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American Journal of Botany 86(11): 1563–1575. 1999.
VESSEL-BEARING STEMS OF VASOVINEA TIANII
GEN. ET SP. NOV. (GIGANTOPTERIDALES) FROM THE
UPPER PERMIAN OF GUIZHOU PROVINCE, CHINA1
HONGQI LI
AND
DAVID WINSHIP TAYLOR2
Department of Biology, Indiana University Southeast, New Albany, Indiana 47150
Permineralized gigantopterid stems of Vasovinea tianii Li et Taylor gen. et sp. nov. were collected from the Upper Permian
of Guizhou Province, China. They are slender and bear prickles, trichomes, and compound hooks. Internally, the stems have
a sparganum cortex, eustele, and secondary xylem. The mesarch protoxylem tracheids have annular to helical thickenings,
and metaxylem tracheary elements have scalariform and/or transversely elongated, bordered pits, while those of the secondary xylem have scalariform to circular bordered pits. Importantly, the inner part of the secondary xylem has large vessel
elements with foraminate-like perforation plates. The hooks and other morphological and anatomical characteristics are
similar to those found in gigantopterids, suggesting that Vasovinea is a member of the Gigantopteridales. The vegetative
plant is reconstructed from permineralized stems and Gigantopteris-type leaves based on the anatomical similarities and
intimate association. The eustele, secondary xylem, and other features support the placement of the order among the seed
plants. Ecologically, Vasovinea is suggested to have been a vine or liana that used compound hooks to climb among the
trees in a Permian tropical rain forest. The occurrence of vessels could have been an efficient adaptation to allow the slender
stems to conduct sufficient water to the large Gigantopteris-type leaves.
Key words:
gigantopterids; Gigantopteris; hooks; lianas; paleoecology; Permian; stems; Vasovinea; vessels.
Fossil specimens of gigantopterids have been found
extensively from the Lower Permian and possibly into
the lowest Lower Triassic sediments throughout southeastern Asia (mostly from China), as well as from several
Lower Permian sites in Texas and Oklahoma, USA. This
group was first reported by Schenk (1883) from Hunan
Province, China, and currently includes more than 40
taxa (H. Li et al., 1994). The distinctive characteristics
of gigantopterids are their large compound or simple
leaves, which are variable in morphology, ranging from
oblong to roughly round shape, entire to toothed margin,
and simple to complex reticulate venation. Conventionally the group has been classified as ferns (Schenk, 1883)
or seed ferns (White, 1912; Asama, 1959; X. Li and Yao,
1983). In terms of relationships to other plants, Asama
(1974, 1982, 1988) proposed that the simple-leafed gigantopterids could have given rise to the angiosperms,
while X. Li and Yao (1983) interpreted their reconstruction of the reproductive organs of Gigantonoclea fukienensis as being ‘‘parti-angiosperms’’ in nature. Despite
1 Manuscript received 16 July 1998; revision accepted 25 March
1999.
This paper represents part of Hongqi Li’s dissertation submitted in
partial fulfillment of the requirements for the Ph.D. degree at the Ohio
State University, Columbus, Ohio. Hongqi Li thanks Drs. Edith L. Taylor and Thomas N. Taylor for professional help, and Dr. William A.
Jensen for guidance and encouragement. The authors thank Dr. Chengsen Li and the Botanical Institute of Beijing for support in fossil-collecting; Dr. Paul Kenrick and the staff of the Swedish Museum of Natural History for loan of gigantopterid specimens; and Drs. Sherwin
Carlquist, Kathleen B. Pigg, Leo J. Hickey, and an anonymous reviewer
for their valuable comments on the manuscript. This research is partially
supported by the Geological Society of America Research Grant
5195-93, the Graduate Student Alumni Research Award, Graduate
School of the Ohio State University, and grants from the Research and
University Graduate School of Indiana University, and the Academic
Affairs of Indiana University Southeast.
2 Author for correspondence (e-mail: [email protected]).
the distinctive leaves, anatomically preserved reproductive organs have not been found so that the systematics
of the group has been uncertain.
Recently, some permineralized gigantopterid leaves
and axes have been reported with many anatomical characteristics that can help in determining the relationships
of gigantopterids to other vascular plants. The permineralized leaves of the gigantopterid Delnortea abbottiae,
reported from Texas, USA, are suggested as being structurally similar to gnetophytes (Mamay et al., 1988). In
contrast, the permineralized leaves of Gigantonoclea
guizhouensis, from the Upper Permian in Guizhou, China, exhibit many features similar to those of angiosperms
(H. Li and Tian, 1990; H. Li et al., 1994). Two types of
permineralized gigantopterid stems also are found associated with the Guizhou gigantopterid leaves (H. Li, Taylor, and Taylor, 1992, 1993). One type is the prickly Aculeovinea yunguiensis (H. Li and Taylor, 1998), which is
considered a seed plant. Another type containing vessels
has been reported preliminarily (H. Li, Taylor, and Taylor,
1996).
Before the report by H. Li, Taylor, and Taylor (1996),
the fossil record of vessels could be traced back to the
Early Cretaceous. In extant plants, vessels consist of vertically linked tracheary elements with perforate end walls
so that they conduct water much more efficiently than
tracheids with imperforate end walls. Vessels are commonly found in angiosperms and gnetophytes, with rarer
occurrences in non-seed plants (see Discussion). Vessels
in living seed plants have been classified in two types,
i.e., foraminate vessels in gnetophytes and scalariform
ones (and/or their derived simple form) in angiosperms
(Bailey, 1944; Carlquist, 1992, 1994, 1996a). Vasovinea
tianii is different from the above two types, possessing
unique, foraminate-like vessels in the secondary xylem
and a possible scalariform-reticulate vessel in the meta-
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xylem. Therefore, the discovery of vessels in gigantopterids is important not only as the earliest fossil record
of vessels, but also in analyzing the systematic relationships and the ecological aspects of the group.
To complement the preliminary study (H. Li, Taylor,
and Taylor, 1996), we now provide a comprehensive description of the permineralized, vessel-bearing gigantopterid stems and establish them as a new taxon, Vasovinea
tianii Li et Taylor gen. et sp. nov. With several lines of
evidence from both permineralized and compression
specimens, we also demonstrate that the new taxon is a
member of the gigantopterids, reconstruct it together with
Gigantopteris-type leaves, analyze its possible habit, and
briefly discuss its systematic relationships to seed plants.
