CC BY
30ym 561.46:551.763
https://doi.Org/10.31111/palaeobotany/2018.9.54
naneoóomaHUKa, 2018, T. 9, C. 54—75 Palaeobotany, 2018, Vol. 9, P. 54—75
FOSSIL EVIDENCE OF INITIAL RADIATION OF CERCIDIPHYLLACEAE
L. B. Golovneva, A. A. Zolina
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 five species of Trochodendroides leaves were recognized, including Trochodendroidespotomacensis (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 affinity, 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 first reliable records of the genus Trochodendroides appear in the early-middle Albian. The relationship of these leaves with Cercidiphyllaceae is confirmed by finds of associated fruits Jenkinsella fila-tovii and by significant 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 floras. These fossils reflect 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, Northeastern Asia.
The modern family Cercidiphyllaceae contains a single genus Cercidiphyllum with two species: C. japoni-cum Siebold et Zuccarini and C. magnificum (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 flowers 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 diversification 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 first recorded from the Oligocene of North America and Europe (Jahnichen 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; Golovneva, 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 first detected by O. Heer (1869) from the Paleocene deposits of Atanekerdluk in West Greenland, and described as Nyssa arctica Heer.
R. W. Brown (1939) first 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-
Komarov Botanical Institute RAS, St. Petersburg, [email protected]
INTRODUCTION
lum arcticum (Heer) R. W. Brown, although he indicated, that fossil infructescences differ 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 differ 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 superficial. In fact, Nyssidium ekmanii has so few distinctive features (small size, elongated shape and ribbed surfaces) that may be fit with many systematically different 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 inner 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 first 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 fructifications and associated foliage with those of extant Cercidiphyllum, supposing that these taxa were closely related.
The most completely reconstructed Cercidiphyllum-like plant isJoffrea 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 different details of carpels, winged seeds and fruits. Joffrea was interpreted as an extinct representative of Cercidiphyllaceae. Based on this material a more comprehensive comparison of all known complete fructification structures and living Cercidiphyllum was undertaken (Crane, Stockey, 1985, 1986). The condensed inflorescences of the modern Cercidiphyllum were hypothesized to have evolved from the racemose type seen in Joffrea, accompanied by a change in suture orientation.
Staminate racemose inflorescences, associated with Trochodendroides leaves and Joffrea shoots, were described later as a separate genus Alasia Golovneva (2006). These inflorescences represent axes with helically 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 ornamentation, 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 first 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 Cretaceous, 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 reflect the earliest radiation of Cercidiphyllaceae. In the result one species of Jenkinsella and five species
of Trochodendroides were recognized, including Trochodendroides potomacensis (Ward) Bell, T. buoren-sis Golovneva, T. sittensis Golovneva, T. vachrameeviana (Iljinskaja) Golovneva, comb. nov., T. denticu-lata (Budantsev et Kiritchkova) Golovneva, comb. nov. and Jenkinsella filatovii (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 Institute (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 flows 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 ofJenkinsella filatovii 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 River basin, Zyryanka River, Buor-Kemyus Formation; 5 — Magadan Region, Omsukchan, Galimyi and Toptan formations; 6 — Primorye, Partizansk, Starosuchan Formation; 7 — Primorye, Konstantinovka, Galenki Formation.
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 tuffaceous deposits of the early-middle Albian Galenki Formation (Krassilov, 1967). Material is kept in the Federal Scientific 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, prefix 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 Formation (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 flora 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 floristic assemblages of the Buor-Kemyus type overlie marine deposits with mollusks of the late Aptian age. The development of the younger Grebenka flora with predominance of angiosperms began in the late Albian-Cenomanian, as indicated by marine mollusks found together with the floral remains (Herman, 1999). These data confirm the early-middle Albian age of the Buor-Kemyus flora.
