Journal of Systematics JSE and Evolution doi: 10.1111/jse.12577 Research Article

Early Oligocene fruits and leaves of Burretiodendron (Malvaceae s.l.) from South China

Sheng‐Lan Xu1, Tatiana M. Kodrul2, Yan Wu1, Natalia P. Maslova3, and Jian‐Hua Jin1*

1State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat‐sen University, Guangzhou 510275, China 2Geological Institute, Russian Academy of Sciences, Moscow 119017, Russia 3Borissiak Paleontological Institute, Russian Academy of Sciences, Moscow 117997, Russia *Author for correspondence. E‐mail: [email protected]; Tel.: 86‐20‐84113348; Fax: 86‐20‐84036215. Received 23 September 2019; Accepted 18 February 2020; Article first published online 21 February 2020

Abstract The genus Burretiodendron Rehder is currently endemic to an area near the China–Vietnam border and the limestone mountains of Thailand and Myanmar. The fossil records of this genus were previously found only from the Miocene of Yunnan, Southwest China, and the Oligocene of Guangxi, South China. Here, we describe fossil fruits and associated leaves of Burretiodendron, which were discovered in the lower Oligocene Shangcun Formation of the Maoming Basin, Guangdong, South China. Morphological comparison with extant and fossil Burretiodendron taxa indicates that fruit fossils belong to the species Burretiodendron parvifructum J. Lebreton Anberrée & Z. K. Zhou. This is one of the earliest fossil records of the genus, providing additional evidence for the early biogeographic history of this genus and supporting the inference that the genus originated in South China. According to the habitat conditions of modern species, we speculate that there were limestone mountains around the Maoming Basin in the early Oligocene. Key words: Burretiodendron, early Oligocene, limestone mountains, mericarp, South China.

1 Introduction Burretiodendron hsienmu Chun & How and Burretiodendron obconicum Chun & How (Chun & How, 1956) into this genus. Burretiodendron Rehder, placed in Malvaceae, subfamily Excentrodendron was segregated from Burretiodendron based Dombeyoideae Beilschmied (Won, 2009), is a genus endemic on absence of a persistent ovary stalk and several foliar to Asia, mainly distributed in the limestone mountain rain morphological characters (an evergreen habit, palmate forest and deciduous forest between 300 and 500 m a.s.l. primary venation with three basal veins, and the presence of near the China–Vietnam border (Zhuge, 1990). The type glands in vein axils). The separation of the two genera is also species of this genus, Burretiodendron esquirolii (H. Lév.) supported by differences in pollen morphology (Tang & Rehder, is ranked as a category II state protection wild plant Gao, 1993), wood anatomy (Tang et al., 2005b), and molecular in China (Fu, 1991). Unfortunately, due to the impact of data (Li et al., 2004). However, this taxonomic assignment habitat reduction and overexploitation, the present distribu- has not been widely accepted (Zhuge, 1990; Wu, 1991; tion area of Burretiodendron has been gradually reduced, and Brummitt, 1992; APG, 2003; Bayer & Kubitzki, 2003). The it is difficult to find any natural forest where Burretiodendron characteristics of bisexual flowers and deciduous habit were is dominant (Tang et al., 2005a). observed in most species of both Burretiodendron and Burretiodendron was described by Rehder (1936) and Excentrodendron after Zhuge (1990) checked all accessible originally placed in Tiliaceae. With the development of the specimens. We retain the type species of Excentrodendron, Angiosperm Phylogeny Group (APG) system, Tiliaceae was E. hsienmu (Chun&How)Chang&Miau(1978)asaspeciesof incorporated into the expanded Malvaceae, and the former Burretiodendron,thatis,B. hsienmu Chun & How (1956), and family was redefined as the subfamily Tilioideae Arn consider the fossils treated here as members of Burretioden- (APG, 2003). As the morphological characteristics of the dron in this broader circumscription. genus are similar to certain genera within the Malvaceae (e.g., There are six living species of Burretiodendron, four of Craigia W. W. Smith & W. E. Evans, Berrya Roxburgh, and which occur in China. Burretiodendron esquirolii occurs in Colona Cavanilles), the systematic position of Burretiodendron Southwest China, parts of Thailand and Vietnam, growing has long been debated (Chang & Miau, 1978; Zhuge, 1990; in canyon slopes and river banks. The main soil types in Li et al., 2004; Tang et al., 2005a, 2005b, 2006; Gao, 2006; Gao the distribution area are limestone soil and lateritic soil et al., 2006). Chang & Miau (1978) established the new genus (Wu, 1995). Burretiodendron kydiifolium Y. C. Hsu & R. Zhuge Excentrodendron Chang & Miau and transferred two species is mainly found in Yunnan Province and is endemic to the

