12447, C. Cripps; HJB12448, H.J. Beker; HJB12450, HJB12452, HJB12453, H.J. Beker; HJB12451 with S. planifolia, H. Knudsen; HJB12454, E. Horak. Upper Wyoming Creek, with Salix arctica, 8 Aug 2008, HJB12456, J. Antibus. Hell-Roaring Plateau, with Salix sp., 14 Aug 2007, ZT12730 (ETH), ZT12731 (ETH), E. Horak.

Beker and co-workers (Beker et al. 2016; Eberhardt et al. 2015a) showed that H. aurantioumbrinum cannot be distinguished from the non-arctic-alpine H. helodes J. Favre based on ITS sequencing, but it can be separated from all other members of H. sect. Denudata. An ITS tree is given in Eberhardt et al. (2015a). The RM dataset includes more collections of H. aurantioumbrinum (15) than the FE dataset (7). Therefore, it is not surprising that the molecular diversity of the RM sequences is higher than that of the FE dataset (Fig. 4C). There are 0–6 [0] bp differences among the FE sequences of H. aurantioumbrinum, 0–9 [0–3] bp differences among the sequences of RM H. aurantioumbrinum and 2–11 [0–3] bp differences between H. aurantioumbrinum and H. helodes. Morphologically, H. aurantioumbrinum and H. helodes are quite different and can be easily separated, for example H. helodes always has a distinct thickening of the cheilocystidium wall at the apex, a feature that is absent in H. aurantioumbrinum. Further, they occur in very different habitats; H. helodes has never, to our knowledge, been confirmed in arctic-alpine habitats.

Hebeloma aurantioumbrinum may have been confused with H. pusillum J.E. Lange, although H. pusillum has much more slender basidiomes that are distinctly two-toned. Hebeloma aurantioumbrinum is squatter and rarely two-toned. Additionally, we are not aware of any confirmed records of H. pusillum in arctic-alpine habitats. Both these species, without any veil (beyond the primordial stage) and with clavate-stiptate cheilocystidia, belong to the Crustuliniformia subsection of section Denudata. This subsection contains many small species that are arctic-alpine specialists that occur with Salix, and these species have only recently been split out and described (Eberhardt et al. 2015a). Collections of H. aurantioumbrinum have been confirmed from a number of arctic and alpine habitats, including Greenland, Iceland, Scandinavia, and Svalbard (Beker et al. 2016). In the Rockies, this species can be recognized by its alpine habitat, association with willows (primarily S. planifolia), small size, lack of veil, and pinkish buff to orange brown uniformly colored pileus often with a white, crenate margin.

concolor for the similar coloration of pileus and stipe, which is not a consistent feature.

Cortina absent. Pileus 15–20 mm, convex, with or without a low broad umbo, becoming plane, smooth, moist, light to medium brown, pruinose with a grayish tint or sheen, lighter towards margin but not distinctly two-toned; margin turned down or not, entire. Lamellae adnexed, subdistant, well-separated, medium broad to broad, L = 25–32 plus lamellulae, dull brown, light brown; edges lighter. No beaded drops reported. Stipe 15–30 × 3–4 mm, equal, apex somewhat lighter tan and pruinose, below totally covered with longitudinal white fibers over a brownish ground base. Context buff. Odor astringent. Exsiccate: pileus medium brown, not two-toned, with grayish tint, dull; lamellae broad, warm cinnamon; stipe long, dull brown, narrow.

Basidiospores yellowish brown, amygdaliform, with a small apiculus, weakly ornamented (O2), loosening perispore observed in a few spores (P0, P1), distinctly dextrinoid (D2, D3), 10.5–12.5 × 6.5–7.5 µm, on average 11.6 × 7.1 µm, Q = 1.65. Basidia 25–34 × 8–10 µm, four-spored. Cheilocystidia gently clavate, some slightly swollen at apex and base, 40–60 × 6–11 µm at apex, 4.5–7 µm in middle, and 4–7 – (8) µm at base. Pleurocystidia absent. Epicutis thickness 60–75 µm, with some encrusted hyphae.

Figure 9. 

Hebeloma subconcolor, DBG-F-022785 and DBG-F-022786.

Two collections reported under willow at alpine elevations of 4000 m in Colorado; noted as cespitose to gregarious.

U.S.A. COLORADO: Clear Creek County, Summit Lake Park, under Salix, some in moss, at 4000 m, 22 Aug 2012, DBG-F-022785; DBG-F-022786, L. Gillman.

The sequences of the two collections for H. subconcolor from the Rocky Mountains are identical. The RM sequence differs by 1–4 [0] bp from the H. subconcolor collections described in Beker et al. (2016) and Grilli et al. (2016), where the ITS ML results were also shown. The closest H. velutipes sequence included in the dataset used in Fig. 5 differs in 3 [0] bp. Hebeloma velutipes is the only species of Hebeloma that cannot be distinguished from H. subconcolor by ITS sequence (Beker et al. 2016; Grilli et al. 2016; Fig. 5). However, morphologically these two species are very different and can be easily separated.

This small species has a grayish cast not found in other taxa in sections Denudata and Velutipes that we report from the Rocky Mountains; also, the lamellae are well separated and few in number. It should be compared to the other non-veiled, small species such as H. aurantioumbrinum and H. vaccinum. Hebeloma velutipes has a different coloration and is larger with many more full length lamellae. Hebeloma subconcolor is known from arctic and alpine locations in the European Alps, Greenland, Iceland and Scandinavia (Beker et al. 2016, 2018).

From hiemalis, winter or wintry, presumably to denote the production of basidiomes in colder seasons or habitats

Cortina absent. Pileus 15–35 mm in diameter, slightly conic-convex or domed-convex, smooth, greasy, pinkish buff, yellowish buff, to pale cream at the margin, with uniform coloration, somewhat hoary, with or without a white rim a few mm wide at margin; margin turned down or rolled in, then wavy. Lamellae narrowly attached, emarginate, somewhat crowded, L = 48–60 plus lamellulae, white to pale milk coffee, pale brown, wood brown; edges white floccose, with drops of liquid. Stipe 20–45 × 5–12 mm, equal, slightly clavate towards the base, whitish cream, totally pruinose (big floccules) for most of length and smoother below. Context white to watery cream, firm. Odor raphanoid, faint. Exsiccate: pileus yellowish brown, not distinctly two-toned; lamellae brown with white edges; stipe white and slimmer than for H. alpinum.

Basidiospores yellowish brown, some coloring slightly brown in Melzer’s, fat-bellied amygdaliform, limoniform, with short snout, apiculate, distinctly ornamented (O2), a few with slightly loosening perispore (P0,P1), rarely guttulate, with thickish wall, slightly dextrinoid (D1, rarely D2), 10–12 × 6–7 µm, on average, 11.1 × 6.8 µm, Q = 1.64. Basidia 25–35 × 7–9, most four-spored, maybe a few two-spored, occasionally with long sterigmata (–5 µm). Cheilocystidia long, gently clavate, clavate-lageniform, some with septa, 35–75 µm long, at apex 6–9 µm, in middle 4–6 µm, at base 4.5–9 µm, thickening sometimes observed in the middle. Pleurocystidia absent. Epicutis thickness 60–200 µm, with some encrusted hyphae.

Figure 10. 

Hebeloma hiemale, CLC3094 and CLC3574.

In the alpine zone with dwarf willows, Dryas and Betula, confirmed from Colorado, Montana, and Wyoming.

