Fossil Evidence of Initial Radiation of Cercidiphyllaceae L

УДК 561.46:551.763 Палеоботаника, 2018, Т. 9, C. 54—75

https://doi.org/10.31111/palaeobotany/2018.9.54 Palaeobotany, 2018, Vol. 9, P. 54—75

FOSSIL EVIDENCE OF INITIAL RADIATION OF CERCIDIPHYLLACEAE L. B. Golovneva, A. A. Zolina

Komarov Botanical Institute RAS, St. Petersburg, [email protected]

Abstract. Cercidiphyllaceae-like leaves and fruits from the Lower Cretaceous deposits of Northeastern Asia were restudied. In the result one species of Jenkinsella fruits and fi ve species of Trochodendroides leaves were recognized, including Trochodendroides potomacensis (Ward) Bell, T. buorensis Golovneva, T. sittensis Golovneva, sp. nov., T. vachrameeviana (Iljinskaja) Golovneva, comb. nov., and T. denticulata (Budantsev et Kiritchkova) Golovneva, comb. nov. Two new combinations and one new species are published. These plants had very small leaves and probably were shrubs. Fruits of Nyssidium orientale Samylina from the Barremian-Aptian Starosuchan Formation (Primorye, Russia) have no follicular characters as Jenkinsella fruits. Their affi nity, not only to Cercidiphyllum-like plants, but to angiosperms in general, is doubtful. Leaves and fruits of Cercidiphyllum sujfunense Krassilov from the lower-middle Albian Galenki Formation (Primorye) also can not be assigned to Cercidiphyllaceae. Leaves have pinnate, brochidodromous venation and are comparable with those of Asiatifolium elegans Sun, Guo et Zheng, which were recorded from the Frentsevka Formation of the Partizansk coal basin, Primorye, Russia, and from the Chengzihe Formation, Northeastern China. Thus, the fi rst reliable records of the genus Trochodendroides appear in the early-middle Albian. The relationship of these leaves with Cercidiphyllaceae is confi rmed by fi nds of associated fruits Jenkinsella fi latovii and by signifi cant diversity of Trochodendroides in the Late Albian-Cenomanian. In the early-middle Albian the genus Trochendroides was a minor component of the conifer-dominated Mesophytic fl oras. These fossils refl ect the early radiation of Cercidiphyllaceae and indicate that this family began to diversify more then 30 million years before the Tertiary. Investigation of the early-middle Albian Cercidiphyllaceae provides important new data for our understanding of the early evolution of eudicots. Keywords: Jenkinsella, Trochodendroides, Cercidiphyllaceae, early eudicots, Lower Cretaceous, North- eastern Asia.

INTRODUCTION The modern family Cercidiphyllaceae contains a single genus Cercidiphyllum with two species: C. japoni- cum Siebold et Zuccarini and C. magnifi cum (Nakai) Nakai, distributed in China and Japan. Both species are deciduous trees which have cordate, palmately veined leaves with crenate margin. Flowers are unisexual and naked. Pistillate fl owers are inicarpellate and borne in clusters (Endress, 1993; Fu, Endress, 2001). Fruits are follicles, containing numerous small winged seeds. The Cercidiphyllaceae have been placed previously in the Hamamelidales (Cronquist, 1981) or treated as a separate order Cercidiphyllales close to Trochodendrales (Takhtajan, 1969; Endress, 1986). Phylo- genetic analyses based on molecular data include the family in Saxifragales (APGIII, 2009). This order is considered as one of the basal lineage of core eudicots, important for understanding of the early evolution of this group (Friis et al., 2011). However, Cercidiphyllaceae experienced an intensive diversifi cation in the past, and its precise phylogenetic position is uncertain. Fossil leaves and reproductive structures that are unequivocally very similar to those of extant Cer- cidiphyllum were fi rst recorded from the Oligocene of North America and Europe (Jähnichen et al., 1980; Manchester, Meyer, 1987; Kovar-Eder at al., 1998). The Cretaceous and Early Tertiary Cercidiphyllum—like leaves are usually assigned to the genus Trochodendroides Berry (Berry, 1922; Crane, 1984, 1989; Golovne- va, Alekseev, 2010; Golovneva et al., 2017). Distinctive follicular fruits that co-occurred with Trochoden- droides leaves have been known for a long time, but early discoveries were considered as belonging to other genera and families (Golovneva, Alekseev, 2017). These fruits were fi rst detected by O. Heer (1869) from the Paleocene deposits of Atanekerdluk in West Greenland, and described as Nyssa arctica Heer. R. W. Brown (1939) fi rst noted the co-occurrence of these follicular fruits with leaves and winged seeds resembling those of extant Cercidiphyllum. Brown assigned all of these remains to single species Cercidiphyl-

54 lum arcticum (Heer) R. W. Brown, although he indicated, that fossil infructescences diff er from those of modern Cercidiphyllum by their racemose organization and some other characters. I. A. Iljinskaja (1974a) and P. R. Crane (1984) suggested using the name Nyssidium Heer for this kind of fruits and this suggestion was widely accepted. The genus Nyssidium was established by Heer (1870) for elongated dispersed fruits from the Paleocene of Spitsbergen. Later these specimens were restudied by Budantsev and Golovneva (2009). The fruits of the type species Nyssidium ekmannii Heer resemble, in a general way, the fruits of Cercidiphyllum-like plants, but they diff er in being twice smaller and without evidence of follicular nature. The fruits of “Nyssa” arctica and other remains of this kind are follicles. They are gradually attenuated at the base into a short stalk and at the apex into a terminal style, have suture grooves, longitudinal or oblique ridges diverging from ventral suture, and transverse striae. The apex and base of Nyssidium fruits are rounded and longitudinal ridges are thinner, more regular and meridional, converging near the base and the top of the fruit. They have no suture grooves and transverse striation. There is no evidence, that Nyssidium had the fruits arranged in a raceme and winged seeds inside. It’s most likely that the similarity of “Nyssa” arctica and Nyssidium ekmanii is only superfi cial. In fact, Nyssidium ekmanii has so few distinctive features (small size, elongated shape and ribbed surfaces) that may be fi t with many systematically diff erent taxa. We believe that Nyssidium corresponds to another type of fruits or, possibly, seeds. The earliest appropriate generic name originally designated for fruits, associated with Trochodendroides leaves, with distinguishable morphology and critical details of in- ner structures is Jenkinsella Reid et Chandler (1933). We proposed to use this name for dispersed follicular fruits, fruits in raceme and infructescences, attached to the shoots (Golovneva, Alekseev, 2017). The genus Jenkinsella was fi rst established for pyritized dispersed fruits and locule casts from the early Eocene London Clay Formation, Great Britain. Subsequently, infructescences, fruits and seeds from the British Early Tertiary were reexamined by Crane (1984). He united branched racemose infructescences previously assigned to Carpolithus gardneri Chandler and fruits Jenkinsella apocynoides Reid et Chandler under the name Nyssidium arcticum (Heer) Iljinskaja. The morphology of fruits was described in detail. Some of them contained winged seeds, similar with those described by Brown. Crane also compared these fructifi cations and associated foliage with those of extant Cercidiphyllum, supposing that these taxa were closely related. The most completely reconstructed Cercidiphyllum-like plant is Joff rea speirsii Crane et Stockey (1985) from the upper Paleocene Paskapoo Formation, Alberta, Canada. The investigation of this species revealed the presence of both long and short shoots and diff erent details of carpels, winged seeds and fruits. Joff rea was interpreted as an extinct representative of Cercidiphyllaceae. Based on this material a more comprehen- sive comparison of all known complete fructifi cation structures and living Cercidiphyllum was undertaken (Crane, Stockey, 1985, 1986). The condensed infl orescences of the modern Cercidiphyllum were hypothe- sized to have evolved from the racemose type seen in Joff rea, accompanied by a change in suture orientation. Staminate racemose infl orescences, associated with Trochodendroides leaves and Joff rea shoots, were described later as a separate genus Alasia Golovneva (2006). These infl orescences represent axes with heli- cally arranged bracts and numerous stamens in their axils. Pollen grains from one specimen were studied by Krassilov and Kodrul (2008). Unlike extant Cercidiphyllum, the pollen grains extracted from the Alasia anthers are small tricolpate with long colpi and a variably microreticulate to verrucate-scabrate ornamenta- tion, whereas Cercidiphyllum pollen grains are triporate. During the Late Cretaceous and Paleocene Trochodendroides, Jenkinsella and Alasia were widespread in middle and high latitudes of the Northern Hemisphere, especially in Northeastern Asia. From the Late Cretaceous of the latter region about 40 species of the genus Trochodendroides were currently described (Golovneva et al., 2008; Golovneva, Alekseev, 2010; Yudova, Golovneva, 2014; Golovneva et al., 2017). Investigation of cuticular features of the Cretaceous Trochodendroides leaves reveals the similarity with those of living Cercidiphyllum (Golovneva, Alekseev, 2010). The earliest occurrences of Trochodendroides and Jenkinsella are known from the early-middle Albian in North America and Northeastern Asia (Golov- neva, Alekseev, 2010, 2017), and the fi rst occurrence of Alasia were recorded from the Turonian-Coniacian deposits of Eastern Siberia (Golovneva, 2006). However, the fossil record of Cercidiphyllaceae from Northeastern Asia, especially from the Early Cre- taceous, is poorly known. In the majority of overviews, this family is not considered among the ancient groups of eudicots and timing of its appearance estimated as the Latest Cretaceous (Friis et al., 2011). In this paper we review the Early Cretaceous occurrences of Cercidiphyllum-like fossils that refl ect the earliest radiation of Cercidiphyllaceae. In the result one species of Jenkinsella and fi ve species

