Brian A. Atkinson

HUBBARDIASTROBUS CUNNINGHAMIOIDES GEN. ET SP. NOV., EVIDENCE FOR A LOWER CRETACEOUS DIVERSIFICATION OF CUNNINGHAMIOID CUPRESSACEAE

Premise of research. The occurrence of six ovulate cones and six leafy branching systems, two of which show attachment of the ovulate cone, reveals a new cunninghamioid fossil conifer from the Cretaceous Apple Bay locality of Vancouver Island, Canada. This anatomically preserved plant expands our understanding of basal Cupressaceae in the fossil record. Methodology. Specimens were studied from anatomical sections prepared by the classic cellulose acetate peel technique. Pivotal results. Vegetative shoots have helically arranged Cunninghamia-like leaves with a single vascular bundle and one to three resin canals. Ovulate cones consist of numerous helically arranged bract/scale complexes with a large bract and a small ovuliferous scale with three separate tips. There are three inverted seeds/ovules attached adaxially, immediately proximal to the free scale tips. Conclusions. This discovery reveals the presence of a new genus and species of basal Cupressaceae, Hubbardiastrobus cunninghamioides, in the Early Cretaceous (Valanginian; ∼136 Ma) of the Northern Hemisphere. These data expand the species richness of fossil Cupressaceae and further document the Cretaceous evolutionary radiation of subfamily Cunninghamioideae.

Hughmillerites vancouverensis sp. nov. and the Cretaceous diversification of Cupressaceae.

UNLABELLED • PREMISE OF THE STUDY Two ovulate conifer cones, one of which is attached terminally to a short leafy shoot, reveal the presence of a new species of Hughmillerites in the Early Cretaceous Apple Bay flora of Vancouver Island, British Columbia, Canada. This ancient conifer expands the diversity of Cupressaceae in the Mesozoic and reveals details about the evolution of Subfamily: Cunninghamioideae.• METHODS Specimens were studied from anatomical sections prepared using the cellulose acetate peel technique.• KEY RESULTS Vegetative shoots have helically arranged leaves that are Cunninghamia-like. Seed cones have many helically arranged bract/scale complexes in which the bract is larger than the ovuliferous scale. Each ovuliferous scale has three free tips that separate from the bract immediately distal to an inverted seed. Several ovuliferous scales show interseminal ridges between seeds.• CONCLUSIONS This study documents a new extinct species of cunninghamioid conifers, Hughmillerites vancouverensis, expanding the record of the genus from the Late Jurassic to the Early Cretaceous. This new extinct species emphasizes the important role that conifers from subfamily Cunninghamioideae played in the initial evolutionary radiation of Cupressaceae. In light of recent findings in conifer regulatory genetics, we use H. vancouverensis to hypothesize that variations of expression in certain gene homologues played an important role in the evolution of the cupressaceous ovuliferous scale.

Anatomically preserved fossil cornalean fruits from the Upper Cretaceous of Hokkaido: Eydeia hokkaidoensis gen. et sp. nov.

PREMISE OF THE STUDY The basal asterid clade Cornales radiated during the Late Cretaceous. However, our understanding of early evolutionary patterns and relationships remain obscure. New data from five permineralized fruits in calcareous concretions from the Upper Cretaceous (Coniacian-Santonian) Haborogawa Formation, Hokkaido, Japan provide anatomical details that aid our knowledge of the group. METHODS Specimens were studied from cellulose acetate peels, and three-dimensional reconstructions were rendered using AVIZO. KEY RESULTS Fruits are drupaceous, roughly pyriform, 2.9-4.3 mm in diameter, with a fleshy mesocarp, transition sclereids, and a stony endocarp of four to five locules, with the septa forming a cross or star-like pattern in transverse section, distinct germination valves, and one apically attached anatropous seed per locule. Vascular tissue occurs in zones between the mesocarp and exocarp, in two rows within the septa, and prominent seed bundles can be traced throughout the fruit sections. Seeds have a single integumentary layer of radially flattened square to rectangular cells and copious cellular endosperm. A fully formed, straight, cellular dicotyledonous embryo, with closely appressed, spathulate cotyledons, is present within each seed. CONCLUSIONS The unique combination of characters shown by these fruits is found in Cornaceae, Curtisiaceae, and Davidiaceae and allows us to describe a new taxon of Cornales, Eydeia hokkaidoensis gen. et sp. nov., with many similarities to extant Davidia involucrata. These fossils underscore the phylogenetic diversification of Cornales that was underway during the Late Cretaceous and support the hypothesis that a Davidia-like fruit morphology is plesiomorphic within Cornales.

