Introduction

Among extant land plants, ferns are a large and diverse group, second only to angiosperms in species number (Tryon and Tryon 1982; Gifford and Foster 1989; Rothwell 1999). In the geological past, ferns have undergone several major radiation events (Rothwell 1987). The Palaeozoic radiation created several families that became extinct at the end of the Permian, though some primitive groups of modern ferns including Marattiaceae, Osmundaceae, and Gleicheniaceae survived through the Palaeozoic and up to the present (Tidwell and Ash 1994; Pryer and Smith 1995). Then, the Mesozoic diversification is proposed to have initiated the evolution of series of modern filicalean families (Phipps et al. 2000). Variation in these long-lived families provides valuable information as to which characters are the most plastic and how each evolved (Phipps et al. 2000).

Compared to morphologically preserved leaves, structurally preserved fern remains not only provide more anatomical details, but also contribute to understanding the evolution and phylogeny of various fern taxa. Though reproductive characters have traditionally been heavily used in fern classification (Bower 1926; Smith 1995; Collinson 1996), anatomical characters of filicalean ferns are also correlated with relationships inferred from cladistic analyses of morphological and molecular data (Serbet and Rothwell 2003). These characters strongly support the hypothesis that internal anatomy is a valuable tool for identifying systematic relationships of fossil ferns (Hasebe et al. 1995; Pryer and Smith 1995; Smith 1995; Rothwell 1999) and provide a vehicle for assessing minimum dates for the origin of leptosporangiate fern clades (Serbet and Rothwell 2003).

Numerous Mesozoic fossil records have been documented worldwide referring to permineralized fern remains of Osmundaceae, Gleicheniaceae, Dennstaedtiaceae, Cyatheaceae, Matoniaceae, and Loxsomacae (e.g., Skog 1976; Sharma and Bohra 1976, 1977; Bohra and Sharma 1979; Nishida and Nishida 1982; Millay and Taylor 1990; Tidwell 1986, 1994; Tidwell and Parker 1987; Tidwell and Ash 1994; Gandolfo et al. 1997; Herendeen and Skog 1998; Phipps et al. 1998, 2000; Tidwell and Skog 1999; Serbet and Rothwell 2003; Cheng and Yang 2017). Mesozoic ferns are well documented in both the northern and southern phytoprovinces of China with diverse and abundant fossil records (Sun et al. 1995a, b; Zhou 1995; Deng and Shang 2000; Wang et al. 2009; Sun et al. 2010; Zhou et al. 2016; Tian et al. 2016). However, almost all these fossil records are represented by leaf impressions/compressions, whereas structurally preserved fern remains are quite scarce in China. Though some permineralized fern rhizomes have been described from the Jurassic of western Liaoning and northern Hebei Provinces, they are all referred to Osmundaceae (Wang 1983; Zhang and Zheng 1991; Matsumoto et al. 2006; Cheng and Li 2007; Cheng et al. 2007; Cheng 2011; Tian et al. 2008, 2013, 2014a, b). Additionally, fern stems referable to Cyatheaceae were recently described from the Upper Cretaceous in the Keshan County of Heilongjiang Province (Cheng and Yang 2017). Other fern lineages have never been reported with structurally preserved fossils from the Mesozoic deposits in China, so far.

In this paper, we described well-preserved fern remains represented by permineralized rhizomes and rachides from the Upper Jurassic Manketouebo Formation in Inner Mongolia, NE China. These fern fossils are assigned to fern families Osmundaceae and Gleicheniaceae. This finding represents the first record of the Jurassic permineralized gleicheniaceous ferns with anatomical details in China, as well as in the Northern Hemisphere.

Material and methods

The fossil fern specimens were collected from the Upper Jurassic Manketouebo Formation on a small hill named Xiehesierde, northeast of the Baiyinbaoligao Village of Daiqintala Town, Horqin Right Wing Middle Banner, Inner Mongolia, NE China (45° 11′ 50″ N, 121° 35′ 10″ E) (Fig. 1). The Manketouebo Formation, represented by a suite of felsic lavas, tuffs, ignimbrites, and volcanoclastic rocks, is widely distributed across the Great Xing’an Range, NE China (Zhang et al. 2010). In the present fossil locality, the Manketouebo Formation unconformably overlies the Lower Permian Shoushangou Formation and comprises tuffaceous sandstone, pebbly sandstone, and crystal tuff (Fu et al. 2012). The outcropped sequence of the Manketouebo Formation is over 150 m in thickness and was divided into five lithological units (Fu et al. 2012) (Fig. 2). The fossil fern remains described here occur in the light gray-green tuff matrix of the Member 5. Besides fern remains, diverse permineralized coniferous wood and cones have also been reported from the same layer in the same locality (Fu et al. 2012; Zheng et al. 2013).

