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Hironoia fusiformis gen. et sp. nov.; a cornalean fruit from the Kamikitaba locality (Upper , Lower Coniacian) in northeastern Japan

Article in Journal of Plant Research · January 2003 DOI: 10.1007/s10265-002-0062-6 · Source: PubMed

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Original Article

Hironoia fusiformis gen. et sp. nov.; a cornalean fruit from the Kamikitaba locality (Upper Cretaceous; Lower Coniacian) in northeastern Japan

Masamichi Takahashi( ) · Peter R. Crane · Steven R. Manchester

M. Takahashi Department of Environmental Sciences, Faculty of Science, Niigata University, Ikarashi, Niigata City, 950-2181 Japan

P.R. Crane Royal Botanic Gardens, Kew, Richmond, Surrey, UK

S.R. Manchester Department of Natural History, Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA

E-mail: [email protected] Phone: +81-25-2626991 Fax: +81-25-2626991

Received: 17 June 2002 / Accepted: 30 August 2002 / Published online:

Abstract. The application of sieving techniques to bulk samples from the Ashizawa Formation, Futaba (Lower Coniacian) of northeastern Honshu, Japan, has yielded well-preserved mesofossil assemblages comparable with those recently described from eastern North America, Europe, and central Asia. Among the most abundant and distinctive components of these assemblages are fusiform fruits that are assigned here to a new genus and species, Hironoia fusiformis gen. et sp. nov. The fruits developed from an epigynous ovary with three to four locules. Each locule bears one seed and has a distinctive dorsal germination valve. These features of the fruit, along with the adnate calyx, indicate an affinity to extant Cornales and specifically the Cornaceae sensu lato. The recognition of an unequivocal cornalean fruit in the Early Coniacian-Early Santonian of Japan provides the earliest record of this group in the fossil record. It also establishes a minimum age for the early divergence of the asterid clade, a major group of living angiosperms comprising more than a third of all species of extant flowering plants.

- 1 - Keywords. Angiosperms - Ashizawa Formation - Cornales - Futaba Group - Hironoia fusiformis gen. et sp. nov. - Japan

Introduction

Over the last 15 years studies of the early fossil history of flowering plants have been revolutionized by the discovery of abundant small, well-preserved and systematically informative fossil flowers, fruits and seeds from Cretaceous sediments. These specimens have yielded spectacular, new information relating to the early diversification of many lineages of extant angiosperms, and have provided new insights into the evolution of angiosperm pollination and dispersal biology (Crane et al. 1995). Most of these new data have been based on mesofossil assemblages discovered in eastern North America and Europe (e.g., Friis 1983, 1984; Knobloch and Mai 1984, 1986; Crane et al. 1994, 1995). Recently, however, similar mesofossil assemblages have been recognized in Kazakhstan, central Asia (Frumin and Friis 1996, 1999), and also from the Futaba Group (Early Coniacian-Early Santonian) of northeastern Japan (Takahashi et al. 1999a, b, 2001).

In parallel with these paleobotanical advances, our understanding of phylogenetic relationships among extant angiosperms has steadily improved through combined analyses of morphological and molecular data (often several genes) for many taxa (Soltis et al. 1999). The increased resolution of natural monophyletic groups among extant angiosperms provides an improved framework for the use of fossils to establish the age and former geographic distribution patterns of angiosperm clades. The Cornales, now identified as the earliest diverging lineage of a major clade of angiosperms - the asterids - are one of many groups of angiosperms in which patterns of evolution are becoming much better understood as a result of integrated neobotanical and paleobotanical investigations. In this paper we describe a new fossil representative of the Cornaceae sensu lato, which is the earliest published record of this family. This material contributes a new species to the very small number of fossil angiosperm reproductive structures so far described from the of Japan (Stopes and Fujii 1910; Nishida 1985, 1991, 1994; Takahashi et al. 1999a, b, 2001), and provides important new information on the time of diversification of the asterid clade.