55 of Trochodendroides were recognized, including Trochodendroides potomacensis (Ward) Bell, T. buorensis Golovneva, T. sittensis Golovneva, T. vachrameeviana (Iljinskaja) Golovneva, comb. nov., T. denticulata (Budantsev et Kiritchkova) Golovneva, comb. nov. and Jenkinsella ﬁ latovii (Samylina) Golovneva et P. Alekseev.

MATERIAL AND METHODS In Northeastern Russia leaves of Trochodendroides potomacensis come from two localities: from the early-middle Albian Buor-Kemyus Formation of the Zyryanka River, the Kolyma River basin, North-East of Russia and from the early-middle Albian Khatyryk Formation of the Lepiske River, the Lena River basin, Eastern Siberia (Fig. 1). Fossils from the Zyryanka River were collected by G. G. Popov and V. A. Samylina in 1957 and are stored at the Komarov Botanical Institute RAS (BIN RAS) in St. Petersburg (collection BIN 508). Specimens from the Lepiske River were collected by A. I. Kiritchkova and Yu. L. Slastenov in 1963. Previously, these collections were kept in the All-Russia Petroleum Research Exploration Insti- tute (VNIGRI), but a few years ago they were transferred to the Komarov Botanical Institute (collection BIN(VNIGRI) 707). Leaves of T. buorensis come from the same layers of the Buor-Kemyus Formation at the Zyryanka River as those of T. potomacensis, and also are stored at the collection BIN 508. The specimens of T. sittensis and T. denticulata come from the Khatyryk Formation of the Lena River basin as those of T. potomacensis, but from another locality at the Sitte River, which ﬂ ows into the Lena River opposite the settlement of Sangar (Fig. 1). Leaves of T. vachrameeviana come from the Kyzylshen Formation in Western Kazakhstan (Fig. 1). Specimens were collected by V. A. Vachrameev in the Karachetau locality and are stored in the Geological Institute RAS in Moscow (the collection GIN 3302). The remains of Jenkinsella ﬁ latovii come from the Lower Cretaceous deposits of the Galimyi and Toptan formations, Kolyma River basin, Northeastern Russia. The specimens were collected by geologists L. V. Ievlev and S. I. Filatov in 1961—1963 and are stored at the BIN RAS, collections BIN 510, 511. The remains of Nyssidium orientale Samylina were discovered in the well No. 1847 drilled in the city Partizansk, in the Lower Cretaceous deposits of the Partizansk (previously Suchan) coal basin, Primorye, Far East of Russia (Fig. 1). They are stored at the BIN RAS, the collection BIN 506.

Fig. 1. Locality map: 1 — Kazakhstan, Karachetau, Kyzylshen Formation; 2 — Lena River basin, Lepiske River, Khatyryk Formation; 3 — Lena River basin, Sitte River, Khatyryk Formation; 4 — Kolyma Ri ver basin, Zyryanka River, Buor-Kemyus Formation; 5 — Magadan Region, Omsukchan, Galimyi and Toptan formations; 6 — Primorye, Partizansk, Starosuchan Formation; 7 — Primorye, Konstantinovka, Galenki Formation.

56 Cercidiphyllum sujfunense Krassilov leaves and fruit were recorded from the Razdolnaya (previously Suifun) coal basin, southern Primorye, Far East of Russia. They were found near Konstantinovka village in tuff aceous deposits of the early-middle Albian Galenki Formation (Krassilov, 1967). Material is kept in the Federal Scientifi c Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the Russian Academy of Sciences, in Vladivostok, (previously Institute of Botany and Soil Science, prefi x before collection numbers IBSS). All material is preserved only as impressions, and details of leaf anatomy were impossible to study. Leaf architectural terminology follows that of Manual of Leaf Architecture (Ellis et al., 2009). Photographs of the specimens were performed using Nikon Coolpix P7700 camera at low-angle illumination. Some specimens were photographed in water to increase contrast.

