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. Hilton

2, J. Galtier

3, and B. Tian

4

1State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy ofSciences, Xiangshan, Beijing, P. R. China2School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston,Birmingham, UK3UMR Botanique et Bioinformatique, CIRAD, TA40/PS2, Montpellier, France4Beijing Graduate School, China University of Mining and Technology, Beijing, P. R. China

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

Abstract. A large permineralized calamitean stem,Arthropitys yunnanensis Tian et Gu from the UpperPermian of southwest China is reinvestigated andinterpreted. The stem has a broad pith and welldeveloped and large carinal canals. Secondaryxylem is thick and characterized by wide paren-chymatous interfascicular zones that remain con-stant in width throughout the wood. Strikingfeatures of the stem include the abundant leaftraces arranged in two whorls in the cortex withthis arrangement previously unrecognized withincalamitean stems, and the presence of growth ringsin secondary xylem that suggest frequent fluctua-tions in environmental stress presumably due tovariations in water availability. Features ofA. yunnanensis infer the stem to be in the epidoge-netical phase of calamitean development, andsuggest it to be the basal part of a large trunk.Comparisons with biomechanical models for ca-lamitean stems suggest this species had a semi-selfsupporting habit.

Key words: sphenopsid, Equisetales, calamite,Arthropitys, Upper Permian, anatomy.

Although represented by the single extantgenus Equisetum L., Equisetales have anextensive fossil record stretching back intothe Late Palaeozoic where they were animportant component of many coal-formingwetland plant communities (DiMichele andHook 1992, Wang et al. 2003). In theseecosystems Equisetales were both diverse andabundant, and are best known from theconceptual whole plants Archaeocalamitesand Calamites (Bateman 1991, Rothwell1999). These extinct taxa are importantbecause they demonstrate a number of mor-phological and anatomical adaptations thathave subsequently been lost within the group,and demonstrate that in the geological pastEquisetales include arborescent forms thatproduced abundant wood and possessed avascular cambium, as well as heterosporousforms that are radically different from thehomosporous living species. These extinctforms not only show patterns of evolution

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

that can not be determined from extanttaxa alone, but they also emphasise that thepresent day range within Equisetophytes rep-resents only a small fraction of the groupsformer diversity (Bateman 1991, Doyle 1998,Rothwell 1999).

In the Palaeozoic floras of China Calam-itean plants constitute a significant compo-nent in coal-forming plant communitieswhere they are frequently reported in com-pression/impression assemblages (e.g. Shen1995). By contrast, only a small number oftaxa have been recognized from permineral-ized assemblages (Tian et al. 1996, see Wanget al. 2003 for recent summary). Anatomi-cally preserved specimens in Chinese coal ballassemblages tend to be fragmentary andpoorly preserved such as those from Shan-dong Province, or, include well preservedsub-aerial rooting systems such as those fromGansu and Shanxi Provinces (WSJ, pers.obs.). However, well-preserved Calamiteanstems are more common in locations inwhich fossil plants are preserved in volcani-clastic tuffs such as those described by Wanget al. (2003) from the Upper Permian JunlianFormation in Sichuan Province.

Within China Gu De-Rong first studiedanatomically preserved Cathaysian calamiteanstems, describing several new taxa in anunpublished Master’s dissertation (Gu 1988).Of the taxa Gu documented only a singlespecies has subsequently been published, withTian and Gu (in Li and Cui 1995) providing apreliminary account of the calamitean stemArthropitys yunnanensis Tian et Gu. Tian andGu’s (1995) account included a few photo-graphic illustrations of this species, but nei-ther detailed description nor systematictreatment were presented. Because type mate-rial has not been designated, the nameArthropitys yunnanensis Tian et Gu is invalid(ICBN Article 37.1). This paper thereforepresents a comprehensive description of theplant based on the original materials investi-gated, conducts a formal systematic treatmentin order to validate the species name, andprovides comparisons with other species of

Arthropitys. We also consider the developmen-tal, evolutionary and environmental impor-tance of A. yunnanensis.

Materials and methods

We document a single permineralized stem that wasbriefly illustrated and named Arthropitys yunnan-ensis by Tian and Gu (in Li and Cui 1995). Thestem was collected from mine spoil at Housuo CoalMine, Fuyuan County, eastern Yunnan Province,southwestern China. This mine works economicallyviable coal seams from the upper part of theXuanwei Formation, a series of marginal conti-nental to marginal marine deposits sediments thatinclude paralic coal swamps and interbeddedsediments that include tuffaceous horizons (Shaoet al. 1998, Hilton et al. 2004). The specimen hasfine grained tuffaceous sediment attached to itsupper and lower surfaces, and was clearly preservedwithin the tuff. The tuff has carbonate cement andcarbonate is the permineralizing agent for cellularpetrifaction.

