Occurrence of Christella (Thelypteridaceae) in Southwest China and its indications of the paleoenvironment of the Qinghai–Tibetan Plateau and adjacent areas
Abstract
The uplift of the Qinghai–Tibetan Plateau dramatically changed the regional topography and climate, profoundly impacting the distribution of many plant lineages. Plant responses to environmental changes are particularly prominent in lineages that require ecological factors differentiated from those present before the uplift of the QTP. Two fossil occurrences of Christella H. Lév., Fl. Kouy–Tchéou (Thelypteridaceae), a fern genus now distributed mainly at low elevations of the pantropics with warm and moist habitats, are described based on fossilized Cenozoic leaf fronds recovered from SW China: late Paleocene Christella nervosa (J. R. Tao) C. L. Xu, T. Su & Z. K. Zhou comb. nov. found in Liuqu, southern Tibet and middle Miocene Christella sp. recovered from the Jinggu Basin in western Yunnan. The frond fossils from both sites share key morphological characteristics that diagnose these fossils as Christella . After detailed comparisons, we further clarified Christella papilio (C. Hope) Holttum, a species distributed in warm, humid habitats at altitudes no more than 1300 m, as the nearest living relative of C. nervosa . This finding suggested that southern Tibet had not reached its present elevation during the late Paleocene (ca. 56 Ma). We propose that the uplift, accompanied by severe cooling and aridification after the late Paleocene, caused the disappearance of Christella in southern Tibet, whereas paleoenvironmental conditions enabled the genus to survive in Yunnan. Our study provides the first example of distributional constraints of ferns in SW China in response to paleoenvironmental changes in the Qinghai–Tibetan Plateau and nearby areas.
1 Introduction
As the largest and highest plateau in the world, the Qinghai–Tibetan Plateau (QTP) experienced dramatic environmental changes in the geological past (An et al., 2001; Wang et al., 2008; Spicer, 2017), which has shaped the climate in nearby regions, such as the monsoonal climate in SW China that is characterized by the seasonality of precipitation (Jacques et al., 2011; Xing et al., 2012; Su et al., 2013; Zhou et al., 2018). These topographic and climatic changes influenced the evolution and distribution of plants, either promoting diversification or extinction (Huang et al., 2016b). For example, in association with change in paleoelevation and paleoclimate, Quercus tibetensis H. Xu, T. Su et Z.K. Zhou sp. nov. disappeared from eastern Tibet (Xu et al., 2016), and Quercus sect. Heterobalanus diversified with the occurrence of the uplift of the Himalayas and the southeastern margin of the QTP (Meng et al., 2017). However, the evolutionary patterns of non‐seed plants, such as ferns, in the QTP and nearby areas are still largely unresolved. Many ferns require wet conditions, and are regarded as good indicators of moisture related to environmental changes (Hoffmann, 1998; Thuiller et al., 2008; Kolk et al., 2017); therefore, it is of great interest to investigate the past spatial distribution of ferns and their paleoenvironmental implications using fossil records.
Ferns are the second largest group of vascular plants with ∼10 000 extant species (Pteridophyte Phylogeny Group (PPG I), 2016). Thelypteridaceae includes two subfamilies, 30 genera, and approximately 1034 species (PPG I, 2016) and is widely distributed across subtropical and tropical regions worldwide. Among Thelypteridaceae members, 18 genera and 365 species are naturally distributed in China (Lin et al., 2013). However, the generic classification of Thelypteridaceae is still being updated by phylogenetic studies because of the high diversity within this family (Holttum, 1971; Pichi Sermolli, 1977; Ching, 1978; Smith, 1990; Smith et al., 2006; He & Zhang, 2012; Christenhusz & Chase, 2014; Almeida et al., 2016). Christella H. Lév., Fl. Kouy–Tchéou is a genus within Thelypteridaceae that has proven complicated in delimiting generic boundaries. Christella was initially defined by Holttum (1976), and it has been revised by the use of molecular evidence from different authors (He & Zhang, 2012; Almeida et al., 2016; PPG I, 2016). Herein, we follow the latest classification system proposed by PPG I (2016), which provides a comprehensive classification for lycophytes and ferns. Christella comprises approximately 70 species and is characterized by anastomosing goniopteroid venation and unicellular elongate glandular hairs on the stalks of sporangia (Holttum, 1976). Christella grows in wet, dense or semi‐open forests at relatively low elevations, mainly in tropical and subtropical regions (Fig. 1A; Holttum, 1976; Mabberley, 1997; Lin et al., 2013).
