Nova Hedwigia 81 1—2 55—78 Stuttgart, August 2005

A morpho-molecular classification of the liverworts

(Hepaticophytina, Bryophyta)
by

Wolfgang Frey and Michael Stech

Institut für Biologie - Systematische Botanik und Pflanzengeographie,
Freie Universität Berlin, Altensteinstr. 6, D-14195 Berlin, Germany

With 1 table and 1 figure

Frey, W. & M. Stech (2005): A morpho-molecular classification of the liverworts (Hepaticophytina,

Bryophyta). - Nova Hedwigia 81: 55-78.
Abstract: Recent molecular analyses and a re-evaluation of morphological and ultrastructural
characters provided new insights into relationships among liverworts (Hepaticophytina, Bryophyta),
and mosses. Considering these results, a new suprageneric classification of liverworts is proposed.
The liverwort classes are grouped into four superclasses. According to the paraphyly of simple
thalloid liverworts, new classes, Pallaviciniopsida and Pelliopsida, are established for taxa formerly
included in the Jungermanniopsida, which in the narrower circumscription comprise only the leafy
liverworts (separated into Jungermanniidae with two new superorders, Jungermannianae and
Porellanae, and Pleuroziidae subclass. nov.) and the Metzgeriidae s.str. (Aneurales ord. nov. and
Metzgeriales). Pallaviciniopsida comprise two monotypic orders, Pallaviciniales and Hymenophytales,
whereas Pelliopsida comprise a single order, Pelliales. Fossombroniopsida are treated here including
Fossombroniaceae, Petalophyllaceae, Allisoniaceae, and Sandeothallaceae. Taxa of ambiguous position
within superclass III according to morphological and molecular data include Makinoaceae,
Noterocladaceae, and Phyllothalliaceae. The present classification on high taxonomic level reflects
the early-divergent evolutionary history of the long-separated major liverwort groups. Selected
morphological-anatomical and ultrastructural characteristics of the higher taxa are provided along
with summaries of fossil records and recent molecular data.
Key words: Hepaticophytina, suprageneric classification, molecular data, superclasses,
Pallaviciniopsida class. nov., Pelliopsida class. nov., Pleuroziidae subclass. nov.

Introduction

Liverworts (Hepaticophytina) comprise an estimated number of c. 6000 species in c.

370 genera. They are a highly diverse plant group with substantial morphological
heterogeneity including ‘complex thallose’, ‘simple thallose’, and ‘leafy’ liverworts.

DOI: 10.1127/0029-5035/2005/0081-0055 0029-5035/05/0081-0055 $ 6.00

© 2005 J. Cramer in der Gebrüder Borntraeger
Verlagsbuchhandlung, D-14129 Berlin · D-70176 Stuttgart
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Few enigmatic taxa with different kinds of leaf-like lobes or lobules (Blasia,
Fossombronia, Haplomitrium, Noteroclada, Phyllothallia, Pleurozia, Sphaerocarpos,
and Treubia) are transitional between the thallose and leafy condition, and probably
represent relics of the early liverwort diversification. Liverworts are widely distributed
on earth, from the arctic to the subantarctic region, with high cover values mainly in
tropical cloud forests and temperate rain forests, but also in desert crusts, and occur
on a wide range of substrates.
Except for some controversial analyses based on 18S rDNA sequences (e.g., Bopp &
Capesius 1998), all molecular analyses resolved the Hepaticophytina as monophyletic,
in accordance with synapomorphic characters such as common archegonial and
antheridial ontogeny without apical cells, unequal division of the archespore cell
into 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 (complex
thallose liverworts) and Jungermanniopsida (simple thallose and leafy liverworts)
and the early separation of Haplomitrium into Haplomitriopsida Stotler & Stotl.-
Crand., three classes were erected based on molecular phylogenies and ultrastructural
analyses of the gametophyte-sporophyte junction: Blasiopsida (Stech & Frey 2001),
Fossombroniopsida (Frey et al. 2001), and Treubiopsida (Stech et al. 2000).
Furthermore, molecular data now confirm the parallel evolution of different thallose
growth forms within the Hepaticophytina. The complex thallose form is restricted
to the monophyletic Marchantiopsida, whereas the thallose or semileafy Metzgeriidae
s.l. (Jungermanniales anacrogynae) are resolved as paraphyletic (e.g., Davis 2004,
He-Nygrén et al. 2004, Stech & Frey 2004, Forrest & Crandall-Stotler 2004, 2005,
Heinrichs et al. 2005). The true simple thallose forms (e.g., Metzgeria, Riccardia),
the semileafy Fossombronialean liverworts and the thallose forms with a central
strand (Pallaviciniaceae, Hymenophytaceae) obviously represent different
evolutionary lineages, which should be assigned to different classes. Consequently,
relationships within the Jungermanniopsida are subject to major change according to
the results of molecular analyses.
In the present study, we propose a new suprageneric taxonomy of the Hepaticophytina.
The 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 & Buck
(2004), and
(ii) to recircumscribe the Jungermanniopsida according to recent molecular analyses.
An overview of distinctive morphological and anatomical characters compiled from
the literature, blepharoplast ultrastructure (after Carothers & Rushing 1988, Pass &
Renzaglia 1995, and others), type of the gametophyte-sporophyte junction (after
Ligrone et al. 1993, Frey et al. 2001, Carafa et al. 2003; cf. Table 1), fossil records
(after Krassilov & Schuster 1984, Oostendorp 1987) and geographical distribution
is provided for the respective taxa. A summary of evolutionary relationships of the
major liverwort groups with particular reference to gametophyte-sporophyte junction
types and the main fossil records is shown in Fig. 1.

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

Class Subclass Order / Family Transfer cells (layers) Foot shape

Gametophyte Sporophyte

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

Superclass I
Treubiopsida Treubiaceae – +(1-2) bulbous
+(3-4) +(2-3) bulbous
Haplomitriopsida Haplomitriaceae +(2-3) +(1-2) bulbous

Superclass II
Blasiopsida Blasiaceae +(2-3) +(1) conical
Marchantiopsida Sphaerocarpidae Sphaerocarpales +(2–3) +(1) spheroidal
Marchantiidae Monocleales +(4-6) +(2) conical
Marchantiales +(2-4) +(1) spheroidal

+(1-2) conical,
bulbous,
cylindrical,
cup-shaped
Ricciales – – –
Superclass III
Fossombroniopsida Fossombroniaceae +(2-3) +(1) bulbous

Reduction of gametophyte and mostly also sporophyte transfer cells (wall ingrowths)
Pallaviciniopsida Pallaviciniaceae – +(1) conical
Hymenophytaceae – – conical
Pelliopsida Pelliaceae – – conical

Superclass IV
Jungermanniopsida Jungermanniidae div. families – +(1) conical, bul-
– +(1-2) bous,
spheroidal
Metzgeriidae Aneuraceae – – conical
(Riccardia) ?+(2) – conical
Metzgeriaceae – – conical

Systematic arrangement of taxa

Superclass I

1. Class Treubiopsida Stech, J.-P.Frahm, Hilger & W.Frey

Order Treubiales Schljakov
Fam. Treubiaceae Verd.
Characterized by the unique “leafy” growth form with 2 lateral rows of alternate,
succubous lobes (interpreted as leafy appendages) and transversely oriented dorsal
lobules (scales), dimorphic leaf cells (scattered cells containing 1 large oil-body,