U.S.A. COLORADO: Summit County, Loveland Pass, 3750 m, with Salix in scrubland, 7 Aug 1999, ZT8072 (ETH), E. Horak; 15 Aug 1997, 3655 m, with Salix, DBG-F-019162, B. Rognerud; 21 Aug 2003, with Salix sp., DBG-F-021418, H. Miller; 20 Aug 1999, 3597 m, with Betula, DBG-F-020440, O.K. Miller; 22 Aug 1999, 3655 m, with Salix sp., DBG-F-020437, O.K. Miller; 16 Aug 1997, 3749 m, with Salix sp., DBG-F-019241, S. Trudell; 19 Aug 1999, 3620 m, DBG-F-021194, V.S. Evenson; 20 Aug 1999, 3620 m, with Salix sp., DBG-F-20431, V.S. Evenson; 20 Aug 1999, 3571 m, with Betula nana, DBG-F-020433, V.S. Evenson; 24 Aug 1999, 3620 m, with Salix sp., DBG-F-019597, N. Smith Weber; Clear Creek County, Mount Goliath, 3658 m, with Salix, 1 Sept 1999, DBG-F-020551, V.S. Evenson; 1 Sept 1999, 3810 m, DBG-F-020550, V.S. Evenson; Boulder County, West of Caribou townsite, 10 July 1988, DBG-F-016104, V.S. Evenson. Sawatch Range, Independence Pass, 13 Aug 2001, 3759 m, with Dryas octopetala and S. reticulata, ZT9828, E. Horak. San Juan County, San Juan Mountains, Mineral Basin, 3835 m, with Salix arctica, 7 Aug 2001, CLC1668 (MONT), C. Cripps. MONTANA: Carbon County, Beartooth Plateau (at the stateline with WY), 3100 m near S. reticulata, 19 July 2001, CLC1574 (MONT), C. Cripps; site 2 at the stateline MT/WY, with S. reticulata 14 Aug 2014, CLC3094 (MONT), C. Cripps; Quad Creek, 3004 m, with S. reticulata and Persicaria vivipara, 8 Aug 2008, HJB12457, M. Nauta; site 1 in Dryas, 11 Aug 2017, CLC3533 (MONT), C. Cripps; with S. planifolia and S. glauca, 17 Aug, 2017, CLC3574 (MONT), C. Cripps; with Salix planifolia, 17 Aug 2017, CLC3575 (MONT), C. Cripps. WYOMING: Park County, Highline Trail, 3200 m, with Dryas octopetala and S. reticulata, 8 Aug 2008, ZT6417 (ETH), E. Horak.

An ITS tree including H. hiemale is given by Eberhardt et al. (2016); the respective network is shown in Figure 4B. The RM dataset includes ITS sequences from 22 collections. These were matched by the same number of sequences from the FE dataset. Hebeloma hiemale ITS sequences were shown to form a well-supported monophylum in ML results presented in earlier studies (Beker et al. 2016; Eberhardt et al. 2016). Beker et al. (2010) showed that it is a species with a relatively high number of different ITS variants. The disparity between variants is mostly caused by gaps and SNPs (single-nucleotide polymorphisms). The number of differences between any pair of sequences of the presented H. hiemale data set is 0–9 [0–2] bp, within the RM sequences 0–8 [0] bp.

This species is widespread across Europe occurring from the subalpine to the alpine, in lowland dunes, shrublands, gardens, and parks; it occurs with a wide array of deciduous and coniferous trees and this includes a number of willow species, including dwarf Salix. Confirmed arctic-alpine reports include those from Canada, Greenland, Iceland, Scandinavia, and Svalbard with Salix herbacea and S. polaris as well as Dryas and Persicaria (Beker et al. 2016). Here it is confirmed with S. reticulata. Hebeloma hiemale has rarely been reported from North America in either subalpine or alpine habitats (Beker et al. 2010), but many collections previously labeled H. alpinum are now confirmed as H. hiemale.

This species looks like a small version of Hebeloma crustuliniforme but usually has more color in the pileus, particularly at the center. It has cheilocystidia that are generally swollen in the lower half, giving an hourglass appearance. The spores are verrucose, more warty than those of H. alpinum, but less so than the spores of H. vaccinum. There was some ambiguity around the delineation of H. hiemale, which was ultimately resolved with selection of an epitype (Beker et al. 2010; Eberhardt et al. 2015a).

For the color of hazelnuts, such as Corylus avellana.

Cortina absent. Pileus 20–40 mm across, hemispherical, convex, can be domed, glabrous-viscid, rich Sayal brown, ochraceous to orange brown, cinnamon brown, with frosty canescence; margin turned down, or rolled in, remaining light colored, downy. Lamellae adnate to subdecurrent, narrow, L = 90 plus lamellulae, pale avellaneous, pale cinnamon, not dark at maturity; edges floccose, beaded. Stipe 25–35 mm × 8–10 mm, equal to clavate, sturdy, white to cream, pruinose at apex, scurfy scales below. Context thick over pileus area, whitish, watery, not changing, or browning a bit in stipe but not from base up. Odor fruity or herbal tones. Exsiccate: medium-sized, cespitose in one group, hemispherical with margin inrolled, evenly colored, ochraceous, smooth to aereolate; stipe white, sturdy.

Basidiospores yellowish brown, amygdaliform, with a small apiculus, weakly ornamented (O1, O2), loosening perispore observed in a few spores (P0, P1), distinctly dextrinoid (D3), 8–11 × 5–6 µm, on average 9.5 × 5.4 µm, Q = 1.76. Basidia 25–34 × 6.5–8.5 µm, two- and four-spored. Cheilocystidia variable, many cylindrical, but also gently clavate, capitate and capitate-stipitate as well as clavate-lageniform, 30–80 × 4–13(–15) µm at apex, 3.5–6.5 µm in middle, and 4–8(–9) µm at base. Pleurocystidia absent. Epicutis thickness 80–130 µm, no encrusted hyphae recorded.

Figure 11. 

Hebeloma avellaneum, DBG-F-019533 and UMICH 10722 (holotype).

Cespitose, or clustered, in low alpine krummholz with conifers and willows. Both collections we have studied are from Colorado.

U.S.A. COLORADO: Summit County, Loveland Pass Lake, 4000 m, under willows, 20 Aug 1999, DBG-F-020434, no conifers mentioned but present in the general area, O.K. Miller Jr; Boulder County, above Mountain Research Station, 3200 m, with small willows (Salix planifolia) and one spruce within 2 m, 1 Aug 1998, DBG-F-019533, V.S. Evenson.

U.S.A. WASHINGTON: Grays Harbor County, Lake Quinault, Olympic National Park, at 75 m, on mossy edge of forest clearing, 8 Nov 1925, MICH 10722, C.H. Kauffman (holotype). CANADA. NEWFOUNDLAND AND LABRADOR: Pinware River at 15 m, under conifers, 7 Sep 2005, HJB14320, leg. J. May.

Based on ITS data, H. avellaneum is monophyletic, but unsupported by bootstrap values (Fig. 3). In terms of phylogeny, its closest relative is H. catalaunicum Beker, U. Eberh., Grilli & Vila, a Mediterranean species. It is also close to H. naviculosporum Heykoop, G. Moreno & Esteve-Rav. and H. nanum Velen. All three species appear to associate with Pinaceae (Beker et al. 2016). The identification of H. avellaneum is supported by type studies. The fourth collection used in Fig. 3 is from Canada (Newfoundland) and has been presented by Voitk et al. (2016) as “Hebeloma sp. sect. Naviculospora”.

Based on our studies of this taxon and of the habitats where it has been collected, we strongly suspect that this species is typically associated with conifers in temperate to subalpine or subarctic habitats. The holotype was collected in a temperate rainforest within the Olympic Peninsula in western Washington state. The often pruinose pileus with distinctive orange tones is indicative of H. sect. Naviculospora. These specimens were found in the low alpine where conifers are possible, and indeed Picea was noted for one collection, but only willows for the other. In the low alpine of the Rocky Mountains, the species might be confused with H. alpinum, H. velutipes, or H. hiemale because of its robust habit and lack of veil, however there are more orange color tones of the pileus; the spores are smaller and more dextrinoid than one would expect for H. alpinum and H. hiemale.

velutinus, for the velvety appearance of the stipe surface.

Cortina absent. Pileus 20–60 mm in diameter, convex, convex-domed, tacky to kidskin, smooth, not spotting, not hygrophanous, nearly unicolor, very pale buff, pale salmon buff, with hoary coating (pruinose); margin incurved but not involute, entire. Lamellae narrowly attached, sinuate or marginate, narrow to broad, slightly crowded, L = 50–75 plus lamellulae, white at first, then milk coffee color; edges white-floccose; beaded drops observed on some. Stipe (25–)30–60 × 7–15 mm, robust, equal and either narrowing or swollen at base up to 20 mm wide, slightly curved or not, pruinose or floccose in top half, longitudinally fibrous in lower half or more smooth. Context whitish, thick in pileus, firm in stipe, stuffed/hollow. Odor raphanoid. Exsiccate: largest of all species recorded; uniform pale buff pileus, lamellae, and stipe.