The stem was cut with a rock saw to revealboth longitudinal and transverse sections. Ex-posed surfaces were prepared by the acetate peeltechnique using HCL to etch the carbonatematrix (Galtier and Phillips 1999). Peels weremounted on glass slides using Eukitt. Photodocumentation was achieved using a Q-ImagingMicropublisher 5.0 digital camera mounted on aZeiss Axioskop for high magnifications and aZeiss Stemi SV II for lower magnifications.Larger peels were photographed with a Canon10D digital SLR camera with 50 mm macro lens.In all cases peels were illuminated from belowand studied under transmitted light. Specimensare deposited in the palaeobotanical collection atthe China University of Mining and Technology(Beijing).

Nomenclatural issues. The name Arthropitysyunnanensis Tian et Gu (in Li and Cui 1995, pgs.54–55) was published invalidly because a type wasnot designated (ICBN Article 37.1). Here wecorrect this oversight by designating and illustrat-ing a lectotype (specimen H35; Figs. 1–21) (ICBNArticles 9.2, 9.9). The lectotype is the samespecimen from which the anatomical preparationsoriginally illustrated by Tian and Gu (in Li and Cui1995) were obtained. In addition, we provide aformal systematic treatment and an extended

230 S. J. Wang et al.: Arthropitys from the Permian of China

species diagnosis (below) based on new observa-tions of the original specimen.

Systematic description

Class: SphenopsidaOrder: EquisetalesFamily: CalamitaceaeGenus: Arthropitys Goeppert 1864Species: A. yunnanensis (Tian et Gu) ex Wang,Hilton, Galtier and Tian 1995. Arthropitysyunnanensis Tian et Gu, in Li and Cui (eds.),Atlas of fossil plant anatomy in China: 54–55.Derivation of specific epiphet – from thecollection locality.Specific diagnosis – Carinal canal large andradially elongate. Carinal canal surrounded by2–3 cells laterally and up to 5–6 cells wide onthe inner side. Interfascicular rays taperinggradually in innermost 1/3 of secondary xylemthickness then maintaining same width out-wards to periphery of secondary xylem. Raycells radially elongate and rectangular in crosssection except 3–4 rows at margins withsmaller tangential dimension and oblique tan-gential walls. Ray cells brick-like in radialsection and typically with numerous small pits,10–20 lm in diameter, on radial walls. Raycells round in tangential section, with diameterincreasing from sides to the middle of the ray.

Still smaller pits existing on their tangentialwalls. Width of fascicular segment increasinggradually outwards until at periphery ofsecondary xylem. Wood tracheids nearlysquare in cross section, 73 lm in averagediameter, with scalariform pitting on radialwalls. Fascicular rays usually 1–3 cells wideand 1–50 cells high (usually 10–20). Ray cellsradially elongate in cross section with tangen-tial diameters ranging from 20–50 (average 31)lm, and radial diameters ranging from 60–270(average 91) lm. In radial section fascicular(secondary) rays heterogeneous, consisting ofbrick-like cells and columnar cells with differ-ent height, ranging from 50–190 (average 94)lm. In tangential section ray cells somewhatvertically elongate with variable height andpitted tangential wall. Ray cells with frequentbrown or dark brown colored resin-like con-tents. Leaf traces large and singly associatedwith low and broad multiseriate rays 1–1.7 mm high and 0.37–0.5 mm wide. Cortexconsisting of loosely distributed large paren-chyma cells with or without contents, andsmall dark brown resinous cells. Leaf tracesusually in 2–3 rings and with less secondaryxylem near periphery of cortex. Leaf tracespass through cortex in steeply upward course.Holotype - Peels and slides made fromspecimen H35 as illustrated by Tian and Gu(in Li and Cui 1995) and illustrated here inFigs. 1–24.Type locality - Housuo Coal Mine, FuyuanCounty, eastern Yunnan Province, China.Geological horizon - Upper part of XuanweiFormation.Age - Wuchiapingian to Changhsingian stagesof the Lopingian, Permian (Zhao et al. 1980,Shao et al. 1998).

Description

General features. The single stem specimenfrom which the species is founded is 30 cmlong and slightly flattened in cross section,with a diameter of 27 · 22 cm including theextra-xylary tissue (Figs. 1–2). Its vasculararchitecture is an equisetostele (sensu Rothwell

Fig. 1. Diagram showing main features of crosssection through internode of Arthropitys yunnanensis.pi pith, sx secondary xylem, c cortex, bt branch trace,small dots show position of individual leaf traces.Same specimen as Fig. 2, scale bar = 50 mm

S. J. Wang et al.: Arthropitys from the Permian of China 231

1999) comprising a central pith (P, Fig. 2)surrounded by protoxylem with carinal canals,metaxylem, abundant secondary xylem with

fascicular and interfascicular rays, a cortexwith abundant leaf traces and branch traces,and, externally, a periderm.

