Abstract
Clavulina J. Schröt. accommodates species usually with coralloid, occasionally simple, infundibuliform, effuse-coralloid, or resupinated basidiomata, typically with two curved sterigmata and hyaline, smooth, guttulated basidiospores. During surveys in the Brazilian Amazon and Northeast Atlantic Rain Forest, several specimens of Clavulina were collected, and, after morphological and DNA analyses based in ITS and nLSU, some of them could not be assigned to known taxa. Thus, six new species are proposed: Clavulina alba, sp. nov. has white basidiomata with cylindrical to flattened branches; C. crystallifera, sp. nov. and C. cystidiata, sp. nov. have crystals among the hyphae, but C. cystidiata has also cystidia; C. simplex, sp. nov. and C. studerae, sp. nov. have simple basidiomata, while C. terminalis, sp. nov. is characterized mainly by the presence of hyphal ends. In addition, the synonymization of C. paraincrustata to C. incrustata is proposed. Description, images and discussion of the new species and the synonymization are provided, as well as insights into the morphological characters, ecology and distribution of Clavulina species.
Similar content being viewed by others
Data availability
All material is deposited in Herbarium URM and TENN. The sequences are deposited in GenBank. Data will be available online after the acceptance of the manuscript in http://www.splink.org.br/ and https://www.ncbi.nlm.nih.gov/genbank/.
Code availability
Not applicable.
References
Argüelles-Moyao A, Garibay-Orijel R, Márquez-Valdelamar LM, Arellano-Torres E (2017) Clavulina-Membranomyces is the most important lineage within the highly diverse ectomycorrhizal fungal community of Abies religiosa. Mycorrhiza 27:53–65. https://doi.org/10.1007/s00572-016-0724-1
Berkeley MJ (1856) Decades of fungi. Decades LXI - LXII. Rio Negro fungi. Hooker’s J Bot Kew Gard Misc 8:272–280
BFG - The Brazil Flora Group (2015) Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia 66:1085–1113. https://doi.org/10.1590/2175-7860201566411
Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian atlantic forest hotspot. Science 323:785–789. https://doi.org/10.1126/science.1166955
Corner EJH (1950) A monograph of Clavaria and allied genera. Dawson of Pall Mall, London, p 740
Corner EJH (1953) Addenda Clavariacea. III. Ann Bot 17(66):347–368. https://doi.org/10.1093/oxfordjournals.aob.a083355
Corner EJH (1966) The clavarioid complex of Aphelaria and Tremellodendropsis. Trans Brit Mycol Soc 39(2):205–211. https://doi.org/10.1016/S0007-1536(66)80054-2
Corner EJH (1970) Supplement to a monograph of Clavaria and allied genera. Nova Hedwigia Beih 33:1–299
Crous PW, Wingfield MJ, Lombard L et al (2019) Fungal Planet description sheets: 951–1041. Persoonia 43:223–425. https://doi.org/10.3767/persoonia.2019.43.06
de Meiras-Ottoni A, Araujo-Neta LS, Gibertoni TB (2017) A checklist of clavarioid fungi (Agaricomycetes) recorded in Brazil. Mycotaxon 132:1–22
Douanla-Meli CM (2007) Fungi of Cameroon. Bibl Mycol 202:1–410
Duhem B, Buyck B (2007) Edible mushrooms from Madagascar (2). Clavulina albiramea comb. nov. (Cantharellales), an edible clavarioid fungus shared between African miombo and Malagasy Uapaca woodland. Nova Hedwigia 85:317–330. https://doi.org/10.1127/0029-5035/2007/0085-0317
Feng B, Wang XH, Ratkowsky D, Gates G, Lee SS, Grebenc T, Yang ZL (2016) Multilocus phylogenetic analyses reveal unexpected abundant diversity and significant disjunct distribution pattern of the Hedgehog Mushrooms (Hydnum L.). Sci Rep 6:25586. https://doi.org/10.1038/srep25586