Basidiospore print deep Sayal brown. Basidiospores yellowish brown, amygdaliform, with a slight snout, apiculate, not guttulate, a bit rough (O1, O2), moderately dextrinoid (D2, D3), no obvious loosening perispore (P0), 10–12 × 6–7 µm, on average 10.4 × 6.6 µm, a few large spores (–18 × –7) present, Q = 1.57. Basidia 26–32 × 7.5–9 µm, clavate, four-spored. Cheilocystidia gently clavate, thin-walled, occasionally bifurcate at apex, 55–80 µm × 7–12 µm at apex, 5–8 µm in middle, 4–7 µm at base. Pleurocystida absent. Epicutis thickness 80–200 µm, with some encrusted hyphae.

Figure 12. 

Hebeloma velutipes, CLC1651 and ZT8072.

In alpine situations, mostly reported with Dryas octopetala and also with Salix in Montana and Colorado.

U.S.A. COLORADO: Gunnison County, Sawatch Range: Cumberland Pass, 3660 m, near Salix glauca but Dryas in vicinity, 4 Aug 2001, CLC1651 (MONT), C. Cripps; Cottonwood Pass, 3700, in pure Dryas octopetala, 4 Aug 2001, CLC1646 (MONT), 12 Aug 2001, CLC1725 (MONT), both C. Cripps. Summit County, Herman Gulch Trailhead, 3200 m, with Salix spp., 26 Aug 1983, DBG-F-005617, V.S. Evenson. MONTANA: Carbon County, Beartooth Plateau, site 1, 3000 m, in pure D. octopetala, 27 July 2004, CLC1980 (MONT), C. Cripps; N of East Summit, with Dryas and Salix reticulata, 30 July 1997, ZT6100 (ETH), E. Horak.

Grilli and co-workers (2016) showed that in ITS ML analyses H. velutipes falls into three unsupported clusters, i.e. one with H. incarnatulum, one with H. leucosarx, and one with H. subconcolor. The latter is discussed above; the former two species do not occur in the kind of habitats sampled in the Rocky Mountains (Beker et al. 2016; Grilli et al. 2016). Hebeloma velutipes cannot be distinguished from these three species based on ITS, but it is distinct from all other species treated in Beker et al. (2016). The reason for the intraspecific variation observed in H. velutipes has already been shown by Aanen et al. (2001), namely that H. velutipes possesses ITS alleles that differ greatly. In the Rocky Mountains, representatives of two of the clusters were found, the H. leucosarx cluster and the H. subconcolor cluster, and the collections from Montana fall into the first of these clusters while those from Colorado fall in the latter cluster. Accordingly, the number of differences are between 2–23 [0–5] bp; seven pairs with 2–6 [0–1] bp differences and seven pairs with 20–23 [2–5] bp differences. Looking at all included collections, the overall figure hardly changes (1–23 bp), although the collections randomly selected from the FE dataset include representatives of all three clusters (Fig. 5). To date we have not observed any morphological or ecological differences between members of the different clusters. The geographical differentiation of the RM representatives of H. velutipes is possibly a sampling artifact.

This species displays the characteristic features of H. sect. Velutipes, i.e. the absence of a veil, presence of a velutinate stipe, and rather strongly dextrinoid spores (reaction can take a while), as well as the gently clavate cheilocystidia. It is known to be common and widely distributed in Europe at lower elevations primarily with deciduous trees but also with coniferous hosts. There are a number of arctic and alpine records, particularly from Svalbard with Dryas octopetala and Salix polaris (Beker et al. 2016), and it has been previously reported from the North American alpine zone (Beker et al. 2010). This species produces relatively large basidiomes for the genus in the alpine; but because of its pale coloration and lack of a veil, young specimens may have been incorrectly identified as H. alpinum or H. hiemale, which are typically smaller. Phylogenetically H. velutipes is not close to these two species but, as mentioned, is related to H. subconcolor, which is smaller with fewer lamellae, grayer coloration and is also reported from the Rocky Mountain alpine zone. Interestingly, almost all Rocky Mountain specimens of H. velutipes were found with Dryas, which might help with field recognition, in addition to its robust stature, and stout white stipe.

alpinum from the alpine.

Cortina absent. Pileus 20–35 mm in diameter, convex to broadly domed, buff to pale brown, rarely brown, slightly paler at margin but not two-toned, smooth, cracking when dry; margin turned down or in. Lamellae attached, emarginate, somewhat broad, pale milk coffee, L = 40–70 plus lamellulae; edges white fimbriate, beaded. Stipe 15–30 × 4–10 mm, rather short, equal, sometimes slightly restricted in middle, clavate, white, firm. Context buff. Odor slightly raphanoid. Exsiccate: pileus brown, slightly caramel color; lamellae dark rusty brown; stipe short, cream color.

Basidiospores yellowish brown, amygdaliform with a snout, more symmetrical in side view, apiculate, sometimes guttulate, weakly ornamented (O1, O2), no loosening perispore noted (P0), very slightly dextrinoid (D0, D1), 10–12 × 6–7 µm, on average 11.2 × 6.6 µm, a few large spores present –18 × –8 µm, Q = 1.69. Basidia 32–40 × 8.5–10.5, mainly four-spored, some possibly two-spored. Cheilocystidia mostly clavate-stiptate, 55–75 µm long, apex width 6.5–10.5 µm, median width 4–5.5 µm, base width 3.5–4.5 µm. Pleurocystidia absent. Epicutis thickness 60–160 µm, with some encrusted hyphae.

Figure 13. 

Hebeloma alpinum, CLC2855 and HJB11123 (Switzerland).

Information is based on one collection from Montana, with mixed dwarf and shrub Salix species.

U.S.A. MONTANA: Park County, Lulu Pass, 3000 m in Salix arctica and S. glauca, 11 Aug 2012, CLC2855 (MONT), C. Cripps.

The only confirmed report we have for this species from the Rocky Mountains relies on a single collection of a few specimens found near Cooke City, Montana at an elevation of 3000 m with dwarf and shrub Salix species. In the network Fig. 4A, this single RM representative of H. alpinum appears rather distant from its European counterparts, which are clustered at one of the centers of the network, i.e. the biggest circle, of the H. alpinum complex. An ITS tree including the H. alpinum complex is given in Eberhardt et al. (2015a). Although this collection appears molecularly quite far removed from its conspecifics, 6–10 [1–2] bp, the total distance is largely due to a 5 bp indel repeating a sequence motif generally present in members of the H. alpinum complex. Thus, the molecular results do not argue against this being H. alpinum. This species is quite variable molecularly as well as morphologically (see the discussion of the alpinum-complex in Beker et al. 2016). The spores of this collection are on the lower end of the range for this taxon, as given in Beker et al. 2016, but still comfortably within the range.

Hebeloma alpinum has been reported previously in North America from the Rocky Mountain alpine zone (Cripps and Horak 2008) and Alaska (Miller 1998), however, most sightings were not molecularly confirmed. There are three records from the Canadian Arctic collected in 1971 and 1974 (Ohenoja and Ohenoja 2010), which have been confirmed molecularly (Beker et al. 2018). Ten collections at the Denver Botanic Garden, originally labeled H. alpinum, are now molecularly confirmed as H. hiemale (see comments for this species).

Favre originally described this species from the Swiss Alps as Hebeloma crustuliniforme var. alpinum Favre (Favre 1955) and Bruchet (1970) elevated it to species level. Hebeloma alpinum appears confined to arctic-alpine habitats and has been reported from such regions of the European Alps, Carpathians, Pyrenees, Greenland, Iceland, Scandinavia, Svalbard, and Switzerland, primarily with Salix reticulata, S. polaris, S. retusa, and Dryas octopetala as well as Persicaria (Beker et al. 2016). The species is in H. sect. Denudata, subsect. Crustuliniformia because of the lack of a veil, the clavate-stipitate shape of the cheilocystidia and molecular data (Eberhardt et al. 2015a). As a relatively robust alpine species, it should be compared to H. hiemale and H. velutipes; the latter has a robust floccose white stipe.

From marginatus, with a margin or border, emphasizing a thin line of tissue near the margin.