STRATIGRAPHY In the territory of Northeastern Asia the early angiosperms come from the nonmarine deposits of several large coal basins, which usually developed throughout almost all of the Lower Cretaceous. Two large coal basins are located in the North-East of Russia, in the Kolyma River basin: the Zyryanka coal basin and the Omsukchan coal basin. The Zyryanka coal basin is distributed in the middle part of the Kolyma River, in the Zyryanka River basin. Coaliferous deposits of this basin were subdivided into three formations (Popov, 1962): the Ozhogina Formation (Neocomian), the Silyap Formation (Aptian) and the Buor-Kemyus For- mation (lower-middle Albian). This sequence contains industrial-quality coal seams and abundant fossil plants, studied by Prynada (1938) and Samylina (1960, 1964, 1967). First angiosperm fossils appear in the upper Buor-Kemyus Formation. The Ozhogina Formation conformably overlies the Upper Jurassic Bastak and Ilintas formations. The more ancient Ilintas Formation is marine and contains mollusks of late Oxford- early Kimmeridge age. The Buor-Kemyus Formation is about 3000 m thick and consists of conglomerates, sandstones, siltstones and mudstones, with numerous coal layers. It is overlain unconformably by Upper Cretaceous nonmarine deposits of the Vstrechninskaya Formation which is probably Turonian-Coniacian in age (Kryshtofovich, 1938; Herman, 2013). The Buor-Kemyus fl ora includes about 80 species and consists of ferns, ginkgophytes, cycadophytes, czekanowskialeans, and conifers Samylina (1964, 1967). Small-leaved angiosperms are rare, but their diversity is rather high, including about 20 species (Kryshtofovich, 1938; Samylina, 1960). Floras of the Buor-Kemyus type are widely distributed in northeastern Russia. Similar assemblages were found in the Omsukchan coal basin in the upper reaches of the Kolyma River, at the Bol’shoy Anuy, Eropol and Penzhina rivers, and in several other localities (Samylina, 1976). In the Aynakhkurgen and Umkuveem depressions and in the Penzhina River basin, plant-bearing deposits with fl oristic assemblages of the Buor-Kemyus type overlie marine deposits with mollusks of the late Aptian age. The development of the younger Grebenka fl ora with predominance of angiosperms began in the late Albian-Cenomanian, as indicated by marine mollusks found together with the fl oral remains (Herman, 1999). These data confi rm the early-middle Albian age of the Buor-Kemyus fl ora. The Omsukchan coal basin is situated in the upper reaches of the Kolyma River, in the Balygychan- Sugoi interfl uve, the Omsukchan district of the Magadan Region (Fig. 1). The Lower Cretaceous terrig- enous and volcanogenous deposits of this basin were fi rstly attributed to the Omsukchan Group, which was later divided into four formations: the Ulyky Formation, the Galimyi Formation, the Aigur Formation and the Toptan Formation (Filatov, 1972; Shczepetov, 1995). Floristic assemblages from the Galimyi, Aigur and Toptan formations were proposed to combine into the Sugoi fl ora, which has signifi cant similarity with the Buor-Kemyus fl ora of the Zyryanka coal basin (Golovneva et al., 2017). Its age was also estimated to be early to middle Albian (Samylina, 1976). Angiosperms from the upper part of the Omsukchan group were described by Samylina (1968, 1976). The terrestrial Cretaceous sediments with subordinate marine or brackish deposits are also widely distributed in Primorye, Far East of Russia. There are two large coal basins in the southern part of this region: the Partizansk (previously Suchan) and the Razdolnaya (previously Suifun) coal basins. The Partizansk basin is situated along the Partizanskaya (previously Suchan) River valley at a distance of about 120 km. The main industrial deposits are located near Partizansk city. The coal-bearing Lower Cretaceous deposits were combined in the Suchan Group, which lie on the Proterozoic gabbroic rocks or on the Klyuchi Formation and are conformably overlain by the volcaniclas- tic Korkino Group (Bugdaeva et al., 2014). The Klyuchi Formation records shallow-marine to nonmarine environments with buchiid bivalves and plants of the Valanginian age (Markevich et al., 2000). The sedi-

57 ments of the Korkino Group contain only few fossil plants (Volynets, 2005) and its age is inferred as the late Albian—early Cenomanian. The coal-bearing deposits of the Suchan Group yielded numerous fossil plants, which were studied by V. A. Krassilov (1967). According to Likht (1961, 1994) and Krassilov (1967) the Suchan Group consists of the Starosuchan, the Severosuchan and the Frentsevka formations. Now the ages of stratigraphic divisions of the Suchan Group are intensely debated. This is connected mostly with problems in recognition and correlation of formation boundaries. On the basis of plant megafossils and palynological data, the age of the Starosuchan Formation was estimated as the Hauterivian-early Aptian or the Barremian—early Aptian (Krassilov, 1967; Resheniya…, 1994; Markevich et al., 2000; Volynets, 2005), and the age of the Severosuchan Formation as the late Aptian or late Aptian-early Albian. The Frentsevka Formation includes marine Trigonia bed in the bottom, which was dated as middle Albian (Markevich et al., 2000). Rare angiosperm pollen grains were recorded from all strata of the Suchan Group (Markevich, 1995). Samylina (1961) described the fruits of Nyssidium orientale from the Starosuchan Formation. Leaves of Araliaephyllum luciferum (Kryshtofovich) Golovneva come from the upper part of Severosuchan Forma- tion (Kryshtofovich, 1929; Golovneva, 2018). The Frentsevka Formation includes more diverse assemblages of small-leaved angiosperms, described by Krassilov (1967). According to Krassilov (1967) the Lower Cretaceous deposits of the Razdolnaya coal basin (the Nikan Group) are divided into the Ussuriysk Formation (Barremian), the Lipovtsy Formation (Aptian) and the Galenki Formation (early-middle Albian). Angiosperms were recorded from the Lipovtsy and Galenki formations (Kryshtofovich, 1929; Krassilov, 1967; Volynets, Bugdaeva, 2017). In Eastern Siberia the Lower Cretaceous deposits are distributed in the Lena-Vilyuy depression (Fig. 1). This is a large basin of non-marine sedimentation, where an almost continuous succession of palaeofl oras from the Upper Jurassic up to the Coniacian can be traced. The Lower Cretaceous deposits are divided into the Batylykh Formation (Berriasian-Valanginian), the Eksenyakh Formation (Aptian) and the Khatyryk formations (early-middle Albian) (Vachrameev, 1958; Kiritchkova, 1985). The ages of formations are based on the composition of fl oristic assemblages and palynological data (Pavlov, 1957; Kiritchkova, 1985). Phy- tostratigraphy of the Jurassic and Lower Cretaceous deposits were studied by Kiritchkova (1985). The Khatyryk fl ora from the Khatyryk Formation is characterized by high species diversity and consists of more than 100 species. This assemblage comprises mostly ferns, cycadophytes, ginkgoaleans, czekanowskialeans, and conifers like other Early Cretaceous fl oras of Northern Asia. Angiosperms are rare, and are represented by several small-leaved species Trochodendroides, Cissites, Celastrophyllum and Morophyllum (Kiritchkova, Slastenov, 1966; Kiritchkova, Budantsev, 1967). The stratigraphy of Western Kazakhstan was studied by Vachrameev (1952). The early angiosperms were found in the middle Albian Kyzylshen Formation of the Chushkakul anticlinal, north of the Aral Sea. The Cenomanian and Turonian deposits are marine in this area. The underlying Cretaceous deposits are terrestrial and distinguished on lithological features into fi ve parts: the Daul Formation (Neocomian), the Muzbel Formation (lower Albian), the Karachetau Formation (lower-middle Albian), the Kyzylshen For- mation (middle Albian) and the Altykydyk Formation (upper Albian). Their ages were based on correlation with marine sections of the Emba River basin. Abundant plant fossils occur only in the Kyzylshen and the Altykydyk formations. They were described by Vachrameev (1952) and later in several papers of Krassilov (Vachrameev, Krassilov, 1979; Krassilov et al., 1983).

