Vessel-Bearing Stems of Vasovinea Tianii Gen. Et Sp

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 ef®cient adaptation to allow the slender stems to conduct suf®cient 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 the distinctive leaves, anatomically preserved reproduc- extensively from the Lower Permian and possibly into tive organs have not been found so that the systematics the lowest Lower Triassic sediments throughout south- of the group has been uncertain. eastern Asia (mostly from China), as well as from several Recently, some permineralized gigantopterid leaves Lower Permian sites in Texas and Oklahoma, USA. This and axes have been reported with many anatomical char- group was ®rst reported by Schenk (1883) from Hunan acteristics that can help in determining the relationships Province, China, and currently includes more than 40 of gigantopterids to other vascular plants. The perminer- taxa (H. Li et al., 1994). The distinctive characteristics alized leaves of the gigantopterid Delnortea abbottiae, of gigantopterids are their large compound or simple reported from Texas, USA, are suggested as being struc- leaves, which are variable in morphology, ranging from turally similar to gnetophytes (Mamay et al., 1988). In oblong to roughly round shape, entire to toothed margin, contrast, the permineralized leaves of Gigantonoclea and simple to complex reticulate venation. Convention- guizhouensis, from the Upper Permian in Guizhou, Chi- ally the group has been classi®ed as ferns (Schenk, 1883) na, exhibit many features similar to those of angiosperms or seed ferns (White, 1912; Asama, 1959; X. Li and Yao, (H. Li and Tian, 1990; H. Li et al., 1994). Two types of 1983). In terms of relationships to other plants, Asama permineralized gigantopterid stems also are found asso- (1974, 1982, 1988) proposed that the simple-leafed gi- ciated with the Guizhou gigantopterid leaves (H. Li, Tay- gantopterids could have given rise to the angiosperms, lor, and Taylor, 1992, 1993). One type is the prickly Acu- while X. Li and Yao (1983) interpreted their reconstruc- leovinea yunguiensis (H. Li and Taylor, 1998), which is tion of the reproductive organs of Gigantonoclea fuki- considered a seed plant. Another type containing vessels enensis as being ``parti-angiosperms'' in nature. Despite has been reported preliminarily (H. Li, Taylor, and Taylor, 1996). 1 Manuscript received 16 July 1998; revision accepted 25 March Before the report by H. Li, Taylor, and Taylor (1996), 1999. the fossil record of vessels could be traced back to the This paper represents part of Hongqi Li's dissertation submitted in partial ful®llment of the requirements for the Ph.D. degree at the Ohio Early Cretaceous. In extant plants, vessels consist of ver- State University, Columbus, Ohio. Hongqi Li thanks Drs. Edith L. Tay- tically linked tracheary elements with perforate end walls lor and Thomas N. Taylor for professional help, and Dr. William A. so that they conduct water much more ef®ciently than Jensen for guidance and encouragement. The authors thank Dr. Cheng- tracheids with imperforate end walls. Vessels are com- sen Li and the Botanical Institute of Beijing for support in fossil-col- monly found in angiosperms and gnetophytes, with rarer lecting; Dr. Paul Kenrick and the staff of the Swedish Museum of Nat- ural History for loan of gigantopterid specimens; and Drs. Sherwin occurrences in non-seed plants (see Discussion). Vessels Carlquist, Kathleen B. Pigg, Leo J. Hickey, and an anonymous reviewer in living seed plants have been classi®ed in two types, for their valuable comments on the manuscript. This research is partially i.e., foraminate vessels in gnetophytes and scalariform supported by the Geological Society of America Research Grant ones (and/or their derived simple form) in angiosperms 5195-93, the Graduate Student Alumni Research Award, Graduate (Bailey, 1944; Carlquist, 1992, 1994, 1996a). Vasovinea School of the Ohio State University, and grants from the Research and University Graduate School of Indiana University, and the Academic tianii is different from the above two types, possessing Affairs of Indiana University Southeast. unique, foraminate-like vessels in the secondary xylem 2 Author for correspondence (e-mail: [email protected]). and a possible scalariform-reticulate vessel in the meta- 1563 1564 AMERICAN JOURNAL OF BOTANY [Vol. 86 xylem. Therefore, the discovery of vessels in gigantop- cm in diameter, bearing compound hooks, prickles, and terids is important not only as the earliest fossil record glandular and tendril-like trichomes. Cortex with paired of vessels, but also in analyzing the systematic relation- vascular traces and sparganum structure in the outer part. ships and the ecological aspects of the group. Eustele with parenchymatous pith and mesarch protoxy- To complement the preliminary study (H. Li, Taylor, lem, consisting of tracheids with annular, helical, or he- and Taylor, 1996), we now provide a comprehensive de- lical-scalariform thickenings. Centripetal metaxylem tra- scription of the permineralized, vessel-bearing gigantop- cheids commonly consisting of one to two layers, while terid stems and establish them as a new taxon, Vasovinea centrifugal metaxylem usually consisting of two to three tianii Li et Taylor gen. et sp. nov. With several lines of layers of tracheary elements; metaxylem tracheary ele- evidence from both permineralized and compression ments with scalariform and/or transversely elongated bor- specimens, we also demonstrate that the new taxon is a dered pits on their lateral walls. Outer portion of the sec- member of the gigantopterids, reconstruct it together with ondary xylem consisting of radial ®les of tracheids and Gigantopteris-type leaves, analyze its possible habit, and smaller vessels. Lateral walls of tracheary elements in brie¯y discuss its systematic relationships to seed plants. secondary xylem exhibiting multiseriate, alternate, and transversely elongate to circular bordered pits. The inner MATERIALS AND METHODS portion of the secondary xylem consisting of large vessels with diameter increasing from ϳ150 to 250 (up to Limestone and