Rhabdoxylon taiyuanense n. sp.: A new botryopterid fern from the Lower Permian of Shanxi Province, North China

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Rhabdoxylon taiyuanense n. sp.: A new botryopterid fern from the Lower Permian of Shanxi Province, North China Jing Ma a , Shi-Jun Wang b,c,∗ , Ke-Qin Sun a a

b

School of Earth Sciences and Resources, China University of Geosciences, Beijing 100083, PR China State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, PR China c State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, PR China Received 30 November 2015; received in revised form 15 March 2016; accepted 4 May 2016

Abstract This paper described a new early leptosporangiate fern occurring in the Lower Permian coal balls from Shanxi Province, North China. The fossil materials include stems, attached and detached petioles and roots, belonging to a same kind of plant. Stems are relatively small in diameter and branch dichotomously. They possess a haplostele with metaxylem tracheids decreasing outward in diameter and showing uniseriate scalariform thickenings. There are no distinguished protoxylem groups in the xylem cylinder. Cortex is parenchymatous and can be divided into three zones according to cell size. Petiolar traces bear different shapes in cross section and show a spiral diverging sequence. Petioles are circular in cross section and cortical cells are much smaller than those of stems. Petiolar traces and petioles possess a single protoxylem group at the adaxial side of the xylem strand. Root traces originate from the cauline stele and go through the cortex in a way perpendicular or oblique to the cauline stele. These characters show great similarities to the genus Rhabdoxylon but are not consistent with its any known species, so it is necessary to create a new species Rhabdoxylon taiyuanense n. sp. for the present plant. The new species probably possesses an upright habit. This is the first report of the existence of the genus Rhabdoxylon in the Cathaysian Flora. The discovery of a new type of the Palaeozoic leptosporangiate fern in China has led to reevaluation of the systematic relationships among species of the Botryopteridaceae. © 2016 Published by Elsevier B.V. on behalf of Nanjing Institute of Geology and Palaeontology, CAS. Keywords: Permian; Taiyuan Formation; Coal ball; Botryopterid fern; Anatomy; Rhabdoxylon taiyuanense n. sp.

1. Introduction Willamson (1878) originally reported, while studying fossil plants in coal balls of the Late Carboniferous (Westphalian A) from England, a sort of fern stem and named it as Rachiopteris cylindrica Williamson. Bancroft (1915) further studied this plant and considered that it could be divided into two types, type ␣ and type ␤. Later these two types were elevated to the generic level after further observations on the specimens of Rachiopteris cylindrica Williamson by Holden (1960), Psalixochlaena for

∗ Corresponding author at: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, PR China. Tel.: +86 10 62836523. E-mail address: [email protected] (S.J. Wang).

type ␣ and Rhabdoxylon for type ␤. Both of them were assigned to the family Botryopteridaceae Renault in previous studies, but now Psalixochlaena has been considered as an independent family, Psalixochlaenaceae (Holmes, 1977, 1981) for the reason that the vegetative and reproductive structure of Psalixochlaena are different from the members of Botryopteridaceae. Rhabdoxylon is still included in Botryopteridaceae (Taylor et al., 2009). The genus Rhabdoxylon is a small early leptosporangiate fern with a simple and isotomic dichotomous stem containing a rodshaped protostele and a single protoxylem strand at the adaxial side of the xylem strand of petiole and rachis (Holden, 1960). There are only two species in this genus at present. The type species Rhabdoxylon dichotomum was erected based on specimens from the Lower Pennsylvanian (Westphalian A) coal balls in England (Holden, 1960). Later a more detailed study of the plant was done by Holmes (1979) who examined the specimens

http://dx.doi.org/10.1016/j.palwor.2016.05.002 1871-174X/© 2016 Published by Elsevier B.V. on behalf of Nanjing Institute of Geology and Palaeontology, CAS.

