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A new Tsuga species from the upper Miocene of Yunnan, southwestern China and its palaeogeographic significance
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ScienceDirect Palaeoworld 22 (2013) 159–167
A new Tsuga species from the upper Miocene of Yunnan, southwestern China and its palaeogeographic significance Yao-Wu Xing a,b, Yusheng (Christopher) Liu c, Tao Su a, Frédéric M.B. Jacques a, Zhe-Kun Zhou a,∗ a
Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, China b Institute of Systematic Botany, University of Zürich, Zürich 8008, Switzerland c Department of Biological Sciences, Box 70703, East Tennessee State University, Johnson City, TN 37614-1710, USA Received 29 April 2013; received in revised form 26 July 2013; accepted 6 September 2013 Available online 19 September 2013
Abstract A new fossil species, Tsuga xianfengensis Xing et Zhou, n. sp., is reported based on two compressed seed cones. The fossil cones were discovered from the upper Miocene Xiaolongtan Formation at the Xianfeng Basin of Yunnan, southwestern China. The discovery of the Tsuga cones confirms the presence of Tsuga in the Miocene of central Yunnan and represents the earliest Tsuga macrofossils in the southwestern China. The new species reveals a close affinity with East Asian Tsuga species, T. chinensis and T. dumosa. It provides fossil evidence to support the molecular data that the Asian clade might be differentiated in the Miocene. © 2013 Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. All rights reserved. Keywords: Tsuga xianfengensis n. sp.; Upper Miocene; Palaeobiogeography; Yunnan; China
1. Introduction The hemlock (genus Tsuga), belonging to the family Pinaceae, is an important component of the subalpine and lowland humid coniferous and broad-leaved forests (Horikawa, 1972; Farjon, 1990; Fu et al., 1999). As Tsuga species are shade tolerant and cannot tolerate long periods of drought, they are usually considered as good indicators of the past environment (LePage, 2003; Yang et al., 2009). Up to twenty five extant species of Tsuga have been described in the past, with eight to thirteen species currently accepted by different authors (Flous, 1936; Gaussen, 1966; Zheng, 1983; Silba, 1986; Farjon, 1990; Fu et al., 1999; Eckenwalder, 2009; Farjon, 2010). Currently, the most accepted system is Farjon’s classification, which contains nine species and two of them occur in western North America, two in eastern North America, two in Japan, and three in China and Himalayas (Farjon, 1990, 2010). It is difficult to explain the biogeography of Tsuga according to phylogenetic analyses based solely on extant species (Havill et al., 2008). For instance, the latest phylogeny showed that one
∗
Corresponding author. Tel.: +86 871 6521 9932; fax: +86 871 6521 9932. E-mail address: [email protected] (Z.-K. Zhou).
eastern North American species, T. canadensis, is sister to the Asian clade whereas the other eastern North American species, T. caroliniana, is nested with Asian species (Havill et al., 2008). They accounted for this current disjunct distribution pattern as a result of an initial widespread circumpolar distribution with subsequent vicariance and extinction events. Fossil evidence provides another source to understand the biogeography of Tsuga. The fossil record of Tsuga was well represented in North America and Eurasia from the Late Cretaceous to Plio-Pleistocene including wood, leaves, seeds, pollen, and seed cones (see review in LePage, 2003). The earliest fossil record of Tsuga was represented by pollen from the Late Cretaceous (ca. 90 Ma) in Poland (Macko, 1963). During the Paleocene, fossil pollen of Tsuga was found from the Spitsbergen and Scotland (Manum, 1962; Boulter and Manum, 1989). From the Eocene to the Pliocene, Tsuga pollen spread into the whole Eurasia and North America (see review in LePage, 2003). During the Pleistocene, Tsuga pollen is found in middle latitudinal regions of Eurasia and eastern North America but disappeared in high latitudinal regions of Eurasia and western North America (see review in LePage, 2003). The earliest known Tsuga macrofossils were discovered from the middle Eocene deposits (ca. 48.7 Ma) in North America (Currah et al., 1998). By examining the distribution patterns of Tsuga fossils, LePage (2003)
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concluded that the exchange of representatives between North America and Europe occurred across the North Atlantic land bridges prior to their demise at the end of the Eocene, whereas the exchange between North America and Asia occurred throughout the Cenozoic across the Beringian Corridor. Fossil pollen records indicate that Tsuga has been widely distributed in North and Northeast China during the Cenozoic (Li, 1998; Wang, 1999; Sun and Wang, 2005; Yang et al., 2009).
During the Paleogene, Tsuga species were widely distributed in North and Northeast China at least to 48◦ N (Xia and Wang, 1987; Li, 1998). Since the Miocene, Tsuga fossil pollen records were abundant from northwestern to eastern China (Wang, 1999; Sun and Wang, 2005). However, the fossil record of Tsuga is sparse in the southwestern China where one-third of extant Tsuga occur. Up to the present, the oldest macrofossil Tsuga preserved as fossil wood in this region was discovered from the
Fig. 1. Location and sampled outcrop of fossil locality (black triangle) of Tsuga xianfengensis n. sp.
