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

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Review of Palaeobotany and Palynology

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

Jian-Wei Zhang a,AshalataD'Rozariob,JonathanM.Adamsc, Xiao-Qing Liang a, Frédéric M.B. Jacques a, Tao Su a, Zhe-Kun Zhou a,⁎ a Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden (XTBG), Chinese Academy of Sciences, Mengla, Yunnan 666303, China b Department of Botany, Narasinha Dutt College, 129, Bellilious Road, Howrah 711101, India c The college of Natural Sciences, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 151-742, Republic of Korea article info abstract

Article history: A fossil cone and associated needles from the upper Miocene Wenshan flora, Yunnan Province, SW China are Received 11 August 2014 recognized as Pinus massoniana Lambert, which is an endemic distributed mostly in southern, central and Received in revised form 12 November 2014 eastern parts of China. The comparisons of these fossils with the three extant variants in this species Accepted 15 November 2014 (P. massoniana var. shaxianensis Zhou, P. massoniana var. massoniana Lambert and P. massoniana var. hainanensis Available online 15 December 2014 Cheng et Fu) indicate that the fossils closely resemble P. massoniana var. hainanensis, which is a tropical montane thermophilic and hygrophilous restricted to Island in southern China. The present finding and a pre- Keywords: fi China vious report of Pinus premassoniana from the same age in southeastern China, which bears close af nities with Comparative morphology modern P. massoniana var. massoniana, suggest that the variation in this species arose earlier than was previously Fossil thought. Thus, the presence of P. massoniana var. hainanensis in the late Miocene Wenshan flora, Yunnan Province Late Miocene in southwestern China suggests (1) the subdifferentiation of P. massoniana began in the late Miocene or earlier; Phytogeography (2) the extant distribution of P. massoniana var. hainanensis might be derived from northern populations – the Pinus massoniana 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 relat- ed to the intensification of monsoon climate after the late Miocene. © 2014 Elsevier B.V. All rights reserved.

1. Introduction extant genus Pinus was classified into two subgenera, four sections and eleven subsections (Krupkin et al., 1996; Price et al., 1998; Gernandt The genus Pinus contains ca. 110 species of evergreen with et al., 2005). Subgenus Pinus L. is distinguishable by two fibrovascular needlelike . It is widespread in north temperate and north tropical bundles per needle with persistent fascicle sheaths, except for Pinus (mountainous) regions, with species found in North America, Central leiophylla Schiede ex Schlechtendal et Chamisso and Pinus lumholtzii America, , North Africa, West Indies, Eurasia (including one spe- Rob et Fernald, subgenus Strobus (D. Don) Lemon by a single fibrovascu- cies crossing the equator in Sumatra) and the Pacific Islands in Sumatra lar bundle per needle with deciduous fascicle sheaths, except for Pinus (Kral, 1993). In China, there are 39 species of Pinus (Fu et al., 1999). nelsonii Shaw, and the dorsal umbo position delineates subsection Strobus Pinus massoniana Lambert, a species with long slender needles of Loudon (terminal umbo) from all other . In this classification about 12–20 cm, is endemic in China and distributed mostly in south- (Gernandt et al., 2005), Pinus massoniana and 16 species found mainly ern, central and eastern parts of the nation, from a few hundred to from Eurasia and the Mediterranean region, were assigned to subsection 2000 m in moist river valleys to the dry mountain plateaus (Fu et al., Pinus sensu Gernandt, Geada López, Ortiz García et Liston in section Pinus 1999). Some populations of P. massoniana are also found on sensu Gernandt, Geada López, Ortiz García et Liston of subgenus Pinus. (eastern China) and Hainan Island (southern China), but the paleogeo- Klaus (1980, 1989) has given another classification of Pinus based graphical evidence for this distribution pattern is lacking. on the location and morphological features of the mucro on the cone Based on the morphological features, such as vascular bundles in a scales. His approach matches the basic frame of existing classifica- needle, persistent fascicle sheaths, needle number per fascicle, needle tion systems (Klaus, 1980, 1989). He subdivided the subgenus resin ducts, cone scale, umbo prickle, seed wing and umbo position, the Pinus into two different groups: centromucronate with the mucro lo- cated in the center of the umbo and excentromucronate with the ⁎ Corresponding author. Tel./fax: +86 691 8715070. mucro situated above the transverse keel. The excentromucronate E-mail address: [email protected] (Z.-K. Zhou). species are further divided into four groups: denticulatomucronate