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in British and Belgian coal balls of same horizon and made a reconstruction. Another species, Rhabdoxylon americanum, was described from the Upper Pennsylvanian of North America (Dennis, 1968). Now the knowledge about the genus Rhabdoxylon is only based on the stems, petioles, rachides, and roots, but nothing is known about its leaves and fertile parts. The condition is very different in Botryopteris Renault, a common botryopterid fern, because its vegetative and fertile parts are well known. The studies of the early leptosporangiate ferns in the Cathaysian Flora are fewer than those of the Euramerican Flora and only some rachides of these ferns were simply reported. Hilton et al. (2001) reported isolated rachides of genus Botryopteris, which are suggestive of the species B. tridentata Renault. These specimens are preserved in tuffitic sediments with the age of the Early Permian from the Taiyuan Formation of Yangshuling mine in Hebei Province, North China. Furthermore, several pinnae of Anachoropteris sp. were reported in an Upper Permian permineralized plant assemblage preserved in volcaniclastic tuff from the Xuanwei Formation, Guizhou Province, southern China (Hilton et al., 2004). In addition, Botryopteris sp. 1, B. sp. 2, Anachoropteris cf. clavata Graham and Etapteris cf. scottii Bertrand were described by Wang et al. (2009) based on specimens in coal balls collected from No.7 coal seam of the Taiyuan Formation in the Xishan Coalfield, Taiyuan, Shanxi Province, North China. Thus, the findings of the Palaeozoic leptosporangiate taxa in China are very rare and have not been well studied. Moreover, nothing is known about the stems and fertile organs of the early leptosporangiate ferns in the Cathaysian Flora. Botryopterid ferns of the Carboniferous are various in taxa and have been well studied (Galtier and Phillips, 1996; Taylor et al., 2009). In contrast the findings of the Permian aged botryopterid ferns are much fewer and only one species, Botryopteris nollii Rößler et Galtier, has been more extensively investigated (Rößler and Galtier, 2003). Thus the Permian aged botryopterid ferns in the Cathaysian Flora will be of great significance in studying the taxonomic diversity, ecological adaptation and evolution of these ferns. This paper is to present a detailed study on a new botryopterid plant from the coal ball of the Early Permian Taiyuan Formation in Shanxi Province, North China. The plant has a haplostelic stem with attached or detached petioles and is very similar in many respects to the genus Rhabdoxylon, but it has several unique features that are different from two existing species, which leads to the creation of a new species, Rhabdoxylon taiyuanense n. sp. It is the first report on the genus Rhabdoxylon in the Permian strata of the world and from the Cathaysian Flora. 2. Materials and methods This study focuses mainly on three stems numbered as Stem 1 (S1), Stem 2 (S2), and Stem 3 (S3). These stems have been found in a single coal ball (numbered as 72009) from No.7 coal seam of Xishan Coalfield in the upper part of the Taiyuan Formation in Taiyuan, Shanxi Province, North China. This formation is a paralic deposit. Coal balls from this locality are the Early Permian in age according to the Chinese stratigraphic system (Wang,

Fig. 1. Rhabdoxylon taiyuanense n. sp. Camera-lucida drawings of selected acropetal serial cross sections (from A36 to A17) of Stem 1 (S1) showing the spiral divergence of petiolar traces. Note a slight increase upward in size of the stem. Root trace in black; petiolar trace in gray. Five petiolar traces are involved.

1989, 2010; Tian et al., 1996). In the past years these coal balls have yielded abundant fossil plants with the anatomical structure (Wang et al., 2009). The coal ball was prepared by the well-known cellulose acetate peel technique (Joy et al., 1956; Galtier and Phillips, 1999). The three stems were revealed by three parallel cut surfaces named as A, B, and C. B and C are opposite and about 3 mm apart. A is about 7 mm apart from B. In order to reveal the extension of stems and the arrangement of petioles on the stem, serial peels have been made on these cut surfaces. Totally, 38 peels (numbered A1 to A38) have been obtained from the surface A, 19 peels (numbered B1 to B19) from the surface B, and 6 peels (numbered from C1 to C6) from the surface C. The change of stem morphology through its length was reconstructed from a series of closely spaced serial sections and some of them were shown in Figs. 1 and 2 by camera-lucida drawings. The slides were observed and photographed using a Nikon microscope under transmitted light with a Nikon 4500 digital camera throughout the work. The plates are processed using CorelDRAW 16.0 and Adobe Photoshop CS 6. Peels and slides of illustrated specimens are stored in the National Museum of

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branching and longitudinal sections of stem (Figs. 3D–F, 4E, F, 5F, 6A, B, E). Repository: The holotype and paratype (peels: 72009–A1 to A38, B1 to B19, C1 to C6; slides: WP11–0214, 0424 to 0443) are stored in the National Museum of Plant History of China, Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing, China. Type locality: Xishan Coalfield in Shanxi Province, North China. Geological horizon: No. 7 coal seam, the upper part of the Taiyuan Formation. Age: Asselian–early Sakmarian; the Early Permian. Diagnosis: Stem up to 6 mm or more in diameter with stele up to 1.75 mm in diameter. No distinct protoxylem groups present in the stele. Tracheid diameter decreasing outward with largest ones up to 50 × 80 ␮m. Tracheids with uniseriate scalariform thickenings. Cortex differentiated into three zones with their cells all longitudinally elongated. Inner cortex narrow with cells tangentially elongated in cross section. Middle cortex with cells about 30–50 ␮m in diameter, while outer cortex with larger cells about 60 × 80 ␮m–70 × 150 ␮m in diameter. Petiole up to 900 ␮m in diameter with flattened xylem strand tangential to the stem surface and with cortex cells much smaller than those of the stem. A single protoxylem group located at the adaxial side of the xylem strand of petiolar traces and petioles, but not forming distinct ridges. Adventitious roots originating from the periphery of the cauline stele, up to 350 × 600 ␮m in diameter with cortical cells thick-walled. 4. Description 4.1. Stem

Fig. 2. Rhabdoxylon taiyuanense n. sp. Camera-lucida drawings of selected acropetal serial cross sections (from A36 to A22) of Stem 2 (S2) showing the isotomous dichotomy of the stem.

Plant History of China, Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing, China.

4.1.1. Stem morphology S1 has a preserved length of about 11 mm with a diameter of about 2.5 × 3.5 mm for most part (Figs. 1, 3A, B) except for the distal end, which has a diameter up to 5.5 × 9 mm (Fig. 3C). S2 has a slightly longer preserved length, 16 mm, than S1 with a uniform diameter, about 4–5 mm. S2 undergoes one isotomous dichotomy (Figs. 2, 3D–F) in the preserved length. S3 is about 4–5 mm in diameter without dichotomy.