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Fig. 1. Phylogenetic relationships of the higher taxa of Hepaticophytina, indicating the approximate
time of divergence of the groups in line with assignable fossil records and distribution of characteristic
gametophyte-sporophyte junction types: 1 With several layers of transfer cells on both side of the
placenta. 2 Sporophyte transfer cells (stc): wall ingrowths relatively thin and highly branched. 3 Stc:
wall ingrowths highly branched and anastomosing, of high structural complexity; wall ingrowths in
gametophyte transfer cells (gtc) partly short and coarse. 4 Gametophyte placental cells without wall
ingrowths. 5 Partly sporophyte placental cells without wall ingrowths. 6 Sporophyte and gametophyte
placental cells without wall ingrowths. Abbreviations: g gametophyte, ju gametophyte-sporophyte
junction with placenta, s sporophyte; B.lob. Blasiites lobatus, G.spp. Gessella spp., G.sal.
Grisellatheca salopensis, H.lan. Hepaticites langii, J.gra. Jungermanniites gracilis, J.keu. J.
keuperianus, L.pap. Laticaulina papillosa, M.cya. Marchantites cyathodoides, M.met.
Metzgeriothallus metzgerioides, M.plu. Muscites plumatus, N.lan. Naiadita lanceolata, P.dev.
Pallaviciniites devonicus, T.kid. Treubiites kidstonii.

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other cells only with chloroplasts), and slime papillae on ventral surface, producing
a thick covering of mucilage (otherwise only in Verdoorniaceae). Blepharoplast of
Calobryalean affinity: lamellar strip (spline) with up to 104 microtubules (widest in
bryophytes), open spline aperture, overlap between anterior and posterior basal bodies.
Gametophyte-sporophyte junction either resembling that of Jungermanniopsida
(Apotreubia: gametophyte placental cells lacking wall ingrowths) or similar to
Fossombronia and Haplomitrium (Treubia: several layers of transfer cells on both
side of the placenta with thin wall ingrowths). No fossil records known. - 2 genera
(11 species), distribution pattern originally Pangaean. - Treubia K.I.Goebel (7),
basically Gondwanan; Malesia, Australasia, Oceania (S Pacific), rather recent
transgression of Wallace’s line, 1 species in Chile; not represented in Africa. -
Apotreubia S.Hatt. & Mizut. (4), predominantly Laurasian.
Based on morphological characters the two extant genera Treubia and Apotreubia
may be regarded as the most archaic living fossils in liverworts and extant models of
an extinct plant group. In molecular trees Treubiopsida are resolved as sister to all
other liverworts, either alone (e.g., Stech & Frey 2001) or together with Haplomitrium
(e.g., Forrest & Crandall-Stotler 2005), similar to cladistic analyses based on male
gametogenesis characters (Garbary et al. 1993). Heinrichs et al. (2005) recently
included Treubiopsida in the Haplomitriopsida, however, with respect to the
morphological and anatomical differences and the fact that at least some of the
shared characters states (e.g., tetrahedral apical cells or the type of the gametophyte-
sporophyte junction) are probably ancestral plesiomorphies, we prefer to maintain
two classes united in a single superclass.

2. Class Haplomitriopsida Stotler & Stotl.-Crand.

Order Haplomitriales H.Buch ex Schljakov
Fam. Haplomitriaceae D•de…ek
Unique features: upright habit, subterranean creeping axis (“rhizome”), undivided
leafy appendages, “isophyllous” with transversely inserted “leaves” (some species
tend toward “anisophylly” and succubous insertion), rhizoids lacking, central strand
present, water-conducting cells resembling that of Takakia, scattered gametangia in
diffuse groups laterally along the stem without specialized protective bracts, massive
seta and an extensive stem-calyptra. Blepharoplast structure: spline with up to 90
microtubules, spline aperture on the left side. Gametophyte-sporophyte junction: 1-
2 sporophyte and 2-3 gametophyte placental cell layers; gametophyte transfer cells
with highly branched and thin, long wall ingrowths, similar to Treubia and
Fossombronia; foot bulbous, collar absent. Fossil records: Gessella Poulsen (2) from
Lower Permian, Denmark. Naiadita lanceolata P.B.Brodie from Upper Triassic of
England is discussed to belong to either Haplomitriopsida or Marchantiopsida subclass
Sphaerocarpidae. - Monotypic. - Haplomitrium Nees (9), basically Gondwanan, center
of diversity in Australasia.
Haplomitrium is morphologically and anatomically isolated by a “serious of
fundamental criteria” (Schuster 1984a) and regarded as an early-diverging lineage
within liverworts. The precise placement of Haplomitrium in molecular trees has

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been problematic and varies depending on taxon sampling, especially the inclusion
vs. exclusion of Treubia, and the applied method (summarized by Shaw & Renzaglia
2004). Cladistic analyses of male gametogenesis characters (Garbary et al. 1993)
and recent molecular analyses including Treubia (e.g., Forrest & Crandall-Stotler
2005) revealed that Haplomitrium plus Treubia form a clade sister to all other
liverworts groups.

Superclass II

1. Class Blasiopsida Stech & W.Frey

Order Blasiales (R.M.Schust.) Stotler & Stotl.-Crand.
Fam. Blasiaceae H.Klinggr.
Thallus with ill-defined midrib grading into unistratose wings (leafy habit), in
colonies. Central strand lacking. 2 rows of flattened multicellular scales (as in
complex thallose liverworts), irregularly dentate, on ventral surface of thallus.
Small ventral hemispherical ‘auricles’ filled with Nostoc colonies and unique,
flasked-shaped gemma-receptacles present (unique in liverworts). Marchantialean
blepharoplast type. Gametophyte-sporophyte junction: 1 sporophyte and 2-3
gametophyte placental cell layers with Marchantialean-type wall ingrowths (transfer
cells). Fossil records: The Late Carboniferous Blasiites lobatus (J.Walton)
R.M.Schust., resembling Blasia pusilla, is supposed to be an ancestor of the extant
taxa (however, see Pelliopsida). The Carboniferous Treubiites kidstonii (J.Walton)
R.M.Schust. with lateral succubously shingled leaves and ventral scales (as in Blasia)
is rejected as a presumable precursor of Treubiopsida, but serves as a model from
which the more frondose, semithallose extant Blasia may be derived. - 2 monotypic
genera. - Blasia L., circumboreal. - Cavicularia Steph., endemic Japan.
Blasia was traditionally included in the Metzgerialean group, but blepharoplast
ultrastructure and a Marchantialean-type gametophyte-sporophyte junction assign
it to the Marchantiopsida. Similarly, latest molecular results resolve Blasia and
Cavicularia as sister to the Marchantiopsida (Forrest & Crandall-Stotler 2005)
with maximum bootstrap support, whereas earlier molecular analyses of Blasia
either suggested a somewhat intermediate position between Marchantiopsida and
Jungermanniopsida (Wheeler 2000, Stech & Frey 2001), or a basal position within
liverworts (He-Nygrén et al. 2004). The molecular separation of Blasia and
Cavicularia in Forrest & Crandall-Stotler (2004) and Heinrichs et al. (2005)
was caused by contaminated Cavicularia DNA (cf. Forrest & Crandall-Stotler
2005).

