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Research Article
Two new species of Collybiopsis (Agaricales, Omphalotaceae) from Eastern North America
expand article infoRonald H. Petersen‡, Karen W. Hughes‡
‡ University of Tennessee, Knoxville, United States of America

Corresponding author: Karen W. Hughes ( khughes@utk.edu )

Academic editor: Thorsten Lumbsch
© 2024 Ronald H. Petersen, Karen W. Hughes.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Petersen RH, Hughes KW (2024) Two new species of Collybiopsis (Agaricales, Omphalotaceae) from Eastern North America. MycoKeys 107: 95-124. https://doi.org/10.3897/mycokeys.107.122634
Open Access

Abstract

Two small gymnopoid fungi from the southern Appalachian Mountains and Massachusetts, Collybiopsis complicata sp. nov. and C. prolapsis sp. nov., are identified and described. A new generic nrITS-LSU phylogeny of Collybiopsis places C. complicata and C. prolapsis in a small clade together with C. minor, and an unknown taxon from Arkansas. This clade adds to the growing circumscription of Collybiopsis (= Marasmiellus).

Key words

Gymnopus, Marasmiaceae, new species, Omphalotaceae, phylogeny, taxonomy

Introduction

Although the southern Appalachian Mountains of the Eastern United States have been explored by numerous mycologists for the last century, not all agarics have been recorded or described. This is especially true of the Great Smoky Mountains National Park (GSMNP) and adjacent regions where L. R. Hesler, together with visiting workers, collected for much of the 20th century, and where the senior author and additional visitors have collected and described fungi for the past 50 years or more (Hesler 1959; Petersen 1977; Desjardin 1989; Mata et al. 2007). Nonetheless, smaller agarics from this species-rich region often remain overlooked. Especially problematic are small litter- and wood-decomposing agarics that dominate the moist understory of the varied conifer-hardwood forests of the southern Appalachian Mountains. Herein, we name and describe two such fungi within Collybiopsis, C. complicata and C. prolapsis, place them within a larger Collybiopsis phylogeny, and note that while originally identified from the southern Appalachian area, C. complicata, at least, has a wider distribution.

Species within Collybiopsis and Gymnopus were previously included within Collybia s.l., a large polyphyletic genus within the Omphalotaceae consisting of transient basidiomes, convex and often non-striate pilei, variably attached lamellae and robust, non-filiform stipes (compared to Marasmius) (Halling 1983; Wilson and Desjardin 2005; Mata et al. 2007). With the advent of molecular methods of assessing fungal relationships, it became clear that morphology alone was insufficient to delineate modern taxonomic relationships and that traditional genera of small saprobic “collybioid” fungi (Marasmius, Marasmiellus and Collybia) were polyphyletic. Collybia s.s. was segregated from Collybia and remaining taxa were transferred to Gymnopus (“gymnopoid fungi”: (Antonín and Noordeloos 1993, 1997). Wilson and Desjardin (2005) examined nrLSU-based phylogenetic relationships among the gymnopoid and marasmioid fungi and designated two unresolved clades, /gymnopus and /marasmiellus. /Marasmiellus contained the type species of Marasmiellus and was dominated by members of Gymnopus section Vestipedes (stipe surface usually with a vesture, hyphae sometimes diverticulate or coralloid). Mata et al. (2007) used molecular data to examine structure within Gymnopus, arriving at clades A-N of “gymnopoid fungi”, confirming placement of the generic type species of Marasmiellus, Marasmiellus juniperinus, within Gymnopus clade D (Mata et al. 2004). Species within Clade D (/Marasmiellus of Wilson and Desjardin 2005) were transferred to Marasmiellus (Oliveira et al. 2019), then Collybiopsis (Petersen and Hughes 2021). Other gymnopoid taxa were subsequently segregated from Gymnopus including Paragymnopus, Mycetinis (Petersen and Hughes 2017), Paramycetinis (Petersen and Hughes 2020), and Pseudomarasmius (Petersen and Hughes 2020). The most recent treatment of the Omphalotaceae overall which included 191 sequences within the Omphalotaceae showed Mycetinis and Paramycetinis as basal to Marasmiellus and sister to a diverse group of taxa including Lentinula and Rhodocollybia (Petersen and Hughes 2020). The terms “gymnopoid” and marasmielloid” thus refer to taxa that historically belonged to Gymnopus or Marasmiellus (spore print white, stipe central, without volva or annulus; lamellae variously attached) but marasmielloid fungi tend to have pale pilei, prostrate and diverticulate hyphae and cheilocystidia arising from horizontal hyphae in the hymenium. Ultimately, both gymnopoid and marasmielloid fungi are defined molecularly as belonging to Gymnopus or Marasmiellus.

Materials and methods

Macromorphology

Below, colors of basidiomatal structures within quotation marks (“”) are from Ridgway (1912) and matching colors from Kornerup and Wanscher (1967) are cited alphanumerically by plate, column, and row (i.e. “28E5”).

Micromorphology

Observations of microscopic structures were made with an Olympus BX60 research microscope fitted with phase contrast microscopy (PhC). Photos were produced using an Olympus Q-color 5 camera/computer attachment. All micromorphology was accomplished with squash mounts of minute amounts of basidioma tissue in 3% aqueous KOH; in some cases, enough material existed to make a second mount in Melzer’s reagent (cited as IKI) to test for amyloidity.

Molecular procedures

DNA was extracted from either dried herbarium specimens or from cultures grown in PD Broth (24g/l Difco Potato Dextrose: Thermo Fisher Scientific, Waltham, Massachusetts) using an E.N.Z.A HP Fungal DNA kit (Omega Bio-Tek Inc., Norcross, GA). The nrITS (Schoch et al. 2012) and nrLSU regions were PCR-amplified using procedures outlined in Hughes et al. (2020b). Primers ITS1F, ITS4, ITS2, and ITS3 were used in various combinations to amplify the whole nrITS region or fragments of the region (White et al. 1989; Gardes and Bruns 1996). Primers LR0R and LR5 were used to amplify the 5’ end of the nrLSU region (Cubeta et al. 1991). PCR products were confirmed by gel electrophoresis. Five µL of the PCR product were treated with 2ul ExoSAP-IT (Thermo-Fisher Scientific) using the manufacturer’s directions. Sanger dideoxy sequencing reactions were performed using BigDye Terminator 3.1 (Thermo-Fisher Scientific) following manufacturers’ directions but with cycles increased to 35. Sanger sequencing was performed by the University of Tennessee UT Genomics Core, College of Arts and Sciences.

