Cryptomarasmius aucubae (Neda) T.S. Jenkinson & Desjardin (2014: 86–94)

Kiyashko, Anna A., Malysheva, Ekaterina F., Antonín, Vladimír, Svetasheva, Tatiana Yu. & Bulakh, Eugenia M., 2014, Fungi of the Russian Far East 2. New species and new records of Marasmius and Cryptomarasmius (Basidiomycota), Phytotaxa 186 (1), pp. 1-28 : 21-24

Cryptomarasmius aucubae (Neda) T.S. Jenkinson & Desjardin (2014: 86–94) ( Fig. 2F , Fig. 9)

Pileus 1–3 mm in diam., initially broadly conical, then hemispherical or convex with slightly depressed centre, sulcate, with slightly undulate margin, not hygrophanous, smooth or slightly pruinose, dull, from whitish or pale yellow (4A3) at margin to brownish yellow (5C8) or ochraceous brown at centre. Flesh thin, concolorous. Lamellae adnate, very few, ventricose, sometimes poorly developed, whitish or pale cream with concolorous edge. Stipe 3–15 × 0.2–0.4 mm, central, filiform, insititious, minutely pruinose and whitish in upper part, smooth below, reddish brown at base (8D4–E4). Odour and taste indistinct.

Basidiospores 6.0–8.9 × 2.5–4.1 µm, χ m = 7.5±0.8 × 3.2±0.5 µm, Q = (1.9)2.1–2.8, Q m = 2.3±0.2, n = 7–14, s = 4; ellipsoid to ellipsoid-fusoid or sublacrimoid, smooth, thin-walled, hyaline, inamyloid, acyanophilous. Basidia 12.5–23.0 × 5.5–7.5 µm, 4-spored, clavate or subcylindrical. Basidioles at first tapered, sometimes with papilla, then clavate. Cheilocystidia of two types: a) lageniform, fusiform to almost utriform, rostrate or subcylindrical, smooth or with a few projections in the middle part, thin-walled, 16–27 × 4.5–10 μm; b) slightly thick-walled Rotalis - type broom cells, main body broadly clavate or pyriform, 10–20 × 9.5–13 μm, projections up to 1.6 μm long. Pleurocystidia 17–29 × 4–10.5 μm, scattered, similar to the first type of cheilocystidia or more cylindrical. Pileipellis a hymeniderm composed of 11–24 × 5.5–18 μm large, broadly clavate, pyriform or subglobose thick-walled Rotalis - type broom cells, often darkly pigmented in KOH; diverticula numerous, up to 2 μm in length. Pileocystidia 14–19 × 4.5–5.5 μm, subcylindrical, lageniform, fusiform, rostrate, smooth or with a few projections in the middle part, thin- or slightly thick-walled, abundant to very sparse. Stipitipellis a cutis made up of cylindrical, thick-walled, diverticulate hyphae up to 7 μm in diam. Caulocystidia usually present but varying considerably in number from sporadic to numerous, lageniform to subcylindrical, 5.2–17.5 × 2.0–4.5 μm. Clamp connections present in all tissues .

FIGURE. Microscopic features of Cryptomarasmius aucubae (LE 289499, 295981). A. Spores. B. Basidia. C. Basidioles. D. Cheilocystidia of type a. E. Cheilocystidia of type b. F. Pleurocystidia. G. Pileocystidia. H. Pileipellis cells. I. Hyphae of stipitipellis with developed and underdeveloped caulocystidia.―Scale bar = 10 μm.

Habitat and distribution: Gregarious on fallen leaves of Phellodendron amurense or other broadleaved trees in deciduous or mixed forest. In the Russian Federation, it is today only known from the Manchurian and Middle Sikhote- Alin mountain systems. Originally described from Japan ( Neda & Doi 1998).

Specimens examined: RUSSIAN FEDERATION. Primorsky Territory: UNR, vicinity of Peishula field reserve station, floodplain of Koryavaya Pad’ river, mixed forest ( Pinus koraiensis , Phellodendron amurense , Chosenia arbutifolia , etc.), on fallen leaves of Phellodendron amurense , 15 Aug. 2011, T. Svetasheva (LE 289499!); ibid., broadleaved lowland forest with Chosenia arbutifolia , Alnus hirsuta , Juglans mandshurica , etc., on fallen leaves, 16 Aug. 2011, N. Psurtseva (LE 295981!); SANR, vicinity of Kabany field reserve station, floodplain of Kabany brook, mixed forest, on leaf litter, 24 Aug. 2011, E. Malysheva (LE 289500!); ibid., vicinity of Yasnaya field reserve station, coniferous-broadleaved forest, on fallen leaves in litter, 22 Aug. 2013, A. Fedosova (LE 295994!); ibid., coniferousbroadleaved forest, on fallen leaves, 21 Aug. 2013, O. Morozova (LE 295992!); ibid., vicinity of Ust’-Shanduy field reserve station, coniferous-broadleaved forest, on fallen leaves, 21 Aug. 2013, E. Pimenova (LE 295993!)― JAPAN. Tokyo, Shibuya, Yoyogi, Meijijingu Shurine (TNS-F-45954!).