MATERIALS AND METHODS
Limestone and mudstone samples with gigantopterid stems and
leaves were collected from a talus pile mined from the upper and middle
parts of the Xuanwei Formation of the Upper Permian at the Shan-JianShu site, Yueliangtian Coal Mine in Panxian County, Guizhou, China,
in 1993. Additional information about the locality and stratigraphy can
be found in H. Li et al. (1994) and H. Li and Taylor (1998).
Permineralized specimens from five limestone samples (L9407,
PLY02, PLY03, PLY04, and L9414), and compressed specimens from
three mudstone samples (L9426, L9448, and L9449) were used. All
samples contain gigantopterid foliage and stem(s) in each, and some
have additional compound hooks as well as other structures, although
not all of these organs from each of the samples are figured in this
paper. Samples PLY03 and PLY04 are small, but each contains a Vasovinea tianii stem and a piece of Gigantopteris-type leaf. Sample
L9407 has numerous pieces of Gigantopteris-type leaves and several
pieces of V. tianii stems. PLY02 is a large sample, weighing more than
8 kg, and contains hundreds of pieces of permineralized (usually gigantopterid) plant organs, including at least two types of gigantopterid
leaves (Gigantopteris and Gigantonoclea), two types of gigantopterid
stems (V. tianii and Aculeovinea yunguiensis; H. Li and Taylor, 1998),
and some undescribed reproductive organs. Specimens of Vasovinea
and Gigantopteris in this sample are relatively fewer in number compared to those of Aculeovinea and Gigantonoclea.
The permineralized stems were sectioned and prepared using the
well-known cellulose acetate peel technique (Phillips, 1976). Areas with
interesting structures from the peels were trimmed, cleaned, and mounted on microscope slides for further observations. Occasionally specimens were peeled in both the transverse and longitudinal sections to
show the structural correlation of both sections (Figs. 1, 6). Specimens
were photographed with an MP-4 camera using 4 3 5 film or with an
Olympus 35-mm camera mounted on an Olympus Steroscan dissecting
microscope. To prepare scanning electron microscope (SEM) samples,
several permineralized wood pieces with vessels were etched with a 1%
HCl solution for ;20 min so that the diluted solution could dissolve
the calcium carbonate slowly to expose cellular structures, e.g., the perforation plates (Figs. 16–19). Then they were mounted and sputter coated with gold before being examined with SEM. The compressed specimens were directly photographed with a Polaroid MP-4 camera.
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cm in diameter, bearing compound hooks, prickles, and
glandular and tendril-like trichomes. Cortex with paired
vascular traces and sparganum structure in the outer part.
Eustele with parenchymatous pith and mesarch protoxylem, consisting of tracheids with annular, helical, or helical-scalariform thickenings. Centripetal metaxylem tracheids commonly consisting of one to two layers, while
centrifugal metaxylem usually consisting of two to three
layers of tracheary elements; metaxylem tracheary elements with scalariform and/or transversely elongated bordered pits on their lateral walls. Outer portion of the secondary xylem consisting of radial files of tracheids and
smaller vessels. Lateral walls of tracheary elements in
secondary xylem exhibiting multiseriate, alternate, and
transversely elongate to circular bordered pits. The inner
portion of the secondary xylem consisting of large vessels with diameter increasing from ;150 to 250 (up to
500) mm towards the primary xylem; vessel elements vertically connected by foraminate-like perforation plates on
the long, inclined (usually) to short, almost horizontal
(occasionally) end walls, each plate with multiseriate, alternate, obliquely elliptical to circular pores without borders. Homocellular, heteroseriate rays occurring every
one to three radial tracheary files, consisting of uni- to
bi-seriate xylic rays and multiseriate medullar rays between xylem segments.
Holotype—Slides L9407-C-B2, L9407-C-B16, and
L9407-D-T2. Figs. 1–4, 6.
Paratypes—Slides PLY02-C10-1-1, PLY02-E-1,
PLY03–01, PLY03–06, PLY03–07, PLY03–11, PLY03–
34, and PLY04-B; Specimens PLY02 and PLY03. Figs.
5, 7–20, 29–30.
The slides and specimens of both the holotype and
paratypes have been deposited in the National Museum
of Plant History of China at the Institute of Botany, Chinese Academy of Sciences, Beijing, China.
Etymology—The generic name is composed of vaso([L] 5 vessel) and vinea ([L] 5 vine) indicating a liana
stem with vessels. The specific name is proposed in honor
of Professor Baolin Tian, the Beijing Graduate School,
China University of Mining and Technology, for his contribution to the study of the Gigantopteris flora of western Guizhou, China.
Locality—Yueliangtian Coal Mine, Panxian County,
Guizhou Province, China.
Stratigraphic occurrence—Lower and Upper Xuanwei Formations, Upper Permian.
Age—Longtanian-Changxingian, Late Permian.
SYSTEMATICS AND DESCRIPTION
Order— Gigantopteridales X. Li et Z. Yao (1983)
Family—Gigantopteridaceae Koidzumi (1936)
Species—Vasovinea tianii gen. et sp. nov.
Generic and specific diagnosis—Stems slender, ;1
Description—The stems are usually ,1 cm in diameter
and up to 5 cm in length. One stem measured ;4 3 6
mm in transverse section (Figs. 1–3, 6), while others were
compressed and calculated to be ;1 cm in diameter
(Figs. 5, 29–30). Well-preserved stems have an epidermis
and hypodermis. The epidermis consists of one layer of
small cells that have relatively thick walls. The layer is
;10 mm thick and its cells are ;10 mm wide and 8 to
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Figs. 1–5. Vasovinea tianii stems. 1. Stem (left) longitudinal section with transverse section at bottom. Note attached basal part of a compound
hook (right side in the box), oblique section of the hook in the middle bottom (arrow), and prickles (arrowheads). Slide L9407-C-B16; bar 5 4
mm, 32.5. 2. Transverse section (14 continuous peels below the transverse section in Fig. 1) showing central xylem segments, two vascular traces
(marked as ‘‘T’’) outside a single lacuna (left arrow), and a prickle at right (right arrow). Slide L9407-C-B2; bar 5 1 mm, 316. 3. Transverse
section (5 mm below the section in Fig. 2) with several xylem segments, sparganum cortex (arrow), and the basal part of a compound hook structure
(H) in an oblique section. Slide L9407-D-T2; bar 5 1 cm, 316. 4. Enlarged portion of a wood segment and a vascular trace (at top) shown in Fig.