The southeastern margins of the QTP and adjacent areas are rich in extant fern species (Fig. 1A). Some Cenozoic fern fossils have been reported from this region, such as Drynaria callispora Su, Zhou et Liu sp. nov. (Su et al., 2011), Drynaria lanpingensis sp. nov. Huang, Su et Zhou (Huang et al., 2016a), Cyclosorus scutum Naugolnykh, Wang, Han et Jin sp. nov. (Naugolnykh et al., 2016), Neolepisorus chingii sp. nov. (Xie et al., 2016), and Goniophlebium macrosorum Xu et Zhou n. sp. (Xu et al., 2017); however, compared with the abundant extant fern species, fossil records of many fern groups, including those of Christella (Thelypteridaceae), are still far from fully investigated, which limits the current understanding of regional fern biodiversity.
The aims of the present study are to: (i) describe well‐preserved Christella fossils from two localities and confirm their systematic assignment; (ii) provide fern fossil evidence to support previous studies indicating that southern Tibet had not reached its present elevation during the late Paleocene (ca. 56 Ma) based on climate ranges of distribution areas of the nearest living relative; and (iii) present important evidence for the spatial distributional patterns of ferns in response to dramatic paleoenvironmental changes in the QTP.
2 Materials and Methods
2.1 Fossil site from Lhaze, southern Tibet
The fossil specimens were collected from thick conglomerates in Liuqu, Lhaze County, southern Tibet, China (29°09′N, 88°06′E, 4160 m a.s.l.; Fig. 1B). These fossiliferous sediments belong to the Liuqu Formation, which is unconformably embedded between ophiolite from Indus–Yarlung to the north and sedimentary rocks from the Tethyan Himalayan sequences to the south, that represents the boundary between the Indian subcontinent and Asian continent (Yin et al., 2006). This site is mainly composed of mottled and reddish sandy conglomerates, as well as reddish sandstones mixed with gray‐green and silty mudstones (Li et al., 2015a). Fossils in this study are preserved in the layer of light gray siltstones from the upper part of the Liuqu Formation. This deposition indicates a transitional alluvial fan or braided river environment (Davis et al., 2002). The previous megafossil information and recent U–Pb dating of zircons constrained the age of the Liuqu Formation to 56 Ma (dating to the late Paleocene) (Fang et al., 2006; Ding et al., 2017). From these fossil‐bearing layers of the formation, leaves, including those of Cyclosorus nervosus J. R. Tao, were previously described, indicating the presence of a subtropical or tropical forest (Tao, 1988; Fang et al., 2006).
2.2 Fossil from Jinggu County, SW Yunnan
A fossil specimen was collected from the Sanhaogou Formation, Jinggu County, western Yunnan, China (23°29′N, 100°41′E, 974 m a.s.l.; Fig. 1B). The Jinggu Basin is in the northern part of the Indochina block, adjacent to the southeast margin of the QTP, which includes a sequence of sediments deposited continuously from the Jurassic to Quaternary (Li et al., 2017b). Our fossil is from the upper part of the Sanhaogou Formation in the Jinggu Basin, which is considered to correspond to the middle Miocene, which could be slightly older than the middle–late Miocene Xiaolongtan flora (He et al., 1996; Li et al., 2015b; Li et al., 2017b). The Sanhaogou Formation is unconformably located above the Oligocene Mengla Group and is covered by Quaternary sand and conglomerates. It consists of red‐grayish to black mudstones, gray and yellow sandstones, and siltstones (He et al., 1996; Wang, 1996). The fossil in this study is preserved in the layer of yellow siltstones from the upper part of the formation. Additionally, some ostracodes, gastropods, and fish fossils as well as abundant plant fossils have been found from the Sanhaogou Formation in Jinggu (Wang, 1996; Li et al., 2017b).
