Plant Systematics and Evolution

, Volume 299, Issue 3, pp 643–658

A new species of Carpinus (Betulaceae) from the Pliocene of Yunnan Province, China

Authors

  • Jing Dai
    • Key Laboratory of Western China’s Environmental Systems of the Ministry of Education and School of Earth ScienceLanzhou University
    • College of Earth ScienceYunnan University
    • Key Laboratory of Western China’s Environmental Systems of the Ministry of Education and School of Earth ScienceLanzhou University
  • Sanping Xie
    • Key Laboratory of Western China’s Environmental Systems of the Ministry of Education and School of Earth ScienceLanzhou University
  • Zhicheng Lin
    • Key Laboratory of Western China’s Environmental Systems of the Ministry of Education and School of Earth ScienceLanzhou University
    • School of Petroleum and Natural Gas EngineeringChongqing University of Science and Technology
  • Jingyu Wu
    • Key Laboratory of Western China’s Environmental Systems of the Ministry of Education and School of Earth ScienceLanzhou University
    • State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences)
  • Kequn Dao
    • Key Laboratory of Western China’s Environmental Systems of the Ministry of Education and School of Earth ScienceLanzhou University
Original Article

DOI: 10.1007/s00606-012-0750-1

Cite this article as:
Dai, J., Sun, B., Xie, S. et al. Plant Syst Evol (2013) 299: 643. doi:10.1007/s00606-012-0750-1

Abstract

Macrofossils of Carpinus have been widely reported from the Cenozoic of the Northern Hemisphere. However, the leaf cuticules of the genus have rarely been described. A new species, named Carpinustengchongensis Dai et B.N. Sun, sp. nov., is identified based on 13 leaf fossils, collected from the late Pliocene Mangbang Formation, Tengchong County of Yunnan Province, China. The important characters of the fossil are its oblong-ovate leaf shape, obliquely cordate base, doubly serrulate margin, straight and moderately thick primary vein, pinnate secondary veins, percurrent tertiary veins, orthogonally reticulate areoles, absence of veinlets, anomocytic stomata with double-layered stomatal rim, well-formed T-pieces and trichome bases, which indicates an affinity within the genus Carpinus section Carpinus subsection Monbeigianae, especially with C. tsaiana. Carpinus fossils were present from the Eocene to Pliocene with disjunctive distribution in the North Temperate Zone, which broadly reflected the present distribution pattern and probably demonstrates the tolerance of Carpinus to environmental change.

Keywords

CarpinusCuticular featuresPlioceneWestern Yunnan

Introduction

Yunnan, located in southwest China, is a significant place of botanical diversity and endemism, where the elements of flora are complicated and rich in species numbers (Wu and Zhu 1987). Many Neogene macrofossil floras and palynofloras are found in Yunnan. In particular, macrofossils are primarily reported from Xiaolongtan, Lanping, Eryuan, Lühe, Lincang, Mangdan, Qujing, and Tengchong (WGCPC 1978; Tao 1986, 1992; Guo and Chen 1989; Liu and Zheng 1995; Yi 2002; Zhao et al. 2004; Wang and Shu 2004; Jacques et al. 2011). Palynofloras have been investigated in Xiaolongtan, Jinggu, Lühe and Yangyi (Song and Zhong 1984; Wang 1996; Xu et al. 2000, 2003, 2004, 2008). In addition, preliminary research on the Mangbang flora by Tao and Du (1982) identified 36 species of fossil plants including the genus of Carpinus based on leaf gross morphology, A further study on the Mangbang Formation reveals a remarkable macrofossil plant assemblage in Tengchong and indicates its significance for reconstructing the late Neogene paleoecology and paleoclimate in western China (Wu et al. 2009). Sun et al. (2003) assigned a fossil leaf from Tengchong to Carpinus subcordata, followed by the discovery of some new materials of the genus Carpinus, which could be anatomically investigated.

Carpinus belongs to the family Betulaceae subfamily Coryloideae (Hall 1952; Jury 1978; Li and Zheng 1979), which is native to the Northern Hemisphere from Europe to eastern Asia, south to the Himalayas, and in North and Central America (Furlow 1979; Heywood 1993). Morphological and phylogenetic studies typically recognize two sections of the genus: Distegocarpus (Sieb. et Zucc.) Sargent and Carpinus (Eucarpinus) Sargent (Winkler 1904; Li and Zheng 1979; Yoo and Wen 2002, 2007). The earliest reliable fossil involucres have been reported from the late Eocene of Japan (Tanai 1972; Crane 1981). However, Pigg and Manchester (2003) later pointed out that the earliest known fruit record of Carpinus comes from the middle Eocene of North America. Although Carpinus leaves have been identified from the Paleocene of Japan and China, their taxonomic affinities are dubious (Uemura and Tanai 1993; Liu 1996). Fossil records of Carpinus from the Eocene to Pliocene are reviewed (Fig. 1). It is clear that a major radiation of the genus took place between the late Eocene and Miocene in the Northern Hemisphere (Heer 1869; Mai and Walther 1978, 1991; Manchester 1999; Liu 2000). Commonly found Carpinus-like leaves are hard to distinguish based on leaf morphology (Manchester and Crane 1987), so a cuticular analysis is necessary for a more accurate identification (Wilhelm 1981). However, previous work has mainly focused on foliar architecture (Tao and Du 1987; Cao and Cui 1989; Liu 1996), with the cuticular microstructure of fossil Carpinus being rarely reported. In this paper, we study the cuticular structure of the Tengchong material using light microscope (LM) and scanning electron microscope (SEM), and compare them with previously reported fossils and extant taxa.
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Fig. 1

