Gymnopus perforans subsp. transatlanticus R.H. Petersen, 2016

Petersen, Ronald H. & Hughes, Karen W., 2016, Micromphale sect. Perforantia (Agaricales, Basidiomycetes); Expansion and phylogenetic placement, MycoKeys 18, pp. 1-122 : 50-61

5A. Gymnopus perforans subsp. transatlanticus R.H. Petersen subsp. nov.

Holotype.

Canada, Quebec, Quebec-Montmorency Co., vic. Beauport, "Camping Municipal de Beauport," 46°54.022'N, 71°10.507"W, 29.VII.2006, coll E. Lickey, TFB 13319 ( TENN-F-61587).

Etymology.

trans- = Latin, on the other side of; -atlanticus = Atlantic Ocean. Referring to distribution across the Atlantic Ocean from the typical subspecies.

Diagnosis.

Differing from typical subspecies as follows: 1) basidiomata diminutive, generally shorter and slenderer; 2) spores, pleurocystidia, basidia smaller than typical; 3) cheilocystidia infrequent, smaller and less differentiated; 4) fruiting on fallen Picea , Abies and Tsuga needles;5) separable by ITS sequence from European G. perforans .

Description.

Basidiomata (Figs 38 , 39A ) diminutive, marasmioid, often in troops, usually attached to individual conifer needles. Pileus 3-14 mm broad, strongly convex early, expanding to plano-convex, often with somewhat depressed disc, some times with small conical umbo, matt to minutely pruinose (especially near margin), occasionally sulcate-striate but usually not so; disc "sayal brown" 6C5, “tawny” 6C6, "ochraceous tawny" 6C5-6, "tawny olive" 6D5-6, "light ochraceous buff" 5A4, "army brown" 8D5, "tilleul buff" 7B2, paler and nearer to "pale ochraceous buff" 4A2, "light ochraceous buff" 5A4, occasionally yellowish near "antimony yellow" 4B6; limb and margin "pale cinnamon pink" 5A2, "pinkish buff" 6A2, "pale pinkish buff" 6A2 near "tilleul buff" 5B3, "pale olive buff" 3B2 to off-white, fading gradually through maturity, finally often off-white overall; context relatively thick on the disc, elsewhere thin and membranous. Lamellae adnate to subdecurrent, distant, arcuate (not ventricose), occasionally forked but with no anastomosis or interveining, with or without pseudocollarium, thickish, narrow (usually less than 1 mm broad), total lamellae 17-23, through lamellae 8-11, often concolorous with pileus, "pinkish buff" 5A3, " pale pinkish cinnamon" 6A2, "light buff" 3A2, "vinaceous buff" 9B2, "light ochraceous buff" 5A4, "tilleul buff" 7B2, after storage often exhibiting a slight blush of cantaloupe ("warm buff" 3A4 to "orange buff" 3A5) as necropigment; lamellar edge entire, not marginate; lamellulae in one rank, poorly developed. Stipe (10-)12-28 × 0.3-1 mm, in two breadth classes (0.3-0.7 mm vs 0.8-1 mm broad, with the latter not always part of collection) but not in length, terete when fresh, ridged and compressed when dry, subinsititious, apex concolorous with lamellae (darker within pileus), a dull reddish brown (near “russet” 7D6), downward soon "mummy brown" 6F8, "bone brown" 7F8, "soot black" 11F3, "chaetura black" 2F3 to visually black, vestured overall (minutely barbed); apical vesture hyaline (appearing white), wispy, downward gathered into minute synnemata and thus appearing barbed, dark brown; surface sometimes bearing small elliptical scars with fimbriate borders, and rarely with rudimentary, acute-tipped rhizomorphs <1 mm long; base subinsititious (with delicate thatch of spikes). Rhizomorphs (Fig. 39B ) of two types: 1) -4 × 0.2-0.7 mm, black, typically curly and branched, often with numerous individuals arising from a single needle, coarse for their length, extensively colonizing the undersides of needles; and 2) -0.5 × 0.05-0.1 mm, black, extremely fine, unbranched, often densely gregarious. Odor negligible to fetid (occasionally weakly alliaceous): taste moderately alliaceous.

