A Multicarpellary Apocarpous Gynoecium from the Late Cretaceous
(Coniacian–Santonian) of the Upper Yezo Group of Obira, Hokkaido,
Japan: Obirafructus kokubunii gen. & sp. nov.
Y
uiK
ajita1,*, M
aYuMiH
anariS
uzuKi2andH
arufuMin
iSHida31Iriomote station, Tropical Biosphere Research Center, University of the Ryukyus, 870, Uehara, Taketomi,
Okinawa 907–1541, Japan. *yuiyuk@gmail.com (author for correspondence); 2Tama, Tokyo 206–0003, Japan; 3Faculty of Science and Engineering, Chuo University, 1–13–27 Kasuga, Bunkyo, Tokyo 112–8551, Japan
Obirafructus kokubunii gen. & sp. nov. (family Incertae Sedis; order Saxifragales) is proposed based on
a permineralized reproductive axis bearing at least 42 spirally arranged follicles. No bracts, perianth, stamens, nor their vestiges are present on the axis or the follicle stalk. It is therefore part of single flower and not an inflorescence. The axis is 57 mm long, woody, and contains scalariform perforations on the vessel walls. The flower is inferred to be unisexual, as in Cercidiphyllaceae (Saxifragales). The lower part, which may have borne male organs, is missing. The follicles consist of a conduplicate carpel with marginal placentas alternately bearing 90–100 seeds in two rows. The follicle has dorsal and ventral ridges and the ventral suture dehisces at maturity. The carpel probably has an apical style and stigma at anthesis. The ovules are bitegmic, anatropous. A nucellar cap plugs the micropyle. The seeds are slightly winged, which may represent hydrochory and/or anemochory. Based on these features, Obirafructus
kokubunii probably inhabited a fluvial plain. The follicle clusters of Joffrea and Jenkinsella (fossil
Cercidiphyllaceae) apparently resemble those of O. kokubunii; but they represent inflorescences.
Obirafructus kokubunii adds a new morphotype to the past diversity of basal Saxifragales.
Key words: anatomy, Cercidiphyllaceae, eudicot, follicle, fossil, inflorescence, Jenkinsella, Joffrea, mor-phology, Saxifragales
Acta Phytotax. Geobot. 72 (1): 1–21 (2021) doi: 10.18942/apg.202009 ISSN 1346-7565
The fossil described here was found in a cal-careous concretion that was collected along the Obirashibe River in Obira, Hokkaido, Japan, where Late Cretaceous shallow to offshore ma-rine sediments of the Haborogawa Formation of the Yezo Group occur. Nishida (2006) first tenta-tively reported the specimen to be a
‘Cercidiphyl-lum-like hamamelid’. The fossil-bearing strata was exposed along the main stream of the Obi-rashibe River. The age has been estimated to cor-respond to the Coniacian to Santonian period based on the associated marine fauna (Takashima
et al. 2004). An ammonite, Gaudryceras sp. (Fig.
1A), in the same concretion often occurs in the Haborogawa Formation and does not contradict the age estimation.
The Cercidiphyllum-like hamamelid fossil is a permineralized reproductive woody axis
bear-ing many follicles and is reminiscent of the mor-phologies of some extant and comparable fossil families of Saxifragales, sensu Angiosperm Phy-logeny Group IV system (2016). Among the Saxi-fragales, the fossil shows morphological similar-ity to Cercidiphyllaceae, both living and fossil forms (Swamy & Bailey 1949, Spongberg 1979, Crane 1984, Crane & Stockey 1985, Feng et al. 2000, Golovneva & Alekseev 2017). The Cercidi-phyllaceae include only two extant species that are restricted to Japan, China, and Korea. Their fossil records extend back to the early-middle Aptian (Golovneva & Alekseev 2017). In this study, we describe the specimen as a new fossil genus of Saxifragales, and particularly similar to Cercidiphyllaceae, without designating a particu-lar family due to scarce information regarding Cretaceous plants.
The fossil exhibits detailed anatomical infor-mation reminiscent of the morphological and functional diversity of basal Saxifragales, or more widely, of early Eudicots during their early diversification in the Cretaceous. We compared the seeds, follicles, and follicle clusters of the fos-sil with specimens of Cercidiphyllaceae to show morphological diversity of the seemingly similar dispersal organs. For comparison, the follicle anatomy of living Cercidiphyllaceae (i.e.,
Cerci-diphyllum japonicum Sieb. & Zucc. ex Hoffm. &
Schult.) was also evaluated in this study.
Material and Methods
The fossil material was embedded in a calcar-eous sandy siltstone concretion Kokubun NSM
PP-9374 (original sample number: Kokubun HKP0001), which was collected in the middle
reaches of the Obirashibe River, Obira town, Hokkaido, Japan. The concretion was cut into several pieces with a Mini-lab-cutter MC110 dia-mond slab saw (Maruto Instrument Co., Ltd., To-kyo, Japan) to obtain both transverse and longitu-dinal planes of the embedded reproductive shoot. For anatomical observations, the cutting planes were peeled sequentially using a cellulose-ace-tate peeling technique (Joy et al. 1956) to obtain serial peels and to make microscope slides of the selected peels. Non-destructive images of the concretions were also obtained using a ScanX-mate-A130S145 X-ray CT scanner (Comscantec-no Co., Ltd., Yokohama, Japan) to confirm the anatomical reconstruction and to search for other notable structures in the concretion. Whole piec-es of the sectioned concretion and the microscop-ic slides were deposited in the Tsukuba Research Department of the National Museum of Nature and Science in Tsukuba, Ibaraki, Japan.