Modern distribution and fossil records of Carpinus (modified from Chen 1994). 1 Modern distribution of section Distegocarpus, 2 Modern distribution of section Carpinus, 3 Pliocene, 4 Miocene, 5 Oligocene, 6 Eocene

Materials and methods

Geological setting

Tengchong is in western Yunnan, close to the southeast of the Qinghai-Tibet Plateau. The present fossils were collected from an open-cast diatomite mine about 1 km west of Tuantian Town (N 24°46′, E 98°38′), Tengchong Country, Yunnan Province, southwest China (Fig. 2). The fossil-bearing horizons occur in the diatomitic sediments of the Mangbang Formation.
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Fig. 2

Fossil location in Tengchong, Yunnan Province, China

The Mangbang Formation is unconformably underlain by the Nanlin Formation and angularly unconformably overlain by the Mingguang Formation. Lithologically, the Mangbang Formation is divided into three units (Ge and Li 1999): the bottom unit which mainly consists of sandy conglomerate, grayish sandy conglomerate, grayish-white clayey siltstone and grayish-white sandstone; the middle unit which is a widely distributed basalt unit about 400 m thick; and the top unit which mainly contains grayish-granitic pebbled sandstone, red mudstone, grayish-red claystone and diatomite. Many fossils have been discovered in the top of the formation (Ge and Li 1999). Li et al. (2004) studied the geological age and sedimentary environment of the Mangbang Formation. Based on stratigraphic correlation, they concluded that the Mangbang flora is of late Pliocene age. Moreover, based on the K–Ar dating of the basaltic middle unit in the Mangbang Formation and the andesitic rocks in the overlying Mingguang Formation (Mu et al. 1987; Jiang 1998; Li et al. 2000), the age of the fossil-bearing layer is considered to be 2.5 ± 0.3 Ma, which is a late Pliocene to early Pleistocene age according to the latest International Stratigraphic Chart 2009.

Fossil materials and preparation

The specimens studied include previously and newly collected materials, which are stored in the Paleontologic Laboratory, Lanzhou University. Cuticular fragments were taken from the fossil specimens. They were first immersed in 10 % HCl solution for 2–5 h to remove calcium carbonate and then washed and immersed in 50 % HF solution for 12–24 h to remove silicates. After that, the fragments were macerated for 1–5 h in a mixed solution of 10 % NaClO and a few drops of 30 % HCl until the upper and lower epidermis separated. After staining in 0.5 % safranine-water solution, the cuticular fragments were mounted on slides, embedded in glycerin, and photographed under a Leica DM4000B light microscope at Lanzhou University. For SEM, the cuticles were mounted on a stub, coated with gold, and examined under a scanning electron microscope (JEOL JSM–5600LV) at the Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences.

Modern materials and preparation

We investigated herbarium material of four modern species from the Kunming Institute of Botany, Yunnan Province and freshly collected leaves of Carpinus cordata Blume from Xi’an Botanic Garden. The leaves of these five species show the closest resemblance to those of the fossil species in morphology They were cut into 2 cm by 2 cm size, immersed in a 1:1 solution of 10 % glacial acetic acid and 10 % H2O2, and then placed in a hot-water bath at 80–90 °C for 4–6 h until the cuticles turned white and transparent, when both the upper and lower epidermis could easily be separated. The same procedures for LM and SEM preparations were then followed as those for the fossil leaves.

Results

Systematics

Family Betulaceae Gray.

Genus Carpinus Linnaeus 1737.

Species: Carpinustengchongensis Dai et B.N. Sun, sp. nov. (Figs. 3, 4a–e, 5a–c, g–i, 6a–e).
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Fig. 3

Leaf morphology of Carpinustengchongensis sp. nov. ae, gscale bars = 1 cm. fscale bars = 0.5 cm. hscale bars = 0.3 cm. a Specimen no. FTP-1-318-7, b specimen no. FTP-2-215-83, c specimen no. FTP-1-008, d specimen no. FTP-1-315-1, e specimen no. FTP-2-223-1, f details of venation enlarged from FTP-2-305-4, showing the orthogonally reticulate higher-order veins, g–h details of venation and serrulation enlarged from d, g showing tertiary veins perpendicular or oblique to secondary veins, d showing secondary vein enter teeth basally