Materials and methods

Plant mesofossils were isolated from two sets of bulk samples collected 1998-2001 in the Futaba Group exposed in northeastern Honshu, Japan. The samples that yielded the fossils described here (collection F16) comprised a poorly sorted carbonaceous black sandy siltstone collected at the Kamikitaba locality along a tributary at the Kitaba River, Hirono-machi, Fukushima Prefecture, northeastern Japan (study Route B of Ando et al. 1995; 37°12 N, 140°57 E). These samples were from the Asamigawa Member of the Ashizawa Formation, which comprises the lowermost sediments in the Futaba Group. About 90 specimens of fusiform fruits were examined. Other levels in the Futaba Group were also sampled and have yielded mesofossil assemblages that lack the characteristic fruits described in this paper.

The Futaba Group is a fluvial to shallow marine sedimentary succession that occurs in the southern Abukuma Belt in northeast Japan close to the Pacific Coast of Honshu (Ando et al. 1995). In the north it unconformably overlies the Abukuma granite, while in the south it rests unconformably on the shales of the Takakurayama Group. It is overlain by Tertiary sediments (Ando 1997). Based on the occurrence of Lower Coniacian ammonites and inoceramids, the age of the Futaba Group is thought to range from Early Coniacian to Early Santonian. The age of the plant-bearing sediments in the Asamigawa Member is probably Early Coniacian (ca. 89 million years B.P., Gradstein et al. 1995).

- 2 - The dispersed palynoflora from the Futaba Group has been described by Miki (1977) and Takahashi (1988). Three samples from the Ashizawa Formation were studied by Miki (1977). Conifer pollen dominated all of the samples with taxodiaceous and podocarpaceous-pinaceous (saccate) grains predominating. Putative araucariaceous pollen also occurred in some samples; and Classopollis (extinct Cheirolepidiaceae) was also consistently present at low levels. Pollen of angiosperms, pteridophytes and presumed cycads, Bennettitales, Ginkgo, and Gnetales were also significant in these palynofloras. Knowledge of the flora of the Futaba Group has recently been expanded significantly by the discovery of mesofossil assemblages have been recovered from the Futaba Group (Takahashi et al. 1999a, 1999b, 2001), which have yielded a rich assemblage of angiosperms, gymnosperms, and pteridophytes, including both reproductive structures and vegetative remains.

Bulk samples were dried, disaggregated in water, and sieved through a 125-µm mesh. The residual carbonaceous debris was then cleaned in hydrofluoric and hydrochloric acids, rinsed in water, and dried in air. Individual specimens were then separated under the dissecting microscope. Some of the specimens were frozen in absolute ethanol with liquid nitrogen and fractured on a TF-1 chamber. Specimens selected for scanning electron microscopy were mounted on polished aluminum scanning electron microscope stubs, sputter coated with platinum-palladium, and examined in a Hitachi S-800 field emission scanning electron microscope (FE-SEM).

All specimens illustrated in this article are deposited in the paleobotanical collections of the Department of Geology and Paleontology, National Science Museum (NSM-PP), Tokyo, 169-0073 Japan.

Systematic description

Class Magnoliopsida

Order Cornales

Family Cornaceae sensu Eyde (1988)

Genus Hironoia gen. nov.

See Figs. 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38..

Diagnosis. Fruit fusiform, developed from an epigynous flower. Perianth attached just above the broadest part of the fruit with free, short, triangular to ovate tepals. Ovary extending beyond the perianth and tapering to a single narrow style. Ovary also narrowing at the base into a slender stalk. Fruit thick-walled, composed mainly of fibers, with three or four locules each containing one pendulous seed. Each locule opening by a single dorsal valve that often becomes detached first at the apex of the ovary.

Type species. Hironoia fusiformis sp. nov.

Etymology. The genus name Hironoia refers to the town of Hirono, which is located close to the site where the fossils were collected.

- 3 - - 4 - Figs. 1-9. Hironoia fusiformis gen. et sp. nov., Kamikitaba assemblage, Asamigawa Member, Ashizawa Formation (lower Coniacian), Futaba Group, Fukushima Prefecture, northeastern JapanFig. 1. Holotype, lateral view of well-preserved fruit showing perianth attached above the broadest part of the fruit; note ovary extending beyond the perianth, tapering to a single narrow style, and narrowing at the base into a slender stalk. NSM-PP12015. Scale bar 500 µm

Fig. 2.Lateral view of well-preserved specimen showing hypanthium and free tepal lobes. NSM-PP12016. Scale bar 500 µm

