Frasnian (Upper Devonian) evidence for multiple ...

Botanical Journal of the Linnean Society (1997), 123: 133–146. With 24 figures

Frasnian (Upper Devonian) evidence for multiple origins of seed-like structures LI CHENG-SEN Institute of Botany, Academia Sinica, Xiangshan, Beijing 100093, China AND JASON HILTON AND ALAN R. HEMSLEY F.L.S. Department of Earth Sciences, University of Wales Cardiff, PO Box 914, Cardiff, CF1 3YE

Received June 1996, accepted for publication October 1996

Reproductive structures of Frasnian (early Late Devonian) age from Wuhan, Hubei province, South China provide evidence for the early emergence of monomegaspory and integumentation in plants of non-progymnosperm affinity. Sphinxia wuhania gen. et sp. nov. pre-dates the occurrence of other reproductive structures exhibiting a similar suite of characters and adds support to the view that evolution towards an ovule may not have been a unique event. Sphinxia possesses a single functional megaspore with associated aborted members of the meiotic tetrad, a distinct, striated sporangial wall, and a sterile envelope bearing proximal spines. The morphology of the structure precludes assignment to any known group of plants in the absence of additional information regarding the parent plant. A progymnospermous affinity is unlikely. Thus, Sphinxia demonstrates that the Devonian progymnosperms did not lack potential competition from similarly specialized reproductive strategies in other plant lineages. ©1997 The Linnean Society of London

ADDITIONAL KEY WORDS: — China – lycopsid – monomegaspory – palaeobotany – progymnosperm – seed.

CONTENTS Introduction . . . . . . . . . . . . . . . . Locality, stratigraphy and specimens . . . . . . . . Methods . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . Systematic palaeobotany . . . . . . . . . . . . Sphinxia Li, Hilton & Hemsley, gen. nov. . . . . . Discussion . . . . . . . . . . . . . . . . . Comparison with other monomegasporic propagules . Comparison with contemporaneous heterosporous plants Conclusions . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . .

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Heterospory has evolved independently within many pteridophytic groups. It is equally apparent that in many of these groups, reduction to a single functional megaspore within each megasporangium (monomegaspory sensu Bateman & DiMichele, 1994) has subsequently emerged. Since this form of reduction has been viewed by many as a pre-requisite for the evolution of the ovule (e.g. Pettitt & Beck, 1968; Pettitt, 1970; Chaloner & Pettitt, 1987; Chaloner & Hemsley, 1991; Hemsley, 1993), much attention has been paid to the occurrence and distribution of this grade of evolution among pteridophytic groups. The numerous occurrences of monomegaspory immediately beg the question of why (apparently) only one group — namely the progymnosperms — further developed this syndrome into that known as the seed-habit (Stewart & Rothwell, 1993). This would involve development of an indehiscent megasporangium, nucellar modification of the distal parts of the megasporangium to form a nucellar apex (for pollen reception/retention prior to fertilization) and envelopment by an integument. Other than the progymnosperms, the rhizomorphic lycopsids of the Carboniferous have approached the seed-bearing grade, with the development of structures enclosing a monomegasporic sporangium (Achlamydocarpon, Lepidocarpon, Miadesmia: Phillips & DiMichele, 1992; Bateman & DiMichele, 1994), as have the sphenopsids (Calamocarpon Baxter, 1963, 1964). These plants apparently failed to diversify to any great extent and became extinct at, or shortly after, the onset of the Permian (Piérart, 1961; Braman & Hills, 1980; Hemsley, 1993). Throughout this time, seed plants (and their propagules) were diverse and widespread (Stewart & Rothwell, 1993). It may be argued that the monomegasporous rhizomorphic lycopsids were late in developing this syndrome and therefore that the gymnospermous derivatives of the monomegasporous progymnosperms had already established a strong foothold in all potential niches. Possibly other factors, such as rhizomorphic lycopsid construction, ontogeny, and restricted environmental tolerances, prevented any incursions into ‘gymnospermous territory’ (Bateman & DiMichele, 1994). Equally, it is clear that the presence of gymnospermic competition during the Pennsylvanian (Cleal, 1994) did not preclude further origins of monomegaspory amongst lycopsids and sphenopsids at that time (Hemsley, 1993; Rice et al., 1996). From this observation alone, one might infer dissimilarity in reproductive strategy of rhizomorphic lycopsids and gymnosperms. Monomegaspory among progymnosperms evolved (possibly more than once) in the Upper Devonian (e.g. Moresnetia, Fairon-Demaret & Scheckler, 1987; Spermolithus, Chaloner, Hill & Lacey, 1977; also see Hilton & Edwards, 1996) and, before the recognition of the structures described here, remained unique to that group (and descendants) until the Viséan (Lower Carboniferous). In situ monomegaspory in lycopsids occurs first in sporangia of Lepidocarpon waltoni (Viséan/Namurian, Scotland) bearing Cystosporites ‘seed-megaspores’ (Hemsley, 1993). Simultaneously, other groups of lycopsids (producing Subcystosporites spore tetrads, Hemsley, 1993) and ferns (e.g. some Stauropteris, producing Didymosporites tetrads, Chaloner, 1958) had evolved similar reproductive strategies. A second radiation of monomegaspory occurs in the Upper Carboniferous, predominantly among the lycopsids and sphenopsids but also again in the putative progymnosperm Cecropsis (Stubblefield & Rothwell, 1989). Decline and extinction of these forms appears rapid at the end of the Carboniferous, and it is only with the radiation of the water ferns, Marsileaceae/

