A dipteridaceous fern with in situ spores from the Lower Jurassic in Hubei, China

Review of Palaeobotany and Palynology 156 (2009) 104–115

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A dipteridaceous fern with in situ spores from the Lower Jurassic in Hubei, China

Gaëtan Guignard a,⁎, Yongdong Wang b, Qing Ni b, Ning Tian b, Zikun Jiang b

a Université de Lyon, F-69622, Lyon, France; Université de Lyon 1, Villeurbanne; CNRS, UMR5125, Paléoenvironments et Paléobiosphère, Franceb Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, PR China

⁎ Corresponding author.E-mail addresses: [email protected] (G. Guigna

(Y. Wang).

0034-6667/$ – see front matter © 2008 Elsevier B.V. Adoi:10.1016/j.revpalbo.2008.09.004

a b s t r a c t
a r t i c l e i n f o
Article history:
Dictyophyllum, a genus of the Received 25 January 2008Received in revised form 4 September 2008Accepted 22 September 2008Available online 11 October 2008
Keywords:DipteridaceaeDictyophyllumin situ sporesLower JurassicHubeiChina

fern familyDipteridaceae,waswidespreadduring the Triassic and Jurassic.However,the in situ spores are relatively poorly known. The specimens described here represent the first report of fertilefronds with in situ spores from Asia. Well-preserved and compressed specimens of the dipteridaceous fernDictyophyllum nilssonii (Brongniart) Goeppert were investigated from the type locality of the Hsiangchi Florain western Hubei province, southern China, collected from the upper part of the Lower Jurassic HsiangchiFormation. Sporangia and in situ spores were examined using light and electron microscopes. The sporangia arerounded, 300–450 µm in diameter, with an oblique annulus. Each sporangium produces 220–280 trilete spores.These are triangular to subtriangular in outline, 40 µm in average diameter, with smooth exines, as well asinterradial thickenings along the laesura situatedon theproximal surface. The in situ spores are comparable to thedispersed trilete spore genusDictyophyllidites. Preliminary observations on the ultrastructure of the in situ sporesare reported, which supply clues for further investigation of the systematics and phylogeny of the Dipteridaceae.In addition, the ecological implications of Dictyophyllum and its associated ferns are briefly discussed.

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1. Introduction

Traditionally, the extant family Dipteridaceae includes one genus,Dipteris Reinward, which is restricted to the Indo-Malayan regionand southern China. Some authors suggest that besides Dipteris, thefamily should also include the genus Cheiropleuria C. Presl (e.g. Katoet al., 2001; Smith et al., 2006; Schuettpelz and Pryer, 2007). The genusDipteriswas previously merged into the genus Polypodium on accountof its sorus being naked and superficial (Bower, 1926). However,Seward and Dale (1901) proposed that the genus Dipteris should berepresentative of the family Dipteridaceae. Morphologically, the leafarchitecture of Dipteris is quite characteristic, arising at distantintervals along a creeping hairy rhizome. The fronds branch dichot-omously with veins that branch at right angles to form a reticulatemesh. Sori are ex-indusiate and arranged on both sides of the midrib.The annulus of the sporangia is oblique. According to recentmorphological and molecular analysis, the family Dipteridaceae isconsidered as systematically a monophyletic clade of gleichenioid,including Dipteridaceae, Gleicheniaceae and Matoniaceae (e.g. Pryeret al., 2004; Schuettpelz et al., 2006; Smith et al., 2006; Schuettpelz andPryer, 2007). Therefore, the Dipteridaceae is of great importance forexploring the phylogeny and evolution of leptosporangiate ferns.

Compared with the limited distribution of extant Dipteridaceous,fossil records were well established during the Mesozoic, forminga significant element of many Mesozoic floras in Gondwana, Eurasia

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and North America (Tidwell and Ash, 1994; Cantrill, 1995), extendingfrom the Triassic to the Cretaceous. The earliest known dipteridaceousferns are recorded from Asia and Europe in the Carnian (Corsin andWaterlot, 1979), and their remains are common in the Lower toMiddle Jurassic (Balme, 1995). Most fossil representatives of theDipteridaceae are known from impression/compression specimens inwhich the bifurcate morphology of the leaf, pattern of venation andsoral characters provide the primary basis of assignment to the family.About six fossil genera have been recognized, including: HausmanniaDunker, Clathropteris Brongniart, Dictyophyllum Lindley and Hutton,Thaumatopteris Goeppert, Goeppertella Oishi and Yamasita and Cam-topteris Presl (Oishi and Yamasita, 1936). Additionally, silicifieddipterid ferns, Polyphacelus and Hausmannia, were reported fromJurassic sediments in Antarctica (Yao et al., 1991) and LowerCretaceous sediments inVancouver Island, Canada (Stockeyet al., 2006).

