全 文 ：植 物 分 类 学 报 43(2): 182–190(2005)
Acta Phytotaxonomica Sinica
———————————
Received: 13 January 2005 Accepted: 26 January 2005
Supported by a Kowledge Innovation Project of the Chinese Academy of Sciences (KSCX2-SW-108).
* Author for correspondence. Fax & Tel.: +86-10-62593385. E-mail: .
Emendation of Sorosaccus gracilis Harris 1935,
a gymnospermous pollen cone
1, 2 LIU Xiu-Qun 3 Francis M. HUEBER 1 LI Cheng-Sen* 1 WANG Yu-Fei
1(Laboratory of Systematic and Evolutionary Botany, Institute of Botany, the Chinese Academy of Sciences,
Beijing 100093, China)
2(Graduate School, the Chinese Academy of Sciences, Beijing 100039, China)
3(Department of Paleobiology, Smithsonian Institution, Washington, DC 20560-0121, USA)
Abstract Study of gymnospermous pollen cones, identified with Sorosaccus gracilis Harris
1935, from the Yangcaogou Formation, Late Triassic of China, has led to the identification of
new and significant characteristics of the species. The new specimens show distinct variations
in the morphology of the distal laminar portions of the microsporophylls. These well-
preserved fossils are helpful in elucidating, reconstructing and revising the diagnostic features
of S. gracilis. After comparing the characteristics of the specimens from China with those of S.
sibiricus Prynada 1962, and of the pollen cones which were respectively assigned to Baiera
longifolia (Pom.) Heer 1876 from Siberia, Russia, S. minor Harris 1935 from Greenland, and
S. umaltensis Krassilov 1972 from Bureya River of Russia, we consider that these four names
should be reduced to the synonymy of S. gracilis. Thus we revise the diagnosis of Sorosaccus.
The significance of Sorosaccus in evolution of pollen cones is discussed. We consider that
Sorosaccus is possibly basic to the evolution of the genus Ginkgo by the reduction of the
number of microsporangia and of microsporophylls. Ginkgo liaoningensis Liu, Crane, Li &
Wang 2005 from the Early Cretaceous of Liaoning Province, China represents likely one of
morphologically intermediate steps between Sorosaccus and G. biloba in evolution.
Key words Sorosaccus gracilis, pollen cone, evolution, Late Triassic, Liaoning.
The genus Sorosaccus was established by Harris in 1935, based on pollen cones initially
found from the Neil Cliff, Liverwort Bed belonging to the Thaumatopteris Zone, in the fossil
flora of Scoresby Sound East Greenland (Harris, 1935). The pollen cones were always
associated with ginkgoalean leaves in East Greenland, and “their microspores were of a type
which occurred in the Ginkgoales and many Gymnosperms” (Harris, 1935). But the genus is
dubious in taxonomic position or is unknown in evolutionary trends. So far, only four species
have been contained in Sorosaccus: S. gracilis Harris 1935, S. minor Harris 1935, S. sibiricus
Prynada 1962 and S. umaltensis Krassilov 1972.
In this paper, the specimens of pollen cone Sorosaccus gracilis from Yangcaogou
Formation (Late Triassic) in Beipiao County, Liaoning Province, China, were studied, and its
likely taxonomic affinity and evolutionary trends were considered. The Late Triassic flora
from Yangcaogou Formation contains Thallites, Neocalamites, Annulariopsis, Danaeopsis,
Dictyophyllum, Todites, Cladophlebis, Nilssonia, Pterophyllum, Sphenobaiera, Baiera,
Ginkgoites, Glossophyllum, Podozamites, Pityophyllum, Cycadocarpidium, Taeniopteris,
Stenorachis (Zhou, 1981).

No. 2 LIU Xiu-Qun et al: Emendation of Sorosaccus gracilis Harris 1935, a gymnospermous pollen cone 183
1 Material and methods
The specimens were collected from Yangcaogou Formation in Zhaomagou Village,
Beipiao County, Liaoning Province, China (Fig. 1). Yangcaogou Formation is regarded as
Late Triassic in age (Zhou, 1981; Zhang & Zheng, 1987). They are preserved as impressions
in a matrix of gray to yellow mudstone. The specimens were observed under a
stereomicroscope Stemi SV 11 and photographed using a Nikon FM2 camera. All specimens
are housed in the National Museum of Plant History of China, Institute of Botany, the Chinese
Academy of Sciences, Beijing, China.