Month 2020 | Volume 00 | Issue 00 | 1–11 © 2020 Institute of Botany, Chinese Academy of Sciences 2 Xu et al. dry and hot valley of the Yuanjiang river (Hsu & Zhuge, 1990). Museum of Biology, Sun Yat‐sen University. Preparation of the Burretiodendron hsienmu grows in Guangxi and Yunnan cuticle of the fossil specimens was achieved using Schulze's provinces and is an important representative of north solution treatment method of Ye (1981). Fragments of fossils tropical karst seasonal rain forest vegetation (Chang & were treated with 10% HCl for 12 h to remove carbonate material, Miau, 1978). It grows well in hills of pure limestone, often then the isolated fragments were treated with Schulze's solution on steep slopes, on bare rock or shale (Wang et al., 1986). (HNO3 [68%] and KClO3 [saturated] with volume ratio of 3:1) for Burretiodendron obconicum is only found in Guangxi approximately 1 h. The reaction was terminated by immersion in Province, growing in evergreen forests on limestone (Tang 10% KOH for 5–10 min. The upper and lower cuticles were et al., 2007). The other two species are Burretiodendron separated by needles using a stereomicroscope Leica S8 APO brilletii Kosterm. from northern Vietnam and Burretiodendron (Leica, Wetzlar, Germany) and studied using a transmitted light siamense Kosterm. common in deciduous forest from microscope (LM) Carl Zeiss Axioscope A1. For scanning electron Thailand and Myanmar (Kostermans, 1961; Zhuge, 1990). microscopy (SEM), cuticles were dehydrated for 10 min each in There is a very limited fossil record of the genus an alcohol series, mounted on standard copper plates, coated Burretiodendron (Fig. 1A). Fruit fossils include Burretiodendron with gold, studied, and photographed using a JSM‐6330F SEM parvifructum J. Lebreton Anberrée & Z. K. Zhou from the upper (JSM, Tokyo, Japan). Miocene Xiaolongtan Formation, Yunnan, Southwest China The morphology of modern Burretiodendron fruits and (Lebreton Anberrée et al., 2015), and Burretiodendron guang- leaves was examined at the Herbarium of South China xiense J. L. Dong & B. N. Sun (the specificepithetguangxiensis Botanical Garden (IBSC) and the Herbarium of Sun Yat‐sen corrected to guangxiense according to the gender of the generic University (SYS). The length (L) and width (W) of each name) from the Oligocene in Ningming County, Guangxi, South specimen were measured, and the ratio range of L/W was China (Dong et al., 2018). Leaf fossils include Burretiodendron used to represent the shape differences. The cuticle of the miocenicum J. Lebreton Anberrée & Z. K. Zhou from the upper modern species was prepared by treating the specimens Miocene of Yunnan (Lebreton Anberrée et al., 2015). with a solution of acetic acid and H2O2 (30%) with volume In this paper, fruit and leaf fossils of Burretiodendron ratio of 1:1 at 75 °C for 2 h. Needles were used to separate from the lower Oligocene Shangcun Formation in the cuticles. The cuticles were dyed with 1% safranin and Maoming Basin, South China, are described and compared examined using the Carl Zeiss Axioscope A1 light microscope with related extant species. This fossil record provides new and the JSM‐6330F SEM. Terminology for the description of important material for the investigation of the possible leaf morphology follows Dilcher (1974) and Ellis et al. (2009), origin center, paleogeography, and paleoecology of the and terminology for the fruit description follows Manchester genus. and O'Leary (2010).