Dictyophyllum is one of the representative genera of the fossilDipteridaceae. It was first described from the Middle Jurassic ofYorkshire in England (Lindley and Hutton, 1834). Worldwide over 20species have been recorded from theMesozoic (Skog, 2001; Collinson,1996; Oishi and Yamasita, 1936;Webb, 1982) from Europe, Asia, Southand North America, Greenland and Australia. It is also a common andtypical index fossilwidely recorded fromthe Late Triassic to Early Jurassicin the southern and northern phytoprovinces of China (Zhou, 1995).

However, the fertile organs and in situ spores of this genus are poorlyknown in the Mesozoic. In situ spores are known in only four speciesbased upon lightmicroscope observations. In this paper, well-preservedfertile structures of Dictyophyllum nilssonii (Brongniart) Goeppert areinvestigated from the Lower Jurassic Hsiangchi Formation in westernHubei, China, using lightmicroscopy (LM), scanningelectronmicroscopy

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Fig. 1. Sketch map showing the fossil plant locality in Xiangxi Town, Zigui County, West Hubei Province, China.

105G. Guignard et al. / Review of Palaeobotany and Palynology 156 (2009) 104–115

(SEM) and transmission electron microscopy (TEM). We provideadditional data about sporangia, annuli and in situ spores of this speciesbased upon observations of Chinese material. Comparisons are madebetween other fossils, extant species (Dipteris) as well as dispersedspores. In addition, some preliminary TEM observations of Chinese Dic-tyophyllum spore wall ultrastructural organisation by Lugardon (1971)are also included here. A detailed study on spore wall ultrastructures ofDictyophyllumwill be published separately.

2. Material and methods

Specimens were collected from the type locality of the HsiangchiFlora in Zigui County, Hubei province (Fig.1). Fossils werewell preservedas compressions of both sterile and fertile leaves in a 50 cm thick bed ofgrey shale and blackmudstone at the top of the Lower JurassicHsiangchiFormation. Detailed descriptions of the locality and stratigraphy havepreviously been provided by Wang (1999, 2002). Co-occurring withDictyophyllum in this horizon and locality are the plants: Marattiaasiatica (Kawasaki) Harris, Todites princeps (Presl) Gothan, Phlebopterispolypodioides Brongniart, Clathropteris obovata Oishi, Coniopteris cf.hemenophylloides (Brongniart) Seward, Cladophlebis spp., Pterophyllumfirmifolium Ye, Ptilophyllum contiguum Sze, Pt. hsingshanense Wu,Otozamites hsiangchiensis Sze, Ctenozamites sp., and Podozamites sp.Among these, the fertile organs and in situ spores of Phlebopterispolypodioides Brongniart (Matoniaceae) and M. asiatica (Kawasaki)Harris (Marattiaceae), as well as cuticular anatomy and ultrastructuresof Sphenobaiera huangii (Sze) Hsu (Ginkgoales) have already beenpublished (Wang, 1999; Wang and Mei, 1999; Wang et al., 2001, 2005).

Fertile specimens were prepared for further examination ofsporangia and spores. Sporangia were removed from the fertilepinnae and first treated with hydrochloric acid (HCl) and hydrofluoricacid (HF), followed by a maceration in Schulze's solution for severalhours. After washing with water, they were then treated with 5%ammonia, followed by several changes in distilled water. Sporangiaand spores were picked using anatomical needles under the stereo-microscope. Part of the material was used for slide preparation andobservation under LM. The other part was placed on the sample stubswith double-sided sticky tape (although sometimes no adhesive wasnecessary for the isolated and single grain preparations). Sporangiaand spores were then sputter-coated with gold and viewed on a JSM6300 SEM at an acceleration voltage of 15–20 Kv in the State KeyLaboratory of Palaeontology and Stratigraphy, NIGPAS, Nanjing, China.For TEM investigations, the sporangia were treated with HF andSchulze's solution (treated material). They were prepared withparaformaldehyde and osmium tetroxide solutions, dehydrated in a

graded ethanol series and then in propylene oxide, followed byembedding in Epon resin according to the process detailed inLugardon (1971) for extant and in Wang et al. (1999, 2001) for fossilspores. The ultrathin sections were cut with a diamond knife andcontrasted with uranyl acetate and lead citrate. The grids were thenexamined with transmission electron microscope Hitachi HU 11B inToulouse University, France. The TEM resin blocks, grids and negativesare retained in Guignard's collection in University of Lyon1 and inLugardon's collection (marked as “LUG”) in Toulouse University.

