Collybiopsis complicata R. H. Petersen, 2024

Petersen, Ronald H. & Hughes, Karen W., 2024, Two new species of Collybiopsis (Agaricales, Omphalotaceae) from Eastern North America, MycoKeys 107, pp. 95-124 : 95-124

Collybiopsis complicata R. H. Petersen sp. nov.

Figs 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11

Holotype.

Tennessee, Blount Co., Great Smoky Mountains National Park, Metcalf’s Bottoms Picnic Area , 9. VI. 1997, coll. Ronald H. Petersen, TFB 9168 ( TENN-F- 055766 ).

Diagnosis.

1) Basidiomata marasmielloid / gymnopoid, gracile, small, with slender stipe; 2) pileus pigmented, especially over disc; 3) pileipellis composed of stalked-coralloid structures and lobed repent hyphae; 4) stipe fully vestured; 5) clamp connections present; 6) cheilocystidia prominent, similar to pileipellis elements; 7) basidiospores 5–8 × 3–4 µm.

Etymology.

Cheilocystidia with complex, branched structure; also complex distribution, from southern Appalachians to New England.

Description.

Basidiomata (Fig. 3 ) scattered-gregarious> 50 basidiomata in <1 2 m, marasmielloid or miniature collybioid. Pileus 6–14 mm broad, shallowly convex to plane by maturity, matt, delicately rivulose-striate; disc “ snuff brown ” (5 E 8), outward “ sayal brown ” (6 C 5) to fleshy tan. Lamellae free to adnexed but seceding in drying to become removed from stipe apex, total lamellae 47–64; through lamellae 24–26, in two major ranks with no anastomosis, 1.5–2 mm broad, subventricose to ventricose by maturity, knife-edged, dull pale tan-gray (near “ tilleul buff ” 7 B 2), bleaching to off-white, often (but not exclusively) becoming pale cream-colored with necropigment; lamellulae in one rank, less than ½ the length through lamellae. Stipe 7–30 (– 45) × 0.7–1.2 mm, terete and remaining so upon drying, minutely vestured overall, somewhat darker than lamellae apically, downward fleshy tan to fleshy brown, drying matt; vesture on upper stipe of scattered delicate squamules composed of individual caulocystidia, on lower stipe a solid turf (but never felty), straw-colored to “ light ochraceous buff ” (5 A 4); insertion insititious on fine twigs and leaves; superficial litter-binding mycelium not observed. Odor and taste negligible.

Pileipellis a thatch of occasional repent encrusted hyphae (Fig. 4 ) and dominant interlocking, stalked-lobose pileocystidia and lobed-diverticulate, repent hyphae (Fig. 5 B, C ); Pileocystidia (Figs 5 A, D ) 27–37 × 5–14 µm, stalked, branching in lobose-coralloid configurations, apparently hyaline, thin- to firm-walled, arising from clamp connections. Subsurface pileipellis hyphae 2.5–10 µm diam, firm-walled, conspicuously clamped, ornamented with small flakes (in profile) but no profile calluses or stripes. Pleurocystidia (Fig. 6 ) common, arising from clamp connections, 32–40 × 7–9 μm, stalked-fusiform with apex often broadly submammillate; contents homogeneous. Basidioles clavate. Basidia (Fig. 7 ) 35–60 × 7–9 µm, clavate to weakly urniform or with somewhat expanded subcapitate apex, (2 –) 4 – sterigmate, arising from clamp connections; sterigmata robust, slightly curved; contents heterogeneous, with scattered, refringent granules. Basidiospores (Fig. 8 B ) (5.5 –) 6.5–8.5 (– 10) × 3–4 (– 5) µm ( Q = 1.56–2.50; Q m = 2.03; L m = 8.02 µm), ellipsoid, flattened adaxially, thin-walled, inamyloid; contents (dried) homogeneous. Lamellar edge sterile. Cheilocystidia (Figs 9 , 10 ) plentiful, 25–40 × 4–15 µm, stalked, lobose-coralloid branched, often with diverticulate-lobed termini, hyaline, thin-walled. Stipe medullary hyphae 4–14 μm diam, strictly parallel, free (not involved in slime matrix), firm-walled, inconspicuously clamped; contents heterogeneous (multigranular). Stipe cortical hyphae 3–5 µm diam, apparently adherent, obscurely clamped, moderately dextrinoid (more or less hyaline without IKI, reddish brown with IKI), firm- to thick-walled (wall – 0.8 μm thick), clamped, producing side branches elongating into caulocystidia. Caulocystidia from upper stipe (Figs 8 A , 11 ) in delicate, interrupted patches – 80 × 4–10 µm, cylindrical to vermiform, usually somewhat gnarled distally with broadly rounded apex, thick-walled (wall often occluding cell lumen), arising as non-septate side branches from slender (1.5–3.5 µm diam, wall – 1.0 µm thick), superficial stipe surface hyphae, strongly dextrinoid (dark brownish red with IKI). Caulocystidia from lower stipe similar, a dense turf of free individuals (not involved in slime matrix), weakly to strongly dextrinoid, – 200 × 3–8 µm, thick-walled (wall / lumen distinction often impossible in IKI; wall – 1.0 µm thick, less dextrinoid than cell contents), tapering gradually to an acutely rounded apex, often gnarled and sometimes forked. Ample evidence of clamp connections in pileipellis, subpellis and pileus trama (i. e. hook cells of disarticulated clamps common and obvious) occasional complete clamps observed at basidial bases.