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Fig. 4

Leaf morphology of Carpinustengchongensis sp. nov. (a–e, g) and extant Carpinustsaiana (f, h–j). a–gScale bars = 1 cm, hscale bar = 0.3 cm, i, jscale bars = 0.2 cm. a Specimen no. FTP-2-215-91, b specimen no. FTP-1-320-5, c specimen no. FTP-1-320-15, d specimen no. FTP-3-304-1, e specimen no. FTP-3-224-25, f herbarium specimen of Carpinustsaiana (Collector: Lv qinghua, field number: 5462, it is housed in Kunming Institute of Botany, Yunnan Province), g details of leaf base from c, showing the cordate base and incurved secondary vein basally, h–j details of venation and serrulation enlarged from f, h showing tertiary veins perpendicular or oblique to the secondary veins, i showing the orthogonally reticulate higher-order veins, j showing secondary vein enter teeth basally

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Fig. 5

Cuticular features of Carpinustengchongensis sp. nov. and Carpinustsaiana Hu under the SEM, a–fscale bars = 40 μm, g–lscale bars = 8 μm. a Inner surface of upper epidermis of Carpinustengchongensis,b inner surface of lower epidermis of Carpinustengchongensis,c outer surface of lower epidermis of Carpinustengchongensis,d inner surface of upper epidermis of Carpinustsaiana,e inner surface of lower epidermis of Carpinustsaiana,f outer surface of lower epidermis of Carpinustsaiana,g inner surface of stomata of Carpinustengchongensis,h–i outer surface of stomata of Carpinustengchongensis, showing the double-layered stomatal rim, j inner surface of stomata of Carpinustsaiana,k–l outer surface of stomata of Carpinustsaiana, showing the double-layered stomatal rim

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Fig. 6

Cuticular features of Carpinustengchongensis sp. nov., Carpinuscordata Blume and Carpinustsaiana Hu under light microscopy. a, b, f, g, i, jscale bars = 50 μm, c–e, h, k, lscale bars = 25 μm. a Upper epidermis of Carpinustengchongensis,b lower epidermis of Carpinustengchongensis,c lower epidermis of Carpinustengchongensis, showing the straight anticlinal walls and double-layered stomatal rim, d trichome base on the upper epidermis of Carpinustengchongensis,e trichome base on the lower epidermis of Carpinustengchongensis,f upper epidermis of Carpinuscordata,g lower epidermis of Carpinuscordata, showing the acicular trichome, h lower epidermis of Carpinuscordata, showing the peltate glandular trichome, i upper epidermis of Carpinustsaiana,j lower epidermis of Carpinustsaiana,k lower epidermis of Carpinustsaiana, showing the undulate anticlinal walls and double-layered stomatal rim, l trichome base of Carpinustsaiana

Holotype: FTP-1-318-7 (Fig. 3a).

Paratypes: FTP-1-008, FTP-1-315-1, FTP-1-317-16, FTP-1-320-5, FTP-1-320-15, FTP-2-155, FTP-2-215-91, FTP-2-215-83, FTP-2-223-1, FTP-2-305-4, FTP-3-224-25; FTP-3-304-1.

Etymology: The specific epithet is based on the name of the fossil locality.

Type locality: Tuantian Town open-cast diatomite mine, Tengchong County, Yunnan Province, China.

Age: The late Pliocene.

Specific diagnosis—Leaf blade ovate-oblong or elliptic, 7–13 cm long by 4.9–8.3 cm wide, with low length to width ratio (1.5–1.9); apex attenuate; base obliquely cordate; leaf margin doubly serrulate, with medium to very small teeth; primary vein thick; secondary veins 13–15 pairs, craspedodromous, curved and branched near leaf margin; tertiary veins percurrent; higher-order veins orthogonally reticulate; areoles regular; veinlets absent; upper epidermis smooth, epidermal cells tetragonal and pentagonal, or elongate, anticlinal walls straight and moderately thick, periclinal walls slightly concave, areolas well developed; lower epidermis thinner than upper epidermis, anticlinal walls straight or slightly rounded; stomata randomly orientated and anomocytic, broadly elliptical or rounded in shape, stomatal length quite large (average 34 μm), with double-layered stomatal rim; T-pieces present; trichome bases occur adaxially and abaxially.

Description

Macro-morphological description—leaf blade is ovate-oblong or elliptic, 7–13 cm long by 4.9–8.3 cm wide; length to width ratio is 1.5–1.9, the widest part being in the middle; apex attenuate, base obliquely cordate (Figs. 3a–e, 4a–c); leaf margin is doubly serrulate, with medium to small teeth, the apical side flexuous or convex, and the basal side straight or convex; the tooth apices are acute, rarely slightly rounded, with acute sinuses between teeth (Fig. 3h); 4–6 teeth present in interval between two consecutive secondary veins; primary vein is straight and moderately thick; secondary veins are straight or slightly curved upwards and the first one at base incurved (Fig. 4g), craspedodromous, up to 13–15 pairs, spaced at 0.3–1.2 cm, increasing basally; angles of secondary veins ranging from 40º to 80º, increasing basally (Figs. 3a, d, 4c); close to the leaf margin the secondary veins slightly curved and branched, entering teeth basally and bending sharply upwards (Fig. 3h), terminating mostly in apices, rarely in sinuses of teeth, branches of secondary veins also terminate in apices of teeth; tertiary veins are percurrent, almost parallel to each other, perpendicular or oblique to the secondary veins and oblique to the primary vein (Fig. 3g), forming an angle of 125°–140° with the primary vein, five to eight tertiary veins per 1 cm of secondary vein; higher-order veins are mostly orthogonally reticulate, areoles commonly regular, without veinlets (Fig. 3f).