mudstone samples with gigantopterid stems and 500) ␮m towards the primary xylem; vessel elements ver- leaves were collected from a talus pile mined from the upper and middle tically connected by foraminate-like perforation plates on parts of the Xuanwei Formation of the Upper Permian at the Shan-Jian- the long, inclined (usually) to short, almost horizontal Shu site, Yueliangtian Coal Mine in Panxian County, Guizhou, China, (occasionally) end walls, each plate with multiseriate, al- in 1993. Additional information about the locality and stratigraphy can ternate, obliquely elliptical to circular pores without bor- be found in H. Li et al. (1994) and H. Li and Taylor (1998). ders. Homocellular, heteroseriate rays occurring every Permineralized specimens from ®ve limestone samples (L9407, PLY02, PLY03, PLY04, and L9414), and compressed specimens from one to three radial tracheary ®les, consisting of uni- to three mudstone samples (L9426, L9448, and L9449) were used. All bi-seriate xylic rays and multiseriate medullar rays be- samples contain gigantopterid foliage and stem(s) in each, and some tween xylem segments. have additional compound hooks as well as other structures, although not all of these organs from each of the samples are ®gured in this HolotypeÐSlides L9407-C-B2, L9407-C-B16, and paper. Samples PLY03 and PLY04 are small, but each contains a Va- L9407-D-T2. Figs. 1±4, 6. sovinea tianii stem and a piece of Gigantopteris-type leaf. Sample L9407 has numerous pieces of Gigantopteris-type leaves and several ParatypesÐSlides PLY02-C10-1-1, PLY02-E-1, pieces of V. tianii stems. PLY02 is a large sample, weighing more than PLY03±01, PLY03±06, PLY03±07, PLY03±11, PLY03± 8 kg, and contains hundreds of pieces of permineralized (usually gi- 34, and PLY04-B; Specimens PLY02 and PLY03. Figs. gantopterid) plant organs, including at least two types of gigantopterid 5, 7±20, 29±30. leaves (Gigantopteris and Gigantonoclea), two types of gigantopterid The slides and specimens of both the holotype and stems (V. tianii and Aculeovinea yunguiensis; H. Li and Taylor, 1998), paratypes have been deposited in the National Museum and some undescribed reproductive organs. Specimens of Vasovinea of Plant History of China at the Institute of Botany, Chi- and Gigantopteris in this sample are relatively fewer in number com- nese Academy of Sciences, Beijing, China. pared to those of Aculeovinea and Gigantonoclea. The permineralized stems were sectioned and prepared using the EtymologyÐThe generic name is composed of vaso- well-known cellulose acetate peel technique (Phillips, 1976). Areas with ([L] ϭ vessel) and vinea ([L] ϭ vine) indicating a liana interesting structures from the peels were trimmed, cleaned, and mount- stem with vessels. The speci®c name is proposed in honor ed on microscope slides for further observations. Occasionally speci- of Professor Baolin Tian, the Beijing Graduate School, mens were peeled in both the transverse and longitudinal sections to show the structural correlation of both sections (Figs. 1, 6). Specimens China University of Mining and Technology, for his con- were photographed with an MP-4 camera using 4 ϫ 5 ®lm or with an tribution to the study of the Gigantopteris ¯ora of west- Olympus 35-mm camera mounted on an Olympus Steroscan dissecting ern Guizhou, China. microscope. To prepare scanning electron microscope (SEM) samples, several permineralized wood pieces with vessels were etched with a 1% LocalityÐYueliangtian Coal Mine, Panxian County, HCl solution for ϳ20 min so that the diluted solution could dissolve Guizhou Province, China. the calcium carbonate slowly to expose cellular structures, e.g., the perforation plates (Figs. 16±19). Then they were mounted and sputter coat- Stratigraphic occurrenceÐLower and Upper Xuan- ed with gold before being examined with SEM. The compressed spec- wei Formations, Upper Permian. imens were directly photographed with a Polaroid MP-4 camera. AgeÐLongtanian-Changxingian, Late Permian. SYSTEMATICS AND DESCRIPTION DescriptionÐThe stems are usually Ͻ1 cm in diameter OrderÐ Gigantopteridales X. Li et Z. Yao (1983) and up to 5 cm in length. One stem measured ϳ4 ϫ 6 mm in transverse section (Figs. 1±3, 6), while others were FamilyÐGigantopteridaceae Koidzumi (1936) compressed and calculated to be ϳ1 cm in diameter (Figs. 5, 29±30). Well-preserved stems have an epidermis SpeciesÐVasovinea tianii gen. et sp. nov. and hypodermis. The epidermis consists of one layer of small cells that have relatively thick walls. The layer is Generic and speci®c diagnosisÐStems slender, ϳ1 ϳ10 ␮m thick and its cells are ϳ10 ␮m wide and 8 to November 1999] LI AND TAYLORÐVESSEL-BEARING GIGANTOPTERID VASOVINEA FROM CHINA 1565

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 ϭ 4 mm, ϫ2.5. 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 ϭ 1 mm, ϫ16. 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 ϭ 1 cm, ϫ16. 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 ϭ 0.5 mm, ϫ36. 5. Stem with vessels in the xylem segments and trichomes on the surface of the stem and embedded in the surrounding sediments (arrowheads). Slide PLY04- B; bar ϭ 2 mm, ϫ7.5. 1566 AMERICAN JOURNAL OF BOTANY [Vol. 86

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 L9407- C-B16; bar ϭ 1 mm, ϫ16. 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-®eld pitting of secondary xylem tracheids on the left side. Slide PLY03±01; bar ϭ 50 ␮m, ϫ200. 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 ϭ 200 ␮m, ϫ68. 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 ®gure, and a protoxylem tracheid with helical to helical-scalariform thickenings on right. Slide PLY03±06; bar ϭ 50 ␮m, ϫ200. 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 ϭ 50 ␮m, ϫ200. 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 ϭ 50 ␮m, ϫ200. 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 ϭ 200 ␮m, ϫ42. (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 ϭ 50 ␮m, ϫ200. November 1999] LI AND TAYLORÐVESSEL-BEARING GIGANTOPTERID VASOVINEA FROM CHINA 1567