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Pliocene deposits from Yunnan Province in southwestern China, which was assigned to the extant T. dumosa (Yi et al., 2005). A few fossil cones have been reported from the late Pliocene Mula Formation, Sichuan Province (Chen et al., 1986). However, molecular phylogeny suggested that the differentiation of Asian species happened during the Miocene (Havill et al., 2008). The controversy between fossil and molecular data limited our understanding on the evolution of Tsuga. In the present study, we report a new Tsuga fossil species based on two compressed cones from the late Miocene Xianfeng flora of Yunnan. This new species is compared with all extant and selected fossil Tsuga species. The discovery of the new species confirms the presence of Tsuga in southwestern China since the late Miocene and agrees with the molecular data that the Asian lineage might be differentiated in the Miocene.
2. Geological setting Two fossil cones were collected from Xianfeng coal mine (Fig. 1; 25◦ 25 N, 102◦ 51 E, 2200 m AMSL), located about 60 km north of Kunming, Yunnan Province, southwestern China. The geology of this coal mine was discussed in several studies and the fossiliferous layers were assigned to the Xiaolongtan Formation (Fig. 2; Xing et al., 1999; Wu et al., 2006). The lithological sequence of this formation comprises four members, named as N1 1 x–N1 4 x. The present fossils were collected in the layer of N1 3 x2 , which also yielded abundant plant macrofossils, shells, and insect fragments (Xing et al., 1999; Wu et al., 2006; Xing et al., 2010, 2012, 2013). Based on mammal fossils (e.g., Potasmochoerus parvulus and Listriodon sp.) (Dong, 2001), plant macrofossils (Zhou, 1985, 2000), and pollen (Wang, 1996), the geological age of the Xiaolongtan Formation was determined as the late Miocene.
3. Materials and methods The fossil and extant cones for comparison were photographed using Canon PowerShot SX100 IS. The paratype was demineralized in cold 5% HCl for 24 h to remove all carbonates, rinsed with distilled water and immersed in 48% HF for 3–5 days. The HF was changed at least twice to ensure removal of silicates. The specimen was then rinsed with distilled water and dried in air. The internal structure of the paratype was examined using X-ray CT scanner (Comscan Techno Co. Ltd., ScanXmateA130S145) at Chuo University, Japan. All the specimens of fossil and living comparatives are housed in the Herbarium of the Kunming Institute of Botany, Chinese Academy of Sciences. Description of morphology follows terminology of Flora of China (Fu et al., 1999). To better determine its systematic position, we compared the morphology of the current fossils with both extant and fossil gymnosperm species. The morphological data of extant species are based on the Flora of China (Fu et al., 1999), Flora of North America (Taylor, 1993), and the Gymnosperm database (Earle, 1997).
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4. Results 4.1. Systematics Family Pinaceae Lindley Genus Tsuga (Endl.) Carrière Tsuga xianfengensis Xing et Zhou, n. sp. (Figs. 3A–G, 4A, D) Etymology: The specific epithet refers to the name of fossil locality. Types: Holotype: HLT 1300 (Figs. 3A, 4A, D). We choose a fragmentary seed cone as the holotype, because the complete one (HLT 1301) may represent an immature cone. Paratype: HLT 1301 (Fig. 3B–G). Diagnosis: Seed cone narrowly ovoid, symmetric. Scales ovate-elliptic to broadly ovate-elliptic, with rounded to acute apices, entire and slightly recurved margins. Bracts nearly cuneate, margin smooth. Cone axis thin. Narrow pith constructed of parenchyma cells. Seeds ovoid to oblong. Collecting locality: The Xianfeng Basin (25◦ 25 N, 102◦ 51 E), about 60 km north of Kunming, Yunnan Province, China (Fig. 1). Occurrence: The upper sub-member (N1 3 x2 ) of the third member of the Xiaolongtan Formation, upper Miocene. Repository: Herbarium of the Kunming Institute of Botany, Chinese Academy of Sciences (KUN). 4.2. Description 4.2.1. External morphology The fossil cones are narrowly ovate, closed, symmetric, 20–30 mm long, 10–15 mm wide (Fig. 3A, B). There are 16–20 woody ovuliferous scales helically arranged around the central axis. The scales are obovate, 6–10 mm long, 5–8 mm wide. The exposed part of the scale is striate. The cone scales near the apex and base of the cone are slightly smaller than those located near the middle (Fig. 3A, B). The apices of the scales are rounded to acute, entire and slightly recurved margins (Fig. 3A, B). The scales of the paratype are slightly thin, which might represent a younger cone (Fig. 3B). 4.2.2. Internal morphology The internal characters of the paratype were examined under the X-ray CT scanning (Fig. 3C–G). The cone axis is roughly 10 mm long, 1.2 mm in diameter. The pith is ca. 0.5 mm in diameter, constructed of parenchyma cells (Fig. 3C, G). Resin canals and sclerenchyma are absent from the pith (Fig. 3C, F, G). The bracts are minute, ca. 3–4 mm long, cuneate in shape (Fig. 3D, E). The seed bodies were not seen. However, there are several seed positions can be seen under the CT scanning (Fig. 3D). It shows that two seeds are borne on the adaxial surface of each ovuliferous scale (Fig. 3D). The seeds are ovoid-oblong, 2–3 mm long, and 1.5–2 mm wide (Fig. 3D). The seed wing cannot be seen.
