Fossil Involucres of Ostrya (Betulaceae) from the Early Oligocene of Yunnan

Home , Ostrya, Ostrya carpinifolia, Ostrya japonica

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

CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan 666303, China

University of Chinese Academy of Sciences, Beijing 100049, China

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.

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

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. Scale bar = 5 mm.

tance varied (Fig. 4e), sometimes fusing into intercostal veins; out of the involucre (e.g., Fig. 3b). This involucre of Ostrya can

intercostal veins nearly perpendicular to longitudinal veins, be easily distinguished from that of Carpinus which is foliaceous

sometimes dichotomous or reticulate (Fig. 4e), distance con- in shape and has a lobed and/or serrate margin with its nutlet

stant; single nutlet impression preserved on some specimens exposed. Apart from that, the involucre of Carpinus has a pin-

(Fig. 4d), ca. 4.5 × 2.0 mm in size, ovoid or oblong in outline, nate venation with a conspicuous midvein. This is distinguished

preserved at the base or loose within involucre (Fig. 4d). from that of Ostrya which has multiple primary veins of nearly

equal strength arising from the base without an evident mid-

Systematic afﬁnity: Ostrya is readily recognized and distin-

vein (Fig. 5). Accordingly, we assigned theses fossils to Ostrya.

guished by its involucre, which is a bladder-like or elliptic bract

However, its morphology, though recognizable at generic level,

with a single nutlet enclosed at the base (Fig. 4d). Sometimes the

is quite conservative at infrageneric level and can hardly serve

nutlet detaches within the involucre (Figs. 3p, 4 d) or even drops

756 T.X. Wang et al. / Palaeoworld 29 (2020) 752–760

Fig. 4. Details of involucres. (a, b) Involucre of Ostrya japonica (extant). (c) Carpinus fossil involucre (LH1-0097a) from the same site. (d, e) Close view of Ostrya

sp. in this study (LH3-229, LH1-0582). Scale bar: 0.5 cm for (a, c, d); 0.5 mm for (b); 2 mm for (e). DV: dichotomous veins; LV: longitudinal veins; NI: nutlet

impression; PV: perpendicular veins.

Table 2

Morphological comparison of involucre of fossil and extant Ostrya. Data of living species are from measurement on specimens in JSTOR, and herbarium at the

Kunming Institude of Botany (KUN), Flora of China (Li and Skvortsov, 1999), and Flora of North America (Furlow, 1997). Data of other fossil species are cited

from Chaney (1927), Tanai (1961), WGCPC (1978), Mai (1997), and Kvacekˇ and Walther (1998).

Species Length of Width of L:W ratio Number Distribution Size of nutlet (mm)

involucre (mm) involucre (mm) of veins

Ostrya sp. in this study 8.40–23.40 4.10–9.50 2.06 6–10 This site 4.2 × 2.4; 4.9 × 2.2

O. japonica 10.09–19.29 4.05–10.38 2.3 5–8 East Asia length 6–7

O. chinensis 12.54–21.52 4.45–9.32 2.3 5–8 East Asia, endemic to China 5–7 × 2-3

O. rehderiana 16.88–25.70 5.85–11.90 2.6 5–8 East Asia, endemic to China 7–10 × 2.5–3

O. trichocarpa 15–24 10–15 – – East Asia, endemic to China 5.5–9 × 2.5–3.5

O. carpinifolia 7.66–20.91 3.80–9.59 2.1 5–9 Europe –

O. virginiana 11.15–26.16 4.46–13.52 2.1 5–9 North America –

O. knowltonii 8.24–21.45 3.87–11.25 2.0 6–9 North America, endemic to USA –

O. chisosensis 9.22–17.27 3.71–6.95 2.4 6–9 North America, endemic to USA –

†O. atlantidis 11–25 5–14 – 8–10 Oligocene–Miocene, Europe 5 × 3

†

O. oregoniana 17–25 8–11 – – Oligocene–Miocene, North America 5 × 3

†O. huziokai 16–21 6–9 – 6–7 Miocene, Japan 6–9 × 3–4

†

O. uttoensis ca. 14 ca. 8 – Miocene, Japan –

†O. szaferi (represented by nutlets) – – – – Late Oligocene–Pliocene, Europe 3.5–5.3 × 2–3.4

