Gradstein & al. • Taxonomic status of Phycolepidoziaceae TAXON 63 (3) • June 2014: 498–508 On the taxonomic status of the enigmatic Phycolepidoziaceae (Marchantiophyta: Jungermanniales) with description of a new species, Phycolepidozia indica S. Robbert Gradstein,1* Benjamin Laenen,2* Jan-Peter Frahm,3† Uwe Schwarz,4 Barbara J. Crandall-Stotler,5 John J. Engel,6 Matthew von Konrat,6 Raymond E. Stotler,5† Blanka Shaw7 & A. Jonathan Shaw7 1 Museum National d’Histoire Naturelle, Department Systématique et Evolution, C.P. 39, 57 Rue Cuvier, 75231 Paris 05, France 2 Institut für Systematische Botanik, Universität Zürich, Zollikerstrasse 107, 8008 Zürich, Switzerland 3 Nees Institut für Biodiversität der Pflanzen, Universität Bonn, Meckenheimer Allee 170, 53111 Bonn, Germany 4 Prestige Grand Oak 202, 7th Main, 1st Cross, HAL IInd Stage, Indira Nagar, Bangalore 560038, India 5 Department of Plant Biology, Southern Illinois University, Carbondale, Illinois 62901-6509, U.S.A. 6 Department of Botany, The Field Museum, Chicago, Illinois 60605-2496, U.S.A. 7 Department of Biology, Duke University, Durham, North Carolina 27708, U.S.A. * contributed equally to this paper Author for correspondence: S. Robbert Gradstein, gradstein@mnhn.fr DOI http://dx.doi.org/10.12705/633.17 Abstract The monospecific Phycolepidoziaceae with the single neotropical species Phycolepidozia exigua is a highly specialized leafy liverwort without vegetative leaves. The extreme reduction of morphological and anatomical characters of Phycolepidozia has caused uncertainties as to the systematic position of the genus and family. In 2012, a second species of Phycolepidozia was detected in the Western Ghats, South India. The Indian plant differs from P. exigua in several respects and is described here as P. (subg. Metaphycolepidozia) indica Gradst., J.-P.Frahm & U.Schwarz. Differences include the massive stem of P. indica, the larger perianth with a crenate, 3-lobed mouth, and the epidermis of the capsule wall made up of non-tiered cells with nodular thickenings on both longitudinal and transverse walls. A phylogenetic analysis using four different chloroplast regions (psbA, psbT, rps4, rbcL) of P. indica and putatively related groups shows that Phycolepidozia is nested within the leafy liverwort family Cephaloziellaceae. Consequently, Phycolepidoziaceae is placed in the synonymy of Cephaloziellaceae. The discovery of P. indica adds a further example to the list of amphi-Pacific tropical disjunctions in bryophytes. Keywords amphi-Pacific tropical disjunction; Cephaloziellaceae; leafless stems; liverworts; molecular phylogeny; Phycolepidozia; taxonomy; Western Ghats Supplementary Material The alignment is available in the Supplementary Data section of the online version of this article at http://www.ingentaconnect.com/content/iapt/tax INTRODUCTION The genus Phycolepidozia R.M.Schust. (Marchantiophyta: Jungermanniales) is a unique, alga-like leafy liverwort, differing from all known liverworts by having stems and branches without leaves and underleaves but with leafy gametoecia. The genus is monospecific, containing the single species P. exigua R.M.Schust. from the Neotropics (Schuster, 1966). Schuster assigned Phycolepidozia to a separate family, Phycolepidoziaceae R.M.Schust., because its characters did not fit any other family. He considered affinities of Phycolepidozia to Cephaloziellaceae, Cephaloziaceae and Lepidoziaceae but excluded it from the latter two families because of the highly reduced seta consisting of only eight rows of cells (four rows of large epidermal cells surrounding four rows of minute inner cells). From Lepidoziaceae the genus differs further by the scattered rhizoids and elaters with tapered ends. By its seta structure Phycolepidozia is similar to Cephaloziellaceae, the reduced 4 + 4 seta being diagnostic of this family. Nevertheless, Schuster (1966) considered a close affinity of Phycolepidozia to Cephaloziellaceae “improbable” because of its very thin, leafless stems and the ciliate perianth mouth, and he suggested that the cephalozielloid seta of Phyco­ lepidozia was a homoplastic character. Phycolepidoziaceae have since been accepted as a separate family by all authors (e.g., Fulford, 1968; Crandall & al., 2009) with the exception of Gradstein & al. (2001) who united Phycolepidoziaceae with Lepidoziaceae. Its single species, Phycolepidozia exigua, was collected in 1966 by the late Dr. Rudolf M. Schuster on the island of Dominica where it was found growing on tree trunks in humid rainforest at ca. 450 m. Attempts to recollect P. exigua in the type locality, or elsewhere, have long been unsuccessful and the species has been redlisted as “Critically Endangered” (Schäfer-Verwimp, 2010; Hallingbäck, 2013). A second locality of the species (based on Received: 29 Sep 2013 | returned for revisions: 7 Nov 2013; 27 Nov 2013; 8 Feb 2014 | revisions received: 24 Nov 2014; 16 Jan 2014; 8 Feb 2014 | accepted: 8 Feb 2014 | not published online ahead of inclusion in print and online issues || © International Association for Plant Taxonomy (IAPT) 2014 498 Version of Record (identical to print version). TAXON 63 (3) • June 2014: 498–508 Gradstein & al. • Taxonomic status of Phycolepidoziaceae a 25-year-old herbarium specimen) has recently been discovered on Cerro Duida in the Guayana Highland of Venezuela (Gradstein, in press). Surprisingly, a