2025 年 29 巻 p. 316-331
The discovery of excellently preserved articulated plant fossils from the Oxfordian (Upper Jurassic) Tochikubo Formation of Shidazawa, Minamisoma, Fukushima, northeast Japan, allows for the description and reconstruction of the new fossil whole-plant bennettitalean Ohaniella ptilofolia gen. et sp. nov., based on preserved axes with attached foliage of the Ptilophyllum jurassicum-type and attached ovuliferous reproductive structures (flowers/seed cones). Recent excavations unveiled plant fossils with axes carrying a whorl of apically arranged leaves, in the centre of which remnants of ovuliferous reproductive structures in the form of possible seed cones are preserved. The findings of Weltrichia-like microsporangiate flowers in the same bedding planes on slabs exclusively yielding foliage of the Ptilophyllum jurassicum-type suggest that (a) these might have been produced by the plants carrying Ptilophyllum jurassicum-type foliage and just have been shed as was the case in the closely related Kimuriella densifolia, and (b) Ohaniella ptilofolia gen. et sp. nov. plants might have formed more or less monotypic stands of shrub thickets referring to special environmental conditions and requirements.
In the last decade, knowledge about the architecture, growth habit, habitat preferences and ecology of bennettitalean plants has made profound advances. Especially the divaricate plant architecture or growth habit identified for many of those plants has contributed significantly to our understanding of the lifestyle or life strategy of williamsoniaceous bennettites (Pott, 2014, 2016; Pott and McLoughlin, 2014; Pott and Axsmith, 2015; Pott et al., 2015, 2016, 2017; Pott and Takimoto, 2022). In particular, the whole-plant taxa Wielandiella angustifolia from the Rhaetian of Sweden, Greenland and Germany, and Wiellandiella villosa from the Callovian–Oxfordian of Inner Mongolia, China, provided a wealth of information (Pott, 2014; Pott et al., 2015; Pott and Jiang, 2017). In one of the most recent accounts of a whole-plant bennettitalean, Pott and Takimoto (2022) described a plant restored from excellently preserved articulated fossils showing divaricately branched axes with attached foliage and ovuliferous flowers in different stages of anthesis and maturation (including mature seed cones). This plant was named Kimuriella densifolia and was discovered in the uppermost portion of the Oxfordian Tochikubo Formation in northeast Japan.
The flora uncovered from the Tochikubo Formation is quite diverse and constitutes lycophytes, sphenophytes, ferns and some conifers (see, e.g. Kimura and Tsujii, 1984; Kimura and Ohana, 1988a, b; Takimoto et al., 1997, 2008; Takimoto and Ohana, 2016; Takimoto, 2018; Pott and Takimoto, 2022). The body of plants, and with it the dominating portion of the vegetation, however, belongs to the group largely circumscribed as cycadophytes. The cycadophytes in a narrower sense comprise the cycads (Cycadales), the bennettitaleans (Bennetittales) and a peculiar group of plants with tangled axes and whorls of entire-margined or segmented leaves on short shoots named Nilssoniales, which, however, shows some affinities to ginkgophytes (Watson and Cusack, 2005; Pott et al., 2012). Besides some cycads (Pseudoctenis, Encephalartites, Cycadites) and several Nilssonia and Nilssoniocladus species, roughly 14 taxa of bennettitaleans have been described until now from the Tochikubo Formation; several more are waiting to being described (Pott and Takimoto, work in progress). Not only are they dominant in number of taxa, but also in the body of preserved fossils assignable to these taxa. Certainly, some plant groups with more robust species do have better preservation potential than others (such as delicate ferns), but embedding or preservation conditions were beneficial for delicate taxa here as well. Still, the number of preserved fossils of cycadophytes is so overwhelmingly high that we can presume cycadophytes, and especially bennettitaleans, were dominating the vegetation that has been preserved in the Tochikubo Formation during the Oxfordian (Late Jurassic).
Here, we describe from the very same outcrop, just slightly off the site where the fossils of K. densifolia were discovered, some recently found fossil slabs that preserved another articulated bennettitalean plant, which is mostly differentiated from K. densifolia by its different foliage and presumably longer growth increments, but smaller vegetative dimensions, as Ohaniella ptilofolia gen. et sp. nov.
The material studied here derives from the upper part of the Oxfordian (Upper Jurassic) Tochikubo Formation, which crops out in Fukushima, northeast Japan. During the construction of the Jōban Expressway (2005–2010) and later construction, the sedimentary layers of the Tochikubo Formation were temporarily exposed at Shidazawa, Haramachi-ku (Shidazawakita, 37°39′01″N, 140°55′03″E; Figure 1) close to the Minamisoma Interchange, giving the opportunity to obtain several thousands of specimens of excellently preserved plant fossils (Ohana and Takimoto, 2008; Takimoto, 2018). The fossils were collected between January 2011 and the end of 2022 by members of the Research Association of the Somanakamura Group. The designated holotype specimen was collected by Muneo Taira on 6 February 2011 from the slope at locality L1 (Figures 1C, 2A), on just the opposite side to the slope from which the Kimuriella specimens were derived (Figure 2A; see Pott and Takimoto, 2022); the designated epitype specimen was collected in 2022 from a slope less than 200 m to the east at locality L2 (Figures 1C, 2A).
