Opuscula Philolichenum, 11: 4-10. 2012. *pdf available online 3January2012 via (http://sweetgum.nybg.org/philolichenum/)

An evolving phylogenetically based taxonomy of lichens and allied fungi BRENDAN P. HODKINSON1 ABSTRACT. – A taxonomic scheme for lichens and allied fungi that synthesizes scientific knowledge from a variety of sources is presented. The system put forth here is intended both (1) to provide a skeletal outline of the lichens and allied fungi that can be used as a provisional filing and databasing scheme by lichen herbarium/data managers and (2) to announce the online presence of an official taxonomy that will define the scope of the newly formed International Committee for the Nomenclature of Lichens and Allied Fungi (ICNLAF). The online version of the taxonomy presented here will continue to evolve along with our understanding of the organisms. Additionally, the subfamily Fissurinoideae Rivas Plata, Lücking and Lumbsch is elevated to the rank of family as Fissurinaceae. KEYWORDS. – higher-level taxonomy, lichen-forming fungi, lichenized fungi, phylogeny

INTRODUCTION Traditionally, lichen herbaria have been arranged alphabetically, a scheme that stands in stark contrast to the phylogenetic scheme used by nearly all vascular plant herbaria. The justification typically given for this practice is that lichen taxonomy is too unstable to establish a reasonable system of classification. However, recent leaps forward in our understanding of the higher-level classification of fungi, driven primarily by the NSF-funded Assembling the Fungal Tree of Life (AFToL) project (Lutzoni et al. 2004), have caused the taxonomy of lichen-forming and allied fungi to increase significantly in stability. This is especially true within the class Lecanoromycetes, the main group of lichen-forming fungi (Miadlikowska et al. 2006). Published here is a higher-level classification of lichens and allied taxa that synthesizes information from various types of analyses. This scheme is adapted from the system currently in use at the New York Botanical Garden (NY), which houses one of the few lichen herbaria in the world to have specimens filed phylogenetically. While taxonomic assignments are based on published data, reason and logic were used in assessing these data, and some taxonomic shifts have been made even when authors neglected to explicitly state their necessity. Thus, this work attempts to achieve a synthesis of our current knowledge of the higher level systematics of lichenized fungi through critical evaluation of the literature. This approach differs markedly from the one used to compile other higher level organizational schemes that include lichen-forming fungi. The outline presented below is available online (http://sweetgum.nybg.org/lichens/), and will be continually updated as our understanding of the organisms changes. This scheme (with the worldwide checklist of lichenicolous fungi as a supplement; http://www.lichenicolous.net/; Lawrey & Diederich 2011) represents the scope of the fungal taxa within the domain of the newly-established International Committee for the Nomenclature of Lichens and Allied Fungi (ICNLAF); for taxa containing both lichens and nonlichens, collaboration with other committees will take place as needed. Therefore, this work serves two purposes: (1) to provide a skeletal outline of the lichens and allied fungi that can be used as a provisional scheme by herbarium/data managers and (2) to announce the online presence of an evolving taxonomic system that defines the intended scope of the ICNLAF.

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BRENDAN P. HODKINSON – International Plant Science Center, The New York Botanical Garden, 2900 Southern Blvd., Bronx, NY 10458-5126, U.S.A. – e-mail: [email protected]

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TAXONOMY In this publication, taxa that are known to be closely related are placed closer to one another, with alphabetical listing generally used only when relationships between taxa cannot be inferred with confidence based on the data at hand. Portions of the outline that differ from recent taxonomic compilations (e.g., Lumbsch & Huhndorf 2010, Smith et al. 2009) are generally annotated with citations from publications that suggest the placement given here. While the outline contains several of the main groups of ascomycetous lichenicolous fungi, many families containing members with this lifestyle are not represented; for a phylogenetically-arranged list of these fungi, please refer to the worldwide checklist of lichenicolous fungi online (http://www.lichenicolous.net/; Lawrey & Diederich 2011). For a list of the genera in each of the ascomycetous families outlined below, refer to Lumbsch and Huhndorf (2010), and for the full higher-level fungal classification into which the taxa are interleaved, see Hibbett et al. (2007). Phylum ASCOMYCOTA Subphylum PEZIZOMYCOTINA Class ARTHONIOMYCETES Arthoniales Chrysothricaceae Arthoniaceae Roccellaceae Class DOTHIDEOMYCETES Subclass Dothideomycetidae Capnodiales Antennulariaceae Subclass Uncertain Patellariales Patellariaceae Trypetheliales Trypetheliaceae Order uncertain Arthopyreniaceae Dacampiaceae Lichenotheliaceae Mycoporaceae Naetrocymbaceae Class EUROTIOMYCETES Subclass CHAETOTHYRIOMYCETIDAE Pyrenulales Celotheliaceae Pyrenulaceae Verrucariales Adelococcaceae Verrucariaceae Subclass MYCOCALICIOMYCETIDAE Mycocalicales Mycocaliciaceae Sphinctrinaceae Class LICHINOMYCETES Lichinales Gloeoheppiaceae Heppiaceae Lichinaceae

