Download Liaoxia Cao et S.Q. Wu (Gnetales): ephedroids from the Early

Pl. Syst. Evol. 262: 239–265 (2006)
DOI 10.1007/s00606-006-0481-2
Liaoxia Cao et S.Q. Wu (Gnetales): ephedroids from the Early
Cretaceous Yixian Formation in Liaoning, northeastern China
C. Rydin1, S. Q. Wu2, and E. M. Friis1
1
2
Swedish Museum of Natural History, Department of Palaeobotany, Stockholm, Sweden
Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China
Received April 25, 2006; accepted July 24, 2006
Published online: December 1, 2006
Springer-Verlag 2006
Abstract. Gnetalean compression-impression fossils are described from the Early Cretaceous Yixian
Formation, Liaoning Province, north-eastern
China, and assigned to six species of Liaoxia Cao
et S.Q. Wu. The fossils have opposite-decussate
phyllotaxis and cones comprising 2–12 pairs of
bracts. Ovulate cones have seeds typically in a
distal position. The species differ from each other
and from previously described fossils in the absence
or presence of leaves, shape of cones and seeds, and
shape and position of cone bracts. The species of
Liaoxia are probably close relatives of extant
species of Ephedra L., but diagnostic reproductive
details that could confirm this hypothesis are not
preserved. The restricted information in the fossils
and the poorly understood morphological diversity
of extant Ephedra, prevent assignment of the fossils
to any particular subgroup of Ephedra, as well as
an explicit exclusion of them from the extant genus.
Key words: Ephedra, Liaoxia, Gnetales, Yixian
Formation, fossils, Early Cretaceous, China, Jehol
Biota.
Gnetales are a small group of seed plants with
about 65–75 species in three genera (Kubitzki
1990). Gross morphology is uniform within
each genus (Ephedra L., Gnetum L. and the
monotypic Welwitschia Hook. f.), but differs
significantly between the genera and there is
also significant ecological divergence between
the genera with representatives in deserts
(Welwitschia), semiarid habitats (Ephedra)
and tropical rain forests (Gnetum). Based on
these data, and the scattered geographic distribution of the group, it has been suggested
that the Gnetales are ancient with a large
extinct diversity (e.g. Arber and Parkin 1908).
Fossil support for a relictual status of the
group has mainly come from isolated pollen
(Wilson 1962, Traverse 1988, Crane and
Lidgard 1989, Osborn et al. 1993, Crane
1996), but recent findings of mega- and
mesofossils from Lower Cretaceous strata of
Asia, Australia, Europe and North and South
America, with vegetative and reproductive
details preserved, show that the group was
diverse and widespread already in the Early
Cretaceous.
Many of the Early Cretaceous gnetalean
megafossils are ephedroid with striate stems,
more or less reduced leaves, and opposite and
decussate phyllotaxis. Such fossils have been
reported from China (Wu et al. 1986, Cao et
al. 1998, Guo and Wu 2000, Sun et al. 2001,
Tao and Yang 2003, Yang et al. 2005), central
Asia (Krassilov 1982, Krassilov and Bugdaeva
240
C. Rydin et al.: Cretaceous ephedroids from China
1982) and from Australia (Krassilov et al.
1998). There are also many undescribed specimens from China and Brazil (see e.g. Wu et al.
2000, Mohr et al. 2004). Early Cretaceous
mesofossils include coalified seeds with unique
Ephedra characters such as a sclerenchymatic
seed envelope with apical papillae, and in situ
polyplicate pollen (Rydin et al. 2004, Rydin et
al. 2006).
In addition to the ephedroid fossils there
are also a few Early Cretaceous megafossils
that may represent the Welwitschia-Gnetum
clade (Crane and Upchurch 1987, Rydin et al.
2003, Dilcher et al. 2005, Rydin et al unpubl.
data), as well as several gnetalean fossils that
are difficult to assign to any of the extant
lineages (e.g. Krassilov 1982, Krassilov and
Bugdaeva 1982, Krassilov 1986, Krassilov and
Bugdaeva 1988, Duan 1998, Sun et al. 2001).
Further, dispersed seeds and pollen assigned to
the extinct order Erdtmanithecales (Pedersen
et al. 1989, Friis and Pedersen 1996, Kvaček
and Pacltová 2001) are probably related to
Gnetales, but the vegetative morphology of
these plants is unknown.
Pre-Cretaceous evidence of the Gnetales
are mainly dispersed polyplicate ephedroid
pollen (e.g. Wilson 1962), but there are also
several records of megafossils that probably
belong to the Gnetales, for instance Ephedrites
sinensis Wu et al. and E. exhibens Wu et al.
from Early Jurassic deposits in Qinghai, China
(Wu et al. 1986). However, most pre-Cretaceous gnetalean megafossils are difficult to
interpret. The Permian cone Palaeognetaleana
auspicia Wang with in situ polyplicate pollen
(Wang 2004), the Late Triassic plant Dechellyia gormani Ash (Ash 1972), and the
Jurassic Ust-Balej fossils of East Siberia
(Krassilov and Bugdaeva 1988), are all examples of fossils that have been discussed as
putative Gnetales, but for which a precise
systematic affinity remains to be established.
In this study we describe a number of
ephedroid fossils from the Liaoning province
of northeastern China collected in sediments of
the Yixian Formation. The Yixian Formation
and the overlaying Jiufotang Formation com-
prise the Jehol Group, famous for its exceptionally rich biota, which include exquisitely
preserved invertebrates, osteichthyan fish,
amphibians, mammals and reptiles including
feathered dinosaurs and early birds (Chang
et al. 2003). Vigorous collisions of plates in the
western rim of the Pacific resulted in intensive
volcanic activity (Wang et al. 1983) during the
deposition of the Yixian Formation and ash
falls repeatedly entombed organisms present in
the area and effectively prevented scavenging
and bacterial decay. The immediate anoxic
conditions provided by the volcanic ash tuffs
permitted the preservation of original softtissue features and stomach contents (Chen
et al. 1998, Zhou and Zhang 2002); even
questions on the physiology of Cretaceous
vertebrates and of plant-animal interactions
can be addressed (Zhou et al., 2003, and
papers in Chang et al. 2003).
In contrast to the anatomical preservation
of many animals of the Jehol Biota, plant
fossils rarely have cellular details intact. Similar to the slightly younger Crato plants of
Brazil, the Jehol plants are compression or
impression fossils, often with various organs
such as stems, leaves and reproductive structures still attached. In rare cases even whole
plants are preserved providing excellent information on gross morphology. Anatomical
features, however, are rarely preserved (e.g.
Wu 1999, Sun et al. 2001, Chang et al. 2003,
Friis et al. 2003, Leng and Friis 2003) and
tissues are often replaced or filled in with pyrite
framboids and microcrystallines (Leng and
Yang 2003).
The Jehol flora comprises a diverse assemblage of bryophytes, lycopods, sphenopsids,
ferns and various seed plants including many
conifers and rare angiosperms (Sun et al. 1998,
Wu 1999, Sun et al. 2001, Sun et al. 2002, Leng
and Friis 2003, Leng et al. 2003, Wu 2003).
Fossils assignable to the Gnetales (Wu 1999,
Sun et al. 2001, Wu 2003) also show some
diversity and include plants described as
Liaoxia chenii Cao et Wu and Eragrosites
changii Cao et Wu (Cao et al. 1998), Chaoyangia liangii (Duan 1998, later synonym of
C. Rydin et al.: Cretaceous ephedroids from China
241
Gurvanella Krassilov 1982), Ephedrites? elegans Sun et Zheng (Sun et al. 2001), and
Ephedra archaeorhytidosperma (Yang et al.
2005). Dispersed ephedroid pollen are reported
to be rare in the Yixian Formation (Li and Liu
1999, Li 2003), but include striate forms
assigned to Ephedripites and the Welwitschialike Jugella. The fossils described here are
similar to extant Ephedra in gross morphology,
but they usually lack anatomical details and
cannot be assigned unambiguously to extant
Ephedra. The genus Ephedrites Göppert et
Berendt is unsuitable for gnetalean fossils and
we have therefore referred the Jehol ephedroids in this study to the genus Liaoxia Cao
et Wu (Cao et al. 1998).
thus corresponds to Barremian age or possibly
early Aptian according to the most recent International Geographic Chart (Gradstein et al. 2004).
