Angiosperm pollen grains of the triprojectate and oculate groups are widely distributed in Upper Cretaceous strata of the Northern Hemisphere, being used as biostratigraphic markers from their high diversification rate. Most reports from northeastern Asia, however, concern terrestrial deposits, and the rich record existing in Japan from marine sequences, with a well-established bio-magnetostratigraphy, appears critical for correlating their range among the Circum Pacific region. Here we propose a revision of Japanese reports of these groups, constraining their diversity to 17 genera and 91 species. A selected array of 15 species of well-preserved triprojectate pollen was further obtained from an abundant sporo-pollen assemblage of a hadrosaurian dinosaur Kamuysaurus japonicus-bearing bone bed in the outer shelf deposits of the Upper Cretaceous Hakobuchi Formation, Yezo Group, recently discovered in the Hobetsu area of Mukawa Town in Hokkaido, Japan; the assemblage co-occurs with the ammonoid Pachydiscus (Neodesmoceras) japonicus belonging to the Nostoceras hetonaiense zone, supporting an early Maastrichtian age.
Introduction
Within the Upper Cretaceous palynostratigraphy of the Northern Hemisphere, pollen belonging to the oculate and triprojectate groups have proved to be reliable stratigraphic index fossils because of their wide varieties of sculpture patterns and high diversification rate (e.g. Srivastava, 1970; Takahashi, 1981, 1982; Nichols and Sweet, 1993; Nichols, 1994). Their chronostratigraphic ranges are well calibrated from radiometric dating, magnetostratigraphy, and ammonoid biostratigraphy of marine and non-marine strata of North America and Asia (e.g. Eberth and Deino, 2005; Cobban et al., 2006; Li et al., 2011; Yoshino et al., 2017; Braman, 2018). In particular, the Campanian to Maastrichtian sequence of the mainly non-marine Horseshoe Canyon (e.g. Srivastava, 1970) and St. Mary River (e.g. Jerzykiewicz and Sweet, 1988) formations, the marine Bearpaw Formation (e.g. Jerzykiewicz et al., 1996) and other formations outcropping in Alberta (Canada) and Montana (USA) have rich pollen assemblages. Recent U–Pb dating with magneto-cyclostratigraphy of the terrestrial succession in the Songliao Basin, China further calibrated the palynostratigraphy including oculate and triprojectate groups (Li et al., 2011; Wu et al., 2014; Yoshino et al., 2017).
Triprojectate pollen (i.e., tridemicolpate pollen with a polar axis and most commonly three equatorial projections [Funkhouser, 1961; Krutzsch, 1970; Stanley, 1970]) is reported from the late Turonian to the Oligocene, and is mostly diversified in Campanian to Maastrichtian sediments, being mainly cosmopolitan but also showing provincialism for some species (Braman, 2013). In Asia, it is the dominant component of many palynofloras of Siberia, Far East Russia, Northeast China, and Japan. Botanical affinities of this group are still unclear due to the lack of in situ material associated with floral remains, but some authors suggested affinities to the Santalales (Funkhouser, 1961; Krutzsch, 1970) or the Apiales (Stanley, 1970) based on morphological similarities to extant pollen grains of these orders, and a possible polyphyletic origin was proposed by Farabee (1990). Angiosperm plants producing triprojectate pollen (or the “Triprojectacites-type”) grew under humid climate conditions (Sweet, 1990) and preferred a marshy paludal environment (Srivastava, 1973).
Oculate type pollen (or the “Oculata-type”) was designated by Chlonova (1962) to include pollen showing an elliptical shape and bilateral symmetry, with one pair of apertures formed on opposite sides of the grain. Only dispersed pollen was reported for this type and no similar pollen is known from extant plants (Chlonova, 1967; Leffingwell et al., 1970; Wiggins, 1976). Therefore, its botanical affinity is not yet clarified. It includes the three genera Azonia Samoilovitch in Samoilovitch and Mtchedlishvili (1961), Wodehouseia Stanley, 1961, and Singularia Samoilovitch in Samoilovitch and Mtchedlishvili (1961), and ranges from the late Santonian to Paleocene of North America, Canada, Greenland, Russia, China and Japan, being most common and widely distributed during the Maastrichtian (e.g. Samoilovitch and Mtchedlishvili, 1961; Stanley, 1961; Wiggins, 1976; Takahashi, 1984).
Bio-magnetostratigraphy is well established in Japan compared to adjacent areas, and palynostratigraphy would provide an additional tool for dating terrestrial strata of Asia with still debated age. In particular, the rich triprojectate and oculate pollen record existing in marine formations of northern Japan appears critical for correlating records from eastern Asia and North America. However, many of these pollen records are from pioneering works, while many nomenclatural modifications were applied to the two groups since then. Geological age of strata including these grains has also been modified.
We propose in this paper a major revision of the triprojectate and oculate pollen records of Japan, and discuss its consequences for the biostratigraphic significance of these groups in the Circum-Pacific region. We further add new well-preserved pollen data obtained from calcareous nodules of a hadrosaurian dinosaur Kamuysaurus japonicus-bearing bone bed of the Hakobuchi Formation, Yezo Group. This assemblage co-occurs with the ammonoid Pachydiscus (Neodesmoceras) japonicus belonging to the Nostoceras hetonaiense zone tentatively correlated with the early Maastrichtian, however, possibly late Campanian according to the uncertainty of magnetostratigraphy and radiometric age. We use triprojectate species of the palynoflora to confirm the age of the K. japonicusbearing bone bed in the Nostoceras hetonaiense zone.
Localities and ages of triprojectate and oculate pollen used for palynostratigraphic compilation
Marine formations yielding triprojectate and oculate pollen used for establishing the palynostratigraphic framework of the present revision are distributed in Northeast Honshu and Hokkaido. In Northeast Honshu, reports exist from the Uge Member of the Taneichi Formation (Takahashi and Sugiyama, 1990), assigned to the Santonian from the inoceramid Sphenoceramus sanrikuensis (Matsumoto and Sugiyama, 1985); the Tamagawa Formation of the Kuji Group (Miki, 1972, 1977; Umetsu and Kurita, 2007), assigned to the Turonian on the basis of 90.51 ± 0.54 Ma of U–Pb age of intercalated tuff beds (Uno et al., 2018), and correlation with the ammonoid (Futakami et al., 1987; Toshimitsu et al., 1995) and inoceramid (Toshimitsu et al., 1995) assemblages of the Kunitan Formation.
