Morphology and ultrastructure of Devonian spores: Samarisporites (Cristatisporites) orcadensis (Richardson) Richardson, 1965

Review of Palaeobotany and Palynology 116 (2001) 87±107

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Morphology and ultrastructure of Devonian spores: Samarisporites (Cristatisporites) orcadensis (Richardson) Richardson, 1965 Charles H. Wellman* Centre for Palynology, University of Shef®eld, Dainton Building, Brook Hill, Shef®eld S3 7HF, UK

Abstract Specimens of the dispersed spore Samarisporites (Cristatisporites) orcadensis (Richardson, 1965) have been isolated from Middle Devonian deposits of Cromarty, Scotland. This is the strata from which the type material was obtained (Richardson, 1960) The specimens are extremely well preserved and of low thermal maturation. Comprehensive investigations using light, scanning electron and transmission electron microscopy provide detailed information on morphology, gross structure and wall ultrastructure. The spores are trilayered, with a bilayered inner body entirely enclosed within an outer layer. There is apparently no cameration between the layers comprising the spore wall. The outer layer is entirely homogeneous, and is extended forming a trilete mark on the proximal surface, a prominent `pseudozona' in the equatorial region and distinctive distal ornament. The inner body is bilayered, with the inner (a) layer comprising closely packed, straight, parallel and continuous lamellae, and the outer (b) layer comprising similar but less closely spaced and more irregular lamellae. The morphological, structural and ultrastructural information is assessed in order to evaluate the taxonomic demarcation of this taxon, and also to shed light on spore wall formation, functional morphology and af®nities/phylogeny. It is suggested that structural interpretation based on light microscope work is susceptible to misinterpretation, because the different layers of multilayered spores often possess different ultrastructure and hence differ in optical properties. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Middle Devonian; spores; Samarisporites; ultrastructure

1. Introduction Analysis of spore/pollen wall ultrastructure is routinely undertaken during research into extant land plants, and has proven critical to our understanding of spore/pollen wall formation, in addition to providing characters useful in phylogenetic analyses. Similar studies have increasingly been applied to fossil material (in situ and dispersed spores/pollen) where they have proven equally useful (e.g. Kurmann and Doyle, 1994 and references therein). Regarding early land plants, spore wall ultrastructure has been * Tel.: 144-114-222-3689; fax: 144-114-222-3650. E-mail address: c.wellman@shef®eld.ac.uk (C.H. Wellman).

reported from latest Ordovician±earliest Silurian dispersed spores (Taylor, 1995a,b, 1996, 1997) and latest Silurian±earliest Devonian in situ spores (Rogerson et al., 1993; Edwards et al., 1995, 1996, 1999; Wellman, 1999; Wellman et al., 1998a,b). To date, however, there have been few reports on spore wall ultrastructure in late Early±early Late Devonian spores (examples include: Pettitt, 1966; Fletcher, 1976; Gensel, 1979; Taylor et al., 1980; Taylor and Brauer, 1983; Gensel and White, 1983; Cichan et al., 1984; Meyer-Melikyan and Telnova, 1989; Telnova, 1993; Foster and Balme, 1994; Taylor and Scheckler, 1996). This is unfortunate as this interval represents a critical period in the evolution and diversi®cation of land plants, including the emergence of several

0034-6667/01/$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0034-666 7(01)00065-3

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important higher taxa, such as the cladoxyls, progymnosperms and sphenopsids (e.g. Gensel and Andrews, 1984). Evolutionary relationships among late Early± early Late Devonian plants is relatively poorly understood, particularly regarding the emergence of the aforementioned higher taxa. This paper is the ®rst contribution emanating from a larger project that aims to document spore wall ultrastructure among a wide variety of Devonian spores types (dispersed and in situ). It is anticipated that this research will shed light on the af®nities and phylogenetic relationships of Devonian dispersed spores and their parent plants, in addition to revealing information on spore wall formation in these ancient plants. This paper reports on the gross morphology and spore wall ultrastructure in dispersed spores of the genus Samarisporites Richardson, 1965, that are placed with the species S. orcadensis (Richardson) Richardson, 1965. 2. Material and methods 2.1. Locality and geology The material described herein was isolated from Middle Devonian deposits from Cromarty, the Black Isle, Scotland. These deposits were selected because of the abundance, excellent preservation and low thermal maturity of the preserved palynomorphs (Lang, 1925; Richardson, 1960, 1962, 1965). Samples of green siltstones and ®ne sandstones were collected from strata exposed in Coal Heugh (NH792672), a small stream draining into Millers Bay, near Cromarty. These strata belong with the Millbuie Sandstone Group (Horne and Hinxman, 1914; Johnstone and Mykura, 1989). This group comprises predominantly ¯uviatile deposits, but also contains a ®sh-bearing horizon that is probably equivalent to the Achanarras horizon and represents a transgression of the Orcadian Lake. These strata are believed to be of Eifelian age (Middle Devonian) based on biostratigraphic evidence from spore assemblages (Richardson, 1960, 1962, 1965; Richardson and McGregor, 1986; Marshall, 1996) and ®sh (e.g. Blieck et al., 1988). 2.2. Preparation and techniques Palynological residues were obtained using standard