Fig. 1
figure 1

Location map for the sources of the fossils. a Map showing the locality of the Horqin Right Wing Middle Banner (HRWMB) in Inner Mongolia, Northeast China. b Sketch map of fossil locality for permineralized fern remains in Daiqintala Town of HRWMB, Inner Mongolia

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Fig. 2
figure 2

Stratigraphic column of the Upper Jurassic Manketouebo Formation in Baiyinbaoligao Village of the Horqin Right Wing Middle Banner in Inner Mongolia, Northeast China (draw based on lithologic descriptions of Fu et al. 2012)

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The petrified fern remains were cut transversely into several thin sections. These sections were prepared by standard methods, including cutting, grinding, and polishing preparations (Hass and Rowe 1999). These sections were then mounted on slides for microscopic examinations. Photographs were taken with OLYMPUS BX51 and YONGXIN BM2000 microscopes. All specimens and slides described in this paper are housed in Shenyang Institute of Geology and Mineral Resources, Shenyang, China with registration numbers BY-01(A-B) and BY-031(A-C).

Systematic palaeontology

Order Filicales

Family Osmundaceae Berchtold et Presl, 1820

Subfamily Osmundoideae Miller, 1971

Genus Ashicaulis Tidwell, 1994

Species Ashicaulis liaoningensis (Zhang et Zheng) Tidwell, 1994

(Fig. 3)

figure 3

Specimen: BY-01 with two slides BY-01-(A-B)

Fossil locality: Baiyingbaoligao Village of Daiqintala Town, Horqin Right Wing Middle Banner, Inner Mongolia, NE China

Formation and age: Manketouebo Formation, Late Jurassic

Repository: The specimen and prepared slides are deposited in the Shenyang Institute of Geology and Mineral Resources, Shenyang, China

Description: This fossil specimen is represented by a petrified rhizome, composed of a stem and a mantle of adhering petiole bases and adventitious roots. Tissue preservation of the present fossil rhizome is generally fair, although some thin-walled cells (e.g., in the pith) are degraded, and sub-cellular details evident in some other fossil Osmundaceae (e.g., Osmundastrum pulchellum: Bomfleur et al. 2014, 2015) are not preserved. The stem is about 8.0 mm in diameter and consists of a pith, a xylem cylinder, and a two-layered cortex (Fig. 3a, b). The pith, 1.4–1.5 mm across, is heterogeneous and composed of isodiametric parenchymatous cells with scattered sclerenchymatous cells (Fig. 3c, d). The xylem cylinder consists of about eight xylem strands, each about 0.5–0.6 mm thick (7–9 tracheids) (Fig. 3c). The xylem strands with mesarch protoxylem elements are mainly composed of metaxylem tracheids surrounding the protoxylem points (Fig. 3c). The xylem cylinder is dissected mostly by definite leaf gaps, which are of intermediate type (Fig. 3c). The phloem is ectophloic, but poorly preserved with no anatomical details.

The cortex contains many helically arranged leaf traces. The whole cortex can be differentiated into two distinct layers, i.e., a 1–1.5 mm thick inner cortex and a 0.9–1.5 mm thick outer cortex (Fig. 3a). The inner cortex is parenchymatous and contains nine leaf traces, whereas the outer cortex is sclerenchymatous with eight leaf traces (Fig. 3a, b). The leaf trace is reniform in shape, with a single endarch protoxylem cluster when departing from the stele (Fig. 3c, e), and becomes C-shaped with two protoxylem strands when entering into the outer cortex (Fig. 3f). Upon departing from the stele, the leaf trace enters the petiolar zone. The petiole base bears two typical stipular wings (Fig. 3i, j). The petiolar size, shape, and sclerenchyma arrangement varies at different levels. The sclerotic ring of the petiole base is heterogeneous, with an abaxial arch of thick-walled fibers in the semicircle (Fig. 3i. j). Only one large sclerenchyma mass occurs on each side of the stipular wing. Additionally, a meniscus sclerenchyma exists in the adaxial concavity of the vascular bundle (Fig. 3i, j). No sclerenchyma tissue occurs in other part of the petiolar cortical region (Fig. 3i, j). Adventitious roots bear typical diarch xylem (Fig. 3g) and always arise endogenously from the stele xylem cylinder (Fig. 3a).