In Hokkaido, pollen records are obtained from the following hemipelagic to shallow marine successions bearing molluscan fossils: the Turonian Tenkaritoge Formation, Santonian–Campanian Haborogawa Formation, Coniacian Nishichirashinai Formation, Campanian Omagari and Osoushinai formations, and Campanian–Maastrichtian Hakobuchi Formation of the Yezo Group (Sato, 1961; Takahashi, 1964, 1965; Miki, 1977; Tanaka and Hirano, 2008), and the Maastrichtian Hamanaka and Oborogawa formations, the Maastrichtian–Danian Akkeshi Formation, and the Paleocene Tokotan Formation of the Nemuro Group (Takahashi and Ueda, 1990; Takahashi, 1991a, b, c; Takahashi and Yamanoi, 1992), the Paleocene Kiritappu Formation (Takahashi, 1991c), and the Maastrichtian–Danian Katsuhira Formation (Takahashi and Yamanoi, 1992).
Geological setting
Kamuysaurus japonicus-bearing bone bed.—Calcareous nodules of the Kamuysaurus japonicus-bearing bone bed were obtained from the Hakobuchi Formation, representing the uppermost part of the Yezo Group. The Hakobuchi Formation consists of lower Campanian–Paleocene shallow marine sandstone and conglomerate facies (Takashima et al., 2004). Matsumoto (1942) further divided the Hakobuchi Formation into five units (IVa–IVe). Kamuysaurus japonicus was found from the middle part of the IVb unit of the Hakobuchi Formation, at the upstream of the Shirafunezawa Creek, in northern Hobetsu area (Figure 1; location of the outcrop, 42°50′48″N, 142°7′20″E), and large-scaled joint excavation was held in 2013 and 2014 by the Hobetsu Museum, Mukawa Town, and Hokkaido University (Kobayashi et al., 2019). The IVb unit is considered as having been deposited in an outer shelf environment based on the presence of glauconite sandstone and the absence of any hummocky cross-stratification (Kusuhashi et al., 2017; Kobayashi et al., 2019). Some marine bivalves (e.g. Nannonavis, Nucula and Inoceramus), gastropods, shark teeth, and fish scales were found at the locality. Moreover, Pachydiscus (Neodesmoceras) japonicus, an index of the Nostoceras hetonaiense zone, was recovered about 5 m below and 3 m above the K. japonicus-bearing horizon (Kobayashi et al., 2019). The age of the Nostoceras hetonaiense zone has been considered as early Maastrichtian, but a possibility could not be completely ruled out that it may start from late Campanian based on magnetostratigraphy (Kodama, 1990) and U–Pb ages (Shigeta et al., 2017a, b). Kodama (1990) identified Chron 32n2n to 32n1n for the Nostoceras hetonaiense zone in the Izumi Group in Southwest Japan, striding the Campanian/ Maastrichtian boundary. For U–Pb radiometric dating, 73.0 ± 1.8 Ma and 70.5 ± 1.1 Ma are reported from the ash beds below and above Gaudryceras izumiense zone, one zone above the Nostoceras hetonaiense zone of Etanpakku Formation in the Soya Hill area, Hokkaido, Japan (Shigeta et al., 2017a). Additionally, the Didymoceras awajiense zone, three zones below the Nostoceras hetonaiense zone, reports a U–Pb age of 72.4 ± 0.8 Ma from a volcanic ash layer (Shigeta et al., 2017b). Thus, a part of the Nostoceras hetonaiense zone may be older than the age assigned to the Campanian/Maastrichtian boundary (72.2 ± 0.2 Ma; Gale et al., 2020).
Figure 1.
Location map and geology of Kamuysaurus japonicus excavation site. A, distribution map of the Yezo Group in Hokkaido; B, geological map of Shirafune-zawa creek, northern Hobetsu area; C, columnar section of the IVb unit of the Hakobuchi Formation, Yezo Group; D, Kamuysaurus japonicus-bearing bone bed from an downward view, with location of the seven jacket samples (modified after Kobayashi et al., 2019).

Terrestrial strata of Japan yielding triprojectate and oculate pollen.—In Northeast Honshu, reports exist from the Kasamatsu Formation of the Futaba Group (Takahashi, 1964), assigned to the late Coniacian from its stratigraphic position between the Ashizawa and Tamayama formations, which yield inoceramids (Matsumoto et al., 1982); the Sawayama Formation of the Kuji Group (Miki, 1972, 1977; Umetsu and Kurita, 2007), tentatively assigned to the early Campanian from its pollen assemblage; and the Yokomichi Formation (Tanai et al., 1978), assigned to the late Campanian from the report of a fission-track zircon dated as 71.2 + 4.4 Ma from the upper part of the formation (Kato et al., 1986).
In Central Japan, triprojectate pollen has been reported from non-marine sequences of the Miyadani-gawa Formation (Kasahara and Shimono, 1974; Takahashi, 1980; Takahashi and Shimono, 1982), the Omichidani Formation (Takahashi, 1991d; Nichols et al., 2010) and the Asuwa Formation (Sazawa et al., 2020). The Miyadani-gawa Formation should intercalate within volcanic rocks of 72–70 Ma (Hoshi et al., 2016), however, the exact relationship between the Miyadani-gawa Formation and latter volcanic rocks is not clear. All these strata have an uncertain age and were assigned to the Maastrichtian from their plant macro- and microfossil assemblages.
Thus, the Sawayama, Miyadani-gawa, Omichidani and Asuwa formations will not be included in stratigraphic considerations of the present study, but mentioned in appendix for their palynoflora. Recently, triprojectate pollen was also recovered from a terrestrial sequence of the Himenoura Group in South Japan (Legrand et al., 2018), assigned to the Maastrichtian based on U–Pb radiometric dating on zircons of 70.0 ± 0.5 Ma (Miyake et al., 2018).
