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(American Journal of Botany. 1998;85:1289-1300.)
© 1998 Botanical Society of America, Inc.

Reconstruction of the Jurassic conifer Sewardiodendron laxum (Taxodiaceae)1

Xuanli Yao5,a, Zhiyan Zhoub and Bole Zhangc

a Department of Biology, University of San Francisco, San Francisco, California 94117; b Nanjing Institute of Geology&Palaeontology, Academia Sinica, Nanjing, Jiangsu 210008, China; and c Qingdao Research Institute of Geotechnical Prospecting and Surveying, Qingdao, Shandong 266030, China


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 SYSTEMATICS
 DESCRIPTION
 DISCUSSION
 REFERENCES
 
Compressed seed cones and pollen cones of Sewardiodendron laxum are described from the Middle Jurassic of Yima, Henan, central China. They are either organically attached to or associated with leafy shoots. Seed cones are terminally borne. Each cone is ovate to elongated, up to 6.5 cm long and 3.5 cm wide, and consists of a stout axis and numerous helically arranged bract–scale complexes. The bract protrudes beyond and is partially fused with the reduced ovuliferous scale. The ovuliferous scale bears approximately six inverted, small, and flattened seeds. Pollen cones are borne in terminal clusters. Microsporophylls are helically arranged, each bearing three abaxial, basally fused pollen sacs. Pollen is assaccate, rounded, and with an inconspicuous pore. Morphological, structural, and cuticular features of seed cones, pollen cones, and leafy shoots of S. laxum are compared with those of fossil and extant conifers. S. laxum is included in Taxodiaceae and believed to have its closest affinities with a Mesozoic conifer Elatides and a group of Cunninghamia-like conifers. It is reconstructed as a half-evergreen tree that lived in a humid, warm-temperate climate.

Key Words: Cunninghamia • Elatides • Jurassic • pollen cone • seed cone • Sewardiodendron • S. laxum • Taxodiaceae


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 SYSTEMATICS
 DESCRIPTION
 DISCUSSION
 REFERENCES
 
The fossil record of conifers suggests that the family Taxodiaceae originated during the Triassic and was well established by the Jurassic (Lemoigne, 1967; Miller, 1982; Yao, Taylor, and Taylor, 1997). In contrast with impoverished Triassic records, Jurassic conifers with Taxodiaceous affinity have been widely reported from both the Northern and Southern Hemispheres. These Jurassic members include the permineralized seed cones Pararaucaria Wieland (Stockey, 1977) and Romeroites Spegazzini (1924) from Argentina, some woods referred to Prototaxodioxylon Vogellehner, Taxodioxylon Hartig, Protocupressinoxylon Eckhold and Cupressinoxylon Goeppert from Laurasia (Zhou and Zhang, 1989b; Philippe, 1994), and compressed/impressed reproductive and/or vegetative remains found in the Northern Hemisphere such as Elatides Heer, Cunninghamites Presl, Farndalea Bose, Sciadopitytes Goeppert and Menge, Sequoia Endl., Sewardiodendron Florin, and a form genus Elatocladus Halle with a possible taxodiaceous affinity (Florin, 1922, 1958; Harris, 1943, 1979; Endo, 1951; Bose, 1961; Jongmans and Dijkstra, 1972). Most of these Jurassic members referred to Taxodiaceae are based on fragmentary remains. Among them, only Elatides [E. williamsonii (Lindley&Hutton) Nathorst] has a complete record of leafy shoots, seed cones, and pollen cones (Harris, 1943, 1979).

Sewardiodendron, a monospecific genus, was established by Florin (1958) based only on vegetative parts of leafy shoots from the Middle Jurassic of Yorkshire, England. Since then no reproductive organs of this plant have been found. Because of this Harris (1979) was disposed to reject this generic name and include most of Florin's specimens in the form genus Elatocladus.

Recently a large number of compressed coniferous seed cones and pollen cones have been discovered from the Middle Jurassic (Yima Formation) of Yima, Henan, central China. These cones are either associated with or directly attached to coniferous leafy shoots identified as Sewardiodendron laxum (Phillips) Florin. Associated with S. laxum, other plants occur in the same bed including leaves and ovule-bearing organs of ginkgoaleans Ginkgo yimaensis Zhou et Zhang, Yimaia recurva Zhou et Zhang, and Baiera hallei Zhou and Zhang, leaves of Sphenobaiera with possible ginkgoalean affinity, a gymnosperm wood Protocupressinoxylon, fronds of the fern Cladophlebis, and some other plant remains (Zhou and Zhang, 1988, 1989a, b, 1992).

