On the Taxonomy of Anomodontaceae and Heterocladium (Bryophyta) К Систематике Anomodontaceae И Heterocladium (Bryophyta) Michael S

Home , Alleniella, Anomodontaceae, Anomodon (plant), Anomodon attenuatus, Arctoa, Dendroalsia

Arctoa (2019) 28: 75–102 doi: 10.15298/arctoa.28.08

ON THE TAXONOMY OF ANOMODONTACEAE AND HETEROCLADIUM (BRYOPHYTA) К СИСТЕМАТИКЕ ANOMODONTACEAE И HETEROCLADIUM (BRYOPHYTA) MICHAEL S. IGNATOV1,2 , ALINA V. F EDOROVA2 & VLADIMIR E. FEDOSOV1 МИХАИЛ С. ИГНАТОВ1,2, АЛИНА В. ФЕДОРОВА2, ВЛАДИМИР Э. ФЕДОСОВ1

Abstract

A molecular phylogenetic analysis based on nuclear ITS, plastid trnS-F, rpl16, atpB–rbcL and mitochondrial nad5 revealed polyphyly in the genus Anomodon, and therefore its segregation into four genera is proposed. The largest clade includes A. viticulosus, the generitype of Anomodon, and all species with a broadly rounded leaf apex, including those with both pluripapillose (A. minor, A. thraustus, A. dentatus) and pseudounipapillose (A. abbreviatus, A. solovjovii) laminal cells. The species of Haplohymenium form a sister clade to Anomodon; however this clade is always maximally supported in Bayesian analyses, and thus Haplohymenium merits taxonomic recognition as a genus of its own. Two closely related species, Anomodon attenuatus and A. giraldii, were found deeply nested in the Neckeraceae, and thus they are segregated in the genus Pseudanomodon (Limpr.) Ignatov & Fedosov. Anomodon rugelii was found to be distant from the core Anomodon clade and is segregated into a new genus Anomodontopsis Ignatov & Fedosov within the Anomodontaceae. Anomodon longifolius has an erratic position in various analyses, appearing basal in the Anomodontaceae clade or sister to the A. rugelii clade in the organellar trees, or in a clade with Heterocladium dimorphum, closer to the Neckeraceae than to the Anomodontaceae, in the tree inferred from nuclear ITS. It is therefore referred to the new genus Anomodontella Ignatov & Fedosov in the Anomodontaceae. Likewise, Heterocladium species form two clades, centered around H. dimorphum and H. heteropterum. The latter group is referred to Lembophyllaceae, while H. dimorphum and related species form a fairly isolated group and are segregated in their own genus Heterocladiella Ignatov & Fedosov in the monogeneric family Heterocladiellaceae Ignatov & Fedosov. The genus Herpetineuron is excluded from the Anomodontaceae.

Резюме

Молекулярно-филогенетический анализ, основанный на последовательностях ITS ядерной ДНК, trnS-F, rpl16 и atpB–rbcL хлоропластной ДНК и nad5 митохондриальной ДНК, выявил поли- филетичность рода Anomodon; предложено разделить его на 4 рода. Самая крупная клада молекулярно-филогенетического дерева включает A. viticulosus, который является типовым видом рода Anomodon, и все виды с широко закругленной верхушкой листа, как с мультипапиллозными клетками пластинки (A. minor, A. thraustus, A. dentatus), так и с “псевдоунипапиллозными” (A. abbreviatus и A. solovjovii). Виды рода Haplohymenium образуют кладу, сестринскую кладе Anomodon s.str.; эта клада имеет максимальную поддержку по результатам Байесова анализа, из чего следует, что Haplohymenium заслуживает таксономический статус самостоятельного рода. Два близкородственных вида, Anomodon attenuatus и A. giraldii, во всех реконструкциях оказываются в одной кладе с видами, относящимися к семейству Neckeraceae (вместе с Homalia trichomanoides); эти два вида выделены в отдельный род Pseudanomodon (Limpr.) Ignatov & Fedosov. Во всех вариантах анализа Anomodon rugelii занимает сестринское положение к высоко поддержанной кладе Anomodon s.str. + Haplohymenium, так что он выделяется в новый род Anomodontopsis Ignatov & Fedosov в семействе Anomodontaceae. Позиция Anomodon longifolius непостоянна: в деревьях, построенных по органеллярным маркерам, он оказывается в базальном положении к кладе Anomodon или формирует кладу с A. rugelii, тогда как в деревьях, построенных по ITS, он находится в кладе с Heterocladium dimorphum; на этом основании описан новый род Anomodontella Ignatov & Fedosov в семействе Anomodontaceae. Виды рода Heterocladium образует две клады, к одной из которых относится H. dimorphum и ко второй – H. heteropterum. Виды последней клады остаются в роде Heterocladium, но этот род предложено относить к семейству Lembophyllaceae, тогда как H. dimorphum и близкий к нему H. procurrens, образующие хорошо изолированную группу, выделены в новый род Heterocladiella Ignatov & Fedosov и семейство Heterocladiellaceae Ignatov & Fedosov. Род Herpetineuron исключен из Anomodontaceae.

KEYWORDS: Anomodon, Heterocladium, mosses, Hypnales, taxonomy, molecular phylogeny, new genera, new family, papillae.

1 – Lomonosov Moscow State University, Faculty of Biology, Moscow 119234 Russia – Россия, 119234, Москва, Московский государственный университет, биологический факультет. E-mails: [email protected]; [email protected] 2 – Tsitsin Main Botanical Garden, Russian Academy of Sciences, Botanicheskaya Str., 4, Moscow 127276 Russia – Россия 127276 Москва, Ботаническая 4, ГБС РАН. 76 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

