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Paleobotany |
2Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, P.R. China; 3Paléobotanique et FRE 2158 Centre National de la Recherche Scientifique (CNRS), Université Claude-Bernard Lyon 1, Bâtiment Darwin-A, 7 rue Dubois, F-69622 Villeurbanne Cedex, France; 4Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611-7800 USA; 5Institute of Geosciences, University of Tübingen, Sigwartstrasse10, D-72076 Tübingen, Germany
Received for publication November 4, 2003. Accepted for publication December 17, 2004.
ABSTRACT
Sphenobaiera huangii (Sze) Hsü is typical Early Mesozoic fossil foliage of Ginkgoales in China. It has been recorded from the Upper Triassic to the Lower Jurassic. The cuticular anatomy is investigated based on material from the type locality, Lower Jurassic Hsiangchi Formation, Zigui County, Hubei Province. The specimens are similar to S. huangii, but contain new information about leaf morphology and cuticular anatomy. Lower and upper cuticle is investigated using light and electron microscopy (LM, SEM, and TEM). Many features are described for the first time, including general structures of lower and upper cuticle, stomata, papillae, and cuticular ultrastructure. At the ultrastructural level, two layers have been distinguished in both lower and upper cuticle, including a homogeneous outer layer with granules and a heterogeneous inner layer with fibrils. Based on a literature comparison between S. huangii and other relevant species of Sphenobaiera, S. huangii may represent the best-known taxon in the genus Sphenobaiera in both leaf morphology and cuticular structures. This study provides the first detailed ultrastructural data on the leaf cuticle of Sphenobaiera, one of the oldest foliage taxa of Ginkgoales, and offers further evidence for potential discussion on the taxonomic relationships of S. huangii with other ginkgoalean taxa.
Key Words: China • fossil • Ginkgoales • Jurassic • leaf cuticle • Sphenobaiera huangii • ultrastructure
The origin and evolution of the "living fossil" Ginkgo have received increased attention and interest from botanists and palaeobotanists. In particular, the discovery and investigation on the reproductive organs (pollen and ovules) of fossil Ginkgoales have provided valuable evidence for understanding its long evolutionary history (Zhou and Zhang, 1988
, 1989
, 1992
; Schweitzer and Kirchner, 1995
; Poort et al., 1996
; Zhou et al., 2002
; Zhou and Zheng, 2003
; Zheng and Zhou, 2004
). However, a number of fossil specimens assigned to Ginkgoales are preserved as compression and/or impression foliage. Therefore, the cuticular structure and anatomy undoubtedly play a significant role for exploring the systematics of foliage taxa of Ginkgoales.
Sphenobaiera is one of the oldest fossil foliage types of Ginkgoales and has a global distribution, mainly in the Northern Hemisphere. It can be traced from the Lower Permian well into the Cretaceous (Taylor and Taylor, 1993
). Florin (1936)
established this genus for leaves originally included in Baiera Braun that are distinguished from those of the type species Baiera muensteriana (Presl in Sternberg) Heer, mainly by having wedge-shaped leaves that lack a distinct petiole. Later, Harris and Millington (1974)
made an important refinement, transferring the wedge-shaped leaves borne in a bundle of dwarf shoots, to the Czekanowskiales (Sphenarion Harris and Miller, 1974
). Since then, Sphenobaiera is generally defined for wedge-shaped leaves that are distinguishable from Ginkgo, Ginkgoites, and Baiera by the absence of a distinct petiole (see also Lydon et al., 2003
). So far, over 50 species have been described worldwide for Sphenobaiera, and for some of them cuticle details are known. However, only a few specimens have been reported as closely associated with the reproductive organs. For example, several Sphenobaiera-type leaves were reported associated with the ovule-organ Karkenia from the Lower Cretaceous of Argentina, the Upper Jurassic of Siberia, the Liassic of Germany, Rhaetic to Jurassic of Iran and Afghanistan, and the Jurassic of Henan, China (Archangelsky, 1965
; Krassilov, 1972
; Schweitzer and Kirchner, 1995
; Zhou et al., 2002
). According to a recent systematic review by Zhou (1997
, 2003)
, it is quite possible for some species of Sphenobaiera, which are characterized by having less divided wedge-shaped leaves and broad segments, to be referred to the family Karkeniaceae of Ginkgoales. The systematic status of most other species of this form-genus is still unknown at the family level.