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Fig. 2. Stratigraphy and lithology of the Xianfeng coal mine (after Xing et al., 2010). The member where the fossils were collected is marked as pentagram.
5. Discussion The fossils possess helically arranged cone-scale complex. In all gymnosperm families, only Pinaceae and Araucariaceae have such cone-scale complex. However, Araucariaceae scales are one-seeded and without distinct bracts, which are different from the current fossils (Silba, 1986). Thus, these two fossils can be clearly assigned to the family Pinaceae. The current
fossils can be distinguished from the genera Pinus (4–50 cm long, Frankis, 2002), Cedrus (5–10 cm long, Vidakovic, 1991), Abies (6–30 cm long, Farjon, 1990), Picea (5–18 cm long, Fu et al., 1999) and Keteleeria (6–25 cm long, Fu et al., 1999) in the Pinaceae, which have much larger cone (Fu et al., 1999). The present fossils are differentiated from Cathaya by having thinner scales than Cathaya (Fu et al., 1999). Pseudotsuga could be easily distinguished from the current fossils in having distinctly
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Fig. 3. The seed cones of Tsuga xianfengensis. (A) Holotype of T. xianfengensis (HLT 1300), showing bracts (Br). (B) Paratype of T. xianfengensis (HLT 1301). (C) Longitudinal scanning of the paratype (HLT 1301) showing the helically arranged cone scales (Sc), bracts (Br), and the central pith (P). (D) Longitudinal scanning of the paratype (HLT 1301) showing the seed positions (Sp) and the bract. (E) Close up of the bract (Br) of the paratype (HLT 1301). (F) Transactional scanning the paratype (HLT 1301) showing the helically arranged scales and the pith (P). (G) Longitudinal scanning the paratype (HLT 1301) showing the helically arranged scales and the pith (P). Scale bar = 1 cm.
exserted bracts and Pseudolarix differs from our fossils in having ovate-lanceolate (pointed triangular) scales (Fu et al., 1999). Our fossils share similar cone size, shapes and scale characters with the genera Larix and Tsuga. However, Larix has ovate or lanceolate bracts (Fu et al., 1999) whereas our fossils have cuneate bracts. Thus, the features of current fossils leave no doubt that the cones belong to the genus Tsuga. In order to better determine the taxonomy of current fossils, we compared them with both extant and fossil species based on the characters of the cones (Table 1). 5.1. Comparison with living species of Tsuga The cone-scale complex characters of the genus Tsuga are very important features and can provide reliable identification
and separation of living and fossil species (LePage, 2003). Seed cones of T. xianfengensis are narrowly ovate, the scales are obovate, scale apex is nearly rounded and margins are slightly recurved, and the bracts are cuneate. The western North American species, T. mertensiana, differs from T. xianfengensis in several characters such as having oblong cylindric cone shape, larger cone size and ligulate to cuspidate bract shape (Table 1; Taylor, 1993; LePage, 2003). T. diversifolia differs from T. xianfengensis in possessing a smooth, not striate, exposed part of the scales (Table 1; Earle, 1997). The fossils could not be distinguished from other extant species by cone shape, size, and other external features. However, bract morphology is a useful, but commonly overlooked, feature for species level segregation in the family Pinaceae (Liu, 1971; LePage and Basinger, 1991, 1995; LePage, 2001). After examining the bract morphology
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Table 1 Comparison of Tsuga xianfengensis n. sp. to living and fossil Tsuga species. Distribution
Cone shape
Cone size (length × width, cm)
Scale shape
Scale size (length × width, cm)
Scale apex
Exposed part of scale
Bract shape
Tsuga xianfengensis n. sp.
Yunnan, southwestern China
Narrowly ovate
2–3 × 1–1.5
Obovate to narrowly ovate
0.6–0.8 × 0.5–0.8
Striate, margin not thickened
Cuneate
T. dumosa
Himalayan region
Ovate or narrowly ovate
1.5–3 × 1–2
Obovate-orbicular
1–1.4 × 0.7–1.2
Striate, margin not thickened
T. chinensis
South China
Ovate
1.5–2.5 × 1.2–1.6
Pentagonal-ovate, subsquare, or suborbicular
0.9–1.2 × 0.8–1.1
Nearly rounded to acute, entire, margins slightly recurved Nearly round to acute, entire, margins slightly recurved Rounded or nearly truncate
T. forrestii
Southwestern China
Narrowly ovoid or ovoid-cylindric
(2)2.5–4 × 1.5–3
Narrowly ovate or oblong
1.3–1.5 × 1–1.3
Rounded or nearly truncate
Striate, glabrous, margin thickened
T. sieboldii
South Japan
Ovoid-conic
(1.6)2–2.5 × 1.4–2
Nearly round
0.8–1.2 × 0.8–1.2
Rounded
Striate
T. diversifolia
North Japan
Ovate to elliptic
1.5–2.5 × 1.5–2
Orbicular to ovate
0.5–1.2 × 0.4–1
Not striate
T. heterophylla
West North America
Ovoid
1.5–2.5 × 1.5–2.5
0.5–1.6 × 0.4–1
Striate
T. caroliniana
East North America East North America
Ovate to elliptic
2.5–4 × 1.5–2.5
Suborbicular to ovate to ovoid-oblong to oblong Ovate to cuneate
Rounded and entire Rounded to obtuse
Cuneate-rhombic, margin denticulate, apex 2-lobed Cuneate-obovate or obtriangular, apex erose, sometimes 2-lobed Cuneate-obovate or obtriangular, apex erose Obtriangular and apically denticulate Truncate and bi-apiculate Triangular
0.6–2 × 0.5–1.2
Striate
Weakly trilobite
Ovoid
1.5–2.5 × 1–1.5
Ovate to cuneate
0.5–1.2 × 0.4–1
Striate
West North America
Oblong to cylindric Elliptic to narrow elliptic
3–8 × 1.1–3
Obovate to cuneate Orbiculate to wide elliptic
0.5–1.5 × 0.5–0.7
Flabellate to truncate and denticulate Ligulate to cuspidate Ligulate to cuspidate
T. canadensis
T. mertensiana T. swedaea (fossil)
2–3.2 × 1–1.5
0.5–1 × 0.5–0.7
Rounded and entire Rounded and often projected outward Rounded to acute Rounded and entire
Striate, glabrous
Not striate Not striate
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Species
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Fig. 4. Comparison the fossil cones and bract with the extant East Asian Tsuga species. (A, D) HLT 1300; (B, E) T. chinensis, KUN 0012413; (C, F) T. chinensis, KUN 0142646; (G, J, H, K) T. dumosa, KUN 0012727; (I, L) T. forrestii, KUN 0143088. Scale bar = 5 mm.
