Pl Syst Evol 272: 155–180 (2008) Plant Systematics DOI 10.1007/s00606-007-0638-7 and Evolution Printed in The Netherlands

Anatomically preserved marattialean plants from the Upper Permian of southwestern China: the trunk of Psaronius panxianensis sp. nov.

X.-Y. He,1,2 S.-J. Wang,1 J. Hilton,3 B.-L. Tian,4 Y.-L. Zhou1

1State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing, People’s Republic of China 2Graduate University of Chinese Academy of Sciences, Beijing, People’s Republic of China 3School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham, UK 4Beijing Graduate School, China University of Mining and Technology, Beijing, People’s Republic of China

Received 20 July 2007; Accepted 6 December 2007; Published online 31 March 2008 Springer-Verlag 2008

Summary. A new species of the marattialean fern strand internal to the PCB and a large V-shaped strand trunk Psaronius Cotta is described from the Upper formed by the connection of two anchor-shaped Permian Cathaysian flora in the Xuanwei Formation strands. Psaronius panxianensis sp. nov. is important of Guizhou Province, SW China, and named as its leaf traces show three distinct ontogenetic P. panxianensis sp. nov. Stems possess a helically development stages within the trunk, with this orga- diverging sequence of leaf traces organized in a 2/7 nization interpreted as a derived condition within phyllotaxy and are characterized by stages of leaf psaroniaceous marattialean fern evolution. In the stem trace development that include an early ontogenetic abundant air space suggests that P. panxianensis lived stage with a single vascular bundle (Stewartiopteris- in waterlogged substrates with aerenchyma facilitating type), a middle stage with two vascular bundles gaseous exchange. However, the presence of marat- (Stipitopteris-type), and a late stage with three vascu- tialean fern dominated communities in the Upper lar bundles. Roots diverge singly or occasionally in Permian of SW China suggest an overall drying trend pairs, arising alternately from the centrifugal surface with these plants replacing earlier lycopsid and of the peripheral cauline bundles (PCB) near the tip, sphenopsid dominated wetland communities. and form both bound and free root mantles. This species is distinguished from all previously recog- nized species from the Euramerican and Gondwana Keywords: Marattiales; Psaronius; Stipitopteris; floras in having an anchor-shaped sclerenchymatous Stewartiopteris; Upper Permian; anatomy

Correspondence: Jason Hilton, School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK e-mail: [email protected] 156 X.-Y. He et al.: Anatomically preserved marattialean plants

Introduction Hsuanwei) Formation in eastern Yunnan and western Guizhou Provinces. The Xuanwei For- Marattialean ferns are an ancient plant lineage mation constitutes part of the Tuffaceous Series with a fossil record stretching back to the that follows extrusion of the Emeishan Basalts, a Carboniferous (Stewart and Rothwell 1993; Liu Large Igneous Province (LIP) closely associated et al. 2000) that are represented by six extant with the End Guadalupian extinction event genera (Angiopteris Hoffmann, Archangiopteris (Wignall 2001; Ali et al. 2005). As well air-fall Christ & Giesenhagen, Macroglossum Copel., and re-worked tuff horizons, the Xuanwei For- Marattia Sw., Christensenia Maxon and Danaea mation includes extensive coal swamps that Smith) primarily distributed in tropical to sub- developed in deltaic and tidal environments tropical equatorial regions. During the Carboni- encroaching into a shallow carbonate platform ferous and Permian, Marattiales were an (Shao et al. 1998). In this context, peat-forming important component of many peat-forming plant plant communities developed in deltaic and communities and are often associated with occu- island settings (Shao et al. 1998) and in some pying drier areas within and surrounding peat- cases peat formation was terminated by tuff forming mires (e.g. Falcon-Lang 2006). Of the deposition. numerous marattialean taxa recognized from this From the Emeishan Basalts and overlying stratigraphic interval, the stem genus Psaronius Xuanwei Formation several species of Psaronius Cotta was originally proposed for permineralized have been previously reported: Psaronius yun- portions of large trunks (Cotta 1832), but is now nanensis Yang, an invalidly published species, also used to refer to the whole-plant (e.g. was reported from a suburb of Kunming City, Rothwell 1999). To date, Psaronius has been eastern Yunnan Province (Yang 1986), P. hex- reported from Europe (Cotta 1832; Corda 1845; agonus Gu et Zhi (1974) from Sichuan Province, Williamson 1876; Stenzel 1906; Grand’Eury P. sinensis Sze (Sze 1942, 1947) from Weining 1877; Zeiller 1890; Hirmer 1927), North America County in Guizhou Province, and P. wangii Tian, (Dawson 1871; Lesquereux 1880; Gillette 1937; Li et Guo (Tian et al. 1992; Tian and Wang 1995; Blickle 1940; Morgan 1959; Rothwell and Blickle Li and Cui 1995; Tian et al. 1996), P. cf. 1982; Mickle 1984), South America (Brongniart magnificus (Li and Cui 1995; Tian et al. 1996) 1872; Pelourde 1912; Dolianti 1948; Herbst 1985, and some other unpublished species (Li 1987) 1999), Southeast Asia (Ogura 1972) and China from Panxian County, western Guizhou Province. (Sze 1942, 1947; Gu et Zhi 1974; Ma 1985; Yang However, few have been subjected to detailed 1986; Li 1987; Tian et al. 1992; Yao et al. 1994). analysis and this to a large extent precludes While somewhat rare during Early Pennsylvanian accurate comparisons being undertaken with times, Psaronius became a dominant member of those species known from other regions and the coal swamp flora by the Late Pennsylvanian stratigraphic intervals. This hinders an accurate within Euramerica and persists throughout the appreciation of the diversity of the genus and in Permian of Cathaysia (Morgan 1959; DiMichele particular, limits understanding of Psaronius and Phillips 1977; Yao et al. 1994; Tian and Wang during its late Permian phase of evolution as 1995; Tian et al. 1992, 1996; Falcon-Lang 2006). recorded in China. Due to this geological longevity, evolutionary In this paper, we describe a new anatomically patterns within the genus are of considerable preserved species of Psaronius, P. panxianensis paleobotanical interest. sp. nov., from the Late Permian Xuanwei Forma- Petrified marattialean stems are common tion occurring in Panxian County, Guizhou Prov- elements in Upper Permian plant assemblages ince, southern China. This provides a detailed in southwestern China where they occur in anatomical account of a new species of this sediments associated with the Emeishan Basalt important plant group at a time in which com- in eastern Yunnan and southern Sichuan Prov- paratively little is known about them from other inces and in the overlying Xuanwei (formerly parts of the world from which existing knowledge X.-Y. He et al.: Anatomically preserved marattialean plants 157 is restricted to the species P. johorensis Ogura peel technique (Galtier and Phillips 1999), using 5% and P. sp. from Malaya (Ogura 1972). This HCl to etch the mineral matrix. Peels were mounted account provides new insights into species on glass slides using Canada Balsam for transmitted diversity within Marattiales from the Permian light observation. Large peels were photographed of China and it also presents new information under reflected light using a Nikon 4500 Digital on evolutionary patterns within the genus Camera. Glass slides were photographed using a Nikon transmitted light microscope with a Nikon 4500 Psaronius. Digital Camera. Images were adjusted using Adobe Photoshop (V.7) and plates constructed using Corel- Materials and methods draw (V.12). Specimens with peels and slides made from it are deposited in the Paleobotanical Depart- The species investigated in this study consists of two ment of the National Herbarium of China, Institute of large trunks preserved in calcium carbonate within Botany, Chinese Academy of Sciences. volcaniclastic tuffs from the Upper Permian Xuanwei Formation in Yueliangtian coal mine, Panxian Systematic description County, western Guizhou Province and Tianba coal Order Marattiales mine of Xuanwei City, eastern Yunnan Province. Family Psaroniaceae Stenzel Specimens were collected within mine spoil so the Genus Psaronius Cotta 1832 precise horizon within the Xuanwei Formation is Type species P. helmintholithus Cotta 1832 unknown. In each case, the trunk is surrounded by Species Psaronius panxianensis He, Wang, green–grey fine-grained tuff that also fills voids Hilton, Tian et Zhou sp. nov. (aerenchymatous cavities) within the plant. Of the two specimens, that from Yueliangtian coal mine (numbered YLT-001) is well-preserved and is desig- Derivation of specific epiphet From Panxian, the nated holotype, whereas the specimen from Tianba district of China where collections were made. coal mine (numbered YXT-001) is somewhat poorer Specific diagnosis Stem with helically diverging preserved but shows distinctive features that allow us leaf traces organized in a 2/7 phyllotaxy. Peripheral to consider it to belong to the same species. sclerenchymatous sheath (PSS) of the stem robust, Geological information on the Xuanwei Forma- 600–1,000 lm thick. Sclerenchymatous strands (SS) tion including plant compression/impression assem- in stem with smaller thickness than PSS mainly blages has been introduced by Yao et al. (1980) and present in stelar cycle 1 and between cycles 1 and 2. Zhao et al. (1980). Fragmentary plant fossils pre- Leaf trace surrounded by SS. Sclerenchymatous served in volcaniclastic tuffs from the Xuanwei strands also distributed along the centripetal side of Formation at Shanjiaoshu coal mine of Panxian the peripheral cauline bundle (PCB) and leaf traces. County, about 10 km away from Yueliangtian coal Anchor-shaped SS associated with the PCB; two such mine, have been preliminarily studied by Hilton et al. strands positioned on either side of a leaf trace and (2004) who documented the sphenopsid cone tending to connect with each other to form a large Calamostachys sp., an unnamed lycopsid strobilus, V- or U-shaped strand. Both PSS and SS in the the filicalean fern Anachoropteris sp., marattialean stem typically with toothed margin because of inva- ferns including fertile fronds of Eoangiopteris sp. and sion of ground tissue (GT). Ground tissue consisting Scolecopteris sp. as well as isolated portions of mainly of aerenchymatous parenchyma. Developmen- Psaronius sp. root mantles, and two kinds of cardio- tal stages of the leaf trace including an early carpalean seed plant ovule. Other permineralized stage with a single vascular bundle (Stewartiopteris- plants have been identified from the Xuanwei Forma- type), a middle stage with two vascular bundles tion at Huopu coal mine, from which Wang et al. (Stipitopteris-type), and a late stage with three vascu- (2006) reported a single species of Cardiocarpus, lar bundles. The late stage with an outer unclosed noting that the assemblage it was contained in is vascular circle and an internal W- or X-shaped fragmentary but diverse. Further work on this assem- vascular bundle. Outer unclosed vascular circle con- blage is in progress. sisting of two vascular bundles. Centripetally posi- The permineralized trunk was cut with a rock saw tioned bundle C-shaped with enrolled ends and with to reveal transverse, tangential and longitudinal concave side directed outwards. Centrifugally posi- surfaces. Cut faces were prepared with the acetate tioned bundle more U-shaped with straight ends and 158 X.-Y. He et al.: Anatomically preserved marattialean plants with concave side directed inwards. A very narrow zone of parenchyma with isodiametric cells and cavities positioned between the bound root zone and PSS. Bound root zone at least up to 420–450 mm thick. Bound roots arranged in disordered or slightly radiating rows, with tangential dimension of 1.5– 2.0 mm and radial dimension of 1.5–2.5 mm, round to radially elongate in cross section. Roots with larger or smaller steles; larger ones consisting of larger trac- heids with 4–11 (typically 5–8) protoxylem strands, while smaller ones consisting of smaller tracheids usually with 5–6 protoxylem strands. Holotype YLT-001 and peels and slides made from it Type locality Yueliangtian coal mine, Panxian County, western Guizhou Province, China. Lectotype YXT-001 and peels and slides made from it Geological horizon Xuanwei Formation. Fig. 1. Transverse section through trunk of Psaro- Age Wuchiapingian to Changhsingian stages of nius panxianensis sp. nov. BRZ-bound root zone; PSS the Lopingian, Permian (Zhao et al. 1980; Shao et al. peripheral sclerenchymatous sheath. Arrow shows the 1998). undulate part of PSS. Scale bar = 20 mm, holotype, YLT-001, peel 5 Description of specimen YLT-001 General features. Specimen YLT-001 is repre- The inner surface of the sheath is strongly sented by a segment of trunk that is 45 mm long. uneven because of invasion of the GT of the stem The real outline of the trunk of the specimen (Fig. 4). is unknown because that its root mantle is Stele. The stem has a polycylic dictyostele incompletely preserved and unequal in thickness that consists of six concentric stelar cycles where present. The trunk has a slightly elliptical (numbered from cycles 1 to 6 inwards). Adjacent outline in transverse section with a size of cycles are separated by empty areas that mark the 120 9 110 mm (Fig. 1). The stem is well pre- position of GT (see below). In cross section of the served and is somewhat ovate in outline in cross stem the number of vascular bundles varies at section where it is approximately 70 9 45 mm different levels due to divisions and fusion (Figs. 1, 2). between neighboring bundles, with between 43 Peripheral sclerenchymatous sheath. The and 46 bundles present that include cauline stem is surrounded by a robust and continuous PSS bundles and leaf traces. Vascular bundles are that varies from 600 to 1,000 lm thick (Figs. 1, 2). roughly arranged in radial rows (Fig. 2). This is nearly straight or widely waved for its most The vascular bundles in stelar cycle 2 to cycle 6 part, but at two narrower sides the sheath is are often nearly band-shaped and slightly waved undulate due to taphonomic deformation. The with their ends more or less incurved. Cycle 1, the sheath consists of sclerenchyma cells that are outermost cycle, consists of alternately arranged usually isodiametric and vary from 15 to 30 lmin PCBs and leaf traces. The PCBs are often C- or diameter in cross section and elongate with the bluntly V-shaped with their ends conspicuously length of 400 lm or more in longitudinal section. incurved centripetally (Fig. 2). The leaf traces, Some larger (up to 80 lm in diameter) thinner- however, possess different vascular configuration walled cells and occasionally cavities occur depending on their developmental stages. in the sclerenchymatous sheath (Figs. 3, 4). Vascular bundles, whether cauline bundles or leaf X.-Y. He et al.: Anatomically preserved marattialean plants 159

