Marasmius haematocephalus (Mont.) Fr.

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 : 114-118

Marasmius haematocephalus (Mont.) Fr.

( Figs 13 ; 14 )

Epicrisis Systematis Mycologici, seu Synopsis Hymenomycetum: 382 ( Fries 1838). — Type: Brazil. Rio de Janeiro State, Rio de Janeiro City, Auguste de Saint Hilaire, holotype not found ( Singer 1976), or none located ( Desjardin 1989), or not extant ( Robert et al. 2013), or supposedly found in the PC herbarium (V. Antonín, pers. comm.).

Agaricus haematocephalus Mont., Annales des Sciences naturelles, Botanique, séries 2, 8: 369 ( Montagne 1837).

Androsaceus haematocephalus (Mont.) Pat. , Journal de Botanique (Morot) 3 (20): 336 ( Patouillard 1889).

Chamaeceras haematocephalus (Mont.) Kuntze, Revisio generum plantarum (Leipzig) 3 (3): 456 ( Kuntze 1898).

EPITYPE. — Brazil. São Paulo State, Iporanga City, Parque Estadual Turístico do Alto Ribeira, Núcleo Santana, 02.III.2012, J.J.S. Oliveira & D.E. Desjardin JO533 (epi-, designated here, SP[SP 445580]!), nrITS ( ON502673 ) and nrLSU ( ON502729 ).

ADDITIONAL EXAMINED MATERIAL. — Brazil. São Paulo State, São Paulo City, Parque Estadual da Cantareira, Núcleo Engordador, 16.II.2012, J.J.S. Oliveira & M. Capelari JO507 (SP[SP 446044]!); Iporanga City, Parque Estadual Turístico do Alto Ribeira, Núcleo Santana, 04.XII.2011, J.J.S. Oliveira JO435 (SP[SP 446079]!); 29.II.2012, J.J.S. Oliveira & D.E. Desjardin JO527 (SP[SP 446068]!); Amazonas State, Novo Airão City, Urubuquara, Rio Unini, 24.X.2019, J.J.S. Oliveira & Francisco JO1363 (INPA[INPA289980]!).

HABIT AND SUBSTRATE. — Marasmioid ( Figs 13 ; 14A 1), close, on dried eudicotyledonous petioles in the forest litter.

DISTRIBUTION. — The species was originally described from Rio de Janeiro, Brazil. Based on the present study, it is only confirmed in the Neotropics. In Brazil, it was reported from Amazonas State ( Berkeley 1856; Berkeley & Cooke 1876; Hennings 1904; this present study), Paraná State ( de Meijer 2001), Pernambuco State ( Kimbrough et al. 1995), Rio de Janeiro State ( Singer 1976), Rondônia State ( Capelari & Maziero 1988) and São Paulo State ( Spegazzini 1889; Grandi et al. 1984; Pegler 1997; Puccinelli & Capelari 2009). However, these collections need to be revised, especially from the other states far from Southeastern Brazil. Based on the traditional view, the species is pantropical, occurring in tropical forests of South America, Africa, Tropical Asia and Oceania.

DESCRIPTION

Pileus ( Figs 13 ; 14A 1)

2.5-16 mm diam., conical, hemispherical to convex, or campanulate, deeply sulcate, center flat, or wrinkled, margin decurved, edge entire to slightly crenate; dark purplish red (N 90 Y 00-40 M 99) when young, then deep to dark blood red (N 70 Y 50-90 M 99) or deep purplish red (N 80 Y 10-50 M 99), dark pinkish red almost purple (N 60 Y 50 M 80); membranous, context thin (<1 mm); glabrous, dry, dull, subvelutinous, non-hygrophanous.

Lamellae ( Figs 13 ; 14A 2 )

Free to narrowly adnate, distant, L = 7-10, equal, narrow, subcultriform, simple, l = 0, opaque, 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 (especially near the pileus edge).

Stipe ( Figs 13 ; 14A 1)

22.4-62 × 0.2-0.5 mm, central, filiform, thin, equal, sometimes with slightly broader base, with circular caliber, chitinous, hollow; apex concolorous with the lamellae, becoming bronze brown (N 40 Y 60 M 50 to N 80 Y 70 M 40) to dark brown (N 90 Y 99 M 80), or almost black at the base, glabrous, smooth, with a silky bright; with a scarce (subinsititious), white, tomentose basal mycelium.

