Species of the Medullosan Ovule Stephanospermum from the Lopingian (Late Permian) ﬂoras of China ⇑ Alan R.T

Journal of Asian Earth Sciences 76 (2013) 59–69

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Journal of Asian Earth Sciences

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Species of the medullosan ovule Stephanospermum from the Lopingian (late Permian) ﬂoras of China ⇑ Alan R.T. Spencer a, , Shi-Jun Wang b,c, Michael T. Dunn d, Jason Hilton e a Department of Earth Sciences and Engineering, Imperial College London, London SW7 2BP, UK b State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, PR China c State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, PR China d Department of Biological Sciences, Cameron University, Lawton, OK 73505, USA e School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK article info abstract

Article history: The medullosan pteridosperm ovule Stephanospermum Brongniart is a well-known component of Carbon- Received 18 April 2013 iferous aged coal-ball and siderite nodule floras from North America and Europe but also occurs in the Received in revised form 3 July 2013 Permian floras of Cathaysia where it is represented by the Lopingian (late Permian) aged species Stephan- Accepted 22 July 2013 ospermum trunctatum (Li) Wang et al. (2009) from coal-balls in the Wangjiazhai Formation in Southern Available online 7 August 2013 China. We provide a detailed emendation of S. trunctatum and illustrate it comprehensively for the first time, and document an additional specimen from the Wangjiazhai Formation coal-ball assemblage that Keywords: we assign to Stephanospermum shuichengensis sp. nov. S. shuichengensis is distinguished from S. truncta- Gymnosperm tum by the absence of apical teeth in the sclerotesta and non-obovate base. The two species of Stephan- Medullosales Trigonocarp ospermum from the Wangjiazhai Formation are important as they extend the stratigraphic and Coal-ball geographical range of the genus from the Pennsylvanian of Euramerica into the Lopingian of Southern Wangjiazhai Formation China, and demonstrate that the genus persisted in wetland, peat forming environments in the run up Shuicheng to the end-Permian mass extinction event. The 44 MY stratigraphic discontinuity between the Euramer- ican and the Cathaysian species, here named the Stephanospermum gap, leads us to infer that the genus was likely to have occurred in the Pennsylvanian–Permian successions of southern Russia and northern China that are geographically and stratigraphically intermediate to the known occurrences but from which the genus has yet to be discovered. Medullosan pteridosperms appear to have become extinct at or immediately prior to the Permian–Triassic boundary that coincides with the Permo–Trias mass extinction event; although the exact causes of this loss in plant diversity remains unknown, a response to regional climatic drying is likely to have been a contributing factor. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction conform to the traditionally circumscribed trigonocarpalean concept (senus Seward, 1917) and are large, radially symmetrical, Medullosans are a comparatively well characterised group of have the nucellus attached to the integument at the chalaza only, Late Palaeozoic pteridosperms that were widespread in wetland and possess a domed or campanulate pollen chamber (Serbet and and moister parts of seasonal wetland settings in the Pennsylva- Rothwell, 1995; Spencer et al., 2013). In the compression/impres- nian of Europe and North America (DiMichele et al., 2006) and sion record, medullosan ovules are typically placed in the genus the Permian of China (Wang et al., 2009). As a group they exhibit Trigonocarpus Brongniart 1828, whereas those known with ana- a range of growth architectures including trees, vines and liana- tomical preservation are variously assigned to the genera Pachytes- like plants. In addition DiMichele et al. (2006) suggest that some ta Brongiart 1874, Stephanospermum Brongniart 1874, medullosans may have been cormose, acaulescent plants. How- Hexapterospermum Brongniart 1874, Polypterospermum Brongniart ever, currently the evidence is lacking for an evolutionary frame- 1874, Codonospermum Brongniart 1874, Rhynchosperma Taylor work in which to determine the relationships between taxa with and Eggert 1967, and Hexaloba Dunn et al. 2002. different growth architectures (DiMichele et al., 2006; Hilton and The genus Stephanospermum at present includes eight species Bateman, 2006). Where known, ovules produced by medullosans from the Pennsylvanian to earliest Permian ﬂoras of Euramerica plus a single species from the Permian of China (see Wang et al.,

⇑ Corresponding author. Tel.: +44 07824325531. 2009; Spencer et al., 2013, for a recent review). The species from E-mail address: [email protected] (A.R.T. Spencer). China occurs in Changhsingian (late Permian) aged coal-balls from