3. Systematic palaeobotany Subdivision Euphyllophytina (sensu Crane and Kenrick, 1996) Family Botryopteridaceae Renault, 1883 Genus Rhabdoxylon Holden, 1960 Type species: Rhabdoxylon dichotomum Holden, 1960. Rhabdoxylon taiyuanense n. sp. (Figs. 1–7) Etymology: The specific name is after the fossil locality Taiyuan City. Types: Holotype: Stem 1 (S1) which exhibits well preserved cross sections of stem and attached petioles (Figs. 3A–C, 4A–D, 5A–E). Paratype: Stem 2 (S2) which exhibits dichotomous

4.1.2. Stem anatomy Stems are nearly circular (Fig. 3A, B) in cross section. However, they could be oval-shaped due to the emission of a petiole (Fig. 3C, D), dichotomy (Fig. 3E) or the compression of the rocks. In the last case the stems are usually with a deformed outline (Fig. 3F). In the center of the stem there is a nearly circular (Figs. 3A, 4A, C, 5B) or elliptical (Figs. 3B–F, 4B, 5A, C) haplostele, which consists of a xylem cylinder and poorly developed phloem. The xylem cylinder is full of tracheids without parenchyma (Fig. 4C). The diameter of xylem cylinder in S1 is about 0.5 × 0.6 mm for the most part but at the distal part it reaches 1 × 1.375 mm (Fig. 3C). In S2 the diameter of the xylem cylinder is about 0.9 × 1.5 mm before the dichotomous branching of the stem (Fig. 3D), but decreases to 0.68 × 0.9 mm after branching (Fig. 3E, F). There are no distinguished protoxylem

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Fig. 3. Rhabdoxylon taiyuanense n. sp. Cross sections of the Stem 1 (A–C) and Stem 2 (D–F) at different levels. All scale bars = 1 mm. (A) Basal part of the Stem 1 with a petiole (P) which has just departed from the stem and a root trace (RT) in the cortex (C) of the stem; Slide WP11–0433. (B) Middle part of the Stem 1 with one petiolar trace (PT) and a petiole diverging from the stem at a nearly right angle to the stem (arrowed); Slide WP11–0427. (C) Upper part of Stem 1 with a larger diameter, showing a petiolar trace (PT) is diverging from the stele (St) at a nearly right angle; the arrow indicates an incipient petiolar trace; Slide WP11–0424. (D) Basal part of the Stem 2 with a stele (St) which is going to dichotomy; note a petiolar trace (PT) in the cortex (C) of the stem and a petiole (P) adhering to the stem; Slide WP11–0439. (E) Middle part of the Stem 2 showing two daughter steles (St) which are produced by equal dichotomous branching and enclosed by the common cortex (C); the red arrows indicate the radially elongated cortical cells with thick walls; Slide WP11–0435. (F) Upper part of the Stem 2 showing two daughter stems which have their own cortex (C) except a small part (arrowed) which connects the both; Slide WP11–0431.

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Fig. 4. Rhabdoxylon taiyuanense n. sp. Enlargements of the stems to show the details. Note the dark colored inner cortex (IC) for containing fungal hyphae. (A–D) in cross section; (E, F) in longitudinal section. (A) Enlargement of Fig. 3A showing the structure of the stem and petiole (P); arrow indicates the tangentially elongated petiolar xylem strand; Slide WP11–0433; scale bar = 0.5 mm. (B) Enlargement of Fig. 3B noting a diverging tangentially elongated petiolar trace (PT); Slide WP11–0427; scale bar = 0.5 mm. (C) Enlargement of A showing details of the cauline stele (St); note the incipient petiolar trace (IPT) adaxial to which there are several layers of tangentially elongated thin-walled cells (arrowed); Slide WP11–0433; scale bar = 100 ␮m. (D) Periphery of the cauline stele showing the phloem (Ph) and xylem (X); note a diverging tangentially elongated petiolar trace (PT); Slide WP11–0430; scale bar = 100 ␮m. (E) From right to left showing the xylem (X) and phloem (Ph) of cauline stele and inner cortex (IC); note the uniseriate scalariform thickenings on metaxylem tracheid walls; Slide WP11–0443; scale bar = 50 ␮m. (F) Details of the inner cortex showing fungal hyphae (arrowed) in cells; Slide WP11–0443; scale bar = 50 ␮m.

