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A systematic overview of fossil osmundalean ferns in China: Diversity

variation, distribution pattern, and evolutionary implications

a,f,g b,c,∗ d b e

Ning Tian , Yong-Dong Wang , Man Dong , Li-Qin Li , Zi-Kun Jiang

a

College of Palaeontology, Shenyang Normal University, Shenyang 110034, China

b

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

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 2006; Schuettpelz and Pryer, 2007; Hennequin et al., 2008).

The extant Osmundales are represented mainly by four genera

Osmundales, a unique group among the oldest existing ferns, within the family Osmundaceae, including Osmunda, Todea,

consist of two major lineages, including the extinct family Leptopteris, and Osmundastrum (Metzgar et al., 2008). The

Guaireaceae and the family Osmundaceae with both living and extensive fossil records show, however, that this order had a

fossil representatives. This fern clade is generally considered much greater distribution and higher diversification in the geo-

as an intermediate between eusporangiate and leptosporan- logical past (Banerji, 1992; Ash and Morales, 1993; Tidwell and

giate ferns (Tidwell and Ash, 1994). It is proposed to be the Ash, 1994; Kiritchkova et al., 1999; Collinson, 2001; Bodor and

stem-group of the Polypodioidae and sister to the remaining lin- Barbacka, 2008; Taylor et al., 2009). Among these records, over

eages of leptosporangiate ferns based on phylogenetic analyses 80 species ascribed to 14 genera of fossil osmundalean rhizomes

(Hasebe et al., 1995; Pryer et al., 2001, 2004; Schuettpelz et al., 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

∗

Corresponding author: Nanjing Institute of Geology and Palaeontology, Chi-

and Osmundastrum mainly in southern China (Wu, 1992; Wang

nese Academy of Sciences, Nanjing 210008, China. Tel.: +86 25 8328 2221;

and Wang, 2001); as a contrast, abundant fossil osmundalean

fax: +86 25 8335 7026.

taxa have been reported from the Palaeozoic to the Cenozoic

E-mail address: [email protected] (Y.D. Wang).

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.

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

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2 N. Tian et al. / Palaeoworld xxx (2015) xxx–xxx

deposits. A couple of such fossil taxa have been investigated Burakova (Wang et al., 2005; Deng, 2007). Some other foliage

in some details, e.g., Todites and fossil rhizomes (Wang et al., taxa referable to the Osmundales have never been documented

2005; Tian, 2011). However, the diversification and distribution in China so far, such as Anomopteris Brongn., Phyllopteroides

features of this fern group are still scarcely considered. Medwell, and Cacumen Cantrill et Webb (Cantrill and Webb,

In this paper, we review the fossil osmundalean ferns in 1987; Banerji, 1992; Cantrill and Nagalingum, 2005; Taylor

China on the basis of known fossil records, with an emphasis et al., 2009).

on its diversity variations, distribution patterns, and evolutionary Osmundaceous pinnae are generally characterized by a

implications. The scope of this review focuses mainly on macro- pinniform venation; however, several specimens with simple

fossil with an exclusion of these osmundalean dispersed spores. reticulated veins were previously assigned to the Osmundaceae

This represents the first comprehensive analysis and overview (Osmundales) in China, such as Abropteris yongrenensis Li et

on the osmundalean fossils in China, and provides new clues Tsao and Reteophlebis simplex Li et Tsao (Li et al., 1976; Wu,

for understanding the origin, radiation, and development of this 1982). In fact, Reteophlebis simplex is a synonym of Cynepteris

fern lineage. lasiophora Ash, which was first reported from the Upper Tri-

assic Chinle Formation of New Mexico, USA (Ye et al., 1986).

2. Materials and methods The latter was ascribed to a well-defined family Cynepteridaceae

(Ash, 1970). The systematic affinity of Abropteris yongrenensis

Materials for this study involve all available published data remains poorly understood. However, it shows a close similar-

concerning fossil Osmundales in China, such as research papers, ity to Reteophlebis simplex (C. lasiophora) in many characters,

monographs and atlases of fossil plants. These fossils mainly fall and may represent an otherwise unknown stock of cynepterida-

into two types, i.e., compression/impression foliage and per- ceous plants. It is noted that the Cynepteridaceae is proposed to

mineralized rhizome. For each type of the data, the systematic be closely related to the fern family Schizaeaceae (Ash, 1970;

attribution, geographical origin, and geological source are com- Axsmith, 2009).

piled. Fossil locality information is plotted in a geographical

map to show the distribution patterns. The stratigraphic data 3.1.1. Genus Todites Seward emend. Harris

are arranged into a time framework, e.g., Early Permian (P1), The genus Todites was erected by Seward (1900) based on

Late Permian (P2), Early Triassic (T1), Middle Triassic (T2), materials from Yorkshire, and was then emended by Harris

etc. on the basis of up-dated biostratigraphic evidence. Selected (1961). It was named for fossil leaves that morphologically

sketch drawings and illustrations of some representative fossil resemble the extant Todea. The sporangia of Todites are always

taxa referred to the Osmundales are given, based on figures, borne along the veins on the dorsal side of the fertile pinnae,

plates, and descriptions from the original publications. which are morphologically similar to the vegetative ones

(Harris, 1961; Wang et al., 2005). The annulus of Todites is

3. Fossil record and diversity of Osmundalean ferns in always strongly apical, covering the entire apical region of

China the sporangium (Harris, 1961; Hewitson, 1962). Todites first

appeared in the Late Permian, with fertile pinnae bearing in

Our general analysis indicates that the earliest record of situ spores from the Upper Permian in Russia (Radcenko,ˇ

Osmundales in China dates back to the Late Palaeozoic (Gu and 1955; Naugolnykh, 2002). It is the most common genus

Zhi, 1974; Li, 1983). During the Mesozoic, the China territory of the Mesozoic osmundaceous plants in China, and about

is divided into two phytoprovinces, i.e., the Northern Phyto- 17 species have been reported (Wang et al., 2005), mainly

province (NPP) and Southern Phytoprovince (SPP), delimited by represented by T. shensiensis, T. denticulatus, T. goeppertianus,

the Kunlun-Qinling-Dabie Mountain Range (Sun et al., 1995a,b; T. williamsonii, T. princeps, and T. scorebyensis (Fig. 1). The

Zhou, 1995). Osmundalean ferns flourished with a high diversity earliest fossil record of Todites in China is from the Middle

in both phytoprovinces during the Mesozoic. Several Cenozoic Triassic (e.g., Todites shensiensis from the Middle Triassic of

fossil taxa of the family are also reported. The following is a Shaanxi and Inner Mongolia) (Sze, 1956; Zhang, 1976; Huang

summary for the diverse type of osmundalean fossils in China. and Zhou, 1980). The genus flourished during the Late Triassic

to the Middle Jurassic, but declined rapidly during the Late

3.1. Osmundalean leaf fossils Jurassic with only one species recorded (T. denticulatus). The

Cretaceous taxon of Todites in China is limited to T. major,

The foliage fossils of the Osmundales are not well studied described from the Lower Cretaceous Yixian Formation in

systematically due to the commonly poor preservation and fre- western Liaoning Province, NE China (Sun et al., 2001).

quent absence of fertile characters. As a result, numerous frond Geographically, Todites is widely distributed in both the NPP

fossils are recognized only as “Osmunda-like” fossil morpho- and SPP (Wang et al., 2005). During the Middle Triassic, almost

genera (Brongniart, 1849; Taylor et al., 1990; Collinson, 2001; all species are restricted to the NPP; however, in the interval from

Van Konijnenburg-Van Cittert, 2002). In China, osmundaceous the Late Triassic to the Early Jurassic, the species diversity is

foliage fossils are very common, represented mostly by Todites much higher in the SPP than that in the NPP. In the Middle

(Seward) Harris, Osmundopsis (Harris) Harris and Osmunda Jurassic, almost all Todites are reported from the NPP again.

