IAWA Journal, Vol. 27 (2), 2006: 129–136

WOOD ANATOMY OF () FROM SOUTHEASTERN YUNNAN, CHINA

Steven R. Manchester1, Zhiduan Chen2 and Zhekun Zhou3

SUMMARY anatomy of Craigia W.W. Sm. & W.E. Evans ( s.l.), a endemic to China and Vietnam, is described in order to provide new characters for assessing its affinities relative to other malvalean genera. Craigia has very low-density wood, with abundant diffuse-in-aggre- gate axial parenchyma and tile cells of the type in the multiseriate rays. Although Craigia is distinct from by the pres- ence of tile cells, they share the feature of helically thickened vessels – supportive of the sister group status suggested for these two genera by other morphological characters and preliminary molecular data. Although Craigia is well represented in the fossil record based on , we were unable to locate fossil corresponding in anatomy to that of the extant . Key words: Craigia, Tilia, Malvaceae, wood anatomy, tile cells.

INTRODUCTION

The genus Craigia is endemic to eastern Asia today, with two in southern China, one of which also extends into northern Vietnam and southeastern Tibet. The genus was initially placed in (Smith & Evans 1921; Hsue 1975), then (Ren 1989; Ying et al. 1993), and more recently in the broadly circumscribed Malvaceae s.l. (including Sterculiaceae, Tiliaceae, and ) (Judd & Manchester 1997; Alverson et al. 1999; Kubitzki & Bayer 2003). Similarities in morphology and staminodes (Judd & Manchester 1997), and chloroplast gene sequence data (Alverson et al. 1999) have suggested a sister relationship to Tilia. Kubitzki and Bayer (2003) circumscribed the of the Malvaceae to include only the genera Craigia and Tilia. Although the Tilia–Craigia clade is well supported by the ndhF analysis (Alverson et al. 1999), Craigia was not included among the malvalean genera studied for plastid atpB or rbcL DNA sequences investigated by Bayer et al. (1999), and the validity of this relationship needs to be tested by other data. Wood anatomy provides useful characters for distinguishing genera among Malvales (Chattaway 1933, 1938; Manchester & Miller 1978; Terada & Suzuki 1998), yet the anat- omy of Craigia has not been examined before because of a lack of samples. We were

1) Florida Museum of Natural History, Gainesville, FL 32611-7800, U.S.A. 2) Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, P.R. China. 3) The Herbarium and Department of Phytotaxonomy & Phytogeography , Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, Yunnan, P.R. China.

Downloaded from Brill.com10/07/2021 08:53:11AM via free access 130 IAWA Journal, Vol. 27 (2), 2006 Manchester, Chen & Zhou — Wood anatomy of Craigia 131 interested to examine the anatomy of Craigia, to evaluate its systematic position relative to other Malvales. Craigia has an excellent fossil record of fruits in North America, Europe and Asia, indicating that the present distribution is relictual (Kvaček et al. 1991, 2002). However, it has been impossible to determine whether fossil woods of the genus are present because anatomical characteristics of the modern genus have been unknown. By describing the wood of the extant genus, we hope to facilitate the recognition of fossil representatives.

MATERIALS AND METHODS

On April 21, 2001, we collected pieces of stem wood from a mature tree of Craigia yunnanensis in Fadou, southeastern Yunnan, China (Fig. 1). The tree is about 20 m high, situated on the south side of the town of Fadou, southeastern Yunnan, China (23° 23.29' N lat., 104° 48.25' E long., altitude 1430 m). It occurs in subtropical forest along with scattered Rhoiptelea, Exbucklandia, Aesculus, Fagus, and Lithocarpus. Samples of wood were pried from the external part of the xylem cylinder a few cm inside the bark and about 1.5 m above the base of the tree. The tree had dropped its and fruits due to the dry season; fallen leaves and fruits were collected as voucher material and deposited at the Missouri Botanical Garden (as MO 5301012).