http://dx.doi.org/10.1016/j.revpalbo.2014.11.006 0034-6667/© 2014 Elsevier B.V. All rights reserved. 58 J.-W. Zhang et al. / Review of Palaeobotany and Palynology 215 (2015) 57–67 with a long mucro positioned on the upper edge of the umbo field, Based on the geological survey (Zhang, 1976; Cai and Li, 2002), the perexcentromucronate with one short mucro positioned near the upper Neozoic sediments of the study area (Wenshan State located in SE Yun- edge of the umbo, erectoexcentromucronate with a long mucro arising nan Subregion of South China Region) is composed of Paleogene just a little above the transverse keel, and duplomucronate characterized Yanshan Group, Neogene Xiaolongtan Formation and Quaternary strata. by an excentric mucro and an additional central protuberance on the The molasses formation of Yanshan Group is composed of coarse clastic horizontal keel, a combination of a centro- and an excentromucronate rocks, heavy layer and lack fossils. Xiaolongtan Formation is the only umbo (Klaus, 1980, 1989). Centromucronate umbos are often present fluvio-lacustrine sediment in the study area, composed of laminated in the American pines and excentromucronate umbos occur in all the sedimentary sequences, and contains abundant animal and plant fossils. Eurasian pines (Klaus, 1989). Pinus massoniana and six other species Exposure of the Xiaolongtan Formation around Wenshan State is from eastern Asia, the Mediterranean and eastern North America, about 200–300 m thick, and generally divided into three members: which bear a short mucro situated near the upper edge of the umbo, the Upper Member (about 41.3 m thick, is missing in the present fossil are perexcentromucronate (Xing et al., 2010; Ding et al., 2013). locality, and distributed mostly in in south of Wenshan The origin of genus Pinus is thought to be Early Cretaceous (Millar, State) is composed of thin layers (b0.1 m) of gray to white-gray marlite; 1998; Ryberg et al., 2012), whereas the estimated divergence times of the Middle Member (65.6 m thick here) consists of thin to medium the two subgenera range from the Late Cretaceous (Millar, 1998)to layers (b0.5 m) of gray-green to gray-yellow mudstone or fine sand- the middle Eocene (Miller, 1976). The earliest known Pinus fossils are stone, with interlayers of coal; and the Lower Member (27.1 m thick permineralized cones from the Wealden of Belgium (Alvin, 1960) and here) comprises medium layers (0.1–0.5 m) of gray to dark-gray con- Yorkshire (Ryberg et al., 2012), which show affinities to the subgenus glomerate or sandstone. The present fossils were collected from the Pinus (Miller, 1976; Willyard et al., 2007). The earliest fossils of the sub- Middle to Lower Members (92.7 m) of the formation which lie primarily genus Strobus are Late Cretaceous permineralized wood (Meijer, 2000), around (Zhang, 1976; Zheng et al., 1999; Fig. 2). The while the earliest leaves (Miller, 1973) or ovulate cones (Axelrod, 1986) Xiaolongtan Formation is late Miocene in age based on lithology, biolog- of the subgenus are reported from the middle Eocene. Hitherto, over 50 ic assemblage and regional comparisons (Dong, 1987; BGMRYP, 1996). fossil species of Pinus have been described in the world (Ding et al., It lies unconformably above the upper Oligocene Yanshan Group and is 2013). overlain unconformably by Quaternary strata (Zhang, 1976). In