2. Notice the angular-shaped vessels and the mesarch primary xylem with tiny protoxylem cells (arrowhead). bar 5 0.5 mm, 336. 5. Stem with
vessels in the xylem segments and trichomes on the surface of the stem and embedded in the surrounding sediments (arrowheads). Slide PLY04B; bar 5 2 mm, 37.5.
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Figs. 6–13. Vasovinea tianii stems. 6. Enlargement from Fig. 1 showing large vessels in both transverse section (upper) and the longitudinal
section (lower) with vertically linked parenchyma cells (arrow) in the inner cortical portion and sclerenchyma strands on the right side. Slide L9407C-B16; bar 5 1 mm, 316. 7. Xylem in longitudinal section with two perforation plates (arrows) in the upper and central lower parts, a typical
lateral wall with bordered pits in the right lower part, and cross-field pitting of secondary xylem tracheids on the left side. Slide PLY03–01; bar 5
50 mm, 3200. 8. Primary xylem (left arrow) and secondary xylem (right) in longitudinal section. Notice the possible vessel element in the metaxylem
that has scalariform-reticulate structures on its long, oblique end wall (arrow), in contrast to the large vessel in secondary xylem on right with a
foraminate-like perforation plate. Slide PLY03–06; bar 5 200 mm, 368. 9. Longitudinal section of a centripetal metaxylem tracheid (on pith side)
with uniseriate scalariform pitting (lower left) and 2–3 rows of transversely elongated bordered pits (left upper, arrowhead). Also seen are two
poorly preserved tracheids with annular thickenings in the middle of the figure, and a protoxylem tracheid with helical to helical-scalariform
thickenings on right. Slide PLY03–06; bar 5 50 mm, 3200. 10. Enlargement from Fig. 8 showing a possible vessel element with a long, highly
inclined end wall (upper arrow) that has a scalariform-reticulate structure without surrounding borders or primary walls. The lower part shows a
broken piece of the lateral wall with imperforate transversely elongated bordered pits (lower arrow). Slide PLY03–06; bar 5 50 mm, 3200. 11.
Enlargement from Fig. 8 showing the perforation plate (pp) with multiseriate pores and the lateral wall of the vessel with bordered pits in the lower
right part. Slide PLY03–06; bar 5 50 mm, 3200. 12. Tangential section showing a long oblique perforation plate connecting two vessel elements
on left and a smaller perforation plate at lower right corner. Slide PLY02-C10-1-1; bar 5 200 mm, 342. (Reprinted with permission from H. Li et
al., 1996. Copyright 1996, American Association for the Advancement of Science.) 13. Tangential section of the secondary xylem showing a
tracheid with circular bordered pits. Slide PLY03–07; bar 5 50 mm, 3200.
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20 mm long. Beneath the epidermis are 2–4 layers of
hypodermal cells that are commonly ;40–50 mm long
and 15–40 mm in diameter, and densely arranged with
the larger cells occurring to the outside and smaller ones
to the inside. Attached to the stems are compound hooks
(see below) and a variety of appendages including prickles and glandular and tendril-like trichomes.
Appendages—The appendages are epidermal-cortical
outgrowths and lack any vascular tissue. They are commonly found on stems, but some smaller appendages can
be found on the compound hooks (Fig. 1, right arrowhead). The prickles on the stems are usually ;450 mm
(up to ;1000 mm) long and 450 mm (up to 550 mm)
wide at their bases, but a narrower one found near the
base of a compound hook is only ;250 mm wide at the
base (Fig. 2, right arrow). Each prickle is covered by the
epidermis and internally composed of vertically elongate
parenchyma cells, 20–30 mm in diameter and 40–50 mm
long. A few parenchyma cells beneath the epidermal cells
are narrower and have thickened cell walls. Some hypodermal cells (dark colored) beneath the base separate
the prickle from the inner part, suggesting that the prickle
is epidermal and cortical in origin. Structurally, these
prickles are nearly identical to those of Aculeovinea yunguiensis (H. Li and Taylor, 1998), but smaller in size.
Glandular trichomes can be found on both the stems
(Figs. 26, 28) and the compound hooks. Generally, they
are 500–2000 mm long and 500–1000 mm in diameter at
their bases. Their basal parts are similar to the prickles
in terms of their structure and the epidermal and cortical
origin. However, their apices consist of either several
large cells (Fig. 28) or a single larger oval cell, 200 mm
in length and 100 mm in diameter, at the tip (Fig. 26).
The tendril-like trichomes (the tendril-like structures in
H. Li, Taylor, and Taylor, 1992, 1993) are long and
curved in shape. These trichomes are ;300 mm in diameter and can be several millimetres long. They contain
similar-shaped parenchyma cells, with the inner cells
slightly enlarged. They may be preserved as tubes (Fig.
30, arrowhead) when the inner parenchyma cells are no
longer preserved. In other sections, these trichomes often
appear as wart-like structures extending from the stems
(Fig. 5, center) or circular rings (Fig. 5, arrowheads) embedded in the surrounding sediments.
Cortical histology—Beneath the hypodermis, in the
well-preserved stems, the cortex consists of a sparganum
structure (i.e., vertically parallel sclerenchymatous
strands alternating with vertical parenchymatous tiers; see
Taylor and Taylor, 1993) towards the outer side (Fig. 3,
bottom) and a wider parenchymatous zone towards the
inside (Figs. 2, 3). The sclerenchyma cells are ;20 mm
in diameter and 1000–3000 mm long (Fig. 6, right). The
cortical parenchyma cells are roughly cuboidal, 45–70
(up to 95) mm in dimension, and vertically linked (Fig.
6, arrow). They are often damaged or crushed, leaving
empty spaces in the cortex (Figs. 3, 5, 6).
Vascular system—A eustelic primary architecture surrounds a poorly preserved pith, which contains cuboidal
parenchyma cells, 40–70 (up to 110) mm in dimension
(Figs. 2, 3). The vascular cylinder is preserved in 5–9
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xylem segments of different sizes that are either well preserved or somewhat crushed. In transverse section, each
large woody segment appears as a sector of an annulus,
with the inner side longer than the outer side, because of
the larger vessels to the pith side and smaller tracheary
elements to the outside.
Along the periphery of the pith, primary xylem bundles and a few solitary tracheids are embedded among
the parenchyma cells. Mesarch protoxylem strands can
be found in the centers of some of the large bundles (Fig.