20 ␮m long. Beneath the epidermis are 2±4 layers of xylem segments of different sizes that are either well pre- hypodermal cells that are commonly ϳ40±50 ␮m long served or somewhat crushed. In transverse section, each and 15±40 ␮m in diameter, and densely arranged with large woody segment appears as a sector of an annulus, the larger cells occurring to the outside and smaller ones with the inner side longer than the outer side, because of to the inside. Attached to the stems are compound hooks the larger vessels to the pith side and smaller tracheary (see below) and a variety of appendages including prick- elements to the outside. les and glandular and tendril-like trichomes. Along the periphery of the pith, primary xylem bundles and a few solitary tracheids are embedded among AppendagesÐThe appendages are epidermal-cortical the parenchyma cells. Mesarch protoxylem strands can outgrowths and lack any vascular tissue. They are com- be found in the centers of some of the large bundles (Fig. monly found on stems, but some smaller appendages can 4, arrowhead at the bottom), but they are frequently dif- be found on the compound hooks (Fig. 1, right arrow- ®cult to distinguish. The protoxylem tracheids can be nar- head). The prickles on the stems are usually ϳ450 ␮m rower than 20 ␮m in diameter with annular to helical or (up to ϳ1000 ␮m) long and 450 ␮m (up to 550 ␮m) helical-scalariform thickenings (Fig. 9). The centripetal wide at their bases, but a narrower one found near the metaxylem usually is one to two cells wide (Fig. 4), and base of a compound hook is only ϳ250 ␮m wide at the the tracheids commonly are less than 50 ␮m in diameter base (Fig. 2, right arrow). Each prickle is covered by the and have scalariform (Fig. 9, left lower part) or 2±3 rows epidermis and internally composed of vertically elongate of transversely elongated, bordered pits (Fig. 9, arrow- parenchyma cells, 20±30 ␮m in diameter and 40±50 ␮m head). The centrifugal metaxylem commonly is 2±3 cells long. A few parenchyma cells beneath the epidermal cells wide (Figs. 4, 8 [left]), with the inner tracheary elements are narrower and have thickened cell walls. Some hy- being narrow and having scalariform bordered pits. The podermal cells (dark colored) beneath the base separate outer elements usually are large, up to 100 ␮mindi- the prickle from the inner part, suggesting that the prickle ameter, and have up to ®ve rows of transversely elon- is epidermal and cortical in origin. Structurally, these gated, bordered pits on the lateral walls. The elongated prickles are nearly identical to those of Aculeovinea yun- pits are arranged into obliquely opposite rows when two guiensis (H. Li and Taylor, 1998), but smaller in size. or three rows are present. In some of those with ®ve rows, Glandular trichomes can be found on both the stems the pit openings are only 2.5 ␮m high but can be up to (Figs. 26, 28) and the compound hooks. Generally, they 16 ␮m wide. However, as the row number increases, the are 500±2000 ␮m long and 500±1000 ␮m in diameter at pits appear to be alternately arranged and pit openings their bases. Their basal parts are similar to the prickles become narrower. in terms of their structure and the epidermal and cortical One centrifugal metaxylem element (Figs. 8 [arrow], origin. However, their apices consist of either several 10), 50 ␮m in diameter, has two types of wall structures. large cells (Fig. 28) or a single larger oval cell, 200 ␮m The tip of the tracheary element forms a long, highly in length and 100 ␮m in diameter, at the tip (Fig. 26). inclined end wall that has a scalariform-reticulate struc- The tendril-like trichomes (the tendril-like structures in ture (Fig. 10, upper arrow). The lower part shows a small H. Li, Taylor, and Taylor, 1992, 1993) are long and broken piece of its lateral wall with oval bordered pits curved in shape. These trichomes are ϳ300 ␮mindi- (Fig. 10, lower arrow). Tracing downwards on the series ameter and can be several millimetres long. They contain of peels, scalariform bordered pits are found on the lateral similar-shaped parenchyma cells, with the inner cells wall of the same element. Therefore, this tracheary ele- slightly enlarged. They may be preserved as tubes (Fig. ment has scalariform and laterally elongated bordered pits 30, arrowhead) when the inner parenchyma cells are no on the lateral walls. However, because there are no bor- longer preserved. In other sections, these trichomes often ders around the scalariform-reticulate structure and no appear as wart-like structures extending from the stems primary walls appeared within the structure, the oblique (Fig. 5, center) or circular rings (Fig. 5, arrowheads) em- end wall appears to be perforated. In other words, this bedded in the surrounding sediments. element possibly could be a vessel member. The secondary xylem has tracheary elements arranged Cortical histologyÐBeneath the hypodermis, in the into radial ®les, each with an inner portion of large ves- well-preserved stems, the cortex consists of a sparganum sels (1±5 vessels wide) and an outer portion of smaller structure (i.e., vertically parallel sclerenchymatous tracheary elements. Several stems show an inner portion strands alternating with vertical parenchymatous tiers; see that is about 3±5 vessels wide. These vessels increase in Taylor and Taylor, 1993) towards the outer side (Fig. 3, diameter from less than 150 ␮mto250␮m towards pri- bottom) and a wider parenchymatous zone towards the mary xylem (Figs. 2±5). The vessel outlines are round inside (Figs. 2, 3). The sclerenchyma cells are ϳ20 ␮m (Figs. 3, 5, 14) or squarish (Figs. 2±5) in transverse sec- in diameter and 1000±3000 ␮m long (Fig. 6, right). The tion. In transverse section, the tracheary elements may cortical parenchyma cells are roughly cuboidal, 45±70 appear as tangential rows of cells of similar size and (up to 95) ␮m in dimension, and vertically linked (Fig. shape (Fig. 4). In addition, in tangential section (Figs. 6 6, arrow). They are often damaged or crushed, leaving [left], 12) the end walls appear at similar levels. One stem empty spaces in the cortex (Figs. 3, 5, 6). has large vessels arranged into radial ®les that are tan- gentially only 1±2 vessels wide, with each vessel up to Vascular systemÐA eustelic primary architecture sur- 500 ␮m in diameter, but outer elements with a much rounds a poorly preserved pith, which contains cuboidal smaller diameter (Figs. 15±16). This latter specimen may parenchyma cells, 40±70 (up to 110) ␮m in dimension represent a different species, but there is insuf®cient ma- (Figs. 2, 3). The vascular cylinder is preserved in 5±9 terial to establish a separate species at this time. 1568 AMERICAN JOURNAL OF BOTANY [Vol. 86