In order to make comparisons with dispersed spores, a dispersedspore assemblage was recovered from the rock matrix on which themegafossils were found using standard palynological preparationtechniques. The dispersed spore samples were mounted on perma-nent slides with glycerine jelly for comparisons with in situ spores.The specimens of Dictyophyllum nilssonii figured in this paper arehoused in the Palaeobotanical Collection of NIGPAS, Nanjing, Chinaunder catalogue numbers PB21076–PB21080.

Extant Dipteris specimenwas observed using herbarium collectionat the Botanical Garden of Lyon, France. The specimen Dipterisconjugata Reinword was originally kept in the Frank Herbariumcollected from Mont Konghi at 400 m altitude in New Caledonia in1911 with the registration number LYJB000854. Sporangia materialwas directly removed from the herbarium specimen using adhesivetape, andwas placed on the stubswith double-sided sticky tape. It wasthen observed under SEM following the same routine preparationtechniques used for the fossil material.

3. Systematic description

Order FilicalesFamily DipteridaceaeGenus Dictyophyllum Lindley and Hutton, (1834)Dictyophyllum nilssonii (Brongniart) Goeppert(Plates I–V, Fig. 2)Selected references:

1836 Phlebopteris nilssonii, Brongniart, p. 376, pl. CXXXII, fig. 21846 Dictyophyllum nilssonii (Brongniart), Goeppert, p. 1191867 Dictyophyllum nilssonii (Brongniart), Schenk, p. 80, pl. XIX, figs. 6–71867 Dictyophyllum acutilobum (Braun), Schenk, p. 77, pl. XIX, figs. 2–5;

pl. XX, fig. 11867 Dictyophyllum obtusilobum Schenk, 1975, pl. XVI, fig. 1, a,b1906Dictyophyllum nilssonii (Brongniart), Nathorst, p. 5, pl. 2; pl. III, figs. 2–81922 Dictyophyllum acutilobum (Braun), Johansson, p. 9, pl. IV, figs. 10–121931Dictyophyllum nilssonii (Brongniart) Goeppert, Harris, p. 81, pl. XIV,fig. 4;

pl. XV, figs. 3, 5, 6, 8; pl. XVI, figs. 1–5, 7, 8, 11, 12; pl. XVII, fig. 9; Text-figs. 29, 301949 Dictyophyllum cf. nilssonii (Brongniart), Sze, p. 5; pl. 4, fig. 2

106 G. Guignard et al. / Review of Palaeobotany and Palynology 156 (2009) 104–115

Fig. 2. Reconstruction of the main morphological features of Dictyophyllum nilssonii from the Lower Jurassic Hsiangchi Formation in West Hubei, China. A, part of a frond, about 11 cm in itsmaximumlength. B, upperpartof a sterilepinna showing the lobe shapeandvenations, about2 cm in length. C, lowerpartof a fertile pinna showing the crowded sporangia coveringa lobe, about2cmin length.D, threesori showing thearrangementof their sporangia, eachbeingabout400µmindiameter.Note the thick, obliqueannulusof thesporangia in the twosori at left. E, sporangiumshowing a very short stalk and oblique annuli (compare with Plate IV, 4–5). F, G, Proximal view of in situ spores showing the trilete marks interradial thickenings, about 40 µm in diameter.


Age and horizon: Early Jurassic, the Hsiangchi FormationLocality: the Xiangxi Town, Zigui County, Hubei Province, ChinaMaterial studied: About ten specimens of the recent collection fromthe type locality of the Hsiangchi Flora. Most of them are sterile; onlyone pinna is preserved as fertile. Foliage materials figured in Plates Iand II are numbered with PB21076–PB21080.

3.1. Description

3.1.1. MegafossilThe specimen of Dictyophyllum nilssonii from Zigui of Hubei is

represented by several leaves varying in size and form. The largestspecimen (Plate I, 4; Fig. 2, A) is the lower part of a leaf and has pinnaewith a midrib 3 mm wide. The lowest part of the lamina of adjacentpinnae is fused, forming aweb. Above this, the margins are first entire,then lobed and bearing lobes (or pinnules) about 5 cm long arising at

Plate I. The sterile leaves of Dictyophyllum nilssonii (Brongniart) Goeppert from the Lower J

1. Middle part of a pinna showing distinct lobes and their venations. PB21078.2. Middle part of a pinna showing lobes. PB21078.3. An upper part of a pinna. PB21077.4. A larger specimen representing the lower part of a frond with three pinnae.

intervals of 2.0–2.4 cm. Towards the upper portion of the pinnae(Plate I, 1, 3) the lobes become smaller, and relatively more crowded atintervals of less than 2 cm (usually 1.5 cm or less). The margins ofthese lobes are usually nearly entire. The midrib of the lobes is distinctand broad. The main lateral veins, which supply the lobes, rise fromthe midrib at an angle of about 60° or at right angles in larger lobes.The lateral veins arise at intervals of 2–5mmand formanetwork (mesh)of irregular polygons. The finest veins are present (Plate I, 1; Fig. 2, B).The fertile pinna (Plate II,1) is similar in shape to the sterile ones, but thewhole part of the under surface of the lobe is covered with a greatnumber of sporangia (Plate II, 2; Fig. 2, C).

