Bryophytes (Liverworts)

Elizabeth A Brown, Royal Botanic Gardens Sydney, New South Wales, Australia
The liverworts are a group of green land plants that diverged before the dominant land plants such as angiosperms and gymnosperms. Together with mosses and hornworts, liverworts differ from all other land plants in having a free living gametophyte (a plant with only one set of chromosomes) as the dominant generation.

Introductory article
Article Contents
. Introduction . Families Included . Economically Important Species . Morphology . Ecology . Phylogeny

Introduction
The liverworts are a group of green land plants that supercially share a number of features with mosses, e.g. a life cycle with a dominant gametophyte generation, an apparently simple sporophyte (attached and substantially dependent on the gametophyte), a dependence on water for fertilization, small size, no secondary growth and rudimentary or no conductive tissues. Liverworts are found in most terrestrial and freshwater habitats, even quite extreme environments such as Antarctica. There are approximately 50008000 species in 300350 genera and they are representatives of a group that were among the rst to colonize land some 400 plus million years ago. Although apparently simple, liverworts exhibit a range of morphologies and life strategies that allow them to successfully colonize and reproduce in a landscape dominated by the owering plants.

. Fossil History

signicant including Lejeuneaceae, Jubulaceae, Lepidoziaceae, Geocalycaceae, Schistochilaceae, Plagiochilaceae, Radulaceae, Jungermanniaceae s.l.). The Metzgeriales has about 30 genera and 13 families (Fossombroniaceae, Pelliaceae, Allisoniaceae, Phyllothalliaceae, Pallaviciniaceae, Sandeothallaceae, Makinoaceae, Blasiaceae, Aneuraceae, Vandiemeniaceae, Metzgeriaceae, Hymenophytaceae, Treubiaceae). The Treubiaceae is sometimes placed in an order of its own. The Calobryales (Haplomitriales) is a small group of c.10 species variously assigned to 13 genera (Haplomitrium, Calobryum, Steeriomitrium) in one family.

Economically Important Species

Bryophytes have an important role in the nitrogen, carbon and water cycles in many environments. From a human perspective, taxa such as Marchantia have been used medicinally in China, India and Europe. Other taxa such as Riccia have been used in the Himalayas and in Chinese herbal medicines. Liverworts have also been investigated chemically and have potential uses as pesticides and antibiotics against bacteria and fungi. Species of Frullania have been implicated in causing contact dermatitis in forestry workers.

Families Included
The ranking and circumscription of some genera and higher level groupings vary in the classication systems currently available. The Hepaticae (liverworts) are typically separated into two groups, the Jungermanniidae/ Jungermannopsida and the Marchantiidae/Marchantopsida (Table 1). The marchantioid group contains two orders, the Sphaerocarpales with two families (the Riellaceae and Sphaerocarpaceae with approximately 14 species in three genera) and the Marchantiales with about 250 species in 30 genera and 13 families (Cleveaceae, Aytoniaceae, Lunulariaceae, Conocephalaceae, Exormothecaceae, Marchantiaceae, Monoseleniaceae, Targioniaceae, Cyathodiaceae, Carrpaceae, Corsiniaceae, Oxymitraceae, Ricciaceae). The Monocleales, a small group containing one genus with two species, is variously placed in the marchantioid or jungermannioid lines on morphological evidence. Recent molecular work supports placement in the marchantioid group. The jungermannioids consist of three or four orders. About 85% of all liverworts belong to the Jungermanniales, which has some 200 genera and 40 families (the most

Morphology
The liverworts have a life cycle similar to that of mosses and hornworts. The haploid gametophyte generation is the dominant free-living generation. The fundamental organization of the Hepaticae is fairly simple. There is an axis (sometimes attened into a thallus) growing from a single apical cell, with unicellular rhizoids, slime papillae (clubshaped cells that are sometimes elaborated) and male and female gametangia (which are usually restricted to particular zones). The spore germinates and produces a short-lived protonema that gives rise to a single gametophyte.
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Bryophytes (Liverworts)

