Calocedrus shengxianensis, a late Miocene relative of C. macrolepis (Cupressaceae) from South China: Implications for paleoclimate and evolution of the genus

Review of Palaeobotany and Palynology 222 (2015) 1–15

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Calocedrus shengxianensis, a late Miocene relative of C. macrolepis (Cupressaceae) from South China: Implications for paleoclimate and evolution of the genus Jian-Wei Zhang a,b, Jian Huang a, Ashalata D'Rozario c, Jonathan M. Adams d, Zhe-Kun Zhou a,⁎ a

Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden (XTBG), Chinese Academy of Sciences, Mengla, Yunnan 666303, China Laboratory of Environmental Chang in Arid Lands, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, 818 South Beijing Road, Urumqi, Xinjiang 830011, China c Department of Botany, Narasinha Dutt College, 129, Bellilious Road, Howrah 711101, India d The College of Natural Sciences, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 151-742, Republic of Korea b

a r t i c l e

i n f o

Article history: Received 17 October 2014 Received in revised form 23 June 2015 Accepted 1 July 2015 Available online 31 July 2015 Keywords: Calocedrus Global cooling Morphology Taxonomy Upper Miocene China

a b s t r a c t The diversification of the relict genus Calocedrus Kurz (Cupressaceae) in the Neogene of eastern Asia has remained unknown due to lack of fossil evidence. A late Miocene species, Calocedrus shengxianensis (He, Sun et Liu) Zhang et Zhou comb. nov., is described on the basis of new fossil material from the Wenshan flora in SE Yunnan, SW China. The species was originally described as Fokienia shengxianensis He, Sun et Liu from the upper Miocene Shengxian flora in E Zhejiang, SE China. The new fossil material includes well-preserved compression of leafy shoots and associated impression of seed cones. Based on the comparisons, this fossil species bears most similarities to the modern Calocedrus macrolepis Kurz, which is presently endemic to eastern Asia, in N India, Laos, NE Myanmar, NE Thailand, Vietnam and S China, but does not occur in SE Yunnan and E Zhejiang. The difference between them lies primarily in the morphology of apex of lateral as well as facial leaves. With the global cooling and uplift of the Qinghai–Tibet Plateau since the late Miocene, the climate in eastern Asia has changed profoundly. This has led to the disappearance of C. shengxianensis from SE Yunnan and E Zhejiang, and the leaf morphological shifts in C. macrolepis: the acute or acuminate leaf apices in the modern C. macrolepis, which are in contrast to the blunt or obtuse ones in the late Miocene C. shengxianensis, have evolved probably to adapt to the humid climate since the late Miocene. © 2015 Elsevier B.V. All rights reserved.

1. Introduction The genus Calocedrus Kurz (Cupressaceae) is an evergreen conifer and also known as incense cedar. It is characterized by flat branchlets with strongly decussate and dimorphic leaves (Thieret, 1993; Fu et al., 1999). This genus contains three relict species and is discontinuously distributed in eastern Asia and western North America, with Calocedrus macrolepis Kurz in S China, N India, Laos, NE Myanmar, NE Thailand and Vietnam, Calocedrus rupestris Averyanov, Nguyên et Phan in N Vietnam, and Calocedrus decurrens (Torrey) Florin in California, Nevada, Oregon of USA and Baja California of Mexico (Thieret, 1993; Fu et al., 1999; Averyanov et al., 2005). The phylogeny of the genus Calocedrus inferred from nuclear ribosomal sequence and fossil evidence demonstrates the genetic uniqueness among these three species: the North American and the Asian species are each monophyletic, diverged in the Oligocene at a time of about 25 Ma (Chen et al., 2009). The diversification of this genus in the Neogene of eastern Asia has remained unknown due to lack of fossil evidence. ⁎ Corresponding author. E-mail address: [email protected] (Z.-K. Zhou).

http://dx.doi.org/10.1016/j.revpalbo.2015.07.004 0034-6667/© 2015 Elsevier B.V. All rights reserved.

The earliest fossils of the genus were from the Oligocene, with representatives in eastern Asia (WGCPC, 1978; Shi et al., 2012), North America (Meyer and Manchester, 1997) and central and southern Europe (Kvaček, 1999). Although there are several paleobotanical evidences indicating that the genus Calocedrus was circumboreal in distribution during the Oligocene and Miocene (Manchester, 1999), with records from western North America (Axelrod, 1964, 1992; Meyer and Manchester, 1997; Kvaček and Rember, 2007), Japan (Onoe et al., 1985), Korea (Huzioka, 1972), China (WGCPC, 1978; Guo, 2011; Shi et al., 2012) and Europe (Kvaček and Hably, 1998; Kvaček, 1999; Kvaček and Rember, 2007). However, taxonomic relationships of these records are controversial because of poor preservation and lack of epidermal structure. By the Pliocene, fossil records became scarce, with relicts discovered in Frankfurt am Main, Germany (Mädler, 1939; Kvaček, 1999) and Yunnan, China (WGCPC, 1978). Most of the oldest fossils resemble the extant eastern Asian species (Shi et al., 2012), and the molecular evidence also supports that the eastern Asian species are primitive among the living species of Calocedrus (Chen et al., 2009). The close resemblance in foliage morphology between the North American and eastern Asian species, and the differences between these Calocedrus species and the European

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Fig. 1. Maps showing the fossil locality of Calocedrus shengxianensis in SE Yunnan, SW China.

species, suggest that the migration of this genus in the mainland through eastern Asia to North American has taken place directly via the Bering land bridge rather than the Old World or North Atlantic land bridges (Shi et al., 2012). The global climate has undergone severe change after the midMiocene warm interval (Tanai, 1967; Wolfe, 1978; Graham, 1999), e.g., global cooling, especially in eastern Asia owing to the uplift of the Qinghai–Tibet Plateau (Harrison et al., 1992; Molnar et al., 1993; Harrison and Mahon, 1995; Mulch and Chamberlain, 2006). The uplift events have led to the amplifying of the dry–wet seasonal contrast of the eastern Asia monsoons (Li, 1999; An et al., 2001; Jacques et al., 2011; Zhang et al., 2012). Studies show that climatic change is driving adaptive shifts within species, and leaf morphology has demonstrated links with climate and varies within species along climate gradients (Walther et al., 2002; Guerin et al., 2012). A morphological response and shift would occur over time due to climatic change (Byars et al., 2007; Guerin et al., 2012). Paleontologists have long used the environmental sensitivity of plants to reconstruct paleoclimate from fossil plant remains, and the sizes and shapes (physiognomy) of fossil leaves are widely applied as proxies for paleoclimatic and paleoecological variables (Dilcher, 1973; Wolfe and Upchurch, 1987; Parrish and Spicer, 1988; Greenwood and Wing, 1995; Wolfe, 1995; Parrish, 1998; Wing et al., 2000; Wilf et al., 2003). Many physiognomic variables correlate significantly with MAT, indicating a coordinated, convergent evolutionary response of fewer teeth, smaller tooth area, and lower degree of blade dissection in warmer environments (Royer et al., 2005). This paper studies a fossil species of Calocedrus, Calocedrus shengxianensis, which was discovered from the upper Miocene of South China. The similarities of this fossil species with the extant Calocedrus macrolepis and the differences in the leaf-morphological features between them would be significant in the discussion of (1) diversity of the genus in the late Miocene; (2) differentiation of this genus in eastern Asia since the late Miocene; and (3) leaf morphological responses and shifts with climatic change. 2. Material and methods 2.1. Geological settings and age Calocedrus fossils were collected from outcrops located in Dashidong Village (23°15′N, 104°15′E, 1482 m asl), Wenshan City, SE Yunnan