Franchi P, Marchetti M (2018) Due nuove specie italiane del Genere Clavulina. Riv Micol 61(1):3–21
Furtado ANM, Daniëls PP, Neves MA (2016) New species and new records of Clavariaceae (Agaricales) from Brazil. Phytotaxa 253(1):001–026. https://doi.org/10.11646/phytotaxa.253.1.1
Furtado ANM, Daniëls PP, Reck MA, Neves MA (2021) Scytinopogon caulocystidiatus and S. foetidus spp. nov., and five other species recorded from Brazil. Mycotaxon 136(1):107–130. https://doi.org/10.5248/136.107
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes: application to identification of mycorrhizae and rusts. Mol Ecol 2:113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Goés-Neto A, Loguercio-Leite C, Guerrero RT (2005) DNA extraction from frozen field-collected and dehydrated herbarium fungal basidiomata: performance of SDS and CTAB-based methods. Biotemas 18:19–32. https://doi.org/10.5007/%25x
Grebenc T, Martín MP, Kraigher H (2009) Ribosomal ITS diversity among the European species of the genus “Hydnum” (Hydnaceae). An del Jardín Botánico Madrid 66S1:121–132. https://doi.org/10.3989/ajbm.2221
He G, Chen SL, Yan SZ (2016) Morphological and molecular evidence for a new species in Clavulina from southwestern China. Mycoscience 57:255–263. https://doi.org/10.1016/j.myc.2016.03.002
Henkel TW, Meszaros R, Aime MC, Kennedy A (2005) New Clavulina species from the Pakaraima Mountains of Guyana. Mycol Prog 4:343–350. https://doi.org/10.1007/s11557-006-0140-6
Henkel TW, Aime MC, Uehling JK, Smith ME (2011) New species and distribution records of Clavulina (Cantharellales, Basidiomycota) from the Guiana Shield. Mycologia 103:883–894. https://doi.org/10.3852/10-355
Hyde KD, Hongsanan S, Jeewon R et al (2016) Fungal diversity notes 367–490: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 80(1):1–270. https://doi.org/10.1007/s13225-016-0373-x
Kalyaanamoorthy S, Minh BQ, Wong TKF, Von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Katoh K, Rozewicki J, Yamada KD (2017) MAFFT online service: multiple sequence alignment interactive sequence choice and visualization. Brief Bioinform bbx108. https://doi.org/10.1093/bib/bbn013
Kennedy PG, Matheny PB, Ryberg KM, Henkel TW, Uehling JK, Smith ME (2012) Scaling up: examining the macroecology of ectomycorrhizal fungi. Mol Ecol 21:4151–4154. https://doi.org/10.1111/j.1365-294X.2012.05703.x
Kornerup A, Wanscher JH (1978) Methuen handbook of colour, 3rd edn. Eyre Methuen Ltd., London
Kotiranta H, Larsson K-H (2013) Sistotrema luteoviride sp. nov. (Cantharellales, Basidiomycota) from Finland. Acta Mycologica 48(2):219–225. https://doi.org/10.5586/am.2013.023
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msy096
Langer E (2001) Phylogeny of non-gilled and gilled basidiomycetes -DNA sequence inferrence, ultrastructure and comparative morphology. Thesis
Larsson K-H (2007) Re-thinking the classification of corticioid fungi. Mycol Res 111:1040–1063. https://doi.org/10.1016/j.mycres.2007.08.001
Larsson E, Larsson K-H, Kõljalg U (2004) High phylogenetic diversity among corticioid homobasidiomycetes. Mycol Res 108(9):983–1002. https://doi.org/10.1017/S0953756204000851
Leal-Dutra CA, Neves MA, Griffith GW, Reck MA, Clasen LA, Dentinger BTM (2018) Reclassification of Parapterulicium Corner (Pterulaceae, Agaricales), contributions to Lachnocladiaceae and Peniophoraceae (Russulales) and introduction of Baltazaria gen. nov. MycoKeys 37:39–56. https://doi.org/10.3897/mycokeys.37.26303