Habitat and phenology.

Fruiting in troops on individual dead conifer needles, chiefly Picea , Tsuga and Abies ( Abies amabilis , Abies balsamea , Abies fraseri , Pices glauca , Picea rubens , Tsuga canadensis , Tsuga heterophylla and other conifer needles; from high-altitude spruce/fir “islands” of southern Appalachian Mountains to Canadian Shield. (for forms fruiting on dead deciduous leaves, see under G. foliiphilus ); late spring (June, southern habitats) to mid-Autumn (September).

Pileipellis involved in a slime matrix with much minute debris, composed of the following elements; 1) pileal hairs (Fig. 40 ) -80 × 4-7 µm diam, erect hyphal tips, often arising in juxtaposition to a clamp connection, embedded in slime matrix, often subcapitulate; and 2) repent hyphae (Fig. 41A, B ) 3.5-10 µm diam, firm-walled, mostly smooth, occasionally encrusted with small scabs with raised profile calluses, conspicuously clamped but with common secondary septa (Fig. 41C, D ), subhyaline individu ally. Pileus trama hyphae loosely interwoven, involved in a slime matrix, conspicuously clamped; lamellar trama loosely interwoven, involved in slime sheaths; hyphae 3-5 µm diam, firm-walled but wall swelling to 1 µm thick, conspicuously clamped. Pleurocystidia (Figs 42 , 43 ) 22-32 × 5-9 µm, fusiform, narrowly fusiform, to irregularly and asymmetrically so with rounded to acute apex, conspicuously clamped, often easily disarticulated; contents distinctly partitioned (Fig. 43 ) to not so (Fig. 42 ). Basidioles clavate; basidia (Figs 44 , 45A ) 20-29 × 5-10 µm, clavate to subcapitulate, 4-sterigmate, conspicuously clamped; contents heterogeneous; effete basidia and pleurocystidia commonly evacuated but not collapsing ( “husking”); subbasidial cells lobate by proliferating clamp connections. Basidiospores (Fig. 39C ) (6-)6.5-9 × 3-4.5 µm (Q = 1.56-2.50; Qm = 1.86; Lm = 7.13 µm). ellipsoid, marasmioid, thin-walled, smooth, inamyloid. Cheilocystidia (Fig. 45B-H ) absent or widely scattered, 25-48(-50) × 8-19(-23) µm, broadly clavate, obpyriform, occasionally irregularly lobed, without setulae, firm- to thick-walled (wall -0.7 µm thick, hyaline), sometimes easily disarticulated, subrefringent (PhC), obscurely clamped, only occasionally extending beyond hymenial structures; contents homogenous to heterogeneous (with several globose inclusions; PhC), occasionally with one or more small refractive guttules. Caulocystidia from stipe apex -50 × 6-9 µm, arising as side branches of surface hypha, thick-walled (wall -2 µm thick), refringent, hyaline, often secondarily septate. Caulocystidia from lower stipe (Fig. 46 ) -180 × 8-11 µm, arising as side branches of stipe surface hypha; basal cell usually swollen somewhat, deep brownish yellow (PhC), producing a thick-walled (wall 1-1.5 µm thick) shaft, gradually tapered distally, often constricted within and occasionally with small side lobe, doubtfully secondarily septate, brittle (although usually not straight); pigmentation equally distributed throughout shaft (not congested apically).

Commentary.

Based on direct comparison between European and northeastern North American specimens, basidiomatal dimensions seem to differ. American basidiomata are, in general, shorter with smaller pilei than European basidiomata, but basidiomata of the American collections seem distributed in two size classes, the larger and more robust of which are commensurate with Europe basidiomata.