The Jehol plant fossils contain few or no
anatomical details. They were studied using dissecting microscope. No attempts were made to do
SEM. The characters of the fossils were documented by photography and compared with fossils
in the literature. All specimens are located in the
Nanjing Institute of Geology and Palaeontology,
Chinese Academy of Sciences, China.
Materials and methods
The fossils are from two horizons in the Yixian
Formation of Liaoning, northeastern China. The
Yixian Formation comprises four beds (from base
to top: Lujiatun Bed, Jianshangou Bed, Dawangzhangzi Bed, Jingangshan Bed). Specimens
PB20717 – PB20720 are from layer seven of the
Jianshangou Bed, in the Huangbanjigou section,
Beipiao (latitude: 41 37¢ north; longitude: 120 50¢
east, see Chen et al. 2005) and specimens PB20721 –
PB20726 are from layer two of the Dawangzhangzi
Bed in the Fanzhangzi section, Lingyuan (appr.
latitude: 41 10¢ north; longitude: 119 45¢ east, see
Wang et al. 2000). The geology of the two sections
is described by Wang et al. (2000) and Chen et al.
(2005) (see also Chang et al. 2003). The age of the
Yixian Formation has been much debated, but
there is now general acceptance for a mid-Early
Cretaceous age of the sequence (see Zhou et al.
2003). Basal basalts and andesites of the Dawangzhangzi Bed have been dated to approximately
122.5 Myr (Wang and Zhou 2003). 40Ar-39Ar dates
of approximately 125 Myr have been obtained
from analyses of sanidine and biotite crystals from
three different tuff layers in the Jianshangou Bed
(Swisher et al. 1999, Swisher et al. 2002) and an
40
Ar-39Ar date of 128 Myr has been obtained from
basalt-andesite in the lowermost Lujiatun Bed
(Wang et al. 2001). Later 40Ar/39Ar dating of the
Lujiatun Bed suggest that this bed may be younger,
approximately 123 Myr (He et al. 2006). The age of
the base of the Yixian Formation (128–123 Myr)
Results
Formal descriptions. Based on new informative specimens of Liaoxia chenii and other
ephedroid fossils from the Yixian Formation
an emended diagnosis of the genus Liaoxia is
presented, and a new combination, Liaoxia
changii, suggested. Further, four new species
are described and assigned to Liaoxia (Liaoxia
acutiformis, L. robusta, L. elongata, L. longibractea).
Spermatophyta
Order Gnetales
Genus Liaoxia Cao et S.Q. Wu (emend. Rydin,
S.Q. Wu et Friis).
Emended generic diagnosis. Plants similar to
extant Ephedra, with erect, striate stems,
distinct and slightly swollen nodes, and opposite-decussate branching. Leaves linear or
lacking. Reproductive structures forming
cones, sessile to pedunculate, rounded to
obovate to elongate in shape, consisting of
opposite-decussate bracts. Seeds ovoid to elliptic in shape, positioned in axil of cone bracts.
Specimens investigated: PB17800, PB17801,
PB17802,
PB17803,
PB17804,
PB20717,
PB20718,
PB20719,
PB20720,
PB20721,
PB20722, PB20723, PB20724, PB20725, PB20726.
Type species. Liaoxia chenii Cao et S.Q.
Wu (emend. Rydin, S.Q. Wu et Friis)
Synonyms and previously published material.
1998 Liaoxia chenii Cao et S.Q. Wu — Cao et
al., p. 231, plate I:1–2.
242
C. Rydin et al.: Cretaceous ephedroids from China
1999 Liaoxia chenii Cao et S.Q. Wu — Wu p.
21, plate XIV:3, XV:3.
2000 Ephedrites chenii (Cao et S.Q. Wu) Guo
et X.W. Wu — Guo and Wu p. 86, plates I:1–
4, II:1–4.
2001 Ephedrites chenii (Cao et S.Q. Wu) Guo
et X.W. Wu — Sun et al. p. 206, plates 24:2,
64:1, 3–6 (non plate 64:7–9).
2003 Liaoxia chenii Cao et S.Q. Wu — Chang,
p. 174, Fig. 241.
Emended specific diagnosis. As for the
genus with the following distinctions. Branches
c. 0.5–3.0 mm wide, internodes 8–40 mm long.
Leaves 5–20 mm long, with two parallel veins.
Cones obovate, 4–10 mm long, 2–5 mm wide,
with 2–6 pairs of bracts. Cone bracts ovate to
triangular and reflexed, c. 4 mm long, with an
acute to attenuate apex, two parallel veins.
Seeds ovoid to elliptic, c. 1 mm long, c. 0.3–
0.7 mm wide.
Holotype. PB17800 (Fig. 1).
Paratype. PB17801.
Type locality. Near Chaomidian at Shangyuan Village of Beipiao, Liaoning, China.
Stratigraphic position and age. Jianshangou
Bed, Yixian Formation, Early Cretaceous
(Barremian-early Aptian?).
Comments on the type material. The holotype of Liaoxia chenii (PB17800, Cao et al.
1998) (Fig. 1) is a reproductive shoot, c. 9 cm
long. It is clearly ephedroid in gross-morphology with striate stems, 1–3 mm wide. Branching is opposite and decussate with distinct
nodes. Internodes are 8–40 mm long. Leaves
are linear, at least 20 mm long and c. 1–2 mm
wide, probably with two parallel veins. Cones
are 5–10 mm long and 3–4 mm wide, obovate
with 2–6 pairs of reflexed cone bracts, c. 4 mm
long, and ovate with an attenuate apex. Cone
bracts have two parallel veins.
Note that in the description of Ephedrites
chenii in Sun et al. (2001), two additional
specimens (plate 64, Figs. 7–9) are presented.
These fossils may be ephedroid, but they lack
features characterising Liaoxia and are not
included here in the synonymy list of Liaoxia
chenii.
New material of Liaoxia chenii. Specimens
PB20717–PB20718 (Figs. 2–4) from the Huangbanjigou Section, includes two compression
fossils with oxidized organic material. The
specimens show distinct features of Liaoxia
chenii and are here included in this species. In
one specimen the uppermost 5 cm of a
branched plant, c. 13 cm wide, is preserved
(Figs. 3–4). The other specimen is a detached
apical part of a reproductive shoot, 2.5 cm
long (Fig. 2). Stems are erect with 8–17 mm
long internodes, longitudinally striate and
2 mm wide in basal parts and 0.5 mm in upper
parts, thicker at nodes. Phyllotaxis is opposite
and decussate. Leaves are linear (Figs. 2–3), up
to at least 7 mm long and 0.1–0.3 mm wide.
Venation is indistinct, but there are apparently
two parallel veins in each leaf. Cones are
axillary at nodes or terminating branches,
sessile or pedunculate, and obovate to elongate, 4–7 mm long, 2.5–5 mm wide and with
2–6 pairs of bracts. Cone bracts are delicate
and with two veins (Fig. 3). They are narrowly
ovate with an acute to attenuate apex, 3–4 mm
long, about 0.8 mm wide at the base, 0.3
towards the apex, decussately arranged and
often reflexed to a position almost at a right
angle to the cone axis. A few seeds are
preserved in the axils of apical or distal cones
bracts of some cones (indicated by an arrow in
Fig. 3). They are ovoid and 0.9–1.1 mm long
and 0.3–0.7 mm wide. No internal or external
anatomical details are preserved.
Liaoxia changii (Cao et S.Q. Wu) Rydin,
S.Q. Wu et Friis comb. nov.
Basionym. Eragrosites changii Cao et S.Q.
Wu (Cao et al., February 1998. Chinese Sci.
Bull. 43: p. 231, plate II:1–3).
Synonyms and previously published material.
1999 Liaoxia changii Cao et S.Q. Wu — Wu, p.
21, plate XV:1, 4.
2000 Ephedrites chenii (Cao et S.Q. Wu) Guo
et X.W. Wu — Guo et Wu p. 86, plates 1:5–7
and 2:5–8.
C. Rydin et al.: Cretaceous ephedroids from China
243
2001 Ephedrites chenii (Cao et S.Q. Wu) Guo
et X.W. Wu — Sun et al. p. 206, plates 24:4,
64:2.
Emended specific diagnosis. As for the
genus with the following distinctions. Branches
c. 0.3–4.0 mm wide, internodes 8–40 mm long.
Leaves absent. Cones elongate to obovate, 4–
6 mm long, 1.5–3 mm wide, with 6–10 pairs of
bracts. Cone bracts erect to slightly reflexed,
2 mm long, with an acute to obtuse apex.
