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Research
Cite this article: Friis EM, Pedersen KR, Crane
PR. 2016 The emergence of core eudicots:
new floral evidence from the earliest
Late Cretaceous. Proc. R. Soc. B 283: 20161325.
http://dx.doi.org/10.1098/rspb.2016.1325
Received: 11 June 2016
Accepted: 14 November 2016
Subject Areas:
evolution, palaeontology, structural biology
Keywords:
fossil flower, rosids, asterid, SRXTM,
synchrotron X-ray microtomography,
tricolporate pollen
Author for correspondence:
Else Marie Friis
e-mail: [email protected]
Electronic supplementary material is available
online at https://dx.doi.org/10.6084/m9.figshare.c.3588719.
The emergence of core eudicots:
new floral evidence from the earliest
Late Cretaceous
Else Marie Friis1, Kaj Raunsgaard Pedersen2 and Peter R. Crane3,4
1
Department of Palaeobiology, Swedish Museum of Natural History, Stockholm, Sweden
Department of Geoscience, University of Aarhus, Aarhus, Denmark
3
Yale School of Forestry and Environmental Studies, New Haven, CT, USA
4
Oak Spring Garden Foundation, Upperville, VA, USA
2
EMF, 0000-0003-2936-2761
Eudicots, the most diverse of the three major clades of living angiosperms, are
first recognized in the latest Barremian–earliest Aptian. All Early Cretaceous
forms appear to be related to species-poor lineages that diverged before the
rise of core eudicots, which today comprise more than 70% of angiosperm
species. Here, we report the discovery of a well-preserved flower, Caliciflora
mauldinensis, from the earliest Late Cretaceous, with unequivocal core eudicot
features, including five sepals, five petals and two whorls of stamens borne on
the rim of a floral cup containing three free carpels. Pollen is tricolporate.
Carpels mature into follicular fruitlets. This character combination suggests
a phylogenetic position among rosids, but more specific assignment is
precluded by complex patterns of character evolution among the very large
number of potentially relevant extant taxa. The whorled floral organization
is consistent with ideas that this stable pattern evolved early and was a prerequisite for more integrated patterns of floral architecture that evolved
later. However, limited floral synorganization in Caliciflora and all earlier
eudicot flowers recognized so far, calls into question hypotheses that substantial diversification of core eudicots had already occurred by the end of the
Early Cretaceous.
1. Introduction
Hypotheses of relationships among living angiosperms recognize a species-poor
basal grade, within which are embedded three major clades; eumagnoliids, monocots and eudicots. Soon after their first appearance in the fossil record about
135 Ma, Early Cretaceous angiosperms include diverse extinct taxa related to
basal grade angiosperms (Austrobaileyales, Chloranthaceae and Nymphaeales),
certain eumagnoliids (Laurales, Magnoliales and Piperales), early monocots
(Alismatales) and basal grade eudicots (e.g. [1–4]). These Early Cretaceous assemblages contrast markedly with Late Cretaceous angiosperm assemblages that are
dominated by fossils related to lineages of core eudicots. Core eudicots comprise
more than 70% of living angiosperm species and both major clades within the
group are well represented in the Late Cretaceous. Late Cretaceous rosids include
a rich record of early Fagales (e.g. [5]) as well as diverse fossils related to other
clades [1]. Late Cretaceous asterids include many taxa related to extant Cornales
and Ericales (e.g. [1,6–9]), the two earliest diverging lineages of the group.
The transition from Early Cretaceous floras, dominated by basal grade lineages
of angiosperms, eumagnoliids and early eudicots, to Late Cretaceous floras
dominated by core eudicots, occurred sometime between the mid-Albian and
the Turonian–Santonian. Here, we describe a new flower from the earliest Late
Cretaceous (earliest Cenomanian) of eastern North America with distinctive features of core eudicots. Together with an unnamed fossil flower of approximately
& 2016 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution
License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original
author and source are credited.