The Omsukchan coal basin is situated in the upper reaches of the Kolyma River, in the Balygychan-Sugoi interfluve, the Omsukchan district of the Magadan Region (Fig. 1). The Lower Cretaceous terrigenous and volcanogenous deposits of this basin were firstly 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 flora, which has significant similarity with the Buor-Kemyus flora 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-
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 Formation (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 palaeofloras 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 floristic assemblages and palynological data (Pavlov, 1957; Kiritchkova, 1985). Phy-tostratigraphy of the Jurassic and Lower Cretaceous deposits were studied by Kiritchkova (1985). The Khatyryk flora 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 floras 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 five parts: the Daul Formation (Neocomian), the Muzbel Formation (lower Albian), the Karachetau Formation (lower-middle Albian), the Kyzylshen Formation (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, fig. 1—3, pl. II, fig. 5, 7; Fig. 2, a—d
Trochodendroides potomacensis (Ward) Bell, 1956, p. 127, pl. 121, fig. 2, pl. 124, fig. 2. — Golovneva, Alek-
seev, 2010, p. 128, pl. I, fig. 1—3, text-fig. 2. Populuspotomacense Ward, 1895, p. 356, pl. IV, fig. 1—3. — Berry, 1911, p. 458, pl. 81, fig. 1, 1a—1e. Populus auriculata Ward, 1895, p. 356, pl. 4, fig. 4. — Ward, 1905, p. 499, pl. 110, fig. 5
Fig. 2. Leaves of Trochodendroides from the early-middle Albian:
a—d — Trochodendroidespotomacensis (Ward) Bell: a — lectotype, after Ward, 1895, pl. 4, fig. 3, Virginia, 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, Kazakhstan, 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.
Populophyllum menispermoides Ward, 1905, p. 498, p. p. quoad pl. 110, fig. 2, 4, non fig. 3. Cercidiphyllum potomacense (Ward) Vachrameev, 1952, p. 190, p. p. quoad nomen. — Samylina, 1960, p. 337, pl. 1, fig. 11, 12.
Tetracentronpotomacense (Ward) Iljinskaja, 1972, p. 21, text-fig. 2 (1); Iljinskaja, 1974b, p. 114, pl. 45,
fig. 11—12, pl. 46, fig. 3—7, text-fig. 71. Prototrochodendroides jacutica Budantsev et Kiritchkova, in Kiritchkova, Slastenov, 1966, p. 165, pl. 5, fig. 19—23. — Iljinskaja, 1974c, p. 107, pl. 43, fig. 4—9, text-fig. 64, fig. 1—3.
Lectotype (designated by Vachrameev, 1952). Specimen, figured by Ward, 1895, pl. 4, fig. 3; USA, Virginia, 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 % 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 flora), 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, fig. 6; Fig. 2, e
Trochodendroides buorensis Golovneva, in Golovneva, Alekseev, 2010, p. 130, pl. 1, fig. 4, text-fig. 3. Zizyphoides sp., Samylina, 1960, p. 343, pl. 1, fig. 6.
Holotype. Spec. BIN 508/765, Russia, Kolyma River basin, Zyryanka River, Buor-Kemyus Formation, early-middle Albian; Golovneva, Alekseev, 2010, pl. 1, fig. 4. — Pl. II, fig. 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, fig. 4; pl. III, fig. 3—6; Fig. 2, g, i
Morophyllum denticulatum Budantsev et Kiritchkova, in Kiritchkova, Budantsev, 1967, A new find of the Lower Cretaceous flora, including angiosperms, in Yakutia, p. 941, pl. II, fig. 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, fig. 8. — Pl. III, fig. 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 different heights, extending about Vâ—% 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 Formation, early-middle Albian.
Trochodendroides sittensis Golovneva, sp. nov.
Pl. I, fig. 5, 6; Fig. 2, h
Trochodendroides sp., Kiritchkova, Budantsev, 1967, p. 942, pl. II, fig. 15, 16.
Holotype. Spec. BIN (VNIGRI) 707/35, Russia, Lena River basin, Sitte River, site 3524, Khatyryk Formation, early-middle Albian. — Pl. I, fig. 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 actinodro-mous, 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 V 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 Formation, early-middle Albian.
Trochodendroides vachrameeviana (Iljinskaja) Golovneva, comb. nov.
Pl. III, fig. 1; Fig. 2, f
Tetracentron vachrameevianum Iljinskaja, 1972, p. 57, text-fig. 2(2). — Iljinskaja, 1974b, p. 115, pl. 45, fig.
4—10, text-fig. 72.
Cercidiphyllumpotomacense auct. non (Ward) Vachrameev, 1952, pl. 13, fig. 5, 6, text-fig. 40.
