Miocene Smilax leaves and associated epiphyllous fungi from Zhejiang, East China and their paleoecological implications

Review of Palaeobotany and Palynology 165 (2011) 209–223

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Research paper

Miocene Smilax leaves and associated epiphyllous fungi from Zhejiang, East China and their paleoecological implications Su-Ting Ding a,b, Bai-Nian Sun a,b,⁎, Jing-Yu Wu a,b, Xiang-Chuan Li a a b

Key Laboratory of Western China's Environmental Systems of Ministry of Education, and College of Earth and Environmental Sciences, Lanzhou University, Lanzhou 730000, China State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, CAS, Nanjing 210008, China

a r t i c l e

i n f o

Article history: Received 12 November 2010 Received in revised form 16 March 2011 Accepted 21 March 2011 Available online 25 March 2011 Keywords: Smilax cuticle epiphyllous fungi Miocene East China

a b s t r a c t Smilax tiantaiensis sp. nov. is described from the Late Miocene Shenxian Formation in Zhejiang Province, East China based on five fossil leaves with fine venation and well preserved cuticles. The fossil leaves are characterized by an ovate shape, entire margin, mucronate apex, rounded base, five primary basal acrodromous veins with reticulate venation in between; leaves hypostomatic, anticlinal walls undulated and stomatal apparatus anomocytic. The fossils have been compared with extant and other fossil species hitherto described in this genus. Some fossil stromata, hyphae and spores identified as Callimothallus pertusus Dilcher (Microthyriaceae) were discovered on the both epidermides of S. tiantaiensis. The climbing habit of Smilax and the presence of the epiphyllous fungus of C. pertusus on the fossil leaves may indicate that the multistratified forest was growing under a humid climate during the Miocene in Zhejiang. © 2011 Elsevier B.V. All rights reserved.

1. Introduction The leaves of Smilacaceae are atypical of monocotyledons in being reticulate between the acrodromous major veins (Inamdar et al., 1983). The family has a generally ‘woody’ climbing habit and was found throughout the world (Holmes, 2002; Cameron and Fu, 2006). Smilacaceae is closely related to and sometimes included in Liliaceae, but most botanists have accepted Smilacaceae as a distinct family for the past thirty years (Hutchinson, 1973; Cronquist, 1981; Dahlgren et al., 1985). Traditionally, Smilacaceae contains three genera: Ripogonum, Heterosmilax and Smilax (Cameron and Fu, 2000). Ripogonum contains six species that occur in eastern Australia, New Guinea and New Zealand (Conran and Clifford, 1985), but the genus has been considered to be an independent family, viz. Ripogonaceae based on the molecular data (Davis et al., 2004; Cameron and Fu, 2006; Chase et al., 2006) and the morphological data (Chen et al., 2006a, 2006b). Smilax is a core genus of the family Smilacaceae with ca. 200 species (Cameron and Fu, 2006) which are distributed in the tropics to subtropics and a few temperate regions, but it is most diverse in East Asia, North America and Central America (Holmes, 2002; Chen et al., 2006a). The earliest Smilax-like fossil leaf was reported from the Late Cretaceous of North America (Bews, 1927) and Northeast Russia

⁎ Corresponding author at: Key Laboratory of Western China's Environmental Systems of Ministry of Education, and College of Earth and Environmental Sciences, Lanzhou University, Lanzhou 730000, China. Tel./fax: + 86 931 8915280. E-mail address: [email protected] (B.-N. Sun). 0034-6667/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.revpalbo.2011.03.004

(Craggs, 2005). In China, reliable fossil records of Smilax have been found from the Paleocene of Henan (Tao et al., 2000), the Eocene of Guangxi (Feng et al., 1977), the Miocene of Yunnan (Tao et al., 2000), the Pliocene of Sichuan (Tao et al., 2000) and the Pleistocene of Guangxi (Liu, 1993). The fossil occurrences of Smilax are frequent in the Cenozoic, but the cuticular investigation of this genus is absent except for Liu (1993) who reported the cuticle features of a Pleistocene leaf from Guangxi, China. In the present study, five fossil leaves from the Late Miocene of China are identified as a new species Smilax tiantaiensis sp. nov. based on a detailed comparison of leaf architecture and cuticular features with those of extant and fossil leaves of Smilacaceae. 2. Materials and methods The fossils described here were collected from the laminated lacustrine sediments at Jiahu Village, Tiantai County, Zhejiang Province, East China (29°09′N, 121°14′E, Fig. 1). Previous studies generally recognized the fossiliferous horizons in the same locality as Xiananshan Formation (e.g. Li, 1984), but later changes to Shengxian Formation (BGMRZP, 1996). The age of the Shengxian Formation is regarded as Late Miocene based on lithostratigraphy and biostratigraphy (Li and Guo, 1982; Li, 1984; BGMRZP, 1989; Liu et al., 1992, 2007, 2008; Li et al., 2010). We performed an exhaustive comparison of the fossils with collections of the extant Smilacaceae in the Institute of Botany, the Chinese Academy of Sciences Herbarium; Kunming Institute of Botany, the Chinese Academy of Sciences Herbarium; Zhejiang University Herbarium, China. The living leaves for cuticular

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Fig. 1. Locality of Smilax fossils in Zhejiang Province, China.

comparisons were collected from the Botanical Garden of Zhejiang University, the Hangzhou Botanical Garden, the Kunming Botanical Garden and Western Hills (Xi Shan) of Kunming, Yunnan Province. The information of partial characters was taken from the literatures (e.g. Chen et al., 2000). Since there is no general consensus on the venation terminology of monocotyledons, we employ the descriptive terms for Smilacaceae foliage as introduced and defined by Conover (1983), while terms on foliar cuticle are after Dilcher (1974) and Conover (1991). The experimental treatments for the fossil and extant cuticles were well described in previous studies (Wu et al., 2009; Li et al., 2010). All specimens, microscope cuticle slides and the stubs for SEM are stored in the Institute of Palaeontology and Stratigraphy, Lanzhou University, Gansu Province, China.

3. Results 3.1. Systematic description Order: Liliales Perleb Family: Smilacaceae Vent. Genus: Smilax L. Species: Smilax tiantaiensis Su-Ting Ding et Bai-Nian Sun sp. nov. Holotype: JH-1-4-428(A, B) (Plate I, 1a and 1b, 6–7; Plate II, 3, 6). Paratype: JH-1-3-004 (Plate I, 2; Plate II, 4–5), JH-1-4-904 (Plate I, 3), JH-1-3-947(A, B) (Plate I, 4a, 4b and 4c, 8–9; Plate II, 1–2), JH-1-4-526 (Plate I, 5). Type locality: Tiantai County, Zhejiang Province, China (Fig. 1). Stratigraphy: Shenxian Formation

Plate I. Smilax tiantaiensis sp. nov. 1–5. 1a. 1b. 2. 3. 4a. 4b. 4c. 5. 6. 7. 8. 9.

