A Large Anatomically Preserved Calamitean Stem from the Upper Permian of Southwest China and Its Implications for Calamitean Development and Functional Anatomy

Pl. Syst. Evol. 261: 229–244 (2006) DOI 10.1007/s00606-006-0434-9

A large anatomically preserved calamitean stem from the Upper Permian of southwest China and its implications for calamitean development and functional anatomy

S. J. Wang1, J. Hilton2, J. Galtier3, and B. Tian4

1State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing, P. R. China 2School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham, UK 3UMR Botanique et Bioinformatique, CIRAD, TA40/PS2, Montpellier, France 4Beijing Graduate School, China University of Mining and Technology, Beijing, P. R. China

Received December 15, 2005; accepted February 19, 2006 Published online: June 21, 2006 Springer-Verlag 2006

Abstract. A large permineralized calamitean stem, Although represented by the single extant Arthropitys yunnanensis Tian et Gu from the Upper genus Equisetum L., Equisetales have an Permian of southwest China is reinvestigated and extensive fossil record stretching back into interpreted. The stem has a broad pith and well the Late Palaeozoic where they were an developed and large carinal canals. Secondary important component of many coal-forming xylem is thick and characterized by wide paren- wetland plant communities (DiMichele and chymatous interfascicular zones that remain con- Hook 1992, Wang et al. 2003). In these stant in width throughout the wood. Striking features of the stem include the abundant leaf ecosystems Equisetales were both diverse and traces arranged in two whorls in the cortex with abundant, and are best known from the this arrangement previously unrecognized within conceptual whole plants Archaeocalamites calamitean stems, and the presence of growth rings and Calamites (Bateman 1991, Rothwell in secondary xylem that suggest frequent fluctua- 1999). These extinct taxa are important tions in environmental stress presumably due to because they demonstrate a number of mor- variations in water availability. Features of phological and anatomical adaptations that A. yunnanensis infer the stem to be in the epidoge- have subsequently been lost within the group, netical phase of calamitean development, and and demonstrate that in the geological past suggest it to be the basal part of a large trunk. Equisetales include arborescent forms that Comparisons with biomechanical models for ca- produced abundant wood and possessed a lamitean stems suggest this species had a semi-self vascular cambium, as well as heterosporous supporting habit. forms that are radically different from the Key words: sphenopsid, Equisetales, calamite, homosporous living species. These extinct Arthropitys, Upper Permian, anatomy. forms not only show patterns of evolution 230 S. J. Wang et al.: Arthropitys from the Permian of China that can not be determined from extant Arthropitys. We also consider the developmen- taxa alone, but they also emphasise that the tal, evolutionary and environmental impor- present day range within Equisetophytes rep- tance of A. yunnanensis. resents only a small fraction of the groups former diversity (Bateman 1991, Doyle 1998, Rothwell 1999). Materials and methods In the Palaeozoic floras of China Calam- We document a single permineralized stem that was itean plants constitute a significant compo- briefly illustrated and named Arthropitys yunnan- nent in coal-forming plant communities ensis by Tian and Gu (in Li and Cui 1995). The where they are frequently reported in com- stem was collected from mine spoil at Housuo Coal pression/impression assemblages (e.g. Shen Mine, Fuyuan County, eastern Yunnan Province, 1995). By contrast, only a small number of southwestern China. This mine works economically taxa have been recognized from permineral- viable coal seams from the upper part of the ized assemblages (Tian et al. 1996, see Wang Xuanwei Formation, a series of marginal conti- et al. 2003 for recent summary). Anatomi- nental to marginal marine deposits sediments that cally preserved specimens in Chinese coal ball include paralic coal swamps and interbedded assemblages tend to be fragmentary and sediments that include tuffaceous horizons (Shao et al. 1998, Hilton et al. 2004). The specimen has poorly preserved such as those from Shan- fine grained tuffaceous sediment attached to its dong Province, or, include well preserved upper and lower surfaces, and was clearly preserved sub-aerial rooting systems such as those from within the tuff. The tuff has carbonate cement and Gansu and Shanxi Provinces (WSJ, pers. carbonate is the permineralizing agent for cellular obs.). However, well-preserved Calamitean petrifaction. stems are more common in locations in The stem was cut with a rock saw to reveal which fossil plants are preserved in volcani- both longitudinal and transverse sections. Ex- clastic tuffs such as those described by Wang posed surfaces were prepared by the acetate peel et al. (2003) from the Upper Permian Junlian technique using HCL to etch the carbonate Formation in Sichuan Province. matrix (Galtier and Phillips 1999). Peels were Within China Gu De-Rong first studied mounted on glass slides using Eukitt. Photo anatomically preserved Cathaysian calamitean documentation was achieved using a Q-Imaging Micropublisher 5.0 digital camera mounted on a stems, describing several new taxa in an Zeiss Axioskop for high magnifications and a unpublished Master’s dissertation (Gu 1988). Zeiss Stemi SV II for lower magnifications. Of the taxa Gu documented only a single Larger peels were photographed with a Canon species has subsequently been published, with 10D digital SLR camera with 50 mm macro lens. Tian and Gu (in Li and Cui 1995) providing a In all cases peels were illuminated from below preliminary account of the calamitean stem and studied under transmitted light. Specimens Arthropitys yunnanensis Tian et Gu. Tian and are deposited in the palaeobotanical collection at Gu’s (1995) account included a few photo- the China University of Mining and Technology graphic illustrations of this species, but nei- (Beijing). ther detailed description nor systematic Nomenclatural issues. The name Arthropitys treatment were presented. Because type mate- yunnanensis Tian et Gu (in Li and Cui 1995, pgs. rial has not been designated, the name 54–55) was published invalidly because a type was Arthropitys yunnanensis Tian et Gu is invalid not designated (ICBN Article 37.1). Here we correct this oversight by designating and illustrat- (ICBN Article 37.1). This paper therefore ing a lectotype (specimen H35; Figs. 1–21) (ICBN presents a comprehensive description of the Articles 9.2, 9.9). The lectotype is the same plant based on the original materials investi- specimen from which the anatomical preparations gated, conducts a formal systematic treatment originally illustrated by Tian and Gu (in Li and Cui in order to validate the species name, and 1995) were obtained. In addition, we provide a provides comparisons with other species of formal systematic treatment and an extended S. J. Wang et al.: Arthropitys from the Permian of China 231

