Ultrastructure of exine of gymnospermous pollen grains from Jurassic and basal Cretaceous deposits in Northwest Europe and implications for botanical relationships

REVIEW OF PALAEOBOTANY AND PALYNOLOGY

ELSEVIER

Review of Palaeobotany and Palynology 99 (1997) 25 54

Ultrastructure of exine of gymnospermous pollen grains from Jurassic and basal Cretaceous deposits in Northwest Europe and implications for botanical relationships D.J. Batten a,,, R.J. D u t t a b a Institute of Geography and Earth Sciences, University of Wales, Aberystwyth SY23 3DB, UK b 16 Ellington Rd, Muswell Hill, London NIO 3DG, UK Received 17 December 1996; received in revised form 10 April 1997; accepted 11 April 1997

Abstract Ultrathin sectioning and examination of gymnosperm pollen grains from various Northwest European, midMesozoic successions has confirmed or added weight to previous suggestions of botanical relationships for some taxa, and indicated possible affinities for others. The sections of Araucariacites australis, Callialasporites dampieri, C. trilobatus and C. turbatus support a derivation from the coniferous family Araucariaceae. Although differing in gross morphology from pollen of both extant Ephedra and Welwitschia of the order Gnetales, Eucommiidites troedssonii has ultrastructural characters in common with these, and with Triassic Equisetosporites. Cerebropollenites macroverrucosus is widely accepted as not being closely comparable to pollen of modern Tsuga, but ultrastructural similarities suggest the possibility of an ancestral connection. The structure of the exine of Clavatipollenites hughesii sensu Schulz from Jurassic deposits is fundamentally different from that of Cretaceous grains referred to the same species, confirming observations made previously on the basis of analysis under the light microscope, and suggesting a possible derivation from cycadalean rather than angiospermous plants. Species of Chasmatosporites may also be linked to the Cycadales, or perhaps to the Ginkgoales. Pihtsporites couperi is shown to be a gymnosperm pollen grain rather than a pteridophyte spore, but more precise (family) links have not been established. The protosaccate structure of Quadraeculina anellaeformis is clearly demonstrated but its botanical affinity remains enigmatic. Previously suggested relationships between Spheripollenites and members of the Araucariaceae, Cupressaceae and Taxaceae are not supported. They do not seem to lie with any modern gymnosperm family, nor with ancient angiosperms. © 1997 Elsevier Science B.V.

Keywords." Mesozoic; pollen; ultrastructure; relationships; gymnosperms

1. Introduction V a r i o u s M e s o z o i c g y m n o s p e r m p o l l e n grains have been sectioned in o r d e r to c o m p a r e a n d c o n t r a s t the structure o f their exines with each * Corresponding author. Fax: + 44-1970-622659; e-mail: [email protected] 0034-6667/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PH 0034-6667(97)00036-5

o t h e r a n d with p u b l i s h e d thin sections o f fossil a n d m o d e r n pollen. T h e a i m was to shed m o r e light on their b o t a n i c a l affinities a n d e v o l u t i o n a r y r e l a t i o n s h i p s t h a n is possible solely on the basis o f gross m o r p h o l o g y . T h e thin sections o b t a i n e d were e x a m i n e d u n d e r a t r a n s m i s s i o n electron m i c r o scope ( T E M ) . S o m e o f the p o l l e n types selected for analysis, n a m e l y species o f Araucariacites,

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D.J. Batten, R.J. Dutta / Review q/Pahteobotany and [email protected] 99 (1997) 25 54

Callialasporites, Clavatipollenites, Eucommiidites

anellae/~n'mis, core preparation DB3377, Danish

and Spheripollenites, have been examined in this way before. They were sectioned again for a variety of reasons: (1) to determine the degree of consistency in structural make up for specimens from geographically widely separated localities and the amount of morphological overlap between genera (Araucariacites, Callialasporites); (2) if possible, to expand on conclusions drawn previously (Eucommiidites, Spheripollenites); and (3) to examine specimens from different stratigraphic levels purported to be of the same species (Clavatipollenites hughesii from Jurassic deposits). Grains for which no transmission electron micrographs have been published hitherto were selected from species of Cerebropollenites, Chasmato,v)orites, Pilasporites and Quadraeculina. Until now, suggestions as to the affinities of C2~rebropollenites and Chasmatosporites have been made solely on the basis of their gross morphology. The botanical relationships of Quadraeculimt and the species of Pilasporites examined (P. couperi, which is not typical of the genus) have previously proved difficult to determine. It was hoped that our analysis might lead to greater precision in this respect.

sector, southern North Sea; Lower Jurassic. Chasmatosporites hians and C. ma/or, preparations BF5188 and 5203, Bagfi Formation, exposure at Korsodde, Bornholm, Denmark; upper Pliensbachian Toarcian. Clavatipollenites hughesii sensu Schulz (1967) and Eucommidiites troedssonii, preparation SB3470, Sose Bugt Member, Ronne Formation, coastal exposure at Sose Bugt, Bornholm. Denmark: Hettangian Sinemurian. Pilasporites couperi, preparation MCP4010, lower Purbeck Group, Lulworth Formation, Perryfield Quarry, Isle of Portland, Dorset, southern England; upper Tithonian or lower Berriasian. Spheripollenites psilatus, core preparation PRC2514, Anholt Borehole, depth 299.9 m, Fjerritslev Formation, Anholt, Denmark: Toarcian, and cuttings preparation PRC2839, Dutch sector, southern North Sea; Toarcian. The samples were processed for their organic content using standard palynological techniques (see, e.g., Batten and Morrison, 1983). Where necessary, finely particulate and amorphous matter was removed by brief ( < 2 minutes) ultrasonic vibration and/or oxidation using fuming nitric acid followed by filtering through a simered glass funnel fitted to a Buchner flask. Individual grains were picked from drops of residue that had been strewn over a glass microscope slide and allowed to dry. Each was immersed in a solution of uranyl acetate for 30 minutes and then washed three or four" times in distilled water. After dehydration in acetone for a similar length of time they were soaked in a 1:1 mixture of resin and acetone for a further 30 minutes prior to being embedded in Emix resin (Agar Scientific, Stanstead, Essex, UK ) of medium hardness in flat moulds and polymerised overnight in an oven. The resulting resin blocks were trimmed and thin sections cut on an ultramicrotome (LBK 880A U L T R O T O M E 11I) using glass knives. Sections that displayed gold or silver-grey interference colours were collected on formvarcoated slot grids and examined under a JEOL JEM-100CX TEM. It was found that the thicker, gold-coloured sections produced the best images at magnifications below × 10,000, and the thinner, silver sections were more suitable for analysis at

2. Material and methods

Specimens of the following taxa (Plate I) were selected for thin-sectioning and study under the TEM: Araucariacites australis, cuttings preparation PRC2836, Delfland Formation, southern North Sea area; upper Kimmeridgian-lower Volgian, and cuttings preparation PRC2996, Weiteveen Formation, southern North Sea area: Kimmeridgian lower Volgian. Calliahtsporites daml)ieri, C. trilobatus and C turbatus, cuttings preparation PRC2836, Delfland Formation, southern North Sea area; upper Kimmeridgian lower Volgian. Cerebropollenites macroverrucosus, cuttings preparation PRC2996, Weiteveen Formation, southern North Sea area; Kimmeridgian lower Volgian. Chasmatosporites apertus and Quadraeculina

D.,L Batten, R.J. Durra / Review o f Palaeobotany and Patynology 99 (1997) 25-54 PLATE

27

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PLATE I

Representative specimens of the taxa sectioned. All magnifications x 500, except where indicated. 1. Araueariacites australis, 2. C~dliatasTyorites trilobatus. 3. Caltialasporites turbatus, 4. Chasmatosporites mcdor. 5. Callialasporites dampieri. 6. Cerebropottenites macroverrucosus. 7. (.'hasmatosporites apertus. 8. (i7~asmato,sporites hians. 9. Clavatipollenites hughesii sensu Schulz, x t000, 10. Eucommiidites troedssonii, x 1000. 11. Pihlsporites couperi. 12. Quadraeeulina anellaefi)rmis'. 13. Spheripollenites psilatus,

p~

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D.J. Batten, R.Z Dutta / Review o f Palaeobotany and Palynology 99 (1997) 25 54

higher magnifications. Hence, for each specimen both gold and silver sections were cut. The former were collected on 2 x 1 mm slot-grids which allow low magnification photographs to be taken without the danger of any areas being obscured by mesh. The silver sections were mounted on 400 mesh grids. All specimens were completely sectioned but failure rates were high for some species (e.g., for Pilasporites couperi). In addition, a few specimens proved on cutting to be awkwardly orientated. Those with a distal sulcus were placed, as far as possible, with the long axis of the aperture at right angles to the plane of sectioning. When selecting specimens for ultrastructural examination both the ontogeny of the grains and their state of preservation were considered. In dispersed fossil pollen assemblages a developmentally immature grain can sometimes be inferred from the structure of its wall, especially around an aperture which may be incompletely formed, but there is no evidence that any of the specimens we sectioned were immature. They were picked on the basis that in transmitted light they seemed to be both typical representatives of the taxa and reasonably well preserved. Hence, although we cannot be absolutely sure in all cases, it is thought that the descriptions in this paper refer mostly, if not entirely, to the characteristic ultrastructure of mature pollen grains.

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3. Systematic palynology: descriptions of thin sections and discussion The terms sexine (and subdivisions thereof) and nexine rather than ectexine, foot layer and endexine (see Punt et al., 1994) are used to describe, respectively, the outer and inner wall layers of the specimens sectioned. Authorities and dates are given for all fossil species with which comparisons are made. Extant species are provided only with the names of authors. Genus Araucariacites Cookson, 1947 ex Couper, 1953

Remarks: Cookson (1947) noted the resemblance of inaperturate grains she encountered in Tertiary lignites from the Kerguelen Archipelago, Southern Ocean, with the pollen of modern members of the Araucariaceae, widely regarded to be the most primitive living family of the Coniferales; hence her decision to name them Araucariacites. She described one species, A. australia'. Kendall (1949) isolated pollen comparable to this species from male cones preserved in the Middle Jurassic succession of northern Yorkshire, England. Attached to leafy shoots identified as Brachyphyllum mamillare Brongniart, 1828, these pollen-bearing organs were also assigned to the

PLATE II

1 3. Araucariaeites australis, specimen 1. 1. Entire cross section, x 2500. 2. Proximal and distal walls showing granular sexine and outer pale, and inner dark nexine, x 10,000. 3. As for 2 at higher magnification; lamellae of nexine barely discernible, x 20,000. 4-6. Araueariacites australis, specimen 2. 4. Outer sexine more coarsely granular than inner part of this layer; outer nexine irregularly lamellated, x 25,000. 5. Equatorial region of specimen comprises a zone of expanded sexine, x 10000. 6. Oblique view of wall showing outer nexine with well- defined lamellae, x 25,000. 7, 9, 10. Calliala.v~orites dumpieri. 7. Entire cross section; sexine of varying thickness, consistent with crumpled appearance in transmitted light, x 2000. 9. Proximal and distal wails tightly adpressed; granular sexine separated from nexine of more homogeneous aspect by a partly vacuolate outer nexinal layer, x 10,000. 10. Granular sexine merges with lamellated nexine via an irregularly lamellate vacuolate zone. x 20,000. 8, 11, 12. Callialasporites trilobatus specimen 1. 8. Granular sexine clearly separated from lamellated nexine in equatorial region, x 15,000. 11. Granular sexine and lamellated nexine in central area of grain are of approximately equal thickness; inner surface of nexine irregularly granulate to apiculate, x 20,000. 12. Cross section of whole specimen, x 1500.

