A systematic overview of fossil osmundalean ferns in China: Diversity

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Received 7 August 2014; received in revised form 9 December 2014; accepted 12 May ...... resemblances to the Palaeocene Osmunda pluma, as well as to.
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A systematic overview of fossil osmundalean ferns in China: Diversity variation, distribution pattern, and evolutionary implications Ning Tian a,f,g , Yong-Dong Wang b,c,∗ , Man Dong d , Li-Qin Li b , Zi-Kun Jiang e a

College of Palaeontology, Shenyang Normal University, Shenyang 110034, China Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China c Key Laboratory of Economic Stratigraphy and Palaeogeography, Chinese Academy of Sciences, Nanjing 210008, China d College of Geosciences, Yangtze University, Wuhan 430100, China e Chinese Academy of Geological Sciences, Beijing 100037, China f State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China g Key Laboratory for Evolution of Past Life in Northeast Asia, Ministry of Land and Resources, Shenyang 110034, China b

Received 7 August 2014; received in revised form 9 December 2014; accepted 12 May 2015

Abstract The order Osmundales is a unique fern taxon with extensive fossil records in geological past. Diverse osmundalean fossils have been reported from China, ranging in age from the Late Palaeozoic to the Cenozoic. Most of them are based on leaf impressions/compressions, but permineralized rhizomes are also well documented. In this study, we provide a systematic overview on fossil osmundalean ferns in China with special references on diversity variations, distribution patterns, and evolutionary implications. Fossil evidence indicates that this fern lineage first appeared in the Late Palaeozoic in China. The Late Triassic to Middle Jurassic interval was the radiation stage. From the Late Jurassic onward, fossil diversity declined rapidly. Cenozoic osmundalean taxa are represented by the relict species of Osmunda. Geographically, osmundalean fossils are found from both the Northern and Southern phytoprovinces of China, though variations are documented for geographical ranges. The Chinese fossil records cover almost all important stages for the macroevolution of the Osmundales, and contribute to further understanding of evolutionary processes of this peculiar fern lineage. © 2015 Published by Elsevier B.V. on behalf of Nanjing Institute of Geology and Palaeontology, CAS. Keywords: Osmundales; Fossil record; Diversity variation; Distribution pattern; Macroevolution; China

1. Introduction Osmundales, a unique group among the oldest existing ferns, consist of two major lineages, including the extinct family Guaireaceae and the family Osmundaceae with both living and fossil representatives. This fern clade is generally considered as an intermediate between eusporangiate and leptosporangiate ferns (Tidwell and Ash, 1994). It is proposed to be the stem-group of the Polypodioidae and sister to the remaining lineages of leptosporangiate ferns based on phylogenetic analyses (Hasebe et al., 1995; Pryer et al., 2001, 2004; Schuettpelz et al., ∗

Corresponding author: Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China. Tel.: +86 25 8328 2221; fax: +86 25 8335 7026. E-mail address: [email protected] (Y.D. Wang).

2006; Schuettpelz and Pryer, 2007; Hennequin et al., 2008). The extant Osmundales are represented mainly by four genera within the family Osmundaceae, including Osmunda, Todea, Leptopteris, and Osmundastrum (Metzgar et al., 2008). The extensive fossil records show, however, that this order had a much greater distribution and higher diversification in the geological past (Banerji, 1992; Ash and Morales, 1993; Tidwell and Ash, 1994; Kiritchkova et al., 1999; Collinson, 2001; Bodor and Barbacka, 2008; Taylor et al., 2009). Among these records, over 80 species ascribed to 14 genera of fossil osmundalean rhizomes have been documented worldwide, ranging from the Permian to the Cenozoic in age (Tian et al., 2008). In China, limited living members of this fern order are distributed, including Osmunda and Osmundastrum mainly in southern China (Wu, 1992; Wang and Wang, 2001); as a contrast, abundant fossil osmundalean taxa have been reported from the Palaeozoic to the Cenozoic

http://dx.doi.org/10.1016/j.palwor.2015.05.005 1871-174X/© 2015 Published by Elsevier B.V. on behalf of Nanjing Institute of Geology and Palaeontology, CAS.

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deposits. A couple of such fossil taxa have been investigated in some details, e.g., Todites and fossil rhizomes (Wang et al., 2005; Tian, 2011). However, the diversification and distribution features of this fern group are still scarcely considered. In this paper, we review the fossil osmundalean ferns in China on the basis of known fossil records, with an emphasis on its diversity variations, distribution patterns, and evolutionary implications. The scope of this review focuses mainly on macrofossil with an exclusion of these osmundalean dispersed spores. This represents the first comprehensive analysis and overview on the osmundalean fossils in China, and provides new clues for understanding the origin, radiation, and development of this fern lineage. 2. Materials and methods Materials for this study involve all available published data concerning fossil Osmundales in China, such as research papers, monographs and atlases of fossil plants. These fossils mainly fall into two types, i.e., compression/impression foliage and permineralized rhizome. For each type of the data, the systematic attribution, geographical origin, and geological source are compiled. Fossil locality information is plotted in a geographical map to show the distribution patterns. The stratigraphic data are arranged into a time framework, e.g., Early Permian (P1 ), Late Permian (P2 ), Early Triassic (T1 ), Middle Triassic (T2 ), etc. on the basis of up-dated biostratigraphic evidence. Selected sketch drawings and illustrations of some representative fossil taxa referred to the Osmundales are given, based on figures, plates, and descriptions from the original publications. 3. Fossil record and diversity of Osmundalean ferns in China Our general analysis indicates that the earliest record of Osmundales in China dates back to the Late Palaeozoic (Gu and Zhi, 1974; Li, 1983). During the Mesozoic, the China territory is divided into two phytoprovinces, i.e., the Northern Phytoprovince (NPP) and Southern Phytoprovince (SPP), delimited by the Kunlun-Qinling-Dabie Mountain Range (Sun et al., 1995a,b; Zhou, 1995). Osmundalean ferns flourished with a high diversity in both phytoprovinces during the Mesozoic. Several Cenozoic fossil taxa of the family are also reported. The following is a summary for the diverse type of osmundalean fossils in China. 3.1. Osmundalean leaf fossils The foliage fossils of the Osmundales are not well studied systematically due to the commonly poor preservation and frequent absence of fertile characters. As a result, numerous frond fossils are recognized only as “Osmunda-like” fossil morphogenera (Brongniart, 1849; Taylor et al., 1990; Collinson, 2001; Van Konijnenburg-Van Cittert, 2002). In China, osmundaceous foliage fossils are very common, represented mostly by Todites (Seward) Harris, Osmundopsis (Harris) Harris and Osmunda Linnaeus, as well as three other genera including Cladophlebis Brongniart, Raphaelia Debey et Ettingshausen, and Tuarella

Burakova (Wang et al., 2005; Deng, 2007). Some other foliage taxa referable to the Osmundales have never been documented in China so far, such as Anomopteris Brongn., Phyllopteroides Medwell, and Cacumen Cantrill et Webb (Cantrill and Webb, 1987; Banerji, 1992; Cantrill and Nagalingum, 2005; Taylor et al., 2009). Osmundaceous pinnae are generally characterized by a pinniform venation; however, several specimens with simple reticulated veins were previously assigned to the Osmundaceae (Osmundales) in China, such as Abropteris yongrenensis Li et Tsao and Reteophlebis simplex Li et Tsao (Li et al., 1976; Wu, 1982). In fact, Reteophlebis simplex is a synonym of Cynepteris lasiophora Ash, which was first reported from the Upper Triassic Chinle Formation of New Mexico, USA (Ye et al., 1986). The latter was ascribed to a well-defined family Cynepteridaceae (Ash, 1970). The systematic affinity of Abropteris yongrenensis remains poorly understood. However, it shows a close similarity to Reteophlebis simplex (C. lasiophora) in many characters, and may represent an otherwise unknown stock of cynepteridaceous plants. It is noted that the Cynepteridaceae is proposed to be closely related to the fern family Schizaeaceae (Ash, 1970; Axsmith, 2009). 3.1.1. Genus Todites Seward emend. Harris The genus Todites was erected by Seward (1900) based on materials from Yorkshire, and was then emended by Harris (1961). It was named for fossil leaves that morphologically resemble the extant Todea. The sporangia of Todites are always borne along the veins on the dorsal side of the fertile pinnae, which are morphologically similar to the vegetative ones (Harris, 1961; Wang et al., 2005). The annulus of Todites is always strongly apical, covering the entire apical region of the sporangium (Harris, 1961; Hewitson, 1962). Todites first appeared in the Late Permian, with fertile pinnae bearing in situ spores from the Upper Permian in Russia (Radˇcenko, 1955; Naugolnykh, 2002). It is the most common genus of the Mesozoic osmundaceous plants in China, and about 17 species have been reported (Wang et al., 2005), mainly represented by T. shensiensis, T. denticulatus, T. goeppertianus, T. williamsonii, T. princeps, and T. scorebyensis (Fig. 1). The earliest fossil record of Todites in China is from the Middle Triassic (e.g., Todites shensiensis from the Middle Triassic of Shaanxi and Inner Mongolia) (Sze, 1956; Zhang, 1976; Huang and Zhou, 1980). The genus flourished during the Late Triassic to the Middle Jurassic, but declined rapidly during the Late Jurassic with only one species recorded (T. denticulatus). The Cretaceous taxon of Todites in China is limited to T. major, described from the Lower Cretaceous Yixian Formation in western Liaoning Province, NE China (Sun et al., 2001). Geographically, Todites is widely distributed in both the NPP and SPP (Wang et al., 2005). During the Middle Triassic, almost all species are restricted to the NPP; however, in the interval from the Late Triassic to the Early Jurassic, the species diversity is much higher in the SPP than that in the NPP. In the Middle Jurassic, almost all Todites are reported from the NPP again. The genus became extinct at the end of the Early Cretaceous in China.

