MYCOTAXON
THE INTERNATIONAL JOURNAL OF FUNGAL TAXONOMY & NOMENCLATURE
VOLUME 136 (2) APRIL-JUNE 2021
a
Entyloma eranthidis sp. nov. on Eranthis longistipitata (Denchev & al.— Fie. 2, p. 379)
ISSN (PRINT) 0093-4666 https://doi.org/10.5248/136-2 ISSN (ONLINE) 2154-8889 MYXNAE 136(2): 253-544 (2021)
EDITORIAL ADVISORY BOARD
ELSE C. VELLINGA (2019-2022), Chair Berkeley, California, U.S.A.
KAREN HANSEN (2014-2021), Past Chair Stockholm, Sweden
XINLI WEI (2019-2023)
Beijing, China
Topp W. OsMUNDSON (2019-2024)
La Crosse, Wisconsin, U.S.A.
ELAINE MALosso (2019-2025)
Recife, Brazil
ALFREDO JUSTO (2021-2026) Saint John, New Brunswick, Canada
ISSN 0093-4666 (PRINT) ISSN 2154-8889 (ONLINE)
MYCOTAXON
THE INTERNATIONAL JOURNAL OF FUNGAL TAXONOMY & NOMENCLATURE
APRIL-JUNE 2021
VOLUME 136 (2)
http://dx.doi.org/10.5248/136-2
EDITOR-IN-CHIEF
LORELEI L. NORVELL editor@mycotaxon.com
Pacific Northwest Mycology Service 6720 NW Skyline Boulevard Portland, Oregon 97229-1309 USA
NOMENCLATURE EDITOR
SHAUN R. PENNYCOOK PennycookS@LandcareResearch.co.nz
Manaaki Whenua Landcare Research Auckland, New Zealand
MyYcoTAxon, LTD. © 2021
www.mycotaxon.com & www.ingentaconnect.com/content/mtax/mt
P.O. BOX 264, ITHACA, NY 14581-0264, USA
Iv ... MYCOTAXON 136(2)
MYCOTAXON
VOLUME ONE HUNDRED THIRTY-SIX (2) — TABLE OF CONTENTS
COonricendd ts, on BS Seba s Prk ee ihagh Fe Sha eR EAA eee eet aap Ae eee vi
Nomenclatural novelties & typifications ........ 0. cece eee eee ees vii
AS EV ACMI OTST to ere. a Se cai ge an Sate Ree EK niece Eke Bake 3 SS Ae eo eager ss aes Sk x
TUOUEE LO TAILOUS 2 Murssd gh Pak hier rid thle hes dP eee hd dee Led he aaAay xi
2O2T SUBMISSION PTOCE ANTES 0 5 bo Oa bones alee 8 WO eee eae eee xiii NEw TAXA
Collybiopsis and its type species, Co. ramealis RONALD H. PETERSEN & KAREN W. HuGHEs 263
Parathozetella microsperma gen. & sp. nov., from the Brazilian Amazon FLAVIA RODRIGUES BARBOSA, PATRICIA OLIVEIRA FIUZA, JOSIANE SANTANA MONTEIRO, ALEXANDRE PEREIRA DA SILVA, Luis FERNANDO PASCHOLATI GUSMAO, RAFAEL FELIPE CASTANEDA-Ruiz 351
Pseudosperma albobrunneum sp. nov. from coniferous forests of Pakistan SANA JABEEN, ZAINAB, HiRA BASHIR, ABDUL NASIR KHALID 361
Entyloma eranthidis sp. nov. on Eranthis longistipitata from Uzbekistan TEODOR T. DENCHEV, CVETOMIR M. DENCHEV, MARTIN KEMLER, DOMINIK BEGEROW 373
Calogaya miniata comb. nov., Huneckia crocina comb. nov., and new neotropical records of Wetmoreana brouardii KARINA WILK 387
Kirschsteiniothelia shimlaensis sp. nov., from Himachal Pradesh, India RaJNISH KUMAR VERMA, I.B. PRASHER, SUSHMA, AJAY KUMAR GAUTAM, KUNHIRAMAN C. RAJESHKUMAR, RAFAEL F. CASTANEDA-Ru1z 401
KEYS
A key to the identification of the genera of lichenized fungi occurring in Thailand VASUN POENGSUNGNOEN, KAWINNAT BUARUANG, KANSRI BOONPRAGOB, H. THORSTEN LuMBSCH 409
NEW RANGES/HOSTS
Dictyostelids from Jilin Province, China, 4 HE ZHU, SONGNING GUO, QIN XUE, ZHUANG LI, XUEPING KANG, YUHUA WEI, Pu Liu, Qi WANG, Yu Li 445
APRIL-JUNE 2021... V
New host and distributional records for Camarosporidiella
in Italy, Russia, and Ukraine DHANDEVI PEM, RAJESH JEEWON, TIMUR S. BULGAKOV,
IRINA V. BONDARENKO-BORISOVA, MINGKWAN DOILOM,
ABDALLAH M. ELGORBAN, RUNGTIWA PHOOKAMSAK, SAISAMORN LUMYONG, KEVIN D. Hype 451
Microbotryum bardanense and M. polygoni-alati -
new records from Nepal TEODOR T. DENCHEV, SUK-Pyo HonG, CvETomIR M. DENCHEV 491
Chlorophyllum hortense newly recorded,
and C. molybdites confirmed, from Pakistan SANA JABEEN, SHAHZEENA ARSHAD, HUMAIRA BASHIR,
MuGHEES HAMID, ANEELA YASMEEN, ABDUL NASIR KHALID 497
New record of Geopora sumneriana from Pakistan IRFANA MAQSAD, BARKAT ALI, TASMIA BASHIR, ABDUL SAMAD Mumtaz 511
Didymocyrtis epiphyscia, Lichenochora weillii, and Lichenoconium xanthoriae newly recorded from Turkey MustaFa Kocakaya 523
Ganoderma leucocontextum, a new record from Pakistan AIsHA UMAR, SHAKIL AHMED, HIRA BASHIR 529
MycosBioTa (FUNGAE) NEW TO THE MYCOTAXON WEBSITE
Lichens from Brazil: a checklist of lichenized fungi
from Acre, in the Amazon (suMMaRy) ANDRE APTROOT, LIDIANE ALVES DOS SANTOS, ISAIAS OLIVEIRA JUNIOR,
JANICE GOMES CAVALCANTE, MARCELA EUGENIA DA SILVA CACERES 541
Basidiomycetes within Calabrian pine (Pinus brutia) ecosystems on the island of Cyprus (summary) MICHAEL LOIZIDES 543
VI ... MYCOTAXON 136(2)
CORRIGENDA
CORRIGENDA FOR MYCOTAXON 136(2) Cited below are mistakes present in files submitted for PDF conversion in the current issue but not detected by the authors until after the paper had
gone to press.
p- 533, line 2 FOR: C. Section of context; D. Lower surface pores; ... READ: C. Lower pores surface; D. Pores section under microscope: ...
p- 533, line 3 FOR: I. Binding hyphae J. ... READ: I. Binding hyphae; J. ...
p. 537, line 1 For: The 5-6 mm long tubes G. leucocontextum ... READ: The 5-6 mm long tubes of G. leucocontextum ...
PUBLICATION DATE FOR VOLUME ONE HUNDRED THIRTY-SIX (1)
MYCOTAXON for JANUARY-MARCH 2021 (I-XvI + 1-262) was issued on April 16, 2021
APRIL-JUNE 2021 ...
NOMENCLATURAL NOVELTIES AND TYPIFICATIONS
PROPOSED IN MYCOTAXON 136(2)
Calogaya miniata (Hoffm.) Wilk & Licking [MB 839870], p. 393 Collybiopsis biformis (Peck) R.H. Petersen [IF 556182] p. 341 Collybiopsis brunneigracilis (Corner) R.H. Petersen [IF 557078], p. 341 Collybiopsis californica (Desjardin) R.H. Petersen [IF 556204]. p. 277 Collybiopsis confluens (Pers.) R.H. Petersen [IF 556183]. p. 341 Collybiopsis dichroa (Berk. & M.A. Curtis) R.H. Petersen [IF 556184], p. 341 Collybiopsis diminuta (Berk. & Broome) R.H. Petersen [IF 556185], p. 341 Collybiopsis disjuncta (R.H. Petersen & K.W. Hughes) R.H. Petersen & K.W. Hughes [IF 556777], p. 341 Collybiopsis eneficola (R.H. Petersen) R.H. Petersen [IF 556186], p. 342 Collybiopsis fibrosipes (Berk. & M.A. Curtis) R.H. Petersen [IF 557077], p. 342 Collybiopsis filamentipes R.H. Petersen [IF 557073]. p. 287 Collybiopsis foliiphila (A.K. Dutta, K. Acharya, Antonin) R.H. Petersen [IF 557080], p. 342 Collybiopsis furtiva R.H. Petersen [IF 556208]. p. 297 Collybiopsis gibbosa (Corner) R.H. Petersen [IF 556187], p. 342 Collybiopsis hasanskyensis R.H. Petersen [IF 557072], p. 309 Collybiopsis indocta (Corner) R.H. Petersen [IF 556188], p. 342 Collybiopsis juniperina (Murrill) R.H. Petersen [IF 556189], p. 342 Collybiopsis luxurians (Peck) R.H. Petersen [IF 556190], p. 342 Collybiopsis melanopus (Wilson, Desjardin & E. Horak) R.H. Petersen [IF 556191], p. 342
VII
vill ... MYCOTAXON 136(2)
Collybiopsis menehune (Desjardin, Halling & Hemmes) R.H. Petersen [IF 556192], p. 343 Collybiopsis mesoamericana (J.L. Mata) R.H. Petersen [IF 556193], p. 343 Collybiopsis micromphaloides (R.H. Petersen & K.W. Hughes) R.H. Petersen [IF 556778], p. 343 Collybiopsis minor R.H. Petersen [IF 556206], p. 317 Collybiopsis neotropica (Singer) R.H. Petersen [IF 556942], p. 343 Collybiopsis nonnulla (Corner) R.H. Petersen [IF 556194], p. 343 Collybiopsis obscuroides (Antonin & Legon) R.H. Petersen [IF 556943], p. 343 Collybiopsis parvula (J.L. Mata, R.H. Petersen & K.W. Hughes) R.H. Petersen [IF 556779], p. 343 Collybiopsis peronata (Bolton) R.H. Petersen [IF 556195], p. 343 Collybiopsis polygramma (Mont.) R.H. Petersen [IF 556944], p. 344 Collybiopsis pseudoluxurians (R.H. Petersen & K.W. Hughes) R.H. Petersen [IF 556196], p. 344 Collybiopsis quercophila (Pouzar) R.H. Petersen [IF 556197], p. 344 Collybiopsis ramealis (Bull.) Millsp. 1913 = Agaricus ramealis Bull. 1788 nom. sanct., [IF 556205, (epitypified)], p. 326 Collybiopsis readiae (G. Stev.) R.H. Petersen [IF 556945], p. 344 Collybiopsis stenophylla (Mont.) R.H. Petersen [IF 557079], p. 344 Collybiopsis subcyathiformis (Murrill) R.H. Petersen [IF 556946], p. 344 Collybiopsis subnuda (Ellis ex Peck) R.H. Petersen [IF 556198], p. 344 Collybiopsis subpruinosa (Murrill) R.H. Petersen [IF 556199], p. 344 Collybiopsis synodica (Kunze ex Fr.) R.H. Petersen [IF 556200], p. 345 Collybiopsis termiticola (Corner) R.H. Petersen [IF 556201], p. 345 Collybiopsis vaillantii (Pers.) R.H. Petersen [IF 556202], p. 345
APRIL-JUNE 2021 ...
Collybiopsis villosipes (Cleland) R.H. Petersen [IF 556203], p. 345 Entyloma eranthidis T. Denchev, Denchev, Kemler & Begerow [IF 557320], p. 382 Huneckia crocina (Kremp.) Wilk [MB 836903], p. 395 Ionaspis aptrootii Poengs. & Lumbsch [MB 835127], p. 427 = Ionaspis tropica Aptroot 1997, nom. illegit. (non Riddle 1920) Kirschsteiniothelia shimlaensis Rajn.K. Verma, Prasher, Rajeshk., Sushma, A.K. Gautam & R.F. Castaneda [IF 557827], p. 404 Parathozetella F.R. Barbosa, J.S. Monteiro, Fiuza, R.F. Castafeda & Gusmao [MB 834624], p. 353 Parathozetella microsperma E.R. Barbosa, J.S. Monteiro, Fiuza, R.E Castaneda & Gusmao [MB 834626], p. 353 Pseudosperma albobrunneum Jabeen, Zainab, H. Bashir & Khalid [MB 840056], p. 364
IX
x ... MYCOTAXON 136(2)
REVIEWERS — VOLUME ONE HUNDRED THIRTY-SIX (2)
The Editors express their appreciation to the following individuals who have,
prior to acceptance for publication, reviewed one or more of the papers
prepared for this issue.
Andreas Beck
Jayarama Bhat
Jerry Cooper
Manuela Dal Forno Pradeep Kumar Divakar Xi-Hui Du
Tine Grebenc
Arthur Grupe
Emerson Luiz Gumboski Danny Haelewaters Shuang-Hui He
Makoto Kakishima Martin Kukwa
John C. Landolt
De-Wei Li
Patrick M. McCarthy
Rosa Maria Arias Mota Lorelei L. Norvell Shaun R. Pennycook Sergio Pérez-Ortega Raquel Pino Bodas Elias Polemis
Huzefa A. Raja
Carmel Sammut Harrie Sipman Tibpromma Saowaluck Steven L. Stephenson Priyanka Uniyal
Else C. Vellinga Nousheen Yousaf
Juan Carlos Zamora Chang-Lin Zhao
APRIL-JUNE 2021... XI
FROM THE EDITOR-IN-CHIEF
LATE AGAIN? — We could write volumes explaining why MycoTaxon 136(2) is delayed. But rather than spew meaningless ink on these pages, we simply offer a brief apologetic explanation: the 2021 April-June MycoTaxon is being released in July/August BECAUSE: the EIC foolishly thought she might prepare her own research paper after closure of 136(1), medical issues and side effects assaulted both editors after April, Oregon melted under a record-breaking June “heat dome” (on June 30 reaching a high 116°F (46.7°C) with no air-conditioning and hot nights), the editorial ADoser publishing application began disintegrating, with InDesign stalling several times daily and finally snatching carefully formatted tables or eating italics from text in front of horrified editorial eyes, and the Internet crashed. Internet service was restored last week. After repeated crashes, the frazzled EIC uninstalled and reinstalled all Adobe applications, imported and formatted missing text and italics anew, restored tables, and more or less successfully converted the final five papers confronting a VERY strange interface. (Some time in the past four years, the Adobe subscription disappeared off the editorial computer, to be replaced by a rickety 2013 application. Don't ask. The EIC’s First Born is convinced the editorial computer is haunted. We see no evidence to the contrary.)
A MYCOTAXON PRIMER TO SCIENTIFIC NAMES: Undergraduates are generally taught that a scientific name comprises Two elements: the name of the genus (capitalized) + the name of the species (all lower case): e.g., Russula campinensis. In mycological taxonomic journals, scientific authors are also expected to cite authorities (generally only once): ie., Russula campinensis (Singer) T.W. Henkel, Aime & S.L. Mill. Authors cited within parentheses are those who originally named the species while those standing outside the brackets transferred the species to a different genus. A species name that serves as the title of a section containing a full description heads a ‘taxonomic section’ and includes the complete taxonomic reference: genus name, species name, naming authors, an abbreviated but complete bibliographic reference, and date of publication. The complete taxonomic reference of the name above is: Russula campinensis (Singer) T.W. Henkel, Aime & S.L. Mill., Mycologia 92(6): 1124 (2000).
Basically, we cite authorities only ONCE per paper to make the text more user friendly. If a species is not part of a taxonomic heading, authorities are cited generally at first mention. Because now complete fungal names (including bibliographic reference) are available on the internet, the Code recommends (for ‘incidental’ mention in a taxonomic paper) that species named by more than two authors be cited as First author & al. (ie., Russula campinensis (Singer) T.W. Henkel & al.).
Index Fungorum also presents a list of standardized author spellings: see http://www.indexfungorum.org/names/AuthorsOfFungalNames.asp . Reference to this list will ensure that each authority is spelled consistently in mycological literature. When in doubt how to present a taxonomic heading, use IndexFungorum (universally available online) as a model.
xi ... MYCOTAXON 136(2)
One last note: although names of synonyms and basionyms are nomenclatural in nature, the decision as to WHICH synonym should be used is a TAxoNoMIC (NOT nomenclatural) decision.
Our 2021 April-June Mycotaxon provides 17 contributions by 70 authors (representing 17 countries) as revised by 35 expert reviewers and the editors.
The NEw Taxa (6 titles) section leads off the issue with a monographic treatment of Collybiopsis, here endorsed over Marasmiellus “especially by (re)describing taxa within the Co. ramealis complex with emphasis on European collections of Co. ramealis;” the authors propose five new species (one a previously described taxon here elevated to species), and 35 new combinations. NEw Taxa also covers ONE new genus (Parathozetella from Brazil) and an additional FouR species new to science representing Entyloma from UZBEKISTAN; Kirschsteiniothelia from Inp1a; Parathozetella from BRAZIL; and Pseudosperma from PAKISTAN. We also offer Two new combinations in Calogaya and Huneckia and ONE epitypification for Collybiopsis (= Agaricus) ramealis.
Keys presents an impressive key to the 258 genera of lichenized fungi in Thailand, which also proposes the replacement name Jonaspis aptrootii for the illegitimate I. tropica.
NEW RANGES/HOSTS (seven titles) report range extensions for [ascomycetes] Camarosporidiella for Iraty, UKRAINE, and Russia and Geopora for PAKISTAN; [basidiomycetes] Chlorophyllum and Ganoderma for PAKISTAN and Microbotryum for NepAL; [lichens] Didymocyrtis, Lichenochora, and Lichenoconium for TURKEY; and [myxomycetes] Dictyostelium for Cu1na. New hosts are cited for Camarosporidiella from UKRAINE.
Papers providing research supported by phylogenetic analysis include seven new species representing Collybiopsis, Entyloma, and Pseudosperma, the two new Calogaya and Huneckia combinations, and nine range extensions.
Our issue concludes with the announcement of two new annotated species lists on our MYCOBIOTA website, covering lichenized fungi from the Amazon (BRAzIL) and basidiomycetes within Calabrian pine ecosystems on CyPRUS.
Warm (no longer hot!) regards and best wishes for good health,
Lorelei L. Norvell (Editor-in-Chief) 21 July 2021
APRIL-JUNE 2021 ... XIII
2021 MyCOTAXON SUBMISSION PROCEDURE
Prospective MycotTaxon authors should download the MycoTaxon 2021 guide, review & submission forms, and MycoTaxon sample manuscript by clicking the ‘file download page’ link on our INSTRUCTIONS TO AUTHORS page before preparing their manuscript. This page briefly summarizes our “4-step’ submission process.
1—PEER REVIEW: Authors first contact peer reviewers (two for journal papers; three for mycobiota/fungae) before sending them formatted text & illustration files and the appropriate 2021 MycoTaxon journal or mycota reviewer comment form. Experts return revisions & comments to BoTH the Editor-in-Chief <editor@mycotaxon.com> and authors. ALL co-authors must correct and proof- read their files before submitting them to the Nomenclature Editor.
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3—FINAL SUBMISSION: All coauthors thoroughly revise and proof-read files to prepare error-free text and images ready for immediate publication. Poorly formatted copy will be rejected or returned for revision. E-mail the final manuscript to the Editor-in-Chief <editor@mycotaxon.com>, adding the accession number to the message and all files, which include a (i) revised 2021 submission form, all (ii) text files and (iii) jpg images, and (iv) FN, IF, or MB identifier verifications for each new name or typification. The Editor-in-Chief acknowledges submissions within two weeks of final submission but requests authors to wait at least 14 days before sending a follow-up query (without attachments).
4—FINAL EDITORIAL REVIEW & PUBLICATION: The Editor-in-Chief conducts a final grammatical and scientific review and returns her editorial revisions to all expert reviewers and coauthors for final author approval. Author-approved files are placed in the publication queue.
The PDF proof and bibliographic & nomenclatural index entries are sent to all coauthors for final inspection. After PDF processing, the Editor-in-Chief corrects ONLY PDF editorial/conversion and index entry errors; corrections of all other errors are listed in the ERRATA of a subsequent issue for no charge. Authors will pay fees for mycobiota uploads, optional open access, and correction of major author errors to the Business Manager <subscriptions@mycotaxon.com> at this time.
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The Mycotaxon Webmaster <mycotaxon@gmail.com> posts announcements, subscription & publication information, and author forms & templates on the official MycoTAXxon site. Our server also hosts the mycobiota web-page for free download of Fungae (regional annotated species lists).
MYCOTAXON ONLINE— www.ingentaconnect.com/content/mtax/mt The MycoTaxon journal publishes four quarterly issues per year. Both open access and subscription articles are offered.
MYCOTAXON
ISSN (print) 0093-4666 (online) 2154-8889 Mycotaxon, Ltd. ©2021
April-June 2021— Volume 136, pp. 263-349 https://doi.org/10.5248/136.263
Collybiopsis and its type species, Co. ramealis
RONALD H. PETERSEN* & KAREN W. HUGHES
Ecology and Evolutionary Biology, University of Tennessee Knoxville, TN 37996-1100.
CORRESPONDENCE TO: repete@utk.edu
ABSTRACT—Collybiopsis (Omphalotaceae, Agaricales) is accepted as the correct genus name for a large clade of non-typical Gymnopus. The type species of Collybiopsis (Agaricus ramealis) is shown to be a genetic complex. Collybiopsis filamentipes, Co. furtiva, Co. hasanskyensis, and Co. minor are proposed as spp. nov. and Co. californica as a stat. nov. Thirty-four additional Collybiopsis comb. nov. are proposed in Appendix I.
Key worps—clade /marasmiellus, morphology, taxonomy, new combinations, new species
Introduction
For many years, agaric taxonomists have dealt with the morphological and molecular diversity of both Gymnopus and Marasmius. Several segregate genera have been carved from Gymnopus, but a large complex of fungi remains, comprising taxa contributed by elements of Gymnopus, Marasmius, and Marasmiellus. This large assemblage has been called Marasmiellus (see Wilson & Desjardin 2005), presumably because the type species of Marasmiellus, Ma. juniperinus, is included. Recent papers by Dutta & al. (2015) and Oliveira & al. (2019) are among the latest to draw attention to Marasmiellus. Two principles were included: 1) presentation of a well-populated phylogeny to demonstrate placement of numerous taxa exhibiting “gymnopoid, “marasmioid,’ and/or “marasmielloid” taxonomic character suites; and 2) the use of the genus name Marasmiellus to represent a large taxonomic group that includes type species of at least two genera (Marasmiellus and Collybiopsis) plus taxa of Gymnopus sect. Vestipedes. While
264 ... Petersen & Hughes
we agree with the taxonomy presented, we choose to follow the International Code of Nomenclature (Turland & al. 2018, Art. 11.3) in accepting the prior genus name, Collybiopsis, for the group that Oliveira & al. (2019) and Wilson & Desjardin (2005) called Marasmiellus.