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

232 S. J. Wang et al.: Arthropitys from the Permian of China

Pith. The pith is hollow and large with adiameter 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 withcarinal canals surrounds the pith. There areapproximately 150 xylem strands present(Fig. 2) with an average spacing betweenstrands of 2.0 mm (Figs. 2–3). In cross section,carinal canals have radial diameters of500—1350 lm and a tangential diameter of150–270 lm. Each carinal canal is triangularor V-shaped (Figs. 4–5) surrounded by nearlyisodiametric elements 30–120 lm in diameter(typically > 60 lm) with light colored, thickcell walls (usually > 5 lm thick). The cavity ofthe carinal canal is lined by a single row of verysmall elements that are the remains of proto-xylem tracheids (arrow, Fig. 5). Protoxylemtracheids are 10–35 (usually 20–30) lm indiameter and are dark brown in color withannular thickenings (arrow, Fig. 6). Elementssurrounding the carinal canal are 2–4 cellsthick on the lateral sides of the cavity and 7–9cells thick on the internal side of the cavity(Fig. 5). In longitudinal section these elementsare variable in shape, from flattened, nearlysquare to longitudinally elongate with hori-zontal or tapered end walls, and vary from 45–340 (typically > 80) lm long (Fig. 6). We havebeen unable to observe any thickening orpitting on the cell walls, precluding theirinterpretation as metaxylem tracheids.

Secondary xylem. A broad zone of sec-ondary xylem is present on the external side ofeach carinal canal (Fig. 4). Secondary xylemranges from 2.6–3.0 cm in thickness and isdivided into fascicular segments of wood andinterfascicular parenchymatous rays (Figs. 3–4). Fascicular segments of wood in contact tothe carinal canal are 400–750 (usually 450–550)lm wide and contain 14–16 rows of elementsthat include tracheids and fascicular rays.These increase in width centrifugally to about1.37–2.5 (usually 1.4–1.8) mm comprisingapproximately 20–30 rows of cells at a distanceof 10 mm from the margin of the pith, and

Figs. 6–8. Anatomical features of Arthropitys yun-nanensis. All scale bars = 300 lm. 6 Tangentiallylongitudinal section through a carinal canal showingprobable metaxylem (MX) in the middle andsurrounding tissue (ST) at each side. Slide: WP2–0016. 7 Cross section showing interfascicular ray (IR)and fascicular wedge of wood (FWW) and growthring (GR). Slide: WP2L-0011. 8 Radial sectionthrough secondary xylem showing tracheids andheterogeneous fascicular ray. Slide: WP2-0102

S. J. Wang et al.: Arthropitys from the Permian of China 233

2–3.25 (usually 2.3–2.6) mm comprising ofapproximately 30–40 rows of cells at themargin of the wood (Fig. 4). Tracheids arenearly square with round angles in crosssection (Fig. 5). The innermost wood tracheidsare small with diameters between 15–20 lmand their diameter enlarges outwards where itcan reach 73 lm in average. The outer layer ofthe tracheid wall is thin and dark browncolored, and is often poorly preserved orabsent. Internal to this layer is a thicker andlighter-colored zone with a thickness generallyof >5 lm. In some tracheids an inner layer ispresent that is in dark brown color and oftenthicker than the middle or light-colored layer.The inner layer is of unequal thickness and isthickest at the four corners and usually thickerat the tangential wall than at the radial wall.Tracheids with tri-layered walls usually have amore or less smaller radial size and largertangential size than those with bi-layered walls,and tend to be distributed in tangential zonesthat are usually 4–10 tracheids thick in theirradial direction (GR in Fig. 7). There areabout ten such zones in the wood (Fig. 3)interpreted to be growth banding. Scalariformpitting occurs on radial wall of the tracheidsand there are about 54–66 pits every 500 lm(Figs. 8, 10). Each elongate scalariform pit isapproximately 30–35 · 3–4 lm in diameter.Occasionally there are also scalariform pits onthe tangential tracheid walls.

The fascicular ray cells are parenchyma-tous and mainly empty but some possess darkbrown colored resin-like contents. Fascicularrays are narrow in cross section (Fig. 7) withsmaller tangential diameters ranging from 20–50 (average 31) lm, and larger radial diametersranging from 60–270 (average 91) lm. Inradial section fascicular rays are heteroge-neous, consisting of brick-like cells and colum-nar cells with different height, ranging from50–190 (average 94) lm (Fig. 8). In each cross-field there are numerous (sometimes > 10)nearly round, oval and obliquely located orhorizontally elongate pits (Fig. 9). In tangen-tial section fascicular rays are 1–50 (usually10–20) cells high and 1–3 (occasionally 4) cells

wide. Ray cells are somewhat vertically elon-gated and of different heights (Fig. 13). Raycells usually have light colored cell walls thatare slightly thinner than those of the tracheidsbut some have an inner dark colored layer(Fig. 8) and these cells are usually distributedin the zones of tracheids with three layeredwalls. Nearly round or slightly elongate pitsoccur on tangential walls of ray cells (Fig. 14).