Province, SW China (Fig. 1). The outcrops are characterized by light-gray or light-yellow pelitic laminated siltstone and mudstone. The laminated sedimentary sequences in Dashidong Village were assigned to the Xiaolongtan Formation (BGMRYP, 1996). The present Calocedrus fossils were collected from the Middle and Lower members of the formation (Zhang et al., 2015a). The Xiaolongtan Formation is late Miocene in age based on lithology, biologic assemblage and regional comparisons (Dong, 1987; BGMRYP, 1996). In Dashidong Village, the Xiaolongtan Formation lies unconformably on the upper Oligocene Yanshan Group, and is overlain unconformably by Quaternary strata (Zhang, 1976). The sedimentary sequences of Xiaolongtan Formation in Dashidong Village (Fig. 2) and Maguan County in Wenshan City yield abundant plant fossils, such as Ailanthus confucii Unger (Su et al, 2013), Bauhinia wenshanensis Meng et Zhou (Meng et al., 2014), Sequoia maguanensis Zhang et Zhou, Pinus massoniana Lambert (Zhang et al., 2015a, 2015b), Burretiodendron Rehder (Anberrée et al., 2015), Calocedrus, Cephalotaxus, Pinus cf. krempfii, fossil fish and insects (e.g., mosquitos, ants).

2.2. Fossil specimens The fossils described here consist of compression of wellpreserved leafy twigs (DMS 0147-0152) and impression of associated seed cones (DMS 0153-0156). Fossil specimens are deposited in the fossil repository of the Paleoecology Research Group, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Science, Yunnan of China.

2.3. Morphology and cuticle study methods Photographs were obtained using a Nikon D700 digital camera under tungsten light. Some specimens were immersed in kerosene to enhance details. Detailed structures of these specimens were observed and photographed under a Leica S8APO stereoscope microscope. The leafy twigs were treated with Schulze's solution (HNO3 and KClO3, 3:1) and KOH, and washed with water to obtain clear cuticles (Kerp, 1990). Epidermal characters were observed using a Leica DM750 stereoscope microscope, photographed under a Leica DFC295 and Zeiss EVOLS10 scanning electron microscope.

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Fig. 2. Stratigraphic column of the Xiaolongtan Formation in Dashidong village, showing the Calocedrus fossils within the bed (based on the description by Zhang (1976)).

3. Results 3.1. Systematics Calocedrus Kurz Family: Cupressaceae Gray sensu lato. Subfamily: Cupressoideae Richard ex Sweet. Calocedrus shengxianensis (He, Sun et Liu) Zhang Jian-Wei et Zhou Zhe-Kun comb. nov. Plates I, II, III, and IV. Basionym: Fokienia shengxianensis He, Sun et Liu, 2012. Review of Palaeobotany and Palynology, 176–177, p. 25. Holotype: Specimen JH-1-4-290 (A, B) kept in the collection of Institute of Paleontology and Stratigraphy, Lanzhou University, China, and illustrated in He, Sun et Liu, 2012. Review of Palaeobotany and Palynology, 176–177, Plate I, 1–2. Paratypes: Specimens JH-1-3-042, JH-2-045, JH-1-046, JH-1-052, JH-1-4-057, JH-1-4-235 (A, B), JH-1-4-290 (A, B), JH-1-4-297, JH-1-4466 (A, B), JH-1-4-476, JH-1-4-477, JH-1-4-478, JH-1-4-949, JH-1-956, JH-224, HNT-11, HNT-25, HNT-50, HNT-51, and HNT-215 kept in the collection of Institute of Paleontology and Stratigraphy, Lanzhou University, China. New material described here: specimens DMS 0147 (Plate I, 1), DMS 0148 (Plate I, 2), DMS 0149 (Plate II, 1), DMS 0150 (Plate II, 2), DMS 0151 (Plate II, 3), DMS 0152 (Plate II, 4), DMS 0153 (Plate IV, 1), DMS 0154 (Plate IV, 2), DMS 0155 (Plate IV, 3) and DMS 0156 (Plate IV, 4) deposited in the fossil repository of the Paleoecology Research Group, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Science, Yunnan of China. 3.2. Description All foliage branches spread in a flattened spray, the ultimate and the penultimate shoots arranged in an alternate manner (Plate I, 1–2). The ultimate shoots arise from the axils of facial leaves in penultimate