2. Class Marchantiopsida Stotler & Stotl.-Crand.

Thirty-two genera with c. 350 species. Highest differentiated gametophytes in the
plant kingdom. Blepharoplast structure uniform, closed apertures, three spline
microtubules wide. Gametophyte-sporophyte junction: 1-2 sporophyte and 2-4
gametophyte placental cell layers; cells of both layers with characteristic wall
ingrowths (highly branched and anastomosing or short and coarse, respectively;

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Marchantialean type). Fossil records: Some enigmatic Lower Devonian microfossils
(epidermal surface tissues, rhizoids) may be regarded as the remains of early
Marchantioid liverworts (Graham et al. 2004). Convincing Marchantioid fossils
obviously unknown from Lower Palaeophytic, starting with the Lower Permian
Marchantites loreus Zalessky (incertae sedis), the unequivocal Middle Triassic
Marchantites cyathodoides (Townrow) H.M.Anderson and M. tennantii H.M.Anderson,
and becoming relatively species rich from Triassic to Eocene. Probably the initial
diversification of the Marchantiopsida took place at the beginning of the relatively
arid Mesophytic, followed by a rapid radiation of Marchantioid taxa coincident
with extreme conditions and ecological reorganisation in Upper Permo-Triassic
time.
Monophyly of the Marchantiopsida is strongly supported by all respective molecular
analyses.

1. Subclass Sphaerocarpidae Stotler & Stotl.-Crand.

Order Sphaerocarpales Cavers
Fam. Sphaerocarpaceae (Dumort.) Heeg
Leafy habit. Marchantialean blepharoplast type and gametophyte-sporophyte junction.
No fossils known. - 2 genera. - Sphaerocarpus Boehm. and the monotypic Geothallus
Campb.

Fam. Riellaceae Engl.

Monotypic. Riella Mont.

2. Subclass Marchantiidae Engl.

1. Order Monocleales R.M.Schust.
Ancient relict group with plesiomorphic characters, e.g., simple thallus and capsule
opening by only one lateral slit. Typical Marchantialean blepharoplast and
gametophyte-sporophyte junction type as well as molecular data (e.g., Meißner et
al. 1998, Wheeler 2000, Forrest & Crandall-Stotler 2005) support the current
classification in the Marchantiidae. No fossils known. - Monotypic. - Monoclea
Hook. (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 see
Crandall-Stotler & Stotler (2000).

3. Order Ricciales Schljakov

2 families, Oxymitraceae Müll.Frib. ex Grolle (Oxymitra Bisch. ex Lindenb.) and
Ricciaceae Reichenb. with 2 genera, Riccia L. and the monotypic Ricciocarpos
Corda.

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Superclass III

Recent molecular analyses based on larger taxon sampling (Davis 2004, He-Nygrén
et al. 2004, Stech & Frey 2004, Forrest & Crandall-Stotler 2004, 2005, Heinrichs et
al. 2005) revealed that the simple thallose liverworts, formerly comprised as
Jungermanniopsida subclass Metzgeriidae (s.l.) with 15 families, 38 genera and c.
500 species, are not monophyletic. These taxa, which form leaf-like lobes or thallus
wings 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 & Crandall-Stotler 2004) comprises different types of
simple thallose or semileafy liverworts, which are here divided into three classes:
Fossombroniopsida, Pallaviciniopsida, and Pelliopsida. The simple thallose
Metzgerialean liverworts (Metzgeriales I sensu Forrest & Crandall-Stotler 2004)
compose the second group that is sister to the leafy liverworts and thus treated as
subclass Metzgeriidae s.str. of the Jungermanniopsida (superclass IV).

1. Class Fossombroniopsida W.Frey & Hilger

Plants thallose. Antheridia in acropetal sequence on upper surface of axis. Oil-bodies
small, numerous. Capsule mostly lacking valves, wall disintegrating into fragments
or 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 surface.
Elaterophore 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. Antheridia
naked. Sporophyte protected by a caulocalyx. Capsule wall without wall thickenings.
Gametophyte-sporophyte junction: 1 sporophyte and 2-3 gametophyte placental transfer
cell layers; cells with thin wall ingrowths, strongly reminescent of the placenta in
Treubia and Haplomitrium; gametophyte placenta transfer cells with strongly branched
wall ingrowths (resembling those of Blasia and Marchantiopsida); a bulbous foot and
absence of a collar support exclusion of Fossombronia from the Jungermanniopsida. -
2 genera (c. 92), worldwide distribution. - Austrofossombronia R.M.Schust. (2),
subantarctic, Andes (Peru-Venezuela). - Fossombronia Raddi (c. 90), from subarctic to
subantarctic regions, centre of diversification in Australia (33 spp.). The
Fossombroniaceae are strongly supported as monophyletic in molecular analyses, with
Allisonia and Petalophyllum as sister groups (Forrest & Crandall-Stotler 2005). The
taxon is thought to be very isolated, immensely old and relict (Schuster 1984a).

Fam. Petalophyllaceae (R.M.Schust.) Stotler & Stotl.-Crand.

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

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Petalophyllum Nees & Gottsche ex Lehm. (6), New Zealand (2), 1 species each in
W Australia, India, and S USA, P. ralfsii (Wils.) Nees & Gottsche, medit.-atlant., W
Europe, N Africa. - Sewardiella Kashyap (1), W Himalayas.

Fam. Allisoniaceae (R.M.Schust. ex Grolle) Schljakov

Plants thallose. Midrib of thallus ill-defined. Central strand lacking. Dioicous.
Antheridia individually protected by a scale. Capsule spherical, wall irregularly tearing
into 5-7 unequal valves, epidermal cells with irregular bands; without elaterophore.
Spores strongly sculptured. - 2 genera (5). - Allisonia Herzog (1), endemic New
Zealand. - Calycularia Mitt. (4), N and E Asia, Himalayas.
Molecular data indicate that the Allisoniaceae are not monophyletic. Both genera
have similar capsule walls and thallus structures, but differ by the presence of a
well-developed pseudoperianth in Calycularia (e.g., Inoue 1976). The placement of
Calycularia has traditionally been problematic and is still tentative based on its
position sister to the Fossombronialean and Pallavicinialean liverworts in molecular
trees.

Fam. Sandeothallaceae R.M. Schust.

Plants thallose. Thalli simple or rarely branched, with uniseriate slime hairs; occasional
with ventral branches. Rhizoids reddish. Antheridia in axils of dorsal scales along
midrib surface. Seta massive. Capsule wall (3)4-5(6)-layered, opening by 2 lateral
slits; without elaterophore. - Monotypic. - Sandeothallus R.M.Schust. (1), India,
Malesia, Samoa.
The systematic position remains ambiguous. Morphologically, Sandeothallus occupies
an intermediate position: gametophytic characters indicate close relationship to
Allisoniaceae, whereas sporophytically it is close to the Pallaviciniaceae (Schuster
1982). Molecular data are so far not available.