2.3 Morphological observation
We observed and photographed the fossil fronds using a Nikon D700 camera (Nikon, Tokyo, Japan). We pictured morphological characters in detail using a Leica S8APO stereomicroscope (Leica, Wetzlar, Germany) coupled with a Smart Digital Microscope (Smart Zoom 5; Zeiss, Oberkochen, Germany). We measured the morphological characters using a vernier caliper and captured the using ImageJ software (version 1.44p; National Institutes of Health, Bethesda, Maryland, USA). No cuticle tissue or in situ spores from these fossil specimens were observed for further morphological study.
We checked specimens of extant ferns at the Herbarium of the Xishuangbanna Tropical Botanical Garden (HITBC) and two databases: Global Plants on JSTOR (http://plants.jstor.org/) and the Chinese Virtual Herbarium (CVH; http://www.cvh.org.cn/). We obtained spatial distribution data of all extant species of Cyclosorus from the Chinese Virtual Herbarium (www.cvh.org.cn) and the Global Biodiversity Information Facility (www.gbif.org).
3 Systematics
3.1 Fossils from the Liuqu Formation
Order Polypodiales Link
Family Thelypteridaceae Ching ex Pic. Serm
Genus Christella H. Lév., Fl. Kouy–Tchéou
Species Christella nervosa (J. R. Tao) C. L. Xu, T. Su & Z. K. Zhou comb. nov.
1988 Cyclosorus nervosus J. R. Tao, p. 228; pl. I: 1∼2
Specimens KUNPC‐XZLZLX3‐0001 (Figs. 2A, 2C), KUNPC‐XZLZLX3‐0002 (Figs. 2B, 2D), KUNPC‐XZLZLX3‐0003 (Fig. 2E), KUNPC‐XZLZLX3‐0004, KUNPC‐XZLZLX3‐0005, KUNPC‐XZLZLX3‐0006, KUNPC‐XZLZLX3‐0007.
Repository Herbarium of Kunming Institute of Botany (KUN), Chinese Academy of Sciences.
Nomenclatural notes We follow the latest classification of ferns proposed by PGG I (2016); many species in Cyclosorus have been assigned to Christella according to this classification. Morphological characters of fossils in this study fall within these in Christella as discussed below.
Description The partly preserved sterile frond is 1‐pinnate‐pinnatifid, catadromous (Figs. 2A, 2C). No less than three pairs of pinnae were preserved along the costa. Pinnae are lanceolate, 8.0–15.0 cm long and ∼2.0 cm wide, comprising at least 20 pairs of alternate segments (Figs. 2A, 2C). Segments are ovoid, oblong to lanceolate with attenuate or obtuse apices, and entire margin (Figs. 2 and 3); they are 1/2 or less than 1/2 pinnatifid. The midveins of each segment are relatively thick and extend to the apex. The angles between the costa and pinnae are 60–90°. The pattern of segment venation is goniopterid, namely, the lateral veins of the segments are not forked; the upper 4–7 pairs of lateral veins are curved toward the segment apex; the lower 6–8 pairs of lateral veins connect with each other (Figs. 2E, 3B). One pair of the basal veinlets from two neighboring segments together with the midvein of the pinna are connected and form triangular areolae (Fig. 2E). Occasionally, pinnatifid connecting veins extend into the triangular areola (Fig. 2E).