2 Material and Methods 3 Systematics 2.1 Geological setting 3.1 Fruits The fossil specimens studied here were collected from Family: Malvaceae Jussieu s.l. the Shangcun Formation in the Maoming Basin, Guangdong Genus: Burretiodendron Rehder, 1936 Province, South China (Fig. 1B). Compressions/impressions Species: Burretiodendron parvifructum J. Lebreton of nine fruits and four leaves of Burretiodendron were Anberrée&Z.K.Zhou ′ ′ found at the Lishan opencast coal mine (21°52 N, 110°40 E). Specimens: MMLS‐083, MMLS‐186, MMLS‐312a, MMLS‐312b, The upper part of the Shangcun Formation mostly consists MMLS‐313a, MMLS‐313b, MMLS‐334a, MMLS‐334b, MM3A‐199, ‐ ‐ of grayish brown and greenish gray compact mudstones MM3A‐212a, MM3A‐212b, MM3A‐271, MM3A‐553a, MM3A‐553b. and sandy shales, and the lower part is composed of Locality: Maoming Basin, Guangdong Province, South siltstones with oil shales and coal seams (Nan & Zhou, 1996). China. Plant fossils are preserved separately in grayish brown to Geological horizon: Shangcun Formation, lower Oligocene. light brown mudstones and siltstones of the upper part of Repository: The Museum of Biology of Sun Yat‐sen the Shangcun Formation representing a large lacustrine University, Guangzhou, China. environment. The low density and distribution of the fossils Description:Eachtwo‐winged mericarp is elliptic suggest that deposition was distant from the shoreline (Figs. 2B, 2C, 2F) to obovate (Figs. 2A, 2E, 2J) in outline, ca. ‐ (Spicer et al., 2017). Plant bearing deposits have been dated 20.0–32.5 mm long, 10.5–23.0 mm wide, L/W ratio 1.4–2.0. to the early Oligocene based on a palynological study The apex is rounded (Figs. 2A, 2D, 2J, 2K) to slightly retuse (Herman et al., 2017). All specimens and slides are housed at (Figs. 2B, 2F, 2G), the base is rounded to acuminate ‐ the Museum of Biology of Sun Yat sen University, (Figs. 2B, 2F, 2G, 2J). The endocarp is placed at the center Guangzhou, China. of the mericarp, 6.4–12.1 mm long, 5.0–8.0 mm wide, L/W ratio 1.3–1.6. The endocarp is obovate with an acute 2.2 Specimen preparation base (Figs. 2A, 2E, 2G), and a rounded apex in the abaxial Plant fossils were photographed using a Canon EOS 500D view (Figs. 2A, 2E, 2J) but retuse apex in the adaxial view (Canon, Tokyo, Japan) digital camera. Macrophotography of the (Figs. 2B, 2G, 2H); septum is visible in the locule area venation of fruit wings and leaves was undertaken using a Zeiss (Figs. 2B, 2G, 2H). The ratio of fruit length to endocarp Stereo Discovery V20 microscope (Zeiss, Baden‐Wurttemberg, length is 2.4–3.3, and fruit width to endocarp width is Germany) equipped with Achromat S 0.3× objective lenses in the 1.7–2.6. Straight strong primary vein extends from the fruit

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Fig. 1. Geographic distribution of Burretiodendron and sketch map of the fossil locality. A, Map showing the distribution of fossil and extant Burretiodendron. The data is modified after the Global Biodiversity Information Facility website (https://www. gbif.org/occurrence/map?taxon_key=7311012). B, Sketch map indicating the location of the Maoming Basin, Guangdong, South China. Base map of China adapted from d‐maps (https://d‐maps.com/index.php?lang=zh). base to the locule area; wing venation extending from the irregularly arranged, 23.0–72.0 μmlongand12.5–32.0 μm endocarp to the wing edges (Figs. 2B, 2C, 2E, 2F) is wide, with an average length of 43.01 μm and an average craspedodromous but not forming elongated areoles width of 22.8 μm(Fig.3D). Sparse trichome bases on the (Fig. 2I). The mericarp surface shows elongated and mericarp surface are surrounded by five radially arranged isodiametric cells, mostly pentagonal and quadrangular, cells (Figs. 3E, 3F). Endocarp tissue is composed of www.jse.ac.cn J. Syst. Evol. 00 (0): 1–11, 2020 4 Xu et al.

