55

Nova Hedwigia 81 1mdash2 55mdash78 Stuttgart August 2005

DOI 1011270029-503520050081-0055 0029-5035050081-0055 $ 600copy 2005 J Cramer in der Gebruumlder Borntraeger

Verlagsbuchhandlung D-14129 Berlin middot D-70176 Stuttgart

A morpho-molecular classification of the liverworts(Hepaticophytina Bryophyta)

by

Wolfgang Frey and Michael Stech

Institut fuumlr Biologie - Systematische Botanik und PflanzengeographieFreie Universitaumlt Berlin Altensteinstr 6 D-14195 Berlin Germany

With 1 table and 1 figure

Frey W amp M Stech (2005) A morpho-molecular classification of the liverworts (HepaticophytinaBryophyta) - Nova Hedwigia 81 55-78

Abstract Recent molecular analyses and a re-evaluation of morphological and ultrastructuralcharacters provided new insights into relationships among liverworts (Hepaticophytina Bryophyta)and mosses Considering these results a new suprageneric classification of liverworts is proposedThe liverwort classes are grouped into four superclasses According to the paraphyly of simplethalloid liverworts new classes Pallaviciniopsida and Pelliopsida are established for taxa formerlyincluded in the Jungermanniopsida which in the narrower circumscription comprise only the leafyliverworts (separated into Jungermanniidae with two new superorders Jungermannianae andPorellanae and Pleuroziidae subclass nov) and the Metzgeriidae sstr (Aneurales ord nov andMetzgeriales) Pallaviciniopsida comprise two monotypic orders Pallaviciniales and Hymenophytaleswhereas Pelliopsida comprise a single order Pelliales Fossombroniopsida are treated here includingFossombroniaceae Petalophyllaceae Allisoniaceae and Sandeothallaceae Taxa of ambiguous positionwithin superclass III according to morphological and molecular data include MakinoaceaeNoterocladaceae and Phyllothalliaceae The present classification on high taxonomic level reflectsthe early-divergent evolutionary history of the long-separated major liverwort groups Selectedmorphological-anatomical and ultrastructural characteristics of the higher taxa are provided alongwith summaries of fossil records and recent molecular data

Key words Hepaticophytina suprageneric classification molecular data superclassesPallaviciniopsida class nov Pelliopsida class nov Pleuroziidae subclass nov

Introduction

Liverworts (Hepaticophytina) comprise an estimated number of c 6000 species in c370 genera They are a highly diverse plant group with substantial morphologicalheterogeneity including lsquocomplex thallosersquo lsquosimple thallosersquo and lsquoleafyrsquo liverworts

56

Few enigmatic taxa with different kinds of leaf-like lobes or lobules (BlasiaFossombronia Haplomitrium Noteroclada Phyllothallia Pleurozia Sphaerocarposand Treubia) are transitional between the thallose and leafy condition and probablyrepresent relics of the early liverwort diversification Liverworts are widely distributedon earth from the arctic to the subantarctic region with high cover values mainly intropical cloud forests and temperate rain forests but also in desert crusts and occuron a wide range of substrates

Except for some controversial analyses based on 18S rDNA sequences (eg Bopp ampCapesius 1998) all molecular analyses resolved the Hepaticophytina as monophyleticin accordance with synapomorphic characters such as common archegonial andantheridial ontogeny without apical cells unequal division of the archespore cellinto a spore mother cell and an elater cell (elaters unique in the plant kingdom)presence of oil-bodies (unique in the plant kingdom) and lunularic acid

In addition to the traditional division of liverworts into Marchantiopsida (complexthallose liverworts) and Jungermanniopsida (simple thallose and leafy liverworts)and the early separation of Haplomitrium into Haplomitriopsida Stotler amp Stotl-Crand three classes were erected based on molecular phylogenies and ultrastructuralanalyses of the gametophyte-sporophyte junction Blasiopsida (Stech amp Frey 2001)Fossombroniopsida (Frey et al 2001) and Treubiopsida (Stech et al 2000)Furthermore molecular data now confirm the parallel evolution of different thallosegrowth forms within the Hepaticophytina The complex thallose form is restrictedto the monophyletic Marchantiopsida whereas the thallose or semileafy Metzgeriidaesl (Jungermanniales anacrogynae) are resolved as paraphyletic (eg Davis 2004He-Nygreacuten et al 2004 Stech amp Frey 2004 Forrest amp Crandall-Stotler 2004 2005Heinrichs et al 2005) The true simple thallose forms (eg Metzgeria Riccardia)the semileafy Fossombronialean liverworts and the thallose forms with a centralstrand (Pallaviciniaceae Hymenophytaceae) obviously represent differentevolutionary lineages which should be assigned to different classes Consequentlyrelationships within the Jungermanniopsida are subject to major change according tothe results of molecular analyses

In the present study we propose a new suprageneric taxonomy of the HepaticophytinaThe main aims are

(i) to establish a system of superclasses to designate relationships between the liver-wort classes analogous to the latest classification of mosses by Goffinet amp Buck(2004) and

(ii) to recircumscribe the Jungermanniopsida according to recent molecular analyses

An overview of distinctive morphological and anatomical characters compiled fromthe literature blepharoplast ultrastructure (after Carothers amp Rushing 1988 Pass ampRenzaglia 1995 and others) type of the gametophyte-sporophyte junction (afterLigrone et al 1993 Frey et al 2001 Carafa et al 2003 cf Table 1) fossil records(after Krassilov amp Schuster 1984 Oostendorp 1987) and geographical distributionis provided for the respective taxa A summary of evolutionary relationships of themajor liverwort groups with particular reference to gametophyte-sporophyte junctiontypes and the main fossil records is shown in Fig 1

57

Table 1 Distribution of transfer cells (layers) and foot shape in the gametophyte-sporophyte junctionin the liverworts (Hepaticophytina) For further details see Frey et al (2001) and Carafa et al (2003)

Class Subclass Order Family Transfer cells (layers) Foot shapeGametophyte Sporophyte

One to several layers of transfer cells on both sides of the placenta

Superclass ITreubiopsida Treubiaceae ndash +(1-2) bulbous

+(3-4) +(2-3) bulbousHaplomitriopsida Haplomitriaceae +(2-3) +(1-2) bulbous

Superclass IIBlasiopsida Blasiaceae +(2-3) +(1) conicalMarchantiopsida Sphaerocarpidae Sphaerocarpales +(2ndash3) +(1) spheroidal

Marchantiidae Monocleales +(4-6) +(2) conicalMarchantiales +(2-4) +(1) spheroidal

+(1-2) conicalbulbouscylindricalcup-shaped

Ricciales ndash ndash ndashSuperclass IIIFossombroniopsida Fossombroniaceae +(2-3) +(1) bulbous

Reduction of gametophyte and mostly also sporophyte transfer cells (wall ingrowths)

Pallaviciniopsida Pallaviciniaceae ndash +(1) conicalHymenophytaceae ndash ndash conical

Pelliopsida Pelliaceae ndash ndash conical

Superclass IVJungermanniopsida Jungermanniidae div families ndash +(1) conical bul-

ndash +(1-2) bousspheroidal

Metzgeriidae Aneuraceae ndash ndash conical(Riccardia) +(2) ndash conicalMetzgeriaceae ndash ndash conical

Systematic arrangement of taxa

Superclass I

1 Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Fam Treubiaceae Verd

Characterized by the unique ldquoleafyrdquo growth form with 2 lateral rows of alternatesuccubous lobes (interpreted as leafy appendages) and transversely oriented dorsallobules (scales) dimorphic leaf cells (scattered cells containing 1 large oil-body

58

Fig 1 Phylogenetic relationships of the higher taxa of Hepaticophytina indicating the approximatetime of divergence of the groups in line with assignable fossil records and distribution of characteristicgametophyte-sporophyte junction types 1 With several layers of transfer cells on both side of theplacenta 2 Sporophyte transfer cells (stc) wall ingrowths relatively thin and highly branched 3 Stcwall ingrowths highly branched and anastomosing of high structural complexity wall ingrowths ingametophyte transfer cells (gtc) partly short and coarse 4 Gametophyte placental cells without wallingrowths 5 Partly sporophyte placental cells without wall ingrowths 6 Sporophyte and gametophyteplacental cells without wall ingrowths Abbreviations g gametophyte ju gametophyte-sporophytejunction with placenta s sporophyte Blob Blasiites lobatus Gspp Gessella spp GsalGrisellatheca salopensis Hlan Hepaticites langii Jgra Jungermanniites gracilis Jkeu Jkeuperianus Lpap Laticaulina papillosa Mcya Marchantites cyathodoides MmetMetzgeriothallus metzgerioides Mplu Muscites plumatus Nlan Naiadita lanceolata PdevPallaviciniites devonicus Tkid Treubiites kidstonii

59

other cells only with chloroplasts) and slime papillae on ventral surface producinga thick covering of mucilage (otherwise only in Verdoorniaceae) Blepharoplast ofCalobryalean affinity lamellar strip (spline) with up to 104 microtubules (widest inbryophytes) open spline aperture overlap between anterior and posterior basal bodiesGametophyte-sporophyte junction either resembling that of Jungermanniopsida(Apotreubia gametophyte placental cells lacking wall ingrowths) or similar toFossombronia and Haplomitrium (Treubia several layers of transfer cells on bothside of the placenta with thin wall ingrowths) No fossil records known - 2 genera(11 species) distribution pattern originally Pangaean - Treubia KIGoebel (7)basically Gondwanan Malesia Australasia Oceania (S Pacific) rather recenttransgression of Wallacersquos line 1 species in Chile not represented in Africa -Apotreubia SHatt amp Mizut (4) predominantly Laurasian

Based on morphological characters the two extant genera Treubia and Apotreubiamay be regarded as the most archaic living fossils in liverworts and extant models ofan extinct plant group In molecular trees Treubiopsida are resolved as sister to allother liverworts either alone (eg Stech amp Frey 2001) or together with Haplomitrium(eg Forrest amp Crandall-Stotler 2005) similar to cladistic analyses based on malegametogenesis characters (Garbary et al 1993) Heinrichs et al (2005) recentlyincluded Treubiopsida in the Haplomitriopsida however with respect to themorphological and anatomical differences and the fact that at least some of theshared characters states (eg tetrahedral apical cells or the type of the gametophyte-sporophyte junction) are probably ancestral plesiomorphies we prefer to maintaintwo classes united in a single superclass

2 Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Fam Haplomitriaceae Dbulldehellipek

Unique features upright habit subterranean creeping axis (ldquorhizomerdquo) undividedleafy appendages ldquoisophyllousrdquo with transversely inserted ldquoleavesrdquo (some speciestend toward ldquoanisophyllyrdquo and succubous insertion) rhizoids lacking central strandpresent water-conducting cells resembling that of Takakia scattered gametangia indiffuse groups laterally along the stem without specialized protective bracts massiveseta and an extensive stem-calyptra Blepharoplast structure spline with up to 90microtubules spline aperture on the left side Gametophyte-sporophyte junction 1-2 sporophyte and 2-3 gametophyte placental cell layers gametophyte transfer cellswith highly branched and thin long wall ingrowths similar to Treubia andFossombronia foot bulbous collar absent Fossil records Gessella Poulsen (2) fromLower Permian Denmark Naiadita lanceolata PBBrodie from Upper Triassic ofEngland is discussed to belong to either Haplomitriopsida or Marchantiopsida subclassSphaerocarpidae - Monotypic - Haplomitrium Nees (9) basically Gondwanan centerof diversity in Australasia

Haplomitrium is morphologically and anatomically isolated by a ldquoserious offundamental criteriardquo (Schuster 1984a) and regarded as an early-diverging lineagewithin liverworts The precise placement of Haplomitrium in molecular trees has

60

been problematic and varies depending on taxon sampling especially the inclusionvs exclusion of Treubia and the applied method (summarized by Shaw amp Renzaglia2004) Cladistic analyses of male gametogenesis characters (Garbary et al 1993)and recent molecular analyses including Treubia (eg Forrest amp Crandall-Stotler2005) revealed that Haplomitrium plus Treubia form a clade sister to all otherliverworts groups

Superclass II

1 Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Fam Blasiaceae HKlinggr

Thallus with ill-defined midrib grading into unistratose wings (leafy habit) incolonies Central strand lacking 2 rows of flattened multicellular scales (as incomplex thallose liverworts) irregularly dentate on ventral surface of thallusSmall ventral hemispherical lsquoauriclesrsquo filled with Nostoc colonies and uniqueflasked-shaped gemma-receptacles present (unique in liverworts) Marchantialeanblepharoplast type Gametophyte-sporophyte junction 1 sporophyte and 2-3gametophyte placental cell layers with Marchantialean-type wall ingrowths (transfercells) Fossil records The Late Carboniferous Blasiites lobatus (JWalton)RMSchust resembling Blasia pusilla is supposed to be an ancestor of the extanttaxa (however see Pelliopsida) The Carboniferous Treubiites kidstonii (JWalton)RMSchust with lateral succubously shingled leaves and ventral scales (as in Blasia)is rejected as a presumable precursor of Treubiopsida but serves as a model fromwhich the more frondose semithallose extant Blasia may be derived - 2 monotypicgenera - Blasia L circumboreal - Cavicularia Steph endemic Japan

Blasia was traditionally included in the Metzgerialean group but blepharoplastultrastructure and a Marchantialean-type gametophyte-sporophyte junction assignit to the Marchantiopsida Similarly latest molecular results resolve Blasia andCavicularia as sister to the Marchantiopsida (Forrest amp Crandall-Stotler 2005)with maximum bootstrap support whereas earlier molecular analyses of Blasiaeither suggested a somewhat intermediate position between Marchantiopsida andJungermanniopsida (Wheeler 2000 Stech amp Frey 2001) or a basal position withinliverworts (He-Nygreacuten et al 2004) The molecular separation of Blasia andCavicularia in Forrest amp Crandall-Stotler (2004) and Heinrichs et al (2005)was caused by contaminated Cavicularia DNA (cf Forrest amp Crandall-Stotler2005)

2 Class Marchantiopsida Stotler amp Stotl-Crand

Thirty-two genera with c 350 species Highest differentiated gametophytes in theplant kingdom Blepharoplast structure uniform closed apertures three splinemicrotubules wide Gametophyte-sporophyte junction 1-2 sporophyte and 2-4gametophyte placental cell layers cells of both layers with characteristic wallingrowths (highly branched and anastomosing or short and coarse respectively

61

Marchantialean type) Fossil records Some enigmatic Lower Devonian microfossils(epidermal surface tissues rhizoids) may be regarded as the remains of earlyMarchantioid liverworts (Graham et al 2004) Convincing Marchantioid fossilsobviously unknown from Lower Palaeophytic starting with the Lower PermianMarchantites loreus Zalessky (incertae sedis) the unequivocal Middle TriassicMarchantites cyathodoides (Townrow) HMAnderson and M tennantii HMAndersonand becoming relatively species rich from Triassic to Eocene Probably the initialdiversification of the Marchantiopsida took place at the beginning of the relativelyarid Mesophytic followed by a rapid radiation of Marchantioid taxa coincidentwith extreme conditions and ecological reorganisation in Upper Permo-Triassictime

Monophyly of the Marchantiopsida is strongly supported by all respective molecularanalyses

1 Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Fam Sphaerocarpaceae (Dumort) Heeg

Leafy habit Marchantialean blepharoplast type and gametophyte-sporophyte junctionNo fossils known - 2 genera - Sphaerocarpus Boehm and the monotypic GeothallusCampb

Fam Riellaceae Engl

Monotypic Riella Mont

2 Subclass Marchantiidae Engl

1 Order Monocleales RMSchust

Ancient relict group with plesiomorphic characters eg simple thallus and capsuleopening by only one lateral slit Typical Marchantialean blepharoplast andgametophyte-sporophyte junction type as well as molecular data (eg Meiszligner etal 1998 Wheeler 2000 Forrest amp Crandall-Stotler 2005) support the currentclassification in the Marchantiidae No fossils known - Monotypic - MonocleaHook (2) probably of Gondwanan origin restricted to hyperhygric habitats

2 Order Marchantiales Limpr in Cohn

12 families (see synopsis below) with 25 genera For subdivision of the order seeCrandall-Stotler amp Stotler (2000)

3 Order Ricciales Schljakov

2 families Oxymitraceae MuumlllFrib ex Grolle (Oxymitra Bisch ex Lindenb) andRicciaceae Reichenb with 2 genera Riccia L and the monotypic RicciocarposCorda

62

Superclass III

Recent molecular analyses based on larger taxon sampling (Davis 2004 He-Nygreacutenet al 2004 Stech amp Frey 2004 Forrest amp Crandall-Stotler 2004 2005 Heinrichs etal 2005) revealed that the simple thallose liverworts formerly comprised asJungermanniopsida subclass Metzgeriidae (sl) with 15 families 38 genera and c500 species are not monophyletic These taxa which form leaf-like lobes or thalluswings from a single wedge-shaped apical cell and are basically anacrogynous(Jungermanniales anacrogynae) are split into two main groups The first group(Metzgeriales II sensu Forrest amp Crandall-Stotler 2004) comprises different types ofsimple thallose or semileafy liverworts which are here divided into three classesFossombroniopsida Pallaviciniopsida and Pelliopsida The simple thalloseMetzgerialean liverworts (Metzgeriales I sensu Forrest amp Crandall-Stotler 2004)compose the second group that is sister to the leafy liverworts and thus treated assubclass Metzgeriidae sstr of the Jungermanniopsida (superclass IV)

1 Class Fossombroniopsida WFrey amp Hilger

Plants thallose Antheridia in acropetal sequence on upper surface of axis Oil-bodiessmall numerous Capsule mostly lacking valves wall disintegrating into fragmentsor via irregular lines into unequal valves from apex downwards Capsule wall 2-4(-6)-layered Spores areolate or with irregular lamellae or spinose on distal surfaceElaterophore lacking elaters 2-3-helical Probably of Gondwanan origin

Order Fossombroniales Schljakov

Fam Fossombroniaceae Hazsl

Main axis with obliquely inserted succubous leaves (leaf-like lobes) Rhizoids purplish(rarely pale brown) Antheridia and archegonia in simple acropetal sequence Antheridianaked Sporophyte protected by a caulocalyx Capsule wall without wall thickeningsGametophyte-sporophyte junction 1 sporophyte and 2-3 gametophyte placental transfercell layers cells with thin wall ingrowths strongly reminescent of the placenta inTreubia and Haplomitrium gametophyte placenta transfer cells with strongly branchedwall ingrowths (resembling those of Blasia and Marchantiopsida) a bulbous foot andabsence of a collar support exclusion of Fossombronia from the Jungermanniopsida -2 genera (c 92) worldwide distribution - Austrofossombronia RMSchust (2)subantarctic Andes (Peru-Venezuela) - Fossombronia Raddi (c 90) from subarctic tosubantarctic regions centre of diversification in Australia (33 spp) TheFossombroniaceae are strongly supported as monophyletic in molecular analyses withAllisonia and Petalophyllum as sister groups (Forrest amp Crandall-Stotler 2005) Thetaxon is thought to be very isolated immensely old and relict (Schuster 1984a)

Fam Petalophyllaceae (RMSchust) Stotler amp Stotl-Crand

Thallus with unistratose dorsal lamellae radiating from midrib to margin or unistratosethallus wings Archegonia clustered rather than scattered Sporophyte protected by apseudoperianth Capsule wall with outer wall thickenings - 2 genera (7) -

63

Petalophyllum Nees amp Gottsche ex Lehm (6) New Zealand (2) 1 species each inW Australia India and S USA P ralfsii (Wils) Nees amp Gottsche medit-atlant WEurope N Africa - Sewardiella Kashyap (1) W Himalayas

Fam Allisoniaceae (RMSchust ex Grolle) Schljakov

Plants thallose Midrib of thallus ill-defined Central strand lacking DioicousAntheridia individually protected by a scale Capsule spherical wall irregularly tearinginto 5-7 unequal valves epidermal cells with irregular bands without elaterophoreSpores strongly sculptured - 2 genera (5) - Allisonia Herzog (1) endemic NewZealand - Calycularia Mitt (4) N and E Asia Himalayas

Molecular data indicate that the Allisoniaceae are not monophyletic Both generahave similar capsule walls and thallus structures but differ by the presence of awell-developed pseudoperianth in Calycularia (eg Inoue 1976) The placement ofCalycularia has traditionally been problematic and is still tentative based on itsposition sister to the Fossombronialean and Pallavicinialean liverworts in moleculartrees

Fam Sandeothallaceae RM Schust

Plants thallose Thalli simple or rarely branched with uniseriate slime hairs occasionalwith ventral branches Rhizoids reddish Antheridia in axils of dorsal scales alongmidrib surface Seta massive Capsule wall (3)4-5(6)-layered opening by 2 lateralslits without elaterophore - Monotypic - Sandeothallus RMSchust (1) IndiaMalesia Samoa

The systematic position remains ambiguous Morphologically Sandeothallus occupiesan intermediate position gametophytic characters indicate close relationship toAllisoniaceae whereas sporophytically it is close to the Pallaviciniaceae (Schuster1982) Molecular data are so far not available

2 Class Pallaviciniopsida WFrey amp Stech class nov

Plantae thallinae prostratae vel in axem prostratum stipitemque erectum divisae partim dendroideaeCosta thalli prominens 1 vel 2(-4) filis centralibus Cellulae filorum centralium elongatae perforataehydroideis similes Capsulae ovoideae ad cylindricae 2 vel 4 valvis dehiscentes

Type family Pallaviciniaceae Mig

Plants thallose prostrate erect or sometimes dendroid Dendroid taxa evolved threetimes independently in Jensenia and Symphyogyna (Pallaviciniaceae) as well as inHymenophyton (Hymenophytaceae) (Schaumann et al 2005) Gametophyte mostlywith central strand composed of thick-walled elongated water-conducting cells withperforations (pores) This pallavicinoid type of water-conducting cells occurs onlyin the Pallaviciniopsida and is unique in bryophytes Antheridia and archegonia(clustered) on dorsal surface of thallus Sporophyte protected by a pseudoperianth(inner involucre) or stem-calyptra Seta massive Capsule ellipsoidal to cylindricaltearing into 2 imperfectly 4 or 4 valves wall bistratose Gametophyte-sporophytejunction gametophyte placental cells without wall ingrowths sporophyte placental

