Leaf and infructescence fossils of Alnus (Betulaceae) from the late Eocene of the southeastern Qinghai–Tibetan Plateau
Abstract
Plant fossils from the Qinghai–Tibetan Plateau (QTP), China are critical to understand not only the diversification history of plants there, but also the paleoenvironmental conditions. Alnus are deciduous trees, mainly distributed in temperate and subtropical regions of Eurasia and North America, and they are well known in the fossil records throughout the Cenozoic in the Northern Hemisphere. We collected numerous well‐preserved Alnus leaf and infructescence fossils from the Lawula Formation (∼34.6 Ma with 40Ar/39Ar dating) at the present elevation of 3910 m a.s.l. in the southeastern QTP. Based on detailed morphological comparisons with existing and fossil species, these fossils show closest affinity to Alnus ferdinandi‐coburgii C. K. Schneid., and we refer to these fossils as A . cf. ferdinandi‐coburgii . These specimens comprise the oldest megafossil record of Alnus in the QTP, and provide solid evidence for the distribution of Alnus there as early as the late Eocene. Extant A . ferdinandi‐coburgii is distributed in areas with mean annual temperature values between 9.7 °C and 16.9 °C, and mean annual precipitation values ranging from 896.2 mm to 1161.2 mm; therefore, fossils of A . cf. ferdinandi‐coburgii suggest a much warmer and wetter climate during the late Eocene than today in the southeastern QTP. This finding is consistent with other evidence for continued uplift of the southeastern QTP after the late Eocene that might be due to the eastward extension of the QTP.
1 Introduction
The Cenozoic uplift of the Qinghai–Tibetan Plateau (QTP) greatly influenced the topography and the climate in Asia (Molnar et al., 2010; Spicer, 2017); however, details of the paleoenvironmental history of the QTP are still under debate (Deng & Ding, 2015). Plant fossils are good indicators of paleoenvironments because their morphology and distribution are related to environmental conditions (Wing & Greenwood, 1993; Wolfe, 1995; Mosbrugger & Utescher, 1997; Tiffney & Manchester, 2001; Jordan, 2011; Morueta‐Holme et al., 2015). Cenozoic floras in the QTP have been studied for decades (Xu et al., 1973; WGCPC, 1978; Spicer et al., 2003; Huang et al., 2016), but plant fossils uncovered from the QTP are still rare. These limited previous paleobotanical studies indicate high plant diversity and dramatic environmental changes on the QTP during the geological past (Tao, 2000; Su et al., 2014; Sun et al., 2015; Xu et al., 2016).
Betulaceae, the birch family, with six genera and approximately 150–200 species of deciduous shrubs or trees, is distributed mainly throughout Eurasia, and North and South America (Li & Skvortsov, 1999). Alnus , as the sister group to the remaining extant Betulaceae (Chen et al., 1999), comprises 26 deciduous tree species widely distributed in temperate and subtropical areas of Eurasia and North America, and some species extend into the northern part of Africa, the Caribbean, and the Andes in South America (Chen, 1994; Ren, 2010). Among the 10 species of Alnus that are native to China, five are endemic (Li & Skvortsov, 1999). Alnus cremastogyne Burkill, A. ferdinandi‐coburgii C. K. Schneid., A. nepalensis D. Don, and A. nitida (Spach) Endl. are distributed in the southern and eastern margins of the QTP, with elevation ranging no more than 3600 m (Ren, 2010).
Many Alnus megafossils have been uncovered from Cenozoic strata in the Northern Hemisphere (Liu et al., 2014). Leaf fossils of Alnus are widely reported from North America, Europe, and Asia (Crane, 1989). Fossilized Alnus infructescences have been found in North America, Europe, and Asia since the Eocene (Hollick, 1936; Crane, 1989; Meyer & Manchester, 1997; Dillhoff et al., 2005, 2013; Liu et al., 2014). Among fossil records in China, Alnus leaf fossils are quite common but only a few infructescence fossils have been reported (WGCPC, 1978). Among the Chinese records, most occurrences have been in the northeastern and southwestern parts of China (WGCPC, 1978). No Alnus infructescence fossils have been reported previously from the QTP.