Leal-Dutra CA, Griffith GW, Neves MA, McLaughlin DJ, McLaughlin EG, Clasen LA, Dentinger BTM (2020) Reclassification of Pterulaceae Corner (Basidiomycota: Agaricales) introducing the ant-associated genus Myrmecopterula gen. nov., Phaeopterula Henn. and the corticioid Radulomycetaceae fam. nov. IMA Fungus 11:1–24. https://doi.org/10.1186/s43008-019-0022-6
Meiras-Ottoni A, Larsson KH, Gibertoni TB (2021) Additions to Trechispora and the status of Scytinopogon (Trechisporales, Basidiomycota). Mycol Prog 20:203–222. https://doi.org/10.1007/s11557-021-01667-y
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE), 2010, New Orleans, Louisiana. Piscataway, NJ: IEEE 1–8. https://doi.org/10.1109/GCE.2010.5676129
Moncalvo JM, Nilsson RH, Koster B, Dunham SM, Bernauer T, Matheny PB, Mclenon T, Margaritescu S, Weiß M, Garnica S, Danell E, Langer G, Langer E, Larsson E, Larsson KH, Vilgalys R (2006) The cantharelloid clade: dealing with incongruent gene trees and phylogenetic reconstruction methods. Mycologia 98:937–948. https://doi.org/10.3852/mycologia.98.6.937
Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Olariaga I, Begoña MJ, García-Etxerbarria K, Salcedo I (2009) Species delimitation in the European species of Clavulina (Cantharellales, Basidiomycota) inferred from phylogenetic analyses of ITS region and morphological data. Mycol Res 113:1261–1270. https://doi.org/10.1016/j.mycres.2009.08.008
Pérez-Pazos E, Villegas-Ríos M, Garibay-Orijel R, Salas-Lizana R (2019) Two new species of Clavulina and the first record of Clavulina reae from temperate Abies religiosa forests in central Mexico. Mycol Prog 18:1187–1200. https://doi.org/10.1007/s11557-019-01516-z
Petersen RH (1967) Notes of clavarioid fungi VI. Two new species and notes on the origin of Clavulina. Mycologia 59:39–47. https://doi.org/10.1080/00275514.1967.12018393
Petersen RH (1983) Notes on clavarioid fungi XVIII. A preliminary outline of Clavulina in Southeastern Australia. Nova Hedwigia 37:19–35
Petersen RH (1988) Notes on clavarioid fungi XXII Three interesting South American collections. Mycologia 80:571–576. https://doi.org/10.2307/3807861
Petersen RH (1988a) The clavarioid fungi of New Zealand. DSIR Science Information Publishing Centre Wellington [Nueva Zelandia]
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14(9):817–818. https://doi.org/10.1093/bioinformatics/14.9.817
Roberts P (1999) Clavarioid fungi from Korup National Park, Cameroon. Kew Bull 54:517–539. https://doi.org/10.2307/4110853
Rodrigues P, Venâncio A, Kozakiewicz Z, Lima N (2009) A polyphasic approach to the identification of aflatoxigenic and non-aflatoxigenic strains of Aspergillus section Flavi isolated from Portuguese almonds. Int J Food Microbiol 129:187–193. https://doi.org/10.1016/j.ijfoodmicro.2008.11.023
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Salas-Lizana R, Villegas-Ríos M, Alvarez-Manjarrez J, Pérez-Pazos E, Farid A, Franck A, Smith ME, Garibay-Orijel R (2023) Neotropical Clavulina: two new species from Mexico and a re-evaluation of Clavulina floridana. Mycologia 1–18. https://doi.org/10.1080/00275514.2022.2148191
Smith ME, Henkel TW, Uehling JK, Fremier AK, Clarke HK, Vilgalys R (2013) The ectomycorrhizal fungal community in a neotropical forest dominated by the endemic dipterocarp Pakaraimaea dipterocarpacea. PLOS ONE 8:e55160. https://doi.org/10.1371/journal.pone.0055160
Staden R, Beal KF, Bonfield JK (1998) The Staden Package. Computer Methods in Molecular Biology 132:115–130, In: Bioinformatics Methods and Protocols Eds Misener, S., Krawetz, S.A. Totowa. Humana Press. https://doi.org/10.1385/1-59259-192-2:115
Studer A, Nusbaumer L, Spichiger L. (Eds.) (2015) Biodiversidade da Reserva Biológica de Pedra Talhada. Biossiera 68.
Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sunderland. Sinauer Associates.
Tabosa FRS, Almeida EM, Melo E, Loiola MIB (2016) Flora do Ceará, Brasil: Polygonaceae. Rodriguésia 67:981–996. https://doi.org/10.1590/2175-7860201667409
Thacker JR, Henkel TW (2004) New species of Clavulina from Guyana. Mycologia 96:650–657. https://doi.org/10.1080/15572536.2005.11832961
Tibpromma S, Hyde KD, Jeewon R et al (2017) Fungal diversity notes 491–602: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 83:1–261. https://doi.org/10.1007/s13225-017-0378-0
Trappe JM, Castellano MA (2007) Clavulina lilliputiana, a diminutive new species from Tasmania. Australian Mycologist 25:87–89
Trifinopoulos J, Nguyen LT, Von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44(W1):W232–W235. https://doi.org/10.1093/nar/gkw256
Uehling JK, Henkel TW, Aime MC, Vilgalys R, Smith ME (2012a) New species and distribution records for Clavulina (Cantharellales, Basidiomycota) from the Guiana Shield, with a key to the lowland neotropical taxa. Fungal Biol 116:1263–1274. https://doi.org/10.1016/j.funbio.2012.09.004
Uehling JK, Henkel TW, Aime MC, Vilgalys R, Smith ME (2012b) New species of Clavulina with effused or resupinate basidiomata from the Guiana Shield. Mycologia 104:547–556. https://doi.org/10.3852/11-130
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
Wartchow F (2012a) Clavulina incrustata, a new species from Pernambuco. Brazil Cryptog Mycolog 33(1):105–113. https://doi.org/10.7872/crym.v33.iss1.2012.105
Wartchow F (2012b) Clavulina amazonensis, an Amazonian fungus discovered in the Atlantic Forest. Tomo 37(1):113–117
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a Guide to Methods and Applications 18:315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Wu CL, He Y, Yan J (2019) Two new species of Clavulina (Cantharellales) from southwestern China based on morphological and molecular evidence. Mycol Prog 18:1071–1078. https://doi.org/10.1007/s11557-019-01506-1
Yuan HS, Lu X, Dai YC et al (2020) Fungal diversity notes 1277–1386: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 104:1–266. https://doi.org/10.1007/s13225-020-00461-7
Acknowledgements
We would like to thank Nelson Lima and Carla Santos for the access to Laboratório de Micologia Aplicada of the Universidade do Minho and help in obtaining the RPB2 sequences; Roberto Garibay-Orijel and his team for sharing their unpublished data about Clavulina; Laura Briscoe from Herbarium NY, Lee Davies from Herbarium K and Lisa Castlebury from Herbarium BPI for the help with the type-specimens; Capes and CNPq for the doctorate scholarship of AMO; Pós-Graduação em Biologia de Fungos (UFPE, Brazil), Capes (Capes-SIU 008/13), CNPq (PQ 307601/2015-3, ICMBio 421241/2017-9, PQ 302941/2019-3) and FACEPE (APQ 0375-2.03/15, APQ-0003-2.03/18) for financing this research.
Funding
This research was funded by Capes (Capes-SIU 008/13), CNPq (PQ 307601/2015–3, ICMBio 421241/2017–9, PQ 302941/2019–3) and FACEPE (APQ 0375–2.03/15, APQ-0003–2.03/18).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Angelina de Meiras-Ottoni. The manuscript was written by all authors. All authors read and approved the final manuscript. Tatiana B. Gibertoni provided funds and supervised this research.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Marco Thines
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
de Meiras-Ottoni, A., Gibertoni, T.B. Clavarioid fungi from Brazil: novelties in Clavulina (Cantharellales). Mycol Progress 22, 25 (2023). https://doi.org/10.1007/s11557-023-01873-w
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11557-023-01873-w