shoots (Plate I, 1–2). Foliage shoots convex on the upper side and concave on the lower side (Plate II, 1–4). Leaves covering the shoots scale-like and imbricate along the axes (Plate II, 5–7). Scale leaves sessile and decurrent along the axes (Plate II, 5–7), decussate, appearing in whorls of four, strongly dimorphic in lateral and facial ones (Plate II, 5–7). Two lateral and two facial leaves in a whorl constitute a cladode-like segment, i.e. branchlet segment (Plate II, 5); branchlet segments wedge-shaped and stacked up along the axis of the shoots (Plate II, 5–7), similar in size in mature shoots, elongate and a little larger in penultimate shoots, becoming smaller toward the distal end of the immature shoots, 2.5 ± 0.8 mm long and 2.1 ± 0.4 mm wide; length/ width ratio ca. 1.2 (Plate II, 5–7). Lateral leaves falcate, 2.4 ± 0.6 mm long, 0.9 ± 0.3 mm wide (Plate II, 5–7), bilaterally flattened, conduplicate and overlapping facial leaf margins (Plate II, 5), with a blunt, incurved apex adhering to the facial leaves (Plate II, 5–7). Bases of two lateral leaves in a segment in contact, forming a cross-like structure (Plate II, 5), margins slightly raised due to the overlapping (Plate II, 5). Facial leaves dorsiventrally flattened and inversely triangular in outline, 2.5 ± 0.7 mm long, 1.2 ± 0.3 mm wide in the top (Plate II, 5). Midrib distinct, extending from the base to apex (Plate II, 5). Top edges of facial leaves appear obtuse or blunt, flattened or arc-like (Plate II, 5–7). But facial leaves could also be falcate, thus their apices are curved inwards, compressed and invisible. Facial leaves in a segment usually a little higher than lateral ones (Plate II, 5–7). Many fine veins on lateral and facial leaves, extending from base to apex (Plate II, 5). Lateral leaves amphistomatic (Plate III, 1–3, 7, 8), abaxial cuticle stomatal-free on upper side of foliage shoot, with ordinary epidermal cells regularly arranged in longitudinal files (Plate III, 1, 7); cells elongate or strongly elongate along the long axis of the leaf, 60 ± 40 μm long and 30 ± 15 μm wide (Plate III, 1, 7) with rectangular or oblique end walls and straight anticlinal walls. Abaxial cuticle of lateral leaf on lower side of foliage shoot with one longitudinally arranged stomatal zone (Plate III, 1, 2, 7, 8). Adaxial cuticle of lateral leaves with a median stomatal zone (Plate III, 3), running along the suture between facial and lateral leaves, partly overlapped by the lateral leaves. The lateral

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Plate I

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Plate II. Fossil leaves of Calocedrus shengxianensis (He, Sun et Liu) Zhang et Zhou comb. nov. 1–4. 5–7.

Foliage shoots convex on the upper side (arrow “a” in 3) and concave correspondingly on the lower side (1, 2, 4; arrow “b” in 3). Bar = 0.5 cm. Enlargement of 1 in Plate I, showing leaves cover the whole shoots, scale-like, imbricate, decurrent, decussate and appearing in whorls of four; dimorphic leaves in a whorl constitute branchlet segments, being wedge-shaped and stacked up along the axis of shoots; lateral leaves falcate, bilaterally flattened, conduplicate and overlapping margins of facial leaves; apices of lateral leaves blunt, incurved and adhere to the facial leaves; lateral leaves contact in the bases; facial leaves appear flattened or could also be falcate, with distinct mid-rib and (or) obtuse apices; many fine parallel veins. Bar = 1 mm.

Plate I. Fossil foliage of Calocedrus shengxianensis (He, Sun et Liu) Zhang et Zhou comb. nov. 1–2.

Showing foliage branches spread in flattened spray, the ultimate shoots and the penultimate shoots in alternate manner, the ultimate shoots arise from the axil of facial leaves in penultimate shoots. Bar = 1 cm.

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Plate III

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Plate IV. Associated seed cones of Calocedrus shengxianensis (He, Sun et Liu) Zhang et Zhou comb. nov. Bar = 1 cm. 1–4.

Seed cones ovate to broadly cylindrical, stalked, having four large fertile seed-scale elements and two small basal-external bract-scale elements; the apices of fertile seed-scale blunt or obtuse, recurved, having short mucros on the back (arrow “a” in 1–2); bract scales attached near the base of seed cones on the two sides (arrow “b” in 3–4), with obtuse apices.

stomatal-free zones composed of 5–6 files of ordinary epidermal cells, generally with a similar morphology and arrangement as in the abaxial cuticle (Plate III, 3). Stomatal zone running from the base to the upper region of leaves, absent in the apex (Plate III, 1, 7). Stomata irregularly arranged, often oriented longitudinally or only slightly oblique (Plate III, 2, 7, 8), near the apex randomly oriented (Plate III, 1, 7), sometimes abut against each other, but hardly sharing subsidiary cells (Plate III, 2, 8, 12, 13). Stomata near the bases of lateral leaves strongly papillate (Plate III, 10–13). Epidermal cells in stomatal zones irregularly shaped, often elongate, strongly papillate (Plate III, 10, 11). Papillae rounded, 20 ± 10 μm in diameter, solitary or sometimes fused with adjacent ones (Plate III, 10–13). Abaxial cuticle of facial leaf on the upper side of foliage shoot is stomata-free, with ordinary epidermal cells arranged in longitudinal files (Plate III, 6). Abaxial cuticle of the facial leaves on the lower side of shoots with a median stomata-free zone and two lateral stomatal zones (Plate III, 4, 5). Stomata-free zones of facial leaves morphologically similar to those of lateral leaves. Stomatal zones run from the base to the upper region of leaves, absent in the apices (Plate III, 4, 5). Stomata randomly arranged, morphologically similar to those on abaxial cuticle of lateral leaves (Plate III, 2, 5). Adaxial cuticle of facial leaves not available in maceration.

Stomatal complexes 55 ± 10 μm long, 45 ± 15 μm wide, haplocheilic, monocyclic (Plate III, 9, 12, 13), with 4–7 subsidiary cells, two being polar (Plate III, 9). Stomatal pits shallow and elongate, elliptical in outline (Plate III, 9), 35 ± 10 μm long, 25 ± 15 μm wide. Guard cells slightly sunken, usually forming a closed aperture (Plate III, 9, 12, 13), periclinal wall inner surface fairly smooth (Plate III, 9). Subsidiary cells irregularly shaped, polygonal, isodiametric or elongate, strongly papillate (Plate III, 8, 9, 12). Each subsidiary cell with a round–oblong proximal papilla forming a distinct Florin ring together with those of other subsidiary cells of the same stomatal complex (Plate III, 13). Florin rings elliptical in outline, 50 ± 15 μm long, 45 ± 10 μm wide (Plate III, 12, 13). Inner cuticle surface of stomatal zones strongly uneven, with concavities of variable shape and size (Plate III, 10, 12), corresponding to outward projecting papillae of subsidiary cells and epidermal cells of the stomatal zone on the outer surface (Plate III, 11, 13). Associated impression of seed cones (Plate IV, 1–4), characteristic of genus Calocedrus in having two small basal-external bract-scale elements, four large fertile seed-scale elements, making up most of the cone specimens and protruding apices of the seed-scale elements. Seed cones ovate to broadly cylindrical, stalked and dehiscent when mature. Cone stalks at least 8 mm long (Plate IV, 3). Four seed scales are erect and decussately arranged on the cones. Bract scales attached

Plate III. Epidermal structures of Calocedrus shengxianensis (He, Sun et Liu) Zhang et Zhou comb. nov. 1.

Abaxial cuticle of a lateral leaf, showing stomata on the lower side of the foliage shoot (arrow “a”), the upper side of foliage shoot nonstomatal (arrow “b”), epidermal cells in

2.