palynological HCl±HF±HCl acid maceration techniques. Following acid maceration, heavy liquid separation was undertaken using zinc chloride, and the residue sieved using a 20 mm mesh. The spores are extremely well preserved and of low thermal maturity, and were not oxidised in any way. Part of the residue was strew mounted onto cover slips and mounted on slides for analysis using a light microscope (LM). Other material was retained for picking in order that individual specimens could be selected and analysed using a Scanning Electron Microscope (SEM) and a Transmission Electron Microscope (TEM). Picking was achieved using the following technique. The palynological residue was transferred from water to ethanol by repeatedly allowing the palynomorphs to settle, pipetting off excess liquid, and adding ethanol. When ethanol concentration was adequate, the residue was strew mounted onto glass slides and the ethanol allowed to evaporate off naturally. The slides were then examined under a microscope attached to a micromanipulator, and selected spores individually picked. Material for SEM analysis was prepared by mounting the individually picked spores on the sticky surface of a double-sided sticky tab attached to a glass coverslip. When a suitable number of specimens had been attached to a coverslip, it was attached to an SEM stub using a further double-sided sticky tab. The stub was then gold coated using a sputter coater, and ready for SEM analysis using a Philips 501B SEM. Material for TEM analysis was prepared by mounting individually picked spores (either singly or in rows of up to ®ve specimens) on a block of freshly prepared agar. The spores were sealed into the block by covering it with molten agar, which solidi®es on cooling. Following dehydration in ethanol, the spores are embedded in Spurr resin. Sections were cut on an microtome using a diamond knife, stained with uranyl acetate followed by Reynold's lead citrate, and examined using a Philips CM10 TEM. Twenty strew mounted slides were prepared and examined using LM. Specimens belonging to the genus Samarisporites are moderately abundant and numerous specimens, including a wide variety of orientations and modes of preservation, were examined in detail. Eight specimens were individually picked and examined using SEM (three oriented proximal face up and ®ve oriented distal face up). Six specimens were

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individually picked and examined using TEM (two blocks were prepared containing one and ®ve specimens respectively). All material (slides, stubs, blocks and sections) are stored in the Centre for Palynology of the University of Shef®eld.

3. Taxonomic discussion 3.1. Generic designation Richardson (1960), in his initial report on dispersed spores from the Middle Devonian deposits of Cromarty, described three similar and very distinctive new spore taxa (C. orcadensis, C. conannulatus and C. mediconus) that he placed with the genus Cristatisporites Potonie and Kremp, 1955. A turma system of classi®cation was utilized and Cristatisporites was placed in Subturma Zonotriletes (Waltz, 1935 in Naumova, 1937), Infraturma Cingulati (Potonie and Klaus, 1954). The new species were characterized by their zonate structure and a distinct distal ornament comprising prominent cones and verrucae. Individual species were separated based largely on the distribution of the distal ornament. It is clear from the diagrammatic reconstruction provided by Richardson (Richardson, 1960, text-®gure 8) that he believed that these spores were bilayered (an exoexine and intexine are annotated but not clearly marked) with no gap (cameration) between the wall layers. It is unclear from the diagram whether-or-not Richardson considered that they were simply zonate or cingulizonate. Subsequently, Richardson (1965) erected a new genus, Samarisporites, and transferred all three taxa into this genus. He differentiated Samarisporites from Cristatisporites primarily on the basis that the latter had ornament on the proximal as well as distal surface. Interestingly, Richardson (1965) placed Samarisporites in Infraturma Zonati (Potonie and Kremp, 1954) rather than Infraturma Cingulati (Potonie and Klaus, 1954). Playford (1971) suggested that following emendation of Cristatisporites (Butterworth et al. in Staplin and Jansonius, 1964), the genus Samarisporites could be abandoned and included species transferred to this genus. Similarly, McGregor and Cam®eld (1982, p.29) stated that ªSamarisporites Richardson (1965),

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proposed nearly simultaneously with, and independently of, the emendations of Cristatisporites by Butterworth et al., is distinguished from the latter only by the requirement that spores in it have an unsculptured proximal face. This distinction is taxonomically trivial, and is especially dif®cult to maintain for those species that have dense, prominent distal sculpture that tends to obscure the details of the proximal face (see also Playford, 1971, p.40). We have not used Samarisporites for this reason, and because it contains some species (e.g. S. megaformis Richardson, 1965) that may be placed more conveniently in Grandispora (see McGregor, 1973).º McGregor and Cam®eld (1982, p.29) went on to note that ªMany of the Devonian specimens that have been assigned by various authors to Cristatisporites, Asperispora, Cingulizonates, Samarisporites, Hymenozonotriletes, and Densosporites apparently have basically similar structure and sculpture (see Staplin and Jansonius, 1964; Richardson, 1965). The group clearly needs to be revised, and the diagnoses of its constituent genera made more precise, with reference both to the type material of the various species contained in them, and the practical aspects of differential diagnosis. It seems unlikely that as many as six genera are necessary to accommodate this complex.º Later on in the same paper McGregor and Cam®eld (1982) also suggest that Devonian spores placed in Densosporites are actually zonate and not truly cingulizonate (and therefore differ from typical Carboniferous representatives of the genus). They recommended that ªfurther work is necessary¼to clarify the structure of the spores herein assigned to Densosporites, and the whole complex of `zonate' Middle Devonian spores placed by various authors in Kraeuselisporites, Samarisporites and Cristatisporitesº (McGregor and Cam®eld, 1982, p.34). In the same year that McGregor and Cam®eld reviewed zonate±cingulizonate Middle Devonian spores, Marshall and Allen (1982) preferred to maintain Samarisporites until ªa more uni®ed set of limits for the densospore group is proposed, which accommodates both Devonian and Carboniferous representatives.º They noted that the emended version of Cristatisporites was unsuitable for species contained within Samarisporites because the emendation: (1) still includes the possible presence of proximal sculpture in the form of a ring of setae; (2) restricts the

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C.H. Wellman / Review of Palaeobotany and Palynology 116 (2001) 87±107

distal sculpture to being dominantly mammoid in type, and showing no differentiation in form. Species included in Samarisporites have no proximal ornament and display a wide variety of distal sculpture. 3.2. Speci®c designation Richardson (1960, 1965) erected three new species of Samarisporites from the Middle Old Red Sandstone of the Orcadian Basin (Scotland) distinguished largely on the basis of the distal ornament: Samarisporites (Cristatisporites) orcadensis (Richardson) Richardson, 1965 characterized by rounded to pointed cones on the central area, and a large number of sharply pointed cones on the periphery forming a dentate margin; Samarisporites (Cristatisporites) conannulatus (Richardson) Richardson, 1965 characterized by large rounded cones, fused in groups on the central area and ¯ange, and fused in a ring around the margin of the central area; Samarisporites (Cristatisporites) mediconus (Richardson) Richardson, 1965 characterized by large rounded cones con®ned to the central area, and few small peripheral cones. Marshall and Allen (1982), also working on Middle Devonian spore assemblages from the Middle Old Red Sandstone of the Orcadian Basin (Scotland), reported all three of these species, but noted that their populations contained intermediate forms and there was a complete morphological transition series between them with the species occupying distinct positions on the various trends. They noted that ªit would be interesting to speculate whether the continuous variation this plexus of species exhibits,