new species of Phycolepidozia differing from P. exigua in several important respects was collected by one of us (US) in the Western Ghats, South India, in November 2012. Because of the puzzling morphology of the genus and uncertainties about the status of the family Phycolepidoziaceae, we employed DNA sequences to explore its phylogenetic relationships. Several genomic regions of leafy liverworts have recently been sequenced and have given important new insights in the intricate phylogenetic relationships within this large group of plants (see Crandall-Stotler & al., 2009, for review). In this study we have employed different chloroplast DNA loci, which are very important and straight-forward sources of information for phylogenetic inference at generic and family level in liverworts (e.g., Stech & Quandt, 2010). By sequencing four chloroplastic regions of Phycolepidozia and comparing the recovered sequences with those of putatively related groups, we assessed the relationships of this enigmatic liverwort. of Life” database (LiToL; http://biology.duke.edu/bryology/ LiToL/) and to 29 accessions from GenBank, using the program Seaview v.4.4.2 (Gouy & al., 2010). The additional accessions were chosen based on putative relationships of Phycolepidoziaceae (Schuster, 1966). Gaps were inserted when necessary to achieve character homology and scored as missing data. We used maximum likelihood (ML) and parsimony (MP) analysis for phylogenetic analysis of the data. Maximum likelihood analysis was performed using the program RAxML-HPC v.7.0.4 (Liu & al., 2011) on the Cipres data portal (Miller & al., 2009). A fifty percent majority-rule consensus tree was built based on one thousand bootstrap replicates using the GTRCAT model and the rapid bootstrapping option. Parsimony analysis was done using PAUPRat (Sikes & Lewis, 2001) on the Cipres data portal. Heuristic searches with 10,000 random taxon replicates were conducted with tree-bisection-reconnection (TBR) branch-swapping. Characters were equally weighted. We also conducted a bootstrap analysis with 100 replicates and 10 random starting points, using the TBR option. A consensus tree was built from the equally best trees retained during the heuristic search and compared to the ML consensus tree for detecting potential disagreement. MATERIALS AND METHODS Relationships of Phycolepidozia and of the family Phycolepidoziaceae were investigated using sequence data from the material of the new species from India. DNA was extracted using the DNeasy Plant Minikit (Qiagen Benelux B.V., Venlo, The Netherlands). Four chloroplast regions (psbA, psbT, rps4, rbcL) were amplified following the protocol described in Laenen & al. (2011). The four loci were concatenated and aligned to six accessions (genera) of the unpublished “Liverwort Tree RESULTS Description of the new species Phycolepidozia indica Gradst., J.-P.Frahm & U.Schwarz, sp. nov. – Holotype: INDIA. Western Ghats, Karnataka State, Coorg District, trail to the summit of Mount Tandiandamol, 25.9 km SSW of Madikeri, 1610 m, on a shaded Fig. 1. Habit of Phycolepidozia indica. — Scale: 1 cm. Version of Record (identical to print version). 499 Gradstein & al. • Taxonomic status of Phycolepidoziaceae rock in remnant forest along the trail, 75°36′34.20″ E, 12°13′14.68″ N, 11 Nov. 2012, U. Schwarz, J.-P. Frahm & F. Schumm s.n. (PC!; isotypes: LWG!, hb. Schwarz 10659!). Morphological description (Figs. 1–2). – Autoicous. Plants forming small, bristle-like greenish mats on rock, consisting of short, creeping rhizomes giving rise to ascending leafless shoots to 8 mm long, without leaves and underleaves but with leafy gametoecia on short branches. Stems irregularly branched, pale green when young, deep green when mature, turning blackish-green when dry, up to 1 cm long, 100–140 µm in diameter, of up to ca. 200 rows of uniformly thickened cells (50–60 epidermal cells, 140–150 inner cells), stem surface straight to remotely angled, without slime papillae; dorsal TAXON 63 (3) • June 2014: 498–508 epidermal cells in surface view irregularly oblong, ca. 13–18 × 7–10 µm, thick-walled, deep green, ventral epidermal cells shorter, subquadrate, inner stem cells narrowly rectangular, pale; stems in cross section ca. 15 cells wide, with numer­ ous strongly and ± evenly thick-walled outer cells (in 3–4 rows) with small lumina surrounding 15–20 thinner-walled and larger inner cells. Branches ventral-intercalary, arising at straight angles from ventral surface of stem. Leaves and underleaves lacking but leaves sometimes indicated by a large, hyaline cell protruding from stem surface, places of leaf insertion indicated by remote crenations of stem sur­ face. Cuticle smooth. Oil bodies present in all green cells of male and female bracts and perianth, (1–)2–5 per cell, rounded to ellipsoid, finely papillose, Jungermannia-type; oil bodies Fig. 2. Phycolepidozia indica. A, habit with gynoecia and androecia (scale: 1 mm); B, stem in cross section (scale: 50 µm); C, dehisced capsule (scale: 0.5 mm); D, cells of middle of inner valve surface (scale: 50 µm); E, seta in cross section (scale: 50 µm); F, cells of perianth mouth (scale: 50 µm); G, stem epidermis cells in surface view (scale: 50 µm). 