Comparison and remarks: The fossil rhizome from Inner Mongolia is characterized by an ectophloic dictyoxylic siphonostele, a two-layered cortex, a mantle of petiole bases, and C-shaped leaf traces. Such a combination of anatomical characters strongly indicates an affinity of the fern family Osmundaceae. Generally, the anatomical characters of this fossil rhizome are consistent with those of the genus Ashicaulis Tidwell, which is featured by possessing ectophloic dictyoxylic siphonostele and complete leaf gaps (Tidwell 1994; Tidwell and Ash 1994; Tian et al. 2008). Vera (2008) proposed merging the form genus Ashicaulis Tidwell (with perforate steles) and Millerocaulis Erasmus ex Tidwell emend. Tidwell (with imperforate steles) into a single genus, the broadly defined Millerocaulis Tidwell emend. E.I. Vera. This was supported by phylogenetic network analysis of Osmundales by Bomfleur et al. (2017). Here, we retain the use of the fossil genus Ashicaulis in this study for Millerocaulis-like axes with perforate steles. To date, over 30 species referred to Ashicaulis have been documented worldwide (Tidwell and Ash 1994; Tian et al. 2008; Cheng 2011; Tian et al. 2014a, b). The petiolar sclerenchyma arrangement is considered a key feature for classifying osmundaceous species (Hewitson 1962; Miller 1971). So far, only six species of Ashicaulis incorporate a heterogeneous petiolar sclerotic ring that resembles our present fossil material. These species are A. johnstonii (Tidwell, Munzing et Banks) Tidwell, A. kidstonii (Stopes) Tidwell, A. liaoningensis (Zhang et Zheng) Tidwell, A. claytoniites Cheng, A. wangii Tian et Wang, and A. plumites Tian et Wang (Cheng 2011; Stopes 1921; Tidwell 1994; Tidwell et al. 1991; Tian et al. 2014a, b). It is noted, based on a detailed phylogenetic network analysis of Osmundales, these species were recently recombined to extant genera as Claytosmunda johnstonii (Tidwell, Munzing et Banks) Bomfleur, Grimm et McLoughlin, Osmunda kidstonii (Stopes) Bomfleur, Grimm et McLoughlin, Claytosmunda chengii Bomfleur, Grimm et McLoughlin, C. liaoningensis (Zhang et Zheng) Bomfleur, Grimm et McLoughlin, C. wangii (Tian et Wang) Bomfleur, Grimm et McLoughlin, and C. plumites (Tian et Wang) Bomfleur, Grimm et McLoughlin, respectively (Bomfleur et al. 2017). In this study, we retain the use of the taxonomic name referring to the fossil genus Ashicaulis Tidwell.

Compared to A. kidstonii, the present specimen has only one sclerenchyma mass in the petiolar vascular bundle concavity, whereas the former bears two sclerenchyma masses (Stopes 1921; Miller 1971). In A. claytoniites, the whole periphery of the sclerotic ring is encircled by thick-walled fibers (Cheng 2011). Differing from A. wangii and A. plumites, the abaxial thick-walled fiber arch on the sclerotic ring never bifurcates into two lateral parts in the new specimen (Tian et al. 2014a, b). Additionally, numerous sclerenchymatous clusters occur in the petiolar inner cortex of A. wangii (Tian et al. 2014a). Generally, the present specimen from Inner Mongolia bears great similarities to A. liaoningensis and A. johnstonii in petiolar structures (Tidwell et al. 1991; Zhang and Zheng 1991). However, the pith of A. johnstonii is homogeneous (Tidwell et al. 1991). Therefore, the present specimen from Inner Mongolia is assigned to A. liaoningensis.