T.X. Wang et al. / Palaeoworld 29 (2020) 752–760 757

almost the same foliar characters, such as lanceolate or ovate

leaf shape, doubly serrate teeth and cordate leaf base, with some

species of its related genera, e.g., Carpinus, Paracarpinus, and

Betula (Crane, 1981; Manchester and Crane, 1987; Mai, 1995;

Meyer and Manchester, 1997; Hably et al., 2000). Liu (1996)

considered that the external veins of Ostrya leaves are much

more developed than those of Carpinus, but we observed that

some Carpinus species such as C. betulus and C. cordata also

have conspicuous external veins while those of O. knowltonii

are not very well developed. Detailed studies on leaf epider-

mal characters have made it possible to distinguish Ostrya from

other genera of Betulaceae based on the structure of stomatal

apparatus (Chen and Zhang, 1991; Liu, 1996), but only with

well-preserved cuticle can such identiﬁcation be made in fos-

sils. Thus, the previously reported Ostrya fossil leaves, if not

associated with fruits and no preserved cuticle, may still require

further investigation.

Fossil wood of Ostrya is distinguishable, and Carpinus also

shows morphological resemblance to that of Ostrya. However,

Ostrya differs from Carpinus in having radial pore arrangement

with many radial multiple pores and sometimes aggregate rays

(Suzuki and Watari, 1994). Despite the taxonomic signiﬁcance

of Ostrya’s wood, these records are less biogeographically rep-

resentative due to the very few occurrences only in the Miocene

of Japan and Korea (Supplementary Table 1) (Suzuki and Watari,

1994; Jeong et al., 2009).

Ostrya

Fig. 5. Diagram showing the difference of involucre venation between Ostrya The involucre of , especially, can serve as a convinc-

and Carpinus. (a) Drawing of Ostrya sp. fossil involucre in this study (LH1- ing and representative evidence for the assignment of Ostrya.

0233b). (b) Drawing of Carpinus fossil involucre from the same site (LH1-

Its diagnostic bladder-like or sac-like involucre fully enclos-

0097a). Scale bar = 0.5 cm.

ing a single nutlet can be readily recognized. It can be easily

distinguished from Carpinus that has a foliaceous involucre

as a diagnostic character on the basis of involucre alone (Wolfe

having serrate margins with its nutlet exposed (Crane, 1981;

and Tanai, 1980). In fact, the size of involucre is variable within

Chen, 1994). Therefore, in most cases, an involucre is neces-

species and even within individual (Table 2), and its shape is

sary to conﬁdently determine the presence of Ostrya. In all,

prone to compression or deposit (author’s observation). The only

fossil records of Ostrya involucre can serve as a robust proxy

extant species having a morphologically distinct involucre is O.

than any other organ to indicate the historical occurrence of

rehderiana, whose base is constricted into a stipe and the involu-

Ostrya.

cre size is relatively large. This constricted base is not seen in

A large quantity of betulaceous fossil leaves were also dis-

our specimens. Besides, the venation pattern of involucre among

covered in the Lühe site (Linnemann et al., 2017), but all of them

modern species is almost identical even between two geograph-

are preserved as impressions and no further cuticle analysis can

ically isolated species. Therefore, the involucre can hardly serve

be made to distinguish some of these leaves from Carpinus to

as an identifying organ, or at least not a convincing organ to make

Ostrya. Thus, the discovery of these Ostrya involucres in Lühe

fossil species delimitation. In terms of other fossil species, there

Basin provides an unequivocal record for the existence of this

is also lack of any distinguishing involucre character between the

genus in East Asia in the early Oligocene.