of the extant species, LePage (2003) stated that the bract shape is distinct within all extant species (Table 1). As T. xianfengensis has cuneate bracts, it could be distinguished from T. sieboldii, T. diversifolia, T. heterophylla, T. caroliniana, and T. candensis, which all have different bract shapes (Table 1). Though LePage (2003) stated that all extant species possess distinct bracts, our examination showed that bract shape is not a
stable character at least in three species from the southwestern China and each species in this region usually possesses different types of bracts (Fig. 4E, F, J–L). However, the cuneate bract could only be found in the three East Asian species. In these three extant species, T. forrestii usually has thickened scale margins, which is different from the current fossils (Fu et al., 1999). Thus, according to the above discussions, T. xianfengensis
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shows a clear affinity with two Asian species, T. chinensis and T. dumosa. 5.2. Comparison with the fossil species of Tsuga The fossil record of Tsuga seed cones is relatively rare. Most of published seed cones usually lack detailed descriptions for comparison. T. swedaea was reported from the middle Eocene of Canada and represents the only fossil Tsuga cones with a detailed description (LePage, 2003). T. swedaea resembles the living species T. mertensiana. It differs from T. xianfengensis in several characters such as cone shape, size, bract-scale complex and seed morphology (Table 1). In southwestern China, Chen et al. (1986) reported some Tsuga fossils of the late Pliocene to early Pleistocene age from the Mula Formation, Sichuan Province. Because the fossils are impressions, only gross morphology was described. The reported fossil cones are ovate-elliptic, 20 mm long and 12 mm wide (Chen et al., 1986). Based on comparisons of cone size and scale shape, the fossils are thought similar to the extant T. dumosa and T. forrestii. Though the gross morphology of Tsuga species from the Mula Formation is also similar to our fossil cones, due to the lack of detailed anatomy, their affinity could not be ascertained here. The comparisons with both the extant and fossil Tsuga species demonstrate that our fossils have a closest affinity with two extant Asian species, T. chinensis and T. dumosa. As no further determination could be made, we describe it as a new species. 5.3. Ecological and palaeogeographical implications of Tsuga xianfengensis Modern Tsuga species are shade tolerant and cannot tolerate long periods of drought, and they require at least 720 mm mean annual precipitation and 634 mm precipitation during growing season in the Asian monsoon region (Yang et al., 2009). In southwestern China, Tsuga species usually occur in the broadleaved evergreen forests (Fu et al., 1999). The closely related extant species of T. xianfengensis, T. chinensis and T. dumosa, all require a warm and humid climate. T. chinensis requires an MAT of 10.9–18.6 ◦ C and an MAP of 635–1489 mm (Yang et al., 2009) and T. dumosa requires an MAT of 15.7–21.7 ◦ C and an MAP of 1096–1864 mm (Utescher and Mosbrugger, 1997–2012). Thus, the discovery of the new Tsuga cones indicates a relatively humid climate in the late Miocene of the central Yunnan, which is also consistent with the palaeoclimatic reconstructions of the Xianfeng flora. The recent palaeoclimatic reconstruction shows that the Xianfeng flora had a warmer (MAT from Coexistence approach: 17.2–21.7 ◦ C) and much more humid (MAP from Coexistence approach: 1206.0–1613.0 mm) climate than the present (MAT: 14.9 ◦ C; MAP: 1003.2 mm) during the late Miocene (Xing et al., 2012). As mentioned above, molecular data suggested that the differentiation of the Asian Tsuga species happened in the Miocene (Havill et al., 2008). However, the previous fossil records of Tsuga in southwestern China, such as the Tsuga wood fossil from the Yangyi Formation (Yi et al., 2005) and fossil cones
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ScienceDirect Palaeoworld 22 (2013) 159–167
A new Tsuga species from the upper Miocene of Yunnan, southwestern China and its palaeogeographic significance Yao-Wu Xing a,b, Yusheng (Christopher) Liu c, Tao Su a, Frédéric M.B. Jacques a, Zhe-Kun Zhou a,∗ a
Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, China b Institute of Systematic Botany, University of Zürich, Zürich 8008, Switzerland c Department of Biological Sciences, Box 70703, East Tennessee State University, Johnson City, TN 37614-1710, USA Received 29 April 2013; received in revised form 26 July 2013; accepted 6 September 2013 Available online 19 September 2013
