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Early Cretaceous floral structures and in situ

tricolpatestriate pollen: New early eudicots from
Portugal
a

Kaj Raunsgaard Pedersen , Maria von Balthazar , Peter R. Crane & Else Marie Friis

Department of Geology, University of Aarhus, AarhusC, Denmark

Department of Palaeobotany, Swedish Museum of Natural History, Stockholm, Sweden

Department of Geophysical Sciences, University of Chicago, Chicago

Version of record first published: 02 Nov 2007.

To cite this article: Kaj Raunsgaard Pedersen , Maria von Balthazar , Peter R. Crane & Else Marie Friis (2007): Early
Cretaceous floral structures and in situ tricolpatestriate pollen: New early eudicots from Portugal, Grana, 46:3, 176-196
To link to this article: http://dx.doi.org/10.1080/00173130701526507

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Grana, 2007; 46: 176196

Early Cretaceous floral structures and in situ tricolpate-striate pollen:

New early eudicots from Portugal

KAJ RAUNSGAARD PEDERSEN1, MARIA VON BALTHAZAR2, PETER R. CRANE3

& ELSE MARIE FRIIS2
Downloaded by [Eastern Kentucky University] at 10:43 18 February 2013

Department of Geology, University of Aarhus, Aarhus-C, Denmark, 2Department of Palaeobotany, Swedish Museum of
Natural History, Stockholm, Sweden, and 3Department of Geophysical Sciences, University of Chicago, Chicago, USA

Abstract
Five new taxa with affinities to extant lineages that diverged at an early stage from the main line of eudicot evolution are
established from the Early Cretaceous (late Aptian or early Albian) Vale de Agua locality, Portugal. Staminate flowers of
Lusistemon striatus and pistillate flowers of Lusicarpus planatus are unisexual without rudiments of the opposite gender. They
are linked by the association of an unusual pollen type found in situ in the stamens and adhering to the stigmatic surface.
The staminate flower, Lusistemon striatus, is composed of six stamens subtended by small perianth parts. The arrangement
of the stamens is difficult to ascertain, but their variable sizes suggests a spiral arrangement. Pollen found in situ is tricolpate
and striate with densely-spaced, sparsely diverging and anastomosing muri that are aligned more or less parallel to the polar
axis. The muri have a conspicuous supratectal ornamentation of fine transverse ridges. The granular infratectal layer forms
an indistinct internal reticulum. The foot layer is thin. Pollen is closely similar to dispersed grains from the Aptian of Egypt
described as STRIOTRI-SEGMUR. It also resembles pollen of the dispersed pollen genus Rutihesperipites, as well as some
dispersed pollen assigned to Striatopollis. Pistillate flowers of Lusicarpus planatus consist of a bicarpellate, syncarpous
gynoecium borne on a short stalk. The styles are bent outwards and expose the double-crested stigmatic regions on their
ventral sides. The only organ preserved besides the gynoecium is a lateral scale-like organ at the base of the stalk. Pollen of
the same type found in Lusistemon striatus occurs on the stigmatic surface of the carpels. Comparisons with extant taxa
demonstrate that Lusistemon and Lusicarpus share many characters with early diverging groups of eudicots, in particular
Buxaceae. In addition to the Lusistemon-Lusicarpus flowers, the Vale de Agua samples also contain three other pistillate
reproductive structures that may be related to early diverging lineages of eudicots. Silucarpus camptostylus has a bicarpellate
and syncarpous gynoecium with two styles; Valecarpus petiolatus and Aguacarpus hirsutus have tricarpellate gynoecia that are
distinguished from each other in the shape and extension of the stigma as well as other details.

Keywords: Buxaceae, flowers, fossils, Portugal, Rutihesperipites, STRIOTRI-SEGMUR, Striatopollis

The eudicot clade comprises about 75% of extant

angiosperm species diversity. It is clearly defined by
its distinctive triaperturate pollen (Doyle & Hotton,
1991; Drinnan et al., 1994; Magallon et al., 1999)
and is also strongly supported by phylogenetic
analyses based on molecular data (e.g., Soltis &
Soltis, 2004). Triaperturate pollen grains are easy to
recognize in the fossil record and the oldest
palaeobotanical evidence of eudicots is provided by
dispersed tricolpate pollen grains from the
Barremian-Aptian transition about 120 million years
ago (Hughes & McDougall, 1990). Subsequently,

from Aptian and Albian deposits there is a greater

diversity of eudicot pollen types, indicating that the
group was already well established at that time and
that its initial diversification was well under way
(Hughes & McDougall, 1990; Penny, 1991; Doyle,
1992). In addition, eudicots are represented by a
diversity of leaf fossils in the later part of the Early
Cretaceous and mid-Cretaceous (e.g., Doyle &
Hickey, 1976). There is also an expanding record
of Early Cretaceous reproductive organs such as
flowers, fruits and dispersed stamens that can be
attributed to the group (e.g., Friis et al., 1988;

Correspondence: Else Marie Friis, Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, Sweden.
E-mail: else.marie.friis@nrm.se
(Received 12 March 2007; accepted 20 June 2007)
ISSN 0017-3134 print/ISSN 1651-2049 online # 2007 Taylor & Francis
DOI: 10.1080/00173130701526507

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Cretaceous flowers of early diverging eudicots

Crane, 1989; Drinnan et al., 1991; Crane et al.,
1993; Pedersen et al., 1994; Leng & Friis, 2003,
2006).
As in other areas of palaeobotanical research the
fossil record of early eudicots comprises mostly
fragmented and dispersed plant organs. One of the
difficulties in interpreting this early fossil record is to
determine, which of these dispersed plant organs
were produced by the same fossil species.
Discoveries of fossil flowers and detached reproductive structures with in situ pollen from the Early
Cretaceous (e.g., Friis et al., 1988, 2000b; Drinnan
et al., 1991; Crane et al., 1993; Pedersen et al.,
1994) have provided valuable information on the
parent plants of fossil eudicot pollen grains that were
previously only known from the dispersed microfossil record. In this paper we provide a further
example. We described five new fossil taxa from the
Early Cretaceous (Aptian or Albian) of Portugal
closely related to Buxales. Two of the taxa,
Lusistemon striatus Pedersen, von Balthazar, Crane
& Friis gen. et sp. nov. and Lusicarpus planatus
Pedersen, von Balthazar, Crane & Friis gen. et sp.
nov., comprise unisexual pistillate and staminate
flowers as well as stamens with the same kind of
tricolpate and striate pollen grains. Another pistillate
structure from the Vale de Agua locality, Aguacarpus
hirsutus Pedersen, von Balthazar, Crane & Friis gen.
& sp. nov., also has tricolpate and striate pollen
adhering to the stigmatic surface. This kind of pollen
is diverse in Early Cretaceous (Aptian and early
Albian) sediments (Penny, 1988) and the pollen
described here corresponds to one of the earliest
records of tricolpate-striate pollen currently recognised as STRIOTRI-SEGMUR from the Aptian of
Egypt (Penny, 1988). The pollen grains also
resemble dispersed Cretaceous pollen assigned to
the pollen genus Rutihesperipites S.K. Srivastava
(Srivastava, 1977) and Striatopollis Krutzsch
(Norris, 1967; Singh, 1971; Ward, 1986). Striate
tricolpate pollen has earlier been associated with the
fossil flowers of Spanomera Drinnan, Crane,
Pedersen & Friis (Drinnan et al., 1991). Several
characters of Spanomera suggest a relationship to
extant Buxaceae (Drinnan et al., 1991) and this is
also the case for the fossils described here. There are
also similarities with extant members of several other
families of early diverging eudicots as well as with
Saxifragales in the core eudicots. In addition to the
fossil flowers with striate pollen, two other taxa of
putative buxalean affinity are also described.
Material and methods
The material described here is from Early
Cretaceous sediments exposed in the opencast clay