Holotype. Spec. GIN 3302/76, Kazakhstan, Karachetau, Kyzylshen Formation, middle Albian; Vachrameev, 1952, pl. 13, fig. 5; Iljinskaja, 1972, p. 57, text-fig. 2(2) — Pl. III, fig. 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 Formation (Potomac Group), eastern United States as Populuspotomacensis. 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, figured by Ward (1895) as the lectotype. Samylina (1960) used the name Cercidiphyllum potoma-censis for small cordate palmately-veined leaves from the lower-middle Albian Buor-Kemyus Formation of the Kolyma River basin (pl. II, fig. 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
(pl. I, fig. 1—3) were first described as Prototrochodendroides jacutica (Kiritchkova, Slastenov, 1966). Later this name was considered as a synonym of Trochodendroidespotomacensis (Golovneva, Alekseev, 2010). Kiritchkova and Slastenov (1966) thought that Prototrochodendroides differs 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 differences 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 secondary veins, which extend from the middle vein in its upper half (Fig. 2 a—d, pl. I, fig. 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 five 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 corresponding 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. filatovii (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 floras.
Originally fruits ofJenkinsella filatovii were described by Samylina (1976) as Kenella filatovii 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, fig. 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 differs from other Jenkinsella species by narrow elongated fruits with rather long curve style and also by thinner longitudinal striation. The follicles of J. filatovii 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 differ 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 flora includes in addition to T.potomacensis another species of the genus Trochodendroides — 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, fig. 6). Unlike T. potomacensis its upper basal veins terminate near the leaf apex.
The Khatyryk flora 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 fist 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 Trochodendroides denticulata are quite large, 3—5 cm in length, ovate in shape, with acute or attenuate apex and cordate or truncate base (pl. III, fig. 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 firstly reported as Trochodendroides sp. by Kiritchkova and Budantsev (1967). Now we described these leaves as a new species. It differs 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 differs 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 firstly described by Vach-rameev (1952) as Cercidiphyllumpotomacense (pl. III, fig. 1). Iljinskaja (1972, 1974b) believed that these leaves are different 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. vach-rameeviana (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 different 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 flattened, 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, fig. 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 affinity, 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 filatovii from the lower-middle Albian deposits of the Omsukchan coal basin.
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, fig. 6). The venation is pinnate, brochidodromous; secondary lateral veins are decurrent near the middle vein. These fossils are completely different 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 ofJixi in Northeastern China (Sun, Dilcher, 2002). Fruit of Cercidiphyllum sujfunense (pl. IV, fig. 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 insufficient 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 differentiated, and we consider that the shrub habit is most probable for these plants. Fruits of Jenkinsella filatovii 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 diversification 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 flora (Wang, Dilcher, 2006). Bell (1956) reported small cordate Trochodendroides leaves from the Dunvegan Formation of Canada. The late Albian-Cenomanian Gre-benka flora from the Krivorechenskaya Formation of the North-East of Russia includes T. deminii Yudova et Golovneva (Golovneva et al., 2017). The Cenomaian Boskho flora (Eastern Siberia) contains two species: Trochodendroides sp. 1 with cordate leaves and Trochodendroides sp. 2 with elliptical leaves (Golovneva, Alekseev, 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 Trochodendroides, all late Albian-Cenomanian species have rather large leaves and were undoubtedly trees.
In the Turonian and Coniacian floras 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 flo-ristic assemlages (Budantsev, 1983; Herman, Lebedev, 1991; Philippova, Abramova, 1993; Golovneva, Alekseev, 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, different Trochodendroides species prevailed in the Cretaceous riparian forests as species of Salix and Populus today.
CONCLUSION
The first reliable occurrences of the genus Trochodendroides were recorded in the early-middle Albian. In this time five 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 confirmed by finds of associated fruits Jenkinsella filatovii and by significant diversity of Trochodendroides in the Upper Albian-Cenomanian deposits. These fossils reflect the early radiation of Cercidiphyllaceae and indicate that the intensive diversification 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.
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 Foundation for Basic Research (project 18-34-00592).