Still smaller pits existing on their tangential walls. Width of fascicular segment increasing gradually outwards until at periphery of secondary xylem. Wood tracheids nearly square in cross section, 73 lm in average diameter, with scalariform pitting on radial walls. Fascicular rays usually 1–3 cells wide and 1–50 cells high (usually 10–20). Ray cells radially elongate in cross section with tangential diameters ranging from 20–50 (average 31) lm, and radial diameters ranging from 60–270 (average 91) lm. In radial section fascicular Fig. 1. Diagram showing main features of cross (secondary) rays heterogeneous, consisting of section through internode of Arthropitys yunnanensis. brick-like cells and columnar cells with differ- pi pith, sx secondary xylem, c cortex, bt branch trace, small dots show position of individual leaf traces. ent height, ranging from 50–190 (average 94) Same specimen as Fig. 2, scale bar = 50 mm lm. In tangential section ray cells somewhat vertically elongate with variable height and pitted tangential wall. Ray cells with frequent brown or dark brown colored resin-like con- species diagnosis (below) based on new observa- tents. Leaf traces large and singly associated tions of the original specimen. with low and broad multiseriate rays 1– 1.7 mm high and 0.37–0.5 mm wide. Cortex Systematic description consisting of loosely distributed large paren- Class: Sphenopsida chyma cells with or without contents, and Order: Equisetales small dark brown resinous cells. Leaf traces Family: Calamitaceae usually in 2–3 rings and with less secondary Genus: Arthropitys Goeppert 1864 xylem near periphery of cortex. Leaf traces Species: A. yunnanensis (Tian et Gu) ex Wang, pass through cortex in steeply upward course. Hilton, Galtier and Tian 1995. Arthropitys Holotype - Peels and slides made from yunnanensis Tian et Gu, in Li and Cui (eds.), specimen H35 as illustrated by Tian and Gu Atlas of fossil plant anatomy in China: 54–55. (in Li and Cui 1995) and illustrated here in Derivation of specific epiphet – from the Figs. 1–24. collection locality. Type locality - Housuo Coal Mine, Fuyuan Specific diagnosis – Carinal canal large and County, eastern Yunnan Province, China. radially elongate. Carinal canal surrounded by Geological horizon - Upper part of Xuanwei 2–3 cells laterally and up to 5–6 cells wide on Formation. the inner side. Interfascicular rays tapering Age - Wuchiapingian to Changhsingian stages gradually in innermost 1/3 of secondary xylem of the Lopingian, Permian (Zhao et al. 1980, thickness then maintaining same width out- Shao et al. 1998). wards to periphery of secondary xylem. Ray cells radially elongate and rectangular in cross Description section except 3–4 rows at margins with smaller tangential dimension and oblique tan- General features. The single stem specimen gential walls. Ray cells brick-like in radial from which the species is founded is 30 cm section and typically with numerous small pits, long and slightly flattened in cross section, 10–20 lm in diameter, on radial walls. Ray with a diameter of 27 · 22 cm including the cells round in tangential section, with diameter extra-xylary tissue (Figs. 1–2). Its vascular increasing from sides to the middle of the ray. architecture is an equisetostele (sensu Rothwell 232 S. J. Wang et al.: Arthropitys from the Permian of China