Abstract A new fossil species, Tsuga xianfengensis Xing et Zhou, n. sp., is reported based on two compressed seed cones. The fossil cones were discovered from the upper Miocene Xiaolongtan Formation at the Xianfeng Basin of Yunnan, southwestern China. The discovery of the Tsuga cones confirms the presence of Tsuga in the Miocene of central Yunnan and represents the earliest Tsuga macrofossils in the southwestern China. The new species reveals a close affinity with East Asian Tsuga species, T. chinensis and T. dumosa. It provides fossil evidence to support the molecular data that the Asian clade might be differentiated in the Miocene. © 2013 Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. All rights reserved. Keywords: Tsuga xianfengensis n. sp.; Upper Miocene; Palaeobiogeography; Yunnan; China
1. Introduction The hemlock (genus Tsuga), belonging to the family Pinaceae, is an important component of the subalpine and lowland humid coniferous and broad-leaved forests (Horikawa, 1972; Farjon, 1990; Fu et al., 1999). As Tsuga species are shade tolerant and cannot tolerate long periods of drought, they are usually considered as good indicators of the past environment (LePage, 2003; Yang et al., 2009). Up to twenty five extant species of Tsuga have been described in the past, with eight to thirteen species currently accepted by different authors (Flous, 1936; Gaussen, 1966; Zheng, 1983; Silba, 1986; Farjon, 1990; Fu et al., 1999; Eckenwalder, 2009; Farjon, 2010). Currently, the most accepted system is Farjon’s classification, which contains nine species and two of them occur in western North America, two in eastern North America, two in Japan, and three in China and Himalayas (Farjon, 1990, 2010). It is difficult to explain the biogeography of Tsuga according to phylogenetic analyses based solely on extant species (Havill et al., 2008). For instance, the latest phylogeny showed that one
∗
Corresponding author. Tel.: +86 871 6521 9932; fax: +86 871 6521 9932. E-mail address: [email protected] (Z.-K. Zhou).
eastern North American species, T. canadensis, is sister to the Asian clade whereas the other eastern North American species, T. caroliniana, is nested with Asian species (Havill et al., 2008). They accounted for this current disjunct distribution pattern as a result of an initial widespread circumpolar distribution with subsequent vicariance and extinction events. Fossil evidence provides another source to understand the biogeography of Tsuga. The fossil record of Tsuga was well represented in North America and Eurasia from the Late Cretaceous to Plio-Pleistocene including wood, leaves, seeds, pollen, and seed cones (see review in LePage, 2003). The earliest fossil record of Tsuga was represented by pollen from the Late Cretaceous (ca. 90 Ma) in Poland (Macko, 1963). During the Paleocene, fossil pollen of Tsuga was found from the Spitsbergen and Scotland (Manum, 1962; Boulter and Manum, 1989). From the Eocene to the Pliocene, Tsuga pollen spread into the whole Eurasia and North America (see review in LePage, 2003). During the Pleistocene, Tsuga pollen is found in middle latitudinal regions of Eurasia and eastern North America but disappeared in high latitudinal regions of Eurasia and western North America (see review in LePage, 2003). The earliest known Tsuga macrofossils were discovered from the middle Eocene deposits (ca. 48.7 Ma) in North America (Currah et al., 1998). By examining the distribution patterns of Tsuga fossils, LePage (2003)
1871-174X/$ – see front matter © 2013 Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. All rights reserved. http://dx.doi.org/10.1016/j.palwor.2013.09.003
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concluded that the exchange of representatives between North America and Europe occurred across the North Atlantic land bridges prior to their demise at the end of the Eocene, whereas the exchange between North America and Asia occurred throughout the Cenozoic across the Beringian Corridor. Fossil pollen records indicate that Tsuga has been widely distributed in North and Northeast China during the Cenozoic (Li, 1998; Wang, 1999; Sun and Wang, 2005; Yang et al., 2009).
During the Paleogene, Tsuga species were widely distributed in North and Northeast China at least to 48◦ N (Xia and Wang, 1987; Li, 1998). Since the Miocene, Tsuga fossil pollen records were abundant from northwestern to eastern China (Wang, 1999; Sun and Wang, 2005). However, the fossil record of Tsuga is sparse in the southwestern China where one-third of extant Tsuga occur. Up to the present, the oldest macrofossil Tsuga preserved as fossil wood in this region was discovered from the
Fig. 1. Location and sampled outcrop of fossil locality (black triangle) of Tsuga xianfengensis n. sp.