2. Class Pallaviciniopsida W.Frey & Stech, class. nov.

Plantae thallinae, prostratae vel in axem prostratum stipitemque erectum divisae, partim dendroideae.
Costa thalli prominens, 1 vel 2(-4) filis centralibus. Cellulae filorum centralium elongatae, perforatae,
hydroideis similes. Capsulae ovoideae ad cylindricae, 2 vel 4 valvis dehiscentes.
Type family: Pallaviciniaceae Mig.
Plants thallose; prostrate, erect or sometimes dendroid. Dendroid taxa evolved three
times independently, in Jensenia and Symphyogyna (Pallaviciniaceae) as well as in
Hymenophyton (Hymenophytaceae) (Schaumann et al. 2005). Gametophyte mostly
with central strand composed of thick-walled, elongated water-conducting cells with
perforations (pores). This pallavicinoid type of water-conducting cells occurs only
in 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 cylindrical,
tearing into 2, imperfectly 4, or 4 valves, wall bistratose. Gametophyte-sporophyte
junction: gametophyte placental cells without wall ingrowths, sporophyte placental

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cells partly without wall ingrowths. Fossil records: Pallaviciniites devonicus (Hueber)
R.M.Schust. from lowermost Upper Devonian (375 mio. y) is the oldest true bryo-
phyte fossil known. The thallose plant bearing a central strand in the gametophyte
axis is superficially similar to the Pallaviciniaceae, in particular to Pallavicinia and
Symphyogyna. Laticaulina papillosa Krassilov from Late Jurassic of Russia also
shows affinities to the Pallaviciniopsida (Symphyogyna). About 65 species.

1. Order Pallaviciniales (R.M.Schust.) W.Frey & Stech, stat. nov.

Basionym: Pallaviciniineae R.M.Schust., Phytologia 56: 65, 1984.
Type (and only) family: Pallaviciniaceae Mig.

Schuster (1984b) erected the Pallaviciniineae to include Pallaviciniaceae,

Sandeothallaceae, and Makinoaceae. In contrast, we consider the Pallaviciniales
monotypic, at least until relationships of Sandeothallus and Makinoa have been
clarified on the molecular level.

Fam. Pallaviciniaceae Mig.

Plants thallose, prostrate without basal stipe and “rhizome” or erect, arising from
a “rhizome” or stipe; dendroid in Jensenia and some species of Pallavicinia and
Symphyogyna. Thallus with well-defined midrib with 1 or 2(-4) central strands
in most taxa present, and unistratose lamina. Water conducting cells elongated,
with tapering ends and thickened walls (c. 8 µm wide and up to 300 µm long),
throughout with numerous pits, produced by dissolution of secondary wall
material associated with modified plasmodesmata. Only few true plasmodesmata-
derived perforations (pores) present (Ø 200-400 nm). No relationship with
tracheids (Frey et al. 1996). Slime papillae on both dorsal and ventral surfaces
of apex sometimes present. Ventral scales absent or small and uniseriate. Dioicous.
Antheridia on dorsal surface of thallus, often in 2-several ranks, associated with
scales. Archegonia clustered on dorsal surface of midrib (gynoecia), deliminated
by a single (Symphyogyna) or double involucres (except Xenothallus). Developing
sporophyte protected by a tubular pseudoperianth (inner involucre) or by a stem-
calyptra. Seta long, massive. Capsule elongate-cylindrical to ovoid, dehiscence
by 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 outermost
sporophytic placental layer. - 9 genera (c. 60), Gondwanan, centres of diversity
in Australasia and S America.
Molecular analyses resolve Pallaviciniaceae as monophyletic (e.g., Forrest &
Crandall-Stotler 2005, Schaumann et al. 2005). These data support a separation
of Moerckia and Hattorianthus (Moerckioideae) from the remaining taxa, a position
of Podomitrium (Podomitrioideae R.M.Schust.) close to the Symphyogynoideae
(Trevis.) R.M.Schust. ex Grolle, and polyphyly of Pallavicinia and the
Pallavicinioideae. Because of ambiguous relationships between these subfamilies,
we include Podomitrioideae and Symphyogynoideae in Pallavicinioideae s.l.

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Subfam. Moerckioideae R.M.Schust.
Thalli without stipe-like base, laterally branched. Midrib without sharply defined
central strand (Moerckia), although sometimes with a weakly defined pair of strands
consisting of slightly elongated cells with swollen walls but without pits; remnants
of plasmodesmata occasionally visible. Two central strands present in Hattorianthus.
Ventral scales uniseriate, fugacious. Gametangia dorsally on leading thalli. Antheridia
in axils of scales. Pseudoperianth (inner involucre) developes after fertilization. - 2
genera. - Moerckia Gottsche (3-4), Holarctic, N to 82°. - Hattorianthus R.M.Schust.
& Inoue (1), endemic stenotype; E Asia, Japan. Probably an early-diverging branch
originating from a Pangaean ancestor, which evolved separately in the Holarctic. In
contrast to the original circumscription of Moerckioideae by Schuster (1982),
Greeneothallus is excluded, and Hattorianthus included.

Subfam. Pallavicinioideae Mig. ex Grolle

(incl. Symphyogynoideae [Trevis.] R.M.Schust. ex Grolle and Podomitrioideae
R.M.Schust.)
Inner involucre (pseudoperianth) distinct, tubular, hiding the rather thin stem-calyptra
within. Thalli narrowed and typically stipe-like at base or dendroid. Midrib with a
conspicuous single or pair of central strands. Gametangia dorsal on leading thalli,
androecia never spicate, with individual antheridia hidden under distinct scales, clearly
anacrogynous (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, centres
of diversity in Australasia and S America. - Pallavicinia Gray (c. 15), temperate-
tropical, P. lyellii (Hook.) Carruth., supposedly subcosmopolitan. Ancient taxon,
probably of Pangaean origin. - Jensenia Lindb. (8-9), southern temperate, subantarctic
and alpine-tropical, centre of diversity in S America, lacking in Laurasia. - Symphyogyna
Nees & Mont. (c. 25), incl. Symphyogynopsis Grolle. Centre of diversity in the
Neotropics and Australasia, lacking in Laurasia. Probably not monophyletic according
to molecular data (cf. Schaumann et al. 2005). - Podomitrium Mitt. (2), Australasia,
Malesia; endemic stenotypes. Close to Symphyogyna, recognition in a monotypic
subfamily is not supported by molecular data (Schaumann et al. 2005). - Xenothallus
R.M.Schust. (1), New Zealand, endemic stenotype. - Greeneothallus Hässel (1), S
Georgia, endemic stenotype. - Seppeltia Grolle (1), Subantarctic, Macquarie I., New
Zealand (South I.); isolated, endemic stenotype provisionally placed in Pallaviciniaceae.

2. Order Hymenophytales (R.M.Schust.) W.Frey & Stech, stat. nov.

Basionym: Hymenophytineae R.M.Schust., Phytologia 56: 66, 1984.
Type (and only) family: Hymenophytaceae R.M.Schust.

Fam. Hymenophytaceae R.M.Schust.

