Research Article |
Corresponding author: Tai-Hui Li ( mycolab@263.net ) Academic editor: María P. Martín
© 2020 Chao-Qun Wang, Tai-Hui Li, Ming Zhang, Xiao-Lan He, Wei-Qiang Qin, Tie-Zhi Liu, Nian-Kai Zeng, Xiang-Hua Wang, Jian-Wei Liu, Tie-Zheng Wei, Jiang Xu, Yue-Qiu Li, Ya-Heng Shen.
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Citation:
Wang C-Q, Li T-H, Zhang M, He X-L, Qin W-Q, Liu T-Z, Zeng N-K, Wang X-H, Liu J-W, Wei T-Z, Xu J, Li Y-Q, Shen Y-H (2020) Hygrophorus subsection Hygrophorus (Hygrophoraceae, Agaricales) in China. MycoKeys 68: 49-73. https://doi.org/10.3897/mycokeys.68.53264
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Hygrophorus subsect. Hygrophorus has been relatively well-studied in Europe and North America, but studies on the taxa in Asia, particularly in China, are still limited. In this study, phylogenetic overviews of genus Hygrophorus, based on the nuclear large subunit (LSU) ribosomal RNA gene and of subsect. Hygrophorus, based on the nuclear ribosomal internal transcribed spacer (ITS) regions were generated. Four new species, i.e. H. brunneodiscus, H. fuscopapillatus, H. glutiniceps and H. griseodiscus are described from southern China; and a rarely reported edible species H. hedrychii is described in detail, based upon the materials from north-eastern China. The main characteristics of the species under subsect. Hygrophorus worldwide are summarised in a table.
East Asia, molecular systematics, taxonomy, waxycap, woodwax
Hygrophorus Fr. (Hygrophoraceae, Agaricales, Basidiomycota) is a cosmopolitan fungal genus, mainly distributed in the northern hemisphere. The characteristics that distinguish the genus are: the ectomycorrhizal habit, robust basidiomata, usually viscid pileus surface, waxy, thick and distant lamellae, divergent lamellar trama and white or hyaline thin-walled basidiospores (
Morphologically, members in subsect. Hygrophorus share the characteristics of glutinous and white or pallid pileus, almost white and sometimes darkening lamellae, glutinous stipe and Cossus-odour, resembling the smell of Cossus cossus (Lepidoptera) (
Phylogenetically, the relationships of subsect. Hygrophorus are still controversial. The ITS-LSU-SSU-RPB2 combined analysis in
During the authors’ study on the diversity of subsect. Hygrophorus in China, five species were discovered. In order to assess their phylogenetic positions, a phylogenetic overview of genus Hygrophorus was conducted, based on all available sequences of the nuclear large subunit (LSU) ribosomal RNA gene from GenBank (
Specimens are deposited in the Mycological Herbarium of Chifeng University (CFSZ), Fungal Herbarium of Hainan Medical University (FHMU), Fungarium of Guangdong Institute of Microbiology (
The total genomic DNA extracted from dry samples using a HiPure Fungus DNA Mini kit (Megen Biotech Co. Ltd., Guangzhou, China) according to the manufacturer’s instructions. Gene regions of the large subunit (LSU) and the internal transcribed spacer (ITS) nuclear ribosomal RNA gene are amplified by Polymerase Chain Reactions with the primers LR5 and LR0R (https://sites.duke.edu/vilgalyslab/rdna_primers_for_fungi/) and ITS1/ITS5 and ITS4 (
Taxa, vouchers, geographic origin and GenBank accession numbers of the newly-generated sequences in this study.