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Figure 1. SEM images of flower bud of Caliciflora mauldinensis gen. et sp. nov. from the Late Cretaceous (earliest Cenomanian) Mauldin Mountain locality, MD, USA;
holotype (PP53985; sample Mauldin Mountain 116). (a – c) Lateral (a) and apical (b,c) views of stalked flower bud showing subtending bract (br), two prophylls
( pp), revolute-valvate sepals (s) and petals ( p). (d ) Detail of petal surface showing dense indumentum of interlocking stellate hairs. (e) Detail of sepal surface
showing a stellate hair.
similar age [10], this new discovery provides the earliest direct
evidence of floral structure in early core eudicots and has implications for understanding the evolution of floral structure
within this hyperdiverse clade of extant angiosperms.
2. Material and methods
The fossil material described here consists of one complete flower
bud, one anthetic flower and three fragments of post-anthetic
flowers, one of which has the remains of a stamen. All five specimens were recovered from samples of Potomac Group sediments
(Mauldin Mountain samples 022, 116, 117) collected from the
Elk Neck Beds at the Mauldin Mountain locality on the Elk Neck
Peninsula, northeastern Maryland, USA (39829’1500 N, 75859’4400
W). The Elk Neck Beds of earliest Cenomanian age have also
yielded inflorescences and flowers of Mauldinia mirabilis Drinnan,
P. R. Crane, E. M. Friis & K. R. Pedersen [11], which is related to
extant Lauraceae, fruits of Couperites mauldinensis K. R. Pedersen,
P. R. Crane & E. M. Friis [12], which are of uncertain affinity
among early diverging angiosperms, and pistillate and staminate flowers of Spanomera mauldinensis Drinnan, P. R. Crane,
E. M. Friis & K. R. Pedersen [13], which are related to extant Buxales. For further details on the geology and age of the Mauldin
Mountain assemblage, see [11].
The specimens are coalified and were treated following
standard methods for Cretaceous mesofossils [1]. The flower bud
was mounted on a brass stub for synchrotron radiation X-ray
microtomography (SRXTM) at the Tomcat beamline of the Swiss
Light Source, Paul Scherrer Institute, Switzerland [14]. It was
measured using a 20 objective with isotopic pixel size of
0.325 mm at 10 keV using a sCMOS detector and a 20 mm thick
LAG:Ce scintillator screen and the specimen was vertically stacked
(for more details on the technique, see [15]). Data derived from the
SRXTM [16] were reconstructed and imaged using AVIZO (v. 6.3,
7.1, 9.0.1, 9.1.1) software for computed tomography.
After SRXTM the flower bud was remounted on an aluminium stub for SEM scanning electron microscopy (SEM),
sputter coated with gold, and examined using a Hitachi S-4300
Field Emission Scanning Electron Microscope at 2 kV. The four
other specimens were also prepared for SEM in the same way.
3. Results
Angiospermae
Core eudicots
Genus. Caliciflora gen. nov.
Type species designated here. Caliciflora mauldiniensis
sp. nov.
Generic diagnosis. Flower small, sessile, with an associated bract and two prophylls borne on a stout stalk.
Staminate and pistillate organs in the same flower. Floral cup
distinct. Perianth with five sepals and five petals borne on
the rim of the floral cup. Sepals free, thick, with broad base
and acute apex; sepal aestivation revolute-valvate. Petals free,
broadening distally from a narrower base, keeled, with a thin
lamina and median rib; petal aestivation open below, quincuncial above. Indumentum dense on the outer surfaces of the
floral cup, sepals and petals composed of interlocking stellate
hairs. Stamens in two whorls, minute with dithecate, tetrasporangiate and dorsifixed anthers. Pollen minute, tricolporate,
psilate. Orbicules present. Gynoecium trimerous with three
free carpels borne on the inside of the floral cup.
Specific diagnosis. As for the genus.
Etymology. Generic name from calice (Latin for cup) and
flos (Latin for flower) and specific name from the Mauldin
Mountain locality where the fossils were collected.
Holotype designated here. PP53985 (sample Mauldin
Mountain 116); figure 1–4d,h.