REFERENCES
APGIII. 2009. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc., 161: 105—121. https://doi.org/10.1111/j.1095-8339.2009.00996.x
Baikovskaya, T. N. 1956. The Upper Cretaceous Floras of Northern Asia. Acta of the Komarov Botanical
Institute, ser. 8, 2: 49—181. (in Russian). Bell, W. A. 1956. Lower Cretaceous floras of Western Canada. Canada Geol. Surv. Mem., 285: 1—331. Berry, E. W. 1911. Systematic paleontology, Lower Cretaceous: Pteridophyta, Cycadophytae, Gymnosper-mae, Monocotyledonae, Dicotyledonae. In: Lower Cretaceous. Baltimore: The Johns Hopkins Press, p. 153—172.
Berry, E. W. 1926. Tertiary floras from British Columbia. Canada Dep. Mines Geol. Surv. Bull., 42: 91—116. Brown, R. W. 1939. Fossil leaves, fruits, and seeds of Cercidiphyllaceae. J. Paleontol., 13: 485—499. Budantsev, L. Y. 1983. History of the Arctic flora of the Early Cenophytic epoch. Leningrad: Nauka, 156 p. (in Russian).
Budantsev, L. Y., Golovneva, L. B. 2009. Palaeogene flora of Spitsbergen. St.-Petersburg: Marafon, 400 p. (in Russian).
Bugdaeva, E. V., Markevich, V. S., Volynets, E. B. 2014. The coal-forming plants of the upper part of the Lower Cretaceous Starosuchan Formation (Partizansk Basin, South Primorye Region). Stratigraphy and Geological Correlation, 22(3): 256—268. Crane, P. R. 1984. A re-evaluation of Cercidiphyllum-like plant fossils from the British Early Tertiary. Bot. J.
Linn. Soc., 89: 199—230. https://doi.org/10.1111/j.1095-8339.1984.tb02196.x Crane, P. R. 1989. Paleobotanical evidence on the early radiation of nonmagnoliid dicotyledons. Pl. Syst.
Evol., 162: 165—191. https://doi.org/10.1007/BF00936916 Crane, P. R., Manchester, S. R., Dilcher, D. L. 1991. Reproductive and vegetative structure of Norden-skioldia (Trochodendraceae), a vesselless dicotyledon from the Early Tertiary of the Northern Hemisphere. Amer. J. Bot., 78(10): 1311—1334. https://doi.org/10.2307/2445271 Crane, P. R., Stockey, R. A. 1985. Growth and reproductive biology of Joffrea speirsii gen. et sp. nov., a Cercidiphyllum-like plant from the Late Paleocene of Alberta, Canada. Canad. J. Bot., 63: 340—364. https://doi.org/10.1139/b85-041 Crane, P. R., Stockey, R. A. 1986. Morphology and development of pistillate inflorescences in extant and
fossil Cercidiphyllaceae. Ann. Miss. Bot. Gard., 73: 382—393. https://doi.org/10.2307/2399118 Cronquist, A. 1981. An integrated system of classification of flowering plants. New York: Columbia Univ. Press, 1262 p.
Doyle, J. A., Hickey, L. J. 1976. Pollen and leaves from the mid-Cretaceous Potomac Group and their bearing on early angiosperm evolution. In: Origin and early evolution of angiosperms. New York: Columbia Univ. Press, p. 139—206.
Ellis, B., Daly, D., Hickey, L. J., Johnson, K., Mitchell, J., Wilf, P., Wing, S. 2009. Manual of leaf architecture.
New York: Cornell Univ. Press, 190 p. Endress, P. K. 1986. Floral structure, systematics and phylogeny in Trochodendrales. Ann. Miss. Bot. Gard.,
73: 297—324. https://doi.org/10.2307/2399115 Endress, P. K. 1993. Cercidiphyllaceae. In: The Families and genera of vascular plants. Vol. II. Berlin, Heidelberg, New York: Springer, p. 250—252. Feng, G. P., Li, C. S., Zhilin, S. G., Wang, Y. F., Gabrielyan, I. G. 2000. Nyssidium jiayinense sp. nov. (Cercidiphyllaceae) of the Early Tertiary from north-east China. Bot. J. Linn. Soc., 134: 471—484. https://doi.org/10.1006/bojl.2000.0335 Filatov, S. I. 1972. Stratigraphy of the nonmarine deposits of the Balygychan-Sugoy trough. Materialy po
geologii i poleznym iskopaemym Severo-Vostoka SSSR, 20: 164—169 (in Russian). Friis, E. M., Crane, P. R., Pedersen, K. R. 2011. Early flowers and angiosperm evolution. Cambridge: Cambridge Univ. Press, 585 p. https://doi.org/10.1017/CB09780511980206
Fu, D. Z., Endress, P. K. 2001. Cercidiphyllaceae. In: Flora of China. St. Louis: Missouri Botanical Garden Press, Vol. 6, p. 126.