China, six fossil species have been described from Cenozoic sedi- The sedimentary sequences in Dashidong Village in Wenshan City ments. Among them, five (Pinus yunnanensis Franch, Pinus speciosa Li, yield abundant plant fossils, such as Quercus, Salix , Dryophyllum, Pinus prototabulaeformis Tao et Wang, Pinus prekesiya Xing, Liu et Zhou Ulmus, Zelkova, Ampelopsis, Populifolia, Glyptostrobus (Zhang, 1976), and Pinus premassoniana Ding et Sun) were established at least on the Ailanthus confucii Unger (Su et al, 2013), Bauhinia wenshanensis Meng basis of seed cones (Tao and Kong, 1973; NIGMR, 1982; Tao and Wang, et Zhou (Meng et al., 2014), Sequoia maguanensis Zhang et Zhou and 1983; Xing et al., 2010; Ding et al., 2013), and Pinus palaeopentaphylla Pinus,andfossilfish and insects (mosquitos, ants, etc.). Tanai et Onoe was based on needles (Guo and Zhang, 2002). The global climate underwent severe changes after the middle Mio- 2.2. Fossil specimens cene warm interval (Tanai, 1967; Wolfe, 1978; Graham, 1999), e.g., global cooling (Zachos et al., 2001; Mosbrugger et al., 2005), espe- The fossils described here consist of a three-dimensionally- cially in eastern Asia owing to the uplift of the Tibetan Plateau preserved seed cone (DMS 0135) and associated compressions of (Harrison et al., 1992; Molnar et al., 1993; Harrison et al., 1995; Mulch needles (DMS 0136-0137). Fossil specimens are deposited in the fossil and Chamberlain, 2006). The uplift of the Tibetan Plateau had not only repository of the Paleoecology Research Group, Xishuangbanna Tropical caused changes in the regional landforms, climate and biodiversity of Botanical Garden, Chinese Academy of Science, Yunnan of China. 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., 2.3. Morphology and cuticle study methods 2011; Zhang et al., 2012). These climate changes have led to the contrac- tion of thermophilic conifers in eastern Asia (Wang and Ge, 2006). Photographs were obtained using a Nikon D700 digital camera Shoots with attached needles and seed cones of Pinus premassoniana (Nikon, Kanagawa, Japan) under tungsten light. Some specimens were have been reported from the upper Miocene of eastern Zhejiang Prov- immersed in kerosene to enhance details. Detailed structures of these ince, southeastern China (Ding et al., 2013). In this paper, new fossils specimens were observed and photographed under a Leica S8AP0 ste- of Pinus massoniana, which were found from the upper Miocene of reoscope microscope (Leica, Wetzlar, Germany). The cone and needles southeastern Yunnan, southwestern China, are described. These re- were treated with Schulze's solution (HNO3 and KClO3, 3:1) and KOH, mains include a three dimensional seed cone and associated needles and washed with water to obtain clear cuticles (Kerp, 1990). Epidermal which have well preserved cuticles. This finding is significant in the dis- characters were observed using a Leica DM750 stereoscope microscope, cussion of the early differentiation among this species. We also discuss and photographed under Leica DFC295 and Zeiss EVOLS10 scanning its paleophytogeographical implications and the possible causes of the electron microscope (Carl Zeiss, Jena, Germany). disappearance of this species from southeastern Yunnan, southwestern China. 3. Results 2. Material and methods 3.1. Systematics 2.1. Geological settings and age