Two rows of ovoid sori are located in the middle of the lateral veins along two sides of the midvein of the segment, with approximately nine sori on each side (Figs. 2F, 3B). In situ spores were not preserved in these specimens.
3.2 Fossil from the Sanhaogou Formation
Order Polypodiales Link
Family Thelypteridaceae Ching ex Pic. Serm
Genus Christella H. Lév., Fl. Kouy–Tchéou
Species Christella sp.
Specimen KUNPC‐JGSHG‐0001 (Fig. 4A)
Repository Herbarium of Kunming Institute of Botany (KUN), Chinese Academy of Sciences.
Description One well‐preserved sterile pinna was recovered (Fig. 4). The pinna is lanceolate, 4.5–5.0 cm long and 1.5–2.0 cm wide, comprising at least 16 pairs of alternate segments (Fig. 4A). Segments are ovoid, oblong with acuminate or obtuse apices, and entire margin (Fig. 4B); they are 1/2 or less than 1/2 pinnatifid. There are at least six pairs of lateral veins arranged along the midveins of each segment. The pattern of segment venation is goniopterid; namely, the lateral veins of the segments are not forked. The upper 2–6 pairs of lateral veins meet at the midvein, forming square areolae (Fig. 4B); the first pair of lateral veins connect to each other forming triangular areola, occasionally forming pentagonal areolae (Figs. 4A, 4C).
4 Discussion
4.1 Assignment of fossils to Christella
Fossils from both sites in this study are 1‐pinnate‐pinnatifid with lanceolate pinnae, shallowly lobed and ovoid segments with attenuate or obtuse apexes and an entire margin. The pattern of segment venation is goniopterid and anastomosing. Specifically, the veinlets are simple and straight, and the first pair of lateral veins connect to each other forming triangular areola, or occasionally pentagonal areola (Figs. 3B, 4A). These characters are typical within Thelypteridaceae (Ching, 1978). There are two subfamilies within the family Thelypteridaceae: Phegopteridoideae Salino, A.R.Sm. & T.E.Almeida, including Macrothelypteris (H. Ito) Ching, Acta Phytotax. Sin., Phegopteris (C. Presl) Fée, Mém. Foug. and Pseudophegopteris Ching, Acta Phytotax. Sin.; Thelypteridoideae C.F.Reed, Phytologia (e.g., Christella H. Lév., Fl. Kouy–Tchéou, Cyclogramma Tagawa, Acta Phytotax. Geobot., Cyclosorus Link, Hort. Berol., Oreopteris Holub, Folia Geobot. Phytotax., Stegnogramma Blume, Enum. Pl. Javae, and Thelypteris Schmidel, Icon., which are most similar with our fossils). First, our fossils differ from species in the subfamily Phegopteridoideae. Free venation not reaching segment margins occurs consistently throughout Phegopteridoideae. This character was considered to be the ancestral trait in Thelypteridaceae (He & Zhang, 2012). Among Thelypteridoideae, most species traditionally treated as Cyclosorus by Zhang (2012) have been assigned to Christella in PPG I (2016). There are only two species left in Cyclosorus , that is, Cyclosorus gongylodes Schkuhr and Cyclosorus interruptus (Willd.) H. Ito, which have meniscioid venation (simple, free veins reaching the segment margin). In addition, Cy. interruptus presents deeply lobed pinnae, in contrast with our fossils. Cyclogramma has >1/2 deeply lobed segments and truncated segment apices, which obviously differ between our fossils and Cyclogramma . Free venation meeting segment margins appears in Oreopteris and Thelypteris . In Stenogramma , line‐shaped sori completely differ from characteristics of fossils uncovered from Tibet, which had irregular, square areolae also dissimilar to the fossil from Jinggu (He & Zhang, 2012; Lin et al., 2013); therefore, our fossils resemble Christella .
