Abstract
Two new fossil taxa referable to the basal eudicot grade are described from the Kamikitaba locality (ca. 89 MYBP, early Coniacian: Late Cretaceous) of the Futaba Group in Japan. These charcoalified mesofossils exhibit well-preserved three-dimensional structure and were analyzed using synchrotron-radiation X-ray microtomography to document their composition and internal structure. Cathiaria japonica sp. nov. is represented by infructescence segments that consist of an axis bearing three to four fruits. The capsular fruits are sessile and dehiscent and consist of a gynoecium subtended by a bract. No perianth parts are present. The gynoecium is monocarpellate containing two pendulous seeds. The carpel is ascidiate in the lower half and conduplicate in the upper part, and the style is deflected abaxially with a large, obliquely decurrent stigma. Pollen grains are tricolpate with a reticulate exine. The morphological features of Cathiaria are consistent with an assignment to the Buxaceae s. l. (including Didymelaceae). Archaestella verticillatus gen. et sp. nov. is represented by flowers that are small, actinomorphic, pedicellate, bisexual, semi-inferior, and multicarpellate. The floral receptacle is cup shaped with a perigynous perianth consisting of several tepals inserted around the rim. The gynoecium consists of a whorl of ten conduplicate, laterally connate but distally distinct carpels with a conspicuous dorsal bulge, including a central cavity. The styles are short, becoming recurved with a ventrally decurrent stigma. Seeds are ca. 10 per carpel, marginal, pendulous from the broad, oblique summit of the locule. Pollen grains are tricolpate with a reticulate exine pattern, suggesting a relationship to eudicots. The morphological features of Archaestella indicate a possible relationship to Trochodendraceae in the basal grade of eudicots. The fossil currently provides the earliest record of the family and documents the presence of Trochodendraceae in eastern Eurasia during the middle part of the Late Cretaceous.
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Introduction
Paleobotanical studies of Cretaceous mesofossils over the last 25 years have demonstrated that the major lineages of early angiosperms were already differentiated by the early Late Cretaceous (Crane et al. 1994, 2004; Friis et al. 1994, 2006, 2011). In recent years the study of mesofossils with scanning electron microscopy (SEM) has been augmented by the application of synchrotron-radiation X-ray microtomography (SRXTM) to provide a more complete understanding of the complex internal structure of the Cretaceous fossils without the need to dissect or section the fossil specimens (e.g., Friis et al. 2007, 2009; Herendeen et al. 2016; Schönenberger et al. 2012; Takahashi et al. 2008a, b, 2014; von Balthazar et al. 2007).
The Kamikitaba flora (Coniacian; Late Cretaceous) is a unique assemblage from northeastern Japan. The mesofossil assemblage was isolated from a poorly sorted carbonaceous, black, sandy siltstone from the lower sediments of the Asamigawa Member of the Ashizawa Formation in the Futaba Group that extends from Iwaki city to Hirono-machi in Fukushima Prefecture. The mesofossils comprising the Kamikitaba assemblage are small, three-dimensional, and charcoalified or mummified/lignitized (mesofossils), including well-preserved angiosperm flowers, fruits, seeds, leaf fragments and wood, as well as shoots, leaves, pollen cones, cone scales and seeds of conifers (Takahashi et al. 1999a). Some of the angiosperm mesofossils have been described as Esgueiria (Combretaceae; Takahashi et al. 1999b), Hironoia (Cornaceae; Takahashi et al. 2002), Lauranthus, Microlaurus (Lauraceae; Takahashi et al. 2001, 2014), Symphaenale (Nymphaeales; Takahashi et al. 2007), Archaefagacea (Fagales; Takahashi et al. 2008a), and Futabanthus (Annonaceae; Takahashi et al. 2008b).
In this paper, we describe two new fossil taxa that are referable to the early-branching lineages of the large eudicot clade. The eudicot clade consists of the core eudicots plus several additional lineages that collectively form a paraphyletic basal grade. These early branching eudicot groups include the Ranunculales (Berberidaceae, Circaesteraceae, Eupteleaceae, Lardizabalaceae, Menispermaceae, Papaveraceae, Ranunculaceae), Sabiaceae, Proteales (Nelumbonaceae, Platanaceae, Proteaceae), Trochodendrales (Trochodendraceae) and Buxales (Buxaceae s. l.) (APG IV 2016). One of the new fossil taxa, Cathiaria japonica is described as a new species. We provide new morphological details for Cathiaria Golovneva et Oskolski based on well-preserved charcoalified fossil fruits. Based on the new information, we suggest a close relationship to the Buxaceae s. l. (including Didymelaceae). The second new fossil taxon, Archaestella verticillatus, is described as a new genus and species that is referable to the Trochodendraceae. The fossil flower and fruits of Archaestella extend the fossil record of Trochodendraceae into significantly earlier Cretaceous rocks than those from which it has been recorded previously. This new discovery helps to bring the fossil history of the Trochodendraceae into line with the long fossil history of other basal eudicot lineages. The description of these mesofossils from the Late Cretaceous of eastern Eurasia documents additional diversity in floral morphology among the Cretaceous angiosperms and represent important additions to our understanding of the history of the early lineages within the eudicots.
