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Vol.8 No.8 August 2003
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Archaefructus – angiosperm precursor
or specialized early angiosperm?
Else Marie Friis1, James A. Doyle2, Peter K. Endress3 and Qin Leng4
1
Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden
Section of Evolution and Ecology, University of California, Davis, CA 95616, USA
3
Institute of Systematic Botany, University of Zurich, 8008 Zurich, Switzerland
4
Nanjing Institute of Geology and Palaeontology, CAS, 39 East Beijing Road, 210008 Nanjing, The People’s Republic of China
2
With molecular analyses indicating that angiosperms
are not closely related to any other extant seed plant
group, information from fossils might provide the only
basis for reconstructing their origin. Therefore the
description of a new Early Cretaceous angiosperm,
Archaefructus, placed as the sister of all extant angiosperms, has created much debate and optimism.
However, we question both the interpretation and the
analysis of Archaefructus, concluding that it might be a
crown-group angiosperm specialized for aquatic habit
rather than a more primitive relative.
The family Archaefructaceae [1] was established to
accommodate two extinct species, Archaefructus liaoningensis [2] and Archaefructus sinensis [1], from the Yixian
Formation in northeastern China. In the initial report [2],
A. liaoningensis was presented as the oldest known
angiosperm because the beds were dated as Late Jurassic.
However, radiometric dating strongly supports a midEarly Cretaceous age for the Yixian Formation [3], close to
the age of the first records of angiosperms in other areas
(Box 1).
The Archaefructaceae were defined as including small
herbaceous water plants with axillary branches terminating in reproductive organs, and with strongly dissected
leaves. Reproductive axes were assumed to be exposed
above water level and were described as solitary flowers
without perianth, with numerous stamens borne in
helically arranged pairs and numerous conduplicate
carpels borne in a helical or whorled arrangement and
maturing into multi-seeded follicles.
Ge Sun et al. [1] evaluated the phylogenetic position of
Archaefructus by including its morphological characters in
a combined three-gene molecular and morphological
analysis, which placed Archaefructus as the sister to
extant angiosperms. We will discuss the characters of
Archaefructus in detail and question aspects of their
interpretation. Our conclusions are based on published
descriptions and illustrations [1,2,4] and our own studies
of additional specimens housed in the Institute of
Vertebrate Paleontology and Paleoanthropology, CAS,
Beijing, China.
Corresponding author: Else Marie Friis ([email protected]).
Ovulate and microsporangiate organs
Reproductive axes are elongate with ovulate organs borne
distally and microsporangiate organs borne proximally.
Some specimens apparently have unisexual (ovulate) axes.
The organs are crowded in young specimens (Fig. 1a) but
spaced out in more mature specimens (Fig. 1b). Ovulate
organs are pedicellate and typically borne in pairs on each
pedicel (Fig. 2). They are elongate with an acuminate apex
and enclose few (A. liaoningensis) or many (A. sinensis)
ovules or seeds.
Although ovulate organs of Archaefructus have not
been shown to have all the features of carpels, in other
respects they are more like angiosperm carpels than they
are like the ovulate organs of other seed plants with
enclosed ovules (Box 2). However, it is not clear that they
were conduplicate (i.e. like a leaf folded lengthwise and
sealed along its margins), or that the fruits were follicles,
as described by Sun et al. [1,2]. Follicles open longitudinally along the ventral side. No such open fruits and
Box 1. Age and palaeoenvironment of Archaefructus
The Archaefructus fossils were all collected in the Yixian Formation,
outcropping in the western part of Liaoning Province in northeastern
China. The Yixian Formation is part of the Jehol Group, which has
yielded a wealth of exquisitely preserved fossil animals, most
notably feathered theropod dinosaurs and a diversity of early
birds. The sediments were deposited in a low-energy lacustrine
environment in a seasonally semiarid climate and are intercalated
with volcanic tuffs and basalts (the environment and biota are
reviewed in Ref. [3]). Although the faunal elements of the Jehol biota
exhibit exceptional preservation, the plant fossils rarely have cellular
details intact, and tissues are often replaced or infilled with pyrite
framboids and microcrystallines [33]. However, some fossil plants
have been preserved with many of the organs (roots, stems, leaves)
still in organic connection. This is unusual for Cretaceous plant
fossils and provides unique information about growth form in early
angiosperms. The only contemporaneous flora with whole-plant
preservation is the Crato flora from the Early Cretaceous of Brazil,
deposited in a similar low-energy lake system [34].