Figs. 2–4. Cross section of the stem of Psaronius panxianensis sp. nov. 2 Enlargement of Fig. 1 showing the entire stem showing anchor-shaped sclerenchymatous strand (SS)(An) adaxial to the meristele of the peripheral cauline bundles (PCB); groove-shaped SS (Gr) surrounding the leaf trace; large V-shaped sclerenchymatous strand (LSS) and vascular bundle (V). Comparing the thickness of meristeles of cycle 2–cycle 6, PCB and leaf trace. IE incurved end of the leaf trace, MP middle part of the leaf trace. Arabic numerals 1–9 represent the position of the leaf traces among which 1 and 8, 2 and 9 are in the same orthostichy. Black arrows indicate roots in the stem. Scale = 10 mm, slide: WP2L-0017. 3–4 Part of the PSS showing parenchymatous cells and air cavities (Ca in 3 and arrows in 4). A marks the area of parenchyma between the stem and bound root zone. All scale bars = 300 lm 160 X.-Y. He et al.: Anatomically preserved marattialean plants traces, consist of xylem strands and surrounding individual meristeles forms voids. However, tissues. Xylem strands in cycle 2 to cycle 6, and of remains of the GT can occasionally be found PCBs and leaf traces in cycle 1 are different in near the PSS, SS and meristeles, and often thickness (Fig. 2) and in the size of tracheids connects or even intrudes these structures (Figs. 5–7). Generally the xylem strands of cycles (Figs. 8, 12, 13). There are two basic types of 2–6 are uniform in thickness and are the thickest, GT. One is aerenchymatous parenchyma in which 0.7–1.4 mm or three to eight cells thick. However the cells are arranged in chains that surround large the xylem strands of the PCBs and leaf traces are air spaces (Figs. 8, 12, 13). The other is paren- not uniform in thickness, usually thinner at their chyma in which the cells are isodiametric with main part and thicker at their incurved ends diameters of about 30–100 lm. Near the periph- (Fig. 2). Xylem strands are 0.5–1.0 mm or two to ery of the stem GT is typically more compact five cells thick in PCBs and 0.1–0.6 mm or one to (Fig. 14), and cells of the GT are slightly elongate six cells thick in leaf traces. Xylem maturation is in longitudinal section (Fig. 15). endarch. Protoxylem is located in irregularly Internal sclerenchymatous tissue. Scleren- spaced groups of four to seven tracheids (Fig. 8), chymatous tissues in the stem are typically and protoxylem tracheids are 20–50 lmin organized in continuous strands. This is mainly diameter. Metaxylem tracheids are polygonal distributed in stelar cycle 1, the outermost cycle, and isodiametric or somewhat radially elongate where it either surrounds leaf traces or extends with the size of 80–250 lm in cycle 2 to cycle 6 along the centripetal side of the PCBs and leaf (Fig. 5), somewhat smaller in PCBs (Fig. 6), and traces. Sclerenchymatous strands usually possess still smaller in leaf traces in cycle 1 (Fig. 7). In uneven sides because of invasion of the GT leaf traces, tracheids in the main part of the (Figs. 12, 21–25). The SS that surround leaf xylem strand are usually a little smaller than traces or extending along the centripetal side of those at the ends (Fig. 2). Small, usually PCBs are usually well developed and consist of 30–50 lm in transverse diameter, nearly isodia- thicker-walled sclerenchymatous cells (Figs. 2,16). metric or radially elongate and polygonal paren- By contrast, those extending along the centripetal chyma cells are dispersed in the metaxylem side of leaf traces are usually weakly developed tracheids and some of them possess dark amor- and consist of thinner-walled sclerenchymatous phous contents (Fig. 5). Tissue surrounding the cells (Figs. 2, 17). xylem strand, where well preserved, consists of The SS located at the centripetal side of the an inner and outer zone. The inner zone is very PCBs has an anchor-shaped configuration thin, about one to three cells thick, and consists (Figs. 2, 18–20). It consists of an arc-shaped of flattened or tangentially elongate thin-walled part extending along the centripetal side of cells with the size of 10–20 9 30–40 lm the vascular bundle and a handle-shaped part (Fig. 10). This zone is usually poorly preserved extending inward from the middle point of the and often present as a brown line (Figs. 6–9), and arc. Two anchor-shaped SS on each side of a we interpret this zone to be phloem. The outer leaf trace tend to be connected with each other zone is usually two to three (occasionally 4–5) by their handle-shaped or arc-shaped parts, cells thick, and consists of small and isodiametric forming a large U- or V-shaped SS (Figs. 2, cells in cross section that are typically 20–80 lm 18, 19, 20). The SS surrounding the leaf traces (usually 30–50 lm) in longitudinal section have a V-, U- or groove-shaped configuration (Figs. 7–11) that are considered to be the vascu- that is related to the different developmental lar bundle sheath. The cells of the vascular stages of the leaf traces (Figs. 2, 18–20). bundle sheath are usually disorderly arranged However, the SS extending along the centripetal whereas in some places they are roughly side of leaf traces are generally developed in the arranged in radial rows. leaf traces in a late developmental stage and are Ground tissue. Ground tissue is poorly often broken due to their thinner-walled scler- preserved and in most cases the areas between enchymatous cell walls (Figs. 2, 17, 21–25). X.-Y. He et al.: Anatomically preserved marattialean plants 161