Fig. 1. Map showing fossil locality.
2 Description

Cones are roughly catkin-like (Figs. 2-5), cylindrical (Figs. 3, 4, 10), 35-45 mm in
length, 6-10 mm in diameter. They consist of a main axis with microsporophylls arranged
helically (Fig. 6). Some specimens (Figs. 2, 6-9) clearly show the microsporophylls with their
arrangement and microsporangia. The main axis, 1-2 mm in diameter, possesses faintly
striated surface (Figs. 3, 4). Microsporophylls, 30-40 in number, arise and are directed
upwardly at acute or obtuse angles to the main axis. The distance from the base of the axis to
the lowest microsporophyll is 10-15 mm. The interval between microsporophylls is 1-1.5
mm. Microsporophylls consist of a lamina bearing microsporangia on the abaxial surface. The
microsporophyll is divided into two parts: a petiole and an upwardly bending, expanded
lamina. The petiole is 2-3 mm long and 0.1-0.5 mm wide. The lamina is 2-5 mm long and
0.2-2.5 mm wide, bending upward and exhibiting considerable variation in outline from
linear-lanceolate to oval (Fig. 11). Some laminae are broken from their petioles away from the
main axis (Fig. 2). Microsporangia, in clusters of 6 to 8, are attached to the lateral and the
abaxial sides of the petiole. Each microsporangium is oval, 1-1.5 mm long and 0.5-1 mm
wide, and dehisces longitudinally.
184 Acta Phytotaxonomica Sinica Vol. 43



Figs. 2-5. Hypotypes of Sorosaccus gracilis. The specimen in Fig. 4 is the counterpart of the specimen in Fig. 3. The
numbers (2A, 2B, 2C, 2D, 2E, 2F, 2G; 3A, 3B, 3C, 3D; 5A, 5B, 5C) show the microsporophylls with microsporangia.
Scale bar = 5 mm.
3 Systematic palaeobotany
DIVISION GYMNOSPERMOPHYTA
ORDER INCERTAE SEDIS
FAMILY INCERTAE SEDIS
Sorosaccus Harris 1935 emend. Liu, Hueber, Li & Wang
Emended generic diagnosis: Pollen cone consisting of a main axis with microsporophylls
arranged helically. Microsporophyll consisting of petiole and lamina bearing microsporangia.
Microsporophyll arising to the axis; lamina bending upward. Microsporangia attached in a
cluster on the lateral and abaxial sides of the petiole. Microsporangium oval, dehiscing
longitudinally.
Type: Sorosaccus gracilis Harris 1935.
Sorosaccus gracilis Harris emend. Liu, Hueber, Li & Wang 1935. Sorosaccus gracilis Harris,
pl. 24, figs. 3-7, 11, 12; pl. 28, fig. 11; text-fig. 50, E, F, H.
Synonyms:
1876. Baiera longifolia Heer, Pars. 53, pl. IX, figs. 8, 9.
1935. Sorosaccus minor Harris, pl. 27, fig. 2.
1962. Sorosaccus sibiricus Prynada, pl. XIII, figs. 7, 8; pl. XVIII, figs. 4a, 5-7; pl. XXI,
fig. 5.
1972. Sorosaccus umaltensis Krassilov, pl. XIX, figs. 1, 2, 4-7, 9.

No. 2 LIU Xiu-Qun et al: Emendation of Sorosaccus gracilis Harris 1935, a gymnospermous pollen cone 185

Figs. 6-9. Magnification of the hypotypes of Sorosaccus gracilis Harris 1935 emend. Liu, Hueber, Li & Wang. 6.
Magnification of the part of the specimen of Fig. 2 and the numbers are corresponding to those in Fig. 2. 7. Magnification
of the left side of the specimen in Fig. 2 and the letter A is corresponding to that in Fig. 2. 8. Magnification of the middle
part of the right side of the specimen in Fig. 2 and the letter F is corresponding to that in Fig. 2. 9. Magnification of the top
of the specimen in Fig. 3 and the letters A and C are corresponding to those in Fig. 3. Scale bar=2 mm.

186 Acta Phytotaxonomica Sinica Vol. 43








Fig. 10. Reconstruction of Sorosaccus gracilis
Harris 1935 emend. Liu, Hueber, Li & Wang.

