An anatomically preserved arborescent lycopsid, Sublepidodendron songziense (Sublepidodendraceae), from the Late Devonian of Hubei, China.

Abstract

Sublepidodendron is a common megafossil plant in the Late Devonian of China, but historically the generic delimitation based on leaf bases masked its true systematic position. A reinvestigation of S. songziense from the Late Devonian Hsiehchingssu Formation, Hubei, China, provides new insights into its internal anatomy and reproductive morphology. This arborescent lycopsid is characterized by small, vertically elongated leaf bases arranged in spirals, presence of false leaf scars, possibly bearing separate cones, and association with a stigmarian rhizomorph. The potential for organic connections of these detached organ genera has been noted for other Sublepidodendron species. The anatomy of S. songziense axes from two levels reveals that the thinner axis may bear an ectophloic siphonostele with a filamentous pith and an outer cortex. The thicker axis has a siphonostele with a branch gap, two-zoned pith with secondary thickenings, multiseriate rays across secondary xylem, a thick periderm, and primary and secondary tracheid walls characterized by "Williamson's striations." Similarities to synapomorphies of Diaphorodendraceae and Lepidodendraceae suggest that S. songziense bears a closer affinity to Lepidodendrales rather than Protolepidodendrales, as formerly thought. Widespread occurrence of Sublepidodendron implies that phylogenetically advanced arborescent lycopsids must have diverged by the Late Devonian.

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American Journal of Botany 89(9): 1468–1477. 2002.
AN ANATOMICALLY PRESERVED ARBORESCENT
LYCOPSID, SUBLEPIDODENDRON SONGZIENSE
(SUBLEPIDODENDRACEAE), FROM THE LATE DEVONIAN
OF HUBEI, CHINA1
QI WANG,2,4SHOU-GANG HAO,2,5DE-MING WANG,2
AND DAVID L. DILCHER3,5
2Department of Geology, School of Earth and Space Sciences, Peking University, Beijing 100871, P. R. China; and
3Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611-7800 USA
Sublepidodendron is a common megafossil plant in the Late Devonian of China, but historically the generic delimitation based on
leaf bases masked its true systematic position. A reinvestigation of S. songziense from the Late Devonian Hsiehchingssu Formation,
Hubei, China, provides new insights into its internal anatomy and reproductive morphology. This arborescent lycopsid is characterized
by small, vertically elongated leaf bases arranged in spirals, presence of false leaf scars, possibly bearing separate cones, and association
with a stigmarian rhizomorph. The potential for organic connections of these detached organ genera has been noted for other Suble-
pidodendron species. The anatomy of S. songziense axes from two levels reveals that the thinner axis may bear an ectophloic sipho-
nostele with a filamentous pith and an outer cortex. The thicker axis has a siphonostele with a branch gap, two-zoned pith with
secondary thickenings, multiseriate rays across secondary xylem, a thick periderm, and primary and secondary tracheid walls char-
acterized by ‘‘Williamson’s striations.’’ Similarities to synapomorphies of Diaphorodendraceae and Lepidodendraceae suggest that S.
songziense bears a closer affinity to Lepidodendrales rather than Protolepidodendrales, as formerly thought. Widespread occurrence of
Sublepidodendron implies that phylogenetically advanced arborescent lycopsids must have diverged by the Late Devonian.
Key words:
arborescent lycopsid; China; Late Devonian; Lepidodendrales; Sublepidodendron songziense.
Arborescent lycopsids are one of the most conspicuous
groups in Late Devonian floras. In recent years, it has become
apparent that this group is in need of further study. Two widely
distributed genera, Lepidodendropsis Lutz (1933) and Suble-
pidodendron (Nathorst) Hirmer (1927), had a very early debut
in the Devonian of China as compared with coeval floras in
Europe, Africa, and America (Sze, 1936a, 1943, 1956; Banks,
1960; Danze ´-Corsin, 1960a, b; Li and Cai, 1978; Chaloner and
Sheerin, 1979; Cai and Wang, 1995; Li, 1997). Consequently,
the Famennian floral assemblage of China was named after
Sublepidodendron mirabile-Lepidodendropsis hirmeri-Hama-
tophyton verticillatum (Cai and Li, 1995), which did not con-
form with Banks’ Archaeopteris (zone VI)/Rhacophyton (zone
VII) scheme (1980). However, relatively little is known about
the genus Sublepidodendron.
Here we present an anatomical study of previously de-
scribed stem impressions of Sublepidodendron songziense
based on the permineralized axes from the Hsiehchingssu For-
mation (sensu lato) of Songzi City, southwestern Hubei Prov-
ince, China. In this formation, the upper nonmarine Clasolite
Member is intercalated with black, fine, arenaceous mudstone
1Manuscript received 1 February 2002; revision accepted 25 April 2002.
This paper represents a portion of Qi Wang’s dissertation submitted to Pe-
king University in partial fulfillment of the requirements of a doctoral degree.
The authors thank Terry A. Lott, Florida Museum of Natural History, for
his help in the preparation of this paper; William DiMichele for his helpful
suggestions; Yi Wang for recently communicating unpublished findings; and
Chun-Yuan Zhou for helping with photography. This study was supported by
the National Natural Science Foundation of China (49972009) and Major
Basic Research Projects of the Ministry of Science and Technology, China
(G2000077700).
4E-mail: happyking2644@sina.com.
5Authors for reprint requests (e-mail: dilcher@flmnh.ufl.edu; sghao@
geo.pku.edu.cn).
containing abundant lycopsids (Feng, 1984; Chen and Jin,
1996; Cai, 2000). The Clasolite Member belongs to the Fa-
mennian because it is correlated with brachiopods (Cyrtospi-
rifer and Tenticospirifer), bivalves (Buchiola), and conodonts
(Polygnathus brevis and Icroides alternatus), which also occur
in the upper part of this member (Zhang, Liao, and Feng,
2001). Since Sze’s (1952) pioneering work on the Devonian
plants from this area, abundant fossil plants have been record-
ed (in Feng et al., 1977; Chen, 1984; Feng, 1984), but most
of them, especially arborescent lycopsids, were mainly based
on compression-impression material. In our collection, Sub-
lepidodendron songziense is preserved as compressions and
petrifications, including large and small axes in various states
of preservation and some distal shoots showing organic con-
nection with the cones on the tips (Fig. 1). Usually, such cones
are loosely assigned to a commonly dispersed organ species,
Lepidostrobus grabaui (Sze, 1936b), from the Upper Devo-
nian of South China (Feng, 1984; Cai and Wang, 1995; Chen,
1999; Jin and Wu, 2001). Two kinds of cones (Figs. 1, 3, 4)
can be identified from isolated cones and may have been de-
tached from the same parent plant. Sublepidodendron song-
ziense was distinguished from other species within Sublepi-
dodendron by Chen (in Feng et al., 1977) on the basis of its
very small, fusiform or oval leaf bases with obtuse corners
(Fig. 2). However, Chen’s syntype specimens are too frag-
mentary to cover all variations of the leaf bases so that me-
gafossils of this species have been variously treated (Feng,
1984; Li and Lan, 1984; Cai and Li, 1995). An overall emen-
dation to S. songziense will not be undertaken here, but rather
new data will be presented for its anatomy.
MATERIALS AND METHODS
All the specimens were collected from one of the syntype localities, Huang-
kuang at Liujiachang, about 30 km southwest of Songzi City, where the De-