64

cells partly without wall ingrowths Fossil records Pallaviciniites devonicus (Hueber)RMSchust from lowermost Upper Devonian (375 mio y) is the oldest true bryo-phyte fossil known The thallose plant bearing a central strand in the gametophyteaxis is superficially similar to the Pallaviciniaceae in particular to Pallavicinia andSymphyogyna Laticaulina papillosa Krassilov from Late Jurassic of Russia alsoshows affinities to the Pallaviciniopsida (Symphyogyna) About 65 species

1 Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Basionym Pallaviciniineae RMSchust Phytologia 56 65 1984

Type (and only) family Pallaviciniaceae Mig

Schuster (1984b) erected the Pallaviciniineae to include PallaviciniaceaeSandeothallaceae and Makinoaceae In contrast we consider the Pallavicinialesmonotypic at least until relationships of Sandeothallus and Makinoa have beenclarified on the molecular level

Fam Pallaviciniaceae Mig

Plants thallose prostrate without basal stipe and ldquorhizomerdquo or erect arising froma ldquorhizomerdquo or stipe dendroid in Jensenia and some species of Pallavicinia andSymphyogyna Thallus with well-defined midrib with 1 or 2(-4) central strandsin most taxa present and unistratose lamina Water conducting cells elongatedwith tapering ends and thickened walls (c 8 microm wide and up to 300 microm long)throughout with numerous pits produced by dissolution of secondary wallmaterial associated with modified plasmodesmata Only few true plasmodesmata-derived perforations (pores) present (Oslash 200-400 nm) No relationship withtracheids (Frey et al 1996) Slime papillae on both dorsal and ventral surfacesof apex sometimes present Ventral scales absent or small and uniseriate DioicousAntheridia on dorsal surface of thallus often in 2-several ranks associated withscales Archegonia clustered on dorsal surface of midrib (gynoecia) deliminatedby a single (Symphyogyna) or double involucres (except Xenothallus) Developingsporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-calyptra Seta long massive Capsule elongate-cylindrical to ovoid dehiscenceby 2 or imperfectly 4 valves epidermal cell walls lacking thickenings Spores 1-celled Elaterophore rudimentary or absent Elaters 2-3-helical Gametophyte-sporophyte junction Wall ingrowths (transfer cells) present in the outermostsporophytic placental layer - 9 genera (c 60) Gondwanan centres of diversityin Australasia and S America

Molecular analyses resolve Pallaviciniaceae as monophyletic (eg Forrest ampCrandall-Stotler 2005 Schaumann et al 2005) These data support a separationof Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa a positionof Podomitrium (Podomitrioideae RMSchust) close to the Symphyogynoideae(Trevis) RMSchust ex Grolle and polyphyly of Pallavicinia and thePallavicinioideae Because of ambiguous relationships between these subfamilieswe include Podomitrioideae and Symphyogynoideae in Pallavicinioideae sl

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

56

Few enigmatic taxa with different kinds of leaf-like lobes or lobules (BlasiaFossombronia Haplomitrium Noteroclada Phyllothallia Pleurozia Sphaerocarposand Treubia) are transitional between the thallose and leafy condition and probablyrepresent relics of the early liverwort diversification Liverworts are widely distributedon earth from the arctic to the subantarctic region with high cover values mainly intropical cloud forests and temperate rain forests but also in desert crusts and occuron a wide range of substrates

Except for some controversial analyses based on 18S rDNA sequences (eg Bopp ampCapesius 1998) all molecular analyses resolved the Hepaticophytina as monophyleticin accordance with synapomorphic characters such as common archegonial andantheridial ontogeny without apical cells unequal division of the archespore cellinto a spore mother cell and an elater cell (elaters unique in the plant kingdom)presence of oil-bodies (unique in the plant kingdom) and lunularic acid

In addition to the traditional division of liverworts into Marchantiopsida (complexthallose liverworts) and Jungermanniopsida (simple thallose and leafy liverworts)and the early separation of Haplomitrium into Haplomitriopsida Stotler amp Stotl-Crand three classes were erected based on molecular phylogenies and ultrastructuralanalyses of the gametophyte-sporophyte junction Blasiopsida (Stech amp Frey 2001)Fossombroniopsida (Frey et al 2001) and Treubiopsida (Stech et al 2000)Furthermore molecular data now confirm the parallel evolution of different thallosegrowth forms within the Hepaticophytina The complex thallose form is restrictedto the monophyletic Marchantiopsida whereas the thallose or semileafy Metzgeriidaesl (Jungermanniales anacrogynae) are resolved as paraphyletic (eg Davis 2004He-Nygreacuten et al 2004 Stech amp Frey 2004 Forrest amp Crandall-Stotler 2004 2005Heinrichs et al 2005) The true simple thallose forms (eg Metzgeria Riccardia)the semileafy Fossombronialean liverworts and the thallose forms with a centralstrand (Pallaviciniaceae Hymenophytaceae) obviously represent differentevolutionary lineages which should be assigned to different classes Consequentlyrelationships within the Jungermanniopsida are subject to major change according tothe results of molecular analyses

In the present study we propose a new suprageneric taxonomy of the HepaticophytinaThe main aims are

(i) to establish a system of superclasses to designate relationships between the liver-wort classes analogous to the latest classification of mosses by Goffinet amp Buck(2004) and

(ii) to recircumscribe the Jungermanniopsida according to recent molecular analyses

An overview of distinctive morphological and anatomical characters compiled fromthe literature blepharoplast ultrastructure (after Carothers amp Rushing 1988 Pass ampRenzaglia 1995 and others) type of the gametophyte-sporophyte junction (afterLigrone et al 1993 Frey et al 2001 Carafa et al 2003 cf Table 1) fossil records(after Krassilov amp Schuster 1984 Oostendorp 1987) and geographical distributionis provided for the respective taxa A summary of evolutionary relationships of themajor liverwort groups with particular reference to gametophyte-sporophyte junctiontypes and the main fossil records is shown in Fig 1

57

Table 1 Distribution of transfer cells (layers) and foot shape in the gametophyte-sporophyte junctionin the liverworts (Hepaticophytina) For further details see Frey et al (2001) and Carafa et al (2003)

Class Subclass Order Family Transfer cells (layers) Foot shapeGametophyte Sporophyte

One to several layers of transfer cells on both sides of the placenta

Superclass ITreubiopsida Treubiaceae ndash +(1-2) bulbous

+(3-4) +(2-3) bulbousHaplomitriopsida Haplomitriaceae +(2-3) +(1-2) bulbous

Superclass IIBlasiopsida Blasiaceae +(2-3) +(1) conicalMarchantiopsida Sphaerocarpidae Sphaerocarpales +(2ndash3) +(1) spheroidal

Marchantiidae Monocleales +(4-6) +(2) conicalMarchantiales +(2-4) +(1) spheroidal

+(1-2) conicalbulbouscylindricalcup-shaped

Ricciales ndash ndash ndashSuperclass IIIFossombroniopsida Fossombroniaceae +(2-3) +(1) bulbous

Reduction of gametophyte and mostly also sporophyte transfer cells (wall ingrowths)

Pallaviciniopsida Pallaviciniaceae ndash +(1) conicalHymenophytaceae ndash ndash conical

Pelliopsida Pelliaceae ndash ndash conical

Superclass IVJungermanniopsida Jungermanniidae div families ndash +(1) conical bul-

ndash +(1-2) bousspheroidal

Metzgeriidae Aneuraceae ndash ndash conical(Riccardia) +(2) ndash conicalMetzgeriaceae ndash ndash conical

Systematic arrangement of taxa

Superclass I

1 Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Fam Treubiaceae Verd

Characterized by the unique ldquoleafyrdquo growth form with 2 lateral rows of alternatesuccubous lobes (interpreted as leafy appendages) and transversely oriented dorsallobules (scales) dimorphic leaf cells (scattered cells containing 1 large oil-body

58

Fig 1 Phylogenetic relationships of the higher taxa of Hepaticophytina indicating the approximatetime of divergence of the groups in line with assignable fossil records and distribution of characteristicgametophyte-sporophyte junction types 1 With several layers of transfer cells on both side of theplacenta 2 Sporophyte transfer cells (stc) wall ingrowths relatively thin and highly branched 3 Stcwall ingrowths highly branched and anastomosing of high structural complexity wall ingrowths ingametophyte transfer cells (gtc) partly short and coarse 4 Gametophyte placental cells without wallingrowths 5 Partly sporophyte placental cells without wall ingrowths 6 Sporophyte and gametophyteplacental cells without wall ingrowths Abbreviations g gametophyte ju gametophyte-sporophytejunction with placenta s sporophyte Blob Blasiites lobatus Gspp Gessella spp GsalGrisellatheca salopensis Hlan Hepaticites langii Jgra Jungermanniites gracilis Jkeu Jkeuperianus Lpap Laticaulina papillosa Mcya Marchantites cyathodoides MmetMetzgeriothallus metzgerioides Mplu Muscites plumatus Nlan Naiadita lanceolata PdevPallaviciniites devonicus Tkid Treubiites kidstonii

59

other cells only with chloroplasts) and slime papillae on ventral surface producinga thick covering of mucilage (otherwise only in Verdoorniaceae) Blepharoplast ofCalobryalean affinity lamellar strip (spline) with up to 104 microtubules (widest inbryophytes) open spline aperture overlap between anterior and posterior basal bodiesGametophyte-sporophyte junction either resembling that of Jungermanniopsida(Apotreubia gametophyte placental cells lacking wall ingrowths) or similar toFossombronia and Haplomitrium (Treubia several layers of transfer cells on bothside of the placenta with thin wall ingrowths) No fossil records known - 2 genera(11 species) distribution pattern originally Pangaean - Treubia KIGoebel (7)basically Gondwanan Malesia Australasia Oceania (S Pacific) rather recenttransgression of Wallacersquos line 1 species in Chile not represented in Africa -Apotreubia SHatt amp Mizut (4) predominantly Laurasian

Based on morphological characters the two extant genera Treubia and Apotreubiamay be regarded as the most archaic living fossils in liverworts and extant models ofan extinct plant group In molecular trees Treubiopsida are resolved as sister to allother liverworts either alone (eg Stech amp Frey 2001) or together with Haplomitrium(eg Forrest amp Crandall-Stotler 2005) similar to cladistic analyses based on malegametogenesis characters (Garbary et al 1993) Heinrichs et al (2005) recentlyincluded Treubiopsida in the Haplomitriopsida however with respect to themorphological and anatomical differences and the fact that at least some of theshared characters states (eg tetrahedral apical cells or the type of the gametophyte-sporophyte junction) are probably ancestral plesiomorphies we prefer to maintaintwo classes united in a single superclass

2 Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Fam Haplomitriaceae Dbulldehellipek

Unique features upright habit subterranean creeping axis (ldquorhizomerdquo) undividedleafy appendages ldquoisophyllousrdquo with transversely inserted ldquoleavesrdquo (some speciestend toward ldquoanisophyllyrdquo and succubous insertion) rhizoids lacking central strandpresent water-conducting cells resembling that of Takakia scattered gametangia indiffuse groups laterally along the stem without specialized protective bracts massiveseta and an extensive stem-calyptra Blepharoplast structure spline with up to 90microtubules spline aperture on the left side Gametophyte-sporophyte junction 1-2 sporophyte and 2-3 gametophyte placental cell layers gametophyte transfer cellswith highly branched and thin long wall ingrowths similar to Treubia andFossombronia foot bulbous collar absent Fossil records Gessella Poulsen (2) fromLower Permian Denmark Naiadita lanceolata PBBrodie from Upper Triassic ofEngland is discussed to belong to either Haplomitriopsida or Marchantiopsida subclassSphaerocarpidae - Monotypic - Haplomitrium Nees (9) basically Gondwanan centerof diversity in Australasia

Haplomitrium is morphologically and anatomically isolated by a ldquoserious offundamental criteriardquo (Schuster 1984a) and regarded as an early-diverging lineagewithin liverworts The precise placement of Haplomitrium in molecular trees has

60

been problematic and varies depending on taxon sampling especially the inclusionvs exclusion of Treubia and the applied method (summarized by Shaw amp Renzaglia2004) Cladistic analyses of male gametogenesis characters (Garbary et al 1993)and recent molecular analyses including Treubia (eg Forrest amp Crandall-Stotler2005) revealed that Haplomitrium plus Treubia form a clade sister to all otherliverworts groups

Superclass II

1 Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Fam Blasiaceae HKlinggr

Thallus with ill-defined midrib grading into unistratose wings (leafy habit) incolonies Central strand lacking 2 rows of flattened multicellular scales (as incomplex thallose liverworts) irregularly dentate on ventral surface of thallusSmall ventral hemispherical lsquoauriclesrsquo filled with Nostoc colonies and uniqueflasked-shaped gemma-receptacles present (unique in liverworts) Marchantialeanblepharoplast type Gametophyte-sporophyte junction 1 sporophyte and 2-3gametophyte placental cell layers with Marchantialean-type wall ingrowths (transfercells) Fossil records The Late Carboniferous Blasiites lobatus (JWalton)RMSchust resembling Blasia pusilla is supposed to be an ancestor of the extanttaxa (however see Pelliopsida) The Carboniferous Treubiites kidstonii (JWalton)RMSchust with lateral succubously shingled leaves and ventral scales (as in Blasia)is rejected as a presumable precursor of Treubiopsida but serves as a model fromwhich the more frondose semithallose extant Blasia may be derived - 2 monotypicgenera - Blasia L circumboreal - Cavicularia Steph endemic Japan

Blasia was traditionally included in the Metzgerialean group but blepharoplastultrastructure and a Marchantialean-type gametophyte-sporophyte junction assignit to the Marchantiopsida Similarly latest molecular results resolve Blasia andCavicularia as sister to the Marchantiopsida (Forrest amp Crandall-Stotler 2005)with maximum bootstrap support whereas earlier molecular analyses of Blasiaeither suggested a somewhat intermediate position between Marchantiopsida andJungermanniopsida (Wheeler 2000 Stech amp Frey 2001) or a basal position withinliverworts (He-Nygreacuten et al 2004) The molecular separation of Blasia andCavicularia in Forrest amp Crandall-Stotler (2004) and Heinrichs et al (2005)was caused by contaminated Cavicularia DNA (cf Forrest amp Crandall-Stotler2005)

2 Class Marchantiopsida Stotler amp Stotl-Crand

Thirty-two genera with c 350 species Highest differentiated gametophytes in theplant kingdom Blepharoplast structure uniform closed apertures three splinemicrotubules wide Gametophyte-sporophyte junction 1-2 sporophyte and 2-4gametophyte placental cell layers cells of both layers with characteristic wallingrowths (highly branched and anastomosing or short and coarse respectively

61

Marchantialean type) Fossil records Some enigmatic Lower Devonian microfossils(epidermal surface tissues rhizoids) may be regarded as the remains of earlyMarchantioid liverworts (Graham et al 2004) Convincing Marchantioid fossilsobviously unknown from Lower Palaeophytic starting with the Lower PermianMarchantites loreus Zalessky (incertae sedis) the unequivocal Middle TriassicMarchantites cyathodoides (Townrow) HMAnderson and M tennantii HMAndersonand becoming relatively species rich from Triassic to Eocene Probably the initialdiversification of the Marchantiopsida took place at the beginning of the relativelyarid Mesophytic followed by a rapid radiation of Marchantioid taxa coincidentwith extreme conditions and ecological reorganisation in Upper Permo-Triassictime

Monophyly of the Marchantiopsida is strongly supported by all respective molecularanalyses

1 Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Fam Sphaerocarpaceae (Dumort) Heeg

Leafy habit Marchantialean blepharoplast type and gametophyte-sporophyte junctionNo fossils known - 2 genera - Sphaerocarpus Boehm and the monotypic GeothallusCampb

Fam Riellaceae Engl

Monotypic Riella Mont

2 Subclass Marchantiidae Engl

1 Order Monocleales RMSchust

Ancient relict group with plesiomorphic characters eg simple thallus and capsuleopening by only one lateral slit Typical Marchantialean blepharoplast andgametophyte-sporophyte junction type as well as molecular data (eg Meiszligner etal 1998 Wheeler 2000 Forrest amp Crandall-Stotler 2005) support the currentclassification in the Marchantiidae No fossils known - Monotypic - MonocleaHook (2) probably of Gondwanan origin restricted to hyperhygric habitats

2 Order Marchantiales Limpr in Cohn

12 families (see synopsis below) with 25 genera For subdivision of the order seeCrandall-Stotler amp Stotler (2000)

3 Order Ricciales Schljakov

2 families Oxymitraceae MuumlllFrib ex Grolle (Oxymitra Bisch ex Lindenb) andRicciaceae Reichenb with 2 genera Riccia L and the monotypic RicciocarposCorda

62

Superclass III

Recent molecular analyses based on larger taxon sampling (Davis 2004 He-Nygreacutenet al 2004 Stech amp Frey 2004 Forrest amp Crandall-Stotler 2004 2005 Heinrichs etal 2005) revealed that the simple thallose liverworts formerly comprised asJungermanniopsida subclass Metzgeriidae (sl) with 15 families 38 genera and c500 species are not monophyletic These taxa which form leaf-like lobes or thalluswings from a single wedge-shaped apical cell and are basically anacrogynous(Jungermanniales anacrogynae) are split into two main groups The first group(Metzgeriales II sensu Forrest amp Crandall-Stotler 2004) comprises different types ofsimple thallose or semileafy liverworts which are here divided into three classesFossombroniopsida Pallaviciniopsida and Pelliopsida The simple thalloseMetzgerialean liverworts (Metzgeriales I sensu Forrest amp Crandall-Stotler 2004)compose the second group that is sister to the leafy liverworts and thus treated assubclass Metzgeriidae sstr of the Jungermanniopsida (superclass IV)

1 Class Fossombroniopsida WFrey amp Hilger

Plants thallose Antheridia in acropetal sequence on upper surface of axis Oil-bodiessmall numerous Capsule mostly lacking valves wall disintegrating into fragmentsor via irregular lines into unequal valves from apex downwards Capsule wall 2-4(-6)-layered Spores areolate or with irregular lamellae or spinose on distal surfaceElaterophore lacking elaters 2-3-helical Probably of Gondwanan origin

Order Fossombroniales Schljakov

Fam Fossombroniaceae Hazsl

Main axis with obliquely inserted succubous leaves (leaf-like lobes) Rhizoids purplish(rarely pale brown) Antheridia and archegonia in simple acropetal sequence Antheridianaked Sporophyte protected by a caulocalyx Capsule wall without wall thickeningsGametophyte-sporophyte junction 1 sporophyte and 2-3 gametophyte placental transfercell layers cells with thin wall ingrowths strongly reminescent of the placenta inTreubia and Haplomitrium gametophyte placenta transfer cells with strongly branchedwall ingrowths (resembling those of Blasia and Marchantiopsida) a bulbous foot andabsence of a collar support exclusion of Fossombronia from the Jungermanniopsida -2 genera (c 92) worldwide distribution - Austrofossombronia RMSchust (2)subantarctic Andes (Peru-Venezuela) - Fossombronia Raddi (c 90) from subarctic tosubantarctic regions centre of diversification in Australia (33 spp) TheFossombroniaceae are strongly supported as monophyletic in molecular analyses withAllisonia and Petalophyllum as sister groups (Forrest amp Crandall-Stotler 2005) Thetaxon is thought to be very isolated immensely old and relict (Schuster 1984a)

Fam Petalophyllaceae (RMSchust) Stotler amp Stotl-Crand

Thallus with unistratose dorsal lamellae radiating from midrib to margin or unistratosethallus wings Archegonia clustered rather than scattered Sporophyte protected by apseudoperianth Capsule wall with outer wall thickenings - 2 genera (7) -

63

Petalophyllum Nees amp Gottsche ex Lehm (6) New Zealand (2) 1 species each inW Australia India and S USA P ralfsii (Wils) Nees amp Gottsche medit-atlant WEurope N Africa - Sewardiella Kashyap (1) W Himalayas

Fam Allisoniaceae (RMSchust ex Grolle) Schljakov

Plants thallose Midrib of thallus ill-defined Central strand lacking DioicousAntheridia individually protected by a scale Capsule spherical wall irregularly tearinginto 5-7 unequal valves epidermal cells with irregular bands without elaterophoreSpores strongly sculptured - 2 genera (5) - Allisonia Herzog (1) endemic NewZealand - Calycularia Mitt (4) N and E Asia Himalayas

Molecular data indicate that the Allisoniaceae are not monophyletic Both generahave similar capsule walls and thallus structures but differ by the presence of awell-developed pseudoperianth in Calycularia (eg Inoue 1976) The placement ofCalycularia has traditionally been problematic and is still tentative based on itsposition sister to the Fossombronialean and Pallavicinialean liverworts in moleculartrees

Fam Sandeothallaceae RM Schust

Plants thallose Thalli simple or rarely branched with uniseriate slime hairs occasionalwith ventral branches Rhizoids reddish Antheridia in axils of dorsal scales alongmidrib surface Seta massive Capsule wall (3)4-5(6)-layered opening by 2 lateralslits without elaterophore - Monotypic - Sandeothallus RMSchust (1) IndiaMalesia Samoa

The systematic position remains ambiguous Morphologically Sandeothallus occupiesan intermediate position gametophytic characters indicate close relationship toAllisoniaceae whereas sporophytically it is close to the Pallaviciniaceae (Schuster1982) Molecular data are so far not available

2 Class Pallaviciniopsida WFrey amp Stech class nov

Plantae thallinae prostratae vel in axem prostratum stipitemque erectum divisae partim dendroideaeCosta thalli prominens 1 vel 2(-4) filis centralibus Cellulae filorum centralium elongatae perforataehydroideis similes Capsulae ovoideae ad cylindricae 2 vel 4 valvis dehiscentes

Type family Pallaviciniaceae Mig

Plants thallose prostrate erect or sometimes dendroid Dendroid taxa evolved threetimes independently in Jensenia and Symphyogyna (Pallaviciniaceae) as well as inHymenophyton (Hymenophytaceae) (Schaumann et al 2005) Gametophyte mostlywith central strand composed of thick-walled elongated water-conducting cells withperforations (pores) This pallavicinoid type of water-conducting cells occurs onlyin the Pallaviciniopsida and is unique in bryophytes Antheridia and archegonia(clustered) on dorsal surface of thallus Sporophyte protected by a pseudoperianth(inner involucre) or stem-calyptra Seta massive Capsule ellipsoidal to cylindricaltearing into 2 imperfectly 4 or 4 valves wall bistratose Gametophyte-sporophytejunction gametophyte placental cells without wall ingrowths sporophyte placental