Golovneva, L. B. 1994. Maastrichtian—Danian Floras of the Koryak Upland. Proceedings Komarov Botanical Institute, 13:1 — 147. (in Russian). Golovneva, L. B. 2006. Alasia, gen. nov. — male inflorescences, associated with Trochodendroides leaves
(Cercidiphyllaceae). Botanicheskii Zhurnal, 91(12): 1898—1906. (in Russian). Golovneva, L. B. 2018. The Chaun flora of the Okhotsk-Chukotka volcanogenic belt. St. Petersburg: Mara-fon, 308 p. (in Russian).
Golovneva, L. B., Alekseev, P. I. 2010. The genus Trochodendroides Berry in the Cretaceous floras of Siberia.
Palaeobotany, 1: 120—166. (in Russian). Golovneva, L. B., Alekseev, P. I. 2017. Taxonomy and morphological diversity of infructescences Jenkinsella co-occurred with Trochodendroides leaves in the Cretaceous and Paleogene. Palaeobotany, 8: 92—121. Golovneva, L. B., Sun, G., Bugdaeva, E. V. 2008. Campanian flora of the Bureya River Basin (Late Cretaceous of the Amur Region). Paleontological Journal, 42(5): 554—567. https://doi.org/10.1134/S0031030108050110 Golovneva, L. B., Alekseev, P. I., Gnilovskaya, A. A., Yudova, D. A. 2017. The genus Trochodendroides (Cercidiphyllaceae) in the Cretaceous flora of Noth-East of Russia. Palaeobotany, 8: 122—179. (in Russian). Golovneva, L., Alekseev, P., Bugdaeva, E., Volynets, E. 2018: An angiosperm dominated herbaceous community from the early-middle Albian of Primorye, Far East of Russia. Fossil Imprint, 74(1—2): 165— 178. https://doi.org/10.2478/if-2018-0012 Heer, O. 1869. Contributions to the fossil flora of North Greenland, being a description of the plants collected by Mr. Edward Whymper during the summer of 1867. Phil. Trans. Royal Soc., 159: 445—488. https://doi.org/10.1098/rspl.1868.0061 Heer, O. 1870. Die Miocene Flora und Fauna Spitzbergens. Kongl. Svenska Vetensk. Akad. Handl., 8(7): 1—98. Herman, A. B. 1999. Cretaceous flora of the Anadyr-Koryak subregion (North-Eastern Russia): systematic composition, age, stratigraphic and florogenic significance. Transactions of the Geological Institute, 529: 1—121. (in Russian).
Herman, A. B. 2013. Albian-Paleocene flora of the North Pacific: systematic composition, palaeofloristics and phytostratigraphy. Stratigraphy and Geological Correlation, 21(7): 689—747. https://doi.org/10.1134/S0869593813070034 Herman, A. B., Lebedev, E. L. 1991. Cretaceous stratigraphy and flora of Northwestern Kamchatka. Transactions of the Geological Institute, 468: 1—189. (in Russian). Hickey, L. J., Doyle, J. A. 1977. Early Cretaceous evidence for angiosperm evolution. Bot. Rev., 43(1):
3—104. https://doi.org/10.1007/BF02860849 Hochuli, P. A., Heimhofer, U., Weissert, H. 2006. Timing of early angiosperm radiation: recalibrating the
classical succession. J. Geol. Soc. London, 163: 587—594. https://doi.org/10.1144/0016-764905-135 Hollick, A. 1936. The Tertiary floras of Alaska. U. S. Geol. Surv. Prof. Paper, 182: 1 — 185. Iljinskaja, I. A. 1972. Correction of the volume of genus Trochodendroides and new fossil species Cocculus.