Cortina present, remnants distinctly present in some. Pileus 15–40(–50) mm in diameter, slightly conic-convex, domed convex, irregular, sometimes with a flat center that can even be dished, smooth or rough due to velipellus, shiny, strongly canescent, underneath dark brown, dark chestnut, to dark caramel color, mostly uniform but two-toned in some and then lighter at margin (more hoary, dingy whitish, or ochraceous in one), with a fine white border around the pileus perimeter a few mm in from margin, not hygrophanous; margin turned down or in, rather persistently so, and then covered with copious veil, often irregular, wavy, fragile. In one collection, the cuticle is rather thick and rubbery. Lamellae deeply emarginate and squared off, some pulling away, somewhat broad, L = 30–40 plus lamellulae, cream, then pinkish buff, darkening to medium coffee brown; edges fimbriate. Stipe 20–40(–45) mm × 2–6(–10) mm, equal, undulating or not, pale buff (some with possible yellow tint), and dark (up to black) at base, pruinose at apex, longitudinally fibrous lower, with a few longitudinal fibrils. Context dingy whitish, some with yellowish tones and dark at base. Odor raphanoid or sourish, sometimes faint. Exsiccate: pileus pale brown to dark brown, some obviously canescent; lamellae medium brown; stipe buff or ocher, darker at base.

Basidiospores yellowish gray, pale in Melzers, elliptical with rounded end, inequilateral in side view, no big apiculus, not guttulate, smooth to slightly punctate or rough (O1, O2), indextrinoid (D0, D1), perispore not loosening (P0), 9–12(–13) × 5.5–7(–8) µm, on average 10.1 × 6.4 µm, Q = 1.59. Basidia 25–35 × 8–9 µm, clavate, two and four-spored. Cheilocystidia lageniform, ventricose, often with very long equal neck, and somewhat gradually swollen base, occasionally clavate at apex, sometimes cylindrical, 35–80 µm long × 4–7 µm at apex, 4–6 in middle, and 7–12 (13) at base, no thickening noticed. Pleurocystidia absent. Epicutis thickness 40–100 µm, with some encrusted hyphae.

Figure 14. 

Hebeloma marginatulum DBG-F-020841 and CLC3545.

In the Rocky Mountain alpine zone, with various willows, including dwarf willows Salix arctica and S. reticulata, and shrub willow S. planifolia. Known from both Colorado and Montana.

U.S.A. COLORADO: Front Range, Loveland Pass, 12 Aug 2013, in Dryas, DBG-F-027694, C. Cripps; 12 Aug 2013, with Salix sp., DBG-F-027695, C. Cripps; 25 Aug 2000, with Salix sp., DBG-F-020708, V.S. Evenson; 21 Aug 2003, with Salix sp., DBG-F-021388, V.S. Evenson; 20 Aug 2013, DBG-F-027682, L. Gillman; 21 Aug 2003, with Salix sp., DBG-F-021405, O.K. Miller, Jr; San Juan County, Cinnamon Pass, 3700 m, with Salix arctica, 29 July 2000, CLC 1413 (MONT), C. Cripps, 3700 m, with Salix arctica, 27 July 2002, CLC1811 (MONT), C. Cripps; 29 July 2000, with S. reticulata and Salix sp., ZT9002 (ETH), E. Horak; Black Bear Basin, 2 Aug 2000, 3830 m, with S. planifolia, CLC1448 (MONT), C. Cripps; 8 Aug 2000, with S. arctica, CLC1449 (MONT), C. Cripps; 11 Aug 2001, with S. reticulata, ZT9813 (ETH), E. Horak; 3760 m, with Salix arctica, 11 Aug 2001, CLC1718 (MONT), C. Cripps; Emma Lake/Horseshoe Basin, 3688 m, with S. arctica, 31 July 2002, CLC1874 (MONT), C. Cripps; 31 July 2002, with S. arctica, CLC1880 (MONT), C. Cripps; Imogene Pass, 29 July 2002, 3850 m, with S. arctica, CLC1836 (MONT), C. Cripps; Mineral Basin, 3850 m, with S. arctica, 29 July 2002, with S. arctica, CLC1840 (MONT), C. Cripps; without obvious host, although Salix in the vicinity, 30 July 2002, CLC1860 (MONT), C. Cripps; with S. arctica and S. planifolia, 30 July 2002, CLC1861 (MONT), C. Cripps; 3835 m, with S. arctica, 7 Aug 2001, CLC1667 (MONT), C. Cripps; Stony Pass, 3840 m, with S. arctica, 28 July 2002, CLC1824 (MONT), C. Cripps; 3840 m, with S. arctica, 28 July 2002, CLC1826 (MONT), C. Cripps. Sawatch Range, Independence, 3 Aug 2000, with Salix sp., DBG-F-020841, DBG-F-020856, V.S. Evenson; 3 Aug 2000 with Salix sp., DBG-F-020843, V.S. Evenson; 3760 m, with S. planifolia, 7 Aug 2000, CLC1478 (MONT), C. Cripps. MONTANA: Carbon County, Beartooth Plateau, site 1, 9 Sept 2000, with S. planifolia, CLC1545 (MONT), C. Cripps; Quad Creek, 8 Aug 2008, with S. planifolia, HJB12458, A. and M. Ronikier; 11 Aug 2017; with Salix reticulata and S. planifolia, 11 Aug 2017, CLC3545 (MONT), C. Cripps.

Hebeloma marginatulum is distinct from other species of the H. mesophaeum complex, but not by much as to molecular distance (Fig. 6B). The species is paraphyletic in relation to the monophylum including the other taxa of the complex. With 0–19 [0–2] bp, the intraspecific variation is quite extensive in H. marginatulum in terms of total differences. Within each dataset, the ITS variation is also quite large, 0–14 [0–2] bp for the RM (29 sequences) and 0–17 [0–2] bp for the FE dataset (21 sequences). However, the total number of considered sequences is also larger than for other species.

This taxon was first described as H. versipelle var. marginatulum by Favre (1955) from the alpine region of the Swiss Alps and was later raised to species level by Bruchet (1970). It is now considered to be restricted to arctic and alpine habitats primarily with dwarf willows (Beker et al. 2016, 2018). Confirmed records show it to be present in these habitats in Canada, Greenland, Iceland, Scandinavia, Svalbard as well as the European Alps and the Carpathians and Rocky Mountains (Eberhardt et al. 2015b; Beker et al. 2016). Vesterholt (2005) described H. polare as a darker brown closely related species, but this has been synonymized with H. marginatulum (Beker et al. 2016). The Rocky Mountain specimens are also mostly uniformly dark brown with a canescent sheen.

Collections from the alpine that are very hoary and dark brown have been misinterpreted as H. bruchetii Bon (Miller and Evenson 2001) before molecular techniques; H. bruchetii, first described as an alpine species, has now been synonymized with H. mesophaeum and should have smaller spores. Hebeloma marginatulum is mentioned as a subalpine species (in Idaho) by Smith et al. (1983) who described two varieties (ver. fallax, var. proximum) from the subalpine in Colorado. Smith’s spore descriptions (dextrinoid with sharp ends) for his varieties may not fit this species, but the authors recognize that these varieties of H. marginatulum, and indeed other closely related species, need more study in North America.

This species is in H. sect. Hebeloma because of basidiomes with a cortina and the ventricose cheilocystidia together with the non-dextrinoid, or barely dextrinoid, spores that are primarily elliptical; within this group, it has an arctic-alpine habitat and relatively large spores (greater than 10 × 6 µm).

alpini- and cola, meaning dweller, to emphasise its alpine habitat, although this taxon is not found exclusively in such habitats.

Cortina present. Pileus robust, fleshy, 20–40 mm in diameter, irregular convex, somewhat domed or not, reddish brown center with grayish tones, outwards ocher and lighter towards margin (buff not white), not particularly two-toned, with hoary canescent coating that dries shiny; margin turned in at first, and then turned down. Lamellae narrowly attached, slight emarginate, or with a tooth, or pulling away, somewhat broad, milk coffee, L = 36–44; edges white floccose. Stipe 30–40 × 5–10 mm, equal, straight or not, whitish and pruinose at apex, dingy ocher and longitudinally fibrillose and striate in lower part, base sometimes encased in sand or earth. Context dingy whitish, darker below, and flesh staining brown; stipe solid or slightly hollow. Odor raphanoid. Exsiccate: pileus and stipe medium ochraceous brown; lamellae dark brown; stipe base encased in soil in the large collection (CLC1577).