two reported species, namely O. oregoniana in western North

Involucres of Carpinus were also discovered in this site

America and O. atlantidis in Europe (Hably et al., 2000). Mor-

(Fig. 4c), indicating that the coexistence of these two phylo-

phological comparison shows that our fossils have a size range of

genetically close genera dates back to as early as 32 ± 1 Ma

8.4–23.4 mm × 4.1–9.5 mm that fall within some fossil species

(Linnemann et al., 2017), which is coeval with European records

and extant species (Table 2). Besides, no other distinguishing

(Kvacekˇ and Walther, 2004; Walther and Kvacek,ˇ 2007) and

characters were found in our fossil specimens. Therefore, we

possibly predates that of North America, because of the lack

assign these fossils to Ostrya sp.

of convincing Paleogene record for Carpinus on this continent

(Manchester, 1999). With abundant Betulaceae fossil materials

4. Discussion

having been discovered in this site (Linnemann et al., 2017), a

4.1. Signiﬁcance of involucre in determining Ostrya more comprehensive palaeobotanical study will give us a bet-

ter understanding of the modernization of Yunnan ﬂora in the

Fossil Ostrya is readily recognized by the presence of its Paleogene.

involucre rather than its leaf, because the leaf of Ostrya shares

758 T.X. Wang et al. / Palaeoworld 29 (2020) 752–760

Fig. 6. Historical geographic distribution of Ostrya based on fossil involucre records (according to Table 1) and its modern distribution.

4.2. Fossil history of Ostrya involucre there is only one previously recognized occurrence in the mid-

dle Miocene of Shanwang, Shandong Province, China, namely

Unequivocal fossil record of Ostrya, here referring to O. uttoensis (WGCPC, 1978). This species showed morpho-

involucre fossils, starts almost simultaneously from the early logical resemblance to O. japonica (WGCPC, 1978), the most

Oligocene of both Europe and North America, represented widely distributed extant Ostrya species in East Asia ranging

by fossil involucres and leaves of O. atlantidis Unger in from central-eastern China to Korea and Japan today (Li and

Czech Republic (Kvacekˇ and Walther, 1998) and O. oregoniana Skvortsov, 1999). No fossil involucre of Ostrya was reported

Chaney in Oregon, USA (Meyer and Manchester, 1997). The from Russia in our knowledge for now.

former occurrence, proved by a K-Ar radiometric dating in ﬂora

of Kundratice, North Bohemia, dates back to 32.75 0.82 Ma 4.3. Biogeographic implications

(Kvacekˇ and Walther, 1998), and had been reported in Czech

Republic and Germany during the early Miocene (Unger, 1852; The fossil involucres from Lühe ﬂora represent the earliest

Engelhardt, 1885; Kvacek,ˇ 2004; Kvacekˇ and Walther, 2004; Ostrya record in East Asia (33–32 Ma) that is virtually coeval

Walther and Kvacek,ˇ 2007; Köhler and Uhl, 2014). The lat- with other fossil species from European (32.75 ± 0.82 Ma)

ter species was ﬁrst discovered in Bridge Creek ﬂora of the and North American (32.58 ± 0.13 Ma) records (Meyer and

Crooked River Basin with an age of 32.58 0.13 Ma supported Manchester, 1997; Kvacekˇ and Walther, 1998; Linnemann et al.,

40 39

by an Ar– Ar dating (Chaney, 1927; Meyer and Manchester, 2017). This is also the southernmost fossil record of Ostrya

1997), and had been observed in Oregon, Idaho and Montana around the world, indicating that Ostrya had inhabited in regions

until the Miocene (Berry, 1934; Becker, 1969; Smiley et al., with a wide latitudinal range from middle to low latitude since