NrITS and nrLSU sequences (Table 1) were concatenated in Geneious R11.1.5 (Geneious 2017) and aligned manually in Aliview (Larsson 2014). The Alignment for Collybiopsis had 177 sequences with 1875 columns, 905 distinct patterns, 605 parsimony-informative sites, and 1172 constant sites. The model of evolution was estimated using Model Finder (Kalyaanamoorthy et al. 2017) in W-IQ Tree (Trifinopoulos et al. 2016) as GTR+F+I+G4. This model was implemented in the generation of a Fast ML tree with 1000 bootstrap replicates, using the web version of IQTree tree (http://iqtree.cibiv.univie.ac.at/) (Fig. 1).

Table 1.
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Collections used in phylogenetic analyses.

Name Location1 Isolate Voucher ITS GenBank Identifier LSU GenBank Identifier Figure
Collybiopsis aff. villosipes Australia: Perth N.L.Bougher NLB470 PERTH:8872252 MT537088 MT537088 Fig. 1
Collybiopsis biforma USA: TN TFB13814 TENN-F-065189 KJ416249 KJ189569 Fig. 1
Collybiopsis biforma USA: NC TFB13890 TENN-F-065586 KJ416248 KJ189570 Fig. 1
Collybiopsis biforma USA: TN GSMNP TFB14250 TENN-F-068108 KJ416246 KJ189568 Fig. 1
Collybiopsis biforma USA: TN, GSMNP TFB14251 TENN-F-068109 KJ416245 KJ189567 Fig. 1
Collybiopsis brunneigracilis Indonesia: Java AWW01 AWW01-SFSU AY639412 no Figs 1, 2
Collybiopsis californica USA: CA DED8372 SFSU-F-024526 MN413337 no Fig. 1
Collybiopsis californica USA: OR iNAT-143113059 no OQ781003 no Fig. 1
Collybiopsis californica USA: WA iNat-29416590 no OK346494 no Fig. 1
Collybiopsis californica USA: CA none SFSU Wright2941 MN413335 no Fig. 1
Collybiopsis californica USA: CA none SFSU Wright 866 MN413336 no Fig. 1
Collybiopsis californica Canada: BC TFB05787 TENN-F-052617 MN413338 no Fig. 1
Collybiopsis complicata USA: Tennessee, GSMNP TFB09168 TENN-F-055766 DQ450029 no Figs 1, 2
Collybiopsis complicata USA: North Carolina, Macon Co. TFB13916 TENN-F-065811 OR500517 OR500517 Figs 1, 2
Collybiopsis complicata as Marasmiellus sp. USA: MA, World’s End, Boston Harbor Islands HUH-F-00964493 FH:BHI-F447 MF161269 no Figs 1, 2
Collybiopsis complicata as Marasmiellus sp. USA: MA, World’s End, Boston Harbor Islands HUH-F-00964494 FH:BHI-F401 MF161247 no Figs 1, 2
Collybiopsis complicata as Marasmiellus sp. USA: MA, World’s End, Boston Harbor Islands HUH-F-00964495 FH:BHI-F034 MF161165 no Figs 1, 2
Collybiopsis confluens USA: NC TFB14075 TENN-F-067822 KP710281 KP710281 Fig. 1
Collybiopsis confluens Germany: Thuringia TFB14114 TENN-F-067864 KP710296 KJ189573 Fig. 1
Collybiopsis confluens Germany: Thuringia TFB14115 TENN-F-067865 KP710292 KJ189578 Fig. 1
Collybiopsis confluens Canada: NB TFB14389 TENN-F-069053 KP710279 KJ189584 Fig. 1
Collybiopsis confluens Canada: NB TFB14409 TENN-F-09073 KP710278 KJ189585 Fig. 1
Collybiopsis dichroa USA: NC TFB01860 TENN-F-048680 MW396869 MW396869 Fig. 1
Collybiopsis dichroa USA: SC TFB05459 TENN-F-051775 MW396868 MW396868 Fig. 1
Collybiopsis dichroa USA: NC, GSMNP TFB09623h1,h2 TENN-F-056584 MW396865-MW396866 MW396865-MW396866 Fig. 1
Collybiopsis dichroa USA:NC TFB10009h1 TENN-F-056721 KY026654 KY026654 Fig. 1
Collybiopsis dichroa USA: NC TFB13873 TENN-F-065569 MW396867 MW396867 Fig. 1
Collybiopsis dichroa USA: TN, GSMNP TFB14111ss1 TENN-F-067859 KY026696 KY026696 Fig. 1
Collybiopsis dichroa USA: TN, GSMNP TFB14111ss2 TENN-F-067859 KY026697 KY026697 Fig. 1
Collybiopsis disjuncta USA: MS TFB14281 TENN-F-068136 KY019643 KY019643 Fig. 1
Collybiopsis disjuncta Type USA: CT TFB14339 TENN-F-069172 KJ416252 PP430330 Fig. 1
Collybiopsis eneficola Canada: Newfoundland 10-09-21AV04 TENN-F-069122 KJ128265 no Fig. 1
Collybiopsis eneficola USA:AK NA MICH:PK6975 KP710270 no Fig. 1
Collybiopsis eneficola USA:AK NA MICH:PK6976 KP710271 no Fig. 1
Collybiopsis eneficola Type Canada: Newfoundland 09-09-26AV13 TENN-F-069123 NR_137613 NG_059502 Fig. 1
Collybiopsis filamentipes Type USA: TN TFB13962 TENN-F-065861 MN897832 MN897832 Fig. 1
Collybiopsis filamentipes Env. Samp. Canada: Alberta KTRF390 NA MG433317 no Fig. 1
Collybiopsis furtiva USA: North Carolina, Highlands DED3973 SFSU-F-024523 MN413339 no Fig. 1
Collybiopsis furtiva Type USA: DED4425 SFSU DED4425 DQ450031 AF042650 Fig. 1
Collybiopsis furtiva USA: North Carolina, Macon Co. DED4584 SFSU-F-024508 MN413340 no Fig. 1
Collybiopsis furtiva USA: North Carolina, Coweeta DED5796h1 SFSU-F-024524h1 MN413341 no Fig. 1
Collybiopsis furtiva USA: North Carolina, Coweeta DED5796h2 SFSU-F-024524h2 MN413342 no Fig. 1
Collybiopsis furtiva USA: GA TFB04796 TENN-F-051097 MN413343 MW396879 Fig. 1
Collybiopsis gibbosa Australia: NT NA MEL:2382838 KP012713 KP012713 Fig. 1
Collybiopsis gibbosa Brazil: Amapa NA URM 90012 KY061202 KY061202 Fig. 1
Collybiopsis gibbosa Brazil: Amapa NA URM 90006 KY061203 KY061203 Figs 1, 2
Collybiopsis hasanskyensis Type Russia: Far Eastern TFB11846 TENN-F-060730 MN897829 no Fig. 1
Collybiopsis hasanskyensis Russia: Far Eastern TFB11847 TENN-F-060731 MN897830 no Fig. 1
Collybiopsis indocta Argentina TFB08605 TENN-F-054944 MW396870 MW396870 Fig. 1
Collybiopsis juniperina Argentina TFB10782 TENN-F-058988 KY026661 KY026661
something wrong Collybiopsis vaillantii USA: TN, GSMNP TFB13739 TENN-F-065155 KY026676 KY026676 Fig. 1
Collybiopsis juniperina USA: LA TFB9889 TENN-F-59540 AY256708 AY256708 Fig. 1
Collybiopsis luxurians Switzerland TBF04283ss10 TENN-F:050619 KJ416240 PP430331 Figs 1, 2