Micro-morphological description—the leaves are hypostomatic, and the cuticles are quite thin; the upper epidermis is smooth, composed of mostly tetragonal and pentagonal, or slightly elongated cells, which are arranged in regular areolae (Fig. 5a); the cells are 12–36 μm (28 μm on average) in size, above the veins are rectangular, considerably elongated, up to 18–53 μm in length and 9–22 μm in width; areolas are well developed, 200–450 μm long by 180–300 μm wide; anticlinal walls are straight and moderately thick, periclinal walls are smooth and slightly concave (Fig. 6a); the lower epidermis also consists of isodiametric or slightly elongated cells about 11–35 μm in size; cells are arranged in areolae as in the upper epidermis (Figs. 5b, 6b); anticlinal walls are straight or rounded; stomata are randomly orientated, broadly elliptical or rounded in shape and variable in size (18–43 μm); stomatal pores are usually visible, sunken with kidney-shaped guard cells; stomatal type is anomocytic, surrounded by 5–8 cells, which are not distinctly different from the normal epidermal cells (Fig. 5b, c, 6b, c); stomatal rim is double-layered, mainly elliptic, rarely fusiform in shape, 8–25 μm long by 3–10 μm wide, its inner margin is smooth and moderately thick (Fig. 5g–i); T-pieces at the polar region of the guard cells are present and perfectly formed (Fig. 5h); trichome bases occur both adaxially and abaxially, girdled by a ring of radiating cells, about 15–35 μm in diameter, and rounded in shape (Fig. 6d, e).

Discussion

Comparison with extant species

The important characteristics of the fossils are the elliptical leaf shape, doubly serrulate leaf margin, stout primary vein, craspedodromous secondary veins, increasing angle of divergence of secondary veins basally, percurrent tertiary veins with well-developed areoles and absence of veinlets indicate their affinities with Carpinus. At first glance, leaves of Carpinus are similar to those of Ostrya, as indicated by Manchester and Crane (1987) who stated that some extant species of Ostrya, e.g., O. carpinifolia Scop., sometimes overlap in architecture with those of Carpinus. Likewise, it is difficult to distinguish some species of Carpinus from Betula. However, further studies show that the veinlets which are without exception present in Betula areoles rarely occur in Carpinus, while the external veins of Ostrya are much more developed than those of Carpinus (Liu 1996). Because of the absence of veinlets and external veins, the fossils should be assigned to Carpinus. Moreover, Carpinus has a double-layered stomatal rim, well developed T-pieces and usually no peltate glandular trichomes in cuticle, which is different from Betula and Ostrya (Chen and Zhang 1991). We also compared the leaf morphology of the fossils with those of 22 modern hornbeams (see Table 1). From the character-by-character comparison, it can be seen that the fossils show great resemblance to Carpinus, while the fossil leaves are commonly wider (4.9–8.3 cm) and have a smaller ratio of length to width (1.5–1.9) than that of modern species of Carpinus (mostly 2–5.5 cm wide, length to width ratio >2).
Table 1

Leaf morphological comparisons of Carpinustengchongensis with previous fossils and selected extant representatives of Carpinus

Species

Leaf shape

Size (cm)

L/W

Apex

Base

Margin

2nd veins

Fossil/extant

References

C. tengchongensis

Ovate-oblong or elliptic

7–13 × 4.9–8.3

1.5–1.9

Acuminate

Obliquely cordate

Irregularly and doubly minutely serrate

13–15

Fossil

Present paper

C. subcordata

Long ovate

3.1–11 × 1.9–4.9

1.7–2.9

Acuminate

Cordate or subcordate

Doubly serrate

14–20

Fossil

WGCPC (1978)

C. miofangiana

Ovate-lanceolate, lanceolate

6.7–11.3 × 3–4.7

2.1–3.5

Acuminate

Rounded or subcordate

Doubly serrate

15–20

Fossil

WGCPC (1978)

C. chaneyi

Long ovate

11 × 5.1

2.2

Caudate-acuminate

Rounded

Doubly serrate

11

Fossil

WGCPC (1978)

C. latifolia

Long ovate

8 × 4.2

1.9

Acuminate

Obliquely rounded

Simply serrate

9

Fossil

WGCPC (1978)

