CALLISTOPHYTALEAN PTERIDOSPERMS from PERMIAN AGED FLORAS of CHINA by LEYLA J

Home , Callistophytaceae, Callistophytales

[Palaeontology, Vol. 54, Part 2, 2011, pp. 287–302]

CALLISTOPHYTALEAN PTERIDOSPERMS FROM PERMIAN AGED FLORAS OF CHINA by LEYLA J. SEYFULLAH and JASON HILTON School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK; e-mails [email protected]; [email protected]

Typescript received 22 September 2009; accepted in revised form 5 April 2010

Abstract: Recent investigations into Permian aged floras Permian period in both North and South China, including from China have highlighted the widespread occurrence of the Upper Shihhotse Formation, Shihchienfeng Group, callistophytalean pteridosperms that challenge previous Xuanwei Formation, and possibly also in the mid-Pennsylva- understanding of their spatial and temporal distribution and nian Benxi Formation. Although macrofossil specimens are diversity. In China, the group spans the Permian period and uncommon elements in the assemblages that contain them, constitutes a distinctive but rare component in many peat- they demonstrate the continuity of callistophytalean pterido- forming environments. The stratigraphically earliest calli- sperms from the Pennsylvanian sub-period into the early stophytalean occurs in the Asselian-Sakmarian stages with Guadalupian epoch of the Permian in North China and into fossils from the Taiyuan Formation of northern China the Lopingian epoch of the Permian in South China. Of the including ovules of Callospermarion undulatum in coal ball species present, both Callistophyton boyssetii and Callosper- assemblages, and ovulate fronds of Norinosperma shanxiensis marion undulatum are known from the Pennsylvanian–earli- and synangiate fronds of Norinotheca shanxiensis in adpres- est Permian age floras of Euramerica, whereas Norinosperma, sion assemblages. More abundant in the fossil records are ad- Norinotheca and Emplectopteris appear to represent endemic pression remains from the Roadian-Wordian stages with the Cathaysian elements. Results imply that callistophytalean Lower Shihhotse Formation preserving abundant vegetative pteridosperms can no longer be excluded from theories of and ovulate remains of Emplectopteris triangularis that is now post-Carboniferous plant evolution and floristics, appearing considered to represent a callistophytalean. The youngest to have played an important role in both Permian and Car- callistophytalean recognised is from the Wuchaipingian- boniferous aged plant communities. The presence of Vesicas- Changhsingian stages with the Xuanwei Formation of pora in several formations from which macro-remains have southern China containing a single stem of Callistophyton not been identified is a hopeful indicator that further calli- boyssetii that provides indisputable evidence of the group in stophytalean pteridosperms are yet to be found. the lead up to the end-Permian mass extinction. These accounts are augmented by analysis of pollen records that Key words: Cathaysian flora, seed plant, pteridosperm, Cal- demonstrate the callistophytalean pollen genus Vesicaspora to listophyton, Callospermarion, Emplectopteris, Norinosperma, be widespread through palynological assemblages from the Norinotheca, Vesicaspora, extinction.

T he seed plant order Callistophytales is a rare but (Rothwell 1980, 1981). The C. poroxyloides plant occurs important group of Palaeozoic pteridosperms that lived only in the Pennsylvanian sub-period of North America in peat-forming mire settings and had scrambling ⁄ climb- but the C. boyssetii plant is known from the Pennsylva- ing habits (Rothwell 1981; DiMichele et al. 2006). They nian of North America and earliest Permian of France constitute the most comprehensively characterised pteri- (Rothwell 1975; Galtier 2008). Both whole plant species dosperm order following a series of detailed investigations comprise stems of Callistophyton Delevoryas and Morgan conducted by Rothwell based on anatomically preserved (1954), ovules of Callospermarion Eggert and Delevoryas specimens in coal balls from the Carboniferous system in (1960), pollen organs of Idanothekion Millay and Eggert North America and chert assemblages from the earliest (1970) containing Vesicaspora-type pollen, with the two Permian system of France (Rothwell 1971, 1972a, b, 1975, whole plants having organs attributable to the same genus 1977, 1980, 1981). From this work, two conceptual whole but as distinct species based on details of their morphol- plant species have now been reconstructed, namely, the ogy and histology (Rothwell 1981). In addition to two Callistophyton poroxyloides plant and the C. boyssetii plant reconstructed whole plant species, other species have been

