Else Marie Friis

Angiosperms (flowering plants) are ecologically dominant in most terrestrial vegetation today, accounting for the bulk of the primary productivity on land. They constitute the most species-rich group of land plants that ever existed, with an overwhelming morphological diversity of flowers and growth forms ranging from the tiniest duckweed to the tallest trees. They also occur in most ecosystems on land

■n from deserts to coastal swamps and even have representatives living in the oceans. Despite their prominent position in the modern world, the an-giosperms diversified very late in the history of land plants and their rise to ecological dominance took place over a relatively short time interval during the Cretaceous, more than 300 million years after plants' first invasion onto the land.

The earliest unequivocal angiosperm fossils are pollen grains from Valanginian—Hauterivian strata of Israel (Brenner, 1996) and southern England (Hughes, 1994), about 130— 135 million years old. Angiosperms are rare in these earliest Cretaceous strata but by the Barremian—Aptian, 10—15 million years after their first occurrence, they were already widely established, and the transition from the ancient Mesozoic vegetation, dominated by gymnosperms (cycads, ginkgos, seed ferns, bennettitaleans, conifers) and pteridophytes (lycopods, horsetails, ferns), to the modern ecosystems was well under way.

Plum trees, tea bushes, walnut trees, sunflowers, rice, and the crops that give us our breakfast cereals are among the familiar angiosperms essential to our everyday lives. The first angiosperms shared many features with their present-day descendants, but they were also different. How different, we do not fully know. The origin and early diversification of angiosperms have been intensively studied for more than 100 years, but many questions remain unresolved regarding the time of their origin, their

Else Marie Friis

i251 Archaefruetus sinensis, an aquatic plant (preserved main axis 15 cm long), from Dawangzhangzi locality (Dawangzhangzi lied of Yixian Formation) in t.ingyuan. Liaoning (ca. i25 or 122 Ma). The left picture shows the close-up view of a reproductive axis. (Photo: Yvonne Arremo/ NRM)

ancestral features, and their closest relatives among other plant groups. So far there are neither clear signals from molecular studies nor universally accepted theoretical models on angiosperm evolution. Therefore, information from the fossil record is crucial to our understanding of angiosperm evolution and for testing various models for their phylogenetic relationships.

The Jehol Group sediments were deposited during the early phases of this Cretaceous vegetational revolution and provide a window to study changes and innovations in Early Cretaceous floras. The deposits preserve a biota that either lived in or was trapped in a system of low-energy lakes. There is no or little indication of transportation prior to fossilization. Some of the plant fossils are preserved as whole plants with roots, stems, leaves and reproductive organs in organic connection, and some of the plants were obviously aquatic. Whole plant preservation is very rare in the fossil record and has been reported only from a few places around the world. Fossil remains of whole water plants are even more unusual because they typically have very delicate structures with low fossilization potential. The Jehol plant assem blage thus provides insight into a part of the vegetational history that is poorly known. Despite the deposition that resulted in whole plant preservation and excellent information on gross morphology, plant fossils from the Jehol sediments have experienced rapid tissue decay during the very early stage of fossilization, which destroyed most of the cell-level structures (Leng and Yang, 2003). This, along with the highly specialized features of water plants, sometimes makes interpretations and systematic inferences very difficult.

History of the search for Jehol angiosperms The first Jehol plants assigned to angiosperms were Potamogeton jeholensis Yabe et Endo and Potamogeton? sp. reported by two Japanese botanists H. Yabe and S. Endo in 1935, but an intensive search for angiosperms did not start until about 60 years later and several putative angiosperms were recently described from the Yixian Formation. The Late Jurassic age assignment of the lower Yixian Formation that was adopted by some authors gave the fossils an older age than angiosperms from other places and certainly contributed to the excitement of the search. The mid-Early Cretaceous age that is now widely accepted (Zhou

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An inflorescenc^aboiii 6.5 cm long) of ArchaefructusfliaiHiingensis with female (Upper) and male (Lower) organs, from Huangbanjigbit locality (Jianshangou Bed ofYixian Formation) in.Beipiao. Liaoning (ca. 125 Ma). (Photo; Yvonne Arremo/ NRM)

Archaefructus Sinensis

MB 253 An almost complete plant (13.4 cm long) of Archaefructus sinensis, from Dawangzhangzi locality (Dawangzhangzi Bed of Yixian Formation) in Lingyuan, Uaoning lea. 125 or 122 Ma). (Photo: Yvonne Arreino/ NRM)

et ill., 2003) places tlic fossils in another context as coeval with early angiosperm floras from other regions. Among the fossil plants that have been recently related to the angiosperms are Cbaayangia Hangst Dnan (Duan, 1997); Eragrosites cbangn Cao et Wu, Liaoxia cbenu Cao et Wu, and "Monocotyledon Leaf' (Cao et al., 1998); Ereniastenoptera Krassilov, Lilites reheensis Wu, Orchidites linearifolius Wu, Orchidites lamtfoliits Wu, Trapa? sp., and Typhaera fusiformis Krassilov (Wu, 1999); Archaefructus liaoningensis Sun,

