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Re-Examination of the Symphyodon Perrottetii (Symphyodontaceae) and Related Species in East and Southeast Asia

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Re-Examination of the Symphyodon Perrottetii (Symphyodontaceae) and Related Species in East and Southeast Asia Hattoria 12: 51–92. 2021 Re-examination of the Symphyodon perrottetii (Symphyodontaceae) and related species in East and Southeast Asia Hiroyuki AKIYAMA1, 2, Rimi REPIN3 & Monica SULEIMAN4 1 Museum of Nature and Human Activities, Hyogo, Yayoigaoka-6, Sanda, Hyogo 669–1546, Japan 2 Institute of Environmental Sciences, University of Hyogo, Yayoigaoka-6, Sanda, Hyogo 669–1546, Japan 3 Research and Education Division, Sabah Parks, 88806 Kota Kinabalu, Sabah, Malaysia 4 Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Jalan UMS, 88400 Kota Kinabalu, Sabah, Malaysia Author for correspondence: Hiroyuki AKIYAMA, [email protected] Abstract Re-examination of morphological features and newly executed molecular analysis based on chloroplast (rbcL, rps4, and trnL-F) and nuclear (ITS1&2) genomes revealed unexpected diversity in Symphyodon perrottetii Mont. s. l. (Symphyodontaceae) in East and Southeast Asia. Japanese plants previously recognized as S. perrottetii are shown to include at least five different species: S. asper (Mitt.) A.Jaeger, S. copelandii Broth., S. gollanioides Nog., S. recurvomarginatus (Dixon & Sakurai) H.Akiyama, comb. nov. and S. rheophilus H.Akiyama, sp. nov. In addition, previous Japanese record of S. echinatus (Mitt.) A.Jaeger is actually S. asper. Symphyodon longispinosus H.Akiyama, sp. nov. from southwestern China is newly described. Subsequently, S. perrottetii s. str. is excluded from China and Japan and has its revised distribution range from southwest India (type locality of S. perrottetii), Sri Lanka, central Thailand, and Singapore. Symphyodon merrillii Broth., once regarded as a synonym of S. perrottetii, is again recognized as a distinct species with its distribution in Malesia and Indochina. Symphyodon ovalifolius H.Akiyama & M.Suleiman, sp. nov. is described and classified under the subgenus Parasymphyodon H.Akiyama & M.Suleiman, subg. nov. Rheoshevockia fontana Ignatov, W.Z.Ma & D.G.Long is again demonstrated to have a unique systematic position sister to the genus Symphyodon. Introduction The bryophyte genus Symphyodon Mont. was established by Montagne (1841) with a single species, S. perrottetii Mont. from Neel-Gherries (＝Nilgiri Hills), southwestern India. The most important traits of S. perrottetii are cylindrical, erect, often distinctly echinate capsules, and reduced endostome. Müller (1850–1851) placed Symphyodon perrottetii under the genus Neckera allied with 51 N. angusta Müll.Hal., a species from Bombay, South India. Mitten (1859) treated Symphyodon as a section of the genus Stereodon (Brid.) Brid., and recombined the above two species and recognized a total of eight species in the section (including five new species based on specimens from Nepal, Khasia and Sikkim). Among them, S. planulus Mitt. was later designated as a member of the genus Aptychella (Broth.) Herzog (formerly as Clastobryopsis M.Fleisch.) as A. planula (Mitt.) M.Fleisch. Jaeger & Sauerbeck (1878) recognized the genus Symphyodon with eight species, mainly following Mitten’s (1859) sectional treatment of Symphyodon. Since then, the number of species in the genus has increased as results of several regional studies (Noguchi 1972; Tixier 1972; Gangulee 1976; Steere 1982; Buck & Ireland 1992; He & Snider 1992, 2000; Churchill 1994; Akiyama 2017a; He & Khang 2012). In a taxonomical revision of Symphyodon, He & Snider (2000) reduced the number of species from 27 known at that time to 15. This is currently considered to be the most reliable literature. After He & Snider’s (1992, 2000) revision, two additional species have been published: Symphyodon leiocarpus H.Akiyama & H.Tsubota (Akiyama & Tsubota 2009) from northern Thailand and S. chrysobasilaris (Broth.) W.Kim & H.Akiyama (Kim et al. 2020) from Hawaii. Thus, a total of 17 species are now recognized for the genus. However, Symphyodon is still one of the most difficult moss groups to define species delimitations because of little morphological difference among the species. The characters that are considered to be important in species identification are highly variable depending on growth conditions, and developmental stages, such as plant sizes, branching patterns, leaf shapes, and degree of laminal cell proration. Along with the genera Chaetomitriopsis M.Fleisch., Chaetomitrium Dozy & Molk., Dimorphocladon Dixon, Phyllodon Schimp., and Rheoshevockia Ignatov, W.Z.Ma & D.G.Long, Symphyodon has usually placed in the Symphyodontaceae M.Fleisch. (Goffinet et al. 2008; Ma et al. 2018; Kim et al. 2020). These genera are commonly characterized by a short, bifid costae, limited alar regions composed of small, quadrate to short-rectangular