Stomatal zone on the abaxial cuticle of lateral leaf, stomata irregularly arranged, oriented longitudinally or only slightly oblique. Bar = 100 μm.

longitudinal files. Bar = 200 μm. 3.

Showing the adaxial cuticle of lateral leaves composed of a median stomatal zone. Bar = 100 μm.

4.

Showing the abaxial cuticle of the facial leaves on the lower side of shoots, composed of a median nonstomatal zone and two lateral stomatal zones. Bar = 200 μm.

5.

Stomatal zone absent in the apex of facial leaf, stomata random in orientation near the apex of facial leaf. Bar = 100 μm.

6.

Abaxial cuticle of facial leaf on the upper side of foliage shoot is nonstomatal. Bar = 100 μm.

7.

Inner cuticle surface, showing abaxial cuticle of a lateral leaf, stomatal zone absent in the apex. Bar = 100 μm.

8.

Inner cuticle surface, showing abaxial cuticle of lateral leaf on the lower side of foliage shoot, stomatal irregularly arranged, often oriented longitudinally or only slightly

9.

Inner cuticle surface, showing a stomatal complex, haplocheilic and monocyclic, elliptical in outline. Bar = 10 μm.

oblique, stomata hardly share subsidiary cells. Bar = 50 μm. 10–11.

Epidermal cells near the base of leaf strongly papillate, the inner cuticle surface strongly uneven (10), with concavities of variable shape and size; corresponding to the outward projecting papillae on the outer surface (11). Bar = 50 μm.

12–13.

Stomata near the base of leaves strongly papillate, each subsidiary cell bears a round–oblong proximal papilla, fused with adjacent ones, forms a distinct Florin ring around the stomatal pit. 12, Inner cuticle surface. 13, Outer cuticle surface. Bar = 30 μm.

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near the base of the seed cone on the two sides. Seed scale woody, flattened, and oblong to lanceolate or long ovate, 14 ± 3 mm long, 6 ± 2 mm wide. Apex of seed scales blunt or obtuse, somewhat recurved with a short thorn- or bulge-like triangular mucro, ca. 1 mm long (Plate IV, 1–2). Bract scales round or oval, 3 ± 2 mm long, 2 ± 1 mm wide, with obtuse apices (Plate IV, 3–4). 4. Discussion 4.1. Taxonomic treatment The typical features of the fossil leaves: lateral branches covered by scale-like leaves or by decurrent leaf bases, leaves opposite in four ranks, deltate to scale-like, decurrent and appressed, indicate that these fossils can be assigned to the family Cupressaceae (Watson and Eckenwalder, 1993; Fu et al., 1999). Some features, such as leafy shoots with opposite or whorled phyllotaxis, reduced to appressed scale-like leaves, suggest that the present fossils can be assigned to Cupressoideae, which is one of the seven subfamilies in Cupressaceae (Gadek et al., 2000). The current fossils cannot be assigned to the following seven of ten genera of the Cupressoideae because of their gross morphological

features. Tetraclinis Masters differs in having whorls of four leaves (Gadek et al., 2000), whereas our fossil material shows an opposite, decussate phyllotaxy. Cupressus L. and Juniperus L. have axillary branchlets arising on all sides of the stem (Gadek et al., 2000), but the current fossils have branchlets restricted to one plane. In Microbiota Komarov, mature foliage leaves are monomorphic (Watson and Eckenwalder, 1993; Gadek et al., 2000), while they are dimorphic in our fossil material. Chamaecyparis Spach has similar facial and lateral leaves (Watson and Eckenwalder, 1993), but they are clearly differentiated in our fossil material. Thuja L. has clearly opposite leaves in four ranks (Watson and Eckenwalder, 1993), but in our fossil material they are apparently in whorls of four. Thujopsis Siebold et Zuccarini ex Endlicher differs in having lateral leaves being 4–7 mm long (Fu et al., 1999), while in our material most leaves are less than 4 mm long. The other three genera in the subfamily Cupressoideae, Fokienia Henry et Thomas (Plate V, 1, 6), Platycladus Spach (Plate V, 2, 7) and Calocedrus (Plate V, 3, 4, 5, 8, 9, 10), show gross morphological features that are generally comparable with those of the here described foliage shoots (Plate II, 5–7), but the epidermal structures are rather different (Plate VI, 1–12). Fokienia has stomata that share subsidiary cells (Plate VI, 1–4), whereas our fossil specimens have more sparsely spaced stomata that rarely share subsidiary cells (Plate III, 2, 12, 13).

Plate V. Comparisons of leaf morphology of Fokienia hodginsii (1, 6), Platycladus orientalis (2, 7), Calocedrus decurrens (3, 8) and Calocedrus macrolepis (4, 9, 5 and 10), showing similar in gross features which are generally comparable with the present foliage shoots. Bar = 1 mm. 1–5. Upper side of foliage shoot. 6–10. Lower side of foliage shoot. 1 and 6. 2 and 7. 3 and 8. 4 and 9. 5 and 10.

Fokienia hodginsii. Flattened dorsiventrally, foliage shoot with upper side (convex) differs from lower side (concave). Platycladus orientalis. Slightly flattened leafy shoots, foliage shoot with upper side similar to the lower side. Calocedrus decurrens. Slightly flattened leafy shoots, weakly dimorphic leaves, foliage shoot with upper side similar to the lower side, branchlet segment thin and slim, margins of two lateral leaves in a segment being parallel. Calocedrus macrolepis var. formosana. Bifacial flattened, foliage shoot with upper side (convex) differs from lower side (concave). Calocedrus macrolepis var. macrolepis. Bifacial flattened, foliage shoot with upper side (convex) differs from lower side (concave), branchlet segment wedge-shaped in outline, strongly dimorphic leaves, and margins of two lateral leaves in a segment contact near the base area.

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Plate VI. Epidermal structures. 1–4.

5–8. 9–12.

Fokienia hodginsii. 1. Showing higher number of stomata in the stomatal bands. Bar = 200 μm. 2. In stomatal zone, stomata sharing subsidiary cells, strongly papillate and forming Florin rings, cells papillate. Bar = 50 μm. 3. Inner cuticle surface, showing stomatal zone strongly uneven, with concavities of variable shape and size. Bar = 50 μm. 4. Outer cuticle surface, showing the outward projecting papillae forming Florin rings. Bar = 100 μm. Platycladus orientalis. 5. Stomata irregularly arranged. Bar = 100 μm. 6. Florin ring around the stomatal pit. Bar = 50 μm. 7. Inner cuticle surface, guard cells sunken. Bar = 10 μm. 8. Outer cuticle surface, showing Florin rings. Bar = 20 μm. Calocedrus decurrens. 9. Stomatal band and regularly arranged epidermal cells. Bar = 100 μm. 10. Florin rings around stomatal pits, cells strongly papillate in stomatal zone. Bar = 50 μm. 11. Inner cuticle surface, showing sunken guard cells and papillate pits. Bar = 20 μm. 12. Outer cuticle surface, showing Florin rings and papillae. Bar = 20 μm.