Taxon | Voucher | Geographic origin | ITS | LSU |
---|---|---|---|---|
H. brunneodiscus | GDGM73213 | China: Hunan | MN378318 | MT093623 |
GDGM75489 | China: Hunan | MN378317 | MT093622 | |
GDGM76934 | China: Hunan | MT093605 | MT093621 | |
H. eburneus | GDGM70059 (BHS2011-11) | USA | MT093608 | |
H. fuscopapillatus | GDGM44412 | China: Sichuan | MN378337 | MT093625 |
LJW1858 | China: Yunnan | MT093606 | MT093626 | |
XHW6609 | China: Yunnan | MT093607 | MT093627 | |
H. glutiniceps | FHMU1578 (Zeng2452) | China: Hainan | MN378311 | |
FHMU2013 (Zeng3052) | China: Hainan | MN378312 | MT093614 | |
GDGM42140 | China: Guangdong | MN378310 | MT093619 | |
GDGM42188 | China: Guangdong | MN378313 | MT093618 | |
GDGM42217 | China: Guangdong | MN378309 | MT093617 | |
GDGM45220 | China: Hainan | MN378315 | MT093620 | |
GDGM53153 | China: Jiangxi | MT093603 | MT093615 | |
GDGM53496 | China: Hunan | MN378314 | ||
HMAS273294 | China: Guangdong | MT093604 | ||
H. griseodiscus | SAAS462 | China: Sichuan | MN378338 | MT093624 |
H. hedrychii | CFSZ2559 | China: Inner Mongolia | MT093610 | |
CFSZ2851 | China: Inner Mongolia | MN378306 | MT093628 | |
CFSZ4268 | China: Inner Mongolia | MT093609 | ||
CFSZ10761 | China: Inner Mongolia | MT093611 | ||
CFSZ18159 | China: Inner Mongolia | MN378308 | MT093629 | |
CFSZ18269 | China: Inner Mongolia | MN378307 | MT093630 |
For the LSU dataset, the newly-obtained sequences and all available Hygrophorus sequences longer than 300 bps from GenBank are treated as ingroups and the sequences of Cantharocybe gruberi (A.H. Sm.) H.E. Bigelow & A.H. Sm. are selected as outgroup, based on
For the aligned LSU dataset, 121 sequences with 980 sites were included, amongst them 119 Hygrophorus sequences are placed in the ingroups and two sequences of Cantharocybe gruberi are in the outgroups. In the LSU phylogenetic tree (Fig.
Phylogram showing the interspecific relationships under the genus Hygrophorus inferred from a LSU dataset using IQ-tree. Sequences of Cantharocybe gruberi were selected as outgroups. Bootstrap values greater than 50% are indicated around the branches. For downloaded sequences, specimen names and GenBank accession numbers are presented; for newly-generated sequences, species names and specimen vouchers are listed. Four newly-described species’ sequences are highlighted in colour; sequences with quotation marks are incorrect names.
For the aligned ITS dataset, 88 sequences with 689 sites were included, two sequences of H. arbustivus are treated as the outgroups and 86 sequences of subsect. Hygrophorus are within the ingroups. At least thirteen respectively-supported clades that correspond to different species were recovered in the ITS phylogenetic tree (Fig.
Phylogram of species under subsect. Hygrophorus inferred from an ITS dataset using IQ-tree. Sequences of Hygrophorus arbustivus were selected as outgroups. Bootstrap values greater than 50% are indicated around the branches. For downloaded sequences, specimen names, GenBank accession numbers and locations are presented; for newly-generated sequences, species names, specimen vouchers and locations are listed. Four newly-described species’ sequences are highlighted in colour; sequences with incorrect names are marked with quotation marks.
According to the molecular phylogenetic analyses (Figs
China, Hunan Province, Zhangjiajie City, Zhangjiajie Campus of Jishou University, on the ground of a forest dominated by Quercus fabri and Q. serrata, elev. ca. 220 m, 29°8'24"N, 110°27'42"E, 26 May 2019, W.Q. Qin (GDGM73213, Holotype!), ITS MN378318.
“brunneo-”: brown, “-discus”: pileus disc. The species epithet “brunneodiscus” (Lat.) refers to the brown pileus disc of this new taxon.
Hygrophorus brunneodiscus differs from H. cossus by the smaller pileus (20–50 mm broad), brownish pileus disc, thinner stipe (4–7 mm wide) and the shorter basidia (32–48 µm long); differs from H. fuscopapillatus and H. griseodiscus by the low elevation distribution and brown pileus disc.