Figs. 2–5. Anatomical features of Arthropitys yunnanensis. 2 Same specimen as Fig. 1 showing gross features of internode. p pith, c cortex, scale bar = 50 mm, and arrow indicating position of periderm enlarged in Fig. 16. Peel: H35-tran 1. 3 EnlargementofapartofFig.2showingchanging pattern of interfascicular rays and fascicular segments. Scale bar = 5 mm. 4 Three interfascicular rays and fascicular segments with large radially elongate carinal canals in cross section. Several rows of persistent interfascicular ray cells neighbor fascicular segments while the middle parts of the interfascicular rays are hollow. Scale bar = 3 mm. Slide: WP2L-0011. 5 Enlargement of inner part of a fascicular segment with large and radially elongate carinal canal showing small protoxylem tracheids (arrow). Scale bar = 0.25 mm. Slide: WP2L-0011

1999) comprising a central pith (P, Fig. 2) fascicular and interfascicular rays, a cortex surrounded by protoxylem with carinal canals, with abundant leaf traces and branch traces, metaxylem, abundant secondary xylem with and, externally, a periderm. S. J. Wang et al.: Arthropitys from the Permian of China 233

Pith. The pith is hollow and large with a diameter of about 16 · 4.5 cm. A perimedul- lary zone is absent. Primary xylem and carinal canals. A dis- crete ring of primary xylem strands with carinal canals surrounds the pith. There are approximately 150 xylem strands present (Fig. 2) with an average spacing between strands of 2.0 mm (Figs. 2–3). In cross section, carinal canals have radial diameters of 500—1350 lm and a tangential diameter of 150–270 lm. Each carinal canal is triangular or V-shaped (Figs. 4–5) surrounded by nearly isodiametric elements 30–120 lm in diameter (typically > 60 lm) with light colored, thick cell walls (usually > 5 lm thick). The cavity of the carinal canal is lined by a single row of very small elements that are the remains of protoxylem tracheids (arrow, Fig. 5). Protoxylem tracheids are 10–35 (usually 20–30) lmin diameter and are dark brown in color with annular thickenings (arrow, Fig. 6). Elements surrounding the carinal canal are 2–4 cells thick on the lateral sides of the cavity and 7–9 cells thick on the internal side of the cavity (Fig. 5). In longitudinal section these elements are variable in shape, from ﬂattened, nearly square to longitudinally elongate with horizontal or tapered end walls, and vary from 45– 340 (typically > 80) lm long (Fig. 6). We have been unable to observe any thickening or pitting on the cell walls, precluding their interpretation as metaxylem tracheids. Secondary xylem. A broad zone of secondary xylem is present on the external side of each carinal canal (Fig. 4). Secondary xylem ranges from 2.6–3.0 cm in thickness and is divided into fascicular segments of wood and interfascicular parenchymatous rays (Figs. 3– Figs. 6–8. Anatomical features of Arthropitys yun- 4). Fascicular segments of wood in contact to nanensis. All scale bars = 300 lm. 6 Tangentially the carinal canal are 400–750 (usually 450–550) longitudinal section through a carinal canal showing probable metaxylem (MX) in the middle and lm wide and contain 14–16 rows of elements surrounding tissue (ST) at each side. Slide: WP2– that include tracheids and fascicular rays. 0016. 7 Cross section showing interfascicular ray (IR) These increase in width centrifugally to about and fascicular wedge of wood (FWW) and growth 1.37–2.5 (usually 1.4–1.8) mm comprising ring (GR). Slide: WP2L-0011. 8 Radial section approximately 20–30 rows of cells at a distance through secondary xylem showing tracheids and of 10 mm from the margin of the pith, and heterogeneous fascicular ray. Slide: WP2-0102 234 S. J. Wang et al.: Arthropitys from the Permian of China