Platycladus differs by lacking outward projecting papillae on the epidermal cells of the stomatal zone on the outer surface (Plate VI, 5–8), whereas the epidermal cells of the stomatal zone in our fossil material, especially those near the base of leaves, are strongly papillate (Plate III, 10–13).

The morphological (Plate II, 1–7) and epidermal features (Plate III, 1–13) of the here described fossil leaves mostly resemble those of the extant genus Calocedrus (Plate V, 3–5 and 8–10; Plate VI, 9–12) (Watson and Eckenwalder, 1993; Fu et al., 1999; Gadek et al., 2000), and thus suggest an assignment to Calocedrus.

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Table 1 Comparisons of Calocedrus shengxianensis with the extant species of the genus.

Leafy shoot Branchlet segment Shape Length (mm) Width (mm) Length/Width Leaf formation Lateral leaf Shape Apex Base Facial leaf Shape Apex Height Stoma distribution

Seed cone Number of scales Size (mm) References

C. shengxianensis

C. macrolepis

C. rupestris

C. decurrens

Upper side convex, lower concave

Upper side convex, lower concave

Both upper and lower sides uniform

Both upper and lower sides uniform

Wedge-shaped 2.5 ± 0.8 2.1 ± 0.4 ca. 1.2 Strongly dimorphic

Wedge-shaped 3–5 2–3 from b2 to N2 Strongly dimorphic

Wedge-shaped to oblong 2–6 3–4 b2 Strongly dimorphic

Oblong 3–14 2–3 2 or more Weakly dimorphic

Falcate Blunt, incurved, adhere to facial leaf

Falcate Acute, incurved, free

Contact

Contact

Oblong Obtuse, incurved, adhere to facial leaf Contact or free

Boat-shaped Acute to blunt, incurved, free Free

Inversely triangular

Long rhombus

Long rhomboid

Appear blunt or flattened About same or a little higher to lateral leaf Hypostomatic on upper side of facial leaf, continuous on lower side of abaxial cuticle in lateral leaf, lack on upper side of abaxial cuticle in lateral leaf

Inversely triangular or oblong Acute or acuminate Obtuse or flattened About same or a little lower to lateral leaf Higher to lateral leaf Hypostomatic on upper side of facial leaf, – continuous on lower side of abaxial cuticle in lateral leaf, lack on upper side of abaxial cuticle in lateral leaf

6 14 ± 3 × 6 ± 2 He et al., 2012; This paper

6 10–20 × 4–6 Fu et al. (1999)

6 17–30 (20–35) × 4–6 Thieret (1993); Farjon (2005)

The associated impression of seed cones (Plate IV, 1–4) which show similar morphological features of the extant genus Calocedrus confirms this assignment. The present seed cones are composed of more than three fertile scales. The bract scales attached near the bases of the seed cones, and the bilaterally symmetrical ovuliferous scales are the features that only occur in the Coniferales. Bracts enveloped by cone scales, being free only at the apices, 3–16 peltate, oblong to cuneate cones scales, are typical for Cupressaceae (Watson and Eckenwalder, 1993; Fu et al., 1999). Features, such as ellipsoid seed cones, dehiscence when having reached maturity, two or three pairs of seed cone scales, woody, basifixed, flattened, oblong cone scales being less than 12 mm in diameter suggest an assignment of the present fossil seed cones to the genus Calocedrus (Watson and Eckenwalder, 1993; Fu et al., 1999). In the subfamily Cupressoideae, Cupressus, Juniperus, Chamaecyparis, Thujopsis and Fokienia have globose or subglobose seed cones; seed cones of Tetraclinis and Microbiota have only four scales that are arranged in two opposite pairs. Thuja seed cones have more (4–6 pairs) overlapping

4 4–6 × 2.5–4 Averyanov et al. (2005)

Acute to blunt About same to lateral leaf Amphistomatic on upper side of facial leaf, discontinuous on both upper and lower sides of abaxial cuticle in lateral leaf

scales. Platycladus seed cones have six to twelve thick scales arranged in opposite pairs (Farjon, 2005). 4.2. Comparisons with the extant species of Calocedrus The foliage of our fossil material clearly differs from that of Calocedrus decurrens (Plate V, 3 and 8; Table 1) from the western North America, one of the three extant species of the genus Calocedrus. Morphologically, the fossil leaf shoots are clearly convex on the upper and concave on the lower side (Plate II, 1–4), the branchlet segments wedge-shaped, fairly thick and stout (Plate II, 5–7), and the leaves strongly dimorphic. While in C. decurrens, its leaf shoots are similar on both upper and lower sides (Plate V, 3 and 8), its branchlet segments narrow, thin and slim, and its leaves weakly dimorphic. Additionally, the lateral leaves of fossils are in contact in the base of the segment, while they are parallel in C. decurrens (Thieret, 1993). The lateral leaves of our fossil specimens have continuous rows of stomata on the lower

Plate VII. Epidermal structures. 1–8.

Calocedrus macrolepis var. macrolepis. 1. Stomatal zone in abaxial cuticle of lateral leaf on the lower side of foliage shoot, stomata irregularly arranged, oriented longitudinally, slightly oblique. Bar = 100 μm. 2. Adaxial cuticle of lateral leaves (arrow indicated), composed of a median stomatal zone. Bar = 200 μm. 3. Abaxial cuticle of facial leaves on the lower side of shoots, composed of a median nonstomatal zone and two lateral stomatal zones. Bar = 200 μm. 4. Abaxial cuticle of facial leaf on the upper side of foliage shoot, nonstomatal. Bar = 100 μm. 5. Inner cuticle surface, showing abaxial cuticle of facial leaves (arrow indicated) on the lower side of shoots, composed of a median nonstomatal zone and two lateral stomatal zones. Bar = 400 μm. 6. Inner cuticle surface, showing adaxial cuticle of lateral leaves (arrow indicated), composed of a median stomatal zone. Bar = 200 μm. 7. Inner cuticle surface, showing a stomatal zone in abaxial cuticle of lateral leaf on the lower side of foliage shoot, stomata hardly share subsidiary cells. Bar = 40 μm. 8. Inner cuticle surface, showing abaxial cuticle of the lateral leaves on the upper side of shoots. Bar = 100 μm.

9–16.