Pileus 20–50 mm broad, hemispherical or conical with a slightly involute or slightly revolute margin when young, becoming convex with an expanded margin when mature, whitish to brownish as a whole, brownish-orange, light brown, yellowish-brown (5C4–5, 5D4–5, 5E5–8) at the disc (about one fourth part of the radius from the centre to the margin), becoming paler to greyish-yellow (4B3–4), greyish-white (4B1) or whitish outwards and white at the margin or with a white marginal zone of 1–2 mm wide, viscid, covered with a glutinous layer of transparent materials when wet. Lamellae short decurrent to decurrent, white, waxy, with 36–40 complete lamellae and 1–3 lamellulae between two complete lamellae; lamella edge concolorous, entire. Stipe 40–90 × 4–7 mm, cylindrical, hollow, nearly equal to slightly thinner at apex and tapering towards the base; pale yellow to greyish-yellow (4A3, 4B3), white to yellowish-white (4A2) at apex, sometimes white at base; sticky, covered with a layer of transparent materials when wet, easily-sticking debris on the slime layer, usually fibrillose or with scattered white fibrillose dots at apex. Context thin, white to light brown, with slight fishy odour.
Basidiospores (6.5)7–9(9.5) × 4–5.5(6) μm [mean length = 7.6 µm, mean width = 4.6 µm], Q = (1.3)1.4–2(2.1), Qm = 1.68, ellipsoid to oblong, smooth. Basidia 32–48 × 6–8.5 µm, Q = 4.1–6.6, Qm = 5.3, clavate, thin-walled, 4-spored, with sterigmata 5.5–7(9) µm long. Pileipellis an ixotrichoderm, composed of septate cylindrical hyphae, covered with a gelatinous layer; hyphae thin-walled, 2.5–5 μm wide, slightly yellowish and glutinous in KOH. Hymenophoral trama divergent, composed of septate, thin-walled and cylindrical hyphae; hyphal cells 45–70 × 6–10 μm, hyaline. Clamp connections present.
Solitary to scattered, on the ground of subtropical broad-leaf forest dominated by Quercus, so far only known from Hunan Province in South Central China.
China, Hunan Province, Zhangjiajie City, Zhangjiajie Campus of Jishou University, 26 October 2018, W.Q. Qin (GDGM75489); ibidem, 30 June 2019, W.Q. Qin (GDGM76934).
Hygrophorus brunneodiscus is characterised by its brown tint on pileus disc, sticky pileus and stipe surface, basidiospores (6.5)7–9(9.5) × 4–5.5(6) μm, basidia 32–48 × 6–8.5 µm and subtropical and low elevation distribution.
Hygrophorus brunneodiscus can be easily recognised within subsect. Hygrophorus for its brownish colour on the pileus disc. Apart from that, H. cossus differs from H. brunneodiscus by having pale ochraceous grey colour at the pileus centre and more slender basidia (48–60 × 7–8.5 μm) (
China, Sichuan Province, Panzhihua City, Yanbian County, Gesala Ecotourism Area, elev. ca. 2900 m, 27°08'10"N, 101°11'33"E, 25 August 2013, M. Zhang & C.Q. Wang (GDGM44412, Holotype!), ITS MN378337.
“fusco-”: dark brown, “-papillatus”: papillate. The species epithet “fuscopalillatus” (Lat.) refers to the dark brown or grey brown papilla on the pileus of the new species.
Differs from H. griseodiscus by the host association with Fagaceae, solitary habit, adnate to subdecurrent lamellae and slightly smaller basidispores measuring (6)7–9.5(10) × (4)4.5–5.5(6) µm. The ITS sequence is 95% similar to H. griseodiscus.
Pileus 20–30 mm broad, convex to hemispherical when young, applanate to plano-concave when mature, with a papilla or small umbo in the centre, white to pale grey (1B1), grey or brownish-grey to olive brown (4E2–3,4F1–3) at papilla, gradually becoming lighter from centre to margin, white to pale grey (1B1) at margin, glutinous when wet; margin even, occasionally split. Lamellae adnate to subdecurrent, white, thick, with 30–36 complete lamellae per pileus and 1–3 lamellulae between two entire lamellae. Stipe 40–60 × 4–5 mm, cylindrical, white to yellowish-grey (4B2), covered by a glutinous layer. Context thin, whitish.
