Research Article
Print
Research Article
Taxonomic studies of bluish Mycena (Mycenaceae, Agaricales) with two new species from northern China
expand article infoQin Na, Zewei Liu, Hui Zeng§|, Binrong Ke§|, Zhizhong Song, Xianhao Cheng, Yupeng Ge
‡ Ludong University, Yantai, China
§ Institute of Edible Mushroom, Fujian Academy of Agricultural Sciences, Fuzhou, China
| National and Local Joint Engineering Research Center for Breeding and Cultivation of Featured Edible Mushroom, Fuzhou, China
Open Access

Abstract

Bluish Mycena are rare, but constitute a taxonomically complex group. A total of eight bluish species in four sections have previously been reported from North America, Europe, Oceania and Asia. Two species with a blue pileus, collected in China during our taxonomic study of Mycena s.l., are described here as new to science: Mycena caeruleogrisea sp. nov. and M. caeruleomarginata sp. nov. Detailed descriptions, line drawings and a morphological comparison with closely-related species, especially herbarium specimens of M. subcaerulea from the USA, are provided. The results of Bayesian Inference and Maximum Likelihood phylogenetic analyses of a dataset of 96 nuclear rDNA ITS and 20 nLSU sequences of 43 Mycena species are also presented. The morphological data and the results of the phylogenetic analyses support the introduction of M. caeruleogrisea and M. caeruleomarginata as new species. A taxonomic key to bluish Mycena species of sections Amictae, Cyanocephalae, Sacchariferae and Viscipelles is provided.

Keywords

Mycenoid fungi, phylogeny, taxonomy, two new taxa

Introduction

Mycena (Pers.) Roussel, with almost 600 species distributed worldwide, is one of the largest genera in Agaricales (He et al. 2019). Maas Geesteranus (1980, 1992a, 1992b) proposed an infrageneric classification of Mycena, based on a combination of macroscopic and microscopic features. In this classification, the species are defined macroscopically based on basidiomata colour (pileus, stipe and lamellae face and edge). Within Mycena, species of sect. Adonideae (Fr.) Quél., now treated as Atheniella Redhead, Moncalvo, Vilgalys, Desjardin & B.A. Perry, sect. Aciculae Kühner ex Singer and sect. Oregonenses Maas Geest., are well characterised by their bright colours, such as pink, red, white or yellow (Maas Geesteranus 1980). Members of sect. Calodontes (Fr. ex Berk.) Quél. are prominently violet and dark colours can also be observed in sect. Rubromarginatae Singer ex Maas Geest. (Robich 2003, 2016; Aravindakshan and Manimohan 2015; Aronsen and Læssøe 2016). In addition, the microscopic characters are also considered to be very important in the infrageneric division of Mycena, containing basidiospores, cheilocystidia, pileipellis and stipitipellis (Maas Geesteranus 1992a, 1992b; Robich 2003, 2016; Aravindakshan and Manimohan 2015; Aronsen and Læssøe 2016). No current published framework exists for the genus as a whole, however and the morphologically based classification of Maas Geesteranus (1992a, 1992b) has not been fully tested and validated. Some recent studies indicate that several Mycena sections, for example, sects. Amparoina T. Bau & Q. Na, Calodontes (Fr. Ex Berk.) Quél and Sacchariferae Kühner ex Singer, are apparently monophyletic, whereas others are not (Harder et al. 2010; Na and Bau 2019b). Several taxa, traditionally assigned to Mycena, such as the Atheniella group, have been removed from the genus and others may need to be incorporated into genera, such as Cruentomycena R.H. Petersen, Kovalenko & O.V. Morozova, Favolaschia (Pat.) Pat., Hemimycena Singer, Panellus P. Karst., Resinomycena Redhead & Singer and Roridomyces Rexer (Redhead and Singer 1981; Rexer 1994; Antonín and Noordeloos 2004; Petersen et al. 2008; Redhead et al. 2012).

Eight bluish Mycena in four sections have been documented so far. Amongst these species, five have been reported from the Northern Hemisphere: M. subcaerulea Sacc. in North America, M. amicta (Fries) Quél. and M. cyanorhiza Quél. in Europe, M. indigotica Wei & Kirschner and M. lazulina Har. Takah., Taneyama and Terashima & Oba in Asia (Smith 1947; Maas Geesteranus 1980, 1992a, 1992b; Perry 2002; Robich 2003; Aronsen and Læssøe 2016; Terashima et al. 2016; Wei and Kirschner 2019; Perry et al. 2020). A bluish tint is often present on the pileus or stipe of these five species, four of them being classified into three sections: sect. Amictae Alexander H. Smith ex Maas Geesteranus,sect. Sacchariferae and sect. Viscipelles Kühner, but M. indigotica has tubes confused with members of Favolaschia (Pat.) Pat. and not assigned any section (Smith 1947; Maas Geesteranus 1980, 1992a, 1992b; Perry 2002; Robich 2003; Aronsen and Læssøe 2016; Terashima et al. 2016; Wei and Kirschner 2019; Perry et al. 2020). The three known bluish Mycena species from the Southern Hemisphere are M. caesiocana Singer, M. cyanosyringea Singer and M. interrupta (Berkeley) Sacc. (Singer 1969; Singer and Gomez 1982; Grgurinovic 2003). These species are distributed in Oceania and South America, Australia, Chile, Costa Rica, New Caledonia and New Zealand, where they usually grow on dead woods, decaying logs or tree stumps in deciduous forests of trees, such as Eucalyptus robusta Smith and Persea lingue (Ruiz & Pav.) Nees and develop basidiomata under high temperatures (Singer 1969; Singer and Gomez 1982; Grgurinovic 2003). The three allied species can be easily recognised: M. caesiocana and M. cyanosyringea are well characterised by the presence of a storm-grey pileus and extremely small basidiomata (pileus diameter and stipe length all less than 3 mm) and M. interrupta has a blue stipe base (Singer 1969; Singer and Gomez 1982; Grgurinovic 2003). In addition, M. cyanocephala Singer described from Chile, is considered to be synonymous with M. interrupta (Grgurinovic 2003). Although M. cyanorhiza, from the Northern Hemisphere, also has a blue stipe base similar to M. interrupta, but differs in pale brown to pale grey pileus and smaller basidiospores and cheilocystidia (Robich 2003; Aronsen and Læssøe 2016; Perry et al. 2020).

To date, fewer than 100 species of Mycena have been documented from China; amongst them, 14 new species have been described in recent years (He and Fang 1994; Guo et al. 1999; Shih et al. 2014; Li et al. 2015; Na and Bau 2018, 2019a, 2019b; Liu et al. 2021). During our investigations of mycenoid fungi in north-western China, we discovered two putative new taxa possessing a blue pileus with a greyish or brownish tint and a gelatinous pileipellis, clearly distinct from other species of Mycena, in the Liupan and Changbai Mountains. The results of our morphological observations and phylogenetic analyses support the introduction of these two new taxa.

Materials and methods

Morphology

Macromorphological observations were made on fresh specimens in the field and from photographs, with colour terms and notation following Kornerup and Wanscher (1978). Specimen pieces were mounted in 5% potassium hydroxide (KOH) and stained with Congo red when necessary. The prepared specimens were observed under a Lab A1 microscope (Carl Zeiss AG, Jena, Germany) and photographed and recorded using the supplied ZEN 2.3 (blue edition) software (Carl Zeiss AG). Melzer’s Reagent was used to test whether spores and tissues were amyloid and dextrinoid (Horak 2005). The dimensions of basidiospores were recorded according to Ge et al. (2021), Liu et al. (2021) and Na et al. (2021, 2022). The examined collections have been deposited in the Fungarium of the Fujian Academy of Agricultural Sciences (FFAAS), China. In the subsequent taxonomic description, author abbreviations follow Index Fungorum (http://www.indexfungorum.org).