Collybiopsis luxurians USA: LA TFB09121 TENN-F-055748 KY026649 KY026649 Figs 1, 2
Collybiopsis luxurians USA: NC TFB10350 TENN-F:057910 AF505765 not done Figs 1, 2
Collybiopsis luxurians USA: NC TFB14060 TENN-F:067806 MW396871 MW396871 Figs 1, 2
Collybiopsis melanopus Type Indonesia: Java AWW54 SFSU:AWWilson 54 AY263425, NR_137539 AY639422., NG_060624 Fig. 1
Collybiopsis menehune AWW15 SFSU:AWWilson 15 AY263443 AY639424 Fig. 1
Collybiopsis menehune USA: HI TFB11587 DEH2320 DQ450043 no Fig. 1
Collybiopsis menehune India CUH:AM074 KJ778753 no Fig. 1
Collybiopsis menehune Type Indonesia: Java DED5866 SFSU: DED5866 AY263426 no Fig. 1
Collybiopsis mesoamericana Costa Rica REH7379 NYBG REH7379 AF505768 no Fig. 1
Collybiopsis mesoamericana Costa Rica TFB10411 TENN-F-058106 DQ450036 no Fig. 1
Collybiopsis minor USA: South Carolina TFB05434 TENN-F-051792 MW396872 MW396872 Fig. 1
Collybiopsis minor Type USA: TN, GSMNP TFB11930 TENN-F-067806 MN413334, NG_228867 MW396880 Figs 1, 2
Collybiopsis neotropica Costa Rica TFB10416 TENN-F-058113 AF505769 no Fig. 1
Collybiopsis nonnulla USA: MS TFB14278 TENN-F-068133 KY026701 no Fig. 1
Collybiopsis nonnulla USA: MS TFB14492 TENN-F-069193 MW396873 MW396873 Fig. 1
Collybiopsis nonnulla v. attenuatus Cameroon NA RAK369.2 MN930621 no Fig. 1
Collybiopsis nonnulla v. attenuatus Cameroon NA RAK372.2 MN930622 no Fig. 1
Collybiopsis nonnullus v. attenuatus Indonesia: Java AWW05 SFSU: AWWilson05 AY263445 AY639445 Fig. 1
Collybiopsis nonnullus v. attenuatus Indonesia: Java AWW55 SFSU: AWWilson55 AY263446 no Fig. 1
Mycetinis opacus USA: TN BM888 TENN-F-070567 MW396878 no Fig. 1
Mycetinis opacus USA: MS TFB09071 TENN-F-054871 MW396877 MW396877 Fig. 1
Collybiopsis parvula Costa Rica TFB10422 TENN-F-058116 AF505774 no Fig. 1
Collybiopsis parvula Mexico NA SR83-10MX KT697977 no Fig. 1
Collybiopsis parvula Type Costa Rica TFB10419 TENN-F-058113 NR_119584, DQ450060 no Fig. 1
Collybiopsis parvula Costa Rica TFB10421 TENN-F-058115 DQ450061 no Fig. 1
Collybiopsis parvula Costa Rica TFB10425 TENN-F-058119 DQ450062 no Fig. 1
Collybiopsis peronata Belgium, Dinante TFB13743 TENN-F-065121 KY026677 KY026677 Fig. 1
Collybiopsis peronata USA: GA TFB14617 TENN-F-069322 KY026738 KY026738 Fig. 1
Collybiopsis peronata Unknown NA CBS223.37 MH855896 no Fig. 1
Collybiopsis polygramma Puerto Rico TFB09628 TENN-F-056589 DQ450028 no Figs 1, 2
Collybiopsis polygramma Korea TFB12806 SFC20120821-64 KJ609162 no Figs 1, 2
Collybiopsis polygramma Puerto Rico NA PR2542TN AY842954 no Figs 1, 2
Collybiopsis polygramma India NA CUH:AM082 KJ778752 no Figs 1, 2
Collybiopsis polygramma Brazil: Amapa NA URM90015 KY074640 no Figs 1, 2
Collybiopsis polygramma Brazil: Para NA URM90016 KY074641 no Figs 1, 2
Collybiopsis polygramma Brazil: Para NA URM90017 KY074642 no Figs 1, 2
Collybiopsis polygramma China, Hunan NA MHHNU 30912 MK214392 no Figs 1, 2
Collybiopsis polygramma China, Jiangxi NA HFJAU0425 MN258643 no Figs 1, 2
Collybiopsis pseudoluxurians holotype USA: Mississippi TFB14290 TENN-F-068144 KY026702, NR_137863 KJ416242 Figs 1, 2
Collybiopsis pseudoomphalodes Costa Rica REH7348 NYBG REH7348 AF505762 no Figs 1, 2
Collybiopsis pseudoomphalodes Puerto Rico NA PR24TN AY842957 no Figs 1, 2
Collybiopsis peronata Russia: LE-BIN1364 no voucher specimen KY026755 KY026755 Fig. 1
Collybiopsis quercophilia Slovakia TFB14570 TENN-F-069267 KY026729 KY026729 Fig. 1
Collybiopsis quercophilia USA: CA TFB14615 TENN-F-069320 KY026736 KY026736 Fig. 1
Collybiopsis quercophilia USA: CA TFB14616 TENN-F-069321 KY026737 KY026737 Fig. 1
Collybiopsis quercophilia USA: CA NA SFSU:25220 KY026761 KY026761 Fig. 1
Collybiopsis ramealis Belgium BR72_41 BR<BEL>:72-41 MW396875 MW396875 Fig. 1
Collybiopsis ramealis UK: Scotland TFB03772 TENN-F-050509 MN413350 MW396885 Fig. 1
Collybiopsis ramealis UK: Scotland TFB06989 TENN-F-055908 MN413372 MW396883 Fig. 1
Collybiopsis ramealis Sweden TFB13520 TENN-F-062867 JF313670 OR500520 Fig. 1
Collybiopsis ramealis Belgium TFB13759 TENN-F-065136 MN413344 MN413344 Fig. 1
Collybiopsis ramealis Belgium TFB13769 TENN-F-065145 MN413345 MN413345 Fig. 1
Collybiopsis ramealis Germany TFB14140c1 TENN-F-067890 MN413355 OR500518 Fig. 1
Collybiopsis ramealis Germany TFB14150c1 TENN-F-067900c1 MN413363 OR500519 Fig. 1
Collybiopsis ramealis Germany TFB14163h1 TENN-F-067912 MN413351 MN413351 Fig. 1
Collybiopsis ramealis Germany TFB14163h2 TENN-F-067913 MN413352 MN413352 Fig. 1
Collybiopsis ramealis Slovakia TFB14555 TENN-F-069251 MW405779 MW396884 Fig. 1
Collybiopsis ramealis Slovakia TFB14556 TENN-F-069252 MN413369 MN413369 Fig. 1
Collybiopsis ramealis Slovakia TFB14559h1 TENN-F-069255h1 MN413370 PP430332 Fig. 1
Collybiopsis ramealis Slovakia TFB14559h2 TENN-F-069255h2 MN413371 PP430332 Fig. 1
Collybiopsis readiae New Zealand TFB07571 TENN-F-053687 DQ450034 no Fig. 1
Collybiopsis readiae New Zealand: Buller District TFB13056 TENN-F-061061 KJ416244 no Fig. 1
Collybiopsis readiae New Zealand NA PDD: 95844 HQ533036 no Fig. 1
Collybiopsis sp. Australia: Christmas Island N.L.Bougher NLB 1292 PERTH:08827494 ON715771 ON715771 Fig. 1
Collybiopsis sp. (Gymnopus sp. 17) USA: CT TFB14334h1 TENN-F-068185 KY026707 KY026707 Fig. 1
Collybiopsis sp. (Gymnopus sp. 17) USA: CT TFB14334h2 TENN-F-068185 KY026708 KY026708 Fig. 1
Collybiopsis sp. “prolapsis” USA: Georgia TFB04800 TENN-F-051101 MW396874 MW396874 Figs 1, 2