1972. Sorosaccus ex. gr. sibiricus Prynada
1962, in Krassilov, Mesozoic Flora of Bureya River
(Ginkgoales and Czekanowskiales), pl. XIX, figs. 3,
8. Nauka, Moscow.
Emended specific diagnosis: Pollen cone
elongate-cylindrical, catkin-like, 20-45 mm long
and 5-10 mm wide. Main axis with micro-
sporophylls arranged helically, cylindrical, 1-2 mm
in diameter, surface faintly striated. Microsporo-
phyll divided into two parts: horizontal petiole and
an expanded lamina. Lamina linear, lanceolate to
oval in outline, bending upward. Microsporangia
attached to lateral and abaxial sides of petiole, 6-8
in number. Microsporangium oval, 0.7-1.5 mm
long, 0.5-1.0 mm wide and longitudinal in
dehiscence.
Holotype: Sorosaccus gracilis Harris, 1935. pl.
24, figs. 5, 6.
Type locality: Scoresby Sound East Greenland,
Denmark.
Horizon: Neil Cliff Formation, Liverwort Bed
of Rhaetic (Late Triassic) and Lower Liassic (Early
Jurassic) (Harris, 1937).
Epitypes: Figs. 2-5. LN-8486, LN-8487,
ZMG-8488, ZMG-8489.
Locality: Zhaomagou Village, Beipiao City,
Liaoning Province, China.
Horizon: Yangcaogou Formation, Late Triassic
(Zhou, 1981; Zhang & Zheng, 1987).
Repository: National Museum of Plant History
of China, Beijing, China.
Distribution: East Greenland, Denmark;
Siberia, Russia; Liaoning, China.
4 Comparison
We compare four species in Sorosaccus: S.
gracilis Harris 1935, S. minor Harris 1935, S.
sibiricus Prynada 1962 and S. umaltensis Krassilov
1972.
Harris (1935) separated Sorosaccus minor
from S. gracilis stating that the former was
“differing in being more slender owing to its
smaller sporophylls (basal region 2 mm long) and
smaller sporangia (0.7×0.5 mm)”. The sporangium
of S. gracilis, 1.1×0.8 mm, is bigger than that of
the type specimen of S. minor (Harris, 1935, pl. 27,
No. 2 LIU Xiu-Qun et al: Emendation of Sorosaccus gracilis Harris 1935, a gymnospermous pollen cone 187

Fig. 11. Variation of microsporophylls without microsporangia of Sorosaccus gracilis in outline. The letters A-N show
respectively the drawings of the microsporophylls without microsporangia in Fig. 3A, Fig. 2A, Fig. 2B, Fig. 2D, Fig. 3B,
Fig. 2C, Fig. 5A, Fig. 2E, Fig. 3D, Fig. 5B, Fig. 2G, Fig. 5C, Fig. 3C, and Fig. 2F.

fig. 2), 0.7×0.5 mm (Table 1). But the size of the sporangium in our specimens, 1-1.5×
0.5-1 mm, covers that of S. minor. We consider that the different sizes show the specimens in
different phases of development. The size of sporophylls in S. minor, with the petiole 2 mm
long, is similar to that in S. gracilis based on Harris’ description, which is 2-4 mm, and the
size is in the range of that of S. gracilis based on our collections, which is 1-3 mm long. It is
very difficult to differentiate S. minor from S. gracilis based only on the size of basal stalks
and microsporangia. We transfer therefore the specimens assigned to S. minor to S. gracilis.

188 Acta Phytotaxonomica Sinica Vol. 43
Table 1 Comparison of specimens assigned to Sorosaccus gracilis Harris 1935 emend. Liu, Hueber, Li & Wang
Notes: Specimen*=Specimens assigned to Sorosaccus gracilis Harris 1935 emend. Liu, Hueber, Li & Wang in this paper;
Petiole*=Petiole of microsporophyll; MIC=Microsporangium; LT=Late Triassic; EJ=Early Jurassic; MJ=Middle Jurassic;
LJ=Late Jurassic.

