Structurally preserved Nilssoniopteris from the Arida Formation (Barremian, Lower Cretaceous) of southwest Japan

Review of Palaeobotany and Palynology 156 (2009) 410–417

Contents lists available at ScienceDirect

Review of Palaeobotany and Palynology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / r ev p a l b o

Structurally preserved Nilssoniopteris from the Arida Formation (Barremian, Lower Cretaceous) of southwest Japan Toshihiro Yamada a,⁎, Julien Legrand b,d, Harufumi Nishida c,d a

Division of Life Sciences, Graduate School of Natural Science and Technology, Kanazawa University, Kanazawa 920-1192, Japan UMR 5143 CNRS, Paléobiodiversité, Systématique, Evolution des Embryophytes/Laboratoire de Paléobotanique et Paléoécologie, Université Pierre et Marie Curie, MNHN, CP 48, 57 rue Cuvier, 75231 Paris Cedex 05, France c Department of Biological Sciences, Faculty of Science and Engineering, Chuo University, Tokyo 112-8551, Japan d Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 113-0033, Japan b

a r t i c l e

i n f o

Article history: Received 7 December 2008 Received in revised form 23 March 2009 Accepted 10 April 2009 Available online 17 April 2009 Keywords: Arida Formation Barremian Bennettitales Nilssonia Nilssoniopteris

a b s t r a c t Strap-shaped foliage previously assigned to Nilssonia ex. gr. schaumburgensis is redescribed as Nilssoniopteris oishii sp. nov., based on structurally preserved foliage from the Barremian Arida Formation in Yuasa District, Wakayama Prefecture, southwest Japan. The newly assigned bennettitalean affinity of the fossil was confirmed with its cuticular morphology exhibiting paracytic (syndetocheilic) stomata, and rachis anatomy. Rachis vascular bundles are basically arranged in a circular form, which is dissected at both lateral sides for the pinna trace departure. This vascular configuration is similar to those of other bennettitalean genera and different from inverted-omega-shaped or C-shaped vascular configuration in the Cycadales. N. oishii is most abundantly found in the Ryoseki-type fossil assemblages which flourished under the dry conditions. This study clears the discrepancy between the abundance of “Nilssonia ex. gr. schaumburgensis” under dry climates and the general climatic preference of Nilssonia species to humid conditions.

1. Introduction The Bennettitales have leaves very similar to those of the Cycadales (Delevoryas, 1982; Pant, 1987), although differences in reproductive structures suggest that these two orders are only distantly related (Crane, 1985; Doyle and Donoghue, 1986; Friis et al., 2007). The foliar similarity appears to have evolved in parallel in the two orders, and epidermal features, such as cell arrangement in the stomatal apparatus and the shape of anticlinal walls of epidermal cells, when applicable, are usually used to distinguish these plants (Harris, 1969; Boyd, 2000; Pott et al., 2007). Hence, it is difficult to assign the specimen to one of these orders, unless epidermal details are preserved. This is also the case for strap-shaped foliage with undivided or sometimes segmented laminae which is abundant in Lower Cretaceous (Hauterivian to Aptian) deposits along the southern side of the Japanese Archipelago. Such foliage has been tentatively assigned to Nilssonia ex. gr. schaumburgensis (Dunker) Nathorst of the Cycadales, based on external morphology (Nathorst, 1890; Yokoyama, 1894; Oishi, 1940; Kimura, 1976; Kimura and Matsukawa, 1979; Kimura and Ohana, 1989; Kimura et al., 1991a). However, it is still possible that some specimens could be assignable to the bennettitalean morphogenus Nilssoniopteris, which shares many external

© 2009 Elsevier B.V. All rights reserved.

features with Nilssonia (Nathorst, 1909; Harris, 1969; Boyd, 2000; Cleal et al., 2006; Pott et al., 2007). Considering the distant phylogenetic relationship between the Bennettitales and Cycadales, the presence of other morphological diagnostic characters that can reliably distinguish the two orders, apart from the epidermal and stomatal features, could be inferred. Anatomical characters often provide useful keys for such higher rank taxonomy, but the rarity of structurally preserved Mesozoic foliage prevents clear anatomical distinction of putative cycad/bennettitoid foliage (Dower et al., 2004). Thus, finding anatomically preserved foliage would improve such identification, as well as adding more biological information to our understanding of these two orders. Here we report structurally preserved Nilssonia schaumburgensistype foliage from the Barremian Arida Formation in Yuasa District, Wakayama Prefecture, in southwest Japan. The foliage is described as a new species of the bennettitalean morphogenus Nilssoniopteris based on anatomical and epidermal features. Foliar anatomy is compared to other bennettitalean and cycadalean genera to exemplify reliable diagnostic features that anatomically distinguish the Bennettitales from other orders. The phytogeographical significance of this finding is also discussed. 2. Geological setting, material, and methods

⁎ Corresponding author. E-mail address: [email protected] (T. Yamada). 0034-6667/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.revpalbo.2009.04.006

Calcareous nodules containing structurally preserved plant fragments were collected at Loc. 2508 in Yoshikawa, Yuasa Town,

T. Yamada et al. / Review of Palaeobotany and Palynology 156 (2009) 410–417

411

Fig. 1. Maps showing the fossil locality and geology around the locality. 1. Map of Japan showing the Yuasa District (arrowhead). 2. Map of the Yuasa District. Boxed area is magnified in panel 3. 3. Fossil locality (#2508) and geological map around the locality based on Obata and Ogawa (1976) and Komatsu (1999). Note that unabbreviated names for the members of the Arida Formation have not given so far since the first description by Obata and Ogawa (1976). Member Al of the Arida Formation by Obata and Ogawa (1976) is included in the Yuasa Formation (Komatsu, 1999).