1367-9120/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jseaes.2013.07.030 60 A.R.T. Spencer et al. / Journal of Asian Earth Sciences 76 (2013) 59–69 the Wangjiazhai Formation and was first documented and partially available, and have the drawback of often forming peels of unequal illustrated by Li (1988) as part of an unpublished PhD thesis. This thickness from which photography of uneven surfaces may be account was subsequently published by Li (1991) who assigned challenging. These limiting factors in addition to non-sequential it to Stephanospermum cf. akenioides noting its similarity with Step- slides, uneven spacing between the peels/film pulls, and with hanospermum akenioides Brongniart 1874 from the Pennsylvanian one specimen only having two peels it has not been possible to of Europe. Li’s (1988, 1991) account was based on a single speci- reconstruct the 3D organisation of the seeds in full. men exposed on the external surface of a coal-ball that was then Mounted slides were photographed with a Cannon EOS 40D cut longitudinally and from which acetate peels were subsequently mounted on a Zeiss Tessovar macro system with illumination pro- made. The same specimen was later included and illustrated with- vided by twin fibre-optic light guides and a ring light. The resulting in an atlas of fossil plant anatomy in China (Li and Cui, 1995, pg. images where processed (cropped, rotated, edge enhanced and 62), although in this account it was erroneously illustrated up- equalised for hue and brightness) in GIMP 2, ImageJ (Abràmoff side-down. In 2009, as part of their revision of the coal-ball floras et al., 2004) and Corel Paint Shop Pro Photo X2 with figures con- of China, Wang et al. reinvestigated the species based on the peels structed in Adobe Illustrator CS4/5 and Inkscape (see Spencer from Li’s earlier investigation, concluding that it was distinct from et al., 2013, for an overview on the software packages used). S. akenioides in having 4 short, triangular apical teeth rather than possessing a conspicuous crown characteristic of S. akenioides 3. Geological information and age (Wang et al., 2009). These distinctions led Wang et al. (2009) to transfer the species into S. trunctatum Wang et al., but other than Specimens occur in coal-balls from the Wangjiazhai Formation the systematic section of that account, the remaining text was pub- in Guizhou Province in South China (Wang et al., 2009). Although lished in the Chinese language so is not available to non-Chinese the full flora has yet to be studied in detail, previous investigations scientists. Furthermore, only key features of S. trunctatum were demonstrate it to include lycopsids (Wang et al., 2009), marattia- emended and illustrated. Here we provide a full systematic ac- lean (He et al., 2006) and osmundalean ferns (Li, 1993; Wang count of S. trunctatum, illustrate it comprehensively and compare et al., 2013), pteridosperms (Seyfullah et al., 2009; Wang et al., it with other species of the genus for the first time. 2009) and cycads (Wang et al., 2011b). In the Wangjiazhai Forma- During the course of our investigation we have also identified tion, peat forming wetland plant communities developed in low- another specimen from the coal-ball assemblage in the Wangjiaz- lying coastal settings with peat formation ceasing with marine hai Formation that conforms to the generic circumscription of Step- incursion, with the onset of marine conditions facilitating the for- hanospermum but is distinct from Stephanospermum trunctatum. mation of coal-balls (Wang et al., 2011a). Coal-balls in these set- This specimen is described and illustrated here for the first time, tings were permineralized by an early diagenetic calcium and comparisons demonstrate it to represent a new species with carbonate cement, but pyritization is also abundant within the a close affinity to species of Stephanospermum from the Pennsylva- coal-balls where presumably it was triggered by early decay of soft nian of Euramerica. We name the new species Stephanospermum tissues in reaction with saline water prior to carbonate mineraliza- shuichengensis Spencer et al. Evolutionary and environmental tion (for overview of coal-ball formation see Scott et al., 1996). implications of the presence of two species of Stephanospermum Wang et al. (2011a) presented a regional stratigraphic correla- in the Lopingian flora of southern China are considered. tion of the Guadalupian–Lopingian aged sedimentary successions in Guizhou Province and concluded that the Wangjiazhai Forma- tion was deposited during the Changhsingian stage of the Lopin- 2. Materials and methods gian (late Permian) Epoch. In a broader geological context, the Wangjiazhai Formation postdates the Emeishan Basalt in this re- This investigation is based on two specimens preserved in car- gion of southwest China that is coincident with the Capitanian bonate coal-balls from the Wangjiazhai coal mine in Shuicheng (middle Permian) extinction, but predates the Permian–Triassic District, Guizhou Province, in southwest China (Tian and Zhang, boundary and its mass extinction event (Bond et al., 2010; Wang 1980; Tian et al., 1996; Wang et al., 2009; see Wang et al., et al., 2011a); the flora of the Wangjiazhai thus represents a snap- 2011a, for location details). The specimen documented by Li shot of terrestrial diversity bounded by mass extinction events (1991) and subsequently Wang et al. (2009) comes from coal-ball each of which had profound consequences for life on Earth. GP2713-2 and is represented by two individual peels mounted on a single slide. The peels labelled GSW-CB-0013 and GSW-2-1/1 appear to represent either side of a specimen revealed by a saw cut 4. Results that destroyed the middle part of the ovule. This specimen was prepared by the acetate peel technique (Galtier and Phillips, 4.1. Description of Stephanospermum trunctatum Wang et al. emend 1999). The second specimen is previously unfigured and from coal-ball GSW-845-2 and is represented by 24 peels (numbered The following description is based on two near longitudinal GSW-CB-0028 to GSW-CB-0052) that also appear to have been ta- peels of the specimen previously figured by Li (1991) and Wang ken to either side of a specimen revealed by a saw cut. This spec- et al. (2009). imen was prepared by the acetate film pull technique (Walton, 1930) during the 1980s by a student of Professor Zhu Weiqing at 4.1.1. Gross morphology the Institute of Botany. For both methods coal-balls were cut using The ovule is 7.9 mm long (from chalaza to the tips of the integ- a rock saw and the cut surfaces etched using 5% hydrochloric acid umentary teeth) and 4 mm wide at the mid-point, is broadly obo- with the sample left to air dry. Acetone was then applied to the vate (Fig. 1a–c), and apically it has three short triangular teeth prepared etched surface. For the acetate peel technique a cellulose (Fig. 1a, b and d) surrounding a micropyle (Fig. 1d). acetate sheet was applied to the specimen and was then allowed to air dry. For the film pull technique liquid cellulose acetate was 4.1.2. Integument poured onto the prepared surface and allowed to air dry. Once The integument comprises of a poorly preserved sarcotestal dry, acetate sheets/films were pulled off the sample and mounted layer, a variably thick sclerotesta and a thin endotesta (Fig. 1c on microscope slides for analysis. Acetate film pulls were routinely and d). For most of the length of the ovule the outermost preserved used to make peels before cellulose acetate sheets became widely layer is the sclerotesta (Fig. 1c), but poorly preserved sarcotesta is A.R.T. Spencer et al. / Journal of Asian Earth Sciences 76 (2013) 59–69 61

Fig. 1. Stephanospermum trunctatum Wang et al. from the Lopingian aged Wangjiazhai Formation prepared as acetate peels. All images in longitudinal sections from coal-ball