3.1.2. Sori and sporangiaThe sporangia are crowded and widespread on a fertile lobe. The

base of each sporangium is concealed in rock-matrix, and the stalks ofsporangia had fallen off before preservation. Thus the exact place of

urassic Hsiangchi Formation in Zigui, West Hubei, China. LM photos. Scale bar=1 cm.

PB21079.


Plate III. 1–8. In situ spores of Dictyophyllum nilssonii (Brongniart) Goeppert from the Lower Jurassic Hsiangchi Formation in Zigui, West Hubei, China. 1–3, SEM photos; 4–8, LMphotos.1–2. Proximal view of spores showing their distinct trilete marks making a superapertural ridge (sar), their interradial thickenings (it) and their smooth surfaces. SEM photos.

1. Scale bar=10 µm.2. Scale bar=5 µm.3. Distal view of an in situ spore. Note that it also shows more or less the interradial thickening of the proximal face. Scale bar=50 µm.4-6. In situ spores under LM. 4. scale bar=20 µm.5-6. Scale bar=12.5 µm.7-8. Dispersed spores assigned to Dictyophyllidites harrisii Couper from the Lower Jurassic in West Hubei. Morphologically, they resemble in situ spores of Dictyophyllum

nilssonii. Scale bars=12.5 µm.


compression of each sporangium is uncertain making their inter-pretation doubtful. It is therefore difficult to interpret their naturalarrangement. However, sometimes it is clear that they occur in very

Plate II. Fertile pinna and sporangia ofDictyophyllumnilssonii (Brongniart) Goeppert from the Low

1. A well-preserved fertile pinna. PB21080. Scale bar=1 cm.2. Detail of photo 1, showing the thick pinna rachis and a lobe covered by crowd3-4. Part of the fertile lobe, showing the arrangement of sporangia and the annuli5. Part of a sporangium showing spore mass containing in situ spores. Scale bar

small and crowded sori of 3–4 sporangia (Plate II, 3, 4; Fig. 2, D). Thesporangia are rounded, about 300–450 µm in diameter and may havevery short stalks (Fig. 2, E). The annulus, forming a ring passing the top

er JurassicHsiangchi Formation in Zigui,WestHubei, China.1–2, LMphotos; 3–5, SEMphotos.

ed sporangia. Scale bar=1 cm.. 3. Scale bar=200 µm; 4. Scale bar=100 µm.=50 µm.

Plate IV. Leaves, sporangia and spores of extant Dipteris conjugata Reinword collected from the Mont Konghi in New Caledonia.1–3, LM photos; 4–9, SEM photos.

1. Frond of Dipteris conjugata. Scale bar=5 cm.2. Part of a leaf showing venation, compare with Plate I-1. Scale bar=1 cm.3. Part of a leaf showing both venation and arrangement of sporangia. Scale bar=0.5 cm.4. Sporangium showing slightly oblique annulus, compare with fossils in Fig. 2D. Scale bar=100 µm.5. Sporangium with a stalk. Scale bar=100 µm.6. Broken sporangium showing spores within and outside the sporangium; Scale bar=100 µm.7. Monolete spores with smooth surfaces. Scale bar=30 µm.8-9. Monolete spores. Scale bars=10 µm.


of the sporangium, is well developed and rather oblique to thesporangial axis, and it is complete, consisting of about 20–25 cellswith projecting sides but sunken interiors (Plate II, 3, 4; Fig. 2, D, E).Each sporangium contains spore masses (Plate II, 5).

3.1.3. In situ sporesSpores are typically trilete, triangular to subtriangular in equatorial

outline, with rounded apices and concave or slightly convex sides(Plate III, 1–6; Fig. 2, F, G). Radius (in the sense of Punt et al., 2007) is

distinct and raised, straight or slightly undulate, extending to 3/4 ofthe spore radius. An interradial thickening (“it” on Plate V, 1), arcuatein shape, named “kyrtome” in Punt's et al. (2007) glossary, is usuallypresent on the proximal surface near or subparallel to laesura, leadingto call these spores “kyrtomate spores”. Both proximal and distalsurfaces are smooth with a thin exine about 0.5 µm in thickness. Noperispore is observed. Spore diameter ranges from 38 µm to 45 µm inequatorial view (40 µm in average). Spore content per sporangiumranges from 220 to 280 (8 sporangia were counted).