INTRODUCTION had previously been separated in a family with this name. The Hypnales form the terminal clade in the phylo- The need to fix this nomenclatural problem for mosses genetic tree of mosses (Newton et al., 2000; Tsubota et remains, so we undertook the present analysis in order to al., 2004; Shaw et al., 2003; Lui et al., 2019). This order solve it as well. In doing so, we paid special attention to is the largest among bryophytes, and also the most diffi- papillae, which seemingly were described without ad- cult for classification, as most characters valuable for equate detail to be considered as a character of familial taxonomy are homoplasic (Huttunen et al., 2012). Many importance, as is usually assumed. of them have been widely used because they look con- MATERIAL AND METHODS spicuous and are easily observed. The molecular phylo- Molecular phylogenetic studies genetic approach to taxonomy has already revealed many cases where morphological characters have been over- The material used in the present study was sampled valued, overturning assumptions about the importance from MW and MHA and supplemented by sequences avail- of, for example, the “Isobryalean peristome” (Buck et able in GenBank. For the molecular-phylogenetic study al., 2000; Tsubota et al., 2002), Neckera-like undulate we used five markers, nuclear ITS1,2 and 5.8 rRNA gene, leaves (Olsson et al., 2011), Drepanocladus-like falcate- plastid region trnS-F, plastid rpl16 gene intron, plastid secund leaves with a costa (Vanderpoorten et al., 2002); atpB-rbcL intergenic spacer and mitochondrial nad5, Hypnum-like falcate-secund leaves without a costa which have been used successfully in numerous studies of (Gardiner et al., 2005; Ignatov et al., 2007; Arikava et pleurocarpous moss phylogeny (Vanderporten et al., 2002; al., 2008; Câmara et al., 2018; Schlesak et al., 2018), Stech & Frey, 2008; Stech & Quandt, 2014; Olsson et al., and a dendroid growth-form (Ignatov et al., 2014). In 2009a,b, 2011, etc.). Our sampling was mostly focused on this paper we will try to address one more such charac- our target groups and was intended to check for the repli- ter, the papillosity of the laminal cells. cation of results obtained in specimens sampled from re- Acrocarpous mosses exhibit a great variety of papil- mote areas of their distribution. Likewise we expanded lose and mammillose cells, which occur in about half of the representation of the types of the genera to which these the families, while pleurocarps usually have smooth species have been assigned. In addition, the genera laminal cells, which probably correlates with the Haplohymenium and Herpetineuron, which are often prosenchymatous cell shape. Elongate multipapillose placed in the Anomodontaceae (cf. Ignatov et al., 2006), laminal cells are characteristics of only one family, the were included to check their affinity with Anomodon. In Meteoriaceae. In other families, papillose cells occur in total 49 specimens were studied de novo. Sequences for a species with short laminal cells, which has caused them suite of species well represented in Genbank were included to be combined together in genera and families. using the Blast facility and previously published recon- For this reason, Brotherus (1925) placed in the structions to provide representation of the major clades of Thuidiaceae genera currently classified in different fami- pleurocarpous mosses, both closely related groups and lies: Myurella (Plagiotheciaceae), Fauriella putative outgroups, thereby placing our data in the con- (Pylaisiadelphaceae), Anomodon (Anomodontaceae), text of a backbone phylogeny of pleurocarpous mosses. Heterocladium (Heterocladiaceae nom. illeg.), Vouchers of the newly sequenced specimens and GenBank Leptopterigynandrum (Taxiphyllaceae), and Miyabea accession numbers of all used sequences are compiled in (Miyabeaceae). Supplementary Materials 1. The original aim of the present study was to address The laboratory protocol was essentially the same as the classification of the genera Anomodon and in previous moss studies, described in detail by, e.g., Heterocladium for the Moss Flora of Russia. A previous Gardiner et al. (2005), Hedenäs (2017). Sequences were analysis (Gardiner et al., 2005) based on limited sam- aligned using MAFFT v. 7.402 (Katoh & Standley, 2013) pling has already revealed their non-monophyly. with standard settings and then edited manually. For the Anomodon rostratus was transferred to Claopodium highly variable ITS indels were considered as missing (Ignatov et al., 2006), while the distant positions of A. data, while in the less informative but unequivocally attenuatus, A. giraldii, A. longifolius and A. rugelii have aligned organellar markers indels were coded using not been discussed, even though some of them were con- simple indel coding technique (Simmons & Ochoterena, firmed in other publications, e.g. Tsubota et al. (2004), 2000) in SeqState 1.4.1 (Müller, 2005). Highly Ignatov et al. (2007), Olsson et al. (2009a,b). Among homoplasic inversion in the trnL-trnF spacer was ex- others, Olsson et al. (2009a) found A. giraldii nested in cluded from the analysis. At first, ITS (97 terminals, 1118 the Neckeraceae and indicated that its phylogenetic po- positions), trnS-F (93 terminals, 1995 positions), rpl16 sition would be discussed in later papers, but this has not (81 terminals, 864 positions), atpB (59 terminals, 705 yet happened. An isolated position of Heterocladium was positions) and nad5 (77 terminals, 1141 positions) were revealed by Gardiner et al. (2005), and Ignatov & analyzed separately to check their congruence. Since no Ignatova (2004) had already segregated it in the family supported conflict of topologies was observed among the Heterocladiaceae. This family name is however illegiti- trees inferred from organellar markers, the sixth dataset mate, as the red algae genus Heterocladia Decaisne, 1841 represented the concatenated, trnS-F, rpl16, atpB and On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 77 nad5 sequences (97 terminals, 4711 bp), and indels were (Heterocladium heteropterum, H. wulfsbergii & H. considered as missing data. The sixth dataset was di- macounii), Neckeraceae s.str. (Neckera pennata, N. vided into two partitions, for cp and mt data. Bayesian menziesii, Forsstroemia trichomitria & Alleniella Analyses were performed by running two parallel analy- complanata), “Neckeraceae II” (Chileobryon, ses in MrBayes 3.2.6 (Ronquist et al., 2012). For the Pendulothecium, Thamnobryum, Homalia, Anomodon p.p., single gene set analyses, each run consisted of six Markov etc.), Orthostichella (O. rigida & O. versicolor), chains, 10 000 000 generations with the default number Anomodontaceae s.str. (Anomodon viticulosus, A. of swaps, and sampling frequency one tree each 2500 thraustus, A. abbreviatus, A. solovjovii, A. minor, generations. For the concatenated dataset the analysis Haplohymenium spp. & Anomodon rugelii), Thuidiaceae consisted of eight Markov chains and 25 000 000 gen- s.str. (Abietinella, Helodium, Pseudoleskeopsis & erations, with the default number of swaps and sampling Boulaya), some poorly represented major lineages frequency one tree each 5 000 generations. The chain (Brachytheciaceae, Meteoriaceae, Calliergonaceae, etc.) temperature was set at 0.02 in all analyses. Convergence and other groups, whose putative phylogenetic affinity of each analysis was evaluated using Tracer1.4.1 varies depending on the marker (Anomodon longifolius, (Rambaut & Drummond, 2007). Consensus trees were Claopodium spp., Herpetineuron toccoae and calculated after omitting the first 25% trees as burn-in. Iwatsukiella). Since sampling in this study was aimed at Analyses were performed on the Cipres Science Gate- revealing the affinities of a few particular lineages, con- way (http://www.phylo.org/portal2) on XSEDE (Miller centrated within the “Anomodontaceae s.l. & et al., 2010). All trees were rooted on Hookeria lucens Lembophyllaceae & Orthostichellaceae & Neckeraceae s.l. (Hedw.) Sm. or on Hookeria lucens and Distichophyllum clade”, inferred from better resolved trees based on ITS crispulum (Hook. f. & Wilson) Mitt. and trnS-F, this group will be discussed in more detail. Morphological observations Most of the groups at familial level were found to be monophyletic, except for Anomodontaceae, Material for SEM was prepared in two ways. Peris- Heterocladiaceae and Neckeraceae. Species placed in the tomes were coated with gold and observed under SEM Anomodontaceae (the genera Anomodon, Herpetineuron Cambridge Instruments CamScan S2 without additional and Haplohymenium) are found in three or four unrelated preparation. Some observations of the leaf and stem struc- clades in the trees obtained. Five species of the genus tures were made in a similar way (this is indicated on the Anomodon form a moderately to highly supported clade photos). In other cases, shoots were wetted in phosphate sister to the Haplohymenium clade. The clade with buffers, fixed in 2% glutaraldehyde for 24 hours, washed Anomodon rugelii in most reconstructions was found in a in water, post-fixed with 2% osmium tetroxide in dis- sister clade to the Anomodon s.str. & Haplohymenium tilled water for 2 hours, washed in water, dehydrated clade, and their common clade is mostly well supported. through an ascending alcohol-acetone series, dried at In reconstructions inferred from organellar markers, the critical point, covered with gold, and observed under SEM clade with Anomodon longifolius splits on the next deeper Cambridge Instruments CamScan S2. node and this node lacks statistical support, while in the Material for Confocal Laser Scanning Microscopy ITS based reconstruction it forms an unsupported group- (CLSM) was taken from herbarium material. Shoots with- ing with the Heterocladium dimorphum clade, which is out fixation were stained by 0,1mM DAPI and berberin sister to the “Neckeraceae s.l.” clade. The clades corre- and investigated under an Olympus FV-1000, with 405 sponding to A. attenuatus and A. giraldii are deeply nested and 473 nm lasers. within the Neckeraceae s.str. clade, close to each other RESULTS and Homalia trichomanoides. In the reconstructions in- Molecular phylogenetic analysis: single gene analyses ferred from ITS and rpl16, the clades with A. attenuatus In general, the topologies inferred from analyses based and A. giraldii form a well-supported clade sister to the on single gene datasets resemble each other, although they Homalia trichomanoides clade. In the reconstruction based differ in resolution and in the statistical support of par- on trnS-F these three unispecific clades are found in ticular clades. In somewhat better resolved reconstructions polytomy, while in the atpB-based reconstruction the inferred from ITS, trnSF and rpl16 Baldwiniella kealeensis, Anomodon attenuatus clade occupies a sister position to Leucodon sciuroides, Dozya japonica, Prionodon densus, the Homalia trichomanoides clade, and their joined clade Cryphaea amurensis and Dendroalsia abietina split in the is sister to the A. giraldii clade. Finally, the clade of basal portion of the trees forming grades or unsupported Herpetineuron occupies an isolated position in reconstruc- clades, while in reconstructions inferred from nad5 and tions inferred from trnS-F and atpB, but forms a well-sup- AtpB sequences these species are found in polytomy with ported clade with the Thuidiaceae clade in the ITS-based other major lineages of pleurocarpous mosses. The latter reconstruction, and shows ambiguous affinity with the core comprises a suite of more or less well defined and sup- Anomodon clade in the nad5-based reconstruction. ported lineages, corresponding to Lembophyllaceae In most reconstructions inferred from the single gene (Isothecium myosuroides, Lembophyllum divulsum, datasets the species placed in the genus Heterocladium Dolichomitriopsis diversiforme), Heterocladiaceae s.str. form two compact highly supported clades, 78 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

Fig. 1. Bayesian tree based on nuclear ITS sequences. Posterior probabilities are shown at branches to the corresponding node. On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 79

Fig. 2. Bayesian tree based on plastic trnS–F region sequences. Posterior probabilities are shown at branches to the corresponding node. 80 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

Fig. 3. Bayesian tree based on plastic rpl16 region sequences. Pos- terior probabilities are shown at branches to the corresponding node. On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 81

Fig. 4. Bayesian tree based on plastic atpB–rbcL region sequences. Posterior probabilities are shown at branches to the corresponding node. 82 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

Fig. 5. Bayesian tree based on mitochondrial nad5 region sequences. Posterior probabilities are shown at branches to the corresponding node. On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 83

Fig. 6. Bayesian tree based on concatenated organellar sequences (trnS–F, rpl16, atpB–rbcL and nad5). Posterior probabilities are shown at branches to the corresponding node. 84 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