GP2713-2. (a) Ovule with prominent dark coloured sclerotesta with attenuated chalaza and prominent apical teeth. Slide GSW-CB-0013, scale bar = 1 mm. (b) Ovule showing rounded apex from which a base of only one tooth is present in the plane of section. Slide GSW-2–1/1, scale bar = 1 mm. (c) Enlargement of chalaza from (a) showing thick, dark sclerotesta, thin vascular nucellar pad, and megaspore membrane containing megagametophytic tissue (Mg). Slide GSW-CB-0013, scale bar = 0.5 mm. (d) Enlargement of the apex of ovule from (a) showing sclerotestal teeth, and remnants of the sarcotesta in the micropylar region. Slide GSW-CB-0013, scale bar = 0.5 mm. (e) Enlargement from (a) showing position of Sarcotesta, sclerotesta and endotesta. Slide GSW-CB-0013, scale bar = 250 lm. (f) Enlargement from (a) showing the nucellus, megaspore membrane and tissues of the cellular megagametophyte. Slide GSW-CB-0013, scale bar = 0.1 mm. (g) Enlargement of the apex of (b) showing the variably thick sclerotesta, and possible 1 position of the micropyle, nucellus and pollen chamber. Slide GSW-21, scale bar = 0.5 mm. Key: En = endotesta; M = megaspore membrane; Mg = megagametophyte tissue; Mi = micropylar region; N = nucellus; P = nucellar pad; Pc = pollen chamber; Sa = sarcotesta; Sc = sclerotesta; T = sclerotestal tooth. 62 A.R.T. Spencer et al. / Journal of Asian Earth Sciences 76 (2013) 59–69 present in the micropylar region between the integumentary teeth (Fig. 2c) but can clearly be seen to have once been oriented circum- (Fig. 1d). ferentially. Interspersed within these cells are chambers of larger In the micropylar region the sarcotesta is 175–237 lm thick thin walled (Fig. 2c, at arrows). Sarcotesta is vascularized by an un- (Fig. 1d) and composed of thick brown walled cells the largest of known number of bundles of which some are located in the mid- which are 18–28 lm in circumference (mean = 23 lm).The smaller region of this inner sarcotesta (Fig. 2c, see box, g). cells, which make up the bulk of the sarcotesta, are too poorly pre- Sclerotesta is approximately 200 lm thick and is bilayered, served to measure. Sarcotesta has in places separated taphonomi- with the cells of the inner zone exhibiting two distinct patterns cally from the underlying sclerotesta (Fig. 1d). (Fig. 2d). The outer zone forms a palisade of cells radiating out- Sclerotesta is bilayered and varies from 160–225 lm thick at ward. These cells are 20–25 lm wide and up to 100 lm long with the chalaza (Fig. 1a–c) and thins on the sides to 60–100 lm cell walls 5–7 lm thick (mean = 5.8 lm). The inner sclerotesta con- (Fig. 1a and b) before thickening to form the apical teeth sists of fibres that are oriented circumferentially at the contact area (Fig. 1c). The outer zone forms a palisade of outward-radiating cells with the outer sclerotesta layer and interwoven internally (Fig. 2e). (Fig. 1e). These cells are 8–10 lm wide and up to 59–77 lm long Cells of the inner layer are 20–30 lm in diameter (mean = 23 lm) with cell walls 2–4 lm thick (mean = 3 lm). The inner zone con- and cell walls 5–7 lm (mean = 5.5 lm) thick. sists of fibres that are oriented circumferentially at the contact area Endotesta is 11 lm wide and is uniseriate and comprises thin with the outer sclerotesta layer (Fig. 1e). Cells of the inner layer are walled cells (Fig. 2d and f). The endotesta is normally attached to 4–15 lm in diameter (mean = 9 lm) with cell walls 2–5 lm the inner surface of the sclerotesta (Fig. 2d) but in other places (mean = 3 lm) thick. has become separated from it (Fig. 2f). The endotesta is 18–25 lm wide comprising (Fig. 1e) a uniseriate layer of large, thin walled cells that is consistently attached to 4.2.3. Nucellus and megaspore the inner surface of the sclerotesta (Fig. 1e). The nucellus is attached to the integument only at the base where it forms a vascular nucellar pad (Fig. 2b) comprised of an 4.1.3. Nucellus and megaspore anastomosing sheath of tracheids and parenchyma cells (Fig. 2h). The nucellus (=megasporangium, see Hilton and Bateman, 1 The pad itself rises up to =4 of the length of the integument 2006) is not fully expanded and is separated from the integument (Fig. 2b). The pollen chamber is not preserved, but the nucellus for the majority of its length. A large vascular nucellar pad occurs does extend to the micropylar end of the ovule (Fig. 2a and b) at the chalaza (Fig. 1a–c) but the nucellus has detached from this where it appears to begin formation of a cellular pollen chamber (Fig. 1a and b) leaving a small papillate extension at the base of wall and membranous pollen chamber floor (Fig. 2a, at arrow). the nucellus (Fig. 1a–c). The nucellus is thin and appears to be The megaspore membrane is not fully expanded to fill the nucellus uniseriate (Fig. 1f) and has a small pollen chamber apically and is approximately 12 lm thick (Fig. 2f) and like the nucellus, ex- (Fig. 1b and g). The megaspore membrane is sometimes fused to tends to near the sclerotesta at the apex of the ovule (Fig. 2a and b). the nucellus (Fig. 1f) but is more often separated from it (e.g. Tissues of the cellular megagametophyte are poorly preserved and Fig. 1c and d). At the apex of the nucellus a small pollen chamber appear to have decayed prior to fossilisation (label in Fig. 2b). occurs but this is imperfectly represented in the available peels but is triangular in longitudinal-section (Fig. 1b and g), and is posi- 4.2.4. Vascularisation tioned beneath a short micropylar tube in the sclerotesta (Fig. 1g) The sheath of tracheids rising from the nucellar pad is one to where the different halves of the integument meet apically. several cells thick and vascular tissues have been observed up to 3= of the length of the nucellus. Vascular tissues have also been ob- 4.1.4. Vascularisation 4 served in the fleshy apical sarcotesta layer (Fig. 2c) where they are The nucellus is vascularised by a large vascular nucellar pad and approximately 25 lm in diameter and exhibit a scalariform wall from where fragments of poorly preserved tracheids surround the thickening pattern (Fig. 2g). The number of integumentary bundles nucellus distal from the pad (Fig. 1c). These tracheids are irregular is unknown. and their organisation appears to represent a net-like layer surrounding the nucellus. No integumentary vascularisation has been found due to poor preservation state. 5. Discussion