Basidiospores elliptical, or some slightly amygdaliform or ovoid, with rounded end, smooth to slightly rough (O0, O1), small apiculus, not guttulate, not dextrinoid (D0), perispore not loosening (P0), 8–11 × 5–6, on average 9.1 × 5.6 µm, Q = 1.63 Basidia clavate, four-spored, 30–35 × 7–8 µm. Pleurocystidia usually absent but occasionally present, sometimes rostrate. Cheilocystidia mostly cylindrical for the top two thirds and then swollen near the base (lageniform or ventricose), 30–70 µm long × 3–8 µm at apex, 3–7 µm in middle, and 6–11 µm at base, no yellow contents noted. Epicutis thickness up to 200 µm, with no encrusted hyphae recorded.

Figure 15. 

Hebeloma alpinicola, DBG-F-020565 and CLC1577.

Collected from two different sites, one in Montana, the second in Colorado. The first site is a mixture of Dryas, Salix planifolia and S. reticulata, with some Persicaria present. The second site is a low alpine zone with dwarf willows. In both cases the growth habit was gregarious, sometimes in rings, sometimes cespitose, but not completely joined.

U.S.A. COLORADO: Gilpin County, Roosevelt National Forest, Little Echo Lake shoreline, near dwarf willows, 3500 m, 4 Sept 1999, DBG-F-020565, V.S. Evenson, M. Brown; 4 Sept 1999, DBG-F-020582, V.E. Evenson. MONTANA/WYOMING state line: Beartooth Plateau, 3020 m, with Persicaria, Geum, sedges, grasses, and quite distant S. planifolia, 19 July 2001, CLC1577 (MONT), C. Cripps; Quad Creek, 4 Aug 2008 with Dryas octopetala and S. reticulata, HJB12439, C. Cripps.

See Table 2.

Figure 6B shows H. alpinicola as paraphyletic and closely related but not mixed with species from the H. mesophaeum complex other than H. marginatulum. The H. alpinicola representatives differ by 0–13 [0–2] bp from each other. Based on morphology and ITS results, the types of seven species, namely H. alpinicola, H. chapmaniae A.H. Sm., H. littenii A.H. Sm., H. nigromaculatum A.H. Sm., H. perigoense A.H. Sm., H. smithii = H. angustifolium A.H. Sm. et al. nom. illegit. (the name Hebeloma angustifolium (Britzelm.)Sacc. already existed) and H. subargillaceum A.H. Sm. are synonyms. The inclusion of the seven types increases the absolute intraspecific variation to 0–16 [0–4] bp. The distance from other species of the complex is 3–22 [0–7] bp within the sample. Although H. alpinicola has not yet been fully tested in multilocus analyses, we consider its distinctive morphology combined with the ITS evidence to be sufficient to assign the four RM collections to this species.

This taxon, with its small ellipsoid, indextrinoid spores and ventricose cheilocystidia is a member of H. sect. Hebeloma. Morphologically it is closely related to H. excedens and H. mesophaeum. It is generally more robust than these two species, especially the stipe, and the pileus is not as two-toned. Colorado collections were described as having gray tones. While further work is needed to decide whether this really is a species distinct from the other two, the molecular evidence coupled with the morphological evidence suggest this to be the case. We have studied a number of collections, from a variety of habitats within North America that all appear to represent this taxon. Hebeloma chapmaniae, H. littenii, H. nigromaculatum, H. perigoense, and H. subargillaceum were all published by Smith et al. (1983) in the same publication that featured H. alpinicola; the replacement name H. smithii is later (Quadraccia 1987). Although there is some molecular variation between these seven collections, it is very small and we see insufficient evidence to separate these species. We have selected the name Hebeloma alpinicola on the grounds that although not all collections are strictly alpine, the majority are at least subalpine.

Originally found in sand in dunes.

Cortina present. Pileus 10–28 mm in diameter, convex, slightly conic-convex, with or without a slight umbo (one papillate), or almost applanate, some sunken in center, smooth, greasy, pale pinkish buff at first, becoming caramel color in center, outwards remaining pale, with a hoary coating, some flecks of white in outer part, mostly appearing pale unicolor; margin turned in or down, covered with white veil tissue or not. Lamellae emarginate to subdecurrent, or pulling away, variable, L = 25–48 plus lamellulae, a bit distant, cream buff to pinkish buff at first, then milk coffee; edges white fimbriate. Stipe 20–50 × 2–6 mm, equal or narrowing a bit at base, dingy whitish buff in top part, sometimes pruinose and base darkening to golden color then blackish brown (not always obvious unless cut open), with fibrils on lower part and/or a few ‘patches of tissue’. Context dingy white, watery buff, dark at base, sometimes splitting, often hollow when mature; tough in base. Odor faintly raphanoid or absent. Exsiccate: mostly pale; pileus buff or more ochraceous buff, center a bit caramel or not; lamellae pale light ocher; stipe buff, not obviously darker at base.

Basidiospores yellowish gray in Melzer’s, mostly elliptical, a few slightly amygdaliform but typically without much snout, no big apiculus, not guttulate, look smooth but may be slightly rough in Melzer’s (O1, O2), not or only very slightly dextrinoid (D0, D1), and no perispore loosening (P0), 9.5–11.5 × 5.5–7 µm, on average 10.3 × 6.2 µm, Q = 1.65. Basidia 20–30 × 8–9 µm, clavate, four-spored mostly. Pleurocystidia absent. Cheilocystidia cylindrical in the upper part and slightly swollen to more swollen at the base, 40–55 µm long × 4.5–6 µm at apex, 4–6 µm in middle, and 7–10.5 µm wide at base, with occasional thickening of the apical wall, some septate and clamped; many with dense yellow contents. Epicutis thickness 25–75 µm, with some encrusted hyphae.

Figure 16. 

Hebeloma dunense, CLC1821 and CLC1845.

In the alpine zone of the San Juan Mountains, with dwarf willows S. reticulata and S. arctica, and shrub willow S. planifolia, some in moss or near streams.

U.S.A. COLORADO: San Juan County, San Juan Mountains, Cinnamon Pass, 3700 m, with dwarf Salix near stream, 29 July 2000, CLC1411 (MONT), C. Cripps; with Salix reticulata, 8 Aug 2000, CLC1434 (MONT), C. Cripps; 29 July 2000 with Salix reticulata, ZT9001 (ETH), E. Horak; Stony Pass, 3840 m, with S. arctica, 28 July 2002, CLC1821 (MONT), C. Cripps; Mineral Basin, with S. arctica and S. planifolia, in moss, 3835 m, 30 July 2002, CLC1845 (MONT), C. Cripps.

Based on ITS data, Hebeloma dunense is phylogenetically not clearly distinguishable, but neither is it molecularly identical to other members of the H. mesophaeum complex (Fig. 6B). The intraspecific variation is 0–10 [0–2] bp (17 sequences), within the RM dataset (5 sequences), 1–7 [0–1] bp. The exclusively RM circle in Fig. 6B is a result of the data selection; this corresponds to ITS variants that do occur in the FE dataset, but did not come up in the random selection of sequences for this species.

For the Rocky Mountain collections, so far, H. dunense has been found more often with dwarf willows S. arctica, S. reticulata, and shrub willow S. planifolia in contrast to H. mesophaeum and H. excedens, which were more often with S. glauca. Originally described from low-elevation dunes with Salix, this species has been more recently recognized in arctic and alpine habitats and from Canada, Greenland, Svalbard, the European Alps, and the Carpathians (Beker et al. 2016; Beker et al. 2018; Eberhardt et al. 2015b).

Rocky Mountain specimens of H. dunense are pale, often with narrow subdecurrent lamellae; the cortina can be scant or absent, some cheilocystidia have dense yellow contents, and the spores, which are ellipsoid and distinctly but not strongly ornamented, are slightly larger than those of H. mesophaeum and H. excedens.

From Greek meso, in the middle, and phaeus, dark-colored. Persoon (1872) particularly mentioned the peculiar reddish brown pileus center “disco rufo-fusco peculiaris” which is characteristic of this taxon.

Cortina present. Pileus 10–20 mm in diameter, convex with low indistinct umbo, or conic-convex, smooth, shiny, greasy, yellowish brown in center, outwards lightening to pale ocher, at margin buff, two-toned, non-translucent; margin entire, turned in when young, covered with veil or not. Lamellae attached, adnate, L = 38–40, pale buff, pinkish buff, then pinkish brown; edges fimbriate. Stipe: 30–45 × 3–5(–8 at base), very gradually larger at base, white, pruinose at apex, and fibrillose and darker below to ocher yellow and then blackish at very base. Context pale, dark in base of stipe. Odor raphanoid. Exsiccate: pileus pale brown, stipe with yellow sheen and darker at base.

