J Plant Res DOI 10.1007/s10265-015-0708-9
REGULAR PAPER
Fertile structures with in situ spores of a dipterid fern from the Triassic in southern China Yongdong Wang · Liqin Li · Gaëtan Guignard · David L. Dilcher · Xiaoping Xie · Ning Tian · Ning Zhou · Yan Wang
Received: 21 September 2014 / Accepted: 25 December 2014 © The Botanical Society of Japan and Springer Japan 2015
Abstract Clathropteris was a typical dipterid fern with well documented fossil record and was widely dispersed during the Mesozoic; however, our knowledge of fertile structures including in situ spores for this genus is still very limited. Here we report well-preserved compression specimens of Clathropteris obovata Oishi from the Late Triassic of Guangyuan, Sichuan Province, China. The specimens show round to oval and exindusiate sori, vertical to oblique annuli in sporangia, and in situ trilete spores with verrucate and baculate sculptures, which are comparable to dispersed spore genera of Converrucosisporites and Conbaculatisporites. Comparisons of relevant fossil taxa suggest that specimens of C. obovata from Triassic of China provide for the first time in Asia the detailed fertile structures with in situ spore characters of dipterid fossil Clathropteris. Unlike living Dipteris, Mesozoic fossils of Dipteridaceae show a high diversity and a range of complex morphology of in situ spores, thus are significant for the evolutionary links between Dipteridaceae and other related
fern clade, including Gleicheniaceae and Matoniaceae of the Gleicheniales.
Y. Wang · L. Li · N. Zhou Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China
D. L. Dilcher Department of Geology, Indiana University, 1001 E. Tenth St., Bloomington, IN 47405, USA
Y. Wang (*) Key Laboratory of Economic Stratigraphy and Palaeogeography, Chinese Academy of Sciences, Nanjing 210008, China e-mail: [email protected]
D. L. Dilcher · N. Tian College of Palaeontology, Shenyang Normal University, Shenyang 110034, China
L. Li · N. Zhou University of Chinese Academy of Sciences, Beijing 100049, China G. Guignard UMR CNRS 5276 Laboratoire de Géologie de Lyon, Département de Biologie, Université Claude Bernard Lyon 1, Herbiers de l’Université Claude Bernard Lyon 1, Villeurbanne Cedex 69622, France
Keywords Dipteridaceae · Clathropteris · Sporangia · In situ spores · Late Triassic · Sichuan · China
Introduction The Late Triassic floras of the Sichuan Basin in southern China have been well known since the 1880s. In particular, fossil plants from the coal-bearing deposits in the Upper Triassic Xujiahe (=Hsuchiaho) Formation from Guangyuan (=Kwangyuan) City of northern Sichuan Province are exceptionally preserved. Plant fossils from this location were first described by Schenk (1883) based on fragmentary specimens, representing the beginning of paleobotanical studies of Triassic plants in China. Subsequently, a series of investigations were reported on systematics
X. Xie College of Geography and Tourism, Qufu Normal University, Rizhao 276826, China Y. Wang School of Geoscience and Technology, Southwest Petroleum University, Chengdu 610500, China
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Fig. 1 Sketch map showing the fossil locality in Xujiahe town of Guangyuan, Sichuan Province, China
and paleoecology of plant fossils from the Xujiahe Formation in the northern Sichuan Basin (e.g. Huang 1992, 1995; Lee 1964; Sze 1933; Sze and Lee 1952; Wu 1999; Yang 1978; Ye et al. 1986). In the Xujiahe flora, Bennettitales are the dominant group with particularly rich taxa (e.g. Pterophyllum, Ptilophyllum, Otozamites). Ferns are the second most diverse group; sphenopsids (e.g. Neocalamites and Equisetites), pteridosperms (Ptilozamites, Lepidopteris), conifers (e.g. Podozamites and Ferganiella) and ginkgos (Baiera, Glossophyllum and Czekanowskia) are common elements (Lee 1964; Wang et al. 2010a; Wu 1999). Ferns are represented in this flora by a variety of taxa, including over 20 species ascribed to 11 genera of 4 families, i.e. Dipteridaceae, Matoniaceae, Osmundaceae and Marattiaceae (Wu 1999). Among them, the Dipteridaceae are particularly remarkable, including 10 species of four genera: Dictyophyllum, Clathropteris, Hausmannia and Thaumatopteris. Although a variety of fossil compression and impression specimens of dipterid foliages have been described from this area (e.g. Lee 1964; Sze 1933; Sze and Lee 1952; Wu 1999), the fertile structures and in situ spores of this fern group are still poorly known. Some fragmentary fertile specimens of Clathropteris have been previously noted from the Late Triassic in Guangyuan, Hechuan and neighboring regions of the Sichuan Basin (Lee 1964; Wu 1999; Ye et al. 1986), however, the detailed structures of their sporangia and in situ spores have not been well-investigated. In this paper, we describe the exceptionally preserved fertile fronds of a dipterid fern, Clathropteris obovata Oishi from the Late Triassic in Guangyuan of Sichuan Province
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based on detailed examination using both light and scanning electron microscopic observations. We offer new data on sporangia, annuli and in situ spores of this Clathropteris species, and compare with fossil and living taxa as well as with dispersed spore types. This represents the first detailed description for fertile structures of fossil Clathropteris from Asia, and thus showing crucial insights for exploring the diversity and evolution of the dipteridaceous fern clade.
Materials and methods The fossil specimens of Clathropteris obovata Oishi (Dipteridaceae) were collected from the Xujiahe town, about 5 km north of Guangyuan City, Sichuan Province (Lee 1964) (Fig. 1). Geologically, Xujiahe town is known as the type locality for the stratigraphic sequences of the Upper Triassic Xujiahe Formation which contains diverse and well-preserved fossil plants. The Xujiahe Formation is underlain by the limestone of Middle Triassic age and is covered by the Lower Jurassic strata. This formation consists mainly of yellow and grey sandstones, shale, and sandy shale, intercalated with carbonaceous shales and coal seams, that yield abundant fossil plants. Four lithological Members (i.e. Members 1–4) are recognized representing a deltaic estuary sandbar and delta plain swamp sedimentary environment (Wang et al. 2010a, b). The age of this flora is designated as Norian to Rhaetian based on associated invertebrate fauna (such as bivalves, ostracods, conchostracas) and palynological assemblages (Chen et al. 1979; Liu 1982; Wu 1999; Wang et al. 2010a, b).
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Diverse fossil plant remains were mainly documented from Members 1 and 3 of this formation (Fig. 2) (Huang 1992, 1995; Wang et al. 2010a). Three well-preserved compression specimens of Clathropteris obovata, including both sterile and fertile leaves, were collected from a bed of black and greyish-black shale and coal seams in the Member 3 of the Xujiahe Formation (Fig. 2). The structure and organization of fertile organs were found in an extremely fine condition of preservation. The soral material was removed mechanically from the fertile pinnule and first treated with hydrochloric acid (HCl) and then hydrofluoric acid (HF), followed by a maceration in Schultz solution. After washing with water, they
were then treated with a 5 % ammonia solution for several min followed by several changes in distilled water. Sporangia and spore material was used for slide preparation and observed under a light microscope (LM). For scanning electron microscope (SEM), material was placed on sample stubs with double-sided sticky tape. They were then sputter-coated with gold and viewed on a JSM 6300 scanning electron microscope at an acceleration voltage of 15–20 kV. All specimens (with registration numbers PB2808-1, PB 2808-4 and PB2808-5), slides and SEM stubs are housed in the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China. In addition, an extant Dipteris specimen from the herbarium collection at the Botanical Garden of Lyon, France was used for comparision. The specimen Dipteris conjugata Reinword was collected from Mont Koghi at 400 m altitude in New Caledonia in 1911 with the registration number LYJB000854. The living sporangia material was observed under SEM for comparison of fossil dipterids with respect to their fertile structures and in situ spores.