Table 1 Classication of the liverworts phylum Marchantiophyta (Hepatophyta/Hepaticae) Class Marchantiopsida Order Marchantiales Family Cleveaceae [Sauteriaceae] Genera Athalamia, Sauteria, Peltolepis Family Aytoniaceae [Rebouliaceae] Genera Reboulia, Mannia, Plagiochasma, Asterella, Cryptomitrium Family Lunulariaceae Genus Lunularia Family Conocephalaceae Genera Conocephalum, Wiesnerella Family Exormothecaceae Genera Exormotheca, ?Stephensoniella Family Marchantiaceae Genera Bucegia, Neohodgsonia, Marchantia, Preissia, Dumortiera, Marchantiopsis Family Monoseleniaceae Genus Monoselenium Family Targioniaceae Genus Targionia Family Cyathodiaceae Genus Cyathodium Family Carrpaceae [Monocarpaceae] Genus Carrpos [Monocarpus] Family Corsiniaceae Genera Cronisia, Corsinia Family Oxymitraceae Genus Oxymitra Family Ricciaceae Genera Riccia, Ricciocarpus, Pteroriccia Order Sphaerocarpales Family Riellaceae Genus Riella Family Sphaerocarpaceae Genera Sphaercarpos, Geothallus Class Jungermanniopsida a Order Monocleales Family Monocleaceae Genus Monoclea Order Calobryales (Haplomitriales) Family Calobryaceae Genera Calobryum, Haplomitrium, Steeriomitrium Order Metzgeriales Family Fossombroniaceae Genera Fossombronia, Petalophyllum, Sewardiella Family Pelliaceae Genera Pellia, Noteroclada Family Allisoniaceae Genera Allisonia, Calycularia Family Phyllothalliaceae Genera Phyllothallia Family Pallaviciniaceae Genera Pallavicinia, Jensenia, Hattorianthus, Podomitrium, Moerckia, Greeneothallus Family Sandeothallaceae Genera Sandeothallus 2

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Bryophytes (Liverworts)

Table 1 (Continued) Family Makinoaceae Genera Verdoornia, Makinoa Family Blasiaceae Genera Blasia, Cavicularia Family Aneuraceae Genera Aneura, Riccardia, Cryptothallus Family Vandiemeniaceae Genus Vandiemenia Family Metzgeriaceae Genera Metzgeria, Austrometzgeria, Apometzgeria Family Hymenophytaceae Genus Hymenophytum b Family Treubiaceae Genera Treubia, Apotreubia Order Jungermanniales Family Herbertaceae Genera Herbertus, Triandrophyllum Family Trichocoleaceae Genera Temnoma, Isophyllaria, Lophochaete, Pseudolepicolea, Archeophylla, Archeochaete, Herzogiaria, Chaetocolea, Trichocolea, Leiomitra, Eotrichocolea, Blepharostoma Family Grolleaceae Genus Grollea Family Trichotemnomaceae Genus Trichotemnoma Family Antheliaceae Genus Anthelia Family Vetaformaceae Genus Vetaforma Family Lepicoleaceae Genus Lepicolea Family Jungermanniaceae Genera Chandonanthus, Tetralophozia, Lophozia, Gymnocolea, Gymnocoleopsis, Anastrophyllum, Anastrepta, Tritomaria, Andrewsianthus, Stenorrhipis, Roivainenia, Gerhildiella, Sphenolobopsis, Mesoptychia, Jamesoniella, Cryptochila, Anomacaulis, Cuspidatula, Denotarisia, Hattoria, Jungermannia, Liochlaena, Cryptocolea, Phragmatocolea, Cryptocoleopsis, Diplocolea, Lophonardia, Scaphophyllum, Notoscyphus, Gottschelia, Mylia Family Gymnomitriaceae Genera Acrolophozia, Herzogobryum, Marsupella, Gymnomitrion, Prasanthus, Eremonotus, Stephaniella, Poeltia Family Scapaniaceae Genera Douinia, Scapania, Diplophyllum Family Blepharidophyllaceae Genera Blepharidophyllum, Clandarium, Krunodiplophyllum Family Delavayellaceae Genus Delavayella Family Geocalyaceae (c.22 genera) Genera Lophocolea, Heteroscyphus, Chiloscyphus, Leptoscyphus, Clasmatacolea, Geocalyx, Harpanthus, Saccogyna, Saccogynidium, Tetracymbaliella, Anomylia, Conoscyphus, Evansianthus, Hepatostolonophora, Leptophyllopsis, Leptoscyphopsis, Pachyglossa, Pigafettoa, Platycaulis, Accogynidium, Xenocephalozia Family Plagiochilaceae Genera Plagiochila, Xenochila, Syzygiella, Protosyzygiella, Acrochila, Chiastacaulon, Pedinophyllum, Plagiochilidium, Plagiochilon, Rhodoplagiochila Family Acrobolbaceae Genera Acrobolbus, Tylimanthus, Marsupidium, Austrolophozia, Lethocolea, Goebelobryum Family Arnelliaceae Genera Southbya, Arnellia, Gongylanthus