Nomenclaturally, Collybiopsis Earle 1909 (with its explicit type species Agaricus ramealis Bull. 1787) has clear priority over Marasmiellus Murrill 1915 (explicitly typified by Ma. juniperinus Murrill). Use of Marasmiellus for this clade would require conservation of this genus name, not yet proposed. In addition, Ma. juniperinus is poorly represented phylogenetically (two ITS-based sequences, neither from the topotype location). Conversely, Co. ramealis is a well-known taxon molecularly represented from original topotype locales. The relative placement of these taxa is shown in Fics 1, 2. To our knowledge, only Horak (1971) has recombined basionyms into Collybiopsis.
Taxonomic circumscription of fungi assigned to Marasmiellus-like taxa has changed and enlarged over the last century. Although an extensive literature chronology could be narrated, this is not the intent of this paper. Instead, literature can be concisely cited, leaving further investigation to the reader. A sketch of this morpho-taxonomic process includes: Antonin & Noordeloos (1993, 1997, 2010); Clements & Shear (1931, 1954); Corner (1996); Donk (1962); Earle (1909); Horak (1968); Kiihner (1933, 1936); Murrill (1915); Patouillard (1900); Singer [1936, 1945, 1948, 1962— dismissing Collybiopsis and accepting Marasmiellus with 59 species; for more on this, see “Discussion” —and 1973 with 134 species listed in Marasmiellus]. Since the introduction of molecular tools in fungal taxonomy, numerous papers have presented phylogenetic trees including or alluding to the group under consideration. These papers include Aldrovandi & al. (2015); Binder & Hibbett (2002); Dentinger & al. (2016); Desjardin (1997); Desjardin & al. (2017); Desjardin & Perry (2017); Dutta & al. (2015); Honan & al. (2015); Hughes & Petersen (2015); Hughes & al. (2001, 2008); Kerekes & Desjardin (2009); Kim & al. (2015); Mata & al. (2004, 2007); Matheny & al. (2006); Moncalvo & al. (2000, 2002); Nakasone & al. (2009); Oliveira & al. (2019); Petersen & Hughes (2014, 2016, 2017a,b); Sandoval-Leiva & al. (2016); and Wilson & Desjardin (2005).
The intent of this paper is to endorse use of Collybiopsis over Marasmiellus, especially by (re)describing taxa within the Co. ramealis complex with emphasis on European collections of Co. ramealis. A list of proposed transfers into Collybiopsis appears in Appendix I.
Collybiopsis resurrected ... 265
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Collybiopsis resurrected ... 267
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WSINVDUO
Collybiopsis resurrected ... 269
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‘ON Worivatay
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WSINVDUO
270 ... Petersen & Hughes
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‘ON Woarivatay
ppnugns ‘0D vpnugns sisdo1qdyjoD stusofiyjodogns ‘oD stusofiyjodaqgns ‘oD siumsofiyzodogns sisdo1qdqjoy
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WSINVDUO
Collybiopsis resurrected ... 271
SLSTCTEAM VLSITEAM eLSTTe AM
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‘ON Worivatay
‘ds sndoumdy
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272 ... Petersen & Hughes
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WSINVDUO
Collybiopsis resurrected ... 273
Materials & methods
ABBREVIATIONS: Throughout this paper, Co = Collybiopsis; G = Gymnopus; M = Marasmius; Ma = Marasmiellus. Colors cited alphanumerically are from Kornerup & Wanscher (1967) and those in quotation marks are from Ridgway (1912). BF = bright field microscopy; PhC = phase contrast microscopy (see also Petersen & Hughes 2017b). TFB = Tennessee field-book number, assigned to fresh collections in order to track specimen, photos, notes, etc.; TENN-F- XXXXXX = official designation of the herbarium of the University of Tennessee (and Mycoportal number). GSMNP = Great Smoky Mountains National Park. In basidiospore metrics, E = range of spore lengths divided by spore widths; E™ = median spore length divided by median spore width; L” = median spore length. In descriptions L = complete lamellae; L + ll = lamellae + lamellulae Herbarium acronyms are from Index Herbariorum.
Metrics of microstructures were calculated using an Olympus BX60 microscope fitted with phase contrast imagery and photographs of microstructures were produced with an Olympus Q_ color camera. Microscope mounts were usually in 3% KOH solution or Melzer’s reagent (abbr. IKI).
Molecular methods for DNA extractions, PCR, and Sanger sequencing of the nuclear ribosomal ITS and LSU regions were described in Aldrovandi et al. (2015). DNA sequence alignments with concatenated ITS and LSU sequences (where available (see TABLE 1) were performed in Geneious 11.0.3 (2017) using Clustal W (Thompson & al. 1994) then manually adjusted in AliView 1.26 (Larsson 2014). Unlike Olivera & al., (2019), we did not delete highly variable regions of the alignment because information content in these regions informed species groupings. PhyML phylogenetic analyses were performed in Geneious 11.0.3 (2017) using a Generalized Time-reversable model (GTR) with 4 nucleotide substitution rate catigories and a gamma rate variation with 4 categories. Values for the transition/transversion ratio, proportion of invariable sites, and gamma distribution parameter were estimated. 500 boot strap replications were performed. Bayesian analysis was performed in Geneious 11/0/3 using MrBayes 3.2.6 (Huelsenbeck & Ronquist 2001) with a GTR model of evolution, 4 chains and a burn-in of 100,000. Chain length was 1,100,000. Sequences were deposited in GenBank (TABLE 1). Specimen data are available in Mycoportal (MyCoPortal 2018).
Taxonomy
AnITS+LSU phylogeny of Collybiopsis is presented in Fic. 1.Gymnopanella nothofagi, Mycetinis spp., and Paramycetinis spp. were selected as related outgroups based on a nrLSU phylogeny in Petersen & Hughes (2020). Collybiopsis as circumscribed in this paper includes Co. dichroa, a genetic complex of several poorly circumscribed taxa. Collybiopsis dichroa I and II
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form natural hybrids but there is no evidence that F2 later progeny are viable (Hughes & al. 2015). Collybiopsis ramealis appears as sister to Co. furtiva and is in a larger, well-supported clade with Co. stenophylla, Co. filamentipes, Co. californica, and Co. foliiphila.
1.00, KT906425 ] Gymnopanella nothofagi
100 KT906426 1.00 KX752265 Mycetinis salalis 98 KX958397 Mycetinis kallioneus KY696758 1.00} Ti00 KY696769 100 MW396877 Mycetinis opacus 1.00 KY696768 98 MW396878 KY696734 1.00 KY696731 10 KY696733 75 KY696748 KY696742 Mycetinis scorodonius KY696739 KY696746 KY696741 KY026644 KY026645 97 KY026642 Paramycetinis cauloscystidiatus 1,00 KY026643 100 KY026622 | 76 KY026638 Paramycetinis austrobrevipes KY026637 1.00 KY026677 KP454027 100 100 77 KY026755 Co. peronata 100 MH855896 0.69 KY026676 97 10.76 KY026765 Co. subnuda 87 MW396876 1.00 KY026696 1.00 |100 KY026697 100 if pgs Sve Co. dichroa MW396866 MW396868 KY026654 MW396869 MW396874 Co. sp. , MN413333 MW396872 Co. minor MN413334 0.55 KY026729 KY026736 Co. quercophila KY026737 KY026761 AY256708 _ Co. juniperina KY026661
KP100305 NR_137539
KY026707 ] “Co. utriformis”as Gymnopus sp 17 L_ KY026708
| Co. melanopus
Collybiopsis resurrected ...
1.00 MF163171 100 L.67 KJ416255 Co. villosipes 59 1.00 DQ450058 93 ni KY404984 33 KT697977 100 DQ450062 DQ450061 Co. parvula NR_119584 AF505774 DQ450060 100 DQ450036 NR_119583 | Co. mesoamericana 1.00 0.95 AF505768 99 96 AF505769 Co. neotropicus 80 1.00 AY263443 1.00 98 Tiss Co. menehune 8 DQ450043 ; — Seti ] Co. subcyathiformis 1.00 HQ533036 100 L927 DQ450034 Co. readiae KJ416244 1.00 KP710279 100 KP710278| Co. confluens ssp. americana 100 1.00 79 KP71028 53 '°l1.00 KP710296 Co. confluens 100 KP710292 1.00 KJ416253 10.98 | 100 NR_137865 72 |) op KJ416246 Co. disjuncta 100 KJ416249 KJ416245 72 KJ416248 KY352520 environmental sample KY026676 Co. vaillantii 98 MF161290 Gymnopus sp. 1.00 0.99 89 [1.00 MN897829 4 ; 100 4 97 MN897830 + Co. hasanskyensis MW396870 Collybiopsis sp. 1 0.93 00 KX958399 ; nse 49 |, oo{100 KX958308 ] Co. obscuroides 100 0G KP710270 1.00} 10° PK6976 Co. eneficola 87 [1.00 KJ128265 100 NR_137613 1.00 MN930621 1.00/| 99 MN930622 £00 98 [1.00 AY263446 | Co. nonnulla 91 100 AY263445 1.00 KY026699 T00 KY026701 MK214392 1.00 MN258643 100 KJ609162 KJ778752 88 KY074640 Co. polygramma KY074641 KY074642 93 AY842954__ DQ450028 1.00 = pene oy “Co. pseudomphalodes”/fibrosipes 100 | 1.00 KY321574 100 L9:29 KY321573 | 1.00 ol 81 KY321575 Gymnopus sp. 81 100 1.00 KY026702 Co. pseudoluxurians 100 10.95 KY026649 08 88 7 at sean 6871 Co. luxurians 69 AF505765 AY639431 Co. trogioides AY639412 Co. brunneigracilis 1,00 KY061203 100 KP012713 oo gibbosa 4 86 KY061202
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npeamatas ] Co. stenophylla
HM488468 environmental
MN897832 : MG433317 Co. filamentipes HM488469 environmental
MN413338_
DQ273359 Co. californica MN413335
MN413337
MN413336
KP317638 he
NR_ 154176 | Co. foliiphila
LC505328 Agaricales sp
FJ179468 Uncultured Agaricales
MW396875
MW405779
MN413346 Co. ramealis MN413350 MN413372 MN413343
DQ450031_
MN413341
MN413342 MN413343 MN413340 93 MN413339
Co. furtiva
Fics 1A, B, C. PhyML tree of concatenated nrITS and LSU Collybiopsis sequences. Support values at the nodes consist of Bayesian posterior probabilities (top value) and PhyML bootstrap support based on 500 replications (bottom value). The outgroup comprises Gymnopanella and Mycetinis. The label on each branch represents the nrITS GenBank accession number. Corresponding LSU sequences are given in TABLE 1. GenBank accession numbers in bold represent types. Taxa described in this paper are also in bold. The phylogeny is divided into three parts with arrows connecting each part.
An nrITS-based phylogeny including all sequenced collections of Co. ramealis (Fic. 2) demonstrates that Co. ramealis represents a complex, not a single taxon. Several issues are resolved or raised. First, European collections are very nearly homogeneous based on nrITS sequences, so topotype Co. ramealis remains a circumscribable taxon well described by Antonin & Noordeloos (2010) and below. Examination of nrITS sequences reveals, however, that the European population consists of two ITS haplotypes and hybrids, with indications that genetic recombination has occurred between haplotypes. Conversely, at least some North American collections (to this time limited to southeastern North America), are clearly separated from Co. ramealis, and are here described as Co. furtiva. Likewise, Marasmiellus ramealis var. californicus lies within Collybiopsis, discrete at species rank and more widely distributed than anticipated.
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MNadaeoe Co. stenophylla oie g Renu 1,00] KP317638 a DQ450033 a cl Co. foliiphila
MN897832 , ‘ 0.89) \91G433317 ] Co. filamentipes
1.00] _| MN413335 100 MN413337 : : MN413336 | Co. californica 1.00 HM488468 , MN413338 HM488469
MN413343 eae PMIN413339 95 MN413340 | 0. furtiva MN413341 MN413342
MN413346 MN413347 MN413348 MN413364 MN413366 1.00 MN413367 36 MN413363 MN413357 MN413362 MN413361 MN413365 MN413355 MN413360 MN413359 4 MN413358 Co. ramealis MN413356 MN413353 MN413350 KJ416235 DQ450030 MN413372 JF313670 MN413353 MN413352 MN413351 KJ416235 MN413344 MN413345 MN413349 MW405779 MN413371 MN413370
Co. ramealis complex
0.08 changes
Fic. 2. PhyML tree of nrITS sequences representing the Collybiopsis ramealis complex. Collybiopsis stenophylla was used as an outgroup. Support values at the nodes consist of Bayesian posterior probabilities (top value) and PhyML bootstrap support based on 500 replications (bottom value). The label on each branch represents the nrITS GenBank accession number.
Taxonomic analyses
Collybiopsis californica (Desjardin) R.H. Petersen, stat. nov. Figs 3-13 IF 556204 BastonyM: Marasmiellus ramealis var. californicus Desjardin, Mycologia 79: 132. 1987.
Ho.totype: USA, California, Los Angeles Co., San Dimas, 34°06’23”N 117°48’25”W, 9.]11.1983, Wright 2941 (SFSU-F s.n.).
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Fic. 3. Collybiopsis californica (Wright 866; SFSU-F-024539). A. Basidiomata and rhizomorphs. B. Basidiospores. C. Termini of caulocystidia.
Scale bars: A = 10 mm; B = 5 um; C = 10 um.
Desjardin (1987) offered a detailed, comprehensive description of Marasmiellus ramealis var. californicus. Our Fic. 2 indicates that the taxon, while related to Co. ramealis (both European and putative American), is separable from Co. ramealis at species rank, triggering the rank change above. The following items are worthy of note: 1) photographic images and discussion of microstructures (Frcs 3-13); and 2) the taxon’s apparent extended geographic distribution.
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Fic. 4. Collybiopsis californica. (Wright 2941 SFSU s.n.). Diverticulate pileipellis hyphae. Scale bars = 10 um.
A comparison of microstructures of Co. californica (Fics 3-13) with those of Co. ramealis (Fics 50-60) includes the nature of the structure of pileipellis hyphae. In Co. ramealis, diverticula are slender, digitate and appear rigid, while those of Co. californica (Fic. 5) are broad, often fin- or node-like, gnarled and repeatedly branched. Pleurocystidia (Fic. 6), basidioles, and basidia (Fic. 7)
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Fic. 5. Collybiopsis californica. (TFB 5787; TENN-F-052617). Pileipellis elements. A, B. Lobate-diverticulate elements. C-G. Diverticulate elements.
are similar to those of Co. ramealis, although somewhat longer. The variability of cheilocystidial shape from broadly clavate to ventricose-rostrate (Fics 8-11) is notable, but lengths and breadths of diverticula (which are often
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Fic. 7. Collybiopsis californica (Wright 2941; SFSU s.n.). A. Basidiole. B-E. Basidia. Scale bars = 10 um.
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Fic. 8. Collybiopsis californica. (Wright 2941; SFSU s.n.). Cheilocystidia. A. Cluster of three individuals. B, C. Individual cheilocystidia. Scale bars = 10 um.
subcapitate) are much longer and stouter. More intriguing, cheilocystidia of Co. californica are often transversely septate (apparently non-clamped; Fics. 11) and apparently easily disarticulated at this septum. The result is frequent subglobose to ventricose diverticulate structures with no evidence of stalk. Whether these structures could act as propagules is unknown. Finally, caulocystidia predictably range from short, simple, individual lobes at upper stipe (Fics 12, 13) to mid- or lower stipe vesture comprising
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Fic. 9. Collybiopsis californica. (DED 8372; SFSU-F-024526). Cheilocystidia. A. Cluster of three individuals. B-E. Individual cheilocystidia.
fascicles of hyphae perpendicular to stipe surface. Smaller such fascicles (Fic. I3) are synnematoid while larger assemblages are acervuloid.
At the time of initial proposal, all collections of Co. californica had been gathered in southern California. Since then, samples of mycelial mats under Pseudotsuga menziesii in northern California and roots of Lithocarpus densiflorus in Oregon have yielded sequences quite similar to those of the southern Californian collections (Bergemann & Garbelotto
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Fic. 11. Collybiopsis californica. (DED 8372; SFSU-F-024526). Cheilocystidia. A. Constricted by not septate cheilocystidium. B, C, E. Septate cheilocystidia. D. Cheilocystidium with septum below constriction. Scale bars = 10 um.
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Fic. 12. Collybiopsis californica. (DED 8372; SFSU-F-024526). Upper stipe ornamentation; individual nodose, digitate caulocystidia. Scale bars = 10 um.
2006; Kluber & al. 2011). Likewise, a sequence from a British Columbian collection (Canada, TENN-F-052617) matches the Californian collections. The species, obviously, exhibits a much wider distribution than originally conceived.
Pileipellis hyphal morphology is reminiscent of that of Gymnopus pyracanthoides (Petersen & Hughes 2016), especially regarding the complexity of diverticulate hyphae and broom cell-like termini of pileipellis hyphae. Basidiomata of the latter species, however, exhibit a slime matrix in the stipe medulla and the pileipellis includes some scanty evidence of gelatinous matrix, placing it in Gymnopus sect. Perforantes.
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Fic. 13. Collybiopsis californica. (DED 8372; SFSU-F-0024526). Mid-stipe ornamentation. Synnematoid fascicle of caulocystidia. Scale bar = 10 um.
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ADDITIONAL SPECIMENS EXAMINED: CANADA, BritTisH CoLumBiA, Chilliwack River Valley, 49°09’38”N 121°57'02”W, 8.X.1992, coll. RHP (as Marasmius androsaceus), TFB 5787 (TENN-F-052617). USA, CALIFORNIA, Los Angeles Co., Marshall Canyon, 34°06’23”N 117°48’25”W, 12.1.1978, coll. G Wright, det. DE Desjardin, Wright 866 (SFSU-F-024539); Marin Co., Point Reyes Nat. Seashore, Horse Trail, 38.043191 N, 122.802687, Wright 2941 (SASFU s.n.); , W, 11.X1.2008, coll. & det. DE Desjardin, DED 8372 (SFSU-F-024526); Trinity Co., Rte 299. Grey’s Falls Campground,40°51’26”N 123°29’30’W, 15.X1.1999. coll. D Largent, TFB 8088 (TENJN-F-055412).
Collybiopsis filamentipes R.H. Petersen, sp. nov. FIGS. 14-23 IF 557073
Differs from Co. furtiva in its narrower basidiospores, its caulocystidial shape and distribution, and its longer and thinner stipe.
Type: USA, Tennessee, Knox Co., Knoxville, 3613 Timberlake Dr, 35°54’49”N 83°57'58’W, 22. VIII.2011, coll. RHP, TFB 13962 (Holotype, TENN-F-065861).
Erymo ocy: Referring to the long, slender stipe.
BASIDIOMATA (Fic. 14A, 15) diminutive, gracile, decidedly mycenoid. Piteus 2-11 mm broad, strongly convex when young, later shallowly convex, matt; disc near “pinkish buff” 6A3, outward somewhat paler, hardly changing color upon drying. LAMELLAE adnexed to subdecurrent, few (L + Il = 12-13; L = 0-1), thickish with rounded edge with no anastomoses or buttressing, subventricose, off-white, developing pastel cantaloupe necropigment upon drying. Stripe 12-21 x 0.5-1 mm, concolorous with lamellae above, slightly darker downward but never darker than “sayal brown” 6C5 developing cantaloupe colored necropigment upon drying, not insititious, upward sometimes subsaccharine, downward almost glabrous. TASTE and opor negligible. RHIZOMORPHS absent.
HABITAT & DISTRIBUTION: apparently associated with Poaceae (lawn grass, dead fine roots of ornamental bamboo); so far extremely restricted to a small area of eastern Tennessee; mid-summer. Known only from the type locality with two collections (1970, 2011).
PILEIPELLIS constructed of three elements with intermediate forms: 1) repent, inflated, free-form hyphae <14 um diam, firm-walled, inconspicuously clamped (due to hyphal inflation), barely roughened to distinctly encrusted in small, densely gregarious patches — no annular or helical patterns observed, with frequent secondary septa (cloissons de retret) (FiGs.16, 17); 2) repent hyphae as in 1) but beset with diverticulate to setuloid ornamentation (F1G.18C); setulae <6 x 1-1.5 um; diverticula <9 x 1-2.5 um at base, lobate to conical, simple to variously branched;
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Fic. 14. Collybiopsis filamentipes. A. Basidiomata. (TFB 13962; TENN-F-065861). B. Basidiospores (upper = TFB 13962; lower = LRH 35861). Scale bar = 5 um (for spores); 5 mm (for basidiomata).
and 3) hyphal termini (Fig 18A, B, D) as in 2), usually antler-branched and with setulae and/or diverticula. Pileus and lamellar trama interwoven; hyphae 3-13 um diam, thin- to firm-walled, conspicuously clamped. PLEUROCYSTIDIA (Fic. 19) 25-32 x 6-8 um, stalked-fusiform, rounded apically, inconspicuously clamped; contents multigranular or multiguttulate,
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Fic. 15. Collybiopsis filamentipes. (TFB 13962; TENN-F-065861). Basidiomata (dried). Scale bar = 10 mm.
occasionally partitioned. Basip1A 26-33 x 7-8 um, clavate, 4-sterigmate, inconspicuously clamped; contents multiguttulate, usually with one major distal guttule. Basipiospores (Fic. 14B) 8-9.5(-10.5) x 2.5-3.5 um (E = 2.29-3.80; E™ = 2.96; L™ = 8.8 um), cylindrical to elongate-ellipsoid, thin-walled, smooth, inamyloid; contents multiguttulate, the guttules usually bipolar. Lamellar edge composed of two elements: 1) CHEILOCYSTIDIA (Fics. 20, 21A-C) plentiful, typically clavate to broadly clavate, 35-70 x 8-18(-25) um, occasionally stoutly dichotomous, conspicuously clamped, hyaline, firm-walled, surmounted by numerous diverticula; diverticula 3-15 x 1.5-2 um, appearing flexuous (not rigid), often branched, sometimes repeatedly so; and 2) DIVERTICULATE HYPHAE (Fic. 21D, E, 22) 5-8 um diam, firm-walled with diverticula in files; diverticula as in 1) above. STIPE MEDULLARY HYPHAE (2-)3.5-7.5 diam, hyaline, embedded in a slime matrix, strictly parallel, thick-walled (wall <1.5 um thick, hyaline), inconspicuously clamped. Stipe cortical hyphae 2-6.5 um diam, thick-walled (wall 1.5 um thick, golden ochre), inconspicuously clamped, producing hyphal termini and side branches (caulocystidia) perpendicular to stipe surface.
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Fic. 16. Collybiopsis filamentipes. (TFB 13962; TENN-F-065861). Pileipellis. A. Intricately encrusted hypha with apical diverticulate outgrowth. Note basidiospores.
B. Free-form hyphae. Short lines indicate secondary septa. Scale bars = 10 um.
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Fic. 17. Collybiopsis filamentipes. (TFB 13962; TENN-F-065861). Pileipellis. Inflated, repent hyphae with moderate encrustation.
Short lines indicate secondary septa. Scale bars = 10 um.
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Fic. 18. Collybiopsis filamentipes. (TFB 13962; TENN-F-065861). Pileipellis. Diverticulate hyphae. A. Inflated hypha with apical diverticula.
B, D. Hyphal terminus with diverticula. C. Diverticulate hypha. Scale bars = 10 um.
CaAULOcysTIDIA (Fic. 23) 5-20(-40) x 6-9 um, columnar to digitate, rarely branched, firm-walled, hyaline, without clamp connections, detersile.