The occurrence of S. laxum in the Middle Jurassic of Yima has only been briefly reported (Yao, Zhou, and Zhang, 1989). In this paper we describe the seed cones and pollen cones of S. laxum together with its vegetative shoots, based on the abundant Chinese material.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
SYSTEMATICS
 DESCRIPTION
 DISCUSSION
 REFERENCES
 
More than 200 specimens containing leafy shoots, seed cones, and pollen cones of S. laxum were collected from the Yima Formation in Northern Open-cast Mine of Yima District, west Henan Province. The formation is considered Middle Jurassic based on palynostratigraphic and floral analysis (Zhang, 1965; Kang et al., 1984). It is up to 120 m thick, and composed of sandstone, mudstone, siltstone, and coal sediments. Abundant fossil plants occur in the siltstone between the lower and middle coal seams of the formation. The bed yielding S. laxum and associated plants is located right under the middle coal seam (Number 2) (Zhou and Zhang, 1989a).

Selected coalified leaves, bract–scale complexes, and microsporophylls of S. laxum were cleaned with hydrofluoric acid, followed by maceration with Schulze's solution. Transfer and bulk maceration were applied to several specimens. Samples were mounted on standard slides and scanning electron microscope (SEM) stubs for observation under light and scanning electron microscopy. Several pollen sacs with in situ pollen were prepared for transmission electron microscope (TEM) examination according to a procedure of Osborn, Taylor, and de Lima (1993). The stained ultrathin sections were observed and photographed under a Zeiss transmission electron microscope.


   SYSTEMATICS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 SYSTEMATICS
DESCRIPTION
 DISCUSSION
 REFERENCES
 
Order
Coniferales

Family
Taxodiaceae

Genus
Sewardiodendron Florin 1958

Emended diagnosis
Main shoot robust and straight, lateral shoot flattened, ultimate branchlet alternate or subopposite; leaves helically arranged on main shoot, but opposite and whorled on lateral shoot; leaf sessile, flattened; vein single; trichomes absent; cuticle thin; hypostomatic stomata in two bands; stoma monocyclic or incompletely dicyclic; guard cells slightly sunken; subsidiary cells in a ring of 4–7; seed cone terminal, ovate to elongated; bract–scale complexes helically arranged; bract prominent and partly fused with reduced ovuliferous scale; approximately six inverted ovules per scale, each small and flattened; pollen cones terminal at a cluster of 7–8; microsporophylls helically arranged, each bearing three pollen sacs abaxially; pollen grain rounded; exine two-parted; sexine thin and delicate; nexine thick and lamellated; pore rounded.

Type species
Sewardiodendron laxum (Phillips) Florin

Species
Sewardiodendron laxum (Phillips) Florin 1958

1875 Taxites laxus, Phillips, p. 231, Pl. 7, fig. 24.

1880 ? Taxites brevifolius, Nathorst, p. 73, Nomen nudum.

1958 Sewardiodendron laxum, Florin, p. 303, Pl. 25, figs. 1–8; Pl. 26, figs. 1–15; Pl. 27, figs. 1–8 (not p. 332, Pl. 45, figs. 1–4).

1979 Elatocladus laxus, Harris, p. 121–125, figs. 55–56. comb. nov.

1984 Elatides williamsonii, Wang, p. 286, Pl. 141, figs. 6–8; Pl. 174, figs. 1–3.

? 1987 Elatides asiatica, Qian et al., p. 85, Pl. 22, fig. 2; Pl. 23, fig. 4; Pl. 26, fig. 2.

Diagnosis (emended)
Main shoot axis up to 9 mm thick, leaves attached at ~90°; lateral shoot axis up to 4 mm thick, bud scale occurring at base (but not of ultimate branchlet), leaves attached at 40°–90°; on lateral shoot leaves displaying in same plane by twisting at base except at shoot apex; leaves sessile, commonly 10–22 mm long x 1.3–2.5 mm wide, longer at middle and shorter near base and apex of branchlet; blade lanceolate, base broad and decurrent, margin entire, vein single and prominent; cuticle delicate, adaxial one ~1 µm thick and abaxial one ~0.5 µm thick; two stomatal bands of abaxial cuticle one to each side of vein, each composed of 2–5 files of densely arranged stomata; stomata oriented variously but often transversely or obliquely; stoma round to elliptical, 56–100 µm in diameter; guard cells slightly sunken and thinly cutinized, aperture well marked; subsidiary cells 4–7 (often 5–6) in a monocyclic or incomplete dicyclic ring; seed cone up to 6.5 cm long and 3.5 cm wide; axis up to 3.5 mm in diameter; bract up to 1.5 cm long, consisting of a basal stalk and an expanded head with an acute apex; ovuliferous scale reduced and fused with bract except for the distal margin; distal margin lobed and denticulate, each associated with a seed; seed ovate, flattened, wingless, 2.2–6.5 mm long and 1.6–3.5 mm wide; micropyle short and pointed; integument cuticles thin and delicate, mostly composed of elongated cells; nucellar cells rectangular to polygonal; megaspore membrane granular at surface; mature pollen cone elongated, up to 22.5 mm long and 6.5 mm wide; microsporophyll constructed of a basal stalk and a distal lamina; pollen sac elongated, up to 1.6 mm long and ~0.3 mm wide, dehiscence longitudinal; enormous numbers of pollen grains produced in each pollen sac; pollen grain 37.5–56.0 µm in diameter; pore ~7.5 µm; surface sculpture scabrate; sexine ~0.04 µm thick; nexine 0.14–0.16 µm thick and composed of up to eight laminae, each uniform in thickness.