Calocedrus macrolepis var. formosana. 9. Abaxial cuticle of the facial leaves on the lower side of shoots, composed of a median nonstomatal zone and two lateral stomatal zones. Bar = 500 μm. 10. Stomatal irregularly arranged, oriented longitudinally or slightly oblique. Bar = 200 μm. 11. Stomatal zone in abaxial cuticle of lateral leaf on the lower side of foliage shoot, stomata hardly share subsidiary cells. Bar = 100 μm. 12. A stomatal complex, haplocheilic and monocyclic, elliptical in outline. Bar = 50 μm. 13. Inner cuticle surface, abaxial cuticle of lateral leaf on the lower side of foliage shoot, strongly uneven, with concavities of variable shape and size. Bar = 20 μm. 14. Outer cuticle surface, showing the Florin rings and outward projecting papillae. Bar = 20 μm. 15. Inner cuticle surface, showing a stomatal complex, elliptical in outline. Bar = 10 μm. 16. Outer cuticle surface, showing abaxial cuticle of the lateral leaves on the upper side of shoots, cells regularly arranged. Bar = 50 μm.

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Plate VII

11

12

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side of the abaxial cuticle (Plate III, 1, 2, 7) and lack of stomata on upper side of the abaxial cuticle (Plate III, 1, 7). However, the lateral leaves of C. decurrens have a few discontinuous rows of stomata on both upper and lower sides of abaxial cuticle (Plate VI, 9–12). In addition, the current associated seed cones are smaller (14 ± 3 mm long) than those of C. decurrens (17–30 mm long) (Thieret, 1993). The present fossils differs distinctly from the eastern Asian species Calocedrus rupestris in having narrowed leaf apices and larger seed cones (14 ± 3 mm long) (Table 1), in the latter, its leaf apices are broadly obtuse and the seed cones are only 4–7 mm long (Averyanov et al., 2005). The present fossils show most similarities with the extant species Calocedrus macrolepis (Table 1), of which two varieties have been described, C. macrolepis var. formosana (Florin) Cheng et Fu (Plate V, 4 and 9) and C. macrolepis var. macrolepis Kurz (Plate V, 5 and 10). The two varieties differ slightly in the shape of the seed-cone-bearing branchlets (Fu et al., 1999). The fossil specimens show the same morphological features as the extant species, i.e. clearly convex leafy shoots on the upper side and concave ones on the lower side, wedge-shaped and less than 4 mm long branchlet segments, strongly dimorphic leaves, the margins of two lateral leaves in a segment being in contact near the base, and flattened facial leaves (Plate II, 5–7; Plate V, 5 and 10). The epidermal structures also show similarities, i.e. hypostomatic facial leaves on the upper side of the shoots, lateral leaves with continuous rows of stomata on the lower side of the abaxial cuticle (Plate III, 1–13; Plate VII, 1–16). The associated impression of the fossil seed cones (Plate IV, 1–4) show a similar morphology as C. macrolepis and have the same size (Fu et al., 1999). The present fossils differ from the extant species mainly in the leaf apices (Table 1). In the extant C. macrolepis, both facial and lateral leaves have acute or acuminate apices (Plate V, 4, 5, 9, 10; Fu et al., 1999), whereas the fossil specimens appear to have only blunt leaf apices (Plate II, 5–7). In the extant species, the incurved lateral leaves have free apices (Plate V, 4, 5, 9, 10), the upper margins of facial leaves being lanceolate or ‘W’-shaped, whereas the lateral leaves of the fossils do not have free apices and the incurved apices adhere to the facial ones (Plate II, 5–7), the top margins of facial leaves are flattened or arc-like. In the extant species, the lateral and facial leaves have the same length, whereas in the fossil specimens the facial leaves are slightly longer than the lateral ones. Because of the poor preservation of the seed cones, further comparisons between the fossils and extant species cannot be made. Based on the above comparisons, the current fossils, although bearing close affinity to the extant Calocedrus macrolepis, apparently belong to an extinct species. 4.3. Comparisons with the fossil species of Calocedrus Four fossil species of Calocedrus have been described with preserved epidermal structure (Table 2). Calocedrus robustior Kvaček et Rember from the middle Miocene of Idaho, northwestern USA, is represented by seed cones and cone stalks with attached leaves (Kvaček and Rember, 2007). The present fossils show similarities to this species in having dimorphic leaves and flattened foliage sprays, but differ in lack of free apices in lateral leaves and (or) acute apices in facial leaves as well as the epidermal features (Table 2). The seed cones of the Wenshan fossils, which show characteristics of Calocedrus macrolepis, differ clearly from those of C. robustior; seed cones of C. robustior are similar to those of Calocedrus decurrens from western North America (Kvaček and Rember, 2007). Calocedrus pliocaenica (Kinkelin) Kvaček (al. Libocedrus pliocaenica Kinkelin) from the Pliocene of the Rhineland, Germany, and Poland has vegetative shoots bearing scale-like leaves (Mädler, 1939; Kvaček, 1999). Our fossils show clear differences with this species in morphological as well as epidermal features (Table 2). Calocedrus suleticensis (Brabenec) Kvaček from the lower Oligocene to lower Miocene of central and southern Europe, is represented by twig fragments with scale-like leaves, an associated seed cone and a seed