Fossils for the present study were collected from outcrops located in Family: PINACEAE Lindley. Dashidong Village (23°15′N, 104°15′E, 1482 m a.s.l.), Wenshan State, SE Genus: Pinus L. Yunnan Province, SW China (Fig. 1). The outcrops are characterized by Subgenus: Pinus L. light-gray or light-yellow pelitic laminated siltstone and mudstone. Section: Pinus sensu Gernandt, Geada López, Ortiz García et The laminated sedimentary sequences in Dashidong Village were previ- Liston. ously assigned to the Huazhige Formation (Zhang, 1976; BGMRYP, Subsection: Pinus sensu Gernandt, Geada López, Ortiz García et 1990). Recently, they have been assigned to the Xiaolongtan Formation Liston. (BGMRYP, 1996; Zheng et al., 1999). Species: Pinus massoniana Lambert. (Plate I) J.-W. Zhang et al. / Review of Palaeobotany and Palynology 215 (2015) 57–67 59

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

Locality: Dashidong Village, Wenshan City, SE Yunnan Province, observed in a stomatal row, but mostly one. Stomatal complexes are SW China. monocyclic and elliptic, 40–50 μm long and 28– 36 μm wide, oriented Age and stratigraphy: Late Miocene, Xiaolongtan Formation. 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 μmwide(Plate III,7–8). 3.2. Description 4. Discussion The seed cone (Plate I,1–4) is woody, elongated, cylindrical to con- ical in shape, about 5.0 cm long and 1.7 cm in diameter, with length to 4.1. Taxonomic treatment 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 The Dashidong ovulate cone conforms to the genus Pinus in bearing arranged around the axis and about 19 are visible on the viewed surface, helically arranged cone–scale complexes and ovuliferous scales that are thus, the total number is about 45 ± 10. expanded at the apex with apophyses and umbos (Miller, 1976). Based Apophyses (Plate I,5–8) are slightly swollen or flat. In the lower part on the above description: the Dashidong cone bears umbos located on of the cone, apophyses are polygonal in shape, about 0.6 ± 0.1 cm in di- the dorsal surface of the apophyses, with short mucros above the trans- ameter and bear no evident transverse or longitudinal keels except for verse keel and near the upper edge of the umbo, characteristic of the some radial ridges; while in the middle and upper part of the cone, perexcentromucronate umbo type (Klaus, 1980, 1989). In the extant apophyses are broadly rhombic, 0.8 ± 0.1 cm wide, 0.7 ± 0.1 cm high genus Pinus, the perexcentromucronate umbo is only present in section and bear evident transverse keels as well as radial ridges. Apophyses Pinus in subgenus Pinus and only seven extant species (Pinus brutia are avallate and umbos are dorsal, elliptic or spindle shaped, Tenore, Pinus halepensis Miller, Pinus pinea L., Pinus resinosa Aiton, 2.5–4mmwide,2–3 mm high and slightly sunken (Plate I,9–12). A Pinus kesiya Gordon, Pinus yunnanensis Franchet and Pinus massoniana short erect mucro lies above the transverse keel near the upper edge Lambert) (Xing et al., 2010; Ding et al., 2013). It is therefore suggested of the umbo (perexcentromucronate) (Plate I,9–12). that the Dashidong cone can be assigned to section Pinus, in subgenus Cone epidermal structure (Plate I,13–16) shows cell spindle, polyg- Pinus. onal or irregular shaped, 5–20 μm long (mostly 17 ± 3 μm), 3–10 μm wide (mostly 15 ± 3 μm), in rows or randomly arranged. 4.2. Comparison with related extant species in section Pinus Associated leaves (Plate III,1–4) are needlelike, in bundles of two, slightly twisted, about 12 cm long, 1 mm in diameter, with pointed The Dashidong cone bears the perexcentromucronate umbos that tip, serrated margin and many longitudinal veins on the surface. exist in seven extant species in section Pinus (Table 1). Among these, Needles are semi-cylindrical in shape (Plate III,3–4) with its abaxial four species (Pinus resinosa, Pinus kesiya, Pinus yunnanensis and Pinus side arched, ventral depressed to a deep groove and base covered by massoniana) are in the subsection Pinus, and three species (Pinus brutia, persistent sheath. Pinus halepensis and Pinus pinea) in the subsection Pinaster Loudon The epidermal structure of the needles (Plate III,7–8) shows rectan- (Gernandt et al., 2005). The Dashidong cone is distinguishable from gular cells, 50–200 μm in length, 10–20 μm in width, but slightly the three Mediterranean pines in subsection Pinaster in that the Medi- broader within the stomatal lines than between the stomatal lines, terranean pines possess rounded apophyses and raised umbos (Silba, and arranged in parallel rows. Cells have undulated or sinuous anticlinal 1986), while the present fossil has rhombic apophyses and sunken walls and vertical or oblique ends. One to two interstomatal cells were umbos. The Dashidong cone differs from the NE American P. resinosa 60 J.-W. Zhang et al. / Review of Palaeobotany and Palynology 215 (2015) 57–67