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could be treated in the same way as in the morphon concept recently outlined by Van der Zwan (1979, 1980).º However, they recovered too few specimens to systematically describe the variation, and either combine the species or record them as separate species or varieties in a morphon. 4. Descriptions 4.1. LM observations (Plate I) Thirty specimens belonging to the Samarisporites `complex' were identi®ed during logging of strew mounts and subjected to detailed analysis using LM. A general description based on examination of all of the specimens is presented in the following account. The description is brief as my observations differ little from those presented by Richardson (1960) in his descriptions, based on LM analysis, of the three species C. orcadensis, C. conannulatus and C. mediconus. However, in the following account there is no attempt to subdivide my observations into the three taxonomic entities described by Richardson as subdivision of the Samarisporites complex is considered later (see p. 93). In terms of gross morphology the spores clearly comprise a dark central area surrounded by a pale zona. The dark central area is formed because the spores are bilayered with a distinct inner body. The inner body is surrounded by an outer layer, that is extended in the equatorial region forming a zona. The junction between the inner body and the outer

PLATE I LM photographs of dispersed Samarisporites orcadensis. All specimens at magni®cation £ 400. 1, 4, 7, 10. Slide CH2/G, England Finder No. (K32/1). Distal ornament comprises large, fused elements largely con®ned to the central area. Note the micropunctate infrasculpture clearly discernible in Figs. 4 and 7, and the indentation and slight thickened in the region where the laesurae meet the equator (bottom left). 2, 3. Slide CH2/G, England Finder No. (T30/2). Distal ornament present over the central area, zona and on the margin. Note the prominent trilete mark. 5, 6. Slide CH2/1, England Finder No. (N38/4). Distal ornament present over the central area, zona and on the margin. Note the micropunctate infrasculpture clearly discernible in Fig. 5. 8, 9. Slide CH2/G, England Finder No. (P52/3). Distal ornament comprises large, fused elements largely con®ned to the central area, and forming an incipient annulus around the margin of the inner body. 11. Slide CH2/C, England Finder No. (O38/3). Distal ornament present over the central area, zona and on the margin. Note the prominent trilete mark. 12. Slide CH2/C, England Finder No. (C45/2). Distal ornament present over the central area, zona and on the margin. Note the rather atypical elongate nature of the ornament.

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C.H. Wellman / Review of Palaeobotany and Palynology 116 (2001) 87±107

layer, at the inner margin of the zona, appears as a distinct break e.g. Plate I, 4, and this is seen particularly clearly in specimens preserved in oblique compression. There is no evidence for separation (cameration) between the inner body and outer layer. The zona appears pale and translucent suggesting that it is probably rather thin walled. The central area appears dark suggesting that the inner body is probably thick walled, although wall thickness over the central area is clearly enhanced due to the bilayered nature of the spore and the dense distal ornament that is developed in the outer layer and is particularly prominent over the central area. The proximal surface appears entirely laevigate over the zona. However, over the central area there is a distinct micropunctate ornament e.g. Plate I, 4,5,7. Using LM analysis it is unclear if this ornament is present on the surface of the outer and/or inner layer, or if indeed it represents infrasculpture in one or both of these layers. However, SEM analysis (see below) indicates that it is not on the spore surface which is entirely laevigate. The trilete mark is prominent e.g. Plate I, 2,3,11. The laesurae are tall and narrow, and often bear prominent folds resulting from ¯attening during compression e.g. Plate I, 2,11. Focusing through the laesurae indicates that there is a suture at their base where they emerge from the surface of the spore e.g. Plate I, 10. The laesurae extend all of the way to the equator, but there is no prominent equatorial thickening, although some specimens exhibit an indentation and appear slightly thickened in the region where the laesurae meet the equator e.g. Plate I, 1. The distal surface bears a distinct ornament. However, the elements are highly variable in both form and distribution. In all cases the central area is densely ornamented. In some specimens the margin of

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the central area is particularly densely ornamented forming an annulus around the margin of this area e.g. Plate I, 8,9. Beyond the densely ornamented central area, the extent of ornamentation on both the zona and equator is variable. In some specimens there is little or no ornament e.g. Plate I, 1,4,7,10, in others it is dense e.g. Plate I, 5,6, and there appears to be a continuum between the two extremes. The elements over the central area are dominated by verrucae. They are usually crowded, and in some specimens elements coalesce forming rugulae. Element bases may be rounded±subrounded±polygonal, or irregular where elements have coalesced. On the zona, elements are generally somewhat smaller and less closely packed than those in the central area. They comprise verrucae and/or apiculate elements (coni±spinae). Element bases are rounded. At the equator elements are predominantly apiculate comprising small coni±spinae. They vary between sparse and crowded, and are occasionally entirely absent. 4.2. SEM observations (Plate II) Eight specimens were picked and examined using SEM. All were preserved in polar compression with the proximal e.g. Plate II, 1,2 and distal face Plate II, 3±7, exposed by three and ®ve specimens respectively. The proximal face is entirely laevigate, except for the presence of coni±spinae at the equator, where they vary from crowded to entirely absent e.g. Plate II, 1. The trilete mark is prominent. The laesurae are tall and narrow, and often bear prominent folds resulting from ¯attening during compression e.g. Plate II, 2. There is no evidence for an external suture. Laesurae extend from the pole to the equator. There is no prominent equatorial thickening, although some

PLATE II SEM images of dispersed Samarisporites orcadensis. All at magni®cation £ 500. Note the range in variation displayed by the distal ornament, and the intergradation between the different types. 1. Stub CW(SHEF)02, Image 0045/99. Proximal surface. 2. Stub CW(SHEF)02, Image 0054/99. Proximal surface. 3. Stub CW(SHEF)02, Image 0043/99. Distal surface `conannulatus-type'. 4. Stub CW(SHEF)02, Image 0052/99. Distal surface `orcadensis-type'. 5. Stub CW(SHEF)02, Image 0048/99. Distal surface `mediconus-type'. 6. Stub CW(SHEF)02, Image 0050/99. Distal surface `orcadensis-type'. 7. Stub CW(SHEF)02, Image 0053/99. Distal surface `orcadensis-type'.

