Cretaceous Research 28 (2007) 348e362
www.elsevier.com/locate/CretRes
Morphology and age of Yimaia (Ginkgoales) from Daohugou Village,
Ningcheng, Inner Mongolia, China
Zhiyan Zhou a,*, Shaolin Zheng b, Lijun Zhang c,d
a
Nanjing Institute of Geology and Palaeontology, Academia Sinica, 39 East Beijing Road, 210008 Nanjing, Jiangsu, PR China
b
Shenyang Institute of Geology and Mineral Resources, Ministry of National Land and Resources, Shenyang 110032, China
c
Liaoning Fossil Resources Preservation Administration Department, Shenyang 110032, China
d
Research Centre of Palaeontology and Stratigraphy, Jilin University, Changchun 130026, China
Accepted 15 May 2006
Available online 12 January 2007
Abstract
New ginkgoalean ovulate organs of Yimaia type were found in the fossil-bearing bed of the village of Daohugou, Ningcheng, Inner Mongolia.
They generally resemble other species of Yimaia and some detached seeds described under the morphogeneric name Allicospermum from the
Lower and Middle Jurassic in shape and size of ovules, but are markedly distinguished by the cuticular structure of the integument. The ultrastructure of the megaspore membrane and the associated leaves also differ from those known in comparable taxa. Ginkgoalean leaves found in
the Daohugou bed are mainly of the Ginkgoites type, some of which are still attached to the shoots. They may be classified in three morphotypes.
Leaves of Ginkgoites Morphotype 1, which are most abundant and closely associated with Yimaia, probably belong to the same plant. The
presence of the Jurassic element Yimaia supports the opinion of some invertebrate palaeontologists that the Daohugou bed is of Jurassic
(most probably mid Jurassic) age. In floristic composition, the Daohugou plant assemblage differs from the early Cretaceous Jehol flora, but
closely resembles the Middle Jurassic flora of northeast China.
Ó 2006 Elsevier Ltd. All rights reserved.
Keywords: Ginkgoales; Ovulate organs; Leaves and shoots; Ultrastructure; Megaspore membrane; Ginkgoites; Jurassic, Inner Mongolia
1. Introduction
The fossil-bearing bed of the lacustrine deposits exposed in
the village of Daohugou, Ningcheng County, Chifeng City, Inner Mongolia Autonomous Region, China (Fig. 1), was referred to the Lower Cretaceous Yixian Formation by Wang
et al. (2000). It was correlated with the Jianshangou bed (radiometrically dated at >120 Ma: Swicher et al., 2002) of the
Yixian Formation in the Beipiao area, Liaoning Province,
from which well-preserved beaked birds, feathered dinosaurs,
other animals and abundant plants of the Jehol Biota have
* Corresponding author.
E-mail addresses: [email protected] (Z.Y. Zhou), syzshaolin@yahoo.
com.cn (S.L. Zheng), [email protected] (L.J. Zhang).
0195-6671/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.cretres.2006.05.004
been recovered (Chen and Jin, 1999; Sun et al., 2001; Chang
et al., 2003; Zhou et al., 2003). However, typical elements of
the Yixian Formation in the Beipiao and Yixian areas, such as
Lycoptera, Ephemeropsis, Eoestheria, Confuciusornis, Peipiaosteus, Protopsephurus and Psittacosaurus have not yet
been found in the Daohugou bed. Although some pterosaurs
and amphibians were considered by Wang (2000) and Wang
et al. (2002) to be Cretaceous in age, insects and conchostracans encountered in the bed suggest that it is much older (middle or early late Jurassic: Ren and Oswald, 2002; Zhang, 2002;
Shen et al., 2003). Field observations also favour a lower
stratigraphic position (Ren et al., 2002; Ji and Yuan, 2002;
Liu and Jin, 2002). Ren et al. (2002) argued that it might be
correlated with the Middle Jurassic Chiulungshan (Jiulongshan) Formation in the Western Hills of Beijing. Here, we record Yimaia-type ovulate organs and associated ginkgoalean
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
349
and studied under both light and scanning electron microscopes. The terminology of the constituent parts of the megaspore membrane is modified from Pettitt (1966, 1977), as in
Zhou (1993) and Zhou et al. (2002).
3. Systematic palaeontology
3.1. Ovulate organs
Order: Ginkgoales
Family: Yimaiaceae Zhou 1997
Genus Yimaia Zhou and Zhang, 1988
Fig. 1. Maps showing the location of the village of Daohugou (leaf), Ningcheng, Inner Mongolia.
vegetative organs from the Daohugou bed and compare these
remains to organs from other localities in an attempt to provide further evidence for the age of the bed.
Yimaia capituliformis sp. nov.
Figs. 2e4, 5BeF, 6C right
Derivation of name. After the shape of the ovulate organ.
Type specimens. Holotype PB20241 (Fig. 2B), paratypes
PB20242e20245 (Fig. 2DeG), B0174 a, b (Fig. 2A, C),
CZ101 (Fig. 6C).
2. Material and methods
All the specimens studied were collected from the fossiliferous bed in the village of Daohugou (ca. 41 180 N, 119 140 E;
Fig. 1), but they are from different sources. Most (field nos.
801e835 and Z01e02) were collected by palaeoentomologists
D.Y. Huang and J.F. Zhang of the Nanjing Institute of Geology
and Palaeontology, Chinese Academy of Sciences (NIGPCAS). Some others (field nos. ZE01e10) were collected by
one of us (SZ). These are all deposited in the NIGPCAS collections, and are numbered PB20209e20245). A few were
borrowed from the Institute of Vertebrate Palaeontology and
Palaeoanthropology, Chinese Academy of Sciences, and the
Research Centre of Palaeontology and Stratigraphy, Jilin University: these are numbered B0174a, b, B0184, B0207 and
CZ101 respectively.
According to Ren et al. (2002) and Liu and Jin (2002), the
Daohugou fossiliferous bed overlies unconformably Archaean
gneiss or other Precambrian rocks. It consists mainly of greyish white to yellowish white tuff, tuffaceous sandstone, tuffaceous siltstone and shale, with a tuffaceous conglomerate at
the base. The whole tuffaceous bed is about 50e80 m thick
and is capped by a thick rhyolitic breccia and andesite. The
fossiliferous layers occur in the lower part of the bed. Plants
are commonly fossilized together with well-preserved insects
and small freshwater conchostracans (Euestheria; Shen
et al., 2003). Although Yimaia and associated plant remains
are considered to be allochthonous, they do not appear to
have undergone long-distance transport before deposition. In
some cases, leaves are found in organic attachment to shoots,
and ovule clusters are connected to the peduncle. As is typical
of volcaniclastic deposits, organic matter is rarely preserved.
Only a few specimens of Yimaia bear coal films. So far, no
useful cuticle of associated ginkgoalean leaves has been obtained from the Daohugou bed. The coal films of Yimaia
were macerated in a conventional way with Schulze’s solution
Type locality and stratigraphic horizon. Daohugou, Nengcheng County, Chifeng City, Inner Mongolia Autonomous Region, China, ca. 41 180 N, 119 140 E; Daohugou bed, probably
Middle Jurassic.
Diagnosis. Ovules, generally 5e7 in a terminal cluster,
orthotropous and sessile, nearly circular in outline, mostly
7e9 mm long and 6.5e8 mm wide, with an ovate stone (sclerotesta) and thick flesh (sarcotesta), in some cases forming
broad lateral margins. Stomata irregularly orientated and distributed on surface of integument, up to about 75 per square
mm. Subsidiary cells strongly papillate. Stomatal pit mouth
narrow. Some epidermal cells with papillate periclinal walls
and punctate anticlinal walls. Megaspore membrane bears
a finely granular foot layer. Patterned layer composed of discrete bacula, which are slightly enlarged towards apex, rarely
branched and connected to one another, perpendicular to foot
layer (i.e., radially aligned). Resin bodies present in flesh.
