The occurrence of Pinus massoniana Lambert (Pinaceae) from the upper Miocene of Yunnan, SW China and its implications for paleogeography and paleoclimate

Review of Palaeobotany and Palynology 215 (2015) 57–67

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The occurrence of Pinus massoniana Lambert (Pinaceae) from the upper Miocene of Yunnan, SW China and its implications for paleogeography and paleoclimate Jian-Wei Zhang a, Ashalata D'Rozario b, Jonathan M. Adams c, Xiao-Qing Liang a, Frédéric M.B. Jacques a, Tao Su a, Zhe-Kun Zhou a,⁎ a b c

Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden (XTBG), Chinese Academy of Sciences, Mengla, Yunnan 666303, China Department of Botany, Narasinha Dutt College, 129, Bellilious Road, Howrah 711101, India The college of Natural Sciences, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 151-742, Republic of Korea

a r t i c l e

i n f o

Article history: Received 11 August 2014 Received in revised form 12 November 2014 Accepted 15 November 2014 Available online 15 December 2014 Keywords: China Comparative morphology Fossil Late Miocene Phytogeography Pinus massoniana

a b s t r a c t A fossil seed cone and associated needles from the upper Miocene Wenshan flora, Yunnan Province, SW China are recognized as Pinus massoniana Lambert, which is an endemic conifer distributed mostly in southern, central and eastern parts of China. The comparisons of these fossils with the three extant variants in this species (P. massoniana var. shaxianensis Zhou, P. massoniana var. massoniana Lambert and P. massoniana var. hainanensis Cheng et Fu) indicate that the fossils closely resemble P. massoniana var. hainanensis, which is a tropical montane thermophilic and hygrophilous plant restricted to Hainan Island in southern China. The present finding and a previous report of Pinus premassoniana from the same age in southeastern China, which bears close affinities with modern P. massoniana var. massoniana, suggest that the variation in this species arose earlier than was previously thought. Thus, the presence of P. massoniana var. hainanensis in the late Miocene Wenshan flora, Yunnan Province in southwestern China suggests (1) the subdifferentiation of P. massoniana began in the late Miocene or earlier; (2) the extant distribution of P. massoniana var. hainanensis might be derived from northern populations – the major distribution of extant P. massoniana – by southward expansion during Neogene or Quaternary climate changes; (3) disappearance of P. massoniana from southeastern Yunnan in southwestern China is probably related to the intensification of monsoon climate after the late Miocene. © 2014 Elsevier B.V. All rights reserved.

1. Introduction The genus Pinus contains ca. 110 species of evergreen conifers with needlelike leaves. It is widespread in north temperate and north tropical (mountainous) regions, with species found in North America, Central America, Mexico, North Africa, West Indies, Eurasia (including one species crossing the equator in Sumatra) and the Pacific Islands in Sumatra (Kral, 1993). In China, there are 39 species of Pinus (Fu et al., 1999). Pinus massoniana Lambert, a species with long slender needles of about 12–20 cm, is endemic in China and distributed mostly in southern, central and eastern parts of the nation, from a few hundred to 2000 m in moist river valleys to the dry mountain plateaus (Fu et al., 1999). Some populations of P. massoniana are also found on Taiwan (eastern China) and Hainan Island (southern China), but the paleogeographical evidence for this distribution pattern is lacking. Based on the morphological features, such as vascular bundles in a needle, persistent fascicle sheaths, needle number per fascicle, needle resin ducts, cone scale, umbo prickle, seed wing and umbo position, the ⁎ Corresponding author. Tel./fax: +86 691 8715070. E-mail address: [email protected] (Z.-K. Zhou).

http://dx.doi.org/10.1016/j.revpalbo.2014.11.006 0034-6667/© 2014 Elsevier B.V. All rights reserved.

extant genus Pinus was classified into two subgenera, four sections and eleven subsections (Krupkin et al., 1996; Price et al., 1998; Gernandt et al., 2005). Subgenus Pinus L. is distinguishable by two fibrovascular bundles per needle with persistent fascicle sheaths, except for Pinus leiophylla Schiede ex Schlechtendal et Chamisso and Pinus lumholtzii Rob et Fernald, subgenus Strobus (D. Don) Lemon by a single fibrovascular bundle per needle with deciduous fascicle sheaths, except for Pinus nelsonii Shaw, and the dorsal umbo position delineates subsection Strobus Loudon (terminal umbo) from all other pines. In this classification (Gernandt et al., 2005), Pinus massoniana and 16 species found mainly from Eurasia and the Mediterranean region, were assigned to subsection Pinus sensu Gernandt, Geada López, Ortiz García et Liston in section Pinus sensu Gernandt, Geada López, Ortiz García et Liston of subgenus Pinus. Klaus (1980, 1989) has given another classification of Pinus based on the location and morphological features of the mucro on the cone scales. His approach matches the basic frame of existing classification systems (Klaus, 1980, 1989). He subdivided the subgenus Pinus into two different groups: centromucronate with the mucro located in the center of the umbo and excentromucronate with the mucro situated above the transverse keel. The excentromucronate species are further divided into four groups: denticulatomucronate