Phylogenetic analysis

Genomic DNAs of the putative new species were extracted from dried materials using a NuClean PlantGen DNA kit (Kangwei Century Biotechnology, Beijing, China). The internal transcribed spacer (ITS) region and the nuclear large subunit (nLSU) of nuclear ribosomal DNA were amplified using the PCR cycling protocol detailed in Ge et al. (2021) with primers ITS1/ITS4 and LR0R/LR7, respectively (White et al. 1990; Hopple and Vilgalys 1999). In addition, no sequence information has been published for M. subcaerulea and only a few ITS sequences of M. cyanorhiza and M. amicta, which were found to be phylogenetically closely related to the new species, are available in GenBank. For three M. subcaerulea specimens, we tried to obtain our target sequences by using next-generation sequencing (NGS) technology and whole-genome sequencing of the specimens was performed on the Illumina sequencing platform (HiSeq PE150) with standard procedures. The 150 bp paired-end libraries were prepared to generate approximately 3G raw data. ITS (GenBank accessions KT900146, NR_154169) and nLSU (GenBank accessions MK629349 and NG_070530) were randomly selected for using as custom seed and custom label databases according to the instructions (https://github.com/Kinggerm/GetOrganelle/wiki/FAQ: How to assemble custom loci?) of the software programme GetOrganelle (Jin et al. 2020). Finally, two ITS sequences (GenBank accessions OL711671 and OL711672) and three nLSU sequences (OL711666, OL711667 and OL711668) were captured from next-generation sequencing data of three specimens (TENN-F-051121, TENN-F-057919 and CUP-A-015335) of M. subcaerulea and used for subsequent analysis. Thirteen sequences (six ITS and seven nLSU) newly generated in this study were deposited in GenBank. Additionally, a total of 103 ITS and nLSU sequences (including Xeromphalina campanella [Batsch] Kühner & Maire, which is often chosen as an outgroup for Mycena) were retrieved from GenBank for use in the phylogenetic analysis. Information on all analysed sequences (116) is given in Table 1. Generated sequences and those retrieved from GenBank were aligned and manually checked using BioEdit 7.0.4.1 and Clustal X 1.81 (Thompson et al. 1997; Hall 1999), with gaps in the alignment treated as missing data. The ITS and nLSU datasets were aligned separately. After estimating the optimal model of nucleotide evolution for the two partitions independently using Modeltest 3.7 (Posada and Crandall 1998), the two datasets were concatenated. The combined aligned dataset, which was deposited in TreeBase (submission ID 29069; study accession URL: http://purl.org/phylo/treebase/phylows/study/TB2:S29069), was subjected to Bayesian Inference (BI) and Maximum Likelihood (ML) phylogenetic analyses. The BI analysis was performed in MrBayes 3.2.6 (Ronquist and Huelsenbeck 2003). For the BI analysis, Markov Chain Monte Carlo chains were run for two million generations, with sampling carried out every 100th generation until the critical value for the topological convergence diagnostic was less than 0.01 (Ronquist and Huelsenbeck 2003). The ML analysis, with a rapid bootstrapping algorithm involving 1,000 replicates, was performed in raxmlGUI 1.5b1 (Stamatakis et al. 2005).

Table 1.

Specimens along with GenBank accession numbers used in the phylogenetic analysis. Sequences newly generated in this study are indicated in bold.

No. Species Voucher Origin ITS ID LSU ID References
1. Mycena abramsii 231a Venice JF908400 Unpublished
2. M. abramsii HMJAU 43282 China MH396626 MK629348 Unpublished
3. M. abramsii HMJAU 43468 China MH396627 Unpublished
4. M. abramsii KA12-0434 Korea KR673481 Kim et al. (2015)
5. M. adscendens Aronsen120803 Norway KT900140 Aronsen and Larsson (2015)
6. M. adscendens Orstadius329-05 Norway KT900141 Aronsen and Larsson (2015)
7. M. adscendens Aronsen061119 Norway KT900142 Aronsen and Larsson (2015)
8. M. adscendens Aronsen120826 Norway KT900143 Aronsen and Larsson (2015)
9. M. albiceps MGW1504 USA KY744173 MF797661 Unpublished
10. M. albiceps SAT1518708 USA KY777372 MF797659 Unpublished
11. M. alnetorum CM14-RG2 USA KU295552 Unpublished
12. M. amicta 189f Italy JF908394 Osmundson et al. (2013)
13. M. amicta 4745-HRL 1312 Canada KJ705188 Unpublished
14. M. amicta CBS 352.50 France MH856655 Vu et al. (2019)
15. M. amicta CBS 254.53 France MH857183 Vu et al. (2019)
16. M. amicta CBS 257.53 France MH857184 MH868722 Vu et al. (2019)
17. M. amicta H6036851 Finland MW540687 Unpublished
18. M. arcangeliana 252b Italy JF908401 Osmundson et al. (2013)
19. M. arcangeliana 252f Italy JF908402 Osmundson et al. (2013)
20. M. caeruleogrisea FFAAS 0001 Holotype China MW051896 OL711662 This study
21. M. caeruleogrisea FFAAS 0002 China MW051897 OL711663 This study
22. M. caeruleomarginata FFAAS 0357 Holotype China OL711669 OL711664 This study
23. M. caeruleomarginata FFAAS 0358 China OL711670 OL711665 This study
24. M. chlorophos ACL257 Malaysia KJ206983 Chew et al. (2015)
25. M. chlorophos ACL271 Malaysia KJ206986 Chew et al. (2015)
26. M. cinerella Aronsen051014 Norway KT900146 Aronsen and Larsson (2015)
27. M. cinerella 173 Russia MF926553 Malysheva et al. (2017)
28. M. citrinomarginata 317h Italy JF908416 Osmundson et al. (2013)
29. M. citrinomarginata AD4TN Tunisia KU973883 Unpublished
30. M. clavicularis 615i Italy JF908466 Osmundson et al. (2013)
31. M. clavicularis 615b Italy JF908467 Osmundson et al. (2013)
32. M. cyanorhiza 120b Italy JF908385 Osmundson et al. (2013)
33. M. deeptha DM334g India JX481737 Aravindakshan et al. (2012)
34. M. diosma KA13-1230 Korea KR673698 Kim et al. (2015)
35. M. diosma 320f Italy JF908417 Osmundson et al. (2013)
36. M. entolomoides HMJAU 43048 China MG654736 Na and Bau (2018)
37. M. entolomoides HMJAU 43052 China MG654737 MK722348 Na and Bau (2018)
38. M. entolomoides HMJAU 43126 China MG654738 MK722349 Na and Bau (2018)
39. M. filopes 3782 Canada KJ705175 Unpublished
40. M. filopes KA12-1699 Korea KR673631 Kim et al. (2015)
41. M. filopes 287f Italy JF908410 Osmundson et al. (2013)
42. M. galericulata DM136-40516 USA OM212953 Unpublished
43. M. galericulata LXL71 China MZ669083 Unpublished
44. M. galericulata F26441 USA MZ317346 Unpublished
45. M. galericulata EP.19-A1625 Greece MT458520 Unpublished
46. M. galericulata 50 Norway MW576935 Unpublished
47. M. galericulata TFB14649 USA MN088382 Unpublished
48. M. illuminans ACL161 Malaysia KJ206975 Chew et al. (2015)
49. M. illuminans ACL175 Malaysia KJ206976 Chew et al. (2015)
50. M. illuminans ACL212 Malaysia KJ206980 Chew et al. (2015)
51. M. leaiana 1028 Italy JF908376 Osmundson et al. (2013)
52. M. leaiana CNH03 (TENN) USA MF686520 Unpublished
53. M. meliigens 39 Italy JF908423 Osmundson et al. (2013)
54. M. meliigena 39d Italy JF908429 Osmundson et al. (2013)
55. M. metata 313b Italy JF908412 Osmundson et al. (2013)
56. M. olivaceomarginata GG436-86 Svalbard GU234119 Geml et al. (2015)
57. M. olivaceomarginata CBS 228.47 France MH856228 MH867756 Vu et al. (2019)
58. M. olivaceomarginata CBS 229.47 France MH856229 MH867757 Vu et al. (2019)
59. M. olivaceomarginata HK47-15 Norway MT153141 Thoen et al. (2020)
60. M. pachyderma 979a Italy JF908491 Osmundson et al. (2013)
61. M. pearsoniana FCME25817 USA JN182198 Harder et al. (2012)
62. M. pearsoniana TENN61544 USA JN182199 Harder et al. (2012)
63. M. pearsoniana TENN61384 USA JN182200 Harder et al. (2012)
64. M. pelianthina CBH164 Denmark FN394548 Unpublished
65. M. pelianthina 108b Italy JF908379 Osmundson et al. (2013)
66. M. pelianthina 108f Italy JF908380 Osmundson et al. (2013)
67. M. plumbea JN198391 China JN198391 Wu et al. (2013)
68. M. plumbea 420526MF0010 China MG719769 Unpublished
69. M. polygramma 439b Italy JF908433 Osmundson et al. (2013)
70. M. polygramma 439f Italy JF908434 Osmundson et al. (2013)
71. M. pura TENN65043 USA JN182202 Harder et al. (2012)
72. M. pura f. alba CBH410 USA FN394595 Unpublished
73. M. purpureofusca SL09-06 Canada HQ604766 Unpublished
74. M. purpureofusca G. Alfredsen Norway JQ358809 Unpublished
75. M. rosea 938a Italy JF908488 Osmundson et al. (2013)
76. M. rosea Champ-21 Spain KX449424 Pérez-Izquierdo et al. (2017)
77. M. rubromarginata 407q Italy JF908430 Osmundson et al. (2013)
78. M. rubromarginata TL-12780 USA KX513845 KX513849 Perry and Desjardin (2016)
79. M. seminau ACL136 Malaysia KF537250 KJ206952 Chew et al. (2015)
80. M. seminau ACL308 Malaysia KF537252 KJ206964 Chew et al. (2015)
81. M. seynesii 71l Italy JF908469 Osmundson et al. (2013)
82. M. seynesii 71h Italy JF908470 Osmundson et al. (2013)
83. M. silvae-nigrae 515 Italy JF908452 Osmundson et al. (2013)
84. M. silvae-nigrae CC 13-12 USA KF359604 Baird et al. (2014)
85. M. stylobates 455 Italy JF908439 Osmundson et al. (2013)
86. M. subcaerul ea TENN-F-051121 USA OL711671 OL711666 This study
87. M. subcaerulea TENN-F-057919 USA OL711672 OL711667 This study
88. M. subcaerulea CUP-A-015335 USA OL711668 This study
89. M. supina 128a Italy JF908388 Osmundson et al. (2013)
90. M. tenax p187i USA EU669224 Unpublished
91. M. tenax OSC 113746 USA EU846251 Unpublished
92. M. viridimarginata 104h Italy JF908378 Osmundson et al. (2013)
93. M. vulgaris 447h Italy JF908435 Osmundson et al. (2013)
94. M. vulgaris 3781 Canada KJ705177 Unpublished
95. M. zephirus KA13-1265 Korea KR673722 Kim et al. (2015)
96. Xeromphalina campanella TFB14487 USA KP835678 KM011910 Aldrovandi et al. (2015)
97. X. campanella TFB7283A USA KM024575 KM024671 Aldrovandi et al. (2015)