SYSTEMATIC DESCRIPTION Class MAGNOLIOPSIDA Order SAXIFRAGALES Family CERCIDIPHYLLACEAE Genus TROCHODENDROIDES Berry, 1922 Trochodendroides potomacensis (Ward) Bell Pl. I, ﬁ g. 1—3, pl. II, ﬁ g. 5, 7; Fig. 2, a—d

Trochodendroides potomacensis (Ward) Bell, 1956, p. 127, pl. 121, fi g. 2, pl. 124, fi g. 2. — Golovneva, Alek- seev, 2010, p. 128, pl. I, fi g. 1—3, text-fi g. 2. Populus potomacense Ward, 1895, p. 356, pl. IV, fi g. 1—3. — Berry, 1911, p. 458, pl. 81, fi g. 1, 1a—1e. Populus auriculata Ward, 1895, p. 356, pl. 4, fi g. 4. — Ward, 1905, p. 499, pl. 110, fi g. 5

58 Fig. 2. Leaves of Trochodendroides from the early-middle Albian: a—d — Trochodendroides potomacensis (Ward) Bell: a — lectotype, after Ward, 1895, pl. 4, ﬁ g. 3, Virgi- nia, Mount Vernon, Patapsco Formation; b — spec. BIN (VNIGRI) 676/1106-1, Lepiske River, Khatyryk Formation; c — spec. BIN 508/770, Zyryanka River, Buor-Kemyus Formation; d — spec. USNM 5387, after Hickey, Doyle, 1977, Virginia, Mount Vernon, Patapsco Formation. e — Trochodendroides buorensis Golovneva, spec. BIN 508/765, holotype, Zyryanka River, Buor-Ke- myus Formation. f — Trochodendroides vachrameeviana (Iljinskaja) Golovneva, spec. GIN 3302/76, holotype, Kazakh- stan, Karachetau, Kyzylshen Formation. g, i — Trochodendroides denticulata (Budantsev et Kiritchkova) Golovneva, Sitte River, Khatyryk Formation: g — spec. BIN (VNIGRI) 707/27, lectotype; i — spec. BIN (VNIGRI) 707/30. h — Trochodendroides sittensis Golovneva, spec. BIN (VNIGRI) 707/35, holotype, Sitte River, Khatyryk Formation. Scale bar 1 cm.

59 Populophyllum menispermoides Ward, 1905, p. 498, p. p. quoad pl. 110, fi g. 2, 4, non fi g. 3. Cercidiphyllum potomacense (Ward) Vachrameev, 1952, p. 190, p. p. quoad nomen. — Samylina, 1960, p. 337, pl. 1, fi g. 11, 12. Tetracentron potomacense (Ward) Iljinskaja, 1972, p. 21, text-fi g. 2 (1); Iljinskaja, 1974b, p. 114, pl. 45, fi g. 11—12, pl. 46, fi g. 3—7, text-fi g. 71. Prototrochodendroides jacutica Budantsev et Kiritchkova, in Kiritchkova, Slastenov, 1966, p. 165, pl. 5, fi g. 19—23. — Iljinskaja, 1974c, p. 107, pl. 43, fi g. 4—9, text-fi g. 64, fi g. 1—3.

Lectotype (designated by Vachrameev, 1952). Specimen, fi gured by Ward, 1895, pl. 4, fi g. 3; USA, Vir- ginia, Mount Vernon, Patapsco Formation, middle-late Albian. — Fig. 2, a. Diagnosis emended. Leaves of small size, widely ovate or ovate, with acute or slightly attenuate apex and cordate, sometimes truncate, base; margin crenate; teeth small, rounded, with obtuse apex and rounded (rarely acute) sinuses, sometimes tongue-shaped; midvein with 2—3 pairs of short secondary veins in upper part of leaf blade; basal veins diverge from one point near the top of petiole; upper basal veins extending about ⅔ of the distance to the apex, where looping with adjacent pair of secondary veins. Material studied. Collection BIN 196, spec. 1652—1655; collection BIN (VNIGRI) 1106, spec. a—d. Kolyma River basin, Zyryanka River, Buor-Kemyus Formation, lower-middle Albian, collection BIN 508, spec. 761-1, 768, 769, 770-1, 2, 786. Stratigraphic horizon and occurrence. USA, Virginia, Mount Vernon, Patapsco Formation, middle- late Albian; Canada, British Columbia, Kingsvale Group, Alberta, Blairmore Group (upper fl ora), Albian; Russia, Lena River basin, Lepiske River, Khatyryk Formation, early-middle Albian; Russia, Kolyma River basin, Zyryanka River, Buor-Kemyus Formation, early-middle Albian.

Trochodendroides buorensis Golovneva Pl. II, ﬁ g. 6; Fig. 2, e

Trochodendroides buorensis Golovneva, in Golovneva, Alekseev, 2010, p. 130, pl. 1, fi g. 4, text-fi g. 3. Zizyphoides sp., Samylina, 1960, p. 343, pl. 1, fi g. 6.

Holotype. Spec. BIN 508/765, Russia, Kolyma River basin, Zyryanka River, Buor-Kemyus Formation, early-middle Albian; Golovneva, Alekseev, 2010, pl. 1, ﬁ g. 4. — Pl. II, ﬁ g. 6. Diagnosis. Leaves small, widely elliptical, with rounded base and apex; margin entire in lower part of lamina and undulate in upper part; upper basal veins terminating near leaf apex. Material studied. Collection BIN 508, spec. 765. Stratigraphic horizon and occurrence. Russia, Kolyma River Basin, Zyryanka River, Buor-Kemyus Formation, early-middle Albian.

Trochodendroides denticulata (Budantsev et Kiritchkova) Golovneva, comb. nov. Pl. I, ﬁ g. 4; pl. III, ﬁ g. 3—6; Fig. 2, g, i

Morophyllum denticulatum Budantsev et Kiritchkova, in Kiritchkova, Budantsev, 1967, A new fi nd of the Lower Cretaceous fl ora, including angiosperms, in Yakutia, p. 941, pl. II, fi g. 7—14.

Lectotype (designated here). Spec. BIN (VNIGRI) 707/27, Russia, Lena River basin, Sitte River, site 3524, Khatyryk Formation, early-middle Albian; Kiritchkova, Budantsev, 1967, pl. II, fi g. 8. — Pl. III, fi g. 4; Fig. 2, g. Diagnosis. Leaves small, ovate, with acute or attenuate apex and cordate or truncate base; margin dentate, teeth small, frequent, equally developed, helmet-shaped or triangular with convex sides, and with attenuate rostrum at apex; midvein with 2—3 pairs of secondary veins in upper part of lamina; upper basal veins diverge from one point near the top of petiole, or sometimes at diff erent heights, extending about ½—⅔ of the distance to the apex, where looping with adjacent pair of secondary veins. Material studied. Collection BIN (VNIGRI) 707, spec. 27, 29—34. Stratigraphic horizon and occurrence. Russia, Lena River basin, Sitte River, site 3524, Khatyryk For- mation, early-middle Albian.

60 Trochodendroides sittensis Golovneva, sp. nov. Pl. I, ﬁ g. 5, 6; Fig. 2, h

Trochodendroides sp., Kiritchkova, Budantsev, 1967, p. 942, pl. II, ﬁ g. 15, 16.