Seeds ovoid, c. 1 mm long, c. 0.2–0.3 mm
wide.
Holotype. As for the basionym: PB17803
(Fig. II:2, Cao et al. 1998).
Paratypes. PB17802, PB17804 (Fig. 5)
(Figs. II:1, 3, Cao et al. 1998).
Type locality. Near Chaomidian at Shangyuan Village of Beipiao, Liaoning, China.
Stratigraphic position and age. Jianshangou
Bed, Yixian Formation, Early Cretaceous
(Barremian-early Aptian?).
Comments on the type material. The holotype (PB17803) and its counterpart (PB17804,
Fig. 5) are poorly preserved impression fossils,
consisting of several separate branches, not all
in connection. Stems are striate, about 0.5–
4.0 mm wide. Nodes are clearly set and slightly
swollen separated by internodes, about
8–40 mm long. Leaves are absent. Cones are
pedunculate to sessile, 5–6 mm long, 2.5–
3 mm wide. There are 6–10 pairs of bracts in
each cone. Bracts are 2 mm long, with acute to
obtuse apices. No seeds are preserved. Some
cones have slightly reflexed cone bracts, which
might indicate that they are female; others are
more narrowly elongate with erect bracts.
They may represent female cones in different
stages of maturity or alternatively, there may
be a mix of male and female branches on this
slab.
New material of Liaoxia changii. Specimen
PB20722 (Figs. 6–8) from the Dawangzhangzi
Bed at the Fanzhangzi Section is a female
plant that in all characters is indistinguishable
from the type specimen of Liaoxia changii
described above, but is better preserved than
the type material. The specimen has weakly
striate stems with swollen nodes. Stems are
0.7–1.7 mm wide with opposite and decussate
branching and internodes about 10–18 mm.
Leaves are absent (Fig. 6). Cones are slightly
obovate to elongate, pedunculate to nearly
sessile, 5–6 mm long and 2.5–3 mm wide
(Fig. 8). Each cone has 6–10 pairs of erect to
slightly reflexed bracts, 2 mm long, and with
acute to obtuse apices. Impressions of seeds
are observed in the axils of some bracts. Seeds
are c. 0.8–1 mm long, 0.2–0.3 mm wide and
ovoid.
Liaoxia acutiformis Rydin, S.Q. Wu et Friis sp.
nov.
Specific diagnosis. As for the genus with the
following distinctions. Branches 0.3–1.4 mm
thick, leaves 2.7–7.0 mm long, 0.2 mm wide,
probably with two parallel veins. Cones elongate (to narrowly obovate), 3.5–6.0 mm long,
c.1.7–2.7 mm wide, with 6–12 pairs of bracts.
Cone bracts erect to slightly reflexed, 1.5–
2.0 mm long, narrowly ovate with acute apex,
two parallel veins.
Etymology. Named after the acute apex of
the cone bracts.
Holotype. PB20721 (Figs. 9–11).
Locality. Fanzhangzi Section, Lingyuan,
Liaoning, China.
Stratigraphic position and age. Dawangzhangzi Bed, Yixian Formation, Early
Cretaceous (Barremian-early Aptian?).
Description and comments. The type material of Liaoxia acutiformis comprises one
compression fossil of an ephedroid plant with
sparse remains of oxidized organic material
preserved (Fig. 9). No anatomical details are
preserved. The shoot is 7 cm long with opposite and decussate branching. Stems are erect
with weak impressions of longitudinal striations, internodes about 6–14 mm long, stems
0.3–1.4 mm wide, thicker at nodes. Leaves are
linear, and opposite at nodes, 2.7–7.0 mm long
and c. 0.2 mm wide (Figs. 9–11). Indistinct
remains of two veins are present in some leaves
(Fig. 10). There are about seven elongate (to
narrowly obovate) cones, 3.5–6 mm long, and
244
C. Rydin et al.: Cretaceous ephedroids from China
about 1.7–2.7 mm wide. Cones are sessile and
placed axillary at nodes or terminally on
branches. Each cone has between 6 and 12
pairs of erect to slightly reflexed bracts that
appear decussately arranged (Fig. 10). Bracts
are narrow and ovate, 1.5–2.0 mm long, with
an acute apex. Seeds or microsporangiate
organs have not been observed.
This fossil is similar to Liaoxia chenii in
vegetative morphology, but the cones are more
elongate in shape. Liaoxia acutiformis is further
distinguished from L. chenii by having a higher
number of bracts, probably up to 12 pairs, in
each cone, in contrast to L. chenii that has 2–6
pairs in each cone. The apex of the cone bracts
differs in being acute to obtuse in L. acutiformis
while it is acute to attenuate in L. chenii.
senting the central part of the plant (Figs. 12–
13). No anatomical details are preserved.
The stems are erect with nodes and internodes. Branching is opposite and the paratype
has multiple axillary units (Fig. 12). Stems are
0.4–1.5 mm thick, thicker towards the base
and at nodes, and have very weak remnants of
longitudinal striations. Leaves are absent.
Cones are axillary at nodes or terminally on
branches and may be sessile or pedunculate.
They are narrowly elongate (Figs. 13–14) and
vary in length between 5–6 mm in the holotype
to 6–10 mm in the paratype, but are all
2–3 mm wide. One cone on the paratype is
smaller and rounded, c. 3 · 3 mm (arrow in
Fig. 12). Each cone comprises 8–12 pairs of
erect and decussately arranged bracts. The
bracts are probably very narrowly ovate, c.
2.5–4 mm long, with attenuate apex. Seeds or
microsporangiate organs have not been
observed.
These plants are similar to Liaoxia changii
(Cao et al. 1998) in the over all ephedroid
habit, and the leaf-less stems, but differ from
Liaoxia changii mainly in that they have
cones with more bracts, which are erect and
have a distinctly pointed, attenuate apex. The
cone bracts of Liaoxia changii are slightly
reflexed and have a less distinctly pointed,
acute apex.
Liaoxia elongata Rydin, S.Q. Wu et Friis sp.
nov.
Specific diagnosis. As for the genus with the
following distinctions. Branches 0.4–1.5 mm
thick, sometimes with multiple axillary nodes.
Leaves absent. Cones narrowly elongate, 5–
10 mm long, c. 2–3 mm wide, with 8–12 pairs
of bracts. Cone bracts erect, 2.5–4 mm long,
with an attenuate apex.
Etymology. Named after the narrowly
elongated cones.
Holotype. PB20724 (Figs. 14–15).
Paratype. PB20723 (Figs. 12–13).
Locality. Fanzhangzi Section, Lingyuan,
Liaoning, China.
Stratigraphic position and age. Dawangzhangzi Bed, Yixian Formation, Early
Cretaceous (Barremian-early Aptian?).
Description and comments. The holotype of
Liaoxia elongata comprises the uppermost
5.5 cm of the plant (Figs. 14–15). An additional specimen is a shoot with slightly larger
structures, c. 4 cm long and 4 cm wide, repre-
Liaoxia robusta Rydin, S.Q. Wu et Friis sp.
nov.
Specific diagnosis. As for the genus with the
following distinctions. Branches 1.5–2 mm
thick, with multiple axillary units. Leaves at
least 15–20 mm long, 0.5–1.0 mm wide. Cones
obovate to elongate 7–16 mm long, c. 6–8 mm
wide, with 4–10 pairs of bracts. Cone bracts
reflexed, 4–7 mm long, ovate with acute to
attenuate apex, one-two parallel veins. Seeds
c
Figs. 1–4. Liaoxia chenii Cao et S.Q. Wu (emend. Rydin, S.Q. Wu et Friis). 1 The holotype of Liaoxia chenii
(PB17800). 2 New specimen (PB20718); the detached apical part of a reproductive shoot. 3–4 New specimen
(PB20717); the uppermost part of a branched plant. Note the seed and the thin leaf indicated by arrows in
Fig. 3. Scale bars = 1 cm in Figs. 1, 2, 4; 0.3 cm in Fig. 3. S = seed; L = leaf
C. Rydin et al.: Cretaceous ephedroids from China
245
246
C. Rydin et al.: Cretaceous ephedroids from China
rounded, elliptic, 2.5–3.5 mm long, 1.2–2 mm
wide.
Etymology. From the robust morphology
of the plant.
Holotype. PB20719. (Figs. 16, 18).
Paratype. (Counterpart) PB20720. (Fig. 17).