(Kvaček and Hably, 1998; Kvaček, 1999). The present fossils are similar to this species in having blunt leaf apices, falcate or boat-shaped lateral leaves, facial leaves with widely triangular tips, but differ in the branching mode and the length of branchlet segments (Table 2). The here described seed cones from Wenshan differ from those from Europe in lacking a subterminal mucro in the basal pair of cone scales (Kvaček, 1999). Calocedrus huashanensis Shi, Zhou et Xie was described recently from the Oligocene of South China, and consists of vegetative shoots bearing scale-like leaves (Shi et al., 2012). The new fossil specimens show similarities with this species in having flattened foliage shoots, alternate branches, strongly dimorphic leaves, but differ clearly in the shape of the branchlet segments, in lacking free acute apices in the lateral leaves and the contacted bases of the lateral leaves in a branchlet segment (Table 2). Other fossils assigned to Calocedrus, show morphological features similar to the present Calocedrus shengxianensis but their epidermal features are still unknown. Calocedrus schornii Meyer et Manchester was established on the basis of leafy shoots and an ovulate cone from the Oligocene of Oregon, USA (Meyer and Manchester, 1997). The new fossils show similarities to this species in having dorsiventrally flattened branchlet, dimorphic lateral and facial leaves, but differ in the size of leaves and the seed cones, and the morphological features of leaf apices (Table 2). Calocedrus lantenoisi (Laurent) Tao is based on leafy shoot fragments from the Oligocene to Pliocene of Yunnan, SW China (WGCPC, 1978; Guo, 2011). Our new fossils differ from C. lantenoisi in the morphology of the leaf apices (Table 2). Calocedrus notoensis (Matsuo) Huzioka from the Miocene of Japan (Onoe et al., 1985) and Korea (Huzioka, 1972) is represented by foliated shoots. This species is comparable to the Wenshan species in bearing flattened foliage shoots, alternate branches, dorsiventrally flattened branchlet, strongly dimorphic leaves with blunt leaf apices (Onoe et al., 1985). The present fossils differ from this species mainly in the shape of the lateral leaves and the morphology of leaf apices (Onoe et al., 1985; Table 2). The above comparisons show the typical difference of the present Calocedrus shengxianensis to the previously described Calocedrus fossils. 4.4. Reassignment of Fokienia shengxianensis Shoots with scale-like, decussate leaves from the upper Miocene of Zhejiang Province in SE China, named Fokienia shengxianensis were described by He et al. (2012). These fossils show typical features of Cupressoideae, e.g., an opposite or whorled phyllotaxy and reduced to appressed scales (Gadek et al., 2000; He et al., 2012). The leaf branches of Fokienia shengxianensis spread in flattened sprays, the decussate leaves are dimorphic and almost in whorls of four; lateral leaves generally less than 4 mm long and overlapping margins of facial ones (He et al., 2012). As discussed above, these fossils fall in the range of three genera in Cupressoideae: Platycladus, Fokienia and Calocedrus (Watson and Eckenwalder, 1993; Fu et al., 1999; Gadek et al., 2000). Because of strongly papillate epidermal cells in the stomatal zone in these foliaged shoots (He et al., 2012), these fossils cannot be assigned to Platycladus, in the latter genus the epidermal cells in the stomatal zone lack papillae (Plate VI, 5–8). In Fokienia and Calocedrus, epidermal cells in the stomatal zone are strongly papillate (Plate VI, 1–4, 9–12). These foliaged shoots were assigned to the genus Fokienia based on the slightly incurved apices of lateral leaves, the lateral leaves overlapping margins of the facial leaves, the hypostomatic nature of the leaves, the quadrangular, rectangular to elongate-rectangular outlines of the epidermal cells, the straight anticlinal walls, the square end walls, the cyclocytic, elliptical stomatal apparati, and the papillae around the stomata (He et al., 2012). As discussed above, all these features also occur in Calocedrus. Therefore, the assignment of these foliaged shoots to the genus Fokienia can be questioned. However, the descriptions and illustrations of He et al. (2012) indicate that stomata are loosely spaced and rarely share subsidiary cells in Fokienia shengxianensis. These characters are found in

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13

Table 2 Comparisons of Calocedrus shengxianensis with the fossil species of the genus. C. shengxianensis

C. schornii

C. notoensis

C. huashanensis

C. suleticensis

C. robustior

C. pliocaenica

C. lantenoisi

Alternate

Alternate

Alternate

Alternate

Opposite

Alternate

Alternate

–

Wedge-shaped b4

Wedge-shaped Wedge-shaped Oblong 4–5 b4 6.8

Wedge-shaped 2

Wedge-shaped 3–4

Wedge-shaped –

– –

Falcate Blunt, incurved, adhere to facial leaf Contact

Falcate Acute, incurved, free Free

Spindly Blunt, tapers upwards, free –

Falcate Acute, tapers upwards, free Free

Falcate Blunt, tapers upwards, free –

Falcate Blunt to apiculate, incurved, free Free

Falcate Acute, tapers upwards, free –

Falcate Acute to acuminate –

Rhomboidal Acute to acuminate –

Rhomboidal Blunt

Obtrullate Acute

Rhomboidal Blunt

Rhomboidal Acute

– –

–

–

Oligocene

Miocene

Absent on upper side of abaxial cuticle in lateral leaf Oligocene

Present on upper side of abaxial cuticle in lateral leaf Middle Miocene

Present on upper side of abaxial cuticle in lateral leaf Pliocene

– Acute to acuminate –

Age

Inversely triangular Appear blunt or flattened Absent on upper side of abaxial cuticle in lateral leaf Late Miocene

Distribution

China, Eastern Asia

Oregon, North America

Korea, Japan, Eastern Asia

China, Eastern Asia

Idaho, North America

Poland, Germany, Europe

Oligocene to Pliocene China, Eastern Asia

Literature

This text

Meyer and Manchester (1997)

Huzioka (1972); Onoe et al. (1985)

Shi et al. (2012)

Kvaček and Rember (2007)

Mädler (1939); Kvaček (1999); Shi et al. (2012)

WGCPC (1978); Guo (2011)

Branch arrangement Branchlet segment Shape Length (mm) Lateral leaf Shape Apex Adjacent base Facial leaf Shape Apex Stoma distribution

Calocedrus. In the extant Fokienia species, the stomata in stomatal zones are densely spaced and share subsidiary cells (Plate VI, 1–4). The comparisons of the Zhejiang fossils with the present new specimens from Yunnan Province show identical characteristics in the morphology of leafy shoots, leaves and epidermal structures that are more typical for Calocedrus than for Fokienia. Therefore it can be concluded that they belong to the same species and that F. shengxianensis must be transferred to Calocedrus. 4.5. Climatic change and the evolution of Calocedrus in the Neogene of South China Based on the discussions above, the late Miocene Calocedrus shengxianensis shows a close affinity to the extant Calocedrus macrolepis and is found in Tiantai County (Zhejiang Province) and Dashidong Village (Yunnan Province) in South China. However, the modern C. macrolepis is now restricted to central-southwest Yunnan, southeast Guizhou, Hainan and Taiwan (Fu et al., 1999; Fang et al., 2011). This modern distribution pattern is probably related to the climatic change in eastern Asia since the late Miocene. The studies (Tanai, 1967; Wolfe, 1978; Graham, 1999) have shown that the global climate had undergone severe change after the midMiocene warm interval, especially in eastern Asia owing to the uplift of the Qinghai–Tibet Plateau (Harrison et al., 1992; Molnar et al., 1993; Harrison and Mahon, 1995; Mulch and Chamberlain, 2006). The uplift events have led to the amplification of the dry–wet seasonal