2–3.25 (usually 2.3–2.6) mm comprising of wide. Ray cells are somewhat vertically elon- approximately 30–40 rows of cells at the gated and of different heights (Fig. 13). Ray margin of the wood (Fig. 4). Tracheids are cells usually have light colored cell walls that nearly square with round angles in cross are slightly thinner than those of the tracheids section (Fig. 5). The innermost wood tracheids but some have an inner dark colored layer are small with diameters between 15–20 lm (Fig. 8) and these cells are usually distributed and their diameter enlarges outwards where it in the zones of tracheids with three layered can reach 73 lm in average. The outer layer of walls. Nearly round or slightly elongate pits the tracheid wall is thin and dark brown occur on tangential walls of ray cells (Fig. 14). colored, and is often poorly preserved or Interfascicular rays start from the pith at a absent. Internal to this layer is a thicker and width of ca. 2 mm (Fig. 4), taper gently lighter-colored zone with a thickness generally centrifugally in the inner 1/3 of wood thick- of >5 lm. In some tracheids an inner layer is ness, and then maintain a similar width or present that is in dark brown color and often increase in width slightly to the outer margin thicker than the middle or light-colored layer. of the wood (Fig. 3). Rays mainly consist of The inner layer is of unequal thickness and is parenchyma cells. Generally 1–3 rows of ray thickest at the four corners and usually thicker cells on both sides of the interfascicular rays or at the tangential wall than at the radial wall. neighboring the fascicular segments of wood Tracheids with tri-layered walls usually have a are of different shape and size and also have a more or less smaller radial size and larger different cell walls morphology from those cells tangential size than those with bi-layered walls, occurring elsewhere in the rays. These periph- and tend to be distributed in tangential zones eral cells usually have smaller tangential diam- that are usually 4–10 tracheids thick in their eter (25–100 lm) and more or less oblique ends radial direction (GR in Fig. 7). There are (Fig. 7). Their walls are usually thick and light about ten such zones in the wood (Fig. 3) colored and of consistent thickness. In con- interpreted to be growth banding. Scalariform trast, the other cells have larger tangential pitting occurs on radial wall of the tracheids diameters (65–150 lm) and have straight ends and there are about 54–66 pits every 500 lm so are usually rectangular in shape. These cells (Figs. 8, 10). Each elongate scalariform pit is have thinner and dark colored cell walls, and approximately 30–35 · 3–4 lm in diameter. do not appear to be very resilient as evidenced Occasionally there are also scalariform pits on by the middle parts of many rays being hollow the tangential tracheid walls. or containing only a few remaining cells. This The fascicular ray cells are parenchyma- is especially common in the inner 1/3 of the tous and mainly empty but some possess dark secondary xylem. brown colored resin-like contents. Fascicular In radial section interfascicular ray cells are rays are narrow in cross section (Fig. 7) with mostly brick-like with straight tangential walls, smaller tangential diameters ranging from 20– but some are horizontally elongated and have 50 (average 31) lm, and larger radial diameters tapering ends. However, in the inner part of ranging from 60–270 (average 91) lm. In the secondary xylem some cells in the centre of radial section fascicular rays are heteroge- interfascicular rays are slightly tangentially or neous, consisting of brick-like cells and colum- horizontally elongated. The interfascicular nar cells with different height, ranging from rays extend axially over the entire length of 50–190 (average 94) lm (Fig. 8). In each cross- the internode, and their position alternates field there are numerous (sometimes > 10) from internode to internode (Figs. 11, 12). nearly round, oval and obliquely located or Internodal regions usually have a length of horizontally elongate pits (Fig. 9). In tangen- 20–25 mm (Fig. 11). tial section fascicular rays are 1–50 (usually Phloem. In most of places the tissue bor- 10–20) cells high and 1–3 (occasionally 4) cells dering the external margin of the secondary S. J. Wang et al.: Arthropitys from the Permian of China 235

Figs. 9–15. Xylem and ray structures of Arthropitys yunnanensis. 9 Enlargement of fascicular ray from Fig. 8 showing pits in cross-field and different shaped ray cells. Scale bar = 250 lm. 10 Radial section of secondary xylem with elongate scalariform pits on tracheid walls. Scale bar = 250 lm. Slide: WP2-0102. 11 Tangential section through secondary xylem showing nodes and internodes. Scale bar = 20 mm. Peel: H35-tan2. 12 Higher magnification of Fig. 11 showing multiseriate fascicular ray with large leaf trace within it (arrow). Scale bar = 1mm.13 Tangential section through secondary xylem showing fascicular rays. Scale bar = 250 lm. Slide: WP2– 0103. 14 Enlargement of Fig. 13 showing ray cells with pits on tangential walls (arrow). Scale bar = 100 lm. 15 Cross section through stem showing area between outmost secondary xylem (SX) and the cortex (C), arrows indicate small black-colored secretory cells arranged in tangential rows. Slide: WP2-0007; Scale bar = 300 lm 236 S. J. Wang et al.: Arthropitys from the Permian of China xylem can not be distinguished from the middle part. Within the leaf traces tracheids cortex, though in some places small dark- range from 14–60 (mostly 30–40) lmin colored secretory cells are richer in number diameter, and intermediate with ray cells that than elsewhere. These secretory cells are more range from 30–70 (mostly 30–50) lmin or less in tangential rows (Fig. 15). diameter. Cortex. The cortex is up to 30 mm thick The cortex has many leaf traces preserved and consists of three kinds of cells that are that are arranged in 2 rings or whorls although loosely arranged; apparently empty paren- in some parts of the stem 3 rings of leaf traces chyma cells, parenchyma cells containing light are seen (Figs. 1, 16). Leaf traces positioned yellow colored cell contents, and small secre- very close to the secondary xylem are usually tory cells containing dark brown colored nearly round in cross section with concentri- contents. In cross section these three kinds of cally developed secondary xylem. Outward the cells have no regular pattern to their distribu- leaf traces become smaller in size and possess tion and occur either individually or in groups less secondary xylem, and the secondary xylem (Figs. 16, 19). The empty and filled paren- occurs in a fan to wedge-shaped arrangement chyma cells are usually greater than 100 lmin (Figs. 19, 20). Tracheids of the secondary maximum dimension, varying in shape from xylem possessing scalariform thickenings. The nearly isodiametric to square, rectangular and leaf trace is mesarch. When the leaf traces are occasionally triangular (Fig. 19). The small far enough from the secondary xylem they secretory cells range from 40–60 lm in max- loose their secondary xylem and only primary imum dimension and are typically square or xylem is present (Figs. 16, 18). rectangular (Fig. 19). In longitudinal section The pattern of leaf trace departure has the small dark-colored secretory cells are been determined from serial cross sections that arranged in vertical files (Figs. 22, 23). In show the leaf traces to move very slowly some sections secretory cells are preferentially outward. From the orientation of the serial distributed in proximity to the secondary peels it is deduced that individual leaf traces xylem (Fig. 15). pass outwards through the cortex in a very Periderm. A periderm-like tissue is some- steep to vertical course. Importantly this times preserved at the periphery of the stem. course is orientated upwards and outwards It consists of sequential layers that may have and is characteristic of leaf traces rather than been formed from successive phellogens. The adventitious roots that pass outwards and most prominent layers consist of apparently downwards from the stem. coalified and radially arranged cells with Branch traces. Only a few branch traces dark contents: they may represent phellem have been observed. In tangential section (PM, Fig. 24). They alternate with layers through the secondary xylem branch traces of thin walled cells that may represent are circular and small with a diameter of phelloderm (PR, Fig. 24). This periderm-like 5 mm. Within branch traces vascular bundles tissue is only observed in a small area of the are poorly developed and are generally hard stem. to distinguish. Branch traces have a large pith Leaf traces. Leaf traces extend in a hori- consisting of tissue similar to the cortex zontal course in the secondary xylem. They are except that the cells are smaller. Branch large and singly associated with low and broad traces pass through the secondary xylem in multiseriate fascicular (secondary) rays 1– a horizontal course. In the cortex branch 1.7 mm high and 0.37–0.5 mm wide in tan- traces are elliptical in cross section and gential section (Fig. 12). Sometimes leaf traces tangentially elongate. Individual branch traces are also associated with the interfascicular rays consist of numerous vascular bundles that are and located in their ends rather than their distributed at equal distances from each other S. J. Wang et al.: Arthropitys from the Permian of China 237

