The specimens studied are summarized in three tables. Tab. 1 gives details of collections whose sequences make up the phylogenetic tree in Fig. 1, excluding an unidentified species in the Omphalina pyxidata complex and the sphagnicolous arrhenias. Data for collections of the unidentified species in the Omphalina pyxidata complex examined for this study, whether shown in Fig. 1 or not, are summarized in Tab. 2, and data for the sphgagnicolous arrhenias examined for this study, including those used to make up the phylogenetic trees in Figs. 1 and 2, are shown in Tab. 3.
Taxonomy
Arrhenia bigelowii Voitk, Lickey & I. Saar, sp. nov. Fig. 3a; 4a–d; 7a, e, f.
MycoBank MB827069
Typification: CANADA, NL, Rocky Harbour bog, 49.577694°N, 57.898916°W, 35 m asl, bog in Sphagnum, 5 Jul 2005, leg. Andrus Voitk 04.07.05.av03. (DAOM744391, holotype)
= Clitocybe gerardiana var. fusca H.E. Bigelow, Mycologia 50(1):401. 1958. USA, MI, Luce Co., Pike Lake, bog in Sphagnum, 11 Sep 1953, leg. Alexander H. Smith, 42574 (MICH 10143, varietal
holotype). Ibid; a solitary partial pileus donated from the holotype collection MICH 10143 to TUF, and accessioned as an isotype (TUF117871! varietal isotype, GenBank MH473348).
Etymology: Bigelowii honours the American mycologist Howard Elson Bigelow, the first to publish this entity as a separate taxon.
Diagnosis. Scaly-capped obligate sphagnopilic denizen of temperate to subarctic raised bogs, pileus usually under 20 mm diameter, occasionally darkens. Pinnate scales distinguish it from smooth-capped sphagnophilic arrhenias; in addition to being somewhat darker most of the time, it can be separated from the other scaly-capped sphagnicolous species, Arr. gerardiana, by an occasional darkening reaction, tendency for more inverted bowl shaped pilei, longer spores, and diagnostic ITS sequence.
Capsule varietal isotype description. Studied material was approximately one-half of a dried pileus with gills attached, approx. 1.5 cm in diam. Cap striate, umbilicate. Microscopic examination of a squash section of gill revealed elongate elliptical spores 6.1–11.4 × 3.2–4.9 µm (ave. 8.4 × 4.0, Q 1.7–2.5, ave 2.1, n=22 spores). No cystidia, but clamp connections readily evident. Four-spored club-shaped basidia, approx. size 34 ×7 µm. Cap structure not examined.
Macromorphology (Fig. 3a; 4a–d): Basidioma: Brown, stipitate, about 8–33 mm tall, in Sphagnum. Uncommonly becomes dusky, with various degrees of black and grey adding to or covering the brown colouration. Stimulus for this change not known. Pileus: 4–24 mm diameter, usually deeply umbilicate and often shaped like an inverted bowl, edges becoming more plane, then crenulate with age, translucently striate, smooth, but covered with somewhat concentric radially arranged scales with darker brown, burr-like, uplifted, centripetally narrowing ends. Narrow brown radial bands over lamellae and lamellulae, alternating with wider, tan intervening bands; the latter become sulcate with time, giving the cap a radially ribbed appearance. Rim of edge darkens with time. Lamellae: moderately spaced, smooth edged, deeply decurrent, with usually three intervening, small lamellulae; developing a few low crossveins beyond maturity, forking very rare; light brown, developing darker edge. Stipe: 2–5 × 10–23 mm, cylindric, straight; becoming somewhat hollow; minutely tomentose, glabrescent with age, brown, sparse white tomentum at base. Context: whitish, odor unremarkable.
Micromorphology: Basidiospores (369 spores, 18 basidiomata, 18 collections, 3 observers) 6.1–17.0 × 3.0–6.1 µm, ave. 10.3 × 4.6 µm, elongate elliptical, Q = 1.6–3.3, ave. 2.3, content homogeneous, some variation in size and shape between individual basidiomata (Fig. 6). Basidia 29–39 × 6.2–8.8 µm, ave. 35 × 7.4 µm; mostly four-spored with occasional two-spored; clavate, hyaline. No pleuro-, cheilo- or caulocystidia, but terminal hyphal cells protrude from stipe as small hairs. Pileipellis a cutis with thin-walled, clamped hyphae, 3.5–13.5 µm wide, hyaline to brownish, with moderately incrusted brown pigment, superficial layers forming small plates on the cell surface (Fig. 7a). Scale tips end with gently swollen rounded unpigmented clear cells (Fig. 7e, f). Clamp connections in all tissues.