For anatomical comparisons, follicles of ex-tant Cercidiphyllum japonicum were collected from the Koishikawa Botanical Garden of the Graduate School of Science of the University of Tokyo, Japan, and fixed with FAA (formalde-hyde: 70% ethyl alcohol: acetic acid = 1 : 18 : 1). The follicles were determined to be immature or
nearly mature before dehiscence. The fixed mate-rials were dehydrated in an ethyl and tertiary-bu-tyl alcohol series and embedded in paraffin. Sec-tions 10 µm thick were cut with a RM2125RTF rotary microtome (Leica Microsystems, Wetzlar, Germany) and stained with Hematoxylin (Sig-ma), Safranin-O (Merck), and Fastgreen (Sigma). Sections of both the fossil and extant C.
japoni-cum were mounted in Canada balsam and
exam-ined under a BX–50 light microscope (Olympus Optical Co. Ltd., Tokyo, Japan). Images were captured with a D–20 digital camera system (Pix-era Corporation, California, USA).
The numerical geological ages used in this pa-per adhere to the International Chronostrati-graphic Chart (Cohen et al. 2013: revised version May 2019).
Results
Systematic DescriptionPhylum Magnoliophyta Order Saxifragales Family incertae sedis
Obirafructus Y. Kajita & H. Nishida gen. nov.
Permineralized angiosperm reproductive shoot, consist-ing of a woody axis bearconsist-ing a number of spirally arranged follicles. Axis in fruiting stage elongate, eustelic; vessels with scalariform perforation plates. Follicle elongate fusi-form to falcate, tapering distally, dehiscing along ventral longitudinal suture; lateral surface transversely striate; placenta marginal. Dorsal midrib of follicle and each side of ventral suture ridged, 3-veined, 1 dorsal and 2 ventral. Follicle wall 3-layered, with pericarp, vascularized meso-carp, and fibrous sclerenchyma endocarp. Seeds numer-ous, flat, in 2 rows along ventral suture, one above the other. Seeds bitegmic, anatropous, winged; wing devel-oped on upper side of main seed body. Seed coats 2, inner and outer; inner seed coat thin; outer seed coat constitut-ing wconstitut-ing and lower fibrous layer. Nucellar wall thickened below endostome, forming a nucellar cap.
Obirafructus kokubunii Y. Kajita & H. Nishida sp. nov. — Figs. 1B–D, 2–10, 11D & 12C, D
Permineralized angiosperm reproductive shoot consist-ing of a woody axis bearconsist-ing more than 42 conduplicate
February 2021 Kajita & al. — Obirafructus kokubunii gen. & sp. nov. 3
follicles in 5 : 8 phyllotaxy. Axis in fruiting stage, more than 57 mm long, 2–5 mm in diam., eustelic; vessels with scalariform perforation plates. Follicles elongate fusiform to falcate, 30–40 mm long, 3 mm in diam., short-stiped, abruptly tapering distally, dehiscing along longitudinal ventral suture; lateral surface transversely striate; cross section nearly round with semicircular dorsal ridge and ventral ridge splits at middle along longitudinal suture. 3-veined, 1 dorsal and 2 on each side of ventral suture. Follicle wall 3-layered; pericarp thin, consisting of an epidermis with actinocytic stomata and hypodermis; me-socarp thick, parenchymatous, vascularized; endocarp composed of fibrous sclerenchyma cells; placenta mar-ginal. Seeds nearly 100, flat, tightly packed in each folli-cle, in 2 rows, one above the other, bitegmic, anatropous, winged on upper side, semicircular to oval, ca. 2 mm long, 1 mm wide along horizontal plane, ca. 0.6 mm thick at middle; wing fleshy parenchymatous inside, on upper side of main seed body, as thick as nucellar portion, anvil-shaped, with narrow marginal extensions horizontally around seed; nucellar portion semicircular to crescent-shaped in horizontal plane, rounded columnar in tangen-tial plane at widest middle portion. Seed coat composed of inner and outer layers; inner seed coat mostly 1 cell thick, 3 cells thick around endostome; outer seed coat
constituting wing and lower fibrous layer, attached to pla-centa on winged side, vascularized by a single bundle on upper middle portion of wing to chalazal end of nucellus. Nucellar wall membranous, thickened below endostome to form a nucellar cap.
Typus. Kokubun NSM PP-9374 (fruits in concretion
block and microscope slides prepared from it) deposited in the Paleobotanical Collection of the National Museum of Nature and Science in Tsukuba, Ibaraki, Japan.
Locality. Japan, Hokkaido, Obira, main stream
of the Obirashibe River, approximately 44º04′53″N 141º57′05″E.
Type strata. Upper Cretaceous (Coniacian to
Santonian) Haborogawa Formation, Yezo Group.
Etymology. The generic name comes from the
town, Obira, where the fossil site is located. The specific epithet honors Mr. Hakuji Kokubun, who found the specimen.
Morphological description. The specimen was
fig. 1. X-ray CT images of calcareous concretion containing a part of reproductive shoot of Obirafructus kokubunii gen. & sp.
nov., specimen Kokubun NSM PP-9374. (A) Ammonite, Gaudryceras sp., embedded in same nodule. Diameter of ammonite shell is about 1 cm. (B) Cross section of main axis, two follicles, and two follicle bases (arrowheads). (C) Radial longitudinal section showing main axis bearing stiped follicles containing numerous seeds. (D) Tangential longitudinal section of a follicle showing two rows of seeds. Note wing tissue on upper side of each seed. f, follicle; fs, follicle stalk; mx, main axis; s, seed; w, seed wing. B–D, Scale bar = 1 mm.
embedded in a calcareous sandy siltstone concre-tion about 25 cm in diameter and broken along lateral and upper surfaces where the specimen had been exposed (Fig. 2). A dark, woody axis with five elongate follicles and some isolated fol-licle sections (Fig. 2A) is present on the lateral surface. More than 11 follicles on the main axis at one end of the concretion were sectioned either transversely or obliquely (Fig. 2A). The follicles radiated upward from the main axis with short internodes at angles of ca. 15° (Figs. 2A & 11D). Although the lower part of the shoot was missing, we estimated the entire follicle cluster of the re-productive shoot to be about 75 mm long and 40 mm wide (Fig. 2A). The shoot apex was embed-ded in the concretion (Fig. 2A). An eroembed-ded follicle on the lateral broken side shows internal seeds in a vertical row (Fig. 2B). The lateral surface of the follicle is transversely striate. We used an X-ray CT scanner to examine the inside of the concre-tion, which was not used for making microscopic sections, to confirm that there were only the three main structures, the single main axis, the folli-cles, and the seeds in the follicle (Figs. 1B–D & 11D).