The two type specimens were examined in detail, and >50 further specimens with disarticulated foliage were also referenced for a sound description of the attached foliage. For comparison, original material of Nipponoptilophyllum bipinnatum (Kimura and Tsuiji, 1984) was also re-examined. The examined specimens are held in the palaeontological collections of the Minamisoma City Museum (MM) in Minamisoma (Minamisōma), Fukushima, and the National Museum of Nature and Science (NSM) in Tsukuba, Ibaraki, under accession numbers MM-000940–000957; NSM PP-8258–8285, NSM PP-8399–8406 and NSM PP-8524. Some of the material studied was temporarily on loan to the Ibaraki Nature Museum (INM) in Bando, Ibaraki, for study by the authors. The studied material also includes original specimens of the pioneering palaeobotanical studies in the Tochikubo Formation by Kimura et al. (1988) and Kimura and Ohana (1988a, b), which were also collected at the Shidazawa locality.
The macrofossils were photographed with a Nikon D80/Nikkor AF-S Micro 60 mm 1:2.8G ED system digital camera. In order to enhance contrast, cross-polarisation (i.e., polarised light sources together with an analysing filter in front of the camera lens) was used. Analysis of hand specimens was performed with Olympus stereo microscopes in the respective museums and high-resolution digital imaging software.
The plant fossils are preserved as compressions in most cases, but attempts to isolate the organic matter and cuticles according to the processes outlined in, for example, Pott (2014, 2016), as well as applying epifluorescence microscopy, did not produce any useful results or cuticle remains (see Kimura et al., 1988; Pott and Takimoto, 2022). Therefore, the descriptions of each plant and its parts are based on the available macrofossils only.
Remarks on terminology.—The most remarkable features of the Bennettitales are their reproductive organs, which can most simply be described as flowers. Although these flowers differed in the details of their anatomy from the true flowers of angiosperms, they clearly represent an experiment in plant architecture that preceded but paralleled in architecture some of the adaptations of modern flowering plants. For this reason and convenience, and as done earlier (e.g. Pott, 2014; Pott and Takimoto, 2022), we here use the term ‘flower’ and related terms such as ‘gynoecium’ for the immature reproductive organs of Bennettitales, always aware of the fact that they do not represent true angiosperm flowers. For the mature ovuliferous flowers, we use the term ‘seed cone’ to avoid suggesting homologies that might not really be supported.
The collected plant fossils come from exposures of the Tochikubo Formation (Figures 1A, 2), which constitutes the middle part of the Somanakamura Group, cropping out in a narrow zone along the eastern margin of the Abukuma Upland at the eastern shoreline of north-eastern Honshu. A precise age of the Tochikubo Formation is difficult to assess; it is generally regarded as of Oxfordian (Late Jurassic) in age, based on the overlying Kimmeridgian–Tithonian Nakanosawa and underlying Callovian Yamagami formations. A detailed description of the geological setting of outcrops of the Tochikubo Formation at the Shidazawa locality was provided by Pott and Takimoto (2022), and therefore, only information indispensable for the present study is mentioned here.
Exposures of the Tochikubo Formation can reach up to 450 m thick locally and constitute mostly non-marine fluvial to near-shore and ‘quiet’ lake deposits, in the middle portion of which shale-predominating alternated sandstone beds are commonly intercalated with thin coal seams and carbonaceous shales. In the latter beds, plant fossils are particularly abundant. The facies comprising the plant beds is regarded as being of mixed load (traction and suspension), deposited in a non-marine environment (Takizawa, 1985). The facies of the Tochikubo Formation change in ascending order from a fluvial to lake association, flood plain, alluvial fan, into a delta-front coastal environment in its uppermost part (Takizawa, 1985; Kubo et al., 1990; Takimoto, 2018). Therefore, the depositional environment of the upper part of the Tochikubo Formation was probably a transitional zone between a deltaic and a coastal environment (see Takizawa, 1985; Ando et al., 2022).
The fossils under study here derive from the plant beds located in the upper part of the Tochikubo Formation (Figure 2). The holotype specimen was collected from a 60-cm-thick grey shale in the layer labelled L1 (Figure 2A); the epitype specimen derived from a 2-m-thick shale bed intercalated between coarse-grained sandstones in the layer labelled L2 (Figure 2A, B), which became thicker eastwards.
Preceding remarks.—In the following section, we describe the growth habit of a whole-plant species reconstructed from articulated fossil specimens. Besides these articulated specimens, several specimens of disarticulated leaves, shed or snapped off unspontaneously, occur on the same and other slabs from the same bedding planes that are assignable to the same whole-plant species. We here include these specimens in the described whole-plant species because there is reasonable assumption that all these organs stem from parent individuals of the same population of this species, even if strict application of fossil taxonomy would also allow the disarticulated organs to be assigned to other fossil taxa such as Ptilophyllum or Weltrichia. We also regard other specimens of disarticulated leaves from the Japanese fossil record as deriving from the same whole-plant species (see below), but we refrain from formally including those in the species to avoid nomenclatural confusion.