Wakayama Prefecture, Japan (Fig. 1, panels 1–3). The Cretaceous system in Yuasa District is composed of the Yuasa, Arida, and Nishihiro Formations, in ascending order. The Yuasa Formation comprises fluvial deposits and overlies pre-Cretaceous rocks of the Chichibu belt unconformably. The Arida Formation consists of shallow marine to offshore deposits and overlies the Yuasa Formation in a conformable way. This formation is further divided into three members, i.e., Am, Au, and At, in ascending order. The Nishihiro Formation consists of fluvial deposits and overlies the Arida Formation in an unconformable fashion (Obata and Ogawa, 1976; Komatsu, 1999). The At Member of the Arida Formation outcrops at Loc. 2508 (Fig. 1, panel 3), and Obata and Ogawa (1976) reported Barremites aff. cassidoides (Uhlig), an ammonoid indicating the uppermost Barremian, from this locality. Plant fossils have been reported from all three formations (Obata and Ogawa, 1976; Kimura and Kansha, 1978a,b; Asama et al., 1979), and the Yuasa Formation is most abundant for plant fossils among the three formations. Plant fossil assemblages of these formations are classified as Ryoseki (or Gondwana)-type floras that flourished under a climate with one or more dry periods annually (Kimura, 1987, 1988; see Section 4.4 for details). The nodule containing Nilssonia schaumburgensis-type foliage was cut into serial sections, and the contained plant fragments were transferred to cellulose acetate film using the peel technique (Joy et al., 1956). The films were mounted on slides using Eukitt (O. Kindler GmbH, Freiburg, Germany). Cuticle observation followed the protocol outlined by Kerp and Krings (1999). A chip of the specimen was soaked in 4% (v/v) hydrochloric acid (HCl) to remove the sediments. After washing in distilled water, the chip was macerated in Schulze's reagent and 5% (w/v) potassium hydroxide (KOH). The detached cuticle was dehydrated and mounted in glycerin jelly. 3. Systematic description Order Bennettitales Engler, 1892 Family unknown Genus Nilssoniopteris Nathorst, 1909 emend. Pott, Krings and Kerp, 2007.

Nilssoniopteris oishii T. Yamada, J. Legrand and H. Nishida sp. nov. Synonymy 1890 1894 1940 1976 1979 1988 1989 1991

Nilssonia cfr. schaumburgensis (Dunker) Nathorst, p. 5, pl. 1, figs. 6–9a. Nilssonia schaumburgensis (Dunker) Nathorst, Yokoyama, p. 227, pl. 20, figs. 12, 14; pl. 21, fig. 14; pl. 22, figs. 5–7. Nilssonia schaumburgensis (Dunker) Nathorst, Oishi, p. 311–314, pl. 26, figs. 9, 10; pl. 27, figs. 5–11; pl. 28, fig. 2 Nilssonia ex. gr. schaumburgensis (Dunker) Nathorst, Kimura, p. 202–204, pl. 3, fig. 5; text-figs. 14a–i. Nilssonia ex. gr. schaumburgensis (Dunker) Nathorst, Kimura and Matsukawa, p. 106–108, pl. 4, figs., 8, 9; text–figs. 12a–c. Nilssonia ex. gr. schaumburgensis (Dunker) Nathorst, Kimura and Ohana, p. 164–166, pl. 12, fig. 3; pl. 13, figs. 2–6; pl. 14, figs. 4, 5; text-figs. 26a–h. Nilssonia ex. gr. schaumburgensis (Dunker) Nathorst, Kimura and Ohana, p. 59. (name only). Nilssonia ex. gr. schaumburgensis (Dunker) Nathorst, Kimura, Ohana and Aiba, p. 30, figs. 37a–f.

Holotype: NSM-PP-9177 (Plate I, 1–6; Plate II, 1–5). Repository: National Museum of Nature and Science, Tokyo. Locality: Loc. 2508 in Yoshikawa, Yuasa, Wakayama Prefecture, Japan (Fig. 1, panel 3). Stratum: Barremian Arida Formation. Diagnosis: Gymnosperm leaf with segmented lamina with dense, simple parallel veins, 27–30 per cm. Stomata confined to intercostal area on abaxial surface. Stomata round to elliptic and oriented perpendicular to veins. Guard cells slightly overlapped by adjacent subsidiary cells. Trichome bases on abaxial surface. Rachis rhomboidal in cross section. Etymology: Specific epithet in honor of the late Prof. Saburo Oishi, who undertook many foundational studies on Japanese Mesozoic flora. Description: The single specimen represents a leaf fragment without apex and base, 1.8 cm long and 0.9 cm wide. The lamina is irregularly segmented into rectangular segments with lateral slits opening at ca. 80° to the rachis tip (Plate I, 1–3). Lamina entire, parallel-sided, and attaches to the adaxial side of the rachis, but the central part of the rachis remains exposed (Plate I, 1, 2, 4). Veins parallel, simple, and concentrated, with 27–30 veins/cm (Plate I, 1, 2).

412

T. Yamada et al. / Review of Palaeobotany and Palynology 156 (2009) 410–417

Plate I. Nilssoniopteris oishii sp. nov. 1. 2. 3. 4. 5. 6.