Results

Phylogenetic analysis

BI and ML reconstructions, based on the optimal evolutionary model selected for the ITS and nLSU partitions (GTR + I + G), recovered similar topologies. The BI tree was selected as a representative phylogeny (Fig. 1).

Figure 1. 

Phylogenetic tree inferred from partial ITS+nLSU sequence data by Bayesian inference and maximum likelihood. The tree is rooted with Xeromphalina campanella. Maximum likelihood support values (BS) ≥ 75 and Bayesian posterior probabilities (BPP) ≥ 0.95 are indicated above or below branches (BS/BPP). Red dots indicate two new species, while green dots indicate Mycena subcaerulea specimens from TENN and CUP.

In the tree shown in Fig. 1, which is based on 116 concatenated ITS+nLSU sequences of 43 Mycena species and the new taxa, the two samples of M. caeruleogrisea and the two samples of M. caeruleomarginata each form monophyletic lineages with high statistical support (M. caeruleogrisea, ML bootstrap support [BS] = 100, Bayesian posterior probability [BPP] = 1.00; M. caeruleomarginata, BS = 100, BPP = 1.00). According to the tree topology, M. subcaerulea is the species most closely related to M. caeruleogrisea and M. caeruleomarginata, consistent with morphology and clusters with the latter two species with high statistical support (BS = 100, BPP = 1.00). The M. subcaerulea clade comprises three samples: CUP-A-015335 (originally identified as M. cyanothrix G.F. Atk.), TENN-F-051121 and TENN-F-057919 (BS = 100, BPP = 1.00). By its morphological features and phylogenetic placement, sample CUP-A-015335 should be re-assigned to M. subcaerulea. The clade comprising M. subcaerulea and the two new taxa are sister to M. amicta, with the clade constituted by these four species in turn sister to M. cyanorhiza. Despite the close relationships, the two new species are strongly supported as distinct from M. amicta and M. cyanorhiza (Fig. 1).

It is noteworthy that the six samples of M. amicta from Europe and North America cluster together with strong support (BS = 100, BPP = 1.00), but the Canadian material (voucher no. 189f) seems to be closer to the Italian sample (voucher no. 4745-HRL 1312) than to the specimens from France and Finland. In addition, M. pachyderma Kühner, a non-bluish species in sect. Viscipelles, is a sister taxon (BS = 79, BPP = 0.97) to M. cyanorhiza in the same section.

Taxonomy

In addition to morphological studies of the new taxa collected in China, morphological observations were made on 17 bluish specimens of Mycena loaned from fungal herbaria in the USA, namely, four specimens from the University of Tennessee (TENN) and 13 specimens from University of Cornell (CUP).

Our morphological observations using a light microscope confirmed the identity of 12 specimens as M. subcaerulea: TENN-F-014183, TENN-F-051121, TENN-F-052683, TENN-F-057919, CUP-A-002382, CUP-A-009686, CUP-A-014679, CUP-A-015138, CUP-A-015335, CUP-A-022677, CUP-A-023037 and CUP-A-023304. Another specimen, CUP-A-021234, previously identified as M. iris, was well characterised as M. amicta, based on its elongated ellipsoid basidiospores and clavate cheilocystidia with a rounded apex. As already noted by Smith (1947), the basidiomata of CUP-A-018443, CUP-A-022667, CUP-A-051322 and CUP-A-051323 were too small to be examined.

Mycena caeruleogrisea Q. Na, Y.P. Ge & H. Zeng, sp. nov.

MycoBank No: MB837656
Figs 2, 3, 4

Diagnosis

This species is characterised by blue pileus, turning bluish-grey with age, pileus covered by a separable, gelatinous pellicle, stipe pruinose and with a blue base and stipe basal disc and acanathocysts of pileipellis absent. Mycena subcaerulea differs from M. caeruleogrisea by a greenish-blue to greyish-brown pileus that turns yellow and remains blue at the centre and margin with age, a greenish-blue to brownish-blue stipe and smaller, globose to subglobose basidiospores.

Holotype

China. Ningxia Hui Autonomous Region: Liangdianxia, Liupan Mountains National Forest Park, Jingyuan County, Guyuan City, 35°21'74"N, 106°18'37"E, 19 July 2020, Qin Na, Yupeng Ge, Hui Zeng, Junqing Yan and Zewei Liu, FFAAS 0001 (collection number MY0164).

Etymology

Refers to the pileus colour: blue when young, becoming bluish-grey with age.

Description

Pileus 12–25 mm in diameter, hemispherical when young, conical, obtusely conical, campanulate with age, shallowly sulcate, translucently striate, almost smooth when young, becoming slightly brownish scaly at the centre, pruinose, with a glabrescent margin, dull blue (23D5) at the centre, margin pallescent to pastel blue (23A4), turning bluish-grey (23D2–23D3), a bit sticky, covered by a separable, gelatinous pellicle. Context white, thin, fragile. Lamellae 16–28 reaching the stem, adnate to slightly adnexed with a short tooth, narrowly spaced, white, with intervenose veins, edges concolorous with the face. Stipe 48–76 × 1.5–2.0 mm, equal or slightly broadened below, hollow, fragile, entirely pruinose (Fig. 2g–i), white, base greyish-blue (23B5) (Fig. 2j, k), covered with white fibrils, a basal disc absent. Odour and taste indistinctive.

Figure 2. 

Fresh basidiomata of Mycena caeruleogrisea a–d M. caeruleogrisea (FFAAS 0001, holotype) e, f M. caeruleogrisea (FFAAS 0002) g–i entirely pruinose stipe j, k bluish base. Scale bars: 10 mm (a–i); 2 mm (j–k). Photographs by Yupeng Ge (a, b) and Qin Na (c–k).