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 ϭ 100 ␮m, ϫ170. 15. A segment of wood in transverse section with large vessels that can be up to 500 ␮m in diameter. Slide PLY02-E-1; bar ϭ 500 ␮m, ϫ21. (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 ϭ 200 ␮m, ϫ40. 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 ϭ 10 ␮m, ϫ1000. 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 ϭ 10 ␮m, ϫ1000. November 1999] LI AND TAYLORÐVESSEL-BEARING GIGANTOPTERID VASOVINEA FROM CHINA 1569

Overall, vessel elements can be up to 4500±5000 ␮m gate, but their lengths are unknown because of their poor long. Their planar end walls vary from short (Fig. 12, preservation. These cells might be the remains of the right lower corner) to very long (up to 1200 ␮m long; phloem ®bers. Fig. 12, left), from oblique (Figs. 12, 14 [upper two ves- A pair of vascular traces (Fig. 2, ``T''), each ϳ750 ␮m sels], 16 [right arrow]) to almost horizontal (Fig. 14, low- in diameter, are found in the cortex, outside a gap (Fig. er left vessel). Most of the end wall is perforated with 2, arrow) between two cauline segments. The two traces multiseriate (up to 12 rows) pores (Figs. 7 [upper right], are of similar size and appear to originate from within 8 [lower right], 11). In the central area, most pores are the gap, resulting in a unilacunar two-trace pattern. The large and roughly circular, 8 ϫ 10 ␮m (Figs. 7, 11) and trace on the left appears to have been just pinched off up to 13 ϫ 15 ␮m (Figs. 18 [middle left], 19 [right]), but from the small-celled, side part of a main cauline xylem some pores are much larger and elliptical, up to 13 ϫ 21 segment. The right trace is bilaterally symmetrical and ␮m (Fig. 19, lower left). Although those pores in the ring-shaped with its abaxial side wider than the adaxial central area are completely perforated without remains of side (only 2±3 cells wide; Fig. 4, upper). The abaxial side border membranes, the pores in peripheral regions are has seven or more tracheids, each up to 40 ␮m in di- smaller and exhibit an incompletely dissolved primary ameter, radially arranged into ®les. These tracheids rep- cell wall (Fig. 18, arrow) that is smooth and shows no resent the primary and, possibly, secondary xylem. The trace of margo threads or tori. central area of the vascular ring is usually empty, occa- In transverse section, the outer zone, up to 20 cells sionally containing the remains of crushed parenchyma wide (6±14 cells wide in Figs. 2±4), contains tracheary cells. This type of trace structure (Figs. 2, 4) may rep- elements that are usually ϳ40 ϫ 50 ␮m (a few up to 120 resent the vascular traces of a leaf. ␮m) in dimension and arranged in radial ®les alternating with rays at every one to three ®les. One of the smaller Compound hook structureÐOn the right side of Fig. tracheary elements, ϳ120 ␮m in diameter, has a planar 1 is a narrow branching axis, or a ``compound hook,'' end wall (Fig. 16, left arrow) with incomplete pores (Fig. which is ϳ4 cm long and has two pairs of opposite 17). The plate exhibits obliquely elongated pits, which branches. Note that this ®gure includes both transverse have smooth rims (Fig. 17, left arrow), and a planar, par- and longitudinal sections of a stem (left) and the com- tially dissolved primary wall (Fig. 17, upper arrow). pound hook (right). The attachment and branching pat- Thus, it has the same type of perforation pattern as in the tern of the compound hook were determined by exam- large vessels, though the dissolution is not as complete. ining the part and counterpart and a series of peels. The In other words, some tracheary elements in the outer zone main axis of the compound hook, 3 mm in diameter, ex- might be vessel elements, while others could be tracheids tends ϳ1 cm from the stem (in the box) through the ma- with imperforate end walls. The lateral walls of both trix and then branches the ®rst time to form a pair of large and small tracheary elements exhibit the same type lateral hook tips. The lower one was obliquely cut of alternately arranged, multiseriate, bordered pits (Figs. through and left an oblique section, while the upper one 7 [lower right], 11 [lower right], 13, 20). These bordered was preserved in the counterpart (Fig. 1, large arrow). pits are obliquely elliptical, 3 ϫ 8 ␮m (Fig. 20, right Then, the main axis becomes thinner (1.6 mm in diam- upper), to nearly circular, 6±8 ␮m in diameter (Fig. 13). eter) and extends ϳ1.6 cm and branches again, resulting Rays consist of homocellular parenchymatous cells, in a second pair of lateral hook tips and a terminal tip, which are usually 8±15 ␮m wide (Fig. 4), 15±25 ␮m each ϳ0.8 mm in diameter at their bases. With additional long, 25±50 ␮m high (Figs. 7 [at left], 13 [at right], 20 peels, the longitudinal section of the main axis of the [at left]), and each cross-®eld has Ն3±9 obliquely ar- compound hook and an oblique section of the upper hook ranged pits (Fig. 7, at left). The xylic rays are well pre- tip of the second pair were exposed. These lateral and served, usually one to two cells wide (Figs. 4, 14) and terminal hook tips curve backwards and are arranged in as tall as 60 cells. Between the cauline xylem segments, roughly the same plane. More details of the attachment there are wedge-shaped gaps (Figs. 2±6, 15 [arrows]) of the compound hook to the main axis (Fig. 3, lower sometimes containing cellular remains that are over three right) are shown in a transverse section which is ϳ5mm cells wide and could be medullary rays. lower from the section in Fig. 2. Here, one large vascular The region of the cambium and inner phloem appears trace (Fig. 3, ``H'') is relatively well preserved in an as a zone of amorphous cellular remains or as an empty oblique section of the compound hook axis. This vascular gap, due to the poor preservation. In several transverse trace is crescent shaped, bilaterally symmetric, and opens sections, there is a narrow, dense cellular zone, surround- towards its adaxial side where the parenchyma cells oc- ing the secondary xylem (Figs. 2±3), composed of 2±4 cur. small cells, which are usually rounded rectangular in As in the stem, the main axis of the compound hook shape, ϳ15 ␮m in diameter, and have lumens commonly also has sparganum cortex. The tracheids in this main 6±8 ␮m in diameter. In tangential section, they are elon- axis are usually 20±45 ␮m in diameter and have helical