Material and methods
The material used in this study consists of sandy mudstone collected from jackets used during the excavation of Kamuysaurus japonicus (Kobayashi et al., 2019), and provided by the Hobetsu Museum, Mukawa town, Japan. Jackets are burlap bandages soaked in plaster for encasing and tightly binding together excavated bones with the surrounding rock matrix and permitting their secured transportation. Samples were collected from seven jackets (J2, J12, J24, J25, J26, J27, J29) stored at the Hobetsu Museum, which covered the chevron (J2), right metatarsus (J12), dorsal vertebrae (J24), scapula (J25), left femur (J27), and skull (J26, J29) of K. japonicus. We collected some samples from the downside part of these jackets, labeled as J24D, J25D, and J29D (Figure 1).
Method for pollen extraction follows Legrand et al. (2013). Pollen grains were observed using a Leica DM2500 Differential Interference Contrast Microscope equipped with a Leica Flexacam C1 Camera, and a JEOL JSM-6010LA Scanning Electron Microscope. Position of the specimen on the slide was recorded using an England Finder graticule (Pyser Optics, Edenbridge, England). Slides were housed in the collection of the Hobetsu Museum, Mukawa town, Japan. We follow nomenclatural and classification systems revised by Wiggins (1976) for the oculate group, and the latest taxonomic modifications and new combinations proposed by Braman (2013) for the triprojectate group. Species rejected and junior synonyms follow Braman (2013); we further consider Aquilapollenites conatus nipponicus Miki, 1977 and Wodehouseia parva Miki, 1977 reported from the Hakobuchi Formation (Miki, 1977) as nomina nuda because of the lack of any description or illustration. Aquilapollenites miyajiense (Takahashi and Shimono) Braman, 2013, Integricorpus kokufuense (Takahashi and Shimono) Braman, 2001, Parviprojectus triauritus (Takahashi) Braman, 2013, Triprojectus nemuroensis (Takahashi, 1991a) Braman, 2013, Triprojectus proprius (Takahashi and Shimono) Braman, 2013, Scollardia nortoni Srivastava, 1966 are listed but were considered as uncertain identifications by Braman (2013) and Srivastava and Braman (2013). Species reported in open nomenclature are listed as their original genus.
After the revision, taxa from Japanese strata include 16 genera and 86 triprojectate species, and one genus and five oculate species (Figure 2, Appendix 1), with 17 species endemic to Japan. Moreover, 15 genera and 60 triprojectate species and one genus and four oculate species have a stratigraphic significance (Figure 2).
Figure 2.
Summary of the stratigraphic distribution of triprojectate and oculate pollen record of Japan. Pollen grains illustrated in related reports are indicated with a star, white in case of grains identifiable on the picture, or black in case of grains poorly recognizable on the picture because of a poor state of preservation and/or badly oriented and/or with a picture in a low resolution or bad quality. Abbreviations: Con., Coniacian; Camp., Campanian; Maastr., Maastrichtian; Fm, Formation.

Figure 3.
Triprojectate pollen obtained from the Hakobuchi Formation, observed under the Differential Interference Contrast Microscope; slide number, and position of pollen using an England Finder, are indicated in brackets. A, Integricorpus kokufuense (equatorial view, J25Db, T59); B, Pseudoaquilapollenites melior (equatorial view, J29Db, J66/2); C, Pseudoaquilapollenites melioratus (equatorial view, J25Dc, X5/1); D, E, Parviprojectus reticulatus (D, equatorial view, J25Db, T65/1; E, polar view, J12a, S23/1); F, G, Orbiculapollis globosus (F, equatorial view, J2a, R47/2; G, polar view, J12a, D38/3); H, Reticorpus delicatus (equatorial view, J25Db, L66/2); I, Triprojectus attenuatus (equatorial view, J25Db, Z62/2). Scale bar, 10 µm.

Results
Well-preserved palynomorphs were obtained from all seven samples of the Hakobuchi Formation, with the best state of preservation observed in jackets J2, J12, and J25. Among them, we could identify six genera and 15 species of triprojectate pollen that we describe below. Pollen of genus Triprojectus is most abundant and diversified with eight species: Triprojectus attenuatus (Funkhouser) Braman, 2013 (Figures 3I, 5E), T. blandus Braman, 2013 (Figures 4A, 5C), T. elegans (Zhao) Braman, 2013 (Figure 4B), T. granatus (Zhou) Braman, 2013 (Figure 4C), T. hakobuchiensis (Sato) Braman, 2013 (Figures 4D, 5I), T. miser (Takahashi) Braman, 2013 (Figure 5D), T. normalis (Takahashi and Shimono) Braman, 2013 (Figures 4E, 5B), and T. turbitus (Tschudy and Leopold) Braman, 2013 (Figure 4F). Genus Parviprojectus is represented by P. reticulatus Mtchedlishvili, 1961 in Samoilovitch and Mtchedlishvili (1961) (Figure 3D, E). Pseudoaquilapollenites is represented by the three species Ps. melior (Takahashi and Shimono) Braman, 2013 (Figures 3B, 5G), Ps. melioratus (Takahashi) Braman, 2013 (Figure 3C) and Ps. mirus (Takahashi) Braman, 2013 (Figure 5H). Integricorpus kokufuense (Figures 3A, 5A), Orbiculapollis globosus (Chlonova) Chlonova, 1961 (Figure 3F, G) and Reticorpus delicatus (Stanley) Braman, 2013 (Figures 3H, 5F) are also present.
Figure 4.
Triprojectate pollen obtained from the Hakobuchi Formation, observed under the Differential Interference Contrast Microscope; slide number, and position of pollen using an England Finder, are indicated in brackets. A, Triprojectus blandus (equatorial view, J25Db, M67/2); B, Triprojectus elegans (equatorial view, J24Db, O70/1); C, Triprojectus granatus (equatorial view, J25Db, X63); D, Triprojectus hakobuchiensis (polar view, J24Db, D54/2); E, Triprojectus normalis (equatorial view, J25Db, S68/4); F, Triprojectus turbitus (equatorial view, J25Db, G33). Scale bar, 10 µm.