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with a long mucro positioned on the upper edge of the umbo field, perexcentromucronate with one short mucro positioned near the upper edge of the umbo, erectoexcentromucronate with a long mucro arising just a little above the transverse keel, and duplomucronate characterized by an excentric mucro and an additional central protuberance on the horizontal keel, a combination of a centro- and an excentromucronate umbo (Klaus, 1980, 1989). Centromucronate umbos are often present in the American pines and excentromucronate umbos occur in all the Eurasian pines (Klaus, 1989). Pinus massoniana and six other species from eastern Asia, the Mediterranean and eastern North America, which bear a short mucro situated near the upper edge of the umbo, are perexcentromucronate (Xing et al., 2010; Ding et al., 2013). The origin of genus Pinus is thought to be Early Cretaceous (Millar, 1998; Ryberg et al., 2012), whereas the estimated divergence times of the two subgenera range from the Late Cretaceous (Millar, 1998) to the middle Eocene (Miller, 1976). The earliest known Pinus fossils are permineralized cones from the Wealden of Belgium (Alvin, 1960) and Yorkshire (Ryberg et al., 2012), which show affinities to the subgenus Pinus (Miller, 1976; Willyard et al., 2007). The earliest fossils of the subgenus Strobus are Late Cretaceous permineralized wood (Meijer, 2000), while the earliest leaves (Miller, 1973) or ovulate cones (Axelrod, 1986) of the subgenus are reported from the middle Eocene. Hitherto, over 50 fossil species of Pinus have been described in the world (Ding et al., 2013). In China, six fossil species have been described from Cenozoic sediments. Among them, five (Pinus yunnanensis Franch, Pinus speciosa Li, Pinus prototabulaeformis Tao et Wang, Pinus prekesiya Xing, Liu et Zhou and Pinus premassoniana Ding et Sun) were established at least on the basis of seed cones (Tao and Kong, 1973; NIGMR, 1982; Tao and Wang, 1983; Xing et al., 2010; Ding et al., 2013), and Pinus palaeopentaphylla Tanai et Onoe was based on needles (Guo and Zhang, 2002). The global climate underwent severe changes after the middle Miocene warm interval (Tanai, 1967; Wolfe, 1978; Graham, 1999), e.g., global cooling (Zachos et al., 2001; Mosbrugger et al., 2005), especially in eastern Asia owing to the uplift of the Tibetan Plateau (Harrison et al., 1992; Molnar et al., 1993; Harrison et al., 1995; Mulch and Chamberlain, 2006). The uplift of the Tibetan Plateau had not only caused changes in the regional landforms, climate and biodiversity of China, but also led to the amplification 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). These climate changes have led to the contraction of thermophilic conifers in eastern Asia (Wang and Ge, 2006). Shoots with attached needles and seed cones of Pinus premassoniana have been reported from the upper Miocene of eastern Zhejiang Province, southeastern China (Ding et al., 2013). In this paper, new fossils of Pinus massoniana, which were found from the upper Miocene of southeastern Yunnan, southwestern China, are described. These remains include a three dimensional seed cone and associated needles which have well preserved cuticles. This finding is significant in the discussion of the early differentiation among this species. We also discuss its paleophytogeographical implications and the possible causes of the disappearance of this species from southeastern Yunnan, southwestern China. 2. Material and methods

Based on the geological survey (Zhang, 1976; Cai and Li, 2002), the Neozoic sediments of the study area (Wenshan State located in SE Yunnan Subregion of South China Region) is composed of Paleogene Yanshan Group, Neogene Xiaolongtan Formation and Quaternary strata. The molasses formation of Yanshan Group is composed of coarse clastic rocks, heavy layer and lack fossils. Xiaolongtan Formation is the only fluvio-lacustrine sediment in the study area, composed of laminated sedimentary sequences, and contains abundant animal and plant fossils. Exposure of the Xiaolongtan Formation around Wenshan State is about 200–300 m thick, and generally divided into three members: the Upper Member (about 41.3 m thick, is missing in the present fossil locality, and distributed mostly in Maguan County in south of Wenshan State) is composed of thin layers (b0.1 m) of gray to white-gray marlite; the Middle Member (65.6 m thick here) consists of thin to medium layers (b 0.5 m) of gray-green to gray-yellow mudstone or fine sandstone, with interlayers of coal; and the Lower Member (27.1 m thick here) comprises medium layers (0.1–0.5 m) of gray to dark-gray conglomerate or sandstone. The present fossils were collected from the Middle to Lower Members (92.7 m) of the formation which lie primarily around Wenshan City (Zhang, 1976; Zheng et al., 1999; Fig. 2). The Xiaolongtan Formation is late Miocene in age based on lithology, biologic assemblage and regional comparisons (Dong, 1987; BGMRYP, 1996). It lies unconformably above the upper Oligocene Yanshan Group and is overlain unconformably by Quaternary strata (Zhang, 1976). The sedimentary sequences in Dashidong Village in Wenshan City yield abundant plant fossils, such as Quercus, Salix, Dryophyllum, Ulmus, Zelkova, Ampelopsis, Populifolia, Glyptostrobus (Zhang, 1976), Ailanthus confucii Unger (Su et al, 2013), Bauhinia wenshanensis Meng et Zhou (Meng et al., 2014), Sequoia maguanensis Zhang et Zhou and Pinus, and fossil fish and insects (mosquitos, ants, etc.). 2.2. Fossil specimens The fossils described here consist of a three-dimensionallypreserved seed cone (DMS 0135) and associated compressions of needles (DMS 0136-0137). 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 (Nikon, Kanagawa, Japan) under tungsten light. Some specimens were immersed in kerosene to enhance details. Detailed structures of these specimens were observed and photographed under a Leica S8AP0 stereoscope microscope (Leica, Wetzlar, Germany). The cone and needles 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, and photographed under Leica DFC295 and Zeiss EVOLS10 scanning electron microscope (Carl Zeiss, Jena, Germany). 3. Results 3.1. Systematics