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 sunk- en umbos, which differs from the protruding umbos in the species of P. salinarum (Mai, 1986)andP. 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 lo- cated in the center of the umbo (Mai, 1986). Pinus driftwoodensis Stockey (Stockey, 1983)andPinus princetonensis Fig. 2. Stratigraphic column of the Xiaolongtan Fm. in Dashidong Village, showing the Stockey (Stockey, 1984) are cylindric seed cones, but their mucro posi- Pinus fossils within the bed. Revised from Zhang (1976). tions are not demonstrated in the descriptions, and their umbos are pro- truding rather than sunken. Cones of Pinus arnoldii Miller are conical with protruding umbos in the presence of a mucro in the umbo, which is absent in the latter (Miller, 1973; Stockey, 1984; Klymiuk et al., 2011), which is different (Farjon, 2005; Erwin and Schorn, 2006). The apophyses in the Dashidong from the new cone. Pinus parabrevis Kilpper also has sunken umbos, cone are avallate and the umbos are not encircled by a ring-like area on but its seed cones are asymmetrical and ovoid in shape (Mai, 1986). the dorsal surface of the apophyses; while in P. kesiya,itsapophysespos- sess clear vallums that encircle the umbos (Erwin and Schorn, 2006). The 4.4. Differentiation of Pinus massoniana in the late Miocene or earlier apophyses of the current cone are transversely keeled, and the umbos are slightly sunken; whereas those of P. yunnanensis are cross keeled Three variations among extant Pinus massoniana have been recog- and somewhat protruding (Fu et al., 1999). nized based on the differences in morphological features of seed cones Based on the morphological features of apophyses and umbos (Plate II, (Fu et al., 1999). P. massoniana var. shaxianensis Zhou is distinguishable 1–8), such as apophyses rhombic, avallate and transversely keeled; from the other two variations by its typical spiny umbos, while the umbos sunken, presence of erect mucros, as well as epidermal structures other two usually have flattened umbos. P. massoniana var. shaxianensis of the cone (Plate I,13–16; Plate II,9–11), such as cells spindle, polygonal is found in Shaxian County, in central Province of southeastern or irregular shaped, in rows or randomly arranged, the Dashidong cone China. P. massoniana var. massoniana Lambert can be distinguished closely resembles extant Pinus massoniana (Fu et al., 1999; Table 1). from P. massoniana var. hainanensis ChengetFubyitsovoidorconical- The associated needles further support the identity of the Dashidong ovoid seed cones, the latter has elongated, ovoid-cylindric seed cones cone. The morphological features (Plate III,1–4): two needles in a bun- (Cheng et al., 1975; Cheng and Fu, 1978). P. massoniana var. massoniana dle, slightly twisted, about 12 cm long and 1 mm in diameter, semi- is the most common variation in China, and has the largest distribution in cylindrical in shape with abaxial surface curved and ventral depressed eastern, central and southern China. P. massoniana var. hainanensis is an to a groove, margin serrated, base with persistent sheath, as well as endangered plant that today is endemic to Hainan Island, in southern the epidermal characters (Plate III, 7, 8): cells rectangular, arranged in China (Cheng et al., 1975; Cheng and Fu, 1978; Fu et al., 1999). parallel rows, its anticlinal walls undulated or sinuous and end ones ver- The presence, in the upper Miocene of SE Yunnan in SW China, of tical or oblique; mostly only one interstomatal cell occurring in a stoma- needles and a woody, elongate, ovoid to cylindrical ovulate cone with tal row; stomata oriented regularly along long axis of needles; stomatal a flattened umbo that closely resembles the extant Pinus massoniana complexes monocyclic and elliptic, are all consistent with those of ex- var. hainanensis suggests a variation of this species outside its current tant Pinus massoniana (Plate III,5,6,9–14; Fu et al., 1999). restricted endemic distribution. Additionally, in the upper Miocene of SE China, shoots with attached 4.3. Comparison with fossil species of Pinus needles and seed cones of Pinus premassoniana have been described from the Shengxian Formation in Jiahu of Zhejiang Province. The seed In genus Pinus, there are about 17 fossil species from the Cenozoic of cones of this species as well as its attached needles closely resemble Eurasia and America that share similar ovulate cone morphological those of the extant P. massoniana both in morphological and cuticular characters with the Dashidong fossils (Table 2). Firstly, four species, characters (Ding et al., 2013). Except for some minor differences be- namely, Pinus prekesiya Xing et Zhou, Pinus premassoniana Ding et tween them, such as the length of the persistent basal sheath and a dis- Sun, Pinus baileyi Axelrod emend. Erwin et Schorn, and Pinus salinarum tinct transverse keel in the fossil species compared to the extant one, (Partsch) Zablocki, all possess perexcentromucronate umbos. The this fossil species is significantly similar to the extant one (Ding et al., Dashidong cone differs from P. prekesiya in lacking vallate apophyses. 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. J.-W. Zhang et al. / Review of Palaeobotany and Palynology 215 (2015) 57–67 61 62 J.-W. Zhang et al. / Review of Palaeobotany and Palynology 215 (2015) 57–67