Specimens of Sorosaccus sibiricus was collected from the Middle Jurassic of eastern
Siberia (Prynada, 1962). Prynada discussed that “the sporophylls of Ust’-Baley specimens are
similar with those from the Lower Jurassic deposits of Greenland but differing from them in
the size of the whole cones and close arrangement of sporophylls”. In fact, the sporophylls of
Ust’-Baley specimens are similar to those of Greenland in the size of the entire cones and
arrangement of sporophylls. Firstly, the size of the specimens assigned to S. sibiricus, 20×
5-7 mm, is covered in that of S. gracilis based on new materials from China, 35-45×6-10
mm (Table 1). The number of microsporangia in S. sibiricus (8 in number) is similar to that of
S. gracilis (6-8 in number). Krassilov (1972) thought that dimensions of pollen cones
ascribed to S. sibiricus by Prynada were insignificantly distinguished from those by Harris.
Thus we move the specimens assigned to S. sibiricus to S. gracilis.
The specimens of Sorosaccus umaltensis were collected from the sediments of the Upper
Jurassic at the right bank of Bureya River, Russia (Krassilov, 1972). Krassilov (1972)
considered that the reproductive organs from Bureya River coincide almost completely with
those of S. gracilis in dimensions of the pollen cones, microsporophylls and microsporangia.
But the pollen grain size of S. umaltensis, 40×27-50×36 µm, is smaller than that of S.
gracilis (90×60 µm) (Harris, 1935). It is uncertain to describe a new species based on the
size of pollen grains since the size of pollen grains varies distinctly in different phases of
development. We also transfer the specimens assigned to S. umaltensis to S. gracilis.
Four specimens (Heer, 1876, pl. IX, figs. 8-11) were described as the pollen cones of
Baiera longifolia based on their general agreement with the pollen cones of Ginkgo and on
their association with the leaves. Harris (1935) considered that they were exactly is the same
nature of Sorosaccus gracilis. After our observation, two specimens (Heer, 1876, pl. IX, figs.
8, 9) from the four show that the cone axis bears the bracts with extended laminae that bend
upward and bear microsporangia. Therefore, we considered that the two belong to Sorosaccus
gracilis.


Specimen* Locality Age Size of
male
cone
(mm)
Diameter
of axis
(mm)
Length of
petiole*
(mm)
Angle of
petiole*
with axis
Numbe
r of
MIC
Size of
MIC
(mm)
Size of
pollen
grain
(µm)
Reference
S. gracilis Greenland,
UK
LT,
EJ
30×8 1 2-4 right angle 6 1.1×0.8 90×60 Harris,
1935
S. minor Greenland,
UK
LT,
EJ
2 0.7×0.5 Harris,
1935
S. sibiricus Siberia,
Russia
MJ 20×
5-7
right angle 8 Prynada,
1962
S. umaltensis Bureya
River,
Russia
LJ 18×8
(Not
intact)
0.5 3.5-4.5 right angle 8 1.0×0.8 40×27
-
50×36
Krassilov,
1972
Specimen
from China
Liaoning,
China
LT 35-45
×
6-10
1-2 3 right or
obtuse
angle
6-8 1-1.5×
0.5-1
In this
paper
No. 2 LIU Xiu-Qun et al: Emendation of Sorosaccus gracilis Harris 1935, a gymnospermous pollen cone 189