Holotype. Spec. BIN (VNIGRI) 707/35, Russia, Lena River basin, Sitte River, site 3524, Khatyryk Formation, early-middle Albian. — Pl. I, ﬁ g. 6; Fig. 2, h. Diagnosis. Leaves small, elliptical, with acute apex and rounded base; margin crenate, teeth unequal in size, slightly adpressed, short, with wide base, rounded, obtuse apex, convex sides and acute sinuses; upper basal veins terminating near leaf apex. Description. Leaves elliptic, 4—5,5 cm long and 2,5—3 cm wide, with acute apex and rounded base. Margin is crenate in upper part of lamina and entire in the base. Teeth are unequal in size, slightly adpressed, short, with wide base, rounded, obtuse apex, convex sides and acute sinuses Primary venation actinodromous, with 3—5 primary veins. Upper basal veins are arcuate and rise to the apex, where they joint with middle vein. Lower basal veins are thinner and extend about ½ of the distance to the apex, where looping with adjacent secondary veins. Lower basal veins and basiscopic branches of upper basal veins form a series of loops along the margin. Short thin veins go from the outer part of the loops to the tooth apices. Tertiary venation is percurrent-reticulate, very thin. Material studied. Collection BIN (VNIGRI) 707, spec. 35—37. Stratigraphic horizon and occurrence. Russia, Lena River basin, Sitte River, site 3524, Khatyryk For- mation, early-middle Albian.

Trochodendroides vachrameeviana (Iljinskaja) Golovneva, comb. nov. Pl. III, ﬁ g. 1; Fig. 2, f

Tetracentron vachrameevianum Iljinskaja, 1972, p. 57, text-fi g. 2(2). — Iljinskaja, 1974b, p. 115, pl. 45, fi g. 4—10, text-fi g. 72. Cercidiphyllum potomacense auct. non (Ward) Vachrameev, 1952, pl. 13, fi g. 5, 6, text-fi g. 40.

Holotype. Spec. GIN 3302/76, Kazakhstan, Karachetau, Kyzylshen Formation, middle Albian; Vach- rameev, 1952, pl. 13, fi g. 5; Iljinskaja, 1972, p. 57, text-fi g. 2(2) — Pl. III, fi g. 1; Fig. 2, f. Diagnosis. Leaves small, widely ovate, with acute apex and rounded or slightly cordate base; margin dentate, teeth helmet-shaped or triangular with convex sides, acute apex and acute or rounded sinuses; upper basal veins departing from the midvein above the lower veins and terminating near the leaf apex. Material studied. Collection GIN 3302, spec. 38, 40, 63, 76, 79. Stratigraphic horizon and occurrence. Kazakhstan, Karachetau, Kyzylshen Formation, middle Albian.

DISCUSSION The genus Trochodendroides appeared in the geological record in the early-middle Albian, when it was represented by several species. Among them, T. potomacensis was the most widely distributed. This species was initially described by Ward (1895, 1905) from the Lower Cretaceous deposits of the Patapsco Forma- tion (Potomac Group), eastern United States as Populus potomacensis. The fossils come from the locality Mount Vernon, situated along the Potomac River in Northern Virginia. The plant-bearing bed belongs to pollen zone II-B of the Potomac Group (Doyle, Hickey, 1976), which is now thought to correspond to the middle-upper Albian (Hochuli et al., 2006). Later this species was revised by Berry (1911), who assigned to P. potomacensis leaves from the same layers, previously described by Ward (1895, 1905) as P. auriculata and Populophyllum menispermoides. Vachrameev (1952) discovered similar leaves in the middle Albian Kyzylshen Formation in Western Kazakhstan. He transferred Populus potomacensis to the extant genus Cercidiphyllum, based on Brown’s (1939) review of Cercidiphyllum-like leaves and fruits from the Tertiary deposits and chose one of the specimens, ﬁ gured by Ward (1895) as the lectotype. Samylina (1960) used the name Cercidiphyllum potomacensis for small cordate palmately-veined leaves from the lower-middle Albian Buor-Kemyus Formation of the Kolyma River basin (pl. II, ﬁ g. 5, 7). Bell (1956) assigned similar leaves from the Lower Cretaceous deposits of Canada to Trochodendroides and created combination T. potomacensis, while Iljinskaja (1972, 1974b) transferred this species to Tetracentron. Leaves from the lower-middle Albian Khatyryk Formation

61 (pl. I, fi g. 1—3) were fi rst described as Prototrochodendroides jacutica (Kiritchkova, Slastenov, 1966). Later this name was considered as a synonym of Trochodendroides potomacensis (Golovneva, Alekseev, 2010). Kir- itchkova and Slastenov (1966) thought that Prototrochodendroides diff ers from Trochodendroides by small leaf sizes and by cordate base. However, morphotypes with such features are rather widely represented in Trochodendroides (Golovneva et al., 2017) and in fact the genus Prototrochodendroides has no diff erences from Trochodendroides. We believe that leaves from the Patapsco Formation, Kingsvale Group, Blairmore Group, Buor-Ke- myus Formation and Khatyryk Formation belong to the same species with the most appropriate name Trochodendroides potomacensis. Leaves of this species are well distinguished from other species of Trochodendroides by cordate base, crenate margin with wide rounded teeth apices and sinuses and by the presence of well-developed secon dary veins, which extend from the middle vein in its upper half (Fig. 2 a—d, pl. I, fi g. 1—3, pl. II, 5, 7). The cordate base and well-developed secondary veins were found in many other Cretaceous and Tertiary species of Trochodendroides (Crane, 1984; Golovneva, Alekseev, 2010; Golovneva et al., 2017), as well as in the modern Cercidiphyllum, but such unusual margin was described only in T. potomacensis. It should be noted that some specimens of T. potomacensis may have sharp sinuses in certain parts of the margin, as is typical for the most species of Trochodendroides with crenate margin and for Cercidiphyllum (Fig. 2, b). The primary venation of T. potomacensis is actinodromous with fi ve basal veins radially diverging from the petiole; secondaries are festooned brochidodromous or semicraspedodromous. This type of venation is characteristic not only for Trochodendroides and Cercidiphyllum, but also for representatives of other families and genera, for example for Tetracentron and Zizyphoides (Trochodendraceae). Relationship of leaves from the Potomac Group previously assigned to “Populus” potomacensis with Trochodendraceae was inferred by many authors (Iljinskaja, 1972, 1974b; Hickey, Doyle, 1977; Crane, 1989). However, in order to establish securely relationship T. potomacensis with Cercidiphyllaceae it is necessary to link them with cor- responding reproductive structures. The earliest occurrence of Jenkinsella fruits, which usually associated with Trochodendroides leaves, was recorded from the lower-middle Albian deposits of the Omsukchan coal basin, where this genus is represented by dispersed fruits of J. fi latovii (Golovneva, Alekseev, 2017). Leaves of T. potomacensis are absent in these beds, but they were found in the contemporaneous deposits of the Zyryanka coal basin. Both coal basins are situated in one region (the Kolyma River basin) and have very similar fossil fl oras. Originally fruits of Jenkinsella fi latovii were described by Samylina (1976) as Kenella fi latovii Samylina and then transferred to Nyssidium (Golovneva, Alekseev, 2010). They are follicular fruits, single or in raceme, narrowly ellipsoid or narrowly obovate in shape, 13—16 mm in length and 4—6 mm in diameter (pl. II, fi g. 1—4). The base is cuneate, decurrent, with short stalk. The apex is acute with attenuate curve style 2—3 mm in length. Outer surface of fruits has thin subparallel longitudinal striation. This species diff ers from other Jenkinsella species by narrow elongated fruits with rather long curve style and also by thinner longitudinal striation. The follicles of J. fi latovii are similar with young follicles of J. jiayinensis that have comparable size, long tapering styles up to 4 mm, poorly developed locules and longitudinal ridges (Golov- neva, Alekseev, 2010). Diverse leaves and infructescences of Trochodendraceae are known from the Paleocene and Eocene of Canada and USA, where they are represented by genera Concavistyon, Pentacentron, Trochodendron and Tetracentron (Pigg et al., 2001, 2007; Manchester et al., 2018). More ancient history of Trochodendraceae is documented by reproductive structures Nordenskioldia and associated leaves Zizyphoides (Crane et al., 1991). The earliest Nordenskioldia fruits were recorded from the Turonian-Coniacian Derevyannogors- kaya Formation of New Siberia Island (Schmalhausen, 1890; Baikovskaya, 1956) and well-documented Zizyphoides leaves are known mostly from the Tertiary deposits. Leaves of Zizyphoides diff er from those of Trochodendroides potomacensis by the base shape and margin characters. The shape of leaf base in Zizyphoides ranges from cuneate to truncate or rounded, but deeply cordate leaves, as in T. potomacensis, was never recorded. The margin is entire, undulate or has irregular crenations in Zizyphoides, while margin is regularly crenate in T. potomacensis. The Buor-Kemyus fl ora includes in addition to T. potomacensis another species of the genus Trochoden- droides — T. buorensis (Golovneva, Alekseev, 2010). It is represented by a single specimen, which is about 1 cm in length, widely elliptical in shape with rounded base and apex and has entire or undulate margin (pl. II, fi g. 6). Unlike T. potomacensis its upper basal veins terminate near the leaf apex.