2.1. Geological settings and age Fossils for the present study were collected from outcrops located in Dashidong Village (23°15′N, 104°15′E, 1482 m a.s.l.), Wenshan State, 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 previously assigned to the Huazhige Formation (Zhang, 1976; BGMRYP, 1990). Recently, they have been assigned to the Xiaolongtan Formation (BGMRYP, 1996; Zheng et al., 1999).

Family: Genus: Subgenus: Section:

PINACEAE Lindley.

Pinus L. Pinus L. Pinus sensu Gernandt, Geada López, Ortiz García et Liston. Subsection: Pinus sensu Gernandt, Geada López, Ortiz García et Liston. Species: Pinus massoniana Lambert. (Plate I)

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Fig. 1. Maps showing the locality for Pinus massoniana-like fossils in SE Yunnan, SW China.

Locality: Dashidong Village, Wenshan City, SE Yunnan Province, SW China. Age and stratigraphy: Late Miocene, Xiaolongtan Formation.

observed in a stomatal row, but mostly one. Stomatal complexes are monocyclic and elliptic, 40–50 μm long and 28–36 μm wide, oriented regularly along the long axis of the needles. Two guard cells are surrounded by 4 to 6 subsidiary cells, usually with two lateral cells on each side and one terminal at each end. Guard cells are 5–10 μm long and 3–5 μm wide (Plate III, 7–8).

3.2. Description 4. Discussion The seed cone (Plate I, 1–4) is woody, elongated, cylindrical to conical in shape, about 5.0 cm long and 1.7 cm in diameter, with length to width ratio 2.9. The cone is closed, with apex tapering and the lower middle part slightly wider. Bract and seed scale complexes are helically arranged around the axis and about 19 are visible on the viewed surface, thus, the total number is about 45 ± 10. Apophyses (Plate I, 5–8) are slightly swollen or flat. In the lower part of the cone, apophyses are polygonal in shape, about 0.6 ± 0.1 cm in diameter and bear no evident transverse or longitudinal keels except for some radial ridges; while in the middle and upper part of the cone, apophyses are broadly rhombic, 0.8 ± 0.1 cm wide, 0.7 ± 0.1 cm high and bear evident transverse keels as well as radial ridges. Apophyses are avallate and umbos are dorsal, elliptic or spindle shaped, 2.5–4 mm wide, 2–3 mm high and slightly sunken (Plate I, 9–12). A short erect mucro lies above the transverse keel near the upper edge of the umbo (perexcentromucronate) (Plate I, 9–12). Cone epidermal structure (Plate I, 13–16) shows cell spindle, polygonal or irregular shaped, 5–20 μm long (mostly 17 ± 3 μm), 3–10 μm wide (mostly 15 ± 3 μm), in rows or randomly arranged. Associated leaves (Plate III, 1–4) are needlelike, in bundles of two, slightly twisted, about 12 cm long, 1 mm in diameter, with pointed tip, serrated margin and many longitudinal veins on the surface. Needles are semi-cylindrical in shape (Plate III, 3–4) with its abaxial side arched, ventral depressed to a deep groove and base covered by persistent sheath. The epidermal structure of the needles (Plate III, 7–8) shows rectangular cells, 50–200 μm in length, 10–20 μm in width, but slightly broader within the stomatal lines than between the stomatal lines, and arranged in parallel rows. Cells have undulated or sinuous anticlinal walls and vertical or oblique ends. One to two interstomatal cells were

