Introduction

The earliest persuasive records of bennettitaleans come from the Late Triassic (Leuthardt 1903; Kräusel and Schaarschmidt 1966; Anderson and Anderson 1989, 2003; Pott et al. 2007c, d). Examples from the Molteno Formation in South Africa are considered to be early to middle Carnian (Anderson and Anderson 2003), whereas those from Lunz, Austria, and Neuewelt, Switzerland, are slightly younger (late Carnian; Cleal 1993; Taylor et al. 2009). Bennettitaleans were widespread and abundant in the Late Triassic-Middle Jurassic, remained locally common in the Late Jurassic and Early Cretaceous, and apparently became extinct in the Late Cretaceous (Mägdefrau 1968; Willis and McElwain 2002). Bennettitaleans reported from older deposits (i.e., pre-Carnian assemblages) need to be considered with caution, since most of those species lack studied or preserved cuticles. The accommodation of species such as Pterophyllum cultelliforme Sze, 1936, Pt. cottaeanum Gutbier, 1835, Pt. blechnoides Sandberger, 1864, Pt. daihoense Kawasaki, 1934, Pt. pruvostii Stockmans and Mathieu, 1939, Pt. fayolii Renault and Zeiller, 1890, Pt. grandeuryi Saporta and Marion, 1885 (taxa names in caption of fig. 58 on p. 109 erroneously swapped) or Pt. eratum Gu and Zhi, 1974 from the Pennsylvanian and Permian of China, Korea, Germany and France in the genus Pterophyllum and thus, in the Bennettitales, remains equivocal.

Although the oldest compelling cycad foliage fossils (i.e., Pseudoctenis) in the Northern Hemisphere derive from the late Carnian (Pott et al. 2007b), the earliest evidence for this genus in the Southern Hemisphere is from the early Carnian (e.g., from the Molteno Formation, cf. Anderson and Anderson 1989). Reports of Pseudoctenis from other early Late Triassic floras (e.g., from the Santa Juan Formation, cf. Leppe and Moisan 2003; Nielsen 2005) are questionable because the macromorphology of the fossils closely corresponds to that of certain Pterophyllum species rather than to Pseudoctenis, and data on the epidermal anatomy are missing. The earliest unequivocal reproductive organs of the true cycads come from the Permian of China (i.e., Primocycas chinensis Zhu and Du, 1981; but compare Norinia cucullata Halle, 1927) and cycad-like foliage was reported from closely related deposits. Gao and Thomas (1989) assumed that foliage assigned to Yuania might be linked to Primocycas megasporophylls due to their occurrence in equivalent beds but since Yuania is now considered to be a noeggerathian, a search for other foliage belonging to the Primocycas plant is needed.

Fig. 1.

Map of NE China and Korea showing the localities from which Pseudoctenis samchokense fossils have been collected (grey symbols) and the locality from which Primocycas chinensis fossils have been described (black symbol).

Many cycadalean and bennettitalean leaves are macromorphologically similar, and can usually be distinguished only on epidermal anatomy following the pioneering work of Thomas and Bancroft (1913). Stomatal morphology is especially significant in the discrimination of the two foliage types (Florin 1933; Martens 1971). Bennettitalean leaves are characterised by syndetocheilic stomata, whereas cycadalean leaves possess haplocheilic stomata. These terms were introduced by Florin (1933), and refer to the development (cellular division) and the resulting morphotype of the stomatal apparatus. However, today the term “brachyparacytic” is the preferred term for bennettitalean stomatal architecture (Martens 1971; Crane 1988; LAWG 1999), rather than the ontogenetic term “syndetocheilic” (Thomas and Bancroft 1913; Florin 1933). Within the gymnosperms, the stomatal type of the Bennettitales is regarded as an autapomorphy with the exception of its occurrence (probably via homoplasy) in two enigmatic groups (i.e., the Welwitschiaceae and the Gnetaceae).