Systematic descriptions
Genus Integricorpus Mtchedlishvili in Samoilovitch and Mtchedlishvili (1961) emend. Braman, 2013
Type species.—Integricorpus bellum Mtchedlishvili in Samoilovitch and Mtchedlishvili, 1961.
Integricorpus kokufuense (Takahashi and Shimono)
Braman, 2001
Figures 3A, 5A
Occurrence.—J2, J12, J25D (few; six specimens).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Pole broad with rounded apex. Equatorial projections triangular in equatorial view. Three long narrow meridional colpi across equatorial projections, reaching the polar regions. Exine fissure surrounding equatorially central body and projections in their middle part. Ornamentation of central body reticulate, the reticulum becoming finer and striate along the equatorial exine fissure; equatorial projections smooth to finely punctate. Polar axis: 30–34 µm; equatorial axis: 25–33 µm. Exine: 0.5–1 µm.
Distribution.—Integricorpus kokufuense is only reported from the Miyadani-gawa Formation of Central Japan (Takahashi and Shimono, 1982).
Figure 5.
Triprojectate pollen obtained from jacket J25D of the Hakobuchi Formation, observed under the Scanning Electron Microscope. A, Integricorpus kokufuense; B, Triprojectus normalis; C, Triprojectus blandus; D, Triprojectus miser; E, Triprojectus attenuatus; F, Reticorpus delicatus; G, Pseudoaquilapollenites melior; H, Pseudoaquilapollenites mirus; I, Triprojectus hakobuchiensis. Scale bar, 10 µm.

Genus Orbiculapollis Chlonova, 1961
Type species.—Orbiculapollis globosus (Chlonova) Chlonova, 1961.
Orbiculapollis globosus (Chlonova) Chlonova, 1961
Figure 3F, G
Occurrence.—J2 (rare), J12 (few) (seven specimens).
Description.—Isopolar pollen grain with three equatorially situated projections. In polar view, polar body subrounded, with equatorial projections very short of a triangular shape. In equatorial view, apical projections rounded with their base extending half of the length of the grain. Polar axis: 18–20 µm; equatorial axis: 21–24 µm. Exine thin, psilate, 1 µm.
Distribution.—This species is reported worldwide from the late Campanian to Eocene (Braman, 2013). It ranges from the Maastrichtian to Paleocene in Japan, and is reported from the Hakobuchi Formation (Takahashi, 1964 as “Trivestibulopollenites sp.”; Takahashi, 1970), the Hamanaka, Oborogawa, Akkeshi formations (Takahashi and Ueda, 1990; Takahashi, 1991a), the Tokotan Formation (Takahashi, 1991b), and the Katsuhira Formation (Takahashi and Yamanoi, 1992) of Hokkaido. It is also reported from the Omichidani Formation of Central Japan (Takahashi, 1991d).
Genus Parviprojectus Mtchedlishvili in Samoilovitch and Mtchedlishvili emend Braman, 2013
Type species.—Parviprojectus reticulatus Mtchedlishvili in Samoilovitch and Mtchedlishvili, 1961.
Parviprojectus reticulatus Mtchedlishvili in Samoilovitch and Mtchedlishvili, 1961
Figure 3D, E
Occurrence.—J2, J25D (few; five specimens).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Pole broad with rounded to conical apex. Equatorial projections triangular in equatorial view. Three long narrow meridional colpi across equatorial projections, reaching the polar regions. Ornamentation of central body reticulate, in some specimens striate in polar regions; equatorial projections smooth to finely punctate. Exine thickening between the poles and the equatorial projections; exine thinner at the extremity of equatorial projections. Polar axis: 28–47 µm; equatorial axis: 27–35 µm. Exine: 0.5 µm.
Distribution.—This species is reported worldwide from the late Campanian to late Eocene (Braman, 2013), and has been reported in Japan from the Campanian to Maastrichtian of the Hakobuchi Formation (Miki, 1977). It is also reported from the Miyadani-gawa Formation (Takahashi and Shimono, 1982).
Pseudoaquilapollenites melior (Takahashi and
Shimono) Braman, 2013
Figures 3B, 5G
Occurrence.—J12 (rare), J25D (few), J29D (rare) (four specimens).
Description.—Subisopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Pole with conical apex. Equatorial projections broad rounded. Colpi extending full length of equatorial projections and for a short distance on polar projections. Ornamentation of central body and equatorial projections finely striate; striae branched arranged polewards. Polar axis: 29–33 µm; equatorial axis: 27–32 µm. Exine: 0.5–1 µm.
Distribution.—Pseudoaquilapollenites melior is only known from Japan, reported from the middle Maastrichtian upper Akkeshi Formation at Ochiishi Bay (Takahashi, 1991a) and the Paleocene (possibly Danian; Naruse et al., 2000) Tokotan Formation (Takahashi and Ueda, 1990). In the Akkeshi Formation, Ps. melior is obtained possibly from the Danian because the first appearance of this species well above the stratigraphic ranges of “lower Maastrichtian” ammonoid Gaudryceras hamanakense and Pachydiscus flexuosus, and inoceramid Sphenoceramus hetonaianus (Matsumoto et al., 1979; Matsumoto and Yoshida, 1979; Naruse et al., 2000). It is also reported from the Miyadani-gawa (Takahashi and Shimono, 1982) and Omichidani (Takahashi, 1991d) formations of Central Japan.
Pseudoaquilapollenites melioratus (Takahashi) Braman, 2013
Figure 3C
Occurrence.—J25D (rare; one specimen).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Pole with conical apex. Equatorial projections broad rounded. Exine between the poles and the equatorial projections thickened. Ornamentation of central body and equatorial projections finely striate; striae branched arranged polewards. Polar axis: 20 µm; equatorial axis: 23 µm. Exine: 0.5 µm.