Materials and methods
Plant mesofossils were isolated from bulk matrix samples of the Kamikitaba locality. The fossil bearing sediments are a poorly sorted, carbonaceous, sandy siltstone. Samples were collected during 1998–2008 from the Asamigawa Member of Ashizawa Formation (Futaba Group), exposed along a tributary of the Kitaba River in Kamikitaba, Hirono-machi, Fukushima Prefecture, northeastern Japan. Sample F16 has yielded diverse mesofossils (Kamikitaba mesofossil flora) that include a range of pteridophytes, conifers, and angiosperms (Takahashi et al. 1999b). Several of these mesofossils have now been studied in detail, along with material recovered from other levels in the Futaba Group (Takahashi et al. 1999a, b, 2002, 2007, 2008a, b). The Asamigawa Member is the lowermost member of the Ashizawa Formation, which itself is the lowermost formation of the Futaba Group. The plant-bearing sediments are probably of lower Coniacian age (ca. 89Myr BP; Cohen et al. 2016) based on ammonites and inoceramids from the middle of the Ashizawa Formation (see Takahashi et al. 1999b for details).
Material collected in the field was dried, disaggregated in water, and sieved through a 125-µm mesh screen to separate the organic debris from the sediment. Residual mineral matter remaining attached to the carbonaceous material was removed by bulk cleaning in hydrofluoric and hydrochloric acids. Samples were then thoroughly rinsed in water and air dried. The mesofossil specimens were examined with a Hitachi S-800 field emission SEM.
The specimens were also imaged with microtomography using the X-ray microscope at the 2-BM-B beamline of Advanced Photon Source (APS) at the US Department of Energy’s Argonne National Laboratory. The measurements were done with X-rays of 15 keV. The exposure time was 600 ms, and 1,800 projections were acquired equi-angularly over 180°. The specimens’ 3-dimensional structures were reconstructed from the projection images with gridrec algorithm (Dowd et al. 1999). Isotropic voxel is 0.74 µm along each dimension. The specimens illustrated in this article are deposited in the paleobotanical collections of the Field Museum, Chicago.
Systematic description
Angiosperms
Eudicots
Order: Buxales
Family: Buxaceae s. l. (including Didymelaceae)
Genus: Cathiaria Golovneva et Oskolski, here emended
Type: Cathiaria zhilinii Golovneva et Oskolski
Emended generic diagnosis: Infructescence compound, consisting of two orders of axes, bearing sessile fruits on the adaxial side. Pistillate flowers alternately or spirally arranged on the spike-like inflorescence. Flower consisting of a single unilocular pistil with distinct stigma and a scale-like bract at the base. No evidence of scars for perianth or stamens. Fruit wall composed of sclerenchyma. Seed coat consisting of lignified hard cells; surface verrucate. Pollen grains tricolpate with reticulate exine.
Cathiaria japonica Takahashi, Herendeen, et Xiao sp. nov. (Figs. 1, 2).
Holotype: Field Museum PP56480. Figures 1a–b, g–i, 2a–k
Paratypes: Field Museum PP56481 (Fig. 1c), PP56482 (Fig. 1d), PP56483 (Fig. 1e), PP56484 (Fig. 1f),
Locality and horizon: The specimens are from the Asamigawa Member of the Ashizawa Formation, Futaba Group. Samples were collected at the Kamikitaba locality, Hirono-machi, Fukushima Prefecture, northeastern Japan (37°12′N, 140°57′E).
Age: early Coniacian (Late Cretaceous)
Derivation of specific epithet: The specific epithet, “japonica”, refers to the source country for these fossils.
Specific diagnosis: Infructescence bearing sessile fruits on the adaxial side (Figs. 1a, c–f, 2a–b). Pistillate flower lacking perianth and is subtended by a scale-like bract (Figs. 1b, 2a–c). No evidence of scars for perianth or stamens (Figs. 1b–c, 2a–c). Gynoecium composed of one carpel with a short style and sessile stigma (Figs. 1b, g, 2c–g). Stigma obliquely decurrent, extending to form a flattened, papillate surface (Fig. 1g). Fruit ellipsoid with a longitudinal suture on the distal (abaxial) side; two seeds are borne in the single locule (Figs. 1b, 2d–g). Fruit wall composed of sclerenchyma. Seed coat consisting of lignified hard cells and having a verrucate surface (Fig. 2h–k). Pollen grains tricolpate with reticulate exine (Fig. 1h –i).
Dimensions: Length of fragmentary axis 2.5 mm, diameter of axis 0.30–0.43 mm, length of scale-like bract 0.25 mm, width 0.47 mm, length of fruit 0.65–1.0 mm, diameter of fruit, 0.44–0.57 mm, length of stigma, 0.30–0.35 mm, width of stigma 0.20–0.25 mm, length of seed 0.55 mm, width of seed 0.26 mm. Polar axis of pollen grains 10 μm, equatorial diameter of pollen grains, 8 μm, diameter of lumina 0.5 μm, width of muri, 0.3–0.4 μm.