C. cf. lanceolata

Broadly lanceolate

4.7–9.7 × 1.7–2.7

2.7–3.6

Caudate-acuminate

Cuneate

Doubly serrate

9–12

Fossil

WGCPC (1978)

C. wulongensis

Elliptic to ovate-lanceolate

4–7 × 1.2–2.5

2.2–3.1

Acuminate

Rounded, subcordate

Doubly serrate

12

Fossil

Li and Guo (1976)

C. cf. fargesiana

Ovate- elliptic

5 × 2.8

1.5

Acuminate

Broadly cuneate

Doubly minutely serrate

13

Fossil

Tao and Du (1987)

C. grandis

Ovate or elliptic

6–7 × 3–4.7

1.5–2.4

Attenuate

Rounded or obtuse, rarely cordate

Doubly serrate

10–12

Fossil

Worobiec and Szynkiewicz (2007)

C. caroliniana

Oblong or ovate

2.8-5.2 × 1.3-3

1.7–2.6

Acuminate

Rounded or convex

Doubly serrate

12–15

Fossil

Stults and Axsmith (2009)

C. cordata

Ovate or ovate-oblong

8–15 × 4–5

1.9–3.2

Acuminate or caudate-acuminate

Unequaly cordate

Doubly setiform serrate

15–20

Extant

Li and Skvortsov (1999)

C. fangiana

Ovate-lanceolate or elliptic-lanceolate

6–27 × 2.5–8

2.3–4.5

Acuminate

Cordate, subrounded or cuneate

Doubly setiform serrate

24–34

Extant

Li and Skvortsov (1999)

C. tientaiensis

Ovate or elliptic

5–10 × 3–5.5

1.6–2.8

Acute

Subcordate or subrounded

Doubly and obtusely shortly serrate

12–15

Extant

Li and Skvortsov (1999)

C. londoniana

Elliptic-lanceolate, oblong or lanceolate

6–12 × 1.7–3.5

2.5–4.8

Acuminate or caudate-acuminate

Rounded-cuneate, cuneate, subrounded

Irregularly and doubly mucronate serrate

11–13

Extant

Li and Skvortsov (1999)

C. viminea

Elliptic, oblong or ovate-lanceolate

6–11 × 3–5

1.9–2.7

Acuminate, acute or caudate

Subcordate or subrounded

Doubly mucronate serrate

12–15

Extant

Li and Skvortsov (1999)

C. putoensis

Elliptic or broadly elliptic

5–10 × 3.5–5

1.7–2.5

Acuminate or acute

Rounded or broadly cuneate

Irregularly and doubly setiform serrate

11–14

Extant

Li and Skvortsov (1999)

C. kweichowensis

Elliptic, narrowly elliptic, oblong or narrowly oblong

8–12 × 3.5–5.5

2.3–3.1

Acuminate or acute

Subrounded or rounded-cuneate

Irregularly and doubly minutely serrate

10–16

Extant

Li and Skvortsov (1999)

C. turczaninowii

Ovate, ovate-elliptic, broadly ovate, or ovate-rhombic

2–6 × 1.3–4

1.6–2.5

Acute or acuminate

Subrounded, broadly cuneate or subcordate

Irregularly doubly serrate or simply serrate

8–12

Extant

Li and Skvortsov (1999)

C. kawakamii

Ovate-lanceolate or oblong-lanceolate

4–5 × 1.8–2.5

1.6–2.5

Acute or caudate acuminate

Subcordate or subrounded

Regularly and doubly serrate

10–15

Extant

Li and Skvortsov (1999)

C. tsaiana

Elliptic, oblong-lanceolate, oblong, or ovate-lanceolate

7–14 × 4.5–6

1.6–2.5

Acuminate

Obliquely cordate or cordate

Irregularly and doubly minutely serrate

14–16

Extant

Li and Skvortsov (1999)

C. chuniana

Elliptic, obovate-oblong or oblong

7–11 × 5–5.5

1. 5–2.1

Acute or acuminate

Cordate

Irregularly or regularly doubly minutely serrate

14–18

Extant

Li and Skvortsov (1999)

C. shensiensis

Oblong or obovate-oblong

6–9 × 3–4.5

1.6–2.7

Acute or acuminate

Cordate or subrounded

Regularly and doubly minutely serrate

14–16

Extant

Li and Skvortsov (1999)

C. pubescens

Oblong, oblong-lanceolate, ovate-lanceolate or elliptic

5–10 × 2–3.5

2.3–3.5

Acuminate

Subrounded-cuneate or subrounded

Regularly and doubly minutely serrate

12–14

Extant

Li and Skvortsov (1999)

C. monbeigiana

Oblong-lanceolate, ovate-lanceolate or elliptic

5–10 × 2.5–4

2.2–3.3

Acute, or caudate- acuminate

Rounded, subcordate or rounded-cuneate

Irregularly and doubly setiform serrate

14–18

Extant

Li and Skvortsov (1999)