4, arrowhead at the bottom), but they are frequently difficult to distinguish. The protoxylem tracheids can be narrower than 20 mm in diameter with annular to helical or
helical-scalariform thickenings (Fig. 9). The centripetal
metaxylem usually is one to two cells wide (Fig. 4), and
the tracheids commonly are less than 50 mm in diameter
and have scalariform (Fig. 9, left lower part) or 2–3 rows
of transversely elongated, bordered pits (Fig. 9, arrowhead). The centrifugal metaxylem commonly is 2–3 cells
wide (Figs. 4, 8 [left]), with the inner tracheary elements
being narrow and having scalariform bordered pits. The
outer elements usually are large, up to 100 mm in diameter, and have up to five rows of transversely elongated, bordered pits on the lateral walls. The elongated
pits are arranged into obliquely opposite rows when two
or three rows are present. In some of those with five rows,
the pit openings are only 2.5 mm high but can be up to
16 mm wide. However, as the row number increases, the
pits appear to be alternately arranged and pit openings
become narrower.
One centrifugal metaxylem element (Figs. 8 [arrow],
10), 50 mm in diameter, has two types of wall structures.
The tip of the tracheary element forms a long, highly
inclined end wall that has a scalariform-reticulate structure (Fig. 10, upper arrow). The lower part shows a small
broken piece of its lateral wall with oval bordered pits
(Fig. 10, lower arrow). Tracing downwards on the series
of peels, scalariform bordered pits are found on the lateral
wall of the same element. Therefore, this tracheary element has scalariform and laterally elongated bordered pits
on the lateral walls. However, because there are no borders around the scalariform-reticulate structure and no
primary walls appeared within the structure, the oblique
end wall appears to be perforated. In other words, this
element possibly could be a vessel member.
The secondary xylem has tracheary elements arranged
into radial files, each with an inner portion of large vessels (1–5 vessels wide) and an outer portion of smaller
tracheary elements. Several stems show an inner portion
that is about 3–5 vessels wide. These vessels increase in
diameter from less than 150 mm to 250 mm towards primary xylem (Figs. 2–5). The vessel outlines are round
(Figs. 3, 5, 14) or squarish (Figs. 2–5) in transverse section. In transverse section, the tracheary elements may
appear as tangential rows of cells of similar size and
shape (Fig. 4). In addition, in tangential section (Figs. 6
[left], 12) the end walls appear at similar levels. One stem
has large vessels arranged into radial files that are tangentially only 1–2 vessels wide, with each vessel up to
500 mm in diameter, but outer elements with a much
smaller diameter (Figs. 15–16). This latter specimen may
represent a different species, but there is insufficient material to establish a separate species at this time.
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Figs. 14–20. Vasovinea tianii. 14. Uni- to biseriate rays (r) and vessels with oblique (above) or almost horizontal (below) perforate end walls.
Slide PLY03–34; bar 5 100 mm, 3170. 15. A segment of wood in transverse section with large vessels that can be up to 500 mm in diameter.
Slide PLY02-E-1; bar 5 500 mm, 321. (Reprinted with permission from H. Li et al., 1996. Copyright 1996, American Association for the
Advancement of Science.) 16. Another section of the specimen in Fig. 15 showing vessel elements with oblique end walls (arrows) at roughly the
same level. Notice that the cell rows of the outer secondary xylem zone are interlaced, i.e., their oblique end walls are in a zigzag form. The
smaller perforation plate (left arrow) is enlarged in Fig. 17, and the larger perforation plate (right arrow) is enlarged in Fig. 18. PLY02, section E;
bar 5 200 mm, 340. 17. Enlargement from Fig. 16 showing an underdeveloped perforation plate with obliquely elongated borderless pits (left
arrow) whose primary wall (upper arrow) is planar without margo threads or tori. bar 5 10 mm, 31000. 18. Enlargement from Fig. 16 showing a
perforation plate. Notice that the smaller pores at the right edge lack borders and have a planar primary cell wall present (arrow). bar 5 10 mm, 31000.
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Overall, vessel elements can be up to 4500–5000 mm
long. Their planar end walls vary from short (Fig. 12,
right lower corner) to very long (up to 1200 mm long;
Fig. 12, left), from oblique (Figs. 12, 14 [upper two vessels], 16 [right arrow]) to almost horizontal (Fig. 14, lower left vessel). Most of the end wall is perforated with
multiseriate (up to 12 rows) pores (Figs. 7 [upper right],
8 [lower right], 11). In the central area, most pores are
large and roughly circular, 8 3 10 mm (Figs. 7, 11) and
up to 13 3 15 mm (Figs. 18 [middle left], 19 [right]), but
some pores are much larger and elliptical, up to 13 3 21
mm (Fig. 19, lower left). Although those pores in the
central area are completely perforated without remains of
border membranes, the pores in peripheral regions are
smaller and exhibit an incompletely dissolved primary
cell wall (Fig. 18, arrow) that is smooth and shows no
trace of margo threads or tori.
In transverse section, the outer zone, up to 20 cells
wide (6–14 cells wide in Figs. 2–4), contains tracheary
elements that are usually ;40 3 50 mm (a few up to 120
mm) in dimension and arranged in radial files alternating
with rays at every one to three files. One of the smaller
tracheary elements, ;120 mm in diameter, has a planar
end wall (Fig. 16, left arrow) with incomplete pores (Fig.
17). The plate exhibits obliquely elongated pits, which
have smooth rims (Fig. 17, left arrow), and a planar, partially dissolved primary wall (Fig. 17, upper arrow).
Thus, it has the same type of perforation pattern as in the
large vessels, though the dissolution is not as complete.
In other words, some tracheary elements in the outer zone
might be vessel elements, while others could be tracheids
with imperforate end walls. The lateral walls of both
large and small tracheary elements exhibit the same type
of alternately arranged, multiseriate, bordered pits (Figs.
7 [lower right], 11 [lower right], 13, 20). These bordered
pits are obliquely elliptical, 3 3 8 mm (Fig. 20, right
upper), to nearly circular, 6–8 mm in diameter (Fig. 13).
Rays consist of homocellular parenchymatous cells,
which are usually 8–15 mm wide (Fig. 4), 15–25 mm
long, 25–50 mm high (Figs. 7 [at left], 13 [at right], 20
[at left]), and each cross-field has $3–9 obliquely arranged pits (Fig. 7, at left). The xylic rays are well preserved, usually one to two cells wide (Figs. 4, 14) and
as tall as 60 cells. Between the cauline xylem segments,
there are wedge-shaped gaps (Figs. 2–6, 15 [arrows])
sometimes containing cellular remains that are over three
cells wide and could be medullary rays.