COMMENTARY: Basidiomata of Co. filamentipes resemble those of Co. furtiva, a southeastern American species in the Co. ramealis complex. An even closer molecular match (~99%) is with Co. californica, distributed along the
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Fic. 19. Collybiopsis filamentipes. (TFB 13962; TENN-F-065861). Pleurocystidia. Scale bars = 10 um.
Fic. 20. Collybiopsis filamentipes. (TFB 13962; TENN-F-065861). Cheilocystidia. Scale bars = 10 um.
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Fic. 21. Collybiopsis filamentipes. (TFB 13962; TENN-F-065861). Cheilocystidia. A-C. Typical forms with apical diverticula.
D, E. Diverticulate hyphae of the hymenium. Scale bars = 10 um.
North American west coast. Collybiopsis filamentipes shares with both inflated cells in the pileipellis, Rameales-structure pileipellis, cheilocystidia bearing long tentacular diverticula, spore shape (Co. furtiva spores slightly wider than those of Co. filamentipes) and caulocystidia shape and distribution. Basidiomatal stature is surely different; stipe (and therefore the stipe length to pileus breadth ratio) is much longer and thinner in Co. filamentipes than in Co. furtiva and Co. californica.
Collybiopsis filamentipes adds to the Co. ramealis clade, species of which exhibit small micromorphological differences separable only with molecular techniques and/or a careful and practiced eye. As in other such compact clades, geographical distributions seem to support micromorphological
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Fic. 22. Collybiopsis filamentipes. (TFB 13962; TENN-F-065861). Diverticulate hyphae of the hymenium. Scale bars = 10 um.
and molecular evidence. That Co. ramealis seems not to occur in North America, and seems replaced by Co. californica, Co. filamentipes and Co. furtiva reflects the same situation in other agaric groups [e.g., Megacollybia rodmanii for M. platyphylla (Hughes & al. 2008); Collybiopsis confluens subsp. campanulatus in North America for the type subspecies in Europe (Hughes & Petersen 2015); Sparassis americana for S. crispa (Hughes & al. (2014, 2015)].
Interestingly, some years after collection of the holotype specimen in 2011, the Hesler specimen was discovered in the herbarium under “Marasmiellus sp.,. collected some 40 years previously within 100 m from the topotype location.
ADDITIONAL SPECIMEN EXAMINED: USA, TENNESSEE, Knox Co., Knoxville, Timberlake Dr., Hesler’s house, 1.VIII.1970, coll. LR Hesler, LRH 35861 (TENN-F-035861).
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Fic. 23. Collybiopsis filamentipes. (TFB 13962; TENN-F-065861). Caulocystidia. A, B, D. Clusters of Caulocystidia. C, E, F Individual caulocystidia. Scale bars = 10 um.
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Collybiopsis furtiva R.H. Petersen, sp. nov. Figs. 24-34 IF 556208
Differs from Old World Co. ramealis by its distinct molecular profile; its hyaline (not pigmented) cheilocystidia; and its generally smaller basidiomata. Type: USA, North Carolina, Macon Co., vic. Highlands, Horse Cove, Rustic Falls area, 35°02'17”N 83°09’32”W, 10.VIII.1987, coll. DE Desjardin (as Ma. ramealis), DED 4425 (Holotype, SSFU-F-024540). Etymo oey: furtiva = furtive, underhanded, secretive, referring to prior identification as Co. ramealis.
Fic. 24. Collybiopsis furtiva. (TFB 11558; TENN-F-059444). Pileipellis and pileus trama. A, B. Diverticulate hyphae of pileus surface. C. Diverticulate hypha ending in a “broom cell-like” hyphal terminus. D. “Antler-shaped” hyphae of subpellis. E. Swollen cells of pileus trama. F. Slender hypha among swollen hyphae of pileus trama. Scale bars = 10 um.
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BASIDIOMATA diminutive, ratio of stipe length to pileus diameter low. PILEUs 5-12 mm broad, strongly convex to subglobose when young, expanding to become shallowly convex to plano-convex with involute margin, finally applanate with upturned margin, opaque, consistently sulcate-striate near margin, matt; disc unicolorous or tinged brownish to avellaneous, otherwise white, orange-white, cream, pinkish cream, grayish-orange 5B2-3, pale orange white 6A2 developing necropigment near “ochraceous buff” 5A5. LAMELLAE adnexed to decurrent by a tooth, close to subdistant (L + ll = 35-52; L = 11-16), thickish, with little or no anastomosis but occasionally showing common forking near pileus margin in large basidiomata, becoming crisped in or after drying, seceding and then sometimes appearing pseudocollariate, white to cream white, near “pale olive buff” 3B2, or buff when fresh, developing
Fic. 25. Collybiopsis furtiva. (DED 4410; TENN-F-057309). Pleurocystidia. Note submammillate apices; clamp connection in E.
Scale bars = 10 um.
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Fic. 26. Collybiopsis furtiva. (TFB 11550; TENN-F-059444). Basidioles and basidia. A. Basidiole. B-H. Mature basidia. Note clamp connections in A, D, F.
Scale bars = 10 um.
ruddy necropigment; lamellar edge fimbriate or appearing crystalline, eroded, remaining white to buff or “pale pinkish buff” 6A2, but not marginate when fresh. Stipe 4-11 x 0.3-1.2 mm, terete or somewhat compressed upward,
300 ... Petersen & Hughes Fic. 27. Basidiospores of Collybiopsis taxa. A. Collybiopsis furtiva. (DED 4410; TENN-F-057309). B. Collybiopsis furtiva. (DED 3973; SFSU-F-024523).
C. Collybiopsis minor. (TFB 11930; TENN-F-059993). Scale bars = 10 um.
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Fic. 28. Collybiopsis furtiva. (DED 4425; SFSU-F-024540). Cheilocystidia. Scale bars = 10 um.
equal or tapered downward and then with minute snow white ring or ruff on stipe base, straight to curved (in drying?), sometimes abruptly pinched at base (similar to adult Ma. praeacutus), opaque or (now) appearing subcartilaginous, loosely stuffed to hollow; upper stipe appearing glabrous to minutely flocculose, concolorous with lamellae, not dextrinoid (sallow greenish yellow in IKI + BF);
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eS
Fic. 29. Collybiopsis furtiva. (DED 4410; TENN-F-057309). Upper stipe surface. Note files of simple lobate branches. Scale bars = 10 um
lower stipe (basal ~1/5) appearing flocculose to wispy, in age light brown 6D6, “avellaneous’ 7B3, reddish brown black to slightly brownish orange 6C5-6when young; insertion appearing insititious. ODoR negligible; TAsTE negligible.
HABITAT & PHENOLOGY: Gregarious; fruiting on well-rotted wood and dead twigs of Rhododendron maximum, Tsuga, various hardwoods, rarely on bark of grape; eastern United States (common in southern Appalachian Mountains); mid-summer.
PILEIPELLIS a well-developed Rameales-structure with two types of hyphae: 1) repent hyphae (Fic. 24A, B) 2.5-6.5 um diam, beset with diverticula; diverticula 1-6.5(-9) x 1-2 um, appearing stiff, nodulose to strangulate, often dichotomously branched, refringent (PhC); and 2) common hyphal termini (Fic. 24C) otherwise resembling the repent hyphae with similar diverticula. Subpellis including free-form or “antler-shaped” hyphal segments and termini (Fic. 24D-F). Pileus and lamellar tramae loosely interwoven, composed of three hyphal types: 1) hyphae 2.5-6.5(-14) um diam, firm-walled, conspicuously clamped; 2) basically similar but with long, free-form, hyaline, inflated cells <15 um diam; and 3) occasional slender hyphae with thickened walls and dense cytoplasm suggestive of gelatinization. PLEUROCysTIDIA (Fic. 25) abundant to often scattered, 20-35 x 6-9 um, hyaline, fusiform, sharply attenuate distally and occasionally submammillate, conspicuously clamped; contents often vaguely partitioned at very apex. Basidioles (Fic. 26A) clavate; BASIDIA (Fic. 26B-H) 20-28 x 6-7 um, narrowly clavate, not capitulate, 4-sterigmate,
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Fic. 30. Collybiopsis furtiva. (DED 4410; TENN-F-057309). Lower stipe surface. A, B, E. Files of surface lobate branches. D. Two lobate branches with suggestion of slime matrix.
Scale bars = 10 um.
conspicuously clamped. Basipiospores (Fic. 27A) (6-)6.5-9(-10) x 2.5-3(-3.5) um (E= 1.86-3.50; E"=2.75; L"=7.6 um), elongate-ellipsoid, tapered proximally (marasmioid), thin-walled, hyaline, inamyloid. CHEILOCYSTIDIA
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DED 3973.) 008 088 8 S8" CQURSDE DESJARDING ©
Fic. 31. Collybiopsis furtiva. (DED 3973; SFSU-F-024523). Basidiomata. Scale bar = 10 mm. Photo courtesy of DE Desjardin.
(Fic. 28) hyaline, thin-walled, always obscurely clamped, very variable from clavate (<50 x 10-13 um) with scattered diverticula over the apical 15-20 um, shorter (base not seen), branched (branches 6-8 um broad, variably diverticulate) to ventricose-rostrate, stalked (<50 um long) with apical inflation <20 um broad, smooth or beset with diverticula varying from papillate (rotalis-like) to tentacular (<10 x 1-1.5 um). UPPER STIPE MEDULLA consistent with medulla of lower stipe (see below); upper stipe cortical hyphae also similar, but surface lobate branches (Fic. 29) seem consistently simple, knobby, not vermiform, perhaps thick-walled, subrefringent. LowER STIPE MEDULLA in minimal slime matrix. Hyphae of two types: 1) broad, 4—7.5 um diam., hyaline, thick-walled (wall <2.5 um thick with evidence of individual gelatinization), obscurely clamped; and 2) slender, 1.5-3 um diam., firm- to thick-walled, conspicuously clamped, occasionally with incomplete clamps (i.e., small, curved, hook-like branches). No tissue dextrinoid. Lower stipe cortical hyphae (Fic. 20) 3.5-7.5 um diam, thick-walled, pigmented (ochraceous brown), producing small, thickly scattered, hyaline, thin- walled, nodulose to vermiform branches (caulocystidia; Fic. 29) 3.5-6.5 um broad. CauLocystTip1a of two types: 1) digitate or peg-like individuals (Fic. 30A, B, E) arising from cortical hyphae as side branches, 4-13 x 2.5-4 um; and 2) cheilocystidia-like (Fic. 30D), with inflated portions surmounted by numerous lobe-like diverticula.
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Fic. 32. Collybiopsis furtiva. (DED 3973; SFSU-F-024523). Cheilocystidia. A. Cluster of cheilocystidia. B. Clavate individual plus divaricately branched individual.
Scale bars = 10 um.
COMMENTARY: Most synonyms listed under Agaricus ramealis in Index Fungorum are homotypic (i.e., based on Bulliard’s basionym). ‘The European neotype designated by Antonin & Noordeloos (1993; France, Calais, Boulogne, Noordeloos 7310, L) serves to establish the taxonomic basis of these homotypic synonyms. Although numerous subspecies and varieties have been proposed, none have been explicitly based on North American material.
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Fic. 33. Collybiopsis furtiva. (DED 3972; SFSU-F-024523). Ventricose-rostrate cheilocystidia. Note prominent diverticula. Scale bars = 10 um.
In order to reach Marasmiellus ramealis in Desjardin’s (1997) key to the genus in the southern Appalachian Mountains, the following characters are required (some a poor match to the description above): 1) basidiospores <10.5 um long; 2) stipe central, habit marasmioid, collybioid or mycenoid, basidiomata NOT pleurotoid, not on monocots; 3) stipe base NOT attenuated to a narrow point, odor not alliaceous nor fetid; 4) pileipellis a
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well-developed Rameales-structure; 5) pileus pigmented overall (including pinkish brown); 6) rhizomorphs absent; 7) pileipellis lacking inflated terminal cells; 8) pileus yellowish brown vs dark brown to brown (separating from Ma. nodosus); 9) context <1 mm thick (vs. context 2-4 mm thick); 10) stipe 0.2-1 mm diam. (vs. stipe 2-3(-11) mm diam.; 11) basidiospores 2.5-4.5 um broad (vs 4.5-7 um broad); 12) cheilocystidia broadly clavate with numerous fine diverticula (vs cheilocystidia irregular in outline, often contorted, and with nodulose outgrowths); and 13) basidiomata formed on epigeous branches and stems of deciduous trees, shrubs or herbaceous dicots (vs basidiomata formed on hypogeous sticks or roots). According to Desjardin (1997), southeastern North America M. ramealis is most commonly confused with Marasmius (now Mycetinis) opacus with larger basidiomata and plentiful white rhizomorphs and rather different pileipellis (see Petersen & Hughes 2017b). Our observations indicate also a resemblance to Ma. praeacutus, distinguished in the field by its pinched stipe and common, persistent basidiomatal primordia.
Stipe surface ornamentation, especially upper stipe, comprises scattered lobes or nodes, more complex on lower stipe. When simple, such nodules are subrefringent, identical with diverticula of cheilocystidia and especially pileipellis Rameales-structure.
Parenthetically, it is interesting to know Earle’s taxonomic concept of Marasmius ramealis. Specimen Earle 767 (collected on N.Y. Botanical Garden grounds and identified by Earle; NY) may be representative. Although microscopic structures are collapsed, diagnostic characters do not totally agree with those of eastern North American Co. “ramealis” (see above). No attempt has been made to extract DNA.
We need to note here an abnormal collection of Co. furtiva (DED 3973, SFSU-F-024523 as Ma. ramealis), collected in the same general area as several other species. Significantly, its nrITS sequence does not differ from those of several other Co. furtiva collections, yet the basidiomata (Fic. 31) are anatomically distinct, particularly the cheilocystidia and stipe ornamentation. In DED 3973 cheilocystidia (Fics. 32, 33) 45-60 x 9-19 um (at widest point), appear to arise deep in the hymenophoral trama (surely longer than basidia or pleurocystidia); are ventricose-rostrate, stalked with an inflated terminus, and rarely branched; and include scattered small, broadly clavate individuals; the stalks (25-40 x 3-5.5 um) are conspicuously clamped, thin-walled, easily distorted or disarticulated with termini that are inflated, thin-walled, unpigmented, and beset with
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Fic. 34. Collybiopsis furtiva. (DED 3973; SFSU-F-024523). Caulocystidial structures. A. Individual caulocystidia. B-D. Coralloid, cheilocystidial structures. Scale bars = 10 um.
numerous (<70) medusoid diverticula; the slender long diverticula (<25 x 1-1.5 um) are usually elongate-digitate but occasionally dichotomously branched, gnarled, subnodulose, and often apically refringent (PhC). Basidiospores (Fic. 27) are significantly larger than those of Co. furtiva. The stipe ornamentation consists of both individual hyphal caulocystidia and coralloid cheilocystidial structures; individual hyphal caulocystidia
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(Fic. 34A) 6-75 x 5-9 um, thick-walled (wall <2 um thick, pallid greenish ochraceous PhC), sometimes appearing in “picket fence” files, broadly rounded to setoid with sharply acute apex; caulocystidia resembling cheilocystidia (Fic. 34B-D) 15-45 x 9-15 um, coralloid with peg-like or capitulate diverticula, thick-walled (wall <1 um, hyaline). Lower stipe ornamented with accumulated heaps of mixed caulocystidial structures. Probably coincidentally, the submammillate pleurocystidial apices of Co. furtiva resemble those of an unidentified Collybiopsis (TFB 23217; TENN-F-023217) close to Gymnopus subnudus in G. sect. Vestipedes (Fic. 1). Cheilocystidia of DED 3973 resemble those of Co. californica (q.v.) but
our molecular nrITS phylogeny (Fic. 2) places its sequence with other southeastern collections typical of Co. furtiva. Coralloid cheilocystidial stipe vesture elements seem unique.
ADDITIONAL SPECIMENS EXAMINED: USA, GEORGIA, Rabun Co., vic. Clayton,
Warwoman Dell Picnic Area, 34°52’58’N 83°20'58”W, 6/15/1992, coll. SA Gordon,
TFB 4796 (TENN-F-051097). NEw YorK, Bronx Co., “Bronx Woods,’ det. WA Murrill,
VIII.1911 (02755903 NY). NorTH CAROLINA, Macon Co., vic. Highlands, Bull Pen
Rd., 28.VII.1987. coll. TJ Baroni, det. DE Desjardin, DED 4410 (TENN-F-057309);
vic. Highlands, Horse Cove, Rustic Falls area, 12.VII.1984, coll. & det. DE Desjardin,
DED 4584 (SFSU-F-024508); vic. Highlands, Cliffside Lake Campground,
29.VII.1986, coll. & det. DE Desjardin, DED 3973 (SFSU-F-024523); 35°02’24”N
83°27'12”W, 30.VI.2002, coll. RHP, TFB 11558 (TENN-F-059444); vic. Otto, Coweeta
Hydrologic Laboratory, Ball Creek Rd., 26.VI.1993, coll. & det. DE Desjardin, DED
5796 (SFSU-F-024524). TENNESSEE, Blount Co., GSMNP, Cades Cove, 35°35’39”N 83°50'31”W, 15.VI1.1957, coll LR Hesler, TFB 7867 (TENN-F-007867).
Collybiopsis hasanskyensis R.H. Petersen, sp. nov. Figs. 35-41 IF 557072 Differs from other Collybiopsis taxa by its diminutive basidiomata that fruit on Alnus twigs and strobili; its unique ITS sequence; its gymnopoid pileipellis lacking a Rameales-structure; its stalked-clavate, smooth to lobate to diverticulate cheilocystidia that are larger than basidia and pleurocystidia, and its pale buff necropigment.
Type: Russia, Primorsky krai, Hasansky Dist., vic. Primorsky, Kedrovaya Reserve, 43°05.87’N 131°33.57’E, 18.VIII.2005, coll RHP, A. Kovalenko, TFB 11846 (Holotype, TENN-F-060730).
ErymMo.oey: Hasansky; district in Primorsky Region of Russia, where the holotype
was collected. BASIDIOMATA (Fic. 31A) diminutive. PILEUs 4-8 mm broad, plane to somewhat depressed with involute margin, matt, delicately radially wrinkled, inward “pinkish buff” 6A3, outward “pale cinnamon pink’ 5A2, becoming
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Fic. 35. Collybiopsis hasanskyensis. (TFB 11846; TENN-F-060730). A. Basidiomata B. Basidiospores Scale bar: A = 5 mm; B = 5 um.
off-white with pale cantaloupe-colored necropigment; pileus context thin, brittle when dried, white. Hymenophore developing a pallid cantaloupe necropigment. LAMELLAE adnate to shallowly decurrent, subdistant to distant, varying from knife-like and then occasionally ventricose (<0.5 mm broad), to reduced to thin pleats, rarely with dichotomy but often buttressed or cross- veined, color unchanged from fresh (off-white with pinkish tint), L + ll = (22—)36-40, L = (9-)12-16, off-white with pinkish tint. STIPE 6-9 x 0.6-0.8 mm, equal to tapering somewhat upward, sometimes with base slightly enlarged to club-shaped, inserted only at base of club, apically minutely roughened (60x), soon appearing glabrous, now cartilaginous (glabrous- shining), pale apically, “sayal brown” 6C5 to dirty grayish brown downward, developing rich cantaloupe necropigment uniformly, consistently with small, off-white, circular, appressed basal pad. Opor and TASTE negligible. RHIZOMORPHS not observed.
HABITAT & DISTRIBUTION: Fruiting on dead Alnus twigs and strobili; late summer and early autumn; presently known only from Hasansky District of far-eastern Russia near North Korea.
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Fic. 36. Collybiopsis hasanskyensis. (TFB 11846; TENN-F-060730). Pileipellis hyphae. A. Heavy annular ornamentation. B. Weak annular ornamentation. C. Hypha with dense contents. D, E. Roughened, “cigar-shaped” hyphal segments. F. Thick-walled hypha with substantial profile calluses. Scale bar 10 um.
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ON «* 4 . 4 4 na
Fic. 37. Collybiopsis hasanskyensis. (TFB 11846; TENN-F-060730). Lamellar trama. A. Trama, showing inflated hyphae. B. Hyphal fragments with dense contents. Scale bar = 10 um.
PILEIPELLIS a repent layer of hyphae 4.5-13 um diam, of several types: 1) thin-walled, without ornamentation, conspicuously clamped; 2) firm- to thick-walled (wall <1 um thick, hyaline), ornamented (Fic. 36C) with two types of thickening; a) hardly visible in profile but vaguely annular in face view (Fic. 36B); b) prominent in profile view with conspicuous profile calluses (Fic. 36F); profile calluses <1.5 um thick, lens-shaped, hyaline, refringent, conspicuously clamped; 3) disarticulated, somewhat inflated cells, cylindrical or cigar-shaped, thick-walled (wall <1 um thick),
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Fic. 38. Collybiopsis hasanskyensis. (TFB 11846; TENN-F-060730). Hymenial structures. A-D. Pleurocystidia. E-H. Basidia. Note clamp connection in E. Scale bar = 10 um.
delicately ornamented in gregarious plaques (Fic. 36D, E); and 4) repent, thin-walled hyphae 4-8 um diam, heavily ornamented with pigmented plaques, perhaps crystalline, protruding from the hyphal wall angularly <4 um high (Fic. 36A). Note: no evidence of Rameales-structure. Pileus and
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Fic. 39. Collybiopsis hasanskyensis. (TFB 11846; TENN-F-060730). Typical cheilocystidia. Scale bars = 10 um.
lamellar trama interwoven (Fic. 37), more tightly so under hymenophore; hyphae 3-6.5(-14) um diam, firm-walled, hyaline, without slime sheath or matrix, conspicuously clamped. Subhymenial hyphae seem to disintegrate
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Fic. 40. Collybiopsis hasanskyensis. (TFB 11846; TENN-F-060730). Diverticulate cheilocystidia. Scale bars = 10 um.
into debris, persistent after hymenial discharge making observation of basal clamps in the hymenium difficult. Evidence of gelatinization absent. PLEUROCYSTIDIA (Fic. 383A—D) common, not abundant, stalked-fusiform, 19-22 x 9-11 um at widest point, inconspicuously clamped; contents more or less homogeneous, not partitioned. BAsip1a (Fic. 38-H) digitate to clavate but not subcapitulate, 18-23 x 9-11 um, occasionally suburniform, 2-4-sterigmate, inconspicuously clamped; sterigmata slender, lyre-shaped;
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Fic. 41. Collybiopsis hasanskyensis. (TFB 11846; TENN-F-060730). Caulocystidia. Scale bars = 10 um.
contents heterogeneous, multi-granular with amorphous inclusions. BASIDIOSPORES (FIG. 35B) 7-11 x 3.5-4.5(-5.5) um (E = 1.82-2.75; E" = 2.29; L™ = 8.8 um), elongate-ellipsoid, widely rounded distally, tapered proximally (marasmioid), thin-walled, hyaline, inamyloid; contents heterogeneous, foamy (i.e. multiguttulate). CHEILOCYSTIDIA (Fic. 39) abundant at lamellar edge, apparently easily disarticulated from basal septum (i-e., appearing without parent hyphae and with no evidence of clamp connection), firm- to thick-walled (wall <1 um thick, hyaline, usually on emergent portion, not portions juxtaposed to other hymenial elements), very variable in shape from subglobose and without lobes, broadly clavate with expanded distal portion with one or few lobes, to columnar, to stalked with distal portion moderately expanded by with almost equal lobes, to occasionally grown out
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distally to form stout diverticula (Fic. 40); diverticula <40 x 3-5 um, often lobed and occasionally branched; measurements really only approximate because forms are so variable, 30-42(-60) x 7-11 um (at widest point), hyaline, often appearing empty (see photos). STIPE ANATOMY: no apparent differentiation of medullary versus cortical hyphae, all 4-6 um diam, firm-walled (not thick-walled), obscurely clamped, apparently uniformly dextrinoid (cut ends of medullary hyphae just as dextrinoid as corticals); clamp connections, if present, inconspicuous. Stipe surface possibly with very thin slime matrix. Stipe apex with covering of inflated, free-form caulocystidia similar to inflated and distorted pleurocystidia (normal pleurocystidia and cheilocystidia common in this caulocystidial covering, some with tentacular apical outgrowths). CAuLocysTIpDIA (Fic. 41) (15-)20-40(-55) x (3-tentacular outgrowth) 8-14 um, simple inflated utriform structures with almost invisible pedicel to repeatedly constricted “chains,” occasionally a combination of tentacular and constricted structures. Lower stipe glabrous.