64

cells partly without wall ingrowths Fossil records Pallaviciniites devonicus (Hueber)RMSchust from lowermost Upper Devonian (375 mio y) is the oldest true bryo-phyte fossil known The thallose plant bearing a central strand in the gametophyteaxis is superficially similar to the Pallaviciniaceae in particular to Pallavicinia andSymphyogyna Laticaulina papillosa Krassilov from Late Jurassic of Russia alsoshows affinities to the Pallaviciniopsida (Symphyogyna) About 65 species

1 Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Basionym Pallaviciniineae RMSchust Phytologia 56 65 1984

Type (and only) family Pallaviciniaceae Mig

Schuster (1984b) erected the Pallaviciniineae to include PallaviciniaceaeSandeothallaceae and Makinoaceae In contrast we consider the Pallavicinialesmonotypic at least until relationships of Sandeothallus and Makinoa have beenclarified on the molecular level

Fam Pallaviciniaceae Mig

Plants thallose prostrate without basal stipe and ldquorhizomerdquo or erect arising froma ldquorhizomerdquo or stipe dendroid in Jensenia and some species of Pallavicinia andSymphyogyna Thallus with well-defined midrib with 1 or 2(-4) central strandsin most taxa present and unistratose lamina Water conducting cells elongatedwith tapering ends and thickened walls (c 8 microm wide and up to 300 microm long)throughout with numerous pits produced by dissolution of secondary wallmaterial associated with modified plasmodesmata Only few true plasmodesmata-derived perforations (pores) present (Oslash 200-400 nm) No relationship withtracheids (Frey et al 1996) Slime papillae on both dorsal and ventral surfacesof apex sometimes present Ventral scales absent or small and uniseriate DioicousAntheridia on dorsal surface of thallus often in 2-several ranks associated withscales Archegonia clustered on dorsal surface of midrib (gynoecia) deliminatedby a single (Symphyogyna) or double involucres (except Xenothallus) Developingsporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-calyptra Seta long massive Capsule elongate-cylindrical to ovoid dehiscenceby 2 or imperfectly 4 valves epidermal cell walls lacking thickenings Spores 1-celled Elaterophore rudimentary or absent Elaters 2-3-helical Gametophyte-sporophyte junction Wall ingrowths (transfer cells) present in the outermostsporophytic placental layer - 9 genera (c 60) Gondwanan centres of diversityin Australasia and S America

Molecular analyses resolve Pallaviciniaceae as monophyletic (eg Forrest ampCrandall-Stotler 2005 Schaumann et al 2005) These data support a separationof Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa a positionof Podomitrium (Podomitrioideae RMSchust) close to the Symphyogynoideae(Trevis) RMSchust ex Grolle and polyphyly of Pallavicinia and thePallavicinioideae Because of ambiguous relationships between these subfamilieswe include Podomitrioideae and Symphyogynoideae in Pallavicinioideae sl

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

57

Table 1 Distribution of transfer cells (layers) and foot shape in the gametophyte-sporophyte junctionin the liverworts (Hepaticophytina) For further details see Frey et al (2001) and Carafa et al (2003)

Class Subclass Order Family Transfer cells (layers) Foot shapeGametophyte Sporophyte

One to several layers of transfer cells on both sides of the placenta

Superclass ITreubiopsida Treubiaceae ndash +(1-2) bulbous

+(3-4) +(2-3) bulbousHaplomitriopsida Haplomitriaceae +(2-3) +(1-2) bulbous

Superclass IIBlasiopsida Blasiaceae +(2-3) +(1) conicalMarchantiopsida Sphaerocarpidae Sphaerocarpales +(2ndash3) +(1) spheroidal

Marchantiidae Monocleales +(4-6) +(2) conicalMarchantiales +(2-4) +(1) spheroidal

+(1-2) conicalbulbouscylindricalcup-shaped

Ricciales ndash ndash ndashSuperclass IIIFossombroniopsida Fossombroniaceae +(2-3) +(1) bulbous

Reduction of gametophyte and mostly also sporophyte transfer cells (wall ingrowths)

Pallaviciniopsida Pallaviciniaceae ndash +(1) conicalHymenophytaceae ndash ndash conical

Pelliopsida Pelliaceae ndash ndash conical

Superclass IVJungermanniopsida Jungermanniidae div families ndash +(1) conical bul-

ndash +(1-2) bousspheroidal

Metzgeriidae Aneuraceae ndash ndash conical(Riccardia) +(2) ndash conicalMetzgeriaceae ndash ndash conical

Systematic arrangement of taxa

Superclass I

1 Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Fam Treubiaceae Verd

Characterized by the unique ldquoleafyrdquo growth form with 2 lateral rows of alternatesuccubous lobes (interpreted as leafy appendages) and transversely oriented dorsallobules (scales) dimorphic leaf cells (scattered cells containing 1 large oil-body

58

Fig 1 Phylogenetic relationships of the higher taxa of Hepaticophytina indicating the approximatetime of divergence of the groups in line with assignable fossil records and distribution of characteristicgametophyte-sporophyte junction types 1 With several layers of transfer cells on both side of theplacenta 2 Sporophyte transfer cells (stc) wall ingrowths relatively thin and highly branched 3 Stcwall ingrowths highly branched and anastomosing of high structural complexity wall ingrowths ingametophyte transfer cells (gtc) partly short and coarse 4 Gametophyte placental cells without wallingrowths 5 Partly sporophyte placental cells without wall ingrowths 6 Sporophyte and gametophyteplacental cells without wall ingrowths Abbreviations g gametophyte ju gametophyte-sporophytejunction with placenta s sporophyte Blob Blasiites lobatus Gspp Gessella spp GsalGrisellatheca salopensis Hlan Hepaticites langii Jgra Jungermanniites gracilis Jkeu Jkeuperianus Lpap Laticaulina papillosa Mcya Marchantites cyathodoides MmetMetzgeriothallus metzgerioides Mplu Muscites plumatus Nlan Naiadita lanceolata PdevPallaviciniites devonicus Tkid Treubiites kidstonii

59

other cells only with chloroplasts) and slime papillae on ventral surface producinga thick covering of mucilage (otherwise only in Verdoorniaceae) Blepharoplast ofCalobryalean affinity lamellar strip (spline) with up to 104 microtubules (widest inbryophytes) open spline aperture overlap between anterior and posterior basal bodiesGametophyte-sporophyte junction either resembling that of Jungermanniopsida(Apotreubia gametophyte placental cells lacking wall ingrowths) or similar toFossombronia and Haplomitrium (Treubia several layers of transfer cells on bothside of the placenta with thin wall ingrowths) No fossil records known - 2 genera(11 species) distribution pattern originally Pangaean - Treubia KIGoebel (7)basically Gondwanan Malesia Australasia Oceania (S Pacific) rather recenttransgression of Wallacersquos line 1 species in Chile not represented in Africa -Apotreubia SHatt amp Mizut (4) predominantly Laurasian

Based on morphological characters the two extant genera Treubia and Apotreubiamay be regarded as the most archaic living fossils in liverworts and extant models ofan extinct plant group In molecular trees Treubiopsida are resolved as sister to allother liverworts either alone (eg Stech amp Frey 2001) or together with Haplomitrium(eg Forrest amp Crandall-Stotler 2005) similar to cladistic analyses based on malegametogenesis characters (Garbary et al 1993) Heinrichs et al (2005) recentlyincluded Treubiopsida in the Haplomitriopsida however with respect to themorphological and anatomical differences and the fact that at least some of theshared characters states (eg tetrahedral apical cells or the type of the gametophyte-sporophyte junction) are probably ancestral plesiomorphies we prefer to maintaintwo classes united in a single superclass

2 Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Fam Haplomitriaceae Dbulldehellipek

Unique features upright habit subterranean creeping axis (ldquorhizomerdquo) undividedleafy appendages ldquoisophyllousrdquo with transversely inserted ldquoleavesrdquo (some speciestend toward ldquoanisophyllyrdquo and succubous insertion) rhizoids lacking central strandpresent water-conducting cells resembling that of Takakia scattered gametangia indiffuse groups laterally along the stem without specialized protective bracts massiveseta and an extensive stem-calyptra Blepharoplast structure spline with up to 90microtubules spline aperture on the left side Gametophyte-sporophyte junction 1-2 sporophyte and 2-3 gametophyte placental cell layers gametophyte transfer cellswith highly branched and thin long wall ingrowths similar to Treubia andFossombronia foot bulbous collar absent Fossil records Gessella Poulsen (2) fromLower Permian Denmark Naiadita lanceolata PBBrodie from Upper Triassic ofEngland is discussed to belong to either Haplomitriopsida or Marchantiopsida subclassSphaerocarpidae - Monotypic - Haplomitrium Nees (9) basically Gondwanan centerof diversity in Australasia

Haplomitrium is morphologically and anatomically isolated by a ldquoserious offundamental criteriardquo (Schuster 1984a) and regarded as an early-diverging lineagewithin liverworts The precise placement of Haplomitrium in molecular trees has

60

been problematic and varies depending on taxon sampling especially the inclusionvs exclusion of Treubia and the applied method (summarized by Shaw amp Renzaglia2004) Cladistic analyses of male gametogenesis characters (Garbary et al 1993)and recent molecular analyses including Treubia (eg Forrest amp Crandall-Stotler2005) revealed that Haplomitrium plus Treubia form a clade sister to all otherliverworts groups

Superclass II

1 Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Fam Blasiaceae HKlinggr

Thallus with ill-defined midrib grading into unistratose wings (leafy habit) incolonies Central strand lacking 2 rows of flattened multicellular scales (as incomplex thallose liverworts) irregularly dentate on ventral surface of thallusSmall ventral hemispherical lsquoauriclesrsquo filled with Nostoc colonies and uniqueflasked-shaped gemma-receptacles present (unique in liverworts) Marchantialeanblepharoplast type Gametophyte-sporophyte junction 1 sporophyte and 2-3gametophyte placental cell layers with Marchantialean-type wall ingrowths (transfercells) Fossil records The Late Carboniferous Blasiites lobatus (JWalton)RMSchust resembling Blasia pusilla is supposed to be an ancestor of the extanttaxa (however see Pelliopsida) The Carboniferous Treubiites kidstonii (JWalton)RMSchust with lateral succubously shingled leaves and ventral scales (as in Blasia)is rejected as a presumable precursor of Treubiopsida but serves as a model fromwhich the more frondose semithallose extant Blasia may be derived - 2 monotypicgenera - Blasia L circumboreal - Cavicularia Steph endemic Japan

Blasia was traditionally included in the Metzgerialean group but blepharoplastultrastructure and a Marchantialean-type gametophyte-sporophyte junction assignit to the Marchantiopsida Similarly latest molecular results resolve Blasia andCavicularia as sister to the Marchantiopsida (Forrest amp Crandall-Stotler 2005)with maximum bootstrap support whereas earlier molecular analyses of Blasiaeither suggested a somewhat intermediate position between Marchantiopsida andJungermanniopsida (Wheeler 2000 Stech amp Frey 2001) or a basal position withinliverworts (He-Nygreacuten et al 2004) The molecular separation of Blasia andCavicularia in Forrest amp Crandall-Stotler (2004) and Heinrichs et al (2005)was caused by contaminated Cavicularia DNA (cf Forrest amp Crandall-Stotler2005)

2 Class Marchantiopsida Stotler amp Stotl-Crand

Thirty-two genera with c 350 species Highest differentiated gametophytes in theplant kingdom Blepharoplast structure uniform closed apertures three splinemicrotubules wide Gametophyte-sporophyte junction 1-2 sporophyte and 2-4gametophyte placental cell layers cells of both layers with characteristic wallingrowths (highly branched and anastomosing or short and coarse respectively

61

Marchantialean type) Fossil records Some enigmatic Lower Devonian microfossils(epidermal surface tissues rhizoids) may be regarded as the remains of earlyMarchantioid liverworts (Graham et al 2004) Convincing Marchantioid fossilsobviously unknown from Lower Palaeophytic starting with the Lower PermianMarchantites loreus Zalessky (incertae sedis) the unequivocal Middle TriassicMarchantites cyathodoides (Townrow) HMAnderson and M tennantii HMAndersonand becoming relatively species rich from Triassic to Eocene Probably the initialdiversification of the Marchantiopsida took place at the beginning of the relativelyarid Mesophytic followed by a rapid radiation of Marchantioid taxa coincidentwith extreme conditions and ecological reorganisation in Upper Permo-Triassictime

Monophyly of the Marchantiopsida is strongly supported by all respective molecularanalyses

1 Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Fam Sphaerocarpaceae (Dumort) Heeg

Leafy habit Marchantialean blepharoplast type and gametophyte-sporophyte junctionNo fossils known - 2 genera - Sphaerocarpus Boehm and the monotypic GeothallusCampb

Fam Riellaceae Engl

Monotypic Riella Mont

2 Subclass Marchantiidae Engl

1 Order Monocleales RMSchust

Ancient relict group with plesiomorphic characters eg simple thallus and capsuleopening by only one lateral slit Typical Marchantialean blepharoplast andgametophyte-sporophyte junction type as well as molecular data (eg Meiszligner etal 1998 Wheeler 2000 Forrest amp Crandall-Stotler 2005) support the currentclassification in the Marchantiidae No fossils known - Monotypic - MonocleaHook (2) probably of Gondwanan origin restricted to hyperhygric habitats

2 Order Marchantiales Limpr in Cohn

12 families (see synopsis below) with 25 genera For subdivision of the order seeCrandall-Stotler amp Stotler (2000)

3 Order Ricciales Schljakov

2 families Oxymitraceae MuumlllFrib ex Grolle (Oxymitra Bisch ex Lindenb) andRicciaceae Reichenb with 2 genera Riccia L and the monotypic RicciocarposCorda

62

Superclass III

Recent molecular analyses based on larger taxon sampling (Davis 2004 He-Nygreacutenet al 2004 Stech amp Frey 2004 Forrest amp Crandall-Stotler 2004 2005 Heinrichs etal 2005) revealed that the simple thallose liverworts formerly comprised asJungermanniopsida subclass Metzgeriidae (sl) with 15 families 38 genera and c500 species are not monophyletic These taxa which form leaf-like lobes or thalluswings from a single wedge-shaped apical cell and are basically anacrogynous(Jungermanniales anacrogynae) are split into two main groups The first group(Metzgeriales II sensu Forrest amp Crandall-Stotler 2004) comprises different types ofsimple thallose or semileafy liverworts which are here divided into three classesFossombroniopsida Pallaviciniopsida and Pelliopsida The simple thalloseMetzgerialean liverworts (Metzgeriales I sensu Forrest amp Crandall-Stotler 2004)compose the second group that is sister to the leafy liverworts and thus treated assubclass Metzgeriidae sstr of the Jungermanniopsida (superclass IV)

1 Class Fossombroniopsida WFrey amp Hilger

Plants thallose Antheridia in acropetal sequence on upper surface of axis Oil-bodiessmall numerous Capsule mostly lacking valves wall disintegrating into fragmentsor via irregular lines into unequal valves from apex downwards Capsule wall 2-4(-6)-layered Spores areolate or with irregular lamellae or spinose on distal surfaceElaterophore lacking elaters 2-3-helical Probably of Gondwanan origin

Order Fossombroniales Schljakov

Fam Fossombroniaceae Hazsl

Main axis with obliquely inserted succubous leaves (leaf-like lobes) Rhizoids purplish(rarely pale brown) Antheridia and archegonia in simple acropetal sequence Antheridianaked Sporophyte protected by a caulocalyx Capsule wall without wall thickeningsGametophyte-sporophyte junction 1 sporophyte and 2-3 gametophyte placental transfercell layers cells with thin wall ingrowths strongly reminescent of the placenta inTreubia and Haplomitrium gametophyte placenta transfer cells with strongly branchedwall ingrowths (resembling those of Blasia and Marchantiopsida) a bulbous foot andabsence of a collar support exclusion of Fossombronia from the Jungermanniopsida -2 genera (c 92) worldwide distribution - Austrofossombronia RMSchust (2)subantarctic Andes (Peru-Venezuela) - Fossombronia Raddi (c 90) from subarctic tosubantarctic regions centre of diversification in Australia (33 spp) TheFossombroniaceae are strongly supported as monophyletic in molecular analyses withAllisonia and Petalophyllum as sister groups (Forrest amp Crandall-Stotler 2005) Thetaxon is thought to be very isolated immensely old and relict (Schuster 1984a)

Fam Petalophyllaceae (RMSchust) Stotler amp Stotl-Crand

Thallus with unistratose dorsal lamellae radiating from midrib to margin or unistratosethallus wings Archegonia clustered rather than scattered Sporophyte protected by apseudoperianth Capsule wall with outer wall thickenings - 2 genera (7) -

63

Petalophyllum Nees amp Gottsche ex Lehm (6) New Zealand (2) 1 species each inW Australia India and S USA P ralfsii (Wils) Nees amp Gottsche medit-atlant WEurope N Africa - Sewardiella Kashyap (1) W Himalayas

Fam Allisoniaceae (RMSchust ex Grolle) Schljakov

Plants thallose Midrib of thallus ill-defined Central strand lacking DioicousAntheridia individually protected by a scale Capsule spherical wall irregularly tearinginto 5-7 unequal valves epidermal cells with irregular bands without elaterophoreSpores strongly sculptured - 2 genera (5) - Allisonia Herzog (1) endemic NewZealand - Calycularia Mitt (4) N and E Asia Himalayas

Molecular data indicate that the Allisoniaceae are not monophyletic Both generahave similar capsule walls and thallus structures but differ by the presence of awell-developed pseudoperianth in Calycularia (eg Inoue 1976) The placement ofCalycularia has traditionally been problematic and is still tentative based on itsposition sister to the Fossombronialean and Pallavicinialean liverworts in moleculartrees

Fam Sandeothallaceae RM Schust

Plants thallose Thalli simple or rarely branched with uniseriate slime hairs occasionalwith ventral branches Rhizoids reddish Antheridia in axils of dorsal scales alongmidrib surface Seta massive Capsule wall (3)4-5(6)-layered opening by 2 lateralslits without elaterophore - Monotypic - Sandeothallus RMSchust (1) IndiaMalesia Samoa

The systematic position remains ambiguous Morphologically Sandeothallus occupiesan intermediate position gametophytic characters indicate close relationship toAllisoniaceae whereas sporophytically it is close to the Pallaviciniaceae (Schuster1982) Molecular data are so far not available

2 Class Pallaviciniopsida WFrey amp Stech class nov

Plantae thallinae prostratae vel in axem prostratum stipitemque erectum divisae partim dendroideaeCosta thalli prominens 1 vel 2(-4) filis centralibus Cellulae filorum centralium elongatae perforataehydroideis similes Capsulae ovoideae ad cylindricae 2 vel 4 valvis dehiscentes

Type family Pallaviciniaceae Mig

Plants thallose prostrate erect or sometimes dendroid Dendroid taxa evolved threetimes independently in Jensenia and Symphyogyna (Pallaviciniaceae) as well as inHymenophyton (Hymenophytaceae) (Schaumann et al 2005) Gametophyte mostlywith central strand composed of thick-walled elongated water-conducting cells withperforations (pores) This pallavicinoid type of water-conducting cells occurs onlyin the Pallaviciniopsida and is unique in bryophytes Antheridia and archegonia(clustered) on dorsal surface of thallus Sporophyte protected by a pseudoperianth(inner involucre) or stem-calyptra Seta massive Capsule ellipsoidal to cylindricaltearing into 2 imperfectly 4 or 4 valves wall bistratose Gametophyte-sporophytejunction gametophyte placental cells without wall ingrowths sporophyte placental

64

cells partly without wall ingrowths Fossil records Pallaviciniites devonicus (Hueber)RMSchust from lowermost Upper Devonian (375 mio y) is the oldest true bryo-phyte fossil known The thallose plant bearing a central strand in the gametophyteaxis is superficially similar to the Pallaviciniaceae in particular to Pallavicinia andSymphyogyna Laticaulina papillosa Krassilov from Late Jurassic of Russia alsoshows affinities to the Pallaviciniopsida (Symphyogyna) About 65 species

1 Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Basionym Pallaviciniineae RMSchust Phytologia 56 65 1984

Type (and only) family Pallaviciniaceae Mig

Schuster (1984b) erected the Pallaviciniineae to include PallaviciniaceaeSandeothallaceae and Makinoaceae In contrast we consider the Pallavicinialesmonotypic at least until relationships of Sandeothallus and Makinoa have beenclarified on the molecular level

Fam Pallaviciniaceae Mig

Plants thallose prostrate without basal stipe and ldquorhizomerdquo or erect arising froma ldquorhizomerdquo or stipe dendroid in Jensenia and some species of Pallavicinia andSymphyogyna Thallus with well-defined midrib with 1 or 2(-4) central strandsin most taxa present and unistratose lamina Water conducting cells elongatedwith tapering ends and thickened walls (c 8 microm wide and up to 300 microm long)throughout with numerous pits produced by dissolution of secondary wallmaterial associated with modified plasmodesmata Only few true plasmodesmata-derived perforations (pores) present (Oslash 200-400 nm) No relationship withtracheids (Frey et al 1996) Slime papillae on both dorsal and ventral surfacesof apex sometimes present Ventral scales absent or small and uniseriate DioicousAntheridia on dorsal surface of thallus often in 2-several ranks associated withscales Archegonia clustered on dorsal surface of midrib (gynoecia) deliminatedby a single (Symphyogyna) or double involucres (except Xenothallus) Developingsporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-calyptra Seta long massive Capsule elongate-cylindrical to ovoid dehiscenceby 2 or imperfectly 4 valves epidermal cell walls lacking thickenings Spores 1-celled Elaterophore rudimentary or absent Elaters 2-3-helical Gametophyte-sporophyte junction Wall ingrowths (transfer cells) present in the outermostsporophytic placental layer - 9 genera (c 60) Gondwanan centres of diversityin Australasia and S America

Molecular analyses resolve Pallaviciniaceae as monophyletic (eg Forrest ampCrandall-Stotler 2005 Schaumann et al 2005) These data support a separationof Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa a positionof Podomitrium (Podomitrioideae RMSchust) close to the Symphyogynoideae(Trevis) RMSchust ex Grolle and polyphyly of Pallavicinia and thePallavicinioideae Because of ambiguous relationships between these subfamilieswe include Podomitrioideae and Symphyogynoideae in Pallavicinioideae sl