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Figure 2. SRXTM volume renderings of flower bud of Caliciflora mauldinensis gen. et sp. nov. from the Late Cretaceous (earliest Cenomanian) Mauldin Mountain locality,
MD, USA; holotype (PP53985; sample Mauldin Mountain 116). (a) Volume rendering of apical view of entire floral bud showing subtending bract (br), prophylls (pp) and
five revolute-valvate sepals (s). (b–g) Transverse views of flower bud at different levels from apex (b) to middle of floral cup (g) showing subtending bract (br), two
prophylls (pp), five revolute-valvate sepals (s), five petals (p), three antesepalous stamens (arrowheads), five antepetalous stamens (asterisks) and three carpels; note
three closely appressed stigmas (c) and the free ventral margins of carpels below the stigmatic region ( f,g) (a, not cut; b, section at level of orthoslice xy0766; c, section
at level of orthoslice xy1756; d, section at level of orthoslice xy1916; e, section at level of orthoslice xy2044; f, section at level of orthoslice xy2233; g, section at level of
orthoslice xy2427). (h,i) Longitudinal views of flower bud in median section showing floral cup surrounding the carpels and with antesepalous stamens (arrowheads) and
antepetalous stamens (asterisks) on the rim of the floral cup (h, section at level of orthoslice xz1112; i, section at level of orthoslice yz0983).
Paratypes. PP34773 (sample Mauldin Mountain 116),
PP54159 (sample Mauldin Mountain 117), PP54160,
PP54161 (sample Mauldin Mountain 022).
Type locality. West of Mauldin Mountain, Elk Neck
Peninsula, MD, USA, (39829’1500 N, 75859’4400 W).
Type horizon and age. Elk Neck Beds, Potomac Group;
Late Cretaceous (Early Cenomanian; lowermost palynological
Zone III).
Description. The taxon is based on a single flower bud
(PP53985), one anthetic flower (PP34773) and three flower
fragments preserved post-anthesis (PP54159–PP54161). The
specimens are linked mainly by their identical stellate trichomes, similarities in the shape of the sepals, the presence
of a floral cup and identical pollen grains in situ in specimens
PP34773 and PP54161 and on the surface in PP54160. Sepals
and petals are well-developed in the floral bud indicating that
it was close to anthesis when fossilized.
The floral bud (figure 1– 4d,h; electronic supplementary
material, 1), the anthetic flower (figure 4a) and one of the
post-anthetic flower fragments have both carpels and
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Figure 3. SRXTM reconstructions (orthoslices) of flower bud of Caliciflora mauldinensis gen. et sp. nov. flower from the Late Cretaceous (earliest Cenomanian)
Mauldin Mountain locality, MD, USA; holotype (PP53985; sample Mauldin Mountain 116). (a) Detail of perianth in transverse section below the apex of the
flower bud showing the thicker sepals with a layer of thin-walled hypodermal cells (asterisks), thin lamina of a folded petal with an almost glabrous inner surface
and a dense indumentum on the outer surface; note the especially clear stellate hair (arrowhead) on the keel of the outer surface of the petal (orthoslice xy1200).
(b) Detail of perianth in transverse section close to the apex of the floral bud showing folded petal with dense indumentum on the outer surface and scattered hairs
on the inner surface (arrowhead) (orthoslice xy1050). (c) Longitudinal sections of sepals (s) and petals ( p) showing dense indumentum; note sepals with dense,
infilled cells towards the outside, and a layer of thin-walled hypodermal cells (asterisks) (orthoslice xz1485). (d ) Detail of perianth and androecium in transverse
section close to the rim of the floral cup showing sepals (s) with dense indumentum of stellate hairs on the outer surface and sepal margins (arrowhead), narrow
base of petal ( p, arrow) and an antepetalous anther (an, arrow) (orthoslice xy1900). (e) Detail of sepal (s) showing glabrous inner surface and dense indumentum of
stellate hairs on the outer surface and sepal margins; note thin-walled cells on the inner surface of the sepal (asterisk) (orthoslice xy1950).
stamens. However, the bud is unusual in having carpels that
appear partly open, with no signs of ovule initiation. It is
therefore possible that the flower was functionally unisexual,
and that only stamens developed to maturity. Alternatively,
ovule development may have been interrupted by insect
damage. There are burrows in the bud and an insect larva
is present between the bract and sepals.