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Fig. 5. Rhabdoxylon taiyuanense n. sp. (A–C) Three acropetal successive cross sections of Stem 1 (S1) showing the forming of a petiolar trace. (A) The lower level showing the petiolar trace in the incipient stage and is united with the cauline stele; note that no distinct protoxylem group is associated with this incipient petiolar trace (IPT); Slide WP11–0430; scale bar = 0.5 mm. (B) The level slightly higher than (A) showing that the incipient petiolar trace (IPT) is now about to depart from the cauline stele and several layers of tangentially elongated thin-walled cells (arrowed) is located to its adaxial side; two root traces (RT) are departing from the cauline stele; Slide WP11–0429; scale bar = 200 ␮m. (C) The level higher than (B) showing that the petiolar trace (PT) has departed from the cauline stele (St); Slide WP11–0428; scale bar = 200 ␮m. (D–F) Petiolar traces in the cortex of the stem with different cross sectional shapes. (D) A cuneiform petiolar trace in the outer cortex of the stem with its adaxial side downward; Slide WP11–0427; scale bar = 200 ␮m. (E) A semi-circular petiolar trace with a single protoxylem group (arrowed) at its adaxial side; Slide WP11–0425; scale bar = 100 ␮m. (F) Petiole base at the periphery of the stem showing the semi-circular shaped xylem strand of the petiolar trace (PT); comparing the outer cortex of the stem with larger cells (C1) and the cortex of petiole base with much smaller cells (C2); Slide WP11–0425; scale bar = 0.5 mm.

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Fig. 6. Rhabdoxylon taiyuanense n. sp. (A) Enlargement of Fig. 5F showing small protoxylem tracheids forming a tangential band (arrowed) at the adaxial side of the xylem strand (X) of the petiolar trace; Slide WP11–0425; scale bar = 100 ␮m. (B) Another petiolar trace of the petiole base with semi-circular xylem strand (X); Slide WP11–0427; scale bar = 100 ␮m. (C) A free petiole in cross section with a tangentially elongated xylem strand (X) with a protoxylem group at its adaxial side (arrowed); Slide WP11–0435; scale bar = 100 ␮m. (D) Another free petiole in cross section with a tangentially elongated xylem strand (X); Slide WP11–0440; scale bar = 200 ␮m. (E) Cross section of a root trace showing its dark colored cortex (C) because of thick-walled cells; Slide WP11–0424; scale bar = 100 ␮m. (F) Cross section of a free root showing its cortex (C) consisting of tangentially elongated cells; Slide WP11–0442; scale bar = 50 ␮m.

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Fig. 3E). Epidermal cells are small and irregular in shape with the diameter of about 30 × 40 ␮m. In longitudinal section of the stem, cells of the inner, middle, and outer cortex are all longitudinally elongated with the length of up to 100 ␮m for the inner cortex (Fig. 4E, F), 150 ␮m for the middle cortex, and 300 ␮m or more for the outer cortex. 4.2. Petiolar trace and petiole

Fig. 7. Rhabdoxylon taiyuanense n. sp. A diagrammatic reconstruction of the stem with attached petioles and roots.

groups in the xylem cylinder (Figs. 4B, C, 5A–C). Tracheids are isodiametric in shape in cross section. Large tracheids usually occupy the center of the xylem cylinder with the diameter measuring from 40 × 60 ␮m to 50 × 80 ␮m and the diameter of tracheids decreases to 20 × 30 ␮m at the margin of the xylem cylinder (Fig. 4C). There are uniseriate scalariform thickenings on longitudinal tracheid walls (Fig. 4D). A narrow and usually discontinuous band of thin-walled cells, possibly phloem, is present at the periphery of the xylem cylinder. The cells of phloem are usually 15–25 ␮m in diameter and smaller than tracheids of xylem (Fig. 4D). In the longitudinal section the cells of the phloem are elongated (Fig. 4E). The cortex of the stem are parenchymatous and can be divided into three zones; inner cortex, middle cortex, and outer cortex (Fig. 4A, B). The inner cortex is 90 to 150 ␮m or 3 to 4 (occasionally 2 or 5) cells wide. Cells are nearly isodiametric or tangentially elongated with the diameter of 25–35 ␮m in cross section and compactly arranged (Fig. 4D). Many of these cells contain abundant fungal hyphae (Fig. 4E, F), which make the zone in dark color (Fig. 5A–C). The middle cortex is about 200 to 400 ␮m or 6 to 9 cells wide. The cells are isodiametric with the diameter ranging from 30 to 50 ␮m and more or less loosely arranged (Figs. 4A–D, 5A–C). The outer cortex has a variable width ranging from 0.7 to 1.5 mm but mostly more than 1 mm, which accounts for about 3/4 of the entire cortex width (Fig. 4A). It consists of large and usually isodiametric cells with the diameter of 60 × 80 ␮m to 70 × 150 ␮m. Cells with thicker walls and radially elongated shape can be seen somewhere (arrows in