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Bryophytes (Liverworts)

Table 1 (Continued) Family Brevianthaceae Genus Brevianthus Family Chonecoleaceae Genus Chonecolea Family Schistochilaceae Genera Pleurocladopsis, Schistochila, Paraschistochila, Pachyschistochila Family Perssoniellaceae Genus Perssoniella Family Balantiopsidaceae Genera Ruizanthus, Isotachis, Eoisotachis, Neesioscyphus, Balantiopsis, Anisotachis Family Gyrothyraceae Genus Gyrothyra Family Lepidoziaceae Genera Lepidozia, Kurzia, Telaranea, Megalembidium, Psiloclada, Sprucella, ?Arachniopsis, Bazzania, Dendrobazzania, Acromastigum, Mastigopelma, Drucella, Zoopsis, Zoopsidella, Paracromastigum, Pteropsiella, Pseudocephalozia, Odontoseries, ?Hyalolepidozia, Lembidium, Isolembidium, Hygrolembidium, Austrolembidium, Chloranthelia, Neogrollea, Micropterygium, Mytilopsis, Protocephalozia Family Phycolepidoziaceae Genus Phycolepidozia Family Calypogeiaceae Genera Calypogeia, Metacalypogeia Family Cephaloziaceae (c.12 genera) Genera Cephalozia, Nowellia, Cladopodiella, Odontoschisma, Metahygrobiella, Anomoclada, Alobiellopsis, Iwaksukia, Schineria, Trabacellula Family Cephaloziellaceae Genus Cephaloziella Family Jackiellaceae Genus Jackiella Family Adelanthaceae Genera Adelanthus, Calyptrocolea, Wettsteinia Family Ptilidiaceae Genus Ptilidium Family Mastigophoraceae Genus Mastigophora Family Chaetophyllopsidaceae Genera Chaetophyllopsis, Herzogianthus Family Lepidolaenaceae Genera Lepidolaena, Gackstroemia, Lepidogyna Family Jubulopsidaceae Genus Jubulopsis Family Neotrichocoleaceae Genera Neotrichocolea, Trichocoleopsis Family Goebeliellaceae Genus Goebeliella Family Porellaceae Genera Porella, Ascidiota, Macvicaria Family Jubulaceae Genera Jubula, Frullania, Neohattoria, Steerea, Schusterella, Amphijubula Family Lejeuneaceae Genera Bryopteris, Brachiolejeunea, Caudalejeunea, Neurolejeunea, Mastigolejeunea, Lopholejeunea, Acrolejeunea, Schineriolejeunea, Marchesinia, Archilejeunea, Verdoornianthus, Thysananthus, Spruceanthus, Dicranolejeunea, Phaeolejeunea, Odontolejeunea, Stictolejeunea, Symbiezidium, Blepharolejeunea, Acanthocoleus, Tuzibeanthus, Ptychanthus, Ceratolejeunea, Omphalanthus, Leucolejeunea, Aureolejeunea, Amphilejeunea, Cheilolejeunea, Hygrolejeunea, Taxilejeunea, Trachylejeunea, Pycnolejeunea, Lepidolejeunea, Lejeunea, Rectolejeunea, Harpalejeunea, Drepanolejeunea, Leptolejeunea,

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Bryophytes (Liverworts)