Since the record of possible Pterophyllum species (and other potential bennettitaleans) from Permian and Carboniferous deposits, mainly from south-eastern and eastern Asia, has increased in recent decades (up to 20 species known to us; see references below), critical evaluation of the morphology and relationships of these fossils is necessary. Here, we describe fossils from the Permo-Carboniferous of China held in the collections of the NRM that were originally assigned to the Bennettitales but yield cuticles with non-bennettitalean stomata. Although the cuticles are very brittle and poorly preserved, they provide useful information to clearly separate these leaves from the bennettitaleans, thus calling into question the identifications of other reported Palaeozoic Pterophyllum species.

Material and methods

The twenty-six studied specimens (specimen numbers given below) housed in the NRM were collected almost 90 years ago at three localities in northern China (Fig. 1). The specimen from Linxi (also spelt Linsi or Linshi), Tangshan area, Hebei, was collected in 1920 by Yao. Eight specimens from Yangjialiang (also spelt Yang-chia-liang), approximately 45 km to the south and 1.5 km to the west of Baode in the valley of Paloukou, north-western Shanxi, were collected in 1921 by T.C. Wang. Seventeen specimens from Damugou (also spelt Ta-mu-kou) near Hua-pi-chuang, Gaoping district, southeastern Shanxi, were obtained by an anonymous collector (accessioned in 1929).

Hand specimens were photographed with a high-resolution Nikon D80 digital camera using polarised light to increase contrast (Schaarschmidt 1973; Crabb 2001). The use of polarised light and high resolution imaging revealed several details (venation, raised surface structures) that are indiscernible to the naked eye. To make the cuticular features visible before destroying the specimens for cuticular analysis, a Leica Diaplan epifluorescence microscope was used. Cuticles were prepared according to procedures outlined by Kerp (1990) and Kerp and Krings (1999). Rock samples with plant remains were dissolved in hydrofluoric acid (40% HF) in order to remove the sediment. Cuticles were macerated according to the standard procedure using Schulze's reagent (35% HNO₃ with a few crystals of KC1O₃) and 5–10% potassium hydroxide (KOH). Macerated cuticles were washed in distilled water, gently dehydrated in pure glycerine, and finally mounted in permanent glycerine-jelly microscope slides.

Geological setting

Shallow marine and continental coal-bearing strata were deposited extensively across the North China Platform through the Pennsylvanian and Permian. These deposits can be broadly subdivided on lithological criteria into several formations, each unit being generally greater than 100 m in thickness, as summarised by Yang (1986a, b). These formations can be correlated between several basins and structural outliers across northern China on the basis of their macrofloral, palynofloral and invertebrate fossil content (Shen 1995; Wu 1995; Shen et al. 2006; Liu et al. 2008). However, precise stratigraphic placement of assemblages from historical collections, such as the material described herein, remains difficult where precise locality details are lacking and where local mapping of lithostratigraphic units is inadequate. Given these limitations, we tentatively ascribe stratigraphic positions and ages for the studied material on the basis of associated macrofossils as outlined below. All studied assemblages derive from the North China-Cathaysian palaeofloristic subprovince of Li and Wu (1996).

Linxi (Tangshan area).—Fossiliferous coal-bearing strata of the Linxi area, Hebei, were assigned to the Kaiping Series/ Formation by Stockmans and Mathieu (1939) and are considered to be broadly correlative with the Taiyuan Formation (Wu 1995). Most of the fossils from this site in the NRM collections provide poor age constraints being only identifiable to generic level (e.g., Neuropteris, Annularia, Sphenophyllum, Cordaites, Pecopteris, and Samaropsis spp.). However, the absence of typical Permian taxa (e.g., Taeniopteris, Callipteridium, Emplecopteridium or Emplecopteris) favours a Pennsylvanian (Stephanian or Gzhelian) age for this assemblage, and correlation with the lower part of the Taiyuan Formation (Wu 1995).

Yangjialiang (south of Baode).—This site is located in exposures of late Palaeozoic strata on the northeastern margin of the Ordos Basin. The coal-rich strata of the Shanxi Formation (palynologically dated as Artinskian-Kungurian; Liu et al. 2008) are the most likely source of the fossils from this site based on the presence of taxa such as Taeniopteris, Protoblechnum, and Neuropteris spp. and the absence of Lobatannularia, Gigantonoclea, and Gigantopteris, which mostly characterize Upper Permian strata in this region (Shen 1995).

