First Record of Moroxylon (Moraceae) from the Neogene of China

168 IAWAIAWA Journal Journal 34 (2), 34 2013: (2), 2013 168–175

Ya-Fang Yin1, Xiao-Li Liu2 and Ye-Ming Cheng3,* 1Wood Anatomy and Utilization Group, Research Institute of Wood Industry, Chinese Academy of Forestry, No. 1 of Dongxiaofu, Haidian District, Beijing 100091, P.R. China 2Beijing Museum of Natural History, No. 126, Tianqiao St, Dongcheng District, Beijing 100050, P.R. China 3The Geological Museum of China, Xisi, Xicheng District, Beijing 100034, P.R. China *Corresponding author; e-mail: [email protected]

abstract A new species of Moroxylon, M. xinhuaensis Yin, Liu & Cheng, with wood anatomical features found in modern Morus (Moraceae), is described from the Neogene of Xinhua, Yuanmou Basin, Yunnan Province, southwest China. This wood represents the first fossil wood ofMorus reported from Asia. It provides additional data for evaluating relationships between the Neogene floras of Europe and eastern Asia. Keywords: Fossil wood, Moroxylon, Morus, Neogene, Yuanmou.

INTRODUCTION

Morus, a genus of deciduous trees and shrubs with 16 species, is widespread across temperate areas of the northern hemisphere (U.S.A., Europe, Japan and China), and extends into tropical regions including the mountains of tropical Africa, Indonesia and South America (Zhou & Gilbert 2003). Species of Morus occur in various types of forest growing both at sea level and up to 2500 m altitude (Ter Welle et al. 1986a). In China, 11 species of Morus are widely distributed as the leaves are used to feed the commercially important silkworms and the mulberry fruit is extensively harvested for human consumption (Zhou & Gilbert 2003). Morus has a Tertiary fossil record indicating that it was once widely distributed throughout North America (U.S.A.), Europe (Czech Republic, Germany, Russia) and East Asia (China) (Collinson 1989; Liu et al. 1996). In this study, we describe a hitherto undescribed wood with similarity to Morus from the Neogene sediments of Yuanmou, Yunnan, China.

MATERIALS AND METHODS

The material described herein was collected from the Earth Forest near Xinhua Village, Yuanmou County, Yunnan Province, southwest China. The sediments of the Xinhua Earth Forest containing sandstone and clay belong to the lower part of the Yuanmou Formation with palaeomagnetic age about 3.4–2.5 Ma B.P. (Qian & Zhou 1991), a Late

Pliocene equivalent of the Shagou Formation (Zhang et al. 1994). Vertebrate fossils also occur in the lower part of the Yuanmou Formation (Pan & Zong 1991). Two fossil wood species, Cedreloxylon cristalliferum (Cheng et al. 2006) and Lagerstroemioxylon yuanmouensis (Cheng et al. 2007), have been described from the Xinhua Earth Forest previously. The material was sectioned following the procedures for permineralised material outlined in Hass & Rowe (1999). Slides are deposited in the Geological Museum of China, Beijing. The thin sections were studied using a microscopic image analyzer (Olympus BX60 with DP72 digital collector). The wood was compared to slides of extant wood species housed in the Wood Collection of the Research Institute of Wood Industry, Chinese Academy of Forestry. Anatomical terms used in this paper follow the recommendations of the IAWA List of microscopic features for hardwood identification (IAWA Committee 1989).

SYSTEMATIC DESCRIPTION

Family: Mo r a c e a e Genus: Moroxylon Selmeier 1993 Species: Moroxylon xinhuaensis Yin, Liu & Cheng, sp. nov. (Fig. 1) Specific diagnosis: Growth ring boundaries distinct. Wood ring porous to slightly semi-ring porous. Vessels in earlywood solitary and in radial or oblique multiples of 2 to 3, latewood vessels in clusters and in radial or oblique multiples of 2–5. Perfora- tion plates simple. Helical thickenings only in narrow vessels, along their entire length. Thin-walled tyloses common. Intervessel pits crowded, alternate, polygonal in outline. Vessel-ray and vessel-parenchyma pits similar to intervessel pits or large and elongate to oval with narrow borders. Parenchyma vasicentric, partly confluent, and marginal. Rays 1–10 cells wide, composed of procumbent body cells and 1–3 (mostly 1) marginal rows of square and/or upright cells. Holotype: P2323, specimen 18 cm long, 5 cm in width. Type locality: Xinhua Village, Yuanmou County, Yunnan Province, China. Lithostratigraphic horizon: Lower part of the Yuanmou Formation. Age: Pliocene. Etymology: The specific epithet is after the fossil locality. Repository: the Geological Museum of China, Beijing, China.