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Fig. 1. Sketch drawing of pinnae/pinnules and venations of some major Todites species in China. (A) Todites shensiensis (P’an), after Sze (1956) and Yang et al. (1994); scale bar = 4 mm. (B) T. princeps (Presl) Gothan, after Sze (1956) and Yang et al. (1994); scale bar = 2 mm. (C) T. williamsonii (Brongn.) Seward, after Chen et al. (1984); scale bar = 2.5 mm. (D) T. denticulatus (Brongn.) Krasser, after Chen et al. (1984); scale bar = 5 mm. (E) T. scorebyensis Harris, after Li et al. (1976); scale bar = 1 cm. (F) T. major Sun et Zheng, based on Sun et al. (2001); scale bar = 1 cm.

The in situ spores of several Todites species (e.g., Todites thomasi, T. denticulatus, T. williamsoni, and T. princeps) were previously investigated in detail (Harris, 1931, 1961; Couper, 1958; Van Konijnenburg-Van Cittert, 1978). Couper (1958) demonstrated that the in situ spores of Todites williamsonii and T. princeps were well correlated with the type specimen of dispersed spore Todisporites major. Tralau (1968) correlated the in situ spores of T. denticulatus to Todisporites cladothecoides. Unfortunately, so far, no records of in situ spores of Todites have been reported in China. 3.1.2. Genus Osmundopsis Harris emend. Harris Osmundopsis, characterized by dimorphic fertile and sterile leaves, is another important Mesozoic genus of osmundalean ferns (Harris, 1961; Van Konijnenburg-Van Cittert, 1996; Naugolnykh, 2002). It was initially established by Harris (1931) for dimorphic tripinnate cladophleboid foliage bearing Osmunda-like fertile foliage but was later emended to also include bipinnate ones (Harris, 1961). The fertile leaves of Osmundopsis are commonly lanceolate, bipinnate or tripinnate with filiform ultimate branches, and bear groups of sporangia (Harris, 1961). The sporangium of Osmundopsis is featured by an apical annulus, which always covers the entire apical region of the sporangium (Harris, 1961; Phipps et al., 1998). The genus differs from Osmunda in the sporangium apical sclerotic cell size (Harris, 1961; Ye et al., 1986). Osmundopsis was previously considered to be an intermediate between Todites and Osmunda (Miller, 1971; Van Konijnenburg-Van Cittert, 1978). A recent study (Escapa and Cúneo, 2012) suggested that Osmundopsis should be referred to a non-leptopteroid paraphyletic group (Osmunda and Osmundastrum) and represents

a natural taxon combining the pinnule morphology of Osmunda (i.e., reduced laminae in fertile zones) with a sporangial morphology closer to that of the genus Todea. In China, Osmundopsis fossils are not as common as Todites, and only six species are documented, ranging from the Late Triassic to the Early Jurassic (Table 1). Among them, Osmundopsis plectrophora Harris shows a widespread range and is reported from the Late Triassic Hsüchiaho Formation in the Sichuan Basin (Ye et al., 1986; Wu, 1999), the Shazhenxi Formation in Hunan Province (He and Shen, 1980; Zhang, 1982), as well as from the Lower Jurassic in Gansu (Yang and Shen, 1988) and Inner Mongolia (Mei et al., 1989). As the type species of the genus, Osmundopsis sturii bears delicate branches covered by obovate sporangia, each with a thickened distal cap (Fig. 2D, E). In China, this species has been described from the Early Jurassic Hsiangchi Formation in Zigui of Hubei (Wu, 1991) and from the Middle Jurassic Xishanyao Formation in Shaerhu coal field of Xinjiang (Dong and Sun, 2011). However, re-examination of the fossil specimens from the Hsiangchi Formation, which was previously described by Wu (1991) as cf. Osmundopsis sturii, indicated that they are fertile pinnae of Todites (probably T. williamsonii) (Wang, 2002). Osmundopsis jingyuanensis Liu has been documented from the Lower Jurassic Daolengshan Formation in Jingyuan of Gansu Province (Liu, 1982). In addition, two undefined species referred to Osmundopsis were reported from the Lower Jurassic in Anhui and Beijing, respectively (Duan, 1987; Huang, 1988). The in situ spores of the Osmundopsis were investigated by several authors (e.g., Harris, 1931, 1961; Couper, 1958; Van Konijnenburg-Van Cittert, 1978, 1996). The in situ spores of O. plectrophora can be well correlated with the type specimen of

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Table 1 List of the fossil records of osmundalean ferns in China. Species Osmundopsis Harris emend. Harris O. plectrophora Harris

Locality

Formation

Age

References

Tieshan of Daxian, Sichuan Wenquan of Kaixian, Chongqing Lanzhou, Gansu

Hsüchiaho Formation Hsüchiaho Formation

Late Triassic

Ye et al., 1986; Wu, 1999; Sun K.Q. et al., 2010 Ye et al., 1986; Sun K.Q. et al., 2010

Gouyadong of Lechang, Guangdong Changyou Banner, Inner Mongolia Yizhang of Hunan O. cf. plectrophora Harris O. jingyuanensis Liu O. sturii (Raciborski) Harris O. sp.

O. sp. Osmunda Linnaeus O. cretacea Samylina

O. sachalinensis Kryshtofovich O. greenlandica (Heer) Brown O. lignitum (Giebel) Stur.

O. totangensis (Colani) Guo O. japonica Thunb.

O. heeri Gaudin Raphaelia Debey et Ettingshausen R. diamensis Seward

Tieshan of Daxian, Sichuan Jingyuan, Gansu Shaerhu coal field of Xinjiang Zhaitang of Western Hills, Beijing Lalijian of Huaining, Anhui Jiaohe, Jilin Huolinhe Basin, Inner Mongolia Tiefa Basin, Liaoning Fuxin Basin, Liaoning Hailar Basin, Inner Mongolia Jiayin, Heilongjiang Jiayin, Heilongjiang Fushun, Liaoning Changchang Basin, Hainan Duotang of Kunming, Yunnan Lianghe Basin of Tengchong, Yunnan Shangzhi, Heilongjiang Diam River of Hefeng County, Xinjiang Junggar Basin, Xinjiang Central Shaanxi, and eastern Gansu Beipiao, Liaoning

Late Triassic

Daxigou Formation Xiaoping Formation

Early Jurassic

Yang and Shen, 1988

Late Triassic

Feng et al., 1977; Sun K.Q. et al., 2010

South Tulesu Formation Shazhenxi Formation Hsüchiaho Formation Daolengshan Formation Xishanyao Formation Yaopo Formation

Early Jurassic

Mei et al., 1989

Late Triassic Late Triassic

He and Shen, 1980; Zhang, 1982, 1986 Wu, 1999

Early Jurassic

Liu, 1982; Zhang et al., 1998

Middle Jurassic

Dong and Sun, 2011

Middle Jurassic

Duan, 1987

Wuchang Formation

Early Jurassic

Huang, 1988

Shansong Formation Huolinhe Formation Xiaoming’anbei Formation Fuxin Formation

Early Cretaceous

Li et al., 1986

Early Cretaceous

Deng, 1995

Early Cretaceous

Chen et al., 1988

Early Cretaceous

Chen et al., 1988

Damoguaihe Formation Wuyun Formation

Early Cretaceous

Deng et al., 1997

Paleocene

Wang et al., 2006

Wuyun Formation

Paleocene

Tao and Xiong, 1986

Guchengzi Formation Changchang Formation ?

Late Eocene

Zhi and Gu, 1978

Late Paleocene to Early Eocene Miocene to Pliocene Late Miocene

Guo, 1979

Dalianhe Formation

Eocene

Zhang et al., 1980

Xishanyao Formation

Middle Jurassic

Gu, 1984

Xishanyao Formation Yan’an Formation

Middle Jurassic

Sun G. et al., 2010

Early Jurassic

Mi et al., 1996

Haifanggou Formation

Middle Jurassic

Zhang et al., 1980; Zhang and Zheng, 1987

?