Dilcher, Zheng et Zhou (Sun et al., 1998) and A. sinensis Sun, Dilcher, Ji er Nixon (Sun et al., 2002); Beipiaoaparva Dilcher, Sun et Zheng, B. rotunda Dilcher, Sun et Zheng, and B. spittosa Dilcher, Sun et Zheng (Sun et a!., 2001); and Sinocarpus decnssaius Leng et Friis (Leng and Friis, 2003). Other putative angiosperms were described based on very fragmentary or poorly preserved material (e.g. several taxa described under the heading "Problematic Angiosperms" by Wu, 1999) and are not discussed further here.

SinocarpusArchaefructus Sinensis

The rapid decay prior to fossilization and possible morphological specialization ot some of the plants to an aquatic environment make it difficult to interpret the morphology and structures. Interpretation and systematic assignment have subsequently been questioned tor many ot these fossils. Chaoyangia liattgii. Eragrosites changii, Liaoxia chenii and Porantogeton jeholensis (later reassigned to Ranunculus jeholensis by Miki, 1964) show distinct affinity with members of the relict seed plant group Gnetales and two of them, Eragrosites changii and Liaoxia chenii were transferred to the extinct genus Epheilrites (Guo and Wu, 2000). Potamogentonl sp., the "Monocotyledon Leaf', Lilites, and the two species of Orchidiles were re-interpreted as conifers (Sun et al., 2000, 2001), an assignment that is also problematic (see below). Archaefructus was originally described as bearing multiparted bisexual and naked flowers and was resolved as sister to all extant angiosperms (Sun et al., 1998, 2002). This interpretation has also been questioned and an alternative explanation offered (Frns et al., 2003), and the possibility that Archaefructus is more closely related to other seed plants was discussed by Zhou and others (2003). In the following sections we comment briefly on fossil plants that srill remain of interest in the discussion on Early Cretaceous angiosperm structure and diversity.

Archaefructus—a submerged water plant The extinct genus Archaefructus was established by Sun and others (1998). The original description included a single species, A. liaoningensis, which was known

■■256 Reconstruction of Sinocarpus decussatus. (Art: Qin l.eng and Yu-gao Ren/ NICP)

1254 Sinocarpus decussatus (5 cm long), an angiosperm with advanced features, from Dawangzhangzi locality (Dawangzhangzi Bed ofYixian Formation) in Lingyuan. Liaoning (ca. 125 or 122 Ma). (Photo: Yvonne Arremo/ NRM)

■hbmh i255 A close-up view of the partly united carpels of the specimen shown in Fig, 254 (Photo: Xiao-yi FaiV N1GP)

only from fragments of reproductive axes. Later more complete specimens were found and an additional species, A. sinensis, was described (Sun et al., 2002). Archaefmctus includes small herbaceous plants with axillary branching and elongated terminal reproductive axes (Figs. 251—253). Their general habit and morphology, particularly the strongly dissected leaves, indicate that the Archaefmctus plants were aquatic. The reproductive axes have ovulate (female) organs above and microsporangiate (male) organs below (Fig. 252). The ovulate organs are often borne in pairs and the microsporangiate organs in clusters of one to four (Figs. 251, 253). The presence of critical angiosperm features of Archaefmctus has not been fully documented, and many of the reproductive features are still poorly understood. The morphology of the reproductive organs indicates that the ovulate organs might be carpels and the microsporangiate organs stamens as in angiosperms. Their arrangement in pairs or clusters along the axis suggests that each reproductive axis is an inflorescence with many laterally arranged flowers (Friis et al., 2003), rather than a single flower as originally described. Each flower in the inflorescence is simple and unisexual with only few parts. The female flowers above consist of one or two carpels and male flowers below one to four (typically two or three) stamens. The flowers are naked, which may be interpreted as a secondary loss. This is compatible with a submerged aquatic nature inferred for the flowers, since flowers underwater do not require perianth parts for protection against desiccation or for attracting pollinators. Similar simple and naked floral structures are typical for modern angiosperms specialized for flowering under water. The position of the inflorescence axes at different levels of the plants (Figs. 251, 253) also supports the interpretation of submerged flowers as do the lax appearance of some of the reproductive