Habitat: Open raised Sphagnum bogs in groups of 1–6 separate basiomata, attached to living Sphagnum with white mycelial tomentum, associated with various bog plants such as Vaccinium oxycoccos L., V. macrocarpon Aiton, Rubus chamaemorus L., Empetrum nigrum L., Andromeda polifolia L., and various bog orchids, reeds and grasses, June–Sept, most plentiful in July. May be found in the same bog at the same time as Arr. gerardiana.
Distribution: Known from North America and Europe; in NL found throughout the province, more common on the Island.
Additional specimens examined: See Table 3.
Comments: Often indistinguishable from Arr. gerardiana: darkening reaction often absent and pileus becomes more plane with age. Although statistical analysis shows that the spore size difference is highly significant (for Q, t = –6.31; d.f. = 788; p < 0.001), spore sizes of the two species overlap sufficiently to make this character useful only when the averages occupy the extremes of their respective range. We elected to describe it as a new species because we wished to provide a fully examined and robust type collection for posterity. Bigelow (1958) described the growth pattern as “scattered”, typical of scaly-capped sphagnicolous arrhenias, whose individual organisms usually produce 1–2 fruiting bodies at any one time, and seldom more than six. Smith’s holotype collection of C. gerardiana var. fusca consists of more than 30 basidiomata, and must sample several individual organisms. Because both Arr. bigelowii and Arr. gerardiana are macro- and micromorphologically very similar, known to occur in the same bog at the same time, a multi-individual collection increases the likelihood of containing both species. We have not examined the entire collection, but only a cap fragment, from which tissue has been removed for both microscopy and molecular studies. This seems inadequate to designate as lectotype, when an abundance of tissue remains in the holotype for the variety, and typifying the species with an ample and fully examined collection seems the more prudent choice. In addition, given the considerable confusion caused by the name “fusconigra” in the past, avoiding a name from the same root seems advantageous, all the moreappropriate because this gives an opportunity to honour Bigelow, the first to recognize this species a new taxon.
Arrhenia gerardiana (Peck) Elborne, Funga Nordica: 913. 2008. FIG. 3b–d; 4 e,f ; 7g, h
Basionym: Agaricus (Clitocybe) gerardianus Peck, Bull. Buffalo Soc. Nat. Sci. 1: 46. 1873.
MycoBank MB542211
Typification: USA: NEW YORK, Ulster Co, New Paltz, June, 1873 (approx.), in “sphagnous marshes”, leg. C.H. Peck. (NYSf 1339.1–4! Lectotype, here designated; MBT10005613). USA: NEW YORK, Rensselaer Co., Sand Lake, June, 1873 (approx.), in “sphagnous marshes”, leg. C.H. Peck. (paratype, NYSf 1340, not seen, possibly lost). USA: NEW YORK, Essex County, North Elba, Mt. Marcy, June, no year, leg. & det. C.H. Peck (as Omphalia gerardiana) M212-S29-4000(7794) (NYSd 4725.1!, epitype, here designated. Mycobank type number MBT10005614).
Capsule lectotype description. The lectotype collection NYSf 1339.1–4, consists of four dried dark brown basidiomata glued to sheets (.1 and .4 further secured with cloth tape), reasonably intact with pieces of stipe and pileus missing. Tallest approx. 5.5 cm high (stipe base to top of upturned cap edge), with widest cap diam. approx. 1.2 cm. Caps striate, umbilicate to funnel-shaped. Microscopic examination of a squash section of gill (3% KOH) from each of the four basidiomata revealed pip-shaped to elliptical spores 6.8–12.4 × 3.4–5.1 µm (ave. 9.2 × 4.2, ave Q = 2.2, n=100 spores). No cystidia. Clamp connections throughout all tissues. Four-spored (rarely two) club-shaped basidia, approx. size 24 × 7 µm. Cap structure not examined.