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specimens exhibit an indentation and are slightly upturned (possibly accounting for the ?thickening observed in LM, see p.) in the region where the laesurae meet the equator e.g. Plate II, 1. Viewed using SEM the proximal face exhibits little or no

evidence for differentiation into a central area and zona, although some specimens e.g. Plate II, 1 bear a concentric fold, that probably forms during compression, either around the margin of the inner body and/or the central area of dense distal ornament.

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SEM images of the distal surface provides an excellent insight into the nature of the distal ornament. In all cases there is a central area that is densely ornamented (presumably corresponding to the central area over the inner body). In some specimens, the margin of this central area is particularly densely ornamented forming a distinct annulus e.g. Plate II, 3. Beyond the densely ornamented central area, the extent of ornamentation on both the zona and equator is variable. In some specimens, there is little or no ornament e.g. Plate II, 5, in others it is dense e.g. Plate II, 6, and there appears to be a continuum between the two extremes. The ornament itself is rather variable in form. The central ornament generally seems to comprise verrucae, that are rounded±subrounded± polygonal at their base, and usually rounded in pro®le, although some elements are straight sided (particularly where the elements are crowded). In some specimens, the verrucae occasionally merge forming rugulae, that are irregular at their base, and rounded in pro®le e.g. Plate II, 6. On the zona, elements are generally somewhat smaller than those over the central area. They comprise rounded verrucae and/or apiculate elements (coni±spinae). Elements at the equator, if present, comprise predominantly small coni±spinae. 4.3. TEM observations (Plates III±VII) TEM descriptions are based on sections of six specimens (referred to as a±f in the following description). All specimens demonstrated features of gross structure and are utilized in the description of this aspect of the spores. Two specimens (a and c) preserved exquisite ultrastructural detail and the

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description of this aspect of the spore walls is based primarily on these specimens. Measurements based on TEM work are presented in Tables 1±4. Note that all of the specimens studied were preserved in equatorial compression and cut, as near as possible, perpendicular to the plane of compression. Dimensions should therefore provide a more or less accurate re¯ection of true thickness. In terms of gross structure, the spores clearly consist of an inner body that is entirely surrounded by an outer layer. The outer layer is extended on the proximal surface forming the trilete mark. It is also extended at the equator of the spores, where both the proximal and distal surfaces extend beyond the inner body, and are closely adpressed, forming a distinct `pseudozona'. In this work pseudozona formed in such a way are distinguished from `true zona' that are believed to comprise a single-layered extension emanating from a central body. The distinctive distal ornament is also formed by extensions in the outer layer. The inner body is 63(70)73 mm in diameter. The outer layer is closely adpressed to the inner body in both the proximal and distal wall. The junction between the outer layer and inner body is usually well de®ned, and forms a distinct suture, with no separation. The junction is often enhanced by the clear differences in colour and composition between the two layers: the outer layer is pale and homogenous and the inner body is darker with lamellate ultrastructure (see later). However, occasionally in the distal wall the junction is rather indistinct, although it can generally be traced along a series of tears/voids e.g. Plate VII, 1,3. At the equator, the outer layer is extended beyond the inner body forming a pseudozona. The zona measure 17(23)33 mm in width.

PLATE III TEM images of Samarisporites orcadensis [1,3 ˆ specimen b (Block 10); 2 ˆ specimen f (Block 10); 4 ˆ specimen e (Block 10); 5,6 ˆ specimen d (Block 10)]. 1. Image Q0629. Section through entire spore. Note the trilete mark (arrow) and the open lumen. Magni®cation £ 900. 2. Image Q0635. Section through entire spore. Note that the outer layer has been lost over the proximal surface (probably during transportation prior to burial). Magni®cation £ 680. 3. Image Q0627. Close up of part of Fig. 1. Note the open lumen and the suture passing up into the trilete mark (arrow). Magni®cation £ 2200. 4. Image Q0632. Section through part of spore illustrating the trilete mark (arrow). Magni®cation £ 2200. 5. Image Q0625. Section of part of spore illustrating the trilete mark. Magni®cation £ 3900. 6. Image Q0637. Close up of Fig. 5. Note the rather complex relationship between the trilete mark and its suture, the inner body (a and b layers) and outer layer, and the lumen. The suture appears to extend through the trilete mark (which essentially comprises the outer layer) but not into the inner body. There appears to be a wedge of material (arrow) present between the inner body and outer layer, and extending for a short distance up into the suture of the trilete mark. Magni®cation £ 6610.