We further compared our fossils with Christella and several other genera including Pronephrium C. Presl, Epimel. Bot., Pseudocyclosorus Ching, Acta Phytotax. Sin., and Sphaerostephanos J. Sm., Gen. Fil. (Hooker). Christella has been revealed to be polyphyletic (He & Zhang, 2012). Species in Christella with anastomosing venation have a well‐supported and close relationship with species distinguished by goniopteroid venation, such as that which appears on our fossils. Pronephrium was found to be polyphyletic, eight species were nested in four clades (Almeida et al., 2016). Our fossils differ from Pronephrium , for example, crenate lobed pinnae, meniscioid venation, and more than one line of sori characterize Pronephrium (He & Zhang, 2012). Pseudocyclosorus has free veins or veins running to sinuses, with deeply lobed pinnae (Almeida et al., 2016). Sphaerostephanos is regarded as the most species‐rich genus of Thelypteridaceae in the Paleotropics. Some distinctive characters differentiate Sphaerostephanos from our fossils, for example, elongate sori, and upper pinnae commonly reduced to 1.0–2.0 cm in length (Holttum, 1979). According to the detailed morphological comparison above, we place our fossil specimens to Christella by the venation type, intensity of lobed segments, and in situ sori patterns (Holttum, 1976; He & Zhang, 2012; Almeida et al., 2016; PPG I, 2016).
4.2 Morphological comparison with extant Christella
The Christelloid clade proposed by Almeida et al. (2016) comprises the core Christella sect. Christella (syn. =Cyclosorus subg. Cyclosorus ) (PPG I, 2016). We chose 14 living species in Christella sect. Christella for further morphological comparison with our fossils. Among all these living species, our fossil specimens share two important morphological characters, namely the shape of the pinna and pattern of the sori. For the fossils from Tibet, the pinna shape is lanceolate, with a truncate base, obtuse to acuminate apex (SP1; Table 1), and the shape of the sori is orbicular or round, located in the middle of the veins/medial (SO1; Table 1). These two characters appear only in five living species, Christella chingii (=Cyclosorus chingii Z. Y. Liu ex Ching et Z. Y. Liu), Christella ciliata (=Cyclosorus ciliatus (Benth.) Ching), Christella heterocarpa (=Cyclosorus heterocarpus (Blume) Ching), Christella hirtisora (=Cyclosorus hirtisorus (C. Chr.) Ching) and Christella papilio (C. Hope) Holttum (=Cyclosorus papilio (C. Hope) Ching).
| Species | Shape of pinna | Length of pinna (cm) | Width of pinna (cm) | Number of segments (pairs) | Shape of segment | Apex of segment | Segment pinnatified | Pattern of sori |
|---|---|---|---|---|---|---|---|---|
| Christella nervosa (J. R. Tao) C. L. Xu, T. Su & Z. K. Zhou comb. nov. | SP1 | 8.0–15.0 | ∼2.0 | ∼20 | Ovoid or oblong | Obtuse | ≤1/3 | SO1 |
| Christella sp. | SP1 | 4.5–5.0 | 1.2–1.5 | ∼16 | Ovoid or oblong | Acuminate | ≤1/2 | Not observed |
| C. acuminata | SP1 | 7.0–11.0 | 0.8–1.2 | 18–24 | Lanceolate or falcate | Cuspidate | 1/2–2/3 | SO2 |
| C. arida | SP1 | ∼10.0 | ∼1.5 | 25–30 | Triangular | Acute | 1/3 | SO2 |
| C. chingii | SP1 | 11.0∼17.0 | 2.5∼3.0 | ∼20 | Ovoid or oblong | Obtuse | 1/4–1/3 | SO1 |
| C. ciliata | SP1 | ∼5.0 | ∼1.0 | ∼13 | Lanceolate or falcate | Truncate | 1/2 | SO1 |
| C. crinipes | SP2 | 12.0–25.0 | 1.4–2.0 | 30–35 | Lanceolate | Obtuse | 1/2–2/3 | SO1 |