Ashicaulis liaoningensis was first described by Zhang and Zheng (1991) as Millerocaulis liaoningensis Zhang et Zheng based on fossil rhizomes from the Middle to Upper Jurassic Tiaojishan Formation in Fuxin City of western Liaoning Province, NE China. Thereafter, it was reassigned to Ashicaulis by Tidwell (1994) based on possession of complete leaf gaps. Just as mentioned, this species was recently recombined as Claytosmunda liaoningensis (Zhang et Zheng) Bomfleur, Grimm et McLoughlin, as part of a detailed re-evaluation of phylogenetically significant anatomical characters within Osmundales (Bomfleur et al. 2017). Fossils of this species have also been reported from the Middle to Upper Jurassic Tiaojishan Formation in the Beipiao City of western Liaoning Province (Tian 2011).

Family Gleicheniaceae (Brown) Presl, 1825

Genus Gleicheniorachis Sharma, 1973

Species Gleicheniorachis sinensis Tian, Wang, Zhang et Liu sp. nov.

(Figs. 4–5)

Fig. 4
figure 4

Gleicheniorachis sinensis Tian, Wang, Zhang et Liu sp. nov. (BY-031-A, C) from the Upper Jurassic Manketouebo Formation in Horqin Right Wing Middle Banner, Inner Mongolia, NE China. a–c Cross-section of the gleicheniaceous racheids, showing the C-shaped vascular bundle (VB) with two incurved adaxial hooks (AH), the sclerenchyma sheath (SC), and the cortex (CT); the arrows indicate that protoxylem clusters, scale bar 1.0 mm. d Cross-section of a rachis, showing details of the C-shaped vascular bundle (VB) with two adaxial hooks and the sclerenchyma sheath (SC), scale bar 0.5 mm

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Fig. 5
figure 5

Gleicheniorachis sinensis Tian, Wang, Zhang et Liu sp. nov. (BY-031-C) from the Upper Jurassic Manketouebo Formation in Horqin Right Wing Middle Banner, Inner Mongolia, NE China. a–f Cross-section of the gleicheniaceous rachides. a Detail of the C-shaped vascular bundle (VB) with two adaxial incurved hooks and the sclerenchyma sheath (SC); the white arrows indicate the protoxylem groups, and the black arrows show the endodermis, scale bar 0.5 mm. b Abaxial part of the rachis, showing details of the vascular bundle (VB), sclerenchyma sheath (SC), inner zone (IC) and outer zone (OC) of the cortex, the black arrows show the endodermis, scale bar 0.5 mm. c Part of the rachis, showing details of the vascular bundle (VB), sclerenchyma sheath (SC), inner zone (IC) and outer zone (OC) of the cortex; the black arrows indicate the endodermis, and the white arrows show the epidermis cells, scale bar 0.5 mm. d Enlargement of the adaxial incurved hooks of the vascular bundle, scale bar 0.1 mm. e, f Details of vascular bundle (VB), and sclerenchyma sheath (SC); the black arrows indicate the endodermis cells, scale bar 0.1 mm

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Specific diagnosis: Permineralized fern rachides consisting of a C-shaped vascular bundle, a distinct sclerenchyma sheath, an endodermis and a cortex, and 1.5–3.0 mm in diameter. The C-shaped vascular bundle, about 1.6 mm in width, with the lateral margins forming two incurved adaxial hooks. The xylem strands consisting of one to three layers of tracheids with over six protoxylem strands, endarch maturation. Sclerenchyma sheath with a thickness of three to five cells surrounding the vascular zone. No sclerenchymatous central column occurring in the vascular bundle concavity. In fully developed rachides, the cortex well developed and differentiated into a parenchymatous inner zone and a sclerenchymatous outer zone. Endodermis, composed of only one single layer of cells, sandwiched between the pericycle and the inner zone of the cortex.

Holotype: BY-031 with three slides BY-031-(A-C)

Repository: The specimen and slides are deposited in the Shenyang Institute of Geology and Mineral Resources, Shenyang, China

Type locality: Baiyinbaoligao Village of Daiqintala Town, Horqin Right Wing Middle Banner, Inner Mongolia, NE China

Formation and age: Manketouebo Formation, Late Jurassic

Etymology: The specific epithet sinensis is proposed for Sino (China), where the fossil locality Horqin Right Wing Middle Banner, Inner Mongolia administratively belongs.