500 Version of Record (identical to print version). TAXON 63 (3) • June 2014: 498–508 Gradstein & al. • Taxonomic status of Phycolepidoziaceae apparently lacking in stem cells. Rhizoids hyaline to pale brown, very scarce, present on rhizomes and occasionally 1–2 near shoot tips, arising singly from ventral epidermal cells (not in bundles), on rhizomes dense and short, hyaline to pale brown, at shoot tips hyaline, elongate. Asexual reproduction not observed. Androecia terminal to intercalary (by continued growth of shoots) on main stems and short or long branches, spicate, leafy. Male bracts very small, imbricate, obliquely spreading, upper part and margins colorless, lower part green, in 6–10 pairs, 0.2 × 0.15 mm, bracts becoming smaller towards apex of spike, bifid to 1/3, sinus wide, V-shaped, lobes trian­ gular, ca. 6 cells long and 6 cells wide at base, bluntly acute, undivided part of lamina deeply pouched, made up of nu­ merous non-tiered cells with evenly thickened walls, margins subentire, bases cuneate and acutely subauriculate; bracts with one globose antheridium; antheridial stalk not seen. Male bracteoles lacking. Gynoecia colorless, on short ventral branches, with connate bracts and bracteoles. Female bracts in 2–3 series, inner bract ovate-elongate, 0.3–0.4 mm long, appressed to perianth base below, spreading above, asymmetrically bifid (to max. 1/4), lobes subacute to shortly ciliate by 1–3 elongate cells, lobe margins irregularly crenate and sometimes with a large lobe-like tooth. Female bracteoles slightly shorter and narrower than bracts, more deeply bifid (to 1/3), lobe margins subentire. Cells of bracts and bracteoles with evenly thickened walls. Perianth long-cylindrical, 1–1.3 mm long, deeply 3-keeled, upper part colorless, deeply 3-lobed at mouth (to 1/4 of perianth length), apical margin crenate. Odontoschisma fluitans Fuscocephaloziopsis lunulifolia 98 Fuscocephaloziopsis crassifolia Fuscocephaloziopsis biloba Fuscocephaloziopsis catenulata Fuscocephaloziopsis pachycaulis 74 55 93 Cephalozia badia Cephalozia bicuspidata 76 Cephaloziaceae 76 99 Fig. 3. Fifty percent majorityrule consensus tree based on 36 accessions using four cpDNA loci and showing the relationship among Cephaloziaceae, Scapaniaceae and Cephaloziellaceae. The position of Phycolepidozia is marked by an asterisk. Values on branches represent bootstrap support. Cephalozia otaruensis 98 84 Andrewsianthus perigonialis Andrewsianthus marionensis Chaetophyllopsis whiteleggei Barbilophozia sp. Neoorthocaulis floerkei 79 Barbilophozia lycopodioides Barbilophozia hatcheri 54 Barbilophozia barbata 96 99 Anastrophyllum tubulosum Anastrophyllum piligerum 99 Anastrophyllum auritum 55 Anastrophyllum nigrescens 52 Scapaniaceae Sphenolobus minutus Anastrophyllum donnianum Anastrophyllum bidens Anastrophyllum michauxii Barbilophozia atlantica 84 Schlakovianthus quadrilobus 53 Anastrepta orcadensis Neoorthocaulis attenuatus Allisoniella sp. 99 100 Cephaloziella divaricata Cephalomitrion aterrimum 92 Kymatocalyx madagascariensis 99 Phycolepidozia indica 95 82 * Cylindrocolea recurvifolia Version of Record (identical to print version). Cephaloziellaceae Gymnocoleopsis multiflora 501 Gradstein & al. • Taxonomic status of Phycolepidoziaceae Sporophyte: Seta very thin, ca. 100–120 µm in diameter, ca. 3 mm long upon elongation, not articulate, formed of 4 rows of very large epidermal cells surrounding 4 minute rows of opposite inner cells, epidermis cells in surface view subrectangular, ca. 70 µm long and 50 µm wide, inner cells lacking towards base of seta. Capsule dark brown, ellipsoid, 0.35 × 0.25 mm, quadrifid to near base. Valves straight, oblong-fusiform, ca. 0.4 mm long and 0.15 mm wide, ca. 15 cells long from base to apex, very thin, bistratose, outer layer wider than inner layer, cells of the two layers not perfectly overlapping. Valve cells not tiered, narrowly rectangular, becoming shorter towards apex; inner valve cells with numerous well-defined, brown, I­shaped thickenings present on all longitudinal and transver­ sal walls, thickening elongate-nodular in surface view, 6–10 on long walls, 1–4 on short walls, thickenings not more pronounced on alternate walls; outer valve cells with much weaker thickenings, visible as dark brown spots in the walls and not nodular-elongate. Spores pale brown, 11–13 µm in diameter, surface densely and finely punctate, 1-celled at dispersal. Elaters free, rather sinuous, tapered to one side, 8–10 µm wide and 180–220(–250) µm long, with 2 brownish spirals. Distribution and ecology. – Only known from the type locality. Further specimens. – INDIA. Western Ghats, Karnataka, Coorg Distr., Mt. Tandiandamol, 1610 m, on shaded rocks in remnant forest along the summit trail, 30 Mar 2013, U. Schwarz & B. Ram s.n. (hb. Schwarz 10752); ibid., 22 Dec 2013, U. Schwarz & S. Kumar s.n. (hb. Schwarz 12300, 12301). Molecular phylogeny. – The concatenation of the four loci resulted in a matrix of 2217 base pairs including 490 polymorphic sites; 289 positions were parsimony-informative. Since the MP and ML topologies did not show any major conflict, only the ML 50% majority-rule consensus tree is shown here (Fig. 3). The tree contained two major well-supported clades, one including accessions of Cephaloziaceae (bootstrap support, BS 99) and the other accessions of Cephaloziellaceae (including Phycolepidozia indica) and Scapaniaceae (BS 99). The TAXON 63 (3) • June 2014: 498–508 latter clade comprised three main lineages in an unresolved relationship, one containing the