| C. dentata | SP1 | 6.0–8.0 | ∼1.5 | 13–15 | Near trapeziform | Obtuse | 1/2 | SO3 |
| C. heterocarpa | SP1 | 10.0–16.0 | 1.0–1.5 | 20–30 | Oblong | Obtuse | 2/3 | SO1 |
| C. hirtisora | SP1 | 13.0–23.0 | 1.2–1.7 | ∼45 | Oblong | Triangular orobtuse | 1/3 | SO1 |
| C. latipinna | SP1 | 3.0–5.0 | ∼1.0 | 15–18 | Lanceolate | Acute | 2/3 | SO2 |
| C. papilio | SP1 | 10.0–18.0 | 1.5–2.0 | 20–25 | Oblong | Obtuse | 2/5–1/2 | SO1 |
| C. parasitica | SP1 | 5.0–20.0 | 0.5–1.5 | 20–25 | Ovoid–oblong | Obtuse | 1/2–2/3 | SO2 |
| C. subelata | SP3 | 10.0–20.0 | 2.0–3.5 | 20–35 | Oblong | Obtuse | 1/4–1/3 | SO1 |
| C. terminans | SP3 | 15.0–25.0 | 1.0–1.8 | 20–35 | Triangular | Subacute or obtuse | 1/3–1/2 | SO2 |
| C. truncata | SP3 | 12.0–30.0 | 1.0–2.5 | 25–40 | Rectangular | Rounded–truncate | 1/4–1/2 | SO1 |
- The detailed morphology of extant species in Christella follows the Flora of China (Lin et al., 2013) and herbarium specimens.
- SO1, orbicular or round sori, located in the middle part of veins/medial; SO2, orbicular or round sori, located in the marginal part of veins/submarginal; SO3, small sori, located in the marginal part of veins/submarginal; SP1, lanceolate, truncate base, obtuse to acuminate apex; SP2, linear to narrow lanceolate, cuneate to truncate base, acuminate apex; SP3, linear to lanceolate, rounded to truncate base, long acuminate apex.
Fossils collected from Tibet show other distinguishing characters such as middle pinnae that are 8.0–15.0 × ∼2.0 cm long; lobed ≤1/3 pinnatifid toward the costa; and ∼20 pairs of segments on the middle pinnae, which are ovoid or oblong, obtuse at the apex, with simple and straight mid‐veins, and anastomosing venation. Christella chingii has forked top mid‐veins of segments, and mid‐veins of segments in fossils are simple and straight to segment apex. Christella ciliata has 1/2 lobed, lanceolate or falcate segments and truncate apices, but our fossils have oblong segments with obtuse apices. Christella heterocarpa is deeply lobed, which is a diagnostic character for fossils in the present study. Christella hirtisora is different from our fossils in morphology; for example, C. hirtisora has ∼45 pairs of segments, triangular apices of segment, and forked top mid‐vein of segments. Thus, when considering diagnostic characters such as shapes of pinnae and segments, and venation pattern, we consider C. papilio as the nearest living relative to the fossils collected from Tibet (Figs. 2 and 3; Table 1).
Tao (1988) first reported Cy. nervosus with sterile fronds from the Liuqu Formation in Tibet. Herein, new fossil materials with fertile fronds in the present study are well‐preserved, which fits quite well with Cy. nervosus from the gross morphology. Therefore, we identified our fossils from Tibet as the same fossil species and updated these fossils to Christella according to the latest classification system (PGG I, 2016), we combine and name them as Christella nervosa (J. R. Tao) C. L. Xu, T. Su & Z. K. Zhou comb. nov.
The fossil pinna found from the Sanhaogou Formation shows typical characters as mentioned above (Fig. 4; Table 1), but it lacks some characters for further comparison, such as the pattern of in situ sori and the pattern of complete pinnae; therefore, we temporarily assign this specimen to Christella sp.