Description Wood ring porous to occasionally slightly semi-ring porous. Growth rings distinct, marked by a change in vessel diameter and distribution from the latewood to the earlywood of subsequent rings, and marginal parenchyma. Narrow growth rings with one row of earlywood pores, wide growth ring with several rows of earlywood pores. Vessels in earlywood either solitary or in radial to oblique multiples of 2 to 3, circular to oval in cross section; mean tangential diameter of solitary vessels 235 µm (range 180–296 µm), mean radial diameter of solitary vessels 299 µm (range 210–400 µm). Latewood vessels in radial or oblique multiples of 2–5, or clusters. Vessel frequency in the latewood 8–17/mm2. Perforation plates simple. Intervessel pits alternate, round 170 IAWA Journal 34 (2), 2013

Figure 1. Moroxylon xinhuaensis Yin, Liu & Cheng, sp. nov. (Moraceae) (P 2323). – A: TS, distinct growth rings, ring porous to semi-ring porous wood, vessels predominantly solitary in earlywood and mostly in radial multiples and clusters in latewood. – B: TS, vessel clusters in latewood, vasicentric parenchyma (upper arrows) and marginal parenchyma (lower arrows). –

Yin et al. – Moroxylon from China 171 to polygonal, 8–13 µm in diameter, pit apertures lens-shaped, sometimes coalescing. Helical thickenings present along the whole length of the narrow vessel elements. Mean vessel element length 243 µm (range 155–305 µm). Vessel-ray and vessel-parenchyma pits either similar to intervessel pits or large and elongate to oval with narrow borders. Thin-walled tyloses common. Axial parenchyma vasicentric, partly confluent, and marginal. Rays 2–4/mm, 1–10-seriate, mostly 6–10-seriate, uni- and biseriate rays few. Multiseriate rays 272–1382 µm (mean 678 µm) high and 30–127 µm (mean 75) wide; composed of procumbent body cells with 1–3 (mostly 1) marginal rows of square or upright cells.

DISCUSSION Comparison with extant woods The diagnostic characters of this fossil, namely ring porous to slightly semi-ring porous wood, vessels solitary and in radial or oblique multiples or clusters, simple perforation plates, alternate intervessel pits, helical thickenings in narrow vessels, vessel- ray pits similar to intervessel pits with narrow borders or simple, abundant thin-walled tyloses, vasicentric to partly confluent parenchyma, and heterocellular rays, indicate its affinities are with Moraceae (Tippo 1938; Metcalfe & Chalk 1950; Ter Welleet al. 1986a, b; Cheng et al. 1992; Wheeler 2011; InsideWood 2004-onwards). The present-day ring porous Moraceae woods compared to the fossil include species of Maclura Nutt., Broussonetia Orteg. and Morus L. (Tippo 1938; Koek-Noorman et al. 1984a, b, c; Ter Welle et al. 1986a, b). The difference between Maclura and the fossil lies in the presence of some homocellular rays and long crystalliferous parenchyma strands in Maclura (Fig. 2A–D), which are absent from the fossil (Fig. 1A–H). Broussonetia and Morus differ in ray pattern and parenchyma. Ring porous species of Broussonetia have rays with 1–4 marginal cells, scanty paratracheal parenchyma, occasionally aliform with short wings, and in initial bands up to 20 cells wide (Fig. 2E–H), and multiseriate rays measure up to 410–510 µm high and 3–5(–7) cells wide (Fig. 2F, G). Rays in Morus have exclusively one row of upright or square marginal cells, but are similar to the fossil in being mostly 4–6 cells wide and measuring up to 425–1100 µm high (Ter Welle et al. 1986a). Parenchyma is both paratracheal, vary- ing from vasicentric to aliform-confluent and in confluent wavy bands, and apotracheal parenchyma arranged in marginal bands (Ter Welle et al. 1986a; Cheng et al. 1992).

