- Research article
- Open Access
Chengia laxispicatagen. et sp. nov., a new ephedroid plant from the Early Cretaceous Yixian Formation of western Liaoning, Northeast China: evolutionary, taxonomic, and biogeographic implications
© Yang et al.; licensee BioMed Central Ltd. 2013
- Received: 14 December 2012
- Accepted: 20 March 2013
- Published: 27 March 2013
The extant Gnetales include three monotypic families, namely, Ephedraceae (Ephedra), Gnetaceae (Gnetum), and Welwitschiaceae (Welwitschia), all of which possess compound female cones that comprise a main axis and 1 to multiple pairs/whorls of bracts subtending a female reproductive unit or having lower pairs/whorls of bracts sterile. However, the evolutionary origin of such a reproductive architecture in Gnetales is controversial in the light of the competing anthophyte versus gnetifer hypotheses of seed plant relationships. Hence, macrofossils demonstrating the structure of compound female cones of the Gnetales should be important to decipher the early evolution of the order.
A new ephedroid plant Chengia laxispicata gen. et sp. nov. is described from the Early Cretaceous Yixian Formation of western Liaoning, Northeast China. The fossil represents a part of a leafy shooting system with reproductive organs attached. The main shoot bears internodes and swollen nodes, from which lateral branches arise oppositely. Reproductive organs consist of female spikes terminal to twigs or axillary to linear leaves. Spikes are loosely arranged, having prominent nodes and internodes. Bracts of the spikes are decussately opposite and comprise 4—8 pairs of bracts. Each bract subtends an ellipsoid seed. Seeds are sessile, with a thin outer envelope and a distal micropylar tube.
Chengia laxispicata gen. et sp. nov. provides a missing link between archetypal fertile organs in the crown lineage of the Gnetales and compound female cones of the extant Ephedraceae. Combined with a wealth of Ephedra and ephedroid macrofossils from the Early Cretaceous, we propose a reduction and sterilization hypothesis that the female cone of the extant Ephedraceae may have stemmed from archetypal fertile organs in the crown lineage of the Gnetales. These have undergone sequentially intermediate links similar to female cones of Cretaceous Siphonospermum, Chengia, and Liaoxia by reduction and sterilization of the lower fertile bracts, shortenings of internodes and peduncles as well as loss of reproductive units in all inferior bracts. The basal family Ephedraceae including Ephedra of the extant Gnetales was demonstrated to have considerable diversity by the Early Cretaceous, so an emended familial diagnosis is given here. The Jehol Biota in Northeast China and adjacent areas contains a plethora of well-preserved macrofossils of Ephedra and ephedroids that show different evolutionary stages including primitive and derived characters of Ephedraceae, so Northeast China and adjacent areas may represent either the centre of origination or one of the centres for early diversification of the family.
- Early Cretaceous
- Female cone
- Jehol biota
- Reduction and sterilization hypothesis
- Yixian Formation
The extant Ephedraceae (Ephedra) usually occupy a basal position in phylogenetic trees of the Gnetales (Figure 1d) while Gnetum and Welwitschia are more derived and are more closely related to each other than either is to Ephedra[14, 17–23, 27–33]. Ephedra has scale-like, linear and 2 (—3) parallel-veined leaves which are often opposite and decussate at nodes and connate at the base into a sheath (e.g., E. equisetina Bunge, E. distachya L., E. sinica Stapf, E. pedunculata Engelm. ex S. Wats., and E. chilensis C. Presl), and ternate phyllotaxis is also not rare (e.g., E. intermedia Schrenk ex C. A. Mey., E. przewalskii Stapf, and E. ochreata Miers) [4, 6, 7, 9] (Figure 1a). In contrast, Welwitschia bears two opposite, enormous strap-like leaves with numerous parallel primary veins (and cross veins with apically oriented chevrons in cotyledons) [6, 7, 9] (Figure 1c), while Gnetum possesses petiolate, broad-laminar and reticulate-veined leaves that are arranged in opposite and decussate manner in most cases [6, 7, 9] (Figure 1b), and ternate phyllotaxis is also present (Yong Yang, unpublished observations). Bracts and reproductive units of female cones of Ephedra and Welwitschia are opposite and decussate in most cases while those of Gnetum are usually whorled at nodes with the fusion of bracts into cupules and occasionally they are spirally arranged [34–36]. Both Gnetum and Welwitschia bear female cones with many whorls of fertile bracts while living Ephedra normally has only the uppermost whorl/pair of bracts fertile [37–39], rarely the inferior bracts subtending female reproductive units [8, 40], or hermaphroditic cones with the lower whorls of bracts bearing male reproductive units but the uppermost whorl possessing female reproductive units [41, 42]. In addition, ovules of the Gnetales have 1—2 outer envelopes and the inner integument upwardly extended into a characteristic micropylar tube. Therefore, well-preserved female reproductive organs of the Gnetales may be easily recognized in the fossil record, and macrofossils of the basal family Ephedraceae are especially important in understanding the origin and phylogenetic relationships of the extant Gnetales.