Description: Numerous isolated fossil rachides were found within the tuffaceous matrix. The rachides are elliptical to circular in cross-section, with diameters of 1.5–3.0 mm (Fig. 4a–c). Each rachis consists of a C-shaped vascular bundle, a distinct sclerenchyma sheath, an endodermis, and a cortex (Fig. 4a–c). The surface of the rachides is smooth with no scales (Fig. 4a–c). The C-shaped vascular bundle is about 1.6 mm in width, with the lateral margins forming two adaxial incurved hooks (Figs. 4a–d, 5a, 5d). The xylem strands consist of one to three layers of tracheids (Fig. 4d, 5a). The protoxylem strands vary (over six) and show typical endarch maturation (Figs. 4a–b, 5a). A distinct sclerenchyma sheath is present surrounding the vascular zone, with a thickness of three to five cells (Figs. 4a–c, 5a–c). Cells of the sclerenchyma sheath are circular or angular, closely placed without intercellular spaces (Fig. 5a, b, e, f). No sclerenchymatous central column occurs in the vascular bundle concavity. In fully developed rachides, the cortex is well developed and differentiated into two zones. The inner zone is parenchymatous with a thickness of four to six cells, whereas the outer zone is sclerenchymatous with a thickness of seven to nine cells (Fig. 5b, c). Generally, the cell size of the inner cortex is remarkably larger than that of the outer cortex. A typical endodermis, composed of only one single layer of cell, is sandwiched between the sclerenchyma sheath and the inner zone of the cortex (Fig. 5e). It completely encloses both the external and internal periphery of the vascular bundle arc (Fig. 5b, e, f). The endodermis cells are parenchymatous and larger than adjacent cells of the sclerenchyma sheath.

Comparison: In gross anatomy, the present fossil rachides from Inner Mongolia show typical petiolar characters of the fern family Gleicheniaceae (Boodle 1901; Bower 1926; Chrysler 1943, 1944). Gleicheniorachis was established by Sharma (1973) based on fossils from India to include isolated gleicheniaceous petioles and rachides. So far, only two species have been referred to this genus, i.e., Gleicheniorachis jurassica Sharma and G. mittrii Bohra et Sharma, which were both reported from the Lower Cretaceous of the Rajmahal Hills, India (Sharma 1973; Bohra and Sharma 1979; Tripathi 2008; Tripathi et al. 2013). Generally, the present fossil material from China resembles Gleicheniorachis in the C-shaped petiolar trace with two incurved adaxial hooks and endarch protoxylem points. It is thus reasonable to assign them to Gleicheniorachis. The present material from Inner Mongolia resembles the two reported species of Gleicheniorachis in gross anatomy but differs in detail, and thus, has been described as a new species Gleicheniorachis sinensis sp. nov. Tian, Wang, Zhang et Liu. Compared to the present new species, a distinct sclerenchymatous column occurs in the vascular bundle concavity of both G. jurassica and G. mittrii (Table 1). However, such a column is absent in the fossil rachides from China. Additionally, only three to five protoxylem points were observed in the xylem of G. mittrii, whereas the number is over six in the new species from China.