According to a preliminary study on the spore ultrastructure byLugardon (1971) (Plate V,1–2), the exospore of Dictyophyllum nilssoniishows a regular thickness on the edges and on the distal pole of thespores. The superapertural ridge (“sar” in Plate V, 1–2; in thepreliminary interpretations by Lugardon, it was called “aperturalfold”) is well developed and the apertural slit extends to a very shortdistance from the top of this ridge in the proximal region.

4. Discussion and comparisons

The taxonomic relationships of major Mesozoic Dipteridaceousgenera have been discussed by many authors (e. g. Harris, 1931; Oishiand Yamasita, 1936; Schweitzer, 1978). In particular, Dictyophyllum isvery closely related to Clathropteris, but it obviously differs mainly inthe pattern of venation (Oishi and Yamasita, 1936). In Dictyophyllumvein meshes are rarely rectangular while in Clathropteris they areusually rectangular. The differences and affinities between Dictyo-phyllum and Thaumaptopteris have been subject to many discussions.Although Thaumaptopteris was synonymized with Dictyophyllum (e.g.Seward, 1900; Harris, 1961; Herbst, 1965; Archangelsky, 1970), fourbasic characters can be used to distinguish them: (i) The base of thefrond [in Dictyophyllum the petiole branches into two arms, eachof which divides dichotomously to give off the pinnae, whereasin Thaumaptopteris the arms are very short so the pinnae are disposedin a funnel-shape at the top of the petiole (Hirmer, 1927; Oishi andYamasita, 1936)]; (ii) The shape of the pinnae [in Thaumaptopteris thepinnae are deeply dissected up to the rachis into long narrow“pinnules”, whereas in Dictyophyllum the dissection is shallow(Nathorst, 1907; Oishi and Yamasita, 1936)]; (iii) Sporangium size[the sporangia in Dictyophyllum are generally smaller with a largernumber per sorus than in Dictyophyllum (Nathorst, 1907; Oishi andYamasita, 1936; Schweitzer, 1978; Webb, 1982)]; (iv) Spore numbers(there are fewer spores in a sporangium in Thaumaptopteris than inDictyophyllum (Halle, 1921; Oishi and Yamasita, 1936; Webb, 1982)).

Dictyophyllum nilssonii is also widely documented in EarlyMesozoic deposits from Germany (Goeppert, 1846; Schenk, 1867;Gothan, 1914; Hirmer, 1927; Krausel, 1958; Weber, 1968), France(Saporta, 1873), East Greenland (Harris, 1926, 1931), Sweden (Moller,1902; Nathorst, 1906; Johansson, 1922), Romania (Popa, 2000), Japan(Oishi and Yamasita, 1936), Iran and Afghanistan (Kilpper, 1964; Fakhr,1977). In China, specimens of D. nilssonii were once documented inthe Lower Jurassic Hsiangchi Flora in Hubei Province as D. cf. nilssonii(Sze, 1949). It was also described in the Upper Triassic to LowerJurassic of other areas in Sichuan (Sze, 1933), Yunnan (Li et al., 1976)and Hunan (Zhou,1983) in South China. These specimens are, however,all fragmentary sterile pinnae or lobes.

4.1. Comparison with other Dictyophyllum species in general morphology

Dictyophyllum nilssonii from West Hubei, China is comparable tosome related species of Dictyophyllum (see Table 1). D. nilssonii fromwestern Hubei of China is similar to D. nathorsti (Zeiller, 1903) in pinnashape, but the pinna of the former is longer and more deeply lobedand each lobe arises from the midrib at a regular distances. The sori ofD. nathorsti are composed of 5–8 smaller (0.15–0.21 mm) sporangia(Zeiller, 1903). D. rugosum L. and H. from the Jurassic of Yorkshire(Harris, 1944) is also similar to D. nilssonii. In D. nilssonii, the leaveshave shorter lobes than in typical D. rugosum; the lobes are morecrowded, and the margin of the fertile pinna is less reflexed, thesporangia have rather more spores, and the spores themselves areslightly different. Themean diameter and the size range of both sporesare similar: 31–58 µm (average 40 µm) in D. rugosum and 38–45 µm inD. nilssonii from China.