Despite the wide distribution of Alnus in the margins of the QTP today, their fossil records in the QTP are still quite rare; only pollen grains of Alnipollenites have been found from the Paleocene to Eocene Lulehe Formation in the northeastern QTP (The Research Institute of Qinghai Petroleum Exploration and Development, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, 1985), and leaf fossils from the Lawula Formation of Markam, southeastern QTP (Tao & Du, 1987). Recently, we collected many Alnus leaf and infructescence fossils from the upper Eocene Lawula Formation of Markam, eastern Tibet, China, which are morphologically different from previous leaf fossil records from the same formation. These represent the earliest megafossil record of Alnus in the QTP. These fossils could not only shed light on the evolution of Alnus in the QTP, but also provide important evidence regarding the paleoenvironmental changes in the southeastern QTP.
2 Material and Methods
2.1 Geological setting
These fossils were collected from Kajun village, approximately 16 km northwest of Gatuo Town in Markam County, southeastern QTP, China (29°45′10″N, 098°25′58″E; 3910 m a.s.l.; Fig. 1). The fossil‐bearing layer belongs to the Lawula Formation, which consists of interbedded mudstones, sandstones, and volcanic rocks (Tao & Du, 1987). Strata of the Lawula Formation are widely distributed in eastern Tibet (Bureau of Geology and Mineral Resources of Xizang Autonomous Region (BGMRXAR), 1997). Fossil materials in our study were collected from mudstones in the lower part of the formation. The age of Kajun flora is 34.6 Ma constrained by 40Ar/39Ar dating (Su et al., 2018), which is in agreement with previous radiometric study of the Lawula Formation (Zhang et al., 2005). The stratigraphy of the Lawula Formation was described in detail by Su et al. (2018, 2014).
2.2 Morphological observation
Fossils in this study were photographed with a Nikon D700 digital camera (Tokyo, Japan). Detailed morphological characteristics were examined and photographed with a Zeiss SteREO Discovery V20 stereomicroscope (Heidenheim, Germany). Because all fossil materials in this study were preserved as impressions, we could not obtain any cuticles for anatomical observation.
To determine the systematic affinities of these fossil specimens, we compared them with modern specimens of Betulaceae housed in herbaria from the Kunming Institute of Botany (KUN) and the Xishuangbanna Tropical Botanical Garden (HITBC); we also compared these fossils with the imagery accessible online of specimens from the Herbarium of the French National Museum of Natural History (http://www.mnhn.fr), the Herbarium of Royal Botanical Gardens, Kew (http://www.kew.org/), the National Herbarium of The Netherlands (NHN) (http://vstbol.leidenuniv.nl/), and the Chinese Virtual Herbarium (CVH; http://www.cvh.org.cn). The terminology used to describe leaf morphology follows the Leaf Architecture Working Group (Ellis et al., 2009).
3 Systematics
Order Fagales Engler
Family Betulaceae Gray
Genus Alnus Miller
Species Alnus cf. ferdinandi‐coburgii C. K. Schneid.
Specimens checked Leaves : MK3‐1488 (Fig. 2A), MK3‐2483 (Fig. 2B), MK3‐2488A (Fig. 2C); Infructescences : MK3‐1778A (Fig. 3A), MK3‐1783B (Fig. 3D), MK3‐2581B (Fig. 3E), MK3‐2582A (Fig. 3F), MK3‐1777A (Fig. 3G).
Repository The laboratory of the Palaeoecology Research Group, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, China.
Locality The Upper Eocene Lawula Formation (34.6 Ma), Kajun village, Markam County, southeastern Tibet, China.