Type specimen (NSM-PP-9177). Scale bar = 5 mm. Line drawing of the type specimen. Scale bar = 5 mm. Section perpendicular to veins. Double-headed arrow indicates a slit between laminar segments. Scale bar = 500 µm. Oblique cross section through rachis showing gross anatomy of the leaf. Arrowhead indicates exposed part of rachis. Note that the upper and lower vascular units have reverse arrangement of tissues. c., crushed tissues, m., mechanical tissues, p., pith, x., xylem tissues. Scale bar = 1 mm. Close up of lamina shown in panel 4. Arrow indicates a stoma on the abaxial surface. Scale bar = 500 µm. External view of adaxial cuticle. Scale bar = 100 µm.

T. Yamada et al. / Review of Palaeobotany and Palynology 156 (2009) 410–417

413

Plate II. Nilssoniopteris oishii sp. nov. 1. 2. 3. 4. 5.

External view of abaxial cuticle. Bracket indicates rachis epidermis. Arrowheads show some of trichome bases. cz., costal zone, iz., intercostal zone. Scale bar = 100 µm. Internal view of stoma. Scale bar = 50 µm. Oblique cross section of stoma shown in panel 5 of Plate I (arrow). s., subsidiary cell, g., guard cell. Scale bar = 50 µm. Longitudinal section parallel to veins. Note that abaxial tissues are not preserved. Scale bar = 250 µm. Oblique cross section showing rachis anatomy. Arrow in the upper left corner shows vascular bundles which supply the lamina. Scale bar = 500 µm.

The leaf is hypostomatic and stomata are confined to inetrcostal zone on the abaxial surface (Plate I, 5, 6; Plate II, 1–3). Pavement cells of adaxial and abaxial epidermis have sinuous anticlinal walls and no papillae on their surface (Plate I, 6; Plate II, 1). The adaxial epidermis consists of rectangular cells oriented parallel to veins, 30–80 µm long and 20–25 µm wide. Differentiation between costal and intercostal zones is not obvious on the adaxial epidermis (Plate I, 6). The abaxial epidermis is divided into costal and intercostal zones in terms of distribution of stomata (Plate I, 5; Plate II, 1), but the pavement cells are not differentiated between the two zones (Plate II, 1). The abaxial pavement cells are randomly oriented, rectangular, 30–50 µm long and15–25 µm wide (Plate II, 1). Hollow trichome bases, round to elliptical and 15–25 µm in diameter, are found in both zones on abaxial epidermis (arrowheads in Plate II, 1). The stomatal apparatuses are round (50–60 × 50–60 µm), paracytic (syndetocheilic), and oriented perpendicular to the veins (Plate II, 1–3). Guard cells are 10– 15 µm wide, 50–60 µm long, and slightly overlapped by the adjacent

subsidiary cell (Plate II, 1–3). Subsidiary cells are 20–30 µm wide and 50–60 µm long (Plate II, 1–3). The lamina is 350–450 µm thick (Plate I, 3–5; Plate II, 4). Both the adaxial and abaxial epidermis are composed of a single-layer of cells (Plate I, 3, 5; Plate II, 4). The mesophyll is differentiated into adaxial palisade tissue and abaxial spongy tissue, both composed of parenchyma cells (Plate I, 3, 5; Plate II, 4). The palisade tissue is one to two cell layers thick, consisting of isodiametric cells or slightly elongated cells perpendicular to the leaf surface (Plate I, 3, 5; Plate II, 4). Spongy tissue occupies about two thirds of the mesophyll (Plate I, 5). Vascular bundles of lateral veins are 150–200 µm in diameter (Plate I, 3, 5), and each bundle is surrounded by a single-layer parenchymatous sheath (Plate I, 5). Collenchymatous tissues are developed both on adaxial and abaxial sides of the bundles, forming wedge-shaped bundle sheath extensions, but such tissues are not developed on the lateral side of the bundle (Plate I, 5). Clusters of collenchymatous cells are located just below the epidermis of the intercostal region (Plate I, 3,

414

T. Yamada et al. / Review of Palaeobotany and Palynology 156 (2009) 410–417

5). No resin bodies were observed within the mesophyll (Plate I, 3, 5; Plate II, 4). The rachis is 2.8 mm wide and rhomboidal in cross section. Each lateral side of the rachis is ridged along the entire length (Plate I, 4; Plate II, 5). Epidermis is sclerified (Plate I, 4; Plate II, 5) and rectangular epidermal cells (10–15 × 30–60 µm) are oriented parallel to long axis of rachis (bracket in Plate II, 1). Hypodermis is 3–5 cell layers thick and sclerified (Plate I, 4; Plate II, 5). In cross section, the rachis vascular bundle appears to consist of a pair of flat, adaxially concave units aligned in parallel (Plate I, 4; Plate II, 5). Each unit comprises xylem tissues with radially-filed tracheids and fibers, crushed tissues with conspicuous cavities (probably disorganized phloem tissues), and mechanical tissues containing fibers, outwardly (Plate I, 4). However, the basic configuration of the rachis bundle is columnar and is compressed from the adaxial side, resulting in a lip-like configuration composed of the two units. As the vascular column is collateral, the xylem tissues of the units face each other across somewhat disintegrated pith (Plate I, 4). The pinna bundles depart from each side of the rachis bundle, leaving a slight gap between them (arrow in Plate II, 5). 4. Discussion 4.1. Comparison to other species The obtained specimen is assigned to Nilssoniopteris based on the following features: strap-shaped leaf, segmented lamina attached to the upper surface of the rachis, exposed adaxial surface of the rachis, sinuous anticlinal walls of epidermal cells, and paracytic (syndetocheilic) stomata (Boyd, 2000; Pott et al., 2007). Foliage with exactly the same external morphology as our specimen, i.e., with dense veins and segmented lamina attached to the upper side of the rachis, is commonly found from the Upper Jurassic to Lower Cretaceous in the outer zone of Japan, including the Yuasa District. Based on these external morphological characters, such foliage has usually been identified as Nilssonia schaumburgensis (Dunker) Nathorst (Nathorst, 1890; Yokoyama, 1894; Oishi, 1940; Kimura, 1976; Kimura and Matsukawa, 1979; Kimura and Ohana, 1989; Kimura et al., 1991a), which was first described from the Lower Cretaceous (Wealden) of Germany (Dunker, 1846). However, the epidermal features of the foliage from the Japanese Upper Jurassic to Lower Cretaceous strata were unknown, because the cuticle had usually disintegrated through diagenesis. Our specimen, an exceptional case of preservation, reveals epidermal cells with sinuous anticlinal walls and paracytic stomatal apparatuses, which are not observed in N. schaumburgensis (Watson, 1969). Therefore, our fossil is designated here as a new species of Bennettitales, Nilssoniopteris