Tracking the Initial Diversification of Asterids: Anatomically Preserved Cornalean Fruits from the Early Coniacian (Late Cretaceous) of Western North America

Premise of research. The initial radiation of core eudicots (>70% angiosperm diversity) occurred during the Late Cretaceous (100.5–66 Ma). While there is strong fossil evidence for this diversification occurring throughout the Cenomanian (100.5–93.9 Ma) and Turonian (93.9–89.8 Ma), there are no unambiguous reports of the largest core eudicot clade, the asterids, from pre-Coniacian deposits (89.8–86.3 Ma). This study provides new insights into the early evolution of asterids by characterizing anatomically preserved fruits from the early Coniacian (∼89 Ma) of North America that represent three new taxa assignable to the earliest-diverging asterid order, Cornales. Methodology. Three fossil fruit types were identified within calcareous concretions from the Upper Cretaceous Eden Main locality on Vancouver Island, British Columbia. Specimens were prepared using the cellulose acetate peel technique. Pivotal results. These fruits have a thick-walled woody endocarp with germination valves, one apically attached seed per locule, and rows of vascular bundles in each septum but no central vascular bundle. The three fruit types differ from each and other cornalean fruits in endocarp size, sculpturing, and histology; thus, each type represents a new taxon: Eydeia vancouverensis sp. nov., Obamacarpa edenensis gen. et sp. nov., and Edencarpa grandis gen. et sp. nov. Conclusions. The taxa characterized in this study are contemporaneous with the previously recognized oldest cornalean, Hironoia fusiformis, from the early Coniacian of Japan. The diversity, geographic distribution, and stratigraphic age of these early cornaleans clearly indicate that the diversification of Cornales was well under way by the Coniacian.

The Early Phylogenetic Diversification of Cornales: Permineralized Cornalean Fruits from the Campanian (Upper Cretaceous) of Western North America

Premise of research. Two permineralized fruits have been found within a single calcareous concretion from the Upper Cretaceous (upper Campanian) Spray Formation of Vancouver Island, British Columbia. These fossils provide additional evidence for the initial phylogenetic diversification of Cornales, the earliest diverging asterid lineage. Methodology. Specimens were prepared using the cellulose acetate peel technique. Pivotal results. A new cornalean species, Suciacarpa xiangae sp. nov., is characterized on the basis of a well-preserved fruit specimen. This fruit is represented by a large ovoid tetralocular sclerenchymatous endocarp. Locules are crescent shaped in transverse section and accompanied by short dorsal germination valves. Valves consist of small isodiametric sclereids as well as a large number of large secretory cavities. The septum and central axis are composed of transversely oriented and interwoven fibers and elongate sclereids. There is no major central vascular bundle; however, there are numerous small bundles scattered within the septa. This fruit has one apically attached seed per locule. An additional cornalean taxon—Sheltercarpa vancouverensis gen. et sp. nov., also represented by a single smooth tetralocular sclerenchymatous endocarp—consists of isodiametric and a few elongate sclereids, with short germination valves, one seed per locule, and lacks a central vascular bundle. Conclusions. Because of unique combinations of characters, the two fruits described in this study represent two new cornalean taxa, S. xiangae sp. nov. and S. vancouverensis gen. et sp. nov. These fruits display mosaics of apomorphic and plesiomorphic characters that occur in families of at least two different major cornalean clades: Cornaceae/Alangiaceae and Nyssaceae/Mastixiaceae/Davidiaceae. The morphological diversity seen in these taxa and other cornaleans from the Late Cretaceous suggests that the Campanian was an important time for the initial phylogenetic diversification of Cornales.