Zhi and Gu, 1978 Tao, 2000

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Table 1 (Continued) Species

Locality

Formation

Age

References

Aru Horqin of Chifeng, Inner Mongolia Mishan, Heilongjiang

Xinmin Formation

Middle Jurassic

Zhang et al., 1980

Yunshan Formation of Longzhaogou Group Qihulin Formation Dongshan Formation Wanbao Formation Dameigou Formation

Late Jurassic

Zheng and Zhang, 1982

Middle Jurassic Early Cretaceous

Cao, 1984 Zheng and Zhang, 1983

Middle Jurassic

Mei et al., 1989

Early Middle Jurassic

Li et al., 1988

Yinmagou Formation

Early Middle Jurassic

Li et al., 1988

Xiayaopo Formation Zhiluo Formation

Middle Jurassic

Chen et al., 1980

Late Middle Jurassic

Ye and Li, 1982; Zhou, 1995

Xishanyao Formation Fuxian Formation Fuxian Formation

Middle Jurassic

Zhang et al., 1998

Early Jurassic Early Jurassic

Huang and Zhou, 1980 Huang and Zhou, 1980

Datong Formation Mentougou Formation

Middle Jurassic Middle Jurassic

Wang, 1984 Wang, 1984

Shahezi Formation Huoshiling Formation

Late Jurassic?

Yang and Sun, 1982a,b

Late Jurassic

Yang and Sun, 1982a,b

Tiaojishan Formation

Middle Jurassic

Zhang and Zheng, 1987

Wanbao Formation

Middle Jurassic

Yang and Sun, 1985

Haifanggou Formation Kezilenuer Formation Xishanyao Formation Xishanyao Formation

Middle Jurassic

Zhang and Zheng, 1987

Middle Jurassic

Zhang et al., 1998

Middle Jurassic

Zhang et al., 1998

Middle Jurassic

Zhang et al., 1998

Middle Jurassic

Chen et al., 1984

Middle Jurassic

Li et al., 1988

Middle Jurassic

Mei et al., 1989

Early Cretaceous Early Cretaceous

Zhang, 1987 Zhang, 1987

Late Jurassic

Yang and Sun, 1982b

Heilongjiang Hegang, Heilongjiang Wanbao of Yao’an, Jilin Dayangtougou of Qaidam Basin, Qinghai Dameigou of Qaidam Basin, Qinghai Mentougou, Beijing Gaotouyao of Dalateqi, Inner Mongolia Hami, Xinjiang

R. prinadai Vachrameev

R. stricta Vachrameev

R. glossoides Vachrameev

R. aff. neuropteroides Debey et Ettingshausen R. sp. R. sp. R. sp. R. sp. R. sp.

Shenmu, Shaanxi Jungar Banner, Inner Mongolia Datong, Shanxi Xiahuayuan of Zhangjiakou, Hebei Yingcheng of Jiutai, Jilin Changtu of Liaoning, and Jiutai of Jilin Changheyingzi, Laimayingzi, and Shebudai of Beipiao, Liaoning Xishala of Zhuluteqi, Inner Mongolia Haifanggou of Beipiao, Liaoning Kelasu River of Kuqa, Xinjiang Shanshan, Xinjiang Kuisu coal mine, northeastern Xinjiang Da’anshan of Beijing North Qaidam Basin, Qinghai Shan-Gan-Ning Basin Fuxin, Liaoning Yingcheng, Jilin Changtu of Liaoning, and Jiutai of Jilin

Upper Yaopo Formation Dameigou Formation Fuxian Formation Fuxin Formation Yingcheng Formation Huoshiling Formation

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Table 1 (Continued) Species

Locality

Formation

Age

References

Qaidam Basin, Qinghai

Dameigou Formation

Middle Jurassic

Li et al., 1988

Tiaojishan Formation Tiaojishan Formation

Middle Jurassic

Cheng and Li, 2007

Middle Jurassic

Cheng et al., 2007

Tiaojishan Formation Tiaojishan Formation Tiaojishan Formation Tiaojishan Formation Tiaojishan Formation Tiaojishan Formation Tiaojishan Formation

Middle Jurassic

Wang, 1983

Middle Jurassic

Zhang and Zheng, 1991

Middle Jurassic

Matsumoto et al., 2006

Middle Jurassic

Cheng, 2011

Middle Jurassic

Tian et al., 2013

Middle Jurassic

Tian et al., 2014a

Middle Jurassic

Tian et al., 2014b

Shuicheng, Guizhou

Wangjiazhai Formation

Late Permian

Li, 1983, 1993

Zhongmingella Wang, Hilton, He, Seyfullah et Shao Shuicheng, Zhongmingella plenasioides (Li) Wang et al. Guizhou

Wangjiazhai Formation

Late Permian

Li, 1983; Wang et al., 2014a

Xuanwei Formation

Late Permian

Li and Cui, 1995; Wang et al., 2014b

Tuarella Burakova T. lobifolia Burakova

Millerocaulis Erasmus ex Tidwell emend. Tidwell M. sinica Cheng et Li Beipiao, Liaoning M. preosmunda Cheng, Wang et Li

Beipiao, Liaoning

Ashicaulis Tidwell A. hebeiensis (Wang) Tidwell

Zhuolu, Hebei

A. liaoningensis (Zhang et Zheng) Tidwell

Beipiao, Liaoning

A. macromedullus Matsumoto, Saiki, Zhang, Zheng et Wang A. claytonites Cheng

Zhuolu, Hebei Beipiao, Liaoning

A. beipiaoensis Tian, Wang, Zhang, Jiang et Dilcher A. wangii Tian et Wang

Beipiao, Liaoning

A. plumites Tian et Wang

Beipiao, Liaoning

Shuichengella Li Shuichengella primitiva (Li) Li

Tiania (Tian et Chang) Wang et al. T. yunnanense (Tian et Chang) Wang et al.

Beipiao, Liaoning

Xuanwei, Yunnan

Notes: 1. Fossil records of the genus Todites have been listed in detail by Wang et al. (2005), hence this taxon is excluded in this table; 2. Fossil records of Cladophlebis in China are not included either in this table for its vague systematic affinity.

dispersed spore Osmundacidites wellmanii (Coper, 1958). Van Konijnenburg-Van Cittert (1978) proposed that the in situ spores of O. sturii also well resemble the dispersed osmundalean spore Osmundacidites wellmanii. Unfortunately, no fertile pinnae with in situ spores have been reported for Osmundopsis in China so far. 3.1.3. Genus Osmunda Linnaeus The genus is morphologically distinguished from other two extant genera Todea and Leptopteris by the facts that its fertile pinnae are contracted with little or no vegetative lamina present and the pinnae are articulated at the point of attachment to the rachis (Hewitson, 1962). Extant Osmunda has a sub-cosmopolitan distribution with its highest diversification in East and Southeast Asia (Tagawa, 1941; Kramer and Green, 1990). The genus was recently split into two genera, Osmunda and Osmundastrum (Jud et al., 2008; Metzgar et al., 2008). The latter is distinguished by rhizome anatomical structures bearing three clusters of thick-walled fibers on the petiolar sclerotic ring (Miller, 1967), but is much more similar to Osmunda in foliage morphology (Escapa and

Cúneo, 2012). In this sense, most of the anatomically unpreserved foliage fossils, which were previously assigned to the genus Osmunda, may be assigned to any of these two genera. Alternatively, Escapa and Cúneo (2012) proposed that these species should be reassigned to the genus Osmundopsis. Several other Mesozoic ferns are assigned to the genus Osmunda, such as O. vakhrameevii, O. krassilovii, and O. sibirica from the Jurassic of Russia, and O. vancouverensis from the Lower Cretaceous of British Columbia, Canada (Kiritchkova et al., 1999; Vavrek et al., 2006). Osmunda claytoniites from the Upper Triassic of Antarctica was regarded as the oldest unequivocal record of Osmunda crown group (Phipps et al., 1998). These lines of fossil evidences imply that Osmunda may represent an example of evolutionary stasis. In China, about seven fossil species of Osmunda have been described (Table 1). Among them, one species is from the Lower Cretaceous (O. cretacea), and the rest are from the Palaeocene (i.e., Osmunda sachalinensis and O. greenlandica), Eocene (O. lignitum and O. heeri), and Neogene (O. totangensis and O. japonica) (Fig. 3) (Zhi and Gu, 1978; Guo, 1979; Zhang et al., 1980; Tao and

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Fig. 2. Pinnae and pinnules of some fossil foliages (Osmunda, Osmundopsis and Raphaelia) in China. (A) Osmunda cretacea Samylina, from the Lower Cretaceous Xiaominganbei Formation in the Tiefa Basin, Liaoning Province (Courtesy Dr. Sheng-Hui Deng); scale bar = 2 cm. (B, C) Raphaelia diamensis Seward, from the Middle Jurassic Xishanyao Formation in the Junggar Basin, Xinjiang (Courtesy Dr. Ge Sun and Dr. Yu-Yan Miao); scale bar = 1 cm. (D) Osmundopsis sturii (Raciborski) Harris, from the Middle Jurassic Xishanyao Formation in the Tuha Basin, Xinjiang, showing the fertile pinnae; scale bar = 4 mm. (E) O. sturii (Raciborski) Harris, from the Middle Jurassic Xishanyao Formation in the Tuha Basin, showing details of the sporangia; scale bar = 300 ␮m.