About 25 species of Sphenobaiera have been described from Mesozoic deposits in China. Among them, Sphenobaiera huangii (Sze) Hsü is the most typical and widespread leaf found in these deposits. It was initially described as Baiera huangii by Sze (1949)
, based on impression specimens from the Lower Jurassic Hsiangchi flora in western Hubei. Subsequently, Hsü (in Sze and Hsü, 1954
) transferred it to the genus Sphenobaiera. Since then, this species has been described from a number of Mesozoic localities in China. Available data show that specimens of S. huangii are also recorded from the Upper Triassic to Middle Jurassic in Jinmen, Hubei (Feng et al., 1977
; Chen, 1984
), western and eastern parts of Sichuan (Yang, 1978
; Duan and Chen, 1982
; Chen et al., 1987
), Fengxian and Yan'an of Shaanxi (Liu, 1982
; Zhang et al., 1998
); Jiangning of Jiangsu (Wang et al., 1982
), Yima of Henan (Zeng et al., 1995
), Beipiao of western Liaoning (Mi et al., 1996
), Datong of Shanxi (Li and Hu, 1984
), and eastern Hunan (Zhang, 1986
) in China. However, most specimens referred to as S. huangii are poorly preserved so yield little information about cuticular anatomy and foliar morphology.
Recently, numerous compressed specimens of Sphenobaiera huangii were collected from the Lower Jurassic Hsiangchi Formation in western Hubei, China. Other plants associated with S. huangii in this formation include nilssonialeans (Nilsonnia), bennettitaleans (Pterophyllum, Ptilophyllum, Tyrmia, Otozamites, Anomozamites, Weltrichia, Zamites, and Ctenis), ferns (Todites, Marattia, Phlebopteris, Dictyophyllum, Clathropteris, Hausmannia, Coniopteris, and Cladophlebis), other ginkgoaleans (Ginkgoites, Baiera), Czekanowskialeans (Czekanowskia, Phenicopsis, Ixostrobus, and Stenorachis), conifers (Podozamites, Ferganiella, Swedenborgia, and Elatocladus), and a pteridosperm (Ctenozamites) (see Wang, 1999
, 2002
). Some of the ferns have been investigated describing fertile organs, in situ spores, and ultrastructure (Wang, 1999
, 2002
; Wang and Mei, 1999
; Wang et al., 2001
). In this paper, we reinvestigate typical ginkgoalean foliage S. huangii, with emphasis on cuticular anatomy, by using scanning and transmission electron microscopy (SEM, TEM), and light microscopic (LM) observations. This study presents the first information of cuticle ultrastructure for the genus Sphenobaiera based on well-preserved Chinese material.
MATERIALS AND METHODS
More than 70 specimens of Sphenobaiera huangii containing cuticle have been collected since 1998 from the type locality in Xiangxi Town of Zigui County, Hubei Province (30°50'20'' N, 110°40'15'' E), where the Jurassic is well exposed. It consists of an extensive succession of red clastic sediments of Middle to Upper Jurassic and a coal-bearing sequence of Lower Jurassic, which is known as the Hsiangchi Formation. This formation is generally regarded as Early Jurassic based on various palaeontological evidence, such as plant megafossils, spores, pollen, bivalves, and megaspores (Li and Shang, 1980
; Wu et al., 1980
; Meng, 1987
; Meng and Zhang, 1987
; Yang and Sun, 1987
; Zhang and Zhang, 1987
). The Hsiangchi Formation is up to 205 m thick and composed of grey to greyish black sandstones, siltstones, mudstones, and carbonaceous shales, intercalated by thin coal seams. This formation unconformably overlies the Upper Triassic Shazhenxi Formation and is conformably overlain by the Xietan Formation of Middle Jurassic age (for detailed information on the stratigraphy, refer to Wang, 1999
, 2002
). All specimens are well preserved as compressions with evident venation and cuticle. In addition, three original specimens from the same locality figured by Sze (1949)
as Baiera huangii were reexamined. They are in the palaeobotanical collection of the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (NIGPAS), Nanjing, with catalog numbers PB 931, PB 933, and PB 934.