Figs. 5–11. Features of the stem anatomy. 5–7 Size difference in tracheids of meristele. 5 Tracheids of meristele in cycle 2 to cycle 6. Slide: WP2-0024. 6 Tracheids of the PCB. Slide: WP2-0024. 7 Tracheids of leaf trace in cycle 1. Slide: WP2-0024. 8–11 Structure of meristeles. 8 Slide: WP2-0015; 9 Slide: WP2-0017; 10 Slide: WP2-0015. 11 Slide: WP2-0026. VS vascular bundle sheath, Ph phloem, X xylem, GT ground tissue, Ca air cavity. Arrows in 8 indicate protoxylem poles, while in 5, 10 and 11 indicate parenchymatous cells between tracheids. All scale bars = 100 lm except 8, 9 and 11 = 200 lm 162 X.-Y. He et al.: Anatomically preserved marattialean plants

Figs. 12–17. Anatomical features of the stem of P. panxianensis. 12 Sclerenchymatous strand (SS) interrupted by aerenchymatous parenchyma (GT). Slide: WP2L-0016. 13 Aerenchymatous parenchyma. Slide: WP2L-0017. 14 Parenchymatous GT with air cavity (arrowed) at the periphery of the stem and the PSS is poorly preserved and represented by a thin dark undulated line. A marks the area of parenchyma between the stem and bound root zone. Slide: WP2L-0017. 15 Longitudinal section, showing SS invaded by GT. Slide: WP2-0026. 16 Cells with thicker walls of SS surrounding the leaf trace. Slide: WP2-0024. 17 Cells with thinner walls distributed along the adaxial side of leaf trace. Slide: WP2-0024. Scale bars in 12, 14, 15 = 200 lm; 13 = 100 lm; 16, 17 = 50 lm X.-Y. He et al.: Anatomically preserved marattialean plants 163

of leaf traces and SS, serial cross sections of the stem have been made. Forty-six peels have been obtained and they are numbered in an acropetal sequence of B-1,…, B-17, 28, 27,…, 1 and 0. Peel B-1 represents the basal part of the sequence and 0 represents the top. These 46 peels represent a length of ca. 40–45 mm of the stem. Phyllotaxy. Three cross sections which roughly represent the basal, middle and top levels of the present specimen are shown in Fig. 18. In each cross section of the stem, seven leaf traces are present that represent seven orthostichies. Leaf traces are arranged in a helical phyllotaxy and are numbered from 0, 1,… according to their diverging order. Leaf trace 7 is in the same orthostichy as leaf trace 0, but at the upper position from the latter. From 0 to 7, the spiral line surrounds the stem twice and contains seven leaf traces, so the stem possesses a 2/7 phyllotaxy. Leaf traces in cycle 1 vary greatly in their shape due to taphonomic deformation. Those located at the two narrow sides of the elliptical stem, such as leaf traces 1, 3 and 6 shown in Figs. 2 and 18, usually have smaller tangential and larger radial dimensions (8–10 vs. 11–20 mm). Those located at two wide sides of the stem, such as leaf traces 0, 2, 4 and 5 (Figs. 2, 18) usually have larger tangential and smaller radial dimen- sions (17–23 vs. 7–15 mm). Origin and developmental stages of the leaf trace. Stelar cycle 1, the outermost cycle, consists of alternatively arranged leaf traces and PCBs. The next internal cycles consist of alternatively arranged cauline bundles and leaf Fig. 18. Schematic serial transverse sections through stem of P. panxianensis. C Basal level (peel gaps, some of which are closed by outgoing leaf B-3), B middle level (peel 28) and A top level (peel 1). traces (Fig. 19). The cauline bundles are roughly Arabic numerals 0, 1, ..., 7 represent the positions of arranged in tangential cycles and radial rows individual leaf traces. Detailed explanation is intro- (Figs. 2, 18). The innermost cycles, cycles 5 and duced in the text. 40% Black colored line PSS and SS; 6, show only a small amount of change through 80% black colored line vascular bundles except of the length of the present specimen; no leaf diverging leaf traces; black colored line vascular traces have been found to originate from them bundles of diverging leaf traces (Fig. 18). The innermost leaf traces we have observed originate from cycle 4 (Fig. 19a). Phyllotaxy and developmental stages of When traced acropetally, leaf traces diverge leaf traces and SS. In order to clearly demon- and are united with the cauline bundle of the strate the phyllotaxy and developmental stages next external cycle (Fig. 19b–e). Eventually the 164 X.-Y. He et al.: Anatomically preserved marattialean plants X.-Y. He et al.: Anatomically preserved marattialean plants 165

Fig. 20. Diagram showing the developmental stages of the leaf traces in cycle 1 and with detailed explanations introduced in the text. Peels: A–E and I (B-8); F (28); G (25); H (l) 1; J (19). 40% Black colored lines PSS and SS; 80% black colored line vascular bundles except of diverging leaf traces; black colored line vascular bundles of diverging leaf traces. Arrows indicate position of small inward projecting strands. All scale bar = 10 mm leaf traces enter cycle 1 and are united with two developmental stages of a single leaf trace, from PCBs to form a large V-shaped vascular bundle it separating from a large V-shaped vascular with inrolled tips (Fig. 19m–p). Leaf traces then bundle (such as leaf trace 7 in Fig. 19a and leaf separate from the large V-shaped vascular trace 9 in Fig. 19q–r) to it diverging from the bundle and enter into the outermost cycle, stem and entering the bound root zone (such as replacing the older one (such as leaf trace 7 in leaf trace 0 in Fig. 19a–c), several leaf traces, Fig. 19a–c, and leaf trace 9 in Fig. 19q, r). arranged in a helical sequence, have been used to Because the length of the present specimen is demonstrate the developmental stages of the leaf too short to permit us to reveal all of the trace in the outmost cycle and changing patterns b Fig. 19. Diagram showing the origin and developmental stages of leaf traces. Detailed explanation is introduced in the text. Peels: A (B-1); B (B-8); C (B-17); D (25); E (4); F (1); G (B-1); H (B-15); I (27); J (5); K (0); L (B-6); M (B-8); N (28); O (0); P (B-1); Q (B-17); R (25). 40% Black colored lines sclerenchymatous sheath and strands; black colored lines vascular bundles of diverging and potential leaf traces. Hollow lines cauline bundles. Arrows indicate the position of small inward projecting strands. All scale bars = 10 mm 166 X.-Y. He et al.: Anatomically preserved marattialean plants