Damugou (Gaoping area).—This site is near the margin of the Quinshi-Linfen Basin, in which the main coal-bearing units are the Taiyuan and Shanxi formations (Shao et al. 2007). The fossil assemblage includes Alethopteris ascendens, Sphenophyllum thonii, Pecopteris orientalis, Emplecopteridium alatum, Odontopteris subcrenulata, and Aphlebia sp. On the basis of the stratigraphiC ranges of taxa outlined by Shen (1995) and the absence of Lobatannularia and gigantopterids, the assemblage most likely derives from the Shanxi Formation (Artinskian-Kungurian). However, a younger age (from the Guadalupian Lower Shihezi Formation) can not be excluded.

Systematic palaeobotany

Fig. 2.

Leaves of cycadalean Pseudoctenis samchokense (Kawasaki, 1934) from Damugou, Gaoping, Shanxi, China. A. NRM S143500-02. B. NRM S143504. C. NRM S143503a. D. NRM S143505. E. NRM S143510. Scale bars 10 mm; arrows indicating prominent petiole and rachis.

Fig. 3.

Different leaves of cycadalean Pseudoctenis samchokense (Kawasaki, 1934); from Damugou, Gaoping (A, B, E), Yangjialiang, Baode, Shanxi (C, F), and Linxi (Tangshan area), Hebei (D), China. A. NRM S143507. B. Enlargement of NRM S143500-02; cf. Fig. 2A. C. NRM S141652 (epitype). D. NRM S146368; E. NRM S143502; F. NRM S141653 (epitype). Scale bars 10 mm; arrows indicating venation details and lateral insertion of decurrent leaflets.

Discussion

Permian cycads.—None of the Permian-Carboniferous species assigned to Pterophyllum (see below), except Pt. grandeuryi and Pt. pruvostii, is similar to Pseudoctenis samchokense in gross macromorphology. Although cuticle details are lacking, we regard Pt. pruvostii from Tangshan (Hebei, China; Stockmans and Mathieu 1939; Gu and Zhi 1974) as most likely conspecific with Ps. samchokense based on macromorphological features and dimensions. Although Pt. pruvostii has wider interspaces between the leaflets and the material figured by Stockmans and Mathieu (1939) is somewhat incomplete, the wider spacing of the leaflets can be caused by growth conditions as demonstrated for Pt. filicoides (Schlotheim, 1822) Zeiller, 1906 from the Upper Triassic of Austria (Pott et al. 2007d). Pterophyllum grandeuryi from the Permian of Blanzy, France (Saporta and Marion 1885) is also very similar to Ps. samchokense in overall morphology, dimensions and epidermal cell pattern. Zeiller (1906) figured some schematic drawings of cuticular remains he obtained from the original specimens of Pt. grandeuryi and Thomas (1930) described the epidermal anatomy of this species in more detail although he mainly referred to the schematic illustrations by Zeiller (1906). Thomas (1930) interpreted the stomata in the drawings and in his own preparations as sunken with up to five thickened subsidiary cells arranged in a circle around the pit. This is not the architecture of a brachyparacytic (syndetocheilic) stoma, hence, Thomas (1930) correctly compared Pt. grandeuryi with Nilssonia mediana (Leckenby, 1864) Nathorst, 1878 from the Jurassic of Scarborough, UK. The stomatal architecture described by Thomas (1930) assigns Pt. grandeuryi clearly to a non-bennettitalean genus. We refrain from regarding Pt. grandeuryi as conspecific with Ps. samchokense due to differences in the architecture of the stomata (i.e., sunken stomata and thickened subsidiary cells in the former). Moreover, Pt. grandeuryi has epidermal anatomy more similar to Pseudoctenis cornelii Pott, Kerp, and Krings, 2007, described from the Carnian of Austria (Pott et al. 2007b).

