Kaj Raunsgaard Pedersen

Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous

Phylogenetic analyses have identified the water lilies (Nymphaeales: Cabombaceae and Nymphaeaceae), together with four other small groups of flowering plants (the ‘ANITA clades’: Amborellaceae, Illiciales, Trimeniaceae, Austrobaileyaceae), as the first diverging lineages from the main branch of the angiosperm phylogenetic tree, but evidence of these groups in the earliest phases of the angiosperm fossil record has remained elusive. Here we report the earliest unequivocal evidence, based on fossil floral structures and associated pollen, of fossil plants related to members of the ANITA clades. This extends the history of the water lilies (Nymphaeales) back to the Early Cretaceous (125–115 million years) and into the oldest fossil assemblages that contain unequivocal angiosperm stamens and carpels. This discovery adds to the growing congruence between results from molecular-based analyses of relationships among angiosperms and the palaeobotanical record. It is also consistent with previous observations that the flowers of early angiosperms were generally very small compared with those of their living relatives.

Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales

Over the past 25 years the discovery and study of Cretaceous plant mesofossils has yielded diverse and exquisitely preserved fossil flowers that have revolutionized our knowledge of early angiosperms, but remains of other seed plants in the same mesofossil assemblages have so far received little attention. These fossils, typically only a few millimetres long, have often been charred in natural fires and preserve both three-dimensional morphology and cellular detail. Here we use phase-contrast-enhanced synchrotron-radiation X-ray tomographic microscopy to clarify the structure of small charcoalified gymnosperm seeds from the Early Cretaceous of Portugal and North America. The new information links these seeds to Gnetales (including Erdtmanithecales, a putatively closely related fossil group), and to Bennettitales—important extinct Mesozoic seed plants with cycad-like leaves and flower-like reproductive structures. The results suggest that the distinctive seed architecture of Gnetales, Erdtmanithecales and Bennettitales defines a clade containing these taxa. This has significant consequences for hypotheses of seed plant phylogeny by providing support for key elements of the controversial anthophyte hypothesis, which links angiosperms, Bennettitales and Gnetales.

Reproductive Structure and Organization of Basal Angiosperms from the Early Cretaceous (Barremian or Aptian) of Western Portugal

A survey of five mesofossil floras from the Early Cretaceous (Barremian or Aptian) of Portugal documents considerable taxonomic and structural diversity among early angiosperms. Currently ca. 140–150 different angiosperm taxa have been identified in these floras, of which ca. 85% are taxa at the magnoliid grade—perhaps also with some basal monocots. Evidence is beginning to emerge that those lineages identified as basal among angiosperms in phylogenetic analyses (recently referred to as the ANITA grade of basal magnoliids, including Amborellaceae, Nymphaeales, Illiciales, Trimeniaceae, and Austrobaileyaceae) were already well represented in the Early Cretaceous, at which time they were probably more diverse than they are today. Many of the fossil angiosperms from the Portuguese floras cannot be assigned to any existing group, and there is clear evidence of significant extinction.

Lauraceous Flowers from the Potomac Group (Mid-Cretaceous) of Eastern North America

Fossil inflorescences and flowers of Mauldinia mirabilis gen. et sp. nov. are described from the early Cenomanian Elk Neck beds of northeastern Maryland, U.S.A., and are assigned to the family Lauraceae. Specimens are exceptionally well preserved and provide the earliest evidence of trimerous floral organization and endosperm in angiosperms. Inflorescences are compound and consist of elongated axes bearing distinctive, spirally arranged lateral, bilobed cladode-like units. Each lateral unit typically bears five sessile bisexual flowers on the adaxial surface. Flowers have a perianth of three small outer and three larger inner tepals, and an androecium of nine fertile stamens in three whorls. In addition, there is an inner fourth whorl of three dorsiventrally flattened staminode-like structures, and each of the three fertile inner stamens has an associated pair of staminode-like appendages with clavate-sagittate heads. Anthers dehisce by two valves that are hinged distally. The gynoecium consists of a superior, unilocular carpel with a single anatropous, pendent ovule. Floral organization in M. mirabilis is the same as that of many extant Lauraceae, and the unique inflorescence structure can also be interpreted in terms of inflorescence patterns in extant taxa. Mauldinia mirabilis is the first unequivocal documentation of Lauraceae from the Cretaceous and provides further evidence for considerable diversity among magnoliid dicotyledons at an early phase in angiosperm diversification.

Diversity in obscurity: fossil flowers and the early history of angiosperms

In the second half of the nineteenth century, pioneering discoveries of rich assemblages of fossil plants from the Cretaceous resulted in considerable interest in the first appearance of angiosperms in the geological record. Darwins famous comment, which labelled the ‘rapid development’ of angiosperms an ‘abominable mystery’, dates from this time. Darwin and his contemporaries were puzzled by the relatively late, seemingly sudden and geographically widespread appearance of modern-looking angiosperms in Late Cretaceous floras. Today, the early diversification of angiosperms seems much less ‘rapid’. Angiosperms were clearly present in the Early Cretaceous, 20–30 Myr before they attained the level of ecological dominance reflected in some mid-Cretaceous floras, and angiosperm leaves and pollen show a distinct pattern of steadily increasing diversity and complexity through this interval. Early angiosperm fossil flowers show a similar orderly diversification and also provide detailed insights into the changing reproductive biology and phylogenetic diversity of angiosperms from the Early Cretaceous. In addition, newly discovered fossil flowers indicate considerable, previously unrecognized, cryptic diversity among the earliest angiosperms known from the fossil record. Lineages that today have an herbaceous or shrubby habit were well represented. Monocotyledons, which have previously been difficult to recognize among assemblages of early fossil angiosperms, were also diverse and prominent in many Early Cretaceous ecosystems.