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D.J. Batten, R.J. Dutta / Review qf'Palaeobotany and Palynoh)gy 99 (1997) 25 54

Araucariaceae (for descriptions of the shoots, see Kendall, 1947). Van Konijnenburg-van Cittert (1971) recorded two pollen-types in cones of B. mamillare from the Middle Jurassic 'Whitby plant bed' on the Yorkshire coast. The first, which was rather more common than the second (59% as opposed to 41%), is spherical in shape and the sexine and nexine are attached to each another. It is comparable to A. australis. In the second type the nexine is separated from the sexine forming an inner body which varies in shape from circular to sometimes triangular. The sexine is folded and wrinkled around the central body and in some cases appears trilobate, in common with representatives of the dispersed pollen genus Callialasporites Sukh Dev. Pollen grains referable to Araucariacites have also been recovered from male cones identified as Nothopehuen brevis Del Fueyo, 1991 encountered in the Lower Cretaceous (probably Aptian) Baquer6 Formation in Santa Cruz Province, southern Argentina (Del Fueyo, 1991). Some of the cones are attached to branches with small leaves of the Brachyphyllum-type. The gross morphology of Araucariacites combined with the macrofossil evidence confirms its gymnospermous nature, and its reference to the Araucariaceae has been generally accepted by palynologists.

Araucariacites australis Cookson, 1947 ex Couper, 1953 (Plate I, 1; Plate I1, 1-6) Description of specimens sectioned: Exine 1.1 1.4 lain thick, distinctly layered. Sexine ca. 0.6 gm thick, composed of irregularly shaped, closely packed granules of sporopollenin 0.1 0.5 pm in diameter; larger granules may dominate outer part, becoming smaller adjacent to nexine. Nexine 0.4 0.6 gm thick, lamellated. Lamellae ca. 0.1 gm thick, commonly difficult to see because they are pressed tightly together; most prominent adjacent to sexine. Outer part of nexine has same electron density as sexine: inner part, which tends to be thinner (ca. 0.1 gin), is darker in colour. Distinctions and comparisons: A specimen of A. australis from the Lower Cretaceous

(Valanginian-Hauterivian) Sunday's River Formation in South Africa was shown by Zavada ( 1992, p. 45, figs. 7 and 8) to have a thick, lamellated nexine similar to that of our specimens but a sexine comprising a homogeneous, imperforate zone that is underlain by an "infrastructural layer of thin irregularly shaped anastomosing rods", beneath which are "thin rods orientated parallel to the surface of the pollen grain", giving this part a laminated appearance. The structure of specimens of Araucariacites sp. from the Lower Cretaceous Baquer6 Formation (see above for details) in southern Argentina (Archangelsky, 1994, pp. 187, 193, 194; pl. 1, figs. 8, 9; pl. 2, fig. 13; pl. 3, figs. 16, 17; pl. 4, figs. 21, 22) bears some resemblance to that seen in both Zavada's and our sections of A. australis. The sexine is composed of elongate granules or rods of sporopollenin which, towards the inner part, are oriented parallel to the surface of the grain. As in all Araucariacites grains that have been examined ultrastructurally, the nexine is lamellated. The spongy sexine of A. hungaricus Defik from Portuguese Upper Cretaceous (Turonian) sediments (Kedves, 1985a, pl. 1, fig. 3) is also composed of granular and elongate sporopollenin elements, but no preferred orientation is apparent in any part of it (see also Kedves, 1994, pl. 13, figs. 1 3: pl. 14). Both A. australis 'aegypticus" and A. balinkaense (=A. fsp. 1 and 2, respectively, in Kedves and Pfirdutz, 1974), from upper Nubian Sandstone (Maastrichtian) deposits in Egypt, have a granular sexine and a lamellated nexine (see Kedves, 1994, pl. 11, figs. 3 7; pl. 12, figs. 1 5). The diameter of the granules decreases towards the nexine. Two genera, Agathis and Araucaria, make up the modern family Araucariaceae. Pollen grains of three species have been sectioned previously. Those ofAgathis alba Foxworthy have a clearly laminated nexine and a granular sexine (Van Campo and Lugardon, 1973, pp. 178, 180, pl. 2, fig. 1). The granules do not seem to be as tightly packed, the surface of the sexine is more uneven, and the nexine does not appear to comprise two layers of differing electron density. Nevertheless, the structure of the wall is clearly similar to that of our specimens of Araucariacites australis. The structure

D.,L Batten, R.J. Dutta / Review of Palaeobotany and Palynology 99 (1997) 25 54

of pollen from Agathis australis D. Don ex Lindley (see Kurmann, 1992, fig. 1F) and Araucaria angustifolia (Bertoloni) Kuntze (see Ueno, 1958, pl. 3, fig. N; 1959, p. 77, fig. 3E) is also similar. Of the pollen grains from taxaceous species that have been sectioned, the sexine of those from Amentotaxus argotaenia (Hance) Pilger is composed of distinct outer and inner layers of large and small granules, respectively (Xi and Wang, 1989, p. 139, fig. 12A, B). In other species, such as Torreya grandis Fort and T. yunnanensis C.Y. Cheng, W.C. Cheng et L.K. Fu, the granules of the outer sexine are partly fused, forming an incomplete tectum (Xi and Wang, 1989, p.139, fig. 13A, D). The sexine of grains from Taxus baccata Linnaeus (cf. Ueno, 1959, fig. 3A; Gullv~tg, 1966, p. 437, pl. 11, fig. a; pl. 12; Pettitt, 1966, pp. 245, 246, pl. 16, figs. 1 3) consists of little more than scattered granules. In general it seems that taxaceous pollen, like Araucariacites australis, possesses both a granular sexine and a lamellated nexine, but the granules tend to be larger and/or more variable in size. The asaccate pollen produced by two genera of the Pinaceae, Larix and Pseudotsuga, have an atectate granular structure similar to that seen in Agathis australis but they may also possess a thin foot layer (inner sexine), although this is not always discernible (Afzelius, 1956, fig. 4; Ueno, 1958, pl. 3, figs. L, M; Gullvhg, 1966, pp. 438,439, pls. 18-20; Kurmann, 1992, fig. 1E; Kurmann and Zavada, 1994, fig. 29). It is not present in Araucariacites australis. Although commonly indistinct, a foot layer may also be encountered in pollen of the Taxodiaceae (e.g., Kedves, 1985b, pl. 5; Xi and Wang, 1989, pp. 129, 133, figs. 5A, 6C, 7C, 8B; Kurmann, 1990a, fig. 12; 1992, fig. 2B), some Cupressaceae [e.g., in Cupressus arizonica E. Greene, see Van Campo and Lugardon, 1973, pl. 2, fig. 2; but not in Platycladus orientalis (Linnaeus) Franco, see Xi and Wang, 1989, fig. 9A] and in the single asaccate, monospecific genus Saxegothaea Lindley of the Podocarpaceae (see S. conspicua Lindley in M6dus et al., 1989, p. 21, fig. 1E, F). Genus Callialasporites Sukh Dev, 1961

31

Remarks: As noted above, pollen comparable to Callialasporites has been found with grains referable to Araucariacites in the male cones associated with Brachyphyllum mamillare. Callialasporitestype grains (recorded as Tsugaepollenites) were also encountered by Townrow (1967) in cones from the Jurassic uppermost Beacon Group of East Antarctica identified as Masculostrobus warrenii Townrow, 1967 and ascribed to the Podocarpaceae. Archangelsky (1966) assigned Apterocladus lanceolatus Archangelsky, 1966 from the Baquer6 Formation in southern Argentina (details above), with which Callialasporites had been associated by Gamerro (1965), to the Podocarpaceae mainly on the basis of leaf cuticle characters. Van Konijnenburg-van Cittert (1971) pointed out, however, that there are several differences between Apterocladus and the other members of the Podocarpaceae, one of which is the form of the pollen grains. Apart from pollen of Saxegothaea, the wall structure of which she considered to be at variance with that of Callialasporites (see above), most grains of modern Podocarpaceae are clearly bi- or trisaccate. Similar Balmeiopsis has been associated with a cone connected to Brachyphyllum irregulare Archangelsky, 1963 and to other isolated cones (Archangelsky and Gamerro, 1967) tentatively suggested to be of podocarpaceous origin (Archangelsky, 1963), but a relationship with the Araucariaceae now seems more likely (e.g., Balme, 1995).

Callialasporites dampieri (Balme, 1957) Sukh Dev, 1961 (Plate I, 5; Plate II, 7, 9, 10)

Description of specimens sectioned: Exine ca. 1.5 ~tm thick, composed of sexine and nexine, both of which have a distinctive structure. Sexine ca. 0.7 lam thick, consisting of irregularly shaped to elongate globules of sporopollenin up to 0.4 ~tm in maximum diameter; forms outer 'envelope' of grain seen in transmitted light. Elongate globules dominate outer part of sexine; long axes mostly perpendicular to surface. Nexine ca. 0.8 ~tm thick, irregularly lamellated, comprises 'inner body' of grain. Individual layers ca. 0.1 ~tm thick; most are tightly adpressed making it difficult to determine

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D.J. Batten, R.J. Dutta / Review of Palaeobotanyand Palynology 99 (1997) 25-54 exactly how m a n y are present; more opened out and clearly delineated adjacent to sexine, giving wall a vacuolate appearance.

Callialasporites trilobatus ( Balme, 1957) Sukh Dev, 1961 (Plate I, 2; Plate II, 8, 11, 12; Plate III, 1, 2, 4) Description o f ~pecimens sectioned: Exine ca. 1.0/am thick, consisting of two distinct layers. Sexine ca. 0.5-0.7/am thick, composed of irregularly shaped globules of sporopollenin < 0 . l - c a . 0.3/am in diameter; forms outer 'envelope' of grain seen in transmitted light. Nexine ca. 0.5 ~tm thick, comprises four or five lamellae ca. 0.1-0.2/am thick forming 'inner body' of grain; inner surface may be unevenly granulate to apiculate. In one specimen nexine is divisible into a paler outer, irregular zone of same electron density as sexine, and a darker, electron dense, inner layer. Callialasporites turbatus (Balme, 1957) Schulz, 1967 (Plate I, 3; Plate III, 3, 5, 6) Description o f specimens sectioned: Exine ca. 1.2/am thick, with readily distinguishable outer and inner layers. Sexine ca. 0.7/am thick, composed of small granules mostly ca. 0.1-0.2/am in diameter; forms outer 'envelope' of grain seen in transmitted light. Nexine ca. 0.5 ~tm thick, lamellated, comprises 'inner body' of grain. Lamellae ca. 1 /am thick but tightly adpressed, rendering it difficult to determine number of layers present; most prominent adjacent to sexine.