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C.H. Wellman / Review of Palaeobotany and Palynology 116 (2001) 87±107

Within the zona there is a distinct suture where the proximal and distal walls are adpressed. Generally there is little or no gap between the proximal and distal wall in the zona, although in some specimens they appear to have been physically separated during compression e.g. Plate III, 1,3. The suture occasionally contains ovoid fragments of material of similar electron density to the outer layer e.g. Plate IV, 6. The suture extends to the inner body and generally there is little or no separation between the inner body and outer layer at the point where the zona diverges. In all cases there is prominent ornament associated with the distal surface. Invariably the ornament covers the entire distal surface that is in contact with the inner body. In some specimens, ornament is present on the zona, although in others it is absent from this region. Four specimens (a, b, d, e) reveal features of the trilete mark Plates III, 1,3,4,5,6; IV, 1,5. In three of the specimens (b, d, e), the trilete mark is tall, narrow and tapered. In a single specimen (a), it is short and stubby, but this is almost certainly an artefact resulting from direct polar compression of the laesurae. Dimensions of the trilete mark are provided in Table 1. All of the trilete marks possess a distinct suture. The suture extends from a short distance below the apex of the trilete mark (never reaching the surface of the spore) to the inner margin of the outer layer (i.e. it abuts against the inner body but does not continue into it). In specimens (a) Plate IV, 5 and (d) Plate III, 5,6, directly below the trilete mark, there is a wedge of material that lies between the inner body and outer

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layer, and extends a short distance up into the suture of the trilete mark. The outer layer varies in thickness in different parts of the spore. Dimensions at these various positions are provided in Table 3. In terms of ultrastructure, the outer layer is usually entirely homogeneous. However, in some specimens, there is a narrow dark layer on the outer margin e.g. specimen (a), Plate IV, although it is likely that this is artefactual. The inner body is fairly uniform in thickness, except that it is slightly thickened in the region of the equator, and in some specimens (a and d) it narrows below the trilete mark to accommodate the wedge of material that lies between the inner body/ outer layer in this region. Dimensions are provided in Table 4. The inner body exhibits complex ultrastructure. It is clearly bilayered. In the following description the inner layer of the inner body will be termed the a-layer and the outer layer of the inner body will be termed the b-layer. Ultrastructural features of the inner body are best illustrated in Plates V±VII. The a-layer is electron dense and is composed of tightly packed lamellae Plates V, 3,4); VI. The lamellae are electron dense and appear black. They are continuous and unbranched. Individual lamellae can occasionally be traced from the distal wall, around the equator, and into the proximal wall. Rarely lamellae are partially detached adjacent to the lumen e.g. Plates VI, 3,6; VII, 2. Measurements taken of these partially detached lamellae suggest they are 0.077 mm in thickness.

PLATE IV TEM images of Samarisporites orcadensis [all specimen a (Block 5)]. 1. Image Q0455. Section through entire spore. Magni®cation £ 1490. 2. Image Q0453. Section through part of spore illustrating the inner body/outer layer relationship where the zona begins at the outer margin of the inner body. Note the junction between the inner body and outer layer and the suture (arrow) between the proximal and distal surface of the outer layer in the zona. Magni®cation £ 6610. 3. Image Q0442. Section through part of spore illustrating the inner body/outer layer relationship where the zona begins at the outer margin of the inner body. Note the junction between the inner body and outer layer (arrows) and the suture between the proximal and distal surface of the outer layer in the zona. Magni®cation £ 11500. 4. Image Q0441. Close up of Fig. 6 illustrating the irregular wall at the periphery of the zona. Magni®cation £ 28500. 5. Image Q0437. Section of part of spore illustrating the trilete mark. Note the rather complex relationship between the trilete mark and its suture, the inner body (a and b layers) and outer layer, and the lumen. The suture appears to extend through the trilete mark (which essentially comprises the outer layer) but not into the inner body. There appears to be a wedge of material (large arrow) present between the inner body and outer layer, and extending for a short distance up into the suture of the trilete mark. The small arrow indicates the outer margin of the inner body. The `squat' trilete mark is probably a consequence of compression. Magni®cation £ 3900. 6. Image Q0438. Section of part of spore illustrating the zona. Note the ovoid fragment of material trapped within the suture of the pseudozona (arrow). Magni®cation £ 2950.

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The b-layer appears paler than the a-layer. It consists of less electron dense material (pale) containing occasional (between 5 and 10) lamellae that are electron dense and appear black [Plates V, 3, 4; VI, 5, 6; and VII. The lamellae are 0.025 mm in thickness.

They are 0.025±0.179 mm apart, becoming less closely spaced away from the a-layer. The lamellae are continuous and are straight near the margin with the a-layer, becoming more irregular towards the outer periphery of the b-layer. Where

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the lamellae become more irregular they are often associated with voids and tears. It is possible that these are artefactual.

5. Discussion 5.1. Gross structure and taxonomic implications Combined LM, SEM and TEM analysis provides detailed information on the structure and morphology of Samarisporites from Cromarty. The spores are clearly trilayered, with a bilayered inner body entirely enclosed within an outer layer. The outer layer forms the characteristic distal ornament, and is extended forming a prominent trilete marks on the proximal surface and a prominent pseudozona equatorially. However, the extent, if any, of cameration is dif®cult to interpret, because the spores have clearly been at least partially compressed. In the fossils, there is no evidence for signi®cant gaps between: (1) the inner body and outer layer; (2) the proximal and distal parts of the outer layer where they are extended into a pseudozona. I believe that at maturity the spores lacked any such cameration. Supporting this interpretation are a number of lines of evidence. For example, although the lumen is usually closed, in some specimens gaps are in places present, indicating that the spores are only partially compressed. No such gaps are ever preserved between the different spore layers, suggesting that they were not originally camerate. Furthermore, where the lumen is closed, the suture marking the original void is often irregular and torn, suggesting that it was physically closed during compression. However, the sutures between the inner body/outer layer, and between the outer layer in the zona, lack any such evidence for disruption, suggesting