Fig. 1. Craigia yunnanensis tree in Fadau, Xichou County, southeastern Yunnan, China. This photograph was taken with the tree in foliage and , December 23, 1985. The same individual had dropped its leaves and fruits when we collected the wood sample in April, 2001. Photo courtesy of Zhuge Ren.

Downloaded from Brill.com10/07/2021 08:53:11AM via free access 130 IAWA Journal, Vol. 27 (2), 2006 Manchester, Chen & Zhou — Wood anatomy of Craigia 131

Fig. 2–6. Craigia yunnanensis secondary xylem. MADw 49060. – 2: Transverse section show- ing semi-ring porosity. Note wide rays and vessels occasionally in multiples. – 3: Transverse section showing diffuse-in-aggregates parenchyma and rays with both sheath and tile cells. – 4 & 5: Tangential sections showing multiseriate rays with sheath and tile cells. – 6: Radial sec- tion showing Pterospermum type tile cells. — Scale bar = 2 mm in 2, 1 mm in 3–6 (bar in 4 applies also to 5 & 6).

Downloaded from Brill.com10/07/2021 08:53:11AM via free access 132 IAWA Journal, Vol. 27 (2), 2006 Manchester, Chen & Zhou — Wood anatomy of Craigia 133

Fig. 7 & 8. Craigia yunnanensis secondary xylem. MADw 49060. Tangential sections showing vessel elements with helical thickening and alternate intravascular pitting. — Scale bar = 50 μm.

The same individual tree had also been collected earlier by other investigators, and is figured in and fruit (Fig. 1), courtesy of Zhuge Ren in December of 1985. The wood sample was donated to the Forest Products Laboratory, Madison, Wisconsin, and bears the catalog number MADw 49060. We only examined the wood of this single tree of Craigia yunnanensis. The extent of variability within the species is not known, and wood of the other species, C. kwangsiensis, unfortunately, was not available. To determine the specific gravity, a block of wood was dried in an oven at 103°C for 24 hr, then weighed (6.3 g). Its volume was determined by displacement of water when dried (19.9 ml) and after soaking 12 hr (21.7 ml). Specific gravity was calculated as oven-dry weight of wood divided by the mass of the water displaced by the woodʼs volume giving a value of 0.29. After softening in boiling water for several hours, the wood was sectioned with a sliding microtome. Some sections were stained in safranin, and others were left unstained and then mounted on glass slides with Canada balsam.

ANATOMICAL DESCRIPTION

Growth rings distinct, delineated by terminal parenchyma and dilation of the multiseriate rays. Wood semi-ring-porous to diffuse-porous (Fig. 2). – Vessels solitary and in radial multiples of 2 to 3 (5) (Fig. 3); vessel frequency 4–7 pores/mm2; tangential diameter 100–380, mean 252 μm, in earlywood, 70–150 μm in latewood; perforations simple; intervessel pits alternate 6.5–7 μm (Fig. 7 & 8); vessel-ray pits similar to intervessel pits, only rarely scalariform. Helical thickening in all vessel elements (Fig. 7), vessel ele- ment lengths 200–540, mean 416 μm; tyloses not observed. – Fibers non-septate, no

Downloaded from Brill.com10/07/2021 08:53:11AM via free access 132 IAWA Journal, Vol. 27 (2), 2006 Manchester, Chen & Zhou — Wood anatomy of Craigia 133

pits observed. – Axial parenchyma in strands of 1 to 4 cells, storied within tracts (Fig. 5), both vasicentric and diffuse-in-aggregates, commonly in uniseriate tangential lines separated by 1–3 tangential rows of fibers (Fig. 3). Cells of vasicentric parenchyma with dark contents as seen in rays, cells of the apotracheal parenchyma lacking dark contents in the observed sample; crystals apparently absent. – Rays heterocellular, 1–15-seriate (Fig. 4 & 5). Uniseriate rays infrequent, composed of exclusively upright cells. Multi- seriate rays commonly with sheath cells and tile cells that are 1–4 times higher than the procumbent cells (Fig. 4– 6), and similar in radial dimension to the axial parenchyma cells. Rays 3.1–4.5 per mm, not storied. Crystals not observed.