Fig. 2. Fossil fruits of Burretiodendron parvifructum J. Lebreton Anberrée & Z. K. Zhou (A–K) and extant species B. hsienmu (L, M). A, MMLS‐083 showing the obovate endocarp. B, F, MMLS‐313a, MMLS‐313b, part and counterpart, elliptic mericarp showing slightly retuse apex and cuneate base, position of straight primary vein (arrowhead). C, MMLS‐312a. D, MMLS‐186. E, Abaxial view of the mericarp. MM3A‐271. G, MM3A‐199 showing the septum in the locule area. Adaxial view. H, Enlargement of the endocarp in B showing heart‐shaped outline of endocarp, septum in the locule area (arrowhead). I, Enlargement of the wing in (C) showing wing venation. J, MMLS‐334b, large mericarp with rounded apex. K, MMLS‐334a, Counterpart of the mericarp in J. L, Inner view of the mericarp of B. hsienmu. M, Whole schizocarp of B. hsienmu. Scale bar = 5mm(A–G, K–M), 1mm(H, I).

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Fig. 3. Mericarp micromorphology, fungal hyphae, and fruiting bodies of Burretiodendron parvifructum (A–I), wing micromorphology of extant species B. hsienmu (J–L). A, Generally pentagonal isodiametric and elongated endocarp cells. Light microscope (LM), MMLS‐083. B, Enlargement of endocarp cells in (A). Note prominently pitted cell walls. C, Endocarp cells. Scanning electron microscope (SEM), MM3A‐553a. D, Elongated and isodiametric cells of mericarp surface. SEM, MM3A‐ 553a. E, F, Trichome bases on the mericarp surface. SEM, MM3A‐553a and MM3A‐199, respectively. G, Branching septate fungal hyphae. LM, MM3A‐199. H, Endophytic fungal fruiting bodies. LM, MM3A‐199. I, Single fungal fruiting body showing polygonal cell wall. LM, MM3A‐199. J, Abaxial view of the wing cuticle showing several stomatal complexes (red arrowhead) and trichomes (blue arrowheads); trichome bases are surrounded by five to eight radial cells. LM. K, Abaxial view of the wing cuticle showing stoma and trichomes. SEM. L, Enlargement of the anomocytic stoma. SEM. Scale bar = 50 μm(A, H, J, K), 20 μm(B, G, I), 10 μm(C–F, L). isodiametric and elongated cells, generally pentagonal, In the internal tissues of these fruits, abundant endophytic 17.4–27.5 μmlongand10.6–18.2 μm wide, with straight pycnidia or perithecium‐like ostiolate fruiting bodies lateral walls having prominent pits between adjacent cells (Figs. 3H, 3I) and branching septate hyphae (Fig. 3G) were (Figs. 3A–3C). found. The fungal fruiting bodies are solitary, rounded, and www.jse.ac.cn J. Syst. Evol. 00 (0): 1–11, 2020 6 Xu et al. approximately 200–230 µm in diameter. The fruiting body because we have isolated mericarps rather than the wall consists of polygonal cells approximately 5–15 µm in complete schizocarpic fruit. Details of the pedicel, placenta- diameter (Fig. 3I). As the classification of the fungi is tion, and three‐dimensionally preserved seeds are also mainly based on special morphology and reproduction absent in our material. type, isolated fossil fruiting bodies and mycelium are poor The fruit types of Malvaceae are mainly capsule and evidence for their systematic identification. Most of the schizocarp, sometimes berrylike (Malvaviscus). Winged fruits endophytes from woody plants belong to the ascomycetes appear only in certain genera of the family, like Ambroma L., of diverse phylogenetic origin (Schueffler & Anke, 2011). Kleinhovia L., Berrya, Colona, Craigia, Hainania Merrill, Pentace Merrill, and Burretiodendron. The five‐winged capsule in 3.2 Leaves Ambroma is obconic, cuplike after dehiscence, and has villous margins. The truncate apex in Ambroma and Hainania Family: Malvaceae Jussieu s.l. ff Genus: Burretiodendron Rehder, 1936 (H. trichosperma Merr.) di ers from the rounded apex Species: Burretiodendron sp. in our fossil. Kleinhovia varies from Burretiodendron in Specimens: MMB‐283, MMB‐335, MMB‐399a, MMB‐399b, terms of wing venation; the main veins being reticulate, MMLS‐123a, MMLS‐123b. forming areoles in Kleinhovia and craspedodromous in Locality: Maoming Basin, Guangdong Province, South Burretiodendron. Berrya capsules have a persistent calyx, with six (or eight) horizontally spreading thin wings. The China. ff Geological horizon: Shangcun Formation, lower Oligocene. seeds are located under the wings, which is very di erent ‐ from centrally placed endocarp in our fossils. The fruits of Repository: The Museum of Biology of Sun Yat sen – ‐ University, Guangzhou, China. Colona are