4.2. Description of second specimen 5.1. Comparisons

The following description is based on information from 24 serial S. trunctatum and the second species share an overall similar acetate film pulls preserving a single ovule in near longitudinal size and organisation but S. trunctatum differs in external morphol- section (Figs. 2 and 3). ogy by having a broadly ovate to obovate base and a flattened apex compared to the oval apex of the second species (Table 1; Fig. 4). 4.2.1. Gross morphology The three sclerotic apical teeth of S. trunctatum, as the etymology The ovule is 7.2 mm long and 3.6 mm wide, is broadly ovate reflects, are truncated extensions whereas the second species has with a rounded base but apically has integumentary extensions prominent sarcotestal extensions and no sclerotesta rounded apex. (Figs. 2a, b and 3). The outermost preserved layer of the seed is a In S. trunctatum the sarcotesta is generally poorly preserved but poorly preserved sarcotesta. A micropyle has not been observed where complete consists of thick, brown walled cells. The sarcotes- and is likely to have been destroyed in preparation of the ovule. ta of S. trunctatum differs from the other specimen in being bi-layered with the inner layer consisting of elongate thin-walled cells 4.2.2. Integument (Table 1; Fig. 4). Both of the Chinese ovules have a bi-layered scle- The sarcotesta (Figs. 2c and 3) is bilayered consisting of an outer rotesta and these are of a similar thickness and both have an outer dermal layer and an inner fleshy layer. The outer layer is 175– layer constructed of cells that radiate outward and form a palisade. 200 lm thick and composed of thick walled cells mostly circumfer- However, the inner sclerotesta of S. trunctatum comprises circum- entially oriented with only a slight tendency to anastomose ferentially oriented cells whereas in the second species they are (Fig. 2c). Cell walls are 7–10 lm thick. Elongated cells of the inner heavily interwoven and more irregular in their orientation. The fleshy layer are highly contorted from taphonomic processes endotesta of both ovules is uniseriate and is comprised of A.R.T. Spencer et al. / Journal of Asian Earth Sciences 76 (2013) 59–69 63

Fig. 2. Stephanospermum shuichengensis sp. nov. from the Lopingian aged Wangjiazhai Formation prepared as acetate film pulls. All images in longitudinal section from GSW-845– 2. (a) Ovule near mid-section showing crushed sarcotesta, sclerotesta, nucellus and megaspore membrane. Possible cellular pollen chamber wall and membranous pollen chamber floor shown by arrow. Slide GSW-CB-0049, scale bar = 1 mm. (b) Ovule in mid-section showing the vascular bundle entering at base and forming the vascular nucellar pad, Slide GSW-CB-0044, scale bar = 1 mm. (c) Bilayered sarcotesta showing outer dermal layer in cross section and inner fleshy layer. Arrows indicates chambers of larger thin walled cells. See (g) for enlargement of vascular bundle with in sarcotesta. Slide GSW-CB-0044, scale bar = 200 lm. (d) Section through integument showing bilayered sclerotesta; note how inner most layer of cells reorient from anastomosing to circumferential near the outer palisade layer. Slide GSW-CB-0050, scale bar = 50 lm. (e) Sclerotesta in the apex of the ovule showing highly interwoven cells; the sclerotesta is bilayered. Slide GSW-CB-0037, scale bar = 200 lm. (f) Section showing sclerotesta and endotesta, nucellus and megaspore membrane. Slide GSW-CB-0050, scale bar = 200 lm. (g) Enlargement from (c) showing vascular bundle in sarcotesta (at arrow). Slide GSW-CB-0044, scale bar = 50 lm. (h) Nucellar pad and vascular bundle entering chalaza. Slide GSW-CB-0047, scale bar = 200 lm. Key: En = endotesta; M = megaspore membrane; Mg = megagametophyte tissue; Mi = micropylar region; N = nucellus; P = nucellar pad; Pc = pollen chamber; Sa = Sarcotesta; Sc = sclerotesta (Sco = outer layer; Sci = inner layer); T = sclerotestal tooth; Vb = vascular bundle. 64 A.R.T. Spencer et al. / Journal of Asian Earth Sciences 76 (2013) 59–69

tridentatum,S. elongatum,S. ovoides andS. konopeonus by having sarcotestal extensions with no underlying sclerotestal support (Oliver, 1904; Taylor, 1962; Leisman and Roth, 1963; Drinnan et al., 1990; Serbet and Rothwell, 1995). It also differs from S. costatum and S. braidwoodensis by exhibiting a bilayered sarcotesta (Good et al., 1982; Spencer et al., 2013). These differences lead us to establish a new species that we name Stephanospermum shuichengensis Spencer, Wang, Dunn et Hilton sp. nov.