177

pit complex near the small village of Vale de Agua in

western Portugal (39379150N, 8519300W). The
sediments at this locality consist predominantly of
grey, reddish or greenish fine-grained sediments of
Early Cretaceous age that were previously assigned
to the Complexos gresosos de Nazare e de CosJuncal (Carta Geologica de Portugal, 27-A Vila
Nova de Ourem, Zbyszewski et al., 1974). These
sediments have subsequently been included in the
Figueira da Foz Formation established by Dinis
(1999, 2001) and according to Dinis (1999) the
plant bearing sediments from the Vale de Agua
locality probably belong to the basal part (Famalicao
Member) of this formation. Based on in situ pollen
and comparisons with other fossil floras from
Portugal a pre-Albian age (Barremian or Aptian)
was suggested for the plant fossil assemblages from
Vale de Agua (Friis et al., 2001). Dinis and
collaborators (Dinis, 2001; Dinis et al., 2002), using
mainly sedimentological and lithofacies correlations,
suggested a late Aptian age for the base of the
Figueira da Foz Formation. Recently, correlation of
a marine sequence in the Algarve Basin (dated on
dinoflagellates and carbon-isotope records) with the
sedimentary sequence in the Lusitanian (Western
Portuguese) Basin has suggested that the base of the
Figueira da Foz Formation could be slightly younger
than previously thought (early Albian) (Heimhofer
et al., 2007), but detailed correlation between the
Figueira da Foz area (Beiro Litoral region) and the
Vale de Agua area (Estremadura region) has not yet
been established.
The fossil plant remains were extracted from the
sediments by sieving in water followed by treatment
with 40% HF, 10% HCl and rinsing in water. The
fossils are typically small, charcoalified or lignitised,
fragments of wood and twigs as well as detached
reproductive organs. Most of the reproductive
organs are fruits and seeds, but the flora also
includes well-preserved flowers that often have their
three-dimensional form intact. Angiosperms are
diverse and associated pollen grains (in situ in
stamens, adhering to gynoecia, or incorporated in
coprolites) are mainly monoaperturate indicating
that most of the diversity is with magnoliid
angiosperms and monocots (Friis et al., 1997,
1999, 2000a, b, 2001). The few triaperturate pollen
types indicate the presence of early eudicots including the fossils described here.
The fossil specimens described in this paper were
isolated from sediment samples Vale de Agua 19,
141, 328, 329 and 364 collected in 1989 (KRP,
EMF, PRC), 1992 (KRP, EMF) and 2000 (KRP).
The fossil material comprises bicarpellate and
tricarpellate gynoecia, as well as staminate flowers
and stamens with in situ striate pollen. For scanning

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178

K. R. Pedersen et al.

electron microscopy (SEM) the specimens were

mounted on SEM stubs, sputter coated with Au,
and studied using a Hitachi S-4300 field emission
scanning electron microscope at 15 KV and a
Philips SEM 515 scanning electron microscope at
15 KV. Pollen grains removed for ultrastructural
examination of the pollen wall were dehydrated in an
ethanol-propylene oxide series, embedded in Epon,
and sectioned with an ultramicrotome at 500
. Sections were stained with uranyl acetate
700 A
and lead citrate and studied using a Jeol-100S
transmission electron microscope. One specimen of
Lusicarpus was studied using synchrotron x-ray
tomographic microscope (SRXTNM) at the Swiss
Light Source at the Paul Scherrer Institute, Villigen,
Switzerland.
The specimens and preparations of the fossil
material are deposited in the collections of the
Swedish Museum of Natural History, Stockholm
(S).
Results
Five different early eudicot reproductive structures
are described here. The material includes: i)
staminate structures with in situ tricolpate, striate
pollen; ii) bicarpellate pistillate structures with
similar tricolpate, striate pollen adhering to the
stigmatic surface; iii) two different tricarpellate
pistillate structures, one without and one with
tricolpate and striate pollen adhering to the stigma;
and iv) one bicarpellate pistillate structure with
tricolpate and reticulate pollen. All of the fossils are
isolated flowers or flower fragments and there is no
information on inflorescence structure.
Systematics
Order Buxales
Family insertae sedis

tricolpate, tectate and striate with dichotomising and

sometimes anastomosing muri that are ornamented
with minute, transversely oriented ridges. Infratectal
layer thin, granular and forming a fine internal
reticulum; foot layer thin.
Type species. Lusistemon striatus sp. nov.
Comments on the genus. The genus is established
based on staminate structures with distinctive in situ
tricolpate and striate pollen. Spanomera Drinnan,
Crane, Pedersen & Friis is another genus established
from the Cretaceous to encompass similar staminate
structures with in situ striate pollen (Drinnan et al.,
1991), but staminate flowers of Spanomera are
organised on a clear opposite and decussate plan
and the in situ pollen grains are distinctively different
(see also Discussion).
Lusistemon striatus sp. nov. (Figures 14).
Derivation of species name. Referring to the striate
pollen.
Specific diagnosis. As for the genus with the following
additions: Tepals narrow. Epidermis of anthers
along the stomium papillate. Pollen grains circular
to slightly elliptical in equatorial view and
subangular in polar view with the colpi positioned
in the centre of the flattened sides. Tectum striate in
non-apertural regions. Muri of intercolpium aligned
more or less parallel to the pollen grain polar axis
forming a slightly undulating pattern, more strongly
aligned over the poles. Granulae of infratectal layer
form an internal reticulum. Colpus membrane
verrucate with finely striate ornamentation on the
verrucae.
Holotype. S122091 from sample Vale de Agua 141,
illustrated Figures 1AE, 2F, 3C,D,F.

Lusistemon gen. nov.

Derivation of generic name. Composed of Lusitania
(old Roman name for Portugal) and stemon (gr.
thread) referring to the staminate nature of these
Portuguese fossil flowers.
Generic diagnosis. Staminate flower with six small
tepals and six stamens of different sizes and
apparently placed opposite the tepals. Anthers
basifixed, attached to filament without distinct
joint; filaments free from each other. Anthers
dithecal and tetrasporangiate; thecae placed
laterally; anther dehiscence by longitudinal slits.
Connective poorly developed between thecae, but
extended apically into a short protrusion. Pollen

Paratypes. S105028 (sample Vale de Agua 19),

S101284 (part on SEM stub; part sectioned for
TEM) and S105042 (sample Vale de Agua 141).
Type locality. Clay pit complex near the village of
Vale de Agua, western Portugal (39379150N,
8519300W).
Age and stratigraphy. Early Cretaceous (late Aptian
or early Albian), Complexos gresosos de Nazare e
de Cos-Juncal basal part (Famalicao Member) of
the Figueira da Foz Formation.
Description and remarks on the species. The staminate
material comprises two flowers (S105028, S122091)

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Cretaceous flowers of early diverging eudicots

Figure 1. Staminate flowers of Lusistemon striatus. SEM-micrographs. AE. Holotype; staminate flower with six stamens. S122091, sample
Vale de Agua 141. A Flower showing unequal length of stamens and subtending organs. B. Same specimen remounted to show stamens
from the other side. C. Close-up of subtending organs. D,E. Apical part of holotype enlarged to show short connective protrusions and
papillate epidermis along stomium. FH. Fragmentary flower with one subtending organ partly preserved. S105028, sample Vale de Agua
19. F. Same specimen as in G remounted to show stamens from inside. G. Flower from outside showing tepals and stamens. H. Close-up of
G, showing extension of connective. Scale bars 100 mm (AH).