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

58

Fig 1 Phylogenetic relationships of the higher taxa of Hepaticophytina indicating the approximatetime of divergence of the groups in line with assignable fossil records and distribution of characteristicgametophyte-sporophyte junction types 1 With several layers of transfer cells on both side of theplacenta 2 Sporophyte transfer cells (stc) wall ingrowths relatively thin and highly branched 3 Stcwall ingrowths highly branched and anastomosing of high structural complexity wall ingrowths ingametophyte transfer cells (gtc) partly short and coarse 4 Gametophyte placental cells without wallingrowths 5 Partly sporophyte placental cells without wall ingrowths 6 Sporophyte and gametophyteplacental cells without wall ingrowths Abbreviations g gametophyte ju gametophyte-sporophytejunction with placenta s sporophyte Blob Blasiites lobatus Gspp Gessella spp GsalGrisellatheca salopensis Hlan Hepaticites langii Jgra Jungermanniites gracilis Jkeu Jkeuperianus Lpap Laticaulina papillosa Mcya Marchantites cyathodoides MmetMetzgeriothallus metzgerioides Mplu Muscites plumatus Nlan Naiadita lanceolata PdevPallaviciniites devonicus Tkid Treubiites kidstonii

59

other cells only with chloroplasts) and slime papillae on ventral surface producinga thick covering of mucilage (otherwise only in Verdoorniaceae) Blepharoplast ofCalobryalean affinity lamellar strip (spline) with up to 104 microtubules (widest inbryophytes) open spline aperture overlap between anterior and posterior basal bodiesGametophyte-sporophyte junction either resembling that of Jungermanniopsida(Apotreubia gametophyte placental cells lacking wall ingrowths) or similar toFossombronia and Haplomitrium (Treubia several layers of transfer cells on bothside of the placenta with thin wall ingrowths) No fossil records known - 2 genera(11 species) distribution pattern originally Pangaean - Treubia KIGoebel (7)basically Gondwanan Malesia Australasia Oceania (S Pacific) rather recenttransgression of Wallacersquos line 1 species in Chile not represented in Africa -Apotreubia SHatt amp Mizut (4) predominantly Laurasian

Based on morphological characters the two extant genera Treubia and Apotreubiamay be regarded as the most archaic living fossils in liverworts and extant models ofan extinct plant group In molecular trees Treubiopsida are resolved as sister to allother liverworts either alone (eg Stech amp Frey 2001) or together with Haplomitrium(eg Forrest amp Crandall-Stotler 2005) similar to cladistic analyses based on malegametogenesis characters (Garbary et al 1993) Heinrichs et al (2005) recentlyincluded Treubiopsida in the Haplomitriopsida however with respect to themorphological and anatomical differences and the fact that at least some of theshared characters states (eg tetrahedral apical cells or the type of the gametophyte-sporophyte junction) are probably ancestral plesiomorphies we prefer to maintaintwo classes united in a single superclass

2 Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Fam Haplomitriaceae Dbulldehellipek

Unique features upright habit subterranean creeping axis (ldquorhizomerdquo) undividedleafy appendages ldquoisophyllousrdquo with transversely inserted ldquoleavesrdquo (some speciestend toward ldquoanisophyllyrdquo and succubous insertion) rhizoids lacking central strandpresent water-conducting cells resembling that of Takakia scattered gametangia indiffuse groups laterally along the stem without specialized protective bracts massiveseta and an extensive stem-calyptra Blepharoplast structure spline with up to 90microtubules spline aperture on the left side Gametophyte-sporophyte junction 1-2 sporophyte and 2-3 gametophyte placental cell layers gametophyte transfer cellswith highly branched and thin long wall ingrowths similar to Treubia andFossombronia foot bulbous collar absent Fossil records Gessella Poulsen (2) fromLower Permian Denmark Naiadita lanceolata PBBrodie from Upper Triassic ofEngland is discussed to belong to either Haplomitriopsida or Marchantiopsida subclassSphaerocarpidae - Monotypic - Haplomitrium Nees (9) basically Gondwanan centerof diversity in Australasia

Haplomitrium is morphologically and anatomically isolated by a ldquoserious offundamental criteriardquo (Schuster 1984a) and regarded as an early-diverging lineagewithin liverworts The precise placement of Haplomitrium in molecular trees has

60

been problematic and varies depending on taxon sampling especially the inclusionvs exclusion of Treubia and the applied method (summarized by Shaw amp Renzaglia2004) Cladistic analyses of male gametogenesis characters (Garbary et al 1993)and recent molecular analyses including Treubia (eg Forrest amp Crandall-Stotler2005) revealed that Haplomitrium plus Treubia form a clade sister to all otherliverworts groups

Superclass II

1 Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Fam Blasiaceae HKlinggr

Thallus with ill-defined midrib grading into unistratose wings (leafy habit) incolonies Central strand lacking 2 rows of flattened multicellular scales (as incomplex thallose liverworts) irregularly dentate on ventral surface of thallusSmall ventral hemispherical lsquoauriclesrsquo filled with Nostoc colonies and uniqueflasked-shaped gemma-receptacles present (unique in liverworts) Marchantialeanblepharoplast type Gametophyte-sporophyte junction 1 sporophyte and 2-3gametophyte placental cell layers with Marchantialean-type wall ingrowths (transfercells) Fossil records The Late Carboniferous Blasiites lobatus (JWalton)RMSchust resembling Blasia pusilla is supposed to be an ancestor of the extanttaxa (however see Pelliopsida) The Carboniferous Treubiites kidstonii (JWalton)RMSchust with lateral succubously shingled leaves and ventral scales (as in Blasia)is rejected as a presumable precursor of Treubiopsida but serves as a model fromwhich the more frondose semithallose extant Blasia may be derived - 2 monotypicgenera - Blasia L circumboreal - Cavicularia Steph endemic Japan

Blasia was traditionally included in the Metzgerialean group but blepharoplastultrastructure and a Marchantialean-type gametophyte-sporophyte junction assignit to the Marchantiopsida Similarly latest molecular results resolve Blasia andCavicularia as sister to the Marchantiopsida (Forrest amp Crandall-Stotler 2005)with maximum bootstrap support whereas earlier molecular analyses of Blasiaeither suggested a somewhat intermediate position between Marchantiopsida andJungermanniopsida (Wheeler 2000 Stech amp Frey 2001) or a basal position withinliverworts (He-Nygreacuten et al 2004) The molecular separation of Blasia andCavicularia in Forrest amp Crandall-Stotler (2004) and Heinrichs et al (2005)was caused by contaminated Cavicularia DNA (cf Forrest amp Crandall-Stotler2005)

2 Class Marchantiopsida Stotler amp Stotl-Crand

Thirty-two genera with c 350 species Highest differentiated gametophytes in theplant kingdom Blepharoplast structure uniform closed apertures three splinemicrotubules wide Gametophyte-sporophyte junction 1-2 sporophyte and 2-4gametophyte placental cell layers cells of both layers with characteristic wallingrowths (highly branched and anastomosing or short and coarse respectively

61

Marchantialean type) Fossil records Some enigmatic Lower Devonian microfossils(epidermal surface tissues rhizoids) may be regarded as the remains of earlyMarchantioid liverworts (Graham et al 2004) Convincing Marchantioid fossilsobviously unknown from Lower Palaeophytic starting with the Lower PermianMarchantites loreus Zalessky (incertae sedis) the unequivocal Middle TriassicMarchantites cyathodoides (Townrow) HMAnderson and M tennantii HMAndersonand becoming relatively species rich from Triassic to Eocene Probably the initialdiversification of the Marchantiopsida took place at the beginning of the relativelyarid Mesophytic followed by a rapid radiation of Marchantioid taxa coincidentwith extreme conditions and ecological reorganisation in Upper Permo-Triassictime

Monophyly of the Marchantiopsida is strongly supported by all respective molecularanalyses

1 Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Fam Sphaerocarpaceae (Dumort) Heeg

Leafy habit Marchantialean blepharoplast type and gametophyte-sporophyte junctionNo fossils known - 2 genera - Sphaerocarpus Boehm and the monotypic GeothallusCampb

Fam Riellaceae Engl

Monotypic Riella Mont

2 Subclass Marchantiidae Engl

1 Order Monocleales RMSchust

Ancient relict group with plesiomorphic characters eg simple thallus and capsuleopening by only one lateral slit Typical Marchantialean blepharoplast andgametophyte-sporophyte junction type as well as molecular data (eg Meiszligner etal 1998 Wheeler 2000 Forrest amp Crandall-Stotler 2005) support the currentclassification in the Marchantiidae No fossils known - Monotypic - MonocleaHook (2) probably of Gondwanan origin restricted to hyperhygric habitats

2 Order Marchantiales Limpr in Cohn

12 families (see synopsis below) with 25 genera For subdivision of the order seeCrandall-Stotler amp Stotler (2000)

3 Order Ricciales Schljakov

2 families Oxymitraceae MuumlllFrib ex Grolle (Oxymitra Bisch ex Lindenb) andRicciaceae Reichenb with 2 genera Riccia L and the monotypic RicciocarposCorda

62

Superclass III

Recent molecular analyses based on larger taxon sampling (Davis 2004 He-Nygreacutenet al 2004 Stech amp Frey 2004 Forrest amp Crandall-Stotler 2004 2005 Heinrichs etal 2005) revealed that the simple thallose liverworts formerly comprised asJungermanniopsida subclass Metzgeriidae (sl) with 15 families 38 genera and c500 species are not monophyletic These taxa which form leaf-like lobes or thalluswings from a single wedge-shaped apical cell and are basically anacrogynous(Jungermanniales anacrogynae) are split into two main groups The first group(Metzgeriales II sensu Forrest amp Crandall-Stotler 2004) comprises different types ofsimple thallose or semileafy liverworts which are here divided into three classesFossombroniopsida Pallaviciniopsida and Pelliopsida The simple thalloseMetzgerialean liverworts (Metzgeriales I sensu Forrest amp Crandall-Stotler 2004)compose the second group that is sister to the leafy liverworts and thus treated assubclass Metzgeriidae sstr of the Jungermanniopsida (superclass IV)

1 Class Fossombroniopsida WFrey amp Hilger

Plants thallose Antheridia in acropetal sequence on upper surface of axis Oil-bodiessmall numerous Capsule mostly lacking valves wall disintegrating into fragmentsor via irregular lines into unequal valves from apex downwards Capsule wall 2-4(-6)-layered Spores areolate or with irregular lamellae or spinose on distal surfaceElaterophore lacking elaters 2-3-helical Probably of Gondwanan origin

Order Fossombroniales Schljakov

Fam Fossombroniaceae Hazsl

Main axis with obliquely inserted succubous leaves (leaf-like lobes) Rhizoids purplish(rarely pale brown) Antheridia and archegonia in simple acropetal sequence Antheridianaked Sporophyte protected by a caulocalyx Capsule wall without wall thickeningsGametophyte-sporophyte junction 1 sporophyte and 2-3 gametophyte placental transfercell layers cells with thin wall ingrowths strongly reminescent of the placenta inTreubia and Haplomitrium gametophyte placenta transfer cells with strongly branchedwall ingrowths (resembling those of Blasia and Marchantiopsida) a bulbous foot andabsence of a collar support exclusion of Fossombronia from the Jungermanniopsida -2 genera (c 92) worldwide distribution - Austrofossombronia RMSchust (2)subantarctic Andes (Peru-Venezuela) - Fossombronia Raddi (c 90) from subarctic tosubantarctic regions centre of diversification in Australia (33 spp) TheFossombroniaceae are strongly supported as monophyletic in molecular analyses withAllisonia and Petalophyllum as sister groups (Forrest amp Crandall-Stotler 2005) Thetaxon is thought to be very isolated immensely old and relict (Schuster 1984a)

Fam Petalophyllaceae (RMSchust) Stotler amp Stotl-Crand

Thallus with unistratose dorsal lamellae radiating from midrib to margin or unistratosethallus wings Archegonia clustered rather than scattered Sporophyte protected by apseudoperianth Capsule wall with outer wall thickenings - 2 genera (7) -

63

Petalophyllum Nees amp Gottsche ex Lehm (6) New Zealand (2) 1 species each inW Australia India and S USA P ralfsii (Wils) Nees amp Gottsche medit-atlant WEurope N Africa - Sewardiella Kashyap (1) W Himalayas

Fam Allisoniaceae (RMSchust ex Grolle) Schljakov

Plants thallose Midrib of thallus ill-defined Central strand lacking DioicousAntheridia individually protected by a scale Capsule spherical wall irregularly tearinginto 5-7 unequal valves epidermal cells with irregular bands without elaterophoreSpores strongly sculptured - 2 genera (5) - Allisonia Herzog (1) endemic NewZealand - Calycularia Mitt (4) N and E Asia Himalayas

Molecular data indicate that the Allisoniaceae are not monophyletic Both generahave similar capsule walls and thallus structures but differ by the presence of awell-developed pseudoperianth in Calycularia (eg Inoue 1976) The placement ofCalycularia has traditionally been problematic and is still tentative based on itsposition sister to the Fossombronialean and Pallavicinialean liverworts in moleculartrees

Fam Sandeothallaceae RM Schust

Plants thallose Thalli simple or rarely branched with uniseriate slime hairs occasionalwith ventral branches Rhizoids reddish Antheridia in axils of dorsal scales alongmidrib surface Seta massive Capsule wall (3)4-5(6)-layered opening by 2 lateralslits without elaterophore - Monotypic - Sandeothallus RMSchust (1) IndiaMalesia Samoa

The systematic position remains ambiguous Morphologically Sandeothallus occupiesan intermediate position gametophytic characters indicate close relationship toAllisoniaceae whereas sporophytically it is close to the Pallaviciniaceae (Schuster1982) Molecular data are so far not available

2 Class Pallaviciniopsida WFrey amp Stech class nov

Plantae thallinae prostratae vel in axem prostratum stipitemque erectum divisae partim dendroideaeCosta thalli prominens 1 vel 2(-4) filis centralibus Cellulae filorum centralium elongatae perforataehydroideis similes Capsulae ovoideae ad cylindricae 2 vel 4 valvis dehiscentes

Type family Pallaviciniaceae Mig

Plants thallose prostrate erect or sometimes dendroid Dendroid taxa evolved threetimes independently in Jensenia and Symphyogyna (Pallaviciniaceae) as well as inHymenophyton (Hymenophytaceae) (Schaumann et al 2005) Gametophyte mostlywith central strand composed of thick-walled elongated water-conducting cells withperforations (pores) This pallavicinoid type of water-conducting cells occurs onlyin the Pallaviciniopsida and is unique in bryophytes Antheridia and archegonia(clustered) on dorsal surface of thallus Sporophyte protected by a pseudoperianth(inner involucre) or stem-calyptra Seta massive Capsule ellipsoidal to cylindricaltearing into 2 imperfectly 4 or 4 valves wall bistratose Gametophyte-sporophytejunction gametophyte placental cells without wall ingrowths sporophyte placental

64

cells partly without wall ingrowths Fossil records Pallaviciniites devonicus (Hueber)RMSchust from lowermost Upper Devonian (375 mio y) is the oldest true bryo-phyte fossil known The thallose plant bearing a central strand in the gametophyteaxis is superficially similar to the Pallaviciniaceae in particular to Pallavicinia andSymphyogyna Laticaulina papillosa Krassilov from Late Jurassic of Russia alsoshows affinities to the Pallaviciniopsida (Symphyogyna) About 65 species

1 Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Basionym Pallaviciniineae RMSchust Phytologia 56 65 1984

Type (and only) family Pallaviciniaceae Mig

Schuster (1984b) erected the Pallaviciniineae to include PallaviciniaceaeSandeothallaceae and Makinoaceae In contrast we consider the Pallavicinialesmonotypic at least until relationships of Sandeothallus and Makinoa have beenclarified on the molecular level

Fam Pallaviciniaceae Mig

Plants thallose prostrate without basal stipe and ldquorhizomerdquo or erect arising froma ldquorhizomerdquo or stipe dendroid in Jensenia and some species of Pallavicinia andSymphyogyna Thallus with well-defined midrib with 1 or 2(-4) central strandsin most taxa present and unistratose lamina Water conducting cells elongatedwith tapering ends and thickened walls (c 8 microm wide and up to 300 microm long)throughout with numerous pits produced by dissolution of secondary wallmaterial associated with modified plasmodesmata Only few true plasmodesmata-derived perforations (pores) present (Oslash 200-400 nm) No relationship withtracheids (Frey et al 1996) Slime papillae on both dorsal and ventral surfacesof apex sometimes present Ventral scales absent or small and uniseriate DioicousAntheridia on dorsal surface of thallus often in 2-several ranks associated withscales Archegonia clustered on dorsal surface of midrib (gynoecia) deliminatedby a single (Symphyogyna) or double involucres (except Xenothallus) Developingsporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-calyptra Seta long massive Capsule elongate-cylindrical to ovoid dehiscenceby 2 or imperfectly 4 valves epidermal cell walls lacking thickenings Spores 1-celled Elaterophore rudimentary or absent Elaters 2-3-helical Gametophyte-sporophyte junction Wall ingrowths (transfer cells) present in the outermostsporophytic placental layer - 9 genera (c 60) Gondwanan centres of diversityin Australasia and S America

Molecular analyses resolve Pallaviciniaceae as monophyletic (eg Forrest ampCrandall-Stotler 2005 Schaumann et al 2005) These data support a separationof Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa a positionof Podomitrium (Podomitrioideae RMSchust) close to the Symphyogynoideae(Trevis) RMSchust ex Grolle and polyphyly of Pallavicinia and thePallavicinioideae Because of ambiguous relationships between these subfamilieswe include Podomitrioideae and Symphyogynoideae in Pallavicinioideae sl

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

59

other cells only with chloroplasts) and slime papillae on ventral surface producinga thick covering of mucilage (otherwise only in Verdoorniaceae) Blepharoplast ofCalobryalean affinity lamellar strip (spline) with up to 104 microtubules (widest inbryophytes) open spline aperture overlap between anterior and posterior basal bodiesGametophyte-sporophyte junction either resembling that of Jungermanniopsida(Apotreubia gametophyte placental cells lacking wall ingrowths) or similar toFossombronia and Haplomitrium (Treubia several layers of transfer cells on bothside of the placenta with thin wall ingrowths) No fossil records known - 2 genera(11 species) distribution pattern originally Pangaean - Treubia KIGoebel (7)basically Gondwanan Malesia Australasia Oceania (S Pacific) rather recenttransgression of Wallacersquos line 1 species in Chile not represented in Africa -Apotreubia SHatt amp Mizut (4) predominantly Laurasian

Based on morphological characters the two extant genera Treubia and Apotreubiamay be regarded as the most archaic living fossils in liverworts and extant models ofan extinct plant group In molecular trees Treubiopsida are resolved as sister to allother liverworts either alone (eg Stech amp Frey 2001) or together with Haplomitrium(eg Forrest amp Crandall-Stotler 2005) similar to cladistic analyses based on malegametogenesis characters (Garbary et al 1993) Heinrichs et al (2005) recentlyincluded Treubiopsida in the Haplomitriopsida however with respect to themorphological and anatomical differences and the fact that at least some of theshared characters states (eg tetrahedral apical cells or the type of the gametophyte-sporophyte junction) are probably ancestral plesiomorphies we prefer to maintaintwo classes united in a single superclass

2 Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Fam Haplomitriaceae Dbulldehellipek

Unique features upright habit subterranean creeping axis (ldquorhizomerdquo) undividedleafy appendages ldquoisophyllousrdquo with transversely inserted ldquoleavesrdquo (some speciestend toward ldquoanisophyllyrdquo and succubous insertion) rhizoids lacking central strandpresent water-conducting cells resembling that of Takakia scattered gametangia indiffuse groups laterally along the stem without specialized protective bracts massiveseta and an extensive stem-calyptra Blepharoplast structure spline with up to 90microtubules spline aperture on the left side Gametophyte-sporophyte junction 1-2 sporophyte and 2-3 gametophyte placental cell layers gametophyte transfer cellswith highly branched and thin long wall ingrowths similar to Treubia andFossombronia foot bulbous collar absent Fossil records Gessella Poulsen (2) fromLower Permian Denmark Naiadita lanceolata PBBrodie from Upper Triassic ofEngland is discussed to belong to either Haplomitriopsida or Marchantiopsida subclassSphaerocarpidae - Monotypic - Haplomitrium Nees (9) basically Gondwanan centerof diversity in Australasia

Haplomitrium is morphologically and anatomically isolated by a ldquoserious offundamental criteriardquo (Schuster 1984a) and regarded as an early-diverging lineagewithin liverworts The precise placement of Haplomitrium in molecular trees has

60

been problematic and varies depending on taxon sampling especially the inclusionvs exclusion of Treubia and the applied method (summarized by Shaw amp Renzaglia2004) Cladistic analyses of male gametogenesis characters (Garbary et al 1993)and recent molecular analyses including Treubia (eg Forrest amp Crandall-Stotler2005) revealed that Haplomitrium plus Treubia form a clade sister to all otherliverworts groups

Superclass II

1 Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Fam Blasiaceae HKlinggr

Thallus with ill-defined midrib grading into unistratose wings (leafy habit) incolonies Central strand lacking 2 rows of flattened multicellular scales (as incomplex thallose liverworts) irregularly dentate on ventral surface of thallusSmall ventral hemispherical lsquoauriclesrsquo filled with Nostoc colonies and uniqueflasked-shaped gemma-receptacles present (unique in liverworts) Marchantialeanblepharoplast type Gametophyte-sporophyte junction 1 sporophyte and 2-3gametophyte placental cell layers with Marchantialean-type wall ingrowths (transfercells) Fossil records The Late Carboniferous Blasiites lobatus (JWalton)RMSchust resembling Blasia pusilla is supposed to be an ancestor of the extanttaxa (however see Pelliopsida) The Carboniferous Treubiites kidstonii (JWalton)RMSchust with lateral succubously shingled leaves and ventral scales (as in Blasia)is rejected as a presumable precursor of Treubiopsida but serves as a model fromwhich the more frondose semithallose extant Blasia may be derived - 2 monotypicgenera - Blasia L circumboreal - Cavicularia Steph endemic Japan

Blasia was traditionally included in the Metzgerialean group but blepharoplastultrastructure and a Marchantialean-type gametophyte-sporophyte junction assignit to the Marchantiopsida Similarly latest molecular results resolve Blasia andCavicularia as sister to the Marchantiopsida (Forrest amp Crandall-Stotler 2005)with maximum bootstrap support whereas earlier molecular analyses of Blasiaeither suggested a somewhat intermediate position between Marchantiopsida andJungermanniopsida (Wheeler 2000 Stech amp Frey 2001) or a basal position withinliverworts (He-Nygreacuten et al 2004) The molecular separation of Blasia andCavicularia in Forrest amp Crandall-Stotler (2004) and Heinrichs et al (2005)was caused by contaminated Cavicularia DNA (cf Forrest amp Crandall-Stotler2005)