Results Systematic descriptions Order—Filicales Family—Dipteridaceae Diels Genus—Clathropteris Brongniart Species—Clathropteris obovata Oishi Figs. 3, 4, 5, 6, 7
Fig. 2 The stratigraphical column and fossil plant horizon of the Upper Triassic Xujiahe Formation in Guangyuan, Sichuan. 1 Limestone, 2 conglomerate, 3 sandstone, 4 siltstone, 5 mudstone, 6 coal, 7 plant fossil bed
Selected references. 1932 Clathropteris obovata, Oishi, p. 291, pl. 30, Fig. 2; pl. 32, Fig. 1 1949 Clathropteris meniscoides, Sze, p. 6, pl. 1, Fig. 5 (=Sze et al. 1963, pl. 27, Fig. 4) 1961 Clathropteris obovata, Harris, p. 123, Fig. 42 1964 Clathropteris meniscoides, Lee, p. 108, pl. 2, Figs. 2a, 3, 4; pl. 3, Figs. 1, 2, 3, 4, 5, 6; text-Fig. 3 1976 Clathropteris obovata, Li, Cao and Wu, p. 109, pl. 1l9, Fig. 5 1980 Clathropteris obovata, Wu, Ye and Li, p. 94, pl. 11, Figs. 1, 2; pl. 12, Figs. 5, 6 Age and horizon. Late Triassic (Norian- Rhaetian), the Xujiahe Formation. Locality. Xujiahe Town, Guangyuan City, Sichuan Province. Material studied. Three specimens with registration numbers PB2808-1, PB2808-4 and PB2808-5 in paleobotanical collection, NIGPAS.
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Fig. 3 Clathropteris obovata Oishi from the Upper Triassic in Guangyuan, Sichuan, China (a– e LM photos). a A fertile pinna, the round to oval impression left behind is the receptacle of sori/sporangia. PB 2808-4. bar 1 cm; b a fertile pinna showing rectangular meshes of venation and the distribution of sori. In this slab, two layers of pinnae are preserved; the second layer of pinna is marked by black and white arrows. bar 1 cm; c detail of b, showing the distribution of sori and sori impression in meshes. PB2808-5, bar 0.5 cm; d three sterile pinnae showing distinct midveins and rectangular meshes. Pinna A and pinna B are overlapped; pinna C is covered by pinnae A and B. PB2808-1. The marginal lobes are marked in left part of pinna a with white dot line, which are indistinct due to the preservation status. bar 1 cm; e higher magnification of two sori in a mesh. bar 0.67 mm
Megafossil. The specimens of Clathropteris obovata Oishi from Guangyuan of Sichuan are represented by several sterile and fertile leaves preserved as compressions (Fig. 3a, b, d). The specimen shows fragments of the sterile pinnae preserved together in a slab (Fig. 3d). They represent the middle to upper part of a sterile leaf and are usually overlapping in preservation, but show distinct midveins and venation patterns. Two fertile specimens show the upper part of fronds with impression/compression of sori in the venation (Fig. 3a, b). The leaf is moderate in size, and the pinna is obovate in outline, more than 12 cm long and 5 cm wide for sterile pinnae (Fig. 3d) and over 5.5 cm long
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and 5.5–8 cm wide for fertile pinnae (Fig. 3a, b). A closer examination of the specimens shows a more or less lobbed pinna margin (Fig. 3a, d). In some cases, the marginal lobe is indistinct due to incomplete preservation of the specimens. The midvein (midrib) is slender, straight or slightly undulated. Secondary veins arise from the midvein at intervals of 8–14 mm, making an angle of about 40°–50° (rarely over 60°) to the base with midvein. Tertiary veins arise at almost right angle to the secondary ones, forming a more or less rectangular mesh of the Clathropteris-type. These meshes vary from 4–7 mm wide and 8–10 mm long for fertile pinna, 4–8 mm wide and 8–12 mm long for sterile
J Plant Res Fig. 4 Clathropteris obovata Oishi from the Upper Triassic in Guangyuan, Sichuan, China showing details of sori and sporangia (a–d LM photos, e–h SEM photos). a Detail of Fig. 3b showing the impression of circular sori in vein meshes. The secondary veins (S), tertiary veins (T) and blind veins (B) are present. bar 1.25 mm; b-d the circular to oval and exindusiate sori consisting of 10–20 sporangia. bar 0.67 mm (b, d); bar 1.25 mm (c); e two more or less rounded and connected sori consisting of several sporangia. bar 270 μm; f detail of e, showing three sporangia with well-developed annuli. bar 71.4 μm; g detail of e, showing three sporangia and annuli. bar 75 μm; h partly preserved sori showing sporangia and annuli. bar 93.5 μm
pinna. The finest veins tend to form rectangular meshes enclosing blind vein-endings (Figs. 3b, d, 4a, 7a, b). Sori and sporangia. Sori are well-preserved and are distributed in rectangular meshes along the midvein, about 2–5 sori per mesh (Fig. 4a). Sori are exindusiate and sporangia are shed after dehiscence to leaving a visible round to oval receptacle (Figs. 3a, c, 4a). Sori are round to oval in outline, range from 0.5–1.5 mm in size. Each sorus consists of 10–20 sporangia (Figs. 3e, 4b–d, 7c, d). Sporangia are round to oval in lateral view (viewed perpendicular to the plane of the annulus) (Fig. 7d–f), ranging from 140 to 300 μm in diameter (average 250 μm). The annulus of the sporangia is vertical to oblique, complete, and composed of
a uniserate ring of 25–30 cells, almost linear in orientation (Figs. 4e–h, 7d–f). Radial wall height of the annular cells ranges from 70 to 80 μm and thickness from 5 to 10 μm. Details of the sporangial stalks and their insertion were not visible in this material. Each sporangium contains spore masses (Fig. 5a–d) and produces about 128–230 spores based on a count of 5 sporangia. In situ spores. Spores are trilete, triangular to subtriangular in equatorial view, with round apices and concave to convex sides (Figs. 5e, 6a–j, 7g, h). Radii of laesurae are raised, straight or slightly sinuous, extending to about 0.6– 1.0 of the spore radius. Both proximal and distal surfaces of spores are covered with verrucate, baculate or granular
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Fig. 5 Clathropteris obovata Oishi from the Upper Triassic in Guangyuan, Sichuan, China showing in situ spores in macerated sporangia (SEM photos). a, b Two sporangia containing large number of spores. bar 40 μm (a); bar 38.5 μm (b); c detail of a spore mass. bar 9 μm; d a rounded triangular spore within a spore mass, showing verrucate and baculate sculptures. bar 5.3 μm; e a triangular spore showing surface sculptures. bar 7.4 μm; f detail of e, showing verrucate and baculate sculpture elements. bar 2.2 μm
sculptures up to 1.5 μm high and 1 μm wide (Figs. 5d–f, 6a–d, 7g, h). Sculptural elements cover the sporoderm and are commonly fused, forming an irregular sinuous cover (Figs. 5e, f, 6a–j, 7g, h). Exine is thin, approximately 0.5 μm thick, excluding sculpture. No perispore is observed. Weakly to strongly developed interradial folds are generally present. Spore size ranges from 22 to 65 μm in equatorial diameter (mean 41 μm).
Discussion The Dipteridaceae have a well-established fossil record extending from the Triassic to the Cretaceous in Eurasia, North America and Gondwana (Cantrill 1995; Escapa et al. 2011; Tidwell and Ash 1994). Fossil taxa of the Mesozoic Dipteridaceae are often regarded as indicators for humid, warm-temperate to subtropical climatic conditions (e.g. Bomfleur and Kerp 2010; Van Konijnenburg-van Cittert 2002; Wang et al. 2009). Clathropteris is one of the
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representative fossil genera of the Dipteridaceae in the Mesozoic. It is widely recorded in Late Triassic and Early Jurassic floras of Eurasia, North America, as well as Argentina and Antarctica (Bomfleur and Kerp 2010; Frenguelli 1941; Herbst 1966). It is a key taxon of the Dictyophyllum–Clathropteris assemblage of the Late Triassic to Early Jurassic in both northern and southern China phytoprovinces (Hsü et al. 1979; Li et al. 1976; Sze 1949; Sun 1981; Sze et al. 1963; Sze and Chow 1964; Wang 2002; Wang et al. 2009; Wu et al. 1980; Zhang and Zheng 1987; Zhou 1984, 1995). Clathropteris was proposed by Brongniart (1828) for specimens with reticulate veins from the Rhaetic beds in Scania. The genus is characterized by large, palmately compound fronds and a unique, orthogonal venation pattern of secondary and tertiary veins (Tidwell and Ash 1994). The original specimens from the Upper Triassic Xujiahe Formation in Guangyuan of Sichuan were first described as Clathropteris meniscoides by Lee (1964) when she studied plant fossils from this locality. Later, these specimens were assigned to Clathropteris obovata Oishi (Li et al.