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Figure 2. External morphology of in situ Lusistemon striatus pollen. SEM-micrographs. A. Pollen grains from specimen in Figure 1 FH.
S105028, sample Vale de Agua 19. BE. Pollen grain from isolated stamen. S101284, sample Vale de Agua 141. B. Equatorial view
showing full length of colpus and verrucae on colpus membrane. C,D. Polar view showing three colpi and parallel arrangement of muri
across polar region. E. Detail of Figure 2B showing striate ornamentation of verrucae on colpus membrane. F. Detail of pollen from
holotype showing surface sculpture and muri that have distinct transverse ridges and muri that occasionally bifurcate. S122091, sample Vale
de Agua 141. Scale bars 10 mm (AD); 1 mm (E, F).

as well as several isolated stamens and stamen

fragments (S101284, S105042).
The best preserved staminate flower (S122091)
is composed of six stamens and remains of
several short bract-like organs (Figure 1AC).

Most likely these structures are abraded and

correspond to the narrow organs of specimen
S105028 (Figure 1FH) that are interpreted as
tepals. No carpels or remains of carpels could be
observed inside the stamens and the flower is

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Cretaceous flowers of early diverging eudicots

Figure 3. Internal structures of in situ Lusistemon striatus pollen. SEM-micrographs. A,B. Pollen grains from specimen in Figure 1FH.
S105028, sample Vale de Agua 19. A. Pollen with muri partly missing exposing infratectal layer. B. Detail of infratectal layer showing
reticulate clustering of granulae. C,D. Details of exine showing transverse ridges of muri and infratectal granular layer. Holotype, S122091,
sample Vale de Agua 141. E. Detail of pollen wall showing infratectal reticulum. S101284, sample Vale de Agua 141. F. Fragmentary grain
showing granular infratectal layer and foot layer (arrowheads). Holotype. Scale bars 5 mm (A, F); 1 mm (BE).

most likely unisexual. The stamens are of

variable sizes ranging from 0.9 mm to 1.3 mm in
length; two are long, three are of intermediate
size and one is relatively short (Figure 1AE). It is
difficult to ascertain the arrangement of the
stamens, but their different sizes may indicate a
spiral arrangement. The other flower (S105028)

is more fragmentary. It consists of four stamens,

three of which are more or less complete, all
about 1.25 mm long (Figure 1FH). In this
flower only two organs are preserved outside the
stamens, both are broken, one longer and one
shorter, fused at the base (Figure 1G, H). They
are interpreted as tepals and inferred from the

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182

Figure 4. Pollen wall ultrastructure of in situ Lusistemon striatus pollen. TEM-micrographs. All sections from specimen S101284, sample
Valede Agua 141. AF. Sections show lighter staining ektexine (muri, infratectal layer and foot layer) and darker staining endexine. A. Crosssection of grain in equatorial region showing detached foot layer and endexine in the center (arrow). B. Section through several pollen grains
showing infratectal reticulum (arrow) and sharply triangular profile of muri. C. Section through several grains showing endexine in aperture
regions (arrow) and detached foot layer of central grain. D. Cross-section more or less parallel to equatorial plane showing thin foot layer still
attached to granular infratectal layer. E. Section through grain outside aperture regions showing ektexine with distinct triangular profiles of
muri, granular infratectal layer, partly detached foot layer, and endexine. F. Section of grain in apertural region showing expanded, finely
granular endexine and verrucae of colpus membrane; note foot layer outside aperture region. Scale bars 5 mm (AF).

position of these two organs opposite to the stamens

the number of tepals were probably equal to the
number of stamens.

Anthers are basifixed and there is no distinct joint

between anther and filament (Figure 1FH).
Filaments are short, broad and free from each other.

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Cretaceous flowers of early diverging eudicots

Anthers are dithecal and tetrasporangiate, 0.8
1.2 mm long and 0.20.3 mm wide (Figure 1BE).
Thecae are lateral, and each appears to open by a
longitudinal slit along its entire length (Figure 1A,
B, E). The connective is poorly developed between
thecae, but it extends apically into a short protrusion
that is more or less triangular in shape (Figure 1D,
E). The epidermis along the stomium is papillate
(Figure 1D, E).
Pollen grains observed in situ in the anthers are
tricolpate, tectate and striate (Figure 2AF). They
are circular to slightly elliptical in equatorial view
(Figure 2A, B) and inter-subangular in polar view
(Figure 2C, D), about 1415 mm in diameter, and
1516 mm long. Colpi are short, about 78 mm long,
resulting in a relatively extensive polar area
(Figure 2BD). In polar view they are positioned
each in the centre of one of the flat sides of the grain.
The tectum is striate in non-apertural regions with
narrow and densely-spaced elongated sculpturing
elements (muri) separated by deep, narrow furrows
(striae). The muri are arranged more or less parallel
to the polar axis forming a slightly undulating
pattern in the intercolpium. They are more obvious
parallel over the poles (Figure 2C, D). The muri
sometimes dichotomise, sometimes anastomose or
have free endings (Figure 2BF). They are about
0.6 mm wide and about 4 mm high with flattened
sides and narrow elliptical to narrow triangular
profile, often with a sharp crest. Muri are ornamented with minute, transversely oriented ridges
(Figure 2E, F). These transverse ridges are rounded
and spaced in a dense and regular pattern. The
ridges and interspacing furrows are of equal dimension, about 0.060.07 mm (Figure 2F). Over the
colpus membrane the sculpture elements are verrucate (Figure 2B, E). Verrucae have finely striate
ornamentation similar to that of the muri
(Figure 2E). The muri are supported by a thin
granular infratectal layer (Figure 3AE) that forms
an indistinct internal reticulum (Figure 3A, B). The
foot layer is very thin and often separates from the
infratectal layer (Figure 3F).
Ultra-thin sections of the pollen wall show an
outer lighter staining layer (ektexine) and an inner
darker staining layer (endexine) (Figure 4 AF).
The ektexine consists of tectum, about 0.6 mm thick,
characterised by the densely spaced muri, a thin
granular infratectal layer, about 0.2 mm thick. The
infratectal layer consists of irregular granulae that
cluster laterally to form a reticulate pattern. This
reticulate arrangement of the granules is particularly
clear in SEM-micrographs of broken specimens
(Figure 3A, B), but is also shown in TEM-micrographs (Figure 4A, B). The foot layer is very thin,
up to about 0.2 mm thick (Figure 4A, EF). The

183

endexine is granular, about 0.15 mm thick in nonapertural regions, but thicker under the apertures
(Figure 4DF).
Lusicarpus gen. nov
Derivation of generic name. Composed of Lusitania
(old Roman name for Portugal) and karpos (gr. fruit)
referring to the pistillate nature of these Portuguese
fossil flowers.
Generic diagnosis. Gynoecium bicarpellate, syncarpous, hypogynous and shortly stalked, supported by a
narrow elongated bract. Gynoecium flattened dorsiventrally with a rounded base. Carpels united for
most of their length. Styles two, short and stout, bent
outwards in anthetic flowers. Stigma double-crested,
not distinctly papillate and covered by secretion.
Pollen grains adhering to stigma tricolpate and striate.
Type species. Lusicarpus planatus sp. nov.
Remarks on the genus. The genus Lusicarpus is established to encompass bicarpellate pistillate structures with tricolpate and striate pollen adhering to
stigmatic surface. Lusicarpus is distinct from bicarpellate pistillate flowers of Spanomera in having
carpels united for most of its length and a correspondingly much shorter stigmatic region (see also
Discussion).
Lusicarpus planatus sp. nov. (Figures 5, 6).
Derivation of species name. Referring to the flat shape
of the gynoecium.
Specific diagnosis. As for the genus with the following
additions: Carpels united up to about 4/5 of their
length. Gynoecium wall glabrous. Stigmatic regions
along ca 2/3 of the length of styles. Tricolpate striate
pollen adhering to stigmatic surface similar to in situ
pollen of Lusistemon striatus.
Holotype. S101305 from sample Vale de Agua 141,
illustrated in Figure 5.
Paratypes. S153149 (sample Vale de Agua 329),
S153156 (sample Vale Agua 328), S153518 (sample
Vale de Aqua 19).
Type locality. Clay pit complex near the village of
Vale de Agua, western Portugal (39379150N,
8519300W).
Age and stratigraphy. Early Cretaceous (late Aptian
or early Albian), Complexos gresosos de Nazare e