Linnaeus, as well as three other genera including Cladophlebis The genus became extinct at the end of the Early Cretaceous in

Brongniart, Raphaelia Debey et Ettingshausen, and Tuarella 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 a natural taxon combining the pinnule morphology of Osmunda

thomasi, T. denticulatus, T. williamsoni, and T. princeps) were (i.e., reduced laminae in fertile zones) with a sporangial mor-

previously investigated in detail (Harris, 1931, 1961; Couper, phology closer to that of the genus Todea.

1958; Van Konijnenburg-Van Cittert, 1978). Couper (1958) In China, Osmundopsis fossils are not as common as Todites,

demonstrated that the in situ spores of Todites williamsonii and and only six species are documented, ranging from the Late Tri-

T. princeps were well correlated with the type specimen of dis- assic to the Early Jurassic (Table 1). Among them, Osmundopsis

persed spore Todisporites major. Tralau (1968) correlated the plectrophora Harris shows a widespread range and is reported

in situ spores of T. denticulatus to Todisporites cladothecoides. from the Late Triassic Hsüchiaho Formation in the Sichuan

Unfortunately, so far, no records of in situ spores of Todites have Basin (Ye et al., 1986; Wu, 1999), the Shazhenxi Formation

been reported in China. in Hunan Province (He and Shen, 1980; Zhang, 1982), as well

as from the Lower Jurassic in Gansu (Yang and Shen, 1988) and

3.1.2. Genus Osmundopsis Harris emend. Harris Inner Mongolia (Mei et al., 1989).

Osmundopsis, characterized by dimorphic fertile and sterile As the type species of the genus, Osmundopsis sturii bears

leaves, is another important Mesozoic genus of osmundalean delicate branches covered by obovate sporangia, each with a

ferns (Harris, 1961; Van Konijnenburg-Van Cittert, 1996; thickened distal cap (Fig. 2D, E). In China, this species has been

Naugolnykh, 2002). It was initially established by Harris described from the Early Jurassic Hsiangchi Formation in Zigui

(1931) for dimorphic tripinnate cladophleboid foliage bearing of Hubei (Wu, 1991) and from the Middle Jurassic Xishanyao

Osmunda-like fertile foliage but was later emended to also Formation in Shaerhu coal field of Xinjiang (Dong and Sun,

include bipinnate ones (Harris, 1961). The fertile leaves of 2011). However, re-examination of the fossil specimens from the

Osmundopsis are commonly lanceolate, bipinnate or tripinnate Hsiangchi Formation, which was previously described by Wu

with filiform ultimate branches, and bear groups of sporangia (1991) as cf. Osmundopsis sturii, indicated that they are fertile

(Harris, 1961). The sporangium of Osmundopsis is featured pinnae of Todites (probably T. williamsonii) (Wang, 2002).

by an apical annulus, which always covers the entire apical Osmundopsis jingyuanensis Liu has been documented from

region of the sporangium (Harris, 1961; Phipps et al., 1998). the Lower Jurassic Daolengshan Formation in Jingyuan of

The genus differs from Osmunda in the sporangium apical scle- Gansu Province (Liu, 1982). In addition, two undefined species

rotic cell size (Harris, 1961; Ye et al., 1986). Osmundopsis was referred to Osmundopsis were reported from the Lower Jurassic

previously considered to be an intermediate between Todites in Anhui and Beijing, respectively (Duan, 1987; Huang, 1988).

and Osmunda (Miller, 1971; Van Konijnenburg-Van Cittert, The in situ spores of the Osmundopsis were investigated by

1978). A recent study (Escapa and Cúneo, 2012) suggested that several authors (e.g., Harris, 1931, 1961; Couper, 1958; Van

Osmundopsis should be referred to a non-leptopteroid para- Konijnenburg-Van Cittert, 1978, 1996). The in situ spores of O.

phyletic group (Osmunda and Osmundastrum) and represents 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 Locality Formation Age References

Osmundopsis Harris emend. Harris

O. plectrophora Harris Tieshan of Hsüchiaho Late Triassic Ye et al., 1986; Wu, 1999;

Daxian, Sichuan Formation Sun K.Q. et al., 2010

Wenquan of Hsüchiaho Late Triassic Ye et al., 1986; Sun K.Q.

Kaixian, Formation et al., 2010

Chongqing

Lanzhou, Gansu Daxigou Early Jurassic Yang and Shen, 1988

Formation

Gouyadong of Xiaoping Late Triassic Feng et al., 1977; Sun K.Q.

Lechang, Formation et al., 2010

Guangdong

Changyou Banner, South Tulesu Early Jurassic Mei et al., 1989

Inner Mongolia Formation

Yizhang of Hunan Shazhenxi Late Triassic He and Shen, 1980; Zhang,

Formation 1982, 1986

O. cf. plectrophora Harris Tieshan of Hsüchiaho Late Triassic Wu, 1999

Daxian, Sichuan Formation

O. jingyuanensis Liu Jingyuan, Gansu Daolengshan Early Jurassic Liu, 1982; Zhang et al., 1998

Formation

O. sturii (Raciborski) Harris Shaerhu coal field Xishanyao Middle Jurassic Dong and Sun, 2011

of Xinjiang Formation

O. sp. Zhaitang of Yaopo Formation Middle Jurassic Duan, 1987

Western Hills,

Beijing

O. sp. Lalijian of Wuchang Early Jurassic Huang, 1988

Huaining, Anhui Formation

Osmunda Linnaeus

O. cretacea Samylina Jiaohe, Jilin Shansong Early Cretaceous Li et al., 1986

Formation

Huolinhe Basin, Huolinhe Early Cretaceous Deng, 1995

Inner Mongolia Formation

Tiefa Basin, Xiaoming’anbei Early Cretaceous Chen et al., 1988

Liaoning Formation

Fuxin Basin, Fuxin Formation Early Cretaceous Chen et al., 1988

Liaoning

Hailar Basin, Damoguaihe Early Cretaceous Deng et al., 1997

Inner Mongolia Formation

O. sachalinensis Kryshtofovich Jiayin, Wuyun Formation Paleocene Wang et al., 2006

Heilongjiang

O. greenlandica (Heer) Brown Jiayin, Wuyun Formation Paleocene Tao and Xiong, 1986

Heilongjiang

O. lignitum (Giebel) Stur. Fushun, Liaoning Guchengzi Late Eocene Zhi and Gu, 1978

Formation

Changchang Changchang Late Paleocene to Guo, 1979

Basin, Hainan Formation Early Eocene

O. totangensis (Colani) Guo Duotang of ? Miocene to Zhi and Gu, 1978

Kunming, Yunnan Pliocene

O. japonica Thunb. Lianghe Basin of ? Late Miocene Tao, 2000 Tengchong,

Yunnan

O. heeri Gaudin Shangzhi, Dalianhe Eocene Zhang et al., 1980

Heilongjiang Formation

Raphaelia Debey et Ettingshausen

R. diamensis Seward Diam River of Xishanyao Middle Jurassic Gu, 1984

Hefeng County, Formation

Xinjiang

Junggar Basin, Xishanyao Middle Jurassic Sun G. et al., 2010

Xinjiang Formation

Central Shaanxi, Yan’an Formation Early Jurassic Mi et al., 1996

and eastern Gansu

Beipiao, Liaoning Haifanggou Middle Jurassic Zhang et al., 1980; Zhang and

Formation Zheng, 1987

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Table 1 (Continued)