species of Cephaloziellaceae and Phycolepidozia indica (BS 100) and the two other ones the members of Scapaniaceae (both BS 84). Phycolepidozia indica was recovered in a strongly supported Cephaloziellaceae subclade (BS 99) together with Cephalomitrion aterrimum (Steph.) R.M.Schust., Cylindrocolea recurvifolia (Steph.) Inoue and Kymatocalyx madagascariensis (Steph.) Gradst. & Váňa, being sister to Cylindrocolea recurvifolia with good support (BS 82). DISCUSSION Morphological differentiation of Phycolepidozia indica. — Phycolepidozia indica resembles P. exigua by having naked stems without leaves and underleaves and with leafy gametoecia, purely ventral-intercalary branching, scattered rhizoids, Jungermannia-type oil bodies, absence of trigones (cell walls thin or evenly thickened), small androecia intercalary on the stem with bifid bracts and no bracteoles, tristichous gynoecia on short-ventral branches with connate bracts and bracteoles, long-cylindrical and deeply 3-keeled perianths with a deeply lobed mouth, a thin seta made up of four large, non-tiered rows of outer cells and four minute inner rows, bistratose capsule valves with thickenings on all longitudinal walls, etc. (Fig. 2). In spite of these striking similarities, the two species differ morphologically in several important respects (Table 1; differences are italicized in the description). The most conspicuous difference is the massive stem of P. indica, which in cross section is made up of about 200 cells including numerous strongly thick-walled cells in 3–4 rows surrounding 15–20 larger and thinner-walled inner cells (Fig. 2B). In contrast, the stems of P. exigua are very thin, consisting of 6 rows (5 outer, 1 inner) of very thin-walled cells. Also, the epidermis cells in P. indica (Fig. 2G) are much smaller and much more thick-walled than those of P. exigua. Oil bodies are present and finely papillose in both species but in P. exigua they occur in stem cells (also Table 1. Comparison of Phycolepidozia exigua R.M.Schust. and P. indica Gradst. & al. Phycolepidozia exigua Phycolepidozia indica Stems 50 µm in diam., of 6 rows of cells 100–140 µm in diam., of ca. 200 rows of cells Leaf position Oil bodies Male bracts indicated by slime papillae in stem cells (and in gametoecia?) 3–6 pairs indicated by crenations on stem surface in gametoecia, not in stem cells 6–10 pairs Male bract lobes Male bract disc Perianth 2–3 cells wide 5–6 cells in 1–2 tiers 0.4–0.5 mm long, 6-lobed, mouth longly ciliate 5–6 cells wide numerous non-tiered cells 1–1.3 mm long, 3-lobed, mouth crenate Capsule valves Valve thickenings Spores Elaters Distribution 230 µm long, of 4 rows of tiered cells on longitudinal walls only 13–15 µm 135–150 µm long tropical America 400 µm long, of 15 rows of non-tiered cells on longitudinal and transverse walls 11–13 µm 180–250 µm long India Habitat bark and soil rock 502 Version of Record (identical to print version). TAXON 63 (3) • June 2014: 498–508 Gradstein & al. • Taxonomic status of Phycolepidoziaceae in gametoecia?) whereas in P. indica they were observed in the gametoecia but not in stem cells. Further differences are seen in the gametoecia and capsules of the two species (Table 1); many of these are quantitative, however. Thus, the male spikes of P. indica are longer than those of P. exigua and the male bracts are larger and made up of non-tiered cells (cells tiered in P. exigua). The perianths of P. indica are almost twice as long as in P. exigua and the mouth is 3-lobed and crenate, not 6-lobed and long-ciliate as in P. exigua. Furthermore, the capsules of P. indica are larger with valves almost twice as long as in P. exigua, the elaters somewhat longer and the spores slightly smaller than in P. exigua. A marked difference is seen in the capsule epidermis which is made up of about 15 rows of non-tiered cells in P. indica, with nodular thickenings occurring on both longitudinal and transverse valve walls (Fig. 2D). In P. exigua, the capsule epidermis is made up of only four rows of tiered cells and nodular thickenings are present only on longitudinal walls, not on transverse walls. It should be noted, however, that these characters are not always stable in leafy liverworts and may vary within species. In Cladopodiella franscisci (Hook.) Jörg. (Cephaloziaceae) and several species of Cephaloziella (Spruce) Schiffn. (Cephaloziellaceae), for example, thickenings may be present or absent on the transverse walls of the capsule epidermis, and in Cephaloziella spinigera R.M.Schust. the epidermal cells may be tiered or non-tiered within a single capsule (Schuster, 1974, 1980). These data suggest that the taxonomic importance of the differences in the capsule walls of the two Phycolepidozia species should not be overrated. Nevertheless, the differences observed between P. exigua and P. indica, especially those in the stem and perianth mouth, indicate that the two species are morphologically rather distant to each other, and they are here therefore placed in different subgenera (see Taxonomic implications). It might even be argued that the two species are not congeneric and that P. indica should be given generic status. We refrain from placing P. indica in a separate genus, however. As shown by Vanderpoorten & al. (2012) and others, an increasingly large number of monospecific genera of liverworts, among them several highly specialized and