Cretaceous origin of dogwoods: an anatomically preserved Cornus (Cornaceae) fruit from the Campanian of Vancouver Island.

Background Cornaceae consists of 58 species, all within the genus Cornus. The Cenozoic record of Cornus is extensive and well documented. Molecular divergence-time studies suggest that crown-group Cornus may have originated by the Late Cretaceous. However, there has been no formal report of Cornus from Cretaceous deposits. Here, we characterize a permineralized fossil fruit assignable to Cornus subg. Cornus from the Upper Cretaceous (Campanian) Shelter Point locality of Vancouver Island, British Columbia, Canada. Methods Serial sections of the specimen were made using the cellulose acetate peel technique. Peels were mounted onto microscope slides and studied by light microscopy. Results The fossil fruit consists of a tri-locular woody endocarp with dorsal germination valves. The locules are sub-triangular to ellipsoidal in transverse section and are separated by thin septa. Endocarp tissue consists of elongated and isodiametric sclereids and secretory cavities. Internal vascular tissue was not observed, but is interpreted to have been located along the outer periphery of the septa for some length, common in many cornalean taxa. There is one seed in each locule, one of which was found to have endosperm and a dicotyledonous embryo. Discussion Woody endocarps with germination valves, without central vascular bundles, and with one seed per locule are characteristic of several families within the order Cornales. The interpreted vascular pattern and presence of secretory cavities indicates that the fossil fruit is assignable to Cornus subg. Cornus. Comparative analysis suggests that the fossil is most similar to Cornus piggae, a species described from the Paleocene of North Dakota. This fossil is the first evidence of crown-group Cornaceae from the Cretaceous and sheds light on both the plesiomorphic fruit characters and the timing of the initial diversification of the family and basal asterid lineage, Cornales.

Lauraceous Flowers from the Eocene of Vancouver Island: Tinaflora beardiae gen. et sp. nov. (Lauraceae)

Premise of research. Twenty-one permineralized fossil flowers assignable to Lauraceae from the Eocene Appian Way locality on Vancouver Island, British Columbia, Canada, provide important anatomical and morphological data for interpreting evolutionary patterns in this diverse magnoliid family. Methodology. Consecutive anatomical sections were prepared using the cellulose acetate peel technique. Morphology and anatomy of the flowers were determined from anatomical sections, and three-dimensional reconstructions were rendered from serial sections using the software Amira. Pivotal results. Fossil flowers with oil bodies, trichomes, pollen, ovary anatomy, and other characters have allowed for the reconstruction of actinomorphic, pedicellate, and trimerous flowers with tepals in two whorls adnate to a shallow hypanthium. Nine fertile stamens occur in three whorls, the innermost of which bears paired glandular appendages, and a fourth whorl of sagittate staminodes surrounds the carpel. Anthers are tetrasporangiate. Stamens of the two outer whorls have median pollen sacs that are shorter than the two marginal pollen sacs. Third-whorl stamens have median pollen sacs that are longer than the marginal pollen sacs. Anthers of the first and second whorls are introrse, while the third-whorl anthers are extrorse. The fossil flowers have diagnostic characters of Lauraceae and are compared to flowers of extinct and extant taxa. Conclusions. The Eocene floral remains are assigned to Tinaflora beardiae gen. et sp. nov. We infer some aspects of floral biology based on different stages of development preserved among the fossils. The combination of well-preserved floral organs and in situ pollen is rare in the fossil record, allowing T. beardiae to expand the diversity of lauraceous floral morphology and provide further evidence for an Eocene radiation of the family in Laurasia.