Table 1 (Continued) Rhaphidolejeunea, Crossotolejeunea, Pictolejeunea, Echinolejeunea, Cyclolejeunea, Macrolejeunea, Cystolejeunea, Sphaerolejeunea, Cladiantholejeunea, Prionolejeunea, Acantholejeunea, Cyrtolejeunea, Dactylolejeunea, Dactylophorella, Leiolejeunea, Cladolejeunea, Potamolejeunea, Amblyolejeunea, Placolejeunea, Cryptolejeunea, Stenolejeunea, Ophthalmolejeunea, Physantholejeunea, Cardiolejeunea, Cephalantholejeunea, Echinocolea, Otolejeunea, Nipponolejeunea, Tuymaella, Siphonolejeunea, Austrolejeunea, Haplolejeunea, Nephelolejeunea, Calatholejeunea, Diplasiolejeunea, Colura, Aphanotropis, Myriocoleopsis, Cololejeunea, Aphanolejeunea, Myriocolea, Schusterolejeunea, Metzgeriopsis Family Radulaceae Genus Radula Family Pleuroziaceae Genera Pleurozia, Eopleurozia
a b

Monocleales sometimes placed in the Marchantiopsida (see text). Sometimes placed in an order of its own.

The gametophyte in the liverworts is considerably more malleable than in the mosses, and traditionally has been separated into three types, (a) leafy shoots, (b) simple thallus and (c) complex thallus with air chambers, but an array of transitional morphologies also occur. The leafy shoots consist of simple stems with two or three rows of leaves one cell thick. The leaves are arranged in two lateral rows with the third row ventral. All the leaves may be similar but more usually the ventral row (known as underleaves or amphigastria) is smaller, dierent in shape and transversely inserted. The two lateral rows of leaves may also be transversely inserted but most are inserted with a dorsal tilt (succubous) or a ventral tilt (incubous). The simple thallus varies from almost leafy (Fossombronia) to multistratose (many layered) and undierentiated (Aneura) or with a multistratose midrib and unistratose (single layered) wings (Metzgeria). The complex thalloids are internally dierentiated into an upper (photosynthetic) layer of air chambers that open dorsally by an air pore and a lower parenchymatous region. The ventral surface has two or more rows of scales and two types of rhizoids (simple and peg). A vast array of morphologies that elaborate and confuse the underlying basic structure can be found in the leafy liverworts (Figure 1). The lateral leaves may have a dorsal (Balantiopsis) or ventral (Radula) lobe or an inrolling of the leaf margin (Cheilolejeunea). In Schistochila the leaves are keeled and bilobed while in Frullania the ventral lobe is formed into a sac that varies from helmet-shaped to elongate and pointed. The leaves may be unlobed (Adelanthus), bid (Herbertus) to many lobed (Lepidozia). All of these features may be further elaborated by teeth or cilia (ne hair-like structures, e.g. Trichocolea). Oil bodies occur in about 90% of liverwort taxa. These are membrane-bound organelles that are not found elsewhere in the plant kingdom and contain terpenoids. In some liverworts the oil bodies are restricted to scattered oil cells. Oil bodies are of some taxonomic interest but need to be observed in fresh material as they break down within a few hours of collecting. The sex organs are formed on the surface of the plant but may become enclosed in subsequent development. The

archegonia are usually protected by some sort of enclosure that may consist of modied leaves (perianth), structures that occur around individual archegonia (pseudoperianths), stem or receptacle-derived structures (perigynia, coelocaules, marsupia) or a simple upgrowth of the thallus. In many genera of the marchantioids the archegonia are borne on erect specialized branches (archegoniophores). The antheridia are typically globose and stalked. The sterile jacket cells are not dierentiated to form an apical cap (as occurs in moss dehiscence, i.e. they shed by rupturing of the jacket). There are three basic types of antheridial development (Haplomitrium/Calobryalian, jungermannioid and marchantioid). The sporophyte develops within the protection of the variously derived gametophytic tissues that also protect the archegonia (or are developed subsequent to fertilization). It is determinate in growth and is dierentiated into a foot (the Riccia group excepted), a seta (stalk) and a capsule. The cells of the seta are thin-walled parenchyma and at spore maturity typically elongate up to 20 times their original length, freeing the capsule from the protective gametophytic tissue. The capsule has a wall one to several cells thick and in most taxa dehiscence occurs by means of dierentiated sutures (typically forming four valves; in the marchantioid line the walls are one cell thick and dehiscence is usually irregular). Liverworts lack various features found in mosses and/or hornworts, i.e. there is no columella, operculum or stomata (pores for gas exchange). The spores are generally interspersed with elaters long cells with spiral thickenings on the walls. The spiral thickening is hygroscopic and after capsule dehiscence twists the cell as it dries, assisting in the dispersal of the spores.