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. Silba (1986) Fu et al. (1999) Fu et al. (1999) Fu et al. (1999) Ding et al. (2013) Fu et al. (1999) Fu et al. (1999) Silba (1986) Silba (1986) Silba (1986) 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 (low- est) 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 ex- tant P. massoniana var. hainanensis grows in a humid subtropical to Not keeled Erect or curve Mediterranean Basin 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 Vallate 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 protruded Vallate Transversely Curve SE Asia protruded Avallate or vallate Cross keeled Erect or curve SW China 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 tem- perature (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 pre- cipitation is 269.6 mm (YMB, 1983). Such a climate would no longer be suitable for Pinus massoniana var. hainanensis, and the present distribu- at or swollen Flattened to raised Subvallate Transversely Erect Mediterranean Basin at Flattened to raised Vallate Transversely Erect M and W Asia fl fl tion of this conifer on Hainan Island probably suggests an adaptive ex- pansion and southward migration after the late Miocene (Tian et al.,

. 2010). Apophyses Umbos Vallate Keel type Mucros Location References Rhombic, swollen Flattened or obtuse, sunken Avallate Transversely Erect C and SE China Studies show that southward expansions are common for montane Pinus temperate in subtropical and tropical latitudes with the global 3.5) 11.0 Bulbous, rounded Raised 5.0 Rhombic, Swollen Sunken 5.0 Rhombic, swollen Sunken 4 5 Rhombic, swollen Flattened or obtuse, sunken Avallate Transversely Erect Hainan 5.0 Rounded, 5.0 Rounded, 3.5 Slightly raised Centrally depressed Avallate Transversely No mucro NE America – cooling of climate in the Neogene, or perhaps during the Quaternary – – – – – – – – 3 Rhombic, swollen Spiny, sunken Avallate Transversely Erect E Zhejiang – 5.0 Width (cm) (2.8 2.5 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 7.4) 7.0 4.0 7.0 4.0 10.0 4.0 12.0 4.0 6.4 3.0 12.0 Wenshan, an area, in the southernmost part of the Chinese mainland, – – – – – – – 92 7 7 2.5 – – – had a climate with higher temperature in the late Miocene compared (cm) (5.2 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 expan-

globose 8.0 sion of Pinus massoniana var. hainanensis. –

ovoid (conical) 4 Thus, these southern populations of P. massoniana var. hainanensis, – ellipsoid 5 cylindric 4 – – nevertheless, may have behaved as minor, secondary refugia in the Quaternary Period, and are of comparatively recent origin. Ovoid 5.0 Ovoid Ovoid to conical 3.0 Ovoid Conical Broad conical 6.0 Broad conical 6.0 Ovoid to conical 4.0 Broad ovoid

4.6. Disappearance of Pinus massoniana from SW China is related to mon- soon climate hainanensis

) Pinus massoniana is currently distributed mostly in southern, central shaxianensis massoniana var. and eastern China, but does not occur in southwest China (Fu et al., var. var. 1999; Zhang et al., 2011; Fig. 3). The formation of this distribution pat- tern and the disappearance of this species from SW China are probably related to the Neogene climate changes in eastern Asia. P. premassoniana ( The climatic context of Pinus massoniana from the upper Miocene of P. kesiya Species Cone shape Length P. yunnanensis P. massoniana Pinus massoniana P. brutia P. massoniana P. halepensis P. resinosa P. pinea

Table 1 Comparisons of the fossil seed cone to the extant perexcentromucronate type cones in Wenshan in SE Yunnan, SW China indicates a warm and humid climate. J.-W. Zhang et al. / Review of Palaeobotany and Palynology 215 (2015) 57–67 63