The thickness of the Yixian Formation reaches 4700 m, with plant
and animal fossils occurring throughout. The age of the Yixian
Formation has been much debated [35] but there is now strong
evidence from radiometric dating that it is Early Cretaceous [3,36–38].
The oldest Archaefructus is from the Jianshangou Bed, which is in
the lower part of the Yixian Formation and dated radiometrically to
, 125 million years, corresponding to the Barremian stage [3],
close to the age of the first well-known angiosperm floras
elsewhere [31,39].
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TRENDS in Plant Science
Vol.8 No.8 August 2003
Box 2. Reproductive structures of Caytonia and
angiosperms
Fig. 1. Line drawings showing details of the reproductive organs of Archaefructus
sp. (a) and Archaefructus liaoningensis (b,c) from the Early Cretaceous Yixian Formation of northeastern China. (a) Immature reproductive axis with densely spaced
ovulate organs (carpels). (b) Mature reproductive axes with carpels above (ovulate
zone) and microsporangiate organs (stamens) below (staminate zone). (c) Basal
part of a mature reproductive axis showing clustering of the stamens in the staminate zone; a few carpels of the ovulate zone are also shown. The paired arrangement of both the carpels and stamens is evident in several places (arrow heads).
Scale bar ¼ 1 cm. (a) Redrawn from Plate 32, Fig. 6, in Ref. [4]; (b) redrawn from
Plate 32, Fig. 3 in Ref [4]; (c) redrawn from Plate 31, Fig. 1, in Ref [4].
(a)
(b)
Ovulate zone
Staminat
zone
Fig. 2. A well-preserved specimen (B0112) of Archaefructus sinensis from the Early
Cretaceous Yixian Formation of northeastern China. (a) Portion of the plant with
small, dissected leaves and several reproductive axes attached to the stem. Most
axes are young with densely spaced reproductive organs, but one is mature with
the organs spaced out. (b) Details of the mature axis showing distinctly paired carpels (arrows). Scale bar ¼ 1 cm.
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Several non-angiospermous Mesozoic seed plants resemble Archaefructus and extant angiosperms in having enclosed ovules, but their
enclosing structures clearly differ from carpels or are poorly understood. The best examples are Caytonia (Caytoniales, a ‘Mesozoic
pteridosperm’ [16]), Irania (related to Czekanowskiales? [40]), and
Leptostrobus (Czekanowskiales [41]). Caytoniales were first
described by Hamshaw Thomas [42] from Yorkshire (UK) as Jurassic
angiosperms, but later Tom Harris [16] documented that Caytonia
had gymnospermous reproduction, with pollen germinating inside
the micropyles of the ovules. Subsequently, the homology of the
ovule-bearing structures (‘cupules’) with carpels was questioned.
The cupules appear to be borne in two rows on a bilateral axis, like
leaflets on the rachis of a compound leaf, unlike carpels, which are
borne like leaves on a radial stem. Caytonia cupules are circinately
curved toward the axis; their plane of symmetry is perpendicular to
the axis, and ovules form an arc perpendicular to this plane of
symmetry. By contrast, the ovulate structures of Archaefructus are
elongate and acuminate, their plane of symmetry is parallel to the
axis, and ovules are attached parallel to the plane of symmetry –
typical features of carpels. Leptostrobus also has ovulate organs
arranged along an axis. They consist of two valves, but each valve
seems to differ from a carpel in its symmetry and in bearing ovules in
an arc perpendicular to its plane of symmetry [41]. Irania also has
paired ovulate organs borne along an axis [40], but the detailed
structure of the organs is unknown and a more detailed comparison
is not possible.