D. muensteri shows leaves shaped like those of Dictyophyllumnilssonii, but they are smaller and have narrower, more distant lobes.The fertile leaves of these two taxa differ in the arrangement of the

sporangia and in the size of the spores. In D. muensteri the sporangiaaremore crowded, but in favourable places the number of sporangiumin a sori is about four. The leaf of D. exile differs from that of otherspecies in the region of attachment of the lobe. The ‘arm’ into whichthe rachis divides is remarkably long, and the web connecting thelamina of adjacent lobes is narrow, not exceeding 1 cm in width. Thepinnae of D. exile resemble those of D. nathorsti, but have shorter,more crowded lobes (teeth-like) than the other species. In D. exile, thesori have about 5 sporangia; D. muensteri has sori with 3–4 sporangia,but sometimes they are hardly recognizable. D. nilssonii has sporangiaattached singly, widely spaced in some specimens, crowded in others.In addition, two species from Japan, i.e. D. japonicum Yokoyama andD. kochibei Yokoyama from the Rhaetian of Nagato and Yamaguchi,show differences from Chinese specimens. According to Yokoyama(1891), Oishi (1932) and Oishi and Yamasita (1936), D. japonicum ischaracterized by its complete reduction of lamina towards the basalportion of the pinnae compared to D. exile. D. kochibei is morpholo-gically very close to Thaumatopteris in respect of the linear pinnulesshallowly lobed at the margin. Its long and narrow pinnules seem towarrant inclusion of this plant under the genus Thaumatopteris (Oishiand Yamasita, 1936). Further comparison between these two specieswith Chinese material is difficult because the Japanese specimensshow no detailed structure of the sporangia and in situ spores.

4.2. Comparison with in situ spores

Presently, spores of four species ofDictyophyllum have been describedand illustrated based on LM observations including, D. rugosum Lindleyand Hutton, D. nilssonii (Brongniart) Goeppert, D. exile (Braun) Nathorst,D. muensteri (Goeppert) Nathorst (Table 1). Spores of D. nilssonii fromYorkshire are described as “rounded, with rather thick smooth walls andprominent tri-radiate scars” (Harris, 1931). In a later publication, Harris(1944) noted that the spore size ranges from 26 μm to 47 μm, averagearound 37 μm.He also described the spores ofD.muensteri, which are likethose of D. nilssonii from Hubei of China in morphology, but he gavesomewhat largerdimensionof spores as 65µm.Thefigured spore is 76µmaccording to themagnification given (Harris,1944). The above descriptionof in situ spores is generally similar, although the size may be variable.However, Harris did not mention the typical arcuate thickenings in hisspore descriptions, which were described clearly by Couper (1958) as“commissures bordered by a clearmargo” based on the re-examination ofHarris' figures. Actually, spores were not suitably oriented in Harris'illustration to seewhether the commissures are raisedor not. According toHarris (1944), spores of D. rugosum were “tetrahedral, walls fairly thick,smooth; when vertically compressed, sides usually concave or flat.Triradiate scars well marked, bordered by strongly thickened cuticle;mean diameter about 40 µm”. The mean width of spore in D. nilssonii is37 μm, which is only slightly less than that of D. rugosum (about 40 μm)from Yorkshire and the size range is considerable and similar in both:31–52 μminD. rugosum, and 26–47 μminD. nilssonii. Spores ofD. rugosumtherefore are similar to those of D. nilssonii in the present study in mostaspects. Harris's description of “strongly thickened cuticle” around thetrilete mark is of course the interradial thickenings. In addition, in situspores of Dictyophyllum exile (Braun) were described from the Triassic ofGermany (Sierotin, 1962; Potonié, 1967). They are trilete triangularwith convex sides; exine is smooth or faintly punctate with a diameter of50–60 µm. Spores of D. exile are therefore different from those ofD. nilssonii, mainly due to lacking of the interradial thickenings and thesomewhat punctate spore surface.

The major differences between sporangia and spores amongrelated Dictyophyllum species are listed in Table 1. It is noteworthythat the previous observations on sori and sporangia as well as sporeswere based on LM illustrations; our study provides detailed informa-tion of sporangia and spores based on SEM and TEM observations. Thisprovides distinct evidence for exploring the spore content of eachsporangium (Plate III, 5). It is obvious that the interradial thickening


along the trilete mark on the proximal face (labelled IT in the plates)as well as spore surface features show some importance for thetaxonomy of Dictyophyllum species. In particular, preliminary TEMobservation of D. nilssonii spore suggests further ultrastructuralcharacters that may provide further clues for understanding thesystematic and phylogenic information of the Dipteridaceae.

4.3. Comparison with dispersed spores

Couper (1958) created the genusDictyophyllidites for dispersed triletespores with arcuate thickenings and smooth exine. He stated thatthis kind of dispersed spore has closer affinities with the Dictyophyllumfern (e.g. D. rugosum, D. nilssonii, D. muensteri). Couper's type species,

Table 1The major differences of sporangia and spores of related Dictyophyllum species.