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

65
mimicking Hymenophyllaceae. Wings unistratose. Well-defined midribs present,
with a central strand and water-conducting cells of pallavicinoid-type. Ventral
scales lacking. Gametangia on morphologically dorsal surface of abbreviated,
highly specialized sexual branches, originating from ventral surface of midrib
at distal sectors of thallus. Androecial branches reduced to small protuberances,
the antheridia each with an individual involucre. Gynoecial branches reduced
to sessile cushions. Involucre double, outer involucre of 2 opposing leaf-like
scales, inner involucre (pseudoperianth) elongated, a cylindrical tube, lobed
and toothed at mouth. Stem-calyptra present. Capsule cylindrical and 4-valved.
Spores unicellular. Elaterophore present. Elaters whip-like, very slender.
Gametophyte-sporophyte junction: Wall ingrowths (transfer cells) absent in
the placental cells of both generations. - Monotypic. - Hymenophyton Dumort.
(3), Gondwanan/palaeoaustral, strictly antipodal (cf. Pfeiffer et al. 2004).
Unique endpoint (Schuster 1984b) in evolution of thallose Pallavicinopsidalean
liverworts.

3. Class Pelliopsida W.Frey & Stech, class. nov.

Plantae thallinae; thalli simplices, sine filis centralibus. Antheridia singulariter cavernulis ad
superficiem thalli dorsalem inserta. Capsulae sphericae, 4 valvis dehiscentes. Elaterophorum basale
adest.
Type family: Pelliaceae H.Klinggr.
Plants thallose, without stipe-like bases and mostly without ventral branches.
Branching pseudodichotomous. Apical cell wedge-shaped or hemidiscoidal. Central
stand lacking. Antheridia sunken individually into chambers on the dorsal surface
along the longitudinal axis and “roofed over” by conoidal projections. Archegonia
in distinct groups on the dorsal thallus surface. Involucre short-tubular or flaplike.
Capsules spherical, with subisodiametric epidermal cells, dehiscing to base into 4
regular valves. Spores multicellular. Elaterophores basal. Fossil records: As no
ventral scales are observed, Blasiites lobatus (J.Walton) R.M.Schust. could perhaps
rather be assigned to Pelliaceae than to Blasiaceae.
Separated from Fossombroniopsida and Pallaviciniopsida by simple thallus
organisation and arrangement of antheridia. Probably a phylogenetically old group
that became adapted to hyperhygric habitat conditions.

Order Pelliales (R.M.Schust.) W.Frey & Stech, stat. nov.

Basionym: Pelliineae R.M.Schust. ex Schljakov
Type (and only) family: Pelliaceae H.Klinggr.

Fam. Pelliaceae H.Klinggr.

Plants fleshy thallose, sparringly, irregularly furcate. Thalli with an obscurely defined
midrib; margins with irregularly shallow lobes. Di- or monoicous. Family restricted
to include only Pellia (concerning the position of Noteroclada, see below). - Pellia
Raddi (5[-6]), Holarctic, cool and temperate regions.

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Families of uncertain positions in superclass III:
Fam. Makinoaceae Nakai
Thalli green, margins pale, crispate. Dioicous. Androecia sunken but aggregated at
the apex of dorsal frond surface. Oil-bodies small, 6-10(15) per cell. Slime papillae
septate, forming slime hairs. Gynoecia posteriorly shielded by a single scale.
Pseudoperianth lacking. Sporophyte protected by a calyptra. Capsule opening by a
lateral slit, elaterophore lacking. Elaters 1-helical and ehelical. - Monotypic. - Makinoa
Miyake (1), E Asia, Philippines, New Guinea.
In molecular analyses Makinoa is either sister to a clade of Fossombronia and
Haplomitrium (He-Nygrén et al. 2004; the position of Haplomitrium is affected by
the absence of Treubia in their analyses) or occupies a basal position among the taxa
of superclass III (Heinrichs et al. 2005). Placement in the Pelliineae, and in particular
a close relationship with Verdoornia, as proposed by Schuster (1964), is clearly
disproved by the molecular data.

Fam. Noterocladaceae (R.M.Schust.) W.Frey & Stech, fam. et stat. nov.

Basionym: Pelliaceae subfam. Noterocladoideae R.M.Schust., J. Hattori Bot. Lab. 70: 145, 1991.
Type (and only) genus: Noteroclada Taylor ex Hook. & Wilson; type species: N. confluens Taylor ex
Hook. & Wilson, London J. Bot. 3: 166, 1844.
Plants leafy, with tetrahedral apical cell. Leaves succubous. Branching at least partly
lateroventral. Central strand lacking. Antheridia scattered in small cavities, cavities
partially elevated above axis. Archegonia in clusters, surrounded by a compressed-
tubular involucre (pseudoperianth). Capsule spherical. Spores large, up to 100 µm in
Ø, multicellular, green; germination endosporous. Seta 2-8(10) cm long, thick.
Monotypic. - Noteroclada Taylor ex Hook. & Wilson (1-2). (?Afro)-Central to
southern S America; probably Gondwanan origin.
Molecular data (e.g., He-Nygrén et al. 2004, Forrest & Crandall-Stotler 2005,
Heinrichs et al. 2005, Schaumann et al. 2005) are ambiguous concerning relationships
of Noteroclada. The polyphyly of Noteroclada in Heinrichs et al. (2005) indicates
that one of the sequenced samples is either misidentified or contaminated. The most
reliable topology supports a position of Noteroclada sister to Pellia (Forrest &
Crandall-Stotler 2005; 70% bootstrap support).

Fam. Phyllothalliaceae E.A.Hodgs.

Plants leafy. Stems consisting of nodes and internodes. Conducting strand absent. Leaves
opposite, polystratose, succubous. Leaf cells very large and thin-walled; trigones absent.
Mucilaginous papillae uniseriate and filamentous at shoot apex and ventral surface of
axis. Ventral appendages or scales absent. Rhizoids colorless. Dioicous. Antheridia and
archegonia clustered on dorsal surface of axis (androecia, gynoecia), associated with
perichaetial or perigonial scales resp. Sporophytes protected by a stem-calyptra. Setae
massive. Capsules tearing into 12-14 valves (Schuster 1984a); epidermal cells with
nodular thickenings. Elaterophores at capsule base. - Monotypic. - Phyllothallia
E.A.Hodgs. (2). New Zealand, Tierra del Fuego, isolated relict taxon.

67
Schljakov (1972) erected the order Phyllothalliales (R.M.Schust.) Schljakov and
placed it, together with Treubiales, Fossombroniales and Metzgeriales, in the
superorder Metzgerianae Schljakov. Molecular data (Forrest & Crandall-Stotler 2005,
Heinrichs et al. 2005) indicate a sistergroup relationship with Pallaviciniopsida,
which, however, are clearly distinct at least gametophytically.

Superclass IV

Class Jungermanniopsida Stotler & Stotl.-Crand.

In the present circumscription, the class Jungermanniopsida comprises leafy liverworts
and the Metzgerialean-type simple thallose liverworts. Molecular data confirm a
common origin of the subclasses Jungermanniidae, Pleuroziidae and Metzgeriidae,
but their relationships remain ambiguous. The ancestral type of these liverworts
probably also had a simple thallose gametophyte growing via a cuneate apical cell
with four cutting faces, and a sporophyte with massive foot and seta. Leafy taxa
with radially symmetrical gametophytes and 3 rows of transversely (or nearly so)
inserted leaves were assumed to be early-diverging groups, from which anisophylly,
oblique inserted leaves and thallose forms derived, as indicated by the loss of transfer
cells in the gametophyte-sporophyte junction.