FRASNIAN SEED-LIKE STRUCTURES

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Salviniaceae (Collinson, 1991; Bateman & DiMichele, 1994; Rothwell & Stockey, 1994) in the Cretaceous that the ferns eventually achieved monomegasporic status. It would therefore appear that within the Palaeozoic at least three evolutionary events gave rise to monomegaspory. We present here evidence of a fourth (and earliest) in the Upper Devonian.

LOCALITY, STRATIGRAPHY AND SPECIMENS

Specimens of the new structure were collected from Milianshan Quarry, near Wuhan City, Hubei province, South China. This quarry is within the Loujia Series of the Upper Devonian, which rests unconformably in this location on sandy mudstones of Middle Silurian age. Ashraf & Li (1993) determined a Frasnian age for this location based on miospore composition, although the exact biostratigraphic interval within the Frasnian is unknown. The present specimens were collected from the lowermost plant assemblage within the Loujia Series, from the same horizon as two plant species, one previously described as the primitive fern Protopteridophyton devonicum (Li & Hsü, 1987) and the other as yet undescribed. Most specimens are preserved as coalified adpressions; true compressions are less frequent. Both types occur within pale grey carbonaceous mudstones that were deposited in a lacustrine environment (Ashraf & Li, 1993; Li & Hsü, 1987) and are intercalated within the dominantly fluviatile facies of the Loujia Series.

METHODS

Dégagement using sharpened tungsten needles (Leclerq, 1960) was employed to expose individual specimens from the overlying sediment when viewed under a binocular microscope. A Wild M3 microscope with Leica photo-attachments was used for photography. Illumination of specimens for both dégagement and photography was provided by a Schott KL1500 twin fibre-optic light source, fitted with polarizing filters. A third polarizing filter was attached to the microscope objective lens for the purpose of reducing glare and enhancing edge and surface feature definition. Scanning electron micrographs were taken using a Cambridge Instruments Stereoscan 360 SEM set at 15 Kv and a working distance of 5–10 mm: specimens were gold-palladium coated with a BioRad SC500 sputter coater.

RESULTS

Light microscopy (Figs 1–14) shows that the specimens consist of a sporangium containing at least one (presumably functional) megaspore and up to three (presumably) abortive megaspores (Figs 6, 8, 9–11). Some specimens possess abortive megaspores of equal size, whereas in others abortive megaspores differ in size. Triradiate marks have not been observed on any of the spores, the aborted spores typically being detached from the functional spore. In certain cases, this fragmented tetrad has a linear appearance (Fig. 10). The functional megaspore is ovate in outline (Fig. 14B), with a papillate appendage occasionally recognizable at the distal end of the megaspore (Fig. 11, arrowed). There are some indications that the surface of the