Species Locality Formation Age References

Aru Horqin of Xinmin Formation Middle Jurassic Zhang et al., 1980

Chifeng, Inner

Mongolia

Mishan, Yunshan Late Jurassic Zheng and Zhang, 1982

Heilongjiang Formation of Longzhaogou

Group

Heilongjiang Qihulin Formation Middle Jurassic Cao, 1984

Hegang, Dongshan Early Cretaceous Zheng and Zhang, 1983

Heilongjiang Formation

Wanbao of Wanbao Middle Jurassic Mei et al., 1989

Yao’an, Jilin Formation

Dayangtougou of Dameigou Early Middle Li et al., 1988

Qaidam Basin, Formation Jurassic

Qinghai

Dameigou of Yinmagou Early Middle Li et al., 1988

Qaidam Basin, Formation Jurassic

Qinghai

Mentougou, Xiayaopo Middle Jurassic Chen et al., 1980

Beijing Formation

Gaotouyao of Zhiluo Formation Late Middle Ye and Li, 1982; Zhou, 1995

Dalateqi, Inner Jurassic

Mongolia

Hami, Xinjiang Xishanyao Middle Jurassic Zhang et al., 1998

Formation

Shenmu, Shaanxi Fuxian Formation Early Jurassic Huang and Zhou, 1980

Jungar Banner, Fuxian Formation Early Jurassic Huang and Zhou, 1980

Inner Mongolia

Datong, Shanxi Datong Formation Middle Jurassic Wang, 1984

Xiahuayuan of Mentougou Middle Jurassic Wang, 1984 Zhangjiakou, Formation

Hebei

R. prinadai Vachrameev Yingcheng of Shahezi Late Jurassic? Yang and Sun, 1982a,b

Jiutai, Jilin Formation

Changtu of Huoshiling Late Jurassic Yang and Sun, 1982a,b

Liaoning, and Formation

Jiutai of Jilin

R. stricta Vachrameev Changheyingzi, Tiaojishan Middle Jurassic Zhang and Zheng, 1987

Laimayingzi, and Formation

Shebudai of

Beipiao, Liaoning

Xishala of Wanbao Middle Jurassic Yang and Sun, 1985

Zhuluteqi, Inner Formation

Mongolia

Haifanggou of Haifanggou Middle Jurassic Zhang and Zheng, 1987

Beipiao, Liaoning Formation

R. glossoides Vachrameev Kelasu River of Kezilenuer Middle Jurassic Zhang et al., 1998

Kuqa, Xinjiang Formation

Shanshan, Xishanyao Middle Jurassic Zhang et al., 1998

Xinjiang Formation

Kuisu coal mine, Xishanyao Middle Jurassic Zhang et al., 1998 northeastern Formation

Xinjiang

R. aff. neuropteroides Debey et Da’anshan of Upper Yaopo Middle Jurassic Chen et al., 1984

Ettingshausen Beijing Formation

R. sp. North Qaidam Dameigou Middle Jurassic Li et al., 1988

Basin, Qinghai Formation

R. sp. Shan-Gan-Ning Fuxian Formation Middle Jurassic Mei et al., 1989

Basin

R. sp. Fuxin, Liaoning Fuxin Formation Early Cretaceous Zhang, 1987

R. sp. Yingcheng, Jilin Yingcheng Early Cretaceous Zhang, 1987

Formation

R. sp. Changtu of Huoshiling Late Jurassic Yang and Sun, 1982b

Liaoning, and Formation

Jiutai of Jilin

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Table 1 (Continued)

Species Locality Formation Age References

Tuarella Burakova

T. lobifolia Burakova Qaidam Basin, Dameigou Middle Jurassic Li et al., 1988

Qinghai Formation

Millerocaulis Erasmus ex Tidwell emend. Tidwell

M. sinica Cheng et Li Beipiao, Liaoning Tiaojishan Middle Jurassic Cheng and Li, 2007

Formation

M. preosmunda Cheng, Wang et Li Beipiao, Liaoning Tiaojishan Middle Jurassic Cheng et al., 2007 Formation

Ashicaulis Tidwell

A. hebeiensis (Wang) Tidwell Zhuolu, Hebei Tiaojishan Middle Jurassic Wang, 1983

Formation

A. liaoningensis (Zhang et Zheng) Tidwell Beipiao, Liaoning Tiaojishan Middle Jurassic Zhang and Zheng, 1991

Formation

A. macromedullus Matsumoto, Saiki, Zhang, Zhuolu, Hebei Tiaojishan Middle Jurassic Matsumoto et al., 2006

Zheng et Wang Formation

A. claytonites Cheng Beipiao, Liaoning Tiaojishan Middle Jurassic Cheng, 2011

Formation

A. beipiaoensis Tian, Wang, Zhang, Jiang et Beipiao, Liaoning Tiaojishan Middle Jurassic Tian et al., 2013

Dilcher Formation

A. wangii Tian et Wang Beipiao, Liaoning Tiaojishan Middle Jurassic Tian et al., 2014a

Formation

A. plumites Tian et Wang Beipiao, Liaoning Tiaojishan Middle Jurassic Tian et al., 2014b Formation

Shuichengella Li

Shuichengella primitiva (Li) Li Shuicheng, Wangjiazhai Late Permian Li, 1983, 1993

Guizhou Formation

Zhongmingella Wang, Hilton, He, Seyfullah et Shao

Zhongmingella plenasioides (Li) Wang et al. Shuicheng, Wangjiazhai Late Permian Li, 1983; Wang et al., 2014a

Guizhou Formation

Tiania (Tian et Chang) Wang et al.

T. yunnanense (Tian et Chang) Wang et al. Xuanwei, Yunnan Xuanwei Late Permian Li and Cui, 1995; Wang et al.,

Formation 2014b

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 Cúneo, 2012). In this sense, most of the anatomically unpre-

Konijnenburg-Van Cittert (1978) proposed that the in situ spores served foliage fossils, which were previously assigned to the

of O. sturii also well resemble the dispersed osmundalean spore genus Osmunda, may be assigned to any of these two gen-

Osmundacidites wellmanii. Unfortunately, no fertile pinnae with era. Alternatively, Escapa and Cúneo (2012) proposed that

in situ spores have been reported for Osmundopsis in China so these species should be reassigned to the genus Osmundop-

far. sis.

Several other Mesozoic ferns are assigned to the genus

Osmunda, such as O. vakhrameevii, O. krassilovii, and O. sibir-

3.1.3. Genus Osmunda Linnaeus

ica from the Jurassic of Russia, and O. vancouverensis from the

The genus is morphologically distinguished from other two

Lower Cretaceous of British Columbia, Canada (Kiritchkova

extant genera Todea and Leptopteris by the facts that its fer-

et al., 1999; Vavrek et al., 2006). Osmunda claytoniites from

tile pinnae are contracted with little or no vegetative lamina

the Upper Triassic of Antarctica was regarded as the oldest

present and the pinnae are articulated at the point of attach-

unequivocal record of Osmunda crown group (Phipps et al.,

ment to the rachis (Hewitson, 1962). Extant Osmunda has

1998). These lines of fossil evidences imply that Osmunda may

a sub-cosmopolitan distribution with its highest diversifica-

represent an example of evolutionary stasis. In China, about

tion in East and Southeast Asia (Tagawa, 1941; Kramer and

seven fossil species of Osmunda have been described (Table 1).