Angiosperm floral structures from the Early Cretaceous of Portugal

Rich fossil floras including structurally preserved flowers, fruits, seeds and dispersed stamens have recently been extracted from mid-Early Cretaceous sediments from Portugal. The material illustrates considerable morphological variability in number and arrangement of floral parts, with the most diversity among magnoliid taxa; relatively few eudicots have been identified. Generally the flowers are small with undifferentiated perianth and massive androecium, and include both bisexual and unisexual forms. The most unexpected result of this study of Early Cretaceous flowers from Portugal is the presence of several epigynous forms at this early stage of angiosperm evolution.

Palaeobotanical evidence on the early radiation of magnoliid angiosperms

Early to mid-Cretaceous Potomac Group sediments have yielded a number of well-preserved angiosperm flowers, fruits, seeds, and dispersed stamens. The most diverse assemblage from the Early Cretaceous part of the sequence is from the Puddledock locality, Virginia, eastern USA. This material is of Early to Middle Albian age and is particularly rich in magnoliid and hamamelidid angiosperms. Flowers and fruits from the Puddledock flora are mostly simple and few-parted and so far only two reproductive structures with numerous parts have been recovered. In this paper we focus on floral organs showing magnoliid features, some of which may be compared to extant taxa, at least at the level of order and perhaps family. Other floral organs are more difficult to classify. Fossils from the Puddledock locality document the earliest appearance of calycanthaceous, and possible lauraceous, floral characters. As recorded also from the Early Cretaceous floras of Portugal, several different kinds of epigynous angiosperm and angiosperm-like reproductive structures are present. The discovery of small Circaeaster-like spiny fruits with monocolpate pollen is especially significant.

Virginianthus calycanthoides gen. et sp. nov.-A Calycanthaceous Flower from the Potomac Group (Early Cretaceous) of Eastern North America

We describe a new well-preserved fossil flower, Virginianthus calycanthoides gen. et sp. nov., from the Early Cretaceous (Early or Middle Albian) of Virginia. The flower is multipartite and has a distinct, deep floral cup. The perianth and androecium are borne on the rim of the floral cup and arranged in several crowded series. Reconstruction of the flower indicates that the perianth is composed of about 12 closely spaced tepals with apically directed hairs on the abaxial surface. The androecium consists of approximately 30-40 closely spaced, sessile stamens. The anthers are dithecate and tetrasporangiate, with the pollen sacs borne toward the abaxial surface. Dehiscence is extrorse through laterally hinged valves. Pollen grains are monocolpate and reticulate and resemble the previously described pollen species Clavatipollenites minutus Brenner. Sterile structures in the transition zone between androecium and gynoecium are interpreted as inner staminodes. The gynoecium is composed of approximately 18-26 carpels borne in several series on the inner surface of the hypanthium. The flower is closely comparable to extant members of the family Calycanthaceae (including Idiospermum) and constitutes the earliest documentation of calycanthoid features in the fossil record. Differences from extant Calycanthaceae are mainly in details of the pollen sacs, anther dehiscence, and pollen morphology.

Reproductive structure and function in CretaceousChloranthaceae

Fossil chloranthoid androecia,Chloranthistemon endressii gen. et spec. nov. are described from the Upper Cretaceous (Upper Santonian or Lower Campanian) of Scania, southern Sweden. They are three-lobed and dorsiventrally flattened with all pollen sacs borne laterally and inclined toward the presumed adaxial surface. The central lobe bears two pairs of pollen sacs, the lateral lobes a single pair each. The morphology, anatomy and valvate dehiscence of the fossil androecia is very similar to that seen in extant species ofChloranthus andSarcandra, but the in situ pollen differs from that of all extantChloranthaceae in being spiraperturate. A single chloranthoid androecium from the Lower Cretaceous (Upper Albian) of Maryland, North America has a more generalized structure thanChloranthistemon endressii. It consists of three stamens that are fused at the base, and each stamen bears two pairs of oppositely positioned pollen sacs. Combined with anatomical information from recentChloranthus the Lower Cretaceous specimen suggests that the androecium in the living genus has arisen by fusion and other modifications of three separate stamens each with a normal complement of four pollen sacs. The structure of both the Upper and Lower Cretaceous androecia suggest that these fossilChloranthaceae were insectpollinated. Macrofossil evidence combined with information from dispersed pollen indicates that theChloranthaceae diversified early in angiosperm fossil history and were an important component of Mid-Cretaceous plant communities.

Early Cretaceous mesofossils from Portugal and eastern North America related to the Bennettitales-Erdtmanithecales-Gnetales group

Four new genera and six new species of fossil seed (Buarcospermum tetragonium, Lignierispermum maroneae, Lobospermum glabrum, L. rugosum, L. stampanonii, Rugonella trigonospermum) are described from five Early Cretaceous mesofossil floras from Portugal and eastern North America. The four genera are distinguished by differences in size, shape, and details of seed anatomy, but all are unusual in having an outer seed envelope with a distinctive anatomical structure that surrounds the nucellus and the integument. The integument is extended apically into a long, narrow micropylar tube. The four new genera are part of a diverse, but previously unrecognized, complex of extinct plants that was widespread in Early Cretaceous vegetation and that coexisted in similar habitats with early angiosperms. The distinctive structure of these seeds, and the strong similarities to other fossil seeds (Ephedra, Ephedripites, Erdtmanispermum, Raunsgaardispermum, and some Bennettitales) already known from the Early Cretaceous, suggests that this newly recognized complex of extinct plants, together with Bennettitales, Erdtmanithecales, and Gnetales (the BEG group), is phylogenetically closely related.