4.1. Taxonomic treatment The Dashidong ovulate cone conforms to the genus Pinus in bearing helically arranged cone–scale complexes and ovuliferous scales that are expanded at the apex with apophyses and umbos (Miller, 1976). Based on the above description: the Dashidong cone bears umbos located on the dorsal surface of the apophyses, with short mucros above the transverse keel and near the upper edge of the umbo, characteristic of the perexcentromucronate umbo type (Klaus, 1980, 1989). In the extant genus Pinus, the perexcentromucronate umbo is only present in section Pinus in subgenus Pinus and only seven extant species (Pinus brutia Tenore, Pinus halepensis Miller, Pinus pinea L., Pinus resinosa Aiton, Pinus kesiya Gordon, Pinus yunnanensis Franchet and Pinus massoniana Lambert) (Xing et al., 2010; Ding et al., 2013). It is therefore suggested that the Dashidong cone can be assigned to section Pinus, in subgenus Pinus. 4.2. Comparison with related extant species in section Pinus The Dashidong cone bears the perexcentromucronate umbos that exist in seven extant species in section Pinus (Table 1). Among these, four species (Pinus resinosa, Pinus kesiya, Pinus yunnanensis and Pinus massoniana) are in the subsection Pinus, and three species (Pinus brutia, Pinus halepensis and Pinus pinea) in the subsection Pinaster Loudon (Gernandt et al., 2005). The Dashidong cone is distinguishable from the three Mediterranean pines in subsection Pinaster in that the Mediterranean pines possess rounded apophyses and raised umbos (Silba, 1986), while the present fossil has rhombic apophyses and sunken umbos. The Dashidong cone differs from the NE American P. resinosa

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Fig. 2. Stratigraphic column of the Xiaolongtan Fm. in Dashidong Village, showing the Pinus fossils within the bed. Revised from Zhang (1976).

in the presence of a mucro in the umbo, which is absent in the latter (Farjon, 2005; Erwin and Schorn, 2006). The apophyses in the Dashidong cone are avallate and the umbos are not encircled by a ring-like area on the dorsal surface of the apophyses; while in P. kesiya, its apophyses possess clear vallums that encircle the umbos (Erwin and Schorn, 2006). The apophyses of the current cone are transversely keeled, and the umbos are slightly sunken; whereas those of P. yunnanensis are cross keeled and somewhat protruding (Fu et al., 1999). Based on the morphological features of apophyses and umbos (Plate II, 1–8), such as apophyses rhombic, avallate and transversely keeled; umbos sunken, presence of erect mucros, as well as epidermal structures of the cone (Plate I, 13–16; Plate II, 9–11), such as cells spindle, polygonal or irregular shaped, in rows or randomly arranged, the Dashidong cone closely resembles extant Pinus massoniana (Fu et al., 1999; Table 1). The associated needles further support the identity of the Dashidong cone. The morphological features (Plate III, 1–4): two needles in a bundle, slightly twisted, about 12 cm long and 1 mm in diameter, semicylindrical in shape with abaxial surface curved and ventral depressed to a groove, margin serrated, base with persistent sheath, as well as the epidermal characters (Plate III, 7, 8): cells rectangular, arranged in parallel rows, its anticlinal walls undulated or sinuous and end ones vertical or oblique; mostly only one interstomatal cell occurring in a stomatal row; stomata oriented regularly along long axis of needles; stomatal complexes monocyclic and elliptic, are all consistent with those of extant Pinus massoniana (Plate III, 5, 6, 9–14; Fu et al., 1999). 4.3. Comparison with fossil species of Pinus In genus Pinus, there are about 17 fossil species from the Cenozoic of Eurasia and America that share similar ovulate cone morphological characters with the Dashidong fossils (Table 2). Firstly, four species, namely, Pinus prekesiya Xing et Zhou, Pinus premassoniana Ding et Sun, Pinus baileyi Axelrod emend. Erwin et Schorn, and Pinus salinarum (Partsch) Zablocki, all possess perexcentromucronate umbos. The Dashidong cone differs from P. prekesiya in lacking vallate apophyses.