Green, 1990). The genus was recently split into two gen-

Among them, one species is from the Lower Cretaceous (O.

era, Osmunda and Osmundastrum (Jud et al., 2008; Metzgar

cretacea), and the rest are from the Palaeocene (i.e., Osmunda

et al., 2008). The latter is distinguished by rhizome anatom-

sachalinensis and O. greenlandica), Eocene (O. lignitum and O.

ical structures bearing three clusters of thick-walled fibers

heeri), and Neogene (O. totangensis and O. japonica) (Fig. 3)

on the petiolar sclerotic ring (Miller, 1967), but is much

(Zhi and Gu, 1978; Guo, 1979; Zhang et al., 1980; Tao and

more similar to Osmunda in foliage morphology (Escapa 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; to those of Todites and Osmunda (Deng and Chen, 2001).

Wang et al., 2006). Furthermore, Cladophlebis is sometimes found in association

Osmunda cretacea (Figs. 2A, 3B, C) is one of the most with other osmundalean fossils, e.g., Todites and Osmundop-

common taxon from the Early Cretaceous in Far-East regions sis or permineralized rhizomes Ashicaulis and Millerocaulis

(Samylina, 1964; Deng, 1995, 2002; Deng and Shang, 2000). (Vakhrameev and Hughes, 1991; Zhang and Zheng, 1991;

It is described mainly from the Early Cretaceous coal-bearing Tidwell and Ash, 1994). However, with its highly homoplas-

strata in northern China, i.e., the Tiefa and Fuxin basins of tic morphology, Cladophlebis might also represent the foliage

Liaoning Province, the Huolinhe and Hailar basins of Inner of some other fern families (e.g., Cyatheaceae, Schizaeaceae,

Mongolia, and the Jiaohe Basin of Jilin Province (Li et al., 1986; and Dennstaedtiaceae) (Villar de Seoane, 1996; Escapa and

Chen et al., 1988; Deng et al., 1997; Deng and Shang, 2000; Cúneo, 2012). Thus, Cladophlebis should not be considered

Deng and Chen, 2001). Li et al. (1986) described two Raphaelia safely related to the Osmundaceae unless sporangium morphol-

species (R. cretacea and R. denticulata) from the Jiaohe Basin, ogy and arrangement are known.

Jilin Province. It is noted that R. cretacea resembles O. cretacea With more than 240 described species, the genus shows a high

in gross morphology and should be transferred to Osmunda. diversity in geological time throughout the world (McLoughlin

Deng and Chen (2001) proposed that the differences between et al., 1995; Barbacka and Bodor, 2008; Bodor and Babacka,

R. denticulata and O. cretacea were insufficient to distinguish 2008). A recent report (Dai et al., 2012) also recognized a new

each other and further suggested that R. denticulata should be species, Cladophlebis yonganensis Dai et Sun, from the Lower

reassigned to the Osmunda. Cretaceous in Fujian Province, southeastern China.

Two other species, Osmunda sachalinensis and O. green- In China, the genus is extensively recorded in the Late Palaeo-

landica, are reported from the Palaeocene Wuyun Formation zoic and Mesozoic deposits. The earliest record of Cladophlebis

in Jiayin of Heilongjiang Province (Tao and Xiong, 1986; Tao, dates back to the Late Palaeozoic in northern China (e.g., Shanxi,

2000; Wang et al., 2006). Osmunda sachalinensis (Fig. 3D), a Inner Mongolia, and Hebei provinces) (Gu and Zhi, 1974; Yang

common element of the Palaeogene floras in Far-East region et al., 1994; Fig. 4A–C). During the Late Triassic, Cladophlebis

(e.g., Sakhalin, Primorye and Priamurye of Russia and Japan), was very common in both the NPP (e.g., the Yanchang Flora)

is characterized by an expanded pinnule base (Kryshtofovich, and the SPP (e.g., the Baoding Flora, Hsüchiaho Flora, Yip-

1936; Tanai, 1970; Ablaev, 1974, 1985; Kamaeva, 1990). In con- inglang Flora, Lamaya Flora, and Shazhenxi Flora) (Deng and

trast, Osmunda greenlandica always shows a broadly cuneate Chen, 2001). In the Jurassic, especially the Middle Jurassic, rep-

pinnule base (Wang et al., 2006). resented by C. denticulata, C. asiatica and C. gigantea (Fig. 4D,

Osmunda lignitum (Fig. 3A), a very common species of H), the genus Cladophlebis reached a remarkably high diversity

Eocene in Europe (Collinson, 2002; Kvacek,ˇ 2002), resembles in the NPP (Zhang et al., 1998). It showed a distinct decline in

the living O. javanica and O. banksiifolia in leaf morphology diversity at the end of the Early Cretaceous. Then, in the Late

(Florin, 1922; Zhi and Gu, 1978), which are nowadays widely Cretaceous, only Cladophlebis sp. was found from the Qing-

distributed in southern and southeastern China (Wu, 1992; Wang shankou Formation in the Songliao Basin and Taipinglinchang

and Wang, 2001). In China, Osmunda lignitum was documented Formation in Jiayin of Heilongjiang, NE China (Tao, 2000).

from the late Eocene Guchengzi Formation in Fushun of Liao- Cenozoic records of Cladophlebis are rare, with only a few

ning Province (Zhi and Gu, 1978) and the late Palaeocene to early species (i.e., Cladophlebis septentrionalis, and Cladophlebis

Eocene Changchang Formation in Hainan Province (Guo, 1979). spp.) documented, from the Wuyun Formation in Jiayin of Hei-

Geographically, these two fossil localities are far away from longjiang (Zhang, 1983; Quan, 2005).

each other. It is thereafter inferred that this species was widely

distributed throughout China territory during the Palaeocene 3.1.5. Genus Raphaelia Debey et Ettingshausen

to Eocene, though no fossils are found in the transition areas Raphaelia, erected by Debey and von Ettingshausen (1859),

between the two remote localities. is another osmundalean fossil genus, represented by both sterile

Osmunda totangensis, originally recognized from the Neo- and fertile foliages (Tidwell and Ash, 1994). The genus is

gene of Duotang in Yunnan Province (Zhi and Gu, 1978), has widely distributed in the Jurassic of Far-East region in Russia

also been found in the Late Miocene deposits in Tengchong with over 12 species (Zhang et al., 1998). It is also extensively

of Yunnan (Tao, 2000). Osmunda totangensis is similar to O. recorded from the Mesozoic (especially the Jurassic) deposits

lignitum in several characters; however, the lobe shape of the of China, represented by R. diamensis, R. stricta, R. prinadai,

former is more anisomerous and smaller than that of the latter. R. glossoides, R. aff. neuropteroides, and several undefined

The pinnule morphology of O. totangensis also resembles those species (Table 1).

of the extant O. banksiifolia, which nowadays is prosperous in Among these taxa, Raphaelia diamensis is the most sig-

Tengchong, the fossil locality of O. totangensis. nificant representative (Figs. 2B, C, 5C, D). Krassilov (1978)

proposed to transfer R. diamensis to the genus Osmunda, retain-

3.1.4. Genus Cladophlebis Brongniart ing its specific name, on the basis of the examination of fertile

Cladophlebis, a sterile fossil genus with large bipinnate pinnules associated to sterile pinnae determined as R. diamen-

Osmunda-like leaves, is considered to be possibly related to sis (Krassilov, 1978; Phipps et al., 1998). However, Vakhrameev

the Osmundaceae (Bodor and Babacka, 2008). The frond, pin- and Hughes (1991) considered this viewpoint to be premature. In

nule, and venation characters of Cladophlebis are always similar 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 et al., 1988). Morphologically, the type species T. lobifolia is

of them to Osmunda. Raphaelia diamensis is reported mainly similar to Disorus nimakanensis Vachrameev in bearing two

from the NPP, including: the Lower Jurassic in Shaanxi and elongated sporangia under the two lateral pinnule margins

Gansu provinces; the Middle Jurassic in Liaoning, Beijing, Inner (Fig. 5B); however, it differs from the latter by both the leaf base

Mongolia, Xinjiang, and Qinghai provinces; the Upper Jurassic form and the in situ spore type (Vakhrameev and Doludenko,

in Longzhaogou of Heilongjiang Province, and the Lower Cre- 1961). In fact, the in situ spores of T. lobifolia (size and exine

taceous in the Boli Basin of Heilongjiang Province (Yang, 1977; ornamentation) resemble those of several osmundalean taxa,

Chen et al., 1980; Zhang et al., 1980; Ye and Li, 1982; Zheng i.e., modern species Osmunda regalis and Middle Jurassic

and Zhang, 1982, 1983; Cao, 1984; Zhang and Zheng, 1987; species Osmunda jurassica Kara-Mursa (Burakova, 1961).