Comparison with fossil woods To date (Gregory et al. 2009; Franco 2010), six genera for fossil woods of the Mora- ceae have been erected: Myrianthoxylon Koeniguer, Ficoxylon Kräusel, Cudranioxy-

← C: TLS, alternate intervessel pits with lens-shaped apertures and coalesced pit apertures (arrow). – D: RLS, helical thickenings in vessel elements. – E: RLS, heterocellular rays, abundant tyloses (arrow) in vessel members. – F: RLS, vessel-parenchyma pits. – G: TLS, multiseriate rays. — Scale bars: 500 μm in A; 200 μm in B, F, G; 20 μm in C, D, E. 172 IAWA Journal 34 (2), 2013 lon Dupéron-Laudoueneix, Artocarpoxylon Mehrotra, Prakash & Bande, Moroxylon Selmeier, and Soroceaxylon Franco. One Miocene Mexican fossil wood was placed in the modern genus Maclura (Martinez-Cabrera & Cevallos-Ferriz 2006). Except

Figure 2. Wood of modern Maclura and Broussonetia. – A, B: Maclura tricuspidata Carrière (CAFw 8299); C, D: Maclura pubescens (Trécul) Zhou et Gilbert (CAFw 17124, Guangdong, China); E, F, G, H: Broussonetia papyrifera (L.) L’Hér. ex Vent. (CAFw 6656, Jiangsu, China). – A, C, E: TS, showing distinct growth rings, ring porous wood, vessel arrangement, and parenchyma. – B: TLS, long crystalliferous parenchyma strands. – D: RLS, homocellular rays. – F, G: TLS, multiseriate rays. – H: RLS, showing heterocellular rays. — Scale bars: 500 μm in A, C, E; 200 μm in F; 100 μm in D, G, H; 50 μm in B. Yin et al. – Moroxylon from China 173 for Maclura martinezii (Martinez-Cabrera & Cevallos-Ferriz 2006) and Moroxylon sturmii (Selmeier 1993), all other Moraceae fossil woods are diffuse porous and thus are distinct from the fossil described here. Maclura martinezii can be differentiated from the present fossil as it has chambered crystalliferous parenchyma strands containing up to 15 crystals and rays with 1–4 rows of marginal cells. Our fossil shows the greatest similarities with Moroxylon sturmii from the Neogene of Bavaria, which has distinct ring porous wood, narrow rays (1–3(–4) cells wide) and multiple rows of earlywood vessels. The fossils from China and Germany share many anatomical features, but the Chinese fossil differs from Moroxylon sturmii in having wider rays and 1(–2) row(s) of earlywood vessels with no tangential clusters in the latewood. Therefore, we consider our material to be anatomically distinct from the type species and erect the new species, Moroxylon xinhuaensis, with the specific epithet indicating its occurrence in Xinhua.

The phytogeographic history of Morus during the Tertiary Lobed fossil leaves from Europe, Asia, and North America have been called Morus (e.g., late Eocene Florissant flora of Colorado, United States, MacGinitie 1953; and late Miocene of the USSR, Takhtajan 1982). Additionally Brown (1962) called an unlobed leaf from the Paleocene of North America Morus (Brown 1962). These early reports need reevaluation. Other records include rare Morus-like or Broussonetia-like leaves (Manchester & Meyer 1987) from the Oligocene John Day Formation, United States (Collinson 1989). Morus fruits with identical morphology to modern mulberries are recorded from the early Eocene of southern England (Chandler 1963) and the former Czechoslovakia (Knobloch 1980), the Miocene of Germany (Gregor 1978), and the former USSR (Takhtajan 1982). In China, the Cenozoic record of Morus includes fossil leaves of Morus asymmetrica Li reported from the Miocene of Nanjing, Jiangsu Province (Li & Guo 1982; Li et al. 1987) and the Miocene of Ninghai, Shengxian Counties, Zhejiang Province (Li & Guo 1982; Guo & Zhou 1992; Liu et al. 1996). The finding of the new wood species from southwestern China shows that Morus was widely distributed in the Neogene of China. The occurrence of Cedreloxylon (Cheng et al. 2006), Pistacioxylon (Cheng et al. 2012), and this Moroxylon species, all from the Neogene of the Yuanmou Basin, indi- cates that Neogene European floras had some similarity with Neogene Chinese floras. This new fossil wood of Moroxylon provides additional data for understanding floral relationships between Europe and eastern Asia.