oishii, to which previously described Japanese N. schaumburgensistype foliage are also assignable. Many species of Nilssoniopteris have secondary veins that are forked in the basal-most part of the segments, while species with simple veins as in Nilssoniopteris oishii are not frequent (Kvaček, 1995). Nilssoniopteris species whose secondary veins are not or rarely forked in the basal part of segments, are listed in Table 1. Among these species, N. oishii is similar to N. smileyana Boyd and N. sp. A from the Early Cretaceous of West Greenland, and N. vulgaris Doludenko from the Middle Jurassic of Georgia in the density of their veins. N. smileyana is very similar to N. oishii in having a segmented lamina and presence of stomatal bands, but is distinguished from N. oishii by asymmetrical laminar segments and absence of trichomes on the abaxial epidermis (Boyd, 2000). N. sp. A is different from N. oishii in the absence of trichome bases on the abaxial epidermis (Boyd, 2000). N. vulgaris differs from N. oishii in prominent papillae on cuticular surface of abaxial epidermis (Doludenko and Svanidze, 1969). The genus Anomozamites is similar to the genus Nilssoniopteris in strap-shaped leaf with segmented lamina. Although Anomozamites typically has laminar segment as long as broad (Harris, 1969; Kustatscher and Van Konijnenburg-Van Cittert, 2007), these two genera are not clearly distinguished in some cases (Pott et al., 2007). Anomozamites minor (Brongniart) Nathorst, reported from the Upper Triassic (Rhatic) of Greenland by Harris (1926, 1932), shows considerable variations from typical Anomozamites laminar form to entire-margined lamina, and some specimens are similar to Nilssoniopteris oishii in an irregularly segmented laminar and having non-forking secondary veins (e.g., Fig. 13, A, B in Harris, 1926). However, the upper cuticle is papillate and guard cells are longer than subsidiary cells in A. minor. 4.2. Shared character in rachis anatomy of Bennettitales Vascular anatomy of the leaf or leaf bases is available for some bennettitalean genera, i.e., Bennettites or Cycadeoidea (Carruthers, 1870; Wieland, 1906; Ogura, 1930; Delevoryas, 1960; Nishida, 1994), Cycadeoidella (Ogura, 1930; Nishida, 1994), Dictyozamites (Bose and Zeba-Bano, 1978), Monathesia (Delevoryas, 1959), Otozamites (Tidwell et al., 1987; Ohana and Kimura, 1991; Dower et al., 2004), Ptilophyllum (Rao and Achuthan, 1968; Gupta and Sharma, 1968; Bose and Kasat, 1972; Bose and Banerji, 1984), and Zamites (Sharma, 1967; Dower et al., 2004). Saiki and Yoshida (1999) illustrated the nodal anatomy of Bucklandia kerae Saiki and Yoshida, showing petiole base anatomy, although the fossil has a unilacunar five-trace gap, which is uncommon in the Bennettitales which commonly have a single trace per leaf gap. Although the number of rachis bundles varies in these genera, all genera have the bundles arranged in a continuous ring or a modified form (Plate III, 1–5), implying that this is a shared

Table 1 Comparison of N. oishii to other species. Taxa

Vein

Vein number per cm

Stomatal band

Trichomes on abaxial surface

Lamina

Segment symmetry

N. N. N. N. N. N. N. N. N. N. N. N. N. N. N.

Simple Rarely forked Rarely forked Rarely forked Rarely forked Rarely forked Simple Rarely forked Rarely forked Rarely forked Rarely forked Rarely forked Rarely forked Simple Simple

27–30 ca. 16 22–25 10 6–12 10–18 18–20 15–25 16–20 10–11 20–32 12 20–30 14–16 20–26

Present Present Present Absent Present Present Present Present Present Present Present Present Present Present Present

Present Present Present Present Present Present Present Present Absent Absent Absent Present Present Present Absent

Segmented Linear Linear Linear Linear, but occasionally lobed Linear Linear Linear Linear Linear Segmented Linear Linear Linear Linear

Symmetrical Not applicable Not applicable Not applicable Symmetrical Not applicable Not applicable Not applicable Not applicable Not applicable Asymmetrical Not applicable Not applicable Not applicable Not applicable

oishii ajorpokensis (1) angustifolia (2) californicum (4) major (5) norvegicus (6) pecinovensis (3) pristis (5) prynadae (7) platyrachis (7) smileyana (8) variabilis (9) vulgaris (2) sp. from Andøya (6) sp. A from Ravn Kløft (8)

Data from (1) Harris (1932), (2) Doludenko and Svanidze (1969), (3) Kvaček (1995), (4) Samylina (1963), (5) Harris (1969), (6) Manum et al. (1991), (7) Wei et al. (2005), (8) Boyd (2000), (9) Bose and Banerji (1984).