J Plant Res Fig. 6 Clathropteris obovata Oishi from the Upper Triassic in Guangyuan, Sichuan, China showing in situ spores (a–d SEM photos, e–j LM photos). a, b Distal view of spores. bar 7 μm (a); bar 7 μm (b); c, d proximal view of spores showing trilete marks. bar 7.7 μm; e–j light microphotos of in situ spores. bar 12.5 μm
1976), a Rhaetic plant proposed by Oishi (1932) from the Nariwa Flora in Japan. Fossil specimens from Guangyuan of Sichuan, China are morphologically similar to the type specimens of C. obovata from Japan in having obovateshaped pinnae and similar venation type. However, Oishi’s diagnosis was proposed based on sterile pinnae, yielding no information of the fertile structures. Harris (1961) gave an emended diagnosis of C. obovata based on Yorkshire materials, but added no detailed data on soral structures. Lee (1964) and Li et al. (1976) did preliminary observations on some fertile specimens of C. obovata from Guangyuan of Sichuan, but provided no detailed information on sori, annuli and sporangia arrangement.
Comparisons with fossil fertile structures and in situ spores Though diverse specimens of Clathropteris have been widely recorded, the fertile structures with in situ spore features were only documented from a few species (Balme 1995) (Table 1). Comparisons indicate a range of similarity amongst the sporangial features of Clathropteris species (Table 1); however, the in situ spores may also differ in morphology. In the Russian specimen of C. obovata var. magna Turatanova–Ketova, the details of fertile structures are poorly preserved, but the in situ spores are triangular with trilete marks, smooth surface and 35–52 μm in diameter (Vladomirovitch 1950). Krassilov (1969) also described
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Fig. 7 Sketch drawing of morphological features and fertile structures of Clathropteris obovata Oishi from the Upper Triassic in Guangyuan of Sichuan, China. a Part of a pinna with lobbed margin, midvein and rectangular meshes. bar 1 cm; b part of a fertile pinna showing venations and distribution of sori in meshes. bar 1 cm; c a sorus with about 20 sporangia, each about 400 μm in diameter.
bar 0.5 cm; d a sorus showing the sporangia and oblique annuli. bar 142 μm; e, f sporangia with complete and vertical annuli, each about 250 μm in size. bar 100 μm; g, h proximal view of in situ spores showing the trilete marks and sculptures, about 40 μm in diameter. bar 15 μm
spores of this Russian species and gave a slightly wider range of spore size (33–65 μm), but with no illustrations. The apparent difference of the spore type indicates that the Russian material may represent another distinct species of Clathropteris. Several fragmentary specimens of C. obovata recorded from the Yorkshire of England shows normal range of pinna size and venation, but do not display detailed information of sporangia and spores (Harris 1961). Fertile structures of two other Clathropteris species have been described from Europe and North America. Specimens of C. meniscoides from Scoresby of East Greenland have round sori consisting of 10–15 spherical sporangia (Harris 1931). However, Schenk (1867) and Zeiller (1903) described 7–19 and 5–12 sporangia per sorus of this species, respectively. The annulus of C. meniscoides is complete and composed of 30 cells. The spore is “roundish or triangular with thick papillate walls, showing triradiate marks” (Harris 1931). The soral and sporangial features of C. meniscoides are comparable to those of C. obovata from the Upper Triassic in Sichuan, China (Table 1). Unfortunately, there is no record of size/diameter range of sori and sporangia for the European material. Their spores are comparable in shape and ornamentation; however, the size and spore output per sporangium were not recorded for the European species of C. meniscoides (Harris 1931). C. walkeri Daugherty from the Late Triassic of USA represents the best-known species of Clathropteris from America (Ash 1970; Litwin 1985). The soral and sporangial
arrangement of C. walkeri is very similar to that of C. obovata in shape and size ranges. Spores of these two species also share similarities in having trilete spore shape (triangular with rounded apex), sculptures (verrucate, baculate and granulate sculptures), spore size ranges (averages 41 μm) and the spore output (128–256 per sporangium) (Table 1). Despite the spore similarities, the taxonomical status of C. walkeri was disputed. It was noted that spores of C. walkeri are identical to those of C. meniscoides from the northeastern USA (Cornet and Traverse, 1975; Litwin 1985). Therefore, C. walkeri and C. meniscoides were regarded as probably conspecific (Litwin 1985).
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Comparison with living dipterid fern The living Dipteridaceae traditionally include one genus, Dipteris Reinward, which is restricted to the Indo-Malayan region and southern China. Some authors suggest that besides Dipteris, the family should also include a sister taxon Cheiropleuria C. Presl ascribed to the family Cheiropleuriaceae (e.g. Kato et al. 2001; Schuettpelz and Pryer 2007; Smith et al. 2006). In order to compare with living dipterid fern, we examined the herbarium specimen Dipteris conjugata Reinword originally collected from New Caledonia (Fig. 8a–f). Morphologically, the Dipteris frond shows marginal tenth, and the major veins show dichotomous pattern, secondary and tertiary veins form pronounced rectangular meshes (Fig. 8a, b). Sporangia are borne in round to oval, exindusiate
Living Cheiropleuria sp
An extensive soral Oblique area present; 128 spores per sporangium
Tetrahedral and trilete spores
Sori round to oval, Vertical to oblique, Roundish or triancomplete, 30 cells gular with thick closely arranged; trilete marks sporangia oval, up to 250 μm in size; 10–15, or 1–19 or 5–12 sporangia per sorus; Vertical to oblique, Trilete, triangular Clathropteris walk- Sori exindusiate, complete and slightly consori round to oval, eri Daugherty vex to concave about 128–256 emend Ash with rounded spores per sporanapex gium Oblique Monolete, bilateral Sori exindusiate, Living Dipteris and ellipsoid circular to oval, conjungata Reinspores sporangia tightly ward clustered into sori; 64 spores per sporangium
Clathropteris meniscoides Brongniart
With papillate, sometimes form rows
–
Litwin (1985) and Ash (1970) Upper Triassic Chinle Formation, Arizona, New Mexico, USA Indo-Malaya and southern China
39–49 μm
Smooth
Kramer and Green Restricted to the (1990), Tryon and Indo-Malaya and Lugardon (1991), southern China Kato et al. (2001) and Guignard et al. (2009)
Bower (1915), Kramer and Green (1990), Tryon and Lugardon (1991), Kato et al. (2001), Stockey et al. (2006) and Guignard et al. (2009)
Harris (1931), Schenk (1867) and Zeiller (1903) Triassic to Jurassic, East Greenland
–
Vladomirovitch (1950) and Krassilov (1969)
This paper
Upper Triassic, Sichuan, China
Jurassic, Khzakstan, USSR
References
Horizons and locality
–
Converrucosisporites-type, Conbaculatisporites-type
Dispersed spore type
22–65 μm, average With subverrucate, Granulatisporitestype 41 μm subbaculate and bluntly echinate (coni-like) sculptures 22–30 μm (up to Smooth 38 μm)
Smooth
Covered with verrucate and baculate sculptures
Spore surface
35–32 μm or 33–65 μm
Triangular with trilete marks
–
Clathropteris obovata var. magna TuratanovaKetova
22–65 μm (averTrilete, triangular age 41 μm) to subtriangular with rounded apices and concave to convex sides
Vertical to oblique, complete, with 25–30 cells
Sori exindusiate, round to oval, 0.5–1.5 mm in size, 2–5 sori per meshe, each sorus with 10–20 round to oval sporangia; 128–256 spores per sporangium –
Clathropteris obovata Oishi
Spore size
Spore shape
Annulus
Sori and sporangia
Species
Table 1 Comparisons of soral and sporangial structures and in situ spores of related fossil species of Clathropteris and living Dipteridaceae taxa