Description. Seventeen ovulate organs have been examined.
Most are impressions of ovule clusters. Only two specimens
(Fig. 6C right and PB20211, unfigured) have ovules attached
to the peduncle. The peduncle is ca. 30 mm long and 2 mm
wide, with the width unchanged throughout the length except
at the slightly enlarged basal end. The surface of the peduncle
is finely striated. The ovules are probably arranged in a close
helix. They are radial and contiguous in the cluster with the
micropyle pointing outwards. Three to seven ovules are visible
on the exposed surface of the cluster (Figs. 2, 6C right).
Compressed ovules (or seeds) are generally similar in shape
and size. They are nearly circular, but some are ovate or oblong in outline owing to displacement of flesh (Fig. 2AeD, G).
The apex (micropyle) is slightly mucronate but rarely visible
(Fig. 2D left, arrow). The ovules are 5e12 mm long and
4e10 mm wide. The stone (sclerotesta) is ovate, 5e9 mm
350
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
Fig. 2. Yimaia capituliformis sp. nov. Enlarged figures of ovulate organs; all scale bars represent 2 mm. A, C, six contiguously arranged ovules partly covered with
coaly matter, showing irregular folds on the surface; dispersed smaller ovate bodies are associated conchostracan shells; paratypes B0174a and B0174b respectively. B, five ovules similarly arranged as in A and C; holotype PB20241 (field no 833). D, E, ovulate organs with seven closely arranged ovules, one in the middle
and the others surrounding it; arrow indicates the somewhat mucronate apex of an ovule in D; paratypes PB20242 and 20243 (field nos. 821 and 824). F, G, laterally compressed ovulate organs; arrows show the scars left by detached ovules; paratypes PB20244 and 20245 (field nos. 832 and 827).
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
long and 3.5e7 mm wide. The flesh (sarcotesta) forms irregular, but mostly longitudinal, wrinkles on the impression. It
varies from 0.3 to 2 mm wide; the greatest width usually on
the lateral sides of the ovules. Neither a pedicel nor a collar
has been detected at the basal part of the ovule. The ovules appear to be attached directly to the peduncle. In some specimens (Fig. 2F, G, arrows), rounded scars 1.2e2 mm in
diameter occur among ovules in the cluster, which are probably left by detached ovules. Detailed measurements of the
ovulate organs are provided in the Appendix.
Coal films of ovules are preserved in only a few cases.
Maceration of the film yields two acid-resistant layers: the
outer cuticle of the integument and the megaspore membrane.
The inner cuticle of the integument and the nucellar cuticle
have not been found. Only faint outlines suggestive of nucellar
cells are sporadically evident when the megaspore membrane
is observed under a light microscope (slide 833-3, not figured).
They are 60e85 mm (or more) long and 25e37 mm wide. The
outer cuticle of the integument is variable in thickness, ranging
from 1.8 to ca. 10 mm. It is thicker over the exposed surface,
but thinner where it is hidden by adjacent ovules. In the thicker
part, cuticular ridges and grooves are evident in surface view
(Fig. 3A). In some cases, the ordinary epidermal cells bear
papillate periclinal walls (Fig. 3B) and developed flanges of
the anticlinal walls (Fig. 3E). In the thinner part, the cuticle
surface is nearly smooth and the cell flanges are less conspicuous (Fig. 3C, D). The ordinary epidermal cells are isodiametric, polygonal or slightly elongate, 20e60 mm long and (16)
20e40 mm wide, in some cases forming ill-defined longitudinal files. The inner surface of the periclinal wall of epidermal
cells is smooth, but very finely granular in texture when
viewed at high magnification (Fig. 5A). The granules are
less than 0.05 mm in diameter. The anticlinal flanges are
straight or slightly wavy, punctate and up to 1.5 mm wide
(Figs. 3D, E, 4A arrows). No trichomes are present.
Haplocheilic stomata are common in the integument
cuticle, but uneven in distribution (Fig. 3BeD), varying in
density from less than 10 to ca. 75 per square mm. They are
randomly orientated (Fig. 3D, E), (60) 80e90 (160) mm long
and 50e70 mm wide. Most apparatuses are polygonal, but
some are oblong (Fig. 3G). Guard cells are sunken and the
thickened part is crescentic when well preserved (Fig. 3E, H),
ca. 30 10 mm. Subsidiary cells (Fig. 3E, G, H) are 4e7,
but mostly six in number, incorporating one or two polar and
the rest lateral. They are strongly papillate and overhang the
guard cells, forming a narrow stomatal pit mouth (Fig. 3B, C,
F). In inner-side view, the subsidiary cells are not specialized,
being only slightly smaller than the ordinary cells. Encircling
cells are present but sparse.
The megaspore membrane is ca. 4e5 mm thick. It consists
of a foot layer and a patterned layer. The foot layer is finely
granular in texture, with granules ca. 0.05e0.1 mm in diameter
(Fig. 5B). The bacula in the patterned layer are up to 5 mm
long and 0.7e2.4 (mostly more than 1) mm wide, usually
with their thickness almost unchanged along their length, but
slightly narrower at the basal end. They may be thinner, or
rapidly enlarged and somewhat rounded or cup-shaped at the
351
distal end (Fig. 5CeE). The bacula are rarely branched and
connected to one another; they are more or less parallel to
one another and perpendicular to the foot layer.
While macerating the coal films of the ovules, a resin body
(Fig. 5F) was detected. It is fusiform, 360 mm long and
148.5 mm wide. The surrounding cells are oblong to polygonal, sometimes isodiametric, with wavy anticlinal walls.
They are 45e60 mm long and 14e27 mm wide.
In close association with the ovulate organs are detached
leaves and leafy shoots mainly of the Ginkgoites type, some
of which are illustrated in Figs. 6 and 7, and described below.
Comparison. In gross morphology, the ovulate organs
described strongly recall those referred to the type species of
Yimaia, Y. recurva Zhou and Zhang (1988, 1992) from the Middle Jurassic Yima Formation of Henan, China. They are similar
in shape and with irregular wrinkles on their surface but are
generally slightly smaller and less numerous in the cluster, although all fall within the range of variation of Y. recurva
(Zhou and Zhang, 1992, p. 159). Only the resin body found
(Fig. 5F) is quite different; it bears some resemblance to those
of Ginkgo, being fusiform and large, while in Y. recurva the
resin bodies are very small and ovoid (Zhou and Zhang,
1992, p. 159; pl. 6, fig. 5).
Both the integument cuticle and the megaspore membrane
are different in structure from those of Y. recurva. The epidermal cells of the upper cuticle of the integument in some cases
have papillate periclinal walls (Fig. 3B) and irregularly thickened, punctate anticlinal walls (Figs. 3E, 4A). In Y. recurva,
the periclinal walls are free of any papilla and the anticlinal
walls are straight and evenly thickened (Zhou and Zhang,
1992, pl. 8, figs. 3, 4). In general, the stomata are more numerous in Y. capituliformis than in the type species, and significantly differ in structure; the subsidiary cells are papillate and
the papillae form strong obtuse bulges projecting over the stomatal pit (Fig. 3B, C, F). In Y. recurva, the subsidiary cells are
normally not as thick as ordinary cells, bearing a thin patch in
the middle of the periclinal wall forming a depression on both
the outer and inner surfaces (Zhou and Zhang, 1992, pl. 5,
figs. 1, 5, 6; pl. 8, figs. 1, 2). Although the megaspore membranes of both forms incorporate generally similar foot and
patterned layers, the bacula in the patterned layer of Y. capituliformis are thicker, more sparsely distributed and regular in
shape and size. They are hardly branched or connected to one
another (Fig. 5C, D). The configuration of the whole of the patterned layer looks, therefore, different from that of Y. recurva
(Zhou and Zhang, 1992, pl. 8, fig. 6; Zhou, 1993, pl. 5, fig. 5).