ACKNOWLEDGEMENTS

This research was supported by the National Natural Science Foundation of China (No. 31170206). We thank Prof. R.C. Mehrotra, Birbal Sahni Institute of Palaeobotany, India, for improvements to an earlier version.

REFERENCES

Brown RW. 1962. Paleocene flora of the Rocky Mountains and Great Plains. U.S. Geological Survey Professional Paper 375: 1–119. 174 IAWA Journal 34 (2), 2013

Chandler MEJ. 1963. The Lower Tertiary floras of Southern England. III. Flora of the Bourne- mouth Beds; the Boscombe, and the Highcliff Sands. British Museum (Natural History), London. Cheng JQ, Yang JJ & Liu P. 1992. Chinese woods. Chinese Forestry Publishing House, Beijing [in Chinese]. Cheng YM, Ferguson DK, Jiang XM, Li CS & Wang YF. 2006. Cedreloxylon cristalliferum, a new record of angiosperm woods from the Pliocene of Yunnan, China. IAWA J. 27: 145– 152. Cheng YM, Li CS, Jiang XM & Wang YF. 2007. A new species of Lagerstroemioxylon from the Pliocene of Yuanmou, Yunnan, China. Acta Phytotaxon. Sin. 45: 315–320. Cheng YM, Mehrotra RC, Jin YG, Yang W & Li CS. 2012. A new species of Pistacioxylon (Anacardiaceae) from the Miocene of Yunnan, China. IAWA J. 33: 197–204. Collinson ME. 1989. The fossil history of the Moraceae, Urticaceae (including Cecropiaceae), and Cannabaceae. In: Crane P & Blackmore S. (eds.), Evolution, Systematics, and Fossil History of the Hamamelidae. Vol. 2. Higher Hamamelidae. Systematics Association Special Volume 40B: 319–339. Clarendon Press, Oxford. Franco MJ. 2010. Soroceaxylon entrerriensis gen. et sp. nov. (Moraceae) de la Formación Ituzaingó (Plioceno-Pleistoceno), Cuenca del río Paraná, Argentina. Rev. Mexic. de Cienc. Geológ. 27: 508–519. Gregor HJ. 1978. The Miocene fruit and seed floras of the Oberpflaz Browncoal. I. Findings from the sandy interbeds. Palaeontographica B 167: 8–103 [In German]. Gregory M, Poole I & Wheeler EA. 2009. Fossil dicot wood names - an annotated list with full bibliography. IAWA J. Suppl. 6. 220 pp. Guo SX & Zhou ZK. 1992. The megafossil legumes from China. In: Herendeen PS & Dilcher DL (eds.), Advances in Legume Systematics: part 4. The Fossil record: 207–223. Royal Botanic Gardens, Kew. Hass H & Rowe NP. 1999. Thin sections and wafering. In: Jones TP & Rowe NP (eds.), Fossil plants and spores: modern techniques: 76–81. Geological Society, London. IAWA Committee. 1989. IAWA List of microscopic features for hardwood identification. IAWA Bull. n.s. 10: 219–332. InsideWood. 2004-onwards. Published on the Internet. http://insidewood.lib.ncsu.edu/search Knobloch E. 1980. Die jungtertiäre flora des slowakischen Teils des Orava-Beckens. Zapadne Karpaty, Ser. Paleontologia 5: 95–126. Koek-Noorman J, Topper SMC & Ter Welle BJH. 1984a. The systematic wood anatomy of Moraceae (Urticales. I. Tribe Castilleae. IAWA Bull. n.s. 5: 183–195. Koek-Noorman J, Topper SMC & Ter Welle BJH. 1984b. The systematic wood anatomy of Moraceae (Urticales). II. Tribe Dorstenieae. IAWA Bull. n.s. 5: 317–319. Koek-Noorman J, Topper SMC & Ter Welle BJH. 1984c. The systematic wood anatomy of Moraceae (Urticales). III. Tribe Ficeae. IAWA Bull. n.s. 5: 330–334. Li HM & Guo SX. 1982. Angiosperm. In: Nanjing Inst. Geol. Min. Res. (ed.), Paleontological Atlas of East China, Part 3, Volume of Mesozoic and Cenozoic: 294–316. Geological Pub- lishing House, Beijing. Li HM, Shao JJ & Huang JN. 1987. Some Neogene plant fossils from Nanjing area, Jiangsu. Acta Palaeont. Sin. 26: 563–575. Liu YS, Guo SX & Ferguson DK. 1996. Catalogue of Cenozoic megafossil plants in China. Palaeontographica Abt. B238: 141–179. MacGinitie HD. 1953. Fossil plants of the Florissant Beds, Colorado. Carnegie Institution of Washington Publications 599: 1–198. Yin et al. – Moroxylon from China 175