The ovules of Caytonia have only one integument, rather than two,
the ancestral state in angiosperms [17]. Sun et al. [2] described ovules
of Archaefructus as bitegmic and anatropous (with two integuments
and a reflexed orientation), but unfortunately their structure is
uncertain. Even in well-preserved specimens (B0112, Fig. 2) we failed
to establish the number of integuments, nature of internal structures,
or orientation and attachment of ovules.
Because they both have four microsporangia, stamens of
angiosperms have often been compared with the synangia of
Caytoniales (Caytonanthus) [42]. These are borne in groups on
lateral stalks along an axis. The stalks often branch several times, but
occasionally there are only two or three synangia grouped closely on
an unbranched stalk, suggesting the arrangement in Archaefructus.
However, Caytonanthus synangia are radial structures with four
equally spaced microsporangia, rather than bilateral structures with
two pairs of sporangia on either side of a sterile connective, like
angiosperm stamens.
Caytonia has figured in discussions of angiosperm origin, but with
the cupules interpreted as homologous with the bitegmic ovules of
angiosperms, not with the carpels [12,14,43 – 46].
no dehiscence line were observed. Even in living material
it is often difficult to see whether carpels are conduplicate,
and it might be impossible in these fossils. Microtome
serial sections would be necessary, but the preservation
does not allow such studies. In Brasenia (Cabombaceae)
and Zannichellia (Zannichelliaceae) (two extant aquatics
belonging to near-basal angiosperm clades, one with
above-water flowers, the other with underwater flowers),
carpels look superficially like those of Archaefructus.
However, they are not conduplicate but completely
ascidiate (i.e. developing like a tube from a ring-like
primordium) [5,6]. Brasenia and Zannichellia have only
one or a few ovules per carpel, but Austrobaileya, another
extant basal angiosperm, has completely ascidiate carpels
with several ovules arranged in two rows [7].
Microsporangiate organs of Archaefructus are borne
in pairs or several together on a short common stalk
(Fig. 1b,c). Sun et al. [1] described these organs as typical
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bilateral angiosperm stamens with two pairs of microsporangia. This is not entirely clear from their figures or
the material we have examined, although some do seem to
show a connective between lateral pollen sacs, like typical
angiosperm stamens, and unlike the radial synangia of
Caytonanthus (Box 2).
Flower or inflorescence?
If Archaefructus is related to the angiosperms, how are its
reproductive axes best interpreted? Both carpels and
stamens are usually borne in pairs or several together
(Figs 1,2). Similar paired carpels and stamens are
unknown in multiparted angiosperm flowers. This
strongly suggests that the reproductive axes are not
flowers, but rather inflorescences consisting of male
flowers towards the base, each with two (sometimes one
or more) stamens, and female flowers consisting of one or
two carpels (or unicarpellate flowers borne singly or in
pairs) at the top. Furthermore, the arrangement of the
organs seems to vary from opposite to subopposite or
helical, which is also more typical of inflorescences than it
is of flowers.
Sun et al. [1] rejected the inflorescence interpretation
because of the absence of bracts or bract scars below the
individual organs. However, flowers in living angiosperms
do not always have a subtending bract (i.e. a bract on the
axis of the next lower order, in the axil of which the flower
is formed). Examples include Hedyosmum (Chloranthaceae) [8] and especially some members of the largely
aquatic monocot order Alismatales. Flowers of Alismatales
provide special analogies for delimiting flowers in Archaefructus. In some alismatalian families that flower underwater, flowers are unisexual and have few organs; for
example, in Cymodoceaceae, male flowers have two
stamens (as in Archaefructus), and in Najas (Hydrocharitaceae) and Zosteraceae they have only a single stamen,
and female flowers have a single carpel. Furthermore, in
some of these taxa, subtending floral bracts are missing
(e.g. Ruppiaceae [9] and Zosteraceae [10]). From the
perspective of living aquatic angiosperms with underwater flowers, the most straightforward interpretation is
that Archaefructus had unisexual flowers: the male
flowers usually with two stamens, the female flowers
with one or two carpels.
