Marasmius rubicundus (Singer) J.S. Oliveira, 2022

S, Jadson José, Oliveira, ouza de, Capelari, Marina, Margaritescu, Simona & Moncalvo, Jean-Marc, 2022, Disentangling cryptic species in the Marasmius haematocephalus (Mont.) Fr. and M. siccus (Schwein.) Fr. species complexes (Agaricales, Basidiomycota), Cryptogamie, Mycologie 20 (5), pp. 91-137 : 120-124

Marasmius rubicundus (Singer) J.S. Oliveira , stat. nov.

( Figs 15B ; 18 )

Marasmius haematocephalus var. rubicundus Singer , Sydowia 18: 337 ( Singer 1965). — Type: Bolivia. La Paz, Nor-Yungas, Charobamba, 1300 m a.s.l., 30.I.1956, Singer B 743 (LIL), holotype; Singer B 737 (LIL); Coroico, 1700 m a.s.l., 7.II.1956, Singer B 945 (LIL); Beni, Vaca Diez, Guayaranerin, 4.III.1956, Singer B 1963 (LIL); Singer B 1755 (LIL).

EPITYPE. — Brazil. São Paulo State, São Paulo City, Parque Estadual da Cantareira, Núcleo Engordador, 30.I.2012, J.J.S. Oliveira & V. Motato-Vásquez JO464 (epi-, designated here, SP[SP 445549]!), nrITS ( ON502658 ) and nrLSU ( ON502728 ).

ADDITIONAL EXAMINED MATERIAL. — Brazil. São Paulo State, Santo André City, Reserva Biológica de Paranapiacaba, 16.XII.2009, M. Capelari & L.A.S. Ramos 4567 (SP[SP 445931]!); M. Capelari & L.A.S. Ramos 4570 (SP[SP 446073]!); 14.I.2010, J.J.S. Oliveira & M. Capelari JO1 (SP[SP 446075]!); 16.III.2010, J.J.S. Oliveira JO43 (SP[SP 446069]!); 15.X.2010, J.J.S. Oliveira & C.L.A. Pires JO223 (SP[SP 446074]!); 16.X.2010, J.J.S. Oliveira & C.L.A. Pires JO228 (SP[SP 445448]!); J.J.S. Oliveira & C.L.A. Pires JO230 (SP[SP 446076]!); 17.X.2010, J.J.S. Oliveira & C.L.A. Pires JO245 (SP[SP 446046]!); J.J.S. Oliveira & C.L.A. Pires JO246 (SP[SP 445454]!); 5.XI.2010, J.J.S. Oliveira JO261 (SP[SP 446051]!); 7.XI.2010, J.J.S. Oliveira & A.V. Costa JO275 (SP[SP 446059]!); 7.XII.2010, J.J.S. Oliveira, P.O. Ventura & A.V. Costa JO281 (SP[SP 445464]!); J.J.S. Oliveira, P.O. Ventura & A.V. Costa JO283 (SP[SP 446061]!); J.J.S. Oliveira, P.O. Ventura & A.V. Costa JO295 (SP[SP 446063]!); J.J.S. Oliveira, P.O. Ventura & A.V. Costa JO296 (SP[SP 445476]!); 9.XII.2010, J.J.S. Oliveira, P.O Ventura & A.V. Costa JO316 (SP[SP 445488]!); J.J.S. Oliveira, P.O. Ventura & A.V. Costa JO318 (SP[SP 446048]!); J.J.S. Oliveira, P.O. Ventura & A.V. Costa JO319 (SP[SP 446047]!); São Paulo City, Parque Estadual das Fontes do Ipiranga, 1.III.2011, J.J.S. Oliveira & F. Karstedt JO330 (SP[SP 446065]!); J.J.S. Oliveira & F. Karstedt JO335 (SP[SP446067]!); J.J.S. Oliveira & F.Karstedt JO338 (SP[SP 446066]!); 18.X.2011, J.J.S. Oliveira & P.O.Ventura JO380 (SP[SP 446064]!); São Paulo City, Parque Estadual da Cantareira, Núcleo Engordador, 19.XII.2011, J.J.S. Oliveira & M. Capelari JO445 (SP[SP 445537]!); J.J.S. Oliveira & M. Capelari JO446 (SP[SP 446054]!); J.J.S. Oliveira & M. Capelari JO447 (SP[SP 446053]!); 9.II.2012, J.J.S. Oliveira & M. Capelari JO481 (SP[SP 446043]!); J.J.S. Oliveira & M. Capelari JO482 (SP[SP 446055]!); J.J.S. Oliveira & M. Capelari JO483 (SP[SP 445560]!); 16.II.2012, J.J.S. Oliveira & M. Capelari JO492 (SP[SP 446045]!); J.J.S. Oliveira & M. Capelari JO514 (SP[SP 446071]!); J.J.S. Oliveira & M. Capelari JO516 (SP[SP 446057]!); Iporanga City, Parque Estadual Turístico do Alto Ribeira, Núcleo Santana, 29.II.2012, J.J.S. Oliveira & D.E. Desjardin JO529 (SP[SP 445577]!); D.E. Desjardin DED8675 (SP[SP 445665]!); Lageado, 29.II.2012, J.J.S. Oliveira & D.E. Desjardin JO534 (SP[SP 446077]!).