C. fargesiana

Ovate-lanceolate, elliptic, ovate-elliptic or oblong

2.5–7.5 × 2–2.5

1.9–3.2

Acute or acuminate

Rounded or subcordate

Irregularly and doubly mucronate serrate

12–16

Extant

Li and Skvortsov (1999)

C. purpurinervis

Oblong-lanceolate, narrowly lanceolate or lanceolate

2–6 × 1–1.7

1.8–3.6

Acuminate

Subrounded or subcordate

Irregularly mucronate serrate

11–13

Extant

Li and Skvortsov (1999)

C. hebestroma

Lanceolate or ovate- lanceolate

5–5.5 × 1.4–1.8

3.2–3.9

Acuminate

Subrounded

Irregularly and simply serrate

11–12

Extant

Li and Skvortsov (1999)

C. tschonoskii

Elliptic, oblong or ovate- lanceolate

5–12 × 2.5–5

2.7–3.6

Acuminate or caudate- acuminate

Subrounded or subrounded-cuneate

Doubly setiform serrate

14–16

Extant

Li and Skvortsov (1999)

C. polyneura

Elliptic-lanceolate, oblong- lanceolate or lanceolate

4–8 × 1.5–2.5

2.8–4.1

Acuminate

Broadly cuneate or subrounded

Doubly and regularly setiform serrate

16–20

Extant

Li and Skvortsov (1999)

C. mollicoma

Oblong-lanceolate or elliptic-lanceolate

5–6.5 × 2–2.5

2.5–3.2

Acuminate or caudate- acuminate

Rounded or rounded-cuneate

Irregularly recurved setiform serrate

14–17

Extant

Li and Skvortsov (1999)

C. omeiensis

Elliptic or ovate-elliptic

6–8 × 2.5–3.5

2.6–3.5

Acuminate or caudate- acuminate

Rounded or broadly cuneate

Simply setiform serrate

12–16

Extant

Li and Skvortsov (1999)

C. rupestris

Oblong-lanceolate or lanceolate

4–5 × 1.5–2

2.3–3

Acuminate

Subrounded or broadly cuneate

Minutely simply setiform serrate

14–17

Extant

Li and Skvortsov (1999)

According to the detailed comparison (Table 1), the present fossils most resemble Carpinus kweichowensis Hu, Carpinus tsaiana Hu, Carpinus monbeigiana Hand.-Mazz., Carpinus pubescens Burk. of sect. Carpinus and Carpinus cordata Blume of sect. Distegocarpus. They all show similar size, have a ovate-oblong or elliptic leaf shape, acuminate apex, obliquely cordate base, irregularly and doubly minutely serrulate margin, and their secondary veins are generally 12–16 except for C. cordata (15–20). We examined the epidermal anatomy of the above five modern species of sect. Carpinus and sect. Distegocarpus. In combination with cuticular data of Chen and Zhang (1991), we confirm that the stomatal rim of Carpinus is uniformly double-layered (Figs. 5g–l, 6c, h, k, 7d, h, l), and the epidermal cells are arranged in regular areolae adaxially (Figs. 6a, f, i, 7a, e, i) with some variations in epidermal anatomy, including the trichomes, cell shape, stomatal type, and undulation of the anticlinal walls. Unicellular acicular trichomes (bases) appear in all of the above species (Figs. 6e, g, l, 7c, f, j). Peltate glandular trichomes are present in C. cordata Blume (Fig. 6h) but are absent from the species of sect. Carpinus, which is somewhat incompatible with the previous statement that peltate glandular trichomes are lacking in Carpinus (Hardin and Bell 1986). In addition, C. cordata differs from the fossils in having brachyparacytic stomata and deeply undulate anticlinal walls abaxially (Fig. 6: G, H). Carpinus tsaiana Hu is very similar to C. tengchongensis except that its lower epidermal cells are a little bigger and its anticlinal walls are more undulate (Figs. 5e, f, 6k). Carpinus monbeigiana Hand.-Mazz. has moderately undulate anticlinal walls and multicellular trichome bases abaxially (Fig. 7b), and striate periclinal walls (Fig. 7a, d). C. kweichowensis Hu is characterized for intensely undulate anticlinal walls abaxially (Fig. 7g, h). C. pubescens Burk. has brachyparacytic stomata, and straight, rounded or weakly undulate anticlinal walls abaxially (Fig. 7k, l). According to Chen and Zhang (1991) Carpinus turczaninowii Hance and Carpinuspolyneura Franch. have brachyparacytic stomata and moderately undulate anticlinal walls abaxially; Carpinus tschonoskii Maxim. has intensely undulate anticlinal walls abaxially; Carpinus viminea Wall. shows undulate-striate cuticular membrane abaxially. Considering all these details, Carpinus tsaiana Hu displays the closest resemblance to C. tengchongensis.
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Fig. 7