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September 2002]1469WANG ET AL.—ANATOMY OF SUBLEPIDODENDRON
Figs. 1–5.
branching and its organic connection to a Lepidostrobus-like cone. Note that there are two other detached cones on the same bedding plane, and the lower cone
and the upper two ones are quite different in shape, which may be identified as two separate cones types. Arrowhead refers to the enlarged part in Fig. 2.
Specimen: WQ-001A. Bar ? 2 cm. 2. The shoot shows that the small leaf bases are arranged in spirals. Arrowhead refers to the false leaf scars as defined by
some authors (al. ‘‘Bogenlinie,’’ Nathorst, 1920; Hirmer, 1927; ‘‘arc foliaire,’’ Danze ´-Corsin, 1958a, b; ‘‘fausse cicatrice foliaire,’’ Chaloner and Boureau, 1967;
Corsin et al., 1973; ‘‘false leaf scar,’’ Meyen, 1976; Thomas and Meyen, 1984). Some leaf bases show the median keels. These are the major diagnostic
characters of the genus Sublepidodendron. Bar ? 2 mm. 3–4. Two types of cones are often preserved isolated on the same bedding plane. They are thought to
correspond to those cones in Fig. 1. Specimens: WQ-018A and WQ-014A. Bars ? 2 cm. 5. A fragmentary part of the stigmarian rhizomorph shows some
elliptical root scars and wrinkled surface. Specimen: WQ-012D. Bar ? 2 cm.
The external morphology of Sublepidodendron songziense. 1. A distal, leafy shoot shows at least three orders of subequal or unequal dichotomous