T. Yamada et al. / Review of Palaeobotany and Palynology 156 (2009) 410–417

415

Plate III. Rachis anatomy of some Bennettitalean species. 1, 2, 4, 5. Scale bars = 5 mm. 3. Scale bar = 2.5 mm. 1. 2. 3. 4. 5.

Cycadeoidea petiolata Ogura. Cross section of petiole. Broken lines show possible vascular configuration. Arrowheads, possible pinna trace. Modified from Ogura (1930, p. 389, Text-fig. 8). Otozamites kerae Ohana and Kimura. Serial sections of midrib with departing lateral pinna trace (arrowheads). Modified from Ohana and Kimura (1991, p. 949, Fig. 3). Ptilophyllum cutchense Morris. Cross section of midrib departing lateral pinna trace (arrowhead). Modified from Rao and Achuthan (1968, p. 250, Text-fig. 6). Cycadeoidella japonica Ogura. Left, diagrammatic illustration showing subsequent changes of leaf trace configuration in the main stem. Right, cross section of leaf base. Modified from Ogura (1930, p. 395, Text-fig. 15 and p. 396, Text-fig. 17). Bucklandia kerae Saiki and Yoshida. Cross section of petiole base. Slender lines connecting vascular bundles show suggested vascular configuration. Modified from Saiki and Yoshida (1999, p.331, Fig. 22K).

416

T. Yamada et al. / Review of Palaeobotany and Palynology 156 (2009) 410–417

character state in the Bennettitales. These petiole traces basically derive from the main stem stele as a single unilacunar trace that distally forms a ring at the very base of the petiole, as observed in Cycadeoidea (Wieland, 1906; Delevoryas, 1960; Nishida, 1994), Cycadeoidella (Plate III, 4; Nishida, 1994), or Monathesia (Delevoryas, 1959). More distally in the rachis, the ring form alignment of the bundles is modified into various forms peculiar to each species. The rachis stele of Otozamites mortonii Dower, R. Bateman and D. W. Stev. in cross section consists of an outer C-shaped collateral bundle with adaxial phloem and an inner, round amphivasal bundle with phloem at its center (Dower et al., 2004). Otozamites sp. from the mid-Mesozoic of southern Tasmania (Tidwell et al., 1987) would have similar vascular configuration to O. mortonii, although exact vascular configuration is not available for the species because of the ill-preserved specimen. These unique vascular configurations can be interpreted as the inner bundle being originally a flat collateral bundle with adaxial xylem and abaxial phloem, which as a whole comprises the adaxial segment of a ring-shaped rachis stele in combination with the C-shaped “outer bundle”. The inner bundle in O. mortonii and O. sp. would be comparable to the inner alignment of bundles of Otozamites kerae Ohana and Kimura because the inner unit sometimes appears to be round mass (rightmost illustration in Plate III, 2). Nilssoniopteris oishii provides additional support to the present interpretation that the bennettitalean rachis stele has a basic ring form. This vascular configuration in the Bennettitales is markedly different from that of the Cycadales, because extant and fossil cycads have petiole with inverted-omega-shaped pattern of vascular bundles or with C-shaped pattern which is secondarily modified shape of inverted-omega (Stevenson, 1990; Yoshida, 2000; Hermsen et al., 2006, 2007).

1988; Yabe et al., 2003; Yamada and Uemura, 2008), which favor warm-temperate or winter-wet climates (Vakhrameev, 1991; Ziegler et al., 1993, 1996; Rees et al., 2000). On the other hand, the Ryosekitype flora is found in the Oxfordian to Albian deposits which outcrop along the outer zone of Japan (i.e., southern side of the Japanese Archipelago facing the Pacific Ocean), and contains abundant microphyllous conifers and cycadophytes (Kimura, 1976; Kimura and Kansha, 1978a,b; Kimura and Matsukawa, 1979; Kimura and Ohana, 1984; Kimura and Okubo, 1985; Kimura et al., 1985; Kimura, 1987; Kimura, 1988; Kimura and Ohana, 1989; Kimura et al., 1991a,b), which possibly grew under a climate with one or more dry periods annually (Vakhrameev, 1991; Ziegler et al., 1993, 1996; Rees et al., 2000). This climatic interpretation is further supported by thick cuticle and the heavily sunken stomata observed in some gymnosperm species (Kimura and Ohana, 1984; Kimura et al., 1985, 1991a). Along with the microphyllous gymnosperms, Nilssonia schaumburgensis-type foliage is most abundant in the Ryoseki-type fossil assemblages (Nathorst, 1890; Yokoyama, 1894; Oishi, 1940; Kimura, 1976; Kimura and Matsukawa, 1979; Kimura and Ohana, 1989; Kimura et al., 1991a). This contrasts with the general preference of Nilssonia species for warm-temperate or winter-wet climates (Vakhrameev, 1991; Ziegler et al., 1993, 1996; Rees et al., 2000). In addition, N. schaumburgensis foliage is not found in the Tetori-type flora (Ohana and Kimura, 1995; Saiki and Wang, 2003). Therefore, N. schaumburgensis is considered to be an exceptional Nilssonia species that flourished under dry conditions (Ohana and Kimura, 1995; Saiki and Wang, 2003). However, our study has revealed that these N. schaumburgensis from Japan is actually a species of bennettitalean Nilssoniopteris, clarifying the discrepancy between the abundance of N. schaumburgensis under dry climates and the climatic preference of other Nilssonia species.