indehiscent, rather rounded in outline, 5 2 winged, or dehiscent separating into two to five 1–4‐ Description: Leaves are simple, unlobed, elliptic to ovate, ff fi ‐ with untoothed slightly sinuous margin (Figs. 4A–4F). All seeded mericarps, which is di erent from ve 1 seeded leaves are incompletely preserved, apices and bases of mericarps in Burretiodendron (Bayer & Kubitzki, 2003). In laminae are missing but a cordate base can be reconstructed addition, the fruit outline of Colona has the characteristic of for some leaves. Laminar maximum incomplete length is apex concave. Pentace and Burretiodendron have the same 11.4 cm, width is 8.0 cm. Primary venation is palmate with wing venation characteristics, but the shape and position of fi the endocarp are obviously different. three basal veins (Fig. 4E). Four to ve pairs of simple ‐ fi agrophic veins are present. Major secondary veins are Craigia has 5 winged capsules super cially resembling the brochidodromous and do not reach the margin; intersecon- fruits of Burretiodendron in outline shape and position of the dary veins are absent. Intercostal tertiary veins are endocarp, which has led to confusion (Smith & Evans, 1921). percurrent with opposite, sinuous to straight course, Our fossil is readily distinguished from Craigia by its occasionally alternate. Quaternary veins are irregular retic- distinctive endocarp shape, which is obovate rather than ulate, areoles are well developed, freely ending veinlets are oblong fusiform to elliptical. Craigia fruits have a fusiform endocarp enclosing 1, 2, or 4 seeds per locule (Bůžek absent (Figs. 4H, 4I). č Leaves are hypostomatic, adaxial epidermis is composed et al., 1989; Kva ek et al., 1991), whereas Burretiodendron has of rectangular or pentagonal ordinary cells, 5.7–16.2 µm only a single seed per cell (Tang et al., 2007). Also, the wing long (Fig. 5A), abaxial epidermis shows irregularly distrib- venation in the fossil species Craigia hainanensis J. H. Jin & uted, randomly oriented stomata and trichome bases T. M. Kodrul is sparser in comparison to our winged fruit surrounded by four to seven radially arranged epidermal (Jin et al., 2009). The species Burretiodendron yunnanense – Kosterm. (Kostermans, 1961) was transferred to Craigia cells (Figs. 5B 5E). Cells of the costal zone are rectangular - to elongated, 6.7–19.7 µm long, 9.3–17.4 µm wide, typically yunnanensis Smith & Evans (Chang & Miau, 1978). Burretio arranged in longitudinal files, with oblique and straight dendron combretoides Chun & How, founded by Chun & How anticlinal cell walls (Figs. 5C, 5F). (1956), was also transferred to Craigia (Yuan et al., 2002). Burretiodendron fruits are elliptical, developed from a sessile or stipitate ovary, and have five wings. The fruit breaks septicidally into 1‐seeded mericarps (Zhuge, 1990). 4 Discussion The main veins of each mericarp fan outward into the 4.1 Generic assignment and comparisons wings from the elliptical central body, and are straight to Winged fruits can be identified from many characters somewhat sinuous in course, occasionally dichotomizing including size, number of wings, patterns of wing venation, and anastomosing (Manchester & O'Leary, 2010). These are wing shape and position, persistence of style(s) and pedicel, completely consistent with the fossil features. Therefore, placentation type, seed number, and orientation, positions we can assign our fossil to the genus Burretiodendron. of the micropyle and raphe, and epidermal anatomy (Manchester & O'Leary, 2010). Our fossils are characterized 4.2 Comparison with fruits of extant and fossil species by elliptic to obovate mericarps with two wings, which are of Burretiodendron laterally aligned with the longitudinal axis, with a centrally Fruit fossils from the Maoming Basin are similar to the fruits placed obovate endocarp and craspedodromous wing of extant species in having an obovate shape and acuminate venation. These features are those of the Malvaceae base (Figs. 2L, 2M). The fossil mericarp L/W ratios are closer to (Lebreton Anberrée et al., 2015). We compared genera that that of extant species B. hsienmu and B. kydiifolium, had similar wing fruit characteristics to those of the fossils. but these extant species are readily distinguishable by the The number of wings is not a definitive feature for our fossils endocarp L/W ratio and the fruit size. Our fossils have a lower