Description and remarks: The fossil specimens are found as fruits borne on a fragmentary spike (Figs. 1a–f, 2a–b). Fruits are alternately or spirally arranged on the short segments of the infructescence axis and are subtended by a persistent floral bract (Figs. 1a–f, 2a–b). The length of the complete infructescence is not clear. The floral bract is long and distinctly acuminate with a narrow apex and irregularly serrate margins and it is almost completely fused basally to enclose the ovary (Figs. 1a–b, 2a–c). There is no evidence of an androecium, and no attached remains of perianth have been observed. The gynoecium is monocarpellate with apical placentation, bearing two pendulous seeds in the single locule (Fig. 2d–g). The carpel is ascidiate in the lower half, conduplicate above, distally deflected abaxially with a dorsiventral suture and a large, obliquely decurrent stigma (Figs. 1b, g, 2c). The fruit is ellipsoid with a longitudinal suture on the distal (abaxial) side. In transverse section the fruits are semicircular in outline, slightly flattened laterally, with a straight ventral (adaxial) margin; the dorsal (abaxial) margin is strongly convex (Figs. 1a–c, 2a–c). The fruit is dehiscent, having a suture at the dorsal margin. The fruit surface consists of elongated epidermal cells (Fig. 1b). The base of the fruit is usually rounded, and the apex is slightly pointed and extends adaxially to form a lip-like stigma (Figs. 1a, b, 2a–c). The papillate stigma is almost sessile (Fig. 1b, g). The seed surface is striate (Fig. 2h–k). Pollen grains are small, 10 μm in polar axis, 8 μm in equatorial axis, and tricolpate with a reticulate exine sculpture pattern (Fig. 1h, i). Colpus is elongated toward the poles of grain (Fig. 1i).
Order: Trochodendrales
Family: Trochodendraceae
Genus: Archaestella Takahashi, Herendeen, et Xiao gen. nov. (Figs. 3, 4, 5, 6, 7)
Type species: Archaestella verticillatus Takahashi, Herendeen, et Xiao sp. nov.
Generic diagnosis: Flower actinomorphic, bisexual, semi-inferior, and multi-carpellate. Floral receptacle concave, with a perigynous perianth consisting of several tepals, borne around the rim. Androecium consisting of ca. 120 stamens with clear differentiation into anther and filament. Gynoecium consisting of a whorl of 10 conduplicate, laterally connate but distally distinct carpels with a conspicuous dorsal bulge, including a small central cavity. Styles recurved with papillate and ventrally decurrent stigma. Ovules ca. 10 per carpel, marginal, pendulous from the broad, concrescent oblique summit of the locule. Seeds with chalazal, apical and lateral wing-like extensions. Pollen grains, tricolpate, with reticulate exine pattern.
Derivation of generic name: Archaestella refers to the meanings of “ancient” and “star”.
Archaestella verticillatus Takahashi, Herendeen, et Xiao sp. nov. (Figs. 3, 4, 5, 6, 7).
Holotype: Field Museum PP56485. Figures 3, 4 and 5.
Paratypes: Field Museum PP56486 (Figs. 6, 7a–c), PP56487 (Fig. 7d–f).
Locality and horizon: The specimens are from the Asamigawa Member of the Ashizawa Formation, Futaba Group. Samples were collected at the Kamikitaba locality, Hirono-machi, Fukushima Prefecture, northeastern Japan (37°12′N, 140°57′E).
Age: early Coniacian (Late Cretaceous)
Derivation of specific epithet: The specific epithet, “verticillatus”, is from the meaning of “whorl”.
Specific diagnosis: Flower pedicellate, actinomorphic, bisexual, half-inferior, and multi-carpellate (Figs. 3a–g, 4a–f, 5a–h, 6a–b, f). Floral receptacle concave with a perigynous perianth consisting of several tepals, borne in two cycles, around the rim (Figs. 4c–f, 5a–h, 6f, 7a). Androecium consisting of ca. 120 stamens with clear differentiation into anther and filament (Figs. 3a–g, 4b–f, 5a, c, e, g, 7b). Gynoecium is syncarpous and consisting of a whorl of 10 conduplicate carpels that are laterally connate basally but distinct distally, with a conspicuous dorsal bulge, including a central cavity (Figs. 3c–g, 4a, c–f, 5a–h, 6a–e). Styles recurved with a papillate and ventrally decurrent stigma (Figs. 3f, g, 4a, c, d, 5a, c). Ovules ca. 10 per carpel, marginal, pendulous from the broad, concrescent oblique summit of the locule (Fig. 7d–f). Seeds with chalazal, apical and lateral wing-like extensions (Fig. 7d–f). Pollen grains, tricolpate, with reticulate exine pattern (Fig. 7c).