Basidiospores [60/3/2] (8.8) 9.3–10.4–11.3 (11.8) × (5.5) 5.7–6.5–6.9 (7.3) μm [Q = 1.57–1.68, Q = 1.60 ± 0.072] [holotype [40/2/1] (9.1) 9.4–10.3–11.3 (11.6) × (5.6) 6.0–6.5–6.9 (7.2) μm, Q = 1.55–1.63, Q = 1.59 ± 0.049], ellipsoid, hyaline in 5% KOH, smooth, guttulate, thin-walled, amyloid. Basidia 22–29 × 7–9 μm, 4- or 2-spored, clavate. Cheilocystidia 40–62 × 4–6 μm, clustered, abundant, elongated clavate or cylindrical, apically broadly rounded, thin-walled, hyaline, forming a sterile lamellae edge. Pleurocystidia absent. Pileipellis an ixocutis with 1–4 μm wide hyphae, smooth or sparsely coated with simple cylindrical excrescences or inflated cells, 3–11 × 1–2 μm, embedded in gelatinous matter; acanathocysts absent. Hypodermium undifferentiated. Hyphae of the stipitipellis 3–8 μm in diameter, smooth, hyaline; caulocystidia 38–69 × 6–8 μm, long cylindrical, smooth, transparent. All tissues dextrinoid. Clamps present in all tissues.

Figure 3. 

Microscopic features of Mycena caeruleogrisea (FFAAS 0001, holotype) a–d basidiospores e–g cheilocystidia h pileipellis i stipitipellis and caulocystidia. Scale bars: 10 μm (a–i). Structures were stained with Congo Red medium before photographing.

Habit and habitat

Scattered on humus and fallen leaves in mixed forests of Acer, Populus, Pinus and Quercus.

Figure 4. 

Morphological features of Mycena caeruleogrisea (FFAAS 0001, holotype) a basidiomata b basidia c basidiospores d cheilocystidia e stipitipellis and caulocystidia f pileipellis. Scale bars: 10 mm (a); 10 μm (b–f). Drawings by Qin Na and Yupeng Ge.

Known distribution

Ningxia Hui Autonomous Region, China.

Additional material examined

Ningxia Hui Autonomous Region: Xiaonanchuan, Jingyuan County, Guyuan City, 20 July 2020, Qin Na, Yupeng Ge, Hui Zeng, Junqing Yan and Zewei Liu, FFAAS 0002 (collection number MY0169).

Remarks

The original description of M. subcaerulea Sacc. was as follows: “Pileo tenuissimo, campanulato v. convexo, striato, glabro, pallide cæruleo-viridi; stipite tenui, æquali, roseo-albo, subtiliter pruinoso; lamellis angustis, confertis, antice attenuatis, candidis; sporis subglobosis. 4 µ. d. Hab. In trunco fagineo in montibus Adirondack Amer. bor. – Cæspitosa, 5 cm. alta; pileus 8–13 mm. latus. Discus margine saturatius coloratus atque pileus cuticula secernibili obtectus.” (Saccardo 1887). This North American species, which also has bluish basidiomata, is the taxon most closely resembling M. caeruleogrisea in both macro- and microscopic features; however, M. subcaerulea differs by a greenish-blue to greyish-brown pileus that turns yellow and remains blue at the centre and margin with age, a greenish-blue to brownish-blue stipe and smaller, globose to subglobose, basidiospores [6–8 × 6–7(8) µm] (Saccardo 1887; Smith 1947). In addition, M. subcaerulea was found solitary, scattered or gregarious on debris, decaying wood or bark around the bases of living trees, especially of oak, but also occurring quite frequently on decaying wood of basswood, elm, beech and other hardwoods (Smith 1947). The following microscopic characteristics of M. subcaerulea were also observed on the 11 CUP-A and TENN-F specimens in our study: basidiospores 5.6–8.3 × 5.3–7.9 µm, globose to subglobose; basidia 19–24 × 6–8 µm, clavate, 4-spored; cheilocystidia 36–55 × 3–6 µm; pileipellis hyphae 2–4 μm wide, coated with cylindrical excrescences or inflated cells, 1.1–14.9 × 0.7–1.4 μm, embedded in gelatinous matter; hyphae of the stipitipellis 4–10 μm in diameter; caulocystidia 42–70 × 4–10 μm, fusiform or cylindrical, smooth; clamps present (Figs 5, 6). In M. cyanorhiza, the base of the stipe can be strikingly sky blue, but it has a pale brown, grey to almost white pileus, a stipe base arising from a patch of fine fibrils, clavate to obpyriform cheilocystidia with finger-like excrescences and basidiospores that are elongated ellipsoid (Q = 1.6–2.2); these features all contrast with those of the new species (Aronsen and Læssøe 2016; Perry et al. 2020) (Table 2). In addition, M. amicta can be easily mistaken for M. caeruleogrisea, as it sometimes also has a bluish pileus when mature and similarly-shaped basidiospores, cheilocystidia and caulocystidia, but M. amicta can be distinguished from the latter species in having a pileus generally more brownish with a bluish tinge more or less present, an indistinct to raphanoid odour, a greyish-brown stipe that has a blue to blue-green base and is covered with a dense, fairly coarse, white pubescence and smaller cheilocystidia (16–45 × 3.5–7 µm); in addition, M. amicta is restricted to growth on wood and woody debris (Robich 2003; Aronsen and Læssøe 2016) (Table 2). Mycena interrupta, which is well characterised by its acid blue to dull blue pileus and translucent stipe, is easily distinguished from M. caeruleogrisea by having smaller basidiomata, free lamellae, a white hirsute basal disc with blue margins on the stipe, broadly ellipsoid to subglobose spores and cheilocystidia covered with coarse excrescences (Grgurinovic 2003) (Table 2). Mycena lazulina, a new taxon reported from south-western Japan, possesses a blue stipe and cheilocystidia with numerous excrescences, which can be used to differentiate it from M. caeruleogrisea (Terashima et al. 2016). Another recently-described species of Mycena from Taiwan, M. indigotica, has blue basidiomata; however, the cap has tubes similar to Boletus and possesses globose basidiospores (Wei and Kirschner 2019).

Table 2.

Morphological comparison of Mycena caeruleogrisea, M. caeruleomarginata, and related species.