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that they may be primary and do not represent closure of a camera. TEM analysis indicates that the spores are `pseudozonate', but that they lack a cingulum (i.e. they are not cingulizonate). This is analogous to McGregor and Cam®eld (1982)s interpretation of Middle Devonian species of Densosporites (see p. 89 and McGregor and Cam®eld, 1982, p. 33). McGregor and Cam®eld suggested that in the species of Densosporites they examined the dark ring on the outer edge of the central body was not a cingulum, but an optical effect resulting from `proximal±distal compression of the thick, strongly convex equatorial±distal region of the exoexine, accentuated by the tendency for concentration and fusion of sculpture at the outer limit of the contact areas'. They proposed as evidence for their interpretation: (1) the thick walled nature of D. devonicus as demonstrated by Allen (1965)'s microtome work; (2) the discontinuous nature of the `cingulum' in some specimens. McGregor and Cam®eld noted that in this respect the Middle Devonian forms were rather different in structure from typical Carboniferous representatives of the genus, and went as far as to suggest that it might be appropriate to assign them to a new genus. Clearly much more work (particularly sectioning) is required before we fully understand the structure of Devonian±Carboniferous zonate± cingulizonate spores, and the utilization of the genera used to accommodate them is standardized. Until such time I prefer to retain the genus Samarisporites for the spores described herein. Regarding speci®c identi®cation, it is clear that the spores are identical to those described by Richardson (1960) who subdivided them into three species. Like Marshall and Allen (1982), I ®nd a high degree of variability in the distal ornament (in terms of nature of the elements and their distribution). All three of the

PLATE V TEM images of Samarisporites orcadensis [all specimen a (Block 5)]. 1. Image Q0452. Close up of part of spore illustrating the junction between the outer layer/inner body and a-layer/b-layer (large and small arrows respectively). Magni®cation £ 15500. 2. Image Q0446. Close up of part of spore illustrating the outer layer and inner body (a and b layers). Junction between inner body and outer layer arrowed. Magni®cation £ 11500. 3. Image Q0443. Close up of part of spore illustrating the junctions between the outer layer/inner body and a-layer/b-layer (large and small arrow respectively). Magni®cation £ 39000. 4. Image Q0449. Close up of part of spore illustrating the junctions between the outer layer/inner body and a-layer/b-layer (large and small arrow respectively). Magni®cation £ 39000.

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species erected by Richardson can be recognized, but these appear as end members with complete morphological integration between them. I suggest they form part of a single population, with a reasonably high degree of intraspeci®c variation involving the nature of the distal ornament, and probably derive from a single plant species. I refer to the spores described herein as Samarisporites orcadensis because: ®rstly, the majority of the spores I examined can most comfortably be accommodated in S. orcadensis; secondly, S. orcadensis is the type species of Samarisporites and will have priority if it is accepted that the S. orcadensis, S. conannulatus and S. mediconus represent a population of a single species and are of®cially transferred into a single species. 5.2. Spore wall formation In the absence of any ontogenetic information, elucidation of spore wall formation is based on interpretation of gross morphology and preserved ®ne ultrastructure in the (presumably mature) spore sections, and is limited and rather speculative. Clearly lamellae are important in construction of both layers (a and b) of the bilayered inner body. It seems most likely that in the outer (b) layer the lamellae accumulated in a centripetal fashion. Towards the outside of the layer, they become thicker, more widely spaced and increasingly contorted. A possible explanation for these observations is that progressively older lamellae (i.e. those towards the outside) had more sporopollenin accreted onto them and hence are thicker and are more widely spaced and disrupted. There is no evidence indicating whether lamellae accumulation in the inner (a) layer was

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centripetal or centrifugal. It is possible that the alayer is simply a continuum of the b-layer, where there was a continuous accumulation of lamellae in a centripetal fashion, and hence younger lamellae are thin, parallel and closely spaced because little sporopollenin accumulated on them. However, it is also possible that the a and b layers are discrete and formed via different processes, rather than forming via a single continuous process (with the observed differences a result of variation due to differential compression and/or sporopollenin accretion). If this is the case, these layers probably formed via different processes either simultaneously or at different times (perhaps due to a distinct phase change). The outer layer is entirely homogeneous. Its mode of formation is unclear. Potentially lamellae might have been involved in its construction, but are not preserved in the mature spore walls because they were occluded during spore wall formation (either as they became increasingly compressed or as increasing amounts of sporopollenin was accreted onto them). Whether or not a tapetum was involved in deposition of the outer layer is also unclear (with sporopollenin derived from the tapetum deposited either directly onto the spore or onto a lamellate substructure). 5.3. Phylogenetic implications There is only one potential report of in situ Samarisporites. From the Middle Devonian of New Brunswick, Canada, Andrews et al. (1975) describe distinctive zonate or possibly pseudosaccate spores from Oocampsa catheta Andrews et al. 1975, a plant that appears intermediate between trimerophytes

PLATE VI TEM images of Samarisporites orcadensis [all specimen c (Block 10)]. 1. Image Q0607. Section through entire spore. Note that the outer layer has been lost over the proximal surface (probably during transportation prior to burial). Magni®cation £ 900. 2. Image Q0608. Close up of Fig. 1. Note where the outer layer has been removed from the proximal surface, both over the inner body and zona. Magni®cation £ 2950. 3. Image Q0616. Close up of Fig. 1 illustrating details of the inner body, and its relationship with the partially preserved outer layer. Magni®cation £ 8900. 4. Image Q0611. Close up of Fig. 1 illustrating the junction between the inner body and ornamented outer layer over the distal surface (arrow). Magni®cation £ 6610. 5. Image Q0610. Close up of Fig. 2 showing details of the inner body, and its relationship with the partially preserved outer layer. Note the junction between the a and b layers (arrow). Magni®cation £ 15500. 6. Image Q0618. Close up of Fig. 3 illustrating the partially detached lamella in the lumen. Magni®cation £ 15500.