1975; Dillhoff et al., 2009). Besides, there is an Ostrya involu- then. Today, Ostrya species are distributed in temperate and

cre record reported in the Miocene ﬂora of Seldovia point ﬂora subtropical forests across the Northern Hemisphere mainly in

from Kenai group, Alaska, which was assigned to O. cf. orego- mid-latitude and low-latitude montane regions, which is gen-

niana (Wolfe and Tanai, 1980). In Europe, there are two other erally similar to its distribution pattern in the early Oligocene

species, namely O. humilis reported by Saporta (1872) and O. (Fig. 6), suggesting that the modern distribution pattern of

oeningensis reported by Heer (1855). These two species and O. Ostrya may have been established by the early Oligocene

atlantidis are in need of further investigation to ascertain their (33–32 Ma).

relationships. However, extant Ostrya species usually have a narrow distri-

In East Asia, about 3 species of fossil involucres were bution restricted mostly in moist montane regions in temperate

reported in the Miocene. O. japonica oblongibracteata was and subtropical forest, and they also colonize limestone moun-

ﬁrst reported with only one specimen in the middle Miocene tains occasionally (Furlow, 1997; Li and Skvortsov, 1999; Pasta

of Japan and Korea (Huzioka, 1943), but this species was later et al., 2016). This is because Ostrya is actually a stenohydric

assigned to O. huziokai based on subsequent discovery of more genus, which means that it has rather constant transpiration and

specimens (Tanai, 1961). Another species, O. subvirginiana, osmotic pressure values even under moderate drought-stressed

was also described from the middle Miocene of Japan and conditions (Pasta et al., 2016), enabling it to colonize both humid

was known from Miocene ﬂora in several localities of Hon- and relatively dryer areas like limestone mountains. Even though

shu and Hokkaido (Tanai, 1961). As for Chinese fossil records, Ostrya may have a wide ecological amplitude and is adaptive

T.X. Wang et al. / Palaeoworld 29 (2020) 752–760 759

to various moisture condition, it has shown some responses to Chaney, R.W., 1927. Geology and palaeontology of the Crooked River Basin,

with special reference to the Bridge Creek ﬂora. Carnegie Institution of

climate change as the European fossil records demonstrate a

Washington, Publication No. 346, 45–138.

southward retreat since the Oligocene, possibly due to the global

Chen, Z.D., 1994. Phylogeny and phytogeography of the Betulaceae (Cont.).

cooling in the late Cenozoic (Fig. 6) (Mosbrugger et al., 2005).

Acta Phytotaxonomica Sinica 32 (2), 101–153 (in Chinese, with English

The Miocene involucre record in Alaska also shows that Ostrya abstract).

had once reached high latitude within the Arctic Circle (Fig. 6) Chen, Z.D., Zhang, Z.Y., 1991. A study on foliar epidermis in Betulaceae. Acta

Phytotaxonomica Sinica 29 (2), 156–163 (in Chinese, with English abstract).

(Wolfe and Tanai, 1980), when global temperature was relatively

Crane, P.R., 1981. Betulaceous leaves and fruits from the British Upper

high according to marine oxygen isotope (Zachos et al., 2001).

Palaeocene. Botanical Journal of the Linnean Society 83, 103–136.

This record also represents Ostrya’s occurrence at the highest

Dillhoff, R.M., Dillhoff, R.A., Dunn, R.E., Meyers, J.A., Strömberg, C.A.E.,

latitude, indicating another evidence of wide distribution rang- 2009. Cenozoic paleobotany of the John Day Basin, central Oregon. In:

ing from high-latitude Alaska to mid-latitude Idaho during the O’Connor, J.E., Dorsey, R.J., Madin, I.P. (Eds.), Volcanoes to Vineyards:

Miocene. Geologic Field Trips through the Dynamic Landscape of the Paciﬁc North-

west. Geological Society of America Field Guide 15, 135–164.