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Pliocene deposits from Yunnan Province in southwestern China, which was assigned to the extant T. dumosa (Yi et al., 2005). A few fossil cones have been reported from the late Pliocene Mula Formation, Sichuan Province (Chen et al., 1986). However, molecular phylogeny suggested that the differentiation of Asian species happened during the Miocene (Havill et al., 2008). The controversy between fossil and molecular data limited our understanding on the evolution of Tsuga. In the present study, we report a new Tsuga fossil species based on two compressed cones from the late Miocene Xianfeng flora of Yunnan. This new species is compared with all extant and selected fossil Tsuga species. The discovery of the new species confirms the presence of Tsuga in southwestern China since the late Miocene and agrees with the molecular data that the Asian lineage might be differentiated in the Miocene.
2. Geological setting Two fossil cones were collected from Xianfeng coal mine (Fig. 1; 25◦ 25 N, 102◦ 51 E, 2200 m AMSL), located about 60 km north of Kunming, Yunnan Province, southwestern China. The geology of this coal mine was discussed in several studies and the fossiliferous layers were assigned to the Xiaolongtan Formation (Fig. 2; Xing et al., 1999; Wu et al., 2006). The lithological sequence of this formation comprises four members, named as N1 1 x–N1 4 x. The present fossils were collected in the layer of N1 3 x2 , which also yielded abundant plant macrofossils, shells, and insect fragments (Xing et al., 1999; Wu et al., 2006; Xing et al., 2010, 2012, 2013). Based on mammal fossils (e.g., Potasmochoerus parvulus and Listriodon sp.) (Dong, 2001), plant macrofossils (Zhou, 1985, 2000), and pollen (Wang, 1996), the geological age of the Xiaolongtan Formation was determined as the late Miocene.
3. Materials and methods The fossil and extant cones for comparison were photographed using Canon PowerShot SX100 IS. The paratype was demineralized in cold 5% HCl for 24 h to remove all carbonates, rinsed with distilled water and immersed in 48% HF for 3–5 days. The HF was changed at least twice to ensure removal of silicates. The specimen was then rinsed with distilled water and dried in air. The internal structure of the paratype was examined using X-ray CT scanner (Comscan Techno Co. Ltd., ScanXmateA130S145) at Chuo University, Japan. All the specimens of fossil and living comparatives are housed in the Herbarium of the Kunming Institute of Botany, Chinese Academy of Sciences. Description of morphology follows terminology of Flora of China (Fu et al., 1999). To better determine its systematic position, we compared the morphology of the current fossils with both extant and fossil gymnosperm species. The morphological data of extant species are based on the Flora of China (Fu et al., 1999), Flora of North America (Taylor, 1993), and the Gymnosperm database (Earle, 1997).
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4. Results 4.1. Systematics Family Pinaceae Lindley Genus Tsuga (Endl.) Carrière Tsuga xianfengensis Xing et Zhou, n. sp. (Figs. 3A–G, 4A, D) Etymology: The specific epithet refers to the name of fossil locality. Types: Holotype: HLT 1300 (Figs. 3A, 4A, D). We choose a fragmentary seed cone as the holotype, because the complete one (HLT 1301) may represent an immature cone. Paratype: HLT 1301 (Fig. 3B–G). Diagnosis: Seed cone narrowly ovoid, symmetric. Scales ovate-elliptic to broadly ovate-elliptic, with rounded to acute apices, entire and slightly recurved margins. Bracts nearly cuneate, margin smooth. Cone axis thin. Narrow pith constructed of parenchyma cells. Seeds ovoid to oblong. Collecting locality: The Xianfeng Basin (25◦ 25 N, 102◦ 51 E), about 60 km north of Kunming, Yunnan Province, China (Fig. 1). Occurrence: The upper sub-member (N1 3 x2 ) of the third member of the Xiaolongtan Formation, upper Miocene. Repository: Herbarium of the Kunming Institute of Botany, Chinese Academy of Sciences (KUN). 4.2. Description 4.2.1. External morphology The fossil cones are narrowly ovate, closed, symmetric, 20–30 mm long, 10–15 mm wide (Fig. 3A, B). There are 16–20 woody ovuliferous scales helically arranged around the central axis. The scales are obovate, 6–10 mm long, 5–8 mm wide. The exposed part of the scale is striate. The cone scales near the apex and base of the cone are slightly smaller than those located near the middle (Fig. 3A, B). The apices of the scales are rounded to acute, entire and slightly recurved margins (Fig. 3A, B). The scales of the paratype are slightly thin, which might represent a younger cone (Fig. 3B). 4.2.2. Internal morphology The internal characters of the paratype were examined under the X-ray CT scanning (Fig. 3C–G). The cone axis is roughly 10 mm long, 1.2 mm in diameter. The pith is ca. 0.5 mm in diameter, constructed of parenchyma cells (Fig. 3C, G). Resin canals and sclerenchyma are absent from the pith (Fig. 3C, F, G). The bracts are minute, ca. 3–4 mm long, cuneate in shape (Fig. 3D, E). The seed bodies were not seen. However, there are several seed positions can be seen under the CT scanning (Fig. 3D). It shows that two seeds are borne on the adaxial surface of each ovuliferous scale (Fig. 3D). The seeds are ovoid-oblong, 2–3 mm long, and 1.5–2 mm wide (Fig. 3D). The seed wing cannot be seen.