Selected cuticles were cleaned with hydrofluoric acid and hydrochloric acid, followed by a maceration in Schulze's solution and a short treatment with 5% ammonia. The lower and upper cuticle were separated and then divided into three fractions for different microscopic observations. A part of the cuticle was mounted on permanent slides for observation and photography under LM. For SEM, the samples were prepared on standard stubs and viewed using a JSM 6300 scanning electron microscope (JEOL, Tokyo, Japan) at an acceleration voltage of 15kV.
For TEM, samples were prepared as for fossil cuticle described in Zhou and Guignard (1998)
and Guignard et al. (1998
, 2001)
. The cuticle was pre-stained with osmium tetroxide before embedding in epoxy resin (epon) and stained with uranyl acetate and lead citrate after cutting with a Reichert Ultracut S ultramicrotome (Reichert-Leica, Vienna, Austria). Transverse and longitudinal sections were cut in the lower and upper cuticle. Twelve resin blocks, belonging to four specimens, and more than 90 grids were made for observation under a Philips CM120 transmission electron microscope (Philips, Eidhoven, Netherlands). The maceration and SEM observations were undertaken in NIGPAS, Nanjing, China, while TEM work was done at the Electron Microscope Center of Biology and Geology (CMEABG) of University Claude Bernard Lyon 1, Villeurbanne, France. All specimens examined in this study (including slides and SEM stubs) are deposited in the palaeobotanical collection of NIGPAS, Nanjing, China with registration numbers PB 931 to PB934 and PB20041 to PB20075. The TEM blocks and sections are retained in the Guignard collection of the University of Lyon 1, France.
RESULTS
Leaf morphology
More than 70 specimens of Sphenobaiera huangii have been investigated in our collection. The material referred to as S. huangii exhibits a wide range in leaf size, varying from 7.5 to 25 cm long (Figs. 1–4). The leaf is narrowly wedge-shaped, becoming gradually narrower toward the base, but without a distinct petiole. In some well-preserved specimens, a swollen base is attached (Figs. 1, 3). The leaves are divided into two nearly equal lobes. The basal undivided portion is 3–12 cm long or about half the leaf length. The width of the leaf base is 2–5 mm (average 4 mm). The two lobes form a basal acute angle that varies from 10° to 25°. The lobes vary from 6.5 to 12 cm long and 8 to 21 mm wide (average 14 mm wide). The apices of the lobes are blunt or rounded (Figs. 1–4). The venation is parallel in the lobes and converges slightly towards the apex (Figs. 2–4). The number of veins are 12–20 per lobe (average 15–16 per lobe), 10–11 veins/cm. Fusiform resin bodies occur on the leaf cuticle and are 200–250 x 700–850 µm in size (Fig. 5).
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Cuticular ultrastructure
The lower and upper cuticle were observed under TEM, both in transverse (Figs. 18–29) and longitudinal sections (Figs. 30–34). These cuticular constructions are generally similar and are composed of two layers: outer layer A and inner layer B (Figs. 18, 30). Layer A is homogeneous and composed of granules about 5 nm in diameter (Figs. 19, 20, 23, 27, 32). Layer B is heterogeneous and composed mainly of fibrils, variable in density and thickness (5–10 nm) (Figs. 21, 24, 25, 29, 33), as well as a mixture of granules that are similar in diameter as observed in layer A. Fibrils are usually short and wavy (Figs. 21, 25, 29, 33), though sometimes they are straight and longer (Fig. 24). The thickness of layers A and B is variable depending on the position of the cuticle. In ordinary epidermal cells, cuticle layer A (about 5 µm thick, 76% of the total cuticle thickness) is thicker than layer B (about 1.5 µm thick, 24% of the total cuticle thickness) (Fig. 18) in transverse sections. No lamellae or polylamellae have been found in the outermost part of the present material.