The flower and the associated bract and two prophylls are
borne on a short, stout stalk (figures 1a and 2h,i). There is no
other information about how the flower was borne on the
plant. The flower bud is about 1.32 mm long and 0.75 mm in
diameter, and has both staminate and pistillate organs preserved.
There is also a distinct floral cup, about 0.17 mm deep and about
0.3 mm in diameter. The anthetic flower (figure 4a) is similar in
size, about 1.2 mm in diameter, somewhat compressed and
with fully formed staminate and pistillate organs.
The perianth is differentiated into an outer whorl of sepals
and an inner whorl of petals. Sepal aestivation is revolutevalvate (figures 1a–c, 2a–f and 4a) and sepals have broad
bases and acute apices. The post-anthetic flower fragments
show that the sepals are persistent. On their ventral surface,
the sepals have a conspicuous hypodermis of thin-walled,
empty cells. This hypodermis is two to several cell layers
thick in the median-basal region, but only one cell layer thick
distally and along the sepal margins (figure 3a,c–e). Hypodermal cells on the dorsal surface of the sepals are distinctly
different with amorphous contents that obscure the anatomical
details of the sepal lamina, including the number of vascular
bundles. The amorphous contents may indicate that these
cells were mucilaginous or perhaps tanniferous (figure 3a,c–e).
Petals are present in the floral bud and in the specimen preserved at anthesis, but not in the post-anthetic specimens.
Petals do not have a distinct claw, but broaden distally from
a narrow base into a broad, keeled lamina with a prominent
median rib and a single vascular bundle (figure 4d). Petals
are folded longitudinally over the midrib and at least the
inner petals appear conduplicate (figure 3a,b). The petals are
narrow at the base, and widely separated by large interspaces.
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Figure 4. SEM (a–c, e– g, i–l ) and SRXTM (d, h) images of carpels, ovules/seeds, stamens and pollen of Caliciflora mauldinensis gen. et sp. nov. from the Late Cretaceous (earliest Cenomanian) Mauldin Mountain locality, MD, USA. (a) Anthetic specimen in apical view showing five sepals, remnants of a keeled petal (arrow), six stamens
and three carpels (PP34773, sample Mauldin Mountain 116). (b,c) Fragment of post-anthetic specimen in apical view (b) showing remains of three carpels (ca) and three
elongated, anatropous, reticulate ovules/seeds (arrowhead) in the most complete carpel; note also remains of the slightly bulging margins of the two other carpels
(arrows) (PP54159; sample Mauldin Mountain 117). (d) Surface rendering of adaxial surface of petal from specimen in figures 1–3 showing the gradual expansion
of the thin petal lamina from the base and the distinct groove, which corresponds to the keel on the abaxial surface (PP53985; sample Mauldin Mountain 116).
(e,f) Fragment of post-anthetic specimen showing the dense indumentum of stellate hairs on the surface of the sepals (e) and scattered on the papillate surface of
the carpel (f ) (PP54160; sample Mauldin Mountain 022). (g) Detail of the apical portion of an anther from anthetic flower in (a) showing numerous pollen grains
in situ (PP34773, sample Mauldin Mountain 116). (h) Volume rendering of the floral bud cut at level of orthoslice xy1905 to show stamens with filament attached
to dorsal side of the anthers (arrow heads) (PP53985; sample Mauldin Mountain 116). (i–l ) Pollen grains are psilate to weakly regulate with three long colpi that
reach almost to the pole; a narrow raised area (bridge) is seen at the middle of the colpi (arrows): note tiny, spherical orbicules (arrowheads) with a central depression
adhering to the inner surface of the thecae and pollen grains (PP54161; sample Mauldin Mountain 022).
Petal aestivation is open at the base (figures 2d and 3d), but
quincuncial above (figures 2b,c and 3a,b).
The androecium consists of two whorls of stamens.
Anthers are almost sessile in the bud and filaments are also
short in both of the more mature specimens (PP34773,
PP54161). In the floral bud, the three stamens that are opposite
the sepals (antesepalous) are borne on the rim of the floral cup.