“Heterocladium s.str.” (H. heteropterum, H. wulfsbergii The first is the unexpected position of some Anomodon & H. macounii) and the Heterocladium dimorphum clade species within the Neckeraceae, which usually have (H. dimorphum & H. procurrens). Only the topology smooth laminal cells, rarely bulging mammillosely (in based on the rpl16 sequences places these clades sister to some species of Thamnobryum), and very rarely each other, though their affinity is not supported statisti- unipapillose (Homaliodendron papillosum), but never cally, while in reconstructions inferred from the ITS and multipapillose. The second is the incongruent position atpB sequences the Heterocladium s.str. grouping forms a of some species, especially Anomodon longifolius and poorly supported clade with the Lembophyllaceae. More- Heterocladium dimorphum in trees inferred from the over, in the ITS-based topology, the weakly supported joint nuclear ITS and organellar markers (Figs. 1-6). The third clade containing Heterocladium s.str. & Lembophyllaceae is the position of Herpetineuron distant to the forms a moderately supported clade with Neckeraceae s.str. Anomodontaceae. (Neckera, Alleniella & Forsstroemia), sister to The arrangement of the outgroup taxa was essentially Nogopterium. This topology conflicts with those obtained the same in all analyses, more or less corresponding to from the rpl16 and nad5 sequences, where the clade con- numerous previously published trees (e.g. Ignatov et al., taining Neckeraceae s.l. (including Anomodon attenuatus 2007; Cox et al., 2010; Huttunen et al., 2012), and there- and A. giraldii but without Lembophyllaceae and fore we skip discussion of this basal part of the tree in Heterocladium s.str.) is highly supported. The topology general, with the exception of Herpetineuron, which is of the trnS-F and nad5 based trees are not informative currently placed in the Anomodontaceae (Granzow-de la on the affinity of the two Heterocladium lineages. Cerda, 1997, 2014; Goffinet et al., 2009; Frey & Stech, Molecular phylogenetic analysis: concatenated 2009). Thus, the following discussion is subdivided into organellar dataset analysis sections dealing with the Anomodontaceae, The topology of the concatenated organellar dataset Heterocladium and Herpetineuron respectively. mostly corresponds to the single gene-based organellar Family Anomodontaceae and the position of Ano- topologies considered above, but is better resolved and modon attenuatus and A. giraldii better supported statistically. All the target groups except Anomodon Herpetineuron toccoae are found in the highly statisti- The polyphyly of found in the present cally supported “Anomodontaceae s.l. & Lembophyllaceae molecular phylogenetic analysis may appear extreme, Anomodon attenuatus A. giraldii & Orthostichellaceae & Neckeraceae s.l. clade”; the former especially with and Anomodon does not group with any other lineages included in the deeply nested in the Neckeraceae. Although Neckera present dataset. The highly supported Anomodontaceae was originally segregated from (Hooker & Tay- clade comprises clades corresponding to (1) Anomodon lor, 1818), at that time the pleurocarp genera were very s.str. (generitype A. viticulosus) excluding A. thraustus; different from their modern circumscriptions. The famil- (2) A. thraustus; (3) Haplohymenium; (4) Anomodon ial classification of pleurocarps took shape in the mid rugelii & A longifolius. The Anomodon s.str. clade lacks XIX century and from the beginning papillose leaf cells statistical support and distinctiveness (branch length), re- were evaluated as a character of great weight: Schimper sulting in the separation of A. thraustus, while the first segregated Leskeaceae (Schimper, 1856), and shortly Anomodon Haplohymenium clade is well delineated and supported; after that Thuidiaceae (Schimper, 1860a). was clade 4 is moderately supported. The clades of Anomodon placed in Leskeaceae in the former publication of attenuatus and A. rugelii are found nested in the Schimper, but not transferred to Thuidiaceae. This was Neckeraceae, as in all single gene-based reconstructions; later done by Fleischer (1923) and Brotherus (1925), and Anomodon attenuatus forms a moderately supported clade most authors of 20th century (Podpera, 1954; Smith, with Homalia trichomanoides, and this clade is sister to 1978; Crum & Anderson, 1981) followed this placement A. giraldii. The two clades of Heterocladium are not im- until the publication of Buck & Vitt (1986). The latter mediately related: The Heterocladium s.str. clade is found authors crucially revised the whole pleurocarpous moss Anomodon in an unsupported sister position to the Lembophyllaceae system, and among other changes placed not with nested Nogopterium, and their joint clade occupies a only in its own family Anomodontaceae (originally seg- sister position to Neckeraceae s.l., with high statistical sup- regated by Kindberg (1897) but disregarded for almost a port, while the Heterocladium dimorphum clade is split century), but also in the order Leucodontales, whereas on the previous node. To a large extent, the topology ob- Thuidiaceae and Leskeaceae were referred to the tained for Heterocladium s.str., Lembophyllaceae and the Hypnales. Most subsequent floras and checklists accepted Heterocladium dimorphum group resembles that inferred the family Anomodontaceae. Buck & Vitt (1986) included Anomodon, from the ITS-based reconstruction, but they differ in the in Anomodontaceae the genera Haplohymenium, Herpetineuron, Lindbergia, Myurella position of the Neckeraceae and Nogopterium. , and Thelia, united mostly by their papillose laminal cells. DISCUSSION Their placement in other families has already been men- The present analysis has revealed or confirmed three tioned, and the position of Herpetineuron will be dis- facts that are new or have not been adequately discussed. cussed below. On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 85

Granzow-de la Cerda (1997) published a thorough and thus we refrain from confirming or rejecting it; more- worldwide revision of Anomodon (incl. Haplohymenium) over, this rare species never occurs with sporophytes in and Herpetineuron, applying cladistic methodology based Russia (Czernyadjeva & Ignatova, 2019). on morphology. He submerged Haplohymenium into a These distinctions help to explain the strange posi- section Haplohymenium of Anomodon, along with sect. tion of subgen. Pseudanomodon in the Neckeraceae, Anomodon and the newly described monospecific sect. namely in a supported clade with Homalia, as already Thraustus. More importantly, the genus Anomodon was mentioned by Tsubota et al. (2002) and Olsson et al. subdivided in two subgenera; the first, subgen. (2009a). The Neckeraceae as a whole, and Homalia in Anomodon, included the three sections just mentioned, particular, have a sharp differentiation between creeping while the second, subgen. Pseudanomodon Limpr., in- stoloniform “primary stems” and pinnately branched sec- cluded A. attenuatus, A. giraldii, A. longifolius and A. ondary stems. The presence of papillae in the leaf cells rostratus. Thus, Granzow-de la Cerda (1997) accepted makes Anomodon quite an odd member of the the latter subgenus with almost the same circumscrip- Neckeraceae; however. the ‘Pinnatella-lineage” of the tion as Limpricht (1895), adding only the East Asian A. Neckeraceae (Olsson et al., 2009a) includes giraldii. Homaliodendron papillosum, a moss with distinctly Limpricht (1895) was the first author who found unipapillose laminal cells. We failed to include material Anomodon heterogeneous in its current circumscription, of it in our own study, but the nad5 sequence from and he subdivided it into two subgenera (although with- GenBank points towards a considerable similarity with out a definite indication of rank). Subgen. Anomodon attenuatus and A. giraldii (cf. Fig. 5). Pseudanomodon (‘Pseud-anomodon’) included A. Summing up, there is no alternative to the placement attenuatus, A. longifolius and A. rostratus, while A. of two latter species in a separate genus within the viticulosus, A. rugelii, and A. (Haplohymenium) triste Neckeraceae, and raising the subgenus Pseudanomodon formed subgen. ‘Euanomodon’. The difference between to generic level is obviously a preferable solution. these subgenera included: the presence vs. absence of a Pseudanomodon (Limpr.) Ignatov & Fedosov, stat. neck with an air space in the lower part of the capsules; nov. – Basionym: Anomodon [unranked] Pseudanomo- mostly acuminate vs. broadly rounded leaf apices; and don (‘Pseud-Anomodon’), Laubm. Deutschl. 2: 774. elongate and smooth vs. mostly isodiametric and papil- 1895. Lectotype (selected by Granzow-de la Cerda, 1997): lose cells of the perichaetial leaves. Although A. Anomodon attenuatus (Hedw.) Huebener. attenuatus was characterized as a somewhat atypical member of the subgenus (the leaf is broadly acute), Species included: Granzow-de la Cerda (1997) selected this species as the Pseudanomodon attenuatus (Hedw.) Ignatov & type of Pseudanomodon. He also found other important Fedosov, comb. nov. – Basionym: Leskea attenuata distinctions in the branching pattern between Anomodon Hedw., Sp. Musc. Frond. 230. 1801. subg. Pseudanomodon and Anomodon s. str. (obtuse- Pseudanomodon giraldii (Müll. Hal.) Ignatov & leaved species related to A. viticulosus): only the species Fedosov, comb. nov. – Basionym: Anomodon giraldii of Pseudanomodon have a truly “Isobryalean” branch- Müll. Hal., Nuovo Giorn. Bot. Ital., n.s. 3: 117. 1896. ing architecture, i.e. have a clearly defined stoloniform Diagnosis: Plants rather large, yellowish green. Pri- “primary stem” giving rise to the secondary stems with mary stem creeping, without central strand, stoloniform, much larger leaves and pinnate branching, contrary to proximal branch leaves broad (wider than long); second- the main stem of, e.g., A. viticulosus, albeit creeping and ary stems with much larger leaves, arcuate, attenuate, with smaller leaves, but having simple branches which pinnately branched, foliage subcomplanate; leaves ligu- never subdivide extensively. According to Granzow-de late, broadly acute, entire or with a few teeth near apex; la Cerda (1997), this difference is clearly correlated with costa ending shortly below apex; laminal cells moder- another character, the central strand, which appears to ately to sparsely papillose, papillae not pedicellate. Ga- be absent in subgen. Pseudanomodon and also metangia only on old axes. Perichaetial leaves with Haplohymenium; however, the latter genus is character- smooth or slightly papillose cells of elongate shape. Cap- ized by much smaller plants with thin stems, and ac- sules symmetric, cylindrical, with neck. Annulus not dif- cordingly may lack a central strand for that reason. In ferentiated; operculum obliquely short-rostrate. Exostome addition, Granzow-de la Cerda (1997) found the posi- teeth striolate proximally, finely papillose distally. tion of the perichaetia in Anomodon attenuatus and A. Endostome with segments about as long as teeth, cilia giraldii to be confined to older parts of the plants and reduced or occasionally developed, short. Spores small. never present beyond the last branching point. This char- Calyptra smooth. acter never occurs in other core Anomodon species and The original description of the subgenus Pseudano- Haplohymenium, with the exception of Haplohymenium modon included also A. rostratus and A. longifolius. The sieboldii. However, the free branching of the latter spe- former species was found nested in a clade of Claopodi- cies makes evaluation of this character rather difficult, um (Gardiner et al., 2005), and accordingly was placed 86 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