DISCUSSION

The most conspicuous features of Craigia wood are its semi-ring porosity, diffuse-in- aggregates parenchyma, rays with tile cells and helically thickened vessel elements. Tile cells are a “special type of apparently empty upright (rarely ) ray cells oc- curring in intermediate horizontal series usually interspersed among the procumbent cells of multiseriate rays.” (IAWA Committee 1989). They are known only from some genera of the Malvaceae (sensu lato), including , Chorisia, , , Desplatzia, , Durio, , , , , Kostermansia, , , , , , , Mollia, Mon- tezuma, Mortoniodendron, Neesia, , , Pterospermum, , , , , , and (OPCN database, E. Wheeler, pers. comm., 2004; Terada & Suzuki 1998). Tile cells vary in size relative to the procumbent cells among different taxa, ranging from the Pterospermum type (higher than the surrounding procumbent cells) to the Durio type (lower than the procumbent cells; Chattaway 1933; Manchester & Miller 1978). Although it has not been emphasized before, tile cells also occur in the Malvalean , as illustrated clearly in several species of by Ilic (1991: 167–169). The occurrence of tile cells does not show any consistent phylogenetic pattern within subclades of the Malvaceae (Judd & Manchester 1997). However, tile cells are defined in such a way that they cannot occur in uniseriate rays. Similarly, they cannot occur in biseriate rays, because such cells would be termed sheath cells. Sheath cells are much more widely distributed across angiosperms than are tile cells, so the distinction is a useful one for purposes of identification. Nevertheless, this distinction between sheath cells and tile cells in Malvales may be artificial, i.e., uniseriate and biseriate rays having the same kind of cells that in multiseriate rays would be classified as tile cells. This character coding problem may explain the apparent homoplasy seen in this feature (Judd & Manchester 1997). The woods of Craigia and Tilia are not as similar anatomically as might have been predicted. Wood of Craigia yunnanensis is less dense (SG = 0.29) than that of Tilia (0.40–0.45, Kribs 1968). The conspicuous tile cells and sheath cells of the rays observ- ed in Craigia do not occur in Tilia, and the parenchyma lines are farther apart in Tilia than in Craigia. The vessels of Tilia are narrower and more densely spaced. All these differences might lead us to question the close affinity between these genera suggested