Mei et al., 1989; Mi et al., 1996; Sun G. et al., 2004, 2010). That is why Tuarella is ascribed to the Osmundaceae. In China,

Raphaelia stricta differs from R. diamensis by its narrow this genus is only represented by the type species T. lobifolia

pinnules, which are inserted on the axis with the whole base recorded from the Lower Jurassic in the Qaidam Basin, Qinghai

(Mei et al., 1989). It has been reported from the Middle Jurassic (Fig. 5A, B) (Table 1) (Li et al., 1988).

of Liaoning and Inner Mongolia (Yang and Sun, 1985; Zhang

and Zheng, 1987). Raphaelia prinadai was documented from

3.2. Osmundalean rhizome fossils

the Middle Jurassic in Liaoning and Jilin provinces (Fig. 5E)

(Yang and Sun, 1982a, b, 1985). Raphaelia glossoides was

Permineralized osmundalean rhizomes have been extensively

reported from the Middle Jurassic in Xinjiang (Zhang et al.,

reported all over the world, representing a high proportion

1998). Raphaelia aff. neuropteroides was described from the

of the osmundalean fossils (Hewitson, 1962; Miller, 1971;

Middle Jurassic in Beijing (Chen et al., 1984). Several Raphaelia

Tian et al., 2008; Taylor et al., 2009). Such permineralized

sp. were documented from the Middle Jurassic in the Qaidam

fossils play an important role in the classification of this

and Shan-Gan-Ning basins, as well as the Lower Cretaceous in

fern lineage (Tidwell and Ash, 1994). Based on rhizoma-

Liaoning and Jilin provinces (Zhang, 1987; Li et al., 1988; Mei

tous anatomical information, the order Osmundales is divided

et al., 1989).

into two families: Osmundaceae and Guaireaceae. The family

Osmundaceae is further separated into two subfamilies, i.e., the

3.1.6. Genus Tuarella Burakova Thamnopteroideae and the Osmundoideae (Tidwell and Ash,

The genus Tuarella Burakova was erected based on Mid- 1994). The Thamnopteroideae, characterized by its protostele

dle Jurassic remains from Turkmenistan (Burakova, 1961). including seven morphogenera (Miller, 1971), might represent

Worldwide, only two species have been referred to Tuarella, an otherwise unknown stock of osmundalean plants (Tidwell

i.e., Tuarella lobifolia and T. petrovii (Burakova, 1961; Li 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 recorded with approximately 10 species belonging to 5 gen-

anatomy, such as Palaeosmunda, Ashicaulis, Millerocaulis, era, i.e., Shuichengella, Zhongmingella, Tiania, Ashicaulis, and

Osmundacaulis, and Aurealcaulis (Gould, 1970; Tidwell and Millerocaulis (Li, 1983; Wang, 1983; Zhang and Zheng, 1991;

Ash, 1994; Cheng and Li, 2007). The four living genera of the Matsumoto et al., 2006; Cheng and Li, 2007; Cheng et al.,

Osmundaceae are also attributed to the Osmundoideae (Tagawa, 2007; Cheng, 2011; Tian et al., 2013, 2014a, b; Wang et al.,

1941; Miller, 1971). The family Guaireaceae now contains 7 2014a, b; Table 1). Historically, there were several reports of Late

genera, including Guairea, Lunea, Donwellicaulis, Itopsidema, Palaeozoic fern rhizomes referable to Palaeosmunda, including

Shuichengella, and the recently established Zhongmingella and P. primitiva Li, P. plenasiosides Li, and P. yunnanense Tian

Tiania (Wang et al., 2014a,b). et Chang (Li, 1983; Li and Cui, 1995). However, these early

Most of the evolutionary information about the order reports were later questioned and reinterpreted as Guaireaceae

Osmundales and the family Osmundaceae comes largely from (Li, 1993; Tidwell and Ash, 1994; Wang et al., 2014a,b).

these structurally preserved rhizomes (Taylor et al., 2009). It As representatives of Guaireaceae, the genera Shuichengella,

is noted that some new insights on the systematic and phy- Zhongmingella, and Tiania were found only in China. Ashicaulis

logenetic relationship among members of Osmundales were and Millerocaulis were well developed in the Middle Jurassic of

provided recently by Wang et al. (2014a), who conducted a China with a remarkable high diversity.

cladistic analysis of a broad range of Osmundales and related In addition, some related fossil taxa from the Palaeozoic of

taxa on the basis of 18 extinct and 6 extant genera and sub- China should be emphasized herein because they show rela-

genera. It was demonstrated that the Thamnopteroideae is not a tionships with the Osmundales. Rastropteris Galtier, Wang,

subfamily of Osmundaceae as previously thought, and the Meso- Li et Hilton was erected based on permineralized material

zoic osmundalean genus Osmundacaulis should be placed in from the Lower Permian Taiyuan Formation in Hebei Province

the family Guaireaceae, rather than in Osmundaceae. In China, (Fig. 6A). The genus is established to accommodate a proto-

fossil taxa of both Osmundaceae and Guaireaceae have been stelic 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., by only one species, Shuichengella primitiva (Li) Li collected

2001). Anatomical characters of Rastropteris, such as the solid from the Late Permian coal ball flora in Shuicheng of Guizhou

homogeneous protostele, leaf trace with initially a single pro- Province, southwestern China (Li, 1983, 1993; Fig. 6B; Table 1).

toxylem and adaxially curved petiole xylem, indicate a close It is characterized by a mixed pith composed of parenchyma

affinity to early members of the Osmundaceae (Galtier et al., and tracheids, a C-shaped leaf trace, and petiole bases with-

2001). It is believed that Rastropteris may be an intermediate out stipular wings. Li (1993) thus proposed a new classification

between Grammatopteris and real catenalean ferns up to the scheme for the Osmundaceae. According to his proposal, the

Osmundaceae (Rößler and Galtier, 2002). whole family was divided into four subfamilies: Osmundoideae,

Thamnopteroideae, Shuichengelloideae, and Guaireoideae (Li,

1993). Consequently, the Shuichengella was believed as a mono-

3.2.1. Genus Shuichengella Li

typic genus of the subfamily Shuichengelloideae. However,

The genus Shuichengella was erected based on reinvesti-

this classification scheme is not widely accepted. Later, the

gations of two anatomically preserved rhizomes which were

Shuichengella was recognized as a member of the osmundalean

originally described by Li (1983) as Palaeosmunda primitiva

family Guaireaceae (Tidwell and Ash, 1994; Wang et al.,

(Li, 1993) for its petiole bases bearing no stipule. This taxon

2014a).

is interpreted as structurally preserved stem of osmundalean

plants, which possesses an ectophloic dictyoxylic siphonos-

tele with mixed pith and a heterogeneous cortex without the 3.2.2. Genus Zhongmingella Wang et al.