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1470 [Vol. 89AMERICAN JOURNAL OF BOTANY
vonian strata is subdivided into three formations. These are, in descending
order: the Hsiehchingssu Formation (Famennian), the Huangchiateng For-
mation (Frasnian), and the Yuntaikwan Formation (Givetian) (Sze, 1952;
Feng, 1984). The plant material was collected from a black, fine, arenaceous
mudstone horizon ranging from 20 to 52 cm thick within the lower part of
the Clasolite Member of the Hsiehchingssu Formation.
Anatomical information is gleaned from two invaluable permineralized
axes. One petrified axis (axis A) is ?10 mm long, which was laying parallel
in the same bedding plane as an incomplete cone (Lepidostrobus grabaui).
These two organs may be from the same source plant, Sublepidodendron
songziense, which is the only megafossil identified from these sediments. The
other one (axis B) is about 30 mm long with partially exposed leaf bases on
the surface of an impression, which can be identified as S. songziense in one
part, and then was gradually fusainized and permineralized towards another
end. The contour of axis B is not intact. They were prepared by standard
procedures of embedding, sectioning, grinding, and polishing for examination
with the light microscope and reflected light (Stein, Wight, and Beck, 1982).
In addition, the freshly cleaved surfaces of the petrified and fusainized axes
were prepared for examination with scanning electron microscopy (SEM;
AMARY 1910FE, Electron Microscopy Laboratory, Peking University). All
specimens and slides are housed in the Palaeontological and Stratigraphical
Section, Department of Geology, Peking University, China.
RESULTS
Description—Transverse sections of axis A show a circular
primary xylem strand with a nearly smooth or undulate margin
(Fig. 6) because the peripheral protoxylem does not form con-
spicuous tooth-like ridges or coronae, but is distributed con-
tinuously. The tracheids are scalariform with minute anasto-
moses or vertical fimbrils connecting the horizontal bars (Figs.
10, 11). The leaf traces are indiscernible, and the mode of their
emission is superficial (Bateman, DiMichele, and Willard,
1992). The primary xylem is exarch (Figs. 6, 7). The stelar
center either lacks cellular preservation or bears an irregularly
filamentous core (Figs. 6–9). Immediately adjacent to the pri-
mary xylem is a poorly preserved narrow band, 2–4 cells
thick, of extraxylary tissue, which may be primary phloem. It
is homogeneous, parenchymatous tissue, and the cell lumina
are largely circular or elliptical in transverse view, elongated
in longitudinal view with horizontal end walls, and possible
sieve cells ill-defined (Figs. 10, 11). Therefore, the primary
vascular system may be an ectophloic siphonostele (Beck,
Schmid, and Rothwell, 1982). In addition, there are patches
of cells that are separated from the stelar tissues by a wide
circumstelar lacuna, which probably belong to the outer cor-
tex. The patches of cells are thick-walled, yellowish-colored,
possibly with resinous contents, rounded in transverse section
and elongate with horizontal or bluntly tapered end walls in
longitudinal section (Figs. 12, 13). The outer cortex has a dis-
continuous layer of cells with periclinal divisions, probably
the result of early stages of secondary cortical initiation (Fig.
12). Under the SEM, the transversely broken surface of par-
tially decorticated axis A shows a stele, about 1 mm in di-
ameter, with some irregular cavities in the center, which may
represent a pith (Fig. 23).
The original specimen of axis B was serially sectioned and
is estimated to be about 5–8 mm thick, but its surface is so
irregular that the anatomical characters observed are often dis-
continuous. Most sections possess distinctive secondary xylem
quite different from the sections of axis A (Figs. 14–22). Re-
markably, the division of the stele occurs by the separation
into unequal columns of stelar tissues. It shows that there is a
lateral branch of the axis with a smaller stele partly surrounded
by secondary xylem or periderm that has the same pith as the
larger stele (Fig. 19). Under reflected light, the piths have well-
defined heterogeneous central tissue, which consists of irreg-
ularly oriented cells and can be subdivided into two zones.
The outer zone, 4–12 or more cells wide and in contact with
the metaxylem, is composed of a mass of larger parenchy-
matous cells than those of the inner zone, and their cell walls
appear to have secondary thickenings. The inner zone, ellip-
tical in cross section, is often crushed, degraded, or partially
separated from the outer zone (Fig. 19). Under transmitted
light, parenchyma cell walls of the inner pith apparently are
secondarily thickened (Fig. 21). Immediately external to the
pith there is a narrow, undulate band of the primary xylem
whose peripheral protoxylem is inconspicuously similar to that
of axis A (Figs. 20, 22). The primary xylem only accounts for
a small area of the total stele, and the tracheal lumina are
generally smaller than those of the parenchymatous pith cells
(Figs. 19, 20, 22). The primary vascular system can be char-
acterized as a siphonostele with a branch gap (see Beck,
Schmid, and Rothwell, 1982). External to the primary xylem,
there is a wide zone of the secondary xylem, which is divided
into wedges by distinctive radially parting along the ray cells
(Figs. 19, 20). Freshly cleaved surfaces of the partly fusainized
axis B show under SEM hive-like secondary xylem crossed
by radial vascular rays. The tracheids have scalariform thick-
enings with vertical threads connecting the horizontal bars,
generally termed ‘‘Williamson’s striations,’’ as described by
many authors (Evers, 1951; Fry, 1954; Smith, 1962; Alvin,
1965; Taylor, 1981; Geng, 1990) (Figs. 24–30). The vascular
rays are multiseriate, 4–6 cells wide, and 4–5 cells high, with
scalariform thickening (Figs. 25–28). A transverse section
shows some discontinuous layers of small, secondary tracheids
peripheral to the inner secondary xylem (Figs. 14, 15). Such
layers at the edge of the secondary xylem are not thought to
be natural, and they appear to be part of the process of deg-
radation and crushing (W. A. DiMichele, Smithsonian Insti-
tution, personal communication, 2001). They do not show fea-
tures sufficient to confidently identify them as a vascular cam-
bium, and they may instead represent sites where the initial
tracheids ceased developing at the end of secondary growth.
The leaf traces are elliptical in shape and composed of isodi-
ametric cells. They are arranged in a low spiral (Fig. 16). The
tracheids are elongated with tapered end walls. External to the
secondary xylem, the cortical zonation is either lacking or dif-
ficult to recognize due to the extreme narrowness and com-
pression of the inner zones and the obliqueness of the sections.
The primary cortex is rarely preserved, in association with
patches of leaf traces, or possibly replaced by the periderm
(Figs. 19, 20, 22). The periderm is often split radially into
large segments, which appear to lack distinct differentiation
into phellem and phelloderm. It consists of radially aligned
areas of tangentially elongated cells, which appear to contain
a kind of yellowish resinous substance (Fig. 22). The leaf ba-
ses are absent.
DISCUSSION
Overall, axis A may be part of a distal branch attached to
a cone or part of a deciduous lateral branching system while
axis B is possibly originated from the terminal part of a trunk
with a lateral branch or from a larger deciduous lateral branch.
As far as the primary vascular systems of the two axes are
concerned, their anatomical characters are extremely similar.