2 Class Marchantiopsida Stotler amp Stotl-Crand

Thirty-two genera with c 350 species Highest differentiated gametophytes in theplant kingdom Blepharoplast structure uniform closed apertures three splinemicrotubules wide Gametophyte-sporophyte junction 1-2 sporophyte and 2-4gametophyte placental cell layers cells of both layers with characteristic wallingrowths (highly branched and anastomosing or short and coarse respectively

61

Marchantialean type) Fossil records Some enigmatic Lower Devonian microfossils(epidermal surface tissues rhizoids) may be regarded as the remains of earlyMarchantioid liverworts (Graham et al 2004) Convincing Marchantioid fossilsobviously unknown from Lower Palaeophytic starting with the Lower PermianMarchantites loreus Zalessky (incertae sedis) the unequivocal Middle TriassicMarchantites cyathodoides (Townrow) HMAnderson and M tennantii HMAndersonand becoming relatively species rich from Triassic to Eocene Probably the initialdiversification of the Marchantiopsida took place at the beginning of the relativelyarid Mesophytic followed by a rapid radiation of Marchantioid taxa coincidentwith extreme conditions and ecological reorganisation in Upper Permo-Triassictime

Monophyly of the Marchantiopsida is strongly supported by all respective molecularanalyses

1 Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Fam Sphaerocarpaceae (Dumort) Heeg

Leafy habit Marchantialean blepharoplast type and gametophyte-sporophyte junctionNo fossils known - 2 genera - Sphaerocarpus Boehm and the monotypic GeothallusCampb

Fam Riellaceae Engl

Monotypic Riella Mont

2 Subclass Marchantiidae Engl

1 Order Monocleales RMSchust

Ancient relict group with plesiomorphic characters eg simple thallus and capsuleopening by only one lateral slit Typical Marchantialean blepharoplast andgametophyte-sporophyte junction type as well as molecular data (eg Meiszligner etal 1998 Wheeler 2000 Forrest amp Crandall-Stotler 2005) support the currentclassification in the Marchantiidae No fossils known - Monotypic - MonocleaHook (2) probably of Gondwanan origin restricted to hyperhygric habitats

2 Order Marchantiales Limpr in Cohn

12 families (see synopsis below) with 25 genera For subdivision of the order seeCrandall-Stotler amp Stotler (2000)

3 Order Ricciales Schljakov

2 families Oxymitraceae MuumlllFrib ex Grolle (Oxymitra Bisch ex Lindenb) andRicciaceae Reichenb with 2 genera Riccia L and the monotypic RicciocarposCorda

62

Superclass III

Recent molecular analyses based on larger taxon sampling (Davis 2004 He-Nygreacutenet al 2004 Stech amp Frey 2004 Forrest amp Crandall-Stotler 2004 2005 Heinrichs etal 2005) revealed that the simple thallose liverworts formerly comprised asJungermanniopsida subclass Metzgeriidae (sl) with 15 families 38 genera and c500 species are not monophyletic These taxa which form leaf-like lobes or thalluswings from a single wedge-shaped apical cell and are basically anacrogynous(Jungermanniales anacrogynae) are split into two main groups The first group(Metzgeriales II sensu Forrest amp Crandall-Stotler 2004) comprises different types ofsimple thallose or semileafy liverworts which are here divided into three classesFossombroniopsida Pallaviciniopsida and Pelliopsida The simple thalloseMetzgerialean liverworts (Metzgeriales I sensu Forrest amp Crandall-Stotler 2004)compose the second group that is sister to the leafy liverworts and thus treated assubclass Metzgeriidae sstr of the Jungermanniopsida (superclass IV)

1 Class Fossombroniopsida WFrey amp Hilger

Plants thallose Antheridia in acropetal sequence on upper surface of axis Oil-bodiessmall numerous Capsule mostly lacking valves wall disintegrating into fragmentsor via irregular lines into unequal valves from apex downwards Capsule wall 2-4(-6)-layered Spores areolate or with irregular lamellae or spinose on distal surfaceElaterophore lacking elaters 2-3-helical Probably of Gondwanan origin

Order Fossombroniales Schljakov

Fam Fossombroniaceae Hazsl

Main axis with obliquely inserted succubous leaves (leaf-like lobes) Rhizoids purplish(rarely pale brown) Antheridia and archegonia in simple acropetal sequence Antheridianaked Sporophyte protected by a caulocalyx Capsule wall without wall thickeningsGametophyte-sporophyte junction 1 sporophyte and 2-3 gametophyte placental transfercell layers cells with thin wall ingrowths strongly reminescent of the placenta inTreubia and Haplomitrium gametophyte placenta transfer cells with strongly branchedwall ingrowths (resembling those of Blasia and Marchantiopsida) a bulbous foot andabsence of a collar support exclusion of Fossombronia from the Jungermanniopsida -2 genera (c 92) worldwide distribution - Austrofossombronia RMSchust (2)subantarctic Andes (Peru-Venezuela) - Fossombronia Raddi (c 90) from subarctic tosubantarctic regions centre of diversification in Australia (33 spp) TheFossombroniaceae are strongly supported as monophyletic in molecular analyses withAllisonia and Petalophyllum as sister groups (Forrest amp Crandall-Stotler 2005) Thetaxon is thought to be very isolated immensely old and relict (Schuster 1984a)

Fam Petalophyllaceae (RMSchust) Stotler amp Stotl-Crand

Thallus with unistratose dorsal lamellae radiating from midrib to margin or unistratosethallus wings Archegonia clustered rather than scattered Sporophyte protected by apseudoperianth Capsule wall with outer wall thickenings - 2 genera (7) -

63

Petalophyllum Nees amp Gottsche ex Lehm (6) New Zealand (2) 1 species each inW Australia India and S USA P ralfsii (Wils) Nees amp Gottsche medit-atlant WEurope N Africa - Sewardiella Kashyap (1) W Himalayas

Fam Allisoniaceae (RMSchust ex Grolle) Schljakov

Plants thallose Midrib of thallus ill-defined Central strand lacking DioicousAntheridia individually protected by a scale Capsule spherical wall irregularly tearinginto 5-7 unequal valves epidermal cells with irregular bands without elaterophoreSpores strongly sculptured - 2 genera (5) - Allisonia Herzog (1) endemic NewZealand - Calycularia Mitt (4) N and E Asia Himalayas

Molecular data indicate that the Allisoniaceae are not monophyletic Both generahave similar capsule walls and thallus structures but differ by the presence of awell-developed pseudoperianth in Calycularia (eg Inoue 1976) The placement ofCalycularia has traditionally been problematic and is still tentative based on itsposition sister to the Fossombronialean and Pallavicinialean liverworts in moleculartrees

Fam Sandeothallaceae RM Schust

Plants thallose Thalli simple or rarely branched with uniseriate slime hairs occasionalwith ventral branches Rhizoids reddish Antheridia in axils of dorsal scales alongmidrib surface Seta massive Capsule wall (3)4-5(6)-layered opening by 2 lateralslits without elaterophore - Monotypic - Sandeothallus RMSchust (1) IndiaMalesia Samoa

The systematic position remains ambiguous Morphologically Sandeothallus occupiesan intermediate position gametophytic characters indicate close relationship toAllisoniaceae whereas sporophytically it is close to the Pallaviciniaceae (Schuster1982) Molecular data are so far not available

2 Class Pallaviciniopsida WFrey amp Stech class nov

Plantae thallinae prostratae vel in axem prostratum stipitemque erectum divisae partim dendroideaeCosta thalli prominens 1 vel 2(-4) filis centralibus Cellulae filorum centralium elongatae perforataehydroideis similes Capsulae ovoideae ad cylindricae 2 vel 4 valvis dehiscentes

Type family Pallaviciniaceae Mig

Plants thallose prostrate erect or sometimes dendroid Dendroid taxa evolved threetimes independently in Jensenia and Symphyogyna (Pallaviciniaceae) as well as inHymenophyton (Hymenophytaceae) (Schaumann et al 2005) Gametophyte mostlywith central strand composed of thick-walled elongated water-conducting cells withperforations (pores) This pallavicinoid type of water-conducting cells occurs onlyin the Pallaviciniopsida and is unique in bryophytes Antheridia and archegonia(clustered) on dorsal surface of thallus Sporophyte protected by a pseudoperianth(inner involucre) or stem-calyptra Seta massive Capsule ellipsoidal to cylindricaltearing into 2 imperfectly 4 or 4 valves wall bistratose Gametophyte-sporophytejunction gametophyte placental cells without wall ingrowths sporophyte placental

64

cells partly without wall ingrowths Fossil records Pallaviciniites devonicus (Hueber)RMSchust from lowermost Upper Devonian (375 mio y) is the oldest true bryo-phyte fossil known The thallose plant bearing a central strand in the gametophyteaxis is superficially similar to the Pallaviciniaceae in particular to Pallavicinia andSymphyogyna Laticaulina papillosa Krassilov from Late Jurassic of Russia alsoshows affinities to the Pallaviciniopsida (Symphyogyna) About 65 species

1 Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Basionym Pallaviciniineae RMSchust Phytologia 56 65 1984

Type (and only) family Pallaviciniaceae Mig

Schuster (1984b) erected the Pallaviciniineae to include PallaviciniaceaeSandeothallaceae and Makinoaceae In contrast we consider the Pallavicinialesmonotypic at least until relationships of Sandeothallus and Makinoa have beenclarified on the molecular level

Fam Pallaviciniaceae Mig

Plants thallose prostrate without basal stipe and ldquorhizomerdquo or erect arising froma ldquorhizomerdquo or stipe dendroid in Jensenia and some species of Pallavicinia andSymphyogyna Thallus with well-defined midrib with 1 or 2(-4) central strandsin most taxa present and unistratose lamina Water conducting cells elongatedwith tapering ends and thickened walls (c 8 microm wide and up to 300 microm long)throughout with numerous pits produced by dissolution of secondary wallmaterial associated with modified plasmodesmata Only few true plasmodesmata-derived perforations (pores) present (Oslash 200-400 nm) No relationship withtracheids (Frey et al 1996) Slime papillae on both dorsal and ventral surfacesof apex sometimes present Ventral scales absent or small and uniseriate DioicousAntheridia on dorsal surface of thallus often in 2-several ranks associated withscales Archegonia clustered on dorsal surface of midrib (gynoecia) deliminatedby a single (Symphyogyna) or double involucres (except Xenothallus) Developingsporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-calyptra Seta long massive Capsule elongate-cylindrical to ovoid dehiscenceby 2 or imperfectly 4 valves epidermal cell walls lacking thickenings Spores 1-celled Elaterophore rudimentary or absent Elaters 2-3-helical Gametophyte-sporophyte junction Wall ingrowths (transfer cells) present in the outermostsporophytic placental layer - 9 genera (c 60) Gondwanan centres of diversityin Australasia and S America

Molecular analyses resolve Pallaviciniaceae as monophyletic (eg Forrest ampCrandall-Stotler 2005 Schaumann et al 2005) These data support a separationof Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa a positionof Podomitrium (Podomitrioideae RMSchust) close to the Symphyogynoideae(Trevis) RMSchust ex Grolle and polyphyly of Pallavicinia and thePallavicinioideae Because of ambiguous relationships between these subfamilieswe include Podomitrioideae and Symphyogynoideae in Pallavicinioideae sl

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

60

been problematic and varies depending on taxon sampling especially the inclusionvs exclusion of Treubia and the applied method (summarized by Shaw amp Renzaglia2004) Cladistic analyses of male gametogenesis characters (Garbary et al 1993)and recent molecular analyses including Treubia (eg Forrest amp Crandall-Stotler2005) revealed that Haplomitrium plus Treubia form a clade sister to all otherliverworts groups

Superclass II

1 Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Fam Blasiaceae HKlinggr

Thallus with ill-defined midrib grading into unistratose wings (leafy habit) incolonies Central strand lacking 2 rows of flattened multicellular scales (as incomplex thallose liverworts) irregularly dentate on ventral surface of thallusSmall ventral hemispherical lsquoauriclesrsquo filled with Nostoc colonies and uniqueflasked-shaped gemma-receptacles present (unique in liverworts) Marchantialeanblepharoplast type Gametophyte-sporophyte junction 1 sporophyte and 2-3gametophyte placental cell layers with Marchantialean-type wall ingrowths (transfercells) Fossil records The Late Carboniferous Blasiites lobatus (JWalton)RMSchust resembling Blasia pusilla is supposed to be an ancestor of the extanttaxa (however see Pelliopsida) The Carboniferous Treubiites kidstonii (JWalton)RMSchust with lateral succubously shingled leaves and ventral scales (as in Blasia)is rejected as a presumable precursor of Treubiopsida but serves as a model fromwhich the more frondose semithallose extant Blasia may be derived - 2 monotypicgenera - Blasia L circumboreal - Cavicularia Steph endemic Japan

Blasia was traditionally included in the Metzgerialean group but blepharoplastultrastructure and a Marchantialean-type gametophyte-sporophyte junction assignit to the Marchantiopsida Similarly latest molecular results resolve Blasia andCavicularia as sister to the Marchantiopsida (Forrest amp Crandall-Stotler 2005)with maximum bootstrap support whereas earlier molecular analyses of Blasiaeither suggested a somewhat intermediate position between Marchantiopsida andJungermanniopsida (Wheeler 2000 Stech amp Frey 2001) or a basal position withinliverworts (He-Nygreacuten et al 2004) The molecular separation of Blasia andCavicularia in Forrest amp Crandall-Stotler (2004) and Heinrichs et al (2005)was caused by contaminated Cavicularia DNA (cf Forrest amp Crandall-Stotler2005)

2 Class Marchantiopsida Stotler amp Stotl-Crand

Thirty-two genera with c 350 species Highest differentiated gametophytes in theplant kingdom Blepharoplast structure uniform closed apertures three splinemicrotubules wide Gametophyte-sporophyte junction 1-2 sporophyte and 2-4gametophyte placental cell layers cells of both layers with characteristic wallingrowths (highly branched and anastomosing or short and coarse respectively

61

Marchantialean type) Fossil records Some enigmatic Lower Devonian microfossils(epidermal surface tissues rhizoids) may be regarded as the remains of earlyMarchantioid liverworts (Graham et al 2004) Convincing Marchantioid fossilsobviously unknown from Lower Palaeophytic starting with the Lower PermianMarchantites loreus Zalessky (incertae sedis) the unequivocal Middle TriassicMarchantites cyathodoides (Townrow) HMAnderson and M tennantii HMAndersonand becoming relatively species rich from Triassic to Eocene Probably the initialdiversification of the Marchantiopsida took place at the beginning of the relativelyarid Mesophytic followed by a rapid radiation of Marchantioid taxa coincidentwith extreme conditions and ecological reorganisation in Upper Permo-Triassictime

Monophyly of the Marchantiopsida is strongly supported by all respective molecularanalyses

1 Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Fam Sphaerocarpaceae (Dumort) Heeg

Leafy habit Marchantialean blepharoplast type and gametophyte-sporophyte junctionNo fossils known - 2 genera - Sphaerocarpus Boehm and the monotypic GeothallusCampb

Fam Riellaceae Engl

Monotypic Riella Mont

2 Subclass Marchantiidae Engl

1 Order Monocleales RMSchust

Ancient relict group with plesiomorphic characters eg simple thallus and capsuleopening by only one lateral slit Typical Marchantialean blepharoplast andgametophyte-sporophyte junction type as well as molecular data (eg Meiszligner etal 1998 Wheeler 2000 Forrest amp Crandall-Stotler 2005) support the currentclassification in the Marchantiidae No fossils known - Monotypic - MonocleaHook (2) probably of Gondwanan origin restricted to hyperhygric habitats

2 Order Marchantiales Limpr in Cohn

12 families (see synopsis below) with 25 genera For subdivision of the order seeCrandall-Stotler amp Stotler (2000)

3 Order Ricciales Schljakov

2 families Oxymitraceae MuumlllFrib ex Grolle (Oxymitra Bisch ex Lindenb) andRicciaceae Reichenb with 2 genera Riccia L and the monotypic RicciocarposCorda

62

Superclass III

Recent molecular analyses based on larger taxon sampling (Davis 2004 He-Nygreacutenet al 2004 Stech amp Frey 2004 Forrest amp Crandall-Stotler 2004 2005 Heinrichs etal 2005) revealed that the simple thallose liverworts formerly comprised asJungermanniopsida subclass Metzgeriidae (sl) with 15 families 38 genera and c500 species are not monophyletic These taxa which form leaf-like lobes or thalluswings from a single wedge-shaped apical cell and are basically anacrogynous(Jungermanniales anacrogynae) are split into two main groups The first group(Metzgeriales II sensu Forrest amp Crandall-Stotler 2004) comprises different types ofsimple thallose or semileafy liverworts which are here divided into three classesFossombroniopsida Pallaviciniopsida and Pelliopsida The simple thalloseMetzgerialean liverworts (Metzgeriales I sensu Forrest amp Crandall-Stotler 2004)compose the second group that is sister to the leafy liverworts and thus treated assubclass Metzgeriidae sstr of the Jungermanniopsida (superclass IV)

1 Class Fossombroniopsida WFrey amp Hilger

Plants thallose Antheridia in acropetal sequence on upper surface of axis Oil-bodiessmall numerous Capsule mostly lacking valves wall disintegrating into fragmentsor via irregular lines into unequal valves from apex downwards Capsule wall 2-4(-6)-layered Spores areolate or with irregular lamellae or spinose on distal surfaceElaterophore lacking elaters 2-3-helical Probably of Gondwanan origin

Order Fossombroniales Schljakov

Fam Fossombroniaceae Hazsl

Main axis with obliquely inserted succubous leaves (leaf-like lobes) Rhizoids purplish(rarely pale brown) Antheridia and archegonia in simple acropetal sequence Antheridianaked Sporophyte protected by a caulocalyx Capsule wall without wall thickeningsGametophyte-sporophyte junction 1 sporophyte and 2-3 gametophyte placental transfercell layers cells with thin wall ingrowths strongly reminescent of the placenta inTreubia and Haplomitrium gametophyte placenta transfer cells with strongly branchedwall ingrowths (resembling those of Blasia and Marchantiopsida) a bulbous foot andabsence of a collar support exclusion of Fossombronia from the Jungermanniopsida -2 genera (c 92) worldwide distribution - Austrofossombronia RMSchust (2)subantarctic Andes (Peru-Venezuela) - Fossombronia Raddi (c 90) from subarctic tosubantarctic regions centre of diversification in Australia (33 spp) TheFossombroniaceae are strongly supported as monophyletic in molecular analyses withAllisonia and Petalophyllum as sister groups (Forrest amp Crandall-Stotler 2005) Thetaxon is thought to be very isolated immensely old and relict (Schuster 1984a)

Fam Petalophyllaceae (RMSchust) Stotler amp Stotl-Crand

Thallus with unistratose dorsal lamellae radiating from midrib to margin or unistratosethallus wings Archegonia clustered rather than scattered Sporophyte protected by apseudoperianth Capsule wall with outer wall thickenings - 2 genera (7) -

63

Petalophyllum Nees amp Gottsche ex Lehm (6) New Zealand (2) 1 species each inW Australia India and S USA P ralfsii (Wils) Nees amp Gottsche medit-atlant WEurope N Africa - Sewardiella Kashyap (1) W Himalayas

Fam Allisoniaceae (RMSchust ex Grolle) Schljakov

Plants thallose Midrib of thallus ill-defined Central strand lacking DioicousAntheridia individually protected by a scale Capsule spherical wall irregularly tearinginto 5-7 unequal valves epidermal cells with irregular bands without elaterophoreSpores strongly sculptured - 2 genera (5) - Allisonia Herzog (1) endemic NewZealand - Calycularia Mitt (4) N and E Asia Himalayas

Molecular data indicate that the Allisoniaceae are not monophyletic Both generahave similar capsule walls and thallus structures but differ by the presence of awell-developed pseudoperianth in Calycularia (eg Inoue 1976) The placement ofCalycularia has traditionally been problematic and is still tentative based on itsposition sister to the Fossombronialean and Pallavicinialean liverworts in moleculartrees

Fam Sandeothallaceae RM Schust

Plants thallose Thalli simple or rarely branched with uniseriate slime hairs occasionalwith ventral branches Rhizoids reddish Antheridia in axils of dorsal scales alongmidrib surface Seta massive Capsule wall (3)4-5(6)-layered opening by 2 lateralslits without elaterophore - Monotypic - Sandeothallus RMSchust (1) IndiaMalesia Samoa

The systematic position remains ambiguous Morphologically Sandeothallus occupiesan intermediate position gametophytic characters indicate close relationship toAllisoniaceae whereas sporophytically it is close to the Pallaviciniaceae (Schuster1982) Molecular data are so far not available

2 Class Pallaviciniopsida WFrey amp Stech class nov

Plantae thallinae prostratae vel in axem prostratum stipitemque erectum divisae partim dendroideaeCosta thalli prominens 1 vel 2(-4) filis centralibus Cellulae filorum centralium elongatae perforataehydroideis similes Capsulae ovoideae ad cylindricae 2 vel 4 valvis dehiscentes

Type family Pallaviciniaceae Mig

Plants thallose prostrate erect or sometimes dendroid Dendroid taxa evolved threetimes independently in Jensenia and Symphyogyna (Pallaviciniaceae) as well as inHymenophyton (Hymenophytaceae) (Schaumann et al 2005) Gametophyte mostlywith central strand composed of thick-walled elongated water-conducting cells withperforations (pores) This pallavicinoid type of water-conducting cells occurs onlyin the Pallaviciniopsida and is unique in bryophytes Antheridia and archegonia(clustered) on dorsal surface of thallus Sporophyte protected by a pseudoperianth(inner involucre) or stem-calyptra Seta massive Capsule ellipsoidal to cylindricaltearing into 2 imperfectly 4 or 4 valves wall bistratose Gametophyte-sporophytejunction gametophyte placental cells without wall ingrowths sporophyte placental