The region of the cambium and inner phloem appears
as a zone of amorphous cellular remains or as an empty
gap, due to the poor preservation. In several transverse
sections, there is a narrow, dense cellular zone, surrounding the secondary xylem (Figs. 2–3), composed of 2–4
small cells, which are usually rounded rectangular in
shape, ;15 mm in diameter, and have lumens commonly
6–8 mm in diameter. In tangential section, they are elon-
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gate, but their lengths are unknown because of their poor
preservation. These cells might be the remains of the
phloem fibers.
A pair of vascular traces (Fig. 2, ‘‘T’’), each ;750 mm
in diameter, are found in the cortex, outside a gap (Fig.
2, arrow) between two cauline segments. The two traces
are of similar size and appear to originate from within
the gap, resulting in a unilacunar two-trace pattern. The
trace on the left appears to have been just pinched off
from the small-celled, side part of a main cauline xylem
segment. The right trace is bilaterally symmetrical and
ring-shaped with its abaxial side wider than the adaxial
side (only 2–3 cells wide; Fig. 4, upper). The abaxial side
has seven or more tracheids, each up to 40 mm in diameter, radially arranged into files. These tracheids represent the primary and, possibly, secondary xylem. The
central area of the vascular ring is usually empty, occasionally containing the remains of crushed parenchyma
cells. This type of trace structure (Figs. 2, 4) may represent the vascular traces of a leaf.
Compound hook structure—On the right side of Fig.
1 is a narrow branching axis, or a ‘‘compound hook,’’
which is ;4 cm long and has two pairs of opposite
branches. Note that this figure includes both transverse
and longitudinal sections of a stem (left) and the compound hook (right). The attachment and branching pattern of the compound hook were determined by examining the part and counterpart and a series of peels. The
main axis of the compound hook, 3 mm in diameter, extends ;1 cm from the stem (in the box) through the matrix and then branches the first time to form a pair of
lateral hook tips. The lower one was obliquely cut
through and left an oblique section, while the upper one
was preserved in the counterpart (Fig. 1, large arrow).
Then, the main axis becomes thinner (1.6 mm in diameter) and extends ;1.6 cm and branches again, resulting
in a second pair of lateral hook tips and a terminal tip,
each ;0.8 mm in diameter at their bases. With additional
peels, the longitudinal section of the main axis of the
compound hook and an oblique section of the upper hook
tip of the second pair were exposed. These lateral and
terminal hook tips curve backwards and are arranged in
roughly the same plane. More details of the attachment
of the compound hook to the main axis (Fig. 3, lower
right) are shown in a transverse section which is ;5 mm
lower from the section in Fig. 2. Here, one large vascular
trace (Fig. 3, ‘‘H’’) is relatively well preserved in an
oblique section of the compound hook axis. This vascular
trace is crescent shaped, bilaterally symmetric, and opens
towards its adaxial side where the parenchyma cells occur.
As in the stem, the main axis of the compound hook
also has sparganum cortex. The tracheids in this main
axis are usually 20–45 mm in diameter and have helical
←
(Reprinted with permission from H. Li et al., 1996. Copyright 1996 American Association for the Advancement of Science). 19. Partial perforation
plate of another vessel showing elliptic-circular pores without borders. The right side shows the plate just as dissolved out of the limestone matrix
in which the primary walls and the borders are inferred to have been missed before the preparation. LPY02; bar 5 10 mm, 31000. 20. Longitudinal
section showing broken parenchyma ray cells on the left and obliquely elongated (right upper) to circular (right lower) bordered pits on the lateral
wall of a secondary tracheid. LPY02; bar 5 18.5 mm, 3540.
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thickening, but a few tracheids are 15–23 mm in diameter
and have smaller, scalariform to transversely elongated,
bordered pits. Distally, the vascular cells gradually become reduced in size and number and eventually vanish
and leave only a hollow center surrounded by densely
packed, thick-walled parenchyma cells, as seen in better
preserved, dispersed hooks, which are 0.8 mm in diameter at their basal parts (Figs. 23, 24).
DISCUSSION
The permineralized stems of Vasovinea tianii exhibit
many well-preserved anatomical structures. We will discuss several structures before we analyze the implications
of the fossil characteristics for determining the affinities,
systematic relationships, and ecology. The tendril-like trichomes have been previously reported as tendril-like
structures because of their curvature (H. Li, Taylor, and
Taylor, 1992, 1993). We have changed the term because
they lack vascular tissues, and their basal parts appear to
be similar to the glandular trichomes in terms of their
structure and epidermal and cortical origin.
The vessels in living plants are widely believed to have
evolved from vertically linked tracheids by the dissolution of the primary cell walls between pit pairs on their
end walls. One type of vessel has foraminate perforation
plates, which develop by the loss of the pit membranes
between circular bordered pit pairs. This type is characteristic of gnetophytes, whose circular bordered pits usually have pit membranes with tori and margo threads (Carlquist, 1996a, b, c), and pores with the remains of the
circular borders that may be slightly raised. Another type
of vessel has scalariform perforation plates, which develop by the loss of the pit membranes (that have a uniform construction with micropores) between scalariform
bordered pit pairs on the highly inclined, elongate, planar
end walls (Carlquist, 1996a, b, c). This type of vessel
commonly occurs in some ferns (e.g., Carlquist and
Schneider, 1997; Schneider and Carlquist, 1998) and basal angiosperms (e.g., Bailey, 1944; Carlquist, 1992, 1994,
1996a), but derived angiosperms may have vessels with
simple perforations that evolved from the scalariform
type.
The vessels of Vasovinea tianii in the secondary xylem
also appear to develop by the dissolution of the pit membranes between pit pairs on the end walls, and the roughly round pores make the vessels superficially similar to
Fig. 32. Reconstruction of stem of Vasovinea tianii Li et Taylor
with compound hooks and actinodromous Gigantopteris-type leaves.
the foraminate type rather than the scalariform type.
However, on a closer examination, we found that the vessels of V. tianii are different from the foraminate type.