Fig. 3. Lateral view of abraded specimen showing fusiform shape. NSM-PP12017. Scale bar 500 µm

Fig. 4. Lateral view of poorly developed specimen showing possible nectariferous rim within the hypanthium. NSM-PP12017. Scale bar 500 µm

Fig. 5. Tepal with an obtuse to rounded apex. NSM-PP12016. Scale bar 300 µm

Fig. 6. Detail of abraded specimen showing a distinctive pattern of internal thickening. NSM-PP12016. Scale bar 300 µm

Fig. 7. Detail of epidermis surface of style. NSM-PP12016. Scale bar 50 µm

Fig. 8. Detail of epidermis surface of style showing fine reticulate pattern on outer surface of cuticle. NSM-PP12016. Scale bar 20 µm

Fig. 9. Surface of style showing elliptical perforations of probable secretary structure. NSM-PP12016. Scale bar 50 µm

- 5 - Figs. 10-18. Hironoia fusiformis gen. et sp. nov., Kamikitaba assemblage, Asamigawa Member, Ashizawa Formation (lower Coniacian), Futaba Group, Fukushima Prefecture, northeastern JapanFig. 10. Abraded specimen showing locules with valvate germination; valve missing from locule on the left, valve still attached at the base on locule to the right. NSM-PP12018. Scale bar 500 µm

- 6 - Fig. 11. Abraded specimen showing outline of germination valve still attached at base; note that separation proceeds downward along the margins of the locule cavity. NSM-PP12019. Scale bar 500 µm

Fig. 12. Abraded specimen showing locule containing the remains of a seed (left) and valve (right). NSM-PP12020. Scale bar 500 µm

Fig. 13. Fractured specimen with two valves missing, showing locules. NSM-PP12021. Scale bar 500 µm

Fig. 14. Fractured specimen showing smooth inner surface of locule. NSM-PP12022. Scale bar 300 µm

Fig. 15. Abraded specimen showing fragmented locule cavity perhaps indicating a less regular mode of dehiscence. NSM-PP12023. Scale bar 500 µm

Fig. 16. Detail of hypanthium surface showing equiaxial epidermal cells. NSM-PP12016. Scale bar 50 µm

Fig. 17. Detail of hypanthium surface showing longitudinally elongate epidermal cells. Scale bar 20 µm

Fig. 18. Short slender stalk at the base of the fruit. NSM-PP12015. Scale bar 150 µm

- 7 - - 8 - Figs. 19-29. Hironoia fusiformis gen. et sp. nov., Kamikitaba assemblage, Asamigawa Member, Ashizawa Formation (lower Coniacian), Futaba Group, Fukushima Prefecture, northeastern JapanFig. 19. Broken specimen showing in situ seed. NSM-PP12024. Scale bar 500 µm

Fig. 20. Fractured specimen showing three locules. NSM-PP12025. Scale bar 500 µm

Fig. 21. Fractured specimen showing four locules: three well-developed. NSM-PP. Scale bar 300 µm

Fig. 22. Fractured specimen showing three locules and two in situ seeds. NSM-PP12027. Scale bar 300 µm

Fig. 23. Fractured specimen showing four locules. NSM-PP12028. Scale bar 300 µm

Fig. 24. Locule cavity composed of tabular more or less equiaxial cells with a smooth surface. NSM-PP12021. Scale bar 200 µm

Fig. 25. Fractured central axis of specimen showing four vascular bundles (arrows). NSM-PP12029. Scale bar 100 µm

Fig. 26. Endocarp composed of fibers. NSM-PP12028. Scale bar 100 µm

Fig. 27. Detail of endocarp showing fibrous sclerenchyma. NSM-PP12087. Scale bar 100 µm

Fig. 28. Vascular bundles showing tracheary elements. NSM-PP12018. Scale bar 10 µm

Fig. 29. Detail of tracheary elements. NSM-PP12028. Scale bar 5 µm

- 9 - Figs. 30-38. Hironoia fusiformis gen. et sp. nov., Kamikitaba assemblage, Asamigawa Member, Ashizawa Formation (lower Coniacian), Futaba Group, Fukushima Prefecture, northeastern JapanFig. 30. Fractured specimen showing seeds; note solitary seed in each locule. NSM-PP12030.