of the SS associated with the leaf trace (Figs. 20 in a lower level and enters the bound root zone in a–j, 21, 22, 23, 24, 25). In Fig. 20a there are two this level. In contrast, leaf trace 7 is newly leaf traces, 7 and 0, which are in the same formed at this level. The vascular bundle of leaf orthostichy. Leaf trace 0 was formed earlier and trace 7 in cross section forms a shallow arc-shape X.-Y. He et al.: Anatomically preserved marattialean plants 167 b Figs. 21–27. Anatomical features of the stem of P. panxianensis revealed in transverse section. 21–25 Different developmental stages of leaf trace. 21–23 Leaf trace 3 in peels B-16, 28 and 20, respectively. 21 Two incurved ends of the leaf trace are close to each other. Note thicker incurved ends (2) and thinner main part (1) of the leaf trace. Arrow shows the GT within the U-shaped SS (U) surrounding the leaf trace. 22 Two incurved ends of leaf trace are connected to each other and form an internal strand (IS) and an outer strand (OS) and both of them are connected to each other by the point (arrowed). SS broken SS located along the centripetal side of the leaf trace. 23 The IS and the OS are departed. Note that small inward projecting strand (arrowed) at the each side of the centripetally 1/3 part of the OS. 24–25 Leaf trace 2 in peels B-8 and 19, respectively. 24 Leaf trace is in nearly same developmental stage as that in 23. 25 The same leaf trace in a higher level showing OS divided into a small centripetal strand (ADS) and a large centrifugal strand (ABS). 26–27 Roots in the stem. 26 Two newly formed roots with large octoarch steles (arrowed) consisting of large tracheids. 1 Centripetal sides, 2 centrifugal sides. Slide: WP2L-0017. 27 One newly formed root with a small polyarch stele (arrowed) consisting of small tracheids. 1 centripetal sides, 2 centrifugal sides. PVB-PCB from which the newly formed root departs. Slide: WP2L-0016. Scale bars in 21–25 = 1 mm, 26, 27 = 200 lm with its main part internally convex and two tips resembles leaf trace 3 in a higher level. There is inrolled centripetally. In Fig. 20b leaf trace 6 is also a small inward projecting strand (arrowed) at shown which was formed earlier than leaf trace 7. the each side of the centripetally 1/3 part of the The vascular bundle of leaf trace 6 is tangentially OS and an inverted X-shaped inner strand (see narrower than leaf trace 7 and this relative also Fig. 24). Figure 20j shows leaf trace 2 at a narrowness may be a function of differential higher level (peel 19) and here the centripetally compression of the specimen. It also has its main 1/3 of the OS has divided and forms a small and part internally convex and its tips strongly shallow C-shaped strand with its slightly inrolled inrolled centripetally. The vascular bundle of tips (see also Fig. 25). A new leaf trace, 9, which leaf trace 5 in Fig. 20c is slightly internally is in a same orthostichy as leaf trace 2, has also convex. In Fig. 20d, leaf trace 4 has a straight, been formed. not internally convex, main part and two strongly Area between the bound root zone and centripetally inrolled tips, which are close to each stem. Between the bound root zone and the other. In Fig. 20e, leaf trace 3 is quite different in sclerenchymatous sheath, a narrow, 0–12 cells shape from leaf traces 7–4 in possessing an thick, zone of isodiametric parenchyma cells externally convex main part and its two centri- occur. These cells typically have diameters of petally inrolled tips touch each other (see also 50–130 lm and possess thinner walls than those Fig. 21). Figure 20f–h shows the same leaf trace of interstitial tissue of bound root zone and some as shown in Fig. 20e but at a higher level (peels cavities as well as tannin cells occur in this zone 28, 25 and 1), and demonstrates the minor (Fig. 28). changes of vascular bundle of the leaf trace 3. Roots. Roots diverge singly, occasionally in It is noted that two inrolled tips of the vascular pairs, and alternatively from the centrifugal side bundle are connected to each other to form an and near the ends of the PCBs. Once departed inverted ‘‘X’’-shaped internal strand (IS) that is from the PCBs, the root goes in a nearly still connected with the outer strand (OS) at the horizontal course and then in a downward and point shown (arrowed) in Fig. 20f (see also outward course. Like those in the root mantle, the Fig. 22). In Fig. 20g, the IS is divided from the roots in the stem also vary in the size of stele and OS and the former is surrounded by the latter (see tracheids (Figs. 26, 27; see below). The cortex of also Fig. 22). Figure 20h shows a small strand the root is usually poorly preserved. The scle- (arrowed) at each side of the centripetally 1/3 part renchyma sheath forms soon after the root has of the OS is projecting inward (see also Fig. 23). departed from the PCB and that of the centrifugal In Fig. 20i leaf trace 2 is shown which is next to side has been formed earlier than the centripetal leaf trace 3 in the peel B-8 and approximately side (Figs. 26, 27). 168 X.-Y. He et al.: Anatomically preserved marattialean plants

Figs. 28–35. Transverse sections through bound root zone of P. panxianensis. 28 Parenchyma zone (A) with air cavities (Ca) between the PSS and bound root zone (arrowed). Slide: WP2L-0016. 29 Part of the bound root zone showing the arrangement of roots. Black arrows show root with large steles while white arrows show roots with small steles. Peel: YLT-0001/B5. 30 Interstitial tissue between the roots. Arrow indicates a narrower cell zone. Slide: WP2-0022. 31 A root from which a lateral roots are diverging (arrows). Slide: WP2L-0016. 32 Cells of the sclerenchymatous sheath. Slide: WP2-0021. 33–35 Three roots possessing tetrarch, pentarch and hexarch steles respectively. Arrows indicate secretory cells with black contents. Slides: WP2-0022, WP2-0021 and WP2-0022. All scale bars = 200 lm except 29 500 lm, 30, 31 = 300 lm and 32 = 50 lm X.-Y. He et al.: Anatomically preserved marattialean plants 169

Figs. 36–42. Transverse section of bound root zone in P. panxianensis showing variation in anatomical configurations. 36 Two heptarch roots with arrow showing secretory cells with black contents. Slide: WP2-0021. 37 An ennearch root. Slide: WP2-0022. 38 A hendecarch root. Slide: WP2L-0013. 39 Enlargement of the stele of the root in 35. Arrows show secretory cells with black content. En endodermis. 40 A root with a small stele (arrowed). Slide: WP2-0021. 41 Enlargement of the stele of the root in 40, showing five xylem arms (arrowed). 42 An abnormal root (arrowed) with a small stele in the bound root zone. Slide: WP2-0022. All scale bars = 200 lm except 39 and 41 which are 50 lm 170 X.-Y. He et al.: Anatomically preserved marattialean plants

Figs. 43–45. Transverse section of Specimen YXT-001. 43 Trunk with oval stem in which 1 and 2 represent positions of two diverged leaf traces. An anchor-shaped SS centripetal to the PCB; CVB crushed vascular bundles of the stem, R roots. Arrow indicates position of undulated part of the PSS at one narrow side of the stem. 44 Enlargement of the stem in 43 showing PCB. 45 Enlargement from 43 showing a part of the bound root zone. Black arrows indicate roots with large steles and white one indicate roots with small steles. Scale bar in 44 = 5 mm, 45 = 1mm X.-Y. He et al.: Anatomically preserved marattialean plants 171

The root mantle of the present specimen is only metaxylem tracheids and also have more (4–11, represented by the bound root zone that is of typically 7) protoxylem poles (Figs. 33–38). variable thickness in this preserved condition, Other roots are usually distributed in the outer measuring about 42–45 mm in thickness on the part of the bound root zone and have the smaller thicker side and 22–25 mm on the thinner side steles. These tend to consists of fewer and smaller (Fig. 1). Free root zone has not been observed. metaxylem tracheids and have fewer (typically Judging from the ratio of the thickness of root zone 5–6) protoxylem poles (Figs. 40, 41). Besides, and the radius of the stem, the specimen appears to there are also some different roots in the bound represent the middle level of a mature trunk. root zone which are usually smaller in dimension Bound roots are arranged in a disordered and the cells of the sclerenchymatous sheath are fashion or in roughly radiating rows (Figs. 1, 2, also smaller in size than those as stated as above 29). Some roots are approximately round while (Fig. 42). These represent lateral roots. others are more or less oval with their long axis orientated in the radial direction (Fig. 29). A Description of specimen YXT-001 dense interstitial tissue made up of parenchyma cells fills the space between bound roots. The General features. The trunk is nearly elliptical cells of interstitial tissue are more or less radially in shape in cross section with the long axis of elongate with different shapes that include cells 125 mm and the short axis of 90 mm. The stem is that are rectangular, subtriangular, elliptical and also elliptical in shape in cross section with the polygonal in cross section (Fig. 30). Individual long axis of 80 mm and the short axis of 55 mm roots are about 0.7–2 mm in diameter, exhibit a (Fig. 43). The root mantle is represented only by prominent sclerenchyma sheath that is about the bound root zone that has the thickness of 15– 0.28–0.5 mm or 8–11 cells thick, and are inter- 30 mm. rupted occasionally by horizontally diverging Sclerenchymatous sheath. The sclerenchy- lateral roots (Fig. 31). The cells of the scleren- matous sheath around the stem is robust and chyma sheath are usually 35–40 lm in diameter varies from 700 to 1,000 lm thick, thus being a and possess thick walls, usually 7–10 lm little thicker than the type specimen. The struc- (Fig. 32). Within the sclerenchyma sheath inner ture of the sheath is similar to that of the type cortical tissue of roots occur in some cases but specimen. There are a number of roots in the are often not well preserved while in other cases peripheral region of the stem and some of them are absent (Figs. 33, 34). Where present, they pass through the sclerenchymatous sheath consist of parenchyma or sometimes aerenchy- (Fig. 43). In general, the stem is poorly preserved matous parenchyma (Fig. 35). The cells of the in comparison with the type specimen. inner cortex are isodiametric in cross section with Stelar organization and other features. The the diameter of 30–100 lm. In general, large SS and meristeles are extensively deformed and it secretory cells filled with black or dark brown is difficult to determine exactly how many contents are distributed in the inner part of the meristelic cycles exist. It is estimated that there inner cortex (Fig. 35, 36). Internal to the inner are seven or eight helically arranged leaf traces in cortex there are two to three layers of cells that each cross section, but the meristelic configura- are flattened with much smaller radial dimension tion of the leaf traces are unknown due to poor and larger tangential one (Fig. 39) and should be preservation. Poorly preserved anchor-shaped SS the endodermis. In most roots, the endodermis is adaxial to the PCBs can be seen in some places poorly preserved and present only as a dark (Figs. 43, 44). brown-colored layer surrounding the stele. The Roots. The roots in the bound root zone are roots possess polyarch and exarch actinosteles. nearly same in the shape and the size or slightly Steles in roots distributed near the stem tend to be smaller than those of the type specimen. There larger in dimension than those positioned else- are also two types of roots depending on the stele where. They also consist of more and larger and tracheid size (Fig. 45) such as those in type 172 X.-Y. He et al.: Anatomically preserved marattialean plants