Order Bennettitales Engl., 1892
Family Williamsoniaceae (Carruth., 1870) Nath., 1913
Genus Ohaniella C.Pott and H.Takimoto, gen. nov.
Generic diagnosis.—Woody plants with sympodially branched (or divaricate) axes with persistent leaf bases along axes below reproductive organs; petiolate leaves of the Ptilophyllum-type, shed as a whole, spirally attached below flowers; main axis terminating in a single flower; microsporangiate and ovuliferous flowers deemed separate, seed cones of the Bennetticarpus-type.
Type.—Ohaniella ptilofolia C.Pott and H.Takimoto, sp. nov.
Etymology.—Named after Tamiko Ohana (*1953) in honour of her excellent contributions to Japanese palaeobotany.
Ohaniella ptilofolia C.Pott and H.Takimoto, sp. nov.
Disarticulated leaves from the Japanese fossil record, here regarded as shed or snapped-off parts of Ohaniella ptilofolia gen. et sp. nov. plants, include:
?1984 Nipponoptilophyllum bipinnatum, pro parte (detached ‘penultimate pinnae’ only), Kimura and Tsujii, p. 385, text-figs. 1b–10 [Oxfordian Tochikubo Formation of the Somanakamura Group]; see ‘Discussion’
1988b Ptilophyllum jurassicum, Kimura and Ohana, p. 151, pl. 8, figs. 1–3; pl. 9, figs. 1, 2; pl. 10, fig. 1; text-fig. 15a–d [Oxfordian Tochikubo Formation of the Somanakamura Group]
?1988b Nipponoptilophyllum bipinnatum Kimura and Tsujii, pro parte (detached ‘penultimate pinnae’ only), Kimura and Ohana, p. 156, text-fig. 19a–d [Oxfordian Tochikubo Formation of the Somanakamura Group] (no new specimens shown, repetition of old sketches only); see ‘Discussion’
1989 Ptilophyllum oshikaense Kimura and Ohana, cum syn., p. 55, pl. 9, figs. 5–8, pl. 10, figs. 1–3, pl. 12, fig. 1, text-fig. 17a–g [Oxfordian portion of the Oginohama Formation; see Takizawa et al., 1974; Okawa et al., 2013]
1991 Ptilophyllum oshikaense Kimura and Ohana, Kimura et al., p. 26, text-fig. 31 [Oxfordian Moné Formation]
Etymology.—From Greek πτ
Specific diagnosis.—As for genus with the following additions: axis increments about as long as leaves; persistent leaf bases elongate-rectangular and widely spaced; leaves petiolate, identical to Ptilophyllum jurassicum; petiole widening distally, spatulate, decurrent; lamina elongate-linear with densely arranged, parallel-sided leaflets; leaflets narrow, straight, parallel-sided for the most part, narrowing abruptly to the obtusely pointed apex, base of leaflet asymmetric, both acroscopic and basiscopic basal margins straight, but sometimes acroscopic basal angle slightly rounded; veins parallel, arising from whole region of attachment, simple, ending near apex; surface of seed cones characterised by rhombic to hexagonal shields (interseminal scale heads).
Types.—Holotype: MM-000940, branched axis with attached leaves, here designated, and figured in Figure 3A. Epitype: MM-000941, branched axis with attached leaves, here figured in Figure 4.
Additional material investigated.—NSM PP-8258–8285, 8399–8406; MM-000942, 000943, 000954, 000955.
Type locality.—Shidazawa, Haramachi-ku (Shidazawakita, 37°39′01″N, 140°55′03″E), Minamisoma, Fukushima, Japan (Figure 1).
Type horizon and age.—Tochikubo Formation, Oxfordian, Late Jurassic (Figure 2).
Distribution.—Oxfordian, Upper Jurassic; Japan.
Description.—Ohaniella ptilofolia gen. et sp. nov. is a fossil whole-plant taxon represented by divaricately branched axes with distally attached whorls of leaves. Two specimens under study yield articulated plant fossils showing prominent branched axes covered with elongate-rectangular persistent leaf bases in the proximal portions and with attached Ptilophyllum-type foliage in the distal portions. Obvious microsporangiate and ovuliferous flowers are so far unknown from the plant, because specimens yielding flowers and seed cones have not been encountered in the close vicinity of the articulated specimens except for two specimens each yielding a Weltrichia-type microsporangiate flower, but since a conspecificity of the latter with O. ptilofolia gen. et sp. nov. cannot be ascertained with confidence, information on the reproductive organs of O. ptilofolia gen. et sp. nov. is scarce.
However, the articulated type specimen yields a solid spherical structure in the centre of the leaf whorl at the position where flowers or seed cones are to be expected as in closely related bennettitalean plants like Kimuriella densifolia and Wielandiella angustifolia (Pott, 2014; Pott and Takimoto, 2022). The structure displays portions of the surface of a bennettitalean gynoecium or seed cone of the Bennetticarpus-type in the form of the characteristic small rhombic to hexagonal shields, reflecting the interseminal scale heads (Pott, 2024). Therefore, we interpret this structure as the surface of an ovuliferous flower, maybe at the stage of a mature or maturing seed cone (see below).