33

Distinctions and comparisons: The exines of all three species sectioned here comprise an atectate, granular sexine which forms the outer 'envelope', and a lamellated nexine forming the inner body of specimens seen under a transmitted light microscope. This structure is closely similar to that of our specimens of Araucariacites australis and of Callialasporites sp. from the Baquer6 Formation (Archangelsky, 1994, pp. 187, 188, 193, 194, pl. 1. figs. 5-7; pl. 2, fig. 12; pl. 3, fig. 18; pl. 4, fig. 20) except that the granules of the sexine in the latter are more elongate. Adjacent to the nexine these may be aligned perpendicular to the surface of the grain; alternatively, particularly at the equator where the sexine is detached, they may be mostly parallel to it. Their construction is also clearly comparable to that of the exine of Balmeiopsis sp. (Archangelsky, 1994, pl. 1, figs. 1-4; pl. 2, figs. 10, 11; pl. 3, figs. 14, 15; pl. 4, fig. 19) from the same succession, and of Balmeiopsis limbatus (Balme) Archangelsky, 1977 from Lower Cretaceous (Aptian-Albian) deposits at Deep Sea Drilling Project Site 361 on the continental rise of the southwest coast of Africa, in which the inner part of the sexine comprises irregularly elongate elements (Zavada, 1992, p. 45, figs. 9-11). Fossil podocarpaceous pollen differs significantly in both gross morphology and ultrastructure. For example, in addition to having three sacci attached to the distal surface of the grain (Baldoni and Taylor, 1982, pl. 1, figs. 2-4), the exine of Trisaccites pollen isolated from a podocarpaceous cone, again from the Baquer6 Formation,

PLATE lll 1, 2, 4. Callialasporites trilobatus, specimen 2. 1. Oblique section showing granular nexine and lamellated, partly vacuolate nexine, inner zone of which is darker and, therefore, more electron dense, x 20,000. 2. Proximal and distal walls closely adpressed; electron dense inner nexine clearly differentiated, x 15,000. 4. As for 2 but at higher magnification; inner nexine has a very finely granular lamellate aspect. × 20,000. 3, 5, 6. Callialasporites turbatus. 3. Part of central area; proximal and distal walls closely adpressed; sexine and nexine clearly delineated, x 10,000. 5. Entire cross section; central area two-layered, forming central body of grain seen in transmitted light, x 1500. 6. Granular sexine underlain by weakly lamellated nexine. × 25,000. 7, 8. Cerebropollenitesmacroverrucosus, specimen 1. 7. Entire cross section; proximal and distal walls closely adpressed, x 1500. 8. Close-up of sacci composed of convoluted sexine. × 5000. 9, 10. Cerebropollenitesmacroverrucosus, specimen 2. 9. Proximal polar part of specimen; globular elenaents of sexine underlain by a thin nexine, x 10,000. 10. Detail of lamellated nexine and adjacent inner sexine. × 25,000.

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D.J. Batten, R.J. Dutta ,; Review ~f Palaeobotany and Palvnology 99 (1997) 25 54

PLATE IV

5

8

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12

D.J. Batten, R.J. Dutta / Review of Palaeobotany and Palynology 99 (1997)25 54 was s h o w n b y B a l d o n i a n d T a y l o r (1982, pp. 26, 28, 30; pl. 2, figs. 2, 5; pl. 3, figs. 1 - 6 ) to be c o m p o s e d o f a c o l u m n a r o u t e r sexine, an alveolate inner sexine, a n d a thin h o m o g e n e o u s nexine. T h e y discussed the similarities between the u l t r a s t r u c t u r e o f Trisaccites a n d pollen o f m o d e r n p o d o c a r p a ceous Dacrycarpus dacrydioides ( R i c h a r d ) D e L a u b e n f e l s which has a sexine o f alveolate to c o l u m e l l a t e structure ( P o c k n a l l , 1981, fig. 1 6 j - l ) . T h e type o f structure shown b y Callialasporites, in c o m m o n with t h a t o f Araucariacites, is seen t o d a y o n l y in a s a c c a t e c o n i f e r a l e a n p o l l e n p r o d u c e d by all m e m b e r s o f the A r a u c a r i a c e a e , Cupressaceae, Taxaceae and Taxodiaceae, and s o m e representatives o f the P i n a c e a e a n d P o d o c a r p a c e a e . O f these, Callialasporites resembles m o s t closely p o l l e n o f the A r a u c a r i a c e a e . This suggests that, on the basis o f u l t r a s t r u c t u r e alone, the affinities o f species o f Callialasporites are m o r e likely to lie with the A r a u c a r i a c e a e t h a n the P o d o c a r p a c e a e , a l t h o u g h links with the l a t t e r c a n n o t be entirely ruled out. G e n u s Cerebropollenites Nilsson, 1958

Remarks: C o u p e r (1958, p. 155) r e g a r d e d the distinctive pollen g r a i n Cerebropollenites macroverru-

35

cosus (as Tsugaepollenites mesozoicus C o u p e r , 1958) to be o f coniferous origin on the basis o f its gross m o r p h o l o g y . H e c o n s i d e r e d it to be similar in s o m e ways to m o d e r n Tsuga pollen b u t p o i n t e d o u t that (1) the exinal folds o f the M e s o z o i c f o r m are larger; (2) there is less differentiation between the p r o x i m a l a n d e q u a t o r i a l sculpture t h a n in the m o d e r n pollen; a n d (3) no M e s o z o i c p l a n t s are k n o w n to have affinities with Tsuga. Cerebropollenites macroverrucosus (Thiergart, 1949) Schulz, 1967 ( P l a t e I, 6; Plate III, 7-10; Plate IV, 1 - 6 ) Description o f specimens sectioned: Exine ca. 0 . 8 - 3 . 2 ~tm thick, t w o - l a y e r e d . Sexine varies in thickness f r o m ca. 0.4 ~tm in vicinity o f sulcus to 2.8 ~tm elsewhere; c o m p o s e d o f irregularly shaped, tightly p a c k e d granules o r globules o f s p o r o p o l lenin o f v a r y i n g size t h a t are j o i n e d t o g e t h e r to f o r m a c o n v o l u t e d layer e n c o m p a s s i n g m a n y small saccate structures. Sacci are either h o l l o w p r o t u berances over nexine o r m o r e o r less solid bodies c o m p o s e d o f a m a s s o f s p o r o p o l l e n i n granules; swellings m a y be less s t r o n g l y d e v e l o p e d in p r o x i m a l p o l a r region, giving sexine a m o r e solid, ' b l o c k y ' a p p e a r a n c e . N e x i n e 0 . 2 - 0 . 4 # m thick,

PLATE IV 1. Cerebropollenitesmaeroverrucosus, specimen 2, showing distal sulcus and, on left-hand side, thin wall adjacent to it; sexlne composed of mostly 'solid' granular bodies rather than hollow sacci, x 10,000. 2, 3, 5. Cerebropollenitesmacroverrucosus, specimen 3. 2. Irregularly granular sexine with only weak development of sacci, x 10,000. 3. Section close to equatorial margin, x 5000. 5. Section through proximal polar region where sexine has a more solid appearance; nexine faintly lamellated, x 20,000. 4, 6. Cerebropollenitesmaeroverrueosus, specimen 4. 4. 'Sacci' comprising irregularly shaped granular masses, x 10,000. 6. Section through comparatively uncompressed specimen; sexine very variable in thickness; 'sacci' mostly composed of granular masses, x 5000. 7, 11. Chasrnatosporites apertus, specimen 1. 7. Entire cross section with distal sulcus; inner sexine alveolate/'crudelycolumellate'; darker inner nexine covers aperture but is mostly pressed against inner surface of nexine of proximal face. x 2500. 11. Sexine is folded back on itself and becomes much thinner adjacent to sulcus, x 10,000. 8, 10. Chasmatosporites apertus, specimen 2. 8. Showing irregularly vacuolate/'crudely columellate' inner sexine and a thin, dark inner nexine, x 5000. 9. Chasmatosporites apertus, specimen 3, showing a dark, loosely structured, perhaps crudely lamellated, inner nexine, x 10,000. 10. Close-up of 8. x 15,000. 12 14. Chasmatosporites hians, specimen l. 12. Cross section of whole specimen with open distal sulcus, x 2000. 13. Inwardly directed protuberances and rods of inner sexine underlain by thin nexine, x 10,000. 14. Sexine becomes much thinner adjacent to sulcus; inner dark nexine extends into aperture, x 15,000.

36 PLATE

D.J. Batten, R.J. Durra/Review ¢~[Palaeobotany and Palynology 99 (1997) 25 54 V

O

8

D.J. Batten, R.J. Dutta / Reriew of Palaeobotany and Palynology 99 (1997)25-54 h o m o g e n e o u s in aspect at low m a g n i f i c a t i o n s but seen to be l a m e l l a t e d at higher power. Distinctions and comparisons: Pollen f r o m several e x t a n t species o f Tsuga have been s h o w n to have a sexine c o m p r i s i n g an outer, c o n v o l u t e d tectum a n d a thin inner, g r a n u l a r zone equivalent to a f o o t layer, a n d a l a m e l l a t e d nexine ( U e n o , 1958; Sivak, 1973, 1978, pl. 3; Van C a m p o a n d Vernier, 1984, fig. 9; K u r m a n n , 1990b, figs. 2 5 - 2 8 , 30-33; K u r m a n n , 1990c, fig. 3b; K u r m a n n , 1992, fig. 1D). In places the t e c t u m a p p e a r s g e m i n a t e a n d discont i n u o u s ( K u r m a n n , 1990b, fig. 31). Elsewhere it m a y have a ' b l o c k y ' aspect ( K u r m a n n , 1990b, figs. 32, 33). It u n d u l a t e s o v e r the f o o t layer ( i n n e r sexine: n o t always clearly discernible o r differentia t e d f r o m nexine) to f o r m a ' s c u l p t u r e ' o f small, h o l l o w sacci (Sivak, 1973, pl. 3, figs. 1, 5; K u r m a n n , 1990b, fig. 32). T h e structure o f the exine o f Cerebropollenites macroverrucosus, a l t h o u g h n o t identical to that o f pollen o f Tsuga, does have a p a r t l y g r a n u l a r sexine a n d a l a m e l l a t e d nexine in c o m m o n . T h e sexine o f C. macroverrucosus f o r m s a single sheet which could be d e s c r i b e d as a c r u d e tectum, a n d this c o m m o n l y u n d u l a t e s over the nexine to f o r m sacci in a similar w a y to the tectum o f Tsuga pollen, b u t it also gives rise to solid, i r r e g u l a r ' v e r r u c a e ' . In a d d i t i o n , unlike the m o d e r n pollen, the fossil