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184

Figure 5. Bicarpellate gynoecium of Lusicarpus planatus. SEM-micrographs. Holotype, S101305, sample Vale de Agua 141. A. Lateral view
of gynoecium and scale-like bract. B. Stylar region of gynoecium. C. Stigmatic area on ventral side of style. D. Scale-like bract at base of
gynoecium. E. Carpel surface showing isodiametric epidermal cells and ridges probably from vascular bundles. F. Detail of stigmatic
surface showing tricolpate-striate pollen grains (arrowheads) embedded in secretion. G. Stomata on carpel surface (arrowheads). Scale bars
500 mm (A); 100 mm (BE); 10 mm (F, G).

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Cretaceous flowers of early diverging eudicots

185

Figure 6. Bicarpellate gynoecium of Lusicarpus planatus. SEM-micrographs. S153149, sample Vale de Agua 329. A. Lateral view of
gynoecium. B. Stylar region of gynoecium. C. Detail of style showing ventral stigma and tricolpate-striate pollen grains (arrowheads)
embedded in secretion. Scale bars 500 mm (A); 100 mm (B, C).

de Cos-Juncal basal part (Famalicao Member) of

the Figueira da Foz Formation.
Description and remarks on the species. The material
comprises four pistillate structures, three with styles
and stigmatic areas well preserved (S101305,
S153149, S153156) and one in which most of the
styles and stigmatic areas are broken off (S153518).
Each pistillate structure is a bicarpellate, syncarpous,
hypogynous gynoecium, borne on a short stalk
(Figures 5, 6), and supported by a small, narrow
bract in a lateral position at the base of the stalk
(Figure 5A, D). The gynoecia are about 1.5
1.7 mm long and 1 mm wide, strongly flattened
dorsi-ventrally and with a rounded base.
The carpels are united for about 4/5 of their length
(Figures 5A, 6A). The two styles are short and stout.
In specimen S101305 the styles are bent outwards
and the distal 2/3 of the ventral margin is composed
of a double-crested stigmatic region (Figure 5 AC).
This specimen might be preserved in anthetic or
post-anthetic stage. In the three other specimens
that have their styles preserved styles diverge much

less prominently (Figure 6 AC). These specimens

may be preserved in a younger, pre-anthetic stage
than specimen S101305. The stigma appears to be
covered with the remains of secretion and was
apparently wet. It is not distinctly papillate
(Figure 5B, C, F). The dorsal surfaces of the styles
exhibit numerous stomata (Figure 5 G).
Synchrotron x-ray tomographic microscopy
showed that the ovary is clearly bilocular and the
thin ovary wall is composed of small isodiametric
cells. Unfortunately, all tissues were densely
packed and the x-ray studies did not reveal further
information on ovule number, organisation, or
placentation.
The gynoecium wall is thin and the fruit was
probably either non-fleshy, indehiscent or a capsule.
The outer epidermis of the gynoecium is glabrous
and composed of small isodiametric cells.
Tricolpate striate pollen identical to that in situ in
the staminate flowers of Lusistemon striatus occurs
abundantly on the stigmatic surface in specimen
S101305 and S153518, partly or fully embedded in
the secretion-like substance (Figure 5 F). The only

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grain encountered of another type was a single

tricolpate and foveolate pollen grain.

Other putative buxalean gynoecia in the Vale de Agua

assemblages
In addition to Lusicarpus planatus the Vale de
Agua assemblages also include another bicarpellate
gynoecium and two different types of tricarpellate
gynoecia that also indicate the presence of early
eudicots.

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Silucarpus gen. nov.

Derivation of generic name. Anagram of Lusicarpus
referring to the morphological similarity of the fruits.
Generic diagnosis. Gynoecium bicarpellate, syncarpous and hypogynous, flattened dorsi-ventrally
with a round base. Carpels united for most of
their length. Styles two, short and stout, bent
outwards at anthesis. Stigma double-crested and
papillate.
Type species. Silucarpus camptostylus sp. nov.
Comments on the genus. Silucarpus is based on a
single fragmentary specimen. The specimen is
closely similar to Lusicarpus, but differs mainly in
having a distinct papillate stigmatic surface. Pollen
grains observed on the stigmatic surface of Silucarpus
are reticulate in contrast to the striate pollen that
occurs on the Lusicarpus stigmas. In extant
angiosperms the nature of the stigmatic surface is
typically constant within a genus and the Lusicarpus
and Silucarpus are therefore here assigned to separate
genera.
Silucarpus camptostylus sp. nov. (Figure 7).
Derivation of species name. From kamptos (gr.
curved) and stylos (gr. pillar) referring to the
curved styles of the fruit.
Specific diagnosis. As for the genus with the following
additions: Carpels united up to about 5/6 of their
length. Stigmatic regions along about 2/3 of the
length of styles. Gynoecium wall glabrous.
Holotype. S154521 (from sample Vale de Agua 364,
illustrated Figure 7).

Age and stratigraphy. Early Cretaceous (late Aptian

or early Albian), Complexos gresosos de Nazare e
de Cos-Juncal basal part (Famalicao Member) of
the Figueira da Foz Formation.
Description and remarks on the species. The single
specimen is slightly damaged and its epidermis is not
well preserved. The gynoecium is flattened and
composed of two carpels that are united to about 5/6
of their length (Figure 7A). It is about 1.1 mm
broad at the level of the ovary and about 1.3 mm
long.
Only one of the two styles is preserved. The
style is bent outwards and has a double-crested
stigma on the ventral side (Figure 7A, B) composed
of long papillae (Figure 7C). The stigma appears
secretory.
The gynoecium wall is thin and the fruit was
probably non-fleshy, indehiscent or a capsule. The
outer epidermis of the gynoecium is glabrous and
composed of small isodiametric cells.
A few pollen grains are present along the rim of
the stigma embedded in stigmatic secretion
(Figure 7 CE). Pollen appears to be tricolpate,
about 18 mm in polar diameter, tectatereticulate with smooth muri and narrow lumina
(Figure 7D, E).
Valecarpus gen. nov.
Derivation of generic name. From Vale de Agua, and
karpos (gr. fruit).
Generic diagnosis. Gynoecium tricarpellate, syncarpous and hypogynous, borne on a short stalk.
Carpels united for most of their length. Ovary
distinctly triangular in cross-section. Stigma sessile,
double-crested, papillate, and secretory restricted to
the distal parts of the three ventral slits; papillae
short and rounded.
Type species. Valecarpus pedicellatus sp. nov.
Remarks on the genus. Valecarpus comprises small
tricarpellate gynoecia/fruits with distinctly triangular
cross-section and short backward bending style.
Valecarpus is distinct from Aguacarpus described
below in having sessile stigmas and stigmatic area
restricted to the distal potion of the ventral slit. It is
further distinguished in having short stigmatic
papillae.
Valecarpus pedicellatus sp. nov. (Figure 8).

Type locality. Clay pit complex near the village of

Vale de Agua, western Portugal (39379150N,
8519300W).