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Peltulaceae Class LECANOROMYCETES Subclass ACAROSPOROMYCETIDAE Acarosporales Acarosporaceae Subclass CANDELARIOMYCETIDAE [Analyses by Miadlikowska et al. (2006) and Schoch et al. (2009) support the recognition of this as a distinct subclass.] Candelariales Candelariaceae Subclass LECANOROMYCETIDAE Rhizocarpales [Analyses by Schoch et al. (2009) indicate that this represents the most basal lineage in Lecanoromycetidae, as defined here.] Rhizocarpaceae Lecideales [Analyses by Miadlikowska et al. (2006) and Schmull et al. (2011) support the recognition of this as a distinct order.] Lecideaceae Peltigerales Collematineae Coccocarpiaceae Collemataceae Placynthiaceae Pannariaceae Peltigerineae Peltigeraceae Lobariaceae Nephromataceae Massalongiaceae [Family established by Wedin et al. (2007).] Vahliellaceae [Family established by Wedin et al. (2011).] Lecanorales Catillariaceae Psoraceae Gypsoplacaceae Pilocarpaceae Cladoniaceae Stereocaulaceae Sphaerophoraceae Calycidiaceae Mycoblastaceae [Including Tephromelataceae based on analyses by Miadlikowska et al. (2006).] Ramalinaceae [Including Crocyniaceae and Megalariaceae based on analyses by Ekman et al. (2008).] Scoliciosporaceae Haematommataceae Lecanoraceae Parmeliaceae Dactylosporaceae Miltideaceae Pachyascaceae Teloschistales Physciineae Physciaceae [Including Caliciaceae based on, e.g., Schmull et al. (2011).] Teloschistineae Brigantiaeaceae [Placement supported by Gaya et al. (2010).] Letrouitiaceae Teloschistaceae

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Megalosporaceae Subclass OSTROPOMYCETIDEAE Sarrameanales [Order established by Hodkinson and Lendemer (2011).] Sarrameanaceae Pertusariales [Order merged/synonymized with Agyriales by Schmitt et al. (2010); name retained in accordance with Hodkinson and Lendemer (2011).] Agyriaceae [Placement supported by Schmitt et al. (2010).] Coccotremataceae Icmadophilaceae Megasporaceae Ochrolechiaceae Pertusariaceae Baeomycetales Anamylopsoraceae Baeomycetaceae Trapeliales [Order established by Hodkinson and Lendemer (2011).] Trapeliaceae Ostropales Odontotremataceae Stictidaceae Coenogoniaceae Porinaceae Sagiolechiaceae [Family established by Baloch et al. (2010).] Gyalectaceae Phlyctidaceae Gomphillaceae [Compositionally equivalent to Gomphilloideae (Walt. Watson ex Hafellner) Rivas Plata, Lücking and Lumbsch (Rivas Plata et al. 2012) minus Solorinellaceae; includes Asterothyriaceae based on analyses by Lücking et al. (2004) and Baloch et al. (2010).] Solorinellaceae [Maintained as distinct from Gomphillaceae based on Baloch et al. (2010).] Fissurinaceae comb. et stat. nov.2 [Compositionally equivalent to Fissurinoideae Rivas Plata, Lücking and Lumbsch (Rivas Plata et al. 2012).] Graphidaceae [Compositionally equivalent to Graphideae Rivas Plata, Lücking and Lumbsch (Rivas Plata et al. 2012).] Thelotremataceae [Includes Ocellularieae Rivas Plata, Lücking and Lumbsch and Thelotremateae Rivas Plata, Lücking and Lumbsch (Rivas Plata et al. 2012).] Myeloconidaceae Phaneromycetaceae Order uncertain Arctomiaceae [Analyses by Schmitt et al. (2010) suggest a possible placement in Pertusariales, but further analyses are required.] Arthrorhaphidaceae Hymeneliaceae [According to analyses by Schoch et al. (2009), the family cannot be placed in Pertusariales or Sarrameanales, but could possibly go with Baeomycetales, Ostropales, or Trapeliales.] Protothelenellaceae (‘Thrombiaceae’) Schaereriaceae [Analyses by Schmull et al. (2011) indicate that the family is nonmonophyletic and that certain members have affinities to Sarrameanales, while others appear as basal to Ostropomycetidae without support.] 2

Fissurinaceae (Rivas Plata, Lücking and Lumbsch) Hodkinson comb. et stat. nov. Mycobank #564112. Basionym. Fissurinoideae Rivas Plata, Lücking and Lumbsch, Fungal Diversity 52: 108. 2012. TYPE: Fissurina Fée.