mantle of leaf-bases and/or adventitious roots and sclerenchy- Zhongmingella is a newly established genus based on the

matic sheaths of leaf traces (Li, 1993). This genus is represented 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 plena- 3.2.4. Genus Millerocaulis Erasmus ex Tidwell emend.

sioides Li (Wang et al., 2014a). Specimen of Zhongmingella Tidwell

was collected from the same locality and horizon with Shuichen- Millerocaulis, Ashicaulis, and Osmundacaulis have been

gella (Li, 1983; Sun K.Q. et al., 2010; Wang et al., 2014a). The generally considered as the three most common Mesozoic rhi-

genus is represented by only one species Zhongmingella ple- zome genera of the Osmundaceae (Tidwell and Ash, 1994),

nasioides (Li) Wang, Hilton, He, Seyfullah et Shao, which is though Wang et al. (2014a) suggested that Osmundacaulis may

preserved as a rhizomatous stem with dictyostelic stele, hetero- be more closely related to Guaireaceae. Their relationships have

geneous pith and cortex comprising parenchyma and uniformly been discussed in detail by several authors (Tidwell, 1994;

distributed secretory cells (Fig. 6C) (Li, 1983; Wang et al., Tidwell and Ash, 1994; Tian et al., 2008; Wang et al., 2014a).

2014a). Anatomical comparisons and results of a cladistic anal- Anatomically, Millerocaulis is characterized by an ectophloic

ysis both support to place the genus in the family Guaireaceae siphonostele, a parenchymatous pith, and thick outer cortex with

(Wang et al., 2014a). The reports of this distinct taxon as well incomplete leaf gaps, and C-shaped leaf traces with endarch

as the Shuichengella markedly improve the anatomical diver- protoxylem (Tidwell, 1986, 1994). With 11 species described

sity of the family Guaireaceae, and indicate that the family worldwide, the genus ranged from the Middle Triassic to the

might have expanded its distribution range to the non-Gondwana Early Cretaceous (Tidwell, 1986; Tian et al., 2008). Addition-

regions. ally, 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

3.2.3. Genus Tiania (Tian et Chang) Wang et al.

Tidwell (1994). In China, two species have been described,

The genus Tiania was erected very recently by Wang et al.

i.e., Millerocaulis sinica (Figs. 6D, 7B) and M. preosmunda

(2014b) based on re-investigations of the original specimens of

(Figs. 6F, 7A) from the Middle Jurassic Tiaojishan Forma-

Palaeosmunda yunnanense Tian et Chang from the Late Permian

tion in Beipiao of Liaoning Province (Cheng and Li, 2007;

Xuanwei Formation in Yunnan Province, SW China. It is demon-

Cheng et al., 2007; Table 1). These two species are similar

strated to represent another new genus within the Guaireaceae.

in many aspects, but differ from each other in the petiolar

The genus is represented by only one species T. yunnanense.

sclerotic ring and sclerenchyma arrangement in the stipular

The stem of T. yunnanense comprises an ectophloic siphonos-

wings. It is noted that these two species are both character-

tele with no leaf gaps, a bilayered pith, and a unilayered cortex

ized by heterogeneous sclerotic rings with sclerenchymatous

with numerous adaxially curved leaf traces.

fibers.

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 3.2.5. Genus Ashicaulis Tidwell

siphonostele without leaf gaps, Tiania is interpreted as an evo-

As an osmundaceous rhizome genus, Ashicaulis is charac-

lutionary

intermediate between the protostelic thamnopterids terized by an ectophloic dictyoxylic siphonostele with definite

and the more advanced dictyostelic osmundaleans (Wang et al.,

leaf gaps (Tidwell, 1994). This taxon was separated from Mille-

2014b).

rocaulis 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 unique mushroom-like scleremchyma mass in the petiolar vas-

by many palaeobotanists (Cantrill, 1997; Matsumoto et al., 2006; cular bundle concavity (Tian et al., 2014b; Fig. 8A). Ashicaulis

Cheng, 2011; Tian et al., 2013, 2014a,b; Wang et al., 2014a), claytoniites shows a special petiolar sclerenchyma arrangement

though controversy remains (Herbst, 2001, 2006; Vera, 2008). (Cheng, 2011).

Totally, over 30 species are referred to this genus with a relative It is noted that all these seven species are documented from

high latitude distribution in both hemispheres (Tian et al., 2008, the Middle Jurassic Tiaojishan Formation in Hebei and Liao-

2013, 2014a,b; Cheng, 2011). ning provinces, northeastern China. Our recent investigations

Seven species of Ashicaulis have been described from on the permineralized specimens from the Middle Jurassic in

China (Table 1), i.e., Ashicaulis hebeiensis, A. liaoningensis, western Liaoning show a much higher anatomical diversity of

A. macromedullosus, A. claytoniites, A. beipiaoensis, A. wangii, osmundalean ferns than currently known, and over 11 additional

and A. plumites (Figs. 6E, G–I; 7C–F) (Wang, 1983; Zhang and species (including eight new species, will be published sepa-

Zheng, 1991; Matsumoto et al., 2006; Cheng, 2011; Tian et al., rately) of Ashicaulis may be recognized in this locality (Tian,

2013, 2014a,b). Among these species, Ashicaulis macromedul- 2011; Fig. 8B–E). Most of the Chinese materials of Ashicaulis

losus, A. hebeiensis, and A. beipiaoensis are with a homogeneous have heterogeneous sclerotic rings, which differ from those taxa

petiolar sclerotic ring (Fig. 7C, E, F); however, Ashicaulis from the Southern Hemisphere. Some of the Chinese specimens

macromedullosus bears no sclerenchyma tissues in the trace show very specialized anatomical structures. For example, in

concavity, whereas A. hebeiensis is distinct by having the lining one of the new species of Ashicaulis, the abaxial side of the

sclerenchyma tissues in the petiolar vascular bundle concavity sclerotic ring is composed of sclerenchymatous fibers with the

associated with sclerenchymatous clusters in the petiolar inner two lateral parts extremely expanding to form a dumbbell-shape

cortex (Fig. 7E). The rest four species are all with heterogeneous (Fig. 8C). However, compared with fossils from the Southern

sclerotic rings. Ashicaulis liaoningensis and A. wangii differ Hemisphere, most of the Chinese materials demonstrate less

from the other two species in having heterogeneous pith (Tian developed sclerenchymatous tissues in the petiolar cortex though

et al., 2014a; Fig. 7D). Ashicaulis plumites is characterized by a 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 reached its maximum diversity during the Late Triassic to the

Middle Jurassic intervals with about 40 species (Fig. 9). In the

4.1. Stratigraphical ranges Late Triassic, the Osmundaceae was represented mainly by two

genera Todites (13 species) and Osmundopsis (2 species). Across

Our analysis indicates that a total of more than 50 species the Triassic/Jurassic boundary, about 14 species of three gen-

referred to 10 genera of osmundalean fossils have been docu- era (Todites, Osmundopsis and Raphaelia) were recorded in the

mented in China excluding the morphogenus Cladophlebis from Early Jurassic (Fig. 9). Todites remained quite common with

this study (Fig. 9; Table 1). These fossil records demonstrate that about six species, three of which (Todites leei, T. nanjingen-

the order Osmundales may have appeared in the Late Palaeozoic sis, T. cf. thomasi) first appeared in the Early Jurassic (Fig. 9).

in China. It is noted that though Rastropteris was documented Osmundopsis showed a relatively higher diversity with up to 5

from the Lower Permian, fossils with unequivocal osmundalean species in the Early Jurassic, but became extinct at the end of

anatomical characters were present in the Late Permian, repre- the Early Jurassic in China (Fig. 9). In this time interval, the

sented by the Guaireaceae (i.e., Shuichengella, Zhongmingella genus Raphaelia, appeared for the first time with one species R.