So far, a variety of pre-Cretaceous macrofossils have been attributed to or compared with extant Gnetales (e.g., Palaeognetaleana auspicia Z.Q. Wang , Dechellyia gormanii Ash [9, 44], Dinophyton spinosus Ash [9, 45, 46], Nataligma dutoitii J.M. Anderson et H.M. Anderson , Sanmiguelia lewisii Cornet [47, 48], Archaestrobilus cupulanthus Cornet , Ephedrites sinensis Wu et al. and Ephedrites exhibens Wu et al. [50, 51]), but their putative relationships to the Gnetales are not unequivocal due to lacking of synapomorphies recognized from the clade (e.g., compound female cones, whorled, opposite and decussate phyllotaxis in leaves, bracts, and bracteoles) and other detail (e.g., polyplicate pollen in situ) as Crane  previously suggested. Hence, the extant genera Ephedra, Gnetum, and Welwitschia, together with two Cretaceous genera Drewria Crane et Upchurch  and Eoantha Krassilov [54, 55], were considered to form a crown group of the Gnetales  while those pre-Cretaceous genera were assigned to either stem-gnetaleans  or seed plants with uncertain affinities [48, 52]. Recently, a wealth of additional Early Cretaceous macrofossils and mesofossils assignable to the crown-gnetaleans have been widely described from South Europe, Northeast China, Mongolia, North America, South America, and Australia , suggesting that three families Ephedraceae, Gnetaceae, and Welwitschiaceae of the extant Gnetales existed and diversified during at least the Early Cretaceous. Of all, macrofossils closely related to Welwitschia and Gnetum are very rare [58–60], but macrofossils and mesofossils (i.e., seeds) assignable to Ephedraceae or even to the extant Ephedra have been extensively reported [61–82]. These members of the Ephedraceae show a very high morphological diversity in both reproductive and vegetative organs across the world except for Africa and Antarctica. According to characteristics of female reproductive organs, Cretaceous ephedroid macrofossils can be classified into three groups, namely: (1) those with female cones bearing 1(—2?) pairs of bracts with only the uppermost pair fertile, e.g., Ephedra carnosa Yang et Wang , E. archaerhytidosperma Yang et al. , E. hongtaoi Wang et Zheng  and E. verticillata Cladera et al.  as well as Alloephedra xingxuei Tao et Yang [57, 65, 66] and two species of Gurvanella Krassilov 1982 [67–69] (= Chaoyangia Duan 1998 [70–73], non Chaoyangia Hou et Zhang 1993  for an Early Cretaceous bird fossil also from Chaoyang District of Liaoning Province, Northeast China; for nomenclatural discussions see [57, 67, 69, 84]); (2) those with female cones possessing multiple whorls of fertile bracts each subtending a female reproductive unit, e.g., numerous species of Liaoxia Cao et Wu 2006  (= Ephedrites Göppert et Berendt 1845 , non Ephedrites Saporta 1891[67, 76]); and (3) those that have ovules surrounded by envelopes lacking supporting bracts and directly attached on the peduncles, e.g., Siphonospermum simplex Rydin et Friis . Therefore, the basal gnetalean family Ephedraceae, including the extant genus Ephedra, was demonstrated to have considerable diversity by the Early Cretaceous.
In this paper, we study a new ephedroid macrofossil from the Early Cretaceous Yixian Formation of western Liaoning Province, Northeast China, and name it Chengia laxispicata gen. et sp. nov.. Our new plant bears a comparatively complete, leafy shooting system with loose female spikes that allow us to discuss the evolution of female cones of the Ephedraceae. We also consider the taxonomic and biogeographic implications of our findings on the basis of abundant ephedroid macrofossils from the Early Cretaceous Jehol Biota of Northeast China and adjacent areas.
Description of the specimens
Identity and affinity
The fossil specimens studied here obviously possess opposite organographic features, including opposite lateral branches, leaves as well as decussately opposite bracts and enveloped seeds, all of which conform to the diagnostic and synapomorphic features of the Gnetales [6, 7, 9, 19, 32, 52, 85, 86]. Hence this plant can be readily classified into the Gnetales, and its linear leaves and decussately opposite bracts that comprise female spikes resemble those of the ephedroids. However, the decussately opposite bracts and loose female spikes with clear nodes and internodes are noticeably different from all known ephedroid fossils [52, 57] and extant Ephedra that bears female cones usually having 2—13 pairs/whorls of cone bracts but with only the uppermost pairs/whorls of bracts being fertile [4, 6, 7, 9]. Therefore, the fossils presented here do not conform to the generic circumscription of Ephedra and require a new name for which we institute Chengia laxispicata gen. et sp. nov. and place it within the ephedroid Gnetales (See Conclusion — Systematics).
The evolution of female cones in Ephedraceae
Previous morphological, anatomical, ontogenetic, and molecular studies supported a reduction hypothesis that female cones of the extant Ephedraceae may have stemmed from a loosely arranged, multi-axial, reproductive organs homologous to the Late Palaeozoic Cordaitales and Permian—Triassic coniferophytes [4, 6, 8, 15, 17, 35, 36, 38–40],[87–94]. With shortening of internodes of the reproductive multi-axial shoot system, both the primary and secondary shoots of Ephedraceae, to some extent, may have experienced a series of structural reductions and finally given rise to compact female cones in extant Ephedra[4, 8, 87, 89]. Hence, female cones similar to laxly arranged reproductive shooting systems would represent more primitive organizations than those resembling to compact reduced female cones of the extant Ephedraceae. Our new fossil Chengia laxispicata gen. et sp. nov. bearing loose female spikes appears to be a missing link to the extant Ephedraceae with compact cones.
Early Cretaceous macrofossils have provided diverse characteristics of female reproductive structures. Ovulate cones of Ephedra carnosa, E. archaeorhytidosperma, E. hongtaoi, Gurvanella dictyoptera Krassilov and G. exquisita Sun et al. [67–69, 80] from the Early Cretaceous Jehol Biota of Northeast China and adjacent areas bear either 1(—2?) pairs or 1 whorl of bracts enclosing 1—3 seeds, effectively demonstrating the same pattern as modern Ephedra that possesses only the uppermost one pair/whorl of fertile bracts. Siphonospermum simplex has linear leaves, opposite phyllotaxis, and ovules with exposed micropylar tubes and surrounded by envelopes, which are attached directly on the peduncles, so these ephedroid features may be plesiomorphic in the Gnetales . Female spikes of Liaoxia have multiple whorls of fertile bracts each subtending a female reproductive unit (or seed) (referring to Liaoxia robusta Rydin et al. ), which provide palaeobotanical evidence for the previous morphological—evolutionary interpretation that the archetypal female cone of Ephedraceae may be compound, with multiple-whorled fertile bracts.
Our new ephedroid fossil-genus Chengia markedly differs from both extant and fossil species of Ephedra by the female cone bearing multiple (4—8) pairs of fertile bracts. It is different from Siphonospermum by the female reproductive unit possessing subtending bracts. Chengia also differs from Liaoxia in having loosely arranged female cones. The female spikes of Chengia have evident nodes and internodes showing similarity to the supposed laxly arranged reproductive shoot system of ancient ancestors, so such female cones in Ephedraceae are more primitive than those of Liaoxia and other ephedroid fossils (e.g., Alloephedra, Gurvanella, and Ephedra).
This ephedroid plant Chengia laxispicata gen. et sp. nov. described from the Early Cretaceous Yixian Formation of Northeast China provides a missing link between archetypal fertile organs of the crown lineage of the Gnetales and compound female cones of the extant Ephedraceae. Based upon a plethora of Ephedra and ephedroid macrofossils from the Early Cretaceous, we propose a reduction and sterilization hypothesis that the female cone of the extant Ephedraceae may have stemmed from archetypal fertile organs of the crown lineage of the Gnetales, which have undergone sequentially intermediate links similar to female cones of Cretaceous Siphonospermum, Chengia, and Liaoxia by a series of transformations that include reduction and sterilization of the lower fertile bracts, shortenings of internodes and peduncles, loss of reproductive units in all inferior bracts. The basal family Ephedraceae including Ephedra of the extant Gnetales was demonstrated to have considerable diversity by the Early Cretaceous, so an emended familial diagnosis is given here. The Jehol Biota in Northeast China and adjacent areas contains a plethora of well-preserved macrofossils of Ephedra and ephedroids that show different evolutionary stages including primitive and derived characters of Ephedraceae, so Northeast China and adjacent areas may represent either the centre of origination for the family or its centre of early diversification.