Leaf morphology. Scale bar = 1 cm. Specimen no. JH-1-4-428A. Specimen no. JH-1-4-428B. Specimen no. JH-1-3-004. Specimen no. JH-1-4-904. Specimen no. JH-1-3-947A. Specimen no. JH-1-3-947B. Specimen no. JH-1-3-947B. Detailed cross veins and veinlets, notice the acrodromous venation. Specimen no. JH-1-4-526. 6–9. Cuticular structures under the light microscopy. Adaxial epidermis of specimen no. JH-1-4-428A. Scale bar = 50 μm. Abaxial epidermis of specimen no. JH-1-4-428A. Scale bar = 200 μm. Abaxial epidermis of specimen no. JH-1-3-947B. Scale bar = 500 μm. Abaxial epidermis of specimen no. JH-1-3-947B. Scale bar = 10 μm.

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Plate II. Cuticular structures of Smilax tiantaiensis sp. nov. under the SEM. 1. 2. 3. 4, 5. 6.

Outer surface of adaxial epidermis, specimen no. JH-1-3-947B. Scale bar = 50 μm. Outer surface of abaxial epidermis, specimen no. JH-1-3-947B. Scale bar = 50 μm. Inner surface of abaxial epidermis, specimen no. JH-1-4-428A. Scale bar = 50 μm. Outer surface of stomatal apparatus, specimen no. JH-1-3-004. Scale bar = 5 μm. Inner surface of stomatal apparatus, specimen no. JH-1-4-428A. Scale bar = 5 μm.

Age: Late Miocene Etymology: The specific epithet, tiantaiensis is derived from the fossil source in Tiantai County.

Diagnosis: Leaves ovate, apex mucronate, base rounded, margin entire; primary veins basal acrodromous, the lower order of venation reticulate between primary veins; leaves hypostomatic,

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epidermis cells irregular with undulated anticlinal walls; stomata anomocytic. 3.2. Description 3.2.1. Morphological characteristics of fossil leaves (Plate I, 1–5) Lamina ovate, symmetrical, 1.9 to 5.3 cm long, 1.3 to 3.3 cm wide, margin entire, apex mucronate or acute, base rounded, petiole 0.8 mm thick and 1.7 mm long (Plate I, 3). Five acrodromous primary veins originate from the base at the attachment of petiole (Plate I, 1a, 1b, 2); the medial primary vein is straight, conspicuous, stout and slightly thicker than the lateral primary veins; the first pair of lateral primary veins depart midvein at 35°–45° angles, arching in an acrodromous pattern about 1/3 the distance between the midvein and leaf margin basally and closer to the margin near the apex; the second pair of lateral primary veins depart midvein at 55°–65° angles and extending 1/2 the leaf length near the leaf margin, curved arches and join at the apex. Secondary viens are pinnate, mixed opposite, alternate percurrent and arise the primary veins at 50°–70° angles (Plate I, 1– 5). Tertiary and higher-order veins usually link the secondary veins to form a reticulate pattern. The free ending ultimate veins are unbranched and the areoles are irregular in shape and size (Plate I, 1a, 1b, 3, 4b, and 4c). 3.2.2. Anatomical characteristics of fossil leaves (Plate I, 6–9; Plate II) The adaxial epidermal cells are irregular in shape, 22–64 μm long and 17–33 μm wide, the anticlinal walls are sinuate (Plate I, 6) and the periclinal walls are rugged (Plate II, 1). The abaxial epidermis is very delicate and thin, almost hyaline, the epidermis cells are somewhat elongate with irregular shape (Plate I, 7–9), the anticlinal walls are mixed concave, convex or slightly sinuous, the periclinal walls are punctate on the inner surfaces (Plate I, 8; Plate II, 2–3). Trichomes or glands are not observed on both adaxial and abaxial epidermis. Leaf hypostomatic. Stomata are distributed randomly and scattered in leaf epidermis, 20–35 μm long and 13–18 μm wide (Plate I, 8, 9; Plate II, 2–6). The type of stomatal apparatus is anomocytic, the guard cells generally surrounded by four or sometimes three contact cells that resemble the normal epidermal cells (Plate I, 8), the pair of ridge–arcs flanking the stomata is prominent (Plate I, 7–8, Plate II, 2–3, 6). 3.3. Comparison The fossil leaves possess ovate shape, entire margin, acrodromous primary veins with reticulate venation between and stomatal apparatus anomocytic. The leaf architectural features of present fossil leaves are common for some monocot plants, especially for the Liliiflorae (Cronquist, 1981; Dahlgren et al., 1985). The families outside the Liliiflorae such as Alismataceae, Aponogetonaceae, Hydrocharitaceae and Araceae have paracytic, tetracytic or hexacytic stomata (Tomlinson, 1982; Inamdar et al., 1983; Dahlgren et al., 1985; Conran et al., 1994), but these types are absent in our fossils. Among the Liliiflorae, reticulate-veined leaves are characteristic of the

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families Trichopodaceae, Dioscoreaceae, Taccacceae, Stemonaceae, Trilliaceae, Smilacaceae, Ripogonaceae, Petermanniaceae, Philesiaceae and Luzuriagaceae (Conover, 1983, 1991). A detailed comparison of leaf architecture and cuticle between the current fossils and the possible extant and fossil similar-looking net-veined Liliiflorae is listed in Table 1. Petermannia (Petermanniaceae) species have axially elongated epidermal cells, with stomata parallel to the leaf long axis (Conran et al., 2009). Philesia and Lapageria (Philesiaceae) have stomata oriented perpendicular to the leaf axis (Conran and Clifford, 1985; Conover, 1991). Ripogonum (Ripogonaceae) species possess prominent suprabasal second pair of lateral primary veins arising from the midrib (Conran et al., 2009), and their cuticles tend to have stronger or clearly defined epidermal cell and regularly U-shaped sinuosities on the epidermal cells with paracytic or brachyparacytic stomata (Pole, 2007; Conran et al., 2009). The fossil genus Petermanniopsis (Petermanniaceae) also possesses basally divergent lateral primary veins (Conran et al., 2009), but the stomata of Petermanniopsis are brachyparacytic and amphibrachyparacytic (Conran and Christophel, 1999) which can be distinguished from the anomocytic stomata in the present fossil leaves. The general shape, margin, and prominent basal acrodromous venation of the present fossil leaves are similar to those of Smilacaceae and Dioscoreaceae (especially to the genus Dioscorea). However, the secondary venation in the leaves of Dioscorea is distinctly opposite percurrent (Conover, 1991; Ding and Gilbert, 2000; Raz, 2002), which is different from the mixed opposite and alternate percurrent secondary veins in the fossils. It is clear that the combination of these features warrants the classification of the fossil leaves to Smilacaceae. 3.3.1. Comparison with extant species Smilacaceae contains two genera, Heterosmilax and Smilax within the APG II (2003) system. However, Cameron and Fu (2006) nested the species of Heterosmilax within the genus Smilax, and treated Smilacaceae as a monogeneric family based on the ITS phylogenic tree. Traditionally, the leaf blades of Heterosmilax usually possess broad-ovate or oblonglanceolate shape with cordate base (Chen et al., 2000), but our fossils are ovate in shape with rounded base. Moreover, Heterosmilax has bigger leaf size, bigger epidermal cell size and stronger epidermal cell anticlinal walls (Plate III, 14; Plate V, 14–15; Plate VI, 14–15; Table 2) than those of our fossils. Koyama (1960) proposed a classification of six sections in Smilax, viz. sect. China T. Koyama, sect. Coprosmanthus Torrey, sect. Coilanthus A. DC., sect. Macranthae Kunth, sect. Smilax T. Koyama and sect. Pleiosmilax (Seeman) A.DC. The first five sections are distributed in China, but the sect. Pleiosmilax which contains two species is only distributed in the Pacific Ocean islands. We have compared the morphology of our fossils with that of Chinese extant Smilax (Plate III, 1–13); the results show that some species, such as S. china, S. davidiana, S. glaucochina, S. cyclophylla and S. stans (Plate III, 1, 4, 5, 8, and 10) have similar laminas with the present fossils. According to cuticular comparisons (Plate IV, 1–15; Plate V, 1–13; Plate VI, 1–13; Table 2), we found there are more or less differences between the