Oligocene to early Miocene Hungary, Bohemia, Central and southern Europe Kvaček and Hably (1998); Kvaček (1999)

contrast of the eastern Asia monsoons (Li, 1999; An et al., 2001; Jacques et al., 2011; Zhang et al., 2012). Former studies on the paleoclimatic implications of Wenshan flora have given controversial results. Xia et al. (2009) regarded the climate to have been warmer and more humid based on the studies of the upper Miocene Xiaolongtan Flora. Su et al. (2013) considered that this area had has cooler and drier climate based on the occurrence of Ailanthus confucii Unger, Anberrée et al. (2015) inferred a higher mean annual temperature and precipitation seasonality with a dry winter and a wet summer based on the occurrence of Burretiodendron. Li et al. (2015) thought that the climate was cooler but more humid than today based on palynological studies. Studies of the gymnosperms from the Wenshan flora, e.g., Sequoia (Zhang et al., 2015a), Pinus massoniana (Zhang et al., 2015b), indicate that the climate in Wenshan during the late Miocene climate of Wenshan was more humid as today. The close morphological resemblance of Calocedrus shengxianensis to Calocedrus macrolepis would suggest similar habitats (Pittermann et al., 2012; Thiel et al., 2012). The modern C. macrolepis grows mostly in mountains, in the areas with MAT (Mean Annual Temperature) 17.9 °C (Table 3), MTCM (Mean Temperature of the Coldest Month) 10.2 °C, MTWM (Mean Temperature of the Warmest Month) 24.1 °C and AP (Annual Precipitation) 1362 mm, PWQ (Precipitation of Warmest Quarter) 638 mm, PCQ (Precipitation of Coldest Quarter) 88 mm (Fang et al., 2011). The climate in Dashidong Village today has a MAT 18.1 °C, MTCM 10.6 °C, MTWM 23.3 °C and AP 1044 mm, PWQ 553 mm, PCQ 45 mm; in Tiantai County has a MAT 17.1 °C, MTCM

Table 3 Comparisons of the climate between late Miocene Xiaolongtan, Wenshan, Tiantai and the extant distribution areas of Calocedrus macrolepis. Location Late Miocene

Xiaolongtan Wenshan Tiantai Extant Wenshan Tiantai Extant distribution of C. macrolepis

MAT (°C)

MTCM (°C)

MTWM (°C)

AP (mm)

PWQ (mm)

PCQ (mm)

References

16.7–19.2 16.6–17.5 9.9–19.7 18.1 17.1 17.9 (14.3–24.3)

7.7–8.7 2.4–5.5

25.4–26.0 27.5–29.7

827.8 608.3–729.9

210.3 76.1–178.9

10.6 5.9 10.2 (4.0–18.7)

23.3 28.7 24.1 (19.6–28.7)

1215–1639 1432.3–1598.9 1117.7–1564.4 1044 1483 1362 (868–2993)

553 545 638 (312–1186)

45 177 88 (28–547)

Xia et al. (2009) Li et al. (2015) Ren et al. (2010) Climate-Data.Org. Climate-Data.Org. Fang et al. (2011)

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5.9 °C, MTWM 28.7 °C and AP 1483 mm, PWQ 545 mm, PCQ 177 mm (Climate-Data.Org.). Based on these data (Table 3), the climate would become drier and have warmer winter and cooler summer in Dashidong Village, and become even warmer in summer and cooler in winter in Tiantai since the late Miocene. This would probably be the reasons that lead to the disappearance of Calocedrus shengxianensis (or its relatives) from these areas. Climatic change would drive adaptive shifts within species, and leaf morphology has demonstrated links with climate and varies within species along climate gradients (Walther et al., 2002). Morphological responses and shifts would occur over time due to climatic change (Byars et al., 2007; Guerin et al., 2012). The comparisons of the climate between the late Miocene of Wenshan (Tiantai) and the extant distribution areas of Calocedrus macrolepis show that the MAT has not changed greatly (Table 3), both AP and PWQ , PCQ of the extant distribution are higher than that of the late Miocene. Based on the above analysis, the humid climate and the acute or acuminate leaf apices in the modern species of C. macrolepis compared to the blunt or obtuse ones in the late Miocene Calocedrus shengxianensis would suggest that: the climatic change has led to leaf morphological responses and shifts, the acute or acuminate leaf apices in the modern species C. macrolepis would have evolved probably to adapt to this humid climate since the late Miocene. 5. Conclusions In this paper, a late Miocene species of the relict conifer Calocedrus Kurz, Calocedrus shengxianensis, is described from South China. This fossil species shows most of similarities with the modern eastern Asian Calocedrus macrolepis Kurz. The differences between them lie primarily in the morphological features of the apex of lateral and (or) facial leaves. For example, the modern species has acute leaf apices, while the fossil one has blunt or obtuse leaf apices. With the global cooling and the uplift of the Qinghai–Tibet Plateau, the climatic change has led to morphological shifts of the leaves in this area: the acute or acuminate leaf apices in the modern C. macrolepis compared to the blunt or obtuse ones in the late Miocene C. shengxianensis have evolved probably to adapt to this humid climate since the late Miocene. Acknowledgments This work was supported by the National Natural Science Foundation of China (41372035). The authors thank Dr. Natalya Nosova from Komarov Botanical Institute of the Russian Academy of Sciences, Dr. Shi Gong-Le from Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences, for providing some references, Dr. Wang Li from Lab Center of XTBG for providing some references and for preparing the scanning electron microscope photos of cuticles. References An, Z.S., Kutzbach, J.E., Prell, W.L., Porter, S.C., 2001. Evolution of Asian monsoons and phased uplift of the Himalaya–Tibetan Plateau since late Miocene times. Nature 411, 62–66. Anberrée, J.L., Manchester, S.R., Huang, J., Li, S.F., Wang, Y.Q., Zhou, Z.K., 2015. First fossil fruits and leaves of Burretiodendron s.l. (Malvaceae s.l.) in southeast Asia: implications for taxonomy, biogeography, and paleoclimate. Int. J. Plant Sci. http://dx.doi.org/10. 1086/682166. Averyanov, L., Hiep, N.T., Loc, P.K., The, P.V., 2005. Distribution, ecology and habitats of Calocedrus rupestris (Cupressaceae) in Vietnam. Turczaninowia 8, 19–35. Axelrod, D.I., 1964. The Miocene Trapper Creek flora of southern Idaho. Univ. Calif. Publ. Geol. Sci. 51, 1–148. Axelrod, D.I., 1992. The middle Miocene Pyramid flora of western Nevada. Univ. Calif. Publ. Geol. Sci. 137, 1–50. BGMRYP (Bureau of Geology), Mineral Resources of Yunnan Province, 1996. Stratigraphy (Lithostratigraphy) of Yunnan Province. China University of Geosciences Press, Wuhan (in Chinese, with English introduction). Byars, S.G., Papst, W., Hoffmann, A.A., 2007. Local adaptation and cogradient selection in the alpine plant, Poa hiemata, along a narrow altitudinal gradient. Evolution 61, 2925–2941.

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