Locality. Huangbanjigou Section, Beipiao,
Liaoning, China.
Stratigraphic position and age. Jianshangou
Bed, Yixian Formation, Early Cretaceous
(Barremian-early Aptian?).
Description and comments. The type material of Liaoxia robusta comprises two compression fossils of an ephedroid, female plant,
part and counterpart, with oxidized organic
material preserved. The shoot is 17 cm long
(Fig. 16), but on the counterpart, only the
uppermost 8 cm are preserved (Fig. 17). No
internal or external anatomical details are
preserved. Precipitations surround the plant
remains and make stems and leaves appear
wider than they are.
Stems are erect with nodes and internodes,
1.5–2 mm thick, thicker at nodes, and have
longitudinal striations-ridges. Phyllotaxis is
opposite and decussate with multiple axillary
units. Leaves are linear, 15–20 mm long and
appear 1.5–2 mm wide, but the width also
comprises precipitates and the leaves were
probably only 0.5–1 mm wide. Indistinct
remains of three or four veins are present on
some leaves. The plant has about 15 ovulate
cones that are rounded to ellipsoid in longitudinal outline. Cones vary in length between 7
and 16 mm, but are all about 6–8 mm wide,
sessile or pedunculate, and are positioned
axillary at nodes or terminally on branches.
Cones comprise between approximately 4 and
10 pairs of reflexed and decussately arranged
bracts. The bracts are ovate, 4–7 mm long,
with a long and acute to attenuate apex. Seeds
are rounded to elliptic, 2.5–3.5 mm long and
1.2–2 mm wide, but no cell structures or other
anatomical details are preserved. There is one
seed in the axil of all cone bracts, including
proximal bracts.
This plant differs from other species of
Liaoxia in that all features are larger. Further,
it has multiple axillary branching, which has
otherwise only been observed for Liaoxia
elongata and L. longibractea, and these species
are clearly different from L. robusta in the
characters of the cones. Liaoxia robusta differs
from Ephedra in the presence of seeds in the
axil of all bracts, not only in distal pairs as in
extant Ephedra.
A detached winged seed occurs in close
association with Liaoxia robusta (Fig. 18).
The seed body of this isolated seed is of
approximately the same length as the in situ
seeds and the possibility that it originates
from a Liaoxia cone cannot be ruled out, but
the shape of the seed and the nature of the
wing suggest that it was more likely produced
by one of the conifers reported for the Yixian
Formation.
Liaoxia longibractea Rydin, S.Q. Wu et Friis
sp. nov.
Specific diagnosis. As for the genus with the
following distinctions. Branches c. 1.5 mm
wide, with multiple axillary branching. Cones
sessile to very shortly pedunculate, rounded,
3.5–4 mm long ()15 mm including bract
apex), c. 2–3 mm wide, with 1–2 pairs of
bracts. Cone bracts reflexed, 10–15 mm long,
extended with a setose apex, two parallel
veins. Seeds elliptic, 2.5–4.0 mm long, c.
1 mm wide.
Etymology. Named after the very long and
narrowly extended cone bracts.
Holotype. PB20725 (Fig. 19).
Paratype. PB20726 (the counterpart,
Fig. 20).
Locality. Fanzhangzi Section, Lingyuan,
Liaoning, China.
Stratigraphic position and age. Dawangzhangzi Bed, Yixian Formation, Early
Cretaceous (Barremian-early Aptian?).
Description and comments. The type material of Liaoxia longibractea comprises two
relatively well-preserved compression fossils
(part and counterpart) with small amounts of
oxidized organic material preserved. No internal or external anatomical details are pre-
C. Rydin et al.: Cretaceous ephedroids from China
247
Figs. 5–8. Liaoxia changii (Cao et S.Q. Wu) Rydin, S.Q. Wu et Friis comb. nov. 5 The counterpart of the
holotype (PB17804). 6–8 New specimen (PB20722); a relatively well-preserved fossil with seeds in the axil of
cone bracts. Leaves are absent in Liaoxia changii. Scale bars = 1 cm in Figs. 5–7; 0.3 cm in Fig. 8. S = seed
248
C. Rydin et al.: Cretaceous ephedroids from China
Figs. 9–11. Liaoxia acutiformis Rydin, S.Q. Wu et Friis sp. nov (PB20721). 9 Overview of this reproductive
shoot. 10 The uppermost cone in close up. No remains of seeds or male structures have been observed in this
specimen. 11 Close up of a node. Scale bars = 1 cm in Fig. 9; 0.3 cm in Figs. 10 and 11. L = leaf; B = branch
served. The shoot is c. 4.5 cm long and
represents the terminal reproductive part of
one branch (Fig. 19). The stem is erect,
1.5 mm thick, and has distinct remnants of
longitudinal striations. Leaves are not present
in the preserved part of the shoot. Reproduc-
C. Rydin et al.: Cretaceous ephedroids from China
249
tive parts are positioned at two nodes separated by a short (6 mm) internode. Branching
is opposite and with multiple axillary units.
Cones are rounded, and vary in length between
3.5 and 4 mm (up to 15 mm long including the
extended bract apex), and are 2–3 mm wide.
Four cones are positioned axillary at the
lowermost node (Fig. 20). They are sessile to
shortly pedunculate. Each cone comprises only
1–2 pairs of bracts, which are reflexed and
decussately arranged. Bracts are probably
ovate, 10–15 mm long and 0.1–0.5 mm wide,
and have a long pointed (setose) apex
(Fig. 20). They have indistinct remains of two
parallel veins (Fig. 20). The upper node comprises sessile cones, densely crowded into a
head-like structure. Seeds are positioned in the
axil of the bracts. They are poorly preserved,
but appear elliptic, 2.5–4 mm long and c.
1 mm wide.
This plant differs from the other species of
Liaoxia in the multiple numbers of sessile
cones at nodes, superficially forming head-like
structures. Another obvious difference is the
extended, very long and narrow apex of the
cone bracts, 10–15 mm long. The bracts of
other species described here are generally only
2–4 mm, (6–7 in L. robusta).
Nomenclatural comments. In 2000, Liaoxia
chenii and Eragrosites changii were re-described jointly as an ephedroid species, Ephedrites chenii (Guo and Wu 2000), based on the
original material of Cao et al. (1998) and one
additional specimen. This taxonomic treatment was followed by Sun et al. (2001), who
based their description on the same specimens
as well as new material. There are, however,
problems with the approach of joining Liaoxia
chenii and Eragrosites changii into a single
species. The specimens originally described as
Liaoxia chenii have a distinct ephedroid habit
with opposite branching, long slender leaves in
opposite and decussate arrangement at the
nodes, and cone bracts with a distinctly
pointed apex (referred to as an ‘‘awn’’ by
Cao et al. 1998). Eragrosites changii (Cao et al.
1998) also represents a plant with an ephedroid
habit, but it differs from Liaoxia chenii in that
leaves are absent, cones have more bracts and
the bracts are shorter, apparently with an
acute to obtuse apex. We find these differences
sufficiently marked to warrant a separation of
the specimens into two different species.
Further, the use of the genus Ephedrites is
inappropriate for ephedroid fossils. The genus
was originally described by Göppert and
Berendt (1845), based on stems with female
reproductive units preserved in Baltic amber
from the Early Cenozoic of Europe. Additional material, including male structures,
convinced Göppert that these plants belonged
to Ephedra (Göppert 1853) and he transferred
the type species (Ephedrites johnianus) to the
extant genus (Göppert 1853, Göppert and
Menge 1883). A few years later, Conwentz
(1886) argued that the male structures probably represented poorly preserved material of
Castanea whereas the female structures (the
type) belonged to the angiosperm family
Loranthaceae and he transferred Ephedra
(Ephedrites) johnianus to Patzea johnianus
(Conwentz 1886).
In 1891, Saporta made an emended diagnosis of Ephedrites (citing the Göppert and
Berendt type material from 1845). He included
two species: one new species based on seeds
Discussion
The type species, Liaoxia chenii, was originally
described as an angiosperm (Cyperaceae) by
Cao et al. (1998). In the same work Cao et al.
described another species, Eragrosites changii,
also assigned to the monocots (Poaceae). The
gnetalean affinity of these two species was,
however, soon pointed out by several authors
(Sun et al. 1998, Guo and Wu 2000). Both
species are here assigned to Liaoxia. We have
altered the terminology but basically followed
the original interpretations made by Cao and
Wu, with one exception. In the original
description of Liaoxia it is stated that the cone
bracts (‘‘glumes’’) are helically arranged (Cao
et al. 1998), but according to our observations
cone bracts are opposite and decussately
arranged.
