Research Paper

Diversity of fungi on Taiwanese fern plants: review and new discoveries

Roland Kirschner, Pei Hsuan Lee, Yao-Moan Huang

Published on: 06 May 2019

Page: 163 - 175

DOI: 10.6165/tai.2019.64.163

  • BibTeX
    •
  • EndNote
    •
  • RIS
    •

    Abstract

    In this review, chances and challenges of investigating fungi on ferns in Taiwan are presented and discussed. Taiwan with a high species number of more than 800 fern species (including lycophytes here) as well as high density of fern plants is an ideal environment for studying the scarcely known fungi that depend as saprotrophs, symbionts and parasites on ferns. In Taiwan only ca. 60 fungi have been recorded on ferns. If we apply the overall estimated average plant-fungus species ratio of ca. five fungi per plant species in a given area, about 90% of fern-associated fungi have not yet been identified in Taiwan. Ca. 30% of fern-associated fungi recorded in Taiwan are rust fungi (Pucciniales, Basidiomycota) and further ca. 10% ascomycetes (Mycosphaerellales), all comprising highly specialized plant parasites. About 3.5% are species of discomycetes (Helotiales, Ascomycota) with most of them being more or less specific saprobic decomposers of dead fern tissues. The illegitimate name Pseudocercospora christellae Haldar & J.B. Ray for a parasitic fungus from India is replaced by the new name Ps. cyclosori. The new name Asterocalycella is proposed for the illegitimate genus Asterocalyx (Helotiales, Ascomycota). A new white mutant of A. mirabilis saprobic on Cyatheaceae is recorded. DNA sequence analysis suggests excluding this genus from the Sclerotiniaceae. Specimens of further Helotiales (Lachnum oncospermatum, Lachnum sp. and Microscypha sp.) from the same decaying leaf are presented as examples for the specific diversity and its incomplete taxonomic knowledge. The new species Teratosperma dicranopteridis found on living Dicranopteris linearis illustrates the difficulty to assign higher taxonomic ranks and specific ecological roles to some fungi.

    Keyword: Ascomycota, Basidiomycota, Biodiversity, Discomycetes, Ferns, Fungi, Taiwan, Teratosperma dicranopteridis

    Literature Cited

    Aptroot, A. 2006. Mycosphaerella and its anamorphs: 2. Conspectus of Mycosphaerella. CBS, Utrecht, The Netherlands.

    Aptroot, A. and L.B. Sparrius. 2003. New microlichens from Taiwan. Fungal Divers. 14(1): 1-50.
    DOI: 10.1007/s13225-010-0054-0View Article Google Scholar

    Bauer, R., D. Begerow, J.P. Sampaio, M. Weiss and F. Oberwinkler. 2006. The simple-septate basidiomycetes: a synopsis. Mycol. Prog. 5(1): 41-66.
    DOI: 10.1007/s11557-006-0502-0View Article Google Scholar

    Braun, U. 2004. Periconiella species occurring on ferns. Feddes Repert. 115(12): 50-55.
    DOI: 10.1002/fedr.200311025View Article Google Scholar

    Braun, U., C. Nakashima and P.W. Crous. 2013. Cercosporoid fungi (Mycosphaerellaceae) 1. Species on other fungi, Pteridophyta and Gymnospermae. IMA Fungus 4(2): 265-345.
    DOI: 10.5598/imafungus.2013.04.02.12View Article Google Scholar

    Bub?k, F. 1916. Systematische Untersuchungen einiger Farne bewohnenden Pilze. Berichte der Deutschen Botanischen Gesellschaft 34: 295-332, plates 7-8.

    Casta?eda Ruiz, R.F. and G. Heredia. 2000. Two new dematiaceous hyphomycetes on Cyathea from Mexico. Cryptogamie, Mycologie 21(4): 221-228.
    DOI: 10.1016/S0181-1584(00)01047-2View Article Google Scholar

    Chen, R.-S., C.-C. Huang, J.-C. Li and J.-G. Tsay. 2008. First report of Simplicillium lanosoniveum causing brown spot on Salvinia auriculata and S. molesta in Taiwan. Pl. Dis. 92(11): 1589.
    DOI: 10.1094/PDIS-92-11-1589CView Article Google Scholar

    Corner, E.J.H. 1950. A Monograph of Clavaria and Allied Genera. Annals of Botany Memoirs. 1. Cambridge, UK: Cambridge University Press.

    Christenhusz, M.J.M., X.-C. Zhang and H. Schneider. 2011. A linear sequence of extant families and genera of lycophytes and ferns. Phytotaxa 19(1): 7-54.
    DOI: 10.11646/phytotaxa.19.1.2View Article Google Scholar

    Dumont, K.P. and S.E. Carpenter. 1978. Sclerotiniaceae XIV. Asterocalyx. Mycologia 70(1): 68-75.
    DOI: 10.2307/3758688View Article Google Scholar

    Ellis, M.B. 1957. Some species of Teratosperma. Mycol. Papers 69: 1-7.