Petiolar traces are originated from a group of tracheids at the outer part of the cauline xylem cylinder and no distinct protoxylem groups are present. This tracheid group is the incipient petiolar trace that could be as wide as 400–500 ␮m in tangential direction (Figs. 4C, 5A). Between the incipient petiolar trace and the cauline xylem cylinder, there are 2 to 3 layers of tangential elongated thin-walled cells that probably are phloem (Figs. 4C, 5B). When petiolar traces enter the cauline cortex they could exhibit different cross-sectional shapes. Some of them are flattened or lens-shaped with slightly convex adaxial and abaxial sides with a much larger tangential dimension (8–10 tracheids or 320 ␮m) than the radial one (4–5 tracheids or 130 ␮m) (Figs. 4B, D, 5A). Others, however, are cuneiform (Fig. 5D) or somewhat semi-circular (Fig. 5E) with a convex adaxial side and a flat abaxial side. One protoxylem group can be seen on the adaxial side of some petiolar traces (Fig. 5E). In the petiole base the trace is typically semi-circular with a convex adaxial side and a flat or even slightly concave abaxial side (Figs. 5F, 6A, B). Petiolar traces diverge in a spiral sequence and in a single cross section of the cauline cortex three petiolar traces can be seen at most. In a length of 11 mm in Stem 1 (S1), six petiolar traces have been revealed, so that the intermodal length of the stem could be about 2 mm. Petioles are circular or elliptical in cross section (Figs. 3A, 4A, 6C, D). Their diameters range from 0.7 mm to 1.5 mm, which is much smaller compared with those of stems. Some petioles are at a very small angle with the stem (Figs. 3A, 4A), but others are at a very big angle and almost perpendicular to the stem (Fig. 3B). The vascular strand of the petiole is usually tangentially elliptical with the size of about 250 × 300 ␮m and the xylem strand is conspicuously tangentially elongated with a convex adaxial side and a flat or slightly convex abaxial side. Small tracheids form a tangential band on the adaxial side (Fig. 6C, D). The largest metaxylem tracheids are up to 50 × 75 ␮m in diameter and possess uniseriate scalariform thickenings on the walls. The cortex of petiole consists of inner cortex and outer cortex. The inner cortex, connected to that of the stem, is 2 to 3 cells or 50–100 ␮m wide with cells tangentially elongated and mostly also filled with fungal hyphae. The outer cortex is about 300 to 400 ␮m in width and cells are 30–40 ␮m in diameter, much smaller than those of the stem (Fig. 4A). 4.3. Root traces and free roots Root traces depart from the periphery of the cauline stele and extend outwardly through the stem cortex in a course perpendicular to (Figs. 3C, E, 5B, C) or oblique with the cauline

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stele (Figs. 3A, B, 5B). There is not any root trace, or there are 1 to 3 root traces, in a single cross section of the stem cortex. The shapes of the root traces in cross section are round to oval (Fig. 6E). Root traces measure from 350 × 600 ␮m to 450 × 700 ␮m in diameter and have a diarch protostele with the diameter about 125 to 130 ␮m. Tracheids of the metaxylem are small, up to 25 ␮m in diameter. Root traces have an independent cortex once it has diverged from the cauline stele. The cortex of root traces is 5–7 cells or 120–180 ␮m in width and consists of thick-walled cells that are nearly isodiametric in cross section (Fig. 6E) and elongated in longitudinal section. Around stems there are free roots which usually have an oval crosssectional shape with a diameter ranging from 250 × 360 ␮m to 300 × 450 ␮m. The cortex is similar to that of root traces except that cells of the free roots are usually tangentially elongated and with thinner walls (Fig. 6F).

5. Discussion The present stems are small (several millimeters in diameter) and possess a solid protostele (or haplostele) with no more than 3 petiolar traces in each cross section of the cortex and the bilaterally symmetrical petiolar xylem strand, which fall into the category of certain Palaeozoic leptosporangiate ferns such as Botryopteridaceae, Anachoropteridaceae, Psalixochlaenaceae, and Kaplanopteridaceae. There are three anatomically preserved genera in Botryopteridaceae, including Botryopteris Renault (the type genus of the family), Rhabdoxylon Holden, and Catenopteris Phillips et Andrews. Botryopteris contains 11 anatomically preserved species up to date and has a long evolutionary history, from Visean of the Early Carboniferous to Permian (Rößler and Galtier, 2003). The advanced or geologically younger species of the genus is characterized by possessing a conspicuously adaxially curved ␻-shaped xylem strand in petiole and rachis with three protoxylem groups on the adaxial side, such as B. cratis Millay et Taylor (Millay and Taylor, 1980), B. tridentata Renault (Phillips, 1970, 1974; Rothwell and Good, 2000), B. forensis Renault (Galtier and Phillips, 1977) and B. nollii Rößler et Galtier (Rößler and Galtier, 2003). However, the xylem strand in petiole and rachis is slightly adaxially curved with one to three protoxylem groups on the adaxial side in the primitive or geologically elder species, such as B. antiqua Kidston (Phillips, 1970, 1974), B. hirsuta (Will.) Scott and B. ramosa (Will.) Scott (Phillips, 1970, 1974; Holmes, 1984), B. dichotoma Holmes et Galtier and B. mucilaginosa Kraentzel (Kraentzel, 1934; Holmes and Galtier, 1983), and B. scottii Holmes (Holmes, 1984). The stem of Botryopteris is usually not dichotomously branching and possesses epiphyllous shoots, but only except for B. dichotoma and B. mucilaginosa which are dichotomously branching and without epiphyllous shoots (Holmes and Galtier, 1983). The cortex of the stem in Botryopteris is usually bi-zoned with the outer cortex consisting of thick-walled cells and the pitting pattern on the metaxylem tracheid walls is complicated, from scalariform thickenings to reticulated and even bordered pitting (Phillips and Andrews, 1966).