Basidiospores (6)7–9.5(10) × (4)4.5–5.5(6) µm [mean length = 8.2 µm, mean width = 5 µm], Q =1.3–1.9, Qm =1.65, broadly ellipsoid, ellipsoid to oblong, smooth, hyaline. Basidia (32)35–46(48) × (6)6.5–8.5(9) µm, Q = 4.4–6.8, Qm = 5.5, clavate, thin-walled, 4-spored, with sterigmata 5–7.5 µm long. Pileipellis an ixotrichoderm, composed of septate and thin-walled cylindrical hyphae, covered with a gelatinous layer; hyphal cells 3–5 μm broad. Hymenophoral trama divergent, composed of septate, thin-walled and cylindrical hyphae; hyphal elements 13–31.5 μm broad. Clamp connections present.
Solitary, on the ground of Fagaceae-dominated forests, so far only known from Sichuan and Yunnan provinces in Southwest China.
China, Yunnan Province, Yulong County, Jade Dragon Snow Mountain, Lijiang Alpine Botanic Garden, on the ground of Quercus pannosa dominated forest, elev. ca. 3267 m, 27°00'02"N, 100°10'52"E, 31 August 2019, J.W. Liu (LJW1858); Binchuan County, Jizushan, on the ground of Castanopsis and Lithocarpus dominated forest, elev. ca. 2853 m, 25°58'06"N, 100°21'39"E, 18 September 2019, X.H. Wang (XHW6609).
Hygrophorus fuscopapillatus is distinguished by the solitary basidiomes, the brownish-grey to olive brown papilla in the pileus centre, the broadly ellipsoid, ellipsoid to oblong basidiospores measuring (6)7–9.5(10) × (4)4.5–5.5(6) µm.
Amongst the members of subsect. Hygrophours, H. griseodiscus closely resembles H. fuscopapillatus; however, H. griseodiscus differs from H. fuscopapillatus by the host association with Pinaceae, the larger pileus (2–4.5 cm broad), the emarginate lamellae with decurrent tooth, the larger basidispores measuring (7)8–10(10.5) × (4)4.5–6(6.5) µm and the broader basidia (7–11 mm broad). In addition, H. brunneodiscus is distinguished from H. fuscopapillatus by the broader pileus (2–5 cm in diam.) and the brownish pileus disc. Hygrophorus cossus is separated by the larger pileus (3–9 cm in diam.), greyish-white lamellae with a cream yellow tint and a thicker stipe (0.6–2 cm broad) (
China, Guangdong Province, Guangzhou City, Tianluhu Forest Park, on the ground of a forest dominated by Castanopsis fissa, elev. ca. 250 m, 23°13'39"N, 113°25'53"E, 6 September 2012, M. Zhang (GDGM42188, Holotype!), ITS MN378313.
“glutini-”: glutinous, “-ceps”: pileus. The species epithet “glutiniceps” (Lat.) refers to the glutinous surface of pileus.
Pileus 8–40 mm broad, hemispherical to convex, often with an inconspicuous umbo and a usually involute margin when young, broad-convex to depressed with a slightly incurved to rarely uplifting margin when mature, covered with a layer of gelatine-like or transparent gluey materials when wet, white with cream or light yellow to orange tint (4A2–4) at disc, becoming light to yellowish-brown (5E8) with age (especially at margin and in wounded area), usually brownish-orange (5C5) to brown (6E8) when exsiccated. Lamellae broadly adnate or with decurrent tooth when young, short to moderately decurrent when mature, white when young, then changing to ochraceous or even brown (6E8), waxy when wet, with 25–30 complete lamellae reaching to stipe and 1–3 lamellulae between two entire lamellae. Stipe 25–60 × 3–6 mm, equal but often thinner at the base, cylindrical but usually curved, white, occasionally with yellowish tint (2A2), covered with transparent glutinous materials when wet. Context thin, white when young, changing to brown when old.
Basidiospores (5)6–8.5(10) × (3.5)4–5.5(6) µm [mean length = 7.1 µm, mean width = 4.7 µm], Q = (1.2)1.3–1.77(2), Qm = 1.52, ellipsoid to oblong, smooth, hyaline. Basidia 35–47 × 5–8.5 µm, Q values usually more than 5, clavate, thin-walled, 4-spored, with sterigmata up to 7.5 µm long, hyaline. Pileipellis an ixotrichoderm, composed of septate hyphae, usually covered with a gelatinous layer; hyphae thin-walled, 3–5 μm wide, with yellowish gluten in KOH. Stipitipellis an ixotrichoderm, hyphae 3–5 μm wide, similar to those of pileipellis. Hymenophoral trama divergent, composed of septate, thin-walled and cylindrical hyaline in 4–17 μm diam. Clamp connections present.