Derivation of species name. Referring to the stalked

gynoecium.

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187

Figure 7. Bicarpellate gynoecium of Silucarpus camptostylus. SEM-micrographs. Holotype, S154521, sample Vale de Agua 364. A. Lateral
view of gynoecium. B. Detail of style showing ventral stigma. C. Stigmatic region enlarged showing pollen grains (arrowheads) embedded in
secretion. D. Reticulate pollen grains embedded in secretion. E. Pollen grain from stigmatic region enlarged. Scale bars 500 mm (A);
100 mm (B); 10 mm (C, D); 5 mm (E).

Specific diagnosis. As for the genus with the following

additions: Stigmatic regions along the upper third of
the apical suture. Gynoecium wall glabrous.
Holotype. S122094 (from sample Vale de Agua 19,
illustrated Figure 8).
Paratype. S122093 (sample Vale de Agua 19).
Type locality. Clay pit complex near the village of
Vale de Agua, western Portugal (39379150N,
8519300W).

Age and stratigraphy. Early Cretaceous (late Aptian

or early Albian), Complexos gresosos de Nazare e
de Cos-Juncal basal part (Famalicao Member) of
the Figueira da Foz Formation.
Description and remarks on the species. Both
specimens are gynoecia composed of three carpels
that are united along almost their entire length
(Figure 8A). They are about 2.5 mm long and
about 1.8 mm broad at the level of the ovary. The
gynoecium has a short stalk (Figure 8A). The region
of the ovary is distinctly triangular in cross-section.

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K. R. Pedersen et al.

Figure 8. Tricarpellate gynoecium of Valecarpus pedicellatus. SEM-micrograph. Holotype, S122094, sample Vale de Agua 19. A. Lateral
view of gynoecium showing short stalk. B. Apical view of gynoecium showing the triangular shape. C. Double crested stigma along upper
part of ventral slit. Scale bars 500 mm (A, B); 100 mm (C).

The stigmas are short and bent backwards. The

stigmatic region is formed by two broad crests in the
upper part of the ventral slit (Figure 8B, C). The
stigmatic surfaces are papillate with papillae that are
short, rounded, and probably secretory (Figure 8C).
There are no remains of associated stamens and no
pollen grains were observed on the gynoecium.
The gynoecium wall is thin and the fruit was
probably non-fleshy, indehiscent or a capsule. The
surface of the gynoecium is glabrous and epidermis
cells small, isodiametric.

Remarks on the genus. The genus Aguacarpus is

established for small tricarpellate gynoecia with
distinctly triangular cross-section and short stout
styles. It is distinguished from Valecarpus in having
more differentiated stylar area with stigmas that is
extended for the full length of the ventral slit.
Further the stigmatic papillae are longer than in
Valecarpus.
Aguacarpus hirsutus sp. nov. (Figures 9, 10).

Aguacarpus gen. nov.

Derivation of species name. Referring to the hirsute

surface of the gynoecium.

Derivation of generic name. From Vale de Agua, the

locality where the fossils were found, and karpos (gr.
fruit).

Specific diagnosis. As for the genus with the following

additions: Gynoecium with long trichomes and
conspicuous stomata.

Generic
diagnosis. Gynoecium
tricarpellate,
syncarpous, and hypogynous, borne on a short
stalk. Carpels united for almost their entire length.
Ovary triangular in cross-section. Styles three, short,
and stout. Stigma double-crested, papillate, and
secretory, extending for the full length of the ventral
suture; stigmatic papillae long, multicellular,
covered with remains of secretion.

Holotype. S153517 from sample Vale de Agua 141,

illustrated Figure 9.

Type locality:. Clay pit complex near the village of

Vale de Agua, western Portugal (39379150N,
8519300W).

Type species. Aguacarpus hirsutus sp. nov.

Age and stratigraphy. Early Cretaceous (late Aptian

or early Albian), Complexos gresosos de Nazare e

Paratype. S101426 (sample Vale de Agua 141).

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189

Figure 9. Tricarpellate gynoecium of Aguacarpus hirsutus. SEM-micrographs. Holotype, S153517, sample Vale de Agua 141. A. Lateral
view of gynoecium. B. Stylar regions enlarged showing ventral stigmas. C. Detail of stigmatic surface showing distinct papillae. D. Close-up
of carpel epidermis showing densely-space trichomes and stomata. Scale bars 500 mm (A); 100 mm (B, D); 50 mm (C).

de Cos-Juncal basal part (Famalicao Member) of

the Figueira da Foz Formation.
Description and remarks on the species. The
gynoecium is tricarpellate, borne on a short stalk
(Figure 10B), and with the carpels united along
almost their entire length (Figures 9A, B and 10A).
The gynoecium is about 1.4 mm long and 0.9 mm
broad at the level of the ovary.
The styles are short and the stigmatic regions run
along the entire ventral side (Figures 9B, 10A). The
stigmatic surfaces are distinctly papillate with long,
multicellular papillae (Figure 9B, C). They are
covered with remains of secretion and were probably
wet.
The gynoecium wall is thin and the fruit was
probably non-fleshy, indehiscent or a capsule. The
epidermis cells of the gynoecium are small
and isodiametric. Numerous long trichomes or
trichome bases, as well as stomata are scattered
over the entire gynoecial surface (Figure 9D).

Pollen grains occur abundantly on the stigmatic

surface of specimen S101426. Grains are tricolpate,
tectate and striate with transverse ridges on the muri,
about 15 mm long (Figure 10C, D).

Discussion
Comparison with dispersed striate pollen from the
Cretaceous
A variety of tricolpate, striate pollen grains have been
reported from Cretaceous and Tertiary palynological
assemblages. Angiosperm pollen grains of this type
have their first occurrences in the early Aptian of
Egypt and Gabon (Penny, 1988; Doyle, 1992,
1999). Among dispersed pollen, the grains in situ
within Lusistemon show the closest similarity to those
described from the Early Cretaceous of Egypt
(Mersa Matruh borehole 1) by Penny (1988) who
documented four different kinds of striate tricolpate
pollen using SEM. All four taxa occur only in the

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K. R. Pedersen et al.

Figure 10. Tricarpellate gynoecium of Aguacarpus hirsutus. SEM-micrographs. S101426, sample Vale de Agua 141. A. Apical part of
gynoecium showing stylar region with stigmas. B. Basal part of fruit showing short stalk. C. Stigmatic surface with pollen grains
(arrowheads) embedded in secretion showing two of three colpi. D. Detail of pollen showing striate sculpture and transverse ridges of muri.
Scale bars 100 mm (A, B); 50 mm (C); 1 mm (D).