Figs. 16–23. Cortex, leaf and branch traces of Arthropitys yunnanensis. 16 Cross section through cortex showing loosely distributed cells and two rings of leaf traces (arrows); the upper ring is outside the lower one. Scale bar = 3 mm. Slide: WP2-0007. 17 Enlargement of Fig. 21 showing several smaller bundles of the branch trace with weakly developed secondary xylem. Scale bar = 200 lm. 18 Enlargement of Fig. 16 showing a small leaf trace from the outer ring that lacks extensive secondary xylem development. Scale bar = 200 lm. 19 Enlargement of Fig. 16 showing several larger leaf traces of the inner ring with well developed secondary xylem. Scale bar = 200 lm. 20 Enlargement of Fig. 19 showing a large leaf trace of the inner ring with extensive secondary xylem. Scale bar = 200 lm. 21 Cross section through cortex showing half of a tangentially elongated branch trace consisting of very small bundles (arrows). Scale bar = 1 mm. 22 Longitudinal section through cortex showing large, empty and brown-filled cells and small dark-colored secretory cells arranged in vertical files (arrows). Scale bar = 1 mm. 23 Enlargement of Fig. 22 showing vertical files of small dark-colored secretory cells (arrows). Scale bar = 200 lm

(Figs. 17, 21). These bundles are generally Discussion smaller than those observed in leaf traces, and Comparisons. Gross morphology and anat- have little or no secondary xylem present omy of the stem described here are consistent (Fig. 17). In cross section through the stem with that of the genus Arthropitys Goeppert four branch traces have been observed at the (1864). Within Arthropitys characters of the same level (Fig. 1). 238 S. J. Wang et al.: Arthropitys from the Permian of China