Apophyses are vallate i.e., the umbos are surrounded by a vallum (Xing et al., 2010). The Dashidong cone differs slightly from P. premassoniana in cone shape; the former is elongated, cylindrical to conical in shape, while cones of P. premassoniana are conical in shape (Ding et al., 2013). The Dashidong cone bears flattened or slightly sunken umbos, which differs from the protruding umbos in the species of P. salinarum (Mai, 1986) and P. baileyi (Erwin and Schorn, 2006). Secondly, the Dashidong cone is perexcentromucronate, with short mucros occurring above the transverse keel and near the upper edge of the umbo, which is different from six species that are denticulatomucronate, namely, Pinus hampeana (Unger) Heer, Pinus nodosa Ludwig, Pinus speciosa Li, Pinus ornata (Sternberg) Brongniart, Pinus dixoni (Bowerbank) Gardner and Pinus urani (Unger) Schimp. These six species have long mucros positioned on the upper edge of the umbo (NIGMR, 1982; Mai, 1986; Teodoridis and Sakala, 2008). Thirdly, the Dashidong cone differs from Pinus brevis Ludwig and Pinus spinosa Roezl, which are erectoexcentromucronate (i.e., having a long mucro arising just a little above the transverse keel), and Pinus engelhardtii Menzel, a centromucronate form, which has the mucro located in the center of the umbo (Mai, 1986). Pinus driftwoodensis Stockey (Stockey, 1983) and Pinus princetonensis Stockey (Stockey, 1984) are cylindric seed cones, but their mucro positions are not demonstrated in the descriptions, and their umbos are protruding rather than sunken. Cones of Pinus arnoldii Miller are conical with protruding umbos (Miller, 1973; Stockey, 1984; Klymiuk et al., 2011), which is different from the new cone. Pinus parabrevis Kilpper also has sunken umbos, but its seed cones are asymmetrical and ovoid in shape (Mai, 1986). 4.4. Differentiation of Pinus massoniana in the late Miocene or earlier Three variations among extant Pinus massoniana have been recognized based on the differences in morphological features of seed cones (Fu et al., 1999). P. massoniana var. shaxianensis Zhou is distinguishable from the other two variations by its typical spiny umbos, while the other two usually have flattened umbos. P. massoniana var. shaxianensis is found in Shaxian County, in central Fujian Province of southeastern China. P. massoniana var. massoniana Lambert can be distinguished from P. massoniana var. hainanensis Cheng et Fu by its ovoid or conicalovoid seed cones, the latter has elongated, ovoid-cylindric seed cones (Cheng et al., 1975; Cheng and Fu, 1978). P. massoniana var. massoniana is the most common variation in China, and has the largest distribution in eastern, central and southern China. P. massoniana var. hainanensis is an endangered plant that today is endemic to Hainan Island, in southern China (Cheng et al., 1975; Cheng and Fu, 1978; Fu et al., 1999). The presence, in the upper Miocene of SE Yunnan in SW China, of needles and a woody, elongate, ovoid to cylindrical ovulate cone with a flattened umbo that closely resembles the extant Pinus massoniana var. hainanensis suggests a variation of this species outside its current restricted endemic distribution. Additionally, in the upper Miocene of SE China, shoots with attached needles and seed cones of Pinus premassoniana have been described from the Shengxian Formation in Jiahu of Zhejiang Province. The seed cones of this species as well as its attached needles closely resemble those of the extant P. massoniana both in morphological and cuticular characters (Ding et al., 2013). Except for some minor differences between them, such as the length of the persistent basal sheath and a distinct transverse keel in the fossil species compared to the extant one, this fossil species is significantly similar to the extant one (Ding et al., 2013). Based on the variations of extant P. massoniana (Fu et al.,

Plate I. Pinus massoniana-like ovulate cone. 1–4. Seed cone and its counterpart, showing three dimensional preserved, conical to cylindrical in shape, bract scale and seed scale complex helically arranged around the axis. Bar = 1 cm. 5–8. Showing apophyses rhombic, slightly swollen, and transversely keeled. Bar = 0.5 cm. 9–12. Showing umbos dorsal and slightly sunken; mucros erect, characterized of perexcentromucronate umbo type. Bar = 2 mm. 13–16. Epidermal structure, cells spindly, polygonal or irregularly shaped, in rows or randomly arranged. 13–15. Bar = 100 μm. 16. Bar = 50 μm.

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Rhombic, swollen Rhombic, Swollen Rhombic, swollen Rounded, flat or swollen Rounded, flat Slightly raised Bulbous, rounded

Spiny, sunken Sunken–protruded Sunken–protruded Flattened to raised Flattened to raised Centrally depressed Raised

Avallate Vallate Avallate or vallate Subvallate Vallate Avallate Vallate

Transversely Transversely Cross keeled Transversely Transversely Transversely Not keeled

Erect Curve Erect or curve Erect Erect No mucro Erect or curve

E Zhejiang SE Asia SW China Mediterranean Basin M and W Asia NE America Mediterranean Basin

Fu et al. (1999) Fu et al. (1999); Ding et al. (2013) Fu et al. (1999) Fu et al. (1999) Fu et al. (1999) Silba (1986) Silba (1986) Silba (1986) Silba (1986) Hainan C and SE China Erect Erect Transversely Transversely Avallate Avallate Flattened or obtuse, sunken Flattened or obtuse, sunken Rhombic, swollen Rhombic, swollen

2.5–5 2.5–4 (2.8–3.5) 2–3 4.0–5.0 4.0–5.0 4.0–5.0 4.0–5.0 3.0–3.5 5.0–11.0 Ovoid–ellipsoid Ovoid Ovoid to conical Broad conical Broad conical Ovoid to conical Broad ovoid–globose

Ovoid–cylindric Conical–ovoid (conical)

Pinus massoniana var. hainanensis P. massoniana var. massoniana (P. premassoniana) P. massoniana var. shaxianensis P. kesiya P. yunnanensis P. brutia P. halepensis P. resinosa P. pinea

4–7 4–7 (5.2–7.4) 5–9 5.0–7.0 3.0–7.0 6.0–10.0 6.0–12.0 4.0–6.4 8.0–12.0

Apophyses Width (cm) Length (cm) Cone shape Species

Table 1 Comparisons of the fossil seed cone to the extant perexcentromucronate type cones in Pinus.