Dimensions: Pedicel of flower, 0.1 mm in diameter, developed to 1.0 mm in diameter in fruit. Flower, 1.2 mm in diameter and 1.2 mm high, developed to 4.2 mm in diameter and 4.0 mm high in fruit. Tepals ca. 0.8 mm wide, length unknown (incomplete). Stamens, 0.2–0.3 mm in length; anthers 0.1 mm in length; filaments, 0.1–0.2 mm. Pollen grains 9.3 μm in equatorial diameter, no data on polar axis. Gynoecium, 0.8 mm in diameter, 0.6 mm high, developed to 3.9 mm in diameter, 1.7 mm high in fruit. Stigma 0.1 mm wide, 0.1 mm high.
Description and remarks: The fossil material consists of three charcoalified specimens (Figs. 3, 4, 5, 6, 7). One of them is a flower in the stage of anthesis with perianth, androecium and gynoecium preserved in a good condition (Figs. 3, 4, 5). The other specimens are young fruits after anthesis (Figs. 6, 7).
Flower The flowers are pedicellate, actinomorphic, bisexual with a broad receptacle and a semi-inferior ovary (Figs. 3, 4, 5, 6, 7). Whorls of perianth parts and stamens are borne along the rim of the receptacle and surround a ring of carpels (Figs. 3a–g, 4c–f). The pedicel is slender at the stage of flower anthesis and becomes stout at fruiting stage (Figs. 1c, e, 6f).
Perianth Elongated scars along the outer margin of the receptacle indicate that the flowers had a perianth of stout and free parts; each perianth part with a thick base. The number and shape of perianth parts are unknown (Figs. 3a–g, 4d–f).
Androecium Numerous, closely spaced stamens are preserved inside the perianth, showing that the androecium is composed of approximately 120 free stamens (Figs. 3a–g, 4b–f, 5a–h). Filaments of outer stamens are long and curve centripetally into the center of flower (Figs. 3a–g, 4b–f). Anthers are basifixed, tetrasporangiate with an acute apex (Figs. 3a, b, f, g, 4b). The dehiscence type is not clear. Pollen grains are tricolpate with fine reticulate exine (Fig. 7c).
Gynoecium The gynoecium is radially symmetrical and consists of one whorl of approximately 10 carpels that form a shallow cavity in the center of the flower (Figs. 3f, g, 4c–f, 6a–f). The carpels are falcate in lateral view and semicircular in transverse view, borne on a short stipe (Figs. 4c, e, 5a–h, 6a, c–e). The ventral margin of the carpel is more or less concave and leaves a small central cavity (Figs. 6c, 7e). The dorsal margin is convex tapering toward the center of flower axis (Figs. 4c–f, 5a–h). The exposed margins of the carpels are free, but it is unclear whether the carpels are completely free (Figs. 4c–f, 5a–h). The styles are short, becoming recurved and ventrally decurrent with a U-shaped stigma (Figs. 3a, f, g, 4a).
Fruits Fruits are small follicles dehiscent along the adaxial margin (Fig. 5a–f). The stigma is not present at the stage of fruit (Fig. 5a–e).
Seed Seeds are small, spindle-shaped, with chalazal slender pointed extension (Fig. 7d–f).
Discussion
Cathiaria: structure
The genus Cathiaria Golovneva and Oskolski was established based on three-dimensionally preserved mesofossils of compound infructescences consisting of two orders of axes bearing sessile fruits from the Novosozyrevsky Formation (Cenomanian—early Turonian) in northern Kazakhstan and Siberia. Golovneva and Oskolski (2007) described two species, C. zhilinii and C. tyensis, which differ in the number of fruits on the lateral axes and in their arrangement. The gynoecium was interpreted to be unilocular bearing a single sub-basal or basal seed. However, the specified seed number should be viewed as uncertain because the interpretation was based on only one side of a fractured specimen. The fruits were described as being subtended by remnants of a bract or perianth at the base and they found no evidence of an androecium. According to Golovneva and Oskolski (2007), the infructescences consist of a main axis and alternate or sub-opposite lateral axes. The main axis is straight and irregularly finely ribbed. The lateral axes in immature condition are short, flattened and bear sessile fruits on the adaxial side; in maturity lateral axes are elongated, more or less cylindrical, and straight or curved. The type species, Cathiaria zhilinii, is characterized by lateral axes of mature infructescences that bear 5–12 sessile fruits, on the adaxial and lateral sides of the axis. There are no fruits on the abaxial surface.
