Available online at www.sciencedirect.com ScienceDirect Palaeoworld 29 (2020) 752–760 Fossil involucres of Ostrya (Betulaceae) from the early Oligocene of Yunnan and their biogeographic implications a,b a a,b a Teng-Xiang Wang , Jian Huang , Wen-Na Ding , Cédric Del Rio , a,∗ a,c,∗ Tao Su , Zhe-Kun Zhou a CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan 666303, China b University of Chinese Academy of Sciences, Beijing 100049, China c Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, China Received 2 July 2019; received in revised form 28 October 2019; accepted 27 November 2019 Available online 3 December 2019 Abstract A new fossil occurrence of Ostrya (Betulaceae) is reported based on 14 involucre impressions from the lower Oligocene of Löhe Basin, Yunnan Province, Southwest China. They are characterized by their bladder-like shape with longitudinal veins and perpendicular or branched intercostal veins that form a reticulate venation. The discovery of these fossil involucres represents the earliest unequivocal fossil record of Ostrya in East Asia and the record at the lowest latitude. Its fossil history suggests that the modern distribution pattern of Ostrya might have been established since the early Oligocene, and that this genus has inhabited low altitude areas since then. © 2019 Elsevier Ireland Ltd Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. Published by Elsevier B.V. All rights reserved. Keywords: Ostrya; Fruit; Involucre; Early Oligocene; Yunnan; Betulaceae 1. Introduction be a morphologically well-defined genus because all the Ostrya species are characterized by their fruit involucre that is bladder- The genus Ostrya Scopoli of the family Betulaceae, com- like with reticulate venation, enclosing a single nutlet. This monly known as hop-hornbeam, consists of 8 extant species involucre shape is distinctive from its neighboring genera, e.g., distributed mainly in the Northern Hemisphere, with one species Carpinus (Chen, 1994; Furlow, 1997; Li and Skvortsov, 1999). in Europe (Ostrya carpinifolia Scopoli), three in North Amer- Therefore, taking into account the phylogenetic uncertainty of ica (O. virginiana (Miller) Koch, O. knowltonii Coville, O. the molecular investigations and the stable morphological cir- chisosensis Correll), and four in East Asia (O. japonica Sar- cumscription of the genus, we consider Ostrya as monophyletic gent, O. rehderiana Chun, O. chinensis Turner (=O. multinervis in this study. Rehder), O. trichocarpa Fang and Wang). Among the East Asian Fossil species of Ostrya are established based mostly on species, the latter three are endemic to China. Recent phyloge- leaves and involucres, a few on nutlet and wood (Supplementary netic analysis on Betulaceae has left the monophyly of Ostrya Table 1), among which the involucre is the most characteris- unsolved because of the conflict between ITS-based phyloge- tic and convincing organ to be recognized. Leaf morphology of netic trees and plastome-based ones, probably due to complex Ostrya overlaps that of Carpinus (Meyer and Manchester, 1997; evolutionary history (Grimm and Renner, 2013; Xiang et al., Hably et al., 2000), and nutlets and woods are less commonly 2014; Yang et al., 2019). However, Ostrya has been considered to reported. Ostrya fossil involucre records have been reported from the Oligocene to Miocene of the Northern Hemisphere (Table 1; reports of other organs presented in Supplementary ∗ Table 1). The earliest fossil records occur almost simultane- Corresponding authors at: CAS Key Laboratory of Tropical Forest Ecol- ously in the early Oligocene of central Europe and western North ogy, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan 666303, China. America, namely O. atlantidis Unger and O. oregoniana Chaney, E-mail addresses: [email protected] (T. Su), [email protected] respectively (Table 1) (Meyer and Manchester, 1997; Kvacekˇ (Z.K. Zhou). https://doi.org/10.1016/j.palwor.2019.11.004 1871-174X/© 2019 Elsevier Ireland Ltd Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. Published by Elsevier B.V. All rights reserved. T.X. Wang et al. / Palaeoworld 29 (2020) 752–760 753 Table 1 Fossil records of Ostrya fruits with their ages and localities. Species Age Locality Reference Ostrya sp. Early Oligocene Lühe Basin, Yunnan Province, Southwest China This study O. atlantidis Early Oligocene Kundratice and Bechlejovice, Czech Republic Engelhardt (1885), Kvacekˇ and Walther (1998, 2004 O. oregoniana Early Oligocene Bridge Creek, Oregon, USA Chaney (1927), Manchester and Crane (1987), Meyer and Manchester (1997) O. atlantidis Late Oligocene Enspel, Westwald, West Germany Köhler and Uhl (2014) O. humilis Late Oligocene Bouches-du-Rhône, Aix-en-Provence, France Saporta (1872) O. oregoniana Late Oligocene Beaverhead, Montana, USA Becker (1969) O. atlantidis Early Miocene Radoboj, Croatia Unger (1852) O. oeningensis Middle Miocene Oeningen, Switzerland Heer (1855), Teodoridis and Kvacekˇ (2005) O. subvirginiana