5.2. Other organs belonging to the same whole-plant species

No other medullosan organs have been identified from this assemblage to date such that both species of Stephanospermum documented from the Wangjiazhai Formation are only known from their distinctive ovules. Considering the similarity of the Chinese species with Stephanospermum akenioides, it is probable that they also pos- sessed stems of Medullosa Cotta type, rachises of the Myeloxylon Brongniart type, and pollen organs of either Codonotheca Sellards, Schopfitheca Delevoryas, Dolerotheca Halle, or Benaultia Rothwell and Eggert. These taxa have not been identified in the Wangjiazhai Formation to date (Tian and Zhang, 1980; Wang et al., 2009). Overall, pteridosperms are a minor component of the flora preserved in coal-balls from the Wangjiazhai Formation that is domi- nated by marattialean and osmundalean ferns, with less frequently occurring lycopsids and other gymnosperms (Tian and Zhang, 1980; Tian et al., 1996; Wang et al., 2009). From the assemblage Seyfullah et al. (2009) documented protostelic pteridosperm stems Fig. 3. Annotated camera-lucida diagram of Stephanospermum shuichengensis sp. nov. from the Wangjiazhai Formation of South China based on peel shown in Fig. 2a. with manoxylic wood and mesarch xylem maturation as Heteran- gium sp. Where known, stems of Heterangium were produced by hydrasperman rather than medullosan pteridosperms (e.g. Seyful- thin-walled cells. Internally the nucellus of both ovules attaches to lah et al., 2009). Li (1991) established Sarcospermum petiolatum Li the integument only at the chalazal end via a large vascularised for isolated ovules from the Wangjiazhai Formation that he inter- nucellar pad. Both ovules have net-like tracheids surrounding the preted to be a trigonocarpalean ovule produced by a medullosan. nucellus, with this feature being characteristic of the genus Step- However, Hilton et al. (2001) scrutinised Li’s illustrations of this hanospermum (Serbet and Rothwell, 1995) but differing from the species and determined that Li had structurally misinterpreted a closely related genus Pachytesta, which lacks this kind of vasculari- hydrasperman-type ovule; what Li illustrated as the main (=nucel- sation (Hoskins and Cross, 1946; Taylor, 1965). lar) bundle is a hydrasperman-type pollen chamber, and the nucel- We concur with Li (1991) and Wang et al. (2009) that S. trunct- lar vascular strands shown by Li are characteristic of atum is distinct from all other species of Stephanospermum (see Ta- hydrasperman rather than medullosan ovules. It is feasible that ble 1 and Fig. 4). However re-examination of the specimen has ovules of S. petiolatum were produced by the same plant as stems shown the apical extensions to consist of three not four sclerotic of Heterangium sp. from the same assemblage as both have features teeth as stated by Li (1991) and Wang et al. (2009). The apical consistent with affinities of hydrasperman pteridosperms. extensions and teeth of S. trunctatum are similar to those of S. akenioides, S. tridentatum, S. elongatum, S. ovoides and S. konopeonus, 5.3. Phytogeographical and evolutionary implications and the construction of thesclerotesta construction is similar to S. ovoides, S. konopeonus, S. elongatum,S. caryoides, S. tridentatum, S. Both species of Stephanospermum from the Wangjiazhai Forma- akenioides (Oliver, 1904; Taylor, 1962; Leisman and Roth, 1963; tion in southern China are only known from this locality and rep- Drinnan et al., 1990; Serbet and Rothwell, 1995). Its dome-shaped resent the stratigraphically youngest species of the genus that pollen chamber is similar to all species of Stephanospermum except extends from the Moscovian to Kasimovian stages of the Carbonif- S. ovoides, S. braidwoodensis, S. elongatum, and S. tridentatum (Tay- erous in North America and the Kasimovian stage in Europe into lor, 1962; Leisman and Roth, 1963; Serbet and Rothwell, 1995; the Changhsingian of Southern China (Fig. 5). Stephanospermum Spencer et al., 2013). However, it differs from the species S. caryo- thus represents one of a small but important number of genera ides, S. braidwoodensis, S.tridentatum, S. ovoides (Oliver, 1904; Tay- that persists from the late Palaeozoic peat forming environments lor, 1962; Serbet and Rothwell, 1995; Spencer et al., 2013)by of Euramerica into Cathaysia (e.g. Hilton et al., 2002; Hilton and having an ovate to obovate base that is more similar to those in Cleal, 2007). However, Stephanospermum is unknown from the c. S. costatum, S. akenioides, and S. konopeonus (Oliver, 1904; Good 44 MY interval between the Pennsylvanian and late Permian occur- et al., 1982; Drinnan et al., 1990). S. trunctatum also differs from rences that we here name the ‘Stephanospermum gap’ (Fig. 5). For S. caryoides and S. tridentatum by not exhibiting a central column this apparent ‘Lazarus’ taxon that reappears with very little change in the pollen chamber (Serbet and Rothwell, 1995), however this in the fossil record after an extensive stratigraphical gap, we con- may be due to removal by taphonomic processes or due to fossil- sider that it is improbable for the genus to have evolved twice ization at an early ontogenetic stage. independently and infer that it must have existed in palaeogeo- The new specimen described here is distinct from S. trunctatum graphical areas between Euramerica and southern China during (see above) and also possesses net-like vascularisation in the the Stephanospermum gap. As medullosans inhabited wetland hab- nucellus and has the characteristic apical extensions and integu- itats, Stephanospermum is likely to have existed in refugial settings mentary organisation consistent with the genus Stephanospermum or inadequately sampled geological successions in the palaeogeo- (see Table 1 and Fig. 4). However, it differs from S. akenioides,S. graphical regions that lay between Euramerica and Cathaysia Table 1 Comparison of species of the Medullosan pteridosperm ovule Stephanospermum. Expanded and modified from Table 1 of Spencer et al. (2013). *S. akenioides was erroneously stated in Spencer et al. (2013) as having been found in ‘‘Europe/USA’’ that is here corrected to show distribution in Europe only.