Cuticular features of Carpinusmonbeigiana Hand.-Mazz., Carpinuskweichowensis Hu and Carpinuspubescens Burk. under light microscopy, a, c, e, g, iscale bars = 50 μm, b, d, f, h, j, kscale bars = 25 μm, lscale bar = 10 μm. a Upper epidermis of Carpinusmonbeigiana,b multicellular trichome of Carpinusmonbeigiana,c lower epidermis of Carpinusmonbeigiana, showing an acicular trichome, d lower epidermis of Carpinusmonbeigiana, showing the striate epidermal cells, e upper epidermis of Carpinuskweichowensis,f trichome base of Carpinuskweichowensis,g lower epidermis of Carpinuskweichowensis,h lower epidermis of Carpinuskweichowensis, showing the intensely undulate anticlinal walls and double-layered stomatal rim, i upper epidermis of Carpinuspubescens,j trichome base of Carpinuspubescens,k lower epidermis of Carpinuspubescens,l Brachyparacytic stomata of Carpinuspubescens, showing the double-layered stomatal rim

Moreover, the fossils have bigger stomata (18–43 μm, average 34 μm) than the selected modern species (average 25–30 μm). The enlargement of stomatal dimensions frequently results from increasing ploidy levels in plants (Masterson 1994; Mishra 1997), and the relevance of stomatal dimensions for species determination has been demonstrated for some species of Betula (Wagner et al. 2000). To what extent the stomatal dimensions can be used for species identification in Carpinus is uncertain. Be this as it may, the stomatal length can be used as a criterion to distinguish the Tengchong taxon from the modern comparable species.

Comparison with previously described fossil leaves

The generic affinity of the Paleocene leaf Carpinus sp. from Xinjiang, northwest China, is debatable (Liu 1992) because no confirmed involucre or fruits of Carpinus have been found before the Eocene (Crane 1989; Pigg and Manchester 2003). This Xinjiang species has been considered as Alnus by Li (1985) because of its very well-developed external veins. The Oligocene Carpinus-like leaves associated with the extinct Asterocarpinus fruits from the John Day Formation of western North America, were formerly assigned to Carpinus (Chaney 1927). Later Manchester and Crane (1987) replaced them by a new genus Paracarpinus because of their consistent co-occurrence with Asterocarpinus. These leaves are typically smaller (2–8 × 1.3–4.2 cm) than the Tengchong taxon, and their secondary veins are straight, rather than slightly curved upwards.

Confirmed Carpinus leaves from the Eocene to Pliocene of China have been extensively described, for example C.subcordata Nathorst, C.miofangiana Hu et Chaney, C.chaneyi Tanai et Suzuki and C. cf. lanceolata Hand.-Mazz. from the Miocene of Shandong Province, east China (Hu and Chaney 1940); C. latifolia Li from the Eocene of Liaoning Province, northeast China (WGCPC 1978), C. wulongensis Li et Guo from the Miocene of Xizang, southwest China (Li and Guo 1976;) as comprehensively reviewed by Liu (1996). However, work on cuticular analysis has only been undertaken recently (Sun et al. 2003; Dai et al. 2009). We compared these published species to our specimens in leaf morphology (Table 1). As shown in Table 1, the present fossils differ from these species in leaf shape, size, number of secondary veins, and details of serrulation.

The European species Carpinus grandis Unger emend. Heer, is well known in the Cenozoic floras of Europe and Asia from the middle Oligocene to early Pliocene (Heer 1857; Li and Guo 1976; Mai 1981; Mai and Walther 1988, 1991; Hummel 1991; Zastawniak and Walther 1998; Worobiec and Szynkiewicz 2007). Carpinus grandis is most probably a collective species including several morphotypes of fossil leaves (Heer 1857). Leaves of C. grandis are elliptic or oblong-ovate, with acute, obtuse or rounded, rarely cordate base, 10–12 pairs of secondary veins, while the present taxon has a cordate base and 13–15 pairs of secondary veins. C. grandis has almost rounded or minutely undulate anticlinal walls and at most imperfectly formed T-pieces, as opposed to the straight anticlinal cell walls and well-developed T-pieces in C. tengchongensis.

Recently, Stults and Axsmith (2009) assigned some mid-Pliocene and Pleistocene fossil material, including leaves and nutlet bracts from the eastern US to an extant species Carpinus caroliniana Walter, the American hornbeam, which is native to the Atlantic and Gulf Coastal Plains of southeastern United States (Thompson et al. 1999). However, the leaves of C. caroliniana are easily distinguishable from the present species by their rounded or convex base and smaller lamina.