Ecology
Liverworts are constrained by a series of factors including the requirement of water for fertilization and the dependence of the sporophyte on the gametophyte. Typically
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Bryophytes (Liverworts)

Figure 1 (a) Incubous leaf insertion, dorsal view. (b) Incubous insertion, ventral view showing underleaves with transverse insertion on the stem. (c) Succubous leaf insertion, dorsal view. (d) Radula; plants lack underleaves and lateral leaves have a ventral lobe; club-shaped perianth protects the emerging sporophyte. (e) Lateral leaf of Schistochila showing keel on lower edge of leaf and cilia on margin. (f) Lateral leaf of Frullania with ventral lobule and stylus between lobule and stem. (g) Lateral leaf of Cheilolejeunea with inrolled ventral lobule. (h) Lateral leaf (half illustrated) of Trichocolea showing extensive lobing that occurs in some liverworts. (i) and (j) Lepidozia species showing some of the variation in extent and number of lobes that may occur in liverworts.

liverworts grow in moist sheltered microhabitats where there is less competition from the larger vascular plants. Moist shaded logs, tree bases and stream banks are obvious habitats but there are many more places where they can be found, particularly those that have a special life strategy. Liverworts rarely dominate a habitat, except for short periods in successional or ephemeral communities; e.g. Marchantia berteroana may be the dominant ground cover in early succession after a re. They may, however, form a conspicuous component, most notably in wet habitats such as cloud forest at high elevations. Asexual methods of gametophyte reproduction appear to be extremely important in the development and maintenance of populations in many liverworts. This can occur by a variety of methods such as the decay of older regions of the plant with the younger regions becoming separated, e.g. Riccia, the production of a variety of specialized propagules (gemmae), e.g. the splash cups of Marchantia, marginal budding of the thallus in Metzgeria
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and regeneration from fragments (known in Herbertus but apparently rare in liverworts). Many liverworts are capable of withstanding periods of desiccation or have developed an annual life cycle that allows them to persist as spores or subterranean tubers (Geothallus). Such features result in taxa such as Riccia and Asterella being important components of soil crusts which prevent erosion in many arid environments.

Phylogeny
The evidence available suggests that the bryophytes consist of three groups, the mosses, liverworts and hornworts, that have been evolutionarily separate from one another for a vast period of time. The relationships of the liverworts are still unresolved with dierent data sets giving somewhat dierent answers.

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Bryophytes (Liverworts)

Typically the liverworts and/or the hornworts are basal to the mosses and vascular plants or are resolved as sister groups to them. The liverworts have been recognized traditionally as a single natural unit but even this view is being questioned, with some molecular data suggesting that the marchantioids are a separate lineage, equivalent to the mosses, hornworts and other liverworts. Within the liverworts there have been two alternative views of evolution. Endlicher hypothesized that there has been a progressive elaboration of the sporophyte, from forms such as the highly simplied capsule of Riccia to massive ones in the leafy liverworts, e.g. Lepicolea. Gottsche, Lindenberg and Nees postulated the opposite, that the most derived groups are the most structurally simple ones; i.e. Riccia, rather than being primitive, is more advanced. These simplistic views have also been challenged in recent works with the suggestion that there are two contrasting evolutionary histories in the marchantioids, one showing progressive morphological elaboration of structures in the gametophyte and the other a simplication of the gametophyte (and sporophyte). There has been no comprehensive phylogenetic analysis of the jungermannioids but interpretations such as those of Schuster are available. He suggests that one of the basic themes has been the xing, ever more rigidly, of a series of malleable features; e.g. in a number of groups ventral branching has been lost as part of an adaptation to tightly appressed growth on hard substrates along with the evolution of a complicatedly bilobed leaf that produces water pockets.