Species Leaves and pinnae Sporangia Sporediameter

Interradialthickenings

Sporesurface

Dispersed sporetypes

References

D. nathorstiZeiller

pinna shorter and less lobed 5–8 smaller sporangiaforming a sorus

40–80 µm – – – Zeiller, 1903

D. rugosumLindley andHutton

pinnae with longer and narrowlobes with undulated margins

3–4 sporangia per sorus 38–58 µm(average40 µm)

triletekyrtomate

smoothfaintlypunctate

Dictyophylliditestype

Thomas, 1911, 1922; Harris, 1931,1944, 1961; Couper, 1958;

D. nilssonii(Brongniart)Goeppert

leaves with much shorter andcrowded lobes, lobe margin lessreflexed

sporangia attachedsingly, widely spaced orcrowded

26–42 µm(average 37–40 µm)

triletekyrtomate

smoothfaintlypunctate

Dictyophylliditesharrisii type

Harris, 1931, 1944; Couper, 1958;Potonié, 1962; this paper

D. exile (Braun)Nathorst

pinnae with more crowded teeth(lobes)

4–7 sporangia per sorus 50–60 µm triletekyrtomate

smooth orfaintlypunctate

Cyathidites andDeltoidosporatype

Sierotin, 1962; Potonié, 1967

D. muensteri(Goeppert)Nathorst

pinnae with smaller, narrower,more distant lobes

crowded sporangia,about 4 in each sorus

65 µm trilete smooth,punctate

Dictyophyllidites;D. paramunsteritype

Potonié, 1962, 1967; Harris, 1931;Couper, 1958; Cornet and Traverse,1975


Dictyophyllidites harrisii has a diameter of about 36 to 56 µm (average45 µm). Almost all of the in situ spores of the present D. nilssonii fromHubei, China are comparable with the dispersed spores of D. harrisiiCouper (Plate III, 7, 8). Some smaller ones, which may represent abortedspores, are similar in shape and size to Dictyophyllum mortoni (de Jersey)Playford and Dettmann, a species with smaller size range (28–45 µm,average 36 µm) first described from the Rhaetic–Liassic of SouthernAustralia (Playford and Dettmann, 1965). It is noteworthy that sporesresembling the above two dispersed species were also found in fossilMatoniaceae sporangia, e.g. Phlebopteris polypodioides from the samehorizon and locality in West Hubei (Wang and Mei, 1999). In addition,Dictyophyllidites paramuensteri, a dispersed spore species with largersize (68–85 µm), was reported from the NewYork Group of eastern U.S.A.(Cornet and Traverse, 1975). The authors compared it with the sporesproduced by Dictyophyllum muensteri (Goeppert) Nathorst.

4.4. Comparison with extant Dipteridaceae species

Recent molecular and morphological investigations suggest thatbesides the genus Dipteris the family Dipteridaceae may also include asister taxon Cheiropleuria C. Presl ascribed to the family Cheiropleur-iaceae (Kramer, 1990a,b; Kato et al., 2001; Smith et al., 2006;Schuettpelz and Pryer, 2007). However, morphologically Dipterisdiffers from Cheiropleuria primarily in having bilateral, monoleteand ellipsoid spores (tetrahedral and trilete in Cheiropleuria) andmonomorphic leaves with discrete sori (sporangia acrostichoid inCheiropleuria) (Tryon and Lugardon,1991). Sporangia in living Dipterismay be tightly clustered into sori that are circular to oval but canbecome confluent so that their individuality is lost (Seward and Dale,1901). In Cheiropleuria there is an “extensive soral area” (Bower,1915).

Plate V. Preliminary interpretations by Lugardon of twoTEM photos showing serial ultrathinthe Lower Jurassic of Hubei (China).

1. Central part (area) of the spore where the superapertural ridge (sar) is quite2. Middle part (area) of the spore radius, located where the superapertural ridge t

bar=0.5 µm. Theabbreviationson theTEMphotos (as=apertural slit; it= interpole; os = other spores) are those which have been added in the translation“L'exospore a une épaisseur régulière de l'ordre de— sur les flans et la face distas'ouvrant vers l'intérieur de la spore qui caractérise toutes les spores de Filicinéejusqu'à une très faible distance de son sommet (de ce bourrelet) dans la région dl'apex de la fente aperturale et la surface externe diminue peu à peu (indiquée poutre de part et d'autre du bourrelet, dans les régions proches du pôle proximal, upar le MeB”. English translation: The exospore shows a regular thickness of abopole (pp) the apertural fold (sar) with its apertural slit (as) opening towards(Filicophytes)— the fold is well developed and the apertural slit extends to a verwhile the distance between the apex of the apertural slit and the outer surfaceaperture. Moreover, on both sides of the fold, in the regions close to the proximprotuberance also observable in this area in SEM.