- 10 - Scale bar 300 µm

Fig. 31. Fractured specimen showing two locules and in situ seed. NSM-PP12031. Scale bar 300 µm

Fig. 32. Detail of in situ seed in locule from Fig. 30. NSM-PP12030. Scale bar 200 µm

Fig. 33. Seed fractured transversely in locule. NSM-PP12032. Scale bar 50 µm

Fig. 34. Detail of Fig. 30 showing pendulous seed attached ventrally near the apex of locule. NSM-PP12030. Scale bar 200 µm

Fig. 35. Small projection near the base of an attached seed that may represent the chalaza. NSM-PP12023. Scale bar 200 µm

Fig. 36. Detail of seed surface composed of transversely elongated cells. NSM-PP12030. Scale bar 30 µm

Fig. 37. Apex of locule showing attachment point of the single seed. NSM-PP12071. Scale bar 100 µm

Fig. 38. Fractured seed coat apparently composed of two sclerified cell layers. NSM-PP12032. Scale bar 5 µm

Hironoia fusiformis sp. nov.

Diagnosis: as for the genus.

Dimensions: length of fruit 2.5-6.5 mm, breadth 1.75-3.5 mm; length of tepals 0.4-0.75 mm, breadth 0.4-0.75 mm; length of seed 2.3-2.6 mm, breadth 1.0-1.1 mm.

Materials: about 90 specimens; some charcoalified, others heavily coalified; described previously as "epigynous flower type 3" (Takahashi et al. 1999a). The holotype is NSM-PP12015. Other specimens include paratypes NSM-PP12016-12032, and NSM-PP12041-12132. All specimens are from collection F16.

Type locality and horizon: collection F16 is from the Asamigawa Member of the Ashizawa Formation, Futaba Group, and of Early Coniacian (Upper Cretaceous) age. Samples were collected at the Kamikitaba locality, Hirono-machi, Fukushima Prefecture, northeastern Japan (37°12 N, 140°57 E).

Etymology: the specific epithet, fusiformis, refers to the shape of the fruits.

Description and remarks: these fruits are recognized by their distinctive fusiform lateral profile (Figs. 1, 2, 3, 4, 10, 11, 12, 13, 14, 19), their subrounded, square to triangular cross section (Figs. 21, 22, 23) and their massive, woody construction (Figs. 26, 27, 28, 29, 30, 31, 32, 33, 34). When broken, they reveal three to four locules, each with a single seed (Figs. 20, 21, 22, 23). The fruit tapers gradually toward the apex above the level at which the perianth is attached. All of the specimens are broken and none shows the style apex and stigma. The tapering portion of the ovary that projects above the perianth is finely striated with an otherwise smooth epidermis. At higher magnifications, the surface of the epidermis has a fine reticulate pattern. A short, slender stalk expands distally into the basal part of the perianth, which is adnate to the fruit wall forming on hypanthium (Fig. 1). The hypanthium has a smooth outer surface with 10-12 ribs running from

- 11 - the base to the level of insertion of the tepals (Figs. 1, 2). The appearance of many specimens in which only parts of the hypanthium are preserved, combined with the complete absence of the hypanthium from abraded specimens (Fig. 3), indicates that the tissues of the hypanthium were only loosely attached to the ovary in mature specimens. Poor preservation of the rim of the hypanthium makes it difficult to determine the number of tepals, but estimates based on the few available specimens in which one or more tepals are preserved suggest that there were six, or perhaps occasionally four (Figs. 1, 2). There is no evidence of other floral organs. Filaments, anthers and pollen are unknown and it is unclear whether the fruits developed from a unisexual or bisexual flower.

A single specimen of a smaller, apparently abortive or immature, fruit (NSM-PP12018) shows two lunate masses of tissue inside and projecting slightly above the hypanthial rim, and partially surrounding the ovary (Fig. 4). We estimate that three such structures (possible nectaries?) would have completely encircled the ovary to form a pulvinate disc. In this specimen the base of the ovary (embedded within the hypanthium) is proportionately shorter than in the mature fruits.