generally referred to the Metzgeriales, occur (Blasiites, Treubiites and Metzgeriothallus). There are records from the Permian that are attributed to the Marchantiales and subsequently a number of records from the Triassic Metzgeriales, Marchantiales and an extinct family, Naiaditaceae, which may have belonged to the Sphaerocarpales, and one or two Jungermanniales. Although there is an increase in the number of specimens that can be assigned to these groups during the Cretaceous, it is not until the early Tertiary (c. 50 million years ago) that species closely resembling modern leafy liverworts are recorded in Baltic amber (members of Cephalozia, Frullania, Porella, Radula, Solenostoma, Scapania). Miocene amber deposits 2030 million years old provide what many believe are the oldest records of living species, the neotropical Marchesinia bracteata and Stictolejeunea squamata.

Further Reading
Bischler H (1998) Systematics and evolution of the genera of the Marchantiales. Bryophytorum Bibliotheca 51: 1129. Bopp M and Capesius I (1998) A molecular approach to bryophyte systematics. In: Bates JW, Ashton NW and Duckett JG (eds) Bryology for the Twenty-rst Century. Leeds: Maney and British Bryological Society. Crandall-Stotler B and Stotler RE (2000) Morphology and classication of the Marchantiophyta. In: Shaw AJ and Gonet B (eds) Bryophyte Biology. Cambridge: Cambridge University Press. Crum H (2001) Structural Diversity of Bryophytes. Ann Arbor: The University of Michigan Herbarium. Endlicher S (1841) Enchiridion Botanicum. Leipzig: W. Engelmann. Gonet B (2000) Origin and phylogenetic relationships of bryophytes. In: Shaw AJ and Gonet B (eds) Bryophyte Biology. Cambridge: Cambridge University Press. Gottsche CM, Lindenberg JBG and Nees von Esenbeck CG (18441847) Synopsis Hepaticarum. Hamburg: Meissner. Kendrick P and Crane PR (1997) The Origin and Early Diversication of Land Plants. A Cladistic Study. Smithsonian Institution Press: Washington and London. Krassilov VA and Schuster RM (1984) Paleozoic and mesozoic fossils. In: Schuster RM (ed.) New Manual of Bryology, vols 1 and 2. Nichinan: The Hattori Botanical Laboratory. Malcolm B and Malcolm N (2000) Mosses and Other Bryophytes. An Illustrated Glossary. Micro-Optics Press: Nelson. Miller NG (1984) Tertiary and quaternary fossils. In: Schuster RM (ed.) New Manual of Bryology, vols 1 and 2. Nichinan: The Hattori Botanical Laboratory. Renzaglia KS and Vaughn KC (2000) Anatomy, development and classication of hornworts. In: Shaw AJ and Gonet B (eds) Bryophyte Biology. Cambridge: Cambridge University Press. Schuster RM (1984) Comparative anatomy and morphology of the Hepaticae. In: Schuster RM (ed.) New Manual of Bryology, vols 1 and 2. Nichinan: The Hattori Botanical Laboratory. Schuster RM (1984) Evolution, phylogeny and classication of the Hepaticae. In: Schuster RM (ed.) New Manual of Bryology, vols 1 and 2. Nichinan: The Hattori Botanical Laboratory.

Fossil History
There is little information on fossilized bryophytes available and to date the macrofossil record has contributed relatively little to the understanding of the transition from green algae to land plants. Dispersed (unattached) spores, however, provide controversial evidence that there was diversication of embryophytes from the mid-Ordovician onwards. The limited ultrastructural data on spore wall morphology is consistent with some of these spores having an anity with the liverworts. In the early Silurian there was a profound change, with the cryptospores being largely replaced by single trilete spores (consistent with a change from hepatic-like to early vascular plants or their progenitors). The earliest known bryophyte is a late Devonian fossil, Pallaviciniites devonicus, that appeared in the record more than 350 million years ago. It is known only from the gametophyte and has a form similar to that of the modern liverwort group Metzgeriales. There are no other fossils known until the Carboniferous, where three more taxa,

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