Description Leaf : Leaf petiolate, simple, petiole ∼0.8 mm long and ∼0.6 mm wide (Fig. 2A); Blades notophyll, 4.7–4.9 cm long, 1.9–3.2 cm wide, L: W ratio 1.5–2.5, elliptic to obovate with medial symmetry and basal asymmetry (Figs. 2A–2C). Leaf apex acuminate or acute (Figs. 2A, 2B), base cuneate or wide cuneate (Figs. 2A, 2C). Margin unlobed and double serrate (Fig. 2F), teeth distributed regularly (Figs. 2A–2C). Teeth mostly with apical flank retroflexed and basal flank concave (Fig. 2D); others with apical flank flexuous and basal flank convex (Fig. 2E). Primary venation pinnate, midvein tapering toward apex. Seven to 10 pairs of major secondary veins parallel to one another (Figs. 2A–2C). Semicraspedodromous secondary veins upwardly curved (Figs. 2A–2C). Sinuous secondary veins entering the teeth along their apical margins (Fig. 2E). Major secondary vein spacing regular and consistent (Figs. 2A–2C). The angle of basal part of the secondary veins to the midvein ∼45°–75° (Figs. 2A–2C). Intersecondary veins present (Fig. 2B, 2C). Tertiary veins mixed percurrent, straight, convex, and sinuous (Figs. 2A–2D). Tertiary veins forming a right or acute (53°–82°) angle with the admedial side of the secondary veins, and a right or obtuse (94°–114°) angle with the exmedial side of the secondary veins (Figs. 2A–2C). Tertiary veins positioned medially of the smaller teeth (Fig. 2G). Quaternaries mixed percurrent, anastomosing with other veins to form irregular reticulate polygons (Fig. 2B). Areolation forming a fine orthogonal network (Fig. 2B).
Infructescence : Infructescence elliptic, 1.1–1.3 cm in length, 1.0–1.1 cm in width; borne singly on one branch. Bracts thick, fan‐shaped; ∼2.9 mm long and ∼1.3 mm wide (Fig. 3). Approximately 18–24 carbonized woody bracts helically arranged along the axis (Figs. 3D–3G). Primary bract thick, elliptic, with acuminate apex, ca. ∼1.0 mm long and ∼0.4 mm wide (Fig. 3B). Secondary bracts thinner than primary bracts, trumpet‐shaped; 1.0–1.3 mm in length and 0.3–0.6 mm in width (Fig. 3B). Peduncles 0.7–1.2 cm long and ∼0.2 cm wide, possessing bud scale scars (Fig. 3D).
4 Discussion
4.1 Morphological comparison
4.1.1 Leaf morphological comparison
Our leaf fossils were assigned to Betulaceae based on gross characteristics, including simple elliptic to ovate blade shape, pinnate venation, acuminate leaf apex, craspedodromous secondary veins, symmetrical bases, and two teeth per secondary vein along the laminar margin (Jones, 1986). Several characteristics of our leaf fossils, such as sinuous secondary veins paralleling one another, consistent space between secondary veins, semicraspedodromous venation (Liu, 1996), and secondary veins entering the teeth along their apical margins (Figs. 2A–2F), are typical leaf characteristics of Alnus (Table 1). Among 26 existing Alnus species, only A. cremastogyne , A. ferdinandi‐coburgii , and A. trabeculosa Hand.‐Mazz. possess semicraspedodromous secondary veins, sinuous secondary veins entering the teeth along their apical margins, and elliptic lamina, which most resemble our leaf fossils (Fig. 4). However, our leaf specimens, possessing decurrent secondary veins, differ from A. cremastogyne which has excurrent ones (Ren et al., 2010; Figs. 4B, 4C). Alnus trabeculosa possesses a rounded laminar base and a medial asymmetrical lamina, which differs from the cuneate laminar base and medial symetrical lamina of our leaf fossils (Ren et al., 2010; Fig. 4D). Moreover, our leaf fossils share many morphological characteristics with A. ferdinandi‐coburgii , such as elliptic lamina, cuneate laminar base, acuminate laminar apex, sinuous secondary veins parallel to one another and upwardly curved, and consistent angle of the secondary vein to the midvein.