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Rhabdoxylon has a small equally dichotomously branching and haplostelic stem with parenchymatous cortex. Petiole and rachis xylem is round or oval in cross section with a single adaxial protoxylem group (Holden, 1960; Dennis, 1968; Holmes, 1979). Catenopteris, containing only a single species C. simplex Phillips et Andrews, is characterized by the slightly adaxially curved xylem strand of the petiole, parenchymatous cortex, a mass of lens-shaped parenchyma adaxial to the incipient petiolar trace, simple uniseriate scalariform thickenings on metaxylem tracheid walls, one root trace associated with a diverging petiolar trace, and no distinct protoxylem group in the cauline stele (Phillips and Andrews, 1966). The stems of Anachoropteridaceae, Psalixochlaenaceae, and Kaplanopteridaceae all, except for Psalixochlaena Holden, produce conspicuously abaxially curved petiolar trace and xylem strand of the petiole (Morgan and Delevoryas, 1954; Tomescu et al., 2006; Galtier and Phillips, 2014). In Psalixochlaena the xylem strand of the petiole base is flattened or lens-shaped and not curved, but it becomes conspicuously abaxially curved distally (Holmes, 1977). Moreover, the stem of Psalixochlaena is extensively branched, either dichotomously or laterally and the protostele has a central zone of small tracheids surrounded by zone of larger tracheids and 1–4 protoxylem groups situated at junction of two zones (Holmes, 1977, 1981; Taylor et al., 2009; Galtier and Phillips, 2014). Compared with the taxa mentioned above, the present stems demonstrate similarities with the genus Rhabdoxylon by their equally dichotomously branching stem, parenchymatous cortex and a single protoxylem group on the adaxial side of the petiolar xylem strand. The present stems also resemble Catenopteris in several aspects, such as parenchymatous cortex, simple uniseriate scalariform thickenings on tracheid walls and no distinct protoxylem groups in the cauline stele. In contrast, there are few similarities between the present stems and Botryopteris of Botryopteridaceae and other families. The cross sectional shape of the xylem strand of petiole and rachis is a diagnostic feature in the taxonomy of the Palaeozoic leptosporangiate ferns. The petiolar xylem strand of the present stems is tangentially elongated and not curved adaxially or abaxially, which is more similar to that of Rhabdoxylon whose petiolar xylem strand is oval or round than to that of Catenopteris whose petiolar xylem strand is slightly adaxially curved. As a result we assign the present stems to the genus Rhabdoxylon. There are two species, R. dichotomum Holden and R. americana Dennis, included in the genus Rhabdoxylon at present. They are easy to be distinguished from the present stems by the cross sectional shape of the petiolar xylem strand, the protoxylem groups in the cauline stele and the structure of the cortex (Table 1). The petiolar xylem strand of R. dichotomum and R. americana is oval or round, whereas in the present stems it is flattened or tangentially elongated. In R. dichotomum there are two protoxylem groups in the protostele, one is persistent in the stem and the other is associated with the forming of the petiolar trace. In R. americana there is only one protoxylem group in the protostele which is associated with the forming of the petiolar trace. However, in the present stems no distinct protoxylem

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Table 1 Comparison of three species of Rhabdoxylon. Species

R. dichotomum

R. americanum

R. taiyuanense n. sp.

Age and location

Lower Pennsylvanian; England and Belgium 1.8–2.1 0.35–0.5 Bi-zoned Present Round to ovoid Holden (1960), Holmes (1979)

Upper Pennsylvanian; Southern Illinois 2–4 0.33–0.5 Bi-zoned Present Round to ovoid Dennis (1968)

Lower Permian; Shanxi Province, North China 3–6 or more 0.5–1.375 Tri-zoned Absent Bar-shaped This paper

Diameter of stem (mm) Diameter of stele (mm) Cortex Protoxylem strand in the stele Petiolar xylem Reference

groups are present in the cauline stele. It is undoubted that the present stems represent a new species of the genus Rhabdoxylon and the specific name R. taiyuanense is suggested for the new species (Fig. 7). When Holden (1960) erected the genus Rhabdoxylon, he also diagnosed it as “stem densely clothed with unbranched multicellular hairs, cortex entirely parenchymatous consisting of an inner zone with abundant intercellular spaces and an outer zone without intercellular spaces” in addition to the other features mentioned above. Holmes (1979), when making a further observation on specimens of R. dichotomum in coal balls from Belgium and England, pointed out that the intercellular spaces are only present in the less well preserved stems which seem to indicate decomposition rather than a natural feature. In R. americana, the intercellular spaces are not present in the cortex (Dennis, 1968). Therefore the intercellular spaces in the cortex should not be taken as a generic feature of Rhabdoxylon. In R. taiyuanense n. sp., the intercellular spaces have also not been observed in the cortex. No hairs on the surface of the stem have been observed even in the sections where the epidermis is obviously present (Figs. 3A, 4A), this does not seem to confirm to the generic diagnosis offered by Holden (1960). In fact in R. dichotomum and R. americana hairs are not present in all stems or in all parts of one stem, therefore the feature that the stem is densely clothed with unbranched multicellular hairs seems unsuitable to be the generic diagnosis of Rhabdoxylon. Together with R. taiyuanense n. sp., there are three species in the genus Rhabdoxylon now. They are different in the geological ages. R. dichotomum is the oldest with the age of the Early Pennsylvanian (= early Westphalian A). R. americana has an age of the Late Pennsylvanian. R. taiyuanense n. sp. is the youngest with the age of the Early Permian. Along with the geological age becoming younger some characters of the three species, e.g., the stem size and the structure of the cauline stele, change regularly, which probably reflect certain evolutionary trends in the genus. The stem size of Rhabdoxylon probably increases along with the geological age becoming younger. R. dichotomum is the smallest with the diameter up to 2.7 mm (Holmes, 1979), but usually only 1.8–2.1 mm (Holden, 1960); R. americana is slightly larger than R. dichotomum with the diameter of 2–4 mm; R. taiyuanense n. sp. is the largest with the diameter up to 6 mm or more. Such an increase of the stem size along with the geological age becoming younger is also present in Botryopteris, a genus with a close relationship with Rhabdoxylon (Galtier and Phillips, 1977, 1996; Rößler and Galtier, 2003). In Botryopteris, the oldest species