ª The Palaeontological Association doi: 10.1111/j.1475-4983.2010.01025.x 287 288 PALAEONTOLOGY, VOLUME 54 assigned to the group including permineralised stems of 1975, 1981). The vascular cambium is bifacial and pro- Johnhallia lacunosa Stidd and Phillips (1982) from Penn- duced a cylinder of xylem and phloem, with periderm sylvanian coal balls of North America (Stidd and Phillips replacing the primary cortex at proximal levels in rela- 1982; DiMichele et al. 2006) and adpression foliage refer- tively old stems (Rothwell 1975, 1981). Callistophyton able to Dicksonites (Schlotheim ex Sternberg) Stertzel and poroxyloides has mesarch vascular bundles and capitate Pseudomariopteris busquetti (Danze´-Corsin) Krings and glands at the margin of the primary cortex differentiating Kerp from the Pennsylvanian sedimentary sequences of it from C. boyssetii that is exarch and has cortical append- Europe (e.g. Rothwell 1981; Krings et al. 2001; Galtier ages that are spine-like (Rothwell 1975, 1981). and Bethoux 2002). Stidd and Phillips (1982) considered In addition to being the most comprehensively recon- Johnhallia to represent a primitive member of the Callist- structed whole plant pteridosperm order that allows fea- ophytales, while Rothwell (1981) and Galtier and Bethoux tures of habit and ecology to be determined (Rothwell (2002) considered Dicksonites pluckenetii to represent the 1981; DiMichele et al. 2006), Callistophytales provide adpression foliage of the Callistophyton plant. Data from valuable information on the reproductive biology of pteri- morphology of Dicksonites suggest the frond had a basal dosperms, including pioneering discoveries on ovule dichotomy although this feature has not yet been verified ontogeny (Rothwell 1971), the oldest evidence of pollen from anatomical information. Evidence from the adpres- tubes (Rothwell 1972a) and pollination drops to facilitate sion record of Dicksonites suggests the presence of two pollination (Rothwell 1977). These studies have led to types that may be distinct species in their own rights, Callistophytales being considered the most reproductively based primarily on differences in the organisation of the sophisticated Palaeozoic pteridosperms (e.g. Rothwell seed-bearing pinnae (Meyen and Lemoigne 1986); while 1980, 1981), pushing back previously interpreted ‘mod- both kinds have fronds with a proximal dichotomy, older ern’ pollination strategies into the Carboniferous period. (Westphalian regional substage; upper Bashkirian to In terms of their evolutionary and phylogenetic impor- upper Moscovian stage) specimens have unmodified tance, they have been included in numerous cladistic fronds with ovules borne subapically on veins in the analyses as the terminal taxon Callistophyton. Cladistic pinnules, whereas in slightly younger (Stephanian regional results demonstrate Callistophyton to diverge from the substage; late Moscovian to Gzhelian stage) fertile fronds, stem after hydrasperman and medullosan pteridosperms ovules are attached subapically to strongly modified pinn- and prior to other, more derived, pteridosperm groups ules. However, it is uncertain whether the two kinds of and cycads (e.g. Rothwell and Serbet 1994; Doyle 2006; Dicksonites relate to the two whole plant species charac- Hilton and Bateman 2006). This position places Callisto- terised from anatomical data, or, whether they represent phyton at an important junction in seed plant evolution phenotypic variation within a single anatomical whole within pteridosperms but may also be of relevance to the plant species (Seyfullah and Hilton 2009: Seyfullah et al. origin of modern seed plant groups including cycads and 2009). Ginkgo. However, in these cladistic results Callistophyton As currently characterised, whole plant species of Cal- is proceeded by, and followed by, evolutionary long listophyton have been reconstructed as small, shrubby branches suggestive of missing taxa or saltational macro- plants with scrambling stems up to 30 mm in diameter evolution (e.g. Bateman and DiMichele 1994; Hilton and (Rothwell 1981). Fronds are small and rarely exceed Bateman 2006; Cleal et al. 2009). 300 mm long and are bipinnately quadrapinnately com- Based on data from North America and Europe, Cal- pound with sphenopterid pinnules (Rothwell 1975, 1981). listophytales first occurred in the middle of the Pennsyl- Branching is axillary with buds or branches borne in the vanian subsystem of the Carboniferous (Rothwell 1981), axils of leaves (Rothwell 1975, 1981). Roots are adventi- but experience a regional demise broadly coinciding with tious and diarch and diverge from the stem distally from the Carboniferous ⁄ Permian boundary (Rothwell 1981) axillary branches where the stem is in close proximity to and have their youngest occurrences in the earliest Perm- ground (Rothwell 1975, 1981). Reproductive organs are ian period of France (Galtier 2008). However, recent borne on the abaxial surface of relatively unmodified investigations highlight the presence of callistophytalean pinnules (Rothwell 1980, 1981) and consist of small car- pteridosperms in Permian age floras from China where diocarpalean ovules (Eggert and Develoryas 1960; Roth- they postdate the stratigraphically youngest macrofossil well 1971, 1981) and radially symmetrical pollen organs evidence recognised from Euramerica. In the present bearing saccate pollen (Rothwell 1972a, b, 1980). In terms paper, we summarise these accounts that are dispersed of its anatomical organisation and structure, the ground within various taxonomic and systematic treatments of tissues of all organs are characterised by ovoid secretory separate floras, provide a comprehensive review of the cavities (Rothwell 1975, 1981). Stems are eustelic with a total geographical and stratigraphical range for the group, parenchymatous pith and have a primary cortex with an and consider the evolutionary and phylogenetic implica- outer sparganum-type sclerenchymatous zone (Rothwell tions of these findings. SEYFULLAH AND HILTON: PERMIAN CALLISTOPHYTALES FROM CHINA 289

GEOLOGICAL INFORMATION termed the Taiyuan Formation. Here, we correct an over- sight of Seyfullah and Hilton (2009) that reported Nori- During the Permian period, modern-day China was com- nosperma and Norinotheca from incorrect localities. posed of several disjunct tectonic blocks that included Higher in the Taiyuan Formation, ovules assigned to separate North and South China landmasses together with Callospermarion undulatum (Neely) Rothwell occur in parts of Gondwana, Angara and Euramerica (Li and Wu coal balls from the Xiedao locality in Shanxi Province, 1996). The specimens documented here occur in the northern China (Tian et al. 1996) within the No. 7 Cisuralian-Guadalupian series of the Permian system in Xishan coal seam (Pan et al. 1985). The Taiyuan Forma- North China and in the Lopingian series of the Permian tion is considered to represent a series of interbedded system of South China (Text-Fig. 1), and in each region, paralic and continental deposits that are considered to be they constitute a distinctive though rare component of of Asselian-Sakmarian age (early Permian). This strati- wetland, peat-forming plant communities that developed graphic position is based on regional scale lithostrati- in lowland settings (Hilton et al. 2004; Hilton and Cleal graphic correlation and fusilinid biostratigraphy (Pan 2007). et al. 1985; Tian et al. 1996). Further details of the The oldest callistophytaleans recognised are from the Tiayuan Formation including its stratigraphic position Taiyuan Formation of North China that includes fertile and palaeobotanical composition were presented by Tian fronds occurring in compression ⁄ impression assemblages et al. (1996) and Hilton and Cleal (2007). at two different localities: with Norinosperma shanxiensis No callistophytalean plants have so far been identiﬁed Seyfullah and Hilton (2009) occurring at the Hei-tu-po from the Shanxi Formation that overlies the Taiyuan locality in Gaoping, Shansi (now Shanxi) Province Formation (Text-Fig. 1), but the callistophytalean species (Locality 77 of Norin 1922), and Norinotheca shanxiensis Emplectopteris triangularis Halle occurs in the overly- Seyfullah and Hilton (2009) at the Hou-ho-kou locality ing Lower Shihhotse Formation (Text-Fig. 1) in North also in Gaoping (Locality 89 of Norin 1922) as docu- China (Seyfullah and Hilton 2009). In the Shanxi regio- mented by Seyfullah and Hilton (2009). Both the Hou- nal sequence, E. triangularis occurs in beds 10, 14 and ho-kou and the Hei-tu-po localities expose Bed 2 of the 16 in the Eastern Hills section and beds 9 and 23 in Shanxi sedimentary succession, as documented by Norin the Western Hills section as documented by Norin (1922), that occurs towards the base of what he termed (1922) and Halle (1927). However, these ‘beds’ repre- the Yuehmenkou Coal Series (Norin 1922) that is now sent successions of beds that may include tens of