and Tiania) (Li, 1993; Wang et al., 2014a,b). The Guaireaceae diamensis.

has a short stratigraphical range and became extinct at the end In the Middle Jurassic, the species diversity of Todites

of Late Permian in China (Fig. 9). declines sharply to only four species (Fig. 9). In contrast,

In China, all the Mesozoic records of Osmundales belonged Raphaelia reaches its maximum in diversity up to seven species.

to the family Osmundaceae (Fig. 9). During the early Mesozoic, Some diverse new taxa occurred for the first time in this inter-

especially the interval from the Early to Middle Triassic, rare fos- val (Fig. 9), such as Tuarella (1 species), Ashicaulis (7 species),

sil records have been reported and only a single species Todites and Millerocaulis (2 species). During the Middle to Late Juras-

shensiensis was described from the Middle Triassic (P’an, 1936; sic transition, the species diversity declines rapidly from 21

Wang et al., 2005). Additionally, some dispersed osmundalean species in the Middle Jurassic to only three species in the Late

spores (e.g., Osmundacidites sebectus) were reported from the Jurassic (Fig. 9). In particular, the three taxa including Tuarella,

Lower Triassic Heshanggou Formation and Middle Triassic Ashicaulis, and Millerocaulis became extinct in China at the end

Tongchuan Formation (Song et al., 2000). The Osmundaceae 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 During the Early–Middle Triassic, marine depositions were

found (Fig. 9). Among them, the genus Osmunda became an dominant in southern China; whereas the terrestrial sediments

important element during the Early Cretaceous in China. Todites were well developed in northern China (Liu and Quan, 1995).

and Raphaelia were extinct at the end of the Early Cretaceous. However, hardly any Early Triassic fossils were found in north-

To date, there is no unequivocal osmundalean record in the ern China due to the dry climate (Sun et al., 1995b). Though

Late Cretaceous interval, though Cladophlebis spp. was reported the Middle Triassic floras in northern China were relatively

from the Taipinglinchang Formation in Jiayin of Heilongjiang more developed than those in the Early Triassic (Sun et al.,

Province, NE China (Quan, 2005). 1995b), osmundalean fossil records were still poor, and only

In the Cenozoic, all fossil records of Osmundaceae were Todites shensiensis was reported in Shaanxi, Inner Mongolia,

ascribed to extant genus Osmunda with six species (Fig. 9). Sev- and Liaoning provinces, northern China (Fig. 10).

eral Cladophlebis species were documented from the Palaeocene From the Late Triassic, the geotectonic framework of China

Wuyun Formation in Jiayin, Heilongjiang Province, NE China greatly influenced Indo-China Movement, and afterwards conti-

(Tao, 2000). nental deposits developed extensively throughout China territory

except parts of Tibet (Liu and Quan, 1995). During the Late Tri-

4.2. Palaeogeographical distribution assic, the SPP was the dominant region for the distribution of the

Osmundaceae with over 20 fossil localities (e.g., Sichuan, Yun-

Geographically, the Osmundaceae shows an extensive dis- nan, Chongqing, and Hubei provinces); in contrast, only five

tribution in the whole territory of China (Fig. 10). However, fossil sites were found in the NPP, including Liaoning, Jilin,

the geographical distribution pattern varies through time. Dur- Hebei, and Shaanxi provinces (Fig. 10). For the Early Jurassic,

ing the Late Palaeozoic, probable osmundalean representatives five localities were reported in the NPP (i.e., Heilongjiang, Lia-

(Rastropteris and Cladophlebis) were documented mostly from oning, Hebei, Gansu, and Qinghai provinces), whereas about 11

northern China, such as Shaanxi and Hebei provinces. In localities were recorded in the SPP, especially the middle-lower

contrast, definite osmundalean rhizome taxa (Shuichengella, Yangtze Blocks (e.g., Hubei, Anhui, and Jiangsu provinces). It

Zhongmingella and Tiania) were reported from Guizhou and is noteworthy that almost all Middle Jurassic osmundalean fos-

Yunnan provinces, SW China (Fig. 10). sils were found from the NPP (Fig. 10), no osmundalean taxa

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were documented from the SPP during the Middle Jurassic to of China yield typical heterogeneous petiolar sclerotic rings.

the Late Cretaceous (Fig. 10). Thus, these Chinese fossil materials show a real potential to

Osmundalean ferns were restricted to NE China from the bridge the evolutionary gap of Osmundales. Recent encour-

Late Jurassic to the Early Cretaceous (Fig. 10). Todites major, aging progresses from China proposed that M. preosmunda

documented from the Yixian Formation in Beipiao of Liaoning and M. sinica be closely related with living Osmunda sub-

Province, is proposed to be the latest fossil record of Todites genus Osmunda (Cheng and Li, 2007; Cheng et al., 2007).

in China. Osmunda cretacea is geographically restricted to NE Ashicaulis claytoniites is treated as a close relative to the extant

China, such as Inner Mongolia, Liaoning, and Jilin provinces O. claytoniana (Cheng, 2011). Yatabe et al. (2005) suggested to

(Fig. 10). The Cenozoic osmundalean ferns were scattered in divide the subgenus Osmunda into subgenus Osmunda and sub-

Heilongjiang and Liaoning provinces of northern China as well genus Claytosmunda (Metzgar et al., 2008). On this account,

as Yunnan and Hainan provinces of southern China (Fig. 10). Osmunda claytoniana is more related to the subgenus Clay-

tosmunda. Ashicaulis hebeiensis is considered to be related to

5. Discussion living Osmunda subgenus Plenasium (Wang, 1983). However,

its leaf trace vascular bundle does not show two protoxylem clus-

Though osmundalean fossils are extensively reported world- ters when departing from the stele, which is a key feature for the

wide, some gaps remain in its evolutionary history (Taylor et al., subgenus Plenasium. Ashicaulis beipiaoensis bears close simi-

2009). As already addressed, Chinese fossil records cover almost larities to Osmunda shimokawaensis from the Middle Miocene

all important stages in the macroevolution of Osmundales; there- of Hokkaido, Japan. They may represent an extinct branch in the

fore a comprehensive analysis on these data will contribute to Osmundaceae evolutionary tree (Tian et al., 2013). In addition,

further understanding of the evolutionary trend of this fern lin- Ashicaulis wangii and A. plumites, show remarkable anatomical

eage. Molecular analysis reveals that the Osmundaceae might resemblances to the Palaeocene Osmunda pluma, as well as to

have arisen in the Late Carboniferous, and then experienced a several taxa of extant Osmunda subgenus Osmunda (Tian et al.,

rapid diversification until the Early Permian (Pryer et al., 2004; 2014a, b). Our recent investigation shows that osmundalean rhi-

Schuettpelz et al., 2006; Schuettpelz and Pryer, 2007). The fern zomes have a high structural and species diversity (17 species) in

genus Grammatopteris reported from the Lower Permian of the Middle Jurassic of western Liaoning (Tian, 2011). Detailed

Europe might be the earliest record of the early osmundalean studies on these fossils will make it possible to provide further

plants (Renault, 1896; Beck, 1920; Galtier et al., 2001), though evidence for understanding the evolutionary lines between the

it is still controversial. The occurrence of Rastropteris, Shuichen- Mesozoic members and the living Osmundaceae.

gella, Zhongmingella, and Tiania in China implies that China is Osmundalean fossils from northeastern China region are

one of the diversification centers for osmundalean ferns during quite abundant since the Middle Jurassic, represented by diverse

the Late Palaeozoic, and indicates the order Osmundales has got species, such as Todites, Ashicaulis, and Millerocaulis (Middle

a considerable range extension in both Northern and Southern Jurassic), Raphaelia and Osmunda cretacea (Early Cretaceous),