Five stamens opposite the petals (antepetalous) are borne
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(a) Systematic assessment
The combination of characters in Caliciflora, including the
actinomorphic organization with an open floral cup, pentamerous whorls of free sepals and petals, two whorls of free
stamens, tricolporate and tectate-imperforate pollen, one
whorl of three free carpels and follicular fruitlets, unequivocally place the fossil taxon among core eudicots. In
addition, while flowers with a floral cup, together with free
petals (choripetalous) and an apocarpous gynoecium, are
found in several groups of rosids, to our knowledge this combination of features is not recorded among asterids or in any
other group of core eudicots.
Resolving the phylogenetic position of Caliciflora among
extant rosids is complicated by the vast number of living species
(around 70 000 extant species, [17]), many of which have not
been studied in detail, combined with the absence of clear morphological synapomorphies that correspond to the higher level
groupings, orders and families recognized based largely on
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4. Discussion
molecular data (e.g. [17–24]). A further problem is that floral
morphology among rosids exhibits considerable variation, and
sometimes there are strong similarities in unusual features
between taxa that are widely separated phylogenetically (e.g.
flowers of Anisophyllea (Anisophylleaceae, Cucurbitales: fabids)
and Ceratopetalum (Cunoniaceae, Oxalidales: COM)) [25]. These
difficulties, coupled with uncertainties over deep relationships
in the rosids, complicate characterization of major clades using
flower morphology [22,26–28] and there are no recent comprehensive attempts to evaluate the evolution of floral characters
in the group as a whole. We therefore compare Caliciflora to
extant rosids only in general terms based on the extensive literature, as well as the few discussions of floral structure that have
taken into account new molecular models of angiosperm
relationships (e.g. [25,26,28–41]).
One of the most distinctive characters of Caliciflora is the
floral cup, which is also characteristic of many rosids, where
it occurs scattered in three major clades (N-fixing clade, COM
clade and malvids), as well as in Myrtales [28,42–45] and
Crossomostomatales [33]. In the N-fixing clade, a floral cup is
present in certain Rosales [40,41] and Cucurbitales [31], while
in the COM clade, it occurs in Celastrales [32], Oxalidales
[30] and Malpighiales [29,35–37,46]. Among malvids, a floral
cup occurs in certain Brassicales [47], Huerteales [28] and
Sapindales [48,49]. Actinomorphic flowers with free perianth
parts are also characteristic of many rosids, and typically
such flowers are pentamerous with a well-differentiated
calyx and corolla as in Caliciflora. The revolute-valvate sepal
aestivation of Caliciflora is also a feature of certain rosids and
occurs scattered in the Cucurbitales (Anisophylleaceae, [31]),
Malpighiales (Rhizophoraceae and Erythroxylaceae, [36]) and
also in Oxalidales (Cunoniaceae and Tremandraceae, [30]).
A characteristic feature of many rosids is flowers with
the same number of floral organs in all whorls (isomerous)
including the gynoecial whorl. However, monocarpellate,
bicarpellate and tricarpellate forms often occur in typically isomerous groups, and some groups of rosids, for example, many
Malpighiales [46] are characterized by heteromerous flowers
with one to three carpels. Also common in several groups of
rosids is apocarpy and in the N-fixing clade it occurs in certain
Rosaceae, as well as Surianaceae and Quillajaceae (both fabids).
In Rosaceae, dry, follicular fruitlets with several seeds borne
centrally on ventral placentae, as well as open ventral sutures,
are known in some members of subfamily Amygdaloideae [50].
The androecial features of Caliciflora are less informative
systematically, but are also consistent with the androecial structure of some members of the N-fixing clade. For example, while
most flowers of Rosaceae have 15 or more stamens, flowers
with fewer stamens occur in the North American cushion
plant, Kelseya uniflora (S. Wats.) Rydb. [51]. Reduction of
stamen number in one of the stamen whorls, as seen in the
Caliciflora flower bud, occurs also in Surianaceae (Fabales).