In mature fruits, tepals are triangular to ovate in shape with an obtuse to rounded apex (Figs. 2, 5). In specimens in which the epidermis has been partially abraded away, the longitudinal ribs are more prominent, revealing vascular bundles ca. 150 µm in diameter (Fig. 6). These vascular bundles are clearly independent from those entering the style (Fig. 8). The surface of the style often shows conspicuous elliptical bulges or perforations, ca. 70 µm long in the epidermis (Figs. 7, 9). These often have a slightly raised rim, and are larger and more conspicuous than stomata. These may be the opening of some kind of secretory structure (Fig. 9), but it is also possible that they are of fugal origin.

Abraded specimens are often rounded at the base and more or less pyriform in shape (Figs. 10, 11). The locules open by valves in which the ovary wall overlying the locule cavity is removed. In several specimens in which the valve is still attached it is clear that the ovary wall begins to break away over the upper part of the locule cavity (Figs. 10, 11). Separation then proceeds downward along the margins of the locule cavity (Figs. 11, 12). In some specimens, the valve is clearly broken along a transverse line near the base of the locule cavity leaving a "window " in the ovary wall (Figs. 13, 14). In other specimens, the ovary wall over the locule cavity has begun to fragment, perhaps indicating a less regular mode of dehiscence (Fig. 15). The surface of the well-preserved hypanthium is smooth composed of equiaxial epidermal cells (Figs. 16, 17). At the base of the fruit there is short slender stalk and in one specimen (Fig. 18) this appears to show two bracteoles. Above the stalk, the base to the fruit expands distally to form the basal part of the hypanthium (Fig. 18).

The fruits are usually three loculed, but a few specimens with four locules have been observed (Figs. 19, 20, 21, 22, 23). The locules are separated from each other by a massive fruit wall. The locule is lined by a layer, one-cell thick, of tabular more or less equiaxial cells with a smooth surface (Fig. 24). The fruit has several vascular bundles in the peripheral portion and three or four vascular bundles situated near the central axis where the three septa intersect, but no clearly developed central vascular bundles (Fig. 25). The outer layers of the fruit, including exocarp and mesocarp, have been removed by abrasion in most of the specimens, such that only the sclerenchymatous endocarp remains. The endocarp forms a uniformly thick wall around each of the locules and forms the septa (Fig. 26). The inner endocarp is composed of fibrous sclerenchyma cells with 4-6-µm-thick cell walls. The peripheral portion of the endocarp is composed of sclerids, 10-20 µm in diameter (Fig. 27). Vascular bundles within the endocarp septa are composed of tracheary elements, 8-11 µm in diameter often with scalriform pits, 0.5-1.0 µm wide (Figs. 28, 29).

Each locule includes a solitary seed (Figs. 30, 31). The seeds are unitegmic, elongate, 2.3-2.6 mm long, conforming in size to the locules, in which they reside (Figs. 31, 32, 33). Seeds are ovate and taper to a point at the apex. Based on the in situ material, the seeds are ca. 2.6 mm long and ca. 1.0 mm

- 12 - wide. Each seed is pendulous, attached ventrally near the apex of the locule and shows a small projection near the base that may represent the chalaza (Figs. 34, 35, 37). The seed surface is composed of transversely elongated cells ca. 36 µm broad and ca. 15 µm high (Fig. 36). The seed coat is composed a sclerified epidermis with two cell-layers (Fig. 38).

Systematic affinities

The order Cornales includes woody or subligneous plants, with small epigynous flowers. The flowers are usually bisexual, actinomorphic, 4-merous or less often 5-merous perianth, with the perianth adnate to ovary, gynoecium of 2-9 (mostly 2) united carpels with a single pendulous ovule in each locule, ovules unitegmic, one per carpel; fruit usually a drupe with a single unilocular to plurilocular stone (Cronquist 1981; APG 1998). The stone of the fruit drupe opens by subapical, adaxial valves at the time of germination (Cronquist 1981, Eyde 1988). The cornalean affinities of Hironoia fusiformis are indicated by the following characters: epigynous perianth and pulvinate disk, endocarp sclerenchymatous, one pendulous seed per locule, and locules opening by dorsal valves from the apex.