foveata, interfascicular rays are narrow, 4–6 cells wide, and maintain their width through the secondary xylem (Andrews 1952, Anderson 1954). In A. deltoides, the interfascicular rays broaden conspicuously toward the periphery of the secondary xylem because of the increase of the tangential dimension of the ray cells (Cichan and Taylor 1983). However A. deltoides is a much smaller stem than our specimen. The specimen we describe here has interfascicular rays that taper only a small amount through the inner 1/3 of the secondary xylem at which point they then maintain their width Fig. 24. Higher magnification of the area indicated outward to the periphery of the secondary by arrow in Fig. 2 showing periderm; PM-phellem, xylem. Renault (1893, Pl. 45, figs. 1, 3) PR-phelloderm. Scale bar = 500 lm illustrates the pattern of change in width of the interfascicular ray in A. bistriata, and this interfascicular rays are important for specific is similar to that of the present specimen except delimitation (Williamson and Scott 1894, that the width of the former is much smaller, Knoell 1935, Anderson 1954, Andrews 1952, only 6–7 cells wide (Renault 1893, 1896; Cichan and Taylor 1983, Wang et al. 2003). Andrews 1952; Boureau 1964) and the latter, Interfascicular rays range from large and more than 15 cells wide. In tangential section broad consisting of more than 20–30 cells such the cells of interfascicular rays of the present as A. approximata and A. major, to smaller specimen are round, however those of other rays only several cells wide such as A. versi- four species are all more or less vertically foveata and A. bistriata, and can be absent as elongate. in A. hirmeri. A further variation seen in the The secondary xylem also plays an impor- interfascicular rays of Arthropitys are their size tant role in specific delimitation within Ar- as they pass through the secondary xylem. For thropitys. Important characters include pitting example, in some species such as A. versifove- patterns on the radial tracheid walls, fascicular ata and A. kansana the interfascicular rays rays and their change from the inner to outer remain of constant in width through the parts of the secondary xylem, the change of the secondary xylem. Interfascicular rays in other width of fascicular segments in the secondary species can vary greatly in width through the xylem (Anderson 1954), and even the size of secondary xylem, either narrowing rapidly tracheids (Cichan and Taylor 1983). outwards as in A. communis or broadening In pitting patterns, the present specimen is gradually as in A. deltoides. The specimen comparable to A. deltoides in possessing elon- described here has interfascicular rays that are gate scalariform pittings. In A. kansana, circu- persistent in width through the secondary lar to slightly elongate bordered pits exist, xylem, and are wide and usually more than while in A. bistriata and A. versifoveata the 15 cells across. This is different from many tracheids exhibit a random mixture of scalar- other species and only four species of Arthrop- iform and reticulate bordered pits. The tan- itys possess persistent interfascicular rays: gential walls of the cells of fascicular rays in A. kansana, A. bistriata, A. versifoveata and the present specimen sometimes are pitted, and A. deltoides. However they are different from this has not previously been mentioned for the our specimen in the width of the interfascicular species A. deltoides, A. kansana, A. versifove- rays and their pattern of change through the ata, and A. bistriata. In radial section, secondary xylem. In A. kansana and A. versi- A. bistriata exhibits homogeneous fascicular S. J. Wang et al.: Arthropitys from the Permian of China 239 rays, but the other three species (A. deltoides, walls to support a possible interpretation of A. kansana, A. versifoveata) and the present these cells as centripetal metaxylem tracheids. specimen possess heterogeneous ones. Marguerier (1970) and Langiaux and Margu- The change of the width of the fascicular erier (1980) designated as ‘‘gaine me´dullaire’’ segments from the inner to outer parts of the a comparable zone of thick-walled cells secondary xylem is different in the present surrounding the carinal canal in Arthropitys specimen from the other four species that have bistriata and A. communis. Andrews (1952) persistent interfascicular rays. In A. deltoides, was also unable to observe specialized thick- the fascicular segment is wedge-shaped with its ening of the walls of similar cells in other width gradually increasing outward (Cichan specimens of Arthropitys. and Taylor 1983). In A. kansana and A. versi- In the stem of Arthropitys yunnanensis foveata, the fascicular segments maintain their described here the cell walls of the interfasci- width through the secondary xylem and their cular rays and fascicular rays are pitted in inner edges are blunt (Andrews 1952, Ander- different directions. This feature has not been son 1954). The fascicular segments of the mentioned in other species. The systematic, present specimen and A. bistriata broadens phylogenetic and environmental significance of outward very slowly and possess a tapered this variation is at present unknown. inner edge. The characters of interfascicular Similar to the secondary tissues of the rays and fascicular segments in the present present specimen, secondary xylem of A. specimen and other four similar species noted deltoides also consists of large tracheids, with above are summarized in Table 1. The distinc- both taxa having average tracheid diameters in tion of the specimen described here agrees with excess of 70 lm. However, other species of Tian and Gu’s (in Li and Cui 1995) taxonomic Arthropitys possess smaller secondary trac- conclusion leading to the erection of Arthro- heids, for example, in A. communis the sec- pitys yunnanensis. ondary tracheids and average in A. communis Characters of systematic significance in 35 · 30 lm and 52 · 50 lminA. junlianensis. Arthropitys. In the specimen we describe, Some authors consider size of the tracheids to large and radially elongate carinal canals are be of little taxonomic significance (e.g. Ander- developed that range from 500–1350 lmin son 1954), whereas other authors consider this radial dimension and from 150–270 lmin to be more or less stable within a single species tangential dimension. In other species carinal and suggest that it does not vary through canals are smaller and are usually less than ontogeny or as phenotypic plasticity (e.g. 200 lm in diameter. Some authors have Cichan and Taylor 1983). Because we only questioned the validity of carinal canal size have a single specimen, we are unable to as criterion for species recognition within consider the significance of large secondary Arthropitys. Anderson (1954) considered its tracheid diameters in A. yunnanensis at the use negligible as it appears to vary with present time. changing pith diameter. Andrews (1952) con- Growth rings and environmental varia- sidered this useful only as a supplementary tion. Growth rings are rarely developed in character if other distinguishing features are the secondary xylem of pteridophytes such as present. From the single specimen of Arthro- arborescent lycopsids and calamites. Although pitys yunnanensis described here it is not Seward (1898) considered that growth rings possible to determine if this character varies were absent in the secondary xylem of cala- within the species. The distinctive band of mites, more recent accounts document calam- thick-walled cells surrounding the carinal itean stems with weakly developed growth canals, laterally and internally, constitutes a rings from the Late Paleozoic floras of particularly distinctive structure. We did not Euramerica. Andrews and Agashe (1965) find evidence of thickening/pitting of the cell reported a large calamitean stem of Arthropitys 4 .J age al.: et Wang J. S. 240