Taxa M. caeruleogrisea M. caeruleomarginata M. subcaerulea M. amicta M. cyanorhiza M. interrupta
Pileus 12–25 mm diam., hemispherical when young, conical, obtusely conical, campanulate with age, smooth when young, becoming slightly brownish scaly at the center, pruinose, acid blue to dull blue at the center and margin pallescent, turning bluish gray, covered by a separable, gelatinous pellicle. 3.5–13 mm in diam., parabolic, obtusely conical when young, hemispherical, campanulate with age, with an umbo at the center, shallowly sulcate, translucent-striate, smooth, gelatinous slightly, the margin infrequently out of flatness, brown to dark brown, becoming acid blue to dull blue towards the margin, with a greyish white margin, covered by a separable, sticky pellicle. (3)5–15(25) mm broad, more or less ovoid with an appressed or slightly incurved margin, becoming obtusely conic to campanulate, surface lubricous subviscid, glabrous or appearing somewhat granulose near the margin, translucent-striate, pellicle tenacious and completely separable, pale blue or greenish blue, soon tinged with brown and assuming various degrees of bluish, greenish, or grayish brown with a pallid margin, often sordid yellowish in age, bluish tints often lingering on the margin. 5–15 mm wide, conical to campanulate, ± sulcate, translucent-striate, finely puberulous, covered with a separable gelatinous pellicle, pale grey-brown or pale sepia brown, sometimes with an olivaceous, greenish or bluish green shade, margin often bluish green, or more rarely dingy citrine to ochraceous yellow. 2–5(–10) mm wide, covered with a (separable), gelatinous pellicle, at first ± globose, then hemispherical to parabolic, becoming convex or somewhat depressed, but also with a small papilla, sulcate, translucent-striate, pruinose, glabrescent, somewhat lubricous, initially pale brown, then pale grey with darked centre, becoming almost white with age. 16 mm in diam., up to 4 mm high, at first subglobose to ovoid-conical, with age becoming convex to shallowly so, slightly depressed at apex, shiny, gelatinous, minutely radially rugulose, ± pruinose in places, at first dull blue at apex, below apex, becoming dull blue towards margin; margin decurved, entire, sulcate, striate, faintly translucent-striate.
Context White, thin, fragile. White, fragile, thin. Thin, pallid, pliant. Very thin to moderately thick at apex, translucent white or translucent greyish white.
Lamellae 16–28 reaching the stem, adnate to slightly adnexed with a short tooth, narrowly spaced, white, with intervenose veins. 14–25 reaching the stem, adnate to slightly adnexed with a short tooth, white, with unconspicuous intervenose veins, edges concolorous with the face. Close to crowded, 18–25 reach the stipe, two or three tiers of lamellulae, ascending-adnate, sometimes narrowly adnate or practically free, narrow to moderately broad, white or tinged grayish, edges slightly fimbriate. 17–25 reaching the stem, ascending, adnexed, greyish to greyish brown; edge whitish, at times yellowish, greenish or bluish near the cap margin. 9–14 reaching the stem, ascending, adnexed to fairly broadly adnate or almost free, sometimes with a pseudocollarium, whitish or pale grey; edge whitish and separable as an elastic-tough thread. Free from stipe or adnately attached to obvious circular descent of pileal flesh, moderately close to distant, five to seven per quadrant, subventricose, moderately broad to broad; edge marginate, blue; sides minutely pruinose, white; with one or two series of lamellulae.
Stipe 48–76 × 1.5–2.0 mm, equal or slightly broadened below, hollow, fragile, pruinose, white, base acid blue in the whole age, covered with white fibrils. 32–46 × 1.0–2.0 mm, equal, base sometimes slightly broaden, fragile, hollow, pruinose, puberulous entirely when young, becoming sparely especially in the middle part when old, yellowish brown to light brown, base with acid blue tinge, covered with a bit white fibrils. 3–8 cm long, 1–2 (2.5) mm. thick, equal, terete, flexuous or strict, tubular, cartilaginous, elastic, at first densely pruinose or minutely pubescent over all form a dense coating of caulocystidia, somewhat glabrescent, base mycelioid, the mycelium blue at first but soon fading to white, bluish to greenish blue above at first, soon fading to grayish or finally sordid brownish. 40–70 × 0.5–2 mm, cylindrical, entirely covered with a dense and fairly coarse, white pubescence, greyish brown, usually somewhat paler at the apex, occasionally with a slight lilaceous or violaceous tint; base at times somewhat rooting, concolorous or with some blue-green stains or entirely blue, even the substrate may be stained blue. 5–30 (–70) × 0.5–1 mm, cylindrical, entirely puberulous, glabrescent in the middle part, pale grey to hyaline-white; base hirsute, sky blue (also in the flesh), springing from a patch of fine, radiating, white fibrils. Up to 22 mm long, cylindrical, moist to dry, often pruinose especially towards base, translucent white, attached to substratum via white pruinose disc borne on a flattened dull blue base.
Odor & taste Indistinctive Indistinctive Mild Indistinct to raphanoid. Smell none or reported as faintly nitrous; taste not recorded. Odour not distinctive.
Spores (9.0) 9.3–11.6 (11.8) × (6.0) 6.2–7.3 (7.7) μm, Q = 1.5–1.7, ellipsoid, amyloid. (6.2) 6.4–7.7 (7.9) × (4.4) 4.7–5.8 (6.0) μm, Q = 1.23–1.54, broadly ellipsoid to ellipsoid, amyloid. 6–8 × 6–7 (8) μm, globose or subglobose, amyloid. 7.5–10.7 × 4.5–6 μm, Q = 1.5–1.9, Qav ≈ 1.6, pip-shaped, amyloid. 6.5–9 × 4–5 μm, Q = 1.6–2.2, Qav ≈ 1.8, pip-shaped, amyloid. (54/3), 8.4–11.6 (x̄ = 9.9, SD = ± 0.7) × 5.7–8.8 (x̄ = 7.0, SD = ± 0.6) μm, Q = 1.4, broadly ellipsoidal rarely subglobose, with prominent short, oblique apiculus, amyloid.
Basidia 22–29 × 7–9 μm, 4- or 2-spored. 26–35 × 6–12 μm, 4- or 2-spored. 4-spored 30–40 × 6–7 μm, clavate, 4-spored. 18–25 × 6.5–11 μm, clavate, 4-spored. (27/2), 21.6–39.8 (x̄ = 29.0, SD = ± 5.2) × 8.3–16.0 (x̄ = 11.6, SD = ± 2.6) μm, 4-spored, rarely 2-spored, sterigmata to 8.8 μm long.
Cheilocystidia 40–62 × 4–6 μm, clustered, abundant, long clavate or cylindrical, apically broadly rounded, thin-walled, hyaline, forming a sterile lamellae edge. 32–48 × 4–6 μm, abundant, clustered, cylindrical or long clavate, apically broadly rounded, thin-walled, hyaline, forming a sterile lamellae edge. Abundant, 32–60 × 5–8 μm, subfusoid with obtuse apices but becoming more or less cylindric, sometimes flexuous, smooth, hyaline. 16–45 × 3.5–7 μm, clavate, subfusiform or more often cylindrical. 9–20 × 5.5–7 μm, embedded in gelatinous matter, clavate to obpyriform, with few, simple to branched excrescences, 3–14 × 1–1.5 μm. Abundant, (30/1), 16.8–44.8 (x̄ = 25.5, SD = ± 6.55) × 5.6–13.6 (x̄ = 8.4, SD = ± 1.8) μm, filamentous, cylindrical, clavate to ovoid, sometimes ventricose at base, with nodulose excrescences.
Pleurocystidia Absent Absent Not differentiated Absent Absent Absent
Pileipellis Hyphae 1–4 μm wide, sparse, smooth or sparsely coated with simple, cylindrical excrescences or inflated cells, 3.1–11.2 × 0.8–1.7 μm, embedded in gelatinous matter. Hyphae 2–4 μm wide, with simple, cylindrical excrescences, 2.0–6.4 × 0.6–1.8 μm, embedded in gelatinous matter. A thick gelatinous pellicle (blue color located along the surface of the pellicle in incompletely gelatinized hyphae). Hyphae 2–4.5 μm wide, branched, anastomosing, smooth with scattered, cylindrical excrescences, embedded in a layer of gelatinous matter. Hyphae 1.5–3.5 μm wide, embedded in gelatinous matter, very branched, covered with scattered, simple to branched excrescences, protruding through the gelatinous layer. Hyphae (28/1), 2.8–8.0 (x̄ = 5.4, SD = ± 1.4) μm in diam., nodulose-diverticulate with dense nodulose to cylindrical excrescences, gelatinized.
Stipitipellis Hyphae 3–8 μm in diameter, smooth, hyaline. Hyphae 3–6 μm in diameter, smooth, hyaline. Hyphae 2–3.5 μm wide, smooth Hyphae 1–3 μm wide, smooth. Hyphae (26/1), 1.6–3.2 (x̄ = 2.4, SD = ± 0.4) μm in diam., not gelatinized.
Caulocystidia 38–69 × 6–8 μm, long cylindrical, smooth, transparent. 19–40 × 4–8 μm, smooth, transparent, two shapes: fusiform or cylindrical. Covered with numerous cystidia, elongated and flexuous. 50–145 × 8–11.5 μm, fusiform to subcylindrical. Up to 60 × 7 μm, simple to furcate or somewhat branched. Often fasciculate, (25/1), 50.6–128.0 (x̄ = 75.0, SD = ± 19.8) × 5.0–8.8 (x̄ = 6.3, SD = ± 1.1) μm, filamentous to slightly ventricose especially towards base, rarely bifurcate.
Clamps Present Present Present Present Present Present
Habitat Scattered, on humus and fallen leaves in Acer, Populus, Pinus, and Quercus mixed forests. Scattered, on rotten wood in Picea, Pinus, Quercus, Robinia, and Tilia mixed forests. Single, scattered or gregarious on debris, decaying wood, or on the bark around the bases of live trees of oak in particular, but also occurring quite frequently on decaying wood of basswood, elm, beech, and other hardwoods. On wood and woody debris, mostly from conifers but also deciduous trees, also among leaves and needles. On conifers (Picea, Pinus and Larix) bark and twigs, often on small bark fragments deep in grass. Generally gregarious, often abundant, rarely solitary or scattered, on fallen decayed logs or stumps of Eucalyptus, Nothofagus, Bedfordia, Pinus, etc. forest.
Distribution China China North America (Alabama, Carolina, New York, Tennessee, Pennsylvania, Michigan); Canada (Nova Scotia, Ontario, Manitoba) Europe (Scandinavia, Netherlands, Italy) Europe (UK, Denmark, Italy) Australia and New Zealand
Occurrence time Summer to autumn. Late summer to early autumn. Spring to fall, more abundant locally in the spring. Late summer to late autumn, rarely in spring. Summer to autumn. March to July.
References This study This study Saccardo 1887; Smith 1947 Robich 2003; Aronsen and Læssøe 2016 Robich 2003; Aronsen and Læssøe 2016; Perry 2020 Grgurinovic 2003
Figure 5. 