B. antiqua (Visean of the Early Carboniferous) has the stems with the diameter up to 4.5 mm; the species of the Middle Pennsylvanian (= Westphalian B to D) have the stems with the diameter up to 7 mm (e.g., B. mucilaginosa Kraentzel) and 8 mm (e.g., B. ramosa (Will.) Scott); the species of the Late Pennsylvanian (= Stephanian) have the stems with the diameter up to 8.3–9.6 mm (e.g., R. forensis Renault); whereas the stems of B. nollii Rößler et Galtier of the Permian age have the diameter up to 11 mm. In Rhabdoxylon the number of the protoxylem groups in the cauline stele probably decreases along with the geological age becoming younger. R. dichotomum possesses two protoxylem groups in its protostele, one is persistent through the whole length of the stem and the other is associated with the forming of the petiolar trace. In the stele of R. americana there is only one protoxylem group that is associated with the forming of the petiolar trace. In R. taiyuanense n. sp., however, no distinct protoxylem groups are present in the stele. Holmes (1979) discussed the habit of R. dichotomum and R. americana based on the arrangement of leaves on the stem. He deduced that R. dichotomum might possess a prostrate habit for its long internodes (usually larger than 10 mm) or loosely arranged leaves, but R. americana might possess an upright habit for its very short internodes (about 1 mm) or closelypacked leaves. The new species probably possesses an upright habit because its internodes are short (about 2 mm) or leaves are closely-packed. 6. Conclusions 1. The present study describes a new early leptosporangiate fern from the Early Permian of North China. The fossil materials include three stems with attached and detached petioles and roots, occurring in a single coal ball from No. 7 coal seam of the Taiyuan Formation in the Xishan Coalfield, Taiyuan, Shanxi Province. These plant remains were assigned to the botryopterid fern Rhabdoxylon Holden by the small dichotomously branched and haplostelic stem with petioles possessing a single protoxylem group at the adaxial side of the xylem strand. A new species R. taiyuanense n. sp. is established. It differs from two known species of Rhabdoxylon mainly by features that there are no distinguished protoxylem groups in the stele and the petiolar xylem strand is bar-shaped or tangentially elongated. 2. The new species probably possesses an upright habit for its short internodes or closely-packed leaves.

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3. This is the first record of the genus Rhabdoxylon from the Permian aged strata and from the Cathaysian Province, so this study bears the significances both on taxonomy and palaeophytogeography of the botryopterid ferns. 4. The foliar members and fertile parts of Rhabdoxylon taiyuanense n. sp. are unknown for the moment. Acknowledgements Jean Galtier (CIRAD, Montpellier) is thanked for help in obtaining literature. This work has been supported by the State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS) project No. Y526010202 and the National Natural Science Foundation of China (Award No. 41530101, 41172014 and 41162001). Editors and two anonymous reviewers are warmly acknowledged for their constructive comments. References Bancroft, H., 1915. A contribution to our knowledge of Rachiopteris cylindrica Will. Annals of Botany 29, 532–565. Crane, P.R., Kenrick, P., 1996. Problems in cladistic classification: higher-level relationships in land plants. Aliso 15, 87–104. Dennis, R.L., 1968. Rhabdoxylon americanum sp. n., a structurally simple fernlike plant from the upper Pennsylvanian of Illinois. American Journal of Botany 55 (8), 989–995. Galtier, J., Phillips, T.L., 1977. Morphology and evolution of Botryopteris, a Carboniferous age fern, Part 2. Observations on Stephanian species from Grand’Croix, France. Palaeontographica B 164, 1–32. Galtier, J., Phillips, T.L., 1996. Structure and evolutionary significance of Palaeozoic ferns. In: Camus, J.M., Gibby, M., Johns, R.J. (Eds.), Pteridology in Perspective. Royal Botanic Gardens, Kew, pp. 417–433. Galtier, J., Phillips, T.L., 1999. The acetate peel technique. In: Jones, T.P., Rowe, N.P. (Eds.), Fossil Plants and Spores: Modern Techniques. Geological Society of London, London, pp. 67–71. Galtier, J., Phillips, T.L., 2014. Evolutionary and ecological perspectives of Late Paleozoic ferns. Part III. Anachoropterid ferns (including Anachoropteris, Tubicaulis, the Sermayaceae, Kaplanopteridaceae and Psalixochlaenaceae). Review of Palaeobotany and Palynology 205, 31–73. Hilton, J., Wang, S.J., Galtier, J., Li, C.S., 2001. An Early Permian plant assemblage from the Taiyuan Formation of northern China with compression/impression and permineralized preservation. Review of Palaeobotany and Palynology 114, 175–189. Hilton, J., Wang, S.J., Galtier, J., Glasspool, I., Stevens, L., 2004. An Upper Permian permineralized plant assemblage in volcaniclastic tuff from the Xuanwei Formation, Guizhou Province, southern China, and its palaeofloristic significance. Geological Magazine 141 (6), 661–674. Holden, H.S., 1960. The morphology and relationships of Rachiopteris cylindrica Williamson. Bulletin of the British Museum (Natural History) Geology 4 (3), 53–69. Holmes, J.C., 1977. The Carboniferous fern Psalixochlaena cylindrica as found in Westphalian A coal balls from England. Part I, structure and development of the cauline system. Palaeontographica B 164, 33–75.