4.3. Comparison of leaf anatomy to Nilssonia Nilssoniopteris is closely similar to the cycadalean genus Nilssonia in its external morphology. These two genera are distinguished based on epidermal features, such as cell arrangement of the stomatal apparatus, i.e., syndetocheilic stomata in Nilssoniopteris versus haplocheilic stomata in Nilssonia (Harris, 1964; Dower et al., 2004; Pott et al., 2007). Dower et al. (2004) stated that the rachis stele of “Nilssonia cf. tenuinervis” (this species requires an alternative species name; see Cleal et al., 2006) is similar to that of the extant cycadalean genus Stangeria, in which the rachis exhibits a C-shaped dorsiventral vascular bundle configuration, although anatomical details are unclear in the rachis of their specimen. If this is the case, vascular bundle configuration could be another anatomical character distinguishing Nilssonia from Nilssoniopteris, with a radially-arranged vascular bundle in Nilssoniopteris. Further observations on rachis anatomy in Nilssonia are needed to explore this possibility. Nilssoniopteris oishii has laminar anatomy similar to Nilssonia orientalis Heer (Stopes, 1910), as well as other cycadalean species i.e., Yelchophyllum omegapetiolaris Hermsen, T. N. Taylor, E. L. Taylor and D. W. Stev. and Zamia integrifolia L. f. (Hermsen et al., 2007), in vascular bundles accompanied by sclerified sheath extensions. However, sheath extensions are also developed in extant angiosperm species to increase mechanical strength of their lamina (e.g., Esau, 1977), suggesting that such mechanical tissues are subject to evolve in parallel. 4.4. Paleophytogeographic and paleoclimatic significance Late Jurassic to Early Cretaceous floras of Japan are separable into two major types, Tetori and Ryoseki (Kimura, 1987, 1988). The Tetoritype flora is found in the Oxfordian to Aptian deposits of the Tetori Group in the Hokuriku district, in the northern part of central Japan. The flora contains abundant pteridophytes, macrophyllous cycadophytes, and ginkgoaleans (Kimura and Sekido, 1976a,b; Kimura, 1987,

Acknowledgments We thank Mr. Y. Mizuno for his assistance in collecting fossils. Dr. K. Uemura provided facilities to make the peel sections. This study was partly supported by a research project of the National Museum of Nature and Science entitled “Historical development and origin of biodiversity under global environmental dynamics.” References Asama, K., Matsukawa, M., Obata, I., 1979. Plant fossils from the Lower Cretaceous Nishihiro Formation. Mem. Natl. Sci. Mus. 12, 83–92. Bose, M.N., Banerji, J., 1984. The fossil floras of Kachchh. I-Mesozoic megafossils. Palaeobotanist 33, 1–189. Bose, M.N., Kasat, M.L., 1972. The genus Ptilophyllum in India. Palaeobotanist 19, 115–145. Bose, M.N., Zeba-Bano, 1978. The genus Dictyozamites Oldham from India. Palaeobotanist 25, 79–99. Boyd, A., 2000. Bennettitales from the Early Cretaceous floras of West Greenland: Pterophyllum and Nilssoniopteris. Palaeontogr., Abt. B 255, 47–77. Carruthers, W., 1870. On fossil Cycadean stems from the secondary rocks of Britain. Trans. Li. Soc. 26, 675–708 (pls. lix–lxiii). Cleal, C.J., Rees, P.M.c.A., Zijlstra, G., Cantrill, D.J., 2006. A classification of the type of Nilssoniopteris Nathorst (fossil Gymnospermophyta, Bennettitales). Taxon 55, 219–222. Crane, P.R., 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Ann. Mo. Bot. Gard. 72, 716–793. Delevoryas, T., 1959. Investigations of North American cycadeoids: Monanthesia. Am. J. Bot. 46, 657–666. Delevoryas, T., 1960. Investigations of North American cycadeoids: trunks from Wyoming. Am. J. Bot. 47, 778–786. Delevoryas, T., 1982. Perspectives on the origin of cycads and cycadeoids. Rev. Palaeobot. Palynol. 37, 115–132. Doludenko, M.P., Svanidze, T.I., 1969. The Late Jurassic flora of Georgia. Trans. Geol. Inst., Acad. Sci. USSR 178, 1–118 (in Russian). Dower, B.L., Bateman, R.M., Stevenson, D.W., 2004. Systematics, ontogeny, and phylogenetic implications of exceptional anatomically preserved cycadophyte leaves from the Middle Jurassic of Bearreraig Bay, Skye, Northwest Scotland. Bot. Rev. 70, 105–120. Doyle, J.A., Donoghue, M.J., 1986. Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Bot. Rev. 52, 321–431.