Hemispheres during the Late Permian. O. wuyunensis and O. greenides (Palaeocene), as well as O. lig-

Fossil evidence shows that evolution of Osmundales pro- nitum (Eocene). These continuous fossil records provide links

ceeded rapidly during the Late Palaeozoic and Early Mesozoic for understanding the Cenozoic diversity variation and evolu-

time (Miller, 1971). The time interval between the Late Triassic tion of the Osmundaceae in East Asia. Obviously, there are also

to the Middle Jurassic is the flourishing period for this order in considerable occurrences of the Cenozoic osmundalean rhizome

China. Schuettpelz and Pryer (2009) suggested that the diversifi- and foliage fossils in other regions of the world (i.e., Slovakia,

cation of osmundalean ferns happened near the Triassic–Jurassic Hungary, Washington of USA, and Trimmelkam of Austria)

transition, when the earliest representatives of the crown group (Miller, 1967, 1971). Together with the above-mentioned

are recorded. This view is supported by the occurrences of abun- regions, northeastern China is proposed to act as one of the

dant osmundalean fossil records in both northern and southern refuges for osmundalean ferns, and plays a significant role in pre-

China. Cenozoic osmundalean fossils show close similarities in serving the gene bank for extant osmundalean ferns in East Asia.

leaf morphology to the extant osmundalean taxa in East Asia,

demonstrating a low evolutionary rate. This is in accordance 6. Concluding remarks

with the low diversification rate of Osmundaceae proposed by

Schuettpelz and Pryer (2009). 1) This study provides for the first time a systematic overview

It is commonly believed that most living osmundalean ferns on the diversity variation and distribution pattern of the fossil

were derived from genera Millerocaulis and Ashicaulis (Tidwell Osmundales in China.

and Ash, 1994). However, evolutionary relationships among 2) Our analysis indicates that totally more than 50 species of

them remain poorly known due to the lack of sufficient interme- 10 genera of osmundalean fossils have been documented in

diate forms. We know that most of extant osmundalean ferns are China excluding the morphogenus Cladophlebis. Geograph-

characterized by bearing heterogeneous petiolar sclerotic rings. ically, they have been reported in both Northern and Southern

However, most of the Mesozoic Millerocaulis and Ashicaulis China phytoprovinces, though these taxa show variations in

species, especially those from the Southern Hemisphere, always geographical ranges.

bear a homogeneous sclerotic ring. On the contrary, the most 3) The Osmundales are first recorded in China in the Late

anatomically preserved fossil rhizomes from the Middle Jurassic Palaeozoic. Representatives with unequivocal osmundalean

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

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anatomical structures are reported from the Late Permian, Bodor, E., Barbacka, M., 2008. Taxonomic implications of Liassic ferns

Cladophlebis Brongniart and Todites Seward from Hungary. Palaeoworld

represented by Guaireaceae. The Late Triassic to Mid-

17, 201–214.

dle Jurassic interval represents a period of radiation for

Brongniart, A., 1849. Tableaux des genres de végétaux fossiles considérés

osmundaceous ferns. From the Late Jurassic onwards, fos-

sous le point de vue de leur classification botanique et de leur distribution

sil diversity declines rapidly. Cenozoic taxa are represented géologique. Dictionnaire Universel d’Histoire Naturelle, Paris, 127 pp.

only by several relictual Osmunda species. Burakova, A.T., 1961. Middle Jurassic ferns from western Turkmenia. Paleon-

tologicheskii Zhurnal 4, 139 (in Russian).

4) Chinese fossil records cover almost all important stages

Cantrill, D.J., 1997. The pteridophyte Ashicaulis livingstonensis (Osmundaceae)

for the macroevolution of the Osmundales, e.g., the origin,

from the Upper Cretaceous of Williams Point, Livingston Island, Antarctica.

radiation, decline and relic, and contribute to further under-

New Zealand Journal of Geology and Geophysics 40, 315–323.

standing of evolutionary lines of this peculiar fern lineage. Cantrill, D.J., Webb, J.A., 1987. A reappraisal of Phyllopteroides Medwell

(Osmundaceae) and its stratigraphic significance in the Lower Cretaceous

of eastern Australia. Alcheringa 11, 59–85.

Acknowledgements Cantrill, D., Nagalingum, N., 2005. Pteridophytes from the Cretaceous of Alex-

ander Island, Antarctica: implications for Cretaceous phytogeography of the

Southern Hemisphere. Review of Palaeobotany and Palynology 137, 83–103.

We thank Prof. Ge Sun (Shenyang), Prof. Xiang-Wu Wu

Cao, Z.Y., 1984. Fossil plants from the Longzhaogou Group in Eastern Hei-

(Nanjing), Prof. Sheng-Hui Deng (Beijing), and Dr. Yu-Yan

longjiang Province (III). In: Research Team on the Mesozoic Coal-bearing

Miao (Beijing) for helpful discussion and courtesy for fossil Formations in Eastern Heilongjiang (Ed.), Fossils from the Middle–Upper

photos. We are grateful to Dr. Mihai Popa (Bucharest) and Prof. Triassic and Lower Cretaceous in Eastern Heilongjiang Province, China,

Part II. Heilongjiang Science and Technology Publishing House, Harbin,

Shi-Jun Wang (Beijing) for their kind reviews on the manuscript.

pp. 1–34 (in Chinese).

Special thanks are due to Dr. M. Philippe (Lyon) and Dr. E.I.

Chen, F., Dou, Y.W., Yang, G.X., 1980. The Jurassic Mantougou-Yudaishan

Vera (Buenos Aires) for their constructive comments for the

Flora from western Yanshan, North China. Acta Palaeontologica Sinica 19,

earlier version of the manuscript. This study was jointly sup- 423–430 (in Chinese, with English abstract).

ported by State Key Programme of Basic Research of Ministry Chen, F., Dou, Y.W., Huang, Q.S., 1984. The Jurassic Flora of Western Hills,

Beijing. Geological Publishing House, Beijing, 136 pp. (in Chinese, with

of Science and Technology, China (Grant No. 2012CB822003),

English abstract).

the National Natural Science Foundation of China (Grant No.

Chen, F., Meng, X.Y., Ren, S.Q., Wu, C.L., 1988. The Early Cretaceous Flora

41302004), the Innovation Project of CAS (Grant No. KZCX-

of Fuxin Basin and Tiefa Basin, Liaoning Province. Geological Publishing

2-YW-154), the Team Program of Scientific Innovation and House, Beijing, 180 pp. (in Chinese, with English abstract).

Interdisciplinary Cooperation of CAS, the State Key Labora- Cheng, Y.M., 2011. A new species of Ashicaulis (Osmundaceae) from the Meso-

zoic of China: a close relative of living Osmunda claytoniana L. Review of

tory of Palaeobiology and Stratigraphy (Nanjing Institute of

Palaeobotany and Palynology 165, 96–102.

Geology and Palaeontology, CAS) (Grant No. 133113), Science

Cheng, Y.M., Li, C.S., 2007. A new species of Millerocaulis (Osmundaceae,

Research Project of Liaoning Provincial Education Department

Filicales) from the Middle Jurassic of China. Review of Palaeobotany and

(Grant No. L2012391) and the Talent Fund of Shenyang Normal Palynology 144, 249–259.

University (Grant No. 91400114006). Cheng, Y.M., Wang, Y.F., Li, C.S., 2007. A new species of Millerocaulis

(Osmundaceae) from the Middle Jurassic of China and its implication

for evolution of Osmunda. International Journal of Plant Sciences 168,

1351–1358.

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