Odor

Not distinctive.

Basidiospores ( Fig. 14B )

(18-)18.3-22.6(-23) × 3-4.9 µm (xrm = 20.1-21 × 3.8-4.2 µm; xmm = 20.5 [± 0.3] × 3.9 [± 0.2] µm; Qrm = 5-5.4; Qmm = 5.2 [± 0.1]; n/s = 30/5), oblong, clavate, subfusoid to fusoid, smooth, hyaline, thin-walled, inamyloid.

Basidia ( Fig. 14C )

19-26.8 × (5.6-)6.2-7.9 µm, clavate, smooth, hyaline to slightly fuscous, thin-walled, with four short and conical obtuse sterigmata, inamyloid.

Basidioles ( Fig. 14D )

(15-)18.5-25.9 × (3.3-)4.8-7.1 µm, cylindrical clavate, clavate, sometimes wavy or with tapered apex, smooth, hyaline to slightly fuscous, inamyloid.

Pleurocystidia ( Fig. 14E )

30.1-76.2 × 7-13.9(-15.5) µm, clavate or cylindrical clavate, lageniform, some capitate, papillate or rarely mucronate, occasionally wavy with apical and shallow constrictions, smooth, fuscous, thin-walled, refractive, inamyloid, abundant although sparse.

Cheilocystidia ( Fig. 14F )

Similar to the Siccus-type broom cells of the pileipellis, but hyaline and with thinner walls; main body 10.3-19.3 × 5.5- 10.6 µm, clavate to slightly turbinate, sometimes flat, seldom branched; setulae apical, erect, 2.1-5.2 × 0.5-1 µm, cylindrical or filiform, needle-like, rarely digitiform, regular in outline, simple or rarely branched, solid, hyaline to fuscous, apex acute.

Lamellar trama

Strongly dextrinoid, irregular, interwoven, hyphae cylindrical, 1.8-5.4 µm diam., regular in outline, branched, hyaline, thin-walled, smooth to slightly rough.

Pileus trama

Strongly dextrinoid, similar to the lamellar trama, hyphae 1.8-6.2 µm diam.

Pileipellis

Hymeniform, composed of Siccus-type broom cells ( Fig. 14G ), pale brown or chestnut brown, bleaching in KOH solution; main body 7.2-20.4 × 5.5-12.1 µm, clavate, turbinate, sometimes branched, ventricose, or flat, hyaline, thin-walled to slightly thick-walled (particularly at the apex), inamyloid; setulae apical, erect, 2.8-6.2 × 0.6-1.3 µm, cylindrical or filiform, needle-like, rarely digitiform, simple, regular in outline, solid, mostly pale brown, apex tapered, obtuse to slightly acute.

Stipe trama

Dextrinoid, especially the internal hyphae and those of the stipe apex, cortical hyphae parallel, packed, cylindrical, regular in outline, 2.7-7.7 µm diam., or slightly inflated, sometimes branched, smooth, dark chestnut brown, yellowish brown when separate, thick-walled; internal hyphae regular in outline, 1.8-8.1 µm diam., hyaline, parallel or interwoven, sometimes with short segments.

Clamp connections

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

REMARKS

Marasmius haematocephalus is the type species of Marasmius sect. Sicci subsect. Siccini ser. Haematocephali sensu Singer (1976) which is characterized by the presence of pleurocystidia, otherwise compatible with ser. Leonini ( Singer 1976). The species epithet means blood red head, (from Greek αίματΟς [haimatos] and ΚΕΦάλι [kephali]), “ rubro -sanguineo ” pileus in the protologue. According to a broad concept, this species seems to produce basidiomata with a high variability of characteristics, especially in the pileus pigmentation, length and shape of both spores and pleurocystidia, and substrate preference. Based on Singer (1958), M. haematocephalus is typically, as the description in the protologue indicates, uniformly blood red, purple, deep purple (not violet) pileated. In Singer (1965, 1976), the sulcate pilei have a large color range of variation from pink, red to purple, even brownish, and with shapes from campanulate, hemispherical, convex to plane. Even obeying a reasonable morphological species spectrum, the criptic nature of taxa in species complex and/ or a non-fine species characterization has made M. haematocephalus a receptacle of many misdetermined specimens with an allegedly pantropical distribution.