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Thelenellaceae Subclass uncertain Umbilicariales Fuscideaceae [Placement supported by Miadlikowska et al. (2006).] Ophioparmaceae [Placement supported by Miadlikowska et al. (2006).] Umbilicariaceae Order uncertain Elixiaceae [Lumbsch et al. (2004) show an affiliation with Umbilicariales, but placement remains uncertain.] Lopadiaceae [Specific placement within Lecanoromycetes unclear based on Ekman et al. (2008).] Class LEOTIOMYCETES Helotiales Helotiaceae Class SORDARIOMYCETES Trichosphaeriales Trichosphaeriaceae Class uncertain Order uncertain Aphanopsidaceae [Data generated by Lumbsch et al. (in prep.) indicate a basal position in Leotiomyceta.] Biatorellaceae [While some species that previously belonged to Biatorella have been placed within Lecanorales, the placement of Biatorella s. str. remains unclear.] Coniocybaceae Microcaliciaceae Epigloeaceae Lyrommataceae [Established by Lücking (2008) with uncertain placement.] Melaspileaceae [Based upon morphology, the group appears to be polyphyletic, containing diverse members of uncertain placement.] Monoblastiaceae [Analyses by Nelsen et al. (2009) support placement outside of Eurotiomycetes and suggest placement in Dothideomyceta (Dothideomycetes/Arthoniomycetes clade).] Sarcopyreniaceae [Placement is uncertain, although Lumbsch & Huhndorf (2010) provide Sordariomycetes incertae sedis as a best guess for Sarcopyrenia.] Strigulaceae [Analyses by Nelsen et al. (2009) support placement outside of Eurotiomycetes and suggest placement in Dothideomyceta (Dothideomycetes/Arthoniomycetes clade).] Thelocarpaceae [Lumbsch et al. (2009) demonstrate this family to be of uncertain placement within Pezizomycotina.] Vezdaeaceae [Lumbsch et al. (2009) show the family to be within Pezizomycotina, but more specific placement is unclear.] Xanthopyreniaceae Phylum BASIDIOMYCOTA Subphylum AGARICOMYCOTINA Class AGARICOMYCETES Subclass AGARICOMYCETIDEAE Agaricales Hygrophoraceae Subclass uncertain Cantharellales Clavulinaceae