Two slabs yield articulated plant remains of axes with attached leaves and are described in detail below; several further specimens yield disarticulated leaves and are used for corroborating the original description of the foliage but are not described in detail. The leaves are identified being identical with P. jurassicum, the original description of which included an examination of more than 83 specimens (Kimura and Ohana, 1988b), and thus can be regarded as profound study, even if the circumscription of the foliage needs to be emended slightly here (see below).
Description of the articulated specimensHolotype.—The largest slab yielding an articulated fossil (MM-000940, holotype; Figure 3) is about 530 mm across and preserves a plant portion that is almost 470 mm long. The preserved specimen constitutes a divaricately branched axis (Figure 3A); the branching appears acute-angled but closer examination reveals the two lateral branches being twisted, probably during the embedding process. Both the primary axis and the lateral branches are 15–18 mm wide and the only lateral axis entirely preserved from a branch axil to the next, where the flower bud terminated linear growth for the season (the presumed annual growth increment), reaches ~190 mm in length (Figure 3A, between arrowheads). Both axes are entirely covered with persistent, elongate to almost rectangular leaf bases or scars of shed leaves in their distal three-fourths (Figures 3A, 5D). The outline of the scars reflects the shape of the spatulate proximal end of the petioles of the leaves (Figures 5E, 6D). The scars are spirally arranged along the axis and marked with longitudinal striae—remnants of the striae of the decurrent leaf bases or spatulate petioles of the leaves. The proximal portions of the axes are marked by prominent longitudinal striae. The right lateral branch carries six or seven petiolate leaves on a 15-mm-wide main axis in a spiral phyllotaxis (Figure 3A, C), while from the other lateral branch only the proximal portion is preserved. No evidence of possibly unpreserved, removed or lacking leaves is found at the centre of the leaf whorl. The leaves are attached at very acute angles of 15°–30°. Leaves are bent over slightly apically. The visible portions of the incomplete leaves are up to 210 mm long and regularly segmented. 33–37 pairs of elongate, parallel-sided leaflets are attached to the upper (adaxial) side of the ventrally keeled and dorsally grooved, longitudinally striate and robust rachis. No leaf apices are preserved.
In analogy to closely related bennettitalean plants such as Kimuriella densifolia, Wielandiella angustifolia and Wielandiella villosa (Pott, 2014; Pott et al., 2015; Pott and Takimoto, 2022), the remnant of a developing or mature seed cone would be to expect in the preserved branch axil (Figure 3A, lower arrowhead). Interpreting a bulbous sedimentary structure preserved at the very appropriate position as such seems too speculative. In addition, if it were a mature seed cone, it could also have been removed prior to embedding by natural shedding or animal feeding. A respective abscission scar, however, is difficult to discern.
When Ohaniella ptilofolia gen. et sp. nov. is compared with the closely related bennettitalean plants mentioned above, the bulbous structure visible in the centre of the leaf whorl between the petioles of the leaves at the apical end of the right lateral branch (Figure 3A, upper arrowhead) can be clearly identified as a reproductive structure. The structure is less well preserved than in the other species mentioned above, and is probably incomplete, about 24 mm long and 14 mm wide, but it displays the diagnostic rhombic to hexagonal shields characteristic of the surfaces of bennettitalean gynoecia and seed cones (Figure 3B, D–F; see, e.g. Pott et al., 2010; Pott, 2014; Pott and McLoughlin, 2014; Pott and Takimoto, 2022). At two places, small predominantly hexagonal shields about 700 μm to 1,000 μm in diameter are visible, displaying a prominent outer edge or rim and a similarly prominent central structure, representing the interseminal scale heads with their heavier cutinised rim and central portion (see Pott, 2014, figs. 12, 13; Pott, 2016, fig. 10). The preservation does not allow for the identification of developed micropyles between the interseminal scale heads. Consequently, it is ambiguous whether the structure represents a flower at the stage of anthesis or a mature seed cone. If the hypothesis of Pott and McLoughlin (2014, text-fig. 8) is strictly applied, one would expect a flower in the stage of anthesis here. However, no bracts covering portions of the gynoecium are visible but may be hidden below the preserved portions of the leaves.
Remarks.—The first photographic documentation of the holotype specimen was made in August 2012 by HT (Figure 3D). A further photographic analysis of the specimen was carried out in October 2015 during the stay of CP in Japan (Figure 3E), but only during the detailed examination of the photographs for this study in November 2022 did CP succeed in recognising the hexagonal shields, the most crucial parts of this fossil. However, a reanalysis of the specimen by HT in 2024, with the emphasis to take new and more detailed photographs of the crucial areas of the fossil for better documentation of the heaxgonal shields, revealed that the formation of marcasite had altered the specimen (Figure 3F) and unfortunately affected (viz. destroyed) the above-mentioned crucial regions of the specimen (compare the photographs in Figure 3D–F).