Downloaded from Brill.com10/07/2021 08:53:11AM via free access 134 IAWA Journal, Vol. 27 (2), 2006 Manchester, Chen & Zhou — Wood anatomy of Craigia 135 by recent investigators. On the other hand, spirally thickened vessel elements, a feature of Tilia (Kukachka & Rees 1943), are also present in C. yunnanensis and might be a synapomorphy. Among traditional ʻTiliaceaeʼ and ʻSterculiaceaeʼ, the only other genera known with spirally thickened vessel elements are Chartacalyx (Kukachka & Rees 1943), Fremonotodendron, Reevesia, and Veeresia (Metcalfe & Chalk 1950; Terada & Suzuki 1998). The shared occurrence of spiral thickening in both Craigia and Tilia might represent a phylogenetically significant synapomorphy, or it might be explained by their adaptation to more temperate conditions. Among dicotyledonous woods in general, there is a higher incidence of spiral thickenings in cooler environments than in warmer environments (Baas 1986; Wheeler & Baas 1993; Wiemann et al. 1998). Given the long histories of both of these genera in temperate environments indicated by the Tertiary fossil record, contrasting with the tropical distribution of the majority of woody malvalean genera, the occurrence of helical thickening could be explained as a parallel climatic adaptation in these two genera. Despite the frequent occurrence of fossil Craigia fruit remains in the Tertiary of Europe, North America and Asia, we failed to find any fossil woods that are referable to the genus. Possibly such low-density wood is less likely to enter the fossil record. Among previously described fossil woods, Craigia is anatomically most similar to the extinct genus Chattawaya from the Eocene of Oregon (Manchester 1980; Wheeler & Manchester 2002). Both have semi-ring porosity, diffuse-in-aggregate parenchyma, and the Pterospermum type of tile cells. Although Manchester (1980) considered Chat- tawaya to be most similar to the extant genus Pterospermum, extant species of that genus have mostly narrower rays with less common multiseriate rays, and the narrow rays are storied. Chattawaya more closely resembles Craigia in having predominantly multiseriate rays. There are, however, differences in vessel distribution and dimensions, and the fossil lacks helically thickened vessel elements. Other malvalean fossil woods with tile cells include Triplochitioxylon from the Eocene of Oregon (Manchester 1979; Wheeler & Manchester 2002), Reevesia from the early Miocene of Japan (Terada & Suzuki 1998), Pterospermoxylon from the Pliocene of (Awasthi et al. 1980), and Grewioxylon from the Tertiary of Europe and Asia (reviewed by Selmeier 2000). Woods assigned to the latter genus include specimens with similarities to Craigia, but apparently lack helically thickened vessel elements. In addition, the fossil genus Wataria from the Oligocene and early Miocene of Japan (Terada & Suzuki 1998; Jeong et al. 2004) is similar in many aspects to Craigia, but it differs by the apparent lack of helically thickened vessels. A more intensive analysis of the fossil malvaceous woods is needed to determine if Craigia is represented among them.

ACKNOWLEDGEMENTS

We thank Dr. Guanghua Zhu for accessioning the voucher specimen in the Missouri Botanical Garden, Dr. Regis B. Miller for accessioning the wood sample and slides in the MADw collection, and Dr. Tang Ya for helpful comments. Jakub Sakala and two anonymous reviewers provided helpful suggestions. This research was supported in part by the Natural Sciences Foundation of China, grant 30130030 to Zhiduan Chen and the National Science Foundation grant INT 0074295 to Steven Manchester.

Downloaded from Brill.com10/07/2021 08:53:11AM via free access 134 IAWA Journal, Vol. 27 (2), 2006 Manchester, Chen & Zhou — Wood anatomy of Craigia 135