Aptian part of the sequence, and extend from the

latest Early Aptian to the end of the Middle Aptian.
Three of the Egyptian striate pollen types have muri
that are smooth or almost smooth and that either
lack supratectal ornamentation or that have only
faint ornamentation. The fourth type, referred to by
Penny (1988) as STRIOTRI-SEGMUR, is closely
similar to the pollen of Lusistemon. Muri in the
intercolpium regions are narrow, densely-spaced,
arranged parallel to the polar axis, and have a
supratectal ornamentation of fine transverse ridges.
The sculpturing elements over the aperture membrane are verrucate. There is also agreement in
pollen size, STRIOTRI-SEGMUR being about
14.519.5 mm long compared to 1415 mm for the
pollen of Lusistemon. Penny (1988) also
mentions that STRIOTRI-SEGMUR has a secondary layer in the sexine, which sometimes forms a
pseudoreticulum. This is not illustrated but it
probably corresponds to the unusual reticulate
meshwork of the infratectal granular layer that

occurs in the Lusistemon pollen. There are only

minor differences between the two kinds of grains:
muri in the Lusistemon pollen have a sharper profile
than in STRIOTRI-SEGMUR and STRIOTRISEGMUR has granulae and shorter muri interspaced between the elongated muri, which does not
occur in the Lusistemon pollen. The verrucae of the
colpus membrane also lack supratectal ornamentation in STRIOTRI-SEGMUR.
The dispersed pollen grains from Egypt described by
Penny (1988) were not given classic binominals, but
similar dispersed striate grains from other Cretaceous
palynological assemblages are typically referred to
various species of the dispersed pollen genus
Striatopollis. Striopollenites Rouse and Rutihesperipites,
are sometimes regarded as junior synonyms of
Striatopollis (for a more comprehensive list of other
tricolpate and striate dispersed pollen genera see
Srivastava, 1977). However, the type species for
Striatopollis and Striopollenites, as well as many
other dispersed pollen grains from the Cretaceous

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Cretaceous flowers of early diverging eudicots

and Tertiary, have only been studied and illustrated
by light microscopy (LM). Details of supratectal
ornamentations or wall stratification are usually
lacking, which precludes detailed comparison with
the in situ pollen considered here and other pollen
grains studied using scanning electron microscopy
(SEM).
Closer examination of the many different kinds of
dispersed tricolpate, striate pollen grains shows
considerable variation in exine ornamentation.
Grains of this kind were evidently produced by
several systematically distinct groups of eudicots.
The type species of Striatopollis, Striatopollis sarstedtensis Krutzsch, was described from the earliest
Paleocene of Wehmingen, Germany (Krutzsch,
1959). It is characterised by non-anastomosing and
generally non-diverging muri that run parallel to the
polar axis in a slightly twisted arrangement. It is thus
distinct from the fossil pollen of the Lusistemon
flower, which has anastomosing and divergent muri
and is also distinct from many other dispersed
Cretaceous pollen assigned to Striatopollis. The
circumscription of Striopollenites Rouse (type species
Striopollenites terasmaei Rouse from the Eocene of
British Columbia, Canada; Rouse, 1962) is closely
similar to that of Striatopollis and the name is
therefore regarded as a junior synonym of
Striatopollis (Potonie, 1966; Ward, 1986).
The genus Rutihesperipites is well documented by
both SEM and LM. The type species,
Rutihesperipites trochuensis (S. K. Srivastava) S. K.
Srivastava, from the Maastrichian of Alberta was
first described as Salixipollenites trochuensis S.K.
Srivastava (Srivastava, 1966). It shares many features with the pollen of Lusistemon described here.
Grains are about 1730 mm in equatorial diameter
and about 2124 mm in polar length with a densely
striate exine. Muri are mostly parallel to the polar
axis, but anastomose regularly, and are ornamented
by fine, closely spaced transverse supratectal ridges.
However, Rutihesperipites trochuensis differs from the
pollen found in Lusistemon in having a much denser
pattern of striations and muri with rounded profiles.
Ward (1986) transferred Rutihesperipites trochuensis
to Striatopollis, but the striation pattern of
Rutihesperipites trochuensis is distinctly different from
that of the type species of Striatopollis. In addition,
the pollen wall of Rutihesperipites trochensis is much
thinner. Because of these differences, and because
Rutihesperipites is well documented by SEM, we
suggest that Rutihesperipites is maintained for dispersed tricolpate and striate pollen grains with
anastomosing muri bearing transverse supratectal
ornamentation.
Dispersed pollen reported from the Albian of
Portugal as Striatopollis trochuensis and Striatopollis cf.

191

trochuensis (Heimhofer et al., 2007) have a different

striation pattern than the type material of
Rutihesperipites trochuensis and clearly do not belong
to this species. These dispersed Portuguese grains
are illustrated by LM-images only and a detailed
comparison with the in situ pollen from Lusistemon is
therefore not possible. However, the dispersed
grains are larger (2025 mm) and are probably not
conspecific with the in situ grains.
Grains described as Striatopollis cf. paraneus
(Norris) Singh from the Cenomanian of Bathurt
and Mornington Islands, eastern Australia
(Dettmann, 1973) were documented by SEM.
They resemble Rutihesperipites and the pollen of
Lusistemon in size, general morphology and sculpturing, but differ in the much more distinct and sharper
supratectal ridges and the rounded profile of the
muri.
Comparison with other fossil reproductive structures from
the Cretaceous
A variety of eudicot reproductive structures have
been described from the Cretaceous. Most of those
from the Late Cretaceous belong to core eudicots
(for a review see Friis et al., 2006a) and none of
them resemble Lusistemon or Lusicarpus. From the
Early Cretaceous the fossil record of eudicot floral
structures is much less extensive. Most of these Early
Cretaceous taxa are related to the Platanaceae
(Crane et al., 1993; Pedersen et al., 1994) and
while the flowers are also unisexual they differ from
Lusistemon-Lusicarpus in their pentamerous organisation, apocarpous gynoecia, and the foveolate to
reticulate sculpture of the pollen wall. However,
flowers of Spanomera mauldinensis Drinnan, Crane,
Friis & Pedersen and Spanomera marylandensis
Drinnan, Crane, Friis & Pedersen from the
Potomac Group sediments of eastern North
America (Drinnan et al., 1991) are much more
similar to the fossil flowers described here.
Spanomera includes staminate and pistillate floral
structures that are sometimes preserved in fragments
of inflorescences. In situ pollen of Spanomera is
tricolpate with a coarse tectum sculpture formed
from high vermiform muri with sharply triangular
profiles. Grains of Spanomera and Lusistemon are
similar in several respects but those of Spanomera are
distinguished by having a distinctive columellate
infratectal layer and a very thick foot layer. Grains of
Spanomera mauldinensis are striate and the muri have
fine transverse striations as in the pollen of
Lusistemon. They were compared to dispersed grains
assigned to Striatopollis paraneus. Grains of
Spanomera marylandensis are striate-rugulate to
reticulate-rugulate with smooth muri. They were

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K. R. Pedersen et al.

compared to dispersed pollen assigned to Striatopollis

vermimuris.
The reproductive structures of Spanomera mauldinensis are the most completely preserved and include
inflorescences with both staminate and pistillate
flowers. The staminate flowers are composed of
one whorl of five bract-like tepals, one whorl of five
stamens opposite the tepals and a central pistillode
(Drinnan et al., 1991). Both the whorl of tepals and
the whorl of stamens have an opposite and decussate
arrangement. The staminate flowers of Lusistemon
differ in having a much less prominent perianth and
in lacking a pistillode. They also seem to have a
spiral arrangement of the stamens in contrast to the
whorled arrangement in Spanomera. The basifixed
anthers of Lusistemon also contrast with the dorsifixed anthers in Spanomera, but in both the thecae
are long, laterally placed and open by longitudinal
slits along their entire length. In both taxa the
anthers also have short and pointed apical connective protrusions.
The pistillate flowers of Spanomera are bicarpellate
with two bract-like tepals, one opposite each carpel,
and two additional bract-like tepals in lateral
position (Drinnan et al., 1991). Lusicarpus is
also bicarpellate but in Spanomera the carpels are
fused only near the base, the stigmatic area extents
along the full length of the ventral suture, and the
stigmatic papillae are long and prominent. In
Lusicarpus there are no remains or scars of stamens
and tepals outside the carpels. The scale-like bract
has a lateral position similar to the inner perianth
whorl of Spanomera.
Although the Portuguese fossils differ from
Spanomera in details of flowers and pollen grains,
and cannot be included in the same genus, the
combination of characters is nevertheless similar and
suggests that Lusistemon-Lusicarpus and Spanomera
may belong to the same evolutionary lineage of early
eudicots (see also systematic discussion below). The
other pistillate structures described from Portugal
(Silucarpus, Valecarpus, Aguacarpus) are not similar
to other pistillate structures described from the
Cretaceous, but may also be part of the same
systematic complex as Spanomera and LusistemonLusicarpus (see Discussion below).