Epitype.—The second slab yielding an articulated fossil (MM-000941, epitype; Figure 4) is about 130×170 mm in size and preserves a plant portion that is almost 135 mm long, with seven or eight petioles of leaves, of which two yield portions of the segmented leaf lamina. In all aspects, the preserved fossil plant has the same features, dimensions and characteristics as the one preserved on the holotype specimen. Five further leaves are visible on the slab, two of which may be attached to the articulated specimen based on their position, but these are covered by sediment, so this association is uncertain. A preparation of the slab may reveal more details but would in turn destroy the surface layer of leaves.
FoliageIn total, 127 specimens with leaves were collected from the outcrop, of which a representative number was analysed to ensure the conspecificity with leaves of Ptilophyllum jurassicum described earlier by Kimura and Ohana (1988b, 1989) and Kimura et al. (1991). Most of the leaves are preserved as fragments only, reaching a length of up to 250 mm and a width of 85 mm in the widest leaf. Leaf shape is narrow and tapering, and petioles are about 35 mm long and 8 mm wide (Figures 3A, C; 4; 5A–C, E, F; 6).
The elongate-obovate leaves are identical to what was described as P. jurassicum by Kimura and Ohana (1988b, 1989) and Kimura et al. (1991). The leaves are petiolate. At their apices, the ~10 distal leaflets decrease rapidly in length giving the leaf apices an acute to lanceolate appearance (Figures 5C, 6A). The specimen under study here with most leaflets preserved yields 43 pairs of leaflets at a length of 245 mm but is incomplete (Figure 5F). The life length of a complete leaf may thus be estimated to >300 mm. The articulated leaflets are oppositely to suboppositely attached to the upper side of the rachis with their symmetrically contracted bases—both the basiscopic and the acroscopic base portion are straight or evenly rounded (Figures 5B, 6E). Lateral leaflets are long and narrow with an elongate-lanceolate, distally tapered outline, and acutely rounded apices (Figures 5A, B; 6E). The leaflets increase in length continuously during the proximal third of the leaf, are then for about the same portion of the leaf equally long and then decrease again continuously towards the apex (Figures 5A, C, E, F; 6A, B, E). The shape of the apical leaflet—if there is any—is unknown because no complete apex is preserved in any of the leaves. The numerous delicate veins in all leaflets bifurcate near the base, then run parallel and end at the margin. They do not converge at the apical portion of the leaflets (Figure 5B). Vein density is given in the original description with c. 50 veins/cm in the middle of the leaflets, but a re-evaluation by us reveals that the density is 26–30 veins/cm only.
Longest leaflets in the leaves under study are commonly 19–32 mm long and up to 4–6 mm wide in their widest portion, while the original description of P. jurassicum states them being up to 30 mm long and up to 5 mm wide at the base. Incomplete leaves under study are up to 26 cm long including petioles and up to 6 cm wide, but most leaves stay slenderer (commonly around 3 cm wide). The original description states here assumed dimensions of more than 14 cm and 6 cm, respectively. The leaf rachis is up to 2 mm wide in the studied leaves and retains its width from the base of the leaf up to the apex. The rachis and petiole appear longitudinally striate on the adaxial side between the insertion areas of the leaflets (Figure 5E). The spatulate petiole is basally expanded, forming a decurrent base that is attached to the main axes of the plant (Figures 5E, 6D). Petioles can be rather long, reaching up to 6 cm in length (up to a fourth of the entire length of the leaves). Rachides are straight and appear very stiff; the leaves are commonly inserted at 15°–30° to the branches; the more proximal leaves might bend over to wider angles. Leaves were shed as a whole leaving scars on the branches that fit in size and outline the preserved petioles.
An extensive statement on some nomenclatural notes regarding the restoration of whole-plant bennettitaleans was provided by Pott and Takimoto (2022), to which we refer the willing reader.
In that paper, Pott and Takimoto (2022) described Kimuriella densifolia, a whole-plant bennettitalean based on excellently preserved articulate fossils from the same formation and outcrops. The plant is characterised by Zamites-type foliage and appears more robust or less delicate in all dimensions than Ohaniella ptilofolia gen. et sp. nov. The leaves are slenderer and commonly shorter in Ohaniella, while growth increments are three times longer in Ohaniella, but only one growth increment is preserved (see Figure 3A, between arrowheads). Despite a similar plant architecture of Ohaniella and Kimuriella, the erection of a new genus for whole-plant bennettitaleans is justified because the foliage of the two plants is placed in two different but sound genera (viz. Ptilophyllum and Zamites, respectively).
As mentioned already by Pott and Takimoto (2022) for Kimuriella, we are not aware of any other plant species or genus that could accommodate the plant described here as O. ptilofolia gen. et sp. nov., which encourages us to erect this new genus for divaricately branched bennettitalean plants in the Williamsoniceae family of the Bennettitales.
Notes on the foliageThe mentioned differences between Ptilophyllum oshikaense from the Oxfordian portion of the Oginohama Formation and the Oxfordian Moné Formation (Kimura and Ohana, 1989; Kimura et al., 1991) and Ptilophyllum jurassicum (Kimura and Ohana, 1988, p. 151) are deemed so marginal that they better range within the limits of intraspecific variation than discriminate between leaf taxa. Especially when comparing the specimens cited in the mentioned publications (Kimura and Ohana, 1988b, 1989; Kimura et al., 1991) and the line drawings based on those, it appears that the range of variation within the species is even larger than between the species. Therefore, we regard P. oshikaense and P. jurassicum conspecific, with the latter having nomenclatural priority.