MYCOBANK. — MB 842539.

HABIT AND SUBSTRATE. — Marasmioid ( Figs 15A ; 18A ), solitary to gregarious, on dried eudicotyledonous leaves and sticks in the forest litter.

DISTRIBUTION. — Originally from La Paz and Beni, Bolivia, as M. haematocephalus var. rubicundus ( Singer 1965, 1976), it is now known from Southeastern Brazil.

DESCRIPTION

Pileus ( Figs 15A ; 18A )

2.5-20.5 mm diam., conical, hemispherical to convex, sulcate, center flat to umbonate, smooth or somewhat wrinkled, margin decurved to almost straight, edge entire to crenate; sometimes pale pinkish beige or salmon color (N 10 Y 20 M 40 to N 10 Y 30 M 50), often “Canna” pink or rose (N 20 Y 00-20 M 40-60), tending to very pale pinkish lilac (N 20 Y 20 M 60), then vibrant or ruby pink (N 40 Y 50 M 80), pinkish red (N 20 Y 50 M 70, N 20 Y 60 M 70 to N 20 Y 70 M70), or pinkish brown “Egyptian red” (N 40 Y 50- 60 M 60), sometimes pink with a slight hue of yellow (N 30 Y 50 M 50), or many times pale red or “Carnelian” (N 60 Y 40-60 M 90-99), light reddish brown (N 50-60 Y 90-99 M 90), with center darker red (N 70 Y 60 M 99) or pinkish brown (N 50 Y 70 M 70), or dark lilac (N 70 Y 00 M 99) or dark pink (N 70 Y 40 M 90); membranous, context thin (<1 mm); glabrous, dry, dull, papyraceus to subvelutinous, non-hygrophanous.

Lamellae ( Figs 15A ; 18A )

Free, adnexed, or sinuate to narrowly adnate, distant to subdistant, L = 7-12, equal, narrow to broad, straight, cultriform to ventricose, simple, l = 0 (-1), dull, smooth, white to cream (N 00 Y 10 M 00), or whitish pink (N 00 Y 10 M 10 or N 00 Y 40 M 10-20), edges even, non-marginate, interlamellar hymenium concolorous with the lamellae faces or partly concolorous with the pileus.

Stipe ( Figs 15A ; 18A )

8-63 × 0.3-0.8 mm, central, filiform, thin, equal, sometimes with broader base, with circular caliber, compressed when dried, chitinous, hollow; apex pale pink (N 00 Y 10 M 10 or N 30 Y 50 M 80) becoming bronze brown (N 40 Y 60 M 50 to N 80 Y 70 M 40) to dark brown (N 80 Y 99 M 30), or almost black at the base, glabrous, smooth, with a silky bright; with a scarce, white, tomentose basal mycelium.

Odor

Not distinctive.

Basidiospores ( Fig. 18B )

(15.4-)16.2-21.7(-22)×2.7-4.7(-5) µm (xrm = 18-19.7 × 3.5-4 µm; xmm = 19 [± 0.5] × 3.8 [± 0.2] µm; Qrm = 4.6- 5.5; Qmm = 5 [± 0.3]; n / s = 30/28), exceptional spore size of JO316 with 18.3-23.9 × 3.1-4.8 µm (xm = 21.3 [± 1.3] × 3.9 [± 0.4] µm; Qm = 5.4 [± 0.6]; n / s = 30/1), oblong, clavate to subfusoid, smooth, hyaline, thin-walled, inamyloid.