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(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 ϭ 10 ␮m, ϫ1000. 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 ϭ 18.5 ␮m, ϫ540. 1570 AMERICAN JOURNAL OF BOTANY [Vol. 86 November 1999] LI AND TAYLORÐVESSEL-BEARING GIGANTOPTERID VASOVINEA FROM CHINA 1571 thickening, but a few tracheids are 15±23 ␮m 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 af®nities, 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 (Ca- rlquist, 1996a, b, c), and pores with the remains of the Fig. 32. Reconstruction of stem of Vasovinea tianii Li et Taylor circular borders that may be slightly raised. Another type with compound hooks and actinodromous Gigantopteris-type leaves. of vessel has scalariform perforation plates, which develop by the loss of the pit membranes (that have a uni- form construction with micropores) between scalariform the foraminate type rather than the scalariform type. bordered pit pairs on the highly inclined, elongate, planar However, on a closer examination, we found that the ves- end walls (Carlquist, 1996a, b, c). This type of vessel sels of V. tianii are different from the foraminate type. commonly occurs in some ferns (e.g., Carlquist and First, the perforation plate is planar (e.g., Figs. 11, 16) Schneider, 1997; Schneider and Carlquist, 1998) and bas- and the number of pores is high (e.g., Figs. 7, 11, 14, 18, al angiosperms (e.g., Bailey, 1944; Carlquist, 1992, 1994, 19). Second, some pores are actually transversely elon- 1996a), but derived angiosperms may have vessels with gate (not circular, e.g., Fig. 19) and lack borders (com- simple perforations that evolved from the scalariform pared pores in Fig. 11 to bordered pits in Fig. 13). Third, type. within some pores the incompletely dissolved pit mem- The vessels of Vasovinea tianii in the secondary xylem branes are planar and lack tori and margo threads (Figs. also appear to develop by the dissolution of the pit mem- 17, 18). Therefore we call these vessels foraminate-like branes between pit pairs on the end walls, and the rough- to distinguish them from those with typical foraminate ly round pores make the vessels super®cially similar to perforation plates. On the other hand, the possible vessel

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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 ϭ 1 cm, ϫ2.4. 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 ϭ 1 cm, ϫ0.9. 23. Longitudinal section of the broken top part of a permineralized hook tip. Notice the hollow center. Slide L9414±1±1; bar ϭ 200 ␮m, ϫ45. 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 ϭ 1 mm, ϫ20. 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 ϭ 200 ␮m, ϫ56. 26. A pair of trichomes, the one on the left has a large apical cell. Slide L9407-B-T2; bar ϭ 200 ␮m, ϫ45. 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 ϭ 1 cm, ϫ1. 28. A glandular trichome with a tapered apical cell. Slide L9407-3-2-2; bar ϭ 200 ␮m, ϫ45. 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 ϭ 1 cm, ϫ1.5. 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 ϭ 2 mm, ϫ6.5. 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 ϭ 200 ␮m, ϫ70. 1572 AMERICAN JOURNAL OF BOTANY [Vol. 86 in the metaxylem appears to be similar to the scalariform nea yunguiensis (H. Li and Taylor, 1998), and Vasovinea type in general structure. tianii. The prickles were described as aculei (H. Li and Another interesting and important structure is the com- Tian, 1990) and spines (H. Li et al., 1994) and have been pound hook. The hook tips are anatomically identical rede®ned as prickles (H. Li and Taylor, 1998) because of with the isolated, permineralized ones (Figs. 23, 24) as- their epidermal and cortical origin, and lack of vascular sociated with Vasovinea stems and Gigantopteris-type tissue. Although the prickles in V. tianii are fewer in leaves. Also they are morphologically well matched with number, smaller, and contain fewer thick-walled paren- the compressed compound hooks (Figs. 21, 22) from the chyma cells, they are similar to prickles of G. guiz- same locality. For example, the compressed compound houensis and A. yunguiensis in structure and origin. Fi- hook shown in Fig. 21 has a 1.2 cm long basal axial part, nally, a sparganum cortex also is found around the vas- a 1.4 cm long middle axial section, and ®ve hook tips cular bundles in Gigantopteris-type leaves (Fig. 25). (the terminal tip is broken), with 2.6, 1.6 and 0.8 mm The leaf traces (ϳ750 ␮m in diameter; Figs. 2 [``T'']. diameters, respectively. As with thorns and tendrils, the Fig. 4 [upper]) in the stem are identical to the vasculature compound hooks could be modi®ed from stems or leaves. (ϳ350 ␮m in diameter; Fig. 31, central part) in a section We suggest that the compound hook of Vasovinea may of a narrow, Gigantopteris-type leaf midrib, in terms of be modi®ed from a leaf, based on the following evidence: the radial rows of tracheids surrounding the triangle- (1) it has a bilaterally symmetrical, crescent-shaped vas- shaped primary xylem. The reduction in the diameter of cular trace (Fig. 3, ``H''), (2) the hook tips are arranged the vasculatures is reasonable, considering they grow out in the same plane, and (3) the branching pattern is similar from the stem cortex through to the midrib. Some thicker, to pinnate leaf venation. secondary veins of a large-sized, Gigantopteris-type leaf (possibly a different species from that of Fig. 31), have Af®nityÐSeveral