    Farr, D.F. and A.Y. Rossman. 2017. Fungal Databases, U.S. National Fungus Collections, ARS, USDA. Retrieved November, 2017, from https://nt.ars-grin.gov/fungaldatabases/

    Frey, W., E. Fischer and M. Stech. 2009. Bryophytes and Seedless Vascular Plants. In: Frey, W. (ed.) Syllabus of Plant Families - A. Engler's Syllabus der Pflanzenfamilien. 13th ed. Vol. 3, Borntraeger, Berlin/Stuttgart, Germany.

    Fries, E.M. 1823. Systema Mycologicum II(2): 275-620.

    Fu, C.H., H.-M. Hsieh, C.-Y. Chen, T.-T. Chang, Y.-M. Huang and Y.-M. Ju. 2013. Ophiodiaporthe cyatheae gen. et sp. nov., a diaporthalean pathogen causing a devastating wilt disease of Cyathea lepifera in Taiwan. Mycologia 105(4): 861-872.
    DOI: 10.3852/12-346View Article Google Scholar

    Gilbertson, R.L. and D.E. Hemmes. 1997: Notes on fungi on Hawaiian tree ferns. Mycotaxon 62: 465-187.

    Guatimosim, E., P.B. Schwartsburd, R.W. Barreto and P.W. Crous. 2016a. Novel fungi from an ancient niche: cercosporoid and related sexual morphs on ferns. Persoonia 37(1): 106-141.
    DOI: 10.3767/003158516X690934View Article Google Scholar

    Guatimosim, E., P.B. Schwartsburd, P.W. Crous and R.W. Barreto. 2016b. Novel fungi from an ancient niche: lachnoid and chalara-like fungi on ferns. Mycological. Prog. 15(12): 1239-1267.
    DOI: 10.1007/s11557-016-1232-6View Article Google Scholar

    Guu, J.-R., Y.-M. Ju and H.-J. Hsieh. 2010. Bionectriaceous fungi collected from forests in Taiwan. Bot. Stud. 51: 61-74.

    Han, J.G., T. Hosoya, G.H. Sung and H.D. Shin. 2014. Phylogenetic reassessment of Hyaloscyphaceae sensu lato (Helotiales, Leotiomycetes) based on multigene analyses. Fungal Biology 118(2): 150-167.
    DOI: 10.1016/j.funbio.2013.11.004View Article Google Scholar

    Hawksworth, D.L. 1979. The lichenicolous Hyphomycetes. Bull. Brit. Mus. Nat. Hist. 6(3): 183-300.

    Hawksworth, D.L. 2001. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol. Res. 105(12): 1422-1432.
    DOI: 10.1017/S0953756201004725View Article Google Scholar

    Hawksworth, D.L. and R. L?cking. 2017. Chapter 4: Fungal Diversity Revisited: 2.2 to 3.8 Million Species. In J. Heitman, B.J. Howlett, Pedro.W. Crous, E.H. Stukenbrock, T.Y. James, N.A. R. Gow eds. The Fungal Kingdom. 79-95pp. American Society for Microbiology, USA.

    Hjortstam, K. and K.H. Larsson. 1997. Corticioid fungi growing on ferns in northern Europe. Windahlia 22: 49-55. H?hnel, F. von 1912. Fragmente zur Mykologie (XIV. Mitteilung, Nr. 719-792). Sber. Akad. Wiss. Wien, Math.-naturw. Kl., Abt. 1, 121: 339-423 + 2 plates.

    Holm, M. and K. Holm. 1978. Some pteridicolous Ascomycetes. Bot. Notiser 131: 97-115.

    Hsieh, W.H. and T.K. Goh. 1990. Cercospora and similar fungi from Taiwan. Maw Chang Book Company, Taipei, Taiwan.

    Hsu, S.T., T.T. Chang, C.C. Chang, J.L. Tsai and T.T. Tsay. 2002. List of Plant Diseases in Taiwan 4th ed. Taiwan Phytopathological Society, Taiwan.

    Huang, T.C. eds. (1993–2003) Flora of Taiwan. Vols. 1–6, 2nd ed., Department of Botany, National Taiwan University, Taipei, Taiwan.

    Hughes, S.J. 1951. Studies on micro-fungi. XIII. Beltrania, Ceratocladium, Diplorhinotrichum, and Hansfordiella (gen. nov.). Mycol. Papers 47: 1-15.