After matching Montagne (1837) and Fries (1838) concepts, the topotypical examined material also agrees with Singer (1958, 1965, 1976) in nearly all aspects. We intended to examine “ R. Singer C 3172 ” and confirm compatible spores’ dimension. We contacted BAFC herbarium to search for Singer’s topotype collection, but without reply during this pandemic time. Antonín (2007) and Shay et al. (2017) mentioned the collection as neotype but did not examine it. Vladimír Antonín (pers. comm.) informed he has a specimen on loan from PC herbarium named as M. haematocephalus collected by Auguste de Saint Hilaire from Brazil that is possibly the authentic type. He shared pictures of the dried specimen that seems macromorphologically quite simitar to our specimens. The examined material herin also agrees with “French Guyana, Ann. 1850, M. Leprieur nº 990 (PC)”, determined by Montagne as M. haematocephalus , and fully revised by Desjardin (1989), but the basidiospores in the Leprieur’s collection seems smaller (16-21.6 × 4.4-5.6µm, xm = 19.1 [± 1.3] × 4.7 [± 0.4] µm, Q = 3.5-4.6, Qm = 4.1 [± 0.3], n = 18).

There was a probable confusion in Dennis (1951); where M. tageticolor Berk. , should be M. haematocephalus from Trinidad (fresh collection), Dominique (type of M. sanguineus Cooke & Massee ) and Bahamas (type of M. atropurpureus Murrill ), compatible with our collections except for the distinctly marginate lamellae of these two later. In fact, Singer (1976) considered M. sanguineus and M. atropurpureus synonyms under M. haematocephalus . However, would the ventricose (broad), distinctly marginate lamellae (edge concolorous with the pileus) be compatible with the protologue of M. haematocephalus? In Singer (1976) , the lamellar edges are not concolorous with the pileus in mature basidiomata except “sometimes” near the pileus margin. It is possible that Singer’s concept was broadened to include the synonyms. Marasmius haematocephalus in Desjardin (1989), of collections from North America forests in the United States (Florida, North Carolina and Tennessee) along with collections from British Honduras, Cuba and Guyana, differs from the examined material only in having more numerous (10-15), broad (up to 2.5 mm), and marginate (pinkish red, deep reddish or violet red) lamellae (sometimes non-marginate) and a wider spore range (16-22 × [3.6-]4-5.6 µm). If the broad, marginate lamellae is a strong diagnostic characteristic in separating species, then there are M. haematocephalus with non-marginate lamellae vs M. sanguineus (synonym: M. atropurpureus ) with marginate lamellae. Thus, the collections with marginate lamellae from North America examined in Desjardin (1989) may be M. sanguineus (or M. atropurpureus ) instead of M. haematocephalus . Pegler (1983) should have had a broad (mix) concept on examined collections from Martinique, Trinidad, Dominique (including the type of M. sanguineus ) and Sri Lanka (type of M. semipellucidus ). The spore range was shorter (16-20 × 3-4.5 µm) than those of collections from São Paulo (18-22 × 3.7-4.5 µm) in Pegler (1997), this later more compatible (the purplish red pileus) with our collection as well as in Dennis (1970) from Venezuela (bright purple pileus with 19-21 × 3-4 µm basidiospores). With the finetuned concept of M. haematocephalus (s. str.) in this study, its various heterotypic synonyms listed in Singer (1976) and other need to be carefully reevaluated in future studies. By revising their protologues (Appendix), none of them seems morphologically compatible with M. haematocephalus s. str. except for the illegitimate M. vinosus Beeli from Africa.