Pollen morphology among rosids is diverse, but small, tricolporate grains similar to those of Caliciflora are common in
many taxa. Often the tectum is reticulate, microreticulate or
foveolate, but grains with a finely rugulate tectum as in
Caliciflora occur in many taxa in the N-fixing clade, including
in Fabaceae (e.g. [52–55]), Surianaceae and Quillajaceae [56],
and Rosaceae (e.g. [57,58]).
The stellate hairs of Caliciflora are distinctive. Similar hairs
occur on the outer surface of sepals and petals in Rhizophoraceae, and in the closely related Ctenolophonaceae [36], as well
as on the outer surface of the sepals in some Cunoniaceae and
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slightly below this level (figure 2c–e,h,i). Anthers are tetrasporangiate, dithecal and dorsifixed (figure 4a,h). They are
very small, up to about 0.15 mm long in the bud and about
0.4 mm long in the anthetic flower. Pollen grains are not
obvious in the flower bud. Anthers in two of the more
mature specimens have abundant minute pollen grains,
about 10 mm long and 5 mm in equatorial diameter. Grains
are prolate-rhomboidal in equatorial view (figure 4i,k,l ) and
semi-angular in polar view (figure 4j). Pollen grains have
three long colpi, each with a small bridge in the middle of
the colpi (figure 4i,k,l ) indicating that the grains are tricolporate. The tectum is psilate-imperforate with weakly rugulate
ornamentation. Tiny, rounded orbicules, about 1 mm in diameter, often with a small central depression, occur on the inside
of the theca wall and the surface of the pollen grains
(figure 4i,k), most probably indicating a secretory tapetum.
The three free carpels (figures 2c–i and 4a,h) are borne on
the inside of the floral cup above the free space of the floral
apex. In the flower bud, the carpels are fully open along
the ventral suture below the stigmatic region (figure 2c– g).
In this specimen, no ovules are developed and there is no
indication of placentation. However, in the more mature
specimens (figure 4b,c) placentation is ventral and apparently
concentrated to the middle part of each carpel.
Ovules/seeds are exposed in one mature carpel
(figure 4b,c). They are small, elongated, anatropous, with a reticulate outer surface, and do not fill out the locule. The fruitlets
are dry follicles that open along their ventral sutures. The inner
part of the fruit wall consists of transversely oriented fibrous
sclereids. The outer epidermis of the fruit wall consists of
equiaxial cells, each with a central papilla (figure 4f ); no stomata have been observed on the carpel or fruit wall.
The outer surface of sepals and petals, as well as the outer
surface of the floral cup is covered by a dense indumentum
of interlocking stellate hairs each composed of up to about 10
long unicellular elements that radiate from a central point
(figures 1a–e, 2a–i, 3a–e and 4e). Scattered stellate hairs also
occur along the margins of the sepals (figure 3d) and on the
inner surface of the petals in the apical region (figures 2i and
3b,c). The inner surface of the sepals and the median and
basal parts of the petals are glabrous (figure 3a,c–e).
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Tremandraceae [30,59]. In flower buds of Rhizophoraceae and
Ctenolophonaceae, the perianth parts are congenitally connected by the hairs in the overlapping regions [36], which
also appears to be the case for Caliciflora. Congenital connection
of sepals by hairs is also reported for Cunoniaceae [30]. Stellate
hairs similar to those of Caliciflora are not widespread in
Rosaceae, but occur in a few taxa (e.g. Sorbaria) [60].
(b) Implications for the origin of core eudicots
Caliciflora mauldinensis from the earliest Cenomanian, very
close to the Early–Late Cretaceous boundary, establishes a
minimum age of about 100 Myr for the origin of core eudicots.
Setting aside the report of a rosid flower from Burmese amber
[61], the age of which is uncertain ( possibly Cenomanian), the
only other mid-Cretaceous core eudicot flower currently
known from around the Early–Late Cretaceous boundary is
the Rose Creek flower reported from the Dakota Formation
[10], which is of broadly similar age, or perhaps very slightly
older [62]. While Caliciflora and the Rose Creek flower differ
dramatically in size, their floral architecture is fundamentally
similar. Both are regular actinomorphic and bisexual flowers
with whorled, pentamerous organization and free floral parts
(figure 5a,b), a prerequisite for the development of more integrated patterns of floral architecture [63] that accompanied
the rapid diversification of core eudicots through the Late
Cretaceous and Cenozoic [1,64].