morphologically well-defined taxa, have recently been relegated to synonymy based on molecular evidence. Without molecular study of P. exigua, the creation of a monospecific genus for P. indica would seem to be premature. Genera are convenient taxonomic vehicles for the naming of groups of species (Humphries & Linder, 2009); only in rare cases they represent single species. Given the current trend in liverwort systematics of reducing monospecific genera, we believe that description of new ones should be done with great care and be avoided unless the relationship of the respective taxon to other genera is clear. In case of P. exigua and P. indica, the latter principle does not apply. The morphological differences between the two species are considerable, however, and undoubtedly warrant placement of the two in separate subgenera. Although vegetative leaves and underleaves are absent in P. indica, the position of the leaves on the stems seems to be indicated by remote crenations of the stem surface. Leaf position, whether incubous or succubous, could not be determined, however. Occasionally, a relatively large, hyaline cell is present on the crenation and this might possibly represent a rudimentary leaf. An ontogenetic study of the development of the gametophyte in this species is necessary to verify this assumption. Schuster (1966) described the presence of small, 2-celled papillae on the stem surface of P. exigua and tentatively interpreted these as rudimentary leaves. In P. indica, however, hyaline papillae were not observed. Phylogeny of Phycolepidozia. — The results of the molecular analysis unequivocally show that P. indica is a member of the family Cephaloziellaceae. Consequently, Phycolepido­ zia and Phycolepidoziaceae are transferred to Cephaloziellaceae. Morphologically, the position of Phycolepidoziaceae in Cephaloziellaceae is strongly supported by the structure of the sporophyte, which is essentially similar in the two families and fundamentally different from that of Cephaloziaceae and Lepidoziaceae, with which Phycolepidoziaceae were also compared previously (Schuster, 1966; Gradstein & al., 2001). Typical cephalozielloid features of the sporophyte of both P. exigua and P. indica are the highly reduced seta, consisting of four rows of large epidermis cells surrounding four rows of minute inner cells, and the bistratose capsule wall with thickenings on all longitudinal walls of the epidermal cells. The 4 + 4 seta is unique to Cephaloziellaceae and not found in any other group of liverworts (e.g., Douin, 1914; Schuster, 1971; Crandall-Stotler & al., 2009). Bistratose capsule walls are also found in Cephaloziaceae and Lepidoziaceae but in these two families thickenings are only developed on alternate walls of the epidermis (“two-phase development” of wall thickenings; Schuster, 1984). Scapaniaceae, which is part of the same clade Cephaloziellaceae in the molecular analysis (Fig. 3), shares with the latter family the presence of thickenings on all longitudinal epidermal walls but differs fundamentally by the thicker seta and capsule wall. Thus, the cephalozielloid sporophytes of P. exigua and P. indica clearly support their position in Cephaloziellaceae and refute placement of P. exigua in a separate family Phycolepidoziaceae as advocated by Schuster (1966), in spite of the leafless gametophyte. Further features supporting the placement of Phycolepidozia in Cephaloziellaceae are the Jungermannia-type oil bodies, the evenly thick-walled cells of stems and gametoecia, lacking trigones, as well as the scattered rhizoids. The similarities in the sporophytes and gametophytes of the two Phycolepidozia species suggests that their leafless habit has resulted from a single evolutionary event and is not due to convergence. A somewhat similar situation is seen in the moss genus Ephemeropsis K.I.Goebel. The present molecular results confirm the monophyly of the Cephaloziellaceae. Based on molecular analyses, Forrest & al. (2006), Heinrichs & al. (2007), Hentschel & al. (2007) and others (see also Crandall-Stotler & al., 2009) found strong evidence for Cephaloziellaceae as a robust lineage sister to, but separate from, Scapaniaceae. De Roo & al. (2007), however, resolved Cephaloziellaceae within a broadly defined Scapaniaceae, albeit with weak support. Our results show an unresolved relationship of the well-supported Cephaloziellaceae and two lineages of Scapaniaceae s.l. Version of Record (identical to print version). 503 Gradstein & al. • Taxonomic status of Phycolepidoziaceae The deviating morphology of Phycolepidozia, viz. absence of leaves and underleaves in this “leafy” liverwort, indicates, along with an increasing body of evidence, that extreme morphological transformations can obscure the phylogenetic signal present in morphological data (e.g., Heinrichs & al., 2012; Vanderpoorten & al., 2012). This may sometimes lead to dramatic differences in the generic or even familial placement of taxa. Examples from liverworts include the monospecific genus Metzgeriopsis K.I.Goebel from Southeast Asia characterized by a unistratose thallus (often interpreted as an enlarged protonema) with leafy sexual branches arising from thallus margins. Recent molecular analysis showed that Metzgeriopsis is a highly modified member of the leafy liverwort genus Colo­ lejeunea (Spruce) Schiffn. (Gradstein & al., 2006). Similarly, the