64

cells partly without wall ingrowths Fossil records Pallaviciniites devonicus (Hueber)RMSchust from lowermost Upper Devonian (375 mio y) is the oldest true bryo-phyte fossil known The thallose plant bearing a central strand in the gametophyteaxis is superficially similar to the Pallaviciniaceae in particular to Pallavicinia andSymphyogyna Laticaulina papillosa Krassilov from Late Jurassic of Russia alsoshows affinities to the Pallaviciniopsida (Symphyogyna) About 65 species

1 Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Basionym Pallaviciniineae RMSchust Phytologia 56 65 1984

Type (and only) family Pallaviciniaceae Mig

Schuster (1984b) erected the Pallaviciniineae to include PallaviciniaceaeSandeothallaceae and Makinoaceae In contrast we consider the Pallavicinialesmonotypic at least until relationships of Sandeothallus and Makinoa have beenclarified on the molecular level

Fam Pallaviciniaceae Mig

Plants thallose prostrate without basal stipe and ldquorhizomerdquo or erect arising froma ldquorhizomerdquo or stipe dendroid in Jensenia and some species of Pallavicinia andSymphyogyna Thallus with well-defined midrib with 1 or 2(-4) central strandsin most taxa present and unistratose lamina Water conducting cells elongatedwith tapering ends and thickened walls (c 8 microm wide and up to 300 microm long)throughout with numerous pits produced by dissolution of secondary wallmaterial associated with modified plasmodesmata Only few true plasmodesmata-derived perforations (pores) present (Oslash 200-400 nm) No relationship withtracheids (Frey et al 1996) Slime papillae on both dorsal and ventral surfacesof apex sometimes present Ventral scales absent or small and uniseriate DioicousAntheridia on dorsal surface of thallus often in 2-several ranks associated withscales Archegonia clustered on dorsal surface of midrib (gynoecia) deliminatedby a single (Symphyogyna) or double involucres (except Xenothallus) Developingsporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-calyptra Seta long massive Capsule elongate-cylindrical to ovoid dehiscenceby 2 or imperfectly 4 valves epidermal cell walls lacking thickenings Spores 1-celled Elaterophore rudimentary or absent Elaters 2-3-helical Gametophyte-sporophyte junction Wall ingrowths (transfer cells) present in the outermostsporophytic placental layer - 9 genera (c 60) Gondwanan centres of diversityin Australasia and S America

Molecular analyses resolve Pallaviciniaceae as monophyletic (eg Forrest ampCrandall-Stotler 2005 Schaumann et al 2005) These data support a separationof Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa a positionof Podomitrium (Podomitrioideae RMSchust) close to the Symphyogynoideae(Trevis) RMSchust ex Grolle and polyphyly of Pallavicinia and thePallavicinioideae Because of ambiguous relationships between these subfamilieswe include Podomitrioideae and Symphyogynoideae in Pallavicinioideae sl

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

61

Marchantialean type) Fossil records Some enigmatic Lower Devonian microfossils(epidermal surface tissues rhizoids) may be regarded as the remains of earlyMarchantioid liverworts (Graham et al 2004) Convincing Marchantioid fossilsobviously unknown from Lower Palaeophytic starting with the Lower PermianMarchantites loreus Zalessky (incertae sedis) the unequivocal Middle TriassicMarchantites cyathodoides (Townrow) HMAnderson and M tennantii HMAndersonand becoming relatively species rich from Triassic to Eocene Probably the initialdiversification of the Marchantiopsida took place at the beginning of the relativelyarid Mesophytic followed by a rapid radiation of Marchantioid taxa coincidentwith extreme conditions and ecological reorganisation in Upper Permo-Triassictime

Monophyly of the Marchantiopsida is strongly supported by all respective molecularanalyses

1 Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Fam Sphaerocarpaceae (Dumort) Heeg

Leafy habit Marchantialean blepharoplast type and gametophyte-sporophyte junctionNo fossils known - 2 genera - Sphaerocarpus Boehm and the monotypic GeothallusCampb

Fam Riellaceae Engl

Monotypic Riella Mont

2 Subclass Marchantiidae Engl

1 Order Monocleales RMSchust

Ancient relict group with plesiomorphic characters eg simple thallus and capsuleopening by only one lateral slit Typical Marchantialean blepharoplast andgametophyte-sporophyte junction type as well as molecular data (eg Meiszligner etal 1998 Wheeler 2000 Forrest amp Crandall-Stotler 2005) support the currentclassification in the Marchantiidae No fossils known - Monotypic - MonocleaHook (2) probably of Gondwanan origin restricted to hyperhygric habitats

2 Order Marchantiales Limpr in Cohn

12 families (see synopsis below) with 25 genera For subdivision of the order seeCrandall-Stotler amp Stotler (2000)

3 Order Ricciales Schljakov

2 families Oxymitraceae MuumlllFrib ex Grolle (Oxymitra Bisch ex Lindenb) andRicciaceae Reichenb with 2 genera Riccia L and the monotypic RicciocarposCorda

62

Superclass III

Recent molecular analyses based on larger taxon sampling (Davis 2004 He-Nygreacutenet al 2004 Stech amp Frey 2004 Forrest amp Crandall-Stotler 2004 2005 Heinrichs etal 2005) revealed that the simple thallose liverworts formerly comprised asJungermanniopsida subclass Metzgeriidae (sl) with 15 families 38 genera and c500 species are not monophyletic These taxa which form leaf-like lobes or thalluswings from a single wedge-shaped apical cell and are basically anacrogynous(Jungermanniales anacrogynae) are split into two main groups The first group(Metzgeriales II sensu Forrest amp Crandall-Stotler 2004) comprises different types ofsimple thallose or semileafy liverworts which are here divided into three classesFossombroniopsida Pallaviciniopsida and Pelliopsida The simple thalloseMetzgerialean liverworts (Metzgeriales I sensu Forrest amp Crandall-Stotler 2004)compose the second group that is sister to the leafy liverworts and thus treated assubclass Metzgeriidae sstr of the Jungermanniopsida (superclass IV)

1 Class Fossombroniopsida WFrey amp Hilger

Plants thallose Antheridia in acropetal sequence on upper surface of axis Oil-bodiessmall numerous Capsule mostly lacking valves wall disintegrating into fragmentsor via irregular lines into unequal valves from apex downwards Capsule wall 2-4(-6)-layered Spores areolate or with irregular lamellae or spinose on distal surfaceElaterophore lacking elaters 2-3-helical Probably of Gondwanan origin

Order Fossombroniales Schljakov

Fam Fossombroniaceae Hazsl

Main axis with obliquely inserted succubous leaves (leaf-like lobes) Rhizoids purplish(rarely pale brown) Antheridia and archegonia in simple acropetal sequence Antheridianaked Sporophyte protected by a caulocalyx Capsule wall without wall thickeningsGametophyte-sporophyte junction 1 sporophyte and 2-3 gametophyte placental transfercell layers cells with thin wall ingrowths strongly reminescent of the placenta inTreubia and Haplomitrium gametophyte placenta transfer cells with strongly branchedwall ingrowths (resembling those of Blasia and Marchantiopsida) a bulbous foot andabsence of a collar support exclusion of Fossombronia from the Jungermanniopsida -2 genera (c 92) worldwide distribution - Austrofossombronia RMSchust (2)subantarctic Andes (Peru-Venezuela) - Fossombronia Raddi (c 90) from subarctic tosubantarctic regions centre of diversification in Australia (33 spp) TheFossombroniaceae are strongly supported as monophyletic in molecular analyses withAllisonia and Petalophyllum as sister groups (Forrest amp Crandall-Stotler 2005) Thetaxon is thought to be very isolated immensely old and relict (Schuster 1984a)

Fam Petalophyllaceae (RMSchust) Stotler amp Stotl-Crand

Thallus with unistratose dorsal lamellae radiating from midrib to margin or unistratosethallus wings Archegonia clustered rather than scattered Sporophyte protected by apseudoperianth Capsule wall with outer wall thickenings - 2 genera (7) -

63

Petalophyllum Nees amp Gottsche ex Lehm (6) New Zealand (2) 1 species each inW Australia India and S USA P ralfsii (Wils) Nees amp Gottsche medit-atlant WEurope N Africa - Sewardiella Kashyap (1) W Himalayas

Fam Allisoniaceae (RMSchust ex Grolle) Schljakov

Plants thallose Midrib of thallus ill-defined Central strand lacking DioicousAntheridia individually protected by a scale Capsule spherical wall irregularly tearinginto 5-7 unequal valves epidermal cells with irregular bands without elaterophoreSpores strongly sculptured - 2 genera (5) - Allisonia Herzog (1) endemic NewZealand - Calycularia Mitt (4) N and E Asia Himalayas

Molecular data indicate that the Allisoniaceae are not monophyletic Both generahave similar capsule walls and thallus structures but differ by the presence of awell-developed pseudoperianth in Calycularia (eg Inoue 1976) The placement ofCalycularia has traditionally been problematic and is still tentative based on itsposition sister to the Fossombronialean and Pallavicinialean liverworts in moleculartrees

Fam Sandeothallaceae RM Schust

Plants thallose Thalli simple or rarely branched with uniseriate slime hairs occasionalwith ventral branches Rhizoids reddish Antheridia in axils of dorsal scales alongmidrib surface Seta massive Capsule wall (3)4-5(6)-layered opening by 2 lateralslits without elaterophore - Monotypic - Sandeothallus RMSchust (1) IndiaMalesia Samoa

The systematic position remains ambiguous Morphologically Sandeothallus occupiesan intermediate position gametophytic characters indicate close relationship toAllisoniaceae whereas sporophytically it is close to the Pallaviciniaceae (Schuster1982) Molecular data are so far not available

2 Class Pallaviciniopsida WFrey amp Stech class nov

Plantae thallinae prostratae vel in axem prostratum stipitemque erectum divisae partim dendroideaeCosta thalli prominens 1 vel 2(-4) filis centralibus Cellulae filorum centralium elongatae perforataehydroideis similes Capsulae ovoideae ad cylindricae 2 vel 4 valvis dehiscentes

Type family Pallaviciniaceae Mig

Plants thallose prostrate erect or sometimes dendroid Dendroid taxa evolved threetimes independently in Jensenia and Symphyogyna (Pallaviciniaceae) as well as inHymenophyton (Hymenophytaceae) (Schaumann et al 2005) Gametophyte mostlywith central strand composed of thick-walled elongated water-conducting cells withperforations (pores) This pallavicinoid type of water-conducting cells occurs onlyin the Pallaviciniopsida and is unique in bryophytes Antheridia and archegonia(clustered) on dorsal surface of thallus Sporophyte protected by a pseudoperianth(inner involucre) or stem-calyptra Seta massive Capsule ellipsoidal to cylindricaltearing into 2 imperfectly 4 or 4 valves wall bistratose Gametophyte-sporophytejunction gametophyte placental cells without wall ingrowths sporophyte placental

64

cells partly without wall ingrowths Fossil records Pallaviciniites devonicus (Hueber)RMSchust from lowermost Upper Devonian (375 mio y) is the oldest true bryo-phyte fossil known The thallose plant bearing a central strand in the gametophyteaxis is superficially similar to the Pallaviciniaceae in particular to Pallavicinia andSymphyogyna Laticaulina papillosa Krassilov from Late Jurassic of Russia alsoshows affinities to the Pallaviciniopsida (Symphyogyna) About 65 species

1 Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Basionym Pallaviciniineae RMSchust Phytologia 56 65 1984

Type (and only) family Pallaviciniaceae Mig

Schuster (1984b) erected the Pallaviciniineae to include PallaviciniaceaeSandeothallaceae and Makinoaceae In contrast we consider the Pallavicinialesmonotypic at least until relationships of Sandeothallus and Makinoa have beenclarified on the molecular level

Fam Pallaviciniaceae Mig

Plants thallose prostrate without basal stipe and ldquorhizomerdquo or erect arising froma ldquorhizomerdquo or stipe dendroid in Jensenia and some species of Pallavicinia andSymphyogyna Thallus with well-defined midrib with 1 or 2(-4) central strandsin most taxa present and unistratose lamina Water conducting cells elongatedwith tapering ends and thickened walls (c 8 microm wide and up to 300 microm long)throughout with numerous pits produced by dissolution of secondary wallmaterial associated with modified plasmodesmata Only few true plasmodesmata-derived perforations (pores) present (Oslash 200-400 nm) No relationship withtracheids (Frey et al 1996) Slime papillae on both dorsal and ventral surfacesof apex sometimes present Ventral scales absent or small and uniseriate DioicousAntheridia on dorsal surface of thallus often in 2-several ranks associated withscales Archegonia clustered on dorsal surface of midrib (gynoecia) deliminatedby a single (Symphyogyna) or double involucres (except Xenothallus) Developingsporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-calyptra Seta long massive Capsule elongate-cylindrical to ovoid dehiscenceby 2 or imperfectly 4 valves epidermal cell walls lacking thickenings Spores 1-celled Elaterophore rudimentary or absent Elaters 2-3-helical Gametophyte-sporophyte junction Wall ingrowths (transfer cells) present in the outermostsporophytic placental layer - 9 genera (c 60) Gondwanan centres of diversityin Australasia and S America

Molecular analyses resolve Pallaviciniaceae as monophyletic (eg Forrest ampCrandall-Stotler 2005 Schaumann et al 2005) These data support a separationof Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa a positionof Podomitrium (Podomitrioideae RMSchust) close to the Symphyogynoideae(Trevis) RMSchust ex Grolle and polyphyly of Pallavicinia and thePallavicinioideae Because of ambiguous relationships between these subfamilieswe include Podomitrioideae and Symphyogynoideae in Pallavicinioideae sl

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

62

Superclass III

Recent molecular analyses based on larger taxon sampling (Davis 2004 He-Nygreacutenet al 2004 Stech amp Frey 2004 Forrest amp Crandall-Stotler 2004 2005 Heinrichs etal 2005) revealed that the simple thallose liverworts formerly comprised asJungermanniopsida subclass Metzgeriidae (sl) with 15 families 38 genera and c500 species are not monophyletic These taxa which form leaf-like lobes or thalluswings from a single wedge-shaped apical cell and are basically anacrogynous(Jungermanniales anacrogynae) are split into two main groups The first group(Metzgeriales II sensu Forrest amp Crandall-Stotler 2004) comprises different types ofsimple thallose or semileafy liverworts which are here divided into three classesFossombroniopsida Pallaviciniopsida and Pelliopsida The simple thalloseMetzgerialean liverworts (Metzgeriales I sensu Forrest amp Crandall-Stotler 2004)compose the second group that is sister to the leafy liverworts and thus treated assubclass Metzgeriidae sstr of the Jungermanniopsida (superclass IV)

1 Class Fossombroniopsida WFrey amp Hilger

Plants thallose Antheridia in acropetal sequence on upper surface of axis Oil-bodiessmall numerous Capsule mostly lacking valves wall disintegrating into fragmentsor via irregular lines into unequal valves from apex downwards Capsule wall 2-4(-6)-layered Spores areolate or with irregular lamellae or spinose on distal surfaceElaterophore lacking elaters 2-3-helical Probably of Gondwanan origin

Order Fossombroniales Schljakov

Fam Fossombroniaceae Hazsl

Main axis with obliquely inserted succubous leaves (leaf-like lobes) Rhizoids purplish(rarely pale brown) Antheridia and archegonia in simple acropetal sequence Antheridianaked Sporophyte protected by a caulocalyx Capsule wall without wall thickeningsGametophyte-sporophyte junction 1 sporophyte and 2-3 gametophyte placental transfercell layers cells with thin wall ingrowths strongly reminescent of the placenta inTreubia and Haplomitrium gametophyte placenta transfer cells with strongly branchedwall ingrowths (resembling those of Blasia and Marchantiopsida) a bulbous foot andabsence of a collar support exclusion of Fossombronia from the Jungermanniopsida -2 genera (c 92) worldwide distribution - Austrofossombronia RMSchust (2)subantarctic Andes (Peru-Venezuela) - Fossombronia Raddi (c 90) from subarctic tosubantarctic regions centre of diversification in Australia (33 spp) TheFossombroniaceae are strongly supported as monophyletic in molecular analyses withAllisonia and Petalophyllum as sister groups (Forrest amp Crandall-Stotler 2005) Thetaxon is thought to be very isolated immensely old and relict (Schuster 1984a)

Fam Petalophyllaceae (RMSchust) Stotler amp Stotl-Crand

Thallus with unistratose dorsal lamellae radiating from midrib to margin or unistratosethallus wings Archegonia clustered rather than scattered Sporophyte protected by apseudoperianth Capsule wall with outer wall thickenings - 2 genera (7) -

63

Petalophyllum Nees amp Gottsche ex Lehm (6) New Zealand (2) 1 species each inW Australia India and S USA P ralfsii (Wils) Nees amp Gottsche medit-atlant WEurope N Africa - Sewardiella Kashyap (1) W Himalayas

Fam Allisoniaceae (RMSchust ex Grolle) Schljakov

Plants thallose Midrib of thallus ill-defined Central strand lacking DioicousAntheridia individually protected by a scale Capsule spherical wall irregularly tearinginto 5-7 unequal valves epidermal cells with irregular bands without elaterophoreSpores strongly sculptured - 2 genera (5) - Allisonia Herzog (1) endemic NewZealand - Calycularia Mitt (4) N and E Asia Himalayas

Molecular data indicate that the Allisoniaceae are not monophyletic Both generahave similar capsule walls and thallus structures but differ by the presence of awell-developed pseudoperianth in Calycularia (eg Inoue 1976) The placement ofCalycularia has traditionally been problematic and is still tentative based on itsposition sister to the Fossombronialean and Pallavicinialean liverworts in moleculartrees

Fam Sandeothallaceae RM Schust

Plants thallose Thalli simple or rarely branched with uniseriate slime hairs occasionalwith ventral branches Rhizoids reddish Antheridia in axils of dorsal scales alongmidrib surface Seta massive Capsule wall (3)4-5(6)-layered opening by 2 lateralslits without elaterophore - Monotypic - Sandeothallus RMSchust (1) IndiaMalesia Samoa

The systematic position remains ambiguous Morphologically Sandeothallus occupiesan intermediate position gametophytic characters indicate close relationship toAllisoniaceae whereas sporophytically it is close to the Pallaviciniaceae (Schuster1982) Molecular data are so far not available

2 Class Pallaviciniopsida WFrey amp Stech class nov

Plantae thallinae prostratae vel in axem prostratum stipitemque erectum divisae partim dendroideaeCosta thalli prominens 1 vel 2(-4) filis centralibus Cellulae filorum centralium elongatae perforataehydroideis similes Capsulae ovoideae ad cylindricae 2 vel 4 valvis dehiscentes

Type family Pallaviciniaceae Mig

Plants thallose prostrate erect or sometimes dendroid Dendroid taxa evolved threetimes independently in Jensenia and Symphyogyna (Pallaviciniaceae) as well as inHymenophyton (Hymenophytaceae) (Schaumann et al 2005) Gametophyte mostlywith central strand composed of thick-walled elongated water-conducting cells withperforations (pores) This pallavicinoid type of water-conducting cells occurs onlyin the Pallaviciniopsida and is unique in bryophytes Antheridia and archegonia(clustered) on dorsal surface of thallus Sporophyte protected by a pseudoperianth(inner involucre) or stem-calyptra Seta massive Capsule ellipsoidal to cylindricaltearing into 2 imperfectly 4 or 4 valves wall bistratose Gametophyte-sporophytejunction gametophyte placental cells without wall ingrowths sporophyte placental

64

cells partly without wall ingrowths Fossil records Pallaviciniites devonicus (Hueber)RMSchust from lowermost Upper Devonian (375 mio y) is the oldest true bryo-phyte fossil known The thallose plant bearing a central strand in the gametophyteaxis is superficially similar to the Pallaviciniaceae in particular to Pallavicinia andSymphyogyna Laticaulina papillosa Krassilov from Late Jurassic of Russia alsoshows affinities to the Pallaviciniopsida (Symphyogyna) About 65 species

1 Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Basionym Pallaviciniineae RMSchust Phytologia 56 65 1984

Type (and only) family Pallaviciniaceae Mig

Schuster (1984b) erected the Pallaviciniineae to include PallaviciniaceaeSandeothallaceae and Makinoaceae In contrast we consider the Pallavicinialesmonotypic at least until relationships of Sandeothallus and Makinoa have beenclarified on the molecular level

Fam Pallaviciniaceae Mig

Plants thallose prostrate without basal stipe and ldquorhizomerdquo or erect arising froma ldquorhizomerdquo or stipe dendroid in Jensenia and some species of Pallavicinia andSymphyogyna Thallus with well-defined midrib with 1 or 2(-4) central strandsin most taxa present and unistratose lamina Water conducting cells elongatedwith tapering ends and thickened walls (c 8 microm wide and up to 300 microm long)throughout with numerous pits produced by dissolution of secondary wallmaterial associated with modified plasmodesmata Only few true plasmodesmata-derived perforations (pores) present (Oslash 200-400 nm) No relationship withtracheids (Frey et al 1996) Slime papillae on both dorsal and ventral surfacesof apex sometimes present Ventral scales absent or small and uniseriate DioicousAntheridia on dorsal surface of thallus often in 2-several ranks associated withscales Archegonia clustered on dorsal surface of midrib (gynoecia) deliminatedby a single (Symphyogyna) or double involucres (except Xenothallus) Developingsporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-calyptra Seta long massive Capsule elongate-cylindrical to ovoid dehiscenceby 2 or imperfectly 4 valves epidermal cell walls lacking thickenings Spores 1-celled Elaterophore rudimentary or absent Elaters 2-3-helical Gametophyte-sporophyte junction Wall ingrowths (transfer cells) present in the outermostsporophytic placental layer - 9 genera (c 60) Gondwanan centres of diversityin Australasia and S America

Molecular analyses resolve Pallaviciniaceae as monophyletic (eg Forrest ampCrandall-Stotler 2005 Schaumann et al 2005) These data support a separationof Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa a positionof Podomitrium (Podomitrioideae RMSchust) close to the Symphyogynoideae(Trevis) RMSchust ex Grolle and polyphyly of Pallavicinia and thePallavicinioideae Because of ambiguous relationships between these subfamilieswe include Podomitrioideae and Symphyogynoideae in Pallavicinioideae sl

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

63

Petalophyllum Nees amp Gottsche ex Lehm (6) New Zealand (2) 1 species each inW Australia India and S USA P ralfsii (Wils) Nees amp Gottsche medit-atlant WEurope N Africa - Sewardiella Kashyap (1) W Himalayas