An underwater flowering habit could also provide a
functional explanation for the lack of a perianth in
Archaefructus. Most extant angiosperm groups with
underwater flowers have lost their perianth. The best
examples are in Alismatales, in which several taxa with
flowers borne above the water have a normal perianth,
whereas other, related taxa have underwater flowers
without a perianth (Cymodoceaceae, some Juncaginaceae,
some Hydrocharitaceae, Posidoniaceae, Ruppiaceae, Zannichelliaceae, some Zosteraceae). Examples from other
orders include Ceratophyllaceae (which have structures
that resemble perianth parts but are interpreted as bracts
because they sometimes have flowers in their axils [11]),
and Callitriche (Veronicaceae). Loss of perianth in underwater-flowering plants can easily be understood on
functional grounds: such flowers do not need protection
against water loss in young stages, so neither sepals nor
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Vol.8 No.8 August 2003
371
subtending floral bracts are necessary, and they do not
need to be optically attractive, so showy parts are not
necessary.
It is therefore likely that there is something wrong in
the original interpretation of Archaefructus, either lack of
consideration of the possibility that Archaefructus was a
completely submerged water plant, or the interpretation of
the flowers as completely lacking a perianth and bracts. If
the flowers had an underwater habit, it would resolve the
puzzle of some of the more unusual features of Archaefructus: unisexual flowers, absence of a perianth and
subtending floral bracts, and low organ number.
Sister group or crown-group angiosperm?
These arguments might not hold if Archaefructus is more
basal than all living angiosperms (i.e. below the crown
group – the most recent common ancestor of all living
angiosperms and its derivatives), which is what Sun et al.
[1] argued based on a cladistic analysis of six modern
outgroups, Archaefructus, 167 living angiosperm species,
molecular sequences of three genes, and 16 morphological
characters, scored in Archaefructus and living groups.
However, the four features that supported the basal
position of Archaefructaceae [1], as ancestral character
states shared with other seed plants, are problematical.
Three of these characters (numbered as in [1]) involve
leaves: (6) vein orders one, (7) laminar vein form
dichotomous, and (8) vein fusion nonanastomosing. Characters 7 and 8 appear redundant, and three fossil taxa
often proposed as closer outgroups of angiosperms,
glossopterids, Gigantopteris and Caytonia [12 –15], have
the angiosperm state of reticulate venation. Furthermore,
the finely dissected leaf morphology of Archaefructus is
unlike that of living outgroups. Such fine dissection
occurred in the earliest Palaeozoic seed plants (the
Sphenopteris leaf type). However, it is rare in Mesozoic
seed plants, with a few exceptions such as Stenopteris [16].
However, similar leaf dissection is common in aquatic
angiosperms, such as Cabomba (not included in the
analysis of [1]) in the near-basal order Nymphaeales,
Ceratophyllum, and some Ranunculaceae, where phylogenetic analyses imply it is derived [17,18].
The ancestral status of the fourth feature, (15) perianth
absent, depends on scoring the perianth as absent in the
outgroups (except Ephedra, scored 0/1). However, independent of our argument that a perianth is commonly lost
in aquatic plants, we question whether it is valid to score
presence or absence of a perianth in gymnospermous taxa
that lack flowers. A less biased scoring would be
‘unknown’, for not applicable. Conversely, perianth-like
sterile appendages do occur in at least one potential fossil
outgroup, Bennettitales [19].
To test whether omission of Cabomba and the treatment
of the perianth character influenced the inferred basal
position of Archaefructus, we added Cabomba to the
matrix (with no molecular characters and with leaves
scored as dissected) and scored the outgroups as unknown
for perianth. With these changes, it is more parsimonious
to associate Cabomba with Archaefructus than with
Brasenia, the one member of Nymphaeales in the matrix
and its sister group based on molecular and morphological
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Vol.8 No.8 August 2003
Monocots
Eumagnoliids
Chloranthaceae
Ceratophyllum
Eudicots
Austrobaileya
Schisandra
Illicium
Brasenia
Cabomba
Archaefructus
Amborella
Archaefructus
Extant outgroups
Crown group angiosperms
Fig. 4. Line drawing of Vitiphyllum – an Early Cretaceous leaf type characterized
by a ternate pattern of dissection (Baltimore, lower Potomac Group, Aptian). This
pattern is generally similar to that of Archaefructus, although the lobes are much
wider and the lamina has reticulate venation. Reproduced, with permission, from
[23].