| Genus | Leaf shape | Leaf apex shape | Midvein course | Secondary vein course | Position of secondary vein entering tooth | Minor secondary vein course | Freely ending veinlets type |
|---|---|---|---|---|---|---|---|
| Alnus | Narrowly to broadly ovate to obovate | Acuminate | Sinuous | Most sinuous, occasionally straight | Apical to medial | Sinuous or constant | Simple to more than three times branching |
| Betula | Wide ovate to elliptic | Acuminate | Sinuous | Most upcurved; some with symmetrical straight vein in middle or basal part, upcurved in apical part | Medial to basal | Sinuous or zig‐zag | Once to twice branching |
| Carpinus | Oblong to elliptic, ovate | Acuminate | Apically sinuous | All (apart from basal) upcurved before entering teeth | Basal | Sinuous or zig‐zag | None |
| Corylus | Wide oblong | Mucronate | Sinuous | Straight | Medial or basal | Constant, sinuous, or zig‐zag | None or single (very rarely once branching) |
| Ostrya | Ovate to oblong | Acuminate | Apically sinuous | Straight | Medial or basal | Constant | None |
| Ostryopsis | Ovate or elliptic‐broadly ovate or ovate‐orbicular | Obtuse or rounded acuminate or acute | Sinuous | Straight or sinuous | Medial or basal | Constant, sinuous, or zig‐zag | Not observed |
Alnus has been widely reported from the Paleocene and younger deposits. Among reported Alnus leaf fossils that we studied, only A. gaudinii (Heer) Knobloch & Kvaček (Worobiec & Szynkiewicz, 2007), A. heterodonta (Newberry) Meyer & Manchester (Meyer & Manchester, 1997), and A . clarnoensis Liu, Manchester & Jin (Liu et al., 2014) present the semicraspedodromous venation pattern. However, the truncate laminar base of A. heterodonta , the typically decurrent basal margins of A. clarnoensis , and cordate or rounded laminar base of A. gaudinii differ from the cuneate base of our fossils (Meyer & Manchester, 1997; Worobiec & Szynkiewicz, 2007; Liu et al., 2014). In China, Alnus fossils are mainly reported in the form of leaves, with no infructescence fossils identified to the species level (Table 2). Among these leaf fossil records, rounded or cordate base is observed in A. corylina Knowlton & Cockerell (WGCPC, 1978), A. protobarbata Tao (Tao & Xiong, 1986), and A. protomaximowiczii Tanai (WGCPC, 1978), which differ from the cuneate or wide cuneate base of our fossils. Several traits of reported fossil species differ from our fossils, for example, midvein sinuous apically (A. prenepalensis Hu & Chaney), obovate oblong lamina, and sinuous midvein (A. schmalhausenii Grub.), marginal teeth CC‐RT or ST‐ST (following the tooth shape notations of Ellis et al., 2009, fig. 321) (A. protomaximowiczii , A. ellipsophylla Li) (WGCPC, 1978), and single teeth near the laminar apex, double teeth in the lower part (A. luxuriosa Li) (WGCPC, 1978).
| Species | Organ | Age | Locality | Reference |
|---|---|---|---|---|
| Alnus protobarbata | Leaf | Paleocene | Jiayin, Heilongjiang, Wuyun Formation | Tao & Xiong, 1986 |
| A. corylina | Leaf | Middle to late Eocene | Fushun, Liaoning, Guchengzi Formation | WGCPC, 1978; Wang et al., 2010 |
| A. ellipsophylla | Leaf | Middle to late Eocene | Fushun, Liaoning, Guchengzi Formation | WGCPC, 1978; Wang et al., 2010 |
| A. luxuriosa | Leaf | Middle to late Eocene | Fushun, Liaoning, Guchengzi Formation | WGCPC, 1978; Wang et al., 2010 |
| A. schmalhausenii | Leaf | Middle to late Eocene | Fushun, Liaoning, Guchengzi Formation | WGCPC, 1978; Wang et al., 2010 |
| A. protomaximowiczii | Leaf | Early middle Miocene | Shanwang, Shandong, Shanwang Formation | WGCPC, 1978; Liang et al., 2003 |
| Leaf | Late Miocene | Markam, Tibet, Lawula Formation | Tao & Du, 1987 | |
| A. nepalensis | Leaf/infructescence | Late Miocene | Xundian, Yunnan, Xiaolongtan Formation | Xing, 2010 |
| Alnus sp. | Leaf | Middle to late Eocene | Fushun, Liaoning, Guchengzi Formation | WGCPC, 1978; Wang et al., 2010 |
| Infructescence | Middle Miocene | Mengla, Yunnan, Dajie Formation | ||