In Brazil, according to the speciesLink – Virtual Herbarium of the Centro de Referência em Informação Ambiental, CRIA (splink.org.br, accessed in November 17th, 2019), 241 collections determined as M. haematocephalus are currently deposited in 23 Brazilian herbaria, collected from the states of Amazonas, Bahia, Espírito Santo, Maranhão, Minas Gerais, Pará, Paraíba, Pernambuco, Piauí, Rio de Janeiro, Rio Grande do Norte, Rio Grande do Sul, Rondônia, Roraima, Santa Catarina and São Paulo ( Brazil). A review of these material is due in another paper considering the M. haematocephalus (s. str.) or M. rubicundus system. Singer (1976) recognized nine varieties in M. haematocephalus based on subtle distinctions and overlapping morphological characteristics: 1) atroviolaceus Singer; 2) haematocephalus ; 3) leucophyllus Singer; 4) macrocephalus Singer; 5) oenechinus Singer; 6) pseudotageticolor Singer (partly marginate lamellae, red); 7) purpureomarginatus Singer (marginate lamellae, garnet red); 8) rubicundus Singer ; and 9) transiens Singer. All these varieties are from the Neotropical realm, mostly from forests of South America. Except for the 8th, these taxa need to be reevaluated with fresh collections. The sixth and seventh may be morphologically compatible with those in Desjardin (1989) with marginate lamellae. In Pegler (1987), the supposed (seems not formalized) additional M. haematocephalus var. obscurior Berk. & Curtis from Cuba has pileus browner than the typical form and with marginate lamellae, more compatible with M. hypophaeus . Desjardin (1991) proposed M. haematocephalus var. anomaloides Desjardin , of collections from Tennessee, United States.

According to the current broad morphological concept, M. haematocephalus has been reported from various localities in South and Central America including some Caribbean islands (Neotropics), and less frequently from southern continental and insular North America (Nearctic) ( Singer 1965, 1976; Dennis 1970; Pegler 1983, 1997; Desjardin 1989), Tropical Africa including Madagascar ( Singer 1964; Pegler 1977; Antonín 2007; Shay et al. 2017), Tropical Asia ( Petch 1948; Pegler 1986; Desjardin et al. 2000; Tan et al. 2009; Wannathes et al. 2009) and Oceania ( Desjardin & Horak 1997). These collections need to be reevaluated given these new data and analyses, and a better understanding of the species complex.

Marasmius haematocephalus may be confused with M. asiaticus , M. pallescens , M. panerythrus Singer , M. pulcherripes , and M. rhodopurpureus Antonín, R.Ryoo & H.D.Shin. Marasmius asiaticus differs by having “less violet” pileus, less numerous lamellae (7-8), slightly larger basidiospores (18.5- 23[-25] × 3.5-5[-6] µm) and a mottled pileipellis ( Tan et al. 2009; as M. distantifolius ). Maramius pallescens differs by having a pale red pileus, shorter basidiospores (11-17 µm in length) and mottled pileus ( Singer 1976). Marasmius panerythus and M. pulcherripes diverges by having shorter basidiospores (13-14 µm in length [ Singer 1976] and [11-]12-15[-16] µm [ Desjardin 1989; Antonín et al. 2012], respectively); and M. rhodopurpureus also has shorter basidiospores (12-15[- 16] µm) and shorter (35-42 µm), non-refractive, clavate pleurocystidia ( Antonín et al. 2012).

In the phylogenetics trees (Figs1; 3), various strains named after M.haematocephalus in previous studies forming a pantropical distribution branched in multiple lineages (para- or polyphyletic), indicating them to be not a single but close, cryptic species in haemat_cp1. Based on combined nrLSU + nrITS data, M. haematocephalus s. str. (JO533) branched in a distinct phylogenetic position as sister to M. auranticapitatus J.S. Oliveira , sp. nov. + M. rubicundus (Singer) J.S. Oliveira , stat. nov. ( Fig. 4 ).

Figures

FIG. 13. — Pictures of fresh basidiomata of Marasmius haematocephalus (Mont.) Fr.: A, JO533 from Atlantic Rainforest (epitype); B, JO1363 from Amazon Forest. Scale bars: 10 mm.

FIG. 14. — Marasmius haematocephalus (Mont.) Fr.(JO533): A1, A2, basidiomata; B, basidiospores;C, basidioles; D, basidia; E, pleurocystidia; F, cheilocystidia; G, Siccus-type broom cells of the pileipellis. Scale bar: A1, 8.9 mm; A2, 5.9 mm; B-G, 10 µm.

FIG. 2. — Best-scored Maximum Likelihood Tree (TL = 0.164547) built from multilocus (nrITS and nrLSU) analysis based on siccus_cp1 in Fig. 1 (DATASET 2a). Support values are BS (70 to 100%) and PP (0.95 to 1.0). Black, thick stems indicate high support and gray, thick stems indicate weak to moderate support. The gray shades highlight siccus_cp2a, siccus_cp2b, and M. siccus s. str. Blue arrows indicate the geographic origin of the strains. Global map is based on Olson & Dinerstein (2002) with forested areas depicted in their biogeographic realms.

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.