First, the perforation plate is planar (e.g., Figs. 11, 16)
and the number of pores is high (e.g., Figs. 7, 11, 14, 18,
19). Second, some pores are actually transversely elongate (not circular, e.g., Fig. 19) and lack borders (compared pores in Fig. 11 to bordered pits in Fig. 13). Third,
within some pores the incompletely dissolved pit membranes are planar and lack tori and margo threads (Figs.
17, 18). Therefore we call these vessels foraminate-like
to distinguish them from those with typical foraminate
perforation plates. On the other hand, the possible vessel
←
Figs. 21–31. The trichomes of the Vasovinea tianii (Figs. 26 and 28) and other associated gigantopterid structures. 21. A compressed compound
hook structure with two pairs of branches. L9448–2; bar 5 1 cm, 32.4. 22. A compressed, incomplete compound hook with two hook tips (arrows)
associated with a Gigantopteris-type leaf that has compound round teeth (top). L9449; bar 5 1 cm, 30.9. 23. Longitudinal section of the broken
top part of a permineralized hook tip. Notice the hollow center. Slide L9414–1–1; bar 5 200 mm, 345. 24. Longitudinal section of a permineralized
hook tip, perpendicular to the section in Fig. 23. The upper end shows the oblique transverse section of the tip as it curves back and the end has
a small hollow center. Slide PLY02-C8(R)-2; bar 5 1 mm, 320. 25. Transverse section of the secondary vein of a Gigantopteris-type leaf showing
the cortical sclerenchyma strands (arrows) and a heart shaped xylem segment enclosed by a poorly preserved cell layer. Slide PLY02-B7; bar 5
200 mm, 356. 26. A pair of trichomes, the one on the left has a large apical cell. Slide L9407-B-T2; bar 5 200 mm, 345. 27. A compressed stem
(at right bottom), possibly belonging to Vasovinea tianii, associated with two pieces of Gigantopteris-type leaves that have complex reticulate
venation (arrows). Note the stem with vertical ribs and grooves. L9426; bar 5 1 cm, 31. 28. A glandular trichome with a tapered apical cell. Slide
L9407-3-2-2; bar 5 200 mm, 345. 29. A vessel-bearing, permineralized stem associated with a leaf of Gigantopteris meganetes Tian and Zhang
(1980) that has complex mesh venation and the compound, rounded teeth. PLY03; bar 5 1 cm, 31.5. 30. Enlargement from Fig. 29 showing the
vessels in the stem in oblique section (top). Arrowhead points to part of a tendril-like trichome in the matrix. Slide PLY03–11; bar 5 2 mm, 36.5.
31. A cross section of a narrow midrib of a Gigantopteris-type leaf has lamina remains (left upper) and radial rows of tracheids (possibly of
secondary xylem) surrounding the tracheids of the triangle-shaped primary xylem in the center. Slide PLY02-C3-43-2; bar 5 200 mm, 370.
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in the metaxylem appears to be similar to the scalariform
type in general structure.
Another interesting and important structure is the compound hook. The hook tips are anatomically identical
with the isolated, permineralized ones (Figs. 23, 24) associated with Vasovinea stems and Gigantopteris-type
leaves. Also they are morphologically well matched with
the compressed compound hooks (Figs. 21, 22) from the
same locality. For example, the compressed compound
hook shown in Fig. 21 has a 1.2 cm long basal axial part,
a 1.4 cm long middle axial section, and five hook tips
(the terminal tip is broken), with 2.6, 1.6 and 0.8 mm
diameters, respectively. As with thorns and tendrils, the
compound hooks could be modified from stems or leaves.
We suggest that the compound hook of Vasovinea may
be modified from a leaf, based on the following evidence:
(1) it has a bilaterally symmetrical, crescent-shaped vascular trace (Fig. 3, ‘‘H’’), (2) the hook tips are arranged
in the same plane, and (3) the branching pattern is similar
to pinnate leaf venation.
Affinity—Several lines of evidence show that Vasovinea tianii is a member of the gigantopterids. The most
important evidence comes from the presence of a permineralized compound hook (Fig. 1), which is attached
to the permineralized stem (Fig. 3, at right). This type of
compound hook structure is unique to gigantopterids and
has not been reported from other fossil or extant plants
(see Menninger, 1970). Significantly, the structure of the
compound hook is identical with those found from the
early Late Permian Gigantopteris floras of Shanxi (5
Shansi in Halle, 1929) Province, northern China (Halle,
1929), and Fujian Province, southern China (Yao, 1983).
Halle (1929) interpreted the hook-like structures as modified leaves of Gigantopteris nicotianaefolia. In 1995,
one of us (Hongqi Li) borrowed and reexamined some
of the Shanxi specimens from the Swedish Museum of
Natural History. He confirmed that one of the gigantopterid leaves had thickened pinnate secondary veins that
distally curved backwards to form hooks, but the basal
part of each secondary vein still bore bilaterally a small
amount of lamina. Thus, the Shanxi specimen clearly
demonstrates a transitional type from a pinnately veined
gigantopterid leaf to a compound hook with opposite
hook tips. Our analysis of the permineralized compound
hooks is in agreement.
Additional features showing the gigantopterid affinity
include the presence of sparganum cortex, prickles, trichomes, and the configuration of the vascular trace. A
similar sparganum cortex is commonly known in many
Paleozoic seed ferns, such as the Carboniferous lyginopterids, medullosans, and callistophytes. Some species,
such as Heterangium kentuckyensis (Pigg, Taylor, and
Stockey, 1987), Microspermopteris aphyllum (Pigg,
Stockey, and Taylor, 1986), and Callistophyton boyssetii
(Rothwell, 1975, 1981) even have similar prickle/trichome-like structures (called ‘‘cortical wings’’ in the first
two references). However, among the plants reported
from the Upper Permian flora of western Guizhou, a sparganum cortex and pickles/trichomes are only found in
gigantopterids (see Tian et al., 1996). These structures
are characteristic of the leaf midribs of Gigantonoclea
guizhouensis (H. Li et al., 1994), the stems of Aculeovi-
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nea yunguiensis (H. Li and Taylor, 1998), and Vasovinea
tianii. The prickles were described as aculei (H. Li and
Tian, 1990) and spines (H. Li et al., 1994) and have been
redefined as prickles (H. Li and Taylor, 1998) because of
their epidermal and cortical origin, and lack of vascular
tissue. Although the prickles in V. tianii are fewer in
number, smaller, and contain fewer thick-walled parenchyma cells, they are similar to prickles of G. guizhouensis and A. yunguiensis in structure and origin. Finally, a sparganum cortex also is found around the vascular bundles in Gigantopteris-type leaves (Fig. 25).
