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Taxonomic Studies of the Trichocoleaceae in Southeast Asia

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Taxonomic Studies of the Trichocoleaceae in Southeast Asia Hattoria 4: 1－42, 2013 Taxonomic studies of the Trichocoleaceae in Southeast Asia. III. The genus Trichocolea Dumort. Tomoyuki Katagiri1, Atsushi Sadamitsu1, Hiroshi Miyauchi1 Hiromi Tsubota2 and Hironori Deguchi1 1Department of Biological Science, Graduate School of Science, 1–3–1, Kagamiyama, Higashi-hiroshima-shi, Hiroshima-ken, 739–8526, Japan 2Miyajima Natural Botanical Garden, Graduate School of Science, Hiroshima University, Mitsumaruko-yama, 1156–2, Miyajima-cho, Hatsukaichi-shi, Hiroshima-ken, 739–0543, Japan Abstract. Seven species, including two new species, of the genus Trichocolea Dumort.: T. iriomotensis T.Katag., T. japonica T.Katag., T. magna T.Katag., T. mollissima (Hook.f. & Taylor) Gottsche, T. pluma (Reinw., Blume & Nees) Mont., T. rudimentaris Steph., and T. tomentella (Ehrh.) Dumort., are recognized for Southeast Asia, including the New Guinea Islands. Distribution data, habitat, taxonomic notes, distinguishing characters of the species, and a key to the species of the genus Trichocolea are provided. Three new synonyms of Trichocolea pluma: Jungermannia tomentella var. javanica Reinw., Blume & Nees, T. samoana Steph., T. tonkinensis Steph., one new synonym of Trichocolea tomentella: T. tomentella f. nodulosa Nees, and one new synonym of Trichocolea rudimentaris: T. fragillima Herzog are proposed. Lectotypes are selected for T. australis Steph. (= T. mollissima), T. striolata Steph. (= T. pluma), T. levifolia Steph. (= T. pluma), and T. rudimentaris Steph. Phylogenetic analyses based on rbcL gene sequences revealed monophyly of Trichocoleaceae in which two clades Eotrichocolea–Leimotra clade and Trichocolea clade were resolved. It is suggested that epicoelocaules, as observed in Trichcocolea and Eotrichocolea, are independently derived from perianth-bearing shoots. Introduction Tournefort (1700, p. 556) originally named a plant, now called Trichocolea tomentella, as “Muscus palustris absinthii folio insipidus” in his Institutiones Rei Herbariae, which is the oldest publication of the species. Vaillant (1727, p. 140) followed Tournefort and used a shorter form “Muscus palustris absinthii folio”. Linnaeus (1753, p. 1134), in his Species Plantarum which is the starting point of the scientific binary nomenclature, listed the Vaillant’s prelinnean phrase name under Jungermannia ciliaris L. (≡ Ptilidium ciliare (L.) Hampe). Ehrhart (1783) recognized a heterogeneous element among the plants so far understood as J. cilialis, and named it Jungermannia tomentella Ehrh. (≡ T. tomentella). 1 The genus Trichocolea Dumort. [type: T. tomentella (Ehrh.) Dumort.] was proposed by Dumortier (1822) to accommodate the two species: T. tomentella (Ehrh.) Dumort. and T. tomentosa (Sw.) Gottsche , although the generic name was initially given under the spelling of “Thricholea”. Reinwardt et al. (1824) studied Javanese liverworts and proposed a variety of Jungermannia tomentella: var. javanica Reinw., Blume & Nees and a new species Jungermannia pluma Reinw., Blume & Nees without recognition of the genus Trichocolea. Nees von Esenbeck (1838) accepted the genus Trichocolea and recognized two species: T. tomentella with six forms, f. tomentella, f. tomentosa (Sw.) Nees, f. javanica (Reinw., Blume & Nees) Nees, f. pluma (Reinw., Blume & Nees) Nees, f. subsimplex (Nees) Nees, and f. nodulosa Nees, and T. lanata (Hook.) Nees. Gottsche et al. (1845), in his Synopsis Hepaticarum which summarised previous works on liverworts worldwide, recognised three species: T. tomentella with six varieties corresponding to the forms mentioned above, T. lanata, and T. polyacantha (Hook.f. & Taylor) Gottsche, Lindenb. & Nees. Gottsche (1864) recognized two sections under the genus Trichocolea: sect. Hirtiflora (≡ sect. Trichocolea) and sect. Laeviflora. Three species: T. tomentella, T. mollissima (Hook.f. & Taylor) Gottsche, and T. lanata were assigned to the section Hirtiflora and T. tomentosa to the section Laeviflora which corresponds to the genus Leiomitra Lindb. [type: L. tomentosa (Sw.) Lindb.] (Lindberg 1875). The genus Eotrichocolea R.M.Schust. [type: E. polyacantha (Hook.f. & Taylor) R.M.Schust.] was segregated from Trichocolea by Schuster (1963), so three distinct genera: Trichocolea, Leiomitra, and Eotrichocolea were recognized for the former Trichocolea s. lat. The monotypic genus Castanoclobos J.J.Engel & Glenny [type: C. julaceus (Hatcher ex J.J.Engel) J.J.Engel & Glenny] from New Zealand was added by Engel & Glenny (2007) to the family Trichocoleaceae Nakai, but Katagiri & Deguchi (2012) placed it in the Pseudolepicoleaceae Fulford & J.Taylor and considered the Trichocoleaceae to comprise only three genera: Eotrichocolea, Leiomitra, and