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,transverselykeeled,withradialridge,umboswithashortmucro(arrow).Bar=0.5cm.7.Enlargementof“c” in 8, apophyse polygonal, umbos slightlysunken(arrow),withradial 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 ex- The global cooling and the uplift of Qinghai-Tibet Plateau are the tant species, but also by the paleoclimatic reconstruction of Xiaolongtan most important climatic factors contributing to the Neogene climate, flora (Xia et al., 2009) near Wenshan area. and had profound impacts on the evolution of vegetation in eastern 64 J.-W. Zhang et al. / Review of Palaeobotany and Palynology 215 (2015) 57–67

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 et al., 2011; Xing et al., 2012; Zhang et al., 2012), especially lower Qinghai-Tibet Plateau and intensification of the Asian monsoon has mean annual temperatures and lack of precipitation in winter and led to the great changes of climate in southwestern China (Jacques spring (YMB, 1983). J.-W. Zhang et al. / Review of Palaeobotany and Palynology 215 (2015) 57–67 65

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

Species Cone shape Symmetric Cone size Vallate Umbos Excentro- Age References (cm)

Pinus massoniana var. Ovoid–cylindric Yes 4.0–7.0 × 2.5–5.0 Avallate Sunken Perexcentro- Late Miocene This text hainanensis P. premassoniana Conical Yes 5.2–7.4 × 2.8–3.5 Avallate Sunken Perexcentro- Late Miocene Ding et al. (2013) P. prekesiya Ovoid–conical Yes 6.0–7.7 × 3.0–3.5 Vallate Sunken Perexcentro- Late Miocene Xing et al. (2010) P. baileyi Conical to oblong Yes 5.0–6.0 × 2.5 Avallate Protruding Perexcentro- Mid Eocene/early Erwin and Oligocene Schorn (2006) P. salinarum Ovoid No 5.2–8.5 × 4.7 – Protruding Perexcentro- Mid Miocene Mai (1986) P. hampeana Long ovoid Yes Length 4–8 Subvallate Flat, sunken Denticulatomucro- Mid Miocene Mai (1986) P. nodosa Ovoid No 6.5 × 4.0 Subvallate Sunken Denticulatomucro- Early Miocene Mai (1986) P. speciosa Elliptic Yes 6.4 × 3.4 – Sunken Denticulatomucro- Miocene NIGMR (1982) P. ornata Ovoid Yes Length b 9 Vallate Flat Denticulatomucro- Oligocene, Miocene Mai (1986); Teodoridis and Sakala (2008) P. dixoni Ovoid No Length N 13 Vallate Sunken Denticulatomucro- Late Miocene Mai (1986) P. urani Ovoid–cylindric No Length N 9 – Sunken Denticulatomucro- Mid–late Miocene Mai (1986) P. brevis Ovoid No Length N 6 Vallate Sunken Erectoexcentro- Pliocene Mai (1986) P. spinosa Ovoid–cylindric No Length N 14 – Protruding Erectoexcentro- Late Eocene–Pliocene Mai (1986) P. engelhardtii – No 12.0 × 7.5 – Protruding Centro- Miocene Mai (1986) P. driftwoodensis Cylindric Yes 3.0–4.0 × 2.7 – Protruding – mid Eocene Stockey (1983) P. princetonensis Cylindric – 4.0–4.8 × 1.5–2.0 – Protruding – Mid Eocene Stockey (1984) P. arnoldii Conical – 5.0–7.0 × 1.8–2.8 – Protruding – Eocene Miller (1973); Stockey (1984) P. parabrevis Ovoid No 5.0 × 2.0 – Sunken – Late Miocene Mai (1986)

The lack of precipitation in winter and spring seasons is adverse to 1978). The dry winter and spring in present-day Wenshan of southeast- the germination of Pinus massoniana and survival of new ern Yunnan would probably prevent the seeds of P. massoniana from seedlings. Cones of P. massoniana mature from October to December germinating. (Fu et al., 1999) and shed seeds in the winter season. The seeds of this Germination studies (Yu, 1959; Qin and Ding, 2012) show that seeds conifer are ready to germinate in spring, from the beginning of March of Pinus massoniana grow and survive best under temperatures consis- to the first third of April, but will only do so if seedbeds are moist and tent with the local climate. Seeds will germinate well under the same the weather is warm enough (Cheng et al., 1975; Cheng and Fu, temperature as the parent live, and that temperature fluctuations

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