Habitat.

Tsuga debris and adjacent hardwood leaves.

Specimens examined.

Massachusetts, Plymouth County, Boston Harbor, World’s End Peninsula, coll LA Kappler, 23. VIII. 2015, ( HUH) BHI 447 (HUH-F- 00964493), Boston Harbor, World’s End Peninsula, Rocky Neck, coll D. Healewaters & LA Kappler, 12. VIII. 2015, ( HUH) BHI 401 (HUH-F- 00964494); World’s End Peninsula, coll D. Healewaters et al., 14. IX. 2013, ( HUH) BHI 034 (HUH-F- 00964495. North Carolina, Macon Co., vic. Highlands, Bull Pen Rd., Ellicott Rock Trailhead, 35 ° 01.010 ' N, 83 ° 08.190 ' W, 20. VII. 2011, coll RHP, TFB 13916 (TENN-F- 065811). Tennessee, Blount Co., GSMNP, Metcalf’s Bottoms Picnic Area, 9. VI. 1997, coll. RHP, TFB 9168 ( TENN 55766).

Commentary.

The strongly modified “ Rameales - structure ” of the pileipellis structures of C. complicata resembles that of species of traditional Marasmiellus [viz. C. ramealis complex, ( Petersen and Hughes 2021)]. This construction comprises a thatch of stalked, ventricose-rostrate structures with lobose, molar-shaped outgrowths. These pileipellis structures conform closely to those of Marasmiellus sect. Dealbati subsect. Dealbatini sensu Singer ( Singer 1973) [Type = Marasmius dealbatus Berk. & Curt. ], of which Marasmius stenophylla ( C. stenophylla , Fig. 2 ) is a member ( Desjardin 1997). M. stenophylla (section Dealbati ) was transferred to Gymnopus sensu lato ( Mata et al. 2004), then to Collybiopsis ( Petersen and Hughes 2021) . Both Desjardin ( Desjardin 1989; 1997) and Hesler (1959) examined type material of M. subsynodicus Murrill , considered by Singer ( Singer 1973) and Desjardin ( Desjardin 1997) to be synonymous with M. stenophylla (Mont.) Singer ). Marasmius dealbatus remains unplaced in modern classifications.

Parenthetically, in C. complicata collections TENN-F- 055766 and HUH-F- 00964493, the lobose individual pileipellis elements dominated the pileipellis, while in TENN-F- 065811 (also C. complicata ), these structures were only occasional in a pileipellis dominated by encrusted filamentous hyphae.

The pileipellis structure of Marasmius Sect. Androsacei (= Gymnopus sect. Androsacei , see Noordeloos and Antonín (2008), is also described as a combination of diverticulate, repent hyphae and siccus - type broom cells (a “ Rameales-structure ”). Our experience with this, however, indicates that the diverticulae (= setulae) of pileipellis cells are much finer, usually vermiform, refringent (PhC) and <1 µm broad. Cheilocystidia of C. complicata are very similar to pileipellis structures, but as a rule are somewhat less complexly branched. Morphologically, the pileipellis of C. complicata might be forced into section Androsacei , but phylogenetically, it is distant from that group in Gymnopus S. S.

