Ganoderma parvulum Murrill, Bull. Torrey Bot. Club. 29: 605 (1902)

Cabarroi-Hernandez, Milay, Villalobos-Arambula, Alma Rosa, Mabel Gisela Torres-Torres,, Decock, Cony & Guzman-Davalos, Laura, 2019, The Ganoderma weberianum - resinaceum lineage: multilocus phylogenetic analysis and morphology confirm G. mexicanum and G. parvulum in the Neotropics, MycoKeys 59, pp. 95-131 : 95

Ganoderma parvulum Murrill, Bull. Torrey Bot. Club. 29: 605 (1902) Figs 4 , 8

≡ Fomes parvulus (Murrill) Sacc. & D. Sacc, Syll. Fung. (Abellini). 17: 123 (1905) [MB241944]

= Fomes stipitatus Murrill, Bull. Torrey Bot. Club. 30(4): 229 (1903) [MB241804]

≡ Ganoderma stipitatum (Murrill) Murrill, N. Amer. Fl. (New York) 9(2): 122 (1908) [MB451185]

= Fomes subamboinensis Henn., Hedwigia 43(3): 175 (1904) [MB148868]

≡ Ganoderma subamboinense (Henn.) Bazzalo & J.E. Wright ex Moncalvo & Ryvarden, Synopsis Fungorum 11: 82 (1997) [MB249603]

≡ Ganoderma subamboinense var. subamboinense Bazzalo & J.E. Wright Mycotaxon 16(1): 302 (1982) [MB417363] (invalid)

Description.

Basidiome annual, sessile or stipitate, solitary or sometimes concrescent or forming several (up to 3) pileus, light in weight, consistency corky-woody; pileus projecting 4.5-8 cm, 6.5-15 cm wide, up to 0.8-3 cm thick at the base, 0.5-0.7 cm at the margin; dimidiate, flabelliform to conchate in pole view, applanate or convex in section; stipe absent or 1.5-4.5 (-8) × 0.5-3 cm, horizontal or dorsally lateral, short and thick or long and tortuous, slightly swollen at the base, laccate, reddish brown (9F6) to dark brown (9F4) or violet brown (10F8) to almost black, stumpy or cylindrical, sometimes with laterals branches; pileal surface smooth, laccate, radially rugose or with concentric deep sulcations or occasionally, slightly zonate with dark lines, fully reddish brown (9F8) to violet brown (10F8), or gradually lighter towards the margin with a yellowish orange (5A7) band; margin white to pale yellow (4A3) or greyish yellow (4C7) to yellowish orange (5A7), entire to slightly lobulated, sometimes incurved; pore surface white, yellowish white (3A2), dull yellow (3B3), or sun yellow (2A5) when fresh and actively growing, greyish yellow (4C7), yellowish brown (5E7), or brownish orange (5C3) on drying, bruising dark brown (6F5), sometimes marked with spots of same aspect than pilear surface (laccate, reddish brown, 9F8); pores 4-5 per mm, round to mainly angular; context 0.3-2.4 cm thick, fibrous, homogeneous to slightly heterogeneous, sometimes zonate, greyish yellow (4B5) to greyish orange (5B3) toward the crust, and brownish orange (6C4) to light brown (6D4) in a narrow zone above the tubes, changing to yellow when cut in fresh specimens, with none to few to several (up to 4) resinous incrustations or occasionally resinous bands (up to 4), sometimes with yellow (3B8) spots throughout the context, with a yellow (3B8) to yellowish orange (4A7) thin line just below the crust; tubes 0.2-0.6 cm long, unstratified, concolorous with lower part of the context.