Interfascicular rays start from the pith at awidth of ca. 2 mm (Fig. 4), taper gentlycentrifugally in the inner 1/3 of wood thick-ness, and then maintain a similar width orincrease in width slightly to the outer marginof the wood (Fig. 3). Rays mainly consist ofparenchyma cells. Generally 1–3 rows of raycells on both sides of the interfascicular rays orneighboring the fascicular segments of woodare of different shape and size and also have adifferent cell walls morphology from those cellsoccurring elsewhere in the rays. These periph-eral cells usually have smaller tangential diam-eter (25–100 lm) and more or less oblique ends(Fig. 7). Their walls are usually thick and lightcolored and of consistent thickness. In con-trast, the other cells have larger tangentialdiameters (65–150 lm) and have straight endsso are usually rectangular in shape. These cellshave thinner and dark colored cell walls, anddo not appear to be very resilient as evidencedby the middle parts of many rays being hollowor containing only a few remaining cells. Thisis especially common in the inner 1/3 of thesecondary xylem.

In radial section interfascicular ray cells aremostly brick-like with straight tangential walls,but some are horizontally elongated and havetapering ends. However, in the inner part ofthe secondary xylem some cells in the centre ofinterfascicular rays are slightly tangentially orhorizontally elongated. The interfascicularrays extend axially over the entire length ofthe internode, and their position alternatesfrom internode to internode (Figs. 11, 12).Internodal regions usually have a length of20–25 mm (Fig. 11).

Phloem. In most of places the tissue bor-dering the external margin of the secondary

234 S. J. Wang et al.: Arthropitys from the Permian of China

Figs. 9–15. Xylem and ray structures of Arthropitys yunnanensis. 9 Enlargement of fascicular ray from Fig. 8showing pits in cross-field and different shaped ray cells. Scale bar = 250 lm. 10 Radial section of secondaryxylem with elongate scalariform pits on tracheid walls. Scale bar = 250 lm. Slide: WP2-0102. 11 Tangentialsection through secondary xylem showing nodes and internodes. Scale bar= 20 mm. Peel: H35-tan2. 12Highermagnification of Fig. 11 showing multiseriate fascicular ray with large leaf trace within it (arrow). Scale bar =1 mm. 13Tangential 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. 15Cross section through stem showing area between outmost secondary xylem (SX) and the cortex (C), arrowsindicate small black-colored secretory cells arranged in tangential rows. Slide: WP2-0007; Scale bar = 300 lm

S. J. Wang et al.: Arthropitys from the Permian of China 235

xylem can not be distinguished from thecortex, though in some places small dark-colored secretory cells are richer in numberthan elsewhere. These secretory cells are moreor less in tangential rows (Fig. 15).

Cortex. The cortex is up to 30 mm thickand consists of three kinds of cells that areloosely arranged; apparently empty paren-chyma cells, parenchyma cells containing lightyellow colored cell contents, and small secre-tory cells containing dark brown coloredcontents. In cross section these three kinds ofcells have no regular pattern to their distribu-tion and occur either individually or in groups(Figs. 16, 19). The empty and filled paren-chyma cells are usually greater than 100 lm inmaximum dimension, varying in shape fromnearly isodiametric to square, rectangular andoccasionally triangular (Fig. 19). The smallsecretory cells range from 40–60 lm in max-imum dimension and are typically square orrectangular (Fig. 19). In longitudinal sectionthe small dark-colored secretory cells arearranged in vertical files (Figs. 22, 23). Insome sections secretory cells are preferentiallydistributed in proximity to the secondaryxylem (Fig. 15).

Periderm. A periderm-like tissue is some-times preserved at the periphery of the stem.It consists of sequential layers that may havebeen formed from successive phellogens. Themost prominent layers consist of apparentlycoalified and radially arranged cells withdark contents: they may represent phellem(PM, Fig. 24). They alternate with layersof thin walled cells that may representphelloderm (PR, Fig. 24). This periderm-liketissue is only observed in a small area of thestem.

Leaf traces. Leaf traces extend in a hori-zontal course in the secondary xylem. They arelarge and singly associated with low and broadmultiseriate fascicular (secondary) rays 1–1.7 mm high and 0.37–0.5 mm wide in tan-gential section (Fig. 12). Sometimes leaf tracesare also associated with the interfascicular raysand located in their ends rather than their

middle part. Within the leaf traces tracheidsrange from 14–60 (mostly 30–40) lm indiameter, and intermediate with ray cells thatrange from 30–70 (mostly 30–50) lm indiameter.

The cortex has many leaf traces preservedthat are arranged in 2 rings or whorls althoughin some parts of the stem 3 rings of leaf tracesare seen (Figs. 1, 16). Leaf traces positionedvery close to the secondary xylem are usuallynearly round in cross section with concentri-cally developed secondary xylem. Outward theleaf traces become smaller in size and possessless secondary xylem, and the secondary xylemoccurs in a fan to wedge-shaped arrangement(Figs. 19, 20). Tracheids of the secondaryxylem possessing scalariform thickenings. Theleaf trace is mesarch. When the leaf traces arefar enough from the secondary xylem theyloose their secondary xylem and only primaryxylem is present (Figs. 16, 18).