Capsule epitype description. The epitype collection NYSd 4725, consisted of ten relatively intact dried dark brown basidiomata, most taped or glued to sheets, with parts missing, and additional pieces with most of the basidiomata missing. Tallest approx. 5.5 cm high (stipe base to top of upturned cap edge), with widest cap diam. approx. 1.2 cm. Caps striate, umbilicate to funnel-shaped. The epitype was selected and designated NYSd 4725.1. Microscopic examination of a squash section of gill revealed pip-shaped to elliptical spores 7.9–11.5 × 3.3–4.2 µm (ave. 9.8 × 3.8, ave Q = 2.6, n=20 spores). No cystidia. Clamp connections throughout all tissues. Four-spored club-shaped basidia, approx. size 24 × 7 µm. Cap structure not examined.
Macromorphology (Fig. 3b–d; Fig. 4e, f): Basidioma: Brown, stipitate, about 10–35 mm tall, in Sphagnum. Pileus: 5–25 mm diameter, usually deeply umbilicate, edges curved down somewhat at the edges, but rarely assuming an inverted bowl shape, becoming plane, then crenulate with age, translucently striate, smooth, but covered with somewhat concentric radially arranged scales with darker brown, burr-like, uplifted, narrow distal ends. These scales seem to recede with age, and occasional very mature specimens with large caps may have no distinctive scales (Fig. 3d; 4f). Narrow brown radial bands over lamellae and lamellulae, alternating with wider, tan intervening bands; the latter become minimally sulcate with time. Rim of edge darkens with time. Lamellae: moderately spaced, smooth edged, deeply decurrent, usually with three intervening, small lamellulae; developing a few low crossveins beyond maturity, forking very rare; light brown, developing darker edge. Stipe: 2–5 × 10–25 mm, cylindric, straight; becoming somewhat hollow; minutely tomentose, which may disappear with age, brown with sparse white tomentum at base. Context: whitish, odor unremarkable.
Micromorphology: Basidiospores (443 spores, 20 basiomata, 17 collections, 3 observers) 6.2–12.9 × 2.8–5.6 µm, ave. 8.9 × 4.2 µm, pip-shaped to elliptical, Q = 1.3 – 3.2, ave. 2.2, content homogeneous, some variation in size and shape between individual basiomata (Fig. 6). Basidia 28 (21–35) × 6.8 (5.6–9.0) µm; mostly four-spored with occasional two-spored; clavate, hyaline. No pleuro-, cheilo- or caulocystidia, but terminal hyphal cells protrude from stipe as small hairs. Pileipellis a cutis with thin-walled, clamped hyphae, 2.5–9.5 µm wide, hyaline to brownish, with moderately incrusted brown pigment, superficial layers forming small plates on the cell surface (Fig. 7b). Scale tips end with gently swollen rounded unpigmented clear cells (Fig. 7g, h). Clamp connections in all tissues.
Habitat: Open raised Sphagnum bogs in groups of 1–6 separate basidiomata, attached to living Sphagnum with white mycelial tomentum, associated with various bog plants such as Vaccinium oxycoccos, V. macrocarpon, Rubus chamaemorus, Empetrum nigrum, Andromeda polifolia, and various bog orchids, reeds and grasses, June–September, most plentiful in July. May be found in the same bog at the same time as Arr. bigelowii.
Distribution: Europe and North America; suspect Holarctic distribution. In NL, throughout the province.
Additional specimens examined: See Table 3.
Comments: Its cap, scaly throughout, sets it apart from smooth-capped sphagnicolous omphalinoids. This character may be lost in very few overly mature and large specimens, requiring microscopic examination to distinguish them from Arr. philonotis, OPCUS, or even lighter-coloured Arr. telmatiaea. Differs from Arr. bigelowii by its more plane pilei, by not turning grey to black in response to unknown stimuli, and shorter spores; these characters are not always evident.