lines of evidence show that Vasovi- a heart-shaped vasculature (Fig. 25), and the tracheids nea tianii is a member of the gigantopterids. The most (each up to ϳ40 ␮m in diameter) are also arranged in important evidence comes from the presence of a per- radial rows. All these radially arranged tracheids are sep- mineralized compound hook (Fig. 1), which is attached arated by parenchyma cells, so they appear to belong to to the permineralized stem (Fig. 3, at right). This type of secondary xylem. This distinguishes them from those U- compound hook structure is unique to gigantopterids and or V-shaped vasculatures in Gigantonoclea guizhouensis has not been reported from other fossil or extant plants leaf veins, which consist only of primary xylem. There- (see Menninger, 1970). Signi®cantly, the structure of the fore, these similar vasculatures suggest that Vasovinea compound hook is identical with those found from the and Gigantopteris-type leaves belong to the same kind early Late Permian Gigantopteris ¯oras of Shanxi (ϭ plant. Shansi in Halle, 1929) Province, northern China (Halle, The biological relationship of Vasovinea tianii stems, 1929), and Fujian Province, southern China (Yao, 1983). Gigantopteris-type leaves, and the compound hooks also Halle (1929) interpreted the hook-like structures as mod- is supported by their intimate association. More than a i®ed leaves of Gigantopteris nicotianaefolia. In 1995, dozen compression leaf species of three gigantopterid one of us (Hongqi Li) borrowed and reexamined some genera have been reported from the Permian ¯ora of of the Shanxi specimens from the Swedish Museum of western Guizhou (Gu and Zhi, 1974; Tian and Zhang, Natural History. He con®rmed that one of the gigantop- 1980; Zhao et al., 1980). Except for the rare Linophyllum terid leaves had thickened pinnate secondary veins that xuanweiensis, the other species belong to Gigantonoclea distally curved backwards to form hooks, but the basal (with simple net veins) or Gigantopteris (with complex part of each secondary vein still bore bilaterally a small reticulate veins). These three genera all have a midrib amount of lamina. Thus, the Shanxi specimen clearly (primary vein) and pinnate secondary veins. Based on our demonstrates a transitional type from a pinnately veined collections from the Guizhou Flora, we have recently rec- gigantopterid leaf to a compound hook with opposite ognized an actinodromous type of gigantopterid leaf that hook tips. Our analysis of the permineralized compound has either three or ®ve primary veins (H. Li and Taylor, hooks is in agreement. 1997a). Both Gigantopteris and the actinodromous leaves Additional features showing the gigantopterid af®nity have complex reticulate venation, and both are so large include the presence of sparganum cortex, prickles, tri- that it is dif®cult to tell from which type a leaf fragment chomes, and the con®guration of the vascular trace. A with complex netted veins comes (e.g., Figs. 22, 27). similar sparganum cortex is commonly known in many Therefore, we prefer to use the term Gigantopteris-type Paleozoic seed ferns, such as the Carboniferous lyginop- for all gigantopterids with complex reticulate venation. terids, medullosans, and callistophytes. Some species, A gigantopterid leaf similar to Gigantonoclea guiz- such as Heterangium kentuckyensis (Pigg, Taylor, and houensis has been reconstructed together with prickly Stockey, 1987), Microspermopteris aphyllum (Pigg, Aculeovinea yunguiensis stems (H. Li and Taylor, 1998). Stockey, and Taylor, 1986), and Callistophyton boyssetii Gigantopteris-type leaves are frequently associated with (Rothwell, 1975, 1981) even have similar prickle/tri- compressed stems that are similar to compressed stems chome-like structures (called ``cortical wings'' in the ®rst of A. yunguiensis in having tiny ribs (Fig. 27), but with two references). However, among the plants reported fewer black dots than the latter. The tiny ribs and the dots from the Upper Permian ¯ora of western Guizhou, a spar- appear to be the remains of a sparganum cortex and the ganum cortex and pickles/trichomes are only found in broken bases of trichomes or prickles of Vasovinea, re- gigantopterids (see Tian et al., 1996). These structures spectively. Gigantopteris-type leaves also are frequently are characteristic of the leaf midribs of Gigantonoclea associated with the compressed hooks, e.g., the com- guizhouensis (H. Li et al., 1994), the stems of Aculeovi- pound hook in Fig. 21. Another specimen has two hooks November 1999] LI AND TAYLORÐVESSEL-BEARING GIGANTOPTERID VASOVINEA FROM CHINA 1573

(Fig. 22, arrows) and is associated with a leaf that has (see above). There is considerable controversy over complex reticulate venation and compound rounded whether the two types of vessels represent two different teeth, similar to the leaf in Figs. 29±30. In permineralized evolutionary lineages or had a single origin in gneto- materials, Gigantopteris-type leaves are frequently asso- phytes and angiosperms (Bailey, 1944; Young, 1981; Mu- ciated with Vasovinea stems as demonstrated in Figs. 29± hammad and Sattler, 1982; Carlquist, 1992, 1994, 1996a). 30. In one of our specimens (L9407), all of the well- However, the foraminate-like vessels of Vasovinea tianii preserved leaves have complex reticulate venation, and differ from both those of gnetophytes and angiosperms. all of six or more anatomically preserved stems have ves- Although super®cially similar to those of the gneto- sels. phytes, the perforation plate of Vasovinea is planar, has Although associational evidence strongly supports the many more pores (which are borderless and can be trans- inference that Gigantopteris-type leaves, compound versely elongated), and has pit membranes (when they hooks, and Vasovinea tianii stems could belong to the exist) without tori or margo threads. This type of fora- same plant species, whether the reticulate leaves are ac- minate-like perforation plate is not known from angio- tinodromous or pinnately veined is still uncertain. We sperms, although the scalariform bordered pits and the reconstructed the V. tianii stems with the actinodromous