The preserved main axis, about 57 mm long, 5 mm × 2 mm in maximum diameter at its base, and 2 mm × 1 mm distally, was slightly crushed laterally. The axis is woody and eustelic (Fig. 3A). In one cross section, 32 follicles and the base of isolated follicle were counted around the main axis (Fig. 4). The follicle phyllotaxy is spiral with eight clockwise and five counterclockwise paras-tichies (Fig. 4B). Based on the reconstructed phyllotaxy, we estimated the minimum number of attached follicles to be 42. Judging from the seed morphology and stage of carpel dehiscence, we estimated that each follicle was at approxi-mately the same stage of development (Fig. 4A). Although the number of vascular bundles was difficult to count, the follicle parastichies (Fig. 4B) that we observed suggest that there were originally five primary bundles in the vascular cylinder of the main axis. The pith consisted of fibrous periphery and inner parenchymatous tis-sues that were heavily crushed near the center (Figs. 3 & 5A, B). The vascular bundles are
prob-ably collateral, although the phloem is not well preserved. The stele is surrounded by thin cortex observable as a black degraded layer (Fig. 3A). The xylem contains thin secondary wood consist-ing of vessels with spiral, scalariform and annu-lar thickenings (Fig. 5C, E) and fibers with simple pits (Fig. 5D). Scalariform perforation plates were observed in some vessels (Fig. 5F).
The follicles were elongate fusiform to fal-cate, 30–40 mm long and up to 3 mm in diameter, with a basal short stalk 3–4 mm long, and tapered distally (Figs. 2A, 4A & 6A, B, D). The follicle stalks lacked nodal structures for other floral or-gans or bracts, branching vascular bundles or ax-illary organs (Fig. 6D, E). One longitudinal ridge along the adaxial surface of the follicle dehisces in the middle to form a ventral slit that extends from the base to the extreme tip of the follicle (Figs. 4, 6A, B & 7B). The follicle trace derives directly from the main vascular cylinder as a woody vascular bundle, which eventually sepa-rates into a dorsal strand (ds, Fig. 3) and two ven-tral strands (vs, Fig. 3). The three traces are com-parable with the three main bundles supplying a typical conduplicate carpel. Each ventral strand immediately divides radially into two bundles (vs1 & vs2, Fig. 3), resulting in five traces at the distal end of the follicle stalk. vs1 continues dis-tally to the ventral ridge whereas vs2 further di-vides to expand in the lateral wall of the follicle (Figs. 3B & 7B, C). The ds enters the dorsal ridge of the follicle (Fig. 7A). No other traces, except those entering the follicles, were observed, pro-viding evidence that no other floral structures originated from the shoot. The follicle consists of a single ovary containing numerous seeds (Figs. 2B & 6D). The ovary shows marginal placenta-tion. The seeds are alternately attached on the placentas located on the adaxial surfaces of the ventral ridges (Figs. 6B, C, 7B & 8B). We ob-served two rows of seeds in cross and tangential sections in one ovary (Figs. 4, 6B & 8D), although the radial longitudinal sections showed seeds aligned in one row (Figs. 2B & 6C, D). Style and stigmatic tissues were not identifiable at most dis-tal tip of the follicle (Fig. 6A). The follicle wall or pericarp was divisible into three regions,
exo-February 2021 Kajita & al. — Obirafructus kokubunii gen. & sp. nov. 5
fig. 2. Calcareous concretion Kokubun NSM PP-9374 containing a reproductive shoot Obirafructus kokubunii gen. & sp. nov.
(A) Entire specimen before sectioning. (B) Upper part of specimen showing a longitudinally broken surface of a follicle containing seeds. f, follicle; fs, follicle stalk; mx, main axis; s, seed. Scale bar = 10 mm (A), 1 mm (B).
fig. 3. Obirafructus kokubunii gen. & sp. nov. (A) Cross section of female reproductive shoot showing structure of main axis (mx) and departing follicle bases. Scale bar = 1 mm. Slide Kokubun NSM PP-9374 Bbot#9. (B) Schematic drawing of lower portion of follicle showing vasculature. co, degraded black layer of cortex; ds, dorsal strand of a follicle; fs, follicle stalk; lv, lateral vascular bundles; p, pith of main axis; vs, ventral strand of a follicle distally dividing into vs1 and vs2.
fig. 4. Obirafructus kokubunii gen. & sp. nov. Cross section of female reproductive shoot. Slide Kokubun NSM PP-9374
Btop#99. (A) General structure. (B) Showing parastichies with eight clockwise (blue) and five counterclockwise (orange)
lines. Follicles are subsequently numbered from proximal to distal. f, follicle; fs, follicle stalk; mx, main axis; vl, ventral slit. Scale bar = 5 mm.
February 2021 Kajita & al. — Obirafructus kokubunii gen. & sp. nov. 7
fig. 5. Obirafructus kokubunii gen. & sp. nov. Anatomical features of main axis. (A) Cross section of pith with axis center to right direction. Peripheral and central cells of pith are smaller and crushed respectively. Slide Kokubun NSM PP-9374
Bbot#9. (B) Longitudinal section of pith with axis center to right direction, showing fibrous periphery (to left) and inner
parenchyma. Slide Kokubun NSM PP-9374 #77. (C–F) Xylem longitudinal sections. Slide Kokubun NSM PP-9374 B1#66. (C) Scalariform (sf) and spiral (sp) vessel thickenings. (D) Simple pits (pi) on fiber walls. (E) Scalariform (sf) and annular (an) vessel thickenings. (F) Scalariform perforation plates (arrowheads). Scale bar = 100 µm.
carp, mesocarp and endocarp (Fig. 7). The exo-carp consists of the outer epidermis and a hypo-dermis 3–5 cells thick (Fig. 7). The hypohypo-dermis corresponds to the dark layers immediately be-low the epidermis (Fig. 7). The epidermal cells were light brown and polygonal in shape in the periclinal section with occasional actinocytic sto-mata (Fig. 7D). The hypodermal cells were flat-tened in cross section, thick-walled, and probably contained a dark tannin-like substance (Figs. 7A–C & 8A). The mesocarp was composed of pa-renchyma (2–10 cells thick) and a nest of vascular bundles in the middle of the tissue (Fig. 7A–C). The mesocarp was thickest at the ventral and dor-sal ridges of the follicle and contained a columnar mass of thick-walled sclerenchymatous fibers that developed along the external surface of the ven-tral and the dorsal bundles, respectively (Figs. 7A, B & 8A, B). The endocarp was a single-cell layer of sclerenchymatous, transversely elongat-ed fibers (Figs. 7A, C & 8C), but did not develop in the placental region (Figs. 6C & 7B).