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Fig. 2. Stratigraphy and lithology of the Xianfeng coal mine (after Xing et al., 2010). The member where the fossils were collected is marked as pentagram.
5. Discussion The fossils possess helically arranged cone-scale complex. In all gymnosperm families, only Pinaceae and Araucariaceae have such cone-scale complex. However, Araucariaceae scales are one-seeded and without distinct bracts, which are different from the current fossils (Silba, 1986). Thus, these two fossils can be clearly assigned to the family Pinaceae. The current
fossils can be distinguished from the genera Pinus (4–50 cm long, Frankis, 2002), Cedrus (5–10 cm long, Vidakovic, 1991), Abies (6–30 cm long, Farjon, 1990), Picea (5–18 cm long, Fu et al., 1999) and Keteleeria (6–25 cm long, Fu et al., 1999) in the Pinaceae, which have much larger cone (Fu et al., 1999). The present fossils are differentiated from Cathaya by having thinner scales than Cathaya (Fu et al., 1999). Pseudotsuga could be easily distinguished from the current fossils in having distinctly
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Fig. 3. The seed cones of Tsuga xianfengensis. (A) Holotype of T. xianfengensis (HLT 1300), showing bracts (Br). (B) Paratype of T. xianfengensis (HLT 1301). (C) Longitudinal scanning of the paratype (HLT 1301) showing the helically arranged cone scales (Sc), bracts (Br), and the central pith (P). (D) Longitudinal scanning of the paratype (HLT 1301) showing the seed positions (Sp) and the bract. (E) Close up of the bract (Br) of the paratype (HLT 1301). (F) Transactional scanning the paratype (HLT 1301) showing the helically arranged scales and the pith (P). (G) Longitudinal scanning the paratype (HLT 1301) showing the helically arranged scales and the pith (P). Scale bar = 1 cm.
exserted bracts and Pseudolarix differs from our fossils in having ovate-lanceolate (pointed triangular) scales (Fu et al., 1999). Our fossils share similar cone size, shapes and scale characters with the genera Larix and Tsuga. However, Larix has ovate or lanceolate bracts (Fu et al., 1999) whereas our fossils have cuneate bracts. Thus, the features of current fossils leave no doubt that the cones belong to the genus Tsuga. In order to better determine the taxonomy of current fossils, we compared them with both extant and fossil species based on the characters of the cones (Table 1). 5.1. Comparison with living species of Tsuga The cone-scale complex characters of the genus Tsuga are very important features and can provide reliable identification
and separation of living and fossil species (LePage, 2003). Seed cones of T. xianfengensis are narrowly ovate, the scales are obovate, scale apex is nearly rounded and margins are slightly recurved, and the bracts are cuneate. The western North American species, T. mertensiana, differs from T. xianfengensis in several characters such as having oblong cylindric cone shape, larger cone size and ligulate to cuspidate bract shape (Table 1; Taylor, 1993; LePage, 2003). T. diversifolia differs from T. xianfengensis in possessing a smooth, not striate, exposed part of the scales (Table 1; Earle, 1997). The fossils could not be distinguished from other extant species by cone shape, size, and other external features. However, bract morphology is a useful, but commonly overlooked, feature for species level segregation in the family Pinaceae (Liu, 1971; LePage and Basinger, 1991, 1995; LePage, 2001). After examining the bract morphology
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Table 1 Comparison of Tsuga xianfengensis n. sp. to living and fossil Tsuga species. Distribution
Cone shape
Cone size (length × width, cm)
Scale shape
Scale size (length × width, cm)
Scale apex
Exposed part of scale
Bract shape
Tsuga xianfengensis n. sp.
Yunnan, southwestern China
Narrowly ovate
2–3 × 1–1.5
Obovate to narrowly ovate
0.6–0.8 × 0.5–0.8
Striate, margin not thickened
Cuneate
T. dumosa
Himalayan region
Ovate or narrowly ovate
1.5–3 × 1–2
Obovate-orbicular
1–1.4 × 0.7–1.2
Striate, margin not thickened
T. chinensis
South China
Ovate
1.5–2.5 × 1.2–1.6
Pentagonal-ovate, subsquare, or suborbicular
0.9–1.2 × 0.8–1.1
Nearly rounded to acute, entire, margins slightly recurved Nearly round to acute, entire, margins slightly recurved Rounded or nearly truncate
T. forrestii
Southwestern China
Narrowly ovoid or ovoid-cylindric
(2)2.5–4 × 1.5–3
Narrowly ovate or oblong
1.3–1.5 × 1–1.3
Rounded or nearly truncate
Striate, glabrous, margin thickened
T. sieboldii
South Japan
Ovoid-conic
(1.6)2–2.5 × 1.4–2
Nearly round
0.8–1.2 × 0.8–1.2
Rounded
Striate
T. diversifolia
North Japan
Ovate to elliptic
1.5–2.5 × 1.5–2
Orbicular to ovate
0.5–1.2 × 0.4–1
Not striate
T. heterophylla
West North America
Ovoid
1.5–2.5 × 1.5–2.5
0.5–1.6 × 0.4–1
Striate
T. caroliniana
East North America East North America
Ovate to elliptic
2.5–4 × 1.5–2.5
Suborbicular to ovate to ovoid-oblong to oblong Ovate to cuneate
Rounded and entire Rounded to obtuse
Cuneate-rhombic, margin denticulate, apex 2-lobed Cuneate-obovate or obtriangular, apex erose, sometimes 2-lobed Cuneate-obovate or obtriangular, apex erose Obtriangular and apically denticulate Truncate and bi-apiculate Triangular
0.6–2 × 0.5–1.2
Striate
Weakly trilobite
Ovoid
1.5–2.5 × 1–1.5
Ovate to cuneate
0.5–1.2 × 0.4–1
Striate
West North America
Oblong to cylindric Elliptic to narrow elliptic
3–8 × 1.1–3
Obovate to cuneate Orbiculate to wide elliptic
0.5–1.5 × 0.5–0.7
Flabellate to truncate and denticulate Ligulate to cuspidate Ligulate to cuspidate
T. canadensis
T. mertensiana T. swedaea (fossil)
2–3.2 × 1–1.5
0.5–1 × 0.5–0.7
Rounded and entire Rounded and often projected outward Rounded to acute Rounded and entire
Striate, glabrous
Not striate Not striate
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Species
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Fig. 4. Comparison the fossil cones and bract with the extant East Asian Tsuga species. (A, D) HLT 1300; (B, E) T. chinensis, KUN 0012413; (C, F) T. chinensis, KUN 0142646; (G, J, H, K) T. dumosa, KUN 0012727; (I, L) T. forrestii, KUN 0143088. Scale bar = 5 mm.