ComMMENTARyY: Although Collybiopsis ramealis exhibits a typical Rameales- structure pileipellis (as the archetype of the structure), this construction is not universal even in the Co. ramealis complex. Singer (1973) included nearly 20 Latin American taxa in M. subsect. Ramealini, but several did not exhibit the characteristic setulose repent hyphae and broom cell-like hyphal termini, and some were described as having a trichodermium of “thorny” or setulose hyphae. [Marasmiellus foliiphilus Dutta & al. (2015) was described and illustrated with such a trichodermium.] Likewise, Co. hasanskyensis lacks Rameales-structure in the pileipellis, instead showing typical gymnopoid repent hyphae, often with annular ornamentation.
Fic. 1 (ITS + LSU-based phylogeny) places Co. hasanskyensis sister to Co. vaillantii in the larger clade including Co. eneficola and Co. biformis.
ADDITIONAL SPECIMEN EXAMINED: RUSSIA, PRIMORSKI KRAI, Hasansky Dist., vic. Primorsky, Kedrovaya Reserve, 43°05.87’N 131°33.57’E, 18.VIII.2005, coll. RHP, TFB 11847 (TENN-F-60731).
Collybiopsis minor R.H. Petersen, sp. nov. Figs. 42-49 IF 556206
Differs from other Collybiopsis taxa by its habit on dead Tsuga twigs; its unique ITS rDNA molecular sequences; its pileipellis a repent layer of interwoven, non-diverticulate hyphae, often encrusted with annular deposit; its complete absence of gelatinized tissue; its pallid vestured stipe; and its conspicuously clamped hyphae (including hymenophore elements).
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Fic. 42. Collybiopsis minor. (TFB 11930; TENN-F-059993). Dried basidiomata on Tsuga twigs. Scale bar = 10 mm.
Type: USA, Tennessee, Blount Co., GSMNP, Turkey Pen Ridge trailhead, 35°36’47”N 83°43'37”W 18.VI. 2004, coll. RHP, TFB 11930 (Holotype, TENN-F-059993).
ErymMo.oey: Minor = small, referring to the size of basidiomata.
BASIDIOMATA (Fic. 41) diminutive. PILEus 4-9 mm broad, applanate, usually with down-curved margin, occasionally with shallow umbo, matt; disc and inner limb “army brown” 8D5 to “wood brown” 7C4; outer limb and margin “vinaceous buff” 9B2 to “tilleul buff” 7B2 (in drying remaining not far from “avellaneous” 7B3), not at all sulcate-striate; margin irregular as though eroded. LAMELLAE close (L + Il = 60-68; L = 20-24), adnexed (but without pseudocollarium), thin, subventricose (<1 mm broad), off-white when fresh, drying pallid yellowish with no necropigment; edges entire, somewhat paler than face; lamellulae in 2-3 ranks, plentiful at pileus margin. STIPE 8-15 x 1-1.5 mm, concolorous with pileus (more or less “avellaneous” 7B3) to somewhat more pallid or off-white where vestured, terete, equal or slightly tapering upward (base thicker than apex), lightly stuffed, vestured throughout; stipe base with conspicuous white ruff <0.5 mm high; insertion
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Fic. 43. Collybiopsis minor. (TFB 11930; TENN-F-059993). Pileipellis elements. A. Smooth, repent hyphae (note basidiospore); B. Hyphae with annular ornamentation; C. Hypha with contents appearing oily; D. Slender hyphae with minute roughening; note clamp connection at right. Scale bars = 10 um.
not insititious. RHIZOMORPHS sporadic, white, ropy (not well-defined), associated with resupinate white pad. TasTE and opor negligible.
HABITAT & PHENOLOGY: Four collections known, all fruiting on very slender dead twigs of Tsuga in southern Appalachian Mountains (Tennessee, South Carolina); June-July.
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Fic. 44. Collybiopsis minor. (TFB 11930; TENN-F-059993). Pileipellis and subpellis hyphae. A. Inflated, ornamented hyphal segment of pileipellis; B-D. Slender, meandering hyphae of subpellis, with occasional lobate side branches. Scale bars = 10 um.
PILEIPELLIS an interwoven repent layer with no evidence of slime deposition, constructed of the following: 1) repent, unoriented hyphae 3-8.5 um diam, firm-walled, conspicuously clamped, ranging from smooth (Fic. 43A) to ornamented; ornamentation ranging from a) scattered spiculate “crystals, unoriented; b) annular or striped ornamentation (Fic. 43B) of varying density and width (profile calluses <1 um thick); contents hyaline, speckled (Fic. 43C) as though oily, to dense and then hypha usually slender (Fic. 43D); 2) inflated hyphal segments (Fic. 44A) <16 um diam,
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Fic. 46. Collybiopsis minor. (TFB 11930; TENN-F-059993). A. Basidiole. B-D. Mature basidia. Note non-refringent, heterogeneous contents. Scale bars = 10 um.
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Fic. 47. Collybiopsis minor. (TFB 11930; TENN-F-059993). Cheilocystidia. A. Cluster of three cheilocystidia; B, C, E-G. Cheilocystidia with distal prong-like ornamentation; D. Cheilocystidium with two simple sterigmatoid apical lobes. Scale bars = 10 um.
clavate to keg-shaped, always ornamented with scattered stripes or annular appearance; 3) slender hyphae (Fic. 44B-D), 2.5-4.5 um diam., firm-walled, often meandering, usually delicately ornamented with spiculate deposits, appearing dense (PhC); and 5) rare cheilocystidium-shaped individuals, 34-46 x 5-7.5 uum, appearing to arise below the subpellis and permeate the pileus surface, clavate, stalked, thick-walled (wall <1.5 um thick, hyaline) distally pronged to coarsely divided with apical prongs. PLEUROCYSTIDIA (Fic. 45) abundant, 35-45 x 5-8 um, slender-fusiform to fusiform, hardly discernable from basidioles when immature, conspicuously clamped;
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Fic. 48. Collybiopsis minor. (TFB 11930; TENN-F-059993). Upper stipe caulocystidia. A. Survey. B-E. Individual caulocystidia. Scale bars = 10 um.
contents multiguttulate by maturity. Basidioles (Fic. 46A) 30-37 x 7-9 um (at widest point), clavate, subcapitulate, clamped; contents multiguttulate; BASIDIA (FIG. 46B-D) 30-43 x 7-9 um, clavate, hardly subcapitulate, 4-sterigmate, clamped; contents mottled, hardly guttulate (not refringent). BASIDIOSPORES (Fic. 27) 9-10(-11) x 4-4.5 um (E = 2.00-2.75; E™ = 2.22; L™ = 9.75 um), ellipsoid, flattened adaxially, hardly tapered proximally,
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Fic. 49. Collybiopsis minor. (TFB 11930; TENN-F-059993). Lower stipe caulocystidia. A. Survey. B-E. Individual caulocystidia. Scale bars = 10 um.
smooth, thin-walled, inamyloid. CHEmLocystipia (Fic. 47) plentiful at lamellar edge, broadly clavate to ventricose-rostrate, firm- to thick-walled (wall <0.5 um thick, hyaline), 30-55 x 12-20 um (at widest point); stalk 15-25 x 3.5-5.5 um, obscurely clamped (easily disarticulated); distal
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inflated portion subglobose to broadly clavate, ranging from simply lobed (Fic. 47D) to beset with several prong-like protuberances; contents usually multiguttulate (guttules scattered, usually small, refringent PhC). Upper STIPE MEDULLA with no evidence of slime or gelatinization; medullary hyphae strictly parallel, of two types: 1) 4-8 um diam., thick-walled (wall <1.5 um thick, hyaline), occasionally clamped; 2) 2-3.5 um diam., thick- walled (wall <0.7 um thick, hyaline), sometimes meandering, occasionally clamped. Upper stipe cortex similar, weakly pigmented (straw-colored), producing caulocystidia as side branches; cAuLOcysTIpIA (Fic. 48) 5-35 x 4-10 um (at widest point), papillate, digitate, cylindrical, often swollen at base, not separated from parent hypha by a septum, thick-walled (wall <1.5 um thick, hyaline). Lower sT1PE medulla with no evidence of slime or gelatinization; medullary hyphae free (not in slime matrix), strictly parallel, of two types: 1) 3.5-8 um diam, firm- to thick-walled (wall <0.7 um thick, hyaline), occasionally clamped; and 2) 2-3.5 um diam, appearing dense (PhC), frequently clamped, often branched and with “H”-connections. Lower stipe cortex weakly pigmented (straw-colored); cortical cells 3-4.5 um diam, thick-walled (wall <0.7 um thick), producing caulocystidia (Fic. 49) as side branches; caulocystidia ranging from broadly fusiform (Fic. 49D, E) to stalked and coarsely lobed (Fic. 49A-C) and inflated <14 um broad, thick-walled (wall <0.7 um thick, hyaline), obscurely clamped. Stipe cortex ochraceous-red-brown in IKI + BF.
CoMMENTARY: The holotype collection (about 25 basidiomata), originally identified as Marasmiellus ramealis, was later revised to Ma. stenophyllus. In reality, the pileipellis lacks any Rameales-structure, and tramal tissues are devoid of any slime or gelatinous deposition. Similar (but apparently unrelated) are Marasmiellus synodicus (Kunze ex Fr.) Singer, a European taxon, and Marasmius subsynodicus Murrill, which differs by fruiting on chips and sticks of Pinus, distant lamellae, greenish yellow pileus, smaller spores (4-5 x 2 um, teste Murrill), and more southern distribution. Phylogenetically, Ma. stenophyllus appears as sister to a yet-unnamed taxon (MW386874) and more broadly to Co. quercophila and Co. melanopus.
ADDITIONAL SPECIMENS EXAMINED: USA, NORTH CAROLINA, Jackson Co., vic. Cashiers, trail to Panthertown Valley from Bald Rock, 13.VIII.1993, coll. Nadya Psurtseva & RHP, TFB 10358 (TENN-F-057197). SouTH CAROLINA, Oconee Co., Walhalla Fish Hatchery, trail to Ellicott Rock, 34°52’58”N 83°20'58’W, 29.VII.1993, coll. RHP, TFB 6284 (TENN-F-052933); Burrell’s Ford Campground, 34°52’58”N 83°20'58’W, 12.VIII.2014, coll. HBS class, TFB 14516 (TENN-F-069211).
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Fic. 50. Collybiopsis ramealis. Basidiomata. A. (TFB 14162; TENN-F-067913). B. (TFB 13769; TENN-F-065145). Scale bars = 10 mm.
Collybiopsis ramealis (Bull.) Millsp., West Virginia Geol. Surv. Pt. 1: 127. 1913. Fics 50-60 = Agaricus ramealis Bull., Herb. France 7: tab no. 336 1788, nom. sanct.
NEOTYPE (designated by Antonin & Noordeloos 1993): France, dept. Pas de Calais, Boulogne sur Mer, 14.X.19873, ME Noordeloos 7310, L.
EpityPe (hic designatus, IF 556205.): Belgium, Couvin, Damon, Ardennes Mts., River de Rome, 50°01.45’N 4°32.21’W, 8.[X.2010, coll. A Methven, TFB 13769 (TENN-F-065145).
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Fic. 51. Collybiopsis ramealis. (TFB 14546; TENN-F-069241). Pileipellis elements. A, B, E. Diverticulate hyphae. C, D. Ornamented hyphae. Scale bars = 10 um.
BASIDIOMATA (Fic. 50) diminutive, gregarious to densely gregarious, occasionally in troops, drying to “ochraceous buff” 5A5 to “wood brown” 7C4. PiteEus 3-15 mm broad, matt, shallowly convex to applanate with involute margin, occasionally abruptly umbonate, never umbilicate but irregularly pulvinate, minimally striate at margin, not hygrophanous; disc off-white, “cream buff” 4A4, “light pinkish cinnamon” 7A2, “cinnamon buff” 6B4 to “sayal brown” 6C5, light brown 6D5-6, or paler when young 6D4,“vinaceous buff” 9B2, outward “pinkish buff” 6A3, “pale pinkish cinnamon” 6A2,
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Fic. 52. Collybiopsis ramealis. (TFB 14546; TENN-F-069241). Pileipellis elements; diverticulate hyphal termini. Scale bars = 10 um.
“pale pinkish buff” 6A2 to “tilleul buff” 7B2, sometimes yellowing in age (orange white 5A2 disc, margin 4A2). LAMELLAE subdecurrent (and then ending abruptly on stipe), adnexed to adnate to appearing free, more or
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Fic. 53. Collybiopsis ramealis. (TFB 14546; TENN-F-069241). Inflated subpellis hyphae. Note prominent clamp connections. Scale bars = 10 um.
less arcuate, not ventricose, seceding slightly when dried to appear free or pseudocollariate, 0.7-1 mm broad, distant, subdistant to close, (L + Il = 40-43, L = 11-14), thickish, usually concolorous with pileus surface, off-white to “pale pinkish buff” 6A2, “warm buff” 5A4, “pale pinkish cinnamon” 6A2, “pinkish buff” 6A2 with white edge, occasionally suffusing to “light pinkish cinnamon” 7A2 sometimes yellowing in age to “cartridge buff” 30A2 and tending toward crisping in older basidiomata; buttressing rare; anastomosis absent. In normal pilei, hymenophore taking on a fleshy necropigment upon drying. STIPE 6-20 x 1-2 mm broad at apex, equal and remaining so or tapering downward to 0.5-0.8 mm broad at base, inflated apically, there “pale pinkish cinnamon” 6A2, to concolorous with lamellae and minutely flocculose, downward “cream buff” 4A4, “sayal brown” 6C5, “cinnamon buff” 6D4, “vinaceous buff” 9B2, “pinkish cinnamon” 7B5, to “clay color” 5C6, at base “cinnamon buff” 6D4 or “wood brown” 7C4, sometimes yellowing 4A2, “yellow ocher” (orange-white 5A2) and then suffusing light brown 6D4 to brownish orange 6C7, in age occasionally suffusing fleshy cream to “Pompeian red” 10C6 toward base, smooth, without basal pad.
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Fic. 54. Collybiopsis ramealis. (TFB 14163; TENN-F-067913). Lamellar trama; diverticulate hyphae. Scale bars = 10 um.
OpDoR sometimes weakly of garlic or fresh but otherwise negligible; TASTE not distinctive.
HABITAT & PHENOLOGY: Hardwood (at least Fagus or Quercus), occasionally on Rubus canes, Crataegus or other woody substrates, rotting wood, branches, twigs and bark; Europe including Scandinavia and Caucasus; late Summer, early Autumn.
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Fic. 55. Collybiopsis ramealis. (TFB 14573; TENN-F-069270). Lamellar trama; inflated hyphal segments and termini. Scale bars = 10 um.
PILEIPELLIS constructed of the following elements: 1) erect filamentous hyphae emerging from subpellis, 25-50 x 4-5 um, equal to subtly subcapitulate, hyaline, firm-walled, arising as side branches from repent hyphae; 2) antler-shaped hyphae 3—7(-10) um diam, branched more or less at right angles, often ending in short, blunt, divaricate spurs (tibiiform; Rameales-structure; Fic. 51A, B); 3) as above but distinctly ornamented in
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Fic. 56. Collybiopsis ramealis. (TFB 14546; TENN-F-069241). Pleurocystidia. Note prominent clamp connection in C. Scale bars = 10 um.
annular or striped configuration (Fic. 51C, D), always in short lengths; 4) repent hyphae 4—8 um diam, beset with closely scattered thumb shaped to digitate setulae 1-4 x 0.7-1.0 um, (Fic. 52B, E) apparently as interseptal hyphal lengths and also as hyphal termini, and then more or less broom cell-like shapes (Fic. 52); setulae as above, often with refringent tips (PhC). Subpellis hyphae loosely interwoven without evidence of slime matrix or sheath, 3.5-15 um diam (Fic. 53), thin- to firm-walled, conspicuously clamped. Pileipellis near pileus margin a coarse Rameales-structure, setulae coarser, knobby, not papillate, closely scattered. Lamellar trama loosely interwoven; hyphae include scattered diverticulate (Fic. 54) and antler-shaped divaricate elements (Fic. 55). PLEUROCYSTIDIA (Fic. 56) 24-33 x 6-7.5 um, common to scattered but not normally abundant, digitate (and then difficult to distinguish from basidioles) to narrowly fusiform, conspicuously clamped; contents heterogeneous with scattered granules and often 1-2 refringent inclusions (PhC). Basidioles (Fic. 57A)
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Fic. 57. Collybiopsis ramealis. (TFB 13755; TENN-F-065145). A. Basidiole. B-D. Basidia. E-H. Basidiospores. Scale bars: A~D = 10 um, E-H = 5 um.
clavate to subcapitulate. Basip1a (Fic. 57B-D) 26-32 x 7-8.5 um, clavate to subtly subcapitulate, 4-sterigmate (sterigmata very slender, easily collapsed), conspicuously clamped; contents heterogeneous with scattered
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Fic. 58. Collybiopsis ramealis. (TFB 14573; TENN-F-069270). Clavate cheilocystidia. Scale bars = 10 um.
granules. BAsIDIOsPORES (Fic. 57E-H) (6—-)7-10(-11.5) x 2.5-4(-4.5) um (E= 1.76-3.20; E™ = 2.39; L™ = 8.61 um), slender ellipsoid, marasmioid (tapered proximally), thin-walled, inamyloid; contents 2-3-guttulate to minutely heterogeneous, appearing foamy. CHEILOCYSTIDIA (FIGs. 58-60) (27-)50-84 x 12-22 um (at widest point), thickly scattered, often appearing as pseudocystidia (i.e. arising in subhymenium, not in hymenium), ranging from clavate (Fic. 58) to typically long ventricose- rostrate to spheropedunculate with apical setulae (Fic. 59, 60), but occasionally misshapen (Fic. 60), thin- to firm-walled; inflated distal portion pigmented (dark ochraceous, PhC); apical outgrowths ranging from papillate to tentacular/coralloid, apparently flexuous (diverticula, not setulae); stalk slender (1.5-2.5 um diam), clamped; contents heterogeneous with scattered minute granular aspect. Occasional cheilocystidia clavate (12-15 um broad, not ventricose-rostrate), beset with scattered papillate setulae. STIPE MEDULLARY HYPHAE strictly parallel, easily extruded in squash mounts, of two types: 1) 4-9 um diam, thick-walled (wall <1 um thick, hyaline), conspicuously clamped; and 2) 1-2.5 um diam, thin- to firm-walled, widely clamped. STIPE CORTICAL HYPHAE 3-6 um diam, thick-walled, weakly pigmented (straw-colored PhC), often papillate on outside wall; papillae 0.5-2 x 1 um, hyaline, thick-walled. Stipe surface
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Fic. 59. Collybiopsis ramealis. (TFB 14573; TENN-F-069270). Ventricose-rostrate cheilocystidia. Scale bars = 10 um.
ornamented with utriform to lobate cells arising as thin-walled termini of surface cortical hyphae, 5-10 um diam. Upper stipe clothed in the following: 1) typical hymenium of basidia, basidioles and occasional pleurocystidia; 2) relatively normal cheilocystidia, but often distorted into odd shapes; and 3) modified cheilocystidia (distinguished by heterogeneous contents and
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Fic. 60. Collybiopsis ramealis. (TFB 14546; TENN-F-069241). Aberrant clavate cheilocystidia. Scale bars = 10 um.
very slight pigmentation) into elongate clavate structures 9-13(-19) um diam (at widest point), appearing as pseudocystidia, smooth to (rarely) beset with apical knobby to coralloid diverticula, firm- to thick-walled (wall <1.0 um thick, hyaline), with basal clamp connection.
COMMENTARY: Bulliard’s illustration clearly shows decurrent, arcuate lamellae (his fig. A) perhaps seceding (his fig. B).
Cheilocystidia of all examined European specimens were pigmented. The pigment is cytoplasmic; the wall is hyaline. Contents are heterogeneous,
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appearing oily with inclusions (PhC). Contents of basidioles and pleurocystidia are homogeneous but contents of mature basidia are heterogeneous, multigranular with a few small refringent guttules. Based on long pedicel stalks, cheilocystidia seem to arise deep in lamellar trama and project through the lamellar edge. This morphology has been termed “pseudocheilocystidia” (Singer 1968).
Copious spores seem to lodge on lamellar surfaces, especially at the lamellar edge. Other than the projections from cheilocystidial apices, there seems not to be a physical attraction. Spores are usually 2-guttulate; guttules polar (at proximal and distal ends of the spore), and refringent.
While the lamellar edge appears smooth at low magnification, it is delicately serrulate at 250x, with pigmented cheilocystidia appearing dark near or at the lamellar edge.
Stipes vary from terete and equal to compressed and tapering downward to a fine insertion reminiscent of that of Marasmiellus praeacutus (see Halling 1987).
Self-crosses were performed on collections TENN-F-052628 (Sweden), TENN-F-065120 (Belgium), TENN-F-065122 (Belgium), TENN-F-065132 (Belgium), and TENN-F-065165 (Belgium). All self-crosses showed tetrapolar mating systems. An intercollection pairing grid developed from single-basidiospore isolates from the Belgian collections showed all collections to be intercompatible, indicating that all belonged to a single mating group.
Earle’s explicit assignment of Marasmius ramealis as type of his genus Collybiopsis did not constitute valid publication of the nomenclatural combination Collybiopsis ramealis (ICN Shenzhen Art, 36:2, see also Antonin & Noordeloos 2010: 316), although his intent was indisputable. Millspaugh (1913) made the earliest valid publication of Collybiopsis ramealis.
There remains a question about Earle’s (1909) use of the AMERICAN CODE OF BOTANICAL NOMENCLATURE (1904, 1907), of which he was a signee, especially Canon 15, embodying the “first species rule.” Earle’s 1909 effort was intended to be explicitly and exclusively taxonomic, not nomenclatural. In his prose summary he does not mention typification or his method of arriving at the type species of the genera in his generic summary. A search of “Tribe I. Agaricaceae §1. Gymnophylli” (Earle, pp 411-433) covering 73 genera reveals that the preponderance of genera were typified by the first (often the only) species listed in the generic protologue. But in the following, a non-first species was chosen: Anthracophyllum, Leptomyces, Prunulus,
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Omphalina, Pilacre, Lepista, Phylloporus, and Melanoleuca. Earle’s mechanical use of “The first species rule” (explicit or implicit) cannot be upheld.
But although Earle was not slavish to “the first-species rule” regarding the protologue of the various genera, he was, indeed, slavish in citing Saccardos Sylloge Fungorum (Vol. 5, covering the agarics). In the various assemblages that Earle recognized as represented in Sylloge, Saccardo’s first species do not appear to have been selected as generic types for Earle’s genera.