S. costatum S. ovoides S. konopeonus S. braidwoodensis S. elongatum Age Period Carboniferous Carboniferous Carboniferous Carboniferous Carboniferous Series Pennsylvanian Pennsylvanian Pennsylvanian Pennsylvanian Pennsylvanian Stage Moscovian (Westphalian B) Moscovian (Westphalian D) Moscovian (Westphalian D) Moscovian (Westphalian D) Moscovian (Westphalian D)-Kasimovian (Stephanian B) Ovule length (mm) 15.0 10.0 12.0–15.0 13.2 13.0–19.0 Major plane width, 8.0 7.0 10.5 10.4 5.0–8.5 including wings (mm) Minor plane width (mm) 8.0 7.0 5.0–6.0 7.4 5.0–8.5 Ovule shape Elliptical Ovate Ovate Ovate Elliptical (longitudinal section) Sarcotesta shape in 12-ribbed Circular 4-winged 4-winged Roundly triangular cross-section at mid- point 59–69 (2013) 76 Sciences Earth Asian of Journal / al. et Spencer A.R.T. Sclerotesta shape in Hexagonal, 3-ribbed Circular Circular Roundly triangular, 3-ribbed Roundly triangular-hexagonal cross-section at mid- point Crown Absent Low, conspicuous Conspicuous Conspicuous Conspicuous, with 6 long apical teeth Micropylar tube length 2.5 Up to 1.5 1.3–1.6 1.8 3.5–5.0 (mm) Number of buttresses Absent Absent Absent Absent 3 primary, 3 secondary Composition of Thin-walled cells with Thin cutinized epidermal Not Preserved Large mucilage-filled and Cellular-thickened radial walls sarcotesta 800–1500yellow contents 150–400layer 300–700 220–1550thin-walled parenchyma cells 200–1200 Thicknesslm) of sarcotesta Arrangement( of Radially elongated interior, Parallel to long axis of ovule Forming external wings Forming external wings Parallel to long axis of ovule sarcotestal cells isodiametric periphery 150 lm thick, up to 1.5 mm broad Sarcotestal 12 bundles, one near top of Numerous bundles 6 bundles Unknown Bundles near inner margin vascularization each rib. Sclerotestal construction Unilayered Bilayered Bilayered Unilayered Bilayered Thickness of sclerotesta 100 260–550 300 170–370 365–750 lm)( Endotesta construction Poorly preserved thin- Coalified, difficult to establish Uniseriate, rectangular cells Uniseriate, thin-walled Uniseriate, thin-walled, elongate parenchymatous cells walled cells with inner morphology rectangular to polygonal cells cuticle. Endotesta thickness Unknown 20–75 18–65 10–30 Unknown (lm) Pollen chamber shape Dome-shaped Campanulate Dome-shaped Campanulate Campanulate Central column Absent Absent Absent Absent Absent Membranous pollen Absent Present Unknown Unknown Present chamber floor Nucellar beak opening 100 lm diam. Sealed 170 lm diam. sealed 170 lm diam. 160 lm Nucellar beak Radially elongate cells, Elongate cells Radially elongate cells, thicker Unknown Radially elongate cells, thicker radial walls construction thicker radial walls radial walls Nucellar vascularization Continuous sheath of Tracheal sheath up to the Continuous sheath of tracheids Unknown Continuous sheath of tracheids up to the pollen chamber tracheids below pollen nucellar folding chamber Distribution North America North America North America North America North America Reference(s) Good et al. (1982) Hall (1954) and Taylor (1962) Drinnan et al. (1990) Spencer et al. (2013) Hall (1954) and Leisman and Roth (1963)

(continued on next page) 65 66 Table 4 (continued) S. tridentatum S. caryoides S. akenioides S.trunctatum S. shuichengensis Age Period Carboniferous Carboniferous Carboniferous Permian Permian Series Pennsylvanian Pennsylvanian Pennsylvanian Lopingian Lopingian Stage Kasimovian (Stephanian B) Kasimovian (Stephanian B) Kasimovian (Stephanian B) Changhsingian Changhsingian Ovule length (mm) 5.5–12.0 15.5 10.0 7.9 7.2 Major plane width 3.0–7.5 12.5 4.0–4.5 4.0 3.6 including wings (mm) Minor plane width (mm) 3.0–7.5 12.5 4.0–4.5 4.0 3.6 Ovule shape Elliptical Oval-circular Elliptical Broadly ovate to obovate, tip Broadly ovate with a rounded base (longitudinal section) truncated Sarcotesta shape in Circular? Circular? Circular? ? ? cross-section at mid- point

Sclerotesta shape in Circular Circular Circular? Circular ? 59–69 (2013) 76 Sciences Earth Asian of Journal / al. et Spencer A.R.T. cross-section at mid- point Crown Conspicuous, with 3 short Low, inconspicuous Conspicuous Low, with 3 short triangular Conspicuous, with 3 teeth apical teeth teeth Micropylar tube length Up to 5.0 1.7 1.7 0.3 Unknown (mm) Number of buttresses 3 Absent Absent Absent Unknown Composition of Cellular-thickened radial Not Preserved Not Preserved Thick brown walled cells Bilayered sarcotesta >40–55walls – – 175–237where preserved. near micropyle 175–200 (outer layer) Sarcotestalm) thickness Arrangement( of Parallel to long axis of ovule – – Unknown Outer layer mostly circumferential with occasional sarcotestal cells anastomosing. Inner layer circumferentially orientated Sarcotestal No bundles near inner Unknown Unknown Unknown Vascularized by unknown number of bundles mid region vascularization margin Sclerotestal construction Bilayered Bilayered Bilayered Bilayered Bilayered Sclerotesta thickness 228–510 900 330 60–225 200 (lm) Endotesta construction Uniseriate, heavily cutinized Thin-walled tissue. Network of thin-walled cells Uniseriate Uniseriate, large thin walled cells cells Endotesta thickness 35 Unknown Unknown 18–25 11 (lm) Pollen chamber shape Campanulate Dome-shaped Dome-shaped Small, Dome-shaped Not Preserved Central column Present Present Absent Absent – Membranous pollen Present Present Present Unknown Present chamber ﬂoor Nucellar beak opening Sealed Sealed Sealed Sealed? – Nucellar beak Radially elongate cells, Radially elongate cells Thick-walled cells, coaliﬁed Unknown – construction thicker radial walls contents 3 Nucellar vascularization Net-like sheath of tracheids Unbroken sheath of tracheids Tracheal mantle, not readily Tracheids in a ‘net like’ Sheath of tracheids up to =4 of the length of the nucellar up to pollen chamber up to the pollen chamber seen in the nucellar wall sheath from pad Distribution North America Europe Europe* China China Reference(s) Serbet and Rothwell (1995) Oliver (1904) Brongniart (1874) and Oliver Li (1991) and Wang et al. This Paper (1904) (2009) This Paper A.R.T. Spencer et al. / Journal of Asian Earth Sciences 76 (2013) 59–69 67