Locality
Northern Open-cast Mine of Yima, Yima District, west Henan Province, central China.

Stratigraphy
Lower Yima Formation. Underlying the middle coal seam (No. 2) (Zhou and Zhang, 1989a).

Age
Middle Jurassic.

Deposition of specimens
All the specimens including slides and stubs are deposited in Nanjing Institute of Geology and Palaeontology, Academia Sinica, Nanjing, China. Figured specimens are within acquisition number PB12814–14815 and PB17557–17605.


   DESCRIPTION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 SYSTEMATICS
 DESCRIPTION
DISCUSSION
 REFERENCES
 
Vegetative shoots
The main shoot axis is 6–9 mm thick, bearing helically arranged leaves that diverge from the axis at ~90° (Figs. 10, 11). The lateral shoot axis is 2–3 mm thick, bearing alternately or suboppositely arranged branchlets (Figs. 1, 40a). Leaves are opposite and whorled on the lateral shoot, and the successional pair often forms a right angle with the former pair (Fig. 12A, B). Although the leaves are helically arranged, they spread as two lateral ranks in one plane by twisting at the base (Figs. 1, 12A). The angle between the blade and the axis ranges from 40° to 90°, but is mostly 40°–70° (Fig. 1). Each leaf is sessile, dorsiventrally flattened, and lanceolate, measuring 10.0–22.0 mm long by 1.3–2.5 mm wide, longer at the middle part and shorter near the base and the apex of the shoot (Figs. 1, 40a, b). The leaf apex is acute and the base is decurrent (Figs. 1, 12A). The margin is entire. A single, prominent vein vascularizes the leaf (Fig. 6). The cuticle of the leaf is thin and delicate. The adaxial cuticle is ~1 µm thick, and the abaxial one is 0.5 µm thick. The epidermal cells of the adaxial and the nonstomatal area of the abaxial cuticles are elongated along the long axis of the leaf, measuring 37.5–62.5 µm long by 12.5–20.0 µm wide. The surface wall of the cell is smooth, and the anticlinal wall is straight. The two stomatal bands of the abaxial cuticle (Fig. 7), one at each side of the vein but closer to the margin, run along the long axis of the leaf and extend almost to the apex. Each band is 237.5–263.5 µm wide and composed of 2–5 files of densely arranged stomata (Fig. 14). The orientation of stomata varies, but is often transverse or oblique (Fig. 14). The stoma is round to elliptical, and 56–100 µm in diameter. It has a shallow pit with a fusiform opening (18.6–37.5 µm long x 15.0–27.5 µm wide) (Fig. 17). The guard cells are slightly sunken (Fig. 17). They are thinly cutinized, and their inner surface walls appear granulate under high magnification (Fig. 15). The stomatal aperture is prominent, 33.3–53.3 µm long, and often parallel to the long axis of the stoma (Figs. 15, 16). The subsidiary cells are 4–7 (often 5–6) in number, and usually one of them is polar (Fig. 15). They surround the guard cells in a monocyclic or incomplete dicyclic ring (Figs. 15, 16). Their surface walls are smooth. The radial walls and the anticlinal walls proximal to guard cells are thinly cutinized. The distal anticlinal walls, however, are strongly cutinized, forming a distinct, inward-extending collar-like structure around the stoma (Fig. 15).



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  		Figs. 1–11. Sewardiodendron laxum . 1. A flattened lateral shoot showing arrangement of ultimate branchlets, and morphology and arrangement of leaves. PB17,598. Scale bar = 1 cm. 2. Two clusters of pollen cones at young stage vertically compressed. PB14,815a. Scale bar = 5 mm. 3. A laterally compressed leafy shoot with a cluster of pollen cones terminally borne. PB14,815b. Scale bar = 5 mm. 4. Mature pollen cones (arrows) terminally borne on a leafy shoot. PB17,595. Scale bar = 5 mm. 5. Two seed cones terminally borne on a leafy shoot. PB17,597. Scale bar = 1 cm. 6. Part of a leaf showing a single vein (arrow head). PB17605. Scale bar = 1 mm. 7. Part of a leaf showing two stomatal bands (arrows). PB17,605. Scale bar = 1 mm. 8. A leafy shoot with three seed cones attached (arrows). PB14,814. Scale bar = 1 cm. 9. A shoot with five attached seed cones (arrows). PB17,603. Scale bar = 1 cm. 10. A main shoot with imprints of leaf bases showing helical arrangement. PB17,594. Scale bar = 1 cm. 11. A main shoot with leaves. PB19,601. Scale bar = 1 cm.