Comparison with extant angiosperms: Systematic

position of Lusistemon and Lusicarpus
The occurrence of distinctive striate pollen in situ in
the stamens, and adhering to the stigmatic region,
indicates that the staminate flowers of Lusistemon
and the pistillate flowers of Lusicarpus were produced by the same kind of plant. In the following
character analysis they are therefore discussed

together. The tricolpate pollen clearly places the

floral structures among eudicot angiosperms and
characters of the fossil further indicate a probable
relationship to lineages that diversified early in the
eudicot radiation.
Floral organization. Unisexual flowers are common
in many early diverging groups of eudicots (e.g.,
Buxaceae, Didymelaceae, Platanaceae, some
Ranunculales, some Sabiaceae) as well as many
early diverging groups of core eudicots (e.g.,
Myrothamnaceae, Gunneraceae) (Drinnan et al.,
1994; von Balthazar & Endress, 2002a, b; von
Balthazar et al., 2003). However, unisexual flowers
also occur widely among other angiosperms
especially in generally wind-pollinated taxa of
Fagales or Saxifragales (e.g., Daphniphyllaceae,
Cercidiphyllaceae, Altingiaceae of Saxifragales;
Endress, 1993b).
Staminate structure. In the extant taxa considered
above, staminate flowers have a simple perianth as
inferred for Lusistemon, or a perianth is lacking as in
Eupteleaceae, Achlys DC. (Berberidaceae), Trochodendron Sieb & Zucc. (Trochodendraceae), Styloceras Juss. (Buxaceae) and perhaps Didymelaceae of
early diverging eudicots, as well as in Altingiaceae,
Cercidiphyllaceae, Daphniphyllaceae p.p. of Saxifragales (Endress, 1986, 1989, 1993a, b; Sutton,
1989; von Balthazar & Endress, 2002a).
Six stamens are the rule in various families of early
diverging eudicots (Papaveraceae, Eupteleaceae,
Lardizabalaceae, Menispermaceae, Berberidaceae,
Notobuxus Oliv. in Buxaceae) and may be present
in Saxifragales (Hamamelidaceae p.p., Daphniphyllaceae) (for an overview see von Balthazar et al.,
2005). However, the arrangement of stamens is
mostly whorled in these taxa and the flowers often
organised in a clear dimerous plan. The stamens of
the fossil are of different sizes and this may indicate
an initiation in succession, but whether in a spiral or
a whorl is unclear.
Filaments are short in the fossil flower, but
extension of the filaments at anthesis cannot be
excluded. Short filaments in anthetic extant flowers
are known from various taxa in early diverging
eudicots (Lardizabalaceae, Berberidaceae, Buxaceae, Didymelaceae, Proteales) as well as Saxifragales (Daphniphyllaceae, Altingiaceae). Anthers
of the fossil are basifixed, which is also common
among these extant groups. Anther dehiscence in the
fossil is lateral, most probably by longitudinal slits
along the entire length of the thecae. Anther
dehiscence by longitudinal slits is found among
many angiosperms including early diverging

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eudicots and early diverging core eudicots, for

example in some wind-pollinated taxa of the
Saxifragales such as Daphniphyllaceae (Endress,
1993b). Connective protrusions as in the fossil are
common among extant taxa at this level of angiosperm evolution (Hufford & Endress, 1989; Endress
& Stumpf, 1991; von Balthazar & Endress, 2002b).
A particular feature of the fossil is its papillate
epidermal cells along the stomium; similar epidermal
cells have been observed in Styloceras (Buxaceae; von
Balthazar & Endress, 2002b).
Pollen. Many early diverging eudicots have
tricolpate pollen, in contrast to the mostly
tricolporate pollen of core eudicots (e.g., Drinnan
et al., 1994; Magallon et al., 1999). However,
tricolpate pollen occurs also scattered among core
eudicots, for example among certain Saxifragales
such as Daphniphyllaceae and Hamamelidaceae
(Zavada & Dilcher, 1986).
Pollen with striate surface ornamentation is
present in a wide range of angiosperm families, both
among early diverging eudicots and various orders of
core eudicots (e.g., Santalales, Saxifragales,
Geraniales, Myrtales, Fabales, Rosales, Sapindales,
Ericales,
Gentianales,
Lamiales,
Solanales,
Asterales, sensu APG II, Walker & Doyle, 1975;
Ward, 1986). However, pollen comparable to the
fossil grains at a more detailed level is rare and
occurs in Berberidaceae (Achlys, Vancouveria C.
Morr. & Decne., Jeffersonia Bart., Nowicke &
Skvarla, 1981; Nowicke & Skvarla, 1982),
Ranunculaceae (Hydrastis Ellis ex L., Trollius L.,
Kumazawa, 1936; Nowicke & Skvarla, 1981; Lee &
Blackmore, 1992), Trochodendraceae (Endress,
1986), Circaeasteraceae (Circaeaster Maxim.,
Kingdonia Balf. f. & W.W. Smith, Nowicke &
Skvarla, 1982), Sapindaceae (Acer L., Halbritter &
Hesse, 2000 onwards), and Fabaceae (Crudia
Schreb., Anthonotha Beauv., Isoberlinia Craib &
Stapf., Germeraad et al., 1968). Among these the
fossil grains are particularly similar to those of
Circaeaster, which are about the same size and that
have an irregularly striate tectum. In Circaeaster as in
the fossil the foot layer and endexine is much thinner
than tectum and infratectal layer, but muri are
apparently smooth without supratectal ornamentation (Nowicke & Skvarla, 1982). Unfortunately
there is no detail on the infratectal layer. The other
member of the Ranunculales mentioned above as
well as Acer also have an extremely thin foot layer
(Nowicke & Skvarla, 1982; Halbritter & Hesse, 2000
onwards), a character that is otherwise very rare
among eudicot angiosperms. However, all of these
taxa lack the distinct transverse ribbing of the muri.
Pollen grains of Buxaceae differ from those of

193

Lusistemon-Lusicarpus in being tricolporate to polyporate with reticulate to rugulate or crotonoid exine

sculpture (Drinnan et al., 1991; Kohler, 2007).
Pistillate structure. The presence of a bicarpellate
superior ovary, as is clearly present in the fossil, is
characteristic for several families among early
diverging eudicots core eudicots (basal Papaveraceae,
and Gunneraceae) as well as Saxifragales
(Hamamelidaceae). Similar pistillate structures also
occur in some Menispermaceae, Circaeasteraceae,
Ranunculaceae, Buxaceae, Sabiaceae, Myrothamnaceae and Daphniphyllaceae.
Syncarpous pistillate structures, as observed in
Lusicarpus, occur in Papaveraceae, Buxaceae,
Sabiaceae, Trochodendraceae, Daphniphyllaceae,
some Hamamelidaceae, and Altingiaceae. The
stigma is double-crested and decurrent to a greater
or lesser extent in several extant taxa (Buxaceae, Didymelaceae, Platanaceae, Myrothamnaceae, Trochodendraceae, Saxifragales: Altingiaceae, Cercidiphyllaceae, Daphniphyllaceae, some wind-pollinated
Hamamelidaceae; Endress & Igersheim, 1999). In
Lusicarpus the stigmatic area is double-crested and
decurrent only in the upper half of the free styles.
The stigma of the fossil is not clearly papillate
compared to the generally distinctly unicellularpapillate, often pear-shaped papillate stigmas of early
diverging eudicots and early diverging core eudicots
(Endress & Igersheim, 1999). Also, in some of the
extant eudicots mentioned above rather than being
papillate the stigmatic surface has multicellular
protuberances [e.g. Podophyllum L. (Berberidaceae),
Hydrastis (Ranunculaceae), Daphniphyllaceae, and
Hamamelidaceae; Endress & Igersheim, 1999)]. The
fossil stigma appears to be secretory as is also the case
in most of the extant taxa considered here.
The only other organ that occurs in Lusicarpus in
addition to the gynoecium is a small bract-like organ.
Since no abscission scars have been observed between
the bract-like organ and the ovary base it is likely that
no staminate organs were present. Whether additional
perianth organs were present outside the bract-like
organ cannot be determined with the material available. The lateral position of the bract-like organ in
respect to the gynoecium axis might indicate that it is a
subtending bract. Flowers of eudicots with only bractlike organs outside the gynoecium are found in extant
Circaeasteraceae, Buxaceae, Didymelaceae, Trochodendraceae and Myrothamnaceae p.p. among early
diverging eudicots and core eudicots, as well as
in some Saxifragales, such as Daphniphyllaceae
(Drinnan et al., 1991, 1994; Hoot et al., 1999; von
Balthazar & Endress, 2002a). A perianth is also
lacking in the bisexual or pistillate flowers of
Eupteleaceae, Trochodendraceae, Myrothamnaceae,