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Fig. 8 Herbarium specimen of living Dipteris conjugata housed in the Botanical Garden of Lyon, France. (a, b LM photos, c–f SEM photos). a Part of a frond showing vein pattern and marginal teeth. bar 5 mm; b major and dichotomous veins forming vein meshes and the distribution of sporangia. bar 5 mm; c, d sporangia showing annulus and stalks. bar 100 μm; e a sporangium with annuli and a fallen stalk mark. bar 10 μm; f a monolete spore. bar 10 μm
sori, scattered on the abaxial surfaces in between the vein meshes (Fig. 8b). The annulus is vertical to slightly oblique and interrupted by the stalk (Fig. 8c–e). Dipteris species typically have 64 spores and Cheiropleuria species can have up to 128 spores per sporangium (Kramer and Green 1990). Sporangia of present fossil Clathropteris obovata have similar distribution pattern in vein meshes, with similar sporangial annuli of living taxa, but each sporangium produces more spores, i.e., 1–2 times more than the living taxa (Table 1). Morphologically, spores of extant Dipteris are characterized by monolete, elliptisoidal shape with a relatively smooth exine, rangeing from 30 to 40 μm in size (Fig. 8f, g). Spores of living Cheiropleuria are tetrahedral and trilete, ranging from 22 to 30 μm in diameter (Kato et al. 2001;Tryon and Lugardon 1991). In contrast, spores of fossil C. obovata from Sichuan of China show differences from those of both extant Dipteris and Cheiropleuria in having trilete marks and rather complicated spore sculptures, as well as circular to oval spore morphology (Table 1). Such kind of spore morphology variation is also recorded in other fossil dipterid taxa. Spores of Dictyophyllum nilssonii (Brongniart) Goeppert from Jurassic of Hubei, China are characterized by trilete spores with smooth spore surface (Guignard et al. 2009). However, spores of Hausmannia sinensis Wang and Zhang from the Jurassic of Inner Mongolia, China, are characterized by baculate sculptures (Wang and Zhang 2010), which show similarities to fossil C. obovata rather than to living taxa. Obviously, unlike the living taxa which have a rather simple spore morphology, the Mesozoic fossil spores of the family Dipteridaceae show quite complicated morphology.
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Comparison with fossil dispersed spores In situ spores of C. obovata from the Upper Triassic of Sichuan, China are closely comparable with two dispersed genera, Converrucosisporites and Conbaculatisporites. They resemble Converrucoisporites cameronii (De Jersey) Playford and Dettmann (1965), a Rhaeto-Liassic species first described from Australia. The sculpture of C. cameronii, as emended by Cornet and Traverse (1975), is mostly verrucate, bacula, coni and clave, and the diameter ranges from 33 to 51 μm (average 42 μm). Such dispersed spores were also recorded from the Late Triassic palynological assemblages in Sichuan, China (Lei 1986). Another dispersed species, Conbaculatisporites mesozoicus Klaus (1960) from the Carnian Alpine Triassic of Europe, also agrees with fossil C. obovata spores in size range (39– 48 μm) and sculptural features, although the dispersed spore has longer radii. Additionally, the dispersed genus Granulatisporites infirmus (Balme) Cornet and Traverse (1975) bears similarities to some in situ spores of fossil C. obovata from the Triassic of Sichuan, China. However, the spore sculpture of G. infirmus is dominated mainly grana and small verrucate, mixed with a few baculi and coni. In addition, another dispersed genus Clathropterisospora was proposed for resembling in situ spores of Clathropteris meniscoides (Zhang 1980, 1984). It is similar to in situ spores of fossil Clathropteris obovata in shape, but differ in having smaller size and denticulate to setaceous sculptures. Morphologically, Clathropterisospora can be compared with other dispersed spore genera, such as Lophotriletes, Acanthotriletes and Apiculatisporites.
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Evolutionary considerations The fertile structures and in situ spores are crucial for determining the evolution and phylogeny of both living and fossil ferns. The living Dipteris and Cheiropleuria have features that are suggestive of highly derived families of the filicales (Rothwell 1987). Clathropteris is one of the typical fossil dipterid ferns in the Mesozoic, however, previous knowledge about fertile organs of Clathropteris is insufficient due to poor preservation of fossil specimens. The exceptionally preserved specimens of C. obovata from China display detailed information on fertile structures, and offers further tie for linking the evolution of this fern family. The superficial type of sorus position in C. obovata demonstrates a more derived nature than the marginal type of sorus in primitive fern groups, i.e. Marattiaceae (Bower 1912, 1923). The exindusiate sorus with well-developed, complete and vertical to oblique annulus in sporangia C. obovata, indicating an intermediate evolution of this plant. The spore output in C. obovata ranges 128–230 per sporangium, which falls into the range of 128–256 spores per sporangium as like the living dipteris. This suggests a more derived nature than those primitive eusporangiate ferns yielding more spore numbers (e.g. thousands of spores in fossil Marattia) (Wang 1999). The spore output number of this fossil shows primitive nature as compared with advanced ferns with around 64 spores per sporangium (e.g. Dicksoniaceae) (Bower 1912, 1923). As shown in Table 1, spores of living dipterid taxa are unique in morphology with smooth surfaces. In contrast, fossil dipterid in situ spores demonstrate a variety of spore morphology with a diverse range of sculpture. Besides Clathropteris, other fossil Dipteridaceae taxa, such as Dictyophyllum and Hausmannia in the Mesozoic, also show a distinct and high morphologic diversity of fossil in situ spores (e.g. Guignard et al. 2009; Stockey et al. 2006; Wang and Zhang 2010). It is noted that two other leptosporangiate families, Matoniaceae and Gleicheniaceae, are generally regarded as closely related to the Dipteridaceae. The evolutionary relationship between these families and other leptosporangiate ferns is not well- understood based on leaf morphology and fertile structures (Pryer et al. 2004; Schuettpelz and Pryer 2007; Smith et al. 2006). However, fossil in situ spore evidence could offer clues for understanding the evolutionary implication for dipterid fern with other related fern groups. Most importantly, it is evident that the fossil spore wall ultrastructure can provide useful evidence for this evolution links (e.g. Grauvogel-Stamm and Lugardon, 2009; Guignard et al. 2009; Wang et al. 1999, 2001). In both fossil and living ferns, spore ultrastructure gradually became simplified from primitive groups to
derived groups. For instance, spore ultrastructure of fossil Marattia is simpler than that of Ophioglossaceae (Wang et al. 2001), but it is more complicated than that of fossil Gleicheniaceae (e.g. Oligocarpia, Wang et al. 1999). In some relevant extant and fossil ferns, such as Dipteridaceae, Gleicheniaceae and Matoniaceae, the general spore morphology is more or less similar. However, in situ spore wall ultrastructures may show certain distinct differences, which implies evolutionary and phylogenetic significances (Van Konijnenburg-van Cittert and Kurmann 1994; Tryon and Lugardon 1991). Further investigations on fossil in situ spores with emphasize on spore wall ultrastructure are thus needed, so as to acquire more evolutionary information for dipterid fern. Acknowledgments We thank Y. Q. Mao (NIGPAS, Nanjing), Frédéric Pautz (Director, Botanical Garden of Lyon), Frédéric Danet (Curator of Lyon Herbarium) (LYJB) and Katherine Dilcher for helpful assistances. We also acknowledge Dr. Mike Pole for helpful suggestion and constructive comments of the manuscript. This study was jointly supported by the State Key Basic Research Program of China (2012CB822003), National Natural Sciences Foundation of China (NSFC 41272010, 40972008 and 40472004), the Knowledge Innovation Project of CAS (KZCX-2-YW-154), and the Team Program from the Chinese Academy of Sciences.