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In general, the two-layered ultrastructure is consistent among different parts of lower and upper cuticle, both in transverse and longitudinal sections. Minor differences lie in varying thickness of the two layers in different cuticular parts (i.e., layer A is thicker in ordinary epidermal cells and anticlinal cell walls, whereas it becomes thinner in subsidiary cells near stomata pits and also in papillae cuticle cells). To summarize all anatomical characters and ultrastructural patterns, a three-dimensional reconstruction of S. huangii cuticle is proposed in Fig. 35.
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Wu et al. (1980)
first described S. huangii cuticle based on two fragmentary specimens from the same locality in Hubei. Some cuticular features of their specimens are generally similar to those described in the present paper according to the light microscopic illustrations. However, in Wu et al.'s specimens, the papillae are absent in the cuticle; they are well developed in our material. In addition, Huang and Zhou (1980)
described several fragmentary specimens as S. huangii from the Lower Jurassic Fuxian Formation in Fugu County of Shaanxi Province, northern China. According to their LM micrographs, the cuticle of S. huangii from Shaanxi has some similarities to our material from Hubei. However, many features such as papillae, resin bodies, and the stomatal density are not recorded in the material from Shaanxi. Detailed comparison is difficult due to poor preservation of specimens from not only Shaanxi, but also other localities in China, even though a few cuticle fragments were based on LM observations (Zeng et al., 1995
; Mi et al., 1996
). In some of the literature, such as Zhang (1986)
and Zhang et al. (1998)
, S. huangii was only cited, descriptions and photographs were lacking.
Sphenobaiera huangii is comparable to several other species with bilobed leaves or less divided leaves and broader lobes or segments, both in leaf morphology and cuticular structure, e.g., S. biloba Prynada (Prynada, 1938
; Samylina, 1967
; Chen et al., 1988
; Deng, 1995
; Deng et al., 1997
), S. jugata Zhou (Zhou, 1989
), S. ikorfatensis (Seward) Florin (Lydon et al., 2003
; Sun et al., 2003
), and S. pulchella (Heer) Florin (Heer, 1876
, 1878
; Samylina, 1963
). Their main differences and similarities in terms of leaf morphology and cuticular structure are summarized in Table 1. It is evident that S. huangii from the Lower Jurassic of Hubei, China, may represent the best-known species so far of the genus Sphenobaiera.
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; Villar de Seoane, 1997a
; Zhou and Guignard, 1998
; Guignard and Zhou, in press
). At the ultrastructural level, S. huangii has two distinct layers—an outer granular layer (A) and an inner fibrillar layer (B)—in ordinary epidermal cells, stomata complex (subsidiary and guard cells), anticlinal walls, and in papillate cell cuticle, both in transverse and longitudinal sections. No polylamellate layer was found in the cuticle.
Compared with epidermal cells, the stomatal complex cuticle of S. huangii has a thicker layer B; that is, the cuticle in both guard cells and subsidiary cells is more fibrillous. This minor structural difference between stomatal complex cells and ordinary epidermal cells was also recorded in other taxa, e.g., Hirmeriella muensterii (Schenk) Jung, belonging to Cheirolepidiaceae of the conifers (Guignard et al., 1998
). This cuticular anatomy of the stomatal complex is known, in extant plants, to be directly related to the exchange of water and other molecules (Larcher, 1995
). In S. huangii, the guard cell cuticle is thinner than subsidiary cell cuticle. From a structure–function view, considering that guard cells are responsible for the opening and closing of stomata, a thinner cuticle is certainly more efficient than a thicker one.