Basidiospores yellow brown, elliptical, a few slightly ovoid, no big apiculus, not guttulate, looks almost smooth even under high magnification (O1), not or only very slightly dextrinoid (D0, D1), and no perispore loosening (P0), 8–10.5(–11) × 5–6.5 µm, on average 9.7 × 5.8 µm, Q = 1.66. Basidia 20–30 × 6–9 µm, clavate, four-spored mostly. Pleurocystidia absent. Cheilocystidia cylindrical in the upper part and slightly swollen to more swollen at the base, rarely fully cylindrical, 30–55 µm long × 4–7 µm at apex, 4–7 µm in middle, and 6–9.5(–10.5) µm wide at base, with occasional thickening of the apical wall, some septate. Epicutis thickness 60–350 µm, with some encrusted hyphae.

Figure 17. 

Hebeloma mesophaeum, CLC1245 and ZT8082.

Known so far only from the Colorado alpine with Salix glauca.

U.S.A. COLORADO: Sawatch Range, Independence Pass, 3760 m, with Salix glauca, 8 Aug 1998, CLC1245 (MONT), C. Cripps; Front Range, Loveland Pass, 7 Aug 1999 with Salix sp., ZT8082 (ETH), E. Horak.

Only two collections from the RM dataset turned out to be H. mesophaeum that differ in their ITS region by 7 [2] bp (Fig. 6B). The sequence variation among all H. mesophaeum sequences (12) of the sample is 1–11 [0–4] bp. Beker et al. (2016) did not manage to delimit H. mesophaeum based on several loci. They suspected that there might be several species hidden within the sample assigned to H. mesophaeum. It appears likely that H. excedens and H. alpinicola are among these ‘cryptic’ taxa. We made sure that the 10 selected sequences from the FE dataset belong to H. mesophaeum in the strict sense. Among the H. mesophaeum representatives of the RM dataset, there is one collection that is reminiscent of H. pubescens. However, because of its ambiguous morphology we decided to keep it in H. mesophaeum. The respective collection (CLC1245) differs by 2–4 [1–2] bp from the available H. pubescens data (3 sequences).

Previously Hebeloma bruchetii Bon was one of the most commonly reported species from arctic and alpine areas, but it has now been synonymized with and folded into H. mesophaeum (Beker et al. 2016). Hebeloma mesophaeum has relatively small elliptical spores that are smooth to slightly rough and not dextrinoid. Hebeloma mesophaeum is a widespread species reported in almost all arctic and alpine habitats, as well as from subalpine, boreal, and lower elevation habitats with a wide variety of hosts (Beker et al. 2016). Also, many varieties have been described in North America (Smith et al. 1983) and in Europe (Vesterholt 2005). Some of the European taxa have been synonymized by the authors (Beker et al. 2016) and it remains to check the 12 North American varieties delineated by Smith et al. (1983).

For the pileus cuticle which can exceed the lamellae.

Cortina present. Pileus 10–25 mm in diameter, shallow convex, campanulate, then almost applanate, slight umbo or not, viscid or greasy, medium cocoa brown to orange caramel in center and pale brown on most of the pileus, with or without white tissue at margin, or with whitish rim; margin originally described as extending beyond the lamellae. Pileus thin-fleshed. Lamellae sinuate, subdecurrent, narrow, becoming broader and eroded, very pale, cream with pinkish buff tint, L = 32–48 plus lamellulae. Stipe 30–50 × 2–4 mm, equal, slightly curved, pale cream, silky, pruinose above ring zone, more dingy brown below but still pale, with a golden brown fibrils in zones, blackening towards base. Context whitish in pileus and stipe apex and yellowish brown in lower stipe down to blackish at base; stipe tough, rubbery. Odor: raphanoid or none. Exsiccate: small, pale buff overall, base of stipe dark in some.

Basidiospores yellow brown, elliptical, a few slightly ovoid, no big apiculus, not guttulate, looks almost smooth to very slightly rough even under high magnification (O1), not or only very slightly dextrinoid (D0,D1), and no perispore loosening (P0), 7–11 × 5–6.5 µm, on average 9.1 × 5.8 µm, Q = 1.55. Basidia 20–30 × 6–9 µm, clavate, four-spored mostly. Pleurocystidia absent. Cheilocystidia cylindrical in the upper part and slightly swollen to more swollen at the base, rarely fully cylindrical, 30–60 µm long × 4–7 µm at apex, 4–6.5 µm in middle, and 6–10 µm wide at base, some septate. Epicutis thickness 65–200 µm, with some encrusted hyphae.

Figure 18. 

Hebeloma excedens, CLC1685 and ZT9830.

In alpine with shrub willow Salix glauca, Colorado.

U.S.A. COLORADO: San Juan County, San Juan Mountains. U.S. Basin, 3658 m, with Salix glauca, 8 Aug 2001, CLC1685 (MONT), C. Cripps. Sawatch Range, Independence Pass, 14 Aug 1999 with Salix sp., ZT7475 (ETH), E. Horak; 12 Aug 1999 with Salix sp., ZT8136 (ETH), E. Horak; 14 Aug 2001 with Salix glauca and S. planifolia, ZT9830 (ETH), E. Horak; 3760 m, with Salix glauca, 13 Aug 2001, CLC1732 (MONT), C. Cripps. Front Range, Loveland Pass, 7 Aug 1999 with Salix sp., ZT8074 (ETH), E. Horak.

NEW YORK: Saratoga at approx. 100 m, with Pinus sp. on sandy soil in woodland, Oct 1870, NYS-F-001123, C.H. Peck (holotype).

Hebeloma excedens was not treated by Beker et al. (2016). The type of H. excedens fits in with the majority of the RM H. excedens collections, but the species cannot be clearly separated from H. mesophaeum (Fig. 6B). Looking at absolute differences, the intraspecific variation of the H. excedens sample (RM + type = 7 sequences) is 0–8 [0–1] bp, whereas the variation in the sample between H. excedens and H. mesophaeum is 2–11 [0–4] bp. In terms of absolute differences, the type of H. excedens is 5–8 [0–1] bp different from other collections referred to this species, but as Fig. 6B shows it is not strongly differentiated from other members of H. excedens, if ambiguous positions are treated as missing data as in networks or equated to their constituting bases as in the ML tree. In terms of absolute differences, the type of H. excedens is 5–11 [0–3] bp away from the H. mesophaeum sequences of the sample. Thus, within the limited support ITS data can give in this case, we do consider the species identification of the RM H. excedens collections as molecularly supported. Until the question of the distinctness and delimitation of this species can be clarified, we prefer to treat it as an independent taxon.

Hebeloma pubescens Beker & U. Eberh. is another species from the H. mesophaeum complex that might occur in the sampled habitats of the Rocky Mountains and is close to H. excedens in Fig. 6B. Based on a small sample (3 sequences available for H. pubescens; 7 sequences for H. excedens), the species vary 5–10 [1–3] bp in their ITS region.

Hebeloma excedens was first described by North American mycologist C.H. Peck; the species, with its lageniform to ventricose cheilocystidia and small elliptical, almost smooth, indextrinoid spores belongs to H. sect. Hebeloma. It is closely allied with Hebeloma mesophaeum, with which we believe it has often been confused. Separating these two taxa morphologically is rather difficult, but it does appear that the pileus of H. excedens may be more evenly colored, less yellow brown, less brown in the center, and it was originally described as having a cuticle that extended beyond the lamellae. The stipe surface appears to have fibrils arranged in zones, in contrast to that of H. mesophaeum. However, further work is required before we can have confidence that these characters are consistently different.

We have examined a number of collections from North America that are morphologically and molecularly consistent with this taxon. Based on these studies it would appear that Hebeloma excedens is widespread across North America and occurs in a wide variety of habitats.

From oreophilus, mountain loving to emphasize its presence in alpine habitats.

Cortina present. Pileus 15–30 mm in diameter, convex, hemispherical, not umbonate, smooth, dry or greasy, medium brown, bay brown, reddish brown, dark black brown, with white to cream rim of fibrillose veil remnants at margin, with hoary coating; margin even or weakly scalloped. Thick waxy pellicle mentioned in one collection. Lamellae emarginate, subdistant, L = 40–50 plus lamellulae, cream at first then milk coffee color, pinkish cinnamon; margin floccose, white. Stipe 15–60 × 3–8 mm, equal or slightly enlarged at base, a bit curved or undulating, whitich, tan, brown, in top part and darkening to blackish brown at base, pruinose in top half and fibrous below, with patches of fibrils. Context watery buff with yellow tint, and blackish brown in base, stipe hollow. Odor raphanoid. Exsiccate pale brown all over, not dark.