37

grains lack a g r a n u l a r f o o t layer ( i n n e r sexine) a n d the lamellae o f the nexine are m o r e delicate a n d difficult to see except at high magnifications. T h e similarities between C. macroverrucosus a n d Tsuga pollen suggest e v o l u t i o n a r y links between the p a r e n t p l a n t s whereas it m a y be inferred f r o m the differences t h a t the f o r m e r is the p r o d u c t o f an ancestral g r o u p which b e c a m e extinct d u r i n g the C r e t a c e o u s Period. G e n u s Chasmatosporites Nilsson, 1958

Remarks: Chasmatosporites was originally d e s c r i b e d as a spore ( N i l s s o n , 1958), b u t because it has a tectate wall a n d a sulcus r a t h e r t h a n a m o n o l e t e suture the generic diagnosis was subseq u e n t l y e m e n d e d b y P o c o c k a n d J a n s o n i u s (1969) to a c c o m m o d a t e these f u n d a m e n t a l pollen c h a r a c ters. T h e i r r e g u l a r i n w a r d p r o t r u s i o n s a n d rod-like extensions o f the inner p a r t o f the sexine, which these a u t h o r s c o m p a r e d to the i n w a r d l y directed r o d s o f s p o r o p o l l e n i n o b s e r v e d in species o f Classopollis, are clearly visible u n d e r the light m i c r o s c o p e . L a t e r they also c o m p a r e d Chasmatosporites with m o d e r n Araucaria pollen ( J a n s o n i u s a n d Hills, 1976, c a r d 448). G r a i n s recovered f r o m species o f the c y c a d a l e a n cone Androstobus, p a r t i c u l a r l y f r o m Androstrobus

PLATE V 1, 2. Chasmatosporites h&ns, specimen 1. I. Outer nexine (foot layer) adjacent to sulcus becomes fragmentary but darker, very thin, inner part is more obvious; oblique lines are knife marks and not a structural feature, x 20,000. 2. Inner sexine showing inwardly directed rod-like structures; outer nexine of similar, homogeneous composition; inner nexine very thin; as for 1, oblique lines are knife marks, x 20,000. 4. Chasmatosporites hians, specimen 2, section through whole grain, x 1500. 3, 5. Chasmatosporites major, specimen 1. 3. Proximal wall showing inwardly directed protuberances and rods of sexine as for the other species; dark inner nexine barely discernible, x 15,000. 5. Section through wall adjacent to sulcus showing reduction in thickness of both sexine and nexine, x 15,000. 6. Chasmatosporites major, specimen 2, thicknesses of sexine and nexine are reduced adjacent to sulcus, x 15,000. 7, 9, 10. (Tavatipollenites hughesii sensu Schulz, Type [. 7. Entire cross section showing homogeneous outer sexine (tectum) underlain by an irregular columellate alveolate meshwork of sporopollenin and a two-layered nexine. × 5000. 9. Close-up of part of 7; lamellate outer nexine and fragmentary nature of electron dense inner nexine more clearly visible, x 10,000. 10. Detail of 9. × 20,000. 8, 11. Clavatipollenites hughesii sensu Schulz, Type II. 8. Entire cross section showing sulcus, thin outer sexine (tectum), variably spaced columella-like elements and pillars, and a very thin nexine, x 5000. 11. Detail of part of 8" outer nexine is of same electron density as sexine; inner nexine is electron dense and more irregularly developed. × 20,000,

38

D.J. Batten, R.J. Dutta / Review c~[Palaeobotany and Palvnology 99 (1997) 25 54

manis Harris, 1941 (e.g., Van Konijnenburg-van Cittert, 1971, pl. 4, fig. 1) found in the Middle Jurassic succession of Yorkshire, resemble Chasmatosporites and are not unlike modern cycadalean pollen, an observation that also applies to pollen from Androstrobus balmei, another Middle Jurassic cone from Yorkshire described more recently by Hill (1990).

Chasmatosporites apertus Nilsson, 1958 (Plate I, 7; Plate IV, 7 11)

Description of spechnens sectioned: Exine ca. 1.5-2.0 lam thick. Sexine divisible into an outer imperforate tectal layer (0.6-1.0 lam thick) and an inner sexine (0.5-0.8 ~tm) that comprises inwardly directed protrusions and rod-like elements of irregular shape, producing an almost alveolate appearance. Nexine also composed of two layers. Outer part (0.1 0.3 [xm: = f o o t layer) homogeneous, of same electron density as inner sexine. Inner part (0.2-0.4 ~tm) electron dense, but less homogeneous than rest of exine. Sexine becomes thinner towards sulcus, eventually disappearing leaving nexine to cover aperture.

Chasmatosporites hians Nilsson, 1958 (Plate I, 8; Plate IV, 12-14; Plate V, 1, 2, 4) Descrit)tion of specimens sectioned: Exine ca. 1.5 lam thick. Sexine divisible into an imperforate, homogeneous outer layer (ca. 0.9 lam thick) and an inner zone (0.3 0.5 lam) composed of inwardly directed protrusions and rod-like elements 0.3 0.4 pm wide. Nexine thin (0.2 ~tm), homogeneous except for an extremely thin, electron dense layer forming inner surface. Sexine thinner adjacent to sulcus and nexine appears to become discontinuous (fragmentary) but may have originally covered aperture.

Chasmatosporites mq/or Nilsson, 1958 (Plate I, 4; Plate V, 3, 5, 6)

Description

of specimens sectioned: Exine 1.6-2.0 gm thick. Sexine divisible into an outer imperforate, homogeneous layer (ca. 0.9 ~tm thick) and an inner sexine (ca. 0.4 gin) composed of

inwardly directed protrusions and rod-like elements 0.3-0.4 ~tm wide. Nexine thin (0.2-0.3 I~m), homogeneous except for an extremely thin, apparently discontinuous electron dense layer forming inner surface. Both sexine and nexine become thinner adjacent to sulcus where inner sexine disappears: aperture presumably covered originally by nexine. Distinctions and comparisons: The inwardly directed protrusions and rod-like elements that comprise the inner sexine of CTmsmato~porites hians and C. major give the wall a crudely columellate appearance, but those of C. apertus are more irregular in shape, rendering it more alveolate than 'columellate'. The rods in C. hians are the most closely packed of the three species. They also persist to the margin of the sulcus whereas in C. mq/or they disappear as the sexine becomes thinner adjacent to it. The homogeneous outer nexine (foot layer) of C. apertus is comparable to that in C. hians and C. major, but the inner, electron dense nexine is much more pronounced, and may appear slightly lamellated. Its presence is barely indicated in the two other species. This may reflect less good preservation of the specimens sectioned, perhaps further implied by the lack of apertural covering by nexine. The grains that Hill (1990, figs. 9 13) isolated from Androstrobus balmei have a tectate alveolate sexine (i.e., homogeneous outer, and alveolate inner parts) and a homogeneous nexine. Chasmatosporites and Araucariacites may sometimes look superficially similar in gross morphology but there is no basis for comparison between their wall structures. Although Pocock and Jansonius (1969) compared the 'columellate' part of the sexine of Chasmatosporites with that of Classopollis', the two genera have little in common otherwise. The ultrastructure of the exine of Chtssopollis has been shown to be fairly variable according to species but it generally includes a tectum, in most cases with a supratectal sculptural layer, a thick inner sexine composed of columellalike elements, and a nexine that is usually lamellated (Pettitt and Chaloner, 1964: M6dus, 1977; Taylor and Alvin, 1984: Rowley and Srivastava, 1986; Pocock et al., 1990; Osborn and Taylor, 1994).

D.J. Batten, R.J. Dutta / Review of Palaeobotany and Palynology 99 (1997) 25-54

Despite some differences at the levels of both family and genus (Audran and Masure, 1977; Dehgan and Dehgan, 1988) the basic structure of all pollen grains of modern cycadalean species that have been sectioned is tectate-alveolate to tectate alveolate/'columellate' with a lamellated nexine (numerous illustrations in Gullv~g, 1966; Skvarla and Rowley, 1970; Audran, 1971, 1978, 1979, 1980, 1981, 1987; Walker and Skvarla, 1975; Audran and Masure, 1976; Pettitt, 1982; Dehgan and Dehgan, 1988; Xi and Wang, 1989; Kurmann, 1992; Kurmann and Zavada, 1994). Although the sexine of Chasmatosporites hians and C. major is not truly alveolate/columellate, it is not unlike that of modern cycadalean grains; this layer in C. apertus may perhaps be regarded as incipiently alveolate. The inner sexine of both fossil and modern grains is composed of rods of sporopollenin although in Chasmatosporites these are fairly thick and closely packed, and do not appear to anastomose, whereas in cycadalean grains the rods tend to be thinner, less closely packed, and anastomosing to varying degrees according to family and genus. Chasmatosporites also has a partly homogeneous rather than an entierely lamellated nexine, but overall the exine of these fossils suggests an ancestral version of a modern cycad grain (cf. Van Konijnenburg-van Cittert, 1971). The construction of the sexine of Chasmatosporites, especially of C. apertus, also resembles that of pollen of the modern ginkgoalean species Ginkgo biloba Linnaeus, which, in common with cycad grains, is tectate-alveolate with coarse, anastomosing rods of sporopollenin. Unlike Chasmatosporites this is, however, again underlain by a lamellated nexine (Rohr, 1977; Audran and Masure, 1978, pl. 3, figs. 2 5; Audran, 1987, fig. 2a, b; Xi and Wang, 1989, fig. 1D; Kurmann, 1992, fig. 1B). Genus Clavatipollenites Couper, 1958

Remarks: Couper (1958) described the genus Clavatipollenites from Lower Cretaceous Wealden (Barremian or possibly lowermost Aptian) rocks of southern England for monosulcate pollen grains that are broadly boat-shaped to subspherical and tectate-microreticulate. Subsequently, trichotomo-

39

sulcate and even tetrachotomosulcate pollen grains have also been included in the genus (e.g., Doyle and Robbins, 1977, and Walker and Walker, 1986 respectively). Couper considered the type species, Clavatipollenites hughesii, to be angiospermous and compared the structure of its wall with that of the pollen of the modern magnoliid Ascarina lucida J.D. Hooker. This is a member of the Chloranthaceae, one of a group of families that is widely regarded as a 'primitive' living angiosperm. Other authors (e.g., Walker and Walker, 1984; Chapman, 1988) have subsequently discussed the similarities between the fossil pollen and modern representatives of this family. Pre-Cretaceous records of the genus (e.g., in Pocock, 1962, 1978; Schulz, 1967; Tralau, 1968; Lund, 1977; Koppelhus, 1991; Batten and Koppelhus, 1996) are sporadic, and the specimens encountered appear under the light microscope to have a spongy-alveolar, rather than a columellate exine. This difference in structure has led some authors (e.g., Tralau, 1968; Van Konijnenburg-van Cittert, 1971; Doyle et al., 1975) to suggest links with the Cycadales. Unlike the Cretaceous forms (see below), the ultrastructure of these older grains has not hitherto been examined under the TEM. Five specimens of apparently the same morphological form of Clavatipollenites were selected for examination in our study. Despite being picked out of a single palynological residue, sectioning revealed three different ultrastructural types (I-III).