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Altingiaceae, Cercidiphyllaceae, and Daphniphyllaceae

(Drinnan et al., 1991, 1994; Hoot et al., 1999; von
Balthazar & Endress, 2002a).
Non-fleshy fruits, either indehiscent or capsular as
inferred for Lusicarpus occur in several of the families
considered above including the Buxaceae. Fruits of
Daphniphyllaceae are fleshy drupes with a thick
endocarp. They are further distinguished in being
unilocular in contrast to the bilocular fruits of Lusicarpus.
Systematic conclusion. Lusistemon and Lusicarpus
display a mosaic of characters that are found in
various extant eudicot families, predominantly
among early diverging eudicots and core eudicots,
as well as in some Saxifragales. Floral characters are
particularly similar to those of Buxaceae, but are also
similar to those of the distantly related
Daphniphyllaceae. Flowers of Buxaceae, like those
of several other early diverging eudicots, are
characterized by a low level of synorganisation
between floral organs. In contrast, in the context of
other Saxifragales, the flowers of Daphniphyllaceae
are adapted to a specific pollination syndrome (i.e.
wind-pollination).
Pollen in the fossil material is distinct and shows a
greater similarity to pollen of other members of early
diverging eudicots. The combined evidence from
reproductive structures and pollen indicates that the
fossil is probably best placed among the early
diverging lineages of eudicots and probably close to
extant Buxaceae.
Inferences of habit and pollination biology. A
characteristic that is particularly noticeable among
the flowers of early diverging eudicots with striate
pollen [e.g., Achlys, Vancouveria, Jeffersonia
(Berberidaceae), Hydrastis (Ranunculaceae), and
Kingdonia and Circaeaster (Circaeasteraceae)] is the
preponderance of white or greenish flowers. Such
flowers are mostly open and have non-specific
pollinators. In addition, many of these are herbaceous
plants of the forest understorey that flower early in the
season in temperate regions. Such flowers are often
pollinated by a variety of smaller insects, in particular
by flies and solitary bees (Motten, 1986).
Systematic position of Silucarpus, Valecarpus and
Aguacarpus
The additional three pistillate reproductive structures from Vale de Agua also show similarities to
Buxaceae. The tricarpellate gynoecium of Valecarpus
with its decurrent, double-crested stigmatic areas
along the upper part of the styles or ventral suture is
particularly similar to extant Buxus L. and Notobuxus
species (Buxaceae, von Balthazar & Endress,

2002b). The interstylar areas of the fossil gynoecium

appear undifferentiated. However, in many extant
Buxus species interstylar nectariferous bulges are
present, although they are less differentiated or
lacking in many African Buxus species and
Notobuxus (von Balthazar & Endress, 2002b). The
fossil stigma also appears to consist of unicellularpapillae, as also occurs in Buxaceae and many other
early diverging eudicots.
The tricarpellate gynoecium of Aguacarpus is
comparable to Lusicarpus in the degree of union of
the carpels, the decurrent stigmas, and the presence
of very similar tricolpate, striate pollen adhering to
the stigmatic surface. It also shows similarity to some
Buxaceae, particularly Notobuxus. It is unfortunate
that more detailed comparisons are not possible
because internal features are unknown.
The bicarpellate gynoecium of Silucarpus with its
reticulate pollen offers a limited number of characters for comparison with extant taxa. Two carpels
comprising a superior ovary and with decurrent,
double-crested stigmatic areas occur in a similar
variety of extant taxa to the pistillate structures
mentioned above (basal Papaveraceae, Sabiaceae,
Gunneraceae, and some Menispermaceae, Circaeasteraceae, Ranunculaceae, Buxaceae, Myrothamnaceae of early diverging eudicots and early diverging core eudicots as well as Hamamelidaceae and
Daphniphyllaceae of Saxifragales, Endress &
Igersheim, 1999). However, the stigma appears
papillate and is more similar to that of early
diverging eudicots and early diverging core eudicots.
Reticulate pollen is present in various families of
these groups, but the reticulum of the fossil pollen is
similar to that of some Buxaceae (Buxus, although
these pollen are usually zono-colporate, pantocolporate or pantoporate, Kohler & Bruckner, 1982;
Kohler, 2007), Sabiaceae (Erdtman, 1952), Platanaceae (Denk & Tekleva, 2006), Menispermaceae
(e.g., Ferguson, 1975; Thanikaimoni, 1984), as well
as Hamamelidaceae (e.g., Erdtman, 1952; Zavada &
Dilcher, 1986) and Cercidiphyllaceae in Saxifragales
(Zavada & Dilcher, 1986).
Conclusions
The fossil reproductive organs from Vale de Agua
add to the expanding record of Early Cretaceous
eudicot angiosperms. Comparisons with extant
plants indicate that the flowers of Lusistemon and
Lusicarpus are related to early diverging groups of
eudicots and are particularly close to extant Buxales.
There is therefore good correspondence between the
early stratigraphic position of these fossils and their
likely position as an early diverging group in eudicot
phylogeny.

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Cretaceous flowers of early diverging eudicots

The in situ pollen grains are very similar to
dispersed grains reported from the early and midAptian of Egypt. Although the fossil grains from
Egypt are probably not conspecific with the pollen
found in Lusistemon, unusual details of the pollen
wall (supratectal striation and infratectal reticulum)
strongly suggest that the two taxa belong to the same
evolutionary lineage and probably the same genus.
This implies that the buxalean lineage, which was
certainly present (based on Spanomera) by the late
Aptian, may already have been established by the
early Aptian. The presence of three other, probably
closely related, taxa in the Vale de Agua flora further
indicate a considerable diversity of early diverging
eudicots supporting the palynological data of diverse
and widespread occurrences of Eudicots in the
Aptian-Albian.
Acknowledgments
We thank B. Kunderup for help in preparing TEM
sections and G. Dancher for permission to use the
TEM facilities at the Institute of Anatomy,
University of Aarhus. We also thank Pat
Herendeen for helpful comments on the text. We
thank Marco Stampanoni for help with SRXTM
performed at the Swiss Light Source, Paul Scherrer
Institut, Villigen, Switzerland. Financial support
from the Swedish Research Council (EMF), the
Carlsberg Foundation (KRP) is gratefully acknowledged. SRXTM was funded by the Swiss Light
Source, European Union FP6 (to P. C. J. Donoghue
and S. Bengtson).
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