Table 1 Comparison of Smilax tiantaiensis sp. nov. (Smti) with possible extant and fossil relatives or similar-looking net-veined monocots (partly referred to Conran et al. (2009)). Character

Smti

Smil

Ripo

Phil

Lapa

Pete

Pets

Dios

Primary vein number Venation acrodromous A second pair of lateral primary veins suprabasal Secondary vein course pinnate Marginal veins dicraeoid externally Sinuous anticlinal walls Adaxial anticlinal sinuosity strong Stomata unoriented Stomata anomocytic

5 Yes No Yes No Yes No Yes Yes

3–7 Yes No Yes No Yes No Yes Yes

5 Yes Yes Yes No Yes Yes Yes No

3 Yes No Yes No No No No No

3 Yes No Yes No Yes No No Yes

5–7 Yes No No No Yes No No Yes

5 Yes No No Yes No No No No

3–9 Yes No Yes No No No Yes Yes

Notes: Smil—Smilacaceae; Ripo—Ripogonaceae; Phil—Philesia; Lapa—Lapageria; Pete—Petermannia; Pets—Petermanniopsis; Dios—Dioscorea.

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Table 2 Cuticular comparison of Smilax tiantaiensis sp. nov. with extant representatives in Smilacaceae. Sample no.

LUP–080052 LUP–080053 LUP–080054 LUP–080055 LUP–080056 LUP–080057 LUP–080058 LUP–080059 LUP–080060 LUP–080061 LUP–080062 LUP–080063 LUP–080064 LUP–080065 LUP–080066 LUP–080067 LUP–080068 LUP–080069 LUP–080070 LUP–080071 LUP–080072 LUP–080081 LUP–080082

Genus/section

Smilax Sect. China

Sect. Coprosmanthus Sect. Coilanthus

Sect. Macranthus

Sect. Smilax Heterosmilax

Species

S. tiantaiensis S. china S. glaucochina S. davidiana S. trinervula S. lebrunii S. ferox S. scobinicaulis S. sieboldii S. riparia S. tsinchengshanensis S. stans S. arisanensis S. glabra S. cyclophylla S. hayatae S. corbularia S. darrisii S. perfoliata S. lanceifolia S. ocreata S. elegantissima H. yunnanensis H. japonica

Adaxial epidermis

Abaxial epidermis

Stomata

UI

CD (n/mm2)

UI

CD (/mm2)

L (μm)

W (μm)

PL (μm)

SD (n/mm2)

1.19–1.59 1.28–1.46 1.45–1.54 1.27–1.45 1.32–1.53 1.21–1.61 1.24–1.47 1.21–1.49 1.43–1.52 1.15–1.33 1.55–1.7 1.20–1.31 1.24–1.36 1.36–1.75 1.59–1.91 1.2–1.35 1.22–1.44 1.09–1.26 1.14–1.24 1.59–2.12 1.19–1.3 1.21–1.33 1.16–1.46 1.43–1.77

1092 428 1247 1364 460 535 391 516 478 345 456 1699 806 374 854 720 998 333 591 361 633 780 402 457

1.10–1.47 1.41–1.72 1.57–1.85 1.31–1.52 1.29–1.62 1.10–1.52 1.18–1.41 1.28–1.53 1.25–1.56 1.31–1.48 1.57–2.12 1.24–1.32 1.24–1.73 1.32–1.75 1.6–1.91 1.21–1.44 1.17–1.28 1.27–1.58 1.41–1.89 1.93–2.49 1.21–1.40 1.20–1.48 1.33–1.65 1.42–1.98

1098 321 1407 1675 615 537 540 618 889 957 346 1589 1203 548 810 1190 880 361 1497 492 768 645 556 503

18.3–29.2 28.7–33.5 19.3–27.3 16.5–25.1 17.5–26.3 27.4–30.9 27.3–35.1 22.5–26.0 22.3–32.0 22.3–31.24 20.2–26.4 22–25 25.5–33.4 23.3–32.8 22.4–28.5 23.3–25.9 20.2–22.5 30.4–38.1 13.4–24.2 25.0–28.0 19.4–24.7 31.4–36.7 33.1–36.2 23.8–26.9

15.8–21.2 30.9–32.9 17–23.9 10–16.4 14.9–28.6 23.8–28.0 19.6–29.7 21.6–26.6 23.1–35.5 16.7–23.3 19.2–24.0 14–20 21.9–26.1 20.3–31.3 21.0–24.8 20.1–23.1 11.4–13.3 28.1–30.2 17.7–24 22.1–25.2 19.6–22.3 25.6–27.1 33.8–36.0 21.7–25.1

9.8–22.2 16.6–22.8 12.4–20.6 8.7–12.7 11.4–17.8 17.8–21.7 15.0–22.8 13.1–17.8 12.3–20.1 11.8–15.5 10.5–13.2 5.2–6.4 15.6–19.9 15.1–22.5 12.5–18.1 14.6–17.4 8.8–11.3 18.2–22.3 6.8–12.6 13.2–18.3 11.5–14.3 12.2–19.5 16.5–24.5 16.2–19.3

242 61 216 300 176 94 161 152 98 107 83 158 340 148 145 179 184 101 206 62 157 119 56 99

Notes: UI—undulation index, CD—cell density, SD—stomatal density, L—length, W—width, PL—pore length.