Clavatipollenites hughesii Couper, 1958, sensu Schulz, 1967 Type I (Plate I, 9; Plate V, 7, 9, 10)

Description of specimens sectioned: Exine ca. 1.9 jam thick. Sexine forms most (1.5 ~tm) of this, and is divisible into a thin (0.2 jam), imperforate, homogeneous outer layer (equivalent to tectum) with a smooth surface, and a thicker inner zone (1.3 jam) comprising an irregular, columellate alveolate open meshwork of anastomosing strands of sporopollenin ca. 0.1 jam in diameter. Nexine ca. 0.4 lam thick, also made up of two layers; that adjacent to sexine is ca. 0.35 jam thick and corn-

40

D.J. Batten, R.J. Dutta / Review o[ Palaeobotany and Palynolo~y 99 (1997) 25 54

P L A T E V1

4

~i ~~i ~i i ~!i~i!ii,i~

5~ ~¸¸¸¸¸~ ~

~ii~

D.J. Batten. R.Z Dutta / Review of Palaeobotany and Palynology 99 (1997) 25-54 p o s e d o f thin lamellae (ca. 0.02 0.05 gm); inner layer is a very thin (0.05 gin), r a t h e r f r a g m e n t a r y , electron dense b a n d . T y p e II ( P l a t e V, 8, 11; Plate VI, l )

Description of specimens sectioned'. Exine 1.1-1.3 lain thick. Sexine f o r m s m o s t (ca. 1.0 gm) o f this, a n d is divisible into a thin (0.2 lam), i m p e r f o r a t e , h o m o g e n e o u s o u t e r layer with a s m o o t h surface a n d an inner zone o f columellalike elements a n d pillars ca. 0 . 1 - 0 . 2 g m wide which merge with one a n o t h e r in places to p r o d u c e a p o o r l y d e v e l o p e d alveolate structure. N e x i n e very thin (0.1 tam), c o m p r i s i n g an outer, h o m o g e n e o u s layer 0.05 g m thick o f s a m e electron d e n s i t y as sexine, a n d an inner zone o f similar thickness which is electron dense a n d f r a g m e n t a r y . T y p e I I I (Plate V!, 2)

Description o f specimen sectioned: Exine 1.0 g m thick, c o m p o s e d o n l y o f sexine. O u t e r p a r t thin ( 0 . 1 - 0 . 2 gm), i m p e r f o r a t e , h o m o g e n e o u s ; inner p a r t thicker (0.8 0 . 9 g m ) , consists o f n a r r o w (0.05 0.1 lam) c o l u m e l l a - l i k e elements which sometimes a n a s t o m o s e . Distinctions and comparisons: In Type I the alveo-

4l

late structure is p r o n o u n c e d whereas in types II a n d I I I it is n o t as well developed, the s t r a n d s o f s p o r o p o l l e n i n a n a s t o m o s i n g less often a n d having a m o r e ' c o l u m e l l a t e ' aspect. The nexine o f T y p e I is thin b u t clearly lamellated; in Type II it is n o t only t h i n n e r a n d m o r e delicate b u t also a p p a r e n t l y n o n - l a m e l l a t e . H o w e v e r , b o t h have an inner, very thin, f r a g m e n t a r y , electron dense layer. In a d d i t i o n to l a c k i n g a nexine, the ' c o l u m e l l a t e ' elements in T y p e I l l are generally s o m e w h a t n a r r o w e r t h a n those o f types I a n d II. The tectate c h a r a c t e r o f specimens o f C r e t a c e o u s Clavatipollenites t h a t have been sectioned is f u n d a m e n t a l l y different. R a t h e r t h a n being alveolate, the sexine is clearly t e c t a t e - p e r f o r a t e to semitectate, a n d the nexine is h o m o g e n e o u s ( D o y l e et al., 1975; W a l k e r a n d Walker, 1984, 1986; C h l o n o v a a n d Surova, 1988; Pedersen et al., 1991; A r c h a n g e l s k y a n d Taylor, 1993), a l t h o u g h in some grains it m a y b e c o m e (slightly) l a m i n a t e d u n d e r the sulcus as in Clavatipollenites cf. hughesii sensu D o y l e et al. (1975, p. 454) a n d the Clavatipollenites-type pollen isolated f r o m seeds referred to Couperites mauldinensis Pedersen, Crane, D r i n n a n et Friis, 1991 (p. 584, fig. 6D, E). It is unlike the c o n t i n u o u s l a m i n a t e d structure seen in Jurassic C. hughesii T y p e I a n d thicker t h a n the delicate nexine o f T y p e II. B o t h these

PLATE VI 1. Clavatipollenites hughesii sensu Schulz, Type II, close-up of exine adjacent to sulcus (see Plate V, 8). x 10,000. 2. Clavatipollenites hughesii sensu Schulz, Type III, outer and inner sexine only; columellate elements mostly slightly tapering inwards, x 15,000. 3 5, 8. Eucommiidites troedssonii, specimen 1. 3. Entire cross section, showing distal sulcus and proximal colpi, x 2500. 4. Enlargement of area around distal sulcus; thickness of lamellated nexine adjacent to opening is reduced, x 10,000. 5. Both proximal and distal walls; outer perforated sexine separated from a thick lamellated nexine by a very narrow inner sexinal layer comprising scattered granules, x 20,000. 8. Enlargement of wall in vicinity of proximal furrow, x 10,000. 6, 9. EucommiMites troedssonii, specimen 2. 6. Granular inner sexine more pronounced in this specimen, x 25,000. 9. Outer sexine less perforated than in specimen I. × 20,000. 7, 12. Pilasporites couperi, specimen 1. 7. Proximal and distal walls closely adpressed; show granular sexme and more homogeneous nexine, x 10,000. 12. Similar to 7 but at higher magnification; nexine does not appear to be lamellated. × 15,000. 10. Pilasporites couperi, specimen 2, entire cross section; central 'cap' clearly delineated, x 1500. 1l. Pilasporites couperi, specimen 3, granulate sexine of this specimen is a little more loosely structured; 'cap' is on lower surface towards right-hand side. x 5000. 13. Quadraeculinaanellaeformis, specimen 1, exine between two protosacci; consists of a thin, undulating rectum, an alveolate zone, a layer of more tightly packed, folded sporopollenin threads, and a very thin inner, electron dense layer of less homogeneous composition, x 20,000.

42

D.J. Batten. R.J. Dutta / Review g/Palaeobotanyand Palvnology 99 (1997) 25 54

observations and evidence from macrofossils (Pedersen et al., 1991) provide support for Couper's hypothesis of chloranthaceous affinities. The tectate alveolate structure of the Jurassic C. hughesii is exhibited by pollen of extant Cycadales, Ginkgoales and saccate members of the Coniferales (see Kurmann, 1992). In general the inner sexine of cycadalean pollen is composed of threads of sporopollenin which tend to be spaced fairly uniformly. As noted above under Chasmatosporites, the degree to which they anastomose varies according to family and genus. The alveolate structure so created appears to be most pronounced in Cycas (e.g., Audran and Masure, 1976, p. 18, pl. 6, figs. 1 5; Dehgan and Dehgan, 1988, fig. 9) but neither the amount nor the type of anastomosing is developed in this or any other member of the Cycadales to the extent seen in C. hughesii Type I. There is some resemblance between the more uniformly columellate wall of C. hughesii Type lI and certain cycadalean pollen such as that of Dioon edule Lindley (e.g., Audran and Masure, 1976, pp. 8, 10, pl. 1, figs. 1-8), D. spinulosum Thiselton-Dyer (Dehgan and Dehgan, 1988, p. 1505, fig. 15), Stangeria eriopus (Kuntze) Nash (Dehgan and Dehgan, 1988, p. 1506, fig. 18), S. paradoxa T. Moore (Audran and Masure, 1976, p. 12, pl. 3, figs, 1 4), and Zamiafischeri Miquel (Audran and Masure, 1976, pp. 12, 14, pl. 4, figs. 1-4), the rods of which tend, however, to be narrower and more closely packed. By contrast, the inner sexine of pollen of Ginkgo biloba, which is composed of thick, irregularly spaced 'columellae' (Audran and Masure, 1978, pl. 3, figs. 1 5), has a very coarse alveolate aspect quite unlike either the delicate anastomosing threads seen in C. hughesii Type I or the more organised structure of the narrow 'columellae' of Type II. In modern coniferous grains the outer region of the sacci, just under the tectum, is alveolate (Kurmann, 1992). This type of structure is also typical of fossil saccate pollen (e.g., Millay and Taylor, 1976; Taylor and Taylor, 1987). Although the alveolate structure in C. hughesii Type I bears some resemblance to that in pollen of species of such modern conifers as Pinus (Xi and Wang, 1989, p. 124, fig. 2C; Kurmann, 1992, fig. IC), Abies

(Kurmann, 1989, p. 2498, fig. 42), and Cedrus (Gullvfig, 1966, p. 438, pl. 17, figs. a, b), it is superficial and has no botanical significance because the gross morphology of these grains is fundamentally different. Genus Eucommiidites Erdtman, 1948 ex Potoni6, 1958, emend. Couper, 1958 Remarks: The initial suggestion (Erdtman, 1948) of an angiospermous relationship for Eucommiidites, implied by its name (extant Eucommia is a dicotyledonous angiosperm), was refuted soon afterwards on both gross morphological and exine structural grounds (Kuyl et al., 1955: Couper, 1958). It has since been linked, albeit tentatively or questionably, with a variety of gymnospermous groups including the Bennettitales, Chlamydospermales and Cycadales (Hughes, 1961: Van Konijnenburg-van Cittert, 1971: Doyle et al., 1975). Most recently it has been placed in its own order, Erdtmanithecales, and family, Erdtmanithecaceae (Friis and Pedersen, 1996). Eucommiidites troedssonii Erdtman, 1948 ex Potoni6, 1958 (Plate I, 10; Plate VI, 3 6, 8, 9) Description ~[ specimens sectioned: Exine ca. 0.7 1.3 ~,tm thick, thinnest in vicinity of apertures: composed of three distinct layers. Outer sexine (tectum) 0.3 0.4 lain thick, perforate. Beneath this is a very thin (0.1 I~m) granular inner sexine which is not always clearly discernible; granules ca. 0.1 gm in diameter. The nexine is the thickest layer at 0.5 0.9 gin. It is also laminated, comprising 5 7 layers of sporopollenin, each of which is ca. 0.1-0.2 lain thick. Distinctions and comparisons: The ultrastructure of the wall of our specimens of Eucommiidites troedssonii is similar to that of E. troedssonii from the Lower Jurassic of Grojek (Grojec), Poland (Scheuring, 1978, text-fig. 6) and E. sp. from the Lower Cretaceous (Aptian or lower Albian) Potomac Group in Delaware (Doyle et al., 1975, pl. 2, figs. 1 3), but the inner sexine is thinner. The granules of the latter in Scheuring's material appear to be fairly well spaced out, but in the sections of Doyle et al. they are tightly packed in a well-developed layer 0.2-0.4 lain thick. These