It is obvious from the above observations that the ovulate
organs described here cannot be referred to the type species.
Evidence from associated leaves (see below) also does not
favour a connection between our specimens and Y. recurva.
Despite the fact that numerous vegetative organs have been
collected from the Daohugou bed, no leaves of the Baiera hallei type, which are considered to belong to the same plant as
Y. recurva, have been found.
Ginkgoalean ovulate organs of the Yimaia type have scarcely
been reported outside China. The oldest known comparable
352
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
Fig. 3. Yimaia capituliformis sp. nov. Scanning electron micrographs of the outer cuticle of the integument. A, outer surface with irregular ridges and grooves;
specimen B0174b. B, cells with thickened and papillate periclinal walls on the outer surface; arrows indicate stomata; PB20241. C, outer surface with indistinct
cell outlines and prominent stomata; B0174b. D, inner surface showing randomly orientated stomata and polygonal epidermal cells with weakly developed anticlinal flanges and smooth periclinal walls; B0174b. E, inner surface showing distinct cells and stomata, encircling cells rarely present; B0174b. F, a stoma in outer
surface view, showing papillate subsidiary cells and wax-like substance on the surface; B0174b. G, inner surface view of an oblong stoma, guard cells only partly
preserved; the periclinal wall of epidermal cells is smooth; arrow indicates a papilla; PB20241. H, a stoma in inner surface view, cutinized part of guard cells
crescentic; PB20241. Scale bars represent 20 mm in A, D, G, 100 mm in B, C, and 10 mm in E, F, H.
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
353
Fig. 4. A, B, Yimaia capituliformis sp. nov., PB20241. Light micrographs of outer cuticle of integument of megaspore membrane; arrows in A indicate punctate
anticlinal walls of ordinary epidermal cells; scale bars represent 5 mm.
specimens were recorded from the Rhaeto-Liassic transitional
layers of Franconia, Germany by Braun (1843). Although
Schenk (1867) threw doubt on the nature of the organs and
described them as young foliage of ferns, a restudy by Kirchner
(1992) confirmed that they are young ovulate organs of Baiera
muensteriana (Presl, in Sternberg) Heer. Kirchner (1992, pl. 1,
figs. 1e3) figured three specimens and some associated seeds.
The specimens in his pl. 1, figs. 1 and 3 were originally
published by Schenk (1867, pl. 9, figs. 1, 2). The young ovulate
organs are different from Yimaia in that they are attached to the
distal end of bifurcate pedicels. No mature organs of the
German species have been found. However, the detached seeds
generally resemble those of both Yimaia recurva and Y. capituliformis. They are about the same shape and size as the Chinese
species, and also bear resin bodies in the flesh. Although such
detached seeds differ from ovules of Y. capituliformis in their
sparsely stomatiferous outer integument cuticle and their epidermal cells with straight, evenly thickened anticlinal flanges,
they are closely similar to ovules of Y. recurva in these respects.
The only feature distinguishing the German species from Yimaia is that the young ovulate organs are pedicellate, but it is
possible that their pedicels were subsequently reduced to the extent that they are undetectable in the mature organ. Ginkgo biloba shows a similar ontogeny. While pedicels are commonly
visible in the juvenile organs, they are normally absent when
mature. A corresponding trend has even been traced in the evolution of ovulate organs of the genus Ginkgo (Zhou, 1991, 1994,
1997; Zhou and Zhang, 1989; Zhou and Zheng, 2003). There is
an alternative possibility, however, as pointed out by Kirchner
(1992, p. 28), which is that mature ovulate organs of Baiera
muensteriana might bear pedicellate ovules as in the young organs and hence differ from those of Yimaia. Further material is
needed to solve this problem. Whether the German ovulate organs belong to Yimaia or not, their poorer preservation precludes closer comparison with our specimens at present.
Similar ovulate organs were found by Black (1929) in association with Baiera gracilis Bunbury [¼B. furcata (L. and H.)
according to Harris and Millington, 1974] in the Middle Jurassic Yorkshire flora. These bear 4e6 ovules attached in terminal clusters to a slender axis. Unfortunately the material has
not yet been traced and restudied. In revising the Yorkshire
Jurassic ginkgoalean plants, Harris and Millington (1974) described only isolated seed stones attributed to B. furcata. According to the description given by Black (1929, p. 424), the
seeds are similar in shape and size to those of Y. recurva
and Y. capituliformis. The surface is commonly wrinkled and
the upper cuticle of the integument is composed of polygonal
cells with fairly thick anticlinal walls and thickened periclinal
walls as in Yimaia. Stomata are not numerous, and the stomatal structure of the integument cuticle differs from that of both
Y. recurva and Y. capituliformis. The subsidiary cells are only
slightly thickened in the middle part (Black, 1929, fig. 10).
They do not form strong obtuse bulges projecting over the stomatal pit as in Y. capituliformis (Fig. 3B, C, F), neither do they
bear a thin patch in the middle of the periclinal wall and form
a depression on both outer and inner surfaces, as in Y. recurva
(Zhou and Zhang, 1992).
Detached seeds similar to those of Yimaia have been referred to the morphogenus Allicospermum Harris (1935).
Among them, A. xystum Harris from Liassic of Greenland,
which has been regarded as the seed of Ginkgoites taeniata
(Braun), is closely comparable in general gross morphology.
The seeds are circular and bear a thick outer integument cuticle and resin bodies in the flesh, as in Y. capituliformis. The
stomata on the integument cuticle are, however, much fewer
in number and different in structure. The subsidiary cell
does not bear a papilla, but is only thickened at or near the
proximal margin in certain specimens (Harris, 1935, p. 122;
fig. 46C, D; pl. 9, fig. 10.). Tralau (1966) considered Allicospermum baiereanum and A. ginkgoideum, described from
the Middle Jurassic of Scania, Sweden, to be related to vegetative leaves assigned respectively to Baiera gracilis and Ginkgoites regnellii. The Swedish seeds are also similar to the
ovules described here in shape and size. Allicospermum baiereanum is easily distinguished by having fewer and structurally
different stomata in the integument cuticle. Tralau (1966 pp.
24e27), did not provide a description or illustration of the stomata of A. ginkgoideum. His description of the epidermal cells
of the integument cuticle indicates that they differ from those
of Y. capituliformis in their thick and straight anticlinal walls.
354
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
Fig. 5. Yimaia capituliformis sp. nov. Scanning electron micrographs of resin body, and ultrastructure of megaspore membrane and cell periclinal wall; all from the
holotype PB20241 except A. A, finely granular inner surface of outer periclinal wall of ordinary epidermal cell; B0174b. BeE, megaspore membrane. B, granular
foot layer. CeE, different views of bacula in the patterned layer of the megaspore. C, bacula differing in size, rarely branched, some with an enlarged head. D,
bacula horizontal and nearly parallel in distribution. E, detail of structure of bacula. F, a resin body, showing outlines of surrounding epidermal cells. Scale bars
represent 2 mm in A, D, 1 mm in B, E, 3 mm in C, and 20 mm in F.