Gnetales Luerss. 1879
Ephedraceae Dumort. 1829, emend.
Type: Ephedra L. 1753, Sp. Pl. 1040.
Dioecious (rarely monoecious) shrubs, sub-shrubs, small tree, climbers, or sometimes perennial herbs. Shoots are profusely and dichasially branched and have many nodes; nodes are usually swollen, sometimes branches are whorled at nodes due to extremely reduction of internodes or alternate on account of suppression of the opposite branch; internodes of twigs possess many fine striations. Leaves are opposite and decussate or ternately whorled at nodes, linear and free to basally connate into a sheath but apices acute and triangular. Leaves are parallel veined, with 2 (—3) veins. Reproductive organs are usually unisexual but hermaphroditic cones occasionally occur. Male cones are terminal to twigs, or pedunculate, or sessile and axillary to leaves, or clustered at nodes, bear multiple pairs/whorls of bracts each of which enclose an axillary male reproductive unit. The male reproductive unit is a shortened shoot and usually consists of a pair of bracteoles enclosing 1 microsporangiophore. The microsporangiophore is fused or distally furcated, and terminated by 2—8 synangia. The synangium is sessile to pedicellate, consists of 2—3 microsporangia, the latter opening by horizontal slits. At maturity, the microsporangiophore is elongated outside the bracteoles and terminated by a few free or fused synangia which produce polyplicate pollen bearing longitudinal ridges and furrows. The female reproductive units (FRUs) or compound female cones are directly terminal to twigs, or pedunculate or sub-sessile or sessile at nodes. The compound female cones if present are trimerous or bimerous, bear 1 to multiple whorls/pairs of leaf-like or specialized bracts, each subtending a female reproductive unit, or only the uppermost whorl/pair of bracts being fertile and the inferior whorls/pairs of bracts becoming sterile. Cone bracts are sometimes modified into dry and membranous, or dry and coriaceous, or fleshy and colourful. Seeds bear an outer envelope and an inner integument which usually extends upward and passes through the opening of the outer envelope, forming a thin and hollow micropylar tube. Micropylar tubes varying in length and shape, 0.2—4 mm long, straight, curved or coiled.
In 1829, the family Ephedraceae was instituted by the Belgian botanist Barthélemy-Charles Dumortier (1797—1878) , who only gave a brief familial diagnosis “ovaire supère stylifère; écailles opposes; ovaire monogyne”. In modern plant taxonomy, the Ephedraceae are usually characterized by features of the sole extant Ephedra[7, 95–99]. However, abundant ephedroid fossil plants from the Early Cretaceous have increasingly broadened our understanding of the circumscription and character variation of the family, so an emended familial diagnosis is provided here. The key diagnoses (Figure 5) of Ephedraceae include enveloped ovules with extruded micropylar tubes (i.e., female reproductive unit), linear leaves opposite and decussate or ternately whorled and having 2—3 parallel veins. In light of the present study, Ephedraceae sensu lato contain Ephedra L. with ca. 50 living species, 4 macrofossil-species (i.e., E. carnosa Yang et Wang, E. archaeorhytidosperm Yang et al., E. hongtaoi Wang et Zheng, E. verticillata Cladera et al. [61–64]), and 2 seed fossil-species (i.e., E. portugallica Rydin et al. and E. drewriensis Rydin et al. ) as well as ephedroid macrofossils Alloephedra Tao et Yang [57, 65, 66], Gurvanella Krassilov [67–69], Liaoxia Cao et Wu , Siphonospermum Rydin et Friis , Leongathia Krassilov et al. , Amphiephedra Miki , and Chengia gen. nov. presented herein, indicating higher generic diversity through time. Early Cretaceous strata of Northeast China contain a plethora of well-preserved macrofossils (that sometimes are comparatively complete individuals) of Ephedra and ephedroids that show different evolutionary stages including primitive and derived characters of Ephedraceae, and in this respect Northeast China and adjacent areas that yield the famous Jehol Biota [102–112] might represent either the centre of origination or one of centres for early diversification of the family.
The generic name “Chengia” is dedicated to the late eminent botanist Cheng Wan-Chun (1904—1983) (Chinese Academy of Forestry, Beijing) who has made enormous contributions to the taxonomy of gymnosperms; the specific epithet “laxispicata”, stemming from the Latin “laxus” + “spicatus”, refers to the loosely arranged female spike which is a conspicuous feature of this fossil-species.
Generic and specific diagnosis
Reproductive shoots branch oppositely at swollen nodes. Internodes bear numerous longitudinal striations. Leaves that subtend lateral branches are long and linear. Female spikes are terminal to twigs or are subtended by the leaf, possessing multiple pairs of loosely arranged female reproductive units. Nodes and internodes of female spikes prominent. Female reproductive units consist of decussately opposite seeds and subtending bracts. Seeds enveloped, with distal micropylar tube.
Description: (see Results — Description of the specimens).
PE 2012041619A, B (Figure 2a—b) (designated here. Part and counterpart specimens).
Stratigraphic horizon and age
Dawangzhangzi Bed in the middle part of the Yixian Formation or Xinfangzi Bed in the lower part of the Yixian Formation (the Early Aptian—earliest Late Aptian of the Early Cretaceous) (see Methods as follows).
Chinese National Herbarium (PE), Institute of Botany, Chinese Academy of Sciences, Beijing, China.
The plant-bearing beds at Dawangzhangzi Village (Figure 6, left), Lingyuan City, Chaoyang District, Liaoning Province, Northeast China have been known since the 1930s. Fossil fish Lycoptera jeholensis Grabau, monocotyledonous plants Potamogeton jeholensis Yabe et Endô, Potamogeton ? sp., gymnosperms Schizolepis jeholensis Yabe et Endô and Czekanowskia rigida Heer were first reported from this Early Cretaceous locality [113, 114]. Subsequently, Potamogeton jeholensis was reclassified as another angiosperm Ranunculus jeholensis (Yabe et Endô) Miki  or an ephedroid plant Ephedrites chenii (Cao et Wu) Guo et X.W. Wu [67, 76] (correctly cited as Ephedrites cheniae Guo et X.W. Wu [57, 75]), which is synonymous with Liaoxia cheniae (Guo et X. W. Wu) Cao et S. Q. Wu . Moreover, Miki  described a new ephedroid plant Amphiephedra rhamnoides Miki from this locality, which is different from our new plant Chengia laxispicata gen. et sp. nov. in bearing “verticillate, scaly leaves on the lateral branches that look more like short shoots” (translated from the original description in Japanese by Atsushi Yabe, 2012, personal communication).