Fig. 3. Sketch drawing of pinnae/pinnules of Osmunda species in China. (A) Osmunda lignitum (Giebel) Stur, based on Zhi and Gu (1978); scale bar = 1 cm. (B, C) O. cretacea Samylina; (B) portion of the sterile frond, based on Deng and Chen (2001), pl. 1, fig. 3, scale bar = 1.5 cm; (C) detail of a sterile pinnule, based on Deng and Chen (2001), pl. 4, fig. 1, scale bar = 1 cm. (D) O. sachalinensis (Krysht), based on Wang et al. (2006); scale bar = 1 cm.

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Xiong, 1986; Xiong, 1986; Tao, 2000; Deng and Chen, 2001; Wang et al., 2006). Osmunda cretacea (Figs. 2A, 3B, C) is one of the most common taxon from the Early Cretaceous in Far-East regions (Samylina, 1964; Deng, 1995, 2002; Deng and Shang, 2000). It is described mainly from the Early Cretaceous coal-bearing strata in northern China, i.e., the Tiefa and Fuxin basins of Liaoning Province, the Huolinhe and Hailar basins of Inner Mongolia, and the Jiaohe Basin of Jilin Province (Li et al., 1986; Chen et al., 1988; Deng et al., 1997; Deng and Shang, 2000; Deng and Chen, 2001). Li et al. (1986) described two Raphaelia species (R. cretacea and R. denticulata) from the Jiaohe Basin, Jilin Province. It is noted that R. cretacea resembles O. cretacea in gross morphology and should be transferred to Osmunda. Deng and Chen (2001) proposed that the differences between R. denticulata and O. cretacea were insufficient to distinguish each other and further suggested that R. denticulata should be reassigned to the Osmunda. Two other species, Osmunda sachalinensis and O. greenlandica, are reported from the Palaeocene Wuyun Formation in Jiayin of Heilongjiang Province (Tao and Xiong, 1986; Tao, 2000; Wang et al., 2006). Osmunda sachalinensis (Fig. 3D), a common element of the Palaeogene floras in Far-East region (e.g., Sakhalin, Primorye and Priamurye of Russia and Japan), is characterized by an expanded pinnule base (Kryshtofovich, 1936; Tanai, 1970; Ablaev, 1974, 1985; Kamaeva, 1990). In contrast, Osmunda greenlandica always shows a broadly cuneate pinnule base (Wang et al., 2006). Osmunda lignitum (Fig. 3A), a very common species of Eocene in Europe (Collinson, 2002; Kvaˇcek, 2002), resembles the living O. javanica and O. banksiifolia in leaf morphology (Florin, 1922; Zhi and Gu, 1978), which are nowadays widely distributed in southern and southeastern China (Wu, 1992; Wang and Wang, 2001). In China, Osmunda lignitum was documented from the late Eocene Guchengzi Formation in Fushun of Liaoning Province (Zhi and Gu, 1978) and the late Palaeocene to early Eocene Changchang Formation in Hainan Province (Guo, 1979). Geographically, these two fossil localities are far away from each other. It is thereafter inferred that this species was widely distributed throughout China territory during the Palaeocene to Eocene, though no fossils are found in the transition areas between the two remote localities. Osmunda totangensis, originally recognized from the Neogene of Duotang in Yunnan Province (Zhi and Gu, 1978), has also been found in the Late Miocene deposits in Tengchong of Yunnan (Tao, 2000). Osmunda totangensis is similar to O. lignitum in several characters; however, the lobe shape of the former is more anisomerous and smaller than that of the latter. The pinnule morphology of O. totangensis also resembles those of the extant O. banksiifolia, which nowadays is prosperous in Tengchong, the fossil locality of O. totangensis. 3.1.4. Genus Cladophlebis Brongniart Cladophlebis, a sterile fossil genus with large bipinnate Osmunda-like leaves, is considered to be possibly related to the Osmundaceae (Bodor and Babacka, 2008). The frond, pinnule, and venation characters of Cladophlebis are always similar

to those of Todites and Osmunda (Deng and Chen, 2001). Furthermore, Cladophlebis is sometimes found in association with other osmundalean fossils, e.g., Todites and Osmundopsis or permineralized rhizomes Ashicaulis and Millerocaulis (Vakhrameev and Hughes, 1991; Zhang and Zheng, 1991; Tidwell and Ash, 1994). However, with its highly homoplastic morphology, Cladophlebis might also represent the foliage of some other fern families (e.g., Cyatheaceae, Schizaeaceae, and Dennstaedtiaceae) (Villar de Seoane, 1996; Escapa and Cúneo, 2012). Thus, Cladophlebis should not be considered safely related to the Osmundaceae unless sporangium morphology and arrangement are known. With more than 240 described species, the genus shows a high diversity in geological time throughout the world (McLoughlin et al., 1995; Barbacka and Bodor, 2008; Bodor and Babacka, 2008). A recent report (Dai et al., 2012) also recognized a new species, Cladophlebis yonganensis Dai et Sun, from the Lower Cretaceous in Fujian Province, southeastern China. In China, the genus is extensively recorded in the Late Palaeozoic and Mesozoic deposits. The earliest record of Cladophlebis dates back to the Late Palaeozoic in northern China (e.g., Shanxi, Inner Mongolia, and Hebei provinces) (Gu and Zhi, 1974; Yang et al., 1994; Fig. 4A–C). During the Late Triassic, Cladophlebis was very common in both the NPP (e.g., the Yanchang Flora) and the SPP (e.g., the Baoding Flora, Hsüchiaho Flora, Yipinglang Flora, Lamaya Flora, and Shazhenxi Flora) (Deng and Chen, 2001). In the Jurassic, especially the Middle Jurassic, represented by C. denticulata, C. asiatica and C. gigantea (Fig. 4D, H), the genus Cladophlebis reached a remarkably high diversity in the NPP (Zhang et al., 1998). It showed a distinct decline in diversity at the end of the Early Cretaceous. Then, in the Late Cretaceous, only Cladophlebis sp. was found from the Qingshankou Formation in the Songliao Basin and Taipinglinchang Formation in Jiayin of Heilongjiang, NE China (Tao, 2000). Cenozoic records of Cladophlebis are rare, with only a few species (i.e., Cladophlebis septentrionalis, and Cladophlebis spp.) documented, from the Wuyun Formation in Jiayin of Heilongjiang (Zhang, 1983; Quan, 2005). 3.1.5. Genus Raphaelia Debey et Ettingshausen Raphaelia, erected by Debey and von Ettingshausen (1859), is another osmundalean fossil genus, represented by both sterile and fertile foliages (Tidwell and Ash, 1994). The genus is widely distributed in the Jurassic of Far-East region in Russia with over 12 species (Zhang et al., 1998). It is also extensively recorded from the Mesozoic (especially the Jurassic) deposits of China, represented by R. diamensis, R. stricta, R. prinadai, R. glossoides, R. aff. neuropteroides, and several undefined species (Table 1). Among these taxa, Raphaelia diamensis is the most significant representative (Figs. 2B, C, 5C, D). Krassilov (1978) proposed to transfer R. diamensis to the genus Osmunda, retaining its specific name, on the basis of the examination of fertile pinnules associated to sterile pinnae determined as R. diamensis (Krassilov, 1978; Phipps et al., 1998). However, Vakhrameev and Hughes (1991) considered this viewpoint to be premature. In addition, sporangium characters of many species of Raphaelia

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Fig. 4. Sketch drawing showing pinnule and venation characters of major Cladophlebis species in China. (A) C. manchurica (Kaw.) Gu et zhi, after Gu and Zhi (1974) and Yang et al. (1994); scale bar = 5 mm. (B) C. ozakii Yabe et Oishi, after Gu and Zhi (1974) and Yang et al. (1994); scale bar = 7 mm. (C) C.? yongwolensis (Kawasaki) Stockmans et Mathieu, after Gu and Zhi (1974) and Yang et al. (1994); scale bar = 1 cm. (D) C. gigantea Oishi, after Chen et al. (1984); scale bar = 9 mm. (E) C. raciborskii Yabe, after Sze (1956) and Yang et al. (1994); scale bar = 1 cm. (F) C. raciborskii Zeiller; scale bar = 2 cm. (G) C. delicatula Yabe et Oishi, after Chen et al. (1984); scale bar = 5 mm. (H) C. asiatica Chow et Yeh, after Chen et al. (1984); scale bar = 8 mm.