The pattern of leaf trace departure hasbeen determined from serial cross sections thatshow the leaf traces to move very slowlyoutward. From the orientation of the serialpeels it is deduced that individual leaf tracespass outwards through the cortex in a verysteep to vertical course. Importantly thiscourse is orientated upwards and outwardsand is characteristic of leaf traces rather thanadventitious roots that pass outwards anddownwards from the stem.

Branch traces. Only a few branch traceshave been observed. In tangential sectionthrough the secondary xylem branch tracesare circular and small with a diameter of5 mm. Within branch traces vascular bundlesare poorly developed and are generally hardto distinguish. Branch traces have a large pithconsisting of tissue similar to the cortexexcept that the cells are smaller. Branchtraces pass through the secondary xylem ina horizontal course. In the cortex branchtraces are elliptical in cross section andtangentially elongate. Individual branch tracesconsist of numerous vascular bundles that aredistributed at equal distances from each other

236 S. J. Wang et al.: Arthropitys from the Permian of China

(Figs. 17, 21). These bundles are generallysmaller than those observed in leaf traces, andhave little or no secondary xylem present(Fig. 17). In cross section through the stemfour branch traces have been observed at thesame level (Fig. 1).

Discussion

Comparisons. Gross morphology and anat-omy of the stem described here are consistentwith that of the genus Arthropitys Goeppert(1864). Within Arthropitys characters of the

Figs. 16–23. Cortex, leaf and branch traces of Arthropitys yunnanensis. 16 Cross section through cortexshowing 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 branchtrace with weakly developed secondary xylem. Scale bar = 200 lm. 18 Enlargement of Fig. 16 showing a smallleaf trace from the outer ring that lacks extensive secondary xylem development. Scale bar = 200 lm. 19Enlargement 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 extensivesecondary xylem. Scale bar = 200 lm. 21 Cross section through cortex showing half of a tangentially elongatedbranch trace consisting of very small bundles (arrows). Scale bar = 1 mm. 22 Longitudinal section throughcortex showing large, empty and brown-filled cells and small dark-colored secretory cells arranged in verticalfiles (arrows). Scale bar = 1 mm. 23 Enlargement of Fig. 22 showing vertical files of small dark-coloredsecretory cells (arrows). Scale bar = 200 lm

S. J. Wang et al.: Arthropitys from the Permian of China 237

interfascicular rays are important for specificdelimitation (Williamson and Scott 1894,Knoell 1935, Anderson 1954, Andrews 1952,Cichan and Taylor 1983, Wang et al. 2003).Interfascicular rays range from large andbroad consisting of more than 20–30 cells suchas A. approximata and A. major, to smallerrays only several cells wide such as A. versi-foveata and A. bistriata, and can be absent asin A. hirmeri. A further variation seen in theinterfascicular rays of Arthropitys are their sizeas they pass through the secondary xylem. Forexample, in some species such as A. versifove-ata and A. kansana the interfascicular raysremain of constant in width through thesecondary xylem. Interfascicular rays in otherspecies can vary greatly in width through thesecondary xylem, either narrowing rapidlyoutwards as in A. communis or broadeninggradually as in A. deltoides. The specimendescribed here has interfascicular rays that arepersistent in width through the secondaryxylem, and are wide and usually more than15 cells across. This is different from manyother species and only four species of Arthrop-itys possess persistent interfascicular rays:A. kansana, A. bistriata, A. versifoveata andA. deltoides. However they are different fromour specimen in the width of the interfascicularrays and their pattern of change through thesecondary xylem. In A. kansana and A. versi-

foveata, interfascicular rays are narrow, 4–6cells wide, and maintain their width throughthe secondary xylem (Andrews 1952, Anderson1954). In A. deltoides, the interfascicular raysbroaden conspicuously toward the peripheryof the secondary xylem because of the increaseof the tangential dimension of the ray cells(Cichan and Taylor 1983). However A. delto-ides is a much smaller stem than our specimen.The specimen we describe here has interfasci-cular rays that taper only a small amountthrough the inner 1/3 of the secondary xylemat which point they then maintain their widthoutward to the periphery of the secondaryxylem. Renault (1893, Pl. 45, figs. 1, 3)illustrates the pattern of change in width ofthe interfascicular ray in A. bistriata, and thisis similar to that of the present specimen exceptthat the width of the former is much smaller,only 6–7 cells wide (Renault 1893, 1896;Andrews 1952; Boureau 1964) and the latter,more than 15 cells wide. In tangential sectionthe cells of interfascicular rays of the presentspecimen are round, however those of otherfour species are all more or less verticallyelongate.

The secondary xylem also plays an impor-tant role in specific delimitation within Ar-thropitys. Important characters include pittingpatterns on the radial tracheid walls, fascicularrays and their change from the inner to outerparts of the secondary xylem, the change of thewidth of fascicular segments in the secondaryxylem (Anderson 1954), and even the size oftracheids (Cichan and Taylor 1983).