Basidiospores amygdaliform, with a small snout, apiculate, not guttulate, finely verrucose (O1, O2), distinctly dextrinoid (D2, D3), no perispore loosening observed (P0), 10–14 × 6–8 µm, on average 11.7 × 6.9 µm, Q = 1.68. Basidia clavate, 25–35 × 8–10 µm, mostly four-spored. Cheilocystidia lageniform, with subcapitate apex, long neck (sometimes wiggly), with gradually swollen base, sometimes septate, length 30–70 × 4–7 µm at apex, 3–6.5 µm in middle, and up to 13 µm at base, no thickening noticed. Pleurocystidia absent. Epicutis thickness 40–75 µm, with no encrusted hyphae recorded.

Figure 19. 

Hebeloma oreophilum, DBG-F-027674 and ZT12733.

In low alpine with Salix species in Montana and Colorado.

U.S.A. COLORADO: Clear Creek County, Denver Mountain Park, Summit Lake, 3911 m, in Salix arctica and S. glauca, 20 Aug 2013, DBG-F-027674, L, Gillman; Summit Lake Park, 3912 m, with Salix sp., 22 Aug 2012, DBG-F-022788, L. Gillman; Arapaho National Forest, Nature Trail, Mount Goliath, 3658 m, in Salix sp, 1 Sept 1999, DBG-F-020558, V.S. Evenson; Pitkin County, White River National Forest, junction of Montezuma Basin and Pearl Pass, in Salix sp., 3658 m, 6 Aug 1999, DBG-F-020053, V.S. Evenson. MONTANA: Carbon County, Beartooth Plateau, Frozen Lakes, with dwarf Salix, 26 July 1997, 3200 m, CLC1102 (MONT), C. Cripps; site 2, 3100 m, 8 Aug 2002, CLC1937 (MONT), with Salix planifolia, C. Cripps; Billings Fen, in moss near S. planifolia, 3048 m, 23 Aug 2017, CLC 3607 (MONT). WYOMING: Beartooth Plateau, Wyoming Creek, with Salix planifolia, 3176 m, 6 Aug 2008, HJB12449, C. Cripps; Beartooth Plateau, Hell-roaring Plateau, near Salix sp., 14 Aug 2007, ZT12733 (ETH), E. Horak.

Hebeloma oreophilum is a member of the H. nigellum complex that cannot always be distinguished from H. nigellum based on ITS data (Fig. 6A). In terms of differences, the H. oreophilum sequences from the sample (9 RM, 10 FE) differ by 0–9 [0–3] bp; 0–8 [0–1] bp within the RM sample. Most similar to H. oreophilum is H. clavulipes, which in this sample differs by 1–11 [0–3] bp. The two species do not share the same habitats. The differences between species sharing the same habitats (H. nigellum and H. spetsbergense) are 3–10 [0–5] bp. Morphologically, the easiest way to separate H. oreophilum from H. hygrophilum and H. nigellum is by the number of full length lamellae, always at least 40 for H. oreophilum and less than 36 for the others. Hebeloma clavulipes is not known from arctic-alpine habitats and has spores with an average width at most 6.6 µm while the average spore width for H. oreophilum is on average at least 6.8 µm. Hebeloma oreophilum has a persisting cortina and the lageniform/ventricose cheilocystidia of H. sect. Hebeloma.

This species was first described from the western Carpathians (Slovakia) with Salix reticulata, S. retusa, or Dryas octopetala on calcareous soil (Eberhardt et al. 2015b). It has since been reported from Canada, Greenland, Scandinavia, Svalbard, and the Rocky Mountains (Beker et al. 2016; Beker et al. 2018).

hygrophilus, because it is often found in moist, wet, boggy ground.

Cortina present. Pileus 15–25 mm in diameter, convex to almost plane, smooth, greasy, center dark brown, reddish brown, lighter towards margin to buff; margin entire. Lamellae emarginate and strongly curved outwards, a bit distant, L = 24 plus lamellulae, pale buff becoming milk coffee color; edges lighter or darker. Stipe 25–35 × 1–2 mm, long and thin, undulating, dingy cream in top half, darkening to blackish at base, apex pruinose, below with longitudinal fibrils. Context dingy cream and brownish black in stipe base. Odor raphanoid. Exsiccate: small; pileus, two-toned, dark brown center, cream towards margin; stipe thin, whitish with a darker base.

Basidiospores slightly amygdaliform, a few with a snout, apiculate, not guttulate, finely verrucose (O2), distinctly dextrinoid (D2, D3), no perispore loosening observed (P0), 10–13 × 6–7.5 µm, on average 11.4 × 6.8 µm, Q = 1.67; a few spores larger –16 × –7 µm present. Basidia clavate, 25–30 × 7–9 µm, four-spored, possibly some two-spored because of larger spores present. Cheilocystidia lageniform, with subcapitate apex, long neck (sometimes wiggly), occasionally septate, with gradually swollen base, or almost cylindrical, length 35–70 × 4–6.5 µm or wider at apex, 4–6 µm in middle, and up to 7–13 µm at base, no thickening noticed. Pleurocystidia absent. Epicutis thickness 100–130 µm, with some encrusted hyphae.

Figure 20. 

Hebeloma hygrophilum, DBG-F-021349 and CLC1462.

Based on four collections from Colorado and Montana, in the alpine zone; all with Salix, and the presence of Sphagnum is mentioned for one.

U.S.A. COLORADO: Pitkin/Lake County, Sawatch Range, Independence Pass, 6 Aug 2000, under S. planifolia, 3660 m, CLC1462 (MONT), C. Cripps; 7 Aug 2000, Salix planifolia, CLC1476 (MONT), 3660 m, C. Cripps. Summit County, near Summit Lake, with Sphagnum sp. and Salix sp., 3658 m, 10 Aug 2003, DBG-F-021349, V.S. Evenson. MONTANA: Beartooth Plateau, Frozen Lakes, at 3200 m, near S. planifolia, 29 Aug 2002, CLC1948 (MONT), C. Cripps.

Figure 6A supports Beker et al. (2016) in that H. hygrophilum is paraphyletic in relation to the other members of the H. mesophaeum complex based on the ITS sequence, although some genotypes seem to be restricted to this species. The four H. hygrophilum representatives from the Rocky Mountains differ by 2–20 [0–2] bp in their ITS, whereas the intraspecific variation of H. hygrophilum within the sample is 1–22 [0–3] bp (14 sequences). Responsible for the high distance values is sample CLC1476 (HJB15297), which differs from all other conspecifics by 15–22 [0–1] bp and from all sequences of the ingroup by 14–22 [0–2] bp, while all other H. hygrophilum samples differ by only 1–9 [0–2] bp from each other. The morphologically closest taxon occurring in the Rocky Mountains is H. nigellum which differs by 3–10 [0–5] (14–21 [0–2]) bp. The values in round brackets are for CLC1476. An unusually high number of SNP positions in CLC1476 is responsible for the large total differences. However, sequences with numerous SNP positions occur occasionally in Hebeloma and are normally reproducable (Beker et al. 2016).

Hebeloma hygrophilum was first described from the Pyrenees in non-alpine habitats above 1250 m (Poumarat and Corriol 2009) and it is known in boreal habitats from northern Europe (Beker et al. 2016). Thus it is typically in subalpine or subarctic habitats. It appears to have been found mostly with Salix and usually in wet areas with moss, typically Sphagnum. Here we report it for the first time in the alpine habitat (with S. planifolia); at least one collection was found in Sphagnum moss. It is molecularly close to H. clavulipes, H. nigellum and H. oreophilum (see below). When found in the alpine, it could be confused with H. nigellum, which is morphologically very similar. However, the spore width of H. nigellum is reported typically with an average over 7 µm, while that for H. hygrophilum is reported with an average of less than 7 µm; to add confusion, both appear to have occasional very large spores likely from two-spored basidia.

From nigellus, meaning blackish for the dark pileus.