TEXT-FIG. 1. Summary of the upper Palaeozoic of North and South China showing approximate correlation of formations. Shaded boxes indicating presence of callistophytalean megafossils, asterisks show formations containing the callistophytalean pollen Vesicaspora. 290 PALAEONTOLOGY, VOLUME 54 metres of strata that in our view are equivalent to defined by Seyfullah and Hilton (2009), with specimens lithostratigraphic members within a formation (see also deposited in the Department of Palaeobotany, Swedish Glasspool et al. 2004). The Lower Shihhotse Formation Museum of Natural History, Stockholm, and numbered is assigned to the Kungurian to Roadian stages of the S138194 to 8 and S138385. Finally, a single stem of Callisto- Permian. Stratigraphic correlation is based on regional phyton boyssetii from the Xuanwei Formation was docu- scale lithostratigraphy and plant fossil biostratigraphy mented by Seyfullah et al. (2009) with mounted peels (see Shen 1995; Glasspool et al. 2004; Hilton and Cleal deposited at the Institute of Botany, Chinese Academy of 2007). Sciences, Beijing, and numbered ATop 01, BBot 01, BTop The youngest callistophytalean recognised is Callisto- 02-21, CBot 02-21, CTop 01-03 and DBot 01. phyton boyssetii collected from Huopu coal mine in Panxian County, Guizhou Province, South China, as previously reported by Seyfullah et al. (2009). This mine RESULTS extracts coal from the Xuanwei Formation that comprises continental sediments, paralic peat-forming mire deposits Ovulate fronds of Norinosperma shanxiensis from the with interbedded plant-bearing tuffs (Zhao et al. 1980; Taiyuan Formation adpression flora Yao et al. 1980; Shao et al. 1998). Stratigraphically, the Xuanwei Formation is referable to the Wuchiapingian to Norinosperma shanxiensis is monotypic and based on a Changhsingian stages of the Permian system (Text-Fig. 1), single informative specimen from the Hei-tu-po locality based on regional-scale correlation and fossil plant bio- in locality in Gaoping, Shansi (now Shanxi). In this spe- stratigraphy (see Wang et al. 2006). cies, only the ovule-bearing foliage is known, with the single specimen of this species either being a fragment of a frond or, more likely, the incomplete tip of a pinna MATERIALS (Seyfullah and Hilton 2009). The pinna rachis has prominent longitudinal striations and bears pinnules that are Ovules of Callospermarion undulatum from Taiyuan For- subalternate on the proximal part of the frond and sub- mation coal balls were previously documented by Wei opposite distally (Pl. 1, fig. 1). Pinnule shape varies from (1992) and Hilton et al. (2002) based on two specimens. ovate-circular to unevenly lobed and entire, and pinnule Of these, one is deposited in the palaeobotanical collections lobes are acutely angled and have secondary veins branch- of the Institute of Botany, Chinese Academy of Sciences, ing from the straight mid-vein. Secondary veins dichoto- Beijing, in 22 mounted serial peels numbered SC-2001-1 to mise unequally several times and continue to pinnule 22. The second specimen is deposited in the palaeobotani- margin. Norinosperma bears bilaterally symmetrical ovules cal collection of China University of Mining and Technol- either singly or in pairs (Pl. 1, figs 1–2), abaxially on the ogy, Beijing, preserved in two mounted peels labelled leaf lamina in the proximal portion of the frond. Ovules Shanxi-Cal1 and Shanxi-Cal2. From compression ⁄ impres- are positioned directly on the veins of a leaf lamina and sion assemblages in the Taiyuan Formation, Norinosperma are pendulous. Ovules are ovate, typically 4 mm long, shanxiensis and Norinotheca shanxiensis were documented with a rounded chalaza and attenuated apex (Pl. 1, fig. by Seyfullah and Hilton (2009) and are deposited in the 2). The surface of the ovule has fine striations originating department of Palaeobotany, Swedish Museum of Natural at point of attachment and spiralling clockwise to the History, Stockholm, with specimens numbered S147975 apex of the ovule (Pl. 1, fig. 2). and S147967 respectively. Characterisation of Emplectopter- Norinosperma is similar to the foliage of the callisto- is triangularis from the Lower Shihhotse Formation is phyalean pteridosperms Dicksonites and Emplectopteris based on descriptions provided by Halle (1927) and as re- (see below) in terms of venation pattern, pinnule shape,

EXPLANATION OF PLATE 1 Figs 1–4. Fertile foliage of the callistophytalean plants Norinosperma shanxiensis Seyfullah and Hilton and Norinotheca shanxiensis Seyfullah and Hilton from the Asselian–Sakmarian (lower Permian) Taiyuan Formation at Hei-tu-pu, Gaoping, Shanxi Province, China. 1, apical fragment of ovulate frond of Norinosperma shanxiensis with four seeds attached to the proximal pinnules (S147975, scale bar represents 5 mm). 2, enlargement from ﬁg. 1 showing cordate ovules preserved three dimensionally under the leaf lamina. 3, Apical fragment of synangiate frond with synangia plunging into sediment under leaf lamina (S147967, scale bar represents 10 mm). 4, enlargement from ﬁg. 3 showing enrolled leaf lamina revealing synangia in lateral (L) and apical (A) orientations (scale bar represents 5 mm). PLATE 1