Distribution.—Pseudoaquilapollenites melioratus is only reported from Asia (Zhou, 1986). In Japan, it is known from the Maastrichtian Akkeshi Formation (Takahashi and Ueda, 1990; Takahashi, 1991a) and the Danian of the Katsuhira Formation of Hokkaido (Takahashi and Yamanoi, 1992). It is also reported from the Miyadani-gawa Formation of Central Japan (Takahashi and Shimono, 1982).
Pseudoaquilapollenites mirus (Takahashi) Braman, 2013
Figure 5H
Occurrence.—J25D (rare; two specimens).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Central body cylindrical with rounded polar apex. Equatorial projections short with a broad base and rounded apex, triangular in equatorial view. Colpi extending full length of equatorial projections and for a short distance on polar projections. Ornamentation of central body and equatorial projections finely striate; striae branched arranged polewards. Polar axis: 25–28 µm; equatorial axis: 25–26 µm. Exine: 0.5 µm.
Distribution.—Pseudoaquilapollenites mirus is only known from Japan, reported from the Maastrichtian to Danian of the Katsuhira Formation of Hokkaido (Takahashi and Yamanoi, 1992). It is also reported from the Miyadani-gawa Formation of Central Japan (Takahashi and Shimono, 1982).
Genus Reticorpus (Krutzsch) Braman, 2013
Type species.—Reticorpus delicatus (Stanley) Braman, 2013.
Reticorpus delicatus (Stanley) Braman, 2013
Figures 3H, 5F
Occurrence.—J2 (common), J12 (few), J25D (few), J27-10 (few), J29D (rare) (26 specimens).
Description.—Anisopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. In equatorial view, equatorial projections and major polar projection of approximately equal size (around 18 µm in length and 12 µm in width), with rounded apex. Equatorial projections slightly inclined toward minor polar projection. Minor polar projection short, protruding very slightly. Exine between the poles and the equatorial projections thickened. Ornamentation of polar projections reticulate; on the major polar projection, reticulate finer toward the apex until becoming psilate on the apex. Ornamentation of equatorial projections scabrate; exine thinner at the apex of equatorial projections. Polar axis: 22–30 µm; equatorial axis: 35–43 µm. Exine: 0.5 µm.
Distribution.—This species is reported worldwide in the Maastrichtian (Braman, 2013), known in Japan from the Omichidani Formation (Takahashi, 1991d) and the Asuwa Formation (Sazawa et al., 2020).
Genus Triprojectus Mtchedlishvili in Samoilovitch and
Mtchedlishvili, 1961
Type species.—Triprojectus dispositus Mtchedlishvili in Samoilovitch and Mtchedlishvili, 1961.
Triprojectus attenuatus (Funkhouser) Braman, 2013
Figures 3I, 5E
Occurrence.—J2 (common), J12 (few), J24D (few), J25D (common), J26-4 (few), J27-10 (few), J29D (few) (36 specimens).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Polar projections short with apex rounded. Equatorial projections broad, wider and longer than the polar projections; exine thinner at the apex of equatorial projections. Exine between the poles and the equatorial projections thickened (width: 2–4 µm). Surface punctate, with punctuations of a regular size (around 1 µm in diameter) uniformly separated. Spinae (size up to 4 µm long and 3 µm wide) present on apices of polar and equatorial projections, and in a band along the equatorial axis widening in the central part of the grain; spinae of the equatorial projections oriented towards the polar axis. Polar axis: 33–55 µm; equatorial axis: 45–75 µm. Exine: 1–1.5 µm.
Distribution.—This species is reported worldwide from the Campanian to Paleocene (Braman, 2013), and has been reported in Japan from the Campanian to Maastrichtian of the Hakobuchi Formation (Takahashi, 1964, 1970; Miki, 1977) and the Paleocene Kiritappu Formation of Hokkaido (Takahashi, 1991c). It is also reported from the Omichidani (Takahashi, 1991d) and Asuwa (Sazawa et al., 2020) formations of Central Japan.
Triprojectus blandus Braman, 2013
Figures 4A, 5C
Occurrence.—J2, J25D (rare; two specimens).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Polar projections cylindrical with sides straight to slightly concave and apex rounded. Equatorial projections short, broad at the base, with rounded to truncated apex. Exine thickened extending from a short distance along polar projections to the 2/3 length of equatorial projections (width: 1 µm). Ornamentation granulate on equatorial projections and equatorial portion of polar body; polar projections reticulate, with psilate apex. Polar axis: 32–39 µm; equatorial axis: 23–42 µm. Exine: 0.5 µm.
Distribution.—Triprojectus blandus is reported only from the late Campanian of the Kanguk Formation in Ellef Ringnes Island, Canadian Arctic Islands (Braman, 2013), although its exact distribution is not described. This study represents the first report from Japan.
Triprojectus elegans (Zhao) Braman, 2013
Figure 4B
Occurrence.—J2 (rare), J24D (rare), J25D (few) (four specimens).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Equatorial view cross-shaped. Exine between the poles and the equatorial projections thickened (width: 1 µm). Equatorial and polar projections of approximately equal size (around 14 µm in length and 9 µm in width). Polar body cylindrical with rounded apices. Equatorial projections straight to slightly concave-sided. Ornamentation granulate to spinate; exine thinner at the apex of equatorial projections. Polar axis: 33–43 µm; equatorial axis: 29–39 µm. Exine: 0.5–1 µm.
Distribution.—Triprojectus elegans is only reported from the Maastrichtian of Far East Russia (Bugdaeva, 2001) and the Mingshui Formation of the Songliao Basin, North East China (Zhao, 1987; Gao et al., 1999; Song et al., 1999), but detailed stratigraphic position is not described. The Mingshui Formation is assigned to the Maastrichtian by magnetostratigraphic and radiometric dating (Scott et al., 2012; Wan et al., 2013). This study represents its first report from Japan.
Triprojectus granatus (Zhou) Braman, 2013
Figure 4C
Occurrence.—J2 (few), J25D (rare), J27-10 (rare) (four specimens).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Equatorial view oblate to diamond-shaped. Exine between the poles and the equatorial projections thickened (width: 2 µm), straight to slightly concave/convex. Polar projections rounded. Equatorial projections short; colpi extending full length of equatorial projections and for a short distance on polar projections. Ornamentation of central body and equatorial projections densely granulate (grana 0.5–1 µm in diameter). Polar axis: 26–33 µm; equatorial axis: 25–27 µm. Exine: 1–2 µm.