Collybiopsis sp. (Gymnopus sp.) USA: WV NA WRW05-1170 KY026764 KY026764 Fig. 1
Collybiopsis sp. (VC-2017f) Brazil: Paraiba NA URM 90043 KY321573 KY321573 Figs 1, 2
Collybiopsis sp. (VC-2017f) Brazil: Paraiba NA URM 90042 KY321574 KY321574 Figs 1, 2
Collybiopsis sp. (VC-2017f) Brazil: Paraiba NA URM 90045 KY321575 KY321575 Figs 1, 2
Collybiopsis sp. (VC-2017f) Brazil: Para NA URM 90051 KY321568 KY321568 Fig. 1
Collybiopsis sp. (VC-2017f) Brazil: Para NA URM 90053 KY321570 KY321570 Fig. 1
Collybiopsis sp. Env. Samp. USA: California Environmental Sample none DQ273359 no Fig. 1
Collybiopsis stenophylla USA: North Carolina, Macon Co. TFB11558 TENN-F-059443 DQ450032 no Fig. 1
Collybiopsis stenophylla USA: North Carolina, Macon Co. TFB11559 TENN-F-059444 DQ450033 no Fig. 1
Collybiopsis stenophylla USA: Georgia TFB04798 TENN-F-051099 MN413330 MW396879 Fig. 1
Collybiopsis stenophylla Belgium TFB13770 TENN-F-065146 MN413346 MW396882 Fig. 1
Collybiopsis stenophylla USA: Tennessee, GSMNP TFB13998 TENN-F-065943 MN413331 MW396886 Fig. 1
Collybiopsis subcyathiformis Brazil: Para NA URM90023 KY404982 KY404982 Fig. 1
Collybiopsis subcyathiformis Brazil: Para NA URM 90022RNA KY404983 KY404983 Fig. 1
Collybiopsis subnuda USA: TN, GSMNP TFB12577 TENN-F-061138 KY026667 FJ750262 Fig. 1
Collybiopsis subnuda USA: NC, Macon Co. TFB14043 TENN-F-065984 MW396876 MW396876 Fig. 1
Collybiopsis subnuda USA: WV NA WRW08-462 KY026765 KY026765 Fig. 1
Collybiopsis trogioides Type Indonesia: Java AWW51 AWW51-SFSU NR_152884 NG_228715 Fig. 1
Collybiopsis vaillantii USA: TN, GSMNP TFB13739 TENN-F-065115 KY026676 KY026676 Fig. 1
Collybiopsis velosipes USA: CA TFB09539 TENN-F-056252 DQ450058 no Fig. 1
Collybiopsis villosipes New Zealand: Fiordland TFB12836 TENN-F-060951 KJ416255 FJ750264 Fig. 1
Collybiopsis villosipes USA: CA inaturalist.org/observations/2708886 NA MF163171 no Fig. 1
Collybiopsis minor USA: South Carolina TFB06284 TENN-F-052933 MW405778 MW396881 Fig. 1
Environmental Sample USA: Oregon clone FON_f09 none HM488468 no Fig. 1
Environmental Sample-soil USA: Oregon clone FON_h10 none HM488469 no Fig. 1
Gymnopanella nothofagi Chile: Aisen PSL 411 SGO163624 KT906426 KT906426 Fig. 1
Gymnopanella nothofagi Chile: Aisen PSL 414 SGO163625 KT906425 KT906425 Fig. 1
Collybiopsis obscuroides Sweden: Jamtland NA GB-0053811 KX958398 KX958398 Fig. 1
Collybiopsis obscuroides Norway: Svalbard NA GB-0150514 KX958399 KX958399 Fig. 1
Gymnopus peronata Canada: BC NA UBC F28402 KP454027 no Fig. 1
Gymnopus sp. (VC-2017k) Brazil: Paraiba NA URM 90054 KY404984 KY404978 Fig. 1
Gymnopus sp. Japan: Okinawa Ns8-1 none LC504922 no Fig. 1
Gymnopus sp. (root sample) Sweden olrim406 none KY352520 no Fig. 1
Gymnopus sp. USA: MS, Boston Harbor Islands BHI-F523a FH:BHI-F523a MF161290 no Fig. 1
Gymnopus sp. (Not in Collybiopsis paper) Costa Rica TFB10494 TENN-F-058602 KY026660 no Fig. 1
Marasmiaceae sp. USA: FL NA FLAS-F-69007 OP163218 no Fig. 1
Marasmiellis sp. USA: Arkansas RA7L5-13a (leaf litter) none MK234195 no Figs 1, 2
Marasmiellus foliiphila India none CUH AM090 KP317637 no Fig. 1
Marasmiellus foliiphila India none CUH AM101 KP317638 no Fig. 1
Marasmiellus sp. Mexico: Oaxaca P196 (soil) NA KR135355 no Fig. 1
Marasmiellus sp. USA: 14147 NA MW023100 no Fig. 1
Mycetinis copelandii USA: CA TFB08084h1 TENN-F-55408 haplotype h1 KY696750 KY696750 Fig. 1
Mycetinis copelandii USA: CA TFB08084h2 TENN-F-55408 haplotype h2 KY696751 KY696751 Fig. 1
Mycetinis kallioneus Norway: Svalvard NA GB-0150513 KX958397 KX958397 Fig. 1
Mycetinis opacus USA: MS TFB14490h1 TENN-F-069200 h1 KY696768 KY696768 Fig. 1
Mycetinis opacus USA: MS TFB14490h2 TENN-F-069200 h2 KY696769 KY696769 Fig. 1
Mycetinis salalis Canada: BC, Vancouver Island NA DAOM:175251 KX752265 KX752265 Fig. 1
Mycetinis scorodonius Sweden TFB03785 TENN-F-050522 KY696731 KY696731 Fig. 1
Mycetinis scorodonius USA: NC TFB03071 TENN-F-050689 KY696733 KY696733 Fig. 1
Mycetinis scorodonius USA: TN, GSMNP TFB03708 TENN-F-050696 KY696734 KY696734 Fig. 1
Mycetinis scorodonius Canada: Nova Scotia TFB05031 TENN-F-051442 KY696739 KY696739 Fig. 1
Mycetinis scorodonius USA: NY TFB04969 TENN-F-053466 KY696741 KY696741 Fig. 1
Mycetinis scorodonius Canada: Nova Scotia TFB05025 TENN-F-053467 KY696742 KY696742 Fig. 1
Mycetinis scorodonius USA: NT TFB04939 TENN-F-053471 KY696746 KY696746 Fig. 1
Mycetinis scorodonius USA: ME TFB05005 TENN-F-053474 KY696748 KY696748 Fig. 1
Paramycetinis austrobrevipes Australia: Tasmania TFB03585 TENN-F-053181 KY026638 KY026638 Fig. 1
Paramycetinis austrobrevipes Australia: Tasmania TFB03591 TENN-F-053146 KY026637 KY026637 Fig. 1
Paramycetinis austrobrevipes Type Australia: Tasmania TFB04033 TENN-F-050135 KY026622 KY026622 Fig. 1
Paramycetinis caulocystidiatus Type New Zealand TFB07148 TENN-F-054050 KY026645 KY026645 Fig. 1
Paramycetinis caulocystidiatus New Zealand TFB07572 TENN-F-053683 KY026642 KY026642 Fig. 1
Paramycetinis caulocystidiatus New Zealand TFB07588 TENN-F-053721 KY026643 KY026643 Fig. 1
Paramycetinis caulocystidiatus New Zealand TFB07589 TENN-F-053725 KY026644 KY026644 Fig. 1
Collybiopsis melanopus Not Indicated NA CUH AM093 KP100305 KP100305 Fig. 1
Collybiopsis mesoamericana Type Costa Rica TFB11005 TENN-F-058613 NR_119583 KY019632 Fig. 1
Collybiopsis folliphilia Type India NA CUH:AM090 NR_154176 NG_060320 Fig. 1
Figure 1. 