Gregarious to scattered, on the ground of subtropical broad-leaf forest dominated by Castanopsis, currently only known from subtropical to tropical areas of China.
China, Guangdong Province, Guangzhou City, Tianluhu Forest Park, 6 September 2012, M. Zhang (GDGM42217); ibidem, 6 September 2012, J. Xu (GDGM42140). Hainan Province, Changjiang County, 3 July 2013, M. Zhang (GDGM45220); Baisha County, Yinggeling National Nature Reserve, elev. ca. 600 m, 1 August 2015, N.K. Zeng 2452 (FHMU1578); Ledong County, Yinggeling National Nature Reserve, elev. ca. 650 m, 4 June 2017, N.K. Zeng 3052 (FHMU2013).
Hygrophorus glutiniceps is macro-morphologically characterised by its subtropical-tropical distribution, white and sticky pileus and stipe, darkening lamellae when mature or wounded. The size of basidiospores [(5)6–8.5(10) × (3.5)4–5.5(6) µm] and basidia [35–47 × 5–8.5 µm] can be used to confirm the recognition. The association with Castanopsis fissa is also helpful for its identification.
Hygrophorus glutiniceps can be morphologically distinguished from closely-related species by the following differences. Hygrophorus cossus looks different from H. glutiniceps in the different ectomycorrhizal connection (with Quercus), the temperate distribution, the longer basidiospores [(7–9.5 μm long in
China, Sichuan Province, Jiuzhaigou, elev. ca. 3100 m, 11 September 2012, X.L. He (SAAS462, Holotype!), ITS MN378338.
“griseo-”: grey, “-discus”: pileus. The species epithet “griseodiscus” (Lat.) refers to the grey disc of the pileus.
Hygrophorus griseodiscus is distinguished from H. brunneodiscus by the greyish pileus with a darker grey pileus disc and larger basidiospores measuring (7)8–10(10.5) × (4)4.5–6(6.5) µm.
Pileus 20–45 mm broad, convex, obtusely umbonate at disc, grey to light grey (1C1, 1D1), medium to dark grey or olive grey (1E1, 1F1–4) at disc, white to pale grey (1B1) at margin, glutinous when wet; margin even, slightly involuted to extended. Lamellae emarginate with decurrent tooth or subdecurrent, white, thick, subcrowded, unequal, with 1–3 lamellulae between two entire lamellae. Stipe 40–70 × 4–6 mm, cylindrical, white to pale grey (1B1), covered with transparent glutinous materials when wet. Context slightly thick, white.
Basidiospores (7)8–10(10.5) × (4)4.5–6(6.5) µm [mean length = 9 µm, mean width = 5.2 µm], Q = 1.4–2.1, Qm = 1.74, ellipsoid, oblong to subcylindrical, smooth, hyaline. Basidia 29–56.5 × 7–11 µm, Q = 3.05–6(6.9), Qm = 4.39, clavate to cylindrical, thin-walled, 4-spored, with sterigmata up to 6 µm long. Pileipellis an ixotrichoderm, covered with a gelatinous layer; hyphae thin-walled, 2.5–6 μm wide. Hymenophoral trama divergent, composed of septate, thin-walled and cylindrical hyphae; hyphal cells 5.5–20 μm in width, hyaline. Clamp connections present.
Scattered, on the ground of subalpine coniferous forest dominated by Abies and Picea, often surrounded by mosses, so far only known from Sichuan Province in Southwest China.
Hygrophorus griseodiscus is characterised by its convex and grey pileus with a dark grey to olive grey disc, emarginate to subdecurrent lamellae. The Asian subalpine coniferous habitat may be a helpful character for its identification.