62 The Khatyryk fl ora from the Lena-Vilyuy depression includes, except T. potomacensis, two additional species of Trochodendroides, but they come from other locality. Leaves of T. potomacensis were found at the Lepiske River, and leaves of T. denticulata and T. sittensis were found at the Sitte River. The fi st species was previously described as Morophyllum denticulatum Budantsev et Kiritchkova (Kiritchkova, Budantsev, 1967). But the venation patterns and the margin features of these leaves correspond to the diagnosis of the genus Trochodendroides and we transfer species Morophyllum denticulatum in this genus. Leaves of Trocho- dendroides denticulata are quite large, 3—5 cm in length, ovate in shape, with acute or attenuate apex and cordate or truncate base (pl. III, fi g. 3—6). The margin is dentate, with small, frequent, helmet-shaped or triangular teeth. The upper basal veins extend about 1/2—2/3 of the distance to the apex and the midvein bears 2—3 pairs of well-developed secondary veins in the upper part of lamina. Similar teeth are characteristic for Trochodendroides rostrata Golovneva et P. Alekseev from the Cenomanian Simonovo Formation, Western Siberia (Golovneva, Alekseev, 2010) and for T. curvidens (Heer) Golovneva et Budantsev from the Eocene of Spitsbergen (Budantsev, Golovneva, 2009). Well-developed secondary veins in upper part of lamina occur in T. potomacensis, T. richardsonii (Heer) Kryshtofovich from Paleocene of Greenland and Spitsbergen, T. speciosa from the Paleocene Fort Union Formation and many others species. T. sittensis from the Sitte River was fi rstly reported as Trochodendroides sp. by Kiritchkova and Budant- sev (1967). Now we described these leaves as a new species. It diff ers from T. denticulata by elliptical shape and by crenate margin with wide, obtuse, slightly adpressed teeth. The upper basal veins of this species terminate near leaf apex. Elliptic leaves occur rather often in the Late Cretaceous Trochodendroides, but most part of species diff ers by bigger size and wider variability of leaf shape. Similar teeth are characteristic for T. kemensis (Ananjev) Golovneva and T. vachrameevii Budantsev from Siberia (Golovneva, Alekseev, 2010), however leaves of T. kemensis are usually expanded in the upper part and those of T. vachrameevii expanded in the lower part. Leaves from the middle Albian Kyzylshen Formation of Kazakhstan were fi rstly described by Vach- rameev (1952) as Cercidiphyllum potomacense (pl. III, fi g. 1). Iljinskaja (1972, 1974b) believed that these leaves are diff erent from the leaves of Trochodendroides (Cercidiphyllum) potomacensis and described them as a new species Tetracentron vachrameevianum. We agree with her decision that the fossils from Kazakhstan are a separate species, but we consider that the assignment of this species to modern genus Tetracentron is unreliable. The genus Tetracentron appears much later in the geological record (Pigg et al., 2007). Although the primary venation pattern of the Kazakhstan fossils is similar to that of Tetracentron, these leaves have another structure of teeth. We transfer this species into Trochodendroides, creating a combination T. vachrameeviana (Iljinskaja) Golovneva, because the main features of the Kazakhstan leaves correspond to those of this genus. These leaves are widely ovate in outline, with acute apex and rounded or slightly cordate base. Margin is dentate, with helmet-shaped or triangular teeth with convex sides, acute apex and acute or rounded sinuses. The upper basal veins depart from the midvein above the lower basal veins and terminate near the leaf apex. This species has rather peculiar set of characters and has no closely similar species among other Trochodendroides, although separate characters occur in diff erent species of this genus. Two other occurrences of putative Cercidiphyllaceae were reported from the Lower Cretaceous of Primo- rye, Far East of Russia: Nyssidium orientale Samylina (1961) and Cercidiphyllum sujfunense Krassilov (1967). The remains of Nyssidium orientale come from the black coaliferous shales which belong to the Sta- rosuchan Formation, the lowest member of the Suchan Group, Partizansk coal basin. These fruits are the ancient angiosperm occurrence on the territory of Russia. They are preserved as compressions and details of the internal structure can not be studied. These fruits are fl attened, wide elliptical in outline, about 10 mm in length and 6 mm in width, with 6—7 narrow ridges running longitudinally over the surface. There is a rounded protrusion about 1,5 mm in diameter on one pole of the fruits and a smooth, without ridges, circle on the other one (pl. IV, fi g. 1—4). Samylina (1961) believed that the external morphology and overall shape of these fruits resemble endocarps of Nyssa (Cornales) and assigned them to form-genus Nyssidium, established by Heer (1870) for Nyssa-like fossils from the Paleogene of Spitsbergen. She did not relate these fruits to Cercidiphyllacae. In fact, N. orientale from the Barremian-Aptian Starosuchan Formation corresponds on the whole to diagnosis of the genus Nyssidium in the sense of Heer (small size, elliptical shape and ribbed surface), but its affi nity, not only to Cercidiphyllum-like plants, but to angiosperms in general, is doubtful. These fossils can be also the seeds of conifers or other gymnosperms. Fruits or seeds N. orientale have no follicular characters, such as stalk, terminal style and suture grooves. We believe that the ancient reproductive structure, related to Cercidiphyllaceae, is Jenkinsella fi latovii from the lower-middle Albian deposits of the Omsukchan coal basin.