nrITS-nrLSU based Maximum Likelihood consensus tree with 1000 bootstrap replicates. The tree was generated using the web version of IQTree tree (http://iqtree.cibiv.univie.ac.at/) using the best-fit model of evolution (GTR+F+I+G4, AIC criteria). Colors represent branch bootstrap support. Red = 95–100% bootstrap support, Purple = 90–94.9% bootstrap support, Blue = 80–89.9% bootstrap support, Aqua = 70–79.9% bootstrap support and Green = 60–69.9 bootstrap support.

In addition, Bayesian analysis was performed on the Collybiopsis alignment in Geneious 11.1.5 using the MrBayes plugin (Huelsenbeck and Ronquist 2001) with a GTR model of evolution (4 Gamma Categories, nst=6, and basefreq=estimated). The MCMC search was carried out with 4 chains for 1,100,000 generations with sampling every 1000 generations. The first 100,000 trees were discarded when likelihood values had reached convergence. Convergence was assessed by ensuring that the average standard deviation of split frequencies was below 0.01. Posterior probabilities were estimated by sampling trees generated after likelihood values had reached equilibrium.

The alignment for the C. complicata subgroup contained 34 sequences with 366 distinct patterns, 182 parsimony-informative sites and 1510 invariant sites. The best-fit model of evolution was estimated using Model Finder in W-IQ-Tree as TIM2+F+I+G4. This model was implemented in the generation of a Fast ML tree with 1000 bootstrap replicates, using the web version of IQTree tree (http://iqtree.cibiv.univie.ac.at/) (Fig. 2). Bayesian analysis was performed as described above.

Figure 2. 

NrITS-nrLSU based Maximum Likelihood consensus tree of the C. complicata/C. prolapsis clade with 1000 bootstrap replicates. The tree was generated using the web version of IQTree tree (http://iqtree.cibiv.univie.ac.at/) using the best-fit model of evolution (TIM2+F+I+G4, AIC criteria). Included taxa were selected based on the Bayesian analysis which showed the C. complicata group and the C. ramealis group as sister taxa. Bootstrap support is indicated below the branches and Bayesian Posterior probabilities above the branches.

Taxa used in both analyses are given in Table 1. Collections retained at TENN have both a field number (TFB = Tennessee Field Book) and a TENN accession number (TENN-F-XXXXXX).

Results

The phylogenetic position of C. prolapsis and C. complicata within Collybiopsis varies between Maximum Likelihood and Bayesian analyses. In Maximum Likelihood analysis, the C. prolapsis/C. complicata clade is sister to a large clade containing elements of Collybia sects. Subfumosae/Vestipedes (Fig. 1.). In Bayesian analysis, the C. prolapsis/C. complicata clade is sister to a clade containing C. ramealis. This is the only major difference between the topologies of the two phylogenetic analyses. Other differences include minor differences in the position of Gymnopus sp. 17, an unnamed Collybiopsis, and C. quercophilia. The nrITS sequences for collections within C. complicata (Table 1) are genetically identical with the exception of a 1bp C/T transition in TENN-F-065811 (0.17% difference). In contrast, GenBank accession OR500517 has 6 differing base pairs (1.05%).

The pileipellis structure of C. prolapsis and C. complicata is similar to that of the infrageneric Collybia sects. Subfumosae and Vestipedes (Halling 1983) on the one hand, and to the cheilocystidial structure of these two species to the Collybiopsis ramealis group (Petersen and Hughes 2021) on the other. Cheilocystidial morphology also comes close to that of C. minor, somewhat morphologically disjunct from the C. ramealis group. In all cases, however, molecular sequences clearly separate the C. ramealis clade, the C. complicata/prolapsis clade and the Collybiopsis subfumosae/vestipedes clade.

Taxonomy

Collybiopsis complicata R.H. Petersen, sp. nov.