4.3 Fossil records of Thelypteridaceae
Among the Thelypteridaceae fossil records, some fossils have a relatively close relationship to Christella when considering the typical morphological characters in this genus, such as the simple, straight lateral veins and the lowest one or two pairs of adjacent veins connecting and forming areolae (Collinson, 2002). Stockey et al. (2006) described Speirseopteris orbiculata gen. et sp. nov. (Thelypteridaceae) fossils from the Paleocene of Paskapoo Formation in Canada. Deeply lobed, forked lateral veins were observed in these fossils, which are different from our fossils. An Eocene macrofossil with in situ sori, Abacopteris stiriacum , was reported from Germany and was later assigned to Cyclosorus stiriacus (UNGER) CHING & TAKHT (Collinson, 2001). Cyclosorus stiriacus has similar characters to fossils in this study, such as ovoid segments with an obtuse apex, entire margin and goniopterid pattern of segment venation, as well as the pattern of sori. However, the pattern of the connection of the lateral veins is the main difference: in Cy. stiriacus , only one lateral vein from the upper segment connects to all lateral veins from the lower segment, but the fossils we uncovered from both sites had six to eight pairs of lateral veins connecting to each other from every two adjacent segments. Naugolnykh et al. (2016) reported a fossil species, Cyclosorus scutum Naugolnykh, Wang, Han et Jin sp. nov., from the Eocene of the Changchang Formation on Hainan Island, South China. Although Cy. scutum shares the goniopterid pattern of segmented venation with our fossils, the costa has a relatively deep groove on Cy. scutum that was not observed in our fossils. In addition, Cy. scutum had 3/4 pinnatifid fronds, but the fossils in the present study had no more than 1/2 pinnatifid fronds. Pole (1992) described Cyclosorus tertiario‐zeelandicus Oliver from the early Miocene of New Zealand. The forked top of the mid‐vein on Cy. tertiario differ from Christella fossils in the present study. Sanín et al. (2016) described fern fossil specimens of Thelypteris from the late Miocene of Colombia, which meet the features with more than one line of parallel veins and areolae. Recently, Mehrotra et al. (2011) reported Cyclosorus eoproliferus (Prasad) Prasad, Ghosh & Tripathi from the middle–late Miocene of Siwalik; Cy. eoproliferus has slightly lobed and nearly entire margins of pinnae and relatively narrow segments with thick mid‐vein. Robledo et al. (2015) found the first fern fossil record of Thelypteridaceae in the neotropics, which was clarified as Thelypteris interrupta (Willd.) Iwatsuki from the late Miocene of Argentina. Thelypteris interrupta has more than 1/2 lobed segments, forked tops of mid‐veins, and costa with relatively deep grooves, which have different features to fossils in the present study.
In view of the recent phylogeny of Thelypteridaceae, Christella has the later divergent trait in Thelypteridaceae according to the anastomosing venation type (He & Zhang, 2012; Almeida et al., 2016). Together with previous fossil records and comparison with C. nervosa , we propose that Christella has a long evolutionary history and diverged no later than the late Paleocene (ca. 56 Ma). Moreover, abundant fossil records of Thelypteridaceae during the Miocene might be owing to the diversification of this family under relatively humid and warm periods at that time (Collinson, 2002).