A detailed comparison of Yimaia capituliformis with the
above-mentioned forms indicates that although most of them
are still insufficiently known, only isolated ovules (seeds) or
immature ovulate organs being found, their ovules are very
similar in gross morphology and differ only in some cuticular
details (Table 1). It is of interest to note that all these more or
less comparable specimens are from the Lower or Middle
Jurassic of the Northern Hemisphere. They are found in close
association with certain ginkgoalean leaves of the Baiera or
Ginkgoites type, as is the case for Yimaia from northern China.
They are clearly related to Yimaia to a certain degree and all
belong to the Ginkgoales, some possibly to the Yimaiaceae
(Zhou, 1997, 2003) and even to the same genus.
3.2. Associated ginkgoalean vegetative organs
Most frequently associated with Yimaia ovulate organs in
the Daohugou bed are detached leaves of Ginkgoites type.
They are fairly abundant and exhibit a considerable variation
in gross morphology. Some dwarf and long shoots are found
with attached Ginkgoites-type leaves. It is likely that at least
some of these Ginkgoites-type leaves and leafy shoots are attributed to the same plant that produced the ovulate organs
Y. capituliformis. Since an organic connection has not been
detected, the associated Ginkgoites leaves and shoots are
only classified tentatively according to their gross morphology
below. Besides Ginkgoites, Sphenobaiera is the other
Table 1
Comparison of Yimaia capituliformis with other species of the genus, similar ginkgoalean ovulate organs and isolated ovules (seeds)
Yimaia capituliformis
Yimaia recurva
Ovulate organs
(B. gracilis)
Seeds and young
ovulate organs
(B. muensteriana)
Allicospermum xystum
A. baiereanum
A. ginkgoideum
Ovulate organ
pedunculate
pedunculate
pedunculate
e
e
e
Ovules (seeds)
shape
number in cluster
size (mm mm)
Resin bodies
(mm mm)
Integument cuticle
(mm)
shape of cells
cell size (mm mm)
periclinal walls
anticlinal walls
circular or ovate
ovate to round
oval
ovules with
pedicels
oval
circular
oval
3e7
5e12 4e10
360 148.5
up to 9
7e10 6.5e10
27.5 15e30
4e6
7e8 6.5e7
e
3(6)
8.25e10.5 6.3e7.9
900 700
e
diameter 11
1000 500
1.8eabout 10
2.5e10
e
up to 10
very thick
e
11 8
2700e1000
mm long
thick
subcordate to
round
e
9e11 10
1000 500 ?
53.6e70 40e57
some papillate
straight, regular in
thickness
e
slightly hickened
straight, strongly
marked
e
e
straight, fairly thick
e
e
e
straight, thick
e
35, but few in
detached seeds
(slightly sunken)
(strongly cutinized)
e
sparsely scattered
e
very few
e
Few
sunken
4e6, without papilla
e
(not thickened)
e
e
(usually present?)
moderately thick
e
B. meunsteriana
e
fairly thick
e
Ginkgoites taeniata
e
e
e
B. gracilis
e
?
e
Ginkgoites
regenllii
Franconia
Liassic
Kirchner, 1992
Greenland
Liassic
Harris, 1935
Stomata
size (mm mm)
density (/mm2)
polygonal to nearly isodiametric in greater part of ovules
20e60 15e40
20e100 17.5e50
15e40 15e35*
some papillate
smooth
thick near centre
punctuate, irregularly
regular in thickness
fairly thick
thickened
irregular in distribution and orientation
60e160 50e70
120e150 80e100
50 80*
10e75
rare
uncommon
Guard cells
Subsidiary cells
deeply sunken
4e7, strongly papillate
sunken
3e6, unspecialized
Encircling cells
Megaspore membrane
bacula
Associated leaves
sometimes present
4e5 mm
discrete
Ginkgoites sp.
usually absent
1.2 (3) mm
scarcely branched
Baiera hallei
Locality
Age
Reference(s)
Inner Mongolia, China
middle Jurassic
this paper
Henan, China
middle Jurassic
Zhou and Zhang, 1992;
Zhou, 1993
sunken
5e7, hardly
thickened
not seen
1e2 mm
e
Baiera gracilis
(furcata)
Yorkshire
middle Jurassic
Black, 1929;
Harris and
Millington, 1974
thick
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
Characters
Scania
middle Jurassic
Tralau, 1966
The figures in parentheses represent the extremes; those accompanied by * are measured from published figures. The characters in parentheses are also derived from published figures.
355
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
356
ginkgoalean vegetative leaf type so far collected from the Daohugou bed. They are rare and very fragmentary and not described here. So far, only Ginkgoites- or Baiera-type
vegetative leaves are considered to be related to Yimaia and
similar reproductive organs (Table 1).
Genus Ginkgoites Seward, 1919
Remarks. Ginkgoites Seward is here used as a morphogeneric
(or form-generic) name for Ginkgo-like fossil leaves that cannot
be attributed to any natural genus of Ginkgoales with certainty
(Zhou, 1991, 1997; Zhou and Zhang, 1989; Watson et al., 1999).
Ginkgoites sp. (Morphotype 1)
Fig. 6
Description. Leaves small to moderate in size, consisting of
a flabellate lamina and a distinct petiole. The lamina is
13e49 mm long and 30e68 mm wide. It is normally wider
than long and the lateral margins form a narrow basal angle
of about 90e110 . Only in a few leaves is the length of the lamina close to the width (Fig. 6B) and in some cases the lamina
has a wider basal angle up to 200e220 (Fig. 6D). The lamina
is deeply divided in the middle down nearly to the apex of the
petiole. The two halves are further divided (1) 2e3 times into
(4) 6 (8e10) segments. The segments are broad oblanceolate to
somewhat obovate in shape, with the widest part 5e7.5 (13.5)
mm wide above the middle, sometimes in the distal one-third.
They have an obtuse to rounded apex and usually distinct venation. The veins bifurcate in the proximal part of the segment,
but become parallel in the middle and distal parts and slightly
convergent at the apex. In the ultimate segments, 4e18 veins
are visible. The number of veins varies according to the width
of the segments, but the distance between adjacent veins is
rather constant, normally less than 1 mm (ranging from ca.
0.4 to 0.8 mm), and there are (10) 12e18 (22) veins per cm.
The petiole is up to 25 mm long and ca. 1.5e2 mm wide in
well-developed leaves, but shorter and stout in smaller leaves.
Comparison and discussion. Five Ginkgoites leaves of Morphotype 1 illustrate the variation in shape and size, and extent
of lamina division (Fig. 6). Since no epidermal characters are
available, they have been grouped together based on their
general resemblance in gross morphology. Leaves of this
type typically have a narrow basal angle, broad oblanceolate
to obovate segments with an obtuse to rounded apex and moderately dense veins (see also Appendix). They are the most
common leaves found in association with Y. capituliformis in
the collection. In one case, a leaf of this type is preserved together with ovulate organs in the same slab as if they were
borne on the same shoot (Fig. 6C). It is very likely that this
type of leaf belongs to Y. capituliformis (Fig. 8).
More or less comparable leaves have been recorded from
Jurassic strata in other parts of China and elsewhere. A close
Fig. 6. Yimaia capituliformis sp. nov. and associated Ginkgoites leaves of Morphotype 1; all scale bars represent 5 mm. A, juvenile leaf with a short and thick
petiole; PB20222 (field no. ZE08). B, small leaf, lamina with six segments forming a narrow basal angle; PB20223 (field no. ZE09). C, leaf with deeply divided
segments that appear to be attached to an ovule organ bearing six contiguously arranged ovules at the top of a peduncle; paratype CZ101. D, well-developed leaf
with eight segments; PB20219 (field no. ZE05). E, less divided large leaf, PB20221 (field no. ZE07).