Morphologically, H. brunneodiscus is distinguished from H. griseodiscus by the brownish pileus disc and smaller basidiospores (6.5–9.5 × 4–5 µm). Hygrophorus cossus differs in the greyish-white lamellae with a cream yellow tint and a thicker stipe (6–20 mm wide) (
Pileus 10–50 mm broad when dried, subglobose when young, becoming hemispherical, convex to nearly plane when mature; margin incurved when young, even, expanded to sometimes slightly upturned when mature; surface covered with a thick layer of transparent and sticky materials, white, with pinkish (7A2) to yellowish (4A2) tones or cream colour (1A2) on the disc. Lamellae adnate to short decurrent, white at first, changing to pinkish-white (7A2) or pale yellow (4A3) or cream colour (1A2), waxy, with 1–3 lamellulae between two entire lamellae. Stipe 20–85 × 3–10 mm when dried, cylindrical or nearly so, often thinner at apex, usually slightly enlarged at base, uneven, with white short fibrils at apex, sometimes longitudinally lacerated when mature, covered with a layer of transparent sticky materials, white, changing to orange white (5A2, 6A2) where touched. Context thick, white when young, pale to pinkish-yellow when mature, with Cossus smell.
Basidiospores (6)7–8(9) × (3.5)4–4.5(5) µm, Q = 1.5–2(2.3), Qm = 1.8, ellipsoid to subcylindrical, colourless, thin-walled, smooth. Basidia 30–40 × 6–9 µm, Q = 4.1–5.7, clavate, 4-spored; sterigmata 4–5 µm long; basal clamp connections common. Pileipellis an ixotrichoderm, composed of septate hyphae, covered with a gelatinous layer; hyphae thin-walled, 4–5 μm wide. Stipitipellis a trichoderm; hyphae 7–10 μm wide, light yellowish-brown intracellular pigment presented in a few hyphae when immersed in 5% KOH solution. Hymenophoral trama composed of septate, thin-walled and cylindrical hyaline hyphae, size 58–105 × 3–23 μm. Clamp connections present.
Scattered to gregarious in the north temperate forests dominated by Betula, known from north-eastern China (this study), as well as from Europe where the species was firstly discovered.
China, Inner Mongolia Autonomous Region, Chifeng City, Harqin Banner, Wangyedian village, 30 August 2007, T.Z. Liu (CFSZ2851); ibidem, 8 August 2017, T.Z. Liu, Y.Q. Guang & N. Liu (CFSZ18159); Hexigten Banner, Jingpeng Town, 15 August 2017, T.Z. Liu & G.L. Yu (CFSZ18269).
Macroscopically, Hygrophorus hedrychii is a distinctive waxycap, which is relatively easily recognised in the field by its white pileus disc and lamellae changing to pale ochraceous pink when mature and the host association with birch. Microscopically, the Chinese specimens agree with the descriptions by
In recent years, the phylogenetic framework of Hygrophorus has been reconstructed by
According to the ITS phylogenetic tree in this study, subsect. Hygrophorus is monophyletic. Thus, the concept of subsect. Hygrophorus proposed by
Previously, five species were confirmed as members of subsect. Hygrophorus, including H. cossus, H. discoxanthus, H. eburneus, H. hedrychii and H. scabrellus (
Apart from the four new species from China, proposed in this study (H. brunneodiscus, H. fuscopapillatus, H. glutiniceps and H. griseodiscus), two species with American sequence samples (“H. chrysaspis Métrod” and H. occidentalis A.H. Sm. & Hesler) and two undescribed species, H. sp1 from Europe and H. sp2 from North America, are present as phylogenetic species under subsect. Hygrophorus. Four sequences labelled as “H. chrysaspis” from USA are grouped together. Although the North American samples have not been proved to be conspecific with the European H. chrysaspis (originally described from France) with molecular evidence due to the absence of the French sequence, the USA samples can still present a member of subsect. Hygrophorus; in addition, Hesler and Smith (1963) has also mentioned that the USA H. chrysaspis resembled H. eburneus (the type species of subsect. Hygrophorus). The American species H. occidentalis, originally described from Michigan (USA), is further confirmed as a member of subsect. Hygrophorus in this study (Table