Adjacent to Dawangzhangzi Village of Lingyuan City, an ephedroid plant Ephedrites? elegans Sun et Zheng  was described from the Jianshangou Bed in the lower part of the Yixian Formation of Huangbanjigou Village (Figure 6, middle), Beipiao City, Chaoyang District, Liaoning Province, Northeast China. Ephedrites? elegans (specimens examined: PB 19175A, B) also bears loosely arranged spikes with clear nodes and internodes, but it differs from our new plant Chengia laxispicata gen. et sp. nov. in having possibly 3—5 bracts per whorl in spikes (see original authors’ description) . Another superficially similar specimen was also reported from the Early Cretaceous Lycoptera beds of Manlaj, eastern Gobi in Mongolia, which Krassilov called “Potamogeton-like spike” bearing 2 or 3 nutlets per node (see original author’s description) .
The specimens used in this study were collected from Dawangzhangzi Village (Figure 6, left), Lingyuan City, Liaoning Province, Northeast China and occur as part and counterpart on a slab of light grey to yellowish, finely laminated siltstone (Figure 2a–b). The plant fossils are preserved as compressions/impressions only with little organic material remaining, and a piece of Lycoptera fish fossil is also present on the same slab. The stratum yielding the present specimens belongs to the informally named “Lycoptera Beds” (i.e., Xinfangzi Bed), which corresponds to the “Jianshangou Bed” in the lower part of the Yixian Formation of Huangbanjigou Village, Beipiao City, Liaoning Province, Northeast China  (Figure 6). However, some palaeontologists [104–107] designated the statum as the Dawangzhangzi Bed, which corresponds to the middle part of the Yixian Formation, overlying the Jianshangou Bed. On the basis of radiometric dating, the Jianshangou and Dawangzhangzi Beds of the middle-lower Yixian Formation are given a geological age ranging from ca. 125 to 120 Ma [104–112], corresponding to the Early Aptian—earliest Late Aptian of the Early Cretaceous in the newest Geologic Time Scale (GTS 2012) .
The fossils (Figures 2 and 3) were photographed with digital cameras (Nikon D700 and Panasonic DMC—FZ30) and under a microscope (Nikon Eclipse E600). Previously published ephedroid macrofossils from the lower part of the Yixian Formation of Huangbanjigou Village (Figure 6, middle), Beipiao City, Liaoning Province, Northeast China were examined at the Institute of Botany (CAS), Beijing (specimens prefixed PE), and Nanjing Institute of Geology and Palaeontology (CAS), Nanjing (specimens prefixed PB). The modern gnetalean plants (Figure 1a–c) were photographed respectively at Chayu (Tibet, China), Shenzhen Fairy Lake Botanic Garden (Guangdong, China), and Dahlem Botanic Garden (Berlin, Germany). Simplified phylogenetic trees (Figure 1d) of the Gnetales within seed plants were adapted from the literature . The illustrations (Figure 4a–b) were drawn using a pointed pen and black inks . The illustrations (Figures 5 and 6) were drawn using CorelDraw 10.0 programme (Chinese edition, Tianlong Corporation, Beijing).
To comply with requirements of the International Code of Nomenclature for algae, fungi, and plants (Melbourne Code), we have deposited paper copies of this article in libraries at the Institute of Botany, Chinese Academy of Sciences, Beijing; Peking University, Beijing; the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing; Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing; Kunming Institute of Botany, Chinese Academy of Sciences, Kunming; Sun Yat-sen University, Guangzhou; Lanzhou University, Lanzhou; Jilin University, Changchun; Shenyang Normal University, Shenyang; National Museum of Natural History, Smithsonian Institution, Washington, D.C.; Indiana University, Bloomington; University of California Museum of Paleontology, Berkeley; Florida Museum of Natural History, the University of Florida, Gainesville; Peabody Museum of Natural History, Yale University, New Haven; Ohio University, Athens; the University of Kansas, Lawrence; the University of Birmingham, Birmingham; National Museum Wales, Cardiff, UK; the Swedish Museum of Natural History, Stockholm; Geological Institute, ETH, Zürich; Charles University, Prague; Institute of Evolution, University of Haifa, Israel; the Staatliche Museum für Naturkunde, Stuttgart; Hungarian Natural History Museum, Budapest; Chuo University, Tokyo; National Museum of Nature and Science, Tsukuba, Japan; National Institute of Carpology, Moscow; Far Eastern Geological Institute, Far Eastern Biological and Soil Institute, the Academy of Sciences of the USSR, Vladivostok; The University of Adelaide, Adelaide, Australia.
We greatly thank two anonymous reviewers for helpful comments on the manuscript. Dr. Shi Gongle and Mr. Yuan Daojun, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (CAS), Nanjing for access to the specimen collections. Dr. Wang Kang, Beijing Botanic Garden, Mr. Ma Xintang and Liu Bing, Institute of Botany, CAS, Beijing for sending the images of Welwitschia, Gnetum, and Ephedra. Mr. Sun Yingbao, Institute of Botany, CAS, Beijing for drawing the reconstruction of this fossil plant. Mr. Zong Ruiwen, China University of Geosciences, Wuhan for graphing the map. Dr. Harufumi Nishida, Chuo University, Tokyo, Dr. Atsushi Yabe, National Museum of Nature and Science, Tsukuba, Dr. Valentin Krassilov, Institute of Evolution, University of Haifa, Mrs. Anna Pavlova, National Institute of Carpology, Moscow, Dr. Eugenia Bugdaeva, Far Eastern Biological and Soil Institute, the Academy of Sciences of the USSR, Vladivostok, and Dr. Wang Shijun, Institute of Botany, CAS, Beijing for providing us with some key references. Dr. Atsushi Yabe, Mr. Makoto Ishimura, Chigasaki City for the linguistic assistance in Japanese. This work was supported by the National Natural Science Foundation of China (nos. 30970177, 31270238, 40972015, and 40830209), the State Key Laboratory of Systematic and Evolutionary Botany, CAS (no. 56176G1044), and the State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, CAS (no. 123106) to QW and YY.