63 The species Cercidiphyllum sujfunense comes from the lower-middle Albian Galenki Formation of the Razdolnaya coal basin, southern Primorye. Krassilov (1967) described under this name both leaves and fruits, although they were not found in organic connection. Leaves are elliptic with cuneate base and entire margin (pl. IV, fi g. 6). The venation is pinnate, brochidodromous; secondary lateral veins are decurrent near the middle vein. These fossils are completely diff erent from the leaves of Cercidiphyllum or Trochoden- droides, which have palmate venation and dentate or crenate margin. Leaves from the Galenki Formation are comparable with those of Asiatifolium elegans Sun, Guo et Zheng, which were recorded from the lower- middle Albian Frentsevka Formation of the Partizansk coal basin (Golovneva et al., 2018) and from the Lower Cretaceous Chengzihe Formation, exposed near the city of Jixi in Northeastern China (Sun, Dilcher, 2002). Fruit of Cercidiphyllum sujfunense (pl. IV, fi g. 5) is similar with Jenkinsella fruits in short stalk and attenuate apex, but it has no suture grooves, longitudinal ridges and transverse striae. We believe that this fruit cannot be assigned to Cercidiphyllaceae. All Lower Cretaceous species of Trochodendroides have very small leaves, as most other angiosperms of this age. Leaves of T. buorensis are 1 cm in length, leaves of T. potomacensis range from 1 to 3 cm. Leaves of T. vachrameeviana reach 1,5—2,5 cm in length. Leaves of T. sittensis and T. denticulata from the Sitte River are a little bigger. Their length varies from 3 to 5 cm that is comparable with size of some Late Cretaceous species of this genus. Such small sizes indicate that these plants were shrubs. Since these plants grew in a humid climate and were associated with alluvial deposits, the small size of their leaves could not be linked with insuffi cient moisture. Some specimens of T. potomacensis and T. vachrameeviana have rather thick petiole, that suggests the possibility of a herbaceous lifestyle. However, leaf lamina and petiole of most species are well diff erentiated, and we consider that the shrub habit is most probable for these plants. Fruits of Jenkinsella fi latovii are also smaller, than fruits from the Tertiary deposits, but some Late Cretaceous species of this genus (J. conferta P. Alekseev et Golovneva, and J. vilyuensis Golovneva et P. Alekseev) may have very small follicles, about 5—7 mm in length (Golovneva, Alekseev, 2017). The diversifi cation of Cercidiphyllaceae began in the early-middle Albian and continued in the late Albian and Cenomanian. In the upper Albian-Cenomanian deposits the diversity of the genus Trochoden- droides increased. The type species T. rhomboidea (Lesquereux) Berry come from the Cenomanian Dakota Formation, USA (Lesquereux, 1874). Later T. elliptica Dilcher et Wang, which distinguished from T. rhomboidea by elliptical shape, was additionally described from the Dakota fl ora (Wang, Dilcher, 2006). Bell (1956) reported small cordate Trochodendroides leaves from the Dunvegan Formation of Canada. The late Albian-Cenomanian Gre- benka fl ora from the Krivorechenskaya Formation of the North-East of Russia includes T. deminii Yudova et Golovneva (Golovneva et al., 2017). The Cenomaian Boskho fl ora (Eastern Siberia) contains two species: Trochodendroides sp. 1 with cordate leaves and Trochodendroides sp. 2 with elliptical leaves (Golovneva, Alek- seev, 2010). In the Cenomanian Simonovo Formation (Western Siberia) three species of Trochodendroides (T. kemensis (Ananjev) Golovneva, T. ananjevii Golovneva, T. rostrata Golovneva et P. Alekseev) were described (Golovneva, Alekseev, 2010). In contrast to the early-middle Albian representatives of the genus Trochoden- droides, all late Albian-Cenomanian species have rather large leaves and were undoubtedly trees. In the Turonian and Coniacian fl oras of Siberia and North-East of Russia Trochodendroides reached the highest systematic and morphologic diversity throughout the Late Cretaceous, up to 5—7 species in some fl o- ristic assemlages (Budantsev, 1983; Herman, Lebedev, 1991; Philippova, Abramova, 1993; Golovneva, Alek- seev, 2010; Golovneva et al., 2017). Usually their remains associated with reproductive structures of Alasia and Jenkinsella (Golovneva, 2006; Golovneva, Alekseev, 2017). In the Turonian and Coniacian deposits leaves of Trochodendroides often dominate in alluvial sediments together with platanaceous leaves. Probably, diff erent Trochodendroides species prevailed in the Cretaceous riparian forests as species of Salix and Populus today.

CONCLUSION The fi rst reliable occurrences of the genus Trochodendroides were recorded in the early-middle Albian. In this time fi ve species (T. potomacensis, T. buorensis, T. sittensis, T. vachrameeviana and T. denticulata) were established in Northeastern Asia. The relationship of these leaves with Cercidiphyllaceae is confi rmed by fi nds of associated fruits Jenkinsella fi latovii and by signifi cant diversity of Trochodendroides in the Up- per Albian-Cenomanian deposits. These fossils refl ect the early radiation of Cercidiphyllaceae and indicate that the intensive diversifi cation of Cercidiphyllaceae began long before the Tertiary, extending the fossil history of the family by 30 million years ago. Investigation of the early-middle Albian Cercidiphyllaceae provides new important data for our understanding of the early evolution of eudicots.

64 ACKNOWLEDGEMENTS The present study was carried out within the framework of the institutional research project of the Komarov Botanical Institute of the Russian Academy of Sciences and was supported by the Russian Foun- dation for Basic Research (project 18-34-00592).