Peck (1873) mentioned two collections in his description of Agaricus gerardianus (NYSf 1339 and NYSf 1340), which become syntypes because he did not designate either as holotype. NYSf 1340 is presumed lost; we designated the remaining collection (NYSf 1339.1–4) with its four basiomata, as lectotype for the species. Comparison of spore size has allowed us to conclude that the lectotype is conspecific with collection NYSd 4725, identified by Peck as Ag. gerardianus. Because the lectotype did not yield DNA, but NYSd 4725 did, we designated the latter as epitype for Arrhenia gerardiana, thus defining the clade in which it resides as that species.
Arrhenia philonotis (Lasch) Redhead, Luzoni, Moncalvo & Vilgalys, Mycotaxon 83: 48. 2002. Fig. 3e; 5a,b; 7c
MycoBank MB374174
Basionym: Agaricus philonotis Lasch, Linnaea 3:394. 1828.
Typification: Holotype probably lost. GERMANY, Baden-Württemberg, Schwarzwald, Ks. Breisgau-Hochschwarzwald, Hinterzarten, Hinterzartener Moor, MTB/Q 8014/4, Sphagnum, 29 Jul 1984, leg. D. Laber, (Neotype, here designated: KR-0003880! Mycobank type number MBT10005615).
Capsule neotype description. The neotype collection KR-0003880, is fragmented with no completely intact basiomata. Larger pieces are parts of at least 4–5 pilei and twice that number of stems, suggesting that the original collection may have consisted of around 8–10 basiomata. Although fragmented, there is a generous amount of material, which otherwise seems to be in good shape. Small strands of moss are seen, including at least one stem attached to what seems to be Sphagnum. By extrapolation, the tallest dried basioma is approx. 5 cm high (stipe base to top of upper cap edge), with widest cap diam. approx. 2.5 cm. Caps smooth, umbilicate. Microscopic examination of a squash section of gill revealed pip-shaped to elliptical spores 7.7–10.4 × 5.2–7.6 µm (ave. 8.9 × 5.8, ave Q = 1.5, n=20 spores). No cystidia. Clamp connections throughout all tissues. Four-spored club-shaped basidia, approx. size 24 × 7 µm. Cap structure not examined.
Macromorphology (Fig. 3e; 5a,b): Basidioma: Brown, stipitate, about 10–38 mm tall, in heaths, bogs and moors with Sphagnum or other moss. Pileus: 5–30 mm diameter, umbilicate, edges curved down becoming plane and crenulate with age, translucently striate, smooth, often covered with thin, fibrillose, adpressed, flat scales, whose tips may become slightly uplifted as scattered thin hairs, denser in the umbilicus. Narrow brown radial bands over lamellae and lamellulae, alternating with wider, tan intervening bands; the latter may become sulcate with time, giving the cap a radially ribbed appearance. Rim of edge darkens with time. Lamellae: moderately spaced, smooth edged, deeply decurrent, with 3–5 intervening, small lamellulae; may develop a few low crossveins beyond maturity, forking very rare; light brown, developing darker edge. Stipe: 2–5 × 10–25 mm, cylindric, straight; becoming somewhat hollow; minutely tomentose, glabrescent, brown with sparse white tomentum at base. Context: whitish, odor unremarkable.
Micromorphology: Basidiospores (102 spores, 5 basidiomata, 5 collections, 2 observers) 6.6–10.9 × 4.2–7.7 µm, ave. 8.7 × 5.6 µm, pip-shaped to elliptical with Q = 1.2 – 2.1, ave. 1.6, content homogeneous, some variation in size and shape between individual basiomata (Fig. 6). Basidia 29.6 (23.3–35.2) × 7.8 (6.1–10.2) µm; mostly four-spored with occasional two-spored; clavate, hyaline. No pleuro-, cheilo- or caulocystidia, but terminal hyphal cells protrude from stipe as small hairs. Pileipellis a cutis with thin-walled, clamped hyphae, 2.0–11.0 µm wide, hyaline to brownish, with moderately incrusted brown pigment, superficial layers forming small plates on the cell surface (Fig. 7c). Clamp connections in all tissues.
Habitat: Barren moors, heaths, fens, raised Sphagnum bogs in groups of 1–6 separate basidiomata, either with Sphagnum or other moss. Associated with various heath plants such as Vaccinium oxycoccos, V. macrocarpon, Rubus chamaemorus, Empetrum nigrum, Andromeda polifolia, reeds and grasses, June–September, most plentiful in August.