- Arber EAN, Parkin J: Studies on the evolution of the angiosperms, the relationship of the angiosperms to the Gnetales. Ann Bot. 1908, 22: 489-515.Google Scholar
- Mehra PN: Occurrence of hermaphrodite flowers and the development of the female gametophyte in Ephedra intermedia Schrenk et Mey. Ann Bot. 1950, 14: 165-180.Google Scholar
- Endress PK: Structures and function of female and bisexual organ complexes in Gnetales. Int J Plant Sci. 1996, 157 (6 suppl.): S113-S125.Google Scholar
- Yang Y: Ph.D. thesis. Systematics and evolution of Ephedra L. (Ephedraceae) from China. 2002, Beijing: Institute of Botany, Chinese Academy of SciencesGoogle Scholar
- Muhammad AF, Sattler R: Vessel structure of Gnetum and the origin of angiosperms. Am J Bot. 1982, 69: 1004-1021. 10.2307/2442898.Google Scholar
- Gifford EM, Foster AS: Comparative morphology of vascular plants. 1989, New York: WH Freeman, 3Google Scholar
- Kubitzki K: Gnetatae. The Families and Genera of Vascular Plants, vol. I. Pteridophytes and gymnosperms. Edited by: Kramer KU, Green PS. 1990, Berlin, Heidelberg: Springer-Verlag, 378-391.Google Scholar
- Yang Y: Ontogeny of triovulate cones of Ephedra intermedia and origin of the outer envelope of ovules of Ephedraceae. Am J Bot. 2004, 91: 361-368. 10.3732/ajb.91.3.361.PubMedGoogle Scholar
- Anderson JM, Anderson HM, Cleal CJ: Brief history of the gymnosperms: classification, biodiversity, phytogeography and ecology. Strelitzia. 2007, 20: 1-280.Google Scholar
- Rydin C, Khodabandeh A, Endress PK: The female reproductive unit of Ephedra (Gnetales): comparative morphology and evolutionary perspectives. Bot J Linn Soc. 2010, 163: 387-430. 10.1111/j.1095-8339.2010.01066.x.PubMedGoogle Scholar
- Friedman WE: Double fertilization in Ephedra, a non-flowering seed plant: its bearing on the origin of angiosperms. Science. 1990, 247: 951-954. 10.1126/science.247.4945.951.PubMedGoogle Scholar
- Friedman WE, Carmichael JS: Double fertilization in Gnetales: implications for understanding reproductive diversification among seed plants. Int J Plant Sci. 1996, 157 (6 suppl.): S77-S94.Google Scholar
- Yang Y, Fu DZ, Wen LH: On double fertilization in Ephedra. Adv Plant Sci. 2000, 3: 67-74.Google Scholar
- Rudall PJ, Hilton J, Vergara-Silva F, Bateman RM: Recurrent abnormalities in conifer cones and the evolutionary origins of flower-like structures. Trends Plant Sci. 2011, 16: 151-159. 10.1016/j.tplants.2010.11.002.PubMedGoogle Scholar
- Yang Y, Fu DZ, Wang Q: Origin of flowers: hypotheses and evidence. Acta Bot Boreal-Occident Sin. 2004, 24: 2366-2380.Google Scholar
- McCoy SR, Kuehl JV, Boore JL, Raubeson LA: The complete plastid genome sequence of Welwitschia mirabilis: an unusually compact plastome with accelerated divergence rates. BMC Evol Biol. 2008, 8: 130-10.1186/1471-2148-8-130.PubMed CentralPubMedGoogle Scholar
- Rothwell GW, Crepet WL, Stockey RA: Is the anthophyte hypothesis alive and well? New evidence from the reproductive structures of Bennettitales. Am J Bot. 2009, 96: 296-322. 10.3732/ajb.0800209.PubMedGoogle Scholar
- Doyle JA: Molecular and fossil evidence on the origin of angiosperms. Annu Rev Earth Planet Sci. 2012, 40: 301-326. 10.1146/annurev-earth-042711-105313.Google Scholar
- Crane PR: Phylogenetic analysis of seed plants and the origin of angiosperms. Ann Missouri Bot Gard. 1985, 72: 716-793. 10.2307/2399221.Google Scholar
- Doyle JA, Donoghue MJ: Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Bot Rev. 1986, 52: 321-431. 10.1007/BF02861082.Google Scholar
- Crane PR, Friis EM, Pedersen KR: The origin and early diversification of angiosperms. Nature. 1995, 374: 27-33. 10.1038/374027a0.Google Scholar
- Doyle JA: Seed plant phylogeny and the relationships of Gnetales. Int J Plant Sci. 1996, 157 (6 suppl.): S3-S39.Google Scholar
- Doyle JA: Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. Mol Phylogen Evol. 1998, 9: 448-462. 10.1006/mpev.1998.0506.Google Scholar
- Nixon KC, Crepet WL, Stevenson D, Friis EM: A reevaluation of seed plant phylogeny. Ann Missouri Bot Gard. 1994, 81: 484-533. 10.2307/2399901.Google Scholar
- Friis EM, Crane PR, Pedersen KR, Bengtson S, Donoghue PCJ, Grimm GW, Stampanoni M: Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature. 2007, 450: 549-553. 10.1038/nature06278.PubMedGoogle Scholar
- Friis EM, Pedersen KR, Crane PR: Early cretaceous mesofossils from Portugal and eastern North America related to the Bennettitales—Erdtmanithecales—Gnetales group. Am J Bot. 2009, 96: 252-283. 10.3732/ajb.0800113.PubMedGoogle Scholar
- Bowe LM, Coat G, dePamphilis CW: Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers. Proc Natl Acad Sci USA. 2000, 97: 4092-4097. 10.1073/pnas.97.8.4092.PubMed CentralPubMedGoogle Scholar
- Hajibabaei M, Xia JN, Drouin G: Seed plant phylogeny: gnetophytes are derived conifers and a sister group to Pinaceae. Mol Phylogen Evol. 2006, 40: 208-217. 10.1016/j.ympev.2006.03.006.Google Scholar
- Braukmann TWA, Kuzmina M, Stefanović S: Loss of all plastid ndh genes in Gnetales and conifers: extent and evolutionary significance for the seed plant phylogeny. Curr Genet. 2009, 55: 323-337. 10.1007/s00294-009-0249-7.PubMedGoogle Scholar