SPECIMENS EXAMINED: BELGIUM, Dimonte, vic. Hever, Jemain, Massembre, 50°09°37’N 4°51’29’E, 7.1X.2010, coll. AS Methven, TFB 13755 (TENN-F-065120); coll. S Adam¢éik, TFB 13745 (TENN-F-065122); vic. Heer, Bois de Baroville, vic. Beauraina, 9.I[X.2010, coll. RHP, TFB 13775 (TENN-F-065151); coll. RHP, TFB 13590 (TENN-F-065165); Couvin, Damon, Ardennes Mts., River de Rome, 50°01.45’N 4°32.21’E, 8.1X.2010, coll. A Methven, TFB 13770 (TENN-F-065146). GERMANY, THURINGIA, vic. Obergebra, off Rte 1016, 51°24.13’N 10°36.05’E, 30.VHIL.2012, coll. RHP, TFB 14162 (TENN-F-067912); TFB 14163 (TENN-F-067913); vic. Menteroda, 51°18.18’N 10°33.52’E, 28. VIII.2012, coll. AS Methven, TFB 14140 (TENN-F-067890); Grosslohram vic Nohra, 51°24.40’N 10°36.88’E, 29.VIII.2012, coll. KWH, TFB 14150 (TENN-F-067900). SLOVAKIA, Nitra, Prostredny Vrich, Lovce, 48°27'04”N 18°20'49”E, 12.1X.2014, coll. RHP TFB 14573 (TENN-F-069270); Zlate Maravce Dist., vic. Hostie, 48°27’59”"N 18°27’35”E, 10.1X.2014, coll A.S. Methven, TFB 14555 (TENN-F-069255); coll A.S. Methven, TFB 14546 (TENN-F-069241). SWEDEN, NARKE, Hjalmarsbaden, Ostra Hagen, 59°16.07’N 15°19.07’E, 10.1X.2008, coll. RHP, TFB 13520 (TENN-F-062867); HALLAND, Toto Parish, 56°54’19"N 12°47’23”E, 24.1X.1991, coll. SA Gordon, RHP, Stig Jacobsson, TFB 4727 (TENN-F-050324); UPPLAND, vic. Uppsala, Fiby Urskog, 59°52’54”N 17°21'13”E, 8.1X.1994, coll. RHP, TFB 7288 (TENN-F-053525); vic. Uppsala, 31X.1994, coll. unknown, TFB 7248 (TENN-F-052628). UNITED KINGDOM, PERTHSHIRE, Pitlochry, Beach Walk along River Garry & vicinity, 56°42’16”N 3°43’47’W, 2.1X.1997, coll. RHP, TFB 6989 (TENN-F-055908).
Discussion
In future taxonomic investigations, some taxa heretofore described as Marasmiellus will be authoritatively sequenced and as a result, will remain securely within Collybiopsis. Other sequenced taxa, however, will not remain in Collybiopsis, with destinations (e.g., Marasmiaceae, Physalacriaceae) unpredictable. For example, taxa within Marasmiellus sect. Candidi, Ma. sect. Stenophylloides, and Ma. sect. Nigripedes (= Tetrapyrgos) seem destined for Marasmiaceae (not Omphalotaceae-Collybiopsis, where Marasmiellus juniperinus belongs). If done carefully, this process will be slow and piecemeal, inviting caution in blanket transfers.
Here it might be noted that Pegler & Young (1971) cited a specimen of Ma. juniperinus from Jamaica (Jamaica, Blue Mountains, 26.XII.1949,
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Proctor: K). DNA sequences from this specimen might furnish a more secure (topotype) connection for the type of Marasmiellus.
The phylogenetic position of Marasmiellus juniperinus is unstable and not well-supported by either Olivera & al. (2019) or our analyses. The Olivera & al. (2019) analysis associated Ma. juniperinus with TENN-F-068185 (TFB14334; Gymnopus sp. 17) and TENN-F-068085 (TFB14228; Gymnopus sp.) but without support. Our current analysis associates Ma. juniperinus with Co. quercophila and Co. melanopus, again without support. The underlying cause is that its ITS sequence diverges from the rest of the sequenced taxa in Collybiopsis but does not clearly belong elsewhere based on its DNA sequences.
Despite the literature summary presented above (see Introduction), Singer's (1962) acceptance of Marasmiellus over Collybiopsis is instructive. For many years during the early 20" century an expanded concept of Marasmius was accepted, including numerous taxa whose micromorphology did not fully conform to the present circumscription of the genus. Kiihner’s (1933, 1936) treatments were especially influential. Both Marasmiellus and Collybiopsis were overlooked as candidates for atypical “Marasmius” taxa. In addition, they were also overlooked by some authors (notably Clements & Shear 1931, 1954) who selected type species for many genera. During these years, Singer (1938) used Hemimycena for a group of agarics he considered to be without a previous home. It was only later (Singer 1950) when he realized that Marasmiellus Murrill 1915 took priority over Hemimycena Singer 1938 that Marasmiellus came into Singer’s purview. In a nomenclatural study of the genera of Agaricales, Donk (1962) summarized the history of Collybiopsis to that date. There he named a “selected” type species as Agaricus calopus. By 1962, Singer had accepted 59 taxa within Marasmiellus and, whether before or after Donk’s publication, Singer also listed Agaricus calopus as type of Collybiopsis. The two authors’ choice superseded Earle’s explicit citation of the generic type for Collybiopsis (also distorting Earle’s intent), thus steering Collybiopsis away from contention for priority over Marasmiellus. Both authors, however, also reported that the taxonomic concept of A. calopus itself was anything but secure, concluding that A. calopus was a “nomen dubium.’ Singer went one step further: if A. calopus was a “nomen dubium,” then Collybiopsis was also a “nomen dubium.’ Singer (1962: 417-418) included Collybiopsis under “genera imperfectly known,’ We contend that Collybiopsis is in no way a dubious name, having been explicitly established by Earle (1909).
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Acknowledgements
We extend our sincere thanks to three anonymous reviewers whose comments and suggestions made this version of the original manuscript stronger. Dr. Else Vellinga caught some substantive errors. Dr. Jerry Cooper, Landcare Research, New Zealand, provided the Millspaugh paper as well as other valuable suggestions. The Mycotaxon Editors excelled in correcting confusing text and formatting and nomenclatural shortcomings; they are sincerely thanked.
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APPENDIX |
Collybiopsis recombinations proposed
The correct name for the large clade considered here is Collybiopsis, which includes the type species of Marasmiellus (M. juniperinus), as well as the type species of Gymnopus sect. Vestipedes (G. confluens). Many epithets of appropriate binomials require transfer to Collybiopsis. Oliveira & al. (2019) made numerous transfers to Marasmiellus but, while we do not disagree with the taxonomy of these transfers, we argue that they are nomenclaturally incorrectly combined in Marasmiellus and not Collybiopsis. The list of corrected transfers below includes such species epithets with which we have experience but not those which we contend require additional investigation. Based on Fic. 1 (ITS + LSU-based phylogeny), appropriate epithets include those below, but as accurate phylogenetic placement of Marasmiellus and Gymnopus taxa (and some Marasmius) is determined, additional transfers will be necessary.
Collybiopsis biformis (Peck) R.H. Petersen, comb. nov. IF 556182 BastonyM: Marasmius biformis Peck, Bull. 1904 [“1903”]. N.Y. State Mus. 67: 25. = Marasmiellus biformis (Peck) J.S. Oliveira. 2019. Mycol. Prog. 18(4): 734.
Collybiopsis brunneigracilis (Corner) R.H. Petersen, comb. nov. IF 557078 BastonyM: Marasmius brunneigracilis Corner. 1996. Nova Hedwigia, Beih. 111: 39. = Gymnopus brunneigracilis (Corner) A.W. Wilson, Desjardin, E. Horak. 2004. Sydowia 56(1): 171. = Marasmiellus brunneigracilis (Corner) J.S. Oliveira. 2019. Mycol. Prog. 18(5): 734.
Collybiopsis confluens (Pers.) R.H. Petersen, comb. nov. IF 556183 BASIONYM: Agaricus confluens Pers. 1796. Observ. Mycol. 1: 8. = Marasmiellus confluens (Pers.) J.S. Oliveira. 2019. Mycol. Prog. 18: 734.
Collybiopsis dichroa (Berk. & M.A. Curtis) R.H. Petersen, comb. nov. IF 556184 BastonyM: Marasmius dichrous Berk. & M.A. Curtis. 1853. Ann. Mag. Nat. Hist. 2 12: 426. = Marasmiellus dichrous (Berk. & M.A. Curtis) J.S. Oliveira. 2019. Mycol. Prog. 18: 734.
Collybiopsis diminuta (Berk. & Broome) R.H. Petersen, comb. nov. IF 56185 BasionyM: Agaricus diminutus Berk. & Broome. 1871. J. Linn. Soc., Bot. 11: 251.
Collybiopsis disjuncta (R.H. Petersen & K.W. Hughes) comb. nov.
IF 556777 BASIONYM: Gymnopus disjunctus R.H. Petersen & K.W. Hughes. 2014. N. Am. Fung. 9: 2. = Marasmiellus disjunctus (R.H. Petersen & K.W. Hughes) J.S. Oliveira. 2019. Mycol. Prog. 18: 734.
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Collybiopsis eneficola (R.H. Petersen) R.H. Petersen, comb. nov. IF 556186 BASIONYM: Gymnopus eneficola R.H. Petersen. 2014. Omphalina 5(5): 5. = Marasmiellus eneficola (R.H. Petersen) J.S. Oliveira. 2019. Mycol. Prog. 18: 734.
Collybiopsis fibrosipes (Berk. & M.A. Curtis) R.H. Petersen, comb. nov. IF 557077 BastonyM: Marasmius fibrosipes Berk. & M.A. Curtis. 1869. J. Linn. Soc. Bot. 10: 293. = Collybia fibrosipes (Berk. & M.W. Curtis) Dennis. 1951. Trans. Brit. Mycol. Soc. 34(4): 448 = Gymnopus fibrosipes (Berk. & M.A. Curtis) J.L. Mata. 2003 Mycotaxon 86: 315.
Collybiopsis foliiphila (A.K. Dutta, K. Acharya & Antonin) R.H. Petersen, comb. nov. IF 557080 BastonyM: Marasmiellus foliiphilus A.K. Dutta, K. Acharya & Antonin. 2015. Mycol. Prog. 14: 5.
Collybiopsis gibbosa (Corner) R.H. Petersen, comb. nov. IF 556187 BastonyM: Marasmius gibbosus Corner. 1996. Nova Hedwigia, Beih. 111: 53. = Marasmiellus gibbosus (Corner) J.S. Oliveira. 2019. Mycol. Prog. 18: 734.
Collybiopsis indocta (Corner) R.H. Petersen, comb. nov. IF 556188 BastonyM: Marasmius indoctus Corner. 1996. Nova Hedwigia, Beih. 111: 60. = Marasmiellus indoctus (Corner) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
Collybiopsis juniperina (Murrill) R.H. Petersen, comb. nov. IF 556189 BastonyM: Marasmiellus juniperinus Murrill. 1915 N. Am. Fl. 9(4): 243.
Collybiopsis luxurians (Peck) R.H. Petersen, comb. nov. IF 556190 BastonyM: Collybia luxurians Peck. 1897. Bull. Torrey Bot. Club 24: 141. = Marasmiellus luxurians (Peck) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
Collybiopsis melanopus (A.W. Wilson, Desjardin & E. Horak) R.H. Petersen, comb. nov. IF 556191 BasIonyM: Gymnopus melanopus A.W. Wilson, Desjardin & E. Horak. 2004. Sydowia 56: 181 = Marasmiellus melanopus (A.W. Wilson, Desjardin & E. Horak) J.S. Oliveira. 2019. Mycol. Prog. 18: 735
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Collybiopsis menehune (Desjardin, Halling & Hemmes) R.H. Petersen, comb. nov. IF 556192 BASsIONYM: Gymnopus menehune Desjardin, Halling & Hemmes. 1999. Mycologia 91(1): 173. = Marasmiellus menehune (Desjardin, Halling & Hemmes) J.S. Oliveira. 2019. Mycol. Prog. 18: 375.
Collybiopsis mesoamericana (J.L. Mata) R.H. Petersen, comb. nov. IF 556193 BASIONYM: Gymnopus mesoamericanus J.L. Mata. 2006. Sydowia 58(2): 283. = Marasmiellus mesoamericanus (J.L. Mata) J.S. Oliveira. 2019. Mycol. Prog. 19: 735.
Collybiopsis micromphaloides (R.H. Petersen & K.W. Hughes) R.H. Petersen, comb. nov. IF 556778 BasionyM: R.H. Petersen & K.W. Hughes. 2014. N. Am. Fungi 9: 6. = Marasmiellus micromphalioides (R.H. Petersen & K.W.Hughes) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
Collybiopsis neotropica (Singer) R.H. Petersen, comb. nov. IF 556942 BastonyM: Collybia neotropica Singer. 1962 [“1961”]. Sydowia 15: 54. = Gymnopus neotropicus (Singer) J.L. Mata. 2003. Mycotaxon 86:313. = Marasmiellus neotropicus (Singer) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
Collybiopsis nonnulla (Corner) R.H. Petersen, comb. nov. IF 556194 BastonyM: Marasmius nonnullus Corner. 1996, Nova Hedwigia, Beih. 111: 76. = Marasmiellus nonnullus (Corner) J.S. Oliveira 2019, Mycol. Prog. 18: 735.
Collybiopsis obscuroides (Antonin & Legon) R.H. Petersen, comb. nov.
IF 556943 BaAsIONYM: Gymnopus obscuroides Antonin & Legon. 2008. Czech Mycol. 60: 14.
Collybiopsis parvula (J.L. Mata, R.H. Petersen & K.W. Hughes) R.H. Petersen, comb. nov. IF 556779 BASIONYM: Gymnopus parvulus J.L. Mata, R.H. Petersen & K.W. Hughes. 2007. Sydowia 58(2): 285. = Marasmiellus parvulus (J.L. Mata, R.H. Petersen & K.W. Hughes) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
Collybiopsis peronata (Bolton) R.H. Petersen, comb. nov. IF 556195 Bastonym: Agaricus peronatus Bolton. 1788. Hist. Fung. Halifax 2: 58. = Marasmiellus peronatus (Bolton) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
344 ... Petersen & Hughes
Collybiopsis polygramma (Mont.) R.H. Petersen, comb. nov. IF 556944 BastonyM: Marasmius polygrammus Montagne. 1854. Ann. Sci. Nat, Bot. ser. 4 1: 118. = Gymnopus polygrammus (Mont.) J.L. Mata. 2003. Mycotaxon 86: 313. = Marasmiellus polygrammus (Mont.) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
Collybiopsis pseudoluxurians (R.H. Petersen & K.W. Hughes) R.H. Petersen, comb. nov. IF 556196 BASIONYM: Gymnopus pseudoluxurians R.H. Petersen & K.W. Hughes. 2014, N. Am. Fung. 9(3): 7. = Marasmiellus pseudoluxurians (R.H. Petersen & K.W. Hughes) J.S. Oliveira. 2019. Mycol. Prog. 19: 736
Collybiopsis quercophila (Pouzar) R.H. Petersen, comb. nov. IF 556197 BastonyM: Marasmius quercophilus Pouzar. 1982. Ceska Mykol. 36(1): 1. = Marasmiellus quercophilus (Pouzar) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
Collybiopsis readiae (G. Stev.) R.H. Petersen, comb. nov. IF 556945 BASIONYM: Crinipellis readiae G. Stev. 1964. Kew Bull. 19(1): 43. = Gymnopus readiae (G. Stev.) J.L. Mata. 2007. Sydowia 58: 289.
Collybiopsis stenophylla (Mont.) R.H. Petersen, comb. nov. IF 557079 BastonyM: Marasmius stenophyllus Mont. 1854. Ann. Sci. Nat., Bot.Ser. 4 1: 116. = Marasmiellus stenophyllus (Mont.) Singer. 1962. Sydowia 15: 58. = Gymnopus stenophyllus (Mont.) J.L. Mata & R.H. Petersen. 2004. Mycoscience 45(1): 221.
Collybiopsis subcyathiformis (Murrill) R.H. Petersen, comb. nov. IF 556946 BastonyM: Marasmius subcyathiformis Murrill. 1915. N. Amer. Fl. 9(4): 269. = Marasmiellus subcyathiformis (Murrill) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
= Gymnopus subcyathiformis (Murrill) Desjardin, Halling & Hemmes. 1999, Mycologia 91: 175.
Collybiopsis subnuda (Ellis ex Peck) R.H. Petersen, comb. nov. IF 556198 BastonyM: Marasmius subnudus Ellis ex Peck. 1898. Bull. Torrey Bot. Club 25: 287. = Marasmiellus subnudus (Ellis ex Peck) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
Collybiopsis subpruinosa (Murrill) R.H. Petersen, comb. nov. IF 556199 BastonyM: Marasmius subpruinosus Murrill. 1915. N. Amer. Fl. 9: 266. = Marasmiellus subpruinosus (Murrill) J.S. Oliveira. 2019. Mycol. Prog. 18: 735.
Collybiopsis resurrected ...
Collybiopsis synodica (Kunze ex Fr.) R.H. Petersen, comb. nov. IF 556200
BASIONYM: Agaricus synodicus Kunze ex Fr. 1830. Linnaea 5: 507.
Collybiopsis termiticola (Corner) R.H. Petersen, comb. nov. IF 556201 BastonyM: Marasmius termiticola Corner. 1996. Nova Hedwigia. Beih. 111: 101. = Marasmiellus termiticola (Corner) J.S. Oliveira. 2019. Mycol. Prog. 18: 736.
Collybiopsis vaillantii (Pers.) R.H. Petersen, comb. nov. IF 556202 BASIONYM: Agaricus ericetorum B vaillantii Pers. 1801. Syn. Meth. Fung. 2: 472.
Collybiopsis villosipes (Cleland) R.H. Petersen, comb. nov. IF 556203 BastonyM: Marasmius villosipes Cleland. 1934. Toadstools Mushrooms S. Austral. 1: 166. = Marasmiellus villosipes (Cleland) J.S. Oliveira. 2019. Mycol. Prog. 18: 736.
345
346 ... Petersen & Hughes
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MYCOTAXON
ISSN (print) 0093-4666 (online) 2154-8889 Mycotaxon, Ltd. ©2021
April-June 2021— Volume 136, pp. 351-357 https://doi.org/10.5248/136.351
Parathozetella microsperma gen. & sp. nov. from the Brazilian Amazon
FLAVIA RODRIGUES BARBOSA’, PATRICIA OLIVEIRA FIUZA?, JOSIANE SANTANA MONTEIRO?, ALEXANDRE PEREIRA DA SILVA}, Luis FERNANDO PASCHOLATI GUSMAO’‘, RAFAEL FELIPE CASTANEDA-RUIZ5
"Instituto de Ciéncias Naturais, Humanas e Sociais, Universidade Federal de Mato Grosso, Ay. Alexandre Ferronato, 1200, 78557-267, Sinop, Brazil
? Programa de Pés-graduacdo em Sistemdtica e Evolucdo, Universidade Federal do Rio Grande do Norte, Campus Universitario, Av. Senador Salgado Filho, 3000, Lagoa Nova, 59078-970, Natal, Brazil
> Museu Paraense Emilio Goeldi, Coordenagdao de Botdnica, Av. Perimetral, 1901 - Terra Firme, Belém, 66077-830, Belém, Brazil
‘Universidade Estadual de Feira de Santana, Programa de Pés-graduacdo em Botanica, Av. Transnordestina s/n, Novo Horizonte, 44036-900, Feira de Santana, Brazil
° Instituto de Investigaciones Fundamentales en Agricultura Tropical ‘Alejandro de Humboldt’ (INIFAT), Académico Titular de la Academia de Ciencias de Cuba, Calle 1 Esq. 2, Santiago de Las Vegas, C. Habana, Cuba, C.P. 17200
* CORRESPONDENCE TO: patyfiuzabio@gmail.com
ABSTRACT—A new genus and species of asexual ascomycete, Parathozetella microsperma, are described and illustrated from decaying plant material collected from three rainforest areas in Mato Grosso and Para States. The new genus resembles Thozetella in sporodochial conidiomata, presence of microawns, and enteroblastic monophialidic conidiogenesis that produces lunate conidia, but Parathozetella can be easily distinguished by the absence of setulae.
KEY worDs—Ascomycota, saprobic fungi, taxonomy, tropical fungi
Introduction The Amazon biome, in addition to its great species richness, is also characterized by its high rate of endemism and highly diverse ecosystems
352 ... Barbosa & al.
(Verissimo & al. 2011). The fungal community found on dead and decaying forest litter is crucial for decomposing the organic matter in soil by providing energy and maintaining a nutritional balance. Among the decomposers, asexual ascomycetes are the most common fungi that decompose different plant substrates in both terrestrial (Costa & Gusmao 2016, Santos & al. 2018) and aquatic habitats (Fiuza & al. 2019, Silva & al. 2014).
Data on fungi in the Amazon currently underestimate diversity due to insufficient research (Monteiro & al. 2019, Sotao & al. 2004). Obtaining an accurate assessment of Amazonian biodiversity is further complicated by the threat to the ecosystem caused by the high rate of deforestation and resulting habitat fragmentation (Magnusson & al. 2013). Approximately 200 asexual ascomycete species have been registered in the Brazilian Amazon in the states of Para (Castro & al. 2012, Monteiro & al. 2013, Santos & al. 2018), Amazonas (Cortez al. 2016, Fiuza & al. 2015), Amapa (Carmo & al. 2014), and Mato Grosso (Barbosa & al. 2015; 2017). Asexual ascomycetes have also been reported in the Amazon from Peru (Matsushima 1993, Zelski & al. 2014) and Ecuador (Matsushima 1993). As many Amazonian species have yet to be discovered, inventory work is encouraged and essential before we lose these precious forests due to anthropogenic factors such as habitat fragmentation and climate change. Our research team, which has focused on the Brazilian Amazon, has discovered many interesting taxa (Barbosa & al. 2015, 2017, 2019, Fiuza & al. 2015, Monteiro & al. 2013). One survey of asexual ascomycetes on plant debris in Amazonia revealed an interesting sporodochial conidioma- producing fungus with microawns and conidia but lacking setulae. While similar to Thozetella Kuntze, the fungus lacked the setulae that characterize this genus. Réblova & Winka (2000) demonstrated the importance of setulae in separating Dictyochaeta Speg. and Codinaea Maire, a concept supported by Seifert & al. (2011) and Li & al. (2012). Thus, we use the absence of setulae to propose a new genus for the previously undescribed fungus from the Brazilian Amazon.
Materials & methods
Expeditions were carried out to three sites at the Brazilian Amazon rainforest: Claudia, Mato Grosso (11934’54”S 55°17’15”W), Parque Nacional do Utinga, Belém, Para (1°23’13”S 48°25’19”W), and Assentamento Rio Vermelho, Santa Barbara do Para, Para (1°10°58”S 48°11’43”W) to collect decaying wood and petioles. Samples were placed in paper bags and taken to the laboratory at Universidade Federal de Mato Grosso (UFMT-Sinop) and Museu Paraense Emilio Goeldi, Para for processing following Castafieda-Ruiz & al. (2016). Permanent slides were prepared in PVL resin
Parathozetella microsperma gen. & sp. nov. (Brazil) ... 353
(polyvinyl alcohol, lactic acid, and phenol) and reproductive structures were measured and photographed under a Leica DM 500 microscope with a coupled digital camera. The holotype was deposited in the Herbario Centro-Norte Mato-Grossense, Sinop, Mato Grosso state, Brazil (CNMT), and additional materials in the Herbario Joao Murga Pires, Belém, Para state, Brazil (MG). Several attempts to obtain this species in pure culture were unsuccessful.