 


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  		Fig. 40. Reconstruction of Sewardiodendron laxum . (a) Leafy shoots with seed cones and pollen cones. (b) A leaf. (c) A bract–scale complex at abaxial view. (d) A microsporophyll. (e) A pollen grain.

 


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  		Fig. 12. Sewardiodendron laxum . (A) Part of an ultimate branchlet with successive leaf pairs numbered from apex to base. PB17,593. Scale bar = 4 mm. (B) Diagram corresponding to Fig. 12A showing double helical arrangement of leaves and approximate planes of successive leaf pairs.

 


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  		Figs. 14–27. Sewardiodendron laxum . 14. Inner surface of abaxial cuticle of a leaf showing transversely oriented stomata in a stomatal band (long axis of leaf vertical). PB17,592. Scale bar = 0.5 mm. 15. A stoma showing two guard cells and a ring of subsidiary cells. Note strongly cutinized anticlinal walls (arrow) of subsidiary cells distal to guard cells . PB17,605. Scale bar = 10 µm. 16. Two stomata showing oblique orientation (long axis of leaf horizontal). PB17,600. Scale bar = 20 µm. 17. Outer surface of abaxial cuticle of a leaf showing slightly sunken guard cells (G) and fusiform opening of stomatal pit. PB17,592. Scale bar = 10 µm. 18. An ovule showing its ovoid shape and pointed micropyle (m). PB17,600a. Scale bar = 0.1 mm. 19. Apical part of an ovule showing a pollen grain (p) in micropyle (m). PB17,600b. Scale bar = 0.1 mm. 20. Detail of micropyle and pollen grain (arrow) from the same ovule shown in Fig. 19 . Scale bar = 20 µm. 21. Megaspore membrane showing granular surface. Higher magnification of specimen shown in Fig. 25 . Scale bar = 5 µm. 22. Adaxial view of a bract–scale complex showing part of a bract (B), one ovuliferous scale lobe (os), and a triangular scar (within bracket) left by a detached seed. PB17,600d. Scale bar = 30 µm. 23. Detail of micropyle end of seed shown in Fig. 18 , showing micropyle (m) and integument cells (arrow). Scale bar = 20 µm. 24. Chalazal end of a seed showing hilum (h) PB17,600. Scale bar = 30 µm. 25. Part of a seed showing nucellus (N) and megaspore membrane (M). PB17,600e. Scale bar = 20 µm. 26. Part of a bract–scale complex showing bract (B) and denticulate distal margin of ovuliferous scale (arrow). PB17,604. Scale bar = 0.1 mm. 27. A seed cone showing helical arrangement of bract–scale complexes, and vascular traces in them (those in bract–scale complexes a, b, and c illustrated in Fig. 28 ). PB17,599. Scale bar = 1 cm.

 
Seed cone and ovule
Seed cones are singly and terminally borne on the ultimate branchlet (Figs. 5, 8, 9, 40a). Each cone is ovate to elongated (Fig. 9), up to 6.5 cm long and 3.5 cm wide. Bract–scale complexes are helically borne on a stout axis up to 3.5 mm in diameter. The bract is up to 1.5 cm long, consisting of a basal stalk and an expanded, flattened head with an acute apex. The ovuliferous scale is reduced and fused with the bract except for the distal margin (Figs. 22, 26, 40c). The distal margin is lobed and denticulate, and each lobe is associated with an inverted seed (Figs. 22, 26, 40c). The seed scar on the ovuliferous scale is obtriangular and measures 270 µm wide and 140 µm high (Fig. 22). Since the bract–scale complexes were easy to break into fragments when dissected, no ovuliferous scale with a full number of attached seeds has been obtained successfully. On the largest fragment obtained from an ovuliferous scale, three attached seeds were observed. However, from the abaxial side of an intact bract–scale complex, six rounded, raised areas were observed in the position where seeds are borne (Fig. 13), which suggests the possible number of seeds per scale. Each seed is small (2.2–6.5 mm long and 1.6–3.5 mm wide), flattened, wingless, ovate to elongatedly ovate, and has a pointed micropyle and a rounded chalazal end (Fig. 18). The hilum is small and elliptical (~80 µm by 60 µm). After maceration with Schulze's solution, the seed layers observed (from outside to inside) include cuticles of the integument, nucellus, and megaspore membrane. The outer cuticle of the integument is thin and composed of longitudinally elongated cells (Fig. 23). The remnants of stone cells of near isodiametric shape sometimes can be observed between the outer and inner cuticles. The inner cuticle of the integument is very thin and delicate. Cells near the micropyle are elongated. Those at slightly lower position are near isodiametric, and have distinct anticlinal walls. Those at the middle and lower part of the ovule are elongated and have thin, inconspicuous anticlinal walls, and this part of the cuticle is often appressed tightly to the nucellus. The nucellar cuticle near the micropyle is often folded and the cell outline is difficult to identify (Fig. 19). At other regions the nucellar cells are rectangular to polygonal, often near hexagonal (Fig. 25). The surface wall of nucellus is finely granulated and the anticlinal wall is weakly cutinized. The megaspore membrane is granular at the surface (Figs. 21, 25). Pollen grains have been observed in the micropyle and the pollen chamber of several ovules (Figs. 19, 20). These pollen grains are morphologically identical to those in situ grains preserved in the pollen sacs of pollen cones.