- Rydin C, Korall P: Evolutionary relationships in Ephedra (Gnetales)—with implications for seed plant phylogeny. Int J Plant Sci. 2009, 170: 1031-1043. 10.1086/605116.Google Scholar
- Zhong BJ, Yonezawa T, Zhong Y, Hasegawa M: The position of Gnetales among seed plants: overcoming pitfalls of chloroplast phylogenomics. Mol Biol Evol. 2010, 27: 2855-2863. 10.1093/molbev/msq170.PubMedGoogle Scholar
- Price RA: Systematics of the Gnetales: a review of morphological and molecular evidence. Int J Plant Sci. 1996, 157 (6 suppl.): S40-S49.Google Scholar
- Huang JL, Giannasi DE, Price RA: Phylogenetic relationships in Ephedra (Ephedraceae) inferred from chloroplast and nuclear DNA sequences. Mol Phylogen Evol. 2005, 35: 48-59. 10.1016/j.ympev.2004.12.020.Google Scholar
- Maheshwari P, Vasil V: Gnetum. 1961, New Delhi: Council of Scientific & Industrial ResearchGoogle Scholar
- Shindo S, Ito M, Ueda K, Kato M, Hasebe M: Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evol Develop. 1999, 1: 180-190. 10.1046/j.1525-142x.1999.99024.x.Google Scholar
- Shindo S, Sakakibara K, Sano R, Ueda K, Hasebe M: Characterization of a floricaula/leafy homologue of Gnetum parvifolium and its implications for the evolution of reproductive organs in seed plants. Int J Plant Sci. 2001, 162: 1199-1209. 10.1086/323417.Google Scholar
- Stapf O: Die Arten der Gattung Ephedra (monograph). Denkschr Kaiserl Akad Wiss Math-Naturwiss Kl. 1889, 56: 1-112.Google Scholar
- Florin R: Über einige neue oder wenig bekannte asiatische Ephedra-Arten der Sect. Pseudobaccatae Stapf. Kongl Svensk Vetensk Akad Handl, 3 Ser. 1933, 12: 264-289.Google Scholar
- Takaso T: Structural changes in the apex of the female strobilus and the initiation of the female reproductive organ (ovule) in Ephedra distachya L. and E. equisetina Bge. Acta Bot Neerl. 1984, 33: 257-266.Google Scholar
- Yang Y: Ontogeny and metamorphic patterns of female reproductive organs of Ephedra sinica Stapf (Ephedraceae). Acta Bot Sin. 2001, 43: 1011-1017.Google Scholar
- Pilger R: Gymnospermae. Die Natürlichen Pflanzenfamilien, band 13. Edited by: Engler A, Prantl K. 1926, Leipzig: Wilhelm EnglemannGoogle Scholar
- Hufford L: The morphology and evolution of male reproductive structures of Gnetales. Int J Plant Sci. 1996, 157 (6 suppl.): S95-S112.Google Scholar
- Wang ZQ: A new Permian Gnetalean cone as fossil evidence for supporting current molecular phylogeny. Ann Bot. 2004, 94: 281-288. 10.1093/aob/mch138.PubMed CentralPubMedGoogle Scholar
- Ash SR: Late Triassic plants from the Chinle Formation in northeastern Arizona. Palaeontology. 1972, 15: 598-618.Google Scholar
- Ash SR: Dinophyton, a problematical new plant genus from the Upper Triassic of the southeastern United States. Palaeontology. 1970, 13: 646-663.Google Scholar
- Krassilov VA, Ash SR: On Dinophyton—protognetalean Mesozoic plant. Palaeontogr Abt B. 1988, 208: 33-38.Google Scholar
- Cornet B: The leaf venation and reproductive structures of a late Triassic angiosperm: Sanmiguelia lewisii. Evol Theory. 1986, 7: 231-309.Google Scholar
- Friis EM, Crane PR, Pedersen KR: Early flowers and angiosperm evolution. 2011, Cambridge: Cambridge University PressGoogle Scholar
- Cornet B: A new gnetophyte from the late Carnian (Late Triassic) of Texas and its bearing on the origin of the angiosperm carpel and stamen. Flowering plant origin, evolution, and phylogeny. Edited by: Taylor DW, Hickey LJ. 1996, New York: Chapman Hall, 32-67.Google Scholar
- Wu XW, He YL, Mei SW: Discovery of Ephedrites from the Lower Jurassic Xiaomeigou Formation, Qinhai. Acta Palaeobot Palynol Sin. 1986, 1: 13-21.Google Scholar
- Li PJ, He YL, Wu XW, Mei SW, Li BY: Early and Middle Jurassic strata and their floras from northeastern border of Qaidam Basin, Qinghai. 1988, Nanjing: Nanjing University PressGoogle Scholar
- Crane PR: The fossil history of the Gnetales. Int J Plant Sci. 1996, 157 (6 suppl.): S50-S57.Google Scholar
- Crane PR, Upchurch GR: Drewria potomacensis gen. et sp. nov., an early Cretaceous member of Gnetales from the Potomac Group of Virginia. Am J Bot. 1987, 74: 1722-1736. 10.2307/2444143.Google Scholar
- Krassilov VA: New floral structure from the Lower Cretaceous of Lake Baikal area. Rev Palaeobot Palynol. 1986, 47: 9-16. 10.1016/0034-6667(86)90003-5.Google Scholar
- Krassilov VA: Diversity of Mesozoic gnetophytes and the first angiosperms. Paleontol J. 2009, 43: 1272-1280. 10.1134/S0031030109100098.Google Scholar
- Doyle JA, Donoghue MJ: Phylogenies and angiosperm diversification. Paleobiology. 1993, 19: 141-167.Google Scholar
- Yang Y: A review on gnetalean megafossils: problems and perspectives. Taiwania. 2010, 55: 346-354.Google Scholar
- Dilcher DL, Bernardes-de-Oliveira ME, Pons D, Lott TA: Welwitschiaceae from the Lower Cretaceous of northeastern Brazil. Am J Bot. 2005, 92: 1294-1310. 10.3732/ajb.92.8.1294.PubMedGoogle Scholar
- Guo SX, Sha JG, Bian LZ, Qiu YL: Male spike strobiles with Gnetum affinity from the Early Cretaceous in western Liaoning, Northeast China. J Syst Evol. 2009, 47: 93-102. 10.1111/j.1759-6831.2009.00007.x.Google Scholar
- Rydin C, Mohr B, Friis EM: Cratonia cotyledon gen. et sp. nov.: a unique Cretaceous seedling related to Welwitschia. Proc R Soc Lond B. 2003, 270 (suppl): S29-S32. 10.1098/rsbl.2003.0044.Google Scholar