Umbos

Vallate

Keel type

Mucros

References

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1999), differences in these features: the length of the persistent basal sheath, and a distinct transverse keel, would probably fall within the range of P. massoniana var. massoniana and these remains assignable to this variation. Therefore, the present discovery of Pinus massoniana var. hainanensis in SW China and P. massoniana var. massoniana from SE mainland China suggests that the differentiation within P. massoniana began in the late Miocene or earlier. 4.5. Neogene climate cooling led to the southward expansion of Pinus massoniana to Hainan Island Extant Pinus massoniana var. hainanensis is restricted to the Bawangling National Forest Park in Hainan Island (Cheng et al., 1975). Natural populations grow in montane environment under a climate with mean annual temperature 21.5 °C, December temperature (lowest) 18.5 °C, May temperature (highest) 22.8 °C, annual precipitation between 1106 mm and 2417 mm, January precipitation of about 82 mm, July precipitation about 1335 mm (CMA, 2014). Thus, the extant P. massoniana var. hainanensis grows in a humid subtropical to tropical climate. Since the late Miocene, the climate in southeastern Yunnan has changed significantly. The main reasons are related to the global cooling in the Neogene (Tanai, 1967; Wolfe, 1978; Tiffney and Manchester, 2001; Zachos et al., 2001; Mosbrugger et al., 2005), and in particular the intensification of the East Asian monsoon climate with the uplift of Qinghai-Tibet Plateau (QTP) (Quade et al., 1989; Harrison et al., 1992; Molnar et al., 1993; Harrison et al., 1995; Li, 1999; An et al., 2001; Liu and Yin, 2002; Mulch and Chamberlain, 2006; Jacques et al., 2011; Zhang et al., 2012). In southeastern Yunnan today, a subtropical monsoon climate (seasonally humid and dry, as demonstrated by Jacques et al. (2011) and Xing et al. (2012)) prevails, with mean annual temperatures from 17.0 °C and 19.3 °C, January temperature (lowest) from 6.3 °C to 14.7 °C, July temperature (highest) from 18.9 °C to 26.1 °C, and annual precipitation varying between 759 and 1172.3 mm, mean January precipitation is 19.5 mm, mean July precipitation is 269.6 mm (YMB, 1983). Such a climate would no longer be suitable for Pinus massoniana var. hainanensis, and the present distribution of this conifer on Hainan Island probably suggests an adaptive expansion and southward migration after the late Miocene (Tian et al., 2010). Studies show that southward expansions are common for montane temperate plants in subtropical and tropical latitudes with the global cooling of climate in the Neogene, or perhaps during the Quaternary glacial stages (Ferguson, 1993; Wang and Ge, 2006; Petit et al., 2008; Tian et al., 2008; Tian et al., 2010). Hainan Island, located in SE Wenshan, an area, in the southernmost part of the Chinese mainland, had a climate with higher temperature in the late Miocene compared to the present day (Micheels et al., 2011). With the global cooling in the Late Neogene, the climate in this area changed accordingly, the cooler climate provided suitable conditions for the southward expansion of Pinus massoniana var. hainanensis. Thus, these southern populations of P. massoniana var. hainanensis, nevertheless, may have behaved as minor, secondary refugia in the Quaternary Period, and are of comparatively recent origin. 4.6. Disappearance of Pinus massoniana from SW China is related to monsoon climate Pinus massoniana is currently distributed mostly in southern, central and eastern China, but does not occur in southwest China (Fu et al., 1999; Zhang et al., 2011; Fig. 3). The formation of this distribution pattern and the disappearance of this species from SW China are probably related to the Neogene climate changes in eastern Asia. The climatic context of Pinus massoniana from the upper Miocene of Wenshan in SE Yunnan, SW China indicates a warm and humid climate.

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Plate II. Comparisons of fossil with extant species, showing similar morphological features between them in apophyses, umbos, mucros and epidermal structures. 1. Apophyses (a, b and c) from fossil cone for comparisons. Bar = 1 cm. 2. Enlargement of “a” in 1, apophyse broadly rhombic in shape, bear evident transverse keels (arrow a) , umbos with a short mucro (arrow b), characteristic of perexcentromucronate umbo type. Bar = 0.5 cm. 3. Enlargement of “b” in 1, apophyse polygonal in shape, with radial ridge (arrow a), umbos slightly sunken, with a short mucro (arrow b). Bar = 0.5 cm. 4. Enlargement of “c” in 1, apophyse polygonal, umbos slightly sunken (arrow a), with radial ridge (arrow b). Bar = 0.5 cm. 5. Enlargement of “a” in 8, apophyse polygonal or rhombic in shape, transverse keeled, umbos with a short mucro (arrow), characteristic of perexcentromucronate umbo type. Bar = 0.5 cm. 6. Enlargement of “b” in 8, apophyse polygonal, transversely keeled, with radial ridge, umbos with a short mucro (arrow). Bar = 0.5 cm. 7. Enlargement of “c” in 8, apophyse polygonal, umbos slightly sunken (arrow), with radial ridge. Bar = 0.5 cm. 8. Extant Pinus massoniana, apophyses (a, b and c) for comparisons. Bar = 1 cm. 9–11. Epidermal structure of modern cone, cells spindle-shaped, polygonal or irregularly shaped, in rows or randomly arranged. 9. Bar = 100 μm. 10–11. Bar = 40 μm.