250
C. Rydin et al.: Cretaceous ephedroids from China
Figs. 12–15. Liaoxia elongata Rydin, S.Q. Wu et Friis sp. nov. 12–13 The central part of the plant is preserved
in this specimen (PB20723). Note the narrowly elongated cones with erect bracts, and a single, smaller and
rounded, probably immature cone. 14–15 The uppermost part of a reproductive shoot (PB20724). Leaves are
absent in this species. Scale bars = 1 cm in Figs. 12 and 15; 0.3 cm in Figs. 13 and 14. C = cone
from the Jurassic of France (Ephedrites armaillensis Saporta), and Ephedrites antiquus,
described by Heer (1876) based on Jurassic
fossils from Ust-Balej, Siberia. Since then,
several authors have used Ephedrites in the
sense of Saporta (1891), (e.g. Wu et al. 1986,
Guo and Wu 2000, Sun et al. 2001), (see also
Table 1). The original description of Ephedrites
(Göppert and Berendt 1845) is, however, validly published and Ephedrites Saporta (1891) a
later illegitimate homonym. A further complication is that the affinity to Ephedra of the
material described by Saporta and Heer has
been questioned (Arber and Parkin 1908,
Krassilov and Bugdaeva 1988), even by Saporta himself (1891, p. 23). Krassilov and Bugdaeva (1988) re-described the winged seeds of
Ephedrites antiquus Heer as parts of a possibly
welwitschioid plant: Heerala antiqua (Heer)
comb. nov. (Krassilov and Bugdaeva 1988).
Thus, Ephedrites Göppert et Brendt is the
basionym of an angiosperm and should not be
used for ephedroid fossils. Conservation of the
homonym Ephedrites Saporta would be possible, but is problematic because of the uncertain
affinity of the fossil material cited by Saporta
(Saporta 1891, p. 23 and 26). These issues have
also been discussed by Yang et al. (2005).
Location
Detached seeds or fruits,
opposite with one flat side
Reproductive branches
Detached leafless branches
Detached seeds or fruits,
opposite with one flat side
Detached winged
seeds or fruits
Reproductive branches
preserved in amber
Description
The type of Ephedrites.
Belongs to Loranthaceae
(Conwentz 1886).
Branches and seeds-fruits of uncertain
affinity. The winged
seeds re-described as
Heerala antiqua.
(Krassilov and Bugdaeva 1988), as
welwitschioid seeds.
Of uncertain affinity.
Comments
The material belongs to
two separate species, previously
described as Liaoxia chenii
and Eragrosites changii
(Cao et al. 1998).
Ephedrites? elegans
Yixian Formation, Early
Reproductive shoot with
Cones (spikes) with bracts at ‘‘nodes’’,
(Sun et al. 2001)
China
Cretaceous
three cones
separated by ‘‘internodes’’
No leaves or nodes preserved Similar to the ‘‘Potamogeton-like
spikes’’ from Manlej (Krassilov 1982).
Ephedrites guozhongiana
Yixian Formation, Early
Vegetative shoot
Strictly dichotomously branched.
(Sun et al. 2001)
China
Cretaceous
Not Gnetales, perhaps
not a seed plant.
Europe
Oligocene-Miocene Reproductive branches
Not Gnetales. Commented e.g. by
Ephedra mengeana
(Göppert and Menge 1883)
preserved in
Conwentz (1886) and Arber
amber
and Parkin (1908).
Not Ephedra. Has been
Ephedrites sotzkianus
Europe
Eocene
Vegetative branches;
commented e.g. by Saporta (1891)
(Unger 1851)
fragmented and probably
and Arber and Parkin (1908).
poorly preserved.
Alternate branching
Xiaomeigou
Jurassic
Reproductive branches,
Fossils with affinity to Ephedra.
Ephedrites sinensis and
Formation, China
fragmented
No reproductive details preserved.
E. exhibens
(Wu et al. 1986)
Jurassic
Europe
Ephedrites armaillensis
(Saporta 1891)
Ephedrites chenii
(Guo and Wu 2000)
Yixian Formation, Early
China
Cretaceous
Jurassic
Sibiria
(Ust-Balej)
OligoceneMiocene
Age
Ephedrites
antiquus (Heer 1876)
Ephedrites johnianus
Europe
(Göppert and Berendt 1845)
Reference
Table 1. Fossil material assigned to Ephedrites
C. Rydin et al.: Cretaceous ephedroids from China
251
252
C. Rydin et al.: Cretaceous ephedroids from China
C. Rydin et al.: Cretaceous ephedroids from China
253
Considering the nomenclatural problems with
the taxon Ephedrites and the difficulty to
unambiguously correlate the present material
with extant Ephedra, we prefer to keep the
name Liaoxia, and suggest that Liaoxia is used
for Ephedra-like megafossils that cannot be
unambiguously assigned to the extant genus.
Interpretation of the new fossils and
comparison with extant species. The material
presented here comprises impression-compression fossils with remains of oxidized organic
material. Most specimens have stems, leaves,
and cones in connection, but none of the fossils
is preserved as whole plants and none has
roots attached. No anatomical details are
preserved. Characters are summarised in
Table 2. The reconstruction of Liaoxia chenii
(Fig. 21) is based on the holotype (PB17800)
and the new specimens (PB20717–PB20718).
Vegetative characters of Liaoxia. The fossils have erect stems, which are longitudinally
striate probably from preserved fibers. Upper
parts are thinner than the basal parts and in all
species the stems become wider at the nodes.
Liaoxia robusta is larger than the other species
and has the widest stems, but the variation is
generally larger within each plant than
between them.
Leaves are absent in Liaoxia changii and L.
elongata; leaf scars are missing in all specimens. In Liaoxia longibractea, only the uppermost part of a reproductive shoot is preserved
and it is unknown whether or not it had leaves.
The other species all have narrow, linear
leaves, opposite at nodes. The leaf bases are
probably sheeted in all the species, but the
poor preservation prevents unambiguous conclusions. The venation is also generally poorly
preserved, but obvious in at least some parts of
the leaves. In all species there is a primary
parallel venation and no second order venation. Liaoxia chenii and L. acutiformis appear
to have two parallel veins. Liaoxia robusta has
four veins.
In extant Ephedra, the size and shape of
leaves and stems may vary significantly within
and between species (Gifford and Foster 1989)
and the variation in the fossils is covered in the
extant genus. For example, Ephedra leaves are
generally minute (less than 10 mm long), ovate
to triangular in shape, but Ephedra foliata has
linear leaves with a well-developed lamina,
often 10–15 mm long, sometimes extending up
to 40 mm in length (Freitag and Maier-Stolte
1994). Leaves of Ephedra have 2–3 parallel
veins (Kubitzki 1990). Second order venation
is unknown in Ephedra, but occurs in Gnetum
and Welwitschia.
Cones and cone bracts of Liaoxia. The
cones of Liaoxia chenii and L. robusta are
obovate and wide, whereas the cones of L.
acutiformis and L. changii are elongate to
slightly obovate. Cones of L. elongata are
narrowly elongate, but one of the cones of L.
elongata has a distinctly different shape and is
smaller and rounded. It was probably preserved in an immature stage. In L. longibractea, the cones are rounded to obovate and
several cones are densely crowded at nodes,
forming a head-like structure. Multiple axillary
branching resulting in four or more cones at a
node is obvious in Liaoxia robusta, L. longibractea and L. elongata, and this feature is also
common in extant Ephedra. Presence of multiple axillary buds is a synapomorphy for the
Gnetales (Crane 1996, Doyle 1996).
Liaoxia chenii has 2–6 pairs of ovate to
triangular cone bracts with a pointed apex.
b
Figs. 16–20. Liaoxia robusta Rydin, S.Q. Wu et Friis sp. nov. and Liaoxia longibractea Rydin S.Q. Wu et Friis
sp. nov. 16–18 Liaoxia robusta sp. nov (PB20719–PB20720); a large species with preserved seeds, also in the axil
of proximal cone bracts. Leaves and stems are surrounded by precipitations that make them appear wider than
they are. 19–20 Liaoxia longibractea sp. nov. (PB20725–PB20726); the uppermost part of a reproductive shoot.