Discussion Comparisons. The gross morphology and anatomical arrangement of the specimens described conform with those of previously recognized trunks of Paleozoic Marattialean stems of the family Psaroniaceae as delimited by Herbst (1986) based on permineralized trunks and petioles. According to Herbst (1986, 1987), there are three genera under the family Psaroniaceae of which Psaronius Cotta, distributed widely throughout Euramerica, Cathaysia and the South American parts of Gondwana, is the most commonly occurring. The remaining two genera, Tietea (Solms-Laubach) Herbst and Tuvichapteris Herbst are only known from the Gondwanan flora in South America. Psaronius is characterized by its regular and cyclic organization of vascular bundles that are mainly tabular or band-shaped and also by its single vascular bundle in leaf traces and petioles (Herbst 1987). Tuvichapteris is distinguished from Psaronius by its greater number of disorderly arranged vascular bundles in the stele and leaf traces and petioles that also have petiole-parenchyma that is a big mass of thick-walled parenchyma located abaxial to many vascular bundles in the petiole (Herbst 1987). Tietea is more similar to Tuvichapteris than to Fig. 46. Comparison of the leaf trace configuration Psaronius and also possesses disorderly arranged and the configuration of sclerenchymatous tissue vascular bundles in the stele (meristeles) and in selected species of Psaronius. A P. blicklei many vascular bundles in leaf traces and petioles, (Morgan 1959, Fig. 33). B P. arrojadoi (Herbst 1985, but shares a certain degree of cyclicity in its outer Fig. 1). C P. octogonus (Yao et al. 1994, Fig. 2). cycles with Psaronius and lacks petiole- D P. panxianensis sp. nov parenchyma. Herbst (1999) also reported an unusual species of Psaronius from the Lower specimen. However, it is a little different from Permian of Brazil, P. sinuosus Herbst, which has the type specimen that in this specimen the larger very long and strongly coiled vascular bundles steles are mainly pentarch to hexarch, while in that are organized in a non-cyclic arrangement and the type specimen they are mainly pentarch to many vascular bundles in leaf traces. As reported octoarch. (Herbst 1999) this species is very different from Although this specimen does not preserve all other species of Psaronius and in our view features of the leaf trace configuration, structure requires further consideration before being further of the vascular bundle and also the GT, we believe interpreted. The present specimens are doubtless it belongs to the same species. Its structure of the of the Psaronius-type as their regular and tabular bound root zone, outline of the stem in the cross vascular bundles are arranged in a cyclic section, structure of the sclerenchymatous sheath arrangement throughout the stem and they have and anchor-shaped SS adaxial to the PCBs are the endarch protoxylem and a robust, continuous same as the type specimen confirming the two sclerenchymatous sheath. specimens belong to a single species. X.-Y. He et al.: Anatomically preserved marattialean plants 173

Fig. 48. Diagram of leaf scars of Psaroniaceae from the Permian of China showing the vascular configu- ration. A Caulopteris sinensis Lee. B Caulopteris Fig. 47. Leaf trace configuration of P. panxianensis manchuriensis Hatae. C Caulopteris sichuanensis (A drawn from peel 20) and P. wangii [B redrawn Zhu, Hu et Li. D Caulopteris henanensis He et Sun. from Pl. 59, Fig. 2 of Tian and Wang (1995)] Thick black line represents outline of leaf scar, thin black line represents position of vascular bundle [A To date, more than 100 species of Psaronius from Fig. 116 of Gu et Zhi (1974); B from Fig. 115 of have been established (Jongmans and Dijkstra Gu et Zhi (1974); C from Fig. 3 of Zhu et al. (1984); 1963; Morgan 1959; Mickle 1984; Dijkstra 1985; D from He and Sun (1998)] Herbst 1985, 1999). The main difference of the present specimens with all other species of internal to the PCB and large V-shaped strand Psaronius, with the exception of P. sinuosus,is formed by connection of two anchor-shaped in the anatomy and organization and the leaf strands (see Fig. 46). Here we concentrate detailed traces. In all other species, leaf traces possess a comparisons with the six species previously single C-, U- or V-shaped vascular bundle of the reported from the Cathaysian Flora as these are Stewartiopterid-type (Stidd 1971). From this, the closest in organization and structure to the there is transition to a stipitopterid type of leaf present specimens: P. sinensis Sze, P. hexagonus trace (Stidd 1971) with an outer O-shaped strand Gu et Zhi, P. jiangsuensis Yao, Liu et Li, and an internal W-shaped strand. But in the P. octogonus Yao, Liu et Li, P. wangii Tian, Li present specimen the leaf traces undergo further et Guo and P. johorensis Ogura. Apart from the transformation: the O-shaped strand divides into above named species, other reports that mention two, with a small C-shaped strand separating Psaronius from China are too limited to enable centripetally and this results in a leaf trace with accurate comparisons; Tian (in Li and Cui 1995) three strands (Figs. 19r, 20j, 25, 46d, 47a). and Tian et al. (1996) briefly illustrated a specimen Furthermore, this leaf trace with three strands is under the name P. cf. magnificus Rothwell et different from the leaf traces of P. sinuosus Blickle that was accompanied by a very simple Herbst that have many vascular bundles that are description, and Tian and Zhang (1980) reported not derived from the vascular configuration of very simply a P. sp., while Yang (1986) reported Stewartiopterid-type and Stipitopterid-type, as P. yunnanensis, but only gave very simple descrip- seen in the present specimens. tion and a simplified diagram of the stem. The The present specimens differ from all species latter taxon was not accompanied by a diagnosis, previously recognized from the Euramerican and illustration nor was a type specimen designated, Gondwana floras in having an anchor-shaped SS and as a consequence the species is invalid. 174 X.-Y. He et al.: Anatomically preserved marattialean plants

Figs. 49, 50. Volcaniclastic tuff void fills of aerenchymatous root cavities and stem of P. panxianensis sp. nov. 49 Boundary between bound root zone showing root cavity (R) and surrounding sediment (V) and localized tuff infill of cavity (arrow). Specimen YXT-001, scale bar = 300 lm. 50 Volcaniclastic sediment from within the stem in plane polarized light showing texture of mineral grains. Specimen YXT-001, scale bar = 200 lm

Psaronius sinensis (Sze 1942, 1947) and are smaller in size, usually 1–2 mm, with the P. johorensis (Ogura 1972) are quite different steles usually of 6–8 protoxylem poles (Yao et al. from the present specimens in the structure of 1994). Further comparisons are restricted by poor leaf traces and configuration of SS in the preservation in P. jiangsuensis. outermost stelar cycle. Both of these species Psaronius octogonus is similar to the present have C-shaped leaf traces with a single vascular specimens in the configuration of SS and leaf bundle and lack anchor-shaped SS internal to the trace in the outermost stelar cycle (Fig. 46c). PCB, and also lack large V-shaped SS formed by However, in P. octogonus cauline bundles are connection of two anchor-shaped SS. P. hexag- arranged in eight regular radial alignments, SS onus seems to possess the same configuration of are distributed throughout the entire transverse the SS in the outermost stelar cycle as that of the section of the stem and the phyllotaxy is whorled present specimens, although the SS in P. hexag- (Yao et al. 1994). In the present specimens, SS onus are not so conspicuous (Gu et Zhi 1974; Li are mainly distributed in stelar cycle 1 and and Cui 1995). However, other differences sep- between cycles 1 and 2. Cauline bundles are arate the species. P. hexagonus possesses a arranged in five irregular radial alignments and C-shaped leaf trace with a single vascular bundle, the phyllotaxy is helical. Besides, the internal whorled phyllotaxy, regularly arranged cauline bundle of the leaf trace in P. octogonus is not as bundles in a hexagonal organization whereas in undulated and the ends of the small centripetal the present specimens leaf traces are composed of bundle are not as enrolled as in the present three vascular bundles and in a helical phyllotaxy specimens (Fig. 46c, d). Moreover, other fea- and with cauline bundles arranged in a less tures, such as the GT, the structure of the vascular regular pattern. bundle and the roots of P. octogonus are In P. jiangsuensis, the leaf traces are poorly unknown because of poor preservation, which preserved which makes it difficult to compare make it difficult to compare it with the present them with those of the present specimens (Yao specimens. et al. 1994). The roots of P. jiangsuensis are Psaronius wangii Tian et al. is a species of larger in size, 3 9 5 mm, with the steles of 9–12 Psaronius based on well-preserved specimens protoxylem poles. In the present specimens, roots from the Cathaysian Flora (Tian et al. 1992; Tian X.-Y. He et al.: Anatomically preserved marattialean plants 175