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and progymnosperms. They suggest that the spores are closest to the dispersed taxa Perotrilites eximius Allen, 1965 or Samarisporites praetervisus (Naumova) Allen, 1965. Dispersed spore assemblages, from the Middle Devonian deposits of eastern Canada (Gaspe and New Brunswick) that have yielded Oocampsa catheta, have been described by McGregor (1973, 1977) and Richardson and McGregor (1986). McGregor (1973) placed Perotrilites eximius Allen, 1965 in tentative synonomy with Grandispora ?macrotuberculata Archangelskaya, a taxon reported from the eastern Canadian sequences. Subsequently McGregor and Cam®eld (1982) of®cially recombined Grandispora (Perotrilites) eximia (Allen) McGregor and Cam®eld, 1982. McGregor (1973) did not report Samarisporites praetervisus (Naumova) Allen, 1965 from the eastern Canadian sequences. McGregor and Cam®eld (1982) placed S. praetervisus with Cristatisporites. Recent TEM analysis of spores obtained from Oocampsa catheta (Wellman and Gensel, in preparation) indicates that it differs dramatically from Samarisporites orcadensis in terms of gross structure. Although the spores of O. catheta and S. orcadensis are similar in that an inner body is surrounded by an outer layer that forms a pseudozona, they differ because in the former there is clear separation between the inner body and outer layer in the distal wall, and the elements comprising the distal sculpture

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are hollow. Therefore I believe that the spores of O. catheta and S. orcadensis are fundamentally different and the former should not be included in the genus Samarisporites. Interestingly, Allen (1965) illustrates and describes thick sections of P. eximius (one of the dispersed spore taxa Andrews et al. (1975) compared with the spores of O. catheta). This taxon appears to be similar in structure to S. orcadensis and may thus warrant inclusion in the genus Samarisporites. More importantly, however, the dispersed spore taxon P. eximius clearly differs in structure from the in situ spores of O. catheta (see above). Hence, if P. eximius and G. ?macrotuberculata are synonymous, it would suggest that O. catheta is not the parent plant of these dispersed spores. However, it is also possible that P. eximius and G. ?macrotaberculata are not synonymous, and G. ?macrotuberculata may thus represent dispersed spores derived from the plant O. catheta. It will be interesting to examine sections of dispersed G. ?macrotuberculata from eastern Canada. There have been few publications reporting on sections of Middle Devonian `cingulizonate' spores and thus comparisons, and phylogenetic interpretation, are currently limited. Allen (1965) examined thick sections (2±3 mm in thickness) of a number of dispersed spore taxa from the Devonian of Vestspitsbergen. These sections provide details of gross structure of the spores but not ultrastructure. They include three taxa of cingulizonate spores: Densosporites

PLATE VII TEM images of Samarisporites orcadensis [all specimen c (Block 10)]. 1. Image Q0624. Section through part of spore illustrating the nature of the inner body. Note the closed lumen, junction between the a and b layers (small arrow) and junction between the inner body and outer layer (large arrow). Note that the outer layer is missing over the proximal surface. Magni®cation £ 15500. 2. Image Q0619. Section through part of spore illustrating the nature of the inner body. Note the lumen (L) containing a partially detached lamella, the junction between the a and b layers (small arrow) and junction between the inner body and outer layer (large arrow). Note the lamellae clearly visible in the b layer. Magni®cation £ 39000. 3. Image Q0621. Section through part of spore illustrating the nature of the inner body. Note the closed lumen and junction between the a and b layers (arrow). The junction between the inner body and outer layer is rather dif®cult to discern, but is probably marked by the aligned series of tears in the lower part of the photograph. Magni®cation £ 28500. 4. Image Q0620. Section through part of spore illustrating the nature of the inner body. Note the lumen (L), the junction between the a and b layers (small arrow) and junction between the inner body and outer layer (large arrow). Note the lamellae clearly visible in the b layer. Magni®cation £ 39000. 5. Image Q0615. Section through part of spore illustrating the nature of the inner body. Note the closed lumen and junction between the a and b layers (arrow). Note that the outer layer is missing over the proximal surface. Magni®cation £ 28500 6. Image Q0622. Section through part of spore illustrating the nature of the inner body. Note the junction between the a and b layers (large arrow). Note that the outer layer is missing over the proximal surface. Magni®cation £ 52000.

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Table 1 Details of trilete mark observed using TEM Specimen

Description

Height (mm)

Basal width (mm)

a [Plate IV,V] b [Plate III (1,3)] d [Plate III (5,6)] e [Plate III (4)]

Short and stubby Tall and tapering Tall and tapering Tall and Tapering

8.9 19.0 11.3 20.0

5.6 3.2 6.5 3.6

Table 2 General dimensions observed using TEM (mm) Specimen

Inner body diameter

Width of zona

Total wall thickness over body (prox. surface)

Total wall thickness over body (dist. surface)

Total wall thickness in zona

a [Plate IV, V] b [Plate III (1,3)] c [Plate VI, VII] d [Plate III (5,6)] e [Plate III (4)] f [Plate III (2)]

73 63 72 ± ± 73

17 and 20 24 and 33 17 and 19 ± ± 23 and 28

± 5.6 ± 2.3 2.3 ±

8.2 13.3 6.4 5.1 5.5 12.2

± 3.1 ± 2.7 2.5 ±

Table 3 Wall thickness (mm) in the outer layer Specimen

Proximal surface over the body

Proximal surface over the zona

Distal surface over the body

Distal surface over the zona

a [Plate IV, V] c [Plate VI, VII] d [Plate III (5,6)]

0.95±2.56 ± 1.51

0.98

4.87 3.48±4.90 ±

2.19

0.93

2.03

Table 4 Wall thickness (mm) in the inner body Specimen

Total proximal

Total distal

a-layer (prox.)

a-layer (dist.)

b-layer (prox.)

b-layer (dist.)

a [Plate IV, V] c [Plate VI, VII] d [Plate III(5,6)]

1.48 1.35 0.76

1.00 1.23

0.18±0.23

0.21±0.26

0.68±2.82 1.13

0.71 1.00

devonicus Richardson, 1960, Samarisporites hesperus Allen, 1965 and Samarisporites triangulatus Allen, 1965. D. devonicus is shown to have a particularly thick distal exine, but the nature of the cingulizonate structure is unclear, and evidence for wall layering is lacking. S. hesperus is shown to have an abruptly

tapering cingulum, although the precise nature of the associated zona is unclear. Interestingly, Allen (1965, p. 715) interpreted the exine as unilayered. S. triangulatus is shown to possess a cingulum that extends into a distinct zona. It is bilayered, with an indistinct intexine that is 1±2 mm in thickness, and is