We counted at least 60 seeds in one of the largest follicles, although it was broken and in-complete. From the estimated follicle length and seed thickness we calculated that there were ~ 90–100 seeds in each follicle. The embryos and other tissues, except for some organic vestiges, were not preserved in the nucellus. We regarded the seeds to be mature because the follicles have started to dehisce (Figs. 4 & 6B). The seeds are flat, semicircular to oval, about 2 mm long, 1 mm wide, and 0.6 mm thick (Figs. 2B, 4A, 6B–D & 9A). The upper half of the seeds (distal direction in the follicle) consists of a fleshy layer of paren-chyma that formed an anvil-shaped wing (Figs. 6C, 8D & 9A, B). It is possible that the wing rep-resented a horn-shaped lateral extension in tan-gential view (Figs. 8D & 9A, B). The seeds were attached to the placenta by a short funiculus that continued to the seed wing (Figs. 6C & 12C, D). The ovules were bitegmic and anatropous; the mi-cropyle formed on the placental side (Figs. 6C & 8B). The outer seed coat consisted of three layers, outer, middle and innermost (Figs. 8B, 9 & 10A– C). The outer layer consisted of the outer epimis with sparse obtuse trichomes and fibrous
der-mal cells surrounding the entire seed (Fig. 9). The fibers were one to several cells thick, elongated in the direction of the funiculus and often filled with brown substances (Figs. 8B, 9 & 10B, C). The fi-brous layer extended to fill the margin of the lat-eral horn-like expansion of the wing (Fig. 9B). The middle layer was thick, parenchymatous and only developed in the upper winged portion of the seed (Figs. 8B, D, 9 & 10A). The parenchyma was 4–15 cells thick and thickest in the middle of the wing (Fig. 9A, B). Some parenchyma cells had pitted walls that we describe as idioblastic (Fig. 10A). We observed a single vascular bundle in the wing parenchyma below the outer fibrous cells (Fig. 9A). In the seed, the vascular bundle ran through the central part of the seed wing and reached the chalazal base (Figs. 9A & 12C, D). The innermost layer of the outer seed coat was one-cell thick and consisted of small, rounded po-lygonal cells filled with dark brown material (Figs. 8B, 9C, D & 10A–C). The inner seed coat was thin and composed of a single layer of flat cells with dark brown material, except at the mi-cropylar end where it was three cells thick and formed the endostome ring (Figs. 8B, 9A, C, D & 10C–E). We observed papillate protrusions on cells toward the inside of the endostome (Fig. 10D). The anticlinal walls of the tegmic cells had minute sinuations (Fig. 10E). The main nucellar body of the seed was located below the wing (Figs. 6C, 9A & 12C, D). The nucellus had a trans-lucent membranous wall (Fig. 9A, D) that thick-ened inside the endostome to form a nucellar cap, which was a small mound-like mass of cells plug-ging the endostome (Fig. 10C).
Follicle Wall of Cercidiphyllum japonicum
We also examined the follicles of
Cercidi-phyllum japonicum as the representative of an
ex-tant species with follicles like those of
Obirafruc-tus. Obvious dorsal and ventral ridges are not
formed in C. japonicum. Three major vascular bundles supply the follicle; one dorsal and one on each side of the ventral suture line (Fig. 13A, B). Longitudinal fibrous bundles were externally as-sociated with each vascular bundle (Fig. 13 A, B). Nests of vascular bundles were in the lateral walls
February 2021 Kajita & al. — Obirafructus kokubunii gen. & sp. nov. 9
fig. 6. Obirafructus kokubunii gen. & sp. nov. Sections of follicle. (A) Tangential longitudinal sequential sections through
ventral suture at follicle top. Upper slide Kokubun NSM PP-9374 Ctop#1. Lower slide Kokubun NSM PP-9374 Ctop#8. No typical stigmatic features are recognized. (B) Cross section showing pairs of winged seeds. Slide Kokubun NSM PP-9374
Btop#3. (C) Radial longitudinal section through placenta (pl). Arrowhead indicates ventral strand of follicle. Slide Kokubun NSM PP-9374 B1#67. (D) Radial longitudinal section of shoot showing main axis and attached follicles. Slide Kokubun NSM PP-9374 B1#67. (E) Longitudinal section showing main axis and attached follicle stalk. Slide Kokubun NSM PP-9374 B1#77. dr, dorsal ridge of follicle; fs, follicle stalk; mx, main axis; nu, nucellus; vr, ventral ridge of follicle;
fig. 7. Obirafructus kokubunii gen. & sp. nov. Follicle structures. A, and B: Cross sections. C: Longitudinal section.
D: Periclinal section. (A) Dorsal ridge. Slide Kokubun NSM PP-9374 Cbot#19. (B) Ventral ridge that dehisced at its
middle. Slide Kokubun NSM PP-9374 Cbot#19. (C) Lateral wall showing three pericarp layers. Note lateral vascular bundles (lv) in parenchymatous mesocarp. Slide Kokubun NSM PP-9374 Btop#5. (D) Outer epidermis with stomata. Slide
Kokubun NSM PP-9374 B1#77. ds, dorsal vascular strand; en, fibrous endocarp; ep, epidermis; fb, fibers; gc, guard cells;
February 2021 Kajita & al. — Obirafructus kokubunii gen. & sp. nov. 11
fig. 8. Obirafructus kokubunii gen. & sp. nov. Follicle and seed structures. A, and B: Radial longitudinal sections of follicle.