One very similar species is Ptilophyllum nipponicum from the Pliensbachian Negoya Formation of the Kuruma Group (Kimura and Tsujii, 1982). These leaves are discriminated from P. jurassicum by a different venation with divergent veins “forking at all levels” in contrast to the almost parallel veins that bifurcate only once basally in P. jurassicum (Kimura and Tsujii, 1982, p. 270).
According to its original description, the detached ‘penultimate pinnae’ of Nipponoptilophyllum bipinnatum (Kimura and Tsujii, 1984; Kimura and Ohana, 1988b), also from the Oxfordian Tochikubo Formation, appear similar in many morphological features but are about 20–30% smaller in a few pinna dimensions compared to P. jurassicum.
However, N. bipinnatum is described as a bipinnate frond with Ptilophyllum-type leaves as first-order pinnae, but the restoration as bipinnate is based on a single, relatively poorly preserved specimen and is questionable in several aspects, with a single segmented ‘pinna’ attached to a ‘branch’ intersection. Convincing evidence as to whether the branching that is on the rock surface surrounded with white paint (probably to enhance the proposed rachial branching) is a true branching or an uncertainty could not be retrieved by studying the original specimen. For the following reasons, we think that the bipinnate nature of N. bipinnatum is not conclusive: (a) there are no leaflets on other adjacent lateral axes; (b) if the leaflets were attached to these lateral axes, they would overlap each other between pinnae; (c) the surface level yielding the foliage is slightly above of the surface level yielding the branches; (d) the bases of the petioles of all known P. jurassicum leaves with preserved petioles are expanded reflecting the afore-mentioned decurrent insertion of the leaves, but there is no such expansion at the insertion points on the secondary axes, or in turn, amongst the numerous fossils, no leaves with not expanded petioles were found. In addition, this latter feature is generally uncommon in bipinnate fronds of modern cycads or (tree) ferns.
Moreover, 49 specimens of detached leaves (‘penultimate pinnae’ in the sense of Kimura and Tsujii (1984)) may suggest single disarticulated segmented leaves instead for pinnae of bipinnate fronds, but it is uncertain whether the 41 specimens studied by Kimura and Ohana (1988b) besides the type specimens are those of Kimura and Tsujii (1984), or if there are additional (new) specimens among them. The bipinnate organisation would be very uncommon in bennettitaleans and has not yet been described from elsewhere as far as we know. However, Ohana et al. (1989) reported a truly bipinnate frond (Nipponoptilophyllum ryosekiense) from the Barremian (Lower Cretaceous) Monobe Formation that is assigned to a presumed bennettitalean genus, but ultimate proof in the form of cuticle to verify the bennettitalean nature was not reported as it probably is not available. In case the bipinnate nature of N. bipinnatum is regarded as uncertain, those ‘penultimate pinnae’ in the sense of Kimura and Tsujii (1984) and P. jurassicum might be conspecific as well.
Whether or not the tiny leaves assigned to Ptilophyllum sp. G, Ptilophyllum sp. H, and Ptilophyllum sp. I, by Kimura and Ohana (1998b) and Kimura et al. (1991) might be referred to P. jurassicum remains questionable, because detailed information on the fossils is lacking, and their very small size is not necessarily a reason for exclusion.
Specimens assigned to Nilssonia pterophylloides by Yokoyama (1895) and later to Ptilophyllum pecten by Ôishi (1940) appear similar in gross morphology, but further information is unavailable. Moreover, these fossils derive from clearly Lower Cretaceous (Berriasian–Albian) strata (Kimura and Kansha, 1978).
Restoration and habitus of Ohaniella ptilofolia gen. et sp. nov.Like the previously published Kimuriella and Wielandiella species, we interpret Ohaniella ptilofolia gen. et sp. nov. as of similar plant architecture, thus having been low-growing shrub-like plants probably up to 1–2 m tall. Thereby, the divaricately branched axes (see Pott and McLoughlin, 2014; Pott and Takimoto, 2022) probably formed tangled shrub thickets with interlaced axes, covering brackish to tidal mudflat areas or delta settings that were regularly flooded such as in mangroves or tideland habitats.
As in other related bennettitalean plants (see Pott and McLoughlin, 2014), Ohaniella plants are also interpreted as divaricately branched shrubs, in which the divaricate axes were producing flowers that terminated growth at the main axis inducing lateral branching. The periodically produced (probably seasonally or annually) new branch increments themselves produced terminal flowers during the next reproduction cycle to again induce lateral branching, a process that continued periodically (viz. season by season; see Pott and McLoughlin, 2014) to form such a plant habitus. Reasons, benefits and downsides of such plant forms have been evaluated and discussed in detail by Pott and McLoughlin (2014), but adopting this type of plant architecture in O. ptilofolia gen. et sp. nov. is warranted by the examination of the fossils at hand.