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  		Fig. 13. Sewardiodendron laxum . Abaxial view of a bract–scale complex showing the imprint of six rounded raised areas (S) probably related to the placentae on which seeds were borne. B = bract; O = ovuliferous scale; V = vascular trace. PB17,600. Scale bar = 0.5 mm.

 
The vascular trace of the bract–scale complex is observed in several compression/impressions (Figs. 27, 28). At the base of the complex it appears as a thick bundle. At the upper portion the bundle divides into three parts. The middle one seems rarely divided, and the two lateral ones each further divides dichotomously one to several times to give rise to fine traces. Bifurcate tips are observed at the end of some of these fine traces.



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  		Fig. 28. Sewardiodendron laxum . Pattern of vascular traces observed in bract–scale complexes a, b, and c of seed cone shown in Fig. 27 .

 
Pollen cone and pollen
Clusters of 7–8 pollen cones are terminally borne on the ultimate branchlets (Figs. 2–4, 40a). Young cones are found attached to leafy shoots (Figs. 2, 3). They are rounded to elliptical, 4 mm or longer, and 3–4 mm wide. Elongated cones of mature or near mature stages are mostly preserved as detached organs (Fig. 29). Only one specimen was found with elongated cones attached to a leafy shoot (Fig. 4). The mature pollen cone is up to 22.5 mm long and 3.0–6.5 mm wide and has numerous microsporophylls helically borne on a slender axis (0.6–1.2 mm thick) (Figs. 30, 31). The microsporophyll is constructed of a basal stalk and an expanded head (Figs. 30, 40d). The stalk is near penparticular to the axis, ~0.7–1.5 mm long and 0.1 mm thick. The upper part of the microsporophyll expands into a rhomboidal distal lamina. It measures 1.4 mm in width and 1.5 mm in height and contains an oval-shaped resin body near the center. In immature cones the microsporophyll head extends upward, each tightly overlapping the one above (Figs. 2, 3). In mature cones, however, the microsporophyll head expands nearly horizontally, leaving a space between microsporophylls and forming a loose cone (Fig. 30). Near the base of the microsporophyll head, three basally fused pollen sacs (Figs. 33, 40d) are borne abaxially. The pollen sac is elongated, measuring 0.8–1.6 mm long and ~0.3 mm wide. The sac consists of rectangular cells in longitudinal arrangement. The surface wall is rough, and the anticlinal wall varies in thickness and sometimes is slightly wavy. The pollen sac is longitudinally dehiscent (Fig. 32). In each pollen sac enormous numbers of pollen grains are produced (Fig. 36). Pollen grains are rounded (Figs. 37, 38, 40e), 37.5–56.0 µm in diameter, but those ~47 µm in diameter are more common. The surface sculpture appears scabrate (Figs. 37–39). The pore is rounded, ~7.5 µm in diameter (Fig. 38), and around it no distinctive elevated area is observed. The exine is divided into sexine and nexine based on their difference in stain affinities (Fig. 34). The sexine stains lightly and measures 0.04 µm thick. The dark-staining nexine is 0.14–0.16 µm thick and lamellated. Up to eight nexine lamellae have been observed, and each is uniform in thickness. Orbicules and a delicate tapetal membrane are observed around some pollen grains (Fig. 35).



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  		Figs. 29–39. Sewardiodendron laxum . 29. Detached pollen cones associated with a leafy shoot. PB17,586. Scale bar = 1 cm. 30. Two pollen cones (arrows) showing cone axis (A) and microsporophylls (m) including a basal stalk and an expanded head. PB17,587. Scale bar = 5 mm. 31. Two pollen cones showing the helically arranged microsporophylls. PB17,586. Scale bar = 5 mm. 32. A pollen sac showing longitudinal dehiscence. PB17,596a. Scale bar = 0.1 mm. 33. Three basally fused pollen sacs from a microsporophyll. PB17,596b. Scale bar = 0.1 mm. 34. Section through a pollen grain showing thin sexine (s) and lamellated nexine. PB,17,602a. Scale bar = 0.2 µm. 35. A section through a pollen sac showing three pollen grains (arrows) and orbicules (o) with tapetal membranes (t) around them. PB17,602b. Scale bar = 2.5 µm. 36. Three pollen sacs (within brackets) full of pollen grains. Arrow indicates the base. PB17,596. Scale bar = 0.1 mm. 37. Two pollen grains showing the rounded shape and scabrate surface. PB17,596a. Scale bar = 10 µm. 38. Two pollen grains showing sexine (s), nexine (n), and a pore (arrow head). PB17,596b. Scale bar = 10 µm. 39. Part of a pollen grain in Fig. 37 (right) under higher magnification showing scabrate surface. PB17,596c. Scale bar = 2.5 µm.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 SYSTEMATICS
 DESCRIPTION
 DISCUSSION
REFERENCES
 