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Fig. 4. Macromorphology of Burretiodendron sp. (A–F, H, I) and extant B. hsienmu (G, J) leaves. A, Unlobed leaf with untoothed slightly sinuous margin. MMB‐335. B, C, Leaf fragment, part, and counterpart. MMB‐399a and MMB‐399b, respectively. D, Agrophic veins. MMB‐283. E, F, Leaf fragment showing basal primary vein (arrowhead) and brochidodromous secondary venation, part, and counterpart. MMLS‐123a and MMLS‐123b, respectively. G, Extant B. hsienmu whole leaf. H, Enlargements of the leaf in F showing irregular reticulate quaternary vein fabric. MMLS‐123b. I, Enlargement of leaf in C showing areoles without freely ending veinlets. MMB‐399b. J, Leaf of B. hsienmu showing intercostal percurrent tertiary veins and irregular reticulate quaternary vein fabric. Scale bar = 10 mm (A–G), 5 mm (H), 1 mm (I, J). endocarp L/W ratio and a smaller fruit size than in extant trichomes are scattered over the abaxial surfaces of modern species (Table 1). Surface cells of fossil mericarps are generally mericarps (Figs. 3J–3L). The cells of the endocarp tissue in B. elongated pentagonal and quadrangular, the average cell size hsienmu (Dong et al., 2018; fig. 7L) are similar in size, shape, is 43.01 × 22.8 μm; sparse trichome bases are surrounded by and prominent pits of cell anticlinal walls to those of fossils five radially arranged cells. Burretiodendron hsienmu closely from the Maoming Basin. resembles fossil species in the shape and size of mericarp There are two species of fossil fruits sharing similarities epidermal cells, which are 22.4 to 73.7 μm long and 15.0 to with our wing fruits: B. parvifructum from Yunnan and 34.2 μm wide (the average cell size is 41.8 × 21.8 μm). B. guangxiense from Guangxi. Burretiodendron parvifructum However, abundant anomocytic stomata and glandular and associated leaves of B. miocenicum were documented www.jse.ac.cn J. Syst. Evol. 00 (0): 1–11, 2020 8 Xu et al.

Fig. 5. Leaf micromorphology of Burretiodendron sp. (A–F, MMB‐399b) and B. hsienmu (G–I). A, Epidermal cells of the adaxial leaf surface. Light microscope (LM). B, Abaxial epidermis showing several trichome bases (arrowheads). LM. C, Trichome base (arrowheads) on vein junction and elongated vein cells. LM. D, Trichome base and stomata on the abaxial leaf surface, inner view. Scanning electron microscope (SEM). E, Stomatal complexes on the abaxial leaf surface, inner view. SEM. F, Vein epidermal cells. SEM. G, Glandular trichome base on the abaxial leaf surface, inner view. SEM. H, Two types of glandular trichomes on the leaf veins, abaxial surface, outer view. SEM. I, Stomata and trichome bases on the abaxial leaf surface, inner view. SEM. Scale bar = 50 μm(B), 20 μm(A, C, F, H, I), 10 μm(D, E, G). from the upper Miocene of the Wenshan and Maguan are markedly tapering downward from the middle part of localities in southeast Yunnan, China (Lebreton Anberrée the fruit to the base. However, the micromorphological et al., 2015). According to a principal component analysis characteristics (cell size and shape, prominently pitted cell with nine measurements of Burretiodendron mericarp and walls) of the B. guangxiense endocarp (Dong et al., 2018; endocarp carried out by Lebreton Anberrée et al. (2015), the Figs. 5D–5F, 5J–5L) are very similar to those of fruit fossils most important traits to distinguish B. parvifructum are the from the Maoming Basin. endocarp L/W ratio and the endocarp width. The endocarp L/W ratio in our fossil is 1.3–1.6, which is in the range of 4.3 Comparison with leaves of extant and fossil species 1.0–1.9 from B. parvifructum, and the width range of the of Burretiodendron endocarp of our fossil (5.0–8.0 mm) is also similar to that Leaves are preserved incompletely, but they exhibit a distinct of B. parvifructum (3.6–6.2 mm). Hence, fossil fruits from venation pattern. Leaf margin characters and the leaf shape the Maoming Basin can be assigned to the species can be easily reconstructed. Palmate leaf venation, untoothed B. parvifructum. margin, and trichomes are common features of Malvaceae The other fossil species, B. guangxiense from the Oligocene (Bayer & Kubitzki, 2003). Fossil leaves from the Maoming Ningming Formation, Guangxi, South China, has a fruit/ Basin are similar to those of some extant Burretiodendron endocarp ratio similar to our fossils, but fruit and endocarp species in terms of shape, venation, and epidermal characters. size is much smaller than that of B. parvifructum. The fruit Both fossil and extant leaves possess reticulate quaternary outline is also different; our fossil fruits appeared narrower venation with well developed areoles and absence of freely in width near the base, whereas the fruits of B. guangxiense ending veinlets in areoles.