C, and D: Tangential sections of follicle. (A) Dorsal ridge tissues. Slide Kokubun NSM PP-9374 Bbot#9. (B) Placental side
of seed (arrowhead shows endostome). Slide Kokubun NSM PP-9374 B1#68. (C) Paradermal view of fibrous endocarp (en). Note simple-pitted cell walls. Slide Kokubun NSM PP-9374 Bbot#9. (D) Two rows of seeds in follicle. Slide Kokubun NSM
PP-9374 Btop#3. fb, fibers; hy, hypodermis; is, inner seed coat; lw, lateral wall of follicle; os, outer seed coat; pa,
parenchyma; w, seed wing. Scale bar = 200 µm.
of the follicle. The pericarp of Cercidiphyllum
ja-ponicum can be divided into three layers (Fig.
13). The exocarp consists only of the outer epi-dermis (Fig. 13). The mesocarp, in which the vas-cular bundles run, is parenchymatous and usually eight cells thick (Fig. 13). We observed three col-umns of vertically oriented fibers in the mesocarp of young carpel sections, one external to the dor-sal vascular bundle and two external to the ven-tral vascular bundles (Fig. 13A, B). Nests of fibers occurred dorsally in the mature mesocarp where the fibers are somewhat directed either vertically or obliquely (Fig. 13C). The mature endocarp was about 12 cells thick at its thickest and was com-posed of horizontally-elongated sclerenchyma-tous fibers (Fig. 13C). The endocarp was not formed in the placental regions (Fig. 13B, C).
Discussion
Obirafructus kokubunii gen. nov. & sp. nov. is
characterized by a woody axis, which helically bears numerous conduplicate follicles containing abundant seeds in two rows along the marginal placenta. The absence of any vestiges of bracts, perianth or stamens on the axis or in the axil of each follicle stalk suggests that the specimen of
O. kokubunii represents a single flower rather
than an inflorescence (Figs. 6D, E & 11D). This view is also supported by the internode anatomy, given that the follicle traces are derived directly from the main woody axis without associated traces of possible axillary organs (Fig. 3).
Although the morphotype, an elongated floral axis with many follicles, is not known in extant
Saxifragales, we inferred that Obirafructus
kokubunii belongs to that order and the most
closely related living relative is Cercidiphyllace-ae, based on the following. Plants having vessels with scalariform perforations, conduplicate and ventricidal carpels, and marginal placenta, as in
O. kokubunii, are only known in saxifragalean
families (Stevens 2001 onwards, Golovneva & Alekseev 2017, Soltis et al. 2018). Among the Saxifragales, follicles (i.e., apocarpous gynoecia) occur in Cercidiphyllaceae and Paeoniaceae. In particular, the former resembles O. kokubunii with regard to the formation of numerous com-pressed, squarish, winged seeds (Mohana Rao
1986, Stevens 2001 onwards, Soltis et al. 2018). Apical styles and stigmas occur in living Cercidi-phyllaceae, and the stigmas are characterized by unicellular papillae (Swamy & Bailey 1949, Spongberg 1979). In fossil Cercidiphyllaceae so far reported, the stigmatic regions are not pre-served (Crane 1984, Crane & Stockey 1985, Feng
et al. 2000, Golovneva & Alekseev 2017).
Al-though the style and the stigmas were not ob-served in O. kokubunii, it is possible that they originally formed but shrunk during follicle de-velopment. The stigma of Cercidiphyllum
japoni-cum actually shrivels after anthesis and falls
sometime before the follicle dehisces (Spongberg
fig. 9. Obirafructus kokubunii gen. & sp. nov. Seed structures. (A) Oblique cross section showing endostome (es) and inner
seed coat (is). Single seed vascular bundle (sv) runs through upper central portion of wing (w) and nearly reaches chalazal base. Note thin and translucent nucellar wall (nw). Slide Kokubun NSM PP-9374 Btop#93. (B) Cross section at marginal portion of seed wing. Note epidermis with obtuse trichomes (ot) on fibrous dermal cells. Slide Kokubun NSM PP-9374
Btop#9. (C) Cross section of seed coats of two vertically aligned seeds. Only outer epidermis and middle layer of outer
seed coat are shown for lower seed. Slide Kokubun NSM PP-9374 B#30. (D) Horizontal longitudinal section of seed coat near chalazal end. Slide Kokubun NSM PP-9374 Bbot#9. fb, fibers; ie, innermost layer of outer seed coat; pa, parenchyma. Scale bar = 100 µm.
February 2021 Kajita & al. — Obirafructus kokubunii gen. & sp. nov. 13
fig. 10. Obirafructus kokubunii gen. & sp. nov. Seed structures. (A) Cross section of winged portion of outer seed coat showing pitted idioblasts in parenchyma layer (pa) and innermost layer (ie). Slide Kokubun NSM PP-9374 Cbot#19. (B) Oblique periclinal section of lower portion of outer seed coat, showing fibrous outer layer (fb) and innermost layer. Slide Kokubun NSM PP-9374 Bbot#9. (C) Radial longitudinal section through entire micropyle, showing endostome (es), inner seed coat (is) and nucellar cap (nc). Slide Kokubun NSM PP-9374 B1#68. (D) Cross section of endostome. Note papillate protrusions of cells in micropylar opening. Slide Kokubun NSM PP-9374 Btop#93. (E) Paradermal view of inner seed coat. Slide Kokubun NSM PP-9374 Btop#5. Scale bar = 50 µm.
1979).