Trichocolea. The genus Trichocolea can be distinguished from the other genera by (1) regularly 1–3-pinnate habit, (2) obliquely to subtransversely inserted leaves, (3) succubous leaf insertion, (4) stem cortex of 1–5 layers of thick-walled cells, (5) epicoelocaule lacking perianth, (6) and ellipsoidal capsule dehiscing into four regular valves. In Southeast Asia, taxonomic revision of the family Trichocoleaceae has remained inadequate since Stephani (1909, 1923) who reported eleven species of Trichocolea s. lat. including eight new species. Sixteen species with two varieties have been so far reported from the area by the following studies (Reinwardt et al. 1824; Nees von Esenbeck 1830; Lindberg 1875; Stephani 1908, 1909, 1923; Herzog 1931, Horikawa 1934; Inoue 1979; Katagiri et al. 2011). The majority of these species, however, remain poorly studied. The current data on the species number of the regions investigated do not seem to reflect the actual distribution of the species. This may be due to different standards for identification and taxonomic treatment of little-known or poorly understood species. The aim of this revision is to provide the first comprehensive survey of SE Asian Trichocolea species and to determine the inter- and intra-generic relationships among the family Trichocoleaceae using molecular phylogenetic analysis. 2 Materials and Methods Taxonomic revision Approximately 1400 herbarium specimens from BISH, BORH, CBM, G, H, HIRO, HO, JE, KYO, L, M, NICH, PC, S, STR, SZG, and TNS were examined in the present study. The morphological concept of the genus Trichocolea was described and SE Aisan species are fully described and illustrated. Distribution data, habitat, taxonomic notes, distinguishing characters of the species, and a key to the species of the genus Trichocolea are provided. Species are listed alphabetically and each includes their basionym and all synonyms recognized in the present study. Deviations for each character were excluded in descriptions. Structural analyses were made by manually dissecting the plant material. The distinctive characters of representative specimens were drawn with the aid of a drawing tube. Detailed surface ornamentation of spores and elaters was investigated using scanning electron microscopy (SEM). Oil-bodies were photographed based on fresh materials for each species. Taxa excluded from Trichocoleaceae are shown at the end with due discussion. Molecular phylogenetic analysis DNA extraction, PCR amplification, and sequencing. Experimental procedures follow Tsubota et al. (2004, 2005). The design of PCR and DNA sequencing primers follows Tsubota et al. (1999, 2000, 2001) and Masuzaki et al. (2010, 2011). Taxon sampling. The phylogenetic tree was constructed based on the ribulose 1,5-bisphosphate carboxylase, large subunit (rbcL, 1428 base pairs). The data set comprised 24 OTUs based on 27 materials including nine species of Trichocoleaceae and five species for outgroups. The Japanese materials of Trichocolea japonica (AB618046 and AB751578) and European materials of T. tomentella (AB751588, AB751589, and AB751590) show identical sequences respectively, and each of them was represented as a single OTU. The outgroups were selected based on Masuzaki et al. (2010, fig. 4). The twenty OTUs among eight species were newly obtained in the present study and the other sequences were downloaded from DNA databases published in Davis (2004), He-Nygrén et al. (2004), Heslewood & Brown (2007), Glenny et al. (2009), and Cooper et al. (2011). The full species names, their GenBank accession numbers, references, and voucher specimens with their sampling localities for each species included in the present study are given in Table 1. The rbcL gene sequences were aligned manually. Phylogenetic analysis. Phylogenetic analysis using the rbcL gene sequences was performed based on maximum likelihood criteria as previously described (Tsubota et al. 2004; Ozeki et al. 2007; Masuzaki et al. 2010) with some differences as follows: Prior to the phylogenetic reconstruction, Kakusan4 (Tanabe 2011) was implemented in AICc (Sugiura 1978) to make a rational decision regarding the nucleotide-based substitution model that best fitted our data, and the approximate unbiased test (AU; Shimodaira 2002, 2004) in the final stage of the analysis scheme. Phylogenetic trees were constructed using the following six program packages to obtain the candidate topologies: (1) RAxML ver. 7.2.6 (Stamatakis 2006) with maximum likelihood (ML) method (Felsenstein 1981) using GTR + gamma model; (2) GARLI ver. 2.0 (Zwickl 2006) with ML method using GTR + gamma + proportion invariant model; (3) PAUPRat (Sikes & Lewis 2001) over PAUP ver. 4.0b10 3 (Swofford 2002) with maximum parsimony (MP) method (Fitch 1971) to implement Parsimony Ratchet searches (Nixon 1999) using the Parsimony Ratchet search strategy with
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