Several distinct species of nuts and involucres of Carpinus have been described from the Cenozoic of Asia, Europe and North America (e.g., Axelrod 1944; Chandler 1963; Mai 1995; Ozaki 1991; Uemura and Tanai 1993; Liu 2000). The description of a new species of Carpinus based upon leaves alone is sometimes problematical (Mai and Walther 1978; Stults and Axsmith 2009). However, based upon the detailed comparisons given above (see also Tables 1, 2), it is concluded that the unique combination of leaf architecture and cuticular features of the present fossils represents a new species Carpinustengchongensis Dai et B.N. Sun, sp. nov.
Table 2

Cuticular comparisons of Carpinustengchongensis with selected fossil and extant representatives of Carpinus

Species

Epidermal cells

(μm)

Areola (μm)

Pattern of anticlinal walls

Stomatal type

Stomatal length (μm)

Stomatal ledge

Trichomes (bases)

Fossil/extant

References

Upper epidermis

Lower epidermis

C. tengchongensis

Tetragonal or pentagonal, 11–36

200–450

Straight

Straight or rounded

Anomocytic

18–43

Elliptic, double-layered

Present abaxially and adaxially

Fossil

Present paper

C. grandis

Isodiametric or elongated, 17.2–46.7

200–300

Rounded or straight

Rounded or minute-undulate

Anomocytic

14.5–36.9

Elliptic or fusiform

Unicellular, present abaxially

Fossil

Worobiec and Szynkiewicz 2007)

C. cordata

Tetragonal, polygon or elongated, 8–26

100–360

Straight or rounded

Weakly undulate or rounded

Brachyparacytic

10–22

Elliptic or fusiform, double-layered

Peltate and acicular trichomes

Extant

Present paper

C. tsaiana

Tetragonal or pentagonal, 12–43

200–470

Straight or weakly undulate

Moderate undulate or straight

Anomocytic

16–40

Elliptic, double-layered

Unicellular

Extant

Present paper

C. kweichowensis

Isodiametric or polygon, 12–45

180–450

Deeply undulate or straight

Intense undulate

Anomocytic

18–37

Narrowly elliptic, double-layered

Unicellular

Extant

Present paper

C. monbeigiana

Isodiametric and striate, 18–36

170–340

Straight or rounded

Moderate undulate

Anomocytic

14–32

Elliptic or fusiform, double-layered

Multicellular and acicular trichomes

Extant

Present paper

C. pubescens

Isodiametric or elongated, 18–45

200–350

Straight

Straight or rounded

Brachyparacytic

16–34

Narrowly elliptic, double-layered

Unicellular

Extant

Present paper

C. turczaninowii

Tetragonal or elongated

Unknown

Straight or weakly undulate

Straight, rounded, or weakly undulate

Brachyparacytic

15–36

Elliptic, double-layered

Unknown

Extant

Chen and Zhang (1991)

C. polyneura

Pentagonal or elongated

Unknown

Unknown

Moderate undulate

Brachyparacytic

14–33

Elliptic or fusiform, double-layered

Unknown

Extant

Chen and Zhang (1991)

C. tschonoskii

Pentagonal or polygon

Unknown

Unknown

Intense undulate

Anomocytic

15–37

Elliptic or fusiform, double-layered

Unknown

Extant

Chen and Zhang (1991)

C. viminea

Pentagonal or polygon and striate

Unknown

Unknown

Moderate undulate

Anomocytic

16–39

Elliptic, double-layered

Unknown

Extant

Chen and Zhang (1991)

Biogeographic implication

Carpinus has been living under a subtropical or warm temperature climatic regime (in North Hemisphere) throughout its geological history (Wolfe 1978, 1979; Guo 1990; Chen 1994). Cenozoic records in the North Temperate Zone broadly reflect its present-day distribution pattern (Yoo and Wen 2007; Fig. 1). Its extant distribution is not distinctly reduced compared with that of the past, which probably demonstrates the tolerance of Carpinus to environmental change. The morphological evolution by environmental selection also reflects the adaptability of the genus (Chen 1994). In contrast to the abundant records during the Miocene, poor records of Carpinus in the Pliocene are anomalous. However, the common presence of Carpinus in the Tengchong flora, with representatives of the sections Distegocarpus and Carpinus (Sun et al. 2003; Tao and Du 1982), indicates the importance and diversity of hornbeam in the late Pliocene of western Yunnan. It is concluded that the mean annual temperature of Pliocene in western Yunnan was similar to that of the present (Xu et al. 2008; Wu et al. 2009), i.e. suitable for the growth of Carpinus. Although the climate is known to have fluctuated wildly since the Pliocene, especially during the glacial periods in the Pleistocene, Carpinus could migrate to lower altitudes along the deep gorges during the cold periods and thus escape the cold. Moreover, the major rivers in Yunnan all flow roughly N–S, which would allow the plants to escape southwards during the glacial periods, and reimmigrate during the interglacials and the Holocene.

Acknowledgments

We are deeply grateful to Dr. Ferguson for revising the manuscript. We are also grateful to Dr. Xiao Liang for comments and discussion, Dr. Su Tao from Kunming Institute of Botany, Chinese Academy of Sciences for collecting comparative material. This research is supported by the the National Basic Research Program of China (973 Program) (No. 2012CB822000), the National Natural Science Foundation of China (No. 41172022; No. 41202001), Specialized Research Fund for the Doctoral Program of Higher Education (Grant No. 20100211110019), Science and Technology Research Project of Chongqing Education Committee (No. KJ121406).

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