Distribution: Known from North America and Europe; Holarctic distribution suspected; not as southerly as the scaly-capped species, in NL so far known only from Labrador.
Additional specimens examined: See Table 3.
Comments: Basiomata resemble those of the scaly-capped species, but are readily distinguished by their obviously smooth caps of somewhat greater diameter, and light colour tending more to greyish brown. Distinguished from Arr. telmatiaea by its lighter hue and from OPC by its greyish rather than reddish brown hues and broader spores.
Arrhenia telmatiaea (Berk. & Broome) Voitk & I. Saar, comb. nov. Fig. 3f,g; 5c,d,e; 7d
MycoBank MB842881
Basionym: Agaricus telmatiaeus Berk. & Cooke. Illustrations of British fungi (Hymenomycetes). Williams and Norgate, London. 2: pl 240. UK, England, Yorkshire Co., Scarboro, 2 Nov 1882, leg. G. Massee (NY12555, holotype!)
= Arrhenia fusconigra (P.D. Orton) P.A. Moreau & Courtec., Documents Mycologiques 34 (135–136): 48 (2008). Basionym: Omphalina fusconigra P.D. Orton, Transactions of the British Mycological Society 43(2): 335. 1960. MycoBank MB518174. UK, Scotland, South Perthshire, Blair Drummond, 28 Sep 1957, leg. J. Grainger (K(M)98588! holotype!).
Capsule holotype description. The holotype collection NY12555, consisted of eight relatively intact dried dark brown basidiomata with adherent Sphagnum, most taped or glued to sheets, with parts missing. Tallest approx. 4.8 cm high (stipe base to top of cap), with widest cap diam. approx. 3.8 cm. Caps striate, umbilicate. Microscopic examination of a squash section of gill revealed pip-shaped to elliptical spores 6.0–8.1 × 3.9–5.8 µm (ave. 7.2 × 4.7, Q=1.3–1.8, ave 1.5, n=30 spores). No cystidia. Clamp connections throughout all tissues. Four-spored club-shaped basidia, approx. size 26 × 7 µm. Cap structure not examined.
Macromorphology (Fig. 3f,g; 5c,d,e) Basidioma dark brown, usually almost blackish, stipitate, about 10–40 mm tall, in Sphagnum. Pileus: 6–32 mm diameter, usually deeply umbilicate, edges curved down in a pronounced arc, becoming plane and then funnel-shaped with age, translucently striate, smooth, with occasional fine, floccules in the umbilicus. Usually dark brown verging on black, but occasionally may remain mostly brown; dark, narrow, radial bands over lamellae and lamellulae, alternating with somewhat lighter deep brown bands; hygrophanous. Rim of edge darkens with time. Lamellae: closely spaced, smooth edged, deeply decurrent, with usually 5–7 intervening lamellulae; forking very rare; medium to dark brown, edge darker. Stipe: 2–6 × 10–28 mm, cylindric, straight; becoming somewhat hollow; minutely tomentose, glabrescent, concolorous with pileus with sparse white tomentum at base. Context: lighter brown, odor unremarkable.
Micromorphology: Basidiospores (241 spores, 12 basiomata, 12 collections) 5.3–11.3 × 3.3–6.6 µm, ave. 7.3 × 4.7 µm, pip-shaped to elliptical, Q = 1.2–2.2, ave. 1.6, content homogeneous, some variation in size and shape between individual basiomata (Fig. 6). Basidia 27.6 (21.8–31.6) × 7.1 (5.5–8.6) µm; mostly four-spored with occasional two-spored; clavate, hyaline. No pleuro-, cheilo- or caulocystidia, but terminal hyphal cells protrude from stipe as small hairs. Pielipellis a cutis with thin-walled, clamped hyphae, 3.5–9.0 µm wide, hyaline to brownish, with sparsely to moderately incrusted brown pigment, superficial layers at times forming small plates on the cell surface (Fig. 7d). Clamp connections in all tissues.
Habitat: Open raised Sphagnum bogs in groups of 1–6 separate basiomata, attached to living Sphagnum with white mycelial tomentum, associated with various bog plants such as Vaccinium oxycoccos, V. macrocarpon, Rubus chamaemorus, Empetrum nigrum, Andromeda polifolia, reeds and grasses, July–September, most plentiful in August. May be found in the same bog at the same time as other northern species.