| Leaf | Miocene | Jianchuan, Yunnan, Shuanghe Formation | WGCPC, 1978; Sun et al., 2011 | |
| Leaf | Late Miocene | Markam, Tibet, Lawula Formation | Tao & Du, 1987 | |
| Infructescence | Late Miocene | Zhaotong, Yunnan, Shuitangba section | Huang et al., 2017 | |
| Infructescence | Late Pliocene | Heqing, Yunnan, Sanying Formation | Huang, 2016 |
Tao & Du (1987) reported A. protomaximowiczii from the Lawula Formation, the same formation from which our fossils were obtained, but it is from different strata based on the floristic components. Alnus protomaximowiczii is similar to our fossils regarding equal spacing between secondary veins (Tao & Du, 1987). However, it differs from our fossils in the round laminar base and CC‐RT teeth type; our fossils have a cuneate or wide cuneate laminar base and RT‐CC or FL‐CV teeth type (following the tooth shape notations of Ellis et al., 2009, fig. 321).
4.1.2 Morphological comparison of infructescences
Infructescence fossils of Alnus were uncovered from the same layer with Alnus leaf fossils in our study. The woody ellipsoidal infructescences of Alnus are easily distinguished from other genera of Betulaceae (Liu et al., 2014). The peduncle characteristics and the size and shape of infructescences are useful identifying characteristics among existing Alnus species (Furlow, 1979). Based on the peduncle characteristics and the size and shape of infructescences, we compared these fossils with specimens representing 25 extant species and one subspecies (Table S1). The long and slender peduncles of A. cremastogyne , A. alnobetula subsp. fruticosa (Rupr.) Raus, A. pendula Matsum., A. glutinosa (L.) Gaertn., and A. trabeculosa differ from the stout peduncle of our fossils (Table S1). The racemose pistillate infructescences of A. nepalensis , A. formosana (Burkill) Makino, A. serrulata (Aiton) Willd., A. incana (L.) Moench, A. hirsuta (Spach) Rupr., and A. rubra Bong. differ from our single pistillate infructescence fossils (Table S1). The asymmetrical infructescences of A. nitida and A. oblongifolia Torr. in W. H. Emory differ from symmetrical infructescences of our fossils. The infructescence shapes of some living species are different from our elliptic infructescence fossils, that is, the oblong infructescences of A. firma Siebold & Zucc., A. subcordata C. A. Mey., and A. japonica (Thunb.) Steud.; the long oblong or ovate infructescences of A. serrulatoides Callier, A. fauriei H. Lév. & Vaniot, A. orientalis Decne., A. maritima (Marshall) Muhl. ex Nutt., A . rhombifolia Nutt., A . acuminata Kunth in F. W. H. von Humboldt, J. A. A. Bonpland & C. S. Kunth, A. matsumurae Callier, and A. jorullensis Kunth in F. W. H. von Humboldt. Alnus ferdinandi‐coburgii and A. cordata (Loisel.) Duby possess stout peduncles that most resemble our fossils (Table S1). The racemose ovate pistillate infructescences and long peduncle of A. cordata differ from single elliptic infructescences and short peduncle of our fossils. In all, our fossils were the most similar to A. ferdinandi‐coburgii in terms of morphology, such as elliptic shape of infructescences, consistently stout peduncles, and possessing a bud scale scar on the peduncle (Figs. 2A–2E).
Most previously figured infructescence fossils of Alnus , such as A. clarnoensis Liu, Manchester & Jin from the middle Eocene, Clarno Formation, Oregon, USA and Alnus sp. (sensu Meyer & Manchester, 1997) from the early Oligocene John Day Formation in Fossil, Oregon, USA, have racemose pistillate infructescence structures (Manchester & Meyer, 1987; Meyer & Manchester, 1997; Liu et al., 2014) that differ from our unbranched, single pistillate infructescence fossils. The scale width of our fossils is only ∼1.3 mm, much narrower than that of A. latibracteosa Mai and A. lusatica Mai from Saxony and Lusatia, Germany (Mai, 1987). Additionally, oblong pistillate infructescences of A. lusatica and Alnus sp. differ from our elliptic fossil infructescences (Mai, 1987; Manchester & McIntosh, 2007).