Fam Allisoniaceae (RMSchust ex Grolle) Schljakov

Plants thallose Midrib of thallus ill-defined Central strand lacking DioicousAntheridia individually protected by a scale Capsule spherical wall irregularly tearinginto 5-7 unequal valves epidermal cells with irregular bands without elaterophoreSpores strongly sculptured - 2 genera (5) - Allisonia Herzog (1) endemic NewZealand - Calycularia Mitt (4) N and E Asia Himalayas

Molecular data indicate that the Allisoniaceae are not monophyletic Both generahave similar capsule walls and thallus structures but differ by the presence of awell-developed pseudoperianth in Calycularia (eg Inoue 1976) The placement ofCalycularia has traditionally been problematic and is still tentative based on itsposition sister to the Fossombronialean and Pallavicinialean liverworts in moleculartrees

Fam Sandeothallaceae RM Schust

Plants thallose Thalli simple or rarely branched with uniseriate slime hairs occasionalwith ventral branches Rhizoids reddish Antheridia in axils of dorsal scales alongmidrib surface Seta massive Capsule wall (3)4-5(6)-layered opening by 2 lateralslits without elaterophore - Monotypic - Sandeothallus RMSchust (1) IndiaMalesia Samoa

The systematic position remains ambiguous Morphologically Sandeothallus occupiesan intermediate position gametophytic characters indicate close relationship toAllisoniaceae whereas sporophytically it is close to the Pallaviciniaceae (Schuster1982) Molecular data are so far not available

2 Class Pallaviciniopsida WFrey amp Stech class nov

Plantae thallinae prostratae vel in axem prostratum stipitemque erectum divisae partim dendroideaeCosta thalli prominens 1 vel 2(-4) filis centralibus Cellulae filorum centralium elongatae perforataehydroideis similes Capsulae ovoideae ad cylindricae 2 vel 4 valvis dehiscentes

Type family Pallaviciniaceae Mig

Plants thallose prostrate erect or sometimes dendroid Dendroid taxa evolved threetimes independently in Jensenia and Symphyogyna (Pallaviciniaceae) as well as inHymenophyton (Hymenophytaceae) (Schaumann et al 2005) Gametophyte mostlywith central strand composed of thick-walled elongated water-conducting cells withperforations (pores) This pallavicinoid type of water-conducting cells occurs onlyin the Pallaviciniopsida and is unique in bryophytes Antheridia and archegonia(clustered) on dorsal surface of thallus Sporophyte protected by a pseudoperianth(inner involucre) or stem-calyptra Seta massive Capsule ellipsoidal to cylindricaltearing into 2 imperfectly 4 or 4 valves wall bistratose Gametophyte-sporophytejunction gametophyte placental cells without wall ingrowths sporophyte placental

64

cells partly without wall ingrowths Fossil records Pallaviciniites devonicus (Hueber)RMSchust from lowermost Upper Devonian (375 mio y) is the oldest true bryo-phyte fossil known The thallose plant bearing a central strand in the gametophyteaxis is superficially similar to the Pallaviciniaceae in particular to Pallavicinia andSymphyogyna Laticaulina papillosa Krassilov from Late Jurassic of Russia alsoshows affinities to the Pallaviciniopsida (Symphyogyna) About 65 species

1 Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Basionym Pallaviciniineae RMSchust Phytologia 56 65 1984

Type (and only) family Pallaviciniaceae Mig

Schuster (1984b) erected the Pallaviciniineae to include PallaviciniaceaeSandeothallaceae and Makinoaceae In contrast we consider the Pallavicinialesmonotypic at least until relationships of Sandeothallus and Makinoa have beenclarified on the molecular level

Fam Pallaviciniaceae Mig

Plants thallose prostrate without basal stipe and ldquorhizomerdquo or erect arising froma ldquorhizomerdquo or stipe dendroid in Jensenia and some species of Pallavicinia andSymphyogyna Thallus with well-defined midrib with 1 or 2(-4) central strandsin most taxa present and unistratose lamina Water conducting cells elongatedwith tapering ends and thickened walls (c 8 microm wide and up to 300 microm long)throughout with numerous pits produced by dissolution of secondary wallmaterial associated with modified plasmodesmata Only few true plasmodesmata-derived perforations (pores) present (Oslash 200-400 nm) No relationship withtracheids (Frey et al 1996) Slime papillae on both dorsal and ventral surfacesof apex sometimes present Ventral scales absent or small and uniseriate DioicousAntheridia on dorsal surface of thallus often in 2-several ranks associated withscales Archegonia clustered on dorsal surface of midrib (gynoecia) deliminatedby a single (Symphyogyna) or double involucres (except Xenothallus) Developingsporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-calyptra Seta long massive Capsule elongate-cylindrical to ovoid dehiscenceby 2 or imperfectly 4 valves epidermal cell walls lacking thickenings Spores 1-celled Elaterophore rudimentary or absent Elaters 2-3-helical Gametophyte-sporophyte junction Wall ingrowths (transfer cells) present in the outermostsporophytic placental layer - 9 genera (c 60) Gondwanan centres of diversityin Australasia and S America

Molecular analyses resolve Pallaviciniaceae as monophyletic (eg Forrest ampCrandall-Stotler 2005 Schaumann et al 2005) These data support a separationof Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa a positionof Podomitrium (Podomitrioideae RMSchust) close to the Symphyogynoideae(Trevis) RMSchust ex Grolle and polyphyly of Pallavicinia and thePallavicinioideae Because of ambiguous relationships between these subfamilieswe include Podomitrioideae and Symphyogynoideae in Pallavicinioideae sl

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

64

cells partly without wall ingrowths Fossil records Pallaviciniites devonicus (Hueber)RMSchust from lowermost Upper Devonian (375 mio y) is the oldest true bryo-phyte fossil known The thallose plant bearing a central strand in the gametophyteaxis is superficially similar to the Pallaviciniaceae in particular to Pallavicinia andSymphyogyna Laticaulina papillosa Krassilov from Late Jurassic of Russia alsoshows affinities to the Pallaviciniopsida (Symphyogyna) About 65 species

1 Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Basionym Pallaviciniineae RMSchust Phytologia 56 65 1984

Type (and only) family Pallaviciniaceae Mig

Schuster (1984b) erected the Pallaviciniineae to include PallaviciniaceaeSandeothallaceae and Makinoaceae In contrast we consider the Pallavicinialesmonotypic at least until relationships of Sandeothallus and Makinoa have beenclarified on the molecular level

Fam Pallaviciniaceae Mig

Plants thallose prostrate without basal stipe and ldquorhizomerdquo or erect arising froma ldquorhizomerdquo or stipe dendroid in Jensenia and some species of Pallavicinia andSymphyogyna Thallus with well-defined midrib with 1 or 2(-4) central strandsin most taxa present and unistratose lamina Water conducting cells elongatedwith tapering ends and thickened walls (c 8 microm wide and up to 300 microm long)throughout with numerous pits produced by dissolution of secondary wallmaterial associated with modified plasmodesmata Only few true plasmodesmata-derived perforations (pores) present (Oslash 200-400 nm) No relationship withtracheids (Frey et al 1996) Slime papillae on both dorsal and ventral surfacesof apex sometimes present Ventral scales absent or small and uniseriate DioicousAntheridia on dorsal surface of thallus often in 2-several ranks associated withscales Archegonia clustered on dorsal surface of midrib (gynoecia) deliminatedby a single (Symphyogyna) or double involucres (except Xenothallus) Developingsporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-calyptra Seta long massive Capsule elongate-cylindrical to ovoid dehiscenceby 2 or imperfectly 4 valves epidermal cell walls lacking thickenings Spores 1-celled Elaterophore rudimentary or absent Elaters 2-3-helical Gametophyte-sporophyte junction Wall ingrowths (transfer cells) present in the outermostsporophytic placental layer - 9 genera (c 60) Gondwanan centres of diversityin Australasia and S America

Molecular analyses resolve Pallaviciniaceae as monophyletic (eg Forrest ampCrandall-Stotler 2005 Schaumann et al 2005) These data support a separationof Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa a positionof Podomitrium (Podomitrioideae RMSchust) close to the Symphyogynoideae(Trevis) RMSchust ex Grolle and polyphyly of Pallavicinia and thePallavicinioideae Because of ambiguous relationships between these subfamilieswe include Podomitrioideae and Symphyogynoideae in Pallavicinioideae sl

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

65

Subfam Moerckioideae RMSchust

Thalli without stipe-like base laterally branched Midrib without sharply definedcentral strand (Moerckia) although sometimes with a weakly defined pair of strandsconsisting of slightly elongated cells with swollen walls but without pits remnantsof plasmodesmata occasionally visible Two central strands present in HattorianthusVentral scales uniseriate fugacious Gametangia dorsally on leading thalli Antheridiain axils of scales Pseudoperianth (inner involucre) developes after fertilization - 2genera - Moerckia Gottsche (3-4) Holarctic N to 82deg - Hattorianthus RMSchustamp Inoue (1) endemic stenotype E Asia Japan Probably an early-diverging branchoriginating from a Pangaean ancestor which evolved separately in the Holarctic Incontrast to the original circumscription of Moerckioideae by Schuster (1982)Greeneothallus is excluded and Hattorianthus included

Subfam Pallavicinioideae Mig ex Grolle

(incl Symphyogynoideae [Trevis] RMSchust ex Grolle and PodomitrioideaeRMSchust)

Inner involucre (pseudoperianth) distinct tubular hiding the rather thin stem-calyptrawithin Thalli narrowed and typically stipe-like at base or dendroid Midrib with aconspicuous single or pair of central strands Gametangia dorsal on leading thalliandroecia never spicate with individual antheridia hidden under distinct scales clearlyanacrogynous (formerly subfam Pallavicinioideae and Symphyogynoideae)Gametangia terminating determinate reduced intercalary branches from lower stipe-like sectors of sterile fronds Androecia spicate antheridia sunken in alveoli acrogynous(formerly subfam Podomitrioideae) - 7 genera (c 55) Mainly Gondwanan centresof diversity in Australasia and S America - Pallavicinia Gray (c 15) temperate-tropical P lyellii (Hook) Carruth supposedly subcosmopolitan Ancient taxonprobably of Pangaean origin - Jensenia Lindb (8-9) southern temperate subantarcticand alpine-tropical centre of diversity in S America lacking in Laurasia - SymphyogynaNees amp Mont (c 25) incl Symphyogynopsis Grolle Centre of diversity in theNeotropics and Australasia lacking in Laurasia Probably not monophyletic accordingto molecular data (cf Schaumann et al 2005) - Podomitrium Mitt (2) AustralasiaMalesia endemic stenotypes Close to Symphyogyna recognition in a monotypicsubfamily is not supported by molecular data (Schaumann et al 2005) - XenothallusRMSchust (1) New Zealand endemic stenotype - Greeneothallus Haumlssel (1) SGeorgia endemic stenotype - Seppeltia Grolle (1) Subantarctic Macquarie I NewZealand (South I) isolated endemic stenotype provisionally placed in Pallaviciniaceae

2 Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Basionym Hymenophytineae RMSchust Phytologia 56 66 1984

Type (and only) family Hymenophytaceae RMSchust

Fam Hymenophytaceae RMSchust

Plants thallose dendroid divided into prostrate rhizome-like axes erect stipeand pluridichotomous flattened fan-shaped megaphyll-like frond thus

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

66

mimicking Hymenophyllaceae Wings unistratose Well-defined midribs presentwith a central strand and water-conducting cells of pallavicinoid-type Ventralscales lacking Gametangia on morphologically dorsal surface of abbreviatedhighly specialized sexual branches originating from ventral surface of midribat distal sectors of thallus Androecial branches reduced to small protuberancesthe antheridia each with an individual involucre Gynoecial branches reducedto sessile cushions Involucre double outer involucre of 2 opposing leaf-likescales inner involucre (pseudoperianth) elongated a cylindrical tube lobedand toothed at mouth Stem-calyptra present Capsule cylindrical and 4-valvedSpores unicellular Elaterophore present Elaters whip-like very slenderGametophyte-sporophyte junction Wall ingrowths (transfer cells) absent inthe placental cells of both generations - Monotypic - Hymenophyton Dumort(3) Gondwananpalaeoaustral strictly antipodal (cf Pfeiffer et al 2004)Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidaleanliverworts

3 Class Pelliopsida WFrey amp Stech class nov

Plantae thallinae thalli simplices sine filis centralibus Antheridia singulariter cavernulis adsuperficiem thalli dorsalem inserta Capsulae sphericae 4 valvis dehiscentes Elaterophorum basaleadest

Type family Pelliaceae HKlinggr

Plants thallose without stipe-like bases and mostly without ventral branchesBranching pseudodichotomous Apical cell wedge-shaped or hemidiscoidal Centralstand lacking Antheridia sunken individually into chambers on the dorsal surfacealong the longitudinal axis and ldquoroofed overrdquo by conoidal projections Archegoniain distinct groups on the dorsal thallus surface Involucre short-tubular or flaplikeCapsules spherical with subisodiametric epidermal cells dehiscing to base into 4regular valves Spores multicellular Elaterophores basal Fossil records As noventral scales are observed Blasiites lobatus (JWalton) RMSchust could perhapsrather be assigned to Pelliaceae than to Blasiaceae

Separated from Fossombroniopsida and Pallaviciniopsida by simple thallusorganisation and arrangement of antheridia Probably a phylogenetically old groupthat became adapted to hyperhygric habitat conditions

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Basionym Pelliineae RMSchust ex Schljakov

Type (and only) family Pelliaceae HKlinggr

Fam Pelliaceae HKlinggr

Plants fleshy thallose sparringly irregularly furcate Thalli with an obscurely definedmidrib margins with irregularly shallow lobes Di- or monoicous Family restrictedto include only Pellia (concerning the position of Noteroclada see below) - PelliaRaddi (5[-6]) Holarctic cool and temperate regions

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

67

Families of uncertain positions in superclass III

Fam Makinoaceae Nakai

Thalli green margins pale crispate Dioicous Androecia sunken but aggregated atthe apex of dorsal frond surface Oil-bodies small 6-10(15) per cell Slime papillaeseptate forming slime hairs Gynoecia posteriorly shielded by a single scalePseudoperianth lacking Sporophyte protected by a calyptra Capsule opening by alateral slit elaterophore lacking Elaters 1-helical and ehelical - Monotypic - MakinoaMiyake (1) E Asia Philippines New Guinea

In molecular analyses Makinoa is either sister to a clade of Fossombronia andHaplomitrium (He-Nygreacuten et al 2004 the position of Haplomitrium is affected bythe absence of Treubia in their analyses) or occupies a basal position among the taxaof superclass III (Heinrichs et al 2005) Placement in the Pelliineae and in particulara close relationship with Verdoornia as proposed by Schuster (1964) is clearlydisproved by the molecular data

Fam Noterocladaceae (RMSchust) WFrey amp Stech fam et stat nov

Basionym Pelliaceae subfam Noterocladoideae RMSchust J Hattori Bot Lab 70 145 1991

Type (and only) genus Noteroclada Taylor ex Hook amp Wilson type species N confluens Taylor exHook amp Wilson London J Bot 3 166 1844

Plants leafy with tetrahedral apical cell Leaves succubous Branching at least partlylateroventral Central strand lacking Antheridia scattered in small cavities cavitiespartially elevated above axis Archegonia in clusters surrounded by a compressed-tubular involucre (pseudoperianth) Capsule spherical Spores large up to 100 microm inOslash multicellular green germination endosporous Seta 2-8(10) cm long thickMonotypic - Noteroclada Taylor ex Hook amp Wilson (1-2) (Afro)-Central tosouthern S America probably Gondwanan origin

Molecular data (eg He-Nygreacuten et al 2004 Forrest amp Crandall-Stotler 2005Heinrichs et al 2005 Schaumann et al 2005) are ambiguous concerning relationshipsof Noteroclada The polyphyly of Noteroclada in Heinrichs et al (2005) indicatesthat one of the sequenced samples is either misidentified or contaminated The mostreliable topology supports a position of Noteroclada sister to Pellia (Forrest ampCrandall-Stotler 2005 70 bootstrap support)

Fam Phyllothalliaceae EAHodgs

Plants leafy Stems consisting of nodes and internodes Conducting strand absent Leavesopposite polystratose succubous Leaf cells very large and thin-walled trigones absentMucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface ofaxis Ventral appendages or scales absent Rhizoids colorless Dioicous Antheridia andarchegonia clustered on dorsal surface of axis (androecia gynoecia) associated withperichaetial or perigonial scales resp Sporophytes protected by a stem-calyptra Setaemassive Capsules tearing into 12-14 valves (Schuster 1984a) epidermal cells withnodular thickenings Elaterophores at capsule base - Monotypic - PhyllothalliaEAHodgs (2) New Zealand Tierra del Fuego isolated relict taxon

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

68

Schljakov (1972) erected the order Phyllothalliales (RMSchust) Schljakov andplaced it together with Treubiales Fossombroniales and Metzgeriales in thesuperorder Metzgerianae Schljakov Molecular data (Forrest amp Crandall-Stotler 2005Heinrichs et al 2005) indicate a sistergroup relationship with Pallaviciniopsidawhich however are clearly distinct at least gametophytically

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

In the present circumscription the class Jungermanniopsida comprises leafy liverwortsand the Metzgerialean-type simple thallose liverworts Molecular data confirm acommon origin of the subclasses Jungermanniidae Pleuroziidae and Metzgeriidaebut their relationships remain ambiguous The ancestral type of these liverwortsprobably also had a simple thallose gametophyte growing via a cuneate apical cellwith four cutting faces and a sporophyte with massive foot and seta Leafy taxawith radially symmetrical gametophytes and 3 rows of transversely (or nearly so)inserted leaves were assumed to be early-diverging groups from which anisophyllyoblique inserted leaves and thallose forms derived as indicated by the loss of transfercells in the gametophyte-sporophyte junction

1 Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts Jungermanniales acrogynae excludingPleurozia) are the largest group of liverworts with about 5500 species monosymmetricand anisophyllous or isophyllous Few taxa secondarily thallose (eg MetzgeriopsisKIGoebel) Gametophytic shoots with tetrahedral apical cell (three cutting faces)and (usually) well-differentiated stems and leaves Stems without central strandaxis usually with outer cortex and inner more delicate medulla Leaves withoutmidrib basically 2-lobed arising from 2 initial cells or 3-several-lobed or undividedmost commonly differentiated as 2 rows of lateral leaves and a single row of ventralunderleaves (amphigastria) Insertion of the lateral leaves transverse or morecommonly oblique plants therefore plusmn flattened with mostly overlapping leaves ineither incubous or succubous orientation Complex-bilobed lateral leaves folded toform ventral and dorsal lobes Dorsal lobe mostly larger than ventral one the ventrallobe may be highly modified into a pouch helmet-shaped lobule or sac Underleavesfrequently small or lacking Leaf cells with or without trigones Oil-bodies usuallypresent in all chorophyllose cells of the gametophyte Rhizoids usually present smoothAntheridia restricted to the axils of leaves sometimes underleaves Archegoniaformation from apical cell terminal on main or branch axes (acrogynous) Developingsporophyte usually protected by a tubular perianth derived from 2 or 3 modifiedfused leaves of important taxonomic value Seta long and distinctly elongating thesporophyte Capsules spherical to cylindrical wall 2-10-stratose regularly dehiscingby 4 valves Spores 6-24(-60) microm Characteristic gametophyte-sporophyte junctionProminent wall labyrinths with thin highly branched wall ingrowths are restrictedto usually one or rarely two layers of the sporophyte side of the placenta gametophyteplacental walls lack ingrowth collapsed gametophyte cells mark the placental space

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

69

Fossil records Lack of any evidence of leafy Jungermanniidae in the Palaeophyticexcept probably Jungermaniites keuperianus (De Gasparis) Oostendorp UpperTriassic Jungermannites gracilis (THalle) Oostendorp from Middle Jurassic ofAntarctic Peninsula is the earliest member of Jungermanniales another early memberof Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic The earlydiversification of the Jungermanniidae is assumed to have taken place inGondwanaland as the major evolutionary events have been confined to GondwanaThe main diversification took place in lsquoco-evolutionrsquo with the evolution of angiospermsand the establishment of tropical rain forest ecosystems

The Jungermanniidae form a clade sister to the Metzgeriidae sstr in the molecularanalyses of Davis (2004) and Forrest amp Crandall-Stotler (2005) Molecular datasupport a separation of Jungermanniidae into two main groups (eg Davis 2004Stech amp Frey 2004 Forrest amp Crandall-Stotler 2005 Heinrichs et al 2005) whichare with exceptions also distinguishable morphologically and ecologically (cfHeinrichs et al 2005) The first group comprises Porellales (RMSchust) SchljakovRadulales (RMSchust) Stotler amp Stotl-Crand and Lepicoleales Stotler amp Stotl-Crand pp and the second Jungermanniales HKlinggr and also some Lepicolealessensu Crandall-Stotler amp Stotler (2000) Both groups were comprised as ordersJungermanniales and Porellales respectively by Heinrichs et al (2005) In congruencewith the high-level classification presented here however we prefer to separate thetwo main lineages as superorders which allows for an ordinal reclassification of thefamilies in future studies For families see synopsis below as well as Stotler amp Crandall-Stotler (2000) and Heinrichs et al (2005)

1 Superorder Jungermannianae WFrey amp Stech superord nov

Ramificatio ventralis insertio foliorum succuba et rhizoidea non fasciculata adsunt Folia plerumque2 initiis crescentia Protonema plerumque exosporum Plantae praecipue terricolae

Type family Jungermanniaceae Reichenb

Occurrence of ventral branching succubous leaf orientation and non-fasciculaterhizoids Protonema normally developing exosporous Development of leaves normallyby means of two initial cells Lack of water-sacs Frequently terrestrial if epiphyticwithout clear morphological adaptations to the epiphytic habitat

2 Superorder Porellanae WFrey amp Stech superord nov

Ramificatio ventralis deest Folia 3 initiis crescentia plerumque biloba lobulus ventralis partim insacculum aut vesiculam aquam continentem transformatum Insertio foliorum incuba vel transversalisRhizoidea fasciculata Sporae multicellulares protonema endosporum Praecipue epiphyta

Type family Porellaceae Cavers

Lack of ventral branching Most taxa with complicate-bilobed leaves with incubousor transverse orientation Rhizoids in bundles (fasciculate) Multicellular spores withendosporous protonema Development of leaves by means of three initial cellsPredominantly epiphytes development of specialized lobules or water-sacs on theventral side of leaves and endosporous protonema probably associated with theepiphytic habitat