REFERENCES

Alverson, W.S., B.A.Whitlock, R. Nyffeler, C. Bayer & D.A. Baum. 1999. Phylogeny of the core Malvales: Evidence from ndhF sequence data. Amer. J. Bot. 86: 1474–1486. Awasthi, N., J.S. Guleria & R.N. Lakhanpal. 1980. A fossil dicotyledonous wood from the Pliocene beds of Mothala, district Kutch, Western India. The Palaeobotanist 25: 199–205. Baas, P. 1986. Ecological patterns in xylem anatomy. In: T.J. Givnish (ed.), On the economy of form and function: 327–262. Cambridge University Press. Cambridge UK. Bayer, C., M.F. Fay, A.Y. De Bruijn, V. Savolainen, C.M. Morton, K. Kubitzki, W.S. Alverson & M.W. Chase. 1999. Support for an expanded family concept of Malvaceae within a recir- cumscribed order Malvales: A combined analysis of plastid atpB and rbcL DNA sequences. Bot. J. Linn. Soc. 129: 267–303. Chattaway, M.M. 1933. Tile cells in the rays of the Malvales. New Phytol. 32: 261–273. Chattaway, M.M. 1938. The wood anatomy of the family Sterculiaceae. Phil. Trans. Royal Soc. B228: 313–365. Hsue Hsiang-How. 1975. Two new species of Sterculiaceae from China. Acta Phytotax. Sinica 15: 72–84. IAWA Committee. 1989. IAWA list of microscopic features for identification. IAWA Bull. n.s. 10: 219–332. Ilic, J. 1991. CSIRO atlas of . Crawford House, CSIRO, Bathorst, Australia. Jeong, E.K., K. Kim, J.H. Kim & M. Suzuki. 2004. Fossil woods from Janggi Group (Early Miocene) in Pohang Basin, Korea. J. Plant Research 117: 183–189. Judd, W.S. & S.R. Manchester. 1997. Circumscription of Malvaceae (Malvales) as determined by a preliminary cladistic analysis of morphological, anatomical, palynological, and chemical characters. Brittonia 49: 384–405. Kribs, D.A. 1968. Commercial foreign woods on the American market. Dover, New York. Kubitzki, K. & C. Bayer. 2003. The families and genera of vascular . V. Malvales, Cap- parales and non-betalain . Springer, Berlin. Kukachka, B.F. & L.W. Rees. 1943. Systematic anatomy of the woods of the Tiliaceae. Univ. Minnesota Agric. Exper. Stat. Tech. Bull. 158: 1–70. Kvaček, Z., Bůžek & S.R. Manchester. 1991. Fossil fruits of Pteleaecarpum Weyland – Tiliaceous not Sapindaceous. Bot. Gaz. 152: 522–523. Kvaček, Z., S.R. Manchester, R. Zetter & M. Pingen. 2002. Fruits and seeds of Craigia bronnii (Malvaceae–Tilioideae) and associated buds from the late Miocene Inden Formation, Lower Rhine Basin, Germany. Rev. Palaeobot. Palyn. 119: 311–324. Manchester, S.R. 1979. Triplochitioxylon (Sterculiaceae): a new genus of wood from the Eocene of Oregon and its bearing on xylem evolution in the extant genus Triplochiton. Amer. J. Bot. 66: 699–708. Manchester, S.R. 1980. Chattawaya (Sterculiaceae): a new genus of wood from the Eocene of Oregon and its implications for xylem evolution of the extant genus Pterospermum. Amer. J. Bot. 67: 59–67. Manchester, S.R. & R.B. Miller. 1978. Tile cells and their occurrence in malvalean fossil woods. IAWA Bull. 1978/2-3: 23–28. Metcalfe, C.R. & L. Chalk. 1950. Anatomy of the . 2 Vol. Clarendon Press, Ox- ford. Ren, Z. 1989. The cladistic analysis of the systematic position of Craigia. Acta Bot. Yunnanica 11: 17–23. Selmeier, A. 2000. Structural variation of Tertiary Grewia woods (Tiliaceae) from East Bavarian Molasse, Germany. Feddes Repert. 111: 465–480.

Downloaded from Brill.com10/07/2021 08:53:11AM via free access 136 IAWA Journal, Vol. 27 (2), 2006

Smith, M.A. & W.E. Evans. 1921. Craigia, a new genus of Sterculiaceae. Trans. Bot. Soc. Edinburgh 28: 69–71. Terada, K. & M. Suzuki. 1998. Revision of the so-called ʻReevesiaʼ fossil woods from the Terti- ary in Japan – a proposal of the new genus Wataria (Sterculiaceae). Rev. Palaeobot. Palyn. 103: 235–251. Wheeler, E.A. & P. Baas. 1993. The potentials and limitations of dicotyledonous wood anatomy for climatic reconstructions. Paleobiology 19: 487–498. Wheeler, E.A. & S.R. Manchester. 2002. Woods of the Eocene Nut Beds flora, Clarno Forma- tion, Oregon, USA. IAWA J., Suppl. 3: 1–188. Wiemann, M.C., E.A. Wheeler, S.R. Manchester & K.M. Portier. 1998. Dicotyledonous wood anatomical characters as predictors of climate. Palaeogeogr., Palaeoclimat., Palaeoecol. 139: 83–100. Ying Tsun-shen, Yu-Long Zhang & D.E. Boufford. 1993. The endemic genera of seed plants of China. Science Press, Beijing.

Downloaded from Brill.com10/07/2021 08:53:11AM via free access