Basidia ( Fig. 18C )

21.3-36.3 × 6-7.5 µm, clavate, smooth, hyaline to slightly fuscous, thin-walled, 4-sterigmate, inamyloid.

Basidioles ( Fig. 18D )

22-28.8 × 5.6-8.8 µm, clavate, sometimes as cystidioles, smooth, hyaline to slightly fuscous, inamyloid.

Pleurocystidia ( Fig. 18E )

(19.5-)25.6-71.7 × 5-12.3 µm, broadly clavate, capitate, almost mucronate or acuminate, with a conical apex, or ampullaceous, or occasionally with apical, serial, slight constrictions, ending with a capitule, smooth, slightly fuscous, thin-walled, refractive, inamyloid, abundant.

Cheilocystidia ( Fig. 18F )

Similar to the Siccus-type broom cells of the pileipellis; main body 11.3-20 × 5.6-10.6 µm, clavate to slightly turbinate, wall somewhat thick, hyaline; setulae more strictly apical, rarely somewhat divergent, erect, 2-7.5 × 0.5-1 µm, cylindrical, digitiform or needle-like, simple, solid, hyaline to pale brown, regular in outline, apex obtuse to slightly acute.

Lamellar trama

Dextrinoid, irregular, interwoven, hyphae cylindrical, 1.5-10 µm diam., regular in outline,branched, hyaline, thin-walled,smooth.

Pileus trama

Dextrinoid, similar to the lamellar trama, hyphae 2-10 µm diam.

Pileipellis

Hymeniform, composed of Siccus-type broom cells ( Fig.18G ), abundant, brown when grouped, bleaching in KOH solution; main body 7.5-20 × 6.3-11.3 µm, clavate, turbinate, sometimes branched, ventricose to irregular in outline, hyaline, thin-walled to slightly thick-walled, weakly dextrinoid; setulae apical, erect, 2-7.5 × 0.6-1 µm, cylindrical, digitiform or needle-like, simple, regular in outline, or slightly contorted, solid, hyaline to pale brown, apex obtuse to slightly acute.

Stipe trama

Dextrinoid especially the internal hyphae and those of the stipe apex, cortical hyphae parallel, cylindrical, regular in outline, 3.8-8 µm diam., smooth, dark chestnut brown, yellowish brown when separated, thick-walled; internal hyphae regular in outline, 2.5-6.5 µm diam., parallel.

Clamp connections

Present in all tissues, except in the cortical hyphae of the stipe.

REMARKS

The type collections were not examined in the present study as we had no reply from LIL herbarium in this pandemic time. However, Singer (1965, 1976) provided enough morphological data to unambiguously determine the examined specimens from São Paulo as authentic representatives of M. haematocephalus var. rubicundus . The pigmentation and size of the pileus, the number of lamellae, and the size of the basidiospores (15-21 × 4-4.8 µm in Singer [1976]) match the examined material. Marasmius rubicundus is 0.7-0.9 % (nrITS) and 0.5-0.7 % (nrLSU) dissimilar to M. haematocephalus , but cladogenesis reveals vicariance in sympatry. In the phylogenetic trees (Figs 1; 3) of nrITS, M. rubicundus (Singer) J.S. Oliveira , stat. nov., M. auranticapitatus J.S. Oliveira , sp. nov., and M. haematocephalus are embedded within haemat_cp2a. In multilocus analyses, nrITS + nrLSU ( Fig. 4 ) and nrITS + rpb 2 + ef 1 - α ( Fig. 5 ), three species were resolved within this complex: M. rubicundus (Singer) J.S. Oliveira , stat. nov. sister to M. auranticapitatus J.S. Oliveira , sp. nov. with high support, and paraphyletic to M. haematocephalus .