are not well preserved; it is therefore inadvisable to transfer all of them to Osmunda. Raphaelia diamensis is reported mainly from the NPP, including: the Lower Jurassic in Shaanxi and Gansu provinces; the Middle Jurassic in Liaoning, Beijing, Inner Mongolia, Xinjiang, and Qinghai provinces; the Upper Jurassic in Longzhaogou of Heilongjiang Province, and the Lower Cretaceous in the Boli Basin of Heilongjiang Province (Yang, 1977; Chen et al., 1980; Zhang et al., 1980; Ye and Li, 1982; Zheng and Zhang, 1982, 1983; Cao, 1984; Zhang and Zheng, 1987; Mei et al., 1989; Mi et al., 1996; Sun G. et al., 2004, 2010). Raphaelia stricta differs from R. diamensis by its narrow pinnules, which are inserted on the axis with the whole base (Mei et al., 1989). It has been reported from the Middle Jurassic of Liaoning and Inner Mongolia (Yang and Sun, 1985; Zhang and Zheng, 1987). Raphaelia prinadai was documented from the Middle Jurassic in Liaoning and Jilin provinces (Fig. 5E) (Yang and Sun, 1982a, b, 1985). Raphaelia glossoides was reported from the Middle Jurassic in Xinjiang (Zhang et al., 1998). Raphaelia aff. neuropteroides was described from the Middle Jurassic in Beijing (Chen et al., 1984). Several Raphaelia sp. were documented from the Middle Jurassic in the Qaidam and Shan-Gan-Ning basins, as well as the Lower Cretaceous in Liaoning and Jilin provinces (Zhang, 1987; Li et al., 1988; Mei et al., 1989). 3.1.6. Genus Tuarella Burakova The genus Tuarella Burakova was erected based on Middle Jurassic remains from Turkmenistan (Burakova, 1961). Worldwide, only two species have been referred to Tuarella, i.e., Tuarella lobifolia and T. petrovii (Burakova, 1961; Li

et al., 1988). Morphologically, the type species T. lobifolia is similar to Disorus nimakanensis Vachrameev in bearing two elongated sporangia under the two lateral pinnule margins (Fig. 5B); however, it differs from the latter by both the leaf base form and the in situ spore type (Vakhrameev and Doludenko, 1961). In fact, the in situ spores of T. lobifolia (size and exine ornamentation) resemble those of several osmundalean taxa, i.e., modern species Osmunda regalis and Middle Jurassic species Osmunda jurassica Kara-Mursa (Burakova, 1961). That is why Tuarella is ascribed to the Osmundaceae. In China, this genus is only represented by the type species T. lobifolia recorded from the Lower Jurassic in the Qaidam Basin, Qinghai (Fig. 5A, B) (Table 1) (Li et al., 1988). 3.2. Osmundalean rhizome fossils Permineralized osmundalean rhizomes have been extensively reported all over the world, representing a high proportion of the osmundalean fossils (Hewitson, 1962; Miller, 1971; Tian et al., 2008; Taylor et al., 2009). Such permineralized fossils play an important role in the classification of this fern lineage (Tidwell and Ash, 1994). Based on rhizomatous anatomical information, the order Osmundales is divided into two families: Osmundaceae and Guaireaceae. The family Osmundaceae is further separated into two subfamilies, i.e., the Thamnopteroideae and the Osmundoideae (Tidwell and Ash, 1994). The Thamnopteroideae, characterized by its protostele including seven morphogenera (Miller, 1971), might represent an otherwise unknown stock of osmundalean plants (Tidwell and Ash, 1994; Matsumoto et al., 2006). The Osmundoideae

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Fig. 5. Sketch drawing of representative species of morphogenera Raphaelia and Tuarella in China, showing frond pinnules and venation characters. (A, B) Tuarella lobifolia Burakova; (A) based on Li et al. (1988), pl. 19, fig. 1, scale bar = 1 cm; (B) fertile pinnule with two adaxial sporangia, after Li et al. (1988), scale bar = 2.5 mm. (C, D) Raphaelia diamensis Seward; (C) portion of the sterile frond, after Chen et al. (1984), scale bar = 5 mm; (D) detail of a sterile pinnule, after Chen et al. (1984); scale bar = 2.5 mm. (E) R. prinadai Vachrameev, after Chen et al. (1988); scale bar = 5 mm.

contains five rhizomatous morphogenera based on stem anatomy, such as Palaeosmunda, Ashicaulis, Millerocaulis, Osmundacaulis, and Aurealcaulis (Gould, 1970; Tidwell and Ash, 1994; Cheng and Li, 2007). The four living genera of the Osmundaceae are also attributed to the Osmundoideae (Tagawa, 1941; Miller, 1971). The family Guaireaceae now contains 7 genera, including Guairea, Lunea, Donwellicaulis, Itopsidema, Shuichengella, and the recently established Zhongmingella and Tiania (Wang et al., 2014a,b). Most of the evolutionary information about the order Osmundales and the family Osmundaceae comes largely from these structurally preserved rhizomes (Taylor et al., 2009). It is noted that some new insights on the systematic and phylogenetic relationship among members of Osmundales were provided recently by Wang et al. (2014a), who conducted a cladistic analysis of a broad range of Osmundales and related taxa on the basis of 18 extinct and 6 extant genera and subgenera. It was demonstrated that the Thamnopteroideae is not a subfamily of Osmundaceae as previously thought, and the Mesozoic osmundalean genus Osmundacaulis should be placed in the family Guaireaceae, rather than in Osmundaceae. In China, fossil taxa of both Osmundaceae and Guaireaceae have been

recorded with approximately 10 species belonging to 5 genera, i.e., Shuichengella, Zhongmingella, Tiania, Ashicaulis, and Millerocaulis (Li, 1983; Wang, 1983; Zhang and Zheng, 1991; Matsumoto et al., 2006; Cheng and Li, 2007; Cheng et al., 2007; Cheng, 2011; Tian et al., 2013, 2014a, b; Wang et al., 2014a, b; Table 1). Historically, there were several reports of Late Palaeozoic fern rhizomes referable to Palaeosmunda, including P. primitiva Li, P. plenasiosides Li, and P. yunnanense Tian et Chang (Li, 1983; Li and Cui, 1995). However, these early reports were later questioned and reinterpreted as Guaireaceae (Li, 1993; Tidwell and Ash, 1994; Wang et al., 2014a,b). As representatives of Guaireaceae, the genera Shuichengella, Zhongmingella, and Tiania were found only in China. Ashicaulis and Millerocaulis were well developed in the Middle Jurassic of China with a remarkable high diversity. In addition, some related fossil taxa from the Palaeozoic of China should be emphasized herein because they show relationships with the Osmundales. Rastropteris Galtier, Wang, Li et Hilton was erected based on permineralized material from the Lower Permian Taiyuan Formation in Hebei Province (Fig. 6A). The genus is established to accommodate a protostelic arborescent fern with mesarch maturation of the xylem

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Fig. 6. Sketch drawing showing the stem structures of permineralized osmundaceous rhizomes in China. (A) Rastropteris pingquanensis Galtier, Wang Li et Hilton, after Galtier et al. (2001); scale bar = 1 cm. (B) Shuichengella primitiva (Li) Li, based on Li (1993); scale bar = 8 mm. (C) Zhongmingella plenasioides (Li) Wang, Hilton, He, Seyfullah et Shao, portion of the transverse section of stem, after Li (1983); scale bar = 2 mm. (D) Millerocaulis sinica Cheng et Li, based on Cheng and Li (2007), pl. I, fig. c; scale bar = 1 mm. (E) Ashicaulis hebeiensis (Wang) Tidwell, based on Wang (1983), fig. 4; scale bar = 1 mm. (F) M. preosmunda Cheng, Wang et Li, based on Cheng et al. (2007), fig. 1(2); scale bar = 1 mm. (G) A. liaoningensis (Zhang et Zheng) Tidwell, after Zhang and Zheng (1991) and Tian et al. (2008); scale bar = 1 mm. (H) A. macromedullosus Matsumoto, Saiki, Zhang, Zheng et Wang, based on Matsumoto et al. (2006); scale bar = 1 mm. (I) A. beipiaoensis Tian, Wang, Zhang, Jiang et Dilcher, after Tian et al. (2013), fig. 5; scale bar = 1 mm.