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megaspore (Fig. 19B) had a fibrous microtopology (Fig. 20). Fine structure of the megaspore wall is generally poorly preserved and offers no indication of taxonomic affinity (Figs 19, 21, 23). Where present, retained wall structure is essentially granular (Fig. 21) but with indications of an original more spongy organization (Figs. 18, 20). In all cases the megaspores are highly compressed, with a lumen only occasionally identifiable (Fig. 23). The sporangial wall (Fig. 14C, 19C) is generally striate, with the ornament running parallel to the larger spore diameter (Figs 8 (arrowed) 16, 17). The sporangium is ovate, with a thin (c. 10 µm) wall. The completely enclosing integument-like structure is interpreted as tubular in shape with the presumably distal portion either absent or poorly preserved in all specimens (Figs 2–15). Both the width and length of the structure varies ranging from 3.78–6.84 mm in length and 1.35–3.87 mm in width, generating a diversity of outlines (compare Figs 2–4, 6, 10). The enclosing structure generally narrows proximally to a thin stalk, not usually in the plane of compression, curving either up or down through the matrix (Figs 2, 3, 5, 10, 12, 14, 15) and reaching 1.9 mm in length. The whole is clearly asymmetric in the plane of compression and, in view of the angle of departure of the stalk, probably asymmetric in all three dimensions. The enclosing structure bears raised, flattened discs of 22 µm diameter on the surface near the presumed point of attachment (Fig. 22), possibly evidence of stomata. Spines are clearly present on the convex outer margin of many specimens (Figs 6, 7) extending to the distal margin, and are occasionally present on the concave side of proximal end (Fig. 6). The spines are variable in outline as a consequence of being truncated by different planes of fracture separating the specimen into two halves (part and counterpart). Spines do not appear to be confined to the margin of the compressed structure. Although generally found as isolated units, one particular specimen clearly consists of a pair of structures (Fig. 1). Although their association and arrangement could be coincidental, they are aligned in the same orientation and it is tempting to infer that this was also their relative position when attached. This interpretation is supported by the presence of a furrow-like impression on several specimens (Figs 5, 7) marking the outline of a formerly adjacent structure. The structure may therefore be considered monomegasporic. However, one specimen appears to have contained more than one large megaspore, indicating that monomegaspory was facultative (Fig. 14). Figures 1–8 Sphinxia gen. et sp. nov.. All scale bars = 2 mm. Fig. 1. Two specimens showing the parallel and overlapping nature of two adjacent specimens, raising the possibility of a ‘cone-like’ arrangement. Specimens CBWh 101 (left) and CBWh 102 (right). Fig. 2. CBWh 125 displaying the tubular envelope with pointed attachment (upper right) and ragged distal margin surrounding a single, ovate megaspore, apparently lacking aborted megaspores. Fig. 3. CBWh 143 displaying an elongate tubular envelope with pointed attachment (top left) and a few poorly preserved spines on the proximal surface. The megaspore is also elongate, possessing a distinct central furrow which presumably marks the position of the distal margin of an adjacent unit (as in Fig. 1). Fig. 4 CBWh 147 with an incomplete proximal curve and apparently lobed distal apex. No megaspores are visible in this specimen; presumably they are still in attachment to the counterpart. Fig. 5. CBWh 142 displaying a well preserved, abruptly terminating, subtending axis (top left). The vegetative envelope bears an irregular distal margin. The single megaspore possesses a distinct central furrow, as in Fig. 3. Fig. 6. CBWh 105 (Holotype) with diagnostic tubular shape and irregular distal end. Spines are visible on both sides of the specimen. A single large megaspore is visible with three isolated abortive megaspores. The aborted spores are arranged linearly at the distal end of the functional megaspore. Of the three abortive megaspores, organic tissues are preserved only on the most distal, the position of the other two being marked by sediment imprints. Fig. 7. CBWh 114 showing well developed spines on the tubular vegetative envelope. The proximal portions of a single functional megaspore are visible, again with a central longitudinal furrow. Fig. 8. Specimen CBWh 109 showing the striated outer layer of the megasporangium (arrowed) with a distinctly irregular distal apex. Small spines are visible on the outer margin of the surrounding vegetative envelope.