This was supported not only by the analogy of the distribution of the extant species, but also by the paleoclimatic reconstruction of Xiaolongtan flora (Xia et al., 2009) near Wenshan area.

The global cooling and the uplift of Qinghai-Tibet Plateau are the most important climatic factors contributing to the Neogene climate, and had profound impacts on the evolution of vegetation in eastern

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Plate III. Comparisons of associated needles with extant species, showing similarity in morphological characters and epidermal structures. 1–2. Fossil two-needled in a fascicle showing a bundle of fossil leaves, base with persistent sheath (arrow in 1), and slightly twisted (arrow in 2). Bar = 1 cm. 3–6. Showing needles semi-cylindrical or semilunar, with many longitudinal veins and serrated edge. Bar = 5 mm. 7–8. Epidermal structures of fossil needles, cells rectangular, arranged in parallel rows, with end walls vertical or oblique and anticlinal walls sinuous (arrow), stomatal row mostly with one interstomatal cell. Bar = 100 μm. 9–14. Epidermal structures of modern Pinus massoniana, cell and stomatal similar to that of fossil materials. 9, 11, and 14. Bar = 100 μm. 10, 12, and 13. Bar = 50 μm.

Asia (Zachos et al., 2001; Mosbrugger et al., 2005). The uplift of Qinghai-Tibet Plateau and intensification of the Asian monsoon has led to the great changes of climate in southwestern China (Jacques

et al., 2011; Xing et al., 2012; Zhang et al., 2012), especially lower mean annual temperatures and lack of precipitation in winter and spring (YMB, 1983).

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Table 2 Comparisons of the present fossil seed cone with the related fossil seed cones in Pinus. Species

Cone shape

Symmetric

Cone size (cm)

Vallate

Umbos

Excentro-

Age

References

Pinus massoniana var. hainanensis P. premassoniana P. prekesiya P. baileyi

Ovoid–cylindric

Yes

4.0–7.0 × 2.5–5.0

Avallate

Sunken

Perexcentro-

Late Miocene

This text

Conical Ovoid–conical Conical to oblong

Yes Yes Yes

5.2–7.4 × 2.8–3.5 6.0–7.7 × 3.0–3.5 5.0–6.0 × 2.5

Avallate Vallate Avallate

Sunken Sunken Protruding

PerexcentroPerexcentroPerexcentro-

P. P. P. P. P.

salinarum hampeana nodosa speciosa ornata

Ovoid Long ovoid Ovoid Elliptic Ovoid

No Yes No Yes Yes

5.2–8.5 × 4.7 Length 4–8 6.5 × 4.0 6.4 × 3.4 Length b 9

– Subvallate Subvallate – Vallate

Protruding Flat, sunken Sunken Sunken Flat

PerexcentroDenticulatomucroDenticulatomucroDenticulatomucroDenticulatomucro-

Late Miocene Late Miocene Mid Eocene/early Oligocene Mid Miocene Mid Miocene Early Miocene Miocene Oligocene, Miocene

P. P. P. P. P. P. P. P.

dixoni urani brevis spinosa engelhardtii driftwoodensis princetonensis arnoldii

Ovoid Ovoid–cylindric Ovoid Ovoid–cylindric – Cylindric Cylindric Conical

No No No No No Yes – –

Length N 13 Length N 9 Length N 6 Length N 14 12.0 × 7.5 3.0–4.0 × 2.7 4.0–4.8 × 1.5–2.0 5.0–7.0 × 1.8–2.8

Vallate – Vallate – – – – –

Sunken Sunken Sunken Protruding Protruding Protruding Protruding Protruding

DenticulatomucroDenticulatomucroErectoexcentroErectoexcentroCentro– – –

Late Miocene Mid–late Miocene Pliocene Late Eocene–Pliocene Miocene mid Eocene Mid Eocene Eocene

Ovoid

No

5.0 × 2.0

–

Sunken

–

Late Miocene

Ding et al. (2013) Xing et al. (2010) Erwin and Schorn (2006) Mai (1986) Mai (1986) Mai (1986) NIGMR (1982) Mai (1986); Teodoridis and Sakala (2008) Mai (1986) Mai (1986) Mai (1986) Mai (1986) Mai (1986) Stockey (1983) Stockey (1984) Miller (1973); Stockey (1984) Mai (1986)

P. parabrevis

The lack of precipitation in winter and spring seasons is adverse to the germination of Pinus massoniana seeds and survival of new seedlings. Cones of P. massoniana mature from October to December (Fu et al., 1999) and shed seeds in the winter season. The seeds of this conifer are ready to germinate in spring, from the beginning of March to the first third of April, but will only do so if seedbeds are moist and the weather is warm enough (Cheng et al., 1975; Cheng and Fu,

1978). The dry winter and spring in present-day Wenshan of southeastern Yunnan would probably prevent the seeds of P. massoniana from germinating. Germination studies (Yu, 1959; Qin and Ding, 2012) show that seeds of Pinus massoniana grow and survive best under temperatures consistent with the local climate. Seeds will germinate well under the same temperature as the parent tree live, and that temperature fluctuations

Fig. 3. Modern distribution of Pinus massoniana in the southern, central and eastern parts of China. “Seed zone” from seed zones of Chinese forest trees-seed zones of Pinus massoniana (GB/ T 8822.6-1988); “Realized occurrence record” is the extant occurrence of Pinus massoniana; “Administrative province region” is the boundary of province in China. Revised from Zhang et al. (2011).