Morphologically, M. rubicundus (Singer) J.S. Oliveira , stat. nov. is very similar to M. haematocephalus , only more conspicuously distinct by having a lighter pileus pigmentation and slightly smaller basidiospores (x mm = 18.9 [± 0.5] × 3.8 [± 0.1] µm, Qmm = 5 [± 0.2] vs xmm = 20.5 [± 0.3] × 3.9 [± 0.2] µm, Qmm = 5.2 [± 0.1]). Marasmius haematocephalus s. str. regards the “ rubro -sanguineo ” of its protologue as deep or dark blood red or vinaceous ( Singer 1958). In fact, the separation of M. rubicundus (Singer) J.S. Oliveira , stat. nov. and M. haematocephalus is very narrow in a broad sense, as they are nearly identical in other morphological characteristics. The species divergence is only evident in multilocus phylogenetic analyses where M. rubicundus (Singer) J.S. Oliveira , stat. nov. is rather closer to M. auranticapitatus J.S. Oliveira , sp. nov. ( Figs 4 ; 5 ). The exceptional spore sizes of JO316, possibly a hybrid, strenghtens the plausibility of the most recent common ancestor between them. Although speciation is demonstrated, this ancestry trace or possible partial intercompatibility and gene flow are elements of a recent divergence. The strain JO316 seems in a transitional/ intermediate position ( Fig. 4 ) along with other strains of M. rubicundus (Singer) J.S. Oliveira , stat. nov., but the basidiospores are more compatible with M. auranticapitatus J.S. Oliveira , sp. nov.. JO316 and JO226 highlights the powerful phylogenetic signal of spore sizes, an evident correlation between this characteristic and the genotype behind the species concepts.

The pale red pileus in M. rubicundus (Singer) J.S. Oliveira , stat. nov. is consistent with M. pallescens , but this later has shorter (11-17 µm) basidiospores ( Singer 1976). For more color pictures showing variation of pileus pigmentation of M. rubicundus (Singer) J.S. Oliveira , stat. nov., see Appendix ( Figs S7-S 11 ). It is not similar to any of the heterotypic synonyms of M. haematocephalus listed in Singer (1976) but M. rhodocephalus Fr. ( Fries 1851; Appendix) with type presumed lost but connection is not sharp.

Figures

FIG. 15. — Pictures of fresh basidiomata: A, Marasmius roseus J.S. Oliveira, sp. nov. (JO352); B, M. rubicundus (Singer) J.S. Oliveira, stat. nov. (JO464); C, M. cf. pallescens Murrill (JO426). Scale bars: 10 mm.

FIG. 18. — Marasmius rubicundus (Singer) J.S. Oliveira,stat. nov.(JO464): A, basidiomata; B, basidiospores;C, basidia; D, basidioles;E, pleurocystidia;F, cheilocystidia; G, Siccus-type broom cells of the pileipellis. Scale bar: A, 19.2 mm; B-G, 10 µm.

FIG. 4. — Best-scored Maximum Likelihood tree (left side, TL = 0.054576) and 50% majority-rule consensus tree (right side, TL = 4.954404) of Bayesian analyses built from multilocus (nrLSU and nrITS) analyses (DATASET 3) of the haemat_cp2a (Fig. 3). Black, thick stems indicate high support and gray, thick stems indicate weak to moderate support. Dark red shade indicates M. haematocephalus (Mont.) Fr., the orange shade indicates M. auranticapitatus J.S. Oliveira, sp. nov. and the pink shade indicates M. rubicundus (Singer) J.S. Oliveira, stat. nov.

FIG. 5. — Best-scored Maximum Likelihood trees (left side,TL = 0.111755;0.135069) and 50% majority-rule consensus trees (right side, TL = 0.106492;0.120539) of Bayesian analyses built from multilocus (nrITS + rpb2 + ef1-α) analyses (DATASET 4) of the haemat_cp2a (Fig. 3). Black, thick stems indicate high support and gray, thick stems indicate weak to moderate support. Orange shade indicates M. auranticapitatus J.S. Oliveira, sp. nov. and the pink shade indicates M. rubicundus (Singer) J.S. Oliveira, stat. nov. Trees on the top includes MC4554 (holotype of M. auranticapitatus J.S. Oliveira, sp. nov.).

FIG. 7. — Marasmius bambusinus (Fr.) Fr. (JO343): A, basidiomata; B, basidiospores;C, basidia; D, basidioles; E, pleurocystidia; F, cheilocystidia; G, Siccus-type broom cells of the pileipellis. Scale bar: A, 10.3 mm; B-G, 10 µm.

FIG. 11. — Marasmius castanocephalus J.S. Oliveira, sp. nov. (JO523): A1, A2, basidiomata; B, basidiospores; C, basidioles; D, pleurocystidia; E, cheilocystidia; F, Siccus-type broom cells of the pileipellis. Scale bar: A1, 18 mm; A2, 10 mm; B-F, 10 µm.