The Saxifragales are estimated to have ap-peared about 120 million years ago, during the Aptian age (Magallón et al. 2015), and fossil Cer-cidiphyllaceae have been reported from the Low-er Cretaceous- (at the earliest from the lowLow-er- lower-middle Albian) to Cenozoic-era strata, mainly based on impression/compression specimens, with the exception of some pyritized materials from the Eocene London Clay (Crane 1984, Crane & Stockey 1985, Feng et al. 2000, Golov-neva & Alekseev 2017). The oldest possible an-cestral ally of extant Cercidiphyllum has been de-scribed as ‘Eocercidiphyllites plants’ from the Turonian of the Negev Desert in Israel (Krassilov
et al. 2005, Krassilov 2010). This morphotype
as-semblage consists of Eocercidiphyllites Krassilov (leaves and shoots), Eocercidianthus Krassilov (fascicle with follicles), and Eocercidispermum Krassilov (seeds) (Krassilov et al. 2005). There is considerable variation in morphology of inflores-cences/infructescences among fossils of Cercidi-phyllaceae, as described in the next paragraph, which has resulted in nomenclatural problems when classifying fossil taxa. As a result, the no-menclature has been revised by synonymizing most names under the genus Jenkinsella Reid & Chandler (Golovneva & Alekseev 2017). Detailed taxonomic comparisons and stratigraphic and pa-leophytogeographic distributions of Jenkinsella
jiayinense (G. P. Feng, C. S. Li, Zhilin, Y. F. Wang
& Gabrielyan) Golovneva & P. Alekseev and oth-er fossil Coth-ercidiphyllaceae can also be consulted in Golovneva & Alekeev (2017). Joffrea speirsii Crane & Stockey from the Paleocene Paskapoo Formation in North America is an exceptional ex-ample of a wholly reconstructed fossil of Cercidi-phyllaceae (Crane & Stockey 1985).
We assume that the flowers of Obirafructus
kokubunii flower were pistillate and produced
multiple follicles (Fig. 11D), although the possi-bility that stamens or a perianth was attached to the missing basal part of the main axis cannot be denied. Living and fossil Cercidiphyllaceae are dioecious and their single follicle or follicle pairs corresponds to a pistillate flower (Fig. 11A–C, Swamy & Bailey 1949, Spongberg 1979, Crane &
Stockey 1985, 1986, Mohana Rao 1986, Feng et
al. 2000, Remizowa et al. 2009, Golovneva &
Alekseev 2017). We compared the follicle clus-ters among species belonging to different genera of Cercidiphyllaceae, Cercidiphyllum japonicum,
Joffrea speirsii, and Jenkinsella jiayinense and O. kokubunii. The complexity of the follicle
clus-ters in Eocercidianthus (not discussed here), was the same as in C. japonicum (Krassilov 2010). The female reproductive shoot of C. japonicum superficially appears as a multicarpellate flower, although it is a short inflorescence composed of 2–6(–13) monocarpous flowers (Fig. 11A, Swamy & Bailey 1949, Tucker & Grimes 1999). In C.
ja-ponicum, each carpel is subtended by a bract,
which may be a tepal (Yan et al. 2007). In addi-tion, rudiments of a floral apex and a second car-pel of single flower were observed in the inflores-cence (van Heel 1986, Endress 1993). The inflo-rescence of Jo. speirsii consists of flowers com-prised of either a single or a pair of carpels; a bract occurs between the carpel stalk or pedicel and the peduncle (Fig. 11B, Crane & Stockey 1985, 1986). In Je. jiayinense the flowers always comprise a pair of carpels with a joint scar be-tween the pedicel and the peduncle, although bracts are not present (Fig. 11C, Feng et al. 2000). In C. japonicum, the adaxial surface of each car-pel faces away from the main inflorescence axis (Fig. 11A, Swamy & Bailey 1949), whereas in Je.
jiayinense, the carpels first face each other and
the carpel stalk later twists and the ventral slit turns to face the outside of infructescence (Fig. 11C, Feng et al. 2000). If O. kokubunii was de-rived from cercidiphylloids with a compound in-florescence, the elongated flower O. kokubunii should be phylogenetically derived from such an-cestral forms through complete reduction of the bracts and other associated floral organs. How-ever, O. kokubunii is older than the estimated di-vergence time of cercidiphylloids (Magallón et
al. 2015). It is also reasonable to consider that O. kokubunii represents a floral morphotype earlier
than the establishment of cercidiphylloid inflo-rescences during the early Cretaceous diversifi-cation of the saxifragalean stem groups. Saxi-fragales are not supported by any morphological
February 2021 Kajita & al. — Obirafructus kokubunii gen. & sp. nov. 15
synapomorphies (Hermsen et al. 2006). The present morphological variation in the order is derived from diversifications in the early Creta-ceous period (Magallón et al. 2015) and possible subsequent extinctions.
The elongated flowers and radially arranged follicles of Obirafructus kokubunii are reminis-cent of Archaefructus Sun, Dilcher, Zheng & Zhou, Archaeanthus Dilcher & Crane, and other fossil magnoliids and ranunculids. Archaefructus
has been the focus of most research since Sun et
al. (1998, 2002) proposed that it was the oldest
angiosperm, from the late Jurassic, and that its reproductive structure represented the most primitive floral state. However, later researchers revised the age of Archaefructus, stating that it corresponded to the Barremian–Aptian age (~125 Ma) and that the elongated ‘flower’ was a bisexu-al inflorescence (Friis et bisexu-al. 2003, Zhou et bisexu-al. 2003, Ji et al. 2004). Additionally, Archaefructus
A
B
C
D
vl
br
vl
br
jo
jo
vl
vl
pd
pe
pd
pe
fs
fs
Fig.
11
pe
fig. 11. Comparison of reproductive shoots. (A) Cercidiphyllum japonicum (modified from Fig. 19 in Crane & Stockey 1986).
(B) Joffrea speirsii (modified from Fig. 20 in Crane & Stockey 1986). (C) Jenkinsella jiayinensis (modified from Fig. 29 of “Nyssidium jiayinense” in Feng et al. 2000). (D) Obirafructus kokubunii gen. & sp. nov. br, bract; fs, follicle stalk; jo, joint of follicle stalk and peduncle; pe, peduncle and branch of peduncle; pd, pedicel vl, ventral slit.
differs from Obirafructus kokubunii in that it is a smaller, herbaceous plant, although fossil speci-mens were compressed and the anatomical struc-ture could not be observed (Friis et al. 2003, Zhou
et al. 2003, Ji & al. 2004). Archaefructus eoflora
Ji, Li, Bowe, Liu & Taylor is reported to demon-strate laminar placentation (Ji et al. 2004), which is distinct from the marginal placentation of
Obi-rafructus. Archaeanthus from the late Albian to
the early Cenomanian age of North America ex-hibits bisexual, multicarpellary, apocarpous flow-ers that bear 100–130 loosely spaced condupli-cate follicles (Dilcher & Crane 1984).