3 4

L A

A L

SEYFULLAH and HILTON, Norinosperma shanxiensis 292 PALAEONTOLOGY, VOLUME 54 pinnule position and ovule morphology. In these genera, Norinotheca is most similar to other callistophytalean secondary veins dichotomise unequally several times and synangiate fronds with abaxial synangia with its gross continue to the pinnule margin, although in Norino- morphology being equivalent to those of Idanothekion sperma there is a distinct secondary vein arising from the (Millay and Eggert) Rothwell (Millay and Eggert 1970; pinnule rachis, while Emplectopteris and Dicksonites have Rothwell 1980), the permineralised equivalent of Dickso- an indistinct secondary vein that is the same strength as nites. Idanothekion synangia are approximately 1.5 mm that of the other veins within the pinnules. Emplectopteris long, radially symmetrical and contain between 6 and 8 has a further difference in its venation pattern as it pos- radially symmetrical sporangia, but there are key differ- sesses weakly anastomosing veins that are not known in ences. Fertile pinnules of Dicksonites bear up to six synan- either Dicksonites or Norinosperma. Foliage of Dicksonites gia per pinnule (Galtier and Bethoux 2002) whereas has pinnules that depart the main rachis at an angle of Norinotheca has only a single synangium per pinnule. The nearly 90 degrees whereas in Norinosperma they are very overall morphology of the pinnules is distinct from those acute. In both Dicksonites and Emplectopteris, ovules are of Dicksonites which has rounded pinnules that are less borne singly but in Norinosperma are borne both singly confluent than those of Norinotheca. Microsporangiate and in pairs. Ovules of each are cardiocarpalean in mor- pinnules of the callistophytalean Emplectopteris are pres- phology but those of Norinosperma lack prominent surfi- ently unknown preventing comparisons, but vegetative cial glands characteristic of both Emplectopteris and and ovulate foliage in this genus lack a single main vein Dicksonites, although faint small glands can be infre- and possess a series of veins that dichotomise twice and quently identified. Following Seyfullah and Hilton (2009), anastomose. This organisation is therefore also distinct we conclude that Norinosperma is a callistophytalean from Norinotheca. pteridosperm that is closely related to both Dicksonites Norinosperma and Norinotheca occur at separate locali- and Emplectopteris. ties in the same region but both within the same bed of the Taiyuan Formation. Considering their similar frond organisation and structure, and as both have indepen- Synangiate fronds of Norinotheca shanxiensis from the dently been assigned to the Callistophytales, Seyfullah and Taiyuan Formation adpression flora Hilton (2009) concluded that they most likely belong to the same plant species but taxonomic separation was Norinotheca shanxiensis is monotypic and based on three required as this could not be conclusively demonstrated. informative specimens from the Hou-ho-kou locality in Gaoping, Shanxi (formerly Shansi) Province. This locality is in close proximity to that in which Norinosperma occurs Callospermarion ovules from the Taiyuan Formation coal (see above), with both coming from ‘bed’ 2 of the Taiyuan balls Formation. As the three available specimens of this genus are closely associated with each other on a single slab, it is Two ovules of this species have been identified in the likely that they belong to a single individual. Each com- coal ball assemblage from the Taiyuan Formation (Hilton prises the apical parts of a fertile frond that bears numer- et al. 2002). Ovules are small, 3.2–3.6 mm wide in the ous abaxial synangia (Pl. 1, fig. 3). In gross morphology, major plane and 2.2–2.6 mm wide in the minor plane the apical frond portions are slightly elongate to triangular (Pl. 2, fig. 1), are ovate in transverse section towards the and bear pinnae alternately. Pinnules are rounded-oval in chalaza but may become ellipsoidal distally, and have outline and approximately 3 mm long and have a pinna 180 degrees rotational (bilateral) symmetry. The outer rachis that is longitudinally striated (Pl. 1, fig. 3). Individ- margin of the integument is irregular and undulate ual pinnules have confluent bases and secondary veins (Pl. 2, fig. 1), and a lateral rib is weakly developed in the depart singly from the mid-rib at an acute angle, with major plane corresponding to the position of the integu- pinnules decreasing in size towards the apex of the frond. mentary bundle (Pl. 2, figs 1–2). The integument consists Veins do not appear to anastomose and secondary veins of four layers: outermost a uniseriate epidermis, a sarc- do not divide. In Norinotheca, both proximal and distal otesa of variable thickness, sclerotesta, and innermost, a pinnules are fertile (Pl. 1, figs 3–4), with synangia posi- thin endotesta (Pl. 2, fig. 3). Within the integumentary tioned singly and underneath the secondary vein. There is cavity, a thin nucellus contains the megaspore that in one synangium per pinnule, and this is positioned half some places preserves tissues of the megagametophyte way along the pinnule. Synangia are radially symmetrical (Pl. 2, fig. 4). (Pl. 1, fig. 4) and comprise eight sporangia that appear to The sarcotesta comprises two zones that intergrade be fused to one another laterally for their entirety. Sporan- with each other; an inner zone of more or less constant gia have longitudinal striations and narrow to form a thickness and the outer varies and widens to form a lat- rounded apex (Pl. 1, fig. 4). eral rib and undulate integument (Pl. 2, figs 1, 3). At the SEYFULLAH AND HILTON: PERMIAN CALLISTOPHYTALES FROM CHINA 293 boundary of the inner and outer zone of the sarcotesta, the type specimen for the genus. Vegetative and fertile numerous spherical to slightly ovate secretory cavities are foliage have the same gross morphology with penultimate present (Pl. 2, figs 1, 5–7). Where well-preserved cavities pinnae subopposite or alternate and with a triangular to have 2–3 layers of rectangular, epithelial cells forming lanceolate outline, while ultimate pinnae are alternate or their border (Pl. 2, fig. 6) and in some cases contain subopposite on the rachis, and are ovate to lanceolate in spherical amber-coloured contents interpreted as resin shape and can be pinnate and pinnatifid or serrate (Pl. 3, (Pl. 2, fig. 5) while in other contain clusters of coprolites figs 1–4). Pinnules typically form an angle of about (Pl. 2, fig. 7) produced by orbatulid mites (Labandiera 30 degrees with the parent rachis (Pl. 3, fig. 3), and indi- et al. 1997). The sclerotesta is badly crushed but consists vidual pinnules are lanceolate to oblanceolate and acutely of 2–3 layers of small and axially elongated cells (Plate 2, pointed, tapering proximally, but attached by a rather fig. 2). Endotesta is also poorly preserved but is uniseriate broad decurrent base. Pinnules in the apical part of the and consists of large, thin-walled, isodiametric parenchy- frond and pinna are entire, growing more confluent matous cells. The base of the ovule has not been observed towards the apex and gradually changing into mere lobes but two integumentary bundles are present at the margin of the ultimate pinnae. By contrast, pinnules in the basal of the sclerotesta and sarcotesta in the major plane (Pl. 2, part of the frond are dissected into lobes that become figs 1–2), their position coinciding with the position of gradually more prominent proximally and finally pass the widest part of the sarcotesta and the lateral integu- into free pinnules of a higher order. Typical pinnules have mentary ribs. Each bundle is terete and consists of 10–15 fine median vein that