It is unknown if this species had leaves or not. Note the spectacular cone bracts, and the densely crowded cones
that form head-like structures. Scale bars = 1 cm in Figs. 16–20. S = seed; L = leaf
4–6
2–3
Sessilepedunculate
2–6;
reflexed
3–4
?a
Ovate (to
triangular)
Acute to
attenuate
?
?
?
?
Female
5–10
3–4
Sessilepedunculate
2–6;
reflexed
4
0.6
Ovate (to
triangular)
Acute to
attenuate
2 parallel
?
?
?
Female
Cone length
Cone width
Cone attachment
Bract length
Bract width
Bract shape
Bract
venation
Seed shape
Seed length
Seed width
Gender
Bract apex
No. of
bract pairs
–
Opposite
No
c. 12
0.5–1.5
Linear
5
0.1–0.3
?
Obovate
Ovoid-elliptic
1
0.3–0.7
Female
3–4
0.3–0.8
Ovate (to
triangular)
Acute to
attenuate
2 parallel
4–6
2.5–5.0
Sessilepedunculate
2–6;
reflexed
Figs. 3–4
Opposite
No
8–17
0.5–2.0
Linear
7
0.1–0.3
2?
Obovate
?
?
?
Female
4
0.5
Ovate (to
triangular)
Acute to
attenuate
2 parallel
2–6;
reflexed
5–7
3–4
Pedunculate
Fig. 2
Opposite
No
?
0.5–1.5
Linear
5
0.3
2
Obovate
?
?
?
Male?
?
Figs. 9–11
Opposite
No
6–14
0.3–1.4
Linear
2.7–7.0
0.2
2?
Elongate
(to narr.
obovate)
3.5–6.0
1.7–2.7
Sessilepedunculate
6–12;
erect-slight.
reflexed
1.5–2.0
?a
Narrowly
ovate
Acute
—
—
—
Male?
?
2.5–3.5
?a
Narrowly
ovate
Attenuate
5–6
2
Pedunculatesessile
8–10; erect
Figs. 14–15
Opposite-decussate
No
9–13
0.4–1.0
Absent
—
—
—
Elongate
Liaoxia
Liaoxia chenii Liaoxia chenii Liaoxia chenii Liaoxia acutiformis Liaoxia
chenii PB17800 PB17801
PB20717
PB20718
PB20721
elongata PB20724
Holotype
Paratype
New material New material New material
New material
Photo
Fig. 1
Branching
Opposite
Multiple axillary b. No
Internode length
8–40
Stem width
1–3
Leaf shape
Linear
Leaves length
20
Leaves width
1
Leaf venation
2?
Cone shape
Obovate
Unit: mm.
Table 2. Species of Liaoxia
—
—
—
Male?
?
4
?a
Narrowly
ovate
Attenuate
(3-)6–10
3
Sessilepedunculate
10–12; erect
Figs. 12–13
Opposite
Yes
?
0.5–1.5
Absent
—
—
—
Elongate
Liaoxia elongata
PB20723
New material
254
C. Rydin et al.: Cretaceous ephedroids from China
No?
8–40
0.5–4.0
Absent
—
—
—
Elongateobovate
5–6
2.5–3.0
Sessilepedunculate
6–10; erectslightly
reflexed
2
0.3
Ovate
Acute to
obtuse
?
—
—
—
Mix?
Multiple axillary b.
Internode lenght
Stem width
Leaf shape
Leaves length
Leaves width
Leaf venation
Cone shape
Cone width
Cone attachment
length
width
shape
apex
2.5–3.0
Sessilepedunculate
6–10; erectslightly
reflexed
2
0.3
Ovate
Acute to
obtuse
?
—
—
—
Mix?
No?
8–40
0.5–4.0
absent
—
—
—
Elongateobovate
5–6
Fig. 5
Opposite
1.5–2.0
Sessilepedunculate
c. 8; erectslightly
reflexed
2
0.3
Ovate
Acute to
attenuate
?
?
1
0.2–0.3
Female (mix?)
No?
10
0.3–0.8
absent
—
—
—
Elongateobovate
4–5
–
Opposite
2.5–3.0
Sessilepedunculate
6–10; erectslightly
reflexed
2
?a
Ovate
Acute to
obtuse
?
Ovoid
0.8–1.0
0.2–0.3
Female
Figs. 6–8
Oppositedecussate
No
10–18
0.7–1.7
absent
—
—
—.
Obovate
to elongate
5–6
4–7
?a
Ovate
Acute to
attenuate
1–2 parallel?
Rounded-elliptic
2.5–3.5
1.2–2.0
Female
6–8
Sessilepedunculate
4–10; reflexed
Yes
15–40
1.5–2.0
Linear
15–20
0.5–1.0
3–4
Obovate
to elongate
7–16
Figs. 16–18
Opposite
2 parallel
Elliptic
2.5–4.0
c. 1.0
Female
10–15
0.1–0.5 apically
Ovate?
Setose
3.5–4 ()15
including
bract apex)
2–3
Sessile- shortly
pedunculate
1–2; reflexed
Yes
6
1.5
?
?
?
?
Rounded
Figs. 19–20
Opposite
Notes. All units in mm. —: Feature absent. ?: Feature poorly preserved. a: Bracts folded and overlapping; exact width not possible to say.
Bract venation
Seed shape
Seed length
Seed width
Gender
Bract
Bract
Bract
Bract
Bract pairs;
position
Cone length
–
Opposite
Photo
Branching
C. Rydin et al.: Cretaceous ephedroids from China
255
256
Fig. 21. Reconstruction of Liaoxia chenii, Cao et
S.Q. Wu (emerd. Rydin, S.Q. Wu et Friis) based on
the holotype (PB17800) and the new specimens
(PB20717–PB20718). Drawing by Pollyanna von
Knorring. Scale bar = 1 cm
The cones of L. acutiformis and L. changii
contain more bracts (6–12 in the former, 6–10
in the latter), but each bract is smaller and has
a less distinctly pointed, acute apex. In L.
elongata the cones have c. 10 pairs of pointed,
narrowly ovate bracts. Several cones of Liaoxia robusta have approximately 4 pairs of
cone bracts but there are also larger cones with
up to 10 bract pairs. The cones of L. longibractea consist of only 1–2 pairs of bracts,
which are very long and conspicuous with their
extended, narrow apex. They are unique
among ephedroid plants, we have not seen
anything similar in any living or fossil species.
C. Rydin et al.: Cretaceous ephedroids from China
The cones of extant Ephedra are compound, consisting of cone bracts and seeds
with extra-integumentary structures of bract
(leaf) origin (Pearson 1929, Crane 1985, Takaso 1985, Pedersen et al. 1989, Yang 2001,
2004). Our interpretation is that the cones of
Liaoxia are also compound with the same
structural arrangement as those of Ephedra,
but the preservation of the material prevents
unambiguous conclusions. Ephedra cones are
generally composed of 2–8 pairs of bracts,
sometimes more. This is in agreement with the
condition in the fossil species, even though the
large specimen of L. elongata has more bracts
than usually seen in extant Ephedra. Many
extant species have obovate to rounded cone
bracts with an obtuse or rounded apex, but
ovate bracts with a pointed apex also occur in
some species.
Seeds. Seeds are preserved as compressions
or impressions in several of the fossils, even
though no anatomical details are preserved.
Like extant Ephedra, Liaoxia chenii has seeds
only in the axil of distal bract. The cone bracts
are delicate and were probably membranous,
not fleshy. They are often fully reflexed, and
several cones seem to lack seeds, indicating
wind dispersal and preservation at a late stage
in the reproduction phase. Delicate cone bracts
with two veins that become reflexed at seed
maturity can for instance be seen in the
African species Ephedra alata.
Contrary to the cones of Liaoxia chenii and
extant Ephedra, the cones of L. changii, L.
robusta and L. longibractea appear to have a
seed in the axil of most bracts, also in proximal
part of the cones. This is interesting as it differs
significantly from Ephedra, which has seeds
mainly in a distal position, but is more similar
to Welwitschia where seeds also occur proximally in the cone. This is conceivably an
ancestral state present in some of the Cretaceous fossils and retained in Welwitschia, (but
see also the discussion below on the distinction
between ephedroid and welwitschioid fossils).
In Liaoxia chenii and L. changii, the seeds
are ovoid to elliptic and small. In Liaoxia
robusta, and L. longibractea they are rounded
C. Rydin et al.: Cretaceous ephedroids from China
257
to elliptic and larger, but all the fossil seeds are
much smaller than seeds of extant Gnetales.