Hyphal system dimitic; generative hyphae 1.6-3.2 µm diam., septate, thin-walled with clamp connections, non-branched, hyaline to yellowish; somatic hyphae as arboriform skeleto–binding hyphae, golden yellow, composed of a basal stalk arising from a clamp, with several secondary processes, branches gradually tapering from 6 µm wide in the primary processes to 1.5-2 µm wide at the thin-walled apices, thick-walled to solid. Pileipellis a crustohymeniderm; cuticular cells clamped at the basal septum, pedicelated, mainly cylindrical to clavate, occasionally slightly apically capitate, rarely with 1-2 lateral protuberances, with regular, rounded end, thick-walled to almost solid, amyloid, the apex occasionally with a radial fine granulation, 40- [~ 60] -75 (-100) x 5-10 um. Hymenium: basidia not seen; basidiospores ovoid to broadly ovoid, the apex shrunken, appearing truncate, exosporium with thick, free to subfree pillars, (6-) 8- [8.9] -9.5 × (4.8-) 5.5- [6.0] -6.5 (-7) µm, Q = 1.45- [1.48] -1.46, ovoid; spore print (6E5), light brown (estimated from spore deposit on the pileus). Chlamydospores in the basidiomata absent, rare, to variably abundant, only in the context, subspherical, ellipsoid, or citriform, sometimes spindle-shaped, terminal or intercalated; smooth-walled to roughened with fine, isolated to partially anastomosed ridges, having a meridian orientation, variably stretching between the two extremities, totally dextrinoid or with dextrinoid content and golden wall, 7-13 × 6-12 µm. Chlamydospores always abundant in pure culture on malt agar, spherical to ellipsoid, sometimes spindle-shaped, often truncated at both ends; terminal or intercalary; when terminal with the apex occasionally papillated; single or golden double walled; with several large guttulae, with dextrinoid contents; smooth first then variably roughened, ornamented with fine partial or continuous ridges, isolated to partially anastomosed, 11-16 (-17.5) × 9-14.5 (-16) µm.

Holotype.

NICARAGUA. C.L. Smith s.n. (NY 985699!).

Known distribution.

Brazil, Colombia, Costa Rica, Cuba, French Guiana, Mexico, Nicaragua, South–eastern USA (Florida).

Specimens examined.

BRAZIL. St. Clara: Río Juruá, Oct 1900, E. Ule 2748, (under Fomes subamboinensis as type of G. subamboinense , F15183 (S). COSTA RICA. Puntarenas: Isla del Coco, orilla del río Genio, represa hidroeléctrica, 0-100 m s.n.m., 5 Jun 2005, E. Fletes– 7619, Lote: 84813 (INB 3976555); Osa, P.N. Corcovado, Estación Sirena, Sendero Guanacaste, bosque primario, 10 m s.n.m., E. Fletes– 266, Lote: 53967 (INB 1546586), río Madrigal, quebrada Ceniza, 200 a 300 m s.n.m., 19 Mar 2003, E. Fletes– 4943, Lote: 73208 (INB 3700175). CUBA. Province La Habana: Municipality Boyeros, Zoológico Nacional de Cuba, on base of a living trunk, 22 Aug 2001, C. Decock and S. Oliva, MUCL 43522 (culture ex. MUCL 43522); Finca La Chata, on base of a living trunk of Casuarina equisetifolia , 27 May 2002, C. Decock w/o #, MUCL 43863 (culture ex. MUCL 43863); Province Villa Clara: Falcon, Carretera Central, dead stump of Casuarina equisetifolia , Aug 2002, C. Decock, CU– 02/14, MUCL 44148 (culture ex 44148 = CRGF 715); Province Sancti Spiritus: Topes de Collantes, on the way to the Caburni, dead trunk, unidentified angiosperm, Sep 2004, C. Decock, CU– 04/12, MUCL 46029 (culture ex 46029 = CRGF 202); Sep 2005, C. Decock, CU– 05/196 (MUCL 47074, culture ex 47074 = CRGF 719); Province Pinar del Río: La Palma, near the Motel La Ciguaraya, decaying stump, unidentified angiosperm, Oct 2005, C. Decock, CU– 05/246, MUCL 47096 (culture ex 47096 = CRGF 722). FRENCH GUIANA. Nouragues National Reserve, Inselberg CNRS research station, dead fallen trunk, unidentified angiosperm, Aug 2010, C. Decock, FG/10-283, MUCL 53123 (culture ex. 53123); 2011, C. Decock, FG/11-481, MUCL 53712 (culture ex. 53712). MEXICO. State of Veracruz: Zentla, camino Huatusco–Maromilla, a la altura de Puentecilla, bosque mesófilo de montaña, alt. 860 m s.n.m. (as G. lucidum ), A. Sampieri 84 (XAL). NICARAGUA. C.L. Smith s.n., as F. stipitatus (holotype of G. stipitatum , NY 985678); C.L. Smith s.n., as F. stipitatus ( “TYPE” of G. stipitatum , NY 985679); without data, C.L. Smith s.n., as F. stipitatus ("Probable TYPE" of F. stipitatus , det. as G. parvulum by Steyaert 1961, NY 985716).