Distribution.—Triprojectus granatus is only reported from the Maastrichtian of Jiangsu, China (Zhou et al., 2009). This study represents its first report from Japan.
Triprojectus hakobuchiensis (Sato) Braman, 2013
Figures 4D, 5I
Occurrence.—J2 (few), J24D (few), J25D (common), J27-10 (few) (20 specimens).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. In equatorial view, polar projections conical with rounded apex; equatorial projections with straight sides and apex rounded. In polar view, triangular-shaped with straight to slightly convex sides, and relatively long and narrow extremities. Short narrow meridional colpi across the apex of equatorial projections. Exine between the poles and the equatorial projections thickened, then exine thinner from the middle to extremities of equatorial projections. Ornamentation finely reticulate, slightly granulate around the apex of equatorial projections. Polar axis: 24–35 µm; equatorial axis: 29–39 µm. Exine: 0.5–1 µm.
Distribution.—Triprojectus hakobuchiensis is only reported from the Campanian Omagari Formation and the Campanian-Maastrichtian Hakobuchi Formation (Sato, 1961; Takahashi, 1967; Miki, 1977), and the Paleocene Tokotan Formation (Takahashi, 1991b) of Hokkaido.
Triprojectus miser (Takahashi) Braman, 2013
Figure 5D
Occurrence.—J25D (rare; one specimen).
Description.—Small isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Polar projections poorly developped, with rounded to tapered apex. Equatorial projections well-developped, with broad base and rounded apex. Colpi short narrow across the apex of equatorial projections. Ornamentation smooth to finely punctate; apex of polar projections smooth. Polar axis: 27 µm; equatorial axis: 29 µm. Exine: 1–1.5 µm.
Distribution.—Triprojectus miser is only reported from the Maastrichtian Akkeshi (Takahashi, 1991a) and Danian of the Katsuhira (Takahashi and Yamanoi, 1992) formations of Hokkaido. It is also reported from the Miyadani-gawa (Takahashi and Shimono, 1982) and Omichidani (Takahashi, 1991d) formations of Central Japan.
Triprojectus normalis (Takahashi and Shimono)
Braman, 2013
Figures 4E, 5B
Occurrence.—J2 (abundant), J12 (few), J24D (few), J25D (common), J26-4 (rare), J27-10 (common), J29D (few) (56 specimens).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Polar projections poorly developed, with rounded apex. Equatorial projections broad, short. Small thickened exine areas at the corner between the polar and equatorial projections (width: 2.5 µm). Colpi short narrow across the apex of equatorial projections. Ornamentation punctate to granulate; apex of polar projections punctate to psilate; on equatorial projections, prominent spinae oriented towards the polar axis, becoming larger towards apices (maximum length: 3.5 µm; width: 2.5 µm). Polar axis: 21–35 µm; equatorial axis: 24–42 µm. Exine: 1–1.5 µm.
Distribution.—This species is reported from the Campanian to Maastrichtian of Far East Russia (e.g. Markevich et al., 1994) and the Kuril Islands (Markevich et al., 2012), Helongjiang, China (Markevich et al., 2011), and Japan, from the Maastrichtian Hamanaka, Oborogawa and Akkeshi formations (Takahashi and Ueda, 1990; Takahashi, 1991a), and Danian of the Katsuhira Formation (Takahashi and Yamanoi, 1992). It is also reported from the Miyadani-gawa (Takahashi and Shimono, 1982) and Omichidani (Takahashi, 1991d) formations of Central Japan.
Figure 6.
Stratigraphic distribution of triprojectate and oculate pollen species of Japan. Revised from Sato (1961), Takahashi (1964, 1965, 1970, 1980, 1991a, b, c, d), Shimada (1967), Miki (1972, 1977), Tanai et al. (1978), Takahashi and Shimono (1982), Takahashi and Sugiyama (1990), Takahashi and Ueda (1990), Takahashi and Yamanoi (1992), Tanaka and Hirano (2008), Nichols et al. (2010), Sazawa et al. (2020). Species only reported from Japan are written in bold. Inoceramid and ammonoid zones are mainly based on Toshimitsu et al. (1995). Turonian to lower Campanian inoceramid biozones are based on Hayakawa and Hirano (2013). U–Pb ages are from Shigeta et al. (2017a, b).

Triprojectus turbitus (Tschudy and Leopold) Braman, 2013
Figure 4F
Occurrence.—J12 (rare), J25D (few), J27-10 (few) (five specimens).
Description.—Isopolar pollen grain with three equatorially situated projections, and one polar projection on each apocolpium. Equatorial view cross-shaped. Equatorial and polar projections of approximately equal size (length: 14–15 µm; width: 12 µm). Polar projections conical with apex rounded. Exine thickened extending from a short distance along polar projections to the 2/3 length of equatorial projections (width: 1.5–2 µm). Ornamentation granulate to spinate; spinae small on polar body, larger and oriented towards the polar axis at the apex of equatorial projections; apex of polar projections granulate to psilate. Exine thinner at the apex of equatorial projections. Polar axis: 30–33 µm; equatorial axis: 30–35 µm. Exine: 0.5–1 µm.
Distribution.—Triprojectus turbitus is mainly reported from the Campanian to Maastrichtian of North America (e.g. Tschudy and Leopold, 1971; Pearson et al., 2001) and Canada (e.g. Evans et al., 2012; Srivastava and Braman, 2013), and has been reported in Asia only from Central East Russia (Hofmann and Zetter, 2007; Hofmann et al., 2008) and Japan, from the Danian of the Katsuhira Formation (Takahashi and Yamanoi, 1992) of Hokkaido. It is also reported from the Omichidani Formation of Central Japan (Takahashi, 1991d). Triprojectus cf. turbitus occurs in the Campanian of the Hakobuchi Formation (Miki, 1977).