Seeds of Ephedra are at least 6–7 mm long
whereas the fossils are only 1–4 mm. The small
size of the fossil seeds is, however, in accordance with other ephedroid seeds from the
Early Cretaceous described from Portugal and
North America (Rydin et al. 2004, Rydin et al.
2006).
Gender. Most species of Ephedra are dioecious with male and female reproductive parts
on separate plants. Male cones often comprise
more bracts than female cones of the same
species and the shape of male and female cone
bracts may differ within a species. All Liaoxia
specimens currently known have only one kind
of cones and we therefore assume that these
ephedroid fossils were also dioecious. Liaoxia
chenii, L. changii, L. robusta and L. longibractea are clearly female plants. Their cone bracts
are reflexed and seeds are present in the axil of
bracts. In contrast, Liaoxia acutiformis and L.
elongata have bracts that are more erect and
without remains of seeds or microsporangiophores. The poor preservation makes interpretation of reproductive details difficult, but the
absences of seeds and the erect position of the
cone bracts might suggest that L. acutiformis
and L. elongata represent male plants. Male
organs of extant Ephedra generally detach
easily, shortly after pollination, which may
explain the absence of preserved microsporangia in these putatively male plants.
Because the Early Cretaceous ephedroids
are interpreted as dioecious, it is possible that
the putatively male specimens actually belong
to the same species as one or two of the female
specimen. To explicitly correlate female and
male plants would require epidermal or other
cellular details not present in this material. It
is, however, interesting to note that Liaoxia
acutiformis is vegetatively closely similar to L.
chenii, but differs in the number and shape of
the cone bracts. Liaoxia acutiformis may be
very closely related to L. chenii, speculatively,
the male plant of L. chenii. Similarly, Liaoxia
changii and L. elongata are vegetatively similar, both lacking leaves, but differ in shape of
cones and cone bracts. Both species have been
found in the Fanzhangzi Section in Lingyuan
and, again speculatively, Liaoxia elongata
could be the male plant of Liaoxia changii.
Other gnetalean fossils from eastern
Asia. Several ephedroid fossils, other than
those described here, have been reported from
China and else where (Table 3). Among them
are Ephedrites sinensis and Ephedrites exhibens
(Wu et al. 1986) from the Jurassic Xiaomeigou
Formation of Qinghai. The fossils are fragmentarily preserved and difficult to compare
with the present material, but they seem to
differ from Liaoxia species in having only a
single pair of seeds and bracts.
Alloephedra xingxuei (Tao and Yang 2003)
from the Dalazi Formation, China, is an
Early Cretaceous fossil interpreted as a close
relative of Ephedra. However, the nature of
branching and reproductive structures is not
fully clear from descriptions and illustrations
and there are features that are not compatible
with the Gnetales (e.g. possibly alternate
branching).
Ephedra archaeorhytidosperma (Yang et al.
2005), collected from the Jianshangou Bed that
also contains Liaoxia chenii and L. robusta, is
clearly ephedroid with striate stems, opposite
branching, terminal female cones consisting of
1–2 seeds with extended micropylar tubes and
bracts or bract scars. Ephedra archaeorhytidosperma differs from most of the Liaoxia species
presented here in that each cone consists of
only 1–2 seeds and bract pairs, whereas the
Liaoxia fossils have cones with more bracts.
Liaoxia longibractea has cones with few bracts
but the very long and narrowly extended cone
bracts of L. longibractea are very different
from those of Ephedra archaeorhytidosperma.
The material of Ephedra archaeorhytidosperma
comprises one associated triangular leaf, which
is poorly preserved and not clearly attached to
the specimen. There is no evidence of leaves at
the nodes. Thus Ephedra archaeorhytidosperma
may lack leaves, as do some species of Liaoxia.
Sun et al. (2001) described two new species
of ephedroid fossils from the Yixian Formation of Liaoning. Branching in Ephedrites
Early
Cretaceous
Early
Cretaceous
Early
Cretaceous
Early
Cretaceous
Early
Cretaceous
Early
Cretaceous
Early
Cretaceous
Dalazi Formation, China
Manlaj, Mongolia
Yixian Formation, China
Potomac Group, North
America
Buarcos, Portugal
Buarcos, Portugal
Yixian Formation, China
Yixian Formation, China
Alloephedra xingxuei
(Tao and Yang 2003)
‘‘Cyperacites sp.’’ plate 20,
figs. 240–243
(Krassilov 1982)
Ephedra archaeorhytidosperma
(Yang et al. 2005)
Ephedra drewriensis
(Rydin et al. 2006)
Ephedra portugallica
(Rydin et al. 2006)
Ephedrispermum lucitanicum
(Rydin et al. 2006)
Ephedrites chenii (Guo and Wu 2000).
(Synonym of Liaoxia chenii
Cao et al., 1998)
Ephedrites? elegans (Sun et al. 2001)
Early
Cretaceous
Age
Location
Reference
Table 3. Fossils with affinity to Ephedra
Reproductive
shoot
Reproductive
shoots
Coalified seeds
Coalified seeds
Coalified seeds
Reproductive
shoot
Reproductive
shoot
Reproductive
shoot
Description
Plant with an ephedroid habit,
but is interpreted as having
alternate branching, which is
otherwise unknown in the
Gnetales.
Ephedroid plant similar to
Liaoxia, but appears to have
longer or distinctly pointed
cone bracts.
Well-preserved Ephedra-fossil,
with vegetative and reproductive
parts in connection. The large
‘‘mature’’ cone is detached and
could potentially belong to another species.
Well-preserved Ephedra seeds
with anatomical details and in
situ pollen.
Well-preserved Ephedra seeds
with anatomical details and in
situ pollen.
Well-preserved ephedroid seeds
with anatomical details and in
situ pollen.
The material belongs to two separate species, previously described as Liaoxia chenii and
Eragrosites changii (Cao et al.
1998).
Similar to the ‘‘potamogeton-like
spikes’’ from Manlej (Krassilov
1982). No leaves or nodes preserved. Cone (spike) with bracts
at ‘‘nodes’’, separated by
‘‘internodes’’.
Comments
258
C. Rydin et al.: Cretaceous ephedroids from China
Early
Cretaceous
Koonwarra Bed, Australia
Yixian Formation, China
Manlaj, Mongolia
Crato Formation,
South America
Leongathia elegans
(Krassilov et al. 1998)
Liaoxia chenii (Cao et al. 1998)
‘‘Potamogeton-like spike’’
(Krassilov 1982)
Undescribed fossils (see e.g.
Mohr et al. 2004)
Early
Cretaceous
Early
Cretaceous
Early
Cretaceous
Early
Cretaceous
Yixian Formation, China
Eragrosites changii (Cao et al. 1998)
Early
Jurassic
Xiaomeigou Formation, China
Ephedrites sinensis and E. exhibens
(Wu et al. 1986)
Reproductive
shoots
Reproductive
‘‘spike’’
Reproductive
shoot
Vegetative
shoot fragments
Reproductive
shoot
Reproductive
shoot fragments
Plants with affinity to Ephedra,
no reproductive details preserved.
Plant with affinity to Ephedra,
initially described as an angiosperm. Leaves absent.
Initially thought to be an angiosperm, later described as Phyllotheca wonthaggiensis
(Sphenopsida) (Drinnan and
Chambers 1986). Suggested to
be ephedroid by Krassilov et al
(1998).
Very similar to extant Ephedra,
but no anatomical details or in
situ pollen. Initially described as
an angiosperm.
Cones (spikes) with bracts at
‘‘nodes’’, separated by ‘‘internodes’’, similar to Ephedrites?
elegans.
The material indicates that
ephedroid plants were present in
north-western Gondwana.
C. Rydin et al.: Cretaceous ephedroids from China
259
260
C. Rydin et al.: Cretaceous ephedroids from China
guozhongiana Sun et Zheng (Sun et al. 2001)
appears to be strictly dichotomous and, as a
consequence of the absence of overtopping, all
branches are of about equal length. Such a
branching pattern is unknown for the Gnetales
and other seed plants, and the affinity of
Ephedrites guozhongiana to Gnetales uncertain. Ephedrites? elegans Sun et Zheng (Sun et
al. 2001) was based on a reproductive branch
from the Yixian Formation. Sun et al. (2001)
included in this species a fossil previously
described as ‘‘Potamogeton-like spike’’ from
the Early Cretaceous of Mongolia (Krassilov
1982). The Chinese fossil has two lateral and
one terminal reproductive axes subtended by a
pair of linear leaves. Reproductive axes comprise c. 5 pairs of broadly ovate leaves or
bracts with a pointed apex and 2–3 distinct
veins. They are similar to the cones of Liaoxia,
but differ in having distinct internodes between
the bract pairs. The ‘‘Potamogeton-like spike’’
from Mongolia consists of a single spike with
five nodes separated by prominent internodes.