cells, and more or less prorate (rarely smooth) laminal cells. In nearly all of the genera in the family, morphological differentiation between stem leaves and branch leaves is highly correlated to branching patterns. The species with bi-pinnately to tri-pinnately branching patterns tend to have highly differentiated stem and branch leaves; in contrast, the species with irregularly and sparsely branching patterns have less differentiated leaves. In addition, some members of the Symphyodontaceae (Chaetomitrium and Symphyodon) are characterized by strong spiny protuberances or spines on the capsule walls and/or the upper part of the setae. Most of the species are epiphytes in slightly moist warm temperate to subtropical forests, but some are rheophytes in such genera as Phyllodon and Rheoshevockia. Sporophytes have not been found in Rheoshevockia, and morphology of capsules is remained ambiguous. Nevertheless, the latter genus is thought to be most closely related to Symphyodon (Ma et al. 2018). As mentioned above, 18 species of Symphyodon are now recognized in the world. Except for S. imbricatifolius, which is known only in Central and northern South America and S. pygmaeus (Broth.) S.He & Snider, a pan-tropical species known from eastern Africa to Southeast Asia and Hawaii, most species of the genus are limited to East and Southeast Asia and the Himalayas in their distribution (He & Snider 2000). According to He & Snider (2000) and other reports, S. perrottetii is the most widely distributed species in the genus, ranging 52 from Sri Lanka, southwestern India, southwestern China, Laos, Thailand, Vietnam, Indonesia, Malaysia, Singapore, Philippines, Taiwan and Japan. The northern limit of its species distribution is the central part of Honshu, Japan, where snow falls in winter (Kiguchi et al. 2006b); while the southern limit is extended to New Guinea (He & Snider 2000). Higuchi (2014) reported the species from the Hawaii Islands (Hawaii Island), but recently this record was revealed to S. chrysobasilatus, a species endemic to the Hawaii Islands (Kim et al. 2020). Symphyodon perrottetii is characterized by sparsely branched secondary stems, which grow slightly to be erect or long-pendulous from the substrate, weak differentiation between stem and branch leaves, acute leaf apices, serrate upper leaf margins, short and double costae usually reaching less than 1/2 of the leaf length, and weakly prorate laminal cells at the upper cell ends (sometimes smooth). In general, a distinct transverse undulation of the upper lamina is a good feature to identify it in the field. However, this species shows a great diversity in morphological features, which may explain why it has been commonly reported in wide distribution ranges. Indeed, it is often difficult to know the species identity solely based on their morphology. Among the species of Symphyodon, it has known that there is remarkable variation in plant sizes, branching patterns, leaf shapes and lengths, extent of serration at upper leaf margins, and costal lengths. The habit variation is also obvious, with some pendulous from tree trunks and others shortly spread horizontally. The degree of proration of laminal cells is also quite variable too, ranging from indistinct to conspicuous, sometimes accompanying some spines. The spines of the capsule walls likewise vary from smooth to strongly echinate with spines reaching 200 µm in length. With the recent development of applying molecular phylogenetic analyses, many studies have shown that some species previously treated as a single species are actually multi-species complex (Heinrichs et al. 2010; Akiyama 2019; Bakalin et al. 2020). In this study, we have re-examined the Asian Symphyodon species, particularly paying attention to S. perrottetii because of its variation and wide distributional range as described above. Morphological variations and molecular features are analyzed using living samples collected from field work in Japan, Taiwan, China, Vietnam, Thailand, Malaysia, Indonesia and the Philippines, as well as using herbarium material on loan. The results show that the commonly recognized S. perrottetii in the region consists multiple species, including several monophyletic clades, and that each of these clades is well defined morphologically. Furthermore, the phylogenetic position of the genus Rheoshevockia, which is considered to be closely related to Symphyodon, was also analyzed. Materials and Methods Taxon sampling We analyzed samples identified as Symphyodon perrottetii based on morphological characteristics, as well as other species of the genus. The morphological characteristics of S. perrottetii include ovate-lanceolate leaves with a more or less undulate upper lamina, acute apices with serration in the upper lamina, double costae, and weak proration of laminal cells. We analyzed as many samples as possible, especially from Japan to know
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