Discussion
Appearance and diversification of triprojectate and oculate pollen in Japan.—The oldest triprojectate report in Japan is represented by Cranwellia sp. from the Turonian Tenkaritoge Formation of the Yezo Group (Tanaka and Hirano, 2008). Triprojectate pollen slightly increases during the Coniacian to Santonian, with the endemic Pentapollenites yezoensis Takahashi, 1964 reported from the late Coniacian Kasamatsu Formation of the Futaba Group (Takahashi, 1964), and Accuratipollis evanidus Chlonova, 1961, Aquilapollenites quadrilobus Rouse emend. Srivastava and Rouse, 1970, and Parviprojectus rigidus (Tschudy and Leopold) Braman, 2013 reported from the Coniacian Nishichirashinai Formation of the Yezo Group (Miki, 1977; Tanaka and Hirano, 2008). Only Accuratipollis enodatus Chlonova, 1961 newly appears from the Santonian and characterizes it; it is also reported from the Uge Member of the Taneichi Formation (Takahashi and Sugiyama, 1990) (Figure 6).
All above species, excepting Accuratipollis enodatus, are still present in the Campanian, further accompanied by Cranwellia rumseyensis Srivastava, 1966, Parviprojectus reticulatus, Pseudoaquilapollenites pachypolus (Martin) Braman, 2013, Triprojectus attenuatus, T. rectus (Tschudy) Braman, 2013, T. turbidus (Tschudy and Leopold) Braman, 2013, and the Japanese endemic species Parviprojectus borealis, P. triauritus (Takahashi) Braman, 2013, and Triprojectus hakobuchiensis in the Omagari, Osoushinai and Hakobuchi formations (Miki, 1977; Tanaka and Hirano, 2008).
Triprojectate and oculate groups drastically increase in diversity and abundance during the Maastrichtian, with 30 new species, while Pentapollenites yezoensis and Parviprojectus triauritus disappear. Triprojectate genera Bratzevaea, Fibulapollis, Integricorpus, Laevicorpus, Orbiculapollis, Reticorpus, and oculate genus Wodehouseia appear during the Maastrichtian (Figure 6).
Ten of the 41 triprojectate and oculate species reported from the Maastrichtian of Japan disappear during this period, while only seven new triprojectate species are reported from the Paleocene, including the new genera Scollardia and Mancicorpus respectively in the Tokotan (Takahashi and Ueda, 1990; Takahashi, 1991a) and Katsuhira (Takahashi and Yamanoi, 1992) formations.
In the Turonian to Danian distribution interval of triprojectate and oculate pollen in Japan, age diagnostic species for within one period appear to be few until the Campanian: none for the Turonian and Coniacian, Accuratipollis enodatus for the Santonian, P. triauritus for the Campanian.
On the other hand, six species are distributed in the Maastrichtian only, and seven species characterize the Danian (Figure 6).
Correlation of distributions around the Circum Pacific region.—During the Late Cretaceous, an epeiric sea separated North America into a Cordillera and the Western Interior, and it has been demonstrated that the Beringian isthmus, which connected Alaska and northeast Siberia since the mid-Cretaceous, permitted the geographic expansion of some floristic components, such as the triprojectate and oculate pollen-producing plants (Hofmann and Zetter, 2007). A provincialism and difference in the distribution of species may however have possibly occurred between the eastern and western sides of the Pacific region. Late Cretaceous pollen species reported from Japan are classified into three types in terms of their distributions (Figure 6): i.e., 1) worldwide distribution (Figure 6: a), 2) Asian distribution (Figure 6: b), 3) disjunct distribution between Japan and North America (Canada and United States) (Figure 6: c). For species only distributed in Asia, it can be noted a quite similar stratigraphic distribution between Japan and the continent. However, species only distributed in the United States and Canada outside Japan generally appear earlier in the United States/Canada (Figure 6). Provincialism of these plant groups is consistent with a westward expansion of floras via the Beringian isthmus in the Circum Pacific region during the Late Cretaceous (Graham, 2018). Similar westward dispersal is also known for some plant-eating animals, such as hadrosaurs, including K. japonicus and its relatives in Asia (Kobayashi et al., 2019).
Wodehouseia spinata, considered as a stratigraphic marker for the late Maastrichtian (Nichols and Johnson, 2008), appears in Japan from the Maastrichtian in the Hakobuchi Formation of the Yubari area (Miki, 1977), which is slightly younger than the K. japonicus-bearing bed of the Hobetsu area (Kobayashi et al., 2019), and in the Katsuhira Formation (Takahashi and Yamanoi, 1992). First occurrences (FOs) of W. spinata was ca. 69.2–68.4 Ma within Chron 31n in the Edmonton Group (Srivastava and Braman, 2013), and ca. 70.5 Ma in the orbitally-tuned Mingshui Formation of China (Wu et al., 2014; Yoshino et al., 2017), i.e., ca. 1 Myr earlier than in Canada, maybe due to uncertainty of pollen fossil records and/or dispersal of W. spinata from Asia to Canada. In Canada, FO of W. spinata is only a single specimen found within the Carbon-Thompson coal interval in the Whitemud Formation, to the southeast corner of Saskatchewan (Binda et al., 1991). This species becomes abundant ca. 67 Ma in the Scollard Formation, upper part of the Edmonton Group (e.g. Srivastava and Braman, 2013). Considering the paleobiogeographic distribution, the appearance of W. spinata in Japan might be close to that in China.
We can guess that further successive palynological studies in other marine sections of the Yezo Group well dated from radiometric ages, magnetostratigraphy and index fossils, such as ammonoids and inoceramids, would provide additional age constraints for palynostratigraphy and plant biogeography, based on accurate correlations. In particular, because a palynological turnover is evident in East Asia across the Campanian–Maastrichtian cooling event, further high-resolution chronostratigraphic work is necessary to understand the botanical response at this period.