and tangentially elongated, bar-shaped leaf traces (Galtier et al., 2001). Anatomical characters of Rastropteris, such as the solid homogeneous protostele, leaf trace with initially a single protoxylem and adaxially curved petiole xylem, indicate a close affinity to early members of the Osmundaceae (Galtier et al., 2001). It is believed that Rastropteris may be an intermediate between Grammatopteris and real catenalean ferns up to the Osmundaceae (Rößler and Galtier, 2002). 3.2.1. Genus Shuichengella Li The genus Shuichengella was erected based on reinvestigations of two anatomically preserved rhizomes which were originally described by Li (1983) as Palaeosmunda primitiva (Li, 1993) for its petiole bases bearing no stipule. This taxon is interpreted as structurally preserved stem of osmundalean plants, which possesses an ectophloic dictyoxylic siphonostele with mixed pith and a heterogeneous cortex without the mantle of leaf-bases and/or adventitious roots and sclerenchymatic sheaths of leaf traces (Li, 1993). This genus is represented

by only one species, Shuichengella primitiva (Li) Li collected from the Late Permian coal ball flora in Shuicheng of Guizhou Province, southwestern China (Li, 1983, 1993; Fig. 6B; Table 1). It is characterized by a mixed pith composed of parenchyma and tracheids, a C-shaped leaf trace, and petiole bases without stipular wings. Li (1993) thus proposed a new classification scheme for the Osmundaceae. According to his proposal, the whole family was divided into four subfamilies: Osmundoideae, Thamnopteroideae, Shuichengelloideae, and Guaireoideae (Li, 1993). Consequently, the Shuichengella was believed as a monotypic genus of the subfamily Shuichengelloideae. However, this classification scheme is not widely accepted. Later, the Shuichengella was recognized as a member of the osmundalean family Guaireaceae (Tidwell and Ash, 1994; Wang et al., 2014a). 3.2.2. Genus Zhongmingella Wang et al. Zhongmingella is a newly established genus based on the reinvestigation of an anatomically preserved stem, which was

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Fig. 7. Sketch drawing showing the petiolar structures of permineralized osmundaceous rhizomes in China. (A) Millerocaulis preosmunda Cheng, Wang et Li, after Cheng et al. (2007); scale bar = 2 mm. (B) M. sinica Cheng et Li, after Cheng and Li (2007); scale bar = 2 mm. (C) Ashicaulis macromedullosus Matsumoto, Saiki, Zhang, Zheng et Wang, after Matsumoto et al. (2006), fig. 3A; scale bar = 1 mm. (D) A. liaoningensis (Zhang et Zheng) Tidwell, after Zhang and Zheng (1991); scale bar = 2 mm. (E) A. hebeiensis (Wang) Tidwell, modified after Wang (1983); scale bar = 2 mm. (F) A. beipiaoensis Tian, Wang, Zhang, Jiang et Dilcher, after Tian et al. (2013), fig. 6A; scale bar = 2 mm.

previously documented by Li (1983) as Palaeosmunda plenasioides Li (Wang et al., 2014a). Specimen of Zhongmingella was collected from the same locality and horizon with Shuichengella (Li, 1983; Sun K.Q. et al., 2010; Wang et al., 2014a). The genus is represented by only one species Zhongmingella plenasioides (Li) Wang, Hilton, He, Seyfullah et Shao, which is preserved as a rhizomatous stem with dictyostelic stele, heterogeneous pith and cortex comprising parenchyma and uniformly distributed secretory cells (Fig. 6C) (Li, 1983; Wang et al., 2014a). Anatomical comparisons and results of a cladistic analysis both support to place the genus in the family Guaireaceae (Wang et al., 2014a). The reports of this distinct taxon as well as the Shuichengella markedly improve the anatomical diversity of the family Guaireaceae, and indicate that the family might have expanded its distribution range to the non-Gondwana regions. 3.2.3. Genus Tiania (Tian et Chang) Wang et al. The genus Tiania was erected very recently by Wang et al. (2014b) based on re-investigations of the original specimens of Palaeosmunda yunnanense Tian et Chang from the Late Permian Xuanwei Formation in Yunnan Province, SW China. It is demonstrated to represent another new genus within the Guaireaceae. The genus is represented by only one species T. yunnanense. The stem of T. yunnanense comprises an ectophloic siphonostele with no leaf gaps, a bilayered pith, and a unilayered cortex with numerous adaxially curved leaf traces. The document of Tiania in China provides further knowledge on the diversity of osmundalean ferns, especially the family Guaireaceae in the Late Permian of South China. Due to its siphonostele without leaf gaps, Tiania is interpreted as an evolutionary intermediate between the protostelic thamnopterids and the more advanced dictyostelic osmundaleans (Wang et al., 2014b).

3.2.4. Genus Millerocaulis Erasmus ex Tidwell emend. Tidwell Millerocaulis, Ashicaulis, and Osmundacaulis have been generally considered as the three most common Mesozoic rhizome genera of the Osmundaceae (Tidwell and Ash, 1994), though Wang et al. (2014a) suggested that Osmundacaulis may be more closely related to Guaireaceae. Their relationships have been discussed in detail by several authors (Tidwell, 1994; Tidwell and Ash, 1994; Tian et al., 2008; Wang et al., 2014a). Anatomically, Millerocaulis is characterized by an ectophloic siphonostele, a parenchymatous pith, and thick outer cortex with incomplete leaf gaps, and C-shaped leaf traces with endarch protoxylem (Tidwell, 1986, 1994). With 11 species described worldwide, the genus ranged from the Middle Triassic to the Early Cretaceous (Tidwell, 1986; Tian et al., 2008). Additionally, Vera (2012) described a new species (M. tekelili Vera) from the Aptian of Antarctic. However, this species would fall in the genus Ashicaulis in the classification scheme of Tidwell (1994). In China, two species have been described, i.e., Millerocaulis sinica (Figs. 6D, 7B) and M. preosmunda (Figs. 6F, 7A) from the Middle Jurassic Tiaojishan Formation in Beipiao of Liaoning Province (Cheng and Li, 2007; Cheng et al., 2007; Table 1). These two species are similar in many aspects, but differ from each other in the petiolar sclerotic ring and sclerenchyma arrangement in the stipular wings. It is noted that these two species are both characterized by heterogeneous sclerotic rings with sclerenchymatous fibers. 3.2.5. Genus Ashicaulis Tidwell As an osmundaceous rhizome genus, Ashicaulis is characterized by an ectophloic dictyoxylic siphonostele with definite leaf gaps (Tidwell, 1994). This taxon was separated from Millerocaulis for bearing numerous complete leaf gaps in the xylem

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Fig. 8. Permineralized osmundaceous rhizomes from the Middle Jurassic in western Liaoning Province, NE China. (A) Ashicaulis plumites Tian et Wang, showing a heterogeneous sclerotic ring and a huge sclerenchyma mass with outward protuberance; scale bar = 1 mm. (B) Ashicaulis n. sp. 1, showing a heterogeneous sclerotic ring and a huge sclerenchyma mass with outward protuberance; scale bar = 1 mm. (C) Ashicaulis n. sp. 2, showing heterogeneous sclerotic ring with the two lateral parts extremely expanded; scale bar = 1 mm. (D) Ashicaulis n. sp. 3, showing numerous scattered sclerenchymatous tissues in the petiolar cortex; scale bar = 1 mm. E. Ashicaulis n. sp. 4, showing numerous scattered sclerenchymatous tissues in the petiolar cortex; scale bar = 1 mm.

cylinder (Tidwell, 1994). This division has been widely accepted by many palaeobotanists (Cantrill, 1997; Matsumoto et al., 2006; Cheng, 2011; Tian et al., 2013, 2014a,b; Wang et al., 2014a), though controversy remains (Herbst, 2001, 2006; Vera, 2008). Totally, over 30 species are referred to this genus with a relative high latitude distribution in both hemispheres (Tian et al., 2008, 2013, 2014a,b; Cheng, 2011). Seven species of Ashicaulis have been described from China (Table 1), i.e., Ashicaulis hebeiensis, A. liaoningensis, A. macromedullosus, A. claytoniites, A. beipiaoensis, A. wangii, and A. plumites (Figs. 6E, G–I; 7C–F) (Wang, 1983; Zhang and Zheng, 1991; Matsumoto et al., 2006; Cheng, 2011; Tian et al., 2013, 2014a,b). Among these species, Ashicaulis macromedullosus, A. hebeiensis, and A. beipiaoensis are with a homogeneous petiolar sclerotic ring (Fig. 7C, E, F); however, Ashicaulis macromedullosus bears no sclerenchyma tissues in the trace concavity, whereas A. hebeiensis is distinct by having the lining sclerenchyma tissues in the petiolar vascular bundle concavity associated with sclerenchymatous clusters in the petiolar inner cortex (Fig. 7E). The rest four species are all with heterogeneous sclerotic rings. Ashicaulis liaoningensis and A. wangii differ from the other two species in having heterogeneous pith (Tian et al., 2014a; Fig. 7D). Ashicaulis plumites is characterized by a

unique mushroom-like scleremchyma mass in the petiolar vascular bundle concavity (Tian et al., 2014b; Fig. 8A). Ashicaulis claytoniites shows a special petiolar sclerenchyma arrangement (Cheng, 2011). It is noted that all these seven species are documented from the Middle Jurassic Tiaojishan Formation in Hebei and Liaoning provinces, northeastern China. Our recent investigations on the permineralized specimens from the Middle Jurassic in western Liaoning show a much higher anatomical diversity of osmundalean ferns than currently known, and over 11 additional species (including eight new species, will be published separately) of Ashicaulis may be recognized in this locality (Tian, 2011; Fig. 8B–E). Most of the Chinese materials of Ashicaulis have heterogeneous sclerotic rings, which differ from those taxa from the Southern Hemisphere. Some of the Chinese specimens show very specialized anatomical structures. For example, in one of the new species of Ashicaulis, the abaxial side of the sclerotic ring is composed of sclerenchymatous fibers with the two lateral parts extremely expanding to form a dumbbell-shape (Fig. 8C). However, compared with fossils from the Southern Hemisphere, most of the Chinese materials demonstrate less developed sclerenchymatous tissues in the petiolar cortex though some exceptions are present (Fig. 8D and E).