■■¡257 Orchidites linearifblius. an uncertain angiosperm (6.7 cm long), w258 Orchidites lancifolius, an uncertain angiosperm (2.2 cm long!, from from lluangbanjigou locality (Jjanshangou Bed of Yixian Huangbanjigou locality (Jianshangou Bed of Yixian Formation) in

Formation) in Beipiao, Liaoning (ca. 125 Ma). (Photo: Xiao-yi Beipiao. Liaoning lea. 125 Ma). iPhoto: Xiao-yi FaiV NIGP) Fan,' NIGPI

■■¡257 Orchidites linearifblius. an uncertain angiosperm (6.7 cm long), w258 Orchidites lancifolius, an uncertain angiosperm (2.2 cm long!, from from lluangbanjigou locality (Jjanshangou Bed of Yixian Huangbanjigou locality (Jianshangou Bed of Yixian Formation) in

Formation) in Beipiao, Liaoning (ca. 125 Ma). (Photo: Xiao-yi Beipiao. Liaoning lea. 125 Ma). iPhoto: Xiao-yi FaiV NIGP) Fan,' NIGPI

Sinocarpus—an angiosperm with advanced features Sinocarpus decussatus comprises a single fragment of an infructescence axis (Figs. 254—256). The specimen is fossilized in the fruiting stage with fruits born on long, slender stalks in an opposite pattern (Figs. 254, 256). The fruits are from hypogynous flowers and composed of (3~) 4 carpels that are partly united. Although the fossil is incomplete and strongly compressed, it is clearly from an angiosperm mainly because of its united carpels. United carpels are generally regarded as a more derived feature in angiosperms and characteristic for most of the "higher" flowering plants called eudicots. The systematic position of Sinocarpus has not been established with certainty, but the fossil shows particular similarity to living eudicot plants that have a combination of derived and more primitive features of angiosperms as seen in members of the Ranunculaceae, Buxaceae, and Myrothamnaceae.

Other possible angiosperms The affinity of other putative angiosperms in the Jehol Flora is still uncertain. Since many of them are fragmentarily preserved or lack reproductive organs, we can only speculate until more information is available. Among these uncertain angiosperms are the vegetative branches of Potamogeton? sp., the "Monocotyledon Leaf", and the two species of Orchidites (Figs. 257, 258). All of them have leaves that in size and shape, venation pattern and arrangement are very similar to each other and may be conspecific. They all display long, linear and lax leaves with parallel venation, and in general appearance they resemble some monocotyledons and also some modern aquatic plants. They were all transferred to the conifers and included in the extinct taxon Liaoningocladus boii Sun, Zheng et Mei (Sun et al., 2001, 2000). Features supporting the affinity with conifers are not clear and the special (syndetocheilic) type of stomata described for Liaoningocladus is characteristic for angiosperms but absent in conifers. It is thus possible that these fossils are indeed angiosperms as first suggested, but their systematic affinity still remains to be studied in more detail. The putative angiosperm Lilites reheensis was also re-interpreted as a conifer and renamed Podocarpites reheensis (Wu) Sun et Zheng (Sun et al., 2001). However, for a full documentation of its systematic position, more details of venation pattern, epidermal structure, and reproductive organs are needed.

Some of the isolated reproductive organs from the Yixian Formation such as those described as Trapa? sp., Beipiaoaparva, B. rotunda and B. spinosa have sturdy spines (Fig. 259), a feature often seen in fruits and seeds of extant mm 259 A spiny fruit (seedl of Beipiaoa spinosa, an uncertain angiosperm (I cm long), from Huangbanjigou locality (Jianshangou Bed of Yixian Formation) in Beipiao, Liaoning (ca. 125 Ma). (Photo: Xiao-yi Fan' NIGP)

aquatic angiosperms, and these organs may also be produced by ancient water plants. But so far they have not been discovered in organic association with any vegetative structures and thus their full nature has yet to be clarified.

The Jehol angiosperms in a global context Although angiosperms are relatively rare in the Jehol Biota and different from plant fossils described from other regions, they are also in broader terms in good agreement with plants from other Barremian—Aptian floras. Small, simple and few parted unisexual flowers as known for Archaefructus are common in contemporaneous floras from Europe and North America and eudicots were established by this time at least in Africa, Europe and North America. The presence of aquatic plants early in the history of angiosperms has also been inferred based on fossils from other places, but so far whole plant evidence for an early specialization to aquatic environment has only been discovered in the Jehol Biota.

DensoisporiteS niicrorugiilatus, spore of a selaginellales

■■¡261 Tenuangulaspvris microverrucosus. spore of a possible selaginellales.

WM 262 Osmundaciditcs wellmanii. spore of a filicales.

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    Are dinosaurs are unisexual?
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