D.J. Batten, R.J. Dutta / Review of Palaeobotany and Palynology 99 (1997) 25 54

authors discussed the similarity between their Eucommiidites sp. and pollen of extant Ephedra and Welwitschia, all of which have a thick tectum with a granular layer beneath and a laminated nexine. They noted that this is consistent with a gnetalean affinity for Eucommiidites, a hypothesis originally put forward by Kuyl et al. (1955, p. 59). A three-layered construction is also displayed in the Eucommiidites-type pollen which Pedersen et al. (1989a) found in situ in the pollen organs Erdtmanitheca texensis Pedersen, Crane et Friis, 1989 from Upper Cretaceous (lower Cenomanian) deposits in Texas, USA, but the tectum comprises between about one half and three-quarters of the total thickness of the wall. It is also imperforate and, although it becomes thinner towards the apertures, the thickness of the lamellated nexine is more or less constant throughout (Pedersen et al., 1989a, p. 285, fig. 3 D - G ; see also Pedersen et al., 1994, figs. 40, 41). Despite some differences from specimens sectioned previously, Pedersen et al. (1989a) thought that these may reflect state of preservation rather than genuine morphological variations. The Eucommiidites grains that Friis and Pedersen (1996) recovered from Eucommiitheca hirsuta Friis et Pedersen, 1996 are smaller, and the lateral colpi are more or less the same length as the main colpus, but the exine appears to be of similar construction (although some of the ultrastructural details are unclear because of poor preservation). Species of Eucommiidites having a wall structure which is clearly different from that orE. troedssonii have, however, been documented by these authors, as well as by Trevisan (1980) and Zavada (1984). The sexine of Zavada's Eucommiidites (labelled E. sp.1) from the Middle Jurassic of Yorkshire is similar in having an inner sexine which comprises granules that tend towards columellae and a granular supratectal layer (Zavada, 1984, p. 451, figs. 2, 3) but, as noted by Pedersen et al. (1989a, p. 286), the lack of lateral colpi in the transmitted light photograph of the whole grain casts doubt upon the identification. One of the two types of Eucommiidites from the Lower Cretaceous 'Poggio Vitalba Zone' of southern Tuscany, Italy, that Trevisan sectioned has an inner sexine composed of large, tightly packed,

43

pillar-like elements (enlarged granules; cf. Doyle in Trevisan, 1980, p. 128) and a granular supratectal layer above a homogeneous tectum (Trevisan, 1980, pp. 100, 102, 104, pl. 9, fig. la-e; pl. 10, fig. l a-d). The sexine of the other type is composed of an innermost thin, homogeneous band adjacent to the lamellated nexine which is overlain by a very thin granular zone, a thick homogeneous layer, and a very thin, dark, homogeneous outer zone distinguishable only on the basis of electron density (Trevisan, 1980, pp. 104, 106, 108, pl. 11, figs. 1, 2a c, 3; pl. 12, fig. la, b; pl. 13, figs. la, b, 2). This type resembles to some extent the Eucommiidites-type pollen isolated from the micropyle of the small seed Erdtmani6permum balticum Pedersen, Crane et Friis, 1989 from the Lower Cretaceous Tornhoj Member of the Jydegfird Formation (upper Berriasian to Valanginian) on Bornholm, Denmark, in having a granular layer sandwiched between two homogeneous parts of the sexine (Pedersen et al., 1989a, p. 290, fig. 6A, B; see also Pedersen et al., 1994, figs. 42, 43). The tectum of the Danish material is, however, perforated, and the granular zone is much more pronounced. On the basis of their analysis Pedersen et al. suggested a relationship with the Bennettitales and Pentoxylales as well as the Gnetales; in other words, with those gymnospermous groups that are thought to be most closely related to the angiosperms. Their recent recovery of the pollen organ Eucommiitheca hirsuta led Friis and Pedersen (1996) to emphasise further an affinity with the anthophytes, and especially with the Gnetales. Hence, there are significant variations in structure of the exine within the genus, but these are confined to the sexine and the ratio of the thickness of sexine to nexine. The nexine makes up half or more of the total exine thickness in E. troedssonii and Eucommiidites sp. of Doyle et al. (1975) whereas the sexine is, or appears to be, thicker than the nexine in the other types discussed. The nexines of all of the grains are lamellated. In view of the inferences drawn above concerning a gnetalean origin for Eucommiidites, comparisons with pollen of extant members of this order, in particular with Ephedra and Welwitschia, are required. The exine of pollen of the species of

44

D.J. Batten, R.J. Durra / Review qf Palaeobota.y and Palynolo&v 99 (1997) 25 54

Ephe&a that have been sectioned (Afzelius, 1956, pl. 1, fig. 5; Ueno, 1960, pl. 2, fig. C; Gullv~g, 1966, pl. 25, fig. a; Van Campo and Lugardon, 1973, pl. 1, figs. 1-5; Hesse, 1984, fig. 2; Zavada, 1984, fig. 7; Kurmann, 1992, fig. 1E; Kurmann and Zavada, 1994, fig. 32) consists of a homogeneous tectum, a granular middle sexine, a very thin, homogeneous inner sexine, and commonly a thick, lamellated nexine. E. troedssonii differs in generally having a perforated tectum and in lacking another layer under the granular middle sexine that is equivalent to the foot layer. Although Trevisan's (1980) sections of Eucommiidites sp. 2 and those of Eucommiidites-type pollen in Pedersen et al. (1989a) do indicate a three layered sexine, the thicknesses of the layers differ from those of the modern pollen. The sexine of the pollen of Welwitschia mirabilis J.D. Hooker, the only representative of the family Welwitschiaceae, is composed of a homogeneous, undulating outer sexine (rectum), a granular middle sexine, and a very thin, homogeneous inner sexine (equivalent to a foot layer): the nexine is laminated ( Ueno, 1960, pl. 2, fig. B; Gullvfig, 1966, pl. 22, figs. a, b; pl. 23, figs. a, b; pl. 24; Hesse, 1984, fig. 4b). Hence, its structure is similar to that of pollen of Ephedra, although Kedves (1987, p. 89, pl. 4, figs. 1-5) recognised a thick foot layer with no endexine beneath. Several types of fossil pollen resemble modern gnetalean grains in general morphology, including Ephedripites and Equisetosporites (which, despite the name, has nothing to do with the Equisetales), and have, therefore, been linked to this group (e.g., Trevisan, 1980; Zavada, 1984; Pocock and Vasanthy, 1988; Osborn et al., 1993). Although differing in gross morphology, their structure bears some resemblance to that of Eucommiidites troedssonii. The rectum is, however, imperforate rather than perforate, and the sexine is thicker than the nexine (Osborn et al., 1993, pl. 1, figs. 5, 6: pl. 2, figs. 1 3, 5, 6: pl. 3, figs. 1 5) rather than vice versa. They are also structurally similar to the Eucommiidites-type pollen associated with Erdtmanitheca texensis, both having a thick, imperforate tectum and a sexine that is thicker and stains lighter than the nexine. Comparisons have, in addition, been made

between fossil pollen of the Bennettitales and Pentoxylales and modern gnetalean grains. Pollen isolated from a silicified bennettitalean cone, C),cadeoidea dacotensis (McBride) Ward, 1894, from the Black Hills of South Dakota, USA, was shown by Taylor (1973, pl. 2, figs. 2, 3; see also Taylor and Taylor, 1987, p. 129) to be composed of two homogeneous sexinal and nexinal layers that can only be distinguished on the basis of electron density, the latter being slightly darker than the sexine. Homogeneity can be a reflection of poor preservation, or related to developmental (ontogenetic) stage. This unusual type of ultrastructure has nothing in common with that observed in E. troedssonii. Subsequent work by Osborn and Taylor clarified and expanded Taylor's initial observations, and does not support a bennettitalean affinity for Eucommiidites. Other wellpreserved, permineralised cycadeoid grains that have a homogeneous but intermittently punctate outer, and granular inner sexine bear a greater resemblance, but they also have a homogeneous, dark-staining nexine. Osborn and Taylor (1995, p. 1079) suggested that Cycadeoidea pollen grains may have a lamellated nexine, but this has yet to be detected (Osborn and Taylor, 1994, figs. 24, 25; Osborn and Taylor, 1995, figs. 6 11, 13 16). The only other cycadeoid grain that has been examined ultrastructurally is from a Middle Triassic bennettitalean microsporophyll Legumhumthus siliquosus ( Leutharat ) Krfiusel et Schaarschmidt, 1966 found in the vicinity of Basel, Switzerland. It also has a homogeneous rectum and a granular infratectum, but the granules are larger and more densely packed than those in CycadeoMea, and they are apparently fused basally to form a foot layer overlying a dark-staining, faintly laminated nexine (Ward et al., 1990, p. 124, pl. 5, figs. 3, 4). Among other suggestions for bennettitalean grains are dispersed monosulcate pollen commonly referred to Cycadopites or Monosulcites (e.g., in Trevisan, 1980), comparable forms having also been found in situ in the micropyles of seeds of the reproductive structure Vardekloe~ltia sulcata Harris, 1932 from Upper Triassic (lower Rhaetian) deposits in East Greenland (Kap Stewart Formation: Pedersen et al., 1989b). However, in

D.,L Batten, R.J. Dutta / Review of Palaeobotany and Palynology 99 (1997) 25 54

common with the other cycadeoid grains discussed, they are not close ultrastructurally to the specimens of Eucommiidites we examined. The sexine of pollen isolated by Osborn et al. (1991) from the pentoxylalean microsporangiate organ Sahnia laxiphora Drinnan et Chambers, 1985 found in Lower Cretaceous (ValanginianAptian) sediments of the Strzelecki Group in Victoria, Australia, is about six times as thick as the nexine. The outer part is homogeneous but it becomes granular in structure adjacent to the nexine (Osborn et al., 1991, pp. 1561, 1563, figs. 6-9; see also Osborn and Taylor, 1994, figs. 9, 12). The granules are large and irregular in shape, unlike those in E. troedsonii which are smaller and of more uniform size. Overall the sexine most closely resembles that of E. sp. 1 of Trevisan (1980). The nexine is more electron dense than the sexine and faintly lamellated. The lamellae are not as 'robust' as those of E. troedssonii. They are most clearly developed adjacent to the sexine.