odd thalloid genus Mizutania Furuki & Z.Iwats. resembling members of Aneuraceae but with leafy bracts, was recently shown to be a member of the leafy liverwort family Calypogeiaceae (Masuzaki & al., 2010). Among mosses several examples are known of genera with highly reduced gametophytes that were difficult to classify, for example Buxbaumia Hedw., Discelium Brid., Ephemerum Hampe, Ephemeropsis, Micromitrium Austin and Viridivellus I.G.Stone (Gradstein & Wilson, 2008; Goffinet & al., 2011). In all these groups, the gametophyte is largely replaced by a persistent, photosynthetically active protonema. A striking example is Ephemeropsis with E. trentepohlioides (Renner) Sainsbury in New Zealand and Tasmania and E. tjibodensis K.I.Goebel in Southeast Asia, North Australia and New Caledonia. Like Phycolepidozia, Ephemeropsis was long placed in a separate family, Ephemeropsidaceae (= Nemataceae), because of the highly modified gametophyte. The peristome and calyptra of Ephemeropsis, however, are similar to those of Daltoniaceae (Buck, 1988). Recent molecular analysis has confirmed that Ephemeropsis is a member of Daltoniaceae (Shaw & al., 2003; Ho & al., 2012). The latter study also showed that the two Ephemeropsis species form a monophyletic lineage, in spite of considerable morphological differences in the gametophyte and the sporophyte generation of the two (Bartlett & Iwatsuki, 1985). Examples of leafless taxa from vascular plants which were long difficult to classify are Cuscuta L. and Psilotum Sw. Cus­ cuta is a heterotrophic flowering plant with strongly reduced leaves, no roots and with reduced chloroplasts. Its leafless habit is similar to that of the heterotrophic Cassytha filifor­ mis L. (Lauraceae) from Africa and is presumably an adaptation to its parasitic life style. Cuscuta has alternatively been treated as a member of Convolvulaceae or as a family in its own right, Cuscutaceae. The extreme reduction of morphological and anatomical characters of Cuscuta has made the systematic position of the genus uncertain. Molecular evidence has shown that the genus is a highly derived member of Convolulaceae (Neyland, 2001). Psilotum was traditionally placed in a separate phylum, Psilophyta, and considered by some the basalmost living vascular plant although relationships to the ophioglossoid ferns had also been noted. Molecular evidence has confirmed that Psilotum is a fern sister to Ophioglossales and not a separate phylum (Qiu & Palmer, 1999; Pryer & al., 2001). 504 TAXON 63 (3) • June 2014: 498–508 There are several liverwort genera with highly unusual morphologies similar to those of Phycolepidozia, Metzgeriopsis and Mizutania that still need study. Examples are the Amazonian Amazoopsis J.J.Engel & G.L.Merr. (Lepidoziaceae), Protocephalozia (Spruce) K.I.Goebel (Cephaloziaceae) and Pteropsiella Spruce (Lepidoziaceae), and Meinungeria Frank Müll. (Lepidoziaceae) from New Caledonia, all of which are characterized by the presence of leafy gametoecia and reduction of vegetative leaves and underleaves. Of these, Meinunge­ ria superficially resembles Phycolepidozia by its worm-like, almost leafless stems and large, subsessile gynoecia (Müller, 2007: fig. 5). However, the presence in Meinungeria of vestigial underleaves (made up of 3–4 radially arranged single cells) and rhizoids originating in bundles from underleaf bases sharply separate this genus from Phycolepidozia. Sporophytes and androecia of Meinungeria are unknown. Owing to their unusual morphology, the phylogenetic relationships of Amazo­ opsis, Meinungeria, Protocephalozia and Pteropsiella remain unclear. Molecular phylogenetic work is necessary to determine the relationships of these unusual plants. Distribution and ecology of Phycolepidozia indica. — Phy­ colepidozia indica was collected near the peak of Mt. Tandiandamol in the Western Ghats, South India. Mount Tandiandamol (1750 m) is the highest peak of the mountainous Coorg District, in the southern part of the Western Ghats. The district has a seasonal tropical climate with the monsoon season starting in June and lasting until November. Annual rainfall in the adjacent Madikeri district is up to 3500 mm with an average number of 118 rainy days per year (Pascal, 1982). Fog during morning hours in the cooler months also contributes to the precipitation. Temperatures range between 19°C and 23°C throughout the year. Geologically the area between Madikeri and Virajpet is made up of metamorphic crystalline rock (granitic gneiss). Suitable rock habitats for bryophytes are mountain cliffs, river banks and sides of tracks. The forest of the summit area of Mt. Tadiandamol is dense and evergreen and has been classified as Schefflera–Gordonia obtusa–Meliosma forest (Pascal, 1986). The predominant tree species are Cinnamomum verum, Gor­ donia obtusa, Litsea stocksii, Meliosma simplicifolia subsp. pungens, Neolitsea zeylanica, Phoebe wighti, Schefflera mi­ crantha, Syzygium caryophyllatum and S. hemisphericum. Bryological exploration of the Western Ghats has a long history, dating back to the 19th century, and the area is being considered a hotspot of biodiversity (Gunawardene & al., 2007). Nevertheless, most bryophyte collecting has been done in parts of the Ghats further to the south, belonging to the states of Kerala and Tamil Nadu. Locations such as the Nilghiri Mts., Palni Hills and Kodaikanal are