Table 1. Marattialean fern taxa previously reported and Wang 1995; Li and Cui 1995; Tian et al. from the Xuanwei Formation 1996). The species was discovered from the same Taxon Authors location and stratigraphic horizon as the present specimens. In some regards P. wangii is similar Vegetative organs to the present specimens as it has the same Pecopteris qingyunensis Zhang Zhao et al. configuration of the SS in the outermost stelar (1980) cycle. However, they differ in numerous other Pecopteris echinata Gu et Zhi Zhao et al. aspects including different organization of (1980) Pecopteris elegantula Zhang Zhao et al. diverging leaf traces. In P. wangii, when the leaf (1980) trace diverges from the stem, its inrolled tips tend Pecopteris fuyuanensis Zhang Zhao et al. to depart from the main body of the leaf trace and (1980) form two small C-shaped strands with their Pecopteris (Asterotheca) guizhouensis Zhao et al. convex side opposite to each other (Fig. 47b). Zhang (1980) The stem is usually radially symmetrical and Pecopteris lingulata Zhang Zhao et al. cauline bundles tend to be arranged in more or (1980) less radial alignment. Roots usually possess large Pecopteris longifolioides Zhang Zhao et al. steles consisting of large tracheids similar to (1980) some roots of the present specimens. The scler- Pecopteris marginata Gu et Zhi Zhao et al. enchymatous sheath and strands are usually (1980) continuous and with smooth sides, which is Pecopteris sahnii Hsu Zhao et al. (1980) unlike the present specimens in which the Protoblechnum (Compsopteris) Guo et al. sclerenchymatous sheath and strands are usually ellipticum (Yang et Chen) (1992) with tooth-like sides and even discontinuous by Caulopteris fuyuanensis Zhao (1990) Zhao (1990) the invasion of the GT. Moreover, the vascular Psaronius wangii Tian et al. Tian et al. bundle sheath in P. wangii differs from the (1992) present specimens. In P. wangii the sheath is P. tianii Li (1987) Li (1987) usually one to two cells thick. These cells are P. cf. magnificus Li (1987) variable in outline in cross section and are more Fertile organs or less angular in shape. The walls of the cells, Zhutheca densata (Gu et Zhi) Liu et al. except for those that contact the GT, are Liu, Li et Hilton (2001) conspicuously thicker than those of the cells of Rajahia guizhouensis Zhang Zhao et al. the GT, which are usually poorly preserved. In (1980) R. minor Zhang Zhao et al. contrast, in the present specimens the vascular (1980) bundle sheath is thicker and two to five (usually R. major Zhang Zhao et al. 2–3) cells thick. The cells are usually nearly (1980) isodiametric in outline and approximately spher- R. mirabilis (Gu et Zhi) Zhang Zhao et al. ical. Furthermore, there is usually a thin layer of (1980) brown colored substance that lacks cellular R. rigida (Yabe et Oishi) Zhang Zhao et al. structure surrounding the sheath that has not (1980) been recorded in P. wangii. D. mirabilis Gu et Zhi Gu et Zhi From the comparisons above we conclude (1974) that the present specimens represent a new D. saraepontanus Stur Gu et Zhi species of Psaronius, for which we erect (1974) P. panxianensis sp. nov. Ptychocarpus tingii Halle Gu et Zhi (1974) Leaf trace configuration. The most distinc- Acitheca? cupressoides Gu et Zhi Gu et Zhi tive character of the new species is its leaf trace (1974) configuration of three vascular bundles that only occurs in two other species also from the 176 X.-Y. He et al.: Anatomically preserved marattialean plants

Cathaysian flora: P. octogonus and P. wangii. henanensis (He and Sun 1998) are all distributed However, in P. wangii the leaf trace configura- in the Late Carboniferous to Early Permian of tion is very different from that in the new species North China. They resemble each other in having (see Figs. 46c, 47b). In P. wangii, when the leaf a much smaller upper bundle that lacks inrolled trace diverges from the stem, its inrolled tips tend tips and an internal bundle that is weakly to depart from the main body of the leaf trace and undulate (Fig. 48a, b, d). However C. sichuan- form two small C-shaped strands with their ensis (Zhu et al. 1984), the sole species distrib- convex sides opposite to each other (Fig. 47b). uted in the Upper Permian of South China, is In P. octogonus, although the leaf trace config- conspicuously different from the former three uration is similar to that of the new species, its species in having an upper bundle that has internal bundle of the leaf trace is not as inrolled tips that is nearly the same size as the undulated and the ends of the small centripetal lower bundle, and a strongly undulate or inverted bundle are not as enrolled as those in the latter V-shaped internal bundle (Fig. 48c). The leaf (Fig. 46c, d). In P. panxianensis, P. wangii and trace configuration of the new species is in this probably P. octogonus, a leaf trace configuration regard similar to the vascular configuration of with three vascular bundles results from devel- C. sichuanensis than to the younger species opment from the Stewartiopterid-type through recorded from North China. the Stipitopterid-type of leaf trace configuration. Species of Caulopteris and Megaphyton Artis This is different from the leaf trace configuration reported from the Carboniferous and Early of Tietea and Tuvichapteris in which many Permian of Euramerica all possess the Stewarti- vascular bundles are disorderly arranged and are opterid and Stipitopterid leaf scar vascular config- not developed from either a Stewartiopterid-type uration (Andrews et al. 1970; Pfefferkorn 1976). or Stipitopterid-type configuration. Vascular configurations like those of C. sinensis, It is interesting that the leaf trace configura- C. henanensis, C. manchuriensis and C. sichuan- tion of the present specimens is same as the ensis have not been documented from the Eur- vascular configuration observed in the leaf scars american Flora, and we have no information on the of several impression–compression species of leaf scar vascular configuration of Psaroniaceae marattialean trunk or stem reported from the from Gondwana. It is very possible that the leaf Carboniferous and Permian floras of Cathaysia. trace configuration with three vascular bundles In Cathaysia, seven species of Caulopteris Lind. such as that of the new species, P. octogonus Yao et Hutt have been reported amongst which only et al. as well as the trivascular leaf scar configu- one, C. wudaensis, possesses the Stipitopterid rations of C. sinensis, C. henanensis, C. manchu- vascular configuration (Sun and Deng 1999). riensis and C. sichuanensis represent a derived Each of the other Caulopteris species possesses a feature within marattialean ferns, appearing geo- vascular configuration very similar to the leaf logically later than the Stewartiopterid leaf trace trace configuration observed in P. panxianensis with a single vascular bundle and Stipitopterid leaf with three vascular bundles in each leaf scar. Of trace with two vascular bundles and scar config- these bundles, two are arranged in a ring within urations observed in all Psaronius, Caulopteris which the third one is positioned, and there is an and Megaphyton species from Euramerica and opening between the two outer bundles. The Gondwana. The oldest leaf scar with the Stewart- upper (adaxial) bundle is usually smaller and is iopterid and Stipitopterid vascular configuration is shallowly C-shaped, while the lower (abaxial) Megaphyton protuberans in the late Mississippian bundle is usually larger and is deeply U-shaped. (Lower Chesterian) of Illinois (Pfefferkorn 1976), By comparison the internal bundle is short and and the oldest species of Psaronius displaying extends horizontally in a different shape from Stewartiopterid and Stipitopterid leaf traces are species to species (e.g. Fig. 48). Caulopteris early Pennsylvanian in age from the Bashkirian sinensis (Li 1963; Gu et Zhi 1974), C. manchu- stage, with P. simplicicaulis (late Namurian; riensis (Hatae 1931; Gu et Zhi 1974) and C. DiMichele and Phillips 1977) and P. renaulti X.-Y. He et al.: Anatomically preserved marattialean plants 177