Botanicheskii Zhurnal, 57(1): 17—30. (in Russian). Iljinskaja, I. A. 1974a. Nyssidium Heer. In: Magnoliophyta Fossilia URSS. Leningrad: Nauka, vol. 1, p. 123— 124. (in Russian)
Iljinskaja, I. A. 1974b. Trochodendrales. In: Magnoliophyta Fossilia URSS. Leningrad: Nauka,. vol. 1, p. 112—125. (in Russian)
Iljinskaja, I. A. 1974c. Prototrochodendroides Budants. et Kiritchk. In: Magnoliophyta Fossilia URSS. Leningrad: Nauka, vol. 1, p. 107—109. (in Russian) Jähnichen, H., Mai, D. H., Walther, H. 1980. Blätter und Früchte von Cercidiphyllum Siebold et Zuccarini
im mitteleuropäischen Tertiär. Schriften. Geol. Wiss., 16: 357—399. Kiritchkova, A. I. 1985. Fitostratigrafiya i flora yurskikh i nizhnemelovykh otlozheniy Lenskogo basseyna [Phytostratigraphy and flora of the Jurassic and Lower Cretaceous deposits of the Lena Basin]. Leningrad: Nedra, 223 p. (in Russian). Kiritchkova, A. I., Budantsev, L. Yu. 1967. A new find of Early Cretaceous flora with angiosperms in Yakutia. Botanicheskii Zhurnal, 52(7): 937—945 (in Russian). Kiritchkova, A. I., Slastenov, Yu. L. 1966. Stratigraphiya i flora nizhnemelovykh otlozhenii r. Lepiske (Za-padnoye Priverkhoyanie) [Stratigraphy and flora of the Lower Cretaceous deposits of the Lepiske River (Western Priverkhoyanie)]. Trudy VNIGRI, 249: 147—169. (in Russian).
Kovar-Eder, J., Meiler, B., Zetter, R. 1998. Cercidiphyllum crenatum (Unger) R. W. Brown in der kohleführenden Abfolge von Oberdorf, N Voitsberg, Steiermark. Mitt. Ref. Geoi. und Paiäont. Landesmuseum Joanneum., 2: 239—263.
Krassiiov, V. A. 1967. Rannemeiovaya flora yuzhnogo Primoriya i ee znachenie diya stratigrafii [Early Cretaceous flora of southern Primorye and its significance for the stratigraphy]. Moscow: Nauka, 264 p. (in Russian).
Krassiiov, V. A., Kodrui, T. M. 2008. In situ pollen of Alasia, a supposed staminate inflorescence of Trocho-dendroides plant. Acta Mus. Nat. Pragae, ser. B, 64(2—4): 115—124.
Krassiiov, V. A., Shilin, P. V., Vachrameev, V. A. 1983. Cretaceous flowers from Kazakhstan. Review of Pal-aeobotany and Paiynoiogy, 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 Potomac Group in Suchan, Ussuriiand, Siberia. Izvestiya Geoiogicheskogo Komiteta, 48(9): 1357—1390. (in Russian).
Kryshtofovich, A. N. 1938. Late Cretaceous piants from the Koiyma River Basin. Contribution to the knowledge of the Koiyma-Indigirka Land, ser. 2, 15: 1 — 16. (in Russian).
Lesquereux, L. 1874. Contributions to the fossil flora of the Western Territories. Part I. The Cretaceous flora. U. S. Geoi. Surv. Rep. Terr., 6: 1 — 136.
Likht, F. R. 1961. Novaya nakhodka flory dvudoi'nykh v nizhnem meiu Suchana [The new finding of dicotyledonous in the Lower Cretaceous deposits of the Suchan coal basin]. Informacionnii Sbornik PGU, 2: 47—50. (in Russian).
Likht, F. R. 1994. Usioviya obrazovaniya i stratigrafiya nizhnemeiovykh otiozhenii yuzhnogo Primoriya [Conditions of generation and stratigraphy of the Lower Cretaceous deposits of southern Primorye]. Russian Journal of Pacific geology, 6: 55—67. (in Russian).
Manchester, S. R., Meyer, H. W. 1987. Oiigocene fossil plants of the John Day Formation, Fossil, Oregon. Oreg. Geoi., 49: 115—127.
Manchester, S. R., Pigg, K. B., Kvacek, 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., Konovaiov, V. P., Maiinovskii, A. I., Fiiippov, A. N. 2000. Nizhnemeiovye otiozheniya Sikhote-Alinya [The Lower Cretaceous deposits of the Sikhote-Alin]. Vladivostok: Dai'nauka, 282 p. (in Russian).