The Ptilophyllum-type foliage of O. ptilofolia gen. et sp. nov. appears less stiff than the Zamites-type foliage of Kimuriella densifolia, whose leaves were likely as robust as in many modern cycads, consequently providing a certain amount of armour to protect the flower buds, anthetic flowers or mature seed cones. Still, the leaves of O. ptilofolia gen. et sp. nov. may also have formed some protection for the developing flower buds or anthetic flowers.
Similar to K. densifolia, it remains unclear for the time being if O. ptilofolia gen. et sp. nov. constitutes monoecious or dioecious plants. The fossils at hand only yield axes with ovuliferous flowers or seed cones terminating the axes. The microsporangiate flowers of O. ptilofolia gen. et sp. nov. are unknown so far; two specimens from the same local outcrop and horizon each yield a fossil besides a leaf of Ptilophyllum jurassicum that can be identified as a disarticulated microsporangiate organ (Figure 6B, C). For Kimuriella, it has been hypothesised that microsporangiate flowers appear to have been targets of scheduled shedding, most likely after having released their pollen load, and then commonly preserved upside-down (Figure 6B, C; Pott and Takimoto, 2022). As the fossils are indicative of no or only very little transportation (Pott and Takimoto, 2022), it can be assumed that the microsporangiate flowers at hand were shed from the same population of plants. There is no indication whether the plants were dioecious or monoecious, but the shedding of microsporangiate flowers prior to anthesis of the ovuliferous flowers in the same population of plants can be regarded as a mechanism to avoid self-pollination. However, this mechanism can develop both in monoecious and dioecious plants. Obviously, the flowers where not hermaphroditic, which is known to have occurred amongst Jurassic bennettitaleans, but this feature was documented for only one species/genus so far (viz. Williamsoniella; Thomas, 1915; Zimmermann, 1933; Harris, 1969; Pott, 2014).
As O. ptilofolia gen. et sp. nov. is interpreted to be very similar to K. densifolia in growth habit and plant architecture, a comparison with other Jurassic whole-plant bennettitaleans (amongst which are some species carrying Ptilophyllum-type foliage) is unessential here as we would only repeat what was discussed in the previous paper (Pott and Takimoto, 2022).
Ecological aspectsBecause the Ohaniella fossils are found in the same major outcrop as the Kimuriella fossils, ecological aspects might not be discussed here further, as a detailed interpretation of the facies, habitat and environment reflected in the Tochikubo Formation has already been provided by Pott and Takimoto (2022). Therefore, only a short summary is compiled here.
The facies of the portion of the Tochikubo Formation containing the plant beds is considered to have been deposited in a non-marine environment (Takizawa, 1985). Based on the potential near-shore position with adjacent lake deposits (Masatani and Tamura, 1959; Mori, 1963; Takizawa, 1985), the plant-bearing beds in the uppermost portion of the Tochikubo Formation might be interpreted to have been deposited in meandering river floodplains with ephemeral lakes or cut-off meanders within deltaic or coastal plain settings. The sedimentary environment of this part of the Tochikubo Formation is interpreted to probably reflect a transitional zone in a coastal environment. The presence of thin coal seams indicates that the environment in the area was stable for longer periods of time enabling the accumulation of large amounts of plant material in low-energy mire settings.
The bennettitaleans from the Tochikubo Formation thus might be interpreted to have been invasive specialist colonisers of the nutrient-poor surfaces of rheo- or ombrotrophic, long-lived, peat-forming mires. Williamsoniaceous bennettitaleans thriving in such exposed and disturbed environments of wide floodplains and levees within deltaic or coastal plain settings and along mire edges with rapidly changing conditions might have evolved strategies to adapt to such prevailing unfavourable environmental conditions. This includes a divaricate growth form and a xeromorphic nature of stiff, leathery leaves (Pott and McLoughlin, 2014). Plants in such environments were subjected to a range of stress-inducing abiotic factors, among these sustained winds, considerable (soil, water and air) salinity and seasonal periods of drought or frost.
Environments in delta settings or mudflat areas with regularly or periodically flooded ephemeral isles or sand bars provide a range of slightly different habitats. Such as in saltmarshes influenced by tides or modern mangroves, only small differences in ground elevation can cause major differences in vegetation cover (see, e.g. Harris, 1932, 1952; Pott, 2006, 2014; Pott and McLoughlin, 2014; Pott et al., 2015, 2016), although no salinity information is available from the Tochikubo Formation.
Ohaniella plants might be interpreted somewhat different from Kimuriella in having more delicate and less stiff foliage and longer growth increments, which may point to slightly different environmental requirements and maybe slightly different habitat preferences. And indeed, the Ohaniella fossils were found at the same major outcrop as Kimuriella but very locally c. 20 m below and 2 m above the horizon of the Kimuriella specimens and about 60 m to the west and 200 m to the east from it. As bennettitaleans have repeatedly been interpreted to have formed rather monotypic shrub thickets (e.g. Pott, 2014; Pott and McLoughlin, 2014; Pott and Takimoto, 2022), Ohaniella may have grown in a slightly different (e.g. less windy) habitat than Kimuriella, which may have been differently influenced by sun radiation, salinity, moisture, soil composition, (ground) water level, sustained winds, to name a few.