(Westphalian A, Williamson 1876). However the available to enable more detailed floristic com- oldest species exhibiting a trivascular configura- parisons to be undertaken, although Hilton et al. tion of its leaf scars from the Cathaysian Flora are (2004) and Wang et al. (2006) documented three latest Pennsylvanian (Stephanian), namely C. species of seed plant ovules from the Xuanwei manchuriensis and C. sinensis. Only P. wangii, Formation, which are in all probability pterido- P. octogonus and the new species have a leaf trace spermalean. Here we postulate a similar trend in configuration with three vascular bundles and are the Upper Permian of South China with the from the Upper Permian thus being considerably Xuanwei Formation to that observed earlier in younger than M. protuberans, P. simplicicaulis Euramerica, representing a drier community than and P. renaulti. the stratigraphically older floras. However, for Paleoenviromental and taphonomic signif- the Xuanwei Formation the floristic and climatic icance. In the Xuanwei Formation large permin- patterns are less straight forwards than those eralized stems of Psaronius are relatively recorded in Euramerica, a problem brought about common and include P. panxianensis sp. nov., by the absence of comparative investigations P. wangii Tian, Li et Guo, P. cf. magnificus made on plant occurrences from this stratigraph- (Herzer) Rothwell et Blickle as well as other ical interval in China. In P. panxianensis the unpublished species (S. J. Wang, work in abundant aerenchymatous GT in its stems and progress). Similarly, compression–impression roots demonstrates that the plant lived in water- marattialean remains are also common in assem- logged conditions in which this airy tissue would blages from the Xuanwei Formation, including have facilitated gaseous exchange between the vegetative leaves of Pecopteris as well as fertile aerial and sub-aerial parts of the plant. While this remains of Zhutheca, Rajahia, Danaeites, Pty- in itself may seem to contradict the postulated chocarpus and Acitheca (see Table 1 for sum- drying outlined above, the sedimentological mary). Although several of these taxa require context of the Xuanwei Formation may in part reinvestigation to verify their structure and explain this. Shao et al. (1998) presented an identity, these accounts collectively demonstrate interesting paleoenvironmental model for the that psaroniaceous marattialean ferns were an Upper Permian of South China, including the important element in the Late Permian wetland Xuanwei Formation, in which marine influenced regional flora from eastern Yunnan, western coals swamp developed in deltaic and tidal–flat Guizhou and southern Sichuan provinces at this environments prograding into a shallow carbon- time, replacing older lycophyte and sphenophyte ate platform. In this context, P. panxianensis may dominated floras (e.g. Shen 1995). This follows a have grown in tidal swamps settings with an similar trend to that recorded in Euramerica at the abundant water supply, albeit saline in composi- end of the Moscovian where lycophyte/spheno- tion. As such, drier terrestrial conditions may phyte dominated communities are replaced by have been offset against water available in these arborescent marattialean fern and pteridosperm tidally influenced settings. dominated floras. In Euramerica, this period of In extant plants, aerenchyma in roots can dramatic community change is associated with result in a small zone of oxygenated soil around the regional demise of wetland peat-forming individual roots providing localized aerobic communities following their mid-Pennsylvanian environments (e.g. Blom et al. 1994). Oxygen- acme (e.g. DiMichele and Phillips 1996; Cleal ated sub-aerial microenvironments have been and Thomas 2005; Hilton and Cleal 2007) and demonstrated to be important for carbonate has been extensively linked to climate change lagersta¨tte preservation (e.g. Baird et al. 1986; and in particular reduction in water availability Allison and Pye 1994) and this may have been an (Cecil 1990; DiMichele and Phillips 1996; important factor contributing to permineralized DiMichele et al. 2001). Comparable synthetic preservation in these settings. However, previous data on Chinese pteridosperm occurrences studies were undertaken in primarily clastic within the Xuanwei Formation are not presently estuarine settings (Fisher et al. 1998; Allison 178 X.-Y. He et al.: Anatomically preserved marattialean plants and Pye 1994) which may not be comparable Brongniart A (1872) Notice sur le Psaronius brasil- with volcaniclastic lithologies and deltatic set- iensis. Bull Soc Bot Fr 19: 3–10 tings such as those we document here. Cecil CB (1990) Palaeoclimate control on strati- In P. panxianensis sp. nov., the aerenchyma- graphic repetition of chemical and siliclastic rocks. tous root cavity is typically filled with diagenetic Geology 18: 533–536 Cleal CJ, Thomas BA (2005) Palaeozoic tropical carbonate (Fig. 49) but in some cases has been rainforests and their effect on global climates: is the infilled with volcaniclastic sediment (Figs. 49, past the key to the present? Geobiology 3: 13–31 50). This shows that some of the root cavities were Corda AJ (1845) Flora Protogaea, Beitra¨ge zur Flora open during sedimentation, allowing tuff to enter der Vorwelt. S. Calvary, Berlin and fill void space. The precise cause of this is Cotta B (1832) Die Dendrolithen in Beziehung auf unknown but is most likely taphonomic in origin; ihren inneren Bau. Arnoldische Buchhandlung, in life the root cavities would have been sealed. Dresden, pp 27–36 Dawson JW (1871) The fossil plants of the Devonian and Upper Silurian rocks of Canada. Geol Surv Can Rafael Herbst is thanked for providing reprints on Montreal, pp 1–92 Psaronius from South America, Shao Longyi (CUMT, Dijkstra SJ (1985) Fossilium catalogus II. Plantae Beijing) and Paul Wignall (Leeds University) for (Filicales, Pteridospermales, Cycadales), Pars 91. discussion on the geology of the Xuanwei Formation Ysel Press, Deventer, pp 573–576 and W. Stein and an anonymous reviewer for com- DiMichele WA, Phillips TL (1977) Monocyclic ments on the manuscript. Various aspects of this Psaronius from the Lower Pennsylvanian of the investigation were supported by the National Natural Illinois Basin. Canad J Bot 55: 2514–2524 Science Foundation of China (30670140 to WSJ), The DiMichele WA, Phillips TL (1996) Climate change, Special Fund from the Director of Institute of Botany, plant extinctions, and vegetational recovery during CAS (to WSJ), the Anne Sleep Fund of the Linnean the Middle-Late Pennsylvanian transition: the case Society of London (to JH) and NERC (NE/D011094/1 of tropical peat-forming environments in North to JH), all of which are gratefully acknowledged. America. In: Hart ML (ed) Biotic recovery from mass extinctions, vol 102 reprint. Geological References Society Special Publication, London, pp 201–221 DiMichele WA, Pfefferkorn HW, Gastaldo RA (2001) Ali JR, Thompson GM, Zhou MF, Song XY (2005) Response of Late Carboniferous and Early Permian Emeishan large igneous province, SW China. plant communities to climate change. Annual Rev Lithos 79(3–4): 475–489 Earth Planet Sci 29: 461–487 Allison PA, Pye K (1994) Early diagenetic mineral- Dolianti E (1948) A paleobotanica no Brasil. Bul Div ization and fossil preservation in modern carbonate Geol e Minas (Rio de Janeiro) 123: 1–62 concretions. Palaios 9: 561–575 Falcon-Lang HJ (2006) Latest Mid-Pennsylvanian Andrews HN, Arnold CA, Boureau E, Doubinger J, tree-fern forests in retrograding coastal plain Leclercq S (1970) Filicophyta. In: Boureau E (ed) deposits, Sydney Mines Formation, Nova Scotia, Traite´ de Pale´obotanique. Tome IV (1), Masson et Canada. J Geol Soc Lond 163: 81–93 Cie, Paris, pp 192–201 Fisher QJ, Raiswell R, Marshall JD (1998) Siderite Baird GC, Sroka SD, Shabica CW, Kuecher GJ (1986) concretions from nonmarine shales (Westphalian A) Taphonomy of Middle Pennsylvanian Mazon of the Pennines, England: controls on their growth Creek area fossil localities: significance of excep- and composition. J Sediment Res A68: 1034–1045 tional fossil preservation in syngenetic concretions. Galtier J, Phillips TL (1999) The acetate peel Palaios 1: 271–285 technique. In: Jones TP, Rowe NP (eds) Fossil Blickle AH (1940) Ohio psaronii. Ph.D. Thesis, plants and spores: modern techniques. Geological University of Cincinnati Society of London, London, pp 67–71 Blom CWPM, Voesenek LACJ, Banga M, Engelaar Gillette NJ (1937) Morphology of some American WMHG, Rijnders JHGM, Van De Steed HM, species of Psaronius. Bot Gaz 99: 80–102 Visser EJW (1994) Physiological ecology of river- Grand’Eury FC (1877) Flore Carbonife`re du De´part- side species: adaptive responses of plants to ment de la Loire et du Centre de la France. Acad submergence. Ann Bot 74: 263–263 Sci Inst Fr Me´m 24: 1–624 X.-Y. He et al.: Anatomically preserved marattialean plants 179