Index Fungorum: IF901185
Figs 3, 4, 5, 6, 7, 8, 9, 10, 11

Holotype

Tennessee, Blount Co., Great Smoky Mountains National Park, Metcalf’s Bottoms Picnic Area, 9.VI.1997, coll. Ronald H. Petersen, TFB 9168 (TENN-F-055766).

Diagnosis

1) Basidiomata marasmielloid/gymnopoid, gracile, small, with slender stipe; 2) pileus pigmented, especially over disc; 3) pileipellis composed of stalked-coralloid structures and lobed repent hyphae; 4) stipe fully vestured; 5) clamp connections present; 6) cheilocystidia prominent, similar to pileipellis elements; 7) basidiospores 5–8 × 3–4 µm.

Etymology

Cheilocystidia with complex, branched structure; also complex distribution, from southern Appalachians to New England.

Description

Basidiomata (Fig. 3) scattered-gregarious >50 basidiomata in <12 m, marasmielloid or miniature collybioid. Pileus 6–14 mm broad, shallowly convex to plane by maturity, matt, delicately rivulose-striate; disc “snuff brown” (5E8), outward “sayal brown” (6C5) to fleshy tan. Lamellae free to adnexed but seceding in drying to become removed from stipe apex, total lamellae 47–64; through lamellae 24–26, in two major ranks with no anastomosis, 1.5–2 mm broad, subventricose to ventricose by maturity, knife-edged, dull pale tan-gray (near “tilleul buff” 7B2), bleaching to off-white, often (but not exclusively) becoming pale cream-colored with necropigment; lamellulae in one rank, less than ½ the length through lamellae. Stipe 7–30(–45) × 0.7–1.2 mm, terete and remaining so upon drying, minutely vestured overall, somewhat darker than lamellae apically, downward fleshy tan to fleshy brown, drying matt; vesture on upper stipe of scattered delicate squamules composed of individual caulocystidia, on lower stipe a solid turf (but never felty), straw-colored to “light ochraceous buff” (5A4); insertion insititious on fine twigs and leaves; superficial litter-binding mycelium not observed. Odor and taste negligible.

Figure 3. 

Collybiopsis complicata. Basidiomata. TFB 13916 (TENN-F-065811). Scale bar: 10 mm.

Pileipellis a thatch of occasional repent encrusted hyphae (Fig. 4) and dominant interlocking, stalked-lobose pileocystidia and lobed-diverticulate, repent hyphae (Fig. 5B, C); Pileocystidia (Figs 5A, D) 27–37 × 5–14 µm, stalked, branching in lobose-coralloid configurations, apparently hyaline, thin- to firm-walled, arising from clamp connections. Subsurface pileipellis hyphae 2.5–10 µm diam, firm-walled, conspicuously clamped, ornamented with small flakes (in profile) but no profile calluses or stripes. Pleurocystidia (Fig. 6) common, arising from clamp connections, 32–40 × 7–9 μm, stalked-fusiform with apex often broadly submammillate; contents homogeneous. Basidioles clavate. Basidia (Fig. 7) 35–60 × 7–9 µm, clavate to weakly urniform or with somewhat expanded subcapitate apex, (2–)4–sterigmate, arising from clamp connections; sterigmata robust, slightly curved; contents heterogeneous, with scattered, refringent granules. Basidiospores (Fig. 8B) (5.5–)6.5–8.5(–10) × 3–4(–5) µm (Q = 1.56–2.50; Qm = 2.03; Lm = 8.02 µm), ellipsoid, flattened adaxially, thin-walled, inamyloid; contents (dried) homogeneous. Lamellar edge sterile. Cheilocystidia (Figs 9, 10) plentiful, 25–40 × 4–15 µm, stalked, lobose-coralloid branched, often with diverticulate-lobed termini, hyaline, thin-walled. Stipe medullary hyphae 4–14 μm diam, strictly parallel, free (not involved in slime matrix), firm-walled, inconspicuously clamped; contents heterogeneous (multigranular). Stipe cortical hyphae 3–5 µm diam, apparently adherent, obscurely clamped, moderately dextrinoid (more or less hyaline without IKI, reddish brown with IKI), firm- to thick-walled (wall –0.8 μm thick), clamped, producing side branches elongating into caulocystidia. Caulocystidia from upper stipe (Figs 8 A, 11) in delicate, interrupted patches –80 × 4–10 µm, cylindrical to vermiform, usually somewhat gnarled distally with broadly rounded apex, thick-walled (wall often occluding cell lumen), arising as non-septate side branches from slender (1.5–3.5 µm diam, wall –1.0 µm thick), superficial stipe surface hyphae, strongly dextrinoid (dark brownish red with IKI). Caulocystidia from lower stipe similar, a dense turf of free individuals (not involved in slime matrix), weakly to strongly dextrinoid, –200 × 3–8 µm, thick-walled (wall/lumen distinction often impossible in IKI; wall –1.0 µm thick, less dextrinoid than cell contents), tapering gradually to an acutely rounded apex, often gnarled and sometimes forked. Ample evidence of clamp connections in pileipellis, subpellis and pileus trama (i.e. hook cells of disarticulated clamps common and obvious) occasional complete clamps observed at basidial bases.

Figure 4. 

Collybiopsis complicata. Pileipellis elements; repent, encrusted hyphae. Sx TFB 9168 (TENN-F-055766). Scale bars: 10 mm.

Figure 5. 

Collybiopsis complicata. Pileipellis elements; pileocystidia A cluster of pileocystidia B, C “Diverticulate” repent hyphae D two lobose hyphal termini. Note clamp connections. TFB 9168 (TENN-F-055766). Scale bars: 10 μm.

Figure 6. 

Collybiopsis complicata. Pleurocystidia Note clamp connection in C. TFB 9168 (TENN-F-055766). Scale bars: 10 μm.

Figure 7. 

Collybiopsis complicata. Basidia. TFB 9168 (TENN-F-055766). Scale bars: 10 μm.

Figure 8. 

Collybiopsis complicata A Caulocystidia B Basidiospores. TFB 9168 (TENN-F-055766). Scale bars: 10 μm (A); 5 μm (B).

Figure 9. 

Collybiopsis complicata. Individual cheilocystidia. TFB 9168 (TENN-F-055766). Scale bars: 10 μm.

Figure 10. 

Collybiopsis complicata. Clusters of cheilocystidia. HUH. HUH-F-00964494. Scale bars: 10 μm.

Figure 11. 

Collybiopsis complicata. Caulocystidia. TFB 9168 (TENN-F-055766) A caulocystidia from upper stipe B, C, D individual caulocystidia. Scale bars: 10 μm.

Habitat

Tsuga debris and adjacent hardwood leaves.