A limited phylogenetic tree based on ITS sequences (see Fig. 87 below), sequences from northeastern North American collections clearly form a clade separate from sequences from Europe (including Scandinavia). Base-pair separation between these two clades is 1.65%. Although heterogeneous, base-pair separation among northeastern North American sequences is 0.71%. Altogether, collections from Europe and North America are not considered to represent species-rank separation, but proposal of a subspecies seems warranted. Separation of all G. perforans sequences from a clade containing G. sublaccatus and G. sequoiae is more robust (2.30% see Fig. 87 below) but both G. sequoiae and G. sublaccatus fall within North American G. perforans . For more on this situation, see discussion under G. perforans .

In eastern North America, characters which separate G. foliiphilus fruiting on dead deciduous leaves, from G. perforans subsp. transatlanticus fruiting on conifer needles: 1) G. foliiphilus exhibits stipe vesture between villose and barbed, but G. perforans subsp. transatlanticus is distinctly spiked/barbed; 2) pileal hairs in G. foliiphilus are stouter than those of G. perforans subsp. transatlanticus , and secondarily septate (this may be an artifact); and 3) pileus surface hyphae of G. foliiphilus are often encrusted in small scabs, while those of G. perforans subsp. transatlanticus are generally smooth.

In examining numerous specimens eventually accepted as G. perforans subsp. transatlanticus , it was unforeseen that a large number of specimens originally fruited on dead Tsuga needles, a host reported as rare by Antonín and Noordeloos (2010), although this is the case in Europe. Tolerance of this substrate affords the opportunity to subsist at lower elevations (and therefore at higher temperatures) in the southern Appalachian Mountains where spruce/fir forests exist only at the highest elevations (and therefore the coldest temperatures). In the future, it will be interesting to see if this condition extends across North America to the Pacific Northwest, where the spcies of spruce, fir, and hemlock are all different from eastern North American taxa.

In G. perforans subsp. transatlanticus , cheilocystidia may be confused with inflated basidia and/or pleurocystidia. Some shapes of clearly swollen elements assumed to be cheilocystidia are suggestive of sterigmata (but always two - four were not seen), and occasional objects of cheilocystidial size are shaped like fat pleurocystidia (broadly fusiform). Repeated preparations from a single pileus also showed numerous cheilocystidia.

Rhizomorphs are here described as of two types. The coarser of these are present in virtually every specimen observed, while the extremely fine type were seen in perhaps 25% of the specimens. It can be doubted that the second type actually belong to subsp. transatlanticus , but without some proof, they must be described as present.

Specimens examined.