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at the initiation of germination will affect seed germination. For example, seeds from the trees living in a warm climate (e.g., southern part of its range) show a higher germination rate when planted in the warm climate than in cold, while, seeds from the trees living in a cold climate (e.g., northern part of its range) show a lower germination rate when grown in a warm climate (Yu, 1959; Qin and Ding, 2012). P. massoniana var. hainanensis from the upper Miocene of southeastern Yunnan presumably lived under similar climate as the extant native species in Hainan, in a climate with mean March temperature between 19.8 °C to 22.6 °C (CMA, 2014). The present day climate in the Wenshan area, represented by mean March temperature of 16.8 °C (YMB, 1983), is characterized by lower temperatures as compared to the late Miocene. Thus, lower temperatures would be adverse to the germination of the P. massoniana seeds. 5. Conclusions An ovulate cone and needles resembling Pinus massoniana var. hainanensis, an endangered conifer endemic to Hainan Island of China, were discovered from the upper Miocene in southwest China. Based on fossil evidence, differentiation within P. massoniana began in the late Miocene or earlier. The extant representation and distribution of this variant (Hainan Island) are derived from northern populations (southern, central and eastern parts of China) – which make up most of the current range of P. massoniana – by southward expansion during Neogene or Quaternary climate changes. Disappearance of P. massoniana from southwestern China is likely related to the amplification of monsoon climate after the late Miocene. Acknowledgments This work was supported by the National Natural Science Foundation of China (41372035 and 41030212) and the Chinese Academy of Sciences 135 program (XTBG-F01). The authors thank Dr. N. Nosova, from Komarov Botanical Institute of the Russian Academy of Sciences, and Dr. L. Wang from XTBG, for providing some references, and the Lab Center of XTBG for preparing the scanning electron microscope photos of the cuticles. This work is a contribution to NECLIME (Neogene Climate Evolution in Eurasia). References Alvin, K.L., 1960. Further conifers of the Pinaceae from the Wealden Formation of Belgium. Mém. Inst. R. Sci. Nat. Bel. 146, 1–39. 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. http://dx.doi.org/10.1038/35075035. Axelrod, D.I., 1986. Cenozoic history of some western American pines. Ann. Mo. Bot. Gard. 73, 565–641. http://dx.doi.org/10.2307/2399194. BGMRYP (Bureau of Geology and Mineral Resources of Yunnan Province), 1990. Regional Geology of Yunnan Province. Geological Publishing House, Beijing (in Chinese, with English introduction). BGMRYP (Bureau of Geology and Mineral Resources of Yunnan Province), 1996. Stratigraphy (Lithostratigraphy) of Yunnan Province. China University of Geosciences Press, Wuhan (in Chinese, with English introduction). 蔡麟孙, 李兴林, 2002. 云南省地质图(1:2,500,000), 含说明. 云南省地质矿产局, 昆明. (Cai, L.S., Li, X.L., 2002. Geological Map of Yunnan Province (1:2,500,000 scale), with Explanatory. Bureau of Geology and Mineral Resources of Yunnan Province, Kunming.) (in Chinese). 郑万钧, 傅立国, 1978. 中国植物志, 第七卷, 裸子植物门. 科学出版社, 北京. (Cheng, W., Fu, L., 1978. Flora Reipublicae Popularis Sinicae. Tomus 7, Gymnospermae. Science Press, Beijing.) (in Chinese). 郑万钧, 傅立国, 诚静容, 1975. 中国裸子植物. 植物分类学报 13, 56–85. (Cheng, W.J., Fu, L.G., Cheng, J.R., 1975. Gymnospermae Sinicae. Acta Phytotaxon. Sin. 13, 56–85.) (in Chinese). CMA, . China meteorological data sharing service system. Last updated 22 May 2014, http://cdc.cma.gov.cn/ (accessed 23 May, 2014). Ding, S.T., Wu, J.Y., Chen, J.L., Yang, Y., Yan, D.F., Sun, B.N., 2013. Needles and seed cones of Pinus premassoniana sp. nov., and associated pollen cone from the upper Miocene in East China. Rev. Palaeobot. Palynol. 197, 78–89. http://dx.doi.org/10.1016/j.revpalbo. 2013.05.004. Dong, W., 1987. Further investigations upon the age and characteristics of the Xiaolongtan Fauna, Kaiyuan Co., Yunnan Province. Vertebr. Palasiat 25, 116–123.

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