Gu et Zhi (1974) Fossil plants of China, 1. Chinese Li Y-J (1987) Studies of the tree fern-Psaronius Cotta in palaeozoic plants. Science Press, Beijing, (in the Xuanwei Formation, Pan County of Guizhou Chinese) Province. M.Sc. Thesis, China University of Mining Guo YT, Tian BL, Han DX (1992) Anatomical study and Technology (in Chinese with English abstract) of the rachis of Compsopteris elliptica and the Li C-S, Cui J-Z (1995) Atlas of fossil plant anatomy systematic position of Compsopteris. Acta Bot Sin of China. Science Press, Beijing 34: 630–633 Liu Z-H, Hilton J, Li C-S (2000) Review of the origin, Hatae N (1931) A new Caulopteris from the Wu-Hu- evolution and phylogeny of Marattiales. Chin Bull Tsui coalfield of South Manchurica, Caulopteris Bot 17: 39–52 manchuriensis sp. nov. Japan J Geol Geogr 9: 9–12 Liu ZH, Li CS, Hilton J (2001) Fertile pinnules of He X-L, Sun B-N (1998) On discovery of the genus Danaeites rigida Gu et Zhi (Marattiales) from the Caulopteris from the Lower Permian in western Upper Permian of south China. Bot J Linn Soc 136: Henan, China. Acta Palaeontol Sin 37: 257–260 107–117 Herbst R (1985) Nueva descripcion de Psaronius Ma S-M (1985) Studies of the tree fern-Psaronius arrojadoi (Pelourde) (Marattiales). Del Permico de Cotta in the coal balls of Taiyuan Formation, Brasil, pp 243–258 Xishan Coal Field, Shanxi Province. M.Sc. Thesis Herbst R (1986) Studies on Psaroniaceae. I. The of China University of Mining and Technology (in family Psaroniaceae (Marattiales) and a redescrip- Chinese with English abstract) tion of Tietea singularis Solms-Laubach, from the Mickle JE (1984) Taxonomy of specimens of the Permian of Brazil. Actas IV Congreso Argentino Pennsylvanian-age marattialean fern Psaronius Paleontologia y Bioestratigrafia 1: 163–171 from Ohio and Illinois. Ill State Mus Sci Paper Herbst R (1987) Studies on Psaroniaceae. II. Tuvicha- 19: 1–64 pteris solmsi nov. gen. et sp. from the Permian of Morgan J (1959) The morphology and anatomy of Paraguay and Uruguay. Actas IV Congr Latinoamer American species of the genus Psaronius. Ill Biol Paleont, Santa Cruz de la Sierra, Bolivia 1: 267–282 Monogr 27: 1–108 Herbst R (1999) Studies on Psaroniaceae. IV. Two Ogura Y (1972) Psaronius from Linggiu, Johore, species of Psaronius from Araguaina, State of Malaya. Geol Palaeontol Southeast Asia 10: 117– Tocantins, Brazil. Facena 15:9–17 124 Hilton J, Cleal CJ (2007) The relationship between Pelourde F (1912) Observations sur le Psaronius Euramerican and Cathaysian tropical floras in the brasiliensis. Ann Sci Nat Bot 9Se´rie 16: 337–352 Late Palaeozoic: palaeobiogeographical and palae- Pfefferkorn HW (1976) Pennsylvanian tree fern ogeographical implications. Earth Sci Rev 85: 85– compressions Caulopteris, Megaphyton and Artis- 116 ophyton gen. nov. in Illinois. Ill State Geol Surv Hilton J, Wang S-J, Galtier J, Glasspool IJ, Stevens L Circ 492: 1–31 (2004) A Late Permian permineralized plant Rothwell GW (1999) Fossil ferns in the resolution of assemblage in volcaniclastic tuffs from the Xuan- land plant phylogeny. Bot Rev 65: 188–218 wei Formation, Guizhou Province, China. Geol Rothwell GW, Blickle AH (1982) Psaronius magni- Mag 141: 661–674 ficus n. comb., a marattialean fern from the Upper Hirmer M (1927) Handbuch der Paleobotanik. R. Pennsylvanian of North America. J Paleontol 56: Oldenbourg, Munich 459–468 Jongmans W, Dijkstra SJ (1963) Fossilium catalogus II. Shao L, Zhang PF, Ren D, Lei JJ (1998) Late Permian Plantae (Filicales, Pteridospermales, Cycadales), coal-bearing carbonate successions in southern vol 28, pars 55. Ysel Press, Deventer, pp 2594–2621 China: coal accumulation on carbonate platforms. Lesquereux L (1880) Description of the coal flora of Int J Coal Geol 37: 235–256 the Carboniferous formation in Pennsylvania and Shen G (1995) Permian floras. In: Li XX (ed) Fossil throughout the United States, vols I and II. Second floras of China through the geological ages Geol Surv of Pennsylvania (Harrisburg), Rept Prog, (English edition). Guangdong Science and Tech- pp 1–694 nology Press, Guanzhou, pp 127–223 Li X-X (1963) Fossil plants of the Yuemenkou Series, Stenzel G (1906) Die Psaronien, Beobachtungen und North China. Palaeontol Sin New Ser A (Whole ser. Betrachtungen. Beitr Palaeontol Geol Oesterreich- No. 148) 6: 1–185, (in Chinese with English abstract) Ungarns Orients 19: 85–123 180 X.-Y. He et al.: Anatomically preserved marattialean plants

Stewart WN, Rothwell GW (1993) Palaeobotany and Williamson WC (1876) On the organization of the the evolution of plants, 2nd ed. Cambridge Uni- fossil plants of the coal measures. Part VII. versity Press, Cambridge Myelopteris, Psaronius and Kaloxylon. Philos Stidd BM (1971) Morphology and anatomy of the Trans Roy Soc Lond 166: 1–25 frond of Psaronius. Palaeontographica_Abt.B 134: Yang Z-C (1986) A new species of the genus 87–123 Psaronius Cotta from Yunan Province, China. Sun KQ, Deng SH (1999) Discovery and significance Geol China 21: 30 of the genus Caulopteris from the Wuda area of Yao Z-Q, Xu J-T, Zheng Z-G, Zhao X-H, Mo Z-G Inner Mongolia. Acta Bot Sin 41: 484–486 (1980) On the biostratigraphy of the Permian and Sze HC (1942) U¨ ber ein neues Exemplar von the boundary between the Permian and Triassic in Psaronius aus dem Omeishan Basalt in Weining western Guizhou-eastern Yunnan. In: Academia (Kueichou) mit besonderer Beru¨cksichtigung des Sinica (eds) Nanjing Institute of Geology and Alters des Basaltes in Su¨dwestchina. Bull Geol Soc Palaeontology. Late Permian coal bearing strata China 22: 105–131 and biota from western Guizhou and eastern Sze HC (1947) On the structures of Psaronius sinensis Yunnan. Science Press, Beijing, pp 1–69 (in from the Omeishan Basalt Series in southwestern Chinese) China. Geol J Amer 55: 160–167 Yao Z-Q, Liu L-J, Li C-D (1994) Psaronii of Tian B-L, Zhang L-W (1980) Fossil atlas of Wan- Gigantopteris-Flora from Jiangsu, China. Acta gjiazhai mine region in Shuicheng, Guizhou. Coal Palaeontol Sin 33: 604–619 Industry Press, Beijing (in Chinese) Zeiller R (1890) Etudes des Gıˇtes Mine´raux de la Tian B-L, Wang S-J (1995) Paleozoic coal ball floras France-Basin Houiller et Permian d’Autun et in China. In: Li X-X (ed) Fossil floras of China d’Epinac, Fasc. 2, Flore fossile through the geological ages (English edition). Zhao H (1990) Late Permian Flora in eastern Yunnan Guangdong Science and Technology Press, and division and correlation of Xuanwei Forma- Guangzhou, pp 202–211 tion. Unpublished M.Sc. Thesis, China University Tian B-L, Li Y-J, Guo Y-T (1992) On the study of of Mining and Technology Psaronius wangii (sp. nov.) from Xuanwei Forma- Zhao X-H, Mo Z-G, Zhang S-Z, Yao Z-Q (1980) Late tion of Pan Xian, Guizhou. In: Li Zhong-Li (ed) Permian flora from western Guizhou and eastern Collected works for memory of the 100 anniversary Yunnan. In: Academia Sinica (eds) Nanjing Insti- of the Birthday of Dr Wang Zhu-Quan. Coal tute of Geology and Palaeontology, Late Permian Industry Press, Beijing, pp 74–78 & 3 pls (in coal bearing strata and biota from western Guizhou Chinese) and eastern Yunnan. Science Press, Beijing, pp 70– Tian B-L, Wang S-J, Guo Y-T, Chen G-R, Zhao H 122 (in Chinese) (1996) Flora of Palaeozoic coal balls in China. Zhu J-N, Hu Y-F, Li Z-J (1984) Upper Permian plants Palaeobotanist 45: 247–254 of Junlian area, south Sichuan. In: Editorial Com- Wang SJ, Hilton J, Liang MM, Stevens L (2006) mittee of Professional Papers of Stratigraphy and Permineralized seed plants from the Upper Permian Palaeontology, Chinese Academy of Geological of southern China: a new species of Cardiocarpus. Sciences (eds) Professional papers of stratigraphy Int J Pl Sci 167: 1247–1257 and palaeontology, vol 11. Geological Publishing Wignall PB (2001) Large Igneous Provinces and mass House, Beijing, pp 133–147 (in Chinese) extinction. Earth Sci Rev 53: 1–33