famous for their richness in species and are the type localities for many species of bryophytes (Manju & al., 2008; Daniels, 2010). In contrast, the adjacent parts of the Western Ghats belonging to the state of Karnataka remain largely unexplored (Frahm & al., 2013). Mount Tandiandamol was visited by L.T. Walker in 1897–98, who collected only moss species (see list in Brotherus, 1899). Records of liverworts from the area are few (Alam, 2012; Verma, 2009), but a comprehensive checklist of liverworts of the Coorg District does not exist. Version of Record (identical to print version). TAXON 63 (3) • June 2014: 498–508 Gradstein & al. • Taxonomic status of Phycolepidoziaceae Currently, the mountain slopes of Mt. Tandiandamol are heavily deforested and the natural vegetation is largely replaced by coffee plantations up to 1200 m and by open grassland with bushes between 1200–1750 m. Some small patches of forest remain in ravines and along the summit trail at 1600–1700 m. Phycolepidozia indica was found on metamorphic crystalline rock in remnant forest along the summit trail, and was quite conspicuous in the field by its naked, leafless stems with numerous gametoecia (Fig. 1). Associated bryophyte species were the mosses Fissidens sp., Dixonia orientalis (Mitt.) H.Akiy. & Tsubota and Thamniopsis utacamundiana (Mont.) W.R.Buck; no other liverwort species were seen growing associated with P. indica. Upon its discovery in November 2012 the species was found on a single rock, but during a revisit of the type locality in December 2013 the species was seen on six further rocks within the forest patch. Possibly, the species has been widespread in the area in the past but has become scarce following deforestation of the slopes of Mt. Tandiandamol. Biogeography of Phycolepidozia. — The disjunct occurrence of Phycolepidozia in the Neotropics and in southern India is intriguing. Thorne (1972) referred to these tropical Asian-Neotropics ranges as amphi-Pacific tropical disjunctions and enumerated 89 genera of flowering plants exhibiting this type of distribution. Past migration via the North Atlantic bridges followed by local extinction and long-range dispersal have been used most commonly to explain these amphiPacific disjunctions, but only few examples have been analysed with molecular phylogenetic and biogeographic methods (Li & Wen, 2013). Among bryophytes, amphi-Pacific tropical disjunctions occur in 16 genera, 7 of mosses and 9 of liverworts (Table 2). The list does not claim to be exhaustive and more bryophyte taxa exhibiting this type of distribution may exist. The amphiPacific tropical disjuncts occur in different habitats such as on tree trunks (Elmerobryum, Mniomalia, Sorapilla, Pictole­ jeunea, Spruceanthus, Vitalianthus), rock (Cololejeunea subg. Chlorolejeunea, Ganguleea, Hymenostyliella, Luisierella, Myriocoleopsis), rotten logs or soil (Lobatiriccardia), living leaves (Cololejeunea subg. Chlorolejeunea, Drepanolejeunea subg. Rhaphidolejeunea) and on twigs and branches in the outer canopy of the rainforest (Ceratolejeunea grandiloba, Rectole­ jeunea). Dispersal scenarios rather than geographical vicariance have usually been proposed by recent authors as the preferred explanations for the intercontinental ranges of bryophyte species and genera (Heinrichs & al., 2009; Gradstein, 2013b). However, most of the amphi-Pacific tropical disjuncts with the exception of Cololejeunea subg. Chlorolejeunea, Myriocoleop­ sis, Lobatiriccardia and Vitalianthus have not been analysed by molecular phylogenetic methods, and their taxonomic circumscriptions are largely based on morphology. To better understand their biogeographic histories, the taxonomic status and distribution of these disjuncts need to be analysed by robust methods. For example, phylogenetic analysis of the putatively Asian-Neotropical Echinocolea R.M.Schust. Table 2. Amphi-Pacific tropical disjunctions in bryophytes. Taxon No. of species Distribution Reference Mosses Austinia Müll.Hall. 2 SE Asia, Neotropics Buck & Crum, 1978; Gradstein & al., 2001 Elmeriobryum Broth. 3 SE Asia, C America Buck & Tan, 2007 Ganguleea R.H.Zander 1 Himalayas, SE Brazil Zander, 1993 Hymenostyliella Bartr. 3 SE Asia, Brazil Zander, 1993 Luisierella Thér. & P.Varde 1 Japan, Java, Neotropics Zander, 1993 Mniomalia Müll.Hal. 2 SE Asia, Neotropics Norris & Koponen, 1987 Sorapilla Mitt. & Spruce 2 E Malesia, N Australia, Ecuador Norris & Koponen, 1987 Liverworts Ceratolejeunea grandiloba J.B.Jack & Steph. 1 (2 subsp.) Java, tropical Andes Gradstein, 2013a Cololejeunea subg. Chlorolejeunea Benedix 2 SE Asia, Ecuador Gradstein & al., 2011 Drepanolejeunea subg. Rhaphidolejeunea (Herzog) Grolle & R.L.Zhu 11 SE Asia, Amazonia Grolle & Zhu, 2000 Lobatiriccardia (Mizut. & S.Hatt.) Furuki 8 SE Asia, Australasia, Ecuador Preußing & al., 2010; Nebel & al., 2013 Myriocoleopsis Schiffn. 3 Vietnam, SE Brazil, Ecuador Pócs, 2010 Phycolepidozia R.M.Schust. 