Distribution: Known from North America and Europe; suspected Holarctic distribution; in NL not as southern as the scaly-capped species, so far known only from Labrador, the Great Northern Peninsula, and the northern east coast.
Specimens examined: See Table 3.
Comments: Its obviously and relatively even dark colour distinguishes it from the other smooth-capped sphagnicolous species, Arr. philonotis, but on occasion may be more dark brown than near-black, requiring microscopic examination to confirm identification. Omphaliaster borealis (M. Lange & Skifte) Lamoure—not recorded in NL to date—is macroscopically very similar, also occurring in northern or alpine raised Sphagnum bogs, but can be distinguished by its globose, spinulose spores (Vašutová et al. 2013).
OPCUS (Omphalina pyxidata complex, unidentified species) Fig. 5f,g
Macromorphology: Basidioma: Brown, stipitate, about 10–44 mm tall, with various mosses in grassland, moor, fen, as well as bog with Sphagnum. Pileus: 8–40 mm diameter, umbilicate, downcurved edges quickly becoming plane, then upturned and crenulate with age, translucently striate but hygrophanous and opaque when dry, smooth, covered with sparse, thin, fibrillose, adpressed, flat scales. Narrow brown or reddish brown radial bands over lamellae and lamellulae, alternating with wider, tan intervening bands. Red more noticeable if opaque. Lamellae: moderately spaced, smooth-edged, deeply decurrent, with 3–5 intervening, small lamellulae; develops low crossveins beyond maturity, forking very rare; very light off-white, contrasting markedly with darker stem and cap. Stipe: 2–7 × 10–38 mm, cylindric, straight concolorous with cap, sparse white tomentum at base. Context: whitish, odor unremarkable.
Micromorphology: Basidiospores (128 spores, 5 sporocarps, 5 collections) 6.3–9.1 × 3.6–5.1 µm, ave 7.8 × 4.4 µm, elliptical, Q = 1.3–2.1, ave. 1.8. Basidia four-spored, clavate, hyaline (Fig. 6). No pleuro-, cheilo- or caulocystidia. Clamp connections in all tissues.
Habitat: Grows with mosses in grassland, fens, moors and bogs; usually 1–4 basidiomata in bogs, but troops of 20 or more in grassland. Season: June–Sept, most plentiful Jul–Aug. Found in the same bog at the same time as the other species.
Distribution: Throughout NL; North America and Europe.
Specimens examined: See Table 1.
Comments: Larger than the arrhenias, often reddish, not greyish, but otherwise similar to Arr. philonotis, but with narrower spores.
Dichotomous key to the species of sphagnicolous omphalinoids of NL
1a. Granular green lichen thalli at base of stem and lack of clamp connections Lichenomphalia
1b. No thalli at base of stem, and clamp connections ……………………………………….. 2
2a. Cap scaly with raised, pointed, often darkened scale tips ……………….. 3
2b. Cap smooth (may be minutely wrinkled, irregular or wooly, or may have adpressed scales, but not with raised scale tips) …………… 4
3.a May undergo significant darkening reaction, spores 6.1–17.0 × 3.0–6.1 µm, ave. 10.3 × 4.6 µm …………………..……………….………. Arrhenia bigelowii
3b. No darkening reaction, spores 6.2–12.9 × 2.8–5.6 µm, ave. 8.9 × 4.2 µm ……….. Arrhenia gerardiana.
4a. Medium (±reddish) brown, mature cap around 30 mm diameter, spores <5 µm wide, distribution throughout NL ……………………………………………….…. OPCUS
4b. Not as above ……………………………………………………………………….. 5
5a. Dark brown, nearly black, northerly distribution, obligate sphagnophile, spores 5.3–11.3 × 3.3–6.6, ave. 7.3 × 4.7 ……………… Arrhenia telmatiaea
5b. Medium to light grey-brown, northerly distribution, facultative sphagnophile, spores 6.6–10.9 × 4.2–7.7, ave. 8.7 × 5.6 ………….. Arrhenia philonotis