The mesofossil specimens from the Kamikitaba locality share the same diagnostic features as seen in Cathiaria zhilinii and C. tyensis, but the excellent preservation of the Japanese material, and visualization using SRXTM, allows for the clarification of several important morphological details. The specimens from the Kamikitaba assemblage are recovered as fragments of axes bearing three or four fruits, which are interpreted to be the lateral axes of Cathiaria. Although the main axis has not been recovered from the Kamikitaba assemblage, most of features of the specimens from Kamikitaba agree with those of Cathiaria zhilinii from Kazakhstan, except for the small size of fruits, stout style and the number of seeds in the fruit. The flower consists of a single unilocular pistil, subtended by a scale-like bract. The style is extremely short and the stigma appears to be sessile. SRXTM does not indicate any perianth scars to be present, thus we conclude that the flower lacks perianth. Although the subtending scale-like structure was interpreted as either a bract or a reduced perianth by Golovneva and Oskloski (2007), SRXTM shows that each fruit is subtended by a single abaxial structure and therefore we interpret it as a persistent bract. The present study using SRXTM shows that Cathiaria is a unisexual female infructescence. No evidence of filaments or stamen scars was observed and we conclude that the flowers were unisexual. No staminate inflorescence specimens have not been recovered. It is unknown whether Cathiaria was monoecious or dioecious.
The fruit has a dorsiventral suture on the distal (abaxial) side. The suture is also observed in the specimens from Kazakhstan (Golovneva and Oskolski 2007, Pl. 3 Figs. 3, 4; Pl. 6, Fig. 2). Whereas Golovneva and Oskolski (2007) found evidence for only a single seed attached sub-basally or basally within a fruit based on SEM observations of a longitudinally fractured fruit, SRXTM of whole fruits demonstrates that the monocarpellate fruit includes two pendulous seeds from an apical placenta in a single locule (Fig. 2d–g). Determining the number of seeds and their attachment might not be so easy to confirm by SEM. The single seed borne in half of a longitudinally fractured fruit (Golovneva and Oskolski 2007, Pl. 4, Fig. 1) would imply the possible presence of two seeds in complete fruits of Cathiaria from Kazakhstan. However, it is still uncertain whether the number of seeds differs between the specimens of Cathiaria from Japan and Kazakhstan. The number of seeds and placentation in a fruit of Cathiaria from Kazakhstan would need to be examined in detail. Given these differences, the specimens from the Kamikitaba locality are described as a new species, Cathiaria japonica.
Cathiaria: systematic relationships
Golovneva and Oskolski (2007) evaluated possible systematic relationships of Cathiaria based on their structural interpretation: unisexual flowers, single unilocular pistil, reduced perianth, nut-like indehiscent one-seeded fruits, and compound infructescences with dorsiventral arrangement of fruits on flattened lateral axes. Golovneva and Oskolski (2007) concluded that there is not any extant taxon that is closely similar to Cathiaria, but they suggested that the infructescence of Cathiaria shares most traits with the Moraceae and partially with the Urticaceae. Although Cathiaria shares a number of features with the Urticales (e.g., compound branched unisexual inflorescences, dorsiventral arrangement of flowers and fruits, flowers with a single unilocular pistil, reduced perianth), the new structural details documented in this study call these conclusions into question. The fruits of Cathiaria japonica contain two seeds, not one as interpreted by Golovneva and Oskolski (2007). The tricolpate reticulate pollen grains of Cathiaria are also different from the porate (2–6 pores) or forate pollen of Moraceae and Urticaceae. These differences may indicate that Cathiaria is not closely related to Moraceae–Urticaceae. Golovneva and Oskolski (2007) also compared Cathiaria with the Chloranthaceae because they share branched unisexual inflorescences, flowers with a single unilocular pistil and reduced perianth, and a one-seeded fruit. Flowers in Chloranthaceae are bisexual or unisexual with a single pendulous ovule in the fruit and the pollen grains are polyforate, 4-colpate, monosulcate, or 5–6-tomosulcate. Golovneva and Oskolski (2007) suggested that Cathiaria differs from extant Chloranthaceae by the adaxial arrangement of flowers and fruits on flattened lateral axes of infructescences and by non-fleshly fruits. However, mesofossils are often influenced by compression and do not necessarily retain their original shape. In addition, it could be difficult to determine whether the fruits were fleshy or not by the condition of mesofossils. Cathiaria differs from extant Chloranthaceae by the dorsiventral suture and a large, obliquely decurrent stigma suture, twin seeds in the locule and the tricolpate pollen grains. We conclude that Cathiaria is not closely related to Chloranthaceae.