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
comparison with any of them cannot be made in the absence of
leaf cuticle. However, the similarities and differences in gross
morphology between the present form and a selection of
leaves are mentioned below.
In China, similar leaves were recorded from the Jurassic of
Shihkuaitsun (Shiguacun) in former Suiyuan Province, now
Inner Mongolia, as Ginkgo cf. hermelinii (Nathorst) Hart by
Sze (1933, p. 28, pl. 7, figs. 5e6), and later referred to
Ginkgo huttonii (Sze, Lee et al., 1963). The two fragmentary
leaves figured resemble the larger leaves of Morphotype 1 in
Fig. 6C and E in the shape of segments and the density of
veins. Typical leaves of Ginkgoites marginatus (Nathorst)
Florin (¼Ginkgoites hermelinii) and Ginkgo huttonii (Sternberg) Heer are easily separated from our material. The segments of G. huttonii are characterized by irregularly
truncated or notched apices (Harris and Millington, 1974).
Ginkgoites marginatus (Nathorst) Florin from Scania differs
in having long and much narrower, linear to lanceolate segments (Lundblad, 1959). Our form has shorter and broader
segments with obtuse or rounded apices. Ginkgoites obrutschewii Seward (1911) from the Jurassic of the Diam River,
northern Xinjiang Uygur Autonomous Region (Chinese
Dzungaria) also bears a general resemblance in leaf and segment shape, but differs in having fewer (only 2e4) segments
and sparser veins. Some smaller leaves of Ginkgo yimaensis
(Zhou and Zhang, 1989, text-fig. 3A, C, F, H) from the Middle Jurassic of Yima, Central China, may be confused with
this type of leaf, but the Yima leaves are usually larger and
have fewer veins per segment. Their associated ovulate organs are quite different.
The leaves in Fig. 6A, B and D resemble some examples
of Ginkgoites taeniata (Braun) from the Thaumatopteris Zone
of East Greenland (Harris, 1935, text-fig. 1B, F, G), which
also shows a considerable variation in shape and size. Segments are, however, narrower and veins sparser in the Greenland specimens. Ginkgoites khorassanicus Fakhr (1977),
described from the LowereMiddle Jurassic of Ferizi, northeast Iran, bears a close resemblance to Morphotype 1 in
shape of leaves and segments, but the leaves are usually
larger and there are fewer veins per segment. Ginkgo cordilobata, described by Schweitzer and Kirchner (1995, p. 16,
pl. 3, figs. 1e7; pl. 4, figs. 1, 2; text-figs. 9, 10) from the
Dogger of Afghanistan is another comparable species. Both
have similar broad segments with obtuse or rounded apices.
The leaves of the Afghan species, however, are much larger;
the lamina always forms a larger basal angle (mostly ca.
180 ) and the widest part of segments is near the apex.
The veins also differ in their variable density and bifurcation
at any place within the segment. The typical Liassic species
in Iran assigned to Ginkgo parasinglaris Kilpper (1971;
Schweitzer and Kirchner, 1995) is easily distinguished from
Morphotype 1 by its larger size and lanceolate segments,
although the small basal angle and the vein density in the
segments are similar.
Ginkgoites sp. (Morphotype 2)
Fig. 7A, B
357
Description. Leaves of moderate size, consisting of a flabellate lamina and a distinct petiole. The lamina is 20e54 mm
long and 21e60 mm wide. Its lateral margins form a narrow
basal angle of 40e80 (rarely up to 130 ). The lamina is
deeply divided 2e3 times into (4) 5e8 segments. The
segments are linear to lanceolate, with the widest part (2e
4 mm) near or above the middle. The apex of segments is obtuse or obtusely pointed. The veins are distinct and bifurcate in
the lower part of the segment. In the ultimate segment, 4e7
veins are visible. There are 14e18 (21) veins per cm. The petiole is 8e35 mm long and about 0.7e2 mm wide.
Some leaves of this type (Fig. 7B, and PB20229 not figured) are found still attached to the distal end of dwarf shoots
of the Ginkgoitocladus type (Krassilov, 1972). The leaf scars
are rhombic and closely arranged, but no scars of vascular
bundles or other details are shown.
Comparison and discussion. Leaves of this type differ from
those of Morphotype 1 mainly in having more deeply dissected lamina and much narrower segments. The veins are
fewer in the ultimate segment of this leaf type, but this is
owing to the difference in segment width. The density of veins
is similar in leaves of the two types (see Appendix), and in
some other respects they are hardly distinguishable from
each other. Both types have a small basal lamina angle and
few segments with an obtuse to rounded apex.
Morphotype 2 is similar to Ginkgoites baieraeformis and
Ginkgoites sp. cf. G. baieraeformis described from the Liassic
of northern Iran by Kilpper (1971, pp. 92, 93) in the number of
segments and deeply divided lamina with a small basal angle.
The segments in our morphotype are, however, wider and
usually contain more veins in the ultimate segments. Schweitzer and Kirchner (1995, p. 24; pl. 6) later transferred the Iranian species to Baiera and included in it a number of leaves
that are quite different from ours in being more dissected
and bearing numerous linear segments.
Leaves of Morphotype 2 also resemble Ginkgoites longifolius (Phillips) (Harris, 1946; Harris and Millington, 1974) in
the density of their veins and the shape of the lamina. The
Yorkshire Jurassic species usually has more and narrower ultimate segments that may fork at their apices. Ginkgoites dissecta Schweitzer and Kirchner (1995, p. 14) from the
Middle Jurassic of Afghanistan bears some resemblance to
this type of leaf in its small basal lamina angle, the number
of segments, and in vein density, but it is larger. In this respect,
it comes closer to leaves of Morphotype 3, described below.
Ginkgoites taeniata (Braun) also includes some leaves (Harris,
1935, text-fig. 10AeC) that match Morphotype 2 in gross
morphology, but it differs in that the apex of each segment
is irregularly notched.
Ginkgoites sp. (Morphotype 3)
Fig. 7C, D
Description. Leaves large, consisting of a narrowly wedgeshaped lamina and a distinct petiole. The lamina is 75e
125 mm long and 42e55 mm wide. Its lateral margins form
358
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
Fig. 7. Associated Ginkgoites leaves, long and short shoots; dispersed small ovate bodies in the figures are associated conchostracan shells. A, enlarged Ginkgoites
leaf of Morphotype 2, lamina deeply divided and segments narrow; B0207. B, several Ginkgoites leaves of Morphotype 2 attached to the apex of a short shoot;
PB20217 (field no. ZE02). C, long and short shoot with attached Ginkgoites leaves of Morphotype 3; PB20230 (field no. ZE04). D, leaf of Ginkgoites Morphotype
3; B0184. Scale bars represent 5 mm in A, B, D, and 1 cm in C.
a very narrow basal angle of 50e60 . The lamina is deeply
divided twice or three times into 4e6 segments. The segments
are linear to lanceolate, with the widest part (6e8.5 mm) near
or above the middle. Their apices are obtusely pointed. The
veins are distinct and bifurcate in the lower part of the segment. In the ultimate segment, 4e13 veins are visible. There
are 12e15 veins per cm. The petiole is 15e50 mm long and
1e2 mm wide.