Fig. 4. Schematic diagrams showing gross morphology of species of Stephanospermum. (a) Stephanospermum costatum. Camera-lucida diagram from Pl. I, 1 of Good et al. (1982). (b) Stephanospermum ovoides. Re-drafted from Fig. 13 of Taylor (1962). (c) Stephanospermum konopeonus. Re-drafted from Fig. 9 of Drinnan et al. (1990). (d) Stephanospermum braidwoodensis. Based on 3D-recontruction data in Spencer et al. (2013). (e) Stephanospermum elongatum. Re-drafted from Fig. 1 in Hall (1954). (f) Stephanospermum tridentatum. Camera-lucida composite diagram from Figs. 1–3 of Serbet and Rothwell (1995). (g) Stephanospermum caryoides. Re-drafted from Fig. 2 in Oliver (1904). (h) Stephanospermum akenioides. Re-drafted from Fig. 1 in Oliver (1904). (i) Stephanospermum trunctatum. Camera-lucida from Fig. 1a. (j) Stephanospermum shuichengensis. Camera-lucida from Fig. 2b. Scale bar for all images = 2 mm except S. elongatum (e) that is reduced by 20% for which the scale bar is 1.6 mm. 68 A.R.T. Spencer et al. / Journal of Asian Earth Sciences 76 (2013) 59–69

processes with the gut of vertebrates where the sarcotesta acts as an animal attractant for dispersal. In Stephanospermum trunctatum the sarcotesta is poorly preserved whereas its preservation is better in Stephanospermum shuichengensis with both species possessing a prominent sclerotesta. It remains uncertain if facultative sarcotestal shedding occurred in medullosan pteridosperms includingStephanospermum or if the generally poor state of preservation of its sarcotesta was due to taphonomic processes.