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Figures 9–14 Sphinxia gen. et sp. nov. All scale bars = 2 mm. Fig. 9. CBWh 120 with an incomplete vegetative sheath. Three megaspores are visible with the proximal one considerably larger than the remaining two. The functional megaspore possesses a longitudinal furrow situated to the right of the centre of the megaspore width. Of the remaining two megaspores, the most distal is the smaller. Both appear to be irregularly shaped, but wider than long. Fig. 10. Specimen CBWh 117 with tubular vegetative envelope and pointed attachment (top right). Two abortive megaspores and one functional megaspore are visible, the abortive spores overlapping each other. The abortive megaspores appear to have a linear arrangement (distally from the functional megaspore) and differ in size. Fig. 11. Specimen CBWh 104. Vegetative envelope with irregular distal margin, surrounding an ovate functional megaspore with a distal papillate appendage. One circular, isolated, abortive megaspore is present. Fig. 12. Specimen CBWh 126B (counterpart of Fig. 13). Fig. 13. Specimen CBWh 126A (counterpart of Fig. 12) with tubular vegetative envelope surrounding a single functional megaspore. Below the distal apex of the specimen is a collection of small spores, not necessarily belonging to the parent plant of Sphinxia. Fig. 14. Specimen CBWh 103 with an incomplete vegetative envelope surrounding a small, ovate functional megaspore and two large abortive megaspores situated distally. A, vegetative envelope; B, megaspore; C, sporangial wall.


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SYSTEMATIC PALAEOBOTANY

Sphinxia Li, Hilton & Hemsley gen. nov. (Tracheophyta, Incertae sedis) Diagnosis. Stalked asymmetric tubular envelope surrounding a single, thin-walled sporangium enclosing one presumably functional megaspore and typically three aborted megaspores. Comment: In view of the large size of some aborted megaspores, some of these may in fact have had a functional status. Etymology-Sphinx: the composite Greek mythical creature who posed questions of innocent passers-by. Type species. Sphinxia wuhania Li, Hilton and Hemsley gen. et sp. nov. Asymmetric tubular enclosing structure 3.78–6.84 mm in length, 1.35–3.87 mm in width, 0.63–3.78 mm, slightly constricted and sometimes lobed at one end, tapering sharply to one edge at the opposite end, reaching 1.9 mm in length. Curved end of tubular structure showing dentate spines, sometimes slightly recurved, present on upper and lower margin and occasionally elsewhere. Raised discs of 22 µm diameter occasionally present on outer surface of enclosing structure. Sporangium thin-walled, with striae orientated along greater diameter. Functional megaspores usually one per sporangium, compressed ranging from 1.71–3.69 mm long and 0.81–2.61 mm wide. Internal structure granular (possibly fibrous), but generally homogeneous. Aborted spores varying in number, not more than three, 150–1000 µm in diameter, rounded or irregular. Holotype. CBWh 105. Locality. Milianshan Quarry, near Wuhan city, Hubei province, South China. Age. Frasnian, Late Devonian. Repository. Institute of Botany, Chinese Academy of Sciences, Beijing Numbers. CBWh 101–147.

DISCUSSION

The arrangement of Sphinxia on the parent plant can only be surmised on the basis of the pairs of structures illustrated in Figure 1, possibly reflecting a elongated, conelike structure, as in Barinophyton citrulliforme (Brauer, 1980). However, from the specimens examined it is difficult to ascertain which end of Sphinxia was the point of attachment to the parent plant. Here it is considered more likely that the point of attachment is the short narrow axis rather than the irregular, partially lobed margin. Attachment by the apparently open end would lead to a more lycopsid-like morphology, but it is less easy to comprehend in terms of the evenly-lobed nature of certain individuals. The point of attachment of Sphinxia, like its arrangement on the parent plant, can only be verified by material found in attachment, but does not detract from its ovule-like status. It is possible that the large megaspore was shed from the enclosing structure as a few otherwise complete specimens lack megaspores. However, on the basis of this

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Figure 24. Line figures showing external reconstruction of Sphinxia wuhania gen et sp. nov (left) and a cut-away (right) illustrating the arrangement of the contents of the enclosing envelope. The pointed apex is interpreted as proximal.