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Corticiales Family uncertain (Marchandiomphalina) Order uncertain Lepidostromataceae [Ertz et al. (2008) propose a distinct family for this group of basidiolichens.] ACKNOWLEDGEMENTS Richard Harris is thanked for his pioneering morphological research aimed at developing a phylogenetic scheme for lichens and allied fungi. The editorial work of James Lendemer on this issue of OP is also greatly appreciated. Additionally, Toby Spribille and an anonymous reviewer are thanked for helpful comments on this manuscript. The author was supported by the NSF-funded ADBC/TCN ‘Lichens, Bryophytes and Climate Change’ project grant (‘Digitization TCN Collaborative Research: North American Lichens and Bryophytes: Sensitive Indicators of Environmental Quality and Change’; EF-1115086). LITERATURE CITED Baloch, E., R. Lücking, H.T. Lumbsch and M. Wedin. 2010. Major clades and phylogenetic relationships between lichenized and non-lichenized lineages in Ostropales (Ascomycota: Lecanoromycetes). Taxon, 59 (5): 1483– 1494. Ekman S., H.L. Andersen and M. Wedin. 2008. The limitations of ancestral state reconstruction and the evolution of the ascus in the Lecanorales (lichenized ascomycota). Systematic Biology, 57: 141–156. Ertz, D., J.D. Lawrey, M. Sikaroodi, P.M. Gillevet, E. Fischer, D. Killmann and E. Sérusiaux. 2008. A new lineage of lichenized basidiomycetes inferred from a two genes phylogeny: the Lepidostromataceae with three species from the tropics. American Journal of Botany, 95: 1548–1556. Gaya, E., B. Ball, A. Holguin, S. Villagra and F. Lutzoni. 2010. Revisiting the classification of Teloschistales (Ascomycota, lichen-forming fungi) and its evolution based on multiple and new phylogenetic loci. IMC9: The Biology of Fungi Programme P3: 106. [https://elsevier.conferenceservices.net/programme.asp?conferenceID=1885&action=prog_list&session=10387] Hibbett, D.S., M. Binder, J.F. Bischoff, M. Blackwell, P.F. Cannon, O.E. Eriksson, S. Huhndorf, T. James, P.M. Kirk, R. Lücking, H.T. Lumbsch, F. Lutzoni, P.B. Matheny, D.J. McLaughlin, M.J. Powell, S. Redhead, C.L. Schoch, J.W. Spatafora, J.A. Stalpers, R. Vilgalys, M.C. Aime, A. Aptroot, R. Bauer, D. Begerow, G.L. Benny, L.A. Castlebury, P.W. Crous, Y.-C. Dai, W. Gams, D.M. Geiser, G.W. Griffith, C. Gueidan, D.L. Hawksworth, G. Hestmark, K. Hosaka, R.A. Humber, K.D. Hyde, J.E. Ironside, U. Koljalg, C.P. Kurtzman, K.-H. Larsson, R. Lichtwardt, J. Longcore, J. Miadlikowska, A. Miller, J.-M. Moncalvo, S. MozleyStandridge, F. Oberwinkler, E. Parmasto, V. Reeb, J.D. Rogers, C. Roux, L. Ryvarden, J.P. Sampaio, A. Schüßler, J. Sugiyama, R.G. Thorn, L. Tibell, W.A. Untereiner, C. Walker, Z. Wang, A. Weir, M. Weiss, M. M. White, K. Winka, Y.-J. Yao and N. Zhang. 2007. A higher-level phylogenetic classification of the Fungi. Mycological Research, 111: 509–547. Hodkinson, B.P. and J.C. Lendemer. 2011. The orders of Ostropomycetidae (Lecanoromycetes, Ascomycota): Recognition of Sarrameanales and Trapeliales with a request to retain Pertusariales over Agyriales. Phytologia, 93(3): 407–412. Lawrey, J.D. and P. Diederich. 2011. Lichenicolous fungi – worldwide checklist, including isolated cultures and sequences available. URL: http://www.lichenicolous.net [7/24/2011]. Lücking, R. 2008. Foliicolous lichenized fungi. Flora Neotropica, 103: 1–867. Lücking, R., B.L. Stuart and H.T. Lumbsch. 2004. Phylogenetic relationships of Gomphillaceae (Ascomycota): evidence from a combined Bayesian analysis of nuclear and mitochondrial sequences. Mycologia, 96: 283– 294. Lumbsch. H.T. and S.M. Huhndorf. 2010. Outline of Ascomycota – 2009. Fieldiana: Life and Earth Sciences, 1: 1–60. Lumbsch, H.T., I. Schmitt, Z. Palice, E. Wiklund, S. Ekman and M. Wedin. 2004. Supraordinal phylogenetic relationships of Lecanoromycetes based on a Bayesian analysis of combined nuclear and mitochondrial sequences. Molecular Phylogenetics and Evolution, 31: 822–832. Lumbsch, H.T., D.G. Zimmermann and I. Schmitt. 2009. Phylogenetic position of ephemeral lichens in Thelocarpaceae and Vezdaeaceae (Ascomycota). Bibliotheca Lichenologica, 100: 389–398. Lumbsch, H.T., M. Eichler, and R. Cezanne. In prep. The genera Aphanopsis and Steinia represent basal lineages within Leotiomyceta. Lutzoni, F., F. Kauff, C.J. Cox, D. McLaughlin, G. Celio, B. Dentinger, M. Padamsee, D. Hibbett, T.Y. James, E. Baloch, M. Grube, V. Reeb, V. Hofstetter, C. Schoch, A.E. Arnold, J. Miadlikowska, J. Spatafora, D. Johnson, S. Hambleton, M. Crockett, R. Shoemaker, G.-H. Sung, R. Lücking, T. Lumbsch, K. O’Donnell, M. Binder, P. Diederich, D. Ertz, C. Gueidan, K. Hansen, R.C. Harris, K. Hosaka, Y.-W. Lim, B. Matheny, H. Nishida, D. Pfister, J. Rogers, A. Rossman, I. Schmitt, H. Sipman, J. Stone, J. Sugiyama, R. Yahr and R.