Table 1 Comparisons on anatomical characters of fossil gleicheniaceous rachides
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Besides Gleicheniorachis, there are also a series of fossil records referred to gleicheniaceous fern, represented by permineralized rhizomes and their attached rachides. A detailed comparison based on anatomical characters of fossil gleicheniaceous rachides is given in Table 1. Among them, Boodlepteris turoniana Gandolfo, represented by well-preserved fusinized rhizomes, petioles, pinnules, sori, and spores, was described from the Upper Cretaceous of New Jersey, USA (Gandolfo et al. 1997). The petiolar cortex of B. turoniana is composed of very thick-walled fibers (Gandolfo et al. 1997); whereas, the cortex of Gleicheniorachis sinensis sp. nov. is two-zoned. Gleichenia chaloneri Herendeen et Skog, described based on fusainized material from the Lower Cretaceous of England, was another anatomically preserved species referred to Gleicheniaceae (Herendeen and Skog 1998). It is noted that the rachis of Gleichenia chaloneri is surrounded by scales; however, no scales were found attached with the fossil rachides from China. Additionally, the petiolar xylem of Gleichenia chaloneri generally consists of a single row of tracheids and thus, differs from that of G. sinensis sp. nov. Karafit (2008) described some permineralized gleicheniaceous rachis segments from the Upper Cretaceous in British Columbia, Canada. They also resemble the present fossil material in gross anatomy. However, their petiolar xylem seems to be also composed of only one single layer of tracheids with a larger size (see in Karafit 2008, Fig. 3). In contrast, the xylem of G. sinensis sp. nov. consists of two to three layers of tracheids. Generally, Gleicheniorachis sinensis sp. nov. from China has more anatomical similarities to the rachis of Gleichenia appianensis Mindell, Stockey, Rothwell et Beard from the Eocene of Vancouver Island, British Columbia, Canada (Mindell et al. 2006), especially in having a two-layered cortex, a sclerenchyma sheath surrounding the vascular bundle, and the number of protoxylem groups (Table 1). However, further comparisons between the two taxa are not possible, since anatomical details of the rhizome are not known for Gleicheniorachis sinensis. Hence, the authors prefer to treat it as a new species of the form genus Gleicheniorachis.

Discussion

The discovery of the osmundaceous fern rhizome Ashicaulis liaoningensis in the Jurassic of Inner Mongolia provides additional information for understanding the palaeogeographical distribution of the fern taxon. This species has been described from the Middle to Upper Jurassic Tiaojishan Formation in the Fuxin and Beipiao regions of western Liaoning Province, NE China (Zhang and Zheng 1991; Tian 2011). The current new finding expands its geographic distribution and indicates that A. liaoningensis was a common component of the Jurassic flora in Northeast China. It is noted, the occurrence of A. liaoningensis is also of stratigraphical significance. The present fossil-bearing strata in Inner Mongolia are preliminarily considered as the Upper Jurassic Manketouebo Formation (Fu et al. 2012). It is noted that the fossil wood assemblages of the Manketouebo Formation, represented by Protaxodioxylon romanense Philippe, Xenoxylon hopeiense Chang and Araucarioxylon batuense Duan (Fu et al. 2012), have also been found from the Middle to Upper Jurassic Tiaojishan Formation in western Liaoning and northern Hebei Provinces (Zhang et al. 2006). This implies that the fossil-bearing strata in Inner Mongolia may be stratigraphically correlated in age with the Tiaojishan Formation in western Liaoning Province.

The family Gleicheniaceae is a primitive leptosporangiate fern lineage represented by about 130 living species referred to six genera (Ogura 1972). The family is considered to have a Palaeozoic origin. Mesozoic Gleicheniaceae ranges from the Early Triassic to the Cretaceous (Tidwell and Ash 1994). In China, Gleicheniaceae have diverse fossil records ranging from the late Palaeozoic to the Cenozoic (Wang et al. 2009). A systematic review of the fossil gleicheniaceous megaplants recorded in China suggests that gleicheniaceous ferns are remarkably diverse in the Early Cretaceous with 12 species (Wang et al. 2009). However, they are very scarce and limited in the Jurassic with only three species of one genus, i.e., Gleichenites nitida Harris from the Lower Jurassic in Hunan Province, southern China; and G. nordenskioldi (Heer) Seward and G. porsildi (Heer) Seward from the Middle to Upper Jurassic Chaoyangtun Formation in Heilongjiang Province, northeastern China (Zheng and Zhang 1982; Zhou 1984). It is noted, the age of the Chaoyangtun Formation is now considered to be Early Cretaceous (Zheng et al. 2005). In other words, no Jurassic gleicheniaceous fossils have been recorded in northern China. Hence, the new discovery represents the first unequivocal record of Jurassic gleicheniaceous ferns in northern China. It is also the first record of the Jurassic permineralized gleicheniaceous fern in the Northern Hemisphere. Undoubtedly, the new findings not only provide information on petiolar anatomy of Gleicheniaceae in the Jurassic, but also contribute to better understanding of the evolution of gleicheniaceous plants in China.

In conclusion, the current discovery of the permineralized fern remains from Inner Mongolia provides new data and evidence for exploring the anatomical diversity of Mesozoic ferns in China, and contributes to further understanding the floral composition of Late Jurassic flora in Northeast China.