is at an acute angle to the mid-vein scalariform tracheids. The nucellus is free from the integ- and in the larger lobed pinnules it often bifurcates. Where ument and is thin-walled, surrounding the megaspore seen secondary veins are almost equally thick as the med- (Pl. 2, fig. 3). Tissues of the megagametophyte are pre- ian vein. Pinnules and pinnule rachis have prominent served in a few places (Pl. 2, fig. 4). glands preserved that produce a speckled appearance to Hilton et al. (2002) identified the Taiyuan ovules as the leaf lamina (Pl. 3, figs 3, 6). the callistophytalean Callospermarion undulatum (Neely) Ovules are attached to the abaxial surface of the pin- Rothwell based on their gross morphology and anatomy, nule on the basal part of the first catadrome vein, its long specifically the undulate nature of the integument and axis generally forming on impression a narrow angle with the presence of numerous, large sarcotestal secretory the pinna-rachis (Pl. 3, fig. 4). Ovules are sessile to the cavities. Callospermarion undulatum and the Chinese pinnule and conform to the gross morphology of the dis- specimens have indistinct layering of the sarcotesta in persed genus Cornucarpus Arber produced by the dis- which larger cells occur towards the outer margin of the tantly related Eremopteris-bearing pteridospermalean plant ovules and both sets of specimens possess a uniseriate (Cleal et al. 2009). They are typically 4 mm long and endotesta. Although more is known about the course of 2 mm wide but the largest ovule observed is 7.5 mm long vascularisation in the Euramerican specimens, where and 4.5 mm wide (Halle, 1932, pl. 1 figs 2–4). Ovules are known these features are consistent with the Chinese platyspermic with 180 degrees rotational symmetry, have specimens which also possess two integumentary bundles a narrow integumentary wing and bicornute integumen- in the major plane situated between the sarcotesta and tary apex (Pl. 3, figs 5–6). The chalazal half of the ovule sclerotesta. The ovules differ from Callospermarion pusil- varies from ovate to elliptical and in this part of the ovule lum Eggert and Delevoryas (Eggert and Develoryas 1960; integumentary wings are narrow and are barely discern- Neely 1951; Rothwell 1980) that has a sarcotesta of able. Distally the wing widens and apically forms the ‘bi- more or less uniformly sized cells, is more distinctly cornute’ apex that comprises of two pointed triangular ribbed with the lateral ribs forming blunt, rounded cusps separated by a sharp sinus (Pl. 3, fig. 6). On the wings and rarely possesses glandular cavities in the surface of all the ovules identified occur small circular sarcotesta (Eggert and Develoryas 1960; Stidd and Hall black glands (arrow in Pl. 3, fig. 6) that are the same as 1970; Rothwell 1980). those on the pinna-rachis and pinnules (Pl. 3, figs 3, 6). Liu et al. (1996) reported a further four species of Em- plectopteris from the Permian floras of China, namely, Emplectopteris triangularis from the Shihhotse Formation E. tangshanensis Liu, Wang and Yao, E. neimongolensis compression ⁄ impression floras Huang, E. sinensis Huang and E. minima Huang. How- ever, these species come from a single locality and have The following account of Emplectopteris triangularis is features that overlap with each other, forming a contin- based on specimens from the Lower Shihhotse Formation uum, with this continuum overlapping with the features as documented by Halle (1927, 1929) and as recently re- of Emplectopteris triangularis from Shanxi Province. This investigated by Seyfullah and Hilton (2009) that included led Seyfullah and Hilton (2009) to consider these species 294 PALAEONTOLOGY, VOLUME 54 to represent a broad morphological range within a single Formation by Seyfullah et al. (2009). The specimen is species rather than representing multiple species. This small, 10 · 5 mm in transverse section (Pl. 4, fig. 1), conclusion is in line with increased understanding of the and preserves part of a single branch trace (Pl. 4, fig. 2). natural variation within species including ecophenotypic, The stem is eustelic and has a parenchymatous pith with ontogenetic and other subtle polymorphism in different discrete primary xylem strands at its periphery that is parts of the individual plants. surrounded by a large amount of secondary xylem In terms of its gross morphology, Emplectopteris triang- (Pl. 4, figs 1–2). The cortex is divided into an inner and ularis is most similar to Dicksonites pluckenetii (Schlotheim outer zone (Pl. 4, figs 3–4) and a vascular cambium is ex Sternberg) Sterzel, a species considered to represent present. The pith is partially crushed and contains small the compression ⁄ impression equivalent of Callistophyton clusters of irregular shaped thin-walled parenchyma cells, (Galtier and Bethoux 2002). Dicksonites pluckenetii differs some with amber contents, irregularly interspersed with in having pinnules that are less triangular and more lobed larger roughly circular secretory cells (Pl. 4, figs 5–6). (e.g. Galtier and Bethoux 2002) and lacks the triangular- Xylem bundles are typically crushed (Pl. 4, fig. 6). Leaf shaped intercalary pinnules seen in Emplectopteris. Fur- traces comprise a single protoxylem strand, possibly with thermore, Emplectopteris lacks the basal dichotomy in the parenchyma surrounded by metaxylem tracheids, but frond that characterises species of Dicksonites. Within more likely only on the centripetal side (Pl. 4, fig. 6). D. pluckenetii, Meyen and Lemoigne (1986) documented Xylem maturation is weakly exarch. The clearest traces two kinds of seed-bearing pinnae, in which specimens observed are a pair that occurs at the margin of the pith from the upper Bashkirian to upper Moscovian stage of (Pl. 4, fig. 6). Incipient leaf traces have a separate proto- the Carboniferous period have unmodified fronds with the xylem strand and are oval in section. Abundant second- seeds borne subapically on veins in the pinnules, whereas ary xylem is present, measuring 0.25 mm at its widest fronds of slightly younger specimens from the upper Mo- point (Pl. 4, figs 1–2). Tracheids of the secondary xylem scovian to upper Gzhelian stages of the Carboniferous sys- are regularly square in outline and vary between 38– tem show seeds attached subapically to strongly modified 62 lm long and wide. Secondary xylem is arranged in pinnules. The unmodified fertile fronds of E. triangularis files of 1–3 cells wide at the start, commonly 1 cell are closest to those of the younger specimens of D. plucke- wide, and files become wider as they extend to the netii although the pinnule morphology is distinct and the periphery of the stem where they can contain up to 5–6 ovules of Emplectopteris are winged. The overall morphol- rows of adjacent tracheids. Rays are poorly defined, nar- ogy of the frond and the morphology and position of the row and consist of crushed tissue visible between the ovules are consistent with features of callistophytalean files of tracheids; where they can be differentiated xylem pteridosperms (Seyfullah and Hilton, 2009). rays are 1–3 cells wide. Some tissues of the vascular cambium are preserved at the edge of the secondary xylem that is composed of layers of crushed cells. The Callistophyton boyssetii from epiclastic tuffs in the cortex is variably preserved with an inner parenchyma- Xuanwei Formation tous layer, a sparganum-type outer cortex with alternating bands of sclerenchyma and parenchyma (Pl. 4, figs A single specimen of this distinctive stem has recently 1, 3–4), a thin epidermis but lacks a preserved cuticle. been identified from epiclastic tuffs within the Xuanwei The inner cortex has a ground tissue of parenchyma