Additional species examined.

BRAZIL. Rio Grande do Sul: Lageado, without date, R. Rick s.n. (holotype of G. perturbatum ) (BPI). CUBA. Province La Habana: Municipality Santiago de Las Vegas, on mango log, 1904, F.S. Earle 309 (holotype of G. perzonatum , NY 985702); on dead mango, 5 Jul 1904, F.S. Earle 658 (holotype of G. argillaceum , NY 01293316). GRENADA. Without data, on dry manchinell, 14 Sep 1905, W.E. Broadway s.n. (holotype of G. pulverulentum , NY 00985705). INDONESIA. Java: without data, P. Serre s.n. (type of G. rivulosum , F181158, S). MEXICO. Estado de México: valle del Tepeite, 10 km NE of Santa María, 10 Aug 1986, E. Bastidas-Varela s.n. (holotype of G. vivianimercedianum , ENCB). SAMOA ISLAND. Without data, Weber s.n. (as “TYPUS” of Fomes weberianus F15098, S); without data, Weber s.n., as Fomes weberianus (B 700021870), " Fomes weberi "), without data, Weber s.n., as Fomes weberianus (B 700007410, “TYPE” of G. weberianum ). TAIWAN. Taipei: on Salix babylonica Linn. ( Salicaceae ), 21 Aug 1983, R.-S. Hseu (isotype of G. microsporum , HMAS 57945, frag. in BR!).

Remarks: Ganoderma mexicanum and G. parvulum have sessile to stipitate basidiomes, more frequently stipitate in the latter, with a basal and horizontal stipe. The type specimens of G. subamboinense ( Fig. 4 I–K ) and of G. stipitatum ( Fig. 8 A–E ), overall, have the same basidiome habit. The two specimens of G. parvulum from the rainforest of French Guiana also were morphologically very homogeneous, stipitate, with a basal and horizontal stipe. In the Greater Antilles (Cuba), G. parvulum was found mostly in anthropic or urban environment and had sessile, dimidiate basidiomes.

The context of both G. mexicanum and G. parvulum was light-colored, usually very pale toward the crust and darker just above the tubes, with none to several brown resinous incrustations or resinous bands variably stretching through the context from the base to the margin. The context in G. parvulum sometimes showed yellow, scattered spots and a thin yellow line just below the crust. Both species have chlamydospores in their context and in pure culture on artificial media. There are not many morphological characters to differentiate them except for the ornamentation of their chlamydospores. However, chlamydospores are sometimes very scarce and difficult to observe in the basidiome. Nonetheless, they are always present, and frequent, in pure culture on artificial media.

The basidiospores were, on average, marginally wider in G. mexicanum in comparison to those of G. parvulum , viz. on average 8.6 × 6.4 µm or 9.0 × 6.0 µm, respectively. The cuticular cells were cylindrical to claviform, occasionally with 1-2 short lateral branches, strongly amyloid, usually smooth or with a fine apical granulation, which was more consistently present in G. parvulum . The cuticular cells also were marginally longer in G. parvulum (up to 100 µm long) compared to those of G. mexicanum (up to 65 µm long).