In pitting patterns, the present specimen iscomparable to A. deltoides in possessing elon-gate scalariform pittings. In A. kansana, circu-lar to slightly elongate bordered pits exist,while in A. bistriata and A. versifoveata thetracheids exhibit a random mixture of scalar-iform and reticulate bordered pits. The tan-gential walls of the cells of fascicular rays inthe present specimen sometimes are pitted, andthis has not previously been mentioned for thespecies A. deltoides, A. kansana, A. versifove-ata, and A. bistriata. In radial section,A. bistriata exhibits homogeneous fascicular

Fig. 24. Higher magnification of the area indicatedby arrow in Fig. 2 showing periderm; PM-phellem,PR-phelloderm. Scale bar = 500 lm

238 S. J. Wang et al.: Arthropitys from the Permian of China

rays, but the other three species (A. deltoides,A. kansana, A. versifoveata) and the presentspecimen possess heterogeneous ones.

The change of the width of the fascicularsegments from the inner to outer parts of thesecondary xylem is different in the presentspecimen from the other four species that havepersistent interfascicular rays. In A. deltoides,the fascicular segment is wedge-shaped with itswidth gradually increasing outward (Cichanand Taylor 1983). In A. kansana and A. versi-foveata, the fascicular segments maintain theirwidth through the secondary xylem and theirinner edges are blunt (Andrews 1952, Ander-son 1954). The fascicular segments of thepresent specimen and A. bistriata broadensoutward very slowly and possess a taperedinner edge. The characters of interfascicularrays and fascicular segments in the presentspecimen and other four similar species notedabove are summarized in Table 1. The distinc-tion of the specimen described here agrees withTian and Gu’s (in Li and Cui 1995) taxonomicconclusion leading to the erection of Arthro-pitys yunnanensis.

Characters of systematic significance in

Arthropitys. In the specimen we describe,large and radially elongate carinal canals aredeveloped that range from 500–1350 lm inradial dimension and from 150–270 lm intangential dimension. In other species carinalcanals are smaller and are usually less than200 lm in diameter. Some authors havequestioned the validity of carinal canal sizeas criterion for species recognition withinArthropitys. Anderson (1954) considered itsuse negligible as it appears to vary withchanging pith diameter. Andrews (1952) con-sidered this useful only as a supplementarycharacter if other distinguishing features arepresent. From the single specimen of Arthro-pitys yunnanensis described here it is notpossible to determine if this character varieswithin the species. The distinctive band ofthick-walled cells surrounding the carinalcanals, laterally and internally, constitutes aparticularly distinctive structure. We did notfind evidence of thickening/pitting of the cell

walls to support a possible interpretation ofthese cells as centripetal metaxylem tracheids.Marguerier (1970) and Langiaux and Margu-erier (1980) designated as ‘‘gaine medullaire’’a comparable zone of thick-walled cellssurrounding the carinal canal in Arthropitysbistriata and A. communis. Andrews (1952)was also unable to observe specialized thick-ening of the walls of similar cells in otherspecimens of Arthropitys.

In the stem of Arthropitys yunnanensisdescribed here the cell walls of the interfasci-cular rays and fascicular rays are pitted indifferent directions. This feature has not beenmentioned in other species. The systematic,phylogenetic and environmental significance ofthis variation is at present unknown.

Similar to the secondary tissues of thepresent specimen, secondary xylem of A.deltoides also consists of large tracheids, withboth taxa having average tracheid diameters inexcess of 70 lm. However, other species ofArthropitys possess smaller secondary trac-heids, for example, in A. communis the sec-ondary tracheids and average in A. communis35 · 30 lm and 52 · 50 lm in A. junlianensis.Some authors consider size of the tracheids tobe of little taxonomic significance (e.g. Ander-son 1954), whereas other authors consider thisto be more or less stable within a single speciesand suggest that it does not vary throughontogeny or as phenotypic plasticity (e.g.Cichan and Taylor 1983). Because we onlyhave a single specimen, we are unable toconsider the significance of large secondarytracheid diameters in A. yunnanensis at thepresent time.

Growth rings and environmental varia-

tion. Growth rings are rarely developed inthe secondary xylem of pteridophytes such asarborescent lycopsids and calamites. AlthoughSeward (1898) considered that growth ringswere absent in the secondary xylem of cala-mites, more recent accounts document calam-itean stems with weakly developed growthrings from the Late Paleozoic floras ofEuramerica. Andrews and Agashe (1965)reported a large calamitean stem of Arthropitys

S. J. Wang et al.: Arthropitys from the Permian of China 239

Table

1.Comparisonofmain

featuresofspeciesofArthropityswithsimilarinterfascicularraystructure

toA.yunnanensis

Species

Interfascicularray

Fascicularray

Fascicularsegment

Changepattern

Cellshapein

t.s.