μ 5 μm 5 μm A A’

5 μm 5 μm B B’

10 μm 3 μm C C’

10 μm 5 μm D D’

Fig. 7. Laminal cell papillae (SEM images from dry herbarium material [ABCD] and material dried at critical point [A’B’C’D’]): A: Anomodon viticulosus (MHA9001940); B: Anomodontopsis rugelii (MHA9001791); C: Pseudanomodon attenuatus (Ukraine, Voronkova, 11.XI.2018, MHA); D: Pseudanomodon giraldii (MHA9001740). On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 87

10 μm μ μ A 10 m B 10 m C

μ 5 m 10 μm D E

10 μm 10 μm 10 μm F G H

μ 10 μm 10 m I J

10 μm 5 μm 10 μm K L M

10 μm 10 μm 10 μm

N O P Fig. 8. Lamina cell papillae of species previously referred to Anomodon s.l. A–C, K, N–P: Anomodontopsis rugelii (MHA9001791); D, L: Anomodon viticulosus (MHA9001940); E: Haplohymenium triste (MW9090494); F–H, M: Pseudanomodon attenuatus (Ukraine, Voronkova, 11.XI.2018, MHA); I–J: P. giraldii (MHA9001740). See also Fig. 7. CLSM images. 88 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV in that genus (Ignatov et al., 2006). Anomodon longifo- case is observed in Haplohymenium longinerve lius will be discussed in more detail below. (Czernyadjeva & Ignatova, 2019). Closer to the leaf mar- The two species referred here to Pseudanomodon form gin (Fig. 9C, D) and just above the smooth basal cell a clade in ITS and rpl16, whereas in the concatenated area (Fig. 9F) the multipapillosity of Anomodon solovjovii dataset and in atpB-rbcL analyses Homalia trichomanoides is especially apparent. appears to be closer to P. attenuatus than to P. giraldii. We Granzow-de la Cerda (1997) included do not intend to give a detailed analysis of this puzzling Haplohymenium in Anomodon subgen. Anomodon, as a situation; a detailed discussion was promised some time separate section. It seems that this decision was quite ago by Olsson et al. (2009a), and presumably will appear adequate for his study, in demonstrating that as a comprehensive special study. It seems worthy men- Haplohymenium is much closer to Anomodon than to tioning that in the same Pinnatella-clade Enroth et al. Pseudanomodon and Claopodium rostratum. However, (2010) revealed a species more similar to Homaliadelphus as Granzow-de la Cerda did not put his study in the than to Pinnatella and any related genera. broader context of pleurocarp systematics at familial level, Among the additional characters differentiating both any recognition that these taxa did not belong to species of Pseudanomodon from the Anomodontaceae Anomodon at all was impossible. The data available now (Anomodon and Haplohymenium) is the much better de- are rather in favor of the recognition of Haplohymenium veloped endostome. as a separate genus. It has a distinct morphology and its At the same time, we must note a considerable differ- clade is situated on a long branch and has maximal sup- ence in the proximal branch leaves, which are compound port in most analyses (Figs. 1-6). The only odd topology (sensu Ignatov & Spirina, 2012) in P. giraldii, and much was found in rpl16, where Anomodon minor fell within more similar to some Neckeraceae (Spirina & Ignatov, the Haplohymenium longinerve clade, which we cannot 2015), while P. attenuatus has proximal branch leaves explain based on the present limited sampling. However, similar to Anomodon (Figs. 12–13). The papillae in Pseu- the independent status of the genus Haplohymenium re- danomodon are different from the massive papillae of quires a fuller discussion, with decisions regarding the Anomodon (Fig. 8), which was noted by Granzow-de la statuses of Anomodon longifolius and A. rugelii. Cerda (1997), who also pointed out that the papillae in Anomodon longifolius was referred to P. giraldii and P. attenuatus are quite different. As shown Pseudanomodon (as a subgenus) by both Limpricht in Fig. 8, P. attenuatus has rather thin cell walls and (1895) and Granzow-de la Cerda (1997), though shar- small papillae which are occasionally forked, while the ing only a few characters with A. attenuatus and A. papillae in P. giraldii are more scattered, always simple, giraldii: the presence of flagelliform branches, the ab- and the dorsal and ventral cell surfaces are thickened. In sence of perichaetia beyond the point of last branching Anomodon and Haplohymenium the cell outlines are con- (although in A. longifolius only thin branches occur on vex, thus the outlines of the dorsal and ventral surfaces the stem distally from the perichaetia), and elongate cells are crenate, while they are plane in both of the Pseuda- in the perichaetial leaves. The papillae of Anomodon nomodon species. longifolius are different from the core species of A new circumscription of the genus Anomodon and Anomodon, Pseudanomodon, and probably from any family Anomodontaceae other pleurocarp (Figs. 10). Higher magnification of moist leaf cells shows that the papillae are not centered over The controversial topologies inferred from the analy- the cell lumen, as is usually assumed, but paired. SEM ses of different DNA regions obviously cannot be fol- images taken from young leaves (Fig. 10A, B) and from lowed literally and require a compromise solution. dry herbarium material (Fig. 10C, D), show the papillae The core group of Anomodon, i.e. A. viticulosus, A. of two neighboring cells originating from the wall be- minor, A. thraustus, A. abbreviatus and A. solovjovii form tween these two cells (sometimes a longitudinal, some- a maximally supported clade in most analyses, and only times a transverse one). In the dry state (Fig. 10C, D), a few comments regarding the two latter species are the papillae are inclined towards the center of the lumen needed. Their laminal cells have papillae of a very un- and their tips cover the concavities that appear as a re- usual shape (Fig. 9) among other Anomodon. Iwatsuki sult of cell drying. (1963) segregated them in a separate section, whereas The proximal branch leaves of Anomodon longifolius Granzow-de la Cerda (1997) lowered their status to are narrow and occasionally compound, sometimes simi- subsectional. The present molecular phylogenetic results lar to those in Anomodon rugelii and Heterocladium showed only a slight segregation, thus supporting the dimorphum and related species, while they are broad in latter view. Although appearing very peculiar, the cells Anomodon, Haplohymenium and Pseudanomodon (Figs. in A. abbreviatus and A. solovjovii are in fact 12). pluripapillose, i.e. the same as in other core Anomodon The peristome of Anomodon longifolius differs strongly species, although one papilla “branch” overtops the oth- from the peristomes of core Anomodon: its exostome teeth ers and in most parts of the leaf each cell has one papilla are relatively narrow, transversely striolate below, longi- much larger than the rest (Fig. 9). A somewhat similar On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 89