EXPLANATION OF PLATE 2 Figs 1–7. Callistophytalean ovules of Callospermarion undulatum (Neely) Rothwell from Asselian-Sakmarian (lower Permian) aged coal balls from the Taiyuan Formation at Xiedao, Shanxi Province, China. 1, transverse section showing undulate outer margin and weakly developed lateral rib in the major plane and numerous secretory cavities in the sarcotesta (slide Sc-2001-5, scale bar represents 1 mm). 2, enlargement from 1 showing poorly preserved integumentary bundle (scale bar represents 25 lm). 3, margin of ovule in transverse section showing position of vascular bundle and week rib in the major plane showing position of megaspore membrane (M), nucellus (N), endotesta (En), sclerotesta (Sc), sarcotesta (Sa) and vascular bundle (VB) (slide Cal-1, scale bar represents 100 lm). 4, nucellus (N), megaspore membrane (M) and tissues of the megagametophyte (MG) (slide Cal-1. 4, scale bar represents 200 lm). 5, secretory cavity containing resin (slide SC-2001-22, scale bar represents 100 lm). 6, enlargement from same specimen as ﬁg. 4 showing three closely spaced secretory cavities with well-preserved cellular differentiation and radially expanded sarcotesta cells (scale bar represents 100 lm). 7, secretory cavity containing numerous dark ovate coprolites (slide SC-2001-22, scale bar represents 100 lm). PLATE 2

1 2

34 N

Sc Sa M M VB Mg

En N

6 7 Sa

SEYFULLAH and HILTON, Callospermarion undulatum 296 PALAEONTOLOGY, VOLUME 54 cells that vary in size and some have amber contents Sporae dispersae Vesicaspora and scattered secretory cavities (Pl. 4, figs 1–3). A wedge-shaped disruption to the inner cortex is present The dispersed pollen genus Vesicaspora Schemel is widely that has muriform parenchyma and is interspersed with accepted as being the pollen of the Callistophyton plant as small files of primary xylem and is interpreted as a produced in Idanothekion type synangia (Millay and Egg- branch trace (Pl. 4, fig. 7), with secretory cells scattered ert 1974; Rothwell 1980; Taylor 1988) in Carboniferous through the tissue. The outer cortex has alternating System sediments in Euamerica. This kind of pollen bands of sclerenchyma and parenchyma (Pl. 4, fig. 3) has now been reported from the Permian sedimentary and is irregular in outline and with secretory cavities. A sequences of China where it appears widespread. For thin-walled, small-celled epidermal layer can be seen in instance, Li et al. (1995) recorded ‘Vesicaspora?’ within some sections; the cells have no contents. Cortical the mid-Pennsylvanian aged Penxi Formation (now Benxi appendages are seen and are partly responsible for the Formation, see Cleal and Wang 2002) of North China, irregularity of the cortical outline (Pl. 4, fig. 4). but this assignment requires validation as it was consid- The specimen from the Xuanwei Formation conforms ered tentative by those authors. Gao et al. (2000) included to the features of the Callistophyton and is indistinguish- Vesicaspora as a distinctive element within the Upper able from those of C. boyssetii (Renault) Rothwell. Permian (Lopingian series) assemblage from the Upper Systematically important similarities include a parenchy- Shihezi (= Shihhotse) Formation in Shangdong Province, matous pith with secretory cells, secondary xylem com- North China, and Hou and Ouyang (2000) documented posed of alternating files of tracheids and rays, and with it within the Sunjiangou Formation in Shanxi Province of tracheids being angular and arranged in files of 1–3 cells northern China that represents the basal-most formation that is typical for the genus although infrequently occur- in the Shihchienfeng Group (Text-Fig. 1). This account ring as files of 1–5 (Rothwell 1975). Rays are 1–3 cells from the Shihchienfeng Group leads us to suspect that wide in the Chinese stem, and 1–4 in species of Callisto- callistophytealean plants were also present in North China phyton. These slight variations in the tracheids files and towards the end of the Permian as they are in South rays in the Chinese stem could be related to the small China at this time. At present, the youngest macrofossil size of the stem and it being relatively immature, but evidence of callistophytalean plants in North China is these are within the ranges observed for Callistophyton Emplectopteris from the Lower Shihhotse Formation, (Rothwell 1975). Of the two species of Callistophyton stratigraphically older than the Lopingian aged Shihch- recognised from the Euramerican floras, only C. boyssetii ienfeng Group. has pith cells with amber contents in common with the Palynological work by Peng et al. (2006) confirmed the Chinese stem (Rothwell 1975). Further similarities with presence of Vesicaspora in the upper part of the Xuanwei C. boyssetii include exarch primary xylem maturation, Formation in South China and demonstrates the genus local amber-coloured cell contents within the paren- extends up to the Lower Triassic boundary in this region. chyma and cortical appendages that are spine-like with However, they noted that Vesicaspora is absent from the large basal regions tapering towards the apex. We are, Early Triassic sedimentary sequences inferring the genus, therefore, confident in our identification of the Chinese and in our view also the callistophytalean pteridosperms, stem as belonging to the callistophytalean pteridosperm became extinct in this region at the end-Permian mass Callistophyton and consider this an accurate identifica- extinction event (e.g. Wignall 2007). Other pollen types tion of the species C. boyssetii, with this account repre- recorded from the Xuanwei Formation by Peng et al. senting the stratigraphically youngest callistophytalean (2006) include trilete forms consistent with lyginopterid macrofossil yet identified. pteridosperms and monolete forms consistent with me-