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Fig. 9. Stratigraphical records of osmundaceous fossils and species diversity variation through geological ages in China. Notes: 1) Fossil records of Cladophlebis are excluded in this figure; 2) The following number refers to different species listed in the figure: (1) Zhongmingella plenasioides (Li) Wang, Hilton, He, Seyfullah et Shao; (2) Shuichengella primitiva (Li) Li; (3) Tiania yunnanense (Tian et Chang) Wang et al.; (4) Todites shensiensis (P’an) Sze; (5) T. asianus Wu; (6) T. crenatum Barnard; (7) T. kwangyuanensis (Li) Ye et Chen; (8) T. microphylla (Fontaine) Li; (9) T. recurvatus Harris; (10) T. scoresbyensis Harris; (11) T. subtilis Duan et Chen; (12) T. yanbianensis Duan et Chen; (13) T. goeppertianus (Münster) Krasser; (14) T. princeps (Presl) Gothan; (15) T. williamsonii (Brongniart) Seward; (16) T. denticulatus (Brongniart) Krasser; (17) T. leei Wu; (18) T. nanjingensis Wang, Cao et Thévenard; (19) T. cf. thomasi Harris; (20) T. major Sun et Zheng; (21) Osmundopsis plectrophora Harris; (22) O. cf. plectrophora Harris; (23) O. jingyuanensis Liu; (24) O. sturii (Raciborski) Harris; (25) O. sp.; (26) O. sp.; (27) Tuarella lobifolia Burakova; (28) Millerocaulis sinica Cheng et Li; (29) M. preosmunda Cheng, Wang et Li; (30) Ashicaulis hebeiensis (Wang) Tidwell; (31) A. liaoningensis (Zhang et Zheng) Tidwell; (32) A. macromedullosus Matsumoto, Saiki, Zhang, Zheng et Wang; (33) A. claytonites Cheng; (34) A. beipiaoensis Tian, Wang, Zhang, Jiang et Dilcher; (35) A. wangii Tian et Wang; (36) A. plumites Tian et Wang; (37) Raphaelia diamensis Seward; (38) R. stricta Vachrameev; (39) R. glossoides Vachrameev; (40) R. prinadai Vachrameev; (41) R. aff. neuropteroides Debey et Ettingshausen; (42) R. sp. Li et al.; (43) R. sp. Mei et al.; (44) Raphaelia sp. Zhang; (45) R. sp. Zhang; (46) R. sp. Yang et al.; (47) Osmunda cretacea Samylina; (48) O. lignitum (Giebel) Stur.; (49) O. sachalinensis Kryshtofovich; (50) O. greenlandica (Heer) Brow.; (51) O. heeri Gaudin; (52) O. totangensis (Colani) Guo; (53) O. japonica Thunb.

4. Spatial and temporal distributions 4.1. Stratigraphical ranges Our analysis indicates that a total of more than 50 species referred to 10 genera of osmundalean fossils have been documented in China excluding the morphogenus Cladophlebis from this study (Fig. 9; Table 1). These fossil records demonstrate that the order Osmundales may have appeared in the Late Palaeozoic in China. It is noted that though Rastropteris was documented from the Lower Permian, fossils with unequivocal osmundalean anatomical characters were present in the Late Permian, represented by the Guaireaceae (i.e., Shuichengella, Zhongmingella and Tiania) (Li, 1993; Wang et al., 2014a,b). The Guaireaceae has a short stratigraphical range and became extinct at the end of Late Permian in China (Fig. 9). In China, all the Mesozoic records of Osmundales belonged to the family Osmundaceae (Fig. 9). During the early Mesozoic, especially the interval from the Early to Middle Triassic, rare fossil records have been reported and only a single species Todites shensiensis was described from the Middle Triassic (P’an, 1936; Wang et al., 2005). Additionally, some dispersed osmundalean spores (e.g., Osmundacidites sebectus) were reported from the Lower Triassic Heshanggou Formation and Middle Triassic Tongchuan Formation (Song et al., 2000). The Osmundaceae

reached its maximum diversity during the Late Triassic to the Middle Jurassic intervals with about 40 species (Fig. 9). In the Late Triassic, the Osmundaceae was represented mainly by two genera Todites (13 species) and Osmundopsis (2 species). Across the Triassic/Jurassic boundary, about 14 species of three genera (Todites, Osmundopsis and Raphaelia) were recorded in the Early Jurassic (Fig. 9). Todites remained quite common with about six species, three of which (Todites leei, T. nanjingensis, T. cf. thomasi) first appeared in the Early Jurassic (Fig. 9). Osmundopsis showed a relatively higher diversity with up to 5 species in the Early Jurassic, but became extinct at the end of the Early Jurassic in China (Fig. 9). In this time interval, the genus Raphaelia, appeared for the first time with one species R. diamensis. In the Middle Jurassic, the species diversity of Todites declines sharply to only four species (Fig. 9). In contrast, Raphaelia reaches its maximum in diversity up to seven species. Some diverse new taxa occurred for the first time in this interval (Fig. 9), such as Tuarella (1 species), Ashicaulis (7 species), and Millerocaulis (2 species). During the Middle to Late Jurassic transition, the species diversity declines rapidly from 21 species in the Middle Jurassic to only three species in the Late Jurassic (Fig. 9). In particular, the three taxa including Tuarella, Ashicaulis, and Millerocaulis became extinct in China at the end of Jurassic.

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Fig. 10. Sketch map showing the geographical distribution of osmundaceous fossils in China. Notes: The symbols refer to different species, and the color indicates different ages; Fossil localities of Cladophlebis are not included in the figure; P1 = Early Permian; P3 = Late Permian; T2 = Middle Triassic; T3 = Late Triassic; J1 = Early Jurassic; J2 = Middle Jurassic; J3 = Late Jurassic; K1 = Early Cretaceous; K2 = Late Cretaceous; Pa = Palaeogene; E = Neogene.

In the Early Cretaceous, only four osmundalean species were found (Fig. 9). Among them, the genus Osmunda became an important element during the Early Cretaceous in China. Todites and Raphaelia were extinct at the end of the Early Cretaceous. To date, there is no unequivocal osmundalean record in the Late Cretaceous interval, though Cladophlebis spp. was reported from the Taipinglinchang Formation in Jiayin of Heilongjiang Province, NE China (Quan, 2005). In the Cenozoic, all fossil records of Osmundaceae were ascribed to extant genus Osmunda with six species (Fig. 9). Several Cladophlebis species were documented from the Palaeocene Wuyun Formation in Jiayin, Heilongjiang Province, NE China (Tao, 2000). 4.2. Palaeogeographical distribution Geographically, the Osmundaceae shows an extensive distribution in the whole territory of China (Fig. 10). However, the geographical distribution pattern varies through time. During the Late Palaeozoic, probable osmundalean representatives (Rastropteris and Cladophlebis) were documented mostly from northern China, such as Shaanxi and Hebei provinces. In contrast, definite osmundalean rhizome taxa (Shuichengella, Zhongmingella and Tiania) were reported from Guizhou and Yunnan provinces, SW China (Fig. 10).