Sporangia of Dictyophyllum nilssonii, however, are scatteredwithin thesmall vein meshes, and there are no distinct sori with a commonreceptacle for the sporangia. Dipteris species typically have 64 sporesper sporangium and Cheiropleuria species can have up to 128 (Kramer,1990a,b). The sporangia of D. nilssonii produce up to 256 spores. In D.nilssonii, the spores are trilete and are triangular to subtriangular inoutline with smooth exines and interradial thickenings along thelaesura in proximal surface. All these morphological features aresimilar to living Dipteris spores. Our preliminary TEM investigationwith Bernard Lugardon seems to demonstrate that the ultrastructuralfeatures of D. nilssonii in situ spores from the Early Jurassic of both Iranand China resemble those of living Dipteris, implying close affinitiesand a phylogenic relationship with extant Dipteridaceae.

4.5. Notes on palaeoecology

In the Lower Jurassic deposits of western Hubei, ferns are one ofthe dominant plant components, including Marattiaceae, Osmunda-ceae, Matoniaceae, Dipteridaceae and Dicksoniaceae (Wang, 2002).Structural analysis based on relative abundance data indicate that theMatoniaceae is the dominant group (42.6% of total fern specimens),represented by Phlebopteris. The Dipteridaceae members rank second(26.8%), but with greater diversity. Four genera have been recognizedfor the Dipteridaceae, including Dictyophyllum, Hausmannia, Cla-thropteris and Thaumatopteris. Among them, Dictyophyllum nilssonii(Brongniart) Goeppert is the most common species. Specimens of thisspecies are frequently found with larger pinnae or fronds. In addition,some fragmentary sterile specimens of D. nathorstii Zeiller, D. rugosumas well asHausmannia sp. and Clathropteris sp. are found in associationwith D. nilssonii, but they are not abundant. The nature of fossil

sections of the aperture in the proximal region of a spore of Dictyophyllum nilssonii from

pre-eminent Photo LUG 01/082a. Scale bar=0.5 µm.hickness is decreasing (compare with SEM photos Plate III, 1–2) Photo LUG 01/083a. Scaleradial thickening; sar=pre-eminent superapertural ridge; pp=proximal pole; dp=distalof Lugardon's handwritten comments (in French) reproduced below, in which he noted:le de spores. Elle présente sur la face proximale le bourrelet apertural avec fente médianes (Filicopsida) (Filicophytes) — ce bourrelet est bien marqué et la fente aperturale s'étendu pôle proximal (fig.); il s'atténue progressivement, tandis que la distance comprise entrear des flèches orientées vers le bas) vers les extrémités de l'aperture (fig). L'exo montre enn épaississement assez fort qui correspond à la protubérancemise en évidence à ce niveauut — on the edges and on the distal pole (dp) of the spores. It presents on the proximalthe inner part of the spore, characterising all the spores belonging to ferns (Filicopsida)y short distance of the top of the fold in the proximal region; it is decreasing progressively,is decreasing gradually (indicated by arrows going down) towards the extremities of theal pole, the exospore shows a pronounced interradial thickening (it) corresponding to the


preservation and the associated sedimentary conditions suggest thatferns from this horizon represent an autochthonous or hypoau-tochthonous fluviatile peat-forming community dominated by theMatoniaceae and Dipteridaceae. This community is ecologicallycharacterized by perennial herbaceous species specialized for growthon the shaded floor of awet, tropical to subtropical forest. Therefore, itindicates a humid, tropical to subtropical climate prevailing during theEarly Jurassic in West Hubei, China. It is a representative plantcommunity recognized for the late Early Jurassic in the SouthernFloristic Province of China (Wang, 2002).

Acknowledgements

This is a special contribution in memory of Dr. Bernard Lugardon forhis great contribution to the study of spore morphology of fossil andliving plants. We acknowledge Dr. Lugardon for his preliminary TEMresults on Dictyophyllum nilssonii. We thank Prof. Z.Y. Zhou (NIGPAS,Nanjing) for his kind suggestions and support, Y.Q. Mao (NIGPAS,Nanjing) and N. Labert (University Lyon 1 France) for technicalassistances. Special thanks are due to the director (Frédéric Pautz) ofthe botanical garden of Lyon, France and the curator (Frédéric Danet) ofthe herbarium (LYJB). This research was jointly supported by theNational Key Basic Research Program of China (2006CB701401), theNational Natural Sciences Foundation of China (NSFC 40472004,40632010), the collaborative research project between the CAS andthe French CNRS, and a special grant from the State Key Laboratory ofPalaeobiology and Stratigraphy in Nanjing, China. This is a publicationUMR5125-08 and a contribution to UNESCO-IUGS project IGCP 506.

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A dipteridaceous fern with in situ spores from the Lower Jurassic in Hubei, China