4.4 Paleoenvironmental implications
Modern species in Christella are mainly distributed in dense forests or semi‐open forests with high humidity in tropical and subtropical regions at low elevations worldwide (Figs. 1 and 5). Thus, the fossils that we uncovered from Yunnan and Tibet might indicate humid and warm climates judging by the present distribution of this genus. In the Liuqu Formation, numerous big leaf fossils have been found, such as Mallotus L., Ficus L., Livistona R. Br., and Magnolia L. (Tao, 1988; Fang et al., 2006). These fossil vegetation types suggest that southern Tibet had tropical or subtropical forests with a warm, humid climate in the late Paleogene (ca. 56 Ma) (Tao, 1988; Fang et al., 2006). Based on morphological similarities, the nearest living relative of C. nervosa is C. papilio , which currently grows in wet areas in forests ranging from 600 to 1300 m in elevations (Lin et al., 2013). This is consistent with the interpretation that southern Tibet had not reached its present elevation during the late Paleocene (Ding et al., 2017). As the flora reported in the Sanhaogou Formation is concerned, some taxa are dominant, such as Fabaceae Lindl. (1836), nom. cons., Fagaceae Dumort. (1829), nom. cons., and Lauraceae Juss. (1789), nom. cons., which also indicates a relatively warm, humid climate during the middle Miocene in the Jinggu Basin (He et al., 1996). Moreover, the paleoecological implication stemming from our fossil records is consistent with paleoclimatic conditions of previous Thelypteridaceae fossil records, indicating a moist, lower latitude environment (Collinson, 2002; Joshi & Mehrotra, 2003; Mehrotra et al., 2011; Sanín et al., 2016). For example, the finding of Cy. eoproliferus , uncovered from the middle–late Miocene of Siwalik, accompanying the comparable modern specimens, indicates the presence of rain forests in the deposition region (Mehrotra et al., 2011).
Fern fossils presented in this paper further support previous studies that the QTP and areas nearby experienced dramatic environmental changes during the Cenozoic (Jacques et al., 2011; Xing et al., 2012; Su et al., 2013, 2018; Ding et al., 2017). Our findings provide additional information regarding the distributional contraction of ferns in response to environmental changes. The collision between India and Asia contributed to the evolution of the QTP and formation of the Himalayas; the collision also led to the southward extrusion of the southeastern margin of the plateau, where the Jinggu Basin is located (Li et al., 2017a, 2017b). Dramatic tectonic activities resulted in significant geographical changes in this region, and influenced the evolution of climate (An et al., 2001; Jacques et al., 2011; Xing et al., 2012; Su et al., 2013; Li et al., 2015b). For example, the altitude of the Liuqu Formation increased from ∼1000 m in the late Paleocene (Ding et al., 2017) to more than 4000 m today, and in response, the climate has become much colder and drier. However, the Jinggu Basin has had a relatively stable environment (currently 974 m a.s.l.). Ultimately, the Christella fossils described in this study provide new evidence for the paleoenvironmental conditions in the QTP and adjacent areas (i.e., southern Yunnan). As species distributions are largely restricted by environmental conditions, more fossil evidence is needed to decipher environmental conditions, such as paleoclimate and paleoelevation, in the geological past.
Overall, we have presented a description and classification of C. papilio as the nearest living relative of fossils from Tibet and reported Christella sp. in the middle Miocene from the Jinggu Basin. Taking the discovery of these two fern fossils into account, the origin and evolution of Christella in SW China could be dated back to 56 Ma. In addition, the presented fossils indicate that during the late Paleocene and middle Miocene, southern Tibet and the Jinggu Basin had warm, humid climates with low elevations. The spatial distribution of Christella has largely been shaped by paleoenvironmental changes.
Acknowledgements
We thank members of the Paleoecology Research Group at Xishuangbanna Tropical Botanical Garden for fossil collection, Public Technology Service Center, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences (CAS) for fossil photography, and Professor Xian‐Chun Zhang, Professor Jian‐Hua Jin, and Professor Harald Schneider for help with classification and suggestions. Many thanks go to Zhuo Zhou for revision in Latin names of new fossil species. This work was supported by the National Natural Science Foundation of China (41661134049, U1502231, 31470325), the Strategic Priority Research Program of CAS (XDA20070301), Key Research Program of Frontier Sciences, CAS (QYZDB–SSW–SMC016), a grant from the Natural Environment Research Council (NE/P013805/1), and the Youth Innovation Promotion Association, CAS (2017439).