Cortina present. Pileus 8–20 mm in diameter, broadly convex to hemispherical to almost plane with a small umbo, greasy, smooth or slightly fibrous, in center dark date brown, chocolate brown, or blackish brown, at margin paler even to cream, appearing two-toned, with hoary sheen, glazed-looking, not hygrophanous; margin inrolled at first, then even (not rimose). Lamellae emarginate, even with a tooth, normally spaced, L = 24–32 with lamellulae, whitish, then pale milk coffee, pale brown, paleness persisting; edges floccose. Stipe 15–50 × 1.5–4 mm, long and slim, equal, undulating a bit, pale dingy whitish in top half darkening to black brown at base, pruinose at apex, below silky-shiny, smooth to fibrillose. Context dingy whitish, darkening to brownish at base, rubbery in stipe. Odor raphanoid. Exsiccate: pileus small, two-toned, center dark brown, outwards cream; lamellae brown, red-brown; stipe long and very thin, cream, dark at base.

Basidiospores yellowish brown, amygdaliform, a few ellipsoid in certain view, no/slight snout, no big apiculus, slightly rough (O1, O2), perispore occasionally observed loosening very slightly (P0, P1), usually distinctly dextrinoid (D2, D3), not guttulate, 10–14.5 × 6–8 µm, on average 11.9 × 7.2 µm, Q = 1.6. Basidia 27–40 × 7.58–10.5 µm, sterigma 2–3 µm, clavate, mainly four-spored. Cheilocystidia lageniform, more or less swollen at the base, top half cylindrical, some apical thickening, some septate, 30–80 × 3.5–6.5 µm at apex, 3.5–6 µm in middle, 6.5–12.5 µm at base. Pleurocystidia absent. Epicutis thickness 40–75 µm, with no encrusted hyphae recorded.

Figure 21. 

Hebeloma nigellum, CLC3614b and CLC1420.

Alpine mostly near Salix planifolia and in moss; reported from Colorado and Montana.

U.S.A. COLORADO: San Juan County, San Juan Mountains, Engineer Pass, in Salix planifolia, 30 July 2000, CLC1420 (MONT), C. Cripps; Cinnamon Pass, in Salix spp., 10 Aug 2001, CLC1707 (MONT), C. Cripps. MONTANA: Beartooth Plateau, Frozen Lakes: at 3200 m in moss near S. planifolia, 21 Aug 2001, CLC1778 (MONT), C. Cripps; N Pass, with S. planifolia, 9 Aug 1998, ZT6425 (ETH), E. Horak; Billings Fen, in moss near S. planifolia, 23 Aug 2017, CLC3614b (MONT), C. Cripps.

According to Beker et al. (2016), H. nigellum is paraphyletic in the ITS region, but monophyletic and bootstrap supported in multi-locus analyses. The corresponding network is in Figure 6A. Hebeloma nigellum is similar in its variabiltiy within the Rocky Mountains (1–7 [0–1] bp differences based on 5 sequences when compared with the random selection of 11 sequences from the FE dataset (0–8 [0–3] bp). As discussed above, H. nigellum is close to and not always distinguishable from H. hygrophilum by ITS sequence. Another arctic and alpine species is H. spetsbergense (discussed below) that cannot be distinguished from H. nigellum by ITS sequence either.

Hebeloma nigellum is a small, slim species with a dark-centered pileus and rather large, dextrinoid, amygdaliform spores. It is widespread across northern Europe, not only in arctic-alpine habitats, and is reported from alpine and arctic habitats in Canada, Greenland, Iceland, Svalbard and the European Alps (Beker et al. 2016, 2018). In molecular and morphological features it is close to H. hygrophilum (which normally associates with Salix in non-arctic-alpine habitats). Hebeloma kuehneri Bruchet, a commonly reported arctic-alpine species, was described in the same paper as H. nigellum with the main differentiation being that the former has more brownish coloration and the latter more blackish tones (Bruchet 1970); a distinction that could not be supported by other lines of evidence. The holotype of H. kuehneri was lost, however, and a new lectotype (selected from the paratypes) has been established (Beker et al. 2016; LY BR66-15); it is sequenced and is a molecular match to H. nigellum. We here follow Beker et al. (2016) in selecting the name H. nigellum over H. kuehneri for this species.

Originally found in Svalbard.

Cortina present. Pileus 10–25 mm in diameter, shallow convex, almost applanate with indistinct umbo or not, smooth, tacky to dry, brown in center, outwards paler brown or more cinnamon, with white edge, not hygrophanous; margin turned down in young specimens, entire. Lamellae attached, adnexed, medium close, L = 26–30, pale cream to milk coffee, to brown; edges indistinct fimbriate. Stipe long and thin, 20–40 × 2–3 mm, equal, cream at apex to dark brown at base, fibrils at apex, and below silky-smooth with longitundinal fibrils. Context cream and brown to black in lower part. Odor raphanoid. Exsiccata: pileus brown, darker brown in center; lamellae reddish brown; stipe thin, cream but darkening at base.

Basidiospores yellow brown, amygdaliform, without a large snout, apiculate, not guttulate, finely verrucose (O1, O2), distinctly and sometimes strongly dextrinoid (D2, D3), no loosening perispore observed (P0), 11–14 × 7–8.5 µm, on average 12.5 × 7.6 µm, Q = 1.65. Basidia 28–35 × 8–10 µm, clavate, mostly four-spored. Cheilocystidia lageniform, with long cylindrical neck, 30–80 × 4–7 µm at apex, 4–5.5 µm in middle, and 7–10.5 µm at base. Pleurocystidia absent. Epicutis thickness 30–35 µm, with no encrusted hyphae recorded.

Figure 22. 

Hebeloma spetsbergense, DBG-F-027678 and BR5020184126599 (HJB 11982, from Svalbard). Scale bar for basidia and cheilocystidia 5 µm, for spores 10 µm. Drawing G. Walther, reproduced from Beker et al. (2016).

Figure 23. 

Micro-morphological features (basidiospores, basidia, cheilocystidia) of Hebeloma species found in the Rocky Mountain alpine zone. 1 H. vaccinum (holotype, Herb. PC) 2 H. aurantioumbrinum ZT12730 3 H. subconcolor ZT 13776 4 H. hiemale ZT9828 5 H. avellaneum DBG-F-019533 6 H. velutipes ZT6100 7 H. alpinum CLC2875 8 H. marginatulum ZT9002 9 H. alpinicola ZT13763 10 H. dunense ZT9001 11 H. mesophaeum ZT8082 12 H. excedens ZT7475 13 H. oreophilum ZT12733 14 H. hygrophilum CLC1462 15 H. nigellum ZT6425 16 H. spetsbergense micro in Fig. 22. Both two and four-spored basidiospores shown for 2, 5, 7, 8, 10, 12, 13, 15. Scale bar: 10 µm. All drawings by E. Horak.

In alpine habitats in Colorado, in moss near Salix species.

U.S.A. COLORADO: San Juan County, San Juan Mountains, Mineral Basin, 31 July 2002, CLC1879 (MONT), C. Cripps. Clear Creek County, Denver Mountain Park, Summit Lake, 3911 m, in Salix arctica and S. glauca, 20 Aug 2013, DBG-F-027678, L. Gillman.

According to Beker et al. (2018), H. spetsbergense cannot be distinguished from similar species by ITS. The two RM collections (Fig. 6A) differ by 4 [0] bp, the variation of H. spetsbergense within the sample (7 sequences) is 0–5 [0–2] bp. Hebeloma nigellum is the most similar species occurring in the same habitat and, within this sample, differs in its ITS by 1–8 [0–3] bp from H. spetsbergense. Morphologically H. spetsbergense is similar to H. hygrophilum and H. nigellum, but its spores appear to be larger. Previously this species was only known from Svalbard (Beker et al. 2016, 2018), and we report it here from North America for the first time. In Svalbard, it was found with Salix Polaris near sea level at a latitude of 78°N. In Colorado, it is reported at elevations of 3700–3800 m and latitudes from 36–38°N, and there is a distance between localities of 6500 km, greatly extending its disjunct range. It remains to be seen, if it also occurs in other arctic and alpine habitats.

With the persistent presence of a cortina and the lageniform or ventricose cheilocystidia, this taxon clearly belongs in H. sect. Hebeloma. The rather strongly dextrinoid amygdaloid spores, less than 14 µm long but more than 7.5 µm wide, distinguish this taxon from the other alpine-arctic species of this section.