To date, the leaf cuticular ultrastructure of Ginkgoales has been reported only for a few fossil and living taxa in the families Karkeniaceae and Ginkgoaceae, including Ginkgoites tigrensis Archangelsky, Ginkgo yimaensis Zhou and Zhang and Ginkgo biloba L. Ginkgoites tigrensis from the Lower Cretaceous of Argentina is a representative member of the Karkeniaceae. Available data demonstrate that the cuticular ultrastructure of S. huangii shows a closer affinity with that of G. tigrensis. According to a recent study by Villar de Seoane (1997a)
, the cuticular ultrastructure of G. tigrensis from Argentina closely resembles that of S. huangii from China. The outer part of the G. tigrensis cuticle is compact and homogeneous, comparable to the outer granular layer of S. huangii. The inner part of the cuticle is slightly reticulate and is structurally similar to the heterogeneous inner layer with fibrils of S. huangii. The polylamellate layer in G. tigrensis is absent (Villar de Seoane, 1997a
). So far, the leaf cuticular ultrastructure is known for only one fossil taxon belonging to Ginkgoaceae of Ginkgoales. According to Guignard and Zhou (in press)
, the leaf cuticle of Ginkgo yimaensis, the oldest Ginkgo from the Jurassic of China, is obviously distinguished from S. huangii in ultrastructural level by having a distinct outer polylamellate layer. The leaf cuticle of living Ginkgo is also different from that of S. huangii. Taylor et al. (1989)
and Guignard and Zhou (in press)
demonstrated that the cuticle of G. biloba is characterized by an outer polylamellate layer and inner granular and fibrillar layers, differing from S. huangii of China at the ultrastructural level.
The studies on the fossil leaf cuticular ultrastructure using transmission electron microscopy started with the pioneer work of Archangelsky et al. (1986)
. Since then, the leaf cuticular ultrastructure is known for a number of fossil taxa or groups, including pteridosperms (Taylor et al., 1989
; Baldoni and Barale, 1996
; Labe and Barale, 1996
; Maheshwari and Bajpai, 1996
; Bajpai, 1997
; Guignard et al., 2001
), bennettitaleans (Barale and Baldoni, 1993
; Villar de Seoane, 2001
), cycadaleans (Artabe and Archangelsky, 1992
; Villar de Seoane, 1997b
), ginkgoaleans (Taylor et al., 1989
; Villar de Seoane, 1997a
; Guignard and Zhou, in press
), czekanowskialeans (Zhou and Guignard, 1998
), as well as conifers (Archangelsky and Taylor, 1986
; Archangelsky et al., 1986
; Del Fueyo et al., 1990
; Barale et al., 1992
; Guignard et al., 1998
; Villar de Seoane, 1998
; Zhou et al., 2000
). Most of the cuticle is marked by an outer polylamellate zone, similar to type 1 of Holloway's (1982)
cuticle classification (six types based on the leaf ultrastructure of living plants). It is noteworthy that Holloway (1982)
is very careful to point out the lamellate structure of the cuticle proper; where it occurs in the cuticular layers, it is difficult to illustrate. Some results may depend upon the staining technique, which can alter the appearance of the cuticle. In this study, S. huangii cuticle is stained using a method similar to that used for G. yimaensis and G. biloba (Guignard and Zhou, in press
), with osmium tetroxide and a post-stain with uranyl acetate and lead citrate. It is evident that the outer polylamellate layers are reported in G. yimaensis and G. biloba (Ginkgoaceae), but were not found in S. huangii, though similar staining was used in both cases.