Dioonites densinervis Halle, 1927 from the Permian of the Taiyuan-Fu area in the Shanxi district of China (Halle 1927) is also broadly similar to Pseudoctenis samchokense. However, leaves of D. densinervis are distinctly smaller (about one-third of the size) than those of the latter and also differ in having leaflet bases that are decurrent on both the acropetal and basipetal margins. This species was erroneously transferred to Nilssonia densinervis by Stockmans and Mathieu (1939) and later illegitimately named N. huabeiensis by Gu and Zhi (1974). Indeed, both views can not be accepted, since Nilssonia is characterised by leaflet insertion on the upper side of the rachis (Pott et al. 2007a), which is not visible in the original specimens, and a cycadalean nature of the epidermis/cuticle is unproven since the specimens do not yield cuticles. Hence, retention of this species in Dioonites is recommended.

Cycad or cycad-like remains from Permian deposits are rare; there are only a few species of cycadophyte foliage formally described. Species broadly similar to Pseudoctenis samchokense include Ps. middridgensis Stoneley, 1958, from the UK, several Zamites species from Commentry, France, described by Renault and Zeiller (1890), and some species from China assigned to Nilssonia, Yuania, Tingia, and Plagiozamites (Halle 1927; Ghu and Zhi 1974; see Wang and Shen 2000; Taylor et al. 2009). Pseudoctenis middridgensis from the Upper Permian (Thuringian) of England is based on a single specimen that yielded only small, ill-preserved cuticle fragments from the rachis, and Stoneley (1958) noted that, in the absence of adequate knowledge of the epidermal anatomy, assignment of this fossil to Pseudoctenis must be considered provisional. The identities of most of the Chinese Nilssonia species are questionable since the figures do not provide sufficient details for confident generic or specific assignment. Moreover, N. huabeiensis is illegitimate (see above). The Zamites remains from France are in almost all cases preserved only as single leaflets and appropriate assignment remains equivocal. The genera Yuania, Tingia, and Plagiozamites, historically included by some researchers in the Cycadales, are better assigned to the Noeggerathiales, an order recently placed in the progymnosperms based on the organisation of their sporophylls and other reproductive organs (Taylor et al. 2009). Historically, the poorly understood Noeggerathiales have been included within the cycads by some workers (cf. Taylor et al. 2009). However, none of the mentioned genera includes foliage that is rudimentarily comparable to the leaves described herein apart from their basic segmented (pinnate) plan.

Fig. 4.

Cuticle details of cycadalean Pseudoctenis samchokense (Kawasaki, 1934); from Yangjialiang, Baode, Shanxi, China. A. NRM S141652-001, adaxial cuticle overview. B. NRM S141652-002, two adjacent stomata in the abaxial cuticle (B₁); different focus (B₂), stomata on the abaxial cuticle (B₃), arrows point to subsidiary cells in B₃. C. NRM S141652-003, abaxial cuticle overview (C₁), arrows pointing to stomata; enlargement on abaxial cuticle (C₂), arrows pointing to stomata; two adjacent stomata in the abaxial cuticle (C₃). Scale bars 10 µm in B₁–B₃ C₃, and 50 µm in A, C₁, C₂.

Several studies have reported rare examples of pinnate, cycad-like foliage from the Permian of Gondwana (e.g., McLoughlin 1992). The best preserved of these fossils is Pteronilssonia gopalii Pant and Mehra, 1963 from the Late Permian of India. That species is broadly similar to Pseudoctenis samchokense in its leaflet dimensions and venation style but differs in having leaflet bases that are decurrent on both the acropetal and basipetal margins. It also has strongly sinuous epidermal cell walls and prominent papillae on the subsidiary cells. On this basis it is considered to represent an atypical compound glossopterid leaf rather than a cycad (Pant 1982).

Since the generic attribution of Pseudoctenis middridgensis is equivocal, the next most similar species to Ps. samchokense is Ps. cornelii from the Carnian of Austria, which to date is the earliest record of a Pseudoctenis species in the Northern Hemisphere (Pott et al. 2007b). Both species agree in several characters (i.e., leaflet size, outline, insertion, gross architecture and size) but differ mainly in the details of their epidermal anatomy (e.g., architecture and position of the stomata, cell wall shape) and the great disparity in their ages. Therefore, a close relationship is not assumed.