Table 1. Comparison of main features of species of Arthropitys with similar interfascicular ray structure to A. yunnanensis Species Interfascicular ray Fascicular ray Fascicular segment Change pattern Cell shape in t.s. Cell shape in t.s. Cell shape in r.s. Change pattern Radial tracheid wall pitting A. deltoides Broadening Inner wood strongly Inner wood strongly Heterogeneous Broadening Elongate conspicuously vertically elongate; vertically elongate; gradually scalariform outward outer wood slightly outer wood slightly outward vertically elongate vertically elongate A. bistriata Similar to that of Nearly isodiametrically Strongly vertically Homogeneous Similar to that of Random mixture A. yunnanensis polygonal elongate A. yunnanensis of scalariform and reticulate bordered pits A. kansana Maintaining same Slightly vertically Similar to Heterogeneous Maintaining the Circular to slightly width through s.x. elongate A. yunnanensis width through s.x. elongate bordered pits

A. versifoveata Similar to that of Similar to that of Similar to that of ? Similar to that of Similar to that of Arthropitys A. kansana A. kansana A. yunnanensis A. kansana A. bistriata A. yunnanensis Tapering outward Round Somewhat vertically Heterogeneous Broadening Elongate scalariform gradually through elongate with gradually inner 1/3 of s.x. variable height outwards rmtePrino China of Permian the from then maintaining width outwards. S. J. Wang et al.: Arthropitys from the Permian of China 241 communis var. septata Andrews that has sec- with extra-xylary tissue have been studied ondary xylem of up to 12 cm in thickness that (Williamson 1871, 1878; Williamson and Scott had more than 10 faint growth rings. The 1894; Renault 1893; Agashe 1964; Eggert 1962; distance between neighboring growth rings Cichan and Taylor 1983; Wang et al. 2003), varies greatly, but the size difference of trac- leaf traces and/or branch traces have not been heids is only slight leading to conclusions that found in the cortex. In A. yunnanensis the climatic variation during the life of the plant presence of whorls of leaf traces in the cortex is was minimal (Andrews and Agashe 1965). unique. This shows that leaf traces had a very Scott et al. (1986) recorded an Archaeocala- oblique to vertical course through the cortex mites stem with three well developed growth instead of being nearly horizontally orientated rings in which the distance between neighbor- as generally assumed for this genus. This may ing rings was also considerable. In this exam- be typical of this species and of the develop- ple, size differences of the tracheids are evident, mental pattern of this particular species. leading Scott et al. (1986) to conclude that Periderm. There is evidence of a periderm- these growth rings recorded ecological changes like tissue composed of concentric or sequen- in environmental stress such as periods of tial layers that may be formed by successive drought rather than regular seasonal or cli- phellogens. This periderm is comparable to the matic variation. In the present specimen, rhytidome made of ‘‘six concentric lamellae’’ growth rings are conspicuous and continuous described by Cichan and Taylor (1983) in through the entire circumference of the sec- A. deltoides. However in A. yunannensis the ondary xylem, with nearly equal distances periderm is a narrow zone preserved at the occurring between neighboring rings. Further- periphery of a massive cortex representing the more, the size differences between tracheids in primary body of the plant. The situation is different rings is not prominent. It is difficult to completely different in A. deltoides that is a make determinations about the cause of this very small stem with no evidence of primary variation without additional specimens of data cortical tissues. on environmental conditions. However, we Ontogeny and development. Compared note that previous accounts of permineralized with data provided by Eggert (1962, Table 1) gymnosperm wood from the same region and on ontogenetic variation in Arthropitys, geological horizon lack growth rings including A. yunnanensis is a large plant that has Guizhouoxylon dahebianense Tian et Li (1992) characters consistent with Eggert’s epidoge- and Walchiopremnon gaoi Tian et al. (1994). In netical phase of development of an aerial this regard we agree with the conclusions of plant. In particular, A. yunnanensis has a Scott et al. (1986) and consider it more likely broad stem diameter (>20 cm) with an that the growth rings in Arthropitys yunnanen- extremely broad zone of primary xylem sis reflected repeated changes in environmental (>100 mm diameter) – the largest stem stud- stress and probably relate to changes in water ied by Eggert had a primary xylem diameter of availability within the growth environment 67 mm. The number of primary vascular rather than indicating seasonality. Palaeocli- strands in A. yunnanensis (approximately 150) matic models for the Upper Permian of is comparable with the values given by Eggert southern China also suggest the absence of who observed a maximum of 172 in other seasonality (e.g. Quan 1992, Rees et al. 1999). species. These size features of A. yunnanensis Leaf and branch traces. Position and struc- are near the maximum for the epidogenetical ture of leaf and branch traces in Arthropitys phase (Eggert 1962), and suggest this speci- yunnanensis are novel. Leaf and branch traces mens is a basal part of the stem. This is have been previously reported passing through confirmed by the relatively short length of the secondary xylem of calamitean stems, and internodes in A. yunnanensis, typically 20– although a number of stems of Arthropitys 25 mm. 242 S. J. Wang et al.: Arthropitys from the Permian of China