Judging from the high morphological similarity among leaf and infructescence fossils in Kanjun flora and A. ferdinandi‐coburgii , we named our fossils as A . cf. ferdinandi‐coburgii .
4.2 Biogeographic and paleoenvironmental implications
The oldest reliable fossils of Alnus in China are infructescence fossils and leaf fossils from the middle to late Eocene Fushun flora (Wang et al., 2010; Liu et al., 2014). Alnus cf. ferdinandi‐coburgii suggests that Alnus was widely distributed in China by at least the late Eocene. The occurrence of A . cf. ferdinandi‐coburgii from the southeastern QTP indicates not only the genus had been surviving on the Plateau since the latest Eocene, but that this fossil population was nearly identical in known features of its morphology to the extant species, A. ferdinandi‐coburgii .
We assume that extant A. ferdinandi‐coburgii is the nearest living relative of our fossils based on the morphological similarities, thus the modern distribution of this species could provide insight into the conditions under which the fossil taxon lived. This line of reasoning leads to hypothesize that the climate of the southeastern QTP during the late Eocene was much warmer and wetter than that of today. Alnus ferdinandi‐coburgii is distributed in areas with mean annual temperature values between 9.7 °C and 16.9 °C, and mean annual precipitation values between 896.2 mm and 1161.2 mm (Table S2), whereas the current mean annual temperature and mean annual precipitation of Markam County are 4.4 °C and 516.5 mm, respectively (http://www.worldclim.org). The warmer climatic conditions during the late Eocene are further supported by abundant leaf remains of other plant groups such as Quercus subgenus Cyclobalanopsis (Xu et al., 2016), as well as Elaeagnus tibetensis T. Su & Z. K. Zhou (Su et al., 2014), which could not possibly grow in such high altitude at the fossil site nowadays. All these fossil taxa indicate a much warmer and wetter climate during the late Eocene than now. Generally, our finding agrees with a recent paleoclimate reconstruction of the Jianchuan Basin along the southeastern margin of the QTP, which also suggested a warm climate during the late Eocene (Sorrel et al., 2017).
During the late Eocene the elevation of the southeastern QTP was much lower than it is today. Alnus ferdinandi‐coburgii is now mainly distributed in Sichuan and Yunnan provinces, adjacent to the QTP, but the elevations range from 950 m to 3050 m (Table S3), while the present day elevation of Kajun is 3910 m. Another fossil species, Quercus tibetensis Xu, Su & Zhou, was previously reported from the same layer with A . cf. ferdinandi‐coburgii , and it was not likely present in the fossil site at such high elevation, even under a warmer climate during the late Eocene (Xu et al., 2016). The east–west extension of the QTP might have contributed to the continued uplift of the southeastern QTP (Royden et al., 2008; Gourbet et al., 2017), which shapes the complex topography and high biodiversity in the southeastern margin of the QTP at the present day.
Acknowledgements
We thank colleagues from the Palaeoecology Research Group in Xishuangbanna Tropical Botanical Garden (XTBG) for the fossil collection, and the Public Technology Service Center, XTBG for imaging. This work was supported by the National Natural Science Foundation of China (Grant Nos. 31470325 and 4161101253 to T. Su, and No. U1502231 to Z.‐K. Zhou), Key Research Program of Frontier Sciences, CAS (No. QYZDB‐SSW‐SMC016 to T. Su), the Foundation of the State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences) (Grant No. 143107 to T. Su, and No. 173128 to H. Xu), a grant from the Natural Environment Research Council (No. NE/P013805/1 to T. Su), and Youth Innovation Promotion Association, CAS (No. 2017439 to T. Su). We thank Professor Steven R. Manchester for many constructive suggestions.