As currently circumscribed, the Cornales include the extant genera, Alangium, Cornus, Curtisia, Grubbia, Mastixia, Diplopanax, Nyssa, Camptotheca, Davidia plus the Hydrangeaceae, Loasaceae, and Hydrostachyaceae (Xiang et al. 1993, 1998; Magallón et al. 1999; Xiang 1999). The latter three families have recently been shown to have cornalean affinities through phylogenetic analyses based on multiple gene sequences, but they are distinguished from other members of the order, and from Hironoia, by their thin-walled capsular fruits that contain many seeds per locule.

Cornalean taxa with thick-walled stony endocarps, single-seeded locules, and dorsal germination valves include Alangiaceae (Alangium), Curtisiaceae (Curtisia), and Cornaceae, which, in the broad sense of Eyde (1988), includes Cornus, Mastixiaceae (Mastixia and Diplopanax), and Nyssaceae (Nyssa, Camptotheca, Davidia). Among these, Mastixiaceae and Nyssaceae, which usually group together in phylogenetic analyses based on molecular data, have stones composed mainly of intertwining fibers, whereas the other genera have stones composed of isodiametric sclereids (Xiang et al. 1998). Hironoia and the nyssoid-mastixioid group are similar in the composition of the endocarps, but Hironoia is distinguished from each genus of the nyssoids-mastixioids group by the number of locules, the elongated style, the fusiform shape and the small fruit size. Although the mosaic of characters in Hironoia precludes assignment to an extant genus, the fiber rather than sclereid composition of the fruit places it within the nyssoid-mastixioid group, and it is significant as a very early member of the cornalean clade (Table 1).

Table 1. Morphological characters of cornalean genera and Hironoia

- 13 - Cornus Alangium Davidia Nyssa Camptotheca Diplopanax Mastixia Curtisia Hironoia Flower Epigynous Epigynous Epigynous Epigynous Epigynous Epigynous Epigynous Epigynous Epigynous 1-2 locular, 1-2 (-4) 1-2 carpels, 6-9 carpels, 1-3 carpels, but the style 1 (-2) carpels, 4 carpels, 3-4 carpels, Gynoecium carpels, Unilocular locules locules locules with 2 or 3 locules locules locules locules branches Dry with Drupe, Drupe, Drupe, Drupe, papery Drupe, Drupe, Drupe, Drupe, longitudinally longitudinally longitudinally longitudinally exocarp, longitudinally longitudinally longitudinally longitudinally Fruit type grooved grooved grooved grooved endocarp grooved grooved grooved grooved stone stone stone stone thin and stone stone stone stone hardly stony Epigynous nectariferous Present Present Absent Present Present Present Present Present Present disk Endocarp Isodiametric Isodiametric Isodiametric Fibers Fibers Fibers Fibers Fibers Fibers tissue sclereids sclereids sclereids Axial vascular Absent Absent Absent Absent Absent Absent Absent Present Absent strand Germination Elongate Elongate Elongate Short, apical Short, apical Elongate Elongate Elongate Elongate valve Dorsal Present when infolds in Absent Absent Absent 2 or more Absent Present Present Absent Absent fruit locules loculed

Comparison with fossil taxa

The fossils described here are all from a single locality (Kamikitaba assemblage, Takahashi et al. 1999a), but very similar material occurs at other localities in Japan. Fossil fruits that may be referable to Hironoia, have been recovered from a locality (sample F11) along the Irimazawa River near Ouhisa-machi within the boundaries of Iwaki city. The sediments at this locality are of the Lower-Middle Tamayama Formation, Futaba Group (Early Santonian, Late Cretaceous). The material is currently represented by too few specimens to be studied in detail (Takahashi, unpublished data). Other specimens that may be referable to Hironoia are also known from the Late Cretaceous (possible Turonian-Santonian) of Hokkaido. The undetermined, trilocular fruit, illustrated based on a cross section of permineralized material from Hokkaido (Nishida 1991; Figs. 32, 34), appears to be morphologically and anatomically very similar to Hironoia (Figs. 20, 21, 22).