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closely adpressed to a ®nely infragranulate exoexine that extends into the equatorial ¯ange. In none of these spores is there obvious separation between different wall layers. As more data on gross structure and wall ultrastructure in Middle Devonian spores becomes available, it is anticipated that detailed comparisons will shed light on the distribution of gross structure/wall ultrastructure characters among different plant groups, and thus facilitate interpretation of spore af®nities and provide characters of use in phylogenetic analysis. 5.4. Functional morphology Comment on the functional morphology of the spore Samarisporites orcadensis is highly speculative in the absence of modelling or any other relevant experimentation. However, it is interesting to re¯ect on possible function, and its relationship to morphological evolution, in the diverse and abundant group of `zonate±pseudosaccate' spores that appear and proliferate during the Devonian. S. orcadensis is interpreted as comprising an inner body surrounded by an outer layer (but with no cameration) with a pseudozona formed by extension, and close adpression, of the outer layer in the equatorial region. Clearly zona (be they true zona or pseudozona) may act to improve the buoyancy of the spore in air, or improve its aerodynamic qualities in some other way, and this is most likely their primary function. Balme (1995) suggests that pseudozona may represent an intermediate stage between cameration and true zona. It is most probable that zona and pseudozona are analogous and have arisen via different routes through homoplasy. Interestingly, all of the spores I have sectioned to date (including species of Auroraspora and Calyptosporites) appear to possess pseudozona and not true zona. The functional morphology of the rather distinctive ornament is uncertain Most likely it either aids the dispersal of the spore (perhaps improving the aerodynamic qualities of the spores), lodging of the spore, or is involved in germination regulation. 5.5. Comments on Middle Devonian spore genera Rather alarmingly, TEM work is demonstrating potential problems with structural interpretations based on LM analysis. It is becoming clear that differ-

105

ent layers in multilayered spores may have differing optical properties, and this can be misleading when attempting to interpret wall thickness and spore structure. This problem is enhanced when coupled with optical effects resulting from compressional artefacts. For example, McGregor and Cam®eld (1982) note that: (1) zona are often thicker than anticipated (as illustrated by the work of Allen, 1965); (2) it is easy to misinterpret the nature of zonae±cingula. Additionally, it can be very dif®cult, if not impossible, to differentiating between a true and pseudo zona through LM work. Regarding Middle Devonian spores, most detailed taxonomic studies are based predominantly on LM analysis. SEM analysis has been undertaken to a certain extent, but reveals little regarding spore structure, while very little work has been based on sectioning. Consequently, the potential for structural misinterpretation based on LM work is worrying. Clearly great care is required and optimally spores should be examined using LM, SEM and TEM to achieve maximum reliable information. Devonian dispersed spores are currently classi®ed in an arti®cial morphology-based classi®cation (e.g. Traverse, 1988). However, there is little agreement among different workers as to which characters are of most use/importance and should be utilized in establishing and de®ning spore genera. This is partially true because there has been limited analysis of the distribution of different characters among different plant taxa (via studies of in situ spores), and hence it is unclear as to which characters are biologically meaningful (i.e. which characters are diagnostic of different plant taxa, and their range of variation within taxa). While I accept that the current arti®cial morphology-based classi®cation is pragmatic with the paucity of in situ spore studies, in my opinion spore genera should as far as possible be based on biologically meaningful characters, and hence our arti®cial morphology-based classi®cation will begin to approach a true biological classi®cation. Thus, spore genera should be modi®ed by of®cially emending them as and when such information becomes available. As a consequence of the confusion over how best to establish and de®ne Devonian spore genera, they have been created on an ad hoc basis. Different workers have utilized different criteria in establishing (and

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utilizing) Middle Devonian spore genera resulting in a state of near chaos. Different workers utilize different genera for essentially the same thing, use the same genus in different ways, place spores with well circumscribed Carboniferous spore genera (and in doing so clearly deviate from the original concept) and so on. In order to resolve these problems and create a more meaningful Middle Devonian spore taxonomy requires: (1) detailed combined LM, SEM and TEM analysis of dispersed spores in order to ascertain their morphological, structural and ultrastructural characters correctly; (2) more work on in situ spores in order to clarify the biological af®nities of the spores, and the range of morphological variation within individual plant taxa; (3) analysis of the distribution of spore characters among the plant kingdom in order to ascertain the biological meaningfulness of characters, and thus identify those that should be used to establish and de®ne spore genera. 6. Conclusions Combined LM, SEM and TEM analysis of dispersed Devonian spores sheds light on spore morphology, gross structure and wall ultrastructure. Such analysis provides characters that allow us to classify the spores (in an arti®cial morphologybased classi®cation). It is demonstrated that TEM analysis is particularly useful in clari®cation of spore gross structure, in addition to providing a whole new suite of ultrastructural characters of potential use in spore classi®cation. Clearly there are currently problems with the taxonomy of Middle Devonian spore genera, largely as a consequence of problems involving the interpretation of spore morphology/structure and disagreement over which characters are of most use in their de®nition. It is anticipated that detailed combined LM, SEM and TEM analysis, incorporated with studies of in situ spores, will help resolve some of these problems. Additionally, such analysis also provides evidence that can be utilized in the interpretation of spore wall formation and spore af®nities/phylogeny. Regarding the latter, it is anticipated that as more work is undertaken we will begin to recognize patterns in the distribution of spore characters

among the plant kingdom, and be able to utilize these to shed light on spore af®nities and interpret spore/plant phylogeny.

Acknowledgements This work was supported by the NERC research grant GR8/03668. I would like to express my gratitude to Mr John Proctor (Department of Biomedical Science, University of Shef®eld) who prepared the material for TEM analysis.

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