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66 Kovar-Eder, J., Meller, B., Zetter, R. 1998. Cercidiphyllum crenatum (Unger) R. W. Brown in der kohlefüh- renden Abfolge von Oberdorf, N Voitsberg, Steiermark. Mitt. Ref. Geol. und Paläont. Landesmuseum Joanneum., 2: 239—263. Krassilov, V. A. 1967. Rannemelovaya fl ora yuzhnogo Primoriya i ee znachenie dlya stratigrafi i [Early Cre- taceous fl ora of southern Primorye and its signifi cance for the stratigraphy]. Moscow: Nauka, 264 p. (in Russian). Krassilov, V. A., Kodrul, T. M. 2008. In situ pollen of Alasia, a supposed staminate infl orescence of Trocho- dendroides plant. Acta Mus. Nat. Pragae, ser. B, 64(2—4): 115—124. Krassilov, V. A., Shilin, P. V., Vachrameev, V. A. 1983. Cretaceous fl owers from Kazakhstan. Review of Pal- aeobotany and Palynology, 40(1—2): 91—113. https://doi.org/10.1016/0034-6667(83)90005-2 Kryshtofovich, A. N. 1929. Discovery of the oldest dicotyledons of Asia in the equivalents of the Poto- mac Group in Suchan, Ussuriland, Siberia. Izvestiya Geologicheskogo Komiteta, 48(9): 1357—1390. (in Russian). Kryshtofovich, A. N. 1938. Late Cretaceous plants from the Kolyma River Basin. Contribution to the knowledge of the Kolyma-Indigirka Land, ser. 2, 15: 1—16. (in Russian). Lesquereux, L. 1874. Contributions to the fossil fl ora of the Western Territories. Part I. The Cretaceous fl ora. U. S. Geol. Surv. Rep. Terr., 6: 1—136. Likht, F. R. 1961. Novaya nakhodka fl ory dvudol’nykh v nizhnem melu Suchana [The new fi nding of dicoty- ledonous in the Lower Cretaceous deposits of the Suchan coal basin]. Informacionnii Sbornik PGU, 2: 47—50. (in Russian). Likht, F. R. 1994. Usloviya obrazovaniya i stratigrafi ya nizhnemelovykh otlozhenii yuzhnogo Primoriya [Conditions of generation and stratigraphy of the Lower Cretaceous deposits of southern Primorye]. Russian Journal of Pacifi c geology, 6: 55—67. (in Russian). Manchester, S. R., Meyer, H. W. 1987. Oligocene fossil plants of the John Day Formation, Fossil, Oregon. Oreg. Geol., 49: 115—127. Manchester, S. R., Pigg, K. B., Kvaček, Z., DeVore, M. L., Dillhoff , R. M. 2018. Newly recognized diversity in Trochodendraceae from the Eocene of Western North America. Int. J. Plant Sci., 179(8): 663—676. https://doi.org/10.1086/699282 Markevich, P. V., Konovalov, V. P., Malinovskii, A. I., Filippov, A. N. 2000. Nizhnemelovye otlozheniya Sikhote-Alinya [The Lower Cretaceous deposits of the Sikhote-Alin]. Vladivostok: Dal’nauka, 282 p. (in Russian). Markevich, V. S. 1995. Melovaya palinofl ora severa Vostochnoi Azii. [Cretaceous Palynofl ora of Northeast- ern Asia]. Vladivostok: Dal’nauka, 200 p. (in Russian). McIver, E. E., Basinger, J. F. 1993. Flora of the Ravenscrag Formation (Paleocene), Southwestern Saskatch- ewan, Canada. Palaeontographica Canadiana, 10: 1—167. Pavlov, V. V., 1957. O palinolgicheskom obosnovanii vozrasta uglenosnyh otlozhenĳ v rajone nizhnego tech- eniya r. Lepiske. [Palinology of coal-bearing deposits in lower reach of Lepiske River]. Sbornik statej po paleontologii i biostratigrafi i, vol. 3. (in Russian). Philippova, G. G., Abramova, L. N. 1993. The Late Cretaceous fl ora of Northeastern Russia. Moscow: Ne- dra, 348 p. (in Russian). Pigg, K. B., Wehr, W. C., Ickert-Bond, S. M. 2001. Trochodendron and Nordenskioldia (Trochodendraceae) from the middle Eocene of Washington State, U.S.A. Int. J. Plant Sci., 162(5): 1187—1198. https://doi.org/10.1086/321927 Pigg, K. B., Dillhoff , R. M., DeVore, M. L., Wehr W. C. 2007. New diversity among the Trochodendraceae from the early-middle Eocene Okanogan Highlands of British Columbia, Canada, and Northeastern Washington State, United States. Int. J. Plant Sci., 168(4): 521—532. https://doi.org/10.1086/512104 Popov, G. G. 1962. The Zyryanka coal basin. Geologiya mestorozhdeniy uglya i goryuchikh slanzev, 10: 32—105. (in Russian). Prynada, V. D. 1938. Materials for the Mesozoic fl ora of the Kolyma River Basin. Contribution to the knowledge of the Kolyma-Indigirka Land, ser. 2, 13: 1—68. (in Russian). Reid, E. M., Chandler, M. E. 1933. The London Clay fl ora. London: British Mus. Nat. Hist., 561 p. Resheniya IV Mezhvedomstvennogo regional’nogo stratigrafi cheskogo soveshchaniya po dokembriyu i fanerozoyu yuga Dalnego Vostoka i Vostochnogo Zabaikal’ya, Khabarovsk, 1990. Ob’yasnitel’naya zapiska k stratigrafi cheskim skhemam. [Resolutions of the IV interdepartmental regional stratigraphic conference on the Precambrian and Phanerozoic in the Far East and Eastern Transbaikalia,

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PLATE I

1—3 — Trochodendroides potomacensis (Ward) Bell, Lena River basin, Lepiske River, Khatyryk Forma- tion, early-middle Albian: 1 — spec. BIN 1196/1652, ×4; 2 — spec. BIN 1196/1655, ×3; 3 — spec. BIN (VNIGRI) 676/1106-1, ×5. 4 — Trochodendroides denticulata (Budantsev et Kiritchkova) Golovneva, Lena River basin, Sitte River, Khatyryk Formation, early-middle Albian, spec. BIN (VNIGRI) 707/30, ×5. 5—6 — Trochodendroides sittensis Golovneva, Lena River basin, Sitte River, Khatyryk Formation, early- middle Albian: 5 — spec. BIN (VNIGRI) 707/37, ×2; 6 — spec. BIN (VNIGRI) 707/35, holotype, ×3.

68 PLATE I

2 3

5 6

69 PLATE II

1—4 — Jenkinsella ﬁ latovii (Samylina) Golovneva et P. Alekseev, Magadan Region, Omsukchan, Galimyi and Toptan formations, early-middle Albian: 1 — spec. BIN 510/5, ×2; 2 — spec. BIN 511/24-1, ×4, holotype; 3 — spec. BIN 511/24-2, ×4; 4 — spec. BIN 511/25, ×2. 5, 7 — Trochodendroides potomacensis (Ward) Bell, Kolyma River basin, Zyryanka River, Buor-Kemyus Formation, early-middle Albian, spec. BIN 508/770: 5 — ×2,5; 7 — ×5. 6 — Trochodendroides buorensis Golovneva, Kolyma River basin, Zyryanka River, Buor-Kemyus Formation, early-middle Albian, spec. BIN 508/765, ×5.

70 PLATE II

1 2 3

4 5

6 7

71 PLATE III

1 — Trochodendroides vachrameeviana (Iljinskaja) Golovneva, spec. GIN 3302/76, Kazakhstan, Karachetau, Kyzylshen Formation, early-middle Albian, ×5. 2—6 — Trochodendroides denticulata (Budantsev et Kiritchkova) Golovneva, Lena River basin, Sitte River, Khatyryk Formation, early-middle Albian: 2, 4 — spec. BIN (VNIGRI) 707/27, lectotype: 2 — ×5; 4 — ×3; 3 — spec. BIN (VNIGRI) 707/29, ×2; 5 — spec. BIN (VNIGRI) 707/34, ×1; 6 — spec. BIN (VNIGRI) 707/30, ×1.

72 PLATE III

5 4

73 PLATE IV

1—4 — Nyssidium orientale Samylina, Primorye, Partizansk city, Starosuchan Formation, Hauterivian- early Aptian: 1 — spec. BIN 506/3749, general view of four fruits, ×2; 2a — spec. BIN 506/3749-1, holotype, ×5; 2b — spec. BIN 506/3749-2, ×5; 3 — spec. BIN 506/3749-5, ×5; 4 — spec. BIN 506/3749-6, ×5. 5—6 — Cercidiphyllum sujfunense Krassilov, Primorye, Konstantinovka, Galenki Formation, early-middle Albian: 5 — spec. IBSS 11-135, fruit, ×4; 6 — spec. IBSS 11-134, leaf, holotype, ×4.

74 PLATE IV

b 1

3 4

5 6