At each node there are 2–3 ‘‘nutlets’’ apparently subtended by bracts with a pointed apex.
Ephedrites? elegans and the ‘‘Potamogeton-like
spike’’ from Mongolia show some resemblance
to Ephedra and welwitschioid fossils in the
striate stems and linear leaves present at least
in the Chinese fossil. However, spikes with
distinct and clearly definable internodes and
reproductive structures at nodes are characteristic for extant Gnetum, and are not seen in
Ephedra and Welwitschia.
Yabe and Endo (1935) described fossils
from Lingyuan as possible members of the
extant angiosperm genus Potamogeton. Later
these fossils were transferred to Ranunculus
(Miki 1964), but Guo and Wu (2000) suggest
that they are related to Ephedra, and Sun et al.
(2001) included them in Ephedrites chenii
(Liaoxia chenii). The published figures (Yabe
and Endo 1935, Figs. 1–3) indicate a vegetative morphology similar to that of Liaoxia, but
show differences in reproductive structures.
Unfortunately, however, there are no details of
the fossils that could be used for comparative
studies.
A possible member of Liaoxia is ‘‘Cyperacites sp.’’ from Mongolia (Krassilov 1982),
characterised by having ‘‘a terminal cyme of
three spike-like structures’’ and ‘‘at the base of
the cyme three hair-like appendages’’. Like
Liaoxia chenii it was originally interpreted as
member of the angiosperm family Cyperaceae,
but it is most likely a gnetalean plant. The
‘‘cymes’’ are similar to cones of Liaoxia, and
apparently composed of acuminate bracts. The
‘‘hair-like’’ structures at the base of the cyme
are probably the veins of two opposite leaves,
one preserved vein of the right leaf, and two
preserved veins of the left leaf.
Phylogenetic implications. The vegetative
characters of the fossils presented here (opposite and decussate phyllotaxis, linear leaves
positioned at distinct nodes separated by long
internodes, parallel venation), in combination
with the reproductive characters (seeds in the
axil of cone bracts in decussate arrangement)
exclude a relationship to any other group than
the Gnetales. Within the Gnetales, Liaoxia are
similar to Ephedra in gross morphology, but
several of these characters (elongated leaves
with parallel venation, cones consisting of
oppositely arranged cone bracts with axillary
seeds) are not unique to Ephedra, but occur
also in Welwitschia. The presence of seeds
inside most cone bracts in the cones of Liaoxia
robusta and Liaoxia changii, would even
suggest a closer affinity to Welwitschia.
Considering only extant species, it may
seem easy to distinguish between Ephedra and
Welwitschia, but among Cretaceous plants,
this distinction is not always straightforward.
For example, Gurvanella first described from
the Early Cretaceous of Mongolia (Krassilov
1982) and later also reported from the Yixian
Formation in Liaoning (as Chaoyangia Duan,
1998), has an ‘‘ephedroid’’ vegetative habit
with opposite branching, striate stems and
linear leaves with parallel venation. However,
the seeds are surrounded by a distinct wing, in
gross morphology similar to the seed wing of
Welwitschia. The venation of the Gurvanellawing has dichotomies and anastomoses, which
is unknown in Ephedra, but present in leaves
C. Rydin et al.: Cretaceous ephedroids from China
261
and cone bracts of Welwitschia (Rodin 1953,
1958).
Yang et al. (2005) argued that Chaoyangia
shares most of its characters with Ephedra, and
Zhou et al. (2003) maintained that the combination of ephedroid and welwitschioid characters in Gurvanella (Chaoyangia) supports a
closer relationship between Ephedra and Welwitschia than currently suggested based on
molecular data (see for example studies by
Magallón and Sanderson 2002, Rydin et al.
2002, Burleigh and Mathews 2004). However,
the similarities between Ephedra and Welwitschia are non-informative plesiomorphic features, and the same is probably true for the
similarities between Ephedra and Gurvanella
(Chaoyangia). Like Drewria potomacensis
Crane et Upchurch (Crane and Upchurch
1987), Welwitschiostrobus murili (Dilcher et
al. 2005) and several undescribed Crato plants
(Barbara Mohr personal communication),
Gurvanella (Chaoyangia) possesses uniquely
derived characters of Welwitschia, but has also
retained primitive vegetative habits with opposite branching and phyllotaxis, swollen nodes
and linear leaves with parallel venation, closely
resembling that of Ephedra. These characters
are general features of the Gnetales; several of
them are in fact also present in Gnetum. It has
for example been shown that the ‘‘reticulate’’
venation pattern in Gnetum actually develops
from parallel venation, and is a result of
successive dichotomies in 5–10 parallel veins
located in the centre of the leaf (Rodin 1967).
Apart from molecular data, there are
several morphological synapomorphies that
support the Gnetum-Welwitschia clade (second
order venation, paracytic stomata, astrosclerids, embryo feeder etc, see e.g. Crane 1985,
Doyle 1996), and the sister relationship between Gnetum and Welwitschia is thus well
corroborated. The fossils of Liaoxia do not
possess any of the features characterizing this
clade and we therefore exclude a close relationship to Welwitschia (and the GnetumWelwitschia crown group as a whole).
We hypothesize that the species of Liaoxia
are most closely related to Ephedra among
extant plants, perhaps even nested within
Ephedra, but unambiguous support for this
suggestion is not available. Synapomorphies
for Ephedra mainly constitute structural details
of the seed envelope and pollen grains, not
preserved in this type of material. Therefore, it
cannot be fully ruled out that the Liaoxia
fossils could represent ephedran or gnetalean
stem lineage(s). Resolving higher level relationships among species of Liaoxia, Ephedra
and ephedroid fossils in the literature is a
challenging task for the future.
Conclusions
The Ephedra-like fossils discussed in this paper
have been assigned to the genus Liaoxia,
previously established by Cao et al. (1998).
New material of six species, of which four are
new, is presented. The features of the fossils
exclude a relationship to any other group than
the Gnetales. Within the Gnetales, a relationship to the Gnetum-Welwitschia clade can be
excluded, however, the preservation stage of
the fossils prevents an unambiguous association with extant Ephedra. Because the name
Ephedrites, previously used for ephedroid
fossils, is the basionym of an angiosperm and
unsuitable for gnetalean fossils, we have used
the genus name Liaoxia and suggest that
Liaoxia is used in the future for Ephedra-like
megafossils that cannot be unambiguously
assigned to the extant genus.
The species of Liaoxia are similar in overall
gross morphology, but differ from each other
and from previously described ephedroid fossils
in morphological details such as the absence or
presence of leaves, shape of the cones and in
shape and position of the cone bracts.
Several studies have indicated that the
diversity of the Gnetales was larger in
the Early Cretaceous than it is today and the
fossils presented here further document this.
The crown group Gnetales is represented in the
Early Cretaceous by Cratonia (Rydin et al.
2003), Welwitschiostrobus (Dilcher et al. 2005),
coalified Ephedra seeds (Rydin et al. 2004,
Rydin et al. 2006) and probably also by
262
C. Rydin et al.: Cretaceous ephedroids from China
Drewria (Crane and Upchurch 1987), Gurvanella (Chaoyangia) (Krassilov 1982, Duan
1998) and undescribed fossils from Brazil
(Barbara Mohr, unpubl. data) and China
(Rydin et al., unpubl. data).
Whether the ephedroid fossils presented
here belong to crown group Gnetales or to
extinct stem groups, is yet to be discovered. We
consider them members of the ephedran lineage,
but due to restricted information in the fossils
and poorly understood morphological diversity
of extant Ephedra, it is not possible to assign
them to any particular subgroup of Ephedra or
to clearly exclude them from the extant genus.
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Research Link Programme (EMF and Zhou Zhonghe), NSFC (SQW) and from the Royal Swedish
Academy of Sciences (CR).
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Addresses of the authors: Catarina Rydin,
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