EXPLANATION OF PLATE 3 Figs 1–6. The callistophytalean plant Emplectopteris triangularis (Halle) Seyfullah and Hilton from the Kungurian–Roadian (mid- Permian) Lower Shihhotse Formation, Taiyuan, Shanxi Province, China. 1, proximal portion of vegetative pinna with triangular intercalated pinnules on rachis between ultimate pinnae (S138197, scale bar represents 5 mm). 2, distal part of vegetative pinna shown in fig. 1 with characteristic weakly anastomosing venation (scale bar represents 5 mm). 3, ultimate pinnule from same specimen as figs 1–2 with characteristic glands and venation (scale bar represents 2 mm). 4, Ovulate pinna with attached ovules (S138385, scale bar represents 5 mm). 5, enlargement from fig. 4 showing ovules attached to the pinnule mid-vein (scale bar represents 5 mm). 6, delicate fertile frond, preserved under Canada-Balsam, with prominent glands visible on the pinna, pinnule rachises and attached ovule (arrow) (S38284, scale bar represents 5 mm). PLATE 3

1 2

SEYFULLAH and HILTON, Emplectopteris triangularis 298 PALAEONTOLOGY, VOLUME 54 dullosan pteridosperms, although in no case are more plant species as previously characterised from Pennsylva- detailed systematic affiliations with parent plants possible. nian to earliest Permian aged floras in Euramerica, Within China, Vesicaspora has been documented in namely the Callistophyton boyssetii plant, suggesting the several sub-Angaran rather than typical Cathaysian floral persistence of this plant species into the Permian of associations according to the floristic segregation pro- China. However, additional organs of the C. boyssetii posed by Li and Wu (1996). For instance, Li et al. (1995) plant such as the pollen organs (Idanothekion glandulo- included Vesicaspora in the palynofloral assemblages from sum) have not been found from China, and this logic is the Guadalupian–Lopingian stage sedimentary sequences placed in a cautionary context that the presence of indi- from the Junggar Basin in Xianjiang Province, and Zhu vidual organ species may not directly equate to the pres- et al. (2005) illustrated Vesicaspora acrifera (Andreyeva) ence of the same whole plant species (e.g. Rothwell 1988; Hart from the Wu’erhe Formation (Guadalupian–Lopin- Trivett and Rothwell 1991; Bateman and Hilton 2009). gian stages) in Xiazijie, Hebuksair County, Xinjiang Prov- To date, no organs unquestionably belonging to the ince of NW China, and Vesicaspora sp. from the Roadian Callistophton poroxyloides plant have been identified from to Wordian stages in the Bieyoulieti Formation in Xianji- Permian aged floras in China. ang Province. These occurrences are important as they In addition to the organs of the Callistophyton boyssetii demonstrate the presence of callistophytalean pollen in plant, the Permian floras of China contain other evidence Angaran-type associations and suggest that callistophyta- of callistophytalean pteridosperms, namely Norinosperma lean plants also occurred in that floristic region, possibly shanxiensis and Norinotheca shanxiensis from the Taiyuan in a floristic context linking Euramerica with China as Formation and Emplectopteris triangularis from the Lower postulated by Hilton and Cleal (2007). These findings also Shihhotse Formation. Each appears to represent an ende- raise the possibility of future discoveries of callistophyta- mic Cathaysian species and suggests diversification within lean plants in the Permian floras of Angara. the group during the Permian period. Unfortunately, anatomy is unknown in each of these species; hence, it is uncertain whether Emplectopteris had a distinctive anat- DISCUSSION omy or was similar to other callistophytalen stems and fronds such as Callistophyton poroxyloides, C. boyssetii or Although the evidence presented here on species from the Johnhallia. It is similarly uncertain whether Norinosperma Permian floras of China is based on low specimen num- and Norinotheca had anatomy consistent with previously bers, in each case the specimens available are sufficient to recognised members of the group. In this regard, the stem document convincingly the presence of callistophytalean of C. boyssetii from the Xuanwei Formation could feasibly pteridosperms. In two cases, the Chinese Permian organ belong to either the whole plant C. boyssetii as currently species (see Bateman and Hilton 2009) are the same as characterised (e.g. Rothwell 1975, 1980, 1981) or it may those previously recorded in the Pennsylvanian of Europe represent the stem of an emplectopterid callistophytalean and North America, namely, the ovule Callospermarion for which anatomy is presently unknown. Frond architec- undulatum from the Taiyuan Formation and the stem ture is not available from the stem of Callistophyton boyss- Callistophyton boyssetii from the Xuanwei Formation. etii from the Xuanwei Formation to further consider this These species are rare in Pennsylvanian peat-forming mire possibility. communities in Euramerica and the same appears to be Emplectopteris is somewhat similar to the Cathaysian true in China, albeit based on a less extensive history of plant Emplectopteridium alatum Kawasaki, but more clo- coal ball research (as summarised by Tian et al. 1996). It sely resembles species of the medullosan Callipteridium is apparent that both species belong to the same whole (Weiss) Grand’Eury in terms of its frond and pinnule