In one specimen (partly figured in Fig. 7C), 5e6 leaves are
borne on a dwarf shoot ca. 15 mm long and 8 mm wide, which
is in turn attached to a shoot that is more than 240 mm long
and ca. 10 mm wide. No distinct leaf scars or other significant
surface markings are visible on the shoots.
Comparison and discussion. Only two specimens of this leaf
morphotype have been found. They differ from Morphotype 2
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
359
Baiera hallei, B. gracilis and Ginkgoites taeniata (Zhou and
Zhang, 1992; Harris and Millington, 1974; and Harris, 1935,
respectively). In these cases, the associated leaves also show considerable variation in shape and size of the lamina and segments.
4. The geological age of the Daohugou bed
Fig. 8. Suggested reconstruction of Yimaia capituliformis sp. nov.
only in their larger size (see Appendix). There are no intermediate specimens between the two types in the collection.
More or less comparable leaves have been recorded from the
Middle Jurassic Upper Yaopo Formation of the Western Hills of
Beijing by Chen et al. (1984, p. 58; pl. 26, figs. 6, 7) under the
name of Ginkgoites aff. sibiricus (Heer). They are similarly
large, with long, narrow segments forming a small basal lamina
angle. Siberian specimens ascribed to Ginkgoites sibiricus
(Doludenko and Rasskasova, 1972), however, cannot be confused with leaves of Morphotype 3. Ginkgoites taeniata and
G. hermelinii (¼G. marginatus) may include some leaves of
similar shape and size (e.g., Gothan, 1914, pl. 31/32, fig.1 under
the name of Baiera taeniata, and Harris, 1935, fig. 6B), although
typical leaves of the two species are readily distinguishable.
General remarks on the associated leaves.
Although the associated Ginkgoites leaves have been referred
to three different morphotypes, they share several common features. As shown in the Appendix, they are close to one another in
having more or less similar basal angles, number of segments,
and veins per cm. The main differences are in the size of laminae
and the width of segments. In Ginkgoales, vegetative leaves
exhibit considerable variation in gross morphology within a single species. Leaves that vary in size and in the extent of divisions
may occur in a single tree of G. biloba. It is, therefore, not impossible that all the three types of leaves belong to the same plant.
Despite the fact that evidence from cuticular structure is
lacking, the close association of Ginkgoites leaves, especially
those of Morphotype 1, with Yimaia capituliformis is significant
(Fig. 6C). As shown in Table 1, all ovulate organs (including
similar isolated seeds) of the Yimaia type are found associated
with Ginkgoites- or Baiera-type leaves. In some of them, large
numbers of specimens have been found and examined, as in
Ginkgoalean ovulate organs of the Yimaia type or similar
detached ovules (seeds) are hitherto known only in Early or
Middle Jurassic deposits (Table 1). Although Yimaia capituliformis is described as a new species, it does indicate a similar
Jurassic, rather than an early Cretaceous, age for the fossiliferous Daohugou bed. It is not possible at present to identify the
associated leaves with any described species of Ginkgoites.
However, all comparable leaves of the three morphotypes are
from Early or Middle Jurassic strata elsewhere in China and
other countries (see above). In the early Cretaceous Yixian
flora of the same region about 100 plant fossils have been
recorded (Wu, 1999; Sun et al., 2001), but neither Yimaiatype ovulate organs nor any similar Ginkgoites leaves described
herein have been found. Fossil ginkgoaleans are, moreover, not
abundant in the Yixian flora. Although it has recently yielded
a new Ginkgo, the ovulate organs are believed to be more
advanced in structure than those of Middle Jurassic type
(Zhou and Zheng, 2003). Further evidence for a Jurassic age
for the Daohugou bed comes from the floristic composition
of the plant assemblage recovered from it. Taxodiaceous conifers referred to Yanliaoa, and bennettitaleans, such as Anomozamites, Cycadolepis and Pterophyllum, are often encountered.
They are all common members of the Middle Jurassic flora in
this part of China (P’an, 1977; Zhang and Zheng, 1987), but
absent from the Yixian flora. On the other hand, angiosperms
and gnetaleans, which are important elements of the Yixian
flora (Cao et al., 1998; Duan, 1998; Sun et al., 1998, 2001;
Wu, 1999; Guo and Wu, 2000; Leng and Friis, 2003), have
not been found in the Daohugou plant assemblage. Hence,
evidence from the fossil plants encountered supports the opinion of some geologists and invertebrate palaeontologists that
the Daohugou bed is probably Middle Jurassic in age.
Acknowledgements
The study was supported by the Major Basic Research
Project of MST China (G2000077700) and the Pilot Project
of Knowledge Innovation Programme, CAS (KZCX2-114).
We thank D.Y. Huang and J.F. Zhang for providing most of
the specimens, the IVPP team on the Jehol Biota for the
loan of some well-preserved specimens, and Y.G. Ren, X.Y.
Fan, X.J. Yang and C.Z. Wang for various technical assistance.
Thank are also due to Professor David Batten and two anonymous referees for their constructive comments on the paper
and linguistic correction.
References
Black, M., 1929. Drifted plant-beds of Upper Estuarine series of Yorkshire.
Quarterly Journal of Geological Society, London 85, 389e437.
360
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
Braun, C.F.W., 1843. Beiträge zur Urgeschichte der Pflanzen. In: Münster,
Zu, G.G. (Eds.), Beiträge zur Petrefaktenkunde, 6, Bayreuth, pp. 1e46.
Cao, Z.Y., Wu, S.Q., Zhang, P.A., Li, J.R., 1998. Discovery of fossil monocotyledons from Yixian Formation, western Liaoning. Chinese Science Bulletin 43, 230e233.
Chang, M.M., Chen, P.J., Wang, Y.Q., Wang, Y. (Eds.), 2003. The Jehol Biota:
The Emergence of Feathered Dinosaurs, Beaked Birds and Flowering Plants.
Shanghai Scientific and Technological Publishers, Shanghai, 208 pp.
Chen, F., Dou, Y.W., Huang, Q.S., 1984. The Jurassic Flora of West Hills, Beijing (Peking). Geological Publishing House, Beijing, 136 pp. (in Chinese,
English summary).
Chen, P.J., Jin, F. (Eds.), 1999. Jehol Biota. Palaeoworld 11 (Special Issue).
Press of University of Sciences and Technology of China, Hefei, 342 pp.
(in Chinese, English abstract).
Doludenko, M.P., Rasskasova, E.S., 1972. Ginkgoales and Czekanowskiales of
the Irkutsk Basin. In: Doludenko, M.P., Lebedev, E.L., Rasskosova, E.S.,
Samylina, V.A. (Eds.), Mesozoic Plants (Ginkgoales and Czekanowskiales) from Eastern Siberia. Nauka, Moskva, pp. 7e43 (in Russian).
Duan, S.Y., 1998. The oldest angiosperm e a tricarpous female reproductive
fossil from western Liaoning Province, NE China. Science in China D
41, 14e20.
Fakhr, M.-S., 1977. Contribution à l’étude de la flore rhéto-liassique de la
formation Shemshak de l’Elbours (Iran). Comité des Travaux Historiques
et Scientifiques, Mémoires. Section Sciences 5, 1e178.
Gothan, W., 1914. Die unterliassische (Rhätische) Flora der Umgegend von Nürenberg. Abhandlungen Naturhistorischen Gesellschaft, Nürenberg 19, 91e186.
Guo, S.X., Wu, X.W., 2000. Ephedrites from latest Jurassic Yixian Formation
in western Liaoning, northeast China. Acta Palaeontologica Sinica 39
(Supplement), 81e91 (in Chinese, English summary).