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Holmes, J.C., 1979. Further observations on the coenopterid fern genus, Rhabdoxylon. Annals of Botany 44, 113–179. Holmes, J.C., 1981. The Carboniferous fern Psalixochlaena cylindrica as found in Westphalian A coal balls from England. Part II. The frond and fertile parts. Palaeontographica B 176, 147–173. Holmes, J.C., 1984. Morphology and evolution of Botryopteris, a Carboniferous age fern, Part IV. Branching patterns of the European species B. hirsuta and B. ramosa. Description of B. scottii n. sp. Palaeontographica B 191, 1–28. Holmes, J.C., Galtier, J., 1983. Morphology and evolution of Botryopteris, a Carboniferous age fern, Part III. Botryopteris dichotoma, a new Westphalian species from Belgium with observations on other species. Palaeontographica B 186, 1–17. Joy, K.W., Willis, A.J., Lacey, W.S., 1956. A rapid cellulose peel technique in palaeobotany. Annals of Botany 20, 1119–1133. Kraentzel, G., 1934. Etude monographique de Botryopteris mucilaginosa sp. nov. Annales de la Societe Geologique de Belgique 56, 51–72. Millay, M.A., Taylor, T.N., 1980. An unusual botryopterid sporangial aggregation from the Middle Pennsylvanian of North America. American Journal of Botany 67 (5), 758–773. Morgan, J., Delevoryas, T., 1954. An anatomical study of a new coenopterid and its bearing on the morphology of certain coenopterid petioles. American Journal of Botany 41, 198–203. Phillips, T.L., 1970. Morphology and evolution of Botryopteris, a Carboniferous age fern, Part 1. Observations on some European species. Palaeontographica B 130, 137–172. Phillips, T.L., 1974. Evolution of vegetative morphology in Coenopterid ferns. Annals of the Missouri Botanical Garden 61, 427–461. Phillips, T.L., Andrews, H.N., 1966. Catenopteris simplex gen. et sp. nov., a primitive pteridophyte from the upper Pennsylvanian of Illinois. Bulletin of the Torrey Botanical Club 93 (2), 117–128. Renault, B., 1883. Cours de Botanique fossile. Fougères. Masson, Paris, 216 pp. Rößler, R., Galtier, J., 2003. The first evidence of the fern Botryopteris from the Permian of the Southern Hemisphere reflecting growth form diversity. Review of Palaeobotany and Palynology 127, 99–124. Rothwell, G.W., Good, C.W., 2000. Reconstructing the Pennsylvanian-age filicalean fern Botryopteris tridentata (Felix) Scott. International Journal of Plant Sciences 161 (3), 495–507. Taylor, T.N., Taylor, E.D., Krings, M., 2009. Paleobotany — The Biology and Evolution of Fossil Plants (Second Edition). Academic Press, London, 1230 pp. Tian, B.L., Wang, S.J., Guo, Y.T., Chen, G.R., Zhao, H., 1996. Flora of Palaeozoic coal balls in China. Palaeobotanist 45, 247–254. Tomescu, A.M.F., Rothwell, G.W., Trivett, M.L., 2006. Kaplanopteridaceae fam. nov., additional diversity in the initial radiation of filicalean ferns. International Journal of Plant Sciences 167, 615–630. Wang, J., 2010. Late Paleozoic macrofloral assemblages from Weibei Coalfield, with reference to vegetational change through the Late Paleozoic Ice-age in the North China Block. International Journal of Coal Geology 83, 292–317. Wang, S.J., 1989. Cordaites in coal ball of Taiyuan Formation of Shanxi and Shandong Provinces and their living environment. Journal of China University of Mining and Technology 18 (4), 71–80 (in Chinese, with English abstract). Wang, S.J., Sun, K.Q., Cui, J.Z., Ma, S.M. (Eds.), 2009. Fossil Plants from Coal Balls in China. Higher Education Press, Beijing, 140 pp. (in Chinese). Willamson, W.C., 1878. On the organization of the fossil plants of the coalmeasures. Part IX. Philosophical Transaction of the Royal Society of London 169, 319–364.

Please cite this article in press as: Ma, J., et al., Rhabdoxylon taiyuanense n. sp.: A new botryopterid fern from the Lower Permian of Shanxi Province, North China. Palaeoworld (2016), http://dx.doi.org/10.1016/j.palwor.2016.05.002