Accompanying floraBesides a considerable number (N=~14) of different bennettitalean species, the accompanying flora reported from the Tochikubo Formation constitutes lycophytes (Lycopodites), sphenophytes (Neocalamites, Equisetites), some delicate ferns such as Adiantopteris, Gleichenites, Onchyopsis, Acrostichopteris, Matonidium, Eboracia, Sphenopteris and Cladophlebis, a number of cycadophytes (including Nilssoniales) other than bennettitaleans, such as Pseudoctenis, Encephalartites, Cycadites, and several Nilssonia and Nilssoniocladus species, and a few fossils assignable to the coniferophytes Elatocladus, Pagiophyllum and Parasequoia (see, e.g. Kimura and Tsujii, 1984; Kimura and Ohana, 1988a, b; Takimoto et al., 1997, 2008; Takimoto and Ohana, 2016; Takimoto, 2018; Pott and Takimoto, 2022).
As this paper is dedicated predominantly to the description and evaluation of Ohaniella ptilofolia gen. et sp. nov., an evaluation of further bennettitaleans and other cycadophytes described and to be described from the Tochikubo Formation, together with a still due comparison of the Tochikubo flora with other Jurassic floras of Japan, will be conducted in separate papers (see Pott and Takimoto, 2022; Pott and Takimoto, in preparation).
Two slabs collected from the Oxfordian Tochikubo Formation in northeast Japan with bennettitalean articulate fossils (branched axes with attached leaves and ovuliferous flowers) preserved were examined together with >50 additional specimens yielding disarticulated leaves and possible microsporangiate organs. Based on the fossils at hand, a whole-plant bennettitalean was restored. We are not aware of any other plant species or genus that could accommodate the plant described here as Ohaniella ptilofolia gen. et sp. nov., consequently necessitating the erection of a new genus for divaricately branched bennettitalean plants in the Williamsoniceae family of the Bennettitales.
Ohaniella ptilofolia gen. et sp. nov. was a low-growing shrub-like plant that probably reached 1–2 m in height. Ohaniella ptilofolia gen. et sp. nov. is very closely related to the previously published Kimuriella densifolia and is interpreted in a similar way concerning growth habit, plant architecture and lifestyle or life strategy. The divaricately branched axes formed tangled shrub thickets. The axes produced flowers that terminated growth of the main axis presumably inducing lateral branching. Ohaniella ptilofolia gen. et sp. nov. produced only one ovuliferous flower per active (lateral) branch at a time or season. Whether O. ptilofolia gen. et sp. nov. constitutes monoecious or dioecious plants is difficult to ascertain because microsporangiate flowers are known only as disarticulated organs that appear to have been shed after having released their pollen load.
Interpretation of the sedimentary environment, taphonomic aspects and the ecological demands of the plants is inferred from the restored habitus of O. ptilofolia gen. et sp. nov. as similar to that of K. densifolia. Due to a smaller plant size, probably less rigid and more delicate leaves, much longer growth increments, and the context of discovery, O. ptilofolia gen. et sp. nov. is interpreted to have grown in a slightly different (maybe less windy) micro-habitat but within the same delta setting constituting ephemeral isles or sand bars that were periodically flooded. When comparing with other williamsoniaceous bennettitaleans exhibiting a divaricate growth form, it is reasonable to assume that O. ptilofolia gen. et sp. nov. also extended its habitat into brackish to tidal mudflat areas or tidelands similar to those found in modern mangroves or saltmarshes.
The authors thank the NEXCO EAST Tohoku regional office and construction company for their permission to access the fossil site and collect fossils. We are very thankful to Muneo Taira, whose sharp eyes discovered the two specimens with several leaves attached to the top of prominent axes, which formed the basis of this study. Muneo Taira, Yasuo Yamaki, Yoshimi Ara and members of the Research Association of the Somanakamura Group kindly provided plant fossils they collected for this study. Atsushi Yabe and Tamiko Ohana of the National Museum of Nature and Science (NSM), Tsukuba, Ibaraki, Japan, kindly provided access to the plant fossils of the Tochikubo Formation, and are thanked for all support provided during CP’s stay in Japan, as well as for taking and sending photographs of specimens later. Taichi Kato, curator of palaeontology at the Ibaraki Nature Museum (INM), Ibaraki, Japan, granted access to the fossils and permission to sample some of the fossils for maceration of cuticles. The cooperation of Fumihiko Futakami and Kunihiro Nakagawa to finally store the fossil specimens in the Minamisoma City Museum (MM), Minamisoma, Fukushima, Japan is greatly acknowledged. Hans Kerp of the Palaeobotany Research Group of the Institute of Geology and Palaeontology, University Münster, Germany is thanked for granting access to laboratories and microscopes for performing the cuticular analysis. Travelling to Japan for studying the fossils at NSM and INM was accomplished during periods when CP received funding through the Swedish Research Council (VR, Stockholm) under grant number 2012-4375. The authors thank Mihai E. Popa (Bucharest) and Toshihiro Yamada (Sapporo) for their constructive reviews of the manuscript.
CP designed the research. CP and HT provided documentation of fossil material. HT provided the fossil material. CP analysed the fossil material. CP and HT contributed to writing the paper. The authors equally contributed to this work, both authors edited the final version of the manuscript.