We further infer that Ostrya might have inhabited higher lati-

Ding, W.N., Huang, J., Su, T., Xing, Y.W., Zhou, Z.K., 2018a. An early Oligocene

tude areas, probably within the Arctic Circle during the Eocene,

occurrence of the palaeoendemic genus Dipteronia (Sapindaceae) from

a time period close to estimated crown group age of Ostrya- Southwest China. Review of Palaeobotany and Palynology 249, 16–23.

Carpinus clade (Xiang et al., 2014), when the global climate Ding, W.N., Kunzmann, L., Su, T., Huang, J., Zhou, Z.K., 2018b. A new fossil

species of Cryptomeria (Cupressaceae) from the Rupelian of the Lühe Basin,

was in a state of “greenhouse” (Zachos et al., 2001). After the

Yunnan, East Asia: Implications for palaeobiogeography and palaeoecology.

dramatic temperature decrease recorded as Eocene–Oligocene

Review of Palaeobotany and Palynology 248, 41–51.

Transition (Zachos et al., 2001), Ostrya moved southward and

Engelhardt, H., 1885. Die Tertiärﬂora des Jesuitengrabens bei Kundratitz in

entered mid-low latitude areas where its southernmost limit can Nordböhmen. Nova Acta Academiae Caesareae Leopoldino-Carolineae

be at low latitudes of Southwest China in the early Oligocene, Germanicae Naturae Curiosorum 48, 259–408 (in German).

Furlow, J.J., 1997. Betulaceae. In: Flora of North America Editorial Committee

and this formed the distribution pattern of Ostrya and lasts until

(Ed.), 1993+. Flora of North America: North of Mexico, Vol. 3. Oxford

now (Fig. 6).

University Press, New York, pp. 507–538.

Grimm, G.W., Renner, S.S., 2013. Harvesting Betulaceae sequences from Gen-

Acknowledgements Bank to generate a new chronogram for the family. Botanical Journal of the

Linnean Society 172, 465–477.

Hably, L., Kvacek,ˇ Z., Manchester, S.R., 2000. Shared taxa of land plants in the

We thank Prof. Steven R. Manchester and Prof. Terry A. Lott

Oligocene of Europe and North America in context of Holarctic phytogeog-

from Florida Museum of Natural History, Prof. Lutz Kunzmann

raphy. Acta Universitatis Carolinae, Geologica 44 (1), 59–74.

from Senckenberg Natural History Collections Dresden and Dr.

Heer, O., 1855. Flora Tertiara Helvetica, Vol. 1. J. Wurster & Compagnie,

Yuqing Wang from Chiba University for offering some important Winterthur, 117 pp. (in German).

references. We also thank colleagues from the Palaeoecology Huzioka, K., 1943. On some fossil involucres of Ostrya and Carpinus from

the Miocene deposits of Hokkaidô and Tyôsen. Journal of the Geological

Research Group of Xishuangbanna Tropical Botanical Garden

Society of Japan 50, 317–325 (in Japanese, with English abstract).

(XTBG) for fossil collecting and Public Technology Service

Jeong, E.K., Kim, K., Suzuki, M., Kim, J.W., 2009. Fossil woods from the Lower

Center, Chinese Academy of Sciences (CAS) for help with fos-

Coal-bearing Formation of the Janggi Group (Early Miocene) in the Pohang

sil photography. We are grateful to Prof. Steven R. Manchester Basin, Korea. Review of Palaeobotany and Palynology 153, 124–138.

and Dr. Gong-Le Shi for their helpful feedback and constructive Köhler, J., Uhl, D., 2014. Die Blatt- und Karpoﬂora der oberoligozänen Fossil-

lagerstätte Enspel (Westerwald, Rheinland-Pfalz, W-Deutschland). Mainzer

suggestions on the manuscript. This research was supported by

Naturwissenschaftliches Archiv Beihefte 35, 1–87 (in German, with English

National Natural Science Foundation of China (No. U1502231,

abstract).