20 μm 10 μm A B

20 μm 10 μm C D

10 μm 10 μm E F Fig. 9. Anomodon solovjvii (MW9001945): papillae shown in CLSM (A, C, E) an SEM (B, D, F) images. A, B: subapical part of leaf; C: lower part of on leaf; E: transverse leaf section. 90 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV tudinally striolate to prominently papillose above, and The acceptance of Haplohymenium however implies finely papillose on the inner surface, whereas in core the necessity of separating Anomodon rugelii. In most Anomodon the teeth are massive, smooth below on the trees it keeps a position sister to the clade of Anomodon outer surface and indistinctly papillose above (Figs. 14). s. str. + Haplohymenium (Figs. 1, 2, 4) or forms a clade The position of Anomodon longifolius in ITS trees in with Anomodontella (Fig. 6). the Neckeraceae–Lembophyllaceae–Echinodiaceae– Iwatsuki (1963) suggested its segregation in a sepa- Ortostichellaceae clade, and in some analyses sister to rate section, i.e. at the same level as Anomodontella. The Heterocladium dimorphum (albeit with very low support), phylogenetic analysis by Granzow-de la Cerda (1997) and its basalmost position in organellar trees (or sister to did not find sufficient morphological distinction in A. A. rugelii, both keeping a basa-l position in this case) rugelii, although the author acknowledged its unique indicate the necessity of excluding A. longifolius from auriculate leaf base (Fig. 11), the compound proximal the genus Anomodon. Therefore it is separated here in branch leaves (“pseudoparaphyllia present” in his termi- its own genus. Its familial placement requires further nology), and the golden to rusty color of the costa. study, but for now, in a view of the topologies of the Additional characters distinguishing A. rugelii from organellar trees, we retain it in the Anomodontaceae. the core Anomodon species include narrow peristome Anomodontella Ignatov & Fedosov, gen. nov. teeth, with the plates markedly narrower than the trabe- culae and papillose on both surfaces, and also the apicu- Anomodontella longifolia Type species: (Schleich. late leaf apex. The latter character is not present in every ex Brid.) Ignatov & Fedosov, comb. nov. – Basionym: leaf, and Granzow-de la Cerda (1997) wrote that it is Pterigynandrum longifolium Schleich. ex Brid., Muscol. unreliable, although even its occasional presence is im- Recent. Suppl. 4: 128. 1819[1818]. Monospecific genus. portant, as it never occurs in Anomodon s. str. However, Etymology Anomodon. : deminutive of an apiculus occurs in Haplohymenium, being especially Diagnosis Anomodontella : differs from other conspicuous in H. triste, although similarly not in every Anomodontaceae in: laminal cells unipapillose on both leaf and every shoot. surfaces, with papillae on the ventral surface more promi- Therefore we segregate A. rugelii in its own mono- nent than on the dorsal, and from all other pleurocarps specific genus. in the paired, “geminate” arrangement of the papillae; compound proximal branch leaves (occurring in Anomodontopsis Ignatov & Fedosov, gen. nov. Anomodontaceae only in A. rugelii); long acuminate Type species: Anomodontopsis rugelii (Müll. Hal.) leaves; smooth and elongate cells in perichaetial leaves; Ignatov & Fedosov. – Basionym: Hypnum rugelii Müll. exostome teeth striolate on outer surface in proximal half Hal., Syn. Musc. Frond. 2: 473. 1851. and highly papillose distally. Etymology: alluding similarity to the genus Additional differentiating features of Anomodontella Anomodon. are the very loose tufts composed of numerous attenuate, Diagnosis. Similar to Anomodon in the broadly flagelliform branches (similar in habit to Heterocladium), rounded leaf apex and leaf shape, but differs in the com- and the dark to yellow-green color of the plants, not glau- pound proximal branch leaves, and the auriculate leaf cous as in most Anomodon and Haplohymenium species. base, as well as in molecular data (Figs. 1–6). Such a color is not unique in the Anomodontaceae, oc- Additional characters: North American, European and curring e.g. in Haplohymenium flagellare and H. West Asian plants are dark green to rusty brown, which longinerve. alone allows the species to be recognized in the field. In * * * East Asia there are probably two infraspecific taxa, one The species closer to A. viticulosus than of which was recognized by Iwatsuki as A. rugelii var. Anomodontella longifolia from three groups: (1) ferrugineus (Besch.) Z. Iwats. However, this form is the Anomodon s. str. (A. viticulosus, A. minor, A. thraustus); same as plants from America, from where A. rugelii was (2) Haplohymenium species; and (3) the monospecific described. Also in the Russian Far East there is another clade of Anomodon rugelii (or, in some trees forming a form of A. rugelii, which is slightly different molecu- clade with A. longifolius). One of the possible taxonomic larly and has more or less glaucous shoots, less different solutions is to lump all the species in the genus from species such as A. viticulosus and A. thraustus; in Anomodon, following Granzow-de la Cerda (1997). At such plants the leaves are contorted, but not so conspicu- the same time, the acceptance of Haplohymenium at ge- ously incurved as in North American and European neric level seems to us reasonable: these much smaller plants. Granzow-de la Cerda (1997) found transitions plants with papillose and hairy calyptrae are well delim- and did not recognize these forms at all. Further molecu- ited and form a highly supported clade in most analyses. lar studies with expanded sampling may reveal that in This unity is somewhat surprising, as Haplohymenium East Asia there are two taxa of Anomodontopsis. includes plants highly polymorphic in papillae structure Description: Plants medium-sized, in rather dense (representing essentially most types known in Anomodon mats, dark green, brownish or, in some populations, some- in its new circumscription). what glaucous-green. Stems erect-ascending, weakly ir- On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 91

10 μm 10 μm A B

10 μm 10 μm C D

20 μm 20 μm E F Fig. 10. Anomodontella longifolia (MHA9001614) A–D: SEM images from herbarium material after drying under critical point (A–dorsal, B–ventral) and just dried (C, D), showing paired papillae “above neighboring cell lumens” originated from the wall between these two cells; E–F: CLSM images of leaf, showing Ï papillae in many cases near the cell wall, which is a result of the latest cell disvision (cf. scheme on the right below, where line 10 μm thickness corresponds to order of cell wall origin, as described in G e.g. Frey, 1970 and Donskov, 2015). G: transverse leaf section. 92 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

10 μm 30 μm A B Fig. 11. Auriculate leaf bases of Anomodontopsis rugelii (MHA9001791); the marginal cells are multipapillose, although they may appear unipapillose at margin (A: CLSM; B: SEM). regularly branched, central strand differentiated; proxi- unclear (it is not indicated in Tropicos, accessed on 19 mal branch leaves compound; rhizoids often abundant. May 2019). Different authors have reported one or other Branch leaves in dry state contorted and often incurved, of the two species as the type: H. dimorphum was men- when wet erect-spreading to subcomplanate, broadly ob- tioned as the type of the genus by Watanabe (1972) and long-ligulate, conspicuously auriculate, with auricles Ignatov & Ignatova (2004), whereas Grout’s (1928) typi- papillose on the side facing the stem; margins plane, al- fication, supposedly the earliest one, was with H. most entire; apex broadly rounded or occasionally apicu- heteropterum (cf. also Enroth et al., 2019). For a long late; costa strong, pellucid, white or with golden to rusty time the genus was placed in the Thuidiaceae (Fleischer, pigmentation, ending shortly below apex, often flexuose, 1923; Brotherus, 1925), but later Buck & Crum (1990) sometimes with lateral offshoots and forked at apex, epi- suggested transferring it to the Pterigynandraceae (along dermal cells smooth; laminal cells isodiametric, small, with Myurella, Habrodon, Iwatsukiella and thick-walled, with high, usually pedicellate papillae on Leptohymenium), where it is accepted in some recent both surfaces, basal juxtacostal cells elongate, pellucid, publications (Magill, 2014). smooth, occupying half of leaf width. Dioicous. The early analysis of Gardiner et al. (2005) showed Perichaetia at ends of terminal secondary branches; that Heterocladium was unrelated to the Thuidiaceae, perichaetial leaves from broad base abruptly constricted where it was traditionally placed, but at the same time to narrowly lanceolate apex, laminal cells papillose. Cap- without any apparent affinity. Thus Ignatov & Ignatova sule exserted on a long seta, symmetric, cylindrical. An- (2004) segregated it in a family Heterocladiaceae. Lim- nulus persistent; operculum obliquely short-rostrate, ited sampling did not allow any further splitting, so de- exostome teeth papillose or indistinctly striolate proxi- spite low support all the species were assumed to form mally, endostome with short basal membrane, segments one lineage. Most subsequent analyses have separated short, irregular or absent. Spores small, 9–14 ìm. Ca- the Heterocladium species in two different clades, and lyptra smooth. Capsules mature in mid-autumn. Heterocladium s. str. (the species grouped around H. The other species of the genus currently accepted in heteropterum) has usually been placed within the the Tropicos database all belong to the genus Anomodon Neckeraceae or Lembophyllaceae or between them in a s. str.: A. dentatus C. Gao is accepted by Granzow-de la grade (cf. Enroth et al., 2019), while the species related Cerda (1997) and Wu et al. (2002), Anomodon to H. dimorphum were usually in a more distant posi- perlingulatus Broth. ex P.C. Wu & Y. Jia is accepted by tion. Wu et al. (2002), while Anomodon rotundatus Paris & The family has been accepted in some floras, e.g. by Broth. was tentatively synonymized with A. thraustus (Wu Hedenäs et al. (2014), but recently it was pointed out et al., 2002) and A. grandiretis Broth. was placed into that the earlier name Heterocladiaceae Decaisne for a synonymy with Anomodon minor (Wu et al., 2002). family of red algae has been overlooked (Enroth et al., Taxonomy of the genus Heterocladium 2019). This family is based on the genus Heterocladia Nageli, which is still in current use and therefore the Heterocladium The genus Bruch, Schimper & W. name cannot be a subject for conservation. H. dimorphum Gümbel was described for two species, The present analyses of different loci resulted in some- H. heteropterum and , but the type species of the genus in what different topologies regarding the position of these On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 93

30 μm A 3

30 μm 20 μm C D 3

50 μm B 2

1 2

1 10 μm μ 30 μm 30 μm 20 μm E F G

3 3 3

4 2 2

1 2 1 μ 30 μm 30 μm 100 μm H I J Fig. 12. Proximal branch leaves of A, B: Anomodon viticulosus (MHA9001940), C: Anomodon thraustus (MHA9002034), D– E: Haplohymenium longinerve (MHA9035366), F–G: Anomodontopsis rugelii (MHA9001791), H–J: Anomodontella longifolia (MHA9001614). Numerals in figures D, G, H, I denote number of compound branch leaves or their parts (cf. Berthier, 1971; Spirina & Ignatov, 2008, 2015). (C, D, H: CLSM; A, B, E–G, I, J: SEM). two groups of Heterocladium. The ITS and atpB analy- Lembophyllaceae to Neckeraceae, between the core clade ses resolve Heterocladium s.str. in a clade with the of the Neckeraceae and the “Pinnatella-clade”. It seems Lembophyllaceae; rpl16 shows the same, but in this case that the position of Heterocladium in the the H. dimorphum clade is found sister to the Lembophyllaceae would be the best solution in the present Heterocladium s.str. clade. The analysis of trnS-F found state of knowledge. the Heterocladium s.str. clade in the grade from The similarity in morphology between Heterocladium 94 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

100 μm B

50 μm A

50 μm D 30 μm C

30 μm 100 μm E F Fig. 13. SEM images of proximal branch leaves of Pseudanomodon attenuatus (A, C, E from Ukraine, Voronkova, 11.XI.2018, MHA) and P. giraldii (B, D, F, from MHA9001740). The branch buds of the former species are similar to those of most pleurocarps, including Anomodon s.str. in having broad proximal branch leaves tightly covering the branch apical cell, whereas in P. giraldii the outermost proximal branch leaves are compound, as in many neckeraceae and related families (cf. Spirina & Ignatov, 2015). On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 95