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

70

2 Subclass Pleuroziidae WFrey amp Stech subclass nov

Plantae foliosae ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisaemerophyta ventralia nulla foliaque disticha Folia prima elobulata folia secunda plerumque in lobulumdorsalem minorem atque in lobum ventralem maiorem divisa Lobulus dorsalis in sacculum autvesiculam aquam continentem transformatum Gynoecia fertilia steriliaque plerumque adsunt

Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963) weprovide a modified diagnosis for the subclass that considers later publications (egThiers 1993) and allows a clearer distinction from the Jungermaniidae sstr

Order Pleuroziales (RMSchust) Schljakov

Fam Pleuroziaceae (Schiffn) MuumlllFrib

Plants leafy usually purplish Stems ascending Only leafy liverwort group with anapical cell with 2 cutting faces (lenticular as in Metzgeriidae) ie stems with notrace of a ventral merophyte and leaves distichous with clasping bases Leaves simplewith the lobule most rudimentary (elobulate) or complicate-bilobed (explanate-lobuled or saccate-lobuled) Larger leaf lobe ventral strongly succubously insertedsmaller lobe (lobule) dorsal with a complex water sac Underleaves lacking Trigonesvery large Structure of the gametophyte-sporophyte junction not known Androeciaand gynoecia on short lateral-axillary branches fertile and sterile gynoecia oftenpresent Gynoecial branches with bi- or trilobed bracts Perianth elongate Capsulespherical to short-ovoid - Monotypic - Pleurozia Dumort (11) primarily epiphytesin moist montane tropical forests

Pleurozia for a long time regarded as an isolated element of the leafy liverwortlineage is resolved by molecular analyses (eg Davis 2004 Heinrichs et al 2005)as sister to a clade of Metzgerialean liverworts (Metzgeriaceae AneuraceaeVerdoorniaceae) Unique features comprise the 2-sided apical cell the specializedwater sac and the sterile gynoecia (eg Thiers 1993) In contrast to the single leafinitial in simple thalloid liverworts that have lsquoleafyrsquo gametophytes leaves of Pleuroziadevelop from 2 initial cells as is typical of true leafy liverworts The distinction ofPleurozia on subclass level indicates that the leafy gametophyte of Pleurozia mayhave developed independently from the Jungermanniidae as circumscribed here byconvergent evolution

3 Subclass Metzgeriidae SEBarthol

Jungermanniales anacrogynae pp Metzgeriales I sensu Forrest amp Crandall-Stotler (2004)

Bartholomew-Began (1990) established the subclass Metzgeriidae for all simplethalloid liverworts (Jungermanniales anacrogynae) In the present circumscriptionthe Metzgeriidae comprise only Aneuraceae Metzgeriaceae Verdoorniaceae(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae andthus at least partly correspond to suborder Metzgeriineae RMSchust

Plants thallose never with leaf-like appendages Apical cell lenticular Gametophyteslacking sharp division into terete stipes and thalli Oil-bodies lacking (Metzgeriaceae)or 1-several per cell large or small Rhizoids in addition to a group situated ventrally

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

71

along midrib often at thallus margins Antheridia and archegonia both clustered insharply delimited androecia and gynoecia on special branches except VerdoorniaAntheridia short-stalked Archegonia often few reduced with very short to absentnecks Sporophytes enclosed in fleshy tissue (calyptra or perigynium) other protectivedevices (perichaetia pseudoperianths) lacking Seta tending to become abbreviatedoften reduced Capsule 4-valved or opening by a lateral slit with conspicuous nodularthickening of epidermal cells Apical elaterophores present Elaters 1-helical or ehelicalrelatively short Spores often lt 20 microm Gametophyte-sporophyte junction bothgametophyte and sporophyte placental cells lack wall ingrowths in Aneura andMetzgeria collapsed cells of gametophytic origin always present in the placentalspace lack of transfer cells in the gametophyte generation is interpreted as a reductionnacreous walls occur in both gametophyte and sporophyte placental layers Fossilrecords Except Hepaticites langii JWalton superficially resembling Metzgeria orAneura no Metzgerialean-like fossils are known Gametophytes in the Metzgeriidaeclade sstr vary from large fleshy undifferentiated thalli (like those of Verdoorniaand Aneura) to small delicate thalli differentiated into midrib and wing as inMetzgeria The Metzgeriidae sstr probably represent a relatively young evolutionarylineage of secondarily simple thallose forms

1 Order Aneurales WFrey amp Stech ord nov

Ordo Metzgeriales similis sed thalli uniformes sine costa alisque unistratosis guttae olei plerumqueadsunt Sporophytum calyptra nuda tutum Elaterophorum apicale prominens vel rudimentale

Type family Aneuraceae HKlinggr

Plants thallose Thalli lacking sharp division into well-defined midrib and unistratosewings without leaf-like lobes Central strand lacking Sporophyte protected by acalyptra (most of the calyptra represents a new tissue developed from the tissuebelow the archegonium a small portion derived from the ventral wall of the fertilizedarchegonium) Involucres and pseudoperianths absent

Fam Aneuraceae HKlinggr

Thalli of several cell layers irregularly branched to regularly 1-3-pinnate sometaxa dendroid Slime papillae present at the apex of axes Specialized marginal rhizoidslacking Oil-bodies usually present (in all or some cells) in most taxa Gametangiaon the dorsal surface of short highly reduced lateral branches Antheridia to varyingdegrees immersed in cavities serially arranged and surrounded either individuallyor in groups of 2 or 3(-5) by flask-shaped to tubular outgrowths of the thallusCalyptra fleshy massive Capsule ovoid to cylindrical outer layer with nodularthickenings on the radial walls dehiscing into 4 valves Elaters 1-helicalElaterophores apical and brushlike Spores unicellular - 4 genera - Aneura Dumort(c 15[-25]) large fleshy und undifferentiated thalli Epidermal cells each with 6-12(12-18 30-60) small oil-bodies Most species dioicous plants smaller than Spores 19-26 microm Taxonomy of Aneura has not been studied critically on a worldwidebasis the distribution of the species remains incompletely known - Lobatiriccardia(Mizut amp SHatt) Furuki (4) Malesia Australasia Japan Thalli large 1-10 cmlong translucent bluish green when fresh segments usually 3-6(7) mm wide densely

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

72

pinnate to bipinnate branching only lateral Epidermal thallus cells with (3-5)6-12relatively large oil-bodies of different size Dioicous Spores 12-19 microm Moleculardata suggest a sister relationship between Aneura and Lobatiriccardia - CryptothallusMalmb (2) Achlorophyllous subterranean saprophyte (unique among bryophytes)especially under moss carpets Thallus densely covered by rhizoids Fungal symbiosis(mycorrhiza) Oil-bodies lacking or few Dioicous Molecular sister genus to Aneura- Riccardia Gray (c 175) subcosmopolitan highest diversity in temperate and coolregions of former Gondwanaland eg 50 of Australasian taxa endemic Thallidelicate considerably varying in habit 1-10 cm long 1-3-pinnately branched sometaxa with erect dendroid growth composed of multiple layers of cells in cross-section without midrib Epidermal cells smaller than inner cells of thalli Cells eachwith 1-3(5-8) large oil-bodies many epidermal cells lacking oil-bodies Slime papillaeclavate 1-2-celled Di- aut- or synoicous Androecial branches with 2 rows ofantheridia Gynoecia on distinct but very short lateral branches Calyptra greenfleshy never scaly or hairy Elaterophores hardly developed Spores 9-15(20-25)microm in Oslash (1)2-celled gemmae endogenously produced by epidermal cells Intragenericrelationships imperfectly known

Fam Verdoorniaceae Inoue

Large fleshy und undifferentiated thalli nearly structureless Dioicous Antheridiaindividually sunken in alveoli Oil-bodies very large 1-3(4) per cell Slimepapillae 1(2)-celled clavate exceedingly large secreting massive amounts ofmucilage Archegonia sessile diffused along the midline of the midrib Gynoeciasurrounded by laciniiform scales Involucres and pseudoperianths lackingSporophyte protected by a calyptra Capsules 4-valved with weak apicalelaterophore Elaters 2-helical - Monotypic stenotype - Verdoornia RMSchust(1) endemic New Zealand

Differs from all other Metzgeriidae sl in the stout short archegonia withoutdifferentiation of a neck and without basal constriction Supposed to be a relic fromthe Palaeozoic lacking any contact points to other Metzgeriales sl However inmolecular trees (eg Stech amp Frey 2001 Forrest amp Crandall-Stotler 2005) Verdoornianests in the Metzgerialean clade

Fam Vandiemeniaceae Hewson

branches cucullate ventral-intercalary Antheridia dorsal on the androecial branchesnot immersed Otherwise like Riccardia - Monotypic - Vandiemenia Hewson (1)endemic Tasmania Relict taxon Possible ancestor linking modern Aneuraceae andMetzgeriaceae So far not included in molecular analyses

Fam Mizutaniaceae Furuki amp ZIwats

Thalli ribbon-like unistratose throughout resembling a fern prothallium oftensubterraneous with many rhizoids Oil-bodies present brownish Perichaetia distinctsmall sessile at margins of thallus Involucres double Gemmae exogenous 1-4-

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

73

celled Antheridia and sporophytes unknown - Monotypic - Mizutania Furuki amp ZIwats (1) Malay Peninsula Borneo One of the simpliest thalli and one of the mostspecialized taxa among liverworts in both vegetative and reproductive structures

So far not included in molecular phylogenies Although most probably a member ofthe Metzgeriidae sstr the systematic placement in the Aneurales remains uncertainand is mainly based on the presence of oil-bodies (resembling those of Riccardia)and the lsquoinflorescencersquo resembling those of both Riccardia and Aneura In contrastthe marginal rhizoids are similar to the marginal hairs of Metzgeria and juvenilethallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki ampIwatsuki 1989)

2 Order Metzgeriales RMSchust ex Schljakov

Fam Metzgeriaceae HKlinggr

Thalli linear with narrow well-defined midrib (in cross section with unistratosecortex and inner medullar cells) and unistratose wings Central strand lacking Apicalcell lenticular with 2 cutting faces Branching primarily terminal dichotomoussometimes ventral-intercalary from ventral side of the midrib Apices protected byephemeral 1-celled clavate slime papillae arising in 2 ranks alternately on eitherside of the midrib Unicellular setose hairs often present on thallus margins (pairedor single) and on ventral surface of midrib occasionally on ventral surface of thewings Oil-bodies lacking or very small (structureless oil-droplets) Dioicous orautoicous Gametangia formed on short highly abbreviated specialized branchesarising from the ventral side of the midrib branches with midrib lacking hairs(ventral surface in Apometzgeria) branches lacking midrib hairy Sporophyteprotected by an elongate hairy fleshy (ldquostemrdquo-)calyptra Pseudoperianth lackingSeta short Capsule short-ovoid to subglobose 4-valved to base with an apicalelaterophore wall bistratose Elaters 1-helical or ehelical attached in bundles at thevalve apex - 4 genera (c 140) cosmopolitan continental areas are devoid ofMetzgeriaceae - Apometzgeria Kuwah (2) N Hemisphere southern S AmericaThallus densely hairy on both surfaces - Metzgeria Raddi (c 135) principally tropicaland S temperate subcosmopolitan Thalli with hairs confined to margins ventralsurface of midrib and sometimes ventral side of wings never copiously hairy ondorsal surface green to brownish sometimes bluish Sexual branches all ventral-intercalary (ventral side of midrib) highly reduced hidden under the thallus wings- Austrometzgeria Kuwah (1) Australasia stenotypic genus Thallus lobed lobemargins saccate (water-sacs) (ldquoStemrdquo-)calyptra covered by flat longitudinallyoriented multicellular dentate scales - Steereella Kuwah (2) Jamaica DominicanRep Cuba Marginal cells of thallus elongated thick-walled (as in mosses) Elatersehelical

Close relationship with Hymenophytaceae as postulated earlier is not confirmed bymolecular analyses (eg Forrest amp Crandall-Stotler 2005 Schaumann et al 2005)It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpointsin parallel evolutionary lineages

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

74

Synopsis of the suprageneric classification of Hepaticophytina

Superclass I

Class Treubiopsida Stech J-PFrahm Hilger amp WFrey

Order Treubiales Schljakov

Treubiaceae Verd

Class Haplomitriopsida Stotler amp Stotl-Crand

Order Haplomitriales HBuch ex Schljakov

Haplomitriaceae Dědeček

Superclass II

Class Blasiopsida Stech amp WFrey

Order Blasiales (RMSchust) Stotler amp Stotl-Crand

Blasiaceae HKlinggr

Class Marchantiopsida Stotler amp Stotl-Crand

Subclass Sphaerocarpidae Stotler amp Stotl-Crand

Order Sphaerocarpales Cavers

Sphaerocarpaceae (Dumort) Heeg Riellaceae Engl

Subclass Marchantiidae Engl

Order Monocleales RMSchust

Monocleaceae (Nees) ABFrank

Order Marchantiales Limpr in Cohn

Aytoniaceae Cavers Cleveaceae Cavers ConocephalaceaeMuumlllFrib ex Grolle Corsiniaceae Engl Cyathodiaceae(Grolle) Stotler amp Stotl-Crand Exormothecaceae MuumlllFribex Grolle Lunulariaceae HKlinggr Marchantiaceae (Bisch)Lindl Monocarpaceae DJCarr ex Schelpe MonosoleniaceaeInoue Targioniaceae Dumort Wiesnerellaceae Inoue

Order Ricciales Schljakov

Oxymitraceae MuumlllFrib ex Grolle Ricciaceae Reichenb

Superclass III

Class Fossombroniopsida WFrey amp Hilger

Order Fossombroniales Schljakov

Fossombroniaceae Hazsl Petalophyllaceae (RMSchust)

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

75

Stotler amp Stotl-Crand Allisoniaceae (RMSchust ex Grolle)Schljakov Sandeothallaceae RMSchust

Class Pallaviciniopsida WFrey amp Stech class nov

Order Pallaviciniales (RMSchust) WFrey amp Stech stat nov

Pallaviciniaceae Mig

Order Hymenophytales (RMSchust) WFrey amp Stech stat nov

Hymenophytaceae RMSchust

Class Pelliopsida WFrey amp Stech class nov

Order Pelliales (RMSchust) WFrey amp Stech stat nov

Pelliaceae HKlinggr

Families of uncertain positions in superclass III

Makinoaceae Nakai Noterocladaceae (RMSchust) WFreyamp Stech fam et stat nov Phyllothalliaceae EAHodgs

Superclass IV

Class Jungermanniopsida Stotler amp Stotl-Crand

Subclass Jungermanniidae Engler

Superorder Jungermannianae WFrey amp Stech superord nov

Families see Stotler amp Crandall-Stotler (2000) and Heinrichs etal (2005)

Superorder Porellanae WFrey amp Stech superord nov

Goebeliellaceae Verd Jubulaceae HKlinggrJubulopsidaceae (Hamlin) RMSchust Lejeuneaceae Casares-Gil Lepidolaenaceae Nakai Neotrichocoleaceae InouePorellaceae Cavers Ptilidiaceae HKlinggr Radulaceae(Dumort) MuumlllFrib

Subclass Pleuroziidae WFrey amp Stech subclass nov

Order Pleuroziales (RMSchust) Schljakov

Pleuroziaceae (Schiffn) MuumlllFrib

Subclass Metzgeriidae SEBarthol

Order Aneurales WFrey amp Stech ord nov

Aneuraceae HKlinggr Mizutaniaceae Furuki amp ZIwatsVandiemeniaceae Hewson Verdoorniaceae Inoue

Order Metzgeriales RMSchust ex Schljakov

Metzgeriaceae HKlinggr

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

76

Acknowledgements

Sincere thanks are due to H Luumlnser for preparing Fig 1

References

BARTHOLOMEW-BEGAN SE (1990) Classification of the Haplomitriales and Metzgerialesinto the subclass Metzgeriidae subclass nov (Hepatophyta Jungermanniopsida) - Phytologia 69164-166

BOPP M amp I CAPESIUS (1998) A molecular approach to bryophyte systematics - In BATESJW NW ASHTON amp JG DUCKETT (eds) Bryology for the twenty-first century 79-88Maney Publ Leeds

CARAFA A JG DUCKETT amp R LIGRONE (2003) The placenta in Monoclea forsteri Hookand Treubia lacunosa (Col) Prosk Insights into placental evolution in liverworts - Ann Bot 92299-307

CAROTHERS ZB amp AE RUSHING (1988) Comparative morphology of the bryophyteblepharoplast - Adv Bryol 3 95-134

CRANDALL-STOTLER B amp RE STOTLER (2000) Morphology and classification of theMarchantiophyta - In SHAW AJ amp B GOFFINET (eds) Bryophyte biology 21-70 CambridgeUniv Press Cambridge

DAVIS EC (2004) A molecular phylogeny of leafy liverworts (Jungermanniidae Marchantiophyta)- In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes- Monogr Syst Bot Missouri Bot Gard 98 61-86

FORREST LL amp BJ CRANDALL-STOTLER (2004) A phylogeny of the simple thalloidliverworts (Jungermanniopsida Metzgeriidae) as inferred from five chloroplast genes - InGOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecular Systematics of Bryophytes -Monogr Syst Bot Missouri Bot Gard 98 119-140

FORREST LL amp BJ CRANDALL-STOTLER (2005) Progress towards a robust phylogeny forthe liverworts with particular focus on the simple thalloids - J Hattori Bot Lab 97 127-159

FREY W HH HILGER amp M HOFMANN (1996) Water-conducting cells of extant Symphyogyna-type Metzgerialean taxa ultrastructure and phylogenetic implications - Nova Hedwigia 63 471-481

FREY W M HOFMANN amp HH HILGER (2001) The gametophyte-sporophyte junctionunequivocal hints for two evolutionary lines of archegoniate land plants - Flora 196 431-445

FURUKI T amp Z IWATSUKI (1989) Mizutania riccardioides gen et sp nov (Mizutaniaceaefam nov) a unique liverwort from tropical Asia - J Hattori Bot Lab 67 291-196

GARBARY DJ KS RENZAGLIA amp JG DUCKETT (1993) The phylogeny of land plants acladistic analysis based on male gametogenesis - Plant Syst Evol 188 237-269

GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 205-239

GRAHAM LE LW WILCOX ME COOK amp PG GENSEL (2004) Resistent tissues ofmodern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils - PNAS 10111025-11029

HEINRICHS J SR GRADSTEIN R WILSON amp H SCHNEIDER (2005) Towards a naturalclassification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL - CryptogamieBryol 26 131-150

77

HE-NYGREacuteN X I AHONEN A JUSLEN D GLENNY amp S PIIPPO (2004) Phylogeny ofliverworts - beyond a leaf and a thallus - In GOFFINET B V HOLLOWELL amp R MAGILL(eds) Molecular systematics of bryophytes - Monogr Syst Bot Missouri Bot Gard 98 87-118

INOUE H (1976) Illustrations of Japanese Hepaticae - 2 - Tsukiji Shokan Publishing Tokyo 193pp

KRASSILOV VA amp RM SCHUSTER (1984) Paleozoic and Mesozoic fossils - In SCHUSTERRM (ed) New manual of Bryology 2 1172-1193 Hattori Nichinan

LIGRONE R JG DUCKETT amp KS RENZAGLIA (1993) The gametophyte-sporophyte junctionin land plants - Adv Bot Res 19 231-317

MEIszligNER K J-P FRAHM M STECH amp W FREY (1998) Molecular divergence patterns andinfrageneric relationship of Monoclea (Monocleales Hepaticae) Studies in austral temperate rainforest bryophytes 1 - Nova Hedwigia 67 289-302

OOSTENDORP C (1987) The Bryophytes of the Palaeozoic and the Mesozoic - Bryoph Bibl34 1-112 39 pl

PASS JM amp KS RENZAGLIA (1995) Comparative microanatomy of the locomotory apparatusof Conocephalum conicum (Hepaticae Conocephalaceae) - Fragm Flor Geobot 40 365-377

PFEIFFER T F SCHAUMANN GG HAumlSSEL DE MENEacuteNDEZ amp W FREY (2004) Inter-and infraspecific relationships in the Gondwanan liverwort genus Hymenophyton Dumort(Hymenophytaceae Hepaticophytina) Studies in austral temperate rain forest bryophytes 23 -Austral Syst Bot 17 407-421

SCHAUMANN F W FREY T PFEIFFER amp M STECH (2005) Molecular circumscriptionintrafamilial relationships and biogeography of the Gondwanan liverwort family PallaviciniaceaeStudies in austral temperate rain forest bryophytes 27 - Plant Syst Evol 252 27-48

SCHLJAKOV RN (1972) On the higher taxa of liverworts (Hepaticae sstr) - Bot Zhurn 57496-508

SCHUSTER RM (1963) Studies on Antipodal Hepaticae I Annotated key to the genera ofantipodal Hepaticae with special reference to New Zealand and Australia - J Hattori BotLab 26185-309

SCHUSTER RM (1964) Studies on Antipodal Hepaticae IV Metzgeriales - J Hattori BotLab27 183-216

SCHUSTER RM (1982) Studies on Hepaticae LIX On Sandeothallus Schust gen n and theclassification of the Metzgeriales - Nova Hedwigia 36 1-16

SCHUSTER RM (1984a) Evolution phylogeny and classification of the Hepaticae ndash InSCHUSTER RM (ed) New manual of Bryology 2 892-1070 Hattori Nichinan

SCHUSTER RM (1984b) Diagnoses of new taxa of Hepaticae - Phytologia 56 65-74

SHAW J amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - Amer JBot 91 1557-1581

STECH M amp W FREY (2001) CpDNA-relationship and classification of the liverworts(Hepaticophytina Bryophyta) - Nova Hedwigia 72 45-58

STECH M amp W FREY (2004) Molecular circumscription and relationships of selected Gondwananspecies of Haplomitrium (Calobryales Haplomtriopsida Hepaticophytina) - Nova Hedwigia 7857-70

STECH M J-P FRAHM HH HILGER amp W FREY (2000) Molecular relationship of TreubiaGoebel (Treubiaceae Treubiopsida) and high taxonomic level classification of the Hepaticophytina- Nova Hedwigia 71 195-208

78

THIERS B (1993) A monograph of Pleurozia (Hepaticae Pleuroziaceae) - Bryologist 96 517-554

WHEELER JA (2000) Molecular phylogenetic reconstructions of the marchantioid liverwortradiation - Bryologist 103 314-333

Received 15 March 2005 accepted in revised form 2 May 2005