Mata et al. (2007) initially designated TENN-F- 055766 (GenBank DQ 450029 , C. complicata ) as Marasmiellus sp. aff. pluvius, but while basidiomata of Marasmiellus pluvius Redhead ( Redhead 1982) have similar stature, they are smaller and are gregarious on Pseudotsuga and Thuja needle beds in southern British Columbia. Further, the pileipellis of Ma. pluvius does not include stalked-lobose structures, but is a “ compactly interwoven layer of densely diverticulate hyphae ” ( Redhead 1982); “ Rameales - structure ”). Cheilocystidia of Ma. pluvius are stalked-vesciculose to clavate with narrow, vermiform setulae quite similar to those of the Ma. ramealis complex. Basidiospores of Ma. pluvius are longer and significantly narrower than those of C. complicata and caulocystidia exhibit a significantly thicker wall than those of C. complicata . While perhaps morphologically congeneric with C. complicata in Collybiopsis , the two species are quite different microscopically and a second GenBank accession under the name Marasmiellus aff. pluvius ( MK 277736 ; NL- 5034: nrLSU sequence only) is 0.22 % different from other C. complicata nrLSU sequences. Marasmiellus pluvius has not yet been transferred to Collybiopsis , but DNA sequences will probably support such transfer when they become available, although specific placement in a phylogeny remains unknown.

The nrITS sequences for collections within C. complicata (Table 1 ) are genetically identical with the exception of a 1 bp C / T transition in TENN-F- 065811 from Macon County, GA (0.17 % difference). This lack of nrITS variation includes three nrITS sequences of specimens collected in a study of Boston ( MA) Harbor Islands ( Haelewaters et al. 2018), and one from the Great Smoky Mountains National Park TENN-F- 055766. Collybiopsis complicata , therefore, seems distributed extensively in temperate Eastern North America. The nearest taxon to C. complicata, GenBankaccession MK 234195 , differs by 6 base pairs (1.05 %) and while this falls within the commonly accepted criteria of 2 % divergence for conspecificity ( Hughes et al. 2009), the lack of variation within C. complicata across a wide geographic range (Boston Harbor Islands vs. Southern Appalachians) argues that C. complicata does not include MK 234195 . Possibly, C. complicata is a recently-diverging taxon that has not accumulated geographical differences.

Figures

Figure 2. NrITS-nrLSU based Maximum Likelihood consensus tree of the C. complicata / C. prolapsis clade with 1000 bootstrap replicates. The tree was generated using the web version of IQTree tree (http://iqtree.cibiv.univie.ac.at/) using the best-fit model of evolution (TIM 2 + F + I + G 4, AIC criteria). Included taxa were selected based on the Bayesian analysis which showed the C. complicata group and the C. ramealis group as sister taxa. Bootstrap support is indicated below the branches and Bayesian Posterior probabilities above the branches.

Figure 3. Collybiopsis complicata. Basidiomata. TFB 13916 (TENN-F- 065811). Scale bar: 10 mm.

Figure 4. Collybiopsis complicata. Pileipellis elements; repent, encrusted hyphae. Sx TFB 9168 (TENN-F- 055766). Scale bars: 10 mm.

Figure 5. Collybiopsis complicata. Pileipellis elements; pileocystidia A cluster of pileocystidia B, C “ Diverticulate ” repent hyphae D two lobose hyphal termini. Note clamp connections. TFB 9168 (TENN-F- 055766). Scale bars: 10 μm.

Figure 6. Collybiopsis complicata. Pleurocystidia Note clamp connection in C. TFB 9168 (TENN-F- 055766). Scale bars: 10 μm.

Figure 7. Collybiopsis complicata. Basidia. TFB 9168 (TENN-F- 055766). Scale bars: 10 μm.

Figure 8. Collybiopsis complicata A Caulocystidia B Basidiospores. TFB 9168 (TENN-F- 055766). Scale bars: 10 μm (A); 5 μm (B).

Figure 9. Collybiopsis complicata. Individual cheilocystidia. TFB 9168 (TENN-F- 055766). Scale bars: 10 μm.

Figure 10. Collybiopsis complicata. Clusters of cheilocystidia. HUH. HUH-F- 00964494. Scale bars: 10 μm.

Figure 11. Collybiopsis complicata. Caulocystidia. TFB 9168 (TENN-F- 055766) A caulocystidia from upper stipe B, C, D individual caulocystidia. Scale bars: 10 μm.