cuticles of the extant species on epidermal cell density, stomatal density and undulated degree of anticlinal walls (undulation index, UI) [refer to Kürschner (1997)] with our fossils. However, the cuticles of most species of Smilax have the same or similar epidermal cell shape, stomatal apparatus type and numbers of stomatal contact cells. 3.3.2. Comparison with fossil species Reliable fossil records of Smilax frequently occurred in the whole Cenozoic in the northern hemisphere (Table 3). The leaves from the Paleocene of Henan (Tao et al., 2000) and Eocene of Guangxi in China (Feng et al., 1977) possess three primary veins, which are different from the five primary veins in present fossils. The Eocene leaf from Wyoming, North America was identified as aff. Smilax has a cordate base and 7 primary veins (Berry, 1929a). The Tennessee specimens (Dilcher and Lott, 2005) have larger sizes (6.5 × 3.8 cm and 8.5 × 6.2 cm) than our fossils. There are two species discovered from the Middle Eocene of Csordakút (Hungary), but one species has a slightly emarginate apex and another has lanceolate shape and asymmetric leaf base (Erdei and Rákosi, 2009). The Oligocene leaf of S. labidurommae from Colorado of North America has a cordate base (MacGinitie, 1953). The Miocene records, such as the leaves from Idaho (Berry, 1930) and Washington (Berry, 1929b) of North America and Ankara of Turkey (Kasapligil, 1977) have cordate or truncate bases, the Yunnan specimen (Tao et al., 2000) possesses only three Plate III. Leaf morphology of extant Smilacaceae. Scale bar = 1 cm. 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.

Smilax china. S. ferox. S. trachypoda. S. davidiana. S. glaucochina. S. sieboldii. S. riparia. S. cyclophylla. S. corbularia. S. stans. S. glabra. S. ocreata. S. hayatae. Heterosmilax japonica.

primary veins, the Romanian specimen (Macovei and Givulescu, 2006) has a triangular shape, and the Iceland specimen (Denk et al., 2005) was preserved imperfectly. After the Miocene, the fossil records of Smilax are limited in East Asia. The Pliocene specimen from Sichuan (Tao et al., 2000) and the Early Pleistocene specimen from Guangxi (Liu, 1993) in China have prominent cuneate bases. The Late Pleistocene leaves from Fukushima Prefecture of Japan (Suzuki and Nakagawa, 1971) were partly preserved and have cuneate or cordate bases. While fossil occurrences of Smilax are frequent in the Cenozoic, cuticular preservation and investigation are rare. Liu (1993) reported a leaf with epidermal cell and stomatal features suggesting a close affinity with the cuticles of Smilax. As most of the Smilax records lack cuticles, a further comparison appears to be limited. A detailed comparison of the fossils and related extant representatives suggests that none of previously mentioned fossils, as well as any extant species, have concordant leaf architectural and cuticular characters similar to our fossil leaves, which further supports that the present fossils represent a new species. 4. Associated epiphyllous fungi Family: Microthyriaceae Saccardo Genus: Callimothallus Dilcher

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Type species: Callimothallus pertusus Dilcher Species: Callimothallus pertusus Dilcher (Plate VII) Selected synonymous list 1965 callimothallus pertusus, Dilcher, p. 13–16, pl. 5, figs. 37–42; pl. 6, figs. 43–46; pl. 7, figs. 47–55. 1975 Callimothallus pertusus, Selkirk p. 83–84, pl. VI, figs.1–2. 1976 Callimothallus pertusus, Jansonius (1976), p. 131, pl. 1, fig. 22. 1978 Callimothallus pertusus, Lange (1978), p. 532, figs. 3, 4, 6. 1989 Callimothallus pertusus, Phadtare, p. 128, figs. 1–3. 1997 Callimothallus pertusus, Kalgutkar (1997), p. 222, pl. 1, fig. 7. 2010 Callimothallus pertusus, Shi, Zhou & Xie, p. 191–194, pl. VI, Figs.1–6. 4.1. Description Stromata occur on the leaves of S. tiantainsis, but most frequently present on the adaxial surface (Plate VII, 1, 2). They are distributed irregularly, sometimes in contact with each other (Plate VII, 1, 3). Stromata are flattened, subcircular to circular in outline, 38–130 μm in diameter. Most specimens are slightly asymmetrical and possess lobed margins (Plate VII, 1–5). They are composed of cells arranged in

more or less regular radiating files from the center of the stromata. Center of the stromata consists of irregularly angled cells, nearly isodiametric, 2.9–5.8 μm in diameter; they become more elongated radially towards the distal margin with the length up to 12.3 μm, except for the marginal cells, which are less elongate or even isodiametric. Stromatal cells were tangentially divided and grew radially, and the marginal cells had stopped growing before further elongation and division (Plate VII, 3–5). Most cells have small pores in the upper surface of periclinal walls, which is ca. 1 μm in diameter, slightly elevated, may be randomly placed and generally limited to peripheral cells. The fungal hyphae radiate beneath from the stromata in some, indistinctly septate, composed of rectangular, thin-walled cells with rounded tips (Plate VII, 6–7). The hyphae are contorted and somewhat irregular in diameter, ranging from 3 to 5 μm, with simple septa that are 6–12 μm apart. Each cell has a distinct pore, which is 1–2 μm in diameter, often surrounded by a darker rim in stained specimens (Plate VII, 6). Free hyphae are usually poorly preserved, part unbranched and sometimes fragmented. Fungal spores are spallogenic (Plate VII, 8–12), unicellate, monoporate, surface psilate, oval to elliptical in shape, 7–9 μm in length and

Plate IV. Cuticular structures of extant Smilacaceae under the light microscopy. Scale bar = 100 μm. 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15.

Adaxial epidermis of Smilax china. Abaxial epidermis of S. china. Adaxial epidermis of S. ferox. Abaxial epidermis of S. ferox. Abaxial epidermis of S. lebrunii. Abaxial epidermis of S. scobinicaulis. Abaxial epidermis of S. glaucochina. Adaxial epidermis of S. trinervula. Abaxial epidermis of S. trinervula. Abaxial epidermis of S. davidiana. Adaxial epidermis of S. sieboldii. Abaxial epidermis of S. sieboldii. Abaxial epidermis of S. riparia. Adaxial epidermis of S. polycephala. Abaxial epidermis of S. polycephala.

Plate V. Cuticular structures of extant Smilacaceae under the light microscopy. Scale bar = 100 μm. (see on page 218) 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15.

Adaxial epidermis of Smilax corbularia. Abaxial epidermis of S. cyclophylla. Adaxial epidermis of S. hayatae. Abaxial epidermis of S. hayatae. Adaxial epidermis of S. darrisii. Abaxial epidermis of S. darrisii. Abaxial epidermis of S. stans. Abaxial epidermis of S. tsinchengshanensis. Adaxial epidermis of S. glabra. Abaxial epidermis of S. glabra. Abaxial epidermis of S. lanceifolia. Abaxial epidermis of S. perfoliata. Abaxial epidermis of S. ocreata. Adaxial epidermis of Heterosmilax yunnanensis. Abaxial epidermis of H. yunnanensis.