Subsequent to the earliest Cenomanian there are only few
fossil floras of Late Cenomanian or Turonian age. Currently no
core eudicot flowers have been described from the Late Cenomanian flora of the Bohemian Basin [65–67] or from the
Cenomanian–Turonian Sarbay flora [68,69]. The mesofossil
flora from Old Crossman Clay Pit of possible Turonian age (e.g.
[8,70]) does contain abundant flowers of core eudicots. However,
the Old Crossman flora is very similar in many respects to
younger mesofossil floras from the Santonian–Campanian of
North America [1]. The interval between the first appearance of
early core eudicot flowers (Caliciflora, Rose Creek flower) and
later flowers with more pronounced synorganization (e.g. Raritaniflora tomentosa Crepet, Nixon & Daghlian) is therefore a
minimum of about 10, or possibly as much 15–20 Myr.
The Late Cretaceous record of both mesofossils and palynofloras both suggest an extensive post-Cenomanian radiation of
core eudicot angiosperms [1,71,72]. However, at the level of
Caliciflora and the Rose Creek flower, and also in older sediments, all other angiosperms that are known so far appear to
be related to early diverging lineages of angiosperms [1],
including early diverging lineages of eudicots (taxa related to
Lardizabalaceae and other members of Ranunculales, Buxales,
Platanaceae and Nelumbonaceae [1,3,73]). Similarly, among
the 21 species of fossil leaves reported from the Rose Creek
locality, 70% of the leaf species and 90% of the leaf specimens
appear to be related to magnoliids or magnoliid grade angiosperms [74]. Four species were unassigned. Only two species
were assigned to core eudicots [74].
5. Conclusion
The characters of Caliciflora unequivocally place this new fossil
angiosperm flower among core eudicots, most likely among
the rosids rather than asterids, perhaps near the base of the
N-fixing clade. Flowers with a floral cup, heteromerous organization, tricolporate, rugulate-tectate pollen and an apocarpous
gynoecium are common at this level of angiosperm evolution,
including in certain Rosaceae, and also in the fabalean family
Surianaceae. More precise systematic placement is precluded
by incomplete knowledge of floral structure over a very large
number of extant species as well as problems of defining the
currently recognized rosid lineages based on floral features
alone. Caliciflora and the Rose Creek flower establish a minimum age for core eudicots that is broadly in agreement with
ideas based on molecular data that suggest a major radiation
of core eudicots in the mid-Cretaceous [17,75–77]. However,
hypotheses suggesting that a significant diversification of
core eudicots was already underway in the Early Cretaceous
[78] are more problematic. Direct fossil evidence of core eudicots prior to around the Early Cretaceous–Late Cretaceous is
currently lacking.
Data accessibility. The specimens are housed in the palaeobotanical collections of the Field Museum of Natural History, Chicago, USA (PP). Raw
data from the SRXTM study are stored at the Swedish Museum of
Natural History, Stockholm, Sweden (raw data PP53985a_B1_B2_).
Competing interests. We declare we have no competing interests.
Funding. Financial support was provided by the Swiss Light Source
(European Union FP6 projects 20130185), by the Swedish Research
Council and by the Edward P. Bass Distinguished Visiting Fellowship
at Yale University.
Acknowledgements. We thank Marco Stampanoni, Federica Marone and
Anna Lindström for help with the SRXTM analyses performed at the
Swiss Light Source, Paul Scherrer Institute, Villigen, Switzerland, and
Pollyanna von Knorring for the linedrawings.
Proc. R. Soc. B 283: 20161325
Figure 5. Floral diagrams of Caliciflora mauldinensis gen. et sp. nov. from the Late Cretaceous (earliest Cenomanian) Mauldin Mountain locality, MD, USA (a) and
the Rose Creek Flower [10] from the latest Early Cretaceous or earliest Late Cretaceous (latest Albian – earliest Cenomanian) Rose Creek locality, NE, USA (b).
Downloaded from http://rspb.royalsocietypublishing.org/ on December 22, 2016
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