The leaf traces (;750 mm in diameter; Figs. 2 [‘‘T’’].
Fig. 4 [upper]) in the stem are identical to the vasculature
(;350 mm in diameter; Fig. 31, central part) in a section
of a narrow, Gigantopteris-type leaf midrib, in terms of
the radial rows of tracheids surrounding the triangleshaped primary xylem. The reduction in the diameter of
the vasculatures is reasonable, considering they grow out
from the stem cortex through to the midrib. Some thicker,
secondary veins of a large-sized, Gigantopteris-type leaf
(possibly a different species from that of Fig. 31), have
a heart-shaped vasculature (Fig. 25), and the tracheids
(each up to ;40 mm in diameter) are also arranged in
radial rows. All these radially arranged tracheids are separated by parenchyma cells, so they appear to belong to
secondary xylem. This distinguishes them from those Uor V-shaped vasculatures in Gigantonoclea guizhouensis
leaf veins, which consist only of primary xylem. Therefore, these similar vasculatures suggest that Vasovinea
and Gigantopteris-type leaves belong to the same kind
plant.
The biological relationship of Vasovinea tianii stems,
Gigantopteris-type leaves, and the compound hooks also
is supported by their intimate association. More than a
dozen compression leaf species of three gigantopterid
genera have been reported from the Permian flora of
western Guizhou (Gu and Zhi, 1974; Tian and Zhang,
1980; Zhao et al., 1980). Except for the rare Linophyllum
xuanweiensis, the other species belong to Gigantonoclea
(with simple net veins) or Gigantopteris (with complex
reticulate veins). These three genera all have a midrib
(primary vein) and pinnate secondary veins. Based on our
collections from the Guizhou Flora, we have recently recognized an actinodromous type of gigantopterid leaf that
has either three or five primary veins (H. Li and Taylor,
1997a). Both Gigantopteris and the actinodromous leaves
have complex reticulate venation, and both are so large
that it is difficult to tell from which type a leaf fragment
with complex netted veins comes (e.g., Figs. 22, 27).
Therefore, we prefer to use the term Gigantopteris-type
for all gigantopterids with complex reticulate venation.
A gigantopterid leaf similar to Gigantonoclea guizhouensis has been reconstructed together with prickly
Aculeovinea yunguiensis stems (H. Li and Taylor, 1998).
Gigantopteris-type leaves are frequently associated with
compressed stems that are similar to compressed stems
of A. yunguiensis in having tiny ribs (Fig. 27), but with
fewer black dots than the latter. The tiny ribs and the dots
appear to be the remains of a sparganum cortex and the
broken bases of trichomes or prickles of Vasovinea, respectively. Gigantopteris-type leaves also are frequently
associated with the compressed hooks, e.g., the compound hook in Fig. 21. Another specimen has two hooks
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(Fig. 22, arrows) and is associated with a leaf that has
complex reticulate venation and compound rounded
teeth, similar to the leaf in Figs. 29–30. In permineralized
materials, Gigantopteris-type leaves are frequently associated with Vasovinea stems as demonstrated in Figs. 29–
30. In one of our specimens (L9407), all of the wellpreserved leaves have complex reticulate venation, and
all of six or more anatomically preserved stems have vessels.
Although associational evidence strongly supports the
inference that Gigantopteris-type leaves, compound
hooks, and Vasovinea tianii stems could belong to the
same plant species, whether the reticulate leaves are actinodromous or pinnately veined is still uncertain. We
reconstructed the V. tianii stems with the actinodromous
Gigantopteris-type leaves (Fig. 32) at this time, because
in sample PLY04 the only leaf that is associated with the
single V. tianii stem is of the actinodromous type. We
also included the tendril-like trichomes, prickles, and
compound hooks, since these structures are attached to
the stems. We placed the hooks in a subopposite arrangement with the leaves because the location of the transverse section with the hook trace (Fig. 3) is ;5 mm below the transverse section with the possible leaf traces
(Fig. 2). However, this reconstruction may need to be
further refined in the future in terms of whether the Vasovinea stems may actually have actinodromous or pinnately veined leaves, or both.
Systematic relationships—Although Vasovinea tianii
is placed in the Gigantopteridales, it is still uncertain to
which higher category the order belongs. Gigantopterids
were first considered to be ferns (Schenk, 1883) and then
seed ferns (White, 1912; Asama, 1959). The latter view
is supported by X. Li and Yao (1983) who reported an
impression specimen with both seed-bearing taeniopteroid and Gigantonoclea fukienensis leaves. However,
whether the axes of those leaves were organically connected or just overlapped together appears unclear.
Although there are no permineralized reproductive organs to clarify whether gigantopterids belong to seed
ferns or other groups, the anatomy of Aculeovinea yunguiensis suggests that the gigantopterids were seed plants
(H. Li and Taylor, 1998). The combination of characters
in Vasovinea tianii, such as vessels, a eustele, sparganum
cortex, and secondary xylem, separates it from the pteridophytes. These characteristics are typical of Paleozoic
seed ferns, such as Heterangium, Microspermopteris, and
Callistophyton (Taylor and Taylor, 1993; Pigg, Stockey,
and Taylor, 1986; Pigg, Taylor, and Stockey, 1987), although none of these genera share the full suite of characters of Vasovinea. In particular, none of them have reticulate-veined leaves and vessel-bearing stems. Although
vessels also are found in some extant ferns and fern allies,
such as some ferns (Jeffrey, 1917; Bliss, 1939; White,
1961; Carlquist and Schneider, 1997; Schneider and Carlquist, 1998), Selaginella (Duerden, 1934), and Equisetum
(Bierhorst, 1958), these vessels commonly have only scalariform perforations and none of these plants have both
a eustele and secondary xylem.
In extant seed plants only gnetophytes and angiosperms typically have vessels, and their vessels are of the
foraminate and scalariform/simple types, respectively
GIGANTOPTERID
VASOVINEA
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(see above). There is considerable controversy over
whether the two types of vessels represent two different
evolutionary lineages or had a single origin in gnetophytes and angiosperms (Bailey, 1944; Young, 1981; Muhammad and Sattler, 1982; Carlquist, 1992, 1994, 1996a).
However, the foraminate-like vessels of Vasovinea tianii
differ from both those of gnetophytes and angiosperms.