Cellshapein

t.s.

Cellshapein

r.s.

Changepattern

Radialtracheid

wallpitting

A.deltoides

Broadening

conspicuously

outw

ard

Inner

woodstrongly

verticallyelongate;

outerwoodslightly

verticallyelongate

Inner

woodstrongly

verticallyelongate;

outerwoodslightly

verticallyelongate

Heterogeneous

Broadening

gradually

outw

ard

Elongate

scalariform

A.bistriata

Sim

ilarto

thatof

A.yunnanensis

Nearlyisodiametrically

polygonal

Strongly

vertically

elongate

Homogeneo

us

Sim

ilarto

thatof

A.yunnanensis

Random

mixture

ofscalariform

and

reticulate

bordered

pits

A.kansana

Maintainingsame

width

throughs.x.Slightlyvertically

elongate

Sim

ilarto

A.yunnanensis

Heterogeneous

Maintainingthe

width

throughs.x.Circularto

slightly

elongate

bordered

pits

A.versifoveata

Sim

ilarto

thatof

A.kansana

Sim

ilarto

thatof

A.kansana

Sim

ilarto

thatof

A.yunnanensis

?Sim

ilarto

thatof

A.kansana

Sim

ilarto

thatof

A.bistriata

A.yunnanensisTaperingoutw

ard

graduallythrough

inner

1/3

ofs.x.

then

maintaining

width

outw

ards.

Round

Somew

hatvertically

elongate

with

variable

height

Heterogeneous

Broadening

gradually

outw

ards

Elongate

scalariform

240 S. J. Wang et al.: Arthropitys from the Permian of China

communis var. septata Andrews that has sec-ondary xylem of up to 12 cm in thickness thathad more than 10 faint growth rings. Thedistance between neighboring growth ringsvaries greatly, but the size difference of trac-heids is only slight leading to conclusions thatclimatic variation during the life of the plantwas minimal (Andrews and Agashe 1965).Scott et al. (1986) recorded an Archaeocala-mites stem with three well developed growthrings in which the distance between neighbor-ing rings was also considerable. In this exam-ple, size differences of the tracheids are evident,leading Scott et al. (1986) to conclude thatthese growth rings recorded ecological changesin environmental stress such as periods ofdrought rather than regular seasonal or cli-matic variation. In the present specimen,growth rings are conspicuous and continuousthrough the entire circumference of the sec-ondary xylem, with nearly equal distancesoccurring between neighboring rings. Further-more, the size differences between tracheids indifferent rings is not prominent. It is difficult tomake determinations about the cause of thisvariation without additional specimens of dataon environmental conditions. However, wenote that previous accounts of permineralizedgymnosperm wood from the same region andgeological horizon lack growth rings includingGuizhouoxylon dahebianense Tian et Li (1992)andWalchiopremnon gaoi Tian et al. (1994). Inthis regard we agree with the conclusions ofScott et al. (1986) and consider it more likelythat the growth rings in Arthropitys yunnanen-sis reflected repeated changes in environmentalstress and probably relate to changes in wateravailability within the growth environmentrather than indicating seasonality. Palaeocli-matic models for the Upper Permian ofsouthern China also suggest the absence ofseasonality (e.g. Quan 1992, Rees et al. 1999).

Leaf and branch traces. Position and struc-ture of leaf and branch traces in Arthropitysyunnanensis are novel. Leaf and branch traceshave been previously reported passing throughthe secondary xylem of calamitean stems, andalthough a number of stems of Arthropitys

with extra-xylary tissue have been studied(Williamson 1871, 1878; Williamson and Scott1894; Renault 1893; Agashe 1964; Eggert 1962;Cichan and Taylor 1983; Wang et al. 2003),leaf traces and/or branch traces have not beenfound in the cortex. In A. yunnanensis thepresence of whorls of leaf traces in the cortex isunique. This shows that leaf traces had a veryoblique to vertical course through the cortexinstead of being nearly horizontally orientatedas generally assumed for this genus. This maybe typical of this species and of the develop-mental pattern of this particular species.

Periderm. There is evidence of a periderm-like tissue composed of concentric or sequen-tial layers that may be formed by successivephellogens. This periderm is comparable to therhytidome made of ‘‘six concentric lamellae’’described by Cichan and Taylor (1983) inA. deltoides. However in A. yunannensis theperiderm is a narrow zone preserved at theperiphery of a massive cortex representing theprimary body of the plant. The situation iscompletely different in A. deltoides that is avery small stem with no evidence of primarycortical tissues.