material it is unclear whether separation of the megaspore and surrounding structures occurred ontogenetically or taphonomically (i.e. post-mortem). In this respect, the surrounding tubular structure cannot be described as an integument, merely as integument-like. The sporangium of Sphinxia contains a single spore tetrad, generally consisting of at least one fertile, and up to three abortive, spores ranging in size from 150 to 1000 µm in diameter. The variation in spore size and lack of clear division of aborted and functional spores might be expected in a case of incipient monomegaspory and is clearly illustrated by extant heterosporous plants, e.g. Selaginella (Duerden, 1929). If it is accepted that all sporangia should contain only one functional spore before the plant can be considered genuinely monomegasporic, problems arise with respect to cases such as Archaeopteris (Chaloner & Pettitt, 1987; Chaloner & Hemsley, 1991) for which it has often been speculated that certain sporangia may have contained only a single functional megaspore, whilst others contain more than one. Here we define any individual which usually possesses a single functional megaspore within a megasporangium as monomegasporic although it is recognized that it may be only Figures 15–23. SEMS of Sphinxia gen et sp. nov. Fig. 15. The entire tubular structure, demonstrating a fold to the left of the specimen induced by formerly adjacent units. The single functional megaspore is clearly visible. CBWh 133. Scale bar = 1 mm. Fig. 16. Detail of the sporangial wall as it extends over the edge of the enclosed megaspore. Surface striations are most evident on this raised area. CBWh 112. Scale bar = 500 µm. Fig. 17. Detail of the striated sporangial wall. CBWh 133. Scale bar = 200 µm. Fig. 18. Detail of the somewhat degraded sporangial wall surface. B, megaspore surface; C, sporangial wall. CBWh 144. Scale bar = 144 µm. Fig. 19. Detail of a fractured specimen clearly showing the granular, degraded megaspore wall, its smooth surface and the overlying sporangial wall. CBWh 116. Scale bar = 50 µm. Fig. 20. Detail of one of the few areas of megaspore surface that shows structure; a spongy, fibrous construction is apparent. CBWh 113. Scale bar = 5 µm. Fig. 21. Detail of a fractured spore wall illustrating the general lack of preservation of complex ultrastructure. CBWh 134. Scale bar = 20 µm. Fig. 22. One of the disclike objects on the surface of the enclosing structure. Its central dividing ridge suggest it may represent a stomata. CBWh 112. Scale bar = 20 µm. Fig. 23. A further fractured specimen demonstrating the relatively homogeneous nature of the megaspore wall and its tendency to split along the lumen. CBWh 112. Scale bar = 20 µm.

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a few individuals that have achieved this degree of reduction. Sphinxia has certainly achieved monomegasporic status in most sporangia (around 95%) and must be considered monomegasporic on this basis, even if a few sporangia fail to meet this requirement. The arrangement of the abortive megaspores in certain examples is of particular interest. Due to lack of specimens displaying conclusive evidence for abortive megaspores in attachment, it is impossible to determine whether the megaspores are in a tetrahedral arrangement, as one might expect, or linear, as appears to be the case in certain specimens. The linear arrangement of spores probably represents a tetrahedral megaspore tetrad from which certain megaspores have become isolated and displaced to differing degrees from their original position in the tetrad.

Comparison with monomegasporic propagules Condrusia Stockmans 1946: Fa2c biozone (Famennian), Belgium. Stockmans (1946) erected the genus Condrusia, initially comprising a single species, C. rumex. Further details of this genus were provided by Stockmans (1948), who illustrated and partially described two species of Condrusia, C. rumex and C. minor. From the figured material is it clear that specimens of Condrusia possess a hastate to ovate-shaped laminar vegetative structure surrounding, in certain cases, a single functional fertile unit (Stockmans, 1948, pl.XI, 4–12). The fertile unit gives the appearance of a single functional megaspore, similar to Sphinxia, although the exact nature of the specimens remains uncertain. These structures are distinct from Sphinxia in that the subtending axis is located centrally and the vegetative surround is laminar and does not envelope the fertile unit. Both species of Condrusia are insufficiently known to allow detailed comparison. Spermolithus devonicus (Johnson) Chaloner, Hill & Lacey 1977: LN-V1 biozones, (Upper Famennian-basal Tournaisian), Ireland. The exact nature and affinity of Spermolithus devonicus remains uncertain. Chaloner et al. (1977) suggested an ovulate nature, (hence gymnospermous affinity) whereas Rothwell & Scheckler (1988) suggest that this has not reached the level of ovular organization. It is clear, however, that certain specimens of Spermolithus (although possibly not all) have attained monomegasporic status. The ultrastructure of the exine/megaspore membrane of Spermolithus has not been investigated and may help to identify its affinity. Spermolithus is distinguished from Sphinxia in that it is bilaterally symmetrical and the surrounding vegetative material (?integument) has two distinct furrows situated immediately proximally and distally to the megasporangium. The mode of attachment of Spermolithus like that of Sphinxia, is unknown. Lepidocarpon Scott 1900. Carboniferous (Viséan-Stephanian, see Braman & Hills, 1980). Lepidocarpon waltoni (Chaloner, 1952, bearing Cystosporites giganteus seed-megaspores) achieved both monomegaspory and a form of integumentation. However, lycopsid megasporophylls are zygomorphic with a generally robust composition, often with a distinct vascular trace. Sphinxia differs considerably from this type of structure in