1. Subclass Jungermanniidae Engler

The Jungermanniidae (leafy liverworts, Jungermanniales acrogynae; excluding
Pleurozia) are the largest group of liverworts with about 5500 species, monosymmetric
and anisophyllous or isophyllous. Few taxa secondarily thallose (e.g., Metzgeriopsis
K.I.Goebel). Gametophytic shoots with tetrahedral apical cell (three cutting faces)
and (usually) well-differentiated stems and leaves. Stems without central strand;
axis usually with outer cortex and inner, more delicate medulla. Leaves without
midrib, basically 2-lobed, arising from 2 initial cells, or 3-several-lobed, or undivided,
most commonly differentiated as 2 rows of lateral leaves and a single row of ventral
underleaves (amphigastria). Insertion of the lateral leaves transverse, or more
commonly, oblique; plants therefore ± flattened with mostly overlapping leaves in
either incubous or succubous orientation. Complex-bilobed lateral leaves folded to
form ventral and dorsal lobes. Dorsal lobe mostly larger than ventral one; the ventral
lobe may be highly modified into a pouch, helmet-shaped lobule or sac. Underleaves
frequently small or lacking. Leaf cells with or without trigones. Oil-bodies usually
present in all chorophyllose cells of the gametophyte. Rhizoids usually present, smooth.
Antheridia restricted to the axils of leaves, sometimes underleaves. Archegonia
formation from apical cell, terminal on main or branch axes (acrogynous). Developing
sporophyte usually protected by a tubular perianth, derived from 2 or 3 modified
fused leaves; of important taxonomic value. Seta long and distinctly elongating the
sporophyte. Capsules spherical to cylindrical, wall 2-10-stratose, regularly dehiscing
by 4 valves. Spores 6-24(-60) µm. Characteristic gametophyte-sporophyte junction:
Prominent wall labyrinths with thin, highly branched wall ingrowths are restricted
to usually one or rarely two layers of the sporophyte side of the placenta; gametophyte
placental walls lack ingrowth; collapsed gametophyte cells mark the placental space.

68
Fossil records: Lack of any evidence of leafy Jungermanniidae in the Palaeophytic,
except probably Jungermaniites keuperianus (De Gasparis) Oostendorp, Upper
Triassic. Jungermannites gracilis (T.Halle) Oostendorp from Middle Jurassic of
Antarctic Peninsula is the earliest member of Jungermanniales, another early member
of Jungermanniidae is Cheirorhiza brittae Krassilov from Late Jurassic. The early
diversification of the Jungermanniidae is assumed to have taken place in
Gondwanaland as the major evolutionary events have been confined to Gondwana.
The main diversification took place in ‘co-evolution’ with the evolution of angiosperms
and the establishment of tropical rain forest ecosystems.
The Jungermanniidae form a clade sister to the Metzgeriidae s.str. in the molecular
analyses of Davis (2004) and Forrest & Crandall-Stotler (2005). Molecular data
support a separation of Jungermanniidae into two main groups (e.g., Davis 2004,
Stech & Frey 2004, Forrest & Crandall-Stotler 2005, Heinrichs et al. 2005), which
are, with exceptions, also distinguishable morphologically and ecologically (cf.
Heinrichs et al. 2005). The first group comprises Porellales (R.M.Schust.) Schljakov,
Radulales (R.M.Schust.) Stotler & Stotl.-Crand., and Lepicoleales Stotler & Stotl.-
Crand. p.p., and the second Jungermanniales H.Klinggr. and also some Lepicoleales
sensu Crandall-Stotler & Stotler (2000). Both groups were comprised as orders
Jungermanniales and Porellales, respectively, by Heinrichs et al. (2005). In congruence
with the high-level classification presented here, however, we prefer to separate the
two main lineages as superorders, which allows for an ordinal reclassification of the
families in future studies. For families see synopsis below as well as Stotler & Crandall-
Stotler (2000) and Heinrichs et al. (2005).

1. Superorder Jungermannianae W.Frey & Stech, superord. nov.

Ramificatio ventralis, insertio foliorum succuba et rhizoidea non fasciculata adsunt. Folia plerumque
2 initiis crescentia. Protonema plerumque exosporum. Plantae praecipue terricolae.
Type family: Jungermanniaceae Reichenb.
Occurrence of ventral branching, succubous leaf orientation and non-fasciculate
rhizoids. Protonema normally developing exosporous. Development of leaves normally
by means of two initial cells. Lack of water-sacs. Frequently terrestrial, if epiphytic,
without clear morphological adaptations to the epiphytic habitat.

2. Superorder Porellanae W.Frey & Stech, superord. nov.

Ramificatio ventralis deest. Folia 3 initiis crescentia, plerumque biloba, lobulus ventralis partim in
sacculum aut vesiculam aquam continentem transformatum. Insertio foliorum incuba vel transversalis.
Rhizoidea fasciculata. Sporae multicellulares, protonema endosporum. Praecipue epiphyta.
Type family: Porellaceae Cavers
Lack of ventral branching. Most taxa with complicate-bilobed leaves, with incubous
or transverse orientation. Rhizoids in bundles (fasciculate). Multicellular spores with
endosporous protonema. Development of leaves by means of three initial cells.
Predominantly epiphytes, development of specialized lobules or water-sacs on the
ventral side of leaves and endosporous protonema probably associated with the
epiphytic habitat.

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2. Subclass Pleuroziidae W.Frey & Stech, subclass. nov.
Plantae foliosae, ab aliis Jungermanniopsidis foliosis cellula apicali lenticulari bifaciali divisae,
merophyta ventralia nulla foliaque disticha. Folia prima elobulata, folia secunda plerumque in lobulum
dorsalem minorem atque in lobum ventralem maiorem divisa. Lobulus dorsalis in sacculum aut
vesiculam aquam continentem transformatum. Gynoecia fertilia steriliaque plerumque adsunt.
Although a latin diagnosis exists for the suborder Pleuroziinae (Schuster 1963), we
provide a modified diagnosis for the subclass that considers later publications (e.g.,
Thiers 1993) and allows a clearer distinction from the Jungermaniidae s.str.

Order Pleuroziales (R.M.Schust.) Schljakov

Fam. Pleuroziaceae (Schiffn.) Müll.Frib.
Plants leafy, usually purplish. Stems ascending. Only leafy liverwort group with an
apical cell with 2 cutting faces (lenticular, as in Metzgeriidae), i.e. stems with no
trace of a ventral merophyte and leaves distichous with clasping bases. Leaves simple,
with the lobule most rudimentary (elobulate), or complicate-bilobed (explanate-
lobuled or saccate-lobuled). Larger leaf lobe ventral, strongly succubously inserted;
smaller lobe (lobule) dorsal, with a complex water sac. Underleaves lacking. Trigones
very large. Structure of the gametophyte-sporophyte junction not known. Androecia
and gynoecia on short lateral-axillary branches, fertile and sterile gynoecia often
present. Gynoecial branches with bi- or trilobed bracts. Perianth elongate. Capsule
spherical to short-ovoid. - Monotypic. - Pleurozia Dumort. (11), primarily epiphytes
in moist, montane tropical forests.
Pleurozia, for a long time regarded as an isolated element of the leafy liverwort
lineage, is resolved by molecular analyses (e.g., Davis 2004, Heinrichs et al. 2005)
as sister to a clade of Metzgerialean liverworts (Metzgeriaceae, Aneuraceae,
Verdoorniaceae). Unique features comprise the 2-sided apical cell, the specialized
water sac and the sterile gynoecia (e.g., Thiers 1993). In contrast to the single leaf
initial in simple thalloid liverworts that have ‘leafy’ gametophytes, leaves of Pleurozia
develop from 2 initial cells, as is typical of true leafy liverworts. The distinction of
Pleurozia on subclass level indicates that the leafy gametophyte of Pleurozia may
have developed independently from the Jungermanniidae as circumscribed here by
convergent evolution.