2 India, Neotropics this paper Pictolejeunea Grolle 6 Borneo, Neotropics Grolle, 1977; Pócs, 2007 Reiner-Drehwald & Grolle, 2012 Rectolejeunea A.Evans 5 N Australia, Neotropics Spruceanthus Verd. 9 SE Asia, Australia, Ecuador, Europe (†) Grolle, 1985; Gradstein & al., 2001, 2002 Vitalianthus R.M.Schust. & Giancotti 2 China, Brazil Version of Record (identical to print version). Wei & al., 2013 505 Gradstein & al. • Taxonomic status of Phycolepidoziaceae showed that the genus is nested in Lejeunea Lib. and may not be monophyletic (Ilkiu-Borges, 2005; but see Heinrichs & al., 2013). Similarly, the circumscriptions of the amphi-Pacific genera Myriocoleopsis, Spruceanthus and Vitalianthus have become questionable based on recent molecular studies (Wilson & al., 2007; Yu & al., 2013; R.L. Zhu, pers. com.). On the other hand, it should be taken into account that the disjunct amphiPacific ranges may reflect insufficient collecting. The moss genus Campylopodiella Card., for example, was long known only from the Neotropics and the Himalayan region and considered an amphi-Pacific disjunct, but was recently detected in Africa (Townsend, 2009). Undercollecting is likely in the case of Phycolepidozia due to its minute size. It may also hold for the epiphyllous Drepanolejeunea subg. Rhaphidolejeunea, the rheophytic Cololejeunea subg. Chlorolejeunea and Myrioco­ leopsis, and the canopy specialists Ceratolejeunea grandiloba and Rectolejeunea, all of which grow in habitats that have been little inventoried. More intensive exploration of their habitats may reveal additional localities for these intriguing amphiPacific taxa. Taxonomic implications Cephaloziellaceae Douin in Mém. Soc. Bot. France 29: 1. 1920 – Type: Cephaloziella (Spruce) Schiffn. = Phycolepidoziaceae R.M.Schust. in Bull. Torrey Bot. Club 93: 442. 1966, syn. nov. – Type: Phycolepidozia R.M.Schust. Phycolepidozia R.M.Schust. in Bull. Torrey Bot. Club 93: 438. 1966 – Type: P. exigua R.M. Schust. Contains two species, in 2 subgenera. Phycolepidozia subg. Phycolepidozia Stem of 6 rows of cells. Male bract disc of 5–6 cells in 1–2 tiers. Perianth mouth 6-lobed, longly ciliate. Capsule valves ca. 230 µm long, of 4 rows of tiered cells; thickening present on longitudinal walls only. Contains P. exigua R.M.Schust. from Dominica and Venezuela. Phycolepidozia subg. Metaphycolepidozia Gradst., J.-P.Frahm & U.Schwarz, subg. nov. – Type: P. indica Gradst., J.-P. Frahm & U.Schwarz Stem of ca. 200 rows of cells. Male bract disc of numerous non-tiered cells. Perianth mouth 3-lobed, crenate. Capsule valves ca. 400 µm long, of 15 rows of non-tiered cells; thickenings present on longitudinal and transverse walls. Contains P. indica Gradst. & al. from South India. 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Dumort., KC184781.1, –, AY462291, JF513486.1; Cephalozia otaruensis Steph., KC184781.1, –, AB476560.1, –; Fuscocephaloziopsis biloba (Herzog) Fulford, –, –, KC184712.1, –; Fuscocephaloziopsis catenulata (Huebener) Váňa & L.Söderstr., –, –, –, AY608053.1; Fuscocephaloziopsis crassifolia (Lindenb. & Gottsche) Váňa & L.Söderstr., KC184780.1, –, KC184711.1, AM398309.1; Fuscocephaloziopsis lunulifolia (Dumort.) Váňa & L.Söderstr., –, –, –, AM398315.1; Fuscocephaloziopsis pachycaulis (R.M.Schust.) Váňa & L.Söderstr., KC184782.1, –, KC184714.1, –; Odontoschisma fluitans (Nees) L.Söderstr. & Váňa, KC184789.1, –, JX305542.1, –. CEPHALOZIELLACEAE. Allisoniella sp., FATOL788, New Zealand, Engel & Konrat 28608 (F), KF851891, –, –, KF851429; Cephalomitrion aterrimum (Steph.) R.M.Schust., L1226, New Zealand, Engel & Konrat 28545 (F), KF851926, –, KF852368, KF851459; Cephaloziella divaricata (Sm.) Schiffn., L1426, Czech Republic, Sova s.n. (DUKE), KF851965, KF852248, KF852399, KF851489; Cylindrocolea recurvifolia (Steph.) Inoue, FATOL445, Japan, Yamaguchi s.n. 23 Sep 2007 (F), KF851848, KF852130, KF852297, KF851399; Gymnocoleopsis cylindriformis (Mitt.) R.M.Schust. (= G. multiflora (Steph.) R.M.Schust.), Venezuela, Söderström 2004/091 (BOL), –, –, –, AM398239; Kymatocalyx madagascariensis (Steph.) Gradst. & Váňa, IBC64, Madagascar, Pocs 9446/AQ (F), AY607990, KF852200, –, AY608111; Phycolepidozia indica Gradst. & al., S India, Schwarz 10659 (PC), KF862486, KF895402, KF862485, KF895403. SCAPANIACEAE. Anastrepta orcadensis (Hook.) Schiffn., JF513391.1, JF513407.1, JF513450.1, JF513468.1; Anastrophyllum auritum (Lehm.) Steph., KC184771.1, –, KC184702.1, –; Anastrophyllum bidens (Reinw. & al.) Steph., KC184769.1, –, KC184700.1, –; Anastrophyllum donnianum (Hook.) Steph., KC184770.1, –, KC184701.1, –; Anastrophyllum michauxii (F.Weber) A.Evans, –, –, AY507390.1, AY507433.1; Anastrophyllum nigrescens (Mitt.) Steph., KC184772.1, –, KC184703.1, –; Anastrophyllum piligerum (Reinw. & al.) Steph., KC184773.1, –, KC184704.1, –; Anastrophyllum tubulosum (Nees) Grolle, KC184774.1, –, KC184705.1, –; Andrewsianthus marionensis (S.W.Arnell) Grolle, KC184775.1, –, KC184706.1; Andrewsianthus perigonialis (Hook.f. & Taylor) R.M.Schust., KC184776.1, –, KC184707.1, –; Barbilophozia atlantica (Kaal.) Müll.Frib., –, –, –, AM398349.1; Barbilophozia barbata (Schreb.) Loeske, AM396187, –, JX305536.1, AM398313; Barbilophozia hatcheri (A.Evans) Loeske, KC184777.1, –, DQ312478.1, AM398338.1; Barbilophozia lycopodioides (Wallr.) Loeske, KC184778.1, –, KC297121.1, AM398333.1; Barbilophozia sp., –, –, JX305573.1, JX308594.1; Chaetophyllopsis whiteleggei (Carringt. & Pears.) Hamlin, –, –, AY462292.1, AY462346.1; Neoorthocalis attenuatus (Mart.) L.Söderstr. & al., –, –, GU373417.1, –; Neoorthocaulis floerkei (Web. & Mohr) L.Söderstr. & al., –, –, KC297118.1, –; Schljakovianthus quadrilobus (Lindb.) Konstant. & Vilnet, –, –, –, AM398324.1; Sphenolobus minutus (Schreb.) Berggr., –, –, DQ312475.1, JX308554.1. 508 Version of Record (identical to print version).