Microscopic features of Mycena subcaerulea a, b basidiospores (TENN-F-057919) c basidiospores (CUP-A-002382) d basidiospores (CUP-A-015138) e–g cheilocystidia (TENN-F-057919) h, i pileipellis (TENN-F-057919) j stipitipellis and caulocystidia (TENN-F-057919). Scale bars: 5 μm (a–d); 10 μm (e–j). Structures were stained with Congo Red medium before photographing.

Figure 6. 

Morphological features of Mycena subcaerulea a basidiospores b basidia c stipitipellis and caulocystidia d cheilocystidia e pileipellis. Scale bars: 10 μm (a–e). Drawings by Qin Na and Yupeng Ge.

Mycena caeruleomarginata Q. Na & Y.P. Ge, sp. nov.

MycoBank No: MB842100
Figs 7, 8, 9

Diagnosis

This species is characterised by dark brown pileus with a blue margin and the stipe densely pruinose, entirely covered with puberulous hairs and stipe basal disc and acanathocysts of pileipellis absent. Mycena subcaerulea differs from M. caeruleogrisea in having a pileus that is distinctly greyish-brown with a blue centre and margin, turning yellow with age, a stipe tinged greenish-blue and globose to subglobose basidiospores.

Holotype

China. Jilin Province: Chixi Protection Station, Erdaobaihe Town, Antu County, Yanbian Korean Autonomous Prefecture, 42°46'35"N, 128°15'04"E, 3 July 2021, Qin Na, Yupeng Ge, Binrong Ke and Chi Yang, FFAAS 0357 (collection number MY0337).

Etymology

Refers to the pileus, which is blue at the margin.

Description

Pileus 3.5–13 mm in diameter, parabolic, obtusely conical when young, hemispherical, campanulate with age, with an umbo at the centre, shallowly sulcate, translucently striate, smooth, slightly gelatinous, the margin infrequently out of flatness, dark brown (6F5–6F7), disc brown (6E6–6E7), becoming greyish-blue (23B5) to blue (23B7) towards the margin (Fig. 7c, d, i), margin grey (23B1) (Fig. 7c, d, i), covered by a separable, viscid pellicle. Context white, fragile, thin. Lamellae 14–25 reaching the stem, adnate to slightly adnexed with a short tooth, white, inconspicuously intervenose, edges concolorous with the face. Stipe 32–46 × 1.0–2.0 mm, equal, base sometimes slightly broadened, fragile, hollow, pruinose, entirely puberulous when young (Fig. 7h), becoming sparingly so, especially in the middle part, when old (Fig. 7e), greyish-brown (5E3) to brown (5E4), base with an greyish-blue (23B5) tinge (Fig. 7a, f), sparsely covered with white fibrils, a basal disc absent. Odour and taste indistinctive.

Figure 7. 

Fresh basidiomata of Mycena caeruleomarginata a–f M. caeruleomarginata (FFAAS 0357, holotype) g–j M. caeruleomarginata (FFAAS 0358) a, f stipe with a bluish base c, d, i pileus with blue margin e, h densely white, pruinose to pubescent stipe. Scale bars: 10 mm (a, b, e, f, g, h); 5 mm (c, d); 2 mm (i, j). Photographs by Qin Na (a–f) and Yupeng Ge (g–j).

Basidiospores [60/3/2] (6.2) 6.4–7.1–7.7 (7.9) × (4.4) 4.7–5.2–5.8 (6.0) μm [Q = 1.23–1.54, Q = 1.36 ± 0.071] [holotype [40/2/1] (6.4) 6.6–7.2–7.7 (7.8) × (4.7) 4.9–5.2–5.3 (5.7) μm, Q = 1.26–1.53, Q = 1.39 ± 0.070], broadly ellipsoid to ellipsoid, hyaline in 5% KOH, guttulate, smooth, thin-walled, amyloid. Basidia 26–35 × 6–12 μm, 4- or 2-spored, clavate. Cheilocystidia 32–48 × 4–6 μm, abundant, clustered, cylindrical or elongated clavate, apically broadly rounded, thin-walled, hyaline, forming a sterile lamellae edge. Pleurocystidia absent. Pileipellis an ixocutis with 2–4 μm wide hyphae, simple, cylindrical excrescences, 2–6 × 1–2 μm, embedded in gelatinous matter; acanathocysts absent. Hypodermium undifferentiated. Hyphae of the stipitipellis 3–6 μm in diameter, smooth, hyaline; caulocystidia smooth, transparent, of two shapes: (1) fusiform or cylindrical, 19–40 × 4–8 μm; (2) extremely long cylindrical, sometimes with a narrow apex, 115–178 × 5–9 μm. All tissues dextrinoid. Clamps present in all tissues.

Figure 8. 

Morphological features of Mycena caeruleomarginata (FFAAS 0357, holotype) a basidiomata b basidia c basidiospores d cheilocystidia e stipitipellis and caulocystidia f pileipellis. Scale bars: 10 mm (a); 10 μm (b–f). Drawings by Qin Na and Yupeng Ge.

Habit and habitat

Scattered on rotten wood in Picea, Pinus, Quercus, Robinia and Tilia mixed forests.

Figure 9. 

Microscopic features of Mycena caeruleomarginata (FFAAS 0357, holotype) a–d basidiospores e–g cheilocystidia h–j pileipellis j stipitipellis and caulocystidia. Scale bars: 5 μm (a–d); 10 μm (e–j). Structures were stained with Congo Red medium before photographing.

Known distribution

Jilin Province, China.

Additional material examined

Jilin Province: Hancongling, Erdaobaihe Town, Antu County, Yanbian Korean Autonomous Prefecture, 42°46'36"N, 128°15'04"E, 4 July 2021, Qin Na, Yupeng Ge, Binrong Ke and Chi Yang, FFAAS 0358 (collection number MY0343).

Remarks

The diagnostic features of M. caeruleomarginata can be used to distinguish this new taxon from the closely-related bluish species M. subcaerulea, M. cyanorhiza, M. amicta and M. interrupta (Table 2). Mycena subcaerulea, the species most similar to M. caeruleomarginata, differs in having a pileus that is distinctly greyish-brown with a blue centre and margin, turning yellow with age, a stipe tinged greenish-blue and globose to subglobose basidiospores (Q = 1.01–1.14) according to the original description and our observations (Saccardo 1887; Smith 1947) (Figs 5, 6; Table 2). Similar to M. caeruleomarginata, M. cyanorhiza has an entirely puberulous, pruinose stipe with a sky blue base and possesses a gelatinous pileus; however, the pileus of M. cyanorhiza is pale brown, grey to almost white, without a bluish tinge and this species has elongated ellipsoid basidiospores (Q > 1.6) and lacks smooth cheilocystidia and caulocystidia (Aronsen and Læssøe 2016; Perry et al. 2020). In addition, M. amicta resembles M. caeruleomarginata in its bluish pileus, pruinose stipe and pileipellis embedded in a layer of gelatinous matter, but the former differs in having a pale grey-brown pileus that is sometimes ochraceous yellow and greenish when young and bluish when old, a raphanoid odour and elongated ellipsoid basidiospores (7.5–10.7 × 4.5–6.0 µm) (Robich 2003; Aronsen and Læssøe 2016). The Southern Hemisphere species M. interrupta is well characterised by its blue pileus at maturity, a translucent stipe with a basal disc and cheilocystidia with excrescences (Grgurinovic 2003). Furthermore, two new species with bluish basidiomata reported from East Asia, M. lazulina and M. indigotica, can be easily distinguished from the new species in their whitish pileus or tubes similar to Boletus; M. lazulina having cheilocystidia with numerous excrescences and M. indigotica possesses globose basidiospores (Terashima et al. 2016; Wei and Kirschner 2019). Mycena caeruleogrisea and M. caeruleomarginata share the same bluish pileus and stipe base, smooth and cylindrical cheilocystidia and pileipellis embedded in a layer of gelatinous matter. Mycena caeruleomarginata can be readily distinguished, however, based on the dark brown colour of the pileus with a blue margin, yellowish-brown to light brown stipe, broadly ellipsoid to ellipsoid spores and caulocystidia of two shapes.