- Yang Y, Wang Q: The earliest fleshy cone of Ephedra from the Early Cretaceous Yixian Formation of Northeast China. PLoS One. 2013, 8: e53652-10.1371/journal.pone.0053652.PubMed CentralPubMedGoogle Scholar
- Yang Y, Geng BY, Dilcher DL, Chen ZD, Lott TA: Morphology and affinities of an Early Cretaceous fossil—Ephedra archaeorhytidosperma sp. nov. (Ephedraceae—Gnetopsida). Am J Bot. 2005, 92: 231-241. 10.3732/ajb.92.2.231.PubMedGoogle Scholar
- Wang X, Zheng SL: Whole fossil plants of Ephedra and their implications on the morphology, ecology and evolution of Ephedraceae (Gnetales). Chin Sci Bull. 2010, 55: 1511-1519. 10.1007/s11434-010-3069-8.Google Scholar
- Cladera G, Fueyo GMD, de Seoane LV, Archangelsky S: Early Cretaceous riparian vegetation in Patagonia, Argentina. Rev Mus Argentino Cienc Nat, N S. 2007, 9: 49-58.Google Scholar
- Tao JR, Yang Y: Alloephedra xingxuei gen. et sp. nov., an early Cretaceous member of Ephedraceae from Dalazi Formation in Yanji Basin, Jilin Province of China. Acta Palaeontol Sin. 2003, 42: 208-215.Google Scholar
- Liu HM, Ferguson DK, Hueber FM, Li CS, Wang YF: Taxonomy and systematics of Ephedrites cheniae and Alloephedra xingxuei (Ephedraceae). Taxon. 2008, 57: 577-582.Google Scholar
- Sun G, Zheng SL, Dilcher DL, Wang YD, Mei SW: Early angiosperms and their associated plants from western Liaoning, China. 2001, Shanghai: Shanghai Scientific and Technological Education Publishing HouseGoogle Scholar
- Krassilov VA: Early Cretaceous flora of Mongolia. Palaeontogr Abt B. 1982, 181: 1-43.Google Scholar
- Akhmetiev MA, Krassilov VA: Recollected proangiosperms and correlation of Upper Mesozoic lacustrine deposits in East Asia. Stratigr Geol Correlation. 2002, 10: 414-418.Google Scholar
- Duan SY: The oldest angiosperm—a tricarpous female reproductive fossil from western Liaoning Province, NE China. Sci China Ser D Earth Sci. 1998, 41: 14-20. 10.1007/BF02932415.Google Scholar
- Wu SQ: A preliminary study of the Jehol flora from western Liaoning. Palaeoworld. 1999, 11: 7-57.Google Scholar
- Wu SQ: Land plants. The Jehol Fossils: the emergence of feathered dinosaurs, beaked birds and flowering plants. Edited by: Chang MM, Chen PJ, Wang YQ, Wang Y, Miao DS. 2003, Shanghai: Shanghai Scientific and Technical Publishers, 167-177.Google Scholar
- Wang X: The dawn angiosperms: uncovering the origin of flowering plants. 2010, Berlin: SpringerGoogle Scholar
- Rydin C, Wu SQ, Friis EM: Liaoxia (Gnetales): ephedroids from the Early Cretaceous Yixian Formation in Liaoning, northeastern China. Pl Syst Evol. 2006, 262: 239-265. 10.1007/s00606-006-0481-2.Google Scholar
- Yang Y: The nomenclature of fossil Ephedraceae. Taxon. 2007, 56: 1271-1273. 10.2307/25065920.Google Scholar
- Guo SX, Wu XW: Ephedrites from latest Jurrassic Yixian Formation in western Liaoning, Northeast China. Acta Palaeontol Sin. 2000, 39: 81-91.Google Scholar
- Rydin C, Friis EM: A new Early Cretaceous relative of Gnetales: Siphonospermum simplex gen. et sp. nov. from the Yixian Formation of Northeast China. BMC Evol Biol. 2010, 10: 183-10.1186/1471-2148-10-183.PubMed CentralPubMedGoogle Scholar
- Krassilov VA, Dilcher DL, Douglas JG: New ephedroid plant from the Lower Cretaceous Koonwarra fossil bed, Victoria, Australia. Alcheringa. 1998, 22: 123-133. 10.1080/03115519808619195.Google Scholar
- Cao ZY, Wu SQ, Zhang PA, Li JR: Discovery of fossil monocotyledons from Yixian Formation, western Liaoning. Chin Sci Bull. 1998, 43: 230-233. 10.1007/BF02898918.Google Scholar
- Zheng SL: Plants. Standard sections of Tuchengzi Stage and Yixian Stage and their stratigraphy, palaeontology and tectonic-volcanic actions. Edited by: Wang WL, Zhang H, Zhang LJ, Zheng SL, Yang FL, Li ZT, Zheng YJ, Ding QH. 2004, Beijing: Geological Publishing House, 203-225.Google Scholar
- Rydin C, Pedersen KR, Friis EM: On the evolutionary history of Ephedra: cretaceous fossils and extant molecules. Proc Natl Acad Sci USA. 2004, 101: 16571-16576. 10.1073/pnas.0407588101.PubMed CentralPubMedGoogle Scholar
- Rydin C, Pedersen KR, Crane PR, Friis EM: Former diversity of Ephedra (Gnetales): evidence from Early Cretaceous seeds from Portugal and North America. Ann Bot. 2006, 98: 123-140. 10.1093/aob/mcl078.PubMed CentralPubMedGoogle Scholar
- Hou LH, Zhang JY: A new fossil bird from Lower Cretaceous of Liaoning. Vertebr PalAsiat. 1993, 31: 217-224.Google Scholar
- Li PX, Cheng ZW, Pang QQ: The horizon and age of the Confuciusornis in Beipiao, western Liaoning. Acta Geol Sin. 2001, 75: 1-13.Google Scholar
- Pearson HHW: Gnetales. 1929, London: Cambridge University PressGoogle Scholar
- Martens P: Les Gnétophytes. Encyclopedia of plant anatomy 12 (2). 1971, Berlin: Gebrüder BorntraegerGoogle Scholar
- Eames A: Relationships of the Ephedrales. Phytomorphology. 1952, 2: 79-100.Google Scholar
- Yamada T, Hirayama Y, Imaichi R, Kato M: AINTEGUMENTA homolog expression in Gnetum (gymnosperms) and implications for the evolution of ovulate axes in seed plants. Evol Devel. 2008, 10: 280-287. 10.1111/j.1525-142X.2008.00237.x.Google Scholar