Markevich, V. S. 1995. Meiovaya palinoflora severa Vostochnoi Azii. [Cretaceous Palynoflora of Northeastern Asia]. Vladivostok: Dai'nauka, 200 p. (in Russian).
McIver, E. E., Basinger, J. F. 1993. Flora of the Ravenscrag Formation (Paieocene), Southwestern Saskatchewan, Canada. Paiaeontographica Canadiana, 10: 1 — 167.
Pavlov, V. V., 1957. O paiinoigicheskom obosnovanii vozrasta ugienosnyh otlozhenij v rajone nizhnego tech-eniya r. Lepiske. [Paiinoiogy of coal-bearing deposits in lower reach of Lepiske River]. Sbornik statej po paieontoiogii i biostratigrafii, voi. 3. (in Russian).
Phiiippova, G. G., Abramova, L. N. 1993. The Late Cretaceous flora 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. Geoiogiya mestorozhdeniy ugiya i goryuchikh sianzev, 10: 32—105. (in Russian).
Prynada, V. D. 1938. Materials for the Mesozoic flora of the Kolyma River Basin. Contribution to the knowledge of the Koiyma-Indigirka Land, ser. 2, 13: 1—68. (in Russian).
Reid, E. M., Chandler, M. E. 1933. The London Clay flora. London: British Mus. Nat. Hist., 561 p.
Resheniya IV Mezhvedomstvennogo regionai'nogo stratigraficheskogo soveshchaniya po dokembriyu i fanerozoyu yuga Dainego Vostoka i Vostochnogo Zabaikai'ya, Khabarovsk, 1990. Ob'yasnitei'naya zapiska k stratigraficheskim skhemam. [Resolutions of the IV interdepartmental regional strati-graphic conference on the Precambrian and Phanerozoic in the Far East and Eastern Transbaikalia,
Khabarovsk, 1990. Explanatory note to stratigraphic schemes]. Khabarovsk: KhGGGP, 1994, 123 p. (in Russian).
Samylina, V. A. 1960. The angiosperms from the Lower Cretaceous of the Kolyma Basin. Botanicheskii Zhurnal, 45(3): 335—352. (in Russian).
Samylina, V. A. 1961. New data on the Lower Cretaceous flora of the southern Primorye. Botanicheskii Zhurnal, 46(5): 634—645. (in Russian).
Samylina, V. A. 1964. Mesozoic flora from the left bank of the Kolyma River (Zyryanka coal basin). Part 1. Equisetales, Polypodiales, Bennettitales. Acta of the Komarov Botanical Institute, ser. 8, 5: 39—79 (in Russian).
Samylina, V. A. 1968. Early Cretaceous angiosperms of the Soviet Union based on leaf and fruit remains. Bot. J. Linn. Soc., 61: 207—218. https://doi.org/10.1111/j.1095-8339.1968.tb00119.x
Samylina, V. A. 1976. Cretaceous flora of the Omsukchan. Leningrad: Nauka, 206 p. (in Russian).
Schmalhausen, J. 1890. Wissenschaftliche Resultate der von der Kaiserlichen Akademie der Wissenschaften zur erforschung des Janalandes und der Neusibirischen Inseln in der Jahren 1885 und 1886 ausgesandten Expedition. Abtheilung II: Tertiäre Pflanzen der Insel Neusibirien. Memoires de l'Academie Imperiale des Sciences de St.-Petersbourg. ser. VII, 37(5): 1—22.
Shczepetov, S. V. 1995. Stratigraphy of the continental Cretaceous of Northeastern Russia. Magadan: DVO AN RAS, 121 p. (in Russian).
Sun, G., Dilcher, D. L. 2002. Early angiosperms from the Lower Cretaceous of Jixi, eastern Heilongji-ang, China. Review of Palaeobotany and Palynology, 121: 91—112. https://doi.org/10.1016/S0034-6667(02)00083-0
Takhtajan, A. L. 1969. Flowering plants: origin and dispersal. Edinburgh: Oliver and Boyd, 310 p.
Vachrameev, V. A. 1952. Stratigrafiya i iskopaemaya flora melovyh otlozhenij zapadnogo Kazahstana [Stratigraphy and fossil flora of the Cretaceous deposits of Western Kazakhstan]. Regionalnaya stratigrafiya SSSR, vol. 1. Moscow: AN SSSR, 385 p. (in Russian).