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REGULAR PAPER
Fertile structures with in situ spores of a dipterid fern from the Triassic in southern China Yongdong Wang · Liqin Li · Gaëtan Guignard · David L. Dilcher · Xiaoping Xie · Ning Tian · Ning Zhou · Yan Wang
Received: 21 September 2014 / Accepted: 25 December 2014 © The Botanical Society of Japan and Springer Japan 2015
Abstract Clathropteris was a typical dipterid fern with well documented fossil record and was widely dispersed during the Mesozoic; however, our knowledge of fertile structures including in situ spores for this genus is still very limited. Here we report well-preserved compression specimens of Clathropteris obovata Oishi from the Late Triassic of Guangyuan, Sichuan Province, China. The specimens show round to oval and exindusiate sori, vertical to oblique annuli in sporangia, and in situ trilete spores with verrucate and baculate sculptures, which are comparable to dispersed spore genera of Converrucosisporites and Conbaculatisporites. Comparisons of relevant fossil taxa suggest that specimens of C. obovata from Triassic of China provide for the first time in Asia the detailed fertile structures with in situ spore characters of dipterid fossil Clathropteris. Unlike living Dipteris, Mesozoic fossils of Dipteridaceae show a high diversity and a range of complex morphology of in situ spores, thus are significant for the evolutionary links between Dipteridaceae and other related
fern clade, including Gleicheniaceae and Matoniaceae of the Gleicheniales.
Y. Wang · L. Li · N. Zhou Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China
D. L. Dilcher Department of Geology, Indiana University, 1001 E. Tenth St., Bloomington, IN 47405, USA
Y. Wang (*) Key Laboratory of Economic Stratigraphy and Palaeogeography, Chinese Academy of Sciences, Nanjing 210008, China e-mail: [email protected]
D. L. Dilcher · N. Tian College of Palaeontology, Shenyang Normal University, Shenyang 110034, China
L. Li · N. Zhou University of Chinese Academy of Sciences, Beijing 100049, China G. Guignard UMR CNRS 5276 Laboratoire de Géologie de Lyon, Département de Biologie, Université Claude Bernard Lyon 1, Herbiers de l’Université Claude Bernard Lyon 1, Villeurbanne Cedex 69622, France
Keywords Dipteridaceae · Clathropteris · Sporangia · In situ spores · Late Triassic · Sichuan · China
Introduction The Late Triassic floras of the Sichuan Basin in southern China have been well known since the 1880s. In particular, fossil plants from the coal-bearing deposits in the Upper Triassic Xujiahe (=Hsuchiaho) Formation from Guangyuan (=Kwangyuan) City of northern Sichuan Province are exceptionally preserved. Plant fossils from this location were first described by Schenk (1883) based on fragmentary specimens, representing the beginning of paleobotanical studies of Triassic plants in China. Subsequently, a series of investigations were reported on systematics
X. Xie College of Geography and Tourism, Qufu Normal University, Rizhao 276826, China Y. Wang School of Geoscience and Technology, Southwest Petroleum University, Chengdu 610500, China
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Fig. 1 Sketch map showing the fossil locality in Xujiahe town of Guangyuan, Sichuan Province, China
and paleoecology of plant fossils from the Xujiahe Formation in the northern Sichuan Basin (e.g. Huang 1992, 1995; Lee 1964; Sze 1933; Sze and Lee 1952; Wu 1999; Yang 1978; Ye et al. 1986). In the Xujiahe flora, Bennettitales are the dominant group with particularly rich taxa (e.g. Pterophyllum, Ptilophyllum, Otozamites). Ferns are the second most diverse group; sphenopsids (e.g. Neocalamites and Equisetites), pteridosperms (Ptilozamites, Lepidopteris), conifers (e.g. Podozamites and Ferganiella) and ginkgos (Baiera, Glossophyllum and Czekanowskia) are common elements (Lee 1964; Wang et al. 2010a; Wu 1999). Ferns are represented in this flora by a variety of taxa, including over 20 species ascribed to 11 genera of 4 families, i.e. Dipteridaceae, Matoniaceae, Osmundaceae and Marattiaceae (Wu 1999). Among them, the Dipteridaceae are particularly remarkable, including 10 species of four genera: Dictyophyllum, Clathropteris, Hausmannia and Thaumatopteris. Although a variety of fossil compression and impression specimens of dipterid foliages have been described from this area (e.g. Lee 1964; Sze 1933; Sze and Lee 1952; Wu 1999), the fertile structures and in situ spores of this fern group are still poorly known. Some fragmentary fertile specimens of Clathropteris have been previously noted from the Late Triassic in Guangyuan, Hechuan and neighboring regions of the Sichuan Basin (Lee 1964; Wu 1999; Ye et al. 1986), however, the detailed structures of their sporangia and in situ spores have not been well-investigated. In this paper, we describe the exceptionally preserved fertile fronds of a dipterid fern, Clathropteris obovata Oishi from the Late Triassic in Guangyuan of Sichuan Province
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based on detailed examination using both light and scanning electron microscopic observations. We offer new data on sporangia, annuli and in situ spores of this Clathropteris species, and compare with fossil and living taxa as well as with dispersed spore types. This represents the first detailed description for fertile structures of fossil Clathropteris from Asia, and thus showing crucial insights for exploring the diversity and evolution of the dipteridaceous fern clade.
Materials and methods The fossil specimens of Clathropteris obovata Oishi (Dipteridaceae) were collected from the Xujiahe town, about 5 km north of Guangyuan City, Sichuan Province (Lee 1964) (Fig. 1). Geologically, Xujiahe town is known as the type locality for the stratigraphic sequences of the Upper Triassic Xujiahe Formation which contains diverse and well-preserved fossil plants. The Xujiahe Formation is underlain by the limestone of Middle Triassic age and is covered by the Lower Jurassic strata. This formation consists mainly of yellow and grey sandstones, shale, and sandy shale, intercalated with carbonaceous shales and coal seams, that yield abundant fossil plants. Four lithological Members (i.e. Members 1–4) are recognized representing a deltaic estuary sandbar and delta plain swamp sedimentary environment (Wang et al. 2010a, b). The age of this flora is designated as Norian to Rhaetian based on associated invertebrate fauna (such as bivalves, ostracods, conchostracas) and palynological assemblages (Chen et al. 1979; Liu 1982; Wu 1999; Wang et al. 2010a, b).
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Diverse fossil plant remains were mainly documented from Members 1 and 3 of this formation (Fig. 2) (Huang 1992, 1995; Wang et al. 2010a). Three well-preserved compression specimens of Clathropteris obovata, including both sterile and fertile leaves, were collected from a bed of black and greyish-black shale and coal seams in the Member 3 of the Xujiahe Formation (Fig. 2). The structure and organization of fertile organs were found in an extremely fine condition of preservation. The soral material was removed mechanically from the fertile pinnule and first treated with hydrochloric acid (HCl) and then hydrofluoric acid (HF), followed by a maceration in Schultz solution. After washing with water, they
were then treated with a 5 % ammonia solution for several min followed by several changes in distilled water. Sporangia and spore material was used for slide preparation and observed under a light microscope (LM). For scanning electron microscope (SEM), material was placed on sample stubs with double-sided sticky tape. They were then sputter-coated with gold and viewed on a JSM 6300 scanning electron microscope at an acceleration voltage of 15–20 kV. All specimens (with registration numbers PB2808-1, PB 2808-4 and PB2808-5), slides and SEM stubs are housed in the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China. In addition, an extant Dipteris specimen from the herbarium collection at the Botanical Garden of Lyon, France was used for comparision. The specimen Dipteris conjugata Reinword was collected from Mont Koghi at 400 m altitude in New Caledonia in 1911 with the registration number LYJB000854. The living sporangia material was observed under SEM for comparison of fossil dipterids with respect to their fertile structures and in situ spores.