Based on the new structural details described here we suggest that Cathiaria is most closely related to the Buxaceae s.l., which are placed among the early-diverging groups of eudicots, often close to the Trochodendraceae (Chase et al. 1993; von Balthazar et al. 2000, APG III 2009, APG IV 2016). The Buxaceae s.l. is now recognized to include the Didymelaceae and Haptanthaceae (APG 2009, 2016; Shipunov and Shipunova 2011). The Buxaceae s.l. are a small family of about 70 species in seven genera (Didymeles, Haptanthus, Buxus, Notobuxus, Sarcococca, Styloceras and Pachysandra), that are characterized by monoecious evergreen herbs to small trees and rather small flowers with an inconspicuous perianth or just a subtending bract (von Balthazar and Endress 2002). Pollen morphology includes tricolpate grains in Didymeles and Notobuxus, 3–7-colporate, 5–12-pantocolporate and 12–40 pantoporate in Buxus, and pantoporate in Sarcococca, Pachysandra and Styloceras (Table 1). Shipunov and Shipunova (2011) suggested that Didymeles is placed as sister to the other genera in the Buxaceae s.l. Golovneva and Oskolski (2007) noted that Cathiaria is similar to Didymeles in the branched unisexual inflorescences, flowers with single unilocular pistil and reduced perianth, but they distinguished Cathiaria from Didymeles by the structure of its female inflorescence consisting of two orders of axes with flattened secondary axes bearing up to 20 flowers, whereas Didymeles have three orders of axes and secondary axes bear paired flowers and fleshy fruits (Sutton 1989; Golovnea and; Oskolski 2007). Pistillate flowers of Cathiaria and Didymeles lack perianth, are subtended by a bract, have a unicarpellate gynoecium with an adaxial suture and a large, truncate or obliquely decurrent bilobate stigma, short style, and tricolpate pollen. Cathiaria and Didymeles differ in the size of the ovary and the number of seeds. Cathiaria japonica has two ovules in the monocarpellate ovary. A single fertile ovule is included in a single locule in Didymeles, and an additional rudimentary ovule is occasionally present in the locule (von Balthazar et al. 2003). The degree of branching of the inflorescence axis is difficult to document in the fossil material due to fragmentation of the charcoalified material. Flowers of Didymeles differ from those of the other five genera of Buxaceae s.l. (Buxus, Notobuxus, Sarcococca, Styloceras and Pachysandra), which are characterized by the presence of 4–6 tepals, 3-carpellate gynoecium with two ovules per carpel, and divergent styles. The rare genus Haptanthus, which is endemic to Honduras, has an unusual inflorescence morphology with a central pistillate flower and two subtending clusters of staminate flowers. The staminate and pistillate flowers are practically naked with minute basal bracts or vestigial perianth. The morphological details have not been made clear for Haptanthus, but the available information clearly distinguishes the genus from Cathiaria.
Drinnan et al. (1991) described Spanomera from eastern North American deposits of 113–98 m.y. age (Albian), which may be a member of stem group Buxaceae s.s. (see also Crepet et al. 2004; Doyle and Endress 2010; Doyle and Upchurch 2014). The pistillate flowers are dimerous, but in the staminate flowers there may be five stamens opposite five tepals, the pollen is tricolpate, and the fruit is follicular (Drinnan et al. 1991). Lusistemon, also with striate, tricolpate pollen (but with different anther insertion and arrangement), from deposits in Portugal of about the same age, seems to be related (Pedersen et al. 2007).
Thus, based on comparison of the available morphological features we conclude that Cathiaria is closely related to Didymeles in the Buxaceae s. l.. The discovery of Cathiaria from North Kazakhstan, Siberia, and Japan suggests that the extinct genus was widely distributed in eastern Laurasia during the Late Cretaceous, and the extant Didymeles is an endemic genus restricted in Madagascar at present.
Archaestella: structure
The genus Archaestella is established based on three-dimensionally preserved mesofossil specimens of a flower and fruits from the lower part of Ashizawa Formation of the Futaba Group (early Coniacian) in northeastern Japan. Archaestella verticillatus, is characterized by an actinomorphic, bisexual and multicarpellate flower. The gynoecium consists of a whorl of 10 conduplicate carpels that are laterally connate basally but distally distinct, with a conspicuous dorsal bulge. In the center of the flower there is a cavity. The styles are recurved with a papillate and ventrally decurrent stigma. There are ca. 10 ovules per carpel, marginal, pendulous from the broad, concrescent oblique summit of the locule. The pollen grains are tricolpate, with a reticulate exine pattern. The central cavity in the gynoecium is preserved until the stage of fruit. The characteristic stigma observed in the flower is absent in the fruiting specimens.
Archaestella: systematic relationships
The overall form of the fossil flowers, with numerous stamens that are clearly differentiated into anther and filament, laterally coherent carpels in a single whorl, and tricolpate pollen, narrows the range of likely systematic relationships and points toward affinities with members of the basal grade of the eudicots. A characteristic gynoecium with more than 10 laterally coherent carpels arranged in a single whorl is present in Menispermaceae, Papaveraceae and Trochodendraceae of the basal eudicot grade (Endress 1990). Among these families, the affinity of Archaestella is clearly with Trochodendraceae. Only Trochodendraceae have an androecium and stamens similar to those of the fossils. In Menispermaceae, the plants are dioecious with unisexual flowers composed of united stamens or free carpels with two ovules. In Papaveraceae the gynoecium is unilocular composed of a syncarpous ovary with sessile stigma or with indistinct to distinct style.
The Trochodendraceae are endemic to eastern Asia, from northeastern India to Japan, and comprise only two monospecific genera, Trochodendron and Tetracentron (Endress 1986). The systematic position of the Trochodendraceae was controversial until relatively recently. Li et al. (2011) and Ren et al. (2007) recently documented the presence of both of perforate vessel elements and tracheary elements in the xylem of Trochodendraceae, which was previously thought to lack vessels. Phylogenetic analyses based on molecular data (APG 2016) have placed the family in the basal eudicot grade close to Buxaceae s.l., along with Ranunculales (Berberidaceae, Circaesteraceae, Eupteleaceae, Lardizabalaceae, Menispermaceae, Papaveraceae, Ranunculaceae), Sabiaceae, and Proteales (Nelumbonaceae, Platanaceae, Proteaceae).