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September 2002]1471WANG ET AL.—ANATOMY OF SUBLEPIDODENDRON
Figs. 6–11.
pith is destroyed or appears to be filamentous. Protoxylem exarch, distributed in a continuous layer at the margin of the tracheary cylinder without conspicuous
ridges or coronae. There are some circumstelar lacunae and residual outer tissues. Slides: Pku-wq-Tr2 and Pku-wq-Tr1. Bars ? 500 ?m. 8. Enlarged stelar
periphery of axis A. The layer appears to be made up of thin-walled cells, which may be explained as the primary phloem (left arrowhead), and are distinctively
larger than the inner protoxylem elements (right arrowhead). Slide: Pku-wq-Tr2. Bar ? 100 ?m. 9. Enlargement of the stelar pith of axis A. It is filamentous
or lacunose with some secondary thickenings. Slide: Pku-wq-Tr1. Bar ? 100 ?m. 10. A longitudinal section of axis A shows scalariform thickened tracheids
with tapering end walls (right arrowhead) and possible phloem elements with horizontal end walls (left arrowhead). Slide: Pku-wq-L3. Bar ? 100 ?m. 11.
Enlarged stele of Fig. 10 in longitudinal view showing tracheids with scalariform thickenings that have minute anastomoses or vertical fimbrils connecting the
horizontal bars (al. ‘‘Williamson’s striations’’). Slide: Pku-wq-L3. Bar ? 100 ?m.
The internal anatomy of Sublepidodendron songziense as seen through the light microscope. 6–7. Two serial transverse sections of axis A. The

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1472 [Vol. 89AMERICAN JOURNAL OF BOTANY
Figs. 12–18.
patchy thick-walled cells, which are rounded in transverse section and elongate with horizontal or bluntly tapered end walls in longitudinal section. They are
interpreted as the outer cortex. Arrowheads refer to a discontinuous layer of cells that appear to initiate an early stage of secondary cortex development. Slides:
Pku-wq-Tr2 and Pku-wq-L3. Bars ? 100 ?m. 14–15. Secondary xylem divided into sections by radial rays in axis B. There are some discontinuous layers at
the secondary xylem periphery, which is composed of distinctively smaller tracheids than most of the inner secondary xylem. Slide: Pku-wq-Tr4. Bars ? 500
?m. 16. A tangential section of the secondary xylem of axis B. Arrowheads refer to two elliptical leaf traces in a low spiral. Slide: Pku-wq-Ta8. Bar ? 100
?m. 17–18. A transverse section of axis B. It shows the partly preserved pith and extrastelar tissues. The lower part is enlarged in Fig. 18, which shows the
outer zone of pith, narrow primary xylem, and wide secondary tissues. Slide: Pku-wq-Tr11. Bars ? 500 ?m.
The internal anatomy of Sublepidodendron songziense as seen through the light microscope. Fig. 12–13. Outermost portion of axis A showing