Results Systematic descriptions Order—Filicales Family—Dipteridaceae Diels Genus—Clathropteris Brongniart Species—Clathropteris obovata Oishi Figs. 3, 4, 5, 6, 7
Fig. 2 The stratigraphical column and fossil plant horizon of the Upper Triassic Xujiahe Formation in Guangyuan, Sichuan. 1 Limestone, 2 conglomerate, 3 sandstone, 4 siltstone, 5 mudstone, 6 coal, 7 plant fossil bed
Selected references. 1932 Clathropteris obovata, Oishi, p. 291, pl. 30, Fig. 2; pl. 32, Fig. 1 1949 Clathropteris meniscoides, Sze, p. 6, pl. 1, Fig. 5 (=Sze et al. 1963, pl. 27, Fig. 4) 1961 Clathropteris obovata, Harris, p. 123, Fig. 42 1964 Clathropteris meniscoides, Lee, p. 108, pl. 2, Figs. 2a, 3, 4; pl. 3, Figs. 1, 2, 3, 4, 5, 6; text-Fig. 3 1976 Clathropteris obovata, Li, Cao and Wu, p. 109, pl. 1l9, Fig. 5 1980 Clathropteris obovata, Wu, Ye and Li, p. 94, pl. 11, Figs. 1, 2; pl. 12, Figs. 5, 6 Age and horizon. Late Triassic (Norian- Rhaetian), the Xujiahe Formation. Locality. Xujiahe Town, Guangyuan City, Sichuan Province. Material studied. Three specimens with registration numbers PB2808-1, PB2808-4 and PB2808-5 in paleobotanical collection, NIGPAS.
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Fig. 3 Clathropteris obovata Oishi from the Upper Triassic in Guangyuan, Sichuan, China (a– e LM photos). a A fertile pinna, the round to oval impression left behind is the receptacle of sori/sporangia. PB 2808-4. bar 1 cm; b a fertile pinna showing rectangular meshes of venation and the distribution of sori. In this slab, two layers of pinnae are preserved; the second layer of pinna is marked by black and white arrows. bar 1 cm; c detail of b, showing the distribution of sori and sori impression in meshes. PB2808-5, bar 0.5 cm; d three sterile pinnae showing distinct midveins and rectangular meshes. Pinna A and pinna B are overlapped; pinna C is covered by pinnae A and B. PB2808-1. The marginal lobes are marked in left part of pinna a with white dot line, which are indistinct due to the preservation status. bar 1 cm; e higher magnification of two sori in a mesh. bar 0.67 mm
Megafossil. The specimens of Clathropteris obovata Oishi from Guangyuan of Sichuan are represented by several sterile and fertile leaves preserved as compressions (Fig. 3a, b, d). The specimen shows fragments of the sterile pinnae preserved together in a slab (Fig. 3d). They represent the middle to upper part of a sterile leaf and are usually overlapping in preservation, but show distinct midveins and venation patterns. Two fertile specimens show the upper part of fronds with impression/compression of sori in the venation (Fig. 3a, b). The leaf is moderate in size, and the pinna is obovate in outline, more than 12 cm long and 5 cm wide for sterile pinnae (Fig. 3d) and over 5.5 cm long
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and 5.5–8 cm wide for fertile pinnae (Fig. 3a, b). A closer examination of the specimens shows a more or less lobbed pinna margin (Fig. 3a, d). In some cases, the marginal lobe is indistinct due to incomplete preservation of the specimens. The midvein (midrib) is slender, straight or slightly undulated. Secondary veins arise from the midvein at intervals of 8–14 mm, making an angle of about 40°–50° (rarely over 60°) to the base with midvein. Tertiary veins arise at almost right angle to the secondary ones, forming a more or less rectangular mesh of the Clathropteris-type. These meshes vary from 4–7 mm wide and 8–10 mm long for fertile pinna, 4–8 mm wide and 8–12 mm long for sterile
J Plant Res Fig. 4 Clathropteris obovata Oishi from the Upper Triassic in Guangyuan, Sichuan, China showing details of sori and sporangia (a–d LM photos, e–h SEM photos). a Detail of Fig. 3b showing the impression of circular sori in vein meshes. The secondary veins (S), tertiary veins (T) and blind veins (B) are present. bar 1.25 mm; b-d the circular to oval and exindusiate sori consisting of 10–20 sporangia. bar 0.67 mm (b, d); bar 1.25 mm (c); e two more or less rounded and connected sori consisting of several sporangia. bar 270 μm; f detail of e, showing three sporangia with well-developed annuli. bar 71.4 μm; g detail of e, showing three sporangia and annuli. bar 75 μm; h partly preserved sori showing sporangia and annuli. bar 93.5 μm
pinna. The finest veins tend to form rectangular meshes enclosing blind vein-endings (Figs. 3b, d, 4a, 7a, b). Sori and sporangia. Sori are well-preserved and are distributed in rectangular meshes along the midvein, about 2–5 sori per mesh (Fig. 4a). Sori are exindusiate and sporangia are shed after dehiscence to leaving a visible round to oval receptacle (Figs. 3a, c, 4a). Sori are round to oval in outline, range from 0.5–1.5 mm in size. Each sorus consists of 10–20 sporangia (Figs. 3e, 4b–d, 7c, d). Sporangia are round to oval in lateral view (viewed perpendicular to the plane of the annulus) (Fig. 7d–f), ranging from 140 to 300 μm in diameter (average 250 μm). The annulus of the sporangia is vertical to oblique, complete, and composed of
a uniserate ring of 25–30 cells, almost linear in orientation (Figs. 4e–h, 7d–f). Radial wall height of the annular cells ranges from 70 to 80 μm and thickness from 5 to 10 μm. Details of the sporangial stalks and their insertion were not visible in this material. Each sporangium contains spore masses (Fig. 5a–d) and produces about 128–230 spores based on a count of 5 sporangia. In situ spores. Spores are trilete, triangular to subtriangular in equatorial view, with round apices and concave to convex sides (Figs. 5e, 6a–j, 7g, h). Radii of laesurae are raised, straight or slightly sinuous, extending to about 0.6– 1.0 of the spore radius. Both proximal and distal surfaces of spores are covered with verrucate, baculate or granular
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Fig. 5 Clathropteris obovata Oishi from the Upper Triassic in Guangyuan, Sichuan, China showing in situ spores in macerated sporangia (SEM photos). a, b Two sporangia containing large number of spores. bar 40 μm (a); bar 38.5 μm (b); c detail of a spore mass. bar 9 μm; d a rounded triangular spore within a spore mass, showing verrucate and baculate sculptures. bar 5.3 μm; e a triangular spore showing surface sculptures. bar 7.4 μm; f detail of e, showing verrucate and baculate sculpture elements. bar 2.2 μm
sculptures up to 1.5 μm high and 1 μm wide (Figs. 5d–f, 6a–d, 7g, h). Sculptural elements cover the sporoderm and are commonly fused, forming an irregular sinuous cover (Figs. 5e, f, 6a–j, 7g, h). Exine is thin, approximately 0.5 μm thick, excluding sculpture. No perispore is observed. Weakly to strongly developed interradial folds are generally present. Spore size ranges from 22 to 65 μm in equatorial diameter (mean 41 μm).
Discussion The Dipteridaceae have a well-established fossil record extending from the Triassic to the Cretaceous in Eurasia, North America and Gondwana (Cantrill 1995; Escapa et al. 2011; Tidwell and Ash 1994). Fossil taxa of the Mesozoic Dipteridaceae are often regarded as indicators for humid, warm-temperate to subtropical climatic conditions (e.g. Bomfleur and Kerp 2010; Van Konijnenburg-van Cittert 2002; Wang et al. 2009). Clathropteris is one of the
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representative fossil genera of the Dipteridaceae in the Mesozoic. It is widely recorded in Late Triassic and Early Jurassic floras of Eurasia, North America, as well as Argentina and Antarctica (Bomfleur and Kerp 2010; Frenguelli 1941; Herbst 1966). It is a key taxon of the Dictyophyllum–Clathropteris assemblage of the Late Triassic to Early Jurassic in both northern and southern China phytoprovinces (Hsü et al. 1979; Li et al. 1976; Sze 1949; Sun 1981; Sze et al. 1963; Sze and Chow 1964; Wang 2002; Wang et al. 2009; Wu et al. 1980; Zhang and Zheng 1987; Zhou 1984, 1995). Clathropteris was proposed by Brongniart (1828) for specimens with reticulate veins from the Rhaetic beds in Scania. The genus is characterized by large, palmately compound fronds and a unique, orthogonal venation pattern of secondary and tertiary veins (Tidwell and Ash 1994). The original specimens from the Upper Triassic Xujiahe Formation in Guangyuan of Sichuan were first described as Clathropteris meniscoides by Lee (1964) when she studied plant fossils from this locality. Later, these specimens were assigned to Clathropteris obovata Oishi (Li et al.