T. Yamada et al. / Review of Palaeobotany and Palynology 156 (2009) 410–417 Dunker, W., 1846. Monographie der norddeutschen Wealdenbildung. Ein Beitrag zur Geognosie und Naturgeschichte der Vorwelt. Oeme und Müller, Braunschweig. Esau, K., 1977. Anatomy of Seed Plants. John Wiley and sons, New York, USA. Friis, E.M., Crane, P.R., Pedersen, K.R., Bengtson, S., Donoghue, P.C.J., Grimm, G.W., Stampanoni, M., 2007. Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature 450, 549–552. Gupta, K.M., Sharma, B.D., 1968. Investigations on the Jurassic flora of the Rajmahal Hills, India. 2-On a new species of Ptilophyllum, P. sahnii from Amarjola in Amarapara region. J. Palaeontol. Soc. India 11, 1966. Harris, T.M., 1926. The Rhaetic flora of Scoresby Sound east Greenland. Medd. Grønl. 68 (2), 44–148. Harris, T.M., 1932. The fossil flora of Scoresby Sound. Part 3. Caytoniales and Bennettitales. Medd. Grønl. 85 (3), 1–133. Harris, T.M., 1964. The Yorkshire Jurassic Flora II. Caytoniales, Cycadales and Pteridosperms. British Museum (Natural History), London. Harris, T.M., 1969. The Yorkshire Jurassic Flora. III. Bennettitales. Trustees of British Museum (Natural History), London. Hermsen, E.J., Taylor, T.N., Taylor, E.L., Stevenson, D.W., 2006. Cataphylls of the Middle Triassic cycad Antarcticycas schopfii and new insights into cycads evolution. Am. J. Bot. 93, 724–738. Hermsen, E.J., Taylor, T.N., Taylor, E.L., Stevenson, D.W., 2007. Cycads from the Triassic of Antarctica: permineralized cycad leaves. Int. J. Plant Sci. 168, 1099–1112. Joy, K.W., Willis, A.J., Lacey, W.S., 1956. A rapid cellulose peel technique in palaeobotany. Ann. Bot. 20, 635–637 (n.s.). Kerp, H., Krings, M., 1999. Light microscopy of cuticles. In: Jones, T. (Ed.), Fossil Plants and Spores: Modern Techniques. Geological Society, London, pp. 52–56. Kimura, T., 1976. Mesozoic plants from the Yatsushiro Formation (Albian), Kumamoto Prefecture, Kyushu, Southwest Japan. Bull. Natl. Sci. Mus. Ser. C 2, 179–208. Kimura, T., 1987. Recent knowledge of Jurassic and Early Cretaceous floras in Japan and phytogeography of this time in East Asia. Bull. Tokyo Gakugei Univ., Sect. 4 39, 87–115. Kimura, T., 1988. Jurassic macrofloras in Japan and palaeophytogeography in East Asia. Bull. Tokyo Gakugei Univ., Sect. 4 40, 147–164. Kimura, T., Kansha, Y., 1978a. Early Cretaceous plants from the Yuasa Ditrict and Aridagawa Valley, Wakayama Prefecture, in the outer zone of Japan. Part I. Bull. Natl. Sci. Mus. Ser. C 4, 99–116. Kimura, T., Kansha, Y., 1978b. Early Cretaceous plants from the Yuasa District and Aridagawa Valley, Wakayama Prefecture, in the outer zone of Japan. Part II. Bull. Natl. Sci. Mus. Ser. C 4, 165–180. Kimura, T., Matsukawa, M., 1979. Mesozoic plants from the Kwanto Mountainland, Gumma Prefecture, in the outer zone of Japan. Bull. Natl. Sci. Mus. Ser. C 5, 89–112. Kimura, T., Ohana, T., 1984. Ptilophyllum elongatum sp. nov., from the Lower Barremian Kimigahama Formation, the Choshi Group, in the outer zone of Japan. Proc. Jpn. Acad., Ser. B 60, 381–384. Kimura, T., Ohana, T., 1989. Late Jurassic plants from the Oginohama Formation, Oshika Group in the outer zone of Northeast Japan (II). Bull. Natl. Sci. Mus. Ser. C 15, 53–70. Kimura, T., Okubo, A., 1985. Nilssonia dictyophylla sp. nov. from the Lower Cretaceous Choshi Group, in the outer zone of Japan. Proc. Jpn. Acad., Ser. B 61, 430–432. Kimura, T., Sekido, S., 1976a. Dictyozamites and some other cycadophytes from the early Lower Cretaceous Oguchi Formation, the Itoshiro Group, Central Honshu, Japan. Trans. Proc. Palaeont. Soc. Japan, N. S. 101, 291–312. Kimura, T., Sekido, S., 1976b. Mesozoic plants from the Akaiwa Formation (Upper Neocomian), the Itoshiro Group, Central Honshu, Japan. Proc. Palaeont. Soc. Japan, N. S. 103, 343–378. Kimura, T., Saiki, K., Arai, T., 1985. Frenelopsis choshiensis sp. nov., a cheirolepidiaceous conifer from the Lower Cretaceous Choshi Group in the outer zone of Japan. Proc. Jpn. Acad., Ser. B 61, 426–429. Kimura, T., Ohana, T., Aiba, H., 1991a. Late Jurassic plants from the Shishiori Group, in the outer zone of northeast Japan (II). Bull. Natl. Sci. Mus. Ser. C 17, 21–40. Kimura, T., Okubo, A., Miyahashi, H., 1991b. Cuticular study of Ptilophyllum leaves from the Lower Cretaceous Choshi Group, in the outer zone of Japan. Bull. Natl. Sci. Mus. Ser. C 17, 129–152. Komatsu, T., 1999. Depositional environments and bivalve fossil assemblages of the Lower Cretaceous Arida Formation, southweat Japan. J. Geol. Soc. Jpn. 105, 643–650. Kustatscher, E., Van Konijnenburg-Van Cittert, J.H.A., 2007. Taxonomical and palaeogeographic considerations on the seedfern genus Ptilozamites with some comments on Anomozamites, Dicroidium, Pseudoctenis and Ctenozamites. N. Jb. Geol. Paläont. Abh. 243, 71–100. Kvaček, J., 1995. Cycadales and Bennettitales leaf compressions of the Bohemian Cenomanian, Central Europe. Rev. Palaeobot. Palynol. 84, 389–412.