- 14 - Among the nyssoids, the extinct genus Amersinia is widespread in the Paleocene of North America, northeastern Russia and northeastern China (Manchester et al. 1999; Feng et al. 2002). Amersinia is interpreted as closely related to the extant genera Davidia and Camptotheca based on the composition of the endocarp. Amersinia obtrullata Manchester, Crane et Golovneva has globose to ellipsoid infructescences with four or five basal deciduous bracts and numerous obtrullate, trilocular fruits with epigynous calyces (Manchester et al. 1999). Each locule bears one seed and has a dorsal germination valve near the apex (Manchester et al. 1999). Hironoia is similar to Amersinia in the trilocular fruit structure, but distinguished from Amersinia by their fusiform shape and their smaller size. Nyssoids are further represented during the Tertiary by leaves and fruits of Nyssa from the Eocene of North America and Europe (Manchester 1994, 2002; Eyde 1997) and of Davidia from the Paleocene of North America (Manchester 2002) and Pliocene of Japan (Kokawa 1965; Tsukagoshi et al. 1997). Hironoia is most similar to Amersinia among the cornalean fossil taxa.

For the two putatively closely related genera Alangium and Cornus, there is a good fossil record during the Tertiary. Unequivocal fruits of Cornus are known from the Paleocene (Crane et al. 1990), as well as from the Eocene (Manchester 1994). The genus has a substantial fossil record through the remainder of the Tertiary and up to the present. Alangium is also well-represented by fruits from the Eocene of North America and Europe (Manchester 1994) and from younger Tertiary sediments of North America, Europe, and Asia (Eyde et al. 1969). Other possible Cornales from Cretaceous sediments include endocarps resembling Cornus from the Santonian-Campanian mesofossil assemblage of Åsen, southern Sweden (Friis in Eyde 1988, and personal communication) as well as recently discovered, three-dimensionally preserved flowers from Coniacian-Santonian strata of western Georgia, USA (Upatoi Creek locality), which show similarities with Hydrangeaceae (Magallón 1997). These fossil flowers have a general similarity with those of Fendlerella A. A. Heller et W. Torrey, but the dorsifixed stamens and psilate pollen grains are unknown among extant Hydrangeaceae and, therefore, the assignment of these flowers to the family is not secure (Magallón et al. 1999). Putative hydrangeaceous flowers have also been described from the Turonian of New Jersey (Crossman locality; Gandolfo 1998). Unequivocal hydrangeoid flowers are known from Eocene and younger rocks during the Tertiary (Mai 1985; Manchester and Meyer 1987; Collinson et al. 1993).

In slightly younger Late Cretaceous sediments (Maastrichtian) four genera of fossil mastixioid fruits (Beckettia, Eomastixia, Mastixicarpum, and Mastixiopsis) have been described from Germany (Knobloch and Mai 1984, 1986). By the Eocene, mastixioid fruit taxa were diverse and common in Europe (Reid and Chandler 1933, Mai 1985) and North America (Manchester 1994, 1999; Tiffney and Haggard 1996; Stockey et al. 1998) and the clade is well represented through the Neogene in Europe.

Based on current information on phylogenetic relationships within Cornales, and the presence of Hironoia in the Early Coniacian, its is evident that the lineages leading to several distinct groups within the order had already differentiated by the middle part of the Late Cretaceous. Further differentiation within the group clearly occurred through the later Cretaceous (as evidenced by the Maastrichtian mastixioids) such that by the Eocene most extant genera were already present. Additional differentiation and speciation within groups, such as the three major clades of Cornales, may have occurred more recently during the Neogene. In a broader context, Hironoia is significant in establishing the age the asterid clade, which contains today at least 85,000 species - more than a third of all species of extant angiosperms. The pivotal phylogenetic position of Cornales as the earliest diverging clade of the asterid group, combined with the Early Coniacian age (ca. 89 million years B.P.; Gradstein et al. 1995) of Hironoia, establishes a minimum age for the Asterid clade.

Acknowledgements. We are very grateful to Else Marie Friis and Patrick S. Herendeen for critical review and constructive comments on the paper. We thank Hisao Ando for providing geological insights, and Hiroshi Tobe for discussion about Cornales. This work was supported by Grants-in-Aid

- 15 - (08640891 and 09640827) from the Ministry of Education, Science, and Culture of Japan to M.T., and by fellowships from the Japan Society for the Promotion of Science in 1997 (S-97128) and 1998 (S-98106) to P.R.C. This work was also supported in part by US National Science Foundation Grants EAR-9614672 to P.R.C. and EAR 0174295 to S.R.M.

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