    Iwatsuki, K. 1992. Ferns and Fern Allies of Japan. Heibonsha, Tokyo, Japan.

    Kirk, P.M. 1985. New or interesting microfungi XIV. Dematiaceous hyphomycetes from Mt Kenya. Mycotaxon 23: 305-352.

    Kirschner, R. and C.-J. Chen. 2007. Foliicolous hyphomycetes from Taiwan. Fungal Divers. 26: 219-239.

    Kirschner, R. and C.-J. Chen. 2010. Periconiella species (anamorphic Mycosphaerellaceae) from Taiwan. Fungal Divers. 44(1): 135-148.
    DOI: 10.1007/s13225-010-0054-0View Article Google Scholar

    Kirschner, R. and L.-C. Liu. 2014. Mycosphaerellaceous fungi and new species of Venustosynnema and Zasmidium on ferns and fern allies in Taiwan. Phytotaxa 176(1): 309-323.
    DOI: 10.11646/phytotaxa.176.1.29View Article Google Scholar

    Kirschner, R. and H. Wang. 2015. New species and records of mycosphaerellaceous fungi from living fern leaves in East Asia. Mycol. Progr. 14(8): 65.
    DOI: 10.1007/s11557-015-1085-4View Article Google Scholar

    Knapp, R. 2011. Ferns and fern allies of Taiwan. KBCC Press, Taipei, Taiwan.

    Knapp, R. 2014 Index to Ferns and Fern Allies of Taiwan. KBCC Press, Gaoshu Township, Pingtung County, Taiwan.

    Knapp, R. and T.-C. Hsu. 2017. Ferns and Fern Allies of Taiwan – Second supplement. KBCC Press, Gaoshu Township, Pingtung County, Taiwan.

    Koukol, O. and D. R?hov?. 2013. Pentaster cepaeophilus gen. et sp. nov. described from surface of empty shells of Cepaea hortensis. Nova Hedwigia 96(3): 495-500.
    DOI: 10.1127/0029-5035/2013/0086View Article Google Scholar

    Kramer, K.U. and P.S. Green. 1990. The families and genera of vascular plants, vol. 1, Pteridophytes and gymnosperms. Berlin: Springer.

    Kumar S., G. Stecher and K. Tamura. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33(7): 1870-1874.
    DOI: 10.1093/molbev/msw054View Article Google Scholar

    Langer, E. 1994. Die Gattung Hyphodontia John Eriksson. Bibliotheca Mycologica 154: 1-298.

    Lindsay, S. and D.J. Middleton. 2009. Development of a multi-access key to the ferns of Thailand. Thai. For. Bull. Bot., Special Issue: 134-137.

    Liou, S.C. and Z.C. Chen. 1977. Notes on Taiwan discomycetes I. (Pezizales and Helotiales). Taiwania 22(1): 29-43.
    DOI: 10.6165/tai.1977.22.29View Article Google Scholar

    Matsushima, T. 1980. Matsushima Mycological Memoirs No. 1. Saprophytic Microfungi from Taiwan, Part 1. Hyphomycetes. Matsushima Fungus Collect., Kobe, Japan.

    Matsushima, T. 1987. Matsushima Mycological Memoirs No. 5. Matsushima Fungus Collect., Kobe, Japan.

    Medel, R. and F. Lorea-Hern?ndez. 2008. Hyaloscyphaceae (Ascomycota) growing on tree ferns in Mexico. Mycotaxon 106: 209-217.

    Mehltreter, K. 2010. Interactions of ferns with fungi and animals. In: Mehltreter, K., Walker, L.R. & Sharpe, J.M. (eds.) Fern Ecology. Cambridge University Press, Cambridge, UK, pp. 220-254.

    Miersch, J. and H. Lehmann. 2015. Mycena alboaculeata, eine neue Helmlingsart mit stacheligem Hut aus Deutschland. Z. Mykol. 81: 337-346.

    Oberwinkler, F. 2012. Evolutionary trends in Basidiomycota. Stapfia 96: 45-104.

    Olariaga, I., X. Laskibar and J. Holec. 2015. Molecular data reveal cryptic speciation within Tricholomopsis rutilans: description of T. pteridicola sp. nov. associated with Pteridium aquilinum. Mycol. Prog. 14(4): 21.
    DOI: 10.1007/s11557-015-1040-4View Article Google Scholar

    Petrini, O., P.J. Fisher and L.E. Petrini. 1992. Fungal endophytes of bracken (Pteridium aquilinum), with some reflections on their use in biological control. Sydowia 44: 282-293.