of the extant species, LePage (2003) stated that the bract shape is distinct within all extant species (Table 1). As T. xianfengensis has cuneate bracts, it could be distinguished from T. sieboldii, T. diversifolia, T. heterophylla, T. caroliniana, and T. candensis, which all have different bract shapes (Table 1). Though LePage (2003) stated that all extant species possess distinct bracts, our examination showed that bract shape is not a
stable character at least in three species from the southwestern China and each species in this region usually possesses different types of bracts (Fig. 4E, F, J–L). However, the cuneate bract could only be found in the three East Asian species. In these three extant species, T. forrestii usually has thickened scale margins, which is different from the current fossils (Fu et al., 1999). Thus, according to the above discussions, T. xianfengensis
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shows a clear affinity with two Asian species, T. chinensis and T. dumosa. 5.2. Comparison with the fossil species of Tsuga The fossil record of Tsuga seed cones is relatively rare. Most of published seed cones usually lack detailed descriptions for comparison. T. swedaea was reported from the middle Eocene of Canada and represents the only fossil Tsuga cones with a detailed description (LePage, 2003). T. swedaea resembles the living species T. mertensiana. It differs from T. xianfengensis in several characters such as cone shape, size, bract-scale complex and seed morphology (Table 1). In southwestern China, Chen et al. (1986) reported some Tsuga fossils of the late Pliocene to early Pleistocene age from the Mula Formation, Sichuan Province. Because the fossils are impressions, only gross morphology was described. The reported fossil cones are ovate-elliptic, 20 mm long and 12 mm wide (Chen et al., 1986). Based on comparisons of cone size and scale shape, the fossils are thought similar to the extant T. dumosa and T. forrestii. Though the gross morphology of Tsuga species from the Mula Formation is also similar to our fossil cones, due to the lack of detailed anatomy, their affinity could not be ascertained here. The comparisons with both the extant and fossil Tsuga species demonstrate that our fossils have a closest affinity with two extant Asian species, T. chinensis and T. dumosa. As no further determination could be made, we describe it as a new species. 5.3. Ecological and palaeogeographical implications of Tsuga xianfengensis Modern Tsuga species are shade tolerant and cannot tolerate long periods of drought, and they require at least 720 mm mean annual precipitation and 634 mm precipitation during growing season in the Asian monsoon region (Yang et al., 2009). In southwestern China, Tsuga species usually occur in the broadleaved evergreen forests (Fu et al., 1999). The closely related extant species of T. xianfengensis, T. chinensis and T. dumosa, all require a warm and humid climate. T. chinensis requires an MAT of 10.9–18.6 ◦ C and an MAP of 635–1489 mm (Yang et al., 2009) and T. dumosa requires an MAT of 15.7–21.7 ◦ C and an MAP of 1096–1864 mm (Utescher and Mosbrugger, 1997–2012). Thus, the discovery of the new Tsuga cones indicates a relatively humid climate in the late Miocene of the central Yunnan, which is also consistent with the palaeoclimatic reconstructions of the Xianfeng flora. The recent palaeoclimatic reconstruction shows that the Xianfeng flora had a warmer (MAT from Coexistence approach: 17.2–21.7 ◦ C) and much more humid (MAP from Coexistence approach: 1206.0–1613.0 mm) climate than the present (MAT: 14.9 ◦ C; MAP: 1003.2 mm) during the late Miocene (Xing et al., 2012). As mentioned above, molecular data suggested that the differentiation of the Asian Tsuga species happened in the Miocene (Havill et al., 2008). However, the previous fossil records of Tsuga in southwestern China, such as the Tsuga wood fossil from the Yangyi Formation (Yi et al., 2005) and fossil cones
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