Observations: C. aucubae is distinguished by tiny basidiocarps, a light yellow-brown or orange pileus, mediumsized basidiospores, cheilocystidia of two types, rare or absent caulocystidia, and the presence of both broom cells and lageniform elements in the pileipellis.

C. aucubae was originally described from Japan as Marasmius aucubae Neda in the sect. Hygrometrici ( Neda & Doi 1998). According to a recent molecular study, this section is segregated as a new genus, Cryptomarasmius T.S. Jenkinson & Desjardin , belonging to the family Physalacriaceae ( Jenkinson et al. 2014) . Fourteen species of sect. Hygrometrici were formally combined in Cryptomarasmius . Among them are Cryptomarasmius crescentiae (Murrill) T.S. Jenkinson & Desjardin , C. corbariensis (Roum.) T.S. Jenkinson & Desjardin and C. minutus (Peck) T.S. Jenkinson & Desjardin , which are similar to C. aucubae in both macro- and micromorphological features ( Singer 1976, Antonín & Noordeloos 2010).

According to the type description ( Neda & Doi 1998), C. aucubae differs from the American species C. crescentiae only in basidiocarp size and substrate, whereas macro- and microscopic features of these two species largely correspond. However, the morphological comparison of the studied Russian and Japanese specimens with the description of the C. crescentiae holotype from Cuba ( Singer 1976) has allowed us to note several characters which can be used to distinguish the latter from C. aucubae : essentially narrower basidiospores (6.5 × 2.7 μm), sparse cheilocystidia of the broom-cell type and lack of lageniform elements in the pileipellis. At present, there are no sequences of C. crescentiae . Therefore, it is impossible to prove the distinctiveness of these species by means of molecular methods.

Another close species, C. corbariensis , differs morphologically in having a darker basidiocarp colour, larger basidiospores (8.5–10 × 3.5–5 µm) and the absence of caulocystidia ( Antonín & Noordeloos 2010). Also this is a distinct species based on both ITS and nrLSU data (Figs. 10, 11).

The morphological differences between the European species C. minutus and C. aucubae are very subtle. C. minutus has slightly larger basidiospores (6–9.5 × 2.7–4(5) µm) than C. aucubae ; the pleurocystidia in M. minutus are almost lecythiform ( Antonín & Noordeloos 2010) while commonly more cylindrical without a distinct capitate apex in M. aucubae . In other characters, the two taxa are very similar. Based on molecular data, C. aucubae is a taxon clearly separated from C. minutus (Fig. 11).

“ Marasmius junipericola ” (ad int.), mentioned by Antonín et al. (2012b) but not sequenced, has conspicuously wider basidiospores (8.0–9.5 × 4.5–5.0 µm, Q m = 1.8) and a mostly smooth stipitipellis hyphae. Cryptomarasmius micraster (Petch) T.S. Jenkinson & Desjardin is characterized by appreciably larger basidiospores (9–11(12) × (3.5)4– 5(5.5) μm) ( Antonín et al. 2012b).

Our observations suggest that C. aucubae is rather a morphologically variable taxon. In both ITS and nrLSU phylogenetic trees (Figs 10, 11), our collections of C. aucubae and the Japanese as well as the Korean specimens, identified initially as Marasmius crescentiae ( Antonín et al. 2012b) , formed one well-supported clade with almost 100 % similarity of sequences (recovered from pairwise comparison). However, their morphological features show noticeable variability concerning the spore size, the shape of the cheilo- and pleurocystidia, the proportions of cheilocystidia of «a» and «b» types, and the presence of pileo- and caulocystidia. It should be noticed that Antonín et al. (2012b) pointed out the absence of caulocystidia in the description of the Korean material of C. aucubae . However it was found that some hyphae of the stipitipellis of most Russian specimens have unusually large projections (up to 17 μm long) resembling underdeveloped caulocystidia as well as scattered true caulocystidia (Fig. 9I). Therefore the occurrence of caulocystidia is a rather unstable feature in this species and the presence or absence of caulocystidia can be considered a dubious taxonomical character.

Therefore, further investigations into the morphology of and phylogenetic relationships among C. crescentiae , C. aucubae , C. corbariensis and C. minutus are needed.

FIGURE 0. Best tree from the ML analyses of the nrITS data set for Cryptomarasmius aucubae and related species. Support values (ML bootstrap percentages/MP bootstrap percentages/Bayesian posterior probabilities) are given on or below the branches. Bayesian posterior probabilities calculated for 1,000,000 generations. All tips are labelled with taxon name, GenBank accession number and country of the specimen’s origin.

Figures

FIGURE 2. Mature basidiocarps. A. Marasmius macrocystidiosus sp. nov. (LE 295996). B–C. Marasmius insolitus sp. nov. (LE 289497). D. Marasmius cohaerens var. mandshuricus var. nov. (LE 295987). E. Marasmius cf. ochroleucus (LE 295978). F. Cryptomarasmius aucubae (LE 289499). G. Marasmius occultatiformis (LE 295976). Scale bar = 1 cm.