Flowers of the extant Trochodendraceae are hypogynous, bisexual, and actinomorphic or dissymmetric. The perianth consists of four sepals (Tetracentron) or is rudimentary (Trochodendron). The stamens have well differentiated filaments and anthers, which are basifixed, tetrasporangiate, apiculate, and latrose with each theca opening by pair of lateral valves. The semi-inferior carpels are syncarpous basally with free styles. In the stylar region the carpels are free and slightly recurved. The carpel flanks are congenitally fused. In the upper part of the ovary a compitum is formed by post genital fusion of the carpels in the center, while in the lower portion of the gynoecium the carpels do not meet in the center, but form a central dome (Chen et al. 2007; Endress 1986, Hsu et al. 2017). The pollen grains are spheroidal and tricolpate with striate-reticulate exine. The flowers of Tetracentron are sessile, small, about 2 mm in diameter, and hypogynous with 4 tepals and 4 stamens in decussate pairs and a whorl of 4 carpels. In fruit the follicles are laterally coherent and distally distinct. Archaestella is similar to Tetracentron in the presence of tepals, but differs in the presence of a pedicel and the larger number of floral parts. The flowers of Trochodendron are pedicellate, about 10 mm in diameter, with 40–70 spirally arranged stamens and one whorl of 4–(6)–17 semi-inferior carpels with free styles. Trochodendron is generally described as lacking a perianth, although variable numbers of rudimentary tepals are recognizable in early ontogenetic stages of flower development, but they are ephemeral and are lost at anthesis (Endress 1986). Wu et al. (2007) confirmed that extant Trochodendron has numerous perianth-like structures in young flowers, suggesting that the perianth of Trochodendron has been secondarily lost, and that both protandrous and protogynous flowers are present. The perianth of Cretaceous Archaestella could represent the ancestral form in Trochodendraceae, although this hypothesis would require testing with phylogenetic analyses. In post-anthetic flowers and fruits of Trochodendraceae the styles are recurved towards the outside of the flower, but in young flowers the tips are close to the center of the flower as also observed in the fossil flowers. The fruits of Trochodendron are follicles that are laterally coherent with distally distinct short recurved styles. The dorsal part of the ovary is horizontally extended at anthesis. Trochodendron and Archaestella share a number of distinctive floral features, including an extensively developed hypanthium and a stout pedicel. These two genera also share a whorl of carpels that form a small cavity of well-developed gynoecium. The features of young flowers of Trochodendron particularly resemble those of Archaestella. The fossil genus Archaestella shares most of the morphological features with the extant Trochodendraceae, particularly in the recurved styles and the small cavity at the cener of the whorl of carpels, although it is uncertain whether anthers dehisce by longitudinal slits or by lateral valves as in Trochodendron. The most striking feature of the Archaestella flowers, compared to flowers of extant Trochodendraceae, is their very small size and the corresponding small size of the stamens, carpels and pollen grains. The small size of Archaestella fits the common pattern seen when many other Late Cretaceous flowers are compared with flowers of their extant relatives (Friis et al. 2011).
Archaestella: comparison with fossil taxa
Although some fossils of the Trochodendraceae are reported from Cretaceous sediments in the Northern Hemisphere, most of these fossils are questioned and reliable data are sparse on the Trochodendraceae during Cretaceous (Friis et al. 2011). “Trochodendrophyll” leaves that are characterized with actinodromous venation and chlorantoid teeth occur in the middle Cretaceous of North America and Eurasia (Crabtree 1987; Crane 1989; Upchurch and Wolfe 1987), but these leaves have been assigned to Cercidiphyllaceae or a variety of extant families including Menispermaceae, Piperaceae, Rhamnaceae and Salicaceae (Crane et al. 1991). A fossil wood, Tetracentronites japonica Nishida, from the Lower Cretaceous of Japan is regarded to a member of Phoroxylon in Bennettitales (Suzuki et al. 1991).
An impression fossil of a pluricarpellate structure was recovered from the Aptian or Albian Crato Formation in Brazil, which appears to be a syncarpous and multilocular gynoecium borne on stout axis. There are eight (or nine?) carpels, laterally fused to from a capsule-like fruit (Mohr and Friis 2000). Mohr and Friis (2000) suggested that the syncarpous capsule-like fossil is a potential basal member of the eudicots, showing some resemblance to the fruits of Trochodendron, although the fossil is much larger, ca. 3 cm in diameter, and differs from extant Trochodendron in the position of styles. Archaestella is much smaller than the pluricarpellate structure from Brazil. The inner structure of the Brazilian specimen is not clear because of the impression fossil.