Harris, T.M., 1935. The fossil flora of Scoresby Sound, East Greenland, 4.
Ginkgoales, Coniferales, Lycopodiales and isolated fructifications. Meddelelser om Grønland 112, 45e148.
Harris, T.M., 1946. Notes on the Jurassic flora of Yorkshire, 28e30. 28. Czekanowskia microphylla (Phillips) Seward; 29. Nilssoniopteris vittata
(Brongn,) Florin; 30. Ginkgoites longifolius (Phillips) n. com. Annals
and Magazine of Natural History 11 (13), 1e24.
Harris, T.M., Millington, W., 1974. Ginkgoales. In: Harris, T.M.,
Millington, W., Miller, J. (Eds.), The Yorkshire Jurassic Flora IV. British
Museum (Natural History), London, pp. 2e78.
Ji, Q., Yuan, C.X., 2002. Discovery of two kinds of protofeathered pterosaurs
in the Mesozoic Daohugou biota in the Ningcheng region and its stratigraphic and biologic significance. Geological Review 48, 221e224 (in
Chinese, English abstract).
Kilpper, K., 1971. Über eine Rät/Lias-Flora aus dem nördlischen Abfall des
Alburs-Gebirges in Nord-Iran. Teil 2: Ginkgophyten-Belaubungen. Palaeontographica B 133, 89e102.
Kirchner, M., 1992. Untersuchungen an einigen Gymnospermen der Fränkischen Rhät-Lias- Grenzschichten. Palaeontographica B 224, 17e61.
Krassilov, V.A., 1972. The Mesozoic Flora of the Bureja River (Ginkgoales
and Czekanowskiales). Nauka, Moskva, 115 pp. (in Russian).
Leng, Q., Friis, E.M., 2003. Sinocarpus decussatus gen. et sp. nov., a new
angiosperm with basally syncarpous fruit from the Yixian Formation of
northeast China. Plant Systematics and Evolution 241, 77e88.
Liu, Y.Q., Jin, X.C., 2002. Mesozoic biota-bearing depositional successions in
the Lingyuan Basin, western Liaoning and their ages: a discussion. Geological Bulletin of China 21, 592e595 (in Chinese, English abstract).
Lundblad, B., 1959. Studies in the Rhaetic-Liassic floras of Sweden, II, 1.
Ginkgophyta from the Mining district of NW Scania. Kungliga Svenska
Vetenskapsakademiens Handlingar 4, 6 (2), 1e38.
P’an, K., 1977. A Jurassic conifer Yanliaoa sinensis gen. et sp. nov. from Yaoliao region. Acta Phytotaxonomica Sinica 15, 69e71 (in Chinese, English
abstract).
Pettitt, J.M., 1966. A new interpretation of the structure of the megaspore
membrane in some gymnospermous ovules. Journal of the Linnean Society
(Botany) 59, 253e263.
Pettitt, J.M., 1977. The megaspore wall in gymnosperms: ultrastructure in
some zooidogamous forms. Proceedings of Royal Society of London B
195, 497e515.
Ren, D., Gao, K.Q., Guo, Z.G., Ji, S.A., Tan, J.J., Song, Z., 2002. Stratigraphic division of the Jurassic in the Daohugou area, Ningcheng, Inner
Mongolia. Geological Bulletin of China 21, 584e591 (in Chinese,
English abstract).
Ren, D., Oswald, D., 2002. A new genus of Kallihemerobiidae from the Middle Jurassic of China (Neuroptera). Stuttgarter Beiträge zur Naturkunde B
317, 1e8.
Schenk, A., 1867. Die fossile Flora der Grenzschichten des Keupers und Lias
Frankens. C.W. Kreidel’s Verlag, Weisbaden, 232 pp.
Schweitzer, H.-J., Kirchner, M., 1995. Die Rhäto-Jurassischen Floren des Iran
und Afghanistans: 8. Ginkgophyta. Palaeontographica B 237, 1e58.
Seward, A.C., 1911. Jurassic plants from Chinese Dzungaria collected by Prof.
Obrutschew. Mémoires du Comité Géologique de St. Pétersburg. Nouvelle
Série 75, 1e61.
Seward, A.C., 1919. Fossil Plants, 4. Cambridge University Press, Cambridge,
543 pp.
Shen, Y.B., Chen, P.J., Huang, D.Y., 2003. Age of the fossil conchostracans
from Daohugou of Ningcheng, Inner Mongolia. Journal of Stratigraphy
27, 311e313 (in Chinese, English abstract).
Sun, G., Dilcher, D.L., Zheng, S.L., Zhou, Z.K., 1998. In search of the first
flower: a Jurassic angiosperm, Archaefructus, from northeast China. Science 282, 1692e1695.
Sun, G., Zheng, S.L., Dilcher, D.L., Wang, Y.D., Mei, S.W., 2001. Early
Angiosperms and their Associated Plants from Western Liaoning, China.
Scientific and Technological Education Publishing House, Shanghai, 227
pp. (in Chinese and English).
Swicher III, C.C., Wang, X.L., Zhou, Z.H., Wang, Y.Q., Jin, F., Zhang, J.Y.,
Xu, X., Zhang, F.C., Wang, Y., 2002. Further support for a Cretaceous
age for the feathered-dinosaur beds of Liaoning, China: New 40Ar/39Ar
dating of Yixian and Tuchengzi formations. Chinese Science Bulletin
47, 135e138.
Sze, H.C., 1933. Beiträge zur mesozoischen Flora von China. Palaeontologia
Sinica A 4 (1), 1e69.
Sze, H.C., Lee, H.H., et al., 1963. Fossil Plants of China, 2. Mesozoic Plants
from China. Science Press, Beijing, 429 pp. (in Chinese).
Tralau, H., 1966. Botanical investigations in the fossil flora of Eriksdal in Fyledalen, Scania. Sveriges Geologiska Undersokning C 611 60 (6), 1e36.
Wang, X.L., Wang, Y.Q., Zhang, F.C., Zhang, J.Y., Zhou, Z.H., Jin, F.,
Hu, Y.M., Gu, G., Zhang, H.C., 2000. Vertebrate biostratigraphy of the
Lower Cretaceous Yixian Formation in Lingyuan, western Liaoning and
its neighbouring southern Nei Mongol (Inner Mongolia), China. Vertebrata
PalAsiatica 38, 81e99 (in Chinese, English summary).
Wang, X.L., Zhou, Z.H., Zhang, F.C., Xu, X., 2002. A nearly complete articulated rhamphorhynchoid pterosaur with exceptionally well-preserved
wing membranes and ‘hairs’ from Inner Mongolia, northeast China. Chinese Science Bulletin 47, 226e230.
Wang, Y., 2000. A new salamander (Amphibia: Caudata) from the Early
Cretaceous Jehol Biota. Vertebrata PalAsiatica 38, 100e103 (in Chinese,
English abstract).
Watson, J., Lydon, S.J., Harrison, N.A., 1999. Consideration of the genus
Ginkgoites Seward and a redescription of two species from the Lower
Cretaceous of Germany. Cretaceous Research 20, 719e734.
Wu, S.Q., 1999. A preliminary study of the Jehol flora from western Liaoning.
In: Palaeoworld 11 (Special Issue). Press of University of Sciences and
Technology of China, Hefei. 7e57 (in Chinese, English summary).
Zhang, J.F., 2002. Discovery of Daohugou Biota (pre-Jehol Biota) with a discussion on its geological age. Journal of Stratigraphy 26, 173e177, 215 (in
Chinese, English abstract).