417

Manum, S.B., Bose, M.N., Vigran, J.O., 1991. The Jurassic flora of Andøya, northern Norway. Rev. Palaeobot. Palynol. 68, 233–256. Nathorst, A.G., 1890. Beiträge zur mesozoischen Flora Japans. Denks. Math.-Nat. Cl. Kaiser. Akad. Wiss., Wien, vol. 57, pp. 41–60. Nathorst, A.G., 1909. Über die Gattung Nilssonia Brongn. mit besonderer Berücksichtigung schwedischer Arten. K. Sven. Vetensk.Akad. Handl. 43, 1–40. Nishida, H., 1994. Morphology and evolution of Cycadeoidales. J. Plant Res. 107, 479–492. Obata, I., Ogawa, Y., 1976. Ammonites biostratigraphy of the Cretaceous Arida Formation, Wakayama Prefecture. Bull. Natl. Sci. Mus. Ser. C 2, 93–110. Ogura, Y., 1930. On the structure and affinities of some Cretaceous plants from Hokkaido. J. Fac. Sci., Imp. Univ. Tokyo, Sect. 3 2, 381–412. Ohana, T., Kimura, T., 1991. Permineralized Otozamites leaves (Bennettitales) from the Upper Cretaceous of Hokkaido, Japan. Trans. Proc. Palaeont. Soc. Japan, N. S. 164, 944–963. Ohana, T., Kimura, T., 1995. Late Mesozoic phytogeography in Eastern Eurasia, with special reference to the origin of angiosperms in time and site. Proc. 15th Int. Symp. Kyungpook Nat. Univ., Korea, pp. 293–328. Oishi, S., 1940. The Mesozoic floras of Japan. J. Fac. Sci., Hokkaido Imp. Univ., Sect. 4 5, 123–480. Pant, D.D., 1987. The fossil history and phylogeny of the Cycadales. Geophytology 17, 125–162. Pott, C., Krings, M., Kerp, H., 2007. First record of Nilssoniopteris (Gymnospermophyta, Bennettitales) from the Carnian (Upper Triassic) of Lunz, Lower Austria. Palaeontology 50, 1299–1318. Rao, A.R., Achuthan, V., 1968. Further contribution to our knowledge of the anatomy of Ptilophyllum. Palaeobotanist 16, 249–257. Rees, P.M.c.A., Ziegler, A.M., Valdes, P.J., 2000. Jurassic phytogeography and climates: new data and model comparisons. In: Huber, B.T., Macleod, K.G., Wing, S.L. (Eds.), Warm Climates in Earth History. Cambridge University Press, Cambridge, pp. 297–318. Saiki, K., Wang, Y., 2003. Preliminary analysis of climate indicator plant distribution in the Early Cretaceous of China. J. Asian Earth Sci. 21, 813–822. Saiki, K., Yoshida, Y., 1999. A new Bennettitalean trunk with unilacunar five-trace nodal structure from the Upper Cretaceous of Hokkaido, Japan. Am. J. Bot. 86, 326–332. Samylina, V.A., 1963. The Mesozoic flora of the lower course of the Aldan River. Paleobotanika 4, 57–139. Sharma, B.D., 1967. Investigations on the Jurassic flora of Rajmahal Hills, India. 3. A review of the genus Ptilophyllum of Morris, with description of two new species from Amarjola in the Rajmahal Hills. Palaeontogr., Abt. B 120, 139–150. Stevenson, D.W., 1990. Morphology and systematics of the Cycadales. Mem. N. Y. Bot. Gard. 57, 8–55. Stopes, M.C., 1910. The internal anatomy of “Nilssonia orientalis”. Ann. Bot. 14, 389–393. Tidwell, W.D., Kim, J.H., Kimura, T., 1987. Mid-Mesozoic leaves from near Ida Bay, southern Tasmania, Australia. Pap. Proc. R. Soc. Tasman. 121, 159–170. Vakhrameev, V.A., 1991. Jurassic and Cretaceous Floras and Climates of the Earth. Cambridge University Press, Cambridge. Watson, J., 1969. A revision of the English Wealden flora, I. Charales-Ginkgoales. Bull. Br. Mus. Nat. Hist., Geol. 17, 210–254. Wei, W., Sun, Y., Wang, Y., 2005. Nilssoniopteris from the Lower Cretaceous Changcai Formation in Yanbian area of Jilin, China. Global Geol. 24, 1–6. Wieland, G.R., 1906. American Fossil Cycads. Carnegie Institution of Washington, Washington, D.C. (Publ. 34). Yabe, A., Terada, K., Sekido, S., 2003. The Tetori-type flora, revisited: a review. Mem. Fukui Pref. Dinosaur Mus. 2, 23–42. Yamada, T., Uemura, K., 2008. The plant fossils from the Kaizara Formation (Callovian, Jurassic) of the Tetori Group in the Izumi district, Fukui Prefecture, Central Japan. Paleontol. Res. 12, 1–17. Yokoyama, M., 1894. Mesozoic plants from Kozuke, Kii, Awa, and Tosa. J. Coll. Sci., Imp. Univ. Jpn. 7, 201–231. Yoshida, A., 2000. Histological study on the petioles of extant cycads. Res. Inst. Evol. Biol. Sci. Rep. 9, 49–71. Ziegler, A.M., Parrish, J.M., Yao, J., Gyllenhaal, E.D., Rowley, D.B., Parrish, J.T., Shangyou, N., Bekker, A., Hulver, M.L., 1993. Early Mesozoic phytogeography and climate. Philos. Trans.R. Soc. Lond., Ser. B 341, 297–305. Ziegler, A.M., Rees, P.M.c.A., Rowley, D.B., Bekker, A., Qing, L., Hulver, M.L., 1996. Mesozoic assembly of Asia: constraints from fossil floras, tectonics, and paleomagnetism. In: Yin, A., Harrison, M. (Eds.), The Tectonic Evolution of Asia. Cambridge University Press, Cambridge, pp. 371–400.