possible vessels in the metaxylem of Vasovinea resemble Gigantopteris-type leaves (Fig. 32) at this time, because those of angiosperms. Therefore, although these vessels in sample PLY04 the only leaf that is associated with the are very important in tracing their origin, we cannot draw single V. tianii stem is of the actinodromous type. We a comprehensive conclusion of the systematic relation- also included the tendril-like trichomes, prickles, and ships of the gigantopterids based on vessel features alone. compound hooks, since these structures are attached to Preliminarily results, based on phylogenetic analyses of the stems. We placed the hooks in a subopposite arrange- a broad suite of characters (H. Li and Taylor, 1997b) and ment with the leaves because the location of the trans- molecular fossil data (Taylor et al., 1998), suggest that verse section with the hook trace (Fig. 3) is ϳ5 mm be- gigantopterids are embedded well within the seed plants low the transverse section with the possible leaf traces and may be another member of the anthophyte clade. (Fig. 2). However, this reconstruction may need to be further re®ned in the future in terms of whether the Va- PaleoecologyÐHalle (1929) reported some hook-bear- sovinea stems may actually have actinodromous or pin- ing gigantopterids from central Shanxi and suggested that nately veined leaves, or both. the gigantopterids grew as lianas in a tropical habitat. Yao (1983) reported additional hooks and also considered the Systematic relationshipsÐAlthough Vasovinea tianii gigantopterids as lianas growing in a lowland tropical is placed in the Gigantopteridales, it is still uncertain to forest. Geographically, Guizhou has been suggested to which higher category the order belongs. Gigantopterids have been in a tropical forest biome during the Late were ®rst considered to be ferns (Schenk, 1883) and then Permian (Lin, Fuller, and Zhang, 1985; Tian et al., 1990; seed ferns (White, 1912; Asama, 1959). The latter view Nie, Rowley, and Ziegler, 1990; Isozaki, 1997). Our ma- is supported by X. Li and Yao (1983) who reported an terial strongly supports these paleoecological predictions impression specimen with both seed-bearing taeniopter- and provides some additional ecophysiological interpre- oid and Gigantonoclea fukienensis leaves. However, tations. whether the axes of those leaves were organically con- The morphology, anatomy, and reconstruction of Va- nected or just overlapped together appears unclear. sovinea tianii support the interpretation that it grew as a Although there are no permineralized reproductive or- vine or liana. In extant lianas, hooks, thorns, tendrils, and gans to clarify whether gigantopterids belong to seed spines/prickles function as attachment organs so the slen- ferns or other groups, the anatomy of Aculeovinea yun- der plants can climb. In particular, hooks only have been guiensis suggests that the gigantopterids were seed plants found in vines, where they are considered very ef®cient (H. Li and Taylor, 1998). The combination of characters climbing organs (Menninger, 1970), and de®ne a group in Vasovinea tianii, such as vessels, a eustele, sparganum called the hook climbers (Putz and Holbrook, 1991). The cortex, and secondary xylem, separates it from the pte- tendril-like trichomes and prickles of V. tianii might also ridophytes. These characteristics are typical of Paleozoic have provided an additional climbing mechanism. seed ferns, such as Heterangium, Microspermopteris, and Anatomical features such as a segmented xylem and Callistophyton (Taylor and Taylor, 1993; Pigg, Stockey, the distribution and structure of its vessels also support and Taylor, 1986; Pigg, Taylor, and Stockey, 1987), al- the inference that Vasovinea tianii was a liana. Just like though none of these genera share the full suite of char- many living lianas, V. tianii contained xylem segments acters of Vasovinea. In particular, none of them have re- dispersed among parenchyma cells. The in¯exible xylem ticulate-veined leaves and vessel-bearing stems. Although segments within soft parenchyma tissues function like vessels also are found in some extant ferns and fern allies, ``multistranded cables'' so that the liana stems could have such as some ferns (Jeffrey, 1917; Bliss, 1939; White, withstood considerable deformation while maintaining 1961; Carlquist and Schneider, 1997; Schneider and Carl- the conductive function (see Carlquist, 1991; Putz and quist, 1998), Selaginella (Duerden, 1934), and Equisetum Holbrook, 1991). Vasovinea tianii stems have large ves- (Bierhorst, 1958), these vessels commonly have only sca- sels abruptly occurring at the inner portion of the sec- lariform perforations and none of these plants have both ondary xylem and small vessels in the outer portion (and a eustele and secondary xylem. possibly in the metaxylem), an arrangement resembling In extant seed plants only gnetophytes and angio- that found in certain extant lianas (Carlquist, 1991). The sperms typically have vessels, and their vessels are of the pores of Vasovinea have completely lost their borders and foraminate and scalariform/simple types, respectively are elongate (8 ϫ 10 to ϳ 13 ϫ 15 ␮m; Figs. 7, 11, 18± 1574 AMERICAN JOURNAL OF BOTANY [Vol. 86