Specimens examined

Massachusetts, Plymouth County, Boston Harbor, World’s End Peninsula, coll LA Kappler, 23.VIII.2015, (HUH) BHI 447 (HUH-F-00964493), Boston Harbor, World’s End Peninsula, Rocky Neck, coll D. Healewaters & LA Kappler, 12.VIII.2015, (HUH) BHI 401 (HUH-F-00964494); World’s End Peninsula, coll D. Healewaters et al., 14.IX.2013, (HUH) BHI 034 (HUH-F-00964495. North Carolina, Macon Co., vic. Highlands, Bull Pen Rd., Ellicott Rock Trailhead, 35°01.010'N, 83°08.190'W, 20.VII. 2011, coll RHP, TFB 13916 (TENN-F-065811). Tennessee, Blount Co., GSMNP, Metcalf’s Bottoms Picnic Area, 9.VI.1997, coll. RHP, TFB 9168 (TENN 55766).

Commentary

The strongly modified “Rameales-structure” of the pileipellis structures of C. complicata resembles that of species of traditional Marasmiellus [viz. C. ramealis complex, (Petersen and Hughes 2021)]. This construction comprises a thatch of stalked, ventricose-rostrate structures with lobose, molar-shaped outgrowths. These pileipellis structures conform closely to those of Marasmiellus sect. Dealbati subsect. Dealbatini sensu Singer (Singer 1973) [Type = Marasmius dealbatus Berk. & Curt.], of which Marasmius stenophylla (C. stenophylla, Fig. 2) is a member (Desjardin 1997). M. stenophylla (section Dealbati) was transferred to Gymnopus sensu lato (Mata et al. 2004), then to Collybiopsis (Petersen and Hughes 2021). Both Desjardin (Desjardin 1989; 1997) and Hesler (1959) examined type material of M. subsynodicus Murrill, considered by Singer (Singer 1973) and Desjardin (Desjardin 1997) to be synonymous with M. stenophylla (Mont.) Singer). Marasmius dealbatus remains unplaced in modern classifications.

Parenthetically, in C. complicata collections TENN-F-055766 and HUH-F-00964493, the lobose individual pileipellis elements dominated the pileipellis, while in TENN-F-065811 (also C. complicata), these structures were only occasional in a pileipellis dominated by encrusted filamentous hyphae.

The pileipellis structure of Marasmius Sect. Androsacei (= Gymnopus sect. Androsacei, see Noordeloos and Antonín (2008), is also described as a combination of diverticulate, repent hyphae and siccus-type broom cells (a “Rameales-structure”). Our experience with this, however, indicates that the diverticulae (= setulae) of pileipellis cells are much finer, usually vermiform, refringent (PhC) and <1 µm broad. Cheilocystidia of C. complicata are very similar to pileipellis structures, but as a rule are somewhat less complexly branched. Morphologically, the pileipellis of C. complicata might be forced into section Androsacei, but phylogenetically, it is distant from that group in Gymnopus S.S.

Mata et al. (2007) initially designated TENN-F-055766 (GenBank DQ450029, C. complicata) as Marasmiellus sp. aff. pluvius, but while basidiomata of Marasmiellus pluvius Redhead (Redhead 1982) have similar stature, they are smaller and are gregarious on Pseudotsuga and Thuja needle beds in southern British Columbia. Further, the pileipellis of Ma. pluvius does not include stalked-lobose structures, but is a “compactly interwoven layer of densely diverticulate hyphae” (Redhead 1982); “Rameales-structure”). Cheilocystidia of Ma. pluvius are stalked-vesciculose to clavate with narrow, vermiform setulae quite similar to those of the Ma. ramealis complex. Basidiospores of Ma. pluvius are longer and significantly narrower than those of C. complicata and caulocystidia exhibit a significantly thicker wall than those of C. complicata. While perhaps morphologically congeneric with C. complicata in Collybiopsis, the two species are quite different microscopically and a second GenBank accession under the name Marasmiellus aff. pluvius (MK277736; NL-5034: nrLSU sequence only) is 0.22% different from other C. complicata nrLSU sequences. Marasmiellus pluvius has not yet been transferred to Collybiopsis, but DNA sequences will probably support such transfer when they become available, although specific placement in a phylogeny remains unknown.

The nrITS sequences for collections within C. complicata (Table 1) are genetically identical with the exception of a 1bp C/T transition in TENN-F-065811 from Macon County, GA (0.17% difference). This lack of nrITS variation includes three nrITS sequences of specimens collected in a study of Boston (MA) Harbor Islands (Haelewaters et al. 2018), and one from the Great Smoky Mountains National Park TENN-F-055766. Collybiopsis complicata, therefore, seems distributed extensively in temperate Eastern North America. The nearest taxon to C. complicata, GenBankaccession MK234195, differs by 6 base pairs (1.05%) and while this falls within the commonly accepted criteria of 2% divergence for conspecificity (Hughes et al. 2009), the lack of variation within C. complicata across a wide geographic range (Boston Harbor Islands vs. Southern Appalachians) argues that C. complicata does not include MK234195. Possibly, C. complicata is a recently-diverging taxon that has not accumulated geographical differences.

Collybiopsis prolapsis

Index Fungorum: IF902313
Figs 12, 13, 14, 15, 16, 17, 18, 19

Holotype

United States, Georgia, Rabun Co., vic. Clayton, Warwoman Dell Picnic Area, 34°52'57.81"N, 83°20'57.99"W, 15.VI.1992, coll. Scott A. Gordon, TFB 4800 (TENN-F-051101).

Diagnosis

1) Basidiomata diminutive, collybioid or marasmielloid, saprophytic on hardwood litter; 2) clamp connections ubiquitous; 3) cheilocystidia “prolapsed,” similar to “ramealis” type, with an abrupt bouquet of branched diverticula; 4) stipe without vesture (i.e. not similar to Gymnopus sect. Vestipedes; 5) resupinate patch significant, with diminutive, white hyphal ropes; 6) necropigment weak over hymenophore; 7) nrITS sequence unique, but quite similar to that of C. complicata and C. minor.

Etymology

Pileo- and cheilocystidia structures with swollen, subspherical excrescences, reminiscent of a prolapse.

Description

Basidiomata diminutive (Fig. 12). Pileus 8–12 mm broad, when fresh rich deep brown (6E6-7, “Brussels brown,” “Sudan brown”), shallowly convex to plane, very vaguely finely sulcate, minutely radially fibrillose; drying grayish brown, more or less unicolorous. Lamellae subdistant, adnate (with very slight non-lamellate hymenium decurrent on stipe apex for less than a millimeter), not ventricose (straight from stipe to margin), total lamellae 30–40, through lamellae 4–10, “off-white” to “cream” to “brown orange”, 6C4 in age; lamellulae rudimentary. Stipe when fresh reported as concolorous with pileus, when dried more or less concolorous with lamellae, terete, hardly twisted, glabrous-shining to somewhat wispy very near base; stipe base with extensive (–1.5 sq cm) resupinate patch, now creamy off-white and appearing varnished and with a few small, off-white synnematoid mycelial ropes. Odor and taste not recorded.