30 μm 100 μm A B

10 μm C 10 μm D

10 μm E 100 μm F

10 μm G Fig. 14. Peristomes of Anomodontella longifolia (A, C, E, G), Anomodon viticulosus (B, D) and Anomodon thraustus (F, 30 μm H). SEM images. H 96 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

100 μm A

Fig. 15. Peristome of Anomodontopsis rugelii (MHA9001791): general view (A) and close up of teeth, showing papillose dorsal surface. SEM. 20 μm B s. str. and core Lembophyllceae (Tangney, 1997; Quandt tinctly differentiated, erect to spreading, ovate, broadly et al., 2009) is not very high; however, some other mar- acute. Dioicous. Capsule horizontal, short-cylindrical, ginal groups which have been referred to the family based curved. Operculum conic-apiculate. Peristome perfect, on molecular phylogenetic inference have likewise not cilia long. Spores small. much in common with the core of the family, e.g. Heterocladiella Ignatov & Fedosov, gen. nov. Nogopterium and Mawenzhangia (Enroth et al., 2018). Heterocladiella dimorpha Multipapillose laminal cells, especially conspicuous in Type species: (Bridel) Hypnum H. macounii, would be odd in the new circumscription Ignatov & Fedosov, comb. nov. – Basionym: dimorphum of the family; it may be inconvenient, but the loss of the Brid., Muscol. Recent., suppl. 2: 149. 1812. Heterocladiella procurrens “smooth laminal cell” character from the diagnosis of Species included: (Mit- the Lembophyllaceae has so much in parallel with the ten) Ignatov & Fedosov, comb. nov. – Basionym: Pterogonium procurrens case of Pseudanomodon that it is already not surprising. Mitt., J. Linn. Soc., Bot. 8: 37. Note that in contrast to the Anomodontaceae, the papil- 1864. Description lae in Heterocladium occur only on the dorsal leaf sur- : Leaves spreading to erect-appressed face, as in the Thuidiaceae and Leskeaceae. when dry, erect-spreading when moist; stem leaves to 1 mm; margins serrate to serrulate; apex acute; costa usu- * * * ally double and short to just below mid leaf; laminal cells The position of the Heterocladium dimorphum group papillose, papillae single, in distal end of cell; basal cells is more indefinite. It forms clades with Anomodontella smooth. in the ITS tree (with low support, Fig. 1) and with Differentiation: The morphological distinction be- Heterocladium in the rpl16 analysis (Fig. 3), but more tween Heterocladiella and Heterocladium includes (1) commonly keeps a separate position in polytomy or grade branching pattern: more or less regularly unipinnate in near Ortostichellaceae, Echinodiaceae, Lembophyllaceae Heterocladiella and strongly to moderately irregularly and Neckeraceae (Figs. 2-6), being in most cases maxi- repeatedly branched in Heterocladium; (2) always smooth mally supported. Considering such genetic differentia- stem cells in Heterocladiella vs. occasionally papillose tion, we suggest segregating the H. dimorphum-group of in Heterocladium; (3) laminal cells smooth to multi- species in a separate genus and family. papillose on dorsal surface in Heterocladium vs. smooth Heterocladiellaceae Ignatov & Fedosov, fam. nova to unipapillose on dorsal surface in Heterocladiella; (4) Monogeneric family, type: Heterocladiella Ignatov leaves appressed at their bases and then reflexed to squar- & Fedosov rose in Heterocladiella vs. leaves somewhat spreading Diagnosis. Stems rather regularly pinnately branched, from stem at their bases in Heterocladium. Hedenäs & densely foliate; central strand present; epidermal cells Bisang (2011) found that species of Heterocladiella have smooth; paraphyllia absent, proximal branch leaves of- both large and dwarf males, whereas dwarf males in ten compound. Stem leaves squarrose, from broadly ovate, Heterocladium s. str. have not been observed. appressed base tapered to triangular acute acumen, * * * broadly decurrent; margins serrate to serrulate; costa According to the Tropicos database (accessed 2 May short, double; laminal cells quadrate to rhomboidal, on 2019), there are nine species of the genus currently ac- dorsal surface with a massive papilla closer to distal end cepted. Two are referred here to Heterocladiella, and none of cell, on ventral surface smooth. Branch leaves dis- of the other species accepted by Tropicos belong to this On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 97

20 μm A

30 μm B

10 μm C

30 μm D

10 μm E

50 μm 30 μm F G

Fig. 16. Heterocladiella dimorpha (MW9043335): Leaf surface (A and C dorsal, and E ventral) and incised and compound proximal branch leaves of (B, D, F, G). 98 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

Ô 32 20 μm A

20 μm B 20 μm C

20 μm D

30 μm E

10 μm F Fig. 17. A–F: Heterocladium macounii (SEM, from Califor- nia, Ignatov & Norris 8.VIII.1989, MHA) and G: H. heteropterum (CLSM, from MHA9033935), showing papillose leaf and stem surfaces and incised to compound proximal branch 20 μm leaves (in C: also scars of broken parts of compound proximal banch leaves (arrowed). G On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 99 genus. Three sequenced species of Heterocladium (H. veloped leaves (Donskov, 2015). We don’t know of any macounii, H. wulfsbergii, H. heteropterum) were found other moss whose ontogeneric sectors are so clearly ap- to be monophyletic in most analyses. According to their parent. Our tentative explanation of this expression is species descriptions Heterocladium angustifolium that the repeated leaf incurvation requires reliable joints, (Dixon) R. Watan., H. capillaceum Broth. ex Ihsiba, H. and the ontogenetic sectors in Herpetineuron are con- pilicuspis Broth. ex Ihsiba and H. tenellum Deguchi & nected by efficient joints (e.g. Figs. 18L, N), often asso- H. Suzuki belong to Heterocladium s. str. ciated with papilla-like thickening (Figs. 18M, P). Note Systematic position of Herpetineuron that in addition to incurved leaf margins, the leaves of Herpetineuron in the dry state are also incurved along The grouping of Herpetineuron with Anomodon was their length. suggested by Brotherus (1907, 1925), who placed these * * * genera in Anomodontoideae (one out of four subdivi- sions of the Thuidiaceae). Subsequent authors placed it The occurrence of papillae and their structural in the Thuidiaceae, e.g. Watanabe (1972), Crum & Ander- variation within phylogenetic lineages son (1981), Noguchi (1991). Buck & Vitt (1986) resur- The present study found mosses with papillose laminal rected the Anomodontaceae, including Herpetineuron and cells in two families where they were either unknown some less closely related genera (discussed above). (Lembophyllaceae) or extremely rare (Neckeraceae). Granzow-de la Cerda (1997) provided a revision of Ano- It seems that the taxonomic value of papillae on the modon and Herpetineuron, but he avoided discussion of leaf lamina has been strongly overestimated in moss sys- the family-level taxonomy. tematics. Some genera or species with papillose laminal Thus, no justification of the close relationship between cells, previously placed in various families based on this Herpetineuron and Anomodon has ever been put forward. character, have already been found to have different af- The molecular phylogenetic analysis (based on rbcL) of finities, like Myurella in the Plagiotheciaceae, while some Tsubota et al. (2004) supported this position, whereas other groups, e.g. Claopodium, actually a relative of the analysis of Cox et al. (2010) (based on rps4 and nad5) Brachytheciaceae, are still awaiting a final verdict. The did not. Not one of five studied loci supported the rela- present analysis indicated that the latter genus has no tionship of Herpetineuron with Anomodon; most mark- affinity with either Anomodon or the Thuidiaceae, where ers left Herpetineuron unresolved in the polytomy outside it was traditionally placed. the Anomodon-clade and the Neckeraceae+ Many pleurocarpous moss families include species Lembophyllaceae+ Orthostichellaceae clade, and ITS in- with cells that are prominently prorate to “dorsally pap- dicated that its closest relationship was with the illose in the distal cell end” but have not evolved fur- Thuidiaceae, with moderate support. In view of the iso- ther to a central-unipapillose or multipapillose state. lated position of Herpetineuron, usually on very long Examples are found in the Brachytheciaceae branch, which reflects its strong divergence and peculiar (Brachythecium (Bryhnia) novae-angliae), morphology, we foresee that Herpetineuron needs its own Pseudoleskeellaceae (Pseudoleskeella papillosa), family. However as sampling of the Thuidiaceae is not Amblystegiaceae (Palustriella decipiens), and sufficient in the present study, we refrain from doing this Hylocomiaceae (Hylocomiadelphus triquetrus). now, and temporarily suggest returning Herpetineuron There are genera which, in different species, develop to the Thuidiaceae. papillae at the distal end of the cell or in a central posi- Some morphological features of Herpetineuron are tion (Myurella, Haplocladium, Pseudoleskea); note that remarkable. Its leaf structure is especially outstanding in these cases (and maybe in most others) the papillae and merits a short comment here. The genus Herpetineron occur only on the dorsal leaf surface. This can lead to includes only a single species, H. toccoae (Sull. & Lesq.) two trends in the complexity in the pattern of papillae, Cardot, a widespread pantropical moss penetrating to the firstly from unipapillose to multipapillose (observed in temperate zone in the eastern sectors of both Eurasia and Claopodium and Thuidium), and secondly from dorsally North America. It grows mostly in habitats which expe- papillose to papillose on both surfaces. The latter trend rience moderately long periods of severe desiccation, re- is gradual, and papillosity on the ventral surface is often quiring the ability to incurve its leaf margins in the dry less prominent compared with the dorsal surface: it is state (Fig. 18A, B, I) and spread them after wetting. The more or less apparent in Haplohymenium (Fig. 8E). There peculiarity of Herpetineuron toccoae is an exceedingly are probably no cases where papillae are present on the conspicuous ontogenetic sector of 4 × 4, 4 × 8, and 8 × 8 ventral surface but absent on the dorsal, although some- cells throughout the leaf (Fig. 18C–H). Such sectors are times the ventral papillae may be larger than the dorsal: universal in mosses, as the moss leaf is always formed Anomodontella provides one such example (Fig. 10A, from a single cell by a number of divisions (Schimper, B, G). A quite separate case consists of papillae in the 1860b; Frey, 1970); they are usually masked by develop- corners of the ontogenetic sectors in Herpetineuron, com- mental irregularities, and far less apparent in fully de- parable with e.g. Atrichum, but rare in pleurocarps. 100 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