Although superficially similar to those of the gnetophytes, the perforation plate of Vasovinea is planar, has
many more pores (which are borderless and can be transversely elongated), and has pit membranes (when they
exist) without tori or margo threads. This type of foraminate-like perforation plate is not known from angiosperms, although the scalariform bordered pits and the
possible vessels in the metaxylem of Vasovinea resemble
those of angiosperms. Therefore, although these vessels
are very important in tracing their origin, we cannot draw
a comprehensive conclusion of the systematic relationships of the gigantopterids based on vessel features alone.
Preliminarily results, based on phylogenetic analyses of
a broad suite of characters (H. Li and Taylor, 1997b) and
molecular fossil data (Taylor et al., 1998), suggest that
gigantopterids are embedded well within the seed plants
and may be another member of the anthophyte clade.
Paleoecology—Halle (1929) reported some hook-bearing gigantopterids from central Shanxi and suggested that
the gigantopterids grew as lianas in a tropical habitat. Yao
(1983) reported additional hooks and also considered the
gigantopterids as lianas growing in a lowland tropical
forest. Geographically, Guizhou has been suggested to
have been in a tropical forest biome during the Late
Permian (Lin, Fuller, and Zhang, 1985; Tian et al., 1990;
Nie, Rowley, and Ziegler, 1990; Isozaki, 1997). Our material strongly supports these paleoecological predictions
and provides some additional ecophysiological interpretations.
The morphology, anatomy, and reconstruction of Vasovinea tianii support the interpretation that it grew as a
vine or liana. In extant lianas, hooks, thorns, tendrils, and
spines/prickles function as attachment organs so the slender plants can climb. In particular, hooks only have been
found in vines, where they are considered very efficient
climbing organs (Menninger, 1970), and define a group
called the hook climbers (Putz and Holbrook, 1991). The
tendril-like trichomes and prickles of V. tianii might also
have provided an additional climbing mechanism.
Anatomical features such as a segmented xylem and
the distribution and structure of its vessels also support
the inference that Vasovinea tianii was a liana. Just like
many living lianas, V. tianii contained xylem segments
dispersed among parenchyma cells. The inflexible xylem
segments within soft parenchyma tissues function like
‘‘multistranded cables’’ so that the liana stems could have
withstood considerable deformation while maintaining
the conductive function (see Carlquist, 1991; Putz and
Holbrook, 1991). Vasovinea tianii stems have large vessels abruptly occurring at the inner portion of the secondary xylem and small vessels in the outer portion (and
possibly in the metaxylem), an arrangement resembling
that found in certain extant lianas (Carlquist, 1991). The
pores of Vasovinea have completely lost their borders and
are elongate (8 3 10 to ; 13 3 15 mm; Figs. 7, 11, 18–
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19) and larger than bordered pits on lateral walls (Figs.
11 [lower right], 20). In extant lianas, vessel end walls
tend to be more thoroughly perforated than those of tree
and shrubby genera in the same family. The vines may
have simple perforations with reduced borders, rather
than scalariform perforations, or have large vessels with
simple perforations and small vessels with scalariform
perforations, instead of all scalariform vessels, or may
have scalariform perforations with fewer bars than in
trees (Carlquist, 1991). Presumably, to overcome the
large resistance to water flow in tracheary elements and
to complement the rapid water loss from the relatively
large leaves, the plants need an extremely efficient waterconducting tissue in their stems (see Ewers, Fisher, and
Chiu, 1989).
Other vessel parameters can also be correlated to habit.
Lianas typically have larger vessel diameters (from an
average of 157 mm to 558 mm in diameter; Carlquist,
1975) than closely related woody trees in both Gnetum
and dicots (Ewers, 1985; Ewers and Fisher, 1989; Ewers,
Fisher, and Chiu, 1990; Fisher and Ewers, 1995). Bamber
and Welle (1994) reported that many liana species from
the Queensland rain forest have vessels 14–57% larger
than tree species of the same genera, and the largest vessel was 610 mm in diameter. In living lianas, the widest
vessel members tend to be the longest (Ewers and Fisher,
1989; Bamber and Welle, 1994). Similarly, the vessel
members of Vasovinea, up to 500 mm in diameter and
4500–5000 mm in length, are in the range of the largest
and longest among all plants, both living and extinct.
The reconstruction of the thin Vasovinea stems with
the large Gigantopteris-type leaves also resembles many
extant lianas that usually possess high leaf-area to stemdiameter ratios (Carlquist, 1975, 1991). Many cordate,
actinodromous gigantopterid leaves are larger than 400
cm2, with some observed in the field up to 1600 cm2, but
these large leaves are associated with slender stems, commonly no more than 1 cm in diameter.
It is also possible to predict the placement of Vasovinea within the forest structure. Extant lianas and vines
with large, cordate leaves and long petioles usually grow
in sunny areas, while those with small, narrow leaves and
short petioles normally grow in more shady environments
(Givnish and Vermeij, 1976). Some Gigantopteris-type
leaves have been found with well-differentiated palisade
and spongy cells (Fig. 25, left) and guard cells sunken in
the stomata (Guo, Tian, and Chang, 1993). The mesophyll differentiation is related to plant species and to habitat with increased palisade differentiation related to increased exposure to light (Esau, 1965). This is in contrast
to the undifferentiated mesophyll as in Gigantonoclea
guizhouensis (H. Li et al., 1994). We suggest that both
Gigantonoclea and Gigantopteris lived in a similar habitat based on the co-occurrence in the sediment, but that
the Gigantopteris-Vasovinea plant grew in the sunny canopy, while the Gigantonoclea-Aculeovinea plant grew in
the shady understory.
In summary, Vasovinea tianii is mainly characterized
by its compound hooks, sparganum cortex, eustelic primary vascular architecture, foraminate-like vessels in the
secondary xylem, and possible vessel elements with scalariform-reticulate structures and tracheids with scalari-
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form or reticulate bordered pits in the metaxylem. These
morphological features suggest that V. tianii represents a
unique seed plant taxon, but its phylogenetic relationships
to seed ferns, gnetophytes, and angiosperms remain to be
further analyzed. The presence of compound hooks and
other anatomical features clearly shows that V. tianii belongs to the gigantopterids, while additional evidence
from the associated permineralized and/or compressed
materials indicates that it should be reconstructed together with Gigantopteris-type leaves as lianas that grew in
the Permian tropical rain forest of western Guizhou, China.
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