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lacking any vascular traces, and being considerably more rounded in outline. Furthermore the vegetative envelope completely surrounds the megasporangium in Sphinxia rather than being a laminate megasporophyll as in Lepidocarpon. Megaspore ultrastructure may be similar in Sphinxia and Lepidocarpon (Chaloner & Hemsley, 1991), but equally, a spongy exine also appears in archaeopterid metaspores (Pettitt, 1965, 1966). Despite the apparent similarity of Sphinxia to certain Lepidocarpon/ Lepidostrobophyllum there is currently a considerable stratigraphic inconsistency between the occurrence of the two groups with the latter first occurring in the lower part of the Middle Carboniferous. Early ovule morphologies: Famennian-Tournaisian All currently recognized early ovulate structures (for review see Hilton & Edwards, 1996) possess an indehiscent, single, functional megaspore, enveloped by a nucellus (sporangial wall) with distal modification for pollination (the nucellar apex or pollen chamber) and surrounded by an integument in the form of discrete lobes (i.e. preovulate sensu Stewart, 1983). It appears that Sphinxia is indehiscent (as most dispersed units retain megaspores), essentially monomegasporic, and has a certain degree of integumentation (although perhaps not a true integument from a seed plant origin), but it lacks the distal nucellar modification necessary for classification as an ovule. In this respect Sphinxia is ‘ovule-like’ but not a true ovule. Sphinxia is further distinguished from all recognized Late Devonian seed morphologies in being asymmetric rather than radially symmetrical (radially isodiametric), with the exception of Spermolithus (discussed above). Suavitas imbricata Rice, Rothwell, Mapes & Mapes, 1996, Virgilian (Late Pennsylvanian), USA. Rice et al. (1996) described and illustrated a single specimen of this anatomically preserved megasporangiate cone which they interpreted as bearing seed analogues of possible lycopsid affinity. However, the sporangia in Suavitas differ from those of Sphinxia in possessing horizontally flattened sporophylls with prominent lateral wings which are larger than the tubular enclosing structure in Sphinxia ranging from 9.5–11.2 mm long and up to 5.6 mm wide. The functional megaspore in Sphinxia may be smaller than that of Suavitas although maximum sizes of the two are similar. Further distinction can be made in that Suavitas has apical dehiscence and lacks an enveloping structure as present in Sphinxia, although both lack distal modification to facilitate pollination as seen in the seed plants.

Comparison with contemporaneous heterosporous plants Barinophyton White, 1905. Emsian-Famennian of Europe, Asia and North America. Barinophyton bore sporangia containing numerous megaspores of variable size in an arrangement similar to that envisaged for Sphinxia (Pettitt, 1965; Brauer, 1980). These, however, have no indication of integumentation; merely an encirclement of the sporangium by the subtending axial branch. Expansion of this structure could conceivably give rise to the complete enclosure of the sporangium. Megaspore ultrastructure is not comparable between Sphinxia and Barinophyton (Taylor & Brauer,