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Fig. 3. Cladogram of Sun et al. [1], simplified, with Cabomba added, showing two
equally parsimonious positions for Archaefructus after scoring non-angiospermous outgroups as unknown (inapplicable) for perianth.
data [18,20]. However, if Cabomba is kept with Brasenia,
as supported by a great body of data, it is equally
parsimonious to place Archaefructus either with Cabomba
or below the angiosperms (Fig. 3). It is only one step less
parsimonious to link it with Ceratophyllum. Thus, judging
from this exercise, it is possible that Archaefructus is on the
stem lineage to angiosperms, but the evidence for this is
ambiguous. Proper exploration of this problem will require a
more comprehensive morphological analysis including more
characters and fossil as well as living outgroups.
It could be objected that leaves of Archaefructus differ
from those of Cabomba, which have several segments
radiating from one point, in having a ternate structure
(dividing into threes). However, in this respect Archaefructus is like the basal eudicot order Ranunculales, in
which some members have highly dissected leaves
(e.g. some Papaveraceae, aquatic species of Ranunculus).
A similar ternate pattern is also known in Early
Cretaceous (Aptian) leaves called Vitiphyllum [21 – 23],
although these are less finely dissected, with several
veins per lobe and reticulations among them (Fig. 4).
Hence it is possible that Archaefructus is not as
isolated in the Early Cretaceous as it seems. Leaves
compared with Vitiphyllum, although less well preserved and more problematical, have been described
from the Albian of Kazakhstan, attached to stems with
inflorescences called Caspiocarpus [24], which were
described as bearing few-seeded follicles. Vitiphyllum
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and Caspiocarpus have been related to Ranunculales
based on leaf architecture and fruit type [24,25].
These observations raise the possibility that Archaefructus is an early eudicot. Eudicots are characterized by
tricolpate pollen (with three longitudinal germination
furrows), which appears globally in the Albian, but
extends back to the Barremian – Aptian [26 – 28], the age
of Archaefructus. A eudicot affinity could be consistent
with the paired arrangement of stamens and carpels in
Archaefructus: dimerous floral organization is common
in basal eudicots (e.g. Papaveraceae, Proteaceae, Tetracentron, Buxaceae), and phylogenetic analyses are consistent with the hypothesis that it is ancestral in the group
[17,29]. The presence of eudicots in the Yixian Formation
is also suggested by the discovery of another fossil plant
with features suggesting a position among near-basal
eudicots (e.g. syncarpous gynoecium) [30].
Pollen grains are usually valuable systematic markers.
Unfortunately, although Sun et al. [1,4] isolated material
from the anthers that they described as monosulcate
pollen, the organic preservation is poor and the pollen
grains are not convincing. They are unusual in their
irregular and angular shape (shown in Refs [1,4]) and their
wide size range (17 – 36 mm). Furthermore, no details are
known about the pollen wall structure.
Conclusions
Although Archaefructus provides important new data on
the early diversification of angiosperms, it is premature to
conclude that it is relevant to their origin. Our interpretation of Archaefructus as a totally submerged water plant
with small, simple and unisexual flowers is in accordance
with inferences from molecular analyses that aquatic
lineages evolved early in the radiation of angiosperms,
both in the near-basal orders Nymphaeales and
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Ceratophyllales and among basal monocots. Our interpretation is also in good agreement with the fossil record of
Early Cretaceous floral structures from Europe and North
America [31,32] where small, simple flowers are predominant. However, whatever its phylogenetic position,
Archaefructus is significant in our understanding of the
early morphological and ecological radiation of angiosperms, especially the existence of multiple early trends
toward an aquatic habit.
Acknowledgements
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We thank Jürg Schönenberger for valuable input and discussion.