Middle Miocene Honshu and Hokkaido, Japan Tanai (1961) O. huziokai Middle Miocene Several localities in Japan Huzioka (1943), Tanai (1961) O. uttoensis Middle Miocene Shanwang, Shandong Province, China WGCPC (1978) O. oregoniana Middle Miocene Clarkia, Idaho, USA Berry (1934), Smiley et al. (1975) Ostrya sp. Late Miocene Cerdanya, Lleida, Spain Barrón (1996) O. cf. oregoniana Miocene Seldovia Point, Alaska, USA Wolfe and Tanai (1980) and Walther, 1998). However, in East Asia, one of its main natu- Ailanthus, Fraxinus, Palaeocarya, Carpinus, Picea (Linnemann ral distribution areas today, Ostrya has not been confirmed prior et al., 2017) and Tsuga (Wu et al., 2020). Besides, leaves of to the Neogene in China, Japan and Korea (Table 1) (Huzioka, both gymnosperm and angiosperm were also excavated, such 1943; Tanai, 1961; WGCPC, 1978). With much older fossils as Cryptomeria (Ding et al., 2018b), Metasequoia, Mahonia, already known from Europe and North America, the Paleogene Quercus, Castanopsis, Ilex, Machilus, and Populus (Linnemann distribution of Ostrya in East Asia still remains unclear, which et al., 2017). is crucial to understanding the origin and evolution of Ostrya’s modern distribution pattern. 2.2. Methods Here we present 14 well-preserved fossil involucres of Ostrya from the lower Oligocene of Lühe Basin, Yunnan Province, Photos of fossil involucres were taken using a Nikon Southwest China. The material described below represents the D700 digital camera. Detailed structure of the specimens was earliest Ostrya fossil involucres from East Asia. The discovery of observed and photographed with a Leica S8AP0 stereo micro- these fossil involucres provides an unequivocal evidence for the scope. Specimen data of living species were obtained from existence of Ostrya in Southwest China in the early Oligocene. JSTOR (https://plants.jstor.org), Chinese Virtual Herbarium Besides, we reviewed the involucre fossil history of Ostrya and (CVH) Data Portal (http://www.cvh.ac.cn/), and herbarium at discussed the biogeographic implications of this finding. the Kunming Institute of Botany (KUN, China). Morphological measurements were made on the digital images using ImageJ 2. Material and methods (http://rsb.info.nih.gov/ij/). Fossil record of Ostrya was com- piled from publications and the online Fossilworks database 2.1. Geological setting (http://fossilworks.org). Fossil fruits were excavated from Lühe Basin, located in 3. Systematics Lühe town, Nanhua County, Yunnan Province, Southwest China ◦ ◦ (Fig. 1) (25 8.5 N, 101 22.5 E, 1882 m a.s.l.). The fossil- Order Fagales Engle bearing section of this study is a series of lacustrine mudstones that were exposed due to recent construction work. These fossil- Family Betulaceae Gray iferous deposits, lying on Cretaceous purple-red silty mudstones Genus Ostrya Scopoli and overlain by a Quaternary laterite (Zhang, 1996), are char- Ostrya sp. acterized by laminated yellow and dark grey silty mudstones intercalated by thin coal beds (Fig. 2). Based on the lowermost (Figs. 3, 4d, e) three layers of volcanic ash, recent U-Pb zircon dating shows Locality: Lühe town, Nanhua County, Yunnan Province, South- an age range between 33 ± 1 Ma and 32 ± 1 Ma, indicating the west China (Fig. 1). age of this fossil-bearing strata to be the earliest Oligocene (Linnemann et al., 2017). Age: The early Oligocene (33–32 Ma). The 14 fossil involucres of Ostrya were preserved as impres- Repository: Paleoecology Collections, Xishuangbanna Tropi- sions and other fossil fruits and cones were collected from the cal Botanical Garden (XTBG), Chinese Academy of Sciences. same lacustrine deposits, e.g., Dipteronia (Ding et al., 2018a), 754 T.X. Wang et al. / Palaeoworld 29 (2020) 752–760 Fig. 1. Fossil locality of Lühe town, Yunnan Province, Southwest China. Fig. 2. Geological cross section of the fossiliferous outcrop in Lühe town, Yunnan Province, Southwest China. Specimens examined: LH1-0085 (Fig. 3a), LH1-0158 Description: Fruits with bladder-like, elliptic or narrowly ellip- (Fig. 3b), LH1-0201 (Fig. 3c, d), LH1-0233 (Fig. 3e, f), LH1- tic to ovate involucres (Fig. 3), 8.4–23.3 mm long, 4.1–9.5 mm 0389 (Fig. 3g, h), LH1-0582 (Fig. 3i), LH1-0669 (Fig. 3m), wide, length to width ratio 1.6:1–2.6:1, 2.1:1 on average; apex LH1-0789 (Fig. 3j), LH2-0076 (Fig. 3n), LH2-0191 (Fig. 3o), rounded or apiculate with small pointed tip, base rounded, not LH3-229 (Fig. 3p), LH3-235 (Fig. 3k), LH3-236 (Fig. 3q), LH3- constricted into a stipe; longitudinal veins 6–10, subparallel, 240 (Fig. 3l). diverging from the base and converging apically, intercostal dis- T.X. Wang et al. / Palaeoworld 29 (2020) 752–760 755 Fig. 3. Fossil involucres of Ostrya sp. collected from Lühe town, Yunnan Province, Southwest China. (a) LH1-0085; (b) LH1-0158; (c, d) LH1-0201; (e, f) LH1-0233; (g, h) LH1-0389; (i) LH1-0582; (j) LH1-0789; (k) LH3-235; (l) LH3-240; (m) LH1-0669; (n) LH2-0076; (o) LH2-0191; (p) LH3-229; (q) LH3-236.