Sewardiodendron laxum was initially described as Taxites laxus by Phillips in 1875, based on a vegetative shoot from the Middle Deltaic, Gristhorpe, Yorkshire. In 1958, Florin reexamined the type specimen and also studied several more leafy shoots from the Lower-Middle Deltaic of various localities in Yorkshire. He provided the first detailed description of this species and discussed the classification of this plant. He also indicated that the branchlet organization, leaf morphology, and cuticle characteristics of this plant resemble those of Sequoia Endl. and Cunninghamia R. Br. in L.C. Rich. of Taxodiaceae rather than those of Taxus L. (Taxaceae). Therefore, Florin removed Phillip's species from the genus Taxites, and established the genus Sewardiodendron to include it. In 1979, Harris slightly emended the diagnosis of this species and provided the first detailed description of phyllotaxy of this plant.

Up to date S. laxum is still the only species described of the genus and has been only reported from the middle Jurassic of Yorkshire and Yima [those from middle Jurassic of Oxfordshire, central southern England (Florin, 1958) are not included in S. laxum (Harris, 1979)]. Seed cones and pollen cones recently found from Yima represent the first reproductive organs of this genus and species. They occur in a large number and various sizes, either associated with or organically attached to coniferous leafy shoots. All these leafy shoots demonstrate morphological and cuticular characteristics that confirm the diagnosis of S. laxum based on the Yorkshire specimens (Harris, 1979). The differences between the Yima and the Yorkshire specimens are slight: only a few Yorkshire specimens have longer or shorter leaves, a greater range (up to 262.5 µm) in width of the stomatal band, and stronger cutinization in subsidiary cells. These differences are considered trivial and not sufficient to warrant a segregation of species.

We agree with Harris (1979) that the specimens from the Middle Jurassic of Oxfordshire (Florin, 1958, p.332, Pl. 45, figs. 1–4) with gradually narrowed leaf base are different from S. laxum. Several Yorkshire specimens with shorter leaves were removed from S. laxum and included in Taxites as a distinct species (T. brevifolius) by Nathorst (1880). However, Florin (1958) disagrees with Nathorst and considers that it is not reliable to distinguish species only based on the leaf length. Harris (1979) supports Florin's interpretation as he found that both the long and short leaf types occur in close association in the Lower Deltaic of Hasty Bank and Hill Hause Nab.

Florin (1958) indicates that two species (Pagiophyllum steenstrupi Bartholin and Taxites? subzamioides Möller) from the Jurassic of Bornholm, Denmark, are similar to S. laxum. He suggests that these two species might belong to the same one and proposes to rename them as Sewardiodendron steenstrupii as a new combination, pending a closer examination of these materials. However, no further study of these Denmark specimens has been made. Therefore, this combination proposed by Florin seems not to be well supported.

Among fossil taxodiaceous conifers, Sewardiodendron appears closely related to Elatides Heer, which is abundant in sediments from the Middle Jurassic to the Lower Cretaceous of Laurasia. S. laxum is particularly similar to E. williamsonii in size, morphology, and structure of seed and pollen cones, and also in number of seeds per scale and number of pollen sacs per microsporophyll. The two genera, however, can be distinguished based on their branching pattern, phyllotaxy, and leaf morphology and anatomy: Elatides has distichously or irregularly branched lateral shoots, helically disposed and displayed leaves, and falcate leaves appearing rhomboidal in transverse section, having adaxial stomata in some species and an inconspicuous vein.

From northern and northeastern China, coniferous shoots comparable with S. laxum are those described as Elatides asiatica (Yokoyama) Krassilov from the Middle Jurassic of Wusugou, Shenmukaokao, Shaanxi province (Qian et al., 1987) and E. williamsonii from Xiahuayuan, Hebei Province (Wang, 1984). Both of them resemble the Yima specimens in external morphology. The cuticular features of the Shaanxi specimens are unknown, and the Hebei specimens are identical to the Yima specimens in the arrangement and structure of stomata. The Hebei specimens were referred to E. williamsonii because the author considered the stomata identical to those of Yorkshire E. williamsonii. However, a closer examination reveals that the Hebei specimens have the Sewardiodendron type leaf rather than the Elatides type, and their stomatal arrangement and structure are also similar to those of S. laxum. It is possible that these specimens from Hebei, Shaanxi, and Yima represent the same species because of their general similarities, and also their common occurrence in the Middle Jurassic of North China Block.