If Primocycas chinensis is accepted as the oldest cycad reproductive structure to date, Pseudoctenis samchokense may be regarded as the oldest cycad foliage species. Bennettitaleans appeared, based on our survey of published data, not before the Middle to Late Triassic and were completely absent during the Palaeozoic even if the sudden mass abundance of bennettitaleans in the floras from Lunz and Neuewelt (Kräusel and Schaarschmidt 1966; Pott et al. 2007c, d, 2008) requires that bennettitaleans had originated earlier than the Carnian.

Alleged Permian bennettitaleans.—Since several fossils from Carboniferous or Permian deposits, including the leaves described here, have been described as possible bennettitalean remains, we re-evaluated reports of the oldest pre-Carnian bennettitaleans. Bennettitaleans first arose in noteworthy abundance during the Carnian (e.g., Anderson and Anderson 1989; Pott et al. 2007c, d). Almost all of the reports of bennettitaleans from older floras are unconvincing since, in most cases, cuticles are lacking or were not described. As the epidermal details identified in this study reveal, reports of bennettitalean foliage from older deposits should be considered equivocal if based on macromorphology alone.

At least 27 species of Pterophyllum have been formally described from Upper Carboniferous and Permian deposits (see also Table 1). Most of these derive from Western Europe, eastern Russia, East Asia and Laos (Table 1). In the Late Palaeozoic, these regions belonged to the Euramerican, Angaran (Siberian and Far East), and Cathaysian (N and S China) phytogeographic provinces (Chaloner and Meyen 1973; Wang and Shen 1996). Assignment of any of these species to Pterophyllum and thereby to the Bennettitales is doubtful. On the basis of the available macromorphological characters and their incompletely known or unknown epidermal anatomies, all species ought to be assigned to Dioonites (Halle 1927; Johanna H.A. van Konijnenburg-van Cittert, personal communication 2008) whose higher level taxonomic affinities are unclear. We finally compare these species to Pseudoctenis samchokense because of their similar age and original assignment to Pterophyllum. Of these, Pt. pruvostii is considered conspecific with Ps. samchokense (see above).

Six species have been described from Permian-Carboniferous deposits of central Europe. The simple descriptions and schematic illustrations of Pterophyllum cottaeanum (Geinitz 1862, 1873) and Pterophyllum blechnoides (Geinitz 1873) together with Barthel's (1976) figure are inadequate to allow assignment to Pterophyllum or support a combination with Pseudoctenis samchokense. Pterophyllum cottaeanum differs in gross lamina shape from Ps. samchokense. Pterophyllum blechnoides from the Carboniferous of southern Germany as figured by Sandberger (1864) is more similar to Dioonites densinervis than Ps. samchokense in leaf shape, leaflet bases and venation pattern, but differs from both in its dimensions. One of the specimens figured by Sandberger (1864: pl. 2: 1) must have had an impressive length of more than 120 cm. Pterophyllum fayolii from the Commentry Basin (France) differs from Ps. samchokense mainly in having acutely pointed leaflets (Renault 1890; Zeiller 1906; Thomas 1930) that are more similar to those of Pt. cultelliforme. Renault (1896) noted that several additional species of Pterophyllum were described from other Carboniferous and Permian localities of France such as Saint Étienne, Montmaillot (Blanzy; i.e., Pt. grandeuryi), Commentry (i.e., Pt. fayolii) and Autun (i.e., Pt. cambrayi Renault, 1894). Some of these lack cuticles, despite Renault's (1890) description of a thin coaly layer partly covering the Pt. fayolii specimen. Later, Zeiller (1906) figured a small piece of cuticle of Pt. fayolii and provided several schematic drawings of cuticles of Pt. grandeuryi but figuring stomata only schematically since he was only able to obtain fragments of the adaxial and abaxial cuticle. The epidermal anatomy of Pt. grandeuryi was later discussed by Thomas (1930) who revealed that it distinctly differs from Mesozoic forms in having non-brachyparacytic stomata.