Archaean-thus is regarded as representing a stem group of
extant Magnoliaceae (Friis et al. 2011). In the Magnoliaceae, abaxial dehiscence is common, but the carpels of Archaeanthus dehisce adaxial-ly (Dilcher & Crane 1984, Romanov & Dilcher 2013). The carpel structure of Archaeanthus is apparently similar to that of O. kokubunii; how-ever, Archaeanthus has hairy stigmatic crests along the ventral ridges (Dilcher & Crane 1984, Romanov & Dilcher 2013). Such a stigmatic re-gion was not present in O. kokubunii, which rep-resents a significant difference from
Archaean-thus.
fig. 12. Comparison of seed structures. A, and B: Cercidiphyllum japonicum (modified from Swamy & Bailey 1949, Krassilov
2010). C, and D: Obirafructus kokubunii gen. & sp. nov. A, and C: Vertical longitudinal sections. B, and D: Sections at broken lines in (A & C), respectively. is, inner seed coat; nu, nucellus; os, outer seed coat; sb, seed base attached to placenta; sv, seed vascular bundle; w, wing.
February 2021 Kajita & al. — Obirafructus kokubunii gen. & sp. nov. 17
The conduplicate follicular morphotype is shared among other late Early to Late Cretaceous fossil forms of earlier magnoliids and ranuncu-lids (Krassilov 2010). Protomonimia H. Nishida & Nishida, Hidakanthus Nishida, Ohsawa, H. Nishida, Yoshida & Kanie, and Keraocarpon Ohana, T. Kimura & Chitaley are included in the former, while Hyrcantha Krassilov & Vachra-meev and Ternaricarpites Krassilov & Volynetz are included in the latter (Krassilov et al. 1983, Nishida & Nishida 1988, Nishida et al. 1996, Ohana et al. 1999, Dilcher et al. 2007, Krassilov & Volynetz 2008). In the former forms, which are permineralized and possible eumagnoliid struc-tures from the Turonian to Santonian of Hokkai-do, Japan, the carpels developed adaxial hairy stigmatic crests rather than the terminal stigmatic area, although the presence of stigmatic hairs was only confirmed in Protomonimia (Nishida & Nishida 1988, Nishida et al. 1996, Ohana et al. 1999). Obirafructus kokubunii has a solitary fol-licle with a short stalk on a woody axis and de-hisces adaxially. Hircantha, however, produces basally united follicles on an herbaceous axis (Krassilov et al. 1983, Dilcher et al., 2007) and
Ternaricarpites has dorsicidal follicles with an
abaxial dehiscent crest (Krassilov & Volynetz 2008). These morphotypes can be interpreted as being derived during earlier diversification of pre- to early Eudicots before the appearance of the core Eudicots, including Saxifragales. There-fore, we hypothesize that O. kokubunii represents a new, permineralized fossil genus of Saxifrag-ales represented by a single carpellate floral axis without assigning it to a particular family. We propose that O. kokubunii represents a new mor-photype that will aid in reconstructing the past diversity of the Saxifragales, and more widely, Eudicots in general.
Comparison with Cercidiphyllum japonicum and Paleoecology of Obirafructus
The general morphology of follicles and seeds in Obirafructus kokubunii and the Cercidiphylla-ceae show many similarities, but there are also anatomical and histological differences between them. We compared the anatomical structures of
O. kokubunii and living Cercidiphyllum japoni-cum based on observations and previous studies,
given that the known anatomical details of fossil Cercidiphyllaceae are limited and depend on the state of preservation of the fossil. Follicles of O.
kokubunii and C. japonicum show a typical
con-duplicate structure with three major vascular bundles in their three-layered walls, but differ in follicle wall (pericarp) proportions and histologi-cal features.
The pericarp in Obirafructus kokubunii and
Cercidiphyllum japonicum is divisible into
exo-carp, mesoexo-carp, and endocarp (Figs. 7 & 13, Mo-hana Rao 1986). The exocarp of O. kokubunii had hypodermal cells containing tannin-like sub-stances, while C. japonicum lacks a hypodermis but produces tannin-containing cells in the outer layer of the mesocarp (Figs. 7A–C, 8A & 13, Mo-hana Rao 1986). The mesocarp of both O.
kokubu-nii and C. japonicum resemble each other in their
parenchymatous nature, thickness, presence of vascular bundles, and occurrence of a vertical fi-ber column along the major three vascular bun-dles in the follicle (Figs. 7 & 13, Mohana Rao 1986). In contrast to the thick endocarp of C.
ja-ponicum, the endocarp of O. kokubunii is thin
and consists of a single layer of fibrous cells (Fig. 7A, C). The endocarp of C. japonicum is also composed of fibrous cells, although it is much thicker (ca. eight cells thick) than that of O.
kokubunii (Figs. 7A, C & 13, Mohana Rao 1986).
In young follicle walls of C. japonicum, the endo-carp is thin, but thickens during a later develop-mental stage via periclinal cell division (Mohana Rao 1986). The transverse orientation of the fi-brous cells of the mesocarp in both genera prob-ably helps to protect the follicle from being crushed and further increases mechanical tension when the follicles dry and dehisce.
The winged seeds or samaras with a one-sid-ed anatropous chalazal wing are widely seen in taxa of Cercidiphyllaceae (e.g., Cercidiphyllum
japonicum, Jenkinsella jiayinense, and Joffrea speirsii; Stockey & Crane 1983, Crane & Stockey
1985, Feng et al. 2000, Krassilov 2010, Golovne-va & Alekseev 2017). The seeds of Obirafructus
fig. 13. Cercidiphyllum japonicum. Follicle cross sections. (A) Dorsal portion of immature follicle. Note absence of hypodermis.