Manchester SR & Meyer HW. 1987. Oligocene fossil plants of the John Day Formation, Fossil, Oregon. Oregon Geology 49: 115–126. Martinez-Cabrera HI & Cevallos-Ferriz SRS. 2006. Maclura (Moraceae) wood from the Miocene of Baja California Peninsula, Mexico: Fossil and biogeographic history of its closer allies. Rev. Palaeobot. Palynol. 140: 113–122. Metcalfe CR & Chalk L. 1950. Anatomy of the dicotyledons. Clarendon Press, Oxford. Pan YR & Zong GF. 1991. Chapter 4: paleontology, section 1: Fossil mammal fauna. In: Qian F & Zhou GF (eds.), Quaternary Geology and Paleoanthropology of Yuanmou, Yunnan, China: 94–102 [in Chinese with English abstract]. Qian F & Zhou GX. 1991. Quaternary geology and palaeoanthropology of Yuanmou, Yunnan, China: 222. Science Press, Beijing [in Chinese with English abstract]. Selmeier A. 1993. Moroxylon nov. gen. (Moraceae), ein verkieseltes Maulbeerholz aus jungter- tiären Schichten Bayerns (Hallertau). Mitt. Bayer. Staatssammlg Paläont. Hist. Geol. 33: 209–226. Takhtajan A (ed.). 1982. Fossil flowering plants of the USSR, Vol. 2, Ulmaceae-Betulaceae. Nauka, Leningrad [in Russian]. Ter Welle BJH, Koek-Noorman J & Topper SMC. 1986a. The systematic wood anatomy of the Moraceae (Urticales). IV. Genera of the tribe Moreae with Urticaceous stamens. IAWA Bull. n.s. 7: 91–128. Ter Welle BJH, Koek-Noorman J & Topper SMC. 1986b. The systematic wood anatomy of the Moraceae (Urticales). V. Genera of the tribe Moreae without Urticaceous stamens. IAWA Bull. n.s. 7: 175–193. Tippo O. 1938. Comparative anatomy of the Moraceae and their presumed allies. Bot. Gazette 100: 1–99. Wheeler EA. 2011. InsideWood - a web resource for hardwood anatomy. IAWA J. 32: 199– 211. Zhang ZH, Liu PG, Qian F, Min LR, Wang Q & Zong GF. 1994. New development in research of Late Cenozoic stratigraphy in Yuanmou Basin. Marine Geol. & Quaternary Geol. 14: 1–18 [in Chinese with English abstract]. Zhou ZK & Gilbert MG. 2003. Moraceae. In: Wu ZY, Raven PH & Hong DY (eds.), Flora of China Vol. 5: 21–73. Missouri Botanical Garden Press, St. Louis, and Science Press, Beijing.

Accepted: 17 January 2013