Plate VI. Cuticular structures of extant Smilacaceae under the SEM. (see on page 219) 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15.

Inner surface of adaxial epidermis of Smilax china. Scale bar = 50 μm. Inner surface of abaxial epidermis of S. china. Scale bar = 50 μm. Inner surface of abaxial epidermis of S. glaucochina. Scale bar = 20 μm. Inner surface of stomatal apparatus of S. glaucochina. Scale bar = 5 μm. Inner surface of abaxial epidermis of S. riparia. Scale bar = 100 μm. Inner surface of stomatal apparatus of S. riparia. Scale bar = 10 μm. Outer surface of adaxial epidermis of S. polycephala. Scale bar = 100 μm. Inner surface of abaxial epidermis of S. polycephala. Scale bar = 100 μm. Inner surface of adaxial epidermis of S. glabra. Scale bar = 100 μm. Inner surface of abaxial epidermis of S. glabra. Scale bar = 100 μm. Inner surface of stomatal apparatus of S. glabra. Scale bar = 20 μm. Inner surface of abaxial epidermis of S. bracteata. Scale bar = 50 μm. Inner surface of stomatal apparatus of S. bracteata. Scale bar = 10 μm. Inner surface of abaxial epidermis of Heterosmilax yunnanensis. Scale bar = 50 μm. Inner surface of stomatal apparatus of H. yunnanensis. Scale bar = 20 μm.

S.-T. Ding et al. / Review of Palaeobotany and Palynology 165 (2011) 209–223

Plate IV

217

218

S.-T. Ding et al. / Review of Palaeobotany and Palynology 165 (2011) 209–223

Plate V (caption on page 216).

S.-T. Ding et al. / Review of Palaeobotany and Palynology 165 (2011) 209–223

Plate VI (caption on page 216).

219

220

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Table 3 Morphological comparison among the fossil species of Smilax L. Taxon

Size (cm)

Shape

Margin Apex

Base

Primary vein Age number

Place

References

Smilax sp. Smilax sp. aff. Smilax Smilax sp.1

Ovate Ovate Ovate Ovate

Entire Entire Entire Entire

3 3 7 5

Entire

Obtuse

5

Smilax sp. 1

6.5 × 3.6

Ovate

Entire

–

5

Dilcher and Lott, 2005

Smilax sp. 2

8.5 × 6.2

Ovate–cordate

Entire

–

Tennessee, USA

Dilcher and Lott, 2005

S. labidurommae Smilax sp. Smilax sp. Smilax sp. S. lamarensis

6.2 × 5.1 11 × 8.7 6.2 × 6.7 11 × 4 8×4

Ovate Ovate Ovate Elliptic Ovate

Entire Entire Entire Entire Entire

Mucronate Mucronate or obtuse Mucronate Acuminate –

Obtuse with concave flanks Obtuse with cordate flanks Cordate Cordate Cordate Truncate Rounded-cordate

Henan, China Guangxi, China Wyoming, USA Csordakút, Hungary Csordakút, Hungary Tennessee, USA

Tao et al., 2000 Feng et al., 1977 Berry, 1929a Erdei and Rákosi, 2009

Lanceolate

Acuminate Probably obtuse – Rounded and slightly emarginate Probably acute

Round Round Cordate Rounded

?Smilax sp.

1.6 × 1.1 6×3 – 3.4– 4.5 × 2.7–3 9.1 × 2.9

5 5 5 – 3

MacGinitie, 1953 Berry, 1930 Berry, 1930 Berry, 1930 Berry, 1929b

Smilax sp. Smilax sp.

– 2.8 × 1.5

– Elliptic

Entire Entire

Acute Acuminate

Rounded Round

5 3

Colorado, USA Idaho, USA Idaho, USA Idaho, USA Washington, USA Iceland Yunnan, China

Smilax cf. aspera

–

Triangular

Entire

Emarginate

–

–

Smilax sp.

–

Ovate

Entire

Mucronate

Cordate

–

Maramures, Romania Ankara, Turkey

Macovei and Givulescu, 2006 Kasapligil, 1977

S. tiantaiensis

1.9–5.3 × 1.3–3.3 –

Ovate

Entire

Acuminate

Rounded

5

Zhejiang, China

This article

Elliptic or lanceolate Lanceolate

Entire

–

Cuneate

3

Sichuan, China

Tao et al., 2000

Entire

–

Cuneate

–

Guangxi, China

Liu, 1993

–

Entire

–

Cuneate or cordate

–

Fukushima, Japan

Suzuki and Nakagawa, 1971

Smilax sp.

Smilax cf. petiolata – S. china

–

5–7 μm in width. There is a dark subcircular patch in the center of each spore under the light microscope (Plate VII, 8 and 9), and it appears as a dished bowl under the scanning electron microscope (Plate VII, 12).

5

Paleocene Eocene Eocene Middle Eocene Middle Eocene Middle Eocene Middle Eocene Oligocene Miocene Miocene Miocene Miocene Miocene Late Miocene Late Miocene Late Miocene Late Miocene Pliocene Early Pleistocene Late Pleistocene

Erdei and Rákosi, 2009

Denk et al., 2005 Tao et al., 2000

Callimothallus was defined as lacking free hyphae and spore by Dilcher (1965). In present study, these spores were also identified as C. pertusus because they are often associated with the stromata and hyphae of this fungal species.

4.2. Comparison and discussion 5. Paleoecology The genus Callimothallus Dilcher (1965) is frequently discovered in the megafossil plants in the late Cretaceous and Cenozoic (Phadtare, 1989; Phipps, 2001). The genus is a morphogenus of multiporate epiphyllous shields on the general lines of a microthyriaceous fruiting body (Dilcher, 1965). Callimothallus has numerous cells with a single pore on the upper surface near the proximal end, so it is easily recognized that even fragments of stromata could be identified (Elsik, 1978). The stromata associated with the leaves of S. tiantaiensis are subcircular in outline with lobed margin, the cells arranged in radiating and a small pore on the periclinal wall of most cells, all the respects demonstrate that the present stromata are identical with those described by Dilcher (1965). Some palaeophytologists assigned some epiphyllous fungi association with fossil Smilax to another genus Phragmothyrites (Elsik, 1978; Sherwood-Pike and Gray, 1988), which closely resembles to Callimothallus in general morphology of stromata, but the cellular pores are absent in the stromata of Phragmothyrites (Selkirk, 1975; Elsik, 1978; Phipps and Rember, 2004). The stromata of Stomiopeltites Alvin and Muir have also been found with Smilax (Phipps and Rember, 2004), but they are short of radiate cells and ostiolate. Selkirk (1975) described some free hyphae of C. pertusus. They are septate, composed of rectangular, thin-walled cells and there is a distinct pore in most of the cells. Based on a morphologic comparison, we found the present hyphae on the leaves of S. tiantaiensis are in accord with the hyphae of C. pertusus described by Selkirk (1975). Many of spallogenic spores (sometimes connected with the stromata) were also found in the cuticles of S. tiantaiensis. However, the genus