1 mm 50 μm 1 mm I11 I10

I9 2 1 I8

A B

50 μm I7

50 μm C I6

D 50 μm E

50 μm F 50 μm G H

0.5 mm μ I 50 m J

μ 50 m K 50 μm L μ 50 m M

50 μm μ 50 μm N 50 m O P Fig. 18. Herpetineuron toccoae (MHA9035729): A: habit, dry, B: habit, wet, C, E–H, M: different views of lamina, showing ontogenetic sectors, and thickenings in corners of these blocks (E: recently dried leaf part where an air bubble has encroached under the cover glass as the slide dried); I: three views of the same transverse leaf section, in wet, half-dry and dry states; K–N, P: leaf transverse sections, showing ontogenetic sectors of four (eight) cells, and papillae at their joints (in P); O: 3D view of leaf surface, highlighting its tetragon pattern; D: young leaf, with numbered ontogenetic sectors, I5 to I11 following Frey’s (1970) terminology. On the taxonomy of Anomodontaceae and Heterocladium (Bryophyta) 101

In general, variation in the pattern of papillosity in China and India. – Tropical Bryology 31: 67–75. https://doi.org/ genera and families is rather gradual, and the placement 10.11646/bde.31.1.12 of the multipapillose Heterocladium in the Lembophyl- ENROTH, J., J. R. SHEVOCK & M. S. IGNATOV. 2018. Mawenzhangia thamnobryoides (Bryophyta, Lembophyllaceae), a new moss genus and laceae and Pseudanomodon in the Neckeraceae (discussed species from the Shangri-la region of Yunnan Province, China. – Phy- in the present paper) looks fairly odd, and further studies totaxa 346(3): 237–246. are needed to understand what lies behind this. In any ENROTH, J., S. OLSSON, S. HUTTUNEN, V. BUCHBENDER, R. case, our knowledge of variation in papillae structure is TANGNEY, M. STECH, L. HEDENÄS & D. QUANDT. 2019. Orthos- still far from complete and future study will certainly tichellaceae fam. nov. and other novelties in pleurocarpous mosses re- The Bryologist 122 219–245. reveal many interesting details for a deeper understand- vealed by phylogenetic analyses. – , (2) : ing of pleurocarp evolution. FLEISCHER, M. 1923. Die Musci der Flora von Buitenzorg, Vol. 4. – Brill, Leiden. Pp. i–xxxi + 1105–1729. ACKNOWLEDGEMENTS FREY, W. 1970. Blattentwicklung bei Laubmoosen. – Nova Hedwigia We are indebted to Tom Blockeel for English correc- 20: 463–556. tions of the manuscript. The work on SEM was per- FREY, W. & M. STECH. 2009. Bryophyta (Musci, mosses). – In: Frey, W. formed partially at User Facilities Center of M.V. (ed.). Syllabus of plant families A. Engler’s Syllabus der Pflanzenfami- Lomonosov Moscow State University under financial lien. Part 3. Bryophytes and seedless vascular plants. 13th ed.. Gebr. Borntraeger Verlagsbuchhandlung, Stuttgart, Germany: 116–257. support of Ministry of Education and Science of Rus- GARDINER, A., M. IGNATOV, S. HUTTUNEN & A. TROITSKY. 2005. sian Federation. The molecular study of Fedosov and Fe- On resurrection of the families Pseudoleskeaceae Schimp. and Pylaisi- dorova was supported by RSF 18-14-00121, and work aceae Schimp. (Musci, Hypnales). – Taxon 54: 651–663. on specimens by Ignatov was conducted in the course of GOFFINET, B., W.R. BUCK & A.J. SHAW. 2009. Morphology, anato- institutional project (19-119012390082-6). my, and classification of the Bryophyta. – In: Goffinet, B. & A.J. Shaw (eds.). Bryophyte biology, 2nd edn. Cambridge: Cambridge Univer- LITERATURE CITED sity Press: 55–138. ARIKAWA, T., H. TSUBOTA, H. DEGUCHI, N. NISHIMURA & M. GRANZOW-DE LA CERDA, I. 1997. Revision and phylogenetic study HIGUCHI. 2008. Phylogenetic analysis of the family Hypnaceae based of Anomodon and Herpetineuron (Anomodontaceae, Musci). – Con- on rbcL gene sequences. pp. 215–225. – In Bryol. New Millennium. tributions from the University of Michigan Herbarium 21: 205–275. Institute of Biological Sciences, University of Malaya, Kuala Lum- GRANZOW-DE LA CERDA, I. 2014. Anomodontaceae. – In: Flora of North pur, Malaysia. America Editorial Committee (eds.), Flora of North America North of BERTHIER, J. 1971. Recherches sur la structure et le développement de Mexico, vol. 28. New York, Oxford University Press: 628–636. l’apex du gamétophyte feuillé des mousses. – Revue Bryologique et GROUT, A. J. 1928. Moss Flora of North America, vol. 3. – Newfane, Lichénologique. 38: 421–551. Vermont, published by Author. 277 pp. BROTHERUS, V. F. 1907. Musci. – In: Engler, A. & K. Prantl (eds.) Die HEDENÄS, L. 2017. Scandinavian Oncophorus (Bryopsida, Oncopho- Natürlichen Pflanzenfamilien I(3). Leipzig, Verlag von Wilhelm En- raceae): species, cryptic species, and intraspecific variation. European gelmann. Journal of Taxonomy 315: 1–34. BROTHERUS, V.F. 1925. Musci. – In: Engler, A. & K. Prantl (eds.) Die HEDENÄS, L. & I. BISANG. 2011. The overlooked dwarf males in mosses Natürlichen Pflanzenfamilien. 2, 11. Berlin: Verlag von Wilhelm En- – Unique among green land plants. – Perspectives in Plant Ecology, gelmann: 1–542. Evolution and Systematics 13: 121–135. BUCK, W. R. & H. A. CRUM. 1990. An evaluation of familial limits HEDENÄS, L., C. REISBORG & T. HALLINGBÄCK. 2014. Bladmos- among the genera traditionally aligned with the Thuidiaceae and sor/Bryophyta Skirmossor–baronmossor, Hookeria–Anomodon. Na- Leskeaceae. – Contributions from the University of Michigan Her- tionalnyckeln Sveriges Fl. Fauna. Bladmossor/Bryophyta. Uppsala: barium 17: 55–69. ArtDababanken, SLU. BUCK, W. R., B. GOFFINET & J. SHAW. 2000. Novel relationships in HOOKER, W. J. & T. TAYLOR. 1818. Muscologia Britannica. – Long- pleurocarpous mosses as revealed by cpDNA sequences. – The Bryolo- man, Hurst, Rees, Orme, and Brown, London. xxxv + 152 pp. gist 103: 774–789. HUTTUNEN, S., N. BELL, V. K. BOBROVA, V. BUCHBENDER, W. BUCK, W. R. & D. H. VITT. 1986. Suggestions for a new familial classi- R. BUCK, C. J. COX, B. GOFFINET, L. HEDENÄS, B.-C. HO, M. S. fication of pleurocarpous mosses. – Taxon 35: 21–60. IGNATOV, M. KRUG, O. I. KUZNETSOVA, I. A. MILYUTINA, A. CÂMARA, P. E. A. S., M. CARVALHO-SILVA, D. K. HENRIQUES, E. NEWTON, S. OLSSON, L. POKORNY MONTERO, J. SHAW, J. GUERRA, M. T. GALLEGO, D. R. POVEDA & M. STECH. M. STECH, A. V. TROITSKY, A. VANDERPOORTEN & D. QUAN- 2018. Pylaisiaceae Schimp. (Bryophyta) revisited. – Journal of DT. 2012. Disentangling knots of rapid evolution: origin and diversifi- Bryology 40(3): 251–264. https://doi.org/10.1080/ cation of the moss order Hypnales. – Journal of Bryology 34(3): 187– 03736687.2018.1472850 211. COX, C.J., B. GOFFINET, N.J. WICKETT, S.B. BOLES & A.J. SHAW. IGNATOV, M.S. & E.A. IGNATOVA. 2004. Flora mkhov srednei chasti 2010. Moss diversity: a molecular phylogenetic analysisa of genera. – evropeiskoi Rossii. Tom 2. Fontinalaceae—Amblystegiaceae. – Arctoa Phytotaxa 9: 175–195. 11, Suppl. 2: 609–960. CRUM, H.A. & L.E. ANDERSON 1981. Mosses of Eastern North Amer- IGNATOV, M. S., O. M. AFONINA & E. A. IGNATOVA. 2006 [2007]. ica (Vol. 1-2). – New York, Colombia University Press, 1328 pp. Check-list of mosses of East Europe and North Asia. – Arctoa 15: 1– CZERNYADJEVA, I.V. & E.A. IGNATOVA. 2019. The genus Haplohyme- 130. nium (Anomodontaceae, Bryophyta) in Russia. – Arctoa 28: 103–115. IGNATOV, M., A. GARDINER, V. BOBROVA, I. MILYUTINA, S. DONSKOV, D. G. 2015. Moss leaf morphogenesis and its correlation with HUTTUNEN & A. TROITSKY. 2007. On relationships of mosses of the leaf shape in Funariaceae (Bryophyta). – Arctoa 24(2): 503–508. the order Hypnales, with the special reference to taxa traditionally clas- ENROTH, J., S. OLSSON, S. HE, J.R. SHEVOCK & D. QUANDT. 2010. sified in Leskeaceae. – In: Newton, A.E. & R. Tangney (eds.), Pleuro- When morphology and molecules tell us different stories, part 2: Pin- carpous mosses: systematics and evolution. CRC Press, Bocan Rota natella homaliadelphoides (Neckeraceae), a new moss species from (Florida): 171-207. 102 M.S. IGNATOV, A.V. FEDOROVA & V.E. FEDOSOV