45

Description

of specimens sectioned: Exine 1.4-1.6/am thick except adjacent to circular-subcircular operculum-like area of wall where both layers become much thinner (ca. 0.3 ~tm). Sexine 1.0-1.2 ~tm thick, composed of granules of sporopollenin ranging in diameter from 0.1 to 0.5/am; larger granules predominate near outer surface. Nexine 0.4-0.6 jam thick, structurally homogeneous. Operculum-like patch consists mostly of sexine up to 2.9/am thick. Distinctions and comparisons: In common with its gross morphology, the granular sexine ofP. couperi suggests derivation from a gymnosperm rather than a pteridophyte. It is similar to that of the Araucariacites specimens we have sectioned, and also to the atectate granular sexines of modern asaccate conifer pollen (Kurmann, 1992), but all of these grains have a lamellated nexine. The lack of lamination could conceivably be a result of homogenisation during the fossilisation process.

Genus PiIasporites Balme et Hennelly, 1956

Genus Quadraeculina Malyavkina, 1949, 1958 ex Potoni6, 1960

Remarks: Pilasporites was first described by Balme

Remarks: Quadraeculina is a distinctive bisaccate

and Hennelly (1956) from Permian deposits in Australia. Their diagnosis of the genus was very broad, and it has since been used subsequently to accommodate spores, algal bodies and pollen grains (as here). Pilasporites couperi was described by Hunt ( 1986, p. 441 ) as a spore from the Purbeck Beds (uppermost Jurassic basal Cretaceous) of southern England. Although a little like the Lower Cretaceous (Wealden) equisetalean spore P. allenii of Batten (1968), it has a more pronounced, irregularly undulating, granulate-verrucate surface and a circular thickened area that is clearly defined and consistently present (Batten and Koppelhus, 1996, pl. 3, fig. 2); it also lacks a perine. Overall its general morphology suggests that it is more likely to be a pollen grain than a spore. Uesuguipollenites callosus, recently described by Dino (1996), differs in having a larger central 'cap' with poorly delineated limits, and usually an equatorial thickening.

(protosaccate: see below) grain which is typically encountered in Upper Triassic and Lower-Middle Jurassic deposits in Northwest Europe. Although obviously gymnospermous, more precise indications of affinity have yet to be established. Species originally attributed to it have been included in the genus Ovalipollis by some authors (e.g., Pocock and Jansonius, 1969, p. 163, pl. 1, fig. 21; Pocock, 1970) but others have argued against this (e.g., Schuurman, 1976, p. 248; Schuurman, 1977, p. 211; Srivastava, 1987, p. 40), pointing out that, unlike Ovalipollis, Quadraeculina has distallyequatorially positioned tenuitates (thin areas of exine: "sexine-free spots in the area of thick sexine" according to Schuurman, 1976, p. 245) and a longitudinal distal sulcus.

Quadraeculina anellaeformis Malyavkina, (Plate I, 12; Plate VI, 13; Plate VII, 1-3)

1949

Description of specimens sectioned: Protosacci up Pilasporites couperi Hunt, Plate VI, 7, 10 12)

1986 (PlateI,

ll;

to ca. 4.0/am thick, divisible into three structural regions which merge with each other: a thin (ca.

46

D.J. Batten, R.J. Dutta ,; Review o f Palaeobotany and Palynology 99 (1997) 25 54

P L A T E VII

2

iiii!!i!!i

PLATE VII 1 3. Quadraeculina anellaejbrmis, specimen 2. 1. Entire cross section, x 2000. 2. Close-up of protosaccate part of specimen showing same structural elements as body of grain (see Plate V, 13) apart from an innermost, very thin, electron dense layer. × 10,000. 3. Part of central area showing mainly folded sporopollenin elements. × 10,000. 4 6. Spheripollenites psilatus, Type I.

D.J. Batten, R.J. Dutta/ Reviewof Palaeobotanyand Palynology99 (1997)25 54 0.1 ~tm), homogeneous rectum which has an uneven (slightly undulating) surface; a zone of sporopollenin threads forming an alveolate layer ca. 1.0 gm thick; an irregular mass of convoluted sporopollenin threads ca. 0.l pm in diameter in centre of protosacci forming a layer 0.7-1.8 lain thick. Exine of ' b o d y ' of grain ca. 2.0 gm thick, divisible into four layers of varying thickness: a rectum (0.1-0.41am), an alveolate layer (0.6-1.0 gin); a zone of folded threads of sporopollenin (ca. 1.0 gin) similar to those in centre of protosacci; and an innermost, very thin (ca. 0.1 gm) layer which is slightly more electron dense than rest of exine, and of less homogeneous structure. Distinctions and comparisons: Both Quadraeculina and Ovalipollis have been regarded as 'protosaccare', meaning that the sacci are "filled with a complex, ramifying system of endosexinous exine elements" (Scheuring, 1974, p. 2). The protosacci (differentially thickened sexine) of Ovalipollis ovalis Krutzsch, 1955 are filled with sporopollenin threads forming an alveolate structure (e.g., Scheuring, 1974, pl. 4, fig. 1). They lack the sinuous threads that characterise the centre of those of Quadraeculina. Comparison with some other protosaccate grains is also merited. These include Platysaccus leschikii Hart, 1960, Protohaploxypinus limpidus (Balme et Hennelly) Balme et Playford, 1967, and Striatopodocarpites phaleratus (Balme et Hennelly) Hart, 1964 from Permian formations in the Bowen and Blair Athol basins, Queensland, Australia. The sexine of P. leschikii is divisible into outer (tectum) and inner layers. The latter is alveolate and entirely fills the sacci. The nexine is laminated and restricted to the body (corpus) of the grain (see Foster, 1979, pl. 27, fig. l c e ) . Both Platysaccus leschikii and Quadraeculina are, there-

47

fore, partly composed of fairly narrow, anastomosing rods of sporopollenin, and have a thin tectum, but Quadraeculina also has an inner exine layer composed of an apparently unordered mass of sporopollenin threads which is found in both the sacci and the body of the grain, and it lacks a lamellated nexine. The sexine of Protohaploxypinus limpidus is alveolate but possibly because of "degradation and homogenisation of the infrastructural elements" (Foster, 1979, p. 90) is much more dense than that in Platysaccus and Quadraeculina. The nexine, like that of Platysaccus, is also more electron dense than the rest of the exine, and appears to be restricted to the body of the grain (Foster, 1979, pl. 31, fig. 4b). The sexine of Striatopodocarpites phaleratus (Foster, 1979, pl. 36, fig. 2b, c) is similar to that of P. limpidus in being alveolate and dense, again perhaps owing to diagenetic alteration. It has a fairly thick, dark, electron dense nexine. Foster (1979) thought that this may originally have been more delicate, as in the sacci of Platysaccus, but that compression and carbonisation caused the structural elements to degrade or become more homogenised. In neither species does the structure of the wall closely resemble that of

Quadraeculina. Grains extracted from the fossil pollen-bearing organs Caytonanthus kochii Harris, 1937 from the lowermost Jurassic (Hettangian) Sagenopteris Shale of East Greenland and C. arberi (Thomas) Harris, 1937 from the Middle Jurassic (Bajocian) Gristhorpe Bed in the Cloughton Formation of Yorkshire, are similar to the dispersed grain Vitreisporites pallidus (Reissinger) Nilsson, 1958. Their sacci are infilled with sporopollenin elements which form a coarse alveolate (spongy) structure. The rectum is fairly thick and homogeneous with a smooth but slightly undulating surface. The

PLATE VI1 (continued) 4. Part of cluster of several specimens; cutting diagonally across photograph are upper and lower walls of a single grain showing a granular supratectal layer, an outer homogeneous sexine, an inner layer of columella-like rods, and a very thin, more electron dense nexine, x 25,000. 5. Oblique section: structure of layers more clearly delineated, x 20,000. 6. Another part of same cluster, x 15,000. 7. Spheripollenitespsilatus, Type II, part of mass of several specimens; nexine much thicker than in Type I and apparently lamellated, x 25,000.

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D.J. Batten, R.J. Durra / Review of Palaeobotany and Palynology 99 (1997) 25-54

nexine, which is slightly less homogeneous than the rest of the exine, is electron dense and crudely laminated (Pedersen and Friis, 1986, p. 257, figs. 5-10). Apart from being, by definition, protosaccate, these grains having nothing in common with Quadraeculina. The alveolate structure is much coarser, the rectum thicker, and the nexine bears little resemblance to the equivalent layer in

Quadraeculina. Protosaccate pollen grains similar in gross morphology to the dispersed pollen genus Alisporites were isolated by Taylor et al. (1987) from the cone Millerostrobus pekinensis Taylor, Delevoryas et Hope, 1987 found in the Upper Triassic Pekin Formation of North Carolina, USA. The sexine is composed of a complex of sinuous sporopollenin threads which vary in thickness and become fewer in number and more robust towards the distal surface of the grains where they have an almost blocky appearance (Taylor et al., 1987, pp. 142, 144, pl. 2, figs. 1-4; pl. 3, fig. 5). The mass of folded sporopollenin threads is similar to that seen in Quadraeculina but there is a greater variation in their thickness, and an alveolate layer is lacking. The nexine appears to be a thin, homogeneous layer. It is possible that some protosaccate grains are in fact eusaccates that have been compressed (see Caytonanthus pollen grains in Osborn and Taylor, 1994, fig. 31). The plane in which thin sections have been taken may also be important because it is sometimes possible for eusaccate pollen to appear protosaccate if a lateral rather than a medial section is examined (see, e.g., Osborn and Taylor, 1994, figs. 33, 34). Nevertheless, some grains including Ovalipollis and Quadraeculina, and probably also the pollen of Millerostrobus pekinensis, do appear to be truly protosaccate. Genus Spheripollenites Couper, 1958

Remarks: Couper (1958) considered Spheripollenites scabratus to be similar to pollen grains recovered from Middle Jurassic male cones associated with the conifer shoot Pagiophyllum connivens Kendall, 1948 in the Yorkshire succession (Kendall, 1948, 1952), although these clearly have the characters of Classopollis. More closely compa-

rable are the grains that Harris (1974) isolated from a pollen sac in the type specimen of the bennettitalean flower Williamsoniella lignieri (Nathorst) Thomas, 1915, also from the Yorkshire Jurassic. Other family relationships were suggested by Couper for S. subgranulatus and S. psilatus, which he likened to pollen of extant Taxus (Taxaceae) and living representatives of the Cupressaceae respectively. The grains of Spheripollenites considered here were identified as S. psilatus. They are from two different localitites, both Early Jurassic (Toarcian) in age (see Section 2). Examination under the TEM revealed two ultrastructural types (I and lI).