Canada, New Brunswick, vic. Alma, Fundy Prov. Park, Maple Grove Back Road , N95°35.368', W64°59.013', 20.IX.2013, coll RHP, TFB 14377 ( TENN-F-69042); same location East Branch Trail , N45°38.587', W65°06.937', 25.IX.2013, coll Gary Samuels, TFB 14392 ( TENN-F-69056); same location, East Branch Trail , N45°38.587', W65°06.937', 25.IX.2013, coll Gary Samuels, TFB 14400 ( TENN-F-69064); same location, East Branch Trail , N45°38.587', W65°06.937', 25.IX.2013, coll RHP, TFB 14395 ( TENN-F-69056); Newfoundland & Labrador, Labrador, Benedict Mts., 31.VII.2010, coll A. Voitk (as M. androsaceus ), AV10.07.31 AV03; Newfoundland , Codroy , Gillis Cabins , N47°52'55", W59°23'36", 11.VI.2011, coll A. Voitk (as Mi. perforans ), AV 11.06.11AV01 ( TENN-F-69046); Newfoundland, Gros Morne Nat. Park , Stuckless Pond, N49°25'55", W57°43'38", 18.IX.2010, coll A. Voitk, AV 10.09.18 AV 14 ; Nova Scotia, Wolfville, Acadia University nature trail, 1.VIII.1992, coll SA Gordon, TFB 5017 ( TENN-F-51431); Cape Split area , 45°20'02" N, 64°30'02"W, 3.VIII.1992, coll. S.A. Gordon, TFB 5029 ( TENN-F-51440) ; Quebec, Quebec-Montmorency Co., vic. Beauport, " Camping Municipal de Beauport ," 46°54.022'N, 71°10.507"W, 29.VII.2006, coll E. Lickey, TFB 13319 ( TENN-F-61587; holotype) . United States, Connecticut, Hartford Co., vic. Colchester, Salmon River State Forest , N41°36'46.77", W72°25'27.43", 31.VIII.2013, coll. Sandy Scheine, TFB 14327 ( TENN-F-68179) ; New York, Cortland Co., vic. Marathon, Hoxie Gorge Preserve , Lower Gorge Trail , N42°32.871', W76°4.707', 3 .IX.2013, coll RHP, TFB 14348 ( TENN-F-68198); Ulster Co. , Frost Valley , Spring Ridge Trail , N41°50'20.7", W74°30'19.9", 9.IX.1989, coll SA Gordon, TFB 2146 ( TENN-F-49764); same location, N41°50'20.7", W74°30'19.9", 9.IX.1989, coll SA Gordon, TFB 2151 ( TENN-F-49782) ; North Carolina, Macon Co., vic. Franklin, Standing Indian Campground , 13.VI.1992, coll SA Gordon, TFB 4913 ( TENN-F-51231); Highlands , 9.VII.1966, coll L.R. Hesler (as Marasmius sp.), TENN-F-29279 ; Tennessee, Blount Co., GSMNP, Indian Gap. Appalachian Trail toward Newfound Gap , near top of ridge, 30.VI.2006, coll RHP & KWH, TFB 13121 ( TENN-F-61211); GSMNP, Cades Cove, N35°35', W83°50', 4.VIII.1962, coll & det L.R. Hesler (as Marasmius sp.), TENN-F-24923; Sevier Co. , GSMNP, Spruce-fir Nature Trail, Clingman's Dome Rd. , N35°34'40.5", W83°28'47.4", 21.VII.1989, coll SA Gordon, TFB 2114 ( TENN-F-49259) .

Figures

Figure 38. Gymnopus perforans subsp. transatlanticus. Basidiomata. Standard bars = 10 mm.

Figure 39. Gymnopus perforans subsp. transatlanticus. A Basidiomata B Rhizomorphs C Basidiospores. Standard bars: A = 10 mm; B = 2 mm; C = 5 µm.

Figure 40. Gymnopus perforans subsp. transatlanticus. Pileal hairs. Standard bars = 10 µm. TENN-F- 29277.

Figure 41. Gymnopus perforans subsp. transatlanticus. Pileipellis elements. A Slender hyphae with thin slime sheath and vague incrustation B Stouter hypha with conspicuous clamp connections C, D Pileipellis hyphae with secondary septa B-D Note multigranular gelatino-mucoid matrix. Standard bars = 10 µm. AV 11.06.11.

Figure 42. Gymnopus perforans subsp. transatlanticus. Pleurocystidia. Standard bars = 10 µm. AV 11.06.11.

Figure 43. Gymnopus perforans subsp. transatlanticus. Pleurocystidia. Note conspicuously partitioned contents. Standard bars = 10 µm. TENN-F- 29277.

Figure 44. Gymnopus perforans subsp. transatlanticus. Basidia. Standard bars = 10 µm. AV 11.06.11.

Figure 45. Gymnopus perforans subsp. transatlanticus. A Basidium B-H Cheilocystidia. Standard bars = 10 µm. TFB 14395 (TENN-F- 69056).

Figure 46. Gymnopus perforans subsp. transatlanticus. Caulocystidia. Standard bars = 10 µm. TFB 14350 (TENN-F- 69000).

Figure 87. PhyML analysis of Gymnopus perforans and G. sequoiae ITS sequences. Distance measurements percent base pair differences for the ITS region only. Bootstrap support greater than 70 % is given to the left of the supported node. Haplotypes are indicated as h 1 or h 2; clones are indicated as c 1, c 2, etc. North American locations are indicated by postal codes.