From northeastern China several other specimens referred to E. asiatica are also similar to S. laxum in external morphology, but distinct in cuticular characteristics, such as the arrangement and/or structure of stomata or other epidermal features. These specimens include those from the Middle Jurassic of Fengcheng and Huoshiling, Liaoning [= E. manchuricus (Yokoyama)Yabe, see Krassilov, 1967] (Yokoyama, 1906; Ôishi, 1933; Yabe and Ôishi, 1933), and from the Upper Jurassic and the Lower Cretaceous of eastern Heilongjiang (Zheng and Zhang, 1982; Zhang and Xiong, 1983). In the Lower Cretaceous of eastern Heilongjiang, some seed cones occur in association with E. asiatica leaves, but no organic attachments have been observed between them (Zheng and Zhang, 1982). Among these cones, only the specimen in Pl. 24, fig. 8 is superficially similar to that of S. laxum. According to the description, each ovuliferous scale probably bears two winged seeds. S. laxum, however, bears approximately six wingless seeds per scale.

Other specimens reported from the Jurassic and Cretaceous of China that superficially resemble S. laxum but lack cuticular information include: Elatides asiatica (= E. manchuricus) (Yabe, 1922; Yabe and Ôishi, 1933; Sze, 1933 a, b; Chen, Yang, and Zhou, 1981; Wang et al., 1982; Liu and Shen, 1982; Zheng and Zhang, 1983; Cao, 1983, 1984; Chen, Dou, and Huang, 1984), E. cf. asiatica (= E. cf. manchuricus) (Huang and Zhou, 1980; Zhang, Chang, and Zheng, 1980; Duan, Chen, and Niu, 1986), E. submanchurica (Yabe and Ôishi, 1933; Tan and Zhu, 1982; Zhang, 1986; Shang, 1987), E. cf. submanchurica (Cao, 1984), E. smittiana (Heer) Seward (Zheng and Zhang, 1983), and E. sp. (Sze and Li, 1963; Huang and Zhou, 1980; Zhang, Chang, and Zheng, 1980; Tan and Zhu, 1982; Cao, 1984; Zhou, 1984).

The affinity of S. laxum has been considered taxodiaceous based only on its vegetative characteristics. Florin (1958) indicates that Sewardiodendron shares characteristics with Sequoia in the lateral branch system and resembles Cunninghamia in leaf shape. In addition, the distribution of stomata of Sewardiodendron is also similar to some extant taxodiaceous members. It resembles Cunninghamia in its monocyclic or dicyclic stomata and shares features with Sequoia in some other epidermal details. Harris (1979) supports Florin's interpretation and indicates that every character of Sewardiodendron can be found in one genus or another in Taxodiaceae. The recent discovery of seed cones and pollen cones of S. laxum provides pivotal evidence supporting the taxodiaceous affinity of the genus. Its seed cone consists of helically arranged and partially fused bract–scale complexes, and each bears numerous, small, and flattened seeds. Its pollen cone has helically arranged microsporophylls, and produces assaccate, rounded pollen with a pore. All these features are characteristics of Taxodiaceae, which suggest that Sewardiodendron is undoubtedly a member of Taxodiaceae based on its reproductive characteristics.

Among the extant genera of Taxodiaceae, Sewardiodendron is believed to have its closest affinity with Cunninghamia. In addition to the common taxodiaceous characteristics, they also share the following features: bract large, ovuliferous scale reduced and small, with only the distal margin free from bract; seed inverted; three basally fused pollen sacs per microsporophyll; no distinctive elevated area around the pore of pollen; leaf sessile, flattened, lanceolate, base decurrent and twisted to display the leaf in a single plane, vein single and prominent. The vascularization of the bract–scale complex in Sewardiodendron also appears similar to that of Cunninghamia, if its middle trace represents the bract trace and the others the scale traces. However, since the information about the vascularization of Sewardiodendron is only based on compression/impressions, it is not known for certain which trace supplies the bract and which supplies the scale and ovules. Different from Sewardiodendron, Cunninghamia has smaller and rounder seed cones, smaller number of bract–scale complexes per cone, and smaller number of seeds (3) per scale. These features may represent a more advanced status as a result of reduction. Cunninghamiostrobus Stopes and Fujii, a Cunninghamia-like conifer, has been described from the Early Cretaceous to the Early Oligocene (see Miller, 1990). Although Cunninghamiostrobus shares more features with Cunninghamia in seed cones, it has a few leaf epidermal features which resemble those of Sewardiodendron and differ from those of Cunninghamia. These features include often transversely or obliquely oriented stomata, and lacking the sinuous walls in epidermal cells (Miller, 1990). Overall, the similarities between Sewardiodendron, Cunninghamia, and Cunninghamiostrobus are remarkable. These similarities suggest that Sewardiodendron is probably ancestral to extant Cunninghamia and a group of extinct Cunninghamia-like conifers.