Ontogeny and development. Comparedwith data provided by Eggert (1962, Table 1)on ontogenetic variation in Arthropitys,A. yunnanensis is a large plant that hascharacters consistent with Eggert’s epidoge-netical phase of development of an aerialplant. In particular, A. yunnanensis has abroad stem diameter (>20 cm) with anextremely broad zone of primary xylem(>100 mm diameter) – the largest stem stud-ied by Eggert had a primary xylem diameter of67 mm. The number of primary vascularstrands in A. yunnanensis (approximately 150)is comparable with the values given by Eggertwho observed a maximum of 172 in otherspecies. These size features of A. yunnanensisare near the maximum for the epidogeneticalphase (Eggert 1962), and suggest this speci-mens is a basal part of the stem. This isconfirmed by the relatively short length ofinternodes in A. yunnanensis, typically 20–25 mm.

S. J. Wang et al.: Arthropitys from the Permian of China 241

Ontogenetic age of the plant. The bestindicator for the age of the plant is thethickness of the secondary xylem (c. 30 mm)that compares to the maximum values given byEggert (1962). However, this does not meanthat the plant was old, as much larger stems areknown; Andrews and Agashe (1965) describedspecimens with wood 120 mm thick, i.e. fourtimes thicker than A. yunnanensis, and thesewere certainly much older stems. FurthermoreRossler and Noll (pers. com. 2005) are describ-ing a specimen of Arthropitys from the Permianof Chemnitz that is c. 60 cm diameter compris-ing c. 30 cm of wood and a pith/primary xylemless than 2 cm diameter with 74 primary xylemstrands. Secondly, the occurrence of a broadcortex (= primary body) suggests that theplant was relatively young as the cortex has notbeen sloughed off by periderm development.The occurrence of a periderm like tissue that isvery narrow and restricted to a small portion ofthe periphery is not an argument against this,because it may be just the beginning ofperiderm development in this plant.

As noted above, the occurrence of com-plete primary cortical tissues is exceptional insuch a large stem and, as Eggert (1962) noted,such tissues generally are missing althoughthey remain the only source from which todetermine the number of leaves on a node ofthe stem. As indicated by Eggert (1962) thisnumber is not strictly related to the numberof cauline primary vascular strands, as inEquisetum; indeed, in those small stems ofCalamites where the cortex is preserved, thereis generally one leaf trace per strand, but inlarge stems there is one leaf trace per twostrands.

Habit of the plant. Previous reconstruc-tions of calamitean plants (e.g. Boureau 1964)suggested a significant diversity of habits. Thiswas supported by recent evidence (Bartheland Rossler 1996) that the large stemmedCalamites gigas was a succulent calamite.Furthermore, biomechanical analyses ofextinct calamites (Mosbrugger 1990, Spatzet al. 1998) suggest the presence of self-sup-porting and semi-self-supporting habits. The

main contributor to mechanical support inthese plants was the peripheral wood cylinderin which lignified tissues, such as secondaryxylem, provided efficient mechanical supportnot provided by non-lignified tissues (Spatzet al. 1998). The vascular cylinder of A.yunannensis is noteworthy as it possesses wideinterfascicular rays composed of non-lignifiedtissue that was unlikely by itself to provideeffective support. Interfascicular tissues com-prise c. 50% of the vascular cylinder with theother c. 50% being the fascicular zone of woodcomprising lignified tissue. This c. 50/50 ratioof fascicular/interfascicular tissue is compara-ble to that observed in A. deltoides, interpretedby Cichan and Taylor (1983) as a feature of alianescent or semi-self supporting habit. Ci-chan and Taylor (1983) also emphasized thelarge diameter of wood tracheids as indicativeof liana wood, a feature also found in A.yunannensis. Despite the major difference insize between A. deltoides and A. yunnanensis,they may both represent semi-self supportingplants similar to lianas. The description of thisnew species from China increases significantlyour knowledge of the habit diversity in calam-itean plants.

We are grateful to Shao Longyi for discussionson the age of the Xuanwei Formation, Ming-MeiLiang for help and support on WSJ’s research visitto the UK, and Bill DiMichele and an anonymousreviewer for comments on the manuscript. Thiswork was supported by the National NaturalScience Foundation of China (Award 30170064 toWSJ), the Special Fund from the Director ofInstitute of Botany, CAS (to WSJ), the ChineseAcademy of Sciences (XSCX2-SW-108 to WSJ)and an Anne Sleep Award of the Linnean Societyof London (to JH).

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Addresses of the authors: Shi-Jun Wang (e-mail:wangsj@ibcas.ac.cn), State Key Laboratory ofSystematic and Evolutionary Botany, Institute ofBotany, Chinese Academy of Sciences, Xiangshan,Beijing, 100093, P. R. China. Jason Hilton (e-mail:j.m.hilton@bham.ac.uk), School of Geography,Earth and Environmental Sciences, University ofBirmingham, Edgbaston, Birmingham, B15 2TT,UK. Jean Galtier (e-mail: jean.galtier@cirad.fr),UMR Botanique et Bioinformatique, CIRAD,TA40/PS2, Boulevard de la Lironde, 34398 Mont-pellier, Cedex 05, France. Baolin Tian, BeijingGraduate School, China University of Mining andTechnology, Beijing 100083, P. R. China.

244 S. J. Wang et al.: Arthropitys from the Permian of China