19) and larger than bordered pits on lateral walls (Figs. form or reticulate bordered pits in the metaxylem. These 11 [lower right], 20). In extant lianas, vessel end walls morphological features suggest that V. tianii represents a tend to be more thoroughly perforated than those of tree unique seed plant taxon, but its phylogenetic relationships and shrubby genera in the same family. The vines may to seed ferns, gnetophytes, and angiosperms remain to be have simple perforations with reduced borders, rather further analyzed. The presence of compound hooks and than scalariform perforations, or have large vessels with other anatomical features clearly shows that V. tianii be- simple perforations and small vessels with scalariform longs to the gigantopterids, while additional evidence perforations, instead of all scalariform vessels, or may from the associated permineralized and/or compressed have scalariform perforations with fewer bars than in materials indicates that it should be reconstructed togeth- trees (Carlquist, 1991). Presumably, to overcome the er with Gigantopteris-type leaves as lianas that grew in large resistance to water ¯ow in tracheary elements and the Permian tropical rain forest of western Guizhou, Chi- to complement the rapid water loss from the relatively na. large leaves, the plants need an extremely ef®cient water- conducting tissue in their stems (see Ewers, Fisher, and LITERATURE CITED Chiu, 1989). Other vessel parameters can also be correlated to habit. ASAMA, K. 1959. Systematic study of so-called Gigantopteris. Science Reports, Tohoku University, Sendai, Japan, Second Series (Geol- Lianas typically have larger vessel diameters (from an ogy) 31(1): 1±72, pls. 1±2. average of 157 ␮m to 558 ␮m in diameter; Carlquist, ÐÐÐ. 1974. Origin of angiosperms inferred from the evolution of 1975) than closely related woody trees in both Gnetum leaf forms. In R. N. Lakhanpal [ed.], Symposium on origin and and dicots (Ewers, 1985; Ewers and Fisher, 1989; Ewers, phytogeography of angiosperms, 1±4. Birbal Sahni Institute of Pa- Fisher, and Chiu, 1990; Fisher and Ewers, 1995). Bamber leobotany, Lucknow, India. and Welle (1994) reported that many liana species from ÐÐÐ. 1982. Evolution and phylogeny of vascular plants based on the principles of growth retardation, Part 5, Origin of angiosperms the Queensland rain forest have vessels 14±57% larger inferred from the evolution of leaf forms. Bulletin of the National than tree species of the same genera, and the largest ves- Science Museum (Tokyo) 8(2): 43±58. sel was 610 ␮m in diameter. In living lianas, the widest ÐÐÐ. 1988. The origin of the angiosperms. Ocean Press, Beijing (in vessel members tend to be the longest (Ewers and Fisher, Chinese). Translated by Z.-G. Gu and L. Shan from K. Asama, 1989; Bamber and Welle, 1994). Similarly, the vessel 1975, The origin of the angiosperms. Sanseido, Tokyo (in Japa- members of Vasovinea, up to 500 m in diameter and nese). ␮ BAILEY, I. W. 1944. The development of vessels in angiosperms and 4500±5000 ␮m in length, are in the range of the largest its signi®cance in morphological research. American Journal of and longest among all plants, both living and extinct. Botany 31: 421±428. The reconstruction of the thin Vasovinea stems with BAMBER, R. K., AND B. J. H. TER WELLE. 1994. Adaptive trends in the the large Gigantopteris-type leaves also resembles many wood anatomy of lianas. In M. Iqbal [ed.], Growth patterns in vas- extant lianas that usually possess high leaf-area to stem- cular plants. Dioscorides Press, Portland, OR. BIERHORST, D. W. 1958. Vessels in Equisetum. American Journal of diameter ratios (Carlquist, 1975, 1991). Many cordate, Botany 45: 534±537. actinodromous gigantopterid leaves are larger than 400 BLISS, M. C. 1939. The tracheal elements in the ferns. American Jour- cm2, with some observed in the ®eld up to 1600 cm2, but nal of Botany 26: 620±624. these large leaves are associated with slender stems, com- CARLQUIST, S. 1975. Ecological strategies of xylem. University of Cal- monly no more than 1 cm in diameter. ifornia Press, Berkeley, CA. ÐÐÐ. 1991. Anatomy of vine and liana stems: a review and synthe- It is also possible to predict the placement of Vasovi- sis. In F. E. Putz and H. A. Mooney [eds.], The biology of vines. nea within the forest structure. Extant lianas and vines Cambridge University Press, Cambridge. with large, cordate leaves and long petioles usually grow ÐÐÐ. 1992. Pit membrane remnants perforation plates of primitive in sunny areas, while those with small, narrow leaves and dicotyledons and their signi®cance. American Journal of Botany short petioles normally grow in more shady environments 79: 660±672. ÐÐÐ. 1994. Wood and bark anatomy of Gnetum gnemon L. Botan- (Givnish and Vermeij, 1976). Some Gigantopteris-type ical Journal of the Linnaean Society 116: 203±221. leaves have been found with well-differentiated palisade ÐÐÐ. 1996a. Wood anatomy of primitive angiosperms: new per- and spongy cells (Fig. 25, left) and guard cells sunken in spectives and synthesis. In D. W. Taylor and L. J. Hickey [eds.], the stomata (Guo, Tian, and Chang, 1993). The meso- Flowering plant origin, evolution and phylogeny. Chapman and phyll differentiation is related to plant species and to hab- Hall, New York, NY. ÐÐÐ. 1996b. Wood, bark, and stem anatomy of Gnetales: a sum- itat with increased palisade differentiation related to in- mary. International Journal of Plant Science 157(6 Supplement): creased exposure to light (Esau, 1965). This is in contrast S58-S76. to the undifferentiated mesophyll as in Gigantonoclea ÐÐÐ. 1996c. Wood, bark, and pith anatomy of Old World species guizhouensis (H. Li et al., 1994). We suggest that both of Ephedra and summary for the genus. Aliso 13: 255±295. Gigantonoclea and Gigantopteris lived in a similar hab- ÐÐÐ, AND E. L. SCHNEIDER. 1997. SEM studies on vessels in ferns. itat based on the co-occurrence in the sediment, but that 2. Pteridium. American Journal of Botany 84: 581±587. DUERDEN, H. 1934. On the occurrence of vessels in Selaginella. Annals the Gigantopteris-Vasovinea plant grew in the sunny can- of Botany 48: 461±465. opy, while the Gigantonoclea-Aculeovinea plant grew in ESAU, K. 1965. Plant anatomy, 2nd ed. John Wiley & Sons, New York, the shady understory. NY. In summary, Vasovinea tianii is mainly characterized EWERS, F. W. 1985. Xylem structure and water conduction in conifer by its compound hooks, sparganum cortex, eustelic pri- trees, dicot trees, and lianas. IAWA Bulletin new series 6:309±317. ÐÐÐ, AND J. B. FISHER. 1989. Variation in vessel length and diameter mary vascular architecture, foraminate-like vessels in the in stems of six tropical and subtropical lianas. American Journal secondary xylem, and possible vessel elements with sca- of Botany 76:1452±1459. lariform-reticulate structures and tracheids with scalari- ÐÐÐ, ÐÐÐ, AND S.-T. CHIU, 1989. Water transport in the liana November 1999] LI AND TAYLORÐVESSEL-BEARING GIGANTOPTERID VASOVINEA FROM CHINA 1575

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