    Phengsintham, P., E. Chukeatirote, E.H.C. McKenzie, M.A. Moslem, K.D. Hyde and U. Braun. 2010. Two new species and a new record of cercosporoids from Thailand. Mycosphere 1(3): 205-212. PPG1. 2016. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 54(6): 563-603.
    DOI: 10.1111/jse.12229View Article Google Scholar

    Pressel, S., M.I. Bidartondo, K.J. Field, W.R. Rimington and J.G. Duckett. 2016. Pteridophyte fungal associations: Current knowledge and future perspectives. J. Syst. Evol. 54(6): 666-678.
    DOI: 10.1111/jse.12227View Article Google Scholar

    Razikin, M.Z.M. 2016. Distribution of Lachnum, pteridocolous fungi on Cyathea in peninsular Malaysia. MSc thesis, Universiti Sains Malaysia.

    Razikin, M.Z.M., H. Nagao and R. Zakaria. 2014. First report of pteridocolous discomycetes, Lachnum lanariceps and L. oncospermatum, on decayed tree fern in Bukit Bendera (Penang Hill), Pulau Pinang, Malaysia. Songklanakarin J. Sci. Technol. 36(4): 407-410.

    Rothfels, C.J., M.A. Sundue, L.Y. Kuo, A. Larsson, M. Kato, E. Schuettpelz and K.M. Pryer. 2012. A revised family-level classification for eupolypod II ferns (Polypodiidae: Polypodiales). Taxon 61: 515-533.

    Sawada, K. 1919. Descriptive catalogue of the Formosan fungi I. Rep. Dept. Agric. Gov. Res. Inst. Formosa 19: 1-695.
    DOI: 10.5962/bhl.title.3911View Article

    Sawada, K. 1944. Descriptive catalogue of the Formosan fungi. Part X. Rep. Dept. Agric. Gov. Res. Inst. Formosa 87: 1-96.

    Sawada, K. 1959. Descriptive catalogue of Taiwan (Formosan) fungi. XI. Special Publ. Coll. Agric. Natl. Taiwan Univ. 8: 1-268.

    Sjamsuridzal, W., H. Nishida, H. Ogawa, M. Kakishima and J. Sugiyama. 1999. Phylogenetic positions of rust fungi parasitic on ferns: evidence from 18S rDNA sequence analysis. Mycoscience 40(1): 21-27.
    DOI: 10.1007/BF02465669View Article Google Scholar

    Smith, AR., K.M. Pryer, E. Schuettpelz, P. Korall, H. Schneider and P.G. Wolf. 2006. A classification for extant ferns. Taxon 55(3): 705-731.
    DOI: 10.2307/25065646View Article Google Scholar

    Stevenson, J.A. 1945. Ferns and fungi. American Fern Journal 35(4): 97-104.
    DOI: 10.2307/1545645View Article Google Scholar

    Sydow, H. 1909. Micromycetes japonici. Ann. Mycol. 7(2): 168-175.

    Uecker, F.A., W.A. Ayers and P.B. Adams. 1980. Teratosperma oligocladum, a new hyphomycetous mycoparasite on sclerotia of Sclerotinia sclerotiorum, S. trifoliorum, and S. minor. Mycotaxon 10(2): 421-427.

    Wu, M.L. 1998. Some Orbilia species new to Taiwan. Fung. Sci. 13(1-2): 17-22.
    DOI: 10.7099/FS.199808.0017View Article Google Scholar

    Wu, M.L. 2002. A new record of pteridicolous Sclerotiniaceae from Taiwan. Fung. Sci. 17: 49-54.

    Wu, M.L., J.H. Haines and Y.Z. Wang. 1998. New species and records of Lachnum from Taiwan. Mycotaxon 67: 341-354.

    Wu, W. and W. Zhuang. 2005. Sporidesmium, Endophragmiella and related genera from China. Fungal Diversity Research Series 15, Fungal Diversity Press, Hong Kong.

    Xia, J.-W., Y.-R. Ma, J.-M. Gao, X.-G. Zhang and Z. Li. 2016. A new species of Blastophragma and three new records of other dematiaceous hyphomycetes from southern China. Nova Hedwigia 102(1): 223-232.
    DOI: 10.1127/nova_hedwigia/2015/0301View Article Google Scholar

    Ye, W., Z.-W. Li, B.C. Tan, Y. Chang, L.-Z. Chen, J.-Y. He and C.-D. Liu. 2007. Study on the biodiversity of ferns from southern to northern Wuyi Moutains. Journal of Xiamen University (Natural Science) 46: 431-437 (in Chinese).

    Yurchenko, E., H.-X. Xiong and S.-H. Wu. 2013. Four new species of Hyphodontia (Xylodon ss. Hjortstam & Ryvarden, Basidiomycota) from Taiwan. Nova Hedwigia 96(3–4): 545-558.
    DOI: 10.1127/0029-5035/2013/0092View Article Google Scholar