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1982) with Barinophyton possessing a two layered sporangium wall with more dense ultrastructure than that of Sphinxia. Longostachys latisporophyllus (Zhu et al.) Cai & Wang, 1995. Givetian of Li Xian, Hunan, China This heterosporous lycopsid from China possesses megasporophylls arranged in a cone, each with a single tetrad containing four equal megaspores on the adaxial surface of the sporophyll (Cai & Wang, 1995, pl. 15; 6, 7). The megasporophyll is elongate in form, possessing a fimbriate margin, and a vascular trace running longitudinally through the centre of the sprorophyll. In these respects Longostachys is clearly distinct from Sphinxia in that it has not attained the organizational grade of integumentation or monomegaspory and Sphinxia lacks a central vascular trace. However, Longostachys from China appears to be more specialized than contemporaneous lycopsids from other areas, being more similar to the Early Carboniferous genus Lepidostrobophyllum (Hirmer) Allen, 1961. Bisporangiostrobus harrisii Chitaley & McGregor, 1988. LN-VI biozones (Upper Famennian-basal Tournaisian), USA. This heterosporous plant possessed paired, terminal, bisporangiate cones with the conventional lycopsid arrangement of megasporophylls at the base, microsporophylls at the tip and a transition of both mega-micro sporangia.Cones consist of sporophylls with reduced laminae and are distally upturned. Laminae are curved with a serrated heel, and at least in this respect resemble Sphinxia. The megasporangia are adaxial on the sporophyll, about 3–4.0 mm in length and contain 22–30 megaspores (Chitaley & McGregor, 1988). Of interest is the thin (one cell) sporangium wall comparable with that of Sphinxia. Progymnospermous heterosporous plants Archaeopteris is known to produce sporangia which contain a variable number of megaspores, and it is a logical assumption that some may have attained monomegaspory (Chaloner & Pettitt, 1987; Chaloner & Hemsley, 1991). Integumentation of these structures is currently unknown. However, Pettitt & Beck (1968) offered a possible affinity with Archaeopteris-like plants for Archaeosperma although Archaeosperma is clearly a gymnospermous ovular structure and bears only partial resemblance to Sphinxia. This supposed transition from few megaspores to monomegaspory in the archaeopterid lineage, also appears to occur somewhat after the earliest occurrence of Sphinxia. Aneurophyte affinity may be discounted, since these are not known to have been heterosporous (e.g. Bateman & DiMichele, 1994), although evidence of the absence of heterospory from the group is inconclusive. Chaleuria, of possible aneurophyte affinity (see Stewart & Rothwell, 1993) demonstrates variation in spore size comparable with Barinophyton, but none of these can strictly be considered megaspores (Turnau & Karczewska, 1987). Protopitys (Smith, 1962), of Early Carboniferous age, shares this character of spore size variation. CONCLUSIONS

Sphinxia represents the earliest evidence so far reported for the independent or combined presence of monomegaspory and integumentation. Its unique morphology


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and organization make assignment to any known plant group problematic. It is distinct from any of the three plant clades that subsequently reached the organizational level of monomegaspory (progymnosperms, lycopsids, sphenopsids) though subsequent discovery of the parent plant may provide the necessary evidence both of affinity and correct mode of attachment. The presence of a vegetative (possibly photosynthetic) layer exterior to the megasporangium also distinguishes Sphinxia from known structures from the Late Devonian and Early Carboniferous, and from the two plant lineages which subsequently attained the level of gross organization involving integumentation (progymnosperms, lycopsids). Sphinxia provides evidence that an earlier episode of monomegaspory occurred at a time apparently favourable to the development of advanced hererospory and that the progymnosperm-gymnosperm lineage was perhaps not the first to produce an enclosed monomegasporic sporangium.

ACKNOWLEDGEMENTS

This research was funded by the National Natural Science Foundation of China (Grants 39230030 and 38321001 to CSL), the Chinese Academy of Sciences (to CSL), the Royal Society of London (to CSL and D. Edwards, and ARH Royal Society University Research Fellowship K5397), and a NERC Research Studentship GT4/92/277/G to JH. We thank M. Fairon-Demaret (Liège) for discussion, D. Edwards, R.M. Bateman and W.G. Chaloner for comments on the manuscript, C. Shute (BMNH) for access to specimen at the Natural History Museum, London, and J. Crawley and V. Williams (Cardiff) for assistance with photography.

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