Taxonomy
Parathozetella ER. Barbosa, J.S. Monteiro, Fiuza, R.F. Castafeda & Gusmao, gen. nov. MB 834624
Differs from Thozetella by the absence of setulae on conidia.
TyPE SPECIES: Parathozetella microsperma ER. Barbosa & al.
ErymMo.oey: Latin, Para- referring to similar; and -thozetella, referring to the genus
Thozetella MycELIvum superficial and immersed, composed of slightly branched, septate, smooth, pale brown hyphae. Conipromarta sporodochial, superficial, scattered, brown. CONIDIOPHORES macronematous, septate, cylindrical, smooth, pale brown to brown. CONIDIOGENOUS CELLS enteroblastic, monophialidic, integrated, determinate, terminal, cylindrical, smooth, pale brown. MICROAWNS mixed and immersed in the white to yellow conidial mass, smooth or verrucose at one end. ConipIA lunate, septate or aseptate, smooth, asetulate, hyaline.
Parathozetella microsperma ER. Barbosa, J.S. Monteiro, Fiuza, R.F. Castafieda & Gusmao, sp. nov. Fig. 1 MB 834626 Differs from Thozetella species by its small conidia that lack setulae.
Type: Brazil, Mato Grosso State, Claudia, on decaying wood of lianes, 9.V.2016, coll. ER. Barbosa (Holotype, CNMTf 81).
ErymMo_oey: Latin, microsperma, refers to the small size of the conidia
MyceELIumM superficial and immersed, hyphae, 2.5 um diam, slightly branched, septate, smooth, pale brown. ConipIOMATA sporodochial, sessile, superficial, scattered, conidial mass white to yellow, 150-320 x 120-200 um. CONIDIOPHORES macronematous, septate, cylindrical, smooth, pale brown to brown. CONIDIOGENOUS CELLS enteroblastic, monophialidic, integrated, determinate, terminal, cylindrical, smooth, subhyaline, 8.5-13 x 2-3 um, with a conspicuous collarette. MICROAWNS aseptate, uncinate, verrucose at one end, hyaline, mixed and immersed in the white to yellow conidial mass, 10-12 x
354 ... Barbosa & al.
Fic. 1. Parathozetella microsperma (holotype, CNMTf 81). A. Conidium; B. Conidia; C. Microawn; D. Conidiogenous cells and microawn; E. Conidiogenous cells; F. Conidiomata. Scale bars: A, C = 5 um; B, D-E = 10 um; F = 20 um.
Parathozetella microsperma gen. & sp. nov. (Brazil) ... 355
1.2-1.5 um. Conip1a lunate, 0-1 septate, smooth, asetulate, hyaline, 4-5 x 1-1.5 um. Sexual morph not observed.
ADDITIONAL SPECIMENS EXAMINED-BRAZIL. PARA STATE: Belém, Parque Estadual
do Utinga, trilha do Patua, on decaying wood of unidentified plant: 29.IV.2019, coll.
J.S. Monteiro (MG 237232). Santa Barbara do Para, Assentamento Rio Vermelho, on
decaying petioles of Bactris gasipaes Kunth (Arecaceae), 16.V.2019, coll. A.P. Silva (MG
237239). CoMMENTS—The production of sporodochia with monophialidic conidiogenous cells invites comparison of Parathozetella with some genera like Mahabalella B. Sutton & S.D. Patil, Menidochium R.F. Castafeda & W.B. Kendr., and Minimidochium B. Sutton. However, the presence of microawns distinguishes Parathozetella from those genera, placing it morphologically closer to Thozetella. In addition to forming conidioma (synnema and sporodochia) and microawns, however, Thozetella is further characterized by conidia with setulae, structures that are absent in Parathozetella.
We consider that production of microawns and asetulate conidia are sufficient to propose a new genus, possibly within Chaetosphaeriaceae, a family characterized by presence of microawns. Réblova (2000) and Reéblova & Winka (2000) maintained that the presence or absence of conidial setulae was morphologically important in separating Dictyochaeta and Codinaea. Moreover, Seifert & al. (2011) and Li & al. (2012) also accepted using conidial setulae as a factor in delineating genera. Given this result we suggest establishing a new genus and species Parathozetella microsperma for our fungus from the Brazilian Amazon.
Acknowledgments
The authors express their sincere gratitude to Dr. De-Wei Li (The Connecticut Agricultural Experiment Station, Windsor CT U.S.A.) and Dr. Huzefa A. Raja (University of North Carolina at Greensboro U.S.A.) for their critical review of the manuscript. ER. Barbosa thanks to “Programa de Pesquisa em Biodiversidade da Amazénia Matogrossense” (Proc. 558225/2009-8, 569382/2008-4) for financial support and to “Programa de Pés-Graduacao em Ciéncias Ambientais” (PPGCAM/UFMT). Patricia Fiuza thanks Coordenagao de Aperfeigoamento de Pessoal de Nivel Superior - Programa Nacional de Pés-doutorado (CAPES-PNPD) for scholarship (Proc. 88882.306016/2018-01). Dr. Lorelei Norvell’s editorial, and Dr. Shaun Pennycook’s nomenclature reviews are greatly appreciated.
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Fiuza PO, Costa LA, Medeiros AO, Gulis V, Gusmao LFP. 2019. Diversity of freshwater hyphomycetes associated with leaf litter of Calophyllum brasiliense in streams of the semiarid region of Brazil. Mycological Progress 18: 907-920. https://doi.org/10.1007/s11557-019-01501-6.
Li DW, Kendrick B, Chen J. 2012. Two new hyphomycetes: Codinaea sinensis sp. nov. and Parapleurotheciopsis quercicola sp. nov., and two new records from Quercus phillyraeoides leaf litter. Mycological Progress 11: 899-905. https://doi.org/10.1007/s11557-011-0805-7.
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Matsushima T. 1993. Matsushima mycological memoirs 7. Published by the author, Kobe.
Monteiro JS, Hernandez-Gutiérrez A, Sotao HMP, Grandi RAP. 2013. Fungos conidiais decompositores ocorrentes em palmeiras e liquens associados na Floresta Nacional de Caxiuana. 341-366, in: PLB. Lisboa (ed.). Caxiuana: Paraiso ainda preservado. Editora do Museu Paraense Emilio Goeldi, Belém.
Monteiro JS, Sarmento PSM, Sotao HMP. 2019. Saprobic conidial fungi associated with palm leaf litter in eastern Amazon, Brazil. Anais da Academia Brasileira de Ciéncias 91(3): e20180545. https://doi.org/10.1590/0001-3675201920180545
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Santos RF dos, Sotao HMP, Monteiro JS, Gusmao LFP, Gutiérrez AH. 2018. Conidial fungi associated with leaf litter of red cedar (Cedrela odorata) in Belém, Para (eastern Brazilian Amazon). Acta Amazonica 48(3): 230-238. http://dx.doi.org/10.1590/1809-4392201704411.
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MYCOTAXON
ISSN (print) 0093-4666 (online) 2154-8889 Mycotaxon, Ltd. ©2021
April-June 2021— Volume 136, pp. 361-372 https://doi.org/10.5248/136.361
Pseudosperma albobrunneum sp. nov. from coniferous forests of Pakistan
SANA JABEEN?®”, ZAINAB’, HIRA BASHIR?®, ABDUL NASIR KHALID?
' Department of Botany, Division of Science & Technology, University of Education, Township, Lahore, Punjab, Pakistan ? Institute of Botany, University of the Punjab, Quaid-e-Azam Campus-54590, Lahore, Punjab, Pakistan ° Department of Botany, University of Okara, Okara 56300, Punjab, Pakistan
* CORRESPONDENCE TO: sanajabeenue@gmail.com; sanajabeen@ue.edu.pk
ABSTRACT—A new species, Pseudosperma albobrunneum, is described and illustrated. The specimens are from different areas of Khyber Pakhtunkhwa province, Pakistan. The identification is based on morphological characters, in combination with molecular phylogenetic analysis of sequences of the ITS region of nuclear ribosomal DNA. The species is found distinct morphologically from all closely related taxa, and molecular data confirm its novelty.
Key worps—ectomycorrhizal, Himalayan, moist temperate, taxonomy
Introduction
Inocybaceae Julich (Basidiomycota, Agaricales) is a highly diversified family of ectomycorrhizal fungi, comprising seven genera and more than 1000 species (Kobayashi 2009; Matheny & al. 2009, 2012, 2019; Kobayashi & Onishi 2010; Kropp & al. 2010; Bougher & Matheny 2011; Bougher & al. 2012; Kokkonen & Vauras 2012; Fan & Bau 2013, 2014; Braaten & al. 2014; Esteve- Raventos & al. 2015; Jabeen & al. 2016; Faroogi & al. 2017; Naseer & al. 2017; Liu & al. 2018; Ullah & al. 2018; Matheny & Kudzma 2019). The family shows more diversification in temperate regions as comparatively fewer species have been reported from tropical rain forests (Matheny & al. 2003; Matheny &
362 ...Jabeen & al.
Bougher 2017). The species have demonstrated ectomycorrhizal associations with as many as 23 families of vascular plants, including low woody shrubs in arctic-alpine habitats making these fungi of high interest (Cripps & al. 2010, Matheny & al. 2019).
Among the 28 species representing different genera in Inocybaceae reported from Pakistan (Ahmad & al. 1997; Ilyas & al. 2013; Saba & al. 2015, 2020; Jabeen & al. 2016; Farooqi & al. 2017; Naseer & al. 2017, 2019; Liu & al. 2018; Ullah & al. 2018; Jabeen & Khalid 2020), eight represent Pseudosperma (Ahmad & al. 1997; Saba & al. 2015, 2020; Liu & al. 2018; Ullah & al. 2018; Jabeen & Khalid 2020).
The many classification systems proposed for the species in Inocybaceae include several clades, sections, subgenera, and genera based on morphological features and molecular phylogenetics (Massee 1904, Heim 1931, Kithner & Romagnesi 1953, Kuyper 1986, Singer 1986, Horak 2005, Matheny & Bougher 2006, Matheny & al. 2009, Larsson & al. 2009, Alvarado & al. 2010, Ryberg & al. 2010, Matheny & Kudzma 2019).
One multigene phylogenetic analysis by Matheny & al. (2019) recognized seven genera within Inocybaceae, including two new genera [Nothocybe Matheny & K.P.D. Latha, Pseudosperma Matheny & Esteve-Rav.], two subgenera elevated to generic rank [Inosperma (Kiihner) Matheny & Esteve- Rav., Mallocybe (Kuyper) Matheny & al.], and three previously described genera [Auritella Matheny & Bougher, Tubariomyces Esteve-Rav. & Matheny, Inocybe (Fr.) Fr. sensu stricto].
Pseudosperma comprises species previously placed in Inocybe sect. Rimosae (Fr.) Quél. and characterized by cheilocystidia, absence of pleurocystidia, hyaline basidia, adnexed to sinuate lamellae, a fibrillose (rarely squamulose) and rimose pileus surface, a cylindrical stipe with a distinctly pruinose, furfuraceous, or somewhat flocculose apex, stipe context not changing color when bruised, odor often spermatic (reminiscent of green corn or honey) but occasionally nil, and smooth elliptic to (occasionally) indistinctly phaseoliform basidiospores (Matheny & al. 2019). Pseudosperma is represented by 70 species in Africa, Asia, Australasia, Europe, North America, and northern South America.
During field surveys for ectomycorrhizal fungi associated with Pinaceae in different areas of Khyber Pakhtunkhwa province, Pakistan, several collections were identified through both morphological and nrDNA ITS sequence analyses. They showed characters similar to species now classified under Pseudosperma. We could not find a published description that fit these
Pseudosperma albobrunneum sp. nov. (Pakistan) ... 363
specimens nor published similar ITS sequences and propose these here as a new species
Material & methods
Samples of basidiomata were collected in four different localities in two administrative divisions of Khyber Pakhtunkhwa province, Pakistan.
Khanian is a small village in the northern Kaghan valley in the Mansehra district, Hazara division, in north-east Khyber Pakhtunkhwa province, immediately south of the main Himalayan range with a typically moist temperate climate and dominated by Cedrus deodara (Roxb. ex D. Don) G. Don along with Abies pindrow (Royle ex D. Don) Royle and Pinus wallichiana A.B. Jacks. (Siddiqui & al. 2013).
The Lower Dir district is located in the Hindu Kush range, Malakand division, in northwestern Khyber Pakhtunkhwa province. The area lies in the valley of the Panjkora river, which originates from the Hindu Kush ranges and joins the Swat River near Chakdara. The climate is dry temperate. Pinus spp. and Quercus oblongata D. Don [= Q. incana Roxb., nom. illeg.] are the dominant tree species (Champion & al. 1965). Among Pinus, P. gerardiana Wall. ex D. Don was the dominant species. Pure Q. oblongata forest was found in the mountain heights (H. Bashir, pers. obs.). Kalam and Mashkun, also situated in the Malakand division, are home to the offshoots of the Hindu Kush range (Hamayun & al. 2003), also dominated by C. deodara forests with Pinus spp. and Q. oblongata (Champion & al. 1965). These areas have a typical dry temperate climate (Stucki & Khan 1999).
Basidiomata were collected and photographed in their natural habitat. Morphological data was recorded from the fresh specimens. Color codes follow Munsell color charts (Munsell 1975). Each collection was dried using a fan heater and preserved in sealed bags. Sections from basidiomata were rehydrated in 5% KOH, stained in Congo red, and observed under a Techno MX4300H compound microscope. Microscopical characters were measured using an ocular micrometer, and drawn with the aid of a camera lucida. The abbreviation (n/m/p) represents ‘Y number of basidiospores measured, ‘m’ number of basidiomata, and ‘p’ number of collections. Basidiospore dimensions were recorded as (a) b-c (d), where (a) and (d) are the extreme values, and the range b-c contains at least 90% of the calculated values; Q indicates the l/w ratio of the spores, and avQ is the average Q of all measured spores. Measurements of hyphae are given as ranges. The collections examined during this study have been deposited in the herbarium, Department of Botany, University of the Punjab, Quaid-e-Azam Campus, Lahore, Pakistan (LAH).
Genomic DNA extraction and PCR amplification of ITS1, 5.88, and ITS2 was carried out following procedures by White & al. (1990), Gardes & Bruns (1993), and Bruns (1995). The PCR products were purified and sequenced at Macrogen Inc. (Korea). The newly generated sequences were deposited in GenBank. For phylogenetic study, consensus sequences of ITS regions were generated in the BioEdit software version 7.2.5 (Hall 1999). Sequence homology search was investigated using the BLAST algorithm at http://www.ncbi.nlm.nih.gov/. Sequences from the closest
364 ...Jabeen & al.
relatives of the Pakistani species were included in the final dataset to reconstruct a phylogeny based on published phylogenies (Larsson & al. 2009, Kropp & al. 2013, Latha & Manimohan 2017, Liu & al. 2018). Sequences from Auritella and Inosperma were chosen as outgroup (Matheny & al. 2009). GenBank accession numbers are included with each taxon name in the phylogenetic tree. Multiple sequences were aligned using the webPRANK tool at https://www.ebi.ac.uk/goldman-srv/webprank/. Maximum likelihood analysis was performed in MEGA version 6 (Tamura & al. 2013) at 1000 bootstrap pseudoreplicates by finding best-fit substitution model with 1000 bootstrap replicates. The phylogeny was inferred by the Maximum Likelihood method based on the General Time Reversible model. A discrete Gamma distribution was used to model evolutionary rate differences among sites (5 categories (+G, parameter = 0.7529)).
Taxonomy
Pseudosperma albobrunneum Jabeen, Zainab, H. Bashir & Khalid, sp. nov. Figs. 1, 2
MB 840056
Differs from Pseudosperma dulcamaroides and P. sororium by the smaller basidiomata, white pileus becoming brownish with age, fibrillose stipe, and smooth, elongate to cylindric, sub-reniform basidiospores.
Type: Pakistan, Khyber Pakhtunkhwa, Hazara division, Mansehra district, Khanian, 2500 m a.s.l., on soil under Cedrus deodara, 5 August 2014, Sana Jabeen SJ102 (Holotype LAH35047; GenBank MG495392).
Erymo.oey: The specific epithet refers to the white to brown basidiomata.
PirEus 1-1.8 cm in diam., conical with a prominent umbo; surface dry, rimose, fibrillose, white (10Y8/4) to brownish (7.5YR6/10); umbo yellowish (5Y8/6) becoming brownish (7.5YR6/10) at maturity; margin incurved when young. LAMELLAE adnexed, moderately close, up to 2 mm deep, golden brown (10YR5/6), with fimbriate edge. STIPE 5.5 x 0.4 cm, central, cylindrical, narrower towards the apex and wider towards the base; surface dry, pruinose towards apex, fibrillose; white (10Y8/4) when young, becoming grayish brown (5R4/1) to brown (7.5YR6/10) upon maturity, context off-white (5Y9/2). ODOR spermatic.
BASIDIOSPORES [100/5/5] (12.7-)13.2-14.4(-16.4) x (5.3-)6.1-6.9 (—8.2) um, avl x avw = 13.8 x 6.5 um, Q = (1.90-)1.94-2.20(-2.50), avQ = 2.00, elongate to cylindric, constricted in the center in side view, sub-reniform, smooth, guttulate, brown in 5% KOH. Basrpia (38.1-)40.3-42.2(-43.7) x (9.2—)9.5-11.8(-12.1) um, 2-4-spored, clavate, guttulate, hyaline in 5% KOH; clamp connections observed at the base. CHEILOCYSTIDIA (20.2-)25.4-27.4 (-30.3) x 4.4-6.5 um, avl x avw = 26.4 x 5.5 um, clavate, connected with basal
Pseudosperma albobrunneum sp. nov. (Pakistan) ... 365
a ee
ta ~ : Ficure. 1. Pseudosperma albobrunneum. A. LAH35288; B. LAH35047 (holotype). Scale bars = 0.5 cm. Photos by Abdul Nasir Khalid and Sana Jabeen.
366 ...Jabeen & al.
~~)
E —_
FiGure. 2. Pseudosperma albobrunneum (holotype, LAH35047). A. Basidiospores; B. Basidia; C. Caulocystidia; D. Cheilocystidia, E. Pileipellis; F Stipitipellis. Scale bars = 10 um. Drawings by Sana Jabeen.
Pseudosperma albobrunneum sp. nov. (Pakistan) ... 367
cell, hyaline in 5% KOH; clamp connections at base common. PLEUROCYSTIDIA absent. CAULOCYSTIDIA at the extreme apex of the stipe, (43.1-)45.2-50.3(- 56.11) x (7.6-)9.4-10.9(-11.2) um, avl x avw = 47.7 x 10.1 um, clavate, hyaline in 5% KOH; clamp connections observed at the base. PILEIPELLIS hyphae 4.6- 7.7 um wide, avw = 6.1 um, septate, filamentous, branched, hyaline in 5% KOH; clamp connections frequent. STIPITIPELLIS hyphae (6.1—)8.3-11.04(-11.69) um wide, avw = 9.7 um, septate, filamentous, rarely branched; terminal cells clavate; clamp connections observed.
ADDITIONAL SPECIMENS EXAMINED: PAKISTAN. KHYBER PAKHTUNKHWA, Malakand division, Lower Dir district, near Darosh, 1840 m a.s.l., on soil under Pinus wallichiana, 4 September 2015, Hira Bashir & Abdul Nasir Khalid D15 (LAH35288; GenBank MG495393); Swat district, Kalam, 2400 m a.s.l., on soil under C. deodara, 4 September 2013, Sana Jabeen SJ146 (LAH35045; GenBank MG495395); Swat district, Mashkun, 2500 m a.s.l., on soil under C. deodara, 5 September 2013, Aamna Ishaq SJ147 (LAH35046; GenBank MG495396); SJ110 (LAH35289; GenBank MG495394). HABITAT & DISTRIBUTION—Himalayan moist Pinaceae-dominated forests (including Pinus roxburghii Sarg., P. wallichiana, and few Cedrus deodara) and dry oak-dominated temperate forests (including Quercus oblongata). Currently known only from Pakistan's Khyber Pakhtunkhwa province. EcoLocy & DISTRIBUTION—1840-2500 m asl in dry and moist temperate coniferous forests, Pakistan.
Molecular phylogenetic analysis
A BLAST search of NCBI comparing the ITS consensus sequence of 658 base pairs from the type specimen of Pseudosperma albobrunneum (LAH35045) was closely similar to HQ604626 & KP783443 sequences named as I. sororia (P. sororium (Kauffman) Matheny & Esteve-Rav. in Index Fungorum) from USA and Russia. The ITS dataset involved 100 nucleotide sequences including these two and others closely related from the BLAST along with sequences generated during this study and those from published literature as well as those chosen as outgroup. Of the total 1642 positions in the final dataset, 771 were conserved, 465 were variable, 342 were parsimony informative, and 114 were present as singletons.
In the phylogenetic tree (Fic. 3), two major clades were recovered within Pseudosperma labeled as clade A and clade B. The P albobrunneum sequences generated during this study formed their own lineage in clade A clustered with P. sororium (HQ604626 & KP783443) but separated from them with 94% boot strap support. The second set of
368 ...Jabeen & al.