J. Syst. Evol. 00 (0): 1–11, 2020 www.jse.ac.cn Early Oligocene fruits and leaves of Burretiodendron 9 3.2 3.6 2.8 1.9 3.4 3.4 2.6 5.9 Fossil leaves assigned to Burretiodendron sp. and those of – – – – – – – – extant B. hsienmu are hypostomatic, abaxial epidermis shows irregularly scattered, randomly oriented anomocytic stomata (Figs. 5D, 5E, 5I), and numerous trichomes distributed on 3.1 2.0 2.7 2.4 3.3 1.7 4.9 2.5 3.9 2.5 3.0 3.0 2.4 1.6 4.2 2.1 – – – – – – – – the veins (Figs. 5C, 5H). Trichome bases are surrounded by radial epidermal cells, four to seven in Burretiodendron sp. versus five to eight in B. hsienmu (Figs. 5B–5D, 5G, 5I). 2.2 2.2 1.7 4.0 1.71.9 2.3 2.1 1.6 2.4 1.8 2.6 3.0 2.1 2.6 2.4 – – – – – – – – Hence, the micromorphological characters further corrobo- rate the assignment of the fossil leaves to the genus Burretiodendron. Identification of leaf fossils at the species 5.2 2.5 6.2 1.0 6.7 1.7 6.9 2.0 7.6 2.2 5.0 1.6 8.0 1.3 4.6 1.2 level is limited due to poor preservation. – – – – – – – – Theonlypreviouslyconfirmed leaf fossil record of the genus is B. miocenicum from Yunnan, China (Lebreton Anberrée et al., 2015). The leaves of Burretiodendron sp. are larger in 17.7 6.7 13.5 4.0 6.5 3.0 8.3 4.5 12.1 5.0 8.5 3.6 11.3 5.6 14.9 6.0 – – – – – – – – length and width than those of B. miocenicum. The epidermal

12.0 cells over the veins of both leaf fossils are rectangular, often elongated arranged in longitudinal files, with straight cell walls; the length of cells is 17.7–43.3 µm in B. miocenicum and 6.7–19.7 µm in Burretiodendron sp. (Figs. 5B, 5C, 5F).

elliptic There is another potential occurrence of Burretiodendron fossil leaves based on a fragment of a leaf from the middle Miocene of the western shore of Khanka Lake near 3.1 Obovate to 1.7 Obovate 11.8 2.5 Obovate 7.9 2.4 Obovate 16.7 1.9 Obovate 5.7 2.0 Obovate 9.8 2.0 Obovate 6.4 2.0 Obovate 4.4 – – – – – – – – Novokachalinsk Village (Primory'e, Russia) that Pavlyutkin (2007) attributed to Excentrodendron.However,itisdifficult to

based on fruit characters verify this identification without the associated diagnostic fruits. 23 1.4 21.5 2.0 21.4 1.6 19.3 1.8 15.2 2.4 23.4 2.5 10.7 1.5 – 10.6 1.4 – – – – – – – 4.4 Paleogeographic and paleoecological implications Previously published Burretiodendron fossil occurrences in South China and Southwest China, the border area between 45.1 18.8 49.9 11.0 38.0 16.9 18.8 8.4 38.9 12.9 18.2 6.6 35.8 20.7 China and Vietnam, span from the Oligocene to Miocene. The 32.5 10.5 – – – – – – – – Fruit outline Endocarp Fruit/endocarp Burretiodendron

20 fruit species B. guangxiense has been found from the 14.3 42.5 33.4 30.5 29.0 Oligocene of Ningming Basin of Guangxi, South China. The age inference is based on lithostratigraphy and palynostrati- graphic studies (Dong et al., 2018). Fossil fruits B. parvifructum and leaves B. miocenicum were collected from

obovate obovate obovate elliptic elliptic elliptic the Xiaolongtan Formation of Yunnan, Southwest China, which is dated to the late Miocene by regional stratigraphic correlation, palynology, and vertebrate fossils (Lebreton Anberrée et al., 2015). Burretiodendron parvifructum de-