References
1 Sun, G. et al. (2002) Archaefructaceae, a new basal angiosperm family.
Science 296, 899 – 904
2 Sun, G. et al. (1998) In search of the first flower: a Jurassic angiosperm,
Archaefructus, from northeast China. Science 282, 1692 – 1695
3 Zhou, Z. et al. (2003) An exceptionally preserved Lower Cretaceous
ecosystem. Nature 421, 807 – 814
4 Sun, G. et al. (2001) Early Angiosperms and Their Associated Plants
from Western Liaoning, China, Shanghai Scientific and Technological
Education Publishing House, China
5 Posluszny, U. and Sattler, R. (1976) Floral development of Zannichellia
palustris. Can. J. Bot. 54, 6541 – 6662
6 Endress, P.K. (2001) The flowers in extant basal angiosperms and
inferences on ancestral flowers. Int. J. Plant Sci. 162, 1111 – 1140
7 Endress, P.K. (1980) The reproductive structures and systematic
position of the Austrobaileyaceae. Bot. Jahrb. Syst. 101, 393 – 433
8 Endress, P.K. (1987) The Chloranthaceae: reproductive structures and
phylogenetic position. Bot. Jahrb. Syst. 109, 153– 226
9 Posluszny, U. and Sattler, R. (1974) Floral development of Ruppia
maritima var. maritima. Can. J. Bot. 52, 1607 – 1612
10 Hartog, C.D. (1970) The seagrasses of the world. Verh. K. Ned. Akad.
Wet. 59, 1 – 275
11 Endress, P.K. (1994) Evolutionary aspects of the floral structure in
Ceratophyllum. Plant Syst. Evol. 8 (Suppl.), 175 – 183
12 Stebbins, G.L. (1974) Flowering Plants, Evolution Above the Species
Level, Harvard University Press, Cambridge, MA, USA
13 Retallack, G. and Dilcher, D.L. (1981) A coastal hypothesis for the
dispersal and rise to dominance of flowering plants. In Palaeobotany,
Palaeoecology, and Evolution (Vol. 2) (Niklas, K.J., ed.), pp. 27 – 77,
Praeger Publishers, New York, NY, USA
14 Doyle, J.A. (1996) Seed plant phylogeny and the relationships of
Gnetales. Int. J. Plant Sci. 157, S3– S39
15 Li, X. ed. (1995) Fossil Floras of China Through the Geological
Ages Guangdong Science and Technology Press, Guangzhou, China
16 Harris, T.M. (1964) The Yorkshire Jurassic Flora II. Caytoniales,
Cycadales and Pteridosperms, British Museum (Natural History),
London, UK
17 Doyle, J.A. and Endress, P.K. (2000) Morphological phylogenetic
analysis of basal angiosperms: comparison and combination with
molecular data. Int. J. Plant Sci. 161, S121 – S153
18 Soltis, P.S. et al. (2000) Basal lineages of angiosperms: relationships and implications for floral evolution. Int. J. Plant Sci. 161,
S97 – S107
19 Crane, P.R. (1988) Major clades and relationships in the ‘higher’
gymnosperms. In Origin and Evolution of Gymnosperms (Beck,
C.B., ed.), pp. 218 – 272, Columbia University Press, New York, NY,
USA
20 Les, D.H. et al. (1999) Phylogeny, classification and floral evolution of
water lilies (Nymphaeaceae; Nymphaeales): a synthesis of nonmolecular, rbcL, matK, and rDNA data. Syst. Bot. 24, 28– 46
21 Fontaine, W.M. (1889) The Potomac or younger Mesozoic flora. U.S.
Geol. Surv. Monogr. 15, 1 – 377
22 Berry, E.W. (1911) Systematic paleontology, Lower Cretaceous:
Pteridophyta, Cycadophytae, Gymnospermae, Monocotyledonae,
http://plants.trends.com
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
373
Dicotyledonae. In Lower Cretaceous (Clark, W.B. et al., eds), pp.
214 – 596, The Johns Hopkins Press, Baltimore, MD, USA
Hickey, L.J. and Doyle, J.A. (1976) Pollen and leaves from the
mid-Cretaceous Potomac Group and their bearing on early
angiosperm evolution. In Origin and Early Evolution of Angiosperms (Beck, C.B., ed.), pp. 139 – 206, Columbia University Press,
New York, NY, USA
Vakhrameev, V.A. and Krassilov, V.A. (1979) Reproductive structures
of angiosperms from the Albian of Kazakhstan. Paleont. Zh. 1979,
121– 128
Doyle, J.A. (2001) Significance of molecular phylogenetic analyses for
paleobotanical investigations on the origin of angiosperms. Palaeobotanist 50, 167– 188
Hughes, N.F. and McDougall, A.B. (1990) Barremian – Aptian angiospermid pollen records from southern England. Rev. Palaeobot.