Climbing plants play important ecological roles in the forest ecosystem dynamics (Nabe-Nielsen, 2001; Schnitzer and Bongers, 2002). Lianas are important components in neotropical floras and Old World tropics (Nabe-Nielsen, 2001). Generally, the presence of extant families of lianas as Icacinaceae, Menispermaceae and Vitaceae has been suggested as an indicator of the multilayered structure (Reid and Chandler, 1933; Wolfe, 1977; Muller, 1981,1984; Upchurch and Wolfe, 1987; Doria et al., 2008). Smilax is a climbing plant with conspicuous tendrils and stout, thorny stems of woody or herbaceous vines, which is often suggested as an indicator of neotropical rain forest (Nabe-Nielsen, 2001; Addo-Fordjour et al., 2008). The present fossil Smilax demonstrates that a multilayered structure existed in the Miocene forests of Zhejiang. The Miocene flora of Shengxian Formation in Zhejiang, East China composed of 46 genera which belong to 26 families (Li and Guo, 1982; Li, 1984; Li et al., 2008; Jia et al., 2009). Some genera, such as Cinnamomum, Carpinus, Cyclobalanopsis, Castanea, Castanopsis, Fagus, Ficus, Lithocarpus, Mallotus, Paliurus, Torreya and Cephalotaxus, demonstrate a humid subtropical evergreen broad-leaved forest in this region in the Late Miocene. Ren et al. (2010) indicated that the region of Zhejiang during the Miocene was a warm subtropical climate based on the Overlapping distribution analysis (refer to Yang et al., 2007) from the plant megafossils of this Formation. The results suggest that the region of Zhejiang during the Miocene was a warm subtropical climate with the mean annual temperature (MAT) of 9.9– 19.7 °C and mean annual precipitation (MAP) of 1117.7–1546.4 mm.

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221

Plate VII. Fossil fungi of Callimothallus pertusus Dilcher on the cuticles of Smilax tiantaiensis sp. nov. 1, 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12.

Stromata on the surface of adaxial epidermis. Scale bar = 100 μm. Two stromata in contact with each other, enlarged from 1. Scale bar = 30 μm. Details of stromata, enlarged from 1. Scale bar = 30 μm. Stromata in contact with a spore, enlarged from 2. Scale bar = 30 μm. Hyphae on the adaxial epidermis. Scale bar = 30 μm. Hyphae on the abaxial epidermis. Scale bar = 50 μm. Spallogenic spores on the adaxial epidermis. Scale bar = 30 μm. Spallogenic spores on the adaxial epidermis. Notice one stromata in contact with a spore. Scale bar = 30 μm. Spallogenic spores on the adaxial epidermis under the SEM. Scale bar = 30 μm. Details of spore under the SEM. Scale bar = 1 μm. Details of spore under the SEM. Scale bar = 1 μm.

In addition, the presence of epiphyllous fungi usually represents a humid tropical–subtropical climate (Dilcher, 1965; Phadtare, 1989; Tripathi, 2001; Phipps and Rember, 2004; Sharma et al., 2005; Shi et al.,

2010). The occurrence of Callimothallus pertusus on the surface of our fossil Smilax leaves might also indicate a further evidence of warm and humid environment in eastern Zhejiang during the Miocene.

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Acknowledgements The authors thank the reviewer, Prof. David Dilcher (Indiana University, USA) for his helpful comments. We also thank Prof. Chengxin Fu (Zhejiang University, China) for providing extant leaves. This paper was conducted under the National Natural Science Foundation of China (No. 40772012), the Specialized Research Fund for the Doctoral Program of Higher Education (Nos. 20100211110019 and 20100211120009), the Foundation of the State Key Laboratory of Paleobiology and Stratigraphy, Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences (No. 103108) and the Fundamental Research Funds for the Central Universities (No. lzujbky-2009-132). References Addo-Fordjour, P., Anning, A.K., Atakora, E.A., Agyei, P.S., 2008. Diversity and distribution of climbing plants in a semi-deciduous rain forest, KNUST botanic garden, Ghana. International Journal of Botany 4 (2), 186–195. APG II (Angiosperm Phylogeny Group II), 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141 (4), 399–436. Berry, E.W., 1929a. The flora of the Frontier Formation. United States Geological Survey. Professional Paper 158, 129–135. Berry, E.W., 1929b. A revision of the flora of the Latah Formation. United States Geological Survey. Professional Paper 154, 225–265. Berry, E.W., 1930. A new Miocene Cercis from Idaho and Washington. Bulletin of the Torrey Botanical Club 57 (4), 239–244. Bews, J.W., 1927. Studies in the ecological evolution of the angiosperms. The New Phytologist 26 (1), 1–21. BGMRZP (Bureau of Geology and Mineral Resources of Zhejing Province), 1989. Geological Memoirs. Series 1, No.11. Regional Geology Records of Zhejiang Province. Geological Publishing House, Beijing, China, pp. 189–204 (in Chinese). BGMRZP, 1996. Lithostraticgraphy of Zhejiang Province. China University of Geosciences Press, Wuhan, China, pp. 91–127 (in Chinese). Cameron, K.M., Fu, C.X., 2000. Untangling the catbriers: phylogenetic studies in Smilacaceae. American Journal of Botany 87 (6), 117 (Abstract). Cameron, K.M., Fu, C.X., 2006. A nuclear rDNA phylogeny of Smilax (Smilacaceae). Aliso 22, 598–605. Chase, M.W., Fay, M.F., Devey, D.S., Maurin, O., Ronsted, N., Davies, T.J., Pillon, Y., Petersen, G., Seberg, O., Tamura, M.N., Asmussen, C.B., Hilu, K., Borsch, T., Davis, J.I., Stevenson, D.W., Pires, J.C., Givnish, T.J., Sytsma, K.J., McPherson, M.M., Graham, S.W., Rai, H.S., 2006. Multigene analyses of monocot relationships: a summary. Aliso 22, 63–75. Chen, S.C., Koyama, T., Liang, S.Y., 2000. Smilax L. and Heterosmilax Kunth. In: Wu, Z.Y., Raven, P.H. (Eds.), Flora of China, vol. 24. Science Press, Beijing and Missouri Botanical Garden Press, St. Louis, pp. 96–117. Chen, S.C., Qiu, Y.X., Wang, A.L., Cameron, K.M., Fu, C.X., 2006a. A phylogenetic analysis of the Smilacaceae based on morphological data. Acta Phytotaxonomica Sinica 44 (2), 113–125. Chen, S.C., Zhang, X.P., Ni, S.F., Fu, C.X., Cameron, K.H., 2006b. The systematic value of pollen morophology in Smilacaceae. Plant Systematics and Evolution 259 (1), 19–37. Conover, M.V., 1983. The vegetative morphology of the reticulate-veined Liliiforae. Telopea 2, 401–412. Conover, M.V., 1991. Epidermal patterns of the reticulate-veined Liliiflorae and their parallel-veined allies. Botanical Journal of the Linnean Society 107 (3), 295–312. Conran, J.G., Christophel, D.C., 1999. A redescription of the Australian Eocene fossil monocotyldeon Petermanniopsis (Lilianae: AFF. Petermanniaceae). Royal Society of South Australia 123 (2), 61–67. Conran, J.G., Clifford, H.T., 1985. The taxonomic affinities of the genus Ripogonum. Nordic Journal of Botany 5, 215–219. Conran, J.G., Christophel, D.C., Scriven, L., 1994. Petermanniopsis angleseaensis gen. & sp. nov.: an Australian fossil net-veined monocotyledon from Eocene Victoria. International Journal of Plant Sciences 155 (6), 816–827. Conran, J.G., Carpenter, R.J., Jordan, G.J., 2009. Early Eocene Ripogonum (Liliales: Ripogonaceae) leaf macrofossils from southern Australia. Australian Systematic Botany 22 (3), 219–228. Craggs, H.J., 2005. Late Cretaceous climate signal of the northern Pekulney Range Flora of northeastern Russia. Palaeogeography, Palaeoclimatology, Palaeoecology 217 (1–2), 25–46. Cronquist, A., 1981. An Integrated System of the Classification of Flowering Plants. Columbia University Press, New York. Dahlgren, R.M.T., Clifford, H.T., Yeo, P.F., 1985. The families of monocotyledons. Springer–Verlag, Berlin pp. 1–520. Davis, J.I., Stevenson, D.W., Petersen, G., Seberg, O., Campbell, L.M., Freudenstein, J.V., Goldman, D.H., Hardy, C.R., Michelangeli, F.A., Simmons, M.P., Specht, C.D., VergaraSilva, F., Gandolfo, M., 2004. A phylogeny of the monocots, as inferred from rbcL and atpA sequence variation, and a comparison of methods for calculating jackknife and bootstrap values. Systematic Botany 29 (3), 467–510. Denk, T., Grimsson, F., Kvacek, Z., 2005. The Miocene floras of Iceland and their significance for late Cainozoic North Atlantic biogeography. Botanical Journal of the Linnean Society 149 (4), 369–417.