During the Early–Middle Triassic, marine depositions were dominant in southern China; whereas the terrestrial sediments were well developed in northern China (Liu and Quan, 1995). However, hardly any Early Triassic fossils were found in northern China due to the dry climate (Sun et al., 1995b). Though the Middle Triassic floras in northern China were relatively more developed than those in the Early Triassic (Sun et al., 1995b), osmundalean fossil records were still poor, and only Todites shensiensis was reported in Shaanxi, Inner Mongolia, and Liaoning provinces, northern China (Fig. 10). From the Late Triassic, the geotectonic framework of China greatly influenced Indo-China Movement, and afterwards continental deposits developed extensively throughout China territory except parts of Tibet (Liu and Quan, 1995). During the Late Triassic, the SPP was the dominant region for the distribution of the Osmundaceae with over 20 fossil localities (e.g., Sichuan, Yunnan, Chongqing, and Hubei provinces); in contrast, only five fossil sites were found in the NPP, including Liaoning, Jilin, Hebei, and Shaanxi provinces (Fig. 10). For the Early Jurassic, five localities were reported in the NPP (i.e., Heilongjiang, Liaoning, Hebei, Gansu, and Qinghai provinces), whereas about 11 localities were recorded in the SPP, especially the middle-lower Yangtze Blocks (e.g., Hubei, Anhui, and Jiangsu provinces). It is noteworthy that almost all Middle Jurassic osmundalean fossils were found from the NPP (Fig. 10), no osmundalean taxa

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were documented from the SPP during the Middle Jurassic to the Late Cretaceous (Fig. 10). Osmundalean ferns were restricted to NE China from the Late Jurassic to the Early Cretaceous (Fig. 10). Todites major, documented from the Yixian Formation in Beipiao of Liaoning Province, is proposed to be the latest fossil record of Todites in China. Osmunda cretacea is geographically restricted to NE China, such as Inner Mongolia, Liaoning, and Jilin provinces (Fig. 10). The Cenozoic osmundalean ferns were scattered in Heilongjiang and Liaoning provinces of northern China as well as Yunnan and Hainan provinces of southern China (Fig. 10). 5. Discussion Though osmundalean fossils are extensively reported worldwide, some gaps remain in its evolutionary history (Taylor et al., 2009). As already addressed, Chinese fossil records cover almost all important stages in the macroevolution of Osmundales; therefore a comprehensive analysis on these data will contribute to further understanding of the evolutionary trend of this fern lineage. Molecular analysis reveals that the Osmundaceae might have arisen in the Late Carboniferous, and then experienced a rapid diversification until the Early Permian (Pryer et al., 2004; Schuettpelz et al., 2006; Schuettpelz and Pryer, 2007). The fern genus Grammatopteris reported from the Lower Permian of Europe might be the earliest record of the early osmundalean plants (Renault, 1896; Beck, 1920; Galtier et al., 2001), though it is still controversial. The occurrence of Rastropteris, Shuichengella, Zhongmingella, and Tiania in China implies that China is one of the diversification centers for osmundalean ferns during the Late Palaeozoic, and indicates the order Osmundales has got a considerable range extension in both Northern and Southern Hemispheres during the Late Permian. Fossil evidence shows that evolution of Osmundales proceeded rapidly during the Late Palaeozoic and Early Mesozoic time (Miller, 1971). The time interval between the Late Triassic to the Middle Jurassic is the flourishing period for this order in China. Schuettpelz and Pryer (2009) suggested that the diversification of osmundalean ferns happened near the Triassic–Jurassic transition, when the earliest representatives of the crown group are recorded. This view is supported by the occurrences of abundant osmundalean fossil records in both northern and southern China. Cenozoic osmundalean fossils show close similarities in leaf morphology to the extant osmundalean taxa in East Asia, demonstrating a low evolutionary rate. This is in accordance with the low diversification rate of Osmundaceae proposed by Schuettpelz and Pryer (2009). It is commonly believed that most living osmundalean ferns were derived from genera Millerocaulis and Ashicaulis (Tidwell and Ash, 1994). However, evolutionary relationships among them remain poorly known due to the lack of sufficient intermediate forms. We know that most of extant osmundalean ferns are characterized by bearing heterogeneous petiolar sclerotic rings. However, most of the Mesozoic Millerocaulis and Ashicaulis species, especially those from the Southern Hemisphere, always bear a homogeneous sclerotic ring. On the contrary, the most anatomically preserved fossil rhizomes from the Middle Jurassic

of China yield typical heterogeneous petiolar sclerotic rings. Thus, these Chinese fossil materials show a real potential to bridge the evolutionary gap of Osmundales. Recent encouraging progresses from China proposed that M. preosmunda and M. sinica be closely related with living Osmunda subgenus Osmunda (Cheng and Li, 2007; Cheng et al., 2007). Ashicaulis claytoniites is treated as a close relative to the extant O. claytoniana (Cheng, 2011). Yatabe et al. (2005) suggested to divide the subgenus Osmunda into subgenus Osmunda and subgenus Claytosmunda (Metzgar et al., 2008). On this account, Osmunda claytoniana is more related to the subgenus Claytosmunda. Ashicaulis hebeiensis is considered to be related to living Osmunda subgenus Plenasium (Wang, 1983). However, its leaf trace vascular bundle does not show two protoxylem clusters when departing from the stele, which is a key feature for the subgenus Plenasium. Ashicaulis beipiaoensis bears close similarities to Osmunda shimokawaensis from the Middle Miocene of Hokkaido, Japan. They may represent an extinct branch in the Osmundaceae evolutionary tree (Tian et al., 2013). In addition, Ashicaulis wangii and A. plumites, show remarkable anatomical resemblances to the Palaeocene Osmunda pluma, as well as to several taxa of extant Osmunda subgenus Osmunda (Tian et al., 2014a, b). Our recent investigation shows that osmundalean rhizomes have a high structural and species diversity (17 species) in the Middle Jurassic of western Liaoning (Tian, 2011). Detailed studies on these fossils will make it possible to provide further evidence for understanding the evolutionary lines between the Mesozoic members and the living Osmundaceae. Osmundalean fossils from northeastern China region are quite abundant since the Middle Jurassic, represented by diverse species, such as Todites, Ashicaulis, and Millerocaulis (Middle Jurassic), Raphaelia and Osmunda cretacea (Early Cretaceous), O. wuyunensis and O. greenides (Palaeocene), as well as O. lignitum (Eocene). These continuous fossil records provide links for understanding the Cenozoic diversity variation and evolution of the Osmundaceae in East Asia. Obviously, there are also considerable occurrences of the Cenozoic osmundalean rhizome and foliage fossils in other regions of the world (i.e., Slovakia, Hungary, Washington of USA, and Trimmelkam of Austria) (Miller, 1967, 1971). Together with the above-mentioned regions, northeastern China is proposed to act as one of the refuges for osmundalean ferns, and plays a significant role in preserving the gene bank for extant osmundalean ferns in East Asia. 6. Concluding remarks 1) This study provides for the first time a systematic overview on the diversity variation and distribution pattern of the fossil Osmundales in China. 2) Our analysis indicates that totally more than 50 species of 10 genera of osmundalean fossils have been documented in China excluding the morphogenus Cladophlebis. Geographically, they have been reported in both Northern and Southern China phytoprovinces, though these taxa show variations in geographical ranges. 3) The Osmundales are first recorded in China in the Late Palaeozoic. Representatives with unequivocal osmundalean

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anatomical structures are reported from the Late Permian, represented by Guaireaceae. The Late Triassic to Middle Jurassic interval represents a period of radiation for osmundaceous ferns. From the Late Jurassic onwards, fossil diversity declines rapidly. Cenozoic taxa are represented only by several relictual Osmunda species. 4) Chinese fossil records cover almost all important stages for the macroevolution of the Osmundales, e.g., the origin, radiation, decline and relic, and contribute to further understanding of evolutionary lines of this peculiar fern lineage. Acknowledgements We thank Prof. Ge Sun (Shenyang), Prof. Xiang-Wu Wu (Nanjing), Prof. Sheng-Hui Deng (Beijing), and Dr. Yu-Yan Miao (Beijing) for helpful discussion and courtesy for fossil photos. We are grateful to Dr. Mihai Popa (Bucharest) and Prof. Shi-Jun Wang (Beijing) for their kind reviews on the manuscript. Special thanks are due to Dr. M. Philippe (Lyon) and Dr. E.I. Vera (Buenos Aires) for their constructive comments for the earlier version of the manuscript. This study was jointly supported by State Key Programme of Basic Research of Ministry of Science and Technology, China (Grant No. 2012CB822003), the National Natural Science Foundation of China (Grant No. 41302004), the Innovation Project of CAS (Grant No. KZCX2-YW-154), the Team Program of Scientific Innovation and Interdisciplinary Cooperation of CAS, the State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS) (Grant No. 133113), Science Research Project of Liaoning Provincial Education Department (Grant No. L2012391) and the Talent Fund of Shenyang Normal University (Grant No. 91400114006).

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Please cite this article in press as: Tian, N., et al., A systematic overview of fossil osmundalean ferns in China: Diversity variation, distribution pattern, and evolutionary implications. Palaeoworld (2015), http://dx.doi.org/10.1016/j.palwor.2015.05.005