Palynol. 65, 145 – 151
Doyle, J.A. (1992) Revised palynological correlations of the lower
Potomac Group (U.S.A.) and the Cocobeach sequence of Gabon
(Barremian – Aptian). Cret. Res. 13, 337– 349
Friis, E.M. et al. (1999) Early angiosperm diversification: the diversity
of pollen associated with angiosperm reproductive structures in Early
Cretaceous floras from Portugal. Ann. Missouri Bot. Gard. 86,
259– 296
Drinnan, A.N. et al. (1994) Patterns of floral evolution in the early
diversification of non-magnoliid dicotyledons (eudicots). Plant Syst.
Evol. 8, 93 – 122
Leng, Q. and Friis, E.M. Sinocarpus decussatus gen. et sp. nov, a new
angiosperm with syncarpous fruits from the Yixian Formation of
Northeast China. Plant Syst. Evol. (in press)
Crane, P.R. et al. (1995) The origin and early diversification of
angiosperms. Nature 374, 27 – 33
Friis, E.M. et al. (2000) Fossil floral structures of a basal angiosperm
with monocolpate, reticulate-acolumellate pollen from the Early
Cretaceous of Portugal. Grana 39, 226 – 245
Leng, Q. and Yang, H. (2003) Pyrite framboids associated with the
Mesozoic Jehol Biota in northeastern China: implications for
microenvironment during early fossilization. Prog. Nat. Sci. 13,
206 – 212
Mohr, B. and Friis, E.M. (2000) Early angiosperms from the Aptian
Crato Formation (Brazil), a preliminary report. Int. J. Plant Sci. 161,
S155 – S167
Barrett, P.M. (2000) Evolutionary consequences of dating the Yixian
Formation. Trends Ecol. Evol. 15, 99 – 103
Swisher, C.C. et al. (1999) Cretaceous age for the feathered dinosaurs
of Liaoning, China. Nature 400, 58 – 61
Swisher, C.C. et al. (2002) Further support for a Cretaceous age
for the feathered-dinosaur beds of Liaoning, China: new 40Ar/39Ar
dating of the Yixian and Tuchengzi formations. Chin. Sci. Bull. 47,
135 – 138
Wang, S-S. et al. (2001) The existing time of Sihetun vertebrate in
western Liaoning – evidence from U– Pb dating of zircon. Chin. Sci.
Bull. 46, 779– 781
Friis, E.M. et al. (2000) Reproductive structure and organization of
basal angiosperms from the Early Cretaceous (Barremian or Aptian) of
Western Portugal. Int. J. Plant Sci. 161, S169 – S182
Schweitzer, H-J. (1977) Die räto-jurassischen Floren des Iran und
Afghanistans. Palaeontogr. B 161, 98 – 145
Harris, T.M. (1951) The fructification of Czekanowskia and its allies.
Philos. Trans. R. Soc. London Ser. B 235, 438 – 508
Thomas, H.H. (1925) The Caytoniales, a new group of angiospermous
plants from the Jurassic rocks of Yorkshire. Philos. Trans. R. Soc.
London Ser. B 213, 299 – 363
Gaussen, H. (1946) Les Gymnospermes, actuelles et fossiles. Trav.
Lab. for. Toulouse. T. II 1, 1 – 130
Crane, P.R. (1985) Phylogenetic analysis of seed plants and the origin
of angiosperms. Ann. Missouri Bot. Gard. 72, 716 – 793
Doyle, J.A. (1978) Origin of angiosperms. Annu. Rev. Ecol. Syst. 9,
365– 392
Doyle, J.A. and Donoghue, M.J. (1986) Seed plant phylogeny and the
origin of angiosperms: an experimental cladistic approach. Bot. Rev.
52, 321 – 431