69
KJ700456 Pseudosperma mimicum 67 | KJ546158 Pseudosperma mimicum KJ726737 Pseudosperma mimicum 87 KF056319 Pseudosperma mimicum soe FJ904124 Pseudosperma mimicum 97 —— FJ904134 Pseudosperma arenicola —— FJ904133 Pseudosperma arenicola 99 HQ604626 Pseudosperma sororium 97 KP783443 Pseudosperma sororium g9 | @ MG495393 Pseudosperma albobrunneum aa @ MG495395 Pseudosperma albobrunneum @ MG495396 Pseudosperma albobrunneum 71| @ MG495394 Pseudosperma albobrunneum @ MG495392 Pseudosperma albobrunneum ih JX630909 Pseudosperma dulcamaroides
FJ904127 Pseudosperma dulcamaroides FJ904126 Pseudosperma dulcamaroides MW010042 Pseudosperma dulcamaroides 75) IQ408754 Pseudosperma breviterincarnatum 99 | JQ408751 Pseudosperma breviterincarnatum JQ408753 Pseudosperma breviterincarnatum JQ408750 Pseudosperma breviterincarnatum 85 | JF908162 Pseudosperma squamatum 99 || AM882780 Pseudosperma squamatum FJ904136 Pseudosperma squamatum 93 FJ904132 Pseudosperma squamatum on JF908260 Pseudosperma spurium FJ904139 Pseudosperma spurium JQ408794 Pseudosperma spurium “| gg) JX436912 Pseudosperma flavellum
JQ724025 Pseudosperma flavellum JQ724026 Pseudosperma flavellum JQ724027 Pseudosperma flavellum NR_153126 Pseudosperma illudens 99; NR_153171 Pseudosperma luteobrunneum KX073581 Pseudosperma luteobrunneum 97 NR_153172 Pseudosperma brunneosquamulosum 4 > NR_153173 Inocybe rubrobrunnea 99 NR_152346 Pseudosperma araneosum KJ729878 Pseudosperma araneosum
99 | MF588965 Pseudosperma pakistanense '— MF575849 Pseudosperma pakistanense 99 97 | AM882769 Pseudosperma obsoletum
AM882770 Pseudosperma obsoletum | 97 NR_119898 Pseudosperma aurora
55 NR_160609 Pseudosperma yunnanensis 83 NR_164070 Pseudosperma notodryinum
r AM882772 Pseudosperma perlatum AM882771 Pseudosperma perlatum NR_121520 Pseudosperma lepidotellum > NR_153169 Pseudosperma griseorubidum 89 99 KY440094 Pseudosperma keralense
NR_160442 Pseudosperma keralense 95 95 — 224 KP171123 Pseudosperma gracilissimum eT oe JQ408755 Pseudosperma gracilissimum KP171122 Pseudosperma gracilissimum gg > NR_171961 Pseudosperma salentinum g9 | NR_165883 Pseudosperma friabile 7 MH216090 Pseudosperma friabile MH216093 Pseudosperma friabile
MH216091 Pseudosperma friabile | 99 |MG742423 Pseudosperma triaciculare
MG742429 Pseudosperma triaciculare
99 | MG742419 Pseudosperma flavorimosum as P. brunneoumbonatum MG742421 Pseudosperma flavorimosum as P. brunneoumbonatum MG495391 Pseudosperma flavorimosum KP636864 Inocybe sp. 99 | MHS78031 Inocybe sp. MH212073 Inocybe sp. NR_171959 Pseudosperma melleum of 74 F 4904165 Pseudosperma umbrinellum FJ904163 Pseudosperma umbrinellum NR_160608 Pseudosperma neoumbrinellum 65 — FJ904158 Pseudosperma bulbosissinum 83 [| FJ904159 Pseudosperma bulbosissimum
65|, FJ904160 Pseudosperma bulbosissimum 81| 87 L
57
AM882765 Pseudosperma bulbosissinum AM882777 Pseudosperma rimosum F908172 Pseudosperma rimosum
71) 'd
MH745138 Pseudosperma himalayense
Lis MH745140 Pseudosperma himalayense H
796995 Pseudosperma himalayense
9 | MG742414 Pseudosperma pinophilum MG742417 Pseudosperma pinophilum ———— NR_171960 Pseudosperma ponderosum 57| 57 it AM882844 Pseudosperma rimosum AM882761 Pseudosperma rimosum t— AM882762 Pseudosperma rimosum 87, FJ904148 Pseudosperma melliolens FJ904149 Pseudosperma melliolens FJ904147 Pseudosperma rimosum
“ HQ604618 Pseudosperma sororium
9 |- HQ604610 Pseudosperma sororium HQ604617 Pseudosperma sororium HQ604607 Pseudosperma sororium JQ408762 Inosperma lanatodiscum
KY616964 Inosperma shawarense
Figure. 3. Molecular phylogenetic analysis of Pseudosperma albobrunneum
Clade B o7 In MH734760 Pseudosperma himalayense
Clade A
Pseudosperma
Inosperma MH578017 Inosperma maculatum
GU062740 Auritella foveata
| Auritella
based on ITS
sequences. Sequences generated during this study are marked with bullets; a red bullet indicates
the holotype sequence.
Pseudosperma albobrunneum sp. nov. (Pakistan) ... 369
P. sororium sequences (HQ604607, HQ604610, HQ604617, HQ604618) found in clade B does not show remarkable genetic similarity with our P. albobrunneum sequences.
Discussion
Pseudosperma albobrunneum is characterized by its whitish to brownish basidiomata, a very prominent long-lasting umbo, a comparatively long and slender stipe, and smooth and elongate to cylindric, sub-reniform basidiospores.
The new Pakistani species resembles the European P. dulcamaroides (Kithner) Matheny & Esteve-Rav., which also has brown basidiomata but with a short stipe compared with its cap diameter and with a non-umbonate pileus that becomes convex to flat at maturity (Larsson & al. 2009).
Pseudosperma sororium (Kauffman) Matheny & Esteve-Rav. showed morphological characters more or less similar to P. albobrunneum as described by Kauffman (1924), but its yellow pileus and basidiospores that are ellipsoid or elongate-ellipsoid and not truly sub-reniform, sub-inequilateral, obtuse at both ends distinguish P sororium from P. albobrunneum. Furthermore, P. sororium has a very strong green corn odor.
In the absence of type studies, modern descriptions of P dulcamaroides (Larsson & al. 2009) and P sororium (as Inocybe, Stuntz 1978) also support P. albobrunneum as morphologically distinct.
Pseudosperma breviterincarnatum (D.E. Stuntz ex Kropp & al.) Matheny & Esteve-Rav. from conifer and quaking aspen forests of the western USA differs by its pinkish lamellae and brownish pileus as well as a pinkish to brownish stipe (Kropp & al. 2013).
Pseudosperma flavorimosum Jabeen & Khalid from Pakistan morphologically resembles P. albobrunneum but can be distinguished by its basidiospores that are elliptical, amygdaliform with broad apex and narrow base (Jabeen & Khalid 2020). In the phylogenic tree (Fic. 3), P. albobrunneum forms a separate clade, supporting its novelty.
Acknowledgements
This work was financially supported by Higher Education Commission (HEC)- Pakistan under Indigenous PhD Fellowship (Phase II). Sincere thanks to Dr. Chang-Lin Zhao (Southwest Forestry University, Kunming, Yunnan, P.R. China), Dr. Tine Grebenc (Department of Forest Physiology and Genetics, Slovenian Forestry Institute, Ljubljana, Slovenia), and Dr. Else C. Vellinga (University of California, Berkeley, USA) for presubmission reviews of the manuscript.
370 ...Jabeen & al.
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MY COTAXON
ISSN (print) 0093-4666 (online) 2154-8889 Mycotaxon, Ltd. ©2021
April-June 2021— Volume 136, pp. 373-385 https://doi.org/10.5248/136.373
Entyloma eranthidis sp. nov. on Eranthis longistipitata from Uzbekistan
TEODOR T. DENCHEV' , CVETOMIR M. DENCHEV’, MARTIN KEMLER’, DOMINIK BEGEROW?”
' Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin St., 1113 Sofia, Bulgaria
? AG Geobotanik, Ruhr-Universitat Bochum, ND 03, Universitatsstrafse 150, 44801 Bochum, Germany
* CORRESPONDENCE TO: ttdenchev@gmail.com
ABSTRACT—A new smut fungus, Entyloma eranthidis on Eranthis longistipitata from Uzbekistan, revealed by molecular, morphological, and ecological evidence, is described and illustrated. It differs from all other species of Entyloma by host specialization on Eranthis and by having longer (<35(-38) um) spores and thicker (<10(-12) um) spore walls. ITS rDNA sequence analysis indicates that the new species does not cluster with other species of Entyloma on Ranunculaceae.
Key worps—Entylomataceae, phylogeny, taxonomy
Introduction
Eranthis Salisb. (Ranunculaceae) is a small genus with a geographic range extending from southern Europe and Turkey to central and east Asia. It contains eleven species (Ruksans & Zetterlund 2018, Park & al. 2019). Four are with yellow perianth-segments: E. hyemalis (L.) Salisb. (native to South Europe), E. cilicica Schott & Kotschy (in the Taurus Mts and Iranian and Iraq Kurdistan; considered by some authors conspecific with previously named species; Davis & al. 1965, Tutin 1993), E. iranica Ruksans & Zetterl. (from Iran), and E. longistipitata Regel (from central Asia) (Frizen 1993, Ruksans & Zetterlund 2018, Park & al. 2019). The remaining species produce white
374 ... Denchev & al.
perianth-segments and have a limited distribution in the Altai-Sayan mountain region in western China or eastern Asia (Li & Tamura 2001, Park & al. 2019).
Only one smut fungus, Urocystis eranthidis (Pass.) Ainsw. & Sampson, is known to infect plants in Eranthis. This fungus is reported from Europe, Asia, North America, and Australia, with all records occurring on yellow-flowered plants: E. hyemalis, E. cilicica, and E. longistipitata (Ciferri 1938; Ainsworth & Sampson 1950; Fischer 1953; Schwarzman 1960; Vanky 1985, 2011; Scholz & Scholz 1988, 2001, 2013; Denchev 1991, 2001; Azbukina & Karatygin 1995; Scholler 1996; Vanky & Shivas 2008; Beenken & Senn-Irlet 2016; Woods & al. 2018). During an examination of fungal loans from the herbarium of University of Turku, Finland (TUR), an unidentified smut fungus on Eranthis longistipitata from Uzbekistan was found. Morphological and molecular studies demonstrated that it represented a new species of Entyloma de Bary. Its host belongs to the group of yellow-flowered species of Eranthis.
Entyloma is a large genus in the Entylomataceae, with 188 recognized species on host plants belonging to 27 families (Vanky 2011; Denchev & al. 2013; Savchenko & al. 2014, 2016; Rossman & al. 2016; Rooney-Latham & al. 2017; Savchenko & Carris 2017; Kruse & al. 2018; Kruse & Thines 2019; Richter & al. 2019). Entyloma species form sori in vegetative organs of plants from many different lineages of eudicots, mostly in leaves, rarely in stems, occasionally in roots, usually forming few to numerous spots, sometimes swellings or galls formed by hypertrophic growth of host tissue. The spores are permanently embedded in the host tissue, singly or in irregular groups, hyaline, yellow or yellowish brown, and usually with a smooth, two-layered wall; very rarely the outer layer is tuberculate (e.g., E. verruculosum) or torn apart into prismatic, pyramidal or coarse and irregular pieces (e.g., E. urocystoides) (Denchev & al. 2013). For many Entyloma species, an asexual morph is also recorded (Vanky 2011).
The importance of host specificity in delimiting species within Entyloma has varied significantly during the last eight decades. Savile (1947) applied a morphological species concept, based on spore sizes and asexual morph. He synonymized species with similar morphology, parasitizing host species on different genera from the same family. As a result of this broad species concept, Savile accepted only eight species of Entyloma on North American asteraceous hosts. Other authors (e.g. Liro 1938, Lindeberg 1959, Vanky 2011) applied narrower species concepts, considering Entyloma species as infecting one or more hosts from the same host genus or occasionally a few
Entyloma eranthidis sp. nov. on Eranthis (Uzbekistan) ...
TABLE 1. Entyloma species and GenBank accession numbers used for
phylogenetic analysis SPECIES Host E. arnicale Arnica montana . arnoseridis Arnoseris minima . atlanticum Geranium tuberosum . australe Physalis cordata . belangeri — . bidentis Bidens pilosa . browalliae Browallia americana bullosum Ranunculus paludosus
calceolariae carmeli chrysosplenii comaclinii corydalis cosmi costaricense dahliae deliliae davenportii diastateae doebbeleri eburneum elstari eranthidis eryngii
eryngii-cretici
E. eryngii-plani
E. ficariae
E. fuscum
E. gaillardianum E. guaraniticum E. helianthi
E. hieracii
E. holwayi
E. jolantae
E. klenkei
E. kochmanii
Calceolaria chelidonioides
Eryngium falcatum
Chrysosplenium alternifolium
Comaclinium montanum
Corydalis bulbosa Cosmos bipinnatus Viguiera sp.
Dahlia sp.
Delilia biflora Diastatea micrantha Dahlia imperialis Ranunculus repens Eranthis longistipitata Eryngium campestre E. creticum
E. planum
Ficaria verna Glaucium flavum Gaillardia aristata Bidens pilosa Helianthus annuus Hieracium sylvaticum Cosmos caudatus Ranunculus oreophilus R. marginatus
R. lanuginosus
GENBANK #
(ITS)
AY854964
AY081017 AY081018 AY081019 AY259074 AY081020 AY081021 MF924658 AY081022 KF310892 AY081024 AY081025 AY081027 KJ728759 AY081028 AY081029 AY081030 AY259064 AY081031 AY081032 MF924689 AY259048 MT118137 AY081033 KF310894 AY081034 MF924702 AY081036 AY081037 AY081038 KU163607 AY081039 AY081040 MF924688 MF924663 MF924678
REFERENCE
Boekhout & al. 2006
Begerow & al. 2002 Begerow & al. 2002 Begerow & al. 2002 Richter & al. 2019 Begerow & al. 2002 Begerow & al. 2002 Kruse & al. 2018 Begerow & al. 2002 Savchenko & al. 2014 Begerow & al. 2002 Begerow & al. 2002 Begerow & al. 2002 Lutz & Piatek 2016 Begerow & al. 2002 Begerow & al. 2002 Begerow & al. 2002 Richter & al. 2019 Begerow & al. 2002 Begerow & al. 2002 Kruse & al. 2018 Richter & al. 2019 this study Begerow & al. 2002 Savchenko & al. 2014 Begerow & al. 2002 Kruse & al. 2018 Begerow & al. 2002 Begerow & al. 2002 Begerow & al. 2002
ofp
Rooney-Latham & al. 2017
Begerow & al. 2002 Begerow & al. 2002 Kruse & al. 2018 Kruse & al. 2018 Kruse & al. 2018
376 ... Denchev & al.
SPECIES Host prt if REFERENCE
E. lagoeciae Lagoecia cuminoides MH295129 Kruse & Thines 2019
E. linariae Linaria vulgaris AY081041 Begerow & al. 2002
E. lobeliae Lobelia laxiflora AY081042 Begerow & al. 2002
E. madiae Madia gracilis AY081043 Begerow & al. 2002
E. magocsyanum Tordylium cordatum KF310891 Savchenko & al. 2016
E. majewskii Ficaria verna MF924713 Kruse & al. 2018
E. matricariae Tripleurospermum perforatum AY081044 Begerow & al. 2002
E. microsporum Ranunculus repens MF924708 Kruse & al. 2018
E. parthenii Parthenium hysterophorus AY081026 Begerow & al. 2002
E. piepenbringiae Ranunculus polyanthemos MF924664 Kruse & al. 2018 subsp. nemorosus
E. polysporum Ambrosia artemisiifolia AY081046 Begerow & al. 2002
E. randwijkense — AY259080 Richter & al. 2019
E. ranunculacearum Ranunculus acris MF924635 Kruse & al. 2018
E. ranunculi-repentis R. repens AY081047 Begerow & al. 2002
E. ranunculi-scelerati R. sceleratus MF924672 Kruse & al. 2018
E. ranunculorum R. auricomus MF924638 Kruse & al. 2018
E. savchenkoi R. paludosus MF924675 Kruse & al. 2018
E. scandicis Scandix verna KF447773 Savchenko & al. 2016
E. serotinum Symphytum officinale AY081048 Begerow & al. 2002
E. thielii Ranunculus montanus MF924692 Kruse & al. 2018
E. verruculosum R. lanuginosus MF924651 Kruse & al. 2018
E. zinniae Zinnia peruviana AY081049 Begerow & al. 2002
closely related host genera. During the last two decades with the application of molecular methods, it became evident that members of Entyloma exhibit a far higher host specificity, parasitizing a single or only a few closely related host species (Begerow & al. 2002, Vanky & Lutz 2010, Savchenko & al. 2014, 2016, Kruse & al. 2018, Kruse & Thines 2019). It also became evident that much higher diversity than currently recognized in Entyloma should be expected (Kruse & al. 2018).
From Uzbekistan, 16 different Entyloma species are known, among which three are recorded on hosts in Ranunculaceae: the E. ranunculi-repentis complex on R. polyanthemos L., E. thalictri J. Schrot. on Thalictrum minus L., and E. winteri Linh. on Delphinium biternatum Huth (Ramazanova & al. 1987, Azbukina & Karatygin 1995).
In the present article, we describe and illustrate a new species of Entyloma on Eranthis from Uzbekistan, and analyze its phylogenetic affinities in Entyloma.
Entyloma eranthidis sp. nov. on Eranthis (Uzbekistan) ... 377
55) Entyloma hieracii AY081039 Entyloma matricariae AY081044 Entyloma polysporum AY081046 Entyloma belangeri AY259074 eo Entyloma gaillardianum AY081037 Entyloma arnicale AY854964 Entyloma chrysosplenii AY081024 BE as Entyloma carmeli KF310892 Entyloma eryngii-cretici KF310894 Entyloma lagoeciae MH295129 Entyloma eryngii-plani AY081034 Entyloma eryngii AY081033 Entyloma dahliae AY081029 Entyloma parthenii AY081026 Entyloma australe AY081019 Entyloma zinniae AY081049 Entyloma doebbeleri AY081032 Entyloma diastateae AY081031 Entyloma guaraniticum AY081038 Entyloma helianthi KU163607 Entyloma cosmi KJ728759 Entyloma bidentis AY081020 Entyloma holwayi AY081040 Entyloma browalliae AY081021 Entyloma calceolariae AY081022 98) Entyloma scandicis KF447773 Entyloma magocsyanum KF310891 Entyloma costaricense AY081028 Entyloma deliliae AY081030 Entyloma arnoseridis AY081017 Entyloma comaclinii AY081025 Entyloma lobeliae AY081042 91 Entyloma elstari AY259048 87 Entyloma madiae AY081043 Entyloma davenportii AY259064 Entyloma serotinum AY081048 Entyloma corydalis AY081027 69) Entyloma bullosum MF924658 100 Entyloma verruculosum MF924651 Entyloma piepenbringiae MF924664 ms Entyloma microsporum MF924708 Entyloma randwijkense AY259080 soy Entyloma eburneum MF924689 60 Entyloma klenkei MF924663 Entyloma jolantae MF924688 Entyloma ranunculi-scelerati MF924672 Entyloma majewskii MF924713 Entyloma kochmanii MF924678 Entyloma ranunculacearum MF924635 Entyloma ranunculorum MF924638 Entyloma ficariae MF924702 72) Entyloma savchenkoi MF924675 100 Entyloma ranunculi-repentis AY081047 Entyloma thielii MF924692 Entyloma linariae AY081041 91 Entyloma atlanticum AY081018 100 Entyloma eranthidis MT118137 Entyloma fuscum AY081036
50
4p
54
100
54]
81
0.02 substitutions/site
Fic. 1. Phylogenetic relationships of Entyloma, based on the RAxML analysis of the complete rDNA internal transcribed spacer (ITS). The new species Entyloma eranthidis is depicted in boldface. Bootstrap values of 1000 repetitions =50 are shown above branches. The phylogeny was rooted according to Begerow & al. (2002).
Materials & methods
Morphological examination
A dried specimen from the herbarium of University of Turku, Finland (TUR) was examined under light microscope (LM) and scanning electron microscope (SEM). For LM observations and measurements, spores were mounted in lactoglycerol solution
378 ... Denchev & al.
(w: la: gl=1:1: 2) on glass slides, gently heated to boiling point to rehydrate the spores, and then cooled. The measurements of spores are given as min-max (extreme values) (mean + 1 standard deviation). For the description of the new species, a total of 300 spores from three sori (100 spores per sorus) were measured. For SEM, spores were attached to specimen holders by double-sided adhesive tape and coated with gold in an ion sputter. The surface structure of spores was observed and photographed at 10 kV accelerating voltage using a Zeiss Sigma VP scanning electron microscope. The description below is based entirely on the specimen examined.
DNA extraction, PCR amplification, and sequencing
Fragments of sori for the smut fungus and leaf tissue for the host plant were removed for DNA extraction. The samples were milled in the Fastprep-24™ Sample Preparation Instrument, using two steel beads. Genomic DNA was isolated using the my-Budget Plant DNA Kit™, according to the manufacturer’s protocol 1 (“Isolation of DNA from plant material using lysis buffer SLS”). The rDNA ITS region was amplified using GoTaq™ Master Mix with primer combination ITS1-F/ITS4 (White & al. 1990, Gardes & Bruns 1993) for the smut fungus and ITS1/ITS4 (White & al. 1990) for the host plant. Standard thermal cycling conditions with annealing temperature of 52 °C were used for amplification. Five pl of PCR products were purified using ExoSAP (1:5 diluted in ddH,O). Amplicons were sequenced in both directions with the BigDye™ Terminator Cycle Sequencing Kit V3.1 on an ABI 3130xl Genetic Analyser at the Faculty of Chemistry and Biochemistry, Ruhr University Bochum, Germany.
Phylogenetic analyses
A multiple sequence alignment of the newly generated Entyloma sequence and representative sequences downloaded from NCBIs GenBank (TABLE 1) was generated using the e-ins-i option in MAFFT v7.450 (Katoh & Standley 2013). Ambiguous positions were removed using GBLOCKS (Castresana 2000) implemented in SEAVIEW (Gouy & al. 2010). A phylogenetic tree was inferred in RAxML 8.2.11 using the GT[RGAMMA nucleotide model and a rapid bootstrapping algorithm with 1000 replicates (Stamatakis 2014). The resulting phylogeny was visualized using FigTree v1.4.3 (Rambaut 2012).
Results: Phylogeny and molecular host identification
The phylogenetic analysis of the ITS data produced a topology similar to previous analyses (Begerow & al. 2002), with notable exceptions (Fic. 1). As in Begerow & al. (2002), all species of Entyloma on asterids, together with E. chrysosplenii and three species known only by their asexual morph, formed a well-supported clade, whereas those on Ranunculales were inferred as paraphyletic. Clades within these large groupings sometimes were incongruent with those of Begerow & al. (2002); however we note that in general our phylogeny showed limited statistical support for many clades. Nevertheless, the Entyloma species on Eranthis longistipitata
Entyloma eranthidis sp. nov. on Eranthis (Uzbekistan) ... 379
D ,
E | Loe
Fic. 2. Entyloma eranthidis on Eranthis longistipitata (holotype, TUR 109 345): A-C. Habit; D. Spores in LM, median view; E. Spores in LM, surface view. Scale bars: A-C = 0.5 cm; D, E= 10 um.
380 ... Denchev & al.
formed a statistically well-supported clade with E. atlanticum on Geranium tuberosum and did not cluster together with other Entyloma species on Ranunculaceae. This clade was sister group to E. fuscum on Glaucium flavum.
The identity of the host plant, Eranthis longistipitata, was confirmed by ITS sequence data (now deposited in the NCBI with accession no. MT484089). The newly generated ITS sequence had a 99-100% sequence identity and 84% query coverage with the available ITS sequences of E. longistipitata in GenBank.
Morphology
The morphology of Entyloma is very simple, and differences between the species are consequently very few and vague (Lindeberg 1959). In this genus, the morphological features most commonly used for separating species are: sorus location and characteristics, spore sizes and wall characteristics, and presence of an asexual morph.
The smut fungus on Eranthis longistipitata from Uzbekistan is characterized by atypically well-defined morphological features, by which it can be easily distinguished from all species currently recognized in Entyloma. With respect to spore size, it produces by far the largest- sized spores in Entyloma. ‘The only other Entyloma that occasionally has spores exceeding 25 um, is E. bullosum (Sacc.) J. Kruse & al., with spore lengths reaching 21.5(-—26.5) um (Vanky 2011, Kruse & al. 2018). Several “Entyloma” species with large “spores” are referred to the Protomycetales (Vanky 2011). Although the smut fungus on Eranthis longistipitata from Uzbekistan has large spores, the morphological features and ITS sequence data clearly determine its position within Entyloma.