3. Subclass Metzgeriidae S.E.Barthol.

Jungermanniales anacrogynae p.p., Metzgeriales I sensu Forrest & Crandall-Stotler (2004).
Bartholomew-Began (1990) established the subclass Metzgeriidae for all simple
thalloid liverworts (Jungermanniales anacrogynae). In the present circumscription
the Metzgeriidae comprise only Aneuraceae, Metzgeriaceae, Verdoorniaceae
(supported by molecular data) as well as Mizutaniaceae and Vandiemeniaceae; and
thus at least partly correspond to suborder Metzgeriineae R.M.Schust.
Plants thallose, never with leaf-like appendages. Apical cell lenticular. Gametophytes
lacking 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

70
along midrib, often at thallus margins. Antheridia and archegonia both clustered in
sharply delimited androecia and gynoecia, on special branches, except Verdoornia.
Antheridia short-stalked. Archegonia often few, reduced, with very short to absent
necks. Sporophytes enclosed in fleshy tissue (calyptra or perigynium), other protective
devices (perichaetia, pseudoperianths) lacking. Seta tending to become abbreviated,
often reduced. Capsule 4-valved or opening by a lateral slit, with conspicuous nodular
thickening of epidermal cells. Apical elaterophores present. Elaters 1-helical or ehelical,
relatively short. Spores often < 20 µm. Gametophyte-sporophyte junction: both
gametophyte and sporophyte placental cells lack wall ingrowths in Aneura and
Metzgeria; collapsed cells of gametophytic origin always present in the placental
space; lack of transfer cells in the gametophyte generation is interpreted as a reduction;
nacreous walls occur in both gametophyte and sporophyte placental layers. Fossil
records: Except Hepaticites langii J.Walton superficially resembling Metzgeria or
Aneura, no Metzgerialean-like fossils are known. Gametophytes in the Metzgeriidae
clade s.str. vary from large, fleshy, undifferentiated thalli (like those of Verdoornia
and Aneura) to small, delicate thalli differentiated into midrib and wing, as in
Metzgeria. The Metzgeriidae s.str. probably represent a relatively young evolutionary
lineage of secondarily simple thallose forms.

1. Order Aneurales W.Frey & Stech, ord. nov.

Ordo Metzgeriales similis sed thalli uniformes, sine costa alisque unistratosis; guttae olei plerumque
adsunt. Sporophytum calyptra nuda tutum. Elaterophorum apicale prominens vel rudimentale.
Type family: Aneuraceae H.Klinggr.
Plants thallose. Thalli lacking sharp division into well-defined midrib and unistratose
wings, without leaf-like lobes. Central strand lacking. Sporophyte protected by a
calyptra (most of the calyptra represents a new tissue developed from the tissue
below the archegonium, a small portion derived from the ventral wall of the fertilized
archegonium). Involucres and pseudoperianths absent.

Fam. Aneuraceae H.Klinggr.

Thalli of several cell layers, irregularly branched to regularly 1-3-pinnate, some
taxa dendroid. Slime papillae present at the apex of axes. Specialized marginal rhizoids
lacking. Oil-bodies usually present (in all or some cells) in most taxa. Gametangia
on the dorsal surface of short, highly reduced lateral branches. Antheridia to varying
degrees immersed in cavities, serially arranged and surrounded, either individually
or in groups of 2 or 3(-5), by flask-shaped to tubular outgrowths of the thallus.
Calyptra fleshy, massive. Capsule ovoid to cylindrical, outer layer with nodular
thickenings on the radial walls, dehiscing into 4 valves. Elaters 1-helical.
Elaterophores 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. 웧 plants smaller than 웨.
Spores 19-26 µm. Taxonomy of Aneura has not been studied critically on a worldwide
basis; the distribution of the species remains incompletely known. - Lobatiriccardia
(Mizut. & S.Hatt.) Furuki (4), Malesia, Australasia, Japan. Thalli large, 1-10 cm
long, translucent, bluish green when fresh, segments usually 3-6(7) mm wide; densely

71
pinnate to bipinnate, branching only lateral. Epidermal thallus cells with (3-5)6-12
relatively large oil-bodies, of different size. Dioicous. Spores 12-19 µm. Molecular
data suggest a sister relationship between Aneura and Lobatiriccardia. - Cryptothallus
Malmb. (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 cool
regions of former Gondwanaland, e.g., 50% of Australasian taxa endemic. Thalli
delicate, considerably varying in habit, 1-10 cm long, 1-3-pinnately branched, some
taxa with erect, dendroid growth, composed of multiple layers of cells in cross-
section, without midrib. Epidermal cells smaller than inner cells of thalli. Cells each
with 1-3(5-8) large oil-bodies; many epidermal cells lacking oil-bodies. Slime papillae
clavate, 1-2-celled. Di-, aut- or synoicous. Androecial branches with 2 rows of
antheridia. Gynoecia on distinct but very short lateral branches. Calyptra green,
fleshy, never scaly or hairy. Elaterophores hardly developed. Spores 9-15(20-25)
µm in Ø. (1)2-celled gemmae endogenously produced by epidermal cells. Intrageneric
relationships imperfectly known.

Fam. Verdoorniaceae Inoue

Large, fleshy und undifferentiated thalli, nearly structureless. Dioicous. Antheridia
individually sunken in alveoli. Oil-bodies very large, 1-3(4) per cell. Slime
papillae 1(2)-celled, clavate, exceedingly large; secreting massive amounts of
mucilage. Archegonia sessile, diffused along the midline of the midrib. Gynoecia
surrounded by laciniiform scales. Involucres and pseudoperianths lacking.
Sporophyte protected by a calyptra. Capsules 4-valved, with weak apical
elaterophore. Elaters 2-helical. - Monotypic stenotype. - Verdoornia R.M.Schust.
(1), endemic New Zealand.
Differs from all other Metzgeriidae s.l. in the stout, short archegonia without
differentiation of a neck and without basal constriction. Supposed to be a relic from
the Palaeozoic, lacking any contact points to other Metzgeriales s.l. However, in
molecular trees (e.g., Stech & Frey 2001, Forrest & Crandall-Stotler 2005) Verdoornia
nests in the Metzgerialean clade.

Fam. Vandiemeniaceae Hewson

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

Fam. Mizutaniaceae Furuki & Z.Iwats.