Key to seven bluish Mycena species of sections Amictae, Cyanocephalae, Sacchariferae, and Viscipelles

1 Cheilocystidia non-smooth 2
Cheilocystidia smooth (sect. Amictae) 4
2 Acanthocysts present (sect. Sacchariferae) M. lazulina
Acanthocysts absent 3
3 Stipe with basal disc (sect. Cyanocephalae) M. interrupta
Stipe without basal disc (sect. Viscipelles) M. cyanorhiza
4 Basidiospores subglobose M. subcaerulea
Basidiospores broadly ellipsoid to ellipsoid 5
5 Caulocystidia of two types: (1) fusiform or cylindrical, 19–40 × 4–8 μm; (2) extremely long, cylindrical (length > 100 μm) M. caeruleomarginata
Caulocystidia of one type, fusiform, subcylindrical to cylindrical (length < 100 μm) 6
6 Pileus pale grey-brown or pale sepia brown, sometimes with an olivaceous, greenish or bluish-green shade; margin often bluish-green or rarely dingy citrine to ochraceous yellow M. amicta
Pileus sky blue, greyish-blue with age; margin blue when young, turning bluish-grey when old M. caeruleogrisea

Discussion

With their blue pileus and gelatinous pileipellis, the new taxa M. caeruleogrisea and M. caeruleomarginata are unique in China. Similar species described from North America and Europe, namely, M. subcaerulea, M. cyanorhiza and M. amicta, have bluish basidiomata as well, but with age, these species often change colours—to green, brown or yellow and the sizes and shapes of their basidiospores and cheilocystidia are also different (Saccardo 1887; Smith 1947; Maas Geesteranus 1980, 1992a, 1992b; Grgurinovic 2003; Robich 2003; Aronsen and Læssøe 2016) (Table 2). Mycena interrupta, described from the Southern Hemisphere, can be distinguished from the two newly-described species, based on both habitat and morphology (Grgurinovic 2003). Mycena lazulina (sect. Sacchariferae), which has a white pileus, blue stipe base, acanthocysts and a non-gelatinised pileipellis, seems to be the most distinct bluish species and is not included in Table 2 (Terashima et al. 2016). According to taxonomic research based on morphology and phylogeny, our newly-described species are more similar to M. subcaerulea and M. amicta and should, thus, be classified into sect. Amictae.

Although pileus colour has been used as a basis for sectional division in Mycena, this character does not seem to be satisfactory for species identification, especially within the same section (Smith 1947; Maas Geesteranus 1980, 1992a, 1992b; Grgurinovic 2003; Robich 2003; Aronsen and Læssøe 2016). In sect. Viscipelles, for example, M. cyanorhiza can be distinctly characterised by the presence of a sky blue stipe, but M. ulmi B.A. Perry & H.W. Keller, M. pachyderma and M. pseudocyanorrhiza Robich do not exhibit any bluish tint (Robich 2003; Aronsen and Læssøe 2016; Perry et al. 2020). A combination of macroscopic and microscopic features, such as the colour of basidiomata and the shapes and sizes of spores, cheilocystidia, pileipellis, caulocystidia and dextrinoid tissues, is, thus, generally regarded as more important for the identification of Mycena taxa.

Acknowledgements

This study was supported by the Natural Science Foundation of Shandong Province (grant No. ZR2020QC001), the National Natural Science Foundation of China (grant No. 3190012), the Natural Science Foundation of Shandong Province (grant No. ZR2019PC028) and the Innovation Team of Shandong Agricultural Industry Technology System (grant No. 26, SDAIT-07-03). We are extremely grateful for the assistance of the Herbaria of Cornell University and the University of Tennessee and especially appreciate the kind help of Collections Manager Margaret Oliver, Dr P. Brandon Matheny and Curator Teresa Iturriaga with specimen loan requests. We sincerely thank Dr Jianwei Liu for help with phylogenetic analyses and Dr Xiaojuan Deng, Mr Bai Wang, Mr Chi Yang and colleagues of the Guyuan Branch Institute of Ningxia Academy of Agriculture and Forestry Sciences for help with fieldwork. We also thank the editors and reviewers for their corrections and suggestions to improve our work.