co nother transitional type between Sorosaccus and
G ing in the period of the Middle-Late Jurassic (Fig.
12 and narrowed lamina at the distal portion of the
m mber of sporangia may have decreased in the
ev lamina at the distal portion of the microsporophyll
m he evolutionary trend of the pollen cones needs
fu ens of pollen cones in organic connection with
fo
5 Discussion
We are trying to relate the genus
Sorosaccus with ginkgoaleans and
deduce its evolution based on the oval
microsporangia dehiscing longitudinally
and the pollen like that in Ginkgoales.
C
So
of
of
lia
fr
C
an
B
“T
E
be
an
sp
la
sp
3-
at
m
en
co
co
ev
of
sh
la
m
ni
co
in
an
Fig. 12. Schematic drawing showing the evolutionary
lineage of several pollen cones from Sorosaccus gracilis to
Ginkgo biloba.
urse of the ginkgoalean pollen cones. A
inkgo (G. liaoningensis), probably occurr
), is interpreted to contain a shortened
icrosporophyll. It suggests that the nu
olutionary process, and the length of the
ay have shortened. The hypothesis of t
rther confirmation after obtaining specim
omparing the whole pollen cone of
rosaccus gracilis with the pollen cone
Ginkgo biloba (the only extant species
the order Ginkgoales) and Ginkgo
oningensis (a pollen cone collected
om the Yixian Formation of Early
retaceous, Liaoning, China) (in our
other paper which is accepted by
otanical Journal of the Linnean Society,
he pollen cones of Ginkgo from the
arly Cretaceous of China, and its
aring on the evolutionary signific-
ce”), it is found that 6-8 micro-
orangia per cluster are attached to
teral and abaxial sides of micro-
orophyll in Sorosaccus gracilis, and
4 pendulous microsporangia are
tached to the abaxial side of
icrosporophylls in Ginkgo liaoning-
sis and 2 in G. biloba. As these pollen
nes are quite similar in outline, we
nsider that Sorosaccus could have
olved to Ginkgo through the reduction
the number of sporangia and
ortening the distal portion of the
mina at the distal portion of the
icrosporophyll (Fig. 12). Ginkgo liao-
ngensis from the Early Cretaceous
uld represent one of morphologically
termediate steps between Sorosaccus
d Ginkgo biloba in the evolutionaryliar axes.
190 Acta Phytotaxonomica Sinica Vol. 43
Acknowledgements We thank Professor Albert Ablaev (Pacific Oceanological Institute,
Far East Branch, Russian Academy of Sciences, Russia), Professor Svetlana V. Syabryaj
(Institute of Geological Sciences, National Academy of Sciences of Ukraine) and Professor
Jan J. Wocicki (W. Szafer Institute of Botany, Polish Academy of Sciences, Poland) for
providing and translating Russian literature. We also thank Mr. Ying-Bao Sun (Institute of
Botany, the Chinese Academy of Sciences, Beijing, China) for his drawings. The work was
supported by a Kowledge Innovation Project of the Chinese Academy of Sciences
(KSCX2-SW-108).
References
Harris T M. 1935. The Fossil Flora of Scoresby Sound East Greenland, Part 4: Ginkgoales, Coniferales,
Lycopodiales and Isolated Fructifications. Meddelelser om GrØnland 112 (1): 145-146.
Harris T M. 1937. The Fossil Flora of Scoresby Sound East Greenland, Part 5: Stratigraphic Relations of the
Plant Beds. Meddelelser om GrØnland 112 (2): 67.
Heer O. 1876. Beiträge zur Jura-Flora Ostsibiriens und des Amurlandes. Mémoires de L’académie Impériale
des Sciences De St.-Pétersbourg, VIIE Série. 22: 53.
Krassilov V A. 1972. Mesozoic Flora of Bureya River (Ginkgoales and Czekanowskiales). Moscow: Nauka.
96-97.
Prynada V D. 1962. Flore Mesozoique de Siberie Orientale et de Transbaikalie. Moscow: Nauka. 368.
Zhang W (张武), Zheng S-L (郑少林). 1987. Early Mesozoic fossil plants in Western Liaoning, China. In: Yu
X-H (于希汉), Wang W-L (王五力), Liu X-T (刘宪亭), Zhang W (张武) eds. Mesozoic Stratigraphy and
Palaeontology of Western Liaoning, China (辽宁西部中生代地层古生物 ). Beijing: Geological
Publishing House. 239-338.
Zhou H-Q (周惠琴). 1981. Discovery of the Upper Triassic flora from Yangcaogou of Beipiao, Liaoning. In:
The Palaeontological Society of China ed. 12th Annual Conference of the Palaeontological Society of
China Selected Papers (中国古生物学会第十二届学术年会论文集). Beijing: Science Press. 188.
裸子植物雄球花——纤细堆囊穗的修订
1, 2刘秀群 3 Francis M. Hueber 1李承森* 1王宇飞
1(中国科学院植物研究所系统与进化植物学重点实验室 北京 100093)
2(中国科学院研究生院 北京 100039)
3(Department of Paleobiology, Smithsonian Institution, Washington, DC 20560-0121, USA)
摘要 研究了采自中国东北晚三叠世羊草沟组的一种裸子植物雄球花——纤细堆囊穗。通过对新材料
的研究,发现这种雄球花小孢子叶末端的裂片在形态上差异很大,这是原来没有发现的十分重要的特征。
这些保存精美的化石对于纤细堆囊穗特征的阐明和修订以及物种复原很有帮助。将中国的标本与西伯
利亚堆囊穗、小堆囊穗、乌尔马堆囊穗和被定为长叶拜拉的雄球花进行了比较,发现它们与纤细堆囊穗在
特征上一致,故将它们处理为纤细堆囊穗的异名。修订后的纤细堆囊穗包括上面所提到的所有种。同时,
也讨论了堆囊穗属可能的演化意义。它可能是银杏属的远祖,经过小孢子囊数目的减少和小孢子叶长度
的缩短而演化到现在的银杏,而产自辽西早白垩世的辽宁银杏可能代表了堆囊穗和现代银杏在形态演
化上的一个中间步骤。
关键词 纤细堆囊穗; 雄球花; 演化; 晚三叠世; 辽宁