No. 41772026, No. 41922010) and NSFC–NERC (Natural

Kvacek,ˇ Z., 2004. Revisions to the Early Oligocene ﬂora of Flörsheim (Mainz

Environment Research Council of the United Kingdom) joint Basin, Germany) based on epidermal anatomy. Senckenbergiana Lethaca

research program (41661134049 and NE/P013805/1). 84, 1–73.

Kvacek,ˇ Z., Walther, H., 1998. The Oligocene volcanic ﬂora of Kundratice near

Litomerice, Ceske Stredohori Volcanic Complex (Czech Republic): a review.

Appendix A. Supplementary data

Acta Musei Nationalis Pragae, Series B, Historia Naturalis 54, 1–42.

Kvacek,ˇ Z., Walther, H., 2004. Oligocene ﬂora of Bechlejovice at Deˇcínˇ from

Supplementary material related to this article can be the neovolcanic area of the Ceské stredohoˇ ríˇ Mountains, Czech Republic.

found, in the online version, at doi:https://doi.org/10.1016/ Acta Musei Nationalis Pragae, Series B, Historia Naturalis 60, 9–60.

j.palwor.2019.11.004. Li, P., Skvortsov, A., 1999. Betulaceae. In: Wu, C.Y., Raven, P.H., Hong, D.Y.

(Eds.), Flora of China. Science Press and Missouri Botanical Garden Press,

Beijing and St. Louis, pp. 286–313.

References Linnemann, U., Su, T., Kunzmann, L., Spicer, R.A., Ding, W.N., Spicer, T.E.V.,

Zieger, J., Hofmann, M., Moraweck, K., Gärtner, A., Gerdes, A., Markos,

Barrón, E., 1996. Caracterización de la familia Betulaceae SF Gray (Magno- L., Zhang, S.T., Li, S.F., Tang, H., Huang, J., Mulch, A., Mosbrugger, V.,

liophyta), en el Vallesiense (Neógeno) de la Cerdanya (Lleida, Espana).˜ Zhou, Z.K., 2017. New U-Pb dates show a Paleogene origin for the modern

Treballs del Museu de Geologia de Barcelona 5, 171–211 (in Spanish, with Asian biodiversity hot spots. Geology 46, 3–6.

English abstract). Liu, Y.S., 1996. Foliar architecture of Betulaceae and a revision of Chinese

Becker, H.F., 1969. Fossil plants of the Tertiary Beaverhead basins in southwest- betulaceous megafossils. Palaeontographica Abteilung B 239, 23–57.

ern Montana. Palaeontographica Abteilung B 127, 1–142. Mai, D.H., 1995. Tertiäre Vegetationsgeschichte Europas: Methoden und Ergeb-

Berry, E.W., 1934. Miocene plants from Idaho. U.S. Geological Survey Profes- nisse. Gustav Fischer Verlag, Jena, 691 pp. (in German).

sional Paper 185-E, 97–125.

760 T.X. Wang et al. / Palaeoworld 29 (2020) 752–760

Mai, D.H., 1997. Die oberoligozänen Floren am Nordrand der Sächsischen Teodoridis, V., Kvacek,ˇ Z., 2005. The extinct genus Chaneya Wang et Manch-

Lausitz. Palaeontographica Abteilung B 244, 1–124 (in German). ester in the Tertiary of Europe — a revision of Porana-like fruit remains

Manchester, S.R., 1999. Biogeographical relationships of North American Ter- from Öhningen and Bohemia. Review of Palaeobotany and Palynology 134,

tiary ﬂoras. Annals of the Missouri Botanical Garden 86, 472–522. 85–103.