Thalli ribbon-like, unistratose throughout, resembling a fern prothallium, often
subterraneous with many rhizoids. Oil-bodies present, brownish. Perichaetia distinct,
small, sessile at margins of thallus. Involucres double. Gemmae exogenous, 1-4-

72
celled. Antheridia and sporophytes unknown. - Monotypic. - Mizutania Furuki & Z.
Iwats. (1) Malay. Peninsula, Borneo. One of the simpliest thalli and one of the most
specialized taxa among liverworts in both vegetative and reproductive structures.
So far not included in molecular phylogenies. Although most probably a member of
the Metzgeriidae s.str., the systematic placement in the Aneurales remains uncertain
and is mainly based on the presence of oil-bodies (resembling those of Riccardia)
and the 웨 ‘inflorescence’ resembling those of both Riccardia and Aneura. In contrast,
the marginal rhizoids are similar to the marginal hairs of Metzgeria, and juvenile
thallus development is similar to both Aneuraceae and Metzgeriaceae (Furuki &
Iwatsuki 1989).

2. Order Metzgeriales R.M.Schust. ex Schljakov

Fam. Metzgeriaceae H.Klinggr.
Thalli linear with narrow, well-defined midrib (in cross section with unistratose
cortex and inner medullar cells) and unistratose wings. Central strand lacking. Apical
cell lenticular, with 2 cutting faces. Branching primarily terminal dichotomous,
sometimes ventral-intercalary from ventral side of the midrib. Apices protected by
ephemeral 1-celled, clavate slime papillae arising in 2 ranks, alternately on either
side of the midrib. Unicellular, setose hairs often present on thallus margins (paired
or single) and on ventral surface of midrib, occasionally on ventral surface of the
wings. Oil-bodies lacking or very small (structureless oil-droplets). Dioicous or
autoicous. Gametangia formed on short, highly abbreviated, specialized branches,
arising from the ventral side of the midrib. 웧 branches with midrib, lacking hairs
(ventral surface in Apometzgeria). 웨 branches lacking midrib, hairy. Sporophyte
protected by an elongate, hairy, fleshy (“stem”-)calyptra. Pseudoperianth lacking.
Seta short. Capsule short-ovoid to subglobose, 4-valved to base, with an apical
elaterophore; wall bistratose. Elaters 1-helical or ehelical, attached in bundles at the
valve apex. - 4 genera (c. 140), cosmopolitan, continental areas are devoid of
Metzgeriaceae. - Apometzgeria Kuwah. (2), N Hemisphere, southern S America.
Thallus densely hairy on both surfaces. - Metzgeria Raddi (c. 135), principally tropical
and S temperate, subcosmopolitan. Thalli with hairs confined to margins, ventral
surface of midrib, and sometimes ventral side of wings; never copiously hairy on
dorsal 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, lobe
margins saccate (water-sacs). (“Stem”-)calyptra covered by flat, longitudinally
oriented, multicellular, dentate scales. - Steereella Kuwah. (2), Jamaica, Dominican
Rep., Cuba. Marginal cells of thallus elongated, thick-walled (as in mosses). Elaters
ehelical.
Close relationship with Hymenophytaceae, as postulated earlier, is not confirmed by
molecular analyses (e.g., Forrest & Crandall-Stotler 2005, Schaumann et al. 2005).
It is thus assumed that both Hymenophytaceae and Metzgeriaceae represent endpoints
in parallel evolutionary lineages.

73
 Synopsis of the suprageneric classification of Hepaticophytina

Superclass I
Class Treubiopsida Stech, J.-P.Frahm, Hilger & W.Frey
Order Treubiales Schljakov
Treubiaceae Verd.
Class Haplomitriopsida Stotler & Stotl.-Crand.
Order Haplomitriales H.Buch ex Schljakov
Haplomitriaceae Dědeček
Superclass II
Class Blasiopsida Stech & W.Frey
Order Blasiales (R.M.Schust.) Stotler & Stotl.-Crand.
Blasiaceae H.Klinggr.
Class Marchantiopsida Stotler & Stotl.-Crand.
Subclass Sphaerocarpidae Stotler & Stotl.-Crand.
Order Sphaerocarpales Cavers
Sphaerocarpaceae (Dumort.) Heeg, Riellaceae Engl.
Subclass Marchantiidae Engl.
Order Monocleales R.M.Schust.
Monocleaceae (Nees) A.B.Frank
Order Marchantiales Limpr. in Cohn
Aytoniaceae Cavers, Cleveaceae Cavers, Conocephalaceae
Müll.Frib. ex Grolle, Corsiniaceae Engl., Cyathodiaceae
(Grolle) Stotler & Stotl.-Crand., Exormothecaceae Müll.Frib.
ex Grolle, Lunulariaceae H.Klinggr., Marchantiaceae (Bisch.)
Lindl., Monocarpaceae D.J.Carr ex Schelpe, Monosoleniaceae
Inoue, Targioniaceae Dumort., Wiesnerellaceae Inoue
Order Ricciales Schljakov
Oxymitraceae Müll.Frib. ex Grolle, Ricciaceae Reichenb.
Superclass III
Class Fossombroniopsida W.Frey & Hilger
Order Fossombroniales Schljakov
Fossombroniaceae Hazsl., Petalophyllaceae (R.M.Schust.)

74
 Stotler & Stotl.-Crand., Allisoniaceae (R.M.Schust. ex Grolle)
Schljakov, Sandeothallaceae R.M.Schust.
Class Pallaviciniopsida W.Frey & Stech, class. nov.
Order Pallaviciniales (R.M.Schust.) W.Frey & Stech, stat. nov.
Pallaviciniaceae Mig.
Order Hymenophytales (R.M.Schust.) W.Frey & Stech, stat. nov.
Hymenophytaceae R.M.Schust.
Class Pelliopsida W.Frey & Stech, class. nov.
Order Pelliales (R.M.Schust.) W.Frey & Stech, stat. nov.
Pelliaceae H.Klinggr.
Families of uncertain positions in superclass III:
Makinoaceae Nakai, Noterocladaceae (R.M.Schust.) W.Frey
& Stech, fam. et stat. nov., Phyllothalliaceae E.A.Hodgs.
Superclass IV
Class Jungermanniopsida Stotler & Stotl.-Crand.
Subclass Jungermanniidae Engler
Superorder Jungermannianae W.Frey & Stech, superord. nov.
Families see Stotler & Crandall-Stotler (2000) and Heinrichs et
al. (2005).
Superorder Porellanae W.Frey & Stech, superord. nov.
Goebeliellaceae Verd., Jubulaceae H.Klinggr.,
Jubulopsidaceae (Hamlin) R.M.Schust., Lejeuneaceae Casares-
Gil, Lepidolaenaceae Nakai, Neotrichocoleaceae Inoue,
Porellaceae Cavers, Ptilidiaceae H.Klinggr., Radulaceae
(Dumort.) Müll.Frib.
Subclass Pleuroziidae W.Frey & Stech, subclass. nov.
Order Pleuroziales (R.M.Schust.) Schljakov
Pleuroziaceae (Schiffn.) Müll.Frib.
Subclass Metzgeriidae S.E.Barthol.
Order Aneurales W.Frey & Stech, ord. nov.
Aneuraceae H.Klinggr., Mizutaniaceae Furuki & Z.Iwats.,
Vandiemeniaceae Hewson, Verdoorniaceae Inoue
Order Metzgeriales R.M.Schust. ex Schljakov
Metzgeriaceae H.Klinggr.

75
 Acknowledgements

Sincere thanks are due to H. Lünser for preparing Fig. 1.

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Received 15 March 2005, accepted in revised form 2 May 2005.

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