References

  • Aldrovandi MS, Johnson JF, O’Meara BC, Petersen RH, Hughes KW (2015) The Xeromphalina campanella/kauffmanii complex: Species delineation and biogeographical patterns of speciation. Mycologia 107(6): 1270–1284. https://doi.org/10.3852/15-087
  • Antonín V, Noordeloos ME (2004) A monograph of the genera Hemimycena, Delicatula, Fayodia, Gamundia, Myxomphalia, Resinomycena, Rickenella, and Xeromphalina (Tribus Mycenae sensu Singer, Mycena excluded) in Europe. IHW-Verlag, 280 pp.
  • Aravindakshan DM, Manimohan P (2015) Mycenas of Kerala. SporePrint Books, Calicut, India, 213 pp.
  • Aravindakshan DM, Kumar TK, Manimohan P (2012) A new bioluminescent species of Mycena sect. Exornatae from Kerala State, India. Mycosphere: Journal of Fungal Biology 3(5): 556–561. https://doi.org/10.5943/mycosphere/3/5/4
  • Aronsen A, Læssøe T (2016) The Genus Mycena s.l. Fungi of Northern Europe Vol. 5. Narayana Press, Gylling, Denmark, 373 pp.
  • Aronsen A, Larsson E (2015) Studier i slaktet Mycena (hattor). Svensk Mykologisk Tidskrift 36(3): 23–29.
  • Baird R, Stokes CE, Wood-Jones A, Watson C, Alexander M, Taylor G, Johnson K, Threadgill P, Diehl S (2014) A molecular clone and culture inventory of the root fungal community associated with Eastern Hemlock in Great Smoky Mountains National Park. Southeastern Naturalist (Steuben, ME) 13(6): 219–237. https://doi.org/10.1656/058.013.s601
  • Chew A, Desjardin DE, Tan YS, Musa MY, Sabaratnam V (2015) Bioluminescent fungi from peninsular Malaysia—A taxonomic and phylogenetic overview. Fungal Diversity 70(1): 149–187. https://doi.org/10.1007/s13225-014-0302-9
  • Ge YP, Liu ZW, Zeng H, Cheng XH, Na Q (2021) Updated description of Atheniella (Mycenaceae, Agaricales), including three new species with brightly coloured pilei from Yunnan Province, southwest China. MycoKeys 81: 139–164. https://doi.org/10.3897/mycokeys.81.67773
  • Geml J, Timling I, Robinson CH, Lennon N, Nusbaum HC, Brochmann C, Noordeloos MC, Taylor DL (2015) An arctic community of symbiotic fungi assembled by long‐distance dispersers: Phylogenetic diversity of ectomycorrhizal basidiomycetes in Svalbard based on soil and sporocarp DNA. Journal of Biogeography 39(1): 74–88. https://doi.org/10.1111/j.1365-2699.2011.02588.x
  • Grgurinovic CA (2003) The genus Mycena in south-eastern Australia. Fungal Diversity Press, 329 pp.
  • Harder CB, Læssøe T, Kjøller R, Frøslev TG (2010) A comparison between ITS phylogenetic relationships and morphological species recognition within Mycena sect. Calodontes in Northern Europe. Mycological Progress 9(3): 395–405. https://doi.org/10.1007/s11557-009-0648-7
  • Harder CB, Lodge DJ, Petersen RH, Hughes KW, Blanco JC, Frøslev TG, Læssøe T (2012) Amyloidity is not diagnostic for species in the Mycena pearsoniana complex (Mycena section Calodontes). Mycological Progress 2012(11): 725–732. https://doi.org/10.1007/s11557-011-0782-x
  • He MQ, Zhao RL, Hyde KD, Begerow D, Kemler M, Yurkov A, McKenzie EHC, Raspé O, Kakishima M, Sánchez-Ramírez S, Vellinga EC, Halling R, Papp V, Zmitrovich IV, Buyck B, Ertz D, Wijayawardene NN, Cui B-K, Schoutteten N, Liu X-Z, Li T-H, Yao Y-J, Zhu X-Y, Liu A-Q, Li G-J, Zhang M-Z, Ling Z-L, Cao B, Antonín V, Boekhout T, da Silva BDB, De Crop E, Decock C, Dima B, Dutta AK, Fell JW, Geml J, Ghobad-Nejhad M, Giachini AJ, Gibertoni TB, Gorjón SP, Haelewaters D, He S-H, Hodkinson BP, Horak E, Hoshino T, Justo A, Lim YW, Menolli Jr N, Mešić A, Moncalvo J-M, Mueller GM, Nagy LG, Nilsson RH, Noordeloos M, Nuytinck J, Orihara T, Ratchadawan C, Rajchenberg M, Silva-Filho AGS, Sulzbacher MA, Tkalčec Z, Valenzuela R, Verbeken A, Vizzini A, Wartchow F, Wei T-Z, Weiß M, Zhao C-L, Kirk PM (2019) Notes, outline and divergence times of Basidiomycota. Fungal Diversity 99(1): 105–367. https://doi.org/10.1007/s13225-019-00435-4
  • Hopple Jr JS, Vilgalys R (1999) Phylogenetic relationships in the mushroom genus Coprinus and dark-spored allies based on sequence data from the nuclear gene coding for the large ribosomal subunit RNA: Divergent domains, outgroups, and monophyly. Molecular Phylogenetics and Evolution 13(1): 1–19. https://doi.org/10.1006/mpev.1999.0634
  • Horak E (2005) Röhrlinge und Blätterpilze in Europa. Elsevier, Spektrum Akad. Verlag, 555 pp.
  • Jin JJ, Yu WB, Yang JB, Song Y, dePamphilis CW, Yi T-S, Li D-Z (2020) GetOrganelle: A fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biology 21(1): e241. https://doi.org/10.1186/s13059-020-02154-5
  • Kim CS, Jo JW, Kwag YN, Sung GH, Lee SG, Kim SY, Shin CH, Han SK (2015) Mushroom Flora of Ulleung-gun and a Newly Recorded Bovista Species in the Republic of Korea. Mycobiology 43(3): 239–257. https://doi.org/10.5941/MYCO.2015.43.3.239
  • Kornerup A, Wanscher JH (1978) Methuen handbook of colour. Eyre Methuen, London.
  • Li Y, Li TH, Yang ZL, Bau T, Dai YC (2015) Atlas of Chinese macrofungal resources. Central Chinese Farmer Press, Zhengzhou, China, 1351 pp.
  • Liu ZW, Na Q, Cheng XH, Wu XM, Ge YP (2021) Mycena yuezhuoi sp. nov. (Mycenaceae, Agaricales), a purple species from the peninsula areas of China. Phytotaxa 511(2): 148–162. https://doi.org/10.11646/phytotaxa.511.2.3
  • Maas Geesteranus RA (1980) Studies in Mycenas-15, A tentative subdivision of the genus Mycena in the Northern Hemisphere. Persoonia 11: 93–120.
  • Maas Geesteranus RA (1992a) Mycenas of the Northern Hemisphere I. Studies in Mycenas and other papers. Koninklijke Nederlandse Akademie van Wetenschappen, Amsterdam.
  • Maas Geesteranus RA (1992b) Mycenas of the Northern Hemisphere II. Conspectus of the Mycenas of the Northern Hemisphere. Koninklijke Nederlandse Akademie van Wetenschappen, Amsterdam.
  • Malysheva V, Malysheva E, Voronina EY, Fedosova A, Bibikov N, Kiseleva DS (2017) Mycorrhiza of Pyroloids (Pyrola rotundifolia, P. media and Orthilia secunda): Species composition of symbionts and trophic status of plants. Mikologiâ i Fitopatologiâ 51(6): 350–364. [in Russian]
  • Na QC, Bau T (2019b) Recognition of Mycena sect. Amparoina sect. nov. (Mycenaceae, Agaricales), including four new species and revision of the limits of sect. Sacchariferae. MycoKeys 52: 103–124. https://doi.org/10.3897/mycokeys.52.34647
  • Na Q, Hu YP, Liu ZW, Zeng H, Qi LL, Ding H, Cheng XH, Ge YP (2021) The first reported occurrence of Leucoinocybe (Porotheleaceae, Agaricales) in China: Leucoinocybe lishuiensis sp. nov. from Zhejiang Province. Nova Hedwigia 113(3–4): 453–469. https://doi.org/10.1127/nova_hedwigia/2021/0661
  • Na Q, Hu YP, Zeng H, Song ZZ, Ding H, Cheng XH, Ge YP (2022) Updated taxonomy on Gerronema (Porotheleaceae, Agaricales) with three new taxa and one new record from China. MycoKeys 89: 87–120. https://doi.org/10.3897/mycokeys.89.79864
  • Osmundson TW, Robert VA, Schoch CL, Baker LJ, Smith A, Robich G, Mizzan L, Garbelotto MM (2013) Filling Gaps in Biodiversity Knowledge for Macrofungi: Contributions and Assessment of an Herbarium Collection DNA Barcode Sequencing Project. PLoS ONE 8(4): e62419. https://doi.org/10.1371/journal.pone.0062419
  • Pérez-Izquierdo L, Morin E, Maurice JP, Martin F, Rincón A, Buée M (2017) A new promising phylogenetic marker to study the diversity of fungal communities: The Glycoside Hydrolase 63 gene. Molecular Ecology Resources 2017(6): 1–17. https://doi.org/10.1111/1755-0998.12678
  • Perry BA (2002) A taxonomic investigation of Mycena in California. Doctoral dissertation, San Francisco State University, San Francisco, the United States.
  • Perry BA, Keller HW, Forrester ED, Stone BG (2020) A new corticolous species of Mycena sect. Viscipelles (Basidiomycota: Agaricales) from the bark of a Living American elm tree in Texas, U.S.A. Journal of the Botanical Research Institute of Texas 14(2): 167–185. https://doi.org/10.17348/jbrit.v14.i2.1000
  • Petersen RH, Hughes KW, Lickey EB, Kovalenko AE, Psurtseva V (2008) A new genus, Cruentomycena, with Mycena viscidocruenta as type species. Mycotaxon 105(4): 119–136.
  • Redhead SA, Singer R (1981) Resinomycena gen. nov. (Agaricales), an ally of Hydropus, Mycena and Baeospora. Mycotaxon 8(1): 150–170. [Fungi]
  • Redhead SA, Moncalvo JM, Vilgalys R, Desjardin DE, Perry BA (2012) Index Fungorum: Published Numbers 14: 1–1.
  • Rexer KH (1994) Die Gattung Mycena s.l., Studien zu ihrer Anatomie, Morphologie und Systematik. Eberhard-Karls-Universität Tübingen, Tübingen, Germany, 132 pp.
  • Robich G (2003) Mycena d’Europa. Associazione Micologica Bresadola, Trento, 728 pp.
  • Robich G (2016) Mycena d’Europa Volume 2. Associazione Micologica Bresadola, Trento, 796 pp.
  • Saccardo PA (1887) Sylloge Hymenomycetum, Vol. I. Agaricineae (in Latin). Sylloge Fungorum, Berlin, 1146 pp.
  • Shih YS, Chen CY, Lin WW, Kao HW (2014) Mycena kentingensis, a new species of luminous mushroom in Taiwan, with reference to its culture method. Mycological Progress 13(2): 429–435. https://doi.org/10.1007/s11557-013-0939-x
  • Singer R (1969) Mycoflora Australis. Beihefte zur Nova Hedwigia 29: 110.
  • Singer R, Gomez LD (1982) Basidiomycetes of Costa Rica. Brenesia 19–20: 31–47.
  • Smith AH (1947) North American species of Mycena. University of Michigan Press, Ann Arbor, Michigan, 521 pp.
  • Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: A fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics maximum likelihood-based inference of large phylogenetic trees. Bioinformatics (Oxford, England) 21(4): 456–463. https://doi.org/10.1093/bioinformatics/bti191
  • Terashima Y, Takahashi H, Taneyama Y (2016) The fungal flora in southwestern Japan, Agarics and boletes. Tokai University Press, Kanagawa, Tokyo, 349 pp.
  • Thoen E, Harder CB, Kauserud H, Botnen SS, Vik U, Taylor AF, Menkis A, Skrede I (2020) In vitro evidence of root colonization suggests ecological versatility in the genus Mycena. The New Phytologist 227(2): 601–612. https://doi.org/10.1111/nph.16545
  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 63: 215–228. https://doi.org/10.1093/nar/25.24.4876
  • Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, AlHatmi A, Groenewald JZ, Cardinali G, Houbraken J, Boekhout T, Crous PW, Robert V, Verkley GJM (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom Fungi and reveals thresholds for fungal species and higher taxon delimitation. Studies in Mycology 92(1): 135–154. https://doi.org/10.1016/j.simyco.2018.05.001
  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, Seliger H, Gelfand DH, Sinsky JJ, White TJ (Eds) PCR Protocols: a Guide to Methods and Applications, 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  • Wu LS, Han T, Li WC, Jia M, Xue LM, Rahman K, Qin LP (2013) Geographic and tissue influences on endophytic fungal communities of Taxus chinensis var. mairei in China. Current Microbiology 66(1): 40–48. https://doi.org/10.1007/s00284-012-0235-z