- Mundry M, Stützel T: Morphogenesis of the reproductive shoots of Welwitschia mirabilis and Ephedra distachya (Gnetales), and its evolutionary implications. Organ Divers Evol. 2004, 4: 91-108. 10.1016/j.ode.2004.01.002.Google Scholar
- Leslie A: Shifting functional roles and the evolution of conifer pollen-producing and seed-producing cones. Paleobiology. 2011, 37: 587-602. 10.1666/10049.1.Google Scholar
- Fu DZ: Nageiaceae—a new gymnosperm family. Acta Phytotax Sin. 1992, 30: 515-528.Google Scholar
- Fu DZ, Yang QE: A new morphological interpretation of the female reproductive organs in Ginkgo biloba L., with a phylogenetic consideration on gymnosperms. Acta Phytotax Sin. 1993, 31: 294-296. 309-317Google Scholar
- Takaso T, Tomlinson PB: Seed cone and ovule ontogeny in Metasequoia, Sequoia and Sequoiadendron (Taxodiaceae—Coniferales). Bot J Linn Soc. 1992, 109: 15-37. 10.1111/j.1095-8339.1992.tb00256.x.Google Scholar
- Tomlinson PB, Takaso T, Cameron EK: Cone and ovule development in Libocedrus (Cupressaceae)—Phenological and morphological aspects. Am J Bot. 1993, 80: 649-659. 10.2307/2445436.Google Scholar
- Yang CY: Ephedraceae. Flora Xinjangensis, vol. 1. Edited by: Yang CY. 1993, Urümqi: Xinjiang Science & Technology & Hygiene Publishing House, 87-109.Google Scholar
- Freitag H, Maier-Stolte M: Ephedraceae. Flora of the Arabian Peninsula and Socotra, vol. 1. Edited by: Miller AG, Cope TA. 1996, Edinburgh: Edinburgh University Press, 75-80.Google Scholar
- Stevenson DW: Ephedraceae. Flora of North America North of Mexico, vol. 2. Edited by: Flora of North America Editorial Committee. 1993, New York: Oxford University Press, 428-434.Google Scholar
- Fu LG, Yu YF, Riedl H: Ephedraceae. Flora of China, vol. 4 Cycadaceae through Fagaceae. Edited by: Wu ZY, Raven PR. 1999, Beijing: Science Press, and St. Louis: Missouri Botanical Garden, 97-101.Google Scholar
- Mabberley DJ: Mabberley’s plant-book: a portable dictionary of plants, their classification and uses. 2008, New York: Cambridge University Press, 3Google Scholar
- Dumortier B-C: Analyse des familles des plantes :avec l'indication des principaux genres qui s'y rattachent. 1829, Ainé : Impr. de J. CastermanGoogle Scholar
- Miki S: Mesozoic flora of Lycoptera beds in South Manchuria. Bull Mukogawa Women’s Univ (Nat Sci). 1964, 12: 13-22.Google Scholar
- Chen PJ: Distribution and spread of the Jehol Biota. Palaeoworld. 1999, 11: 1-6.Google Scholar
- Ji Q: On the Mesozoic Jehol Biota of China. Geol Rev. 2002, 48: 290-296.Google Scholar
- Wang XL, Wang YQ, Zhang FC, Zhang JY, Zhou ZH, Jin F, Hu YM, Gu G, Zhang HC: Vertebrate biostratigraphy of the Lower Cretaceous Yixian Formation in Lingyuan, western Liaoning and its neighboring southern Nei Mongol (Inner Mongolia), China. Vertebr PalAsiat. 2000, 38: 81-99.Google Scholar
- Leng Q, Friis EM: Sinocarpus decussatus gen. et sp. nov., a new angiosperm with basally syncarpous fruits from the Yixian Formation of Northeast China. Pl Syst Evol. 2003, 241: 77-88. 10.1007/s00606-003-0028-8.Google Scholar
- Chang MM, Chen PJ, Wang YQ, Wang Y, Miao DS: The Jehol Fossils: the emergence of feathered dinosaurs, beaked birds and flowering plants. 2003, Shanghai: Shanghai Scientific and Technical PublishersGoogle Scholar
- Zhou ZH, Barrett PM, Hilton J: An exceptionally preserved Lower Cretaceous ecosystem. Nature. 2003, 421: 807-814. 10.1038/nature01420.PubMedGoogle Scholar
- Zhou ZH: Evolutionary radiation of the Jehol Biota: chronological and ecological perspectives. Geol J. 2006, 41: 377-393. 10.1002/gj.1045.Google Scholar
- Chang SC, Zhang HC, Hemming SR, Mesko GT, Fang Y: Chronological evidence for extension of the Jehol Biota into southern China. Palaeogeogr Palaeoclimat Palaeoecol. 2012, 344–345: 1-5.Google Scholar
- Bugdaeva EV, Markevich VS: The age of Lycoptera beds (Jehol Biota) in Transbaikalia (Russia) and correlation with Mongolia and China. Bernissart dinosaurs and early terrestrial ecosystems. Edited by: Godefroit P. 2012, Bloomington: Indiana University Press, 452-464.Google Scholar
- Chen PJ, Wang QF, Zhang HC, Cao MZ, Li WB, Wu SQ, Shen YB: Jianshangou Bed of the Yixian Formation in West Liaoning, China. Sci China Ser D Earth Sci. 2004, 34: 883-895.Google Scholar
- Chang SC, Zhang HC, Renne PR, Fang Y: High-precision 40Ar/39Ar age for the Jehol Biota. Palaeogeogr Palaeoclimat Palaeoecol. 2009, 280: 94-104. 10.1016/j.palaeo.2009.06.021.Google Scholar
- Yabe H, Endô S: Potamogeton remains from the Lower Cretaceous ? Lycoptera beds of Jehol. Proc Imp Acad Tokyo. 1935, 11: 274-276.Google Scholar
- Yabe H, Endô S: Strobilus of Schizolepis from the Lycoptera-beds of Jehol. Proc Imp Acad Tokyo. 1934, 10: 658-660.Google Scholar
- Gradstein FM, Ogg JG, Schmitz MD, Ogg GM: The Geologic Time Scale 2012. 2012, Boston: ElsevierGoogle Scholar
- Sun YB: Drawing method of the black line chart in botanical scientific illustration. Guihaia. 2012, 32: 55-60.Google Scholar
- McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, van Reine WF P’h, Smith GF, Wiersema JH, Turland NJ: International Code of Nomenclature for algae, fungi, and plants (Melbourne Code) adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. 2012, Königstein: Koeltz Scientific BooksGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.