Cunninghamia beardii sp. nov. (Cupressaceae: Cunninghamioideae), Anatomically Preserved Pollen Cones from the Eocene of Vancouver Island, British Columbia, Canada

Premise of research. A large pollen cone cluster attached to a cunninghamioid twig and surrounded by leaves has been identified from Eocene calcium carbonate marine concretions from the Appian Way locality on Vancouver Island, British Columbia, Canada. The cluster preserves 18 cones but probably bore at least 24 pollen cones based on cone placement in the cluster. Methodology. Specimens were studied using the cellulose acetate peel technique, and reconstructions were made with ImageJ visualization software. Pollen was examined using SEM. Pivotal results. Cones are helically arranged around the tip of an ultimate leafy branch that terminates in scale leaves, each showing a central resin canal. Vegetative leaves on the twig are amphistomatic, showing typical cunninghamioid anatomy, with a large central resin canal abaxial to the vascular bundle, an elongate zone of transfusion tissue, a nonplicate mesophyll, and a hypodermis three to four cells thick. Each pollen cone is produced in the axil of a bract and has three scale leaves surrounding the base of the cone axis. Individual pollen cones have helically arranged microsporophylls, each with three elongate abaxial pollen sacs. While the cones are immature, pollen sacs with pollen are present in several cones. The exine is scabrate, with numerous orbicules, and no papilla is evident. Conclusions. This cluster provides the first detailed anatomically preserved fossil evidence for the pollen cones of Cunninghamia. It shows a large number of similarities to the pollen cone clusters of extant Cunninghamia lanceolata and Cunninghamia konishii and the Late Cretaceous Cunninghamia taylorii, strengthening hypotheses for a basal position of cunninghamioids within the Cupressaceae and further demonstrating that some characters of Cunninghamia have remained relatively unchanged since at least the mid-Cretaceous.

Cupressaceous Pollen Cones from the Early Cretaceous of Vancouver Island, British Columbia: Morinostrobus holbergensis gen. et sp. nov.

Premise of research. Four small pollen cones bearing pollen have been found attached to a leafy twig in a calcareous concretion from the Valanginian Apple Bay locality, northern Vancouver Island, British Columbia, increasing the known morphological diversity of Early Cretaceous cupressaceous pollen cones. Methodology. Specimens were prepared using the cellulose acetate peel technique, pollen was examined using SEM, and three-dimensional reconstructions were rendered with Avizo. Pivotal results. The small, subglobose cones bear helically arranged microsporophylls with a central resin canal. Each sporophyll bears three abaxial pollen sacs. Walls of pollen sacs are comprised of radially elongated rectangular cells with prominent wall thickenings. Most pollen sacs are intact and contain numerous, nonsaccate pollen grains. Pollen is 16–24 μm in diameter with one exit papilla that forms a low protuberance on the grain. External surfaces of grains are scabrate with numerous orbicules and macrogranules, and the nexine is laminated. Cone and pollen morphology most closely resemble taxa of the taxodioid Cupressaceae. The number of pollen sacs per microsporophyll is similar to Athrotaxis, Metasequoia, Sequoia, Sequoiadendron, and the Paleogene fossil conifer Homalcoia. Arrangement of cones on branches differs from those of Athrotaxis, Metasequoia, and Homalcoia; pollen lacks the long distal papilla of Sequoia and Sequoiadendron and is most similar in size to that in some cupressoid Cupressaceae in Chamaecyparis, Thuja, and Juniperus but with a smaller aperture. Conclusions. This combination of features is unlike that found in any living or extinct species of Cupressaceae. The fossil species is described as Morinostrobus holbergensis gen. et sp. nov., furthering our understanding of character evolution within Cupressaceae s.l. and adding to the evidence that the Lower Cretaceous was a time of increasing cupressaceous diversity.

The Development and Structure of Cornalean Flowers and Fruits

The order Cornales (dogwood order) is the earliest diverging lineage within the most diverse group of flowering plants the asterids, which number over 80,000 living species [1]. This order contains an impressive diversity of flower and fruit morphologies, which makes Cornales an important resource for understanding the early evolutionary diversification of asterids. Fortunately, the Cornales is exceptional in having an excellent fossil record dating back to the Late Cretaceous (100-66 Ma), thus providing a rich source of crucial data for a wide range of evolutionary studies [2, 3]. Recent investigations have generated several hypotheses of cornalean evolution and systematics that remain untested by comparative morphological and anatomical studies, and fossils provide critical data both for testing those hypotheses and for reconstructing the early evolutionary history of the group [3].