Dilcher, D.L., 1965. Epiphyllous fungi from Eocene deposits in western Tennessee. Palaeontographica Abteilung B 116, 1–54. Dilcher, D.L., 1974. Approaches to the identification of angiosperm leaf remains. Botanical Review 40 (1), 1–157. Dilcher, D.L., Lott, T.A., 2005. A middle Eocene fossil plant assemblage (Powers Clay Pit) from western Tennessee. Bulletin Florida Museum Natural History 45 (1), 1–43. Ding, Z.D., Gilbert, M.G., 2000. Dioscoreaceae. In: Wu, Z.Y., Raven, P.H. (Eds.), Flora of China. : Flagellariaceae through Marantaceae, vol. 24. Science Press, Beijing and Missouri Botanical Garden Press, St. Louis, pp. 276–296. Doria, G., Jaramillo, C.A., Herrera, F.A., 2008. Menispermaceae from the Cerrejón Formation, Middle to Late Paleocene, Colombia. American Journal of Botany 95 (8), 954–973. Elsik, W.C., 1978. Classification and geologic history of the microthyriaceous fungi. In: Bharadwaj, D.C., Lele, K.M., Kar, R.K. (Eds.), Proceedings of 4th International Palynological Conference. Birbal Sahni Institute of Palaeobotany, Lucknow, India, pp. 331–342. Erdei, B., Rákosi, L., 2009. The Middle Eocene flora of Csordakút (N Hungary). Geologica Carpathica 60 (1), 43–57. Feng, S.N., Meng, F.S., Chen, G.X., Xi, Y.H., Zhang, C.F., Liu, Y.A., 1977. Plant kingdom. In: Hubei Institute of Geological Science (Ed.), FossilAtlas of Central and South China. : Mesozoic and Cenozoic, vol. III. Geological Publishing House, Beijing, China, pp. 195–262 (in Chinese). Holmes, W.C., 2002. Smilacaceae Ventenat. In: Flora of North America Editorial Committee (Ed.), Flora of North America, vol. 26. Oxford University Press, New York and Oxford, pp. 468–478. Hutchinson, J., 1973. The Families of Flowering Plants Arranged According to a New System Based on Their Probable Phylogeny, 3rd ed. Clarendon Press, Oxford, UK, pp. 1–492. Inamdar, J.A., Shenoy, K.N., Rao, N.V., 1983. Leaf architecture of some monocotyledons with reticulate venation. Annals of Botany 52 (5), 725–736. Jansonius, J., 1976. Palaeogene fungal spores and fruiting bodies of the Canadian Arctic. Geoscience and Man 15, 129–132. Jia, H., Sun, B.N., Li, X.C., Xiao, L., Wu, J.Y., 2009. Microstructures of one species of Quercus from the Neogene in Eastern Zhejiang and its palaeoenvironmental indication. Earth Science Frontiers 16 (5), 79–90 (in Chinese with English abstract). Kalgutkar, R.M., 1997. Fossil fungi from the lower Tertiary Iceberg Bay Formation, Eukeka Sound Group, Axel Heiberg Island, Northwest Territories, Canada. Review of Palaeobotany and Palynology 97 (1–2), 197–226. Kasapligil, B., 1977. A late-Tertiary conifer–hardwood forest from the vicinity of Güvem village, near Kizilcahamam. Bulletin of the Mineral Research and Exploration Institute (Turkey) 88, 25–55. Koyama, T., 1960. Materials toward a monograph of the genus Smilax. Quarterly Journal of Taiwan Museum 13 (1–2), 1–61. Kürschner, W.M., 1997. The anatomical diversity of recent and fossil leaves of the durmast oak (Quercus petraea Lieblein/Q.pseudocastanea Goeppert)—implications for their use as biosensors of palaeoatmospheric CO2 levels. Review of Palaeobotany and Palynology 96 (1–2), 1–30. Lange, R.T., 1978. Southern Australian Tertiary epiphyllous fungi, modern equivalents in the Australasian region, and habitat indicator value. Canadian Journal of Botany 56 (5), 532–541. Li, H.M., 1984. Neogene floras from eastern Zhejiang, China. In: Whyte, R.O. (Ed.), The Evolution of the East Asian Environment. : Palaeobotany, Palaeozoology and Palaeoanthropology, vol. II. Centre of Asian Studies, University of Hong Kong, Hong Kong, China, pp. 461–466. Li, H.M., Guo, S.X., 1982. Angiospermae. In: Nanjing Institute of Geology and Mineral Resources (Ed.), Paleontological Atlas of East China, Part 3, Volume of Mesozoic and Cenozoic. Geological Publishing House, Beijing, China, pp. 294–316 (in Chinese). Li, M.T., Sun, B.N., Xiao, L., Ren, W.X., Li, X.C., Dai, J., 2008. Discovery of Betula mioluminifera Hu et Chaney from the Miocene in Eastern Zhejiang and reconstruction of palaeoclimate. Advances in Earth Science 23 (6), 651–658 (in Chinese with English abstract). Li, X.C., Sun, B.N., Xiao, L., Wu, J.Y., Lin, Z.C., 2010. Leaf macrofossils of Ilex protocornuta sp. nov. (Aquifoliaceae) from the Late Miocene of East China: implications for palaeoecology. Review of Palaeobotany and Palynology 161 (1–2), 87–103. Liu, Y.S., 1993. A palaeoclimatic analysis on the early Pleistocene flora of Changseling Formation, Baise Basin, Guangxi. Acta Palaeontologica Sinica 32 (2), 151–170 (in Chinese with English abstract). Liu, R.X., Chen, W.J., Sun, J.Z., Li, D.M., 1992. The K–Ar age and tectonic environment of Cenozoic rock in China. In: Liu, R.X. (Ed.), The Age and Geochemistry of Cenozoic Volcanic Rock in China. Seismic Press, Beijing, China, pp. 1–43. Liu, Y.S., Zetter, R., Ferguson, D.K., Mohr, B.A.R., 2007. Discriminating fossil evergreen and deciduous Quercus pollen: a case study from the Miocene of eastern China. Review of Palaeobotany and Palynology 145 (3–4), 289–303. Liu, Y.S., Zetter, R., Ferguson, D.K., Zou, C., 2008. Lagerstroemia (Lythraceae) pollen from the Miocene of eastern China. Grana 47 (4), 262–271. MacGinitie, H.D., 1953. Fossil plants of the Florissant Beds, Colorado. Carnegie Institution of Washington Publication no. 559, pp. 1–198. Macovei, Gh., Givulescu, R., 2006. The present stage in the knowledge of the fossil flora at Chiuzbaia Maramures, Romania. Carpathian Journal of Earth and Environmental Sciences 1 (1), 41–52. Muller, J., 1981. Fossil pollen records of extant angiosperms. The Botanical Review 47 (1), 1–142. Muller, J., 1984. Significance of fossil pollen for angiosperm history. Annals of the Missouri Botanical Garden 71 (2), 419–443. Nabe-Nielsen, J., 2001. Diversity and distribution of lianas in a neotropical rain forest, Yasuni National Park, Ecuador. Journal of Tropical Ecology 17 (1), 1–19. Phadtare, N.R., 1989. Palaeoecologic significance of some fungi from the Miocene of Tanakpur (U.P.) India. Review of Palaeobotany and Palynology 59 (1–4), 127–131.