Ontogenetic age of the plant. The best main contributor to mechanical support in indicator for the age of the plant is the these plants was the peripheral wood cylinder thickness of the secondary xylem (c. 30 mm) in which lignified tissues, such as secondary that compares to the maximum values given by xylem, provided efficient mechanical support Eggert (1962). However, this does not mean not provided by non-lignified tissues (Spatz that the plant was old, as much larger stems are et al. 1998). The vascular cylinder of A. known; Andrews and Agashe (1965) described yunannensis is noteworthy as it possesses wide specimens with wood 120 mm thick, i.e. four interfascicular rays composed of non-lignified times thicker than A. yunnanensis, and these tissue that was unlikely by itself to provide were certainly much older stems. Furthermore effective support. Interfascicular tissues com- Rossler and Noll (pers. com. 2005) are describ- prise c. 50% of the vascular cylinder with the ing a specimen of Arthropitys from the Permian other c. 50% being the fascicular zone of wood of Chemnitz that is c. 60 cm diameter compris- comprising lignified tissue. This c. 50/50 ratio ing c. 30 cm of wood and a pith/primary xylem of fascicular/interfascicular tissue is compara- less than 2 cm diameter with 74 primary xylem ble to that observed in A. deltoides, interpreted strands. Secondly, the occurrence of a broad by Cichan and Taylor (1983) as a feature of a cortex (= primary body) suggests that the lianescent or semi-self supporting habit. Ci- plant was relatively young as the cortex has not chan and Taylor (1983) also emphasized the been sloughed off by periderm development. large diameter of wood tracheids as indicative The occurrence of a periderm like tissue that is of liana wood, a feature also found in A. very narrow and restricted to a small portion of yunannensis. Despite the major difference in the periphery is not an argument against this, size between A. deltoides and A. yunnanensis, because it may be just the beginning of they may both represent semi-self supporting periderm development in this plant. plants similar to lianas. The description of this As noted above, the occurrence of com- new species from China increases significantly plete primary cortical tissues is exceptional in our knowledge of the habit diversity in calam- such a large stem and, as Eggert (1962) noted, itean plants. such tissues generally are missing although they remain the only source from which to We are grateful to Shao Longyi for discussions determine the number of leaves on a node of on the age of the Xuanwei Formation, Ming-Mei the stem. As indicated by Eggert (1962) this Liang for help and support on WSJ’s research visit number is not strictly related to the number to the UK, and Bill DiMichele and an anonymous reviewer for comments on the manuscript. This of cauline primary vascular strands, as in work was supported by the National Natural Equisetum; indeed, in those small stems of Science Foundation of China (Award 30170064 to Calamites where the cortex is preserved, there WSJ), the Special Fund from the Director of is generally one leaf trace per strand, but in Institute of Botany, CAS (to WSJ), the Chinese large stems there is one leaf trace per two Academy of Sciences (XSCX2-SW-108 to WSJ) strands. and an Anne Sleep Award of the Linnean Society Habit of the plant. Previous reconstruc- of London (to JH). tions of calamitean plants (e.g. Boureau 1964) suggested a significant diversity of habits. This was supported by recent evidence (Barthel References and Rossler 1996) that the large stemmed Agashe S. N. (1964) The extra-xylary tissues in Calamites gigas was a succulent calamite. certain calamites from the American Carboni- Furthermore, biomechanical analyses of ferous. Phytomophology 14: 598–611. extinct calamites (Mosbrugger 1990, Spatz Anderson B. R. (1954) A study of American petrified et al. 1998) suggest the presence of self-sup- Calamites. Ann. Missouri Bot. Gard. 41: 395– porting and semi-self-supporting habits. The 418. S. J. Wang et al.: Arthropitys from the Permian of China 243

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