J Plant Res Fig. 6 Clathropteris obovata Oishi from the Upper Triassic in Guangyuan, Sichuan, China showing in situ spores (a–d SEM photos, e–j LM photos). a, b Distal view of spores. bar 7 μm (a); bar 7 μm (b); c, d proximal view of spores showing trilete marks. bar 7.7 μm; e–j light microphotos of in situ spores. bar 12.5 μm
1976), a Rhaetic plant proposed by Oishi (1932) from the Nariwa Flora in Japan. Fossil specimens from Guangyuan of Sichuan, China are morphologically similar to the type specimens of C. obovata from Japan in having obovateshaped pinnae and similar venation type. However, Oishi’s diagnosis was proposed based on sterile pinnae, yielding no information of the fertile structures. Harris (1961) gave an emended diagnosis of C. obovata based on Yorkshire materials, but added no detailed data on soral structures. Lee (1964) and Li et al. (1976) did preliminary observations on some fertile specimens of C. obovata from Guangyuan of Sichuan, but provided no detailed information on sori, annuli and sporangia arrangement.
Comparisons with fossil fertile structures and in situ spores Though diverse specimens of Clathropteris have been widely recorded, the fertile structures with in situ spore features were only documented from a few species (Balme 1995) (Table 1). Comparisons indicate a range of similarity amongst the sporangial features of Clathropteris species (Table 1); however, the in situ spores may also differ in morphology. In the Russian specimen of C. obovata var. magna Turatanova–Ketova, the details of fertile structures are poorly preserved, but the in situ spores are triangular with trilete marks, smooth surface and 35–52 μm in diameter (Vladomirovitch 1950). Krassilov (1969) also described
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Fig. 7 Sketch drawing of morphological features and fertile structures of Clathropteris obovata Oishi from the Upper Triassic in Guangyuan of Sichuan, China. a Part of a pinna with lobbed margin, midvein and rectangular meshes. bar 1 cm; b part of a fertile pinna showing venations and distribution of sori in meshes. bar 1 cm; c a sorus with about 20 sporangia, each about 400 μm in diameter.
bar 0.5 cm; d a sorus showing the sporangia and oblique annuli. bar 142 μm; e, f sporangia with complete and vertical annuli, each about 250 μm in size. bar 100 μm; g, h proximal view of in situ spores showing the trilete marks and sculptures, about 40 μm in diameter. bar 15 μm
spores of this Russian species and gave a slightly wider range of spore size (33–65 μm), but with no illustrations. The apparent difference of the spore type indicates that the Russian material may represent another distinct species of Clathropteris. Several fragmentary specimens of C. obovata recorded from the Yorkshire of England shows normal range of pinna size and venation, but do not display detailed information of sporangia and spores (Harris 1961). Fertile structures of two other Clathropteris species have been described from Europe and North America. Specimens of C. meniscoides from Scoresby of East Greenland have round sori consisting of 10–15 spherical sporangia (Harris 1931). However, Schenk (1867) and Zeiller (1903) described 7–19 and 5–12 sporangia per sorus of this species, respectively. The annulus of C. meniscoides is complete and composed of 30 cells. The spore is “roundish or triangular with thick papillate walls, showing triradiate marks” (Harris 1931). The soral and sporangial features of C. meniscoides are comparable to those of C. obovata from the Upper Triassic in Sichuan, China (Table 1). Unfortunately, there is no record of size/diameter range of sori and sporangia for the European material. Their spores are comparable in shape and ornamentation; however, the size and spore output per sporangium were not recorded for the European species of C. meniscoides (Harris 1931). C. walkeri Daugherty from the Late Triassic of USA represents the best-known species of Clathropteris from America (Ash 1970; Litwin 1985). The soral and sporangial
arrangement of C. walkeri is very similar to that of C. obovata in shape and size ranges. Spores of these two species also share similarities in having trilete spore shape (triangular with rounded apex), sculptures (verrucate, baculate and granulate sculptures), spore size ranges (averages 41 μm) and the spore output (128–256 per sporangium) (Table 1). Despite the spore similarities, the taxonomical status of C. walkeri was disputed. It was noted that spores of C. walkeri are identical to those of C. meniscoides from the northeastern USA (Cornet and Traverse, 1975; Litwin 1985). Therefore, C. walkeri and C. meniscoides were regarded as probably conspecific (Litwin 1985).
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Comparison with living dipterid fern The living Dipteridaceae traditionally include one genus, Dipteris Reinward, which is restricted to the Indo-Malayan region and southern China. Some authors suggest that besides Dipteris, the family should also include a sister taxon Cheiropleuria C. Presl ascribed to the family Cheiropleuriaceae (e.g. Kato et al. 2001; Schuettpelz and Pryer 2007; Smith et al. 2006). In order to compare with living dipterid fern, we examined the herbarium specimen Dipteris conjugata Reinword originally collected from New Caledonia (Fig. 8a–f). Morphologically, the Dipteris frond shows marginal tenth, and the major veins show dichotomous pattern, secondary and tertiary veins form pronounced rectangular meshes (Fig. 8a, b). Sporangia are borne in round to oval, exindusiate
Living Cheiropleuria sp
An extensive soral Oblique area present; 128 spores per sporangium
Tetrahedral and trilete spores
Sori round to oval, Vertical to oblique, Roundish or triancomplete, 30 cells gular with thick closely arranged; trilete marks sporangia oval, up to 250 μm in size; 10–15, or 1–19 or 5–12 sporangia per sorus; Vertical to oblique, Trilete, triangular Clathropteris walk- Sori exindusiate, complete and slightly consori round to oval, eri Daugherty vex to concave about 128–256 emend Ash with rounded spores per sporanapex gium Oblique Monolete, bilateral Sori exindusiate, Living Dipteris and ellipsoid circular to oval, conjungata Reinspores sporangia tightly ward clustered into sori; 64 spores per sporangium
Clathropteris meniscoides Brongniart
With papillate, sometimes form rows
–
Litwin (1985) and Ash (1970) Upper Triassic Chinle Formation, Arizona, New Mexico, USA Indo-Malaya and southern China
39–49 μm
Smooth
Kramer and Green Restricted to the (1990), Tryon and Indo-Malaya and Lugardon (1991), southern China Kato et al. (2001) and Guignard et al. (2009)
Bower (1915), Kramer and Green (1990), Tryon and Lugardon (1991), Kato et al. (2001), Stockey et al. (2006) and Guignard et al. (2009)
Harris (1931), Schenk (1867) and Zeiller (1903) Triassic to Jurassic, East Greenland
–
Vladomirovitch (1950) and Krassilov (1969)
This paper
Upper Triassic, Sichuan, China
Jurassic, Khzakstan, USSR
References
Horizons and locality
–
Converrucosisporites-type, Conbaculatisporites-type
Dispersed spore type
22–65 μm, average With subverrucate, Granulatisporitestype 41 μm subbaculate and bluntly echinate (coni-like) sculptures 22–30 μm (up to Smooth 38 μm)
Smooth
Covered with verrucate and baculate sculptures
Spore surface
35–32 μm or 33–65 μm
Triangular with trilete marks
–
Clathropteris obovata var. magna TuratanovaKetova
22–65 μm (averTrilete, triangular age 41 μm) to subtriangular with rounded apices and concave to convex sides
Vertical to oblique, complete, with 25–30 cells
Sori exindusiate, round to oval, 0.5–1.5 mm in size, 2–5 sori per meshe, each sorus with 10–20 round to oval sporangia; 128–256 spores per sporangium –
Clathropteris obovata Oishi
Spore size
Spore shape
Annulus
Sori and sporangia
Species
Table 1 Comparisons of soral and sporangial structures and in situ spores of related fossil species of Clathropteris and living Dipteridaceae taxa