The well-preserved seed and pollen cones of the Yima S. laxum provide ideal material for understanding the reproductive biology of this plant. Morphological, structural and cuticular similarities between attached and detached cones suggest that these cones of various sizes represent different developmental stages of the same plant. This conclusion is also supported by the similarities in bract–scale complex stomata of detached seed cones and S. laxum leaves and that the coniferous leafy shoots preserved in the same bed are exclusively S. laxum.

In cuticles of the microsporophyll no stomata have been observed, which indicates a short life period of the pollen cone. Pollen cones are terminally borne in a cluster. They are small, not showy, and lacking secretory cells or structures. Each pollen sac produces rounded pollen with weak surface sculpture in vast quantities. All these characteristics are common for anemophilous species. Therefore, this extinct conifer is believed wind pollinated, as are extant conifers. Furthermore, the micropyle of the ovule is thin and pointed, lacking any special structure for pollen to land on or to be trapped in, which implies that this plant probably produced pollen drops for capturing the pollen. In addition, in several ovules examined, pollen grains have been found in both the micropyle and the pollen chamber. These grains are identical to those in situ grains in size and morphology and are believed to be the pollen of the same plant that was preserved during pollination. The identical diameter of the pollen and the micropyle also suggests that pollen drops, which assist in drawing down the pollen through the thin micropyle, might be involved in pollination.

The seeds of S. laxum are probably dispersed also by wind. The high, terminal position of the seed cones provides a distance advantage for wind dispersal of seeds. The seeds, small, flattened and produced in large numbers in each cone, also suggest wind dispersal.

Although no direct evidence has been found to demonstrate that this plant is a tree instead of a shrub, it seems reasonable to make this assumption since its leaf and branch morphology and reproductive biology are similar to that of Cunninghamia. Harris (1979) suggests that the shoots of S. laxum might be deciduous based on its thin and delicate leaf cuticles and that the position of its bud scales similar to that of deciduous Taxodium rather than evergreen Sequoia. Among the abundant specimens collected from Yima, leaves have been found attached to both lateral and main branches, but no detached leaves have ever been observed. This type of preservation implies that this plant was probably evergreen, or half evergreen (the deciduous lateral shoots shed with intact leaves, but the leaves on the main branches do not shed annually). Based on the leaf preservation in Yima and Florin's study on bud scales and leaf cuticles, it seems more plausible that S. laxum is a half-evergreen tree.

Similar to the lack of detached leaves, no detached seed bract–scale complexes and pollen cone microsporophylls have been found among the abundant materials collected. Those mature seed cones and pollen cones with pollen and seed shed still have intact bract–scale complexes and microsporophylls. Therefore, both the bract–scale complex and the microsporophyll of S. laxum are probably persistent.

The climate in which S. laxum lived is believed warm, humid, and seasonal. This is partially based on the leaf morphology of S. laxum, including the thin blade, thin cuticle, and slightly sunken stomata with most of the guard cell exposed. Additional evidence suggesting this climate are the associated plants, including several ginkgoaleans, ferns, a wood with distinctive annual rings, and also some fungi and trace of fungal activities marked on the plants. These plants and S. laxum are not considered to have been transported for long distances, based on their near perfect preservation, such as the intact shoots with attached seed cones and pollen cones, and the delicate attachment of pollen sacs on the microsporophyll in S. laxum, and numerous axes with intact ovules in several ginkgoaleans. In addition, the associated wood fossils are permineralized with authigenic siderites, which usually require still water and a weakly reduced environment (Zhou and Zhang, 1989b).

Sewardiodendron laxum represents one of a few Mesozoic conifers with a complete record of vegetative shoots, seed cones, and pollen cones. The discovery of its reproductive organs from Yima resumes the taxonomic position of Sewardiodendron as a natural genus. The occurrence of S. laxum in the Middle Jurassic of both England and China implies that this conifer probably flourished on the Eurasian Continent during the Middle Jurassic or earlier. Based on current records of Sewardiodendron, it is difficult to determine exactly when and where it originated and how it migrated. However, as a Jurassic conifer that is possibly ancestral to extant Cunninghamia and closely related to the Jurassic-Cretaceous Elatides of Eurasia, S. laxum probably played an important role in the evolution and distribution of both Mesozoic and modern conifers of Taxodiaceae.


   FOOTNOTES
 
1 The authors thank Mr. Renbao Zhang and Mrs. Shaohua Sang for providing some specimens used in this research and for their help during our field trips; and Dr. Patricia J. Schulz for her advice and support in TEM technology. This research was supported in part by grant number 49610710383 from NNSF (National Natural Science Foundation) of China and a Fellowship from the Ministry of Personnel of China to X. Yao, and grant number 449372080 from NNSF of China to Z. Zhou. Back

5 Author for correspondence. Back


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 SYSTEMATICS
 DESCRIPTION
 DISCUSSION
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