A second morphological feature distinguishing this fungus from all currently known Entyloma species is its spore wall, which is remarkably thick, (3.5-)4.5-10(-12) um, with a cracked outer layer. The only other Entyloma that has a spore wall reaching 10 um, is E. martindalei (Peck) Piatek, with the inner layer being c. 0.5 um and the outer layer (1-)2-5 (-9.5) um thick (Vanky 2011). For the Entyloma spp. parasitizing hosts in the Ranunculales, thick spore walls with cracked outer layer are not an uncommon morphological feature (e.g., the spore walls of E. urocystoides Bubak on Corydalis solida (L.) Clairv., E. bullosum on Ranunculus paludosus Poir., and E. microsporum (Unger) J. Schrét. on Ranunculus spp.; Denchev 2001, Vanky 2011, Kruse & al. 2018).
Entyloma eranthidis sp. nov. on Eranthis (Uzbekistan) ... 381
Fic. 3. Entyloma eranthidis on Eranthis longistipitata (holotype, TUR 109 345). Spores in SEM. Scale bars: A, B = 10 um; C, D = 5 um.
382 ... Denchev & al. Taxonomy
Entyloma eranthidis T. Denchev, Denchev, Kemler & Begerow, sp.nov. _—_- FIGs 2, 3 IF 557320
Differs from the other Entyloma species by specialization on Eranthis and by having larger spores and thicker spore walls.
Type—on Eranthis longistipitata: Uzbekistan, Tashkent Region, NE of Tashkent, W Tian Shan, Ugamskii Khrebet, NE of Charvak Reservoir, 1100 m, 41°43’N 70°05’E, 1 May 1992, leg. Y. Makinen 92-163 (Holotype, TUR 109 345).
EryMoLoGcy—tThe epithet refers to the host genus.
Sor! in leaves, forming irregularly rounded spots, 0.5-2.5 mm long, larger by fusion, amphigenous, not limited by veins, sometimes slightly protruding, reddish brown, peripherally greenish on adaxial side, clay buff on abaxial side of leaves. SPORES single, embedded in leaf tissue, usually irregular (because of the cracked surface), variable in size (18—)20—35(-38) x (16.5—)18-28(-31.5) (26.8 + 3.3 x 23.3 + 2.8) um (n = 300), light to medium yellowish brown; spore wall two-layered, (3.5—)4.5-10(-12) um thick, inner layer yellowish brown, unevenly thickened, (0.8—)1.0-3.5(—4.3) um thick, outer layer hyaline, highly variable in thickness, (2.5-)3.5-7.5(-9.5) um thick, initially smooth, at maturity cracking and rupturing irregularly, some ruptures reaching inner layer. As seen by SEM, outer spore wall layer very irregularly ruptured, often forming irregular ridge-like structures. ANAMORPH not seen.
CoOMMENTS— The immature spores of E. eranthidis are hyaline, with smaller sizes and a thinner, not ruptured, spore wall. Entyloma eranthidis is known only from the type locality.
Acknowledgements
The authors gratefully acknowledge Prof. Makoto Kakishima (University of Tsukuba, Tsukuba, Japan) and Dr. Shuang-Hui He (Beijing Forestry University, China) for critically reading the manuscript and serving as pre-submission reviewers, Curator of TUR (Herbarium of University of Turku) for sending specimens, and Tanja Rollnik (Ruhr-Universitat Bochum) for preparing the SEM images.
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MY COTAXON
ISSN (print) 0093-4666 (online) 2154-8889 Mycotaxon, Ltd. ©2021
April-June 2021—Volume 136, pp. 387-400 https://doi.org/10.5248/136.387
Calogaya miniata comb. nov., Huneckia crocina comb. nov., and new neotropical records of Wetmoreana brouardii
KARINA WILK
W. Szafer Institute of Botany, Polish Academy of Sciences, Lubicz 46, 31-512 Krakow, Poland
CORRESPONDENCE TO: k.wilk@botany.pl
ABSTRACT—New combinations Calogaya miniata and Huneckia crocina are proposed for species previously placed in Caloplaca s.lat., following the revised classification of Teloschistaceae. The taxonomy of Wetmoreana brouardii is discussed in relation to Caloplaca ochraceofulva, and its current world distribution is presented, including new records from Chile, Colombia, Peru, and Uruguay.
Key worps—lichenized Ascomycota, nomenclature, South America, Teloschistaceae
Introduction
Since the publication of the new systematic arrangement of Teloschistaceae (Arup & al. 2013), many new genera have been proposed (e.g., Kondratyuk & al. 2014a, 2017; Sochting & al. 2014a, b; Wilk & al. 2021), with the family now comprising more than 100 genera (Kondratyuk & al. 2018). The genera are distributed among the subfamilies Caloplacoideae, Teloschistoideae, and Xanthorioideae (Gaya & al. 2012; Arup & al. 2013).
During an ongoing taxonomic and molecular survey on Teloschistaceae in Bolivia and Peru, many new discoveries were made, some already published in Wilk & Flakus (2017), Wilk (2020), and Wilk & al. (2021). In this work, two new nomenclatural combinations for species previously placed in Caloplaca s.lat. are proposed in Calogaya Arup &al., and Huneckia S.Y. Kondr. & al. Calogaya is well-delimited molecularly (Gaya & al. 2011 as “Caloplaca saxicola group”; Arup & al. 2013; Vondrak & al. 2016, 2018).
388 ... Wilk
Huneckia is a genus recently proposed to accommodate two species, H. pollinii (A. Massal.) S.Y. Kondr. & al. and H. rheinigera (Elix & S.Y. Kondr.) S.Y. Kondr. & al., both characterized by production of an unusual, thick-walled type of ascospore (Kondratyuk & al. 2014a). Huneckia seems to be well-defined molecularly, morphologically, and chemically (see below for further discussion).
Current phylogenetic analyses based on three rDNA loci (ITS, nucLSU, and mtSSU) place Caloplaca crocina, a species producing hourglass-shaped ascospores, in Huneckia (Caloplacoideae) and Caloplaca rouxii in Calogaya (Xanthorioideae).
Wetmoreana brouardii is morphologically similar and often misidentified as Caloplaca ochraceofulva (Mull. Arg.) Jatta, for which molecular data are not yet available. Both taxa are discussed below, and the current world distribution of W. brouardii is presented.
Materials & methods
This study is based on the collections from the following herbaria: B, BM, E, G, KRAM, LD, M, MEL, MIN, S, and UPS. For species identification morphological characters were measured from dry material using a Nikon SMZ 1270 dissecting microscope. Anatomical characters were measured from hand-cut sections mounted in water using a Nikon Eclipse 50i light microscope. The conidia were measured based on photographs. To study the thallus anatomy of W. brouardii and C. ochraceofulva high-quality cross sections of lobes were prepared by selecting lobes which overlap other lichen thalli if possible. The granulation of anatomical structures was observed in polarized light, and solubility of granules/crystals and colour reactions were determined using 25% KOH (K) and 65% nitric acid (N). Hydrochloric acid (HCl) was used to test for the presence of calcium carbonate (CaCO,) in the rocky substrate. Thallic and apothecial terminology follows Bungartz (2002) and Ryan & al. (2002, 2012). Photographic documentation was made with a Nikon DS-Fi2 digital camera combined with the imaging software NIS-Elements D v. 4.30.
The sequences used in the study were sourced from Wilk & al. (2021) and references therein (see Table 1 for voucher information and GenBank accession numbers). The datasets were subjected to maximum likelihood (ML) analysis in RAXML v. 8.2.0 (Stamatakis 2014) under the GTR-Gamma model. Branch support was assessed by bootstrapping (100 replicates). Phylogenetic trees were visualized and edited in FigTree v. 1.4.4 (Rambaut 2018) and Inkscape v. 0.92 graphic software (http://inkscape.org).
The current phylogenetic analyses are a continuation of the study started by Wilk & al. (2021), and the phylogenetic Teloschistaceae tree therein was used as reference tree for this survey.
389
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Blastenia_ammiospila lastenia_crenularia
‘Caloplaca'_lecanorocarpa *Caloplaca'_lecapustulata
= Huneckia_crocina_comb. nov.
100,
Fic. 1. Phylogenetic placement of Huneckia crocina within the subfamily Caloplacoideae derived from maximum likelihood (ML) analyses of rDNA ITS, nucLSU, and mtSSU loci. ML bootstrap values are presented at the nodes. Squamulea subsoluta was used to root the tree. Huneckia genus, including H. crocina, is marked with grey.
Phylogenetic results
The phylogenetic analyses based on three rDNA loci (ITS, nuLSU and mtSSU) nest Caloplaca crocina within Caloplacoideae with a strongly supported (BS = 99) sister relationship to Huneckia pollinii and H. rheinigera (Fic. 1; see also Wilk & al. 2021: Fig. 1, Suppl. Fig. 1). Within the C. crocina clade is clearly separated from the latter two species by its long branch. The Huneckia clade is sister to ‘Caloplaca’ lecapustulata Aptroot & M. Caceres and ‘C. lecanorocarpa Aptroot & M. Caceres, but with only moderate support (BS = 79). The relationship of Huneckia to other representatives of Caloplacoideae is resolved without support, indicating its close relationship to Blastenia A. Massal., Eilifdahlia S.Y. Kondr. & al., Franwilsia S.Y. Kondr. & al., Gyalolechia A. Massal., and ‘Caloplaca’ fernandeziana (Zahlbr.) Follmann & Redon. Before our research, the phylogenetic position of C. crocina was unknown, although its potential placement in Huneckia could be inferred based on certain morphological characters, especially the thick walls of the ascospores. Thick-walled ascospores, however, cannot be treated as distinctive for the genus, because this type of ascospore occurs also in Flavoplaca Arup & al. [e.g., FE dichroa (Arup) Arup & al. and F. calcitrapa (Nav.-Ros. & al.) Arup & al.; Xanthorioideae}.
The phylogenetic analyses based on three-loci dataset (ITS, nuLSU, and mtSSU) nests Caloplaca rouxii within Calogaya (Xanthorioideae) (Wilk & al. 2021: Fig. 1, Suppl. Fig. 1). Within the Calogaya clade C. rouxii, C. arnoldiiconfusa Gaya & Nav.-Ros., and C. saxicola (Hoffm.) Nordin form a
Calogaya & Huneckia combs. nov. (South America) ... 393
Xanthoria_parietina 0 Calogaya_lobulata2 Calogaya_lobulata1 45 &2logaya_amoldii_subsp_obliterata Calogaya_arnoldii_s_lat pp ouaveanol ii1 Calogaya_arnoldii2
Calogaya_arnoldiiconfusa
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Calogaya_schistidii Calogaya_sp Calogaya_pusilla2
Calogaya_pusilla1 Calogaya_alaskensis
Calogaya_polycarpoides Calogaya_biatorina3 ie Calogaya_biatorina1
= Calogaya_biatorina4
0.03 Calogaya_biatorina2
Fic. 2. Phylogenetic placement of Calogaya miniata (marked in grey) within the subfamily Xanthorioideae derived from maximum likelihood (ML) analyses of rDNA ITS locus. ML bootstrap values are presented at the nodes. Xanthoria parietina was used to root the tree.
well-supported (BS = 95) group of closely related taxa (Fic. 2). The phylogenetic position of Caloplaca rouxii within Calogaya was also studied in detail by Gaya & al. (2011), who noted the monophyly of C. rouxii, while C. saxicola appears monophyletic or polyphyletic depending on the phylogenetic analysis. The polyphyly of C. saxicola has been discussed in detail by Gaya & al. (2011) and Vondrak & al. (2018).
Taxonomy: new combinations
Calogaya miniata (Hoffm.) Wilk & Liicking, comb. nov. MB 839870 = Psora miniata Hoffm., Enum. Lich.: 63 (1784); Descr. Pl. Cl. Crypt. 3(2): 16 (1801). Type: Spain. Catalunya, Lleida, Alt Urgell, Figols I Alinya, entre el Perdé dels Quatre Batlles I el Prat Llarg, elev. 2200-2382 m, 2001, Navarro-Rosinés (BCN, neotype, designated by Gaya 2009). = Lichen miniatus Hoftm., Enum. Lich.: 62 (1784) [nom. illeg., ICN (Shenzen) Art. 53, non Lichen miniatus L 1753]. = Lobaria miniata (Hoftm.) Hoftm., Deutschl. Fl. 2: 158 (1796) [“1795”]. = Caloplaca rouxii Gaya, Nav.-Ros. & Llimona, Biblioth. Lichenol. 101: 82 (2009) [nom. illeg., ICN (Shenzen) Art. 52].
394 ... Wilk
For taxonomic description, distribution, illustrations, and further synonyms, see Gaya (2009).
NOMENCLATURAL NOTES—Calogaya miniata was first described by Hoffmann (1784: 62), under the name Lichen miniatus Hoftm.., an illegitimate later homonym of L. miniatus L. Gaya (2009) proposed Caloplaca rouxii as a replacement name for the illegitimate L. miniatus Hoffm. However, Hoffmann (1784: 62-63) had originally published two alternative names (L. miniatus and Psora miniata) for this species, both of which are valid [ICN (Shenzhen) Art. 36.3], but as Lichen miniatus Hoftm. is illegitimate, Psora miniata remains the legitimate basionym of the species, a name also used in a subsequent treatment of the species by the same author (Hoffmann 1801). Gaya’s (2009) replacement name Caloplaca rouxii is superfluous and illegitimate, because Gaya (2009) cited Lichen miniatus Hoffm. as the replaced synonym and Psora miniata is an alternative name based on the same type [ICN (Shenzhen) Arts 52.1, 52.2(e)].
Hoffmann (1796: 158) also published the combination Lobaria miniata, based on Lichen miniatus Hoftm. Subsequently, this has been interpreted as being based on Lichen miniatus L., being cited as Lobaria miniata (L.) Hoffm. and interpreted as a homotypic synonym of Dermatocarpon miniatum (L.) W. Mann. However, Hoffmann’s combination is clearly based on Lichen miniatus Hoftm., not L. miniatus L., both explicitly [“Enum. Lich. 62. (Lich. miniatus)”| and implicitly by describing the lichen as “foliois ... miniatis,’ i.e., scarlet or cinnabar-red, and not grey as in D. miniatum. The correct citation of this combination is therefore Lobaria miniata (Hoftm.) Hoffm. If Hoffmann had not already established the alternative name Psora miniata twelve years prior in 1784, Lobaria miniata (as a replacement name for L. miniatus Hoffm.) would have had priority over the erroneously presumed first publication of Psora miniata five years later in 1801.
Hoffmann (1784) did not cite any material in the protologue of Lichen miniatus/Psora miniata. Later he provided a color plate under the name Psora miniata (Hoffmann 1801: Tab. LX). However, as it cannot be established that this illustration and its underlying specimen were part of the original material, they are not available for lectotypification and have no priority in terms of typification. The neotypification proposed by Gaya (2009) is therefore appropriate.
Calogaya & Huneckia combs. nov. (South America) ... 395
Fic. 3. Wetmoreana brouardii, habitus and cross section of thallus: A. Wetmore 69973 (MIN); B, C. Wetmore 79665 (MIN). Caloplaca ochraceofulva, habitus and cross section of thallus: D. Geesteranus 10299 (LD); E, E. Kofler (LD1066528). B, E = in regular light; C, F = in polarized light. Scale bars: A = 2.5 mm; B,C, E, F = 50 um; D =2 mm.
Huneckia crocina (Kremp.) Wilk, comb. nov. MB 836903 = Lecidea crocina Kremp., Flora 61: 519 (1878). Type: Argentina. 1873-1874, Lorentz & Hieronymus (MI, holotype). = Caloplaca crocina (Kremp.) Wilk & R. Vargas, Mycotaxon 132: 127 (2017).
396 ... Wilk
Additional synonyms, taxonomic description, distribution, and illustrations are available in Wilk & Flakus (2017).
TAXONOMIC NOTES—Huneckia includes three species: H. pollinii (type species), H. rheinigera (Kondratyuk & al. 2014a), and the newly transferred H. crocina. These species are morphologically similar to one another. They produce continuous to areolate grayish thalli and dark orange to brownish, biatorine or zeorine apothecia. The apothecial margin (true exciple) is prosoplectenchymatous, composed of radiating, conglutinating hyphae. The ascospores are polarilocular, characterized by clearly thickened terminal spore walls (also called hourglass-shaped, sand-clock, or sand-glass types). The diagnostic characters for these and similar Caloplaca s.lat. species are discussed in Wilk & Flakus (2017: Table 1). Huneckia is characterized by specific anthraquinones, mainly chrysophanol, chrysophanal and rhein (Kondratyuk & al. 2014a), although the chemical composition of lichen secondary metabolites present in H. crocina has not been studied. The genus is mostly similar to Blastenia. For characters distinguishing among these taxa see Vondrak & al. (2019). Huneckia pollinii is widespread in the Northern Hemisphere (Wetmore 1994; Miao & al. 2018), H. rheinigera is known from Australia (Kondratyuk & al. 2007), and H. crocina is common in South America (Wilk & Flakus 2017). Huneckia pollinii and H. rheinigera are well-illustrated in Schumm & Aptroot (2019a,b) and H. crocina in Wilk & Flakus (2017).
Taxonomy: new records
Wetmoreana brouardii (B. de Lesd.) Wilk & Sachting, Pl. Fung. Syst. 65(2): 562. 2020. Fic. A-C A taxonomic description is available in Wetmore & Karnefelt (1998).
SPECIMENS EXAMINED— CHILE. VaLparaiso, Cuesta de Chacabuco, Follmann 12885 (B). COLOMBIA. CunDINAMARCA, Narifio, Munic. Imues, near El Pedregal, towards Tuquerres, on road Pasto-Tumaco, elev. 1880 m, 16 June 1986, Sipman 33540 (B). PERU. Dept. AREQUIPA, Prov. Caylloma, Canon del Colca canyon, below Tapay village, open semi-desert montane area, elev. 2774 m, 6 July 2006, Flakus 9663 & Cykowska (KRAM; fertile specimen). URUGUAY. Dept. CANELONES, Parador Tajes, El Cerroto, elev. 10- 20 m, 19 Feb 1950, Osorio 2135 (B). MEXICO. Baja CALIFORNIA Sour, Sierra Laguna, along river bottom Picacho de La Laguna, elev. 500 m, 16 Feb 1993, Wetmore 72011 (B), open oak forest (Quercus tuberculata) with shrubs, along ridge leading to the crest after turnoff to Rancho La Victoria, elev. 1400 m, 6 Jan 1998, Wetmore 79665 (MIN). CHIHUAHUA, Sierra la Cinguita, eastern side, 9 km west of Moctezuma along route 10, elev. 1120 m, 16 March 1992, Wetmore 69973 (MIN).
MATERIAL INVESTIGATED FOR COMPARISON—Caloplaca ochraceofulva. (Fic. 3, D-F) KENYA. RIFT VALLEY PROVINCE, distr. Nakuru, 1949, Geesteranus 10299 & L4644a
Calogaya & Huneckia combs. nov. (South America) ...
TABLE 2. Comparison of Wetmoreana brouardii and Caloplaca ochraceofulva
CHARACTERS
VEGETATIVE PROPAGULES
SPORES (um) SEPTUM (um)
THALLUS
LOBE THICKNESS (tm) CORTEX
CORTEX CONES ALGAE
MEDULLA
CaAOX CRYSTALS
PYCNIDIA
Conrpia (ttm)
SUBSTRATE
DISTRIBUTION
REFERENCES
W. brouardii
Papillae, laminal
10-13 x 4-6 2.5-3.5
Thin
90-250 Cell lumina rounded Absent or indistinct Continuous Thin, indistinctly separated from the algae layer
Absent (medulla may illuminated in polarized light due to the lichen substances, in K & N insoluble)
Rare
Long bacilliform, 4.0 x 1.1 (mean)
Siliceous rocks
Widespread in Americas, and Arabian Peninsula
This paper
C. ochraceofulva
Isidia, marginal 10-16 x 4-8 2-4 Thick 130-400 Cell lumina elongated Distinct
Discontinuous, in distinct groups
Thick, distinctly separated
Distinct layer (35-75 um thick; in K
397
insoluble, in N soluble) at a distance of c.
100 pm from the thallus surface, on the border between algal layer and medulla
Common
Short bacilliform or ovoid, 3.1 x 1.2 (mean) Siliceous or calcareous rocks Widespread in Africa, and Arabian Peninsula and South America This paper
(LD). LESOTHO. LeEriBeE, Buthabuthe, 1963, Kofler s.n. (LD1066528, LD1066592), Kopje near Buthabuthe, 1963, Kofler s.n. (LD1024127). NAMIBIA, OTJOZONDJUPA REGION, Waterberg Plateau National Park, primary forest with large Ficus at the base of Waterberg Plateau, elev. 1469 m, 15 June 2019, Flakus 19/162 (KRAM, DUKE). SOMALILAND. Serrubgebirge, 1885, Hildebrandt s.n. (G66459, Lectotypus). SOUTH AFRICA. Natal, Vryheid Div., 1953, Almborn 7976 (LD1024960, LD1024896; fertile specimens). ORANGE FREE StaTE, Div. Ladybrand, 1949, Geesteranus L6546 (LD). SAUDI ARABIA. Asir ReGion, Al Dalaghan area, Asir National Park, 1982, Zapletal s.n. (BM1247493, E905776, E905777). ARGENTINA, Jujuy, Santa Barbara, 1901, Fries 50 (LD). URUGUAY, Dept. MALDONADO, Rio de la Plata, Isla Gorriti, 1984, Osorio
8345 (MIN).
TAXONOMIC NOTE—Wetmoreana brouardii is characterized by the clearly
lobate, thin thallus, closely appressed to the substratum. The thallus is orange to reddish, abundantly covered by distinct, laminal papillae. According to Wetmore & Karnefelt (1998) apothecia are very rare, sessile, and <0.5 mm; the ascospores are polarilocular (11-14 x 5.5-7.0 um) with a 3.5-4.0 um thick
septum.
Wetmoreana brouardii is often misidentified as Caloplaca ochraceofulva, which is closely related (Wilk & Licking, unpubl. data) but which differs from
398 ... Wilk
W. brouardii in having a distinctly thicker, yellow-orange (not reddish) and isidiate thallus. Another distinguishing feature is the presence or absence of calcium oxalate crystals (pol+ white) in the thallus. They are present in C. ochraceofulva, forming a distinct layer along the border between the algal layer and medulla, but absent in all studied material of W. brouardii (Fie. 3, TABLE 2). Medullary crystals are diagnostic for other Wetmoreana species, such as W. appressa, W. texana, and the probably related Caloplaca eugyra (Tuck.) Zahlbr. (Wetmore & Karnefelt 1998).
HABITAT AND DISTRIBUTION— Wetmoreana brouardii occurs on siliceous rocks. It was reported from North America in Mexico and USA (Nash & al. 1998; Wetmore & Karnefelt 1998); from the Arabian Peninsula in Saudi Arabia (Bokhary & al. 1993) and Qatar (Al-Thani & Al-Meri 2011); from Central America in Guatemala (Wetmore & Karnefelt 1998), and from South America in Brazil (Aptroot & al. 2017), Ecuador (Galapagos Islands), (Bungartz & al. 2013), and Venezuela (Aptroot 2015).
New records of Wetmoreana brouardii are reported here from Chile, Peru, Uruguay, and Colombia. The Peruvian material cited previously by Wetmore & Karnefelt (1998) lacked locality data, provided here.
Acknowledgements
I am grateful to R. Licking (BGBM, Germany), M. Kukwa (UG, Poland), A. Beck (BSM, Germany), and Shaun Pennycook for reviewing the manuscript and providing important suggestions and improvements. I thank the curators of the herbaria B, BM, E, G, KRAM, LD, M, MEL, MIN, S and UPS for loan of specimens. Financial support was provided by the National Science Centre (NCN, grant no. N N303 821740).
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