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Fig. 8 Herbarium specimen of living Dipteris conjugata housed in the Botanical Garden of Lyon, France. (a, b LM photos, c–f SEM photos). a Part of a frond showing vein pattern and marginal teeth. bar 5 mm; b major and dichotomous veins forming vein meshes and the distribution of sporangia. bar 5 mm; c, d sporangia showing annulus and stalks. bar 100 μm; e a sporangium with annuli and a fallen stalk mark. bar 10 μm; f a monolete spore. bar 10 μm
sori, scattered on the abaxial surfaces in between the vein meshes (Fig. 8b). The annulus is vertical to slightly oblique and interrupted by the stalk (Fig. 8c–e). Dipteris species typically have 64 spores and Cheiropleuria species can have up to 128 spores per sporangium (Kramer and Green 1990). Sporangia of present fossil Clathropteris obovata have similar distribution pattern in vein meshes, with similar sporangial annuli of living taxa, but each sporangium produces more spores, i.e., 1–2 times more than the living taxa (Table 1). Morphologically, spores of extant Dipteris are characterized by monolete, elliptisoidal shape with a relatively smooth exine, rangeing from 30 to 40 μm in size (Fig. 8f, g). Spores of living Cheiropleuria are tetrahedral and trilete, ranging from 22 to 30 μm in diameter (Kato et al. 2001;Tryon and Lugardon 1991). In contrast, spores of fossil C. obovata from Sichuan of China show differences from those of both extant Dipteris and Cheiropleuria in having trilete marks and rather complicated spore sculptures, as well as circular to oval spore morphology (Table 1). Such kind of spore morphology variation is also recorded in other fossil dipterid taxa. Spores of Dictyophyllum nilssonii (Brongniart) Goeppert from Jurassic of Hubei, China are characterized by trilete spores with smooth spore surface (Guignard et al. 2009). However, spores of Hausmannia sinensis Wang and Zhang from the Jurassic of Inner Mongolia, China, are characterized by baculate sculptures (Wang and Zhang 2010), which show similarities to fossil C. obovata rather than to living taxa. Obviously, unlike the living taxa which have a rather simple spore morphology, the Mesozoic fossil spores of the family Dipteridaceae show quite complicated morphology.
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Comparison with fossil dispersed spores In situ spores of C. obovata from the Upper Triassic of Sichuan, China are closely comparable with two dispersed genera, Converrucosisporites and Conbaculatisporites. They resemble Converrucoisporites cameronii (De Jersey) Playford and Dettmann (1965), a Rhaeto-Liassic species first described from Australia. The sculpture of C. cameronii, as emended by Cornet and Traverse (1975), is mostly verrucate, bacula, coni and clave, and the diameter ranges from 33 to 51 μm (average 42 μm). Such dispersed spores were also recorded from the Late Triassic palynological assemblages in Sichuan, China (Lei 1986). Another dispersed species, Conbaculatisporites mesozoicus Klaus (1960) from the Carnian Alpine Triassic of Europe, also agrees with fossil C. obovata spores in size range (39– 48 μm) and sculptural features, although the dispersed spore has longer radii. Additionally, the dispersed genus Granulatisporites infirmus (Balme) Cornet and Traverse (1975) bears similarities to some in situ spores of fossil C. obovata from the Triassic of Sichuan, China. However, the spore sculpture of G. infirmus is dominated mainly grana and small verrucate, mixed with a few baculi and coni. In addition, another dispersed genus Clathropterisospora was proposed for resembling in situ spores of Clathropteris meniscoides (Zhang 1980, 1984). It is similar to in situ spores of fossil Clathropteris obovata in shape, but differ in having smaller size and denticulate to setaceous sculptures. Morphologically, Clathropterisospora can be compared with other dispersed spore genera, such as Lophotriletes, Acanthotriletes and Apiculatisporites.
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Evolutionary considerations The fertile structures and in situ spores are crucial for determining the evolution and phylogeny of both living and fossil ferns. The living Dipteris and Cheiropleuria have features that are suggestive of highly derived families of the filicales (Rothwell 1987). Clathropteris is one of the typical fossil dipterid ferns in the Mesozoic, however, previous knowledge about fertile organs of Clathropteris is insufficient due to poor preservation of fossil specimens. The exceptionally preserved specimens of C. obovata from China display detailed information on fertile structures, and offers further tie for linking the evolution of this fern family. The superficial type of sorus position in C. obovata demonstrates a more derived nature than the marginal type of sorus in primitive fern groups, i.e. Marattiaceae (Bower 1912, 1923). The exindusiate sorus with well-developed, complete and vertical to oblique annulus in sporangia C. obovata, indicating an intermediate evolution of this plant. The spore output in C. obovata ranges 128–230 per sporangium, which falls into the range of 128–256 spores per sporangium as like the living dipteris. This suggests a more derived nature than those primitive eusporangiate ferns yielding more spore numbers (e.g. thousands of spores in fossil Marattia) (Wang 1999). The spore output number of this fossil shows primitive nature as compared with advanced ferns with around 64 spores per sporangium (e.g. Dicksoniaceae) (Bower 1912, 1923). As shown in Table 1, spores of living dipterid taxa are unique in morphology with smooth surfaces. In contrast, fossil dipterid in situ spores demonstrate a variety of spore morphology with a diverse range of sculpture. Besides Clathropteris, other fossil Dipteridaceae taxa, such as Dictyophyllum and Hausmannia in the Mesozoic, also show a distinct and high morphologic diversity of fossil in situ spores (e.g. Guignard et al. 2009; Stockey et al. 2006; Wang and Zhang 2010). It is noted that two other leptosporangiate families, Matoniaceae and Gleicheniaceae, are generally regarded as closely related to the Dipteridaceae. The evolutionary relationship between these families and other leptosporangiate ferns is not well- understood based on leaf morphology and fertile structures (Pryer et al. 2004; Schuettpelz and Pryer 2007; Smith et al. 2006). However, fossil in situ spore evidence could offer clues for understanding the evolutionary implication for dipterid fern with other related fern groups. Most importantly, it is evident that the fossil spore wall ultrastructure can provide useful evidence for this evolution links (e.g. Grauvogel-Stamm and Lugardon, 2009; Guignard et al. 2009; Wang et al. 1999, 2001). In both fossil and living ferns, spore ultrastructure gradually became simplified from primitive groups to
derived groups. For instance, spore ultrastructure of fossil Marattia is simpler than that of Ophioglossaceae (Wang et al. 2001), but it is more complicated than that of fossil Gleicheniaceae (e.g. Oligocarpia, Wang et al. 1999). In some relevant extant and fossil ferns, such as Dipteridaceae, Gleicheniaceae and Matoniaceae, the general spore morphology is more or less similar. However, in situ spore wall ultrastructures may show certain distinct differences, which implies evolutionary and phylogenetic significances (Van Konijnenburg-van Cittert and Kurmann 1994; Tryon and Lugardon 1991). Further investigations on fossil in situ spores with emphasize on spore wall ultrastructure are thus needed, so as to acquire more evolutionary information for dipterid fern. Acknowledgments We thank Y. Q. Mao (NIGPAS, Nanjing), Frédéric Pautz (Director, Botanical Garden of Lyon), Frédéric Danet (Curator of Lyon Herbarium) (LYJB) and Katherine Dilcher for helpful assistances. We also acknowledge Dr. Mike Pole for helpful suggestion and constructive comments of the manuscript. This study was jointly supported by the State Key Basic Research Program of China (2012CB822003), National Natural Sciences Foundation of China (NSFC 41272010, 40972008 and 40472004), the Knowledge Innovation Project of CAS (KZCX-2-YW-154), and the Team Program from the Chinese Academy of Sciences.
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