6. Systematic palaeobotany

Phylum SPERMATOPHYTA. Order MEDULLOSALES Corsin, 1960. Genus Stephanospermum Brongniart, 1874. Species Stephanospermum trunctatum SJ Wang et al. 2009 emend. ART Spencer, SJ Wang, MT Dunn et J Hilton sp. nov. 1988 Stephanospermum cf. akenioides ZM Li – Unpublished PhD thesis, Institute of Botany, Chinese Academy of Sciences, Beijing; Pls 1–4; Pl 5, Fig. 1. 1991 Stephanospermum cf. akenioides ZM Li – Cathaya 3, 115– 133 – Figs. 1–20. 1995 Stephanospermum cf. akenioides– Pg. 62 in CS Li and JZ Cui (Eds.), Atlas of fossil plant anatomy in China. Science Press, Beijing. 2009 Stephanospermum trunctatum SJ Wang, KQ Sun, JZ Cui et SM Ma – Pgs 94–95 in SJ Wang, KQ Sun, JZ Cui and SM Ma, Fossil plants from coal balls in China. Higher Education press, China. Geological horizon: Wangjiazhai Formation of Southern China. Stratigraphic age: Changhsinghian, late Permian. Emended specific diagnosis: Seeds with obovate base and truncated apex comprising of 3 sclerotic teeth that are triangular in longitudinal section. Sclerotesta bilayered comprising an outer Fig. 5. Stratigraphical and phytogeographical distribution of species of the zone consisting of a uniseriate layer of columnar cells and an inner medullosan ovule Stephanospermum showing inferred timing of west to east migration from North America into China via Europe and suggested refugial zone with 5–10 layers of isodiametric cells. Nucellus free from settings. Data from sources listed in Table 1. integument except at the chalaza and with a low micropylar beak apically, with a net-like vascularisation. The outermost layer of during the Stephanospermum gap (Fig. 5). The most likely basins cells of the megagametophyte epidermis-like with thickened outer would have included the late Pennsylvanian Donets Basin (e.g. Sni- periclinal walls. girevskaya, 1972) or adjacent basins in the Pennsylvanian–Cisura- Holotype: Mounted peel GSW-CB-0013 from coal-ball GP2713-2. lian of southern Russia, and the Cisuralian aged wetlands of North Depository: Institute of Botany, Chinese Academy of Sciences, China (e.g. Hilton and Cleal, 2007; Stevens et al., 2011, Fig. 5). The Xiangshan, Beijing, PR China. fossil assemblages from the Donets Basin have not been studied in Remarks: In accordance with the International Code of Botanical detail to date but appear to include a typical ‘Euramerican’ styled Nomenclature (McNeill et al., 2012) the species Stephanospermum wetland plant community (e.g. Snigirevskaya, 1972; Hilton and trunctatum is validly published. However, here we correct the de- Cleal, 2007). By contrast the Cisuralian wetland floras of North Chi- tails of the holotype designated by Wang et al. (2009) that referred na have been studied in more detail (e.g. Tian et al., 1996; Hilton to the coal-ball rather than an individual specimen preserved in it, and Cleal, 2007; Wang et al., 2009; Stevens et al., 2011) but Step- designating the first peel illustrated as the holotype (Section 9.1, hanospermum has not been identified. We consider that Stephano- ex. 2). spermum represents a likely component of these floras that has not Furthermore, we have emended the diagnosis of Wang et al. yet been identified. Here it is important to recognise that even in (2009) by removing precise measurements that would prevent assemblages in which Stephanospermum occurs, it is uncommon additional specimens being placed within the species and through and infrequently encountered in surveys of coal-ball peels; the ab- adding the presence of ‘net-like’ tracheids in the nucellus that sence of Stephanospermum from the Donets Basin and North China shows it to be a species of Stephanospermum as currently defined. may be a consequence of the relatively poor sampling of these SpeciesStephanospermum shuichengensis ART Spencer, SJ Wang, successions. MT Dunn et J Hilton sp. nov. Geological horizon: Wangjiazhai Formation of Southern China. 5.4. Taphonomic considerations Stratigraphic age: Changhsinghian, late Permian. Specific diagnosis: Seeds with rounded based, broadly oval in In the fossil record seeds are frequently encountered lacking longitudinal section, displaying apical sarcotestal extensions. Sar- their outermost sarcotestal tissues (Wang et al., 2003, 2006) from cotesta bilayered with an outer dermal layer and an inner fleshy which differences in preservation potential between soft, fleshy layer. Outer sarcotesta composed of thick walled cells mostly cir- sarcotesta cells and harder, sclerotic, sclerotestal cells may be cumferentially oriented with occasional anastomosing. Elongated apparent. However, other processes may contribute to this includ- cells of the inner sarcotesta fleshy and oriented circumferentially. ing ontogenetic sloughing of the outer fleshy layers as seeds ma- Sclerotesta bilayered with outer sclerotesta forming a palisade of ture as interpreted for the Callistophytalean ovule cells radiating outward, whereas cells of the inner sclerotesta exhi- Callospermarion (Rothwell, 1971, 1980) and removal by digestive bit two distinct patterns (circumferentially oriented fibres at the A.R.T. Spencer et al. / Journal of Asian Earth Sciences 76 (2013) 59–69 69 contact area with the outer sclerotesta and interwoven internally). Hilton, J., Wang, S.-J., Zhu, W.-Q., Tian, B., Galtier, J., Wei, A.-H., 2002. Endotesta uniseriate and comprising of thin walled cells. Nucellus Callospermarion ovules from the Early Permian of northern China: palaeoforistic and palaeogeographic significance of callistophytalean seed– is free of the integument except at the base where it arises from a ferns in the Cathaysian Fora. Review of Palaeobotany and Palynology 120, 301– large vascular nucellar pad. Sheath of tracheids arises from the 314. nucellar vascular pad and surrounds the nucellus distally. Vascular Hoskins, J.H., Cross, A.T., 1946. Studies in the Trigonocarpales. Part II. Taxonomic problems and a revision of the genus Pachytesta. American Midland Naturalist bundles present in the sarcotesta of the apex. 36, 331–361. Holotype: 24 acetate film pulls numbered GSW-CB-0028 to Leisman, G.A., Roth, J., 1963. A reconsideration of Stephanospermum. Botanical GSW-CB-0052 from coal ball GSW-845-2. Gazette 124, 231–240. Li, Z.-M., 1988. The Preliminary Study on Seeds and Gigantopteris from Coal Balls in Depository: Institute of Botany, Chinese Academy of Sciences, China. Unpublished PhD Thesis, Institute of Botany, Chinese Academy of Xiangshan, Beijing. Sciences, Beijing, 1–77 & pls. 71–40. Etymology: The specific epithet is derived from the county of Li, Z.-M., 1991. Stephanospermum cf. akenoides Brongniart and Sarcospermum petiolulatum Z. M. Li sp. nov. in Chinese coal balls. Cathaya 3, 115–133. Shuicheng in which the Wangjiazhai Formation is found. Li, Z.-M., 1993. The genus Shuichengella gen. nov. and systematic classification of the Remarks: Stephanospermum shuichengensis sp. nov. is distin- order Osmundales. Review of Palaeobotany and Palynology 77, 51–63. guished from other species of Stephanospermum by having apical Li, C.-S., Cui, J.-Z., 1995. Atlas of Fossil Plant Anatomy in China. Science Press, Beijing, teeth formed from sarcotesta rather than sclerotesta, which occurs p. 132. McNeill, J., Barrie, F.R., Buck, W.R., Demoulin, V., Greuter, W., Hawksworth, D.L., in the species Stephanospermum akenioides, Stephanospermum tri- Herendeen, P.S., Knapp, S., Marhold, K., Prado, J., Prud’homme van Reine, W.F., dentatum, Stephanospermum elongatum, Stephanospermum ovoides, Smith, G.F., Wiersema, J.H., Turland, N.J., 2012. International Code of Stephanospermum caryoides and Stephanospermum konopeonus), Nomenclature for Algae, Fungi, and Plants (Melbourne Code), Adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. by having a bi-layered sarcotesta (unlike S. costatum and S. braid- Publ. 2012. Koeltz Scientific Books, Koenigstein, Germany, p. 240. woodensis), and lacking wings (unlike S. konopeonus and S. braid- Oliver, F.W., 1904. On the structure and affinities of Stephanospermum Brongniart, a woodensis) (see Table 1). genus of fossil gymnosperm seeds. Transactions of the Linnean Society of London. Botany 6, 361–400. Rothwell, G.W., 1971. Ontogeny of the Paleozoic Ovule, Callospermarion pusillum. Acknowledgements American Journal of Botany 58, 706–715. Rothwell, G.W., 1980. The Callistophytaceae (Pteridosperma). II. Reproductive features. Palaeontographica Abt. B Palaeophytol 173, 85–106. We thank Professor Wei-Qing Zhu for providing access to spec- Scott, A.C., Mattey, D.P., Howard, R., 1996. New data on the formation of imens and for discussion. Some of this work was funded as part of a Carboniferous coal balls. Review of Palaeobotany and Palynology 93, 317–331. PhD investigation by ARTS at Imperial College London. Work by Serbet, R., Rothwell, G.W., 1995. 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