The cuticle of S. huangii from the Lower Jurassic of Hubei, China, has some affinities with both Holloway's type 3 and type 6. In type 3, the cuticle is partly reticulate without the granular layer in S. huangii. Type 6 has many different layers, but they are very different from S. huangii. It is known that a cuticle with an outer homogeneous layer as described in S. huangii is very distinct and rarely reported in living and fossil records. A more or less similar structure was reported in two fossil cycadalean leaves from the Lower Cretaceous of Argentina (Villar de Seoane, 1997b
) and in Phoenicopsis and Arctobaiera leaves of the Czekanowskiales from the Jurassic of Henan, central China (Zhou and Guignard, 1998
), but the cuticle of these taxa are otherwise very different in general structure. No known fossil ginkgoalean member bears a cuticle similar in ultrastructure to S. huangii; only G. tigrensis (Karkeniaceae) has a close affinity with S. huangii at the ultrastructural level.
Previous and recent studies show that some species of Sphenobaiera are associated with the ovule Karkenia, belonging to the family Karkeniaceae (Archangelsky, 1965
; Krassilov, 1972
; Schweitzer and Kirchner, 1995
; Zhou et al., 2002
), whereas other species of Sphenobaiera are associated with Ginkgo-type ovules. However, in most species of Sphenobaiera, their ovule-bearing organs are still unknown. Obviously, the genus Sphenobaiera is difficult to place into any known family within the Ginkgoales, based upon either leaf morphology and/or general cuticular features. According to this investigation, the ultrastructural data of S. huangii cuticle may imply a potential affinity to the family Karkeniaceae of Ginkgoales. We have provided useful information for exploring the relationship of the leaf cuticle construction among different taxa and about the extent of variation in a given taxon and for assessing the significance of cuticular structure in plant taxonomy. Further work is obviously needed in order to provide more reliable data on reproductive organs associated with S. huangii and to confirm its systematic status.
In summary, this investigation of S. huangii from the Early Jurassic in Hubei, China, provides new insights into the cuticular anatomy, as well as the variation in leaf morphology. Many features are described for the first time for this species, based upon light and electron microscopic observations, including general structure of lower and upper cuticle, stomata, and papillae. At the ultrastructural level, two layers have been distinguished in both lower and upper cuticle, including a homogeneous outer layer with granules and a heterogeneous inner layer with fibrils. Comparison with literature between S. huangii and other relevant species of Sphenobaiera indicate that this species from the Lower Jurassic of China may represent the best-known taxon in the genus Sphenobaiera in both leaf morphology and cuticular structures. Particularly, this study provides the first detailed ultrastructural data on the leaf cuticle of Sphenobaiera, one of the oldest foliage taxa of ginkgoales. This offers further evidence for potential discussion on the taxonomic relationships with other ginkgoalean taxa.
FOOTNOTES
1 The authors thank Prof. Zhiyan Zhou (Nanjing) for helpful suggestion and comments to this study; Prof. Zhaoqi Yao (Nanjing) and Dr. E. V. Bugdaeva (Vladivostok) for kindly translating the Russian references; Mr. Yongqiang Mao (Nanjing) and Mr. Nicolas Labert (Lyon) for technical assistances during the preparation of SEM and TEM samples, and Mr. Terry A. Lott (Gainesville) for help in the preparation of this paper. We thank three anonymous reviewers for their helpful comments and suggestions. This research was supported by the PRA collaborative project between China and France, the National Natural Science Foundation of China Grant (No. 40472004, 40372008, 39900007), the State Key Laboratory of Palaeobiology and Stratigraphy Grant (No. 043113), the Pilot Project of the Knowledge Innovation Program, CAS (No. KZCX2-SW-129), the Talent Training Fund of the State Basic Science Project, NSFC (No. 040203), and the National Science Foundation, U.S.A. (INT 0074295). The first author (Y. D. Wang) acknowledges his sincere thanks for the support of a Research Fellowship from the Alexander von Humboldt Foundation of Germany. This paper is the University of Florida Contribution to Paleobiology publication no. 571. 
6 Authors for correspondence (e-mails: ydwang{at}nigpas.ac.cn
; dilcher{at}flmnh.ufl.edu
)
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