Vachrameev, V. A. 1958. Stratigrafiya i iskopaemaya flora yurskih i melovyh otlozhenij Vilyujskoj vpadiny i prilegayushchej chasti Priverhoyanskogo progiba [Stratigraphy and fossil flora of the Jurassic and Cretaceous deposits of the Vilyui depression and adjacent part of the Priverhoyansk depression]. Regionalnaya stratigrafiya SSSR, vol. 3. Moscow: AN SSSR, 137 p. (in Russian).
Vachrameev, V. A., Krassilov, V. A. 1979. Reproductivnye organy zvetkovykh iz alba Kazachstana [Reproductive organs of angiosperms from the Albian of Kazakhstan]. Paleontologicheskii Zhurnal, 1979(1): 121 — 128. (in Russian).
Volynets, E. B. 2005. The Aptian—Cenomanian flora of Primorye, part 1: Floral assemblages. Stratigraphy and Geological Correlation, 13: 613—631.
Volynets, E. B., Bugdaeva, E. V. 2017. The Aptian-Cenomanian flora of the Razdolnaya coal basin (Primorye region, Russia). Island Arc, 26: e12171. https://doi.org/10.1111/iar.12171
Ward, L. F. 1895. The Potomac Formation. U. S. Geol. Surv. Ann. Rep., 15: 307—397.
Ward, L. F. 1905. Status of the Mesozoic floras of the United States. U. S. Geol. Surv. Monogr., 48: 1—616.
Yudova, D. A., Golovneva, L. B. 2010. The genus Trochodendroides Berry in the Chingandzha flora of Northeastern Russia. Palaeobotany, 5: 60—72. (in Russian).
PLATE I
1—3 — Trochodendroides potomacensis (Ward) Bell, Lena River basin, Lepiske River, Khatyryk Formation, early-middle Albian:
1 — spec. BIN 1196/1652, x4;
2 — spec. BIN 1196/1655, x3;
3 — spec. BIN (VNIGRI) 676/1106-1, x5.
4 — Trochodendroides denticulata (Budantsev et Kiritchkova) Golovneva, Lena River basin, Sitte River,
Khatyryk Formation, early-middle Albian, spec. BIN (VNIGRI) 707/30, x5. 5—6 — Trochodendroides sittensis Golovneva, Lena River basin, Sitte River, Khatyryk Formation, early-middle Albian:
5 — spec. BIN (VNIGRI) 707/37, x2;
6 — spec. BIN (VNIGRI) 707/35, holotype, x3.
PLATE II
1—4 — Jenkinsellafilatovii (Samylina) Golovneva et P. Alekseev, Magadan Region, Omsukchan, Galimyi and Toptan formations, early-middle Albian:
1 — spec. BIN 510/5, x2;
2 — spec. BIN 511/24-1, x4, holotype;
3 — spec. BIN 511/24-2, x4;
4 — spec. BIN 511/25, x2.
5, 7 — Trochodendroidespotomacensis (Ward) Bell, Kolyma River basin, Zyryanka River, Buor-Kemyus
Formation, early-middle Albian, spec. BIN 508/770: 5 — x2,5; 7 — x5. 6 — Trochodendroides buorensis Golovneva, Kolyma River basin, Zyryanka River, Buor-Kemyus Formation, early-middle Albian, spec. BIN 508/765, x5.
PLATE III
1 — Trochodendroides vachrameeviana (Iljinskaja) Golovneva, spec. GIN 3302/76, Kazakhstan,
Karachetau, Kyzylshen Formation, early-middle Albian, x5. 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 — x5; 4 — x3; 3 — spec. BIN (VNIGRI) 707/29, x2;
5 — spec. BIN (VNIGRI) 707/34, xl;
6 — spec. BIN (VNIGRI) 707/30, xl.
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, x2; 2a — spec. BIN 506/3749-1, holotype, x5; 2b — spec. BIN 506/3749-2, x5;
3 — spec. BIN 506/3749-5, x5;
4 — spec. BIN 506/3749-6, x5.
5—6 — Cercidiphyllum sujfunense Krassilov, Primorye, Konstantinovka, Galenki Formation, early-middle Albian:
5 — spec. IBSS 11-135, fruit, x4;
6 — spec. IBSS 11-134, leaf, holotype, x4.