The fossil genus Nordenskioeldia is widespread from Late Cretaceous to Miocene of the Northern Hemisphere (Crane et al. 1991; Pigg et al. 2001; Wang et al. 2009). The fossil record of Nordenskioeldia has been reviewed by Crane (1989), Crane et al. (1990, 1991), Manchester et al. (1991), Pigg et al. (2001, 2007) and Wang et al. (2009). The fruit of Nordenskioeldia is described as schizocarpic, consisting of 10–20 fruitlets arranged in a whorl around a parenchymatous central column. Each fruitlet has a laterally concrescent single-seed. The central column tapers apically and is bilaterally symmetrical, with regular longitudinal ridges developed between each of the adjacent fruitlets. In Nordenskioeldia, remains of the receptacle and exocarp persist on the infructescence axis after dehiscence as a shallow cup with a central column. Dispersed fruitlets are D-shaped in outline, dehiscent and contain a single small ovate seed (Crane et al. 1991). Doweld (1998) suggested that the fruits of the extant Trochodendraceae are syncarpous, lack a central colum, and contain many seeds in the locules, unlike the “one-seeded” fruitlets of Nordenskioeldia. The extinct Cretaceous genus Archaestella differs from Nordenskioeldia in the syncarpous fruits, presence of a central cavity and lack of a central column, and presence of many seeds in each locule.
There are many reports of fossil infructescence and fruits of Trochodendron, such as from the Miocene of Clarkia and Emerald Creek, Idaho (Manchester et al. 1991), the Eocene McAbee and One Mile Creek sites of British Columbia, Canada, and the Eocene Republic flora of Washington, USA (Pigg et al. 2001, 2007). The fossil fruits of Trochodendron from the middle Eocene of Washington State, 2.0–3.7 mm wide, supported by peduncles that are very similar to the extant T. aralioides (Pigg et al. 2001). Trochodendron drachukii are from the Early to Middle Eocene of McAbee near Cache Creek, Columbia, Canada, is a well-preserved paniculater infructescence that has a woody axis and fruits, 3–4 mm long × 3–4 mm wide consisting of six or more fused carpels. Fossil fruits of Trochodendron are also known from the late Miocene of Iwate Prefecture, Japan (Uemura 1988).
The fossil record of Tetracentron was reviewed by Grímsson et al. (2008). Fossil fruits of Tetracentron remberi were described from the Middle Miocene Clarkia locality, Idaho, United States (Manchester and Chen 2006), and T. atlanticum was recovered from the Middle Eocene of Iceland and Middle Miocene of western North America (Grímsson et al. 2008). Fruits of T. atlanticum are slightly narrower, more elliptical, and longer than the fruits of T. remberi. The fossil fruits of Tetracentron are quite similar to the extant T. sinense, which are tetralocular capsules with four styles. The general organization of the fossil and extant fruits is identical (Grímsson et al. 2008). Tetracentron is different from Archaestella by the fruits of four carpels.
Conclusion
Cathiaria and Archaestella provide important new information about the early history of the eudicot clade. The first evidence of the group comes from tricolpate pollen grains in the late Barremian or Aptian of South America, Africa, and the Middle East (Northern Gondwana), as reviewed by Doyle (2012). The main radiation of the basal eudicots is considered to have occurred during the Albian (Early Cretaceous) (Crane 1989; Doyle 2012; Doyle and Hickey 1976). The new fossil genus Archaestella provides the earliest record of the Trochodendraceae. The new species Cathiaria japonica provides structural details that help to clarify the systematic relationships of this previously described fossil genus, The presence of Cathiaria and Archaestella in the Kamikitaba assemblage suggests that the two basal eudicot families, Trochodendraceae and Buxaceae (including Didymelaceae), had differentiated by the Coniacian (Late Cretaceous) in eastern Eurasia. The two families were members of the late Cretaceous paleoflora in eastern Eurasia, with the other Angiosperm families including Annonaceae, Nymphaeaceae, Lauraceae, Combretaceae, Cornales and Fagales, with Conifers and Pteridophytes.
Change history
07 June 2017
An erratum to this article has been published.
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Acknowledgements
The authors thank Peter R Crane and Stephen R Manchester for constructive and helpful comments on the manuscript. The study was funded by Grants-in-Aid for Scientific Research (21570092, 24570097 and 16K07477) from Japan Society for the Promotion of Science to M. T. and NSF Grant DEB-1348456 to P.S.H. Use of the Advanced Photon Source, an Office of Science User Facility operated for the US Department of Energy (DOE) Office of Science by Argonne National Laboratory, was supported by the US DOE under Contract No. DE-AC02-06CH11357.
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An erratum to this article is available at https://doi.org/10.1007/s10265-017-0957-x.
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Takahashi, M., Herendeen, P.S. & Xiao, X. Two early eudicot fossil flowers from the Kamikitaba assemblage (Coniacian, Late Cretaceous) in northeastern Japan. J Plant Res 130, 809–826 (2017). https://doi.org/10.1007/s10265-017-0945-1
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DOI: https://doi.org/10.1007/s10265-017-0945-1