EXPLANATION OF PLATE 4 Figs 1–7. The callistophytalean stem Callistophyton boysetii from the upper Permian (Wuchapingian–Changhsingian) Xuanwei Formation of Guizhou Province, southern China. 1, stem showing organisation and partial envelope of sparganum-type outer cortex (slide BTop ⁄ 20, scale bar represents 1 mm). 2, stem at different level to ﬁg. 1 showing less outer cortex but with inner cortex and pith well preserved (slide CBot ⁄ 20, scale bar represents 1 mm). 3, sparganum-type outer cortex of alternating bands of parenchyma and sclerenchyma and showing secretory cell (Slide BTop ⁄ 20, scale bar represents 200 lm). 4, multicellular epidermal gland (slide BTop ⁄ 20, scale bar represents 250 lm). 5, enlargement from ﬁg. 1 showing pair of traces with the possible parenchyma strand arrowed (slide BTop ⁄ 6, scale bar represents 500 lm). 6, pair of traces (arrowed) where pith is no longer preserved (slide BTop ⁄ 6, scale bar represents 500 lm). 7, tissues of the large trace in inner cortex showing parenchyma, xylem and secretory cells (Slide CBot ⁄ 10, scale bar represents 500 lm). PLATE 4

2 3

5 6 7

SEYFULLAH and HILTON, Callistophyton boysetii 300 PALAEONTOLOGY, VOLUME 54 morphology. Similarities between Emplectopteris and Em- from post-Carboniferous theories of plant evolution and plectopteridium were noted by Kawasaki (1927) based on floristics, and it appears to have played an important role the presence of the intercalary pinnules, but Emplectopter- in both Permian and Carboniferous aged plant communi- is has a more or less decurrent midrib, with veins arising ties. The available macrofossil evidence from South solely from the midrib while Emplectopteridium has a China, in agreement with the playnofloral record from straight midrib and veins can arise from both the mid- the same region (Peng et al. 2006), suggests that the Cal- rib and the pinna-rachis; here, we note the difference in listophytales became extinct at the end of the Permian. frond architecture between meduollosan and callisto- This report therefore adds another plant group to those phytalean plants reliably distinguishes the groups. In that went extinct in this mass extinction event, apparently certain earlier works, Emplectopteris triangularis was asso- not surviving into the Mesozoic. ciated with other Palaeozoic pteridosperm foliage includ- The sporae dispersae genus Vesicaspora inferred to origi- ing the Cathaysian plant Emplectopteridium alatum nate from callistophytalean pteridosperms is found from Kawasaki and these plants were interpreted as showing the early Desmoinesian (= latest Bolsovian – early Asturi- theoretical patterns in frond and pinnule evolution (e.g. an, mid-Moscovian) based on the distribution of the spe- Asama 1982). Asama’s theories are now recognised as cies V. wilsonii in Euramerica (D. Mclean, pers. comm. forming a transformational series in distantly related taxa, 2009). During the Bolsovian (Mid-Moscovian), evidence representing convergent features of leaf physiognomy of callistophytalean macrofossils are rare but include the rather than evolutionary descent within a single lineage. poorly known species Dicksonites geisheckii from Saar-Lor- Based on the available information on Emplectopteridium, raine and D. irregularis from Central Bohemia (Wagner we are uncertain of its affinity but consider it a possible 1971; C. J. Cleal, pers. comm. 2009), lending support to contender as a callistophytalean; the genus clearly war- the palynological evidence of Vesicaspora at this time. rants further investigation to determine its systematic and Vesicaspora is here shown to occur through the Perm- phylogenetic significance. Callipteridium possesses mesh ian of North and South China, but the genus ranges up venation and a small intercalary pinnule and is further into the Middle or Late Triassic in other places, suggest- distinguished from Emplectopteris by its basal frond ing the group had more widespread distribution. For dichotomy, intercalated pinnae on the primary rachis instance, Jha and Jha (1996) reported Vesicaspora in branches, and cyclopterid foliage segments. However, Permian-aged Gondwanan coals from India from which stratigraphically younger species of Callipteridium have Callistophytales have not previously been identified from intercalated pinnules on their ultimate rachises as in Em- macrofloral evidence. Furthermore, Zavattieri et al. (2003) plectopteris, but this represents parallel evolution of this reported Vesicaspora from the Late Triassic of Chile and feature in a distinct lineage rather than an affinity with as part of a Gondwanan flora, that if correct, represents Emplectopteris. the highest stratigraphical occurrence of the genus we are Krings et al. (2001) inferred Pseudomariopteris busquetti aware of and suggests a considerably extended range for (Danze´-Corsin) Krings and Kerp, from the Pennsylvanian callistophytalean plants in Gondwana. However, in our and Lower Permian of France and Germany, to represent view this remains speculative and requires detailed sys- a callistophytalean based primarily on its similarity with tematic investigations before being universally accepted as Dicksonites, including features of ovule position and frond Late Triassic evidence for callistophytalean pteridosperms. architecture. As far as the present authors are aware, Pseudomariopteris has not been identified from the Palae- Acknowledgements. We thank Jean Galtier (CIRAD, Montpel- ozoic floras of China. lier), Jun Wang (Nanjing Institute of Geology and Palaeontolo- The data summarised here on callistophytalean plants gy) and Shi-Jun Wang (Institute of Botany, Chinese Academy of from the Permian floras of China are important as these Sciences, Beijing) for discussion, D. Mclean (MB Biostratigra- significantly extend the stratigraphic range of calli- phy) for palynological consultations, and Chris Cleal (National Museum, Cardiff) and Stephen McLoughlin (Swedish Museum stophytalean pteridosperms that can no longer be thought of Natural History) for reviewing the manuscript. Parts of this to have become extinct broadly coinciding with the Car- study were undertaken as part LJS’s doctoral thesis supported by boniferous-Permian boundary. Previous evidence from the University of Birmingham, and access to the collections at Europe and North America on their regional demise is the NRM (Stockholm) were supported by Synthesys Award SE- coincident with large-scale changes in sedimentary facies TAF 112 for which Else Marie Friis, David Cantrill (now Royal in which apparent changes in floral composition reflect Botanic Gardens, Melbourne) and the staff at the Paleobotanical changes in plant geographical distributions rather than an Department are thanked. Fieldwork to collect specimens from extinction episode (Cleal and Wang 2002; Hilton et al. the Xuanwei Formation was enabled by NERC (Award 2002; Hilton and Cleal 2007). The extended range of Cal- NE ⁄ D011094 ⁄ 1). listophytales, combined with its added diversity during Editor. Chris Berry the Permian, means the group can no longer be excluded SEYFULLAH AND HILTON: PERMIAN CALLISTOPHYTALES FROM CHINA 301

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