S.-T. Ding et al. / Review of Palaeobotany and Palynology 165 (2011) 209–223 Phipps, C.J., 2001. The evolution of epiphyllous fungal communities with an emphasis on the Miocene of Idaho. Ph D Thesis, University of Kansas, Kansas, USA, 151 pp. Phipps, C.J., Rember, W.C., 2004. Epiphyllous fungi from the Miocene of Clarkia, Idaho: reproductive structures. Review of Palaeobotany and Palynology 129 (1–2), 67–79. Pole, M.S., 2007. Monocot macrofossils from the Miocene of southern New Zealand. Palaeontologia Electronica 10 (3), 1–21. Raz, L., 2002. Dioscoreaceae. In: Flora of North America Editorial Committee (Ed.), Flora of North America, vol. 26. Oxford University Press, New York and Oxford, pp. 479–485. Reid, E.M., Chandler, M.E.J., 1933. The London Clay Flora. British Museum (Natural History), London, UK. 561pp. Ren, W.X., Sun, B.N., Xiao, L., 2010. Quantitative reconstruction on paleoelevation and paleoclimate of Miocene Xiananshan Formation in Ninghai, Zhejiang Province. Acta Micropalaeontologica Sinica 27 (1), 93–98 (in Chinese with English abstract). Schnitzer, S.A., Bongers, F., 2002. The ecology of lianas and their role in forests. Trends in Ecology & Evolution 17 (5), 223–230. Selkirk, D.R., 1975. Tertiary fossil fungi from Kiandra, New South Wales. Proceedings of the Linnean Society of New South Wales 100 (1), 70–94. Sharma, N., Kar, R.K., Agarwal, A., Kar, R., 2005. Fungi in dinosaurian (Isisaurus) coprolites from the Lameta Formation (Maastrichtian) and its reflection on food habit and environment. Micropaleontology 51 (1), 73–82. Sherwood-Pike, M., Gray, J., 1988. Fossil leaf-inhabiting fungi from northern Idaho and their ecological significance. Mycologia 80 (1), 14–22.

223

Shi, G.L., Zhou, Z.Y., Xie, Z.M., 2010. A new Cephalotaxus and associated epiphyllous fungi from the Oligocene of Guangxi, South China. Review of Palaeobotany and Palynology 161 (3–4), 179–195. Suzuki, K., Nakagawa, H., 1971. Late Pleistocene flora from the Pacific coast of Fukushima Prefecture, Japan. The science reports of the Tohoku University, 2nd Series. Geology 42 (2), 187–198. Tao, J.R., Zhou, Z.K., Liu, Y.S., 2000. The Evolution of the Late Cretaceous–Cenozoic Floras in China. Science Press, Beijing, China. 282pp. (in Chinese). Tomlinson, P.B., 1982. Helobiae (Alismatales). In: Metcalfe, C.R. (Ed.), Anatomy of the Monocotyledons, VII. Clarendon Press, Oxford, UK. 559 pp. Tripathi, A., 2001. Fungal remains from Early Cretaceous Intertrappean Beds of Rajmahal Formation in Rajmahal Basin, India. Cretaceous Research 22 (5), 565–574. Upchurch, G.R., Wolfe, J.A., 1987. Mid Cretaceous to Early Tertiary vegetation and climate: evidence from fossil leaves and woods. In: Friis, E.M., Chaloner, W.G., Crane, P.R. (Eds.), The origins of angiosperms and their biological consequences. Cambridge University Press, Cambridge, UK, pp. 75–105. Wolfe, J.A., 1977. Palaeogene floras from the Gulf of Alaska region. United States Geological Survey. Professional Paper 997, 1–108. Wu, J.Y., Sun, B.N., Liu, Y.S., Xie, S.P., Lin, Z.C., 2009. A new species of Exbucklandia (Hamamelidaceae) from the Pliocene of China and its paleoclimatic significance. Review of Palaeobotany and Palynology 155 (1–2), 32–41. Yang, J., Wang, Y.F., Spicer, R.A., Mosbrugger, V., Li, C.S., Sun, Q.G., 2007. Climatic reconstruction at the Miocene Shanwang Basin, China, using leaf margin analysis, CLAMP, coexistence approach, and overlapping distribution analysis. American Journal of Botany 94 (4), 599–608.