The distribution ranges and ecologies of both species are still little known. Ganoderma parvulum , as here interpreted, had been observed from the Brazilian Amazon, Colombia, and French Guiana in South America, Costa Rica and Nicaragua in Mesoamerica, and up to Cuba in the Caribbean. Loyd et al. (2017, 2018) reported G. cf. weberianum from the subtropical southern Florida (USA) on the basis of two specimens (UMNFL 32 and UMNFL 100), which DNA sequences, nevertheless, were deposited in GenBank under G. subamboinense var. laevisporum . Loyd et al. (2018) described striated chlamydospores in the context of these specimens, which points toward G. parvulum . Our multilocus phylogenetic inferences showed that these Florida specimens nested within the G. parvulum clade ( Fig. 1 ). However, there was incongruence between the topology resulting from the multilocus-based phylogenies and the ITS-based inferences ( Fig. 2 ) regarding the position of UMNFL 100. The ITS sequences of this showed a change in three nucleotide positions, that could represent a misreading of the sequencer. Notwithstanding, these reports extend the distribution range of G. parvulum northerly to the subtropical, south–eastern USA. This ample distribution would imply a broad ecological range, but also could encompass a hidden diversity.

In French Guiana, G. parvulum has been observed at the Nouragues Nature Reserve (~ 4°04′18″N, 52°43′57″W), a spot of primary, very humid (3000 mm of rain / year), tropical rainforest characteristic of the Guianas shield, which belongs to the larger Amazonian rain forest phytochorion. Locally, this species was uncommon; three basidiomes only were observed during six, two- to three-weeks long surveys of polypores. These three specimens were found emerging from dead, fallen trunks. In French Guiana, it has been observed also once in an anthropic, semi-urban environment (culture BRFM 1043, voucher specimen and data on the substrate and host unavailable). The type specimen of G. parvulum , originating from Brazil, was also, most likely, collected in the same phytochorion. In Cuba, Greater Antilles, the species has been observed mostly in anthropic, urban or semi-urban environments (cf. list of specimens examined).

Ganoderma mexicanum , as here interpreted, has been observed from Argentina, Brazil, Martinique (Lesser Antilles), and Mexico. In Mexico, the species is known from a rather restricted area of the Morelos State, which is the type locality of G. mexicanum and G. sessiliforme , and of a third additional specimen collected in secondary tropical forest with Quercus sp. ( Torres-Torres et al. 2015). Raymundo et al. (2013) and López-Peña et al. (2016) also reported G. sessiliforme from xerophylic vegetation with Quercus sp. in Sonora, but the voucher specimens were not available for confirmation. In Martinique, the species was found in mesophylic to distinctly xerophylic forests, which could represent, locally, its preferential habitat. Several collections came from The Caravelle Peninsula, which is characterized by a seasonally dry season.

Figures

Figure 1. Phylogeny of the Ganoderma weberianum - resinaceum complex based on concatenated ITS, rpb 2, and tef 1 - α sequence data obtained by Maximum Likelihood (ML). Bayesian posterior probability (PP) above 0.85 and bootstrap values (BS) from ML above 75 % are shown (PP / BS).

Figure 2. Phylogeny of the Ganoderma weberianum complex from the Neotropics based on rDNA ITS sequence data obtained by Maximum Likelihood (ML). Bayesian posterior probability (PP) above 0.85 and bootstrap values (BS) from ML above 75 % are shown (PP / BS).

Figure 4. Morphological features and microscopic structures of Ganoderma parvulum A-H MUCL 53123 A pilear surface B cuticular cells C-D basidiospores with free to subfree pillars E-H chlamydospores ornamented with free to partially anastomosed ridges E-F from context G-H from culture I-K E. Ule 2748 (as G. subamboinense, holotype) I upper surface of basidiomata, copyright: Naturhistoriska riksmuseet, Stockholm J cuticular cells K chlamydospores ornamented with partially anastomosed ridges, from context, in KOH. Scale bars: 1 cm (A); 5 μm (B).

Figure 8. Morphological features and microscopic structures of type specimens of Ganoderma A-E Ganoderma stipitatum (NY 985678, holotype) A basidiomata B-C context B brown stripes of resinous deposits C numerous bodies of the resin-like deposits D-E chlamydospore, ornamented with partially anastomosed ridges, from context F-I Ganoderma perzonatum (NY 985702, holotype), F basidiomata, copyright: NY Botanical Garden G cuticular cells, cylindrical, with incrustations H-I chlamydospore with fine longitudinal ridges, from context. Scale bar: 1 cm (A-C).