Figure 12. 

Collybiopsis prolapsis A basidioma B basidiospores, Scale bars: 8 mm (A); 5 µM (B).

Pileipellis a repent layer of free (with no evidence of slime matrix or individual slime sheath), filamentous hyphae of the following types: 1) dermatocystidia (Fig. 13) clavate to fusiform to inflated and tapering distally, 7–11.5 μm diam, smooth (Fig. 13A, B) to ornamented in annular pattern (Fig. 13C, E), apparently arising at a clamp connection; contents homogeneous to heterogeneous with scattered inclusion (Fig. 13D); 2) repent hyphae 3.5–8 μm diam, thin- to firm-walled, varying as follows: a) minutely roughened (Fig. 14A); b) ornamented with individual scabs, flattened in flake-like scales, individual lumps –2 μm high (Fig. 14B), spiculate structures (Fig. 14C) and/or annular ornamentation with profile calluses (Fig. 14D); 3) smooth, repent hyphae 3.5–7.5 μm diam, with occasional filamentous side branches (Fig. 15A–C); branches simple, lobate to branched, not arising from clamp connections; and 4) thick-walled, usually somewhat inflated hyphae 5.5–10.5 μm diam, with thick-walled cog-like warts, 1.5–2.5 × 1–2.5 μm (Fig. 16A, B); intermediate forms (Fig. 16C) occasional. Pileal and lamellar tramae interwoven; hyphae 3–8.5 μm diam, firm-walled, frequently and conspicuously clamped, in lamellar trama with slender hyphae 2–3.5 μm diam. Pleurocystidia (Fig. 17) 24–34 × 7–11 μm, abundant, stalked-fusiform, near lamellar edge ampulliform with rounded apex, conspicuously clamped; contents homogeneous to heterogeneous with crystal-like inclusions. Basidia (Fig. 18) more or less stalked-columnar (not urniform, not clavate), 27–35 × 8–12 μm, 4-sterigmate (sterigmata slender, slightly curved), conspicuously clamped; contents homogeneous to minutely heterogeneous. Basidiospores (Fig. 12B) (9–)9.5–10.5 × 4–4.5(–5) μm (Q = 2.10–2.50; Qm = 2.05; Lm = 9.75 μm), elongate-ellipsoid, somewhat tapered proximally, thin-walled, hyaline; contents homogeneous to heterogeneous-subrefringent. Cheilocystidia (Fig. 19 A–G) ventricose-rostrate to stalked-globose, hyaline, firm- to thick-walled (wall –1 μm thick, especially laterally, smooth), conspicuously clamped, apically producing a cluster of diverticula; diverticula –16 × 1–2.5(–4) μm, repeatedly dichotomously branched, often inflated somewhat apically (Fig. 19 A, B). Stipe medullary hyphae thick-walled, occasionally conspicuously clamped, of two types: 1) 4.5–8.5 μm diam, seldom branched; contents heterogeneous (multigranular); and, 2) 2–3.5 μm diam, occasionally branched; contents homogeneous. Stipe cortical hyphae similar to slender medullary hyphae. Resupinate patch composed of tightly interwoven hyphae in a slime matrix; hyphae of two types, both inconspicuously clamped: 1) 3–5.5 μm diam, thick-walled (wall –1 μm thick, refringent; PhC); and 2) 2.5–4 μm diam, thick-walled (wall –0.7 μm thick, non-refringent), frequently branched.

Figure 13. 

Collybiopsis prolapsis. Dermatocystidia. Scale bars: 10 µM.

Figure 14. 

Collybiopsis prolapsis. Repent pileipellis hyphae. Scale bars: 5 µM.

Figure 15. 

Collybiopsis prolapsis. Smooth, repent hyphae with ‘Subfumosae’ side branches. Scale bars: 5 µM.

Figure 16. 

Collybiopsis prolapsis. Dermatocystidia, thick-walled, inflated, often ornamented. Scale bars: 7.5 µM.

Figure 17. 

Collybiopsis prolapsis. Pleurocystidia. Scale bars: 30 uM.

Figure 18. 

Collybiopsis prolapsis. Basidia. Scale bars: 30 uM.

Figure 19. 

Collybiopsis prolapsis. Cheilocystidia. Clusters with diverticula (A, B) Individual Cheilocystidia (C–G).Scale bars: 16 uM (A, B).

Commentary

Specimen notes on undried specimens for the holotype specimen, TENN-F-051101, report lamellae as brownish-orange (6C4) in age. Similar pigmentation is currently evident on dried material, presumably a necropigment (approximately “Light ochraceous salmon,” “Light salmon orange,” more or less characteristic of the Collybiopsis ramealis complex.)

The pileipellis is a poorly developed Gymnopus structure (Hughes and Petersen 2015), with only a few “diverticulate” hyphal termini as described by Halling (1983); typical of section Subfumosae. Conversely, the typical Ramealis pileipellis structure is quite different. There, the typical diverticula are cog-like (not wart-like) and the surrounding hyphal walls thickened (vaguely similar to those shown in Fig. 16A, B). Clamp connections are common and conspicuous throughout. The thick walls of stipe medullary hyphae appears to be laminate, often peeling into narrow shards (as in peeling a banana).

Cheilocystidia, while highly distinctive, are not totally unique. Collybiopsis straminipes cheilocystidia are similar, but the specimens examined (Desjardin and Petersen 1989, including the type) were clampless and from spruce-fir zone. A clamped variety (Marasmius straminipes var. fibulatus Desjardin & R.H. Petersen) is from lower elevation and hardwood (Quercus litter) substrate.

Discussion

The fragmentation and rearrangement of the agaricoid Omphalotaceae, Marasmius and Marasmiellus is ongoing as molecular data identifies new taxa and associations (Owings and Desjardin 1997; Wilson and Desjardin 2005; Matheny et al. 2006; Mata et al. 2007; Hughes and Petersen 2015; Petersen and Hughes 2016; Petersen and Hughes 2017; Petersen and Hughes 2021). This understudied group of small gymnopoid mushrooms will continue to enlarge as environmental studies identify new members and define their niches.

Acknowledgements

We thank the National Park Service Great Smoky Mountains National Park for collecting permits. We also thank Drs. Tom May and Andrew Methven for their considerable time and effort in reviewing this manuscript.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

We thank the National Science Foundation (NSF DEB-9978011) for funding the field work underlying this manuscript.

Author contributions

Karen W. Hughes: Molecular characterizations, phylogenetic analysis, wrote parts of paper. Ronald H. Petersen: Morphological analyses, wrote parts of paper.

Author ORCIDs

Ronald H. Petersen https://orcid.org/0000-0002-3170-5770

Karen W. Hughes https://orcid.org/0000-0003-2865-8798

Data availability

All of the data that support the findings of this study are available in the main text.

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