Extant Elliptic to Extant Obovate 34.1 scribed in this paper was dated to the early Oligocene, revealing that Burretiodendron might have originated in South China by the early Oligocene. Our fossils were found outside the modern distribution area, suggesting that the genus formerly had a wider distribution. Burretiodendron currently is only distributed in Southwest China, South China, northern Vietnam, southern Thailand, and Myanmar. Modern Burretiodendron species have strict survival Dong et al. (2018); §Lebreton Anberrée et al. (2015). EL, endocarp length; EW, endocarp width; FL, fruit length; FW, fruit width; L, length; W, width.

‡ climate requirements. Generally, this genus inhabits regions with an average annual temperature of 15–27.5 °C and an Vietnam Southwest China – Guangdong, South ChinaGuangxi, South ChinaYunnan, Southwest China Oligocene EllipticSouthwest to China, Thailand, Miocene OligoceneGuangxi, South China; Yunnan, Obovate Elliptic to Guangxi, South ChinaThailand 11.8 and MyanmarYunnan, Southwest China Extant Extant Obovate to Extant Obovate to Obovateannual to precipitation of 886 2067 mm. Extant Burretiodendron

‡ species are strictly tropical trees and are mostly confined § to limestone substrate (Lebreton Anberrée et al., 2015).

§ Burretiodendron primarily grows in mountain rain forests and † § dry deciduous forests, most commonly between 300 and § 550 m a.s.l. (Wang et al., 1986; Zhuge, 1990). § Li et al. (2006) studied the Maoming Basin sedimentary J. Lebreton Anberrée § J. L. Dong & B. N. Sun Y. C. Hsu & R. Zhuge

Chun & How characteristics and distribution regularity of oil shale, and Kosterm. (H. Lév.) Rehder Chun & How

Comparison of fossils from Maoming Basin with extant and fossil species of speculated on the possible development in the Maoming Basin of a swampy and lacustrine sedimentary environment

& Z. K. Zhou during the early Oligocene. The CLAMP technique AS (pers. obs., unpublished data, 2018); B. kydiifolium Table 1 † B. obconicum B. parvifructum B. esquirolii SpeciesFossils from Maoming Basin Occurrence Age Shape L (mm) W (mm) L/W Shape L (mm) W (mm) L/W FL/EL FW/EW B. hsienmu B. guangxiense B. siamense (Climate Leaf Analysis Multivariate Program) with 46 leaf www.jse.ac.cn J. Syst. Evol. 00 (0): 1–11, 2020 10 Xu et al. morphotypes from the Shangcun flora indicate a humid Bayer C, Kubitzki K. 2003. Malvaceae. In: Kubitzki K, Bayer C eds. subtropical climate with hot summers and warm winters The families and genera of vascular plants. Berlin: Springer‐Verlag. – (Herman et al., 2017). These climatic conditions are consistent 5: 225 311. with those under which Burretiodendron survives today. Brummitt RK. 1992. Vascular plant families and genera. Kew: Royal Moreover, the Maoming Basin is surrounded by the Botanic Gardens. Cambrian and Devonian sedimentary strata consisting of Bureau of Geology and Mineral Resources of Guangdong Province. limestones, carbonaceous shales, and dolomites interbedded 1988. Regional geology of Guangdong Province. Beijing: Geological with sandstones and siliceous rocks (Bureau of Geology Publishing House. (in Chinese with English abstract) and Mineral Resources of Guangdong Province, 1988). Bůžek C, Kvaček Z, Manchester SR. 1989. Sapindaceous affinities of Modern Burretiodendron species usually grow in red the Pteleaecarpum fruits from the Tertiary of Eurasia and North calcareous soil and laterite soil (Zhuge, 1990). Therefore, America. Botanical Gazette 150: 477–489. the discovery of our fossil from Shangcun Formation is Chang HT, Miau RH. 1978. The taxonomy of Excentrodendroideae consistent with the presence of limestone mountains around Tiliaceae. Acta Scientiarum Naturalium Universitatis Sunyatseni the Maoming Basin. 3: 19–26. Chun WY, How FC. 1956. 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