Manchester, S.R., Crane, P.R., 1987. A new genus of Betulaceae from the Unger, F., 1852. Iconographia plantarum fossilium. Abbildungen und Beschrei-

Oligocene of western North-America. Botanical Gazette 148, 263–273. bungen fossilier. Pfanzen. Denkschriften Akademie der Wissenschaften 4,

Meyer, H.W., Manchester, S.R., 1997. The Oligocene Bridge Creek Flora of 73–118 (in German).

the John Day Formation, Oregon. University of California Publications in Walther, H., Kvacek,ˇ Z., 2007. Early Oligocene ﬂora of Seifhennersdorf (Sax-

Geological Sciences 141, 1–195. ony). Acta Musei Nationalis Pragae, Series B, Historia Naturalis 63, 85–174.

Mosbrugger, V., Utescher, T., Dilcher, D.L., 2005. Cenozoic continental cli- WGCPC (Writing Group of Cenozoic Plants of China), 1978. Fossil Plants of

matic evolution of Central Europe. Proceedings of the National Academy of China, Vol. 3: Cenozoic Plants from China. Science Press, Beijing, 232 pp.

Sciences of the United States of America 102, 14964–14969. (in Chinese).

Pasta, S., de Rigo, D., Caudullo, G., 2016. Ostrya carpinifolia in Europe: Wolfe, J.A., Tanai, T., 1980. The Miocene Seldovia Point Flora from the Kenai

distribution, habitat, usage and threats, Ostrya carpinifolia in Europe: dis- Group, Alaska. U.S. Geological Survey Professional Paper 1105, 1–52.

tribution, habitat, usage and threats. In: San-Miguel-Ayanz, J., de Rigo, D., Wu, M.X., Huang, J., Su, T., Leng, Q., Zhou, Z.K., 2020. Tsuga seed cones

Caudullo, G., Houston Durrant, T., Mauri, A. (Eds.), European Atlas of For- from the late Paleogene of southwestern China and their biogeographical

est Tree Species. Publication Ofﬁce of the European Union, Luxembourg, and paleoenvironmental implications. Palaeoworld 29, 617–628.

pp. 112–113. Xiang, X.G., Wang, W., Li, R.Q., Lin, L., Liu, Y., Zhou, Z.K., Li, Z.Y., Chen,

Saporta, G., 1872. Études sur la végétation du sud-est de la France à l’époque Z.D., 2014. Large-scale phylogenetic analyses reveal fagalean diversiﬁ-

Tertiaire. Suppl. 1, Révision de la Flore des gypses d’Aix. Masson, Paris (in cation promoted by the interplay of diaspores and environments in the

French). Paleogene. Perspectives in Plant Ecology, Evolution and Systematics 16,

Smiley, C.J., Gray, J., Huggins, L.M., 1975. Preservation of Miocene fossils 101–110.

in unoxidized lake deposits, Clarkia, Idaho — with a section on fossil Yang, X.Y., Wang, Z.F., Luo, W.C., Guo, X.Y., Zhang, C.H., Liu, J.Q., Ren,

Insecta by W. F. Barr and J. M. Gillespie. Journal of Paleontology 49 (5), G.P., 2019. Plastomes of Betulaceae and phylogenetic implications. Journal

833–844. of Systematics and Evolution 57 (5), 508–518.

Suzuki, M., Watari, S., 1994. Fossil wood ﬂora of the early Miocene Nawa- Zachos, J., Pagani, M., Sloan, L., Thomas, E., Billups, K., 2001. Trends, rhythms,

mata Formation of Monzen, Noto Peninsula, Central Japan. Journal of Plant and aberrations in global climate 65 Ma to present. Science 292, 686–693.

Research 107, 63–76. Zhang, Y.Z., 1996. Multiple Classiﬁcation and Correlation of the Stratigraphy

Tanai, T., 1961. Neogene ﬂoral change in Japan. Journal of the Faculty of Sci- in China. Stratigraphy (Lithostratic) of Yunnan Province. China University

ence, Hokkaido University, Series IV, Geology and Mineralogy 11, 119–398. of Geosciences Press, Wuhan, 366 pp. (in Chinese).