(B) Ventral portion of follicle in A. (C) Follicle at a later developmental stage showing pericarp structures. Note thick endocarp. Ventral slit (vl) to right. ds, dorsal strand; en, fibrous endocarp; ep, outer epidermis; fb, fibers; me, mesocarp; pl, placenta; s, seed; vs, ventral strand. Scale bar = 100 µm.
February 2021 Kajita & al. — Obirafructus kokubunii gen. & sp. nov. 19
bitegmic, anatropous ovules and the micropyle was formed by the outer and inner seed coats (Figs. 8B, 10C & 12A, C, Mohana Rao 1986, En-dress & Igersheim 1999). The outer seed coat on the funicular side was indistinguishable from the funicular tissue in the two species (Figs. 6C, 8B & 12A, C, Endress & Igersheim 1999). The ob-tuse trichomes of the outer epidermis and the fi-brous cell layers in the outer seed coat observed in Obirafructus kokubunii (Figs. 8B & 9) were not seen in C. japonicum (Mohana Rao 1986, En-dress & Igersheim 1999). However, in Jo.
speir-sii, a finely striate seed surface was observed and
may possibly show the impressions of the fibrous layer in the outer seed coat (Crane & Stockey 1985). The inner seed coat of O. kokubunii had 1–3 cell layers that were composed of dark brown cells (Figs. 9C, D & 10), while the inner seed coat of C. japonicum was a three-cell layer of paren-chyma (Endress & Igersheim 1999, Mohana Rao 1986).
A nucellar cap was seen in Obirafructus
kokubunii (Figs. 8B & 10C), but not observed in Cercidiphyllum japonicum (Endress & Igersheim
1999). However, several families in Saxifragales form a nucellar cap (Stevens 2001 onwards). In C.
japonicum, the ovule is epitropous (the micropyle
is located above the raphe), and the chalazal side of the seeds expands conspicuously to form a wing in a longitudinal downward manner to the follicle base (Fig. 12A, B). In O. kokubunii, the ovule was apotropous (the micropyle was located under the raphe), and the wing of the seed was formed by lateral extension of the anvil-shaped parenchymatous tissue above the main seed body (Figs. 8D & 9A, B), with limited expansion on the charazal side (Fig. 6B). We cannot conclude that the difference in ovule position with regard to the raphe between O. kokubunii and C. japonicum is taxonomically significant because the ovule posi-tion may sometimes vary within the same ovary (Decraene et al. 2000). It is interesting to note that Krassilov (2010) reported anomalies in the shape of the wing of C. japonicum, including a symmetrical samara developing a bilateral wing. Such anomalies suggest that the widespread non-symmetrical seeds in the Cercidiphyllaceae are
derived from ancestral forms with equally devel-oped peripheral wings. The mid-Albian seeds of
Eocercidispermum from Israel are interpreted as
representing such an ancestral Cercidiphyllum morphotype (Krassilov 2010).
Crane & Stockey (1985) recognized a vascu-lar ‘hair-pin loop’ in the seed wing as a common feature of Cercidiphyllum-like plants, and
Obi-rafructus kokubunii shows similar seed
vascula-ture (Fig. 12C). The vascular bundle in C.
japoni-cum, however, forks once at the hair-pin, leaving
a tiny bundle on the opposite side (Fig. 12A, Krassilov 2010). If this branching is a rudimen-tary ovule-supplying bundle, it may support the idea that the primitive character state of the an-giosperm ovule in the early stage of carpel/ovule evolution was multiovulate, which has been de-duced from Evo-Devo studies (Yamada et al. 2016, Nishida et al. 2018). In the seed vasculature of O. kokubunii, such branching was not ob-served.
We here consider the habit and habitat of
Obi-rafructus kokubunii based on the anatomical
fea-tures of the specimen. The follicles were hypoth-esized to have matured because they have started to dehisce (Figs. 4 & 6B). The large number of seeds and the small size of the seed-wing indicate non-zoochoric dispersal as common among both fossil and living Cercidiphyllaceae. The samaras in Cercidiphyllaceae are clearly adapted for ane-mophily, and the follicles twisting to face the ventral opening on the outside of the infructes-cence represent a characteristic of efficient seed dispersal. The narrower, thicker, and anvil-shaped wing tissue of O. kokubunii (Figs. 6C, 8D & 9A, B) appears to be suitable for both ane-mophily and hydrochory. Floating with the main seed body downward might be an adaptive char-acteristic that promotes safe seed germination, given that the seed is covered and protected by the wing tissue on sedimentary soil surfaces or the desiccating shallow water at fluvial margins. The seed coat with sclerenchymatous fibers in O.
kokubunii might increase seed durability. The
nu-cellar cap plugging the micropyle (Fig. 10C) may have protected the nucellus and embryo from ei-ther desiccation or water immersion. We ei-
there-fore suspect that O. kokubunii grew on a fluvial plain and dispersed its seeds via both water and wind. With regard to the study on vessel perfora-tion by Lens et al. (2016), plants with scalariform perforations tend to grow in environments with-out drought stress. For example, scalariform per-forations occur in Cercidiphyllum japonicum, which prefers margins of water or wet environ-ments (Swamy & Bailey 1949, Ishida & Ohtani 1974). Although the wood anatomy of O.
kokubu-nii is unknown, the scalariform perforations in
the main axis support similar habitat preferences.
We are grateful to Mr. Hakuji Kokubun for donating the specimen. Thanks are due to Mr. Yusuke Takebe, Chuo University, who prepared X-ray CT images. Special thanks to Prof. Toshihiro Yamada, Osaka City University, for identifying the ammonoids in the concretion. Materi-als of Cercidiphyllum japonicum were provided by Koi-shikawa Botanical Garden, Graduate School of Science, the University of Tokyo. This study was partly supported by Chuo University Personal Research Grant to HN in 2015 and 2017. We are thankful for the financial support from the Tropical Biosphere Research Center, University of the Ryukyus.
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