IGNATOV, M. S., O. I. KUZNETZOVA & I. V. CZERNYADJEVA. 2014. RONQUIST, F., M. TESLENKO, P. VAN DER MARK, D.L. AYRES, A. On the systematic position of Leptodictyum mizushimae (Bryophyta). DARLING, S. HÖHNA, B. LARGET, L. LIU, M.A. SUCHARD & – Arctoa 23: 185–193. J.P. HUELSENBECK. 2012. MrBayes 3.2: efficient Bayesian phylo- IGNATOV, M. S. & U. N. SPIRINA. 2012. Morphogenesis of proximal genetic inference and model choice across a large model space. – Sys- branch leaves in mosses. – Russian Journal of Developmental Biolo- tematic Biology 61: 539–542. gy 43(3): 148–156. SCHIMPER, W. P. 1856. Corollarium Bryologiae Europaeae, – Stuttgart, IWATSUKI, Z. 1963. A revision of the East Asiatic species of the genus E. Schweizerbart, 140 pp. Anomodon. – Journal of the Hattori Botanical Laboratory 26: 27–62. SCHIMPER, W. P. 1860a. Synopsis Muscorum Europaeorum. – Stuttgart, KATOH, K. & D.N. STANDLEY. 2013. MAFFT Multiple Sequence E. Schweizerbart. 733 pp. Alignment Software Version 7: Improvements in Performance and Us- SCHIMPER, W. P. 1860b. Icones morphologicae atque organographicae- ability. – Molecular Biology and Evolution 30(4): 772–780. introductionem synopsu muscorum europaeorum praemissam illus- KINDBERG, N.C. 1897. Genera of European and North American Bry- trantes. – Stuttgart, E. Schweizerbart. 26 pp. ineae (Mosses). – Göteborg, Published by Author. 40 pp. SCHLESAK, S., L. HEDENAS, M. NEBEL & D. QUANDT. 2018. Clean- LIMPRICHT, K. G. 1895. Die Laubmoose Deutschlands, Oesterreichs ing a taxonomic dustbin: placing the European Hypnum species in a und der Schweiz, Bd. 2. – Leipzig, Eduard Kummer. phylogenetic context! – Bryophyte Diversity & Evolution 40(2): 37– 54. LIU, Y., M. JOHNSON, C. J. COX, R. MEDINA, N. DEVOS, A. VANDERPOORTEN, L. HEDENÄS, N. BELL, J. R. SHEVOCK, B. SHAW, J., C. J. COX, B. GOFFINET, W. R. BUCK & S. B. BOLES. AGUERO, D. QUANDT, N. WICKETT, J. SHAW & B. GOFFINET. 2003. Phylogenetic evidence of a rapid radiation of pleurocarpous moss- 2019. Resolution of the ordinal phylogeny of mosses using targeted es (Bryophyta). – Evolution 57: 2226–2241. https://doi.org/10.1111/ exons from organellar and nuclear genomes. – Nature Communica- j.0014-3820.2003.tb00235.x tions 10: 1485 [1–11]. SIMMONS, M.P. & H. OCHOTERENA. 2000. Gaps as characters in MAGILL, R. E. 2014. Pterigynandraceae. – In: Flora of North America sequence-based phylogenetic analyses. – Systematic Biology 49 (2): Editorial Committee (eds.) Flora of North America North of Mexico 369–381. 28: 366–372. SMITH, A. J. E. 1978. The Moss Flora of Britain & Ireland. – Cam- MILLER, M.A., W. PFEIFFER & T. SCHWARTZ. 2010. Creating the bridge, Cambridge University Press, 706 pp. CIPRES Science Gateway for inference of large phylogenetic trees. – SPIRINA, U.N. & M.S. IGNATOV. 2008. Branch development and pseu- In: Proceedings of the Gateway Computing Environments Workshop doparaphyllia of Hypnum cupressiforme (Hypnales, Musci). – Arctoa (GCE), 14 Nov. 2010, New Orleans, LA: 1–8. 17: 139-160. MÜLLER, K. 2005. SeqState. – Applied Bioinformatics 4 (1): 65–69. SPIRINA, U. N. & M. S. IGNATOV. 2015. Bilobed leaves in mosses? NEWTON, A.E., C.J. COX, J.G. DUCKETT, J.A. WHEELER, B. GOFFI- Structure and adaptive significance of proximal branch leaves in Lem- NET, T.A.J. HEDDERSON & B.D. MISHLER. 2000. Evolution of bophyllaceae. – Arctoa 24(1): 124–140. the major moss lineages: phylogenetic analyses based on multiple gene STECH, M. & D. QUANDT. 2014. 20,000 species and five key markers: sequences and morphology. – The Bryologist 103: 187–211. The status of molecular bryophyte phylogenetics. – Phytotaxa 9 (1): NOGUCHI, A. 1991. Illustrated Moss Flora of Japan. Pt. 4. – Nichinan, 196–228. Hattori Botanical Laboratory, pp. 743–1012. STECH, M. & W. FREY. 2008. A morpho-molecular classification of the OLSSON, S., V. BUCHBENDER, J. ENROTH, S. HUTTUNEN, L. mosses (Bryophyta). – Nova Hedwigia 86: 1–21. HEDENÄS & D. QUANDT. 2009a. Evolution of the Neckeraceae: TANGNEY, R.S. 1997. A generic revision of the Lembophyllaceae. –Jour- resolving the backbone phylogeny. – Systematics and Biodiversity 7: nal of the Hattori Botanical Laboratory 81: 123–153. 419–432. https://doi.org/10.1017/S1477200009990132 TSUBOTA, H., T. ARIKAWA, H. AKIYAMA, E. D. LUNA, D. GONZA- OLSSON, S., V. BUCHBENDER, J. ENROTH, L. HEDENÄS, S. HUT- LEZ, M. HIGUCHI & H. DEGUCHI. 2002. Molecular phylogeny of TUNEN & D. QUANDT. 2009b. Phylogenetic analyses reveal high hypnobryalean mosses as inferred from a large-scale dataset of chloro- levels of polyphyly among pleurocarpous lineages as well as novel plast rbcL, with special reference to the Hypnaceae and possibly related clades. – The Bryologist 112: 447–466. https://doi.org/10.1639/0007- families. – Hikobia 13: 645–665. 2745-112.3.447 TSUBOTA, H., E. D. LUNA, D. GONZÁLEZ, M. S. IGNATOV & H. OLSSON, S., J. ENROTH, V. BUCHBENDER, L. HEDENÄS, S. HUT- DEGUCHI. 2004. Molecular phylogenetics and ordinal relationships TUNEN & D. QUANDT. 2011. Neckera and Thamnobryum (Necker- based on analyses of a large-scale data set of 600 rbcL sequences of aceae. Bryopsida): Paraphyletic assemblages. – Taxon 60(1): 36–50. mosses. – Hikobia 14: 149–170. PODPERA, J. 1954. Conspectus Muscorum Europaeorum. – Praha, VANDERPOORTEN, A., L. HEDENÄS, C.J. COX & A.J. SHAW. 2002. Nakladatelstvi Cesk. Akad. Ved., 699 pp. Phylogeny and morphological evolution of the Amblystegiaceae (Bry- QUANDT, D., S. HUTTUNEN, R. TANGNEY & M. STECH. 2009. opsida). – Molecular Phylogenetics and Evolution 23 (1): 1–21. Back to the Future? Molecules Take Us Back to the 1925 Classifica- WATANABE, R. 1972. A revision of the family Thuidiaceae in Japan and adja- tion of the Lembophyllaceae (Bryopsida). – Systematic Botany 34(3): cent areas. – Journal of the Hattori Botanical Laboratory 36: 171–320. 443–454. WU, P.-C. 2002. Thuidiaceae. – In: Wu Peng-cheng, M. R. C. & S. He. RAMBAUT, A., & A.J. DRUMMOND. 2007. Tracer. – Computer pro- 2002. Hookeriaceae–Thuidiaceae. 6. viii + 221 pages. In Moss Fl. gram and documentation distributed by the author, website http:// China. Science Press & Missouri Botanical Garden, Beijing, New York beast. bio. ed. ac. uk/Tracer & St. Louis.