Comparison of our new data with previous ones on the Hakobuchi Formation.—Seventeen species of triprojectate and oculate pollen were previously reported from the Hakobuchi Formation (Sato, 1961; Takahashi, 1964, 1965, 1967, 1970; Shimada, 1967; Miki, 1977). Among the 15 species of triprojectate pollen described in this study, Orbiculapollis globosus (Takahashi, 1964), Parviprojectus reticulatus (Miki, 1977), Triprojectus attenuatus (Takahashi, 1964, 1970; Miki, 1977), T. hakobuchiensis (Sato, 1961; Takahashi, 1967; Miki, 1977) and T. cf. turbitus (Miki, 1977) were previously reported from the Hakobuchi Formation. They were noted as rare or few in the formation, excepted T. hakobuchiensis reported as common, in accordance with our results; we however also observed T. attenuatus as common in some samples. Triprojectus normalis is the most represented species in our assemblages and the only one that could be noted as abundant (more than 10% of the total assemblage), while it was not reported from the Hakobuchi Formation in previous studies.
Pseudoaquilapollenites melior, Ps. melioratus, Ps. mirus, Triprojectus miser and T. normalis are reported from the Nemuro Group (Takahashi and Ueda, 1990; Takahashi, 1991a) and/or the Katsuhira Formation (Takahashi and Yamanoi, 1992) of Hokkaido. Integricorpus kokufuense and Reticorpus delicatus were previously reported from Central Japan (Takahashi and Shimono, 1982; Takahashi, 1991d; Sazawa et al., 2020) but are firstly found in Hokkaido, while Triprojectus blandus, T. elegans, and T. granatus are firstly reported from Japan. All those species, excepting T. blandus, were only reported from Japan, China or Russia, indicating a distribution in Asia wider than previously thought. In particular, T. normalis and R. delicatus are abundant and noted as dominant elements in some samples from the Hakobuchi Formation.
Geographical and stratigraphical distribution of pollen species obtained from the K. japonicus bone bed.—Among identified pollen species from the K. japonicus-bearing bone bed, we found cosmopolitan species (Orbiculapollis globosus, Parviprojectus reticulatus, Reticorpus delicatus, Triprojectus attenuatus) along with species mainly represented in Canada and North America (Triprojectus turbitus). These species only co-occur in the Maastrichtian based on reliable indices such as radiometric dating, magnetostratigraphy, and ammonite biostratigraphy (e.g. Eberth and Deino, 2005; Cobban et al., 2006). All other species are distributed mainly or exclusively in Asia (Figure 6). Triprojectus blandus, T. elegans and T. granatus have never been found in Japanese strata until this study, while Integricorpus kokufuense, Pseudoaquilapollenites melior, Ps. melioratus, Ps. mirus, Triprojectus hakobuchiensis and T. miser seem to be endemic to Japan. Among taxa with an Asian distribution and stratigraphic significance, only T. hakobuchiensis is reported from the Campanian and Maastrichtian, while Ps. melior, Ps. melioratus, Ps. mirus, T. elegans and T. granatus have their range restricted from the Maastrichtian.
Miki (1977) suggested a change in spore and pollen assemblages across the Campanian/Maastrichtian boundary in northern Japan, however, the detailed stratigraphic position and their relation with molluscan biostratigraphy across the Campanian/Maastrichtian is not well constrained and needs to be confirmed. The palynofloral assemblage described from the Hakobuchi Formation in this study does not include species defined by Miki (1977) as definitively Campanian, but only species previously reported from the Campanian–Danian, Maastrichtian, Maastrichtian–Danian, or Danian. In the Hakobuchi Formation, Parviprojectus reticulatus, Triprojectus attenuatus and T. hakobuchiensis were previously reported across the Campanian–Maastrichtian (Sato, 1961; Takahashi, 1964, 1965, 1967; Shimada, 1967; Miki, 1977), and Orbiculapollis globosus from the Maastrichtian (Takahashi, 1964). In northern Japan, T. attenuatus is reported from the Campanian–Danian; T. hakobuchiensis and P. reticulatus from the Campanian–Maastrichtian; Ps. melioratus from the Maastrichtian; T. miser, T. normalis, Ps. melior, Ps. mirus, and O. globosus from the Maastrichtian–Danian; T. turbitus from the Danian (Figure 2). The triprojectate pollen assemblage obtained from the hadrosaur Kamuysaurus japonicus-bearing bone bed of the Hakobuchi Formation then appears consistent with the early Maastrichtian age previously proposed for the bone-bed by Kobayashi et al. (2019) on the basis of co-occurred ammonite Pachydiscus (Neodesmoceras) japonicus.
Conclusion
We revised records of triprojectate and oculate pollen from Japan based on recent taxonomical updates of these groups: 16 genera and 86 species for the triprojectate group, and one genus and five species for the oculate group. Among them, 17 species are endemic to Japan. The record of the triprojectate and oculate groups in Japan extends from the Turonian to Paleocene, being most diversified during the Maastrichtian, and confirms age diagnostic species. Age ranges of Asian-endemic species are almost the same between continental Asia and Japan, while pollen species distributed disjunctly in Japan and North America tend to occur earlier in North America. This tendency implies a westward expansion of floras around the Circum Pacific region via the Beringian isthmus during the Late Cretaceous.
The triprojectate pollen assemblage obtained from the Kamuysaurus japonicus-bearing bone bed of the Hakobuchi Formation consists of six cosmopolitan species associated with nine Asian species. Three species reported from North America, as well as two species reported from Japan and China, have their distribution range well calibrated from cyclostratigraphic, magnetostratigraphic and radiometric data, that support an early Maastrichtian age. We can guess that further successive palynological studies in marine successions of Japan will provide additional age constraints, allowing direct correlation between marine and non-marine strata.
Acknowledgements
We thank the excavation and preparation teams of the Hobetsu Museum and the Hokkaido University Museum for sharing the material. This study was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (19H02012 to MI and 20K04148 to JL). We are very grateful to Toshihiro Yamada and Uxue Villanueva Amadoz for their review and all their fruitful comments that improved the final version of the manuscript. We thank Harufumi Nishida, Chuo University, Akihisa Kitamura and Shinichi Sato, Shizuoka University, for their critical comments; the Museum of Natural and Environmental History, Shizuoka, for supporting equipment for observation of the palynological samples.
© by the Palaeontological Society of Japan