Spheripollenites psilatus Couper, 1958 Type I (Plate I, 13; Plate VII, 4-6)

Description of specimens sectioned: Exine ca. 0.6 0.9 [am thick, composed of sexine, nexine, and a supratectal layer. Sexine divisible into an outer homogeneous part (tectum) ca. 0.1 [am thick and an inner layer of columella-like rods of sporopollenin mostly ca. 0.1-0.2 [am wide and 0.2 0.3 I~m high. Nexine very thin (ca. 0.04 [am), electron dense. Supratectal layer ca. 0.2 0.3 [am thick, consists of elongate granular elements ca. 0.05 0.2 lain in maximum diameter, orientated with their long axes perpendicular to uneven outer surface. Type II (Plate VII, 7)

Description of specimens sectioned: Exine 0.6 0.7 }am thick, composed of sexine, nexine and a supratectal layer. Sexine divisible into an outer, homogeneous part (tectum) ca. 0.1 lain thick and an inner layer of columella-like sporopollenin elements ca. 0.2 [am wide and 0.1 0.2 [am high. Nexine 0.2 [am thick, electron dense, apparently lamellated although this is difficult to discern. Supratectal layer ca. 0.2 jam thick, mostly consists of tightly packed granules typically ca. 0.05 [am in diameter, some of which are elongate with their long axes perpendicular to uneven outer surface. Distinctions and comparisons: The main difference between S. psilatus types I and I1 is in the construction of the nexine. In Type I it is a very thin,

D.J. Batten, R.J. Dutta / Review of Palaeobotany and Palynology 99 (1997) 25-54

electron dense layer of sporopollenin whereas in Type II it is much thicker and also appears to be lamellated. Figures of a thin-sectioned specimen of S. scabratus Couper, 1958 in Kedves and Pfirdutz (1973, pl. 6, figs. 3-6; see also Kedves, 1994, pl. 17, figs. 1-5) indicate a tectum covered with fine, densely packed projections, a crude columellate layer and a very thin nexine (foot layer); in other words, a structure essentially identical to that encountered in S. psilatus Type I. The atectate granular sexines and lamellate nexines of araucariaceous, cupressaceous and taxaceous pollen grains (see above) are quite unlike the structure of both types of Spheripollenites psilatus, which in turn differs from that encountered in any other grains, modern or fossil. It is also unknown in algal cysts from which they can be difficult to differentiate when examined in transmitted light.

4. Discussion

Modern gymnosperm pollen grains have sexines that are either granular or alveolate (i.e., having a sponge-like texture). Kurmann (1992) grouped them into three structural types: (1) tectate with an alveolate sexine, as in cycadalean, ginkgoalean and saccate coniferalean pollen; (2) atectate with a granular sexine, characteristic of asaccate coniferalean pollen; (3) tectate with a granular sexine, as in pollen of the Gnetales. Each has a lamellated nexine, a feature that applies also to most fossil gymnospermous grains (e.g., Doyle et al., 1975). All specimens of Araucariacites examined to date have a thick lamellated nexine but there appears to be some variation in the ultrastructure of the sexine. In the specimens of A. australis sectioned here, and in A. australis 'aegypticus' and A. balinkaense, this is composed of irregularly shaped granules of sporopollenin. In other species that have been described the granules are more elongate and may anastomose. The lamellated nexine and atectate, granular sexine of our specimens resemble to varying degrees the structure of the exine of asaccate grains of extant coniferalean species (Kurmann, 1992, 1994) including many members of the

49

Araucariaceae, Cupressaceae, Taxaceae and Taxodiaceae, and some of the Pinaceae and Podocarpaceae. Of these, they are most similar to modern araucariaceous grains (Ueno, 1958, 1959; Van Campo and Lugardon, 1973; Kurmann, 1992). This supports previous suggestions of a close relationship between at least some assemblages of Jurassic A. australis and the ancient coniferous family Araucariaceae. It is likely that all three species of Callialasporites studied were produced by closely related parent plants (cf. Balme, 1995). The similarity of the wall structure to that of the Araucariacites pollen sectioned suggests that these too are related, which is hardly unexpected in view of the fact that single male cones of Brachyphyllum mamillare have yielded grains referable to both genera. Support for an araucariaceous origin for this type of cone (Van Konijnenburg-van Cittert, 1971 ) is borne out by ultrastructural similarities between the exines of Araucariacites, Callialasporites and modern pollen of this family. Although not previously doubted, the presence of a lamellated nexine in Cerebropollenites supports a gymnospermous derivation. The exine structure of C. macroverrucosus suggests an ancestral version of the wall in pollen of Tsuga. The sexine is more granular, but an evolutionary transformation of this sheet of granules to a tectum like that in the modern grains is readily envisaged. Hence, a relationship between the parent plants of Cerebropollenites and extant Tsuga is quite possible. The lamellated nexine which is characteristic of most gymnosperm grains is lacking in Chasmatosporites or, as in C. apertus, only barely suggested in the electron dense inner exine. The elongate elements of the inner sexine of all three species examined are not as well developed as the columellae of many angiospermous grains, but they resemble comparable structures encountered in the exine of some other fossil gymnosperm pollen such as Classopollis and Spheripollenites, which differ, however, in other respects. No natural relationships with these taxa are suggested, nor with araucariaceous pollen. Links with cycadalean and ginkgoalean pollen grains are stronger. Our ultrastructural analysis has confirmed previ-

50

D.J. Batten, R.J. Durra ,' Review (~f Palaeobotany and Palynologv 99 (1997) 25 54

ous suggestions based on light microscopic observations that the Jurassic form of Clavatipollenites hughesii is different from the Cretaceous type (and other) material, which is characterised by having a columellate sexine and a homogeneous rather than a lamellated nexine. Although only C. hughesii Type I has a lamellated nexine, and despite differing thicknesses and anastomosing characters of the sporopollenin threads, the construction of the sexine of Type II suggests that the two forms are derived from related, if not the same species of plant. The lack of a nexine, and perhaps also the presence of very narrow, delicate 'columellae' in Type III, suggest a degraded form of Type II. The structure of the wall of the latter closely resembles that of modern cycadalean grains and lends support to the views of Tralau (1968) and Doyle et al. (1975) that Jurassic Clavatipollenites has cycadalean affinities. Although differing in gross morphology, the basic exine structure of Eucommiidites, including the type with an inner sexine composed of enlarged granules, is similar to that of pollen of both Ephedra and Welwitschia of the Gnetales. Some ultrastructural characters in c o m m o n with Triassic Equisetosporites spp. of presumed ephedralean origin may also add weight to this argument. Zavada and G a b a r a y e v a (1991) considered W. mirabilis to have more in c o m m o n with primitive angiosperms than with other gymnosperm taxa that have been studied. However, whether the similarities suggest that the Gnetales are the ancestors of the angiosperms or merely provide evidence of the development of some angiospermous characters within a gymnospermous group is so far unresolved. The Gnetales have a poor macrofossil record. It is possible that Eucommiidites provides evidence for this group in the Jurassic but it remains equally feasible that it represents another group of Mesozoic plants which became extinct (Hughes, 1961" Doyle et al., 1975). The ultrastructure of Pihtsporites couperi is unlike that of any spore or pollen grain, fossil or recent, which has been examined ultrastructurally. Although the specimens examined lack the lamellar nexine which is characteristic of most pollen of gymnospermous origin, it is likely to be so derived.

It is not possible to be more precise than this at present. The conclusions of Schuurman ( 1976, 1977) and Srivastava (1987) that Quadraeculina should be regarded as a genus separate from Ovalipollis, are corroborated here. Compared to other pollen, the tripartite construction of the sacci and the lack of a distinct central body in Quadraeculina is unusual. Under the tectum the sacci of the other grains discussed are either filled with sporopollenin threads (Millerostrobus pollen) or are alveolate (Phttysaccus, Protohaploxypinus, and Caytonanthus pollen). Protosaccate (and eusaccate) grains are thought to have arisen via the separation of the sexine fi'om the nexine at the sacci but in Quadraeculina nearly all the exine layers that are present in the 'non-saccate' part of the grain are also in the sacci. This observation does not, however, help to resolve the question of the affinity of Quadraeculina, which remains enigmatic. The nexine of Spheripollenites psih~tus Type 1 is thin and electron dense whereas in Type lI it is thicker and appears to be lamellated. Otherwise these grains are structurally similar. Couper's (1958) suggestion of a link between Spheripollenites and members of the Araucariaceae, Cupressaceae and Taxaceae is not supported. Its affinities do not seem to lie with any modern gymnosperm family. On the other hand the suggestion of Kedves and Pfirdutz ( 1973, p. 311 ) that S. scabratus is "probably one of the representatives of the ancient Angi[o]spermatophyte type" remains unproven. Although Type 1 lacks a laminated nexine, the columella-like elements of the inner sexine are unlike those in angiospermous grains.

5. Conclusion

T E M examination of the pollen grains considered in this paper has revealed some structures that are not usually thought of as typically gymnospermous, such as homogeneous nexines and 'crudely columellate' sexines. A lamellated nexine is often regarded as characteristic of gymnosperm pollen, yet non-lamellar nexines were observed in C77asmatosporites, Clavatipollenites Type I l,

D..L Batten, R.J. Dutta / Review of Palaeobotany and Palynology 99 (1997) 25 54 Pilasporites couperi a n d Spheripollenites Type I. The possibility that the lack of lamellae is a result of h o m o g e n i s a t i o n d u r i n g fossilisation c a n n o t , however, be dismissed. Less likely, in o u r o p i n i o n , is that the specimens sectioned were n o t fully developed (i.e., they were ontogenetically i m m a ture). The sexines o f Chasmatosporites hians, C. major a n d Spheripollenites types I a n d II include elongate c o m p o n e n t s that are m o r e like columellae t h a n similar exinal rods that have been k n o w n for m a n y years in Classopollis a n d a few specimens of Eucommiidites. A l t h o u g h they c a n n o t be described as true columellae in the a n g i o s p e r m o u s sense, they are far r e m o v e d from granules. I n a n g i o s p e r m pollen, columellae have been associated with the storage of substances involved in dispersal a n d stigma i n t e r a c t i o n ( H e s l o p - H a r r i s o n , 1976; Hesse, 1981; a n d others). It is, however, more likely that the irregular sexinal rods in the g y m n o s p e r m o u s grains described h a d a n o t h e r , perhaps h a r m o m e g athic, function. T h a t these pollen c a n n o t be closely linked to the p r o d u c t s of m o d e r n g y m n o s p e r m s implies d e r i v a t i o n f r o m ancestral groups which are n o w extinct.

Acknowledgements R J D t h a n k s the N a t u r a l E n v i r o n m e n t Research C o u n c i l for the s u p p o r t of a research studentship. DJB is grateful for a g r a n t from the Research F u n d of the U n i v e r s i t y of Wales, A b e r y s t w y t h , to enable this w o r k to be completed. The D a n i s h samples were p r o v i d e d by D r E.B. K o p p e l h u s . Prof. E.M. Friis a n d a n a n o n y m o u s referee m a d e some helpful c o m m e n t s o n the m a n u s c r i p t .

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