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Vilgalys. 2004. Assembling the fungal tree of life: Progress, classification, and evolution of subcellular traits. American Journal of Botany, 91: 1446–1480. Miadlikowska, J., F. Kauff, V. Hofstetter, E. Fraker, M. Grube, J. Hafellner, V. Reeb, B.P. Hodkinson, M. Kukwa, R. Lücking, G. Hestmark, M. Garcia Otalora, A. Rauhut, B. Büdel, C. Scheidegger, E. Timdal, S. Stenroos, I. Brodo, G. Perlmutter, D. Ertz, P. Diederich, J.C. Lendemer, P. May, C.L. Schoch, A.E. Arnold, C. Gueidan, E. Tripp, R. Yahr, C. Robertson and F. Lutzoni. 2006. New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia, 98(6): 1088–1103. Nelsen, M.P., R. Lücking, M. Grube, J.S. Mbatchou, L. Muggia, E. Rivas Plata and H.T. Lumbsch. 2009. Unravelling the phylogenetic relationships of lichenised fungi in Dothideomyceta. Studies in Mycology, 64: 135–144. Rivas Plata, E., R. Lücking and H.T. Lumbsch. 2012. A new classification for the family Graphidaceae (Ascomycota: Lecanoromycetes: Ostropales). Fungal Diversity, 52: 107–121. Schmitt, I., J.D. Fankhauser, K. Sweeney, T. Spribille, K. Kalb and H.T. Lumbsch. 2010. Gyalectoid Pertusaria species form a sister-clade to Coccotrema (Ostropomycetidae, Ascomycota) and comprise the new lichen genus Gyalectaria. Mycology, 1(1): 75–83. Schmull, M., J. Miadlikowska, M. Pelzer, E. Stocker-Wörgötter, V. Hofstetter, E. Fraker, B. P. Hodkinson, V. Reeb, M. Kukwa, H. T. Lumbsch, F. Kauff, and F. Lutzoni. 2011. Phylogenetic affiliations of members of the heterogeneous lichen-forming genus Lecidea sensu Zahlbruckner (Lecanoromycetes, Ascomycota). Mycologia 103(5): 983-1003. Schoch, C.L., G.-H. Sung, F. López-Giráldez, J.P. Townsend, J. Miadlikowska, V. Hofstetter, B. Robbertse, P.B. Matheny, F. Kauff, Z. Wang, C. Gueidan, R.M. Andrie, K. Trippe, L.M. Ciufetti, A. Wynns, E. Fraker, B.P. Hodkinson, G. Bonito, R. Yahr, J.Z. Groenewald, M. Arzanlou, G.S. de Hoog, P.W. Crous, D. Hewitt, D.H. Pfister, K. Peterson, M. Gryzenhout, M.J. Wingfield, A. Aptroot, S.-O. Suh, M. Blackwell, D.M. Hillis, G. W. Griffith, L.A. Castlebury, A.Y. Rossman, H.T. Lumbsch, R. Lücking, B. Büdel, A. Rauhut, P. Diederich, D. Ertz, D.M. Geiser, K. Hosaka, P. Inderbitzin, J. Kohlmeyer, B. Volkmann-Kohlmeyer, L. Mostert, K. O’Donnell, H. Sipman, J.D. Rogers, R.A. Shoemaker, J. Sugiyama, R.C. Summerbell, W. Untereiner, P. Johnston, S. Stenroos, A. Zuccaro, P. Dyer, P. Crittenden, M.S. Cole, K. Hansen, J.M. Trappe, F. Lutzoni and J.W. Spatafora. 2009. The Ascomycota Tree of Life: A Phylum Wide Phylogeny Clarifies the Origin and Evolution of Fundamental Reproductive and Ecological Traits. Systematic Biology, 58(2): 224–239. Smith, C.W., A. Aptroot, B.J. Coppins, A. Fletcher, O.L. Gilbert, P.W. James and P.A. Wolseley (eds.). 2009. The Lichens of Great Britain and Ireland. London: The British Lichen Society, 1046 pp. Wedin, M., P.M. Jørgensen and E. Wiklund. 2007. Massalongiaceae fam. nov., an overlooked monophyletic group among the cyanobacterial lichens (Peltigerales, Lecanoromycetes, Ascomycota). The Lichenologist, 39(1): 61–67. Wedin, M., P.M. Jørgensen and S. Ekman. 2011. Vahliellaceae, a new family of cyanobacterial lichens (Peltigerales, Ascomycetes). The Lichenologist, 43(1): 67–72.

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