From East Asia, five species assigned to Pterophyllum have been reported. Pterophyllum cultelliforme differs from Pseudoctenis samchokense in having leaflets resembling a small knife (Sze 1936). Pterophyllum daihoense from the Heian System of South Korea was described by Kawasaki (1931, 1934) as having a segmented proximal region and an entire-margined lamina in the distal part of the leaf; it also differs from Ps. samchokense in size and insertion angles of the leaflets. A few illustrations of Pt. eratum were provided with the Chinese descriptions of this species by Gu and Zhi (1974) and Huang (1987). Based on the figures, Pt. eratum is similar to Ps. samchokense, especially to specimens NRM S141652 and NRM S141653 in arrangement, size and shape of the leaflets, but it lacks cuticle and the overall architecture of the leaf is not evident in the figured specimens. Pterophyllum bipartitium nom. nud. and Pt. nilssonioides nom. nud. (figured by Kawasaki 1931) were discussed by Sze (1936), who doubted their affinity to Pterophyllum. In fact, they were not included in Pterophyllum later in the text by Kawasaki (1934) accompanying the preceding atlas volume (Kawasaki 1931). Sze (1936) proposed that both species be better included in Taeniopteris or Nilssonia. Based on examination of Kawasaki's (1931) figures, we agree with a preliminary assignment of those specimens to Nilssonia due to agreements in macromorphology (i.e., entire-margined lamina parts and leaflets inserted on the upper side of the rachis). Shen (1995) provided in his synoptic species list seven further species: Pterophyllum bifidum Xiao, Pt. huabeiense Fang, Pt. maxum Shen, Pt. nanshanense Durante, Pt. shangdonense Sun, Pt. shanxiense Zhao, and Pt. striatum Hu and Du, 1982. All species except the last could not be traced completely due to incomplete referencing and thus comparison was not possible. Pteropyhllum striatum from the Permian of Shanxi has distinctly slender leaflets (up to 3 mm in width) than Ps. samchokense (Zhu et al. 1982). We assume that the remainder are better referred to Dioonites due to their similar lack of epidermal details.

Table 1.

Synopsis of the Pterophyllum species reported from Permo-Carboniferous deposits.

Central Asian assemblages include seven Pterophyllum species, of which some were already described as questionably assigned to the genus. The material of Schwedov (1961) and Vozenin-Serra (1979) assigned to Pt. slobodskiensis Schwedov, 1961, Pt. kotschetkovii Schwedov, 1961, and Pt. fromagetii Vozenin-Serra, 1979 is sparse and not convincingly described; hence comparisons can only be superficial. The figured specimens of Schwedov (1961) differ from Pseudoctenis samchokense in having relatively wider and shorter leaflets and coarser venation. The descriptions of these taxa lack cuticle details although cuticle possibly exists (at least in Pt. slobodskiensis and Pt. kotschetkovii, thus accommodation in Pterophyllum remains equivocal). Vozenin-Serra (1979) argued that “the cuticle, when preserved, shows the genus Pterophyllum to undeniably approach extant Dioon in its xerophytic characters”. If this view is taken into account, the Laotian material assigned to Pt. fromagetii is hard to compare either to Dioon or any other cycadophyte, since cuticular details are lacking. Consequently, the systematic position of Pt. fromagetii remains equivocal. Zimina and Zimina (2005) described four taxa from the Upper Permian of Southern Primorye but the assignment of Pt.? sitsense Zimina and Zimina, 2005, Pt.? ratnoense Zimina and Zimina, 2005, Pt. klyuchense Zimina and Zimina, 2005 and Pt. shevelevskiense Zimina and Zimina, 2005 to that genus is questionable. The specimens lack cuticular information, which would require assignment of the leaves to Dioonites rather than Pterophyllum. In addition, the separation of the four species is based mainly on small differences in vein density and leaflet width; hence these forms may represent intraspecific variants (Stearns and Hoekstra 2005).

Conclusion.—Cuticular studies of Permian cycad-like leaves from China revealed that generic and higher taxonomic assignments of foliage from Palaeozoic deposits must be undertaken with great care. No evidence could be found that any Palaeozoic leaves are assignable to bennettitaleans; moreover, the cycadalelan nature of these leaves was demonstrated. Such foliage may not be assigned to Pterophyllum due to the clear bennettitalean nature of that genus. Assignment to the typical cycadalean genus Pseudoctenis is recommended for Ps. samchokense.