It is worth mentioning that the species diversity within subsect. Hygrophorus may be underestimated for these two main reasons: 1) some species from the well-studied countries may have been left out. For example, H. occidentalis had been listed in the North American monograph (Hesler and Smith 1963), but it was not included in
Species | Pileus size (cm) | Colour of mature pileus | Colour of lamellae | Stipe width (cm) | Spore size (μm) | Host- connection | Reference |
---|---|---|---|---|---|---|---|
H. brunneodiscus | 2–5 | White with brownish-orange to light brown at the disc | White | 0.4–0.7 | 6.5–9.5 × 4–5 | Quercus | This study |
H. cossus | 3–9 | Pale ochraceous grey at the centre of the pileus | Greyish-white with a cream yellow tint | 0.6–2.0 | 7–9 × 4–5 | Quercus |
|
H. discoxanthus | 3–7 | White with rusty-brown margin upon drying | White as young, then rusty brown | 0.5–1.2 | 6.5–9 × 3.5–5.5 | Fagus |
|
H. eburneus | 2–7 | White | Cream-white as young then cream-yellow | 0.4–1.0 | 7.5–10 × 4–5.5 | Fagus |
|
H. fuscopapillatus | 2–3 | White to pale grey at margin, pale grey to olive brown at papilla | White | 0.4–0.5 | (6)7–9.5(10) × (4)4.5–5.5(6) | Fagaceae | This study |
H. glutiniceps | 0.8–4 | White with cream or light yellow to orange tint at disc | White when young, then changing to ochraceous or even brown | 0.3–0.6 | (5)6–8.5(10) × (3.5)4–6 | Castanopsis | This study |
H. griseodiscus | 2–4.5 | Grey to light grey with dark grey at disc | White | 0.4–0.6 | (7)8–10(10.5) × (4)4.5–6(6.5) | Abies or Picea | This study |
H. hedrychii | 3–8 | White with orange-pinkish tint at centre | White with orange-pinkish tint | 0.5–1.0 | 6.5–9 × 3.5–5 | Betula |
|
H. occidentalis | 2–8(10) | “hair brown” to “fuscous”, at times yellowish or smoky at disc | White then tinged cream | 0.3–1(1.5) | 6–8 ×3.5–5 | unclear | Hesler and Smith 1963 |
H. scabrellus | 2.4–2.8 | Off-white with dark green | Off-white to beige | 2.1–2.4 | 6.5 × 3.84 | Quercus |
|
Some Hygrophorus taxa are difficult to be distinguished with the naked eye by the specific differences of macro-morphological characteristics and it will be harder when considering the infraspecific variations; the microscopic features for distinguishing Hygrophorus species are also limited, since they usually lack cystidia and have slight interspecific differences in the size and shape of basidiospores and basidia.
Due to the morphological similarity, misidentifications are common in subsect. Hygrophorus. For example, 15 samples with the same name as “H. eburneus” are included in the analysis (Fig.
It is worthy to mention that, although some samples might have been misidentified, their molecular sequences can still provide some useful information for analysing the relationships amongst the samples or even potentially representing some undescribed taxa and reflecting richer species diversity.
Ecologically, according to the authors’ investigation since 2010, Hygrophorus species are relatively rare in the subtropical to tropical areas of Guangdong and Hainan Provinces in South China. The reports of the Chinese Hygrophorus are mainly concentrated in the temperate regions and in the high-elevation areas of subtropical zone (
With the application of integrative taxonomy, considering the morphology characteristics, molecular data, the symbiotic association of plants etc., it is now easier to distinguish species within subsect. Hygrophorus. Even the study of genus Hygrophorus has entered an era in which a mass of new species have been discovered (
The authors sincerely thank the editors and reviewers for their valuable comments and suggestions. Thanks are given to Dr David Hibbett for giving specimens to the first author. Thanks are given to Dr Yi-Jian Yao and Ms Liu Yang for their help in loaning specimens. Thanks are given to Mr Jun-Yan Xu for identifying plant species. This study is supported by the National Natural Science Foundation of China (Nos. 31800013, 31760004), the GDAS’ Project of Science and Technology Development (No. 2020GDASYL-20200104013), the Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment, China (No. 2019HJ2096001006), the Science and Technology Planning Project of Guangdong Province, China (Nos. 2018B030324001, 2018B020205001) and the Science and Technology Planning Project of Guizhou Province, China (No. Qian Ke He Fu Qi [2019] 4007).