Zhang, W., Zheng, S.L., 1987. Early Mesozoic fossil plants in western
Liaoning, northeast China. In: Yu, X.H., Wang, W.L., Liu, X.T., Zhang,
W. et al. (Eds.), Mesozoic Stratigraphy and Palaeontology of Western
Liaoning, 3 (7). Geological Publishing House, Beijing, pp. 239e338 (in
Chinese, English abstract).
Zhou, Z.H., Barrett, P.M., Hilton, J., 2003. An exceptionally preserved Lower
Cretaceous ecosystem. Nature 421, 807e814.
Zhou, Z.Y., 1991. Phylogeny and evolutionary trends of Mesozoic ginkgoaleans e a preliminary assessment. Review of Palaeobotany and Palynology
68, 203e216.
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
Zhou, Z.Y., 1993. Comparative ultrastructure of fossil and living ginkgoacean megaspore membranes. Review of Palaeobotany and Palynology
78, 167e182.
Zhou, Z.Y., 1994. Heterochronic origin of Ginkgo biloba type ovule organs.
Acta Palaeontologica Sinica 33 (2), 1e9 (in Chinese, English
summary).
Zhou, Z.Y., 1997. Mesozoic ginkgoaleans: a systematic review. In: Hori, T.,
Ridge, R.W., Tulecke, W., Del Tredici, P., Trémouillaux-Guiller, J.,
Tobe, H. (Eds.), Ginkgo biloba e A Global Treasure from Biology to
Medicine. Springer-Verlag, Tokyo, pp. 183e206.
Zhou, Z.Y., 2003. Mesozoic ginkgoaleans: phylogeny, classification and
evolutionary trends. Acta Botanica Yunnanica 25, 377e396 (in Chinese,
English abstract).
361
Zhou, Z.Y., Zhang, B.L., 1988. Two new ginkgoalean female reproductive
organs from the Middle Jurassic of Henan Province. Science Bulletin
(Kexue Tongbao) 33, 1201e1203.
Zhou, Z.Y., Zhang, B.L., 1989. A Middle Jurassic Ginkgo with ovule-bearing
organs from Henan, China. Palaeontographica B 211, 113e133.
Zhou, Z.Y., Zhang, B.L., 1992. Baiera hallei Sze and associated ovule-bearing
organs from the Middle Jurassic of Hunan, China. Palaeontographica B
224, 151e169.
Zhou, Z.Y., Zhang, B.L., Wang, Y.D., Guignard, G., 2002. A new Karkenia
(Ginkgoales) from the Jurassic Yima formation, Henan, China and its megaspore
membrane ultrastructure. Review of Palaeobotany and Palynology 120, 91e105.
Zhou, Z.Y., Zheng, S.L., 2003. The missing link of Ginkgo evolution. Nature
423, 821e822.
Appendix
Measurements of ovulate organs
Specimens
(field or temporary
numbers in
parentheses)
Number
of ovules
visible
PB20242 (821)
PB20240 (822)
PB20239 (823)
PB20243 (824)
PB20238 (825)
PB20209 (826)
PB20245 (827)
PB20210 (830)
PB20211 (831) (peduncle
31 mm 1 mm)
PB20244 (832)
PB20241 (833)
PB20212 (834)
PB20213 (835)
PB20232 (836)
PB20233 (837)
B0174a,b
CZ101 (peduncle
30 mm 1.4 mm)
7
5
3
7
2
3
6
5
7
3
5
6
5
4
6
6
5
Ovule
Stone
shape
Flesh
length
widest part
length
width
width
ovateeelliptical
ovateefusiform
nearly circular
ovateeelliptical
nearly circular
Elliptical
nearly circular
nearly circular
nearly circular
7e9.3
9e11
7e8
8e9
7
12
7
7e7.5
7e7.5
6e9
5e6
6.5e7
6.3e7
6.5e7
11
7
7e7.5
7
7
e
e
7e9
5.5
e
7
7.5
6.5
6.5
e
e
6.3
5
e
6
5.5
4e4.5
2
e
e
0.3e0.7
1e2
e
1
0.5e1.5
0.5
ovateecircular
nearly circular
nearly circular
Ovate
Elliptical
nearly circular
ovateeelliptical
nearly circular
9.5
8e9
6.5
5e6
7e9
7e9
8e9
6e7
7.5e8
8.5
5e6
4e4.5
6.5e8
5e7
7e8.5
5.5e6.5
8
8e8.5
e
5e5.5
7e8
e
e
5.5
5.5
6.5e7
e
3.5e4
5e5.5
e
e
5
0.5e1.5
0.5e1
e
0.5
1e2
e
e
1
(all in mm)
Measurements of associated leaves
Specimens
(field or temporary
numbers in
parentheses)
Morphotype 1
PB20214 (811)
PB20215 (812)
PB20216 (Z01)
PB20217 (Z02)
PB20219 (ZE05)
PB20220 (ZE06)
PB20221 (ZE07)
PB20222 (ZE08)
PB20223 (ZE09)
PB20224 (ZE10)
PB20237 (818)
PB20234 (815)
PB20235 (816)
PB20236 (817)
NEUP0006
Laminae
Segments
Petiole
Number of veins
length
(mm)
width
(mm)
basal angle
(degree)
times of
division
number
widest
part
(mm)
length
(mm)
width
(mm)
per cm
per
segment
13
40
32
19
23
34
45
20
30
40
30
20þ
27
40
49
30
45þ
41
34
68
56
62
29
33
43
50þ
40
50þ
40þ
47
180
90
90
180
200
110
110
110
75
90
220
180
220
90?
90
2
3
2
3
3
3
2
3
3
3
3e4
3
3e4
3e4
3
4
8
4
5
8
6
4
6
6
6
11
6?
10
6?
4
5
6.5
9.5
8
7.5
7.5
13.5
7
6.2
5
5.5
7
6
5.5
11.5
e
15þ
15
e
13
23
25
6.5
15
e
>15
15
>13
e
20
e
1þ
1.4
e
1.7
2.2
1.5
2
1.5
e
2.8
3
1.4
2
2
18e22
16e18
e
10e12
18e20
14
12e14
22
16
14
12e14
16e18
12e14
12
14
8e12
6e7
12e18
8e14
8e12
8e12
14e18
6e12
4e9
7
5e6 (7)
8e10
5e7
(4) 5e7
10e13
(continued on next page)
Z.Y. Zhou et al. / Cretaceous Research 28 (2007) 348e362
362
Appendix (continued )
Specimens
(field or temporary
numbers in
parentheses)
Laminae
Segments
length
(mm)
width
(mm)
basal angle
(degree)
times of
division
Morphotype 2
PB20225 (801)
PB20226 (802)
PB20231 (807)
PB20227 (813)
PB20228 (ZE01)
PB20218 (ZE02)
PB20229 (ZE03)
B0207
40
31
20
25þ
42.5
e
54
30
38
45þ
26
21
60
e
40
32
70
80
130
70
50
40
60
70
3
3
3
3
3
2
3
3
Morphotype 3
B0184
PB20230 (ZE04)
75þ
125
42
55
60
50
3
2
number
Petiole
Number of veins
widest
part
(mm)
length
(mm)
width
(mm)
per cm
per
segment
5
5
6
5
7
4
8
8
4
4.3
2
4
4
3.5
4
3
20þ
18þ
8
e
35
13e35
e
14
1.3e2
1.2
15
1
1.2
0.7e1
e
1.2
15e18
15e18
20
14
16e20
2014e16
18e21
4e6
4e6
4
4e7
4e5
6
2e4
4e5
6
4
6
8.5
50
15e20
2
1
12e15
12e14
4e7
6e13